PRIMARY RESEARCH PAPER

Assessing coral bleaching and recovery with a colourreference card in Watamu Marine Park, Kenya

Simone Montano • Davide Seveso • Paolo Galli •

David O. Obura

Received: 30 July 2009 / Revised: 21 July 2010 / Accepted: 3 August 2010 / Published online: 17 August 2010

� Springer Science+Business Media B.V. 2010

Abstract With this study we estimated the changes

in colour, bleaching and mortality of coral colonies

from February to December 2007, using the colour

reference card method. The study was developed in

the Watamu Marine Park lagoon (Kenya), bridging the

local summer when seawater temperatures were

highest and coral bleaching risk was at its maximum.

Seven coral genera were selected, and their colour

recorded using a colour reference card (Coral Watch

card). Seven different scenarios of bleaching and

mortality were observed, varying among the coral

genera and between two species in the genus Pocil-

lopora. Twenty percent of the colonies bleached, of

which 50% died. Only 15% of the coral that did not

bleach died. Branching genera had a higher bleaching

incidence than massive and sub-massive genera.

Pocillopora showed the highest bleaching suscepti-

bility, followed by Acropora, and the highest level of

mortality. Of the two species of Pocillopora consid-

ered in this study, P. eydouxi showed higher bleaching

and mortality levels, while P. verrucosa bleached less

and experienced only partial mortality. Our results

evidenced different patterns of coral bleaching and

mortality which were easily and clearly detected with

the colour card method during both bleaching and a

post-bleaching events.

Keywords Coral bleaching � Reference card �Pocillopora � Watamu Marine Park

Introduction

Coral bleaching is characterised by the loss of dino-

flagellate symbionts (genus Symbiodinium) and/or

symbiont pigmentation (Hoegh-Guldberg & Smith,

1989; Brown, 1997) from the holobiont which causes

colour loss/decrease in the coral colony, which can

become paler to white. Colour bleaching is triggered by

a number of stressful factors including the temperature

increase of superficial waters (Jokiel & Coles, 1990;

Brown, 1997). In the last two decades, frequency and

severity of coral bleaching increased as water temper-

ature increased, at rates that had never been detected

before. Since further increases in water temperature are

expected, thus a dramatic impact on coral bleaching

can be foreseen for the next 30–50 years (Hoegh-

Guldberg, 1999; Hughes et al., 2003).

Coral bleaching has several consequences for the

organism, including reduced growth and reproduction,

Handling editor: P. Viaroli

S. Montano (&) � D. Seveso � P. Galli

Department of Biotechnologies and Biosciences,

University of Milan-Bicocca, Piazza della Scienza 2,

20126 Milan, Italy

e-mail: simone.montano@unimib.it

D. O. Obura

CORDIO East Africa, 9 Kibaki Flats, Kenyatta Public

Beach, P.O. BOX 10135, Mombasa 80101, Kenya

123

Hydrobiologia (2010) 655:99–108

DOI 10.1007/s10750-010-0407-4

increased mortality (Brown, 1997) and ecological

implications for the reef, including significant reduc-

tions in cover of susceptible species, changes in

community composition, decrease in species diversity

and associated decrease in reef growth and habitat

diversity (Glynn, 1993). Differential coral bleaching

susceptibilities and post-bleaching colour change,

survival or mortality have been observed, with varia-

tion among coral taxa, populations and even colonies

on an individual reef (Coles & Brown, 2003). At the

species level, one of the clearest associations with these

different susceptibilities is their growth rates, with

branching and faster growing corals (e.g. acroporids

and pocilloporids) being more severely affected by

bleaching than massive and slower growing species,

e.g. poritids and faviids, (Marshall & Baird, 2000;

McClanahan et al., 2004; Obura, 2005a). Branching

and susceptible species also show higher post-bleach-

ing recovery rate of zooxanthellae population and high

post mortality recovery of new corals (Kayanne et al.,

2002).

Total or partial mortality in corals is the most

important consequence of coral bleaching (Glynn,

1990; McClanahan et al., 2008). However, if colonies

survive, zooxanthellae repopulate the coral tissues

and the corals recover their normal colour and

metabolic activity (Brown, 1997). Repopulation

may occur through a variety of mechanisms including

division of existing symbionts and/or uptake from the

water column, and it is now clear that it may involve

competitive dynamics and shifts among zooxanthel-

lae clades with different physiological advantages in

the post-bleaching phase and/or under different

environmental conditions (Baker, 2003).

Coral colour is the most general indicator of

bleaching, a direct consequence of loss of symbionts

and/or pigment. However, though easy to record in

situ, it reveals little about internal physiological state

and symbiont population trends. Nevertheless,

recording coral colour is the simplest and most direct

measure of bleaching, and it is used for direct

underwater observations, in photographic transects

and in visual or multispectral remote sensing devices

borne in the air or on satellites. With increasing

frequency of bleaching events, and with high vari-

ability in their intensity and consequences, rapid

visual methods will be invaluable in documenting

and understanding future trends in coral bleaching. In

this study, we apply an inexpensive, objective, rapid

and non-invasive method, based on a colour reference

card (Siebeck et al., 2006) to assess bleaching and

post bleaching recovery in the lagoon of the Watamu

Marine Park, Kenya. The colour reference card

method has been used for the first time in situ to

monitor the same coral colonies in time, evaluating

any bleaching and post-bleaching mortality during

the northeast monsoon (local summer season). Dif-

ferent coral genera have been studied to further

understand bleaching and mortality dynamics of

Kenyan reef corals and to test the effectiveness of

the proposed method.

Materials and methods

Study sites

The study was undertaken on coral patches inside the

lagoon of Watamu Marine National Park (3�220N;

39�590E) in Kenya, between December 2006 and

December 2007. The park extends over a 10 km2 area

and encloses a lagoon with low and uniform topogra-

phy dominated by a seagrass beds, sand and shallow

flats, with coral patches on eroded inner reef structures

(Kaunda-Arara & Rose, 2004). The study area is

situated in the richest coral zone of the lagoon called

Coral Garden, approximately 300 m from shore. The

marine park has been protected from all forms of

resource extraction since 1968. Sea surface tempera-

tures for Watamu Marine Park area (Fig. 1) were

obtained from remote sensing records (http://disc.sci.

gsfc.nasa.gov/techlab/giovanni/).

Survey method

Between December 2006 and February 2007, the study

area was mapped, the position of the coral patches

inside the lagoon were geo-referenced and their

general shape and living cover were noted. Seven

genera of hard corals with different growth morphol-

ogies and bleaching susceptibilities (Marshall & Baird,

2000, Obura, 2001) were sampled: Pocillopora, Acro-

pora, Favia, Platygyra, Galaxea, Echinopora and

Porites (massive colonies only). These genera were

also the most common in the studied area, but sample

sizes varied widely, from 59 (Pocillopora) to 8

(Porites), totaling 181 colonies. Within the genus

Pocillopora two species (Pocillopora eydouxi and

100 Hydrobiologia (2010) 655:99–108

123

Pocillopora verrucosa) were distinguished (Table 1),

with 30 and 29 colonies each, respectively. Colonies

were selected haphazardly and for ease of re-location

and colour analysis, identified and their position

marked and documented using underwater photo-

graphs and hand-drawn maps. Both video (Sony

dcr-hc30 with Isotta spj-b Isotecnic housing) and

photography (Canon A710 IS with Ikelite housing)

were utilized also for a qualitative evaluation of coral

health. Colonies were located between 1 and 6 m depth.

Observations on the coral colonies were made at

eight sample points, classified into three categories

based on local seasons and bleaching risk:

(1) during the warm northeast monsoon before bleach-

ing—2nd February to 13th March (samples 1–4);

(2) at the end of the northeast monsoon and during

the calm transition between monsoons, when

bleaching risk is highest and often observed—

April (sample 5); and

(3) during the southeast monsoon when tempera-

tures are lower and after any bleaching has

finished—15th August to December (samples

6–8).

Coral colour was determined using an underwater

colour reference card (Coral Watch colour card,

Siebeck et al., 2006). It presents four colour hues

typical for corals (brown, pink, green and ochre), and

for each colour a 6 point brightness/saturation scale to

record visible differences in coral colour from white/

pale (levels 1 and 2) to dark (6). Each brightness/

saturation point corresponds to zooxanthellae or pig-

ment concentrations. However, there is a high level of

variability in the correlation between zooxanthellae

and pigment concentrations with colour. For this study,

we therefore determined that differences in colour

of 2 scale points are necessary to infer differences

in zooxanthellae or pigments, and hence bleaching

(lightening) or recovery (darkening) (Siebeck et al.,

2006). Following bleaching, if the colony returned to

its original colour level, this was considered as total

colour recovery. If colour resumption was not total the

coral was categorized as having partially recovered. At

each sampling period the darkest portions of a colony

was scored using the most appropriate hue on the

reference card, and the incidence of partial or full

mortality was also noted. Following mortality, the

exposed skeletons were covered by algal turf and other

organisms.

Data analysis

The number of colonies showing a particular colour

shade in each sampling period was shown in

frequency histograms. To better show coral colour

Fig. 1 Sea surface

temperature for Watamu

Marine Park Area from

December 2006 to

December 2007 (Source:

http://disc.sci.gsfc.nasa.gov/

techlab/giovanni/)

Hydrobiologia (2010) 655:99–108 101

123

variations over all sampling time it was chosen to

illustrate only four of the eight samples (February,

April, August and December samples). The full

datasets were analyzed for changes in coral colour

and mortality using nonparametric multivariate tech-

niques, cluster analysis and nonmetric, multidimen-

sional scaling (nMDS) using the PRIMER statistical

package (Clarke & Gorley, 2001). The clusters were

obtained creating a distance matrix from the colour

values (1–6) and mortality (0) for the colony at each

of the sampling time, and linked using the group

average. nMDS was done using normalized euclidean

distance, without transformation.

Results

Seawater temperature (Fig. 1) showed a maximum in

March and minimum in August 2007 (&30 and

25.5�C, respectively), though with a secondary high

of 28�C in December 2006 and 2007, and a secondary

low of 27�C in January 2007.

In February, the 92% of Pocillopora colonies

(Fig. 2) were attained in the darkest colour shade (6),

with lightening to April shown by an increase in

frequency of colour classes 5, 4, 3 and 2. In August,

the frequency of colour class 6 increased, and

remained stable to December. Also in August,

mortality was recorded, which increased in Decem-

ber. The pattern for Acropora was similar, with

lightening of colonies from February to April,

followed by recovery of colour to August and

December but accompanied by mortality in August.

Platygyra and Echinopora showed similar patterns of

lightening colour from February to April, which

progressed into August and no change to December.

Favia and Galaxea showed different patterns, with

either a darkening of colour or no change from

February to April, then lightening in August to

December. No colour or changes or mortality were

observed in Porites. From samples 1–4, though there

was a general lightening of most colonies, none of

these transitions were [1 shade, so were not classi-

fied as bleaching.

Cluster analysis showed three principal clusters

among the genera (Fig. 3). The first cluster included

Pocillopora and Acropora, representing higher levels

of bleaching in April and mortality in August and

December. The second cluster was split into two

groups: Galaxea and Echinopora in one and Favia,

Platygyra and Porites in the other.

In April, a number of colonies bleached while

others did not, and from then to August and

December, seven bleaching conditions were identi-

fied and classified as bleaching scenarios (Table 1).

The 18.8% of colonies bleached in April. From

August to December, the majority of the bleached

colonies suffered full mortality (B4), followed by

those that fully recovered to pre-bleaching colour

(B2), those that partially recovered to pre-bleaching

colour (B3), and those that remained bleached (B1).

Of the 81.2% of colonies that remained normal in

April, the largest proportion did not undergo any

colour variation from August to December (N1),

and the remainder experienced equal full mortality

and bleaching (N2 and N3, respectively). Colour and

mortality dynamics were different before bleaching

from after bleaching; a MDS plot shows the samples

1–4 in one cluster and 6–8 in another, with sample 5

distinct from both (Fig. 4). The trajectory through the

points is in the order from 1 to 8. The separation of

point 5 from 1–4 along the y-axis reflects the higher

level of bleaching in April, while the separation of

points 6–8 along the x-axis is due to mortality, and

Table 1 List and

description of the seven

different scenarios observed

between February and

December 2007

Each scenario is indicated

by a code, bleaching

presence (B) or absence (N)

in April, post-bleaching

colour variation and

mortality events between

August and December

Scenario

code

April August–December Proportion of colonies (%)

Bleaching Colour variation Mortality Of total Of N or B

N1 No No No 55.8 68.8

N2 No No Yes 12.7 15.6

N3 No Bleaching No 12.7 15.6

B1 Yes No No 2.8 14.9

B2 Yes Total recovery No 5.5 29.3

B3 Yes Partial recovery No 1.6 8.5

B4 Yes No Yes 8.9 47.3

102 Hydrobiologia (2010) 655:99–108

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Fig. 2 Colour frequency and mortality during selected months

of sampling in the Watamu marine National Reserve during

2007. Data is shown for the genera Pocillopora, Acropora,

Favia, Platygyra, Galaxea and Echinopora and the species

Pocillopora eydouxi and P. verrucosa. The colour values

represent the 6 points brightness/saturation scale on the colour

reference card from white/bleached (1) to dark (6)

Hydrobiologia (2010) 655:99–108 103

123

their intermediate position along the y-axis by high

variation in colour.

Pocillopora showed the highest frequency of

bleaching in April (47.5%, Table 2), followed by

Echinopora, Galaxea and Acropora. Platygyra

showed a low frequency of bleaching of 3.2%. No

Porites or Favia colonies bleached in April. In

August/December, bleaching occurred especially in

Favia, and in Platygyra and Galaxea. Total recovery

of pre-bleaching colour occured only for Pocillopora,

partial recovery of colour occurred for Acropora and

Platygyra colonies and also for Pocillopora.

Some colonies experienced partial mortality, as

opposed to the full mortality presented in Table 2 and

Fig. 2 (Table 3). For Acropora and Pocillopora, a

larger proportion of colonies showed full mortality

than partial mortality, while Favia showed the

opposite. Platygyra and Galaxea suffered some

partial mortality but no full mortality, and no

mortality or either type was observed in Echinopora

and Porites. Colour and mortality patterns varied

between the two species of Pocillopora (Fig. 2) with

P. eydouxi showing lighter colours and higher

bleaching levels in April than P. verrucosa, followed

by greater full mortality and less recovery of colour

in August and December. In contrast, P. verrucosa

showed higher levels of partial mortality.

nMDS of the colour and mortality dynamics of all

colonies shows two main clusters in the case of

genus/species identity (Fig. 5a), with Pocillopora

eydouxi colonies mostly separated in a cluster with

some Acropora and some P. verrucosa colonies.

Otherwise, most other genera, and P. verrucosa and

Acropora colonies were in the main cluster, with

some sub-structure distinguishing Acropora and

Echinopora colonies from the rest. Classified by

bleaching scenario (Fig. 5b), the scenarios that

include mortality (n2, b4) are clearly segregated

towards the left of the plot, in a main cluster and sub-

clusters separate from the scenarios in which there

was no mortality. The non-mortality scenarios are

broadly mixed among one another, though with

bleaching scenarios mostly contained in the upper

sub-cluster.

Fig. 3 Cluster analysis of the monitored genera through

darkest portion surface analysis

Fig. 4 nMDS of colony

colour for all sampled

colonies during the 8

sampling periods from

February to December 2007

(t1–t8). Before (1), during

(2) and after (3) bleaching

symbols are shown for the

time periods, and %

similarity contours from a

cluster analysis

104 Hydrobiologia (2010) 655:99–108

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Discussion

The temperature patterns recorded for 2007 in

Watamu followed the normal bimodal pattern for

East African reefs (McClanahan, 1988). Bleaching

occurred as expected, in April, at the end of the

summer season and during or just after the maximum

temperatures in March when thermal stress was

highest. The thermal stress was probably amplified by

the water stagnation, slow hydrodynamics, with

temperatures likely exceeding the remote sensed

values (McClanahan et al., 2007).

Results showed a moderate bleaching event, with

18.8% of the colonies bleached and 21.6% mortality.

While there were more dead corals that had not

bleached (12.7%) than had bleached (8.9%), the

mortality rate was much higher for bleached corals, at

almost 50%, compared to 15% for non-bleached

corals. Pocillopora and Acropora were most suscep-

tible, with highest bleaching rates, while Platygyra,

Favia, Galaxea and Echinopora were relatively

unaffected. Porites showed no level of bleaching or

mortality. Full mortality was highest in Pocillopora,

associated with its high bleaching rate. Where partial

mortality was observed, none of the colonies showed

any regrowth of tissue over the sampling time, while

many of them died completely. These patterns have

been found in the same suite of genera in East Africa

in the past (Obura, 2001, 2005b), with Acropora and

Pocillopora most susceptible to bleaching and mor-

tality, Porites least affected in terms of mortality

though it is often recorded with high levels of mild

bleaching. Other genera are intermediate between the

two. In agreement with other studies, branching

corals with elevated growth rates were the most

susceptible, while massive, submassive and encrust-

ing forms were less susceptible (Gleason, 1993;

Hoegh-Guldberg & Salvat, 1995; Marshall & Baird,

2000; Loya et al., 2001).

Table 2 Frequency of scenarios for each genus, for Pocillopora species and for the total number of colonies analyzed inside Coral

Garden through darkest portion surface analysis between February and December 2007

Genus Species Growth form # Frequency of scenarios (%)

N N1 N2 N3 B B1 B2 B3 B4

Pocillopora Branching 59 52.5 35.5 15.3 1.7 47.5 5.1 17.0 1.7 23.7

Pocillopora eydouxi (30) (50) (30) (16.7) (3.3) (50) (6.7) (10) (–) (33.3)

Pocillopora verrucosa (29) (55.2) (41.4) (13.8) (–) (44.8) (3.4) (24.2) (3.4) (13.8)

Acropora Branching 15 93.3 73.3 20 – 6.7 – – 6.7 –

Favia Submassive 28 100 42.9 21.4 35.7 0 – – 0 –

Platygyra Massive 31 96.8 61.3 6.5 29 3.2 – – 3.2 –

Galaxea Submassive 20 90 65 15 10 10 – – – 10

Echinopora Encrusting 20 90 85 – 5 10 10 – – –

Porites Massive 8 100 100 – – 0 – – – –

Overall 181 81.2 55.8 12.7 12.7 18.8 2.8 5.5 1.6 8.9

The different coral growth forms, the number of colonies analyzed (#) and the different scenarios observed (N1, N2, N3 and B1, B2,

B3, B4) are reported

Table 3 Percent frequency of full and partial colony mortality

for each genus, for Pocillopora species and for the total

number of colonies (overall) analyzed inside Coral Garden

between February and December 2007

Genus Species Mortality (%)

Full Partial

Pocillopora 23.7 15.3

Pocillopora eydouxi 40 10

Pocillopora verrucosa 6.9 20.7

Acropora 13.3 6.7

Favia 3.6 17.8

Platygyra – 6.5

Galaxea – 25

Echinopora – –

Porites – –

Overall 9.4 12.2

Hydrobiologia (2010) 655:99–108 105

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Colour varied greatly in individual coral colonies,

in patches and mosaics across a colony surface, and

colour classes 4–6 was present on apparently normal

corals at the same time. Growing edges (tips of

branches and edges of plates) were frequently white

or pale. The correlation between colour and zooxan-

thellae and pigment concentrations was relatively

weak (Fitt et al., 2001; Siebeck et al., 2006).

This study shows how the colour card method

enables multiple observers, in the water at different

times, to record quantitative data on bleaching with

similar findings. Selecting only the darkest portion of

the colony surface for data collection in this study

minimized subjectivity and variability in the dataset,

facilitating comparisons between the sampling times.

However, it may also result in under-reporting of

bleaching by ignoring lighter patches of a colony

surface.

Sampling was not conducted between April and

August 2007 due to the rough southeast monsoon and

facilities being closed. During strong bleaching events,

maximum bleaching levels in Kenya occur in April or

Fig. 5 nMDS of colony

colour for all sampled

colonies during the eight

sampling periods from

February to December 2007

(same data as Fig. 3).

Percent similarity contours

are shown from a cluster

analysis: A by genus, B by

bleaching scenario

106 Hydrobiologia (2010) 655:99–108

123

May, after which recovery or mortality are the two

possible outcomes. Since we did not sample in May,

maximal bleaching may have been under-sampled,

though because mortality is permanent, this was

accurately sampled. The relationship between levels

of bleaching and mortality is not straightforward

(McClanahan, 2004). While the mortality rate of

corals that did bleach was higher than that of corals

that did not bleach, significant mortality without

bleaching was recorded. The patterns recorded of

partial mortality are not clearly related to bleaching.

This was highlighted for the two Pocillopora species,

where P. eydouxi suffered more bleaching and full

mortality, while P. verrucosa suffered less bleaching

but more partial mortality. A similar comparison

between the two species was observed during a mild

bleaching event in 2003, 100 km to the south in

Mombasa, where P. verrucosa presented delayed

bleaching, a higher partial mortality rate, and a delay

in the appearance of the first completely dead colonies

(Obura, 2005b).

Acropora presented lower bleaching and mortality

rates than Pocillopora, but was slower to regain

colour in August and December. These two genera

are often reported as being among the most suscep-

tible to bleaching (Marshall & Baird, 2000; Loya

et al., 2001, Obura, 2001), but there are clearly

differences in their responses that may reflect differ-

ent life history strategies, with Acropora being a

more dominant, space-occupying genus, and Pocil-

lopora a more opportunistic and ephemeral genus

(Obura, 2001). The implications of life history

strategy on bleaching dynamics are not yet well

understood, but it is possible that as a stress resistance

mechanism (Obura, 2009a), recovery from bleaching

will be least important to opportunistic strategies

such as in Pocillopora, and more important to

strategies based on dominating space and persisting

through stressful conditions (Obura, 1995, 2009b).

Thus, as a fast growing species like Acropora shows

high bleaching rates, but as a space dominant it may

invest more resources in surviving bleaching to

maintain its competitive advantage. The complete

lack of bleaching in Porites reported here is unusual,

as in the same habitats it has in the past been reported

with high rates of bleaching, but at low intensity and

with low mortality (Obura, 1995, 2001).

A noticeable degree of bleaching (N3) occurred in

the faviid genera Favia, Platygyra and Echinopora

and in Galaxea. It is unlikely that this bleaching was

related to high seawater temperatures in March/April,

as the strong decline in temperature reaching a

minimum in August provides protection and time to

recover from earlier heat stress. With most of these

corals in the same family, it may be a characteristic of

faviids responding to other environmental conditions

or an annual cycle. Alternatively, rough conditions in

the southeast monsoon in May–August may result in

resuspension of sediment and some stress to corals,

and these genera may be more susceptible than the

other genera studied.

Though bleaching of corals is only a rough

indicator of the density and physiological state of

zooxanthellae symbiotic in coral tissues (Fitt et al.,

2001) it nevertheless is of great importance to the

symbiosis as a final stage of resistance to severe stress

(Coles & Brown, 2003, Obura, 2009a). In its final

stages, it is also among the easiest indicators to

document non-invasively, and by observers in the

water as well as by sensors on airplanes and even

satellites. This study further supports the value of the

colour reference card method (Siebeck et al., 2006) in

monitoring colour change in individual colonies over

time, offering a simple tool for non-technical observ-

ers to contribute accurate and quantitative data to the

monitoring of coral reef health around the world.

Acknowledgments We are thankful to CORDIO (Coastal

Oceans Research and Development in the Indian Ocean) and

Kenya Wildlife Service (KWS) for the scientific support. We are

grateful to Ms. Ellen Bermann for hospitality and for technical

support. Finally we express our gratitude to Francesca Benzoni

for her support and help throughout the study.

References

Baker, A. C., 2003. Flexibility and specificity in coral–algal

symbiosis: diversity, ecology and biogeography of Sym-

biodinium. Annual Review of Ecological System 34:

661–689.

Brown, B. E., 1997. Coral bleaching: causes and consequences.

Coral Reefs 16: 129–138.

Clarke, K. R. & R. N. Gorley, 2001. PRIMER v5 user manual/

tutorial. PRIMER-E Ltd., Plymouth.

Coles, S. L. & B. E. Brown, 2003. Coral bleaching-capacity for

acclimatization and adaption. Advance in Marine Biology

46: 183–223.

Fitt, W. K., B. E. Brown, M. E. Warner & R. P. Dunne, 2001.

Coral bleaching: interpretation of thermal tolerance limits

and thermal thresholds in tropical corals. Coral Reefs 20:

51–65.

Hydrobiologia (2010) 655:99–108 107

123

Gleason, M. G., 1993. Effects of disturbance on coral com-

munities: bleaching in Moorea, French Polynesia. Coral

Reefs 12: 193–201.

Glynn, P. W., 1990. Coral mortality and disturbances to coral

reefs in the tropical eastern Pacific. In Glynn, P. W. (ed.),

Global Ecological Consequences of the 1982–83 El Nino-

Southern Oscillation. Elsevier, Amsterdam: 55–126.

Glynn, P. W., 1993. Coral-reef bleaching-ecological perspec-

tives. Coral Reefs 12: 1–17.

Hoegh-Guldberg, O., 1999. Climate change, coral bleaching

and the future of the world’s coral reefs. Marine Fresh-

water Research 50: 839–866.

Hoegh-Guldberg, O. & B. Salvat, 1995. Periodic mass bleaching

of reef corals along the outer reef slope in Moorea, French

Polynesia. Marine Ecology Progress Series 121: 181–190.

Hoegh-Guldberg, O. & G. J. Smith, 1989. The effect of sudden

changes in temperature, irradiance and salinity on the

population density and export of zooxanthellae from the

reef corals Stylophora pistillata (Esper 1797) and Seria-

topora hystrix (Dana 1846). Experimental Marine Biology

and Ecology 129: 279–303.

Hughes, T. P., A. H. Baird, D. R. Bellwood, M. Card, S.

R. Connoly, C. Folke, R. Grosberg, O. Hoegh-Guldberg,

J. B. C. Jackson, J. Kleypas, J. M. Lough, P. Marshall, M.

Nystrom, S. R. Palumbi, J. M. Pandolfi, B. Rosen & J.

Roughgarden, 2003. Climate Change, human impacts, and

the resilience of coral reefs. Science 301: 929–933.

Jokiel, P. L. & S. L. Coles, 1990. Response of Hawaiian and

other Indo-Pacific reef corals to elevated temperature.

Coral Reefs 8: 155–162.

Kaunda-Arara, B. & G. A. Rose, 2004. Effects of marine reef

National Parks on fishery CPUE in coastal Kenya. Bio-

logical Conservation 118: 1–13.

Kayanne, H., S. Harii, Y. Ide & F. Akimoto, 2002. Recovery of

coral populations after the 1998 bleaching on Shiraho

Reef, in the southern Ryukyus, NW Pacific. Marine

Ecology Progress Series 239: 93–103.

Loya, Y., K. Sakai, K. Yamazato, Y. Nakano, H. Sambali & R.

van Woesik, 2001. Coral bleaching: the winners and the

losers. Ecology Letters 4: 122–131.

Marshall, P. A. & A. H. Baird, 2000. Bleaching of corals on the

Great Barrier Reef: differential susceptibilities among

taxa. Coral reefs 19: 155–163.

McClanahan, T. R., 1988. Seasonality in East Africa’s coastal

waters. Marine Ecology Progress Series 44: 191–199.

McClanahan, T. R., 2004. The relationship between bleaching

and mortality of common corals. Marine Biology 144:

1239–1245.

McClanahan, T. R., A. H. Baird, P. A. Marshall & M.

A. Toscano, 2004. Comparing bleaching and mortality

responses of hard corals between southern Kenya and the

Great Barrier Reef, Australia. Marine Pollution Bulletin

48: 327–335.

McClanahan, T. R., M. Atewebheran, C. Muhando, J. Maina &

S. Mohammed, 2007. Effects of climate and seawater

temperature variation on coral bleaching and mortality.

Ecological Monographs 77(4): 503–525.

McClanahan, T. R., M. Ateweberhan & J. Omukoto, 2008.

Long-term changes in coral colony size distributions on

Kenyan reefs under different management regimes and

across the 1998 bleaching event. Marine Biology 153:

755–768.

Obura, D., 1995. Environmental stress and life history strategies,

a case study of corals and river sediment from Malindi,

Kenya. PhD thesis, University of Miami, Miami, FL.

Obura, D., 2001. Can differential bleaching and mortality

among coral species offer useful indicators for assessment

and management of reefs under stress? Bulletin of Marine

Science 6: 421–442.

Obura, D., 2005a. Resilience and climate change: lessons from

coral reefs and bleaching in the Western Indian Ocean.

Estuarine, Coastal and Shelf Science 63(3): 353–72

Obura, D., 2005b. Kenya, coral reef resilience studies. In

Souter, D., O. Linden, D. Wilhemsson, D. Obura & D

(eds), Coral Reef Degradation in the Indian Ocean. Status

Reports 2005. CORDIO/SAREC Marine Science Pro-

gram, Stockholm: 25–31.

Obura, D., 2009a. Reef corals bleach to resist stress. Marine

Pollution Bulletin 58: 206–212.

Obura, D., 2009b. Bleaching as a life history trait in coral-zoo-

xanthellae holobionts—relevance to acclimatization and

adaptation. In Proceedings of the 11th International Coral

Reef Symposium, Ft. Lauderdale, FL, 7–11 July 2008.

Siebeck, U. E., N. J. Marshall, A. Kluter & O. Hoegh-Guld-

berg, 2006. Monitoring coral bleaching using a colour

reference card. Coral Reefs 25: 453–460.

108 Hydrobiologia (2010) 655:99–108

123