Marine Biology

, 164:185 | Cite as

When the tiny help the mighty: facilitation between two introduced species, a solitary ascidian and a macroalga in northern Patagonia, Argentina

  • Patricio Javier PereyraEmail author
  • Paula de la Barra
  • Marianela Gastaldi
  • Juan Francisco Saad
  • Fausto Nahuel Firstater
  • Maite Andrea Narvarte


Facilitation is recognized as one of the mechanisms by which nonnative species are integrated into new assemblages. The solitary ascidian Styela clava and the macroalga Undaria pinnatifida were introduced to San Antonio Bay, Argentina, with a couple of years of difference. We studied the occurrence pattern of both species in the area and tested the hypothesis that S. clava facilitates U. pinnatifida through a manipulative experiment. Our results clearly suggest a facilitation process between these species. The probability of finding U. pinnatifida is 30% higher in sites where S. clava is present and higher recruitment of U. pinnatifida occurred where S. clava is present than where it had been experimentally removed. Increased habitat complexity by the stalked ascidian S. clava can facilitate the establishment of U. pinnatifida by providing refugee from grazers, increasing surface for settlement, or providing greater access to light.



PJP, MG and JFS were supported by a postdoctoral scholarship granted by CONICET and PB was supported by a doctoral scolarship granted by CONICET, Argentina. This project was partially supported by the Agencia Nacional de Promoción Científica y Tecnológica (ANPCyT, Grant PICT CONAE-CONICET No. 04/2010 to MN). Matías Mancuso provided useful help in the field. Two anonymous reviewers helped to improve the manuscript.

Compliance with ethical standards

Conflict of interest

We declare that we have no conflict of interest. All the authors consented and agreed to carry out this research. All animals have been sampled and treated according to the national legislation. All permission to work in our study area were obtained prior the start of the experiments.


  1. Bertness MD, Callaway R (1994) Positive interactions in communities. Trends Ecol Evol 9:191–193. doi: 10.1016/0169-5347(94)90088-4 CrossRefGoogle Scholar
  2. Bracken MES (2004) Invertebrate-mediated nutrient loading increases growth of an intertidal macroalga1. J Phycol 40:1032–1041. doi: 10.1111/j.1529-8817.2004.03106.x CrossRefGoogle Scholar
  3. Bracken MES, Gonzalez-Dorantes CA, Stachowicz JJ (2007) Whole-community mutualism: associated invertebrates facilitate a dominant habitat-forming seaweed. Ecology 88:2211–2219. doi: 10.1890/06-0881.1 CrossRefGoogle Scholar
  4. Bruno JF, Stachowicz JJ, Bertness MD (2003) Inclusion of facilitation into ecological theory. Trends Ecol Evol 18:119–125. doi: 10.1016/S0169-5347(02)00045-9 CrossRefGoogle Scholar
  5. Bulleri F (2009) Facilitation research in marine systems: state of the art, emerging patterns and insights for future developments. J Ecol 97:1121–1130. doi: 10.1111/j.1365-2745.2009.01567.x CrossRefGoogle Scholar
  6. Bulleri F, Benedetti-Cecchi L (2008) Facilitation of the introduced green alga Caulerpa racemosa by resident algal turfs: experimental evaluation of underlying mechanisms. Mar Ecol Prog Ser 364:77–86. doi: 10.3354/meps07484 CrossRefGoogle Scholar
  7. Burnham KP, Anderson DR, Burnham KP (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New YorkGoogle Scholar
  8. Casas G, Scrosati R, Piriz ML (2004) The invasive kelp Undaria pinnatifida (Phaeophyceae, Laminariales) reduces native seaweed diversity in Nuevo Gulf (Patagonia, Argentina). Biol Invasions 6:411–416. doi: 10.1023/B:BINV.0000041555.29305.41 CrossRefGoogle Scholar
  9. Casas GN, Piriz ML, Parodi ER (2008) Population features of the invasive kelp Undaria pinnatifida (Phaeophyceae: Laminariales) in Nuevo Gulf (Patagonia, Argentina). J Mar Biol Assoc U K 88:21–28. doi: 10.1017/S0025315408000246 CrossRefGoogle Scholar
  10. Castilla JC, Lagos NA, Cerda M (2004) Marine ecosystem engineering by the alien ascidian Pyura praeputialis on a mid-intertidal rocky shore. Mar Ecol Prog Ser 268:119–130. doi: 10.3354/meps268119 CrossRefGoogle Scholar
  11. Castro K, Epherra L, Raffo MP, Rubilar T (2015) Importancia relativa del alga invasora Undaria pinnatifida en la dieta del erizo de mar Arbacia dufresnii: comparación entre ambientes con diferentes estadios de invasión. Dissertation, IX Jornadas Nacionales de Ciencias del MarGoogle Scholar
  12. Claar DC, Edwards KF, Stachowicz JJ (2011) Positive and negative effects of a dominant competitor on the settlement, growth, and survival of competing species in an epibenthic community. J Exp Mar Biol Ecol 399:130–134. doi: 10.1016/j.jembe.2011.02.014 CrossRefGoogle Scholar
  13. Core Team R (2016) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  14. Crawley MJ (2007) The R book. Wiley, ChichesterCrossRefGoogle Scholar
  15. Edwards KF, Stachowicz JJ (2011) Spatially stochastic settlement and the coexistence of benthic marine animals. Ecology 92:1094–1103. doi: 10.1890/10-1332.1 CrossRefGoogle Scholar
  16. Farrell P, Fletcher RL (2006) An investigation of dispersal of the introduced brown alga Undaria pinnatifida (Harvey) Suringar and its competition with some species on the man-made structures of Torquay Marina (Devon, UK). J Exp Mar Biol Ecol 334(2):236–243. doi: 10.3391/bir.2014.3.2.01 CrossRefGoogle Scholar
  17. Gelós EM, Spagnuolo JO, Schillizzi RA, Gómez EA (1994) Textura y mineralogía de los sedimentos de playa entre San Antonio Oeste (Río Negro) y Puerto Lobos (Chubut). Rev Asoc Geol Argent 49:85–92Google Scholar
  18. Goldstien SJ, Dupont L, Viard F, Hallas PJ, Nishikawa T, Schiel DR, Gemmell NJ, Bishop JDD (2011) Global phylogeography of the widely introduced north west pacific ascidian Styela clava. PLoS One 6:e16755. doi: 10.1371/journal.pone.0016755 CrossRefGoogle Scholar
  19. Gutiérrez JL, Jones CG, Strayer DL, Iribarne OO (2003) Mollusks as ecosystem engineers: the role of shell production in aquatic habitats. Oikos 101:79–90. doi: 10.1034/j.1600-0706.2003.12322.x CrossRefGoogle Scholar
  20. Harder T (2008) Marine epibiosis: concepts, ecological consequences and host defense. In: Costerton JW (ed) Marine and industrial biofouling. Springer, Berlin, pp 219–231Google Scholar
  21. Isla FI, Bértola GR, Schnack EJ (2001) Morfodinámica de playas meso y macromareales de Buenos Aires, Río Negro y Chubut. Rev Asoc Argen Sedimentol 8:51–60Google Scholar
  22. Maida M, Coll JC, Sammarco PW (1994) Shedding new light on scleractinian coral recruitment. J Exp Mar Biol Ecol 180:189–202. doi: 10.1016/0022-0981(94)90066-3 CrossRefGoogle Scholar
  23. Martinetto P, Daleo P, Escapa M, Albertia J, Isaccha JP, Fanjula E, Bottoa F, Pirizb ML, Poncec G, Casasb G, Iribarnea O (2010) High abundance and diversity of consumers associated with eutrophic areas in a semi-desert macrotidal coastal ecosystem in Patagonia, Argentina. Estuar Coast Shelf Sci 88:357–364. doi: 10.1016/j.ecss.2010.04.012 CrossRefGoogle Scholar
  24. Martinetto P, Teichberg M, Valiela I, Montemayor D, Iribarne O (2011) Top-down and bottom-up regulation in a high nutrient—high herbivory coastal ecosystem. Mar Ecol Prog Ser 432:69–82. doi: 10.3354/meps09173 CrossRefGoogle Scholar
  25. Monteiro SM, Chapman MG, Underwood AJ (2002) Patches of the ascidian Pyura stolonifera (Heller, 1878): structure of habitat and associated intertidal assemblages. J Exp Mar Biol Ecol 270:171–189. doi: 10.1016/S0022-0981(02)00020-5 CrossRefGoogle Scholar
  26. Morelissen B, Dudley BD, Phillips NE (2016) Recruitment of the invasive kelp Undaria pinnatifida does not always benefit from disturbance to native algal communities in low-intertidal habitats. Mar Biol 163:241. doi: 10.1007/s00227-016-3014-8 CrossRefGoogle Scholar
  27. Pereyra PJ, Narvarte M, Tatián M, González R (2015) The simultaneous introduction of the tunicate Styela clava (Herdman, 1881) and the macroalga Undaria pinnatifida (Harvey) Suringar, 1873, in northern Patagonia. Bio Invasions Rec 4:179–184. doi: 10.3391/bir.2015.4.3.04 Google Scholar
  28. Piriz ML, Casas G (1994) Occurrence of Undaria pinnatifida in Golfo Nuevo, Argentina. Appl Phycol Forum 10:4Google Scholar
  29. Piriz ML, Eyras MC, Rostagno CM (2003) Changes in biomass and botanical composition of beach-cast seaweeds in a disturbed coastal area from Argentine Patagonia. J Appl Phycol 15:67–74. doi: 10.1023/A:1022959005072 CrossRefGoogle Scholar
  30. Rimondino C, Torre L, Sahade R, Tatián M (2015) Sessile macro-epibiotic community of solitary ascidians, ecosystem engineers in soft substrates of Potter Cove, Antarctica. Polar Res 34:1–9. doi: 10.3402/polar.v34.24338 CrossRefGoogle Scholar
  31. Rodriguez LF (2006) Can invasive species facilitate native species? evidence of how, when, and why these impacts occur. Biol Invasions 8:927–939. doi: 10.1007/s10530-005-5103-3 CrossRefGoogle Scholar
  32. Schwindt E, López Gappa J, Raffo MP, Tatián M, Bortolus A, Orensanz JM, Alonso G, Diez ME, Doti B, Genzano G, Lagger C, Lovrich G, Piriz ML, Mendez MM, Savoya V, Sueiro MC (2014) Marine fouling invasions in ports of Patagonia (Argentina) with implications for legislation and monitoring programs. Mar Environ Res 99:60–68. doi: 10.1016/j.marenvres.2014.06.006 CrossRefGoogle Scholar
  33. Sellheim K, Stachowicz JJ, Coates CR (2010) Effects of a nonnative habitat-forming species on mobile and sessile epifaunal communities. Mar Ecol Prog Ser 398:69–80. doi: 10.3354/meps08341 CrossRefGoogle Scholar
  34. Simkanin C, Davidson IC, Dower JF, Jamieson G, Therriault TW (2012) Anthropogenic structures and the infiltration of natural benthos by invasive ascidians. Mar Ecol 33:499–511. doi: 10.1111/j.1439-0485.2012.00516.x CrossRefGoogle Scholar
  35. Simkanin C, Fofonoff PW, Larson K, Lambert G, Dijkstra JA, Ruiz GM (2016) Spatial and temporal dynamics of ascidian invasions in the continental United States and Alaska. Mar Biol 163:1–16. doi: 10.1007/s00227-016-2924-9 CrossRefGoogle Scholar
  36. South PM, Thomsen MS (2016) The ecological role of invading Undaria pinnatifida: an experimental test of the driver–passenger models. Mar Biol 163:175. doi: 10.1007/s00227-016-2948-1 CrossRefGoogle Scholar
  37. Stachowicz JJ (2001) Mutualisms, positive interactions, and the structure of ecological communities. Bioscience 51:235–246. doi:10.1641/0006-3568(2001)051[0235:MFATSO]2.0.CO;2Google Scholar
  38. Suárez-Jímenez R, Hepburn CD, Hyndes GA, Mc Leod RJ, Taylor RB, Hurd CL (2015) Do native subtidal grazers eat the invasive kelp Undaria pinnatifida? Mar Biol 162:2521–2526. doi: 10.1007/s00227-015-2757-y Google Scholar
  39. Teichberg M, Fox SE, Olsen YS, Valiela I, Martinetto P, Iribarne O, Muto EY, Petti MAV, Corbisier TN, Soto-Jímenez M, Páez-Osuna F, Castro P, Freitas H, Zitelli A, Cardinaletti M, Tagliapietras D (2010) Eutrophication and macroalgal blooms in temperate and tropical coastal waters: nutrient enrichment experiments with Ulva spp. Glob Change Biol 16:2624–2637. doi: 10.1111/j.1365-2486.2009.02108.x Google Scholar
  40. Thompson GA, Schiel DR (2012) Resistance and facilitation by native algal communities in the invasion success of Undaria pinnatifida. Mar Ecol Prog Ser 95:95–105. doi: 10.3354/meps09995 CrossRefGoogle Scholar
  41. Thompson RC, Wilson BJ, Tobin ML, Hill AS, Hawkins SJ (1996) Biologically generated habitat provision and diversity of rocky shore organisms at a hierarchy of spatial scales. J Exp Mar Biol Ecol 202:73–84. doi: 10.1016/0022-0981(96)00032-9 CrossRefGoogle Scholar
  42. Valentine JP, Johnson CR (2003) Establishment of the introduced kelp Undaria pinnatifida in Tasmania depends on disturbance to native algal assemblages. J Exp Mar Biol Ecol 295:63–90. doi: 10.1016/S0022-0981(03)00272-7 CrossRefGoogle Scholar
  43. Valentine JP, Johnson CR (2004) Establishment of the introduced kelp Undaria pinnatifida following dieback of the native macroalga Phyllospora comosa in Tasmania, Australia. Mar Freshw Res 55:223–230. doi: 10.1071/MF03048 CrossRefGoogle Scholar
  44. Valentine JP, Johnson CR (2005) Persistence of the exotic kelp Undaria pinnatifida does not depend on sea urchin grazing. Mar Ecol Prog Ser 285:43–55. doi: 10.3354/meps285043 CrossRefGoogle Scholar
  45. Wahl M, Mark O (1999) The predominantly facultative nature of epibiosis: experimental and observational evidence. Mar Ecol Prog Ser 187:59–66. doi: 10.3354/meps187059 CrossRefGoogle Scholar
  46. Zhan A, Briski E, Bock DG, Ghabooli S, Mac Isaac HJ (2015) Ascidians as models for studying invasion success. Mar Biol. doi: 10.1007/s00227-015-2734-5 Google Scholar
  47. Zuur AF (2009) Mixed effects models and extensions in ecology with R. Springer, New YorkCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • Patricio Javier Pereyra
    • 1
    • 2
    • 3
    Email author
  • Paula de la Barra
    • 1
    • 2
  • Marianela Gastaldi
    • 2
    • 3
  • Juan Francisco Saad
    • 2
    • 3
  • Fausto Nahuel Firstater
    • 1
    • 2
    • 3
  • Maite Andrea Narvarte
    • 1
    • 2
    • 3
  1. 1.Centro de Investigación Aplicada y, Transferencia Tecnológica en Recursos Marinos Almirante Storni (CIMAS)San Antonio OesteArgentina
  2. 2.CONICETCiudad Autónoma de Buenos AiresArgentina
  3. 3.Escuela Superior de Ciencias Marinas, Universidad Nacional del ComahueSan Antonio OesteArgentina

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