Home Spore dispersal in the intertidal kelp Lessonia spicata: macrochallenges for the harvested Lessonia species complex at microscales of space and time
Article
Licensed
Unlicensed Requires Authentication

Spore dispersal in the intertidal kelp Lessonia spicata: macrochallenges for the harvested Lessonia species complex at microscales of space and time

  • Gloria M. Parada

    Gloria M. Parada obtained her degree in Marine Biology from the Universidad de Valparaíso (Chile) and her MSc degree in Management of Marine Resources from CICIMAR-IPN (La Paz, BCS Mexico). Her research focused on several ecological aspects of the Laminariales and she worked for several years designing investment projects for small-scale farmers and small-scale fishermen of the Chilean coasts. At present, she works as a professional consultant for Visión Oceánica Ltd., in Santiago, Chile.

    , Florence Tellier

    Florence Tellier is an Assistant Professor at the Universidad Católica de la Santísima Concepcion, in Concepcion, Chile. She obtained her PhD in 2009 from the Pontificia Universidad Católica de Chile and the Université Pierre et Marie Curie (UPMC-Paris 6-Sorbonne Universités) under a joint PhD program. The present publication was drafted in collaboration with E. A. Martinez and G. M. Parada during her postdoctoral position at the Universidad Católica del Norte, in Coquimbo, Chile. Her research interests include speciation and dispersal and adaptation mechanisms in marine macroalgae with a particular focus on the evolutionary processes affecting Laminariales.

    and Enrique A. Martínez

    Enrique A. Martínez obtained his PhD from the Pontificia Universidad Católica where he worked on the ecology and evolution of microscopic stages of Chilean kelps. For 20 years he researched and published about the complex life history of seaweeds. Motivated by the disappearance of small-scale farmers and increasingly poor nutritional quality of human foods, he began to study the Andean plant Quinoa. Overharvesting pressures on kelp and new discoveries in kelp micro-evolutionary issues moved Enrique and his colleagues to reanalyze unpublished kelp data to provide novel insight for kelp management. He is an ad honorem head professor at the Universidad Católica del Norte and a CEAZA Associate Researcher.

    EMAIL logo
Published/Copyright: July 29, 2016

Abstract

The intertidal coast of Chile has two cryptic kelp species, Lessonia spicata and L. berteroana, which share closely situated, but not overlapping, high-energy habitats. Their populations recover slowly after major disturbances and massive mortalities, suggesting that dispersal from remnant populations is strongly limited. This low dispersal is also a factor that probably favours the speciation process. Understanding the limiting factors for spore dispersal is crucial. Here we evaluated 1. spore dispersal and spore dilution over distance, 2. if submersion in calm waters for a specific period of time is needed for the settlement of spores before exposure to water movement, and 3. duration of spore attachment ability. Results were consistent with the hypothesis of low-distance dispersal of spores: stained-spore dilution was high at short spatial scales (<4 m); spores settled quickly (1–2 min) even under constant water movement, but they lost the ability to attach rapidly (≤16 h). Water motion did not affect spore attachment to the substratum, a fact probably resulting from an adaptation to high energy intertidal habitats. The very low dispersal range of the spores may explain the strong genetic differentiation at small spatial scales, the speciation event that occurred within the Lessonia species complex and the slow recovery of L. berteroana after massive mortalities occurring with the 1982/1983 El Niño Southern oscillation event.

About the authors

Gloria M. Parada

Gloria M. Parada obtained her degree in Marine Biology from the Universidad de Valparaíso (Chile) and her MSc degree in Management of Marine Resources from CICIMAR-IPN (La Paz, BCS Mexico). Her research focused on several ecological aspects of the Laminariales and she worked for several years designing investment projects for small-scale farmers and small-scale fishermen of the Chilean coasts. At present, she works as a professional consultant for Visión Oceánica Ltd., in Santiago, Chile.

Florence Tellier

Florence Tellier is an Assistant Professor at the Universidad Católica de la Santísima Concepcion, in Concepcion, Chile. She obtained her PhD in 2009 from the Pontificia Universidad Católica de Chile and the Université Pierre et Marie Curie (UPMC-Paris 6-Sorbonne Universités) under a joint PhD program. The present publication was drafted in collaboration with E. A. Martinez and G. M. Parada during her postdoctoral position at the Universidad Católica del Norte, in Coquimbo, Chile. Her research interests include speciation and dispersal and adaptation mechanisms in marine macroalgae with a particular focus on the evolutionary processes affecting Laminariales.

Enrique A. Martínez

Enrique A. Martínez obtained his PhD from the Pontificia Universidad Católica where he worked on the ecology and evolution of microscopic stages of Chilean kelps. For 20 years he researched and published about the complex life history of seaweeds. Motivated by the disappearance of small-scale farmers and increasingly poor nutritional quality of human foods, he began to study the Andean plant Quinoa. Overharvesting pressures on kelp and new discoveries in kelp micro-evolutionary issues moved Enrique and his colleagues to reanalyze unpublished kelp data to provide novel insight for kelp management. He is an ad honorem head professor at the Universidad Católica del Norte and a CEAZA Associate Researcher.

Acknowledgments

We are grateful for the help provided by J.M. Bogdanovich, F. Ogalde, P. Martínez, E. Wieters and C. Buffet for field and laboratory experiments. Funds were provided through the following grants: DIPUC; IFS A/2497-1; FONDECYT 1990235, 11121504; IAI-SGP-024 and FONDAP-CASEB-Program 7. Comments and English corrections by G. Filloramo, L. Retamal, D. Prehn, L. Eaton, W. Kreger, M. Thiel, M. Dring, the editor, and by two anonymous reviewers are deeply appreciated. As well we thank L. Parada for the drawings and Maria Teresa and Nora Elena for hosting G.M. Parada and E.A. Martínez over the last months during which the manuscript was finished. We dedicate this work to Dr. Rafael Riosmena Rodríguez (Programa de Investigación en Botánica Marina, UABCS, La Paz, Mexico) who recently passed away.

References

Alberto, F., P.T. Raimondi, D.C. Reed, N.C. Coelho, R. Leblois, A. Whitmer and E.A. Serrão. 2010. Habitat continuity and geographic distance predict population genetic differentiation in giant kelp. Ecology 91: 49–56.10.1890/09-0050.1Search in Google Scholar PubMed

Anderson, E.K. and W.J. North. 1966. In situ studies of spore production and dispersal in the giant kelp Macrocystis. In: Young, E. G., McLochlan, J. L. (Eds.). Proceeding International Seaweed Symposium. Peregamon Press, Oxford, pp. 73–86.10.1016/B978-0-08-011841-3.50011-2Search in Google Scholar

Bixter, H.J. and H. Porse. 2011. A decade of change in the seaweed hydrocolloids industry. J. Appl. Phycol. 23: 321–335.10.1007/s10811-010-9529-3Search in Google Scholar

Bobadilla, M. and B. Santelices. 2005. Variations in the dispersal curves of macroalgal propagules from a source. J. Exp. Mar. Biol. Ecol. 327: 47–57.10.1016/j.jembe.2005.06.006Search in Google Scholar

Charters, A.C., M. Neushul and D. Coon. 1973. The effect of water motion on algal spore adhesion. Limnol. Oceanogr. 18: 884–896.10.4319/lo.1973.18.6.0884Search in Google Scholar

Cie, D.K., and M.S. Edwards. 2011. Vertical distribution of kelp zoospores. Phycologia 50: 340–350.10.2216/10-48.1Search in Google Scholar

Cohen S, S. Faugeron, E.A. Martínez, J.A. Correa, F. Viard, C. Destombe and M. Valero. 2004. Molecular identification of two sibling species among collections of Gracilaria chilensis (Rhodophyta, Gracilariales). J. Phycol.40: 742–747.10.1111/j.1529-8817.2004.03203.xSearch in Google Scholar

Dayton, P.K. 1973. Dispersion, dispersal and persistence of the annual intertidal alga, Postelsia palmaeformis Ruprecht. Ecology. 54: 433–438.10.2307/1934353Search in Google Scholar

Destombe, C., J. Godin, C. Lefebvre, O. Dehorter and P. Vernet. 1992. Differences in dispersal abilities of haploid and diploid spores of Gracilaria verrucosa (Gracilariales, Rhodophyta). Bot. Mar.35: 93–98.10.1515/botm.1992.35.2.93Search in Google Scholar

Edwards, M.S. and G. Hernández-Carmona. 2005. Delayed recovery of giant kelp near its southern range limit in the North Pacific following El Niño. Mar. Biol. 147: 273–279.10.1007/s00227-004-1548-7Search in Google Scholar

Engel, C.R., C. Destombe and M. Valero. 2004. Mating system and gene flow in the red seaweed Gracilaria gracilis: effects of haplo-diploid life history and intertidal rocky shore landscape on fine-scale genetic structure. Heredity 92: 289–298.10.1038/sj.hdy.6800407Search in Google Scholar PubMed

Faugeron, S., E.A. Martínez, J.A. Correa and C. Billot. 2005. Long-term copper mine waste disposal in northern Chile associated with gene flow disruption of the intertidal Lessonia nigrescens. Mar. Ecol. Prog. Ser. 288: 129–140.10.3354/meps288129Search in Google Scholar

Funk, D.J. and K.E. Omland. 2003. Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu. Rev. Ecol. Syst. 34: 397–423.10.1146/annurev.ecolsys.34.011802.132421Search in Google Scholar

González, A., J. Beltrán, L. Hiriart-Bertrand, V. Flores, B. de Reviers, J.A. Correa and B. Santelices. 2012. Identification of cryptic species in the Lessonia nigrescens complex (Phaeophyceae, Laminariales). J. Phycol.48: 1153–1165.10.1111/j.1529-8817.2012.01200.xSearch in Google Scholar PubMed

Hinojosa, I., M. Pizarro, M. Ramos and M. Thiel. 2010. Spatial and temporal distribution of floating kelp in the channels and fjords of southern Chile. Estuar. Coast. Shelf S. 87: 367–377.10.1016/j.ecss.2009.12.010Search in Google Scholar

Hoffmann, A. 1987. The arrival of seaweed propagules at the shore: a review. Bot. Mar. 30: 151–165.10.1515/botm.1987.30.2.151Search in Google Scholar

Irwin, D.E. 2002. Phylogeographic breaks without geographic barriers to gene flow. Evolution 56: 2383–2404.10.1111/j.0014-3820.2002.tb00164.xSearch in Google Scholar PubMed

Kendrick, G.A. and D.I. Walker. 1991. Dispersal distances for propagules of Sargassum spinuligerum (Sargassaceae, Phaeophyta) directly measured by vital staining and venturi suction sampling. Mar. Ecol. Prog. Ser. 79: 133–138.10.3354/meps079133Search in Google Scholar

Krueger-Hadfield, S.A., D. Roze, J.A. Correa, C. Destombe and M. Valero. 2015. O father where art thou? Paternity analyses in a natural population of the haploid–diploid seaweed Chondrus crispus. Heredity114: 185–194.10.1038/hdy.2014.82Search in Google Scholar PubMed PubMed Central

Kuo, C.H. and J.C. Avise. 2005. Phylogeographic breaks in low-dispersal species: the emergence of concordance among gene trees. Genetica 124: 179–186.10.1007/s10709-005-2095-ySearch in Google Scholar PubMed

Ladah, L.B. and J.A. Zertuche-González. 2007. Survival of microscopic stages of a perennial kelp (Macrocystis pyrifera) from the center and the southern extreme of its range in the Northern Hemisphere after exposure to simulated El Niño stress. Mar. Biol. 152: 677–686.10.1007/s00227-007-0723-zSearch in Google Scholar

Lüning, K. and D.G. Müller. 1978. Chemical interaction in sexual reproduction of several Laminariales: release and attraction of spermatozoids. Z. Pflanzenphysiol. 89: 33–41.10.1016/S0044-328X(78)80006-3Search in Google Scholar

Macaya, E.C. and G.C. Zuccarello.2010a. DNA barcoding and genetic divergence in the giant kelp Macrocystis (Laminariales). J. Phycol. 46: 736–742.10.1111/j.1529-8817.2010.00845.xSearch in Google Scholar

Macaya, E.C. and G.C. Zuccarello. 2010b. Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar. Ecol. Prog. Ser. 420: 103–112.10.3354/meps08893Search in Google Scholar

Macaya, E.C., S. Boltaña, I.A. Hinojosa, J.E. Macchiavello, N.A. Valdivia, N.R. Vásquez, A.H. Buschmann, J.A. Vásquez, J.M.A. Vega and M. Thiel. 2005. Presence of sporophylls in floating kelp rafts of Macrocystis spp (Phaeophyceae) along the Chilean Pacific coast. J. Phycol. 41: 913–922.10.1111/j.1529-8817.2005.00118.xSearch in Google Scholar

Maggs, C. and M.E. Callow. 2003. Algal spores. In: eLS. John Wiley and Sons Ltd., Chichester. Available at http://www.els.net10.1038/npg.els.0000311.Search in Google Scholar

Martínez, E.A. 1999. Latitudinal differences in thermal tolerance among microscopic sporophytes of the kelp Lessonia nigrescens (Phaeophyta: Laminariales). Pacific Sci. 53: 74–81.Search in Google Scholar

Martínez, E. and J.A. Correa. 1993. Sorus-specific epiphytism affecting the kelps Lessonia nigrescens and L. trabeculata (Phaeophyta). Mar. Ecol. Prog. Ser. 96: 83–92.10.3354/meps096083Search in Google Scholar

Martínez, E.A. and B. Santelices. 1998. Selective mortality on haploid and diploid microscopic stages of Lessonia nigrescens Bory (Phaeophyta, Laminariales). J. Exp. Mar. Biol. Ecol. 229: 219–239.10.1016/S0022-0981(98)00063-XSearch in Google Scholar

Martínez, E.A., L. Cárdenas and R. Pinto. 2003. Recovery and genetic diversity of the intertidal kelp Lessonia nigrescens (Phaeophyceae) 20 years after El Niño 1982/83. J. Phycol. 39: 504–508.10.1046/j.1529-8817.2003.02191.xSearch in Google Scholar

Ojeda, F.P. and B. Santelices. 1984. Dominance of Lessonia nigrescens (Phaeophyta) in central Chile. Mar. Ecol. Prog. Ser. 19: 83–91.10.3354/meps019083Search in Google Scholar

Parada, G.M. 2001. Factores inhibitorios y facilitadores en el reclutamiento de Lessonia nigrescens (Bory 1826). Marine Biology degree thesis. Chile: Universidad de Valparaíso.Search in Google Scholar

Pearson, G.A. and E.A. Serrão. 2006. Revising synchronous gamete release by fucoid algae in the intertidal zone: fertilization success and beyond?. Integr. Comp. Biol. 46: 587–597.10.1093/icb/icl030Search in Google Scholar PubMed

Reed, D.C., D.R. Laut and A.W. Ebeling. 1988. Variation in algal dispersal and recruitment: the importance of episodic events. Ecol. Monogr. 58: 321–335.10.2307/1942543Search in Google Scholar

Reed, D.C., C.D. Amsler and A.W. Ebeling. 1992. Dispersal in kelps: factors affecting spore swimming and competency. Ecology 73: 1577–1585.10.2307/1940011Search in Google Scholar

Reed, D.C., M.A. Brezezinski, D.A. Coury, W.H. Graham and R.L. Petty. 1999. Neutral lipids in macroalgal spores and their role in swimming. Mar. Biol. 133: 737–744.10.1007/s002270050515Search in Google Scholar

Rothäusler, E., I. Gómez, I.A. Hinojosa, U. Karsten, L. Miranda, F. Tala and M. Thiel. 2011. Kelp rafts in the Humboldt Current: Interplay of abiotic and biotic factors limit their floating persistence and dispersal potential. Limnol. Oceanogr. 56: 1751–1765.10.4319/lo.2011.56.5.1751Search in Google Scholar

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

Santelices, B. and D. Aedo. 1999. Evaluating substances that facilitate algal spore adhesion. Hydrobiologia 398/399: 241–246.10.1007/978-94-011-4449-0_27Search in Google Scholar

Segovia, N.I., J.A. Vásquez, S. Faugeron and P.A. Haye. 2015. On the advantage of sharing a holdfast: effects of density and occurrence of kin aggregation in the kelp Lessonia berteroana. Mar. Ecol.36: 1107–1117.10.1111/maec.12206Search in Google Scholar

Sundene, O. 1962. The implications of transplant and culture experiment on the growth and distribution of Alaria esculenta. Nytt Mag. Bot. 9: 155–174.Search in Google Scholar

Tellier, F., A.P. Meynard, J.A. Correa, S. Faugeron and M. Valero. 2009. Phylogeographic analyses of the 30°S south-east Pacific biogeographic transition zone establish the occurrence of a sharp genetic discontinuity in the kelp Lessonia nigrescens: Vicariance or parapatry? Mol. Phylogenet. Evol. 53: 679–693.10.1016/j.ympev.2009.07.030Search in Google Scholar PubMed

Tellier, F., J. Tapia, S. Faugeron, C. Destombe and M. Valero. 2011a. The Lessonia nigrescens species complex (Laminariales, Phaeophyceae) shows strict parapatry and complete reproductive isolation in a secondary contact zone. J. Phycol. 47: 894–903.10.1111/j.1529-8817.2011.01019.xSearch in Google Scholar PubMed

Tellier, F., J.M.A. Vega, B.R. Broitman, J.A. Vásquez, M. Valero and S. Faugeron. 2011b. The importance of having two species instead of one in kelp management: the Lessonia nigrescens species complex. Cah. Biol. Mar. 52: 455–465.Search in Google Scholar

Valero, M., C. Destombe, S. Mauger, C. Ribout, C.R. Engel, C. Daguin-Thiébaut and F. Tellier. 2011. Using genetic tools for sustainable management of kelps: a literature review and the example of Laminaria digitata. Cah. Biol. Mar. 52: 467–483.Search in Google Scholar

Valero, M., C. Engel, C. Billot, B. Kloareg and C. Destombe. 2001. Concepts and issues of population genetics in seaweeds. Cah. Biol. Mar. 42: 53–62.Search in Google Scholar

Vega, J.M.A., B.R. Broitman and J.A. Vásquez. 2014. Monitoring the sustainability of Lessonia nigrescens (Laminariales, Phaeophyceae) in northern Chile under strong harvest pressure. J. Appl. Phycol. 26: 791–801.10.1007/s10811-013-0167-4Search in Google Scholar

Received: 2016-4-21
Accepted: 2016-6-30
Published Online: 2016-7-29
Published in Print: 2016-8-1

©2016 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 23.9.2025 from https://www.degruyterbrill.com/document/doi/10.1515/bot-2016-0034/html
Scroll to top button