Skip to main content
Log in

Photosynthetic plasticity of the genus Asparagopsis (Bonnemaisoniales, Rhodophyta) in response to temperature: implications for invasiveness

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Invasive species display remarkable levels of ecophysiological plasticity, which supports colonization, population establishment and fitness across their introduction range. The red seaweed genus Asparagopsis comprises genetically homogeneous invasive species (A. armata) and cryptic species complexes (A. taxiformis sensu lato) consisting of invasive mitochondrial lineages introduced worldwide. The photosynthetic plasticity of Australian, Mediterranean and Hawaiian Falkenbergia stages (i.e. the tetrasporophytic stage) of A. taxiformis lineages 2, 3 and 4 and Mediterranean isolates of A. armata was assessed by challenging their photosynthetic performance at five different temperatures (12–26 °C). Our aim is to portray the photosynthetic profiles in relation to temperature for each of the aforementioned Asparagopsis OTUs. We additionally test the physiological response of A. taxiformis lineage 2 sampled within its invasive (Mediterranean Sea) and native range (Australia) to identify physiological features associated with invasive strains. Based on photosynthesis optima, Asparagopsis isolates were recovered into a tropical (NL2 and L4) and a temperate (AA, Il2 and L3) group that presented no differences in most photosynthetic parameters at the experimental temperatures, thus indicating a greater physiological plasticity. On the other hand, low Ic values together with an apparent lack of sensitivity in the photosynthetic response to changing temperatures were revealed for the Mediterranean lineage 2, indicative of adaptive benefits that likely support its invasive success compared to the rest of the genus. Our results represent a valuable resource to predict distributional shifts in some of the lineages and to anticipate control programs for lineage 3, potentially invasive.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Altamirano M, Muñoz AR, De la Rosa J, Barrajón-Mínguez A, Barrajón-Domenech A, Moreno-Robledo C, Arroyo MC (2008) The exotic invasive species Asparagopsis taxiformis (Delile) Trevisan (Bonnemiasonial Rhodophyta) on Andalusian coasts (Southern Spain): new records, invaded communities and reproductive stages. Acta Bot Malacit 33:1–11

    Google Scholar 

  • Andreakis N, Schaffelke B (2012) Invasive marine seaweeds: pest or prize? In: Wiencke C, Bischof K (eds) Seaweed biology, vol 219. Ecological studies. Springer, Berlin, pp 235–262. doi:10.1007/978-3-642-28451-9_12

    Google Scholar 

  • Andreakis N, Procaccini G, Kooistra WHCF (2004) Asparagopsis taxiformis and Asparagopsis armata (Bonnemaisoniales, Rhodophyta): genetic and morphological identification of Mediterranean populations. Eur J Phycol 39(3):273–283. doi:10.1080/0967026042000236436

    Article  CAS  Google Scholar 

  • Andreakis N, Koolstra WHCF, Procaccini G (2007a) Microsatellite markers in an invasive strain of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta): insights in ploidy level and sexual reproduction. Gene 406(1–2):144–151. doi:10.1016/j.gene.2007.08.013

    Article  CAS  PubMed  Google Scholar 

  • Andreakis N, Procaccini G, Maggs C, Kooistra WHCF (2007b) Phylogeography of the invasive seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) reveals cryptic diversity. Mol Ecol 16(11):2285–2299. doi:10.1111/j.1365-294X.2007.03306.x

    Article  CAS  PubMed  Google Scholar 

  • Andreakis N, Kooistra WH, Procaccini G (2009) High genetic diversity and connectivity in the polyploid invasive seaweed Asparagopsis taxiformis (Bonnemaisoniales) in the Mediterranean, explored with microsatellite alleles and multilocus genotypes. Mol Ecol 18(2):212–226

  • Bolton JJ, Andreakis N, Anderson RJ (2011) Molecular evidence for three separate cryptic introductions of the red seaweed Asparagopsis (Bonnemaisoniales, Rhodophyta) in South Africa. Afr J Mar Sci 33(2):263–271. doi:10.2989/1814232x.2011.600339

    Article  Google Scholar 

  • Bonin DR, Hawkes MW (1987) Systematics and life histories of New Zealand Bonnemaisoniaceae (Bonnemaisoniales, Rhodophyta): I. The genus Asparagopsis. NZ J Bot 25(4):577–590

    Article  Google Scholar 

  • Boudouresque CF, Verlaque M (2002) Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Mar Pollut Bull 44(1):32–38

    Article  CAS  PubMed  Google Scholar 

  • Boudouresque CF, Verlaque M (2010) Is global warming involved in the success of seaweed introductions in the mediterranean sea? Seaweeds and their role in globally changing environments. Springer, Berlin, pp 31–50

    Chapter  Google Scholar 

  • Bradshaw AD (1965) Evolutionary significance of phenotypic plasticity in plants. Adv Genet 13(1):115–155

    Article  Google Scholar 

  • Bradshaw WE, Holzapfel CM (2006) Evolutionary response to rapid climate change. Science (Washington) 312(5779):1477–1478

    Article  CAS  Google Scholar 

  • Breeman AM (1988) Relative importance of temperature and other factors in determining geographic boundaries of seaweeds—experimental and phenological evidence. Helgolander Meeresun 42(2):199–241. doi:10.1007/Bf02366043

    Article  Google Scholar 

  • Breeman A, Oh YS, Hwang MS, Van Den Hoek C (2002) Evolution of temperature responses in the Cladophora vagabunda complex and the C. albida/sericea complex (Chlorophyta). Eur J Phycol 37(1):45–58

    Article  Google Scholar 

  • Cebrián E, Ballesteros E (2004) Zonation patterns of benthic communities in an upwelling area from the western Mediterranean (La Herradura, Alboran Sea). Scientia Marina 68(1):69–84

    Article  Google Scholar 

  • Davidson AM, Jennions M, Nicotra AB (2011) Do invasive species show higher phenotypic plasticity than native species and, if so, is it adaptive? A meta-analysis. Ecol Lett 14(4):419–431. doi:10.1111/j.1461-0248.2011.01596.x

    Article  Google Scholar 

  • Davison IR (1991) Environmental effects on algal photosynthesis: temperature. J Phycol 27(1):2–8

    Article  Google Scholar 

  • De Clerck O, Gavio B, Fredericq S, Barbara I, Coppejans E (2005) Systematics of Grateloupia filicina (Halymeniaceae, Rhodophyta), based on rbcL sequence analyses and morphological evidence, including the reinstatement of G-minima and the description of G-capensis sp nov. J Phycol 41(2):391–410. doi:10.1111/j.1529-8817.2005.04189.x

    Article  Google Scholar 

  • Dieck I (1993) Temperature tolerance and survival in darkness of kelp gametophytes (Laminariales, Phaeophyta): ecological and biogeographical implications. Mar Ecol Prog Ser 100:253-253

  • Eggert A (2012) Seaweed responses to temperature. Seaweed biology. Springer, Berlin, pp 47–66

    Chapter  Google Scholar 

  • Eggert A, Visser RJ, Van Hasselt PR, Breeman AM (2006) Differences in acclimation potential of photosynthesis in seven isolates of the tropical to warm temperate macrophyte Valonia utricularis (Chlorophyta). Phycologia 45(5):546–556

  • Flagella MM, Andreakis N, Hiraoka M, Verlaque M, Buia MC (2010) Identification of cryptic Ulva species (Chlorophyta, Ulvales) transported by ballast water. J Biol Res-Thessaloniki 13:47–57

    CAS  Google Scholar 

  • Flores-Moya A, Fernández JA, Niell FX (1996) Growth pattern, reproduction, and self-thinning in seaweeds. J Phycol 32:767–769

    Article  Google Scholar 

  • Galil BS (2000) A sea under siege–alien species in the Mediterranean. Biol Invasions 2(2):177–186

    Article  Google Scholar 

  • Genovese G, Tedone L, Hamann MT, Morabito M (2009) The Mediterranean red alga Asparagopsis: a source of compounds against Leishmania. Mar Drugs 7(3):361–366

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Guiry M, Dawes CJ (1992) Daylength, temperature and nutrient control of tetrasporogenesis in Asparagopsis armata (Rhodophyta). J Exp Mar Biol Ecol 158:197–217. doi:10.1016/0022-0981(92)90227-2

    Article  Google Scholar 

  • Guiry M, Guiry G (2011) AlgaeBase. World-wide electronic publication, National University of Ireland, Galway

    Google Scholar 

  • Hall TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98

    CAS  Google Scholar 

  • Hanelt D (1996) Photoinhibition of photosynthesis in marine macroalgae. Sci Mar 60:243-248

  • Henley WJ (1993) Measurement and interpretation of photosynthetic light-response curves in algae in the context of photoinhibition and diel changes. J Phycol 29:729–739

    Article  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation: mechanism and process in physiological evolution. Oxford Unviversity Press, New York, p 466

  • Knowlton N (1993) Sibling species in the sea. Annu Rev Ecol Syst 24:189–216. doi:10.1146/annurev.ecolsys.24.1.189

    Article  Google Scholar 

  • Kooistra WHCF, Coppejans EGG, Payri C (2002) Molecular systematics, historical ecology, and phylogeography of Halimeda (Bryopsidales). Mol Phylogenet Evol 24(1):121–138. doi:10.1016/S1055-7903(02)00221-X

    Article  CAS  PubMed  Google Scholar 

  • Lüning K (1990) Seaweeds. Their environment, biogeography and ecophysiology. Wiley, New York

    Google Scholar 

  • Manilal A, Sujith S, Sabarathnam B, Kiran GS, Selvin J, Shakir C, Lipton AP (2010) Bioactivity of the red algae Asparagopsis taxiformis collected from the Southwestern coast of India. Braz J Oceanogr 58(2):93–100

    Article  Google Scholar 

  • Mata L, Schuenhoff A, Santos R (2010) A direct comparison of the performance of the seaweed biofilters, Asparagopsis armata and Ulva rigida. J Appl Phycol 22(5):639–644

    Article  CAS  Google Scholar 

  • Necchi O (2004) Photosynthetic responses to temperature in tropical lotic macroalgae. Phycol Res 52:140–148

    Article  Google Scholar 

  • Ní Chualáin F, Maggs CA, Saunders GW, Guiry MD (2004) The invasive genus Asparagopsis (Bonnemaisoniaceae, Rhodophyta): molecular systematics, morphology and ecophysiology of Falkenbergia isolates. J Phycol 40(1):1112–1126

    Article  Google Scholar 

  • Nyberg CD, Wallentinus I (2005) Can species traits be used to predict marine macroalgal introductions? Biol Invasions 7(2):265–279. doi:10.1007/s10530-004-0738-z

    Article  Google Scholar 

  • Osmond CB (1994) What is photoinhibition? Some insights from comparisons of shade and sun plants. In: Baker NR, Bowyer JR (eds) Photoinhibition of photosynthesis from molecular mechanisms to the field. Bios Scientific Publishers, Oxford, pp 1–24

  • Padilla-Gamiño JL, Carpenter RC (2007) Seasonal acclimatization of Asparagopsis taxiformis (Rhodophyta) from different biogeographic regions. Limnol Oceanogr 52(2):833–842

    Article  Google Scholar 

  • Pandit MK, Pocock MJ, Kunin WE (2011) Ploidy influences rarity and invasiveness in plants. J Eco 99(5):1108-1115

  • Paul AN (2006) The ecology of chemical defense in a filamentous red alga. Doctoral Thesis. University of New South Wales. Sydney, Australia

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    Article  CAS  PubMed  Google Scholar 

  • Provasoli L (1968) Media and prospects for the cultivation of marine algae. In: Cultures and collections of algae. Proceedings of the US–Japan conference, Hakone, Sept 1966, 1968. Japanese Society for Plant Physiology, pp 63–75

  • Raniello R, Lorenti M, Brunet C, Buia MC (2004) Photosynthetic plasticity of an invasive variety of Caulerpa racemosa in a coastal Mediterranean area: light harvesting capacity and seasonal acclimation. Mar Ecol Prog Ser 271:113–120

    Article  Google Scholar 

  • Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77(6):1655–1661

    Article  Google Scholar 

  • Richards CL, Bossdorf O, Muth NZ, Gurevitch J, Pigliucci M (2006) Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecol Lett 9(8):981–993

    Article  PubMed  Google Scholar 

  • Salvador N, Gómez Garreta A, Lavelli L, Ribera MA (2007) Antimicrobial activity of Iberian macroalgae. Sci Mar 71(1):101–114

    Article  Google Scholar 

  • Schaffelke B, Smith JE, Hewitt CL (2006) Introduced macroalgae—a growing concern. J Appl Phycol 18(3–5):529–541. doi:10.1007/s10811-006-9074-2

    Article  Google Scholar 

  • Schmidt-Roach S, Lundgren P, Miller K, Gerlach G, Noreen AME, Andreakis N (2013) Assessing hidden species diversity in the coral Pocillopora damicornis from Eastern Australia. Coral Reefs 32(1):161–172

  • Sherwood AR (2008) Phylogeography of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) in the Hawaiian Islands: two mtDNA markers support three separate introductions. Phycologia 47(1):79-88

  • Smith LD (2009) The role of phenotypic plasticity in marine biological invasions. Biological invasions in marine ecosystems. Springer, Berlin, pp 177–202

    Chapter  Google Scholar 

  • Stearns SC (1989) The evolutionary significance of phenotypic plasticity. BioScience 39(7):436–445

  • Swofford DL (2002) PAUP*. Phylogenetic analysis using parsimony (*and Other Methods). Version 4. Sinauer Associates, Sunderland

  • Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176(2):256–273. doi:10.1111/j.1469-8137.2007.02207.x

    Article  PubMed  Google Scholar 

  • Thresher R Key threats from marine bioinvasions: a review of current and future issues. In: Marine bioinvasions, Proceedings of the first national conference, 1999. pp 24–36

  • Uwai S, Nelson W, Neill K, Wang WD, Aguilar-Rosas LE, Boo SM, Kitayama T, Kawai H (2006) Genetic diversity in Undaria pinnatifida (Laminariales, Phaeophyceae) deduced from mitochondria genes—origins and succession of introduced populations. Phycologia 45 (6):687–695

  • Verlaque M, Boudouresque C (2004) Invasions biologiques marines et changement global. Actes des 2:74–75

    Google Scholar 

  • Webster N, Pantile R, Botte E, Abdo D, Andreakis N, Whalan S (2013) A complex life cycle in a warming planet: gene expression in thermally stressed sponges. Mol Ecol 22(7):1854–1868. doi:10.1111/mec.12213

    Article  CAS  PubMed  Google Scholar 

  • Wellburn AR (1994) The spectral determination of chlorophylls a and b, as well as total carotenoids, using various solvents with spectrophotometers of different resolution. J Plant Physiol 144(3):307-313

  • Zanolla M, Carmona R, De La Rosa J, Salvador N, Sherwood AR, Andreakis N, Altamirano M (2014) Morphological differentiation of cryptic lineages within the invasive genus Asparagopsis (Bonnemaisoniales, Rhodophyta). Phycologia 53(3):233–242

    Article  Google Scholar 

  • Zanolla M, Altamirano M, Carmona R, De La Rosa J, Souza-Egipsy V, Sherwood A, Tsiamis K, Barbosa AM, Muñoz AR, Andreakis N. Worldwide spread and invasive risk assessment of species with cryptic lineages: the case of the red seaweed genus Asparagopsis (Bonnemaisoniales, Rhodophyta) (in preparation)

  • Zenetos A, Gofas S, Verlaque M, Cinar ME, Raso JEG, Bianchi CN, Morri C, Azzurro E, Bilecenoglu M, Froglia C, Siokou I, Violanti D, Sfriso A, San Martin G, Giangrande A, Katagan T, Ballesteros E, Ramos-Espla A, Mastrototaro F, Ocana O, Zingone A, Gambi MC, Streftaris N (2010) Alien species in the Mediterranean sea by 2010. A contribution to the application of European Union’s Marine Strategy Framework Directive (MSFD). Part I. Spatial distribution. Mediterranean Marine Sci 11(2):381–493

    Article  Google Scholar 

  • Zerebecki RA, Sorte CJ (2011) Temperature tolerance and stress proteins as mechanisms of invasive species success. PLoS One 6(4):e14806

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zuccarello GC, West JA (2002) Phylogeography of the Bostrychia calliptera-B-pinnata complex (Rhodomelaceae, Rhodophyta) and divergence rates based on nuclear, mitochondrial and plastid DNA markers. Phycologia 41(1):49–60. doi:10.2216/i0031-8884-41-1-49.1

    Article  Google Scholar 

  • Zuccarello GC, West JA (2003) Multiple cryptic species: molecular diversity and reproductive isolation in the Bostrychia radicans/B-moritziana complex (Rhodomelaceae, Rhodophyta) with focus on north american isolates. J Phycol 39(5):948–959

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work has been funded by the projects CGL2008/01549/BOS (MINISTERIO DE CIENCIA E INNOVACIÓN, Spain), P09-RNM-5187 (CONSEJERÍA DE INNOVACIÓN, CIENCIA Y EMPRESA, JUNTA DE ANDALUCÍA, Spain), 806/5.03.3553 and 806/5.03.3673 (INSTITUTO DE ESTUDIOS CEUTÍES, Spain), and has been developed in the framework of the Research Collaboration Agreement between CONSEJERÍA DE MEDIO AMBIENTE DE LA JUNTA DE ANDALUCÍA and the UNIVERSITY OF MÁLAGA. Marianela Zanolla is a PhD student of the project P09-RNM-5187 from the CONSEJERÍA DE INNOVACIÓN, CIENCIA Y EMPRESA, JUNTA DE ANDALUCÍA, Spain; also supported by the “Plan Propio” from the UNIVERSITY OF MÁLAGA. NA is supported by the COMMONWEALTH ENVIRONMENTAL RESEARCH FACILITIES (CERF) Marine Biodiversity Hub. The CERF program is an Australian Government initiative supporting world class, public good research and is a collaborative partnership between the UNIVERSITY OF TASMANIA, CSIRO Wealth from OCEANS FLAGSHIP, Geoscience Australia, AUSTRALIAN INSTITUTE OF MARINE SCIENCE and MUSEUM VICTORIA. Some of the analyses of Hawaiian specimens were supported by a U.S. NATIONAL SCIENCE FOUNDATION GRANT (DEB-0542608) to A.R.S. and G.G. Presting.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. Zanolla.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zanolla, M., Altamirano, M., Carmona, R. et al. Photosynthetic plasticity of the genus Asparagopsis (Bonnemaisoniales, Rhodophyta) in response to temperature: implications for invasiveness. Biol Invasions 17, 1341–1353 (2015). https://doi.org/10.1007/s10530-014-0797-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0797-8

Keywords

Navigation