Journal of Oceanography, Vol. 65, pp. 245 to 258, 2009
Influence of Non-Photosynthetic Pigments on Light Absorption and Quantum Yield of Photosynthesis in the Western Equatorial Pacific and the Subarctic North Pacific A NIL K UMAR V IJAYAN 1 , T AKASHI Y OSHIKAWA 2 *, S HIGEKI W ATANABE 1 , H IROAKI S ASAKI 3, K AZUHIKO MATSUMOTO4, SEI -ICHI SAITO5, SHIGENOBU TAKEDA1 and K EN FURUYA1 1
Graduate School of Agricultural and Life Sciences, The University of Tokyo, Bunkyo-ku, Tokyo 113-8657, Japan 2 School of Marine Science and Technology, Tokai University, Orido, Shimizu-ku, Shizuoka 424-8610, Japan 3 Seikai National Fisheries Research Institute, Fisheries Research Agency, Taira-machi, Nagasaki-shi, Nagasaki 851-2213, Japan 4 Mutsu Institute for Oceanography (MIO), Japan Agency for Marine-Earth Science and Technology Center (JAMSTEC), Sekine, Mutsu, Aomori 035-0022, Japan 5 Graduate School of Fisheries Sciences, Hokkaido University, Hakodate 041-8611, Japan (Received 28 January 2008; in revised form 6 November 2008; accepted 7 November 2008) ∗ Regional variations in the contribution of non-photosynthetic pigments ( anp ) to the ∗ total light absorption of phytoplankton ( aph ) and its influence on the maximum quantum yield of photosynthesis (φ m) were investigated. In the western equatorial Pacific, ∗ ∗ the surface anp : aph ratio was higher in the western warm pool than that in the upwelling region. This difference appears to be attributable to severe nitrate depletion and higher percentage of prokaryotes, which can accumulate very high concentrations of zeaxanthin in the western warm pool. In the subarctic North Pacific, the ∗ ∗ : aph ratio was expected to be higher in the Alaskan Gyre where the thermocline is anp sharper and iron limitation may possibly be more severe than in the Western Subarctic Gyre. However, the ratio was actually higher in the Western Subarctic Gyre, contradictory to our expectations. This east-west variation appears to be attributable to changes in the taxonomic composition; cyanobacteria were more abundant in the ∗ ∗ Western Subarctic Gyre. The values of anp : aph and its vertical variations were relatively small in the subarctic North Pacific compared to those in the western equatorial Pacific. These inter-regional variations appear to be attributable to the lower solar radiation intensity, smaller percentage of cyanobacteria, and relatively strong ∗ ∗ vertical mixing in the subarctic North Pacific. The spatial variations in anp : aph significantly influence φ m. In comparison with φ m based on the total light absorption (φ m ph), the values corrected for the contribution of non-photosynthetic pigments (φ m ps) showed an increase in both the western equatorial Pacific and the subarctic North Pacific.
Keywords: ⋅ Light absorption coefficient, ⋅ photosynthetic pigments, ⋅ non-photosynthetic pigments, ⋅ quantum yield of photosynthesis, ⋅ western Equatorial Pacific, ⋅ subarctic North Pacific.
of photosynthesis (φm) defines the efficiency of carbon fixation (or oxygen production) per absorbed photon and is a sensitive indicator of the nutrient status and relative growth rate of phytoplankton (Cleveland and Perry, 1987). The theoretical upper limit of φ m is 0.125 mol C (mol photon)–1 if all the absorbed photons are used only for photosynthetic photochemistry (Kok, 1960). However, in a natural environment the measured values of φ m (φm ph) calculated using the spectrally averaged value of
1. Introduction Light absorption by phytoplankton pigments is the first step of the photosynthetic process in the sea. The chlorophyll-specific light absorption coefficient (a∗ph(λ), Table 1) represents the ability of phytoplankton pigments to absorb light in seawater. The maximum quantum yield * Corresponding author. E-mail:
[email protected] Copyright©The Oceanographic Society of Japan/TERRAPUB/Springer
245
Table 1. List of symbols used in the text. Symbol ∗
Definition
Units
a ph(λ ) a ∗ps(λ ) a ∗np(λ ) ∗ aph
m2 (mg m2 (mg m2 (mg ∗ Spectrally averaged value of a ph(λ ), not weighted by the spectral distribution of ambient light m2 (mg
∗ aps
Spectrally averaged value of a∗ps(λ), not weighted by the spectral distribution of ambient light
Chlorophyll-specific light absorption spectrum of all phytoplankton pigments Chlorophyll-specific light absorption spectrum of photosynthetic pigments Chlorophyll-specific light absorption spectrum of non-photosynthetic pigments
TChl TChl TChl TChl
a)−1 a)−1 a)−1 a)−1
m2 (mg TChl a)−1
∗ anp
Spectrally averaged value of a np(λ ), not weighted by the spectral distribution of ambient light m2 (mg TChl a)−1
a∗
Maximum light utilization coefficient of photosynthesis
φm φ m ph
Maximum quantum yield of photosynthesis ∗ φm calculated using the value of aph
[mg C (mg TChl a)−1h−1] [µ mol photons m −2s −1]−1 mol C (mol photon)−1 mol C (mol photon)−1
φm ps
∗ φm calculated using the value of aps
mol C (mol photon)−1
∗
∗ a∗ph(λ) ( aph ) are often lower than the theoretical maximum value (e.g. Babin et al., 1996). This discrepancy is mainly ascribed to two changes in the photosynthesis process (Sakshaug et al., 1997). One is the reduction in the photochemical electron transport efficiency, particularly in a low-nutrient environment (Falkowski and Raven, 1997). The other major cause is the accumulation of nonphotosynthetic pigments such as alloxanthin, zeaxanthin, β-carotene, and diadinoxanthin in high-irradiance, lownutrient environments (Olaizola et al., 1994). Non-photosynthetic pigments absorb photosynthetically active radiation, but they do not transfer the excitation energy to the reaction centers, losing it as heat or fluorescence through a process called the xanthophyll cycle. ∗ It is convenient to separate aph into light absorption ∗ by photosynthetic pigments ( aps ) and that by non-photo∗ synthetic pigments ( anp ) for the evaluation of these two causes of variation in φ m ph (Sosik and Mitchell, 1995; ∗ Allali et al., 1997). When calculated using aps only, the φ m values (φ m ps) are corrected for the effect of non-photosynthetic pigments; its variations are then considered to be caused only by the photochemical electron transport efficiency and carbon fixation. In fact, several studies have reported that the vertical variation in φm ph was ∗ larger than that of φ m ps, suggesting that aps and φ m ps are better parameters for bio-optical primary production models (Sosik and Mitchell, 1995; Allali et al., 1997). There are two main approaches to obtaining a ∗ ps ( λ ): the fluorometric approach (Sosik and Mitchell, 1995) and a combination of the usual determination of a∗ph(λ) and its decomposition based on pigment analysis by HPLC (Allali et al., 1997). The former method has the advantage that it is not influenced by the packaging effect. However, it assumes an equal distribution of pigments between PS I and PS II, which may not be valid for some phycobiliprotein-containing species such as cyanobacteria
246
A. K. Vijayan et al.
and cryptophytes (Neori et al., 1988). On the other hand, the latter method has the advantage that it simultaneously provides information about the taxonomic composition and the ratio of the concentration of non-photosynthetic pigments to the total pigment concentration (NPP index, Babin et al., 1996). Previous studies conducted in low-latitude, oligotrophic waters (Sosik and Mitchell, 1995; Allali et al., 1997) suggested that the regional variations in the contribution of non-photosynthetic pigments to the total ∗ ∗ light absorption ( anp : aph ) were controlled by the physiochemical environmental conditions and the species composition of phytoplankton assemblages. It is there∗ ∗ fore expected that the ratio anp : aph and its influence on the quantum yield of photosynthesis is greater in lowlatitude oligotrophic waters (e.g. equatorial Pacific) where the solar radiation intensity is very high and prokaryotic Synechococcus and Prochlorococcus dominate as compared to that in mid-latitude mesotrophic waters (subarctic North Pacific) where eukaryotic phytoplankton dominate. In addition to the above inter-regional variations, intraregional variations are also expected. For example, in the western equatorial Pacific the influence of non-photosynthetic pigments is expected to be relatively small in the upwelling region (UP) where low-nutrient stress is alleviated as compared to the western warm pool (WWP) where nitrate is depleted at the surface layer (Minas et al., 1986). The subarctic North Pacific has two gyre systems, the Western Subarctic Gyre (WSG) and the Alaskan Gyre (AG). Both of them are known to be high-nutrient low-chlorophyll (HNLC) regions (Harrison et al., 1999), where the photosynthetic performance of phytoplankton is reduced by iron limitation, particularly in the AG (Suzuki et al., 2002). Thus, the influence of non-photosynthetic pigments is expected to be larger in the AG than in the WSG.
In the present study we first investigated the spatial variations in the contribution of non-photosynthetic pig∗ ∗ ments to total absorption ( anp : aph ) within and between the western equatorial Pacific and subarctic North Pacific, based on measurements of the light absorption spectrum of phytoplankton, pigment concentrations, and the photosynthesis-irradiance (P-E) relationship. Second, we evaluated the influence of non-photosynthetic pigments on the maximum quantum yield of photosynthesis by com∗ paring the values calculated using aph (i.e. φm ph) and those ∗ calculated based on aps (i.e φm ps).
N9
N10
N11
N8 Bering Sea
N14 N15 N16
N6
N4
Alaskan Gyre
N2&3 Western Subarctic Gyre
2. Materials and Methods E2
2.1 Field observations and water sampling The Mirai MR 98-K02 cruise was conducted from December 1998 to January 1999 in the western equatorial Pacific Ocean (Fig. 1). The Hakuho-Maru KH-97-2 cruise was undertaken in the subarctic North Pacific from July to September 1997. Water samples were obtained using Niskin bottles mounted on a rosette sampler fitted with CTD systems (SBE911plus during the MR 98-K02 cruise and SBE9plus during the KH-97-2 cruise, Sea-Bird Electronics, Inc., USA). Water samples for the measurement of the light absorption spectrum of phytoplankton, pigment concentrations, and nutrient analysis were obtained from up to 11 layers within a depth of 200 m. Water samples for the P-E relationship experiment were obtained from the surface only (within a depth of 10 m) at nine stations (E3 to E12) in the western equatorial Pacific and from two to four layers at three stations (N4, N6, and N15) in the subarctic North Pacific (Fig. 1). The P-E relationship experiment was not conducted at Stn. E2 in the western equatorial Pacific (Fig. 1). The concentrations of dissolved inorganic nitrate, ammonium, and phosphate were determined using autoanalyzers (TRAACS800 during the MR 98-K02 cruise and TRAACS2000 during the KH-97-2 cruise, Bran+Luebbe, Germany). The wavelength-integrated downward photosynthetically available radiation (PAR; 400–700 nm) was measured using an underwater spectroradiometer (MER2040, Biospherical, USA). The depth of the euphotic zone was defined as the depth at which the downward PAR is 1% of the level immediately below the sea surface. The mixed layer depth was defined at depth where sigma-t increased by 0.125 from its surface reference value (Bouman et al., 2006). 2.2 Spectral light absorption of phytoplankton The light absorption spectrum of phytoplankton was measured by the quantitative filter technique (QFT) (Mitchell, 1990). The particulates were collected from seawater samples onto 25-mm GF/F glass fiber filters
Western Warm Pool
E5
Upwelling Region E8
E6
E3
E7
E9
E10 E12 E11
Fig. 1. Map of the study area showing the station positions. Station numbers are N2&3 to N6 (Western Subarctic Gyre), N8 to N11 (Bering Sea), N14 to N16 (Alaskan Gyre) for the KH-97-2 cruise and E2 to E7 (western warm pool), E8 to E12 (upwelling region) for the MR 98-K02 cruise.
under low vacuum pressure (28°C) and nutrient-poor water (
