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The effects of temperature and nutrient concentrations on nitrate and phosphate uptake in different species of Porphyra from Long Island Sound (USA)

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The effects of temperature and nutrient concentrations on nitrate and phosphate uptake in different species of Porphyra from Long Island Sound (USA)
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  The effects of temperature and nutrient concentrations on nitrate and phosphate uptake indifferent species of   Porphyra  from Long IslandSound (USA) A. Pedersen a, *, G. Kraemer   b , C. Yarish a  a   Norwegian Institute for Water Research, 0411 Oslo, Norway  b  Division of Natural Science, Purchase College, State University of New York, Purchase, NY 10577, USA Received 28 January 2004; received in revised form 4 April 2004; accepted 8 May 2004 Abstract Uptake rates of nitrate and phosphate were measured for four species and one variety of   Porphyra from Long Island Sound (USA) at two temperatures and two nutrient medium concentrations at increasing intervals over a 24- or 48-h period. Maximum uptake rates found were:  V   30  A M0–1 h =73.8  A mol NO 3  g  1 DW h  1 and  V  3  A M0–1 h =16.7  A mol PO 4  g  1 DW h  1 , in the two thinnest   Porphyra . We foundthat the nitrate uptake rates were significantly greater at 30  A M than 3  A M NO 3  concentration, and that the uptake rates decreased with time of exposure. Temperature (5, 15, and 25  8 C) did not have asstrong an effect on nitrate uptake rates as did nutrient concentration.  Q 10  values and uptake rates at four different nitrate concentrations indicated that nutrient uptake at 5  8 C was initially an active process. After 24 h, the processes involved appeared passive as  Q 10  values were between 1.0 and 1.3and nitrate uptake curves were linear. Nitrate uptake rates correlated positively with the surface area/ volume (SA/V) ratio. No coherent trends were found for uptake of phosphate, except that the uptakerates were significantly higher in 30  A M NO 3  medium as opposed to 3  A M NO 3 . We did not find anysignificant difference in uptake rate and pattern between the summer species  Porphyra purpurea (Roth.) C. Agardh, the eurythermic  Porphyra suborbiculata  Kjellm., the winter species  Porphyra 0022-0981/$ - see front matter   D  2004 Elsevier B.V. All rights reserved.doi:10.1016/j.jembe.2004.05.021* Corresponding author. NIVA, P.O.B. 176 Kjelsa˚s, 0411 Oslo, Norway. Tel.: +47 22 18 5168; fax: +47 2218 5200.  E-mail address:  are.pedersen@niva.no (A. Pedersen).Journal of Experimental Marine Biology and Ecology312 (2004) 235–252www.elsevier.com/locate/jembe  rosengurttii  J. Coll and J. Cox, and the two varieties of   Porphyra leucosticta  Thur. Le Jol. (bothwinter species). D  2004 Elsevier B.V. All rights reserved.  Keywords: Porphyra  spp.; Nitrate; Phosphate; Uptake; Ecophysiology; ANW—Atlantic North West, NewEngland; LIS—Long Island Sound 1. Introduction The nutrients nitrate (N) and phosphate (P) are two of the most important elementsrequired for algal growth, and one or the other often limits growth (DeBoer, 1981;Lapointe, 1987). Uptake involves both passive and active transport (D’Elia and DeBoer,1978). However, in the natural environment, active transport through the plasmalemma isthe most common mechanism as the concentrations inside the cells are usually in themillimole range, while concentrations outside are typically 1000-fold lower (micromolerange; Lobban and Harrison, 1994). Physical, chemical, and biological factors all affect  uptake rates of nutrients. Of the physical factors, the most important ones are light,temperature, water motion, and desiccation (Lobban and Harrison, 1994). Irrradiance has a direct effect on the uptake of nitrate (Wheeler, 1982), while spectral quality also affects the uptake and reduction of nitrate or phosphate (Lopez-Figueroa and Ruediger, 1991; Rai andRai, 1997). Temperature influences the uptake of nutrients through  Q 10  effects on algalmetabolism (Raven and Geider, 1988). However, algal metabolic response rates vary with species (Harlin and Craigie, 1978; Topinka, 1978). Many studies have demonstrated the strong influence of temperature on uptake of different nutrients (Asare and Harlin, 1983;Duke et al., 1989; Kautsky, 1990; Peckol et al., 1994; Chopin et al., 1995; Rivers andPeckol, 1995; Davison and Pearson, 1996; Gerard, 1997; Kinney and Roman, 1998; Ozakiet al., 2001). In general, the optimum temperature for uptake coincides with the optimumtemperature for growth.Desiccation is a normal but stressful event in the midlittoral zone and even more so in thesupralittoral zone (Hurd and Dring, 1991; Herna´ndez et al., 1995). Some desiccations enhance short-term (10–30 min) nutrient uptake rates upon rewetting (Thomas and Turpin,1980; Thomas et al., 1987). Nutrient concentration in the medium and its chemical speciesis also of great importance (DeBoer et al., 1978; DeBoer, 1981; Chopin et al., 1990; Peckolet al., 1994; Sfriso, 1995; Braga and Yoneshigue Valentin, 1996; Harrison and Hurd, 2001)as well as the intracellular nutrient concentration (Gerard, 1982; Wheeler et al., 1984;Wheeler and Srivastava, 1984; Pedersen and Borum, 1996; Viaroli et al., 1996). Highinternal concentrations of a specific nutrient will repress uptake of the same nutrient (Chopin et al., 1990; Lobban and Harrison, 1994). One nutrient (e.g., ammonium) can have an antagonistic effect on the uptake of another (e.g., nitrate) when added simultaneously(DeBoer, 1981). Another biological factor that influences nutrient uptake is algal morphology [i.e., shape quantified as surface area/volume (SA/V) ratio] (Rosenberg andRamus, 1984; Wallentinus, 1984; Hein et al., 1995; Taylor et al., 1998; Neori et al., 2004).Several specific enzymes are involved in the assimilation of each nutrient. However, theenzymes involved in both nitrate and phosphate uptake and assimilation are primarily  A. Pedersen et al. / J. Exp. Mar. Biol. Ecol. 312 (2004) 235–252 236  regulated by concentration of substrate, internal concentrations, and temperature (Syrett,1981; Hanisak, 1983).From an ecological perspective, the occurrence of species at different times of the year and in different zones on the shorelines implies that their rates of uptake and assimilationmight reflect their spatial and temporal occurrence on the shorelines. Long Island Sound(LIS), USA, is inhabited by several species of   Porphyra  including  Porphyra suborbiculata  Kjellm.,  Porphyra purpurea  (Roth) C Agardh.,  Porphyra rosengurttii  J.Coll and J. Cox, and  Porphyra leuco sticta  Thur. Le Jol. The latter taxon has at least onedistinct morphological type; A (sensu Neefus et al., 2000).  P. rosengurttii  was described as  P. leucosticta  type C in Neefus et al. (2000); however, it was shown by Blodgett et al. (2002) to resemble  P. rosengurttii  J. Coll and J. Cox by DNA sequencing, hence referredin this paper as so. The occurrence of these species differs both temporarily and spatially(Pedersen et al., personal communication). Their ability to take up and assimilate nitrateand phosphate may vary as their access to these nutrients differs. In this study, weexamined whether temperature or nutrient concentration is related to the uptakecharacteristics of five types (four species plus one variety) of   Porphyra  and if anydifferences could reflect the spatial and temporal occurrences of the different types. 2. Materials and methods  Nutrient uptake measurements were performed on five types of   Porphyra  collected fromthree different locations in LIS . P. suborbiculata , a eurythermic species occurring from fallto spring, was collected in January and February 2001 and December 2002, at Cove IslandPark, Stamford, CT (N: 41 8 2, 644  V ; W: 73 8 30, 133  V ).  P. rosengurttii , a winter speciesoccurring from November to May, was collected in January 2002 at Cove Island Park,Stamford, CT.  P. purpurea , a late summer species, was collected in September 2001 east of Port Jefferson, NY (N: 40 8 57, 862  V ; W: 73 8 2, 689  V ).  P. leucosticta , found in the midlittoralto shallow sublittoral from March to late May, was collected in early May 2001 from WhitePoint, Waterford, CT (N: 41 8 18, 180  V ; E:  72 8 08, 050  V ). Another strain of   P. leucosticta was collected at Cove Island Park, Stamford, CT. The strain, type A (sensu Neefus et al.,2000), is mainly distinguished from the  P. leucosticta  holotype by its thallus morphology,thallus thickness, reproductive areas, and DNA. The thickness of the vegetative thallus of   P.leucosticta  type A and the holotype is 18–24 and 35–45  A m, respectively.  P. leucosticta type A, which occurs in low littoral to shallow sublittoral from January to May, wascollected for the experiments in March 2001. Based on these differences and those found by Neefus et al. (2000), type A was treated as a different strain of   P. leucosticta .The algae were kept in aerated autoclaved seawater (ASW) at 5  8 C except for   P. purpurea , which was kept in 15  8 C, followed by acclimatization for 2 days at theappropriate test temperatures in aerated ASW. A short daylength light regime (8:16; L:D)was applied to all species except for the summer species  P. purpurea , which as run duringuptake experiments in 25  8 C in neutral day photoperiods (12:12; L:D). Circular disks of either 20 or 14 mm in diameter, depending on the size of the blades, were then punchedout of the thallus and kept in aerated ASW for another day before being transferred intoaerated artificial seawater (Tropic Marine R ; Dr. Biener Aquarientechnik, Germany), with  A. Pedersen et al. / J. Exp. Mar. Biol. Ecol. 312 (2004) 235–252  237  no inorganic nitrate or phosphate enrichment (detection levels were 0.7 and 0.3  A mol,respectively). The disks were kept in aerated artificial seawater for 5 days before theuptake experiments at a light irradiance of 100  A mol m  2 s  1 . To prevent or delay sporeformation in the blades, the light attenuation was reduced to 50  A mol m  2 s  1 during theuptake experiments.The uptake experiments were performed in two aerated artificial seawater media: one alow-concentration medium (LCM) augmented with 0.5  A mol of NaHPO 4  and 3  A mol of  NaNO 3 , and the other a high-concentration medium (HCM) with 3  A mol of NaHPO 4  and30  A mol of NaNO 3 . These concentrations are in the range of nutrient concentration foundin local marine coastal areas (National Oceanic and Atmospheric Administration/NationalOcean Service: http://www.co-ops.nos.noaa.gov/pub.html). Experimental temperatures were 5 and 15  8 C for all species except for the experiment with the summer species  P. purpurea , which were run at 5 and 25  8 C. Experiments with disks of   P. leucosticta  type Awere run at two additional concentrations of 7 and 15  A mol of NaNO 3  with 0.7 and 1.5 A mol of NaHPO 4 , respectively.During the experiments, the algae were placed in aerated 250-ml Erlenmeyer bottleswith 200 ml of incubation medium. Water samples (10 ml) for nutrient measurements weretaken at 1, 4, 8, 24, and 48 h for   P. leucosticta  and  P. leucosticta  type A and 1, 3, 6, 10, and24 h for all others types. The total incubation volume of the bottles was replaced at everysampling. The calculated uptake rates are the average rates between these sampling times(i.e., 1 h represents uptake at 0–1 h interval, and the 24-h uptake occurred at 10–24 hinterval). Four replicate tests flasks were used for each nutrient medium. However, theyrepresented pseudo-replicates for temperature as all were incubated in the same chamber.Samples from the incubated media were analyzed for inorganic N and P by theEnvironmental Research Institute, University of Connecticut, using a Four-Channel AutoAnalyzer equipped with High-Sensitivity Seawater Cartridges (Lachat-QuikChem AE IonAnalyzer; Hach, Loveland, CO).Samples for dry weight (DW) were taken prior to the experiments and at the end. DWwas measured after drying the samples for 48 h at 55  8 C. Statistical differences betweenuptake rates and time were tested, when appropriate, by parametric paired  t   tests(MINITAB; Minitab). When testing statistical differences between temperatures, all  Porphyra  spp. were joined and tested as a group by a parametric paired  t   test astemperature in these experiments was to be treated as pseudo-replicates.  p  values  N 0.05were considered nonsignificant (n.s.) Regression analyses were based on linear (  y = ax + b )and hyperbolic equations resembling Michaelis–Menten uptake kinetics [  f   = ax /( b +  x )] inSigmaplot 8 and MINITAB. 3. Results 3.1. P. suborbiculata Uptake of nitrate in  P. suborbiculata  was 1.3 times higher at 15  8 C than at 5  8 C(  p b 0.001) and, on average, sevenfold higher in HCM than in LCM (  p b 0.001) (Fig. 1A).The rates varied from  V  3  A M10–24 h =0.8 to  V   30  A M6–10 h =36.7  A mol NO 3  g  1 DW h  1 . The initial  A. Pedersen et al. / J. Exp. Mar. Biol. Ecol. 312 (2004) 235–252 238  uptake rates in HCM were two times higher during the first hour than during the last  period (10–24 h) at both 5 and 15  8 C, and three to six times higher in LCM. In HCM, theuptake rates decreased except for a temporary increase in uptake rates from 6 to 10 h,especially at 15  8 C. Fig. 1. Nitrate uptake rates in  P. suborbiculata  (A),  P. purpurea  (B), and  P. rosengurttii  (C) in two concentrationsof medium; LCM (3  A mol NO 3 +0.5  A mol PO 4 ) and HCM (30  A mol NO 3 +3  A mol PO 4 ) at 5 and 15  8 C for   P. suborbiculata  and  P. rosengurttii , and at 5 and 25  8 C for   P. purpurea . Error bars are standard error.  A. Pedersen et al. / J. Exp. Mar. Biol. Ecol. 312 (2004) 235–252  239
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