Seagrass survival during pulsed turbidity events: the effects of light deprivation on the seagrasses...

Aquatic Botany 65 (1999) 105–121

Seagrass survival during pulsed turbidity events:the effects of light deprivation on the seagrasses

Halodule pinifoliaandHalophila ovalis

B.J. Longstaff, W.C. Dennison∗Department of Botany, The University of Queensland, St. Lucia, Queensland 4072, Australia

Abstract

Pulsed turbidity events caused by factors such as flooding rivers have the potential to seriouslyimpact seagrass communities by depriving the plants of all available light. The effects of lightdeprivation was investigated on the survival, morphology and physiology of the tropical seagrassesHalodule pinifoliaandHalophila ovalisgrowing in the South-East Gulf of Carpentaria, Australia,a region where pulsed flood events are common. Additionally, physiological and morphological re-sponses to light availability along natural gradients were examined. Responses to both experimentaland natural light gradients were investigated for their potential use as indicators of impending sea-grass loss during pulsed turbidity events.H. pinifolia was deprived of light for 80 days using in situshade screens and the following parameters measured at three depths and under the shade screens:biomass, shoot density, canopy height, amino acid content, chlorophyll content,d13C signature, %Cand sugar concentration. The quantity of light was extremely variable, with mean daily irradiancesbetween 9–12 mol photons m−2 day−1, and a range of 0.05–42 mol photons m−2 day−1. H. pinifo-lia leaf amino acid content increased with increased water depth (from 8 to 18mmol g fresh wt.),chlorophyll a to b ratio decreased (from 2.4 to 2.1) andd13C values became more negative (from−9 to−12).H. ovalisdisplayed little tolerance to light deprivation, with plant death occurring after38 days in the dark.H. pinifolia showed a high degree of tolerance to light deprivation with nobiomass loss before day 38 and complete die-off predicted after 100 days. Shoot density, biomassand canopy height all declined after 38 days. Physiological parameters that responded significantlyto the light deprivation were the amino acids which increased (from 20 to 80mmol g fresh wt.), thechlorophyll a to b ratio which decreased (from 2.5 to 2.1) and the values which became more neg-ative (from−9 to−10). Changes in leaf physiology (e.g. amino acid content, chlorophyll contentandd13C) occurred before morphological changes (e.g. biomass, shoot density, canopy height) ordie-off, and were thus considered to be potential indicators of impending seagrass die-off duringlight deprivation. In conclusion, only long duration (>38 days) pulsed turbidity events would have a

∗ Corresponding author. Tel.: +61-7-3365-2073; fax: +61-7-3365-7321E-mail address:[email protected] (W.C. Dennison)

0304-3770/99/$ – see front matter ©1999 Elsevier Science B.V. All rights reserved.PII: S0304-3770(99)00035-2

106 B.J. Longstaff, W.C. Dennison / Aquatic Botany 65 (1999) 105–121

detrimental impact onH. pinifolia growing in the Gulf of Carpentaria and that by assessing specificphysiological responses, seagrass loss during pulsed turbidity events can predicted. ©1999 ElsevierScience B.V. All rights reserved.

Keywords:Pulsed turbidity; Survival; Seagrass;Halodule; Halophila; Light deprivation

1. Introduction

Distribution and abundance of seagrasses is controlled by a range of environmental con-ditions including light availability (Dennison and Alberte, 1985; Dennison, 1987), nutri-ent availability (Short, 1987), water motion (Fonseca and Kenworthy, 1987) and grazing(Lanyon et al., 1989). Of these, light availability is considered one of the more important en-vironmental parameters, controlling the depth to which seagrasses can grow and excludingseagrasses from areas with low light conditions (Dennison et al., 1993; Abal and Dennison,1996) While it is recognised that the quantity of light required by seagrasses is high in com-parison to other marine and terrestrial flora (Dennison et al., 1993; Duarte, 1991; Abal etal., 1994), there is still much contention on the actual quantity of light required by seagrassfor long-term survival. Estimates of light requirements of seagrasses differ between species(e.g., 4.4 and to 29% of surface light) and within a species (e.g. 5 to 20% of surface light)(Dennison et al., 1993) while an average requirement of seagrasses as a group of plants hasbeen calculated to be 11% of surface light (Duarte, 1991).

One reason that large differences in light requirements have been calculated is that lightmeasurements are often conducted over short time scales and do not account for the effectof seasonal or pulsed changes in light availability (Moore et al., 1997). The importance ofpulsed turbidity events on seagrass survival was recently highlighted when over 1000 km2

of seagrass were lost from a region after two flood events in short succession (Preen et al.,1995). Pulsed turbidity events are caused by factors such as sediment resuspension duringstrong winds, dredging activities and flooding rivers (Longstaff et al., 1999; Zimmermanet al., 1991; Moore et al., 1997). Due to the extreme nature of these events seagrassescan be deprived of nearly all light for brief or extended periods. The duration of the lightdeprivation can vary from 2–3 days during wind driven resuspension events to many weeksduring flooding events (Longstaff et al., 1999; Zimmerman et al., 1991; Moore et al., 1997)

Seagrass species vary widely in their tolerance to light deprivation. Some species have alow degree of tolerance, surviving for only 1 month when deprived of light (e.g.,Halophilaovalis, Longstaff et al., 1999). Other species show a high degree of tolerance, surviving formore than 5 months below their minimum light requirements (e.g.,Thalassia testudinumLee and Dunton, 1997;Posidonea sinuosa, Gordon et al., 1994). As seagrass species havedifferent (a) long-term light requirements and (b) tolerances to transient period of lightdeprivation, the distribution, abundance and composition of seagrasses in a region may bea function of both the long-term trends in light availability and by their ability to survivepulsed turbidity events (Longstaff et al., in press; Moore et al., 1997)

The purpose of this study was to determine the impacts of pulsed turbidity events on thesurvival ofHalodule pinifoliaandH. ovalis. In addressing this aim, the effects of natural lightgradient (occurring with increased water depth) and the effects of light deprivation (achieved

B.J. Longstaff, W.C. Dennison / Aquatic Botany 65 (1999) 105–121 107

Fig. 1. Location of seagrass, experimental site and natural light gradient monitoring sites on Alligator Banks inthe South-East Gulf of Carpentaria.

through shading) were studied. In addition, a suite of morphological and physiologicalresponses ofH. pinifolia were assessed to determine if any of these responses to lightdeprivation could be used as biological indicators of impending seagrass loss during pulsedturbidity events.

2. Methods

2.1. Site selection

The study was conducted in a remote 15 km2 area of seagrass in the South Eastern cornerof the Gulf of Carpentaria, Australia, near the Port of Karumba (17◦27.4′ S 140◦45.6′ E)(Fig. 1). Weather patterns in this tropical location are characterised by summer monsoonalrains resulting in pulsed river flows. Frequency and duration of the pulsed river flows wasassessed through the interpretation of long-term (10 years) rainfall data for the region(obtained from the Bureau of Meteorology).

Seagrass was present predominantly within the intertidal region, with an approximatevertical distribution ranging between 0.1 m below lowest astronomical tide (LAT) and 1.5 mabove LAT in a region that experiences a tidal range of 3 m. The dominant seagrass in thearea wasH. pinifolia, a thin-leaved seagrass with a relatively homogenous distribution.H.ovalis, a small broad-leafed seagrass occurred as an understorey species with a low biomassand a patchy distribution.

Five sampling sites were established in the seagrass meadow between July and November1996 (Fig. 1). Two sites were located towards the shallow edge of the meadow (Sites 1 and2), one site was located within the middle of the meadow (Site 3) and two sites were locatedat the deep edge of the meadow (Sites 4 and 5). Shade screens were deployed at the shallowedge (Site 1). Integrated light measurements were conducted at one shallow site (Site 1) andthe two deep sites (Sites 4 and 5). All sites were used for measurements of physiologicaland morphological responses to natural light gradients.

2.2. Natural light gradient investigation

Light availability was measured using 2p light sensors (Dataflow systems, Australia)programmed to determine the average quantity of light over a 5 min interval. Two of these


light sensors were placed at the deep edge of the seagrass meadow (Sites 4 and 5) andone near the shallow edge of the meadow (Site 1) (Fig. 1). At these sites the light sensorwas arranged so that light at the top of the canopy was being monitored. The sensors werecleaned at 7–10 day periods during which time the data from the loggers was downloaded.

To determine the variability of seagrass morphology and physiology along the naturallight gradient, samples of seagrass were collected from the five monitoring sites in October,1996. At each monitoring site three seagrass cores were randomly collected using a sedimentcorer (15 cm diameter, 25 cm deep). Cores were washed in salt water to remove sedimentsand then stored at –18◦C until analyses.

2.3. Light deprivation experiment

Seagrasses were deprived of light using 2.2 m diameter screens covered in black poly-thene. Three of these screens were randomly erected about the experimental site by sus-pending them 0.25 m above the substrate surface using steel rods (Fig. 2). Three non-shadedcontrol treatments (2.2 m diameter) were also randomly established about the site. Severingconnecting rhizomes with a knife prevented translocation of material between shaded andadjacent non-shaded seagrasses.

The quantity of light available to the seagrass at the shaded and non-shaded area wasdetermined using a 2p light sensor and a logger which was programmed to average quantaover a 5 min interval. The light loggers were secured into the sediment with the sensorprotruding to the top of the seagrass canopy. The sensors were cleaned at 7–10 day periodsduring which time the data from the loggers was downloaded. The gradient of light underthe shade screens, from the edge to the centre, was determined at 0.2 m intervals using aLi-Cor 4p quantum sensor.

Seagrass samples were removed from the shaded and control sites at 7–14 day intervalsfor a 78 day period. At each sample time, three cores of seagrass were removed from each

Fig. 2. Shading apparatus used to deprive seagrasses of light. The 2.2 m screen is covered in black polythene andthen suspended above the seagrass with steel supports. Graph demonstrates the percentage of ambient light thatcan penetrate beneath the shade screens.


replicate using a sediment corer (15 cm diameter, 25 cm deep). Cores were washed in saltwater to expose intact root, rhizome and shoot material, the washed seagrass was immedi-ately frozen until required for analysis. To avoid destruction of the shaded area through thecontinued removal of sediment cores, each core that was removed from an experimentalunit was replaced by a core collected at least 10 m distance from the experimental site. Toavoid coring a previously cored area, a plastic tag was placed in the centre of transplantedcores to mark its location. At the termination of the experiment, a number of transplantedcores were carefully retrieved to determine the extent of rhizome exchange between trans-planted areas and surrounding area. This investigation established that minimal exchangeof rhizome between transplanted and non-transplanted seagrass occurred.

2.4. Sample analysis

2.4.1. Biomass, shoot density and canopy heightSeagrass samples collected from the shading experiment and natural light gradient sur-

vey, were sorted into above-ground (leaves) and below-ground (rhizome + roots) material.Below-ground tissue was rinsed in freshwater then oven-dried (60◦C; 48 h). Above-groundmaterial was retained for determination of shoot density (m−2) and canopy height. Canopyheight was defined as the mean length of the 10 longest shoots per sample. After morphome-tric analysis, above-ground material was also dried (60◦C; 48 h) for biomass determination.

2.4.2. Amino acidsFresh tissue from the central section of approximately 10H. pinifolia leaves was used for

all amino acid analyses. The central section of the leaf was used to avoid new basal growthand the older decaying leaf tip. The fresh leaf material was weighed (∼0.1 g), diced into1 mm2 sections and placed in 2 ml of methanol. Samples were then stored at<4◦C untilquantitatively analysed for amino acids with a Beckman 6300 High Performance AminoAcid Analyser.

2.4.3. Chlorophyll contentChlorophyll analysis was conducted on the central 40 mm of three leaf blades per site. The

width of the 40 mm sections was measured using Vernier callipers in order to determinethe area of leaf material analysed. Leaf blades were macerated using a razor blade thenground using a mortar and pestle with 10 ml of 80% acetone. The acetone extracts werestored at 4◦C for 12 h to settle suspended material. Absorbance of the extracts was thenmeasured in a spectrophotometer at 725, 663 and 645 nm (Dennison, 1990). Chlorophyll aand b concentrations were calculated according to Arnon (1949).

2.4.4. Stable carbon isotope ratio (d13C) and percent carbon (%C)Samples of fresh leaf tissue were collected from each survey site, oven dried (60◦C;

48 h), then ground to a powder in a rotary vane mill. Ground samples (sample weightwas x to x mg dry wt.) were oxidised in a Roboprep CN Biological Sample Converterand the resulting gases analysed for percentage carbon (%C),13C and12C isotopes using acontinuous flow-isotope ratio mass spectrometer (Europa Tracemass). Carbon stable isotope


ratios (d13C) are expressed as the relative per million (‰) difference between the sampleand the standard of Pee Dee Belemnite carbonate (Peterson and Fry, 1987).

2.4.5. Storage carbohydrate analysisOven-dried rhizome material was ground to a fine powder using a rotary vane mill. Sugars

were removed from the ground tissue with three sequential 5 min extractions in 80% (v/v)ethanol at 80◦C. Sugar content of the extract was determined by the phenol–sulphuric acidcolorimetric method (Dubois et al., 1956) using sucrose as a standard.

2.4.6. Leaf growthThe effect of light reduction on leaf growth was assessed after 60 days of light deprivation.

At each shade site a 25 cm2 area of seagrass was defined using plastic pegs. All seagrassleaves within the defined area were trimmed to the height of the sediment surface withscissors. After 7 days, a core of seagrass was carefully removed from the centre of themarked area. Leaf growth was calculated as the quantity of leaf material produced (g drywt.) during the 7 day period. Growth per shoot was calculated by dividing the new leafbiomass by the number of shoots. Growth per m2 was calculated by multiplying the growthper shoot by the shoot density.

2.5. Statistical analysis

2.5.1. Natural light gradient investigationMeans and standard errors of all variables were calculated for each survey site. The

relationship between measured variables and sample depth was statistically tested usingone-way analyses of variance, followed by the Fisher’s pair-wise comparison of means. Aprobability value ofp< 0.05 was considered significant.

2.5.2. Responses to light deprivationMeans and standard errors of each variable were calculated for each light treatment and

sample time. Split unit analysis of variance (ANOVA) was used to test for significant dif-ference between light treatment. Significant results were followed with a one-way ANOVAto test for differences between the treatment and control at each sample time. Seagrassparameters only measured after 78 days of shading were tested using students t-test. Aprobability value ofp< 0.05 was considered significant for all tests. All statistical analyseswere conducted using theMINITAB software package.

3. Results

3.1. Natural light gradient

Rainfall in the South-East Gulf of Carpentaria is generally restricted to 3–4 months ofthe year with a dry period separating the wet seasons (Fig. 3). Rainfall during the rainyseason is also variable, with days of extreme falls (200 mm) being followed by days of little


Table 1Quantity of light received by seagrass at monitoring sites and experimental area; LAT = Lowest astronomical tide

Approximate depth(m above/below LAT)

Mean daily irradiance(mol photons m−2

day−1)

Maximum–minimumdaily irradiance (molphotons m−2 day−1)

Light availability(% surfaceirradiance)

Surface 63 78–7 100Site 1 (Control) 1.5 m above LAT 30 58–0.1 47Site 1 (Shaded) 1.5 m above LAT 0.106 0.175–0 0.16Site 4 (Deep edge) 0 m at LAT 12 42–0.1 19Site 5 (Deep edge) 0.1 m below LAT 9 39–0.05 14

rainfall (<20 mm). This rainfall data not only demonstrates the extremes of rainfall, but alsoindicates the pulsed nature of the river flows and resultant turbidity plumes in the region.

Light monitoring over the 4-month monitoring period demonstrated that the ambient lightenvironment in the South East Gulf of Carpentaria was highly variable even within the dryseason. Periods occurred when the seagrass was receiving almost no light and days whenthe seagrass was receiving very high light (Table 1). The variability of the light climatewas due to the intertidal location of the seagrass in an environment of naturally turbidwater. Surface irradiance values during the experimental period were high and consistentdue to long periods of cloudless days. Quantity of light reaching the seagrass at Site 1 was,on average, half the surface irradiance, but as with all the sites, the light was temporallyextremely variable. Periods of very low or zero light would occur on days when high tidesoccurred at midday, and high light conditions occurred when low tides occurred duringmidday. At the deep edge of the seagrass meadow, mean daily irradiance was only 15–20%of surface irradiance, and for the same reasons as the shallow site was temporally extremelyvariable (Table 1).

H. pinifolia was the dominant seagrass in the study region, with a biomass of 113 g drywt. m−2 being recorded at Site 4. In comparison,H. ovalisbiomass is significantly lowerwith no H. ovalisgrowing at the deeper sites and very little ( less than 3 g dry wt. m−2) atthe shallow site. The biomass ofH. pinifolia did not decline with depth (as was predictedby known responses to reduced light with depth) with the deepest sites recording both thegreatest (113 g dry wt. m−2) and least (17 g dry wt. m−2) biomass values (Table 2 ). Thenarrow width ofH. pinifolia leaves meant that very high shoot densities could occur with3528 shoots m−2 recorded at the shallow site (Table 2). The mean canopy height ofH.pinifolia shoots was not significantly different between sites (15–17 cm) except for Site 4which had significantly shorter shoots (12 cm).

Amino acid concentrations ofH. pinifolia leaves at the five survey sites ranged from 8to 18mmol g fresh wt.−1(Table 2). Unlike the biomass and shoot density, the amino acidconcentrations showed an increasing trend with water depth. Leaves from the shallow siteshad significantly lower (p< 0.05) amino acid concentrations than the deep sites. However,amino acid concentration at the mid-depth site was not significantly different from those atthe shallow site or deep Site 4.

The ratio of chlorophyll a to b withinH. pinifolia leaves ranged from 2.0 to 2.4 (Table2). A decrease in chlorophyll a to b ratio was observed with increasing water depth; ratiosat the deep edge sites being significantly lower than the ratios at the mid and shallow sites.


Table 2Mean values forHalodule pinifoliamorphology and physiology at the five monitoring sitesa

Shallow Mid Deep

Site 1 Site 2 Site 3 Site 4 Site 5

Biomass (g dry wt. m−2) 96 a 31 a 35 a 113 a 17 aShoot density (shoots m−2) 3528 a 2371 abc 1736 bd 3715 a 1363 cdCanopy height (cm) 15 a 17 a 16 a 12 16 aAmino acid conc.(mmol g fresh wt.−1) 8 a 8.6 a 10.6 ac 13.7 bc 17.6 bChlorophyll content (mg chlorophylla + b cm−2) 21 a 36 28 b 23 a 30 bChlorophyll ratio (Chlorophyll a/b) 2.4 a 2.3 a 2.4 a 2.2 b 2.0 bCarbon isotope ratio (d13C) −9.9 a −9.3 a −10.7 b −11.9 c −12.3 cSugar concentration (mg g dry wt.−1) 21 a 21 a 40 a 35 a 26 aLeaf carbon content (%) 32.5 ab 31.7 a 33.5 acd 34.9 c 34.1 bd

a Values in each row with the same letter are not significantly different atp< 0.05.

H. pinifolia leaf chlorophyll a + b concentrations at the five sites ranged from 22 to 37 mgchlorophylla + b cm−2 (Table 2). There was no observable relationship between chlorophyllcontent and depth.

The ratio of the light12C isotope in relation to the heavier13C isotope (d13C) also changeddown the depth gradient. The mean13C of H. pinifolia leaves at the two deep edge siteswas –12‰ (Table 2). This value was significantly different (p< 0.05) than the mean value–10‰, recorded at the two shallow sites. Mean %C concentration inH. pinifolia leavesranged between 32 and 35%. The two deep edge sites had slightly higher mean values(34–35%) than the shallow sites (32–33%), however, these differences were not significant(p> 0.05). Sugar concentrations in the rhizome ofH. pinifolia from the five survey sitesranged between 20 and 40 mg g−1. There was no relationship between sugar content andseagrass depth (Table 2).

3.2. Responses to light deprivation

The quantity of light across the radius of the shade screens was assessed using a 4p

light sensor that monitors incoming light from all angles. Using this sensor we demon-strated that light at the edge of the screen is reduced by half and that light was rapidlyreduced over the first 0.2 m to less than 2% of ambient light (Fig. 2). Long-term mon-itoring of light was conducted using 2p sensors that only measure down-welling lightand as a consequence values would be lower than those measured using a 4p sensor.Long-term monitoring showed that the seagrass received an average down welling ir-radiance 0.106 mol photons m−2 day−1, corresponding to 0.35% of ambient light(Table 1).

No significant decline in the biomass ofH. pinifoliawas observed after 38 days of shadingto 0% of ambient light (Fig. 4a). Time course analysis demonstrated that biomass declinedrapidly after day 38, with the biomass at day 78 being 70% less than at day 38. Extrapolationof the biomass decline beyond the duration of the experiment indicates that complete plantdie-off would occur after 90 to 100 days in the dark. Biomass ofH. ovalisreceiving 0% ofambient light, declined rapidly during the first 38 days of light deprivation, with nearly alltheH. ovalishaving died by day 38 (Fig. 4b).


Fig. 4. Responses ofHalodule pinifoliaandHalophila ovalistotal biomass to 78 days of light deprivation.

The density ofH. pinifoliashoots during shading followed a similar pattern as the biomass(Fig. 5a). No significantly decline in shoot density (p> 0.05) occurred over the first 38 daysof light deprivation but between day 38 and 78 the shoot densities declined significantly(p< 0.05) to less than 1200 shoots m−2. Mean canopy height ofH. pinifolia prior to shadingwas 13 cm (Fig. 5b). Canopy height of shaded plants increased significantly (p< 0.05) overthe first 38 days of light deprivation to 15 cm. Between day 38 and 78 canopy height declinedsignificantly (p< 0.05) to 10 cm.

The amino acid concentration ofH. pinifolia increased significantly (p< 0.05) duringshading, with concentrations at day 67 being over 7 times the control concentrations (Fig.6a). The amino acids proline, glutamine and asparagine comprised over 80% of the totalamino acid content of these plants.

Chlorophyll concentration of non-shadedH. pinifolia was 21 mg cm−2, however, after78 days of shading chlorophyll concentrations increased significantly (p< 0.05) to 32 mgchlorophylla + b m−2 (Table 3 ). Prior to shading, the chlorophyll a to b ratio inH. pinifolialeaves was 2.5 (Fig. 6b). During shading, the chlorophyll a to b ratio declined significantly(p< 0.05) to 2.15. At day 38, however, the chlorophyll a to b ratio of control plants alsodeclined, so that on day 38 there was no significant difference between plant from the 0%ambient light treatment and the control treatment.

During light deprivation the lighter12C isotope was preferentially taken up over theheavier13C isotope and as a consequence thed13C value declined during shading (Fig. 6c).Initial 13C values were approximately –9‰, and declined significantly to−10.5‰ when


Fig. 5. Effects of light deprivation on the shoot density and canopy height of the seagrassHalodule pinifolia.

Table 3Means forHalodule pinifolialeaf physiology and growth after 80 days light deprivationa

Control 78 days light deprivation

Chlorophyll concentration (mg chlorophylla + b cm−2) 21± 0.9 a 28± 0.9 bRhizome sugar concentration (mg g dry wt.−1) 21± 1.7 a 23± 2.5 aLeaf %C 32± 0.6 a 26± 0.5 bShoot growth rate (mg dry wt. shoot−1day−1) 0.22± 0.03 a 0.1± 00 aAreal growth rate (mg dry wt. m−2 day−1) 736±73 a 202± 10 a

a Values in each row with the same letter are not significantly different atp< 0.05

shaded (Fig. 6c). Both the concentration of sugar in the rhizomes, and %C in the leaves didnot change during shading (Table 3). Growth rates ofH. pinifolia were significantly reducedduring light deprivation with growth rates per shoot being reduced by 50% in response tolight deprivation (Table 3). Due to low shoot densities in the light deprived treatment, growthrates per m−2 were reduced by over 70% when compared to control values.

4. Discussion

Light monitoring at the deep edge of the seagrass distribution has established that onaverage,H. pinifolia required greater than 14% of surface irradiance (SI) to survive. This


Fig. 6. Physiological response ofHalodule pinifoliato 78 days of light deprivation. (a) changes in leaf amino acidsconcentrations, (b) changes in chlorophyll a to b ratio, (c) changes in the leaf carbon isotope ratio (13C).

study was conducted in the ‘dry’ season, a period when surface light and water clarity islikely to be greatest (Hillman and Raaymakers, 1996) (Fig. 3). Consequently, the averageminimum light requirements ofH. pinifolia may be considerably less than 14% SI duringthe monsoon season when cloud cover and rainfall is greatest. Nevertheless, the minimumquantity of light measured (14% SI) during the monitoring period is significantly less thanthat recorded for otherHalodule species. For example, Kenworthy and Fonseca (1996)estimatedHalodule wrightii’s minimum light requirements to be between 24% and 37%of SI, while Dunton (1994) estimated a minimum requirement of 18% of SI. Integratedlight monitoring indicates thatH. pinifolia experiences an extremely variable light climate(periods of high light and no light) and an average light availability well below that recordedfor otherHalodulespp.

Results from the light deprivation experiment indicate thatH. pinifolia is not only ableto survive in an environment with a low average light availability, but is also able to survivefor an extended period of time in near darkness. In contrast, other seagrasses have exhibited


a rapid loss of biomass during the first month of severe light reduction. For example, leafdensities ofHeterozostera tasmanica(Bulthuis, 1983a) andPosidonia sinuosa(Gordon etal., 1994) declined by 70% during the first month of exposure to 2 and 1% of ambient light,respectively. The resilience ofH. pinifolia to long periods of light deprivation is likely tobe of paramount importance to the long-term survival of this species in the South-East Gulfof Carpentaria. This region of Australia periodically receives monsoonal rains that resultin highly turbid flood-waters covering over the seagrass beds (Hillman and Raaymakers,1996). Consequently seagrasses in the region are likely to experience long periods of lightdeprivation during the monsoon season.

In contrast to the long survival time ofH. pinifolia, H. ovalisdisplayed a low tolerance tolight deprivation, with complete plant death occurring after 38 days in the dark. A similarintolerance to light deprivation has also been demonstrated for monospecificH. ovalisplantsgrowing in sub-tropical waters (Longstaff et al., 1999). In this study complete plant deathwas estimated to occur after 30 days of light deprivation. AsH. ovalis displays limitedtolerance to light deprivation, the long-term survival strategy of this species in this regionmay be based on it ability to rapidly regrow from seed and/or vegetative fragments afterlight deprivation. This long-term survival strategy ofHalophilaspecies to perturbations hasalso been suggested to occur elsewhere (Kenworthy, 1992).

Most previous research has concentrated on assessing the impact of more moderatelight reductions on seagrasses (Backman and Barilotti, 1976; Dennison and Alberte, 1982;Bulthuis, 1983a). Some recent shading studies indicate that the period of time a seagrasscan survive below the minimum light requirement may be increased by photoadaptiveresponses such as increased chlorophyll content, changes in the chlorophyll a to b ratio,increased canopy height and shoot thinning (Abal et al., 1994; Czerny and Dunton, 1995;Van Lent et al., 1995; Lee and Dunton, 1997). In the present study,H. pinifolia was alsonoted to photoadapt, with an increased chlorophyll content, decreased chlorophyll a to bratio and an increased canopy height being recorded. However, because the species receivedvirtually no light, these responses would have had little positive effect on photosyntheticrates. In fact, the energetic cost of producing and maintaining more pigments and longershoots, with little net return, may have had a negative impact on the long-term survival.

Several parameters were responsive to both the natural light gradient and the light depriva-tion; chlorophyll a to b ratio, leaf amino acid concentration and leafd13C value. Decreasingchlorophyll a/b with depth has been observed in a number of seagrass species includingZostera marina(Dennison and Alberte, 1985),H. ovalis(Longstaff et al., 1999),Halophilaspp.,Halodulespp.,Syringodium filiforma, Thalassia testudinum(Wigington and McMil-lan, 1979; Lee and Dunton, 1997). A decrease in the chlorophyll a/b has been considered anadaptive response that increases the light absorption efficiency of the seagrass (Abal, 1996;Lee and Dunton, 1997).

Amino acid concentrations in seagrasses are responsive to a number of environmentalvariables: salinity stress increased proline concentrations in four subtropical seagrass species(Pulrich, 1986) and water depth was shown to affect amino acid concentrations inPosidoniaoceanica(Pirc, 1984) but notThalassodendron ciliatum(Parnik et al., 1992). Ambientsediment nutrient concentration and sediment nutrient addition can also have a significanteffect on amino acid concentrations (Udy and Dennison, 1997a, b). The elevated amino acidcontent at depth and in response to light deprivation in the present study could be related


to the balance of nutrient versus light limitation of seagrass growth, with the pronouncedlight limitation leading to high amino acid concentrations.

The carbon isotope ratio (d13C) of H. pinifolia leaves became more negative duringshading and in response to increased water depth. Thed13C signature of seagrasses is knownto be affected by a broad range of environmental conditions including light availability(Abal, 1996; Grice et al., 1996; Longstaff et al., 1999), water motion (Abal and Dennison,in press; France and Holmquist, 1997), water temperature and the source of the dissolvedinorganic carbon pool (DIC) (Cooper and Deniro, 1989; Hemminga et al., 1994). In thepresent study it is unlikely that water temperature and DIC source caused the decline ind13C with depth as the sites were situated relatively close together. Similarly, the poorcorrelation between shoot density andd13C suggests that water motion is not causing thechange ind13C with depth (Abal and Dennison, in press). Decreasingd13C with depth andin response to shading may be due to a reduction in the uptake of13C in relation to12C.The preferential uptake of12C over13C occurs because less energy has to be expended inthe uptake of12C in comparison to13C (Abal and Dennison in press; Grice et al. 1996;Longstaff et al., 1999).

In the present study some seagrass parameters such as shoot density and biomass did notshow a relationship with depth. For example, highest (Site 4) and lowest (Site 5) biomassand shoot densities was recorded at the two deep sites. These differences indicate that otherenvironmental factors (apart from light) are influencing the physiology and the morphologyof the seagrass. Other environmental influences known to affect seagrasses that may alsoexplain the difference in Sites 4 and 5 seagrass include nutrient availability (Short, 1987; Udyand Dennison, 1997a) and sediment characteristics (grain size, composition, compaction). Itinteresting to note that the sediment characteristic at Site 4 (coarse sand) were considerablydifferent to Site 5 (mud). Thus (a) the high root and rhizome biomass and (b) the low aminoacid and chlorophyll content at Site 4 in comparison to Site 5 may be the result of nutrientlimitation within the sediment at that site.

By assessing a range of seagrass physiological and morphological responses to lightreduction it may be possible to predict impending seagrass loss during light reduction events.Such predictive capacity would be invaluable in situations where the duration and extentof turbidity plumes can be controlled (e.g., during dredging operations). By investigatingthe responses ofH. pinifolia to natural light gradients and light deprivation, a suite ofsuitable parameters can be selected to indicate seagrass health. Changes in shoot density,blade width and chlorophyll content during shading have been identified as indicators ofThalassia testudinumstress during light reduction (Dunton, 1994).

Morphological responses have traditionally been used to indicate a detrimental impact onthe seagrass community has started (e.g.,Posidonia sinuosa, shoot density and leaf length)(Gordon et al., 1994). In the present study, the morphological responses observed were de-creases in biomass, shoot density and canopy height. Physiological responses, however, candetect declining seagrass health and impending seagrass die-off before substantial morpho-logical changes occur. Physiological responses of impendingH. pinifolia loss during lightdeprivation were identified these being; (1) increases in amino acid content, (2) decreasesin chlorophyll a/b ratios (3) decreases ind13C values (Fig. 7).

Although it is well recognised that seagrasses will exhibit morphological and physio-logical responses to light reduction, the type of response, the intensity of the response and


Fig. 7. Summary of the physiological and morphological changes inHalodule pinifoliaduring light deprivation.

the time required for a response to occur depends upon: (a) the species of seagrass e.g.,(Grice et al., 1996), (b) the intensity and duration of the light reduction (Bulthuis, 1983a;Gordon et al., 1994) and (c) the interaction of other environmental conditions such as watertemperature (Bulthuis, 1983b) and nutrient availability (Van Lent et al., 1995; Abal, 1996).Due to the complexity of biological and environmental factors that can influence seagrassesresponses to light reduction, it is necessary that early warning indicators be developed forthe specific seagrass community that may be affected.

Acknowledgements

We would like to thank the following people for their assistance in establishing andconducting this research; Mark Read and Hamish Malcome (Queensland Department ofEnvironment), Warren Lee Long (Queensland department of Primary Industries), CraigeWitt, Wayne Young and Alan Chartaris (WBM Oceanics), Mark McLennan and MarkO’Donohue (University of Queensland). Funding for this research was provided by thePorts Corporation of Queensland.

References

Abal, E.G., 1996. Light, nutrient and water quality interactions with the seagrass,Zostera capricorniAschers.PhD Thesis, Department of Botany, The University of Queensland, Brisbane, Australia.

Abal, E.G., Dennison, W.C., 1996. Seagrass depth range and water quality in Southern Moreton Bay, Queensland,Australia. Mar. Freshwater Res. 47, 763–771.

Abal, E.G., Dennison, W.C., in press. Stable isotope ratios, morphology and growth adaptations ofZosteracapricorni in response to in situ light reduction. J .Exp. Mar. Biol. Ecol.

Abal, E.G., Loneragan, N., Bowen, P., Perry, C.J., Udy, J.W., Dennison, W.C., 1994. Physiological andmorphological responses of the seagrassZostera capricorniAschers. to light intensity. J. Exp. Mar. Biol.Ecol. 178, 113–129.

Arnon, D.I., 1949. Copper enzymes in isolated chloroplast. Polyphenoloxidase inBeta vulgaris. Plant Physiology58, 1–15.

Backman, T.W., Barilotti, D.C., 1976. Irradiance reduction: effects on standing crop of the eelgrassZostera marina.Marine Biology 34, 33–40.

Bulthuis, D.A., 1983a. Effects of in situ light reduction on density and growth of the seagrassHeterozosteratasmanica(Martens ex Aschers.) den Hartog in Western Port, Victoria, Australia. J. Exp. Mar. Biol. Ecol 67,91–103.


Bulthuis, D.A., 1983b. Effects of temperature on the photosynthesis-irradiance curve of the Australian seagrass,Heterozostera tasmanica. Mar. Biol. Lett. 4, 47–57.

Cooper, L.W., Deniro, M.J., 1989. Stable carbon isotope variability in the seagrassPosidonia oceania: evidencefor light intensity effects. Mar. Ecol. Prog. Ser. 50, 225–230.

Czerny, A.B., Dunton, K.H., 1995. The effects of in situ light reduction on the growth of two subtropical seagrassesThalassia testudinumandHalodule wrightii. Estuaries 18, 418–427.

Dennison, W.C., 1987. Effects of light on seagrass photosynthesis, growth and depth distribution. Aquat. Bot. 27,15–26.

Dennison, W.C., 1990. Seagrasses: chlorophyll content. In: Phillips, R.C. (Ed.), Seagrass Research Methods,UNESCO, pp. 83–86.

Dennison, W.C., Alberte, R.S., 1982. Photosynthetic responses ofZostera marinaL. (Eelgrass) toin situmanipulation of light intensity. Oecologia 55, 137–144.

Dennison, W.C., Alberte, R.S., 1985. Role of daily light period in the depth distribution ofZostera marina(eelgrass). Mar. Ecol. Prog. Ser. 25, 51–62.

Dennison, W.C., Orth, K.A., Moore, R.J., Stevenson, J.C., Carter, V., Kollar, S., Batiuk, R.A., 1993. Assessingwater quality with submersed aquatic vegetation. BioScience 43, 86–94.

Duarte, C.M., 1991. Seagrass depth limits. Aquat. Bot. 40, 363–378.Dubois, M., Gilles, K.A., Hamilton, J.K., Rebers, P.A., Smith, F., 1956. Colorimetric method for determination of

sugars and related substances. Anal. Chem. 28, 350–356.Dunton, K.H., 1994. Seasonal growth and biomass of the subtropical seagrassHalodule wrightii in relation to

continuous measurements of underwater irradiance. Mar. Biol. 120, 479–489.Fonseca, M.S., Kenworthy, W.J., 1987. Effects of current on photosynthesis and distribution of seagrasses. Aquat.

Bot. 27, 59–78.France, R.L., Holmquist, J.G., 1997.d13C Variability of macroalgae: effects of water motion via baffling by

seagrasses and mangroves. Mar. Ecol. Prog. Ser. 149, 305–308.Gordon, D.M., Grey, K.A., Chase, S.C., Simpson, C.J., 1994. Changes to the structure and productivity of a

Posidonia sinuosameadow during and after imposed shading. Aquat. Bot. 47, 265–275.Grice, A.M., Loneragan, N.R., Dennison, W.C., 1996. Light intensity and the interactions between physiology,

morphology and stable isotope ratios in five species of seagrass. J. Exp. Mar. Biol. Ecol. 195, 91–110.Hemminga, M.A., Slim, F.J., Kazungu, J., Ganssen, G.M., Nieuwenhuize, J., Kruyt, N.M., 1994. Carbon outwelling

from a mangrove forest with adjacent seagrass beds and coral reef (Gazi Bay, Kenya). Mar. Ecol. Prog. Ser.106, 291–301.

Kenworthy, W.J., 1992. Protecting fish and wildlife habitat through a better understanding of the minimum lightrequirements of sub-tropical seagrasses in the south-eastern United States and Caribbean basin. PhD Thesis,North Carolina State University, Raleigh, North Carolina.

Kenworthy, W.J., Fonseca, M.S., 1996. Light requirements of seagrassesHalodule wrightii and Syringodiumfiliforme derived from the relationship between diffuse light attenuation and maximum depth distribution.Estuaries 19, 740–750.

Lanyon, J.M., Lumpus, C.J., Marsh, H., 1989. Dugong and turtles: grazers in the seagrass system. In Larkum,A.W.D., McComb, A J., Shepherd, S.A. (Eds.), Biology of Seagrasses: A Treatise on the Biology of Seagrasseswith Special Reference to the Australian Region, Elsevier, Amsterdam, pp. 610–633.

Lee, K., Dunton, K.H., 1997. Effects of in situ light reduction on the maintenance, growth and partitioning ofcarbon resources inThalassia testudinumBanks ex Konig. J. Exp. Mar. Biol. Ecol. 210, 53–73.

Longstaff, B.J., Loneragan, N.R., O’Donohue, M., Dennison, W.C., 1999. The effects of light deprivation on thesurvival and recovery of the seagrassHalophila ovalis, J. Exp. Mar. Biol. and Ecol. 234, 1–27.

Moore, K.A., Wetzel, R.L., Orth, R.J., 1997. Seasonal pulses of turbidity and their relations to eelgrass (ZosteramarinaL.) survival in an estuary. J. Exp. Mar. Biol. Ecol. 215, 115–134.

Parnik, T., Bil, K., Kolmakov, P., Titlyanov, E., 1992. Photosynthesis of the seagrassThalassodendron ciliatum:leaf anatomy and carbon metabolism. Photosynthetica 26, 213–223.

Peterson, B.J., Fry, B., 1987. Stable isotopes in ecosystem studies. Ann. Rev. Ecol. Syst. 18, 293–320.Pirc, H., 1984. Growth dynamics inPosidonia oceanica(L.) Delile 1. seasonal changes of soluble carbohydrates,

starch, free amino acids, nitrogen and organic anions in different parts of the plant P.S.Z.N.I. Mar. Ecol. 6,141–165.


Preen, A.R., Lee Long, W.J., Coles, R.G., 1995. Flood and cyclone related loss, and partial recovery, of more than1000 km2 of seagrass in Hervey Bay, Queensland, Australia. Aquat. Bot. 52, 3–17.

Pulrich, W.M., 1986. Variation in leaf soluble amino acid and ammonium content in subtropical seagrasses relatedto salinity stress. Plant Physiol. 80, 283–286.

Short, F.T., 1987. Effects of sediment nutrients on seagrasses: literature review and mesocosm experiment. Aquat.Bot. 27, 41–57.

Udy, J.W., Dennison, W.C., 1997a. Growth and physiological responses of three seagrass species to elevatedsediment nutrients in Moreton Bay, Australia. J. Exp. Mar. Biol. Ecol. 217, 253–277.

Udy, J.W., Dennison, W.C., 1997b. Physiological responses of seagrasses used to identify anthropogenic nutrientinputs. Mar. Freshwater Res. 48, 605–614.

Van Lent, F., Verchuure, J.M., Van Veghel, L.J., 1995. Comparative study on populations ofZostera marinaL.(eelgrass): in situ nitrogen enrichment and light manipulation. J. Exp. Mar. Biol. Ecol. 185, 55–76.

Wigington, J.R., McMillan, C., 1979. Chlorophyll composition under controlled light conditions as related to thedistribution of seagrasses in Texas and the U.S. Virgin Islands. Aquat. Bot 6, 171–184.

Zimmerman, R.C., Reguzzoni, J.L., Wyllie-Echeverria, S., Josselyn, M., Alberte, R.S., 1991. Assessment ofenvironmental suitability for growth ofZostera marinaL. (eelgrass) in San Francisco Bay. Aquat. Bot. 39,353–366.

Seagrass survival during pulsed turbidity events: the effects of light deprivation on the seagrasses...

Documents

Transcript of Seagrass survival during pulsed turbidity events: the effects of light deprivation on the seagrasses...