Accessible Requires Authentication Published by De Gruyter November 21, 2017

Reproductive ecology of an invasive lineage 2 population of Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta) in the Alboran Sea (western Mediterranean Sea)

Marianela Zanolla, Raquel Carmona and María Altamirano
From the journal Botanica Marina


Can the reproductive traits of Asparagopsis taxiformis contribute to its success as an invader? We present the reproductive phenology of a population located in southern Spain and a quantitative study of gametophyte reproductive structures. Reproductive allocation (the proportion of biomass allocated to reproductive tissue) in different size classes was analysed to investigate whether the shoot size influences the reproductive output of this population. Gametophytes were found to be reproductive in spring, autumn and the beginning of winter, whereas fertile tetrasporophytes were never observed. High reproductive performance was recorded in July, when reproductive allocation was surprisingly low (12.74±4.79%). Reproductive allocation of each size class varied over the study period, ensuring a continuous reproductive yield. The shoot size for reproduction ranged between 4–6 cm and 24–26 cm. An analysis of reproductive and vegetative volume suggested that reproductive allocation decreases with shoot size, which, as intermediate size classes are the most abundant and most persistent in the field throughout the year, optimizes the reproductive output. Reproduction in gametophytes was independent of environmental conditions in the study area. The yearly persistence of gametophytes together with the abundance of tetrasporophytes makes this population a donor source for future invasive populations.


This work was 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 was developed in the framework of the Research Collaboration Agreement between Consejería de Medio Ambiente y Ordenación del Territorio de la Junta de Andalucía and the University of Málaga. M. Zanolla was funded by the scholarship Personal Investigador en Formación from the Consejería de Economía, Innovación, Ciencia y Empleo, Junta de Andalucía. We thank Julio De la Rosa for helping us in most of the field sampling surveys. The authors would like to thank the anonymous reviewers and especially Prof. Matthew J. Dring for their suggestions which improved the quality of our manuscript.


Åberg, P. 1996. Patterns of reproductive effort in the brown alga Ascophyllum nodosum. Mar. Ecol. Progr. Ser. 138: 199–207.10.3354/meps138199 Search in Google Scholar

Altamirano, M., A.R. Muñoz, J. De la Rosa, A. Barrajón-Mínguez, A. Barrajón-Domenech, C. Moreno-Robledo and M.C. Arroyo. 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. Search in Google Scholar

Andreakis, N. and B. Schaffelke. 2012. Invasive marine seaweeds: pest or prize? In: (C. Wiencke and K. Bischof, eds.) Seaweed biology. Springer Berlin Heidelberg. pp. 235. Search in Google Scholar

Andreakis, N., G. Procaccini and W.H. Kooistra. 2004. Asparagopsis taxiformis and Asparagopsis armata. Bonnemaisoniales, Rhodophyta: genetic and morphological identification of Mediterranean populations. Eur. J. Phycol. 39: 273–283.10.1080/0967026042000236436 Search in Google Scholar

Andreakis, N., G. Procaccini, C. Maggs and W.H. Kooistra. 2007. Phylogeography of the invasive seaweed Asparagopsis Bonnemaisoniales (Rhodophyta) reveals cryptic diversity. Mol. Ecol. 16: 2285–2299.10.1111/j.1365-294X.2007.03306.x Search in Google Scholar

Andreakis, N., W.H. Kooistra and G. Procaccini. 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: 212–226.10.1111/j.1365-294X.2008.04022.x Search in Google Scholar

Andreakis, N., P. Costello, M. Zanolla, G.W. Saunders and L. Mata. 2016. Endemic or introduced? Phylogeography of Asparagopsis (Florideophyceae) in Australia reveals multiple introductions and a new mitochondrial lineage. J. Phycol. 52: 141–147.10.1111/jpy.12373 Search in Google Scholar

Ang, P.O. Jr. 1992. Cost of reproduction in Fucus distichus. Mar. Ecol. Prog. Ser. 89: 25–35.10.3354/meps089025 Search in Google Scholar

Aranda, J., F.X. Niell and J.A. Fernández. 1984. Production of Asparagopsis armata (Harvey) in a thermally-stressed intertidal system of low tidal amplitude. J. Exp. Mar. Biol. Ecol. 84: 285–295.10.1016/0022-0981(84)90186-2 Search in Google Scholar

Araújo, R., J. Violante, R. Pereira, H. Abreu, F. Arenas and I. Sousa-Pinto. 2011. Distribution and population dynamics of the introduced seaweed Grateloupia turuturu (Halymeniaceae, Rhodophyta) along the Portuguese coast. Phycologia 50: 392–402.10.2216/10-65.1 Search in Google Scholar

Arenas, F. and C. Fernández. 1998. Ecology of Sargassum muticum (Phaeophyta) on the north coast of Spain. III. Reproductive ecology. Bot. Mari. 41: 209–216. Search in Google Scholar

Back, S., J.C. Collins and G. Russel. 1993. Comparative reproductive biology of the Gulf of Finland and the Irish sea Fucus vesiculosus L. Sarsia 78: 265–272.10.1080/00364827.1993.10413540 Search in Google Scholar

Barret, S.C. 2011. Why reproductive systems matter for the invasion biology of plants. In: (D.M. Richardson, ed). Fifty years of invasion ecology: the legacy of Charles Elton. Wiley-Blackwell, UK. pp. 195. Search in Google Scholar

Bohanak, A. and K. van der Linde. 2004. RMA: software for reduced major axis regression, Java version. Website: (accessed 18 Dec 2015). Search in Google Scholar

Bonin, D.R. and M.W. Hawkes. 1987. Systematics and life histories of New Zealand Bonnemaisoniaceae (Bonnemaisoniales, Rhodophyta): I. The genus Asparagopsis. N. Z. J. Bot. 25: 577–590.10.1080/0028825X.1987.10410088 Search in Google Scholar

Boudouresque, C. and M. Verlaque. 2010. Is global warming involved in the success of seaweed introductions in the Mediterranean Sea? In: (J. Seckbach, R. Einav and A. Israel, eds.) Seaweeds and their role in globally changing environments. Springer, Berlin. pp. 31–50. Search in Google Scholar

Breeman, A.M. 1988. Relative importance of temperature and other factors in determining geographic boundaries of seaweeds: experimental and phenological evidence. Helgol. Mar. Res. 42: 199–241. Search in Google Scholar

Byers, J.E. 2002. Physical habitat attribute mediates biotic resistance to non- indigenous species invasion. Oecologia. 130: 146–156.10.1007/s004420100777 Search in Google Scholar

Cebrián, E. and E. Ballesteros. 2010. Invasion of Mediterranean benthic assemblages by red alga Lophocladia lallemandii (Montagne) F. Schmitz: depth-related temporal variability in biomass and phenology. Aq. Bot. 92: 81–85.10.1016/j.aquabot.2009.10.007 Search in Google Scholar

Ceccherelli, G. and F. Cinelli. 1999. The role of vegetative spreading in dispersal of the invasive alga Caulerpa taxifolia in the Mediterranean. Mar. Ecol. Prog. Ser. 163: 289–294. Search in Google Scholar

Chihara, M. 1962. Life cycle of the Bonnemaissoniaceous algae in Japan 2. Science Republic Tokyo Kyoiku Daigaku, B. 11: 27–33. Search in Google Scholar

Cole, L.C. 1956. The population consequence of life-history phenomena, Q. Rev. BM. 29: 103–137. Search in Google Scholar

Destombe, C., J. Godin, M. Nocher, S. Richerd and M. Valero. 1993. Differences in responses between haploid and diploid isomorphic phases of Gracilaria verrucosa (Rhodophyta: Gigartinales) exposed to artificial environmentalconditions. In: Fourteenth International Seaweed Symposium, Springer, Netherlands. pp. 131–137. Search in Google Scholar

DeWreede, R.E. and T. Klinger. 1988. Reproductive strategies in algae. Oxford University Press, New York. pp. 267. Search in Google Scholar

Dijoux, L., F. Viard and C. Payri. 2014. The more we search, the more we find: discovery of a new lineage and a new species complex in the genus Asparagopsis. PLoS One 9: e103826.10.1371/journal.pone.0103826 Search in Google Scholar

Edyvean, R.G.J. and H. Ford. 1984. Population biology of the crustose red alga Lithophyllurn incrustans Phil. 2. A comparison of populations from three areas of Britain. Biol. J. Lin. Soc. 23: 353–363.10.1111/j.1095-8312.1984.tb00151.x Search in Google Scholar

Eggert, A. 2012. Seaweed responses to temperature. In: (C. Wiencke and K. Bischof, eds.) Seaweed biology. Springer, Berlin Heidelberg. pp. 47–66. Search in Google Scholar

Fralick, R.A. and A.C. Mathieson. 1973. Ecological studies of Codium fragile in New England, USA. Mar. Biol. 19: 127–132.10.1007/BF00353583 Search in Google Scholar

Guiry, M.D. and C.J. Dawes. 1992. Daylength, temperature and nutrient control of tetrasporogenesis in Asparagopsis armata. Rhodophyta. J. Exp. Mar. Biol. Ecol. 158: 197–217.10.1016/0022-0981(92)90227-2 Search in Google Scholar

Harvey, W.H. 1855. Some account of the marine botany of the colony of Western Australia. Trans. R. Ir. Acad. 22: 525–566. Search in Google Scholar

Hurd, C.L., P.J. Harrison, K. Bischof and C.S. Lobban. 2014. Seaweed ecology and physiology. Cambridge University Press, London. pp. 551. Search in Google Scholar

Kennedy, T.A., S. Naeem, K.M. Howe, J.M.H. Knops, D. Tilman and P. Reich. 2002. Biodiversity as a barrier to ecological invasion. Nature 417: 636–638.10.1038/nature00776 Search in Google Scholar

Klinkhamer, P.G.L., T.J. de Jong and E. Meelis. 1990. How to test for proportionality in the reproductive effort of plants. Am. Nat. 135: 291–300.10.1086/285045 Search in Google Scholar

Lee, R.E. 2008. Phycology, 4th edition. Cambridge University Press, New York. pp. 547. Search in Google Scholar

Littler, M.M. and D.S. Littler. 1980. The evolution of the thallus form and survival strategies in benthic marine macroalgae: field and laboratory test from a functional form model. Am. Nat. 116: 25–44.10.1086/283610 Search in Google Scholar

Mairh, O.P. 1977. Studies on Asparagopsis taxiformis Delile Collins and Harvey from Indian waters. J. Mar. Biol. Assoc. India. 19: 97–106. Search in Google Scholar

Mathieson, A.C. and Z. Guo. 1992. Patterns of fucoid reproductive biomass allocation. Br. Phycol. J. 27: 271–292.10.1080/00071619200650261 Search in Google Scholar

Monro, K. and A.G. Poore. 2009. The potential for evolutionary responses to cell-lineage selection on growth form and its plasticity in a red seaweed. Am. Nat. 173: 151–163.10.1086/595758 Search in Google Scholar

Ní Chualáin, F., C. Maggs, G.W. Saunders and M.D. Guiry. 2004. The Invasive Genus Asparagopsis. bonnemaisoniaceae, rhodophyta: molecular systematics, morphology, and ecophysiology of Falkenbergia isolates. J. Phycol. 40: 1112–1126.10.1111/j.1529-8817.2004.03135.x Search in Google Scholar

Plouguerné, E., K. Le Lann, S. Connan, G. Jechoux, E. Deslandes and V. Stiger-Pouvreau. 2006. Spatial and seasonal variation in density, reproductive status, length and phenolic content of the invasive brown macroalga Sargassum muticum (Yendo) Fensholt along the coast of Western Brittany (France). Aq. Bot. 85: 337–344.10.1016/j.aquabot.2006.06.011 Search in Google Scholar

Reekie, E.G. and F.A. Bazzaz. 1987. Reproductive effort in plants. 1. Carbon allocation to reproduction. Am. Nat. 129: 876–896.10.1086/284681 Search in Google Scholar

Robertson, B.L. 1987. Reproductive ecology and canopy structure of Fucus spiralis L. Bot. Mar. 30: 475–482. Search in Google Scholar

Rojas, J., A. Lemus and E.K. Ganesan. 1982. El ciclo vital “in vitro” del alga marina roja Asparagopsis taxiformis (Bonnemaisoniales, Rhodophyta). Venezuela, Universidad de Oriente. Bol. Inst. Ocean. 21: 101–112. In Spanish. Search in Google Scholar

Sakai, A.K., F.W. Allendorf, J.S. Holt, D.M. Lodge, J. Molofsky, K.A. With, S. Baughman, R.J. Cabin, J.E. Cohen, N.C. Ellstrand, D.E. McCauley, P. O‘Neil, I.M. Parker, J.N. Thompson and S.G. Weller. 2001. The population biology of invasive species. Annu. Rev. Ecol. Syst. 32: 305–332.10.1146/annurev.ecolsys.32.081501.114037 Search in Google Scholar

Samson, D.A. and K.S. Werk. 1986. Size-dependent effects in the analysis of reproductive effort in plants. Am. Nat. 127: 667–680.10.1086/284512 Search in Google Scholar

Santelices, B. 1990. Patterns of reproduction, dispersal and recruitment in seaweeds. Oceanogr. Mar. Biol. Ann. Rev. 28: 177–276. Search in Google Scholar

Sokal, R.R. and F.J. Rohlf. 1969. Single classification analysis of variance. Biometry. In: (R. Emerson, D. Kennedy and R. Park, eds.) The principles and practice of statistics in biological research. W.H. Freeman, San Francisco. pp. 249. Search in Google Scholar

Stachowicz, J.J., H. Fried, R.W. Osman and R.B. Whitlatch. 2002. Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83: 2575–2590.10.1890/0012-9658(2002)083[2575:BIRAME]2.0.CO;2 Search in Google Scholar

Streftaris, N. and A. Zenetos. 2006. Alien marine species in the Mediterranean-the 100 “worst invasives” and their impact. Mediterr. Mar. Sci. 7: 87–118.10.12681/mms.180 Search in Google Scholar

Tala, F. and F. Chow. 2014. Phenology and photosynthetic performance of Porphyra sp. (Bangiophyceae, Rhodophyta): seasonal and latitudinal variation in Chile. Aq. Bot. 113: 107–116.10.1016/j.aquabot.2013.11.005 Search in Google Scholar

Tsiamis, K. and P. Panayotidis. 2007. First record of the red alga Asparagopsis taxiformis (Delile) Trevisan de Saint-Léon in Greece. Aq. Inv. 2: 435–438.10.3391/ai.2007.2.4.14 Search in Google Scholar

Viejo, R.M., B. Martínez, J. Arrontes, C. Astudillo and L. Hernández. 2011. Reproductive patterns in central and marginal populations of a large brown seaweed: drastic changes at the southern range limit. Ecography. 34: 75–84.10.1111/j.1600-0587.2010.06365.x Search in Google Scholar

Vijayaraghavan, M.R. and B. Bhatia. 1997. Red algae: structure, ultrastructure and reproduction. APH Publishing Corporation, New Delhi. Vol. 2. pp. 306. Search in Google Scholar

Zanolla, M., R. Carmona, J. De la Rosa, N. Salvador, A.R. Sherwood, N. Andreakis and M. Altamirano. 2014. Morphological differentiation of cryptic lineages within the invasive genus Asparagopsis (Bonnemaisoniales, Rhodophyta). Phycologia 53: 233–242.10.2216/13-247.1 Search in Google Scholar

Zanolla, M., M. Altamirano, R. Carmona, J. De la Rosa, A.R. Sherwood and N. Andreakis. 2015. Photosynthetic plasticity of the genus Asparagopsis (Bonnemaisoniales, Rhodophyta) in response to temperature: implications for invasiveness. Biol. Inv. 17: 1341–1353.10.1007/s10530-014-0797-8 Search in Google Scholar

Zanolla, M., M. Altamirano, J. De la Rosa, F.X. Niell and R. Carmona. 2017a. Size structure and dynamics of an invasive population of lineage 2 of Asparagopsis taxiformis (Florideophyceae) in the Alborán Sea. Phycol. Res. DOI: 10.1111/pre.12189. Search in Google Scholar

Zanolla, M., M. Altamirano, R. Carmona, J. De la Rosa, V. Souza-Egipsy, A.R. Sherwood, K. Tsiamis, A.M. Barbosa, A.R. Muñoz and N. Andreakis. 2017b. Assessing global range expansion in a cryptic species complex: insights from the red seaweed genus Asparagopsis (Florideophyceae). J. Phycol. doi: 10.1111/jpy.12598-17-015. Search in Google Scholar

Zhang, Q.S., W. Li, S. Liu and J.H. Pan. 2009. Size-dependence of reproductive allocation of Sargassum thunbergii (Sargassaceae, Phaeophyta) in Bohai Bay, China. Aq. Bot. 91: 194–198.10.1016/j.aquabot.2009.06.003 Search in Google Scholar

Received: 2017-4-2
Accepted: 2017-10-12
Published Online: 2017-11-21
Published in Print: 2017-11-27

©2017 Walter de Gruyter GmbH, Berlin/Boston