Skip to main content

Photosynthetic performance and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) along a gradient of depth and seasonality in the ecoregion of Magellan, Chile

Abstract

Macrocystis pyrifera (L.) C. Agardh is a species that forms extensive underwater forests along the coastline of the ecoregion of Magellan. There, this alga is exposed to marked variation in photoperiod, temperature, and irradiance, which are modulated by daily and seasonal climatic variations. This study aims to understand the ecophysiological behavior of M. pyrifera, in a natural forest localized in Puerto del Hambre, Magellan Region of Chile, along spatial (depth) and temporal (season) gradients of physical drivers by analyzing algal responses in terms of the photosynthetic pigments and fluorescence yield. In the apical, middle, and basal fronds, the following photosynthetic parameters were seasonally measured: electron transport efficiency (α), maximum relative rate of electron transport (rETRmax), saturation point (E k ), and pigments such as chlorophyll a (Chl a), chlorophyll c (Chl c), and fucoxanthin. Both seasonal and stratified variations were observed. In autumn, α was decreased in the middle fronds (0.136 ± 0.030 (μmol photons m−2 s−1)−1) with respect to apical and basal fronds of autumn. For parameters such as E k , this decrease was observed relative to the depth gradient, with significant differences (p < 0.05) between distinct fronds. rETRmax was high in the apical fronds in spring, autumn, and winter. High Chl a concentration was maintained in all seasons, while the concentration of Chl c in the apical fronds tended to be lower. The concentration of fucoxanthin remained stable without significant differences between dissimilar types of fronds, for seasons (spring, summer, autumn, and winter). The Chl a/Chl c ratio increased with depth, while the Chl a/fucoxanthin ratio varies seasonally. Variations of light intensity in a natural population in a depth gradient and pigment variations in M. pyrifera with the depth stratification reveal the behavior of these algae in the ecoregion of Magellan where Chl a, through the apical fronds, could be regulating the photosynthetic activity of the plants at stratification level. Furthermore, the increase in Chl c and fucoxanthin towards the middle and basal fronds showed similar trends as those measured for α, thus signifying higher photosynthetic efficiency at greater depth. Overall, our results indicate marked seasonal and depth acclimation to different environmental conditions. This study is the first of its kind for the ecoregion of Magellan in which M. pyrifera represents a keystone species of utmost ecological significance.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

References

  • Anderson JM, Chow WS, Park YI (1995) The grand design of photosynthesis: acclimation of the photosynthetic apparatus to environmental cues. Photosynth Res 46:129–139

  • Becker S, Graeve M, Bishof K (2010) Photosynthesis and lipid composition of the Antarctic endemic rhodophyte Palmaria decipiens, effects of changing light, and temperature levels. Polar Biol 33:945–955

    Article  Google Scholar 

  • Beer S, Björk M, Beardall J (2014) Photosynthesis in the marine environment. Wiley, Oxford, pp 61–64

    Google Scholar 

  • Bozinovic F, Calosi P, Spicer J (2011) Physiological correlates of geographic range in animals. Annu Rev Ecol Evol Syst 42:155–179

    Article  Google Scholar 

  • Buschmann A, Pereda S, Varela D, Rodriguez J, López A, González L, Schilling M, Henríquez E, Hernández M (2014) Ecophysiological plasticity of annual populations of giant kelp (Macrocystis pyrifera) in a seasonally variable coastal environment in the Northern Patagonian Inner Seas of Southern Chile. J Appl Phycol 26:837–847

    Article  Google Scholar 

  • Cabello-Pasini A, Aguirre-von-Wobeser E, Figueroa F (2000) Photoinhibition of photosynthesis in Macrocystis pyrifera (Phaeophyceae), Chondrus crispus (Rhodophyceae) and Ulva lactuca (Chlorophyceae) in outdoor culture systems. J Photochem Photobiol 57:169–178

    CAS  Article  Google Scholar 

  • Castelo D, Trigueiro T, Colepicolo P, Marinho Soriano E (2012) Seasonal changes in the pigment composition of natural population of Gracilaria domingensis (Gracilariales, Rhodophyta). Braz J Pharmacog 22:874–880

  • Claudet J, Pelletier D, Jouvenel JY, Bachet F, Galzin R (2006) Assessing the effects of marine protected area (mpa) on a reef fish assemblage in a Northwestern Mediterranean marine reserve: identifying community-based indicators. Biol Conserv 130:349–369

    Article  Google Scholar 

  • Colombo-Pallotta M, García Mendoza E, Ladah L (2006) Photosynthetic performance, light absorption, and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) blades from different depths. J Phycol 42:1225–1234

    CAS  Article  Google Scholar 

  • Delgado-Vargas F, Jiménez A, Paredes-López O (2000) Natural pigments: carotenoids, anthocyanins, and betalains—characteristics, biosynthesis, processing, and stability. Crit Rev Food Sci Nutr 40:173–289

    CAS  Article  PubMed  Google Scholar 

  • Edwards M, Kim K (2010) Diurnal variation in relative photosynthetic performance in giant kelp Macrocystis pyrifera (Phaeophyceae, Laminariales) at different depths as estimated using PAM fluorometry. Aquat Bot 92:119–128

    CAS  Article  Google Scholar 

  • Fernandes F, Barbosa M, Oliveira AP, Azevedo IC, Sousa-Pinto I, Valentão P, Andrade PB (2016) The pigments of kelps (Ochrophyta) as part of the flexible response to highly variable marine environments. J Appl Phycol 28:3689–3696

    CAS  Article  Google Scholar 

  • Frank H, Chynwat V, Desamero R, Farhoosh R, Erickson J, Bautista J (1997) On the photophysics and photochemical properties of carotenoids and their role as light–harvesting pigments in photosynthesis. Pure Appl Chem 69:2117–2124

    CAS  Article  Google Scholar 

  • Gao K, Umezaki I (1988) Comparative photosynthetic capacities of the leaves of upper and lower parts of Sargassum plants. Bot Mar 31:231–236

    CAS  Article  Google Scholar 

  • Gerard V (1984) The light environment in a giant kelp forest: influence of Macrocystis pyrifera on spatial and temporal variability. Mar Biol 84:189–195

    Article  Google Scholar 

  • Graham M, Vasquez J, Buschmann A (2007) Global ecology of the giant kelp Macrocystis: from ecotypes to ecosystems. Oceanogr Mar Biol 45:39–88

    Google Scholar 

  • Griffiths M, Harrison S, Smit M, Maharajh D (2016) Major commercial products from micro–and macroalgae. In: Bux F, Chisti Y (eds) Algae biotechnology. Springer, Cham, pp 269–300

    Chapter  Google Scholar 

  • Guimarães SMPB (2003) Uma análise da diversidade da flora marinha bentônica do estado do Espírito Santo, Brasil. Hoehnea 30:11–19

    Google Scholar 

  • Gunnarsson K, Ingólfsonn A (1995) Seasonal changes in the abundance of intertidal algae in Southwestern Iceland. Bot Mar 38:69–77

    Article  Google Scholar 

  • Gupta S, Abu-Ghannam N (2011) Bioactive potential and possible health effects of edible brown seaweeds. Trends Food Sci Technol 22:315–326

    CAS  Article  Google Scholar 

  • Karsten U (2007) Research note: salinity tolerance of Arctic kelps from Spitsbergen. Phycol Res 55:257–262

    Article  Google Scholar 

  • Karsten U (2012) Seaweed acclimation to salinity and desiccation stress. In: Wiencke C, Bishoff K (eds) Seaweed biology. Springer, Berlin, pp 87–107

    Chapter  Google Scholar 

  • Kim S, Bhatnagar I (2011) Physical, chemical, and biological properties of wonder kelp—Laminaria. Adv Food Nutr Res 64:85

    CAS  Article  PubMed  Google Scholar 

  • Koch K, Thiel M, Hagen W, Graeve M, Gómez I, Jofre D, Hoffman L, Tala F, Bischof K (2016) Short and long term acclimation patterns of the giant kelp Macrocystis pyrifera (Laminariales, Phaeophyceae) along a depth gradient. J Phycol 52:260–273

    CAS  Article  PubMed  Google Scholar 

  • Lichtenthaler HK, Babani F (2004) Light adaptation and senescence of the photosynthetic apparatus. Changes in pigment composition, chlorophyll fluorescence parameters and photosynthetic activity. In: Papageorgiou GC, Govindjee (eds) Chlorophyll a fluorescence: a signature of photosynthesis. Springer, Dordrecht, pp 713–736

    Chapter  Google Scholar 

  • Macaya EC, Zucarello GC (2010) Genetic structure of the giant kelp Macrocystis pyrifera along the southeastern Pacific. Mar Ecol Prog Ser 420:103–112

    Article  Google Scholar 

  • Manley S (1984) Micronutrient uptake and translocation by Macrocystis pyrifera. J Phycol 20:192–201

    CAS  Article  Google Scholar 

  • Mansilla A, Palacios M, Aguilar S (2004) Efecto de la Salinidad en el Desarrollo Inicial de Sarcothalia Crispata (Bory) Leister (Rhodophyta, Gigartinales) Bajo Condiciones de Laboratorio. An Inst Patagonia 32:13–23

    Google Scholar 

  • Meléndez-Martínez A, Vicario I, Heredia F (2007) Pigmentos carotenoides: consideraciones estructurales y fisicoquímicas. Arch Latinoam Nutr 57:109–117

    PubMed  Google Scholar 

  • Ojeda J (2013) Dinámica estacional de macroalgas y moluscos intermareales y su relación con el conocimiento tradicional ecológico yagán, en canales subantárticos del Cabo de Hornos: una aproximación biocultural desde la filosofía ambiental de campo. Postgraduate Thesis, Universidad de Magellan, Punta Arenas, Chile, 145 pp

  • Ojeda J, Rosenfeld S, Marambio J, Rozzi R, Mansilla A (2014) Patrones estacionales y espaciales de la diversidad de moluscos intermareales de Bahía Róbalo, canal Beagle, Reserva de la Biosfera Cabo de Hornos, Chile. Rev Biol Mar Ocean 49(3):493–509

  • Pangestuti R, Kim S (2011) Biological activities and health benefit effects of natural pigments derived from marine algae. J Funct Foods 3:255–266

    CAS  Article  Google Scholar 

  • Platt T, Gallegos CL, Harrison WG (1980) Photoinhibition of photosynthesis in natural assemblages of marine phytoplankton. J Mar Res 38:687–701

    Google Scholar 

  • Quitral V, Morales C, Sepúlveda M, Schwartz M (2012) Propiedades nutritivas y saludables de algas marinas y su potencialidad como ingrediente funcional. Rev Chil Nutr 39:196–202

    Article  Google Scholar 

  • Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquat Bot 82:222–237

    CAS  Article  Google Scholar 

  • Ramlov F, de Souza J, Farias A, Maraschin M, Horta P, Yokoya N (2012) Effects of temperature, salinity, irradiance, and nutrients on the development of carposporelings and tetrasporophytes in Gracilaria domingensis (Kütz.) Sonder ex Dickie (Rhodophyta, Gracilariales). Bot Mar 55:253–259

    Article  Google Scholar 

  • Ramus J, Lemons F, Zimmerman C (1977) Adaptation of light-harvesting pigments to downwelling light and the consequent photosynthetic performance of the eulittoral rockweeds Ascophyllum nodosum and Fucus vesiculosus. Mar Biol 42:293–293

    CAS  Article  Google Scholar 

  • Rautenberger R, Bischof K (2016) Dynamic summer solar radiation in Antarctic coastal ecosystems and its effects on photosynthesis of the endemic Antarctic brown macroalga Desmarestia menziesii (Phaeophyceae). Algol Stud 151-152:123–150

  • Rautenberger R, Mansilla A, Gómez I, Wiencke C, Bischof K (2009) Photosynthetic responses to UV- radiation of intertidal macroalgae from the Strait of Magellan (Chile). Rev Chil Hist Nat 82:43–61

    Article  Google Scholar 

  • Reiskind JB, Madsen TV, Van Ginkel LC, Bowes G (1997) Evidence that inducible C4-type photosynthesis is a chloroplastic CO2- concentrating mechanism in Hydrilla, a submersed monocot. Plant Cell Environ 20:211–220

    CAS  Article  Google Scholar 

  • Rothäusler E, Gómez I, Hinojosa I, Karsten U, Tala F, Thiel M (2011a) Physiological performance of floating giant kelp Macrocystis pyrifera (Phaeophyceae): latitudinal variability in the effects of temperature and grazing1. J Phycol 47:269–281

    Article  PubMed  Google Scholar 

  • Rothäusler E, Gómez I, Karsten U, Tala F, Thiel M (2011b) Physiological acclimation of floating Macrocystis pyrifera to temperature and irradiance ensures long–term persistence at the sea surface at mid–latitudes. J Exp Mar Biol Ecol 405:33–41

    Article  Google Scholar 

  • Russell G (1986) Variation and natural selection in marine macroalgae. Oceanogr Mar Biol Annu Rev 24:309–377

    Google Scholar 

  • Seely GR, Duncan MJ, Vidaver WE (1972) Preparative and analytical extraction of pigments from brown algae with dimethyl sulfoxide. Mar Biol 12:184–188

    CAS  Article  Google Scholar 

  • Sexton J, McIntyre P, Angert RK (2009) Evolution and ecology of species range limits. Annu Rev Ecol Evol Syst 40:415–436

    Article  Google Scholar 

  • Skene K (2004) Key differences in photosynthetic characteristics of nine species of intertidal macroalgae are related to their position on the shore. Can J Bot 82:177–184

    Article  Google Scholar 

  • Vergara J (2003) Tipología y clasificación de fiordos y piedmonts submarinos de Magellan. Chile Invest Geogr Chile 37:21

    Google Scholar 

  • Wheeler WN (1980) Pigment content and photosynthetic of the frond of Macrocystis pyrifera. Mar Biol 56:97–102

    CAS  Article  Google Scholar 

  • Yokoya NS, Necchi O Jr, Martins AP, Gonzalez SF, Plastino EM (2007) Growth responses and photosynthetic characteristics of wild and phycoerythrin-deficient strains of Hypnea musciformis (Rhodophyta). J Appl Phycol 19:197–205

    CAS  Article  Google Scholar 

Download references

Acknowledgements

The authors wish to thank to the project FONDECYT 1140940 “Macroalgal adaptive radiation: potential links to ecological niche diversity in the ecoregion of Magallanes and Chilean Antarctic.” We are thankful for the graduate scholarships by the Institute of Ecology and Biodiversity granted to FM (ICM, P05-002) and JPR (ICM, P05-002) and to JM (PFB-23-2008) and SR (ICM P05-002).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to J. Marambio.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Marambio, J., Rodriguez, J.P., Mendez, F. et al. Photosynthetic performance and pigment composition of Macrocystis pyrifera (Laminariales, Phaeophyceae) along a gradient of depth and seasonality in the ecoregion of Magellan, Chile. J Appl Phycol 29, 2575–2585 (2017). https://doi.org/10.1007/s10811-017-1136-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10811-017-1136-0

Keywords

  • Macrocystis pyrifera
  • Phaeophyta
  • Eco-physiology
  • Sub-Antarctic region
  • Chile