Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

Contents lists available at ScienceDirect

Journal of Experimental Marine Biology and Ecology

j ourna l homepage: www.e lsev ie r.com/ locate / jembe

Acclimation and adaptation of scleractinian coral communities along environmentalgradients 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 Coral Reef Research Unit, Department of Biological Sciences, University of Essex, Colchester CO4 3SQ, United Kingdomb College of Earth, Ocean and Environment, University of Delaware, 700 Pilottown Road, Lewes, Delaware 19958, United States

⁎ Corresponding author.E-mail address: sjhenn@udel.edu (S.J. Hennige).

1 Present address: College of Earth, Ocean and Environ700 Pilottown Road, Lewes, Delaware 19958, United Sta

0022-0981/$ – see front matter © 2010 Elsevier B.V. Aldoi:10.1016/j.jembe.2010.06.019

a b s t r a c t

a r t i c l e i n f o

Article history:Received 5 March 2010Received in revised form 16 June 2010Accepted 17 June 2010

Keywords:AcclimationAdaptationEnvironmental gradientsMarginal reefsMassive coralsSymbiodinium

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. Thisgradient included ‘optimal’, intermediate and marginal sites, where conditions were close to the survivalthreshold limit for corals. Coral communities changed across this gradient from diverse, mixed growth formassemblages to specialised, massive growth form dominated communities. The massive coral Goniastrea asperawas the only species identified at the most marginal and optimal sites. Branching species Acropora formosa andPorites cylindrica were only identified at optimal sites. The in hospite Symbiodinium community also changedacross the environmental gradient frommembers of the Symbiodinium clade C onoptimal reefs (in branching andmassive species) to clade D on marginal reefs (in massive species). Substantial variability in respiration andphotosynthesiswas observed inmassive coral species under different environmental conditions, which suggeststhat all corals cannot be considered equal across environments. Studying present-day marginal environments iscrucial to further understanding of future reef bio-diversity, functioning and accretion, and fromwork presentedhere, it is likely that as future climate change extendsmarginal reef range, branching coral diversitymay decreaserelative to massive, more resilient corals.

ment, University of Delaware,tes.

l rights reserved.

© 2010 Elsevier B.V. All rights reserved.

1. Introduction

Scleractinian corals are often associated with clear blue water tropicalreefs, 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 andaragonite saturation states are often drastically higher or lower thanrequired for optimum growth (Rogers, 1990; Miller and Cruise, 1995;Guinotte et al., 2003). Consequently, scleractinian corals are pushed closeto the threshold required for net coral growth. Some of theseenvironmental conditions are associated with high latitude reefs, whichhave been termed marginal reefs (Celliers and Schleyer, 2002; Perry andLarcombe, 2003; Celliers and Schleyer, 2008). However, the criteria for areef tobe consideredmarginal (Kleypas et al., 1999) canalsobemet at lowlatitudes (Kleypas et al., 1999; Bak and Meesters, 2000; Guinotte et al.,2003), in particular, intertidal, fringing mangroves and terrestrial basin

areas (Rogers, 1990; Mitchell and Furnas, 1997; Anthony, 2000).Regardless of the location of thesemarginal reefs, coralsmust successfullyrespond to substantial variations (or gradients) in growth conditions inorder to successfully recruit and survive.

Successful colonisation (recruitment and growth) across environmen-tal gradients requires that both the symbiotic microalgae(Symbiodinium spp.) and the host coral optimise available resources,while retaining the physiological plasticity needed to survive underdifferent conditions. This trade-off can potentially be achieved throughcareful interplay between acclimatization and adaptation (Falkowski andLaRoche, 1991; Iglesias-Prieto and Trench, 1994; Hennige et al., 2009).Acclimatization can be achieved through up or down-regulation of keyprocesses used to obtain resources for growth or maintenance. InSymbiodinium, 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; Hennigeet al., 2009) and Rubisco content per cell (Sukenik et al., 1987; MacIntyreet al., 2002). Host acclimatization may include regulating heterotrophicfeeding rates (Anthony, 2000; Anthony and Fabricius, 2000), UV or heatprotective compounds (Shick et al., 1996; Dunlap and Shick, 1998; Bairdet al., 2009) or respiration rates (Anthony and Hoegh-Guldberg, 2003).Plasticity in coral morphology has also been noted under different

Fig. 1. Map of study sites in the Wakatobi Marine National Park, S.E Sulawesi, Indonesiawith 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.

144 S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

environmental conditions both at the colony (Anthony and Hoegh-Guldberg, 2003;Anthonyet al., 2005) andcorallite level (Toddet al., 2004;Crabbe and Smith, 2006).

Given that environmental conditions inmarginal systems are less thanoptimal, it is expected that acclimatization would require considerableresource allocation, which in turn will lower achievable productivity, andultimately growth (Dubinsky et al., 1984; Miller and Cruise, 1995; Masset al., 2007). This may be particularly important on marginal reefs, asavailable resources may not be enough to compensate for the increaseddemand that marginal environments impose upon many resident corals.Equally, resourcesmay only be obtainable by some coral species e.g. thosewith the ability to heterotrophically feed on multiple size classes ofplankton (Clayton and Lasker, 1982; Houlbreque et al., 2004).

Adaptation is also important and can be a result of host or symbiontcompetitive fitness, with specific genetic variants within or betweenspecies specialising in growth conditions that differ from clear bluewaters. Selection for the symbiont is well documented along environ-mental gradients (LaJeunesse et al., 2004), as are responses to transientstress events (Kinzie et al., 2001; Baker, 2003; Thornhill et al., 2006).Similarly, coral assemblages in terms of species composition maychange as environmental conditions become less than optimum. Anexample is the proliferation of heat tolerant corals in thermally extreme(sometimes intertidal) environments, where environmental history ofindividual coral species can moderate susceptibility to environmentalperturbations (Brown et al., 2000; Brown et al., 2002a; Middlebrooket al., 2008). Additionally, a shift from branching and massive coralcommunities to massive dominated communities in sub-optimalenvironments may reflect an apparent greater tolerance of massivecorals towithstandenvironmental stress (West and Salm,2003;Kenyonet al., 2006).

Identifying patterns and processes of how coral communities respondto environmental conditions has long been a goal in understandingcommunity response to predicted climate change (Hoegh-Guldberg,1999; Pittock, 1999; Guinotte et al., 2003) and also to anthropogenicstressors suchas increased sedimentation and terrestrial runoff (Fabricius,2005). One study in particular has predicted that marginal reef rangewillsubstantially increase as a result of climate change leading to additionalareas of ‘borderline’ high temperature regimes (Guinotte et al., 2003),which may even become ‘normality’ as aquatic environments rapidlychange (Guinotte et al., 2003); as such, many reef forming coral specieswill be placed under potentially stressful growth conditions. Examiningcoralswithinpresent-daymarginal conditions is thus an important step indetermining how coral reef form and function will appear under futureclimates. At present, such fundamental information is almost entirelylacking. Fortunately, present-day environmental gradients including highand low-latitude marginal systems provide a natural study ground forcorals' 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 areef system in Indonesia. Coral distribution and abundance weremeasured as well as fundamental properties relating to productivity andmetabolism. The identification of in hospite symbionts across the gradientwas also determined. The results are discussed in the context of (1)whichspecies are better suited to exist in sub-optimal (marginal) environmentsand what mechanisms may facilitate this, and (2) whether certainholobionts are ‘pre-adapted’ to survive predicted future climate change.

2. Methods

2.1. Sites along an environmental gradient

Five sites within the Wakatobi Marine National Park reef systemwere selected to provide a range of conditions along an environmentalgradient from ‘optimal’ tomarginal (Fig. 1, Table 1). Here, ‘optimal’ sitesrefer to regional sites where coral abundance and diversity is high, and

where environmental conditions are close to the expected ‘optimal’average. The light-temperature environment was characterised in twoseparate field seasons (July–August 2007; July–August 2008) usingHOBO temperature (°C) and light (lux) loggers (Onset, Massachusetts,U.S.A). These loggers were deployed for 1-week periods at similar tidalcycles (where low tide coincided with midday at all sites) to obtainlight-temperature minima and maxima. Loggers were de-fouled dailyby wiping the bio-film from the upper surface. Lux was used to assessrelative diurnal changes in light levels between sites. Since lux is ameasure of light weighted to a human perspective, HyperOCRhyperspectral radiometers (Satlantic, Halifax, Canada) were conse-quently used to assess light quality at all sites in 2007.

A time-synched surface reference radiometer and an underwaterradiometer at 1 m (down-welling irradiance), were used to assesswavelength specific light attenuation coefficients, Kd(λ), according toBeer Lambert's Law from 400 to 700 nm for all sites (Eq. (1)) where E isirradiance. 1 m was the maximum depth at marginal sites so Kd(λ) wasassessed between 0 and 1 m at all sites for consistency. Kd per site wascalculated from the average Kd(400–700nm) (Eq. (2)), and then used tocalculate optical depth, ζ (dimensionless, Eq. (3)), to compare sites ofdiffering turbidity.

KdðλÞ = ½ ln E1mð ÞðλÞ– ln E0:1mð ÞðλÞ�= 0:9m ð1Þ

Kd siteð Þ = ⌊∑400700 Kd λð Þ⌋= 300 ð2Þ

ζ = Kd siteð Þ⋅depth ð3Þ

During 2008 data collection, Kd was assessed using a photosynthet-ically available radiation (PAR) sensor attached to a pulse amplitudemodulated fluorometer (Walz), where E in Eq. (1) represents PAR. TheWalz PAR sensor was calibrated against a Li-Cor quantum sensor. This

Table 1Summary table of all measured environmental characteristics of each site including diurnal temperature range (°C), turbidity (Kd (site)) and site latitude and longitude. Sitecommunity 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 andLangeira 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 independentcolony 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 temperaturerange °C (min–max)

Kd (site) Site latitudeand longitude

No. species on 50 mtransects

Target speciespresent

Symbiodiniumclade

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) A. formosa C (2†)

F. abdita –

G. aspera C (2)

P. cylindrica C (2†)

P. lobata C (2)

P. lutea C (5)

Sampela 26.6–29.1 0.31 N/A 5 28′ 54.79″ S, 123 44′ 43.49″ E 32.5 (2.50) A. formosa C (9)

F. abdita –

P. cylindrica C (1)

P. lobata –

P. lutea –

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) F. abdita D (1)

G. aspera D (4†)

P. lobata C (4)

P. lutea C (3)

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) F. abdita –

G. aspera D (1)

P. lobata C (4)

P. lutea C (1)

Langeira 24.6–33.6 1.34 N/A 5 28′ 29.79″ S, 123 42′ 04.86″ E 1 (0.00) G. aspera D (6†)

145S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

was repeated at similar tidal states over sequential days to obtain anaverage site Kd.

Sites were ranked according to light availability and diurnaltemperature ranges: increased marginality was characterised byhigher values of Kd (site) and by diurnal range (variability) of lightand temperature. Although water movement directly affects thesevariables, Kd and diurnal range of light and temperature arequantifiable and their impact upon coral survival has been documen-ted in previous studies (Brown et al., 2000; Loya et al., 2001;West andSalm, 2003). Following these criteria, Site 1 (Pak Kasims) and Site 2(Sampela) were ‘optimal sites’ with relatively low turbidity (low siteKd) and diurnal ranges (Table 1). Sites 1 and 2 were both regularlysubject to fast current and high winds. Maximum depth at Site 1 wasca. 40 m and Site 2 was 15 m. Site 3 (Loho) was more turbid and wassituated adjacent to sea grass beds that bordered a mangrove system(Fig. 1). Coral depth was ca. 1 m and corals were not exposed to directsunlight until midday due to the sheltered aspect of the west-facingreef. Site 4 (Lamohasi) was a sheltered site ca. 1.5 m deep adjacent todense mangroves, and experienced fast tidal flow; this site wasperiodically extremely turbid as a result of sediment export from themangroves during the tidal cycles. Site 5 (Langeira) was a highlyturbid environment (Table 1) situated directly in front of largemangroves. Corals at this site were often in isolated pools, ca. 0.5 mdeep at low tide. Sites were thus ranked from optimal to marginal as:Pak KasimsNSampelaNLohoNLamohasiNLangeira (Table 1).

2.2. Coral species

Coral speciesG. aspera, P. lutea, P. lobata and F. abditawere chosen forthis study based on presence at more than one site. 50 m continuousline-intercept transects (n=3) were used to categorise the benthicbiota (and target coral species) at Pak Kasims and Sampela (at 5 m)(Table 1) according to English et al. (1997). In marginal habitats wherecoral populations were sporadic, 50×2 m belt transects (100 m2) wereused to assess coral presence. Size (maximum length) frequencydistribution of all identified corals in marginal habitats size was alsoassessed.

G. aspera, P. lutea, P. lobata and F. abdita are cosmopolitan massivecoral species. G. aspera has been observed in marginal systems across

geographic regions (Brown et al., 2002b; Kai and Sakai, 2008). P. luteaand P. lobata are two of the most abundant massive coral species inSulawesi across geographic regions (Holl, 1983; Hennige et al.,2008a), and F. abdita is common in most reef environments, bothturbid and non-turbid (Holl, 1983; Veron, 2000). Both P. cylindrica andA. 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 depthwithin each site. Optical depthsvaried between sites and sometimes species since sampling dependedupon available colonies. Fragments were returned to the shore-basedlaboratory for photosynthesis (oxygen production) light responsecurve and respiration rate measurements using a respirometerconstructed from a glass vessel with an integrated optode (Aanderaa,Norway). The optode measured both the O2 concentration as well asany temperature drift, and all data were logged at 5 s intervals to a PCvia Oxyview software (Aanderaa, Norway). A stir bar ensured constantwater mixing and thus comparable conditions throughout the vesseland over the optode membrane. Initially, a respiration rate wasrecorded for 20 min in dark conditions. An actinic light (tungstenhalogen) was subsequently used to illuminate the respirometer inthree steps, each lasting 20 min. Light levels were 100, 250 and500 μmol photons m−2 s−1. Oxygen drift per unit time was used tocalculate hourly rates of respiration (R, μmol O2 cm−2 h−1), netphotosynthesis (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 (Marsh1970) and ImageTool (UTHSCSA) tomeasure tin foil surface area. All rateswere additionally normalised to chlorophyll a content of the fragment,which was calculated using methanol and a spectrophotometer inaccordance with Porra et al. (1989). During the 2007 field season,chlorophyll a extracts (methanol) were processed in a FIRe fluorometerand minimum fluorescence values (Fo) were recorded. These were laterconverted to μgchlaml−1by runninga calibration curvewith chlorophylla standards between the FIRe and a spectrophotometer. During the 2008field season, chlorophyll a extracts were processed on site with an OceanOptics (2000+) spectrophotometer.

146 S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

Oxygen production was not assessed on branching coral speciesA. formosa and P. cylindrica since the unidirectional light source usedto assess photosynthesis could not illuminate all sides of thebranching fragments. Time between in situ sample collection andexperimentation was typically b1 h.

2.4. Daily productivity

Light responseproductivity rates aswell as respiration rateswereusedto estimate the daily (diel) gross productivity. The light dependency ofphotosynthesis was assessed by fitting a modified model of Jassby andPlatt (1976) via least squares non-linear regression as outlined inHennigeet al. (2008a) to determine maximum gross productivity PGMAX (μmolO2 cm−2 (or chl a−1)s−1), (Eq. (4)), where α (dimensionless) and Edescribe lightdependentphotosynthesis and light applied to the fragment(μmol photons m−2 s−1). Prior to determining PGMAX, PG datawere plottedagainst appliedE to confirm that PG response to Ewas consistentwith thatof previously published coral photosynthesis (or electron transport rate)-irradiance curves.

PG = PMAXG −½1−expð−α⋅E=PMAX

G 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 lightdependent rates of gross productionper hour (μmolO2 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 spectraldiscrepancies between the actinic light source used to measurephotosynthesis, and the in situ light spectra of corals at different sitesfrom knowledge of spectrally resolved absorbance, a* (following Suggettet al., 2007).

a* =∑400

700ðaðλÞEðλÞÞ

,∑400

700ðEðλÞÞ

ð5Þ

where E is the amount of light (μmol photons m−2 s−1) and a is theabsorbance of the coral determined via reflectance measurementsobtained using anOceanOptics USB 2000+spectrophotometer followingEnriquez et al. (2005). A dark chamber was used for all reflectancemeasurements to prevent signal contamination. Blank measurements(to account for signal scattering and skeletal transmission) weresubsequently obtained for each fragment after removing all coral tissuein aweak bleach solution for 24 h. In situ spectral irradiancewas obtainedusing Satlantic radiometers (see above).

PG(E) was then weighted to the in situ light spectrum

PGðEÞ� = PGðEÞ⋅a*ðinsituÞ�

a*ðlabÞð6Þ

where ‘in situ’ and ‘lab’ refer to Eq. (5) using spectrally resolved values ofeither the in situ or respirometer incident light (E). Daily gross production(PG(D), μmolO2 cm−2 day−1)wasfinally calculated fromthe integral of PG(E) (μmol O2 cm−2 h−1) throughout the diurnal period as Eq. (7) and theassumption thatunder super-saturating light intensities, down-regulationof photosynthesis did not occur, where t is hours.

PG Dð Þ = ∑Dawn

DuskPG Eð Þ Δt ð7Þ

Thedaily respiration rate (R(D))was calculated from theproduct of thehourly 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 netproduction, 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 with96% ethanol and refrigerated for the subsequent genetic identification ofthe Symbiodinium. DNAwas isolated according to LaJeunesse et al. (2003)using aWizard isolation kit (Promega). The large ribosomal subunit (28S)was amplified using previously developed primers 28Sforward and28Sreverse following Baker (1999). The resulting PCR product wasenzymatically digested with HhaI and TaqI for 5 h at 37 °C and 65 °C,respectively. The subsequent restriction fragments were separated byelectrophoresis on a 2% agarose gel for 1 h at 120 V and compared to thepatterns 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; spectrafrom Pak Kasims and Sampela were similar, apart from increased redlight attenuation at Sampela (Fig. 2A). Loho exhibited increasedattenuation in the blue (ca. 400–500 nm) relative to Sampela and PakKasims, while Langeira appeared to be heavily affected by photosyn-thetic matter in the water column, as indicated by the lack of down-welling irradiance at 1 m in the blue region (400–550 nm) and at thechlorophyll peak at ca. 680 nm (Fig. 2B). Spectrally resolved lightattenuation coefficients, Kd(λ), calculated from the difference betweenspectrally resolved light was similar (ca. 0.2) between 400 and 550 nmfor Sampela andPakKasims. Above550 nm,Kd(λ)washigher at Sampelathan at Pak Kasims (Fig. 2C). In contrast, both Loho and Langeira hadvariable Kd(λ) between 400 and 700 nm (Fig. 2D), which was oftendouble that of Sampela or Pak Kasims Kd(λ). Light quality at Lamohasi(down-welling irradiance and Kd(λ), between 400 and 700 nm)was notassessed and was assumed to be similar to that of the adjacentmangrove fringing reef, Loho.

Spectrally averaged Kd(400–700) values calculated for Pak Kasims andSampela (Table 1) during 2007 were similar to those measured at thesesites 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 sitemarginality) cannot be used to directly compare the amountof light coralsreceived. Consequently, optical depths (see Methods) were used toconvey that marginal corals, which were 1 m deep, were often subjectedtohigher (andmorevariable) light intensities than con-specific species onoptimal reefs.

3.2. Coral assemblages across environmental gradients

The total number of coral species decreased from optimal tomarginal reef sites (Table 1). Changes in species diversity wereaccompanied by changes in morphological diversity: branching specieswere only present at Pak Kasims and Sampela, and thus only massivespecieswere observed at Loho, Lamohasi and Langeira.Of the six speciesexamined here, only P. lobata, P. lutea, F. abdita and G. aspera werepresent atmore than 2 sites (Tables 1 and 2). The abundance ofG. asperaat optimal siteswas relatively low; however, as conditionsbecamemoremarginal and the presence of other species decreased (Table 1), therelative abundance of G. aspera increased (Table 2) from b1 colony per50 m line-intercept transect to 26 over 100 m2 at Langeira, wheretemperature and light levels were high. Similarly, the relativeabundance of P. lobata and F. abdita also generally increased along theenvironmental gradient moving from optimal to marginal sites, butwerenot represented at allmarginal sites. In contrast, P. luteaabundancedecreased from optimal tomarginal sites. Due to site profile limitations,coral abundance was compared between transects 5 m deep at PakKasims and Sampela, and at 1 m at the marginal sites (Table 1).However, all six target species were present at both Pak Kasims and

Fig. 2.Down-welling light spectra (normalised to1) at1 mat (A) optimal sites Sampela andPakKasims, and (B)marginal sites at Loho and Langeira. Attenuation coefficientsKd(λ) between0.1 mand1 m from400 to 700 nmat (C) Sampela and PakKasims, and (D) at Loho and Langeira.Nodatawas available for Lamohasi, but bothdown-welling spectra andKd(λ) for Lamohasiwere assumed to be similar to Loho, due to the proximity and similar mangrove-bordering properties of both sites.

147S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

Sampela at depths of up to 15 m (data not shown), and hence were notlimited to high light habitats. Size frequency data ofmarginal 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 productionwas dissimilar between coral species at anyone optical depth (Fig. 4A). When all species data were combinedtogether, daily oxygen production did not display a significant trendagainst optical depth. This was also true for PG(D) in each individualspecies versus optical depth. However, when PG(D) was compared atshallow optical depths within species (excluding the deepest opticaldepth data) some species such asG. aspera and P. lutea increased PG(D) atlower optical depths (higher light), while some (P. lobata) exhibited nodifference (Fig. 4A). Daily respiration data were similar to PG(D) data(Fig. 4A,B) but variability between species and optical depths washigher. Oxygen production and respiration were also normalised tochlorophyll a content of the in hospite Symbiodinum and displayedsimilar variability to results in Fig. 4 (data not shown). However, datareported here was normalised to cm2 to account for host metabolism.

Table 2The number of target species A. formosa, F. abdita, G. aspera, P. cylindrica, P. lobata and P. lute50×2 m belt transects (at Loho, Lamohasi and Langeira at 1 m, ±SE, n=3) across environ

Site Species number

G. aspera F. abdita P. lobata

Pak Kasims 0.33 (0.27) 0.67 (0.33) 1.33 (0.Sampela 0.00 0.33 (0.27) 0.33 (0.Loho 1.33 (0.88) 2.00 (0.50) 6.67 (3.Lamohasi 0.00 2.25 (1.93) 18.4 (3.7Langeira 26.0 (4.00) 0.00 0.00

a This colony count represents both P. lobata and P. lutea numbers due to difficulty in sp

When daily respiration, R(D),was expressed as a ratio to daily grossoxygen production (PG(D), Fig. 4C) no single trend was observed acrossall species and sites. However, R(D):PG(D) increased with optical depthfor G. aspera when Lamohasi data (the deepest optical depth) wasomitted (Pearson correlation=0.912, pb0.005, n=9, or 0.294,p=0.380, n=12 including Lamohasi data points). Trends for bothP. lobata and P. lutea data appears consistent with G. aspera R(D):PG(D)data when Lamohasi data were omitted, although including all datapoints, trends were non-significant. Consequently, R(D):PG(D) does notcorrelate with optical depth consistently (including all sites) across anyspecies examined here.

3.4. Symbiodinium community structure

A change in Symbiodinium community composition across environ-mental gradientswasobserved in the target coral species (Table1). TypeCSymbiodinium was present in all coral colonies sampled at optimal sites(Pak Kasims and Sampela). As sites became more marginal (Loho andLamohasi), Symbiodinium type Dwas identified in addition to type C, andin the most marginal habitat (Langeira), only type D Symbiodinium wasnoted (Table 1).

G. aspera was the only coral species observed across sites to havedifferent clades of Symbiodinium. In particular, clade C Symbiodinium

a on 50 m line-intercept transects (at Pak Kasims and Sampela at 5 m, ±SE, n=3) andmental gradients from optimal to marginal sites in descending order.

P. lutea P. cylindrica A. formosa

67) 18.7 (5.61) 9.67 (2.40) 1.33 (0.67)27) 11.7 (3.18) 1.33 (0.88) 0.33 (0.27)72) 4.00 (2.08) 0.00 0.005)a 0.00 0.00 0.00

0.00 0.00 0.00

ecies identification on snorkel transects in turbid waters.

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 atLamohasi (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.

148 S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

was noted at Pak Kasims (the most optimal site), but at all other siteswhere G. aspera samples were taken, clade D was recorded (Table 1).Other target species observedatmultiple siteswerenot found to containdifferent algal clades. An additional but faint band was observedfollowing restriction fragment length polymorphism of G. asperaSymbiodinium samples from Lamohasi. This additional banding patternmatched the C clade identified in other samples and could indicate thebackground presence of a C clade Symbiodinium, but this was notquantified.

4. Discussion

4.1. Coral community structure across environmental gradients

Coral diversity and abundance decreased from optimal to marginalenvironments in response to changes in light availability, temperature(absolute levels and daily range) and turbidity (Bak andMeesters, 2000;Vermeij and Bak, 2002; Schleyer and Celliers, 2003). Previous studies forthis region reported that percentage coral cover decreased from PakKasims to Sampela (ca. 50 to 30%) (Hennige et al., 2008a), thus resultshere were consistent with previous work. Additionally, the mostmarginal site, Langeira, had very low total coral cover (ca. b5%),which is consistent with previous high latitude reef studies (Harriottand Banks, 2002; Perry and Larcombe, 2003). However, the factors thataccount 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, exceptionsmayexist to the trend described here (and in cited research) of decreasedcoral abundance and diversity as marginality increases.

The relative abundance of certain massive species increased fromoptimal to marginal environments. In contrast, branching species werenot identified in marginal environments. Low profile (colonies whichextend horizontally as well as vertically, rather than just extendvertically) massive coral species such as G. aspera dominated at themost marginal site, presumably as a result of mechanical (stability) andphysiological limitations in branching (and othermassive) species. Lowprofile massive corals are structurally more stable than branchingspecies (Madin, 2005), and their presence inmarginal habitats (and theabsence of branching species) may reflect seasonal occurrence ofhydrodynamic disturbance events unobserved in this investigation, orthe unsuitability of branching species in unstable substrateenvironments.

4.2. Acclimatization and adaptation across environmental gradients

Clearly, factors for optimal growth, such as light and temperature aremuch more variable in marginal environments (Table 1). Corals musttherefore continually invest in tracking the changing environment via

acclimatization or protection. As noted in previous studies on Symbiodi-nium acclimation (Iglesias-Prieto and Trench, 1994; Hennige et al., 2008b,2009), energetic demands of repair following damage (light or temper-ature mediated) lead to ‘pre-emptive’ strategies to prevent damagearising. In corals, both the host and the Symbiodinium need protectionunder extreme environments, and certain coral hosts are able to producephoto- or thermal-protective pigments and proteins to facilitate this(Shick et al., 1996; Dunlap and Shick, 1998; Brown et al., 2002b; Baird etal., 2009). However, the ability of the coral to synthesise suchproducts arespeciesdependent adaptations.Heat shockproteins,whichare likely akeymechanism by which marginal corals protect themselves, have beenidentified in G. aspera (Brown et al., 2002b), which may explain theirdominance in thermally marginal habitats such as Langeira. However,these ‘pre-emptive’ strategies carry an energetic cost, and it is feasible thatfaster growing branching species do not have the resources available forsuch strategies or for repair following damage (compared to massivespecies). Having such alternative strategies for competing in reefenvironments is consistent with the theory of increased resilience inslower growing massive species (as noted in Pacific corals) (Loya et al.,2001; West and Salm, 2003; Kenyon et al., 2006), which are thus bettersuited to acclimate to changes in environmental variables (Gates andEdmunds, 1999).

Daily gross productivity, PG(D), was variable between andwithin coralspecies across environmental gradients. Oxygen production would beexpected to increase with increased external light availability (Anthonyand Hoegh-Guldberg, 2003;Mass et al., 2007); however, this patternwasnot strictly observed in data here, suggesting that under more extremelight environment ranges (marginal habitats discussed here), such arelationship may not hold. Despite some coral species not conforming tothe expected trend of increased oxygen production with increased sitelight availability, the expected trendwasobserved if Lamohasi data,whichwas considered an outlier in all data comparisons here, was omitted.Lamohasi was considered an outlier since data collected from this siteusually fell outside of trends observed at other sites. This may be due tovariability 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 samplingperiods (Table 1). Additionally, Kd (site) or Kd(λ) values used in thisinvestigation do not inform of seasonal changes whichmay be importantwhen considering coral acclimatization and adaptation, since acclimati-zation can only occur within the confines of long term adaptations. Thedifferences in light quality at different sites may also partially explainvariable results. Thedown-welling irradianceat Langeira (Fig. 2) indicatedhigh re-suspension of sediment and possibly associated benthic algalcommunities (Bak and Meesters, 2000). This would directly affect coralPhotosyntheticallyUseableRadiation, PUR (Kinzie andHunter, 1987;Kirk,1994;MacIntyre et al., 2002) and thereforehowtheywere acclimatized tooptimise daily productivity.

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 targetspecies 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.

149S.J.H

ennigeet

al./Journal

ofExperim

entalMarine

Biologyand

Ecology391

(2010)143

–152

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 betweenPG(D) and optical depth. No specific acclimatization strategies could beconcluded fromvariable respiration data other than that cnidarian hostshave dissimilar acclimatization strategies. These strategies likely reflectthe compromise unique to each coral species in minimising respiratorydemand (Anthony and Hoegh-Guldberg, 2003) in energeticallydemanding environments.Heterotrophy and sediment loading (leadingto sediment removal) can both affect respiration rates of the host(Szmant-Froelich and Pilson, 1984; Rogers, 1990) and would both beimportant in themarginal environments discussed here. The suspendedsediments at marginal sites may provide a food source for certainspecies, as photosynthetically derived energy may not always beenough to provide the entire energy requirement of a coral, especiallywhen mucus production may be large (for sediment removal) and cellmaintenance costs high (Crossland et al., 1980; Dubinsky et al., 1984;Porter et al., 1984). The ability to up-regulate feeding rates in turbidenvironments is thus a key acclimatization strategy (Anthony andFabricius, 2000) and would be typically accompanied by an increase inrespiration (Szmant-Froelich and Pilson, 1984).

However, sediment rejection or clearing from corals will also affectrespiration rates (Riegl and Branch, 1995) and is a function of coralmorphology, growth and behaviour (Rogers, 1990; Stafford-Smith, 1993).Certaingeneraareknowntobegood toleratorsof turbid conditions suchasPorites (DikouandvanWoesik, 2006),whichcouldexplain thepresenceofP. lutea and lobata inmarginal environmentshere. Additionally,Goniastreaspecies have also been noted to have relatively high densities in turbidenvironments (Dikou and vanWoesik, 2006) indicating that they too cantolerate turbid conditions (in addition to other marginal conditions).Considering that increased sedimentation can increase or decreaserespiration dependent upon active sediment removal mechanisms ordecreased productivity (Rogers, 1990; Riegl and Branch, 1995), and thatpotential heterotrophy can increase respiration (Szmant-Froelich andPilson, 1984), the variable respiration data across and within species islikely a product of species-specific acclimatization abilities coupled withnon-linear environmental factors which can heavily influence respirationrates.

4.3. Adaptive changes and life history

Symbiodinium community structure changed across the environ-mental gradient. Symbiodinium type at optimal sites was dominated byclade C, whereas at more marginal sites (identified in Table 1) clade Dtypeswere 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 wheretemperatures reach 34 °C, and comparisonwith 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 ofSymbiodinium are necessarily thermally tolerant (Tchernov et al., 2004) asSymbiodinium sub-cladesmaydiffer in a variety ofways as noted for otherclades of Symbiodinium (Hennige et al., 2009). The presence of clade D inothermarginal habitatswhere temperatures did not exceed30 °C (duringthe time of experimentation) indicates that thermal tolerancemay not bethe only reason for corals harbouring clade D symbionts. A perhapsequally important characteristicmay be holobiont tolerance to the overalltemperature range and the rate of temperature change at a particular site.

Previous studies have speculated that clade D symbionts are suited tolow light environments (Ulstrup and van Oppen, 2003; Mostafavi et al.,2007), which would correspond to the high turbidity associated with allthe marginal sites in this present work. However, the shallow depth ofLangeira and Loho negates any light reducing effect of turbid water andconsequently clade D symbionts were found in high light sites (LangeiraandLoho) inaddition to low light sites (Lamohasi). Consequently, it seemslikely that cladeD Symbiodiniummaynotbewell adapted to just one set ofconditions, butmay rather be a very resilient symbiont (Toller et al., 2001;

Mostafavi et al., 2007), which makes it ideal for marginal (and highlyvariable) environments. However, it is important to note that both thesymbiont and host need tolerant properties to survive under marginalconditions (Brown et al., 2002b; Fitt et al., 2009), and that hosting atolerant symbiont alone may not confer large advantages to a coral host(Abrego et al., 2008).

The host-Symbiodinium specificity of target species here wasunknown but raises the interesting question as to whether certainspecies only found at optimal sites, such as P. cylindrica and A. formosa,can associate with clade D Symbiodinium found in other marginal coralspecies. Porites don't often associate with clade D Symbiodinium despitebeing one of themost tolerant corals worldwide (Baker et al., 2004; Statet al., 2009; LaJeunesse et al., 2010) butA. formosa is known tohost cladeD Symbiodinium in addition to C (Huang et al., 2006). However,LaJeunesse et al. (2010) observed no environmental influence on cladeD presence in Porites or Acropora in the Indo-Pacific.

Species in this study, such asG. aspera (whichhas also been recordedas heat tolerant (Brown et al., 2002b)), which harboured a C clade atoptimal sites, and D clade at marginal sites may be pre-adapted to dowell under a variety of different environments. Given the presence ofbackground symbionts belonging to clade C in G. aspera, it is likely thatthis host represents a polymorphic symbiosis capable of harbouringmore thanone symbiont type (LaJeunesse, 2002; LaJeunesse et al., 2004;Goulet, 2006).

Coral life history characteristics across environmental gradientsmaypartially explain the low abundance of ‘tolerant’ species at optimal sites;where abundance of cosmopolitan corals P. lobata and G. aspera wasrelatively low compared to A. formosa and P. cylindrica. Lowerabundance of the cosmopolitan species here may be dependent uponrecruit availability, which is directly impacted upon by the presence ofparent colonies, their size and their growth strategies. Branching speciesare often considered to havehigh reproductive output in addition to fastgrowth (McClanahan et al., 2007; Riegl and Purkis, 2009), and if it ishypothesised that within reef recruitment is more important thanrecruit supplies from neighbouring reefs, then high coral abundance ordominance would inevitably ‘reinforce’ local populations. Species withlow abundance at these optimal sites (such as corals P. lobata andG. aspera)may thus not increase in abundance unless some catastrophicevent removes dominant species (Connell, 1978).

Under marginal conditions, the relatively small diversity of coralsmust be able to reproduce to be evolutionarily viable; either to fullycolonise such systems or to act as reef ‘refuges’ for certain species whichcould potentially act to ‘re-seed’ optimal reefs following environmentalperturbations. Thepresence of P. lutea, P. lobata, F. abdita andG. aspera inmultiple size classes at marginal habitats indicates that past coralrecruitmentwas not an isolated event, as otherwise all present colonieswould have a similar size category (if growth variability between coralsof the same age is assumed to be relatively small compared to sizevariability dictated by age of coral). However, the lack of corals under5 cmmay indicate that recruitment comes primarily fromoutside of themarginal systems (separated by ca. 100–200 m from the marginalhabitats). 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) couldalso be an adaptation tomarginal environments, as genotypes that haveadapted to local conditions (such as high temperature, salinity andsedimentation) will often dominate through asexual reproduction(Adjeroud and Tsuchiya, 1999; Bak and Meesters, 2000; Nishikawaand Sakai, 2005). Importantly reproduction is determined by coral ageand not by size in G. aspera (Kai and Sakai 2008), which may beparticularly relevant at marginal sites.

5. Conclusions

Change in coral community structure across environmental gradientsis likely sustainedby long termevolutionarypressures upon theholobiont

151S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

to tolerate highly variable environments. Coral species colonising themarginal habitats studied here were massive in their morphology,cosmopolitan in their distribution and resilient to a high degree ofvariability in factors which effect coral growth (light, temperature andsediment loading). However, the reef framework that develops inmarginal habitats is more discontinuous than on optimal reefs. Nodoubt 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 alsoassociated with clade D Symbiodinium, which has been documented asbeinga resilient symbiontunder conditionswhichcanbeexperienced inmarginal environments. Hosting clade D Symbiodinium likely increasesthe fitness of corals in marginal environments. However, holobiontrespiration, and to a lesser degree, oxygen production was still variableacross environmental gradients, indicating that holobiont acclimatiza-tion strategies and adaptationsare species specific andare responding toa variety of factors such as changes in light availability, temperature andturbidity to facilitate survival. Importantly, this plasticity betweenspecies across energetically demanding environments demonstrateshow each coral has a trade-off between minimising energeticexpenditure while retaining adequate protection, maintenance andrepair capabilities. Consequently, not all corals can be considered equal.

As future climate change extendsmarginal reef range, branching coraldiversity may decrease in contrast to massive, more resilient corals. Thiswouldhave large-scale impacts upon (1) reef bio-diversity andecosystemservices, and (2) reef metabolism and net reef accretion rates, sincemassive species are typically slow growers. Thesemarginal environmentsthus represent useful systems to study now, to better understand reefstructure, functioning and accretion in the face of future climate change.

Acknowledgements

This work was funded through a National Environmental ResearchCouncil (NERC) PhD studentship to SJH, a NERC fellowship to DJSu and byOperation Wallacea through collaboration with the Wakatobi TamanNational. Also, thanks to theWallacea Foundation, J. Jompaof theCentreofCoral Reef Studies, Hasanuddin University, and the Indonesian Institute ofSciences (LIPI). I am also grateful to Daniel Exton for assistance inpreparing the map for this manuscript. [SS]

References

Abrego, D., Ulstrup, K.E., Willis, B.L., van Oppen, M.J.H., 2008. Species-specificinteractions between algal endosymbionts and coral hosts define their bleachingresponse to heat and light stress. Proc. R. Soc. B 275, 2273–2282.

Adjeroud, M., Tsuchiya, M., 1999. Genetic variation and clonal structure in thescleractinian coral Pocillopora damicornis in the Ryukyu Archipelago, southernJapan. Mar. Biol. 134, 753–760.

Anthony, K.R.N., 2000. Enhanced particle-feeding capacity of corals on turbid reefs(Great Barrier Reef, Australia). Coral Reefs 19, 59–67.

Anthony, K.R.N., Connolly, S.R., 2004. Environmental limits to growth: physiologicalniche boundaries of corals along turbidity-light gradients. Oecologia 141, 373–384.

Anthony, K.R.N., Fabricius, K.E., 2000. Shifting roles of heterotrophy and autotrophy incoral energetics under varying turbidity. J. Exp. Mar. Biol. Ecol. 252, 221–253.

Anthony, K.R.N., Hoegh-Guldberg, O., 2003. Variation in coral photosynthesis,respiration and growth characteristics in contrasting light microhabitats: ananalogue to plants in forest gaps and understoreys? Func. Ecol. 17, 246–259.

Anthony, K.R.N., Hoogenboom, M.O., Connolly, S.R., 2005. Adaptive variation in coralgeometry and optimization of internal colony light climates. Func. Ecol. 19, 17–26.

Baird, A.H., Babcock, R.C., Mundy, C.P., 2003. Habitat selection by larvae influences thedepth distribution of six common coral species. Mar. Ecol. Prog. Ser. 252, 289–293.

Baird, A.H., Bhagooli, R., Ralph, P.J., Takahashi, S., 2009. Coral bleaching: the role of thehost. Trends Ecol. Evol. 24, 16–20.

Bak, R.P.M., Meesters, E.H., 2000. Acclimatization/adaptation of coral reefs in a marginalenvironment. Proceedings 9th International Coral Reef Symposium.

Baker, A.C., 1999. The symbiosis ecology of reef-building corals. Ph.D. thesis. Univ. ofMiami.

Baker, A.C., 2003. Flexibility and specificity in coral-algal symbiosis: diversity, ecologyand biogeography of Symbiodinium. Annu. Rev. Ecol. Evol. Syst. 34, 661–689.

Baker, A.C., Starger, C.J., McClanahan, T.R., Glynn, P.W., 2004. Corals' adaptive responseto climate change. Nature 430, 741.

Birrell, C.L., McCook, L.J., Willis, B.L., 2005. Effects of algal turfs and sediment on coralsettlement. Mar. Pollut. Bull. 51, 408–414.

Brown, B.E., Dunne, R.P.,Warner,M.E., Ambarsari, I., Fitt,W.K., Gibb, S.W., Cummings, D.G.,2000. Damage and recovery of photosystem II during a manipulative bleachingexperiment on solar bleaching in the coral Goniastrea aspera. Mar. Ecol. Prog. Ser. 195,114–124.

Brown, B.E., Dunne, R.P., Goodson, M.S., Douglas, A.E., 2002a. Experience shapes thesusceptibility of a reef coral to bleaching. Coral Reefs 21, 119–126.

Brown, B.E., Downs, C.A., Dunne, R.P., Gibb, S.W., 2002b. Exploring the basis ofthermotolerance in the reef cobral Goniastrea aspera. Mar. Ecol. Prog. Ser. 242,119–129.

Celliers, L., Schleyer, M.H., 2002. Coral bleaching on high latitude reefs at Sodwana Bay,South Africa. Mar. Pollut. Bull. 44, 1380–1387.

Celliers, L., Schleyer, M.H., 2008. Coral community structure and risk assessment ofhigh-latitude reefs at high latitude reefs at Sodwana Bay, South Africa. Biodivers.Conserv. 17, 3097–3117.

Clayton, W.S., Lasker, H.R., 1982. Effects of light and dark treatments on feeding bythe reef coral Pocillopora damicornis (Linnaeus). J. Exp. Mar. Biol. Ecol. 63,269–279.

Connell, J.H., 1978. Diversity in tropical rain forests and coral reefs—high diversity oftrees and corals is maintained only in a non-equilibrium state. Science 199,1302–1310.

Crabbe, M.J.C., Smith, D.J., 2006. Modelling variations in corallite morphology of Galaxeafasicularis coral colonies with depth and light on coastal fringing reefs in theWakatobi Marine National Park (S.E Sulawesi, Indonesia) Comput. Biol. Chem. 30,155–159.

Crossland, C.J., Barned, D.J., Borowitzka, M.A., 1980. Diurnal lipid and mucus productionin the staghorn coral Acropora acuminata. Mar. Biol. 60, 81–90.

Deitzer, G., 1994. Spectral comparisons of sunlight and different lamps. In: Tibbitts, T.W.(Ed.), International lighting incontrolledenvironmentsworkshop,NASA-CP-95-3309,pp. 197–199.

Dikou, A., van Woesik, R., 2006. Survival under chronic stress from sediment load:spatial patterns of hard coral communities in the southern islands of Singapore.Mar. Pollut. Bull. 52, 1340–1354.

Dubinsky, Z., Falkowski, P.G., Porter, J.W., Muscatine, L., 1984. Absorption andutilization of radiant energy by light-adapted and shade-adapted colonies of thehermatypic coral Stylophora pistillata. Proc. R. Soc. Lond. B 222, 203–214.

Dunlap,W.C., Shick, J.M., 1998. Ultraviolet radiation-absorbingmycosporine-like aminoacids in coral reef organisms: a biochemical and environmental perspective.J. Phycol. 34, 418–430.

English, S., Wilkinson, C., Baker, V., 1997. Survey manual for marine resources.Australian Institute of Marine Sciences, Townsville, Australia.

Enriquez, S., Mendez, E.R., Iglesias-Prieto, R., 2005. Multiple scattering on coralskeletons enhances light absorption by symbiotic algae. Limnol. Oceanogr. 50,1025–1032.

Fabricius, K.E., 2005. Effects of terrestrial runoff on the ecology of corals and coral reefs:review and synthesis. Mar. Pollut. Bull. 50, 125–146.

Falkowski, P.G., LaRoche, J., 1991. Acclimation to spectral irradiance in algae. J. Phycol.27, 8–14.

Fitt, W.K., Gates, R.D., Hoegh-Guldberg, O., Bythell, J.C., Jatkar, A., Grottoli, A.G., Gomez,M., Fisher, P., LaJeunesse, T.C., Pantos, O., Iglesias-Prieto, R., Franklin, D.J., Rodrigues,L.J., Torregiani, J.M., vanWoesik, R., Lesser, M.P., 2009. Response of two Indo-Pacificcorals, Porites cylindrical and Stylophora pistillata to short-term thermal stress: thehost does matter in determining the tolerance of corals to bleaching. J. Exp. Mar.Biol. Ecol. 373, 102–110.

Gates, R.D., Edmunds, P.J., 1999. The physiological mechanisms of acclimatization intropical reef corals. Am. Zool. 39, 30–43.

Goulet, T.L., 2006.Most coralsmay not change their symbionts. Mar. Ecol. Prog. Ser. 321, 1–7.Guinotte, J.M., Buddemeier, R.W., Kleypas, J.A., 2003. Future coral reef habitat

marginality: temporal and spatial effects of climate change in the Pacific basin.Coral Reefs 22, 551–558.

Harriott, V.J., Banks, S.A., 2002. Latitudinal variation in coral communities in easternAustralia: a qualitative biophysical model of factors regulating coral reefs. CoralReefs 21, 83–94.

Hennige, S.J., Smith, D.J., Perkins, R., Consalvey, M., Paterson, D.M., Suggett, D.J., 2008a.Photoacclimation, growth and distribution of massive coral species in clear andturbid waters. Mar. Ecol. Prog. Ser. 369, 77–88.

Hennige, S.J., Suggett, D.J., Warner, M.E., McDougall, K.E., Smith, D.J., 2008b. Unravellingcoral photoacclimation: Symbiodinium strategy and host modification. Proceedingsof the 11th International Coral Reef Symposium. Ft. Lauderdale, Florida.

Hennige, S.J., Suggett, D.J., Warner, M.E., McDougall, K.E., Smith, D.J., 2009. Photobiologyof Symbiodinium revisited: bio-physical and bio-optical signatures. Coral Reefs 28,179–195.

Hodgson, G., 1990. Sediment and the settlement of larvae of the reef coral Pocilloporadamicornis. Coral Reefs 9, 41–43.

Hoegh-Guldberg, O., 1999. Climate change, coral bleaching and the future of the world'scoral reefs. Mar. Freshw. Res. 50, 839–866.

Holl, M., 1983. Zonation and Diversity of Scleractinia on Reefs off S.W. Sulawesi,Indonesia. Drukkery Kanters BV, Alblasserdam.

Houlbreque, F., Tambutte, E., Richard, C., Ferrier-Pages, C., 2004. Importanceof amicro-dietfor scleractinian corals. Mar. Ecol. Prog. Ser. 282, 151–160.

Huang, H., Dong, Z.J., Huang, L.M., Zhang, J.B., 2006. Restriction fragment lengthpolymorphism analysis of large subunit rDNA of symbiotic dinoflagellates fromscleractinian corals in the Zhubi Coral Reef of the Nansha Islands. J. Int. Plant. Biol.48, 148–152.

Iglesias-Prieto, R., Trench, R.K., 1994. Acclimation and adaptation to irradiance insymbiotic dinoflagellates. 1. Responses of the photosynthetic unit to changes inphoton flux-density. Mar. Ecol. Prog. Ser. 113, 163–175.

152 S.J. Hennige et al. / Journal of Experimental Marine Biology and Ecology 391 (2010) 143–152

Jassby, A.T., Platt, T., 1976. Mathematical formulation of the relationship betweenphotosynthesis and light for phytoplankton. Limnol. Oceanogr. 21, 540–547.

Kai, S., Sakai, K., 2008. Effect of colony size and age on resource allocation betweengrowth and reproduction in the corals Goniastrea aspera and Favites chinensis. Mar.Ecol. Prog. Ser. 354, 133–139.

Kenyon, J.C., Vroom, P.S., Page, K.N., Dunlap, M.J., Wilkinson, C.B., Aeby, G.S., 2006.Community structure of hermatypic corals at French frigate shoals, NorthwesternHawaiian Islands: capacity for resistance and resilience to selective stressors. Pac.Sci. 60, 153–175.

Kinzie, R.A., Hunter, T., 1987. Effect of light quality on photosynthesis of the reef coralMontipora-verrucosa. Mar. Biol. 94, 95–109.

Kinzie, R.A., Takayama, M., Santos, S.R., Coffroth, M.A., 2001. The adaptive bleachinghypothesis: experimental tests of critical assumptions. Biol. Bull. 200, 51–58.

Kirk, J.T.O., 1994. Light & Photosynthesis in Aquatic Ecosystems. Cambridge University Press.Kleypas, J.A., 1996. Coral reef development under naturally turbid conditions: fringing

reefs near Broad Sound, Australia. Coral Reefs 15, 153–167.Kleypas, J.A., McManus, J.W., Menez, L.A.B., 1999. Environmental limits to coral reef

development: where do we draw the line? Am. Zool. 39, 146–159.LaJeunesse, T.C., 2002. Diversity and community structure of symbiotic dinoflagellates

from Caribbean coral reefs. Mar. Biol. 141, 387–400.LaJeunesse, T.C., Loh, W.K.W., van Woesik, R., Hoegh-Guldberg, O., Schmidt, G.W., Fitt,

W.K., 2003. Low symbiont diversity in southern Great Barrier Reef corals, relative tothose of the Caribbean. Limnol. Oceanogr. 48, 2046–2054.

LaJeunesse, T.C., Bhagooli, R., Hidaka, M., DeVantier, L., Done, T., Schmidt, G.W., Fitt,W.K., Hoegh-Guldberg, O., 2004. Closely related Symbiodinium spp. differ inrelative dominance in coral reef host communities across environmental,latitudinal and biogeographic gradients. Mar. Ecol. Prog. Ser. 284, 147–161.

LaJeunesse, T.C., Pettay, D.T., Sampayo, E.M., Niphon, P., Brown, B., Obura, D.O., Hoegh-Guldberg, O., Fitt, W.K., 2010. Long-standing environmental conditions, geographicisolation and host-symbiont specificity influence the relative ecological dominance andgenetic diversification of coral endosymbionts in the genus Symbiodinium. J. Biogeogr 37,785–800.

Lien, Y.T., Nakano, Y., Plathong, S., Fukami, H., Wang, J.T., Chen, C.A., 2007. Occurrence ofthe putatively heat-tolerant Symbiodinium phylotype D in high-latitudinal outlyingcoral communities. Coral Reefs 26, 35–44.

Loya, Y., Sakai, K., Yamazato, K., Nakano, Y., Sambali, H., van Woesik, R., 2001. Coralbleaching: the winners and the losers. Ecol. Lett. 4, 122–131.

MacIntyre, H.L., Kana, T.M., Anning, T., Geider, R.J., 2002. Photoacclimation ofphotosynthesis irradiance response curves and photosynthetic pigments inmicroalgae and cyanobacteria. J. Phycol. 38, 17–38.

Madin, J.S., 2005. Mechanical limitations of reef corals during hydrodynamicdisturbances. Coral Reefs 24, 630–635.

Marsh, J.A., 1970. Primary productivity of reef-building calcareous red algae. Ecology51, 255–565.

Mass, T., Einbinder, S., Brokovich, E., Shashar, N., Vago, R., Erez, J., Dubinsky, Z., 2007.Photoacclimation of Stylophora pistillata to light extremes: metabolism andcalcification. Mar. Ecol. Prog. Ser. 334, 93–102.

McClanahan, T.R., Ateweberhan, M., Graham, N.A.J., Wilson, S.K., Ruiz Sebastian, C.,Guillaume, M.M.M., Bruggemann, J.H., 2007. Western Indian Ocean coralcommunities: bleaching responses and susceptibility to extinction. Mar. Ecol.Prog. Ser. 337, 1–13.

Middlebrook, R., Hoegh-Guldberg, O., Leggat,W., 2008. The effect of thermal history on thesusceptibility of reef-building corals to thermal stress. J. Exp. Biol. 211, 1050–1056.

Mieog, J.C., van Oppen, M.J.H., Cantin, N.E., Stam, W.T., Olsen, J.L., 2007. Real-time PCRreveals a high incidence of Symbiodinium clade D at low levels in four scleractiniancorals across the Great Barrier Reef: implications for symbiont shuffling. Coral Reefs26, 449–457.

Miller, R.L., Cruise, J.F., 1995. Effects of suspended sediments on coral growth—evidencefrom remote sensing and hydrologic modelling. Remote Sens. Environ. 53, 177–187.

Mitchell, A.W., Furnas, M.J., 1997. Terrestrial inputs of nutrients and suspendedsediments to the GBR lagoon. Proceedings: the Great Barrier Reef. Science, use andmanagement. Townsville 1, 59–71.

Mostafavi, P.G., Fatemi, S.M.R., Shahhosseiny, M.H., Hoegh-Guldberg, O., Loh, W.K.W.,2007. Predominance of clade D Symbiodinium in shallow-water reef-building coralsoff Kish and Larak Islands (Persian Gulf, Iran). Mar. Biol. 153, 25–34.

Mundy, C.N., Babcock, R.C., 1998. Role of light intensity and spectral quality in coralsettlement: implications for depth-dependent settlement? J. Exp. Mar. Biol. Ecol.223, 235–255.

Nishikawa, A., Sakai, K., 2005. Genetic connectivity of the scleractinian coral Goniastreaaspera around the Okinawa Islands. Coral Reefs 24, 318–323.

Perry, C.T., Larcombe, P., 2003. Marginal and non-reef building coral environments.Coral Reefs 22, 427–432.

Pittock, A.B., 1999. Coral reefs and environmental change: adaptation to what? Am.Zool. 39, 10–29.

Porra, R.J., Thompson, W.A., Kriedemann, P.E., 1989. Determination of accurateextinction coefficients and simultaneous-equations for assaying chlorophyll aand chlorophyll b extracted with 4 different solvents—verification of theconcentration of chlorophyll standards by atomic-absorption spectroscopy.Biochim. Biophys. Acta 975, 384–394.

Porter, J.W., Muscatine, L., Dubinsky, Z., Falkowski, P.G., 1984. Primary production andphotoadaptation in light-adapted and shade-adapted colonies of the symbioticcoral, Stylophora pistillata. Proc. R. Soc. Lond. B 222, 161–180.

Riegl, B., Branch, G.M., 1995. Effects of sediment on the energy budgets of fourscleractinian (Bourne 1990) and five alcyonacean (Lamouroux 1816) corals. J. Exp.Mar. Biol. Ecol. 186, 259–275.

Riegl, B.M., Purkis, S.J., 2009. Model of coral population response to acceleratedbleaching and mass mortality in a changing climate. Ecol. Model 220, 192–208.

Rogers, C.S., 1990. Responses of coral reefs and reef organisms to sedimentation. Mar.Ecol. Prog. Ser. 62, 185–202.

Rowan, R., 2004. Themal adaptation in reef coral symbionts. Nature 430, 742.Schleyer, M.H., Celliers, L., 2003. Coral dominance at the reef-sediment interface in

marginal coral communities in Sodwana Bay, South Africa. Mar. Freshw. Res. 54,967–972.

Shick, J.M., Lesser, M.P., Jokiel, P.L., 1996. Effects of ultraviolet radiation on corals andother coral reef organisms. Glob. Change Biol. 2, 527–545.

Sotka, E.E., Thacker, R.W., 2005. Do some corals like it hot? Trends Ecol. Evol. 20, 59–62.Stafford-Smith, M.G., 1993. Sediment-rejection efficiency of 22 species of Australian

scleractinian corals. Mar. Biol. 115, 229–243.Stat, M., Loh, W.K.W., LaJeunesse, T.C., Hoegh-Guldberg, O., Carter, D.A., 2009. Stability

of coral-endosymbiont associations during and after a thermal stress event in thesouthern Great Barrier Reef. Coral Reefs 28, 709–713.

Suggett, D.J., Le Floc'H, E., Harris, G.N., Leonardos, N., Geider, R.J., 2007. Differentstrategies of photoacclimation by two strains of Emiliania huxleyi (Haptophyta).J. Phycol. 43, 1209–1222.

Sukenik, A., Bennett, J., Falkowski, P.G., 1987. Light saturatedphotosynthesis—limitationbyelectron transport or carbon fixation. Biochim. Biophys. Acta 891, 205–215.

Szmant-Froelich, A., Pilson, M.E.Q., 1984. Effects of feeding frequency and symbiosiswith zooxanthellae on nitrogen-metabolism and respiration of the coral Astrangiadanae. Mar. Biol. 81, 153–162.

Tchernov, D., Gorbunov, M.Y., de Vargas, C., Yadav, S.N., Milligan, A.J., Haggblom, M.,Falkowski, P.G., 2004. Membrane lipids of symbiotic algae are diagnostic of sensitivityto thermal bleaching in corals. Proc. Natl Acad. Sci. USA 101, 13531–13535.

Thornhill, D.J., Fitt, W.K., Schmidt, G.W., 2006. Highly stable symbioses among westernAtlantic brroding corals. Coral Reefs 25, 515–519.

Todd, P.A., Ladle, R.J., Lewin-Koh, N.J.I., Chou, L.M., 2004. Genotype x environmentinteractions in transplanted clones of the massive coral Favia speciosa andDiploastrea heliopora. Mar. Ecol. Prog. Ser. 271, 167–182.

Toller, W.W., Rowan, R., Knowlton, N., 2001. Zooxanthellae of theMontastraea annularisspecies complex: patterns of distribution of four taxa of Symbiodinium on differentreefs and across depths. Biol. Bull. 210, 348–359.

Ulstrup, K.E., van Oppen, M.J.H., 2003. Geographic and habitat partitioning ofgenetically distinct zooxanthellae (Symbiodinium) in Acropora corals on the GreatBarrier Reef. Mol. Ecol. 12, 3477–3484.

Vermeij, M.J.A., Bak, R.P.M., 2002. How are coral populations structured by light?Marine light regimes and the distribution of Madracis. Mar. Ecol. Prog. Ser. 223,105–116.

Veron, J.E.N., 2000. Corals of the World. Australian Institute of Marine Science,Townsville, Australia.

West, J.M., Salm, R.V., 2003. Resistance and resilience to coral bleaching: implicationsfor coral reef conservation and management. Conserv. Biol. 17, 956–967.