Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
Contents lists available at ScienceDirect
Journal of Experimental Marine Biology and Ecology
j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / j e m b e
Patterns of resistance and resilience of the stress-tolerant coral Siderastrea radians
(Pallas) to sub-optimal salinity and sediment burial
Diego Lirman a,⁎, Derek Manzello b
a
University of Miami, Rosenstiel School of Marine and Atmospheric Science, Marine Biology and Fisheries Division,
4600 Rickenbacker Cswy., Miami, Florida 33149, USA
b
Atlantic Oceanographic and Meteorological Laboratory, National Oceanic and Atmospheric Administration, Miami, Florida 33149, USA
a r t i c l e
i n f o
Article history:
Received 18 August 2008
Received in revised form 21 October 2008
Accepted 22 October 2008
Keywords:
Corals
Resilience
Resistance
Salinity stress
Sediment burial
a b s t r a c t
The coastal lagoons of south Florida, U.S., experience fluctuating levels of sedimentation and salinity and contain
only a subset of the coral species found at the adjacent reefs of the Florida Reef Tract. The dominant species within
these habitats is Siderastrea radians, which can reach densities of up to 68 colonies m- 2 and is commonly exposed
to salinity extremes (b 10 psu to N 37 psu) and chronic sediment burial. In this study, we document the patterns of
resistance and resilience of S. radians to sub-optimal salinity levels and sediment burial in a series of short-term,
long-term, acute, chronic, single-stressor, and sequential-stressor experiments.
S. radians displayed remarkable patterns of resistance and resilience and mortality was documented only under
prolonged (≥48 h) continuous exposure to salinity extremes (15 and 45 psu) and chronic sediment burial. A
reduction in photosynthetic rates was documented for all salinity exposures and the decrease in photosynthesis
was linearly related to exposure time. Negative impacts on photosynthetic rates were more severe under low
salinity (15 psu) than under high salinity (45 psu). Corals exposed to intermediate, low-salinity levels (25 psu),
exhibited initial declines in photosynthesis that were followed by temporary increases that may represent
transient acclimatization patterns. The impacts of sediment burial were influenced by the duration of the burial
period and ranged from a temporary reduction in photosynthesis to significant reductions in growth and tissue
mortality. The maintenance of P/R ratios N 1 and the rapid (b24 h) recovery of photosynthetic rates after burial
periods of 2-24 h indicates that S. radians is able to resist short-term burial periods with minor physiological
consequences. However, as burial periods increase and colonies become covered at multiple chronic intervals,
sediment burial resulted in extended photosynthetic recovery periods, reduced growth, and mortality. Under
normal conditions (i.e., no salinity stress), S. radians was very effective at clearing sediments, and N 50% of the
colonies' surface area was cleared within 1 h. However, clearing rates were influenced by physiological status, and
prior exposure to sub-optimal salinity significantly reduced the clearing rates of stressed colonies.
The response of S. radians to disturbance documented in this study characterizes this species as highly stresstolerant and provides an explanation for its present high abundance in both reef and marginal environments.
Moreover, the key life-history attributes of S. radians, such as brooding reproductive strategy, small colony size,
high stress-tolerance, and high recruitment rates, suggest the potential for this species to replace reef-building
taxa under increased disturbance scenarios in Florida and elsewhere in the region.
© 2008 Elsevier B.V. All rights reserved.
1. Introduction
Coral reefs have undergone a drastic decline in diversity, abundance,
and condition in the recent past that has focused attention on the
impacts of single and multiple stressors on coral abundance, distribution, and condition (e.g., Gardner et al., 2003; Hughes et al., 2003;
Pandolfi et al., 2003; Wilkinson, 2004). While patterns of decline have
been widespread across spatial scales and taxonomic groups, reviews of
the impacts of coral disturbances based on correlational and experi⁎ Corresponding author.
E-mail address: [email protected] (D. Lirman).
0022-0981/$ – see front matter © 2008 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2008.10.024
mental studies indicate that the response of corals to both chronic and
acute stress can be highly species-specific (e.g., Jokiel and Coles, 1990;
Coles and Jokiel, 1992; Fabricius, 2005). In fact, the species-specific
susceptibility of corals to disturbances is reflected in the patterns of coral
decline observed in the Caribbean, which have been characterized by the
loss of the main reef-building coral taxa (Hughes, 1994; Hughes and
Tanner, 2000; Kramer, 2003) and corresponding increases in the relative
cover of stress-resistant, weedy coral species (Green et al., 2008).
In Florida, declines of up to 95 % in the cover of Acropora spp. and
Montastraea spp. have been reported, underscoring the high susceptibility of these taxa to increased temperature, coral diseases, and
hurricane impacts (Jaap et al., 1988; Dustan, 1999; Dustan et al., 2001;
D. Lirman, D. Manzello / Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
Miller et al., 2002; Palandro et al., 2003). In the Caribbean region, high
mortality and limited sexual recruitment of reef-building taxa has
resulted in the increased predominance of stress-tolerant, early
colonizing taxa like Porites and Agaricia on natural (Hughes and Connell,
1999; Kramer, 2003; Green et al., 2008) and artificial substrate (Lirman
and Miller, 2003; Vermeij, 2005).
South Florida's Biscayne Bay and Florida Bay experience extreme
and highly variable levels of sedimentation and salinity. Hardbottom
habitats within these lagoons contain coral communities with only
a subset of the species found at the adjacent reefs of the Florida
Reef Tract. Siderastrea radians, which can reach densities of up to 68
colonies m- 2, is the dominant Scleractinian in these habitats (Lirman
et al., 2003). In Biscayne Bay, S. radians colonies are found in
shallow (b2 m) nearshore habitats influenced by the inflow of
freshwater from canal structures that can cause salinities to drop
dramatically (to b5 psu) over a period of hours and remain well below oceanic values for extended periods of time. The shallow nature
of this basin and the limited water turnover can also create hypersaline (N37 psu) conditions during the dry season (Jan-April)
(Lirman et al., 2008). Lastly, high sedimentation and sediment
migration rates in these basins can cause N45% of colonies to be
completely buried at any given time (Lirman et al., 2003).
In addition to being the dominant species in the coastal lagoons of
southeast Florida, S. radians is a ubiquitous component of coral
communities of the Florida Reef Tract where it usually occupies highsedimentation, low-lying locations within these habitats (Chiappone
and Sullivan, 1994; Lirman and Fong, 2007). The high recruitment
potential of this species makes it a very successful early colonizer on
newly available substrate such as reef restoration structures (Miller and
Barimo, 2001; Lirman and Miller, 2003) and wrecks (Vermeij, 2005).
Finally, high abundance of this species in disturbed or marginal
environments has also been documented by Lewis (1989) in Barbados
and by Moses et al. (2003) in the Cape Verde Islands.
In this study, we document the patterns of resistance (i.e., the
intensity and duration of a stressor needed to elicit a significant negative
response) and resilience (i.e., the rate of return to a pre-disturbance
state) of Siderastrea radians exposed to sub-optimal salinity levels and
sediment burial, two stress factors commonly encountered by this
species in its natural lagoon habitat in a series of short-term, long-term,
acute, chronic, single-stressor, and sequential-stressor experiments. The
response of S. radians to single and multiple stressors documented in
this study characterizes this species as highly stress-tolerant and
provides an explanation for its high abundance in both reef and
marginal non-reef environments.
2. Materials and methods
Colonies of Siderastrea radians (b4 cm in diameter) were collected
from Biscayne Bay, Florida, and kept in outdoor tanks for an acclimation
period of 2-3 weeks. All the experiments were conducted under ambient
light in a water table for temperature control and colonies were kept in
flow-through outdoor tanks during all recovery periods. The stressor
levels and exposure times were chosen to cover the range of sub-optimal
conditions encountered by corals in Biscayne Bay, especially in those
habitats influenced by freshwater inflow from water management
canals (Lirman et al., 2003, 2008).
Two types of experiments were performed: (1) single-exposure
experiments where corals were exposed to a treatment for different
lengths of time; and (2) multiple-exposure experiments where corals
were exposed to treatments for 24 h at weekly intervals over a period of
three months. Coral condition was assessed as tissue coloration and
polyp appearance (retracted or extended). Colony coloration was
classified as normal (normal pigmentation throughout the colony),
pale (lighter coloration in the coral theca and coenosteum), and
bleaching (white coloration throughout the colony) (Lirman et al.,
2002). The surface area of each colony was measured with calipers
73
assuming a hemispherical shape, and growth or partial mortality were
assessed by documenting changes in live tissue area over time. To
measure photosynthesis and respiration rates, corals were placed in
clear and opaque 1-liter containers sealed to prevent gas diffusion.
Concurrently, control light and dark containers without corals were used
to account for photosynthesis and respiration due to the plankton and
bacterial components of seawater as described by Manzello and Lirman
(2003). Corals were kept within the sealed containers for 2 h, after which
dissolved oxygen was measured. Photosynthesis and respiration rates
were always measured under experimental conditions during the last
2 h of the exposure period. For example, for a 4-hr exposure to 25 psu,
corals were kept in 20-1 containers at 25 psu for the first 2 h. After the
initial 2 h, the corals were transferred to dark and light 1-1 containers
filled with water at 25 psu for the remainder of the exposure period (i.e.,
2 h), over which photosynthesis and respiration rates were measured.
The water used for all the 1-1 containers was drawn from a single, wellmixed batch so that initial conditions were similar for all corals. Lastly, to
reduce the amount of variability due to daily variations in photosynthetic rates as well as the variable light intensity during incubation
times, the parameters obtained for each experiment were compared
only to those obtained for control corals that were run simultaneously.
Photosynthetic rates were expressed as: (1) net photosynthesis (i.e.,
changes in mg O2 cm- 2 hr- 1); and (2) relative photosynthesis. Relative
photosynthesis was calculated as the deviation from the mean value
obtained for the corresponding coral controls, allowing for comparisons
among data collected at different dates and times (Manzello and Lirman,
2003). Differences in mean photosynthetic, respiration, and growth
rates were tested with Wilcoxon rank-sum tests (2 groups) and KruskalWallis tests (N2 groups) due to non-conformity to the normality
assumption required for parametric tests (Sokal and Rohlf, 1995).
Recovery was deemed complete when no significant differences in net
photosynthetic rates were found between exposed and control corals.
2.1. Single-Exposure Experiments
Salinity Exposure: Colonies of S. radians (n = 10 colonies per treatment)
were exposed to treatments of 15, 25, 35 (oceanic controls), and 45 psu
in a series of short-term (2, 4, 6, 24, 48 h) and long-term (7 and 21 d)
exposure experiments. Salinity levels were adjusted by adding freshwater to compensate for evaporation and the water was changed every
3 d during long-term exposure experiments. High-salinity treatments
(45 psu) were created using seawater concentrated through evaporation. After exposure, corals were returned to outdoor mesocosms and
photosynthesis and coral survivorship and photosynthesis and respiration rates were measured as described.
Sediment Burial: Colonies of S. radians (n = 10 colonies per treatment)
were buried completely under sediments for 1, 4, 24, and 48 h.
Sediments were collected from Biscayne Bay, rinsed with freshwater,
and dried for 48 h prior to the experiments. Enough sediment was added
to ensure that the corals would not be able to uncover any portion of the
colony during the exposure period. After the burial time, corals were
rinsed to remove sediments and photosynthesis and respiration were
measured as described. The photosynthetic rates of previously buried
corals were monitored after 24 h, 48 h, and 7 d to document recovery
patterns. Control corals were buried concurrently with experimental
corals, but sediments were removed immediately for these controls.
Photosynthesis and respiration rates of control corals were determined
as described for the exposed corals.
A second experiment was conducted to document sediment clearing
rates and to evaluate whether sediment clearing rates in S. radians are
influenced by colony shape. For this experiment, hemispherical colonies
(sphericity index = mean height-to-diameter = 0.55, n = 15) and flat
colonies (sphericity index = 0.4, n = 8) were used (Riegl, 1995). Dead
hemispherical colonies (n= 8) were used as controls. Containers with
sediments spread evenly over the bottom were placed in an outdoor
tank. Corals were placed on the surface of the sediments and slowly
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D. Lirman, D. Manzello / Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
Table 1
Mean rates (±S.D.) of net photosynthesis and respiration (mg O2 cm- 2 hr- 2) for colonies of Siderastrea radians exposed of salinity treatments for different exposure periods. Each
exposure experiment had a corresponding control treatment exposed to 35 psu seawater. Pg/R=mean gross photosynthesis rates / mean respiration rates
15 psu
25 psu
45 psu
Time
Type
Photosynthesis
Respiration
Pg/R
Photosynthesis
Respiration
Pg/R
Photosynthesis
Respiration
Pg/R
2h
exp.
control
exp.
control
exp.
control
exp.
control
exp.
control
exp.
control
exp.
control
0.029 (0.004)
0.07 (0.019)
0.024 (0.006)
0.06 (0.02)
0.009 (0.006)
0.041 (0.01)
0.002 (0.002)
0.046 (0.012)
- 0.004 (0.011)
0.054 (0.020)
- 0.006 (0.021)
0.036 (0.013)
- 0.004 (0.017)
0.042 (0.015)
0.019 (0.002)
0.022 (0.007)
0.014 (0.008)
0.019 (0.004)
0.009 (0.004)
0.025 (0.009)
0.006 (0.006)
0.027 (0.011)
0.027 (0.021)
0.012 (0.007)
0.019 (0.014)
0.013 (0.01)
0.023 (0.013)
0.016 (0.026)
2.5
4.2
2.7
4.2
2.0
2.6
1.3
2.7
0.8
5.5
0.7
3.8
0.8
3.6
0.015 (0.006)
0.039 (0.018)
0.022 (0.006)
0.036 (0.009)
0.016 (0.005)
0.039 (0.006)
0.017 (0.008)
0.038 (0.003)
0.025 (0.008)
0.041 (0.009)
0.014 (0.003)
0.051 (0.014)
0.018 (0.005)
0.032 (0.01)
0.009 (0.002)
0.008 (0.003)
0.005 (0.002)
0.01 (0.006)
0.008 (0.003)
0.012 (0.005)
0.015 (0.025)
0.013 (0.01)
0.022 (0.009)
0.009 (0.002)
0.004 (0.003)
0.018 (0.005)
0.01 (0.003)
0.013 (0.01)
2.7
5.9
5.4
4.6
3.0
4.3
2.1
3.9
2.1
5.6
4.5
3.8
2.8
3.5
0.022 (0.006)
0.027 (0.006)
0.018 (0.006)
0.027 (0.011)
0.017 (0.004)
0.023 (0.009)
0.011 (0.003)
0.026 (0.004)
0.016 (0.012)
0.071 (0.013)
0.029 (0.019)
0.098 (0.032)
-
0.009 (0.004)
0.005 (0.004)
0.014 (0.007)
0.009 (0.003)
0.019 (0.005)
0.013 (0.003)
0.023 (0.021)
0.016 (0.005)
0.026 (0.004)
0.039 (0.038)
0.022 (0.069)
0.025 (0.02)
-
3.4
6.4
2.3
4.0
1.9
2.8
1.5
2.6
1.6
2.8
2.3
4.9
-
4h
6h
8h
24 h
48 h
7 days
covered with additional sediments until the colonies were no longer
visible. Clearing of the sediments commonly occurred from the top of
the colony in a circular pattern, increasing gradually in diameter. The
surface area of the cleared tissue was measured every hour and used to
calculate the percent of total surface area of each colony cleared over
time (Weber et al., 2006).
2.2. Multiple Exposure Experiments
S. radians colonies (n = 10 colonies per treatment) were exposed to
salinity treatments (15, 25, 35 (oceanic controls), and 45 psu) and
sediment burial for 24 h at weekly intervals for up to three months.
Corals were placed in outdoor tanks between exposure periods. Coral
growth and partial mortality were assessed every 4 weeks.
2.3. Salinity and Sediment Burial
To evaluate the impacts of prior exposure to sub-optimal salinity
on the sediment-clearing response of S. radians, sediment-clearing
trials were conducted following 24 h of exposure to 20 psu (n = 16 colonies), 25 psu (n = 16 colonies), 35 psu (controls, n = 15 colonies), and
45 psu (n = 12 colonies). While 15 psu was used as the lowest salinity
treatments in all previous experiments, salinity levels reached 20 psu
during the sediment clearing experiment. All of the colonies used
were hemispherical. A second sediment-clearing trial was performed
24 h and 5 d after the initial experiment to document the recovery of
the sediment clearing response after return to control oceanic salinity
conditions.
Recovery of photosynthetic rates took 24 h for the corals exposed for
2 h, 5 d for the corals exposed for 4 and 6 h, and 7-10 d for corals exposed
for 8, 24 and 48 h. The relative photosynthetic rates of the surviving
corals exposed for 7 d were still depressed compared to controls after
21 d of recovery. Coloration of the surviving colonies exposed to 15 psu
for 7 d returned to normal after 6 weeks of recovery.
Photosynthetic rates of S. radians exposed to 25 psu were significantly
lower than the corresponding controls for all exposure periods from
2 h -7 d (p b 0.05 for all tests) (Table 1; Fig. 1). The recovery of photosynthetic rates took 24 h for corals exposed for 2-24 h, 48 h for corals
exposed for 48 h, and 9 d for corals exposed for 7 d. Photosynthesis
always exceeded respiration and no tissue mortality was observed for
any of the short-term exposures. While tissue paling was observed after
exposures of 24 h -7 d, complete bleaching was not observed. No tissue
mortality was observed during long-term exposures and normal tissue
coloration returned within 6 weeks of recovery.
Photosynthetic rates of S. radians exposed to 45 psu were lower than
the corresponding controls for all exposure periods from 2-48 h, but
significant decreases were only observed for exposures of 8-48 h
(p b 0.05 for all tests) (Table 1; Fig. 1). Photosynthesis always exceeded
respiration and no tissue mortality was observed for any of the
treatments. The recovery of photosynthetic rates took longer for corals
exposed to 45 psu than any of the previous exposure experiments (1525 psu). Recovery of photosynthetic rates took 7 d for the corals exposed
for 8 h,14 d for the corals exposed for 24 h, and 21 d for corals exposed for
48 h. Tissue coloration was pale after 7 d and 21 d and recovered fully for
3. Results
3.1. Salinity Exposure
The immediate reaction of corals exposed to salinity stress was polyp
retraction and tissue paling. Net photosynthesis of S. radians was
significantly lower following 2, 4, 6, and 8 h of exposure to 15 psu
compared to controls (p b 0.05 for all tests). In corals exposed to 15 psu
for 24 h, 48 h, and 7 d, respiration rates exceeded photosynthesis
(Table 1; Fig.1). While respiration rates for corals exposed to 15 psu were
lower than those of the controls for exposures of 2, 4, 6, and 8 h, these
declines were only significant for corals exposed for 6 and 8 h (p b 0.05
for both tests). In contrast, longer exposures (24 h, 48 h, and 7 d),
resulted in an increase in respiration rates of exposed corals in
comparison to controls, and P/R values that were b1 (Table 1). Two of
the colonies exposed for 48 h died. After one week of exposure to 15 psu,
all corals were completely bleached and 4 of the 10 colonies died. After
3 weeks of exposure, all of the colonies in the 15 psu treatment died.
Fig. 1. Relative photosynthesis of Siderastrea radians exposed to different salinity
treatments. ⁎ = respiration exceeded photosynthesis.
D. Lirman, D. Manzello / Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
75
80% of colonies after 6 weeks of recovery. After 21 d of exposure, 2
colonies from the 45 psu treatment exhibited partial tissue losses of 40%
and 55% of the original live tissue surface area.
3.2. Sediment Burial
Tissue paling was observed for all colonies buried regardless of burial
time. No significant impacts on photosynthesis or respiration were
documented after burial periods of 1 and 2 h (pN 0.05). However, when the
burial period increased to 4 and 24 h, significant declines in photosynthesis were documented (pb 0.05). No significant differences in respiration
rates were observed for any of the burial periods. After the longest burial
period (48 h), respiration exceeded photosynthesis (Fig. 2). S. radians
colonies that were buried for 24 h recovered full photosynthetic ability
after 48 h, and colonies buried for 48 h recovered fully after one week.
Hemispherical colonies of S. radians showed a rapid sedimentclearing response and were able to uncover 56.8 % (S.E.M.= ±6.8) of their
surface area within 1 h and 92.7 % (±4.2) within 4 h (Fig. 3). In contrast,
flat colonies cleared a significantly lower percentage of their surface area
(36.4% (±15.1) after 1 h and 57.4 % (±13.8) 4 h) (p b 0.05). None of the dead
control colonies cleared any sediment during the 4 h burial experiment.
3.3. Multiple Exposure Experiments
No significant differences in growth were documented for S. radians
colonies exposed to 15 psu (mean radial growth = 0.28 mm mo- 1 ± 0.14),
25 psu (0.34 mm mo- 1 ± 0.13), 35 psu (controls, 0.33 mm mo- 1 ± 0.11),
and 45 psu (0.22 mm mo- 1 ± 0.22) for 24 h at weekly intervals for 30 d
(p N 0.05). However, after 60 d (i.e., 8 exposures) the growth rates of
corals in the extreme treatments, 15 psu (0.34 mm mo- 1 ± 0.16) and
45 psu (0.37 mm mo- 1 ± 0.17), were significantly lower than the growth
rates of the controls (0.57 mm mo- 1 ± 0.12) (p b 0.05). No tissue mortality
was observed during these chronic exposures.
The growth of S. radians colonies buried under sediments for 24 h at
weekly intervals (0.14 mm mo- 1 (±0.12), n = 10) was significantly
reduced after 30 d (i.e., 4 exposures) (p b 0.05) compared to control
corals (0.39 mm± 0.13). Furthermore, 50 % of the experimental colonies
suffered complete mortality after 3 months, while control colonies
showed no signs of partial mortality over the same period.
3.4. Salinity and Sediment Burial
Prior exposure to salinity extremes (45 and 20 psu) had a significant
effect on the ability of S. radians to clear sediments (Fig. 3). Control
Fig. 3. Mean % sediment clearance (± S.E.M.) of Siderastrea radians based on prior
exposure to different salinity treatments and colony shape. Colonies were exposed to
the salinity treatments for 24 h prior to sediment burial.
colonies were able to clear a significantly larger percentage of their
surface area compared to corals that were previously exposed to suboptimal salinity treatments (p b 0.01). Four hours after burial, 41% and
36% of the surface of colonies exposed to 45 and 20 psu, respectively,
were clear of sediments. In contrast, corals exposed to 25 psu and
ambient salinity (35 psu) had 62% and 92% of their surface cleared
respectively. S. radians colonies exposed to 25 and 45 psu recovered the
ability to clear sediments efficiently (i.e., no significant differences
between exposed and control corals) after 24 h of recovery, but it took
considerably longer (5 d) for those colonies previously exposed to 20 psu
to clear sediments as fast as control corals.
4. Discussion
Siderastrea radians displayed remarkable patterns of resistance and
resilience to the stressors tested in this study and tissue mortality was
documented only under prolonged (≥48 h) continuous exposure to
salinity extremes (15 and 45 psu) and chronic sediment burial. Acute and
shorter-term exposures resulted in only a transient depression of
photosynthetic rates. The response of S. radians to increasing levels of
disturbance followed a progression that included: (1) polyp retraction;
(2) reduced photosynthesis and either increased or decreased respiration; (3) tissue paling; (4) bleaching; (5) reduction in growth rates; and
finally (6) tissue mortality. Polyp retraction as an immediate reaction to
stress decreases the surface area of the tissue in contact with the
surrounding environment was also observed for S. siderea (Muthiga and
Szmant, 1987), Porites astreoides (Lirman, 2001), P. furcata (Manzello and
Lirman, 2003) and numerous other species of Caribbean (Bak and
Elgershuzien, 1976) and Australian (Stafford-Smith and Ormond, 1992)
corals. Changes in coloration (i.e., paling) are also commonly reported as
a signal of stress for corals subject to salinity, sedimentation, and other
stressors, and the progression from polyp retraction to paling to
bleaching under extended or more severe stress has been previously
reported by Coles and Jokiel (1992), Stafford-Smith (1993), and Wessling
et al. (1999). Philipp and Fabricius (2003) concluded that the change in
coloration of corals exposed to sediments was likely due to the expulsion
of zooxanthellae from the host tissue, a response that was also
documented for corals under hypo-osmotic stress by Kerswell and
Jones (2003).
4.1. Salinity Stress
Fig. 2. Relative photosynthesis of Siderastrea radians buried under sediments for
different periods of time. ⁎ = respiration exceeded photosynthesis.
The sudden exposure to sub-optimal salinity levels caused a
consistent decrease in photosynthetic rates of S. radians. In contrast,
the response of respiration rates to changes in salinity was highly
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D. Lirman, D. Manzello / Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
variable as described by Vernberg and Vernberg (1972) for both marine
and estuarine species. The decrease in photosynthesis relative to
controls for corals exposed to salinity extremes was linearly related to
exposure time, but negative impacts on coral photosynthetic rates were
more severe under low salinity (15 psu) than under high salinity
(45 psu). In contrast, photosynthetic recovery took longer for corals
exposed to higher salinity.
A reduction in photosynthesis is the most commonly documented
effect of salinity stress on corals (reviewed by Coles and Jokiel, 1992) and
the decrease is often directly proportional to the magnitude or duration
of the salinity change (Muthiga and Szmant, 1987). However, the
impacts of salinity stress appear to be highly species-specific. In Florida,
patterns of high tolerance to sub-optimal salinity were recorded for
S. siderea and Porites furcata, which were able to withstand sudden and
extended changes in salinity without lethal impacts (Muthiga and
Szmant, 1987; Manzello and Lirman, 2003). The reef-building coral
Montastraea annularis was able to sustain autotrophy and showed no
tissue mortality after exposure to 40 psu for 36 h (Porter et al., 1999), but
P. porites showed high mortality after 5 d of exposure to 15 and 45 psu
(Marcus and Thouraug, 1981). For S. radians, P/R ratios were maintained
N1 under most experimental stressful conditions and full photosynthetic recovery was documented for all but the most extreme salinity
treatments, establishing the resilience of this species to salinity stress at
both ends of the osmotic spectrum encountered in Biscayne Bay.
Little information is presently available on the osmoregulatory
mechanisms of corals exposed to salinity stress. Nevertheless, previous
studies have shown that a limited number of euryhaline coral species are
in fact able to withstand and quickly recover from osmotic stress (Coles
and Jokiel,1992). In the present study, corals exposed to intermediate, lowsalinity levels (25 psu), exhibited initial sharp declines in photosynthesis
that were followed by temporary increases that may represent transient
acclimatization patterns. This pattern was also observed by Manzello and
Lirman (2003) for P. furcata, suggesting that corals commonly exposed to
rapid environmental fluctuations may exhibit a limited capacity for
osmoregulation (Mayfield and Gates, 2007). The mechanisms involved in
the response of corals to osmotic stress, which clearly warrant further
examination, may include behavioral responses such as polyp retraction to
limit water and gas exchange with the external medium and physiological
responses through the production of organic osmolytes to protect cell
volume regulation (Mayfield and Gates, 2007). While it is not yet known
what mechanisms specifically confer S. radians its high levels of resilience
and resistance to stress, it is clear that a further understanding of how
unusually hardy coral species can thrive in marginal environments will
provide important insights into the future ability of corals to persist
through large-scale habitat modifications and climate change.
4.2. Sediment Burial
The impacts of sediment burial on S. radians were influenced by the
duration of the burial period and ranged from a temporary reduction in
photosynthesis to significant reductions in growth and tissue mortality.
The maintenance of P/R ratios N1 and the rapid (i.e., b24 h) recovery of
photosynthetic rates after burial periods of 2-24 h indicates that
S. radians is able to resist short-term burial periods with minor
physiological consequences. However, as burial periods increase and
colonies become covered at multiple chronic intervals, the impacts of
sediment burial can become significant, resulting in extended photosynthetic recovery periods (7 d for a 48 h burial), reduced growth, and,
ultimately, colony mortality.
Sedimentation is regarded as an increasing threat to coral reefs
(reviewed by Fabricius, 2005). The impacts associated with sedimentation and sediment burial include reduced photosynthesis and increased
respiration (Riegl and Branch, 1995; Philipp and Fabricius, 2003; Weber
et al., 2006), tissue mortality (Rogers, 1983, 1990), reduced growth
(Dodge et al., 1974; Rice and Hunter, 1992), and reduced fertilization,
larval survivorship, and recruitment (Gilmour, 1999; Babcock and Smith,
2000). Previous research has identified the genus Siderastrea as a
competent sediment remover (Hubbard and Pocock, 1972) and the
tolerance of S. radians species to burial has been highlighted in the
pioneer work by Mayer (1918) who reported that this species was only
“half killed” after being covered by sediments for N73 h.
Under normal conditions (i.e., no salinity stress), S. radians was very
effective at clearing sediments, and N50% of the colonies' surface area
was cleared within 1 h after burial. Rapid initial sediment clearing,
followed by a slower response has been documented for numerous
other corals species by Lasker (1980), Stafford-Smith (1993), and Riegl
(1995). The clearing response of buried corals is potentially influenced
by both active behavioral factors (e.g., tissue swelling, mucus production, tentacular and ciliary action) and factors influenced by colony
shape (Hubbard and Pocock,1972; Stafford-Smith and Ormond,1992). In
this study, we showed that both active and passive factors play a role in
the clearing response of S. radians as only live colonies cleared sediments and hemispherical colonies cleared sediments faster than flatter
colonies.
4.3. Sequential Stressors
S. radians was shown to be well-suited to resist and recover from
single stressors. However, the sequential exposure of colonies to salinity
and sediment burial highlighted the interactive negative influence of
multiple stressors. The clearing rates of S. radians were influenced by the
physiological status of colonies and prior exposure to sub-optimal
salinity significantly reduced the clearing rates of stressed colonies that
were unable to clear sediments efficiently. The energetic costs of
sediment clearing can be considerable (Riegl and Branch, 1995), and the
inability to clear sediments exposes corals to further stress as anoxic
conditions under sediments can cause tissue bleaching and subsequent
mortality (Weber et al., 2006). Thus, even highly resistant and resilient
corals like S. radians can become susceptible to sequential stressors that
would not normally cause long-term impacts when encountered
individually. The impacts of sequential stressors and the effects of
impaired physiological status on stress resistance and resilience are
topics of renewed scientific and management interest as the frequency
and intensity of both human and natural stressors increase over time.
Some examples of the interactive effects of stressors include the higher
susceptibility to elevated temperature of corals exposed to low salinity
(Coles and Jokiel, 1978), the higher levels of bleaching in areas with high
sedimentation (Nemeth and Sladek-Nowlis, 2001), and the increased
prevalence of coral diseases in corals previously weakened by elevated
temperatures and bleaching (Bruno et al., 2007; Whelan et al., 2007;
Wilkinson and Souter, 2008).
The ecological niche of coral species is defined partly by patterns of
resistance and resilience to stress. For example, the high resistance and
resilience of S. radians to different coral stressors allows this species to
thrive in habitats that commonly limit the diversity, abundance, growth,
survivorship, and spatial distribution of more susceptible corals. The
drastic decline in coral abundance reported for the Caribbean region
over the past several decades (Gardner et al., 2003) has been
characterized by the high mortality of the main reef-building coral
genera like Acropora and Montastraea. In Florida, the high susceptibility
of these taxa to hurricanes, diseases, and changes in water quality has
resulted in significant declines in the condition and abundance of these
keystone members of the reef community (Dustan et al., 2001; Miller
et al., 2002; Palandro et al., 2003). Moreover, the lack of recruitment
success of these genera raises concern about their long-term recovery
potential. In contrast, more stress-tolerant taxa like Siderastrea and
Porites continue to be both dominant components and successful
recruiters on Florida reefs (Miller et al., 2002; Tougas and Porter, 2002;
Lirman and Fong, 2007). These patterns may set up the stage for the
relative increase of tolerant taxa and even the replacement of
susceptible taxa by stress-tolerant species. Such scenarios have been
predicted and documented by Aronson and Precht (2001), Aronson et al.
D. Lirman, D. Manzello / Journal of Experimental Marine Biology and Ecology 369 (2009) 72–77
(2002), and Green et al. (2008) in Caribbean reef systems. The key lifehistory attributes of S. radians, such as brooding reproductive strategy,
small colony size, high stress tolerance, and high recruitment potential,
all suggest a similar role for this species under increased disturbance
scenarios in Florida and elsewhere in the Caribbean region.
Acknowledgements
Funding for this project was provided by NOAA's Coastal Ocean
Program (Award NA17RJ1226), EPA STAR Program (#Award R-82745301-0), and the Florida Department of Environmental Protection (Award
NRD08).
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