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Marine Biology

, 164:193 | Cite as

In situ common garden assays demonstrate increased defense against natural fouling in non-native populations of the red seaweed Gracilaria vermiculophylla

  • Shasha Wang
  • Florian Weinberger
  • Luyang Xiao
  • Masahiro Nakaoka
  • Gaoge Wang
  • Stacy A. Krueger-Hadfield
  • Erik E. Sotka
  • Dapeng Bian
  • Mark Lenz
Original paper

Abstract

The susceptibility of native and non-native populations of the red alga Gracilaria vermiculophylla to fouling was compared in common garden experiments. Native and non-native algae were enclosed into dialysis membrane tubes, and the tubes were exposed to natural fouling. Fouling on the outside of the tubes was mediated by chemical compounds excreted by G. vermiculophylla that diffused through the membranes. Fouling pressure was significantly higher in the Kiel Fjord (non-native range) than in Akkeshi Bay (native range), but, at both sites, tubes containing non-native G. vermiculophylla were less fouled than those with native conspecifics. This is the first in situ evidence that susceptibility to fouling differs between native and non-native populations of an aquatic organism. The technique of enclosing organisms into dialysis tubes represents a simple, efficient and accurate way to test chemical antifouling defenses and could possibly be applied to other organisms.

Notes

Acknowledgements

S. Wang was supported by a scholarship from the China Scholarship Council (CSC) at GEOMAR—Helmholtz-Zentrum für Ozeanforschung in Kiel. We would like to thank Prof. Dr. Martin Wahl for his valuable support and technical advices for experimental design. We are thankful to Renate Schütt for her great help in epibionts identification and to Nadja Stärck for her technical advices and help with field work preparation. We are very grateful to Dr. Inken Kruse, Dr. Takehisa Yamakita, Haruka Yamaguchi and Carola Schuller for collecting and sending algal samples. We acknowledge: NSF BIO-OCE-1357386.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Funding

This study was funded by the China Scholarship Council (CSC) (Number 201206330050).

Ethical approval

All applicable international, national and/or institutional guidelines for the care and use of animals were followed.

Data accessibility

All experimental data underlying this publication are available from the PANGAEA repository (doi: https://doi.pangaea.de/10.1594/PANGAEA.865280).

Supplementary material

227_2017_3226_MOESM1_ESM.pdf (161 kb)
Supplementary material 1 (PDF 161 kb)

References

  1. Bach CE, Hazlett BA, Rittschof D (2006) Sex-specific differences and the role of predation in the interaction between the hermit crab, Pagurus longicarpus, and its epibiont, Hydractinia symbiolongicarpus. J Exp Mar Biol Ecol 333:181–189. doi: 10.1016/j.jembe.2005.12.003 CrossRefGoogle Scholar
  2. Bellorin AM, Oliveira MC, Oliveira EC (2004) Gracilaria vermiculophylla: a western Pacific species of Gracilariaceae (Rhodophyta) first recorded from the eastern Pacific. Phycol Res 52:69–79. doi: 10.1111/j.1440-1835.2004.tb00317.x CrossRefGoogle Scholar
  3. Blossey B, Nötzold R (1995) Evolution of increased competitive ability in invasive nonindigenous plants: a hypothesis. J Ecol 83:887–889. doi: 10.2307/2261425 CrossRefGoogle Scholar
  4. Buschbaum C, Buschbaum G, Schrey I, Thieltges DW (2007) Shell-boring polychaetes affect gastropod shell strength and crab predation. Mar Ecol Prog Ser 329:123–130. doi: 10.3354/meps329123 CrossRefGoogle Scholar
  5. Buschmann AH, Gómez P (1993) Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes. Hydrobiologia 261:345–351CrossRefGoogle Scholar
  6. Cacabelos E, Olabarria C, Incera M, Troncoso JS (2010) Do grazers prefer invasive seaweeds? J Exp Mar Biol Ecol 393:182–187CrossRefGoogle Scholar
  7. Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443CrossRefGoogle Scholar
  8. 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
  9. Costerton JW, Cheng KJ, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Annu Rev Microbiol 41:435–464CrossRefGoogle Scholar
  10. Crimaldi JP, Thompson JK, Rosman JH, Lowe RJ, Koseff JR (2002) Hydrodynamics of larval settlement: the influence of turbulent stress events at potential recruitment sites. Limnol Oceanogr 47:1137–1151CrossRefGoogle Scholar
  11. da Gama BAP, Plouguerné E, Pereira RC (2014) The antifouling defence mechanisms of marine macroalgae. In: Bourgougnon N (ed) Advances in botanical research. Academic Press, Oxford, pp 413–440Google Scholar
  12. Freshwater DW, Montgomery F, Greene JK, Hamner RM, Williams M, Whitfield PE (2006) Distribution and identification of an invasive Gracilaria species that is hampering commercial fishing operations in southeastern North Carolina, USA. Biol Invasions 8:631–637. doi: 10.1007/s10530-005-1809-5 CrossRefGoogle Scholar
  13. Guillemin ML, Akki SA, Givernaud T, Mouradi A, Valero M, Destombe C (2008) Molecular characterisation and development of rapid molecular methods to identify species of Gracilariaceae from the Atlantic coast of Morocco. Aquat Bot 89:324–330. doi: 10.1016/j.aquabot.2008.03.008 CrossRefGoogle Scholar
  14. Hammann M, Wang GG, Rickert E, Boo SM, Weinberger F (2013) Invasion success of the seaweed Gracilaria vermiculophylla correlates with low palatability. Mar Ecol Prog Ser 486:93–103. doi: 10.3354/meps10361 CrossRefGoogle Scholar
  15. Hammann M, Rempt M, Pohnert G, Wang G, Boo SM, Weinberger F (2016a) Increased potential for wound activated production of Prostaglandin E-2 and related toxic compounds in non-native populations of Gracilaria vermiculophylla. Harmful Algae 51:81–88. doi: 10.1016/j.hal.2015.11.009 CrossRefGoogle Scholar
  16. Hammann M, Wang GG, Boo SM, Aguilar-Rosas LE, Weinberger F (2016b) Selection of heat-shock resistance traits during the invasion of the seaweed Gracilaria vermiculophylla. Mar Biol 163:104. doi: 10.1007/s00227-016-2881-3 CrossRefGoogle Scholar
  17. Hemmi A, Mäkinen A, Jormalainen V, Honkanen T (2005) Responses of growth and phlorotannins in Fucus vesiculosus to nutrient enrichment and herbivory. Aquat Ecol 39:201–211CrossRefGoogle Scholar
  18. Honkanen T, Jormalainen V (2005) Genotypic variation in tolerance and resistance to fouling in the brown alga Facus vesiculosus. Oecologia 144:196–205. doi: 10.1007/00442-005-0053-0 CrossRefGoogle Scholar
  19. Johnson CR, Chapman ARO (2007) Seaweed invasions: introduction and scope. Bot Mar 50:321–325. doi: 10.1515/bot.2007.037 Google Scholar
  20. Keane RM, Crawley MJ (2002) Exotic plant invasions and the enemy release hypothesis. Trends Ecol Evol 17:164–170CrossRefGoogle Scholar
  21. Koehl MAR, Crimaldi JP, Dombroski DE (2013) Wind chop and ship wakes determine hydrodynamic stresses on larvae settling on different microhabitats in fouling communities. Mar Ecol Prog Ser 479:47–62. doi: 10.3354/meps10193 CrossRefGoogle Scholar
  22. Korpinen S, Honkanen T, Vesakoski O, Hemmi A, Koivikko R, Loponen J, Jormalainen V (2007) Macroalgal communities face the challenge of changing biotic interactions: review with focus on the Baltic Sea. Ambio 36:203–211. doi:10.1579/0044-7447(2007)36[203:mcftco]2.0.co;2Google Scholar
  23. Krueger-Hadfield SA, Kollars NM, Byers JE, Greig TW, Hammann M, Murray DC, Murren CJ, Strand AE, Terada R, Weinberger F, Sotka EE (2016) Invasion of novel habitats uncouples haplo-diplontic life cycles. Mol Ecol 25:3801–3816. doi: 10.1111/mec.13718 CrossRefGoogle Scholar
  24. Lake JC, Leishman MR (2004) Invasion success of exotic in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117:215–226. doi: 10.1016/s0006-3207(03)00294-5 CrossRefGoogle Scholar
  25. Leonardi PI, Miravalles AB, Faugeron S, Flores V, Beltrán J, Correa JA (2006) Diversity, phenomenology and epidemiology of epiphytism in farmed Gracilaria chilensis (Rhodophyta) in northern Chile. Eur J Phycol 41:247–257. doi: 10.1080/09670260600645659 CrossRefGoogle Scholar
  26. Lion U, Wiesemeier T, Weinberger F, Beltrán J, Flores V, Faugeron S, Correa J, Pohnert G (2006) Phospholipases and galactolipases trigger oxylipin-mediated wound-activated defence in the red alga Gracilaria chilensis against epiphytes. ChemBioChem 7:457–462. doi: 10.1002/cbic.200500365 CrossRefGoogle Scholar
  27. Lubchenco J, Olson AM, Brubaker LB, Carpenter SR, Holland MM, Hubbell SP, Levin SA, Macmahon JA, Matson PA, Melillo JM, Mooney HA, Peterson CH, Pulliam HR, Real LA, Regal PJ, Risser PG (1991) The sustainable biosphere initiative: an ecological research agenda: a report from the Ecological Society of America. Ecology 72:371–412. doi: 10.2307/2937183 CrossRefGoogle Scholar
  28. Nejrup LB, Pedersen MF (2012) The effect of temporal variability in salinity on the invasive red alga Gracilaria vermiculophylla. Eur J Phycol 47:254–263. doi: 10.1080/09670262.2012.702225 CrossRefGoogle Scholar
  29. Nyberg CD, Wallentinus I (2009) Long-term survival of an introduced red alga in adverse conditions. Mar Biol Res 5:304–308. doi: 10.1080/17451000802428159 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. Paul NA, de Nys R, Steinberg PD (2006a) Chemical defence against bacteria in the red alga Asparagopsis armata: linking structure with function. Mar Ecol Prog Ser 306:87–101. doi: 10.3354/meps306087 CrossRefGoogle Scholar
  32. Paul NA, de Nys R, Steinberg PD (2006b) Seaweed-herbivore interactions at a small scale: direct tests of feeding deterrence by filamentous algae. Mar Ecol Prog Ser 323:1–9. doi: 10.3354/meps323001 CrossRefGoogle Scholar
  33. Rempt M, Weinberger F, Grosser K, Pohnert G (2012) Conserved and species-specific oxylipin pathways in the wound-activated chemical defense of the noninvasive red alga Gracilaria chilensis and the invasive Gracilaria vermiculophylla. Beilstein J Org Chem 8:283–289. doi: 10.3762/bjoc.8.30 CrossRefGoogle Scholar
  34. Rickert E, Karsten U, Pohnert G, Wahl M (2015) Seasonal fluctuations in chemical defenses against macrofouling in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Biofouling 31:363–377. doi: 10.1080/08927014.2015.1041020 CrossRefGoogle Scholar
  35. Rickert E, Lenz M, Barboza FR, Gorb SN, Wahl M (2016) Seasonally fluctuating chemical microfouling control in Fucus vesiculosus and Fucus serratus from the Baltic Sea. Mar Biol 163:203CrossRefGoogle Scholar
  36. Roleda MY, Nyberg CD, Wulff A (2012) UVR defense mechanisms in eurytopic and invasive Gracilaria vermiculophylla (Gracilariales, Rhodophyta). Physiol Plant 146:205–216. doi: 10.1111/j.1399-3054.2012.01615.x CrossRefGoogle Scholar
  37. Saha M, Wahl M (2013) Seasonal variation in the antifouling defence of the temperate brown alga Fucus vesiculosus. Biofouling 29:661–668. doi: 10.1080/08927014.2013.795953 CrossRefGoogle Scholar
  38. Saha M, Wiese J, Weinberger F, Wahl M (2016) Rapid adaptation to controlling new microbial epibionts in the invaded range promotes invasiveness of an exotic seaweed. J Ecol 104:969–978. doi: 10.1111/1365-2745.12590 CrossRefGoogle Scholar
  39. Saunders GW (2009) Routine DNA barcoding of Canadian Gracilariales (Rhodophyta) reveals the invasive species Gracilaria vermiculophylla in British Columbia. Mol Ecol Resour 9:140–150. doi: 10.1111/j.1755-0998.2009.02639.x CrossRefGoogle Scholar
  40. 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
  41. Sfriso A, Maistro S, Andreoli C, Moro I (2010) First record of Gracilaria vermiculophylla (Gracilariales, Rhodophyta) in the po delta lagoons, Mediterranean sea (Italy). J Phycol 46:1024–1027. doi: 10.1111/j.1529-8817.2010.00893.x CrossRefGoogle Scholar
  42. Spalding MD, Fox HE, Halpern BS, McManus MA, Molnar J, Allen GR, Davidson N, Jorge ZA, Lombana AL, Lourie SA, Martin KD, McManus E, Molnar J, Recchia CA, Robertson J (2007) Marine ecoregions of the world: a bioregionalization of coastal and shelf areas. Bioscience 57:573–583. doi: 10.1641/b570707 CrossRefGoogle Scholar
  43. Stastny M, Schaffner U, Elle E (2005) Do vigour of introduced populations and escape from specialist herbivores contribute to invasiveness? J Ecol 93:27–37. doi: 10.1111/j.1365-2745.2004.00962.x CrossRefGoogle Scholar
  44. Streftaris N, Zenetos A, Papathanassiou E (2005) Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanogr Mar Biol 43:419–453Google Scholar
  45. Strong JA, Maggs CA, Johnson MP (2009) The extent of grazing release from epiphytism for Sargassum muticum (Phaeophyceae) within the invaded range. J Mar Biol Assoc UK 89:303–314. doi: 10.1017/s0025315408003226 CrossRefGoogle Scholar
  46. Svensson JR, Nylund GM, Cervin G, Toth GB, Pavia H (2013) Novel chemical weapon of an exotic macroalga inhibits recruitment of native competitors in the invaded range. J Ecol 101:140–148. doi: 10.1111/1365-2745.12028 CrossRefGoogle Scholar
  47. Thevanathan R, Nirmala M, Manoharan A, Gangadharan A, Rajarajan R, Dhamothrarn R, Selvaraj S (2000) On the occurrence of nitrogen fixing bacteria as epibacterial flora of some marine green algae. Seaweed Res Utiln 22:189–197Google Scholar
  48. Thomsen MS, McGlathery KJ, Tyler AC (2006) Macroalgal distribution patterns in a shallow, soft-bottom lagoon, with emphasis on the nonnative Gracilaria vermiculophylla and Coldium fragile. Estuar Coast 29:465–473CrossRefGoogle Scholar
  49. Tseng CK, Xia BM (1999) On the Gracilaria in the Western Pacific and the southeastern Asia region. Bot Mar 42:209–217. doi: 10.1515/bot.1999.024 CrossRefGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. Vitousek PM, Dantonio CM, Loope LL, Westbrooks R (1996) Biological invasions as global environmental change. Am Sci 84:468–478Google Scholar
  52. Wahl M (1989) Marine epibiosis. I. Fouling and antifouling: some basic aspects. Mar Ecol Prog Ser 58:175–189CrossRefGoogle Scholar
  53. Wahl M (2008) Ecological lever and interface ecology: epibiosis modulates the interactions between host and environment. Biofouling 24:427–438CrossRefGoogle Scholar
  54. Wahl M, Mark O (1999) The predominantly facultative nature of epibiosis: experimental and observational evidence. Mar Ecol Prog Ser 187:59–66CrossRefGoogle Scholar
  55. Wang S, Wang G, Weinberger F, Bian D, Nakaoka M, Lenz M (2016) Anti-epiphyte defences in the red seaweed Gracilaria vermiculophylla: non-native algae are better defended than their native conspecifics. J Ecol. doi: 10.1111/1365-2745.12694 Google Scholar
  56. 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 CrossRefGoogle Scholar
  57. Wikström SA, Steinarsdóttir MB, Kautsky L, Pavia H (2006) Increased chemical resistance explains low herbivore colonization of introduced seaweed. Oecologia 148:593–601. doi: 10.1007/s00442-006-0407-2 CrossRefGoogle Scholar
  58. 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
  59. Yamamoto K, Endo H, Yoshikawa S, Ohki K, Kamiya M (2013) Various defense ability of four sargassacean algae against the red algal epiphyte Neosiphonia harveyi in Wakasa Bay, Japan. Aquat Bot 105:11–17. doi: 10.1016/j.aquabot.2012.10.008 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Benthic Ecology, GEOMAR Helmholtz Centre for Ocean Research KielKielGermany
  2. 2.Weihai Changqing Ocean Science and Technology Co., Ltd.RongchengChina
  3. 3.Akkeshi Marine Station, Field Science Center for Northern BiosphereHokkaido UniversityHokkaidoJapan
  4. 4.College of Marine Life SciencesOcean University of ChinaQingdaoChina
  5. 5.Institute of Evolution and Marine BiodiversityOcean University of ChinaQingdaoChina
  6. 6.Department of BiologyUniversity of Alabama at BirminghamBirminghamUSA
  7. 7.Grice Marine Laboratory and the Department of BiologyCollege of CharlestonCharlestonUSA

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