Marine Biology

, 164:164 | Cite as

Modulation of different kelp life stages by herbivory: compensatory growth versus population decimation

  • João N. FrancoEmail author
  • Thomas Wernberg
  • Iacopo Bertocci
  • David Jacinto
  • Paulo Maranhão
  • Tânia Pereira
  • Brezo Martinez
  • Francisco Arenas
  • Isabel Sousa-Pinto
  • Fernando Tuya
Original paper


Partitioning the effects of herbivory on different life stages of primary producers is key to understanding the population-wide consequences of herbivory. We assessed the performance of microscopic (MiS <1 mm) juveniles, macroscopic (MaS) juveniles and adult kelp (Laminaria ochroleuca) under contrasting herbivory regimes through a herbivore exclusion field experiment. The abundance of MiS and the survival of MaS decreased by 67 and 63%, respectively, when herbivorous fishes and sea urchins were present. Blade growth (linear and area) of adult kelp displayed contrasting patterns under herbivore pressure: a 60% increase and a 46% decrease, respectively. These results indicate that while herbivory severely reduces juvenile survival, it may also induce compensatory growth (measured as linear growth) in adult kelp. In summary, we here demonstrate how herbivory affects all sporophyte life stages of the kelp L. ochroleuca. This is likely to have important implications for situations where historical patterns of herbivore presence and herbivory are changing, such as is increasingly the case in many temperate regions due to warming around the world.



Financial support was provided by the European Regional Development Fund (ERDF) through the ‘Programa Operacional Factores de Competitividade’ (POFC-COMPETE) within the ‘Quadro de Referência Estratégico Nacional (QREN)’ and the Portuguese Fundação para a Ciência e a Tecnologia (FCT) through the project ‘Efeitos do clima oceânico na macroecologia e resiliência a perturbações dos povoamentos de kelps’—OCEANKELP (PTDC/MAR/109954/2009); and the strategic project UID/MAR/04292/2013 Granted to MARE. João N. Franco was supported by a FCT PhD Grant (SFRH/BD/84933/2012). Thomas Wernberg was supported by Grants from the Australian Research Council (FT110100174, DP170100023). We are very grateful to Nuno Vasco Rodrigues, ESTM-IPLEIRA volunteers and Haliotis and AquaSubOeste Diving centres for their valuable help during experimental set-up and maintenance.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


This study was funded by Portuguese Fundação para a Ciência e a Tecnologia (FCT) through the projects: OCEANKELP (PTDC/MAR/109954/2009), UID/MAR/04292/2013 and a PhD Grant (SFRH/BD/84933/2012) and the Australian Research Council (FT110100174, DP170100023).

Ethical approval

This article does not contain any studies with animals performed by any of the authors.

Supplementary material

227_2017_3196_MOESM1_ESM.pdf (173 kb)
Supplementary material 1 (PDF 172 kb)


  1. Araújo RM, Assis J, Aguillar R et al (2016) Status, trends and drivers of kelp forests in Europe: an expert assessment. Biodivers Conserv 25:1319–1348. doi: 10.1007/s10531-016-1141-7 CrossRefGoogle Scholar
  2. Assis J, Coelho NC, Lamy T et al (2016) Deep reefs are climatic refugia for genetic diversity of marine forests. J Biogeogr 43:833–844. doi: 10.1111/jbi.12677 CrossRefGoogle Scholar
  3. Assis J, Tavares D, Tavares J, Cunha A (2009) Findkelp, a GIS-based community participation project to assess Portuguese kelp conservation status. J Coast Res 3:1469–1473Google Scholar
  4. Bañón R, Mucientes G (2009) First record of Seriola fasciata (Carangidae) from Galician waters (NW Spain). A new northernmost occurrence in the NE Atlantic. Cybium 33:247–248Google Scholar
  5. Bartsch I, Wiencke C, Bischof K et al (2008) The genus Laminaria sensu lato: recent insights and developments. Eur J Phycol 43:1–86. doi: 10.1080/09670260701711376 CrossRefGoogle Scholar
  6. Bennett S, Wernberg T, de Bettignies T et al (2015) Canopy interactions and physical stress gradients in subtidal communities. Ecol Lett 18:677–686. doi: 10.1111/ele.12446 CrossRefGoogle Scholar
  7. Biskup S, Bertocci I, Arenas F, Tuya F (2014) Functional responses of juvenile kelps, Laminaria ochroleuca and Saccorhiza polyschides, to increasing temperatures. Aquat Bot 113:117–122. doi: 10.1016/j.aquabot.2013.10.003 CrossRefGoogle Scholar
  8. Boege K, Marquis RJ (2005) Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends Ecol Evol 20:441–448. doi: 10.1016/j.tree.2005.05.001 CrossRefGoogle Scholar
  9. Bruno JF, O’Connor MI (2005) Cascading effects of predator diversity and omnivory in a marine food web. Ecol Lett 8:1048–1056. doi: 10.1111/j.1461-0248.2005.00808.x CrossRefGoogle Scholar
  10. Burkepile DE (2013) Comparing aquatic and terrestrial grazing ecosystems: is the grass really greener? Oikos 122:306–312. doi: 10.1111/j.1600-0706.2012.20716.x CrossRefGoogle Scholar
  11. Cerda O, Karsten U, Rothäusler E et al (2009) Compensatory growth of the kelp Macrocystis integrifolia (Phaeophyceae, Laminariales) against grazing of Peramphithoe femorata (Amphipoda, Ampithoidae) in northern-central Chile. J Exp Mar Biol Ecol 377:61–67. doi: 10.1016/j.jembe.2009.06.011 CrossRefGoogle Scholar
  12. Davenport AC, Anderson TW (2007) Positive indirect effects of reef fishes on kelp performance: the importance of mesograzers. Ecology 88:1548–1561CrossRefGoogle Scholar
  13. Dayton PK (1972) Towards an understanding of community resilience and the potential effects of enrichment to the benthos at McMurdo Sound, Antarctica. In: Parker BC (ed) Proceedings of the Colloquium on conservation problems in Antarctica. Allen Press, Lawrence, pp 81–95Google Scholar
  14. Duffy JE, Hay ME (2000) Strong impacts of grazing amphipods on the organization of a benthic community. Ecol Monogr 70:237. doi: 10.2307/2657176 CrossRefGoogle Scholar
  15. Fernandez C (2011) The retreat of large brown seaweeds on the north coast of Spain: the case of Saccorhiza polyschides. Eur J Phycol 46:352–360. doi: 10.1080/09670262.2011.617840 CrossRefGoogle Scholar
  16. Figurski JD, Malone D, Lacy JR, Denny M (2011) An inexpensive instrument for measuring wave exposure and water velocity. Limnol Oceanogr Methods 9:204–214. doi: 10.4319/lom.2011.9.204 CrossRefGoogle Scholar
  17. Filbee-Dexter K, Feehan CJ, Scheibling RE (2016) Large-scale degradation of a kelp ecosystem in an ocean warming hotspot. Mar Ecol Prog Ser 543:141–152. doi: 10.3354/meps11554 CrossRefGoogle Scholar
  18. Filbee-Dexter K, Scheibling R (2014) Sea urchin barrens as alternative stable states of collapsed kelp ecosystems. Mar Ecol Prog Ser 495:1–25. doi: 10.3354/meps10573 CrossRefGoogle Scholar
  19. Franco JN, Wernberg T, Bertocci I et al (2015) Herbivory drives kelp recruits into “hiding” in a warm ocean climate. Mar Ecol Prog Ser 536:1–9. doi: 10.3354/meps11445 CrossRefGoogle Scholar
  20. Franco JN, Tuya F, Bertocci I, Rodríguez L, Martínez B, Sousa-Pinto I, Arenas F (2017) The ‘golden kelp’ Laminaria ochroleuca under global change: Integrating multiple eco-physiological responses with species distribution models. J Ecol 1–12. doi: 10.1111/1365-2745.12810
  21. Gagnon P, Himmelman JH, Johnson LE (2003) Algal colonization in urchin barrens: Defense by association during recruitment of the brown alga Agarum cribrosum. J Exp Mar Biol Ecol 290:179–196. doi: 10.1016/S0022-0981(03)00077-7 CrossRefGoogle Scholar
  22. Gaines S, Lubchenco J (1982) A unified approach to marine plant-herbivore interactions. II. Biogeography. Annu Rev Ecol Syst 13:111–138CrossRefGoogle Scholar
  23. Gao X, Endo H, Yamana M et al (2013) Compensatory abilities depending on seasonal timing of thallus excision of the kelp Undaria pinnatifida cultivated in Matsushima Bay, northern Japan. J Appl Phycol 25:1331–1340. doi: 10.1007/s10811-013-9989-3 CrossRefGoogle Scholar
  24. Hanley TC, La Pierre KJ (2015) Trophic ecology: bottom–up and top–down interactions across aquatic and terrestrial systems. In: Hanley TC, La Pierre KJ (eds) Trophic Ecology. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  25. Hay KB, Poore AGB, Lovelock CE (2011) The effects of nutrient availability on tolerance to herbivory in a brown seaweed. J Ecol 99:1540–1550. doi: 10.1111/j.1365-2745.2011.01874.x CrossRefGoogle Scholar
  26. Henriques S, Pais MP, Costa MJ, Cabral HN (2013) Seasonal variability of rocky reef fish assemblages: detecting functional and structural changes due to fishing effects. J Sea Res 79:50–59. doi: 10.1016/j.seares.2013.02.004 CrossRefGoogle Scholar
  27. Jacinto D, Bulleri F, Benedetti-Cecchi L, Cruz T (2013) Patterns of abundance, population size structure and microhabitat usage of Paracentrotus lividus (Echinodermata: Echinoidea) in SW Portugal and NW Italy. Mar Biol 160:1135–1146. doi: 10.1007/s00227-013-2166-z CrossRefGoogle Scholar
  28. Lima FP, Ribeiro PA, Queiroz N et al (2007) Do distributional shifts of northern and southern species of algae match the warming pattern? Glob Chang Biol 13:2592–2604. doi: 10.1111/j.1365-2486.2007.01451.x CrossRefGoogle Scholar
  29. Ling SD, Ibbott S, Sanderson JC (2010) Recovery of canopy-forming macroalgae following removal of the enigmatic grazing sea urchin Heliocidaris erythrogramma. J Exp Mar Biol Ecol 395:135–146. doi: 10.1016/j.jembe.2010.08.027 CrossRefGoogle Scholar
  30. Ling SD, Scheibling RE, Rassweiler A et al (2014) Global regime shift dynamics of catastrophic sea urchin overgrazing. Philos Trans R Soc B Biol Sci 370:20130269. doi: 10.1098/rstb.2013.0269 CrossRefGoogle Scholar
  31. Maron JL, Crone E (2006) Herbivory: effects on plant abundance, distribution and population growth. Proc R Soc Biol Sci 273:2575–2584. doi: 10.1098/rspb.2006.3587 CrossRefGoogle Scholar
  32. Moles AT, Bonser SP, Poore AGB et al (2011) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Funct Ecol 25:380–388. doi: 10.1111/j.1365-2435.2010.01814.x CrossRefGoogle Scholar
  33. Muth AF (2012) Effects of zoospore aggregation and substrate rugosity on kelp recruitment success. J Phycol 48:1374–1379. doi: 10.1111/j.1529-8817.2012.01211.x CrossRefGoogle Scholar
  34. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398CrossRefGoogle Scholar
  35. Pace M, Cole J, Carpenter S, Kitchell J (1999) Trophic cascades revealed in diverse ecosystems. Trends Ecol Evol 14:483–488CrossRefGoogle Scholar
  36. Pansch C, Gómez I, Rothäusler E et al (2008) Species-specific defense strategies of vegetative versus reproductive blades of the Pacific kelps Lessonia nigrescens and Macrocystis integrifolia. Mar Biol 155:51–62. doi: 10.1007/s00227-008-1006-z CrossRefGoogle Scholar
  37. Parke M (1948) Studies on British Laminariaceae. I. Growth in Laminaria saccharina (L.) Lamour. J Mar Biol Assoc United Kingdom 27:651. doi: 10.1017/S0025315400056071 CrossRefGoogle Scholar
  38. Pereira TR, Engelen AH, Pearson GA et al (2011) Temperature effects on the microscopic haploid stage development of Laminaria ochroleuca and Sacchoriza polyschides, kelps with contrasting life histories. Cah Biol 52:395–403Google Scholar
  39. Piñeiro-Corbeira C, Barreiro R, Cremades J (2016) Decadal changes in the distribution of common intertidal seaweeds in Galicia (NW Iberia). Mar Environ Res 113:106–115. doi: 10.1016/j.marenvres.2015.11.012 CrossRefGoogle Scholar
  40. Pinho D, Bertocci I, Arenas F et al (2015) Spatial and temporal variation of kelp forests and associated macroalgal assemblages along the Portuguese coast. Mar Freshw Res 67:113–122. doi: 10.1071/MF14318 CrossRefGoogle Scholar
  41. Poore AGB, Gutow L, Pantoja JF et al (2014) Major consequences of minor damage: impacts of small grazers on fast-growing kelps. Oecologia 174:789–801. doi: 10.1007/s00442-013-2795-4 CrossRefGoogle Scholar
  42. Proulx M, Mazumder A (1998) Reversal of grazing impact on plant species richeness in nutrient-poor vs. nutreitn-rich ecosystems. Ecology 79:2581–2592. doi:10.1890/0012-9658(1998)079[2581:ROGIOP]2.0.CO;2Google Scholar
  43. Raybaud V, Beaugrand G, Goberville E et al (2013) Decline in kelp in west Europe and climate. PLoS One 8:1–10. doi: 10.1371/journal.pone.0066044 CrossRefGoogle Scholar
  44. Rodrigues NV, Correia JPS, Graça JTC et al (2012) First record of a whale shark Rhincodon typus in continental Europe. J Fish Biol 81:1427–1429. doi: 10.1111/j.1095-8649.2012.03392.x CrossRefGoogle Scholar
  45. Russell BD, Harley CDG, Wernberg T et al (2012) Predicting ecosystem shifts requires new approaches that integrate the effects of climate change across entire systems. Biol Lett 8:164–166. doi: 10.1098/rsbl.2011.0779 CrossRefGoogle Scholar
  46. Sivertsen K (2006) Overgrazing of kelp beds along the coast of Norway. J Appl Phycol 18:599–610. doi: 10.1007/s10811-006-9064-4 CrossRefGoogle Scholar
  47. Smale DA, Wernberg T, Yunnie ALE, Vance T (2015) The rise of Laminaria ochroleuca in the western english channel (UK) and comparisons with its competitor and assemblage dominant Laminaria hyperborea. Mar Ecol 36:1033–1044. doi: 10.1111/maec.12199 CrossRefGoogle Scholar
  48. Steneck RS, Graham MH, Bourque BJ et al (2002) Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ Conserv 29:436–459. doi: 10.1017/S0376892902000322 CrossRefGoogle Scholar
  49. Targett N, Coen L (1992) Biogeographic comparisons of marine algal polyphenolics: evidence against a latitudinal trend. Oecologia 89:464–470CrossRefGoogle Scholar
  50. Teixeira CM, Gamito R, Leitão F et al (2014) Trends in landings of fish species potentially affected by climate change in Portuguese fisheries. Reg Environ Chang 14:657–669. doi: 10.1007/s10113-013-0524-5 CrossRefGoogle Scholar
  51. Tuya F, Cacabelos E, Duarte P et al (2012) Patterns of landscape and assemblage structure along a latitudinal gradient in ocean climate. Mar Ecol Prog Ser 466:9–19. doi: 10.3354/meps09941 CrossRefGoogle Scholar
  52. Van Alstyne K, Ehlig J, Whitman S (1999) Feeding preferences for juvenile and adult algae depend on algal stage and herbivore species. Mar Ecol Prog Ser 180:179–185. doi: 10.3354/meps180179 CrossRefGoogle Scholar
  53. Van Alstyne KL, Whitman SL, Ehlig JM (2001) Differences in herbivore preferences, phlorotannin production, and nutritional quality between juvenile and adult tissues from marine brown algae. Mar Biol 139:201–210. doi: 10.1007/s002270000507 CrossRefGoogle Scholar
  54. Vergés A, Doropoulos C, Malcolm HA et al (2016) Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp. Proc Natl Acad Sci 113:13791–13796. doi: 10.1073/pnas.1610725113 CrossRefGoogle Scholar
  55. Vergés A, Paul NA, Steinberg PD (2008) Sex and life-history stage alter herbivore responses to a chemically defended red alga. Ecology 89:1334–1343. doi: 10.1890/07-0248.1 CrossRefGoogle Scholar
  56. Vergés A, Steinberg P, Hay ME et al (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:201408CrossRefGoogle Scholar
  57. Voerman SE, Llera E, Rico JM (2013) Climate driven changes in subtidal kelp forest communities in NW Spain. Mar Environ Res 90:119–127. doi: 10.1016/j.marenvres.2013.06.006 CrossRefGoogle Scholar
  58. Wernberg T, Bennett S, Babcock RC et al (2016) Climate-driven regime shift of a temperate marine ecosystem. Science 353:169–172. doi: 10.1126/science.aad8745 (80-) CrossRefGoogle Scholar
  59. Zarco-Perello S, Wernberg T, Langlois TJ, Vanderklift MA (2017) Tropicalization strengthens consumer pressure on habitat-forming seaweeds. Sci Rep 7:820. doi: 10.1038/s41598-017-00991-2 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  • João N. Franco
    • 1
    • 2
    Email author return OK on get
  • Thomas Wernberg
    • 3
  • Iacopo Bertocci
    • 1
    • 4
  • David Jacinto
    • 5
  • Paulo Maranhão
    • 6
  • Tânia Pereira
    • 1
  • Brezo Martinez
    • 7
  • Francisco Arenas
    • 1
  • Isabel Sousa-Pinto
    • 1
    • 2
  • Fernando Tuya
    • 8
  1. 1.CIIMAR, Centro Interdisciplinar de Investigação Marinha e AmbientalTerminal de Cruzeiros do Porto de LeixõesMatosinhosPortugal
  2. 2.Departamento de Biologia, Faculdade de CiênciasUniversidade do PortoPortoPortugal
  3. 3.School of Biological Sciences and UWA Oceans Institute (M470)University of Western AustraliaCrawleyAustralia
  4. 4.Stazione Zoologica Anton DohrnNaplesItaly
  5. 5.MARE-Marine and Environmental Sciences Centre, Laboratório de Ciências do MarUniversidade de ÉvoraSinesPortugal
  6. 6.MARE-Marine and Environmental Sciences Centre, ESTMInstituto Politécnico de LeiriaPenichePortugal
  7. 7.Rey Juan Carlos UniversityMóstolesSpain
  8. 8.IU-ECOAQUA, Grupo en Biodivesidad y Conservación, Marine Sciences FacultyUniversidad de Las Palmas de Gran CanariaLas PalmasSpain

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