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MS11-Mmar Delebecq.Pdf Cah. Biol. Mar. (2011) 52 : In situ photosynthetic performance of Laminaria digitata (Phaeophyceae) during spring tides in Northern Brittany Gaspard DELEBECQ1,2,3,4, Dominique DAVOULT3,4, Dominique MENU2, Marie-Andrée JANQUIN1,2, Aline MIGNÉ3,4, Jean-Claude DAUVIN5 and François GEVAERT1,2 (1)Université Lille1, Univ Lille Nord de France, Station Marine, F-62930 Wimereux, France Fax 00 33 21 99 29 01. E-mail: [email protected] (2) CNRS, UMR 8187 LOG, F-62930 Wimereux, France (3) UPMC Univ Paris 06, Station Biologique, F-29680 Roscoff, France (4) CNRS, UMR 7144 AD2M, F-29680 Roscoff, France (5) Université de Caen Basse Normandie, Laboratoire Morphodynamique Continentale et Côtière, UMR CNRS 6143 M2C, 2-4 rue de Tilleuls, F-14000 Caen, France Abstract: The ability of Laminaria digitata (Hudson) J.V. Lamouroux to cope with rapid and drastic changes in light was studied in the field by measuring photosystem II fluorescence, net oxygen production and pigment content. Experiments were conducted during two spring tides of late spring in Northern Brittany where low spring tides occur around noon. Daily patterns of the photosynthetic performance of Laminaria digitata were observed in relation to changes in incident under- water light. Photoinhibitory light exposure induced a sharp decrease of the optimal quantum yield (Fv/Fm), a decline of the net oxygen production in the first of the two spring tides investigated and a concomitant increase in the de-epoxidation ratio of the Violaxanthin pool. Photoinhibition persisted at a lower extent at the end of the day and complete recovery was achieved during the night. The implications of the photoinhibition of photosynthesis of Laminaria digitata are discussed in relation to the natural ambient conditions experienced in the field. Résumé : Performances photosynthétiques in situ de Laminaria digitata (Phaeophyceae) au cours des marées de vives-eaux en Bretagne Nord. La capacité de Laminaria digitata (Hudson) J.V. Lamouroux à faire face aux variations rapides et prononcées de lumière a été étudiée in situ en mesurant la fluorescence du photosystème II, la production nette d’oxygène et les contenus pigmentaires. Les expériences ont été réalisées au cours de deux marées de vives-eaux en fin de printemps en Bretagne Nord, où les basses mers ont lieu au zénith. Des changements journaliers des performances photosynthétiques ont été observés en relation avec les éclairements perçus au cours de la journée. L’exposition à des éclairements photo - inhibants a entraîné une forte diminution du rendement quantique optimal (Fv/Fm), une diminution de la production nette d’oxygène au cours du premier des deux cycles de marées étudiés, en lien avec une augmentation du taux de dé- époxydation de la Violaxanthine. La photoinhibition a persisté en fin de journée et la restauration complète a été atteinte au cours de la nuit. Les implications du phénomène de photoinhibition de la photosynthèse de Laminaria digitata sont discutées en lien avec les conditions du milieu. Keywords: Kelp l Photoinhibition l Net oxygen production l Chlorophyll fluorescence l Xanthophyll cycle Reçu le 9 novembre 2010 ; accepté après révision le 28 mars 2011. Received 9 November 2010; accepted in revised form 28 March 2011. 2 PHOTOSyNTHESIS OF LAMINARIA DIGITATA Introduction (Huppertz et al., 1990) which protects the photosynthetic apparatus from excess of light. This down-regulation of Kelp beds are a major feature of temperate coastal PSII efficiency is associated with the setting up of photo- ecosystems. They constitute dense populations inhabiting protective mechanisms and is generally separated in two rocky shores from the low intertidal to the uppermost part processes. The first part which is called “dynamic photo - of subtidal areas. By their productivity (Mann, 1973) and inhibition” corresponds to the dissipation of excess energy structure, they largely contribute to the functioning of the from the PSII reaction centres as heat via the completely ecosystem. They bring basal source of marine food web reversible xanthophyll cycle (XC) in the Light Harvesting through bacterial-mediated degradation and provide shelter Complexes (LHC) of the PSII (Harker et al., 1999). The for a large diversity of organisms such as macroalgae and second part is called “chronic photoinhibition” and is macrofauna. Moreover, some kelp species, like Laminaria associated with the turn-over of the D1 protein, a subunit of digitata (Hudson) J.V. Lamouroux, are of particular interest the PSII core which is essential for the electron transfer. in the view of the alginate industry. Due to the recent The degradation of the protein D1 subunit inactivates the reduction in abundances of Laminaria digitata along the PSII allowing the wastage of the excess photons. The French coast of the English Channel (Gevaert et al., 2008) reversibility of the chronic part of photoinhibition depends many questions are arising on the consequences of a rapid on the balance between the rate of degradation and repair of environmental change on Laminaria digitata. As a photo - the D1 subunit (Critchley & Russell, 1994; Carr & Björk, autotroph, interactions of Laminaria digitata with light are 2007) and hence is slower than the dynamic phase. crucial in all aspects of the life cycle. Light will drive Photoinhibition was studied in large kelp species (Hanelt species composition, abundance and productivity (Gerard, et al., 1997; Gevaert et al., 2002; Altamirano et al., 2004) 1984) and thereby the vertical distribution of macroalgae mostly with Pulse-Amplitude-Modulated (PAM) (Markager & Sand-Jensen, 1992; Häder & Figueroa, 1997; fluorescence, which is recognized as a reliable and Roleda et al., 2006). Incident underwater light arriving on powerful tool. In situ measurements of oxygen production macroalgae is highly variable on many different time scales are scarcer due to the technical issues associated with the as it depends on the combination of the solar elevation, the deployment of large chamber with enough power supply weather, the optical properties of seawater (scattering and for mixing and renewal of the media for a complete tidal absorption processes) and the tidal elevation which plays a cycle. Very few studies report accurate rates of primary major role in coastal areas. Semi-diurnal tides drive productivity of macroalgae in the field during a complete complex schemes of tidal elevation throughout the year tidal cycle or a complete day (see Fairhead & Cheschire, with the alternation of spring/neap tide cycles. In Northern 2004 and references in). PAM fluorescence and oxygen Brittany, where low spring tides occur around noon, production measurements provide different but highly Laminaria digitata experiences drastic and rapid changes complementary results. When PAM fluorescence provides of light exposure. The questions that are arising are: how insight on the PSII efficiency and the rate of electron does Laminaria digitata cope with these rapid changes in transfer through PSII on a small part of the thallus, oxygen light and what are the incidences of those exposures on its production provides insight on the whole photosynthetic photosynthetic performance? processes including the activity of the Calvin cycle as well The ability to withstand high light exposure during as the total respiration of the whole entire sporophyte. consecutive days and to recover from it is crucial for In our study, we propose to combine these two preventing the formation of oxygen radicals and complementary techniques in order to bring a complete and maintaining a sufficient photosynthetic performance for accurate description of the photosynthetic pattern of ensuring a daily autotrophic carbon balance. This ability Laminaria digitata throughout a whole tidal cycle. We could be one of the major factors regulating the upper depth studied the daily photosynthetic activity of Laminaria limit of a species (Hanelt, 1998; Harker et al., 1999). digitata under the light conditions of two spring tides of Exposure to high light at noon can lead to a reduction in late spring using PAM fluorescence, oxygen production photosynthesis efficiency of macroalgae, a process called measurements and pigment analyses. The aim of the study photoinhibition (Long et al., 1994) and commonly observed was to elucidate (1) if photoinhibition of photosynthesis in the field (Henley et al., 1991; Hanelt et al., 1993; Hanelt, occurs in the field and (2) how Laminaria digitata copes 1998; Gevaert et al., 2003, Hanelt & Roleda, 2009). with it. This study was a part of the French program ANR These authors pointed out the occurrence of a diurnal ECOKELP and was used to determine if Laminaria pattern of photoinhibition and photosynthetic performances digitata present sufficient mechanisms to face the rapid in macroalgae in relation to the diurnal changes of incident changing light conditions in the field in order to further irradiances. Photoinihibition mainly corresponds to an predict its response to rapid environmental changes in active decrease in photosystem II (PSII) efficiency coastal areas. G. DELEBECQ, D. DAVOULT, D. MENU, M.-A. JANQUIN, A. MIGNÉ, J.-C. DAUVIN, F. GEVAERT 3 Materials and Methods where Ft is the steady-state level of the fluorescence under ’ ambient light and Fm the maximal level of fluorescence obtained using a 0.8 s saturating pulse (2500 µmol.m-2.s-1). Study site фPSII is used to calculate the rETR which is an indication of The photosynthetic performance of Laminaria digitata was overall photosynthesis
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