Morphological Changes in Polyp Structure of Massive Coral Species in Clear and Turbid Waters

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Research from the tropical and subtropical waters of the world’s oceans.

Rafael J. Araújo, Assistant EditorBulletin of Marine ScienceRosenstiel School of Marine and Atmospheric Science4600 Rickenbacker CausewayMiami, Florida 33149-1031 [email protected]

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BULLETIN OF MARINE SCIENCE. 88(1):000–000. 2012http://dx.doi.org/10.5343/bms.2010.1086

1Bulletin of Marine Science© 2012 Rosenstiel School of Marine and Atmospheric Science of the University of Miami

MORPHOLOGICAL CHANGES IN POLYP STRUCTURE OF MASSIVE CORAL SPECIES IN CLEAR AND TURBID WATERS

C Pisapia, SJ Hennige, J Haapkylä, R Matteucci, and DJ Smith

ABSTRACT

We explored variations in polyp morphology of four ecologically important massive coral species, Porites lutea (Milne-Edwards and Haime, 1860), Diploastrea heliopora (Lamarck, 1816), Favia speciosa (Dana, 1846), and Favia matthaii (Vaughan, 1918), across a depth gradient and among sites of differing turbidity within the Wakatobi Marine National Park, Indonesia. Increased polyp area with decreased light availability was found in all target species except F. speciosa, whereas polyp density only varied across sites or depth in D. heliopora, P. lutea, and F. speciosa. Variability in polyp morphology may reflect both an optimization of light capture and an increase in heterotrophic efficiency of the host to compensate for decreased photosynthesis with depth. The morphological variability demonstrated in these key species, which acts to optimize environmental suitability, may be a crucial attribute that has contributed to the success and abundance of these species within the Wakatobi Marine National Park.

As the potential for environmental stress increases, it becomes increasingly im-portant to understand whether environmentally regulated coral morphological vari-ation, likely driven by phenotypic plasticity and/or genetic variability, plays a role in determining coral abundance across habitats. The present study focues on intraspe-cific morphological variation in massive scleractinian corals, which are a key compo-nent of many reefs worldwide (Kenyon et al. 2006, Hennige et al. 2008).

Light is a critical factor in the ecology, distribution, physiology, and morphology of these reef-building corals (Dubinsky and Stambler 2005), and affects several process-es, such as calcification rates (Foster 1977, Mass et al. 2007), settlement, and recruit-ment (Maida et al. 1994). It is known that symbiotic zooxanthellae, Symbiodinium, which reside within the gastrodermis of polyp tissue (Muscatine 1990), are capable of responding to changes in the light environment (Hennige et al. 2009). However, variation in the quantity of light received by a colony has consequences for both Symbiodinium and the host coral, which may be morphologically acclimated or adapted to maximize light collection (Foster 1977, Todd et al. 2001, 2004, Mass et al. 2007). Colony growth, morphology, and corallite structure are thus dependent upon incident light (Goreau 1959, Todd et al. 2004, Einbinder et al. 2009), which decreases with increasing depth, and is affected by water properties such as suspended sedi-ment that absorbs and scatters light (Rogers 1990). Hence, light (and the way that it is affected by water properties) is likely to be the primary factor affecting symbiotic scleractinian colony growth and morphology, and its attenuation can be measured with the vertical attenuation coefficient (Kd , Kirk 1994). Kd accounts first for the at-tenuation of light caused by the physical traits of water, then by other light-absorbing or scattering bodies like plankton and minerals. Acclimation and adaptation of corals

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to different site turbidities is crucial to facilitate survival, as coral energetic budgets are heavily affected by changes in downwelling irradiance (Anthony and Fabricius 2000). Corals under different conditions maintain a positive energy balance by pho-totrophic and heterotrophic acclimation, which are constrained in part by the host (Anthony and Fabricius 2000).

In the present study, we assessed the distribution and morphological adaptations of four coral species: Porites lutea (Milne-Edwards and Haime, 1860), Diploastrea heliopora (Lamarck, 1816), Favia speciosa (Dana, 1846), and Favia matthaii (Vaughan, 1918). These four species have been previously characterized in terms of growth and photophysiology (Hennige et al. 2008) across a depth gradient and between sites of differing turbidity, thus our focus was on morphological changes in polyp structure. Our goal was to assess whether all four massive species respond to decreasing light availability by increasing (retracted) polyp size, and whether the most abundant coral species exhibited the greatest change.

Methods

Study Sites.—Sites were located in the Wakatobi Marine National Park off Southeast Sulawesi, Indonesia. We selected three sites of differing turbidity and light availability, which have been described previously in terms of sedimentation and light attenuation by Crabbe and Smith (2005) and Hennige et al. (2008). Kd used in our study was reported by Hennige et al. (2008), where light (Photosynthetically Available Radiation, PAR) was recorded between 0 and 13 m with a submersible PAR sensor (Walz) in June–August 2007 and need to calculate Kd using Beer-Lambert’s Law (see Kirk 1994, Hennige et al. 2008). Site 1, Sampela, was a rela-tively turbid and degraded reef adjacent to a local Bajo community (Kd (PAR) = 0.20 ± 0.02 m−1). Site 2, Kaledupa, was a “pristine” site, with low human use, high flow rates, and medium tur-bidity (Kd (PAR) = 0.18 ± 0.01 m−1). Site 3, Pak Kasim’s, was a fringing reef off Hoga Island, with intermediate turbidity and human use (Kd (PAR) = 0.13 ± 0.01 m−1, Fig. 1). The light attenuation coefficient and sample depth were used to assess optical depth (ζ) of corals, which accounts for water depth and turbidity following Kirk (1994) as ζ = Kd z, where z is depth (m), so that at an identical depth, corals at a turbid site are at a greater optical depth than those at a non-turbid site. Average water column (0–18 m) temperature was measured using HOBO data loggers (Onset, USA) and ranged between 25 and 28 °C during data collection (June–August 2007). The four coral species D. heliopora, F. speciosa, F. matthaii, and P. lutea were abundant at all sites.

Sampling Methodology.—Presence of target coral species was recorded at each site along three replicate 30 × 2 m belt transects laid 5 m apart on the reef flat (5 m depth), crest (10 m depth), and slope (15 m depth). Five colonies of every coral species were photographed at each depth (with ~10 m between each replicate colony) for a total of 15 colonies of each species per site. Photographs of target corals were taken within a custom 10 × 10 cm graded grid using an Olympus camera FE-230. These photos were then used to assess (retracted) polyp area, polyp length, and the distance between polyps by processing digitized images in Image-Tool UTHSCSA (University of Texas Health Science Center, San Antonio, Texas; Fig. 2). In every image, 10 polyps were randomly chosen to assess polyp area and length. To assess polyp density, we recorded the distance between the edges of two oral discs (to the nearest neighbor; Fig. 2).

Data Analyses.—Since polyp area, length, and distance potentially may be correlated, multivariate analyses of variance (MANOVA) were performed. If MANOVA results were sig-nificant, then variation in polyp area, length, and distance with increasing optical depth and among sites was tested, using a two-way orthogonal analysis of variance (ANOVA) on each

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species using optical depth and site as variables. A Tukey post hoc analysis was performed for each species to examine interactions between the two variables, site and optical depth. For F. matthaii, a one-way ANOVA was utilized with Tukey post hoc analysis, as data were only available for Site 1. Data for F. speciosa, F. matthaii, and D. heliopora were log-transformed to meet the assumptions of homogeneity of variance and normality. To assess the relationship between optical depth and polyp area in all four species, a Pearson’s correlation was also per-formed (n = 9). The colony mean was used for the MANOVA and ANOVA, while the transect mean was used for the correlation. All tests were performed with STATISTICA 7.0 (StatSoft) software.

Results

MANOVA results using polyp area, polyp length, and distance between polyps as variables for each coral species were significant, suggesting that there were multivar-iate differences between groups for D. heliopora, P. lutea, F. matthaii, and F. speciosa (Table 1). Subsequent ANOVA results indicate that polyp area and distance between polyps differed significantly with optical depth and between sites for some species (Tables 2, 3), while there was no significant change in polyp length among sites and with optical depth in all the coral species (ANOVA: P > 0.05). Specifically, polyp area increased significantly with increasing optical depth in P. lutea, D. heliopora, and F. matthaii (Table 2, Fig. 3). However, deviations from this trend were observed at spe-cific sites, such as D. heliopora polyp area decreasing between optical depth 0.65 (5

Figure 1. Study sites within the Wakatobi Marine National Park, southeast Sulawesi, Indonesia. Site 1 (5°28´S, 123°44É) was situated next to a Bajo village, Site 2 (5°30´S, 123°45É) was situated off Kaledupa, and Site 3 (5°28´S, 123°45É) was situated on the Hoga reef. Adapted from Hennige et al. (2008).


m) and 1.3 (10 m) at Site 3, but increasing between optical depth 1.3 and 1.95 (15 m, Fig. 3C). Site-specific differences are evident in the significant interaction between site and optical depth for D. heliopora (Table 2). The distance between polyps also increased significantly with optical depth in D. heliopora and F. speciosa, although, again, there was significant interation between site and optical depth for D. heliopora (Table 3). Site did not have significant effect on polyp area (Table 2), but did influ-ence the distance between polyps in P. lutea and F. speciosa (Table 3, Fig. 4). Tukey posthoc tests revealed that the spacing of retracted polyps of shallow F. speciosa colonies at Site 1 differed from shallow and deep polyps at Site 2 and 3 (Tukey test: P < 0.05). Similarly, D. heliopora polyps at optical depth 1.3 (10 m) at Site 3 differed from both the shallow and deep polyps at Site 1 and 2 in terms of area, length, and

Table 1. Results of MANOVA of coral polyp area, polyp length, and distance between polyps with optical depth (ζ) at three study sides off Sulaweis, Indonesia, for the massive corals, Favia speciosa, Porites lutea, Diploastrea heliopora, and Favia matthaii.

df F PF. speciosa

Site 4 6.6 < 0.001Optical depth 4 7.5 < 0.001

P. luteaSite 4 15.1 < 0.001Optical depth 4 9.3 < 0.001

D. helioporaSite 4 8.3 < 0.001Optical depth 4 19.7 < 0.001

F. matthaiiOptical depth 4 6.7 < 0.001

Figure 2. Favia speciosa at Site 1 crest. Morphometric characters extracted for analysis. PA: polyp area; PL: polyp length, maximum diameter across polyp; and PD: corallite spacing, minimum distance between the edges of two oral discs (to the nearest neighbor).

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spacing (Tukey test: P < 0.05). In addition to the previously mentioned interactions, site interacted with optical depth to polyp area in F. speciosa (Table 2, Fig. 3A) and polyp length (df = 4/36, F = 2.66, P = 0.04) in D. heliopora. Similarly, actual depth and site had a significant interactive effect on polyp area in F. speciosa (ANOVA: df = 4, 36; F = 2.56, P = 0.04) and on polyp area (ANOVA: df = 4, 36; F = 3.14, P = 0.02), length (ANOVA: df = 4, 36; F = 2.66, P = 0.04), and distance (ANOVA: df =4, 36; F = 3.12, P = 0.02) in D. heliopora.

Table 2. Results of ANOVA of coral polyp area with optical depth (ζ) at three study sites off Sulawesi, Indonesia, for the massive corals, Favia speciosa, Porites lutea, Diploastrea heliopora, and Favia matthaii. NS denotes non-significant.

df df Error F PF. speciosa

Site 2 36 2.65 NSOptical depth 2 36 2.65 NSSite × optical depth 4 36 2.65 0.04

P. luteaSite 2 36 0.64 NSOptical depth 2 36 3.56 0.03Site × optical depth 4 36 1.07 NS

D. helioporaSite 2 36 0.30 NSOptical depth 2 36 4.42 0.02Site × optical depth 4 36 3.14 0.02

F. matthaiiOptical depth 2 9 5.28 0.04

Table 3. Results of ANOVA of distance between coral polyps with optical depth at three study sites off Sulawesi, Indonesia, for the massive corals, Favia speciosa, Porites lutea, Diploastrea heliopora, and Favia matthaii. NS denotes non-significant.

df df Error F PF. speciosa

Site 2 36 7.21 0.02Optical depth 2 36 12.33 < 0.001Site × optical depth 4 36 1.89 NS

P. luteaSite 2 36 3.63 0.03Optical depth 2 36 2.65 NSSite × optical depth 4 36 1.2 NS

D. helioporaSite 2 36 0.73 NSOptical depth 2 36 3.95 0.02Site × optical depth 4 36 3.12 0.02

F. matthaiiOptical depth 2 9 2.45 NS


Discussion

Despite frequent site-specific responses, three massive coral species off Sulawesi, Indonesia, exhibited a general trend of increased polyp area with decreased light availability regardless of the amount of sedimentation. Increased polyp area could be a structural acclimation in low light situations to increase the potential for hetero-trophic efficiency (Anthony 2000, Anthony and Fabricius 2000). The trend observed across the massive species with regard to optical depth indicates that light (driven by depth or turbidity) is likely to be the driving factor behind these morphological changes. However, the additional effects of sedimentation may also be important (Rogers 1990).

Increased coral polyp area on reef slopes is likely a result of acclimation leading to changes in skeletal structure in a reduced light regime, driven by autotrophic or heterotrophic demands. Both Todd et al. (2001) and Caras et al. (2008) documented increased coral polyp sizes with increased sedimentation rates and\or decreased light levels. Importantly, sedimentation may have a dual role in polyp morphological adaptation: by affecting light attenuation and potentially as a source of food. It is un-known whether larger polyp areas and accompanying changes in skeletal reflectance primarily optimize light capture efficiency, or increase heterotrophic efficiency of the host to compensate for decreased photosynthesis at depth (Anthony 2000, Anthony and Fabricius 2000, Todd et al. 2001), but it is likely that changes in polyp sizes and

Figure 3. Mean area (mm2 ± SE) of polyps of (A) Favia speciosa, (B) Porites lutea, (C) Diploastrea heliopora, and (D) Favia matthaii from Sites 1, 2, and 3 vs optical depth (ζ, dimensionless).

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spacing reflect components of both. Small and densely packed polyps may optimize light harvesting by increasing the surface area available for zooxanthellae (Anthony and Fabricius 2000, Einbinder et al. 2009). On the other hand, larger and fewer pol-yps may aid food capture (Einbinder et al. 2009). Some species are also capable of increasing feeding rates with depth (decreasing light availability, Palardy et al. 2005). However, other species, such as Stylophora pistillata (Esper, 1797), do not increase heterotrophic intake with depth (Alamaru et al. 2009) and may rely on decreasing polyp sizes with depth to maximize light harvesting (Einbinder et al. 2009). Larger polyps may also limit smothering stress by sediment settling, which potentially re-duces colony growth (Rogers 1990). Larger polyps, which may aid in sediment rejec-tion (Stafford-Smith and Ormond 1992), are therefore likely to be an advantage in turbid habitats.

Intraspecific morphological variation of our target corals suggests an ability to ac-climate across gradients, making P. lutea, D. heliopora, F. speciosa, and F. matthaii ecologically important corals within the Wakatobi Marine National Park. This mor-phological variation is consistent with the findings of previous studies which noted that the distribution of the four target coral species was attributable to host differ-ences and not to Symbiodinium acclimatory abilities [Hennige et al. 2008, although different Symbiodinium types can affect ecological and physiological host traits

Figure 4. Mean distance (mm ± SE) between polyps of (A) Favia speciosa, (B) Porites lutea, (C) Diploastrea heliopora, and (D) Favia matthaii from Sites 1, 2, and 3 vs optical depth (ζ, dimensionless).


including growth and tolerance to heat and light stress (LaJeunesse 2001, Abrego et al. 2008)]. The dominance of P. lutea (see Hennige et al. 2008) across sites examined here may be partially due to its ability to vary its polyp morphology to optimize envi-ronmental suitability. The relatively lower abundance of F. speciosa across sites, cou-pled with the narrower range of morphological change observed with regard to polyp area is consistent with this hypothesis. Consequently, although morphological varia-tion cannot solely determine coral distribution across environmental gradients, it is an important consideration in future studies, as without host morphological chang-es, acclimation of heterotrophy and photosynthesis would be severely constrained.

Acknowledgments

We thank Operation Wallacea, the Indonesian Institute of Sciences and J Jompa (UNHAS) for their support. We also thank M Flavell for help in editing figures and C Mattone for help with statistical analyses, and comments from MS Pratchett and the anonymous reviewers, which greatly improved this manuscript.

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Date Submitted: 5 October, 2010.Date Accepted: 2 June, 2011.Available Online:

Addresses: (CP, JH) ARC Centre of Excellence for Coral Reef Studies, James Cook University of North Queensland, Townsville, Queensland 4811, Australia. (SJH) Centre of Marine Biodiversity and Biotechnology, Heriot Watt University, Edinburgh, United Kingdom. (RM) Università Degli Studi Di Roma “La Sapienza,” Rome, 00185, Italy. (DJS) University of Essex, Wivenhoe Park, Essex, CO43SQ United Kingdom. Corresponding Author: (CP) E-mail: <[email protected]>.

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Morphological Changes in Polyp Structure of Massive Coral Species in Clear and Turbid Waters