Abstract
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.
About the authors
Marianela Zanolla obtained her PhD in Biology at the University of Malaga (Spain) in the ALIAN (ALgas Invasoras de Andalucia, invasive algae from Andalucia) project. Her PhD focused mainly on Asparagopsis taxiformis and Caulerpa racemosa. Presently, Dr. Zanolla is a postdoctoral researcher for the project “A National Marine Biodiscovery Laboratory” at the National University of Ireland, Galway. For this project she deals with sampling and identification of algae, culturing seaweeds of economic interest and performing experiments aimed at optimizing the culture conditions of targeted metabolites in seaweeds.
Raquel Carmona is an Associate Professor at the Universidad de Málaga (Spain), where she received her PhD for her work on the metabolic responses of two rhodophytes to light quality. She enjoyed a postdoctoral contract at the University of Connecticut (USA) studying the use of seaweeds as biofilters in integrated aquaculture, and a postdoctoral grant on the ecophysiology of a commercial agarophyte at the Universidade do Algarve (Portugal). Her recent research has focussed on the ecophysiological responses of seaweeds to anthropogenic factors, such as nutrient enrichment and temperature and CO2 increase in marine ecosystems, and ecological aspects of macroalgal invasions in the Mediterranean Sea.
María Altamirano is a Professor of Botany at the Universidad de Málaga, Spain. She was awarded a PhD at the same University, which focused on the effects of UV on marine macroalgae, and afterwards did her postdoctoral research at Kobe University, Japan. Since 2003, she has been working as a Professor at Plant Biology Department focusing her research on biodiversity and ecophysiology of marine photosynthetic organisms, mainly seaweeds. Her recent research is concentrated on invasive seaweed species in the Mediterranean Sea and ecological adaptation of extremophyle photosynthesizers in acidic and hot spring waters. She is Secretary of the Spanish Phycological Society.
Acknowledgements
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.
References
Åberg, P. 1996. Patterns of reproductive effort in the brown alga Ascophyllum nodosum. Mar. Ecol. Progr. Ser. 138: 199–207.10.3354/meps138199Search 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. 235.10.1007/978-3-642-28451-9_12Search 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: 273–283.10.1080/0967026042000236436Search 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.xSearch 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.xSearch 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.12373Search in Google Scholar
Ang, P.O. Jr. 1992. Cost of reproduction in Fucus distichus. Mar. Ecol. Prog. Ser. 89: 25–35.10.3354/meps089025Search 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)90186-2Search 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: 392–402.10.2216/10-65.1Search 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: 209–216.10.1515/botm.1998.41.1-6.209Search 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: 265–272.10.1080/00364827.1993.10413540Search 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: http://www.kimvdlinde.com/professional/rma.html (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.1987.10410088Search 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. 31–50.10.1007/978-90-481-8569-6_3Search 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: 199–241.10.1007/BF02366043Search in Google Scholar
Byers, J.E. 2002. Physical habitat attribute mediates biotic resistance to non- indigenous species invasion. Oecologia. 130: 146–156.10.1007/s004420100777Search in Google Scholar PubMed
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.2009.10.007Search 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: 289–294.10.3354/meps163289Search 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: 103–137.10.1007/978-3-642-81046-6_21Search 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.0103826Search in Google Scholar PubMed PubMed Central
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.xSearch in Google Scholar
Eggert, A. 2012. Seaweed responses to temperature. In: (C. Wiencke and K. Bischof, eds.) Seaweed biology. Springer, Berlin Heidelberg. pp. 47–66.10.1007/978-3-642-28451-9_3Search 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/BF00353583Search 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)90227-2Search in Google Scholar
Harvey, W.H. 1855. Some account of the marine botany of the colony of Western Australia. Trans. R. Ir. Acad. 22: 525–566.10.5962/bhl.title.112433Search 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/nature00776Search in Google Scholar PubMed
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: 291–300.10.1086/285045Search 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: 25–44.10.1086/283610Search 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: 271–292.10.1080/00071619200650261Search 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: 151–163.10.1086/595758Search in Google Scholar PubMed
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.xSearch 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.2006.06.011Search in Google Scholar
Reekie, E.G. and F.A. Bazzaz. 1987. Reproductive effort in plants. 1. Carbon allocation to reproduction. Am. Nat. 129: 876–896.10.1086/284681Search in Google Scholar
Robertson, B.L. 1987. Reproductive ecology and canopy structure of Fucus spiralis L. Bot. Mar. 30: 475–482.10.1515/botm.1987.30.6.475Search 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.32.081501.114037Search 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: 667–680.10.1086/284512Search 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;2Search 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.180Search 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.2013.11.005Search 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.2007.2.4.14Search 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.xSearch 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: 233–242.10.2216/13-247.1Search 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/s10530-014-0797-8Search 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.12189.10.1111/pre.12189Search 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.12598-17-015.10.1111/jpy.12598-17-015Search 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.2009.06.003Search in Google Scholar
©2017 Walter de Gruyter GmbH, Berlin/Boston
