Coral Reefs

, 28:999

Effect of colony size and surrounding substrate on corals experiencing a mild bleaching event on Heron Island reef flat (southern Great Barrier Reef, Australia)


    • Centre for Marine StudiesThe University of Queensland
  • M. del C. Gomez-Cabrera
    • Centre for Marine StudiesThe University of Queensland
  • O. Hoegh-Guldberg
    • Centre for Marine StudiesThe University of Queensland

DOI: 10.1007/s00338-009-0546-0

Cite this article as:
Ortiz, J.C., Gomez-Cabrera, M.d.C. & Hoegh-Guldberg, O. Coral Reefs (2009) 28: 999. doi:10.1007/s00338-009-0546-0


In January–May 2006, Heron Island in the Great Barrier Reef experienced a mild bleaching event. The effect of colony size, morphology and surrounding substrate on the extent of bleaching was explored. In contrast with previous studies, colony size did not influence bleaching sensitivity, suggesting that there may be a threshold of light and temperature stress beyond which size plays a role. Also contrasting with previous studies, massive corals were more affected by bleaching than branching corals. Massive corals surrounded by sand were more affected than the ones surrounded by rubble or dead coral. It is hypothesized that light reflectance from sand increases stress levels experienced by the colonies. This effect is maximized in massive corals as opposed to branching corals that form dense thickets on Heron Island. These results emphasize the importance of the ecological dynamics of coral communities experiencing low, moderate and high levels of bleaching for the understanding of how coral communities may change under the stress of climate change.


Coral bleachingColony sizeCoral growth morphCoral-surrounding substrate


Coral reefs are considered to be one of the first of the earth’s ecosystems to show a dramatic response to climate change. The intensity and frequency of events termed mass coral bleaching (to describe the large geographical area involved) have been steadily increasing, with events such as the global bleaching in 1998 emphasizing the extent to which climate change can destabilize ecosystems. In just 12 months, an estimated 16% of the world’s corals died in 1998 (Wilkinson 2000). Understandably, much of the ecological literature has focused on the outcomes of these extreme events (Glynn 1983; Goreau 1992; Phongsuwan 1998; Aeby et al. 2003; Berkelmans et al. 2004). Meanwhile, the dynamics and ramifications of more subtle and sublethal events have not been explored but could be argued as being of equal importance to the understandings of a warming climate.

Sub-lethal impacts of thermal stress may involve a range of variables including effects on growth (Goreau and MacFarlane 1990) and reproduction (Szmant and Gassman 1990). Stress at low levels may also influence corals differently. Given that the level of stress is not high enough to overpower the variability in susceptibility, the differences between individuals and species will be maximized. In previous studies, the coral response to thermal stress has been shown to vary according to colony size (Bak and Meesters 1998, 1999; Shenkar et al. 2005), with predictions made regarding the size distribution of colonies within coral communities changing as a consequence of size-dependent bleaching and mortality (Bak and Meesters 1999). Similarly, growth form has been suggested as a risk factor to thermal stress (Hoegh-Guldberg and Salvat 1995; Marshall and Baird 2000; Loya et al. 2001).

In the summer of 2006, Heron Island reef experienced a mild bleaching event. The water temperature reached more than three degrees over the long term average for part of the season, and bleached colonies started to appear by the second week of December 2005 (Leggat et al. 2006). Up to 30% of the corals on the intertidal reef flat of Heron Island showed evidence of thermal stress by way of colour loss. This mild bleaching event provided an opportunity to attempt to answer the following questions:
  1. 1.

    What is the effect of mild thermal stress on corals with different growth morphologies?

  2. 2.

    Is susceptibility to the effects of mild thermal stress influenced by colony size?

  3. 3.

    Does the substrate surrounding a coral colony influence its susceptibility to bleaching?


Materials and methods

Sampling design and data collection

The measurements were recorded in a section of the southwest Heron Island reef flat. This area is homogeneous in depth (0–220 cm depending on tide) and it gets exposed at low tide. Every coral colony (2001 colonies in total) was studied in an area that was 61 m × 160 m (9,769 m2). This area was haphazardly selected from the Heron Island reef flat, and a GPS was used to ensure that all the colonies within the area were sampled only once. The following measurements were recorded for each colony:

Colony projected area (cm2) was estimated using a 50 cm × 50 cm quadrat subdivided in 100 squares. The quadrat was located on top of the colony, and the number of squares where the coral occupied >25% covering the colony was counted.

Growth form was noted for each colony and was assigned to one of two morphological categories (massive or branching corals as defined by Veron 2000) as the majority of corals in the study area fit into these categories. To increase the resolution of the study, the most abundant genera (with a relative abundance of about 50% of the colonies within that growth morph) were identified separately generating a total of four categories: Branching Acropora (A), other branching corals (B), massive Porites (P) and other massive corals (M).

Coral colour cards were used to assess the intensity of dinoflagellate pigments in each of the 2001 colonies (Siebeck et al. 2006). To do this, the lightest and the darkest sections of each colony were noted, along with the proportion of each colony being assigned to each colour. The proportion of the colony covered by each colour was used to obtain a weighted average colour for each colony as a continuous value from one (lightest: bleached) to six (darkest: normal), following Eq. 1.
$$ {\text{Cc}} = ({\text{Dc}} \times {\text{Da}}) + ({\text{Lc}} \times {\text{La}}) $$
where Cc is the colony average colour, Dc is the darkest colour found in the colony, Da is the proportion of the colony covered by the darkest colour, Lc is the lightest colour and La is the proportion of the colony covered by the lightest colour. To account for the potential confounding effect of differences in “normal” colours among the morphs, the average colour for the colonies that were in the upper range of the colour distribution (i.e., 5% darkest corals) for each morph was calculated. Then, the difference between the “normal” average colour and the actual average colour was calculated as a percentage.

To examine whether the substrates surrounding a colony affected its bleaching state, the types of substrate surrounding each colony were recorded, assigning the most prevalent substrate to each of the three categories: Sand (S); rubble (R: calcium carbonate fragments bigger than 2 cm and smaller than 10 cm diameter and not attached to the substrate) and dead coral (D: calcium carbonate fragments bigger than 10 cm diameter attached to the substrate).

Data analysis

To compare the effect of the coral morphology, the substrates surrounding the coral colonies and the size of the colony on the average colony colour, a three-factor analysis of covariance (ANCOVA) was performed. The model included coral colony colour as the dependent continuous variable, coral growth morph as a fixed factor with four levels (A, B, P and M), surrounding substrate as a fixed factor with three levels (S, R and D) and colony size as a continuous predictor (covariate). The assumption of homogeneity of variance as well as equality of variance (for the covariate) was tested and satisfied for both the categorical predictors and the covariates including the interactions. Because the range of values for the covariate (colony size) was different between the morphologies (Acropora 25–25,800, Branching 25–8,000, Massive 20–2,000, Porites 20–2,500 cm2), a separate slopes model was used for the covariate. This model is equivalent to a nested model for categorical factors; therefore, only the highest level interaction of the covariate is included in the model (Hill and Lewicki 2006) When a statistically significant difference was found, the least significant distance test (LSD) was used to determine which of the levels of the variable were different. All the statistical analyses were done using STATISTICA (Data Analysis Software System), v7 (StatSoft, Inc. 2004).

Results and discussion

Of the 2001 colonies studied, 11.3% had average colours that were lower than 2 (highly bleached), while 33.3 and 36.8% had intermediate colours (average 2–3 and 3–4), respectively, and 17.85% were very dark in colour (4–6). This relatively low percentage of heavily bleached colonies suggests that the bleaching event on Heron Island reef flat in 2006 can be considered mild in comparison with other bleaching events where the percentage of bleached colonies varied between 25 and 95% (Glynn 1983, 1996; Faure et al. 1984; Phongsuwan 1998; Berkelmans and Oliver 1999; McGrath and Smith 2003; Donner et al. 2005; Miller et al. 2006).

In contrast to previous studies (Bak and Meesters 1998, 1999; Shenkar et al. 2005), coral colony size did not affect the risk of bleaching, regardless of the colony growth form or the substrate surrounding the colony (Table 1). This contrast has two potential explanations. Firstly, the differences may have arisen due to different statistical assumptions. In the present study, colony size was incorporated in the statistical model as a continuous variable. In previous studies, however, size has been tested as a categorical variable creating size categories and using a contingency table type of approach to test significance (Bak and Meesters 1998, 1999). This difference in statistical approaches makes the direct comparison of the results extremely difficult. The use of a different set of size classes could potentially produce different results. Nevertheless, for the purposes of this study, it was not appropriate to use size as a categorical variable, because it would not have been possible to have the three factors (size, surrounding subtrate and morph) in the same analysis. Secondly, previous studies focused on the colony size effect within fairly severe mass bleaching events, while the 2006 bleaching event on Heron Island was mild. Size may become an important factor in the susceptibility of a colony to bleaching only after a stress level or threshold is reached. If this is the case, the fact that size appears not to influence bleaching susceptibility in mild bleaching events needs consideration within any model or prediction of the effect of climate change on coral reefs, since mild bleaching events are much more frequent than moderate to severe events.
Table 1

Three factor ANCOVA with separate slopes model for the continuous predictor (colony size)







Post hoc LSD test








Morph × surrounding × size





















Morphology × surrounding






AxS, AxR, AxD > MxS, MxD, PxD, PxR

BxS, BxR, BxD > MxS MxD, PxD, PxR

MxS < MxR






Post hoc comparisons shown are the ones significant at p < 0.05

A branching Acropora, M other massive corals, B other branching corals, P branching Porites, S sand, D dead coral, R rubble

The difference in the colony colour between the sampled colonies and the healthier colonies (5% upper range of colony colour per morph) showed a similar pattern as the one shown by the actual average colour before standardizing. Branching Acropora and other branching showed a highest percentage of the original colour (70.1 and 67.2%) in comparison with massive Porites and other massive corals (58.5 and 60.1%; Fig. 1, see also Table 1 for significance). Most studies on differential susceptibility to bleaching suggest the opposite results (branching corals being more susceptible than corals exhibiting massive growth morphologies) (Hoegh-Guldberg and Salvat 1995; Fitt and Warner 1995; Marshall and Baird 2000; Loya et al. 2001). One consideration that must be made is that in the study area, many branching corals were heavily bleached in small areas of the colony while still dark in others. When the weighted average is calculated, unless the level of bleaching is very high (colour card values <2), the final colour associated to the colony ends up relatively dark. On the other hand, most of the massive corals were homogenously pale (colour card values between 2 and 3). Therefore, the average colony colour was lighter for massive corals even though the only colonies that presented extremely bleached areas (colour card value of 1) were branching colonies. Again, the fact that this study was undertaken in a mild bleaching event, suggests that the differential susceptibility to bleaching depends on the level of stress being experienced. Massive corals may be more susceptible to mild bleaching events while branching corals are more susceptible to severe events. The sub-lethal effect that this differential bleaching may have on the corals (Goreau and MacFarlane 1990; Szmant and Gassman 1990) may have importance for how reefs change over the next couple of decades as the frequency of low level stress events increases (Hoegh-Guldberg 1999).
Fig. 1

Average colour per colony as a function of surrounding substrate and coral growth morphology. Error bars represent two times standard error. D dead coral, R rubble, S sand, A branching Acropora, B other branching corals, M other massive corals, P massive Porites

The effect of surrounding substrate on colony susceptibility to bleaching had not been studied before but appears to be important. In this study, ‘other massive corals’ surrounded by sand were bleached to a greater extent (lower colour scores) than ‘other massive corals’ surrounded by rubble, while ‘other massive corals’ surrounded by dead coral presented intermediate colour values (Fig. 1, significant LSD differences showed in Table 1). It is hypothesized that the highly reflective sands amplify the light intensity surrounding coral colonies and that this increases the extent of bleaching arising from thermal stress, as predicted from our physiological understanding of bleaching (Jones et al. 1998; Hoegh-Guldberg 1999). It was noticed that the ‘other massive corals’ surrounded by sand were generally lighter in colour on the sides of the colony in comparison with the sides of ‘other massive corals’ surrounded by rubble or dead coral. This contrasts with the effect of substrates such as rubble or dead coral, which are commonly covered by a layer of algae that would potentially absorb light and minimize the reflection of light onto the coral colonies. In the case of the branching corals, the effect is not as strong probably because of the fact that branching corals on the Heron Island reef flat form dense thickets where only a small proportion of the live tissue is exposed to the reflectance from the sand. In contrast to ‘other massive corals’, this effect was not evident in massive Porites. The bigger size of the Porites colonies on the Heron reef flat (about six times bigger in average than all the other massive species) makes the proportion of the colony exposed to the effect of the sand reflectance much smaller. This result may be of particular importance for further studies that aim to predict mass bleaching events. Particularly for remote sensing approaches, where detecting the proportion of sand in a reef is one of the best developed capabilities of remote sensing coral reef mapping (Mumby et al. 1997; Andrefouet and Robinson 2003; Phinn et al. 2005). If the relationship between proportion of sand and bleaching susceptibility is a general pattern, (the small scale of this study does not allow for this type of generalisation) then, including the sand/rubble ratio in coral bleaching models would potentially improve the accuracy of such models.

This study has suggested that the ecological dynamics of mild versus severe bleaching events may differ. These differences may have relevance for understanding how relatively small changes in environmental conditions over the next few decades may modify the growth, reproduction and community dynamics of coral communities and have important ramifications for how managers respond to the changing fortunes of different species and growth morphologies of corals. Clearly, these aspects of the ecology of mild coral bleaching need consideration in future studies.


The authors would like to thank Zubin Agarwal, Rahul Vasavada and Boyko Kakaradov from the Stanford University–University of Queensland study abroad program for their help with the fieldwork component of this project.

Copyright information

© Springer-Verlag 2009