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Photoinhibition in Common Atlantic Macroalgae Measured on Site in Gran Canaria

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Photoinhibition in Common Atlantic Macroalgae Measured on Site in Gran Canaria Helgol Mar Res (2001) 55:67–76 DOI 10.1007/s101520000066 ORIGINAL ARTICLE D.-P. Häder · M. Porst · M. Lebert Photoinhibition in common atlantic macroalgae measured on site in Gran Canaria Received: 18 January 2000 / Received in revised form: 15 May 2000 / Accepted: 19 May 2000 / Published online: 6 February 2001 © Springer-Verlag and AWI 2001 Abstract The photosynthetic quantum yield was analysed Introduction in four common atlantic macroalgae, the Rhodophytes Gelidium arbuscula and Halopithys incurvus and the About 50% of the primary biomass production on the Phaeophytes Halopteris scoparia and Lobophora variegata earth is based on aquatic ecosystems (Houghton and in Gran Canaria, Canary Islands at their growth site. Woodwell 1989; Siegenthaler and Sarmiento 1993). The fluorescence parameters were measured using a Most of the aquatic productivity is due to phytoplankton, portable pulse amplitude modulated (PAM) fluorometer however, macroalgae play an important role, especially (PAM 2000) instrument and a diving PAM under water in coastal areas. In addition to biomass productivity, without removing the thalli from their growth sites. Solar macroalgal forests serve as breeding grounds for fish, radiation was monitored continuously above and under mollusks and crustaceans. Macroalgae also have signifi- water during the whole experimental period using two cant economic potentials, being used in the production of three-channel dosimeters (European light dosimeter food for humans and animals, fertilizers and cosmetics, network; ELDONET) (Real Time Computer, Möhrendorf, to name only a few. Germany). These instruments measure solar radiation in Light is probably the most decisive factor in the three wavelength ranges, ultraviolet (UV)-A, UV-B and coastal environment which determines the vertical distri- photosynthetic active radiation (PAR). In all four algae bution of macroalgae (Lüning 1985). Sessile algae face a the effective photosynthetic quantum yield decreased serious stress when exposed to unfiltered solar irradiation significantly from the optimal values measured after and have been found to respond to this with reversible dark adaptation due to exposure to 15 min solar radiation, photoinhibition (Franklin and Forster 1997; Häder et al. but at least partially recovered subsequently in the shade 1998). Recent research has identified several other targets within several hours. Increasing the exposure period of short-wavelength solar radiation: damage to the water- to 30 min intensified the photoinhibition. In some algae splitting site and the reaction centre of photosystem II no recovery was observed after this treatment and in as well as cellular membranes (Murphy and Vu 1996). others no significant recovery could be detected. Expo- Another important target is the DNA where exposure to sure to unfiltered solar radiation caused a significantly solar ultraviolet (UV)-B radiation induces mainly thymine higher photoinhibition than PAR-only radiation or PAR dimers which cause mutations and permanent damage plus UV-A. A substantial inhibition was found in all if not removed by the repair-enzyme photolyase. This algae at their growth sites in the water column when enzyme is activated by long UV-A and blue light the sun was at high angles, as measured with the diving (Sommaruga et al. 1996). PAM. During events of photoinhibition the photosynthetic electron transport in photosystem II is actively decreased Keywords Gelidium arbuscula · Halopythis incurvus · (Trebst 1991) to protect the photosynthetic apparatus Halopteris scoparia · Lobophora variegata · from excessive solar energy. The underlying biochemical Pulse amplitude modulated fluorescence mechanism is radiation-induced damage to the D1 protein which is subsequently removed by a protease. During the recovery period the lost protein is replaced by newly D.-P. Häder (✉) · M. Porst · M. Lebert synthesized D1. Institut für Botanik und Pharmazeutische Biologie, Early investigations of photosynthesis in macroalgae Friedrich-Alexander-Universität Erlangen-Nürnberg, Staudtstrasse 5, 91058 Erlangen, Germany have been restricted to spectroscopic and gas exchange e-mail: [email protected] measurements (Field et al. 1989). Since the 1980s Tel.: +49-9131-8528216, Fax: +49-9131-8528215 the development of pulse amplitude modulation (PAM) 68 fluorescence has facilitated and supplemented the analysis water irradiances and calculate the transmission in the three indi- of important ecophysiological data (Briantais et al. 1986; vidual bands. All data are transferred to the central server of the ELDONET server in Pisa (Marangoni et al. 2000) where they can Schreiber and Bilger 1987, 1993; Krause and Weis be seen and downloaded by any interested user. 1991). While most fluorescence techniques allow only the measurement of steady state parameters, PAM fluorescence measurements permit the analysis of Plant material adaptive processes in the photosynthetic and the physio- Specimens of a number of atlantic macroalgae were used for the logical status of the photosynthetic apparatus by a non- experiments. Common species were selected which inhabit the invasive technique. tidal and subtidal zone: the red algae Gelidium arbuscula and Recent miniaturization and development of a computer- Halopithys incurvus and the brown algae Lobophora variegata, and Halopteris scoparia. The analyses were carried out on mostly based PAM fluorometer allows the application of the sunny days in October 1997 on an east-facing rocky shore equipment in the field (Schreiber et al. 1986). The easily (Arinaga) of Gran Canaria, Canary Islands (27.0°N, 16.5°W). portable instrument can be employed at the growth site to determine key photosynthetic parameters (Schreiber Measurements of PAM fluorescence and Bilger 1993; Schreiber et al. 1994). In the past few years another instrument, the diving PAM, has been The basis of PAM measurements is the determination of key flores- developed for measurements under water, allowing the cence parameters. As a starting point the background chlorophyll user to analyse subtidal species at their growth site in the fluorescence signal, Fo, is induced by a weak red light source in a dark-adapted specimen. Under these conditions the photosystem II water column. reaction centres are open. Subsequently the photosystem II reaction The measured fluorescence parameters can be used centres are closed by a saturating white light pulse which induces for the subsequent quenching analysis based on the maximal fluorescence (F ). When these measurements are performed m ′ assumption that two parallel processes reduce the on light-adapted specimens a Fo value is found which may be either higher or lower than in the dark-adapted specimens and a fluorescence: photochemical and non-photochemical ′ maximal fluorescence (Fm ) which is usually lower than Fm. quenching. The first indicates the use of the radiation Two portable pulse amplitude modulated fluorometers (PAM energy in the photosynthetic apparatus while the latter is 2000 and diving PAM; Walz, Effeltrich, Germany) were employed thought to be due to the build-up of charge and the pH to analyse the photosynthetic quantum yield on site (Schreiber et gradient across the thylakoid membrane (Schreiber et al. al. 1986). In the first set of experiments the thalli were selected immediately before the analysis and placed into custom-made UV- 1995; Krause and Weis 1991). transparent Plexiglas holders (GS 2458; Röhm and Haas, Darms- The photosynthetic quantum yield can be determined tadt, Germany) with open sides to allow unrestricted water flow using empirical equations developed by Genty et al. past the specimens. Four replicates were used for the same species (1989) and Weis and Berry (1987) for which no knowledge with at least eight independent thalli: The first set of experimental devices allowed unfiltered solar radiation to reach the specimens. of the dark fluorescence parameters, initial fluorescence The second set was covered with UV cut-off filter foils which in the dark-adapted state, when all reaction centres are removed short-wavelength radiation <320 nm (Montagefolie, open (Fo) and maximal fluorescence in the dark-adapted no. 10155099; Folex, Dreieich, Germany) and a third set was state when all reaction centres are closed (F ), is covered with filter foils which removed all UV radiation <395 nm m (Ultraphan UV Opak; Digefra, Munich, Germany). The transmission necessary. The validity of this approach has been demon- spectra of these filter foils can be found in Figueroa et al. (1997). strated by parallel gas exchange measurements (Schreiber A final set was subjected to the same experimental conditions and Bilger 1993). except the exposure period to solar radiation. All sample holders The aim of the present paper was to analyse the with the selected specimens were placed in shallow water on site photosynthetic quantum yield in common atlantic macro- in the shade for 30 min. Subsequently, the thalli were exposed to solar radiation for different times. Then the samples were returned algae on site and determine the degree of photoinhibition to the shade to allow them to recover from photoinhibition. The during exposure to solar irradiation. In addition, the photosynthetic parameters were determined and the quantum yield photosynthetic quantum yield was followed during the calculated in all experimental sets after the dark period, after the daily cycle at the growth site of the algae. The relative exposure time and at predetermined times during
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