Estuarine, Coastal and Shelf Science 73 (2007) 551e562www.elsevier.com/locate/ecss

Patterns in tropical seagrass photosynthesis in relation tolight, depth and habitat

Stuart J. Campbell a,b,*, Len J. McKenzie a,b, Simon P. Kerville a,b, Juanita S. Bite c

a Northern Fisheries Centre, Queensland Fisheries Service, Department of Primary Industries and Fisheries, PO Box 5396,Cairns, Qld 4870, Australia

b CRC Reef Research Centre, PO Box 772, Townsville, Qld 4810, Australiac James Cook University, Townsville, Qld 4810, Australia

Received 22 April 2006; accepted 16 February 2007

Available online 27 April 2007

Abstract

Seagrass meadows across north-eastern Australia, survive a range of environmental conditions in coastal bays, reefs, estuarine and deepwaterhabitats through adaptation of a range of structural, morphological and physiological features. The aim of this study was to investigate the in-fluence of spatial features (habitat type, site and depth) and photon flux on the photosynthetic performance of 11 tropical seagrass species. Pulseamplitude modulated (PAM) fluorometry was used to generate rapid light curves from which measures of maximal electron transport rate(ETRmax), photosynthetic efficiency (a), saturating irradiance (Ek) and effective quantum yield (DF/Fm0) were derived. The amount of lightabsorbed by leaves (absorption factor) was also determined for each population. In intertidal habitats many seagrass species exhibited typicalsun-type responses with a close coupling of both ETRmax and Ek with photon flux. Photosynthetic performance ranged from minima in Thalas-sodendron ciliatum to maxima in Syringodium isoetifolium. The absence of a coupling between photosynthetic performance and photon flux insubtidal populations was most likely due to highly variable light climates and possible light attenuation, and hence the photo-biology of estuarineand deepwater seagrasses exhibited photosynthetic responses indicative of light limitation. In contrast seagrass species from shallow reef andcoastal habitats for the most part exhibited light saturation characteristics. Of all the variables examined ETRmax, Ek and DF/Fm0 were mostresponsive to changing light climates and provide reliable physiological indicators of real-time photosynthetic performance of tropical sea-grasses under different light conditions.� 2007 Elsevier Ltd. All rights reserved.

Keywords: fluorescence; photosynthesis; seagrass; photon flux; PAM; tropical; habitat

1. Introduction

The north-eastern region of Australia possesses a range ofmarine habitats including estuaries near the entrance of rivers,coastal embayments, calcareous reefs and deepwater habitats(Carruthers et al., 2001). Seagrass meadows are a dominantstructural component of these ecosystems, subject to a rangeof environmental conditions along gradients of photon flux

* Corresponding author. Present address: Wildlife Conservation Society,

Marine Programs, Jalan Pangrango 8, PO Box 16151, West Java, Bogor,

Indonesia.

E-mail address: scampbell@wcs.org (S.J. Campbell).

0272-7714/$ - see front matter � 2007 Elsevier Ltd. All rights reserved.

doi:10.1016/j.ecss.2007.02.014

associated with tidal movement, distance from riverine sys-tems, depth gradients and seasonal turbidity events influencedby terrigenous runoff.

Light availability is often the most important factor control-ling seagrass productivity, distribution and survival (Longstaffet al., 1999; Carruthers et al., 2002; Biber et al., 2005), yetother factors such as nutrient availability and physical distur-bance from terrigenous runoff also influence seagrass survival.Fluctuations in seasonal turbidity and light availability due topulsed river flow inputs and wind driven re-suspension imposestrong selective pressures on seagrasses, which undergo eco-physiological acclimation to cope with changing light climates(Waycott et al., 2005). Physiological traits may vary with

552 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

species, location and habitat type and determine seagrass resis-tance to limiting conditions, while many other factors (e.g., re-cruitment, growth rate and sediment chemistry) influence theresilience of a meadow following disturbance.

Adaptation of seagrasses to fluctuating light climates in-volves the acclimation of a number of photosynthetic character-istics that can improve their resilience, by supporting growth andreducing susceptibility to limiting conditions. These physiolog-ical traits respond to dynamic changes in external irradiance byphoto-adaptive (i.e., pigment ratios, saturating light irradiancesand photosynthetic efficiencies) and photo-protective re-sponses. The capacity of seagrasses to photo-adapt and regulatetheir photosynthetic performance (e.g., low saturating irradi-ance, Ek and high photosynthetic efficiencies, a) to changinglight climates has been demonstrated along depth profiles(Ralph et al., 1998; Schwarz and Hellblom, 2002; Silva and San-tos, 2003) and turbidity gradients (Campbell et al., 2003) usingchlorophyll fluorescence techniques. These techniques can beused to examine the dynamic behaviour of seagrass photosyn-thesis under fluctuating light regimes as the plant attempts toreach maximal electron transport rates to achieve optimal pho-tosynthesis. Electron transport rates are derived from fluores-cence yields, the incident photosynthetic photon flux density(PPFD) and the proportion of PPFD absorbed by leaves (Beeret al., 2001). Although leaf absorption factor values have beenshown to differ considerably within species, both within leaf(e.g., Thalassia testudinum: Enriquez et al., 2002), betweenleaves of different age (e.g., T. testudinum: Durako and Kunzel-man, 2002), and with depth (e.g., Halophila stipulacea: Schwarzand Hellblom, 2002; Zostera noltii: Silva and Santos, 2003),there are limited studies examining spatial and inter-species var-iability in this parameter (Ralph et al., 1998).

With the development of PAM fluorometry it is possible torapidly measure real-time changes in the photosynthetic activ-ity of seagrasses in response to diurnal and depth-related fluc-tuations in PPFD (Ralph et al., 1998; Schwarz and Hellblom,2002; Campbell et al., 2003; Runcie and Durako, 2004) andspecies related effects (Major and Dunton, 2002; Campbellet al., 2003; Durako et al., 2003; Silva and Santos, 2003).Maximal rates of electron transport, or photosynthetic rates,are achieved during midday and are generally 1.5- to 5-foldhigher than rates measured in the morning and afternoon(Ralph et al., 1998; Campbell et al., 2003; Silva and Santos,2003). Photosynthetic performance in response to diurnal,depth and turbidity related changes in PPFD can vary withshort-term (e.g., daily and tidal) and long-term (e.g., seasonal)time scales as a function of light attenuation resulting fromsemi-diurnal tidal movements, turbidity and chlorophyll con-centrations. Intraspecific differences in seagrass photosyn-thetic performance using PAM fluorometry have beendescribed previously for some temperate and tropical seagrassspecies (Beer et al., 1998; Major and Dunton, 2002; Campbellet al., 2003; Durako et al., 2003; Silva and Santos, 2003) yetfew studies have compared photosynthetic features withinmulti-species stands of seagrasses from different habitat types.

In north-east Australia four major habitat types (estuarine,coastal, reef and deepwater) have been described which

encompass the range of ecological functions and controllingfactors (e.g., low light, low nutrients, physical disturbanceand terrigenous runoff) within seagrass ecosystems (Car-ruthers et al., 2001). These habitats provide a basis to investi-gate processes that control seagrass physiology. In this paperwe characterise the photosynthetic performance of multi-species stands of tropical seagrasses at meadow (site) andecosystem (habitat) spatial scales at which disturbances to sea-grass populations often occur. We also examine relationshipsbetween photosynthetic variables and abiotic variables of pho-ton flux and depth, to elucidate general relationships betweenseagrass physiology and these factors.

2. Methods

We measured the photosynthetic performance of seagrassesin the four major habitat types (estuarine, coastal, reef anddeepwater) in which processes that control seagrass productiv-ity have been defined (Carruthers et al., 2001). We chose six lo-cations (Hervey Bay [Burrum Heads and Urangan], MourilyanHarbour, Cairns Harbour, Green Island, Lizard Island and Or-man Reef (Torres Strait)), in tropical Queensland (Fig. 1),each representing at least one of the four habitat types describedby Carruthers et al. (2001). At each of the six locations andwithin each of the four potential habitat types present, one totwo sites were examined to measure the photosynthetic perfor-mance of those seagrass species present between November2003 and March 2004. Species selected for measurementincluded all intertidal species found at each location and thedominant subtidal species found between 1 and 20 m.

2.1. Photosynthetic photon flux density

Photosynthetic photon flux density (PPFD) (mmol photo-ns m�2 s�1) was measured using the optical light sensor ofthe PAM fluorometer (Waltz, Germany) calibrated with a Li-Cor (USA) quantum sensor. Measures of PPFD were madeat the start, and end of each set of rapid light curves. Fora given depth there was wide variation in PPFD among loca-tions due to differences in water clarity (e.g., suspended mat-ter) and turbidity in different locations. The variation in PPFDat a given site and depth was generally low, although somevariability at a given depth (e.g., at Green Island) was due tofluctuating light levels (turbid water and some cloud cover)during sampling between 11:00 and 13:00 h.

2.2. Light adapted rapid light curves (RLCs)

At each site, measures of rapid light curves were made onthe midpoint of 10 replicate leaves from separate plants foreach species between 11:00 and 13:00 h during sunnyconditions, and are thus likely to represent the maximal pho-tosynthetic electron transport rates (ETRmax). RLCs were gen-erated automatically with a diving PAM using an incrementalsequence of actinic illumination periods, with light intensitiesincreasing in nine steps from 0 to 2400 mmol photons m�2 s�1

PPFD. Each illumination period lasted 10 s, at the end of

553S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

Fig. 1. Survey locations in Queensland, Australia.

which time, F, and following a saturating pulse of white light(800 ms of 8000 mmol photons m�2 s�1 PPFD), Fm0, wasmeasured.

Photosynthetic electron transport rates were calculated as theproduct of effective quantum yield (FPSII¼ F� Fm0/Fm0 ¼DF/Fm0; where F is initial fluorescence, Fm0 is maximum fluores-cence and DF is variable fluorescence), the incubation irradiance(I ) and the fraction of light absorbed by the leaf, the absorbancefactor (AF). This value was multiplied by 0.5, as it is assumedthat half the photons required for the movement of electronsalong the photosystem pathways are absorbed by PSII (Schreiberet al., 1995). Effective quantum yields (DF/Fm0) presented in thisstudy are the first quantum yield of each rapid light curve(PPFD¼ 0 mmol photons m�2 s�1) measured before applicationof the increasing irradiances and provide a measure of light adap-ted quantum yield (Saroussi and Beer, 2006). AF values for allspecies were derived by measuring the proportion of light ab-sorbed by single leaves according to the method described byBeer et al. (2001). The maximal rate of ETR (ETRmax) anda were calculated by fitting the RLC data to an exponential func-tion; ETR¼ ETRmax(1� exp[�a(I )/ETRmax]) modified fromJassby and Platt (1976); where ETR is electron transport rateand I is irradiance. The onset of light saturation (Ek) was calcu-lated as ETRmax/a where photo-inhibition was detected in sea-grass photosynthesis maximal irradiances were not included

when fitting RLC data to the exponential function to deriveETRmax and a.

2.3. Data analysis

To evaluate the effect of photosynthetic photon flux density(PPFD) on photosynthetic variables among intertidal and subti-dal seagrasses, regression analysis was used to test for relation-ships between mean species photosynthetic variables (ETRmax,a, Ek and DF/Fm0 and absorption factor) and mean in situ PPFD,separately for all intertidal sites and all subtidal sites. Intertidalsaturating irradiance (Ek) was loge transformed prior to analysisto meet assumptions of normality (Systat Version 10.2).

For all data pooled, separate plots of mean photosyntheticvariables (ETRmax, a, Ek and DF/Fm0 and absorption factor)against photosynthetic photon flux density (mmol photo-ns m�2 s�1) and depth (m) were made. To evaluate possiblecovarying effects of PFD and depth (covariate) on photosyn-thetic variables (ETRmax, a, Ek, DF/Fm0 and absorption factor),for all species and sites pooled, stepwise regression analysiswas also used. ETRmax, was loge transformed, saturating irra-diance (Ek) was square-root transformed and effective quan-tum yield was arcsine square-root transformed prior toanalysis to meet assumptions of normality (Systat Version10.2). To evaluate if seagrass species at different depths

554 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

(0e1 m, 1e3 m, 3e7 m and 7e20 m) were light limited orlight saturated we plotted Ek against incident PPFD (mmolphotons m�2 s�1) for each depth category.

Nested ANOVA was used to test for differences among sea-grass population site means of the four photosynthetic vari-ables (ETRmax, a and Ek, DF/Fm0) (n¼ 2e8) within habitats(estuary, coastal, reef and deepwater) (n¼ 4). Factors werehabitat type (random; 4 levels, estuary, coastal, reef and deep-water), site nested in habitat (random; 2e3 levels of siteper habitat). ETRmax and Ek data were loge transformed andDF/Fm0 data were arcsine square-root transformed prior toanalysis to meet assumptions of normality.

PCA was performed using Statistica (v. 6.0) to examine ifthe seagrass populations were grouped according to habitattype (estuary, coastal, reef and deepwater) based on the fourphotosynthetic variables (ETRmax, a, Ek and DF/Fm0). Incidentlight (PPFD mmol photons m�2 s�1) and depth were entered asindependent factors to evaluate their influence on possiblehabitat groupings.

3. Results

3.1. Site characteristics

Sediment and habitat characteristics of all locations areshown in Table 1. There was a negative relationship betweendepth and photosynthetic photon flux density (PPFD) (Fig. 2).At depths shallower than 3 m PPFD ranged from 128 to1250 mmol photons m�2 s�1. Low PPFD values (<200 mmolphotons m�2 s�1) were recorded in turbid waters of CairnsHarbour and Mourilyan Harbour, intermediate values (>200to 500 mmol photons m�2 s�1) were recorded in MourilyanHarbour and Orman Reef and high values (>650 mmol photo-ns m�2 s�1) were recorded at all other locations (Table 2). Atdepths greater than 5 m the PPFD ranged from 33 to 93 mmolphotons m�2 s�1 (Table 3).

3.2. Photosynthetic variables: comparison amongspecies and relationships between photosyntheticvariables and PPFD

The photosynthetic characteristics of each species testedfrom each location and depth are shown for intertidal speciesin Table 2 and for subtidal species in Table 3. Higher maximalelectron transport rates (ETRmax), higher saturating irradiancesand lower quantum yields were generally found for intertidalcompared with subtidal species (Fig. 3).

3.2.1. IntertidalFor intertidal habitats there was a significant positive rela-

tionship (F1,7¼ 22.7, P¼ 0.002, r2¼ 0.76) between meanETRmax (all species) and photosynthetic photon flux density(PPFD) (Fig. 3a). The positive relationship was due to rela-tively higher ETRmax rates (>100 mmol e�m�2 s�1) in Cymo-docea spp., Halodule uninervis, Thalassia hemprichiiand Syringodium isoetifolium occurring at photon fluxes>600 mmol photons m�2 s�1) (Fig. 3a) compared with Enha-lus acoroides, Halophila ovalis, Zostera capricorni and Tha-lassodendron ciliatum which had ETRmax rates <100 mmole�m�2 s�1 at <600 mmol photons m�2 s�1. There was nosignificant relationship (F1,8¼ 1.83, P¼ 0.218, r2¼ 0.21)between mean a and PPFD, (Fig. 3b) but a positive relation-ship between saturating irradiance (Ek) and photon flux(F1,8¼ 7.36, P¼ 0.030, r2¼ 0.43) was found (Fig. 3c). Norelationships were found between PPFD and mean effectivequantum yield (DF/Fm0) F1,8¼ 4.64, P¼ 0.068, r2¼ 0.40) orabsorbance factor (AF) (F1,8¼ 3.09, P¼ 0.122, r2¼ 0.31)(Fig. 3d and e).

3.2.2. SubtidalNo significant relationship was evident between ETRmax

and PPFD (F1,8¼ 0.992, P¼ 0.348, r2¼ 0.11) among subti-dal species (Fig. 3f). Subtidal species generally had ETRmax

rates less than 100 mmol e�m�2 s�1, and were restricted tomean PPFD’s generally less than 250 mmol photons m�2 s�1.Species at 2e3 m depth generally had higher ETRmax rates

0

200

400

600

800

1000

1200

1400

0 5 10 15 20 25Depth (m)

Phot

on fl

ux d

ensi

ty(μ

mol

pho

tons

m-2

s-1

)

Fig. 2. Photosynthetic photon flux density (mmol photons m�2 s�1) against

depth (m) at each location: Green Island (open diamonds), Orman Reef (closed

diamonds), Hervey Bay, (open squares), Cairns Harbour (closed squares),

Mourilyan Harbour, (open triangles), Lizard Island (closed triangles).

Table 1

Description of each location by ecological niche, substrate and habitat type

Location Ecological niche Substrate Habitat type

Hervey Bay Mid intertidaledeep subtidal Mudesand Coastal/deepwater

Mourilyan Harbour Mid intertidal Sand Estuary

Cairns Harbour Mid intertidal Mud Estuary

Green Island Upper intertidaledeep subtidal Calcareous sand Reef/deepwater

Lizard Island Mid intertidaledeep subtidal Calcareous sand Reef/deepwater

Orman Reef Low intertidaleshallow subtidal Calcareous sand Reef

555S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

Table 2

Intertidal seagrasses. Mean (�SE) effective quantum yield, ETRmax, photosynthetic efficiency (a), saturating irradiance (Ek) (n¼ 10) and fraction of incident light

absorbed by a leaf (AF) (n¼ 4e5). Location, site code, depth (m) and in situ photosynthetic photon flux density (PPFD) (mmol photon m�2 s�1) for each seagrass

are presented

Species location,

site code

Depth

(m)

PPFD Quantum yield ETRmax a Ek AF

Halophila ovalis

Hervey Bay: Urangan UG1 0 720 0.50 (0.001) 125.6 (47.4) 0.24 (0.09) 537.8 (56.7) 0.61

Hervey Bay: Burrum Heads BH1 0 659 0.46 (0.02) 107.2 (7.2) 0.18 (0.01) 597.3 (31.0) 0.56

Mourilyan Harbour C14 2 333 0.77 (0.01) 49.4 (4.5) 0.27 (0.004) 180.5 (16.3) 0.48

Mourilyan Harbour C8 2 333 0.69 (0.009) 44.7 (3.9) 0.21 (0.005) 213.9 (20.3) 0.42

Cairns Harbour RB1 2 128 0.77 (0.004) 54.9 (1.8) 0.34 (0.005) 158.9 (5.2) 0.68

Cairns Harbour EP1 2 189 0.70 (0.02) 56.5 (2.4) 0.29 (0.01) 193.1 (6.8) 0.56

Green Is. GI1 0 798 0.53 (0.02) 137.9 (6.5) 0.20 (0.01) 680.5 (36.3) 0.56

Lizard Is. LI1 1 798 0.55 (0.02) 75.4 (3.4) 0.12 (0.005) 607.3 (85.4) 0.45

Lizard Is. LI4 1 865 0.58 (0.01) 112.07 (4.7) 0.12 (0.002) 947.0 (53.2) 0.34

Zostera capricorniHervey Bay: Burrum Heads BH1 0 659 0.54 (0.04) 133.1 (16.9) 0.20 (0.01) 666.5 (8.5) 0.56

Hervey Bay: Urangan UG1 0 720 0.45 (0.03) 96.22 (5.4) 0.22 (0.013) 441.4 (30.4) 0.58

Mourilyan Harbour LB1 0 259 0.73 (0.02) 39.3 (3.6) 0.18 (0.009) 218.9 (16.2) 0.59

Mourilyan Harbour BS1 0 293 0.76 (0.01) 61.8 (4.5) 0.27 (0.01) 236.8 (24.0) 0.59

Cairns Harbour EP1 2 189 0.73 (0.01) 63.6 (2.3) 0.31 (0.003) 205.1 (8.9) 0.66

Cairns Harbour RB1 2 128 0.74 (0.01) 61.3 (4.8) 0.37 (0.008) 166.1 (12.3) 0.62

Halodule uninervisGreen Is. GI1 0 998 0.66 (0.01) 183.3 (8.9) 0.34 (0.01) 548.3 (37.9) 0.70

Lizard Is. LI1 1 865 0.57 (0.01) 99.2 (3.04) 0.17 (0.003) 601.00 (27.5) 0.40

Cymodocea rotundataGreen Is. GI1 0 824 0.64 (0.03) 149.4 (9.1) 0.38 (0.02) 407.1 (39.8) 0.72

Cymodocea serrulata

Green Is. GI1 0 971 0.67 (0.02) 171.9 (8.4) 0.42 (0.01) 415.5 (33.9) 0.79

Orman Reef MB1 2 557 0.66 (0.02) 68.7 (6.4) 0.29 (0.01) 243.66 (26.3) 0.56

Enhalus acoroides

Orman Reef MB1 2 557 0.66 (0.02) 103.9 (10.9) 0.30 (0.01) 365.5 (52.7) 0.71

Thalassodendron ciliatum

Orman Reef MB1 2 176 0.74 (0.01) 46.84 (2.2) 0.28 (0.01) 169.6 (13.6) 0.58

Thalassia hemprichiiGreen Is. GI1 0 958 0.64 (0.02) 157.1 (11.3) 0.41 (0.01) 389.2 (38.4) 0.78

Orman Reef MB1 1 1143 0.39 (0.09) 112.2 (5.9) 0.37 (0.01) 307.5 (19.3) 0.72

Syringodium isoetifoliumGreen Is. GI1 0 1250 0.65 (0.02) 261.3 (15.1) 0.32 (0.01) 831.1 (62.8) 0.73

Orman Reef MB1 2 559 0.75 (0.01) 68.0 (3.6) 0.27 (0.01) 248.4 (13.8) 0.57

than those growing at depths of 5 m or deeper (Table 3,Fig. 3f).

The negative relationship (F1,8¼ 5.48, P¼ 0.047,r2¼ 0.41) between mean a and PPFD was due to high a indeepwater (10e20 m) species at low light climates, a rangeof low and high values among species at 3e7 m, with the low-est value recorded for Halodule uninervis (Table 3, Fig. 3g).Significant positive relationships between Ek and PPFD(F1,8¼ 10.88, P¼ 0.011, r2¼ 0.56) were due to higher Ek

values of H. uninervis and Halophila ovalis at 5 m comparedwith other seagrass species at depths greater than 5 m(Fig. 3h). Deepwater seagrasses growing at 10e20 m hadthe lowest Ek values (Fig. 3h).

No relationships were found between PPFD and mean ef-fective quantum yield (DF/Fm0) (F1,8¼ 2.84, P¼ 0.191,r2¼ 0.26) or absorbance factor (AF) (F1,8¼ 3.09, P¼ 0.343,r2¼ 0.04) (Fig. 3i and j).

3.3. Light saturation versus incident PPFD

Mean saturating irradiances (Ek) of seagrasses (pooled) atintertidal and shallow subtidal sites (0e1 m and 1e3 m),were mostly less than PPFD (mmol photons m�2 s�1) indicat-ing light saturation (Fig. 4). In contrast mean saturating irradi-ances (Ek) of seagrasses (pooled) at mid to deepwater subtidalsites (3e7 m and 7e20 m) were mostly greater than incidentphoton flux density indicating light limitation (Fig. 4).

3.4. Relationships among photosynthetic variables,PPFD and depth

A significant positive effect (P< 0.05) of increasing PPFDand decreasing depth on ETRmax and saturating irradiance (Ek)across all species and sites pooled was found (Table 4, Figs. 5and 6). Effective quantum yield had positive relationships with

556 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

Table 3

Subtidal seagrasses. Mean (�SE) effective quantum yield, ETRmax, photosynthetic efficiency (a), saturating irradiance (Ek) (n¼ 10) and fraction of incident light

absorbed by a leaf (AF) (n¼ 4e5). Location, site code, depth (m) and in situ photosynthetic photon flux density (PPFD) (mmol photon m�2 s�1) for each seagrass

are presented

Species location,

site code

Depth

(m)

PPFD Quantum yield ETRmax a Ek AF

Halophila ovalis

Hervey Bay: Burrum Heads HB21 5 80 0.71 (0.012) 74.7 (5.0) 0.33 (0.009) 227.9 (16.4) 0.55

Hervey Bay: Burrum Heads HB25 5 253 0.75 (0.009) 31.2 (2.6) 0.26 (0.01) 119.6 (10.8) 0.45

Hervey Bay: Burrum Heads HB4 10 40 0.79 (0.005) 49.1 (3.9) 0.35 (0.005) 140.6 (11.7) 0.52

Hervey Bay: Burrum Heads HB5 10 40 0.76 (0.005) 20.8 (1.5) 0.25 (0.01) 83.96 (6.2) 0.55

Green Is. GI2 5 257 0.61 (0.008) 143.2 (7.6) 0.29 (0.01) 506.4 (35.4) 0.64

Green Is. GI3 10 86 0.70 (0.007) 136.2 (3.3) 0.34 (0.01) 399.2 (12.6) 0.64

Lizard Is. LI2 5 306 0.50 (0.017) 105.0 (6.4) 0.17 (0.01) 630.8 (66.1) 0.49

Lizard Is. LI5 5 306 0.57 (0.036) 85.3 (5.7) 0.22 (0.02) 400.1 (25.3) 0.50

Lizard Is. LI3 20 33 0.72 (0.018) 41.9 (4.2) 0.27 (0.01) 156.3 (17.4) 0.43

Lizard Is. LI6 20 33 0.75 (0.009) 49.0 (3.4) 0.27 (0.01) 178.6 (11.9) 0.45

Orman Reef MB1 3.5 97 0.66 (0.008) 71.6 (5.1) 0.35 (0.01) 208.3 (16.0) 0.64

Orman Reef TN1 7 80 0.75 (0.008) 87.4 (10.1) 0.29 (0.01) 304.0 (41.0) 0.52

Halophila decipiensOrman Reef TN1 7 93 0.59 (0.046) 58.5 (3.8) 0.22 (0.03) 294.9 (44.8) 0.53

Halophila spinulosa

Hervey Bay: Burrum Heads HB21 5 80 0.70 (0.018) 73.1 (4.10) 0.41 (0.02) 182.7 (15.0) 0.56

Hervey Bay: Burrum Heads HB25 5 253 0.73 (0.008) 19.7 (1.03) 0.20 (0.01) 98.1 (3.4) 0.45

Hervey Bay: Burrum Heads HB4 10 40 0.73 (0.005) 14.8 (0.52) 0.23 (0.006) 65.3 (3.2) 0.53

Hervey Bay: Burrum Heads HB5 10 40 0.75 (0.005) 63.9 (3.43) 0.29 (0.009) 222.2 (14.6) 0.53

Orman Reef TN1 7 66 0.67 (0.027) 68.0 (4.54) 0.26 (0.016) 267.3 (18.4) 0.63

Halodule uninervis

Cairns BP1 3 140 0.73 (0.018) 12.9 (1.08) 0.07 (0.003) 191.2 (23.7) 0.46

Lizard Is LI2 5 306 0.62 (0.018) 119.8 (8.2) 0.20 (0.02) 619.5 (110.9) 0.66

Cymodocea serrulata

Orman Reef MB1 5 138 0.70 (0.008) 47.4 (2.54) 0.35 (0.02) 145.1 (16.6) 0.73

Orman Reef TN1 7 86 0.73 (0.016) 66.5 (2.86) 0.26 (0.004) 255.1 (11.4) 0.68

Thalassodendron ciliatum

Orman Reef MB1 5 126 0.65 (0.01) 42.6 (2.54) 0.20 (0.02) 221.6 (21.3) 0.72

Syringodium isoetifoliumOrman Reef MB1 3.5 109 0.67 (0.02) 103.2 (5.6) 0.35 (0.01) 298.1 (19.0) 0.75

Orman Reef TN1 7 73 0.82 (0.01) 101.8 (4.4) 0.29 (0.003) 346.9 (16.5) 0.62

decreasing PPFD and increasing depth (Figs. 5 and 6) but thiswas significant only with PPFD. Absorbance factor showeda significant negative relationship with depth only (Table 4,Fig. 6). No effect of PPFD or depth on photosynthetic effi-ciency (a) was found.

3.5. Effects of site and habitat on photosyntheticvariables

Photosynthetic variable means (ETRmax, a, Ek and DF/Fm0)significantly differed among habitat types (all P val-ues¼ 0.001) (Table 5). Mean ETRmax in both of the reefs sitesand one coastal site were significantly higher than both estua-rine sites and two of the three deepwater sites, while onecoastal and one reef site were site were significantly higherthan both estuarine and two deepwater sites (Fig. 7). The op-posite trend was found for DF/Fm0 with higher values in thetwo estuarine and two deepwater sites than three of the fourcoastal and reef sites. Differences among a means were dueto higher values at one reef site and lower values at 1 coastalsite than all other sites.

Significant differences among sites (nested within habitattypes) were found for ETRmax (F3,5¼ 4.281, P¼ 0.003) andEk (F3,5¼ 1.531, P¼ 0.001) (Table 5) although they explainedless of the variation than habitat alone. For ETRmax and Ek

these differences were due to higher ETRmax and Ek at GreenIsland compared with Orman Reef (reef habitats) and higherETRmax and Ek at Orman Reef compared with Hervey Bayand Lizard Island in deepwater habitats (Fig. 7).

PCA revealed some separation of habitat types (estuary,coastal, reef and deepwater) based on the four photosyntheticvariables (ETRmax, a, Ek and DF/Fm0) and habitat features(depth, PPFD) (Fig. 8). Around 76.82% of the variation wasexplained by two axes (factors 1 and 2) of the PCA. For themost part estuary and deepwater populations were moreclosely associated with each other, although 5 (four coastal,one reef) of the 28 coastal and reef sites were grouped amongestuary and deepwater sites. Estuary and deepwater sites wereinfluenced by depth and photosynthetic efficiencies (a and DF/Fm0). Coastal sites were separated as a distinct group exceptfor these four sites. Reef sites were more spread out; most siteswere associated with high ETRmax, high Ek and PPFD, three

557S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

R2 = 0.580

100200300400500600700800900

0100200300400500600700800900

TC

HUHOSI

HOHO

HS

HD

HSCS

h

R2 = 0.31

Abso

rban

ce fa

ctor

Abso

rban

ce fa

ctor

TH

TC HU

CRCS

EA

SIZC

HO

e

R2 = 0.04

TC

HU

CSSI

HO

HSHO

HD HO

HS

j

R2 = 0.40Qua

ntum

yie

ld (Δ

F /F

m')

Qua

ntum

yie

ld (Δ

F /F

m')

TH

TC

HUCR

CSEA SI

ZC HO

d

R2 = 0.43

E k (μ

mol

pho

tons

m-2

s-1

)

E k (μ

mol

pho

tons

m-2

s-1

)

TH

TC

HU

CR

CSEA

HOSI

ZC

c

R2 = 0.760

20406080

100120140160180200

0 200 400 600 800 1000 1200 1400Photon flux density (μmol photons-1 m-2 s-1) Photon flux density (μmol photons m-2 s-1)

Photon flux density (μmol photons m-2 s-1)Photon flux density (μmol photons m-2 s-1)

Photon flux density (μmol photons m-2 s-1) Photon flux density (μmol photons m-2 s-1)

Photon flux density (μmol photons m-2 s-1)Photon flux density (μmol photons m-2 s-1)

Photon flux density (μmol photons m-2 s-1)Photon flux density (μmol photons m-2 s-1)

ETR

max

(μm

ol e

-1 m

-2 s

-1)

ETR

max

(μm

ol e

-1 m

-2 s

-1)

HU

TC

EA

HOZC

THCS

SICR

a

R2 = 0.21

α (μ

mol

ele

ctro

ns/p

hoto

ns)

α (μ

mol

ele

ctro

ns/p

hoto

ns)

THTC

HU

CRCS

EASI

ZC HO

b

R2 = 0.110

20406080

100120140160180200

0 50 100 150 200 250 300 350 400

0 200 400 600 800 1000 1200 1400 0 50 100 150 200 250 300 350 400

0 200 400 600 800 1000 1200 1400 0 50 100 150 200 250 300 350 400

0 200 400 600 800 1000 1200 1400 0 50 100 150 200 250 300 350 400

0 200 400 600 800 1000 1200 1400 0 50 100 150 200 250 300 350 400

HOHU

HS

HD

SI

TCHS

HO

HO

CS

f

R2 = 0.260.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

0.3

0.4

0.5

0.6

0.7

0.8

0.9

1.0

TC

HUCSHS SI

HD

HO

HOHS

HO

i

R2 = 0.410.0

0.1

0.2

0.3

0.4

0.5

0.6

0.0

0.1

0.2

0.3

0.4

0.5

0.6

TC HU

CSSIHO

HS

HO

HD

HOHS

g

Fig. 3. Plots of relationships between the photosynthetic variables, ETRmax, photosynthetic efficiency (a), saturating irradiance (Ek), effective quantum yield (DF/

Fm0) and absorption factors against photosynthetic photon flux density (mmol photons m�2 s�1) for (aee) intertidal speceis (closed squares) and (fej) subtidal spe-

cies at 3e7 m (closed squares), subtidal Halophila ovalis and Halophila spinulosa at 10 m (open squares) and subtidal Halophila ovalis at 20 m (open circles).

Species codes are Cymodocea rotundata (CR), Cymodocea serrulata (CS), Enhalus acoroides (EA), Halodule uninervis (HU), Halophila ovalis (HO), Halophila

spinulosa (HS), Syringodium isoetifolium (SI) Thalassia hemprichii (TH), Thalassodendron ciliatum (TC) and Zostera capricorni (ZC).

558 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

sites were associated with a and DF/Fm0 and two sites had in-termediate characteristics (Fig. 8).

4. Discussion

This study has demonstrated an influence of habitat andphoton flux on photosynthetic performance of seagrasses,

0

200

400

600

800

1000

1200

1400

0 200 400 600 800 1000 1200 1400Photon flux density (μmol photons m-2 s-1)

Satu

ratin

g irr

adia

nce

(μm

ol p

hoto

ns m

-2 s

-1)

Fig. 4. Mean site saturating irradiance (Ek) against photosynthetic photon flux

density (mmol photons m�2 s�1) at each depth category for all seagrasses

pooled: 0e0.5 m depth (open squares), 1e2 m depth (open diamonds), 3e7 m depth, (closed squares), 10e20 m depth (closed circles). The solid line

represents a 1:1 ratio between Ek and photon flux density (mmol photo-

ns m�2 s�1). Seagrasses at sites above the line are light limited, while those

below the line are light saturated.

Table 4

Stepwise regression ANOVA of the effects of photon flux density (PFD) and

depth (m) on, ETRmax, (loge transformed) photosynthetic efficiency (a), satu-

rating irradiance (Ek) (square-root transformed) effective quantum yield (arc-

sine square-root transformed) and absorbance factor for all species from all

sites and depths

Regression factors df MS F P

ETRmax

PFD 1 2.885 14.98 0.001

Depth 8 0.488 2.53 0.024

Residual 41

Photosynthetic efficiency (a)

PFD 1 0.018 3.341 0.075

Depth 8 0.010 1.895 0.098

Residual 41

Saturating irradiance (Ek)

PFD 1 518.03 43.88 0.001

Depth 8 25.79 2.19 0.049

Residual 41

Quantum yield (DFv/Fm0)

PPFD 1 0.107 20.92 0.001

Depth 8 0.009 1.75 0.115

Residual 41

Absorbance factor

PFD 1 0.007 0.824 0.369

Depth 8 0.019 2.271 0.041

Residual 41

particularly at intertidal sites where photosynthesis was mostclosely coupled with light availability. For subtidal sites the re-sponse was less clear, although saturating irradiances amongspecies were coupled with changes in photon flux along depthgradients. Of all variables examined intertidal ETRmax andboth intertidal and subtidal Ek were most responsive tochanges in light associated with depth changes. These patternswere generally characterised by decreased ETRmax and Ek andan increase in DF/Fm0 with depth. For subtidal plants photo-synthetic efficiency (a) also increased with depth indicatingphoto-acclimation and an increased efficiency of these plantsto capture photons. In contrast absorbance factor was not re-sponsive to changes in light associated with depth gradientsand would not be a dependable measure of physiological re-sponse to changing photon flux. The positive relationship be-tween ETRmax and PPFD at shallow sites supports thegeneral relationship for seagrasses shown in previous studies(Ralph, 1996; Campbell et al., 2003; Silva and Santos, 2003;Lan et al., 2005). The twofold lower ETRmax and three- to six-fold lower Ek in estuarine and deepwater habitats is consistentwith our knowledge that light is a key factor that limits andthreatens seagrass distribution and survival in estuarine anddeepwater habitats in north-eastern Australia (Carrutherset al., 2002). The photosynthetic performance of seagrasseswithin many but not all reef habitats revealed that light was of-ten not limiting, possibly because nutrient supply is a majorlimiting factor in these environments (Udy et al., 1999).

The coupling of ETRmax and photon flux found amongsome speceis in the present study is consistent with that re-corded for a range of species (Beer et al., 1998; Ralph et al.,1998), yet this is the first report among species from multi-species stands at ecosystem scales, and few have shown thisto occur among stands of the same species growing in differentlight habitats (Schwarz and Hellblom, 2002). This relationshipwas strongest among intertidal seagrasses where physiologicaland growth responses to light climates are often shaped byspecies-specific characteristics such as morphological andstructural features (Balestri et al., 2003; Miller et al., 2005;Hauxwell et al., 2006). The pattern of increased photosyn-thetic performance was evident among all intertidal speciesfor ETRmax but for Ek exceptions included reef species Thalas-sia hemprichii and Cymodocea serrulata which, while exposedto high photon fluxes, exhibited relatively low Ek equivalent toZostera capricorni growing in estuarine habitats. Both reefspecies showed relatively efficient a compared with Z. capri-corni which suggests a more efficient capture of photons anda high demand for light that would benefit the growth of theseplants in multi-species stands. Although a general relationshipexisted between photosynthetic performance and photon fluxamong intertidal stands of seagrass, in some cases, species-specific responses to photon flux in particular habitats arelikely to influence their photosynthetic performance, growthresponses and regulate overall population productivity.

The uncoupling of physiology (e.g., ETRmax) and photonflux among seagrass populations in subtidal environments sug-gests that instantaneous light measures may not truly reflectthe light history to which all plants were exposed. In these

559S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

R2 = 0.68

0

50

100

150

200

250

300

0 600 1200

ETR

max

(μm

ol e

-1 m

-2 s

-1) a

R2 = 0.510

200

400

600

800

1000

1200

Photon flux density(μmol photons m-2 s-1)

E K (μ

mol

pho

tons

m-2

s-1

)

c

R2 = 0.56

0.0

0.2

0.4

0.6

0.8

1.0

Effe

ctiv

e qu

antu

m y

ield

(ΔF

v /F

m)

d

R2 = 0.0010.0

0.1

0.2

0.3

0.4

0.5

α (μ

mol

e- /μ

mol

pho

tons

) b

R2 = 0.06

0.0

0.2

0.4

0.6

0.8

1.0

Photon flux density(μmol photons m-2 s-1)

Abso

rpan

ce fa

ctor

e

900300 0 600 1200900300

0 600 12009003000 600 1200900300

0 600 1200900300

Fig. 5. Plots of photosynthetic variables (ETRmax, photosynthetic efficiency (a); saturating irradiance (Ek); effective quantum yield (DF/Fm0) and absorption

factors) against photosynthetic photon flux density (mmol photons m�2 s�1) for all species (n¼ 51).

environments responses of seagrass to photon flux may betempered by biotic and abiotic factors (e.g., epiphytes, sus-pended matter, sedimentation and phytoplankton) that attenu-ate light reaching the surface of seagrass leaves, potentiallyimpeding physiological performance (Hauxwell et al., 2006).Although this may also occur in both intertidal and subtidalhabitats, the uncoupling was evident in coastal populationsof subtidal Halophila ovalis and Halophila spinulosa in Her-vey Bay where lower ETRmax corresponded with relativelyhigh incident photon flux. Factors other than in situ photonflux (e.g., wave action and settlement of sediments on leaves)may therefore influence the photo-chemistry of these sea-grasses, as there was no obvious site-related difference inthe morphology, structural attributes, leaf densities or epiphyteloads of these seagrasses (unpublished data).

The strong positive relationship between Ek and PPFDamong species suggests a photo-adaptive response wherelow Ek values and high photosynthetic efficiencies (a) at depthallow more efficient and optimal use of low light climates.Among intertidal species the responses of Ek and ETRmax to

photon flux were similar, with high values for Halodule unin-ervis and Syringodium isoetifolium that would arguably makethese species highly competitive for available light and resil-ient to reductions in light availability. The low values recordedfor Thalassodendron ciliatum and Zostera caprcorni may bedue to low production rates (Duarte and Chiscano, 1999;Touchette and Burkholder, 2000) where both species are com-monly restricted to tidal pools that protect from desiccation,yet these habitats often exhibit low light conditions resultingfrom wind driven turbidity and suspension of sediments. Forthe most part, intertidal seagrasses had lower Ek values com-pared with in situ photon fluxes, and are therefore likely tobe light saturated during midday periods. In contrast saturatingirradiances of subtidal seagrasses were higher than in situ pho-ton fluxes suggesting that they were most likely light limitedduring peak solar insolation and least likely to be resilient toreductions in photon flux. Saturating irradiances generally de-creased with depth among subtidal species with highest valuesfound for H. uninervis and Halophila ovalis at 3e7 m depthand lowest values found in deepwater (10e20 m depth)

560 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

R2 = 0.010.0

0.1

0.2

0.3

0.4

0.5

α (μ

mol

ele

cton

s/ph

oton

s)

b

R2 = 0.30

0

50

100

150

200

250

300

ETR

max

(μm

ol e

-1 m

-2 s

-1)

a

R2 = 0.22

0

200

400

600

800

1000

1200

Depth (m)

E K (

μmol

e-1

m-2

s-1

)

c

1111

0 1051

R2 = 0.18

0.0

0.2

0.4

0.6

0.8

1.0

Effe

ctiv

e qu

antu

m y

ield

(ΔF

v /F

m')

d

R2 = 0.10

0.0

0.2

0.4

0.6

0.8

1.0

Depth (m)Ab

sorp

ance

fact

or

e

0 1051

Fig. 6. Plots of photosynthetic variables (ETRmax, photosynthetic efficiency (a), saturating irradiance (Ek), effective quantum yield (DF/Fm0) and absorption

factors) against depth (m) for all species (n¼ 51).

Table 5

Nested ANOVA of the effects of habitat and site (habitat) on ETRmax, (loge

transformed), photosynthetic efficiency (a), saturating irradiance (Ek) (loge

transformed) and effective quantum yield (arcsine square-root transformed)

for all species from all sites and depths

Source df MS F-ratio P

ETRmax

Habitat 3 2.255 11.087 0.001

Site (Habitat) 5 0.871 4.281 0.003

Error 42 0.203

Alpha

Habitat 3 0.032 7.431 0.001

Site (Habitat) 5 0.007 1.531 0.201

Error 42 0.004

Ek

Habitat 3 2.181 13.557 0.001

Site (Habitat) 5 1.178 7.324 0.001

Error 42 0.161

DF/Fm0

Habitat 3 0.106 9.842 0.001

Site (Habitat) 5 0.006 0.594 0.705

Error 42 0.011

H. ovalis and Halophila spinulosa. To compensate for light-limiting conditions H. ovalis and H. spinulosa at depthsgreater than 5 m exhibited shade-type characteristics (e.g.,low Ek: 65e399.2 mmol photons m�2 s�1) that maximise lightacquisition at low light fluxes. Light saturation for these spe-cies is more likely to be achieved when diurnally regulatedsaturating photon fluxes approximate in situ photon fluxes dur-ing morning and afternoon.

Depth-related increases in DF/Fm0 afford more efficient useof low light climates in deepwater plants compared with inter-tidal plants. The negative relationship of DF/Fm0 and PPFD isa pattern consistent with the notion that although intertidalplants are adapted to high light environments (i.e., highETRmax and Ek), they are capable of reducing DF/Fm0 athigh irradiance as a trade off between photosynthetic effi-ciency and photo-protection (Ralph et al., 1998; Schwarzand Hellblom, 2002; Silva and Santos, 2003). No such rela-tionship was found for a when all species were pooled, al-though the significant negative relationship between a andPPFD among subtidal species is consistent with the notionof increasing photosynthetic efficiency with increasing depth.Saroussi and Beer (2006) suggest that a should be calculated

561S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

0.0

0.2

0.4

0.6

0.8

1.0

Effe

ctiv

e qu

antu

m y

ield

(ΔF

/Fm

')

ab

bb

a abaaab

0

50

100

150

200

Cai

rns

Mou

rilya

nH

erve

yB

ayLi

zard

Is.

Gre

en Is

.O

rman

Ree

fH

erve

yB

ayLi

zard

IsO

rman

Ree

f

Cai

rns

Mou

rilya

n

Her

vey

Bay

Liza

rd Is

.

Gre

en Is

.

Orm

anR

eef

Her

vey

Bay

Liza

rd Is

Orm

anR

eef

Cai

rns

Mou

rilya

nH

erve

yB

ayLi

zard

Is.

Gre

en Is

.O

rman

Ree

fH

erve

yB

ayLi

zard

IsO

rman

Ree

f

Cai

rns

Mou

rilya

nH

erve

yB

ayLi

zard

Is.

Gre

en Is

.O

rman

Ree

fH

erve

yB

ayLi

zard

IsO

rman

Ree

f

Estua-rine

ETR

max

(μm

ol e

- m-2

s-1

)a

c

bab

ab

aa

b

0

200

400

600

800

Ek

(μm

ol p

hoto

ns m

-2 s

-1)

a cc

a

b

b

ab

aa

0

0.1

0.2

0.3

0.4

0.5

α (μ

mol

e- /μ

mol

pho

tons

m-2

s-1

)

abc acc

b

aa acacac

DeepwaterReefCoastal Estua-rine

DeepwaterReefCoastal

Estua-rine

DeepwaterReefCoastalEstua-rine

DeepwaterReefCoastal

Fig. 7. Mean (�SE) (of site means) ETRmax, photosynthetic efficiency (a), saturating irradiance (Ek) and effective quantum yield (DF/Fm0) of each site (nested

within four habitat types) for all species pooled (n¼ 2e8). Different superscript letters denote significant difference (P< 0.05) between mean habitat variables.

F/Fm' ETRmax

Ek

55.32%

21.50% Depth

PPFD

α

Fig. 8. Principal components analysis of site means of species photosynthetic

variables (ETRmax, a, Ek and DF/Fm0) and site features (depth (m) and PPFD

(mmol photons m�2 s�1)). Habitat types denoted by open diamonds (estuary),

open circles (deepwater), closed circles (coastal) and closed squares (reef).

using absorbed rather than incident PPFD, however, whenthese were calculated (data not shown) no relationship existedbetween a and depth or PPFD. Our findings concur withSaroussi and Beer (2006) that a is not a good indicator of pho-tosynthetic performance and that DF/Fm0 measured just priorto applying the increasing irradiances, provides the best mea-sure of photosynthetic efficiency. The decline in DF/Fm0 athigher light fluxes was generally due to decreasing Fm ratherthan increases in Fo (data not shown), indicative of photo-chemical quenching rather than destruction of PSII reactioncentres, a pattern also found in Halophila johnsonii (Durakoet al., 2003). The weak negative relationship between absor-bance factor and depth across all species pooled implies thatthis parameter can vary considerably within and among spe-cies most likely from variations in local light climates andspecies characteristics (Schwarz and Hellblom, 2002; Silvaand Santos, 2003). Indeed, for Halophila ovalis, a speciesubiquitous in its geographic and depth range, the absorptionfactor varied between regions and showed no consistent deptheffect among sites. This finding contrasts with other seagrassspecies where absorbance factors have been found to reflectchlorophyll concentrations showing maximal values in lowlight conditions (Major and Dunton, 2002; Schwarz andHellblom, 2002).

562 S.J. Campbell et al. / Estuarine, Coastal and Shelf Science 73 (2007) 551e562

5. Conclusion

The study has shown that ETRmax, Ek and DF/Fm0 are goodindicators of seagrass physiological performance in relation tophoton flux and depth. Among intertidal populations the re-sponses of seagrass photosynthesis to photon flux and depthwere generally stronger than for subtidal seagrasses, but excep-tions to these patterns were evident at both intertidal and subtidalsites. The uncoupling of photosynthesis and light among somespecies was most likely because of individual species responsesto changes in light that occur among and within habitats. Theseparation of sites according to seagrass physiology could be de-fined to some extent by habitat type yet exceptions reveal the lo-calised uncoupling of seagrass photosynthetic performance andphoton flux within coastal and reef habitats most likely due totemporal and spatial fluctuations in light. Nevertheless, thisstudy provides a first attempt in tropical Australia to define thesehabitats according to seagrass photosynthetic performance andphoton flux characteristics. The work highlights the importanceof photon flux as a primary factor driving seagrass growth andshows that physiological measures can be used to evaluate theability of plants to adapt and tolerate ambient conditions acrossa range of habitat types.

Acknowledgments

This work was funded by the Australian Cooperative Re-search Centre Program through the CRC Reef Reserch Centreand the Department of Primary Industries, Queensland, Aus-tralia. Thanks to Meredith Campey who assisted with dataanalyses and Fred Short and Robert Coles who assisted withreviews of the manuscript.

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