In Situ Photosynthesis in the Seagrass Halodule Wrightii in a Hypersaline Subtropical Lagoon*

MARINE ECOLOGY PROGRESS SERIES Vol. 107: 281-293. 1994 Published April 28 Mar. Ecol. Prog. Ser.

In situ photosynthesis in the seagrass Halodule wrightii in a hypersaline subtropical lagoon*

Kenneth H. Dunton', David A. ~omasko~

'Marine Science Institute, The University of Texas at Austin, Marine Science Institute, PO Box 1267, Port Aransas, Texas 78373, USA 2SarasotaBay National Estuary Program, 1550 Ken Thompson Parkway, Sarasota, Florida 34236, USA

ABSTRACT: Photosynthesis versus irradiance (P vs 1) parameters in the shoalgrass Halodule wrlghtii Ascherson were calculated from measurements of oxygen evolution collected in situ, using entire plants in Laguna Madre, Texas, USA. Eleven expenmental incubations were performed from May 1989 to April 1991 using pulsed oxygen electrodes that collected data continuously under natural daylight conditions For comparison with in situ measurements of photosynthesis, Pvs 1 parameters were calculated from laboratory measurements on blade segments incubated In a small volume chamber. For field plants, average saturation 111-adiance (I,) was 319 pm01 m-2 S-', photosynthetic capacity (P,,,) was 374 pm01 O2 g-l dry wt (dw) h-', and relative quantum efficiency (a) generally ranged from 0.5 to 1.6 pm01 O2 g-I dw h-l (pm01 photons m-2S-').'. Whole plant respration was 70 pm01 g'dw (leaf) h', and compensation irradiance (I,,) was ca 85 pm01 m-2 S-' Chlorophyll a concentrations averaged 12.8 mg g-' dw. and the mean chl d:chl b ratio over the 2 yr period was 2 2 For blade segments incubated in the laboratory under similar temperatures to field plants and at corresponding chlorophyll concentrations. P,,, was not significantly different but a was signif~cantlyhigher, ranging from 3.4 to 5.3 pm01 O2 g-' dw h-' (~.lmolphotons nr2 S-').' The higher a values resulted In significantly lower estimates for 1, (mean of 101 pm01 m-2 S-'). The higher U in laboratory plants was largely related to the perpendicular orientation of leaf tissue to a directed hght field, which is not reflective of natural conditions for H. wrightii. The significant difference in 1, values calculated from incubations performed in the laboratory and field has profound effects on model calculations of H,,,, the duration of irradiance- saturated photosynthesis, and thus predictions of the minimum llght requirements required to sustain growth in H. wrightii. Consequently, the application of laboratory-derived 1, values for H. wrightii would result in overestimates of its maximum depth limlts and rates of area1 primary production

KEY WORDS. Photosynthesis . Seagrasses . Halodule wrightil . Texas . Subtrop~cal. Light . PAR Photophysiology . Shoalgrass

INTRODUCTION In Texas, USA, the occurrence of high finfish production in estuaries dominated by seagrasses and the There are no cornfields in the sea, yet seagrass concentration of overwintering waterfowl in seagrass meadows occur over vast areas and are among the meadows are no coincidence. In Laguna Madre, which most productive of plant communities (McRoy & produces more than 66% of the state's annual finfish McMillan 1977). They provide important structural harvest (Hedgpeth 1967), Hellier (1962) and Odum & complexity to coastal habitats and are used both as Wilson (1962) found a positive correlation between substrata and food for a wide variety of flora and fauna, gross photosynthesis (95 % of which is seagrass or algal including endangered sea turtles (Thayer et al. 1975, epiphytes) and fish biomass. In addition, Cornelius Fry & Parker 1979, Blorndall 1980, McRoy & Helffench (1977) found that 4 to 5 % of the autumn standing crop 1980). of the shoalgrass Halodule w~llghtii in Laguna Madre was consumed by redhead ducks. McMahan (1969) 'The University of Texas at Austin, Marine Science Institute calculated that shoalgrass made up 84 to 89% of the Contribution No. 900 diet for pintail and redhead ducks.

O Inter-Research 1994 Resale of full article not permitted 282 Mar. Ecol. Prog. Ser 107: 281-293, 1994

Despite the large volume of information published photosynthetic efficiency and levels of light saturation on the trophic and functional value of seagrasses, our for this species. Pigment levels within the leaves were knowledge of the basic biology of this group is still also assessed to determine if any variations in P vs I inadequate to sufficiently predict the effects of envi- parameters could be related to changes in chlorophyll ronmental perturbations on seagrass growth and pro- a and b (chl a and b) content. For comparison to field ductivity (Zimmerman et al. 1991). For example, measurements of photosynthesis, leaf segments of H. Laguna Madre is characterized by over 730 km2 of wrightii were also incubated under carefully con- seagrass meadows composed of 5 different species trolled conditions of light and temperature in the labo- (Quammen & Onuf 1993) that represent about 85% of ratory. The 2 approaches yielded significantly different total seagrass vegetation in the entire coastal zone of results and indicated that the use of saturation irradi- Texas (Onuf pers. comm.). Yet losses of seagrasses in ance values derived from laboratory measurements of the lower Laguna Madre since the mid-1970s have photosynthesis may not always be appropriate in the been documented by McMahan (1969) and Merkord development of models to predict seagrass depth dis- (1978). A vegetational survey in 1988 by Quammen & tributions and productivity in the marine environment. Onuf (1993) confirmed a 140 km2 decrease in cover since 1965-67. The decline in seagrass cover has been attributed to light reduction caused by high turbidities METHODS that resulted from maintenance dredging (Merkord 1978, Quammen & Onuf 1993, Onuf 1994). In addition, In situ photosynthetic measurements. We examined the occurrence of a brown tide algal bloom in Laguna P vs I relationships in a monotypic meadow of Halo- Madre since June 1990 has further stressed seagrass populations through chronic light reduction (Dunton 1994). It is clear that predicting the effect of chronic reductions in underwater irradiance, as well as efforts to manage the remaining seagrass resources through habitat restoration and the establishment of water transparency criteria, require an accurate knowledge of the plant's photosynthetic light requirements. Such quanti- tative information becomes extremely valuable when combined with long-term in situ measurements of photosynthetically active radiation (PAR). Few studies have addressed photosynthetic carbon production in conjunction with GUF OF MEXICO definitive measurements of PAR for accurate calculation of photosynthesis versus irradiance (Pvs I) parameters. However, even for species which have been studied extensively, such as Zostera marina, measurements of saturation irradiance can vary considerably (e.g. from 35 to Mansfield Pass 230 pm01 photons m-2 S-' at 15°C; Drew 1979, Zimmerman et al. 1989).Such variations may be a product of the techniques employed rather than a reflection of actual differences in a spe- 0 15 30 cies' photosynthetic physiology. This further kilometers complicates the use of P vs I parameters in ex- plaining the current distribution of seagrasses Brazos Sun/iogo Pars from measurements of underwater light fields. In this study, we examined the photosynthetic rates for entire Halodule wrightii plants from in situincubations made periodically over a 2 yr period in Laguna Madre, Texas. We also made concurrent measurements of underwater Fig. 1.Location of the experimental study site (LIM-151)In the upper quantum irradiance to estimate parameters of Laguna Madre. Texas, USA Dunton & Tomasko: Halodule photosynthesis In a hypersal~nelagoon 283

dule wrightii in the upper Laguna Madre, Texas (Sta- blades while they were positioned and pressed firmly tion LM-151; 27" 21' N; 97' 22' W; Fig. 1).The average into the seabed to a depth of 10 cm. Underwater PAR depth at this site was 1.3 m (Dunton 1994) which is (400 to 700 nm) was measured at 5 S intervals and inte- close to the maximum depth penetration for actively grated every 5 min on a continuous basis using an LI- growing populations of H. wrightii (1.6 to 1.8 m; Onuf 193SA spherical quantum sensor, which provided pers. comm.) in upper Laguna Madre. input to a LI-1000 datalogger (LI-COR, Lincoln, NE, Experimental incubations were conducted at 2 to USA). The sensor was placed adjacent to the chambers 4 mo intervals from May 1989 to April 1991. About at canopy level (Fig. 2). Salinity was determined in the 2 wk prior to the in situ work, we removed dead field using a refractometer calibrated against an Orion leaves, algal epiphytes and drift macroscopic algae 140 salinometer. within a 2 m2 area. Algal epiphytes were seldom Dissolved oxygen measurements were collected observed on leaves of Halodule wrightii in Laguna using an Endeco/YSI Type 1125 Pulsed Dissolved Oxy- Madre, and may be related to the hypersaline condi- gen System. The system utilizes 4 YSI 1128 oxygen tions and low nutrient concentrations in the upper La- electrodes, is flow insensitive, offers high resolution guna (Jewett-Smith 1991). If present, epiphytes were (+0.4 PM), and is capable of collecting continuous either removed by hand or by clipping the top few measurements of dissolved oxygen and temperature at centimeters of the oldest blades having the highest selectable intervals. For incubations with Halodule concentration of these attached plants. Immediately wrightii, the probes were programmed to collect mea- prior to the deployment of incubation chambers on surements of dissolved oxygen at 15 min intervals. the seabed, the area was again raked clean of detritus Chambers were typically deployed by 18:OO h and and macroalgae. allowed to equilibrate for several hours prior to data Photosynthetic incubations of whole plants were collection. Once oxygen values had stabilized, water conducted in situusing four 5 1 chambers placed on the samples were collected periodically for oxygen deter- seabed by divers. Clear acrylic plastic chambers were mination~using the Winkler method (Strickland & Par- 12 cm in diameter and 45 cm high (Fig. 2). The top of sons 1972) to insure that the probes were operating each chamber was permanently sealed and contained within calibration (calibrations were conducted in the a tapered opening for an oxygen probe and a 1.2 cm laboratory prior to the cruise). Constant monitoring of diameter sampling port plugged with a rubber septum. the data output via RS-232 interface to a laptop com- A small battery-powered submersible pump provided puter using Endeco software permitted the monitoring circular water movement within the chamber for 3 min of oxygen tensions within the chambers and avoidance periods at 2 min intervals, as tilggered by an external of saturating oxygen concentrations. If saturation computer running in BASIC. During deployment of the occurred, oxygen levels were reduced 40 to 50% by chambers, care was taken to avoid cutting shoots or bubbling N2 into the chamber for 2 to 3 min. Any

Fig. 2. Photosynthetic oxygen chamber used for in situ incubations in Laguna Madre. Four chambers constructed entirely of clear acrylic were employed simultaneously during each incubation. See text concerning details of data acquisition Mar. Ecol. Prog. Ser. 107: 281-293, 1994

remaining gas bubbles were removed using the 1.2 cm mizing residuals as reported for phytoplankton and diameter sampling port at the top of the chamber. marine macroalgae (Chalker 1980, Coutinho & Zing- Plants were incubated under natural daylight condi- mark 1987, Geider & Osborne 1992). All curve-fitting tions, although neutral density shade cloth was occa- was performed statistically on a 486 PC using nonlin- sionally deployed over the chambers to achieve a ear least squares regression techniques (SAS Institute desired light level. Incubations generally ranged from 1987). P vs I parameters were estimated simultane- 0.5 to 1.5 h to maintain a given light level. To assess the ously using a derivative-free algorithm (The Dudly effect of phytoplankton on oxygen levels within the algorithm) of Ralston & Jennrich (1978).The saturation chambers, we performed light and dark bottle incuba- irradiance, Ik,was defined as the ratio of the 2 model tions and obtained total water column chlorophyll con- parameters, a and P,,,: centrations following Parsons et al. (1984). Although the contributions made by phytoplankton were usually insignificant (< 5 % of chamber photosynthesis at P,,,), the onset of a brown algal chrysophyte bloom in late Respiration and calculation of whole-plant compen- spring 1990 caused significant increases in chlorophyll sation irradiance. Estimation of the compensation irra- concentrations in the upper Laguna Madre (Stockwell diance for an entire plant (blades and their associated et al. 1993). To avoid the necessity of making correc- below-ground tissues), required a knowledge of the tions for the oxygen contributions made by phyto- root:shoot ratios (RSR) for Halodule wrightii and mea- plankton, the water within the chambers was cycled surements of leaf and root/rhizome dark respiration sequentially through 10 and 1 pm filter cartridges for a rates. During each experimental chamber incubation, 15 rnin period. This procedure effectively reduced we collected blade and root/rhizome material for dark chlorophyll concentrations in the chambers to negligi- bottle incubations performed at night in situ. Samples ble levels. containing entire blades and root/rhizome tissue were Photosynthetic rates were calculated from changes separated and washed immediately after collection in dissolved oxygen concentrations in the chamber and sorted into 4 replicate 300 m1 BOD bottles for each over the duration of each incubation. Net chamber tissue type. Two additional bottles were deployed to photosynthesis was determined from slopes by regres- correct for water column respiration, which normally sion analysis of linear portions of recorded time series exhibited negligible oxygen uptake over the 2 to 3 h at each light level. Chamber respiration rates (for incubation period. Oxygen concentrations in each bot- calculation of plant, animal, bacterial and chemical tle were measured using an oxygen electrode or by oxygen demand) were determined from incubations chemical analysis using the Winkler Method (Parsons conducted the evening prior to the photosynthetic et al. 1984). The incubated shoot and root/rhizome tis- incubation. Respiration by non-seagrass tissues was sue was then dried to a constant weight at 60°C for variable but generally accounted for 10 to 50 % of total 24 to 48 h. Results are expressed in pm01 0, g-' dry wt chamber respiration. Gross photosynthesis at each (dw) tissue h-'. light level (PGlI,)among the 4 replicate chambers was The apportionment of above- and below-ground calculated similarly to that outlined by Fourqurean & tissue was measured from biomass samples retrieved Zieman (1991) in which PG,I,represents the sum of net from the 4 experimental chambers used in the P vs I chamber photosynthesis and chamber respiration, nor- incubations. Pigmented leaves and shoots (above- malized to the pigmented shoot and leaf biomass in the ground tissue) were separated from non-photosyn- chamber thetic shoot and root/rhizome portions; the tissues were washed sequentially through 12 mm and 1.0 mm [Pchamber net (I] + Rchamber] p~(l] = mesh screens to remove sediments, detritus, and shell B~eaf material. The pooled material from the 2 components Gross photosynthetic rates were expressed in units were dried and indices of RSR determined. Total plant of pm01 O2 g-I dry wt leaf h-'. respiration (Rp)was normalized to 1 g dry wt of leaf tis- P vs I model calculations. P vs I data were fit to the sue and calculated from the respiratory demands of hyperbolic tangent function of Jassby & Platt (1976): leaf tissue (RIeaI)and root/rhizome (R,,,) tissue based on the proportion of root/rhizome tissue needed to support that leaf tissue (the RSR ratio): where P,,, is the light-saturated rate of photosynthesis, a is light-limited slope of P vs I curve and I is the Whole plant compensation irradiance (I,,), the light irradiance. This function usually provides the best fit to level at whlch the rate of photosynthetic oxygen evolu- P vs I curves based on both goodness of fit and mini- tion (P) is equivalent to the total respiratory demands Dunton & Tomasko Halodule ph otosynthesls in a hypersaline lagoon 285

of the plant (Rp),was then determined mathematically from the hyperbolic tangent function by setting RP equal to P, substituting ICpfor I in Eq. (2) and solving for Icp: P I,, = 1-1 coth[A) pm,* pm,, Laboratory P vs I measurements. For comparison with in situ measurements of photosynthesis, vegeta- tive shoots were collected from cores gathered at the study site in late April 1993 for laboratory-based metabolic rate measurements. Entire plants (shoots, roots and associated sediment) were placed in holding tanks with continuous running seawater (25 to 26°C) and Time (rn~nutes) exposed to ca 100 pm01 photons m-' S-' under a daily Fig. 3. Halodule wrightii. Photosynthetic oxygen evolution photoperiod of 12 h light:12 h dark under fluorescent and respiratory uptake in blade segments as a function of lamps. Leaf segments (3 cm lengths) were cut 2 to 4 h time at different light levels. Asterisk denotes light level that was not preceded by a 6 rnin dark period (see text) prior to the start of the physiological measurements to minimize the effects of wound respiration (blade tissue turned increasingly brown from cut areas if held > 12 h). Plants were incubated within 1 to 3 d of initial described above for incubations that averaged 4 to collection. We performed the P vs I measurements at 6 min. P vs I data were fit to the hyperbolic tangent 29 "C to facilitate direct comparison with field incuba- function (Eq.2) of Jassby & Platt (1976); leaf compen- tion~.Five of the eleven in situincubations were con- sation irradiance (I,,,,,,,) was determined similarly as ducted at temperatures ranging between 28 and 30 "C denoted for I,, in Eq. (5). (mean 29°C) and provided a sufficient sample for sta- Because of concerns about effects of lacuna1 gas stor- tistical comparison at this temperature. age on the measurement of photosynthesis, we estab- Oxygenic photosynthesis and respiration rates were lished a minimal period of stabilization following intro- measured on leaf segments using a polarographic O2 duction of blade tissue into the chamber and after electrode in a modified water-jacketed incubation establishment of each new light level. The duration of chamber (13 m1 vol; Rank Bros., Bottisham, UK). The this period was based on a time-course experiment at electrode was calibrated using NZ-purged and air- 3 different light levels, similar to that performed by saturated media. An underwater LI-192SA quantum Drew (1978). The results (Fig. 3) show that a constant sensor fitted on one side of the square chamber and rate of oxygen evolution into the incubation chamber connected to a LI-1000 datalogger provided accurate was delayed from 1 to 10 min as a function of light level measurement of PFD (photon flux density) within the and prior exposure to darkness. The lag period for dark chamber. Photosynthetic rates were measured at 10 respiration was less than 3 min, but was about 10 min different irradiances using a Kodak slide projector at 63 pm01 m-' S-' (following dark respiration) and (300 W ELH G.E. bulb) as a light source and slides fab- 4 min at 335 pm01 m-' S-' (following a 6 min dark ricated from Kodak neutral density filters. Respiration period). However, the lag period dropped to about rates were measured in the dark. Initial 0' concentra- 1 min at 335 pm01 m-' S-' if no dark period preceded tions were decreased to about 25% of air saturation by the measurement (the linear slopes remained the bubbling with NZ immediately prior to photosynthetic same). These observations became the basis for the measurements, which proceeded sequentially from the procedure outlined above, in which blade segments lowest (6 pm01 m-' S-') to the highest (1100 pm01 m-* were measured at sequential increases in PAR follow- S-') level of PAR. Rates of dark respiration were per- ing the measurement of dark respiration with the formed near levels of oxygen saturation prior to the incorporation of a 4 rnin stabilization period prior to start of the photosynthetic incubations. Temperature each measurement. was controlled at 29.0 + 0.5 "C by a refrigerated circu- Measurement of leaf chlorophyll content. Until lating water bath; a magnetic stirrer insured rapid October 1992, we extracted chlorophylls from leaf tis- mixing for both the electrode and the tissue segment. sue by repeated grinding of pre-weighed tissue sam- Digital data output was recorde~continuouslyusing a ples in 90 % cold acetone buffered with 0.05% MgC03 Computer Boards A/D converter and Labtech Note- using chilled pestles and mortars with washed sea book Software (Ver. 6.3.0) running under MS-DOS sand. The extract was made up to a known volume, on a 286-AT computer. Slopes were determined as centrifuged, and absorbances measured at 664 and 286 Mar. Ecol. Prog. Ser.

647 nm on a Shimadzu UV 160U spectrophotometer. termine significant differences among sampling dates. Chl a and b content was then determined using the Significant differences in P vs I parameters were equations from Jeffrey & Humphrey (1975) for 90% tested using a 2-sample t-test. acetone. After October 1992, we employed an alterna- tive extraction technique utilizing N, N-dimethyl for- mamide (DMF) which did not require grinding of plant RESULTS tissue, thus saving time and effort as well as reducing potential sources of error. Pre-weighed tissue samples In situ photosynthesis of entire plants were extracted overnight in glass screw-cap tubes containing DMF; the resulting extract was measured The P vs I curves for Halodule wrightii plants incu- as described above and chl a and b content determined bated in situ over a 2 yr period in Laguna Madre exhib- using the equations of Porra et al. (1989). Appropriate ited marked similarity (Fig. 4). Photosynthetic relation- corrections were made for a turbidity blank at 750 nm ships were explained well by the hyperbolic tangent in both methods. Comparison of the results using the function of Jassby & Platt (1976), with all curves ex- 2 techniques on blade tissue collected on a variety of hibiting an r2 > 0.95. Incubations conducted through- occasions yielded no significant differences in chl a out the day at a variety of light levels showed, in most or chl b content (paired t-test, p 2 0.65 and p 2 0.08 instances, no apparent or consistent differences in respectively, n = 12). photosynthetic oxygen production between morning Statistics. Sidtistical analyses were performed on a and afternoon periods at similar light levels. No obvi- 486 PC using a general linear model procedure (SAS ous seasonal trends in P vs I parameters were appar- Institute Inc. 1987). Significant differences in chloro- ent, despite temperatures that ranged from 12 to 30°C phyll content among sampling dates was tested using over the course of this study. a l-way ANOVA. When a significant difference for a Excluding the high P,,, and I, values obtained in main effect (p < 0.05) was observed, the means were January 1990, gross P,,, averaged 374 pm01 O2 g-I dw analyzed by a Tukey multiple-comparison test to de- leaf h-', and I,, averaged 319 pm01 photons m-' S-'

September 1989

600

400

200 200 7h C 0 200 400 600 800 1000 0 200 400 600 800 1000 0 200 400 600 800 1000 0 200 400 600 800 1000 3 1400 F January l990 600 May 1990

-0 600 200 5 400 U 200 0 U) 0 200 400 600 800 1000 0 200 400 600 800 1000 0 200 400 600 800 1000 0 200 400 600 800 1000 U) L a 600 February 1991 April 1991 PFD (pmol photons m -*S -l) 12°C 600 I 26.C

200 betweenFig. 4. Halodule photosynthetic wnghtii. oxygen P vs I productioncurves. Relationship and PFD 400L:~icb-' measured In situfor entire plants from May 1989 to April 0 1991. Values are X * SE; n = 3 to 4 for most light levels 0 200 400 600 800 1000 o 200 400 600 800 1000 achieved in morning (0) or afternoon (m). Where no error bars appear. SE is less than the size of the symbol. Note PFD (pm01 photons m -*S -') adjustment in y-axis scale between some months Dunton & Tomasko: Halodule photosynthesis in a hypersaline lagoon 287

Table l. Haloduie wnghtii. Seasonal variation in the Pvs Iparameters for entire plants based on in sit~measurements of oxygen evolution and root:shoot ratios (RSR)

Date Temp. Salinity P,,I,x R ad h 'c P RSR ("c) (X.) (pm01 0, g-l dw leaf h-l) (pm01m-, S-')

May 1989 28 4 5 533 117 15 353 l?? Jul 1989 30 4 7 688 75 16 434 119 Sep 1989 3 0 48 427 59 1.6 270 93 Nov 1989 26 45 386 89 1.1 345 100 Jan 1990 20 39 1104 58 2.4 453 141 Mar 1990 19 4 8 - - 0.6 - 70 May 1990 29 38 223 76 0.6 365 46 Ju1 1990 30 45 33 1 116 1 .O 321 120 Oct 1990 24 50 340 72 1.1 306 80 Feb 1991 12 3 2 140 75 0.5 286 37 Apr 1991 26 45 300 62 1.6 189 98

apm~lO2 g-' dw leaf h-' (pmol photons m-' S-')-'

(Table 1). No data on these parameters are available sponding to peaks in total chlorophyll content. The for March 1990 since maximum PFD achieved during high chlorophyll concentrations and lower chl a:chl b the entire incubation period was 343 pm01 m-' S-' due ratios in H. wrightii coincided with the highest P,,, to low incident PAR under a heavy overcast. The low- (January 1990) and lowest Ik (April 1991) recorded over est P,,,,, value recorded (140 pm01 O2 g-' dw leaf h-') the 2 yr experimental period. Blades collected in April occurred in February 1991 at an incubation tempera- 1993 for laboratory Pvs Iexperiments exhibited a total ture of 12 "C. This contrasts with the high P,,,,, value of chlorophyll concentration of 10.8 mg g-' dw (SE = 0.6, 1105 pm01 0' g-' dw leaf h-' the previous January at 20°C. Values of relative quantum efficiency, a, ranged from 0.5 to 1.6 pm01 O2 g-' dw leaf h-' (pmol photons LAGUNA MADRE m-2 s-l )-' excluding the January 1990 value of 2.4. 25 Station LM-151 Whole plant respiration generally ranged from about 60 to 90 pm01 O2 g-l dw leaf h-' (average 71 pm01 O2 g-' dw leaf h-', with 2 abnormally high respiration values (over 115 pm01 O2 g-I dw leaf h-') recorded in May 1989 and July 1990 (overall average of 80 pm01 O2 g-I dw leaf h-'). Average blade respiration from bottle incubations made during each visit to the study site g l,,,,,,,,,,,,,,,,,, was 41.5 (SE = 7.3, n = 11) compared to 16.1 pm01 O2 c- 0 AJAODFAJAODFA g-' dw h-' (SE = 4.9, n = 11) for root and rhizome tissue. Whole plant compensation irradiance (I,,) averaged 85 pm01 m-2 s-' for root-shoot ratios that ranged from 1.3 to 4.2, but was much higher for ratios of about 5 or greater. Water salinities varied in response to pre- cipitation and showed little seasonality, ranging from 32 to 52Ym.

Pigment content AJAODFAJAODFA Total chlorophyll from Halodule wnghtii leaf tissue 1989 1990 1991 ranged from 7.6 to 19.5 mg g-' dw, with peaks at 19.5 and 19.1 mg g-' dw in January 1990 and May 1991 Fig. 5. Halodule wrightii. Variations in chl a content (upper panel) and chl a:chl b ratios (lower panel) for plants collected 5). respectively (Fig. Ratios of chl a:chl b ranged from from March 1989 through May 1991 at Station LM-151. 1.3 to 2.9 over the 2 yr period of in situincubations with Values are X * SE (n = 6). Where no error bars appear, SE is lower chl a:chl b ratios (1.3 and 2.0 respectively) corre- less than the size of the symbol Mar. Ecol. Prog. Ser. 107: 281-293, 1994

incubated in situ (range 0.5 to 2.4). Since Ih is empiri- cally derived from estimates of P,,,,, and a, and P,,,,, values were relatively the same between the 2 experimental approaches, the lower Ih values for blade segments can be ascribed to the 3-fold increase in a. The higher values of a for blade segments is not related to total leaf chlorophyll concentrations and chl a:chl b ratios, which were nearly the same as recorded from leaf tissue of entire plants incubated in situ. Statistical comparisons of the Pvs Iparameters obtained between plants incubated in the field and of blade segments measured under laboratory conditions yielded values

PFD (vrnolphotons m-2S-') of Ik, Ic(leaf,/Icprand a that were significantly different (p < 0.05) between the 2 approaches. Fig. 6. Halodule wrightii.P vs I curves for 6 replicate blade segments (denoted by different symbols) measured under laboratory conditions at 29'C. Plants were collected in late Apnl 1993 from Station LM-151 DISCUSSION

Photosya%etic !ight requirements of seagrasses: n = 6) and a chl a:chl b ratio of 2.6, which were not comparison of techniques significantly different (p > 0.05) from measurements collected during the 2 yr experimental period. Efforts to gain a more thorough and accurate under- standing of the minimum light requirements necessary to sustain growth in seagrasses has focused on plant Laboratory measurements of photosynthesis using carbon budgets and the energy demands of below- blade segments ground plant tissues (Zimmerman et al. 1989, Fourqurean & Zieman 1991, Olesen & Sand-Jensen Six P vs I curves were generated from individual 1993).The importance of below-ground tissues in esti- blade segments of Halodule wrightii plants collected mating light compensation points (I,) was demon- from Station LM-151 in late April 1991 (Fig. 6). Photo- strated by Olesen & Sand-Jensen (1993), who found synthetic measurements made at 29OC in the labora- the I, for growth of entire eelgrass Zostera marina tory were described well by the hyperbolic tangent plants at 21 "C was considerably higher (47 pm01 function of Jassby & Platt (1976), and r2 was >0.95 for S-') than compared to leaves alone (30 pm01 m-, S-'). each of the curves. Estimates of leaf I, for eelgrass have been reported A summary of the calculated P vs I parameters is even lower (from 10 to 17 pm01 m-' S-') at similar tem- shown in Table 2. Gross P,,, values ranged from 356 to peratures (Dennison & Alberte 1982, Marsh et al. 491 pm01 0, g-' dw leaf h-', similar to the range in 1986). P,,,, values derived from entire plants in situ (Table 1). The incorporation of below-ground biomass, which However, Ih values ranged from 90 to 110 pm01 m-' S-', often accounts for up to 85% of the biomass of many ca one-third the average of in sifu incubated plants. seagrasses (Eleuterius 1987, Lindeboom & Sandee Similarly, values of a averaged ca 3 times greater for 1989, Dunton 1990, Fourqurean & Zieman 1991), can blade segments [range 3.4 to 5.3 pm01 0, g-I dw leaf therefore have a profound impact on estimates of I, for h-' (pmol photons m-2 S-')-'] than in whole plants entire plants, and hence on H,,,,, the duration of time

Table 2. Halodule wrightii.Comparison of average P vs I parameters gathered from entire plants incubated in the field at 28 to 30°C (see Table 1) versus blade segments examined under controlled laboratory condtions at 29OC. Values are R*SE

Parameter Entire plants (field) Blade segments (lab) Comparison of P vs I (n = 5) (n = 6) parameters

P,,, (pm01 O2 g-I dw leaf h-') 441 r 80 421 * 21 p = 0.82 a [pmol O2 g-I dw h-' (pm01 photons m-2 S-')-'] 1.3 + 0.2 4.2 + 0.3 p = 0 0004 I, (pm01 m-' S-') 349 r 27 101 + 4 p = 0.0008 I, (pm01 m-2S-') 111 *21 22 + 2 p = 0.0001 Dunton & Tomasko: Halodulephotosynthesis in a hypersaline lagoon

Table 3. Variation in Ikand I, values as a function of the expenmental approach employed for measurement of photosynthesis in eelgrass Zostera manna nd: not determined

ih 4 Temp. Technique Location Source (pm01 m-2 S-') ("C) (USA)

230 28 15 Bottles, 7 cm leaf segments. California Drew (1979) Winkler 100 10 20 Rank Bros. O2 electrode Woods Hole. MA Dennison & Alberte (1982) chamber, 2 cm blade segments 348 nd 20 Large chambers in situ, entire Chesapeake Bay, VA Wetzel & Penhale (1983) plants, I4C uptake 65-120 15-25 20 Rank Bros. O2 electrode Woods Hole. MA Dennison & Alberte (1985) chamber, 2 cm blade segments 7 8 17 20 Rank Bros. O2 electrode Woods Hole, MA Marsh et al. (1986) chamber, 2 cm blade segments 35 nd 15 Small-volume chamber, blade San Francisco Bay, CA Zimmerman et al. (1991) segments, O2 electrode

that PAR is above compensation irradiance. In this Values of <3 pm01 m-2 S-' for I, at temperatures of study, our estimates of whole plant compensation irra- 10 "C or less have been reported for eelgrass (Marsh et diance (I,,) for Halodule wrightii were also consider- al. 1986), whose lower depth boundary corresponds to ably higher than that of blade I, (Table 2). However, 11% of surface irradiance (Dennison 1987, Olesen & the reasons for this difference cannot be attributed Sand-Jensen 1993). However, I, values for growth in solely to the inclusion of below-ground tissue respira- some common macroalgae are also close to this range tion in the calculation of I,,, since blade respiration of (0.3 to 2.5 pm01 m-2 S-'), yet their minimum light laboratory incubated plant segments was often greater requirements are nearly an order of magnitude lower, than the respiration values calculated for entire plants 0.12 to 0.61% of surface PAR (Markager & Sand- measured in situ. The higher respiration for 3 cm blade Jensen 1992). Similarly, values of 35 pm01 m-2 s-' for segments may be due to a cumulative wounding effect saturation irradiance (at 10 to 15OC) for eelgrass that is minimized when using entire leaves in 300 m1 (Marsh et al. 1986, Zimmerman et al. 1991) are lower BOD bottles. However, the effect of elevated leaf seg- than reported for arctic kelp (Dunton & Jodwalis 1988), ment respiration on Ic,is minimized by the higher pho- whose total annual quantum dose of irradiance is prob- tosynthetic response of leaf tissue in laboratory incuba- ably received by most seagrass communities within a tion~.The greater photosynthetic response of blade 1 wk summer period (Dunton 1994). segments at limiting light levels cannot be attributed to The apparent differences in the minimum light re- changes in leaf chlorophyll content, which have quirements needed to sustain growth and achieve remained virtually unchanged between 1989 and 1993 light-saturated photosynthesis are largely explained (present paper and Dunton unpubl. data). The photo- by the experimental techniques employed, as shown synthetic performance of blade segments of H. wrightii in this study and as summarized in Table 3 for Zo- from other sites in south Texas at 30 'C have also been stera marina. In eelgrass, I, and Ik values were gener- nearly identical to the response depicted in Fig. 6 for ally lowest when blade segments were oriented per- this species (Czerny 1994). pendicular to a directed light field, usually within a The measurement of photosynthesis in the labora- small stirred chamber (e.g. Marsh et al. 1986, Zim- tory, in which a small blade segment of Halodule merman et al. 1991). In contrast, I, and Ik values were wrightii was positioned perpendicular to a directed considerably higher when whole leaves or blade seg- light field, resulted in high relative quantum efficien- ments were incubated in bottles or large chambers cies (a). Plants incubated in situ under a naturally which were not purposely aligned to incoming PAR diffuse underwater light field exhibited lower values (Drew 1979, Wetzel & Penhale 1983), as also shown of a. In the absence of any significant difference in in this study. Estimations of H,,,, the duration of irra- chlorophyll concentration, field- and laboratory-incu- diance-saturated photosynthesis (Dennison & Alberte bated plants exhibited similar rates of light-saturated 1982), may therefore vary widely. The use of labora- photosynthesis (Table 2). Consequently, I, and Ik val- tory-derived P vs I parameters may lead to an overes- ues for laboratory-incubated plants are significantly timation of photosynthesis as argued by Fourqurean lower. & Zieman (1991), or to prediction of maximum depth 290 Mar. Ecol. Prog. S

limits that are not observed in the field (Zimmerman one instance we conducted P vs I measurements at et al. 1991). 12°C (early February 1991), and found that P,,, values Continuous measurements of underwater irradiance dropped to 140 pm01 O2 g-' dw leaf h-', compared to near the maximum depth limits of Halodule wnghtii the overall average of 374 pm01 0, g-' dw leaf h-' The clearly indicate that the depth limits and productivity large decrease in light-saturated photosynthesis in H. of H. wrightii cannot be explained using P vs I para- wrightii at 12 "C is a consequence of reduced metabolic meters derived from our laboratory experiments using activity caused by the temperature dependence of the blade segments (Dunton 1994). Evidence for this con- dark reactions of photosynthesis, as reported in several clusion is based on observations from 3 different estu- studies on seagrasses (reviewed by Bulthuis 1987). arine systems in south Texas. Compilation of data pre- In contrast, the extremely high P,, measured at sented in this paper and Pvs I measurements collected 20°C in January 1990 (1104 pm01 O2 g-' dw leaf h-') at 2 other locations in Texas (Dunton unpubl. data), corresponded with a peak in total leaf chlorophyll and have established Ik(t,eldland I,, values for H. wrightii of low chl a:chl b ratios. The significant increase in blade 315 and 80 pm01 m-2 S-' respectively. Based on this chlorophyll followed a precipitous drop in underwater information, Dunton (1994) found that the onset of a PAR during the preceding months (Dunton 1994). A brown algal bloom in late spring 1990 in Laguna second peak in blade chlorophyll content in May 1991 Madre (Stockwell et al. 1993) dropped Hsat,fleld,values was also associated with extremely low values of from 5 to about 2 h. The decline in H,,, also coincided underwater irradiance (Dunton 1994) and a lower Ik with a 24 to 46% decrease in spring leaf elongation value. Increases in chlorophyll content in aquatic rates and a steady decline in total plant biomass to less plants has been associated with significant correlations than half pre-brown tide levels; in contrast Hsat(lablval- in both a (Goldsborough & Kemp 1988) and P,, ues exhibited little change (remaining at or above 6 h) (Nielsen & Sand-Jensen 1989). These observations when derived from laboratory P vs I parameters indicate that Halodule wrightii may possess some (Ikjlabj= 101 pm01 m-2 S-'). At the deep edge of a sea- capacity for photosynthetic adjustment in response to grass bed in Corpus Christi Bay, H,a,(f,,~ld,during spring its underwater light environment as reflected by and summer generally averaged 3 to 5 h compared to changes in P vs I parameters. Such adjustments have 27 h for Hsat(lab,;in San Antonio Bay, a H. wrightii bed been well documented in experimental manipulations disappeared when Hsatlfleld)dropped to < 2 h over an with underwater irradiance for Zostera marina (Denni- 8 mo period but values remained well above 5 h son & Alberte 1985). Additionally, seagrasses from (Dunton 1994). In all 3 examples noted above, Hsatllabl deep edges of meadows typically have higher chloro- values were either largely insensitive to declines in phyll content than plants from shallow edges (Drew water transparency to which H. wrightii responded, or 1978, Wiginton & McMillan 1979, Dennison & Alberte provided unrealistic estimates of H,,, for populations 1982, 1985, Dawes & Tomasko 1988). living near their maximum depth. In conclusion, We observed no differences in photosynthetic pro- although laboratory measurements of photosynthesis duction between morning and afternoon incubations at using blade segments are invaluable in addressing similar light levels. However, Halodule wnghtii was specific physiological questions [e.g. temperature not normally exposed to levels of PAR above 800 pm01 effects on photosynthesis (Marsh et al. 1986), inorganic m-2 s-l and failed to show any clear signs of photo- carbon uptake effects on photosynthesis (Durako inhibition at higher light levels. In contrast, Libes 1993)l extrapolation of laboratory P vs I parameters (1986) noted a depression in afternoon photosynthesis to field populations may not provide the accuracy in Posidonia oceanica that were incubated in situ, but required to successfully model seagrass production attributed this response to the high light conditions from in situ measurements of PAR. that occurred during the day when plants were frequently exposed to an irradiance equivalent to 1400 pm01 m-2 S-'. Photosynthetic performance in Halodule wrightii The light-saturated rates of photosynthesis for Halo- dule wrightii reported here are in the range of values We observed little variation in P vs I parameters in reported for Halodule spp. in previous studles using Halodule wrightii over the 2 yr experimental period. bottles or large incubation vessels in sifu (Williams & This is most likely a consequence of the small temper- McRoy 1982, Morgan & Kitting 1984, Lindeboom & ature range of most incubations (between 24 and Sandee 1989, Zieman et al. 1989) or under artificial 30°C), the lower resolution of this approach in the light (Beer & Waisel 1982). For H. wrightii, Williams & measurement of photosynthetic oxygen evolution and McRoy (1982) noted that P,,, ranged from about 250 to the corrections required for chamber oxygen demand 340 pm01 C g-' dw leaf h-' for Texas plants, and from (compared to controlled laboratory experiments). In about 250 to 1580 pm01 C g-' dw leaf h-' for Puerto Dunton & Tomasko: Halodule photosynthesis in a hypersaline lagoon 291

Table 4. Comparison of light-saturated rates of gross photosynthesis among seagrasses, freshwater angiosperms, and terrestrial plants based on rates of oxygen evolution. Asterisks denote rates of carbon production that were converted to oxygen based on a photosynthetic quotient of unity

Species Temp. P,,,,, 1.1rnol Or h-': Source -- ("C) g -l dw mg chl-' Seagrasses Cymodocea nodosa Drew (1979) Halodule tvrjqhtij This study Halophila stipulacea Drew (1979) Phyllospadix torreyi Drew (1979) Posidona oceanica Drew (1979) Ruppia drepanensls Garcia et al. (1991) Thalassia testidmum Dawes & Tomasko (1988) Zostera marina Drew (1979) Zostera marina Denn~son& Alberte (1982) Freshwater angiosperms Elodea canadensis Nielsen & Sand-Jensen (1989) Myriophyllurn spicatum Nielsen & Sand-Jensen (1989) Potamogeton crispus Nielsen & Sand-Jensen (1989) Terrestrial plants Shade plants 25 - 0.8' 9 2' Bjorkman (1981) Sun plants 25 - 2.1' 39.5 ' Bjorkman (1981)

Rico plants. In Florida Bay, Zieman et al. (1989) models that utilize parameters of H,,, and H,,,,. Mean reported leaf production in H. wrightii ranging from ratios of net photosynthesis to dark respiration (P,,,,: R), 126 to 277 pm01 C g-' dw h-'. In studies of H. uninervis useful indicators of plant productivity (Bowes & in the Red Sea, Beer & Waisel (1982) reported an Ik Salvucci 1989), generally ranged from 2 to 4 for H. value of 300 pm01 m-' S-', ICII,,,,values of 20 to 40 pm01 wrightii, slightly lower than blade P,,,,:R ratios m-2 S-', and P,, values of 21 pm01 O2 mg chl h-'. reported for Zostera marina (Zimmerman et al. 1991). Interestingly, we found light-saturated rates of photo- However, P,,,: R values for H. wrightii include the res- synthesis, expressed per unit chlorophyll content, for piratory demands of below-ground tissue as well as H. wrightii and other seagrasses similar to values leaves. Based on our observations of the depth distnb- reported for other aquatic plants and in terrestrial ution and productivity of H. wrightii in Texas estuaries, leaves (Table 4). However, photosynthetic production the Pvs Iparameters derived from whole plant incuba- in submerged aquatic macrophytes per unit biomass or tions are more realistic than laboratory-derived values surface area is usually lower than in terrestrial plants, and can be used reliably in models that address sea- as noted by Nielsen & Sand-Jensen (1989), because of grass production and their minimum light require- the thinner leaves and thus lower chlorophyll content ments. However, uncertainty with respect to the car- possessed by submerged plants. The chlorophyll con- bon demands and role of below-ground tissue continue tent and chl a:chl b ratios presented in this paper for to compromise our ability to effectively manage sea- blade tissue of H. wrightij are in general agreement grass populations that are increasingly subjected to with results for a variety of seagrasses (Drew 1978, chronic reductions in underwater light. Wiginton & McMillan 1979, Dennison & Alberte 1982, Garcia et al. 1991, Zimmerman et al. 1991). The measurements of photosynthetic production Acknowledqements. We thank our enthusiastic field crew, S. presented here provide a mire redlistic estimate of the Archer, B Hardegree (who always found the site), T. ~lson, in situ physiological light requirements for and J. Tolan and our equally cheery laboratory technicians M. Herndon and K. Jackson for their excellent support of this wrightii. In measurements are because research. Our gratitude and special thanks to S. Schonberg they take into account problems relating to self-shad- for aqain providinq crucial computational and qraphical assis- ing (Pkrez & Romero 1992) and natural variations in tance. his stud; benefited greatly from di&;ssions with underwater irradiance. These estimates are useful in many colleagues, most of whom are referenced in this paper. We also gratefully thank C. Onuf. J. Lawrence and 2 anony- net carbon under different light mous reviewers who provided very helpful and constructive regimes and in theoretical calculations of the minimum ,,tlcisms on earlier drafts of this ~h~ work was daily quantum requirements of H. wrightii based on supported by the Texas Higher ducati ionCoordinating 292 Mar. Ecol. Prog. SE

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This article was presented by J. M. Lawrence (Senior Manuscript first received: August 13, 1993 Editorial Advisor), Tampa, Florida, USA Revised version accepted: January 25, 1994