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Effect of Water Flow on the Photosynthesis of Three Marine Macrophytes from a Fringing-Reef Lagoon

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Effect of Water Flow on the Photosynthesis of Three Marine Macrophytes from a Fringing-Reef Lagoon MARINE ECOLOGY PROGRESS SERIES Vol. 323: 119–132, 2006 Published October 5 Mar Ecol Prog Ser Effect of water flow on the photosynthesis of three marine macrophytes from a fringing-reef lagoon Susana Enríquez*, Aimee Rodríguez-Román Laboratorio de Fotobiología, Unidad Académica Puerto Morelos, Universidad Nacional Autónoma de México (ICML-UNAM), Apdo. Postal 1152, 77500 Cancun, Mexico ABSTRACT: We studied the effect of water flow on the reduction of the photosynthetic electron trans- port rates (ETR) of the seagrass Thalassia testudinum and the brown algae Lobophora variegata and Padina sanctae-crucis. The main objective of this study was to contribute to the understanding of the magnitude of carbon limitation in a sheltered, shallow coral reef environment, while improving the use of the fluorescence technique. The results confirm that photosynthesis, in the 3 species, is sink limited at normal seawater pH. Considering that the actinic light intensity chosen for the experimen- tal design was close to saturation irradiance for the 3 species, stronger ETR declines are expected under larger carbon requirements at supersaturating irradiance. The results suggest that photo- synthesis may be strongly carbon limited in sheltered coral reef environments. Nevertheless, pharmacological experiments revealed the occurrence of carbon concentration mechanisms (CCM) related to: (1) the external presence of the enzyme carbonic anhydrase under very low hydrodyna- mics, when the diffusive boundary layers stabilize and enzyme losses are minimal (L. variegata and – T. testudinum) and (2) the ability to take up HCO3 (T. testudinum and P. sanctae-crucis). The possi- bility that the capacity to calcify may be associated with the CCM of P. sanctae-crucis needs further testing. These results suggest that photosynthetic organisms adapted to coral reef systems, where calm, cloudless days with minimal water turbulence and maximum light penetration are common, have developed efficient CCMs. The study also supports the utility of the fluorescence technique for the analysis of the photosynthetic response to hydrodynamics within the limits imposed by the linear- ity between oxygen-based and fluorescence-based photosynthesis determinations. It also empha- sizes the importance of light absorption determinations for accurate estimations of ETR values. KEY WORDS: Brown algae · Carbon limitation · Carbon concentration mechanisms · CCM · Coral reef · Electron transport rate · ETR · Fluorescence · Thalassia testudinum · Water Resale or republication not permitted without written consent of the publisher INTRODUCTION magnitude) in water than in air (Raven 1984). The importance of carbon limitation in the reduction of Photosynthesis in aquatic environments is exposed marine primary production has not yet been fully eval- to stronger limitation by carbon availability than in ter- uated, nor has the diverse capacity of photosynthetic restrial ecosystems (Madsen & Sand-Jensen 1991). organisms to counterbalance this effect. Marine envi- Dense biomass stands in aquatic communities have ronments are characterized by high total alkalinity photosynthetic rates that are a third lower than those values. However, the high concentrations of inorganic in terrestrial communities. Photosynthesis in water also carbon dissolved in seawater do not necessarily reflect exhibits larger reductions for similar declines in inor- high carbon availability for photosynthesis, given that ganic carbon availability (Krause-Jensen & Sand- the concentration of CO2, which is the most accessible Jensen 1998). These differences are explicable by the inorganic carbon form for photosynthesis, is between – lower diffusion rates of CO2 and HCO3 (4 to 5 orders of 10.2 and 18.8 µM in the temperature range from 5 to *Email: [email protected] © Inter-Research 2006 · www.int-res.com 120 Mar Ecol Prog Ser 323: 119–132, 2006 25°C and under the current atmospheric equilibrium Marine life is currently experiencing important – (Raven 1984). Under these conditions, the HCO3 con- changes associated with global climate change. How- centration has a relatively constant value of 2 mM. ever, few data are available on the physiological Thus, most of the inorganic carbon available for photo- responses of marine macrophytes to the predicted synthesis in the marine environment is in an ionic form increases in water temperature, CO2 availability and not directly accessible for photosynthesis. UV-B radiation (e.g. Beer & Koch 1996, Zimmerman et According to Fick’s law, carbon fluxes are directly al. 1997). In the present paper, we study the magnitude associated with the diffusion coefficient and with dif- of carbon limitation on the photosynthesis of the sea- ferences in the inorganic carbon concentration be- grass Thalassia testudinum and the brown algae tween both external and internal tissue environments Lobophora variegata and Padina sanctae-crucis. The (Raven & Richardson 1986), but inversely associated effect of water flow was examined on the reduction of with the thickness of the boundary layer surrounding the photosynthetic electron transport rates of these 3 the tissue. The boundary layer is an important molecu- species of benthic coral reef primary producers. The lar diffusion barrier for carbon incorporation in photo- main objective of this study was to contribute to the synthesis (Kirk 1994). The resistance imposed by the understanding of the magnitude of carbon limitation in boundary layer has been shown to be larger than that a sheltered, shallow coral reef environment, while of the cuticle, cell wall, and cell and chloroplast mem- improving the use of the fluorescence technique in the branes (Larkum et al. 1989). Boundary layer thickness analysis of the photosynthetic response. We chose is variable and dependent on: (1) the size and shape of these 3 species because in the reef-lagoon studied the photosynthetic surfaces (Nowell & Jumars 1984), in (Puerto Morales, Mexico), T. testudinum is the domi- particular surface roughness and/or the presence of nant species, L. variegata is increasing in abundance, hairs or any other protruding structures that may while the presence of P. sanctae-crucis has been generate water turbulence or stabilize a laminar flow reduced to a seasonal or rare species. In addition, we surrounding the tissue, and (2) the intensity and direc- expected to obtain contrasting photosynthetic respon- tionality of the water flow (Wheeler 1980, MacFarlane ses to water flow reduction and in the possible CCMs & Raven 1989). Hence, hydrodynamism appears to be involved. The 2 brown algae have a similar shape, but a primary factor that should be considered in the eval- P. sanctae-crucis also has the capacity to calcify, simi- uation of the magnitude of carbon limitation of photo- lar to an important fraction of the coral reef primary synthesis in the aquatic environment. producers. The quantification of interspecific differ- The development of different mechanisms, which ences in the photosynthetic sensitivity to water flow promote intracellular accumulation of CO2 (carbon reductions and in the diversity of their functional concentration mechanism, CCM) allow photosynthetic CCMs may contribute to highlighting ecological differ- organisms to reduce the effect of carbon limitation on ences and spacio-temporal variability in the photo- photosynthesis. In many aquatic primary producers, synthetic performance, growth and abundance of the CCM activity has been associated with the direct or indi- small, but representative, group of primary producers – rect use of HCO3 (Smith & Bidwell 1989, Maberly 1990, of the coral reef system examined in the present study. Bjørk et al. 1992, James & Larkum 1996, Beer & Rehn- It may also provide useful information in identifying berg 1997, Invers et al. 1999, 2001). The capacity to take the differential sensitivity of these species to global – up HCO3 has been detected in several fresh- and brack- changes. To improve our understanding of the possible ish-water macrophytes and in marine macrophytes CCMs involved, pharmacological experiments were (Borowitzka 1982, Drechsler & Beer 1991). Also, the also carried out. activity of the enzyme carbonic anhydrase (CA) has been broadly documented (Borowitzka 1982, Giordano & Maberly 1989, James & Larkum 1996, Beer & Rehnberg MATERIALS AND METHODS 1997, Bjørk et al. 1997, Invers et al. 1999), although its location and relative importance as a CCM is still con- The species examined were collected between 2 and troversial. β-carboxylation and enzymes such as phos- 3 m depth in a fringing-reef lagoon (Puerto Morelos, phoenol pyruvate carboxylase (PEPC), phosphoenol Yucatan peninsula, Mexico) between August and Sep- pyruvate carboxykinase (PEPCK), pyruvate carboxylase tember 2001, and acclimated in tanks with running fil- (PC), acetyl CoA carboxylase (ACoC), etc., which tered seawater pumped directly from the reef lagoon facilitate metabolic alternatives to the inorganic carbon to the aquarium facility at the station of the Universi- carboxylation, make an important contribution to the dad Nacional Autónoma de México (UNAM) in Puerto CCMs (Bowes 1985, Raven & Osmond 1992). These Morelos (UAPM). Organisms were maintained for 1 d mechanisms appear in taxonomically distant organisms in the tanks before being used in the experiments. A that broadly differ in size and shape. subsample of Thalassia testudinum shoots was main- Enríquez & Rodríguez-Román: Effect of water flow on macrophyte photosynthesis 121 tained for 6 d, and a
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