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Journal of Experimental Marine Biolog
Photosynthetic responses of seven tropical seagrasses to elevated
seawater temperature
Stuart J. Campbell a,b, Len J. McKenzie a,b,*, Simon P. Kerville a
a Northern Fisheries Centre, Department of Primary Industries and Fisheries, PO Box 5396, Cairns, Qld, 4870, Australiab CRC Reef Research Centre, PO Box 772, Townsville, Qld, 4810, Australia
Received 8 December 2004; received in revised form 24 April 2005; accepted 15 September 2005
Abstract
This study uses chlorophyll a fluorescence to examine the effect of environmentally relevant (14 h) exposures of thermal stress
(3545 8C) on seagrass photosynthetic yield in seven tropical species of seagrasses. Acute response of each tropical seagrassspecies to thermal stress was characterised, and the capacity of each species to tolerate and recover from thermal stress was
assessed. Two fundamental characteristics of heat stress were observed. The first effect was a decrease in photosynthetic yield (Fv /
Fm) characterised by reductions in F and FmV. The dramatic decline in Fv /Fm ratio, due to chronic inhibition of photosynthesis,
indicates an intolerance of Halophila ovalis, Zostera capricorni and Syringodium isoetifolium to ecologically relevant exposures of
thermal stress and structural alterations to the PhotoSystem II (PSII) reaction centres. The decline in FmV represents heat-induced
photoinhibition related to closure of PSII reaction centres and chloroplast dysfunction. The key finding was that Cymodocea
rotundata, Cymodocea serrulata, Halodule uninervis and Thalassia hemprichii were more tolerant to thermal stress than H. ovalis,
Z. capricorni and S. isoetifolium. After 3 days of 4 h temperature treatments ranging from 25 to 40 8C, C. rotundata, C. serrulataand H. uninervis demonstrated a wide tolerance to temperature with no detrimental effect on Fv /FmV qN or qP responses. These
three species are restricted to subtropical and tropical waters and their tolerance to seawater temperatures up to 40 8C is likely to bean adaptive response to high temperatures commonly occurring at low tides and peak solar irradiance. The results of temperature
experiments suggest that the photosynthetic condition of all seagrass species tested are likely to suffer irreparable effects from
short-term or episodic changes in seawater temperatures as high as 4045 8C. Acute stress responses of seagrasses to elevatedseawater temperatures are consistent with observed reductions in above-ground biomass during a recent El Nino event.
Crown Copyright D 2005 Published by Elsevier B.V. All rights reserved.
Keywords: Seagrass; Elevated temperature; Global warming; El Nino; Tropical; Australia
1. Introduction
Shallow water tropical seagrasses are exposed to a
range of environmental stresses, including high solar
radiation, ultra-violet radiation, desiccation and temper-
0022-0981/$ - see front matter. Crown Copyright D 2005 Published by Els
doi:10.1016/j.jembe.2005.09.017
* Corresponding author. Northern Fisheries Centre, Department of
Primary Industries and Fisheries, PO Box 5396, Cairns, Qld, 4870,
Australia. Tel.: +61 7 4035 0131; fax: +61 7 4035 4774.
E-mail address: [email protected] (L.J. McKenzie).
ature fluctuations. Fluctuations in seasonal seawater
temperatures in tropical habitats range from 19.8 to
41 8C (McKenzie, 1994; McKenzie and Campbell,2004). Critical thermal stress has been reported in
temperate seagrasses at temperatures exceeding 35 8C(Bulthuis, 1983; Ralph, 1998), but few studies have
examined temperature responses of tropical seagrass
species (Fong and Harwell, 1994; Terrados and Ros,
1995). Tropical species of seagrasses generally increase
their photosynthesis at elevated temperatures (Perez and
y and Ecology 330 (2006) 455468
evier B.V. All rights reserved.
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S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468456
Romero, 1992; Terrados and Ros, 1995). However,
temperatures rising above the normal upper limit of
35 8C can inhibit carbon production in plants becausehigh temperatures bring about increased respiration
(Bulthuis, 1983; Ralph, 1998) and photosynthetic en-
zyme breakdown (Bruggeman et al., 1992; Ralph,
1998). Light requirements for carbon production are
also greater at higher temperatures because of increased
compensation irradiance (Bulthuis, 1987).
Thermal stress has a significant impact on the bio-
geographical distribution and condition of seagrass
meadows (Bulthuis, 1983; Hillman et al., 1989; McMil-
lan, 1984; Ralph, 1998). Climatic factors influencing
the ambient water temperature of seagrass meadows
include global temperature oscillations (e.g. El Nino),
global warming, seasonal and diurnal fluctuations
(Short and Neckles, 1999). Anthropogenic causes of
seawater temperature increases include the release of
heated effluents into shallow embayments where sea-
grasses proliferate (Thorhaug et al., 1978). Seawater
and air temperatures are factors that limit the upper
distributional limits of seagrass meadows. Seagrasses
in shallow pools of water are not only exposed to
elevated temperatures during midday sun exposure,
but they are also subject to desiccation during low
tidal periods and high PAR and UV radiation (Dawson
and Dennison, 1996; Durako and Kunzelman, 2002).
Mean sea temperature increases of up to 2 8C may havea severe impact on species of seagrass that survive at
the upper limit of their thermal tolerance (Ralph, 1998).
Increases in seawater temperatures of up to 10 8C abovethe seasonal average can occur in tropical shallow water
pools especially during spring low tides and during
midday solar exposure (McKenzie and Campbell,
2004;www.seagrasswatch.org). During these events
seagrasses may be exposed to elevated seawater tem-
peratures for periods of 3 to 4 h. High seawater tem-
peratures and desiccation have negatively affected
seagrass meadows in a number of areas worldwide
(Seddon and Cheshire, 2000; Walker and Cambridge,
1995; Erftemeijer and Herman, 1994) with one episode
of seagrass loss linked to an El Nino climatic pattern
(Seddon and Cheshire, 2000).
The effects of thermal stress on photosynthesis,
productivity and morphology of seagrasses have been
examined mostly in temperate habitats (Drew, 1979;
McMillan and Phillips, 1979; McMillan, 1983;
Bulthuis, 1987). These studies suggest that changes in
seawater temperature on seagrass habitats are depen-
dent on a number of interacting factors including: du-
ration of exposure, acclimatisation (thermal history),
light regime and leaf maturity (Bulthuis, 1987; Seddon
and Cheshire, 2000). Fong and Harwell (1994) suggest
that the productivity of tropical seagrass species starts
to decline above 30 8C but few studies have examinedthe thermal tolerance of tropical seagrass species to
changes in seawater temperature. Thorhaug et al.
(1978) reported that at temperatures elevated 34 8Cabove ambient, Thalassia testudinum showed evidence
of reduced standing crop and productivity, and that
tropical plants were more tolerant than subtropical
plants to elevated temperature. However, some species
(e.g. Halophila ovalis) with a wide geographical toler-
ance have a broad temperature tolerance (Ralph, 1998)
but tolerance of tropical seagrass species to periods of
high temperature exposure is less studied.
We used measures of effective photosynthetic quan-
tum yield to examine the effect of 14 h exposures of
thermal stress (3545 8C) on seagrass photosyntheticyield over a 3-day period. A pulse amplitude modulated
(PAM) fluorometer was used to measure effects of
thermal stress on chlorophyll a fluorescence within
PhotoSystem II (PSII), the most temperature sensitive
component of the photosynthetic apparatus (Ralph,
1998). The objectives of the present study were to:
characterise the acute response of 7 species of tropical
seagrass to thermal stress; assess each species capacity
to tolerate thermal stress and to assess the capacity of
tropical seagrasses to recover from thermal stress.
2. Methods
Six species of seagrass (Cymodocea rotundata,
Cymodocea serrulata, Halodule uninervis, Halophila
ovalis, Syringodium isoetifolium, Thalassia hempri-
chii) were collected at Green Island in northern
Queensland, Australia (38815V S 145821V E). Zosteracapricorni was collected from Cairns Harbour, Queens-
land, Australia (16853V S, 145846V E) (Fig. 1). Allplants were collected in the afternoon prior to the
start of the experiment and acclimated overnight in
oxygenated seawater maintained at 26 8C.Three temperature treatments were conducted over
three 5-day periods in May 2003. Each experiment
consisted of a control temperature treatment at 26 8C(n =8), representing the ambient temperature of seawa-
ter at Green Island in May, and three elevated temper-
ature treatments (each n =8) consisting of plants
exposed to 35, 40 or 45 8C. Plants were held in separate2 l containers with oxygenated re-circulating seawater.
All containers were immersed within a larger aquarium
(60 l), where they were acclimated overnight (26 8C).On each experimental day, the 2 l containers of
plants were directly transferred to the re-circulating
http:www.seagrasswatch.org
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Fig. 1. Location of Green Island and Cairns Harbour on the north-eastern coast of Queensland, Australia.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 457
treatment seawater system at 1100 h, which was then
elevated to the treatment temperature over a period of
1530 min. Plants were exposed to treatment tempera-
tures (35, 40 or 45 8C) for 4 h (from 1100 to 1500 h).
The photochemical efficiency of PhotoSystem II (PSII)
and the effective quantum yield of photochemistry
(DF /FmV) were evaluated by subjecting light adaptedleaves to saturating pulses of light using a pulse ampli-
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S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468458
tude modulated (PAM) fluorometer (Diving-PAM)
(Walz, Germany). For each seagrass plant the basic
parameters of chlorophyll fluorescence (F, FmV) were
measured on the leaf shoot adjacent to the meristem, on
8 replicate leaves of each seagrass species, every hour
from 1100 to 1500 h. The mid-portion of each leaf (3
cm from meristem) was held in a leaf clip (Walz,
DIVING LC) and fluorescence measurements were
made underwater with the light probe joined to the
leaf clip. A weak pulsed red light (b1 Amol quantam2 s1) was applied to determine F in an illuminated
state. A saturating pulse (800 ms of 8000 Amol quantam2 s1 PAR) was then applied to FmV in an illumi-
nated state. The change in fluorescence (Fv or DF)caused by the saturating pulse (FmVF) in relationto the maximal fluorescence (FmV) is a measure of
quantum yield (Genty et al., 1989). The effective quan-
tum yield is given by DF /FmV (Eq. (1)). The separationof photochemical quenching (qP) and non-photochem-
ical quenching (qN) of chlorophyll fluorescence pro-
vides insight to the regulatory processes occurring
within the photosynthetic apparatus (Bolhar-Norden-
kampf et al., 1989). The quenching characteristics at
each time interval were calculated from Fv, F, and FmV(Bolhar-Nordenkampf et al., 1989).
Y FmV FV =FmV Fv=FmV 1
where
Y = effective quantum yield
FmV = maximal fluorescence in light adapted leaves
FV = initial fluorescence in light adapted leavesFv = (FmVFV)
At 1500 h all replicate plants were returned to
acclimation conditions at 26 8C overnight. On days 2and 3, the experiment was repeated. On days 4 and 5 all
plants were retained at 26 8C to determine recoveryrates following thermal stress. Parameters of chloro-
phyll fluorescence (F, FmV), photochemical quenching
Table 1
Absorbance factors, ecological niche, substrate and location of 7 species of
Species Absorbance factor
(F95% confidence interval)Ecological
Cymodocea rotundata 0.72F0.02 Mid-intertiCymodocea serrulata 0.79F0.02 Shallow suHalodule uninervis 0.70F0.03 Mid-intertiHalophila ovalis 0.56F0.04 Upper inteThalassia hemprichii 0.78F0.01 Mid-intertiZostera capricorni 0.48F0.03 Upper inteSyringodium isoetifolium 0.73F0.04 Shallow-de
(qP) and non-photochemical quenching (qN) were
made on 8 replicate leaves of each species at 1100
h on each day for control and treatment plants.
The proportion of incident irradiance absorbed by
leaves was determined for 5 replicate leaves for each
species. Each leaf was placed over the light sensor of
the Diving-PAM and incident saturating PAR recorded
with and without leaf according to the method de-
scribed by Schwarz and Hellblom (2002). The light
path distance was 3 mm, as that gave consistent optimal
readings of quantum yield of 0.700.80 for dark
adapted leaves healthy leaves. The measures were
made to determine if there were differences in leaf
absorbance that may explain responses to seawater
temperature exposure.
Mean quantum yield values at 50 h (end of temper-
ature exposure period) and 96 h (end of recovery
period) were analysed relative to mean control values
to provide a summary of plant responses at the 3
temperature exposure treatments. A three way
ANOVA (SYSTAT vers. 10.2) was used to test for
the effect of species, experiment (35, 40 and 45 8C)and treatment (control, temperature exposed). Data
were arcsin square-root transformed prior to analysis.
3. Results
3.1. Absorbance factors
The proportion of incident irradiance absorbed by
leaves ranged from 0.70 to 0.79 for C. serrulata, C.
rotundata, H. uninervis, T. hemprichii, S. isoetifolium
and less than 0.70 for H. ovalis and Z. capricorni
(Table 1). Habitat characteristics of all species are
also presented (Table 1).
3.2. Quantum yield relative to controls
The percentage of effective quantum yield of plants
exposed to temperature treatments relative to control
tropical seagrasses
niche Substrate Location
dalshallow subtidal Sand Green Island reef-flat
btidal Sand Green Island lagoon
dalshallow subtidal Sand Green Island reef-flat
rtidaldeep subtidal Sand Green Island reef-flat
dalshallow subtidal Sand Green Island reef-flat
rtidalshallow subtidal Mud Cairns Harbour mud-bank
ep subtidal Sand Green Island lagoon
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S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 459
treatments was calculated at 50 and 96 h. At 50 and 96
h the exposure/control percentage of effective quantum
yield of C. rotundata, C. serrulata, H. uninervis and T.
hemprichi, at 35 and 40 8C, ranged from 86% to 105%;for H. ovalis and S. isoetifolium these values ranged
from 43% to 69% and 61% to 81%, respectively (Fig.
2). At 45 8C (50 and 96 h) all species had effectivequantum yield values 537% of controls (Fig. 2). Re-
sponse was significantly different between control and
exposed for each treatment and for all species at both
50 (Table 2) and 96 h (Table 3) treatments.
0
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Fig. 2. Percentage (exposed/control) of effective quantum yield
(DF /FmV) for each seagrass species (o = Halophila ovalis, x =Halodule uninervis, 5 = Syringodium isoetifolium, E = Zosteracapricorni, w = Cymodocea rotundata, D = Cymodocea serrulata,. = Thalassia hemprichii) (4 h at 35, 40 and 45 8C) exposed toseawater temperatures, at (a) 50 h (day 3 of exposure) and (b) 96
h (end of recovery period).
3.3. Fluorescence values ( F and FmV)
For light adapted C. rotundata, C. serrulata and H.
uninervis the initial minimum fluorescence (F) was
relatively steady when exposed to 35 8C, 40 8C andrespective control treatments during the 3-day 4 h expo-
sures (Fig. 3). A few times during the 5-day experi-
ment lower F values were evident for S. isoetifolium
and T. hemprichi at 35 8C compared with controls, andfor H. ovalis, S. isoetifolium and T. hemprichi at 40 8Ccompared to controls (Fig. 3). At 45 8C the decline inF, compared with control treatments, occurred after 24
h in all species and persisted during the 2-day recovery
(25 8C) period.No difference in maximum fluorescence (FmV) could
be detected between control (26 8C) and thermal treat-ments (35, 40 8C) for C. rotundata, C. serrulata and H.uninervis during the 3-day exposure and 2-day recovery
(25 8C) period (Fig. 4). Similarly no difference betweencontrol and 35 8C treatments was found for Z. capricorniand H. ovalis. In contrast lower FmV values relative to
controls were found for T. hemprichi and S. isoetifolium
at 35 8C and for T. hemprichi, S. isoetifolium and H.ovalis at 40 8C during the 3-day thermal exposure and 2-day recovery period. For Z. capricorni lower FmV values
at 40 8C were found relative to controls during the finalday of thermal treatment and day 1 of recovery (Fig. 4).
For all species FmV declined by greater than 50% in the
first 2 h of 45 8C exposure, and during day 2 of 45 8Cexposure FmV declined to less than 80% of the initial
value in all species (Fig. 4).
3.4. Effective quantum yield (DF /FmV)
For C. rotundata, C. serrulata , H. uninervis and Z.
capricorni the effective quantum yield was relatively
steady when exposed to 35 8C, 40 8C and respectivecontrol (26 8C) treatments during the 3-day 4 h expo-sures (Fig. 5). At 40 8C, DF /FmV values for S. iso-etifolium, Z. capricorni and H. ovalis were 1035%
lower than control plants (Fig. 5). A decline in H. ovalis
DF /FmV to 50% of initial values occurred during the 2-day post-thermal stress recovery period (Fig. 5). At 45
8C a rapid decline in DF /FmV after 1 h was observedfor all species and persisted during the 3-day exposure
and 2-day recovery period.
A significant three way interaction between species,
experiment and treatment at 50 h was explained by
similar yield values of all species at 35 8C relative tocontrols, lower yield values for H. ovalis and S. iso-
tetifolium at 40 8C compared to all other species andcontrols and lower values for all species at 45 8C
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Table 2
Three way ANOVA of the effects of temperature (control vs exposed), treatment (35, 40, 45 8C) and species on effective quantum yield in 8 seagrassspecies at 50 h after exposure to temperature treatments for 4 h over a 3-day period (n =328)
Source Sum-of-squares df Mean-square F-ratio P
Temperature 7.862 2 3.931 302.238 0.000
Treatment 5.064 1 5.064 389.344 0.000
Species 0.203 6 0.034 2.601 0.018
Temperature treatment 7.089 2 3.544 272.531 0.000Temperature species 0.550 12 0.046 3.527 0.000Treatment species 0.137 6 0.023 1.758 0.108Temperature treatment species 0.286 12 0.024 1.830 0.043Error 3.720 286 0.013
Data were arcsin square-root transformed prior to analysis.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468460
compared to controls. A similar pattern was evident at
96 h, except that S. isotetifolium at 40 8C was not lowerthan controls suggesting recovery of this species after
exposure to 25 8C.
3.5. Quenching coefficients (qP and qN)
There was no apparent difference in qP between
control plants and those exposed to 35 8C. Similarlyfor plants of C. rotundata, C. serrulata, H. uninervis, S.
isoetifolium, T. hemprichii and Z. capricorni exposed
to 40 8C, photochemical quenching (qP) values did notdiffer from respective control (26 8C) treatments duringthe 3-day 4 h exposures (Fig. 6). For H. ovalis and qP
values at 40 8C were up to 20% lower compared withcontrols. A decline in H. ovalis qP to 75% of initial
values occurred during the 2-day post-thermal stress
recovery period (Fig. 6). At 45 8C a rapid decline inqP after 1 h was observed for all species and persisted
during the 3-day exposure and 2-day recovery period.
Non-photochemical quenching remained near 0 for
most species at 35 8C, 40 8C and respective control (268C) treatments (Fig. 7). At 40 8C non-photochemicalquenching (qN) for H. ovalis ranged between 0.2 and
0.6 on days 1 and 3 and increased to 0.8 during the
recovery period. By day 2 at 45 8C non-photochemical
Table 3
Three way ANOVA of the effects of temperature (control vs exposed), treatm
species at 96 h after exposure to temperature treatments for 4 h over a 3-da
Source Sum-of-squares
Temperature 8.819
Treatment 6.968
Species 0.671
Temperature treatment 9.600Temperature species 1.636Treatment species 0.220Temperature treatment species 0.507Error 3.533
Data were arcsin square-root transformed prior to analysis.
quenching (qN) was 1012 fold higher than respective
control (25 8C) treatments.
4. Discussion
The key finding of this study was that C. rotundata,
C. serrulata , H. uninervis and T. hemprichi were more
tolerant to thermal stress than S. isoetifoilum, Z. capri-
corni and H. ovalis. After 3 days of 4 h temperature
treatments ranging from 26 to 40 8C, C. rotundata, C.serrulata and H. uninervis demonstrated a wide toler-
ance to temperature with no effect on DF /FmV, qN orqP responses. These three species are restricted to
subtropical and tropical waters and their tolerance to
seawater temperatures of 40 8C is likely to be anadaptive response to high temperatures commonly
occurring at low tides and peak solar irradiance. Both
C. rotundata and C. serrulata were also more tolerant
for the initial 4 h treatment of 45 8C compared with allother species. Experimental responses in the present
study occurred at less than 100 Amol m2 s1, belowsaturation for these species (unpubl data), and the sen-
sitivity of seagrass species is likely to be greater at high
in situ irradiances during peak solar intensities. Indeed
Ralph (1999) found that elevated light and osmotic
stress increased the sensitivity of H. ovalis to thermal
ent (35, 40, 45 8C) and species on effective quantum yield in 8 seagrassy period (n =328)
df Mean-square F-ratio P
2 4.410 368.227 0.000
1 6.968 581.836 0.000
6 0.112 9.342 0.000
2 4.800 400.813 0.000
12 0.136 11.385 0.000
6 0.037 3.068 0.006
12 0.042 3.526 0.000
295 0.012
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C. rotundata (45 degrees)
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900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
T. hemprichii (40 degrees)
0
100
200
300
400
500
600
700
800
900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
T. hemprichii (35 degrees)
0
100
200
300
400
500
600
700
800
900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Zostera (45 degrees)
0
100
200
300
400
500
600
700
800
900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Zostera (40 degrees)
0
100
200
300
400
500
600
700
800
900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Zostera (35 degrees)
0
100
200
300
400
500
600
700
800
900
1000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Fig. 3. Minimum fluorescence ( F) for each seagrass species exposed to control (o) (26 8C) and treatment (n) (4 h at 35, 40 and 45 8C) seawatertemperatures, for each treatment day and subsequent recovery period. The break in the data-line represents the end of each exposure period.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 461
-
C. rotundata (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
C. rotundata (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
C. rotundata (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
C. serrulata (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
C. serrulata (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
C. serrulata (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
H. ovalis (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
H. ovalis (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
H. ovalis (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Halodule uninervis (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Halodule uninervis (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Halodule uninervis (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
S. isoetifolium (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
S. isoetifolium (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
S. isoetifolium (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
T. hemprichii (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
T. hemprichii (40 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
T. hemprichii (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Zostera (45 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Zostera (40 degrees)
0
500
1000
1500
2000
2500
3000
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Zostera (35 degrees)
0
500
1000
1500
2000
2500
3000
3500
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Max
imu
m f
lou
resc
ence
(F
m')
Fig. 4. Maximum fluorescence ( FmV) for each seagrass species exposed to control (o) (26 8C) and treatment (n) (4 h at 35, 40 and 45 8C) seawatertemperatures, for each treatment day and subsequent recovery period. The break in the data-line represents the end of each exposure period.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468462
-
C. rotundata (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
C. rotundata (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
C. rotundata (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
C. serrulata (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
C. serrulata (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
C. serrulata (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
H. ovalis (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ldH. ovalis (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
H. ovalis (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Halodule uninervis (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Halodule uninervis (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Halodule uninervis (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
S. isoetifolium (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
S. isoetifolium (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
S. isoetifolium (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
T. hemprichii (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
T. hemprichii (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
T. hemprichii (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Zostera (45 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Zostera (40 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Zostera (35 degrees)
0
0.1
0.2
0.3
0.4
0.5
0.6
0.7
0.8
0.9
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
effe
ctiv
e q
uan
tum
yie
ld
Fig. 5. Effective quantum yield ( Y) for each seagrass species exposed to control (o) (26 8C) and treatment (n) (4 h at 35, 40 and 45 8C) seawatertemperatures, for each treatment day and subsequent recovery period. The break in the data-line represents the end of each exposure period.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 463
-
C. rotundata (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
C. rotundata (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
C. rotundata (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
C. serrulata (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
C. serrulata (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
C. serrulata (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
H. ovalis (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
H. ovalis (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
H. ovalis (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Halodule uninervis (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Halodule uninervis (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Halodule uninervis (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
S. isoetifolium (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
S. isoetifolium (40 degrees)
0
1
2
3
4
5
6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
S. isoetifolium (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
T. hemprichii (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
T. hemprichii (40 degrees)
0
1
2
3
4
5
6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
T. hemprichii (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Zostera (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Zostera (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Zostera (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
Ph
oto
chem
ical
qu
ench
ing
(q
P)
Fig. 6. Photochemical quenching (qP) for each seagrass species exposed to control (o) (26 8C) and treatment (n) (4 h at 35, 40 and 45 8C) seawatertemperatures, for each treatment day and subsequent recovery period. The break in the data-line represents the end of each exposure period.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468464
-
C. rotundata (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
C. rotundata (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
C. rotundata (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
C. serrulata (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
C. serrulata (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
C. serrulata (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
H. ovalis (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
H. ovalis (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
H. ovalis (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Halodule uninervis (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Halodule uninervis (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Halodule uninervis (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
S. isoetifolium (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
S. isoetifolium (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
S. isoetifolium (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
T. hemprichii (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
T. hemprichii (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
T. hemprichii (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Zostera (45 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Zostera (40 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Zostera (35 degrees)
0
0.2
0.4
0.6
0.8
1
1.2
1.4
1.6
0 1 2 3 4 24 25 26 27 28 48 49 50 51 52 72 96
No
n-p
ho
toch
emic
al q
uen
chin
g (
qN
)
Fig. 7. Non-photochemical quenching (qN) for each seagrass species exposed to control (o) (26 8C) and treatment (n) (4 h at 35, 40 and 45 8C)seawater temperatures, for each treatment day and subsequent recovery period. The break in the data-line represents the end of each exposure
period.
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 465
-
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468466
stress, suggesting that seagrass species may be even
less tolerant to high seawater temperatures during mid-
day saturating light exposure.
Symptoms of thermal stress found for H. ovalis, S.
isoetifolium and Z. capricorni at 40 8C suggest alower thermal tolerance and a susceptibility to eco-
physiological damage when climatic conditions result
in atypically high seawater temperatures. All are eu-
rythermal species with a broad thermal tolerance (10
35 8C) found growing in both tropical (McKenzie,1994) and temperate waters (Ralph, 1998; Campbell
et al., 2003a,b). Their low tolerance to high tempera-
tures (N35 8C) suggests that their photosynthetic con-dition would suffer detrimental effects from episodic
increases in water temperatures greater than 35 8C.Ralph (1998) also found that H. ovalis was intolerant
to temperatures above 37 8C over a 5 h period. Thequantity of light absorbed by leaves of H. ovalis is
lower than other species examined (Table 1) suggest-
ing it has lower leaf thickness and chlorophyll pig-
mentation. These characteristics may in part explain its
susceptibility to temperature relative to other species.
McMillan (1983) also found that H. ovalisminor
complex was susceptible to temperature with no sur-
vival of small leaved cultures after 18 h exposure to
39 8C and similarly no survival of larger leaf culturesafter 48 h exposure to 39 8C.
The susceptibility of S. isoetifolium to temperature
may be associated with its cylindrical morphology
(high surface area to volume ratio), the presence of
a thin leaf cuticle and thin vascular-bundle cell walls
(Kuo, 1993). Such leaf anatomy and ultrastructure is
advantageous for nutrient uptake and gaseous ex-
change and this species has been found to have a
relatively high production rate (0.92 g DW m2
d1) compared with other species used in this exper-
iment (0.010.50 g DW m2 d1) (Duarte and Chis-
cano, 1999). The morphology, however, would also
expose a proportionally high area of leaf tissue per
volume to stress from increased seawater temperature.
It is a species that previously has been restricted to
subtidal waters because of an intolerance to high
temperatures (i.e. 40 8C) in intertidal reef habitats(McMillan, 1983; Bridges and McMillan, 1986).
McMillan (1983) reported that both S. isoetifolium
and S. filiforme cultures were least tolerant to tem-
peratures of 39 8C relative to 7 other tropical genera.This susceptibility was attributed to its lack of distri-
bution in shallow waters that are exposed to high air
and seawater temperatures. At elevated temperatures
damage to photosynthetic tissue is likely to arise from
a loss of specific enzyme activity and changes in
transport of molecules and to membrane function
(Ralph, 1998). Damaged cells are characterised by a
brownish-black discoloration of cell wall and contents
(Biebl and McRoy, 1981; Walker and Cambridge,
1995).
We observed two fundamental characteristics of heat
stress to seagrasses using saturation PAM fluorometry.
The first effect was a decrease in photosynthetic yield
characterised by reductions in F and FmV. The dramatic
decline in Fv /FmV ratio, due to chronic inhibition of
photosynthesis, indicates an intolerance of H. ovalis, S.
isoetifolium and Z. capricorni to ecologically relevant
exposures of thermal stress. The decline in F and FmV is
indicative of structural alterations to the PSII reaction
centres that can take several days to recover (Ralph,
1998; Macinnis-Ng and Ralph, 2004). The decline in
FmV represents heat-induced photoinhibition related to
closure of PSII reaction centres and chloroplast dys-
function (Havaux, 1994). Such a response is likely due
to a combination of factors including increased respi-
ration, photoinhibition and enzyme breakdown. For
both Z. capricorni and H. ovalis the inability to recover
following 3 days of elevated temperature exposure (40
and 45 8C) suggests irreparable damage to chloroplaststructure and PSII function. The resulting burden to the
carbon balance of the plant would limit the survival
potential of seagrass leaves at temperatures greater than
40 8C.The second effect was an increase in non-photo-
chemical quenching, coupled with a decrease in pho-
tochemical quenching. Non-photochemical quenching
is considered to reflect a mechanism for photo-protec-
tion which is designed to protect the over-reduction of
the photosynthetic electron transport chain by dissipa-
tion of excess absorbed light energy in the PSII an-
tenna system as heat (Demmig-Adams, 1990).
Increases in non-photochemical quenching in H. ovalis
after 96 h exposure to temperatures greater than 30 8Chave been reported (Ralph, 1998), and the current
study shows that non-photochemical quenching rapidly
increased at temperatures of 40 8C and above. Rapidand complete decline of qP in three species at 40 8Cand in all 7 species at 45 8C suggests chloroplastmembrane damage eliminating electron transport and/
or temperature-dependent enzyme inactivation (Brug-
geman et al., 1992). As thermal stress was observed in
all 7 seagrass species after 1 h at 45 8C, heat inducedphotoinhibition and closure of PSII reaction centres
occurred rapidly and was irreparable. Damage to
PSII function in heat stress has been reported for 1
species of seagrass (Ralph, 1999) and some corals
(Jones et al., 1998). The lack of recovery by all species
-
S.J. Campbell et al. / Journal of Experimental Marine Biology and Ecology 330 (2006) 455468 467
at 45 8C suggests that photosynthetic enzymes havebeen inactivated or damaged (Bruggeman et al., 1992)
and acclimation to these temperatures for short (4 h)
exposure periods is unlikely. The resultant reduced
consumption of ATP can lead to an accumulation of
stored energy in the thykaloid membrane and an in-
crease in the proton gradient within PSII (Ralph,
1998). Excess absorbed light energy unable to be
used in the photosynthetic process is dissipated with
the resulting increase in non-photochemical quenching
(qN) and decrease in photochemical quenching (qP),
as demonstrated in this study. The recovery of Z.
capricorni photosynthetic yield after exposure to
high temperatures indicates a protective role of PSII
down-regulation consistent with that found previously
in H. ovalis (Ralph, 1998).
Results from the present study show that relatively
short exposures (b4 h) of elevated seawater tempera-
tures can damage seagrass physiology. Such conditions
are most likely to occur from November to May when
high solar irradiance and high seawater temperatures
combine to inhibit photosynthesis. Such findings are
consistent with declines in seagrass abundance during
the recent climatic anomalies in 2001/2002 in northern
Queensland (Roelofs et al., 2003; Campbell et al.,
2003a,b). Average seawater temperatures during the
austral summer of 2001/2002 increased by 12 8C(Berkelmans et al., 2004; Jones et al., 2004) and ele-
vated seawater temperatures (N35 8C) were recorded inshallow pools at low tide (McKenzie and Campbell,
2004). Meteorological data suggests that negative tides
were infrequent during solar noon periods in the austral
summer of 2001/2002, suggesting that exposure and
desiccation of seagrass leaves at low tide could not
fully explain seagrass dieback.
The results of temperature experiments here sug-
gest that the photosynthetic condition of all seagrass
species tested is likely to suffer irreparable effects
from short-term or episodic changes in seawater
temperatures as high as 4045 8C. Species differin their thermal tolerance making some (e.g. H.
ovalis, S. isoetifolium, Z. capricorni) more suscepti-
ble to thermal stress than others. Tolerance to tem-
peratures up to 40 8C in C. rotundata, C. serrulata,H. uninervis and T. hemprichii demonstrates an
adaptive tolerance of PSII reaction centres and chlor-
oplasts to temperature increases. H. ovalis, S. iso-
etifolium and Z. capricorni would appear least
thermo-tolerant of all species examined and that
may explain in part their biogeographical distribution
and recent loss in some tropical habitats in north
Queensland (unpubl data).
It may at first appear unusual that both H. ovalis and
Z. capricorni were the species least tolerant to tempera-
tures of z40 8C, as species appear well adapted to growin upper intertidal areas where shallow pools of water
can exceed 40 8C. The results of temperature experi-ments here suggest that they cannot tolerate extended
periods (N4 h) of temperatures z40 8C. Z. capricorni isnear the northern limit of its distribution in north Queens-
land, suggesting it may be intolerant of seawater tem-
peratures at latitudes above 108 S. In contrast H. ovalisand S. isoetifoilium are widespread throughout tropical
latitudes and morphological characteristics would ap-
pear to limit their tolerance to high seawater tempera-
tures. The ability of H. ovalis leaves to grow and
turnover rapidly may in part compensate for shoot loss
during excessive seawater temperature rises. The small
leaves of H. ovalis also flatten on the sediment surface
during low tide, a feature that keeps them moist and
protects them from desiccation (Bjork et al., 1999). On
the other hand S. isoetifolium is restricted to shallow
subtidal waters and its ecological niche suggests a ge-
netic intolerance to excessive temperatures, although
other ecological factors are likely to determine the
niche of seagrasses within habitats experiencing extreme
changes in environmental conditions.
An understanding of the thermal tolerance of tropical
species of seagrass is important to understand the stress
symptoms of seagrass ecosystems to climatic changes
that may lead to changes in seagrass species composition
and seagrass decline. Implications of the loss of species
and change in species dominance have ramifications for
herbivorous marine animals that target seagrass for food
and animals that use seagrass areas for habitat.
Acknowledgments
We thank Rudi Yoshida and Kate Pritchard for their
assistance in conducting laboratory experiments and
Rob Coles for providing review comments. This work
was supported by the Australian Cooperative Research
Centre Program through the CRC Reef Research Cen-
tre, and the Department of Primary Industries and
Fisheries, Queensland. [SS]
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Photosynthetic responses of seven tropical seagrasses to elevated seawater temperatureIntroductionMethodsResultsAbsorbance factorsQuantum yield relative to controlsFluorescence values (F and Fm)Effective quantum yield (DeltaF/Quenching coefficients (qP and qN)
DiscussionAcknowledgmentsReferences