Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
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
Acclimation and adaptation of scleractinian coral communities along environmental
gradients within an Indonesian reef system
Sebastian J. Hennige a,⁎,1, David J. Smith a, Sarah-Jane Walsh a, Michael P. McGinley b,
Mark E. Warner b, David J. Suggett a
a
b
Coral Reef Research Unit, Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, United Kingdom
College of Earth, Ocean and Environment, University of Delaware, 700 Pilottown Road, Lewes, Delaware 19958, United States
a r t i c l e
i n f o
Article history:
Received 5 March 2010
Received in revised form 16 June 2010
Accepted 17 June 2010
Keywords:
Acclimation
Adaptation
Environmental gradients
Marginal reefs
Massive corals
Symbiodinium
a b s t r a c t
In 2007 and 2008, multiple sites were identified in the Wakatobi Marine National Park, South East Sulawesi,
Indonesia, which each represented a point along a gradient of light quality, temperature and turbidity. This
gradient included ‘optimal’, intermediate and marginal sites, where conditions were close to the survival
threshold limit for corals. Coral communities changed across this gradient from diverse, mixed growth form
assemblages to specialised, massive growth form dominated communities. The massive coral Goniastrea aspera
was the only species identified at the most marginal and optimal sites. Branching species Acropora formosa and
Porites cylindrica were only identified at optimal sites. The in hospite Symbiodinium community also changed
across the environmental gradient from members of the Symbiodinium clade C on optimal reefs (in branching and
massive species) to clade D on marginal reefs (in massive species). Substantial variability in respiration and
photosynthesis was observed in massive coral species under different environmental conditions, which suggests
that all corals cannot be considered equal across environments. Studying present-day marginal environments is
crucial to further understanding of future reef bio-diversity, functioning and accretion, and from work presented
here, it is likely that as future climate change extends marginal reef range, branching coral diversity may decrease
relative to massive, more resilient corals.
© 2010 Elsevier B.V. All rights reserved.
1. Introduction
Scleractinian corals are often associated with clear blue water tropical
reefs, but can inhabit a wide variety of more ‘atypical’ environments
(Kleypas, 1996; Guinotte et al., 2003; Anthony and Connolly, 2004).
Conditions within these atypical environments, such as light availability,
sediment loading, inorganic nutrient input, temperature, salinity and
aragonite saturation states are often drastically higher or lower than
required for optimum growth (Rogers, 1990; Miller and Cruise, 1995;
Guinotte et al., 2003). Consequently, scleractinian corals are pushed close
to the threshold required for net coral growth. Some of these
environmental conditions are associated with high latitude reefs, which
have been termed marginal reefs (Celliers and Schleyer, 2002; Perry and
Larcombe, 2003; Celliers and Schleyer, 2008). However, the criteria for a
reef to be considered marginal (Kleypas et al., 1999) can also be met at low
latitudes (Kleypas et al., 1999; Bak and Meesters, 2000; Guinotte et al.,
2003), in particular, intertidal, fringing mangroves and terrestrial basin
⁎ Corresponding author.
E-mail address: [email protected] (S.J. Hennige).
1
Present address: College of Earth, Ocean and Environment, University of Delaware,
700 Pilottown Road, Lewes, Delaware 19958, United States.
0022-0981/$ – see front matter © 2010 Elsevier B.V. All rights reserved.
doi:10.1016/j.jembe.2010.06.019
areas (Rogers, 1990; Mitchell and Furnas, 1997; Anthony, 2000).
Regardless of the location of these marginal reefs, corals must successfully
respond to substantial variations (or gradients) in growth conditions in
order to successfully recruit and survive.
Successful colonisation (recruitment and growth) across environmental gradients requires that both the symbiotic microalgae
(Symbiodinium spp.) and the host coral optimise available resources,
while retaining the physiological plasticity needed to survive under
different conditions. This trade-off can potentially be achieved through
careful interplay between acclimatization and adaptation (Falkowski and
LaRoche, 1991; Iglesias-Prieto and Trench, 1994; Hennige et al., 2009).
Acclimatization can be achieved through up or down-regulation of key
processes used to obtain resources for growth or maintenance. In
Symbiodinium, this may include photosynthetic reaction centres
(Iglesias-Prieto and Trench, 1994; MacIntyre et al., 2002; Hennige et al.,
2009), pigment species and organisation (Suggett et al., 2007; Hennige
et al., 2009) and Rubisco content per cell (Sukenik et al., 1987; MacIntyre
et al., 2002). Host acclimatization may include regulating heterotrophic
feeding rates (Anthony, 2000; Anthony and Fabricius, 2000), UV or heat
protective compounds (Shick et al., 1996; Dunlap and Shick, 1998; Baird
et al., 2009) or respiration rates (Anthony and Hoegh-Guldberg, 2003).
Plasticity in coral morphology has also been noted under different
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S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
environmental conditions both at the colony (Anthony and HoeghGuldberg, 2003; Anthony et al., 2005) and corallite level (Todd et al., 2004;
Crabbe and Smith, 2006).
Given that environmental conditions in marginal systems are less than
optimal, it is expected that acclimatization would require considerable
resource allocation, which in turn will lower achievable productivity, and
ultimately growth (Dubinsky et al., 1984; Miller and Cruise, 1995; Mass
et al., 2007). This may be particularly important on marginal reefs, as
available resources may not be enough to compensate for the increased
demand that marginal environments impose upon many resident corals.
Equally, resources may only be obtainable by some coral species e.g. those
with the ability to heterotrophically feed on multiple size classes of
plankton (Clayton and Lasker, 1982; Houlbreque et al., 2004).
Adaptation is also important and can be a result of host or symbiont
competitive fitness, with specific genetic variants within or between
species specialising in growth conditions that differ from clear blue
waters. Selection for the symbiont is well documented along environmental gradients (LaJeunesse et al., 2004), as are responses to transient
stress events (Kinzie et al., 2001; Baker, 2003; Thornhill et al., 2006).
Similarly, coral assemblages in terms of species composition may
change as environmental conditions become less than optimum. An
example is the proliferation of heat tolerant corals in thermally extreme
(sometimes intertidal) environments, where environmental history of
individual coral species can moderate susceptibility to environmental
perturbations (Brown et al., 2000; Brown et al., 2002a; Middlebrook
et al., 2008). Additionally, a shift from branching and massive coral
communities to massive dominated communities in sub-optimal
environments may reflect an apparent greater tolerance of massive
corals to withstand environmental stress (West and Salm, 2003; Kenyon
et al., 2006).
Identifying patterns and processes of how coral communities respond
to environmental conditions has long been a goal in understanding
community response to predicted climate change (Hoegh-Guldberg,
1999; Pittock, 1999; Guinotte et al., 2003) and also to anthropogenic
stressors such as increased sedimentation and terrestrial runoff (Fabricius,
2005). One study in particular has predicted that marginal reef range will
substantially increase as a result of climate change leading to additional
areas of ‘borderline’ high temperature regimes (Guinotte et al., 2003),
which may even become ‘normality’ as aquatic environments rapidly
change (Guinotte et al., 2003); as such, many reef forming coral species
will be placed under potentially stressful growth conditions. Examining
corals within present-day marginal conditions is thus an important step in
determining how coral reef form and function will appear under future
climates. At present, such fundamental information is almost entirely
lacking. Fortunately, present-day environmental gradients including high
and low-latitude marginal systems provide a natural study ground for
corals' adaptive (and acclimatory) capacity.
Here, we examined 6 key coral species, Goniastrea aspera, Porites lutea,
Porites lobata, Porites cylindrica, Favites abdita and Acropora formosa
(see Veron, 2000), across an environmental gradient (five sites) within a
reef system in Indonesia. Coral distribution and abundance were
measured as well as fundamental properties relating to productivity and
metabolism. The identification of in hospite symbionts across the gradient
was also determined. The results are discussed in the context of (1) which
species are better suited to exist in sub-optimal (marginal) environments
and what mechanisms may facilitate this, and (2) whether certain
holobionts are ‘pre-adapted’ to survive predicted future climate change.
where environmental conditions are close to the expected ‘optimal’
average. The light-temperature environment was characterised in two
separate field seasons (July–August 2007; July–August 2008) using
HOBO temperature (°C) and light (lux) loggers (Onset, Massachusetts,
U.S.A). These loggers were deployed for 1-week periods at similar tidal
cycles (where low tide coincided with midday at all sites) to obtain
light-temperature minima and maxima. Loggers were de-fouled daily
by wiping the bio-film from the upper surface. Lux was used to assess
relative diurnal changes in light levels between sites. Since lux is a
measure of light weighted to a human perspective, HyperOCR
hyperspectral radiometers (Satlantic, Halifax, Canada) were consequently used to assess light quality at all sites in 2007.
A time-synched surface reference radiometer and an underwater
radiometer at 1 m (down-welling irradiance), were used to assess
wavelength specific light attenuation coefficients, Kd(λ), according to
Beer Lambert's Law from 400 to 700 nm for all sites (Eq. (1)) where E is
irradiance. 1 m was the maximum depth at marginal sites so Kd(λ) was
assessed between 0 and 1 m at all sites for consistency. Kd per site was
calculated from the average Kd(400–700 nm) (Eq. (2)), and then used to
calculate optical depth, ζ (dimensionless, Eq. (3)), to compare sites of
differing turbidity.
KdðλÞ = ½ lnðE1 m ÞðλÞ– lnðE0:1 m ÞðλÞ = 0:9 m
⌊
400
⌋
ð1Þ
Kd ðsiteÞ = ∑700 Kd ðλÞ = 300
ð2Þ
ζ = Kd ðsiteÞ⋅depth
ð3Þ
During 2008 data collection, Kd was assessed using a photosynthetically available radiation (PAR) sensor attached to a pulse amplitude
modulated fluorometer (Walz), where E in Eq. (1) represents PAR. The
Walz PAR sensor was calibrated against a Li-Cor quantum sensor. This
2. Methods
2.1. Sites along an environmental gradient
Five sites within the Wakatobi Marine National Park reef system
were selected to provide a range of conditions along an environmental
gradient from ‘optimal’ to marginal (Fig. 1, Table 1). Here, ‘optimal’ sites
refer to regional sites where coral abundance and diversity is high, and
Fig. 1. Map of study sites in the Wakatobi Marine National Park, S.E Sulawesi, Indonesia
with latitude and longitude degrees and minutes. Adapted from Hennige et al. (2008a).
Sites and numbered 1–5 from optimal to marginal; Site 1—Pak Kasims; 2—Sampela;
3—Loho; 4—Lamohasi; 5—Langeira.
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
145
Table 1
Summary table of all measured environmental characteristics of each site including diurnal temperature range (°C), turbidity (Kd (site)) and site latitude and longitude. Site
community data includes the number of species on 50 m line-intercept transects (at Pak Kasims and Sampela at 5 m, ± SE, n = 3) and 50 × 2 m belt transects (at Loho, Lamohasi and
Langeira at 1 m, ±SE, n = 3), and the target species identified. In hospite Symbiodinium clade identification was according to the large ribosomal subunit 28S, with independent
colony replicate number in parentheses. † indicates replicates taken from both 2007 and 2008. * represents results where P. lobata and P. lutea have been amalgamated to one species
(due to identification difficulty).
Site
Daily temperature
range °C (min–max)
Kd (site)
2007
2008
Pak Kasims
26.3–28.1
0.16
0.17 (0.01)
5 28′ 04.44″ S, 123 45′, 21.30″ E
34.3 (8.88)
Sampela
26.6–29.1
0.31
N/A
5 28′ 54.79″ S, 123 44′ 43.49″ E
32.5 (2.50)
Loho
24.2–28.6
1.19
0.31 (0.03)
5 32′ 49.13″ S, 123 52′ 19.50″ E
5.0 (1.15)
Lamohasi
24.8–29.4
N/A
3.82 (0.99)
5 32′ 43.62″ S, 123 51′ 43.37″ E
1.67* (0.33)
Langeira
24.6–33.6
1.34
N/A
5 28′ 29.79″ S, 123 42′ 04.86″ E
1 (0.00)
Site latitude
and longitude
was repeated at similar tidal states over sequential days to obtain an
average site Kd.
Sites were ranked according to light availability and diurnal
temperature ranges: increased marginality was characterised by
higher values of Kd (site) and by diurnal range (variability) of light
and temperature. Although water movement directly affects these
variables, Kd and diurnal range of light and temperature are
quantifiable and their impact upon coral survival has been documented in previous studies (Brown et al., 2000; Loya et al., 2001; West and
Salm, 2003). Following these criteria, Site 1 (Pak Kasims) and Site 2
(Sampela) were ‘optimal sites’ with relatively low turbidity (low site
Kd) and diurnal ranges (Table 1). Sites 1 and 2 were both regularly
subject to fast current and high winds. Maximum depth at Site 1 was
ca. 40 m and Site 2 was 15 m. Site 3 (Loho) was more turbid and was
situated adjacent to sea grass beds that bordered a mangrove system
(Fig. 1). Coral depth was ca. 1 m and corals were not exposed to direct
sunlight until midday due to the sheltered aspect of the west-facing
reef. Site 4 (Lamohasi) was a sheltered site ca. 1.5 m deep adjacent to
dense mangroves, and experienced fast tidal flow; this site was
periodically extremely turbid as a result of sediment export from the
mangroves during the tidal cycles. Site 5 (Langeira) was a highly
turbid environment (Table 1) situated directly in front of large
mangroves. Corals at this site were often in isolated pools, ca. 0.5 m
deep at low tide. Sites were thus ranked from optimal to marginal as:
Pak Kasims N Sampela N Loho N Lamohasi N Langeira (Table 1).
2.2. Coral species
Coral species G. aspera, P. lutea, P. lobata and F. abdita were chosen for
this study based on presence at more than one site. 50 m continuous
line-intercept transects (n = 3) were used to categorise the benthic
biota (and target coral species) at Pak Kasims and Sampela (at 5 m)
(Table 1) according to English et al. (1997). In marginal habitats where
coral populations were sporadic, 50 × 2 m belt transects (100 m2) were
used to assess coral presence. Size (maximum length) frequency
distribution of all identified corals in marginal habitats size was also
assessed.
G. aspera, P. lutea, P. lobata and F. abdita are cosmopolitan massive
coral species. G. aspera has been observed in marginal systems across
No. species on 50 m
transects
Target species
present
Symbiodinium
clade
A. formosa
F. abdita
G. aspera
P. cylindrica
P. lobata
P. lutea
A. formosa
F. abdita
P. cylindrica
P. lobata
P. lutea
F. abdita
G. aspera
P. lobata
P. lutea
F. abdita
G. aspera
P. lobata
P. lutea
G. aspera
C (2†)
–
C (2)
C (2†)
C (2)
C (5)
C (9)
–
C (1)
–
–
D (1)
D (4†)
C (4)
C (3)
–
D (1)
C (4)
C (1)
D (6†)
geographic regions (Brown et al., 2002b; Kai and Sakai, 2008). P. lutea
and P. lobata are two of the most abundant massive coral species in
Sulawesi across geographic regions (Holl, 1983; Hennige et al.,
2008a), and F. abdita is common in most reef environments, both
turbid and non-turbid (Holl, 1983; Veron, 2000). Both P. cylindrica and
A. formosa are branching species which can dominate on certain reefs.
2.3. Metabolic assessment
Triplicate fragments from each coral species (separate colonies)
were taken from a single optical depth within each site. Optical depths
varied between sites and sometimes species since sampling depended
upon available colonies. Fragments were returned to the shore-based
laboratory for photosynthesis (oxygen production) light response
curve and respiration rate measurements using a respirometer
constructed from a glass vessel with an integrated optode (Aanderaa,
Norway). The optode measured both the O2 concentration as well as
any temperature drift, and all data were logged at 5 s intervals to a PC
via Oxyview software (Aanderaa, Norway). A stir bar ensured constant
water mixing and thus comparable conditions throughout the vessel
and over the optode membrane. Initially, a respiration rate was
recorded for 20 min in dark conditions. An actinic light (tungsten
halogen) was subsequently used to illuminate the respirometer in
three steps, each lasting 20 min. Light levels were 100, 250 and
500 μmol photons m−2 s− 1. Oxygen drift per unit time was used to
calculate hourly rates of respiration (R, μmol O2 cm−2 h− 1), net
photosynthesis (PN, μmol O2 cm−2 h− 1) and gross photosynthesis
(PG, μmol O2 cm−2 h− 1 = PN − R).
Coral surface areas were quantified using the tin foil method (Marsh
1970) and Image Tool (UTHSCSA) to measure tin foil surface area. All rates
were additionally normalised to chlorophyll a content of the fragment,
which was calculated using methanol and a spectrophotometer in
accordance with Porra et al. (1989). During the 2007 field season,
chlorophyll a extracts (methanol) were processed in a FIRe fluorometer
and minimum fluorescence values (Fo) were recorded. These were later
converted to μg chl a ml− 1 by running a calibration curve with chlorophyll
a standards between the FIRe and a spectrophotometer. During the 2008
field season, chlorophyll a extracts were processed on site with an Ocean
Optics (2000+) spectrophotometer.
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S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
Oxygen production was not assessed on branching coral species
A. formosa and P. cylindrica since the unidirectional light source used
to assess photosynthesis could not illuminate all sides of the
branching fragments. Time between in situ sample collection and
experimentation was typically b1 h.
2.4. Daily productivity
Light response productivity rates as well as respiration rates were used
to estimate the daily (diel) gross productivity. The light dependency of
photosynthesis was assessed by fitting a modified model of Jassby and
Platt (1976) via least squares non-linear regression as outlined in Hennige
et al. (2008a) to determine maximum gross productivity PMAX
(μmol
G
O2 cm− 2 (or chl a− 1)s− 1), (Eq. (4)), where α (dimensionless) and E
describe light dependent photosynthesis and light applied to the fragment
(μmol photons m−2 s− 1). Prior to determining PMAX
, PG data were plotted
G
against applied E to confirm that PG response to E was consistent with that
of previously published coral photosynthesis (or electron transport rate)irradiance curves.
MAX
PG = PG
−½1−expð−α⋅E=PG
MAX
Þ
ð4Þ
In situ light intensity was recorded at all sites over 12 h light periods
(on 4 separate days) and applied to Eq. (4) to calculate in situ light
dependent rates of gross production per hour (μmol O2 cm−2 h− 1), PG(E).
For this, in situ light was converted from lux to μmol photons m−2 s− 1
according to Deitzer (1994) and further modified to account for spectral
discrepancies between the actinic light source used to measure
photosynthesis, and the in situ light spectra of corals at different sites
from knowledge of spectrally resolved absorbance, a* (following Suggett
et al., 2007).
400
a* =
∑ ðaðλÞEðλÞÞ
,
ð5Þ
700
400
∑ ðEðλÞÞ
700
where E is the amount of light (μmol photons m−2 s− 1) and a is the
absorbance of the coral determined via reflectance measurements
obtained using an Ocean Optics USB 2000+ spectrophotometer following
Enriquez et al. (2005). A dark chamber was used for all reflectance
measurements to prevent signal contamination. Blank measurements
(to account for signal scattering and skeletal transmission) were
subsequently obtained for each fragment after removing all coral tissue
in a weak bleach solution for 24 h. In situ spectral irradiance was obtained
using Satlantic radiometers (see above).
PG(E) was then weighted to the in situ light spectrum
a*ðinsituÞ
PG ðEÞ = PG ðEÞ⋅
a*ðlabÞ
ð6Þ
where ‘in situ’ and ‘lab’ refer to Eq. (5) using spectrally resolved values of
either the in situ or respirometer incident light (E). Daily gross production
(PG(D), μmol O2 cm−2 day− 1) was finally calculated from the integral of PG
(E) (μmol O2 cm−2 h− 1) throughout the diurnal period as Eq. (7) and the
assumption that under super-saturating light intensities, down-regulation
of photosynthesis did not occur, where t is hours.
Dawn
PGðDÞ = ∑ PG ðEÞ Δt
Dusk
ð7Þ
The daily respiration rate (R(D)) was calculated from the product of the
hourly respiration rate and the number of hours of daylight (n), (i.e. R·n),
to enable the comparison with PG(D) and also calculation of daily net
production, PN(D) (μmol O2 cm− 2 day− 1)=PG(D) +R(D).
2.5. Symbiodinium identification
After experimentation, coral fragments were placed in 2 ml vials with
96% ethanol and refrigerated for the subsequent genetic identification of
the Symbiodinium. DNA was isolated according to LaJeunesse et al. (2003)
using a Wizard isolation kit (Promega). The large ribosomal subunit (28S)
was amplified using previously developed primers 28Sforward and
28Sreverse following Baker (1999). The resulting PCR product was
enzymatically digested with HhaI and TaqI for 5 h at 37 °C and 65 °C,
respectively. The subsequent restriction fragments were separated by
electrophoresis on a 2% agarose gel for 1 h at 120 V and compared to the
patterns of known Symbiodinium types from clades A, B, C, and D.
3. Results
3.1. Site light quality and quantity
Down-welling light spectral quality varied between sites; spectra
from Pak Kasims and Sampela were similar, apart from increased red
light attenuation at Sampela (Fig. 2A). Loho exhibited increased
attenuation in the blue (ca. 400–500 nm) relative to Sampela and Pak
Kasims, while Langeira appeared to be heavily affected by photosynthetic matter in the water column, as indicated by the lack of downwelling irradiance at 1 m in the blue region (400–550 nm) and at the
chlorophyll peak at ca. 680 nm (Fig. 2B). Spectrally resolved light
attenuation coefficients, Kd(λ), calculated from the difference between
spectrally resolved light was similar (ca. 0.2) between 400 and 550 nm
for Sampela and Pak Kasims. Above 550 nm, Kd(λ) was higher at Sampela
than at Pak Kasims (Fig. 2C). In contrast, both Loho and Langeira had
variable Kd(λ) between 400 and 700 nm (Fig. 2D), which was often
double that of Sampela or Pak Kasims Kd(λ). Light quality at Lamohasi
(down-welling irradiance and Kd(λ), between 400 and 700 nm) was not
assessed and was assumed to be similar to that of the adjacent
mangrove fringing reef, Loho.
Spectrally averaged Kd(400–700) values calculated for Pak Kasims and
Sampela (Table 1) during 2007 were similar to those measured at these
sites previously; in 2005 (Hennige et al. 2008a) and also during 2008
(Table 1). However, since the sampling depth varied at all sites
(see Methods), Kd values (which were used to partially define site
marginality) cannot be used to directly compare the amount of light corals
received. Consequently, optical depths (see Methods) were used to
convey that marginal corals, which were 1 m deep, were often subjected
to higher (and more variable) light intensities than con-specific species on
optimal reefs.
3.2. Coral assemblages across environmental gradients
The total number of coral species decreased from optimal to
marginal reef sites (Table 1). Changes in species diversity were
accompanied by changes in morphological diversity: branching species
were only present at Pak Kasims and Sampela, and thus only massive
species were observed at Loho, Lamohasi and Langeira. Of the six species
examined here, only P. lobata, P. lutea, F. abdita and G. aspera were
present at more than 2 sites (Tables 1 and 2). The abundance of G. aspera
at optimal sites was relatively low; however, as conditions became more
marginal and the presence of other species decreased (Table 1), the
relative abundance of G. aspera increased (Table 2) from b1 colony per
50 m line-intercept transect to 26 over 100 m2 at Langeira, where
temperature and light levels were high. Similarly, the relative
abundance of P. lobata and F. abdita also generally increased along the
environmental gradient moving from optimal to marginal sites, but
were not represented at all marginal sites. In contrast, P. lutea abundance
decreased from optimal to marginal sites. Due to site profile limitations,
coral abundance was compared between transects 5 m deep at Pak
Kasims and Sampela, and at 1 m at the marginal sites (Table 1).
However, all six target species were present at both Pak Kasims and
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
147
Fig. 2. Down-welling light spectra (normalised to 1) at 1 m at (A) optimal sites Sampela and Pak Kasims, and (B) marginal sites at Loho and Langeira. Attenuation coefficients Kd(λ) between
0.1 m and 1 m from 400 to 700 nm at (C) Sampela and Pak Kasims, and (D) at Loho and Langeira. No data was available for Lamohasi, but both down-welling spectra and Kd(λ) for Lamohasi
were assumed to be similar to Loho, due to the proximity and similar mangrove-bordering properties of both sites.
Sampela at depths of up to 15 m (data not shown), and hence were not
limited to high light habitats. Size frequency data of marginal reef corals
(Fig. 3) demonstrates that the highest frequency of colonies (both G.
aspera and Porites sp.) were between 5 and 20 cm long. However,
colonies of both species were documented reaching sizes of 40–60 cm.
3.3. Metabolic assessment
Daily oxygen production was dissimilar between coral species at any
one optical depth (Fig. 4A). When all species data were combined
together, daily oxygen production did not display a significant trend
against optical depth. This was also true for PG(D) in each individual
species versus optical depth. However, when PG(D) was compared at
shallow optical depths within species (excluding the deepest optical
depth data) some species such as G. aspera and P. lutea increased PG(D) at
lower optical depths (higher light), while some (P. lobata) exhibited no
difference (Fig. 4A). Daily respiration data were similar to PG(D) data
(Fig. 4A,B) but variability between species and optical depths was
higher. Oxygen production and respiration were also normalised to
chlorophyll a content of the in hospite Symbiodinum and displayed
similar variability to results in Fig. 4 (data not shown). However, data
reported here was normalised to cm2 to account for host metabolism.
When daily respiration, R(D),was expressed as a ratio to daily gross
oxygen production (PG(D), Fig. 4C) no single trend was observed across
all species and sites. However, R(D):PG(D) increased with optical depth
for G. aspera when Lamohasi data (the deepest optical depth) was
omitted (Pearson correlation = 0.912, p b 0.005, n = 9, or 0.294,
p = 0.380, n = 12 including Lamohasi data points). Trends for both
P. lobata and P. lutea data appears consistent with G. aspera R(D):PG(D)
data when Lamohasi data were omitted, although including all data
points, trends were non-significant. Consequently, R(D):PG(D) does not
correlate with optical depth consistently (including all sites) across any
species examined here.
3.4. Symbiodinium community structure
A change in Symbiodinium community composition across environmental gradients was observed in the target coral species (Table 1). Type C
Symbiodinium was present in all coral colonies sampled at optimal sites
(Pak Kasims and Sampela). As sites became more marginal (Loho and
Lamohasi), Symbiodinium type D was identified in addition to type C, and
in the most marginal habitat (Langeira), only type D Symbiodinium was
noted (Table 1).
G. aspera was the only coral species observed across sites to have
different clades of Symbiodinium. In particular, clade C Symbiodinium
Table 2
The number of target species A. formosa, F. abdita, G. aspera, P. cylindrica, P. lobata and P. lutea on 50 m line-intercept transects (at Pak Kasims and Sampela at 5 m, ± SE, n = 3) and
50 × 2 m belt transects (at Loho, Lamohasi and Langeira at 1 m, ±SE, n = 3) across environmental gradients from optimal to marginal sites in descending order.
Site
Pak Kasims
Sampela
Loho
Lamohasi
Langeira
a
Species number
G. aspera
F. abdita
P. lobata
P. lutea
P. cylindrica
A. formosa
0.33 (0.27)
0.00
1.33 (0.88)
0.00
26.0 (4.00)
0.67
0.33
2.00
2.25
0.00
1.33 (0.67)
0.33 (0.27)
6.67 (3.72)
18.4 (3.75)a
0.00
18.7 (5.61)
11.7 (3.18)
4.00 (2.08)
0.00
0.00
9.67 (2.40)
1.33 (0.88)
0.00
0.00
0.00
1.33 (0.67)
0.33 (0.27)
0.00
0.00
0.00
(0.33)
(0.27)
(0.50)
(1.93)
This colony count represents both P. lobata and P. lutea numbers due to difficulty in species identification on snorkel transects in turbid waters.
148
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
Fig. 3. Size frequency distribution using maximum length and 5 cm bins of (A) G. aspera at marginal sites Langeira (white) and Loho (grey), and of (B) P. lutea and P. lobata at
Lamohasi (white) and Langeira (grey) from triplicate 50 × 2 m belt transects. Results from P. lutea and P. lobata have been combined in (B) as Porites.
was noted at Pak Kasims (the most optimal site), but at all other sites
where G. aspera samples were taken, clade D was recorded (Table 1).
Other target species observed at multiple sites were not found to contain
different algal clades. An additional but faint band was observed
following restriction fragment length polymorphism of G. aspera
Symbiodinium samples from Lamohasi. This additional banding pattern
matched the C clade identified in other samples and could indicate the
background presence of a C clade Symbiodinium, but this was not
quantified.
4. Discussion
4.1. Coral community structure across environmental gradients
Coral diversity and abundance decreased from optimal to marginal
environments in response to changes in light availability, temperature
(absolute levels and daily range) and turbidity (Bak and Meesters, 2000;
Vermeij and Bak, 2002; Schleyer and Celliers, 2003). Previous studies for
this region reported that percentage coral cover decreased from Pak
Kasims to Sampela (ca. 50 to 30%) (Hennige et al., 2008a), thus results
here were consistent with previous work. Additionally, the most
marginal site, Langeira, had very low total coral cover (ca. b5%),
which is consistent with previous high latitude reef studies (Harriott
and Banks, 2002; Perry and Larcombe, 2003). However, the factors that
account for decreased coral cover such as larval recruitment, turbidity,
temperature, aragonite saturation and competition (Harriott and Banks,
2002) will be unique to each reef system. Consequently, exceptions may
exist to the trend described here (and in cited research) of decreased
coral abundance and diversity as marginality increases.
The relative abundance of certain massive species increased from
optimal to marginal environments. In contrast, branching species were
not identified in marginal environments. Low profile (colonies which
extend horizontally as well as vertically, rather than just extend
vertically) massive coral species such as G. aspera dominated at the
most marginal site, presumably as a result of mechanical (stability) and
physiological limitations in branching (and other massive) species. Low
profile massive corals are structurally more stable than branching
species (Madin, 2005), and their presence in marginal habitats (and the
absence of branching species) may reflect seasonal occurrence of
hydrodynamic disturbance events unobserved in this investigation, or
the unsuitability of branching species in unstable substrate
environments.
4.2. Acclimatization and adaptation across environmental gradients
Clearly, factors for optimal growth, such as light and temperature are
much more variable in marginal environments (Table 1). Corals must
therefore continually invest in tracking the changing environment via
acclimatization or protection. As noted in previous studies on Symbiodinium acclimation (Iglesias-Prieto and Trench, 1994; Hennige et al., 2008b,
2009), energetic demands of repair following damage (light or temperature mediated) lead to ‘pre-emptive’ strategies to prevent damage
arising. In corals, both the host and the Symbiodinium need protection
under extreme environments, and certain coral hosts are able to produce
photo- or thermal-protective pigments and proteins to facilitate this
(Shick et al., 1996; Dunlap and Shick, 1998; Brown et al., 2002b; Baird et
al., 2009). However, the ability of the coral to synthesise such products are
species dependent adaptations. Heat shock proteins, which are likely a key
mechanism by which marginal corals protect themselves, have been
identified in G. aspera (Brown et al., 2002b), which may explain their
dominance in thermally marginal habitats such as Langeira. However,
these ‘pre-emptive’ strategies carry an energetic cost, and it is feasible that
faster growing branching species do not have the resources available for
such strategies or for repair following damage (compared to massive
species). Having such alternative strategies for competing in reef
environments is consistent with the theory of increased resilience in
slower growing massive species (as noted in Pacific corals) (Loya et al.,
2001; West and Salm, 2003; Kenyon et al., 2006), which are thus better
suited to acclimate to changes in environmental variables (Gates and
Edmunds, 1999).
Daily gross productivity, PG(D), was variable between and within coral
species across environmental gradients. Oxygen production would be
expected to increase with increased external light availability (Anthony
and Hoegh-Guldberg, 2003; Mass et al., 2007); however, this pattern was
not strictly observed in data here, suggesting that under more extreme
light environment ranges (marginal habitats discussed here), such a
relationship may not hold. Despite some coral species not conforming to
the expected trend of increased oxygen production with increased site
light availability, the expected trend was observed if Lamohasi data, which
was considered an outlier in all data comparisons here, was omitted.
Lamohasi was considered an outlier since data collected from this site
usually fell outside of trends observed at other sites. This may be due to
variability in site turbidity and seasonality not accounted for in this study,
as neighbouring site Loho (which was considered similar to Lamohasi)
displayed vastly different attenuation coefficients between two sampling
periods (Table 1). Additionally, Kd (site) or Kd(λ) values used in this
investigation do not inform of seasonal changes which may be important
when considering coral acclimatization and adaptation, since acclimatization can only occur within the confines of long term adaptations. The
differences in light quality at different sites may also partially explain
variable results. The down-welling irradiance at Langeira (Fig. 2) indicated
high re-suspension of sediment and possibly associated benthic algal
communities (Bak and Meesters, 2000). This would directly affect coral
Photosynthetically Useable Radiation, PUR (Kinzie and Hunter, 1987; Kirk,
1994; MacIntyre et al., 2002) and therefore how they were acclimatized to
optimise daily productivity.
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
Fig. 4. (A) Daily gross oxygen production, PG(D) (μmol O2 cm− 2 day− 1), (B) daily respiration, R(D) (μmol O2 cm− 2 day− 1) and (C) daily respiration: daily gross photosynthesis, R(D):PG(D) (dimensionless) (± SE from replicates n = 3) of target
species A. formosa, P. cylindrica, P. lobata, P. lutea, F. abdita and G. aspera against optical depth (dimensionless). Site names and Symbiodinium clades identified in coral samples are denoted on the right.
149
150
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
When daily respiration and productivity were expressed as a ratio,
R(D):PG(D), plots were heavily influenced by the relationship between
PG(D) and optical depth. No specific acclimatization strategies could be
concluded from variable respiration data other than that cnidarian hosts
have dissimilar acclimatization strategies. These strategies likely reflect
the compromise unique to each coral species in minimising respiratory
demand (Anthony and Hoegh-Guldberg, 2003) in energetically
demanding environments. Heterotrophy and sediment loading (leading
to sediment removal) can both affect respiration rates of the host
(Szmant-Froelich and Pilson, 1984; Rogers, 1990) and would both be
important in the marginal environments discussed here. The suspended
sediments at marginal sites may provide a food source for certain
species, as photosynthetically derived energy may not always be
enough to provide the entire energy requirement of a coral, especially
when mucus production may be large (for sediment removal) and cell
maintenance costs high (Crossland et al., 1980; Dubinsky et al., 1984;
Porter et al., 1984). The ability to up-regulate feeding rates in turbid
environments is thus a key acclimatization strategy (Anthony and
Fabricius, 2000) and would be typically accompanied by an increase in
respiration (Szmant-Froelich and Pilson, 1984).
However, sediment rejection or clearing from corals will also affect
respiration rates (Riegl and Branch, 1995) and is a function of coral
morphology, growth and behaviour (Rogers, 1990; Stafford-Smith, 1993).
Certain genera are known to be good tolerators of turbid conditions such as
Porites (Dikou and van Woesik, 2006), which could explain the presence of
P. lutea and lobata in marginal environments here. Additionally, Goniastrea
species have also been noted to have relatively high densities in turbid
environments (Dikou and van Woesik, 2006) indicating that they too can
tolerate turbid conditions (in addition to other marginal conditions).
Considering that increased sedimentation can increase or decrease
respiration dependent upon active sediment removal mechanisms or
decreased productivity (Rogers, 1990; Riegl and Branch, 1995), and that
potential heterotrophy can increase respiration (Szmant-Froelich and
Pilson, 1984), the variable respiration data across and within species is
likely a product of species-specific acclimatization abilities coupled with
non-linear environmental factors which can heavily influence respiration
rates.
4.3. Adaptive changes and life history
Symbiodinium community structure changed across the environmental gradient. Symbiodinium type at optimal sites was dominated by
clade C, whereas at more marginal sites (identified in Table 1) clade D
types were recorded, similar to findings in previous studies (Toller et al.,
2001; Sotka and Thacker, 2005; Lien et al., 2007; Mostafavi et al., 2007).
The presence of clade D in the most marginal environment where
temperatures reach 34 °C, and comparison with previous studies (Rowan,
2004; Mieog et al., 2007; Mostafavi et al., 2007; LaJeunesse et al., 2010),
infers that clade D here is thermally tolerant. However, not all D types of
Symbiodinium are necessarily thermally tolerant (Tchernov et al., 2004) as
Symbiodinium sub-clades may differ in a variety of ways as noted for other
clades of Symbiodinium (Hennige et al., 2009). The presence of clade D in
other marginal habitats where temperatures did not exceed 30 °C (during
the time of experimentation) indicates that thermal tolerance may not be
the only reason for corals harbouring clade D symbionts. A perhaps
equally important characteristic may be holobiont tolerance to the overall
temperature range and the rate of temperature change at a particular site.
Previous studies have speculated that clade D symbionts are suited to
low light environments (Ulstrup and van Oppen, 2003; Mostafavi et al.,
2007), which would correspond to the high turbidity associated with all
the marginal sites in this present work. However, the shallow depth of
Langeira and Loho negates any light reducing effect of turbid water and
consequently clade D symbionts were found in high light sites (Langeira
and Loho) in addition to low light sites (Lamohasi). Consequently, it seems
likely that clade D Symbiodinium may not be well adapted to just one set of
conditions, but may rather be a very resilient symbiont (Toller et al., 2001;
Mostafavi et al., 2007), which makes it ideal for marginal (and highly
variable) environments. However, it is important to note that both the
symbiont and host need tolerant properties to survive under marginal
conditions (Brown et al., 2002b; Fitt et al., 2009), and that hosting a
tolerant symbiont alone may not confer large advantages to a coral host
(Abrego et al., 2008).
The host-Symbiodinium specificity of target species here was
unknown but raises the interesting question as to whether certain
species only found at optimal sites, such as P. cylindrica and A. formosa,
can associate with clade D Symbiodinium found in other marginal coral
species. Porites don't often associate with clade D Symbiodinium despite
being one of the most tolerant corals worldwide (Baker et al., 2004; Stat
et al., 2009; LaJeunesse et al., 2010) but A. formosa is known to host clade
D Symbiodinium in addition to C (Huang et al., 2006). However,
LaJeunesse et al. (2010) observed no environmental influence on clade
D presence in Porites or Acropora in the Indo-Pacific.
Species in this study, such as G. aspera (which has also been recorded
as heat tolerant (Brown et al., 2002b)), which harboured a C clade at
optimal sites, and D clade at marginal sites may be pre-adapted to do
well under a variety of different environments. Given the presence of
background symbionts belonging to clade C in G. aspera, it is likely that
this host represents a polymorphic symbiosis capable of harbouring
more than one symbiont type (LaJeunesse, 2002; LaJeunesse et al., 2004;
Goulet, 2006).
Coral life history characteristics across environmental gradients may
partially explain the low abundance of ‘tolerant’ species at optimal sites;
where abundance of cosmopolitan corals P. lobata and G. aspera was
relatively low compared to A. formosa and P. cylindrica. Lower
abundance of the cosmopolitan species here may be dependent upon
recruit availability, which is directly impacted upon by the presence of
parent colonies, their size and their growth strategies. Branching species
are often considered to have high reproductive output in addition to fast
growth (McClanahan et al., 2007; Riegl and Purkis, 2009), and if it is
hypothesised that within reef recruitment is more important than
recruit supplies from neighbouring reefs, then high coral abundance or
dominance would inevitably ‘reinforce’ local populations. Species with
low abundance at these optimal sites (such as corals P. lobata and
G. aspera) may thus not increase in abundance unless some catastrophic
event removes dominant species (Connell, 1978).
Under marginal conditions, the relatively small diversity of corals
must be able to reproduce to be evolutionarily viable; either to fully
colonise such systems or to act as reef ‘refuges’ for certain species which
could potentially act to ‘re-seed’ optimal reefs following environmental
perturbations. The presence of P. lutea, P. lobata, F. abdita and G. aspera in
multiple size classes at marginal habitats indicates that past coral
recruitment was not an isolated event, as otherwise all present colonies
would have a similar size category (if growth variability between corals
of the same age is assumed to be relatively small compared to size
variability dictated by age of coral). However, the lack of corals under
5 cm may indicate that recruitment comes primarily from outside of the
marginal systems (separated by ca. 100–200 m from the marginal
habitats). Genetic analysis would be needed to confirm this. However,
reproductive strategies and larval recruitment ability (Hodgson, 1990;
Mundy and Babcock, 1998; Baird et al., 2003; Birrell et al., 2005) could
also be an adaptation to marginal environments, as genotypes that have
adapted to local conditions (such as high temperature, salinity and
sedimentation) will often dominate through asexual reproduction
(Adjeroud and Tsuchiya, 1999; Bak and Meesters, 2000; Nishikawa
and Sakai, 2005). Importantly reproduction is determined by coral age
and not by size in G. aspera (Kai and Sakai 2008), which may be
particularly relevant at marginal sites.
5. Conclusions
Change in coral community structure across environmental gradients
is likely sustained by long term evolutionary pressures upon the holobiont
S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152
to tolerate highly variable environments. Coral species colonising the
marginal habitats studied here were massive in their morphology,
cosmopolitan in their distribution and resilient to a high degree of
variability in factors which effect coral growth (light, temperature and
sediment loading). However, the reef framework that develops in
marginal habitats is more discontinuous than on optimal reefs. No
doubt this contributes to the functional role that corals play in these
(and therefore possible future) environments.
Corals found in the most marginal habitats explored here were also
associated with clade D Symbiodinium, which has been documented as
being a resilient symbiont under conditions which can be experienced in
marginal environments. Hosting clade D Symbiodinium likely increases
the fitness of corals in marginal environments. However, holobiont
respiration, and to a lesser degree, oxygen production was still variable
across environmental gradients, indicating that holobiont acclimatization strategies and adaptations are species specific and are responding to
a variety of factors such as changes in light availability, temperature and
turbidity to facilitate survival. Importantly, this plasticity between
species across energetically demanding environments demonstrates
how each coral has a trade-off between minimising energetic
expenditure while retaining adequate protection, maintenance and
repair capabilities. Consequently, not all corals can be considered equal.
As future climate change extends marginal reef range, branching coral
diversity may decrease in contrast to massive, more resilient corals. This
would have large-scale impacts upon (1) reef bio-diversity and ecosystem
services, and (2) reef metabolism and net reef accretion rates, since
massive species are typically slow growers. These marginal environments
thus represent useful systems to study now, to better understand reef
structure, functioning and accretion in the face of future climate change.
Acknowledgements
This work was funded through a National Environmental Research
Council (NERC) PhD studentship to SJH, a NERC fellowship to DJSu and by
Operation Wallacea through collaboration with the Wakatobi Taman
National. Also, thanks to the Wallacea Foundation, J. Jompa of the Centre of
Coral Reef Studies, Hasanuddin University, and the Indonesian Institute of
Sciences (LIPI). I am also grateful to Daniel Exton for assistance in
preparing the map for this manuscript. [SS]
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