Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species
-
Camilo López-Cristoffanini
, Florence Tellier , Ricardo Otaíza , Juan A. Correa and Loretto Contreras-Porcia
Abstract
Tolerance to air exposure should be an important feature in determining the geographic distribution of seaweeds. Two sibling kelp species with contrasting latitudinal distributions were selected to test the relationship between their distribution and air exposure tolerance: Lessonia berteroana distributed between 18° and 30°S and Lessonia spicata, which is found from 29° to 41°S along the Chilean coast. This region presents a latitudinal gradient of environmental variables, which leads to an increase in air exposure as latitude decreases. Therefore, populations of L. spicata are likely to be exposed to lower desiccation levels than those of L. berteroana. To assess adaptation to air exposure, early stages of development of these species were exposed to air daily for 0, 0.5, 1, and 2 h, and the activities of two antioxidant enzymes (ascorbate peroxidase and catalase) were measured. Results showed that L. spicata spores ceased their postgermination development when exposed to 1 and 2 h of air, contrasting with L. berteroana, in which spore development was not abruptly stopped as for L. spicata. In addition, the apparent inactivation of the antioxidant enzyme catalase in both species strongly suggests a lower buffering capacity to an excess of reactive oxygen species (ROS) triggered by air exposure. Thus, air exposure seems an important factor determining the northern geographic limit of L. spicata.
This work was supported by FONDECYT 11085019 and FONDECYT 1120117 to L.C-P. Additional funding came from FONDECYT 11121504 grant and from the UCSC Dirección de Investigación to F.T., FONDAP 1501-0001 (CONICYT) to the Center for Advanced Studies in Ecology and Biodiversity (CASEB) Program 7, and ICA grant to J.C. Collaborative work was done within the framework of the GDRI “Diversity, Evolution and Biotechnology of Marine Algae “DEBMA.” We are especially grateful to C. Lovazzano, E. Guajardo, C. Sordet, M. R. Flores-Molina, and the Chango-Lab for field assistance, to J. Beltrán, D. Thomas, and L. Hiriart-Bertrand for help in culture work, to V. Flores for imaging acquisition and to B. Broitman, L. Chaparro, M. Valero, and N. Valdivia for their valuable suggestion in statistical and climatic analyses. We particularly appreciate the constructive comments from the Editor and from two anonymous reviewers that helped improve the manuscript.
References
Alpert, P. 2005. The limits and frontiers of desiccation-tolerant life. Integr. Comp. Biol. 45: 685–695.10.1093/icb/45.5.685Search in Google Scholar
Asada, K. 1999. The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu. Rev. Plant Physiol. 50: 601–639.10.1146/annurev.arplant.50.1.601Search in Google Scholar
Avila, M., A.J. Hoffmann and B. Santelices. 1985. Interacciones de temperatura, densidad de flujo fotónico y fotoperiodo sobre el desarrollo de etapas microscópicas de Lessonia nigrescens (Phaeophyta, Laminariales). Rev. Chil. Hist. Nat. 58: 71–82.Search in Google Scholar
Bell, E.C. 1993. Photosynthetic response to temperature and desiccation of the intertidal alga Mastocarpus papillatus. Mar. Biol. 117: 337–346.10.1007/BF00345679Search in Google Scholar
Bergey, E.A., P. Bunlue, S. Silalom, D. Thapanya and P. Chantaramongkol. 2010. Environmental and biological factors affect desiccation tolerance of algae from two rivers (Thailand and New Zealand) with fluctuating flow. J. N. Am. Benthol. Soc. 29: 725–736.10.1899/09-068.1Search in Google Scholar
Bickford, D., D.J. Lohman, N.S. Sodhi, P.K.L. Ng, R. Meier, K. Winker, K.K. Ingram and I. Das. 2006. Cryptic species as a window on diversity and conservation. Trends Ecol. Evol. 22: 148–155.10.1016/j.tree.2006.11.004Search in Google Scholar
Blokhina, O., E. Virolainen and K.V. Fagerstedt. 2003. Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann. Bot. 91: 179–194.Search in Google Scholar
Burritt, D.J., J. Larkindale and C.L Hurd. 2002. Antioxidant metabolism in the intertidal red seaweed Stictosiphonia arbuscula following desiccation. Planta 215: 829–838.10.1007/s00425-002-0805-6Search in Google Scholar
Casey, K.S. and P. Cornillon. 1999. A comparison of satellite and in situ-based sea surface temperature climatologies. J. Climate 12: 1848–1863.10.1175/1520-0442(1999)012<1848:ACOSAI>2.0.CO;2Search in Google Scholar
Collén, J. and I.R. Davison. 1999a. Reactive oxygen production and damage in intertidal Fucus spp. (Phaeophyceae). J. Phycol. 35: 54–61.10.1046/j.1529-8817.1999.3510054.xSearch in Google Scholar
Collén, J. and I.R. Davison. 1999b. Reactive oxygen metabolism in intertidal Fucus spp. (Phaeophyceae). J. Phycol. 35: 62–69.10.1046/j.1529-8817.1999.3510062.xSearch in Google Scholar
Compo, G.P., J.S. Whitaker, P.D. Sardeshmukh, N. Matsui, R.J. Allan, X. Yin, B.E. Gleason, R.S. Vose, G. Rutledge, P. Bessemoulin, S. Brönnimann, M. Brunet, R.I. Crouthamel, A.N. Grant, P.Y. Groisman, P.D. Jones, M. Kruk, A.C. Kruger, G.J. Marshall, M. Maugeri, H.Y. Mok, Ø. Nordli, T.F. Ross, R.M. Trigo, X.L. Wang, S.D. Woodruff and S.J. Worley. 2011. The Twentieth Century Reanalysis Project. Q. J. R. Meteorol. Soc. 137: 1–28.10.1002/qj.776Search in Google Scholar
Contreras, L., A. Moenne and J.A. Correa. 2005. Antioxidant responses in Scytosiphon lomentaria (Phaeophyceae) inhabiting copper-enriched coastal environments. J. Phycol. 41: 1184–1195.10.1111/j.1529-8817.2005.00151.xSearch in Google Scholar
Contreras, L., M.H. Medina, S. Andrade, V. Oppliger and J.A. Correa. 2007. Effects of copper on early developmental stages of Lessonia nigrescens Bory (Phaeophyceae). Environ. Pollut. 145: 75–83.10.1016/j.envpol.2006.03.051Search in Google Scholar PubMed
Contreras, L., D. Mella, A. Moenne and J.A. Correa. 2009. Differential responses to copper-induced oxidative stress in the marine macroalgae Lessonia nigrescens and Scytosiphon lomentaria (Phaeophyceae). Aquat. Toxic. 94: 94–102.10.1016/j.aquatox.2009.06.004Search in Google Scholar PubMed
Contreras-Porcia, L., D. Thomas, V. Flores and J.A. Correa. 2011. Tolerance to oxidative stress induced by desiccation in Porphyra columbina (Bangiales, Rhodophyta). J. Exp. Bot. 62: 1815–1829.10.1093/jxb/erq364Search in Google Scholar PubMed PubMed Central
Contreras-Porcia, L., S. Callejas, D. Thomas, C. Sordet, G. Pohnert, A. Contreras, A. Lafuente, M.R. Flores-Molina and J.A. Correa. 2012. Seaweeds early development: detrimental effects of desiccation and attenuation by algal extracts. Planta 235: 337–348.10.1007/s00425-011-1512-ySearch in Google Scholar PubMed
Contreras-Porcia, L., C. López-Cristoffanini, C. Lovazzano, M.R. Flores-Molina, E. Guajardo, D. Thomas, A. Nuñez, J.A. Correa, M. Kube and R. Reinhardt. 2013. Differential gene expression in Pyropia columbina (Plantae, Rhodophyta) under natural hydration and desiccation stress. Lat. Am. J. Aquat. Res. 41: 933–958.Search in Google Scholar
Correa, J.A. and J.L. McLachlan. 1991. Endophytic algae of Chondrus crispus (Rhopophyta). III. Host specificity. J. Phycol. 27: 448–459.10.1111/j.0022-3646.1991.00448.xSearch in Google Scholar
Dorgelo, J. 1976. Intertidal fucoid zonation and desiccation. Aquat. Ecol. 10: 115–112.10.1007/BF02282219Search in Google Scholar
Dring, M.J. and F.A. Brown. 1982. Photosynthesis of intertidal brown algae during and after periods of emersion: a renewed search for physiological causes of zonation. Mar. Ecol. Prog. Ser. 8: 301–308.10.3354/meps008301Search in Google Scholar
Druehl, L.D. and J.M. Green. 1982. Vertical distribution of intertidal seaweeds as related to patterns of submersion and emersion. Mar. Ecol. Prog. Ser. 9: 163–170.10.3354/meps009163Search in Google Scholar
Finke, G.R., S.A. Navarrete and F. Bozinovic. 2007. Tidal regimes of temperate coasts and their influences on aerial exposure for intertidal organisms. Mar. Ecol. Prog. Ser. 343: 57–62.10.3354/meps06918Search in Google Scholar
Foyer, C.H. and G. Noctor. 2009. Redox regulation in photosynthetic organisms: signaling, acclimation, and practical implications. Antiox. Redox Signal. 11: 861–905.Search 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.Search in Google Scholar
Helmuth, B., B.R. Broitman, C.A. Blanchette, S. Gilman, P. Halpin, C.D.G. Harley, M.J. O’Donnell, G.E. Hofmann, B. Menge and D. Strickland. 2006. Mosaic patterns of thermal stress in the rocky intertidal zone: implications for climate change. Ecol. Monogr. 76: 461–479.10.1890/0012-9615(2006)076[0461:MPOTSI]2.0.CO;2Search in Google Scholar
Lovazzano, C., S. Andrade, C. Serrano, J.A. Correa and L. Contreras-Porcia. 2013. Comparative analysis of the peroxiredoxin activation in the brown macroalgae Scytosiphon gracilis and Lessonia nigrescens (Phaeophyceae) under copper stress. Physiol. Plant. 149: 378–388.10.1111/ppl.12047Search in Google Scholar
Martínez, EA. 1999. Latitudinal differences in thermal tolerance among microscopic sporophytes of the kelp Lessonia nigrescens (Phaeophyta: Laminariales). Pac. Sci. 53: 74–81.Search in Google Scholar
Mislan, K.A.S., D.S. Wethey and B. Helmuth. 2009. When to worry about the weather: role of tidal cycle in determining patterns of risk in intertidal ecosystems. Glob. Change Biol. 15: 3056–3065.10.1111/j.1365-2486.2009.01936.xSearch in Google Scholar
Noctor, G. and C.H. Foyer. 1998. Ascorbate and glutathione: keeping active oxygen under control. Annu. Rev. Plant Physiol. Plant Mol. Biol. 49: 249–279.10.1146/annurev.arplant.49.1.249Search in Google Scholar
Oppliger, L.V., J.A. Correa, S. Faugeron, J. Beltrán, F. Tellier, M. Valero and C. Destombe. 2011. Sex ratio variation in the Lessonia nigrescens complex (Laminariales, Phaeophyceae): effect of latitude, temperature and marginality. J. Phycol. 47: 5–12.Search in Google Scholar
Oppliger, L.V., J.A. Correa, A.H. Engelen, F. Tellier, V. Vieira, S. Faugeron, M. Valero, G. Gomez and C. Destombe. 2012. Temperature effects on gametophyte life-history traits and geographic distribution of two cryptic kelp species. PLoS One 7: e39289.10.1371/journal.pone.0039289Search in Google Scholar
Ratkevicius, N., J.A. Correa and A. Moenne. 2003. Copper accumulation, synthesis of ascorbate and activation of ascorbate peroxidase in Enteromorpha compressa (L) Grev. (Chlorophyta) from heavy metal-enriched environments in northern Chile. Plant Cell Environ. 26: 1599–1608.Search in Google Scholar
Repetto, G., A. Peso and J.L. Zurita. 2008. Neutral red uptake assay for the estimation of cell viability/cytotoxicity. Nat. Prot. 3: 7.10.1038/nprot.2008.75Search in Google Scholar
Schagerl, M. and Möstl, M. 2011. Drought stress, rain and recovery of the intertidal seaweed Fucus spiralis. Mar. Biol. 158: 2471–2479.Search in Google Scholar
Sexton, J.P., P.J. McIntyre, A.L. Angert and K.J. Rice. 2009. Evolution and ecology of species range limits. Annu. Rev. Ecol. Evol. Syst. 40: 415–436.10.1146/annurev.ecolsys.110308.120317Search in Google Scholar
Smith, C.M. and J.A. Berry. 1986. Recovery of photosynthesis after exposure of intertidal algae to osmotic and temperature stresses: comparative studies of species with differing distributional limits. Oecologia 70: 6–12.10.1007/BF00377105Search in Google Scholar
Smith, P.K., R.I. Krohn, G.T. Hermanson, A.K. Mallia, F.H. Garthner, M.D. Provenzano, E.K. Fujimoto, N.M. Goeke, B.J. Olson and D.C. Klenk. 1985. Measurement of protein using bicinchoninic acid. Anal. Biochem. 150: 76–85.10.1016/0003-2697(85)90442-7Search in Google Scholar
Steneck, R.S., M.H. Graham, B.J. Bourque, D. Corbett, J.M. Erlandson, J.A. Estes and M.J. Tegner. 2002. Kelp forest ecosystems: biodiversity, stability, resilience and future. Environ. Conserv. 29: 436–459.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
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.Search in Google Scholar
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. 42: 455–465.Search in Google Scholar
Thiel, M., E.C. Macaya, E. Acuña, W.E. Arntz, H. Bastias, K. Brokordt, P.A. Camus, J.C. Castilla, L.R. Castro, M. Cortés, C.P. Dumont, R. Escribano, M. Fernandez, J.A. Gajardo, C.F. Gaymer, I. Gomez, A.E. González, H.E. González, P.A. Haye, J.E. Illanes, J.L. Iriarte, D.A. Lancellotti, G. Luna-Jorquera, C. Luxoro, P.H. Manriquez, V. Marín, P. Muñoz, S.A. Navarrete, E. Perez, E. Poulin, J. Sellanes, H.H. Sepúlveda, W. Stotz, F. Tala, A. Thomas, C.A. Vargas, J. Vásquez and J.M.A. Vega. 2007. The Humboldt Current System of northern and central Chile. Oceanogr. Mar. Biol. Annu. Rev. 45: 195–134.10.1201/9781420050943.ch6Search in Google Scholar
Underwood, A. J. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge University Press, Cambridge, UK. pp. 504.Search in Google Scholar
Zar, J.H. 2010. Biostatistical analysis. 5th Edition. Pearson Prentice-Hall, Upper Saddle River, NJ. pp. 960.Search in Google Scholar
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Articles in the same Issue
- Masthead
- Masthead
- Research articles
- Ecological dynamics of Zostera marina (eelgrass) in three adjacent bays in Atlantic Canada
- Historical and present distribution of Zostera marina in the high north (Troms County, northern Norway) – a decline over the last century
- Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species
- Colpomenia bullosa crust (Phaeophyceae) stressed less by grazing than by abiotic factors in high intertidal rockpools in southeast Australia
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- The first record of Grateloupia subpectinata from the New Zealand region and comparison with G. prolifera, a species endemic to the Chatham Islands
- Neosiphonia baliana sp. nov. and N. silvae sp. nov. (Rhodomelaceae, Rhodophyta) from Bali, Indonesia
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- Morphology and life stages of the potentially pinnatoxin-producing thecate dinoflagellate Vulcanodinium rugosum from the tropical Mexican Pacific
- Short communication
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Articles in the same Issue
- Masthead
- Masthead
- Research articles
- Ecological dynamics of Zostera marina (eelgrass) in three adjacent bays in Atlantic Canada
- Historical and present distribution of Zostera marina in the high north (Troms County, northern Norway) – a decline over the last century
- Tolerance to air exposure: a feature driving the latitudinal distribution of two sibling kelp species
- Colpomenia bullosa crust (Phaeophyceae) stressed less by grazing than by abiotic factors in high intertidal rockpools in southeast Australia
- Assessment of Fucus virsoides distribution in the Gulf of Trieste (Adriatic Sea) and its relation to environmental variables
- Long-term changes in sublittoral macroalgal assemblages related to water quality improvement
- Linking macroalgal δ15N-values to nitrogen sources and effects of nutrient stress on coral condition in an upwelling region
- Non-coralline crustose algae associated with maerl beds in Portugal: a reappraisal of their diversity in the Atlantic Iberian beds
- Hydrolithon abyssophila sp. nov. (Hydrolithoideae, Corallinales), a bisporic coralline from the insular shelf edge of Puerto Rico and the Virgin Islands (US)
- The first record of Grateloupia subpectinata from the New Zealand region and comparison with G. prolifera, a species endemic to the Chatham Islands
- Neosiphonia baliana sp. nov. and N. silvae sp. nov. (Rhodomelaceae, Rhodophyta) from Bali, Indonesia
- Effects of density and substrate type on recruitment and growth of Pyropia torta (Rhodophyta) gametophytes
- Morphology and life stages of the potentially pinnatoxin-producing thecate dinoflagellate Vulcanodinium rugosum from the tropical Mexican Pacific
- Short communication
- Fungal endophytes of the seagrasses Halodule wrightii and Thalassia testudinum in the north-central Gulf of Mexico