Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs

REVIEW

Assessing the ‘deep reef refugia’ hypothesis:focus on Caribbean reefs

P. Bongaerts • T. Ridgway • E. M. Sampayo •

O. Hoegh-Guldberg

Received: 25 February 2009 / Accepted: 17 December 2009 / Published online: 27 January 2010

� Springer-Verlag 2010

Abstract Coral reefs in shallow-water environments

(\30 m) are in decline due to local and global anthropogenic

stresses. This has led to renewed interest in the ‘deep reef

refugia’ hypothesis (DRRH), which stipulates that deep reef

areas (1) are protected or dampened from disturbances that

affect shallow reef areas and (2) can provide a viable

reproductive source for shallow reef areas following dis-

turbance. Using the Caribbean as an example, the assump-

tions of this hypothesis were explored by reviewing the

literature for scleractinian corals—the reef framework

builders on tropical reefs. Although there is evidence to

support that deep reefs ([30 m) can escape the direct effects

of storm-induced waves and thermal bleaching events, deep

reefs are certainly not immune to disturbance. Additionally,

the potential of deep reefs to provide propagules for shallow

reef areas seems limited to ‘depth-generalist’ coral species,

which constitute only *25% of the total coral biodiversity.

Larval connectivity between shallow and deep populations

of these species may be further limited due to specific life

history traits (e.g., brooding reproductive strategy and ver-

tical symbiont acquisition mode). This review exposes how

little is known about deep reefs and coral reproduction over

depth. Hence, a series of urgent research priorities are pro-

posed to determine the extent to which deep reefs may act as

a refuge in the face of global reef decline.

Keywords Deep coral reef � Refugia � Mesophotic �Global climate change � Disturbance

Introduction

Coral reef communities have shown a remarkable persis-

tence in taxonomic composition and diversity over at least

the past 500,000 years (Pandolfi 2002). In the last 30 years,

however, there has been an unprecedented decline in the

distribution and abundance of coral communities (Pandolfi

2002; Gardner et al. 2003; Bruno and Selig 2007) with

approximately 26% of the remaining coral reefs now

considered to be under immediate or long-term threat

(Wilkinson 2004). The decline of coral communities has

been attributed to local factors such as over-fishing of key

functional groups, declining water quality, and the physical

degradation of coral reefs by human activities such as

destructive fishing and unsustainable tourism. Moreover,

rising atmospheric greenhouse gas concentrations pose a

major threat to coral reefs principally through (1) global

warming, which has dramatically increased incidences of

mass coral bleaching and subsequent mortality events and

(2) acidification of ocean waters, causing a decrease in

Communicated by Guest Editor Dr. John Marr

P. Bongaerts (&) � T. Ridgway � E. M. Sampayo �O. Hoegh-Guldberg

Centre for Marine Studies, and ARC Centre of Excellence for

Coral Reef Studies, The University of Queensland, St Lucia,

QLD 4072, Australia

e-mail: [email protected]

P. Bongaerts

CARMABI Research Institute, Piscaderabaai z/n, PO Box 2090,

Willemstad, Curacao

Present Address:T. Ridgway

Climate Change Group, Great Barrier Reef Marine park

Authority, Townsville, QLD 4810, Australia

Present Address:E. M. Sampayo

Department of Biology, Pennsylvania State University,

University Park, PA 16802, USA

123

Coral Reefs (2010) 29:309–327

DOI 10.1007/s00338-009-0581-x

coral growth and calcification rates (Kleypas et al. 1999;

Hoegh-Guldberg et al. 2007; Cooper et al. 2008; Bak et al.

2009; De’ath et al. 2009). Current estimates of climatic

changes dwarf even the fastest rates of change during the

glacial cycles of the past 420,000 years, which are 2–3

orders of magnitude slower that that seen over the past

100 years (Hoegh-Guldberg et al. 2007).

The extent to which reefs are affected by environmental

stressors is not uniform, and specific areas/zones may be

able to (partially) escape certain disturbances. Such zones

may constitute refugia (where species can survive during

periods of adverse conditions elsewhere) and may play an

important role in the recovery of impacted reef areas

(Ridgway and Hoegh-Guldberg 2002; Hoegh-Guldberg

et al. 2008). In particular, the observation that some areas are

less affected by global thermal stress events, due to cooler or

more stable conditions, has led to the idea that these areas

may act as thermal refugia for corals (Vermeij 1986; Glynn

1996; Riegl and Piller 2003; Halfar et al. 2005). According

to Glynn (1996), potential refugia include areas exposed to

cool upwelling conditions, high-latitude communities,

ocean banks or island shores, and moderate to deep reef

ecosystems.

The ‘deep reef refugia’ hypothesis (DRRH) has gained in

popularity in the recent literature (Hughes and Tanner 2000;

Feingold 2001; Glynn et al. 2001; West and Salm 2003;

Riegl and Piller 2003; Armstrong et al. 2006; Venn et al.

2009; Lesser et al. 2009a; Hinderstein et al. 2010). Glynn

(1996), who first postulated this hypothesis, highlighted that

deeper reefs are less affected by thermal stress events and

thus have the potential to act as refugia. However, the

refugia potential might not be limited to avoiding elevated

seawater temperatures as the intensity of other stressors,

such as storm-induced waves, is also negatively correlated

with depth (Liddell and Ohlhorst 1988). With the recent

evidence pointing to coral populations being largely self-

seeding and more closed than previously thought (Ayre and

Hughes 2000; Baums et al. 2005; Underwood et al. 2007;

and references therein), the potential of deep reefs to act as a

local recruitment source for the shallow has become an

integrated part of the DRRH (Hughes and Tanner 2000;

Lesser et al. 2009a).

Given the increasing pressure on coral reefs and the

recent scientific findings on coral population connectivity,

coupled with the recent interest in deeper coral communi-

ties, the purpose of this paper is twofold. First, it reviews the

current understanding of the potential role of deeper reefs as

(reproductive) refugia for scleractinian corals, and secondly,

it provides a guide for future research directions. In doing so,

the underlying assumptions of the DRRH are explored,

which stipulate that deep reef areas (1) are protected or

dampened from disturbances that affect shallow reef areas

and (2) can provide a viable reproductive source for shallow

reef areas following disturbance. Despite deeper tropical

reef communities occurring in the Pacific and Indian Oceans

(e.g., Fricke and Schuhmacher 1983; Maragos and Jokiel

1986; Kahng and Kelley 2007), the present study focuses

specifically on the relatively well-documented deep reefs of

the Caribbean in the Western Atlantic (e.g., Goreau and

Goreau 1973; Bak 1977; Van den Hoek et al. 1978; Bak and

Luckhurst 1980; Fricke and Meischner 1985; Bak and

Nieuwland 1995; Bak et al. 2005; Jarrett et al. 2005; Arm-

strong et al. 2006; Culter et al. 2006) to evaluate these

assumptions. Finally, critical information gaps are high-

lighted, and potential future research directions are

presented.

Deep reefs in the Caribbean

To accurately evaluate the potential of deep reefs to act as

refugia, it is important to first consider the abundance and

particular physical characteristics that govern deep Carib-

bean coral communities. At the outset, it is imperative to

define the somewhat relative (and subjective) term ‘deep

reef’ in order to overcome potential confusion between

terms such as ‘deep-water reef’ and ‘deep-sea reef’, which

have been used in the past to refer to both cold-water and

non-phototrophic systems as well as warm-water and light-

dependant coral ecosystems. In this respect, the term

‘mesophotic’, which was traditionally used to describe the

depth range of Halimeda bioherms (Pomar 2001), may be

particularly useful and has recently been adopted to refer to

deep but light-dependent coral ecosystems (Armstrong et al.

2006; Menza et al. 2007; Hinderstein et al. 2010). Although

a technical definition for ‘mesophotic’ is still lacking in the

coral literature, it is loosely defined as the depth range

between 30 m and the depth at which light in the water

column is too low to sustain the growth of corals that depend

on their phototrophic obligate symbionts (dinoflagellates of

the genus Symbiodinium). In the Caribbean, this lower depth

limit is often around 80 m (Kahng et al. 2010), even though

in some locations with exceptionally clear water, it may

extend down to *100 m (Reed 1985; Liddell and Ohlhorst

1988).

Even though information is scarce, it is possible to make

some general observations about the distribution and

occurrence of mesophotic reefs. The environmental condi-

tions (e.g., temperature, salinity, nutrients, light availability,

and aragonite saturation state) required for coral reefs to

accrete net amounts of carbonate over time are outlined in

Kleypas et al. (1999). Some of these parameters (principally

temperature, light, and nutrients) can be depth dependent,

and the geographic distribution of mesophotic coral com-

munities does, therefore, not necessarily overlap with areas

that sustain shallow coral reef communities. The majority of

310 Coral Reefs (2010) 29:309–327

123

coral reefs occur in tropical seas at depths of less than 30 m

(Huston 1985), and this is predominantly driven by the

reduction in light availability with depth. The euphotic zone,

defined as the depth range to which sufficient light is

available to support photosynthetic activity, determines the

lower depth limit of hermatypic corals. The actual depth

range of the euphotic zone varies between locations in the

Western Atlantic depending on local light attenuation

coefficients (Kleypas et al. 1999; Kahng et al. 2010), which

are determined by the concentrations of dissolved organic

matter, phytoplankton, and sediment loads in the water. For

example, the euphotic depth in Curacao and southwest

Florida ranges from 60 to 75 m (Van den Hoek et al. 1978;

Jarrett et al. 2005), whereas the clearer, oceanic waters off

Bermuda support a euphotic depth of [100 m (Fricke and

Meischner 1985).

Scleractinian corals at mesophotic depths often exhibit

flat, plate-like morphologies to maximize light capture

(Titlyanov 1987; Merks et al. 2004) and may utilize dif-

ferent symbionts to cope with the environmental light field

(intensity and spectral quality) of deeper reef zones (Igle-

sias-Prieto and Trench 1997; Iglesias-Prieto et al. 2004;

Sampayo et al. 2007; Frade et al. 2008). Despite these

adaptations to maximize light use, the total contribution of

photosynthesis to calcification is reduced in mesophotic

corals (McCloskey and Muscatine 1984). Although this

deficit may be supplemented with heterotrophic feeding

(McCloskey and Muscatine 1984; Mass et al. 2007; Ala-

maru et al. 2009; Lesser et al. 2009b), facilitated by the

influx of deep nutrient-rich oceanic waters at greater depths

(Leichter et al. 1996; Leichter and Genovese 2006), total

reef accretion is negatively correlated with increasing depth

(Grigg 2006).

The formation of mesophotic reefs is further influenced

by the presence of thermoclines and the availability of

suitable substrate. Strong shallow thermoclines (of several

degrees Celsius) can prevent the development of mesoph-

otic coral communities at locations where healthy shallow

communities exist (e.g., Northwest Hawaiian Archipelago;

Grigg 2006), but such thermal stratification of the water

column is usually restricted to higher latitudes and has not

yet been documented for the tropical reefs of the Caribbean.

In contrast, the availability of hard substrate has been indi-

cated as an important limiting factor in the formation of

Caribbean deep reef communities (Bak 1977). The substrate

supporting most mesophotic coral communities consists of

limestone structures deposited during the late Pleistocene or

early Holocene but also frequently consists of rhodolith

banks (Fricke and Meischner 1985; Littler et al. 1991;

Garcıa-Sais et al. 2008; Rivero-Calle et al. 2009), which

provide suitable hard substrate when agglutinated into solid

banks by red coralline algae (Fricke and Meischner 1985).

Even though light and substrate conditions may favor the

formation of mesophotic coral communities, the accumu-

lation of sediment often prevents the growth of sessile

organisms (Goreau and Goreau 1973) before light becomes

limiting (Bak 1977). Substrate limitation due to sediment

accumulation generally does not play a role on the vertical

walls that are common in the Caribbean on most fore-reef

slopes in excess of 50–60 m (Liddell and Ohlhorst 1988),

with the exception of localized areas where sediment

accumulates into sand channels or chutes (Hubbard 1989).

However, near-vertical reef profiles receive lower irradi-

ances relative to low-angle substrates (Brakel 1979) and

only certain species can successfully grow on these steep,

vertical walls (Liddell and Ohlhorst 1988).

An accurate assessment of the distribution and abundance

of mesophotic reef areas and their relative contribution to

total coral reef surface area is currently restricted due to the

lack of large-scale mapping studies that include deeper

habitats. Nonetheless, mesophotic coral ecosystems have

been reported throughout the Caribbean, including the

Bahamas (Porter 1973), Barbados (Macintyre et al. 1991),

Bermuda (Fricke and Meischner 1985), Curacao (Bak

1977), Florida (Jarrett et al. 2005), Jamaica (Goreau and

Goreau 1973), Puerto Rico (Garcıa-Sais et al. 2008) and the

US Virgin Islands (Armstrong et al. 2006). Recent techno-

logical advances in multibeam sonar, remotely operated

vehicles (ROVs), and autonomous underwater vehicles

(AUVs) do, however, provide the means to map deep reefs

on a large scale (with a limitation of the high costs

involved), and initial mapping efforts have revealed exten-

sive areas of mesophotic coral bank ecosystems on the

Puerto Rican shelf (Armstrong 2007; Menza et al. 2007;

Rivero-Calle et al. 2009), with an estimated area of 300 km2

for the mesophotic reef complex located south of the

northern Virgin Islands (Smith et al. 2010). Similarly, large

areas of mesophotic ecosystems are expected to occur

elsewhere in the Caribbean, either as submerged banks (e.g.,

the Saba Bank; Van der Land 1977; Toller et al. 2008) or as

part of the many fringing and barrier reef systems that occur

directly adjacent to deep oceanic water.

Deep reefs as refugia for episodic disturbances

Disturbances and threats to coral reefs have received con-

siderable attention over the past decade, but when consid-

ering the potential of mesophotic reefs to act as refugia, it is

critical to determine the depth to which disturbances extend.

Some episodic stressors may act indiscriminately over the

entire euphotic depth range, whereas the effect of others

may be limited to a certain depth range or diminish as depth

increases. Despite a wealth of information in the scientific

literature on the effects of disturbances on shallow-water

coral reefs, only limited accounts can be found for deeper

Coral Reefs (2010) 29:309–327 311

123

Ta

ble

1R

epo

rted

dis

turb

ance

sin

the

Car

ibb

ean

for

wh

ich

the

effe

cto

nth

ed

eep

reef

([3

0m

)h

asb

een

asse

ssed

Dis

turb

ance

Tim

eo

fo

ccu

rren

ceL

oca

tio

nC

itat

ion

Dep

thra

ng

e

asse

ssed

(m)

Dep

thra

ng

e

affe

cted

(m)

Co

mm

ent

Sto

rmev

ents

Hu

rric

ane

Ger

ta1

97

8B

eliz

eH

igh

smit

het

al.

(19

80

)*

0–

30

0–

25

Dam

age

was

evid

ent

ov

erth

een

tire

dep

thra

ng

e,ex

cep

t

[2

5m

on

the

fore

-ree

fsl

op

e

Hu

rric

ane

All

en1

98

0Ja

mai

caW

oo

dle

yet

al.

(19

81)

0–

50

0–

14

Mo

std

amag

elo

cali

zed

on

shal

low

reef

(\1

5m

);h

ow

ever

,

dam

age

was

app

aren

td

ow

nto

50

m

Hu

rric

anes

Gil

ber

tan

d

Joan

19

88

–1

98

9B

on

aire

Ko

blu

kan

dL

yse

nk

o(1

99

2)

1.5

–3

71

1–

20

Dam

age

vis

ible

bel

ow

[2

0m

,b

ut

reef

mo

staf

fect

edat

inte

rmed

iate

dep

ths

Hu

rric

ane

Hu

go

/sed

imen

t

tran

spo

rt

19

89

–1

99

0U

SV

irg

inIs

lan

ds

(St.

Cro

ix)

Hu

bb

ard

(19

92

),

Aro

nso

net

al.

(19

94

)

8–

34

8–

34

As

are

sult

,co

ral

cov

erd

ecli

ned

do

wn

to3

4m

(ho

wev

er,

[2

7m

A.

lam

arc

kiw

asth

eo

nly

com

mo

nco

ral)

Hu

rric

ane

Len

ny

/

sed

imen

ttr

ansp

ort

19

99

Bo

nai

reB

aket

al.

(20

05

)*

0–

40

[3

0M

ort

alit

yh

igh

est

(40

%)

inco

rals

wit

ha

pla

te-l

ike

mo

rph

olo

gy

Hu

rric

ane

Rit

a2

00

5–

20

06

Flo

wer

Gar

den

Ban

ks

and

vic

init

y

Ro

bb

art

etal

.(2

00

9)

22

–6

0*

22

–4

0M

od

erat

ed

amag

eo

bse

rved

do

wn

to4

0m

on

the

Eas

t

Flo

wer

Gar

den

Ban

ks,

bu

tm

ost

lyli

mit

edto

shal

low

area

s

\3

0m

Dis

ease

ou

tbre

aks

Pre

val

ence

of

cora

l

dis

ease

s

20

03

–2

00

5U

SV

irg

inIs

lan

ds

Cal

nan

etal

.(2

00

8),

Sm

ith

etal

.(2

00

8)

5–

42

5–

42

Dis

ease

pre

val

ence

acro

ssd

epth

s,w

ith

pre

do

min

antl

y

wh

ite

syn

dro

me

and

yel

low

blo

tch

on

the

dee

pre

ef

Ou

tbre

ako

fw

hit

e

syn

dro

me

20

05

–2

00

7F

low

erG

ard

en

Ban

ks

Hic

ker

son

etal

.(2

00

8)

?[*

20

Par

tial

mo

rtal

ity

reco

rded

in2

00

7

Ou

tbre

ako

f‘‘

inte

rco

stal

mo

rtal

ity

syn

dro

me’

’

20

07

US

Vir

gin

Isla

nd

s

(HB

-MC

D)

Sm

ith

etal

.(2

01

0)

*2

5–

50

0–

14

Dis

ease

larg

ely

abat

edb

y2

00

8

Alg

al

blo

om

s

Alg

alb

loo

ms

(Co

diu

msp

.)

19

89

–1

99

5F

lori

da

(SE

)L

apo

inte

( 19

97),

Lap

oin

teet

al.

(20

05

)

?2

4–

43

Blo

om

so

fth

ech

loro

ph

yte

Co

diu

mis

thm

ocl

ad

um

dri

ven

by

lan

d-b

ased

nu

trie

nt

dis

char

ges

(sew

age)

Alg

alb

loo

ms

(Ca

ule

rpa

spp

.)

19

98

–2

00

4F

lori

da

(SE

)L

apo

inte

and

Yen

tsch

,

per

son

alco

mm

un

icat

ion

0–

50

20

–5

0B

loo

ms

of

Ca

ule

rpa

spp

.d

riv

enb

yla

nd

-bas

edn

utr

ien

t

dis

char

ges

(sew

age)

Co

ral

ble

ach

ing

Co

ral

ble

ach

ing

even

t

(war

m-w

ater

)

19

87

–1

98

8B

aham

asL

ang

etal

.(1

98

8)

0–

91

0–

60

Ble

ach

ing

ob

serv

edd

ow

nto

60

m;

late

rsu

rvey

sal

so

rev

eale

dso

me

ble

ach

ing

[6

5m

Co

ral

ble

ach

ing

even

t

(war

m-w

ater

)

19

87

–1

98

8P

uer

toR

ico

Bu

nk

ley

-Wil

liam

set

al.

(19

91)

0–

89

0–

60

Ble

ach

ing

ob

serv

edd

ow

nto

60

mo

ver

ad

epth

ran

ge

of

89

m

Co

ral

ble

ach

ing

even

t

(co

ld-w

ater

)

19

96

–1

99

8C

ura

cao

Bak

etal

.(2

00

5)

*0

–4

0[

30

Ble

ach

ing

of

Ag

ari

cia

spp

.o

nth

ed

eep

reef

sug

ges

ted

tob

e

rela

ted

toco

ld-w

ater

ble

ach

ing

Un

iden

tifi

ed

Ex

ten

siv

ere

cen

tco

ral

mo

rtal

ity

20

04

–2

00

5U

SV

irg

inIs

lan

ds

Men

zaet

al.

(20

07

)3

0–

40

37

–4

0R

ecen

tm

ort

alit

yev

ent

ind

icat

edb

yal

gal

turf

on

dea

dco

ral

(lo

sso

fco

ral

cov

eres

tim

ated

at2

5%

)

312 Coral Reefs (2010) 29:309–327

123

coral communities (Table 1). Processes that reduce the

presence of coral reefs can be natural and anthropogenic,

and their impacts range from local to global depending on

scale and intensity.

Natural disturbances

Over the past decades, storm events and disease outbreaks

have strongly influenced coral reefs worldwide (Connell

1997). Storms are a common feature throughout the Carib-

bean, and the effects of storms on coral reef communities in

relation to depth are relatively well documented (Banner

1961; Stoddart 1962; Glynn et al. 1964; Woodley et al.

1981; Rogers et al. 1982, 1983; Kjerfve et al. 1986; although

few studies assess damage at depths[30 m, Table 1). These

data indicate that mesophotic reef areas are largely sheltered

from direct physical damage of storm-induced waves but are

not spared from indirect effects (e.g., debris avalanches or

sedimentation). Coral debris originating from storm impacts

can be transported down the reef slope, causing damage to

deeper coral assemblages (Dollar 1982), and this process is

correlated with the angle of the reef slope. For example, in

French Polynesia (Harmelin-Vivien and Laboute 1986),

following the 1982/1983 hurricane season, large reef areas

between 30 and 90 m with steep reef slope angles ([45�)

suffered high mortality through debris avalanches, while

reefs with low-angle slopes (\25�) in the same location were

only damaged in the shallows. Besides damage from coral

debris, storms can cause transport of fine sediments from the

shallows into the mesophotic sections (Hubbard 1992),

especially on fringing reefs bordering artificial sand beaches

(Nagelkerken 2006). Fine sediments smother coral colonies

and can cause significant mortality on deeper coral com-

munities (Bak et al. 2005). Substrate and community

structure of the deep reef is an additional consideration,

because taxa with thin skeletal features such as Agaricia

spp., which are often dominant on deep reef slopes, are

somewhat more fragile and less adept at removing sediment

compared to the hard plates formed by members of the

Montastraea annularis species complex that dominate

submerged banks (Smith et al. 2010). Finally, hurricane-

related pressure on Caribbean reef systems may play a

greater role over time given that a 0.5�C increase in sea

surface temperature is predicted to increase hurricane

intensity and frequency in the Caribbean (Webster et al.

2005; Saunders and Lea 2008). Despite this, the limited

accounts on storm-related damage to mesophotic depths

(Table 1) suggest that the direct effects of storm damage

will generally always be greatest on shallower reef sections.

Disease forms part of the natural cycle of reef-building

corals, but its abundance and prevalence within the marine

environment can be amplified by anthropogenic influences.

For example, stress may lower disease resistance, and the

frequency of coral disease is projected to increase, as sea

temperatures and/or local anthropogenic stresses increase

(Harvell et al. 1999; Selig et al. 2006). As most coral dis-

eases are host specific, their distribution over the reef slope

is generally limited to the depth range of the coral host. For

example, the outbreak of white-band disease on Caribbean

Acropora in the 1980s and 1990s was limited to the shallows

due to the restriction of Acropora to shallow water (Aronson

and Precht 2001). Besides the outbreak of ‘‘intercostal

mortality syndrome’’ in the US Virgin Islands (Smith et al.

2010), which was confined to deeper basin habitats

([35 m), other recent reports of coral disease along depth

gradients (Calnan et al. 2008; Smith et al. 2008) do not show

depth-specific disease prevalence in species with a broad

depth distribution. Several coral diseases such as black band

disease, dark spots disease, white syndrome, and yellow

blotch (band) disease were first documented in shallower

reefs but have since been reported on mesophotic reef sec-

tions (Table 1).

Few cases of invasive species have been documented in

the Caribbean, and deleterious invasions such as those

reported for temperate regions have yet to be reported

(Coles and Eldredge 2002; Wilkinson 2004). Despite the

fact that Caribbean reefs were hit somewhat harder hit by

disease compared to their Indo-Pacific counterparts (Weil

2004), they have been less impacted by predatory species

(e.g., Acanthaster planci and Drupella outbreaks; Colgan

1987; DeVantier and Deacon 1990; Turner 1994). The Indo-

Pacific lionfish (Pterois spp.) and the ahermatypic coral

Tubastrea coccinea are recent examples of invasive species

that have successfully radiated throughout the Caribbean

(Fenner and Banks 2004; Whitfield et al. 2007; Green and

Cote 2009). T. coccinea occurs over a large depth range, but

its distribution (and hence impact) is presently restricted to

cryptic and artificial habitats (Vermeij 2005). The threat of

the lionfish is currently considered to be restricted to fish

communities (Albins and Hixon 2008; Green and Cote

2009) but could potentially have an indirect impact (e.g.,

increase in algal growth), particularly on the shallow coral

community, through increased predation of juvenile her-

bivorous fish.

Local anthropogenic disturbances

The proximity of a coral reef to land-based disturbances is

directly related to the level of exposure to nutrient

enrichment, influx of toxins (such as herbicides and pesti-

cides), and sedimentation (Menza et al. 2008; Smith et al.

2008). The differential effect of these stressors over depth

has not been well described, although sedimentation is

perhaps an exception in that it affects coral communities by

reducing the amount of light and available substrate as well

as interfering with photosynthesis and feeding. Sediments

Coral Reefs (2010) 29:309–327 313

123

can smother coral colonies, even though corals may

employ several physiological and behavioural avoidance

strategies (Stafford-Smith and Ormond 1992). Colony and

calyx morphologies play important roles in the passive

removal of sediment, with dome-shaped colony morphol-

ogy, and large polyps being particularly efficient at

removing large particles (Hubbard and Pocock 1972). As a

response to lower light levels, most mesophotic reef corals

tend to have a flat plate-like morphology that traps sedi-

ment, and although this increased susceptibility to sedi-

mentation is normally not problematic due to the relatively

lower rates of sedimentation on the deeper reef (Bak and

Engel 1979; Smith et al. 2008), increased sediment levels

(due to storm activity) have been reported to result in large-

scale mortality among mesophotic corals (Bak et al. 2005).

Nutrient enrichment adversely affects shallow reefs by

fueling blooms of macroalgae and phytoplankton. Such

blooms can be particularly catastrophic in combination

with other stressors such as hurricanes and elimination of

herbivores by overfishing (Hughes and Connell 1999).

Increased macroalgal growth leads to an intensified com-

petition for space and reduces survivorship of coral recruits

(Bak and Engel 1979; Hunte and Wittenberg 1992; Ver-

meij 2006), while phytoplankton blooms decrease light

availability for corals and other benthic organisms (Hallock

and Schlager 1986). Isolated examples such as blooms of

low-light-adapted macroalgae (e.g., Codium isthmocladum

and Caulerpa spp.) have been reported on deep reefs (20–

50 m) in Florida (Lapointe 1997; Lapointe et al. 2005;

Lapointe and Yentsch pers. comm. Table 1). Additionally,

in some instances, sewage outflow is discharged directly

onto deep reef communities resulting in deep-water-

restricted nutrient enrichment (Proni et al. 1994). Given

that light is already limiting on mesophotic reefs, a further

reduction in available irradiance through nutrient levels,

macroalgae, and phytoplankton blooms has the potential to

affect the viability of deeper light-dependent communities.

The overexploitation of key fish species is one of the

most direct anthropogenic disturbances that impact coral

reef ecosystems (Jackson et al. 2001; Hughes et al. 2007;

Stallings 2009). Whether or not it has a depth-related

component is unclear, although near-shore fishing intensi-

ties are usually more pronounced in the shallows (e.g.,

Polunin and Roberts 1993). Not only the intensity of fish-

ing is important, but also the species that are targeted at the

different sections of the reef. For example, herbivory

diminishes with depth (Hay et al. 1983; Brokovich et al.

2010) and key grazers, such as parrotfish and damselfish

species are usually restricted to the shallower reef (\30 m;

Liddell and Avery 2000). Thus, the removal of herbivorous

fishes might not have such deleterious effects on the deep

reef but has significant effects on ecosystem functioning of

shallow reefs (Jackson et al. 2001). This has also become

apparent during the mass mortalities of the Caribbean sea

urchin Diadema antillarum (Lessios 1988), which had

major impacts only on shallower zones, due to D. antilla-

rum’s predominance as an herbivore at these depths

(Morrison 1988). Finally, a range of other local anthropo-

genic disturbances, such as diving and snorkeling-related

activities, spear fishing, and ship groundings are largely

restricted to shallow reef sections.

Global anthropogenic disturbances

Sea surface temperature increases, or anomalies cause mass

coral bleaching events that have been responsible for the

significant mortality of reefs worldwide over the past two

decades (Hoegh-Guldberg 1999; Hoegh-Guldberg et al.

2007). Coral bleaching is mainly caused by elevated tem-

peratures but is exacerbated by high irradiance levels

(Jokiel and Coles 1977). Coral bleaching has been reported

down to 30–60 m of depth (Bak et al. 2005; Bunkley-

Williams et al. 1991; Lang et al. 1988), but the effects

of warm-water bleaching are generally considered to be

more pronounced in shallow water (Fisk and Done 1985;

Wilkinson and Souter 2008).

The bathymetric effect of bleaching susceptibility can

be explained through the relatively homogenous and tem-

porally stable irradiances beyond 30–40-m depth (Vermeij

and Bak 2002). Also, the thermal regimes between shallow

and deep reefs can be markedly different, due to the pulsed

delivery of oceanic sub-thermocline water to the deeper

reef sections. This phenomenon is common on reefs loca-

ted adjacent to deep oceanic water (such as the many

fringing reef slopes of the Caribbean) (Leichter et al. 1996;

Bak et al. 2005; Leichter and Genovese 2006; Lesser et al.

2009a), and although these influxes may cause higher

temperature variability in deep water, long-term averages

and maximum temperatures remain lower compared to the

shallows (Frade et al. 2008). Examples of this differential

include a 1�C difference in average summer temperature

between the shallow (5–7 m) and deep (35–40 m) deep

reef in the Florida Keys (Leichter et al. 1996) and Curacao

(Frade et al. 2008) but can be substantially greater (i.e.,

[1�C difference) over broader depth ranges (Bak et al.

2005; Lesser et al. 2009a). Given that exposures to tem-

peratures 1–2�C higher than the long-term monthly average

have repeatedly led to mass coral bleaching events (Hoegh-

Guldberg 1999), the regular cold-water influxes on deeper

reefs may indeed offer an escape from thermal stress.

Nonetheless, bleaching susceptibility varies between spe-

cies and across environmental gradients due to acclimation/

adaptation to different thermal regimes (Coles and Brown

2003), and shallow corals may exhibit a broader thermal

tolerance (Birkeland 1997). Additionally, extensive cooling

of deeper water can lead to so-called coldwater bleaching

314 Coral Reefs (2010) 29:309–327

123

as observed in Bonaire (Kobluk and Lysenko 1994) and the

US Virgin Islands (Menza et al. 2007). Thus, although

there are indeed more studies that report bleaching at

shallow (rather than deep) reef sections, the general view

that bleaching is usually restricted to shallow water should

be interpreted with caution due to the lack of quantitative

bleaching studies over large depth ranges.

Finally, global warming is driving increases in sea level

as a result of the thermal expansion of seawater and the

melting of ice trapped in landlocked glaciers and ice sheets.

The Intergovernmental Panel on Climate Change (IPCC)

consequently has predicted sea level rises of 18–59 cm

during the twenty-first century (IPCC 2007). Recent changes

in the arctic ice sheet plus growing evidence from other

sources have shown that IPCC projections for sea level rise

are conservative, and that sea levels will increase by at least

1 m by 2100 (Rahmstorf et al. 2007). Even though vertical

reef accretion rates have kept up with rapidly rising sea

levels in the geological past, coral reefs have also ‘drowned’,

vanishing into the aphotic zone when accretion rates fall

behind rising sea level rates (Grigg and Epp 1989). Projected

sea level changes, therefore, have the potential to push deep

reefs below the euphotic zone (Brown 1997), especially

when increased thermal stress and ocean acidity simulta-

neously reduce coral growth rates (Cooper et al. 2008).

Deep reefs as a source of propagules for shallow areas

The ability of deeper sections of coral reefs to supply

recruits to shallow reef areas has become a central

assumption within the DRRH. Recovery from disturbances

depends largely on the recruitment of larvae from either

local or distant sources, and the availability of such larval

sources is therefore crucial (Hughes and Tanner 2000).

Recent genetic evidence demonstrates that many coral

populations are largely self-seeding (see Ayre and Hughes

2000; Baums et al. 2005; and references therein), and larval

dispersal can be as low as 100 m in some species

(Underwood et al. 2007), which challenges the idea that

reef systems may be rapidly repopulated from external

larval sources after adult populations have declined. Deep

reefs can only act as a (local) reproductive source for the

shallow if (1) sufficient overlap exists in community

structure between the shallow and deep and (2) sufficient

larval exchange occurs from deep to shallow communities.

Coral community structure over depth

The mesophotic reefs of the Caribbean exist as extensions of

the shallow reef slope or as isolated coral dominated com-

munities on deep submerged plateaus or ridges (e.g., Flower

Garden Banks (Gulf of Mexico) and the Puerto Rican Shelf).

When forming part of a slope, the deeper reef typically

shows a gradual depth zonation, progressing from moderate

coral cover to a few isolated colonies in deeper water. In

terms of coral biodiversity, the general trend is increasing

species richness from the surface to an intermediate depth,

followed by a continuous decrease with depth into the

mesophotic zone (Bak 1977; Sheppard 1982; Huston 1985).

Caribbean mesophotic reefs are usually dominated by

members of the genera Agaricia (mainly A. grahamae and

A. lamarcki), followed by Montastraea (mainly M. cav-

ernosa) and Madracis (mainly M. formosa and M. pharen-

sis) (Bak 1977; Van den Hoek et al. 1978; Bak et al. 2005;

Jarrett et al. 2005; Culter et al. 2006; Venn et al. 2009), with

the exception of submerged banks, where members of the

Montastraea annularis species complex (which form thick

plates at these depths) are usually the dominant members of

the coral community (Garcıa-Sais et al. 2008; Rivero-Calle

et al. 2009; Smith et al. 2010). The decrease in species

richness over depth extends to the aphotic zone (\1% of

surface irradiance) where light-dependent corals gradually

disappear and are replaced by azooxanthellate corals, sty-

lasterids, sponges, and coralline-, turf- and macro-algae

(mainly Halimeda, Lobophora and Dictyota spp.) (Van den

Hoek et al. 1978).

Knowledge of the distribution of coral species down the

reef slope is useful to assess which species are the most

likely candidates in the deep to replenish shallow reef zones.

So-called ‘shallow-specialist’ species obviously do not

occur on the mesophotic reef, whereas ‘deep-specialist’

species do not appear to be successfully recruiting to shal-

low water (Bak and Engel 1979). In contrast, ‘depth-gen-

eralist’ species exhibit wide depth ranges, and reef

populations of these species are able to at least partially

escape depth-related stressors. The fact that these species

occur on both shallow and mesophotic reefs (although

sometimes with different substrate preferences over depth;

Vermeij and Bak 2003) suggests that they may form a single

metapopulation over the reef slope and as such would be

likely candidates to supply offspring up the reef slope. A

detailed compilation of data on the vertical distribution of

zooxanthellate coral species in the Caribbean and Bermuda

(Table 2) indicates that *25% of the species (total n = 53)

occurs over large depth ranges (i.e., are ‘depth-generalists’)

encompassing both the shallow reef and upper mesophotic

zone (30–60 m). Several of these species (e.g., Madracis

pharensis, Montastrea cavernosa, and Stephanocoenia in-

tersepta) can be considered ‘extreme depth-generalists’, as

their distribution extends into the lower mesophotic zone

([60 m); however, the majority of species does not occur

deeper than the upper mesophotic zone (30–60 m) (Reed

1985; Rezak et al. 1990; Phillips et al. 1990; Jarrett et al.

2005; Culter et al. 2006). Only a few species (13%, Table 2;

e.g., Agaricia grahamae, Scolymia cubensis, and Madracis

Coral Reefs (2010) 29:309–327 315

123

Ta

ble

2L

ist

of

zoo

xan

thel

late

cora

lsp

ecie

so

fth

eC

arib

bea

nan

dB

erm

ud

aw

ith

info

rmat

ion

on

thei

rb

ath

ym

etri

cd

istr

ibu

tio

n,

sym

bio

nt

zon

atio

n,

and

rep

rod

uct

ive

mo

de

Sp

ecie

sC

om

mo

n

insh

allo

w

Co

mm

on

ind

eep

Sy

mb

ion

tzo

nat

ion

Rep

rod

uct

ive

mo

de

(ty

pe)

Rec

entl

y

rep

ort

ed

[3

0m

Max

.

dep

th

(m)

Lo

cati

on

sR

efer

ence

sZ

on

atio

nan

dd

epth

ran

ge

inv

esti

gat

ed

Ref

eren

ces

Acr

op

ori

dae

Acr

op

ora

cerv

ivo

rnis

Yes

No

50

Jam

aica

Go

reau

and

Wel

ls(1

96

7)

Cla

dal

(1–

28

m)

Bak

eret

al.

(19

97)

Bro

adca

st

Acr

op

ora

pa

lma

taY

esN

oN

on

e(1

–3

m)

Bak

eret

al.

(19

97)

Bro

adca

st

Acr

op

ora

pro

life

raY

esN

oU

nk

no

wn

Ag

aric

idae

Bro

od

ing

Ag

ari

cia

ag

ari

cite

sY

esN

o7

5C

ub

a;C

ura

cao

;Ja

mai

ca;

US

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),

Ku

hlm

ann

(19

83

),H

ug

hes

and

Jack

son

(19

85)

Bro

od

ing

Ag

ari

cia

fra

gil

isY

esY

es8

0B

erm

ud

a;C

ub

a;F

lori

da

(US

);Ja

mai

ca;

US

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Ku

hlm

ann

(19

83

),

Fri

cke

and

Mei

sch

ner

(19

85

),Ja

rret

tet

al.

(20

05),

Cu

lter

etal

.(2

00

6)

Bro

od

ing

Ag

ari

cia

gra

ha

ma

eN

oY

es1

15

Bah

amas

;C

ub

a;C

ura

cao

;

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Go

reau

(19

73

),B

ak(1

97

7),

Van

den

Ho

eket

al.

(19

78

),K

uh

lman

n(1

98

3),

Ree

d(1

98

5),

Bak

etal

.(2

00

5)

Bro

od

ing

Ag

ari

cia

hu

mil

isY

esN

o7

0Ja

mai

caG

ore

auan

dW

ells

(19

67

)B

roo

din

g

Ag

ari

cia

lam

arc

kiN

oY

es7

5C

ub

a;C

ura

cao

;F

lori

da

(US

);

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

ldb

erg

(19

73),

Go

reau

and

Go

reau

(19

73

),

Bak

(19

77),

Van

den

Ho

eket

al.

(19

78

),

Bak

and

Lu

ckh

urs

t(1

98

0),

Ku

hlm

ann

(19

83),

Hu

gh

esan

dJa

ckso

n(1

98

5),

Bak

etal

.(2

00

5),

Jarr

ett

etal

.(2

00

5),

Cu

lter

etal

.(2

00

6)

Bro

od

ing

Ag

ari

cia

ten

uif

oli

aY

esN

oB

roo

din

g

Ag

ari

cia

un

da

taN

oN

o8

0C

ub

a;C

ura

cao

;Ja

mai

ca;

US

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),V

an

den

Ho

eket

al.

(19

78

),K

uh

lman

n(1

98

3)

Bro

od

ing

Lep

tose

ris

cucu

lla

ta(s

yn

on

ym

ou

sw

ith

Hel

iose

ris

cucu

lla

ta)

Yes

Yes

10

8B

aham

as;

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),

Ku

hlm

ann

(19

83

),R

eed

(19

85),

Hu

gh

es

and

Jack

son

(19

85),

Jarr

ett

etal

.(2

00

5),

Cu

lter

etal

.(2

00

6)

Bro

od

ing

Ast

roco

enid

ae

Ste

ph

an

oco

enia

inte

rsep

ta(f

orm

erly

clas

sifi

edas

S.

mic

hel

inii

)

Yes

Yes

95

Ber

mu

da;

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

,U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73),

Bak

(19

77),

Van

den

Ho

eket

al.

(19

78

),

Ku

hlm

ann

(19

83

),F

rick

ean

dM

eisc

hn

er

(19

85),

Bak

etal

.(2

00

5)

Cla

dal

(8–

25

m)

Ro

wan

(19

98

),

War

ner

etal

.

(20

06

)

Bro

adca

st

Car

yo

ph

yll

idae

316 Coral Reefs (2010) 29:309–327

123

Ta

ble

2co

nti

nu

ed

Sp

ecie

sC

om

mo

n

insh

allo

w

Co

mm

on

ind

eep

Sy

mb

ion

tzo

nat

ion

Rep

rod

uct

ive

mo

de

(ty

pe)

Rec

entl

y

rep

ort

ed

[3

0m

Max

.

dep

th

(m)

Lo

cati

on

sR

efer

ence

sZ

on

atio

nan

dd

epth

ran

ge

inv

esti

gat

ed

Ref

eren

ces

Eu

smil

iafa

stig

iata

Yes

No

65

Cu

ba,

Jam

aica

,U

SV

irg

in

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Ku

hlm

ann

(19

83)

Bro

od

ing

Fav

iid

ae

Co

lpo

ph

ylli

an

ata

ns

(pre

vio

usl

yal

so

clas

sifi

edas

C.

bre

vise

ria

lis)

Yes

Yes

55

Ber

mu

da;

Cu

ba;

Cu

raca

o;

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Wel

ls(1

96

7),

Ku

hlm

ann

(19

83

),

Hu

gh

esan

dJa

ckso

n(1

98

5),

Bak

etal

.

(20

05)

Bro

adca

st

Dip

lori

acl

ivo

saY

esN

oB

road

cast

Dip

lori

ala

byr

inth

ifo

rmis

Yes

No

43

Ber

mu

da;

Jam

aica

Go

reau

and

Wel

ls(1

96

7),

Fri

cke

and

Mei

sch

ner

(19

85

)

Cla

dal

(?)

Ro

wan

(19

98

)B

road

cast

Dip

lori

ast

rig

osa

Yes

Yes

47

Ber

mu

da;

Cu

raca

o;

Flo

wer

Gar

den

Ban

ks;

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Fri

cke

and

Mei

sch

ner

(19

85

),B

aket

al.

(20

05),

Arm

stro

ng

etal

.(2

00

6),

Viz

e(2

00

6)

Bro

adca

st

Fa

via

fra

gu

mY

esN

oB

roo

din

g

Ma

nic

ina

are

ola

taY

esN

o6

5F

lori

da

(US

);Ja

mai

caG

ore

auan

dW

ells

(19

67

),G

old

ber

g(1

97

3)

Bro

od

ing

Mo

nta

stra

eaa

nn

ula

ris

Yes

No

80

Ber

mu

da;

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73),

Bak

(19

77),

Ku

hlm

ann

(19

83

),F

rick

ean

d

Mei

sch

ner

(19

85

),H

ug

hes

and

Jack

son

(19

85)

Cla

dal

(0–

15

m)

Ro

wan

and

Kn

ow

lto

n(1

99

5),

To

ller

etal

.

(20

01

),W

arn

er

etal

.(2

00

6)

Bro

adca

st

Mo

nta

stra

eaca

vern

osa

Yes

Yes

11

3B

aham

as;

Bar

bad

os;

Ber

mu

da;

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Flo

wer

Gar

den

Ban

ks;

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73

),

Bak

(19

77

),V

and

enH

oek

etal

.(1

97

8),

Bak

and

Lu

ckh

urs

t(1

98

0),

Ku

hlm

ann

(19

83

),F

rick

ean

dM

eisc

hn

er(1

98

5),

Ree

d

(19

85

),H

ug

hes

and

Jack

son

(19

85

),

Mac

inty

reet

al.

(19

91

),L

idd

ell

etal

.

(19

97

),Ja

rret

tet

al.

(20

05

),A

rmst

ron

g

etal

.(2

00

6),

Cu

lter

etal

.(2

00

6),

Viz

e

(20

06

),L

esse

ret

al.

(20

09

b)

Su

b-c

lad

al(3

–9

1m

)W

arn

eret

al.

(20

06

),

Les

ser

etal

.

(20

09

b)

Bro

adca

st

Mo

nta

stra

eafa

veo

lata

Yes

No

Cla

dal

(0–

25

m)

Ro

wan

and

Kn

ow

lto

n(1

99

5),

To

ller

etal

.

(20

01),

War

ner

etal

.(2

00

6)

Bro

adca

st

Mo

nta

stra

eafr

an

ksi

Yes

Yes

39

Flo

wer

Gar

den

Ban

ks

To

ller

etal

.(2

00

1),

Viz

e(2

00

6)

Cla

dal

(4–

38

m)

To

ller

etal

.(2

00

1)

Bro

adca

st

Coral Reefs (2010) 29:309–327 317

123

Ta

ble

2co

nti

nu

ed

Sp

ecie

sC

om

mo

n

insh

allo

w

Co

mm

on

ind

eep

Sy

mb

ion

tzo

nat

ion

Rep

rod

uct

ive

mo

de

(ty

pe)

Rec

entl

y

rep

ort

ed

[3

0m

Max

.

dep

th

(m)

Lo

cati

on

sR

efer

ence

sZ

on

atio

nan

dd

epth

ran

ge

inv

esti

gat

ed

Ref

eren

ces

So

len

ast

rea

bo

urn

on

iY

esN

oB

road

cast

So

len

ast

rea

hya

des

Yes

No

Bro

adca

st

Mea

nd

rin

idae

Den

dro

gyr

acy

lin

dri

cus

Yes

No

Bro

adca

st

Dic

ho

coen

iast

oke

si(p

rev

iou

sly

also

clas

sifi

edas

D.

stel

lari

s)

Yes

Yes

65

Ber

mu

da;

Cu

raca

o;

Flo

rid

a

(US

);Ja

mai

ca

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73),

Go

reau

and

Go

reau

(19

73

),V

and

enH

oek

etal

.(1

97

8),

Fri

cke

and

Mei

sch

ner

(19

85

),

Ven

net

al.

(20

09

)

Cla

dal

(?–

60

m)

Ven

net

al.

(20

09

)B

road

cast

Mea

nd

rin

am

ean

dri

tes

Yes

Yes

80

Ber

mu

da;

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73),

Bak

(19

77),

Ku

hlm

ann

(19

83

),F

rick

ean

d

Mei

sch

ner

(19

85

),V

enn

etal

.(2

00

9)

Cla

dal

(?–

60

m)

Ven

net

al.

(20

09

)B

roo

din

g

Mu

ssid

ae

Iso

ph

ylla

stre

ari

gid

aY

esN

oB

roo

din

g

Iso

ph

ylli

asi

nu

osa

Yes

No

32

Ber

mu

da

Fri

cke

and

Mei

sch

ner

(19

85

)B

roo

din

g

Mu

ssa

an

gu

losa

Yes

No

59

Jam

aica

Go

reau

and

Wel

ls(1

96

7)

Bro

od

ing

Myc

eto

ph

ylli

afe

rox

Yes

No

Bro

od

ing

Myc

eto

ph

ylli

aa

lici

ae

Yes

No

65

Cu

ba;

Cu

raca

o;

Jam

aica

;U

S

Vir

gin

Isla

nd

s

Go

reau

and

Go

reau

(19

73

),B

ak(1

97

7),

Van

den

Ho

eket

al.

(19

78

),K

uh

lman

n(1

98

3)

Bro

od

ing

Myc

eto

ph

ylli

ala

ma

rcki

an

a(p

rev

iou

sly

also

clas

sifi

edas

M.

da

na

an

a)

Yes

No

75

Cu

ba;

Flo

rid

a(U

S);

Jam

aica

;

US

Vir

gin

Isla

nd

s

Go

reau

and

Wel

ls(1

96

7),

Go

ldb

erg

(19

73),

Ku

hlm

ann

(19

83

)

Bro

od

ing

Myc

eto

ph

ylli

are

esi

No

No

65

Cu

raca

o;

Jam

aica

Go

reau

and

Go

reau

(19

73),

Bak

(19

77

)B

roo

din

g

Sco

lym

iacu

ben

sis

No

Yes

92

Bah

amas

;B

erm

ud

a;C

ub

a;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Go

reau

(19

73

),B

ak(1

97

7),

Van

den

Ho

eket

al.

(19

78

),K

uh

lman

n(1

98

3),

Fri

cke

and

Mei

sch

ner

(19

85

),R

eed

(19

85

),

Jarr

ett

etal

.(2

00

5),

Cu

lter

etal

.(2

00

6)

Bro

od

ing

Ocu

lin

idae

Ocu

lin

ad

iffu

saY

esN

oU

nk

no

wn

Ocu

lin

aro

bu

sta

Yes

No

Un

kn

ow

n

318 Coral Reefs (2010) 29:309–327

123

Ta

ble

2co

nti

nu

ed

Sp

ecie

sC

om

mo

n

insh

allo

w

Co

mm

on

ind

eep

Sy

mb

ion

tzo

nat

ion

Rep

rod

uct

ive

mo

de

(ty

pe)

Rec

entl

y

rep

ort

ed

[3

0m

Max

.

dep

th

(m)

Lo

cati

on

sR

efer

ence

sZ

on

atio

nan

dd

epth

ran

ge

inv

esti

gat

ed

Ref

eren

ces

Ocu

lin

ate

nel

la(r

epo

rted

colo

nie

s

are

po

ten

tial

ly

azo

ox

anth

ella

te)

No

Yes

75

Flo

rid

a(U

S)

Jarr

ett

etal

.(2

00

5),

Cu

lter

etal

.(2

00

6)

Un

kn

ow

n

Po

cill

op

ori

dae

Ma

dra

cis

carm

ab

iN

oY

es4

0C

ura

cao

Ver

mei

jan

dB

ak(2

00

3),

Fra

de

etal

.(2

00

8)

Bro

od

ing

Ma

dra

cis

dec

act

isY

esY

es9

8C

ura

cao

;F

lori

da

(US

)G

ore

auan

dW

ells

(19

67

),B

ak(1

97

7),

Fri

cke

and

Mei

sch

ner

(19

85

),R

eed

(19

85

),

Ver

mei

jan

dB

ak(2

00

3),

Jarr

ett

etal

.

(20

05),

Cu

lter

etal

.(2

00

6),

Fra

de

etal

.

(20

08)

No

ne

(5–

25

m)

and

clad

al(?

–6

0m

)

Fra

de

etal

.(2

00

8),

Ven

net

al.

(20

09)

Bro

od

ing

Ma

dra

cis

form

osa

No

Yes

75

Cu

ba;

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Go

reau

(19

73

),B

ak(1

97

7),

Van

den

Ho

eket

al.

(19

78

),K

uh

lman

n(1

98

3),

Ver

mei

jan

dB

ak(2

00

3),

Jarr

ett

etal

.

(20

05),

Cu

lter

etal

.(2

00

6),

Fra

de

etal

.

(20

08)

Bro

od

ing

Ma

dra

cis

mir

ab

ilis

Yes

No

No

ne

(5–

25

m)

Fra

de

etal

.(2

00

8)

Bro

od

ing

Ma

dra

cis

ph

are

nsi

sY

esY

es1

33

Cu

raca

o;

Flo

rid

a(U

S);

Jam

aica

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),

Ver

mei

jan

dB

ak(2

00

2),

Ver

mei

jan

dB

ak

(20

03),

Jarr

ett

etal

.(2

00

5),

Cu

lter

etal

.

(20

06),

Fra

de

etal

.(2

00

8)

Su

b-c

lad

al(5

–4

0m

)F

rad

eet

al.

(20

08

)B

roo

din

g

Ma

dra

cis

sen

ari

aN

oY

es6

0C

ura

cao

Bak

(19

77

),V

erm

eij

and

Bak

(20

03

),F

rad

e

etal

.(2

00

8)

No

ne

(5–

40

m)

Fra

de

etal

.(2

00

8)

Bro

od

ing

Po

riti

dae

Po

rite

sa

stre

oid

esY

esY

es7

0B

erm

ud

a;C

ub

a;C

ura

cao

;

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),

Ku

hlm

ann

(19

83

),F

rick

ean

dM

eisc

hn

er

(19

85),

Hu

gh

esan

dJa

ckso

n(1

98

5),

Arm

stro

ng

etal

.(2

00

6)

Cla

dal

(2–

25

m)

Ro

wan

(19

98

),

War

ner

etal

.

(20

06

)

Bro

od

ing

Po

rite

sb

ran

ner

iY

esN

oB

roo

din

g

Po

rite

sco

lon

ensi

sY

esN

oB

roo

din

g

Po

rite

sp

ori

tes

f.

div

ari

cata

Yes

Yes

75

Flo

rid

a(U

S);

Jam

aica

Go

reau

and

Wel

ls(1

96

7),

Jarr

ett

etal

.

(20

05

),C

ult

eret

al.

(20

06

)

Bro

od

ing

Po

rite

sp

ori

tes

f.

furc

ata

Yes

No

50

Jam

aica

Go

reau

and

Wel

ls(1

96

7)

Bro

od

ing

Po

rite

sp

ori

tes

f.

po

rite

sN

oN

o3

4B

erm

ud

aF

rick

ean

dM

eisc

hn

er(1

98

5)

Bro

od

ing

Coral Reefs (2010) 29:309–327 319

123

formosa) are observed exclusively on mesophotic reefs

(i.e., ‘deep-specialists’), and a relatively large number of

species are limited to the shallow reef (55%, Table 2;

\30 m; i.e., ‘shallow-specialists’). These numbers corre-

spond roughly (although the numbers of ‘depth-generalist’

species are somewhat higher) with depth-distribution pat-

terns described for species by Goreau and Wells (1967) in

Jamaica (‘depth-generalist’ spp. 36%; ‘shallow-specialist’

spp. 53%; and ‘deep-specialist’ spp. 11%) and by Bak

(1977) at two reef localities in Curacao (‘depth-generalist’

spp. 41%; ‘shallow-specialist’ spp. 44%; and ‘deep-spe-

cialist’ spp. 18%). Interestingly, these percentages are also

similar to those observed for highly diverse coral commu-

nities (total n = 152) in the Indian Ocean (Chagos Archi-

pelago), with *25% of the species occurring over large

depth ranges, and 57 and 18% of the species representing

‘shallow- and deep-specialists’, respectively (Sheppard

1981). Even though proportions will vary geographically

between regions and locations (as will the presence/absence

on shallow and deep reefs of the species in Table 2),

roughly a quarter of the scleractinian coral species in the

Caribbean exhibit distributions that encompass both the

shallow reef and upper mesophotic zone, and therefore

based purely on community composition and species dis-

tribution ranges, represent candidate species that have the

potential to provide propagules for recruitment in shallower

zones.

Reproduction and recruitment as a function of depth

Although ‘depth-generalist’ coral species on the mesoph-

otic reef are likely candidates to provide propagules for the

shallow reef, there is currently no direct evidence that

larval exchange between shallow and deep populations

actually occurs (i.e., that these species form panmictic

populations over the reef slope). Both coral life histories

and symbiont associations have the potential to strongly

influence recruitment patterns over depth, and it is,

therefore, pertinent to explore these to evaluate whether

species from the deep reef can act as a reproductive source

for the shallow.

The variation in bathymetric distribution ranges of

different coral species seems to be determined by pre-

settlement rather than post-settlement processes (Mundy

and Babcock 2000), as depth distributions of juveniles

mirror those of adult colonies (Bak and Engel 1979), and

larvae preferentially select parental habitat substratum

(Baird et al. 2003) by differentiating between light inten-

sity and spectral composition (Mundy and Babcock 1998).

Therefore, even though recruitment processes on bare

substrata can differ from those occurring in mature com-

munities (Grigg and Maragos 1974; Tomasik et al. 1996;

Vermeij 2006), it appears unlikely that ‘deep-specialist’Ta

ble

2co

nti

nu

ed

Sp

ecie

sC

om

mo

n

insh

allo

w

Co

mm

on

ind

eep

Sy

mb

ion

tzo

nat

ion

Rep

rod

uct

ive

mo

de

(ty

pe)

Rec

entl

y

rep

ort

ed

[3

0m

Max

.

dep

th

(m)

Lo

cati

on

sR

efer

ence

sZ

on

atio

nan

dd

epth

ran

ge

inv

esti

gat

ed

Ref

eren

ces

Sid

eras

trei

dae

Sid

era

stre

ara

dia

ns

Yes

No

33

Jam

aica

Go

reau

and

Wel

ls(1

96

7)

Bro

od

ing

Sid

era

stre

asi

der

eaY

esY

es7

0C

ub

a;C

ura

cao

;F

lori

da

(US

);

Jam

aica

;U

SV

irg

inIs

lan

ds

Go

reau

and

Wel

ls(1

96

7),

Bak

(19

77

),

Go

ldb

erg

(19

73

),K

uh

lman

n(1

98

3),

Hu

gh

esan

dJa

ckso

n(1

98

5),

Arm

stro

ng

etal

.(2

00

6)

No

ne

(8–

25

m)

War

ner

etal

.(2

00

6)

Bro

adca

st

‘Co

mm

on

insh

allo

w’

refe

rsto

bei

ng

rep

ort

edb

yH

um

ann

and

DeL

oac

h(2

00

2)

toco

mm

on

lyo

ccu

rat

shal

low

erd

epth

s.‘R

ecen

tly

rep

ort

ed[

30

m’

refe

rsto

bei

ng

rep

ort

ed[

30

min

the

pas

t

10

yea

rs(t

og

ive

ap

rese

nt-

day

esti

mat

eo

fd

epth

-dis

trib

uti

on

and

toav

oid

tax

on

om

ical

amb

igu

itie

s).

‘Zo

nat

ion

’re

fers

tow

het

her

the

asso

ciat

edS

ymb

iod

iniu

mar

ep

arti

tio

ned

ov

erd

epth

inth

at

spec

ies,

wit

h‘C

lad

al’

refe

rrin

gto

ash

ift

insy

mb

ion

tcl

ade

(e.g

.,fr

om

Bto

C),

wh

ile

‘Su

b-c

lad

al’

refe

rsto

ash

ift

insy

mb

ion

tsu

bcl

ade

(e.g

.,fr

om

B7

toB

15

).R

epro

du

ctiv

em

od

esar

ead

op

ted

fro

mT

rnk

aan

dM

ou

ldin

g(2

00

6)

320 Coral Reefs (2010) 29:309–327

123

species will colonize bare substratum on the shallow reef.

‘Depth-generalist’ species are, therefore, the most likely

candidates to facilitate recruitment to the shallow reef.

However, pre-settlement (in addition to post-settlement)

processes could potentially vary between shallow and deep

populations of ‘depth-generalist’ species, resulting in (or

reinforcing) intra-specific genetic structuring and limiting

larval connectivity up the reef slope.

Genetic structuring could originate through local adap-

tation of coral populations (reviewed in Baums 2008) to the

unique environmental conditions in shallow versus deep

habitats. However, genetic assessments that specifically

address genetic structuring of coral host populations over

depth are lacking to date. Broadcasting species are less

likely to form genetically distinct populations in the shal-

low and deep, because mass spawning in certain species of

deep corals is observed to be synchronized with their

shallow-water counterparts (e.g., M. cavernosa, M. franksi,

and Diploria strigosa; Vize 2006), and mixing of sperm

and eggs from the entire depth range is expected to occur at

the surface (Willis et al. 2006). Most coral species in the

Caribbean (and all species exclusive to the mesophotic

zone) exhibit a brooding reproductive mode, and these

species are more likely to exhibit small-scale genetic

structuring (e.g., Ayre and Hughes 2000).

As scleractinian corals live in a mutualistic symbiosis

with Symbiodinium, the combination of the physiological

tolerances of each partner determines the ability of the

holobiont (host plus endosymbiont) to occupy, compete,

and thrive within its environment (Iglesias-Prieto and

Trench 1997). In terms of the endosymbionts, the presence

of distinct varieties has been shown to influence the sur-

vival and competitive ability of juvenile corals (Rodriguez-

Lanetty et al. 2004; Little et al. 2004; Gomez-Cabrera et al.

2007). Comparing endosymbiont community composition

of parental populations and offspring reveals that, similar

to selection of parental habitat, juveniles adopt Symbiodi-

nium types similar to that of the parent (Coffroth et al.

2001; Weis et al. 2001; Rodriguez-Lanetty et al. 2004).

‘Depth-generalist’ coral species can either harbor a single

symbiont over their entire range or show a cladal or sub-

cladal shift of symbionts with depth (e.g., Rowan and

Knowlton 1995; Warner et al. 2006; Sampayo et al. 2007;

Frade et al. 2008). However, nine out of ten ‘depth-gen-

eralist’ Caribbean species studied to date exhibit a zonation

of Symbiodinium over depth with the exception of Sider-

astrea siderea (Table 2). In addition, processes of symbi-

ont transfer and specialization of the symbionts to

particular environments may impose limitations to the

colonization and survival of coral offspring within certain

habitats. For example, coral species with vertical trans-

mission (maternal acquisition of symbionts) may be limited

in their ability to settle outside the direct parental range if

depth-specific symbionts are transferred to the offspring

(e.g., Meandrina meandrites and Porites astreoides;

Table 2). Such limitations are not expected for corals with

horizontal transmission strategies (i.e., that acquire their

Symbiodinium from the water column), or those that harbor

a single Symbiodinium type throughout their entire distri-

bution range. The prevalence of Symbiodinium zonation

and a vertical symbiont acquisition mode in ‘depth-gener-

alist’ species further increases the likelihood of genetic

differentiation (and reduced gene flow) between shallow

and deep coral populations.

Evaluation of the ‘deep reef refugia’ hypothesis

This paper set out to explore the potential role of mesophotic

coral communities to act as ‘deep reef refugia’ (Glynn 1996;

Riegl and Piller 2003; Armstrong et al. 2006). Given the

rapid changes coral reefs currently face, the potential of

deep reef sections to function as refugia has generated

growing scientific and management interest in these com-

munities (e.g., this issue and http://www.mesophotic.org).

In this study, the current knowledge of deep reefs in the

Caribbean was used to assess whether mesophotic reef areas

(1) are protected or dampened from disturbances that affect

shallow reef areas and (2) can provide a viable reproductive

source for shallow reef areas following disturbance.

Some of the disturbances on coral reefs have the potential

to act indiscriminately over the entire depth range (e.g.,

sedimentation, nutrient enrichment, and influx of toxins).

However, the case history of the Caribbean provides clear

examples of major disturbances that only affected the

shallow sections of the reef (Table 1) such as the outbreak of

white-band disease, the mass mortality of Diadema, and

several hurricanes, and thermal bleaching events, leaving

deeper reef sections relatively unaffected. This said,

mesophotic communities face their own set of occasional

stressors, including catastrophic sedimentation, deep-water

macroalgal blooms, and cold-water bleaching (Table 1) and

consequently are not immune to disturbances. Additionally,

the slow growth (Hughes and Jackson 1985), fragile skele-

tons, and plate-like morphology of mesophotic corals make

these communities more susceptible to damage through

breakage and smothering. Nonetheless, mesophotic com-

munities have on several occasions provided an escape to

the effects of storm-induced waves and anomalies in sea

surface temperature (Table 1); two acute threats that are

predicted to become more severe in the coming decades.

Even though the ability to escape the impact of storm-

induced waves has limitations (depending on bathymetry

and levels of sedimentation), and the ability of deep reefs to

provide a thermal escape is poorly understood (i.e., the roles

of light/temperature, local acclimation/adaptation, and

Coral Reefs (2010) 29:309–327 321

123

http://www.mesophotic.org

species-specific differences), it does provide some support

for the validity of the DRRH.

The evidence to support the idea that mesophotic reef

areas will act as a viable reproductive source for shallow

reef areas is, however, limited. Much of our knowledge of

recruitment and dispersal in corals is limited to data on

established or mature communities and does not include

metrics on the possibilities when new habitat becomes

available (e.g., Grigg and Maragos 1974; Tomasik et al.

1996; Vermeij 2006). Based on patterns of the distribution

across depth alone, the upper mesophotic zone (30–60 m)

yields the greatest potential for larval linkages between

deep and shallow communities, because it contains a large

number of ‘depth-generalist’ species. It must be noted that

some ‘depth-generalist’ species occur in cryptic locations

on the shallow reef (e.g., Madracis pharensis; Vermeij and

Bak 2002), which limits their ability to colonize bare

substrate on the shallow reef. Despite the overlap in coral

community structure between the shallow reef and upper

mesophotic zone, our understanding of the genetic struc-

ture and recruitment biology of such coral species is

insufficient to be able to distinguish panmixis versus

genetic structuring over depth. The predominance of corals

with a brooding reproductive mode and zonation of sym-

bionts over depth suggests that the capacity for genetic

exchange between the shallow and deep reef may be lim-

ited to a subset of coral species on Caribbean reef slopes.

Recommendations

The considerable information available for shallow-water

coral populations contrasts the relatively small amount

present for coral communities occurring over 30 m (Bak

et al. 2005; Menza et al. 2008). Given their potential

importance with respect to global issues such as climate

change, greater efforts should be exerted to understand the

ecology and structural heterogeneity of mesophotic coral

communities, and the potential linkages that exist with

shallow-water counterparts. In formulating this review, a

number of critical research areas become apparent not only

for the Caribbean but for reef ecosystems globally.

The first area concerns the distribution and abundance of

mesophotic coral ecosystems (in relation to shallow coral

reefs), and the role of marine protected areas (MPAs) in

providing protection for these important and often biolog-

ically diverse ecosystems. So far, only a small number of

mesophotic communities have been described (Kahng et al.

2010). Thus, targeted mapping explorations should be

undertaken at locations where the requirements for deep

reef formation are likely to be met (i.e., oligotrophic con-

ditions and clear waters, availability of hard substrate, and

absence of a strong shallow thermocline). Given the

logistical complexity of research in the mesophotic realm,

such studies would greatly benefit from international col-

laborations whereby the cost-intensive facilities can be

shared among different research groups and funding

agencies. The second area involves improving our under-

standing the relationship between physical, chemical, and

biological stress factors and depth. This is especially

important in terms of understanding the resilience of reefs

to future disturbances arising from climatic change. In

particular, the notion that temperature-induced bleaching is

generally restricted to shallow depths urgently needs to be

evaluated by pre- and post-bleaching surveys over broader

depth ranges (i.e., encompassing the mesophotic zone),

coupled with long-term temperature monitoring over depth.

It is crucial to determine the causal mechanisms behind the

bathymetric patterns of coral bleaching, such as the role of

cold-water influxes in providing thermal relief and the

occurrence of local adaptation/acclimation in coral com-

munities to the distinct thermal patterns occurring on the

shallow and deep reef.

Finally, perhaps the most urgent research question

concerns whether mesophotic coral communities are able

to contribute recruits to shallow-water habitats. High-res-

olution genetic studies should be able to assess the con-

nectivity between shallow and deep coral populations in a

variety of species covering both brooding and broadcasting

strategies (and both vertical and horizontal symbiont

acquisition modes). Ideally, these studies should assess

both the coral host and their associated Symbiodinium and

should be conducted in conjunction with regional geo-

graphic population genetic assessments to allow compari-

son between intra- and inter-reef genetic structuring. Even

though genetic studies will only provide an indirect mea-

sure of reef connectivity, the information will indicate

whether ‘depth-generalist’ species are indeed suitable

candidates to aid in the rapid recovery of shallow reefs.

Additionally, reciprocal depth-transplantations of offspring

from shallow and deep coral colonies will inform us about

the respective roles of genetic adaptation versus phenotypic

plasticity in the opportunistic success of ‘depth-generalist’

coral species and the ability of offspring to survive outside

their parental depth range.

Conclusion

Reef communities represent a dynamic equilibrium

between processes that reestablish coral reefs (‘recovery’)

and those that lead to the deterioration of reef communities

(‘disturbance’). If anything, the upper mesophotic (30–

60 m) zone holds the greatest potential to aid in reef

recovery following disturbance due to the species overlap

with the shallow reef and the ability to (partially) escape

322 Coral Reefs (2010) 29:309–327

123

certain disturbances. Although there is clearly much to

learn about mesophotic coral ecosystems and restrictions

seem to apply, their potential to act as refugia and sub-

sequent reproductive sources for shallow reef areas remains

a hopeful aspect of the biology of coral reefs as they enter a

century of unprecedented human disturbance.

Acknowledgments The authors would like to thank Mark Vermeij,

Tyler Smith, Thomas Bridge, Kyra Hay, Cynthia Riginos, Petra

Visser, and five anonymous reviewers for valuable comments that

significantly improved the manuscript. The authors of this study were

supported by the Coral Reef Targeted Research Project (www.

gefcoral.org) and the Australian Research Council Centre of Excel-

lence in Coral Reef Studies. This is a contribution from the Coral

Reef Ecosystems Laboratory at The University of Queensland (www.

coralreefecosystems.org).

References

Alamaru A, Loya Y, Brokovich E, Yam R, Shemesh A (2009) Carbon

and nitrogen utilization in two species of Red Sea corals along a

depth gradient: Insights from stable isotope analysis of total

organic material and lipids. Geochim Cosmochim Acta 73:5333–

5342

Albins MA, Hixon MA (2008) Invasive Indo-Pacific lionfish Pteroisvolitans reduce recruitment of Atlantic coral-reef fishes. Mar

Ecol Prog Ser 367:233–238

Armstrong RA (2007) Deep zooxanthellate coral reefs of the Puerto

Rico: US Virgin Islands insular platform. Coral Reefs 26:945

Armstrong RA, Singh H, Torres J, Nemeth RS, Can A, Roman C,

Eustice R, Riggs L, Garcia-Moliner G (2006) Characterizing the

deep insular shelf coral reef habitat of the Hind Bank Marine

Conservation District (US Virgin Islands) using the Seabed

autonomous underwater vehicle. Cont Shelf Res 26:194–205

Aronson RB, Precht WF (2001) White-band disease and the changing

face of Caribbean coral reefs. Hydrobiologia 460:25–38

Aronson RB, Sebens KP, Ebersole JP (1994) Hurricane Hugo’s

impact on Salt River submarine canyon, St. Croix, US Virgin

Islands. In: Ginsburg RN (ed) Proceedings of the colloquium on

global aspects of coral reefs: Health, hazards and history.

Rosenstiel School of Marine and Atmospheric Science, Miami,

pp 189–195

Ayre DJ, Hughes TP (2000) Genotypic diversity and gene flow in

brooding and spawning corals along the Great Barrier Reef,

Australia. Evolution 54:1590–1605

Baird AH, Babcock RC, Mundy CP (2003) Habitat selection by larvae

influences the depth distribution of six common coral species.

Mar Ecol Prog Ser 252:289–293

Bak RPM (1977) Coral reefs and their zonation in Netherlands

Antilles. Studies in Geology 4:3–16

Bak RPM, Luckhurst BE (1980) Constancy and change in coral reef

habitats along depth gradients at Curacao. Oecologia 47:145–

155

Bak RPM, Engel MS (1979) Distribution, abundance and survival of

juvenile hermatypic corals (Scleractinia) and the importance of

life history strategies in the parent coral community. Mar Biol

54:341–352

Bak RPM, Nieuwland G (1995) Long-term change in coral commu-

nities along depth gradients over leeward reefs in the Nether-

lands Antilles. Bull Mar Sci 56:609–619

Bak RPM, Nieuwland G, Meesters EH (2005) Coral reef crisis in deep

and shallow reefs: 30 years of constancy and change in reefs of

Curacao and Bonaire. Coral Reefs 24:475–479

Bak RPM, Nieuwland G, Meesters EH (2009) Coral growth rates

revisited after 31 years : what is causing lower extension rates in

Acropora palmata? Bull Mar Sci 84:287–294

Baker AC, Rowan R, Knowlton N (1997) Symbiosis ecology of two

Caribbean acroporid corals. Proc 8th Int Coral Reef Symp

2:1295–1300

Banner AH (1961) Submarine effects of the typhoon. Atoll Res Bull

75:75–78

Baums IB, Miller MW, Hellberg ME (2005) Regionally isolated

populations of an imperiled Caribbean coral, Acropora palmata.

Mol Ecol 14:1377–1390

Baums IB (2008) A restoration genetics guide for coral reef

conservation. Mol Ecol 17:2796–2811

Birkeland C (ed) (1997) Life and death of coral reefs. Chapman, New

York, pp 140–147

Brakel WH (1979) Small-scale spatial variation in light available to

coral reef benthos: quantum irradiance measurements from a

Jamaican reef. Bull Mar Sci 29:406–413

Brokovich E, Ayalon I, Einbinder S, Segev N, Shaked Y, Genin A,

Kark S, Kiflawi M (2010) Grazing pressure on coral reefs

decreases across a wide depth gradient in the Gulf of Aqaba, Red

Sea. Mar Ecol Prog Ser (in press)

Brown BE (1997) Coral bleaching: causes and consequences. Coral

Reefs 16:129–138

Bruno JF, Selig ER (2007) Regional decline of coral cover in the

Indo-Pacific: timing, extent, and subregional comparisons. PLoS

One 8:e711

Bunkley-Williams LC, Morelock J, Williams EH (1991) Lingering

effects of the 1987 mass bleaching of Puerto Rican coral reefs in

mid to late 1988. J Aquat Anim Health 3:242–247

Calnan JM, Smith TB, Nemeth RS, Kadison E, Blondeau J (2008)

Coral disease prevalence and host susceptibility on mid-depth

and deep reefs in the United States Virgin Islands. Rev Biol Trop

56:223–234

Coffroth MA, Santos SR, Goulet TL (2001) Early ontogenic

expression of specificity in a cnidarian-algal symbiosis. Mar

Ecol Prog Ser 222:85–96

Coles SL, Eldredge LG (2002) Non-indigenous species introductions

on coral reefs: A need for information. Pac Sci 56:191–209

Coles SL, Brown BE (2003) Coral bleaching—capacity for acclim-

itization and adaptation. Adv Mar Biol 46:183–223

Colgan MW (1987) Coral reef recovery on Guam (Micronesia) after

catastrophic predation by Acanthaster planci. Ecology 68:1592–

1605

Cooper TF, De’ath G, Fabricius KE, Lough JM (2008) Declining

coral calcification in massive Porites in two nearshore regions of

the northern Great Barrier Reef. Global Change Biol 14:529–538

Connell JH (1997) Disturbance and recovery of coral assemblages.

Coral Reefs 16(Suppl):S101–S113

Culter JK, Ritchie KB, Earle SA, Guggenheim DE, Halley RB,

Ciembronowicz KT, Hine AC, Jarrett BD, Locker SD, Jaap WC

(2006) Pulley reef: a deep photosynthetic coral reef on the West

Florida Shelf, USA. Coral Reefs 25:228

De’ath G, Lough JM, Fabricius KE (2009) Declining coral calcifi-

cation on the Great Barrier Reef. Science 323:116–119

DeVantier LM, Deacon G (1990) Distribution of Acanthaster planciat Lord Howe Island, the southern-most Indo-Pacific reef. Coral

Reefs 9:145–148

Dollar SJ (1982) Wave stress and coral community structure in

Hawaii. Coral Reefs 1:71–81

Feingold J (2001) Responses of three coral communities to the 1997–

98 El Nino-Southern Oscillation: Galapagos Islands, Ecuador.

Bull Mar Sci 69:61–77

Fenner D, Banks K (2004) Orange cup coral Tubastrea coccineainvades Florida and the flower Garden Banks, Northwestern Gulf

of Mexico. Coral Reefs 23:505–507

Coral Reefs (2010) 29:309–327 323

123

http://www.gefcoral.org

http://www.gefcoral.org

http://www.coralreefecosystems.org

http://www.coralreefecosystems.org

Fisk D, Done T (1985) Taxonomic and bathymetric patterns of

bleaching in corals, Myrmidon Reef (Queensland). Proc 5th Int

Coral Reef Symp 6:149–154

Frade PR, Jongh de F, Vermeulen F, van Bleijswijk J, Bak RPM (2008)

Variation in symbiont distribution between closely related coral

species over large depth ranges. Mol Ecol 17:691–703

Fricke HW, Schuhmacher H (1983) The depth limits of Red Sea stony

corals: An ecophysiological problem (a deep diving survey by

submersible). Mar Ecol 4:163–194

Fricke H, Meischner D (1985) Depth limits of Bermudan scleractinian

corals: a submersible survey. Mar Biol 88:175–187

Garcıa-Sais JR, Appeldoorn R, Battista T, Bauer L, Bruckner A,

Caldow C, Carrubba L, Corredor J, Diaz E, Lilyestrom C,

Garcıa-Moliner G, Hernandez-Delgado E, Menza C, Morell J,

Pait A, Sabater J, Weil E, Williams E, Williams S (2008) The

state of coral reef ecosystems of the Commonwealth of Puerto

Rico. In: Waddell J, Clarke A (eds) The state of coral reef

ecosystems of the United States and Pacific Freely Associated

States: 2008 NOAA Technical Memorandum NOS NCCOS 78.

NOAA/NCCOS Center for Coastal Monitoring and Assess-

ment’s Biogeography Team, Silver Spring, MD, pp 75–116

Gardner TA, Cote IM, Gill JA, Grant A, Watkinson AR (2003) Long-

term region-wide declines in Caribbean corals. Science 301:

958–960

Glynn PW (1996) Coral reef bleaching: facts, hypotheses and

implications. Global Change Biol 2:495–509

Glynn PW, Almodovar LR, Gonzalez JG (1964) Effects of hurricane

Edith on marine life in La Parguera, Puerto Rico. Caribb J Sci

4:335–345

Glynn PW, Mate JL, Baker AC, Calderon MO (2001) Coral bleaching

and mortality in Panama and Ecuador during the 1997–1998 El

Nino–Southern Oscillation even. Spatial/temporal patterns and

comparison with the 1982–1983 event. Bull Mar Sci 69:79–109

Goldberg WM (1973) The ecology of the coral octocoral communi-

ties off the southeast Florida coast: geomorphology, species

composition and zonation. Bull Mar Sci 23:465–488

Gomez-Cabrera MC, Ortiz J, Loh W, Ward S, Hoegh-Guldberg O

(2007) Acquisition of symbiotic dinoflagellates (Symbiodinium)

by juveniles of the coral Acropora longicyathus. Coral Reefs

27:219–226

Goreau TF, Goreau NI (1973) The ecology of Jamaican coral reefs. II.

Geomorphology, zonation, and sedimentary phases. Bull Mar Sci

23:399–464

Goreau TF, Wells JW (1967) The shallow-water Scleractinia of

Jamaica: revised list of species and their vertical distribution

ranges. Bull Mar Sci 17:442–453

Green SJ, Cote IM (2009) Record densities of Indo-Pacific lionfish on

Bahamian coral reefs. Coral Reefs 28:107

Grigg RW (2006) Depth limit for reef building corals in the Au’au

Channel. S.E. Hawaii. Coral Reefs 25:77–84

Grigg RW, Epp D (1989) Critical depth for the survival of coral

islands: effects on the Hawaiian archipelago. Science 243:638–

641

Grigg RW, Maragos JE (1974) Recolonization of hermatypic corals

on submerged lava flows in Hawaii. Ecology 55:387–395

Halfar J, Godinez-Orta L, Riegl B, Valdez-Holguin JE, Borges JM

(2005) Living on the edge: high-latitude Porites carbonate

production under temperate eutrophic conditions. Coral Reefs

24:582–592

Hallock P, Schlager W (1986) Nutrient excess and the demise of coral

reefs and carbonate platforms. Palaios 1:389–398

Harmelin-Vivien ML, Laboute P (1986) Catastrophic impact of

hurricanes on atoll outer reef slopes in the Tuamotu (French

Polynesia). Coral Reefs 5:55–62

Harvell CD, Kim K, Burkholder JM, Colwell RR, Epstien PR, Grimes

DJ, Hofmann EE, Lipp EK, Osterhaus ADME, Overstreet RM,

Porter JW, Smith GW, Vasta GR (1999) Emerging marine

diseases - Climate links and anthropogenic factors. Science

285:1505–1510

Hay ME, Colburn T, Downing D (1983) Spatial and temporal patterns

in herbivory on a Caribbean fringing reef: the effects on plant

distribution. Oecologia 58:299–308

Hickerson EL, Schmahl GP, Robbart M, Precht WF, Caldow C (2008)

State of coral reef ecosystems of the Flower Garden Banks,

Stetson Bank, and Other Banks in the Northwestern Gulf of

Mexico. In: Waddell JE, Clarke AM (eds), The state of coral reef

ecosystems of the United States and Pacific Freely Associated

States: 2008. NOAA Technical Memorandum NOS NCCOS 73.

NOAA/NCCOS Center for Coastal Monitoring and Assess-

ment’s Biogeography Team. Silver Spring, MD

Highsmith R, Riggs A, D’Antonio C (1980) Survival of hurricane-

generated coral fragments and a disturbance model of reef

calcification/growth rates. Oecologia 46:322–329

Hinderstein LM, Marr JCA, Martinez FA, Dowgiallo MJ, Puglise KA,

Zawada D, Pyle R (2010) Introduction to mesophotic coral

ecosystems: Characterization, ecology, and management. Coral

Reefs (this issue)

Hoegh-Guldberg O (1999) Climate change, coral bleaching and the

future of the world’s coral reefs. Mar Freshw Res 50:839–866

Hoegh-Guldberg O, Mumby PJ, Hooten AJ, Steneck RS, Greenfield

P, Gomez E, Harvell CD, Sale PF, Edwards AJ, Caldeira K,

Knowlton N, Eakin CM, Iglesias-Prieto R, Muthiga N, Bradbury

RH, Dubi A, Hatziolos ME (2007) Coral reefs under rapid

climate change and ocean acidification. Science 318:1737–1742

Hoegh-Guldberg O, Hughes L, McIntyre S, Lindenmayer DB,

Parmesan C, Possingham HP, Thomas CD (2008) Assisted

colonization and rapid climate change. Science 321:345–346

Hubbard DK (1989) The shelf-edge reefs of Davis and Cane Bays,

northwestern St. Croix, U.S.V.I. In: Hubbard DK (ed) Terrestrial

and marine geology of St. Croix, US Virgin Islands. West Indies

Lab. Special Publ No 8, pp 167–179

Hubbard DK (1992) Hurricane-induced sediment transport in open-

shelf tropical systems–an example from St Croix, United States

Virgin Islands. J Sediment Petrol 62:946–960

Hubbard JAEB, Pocock YP (1972) Sediment rejection by recent

scleractinian corals: a key to paleo-environmental reconstruc-

tion. Geol Rundsch 61:598–626

Hughes TP, Jackson JBC (1985) Population dynamics and life

histories of foliaceous corals. Ecol Monogr 55:141–166

Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: A

long-term perspective. Limnol Oceanogr 44:932–940

Hughes TP, Tanner JE (2000) Recruitment failure, life histories, and

long-term decline of Caribbean corals. Ecology 81:2250–2263

Hughes TP, Rodrigues RJ, Bellwood DR, Ceccarelli D, Hoegh-

Guldberg O, McCook L, Moltschaniwskyj L, Pratchett MS,

Steneck R, Willis B (2007) Phase shifts, herbivory, and the

resilience of coral reefs to climate change. Curr Biol 17:360–365

Humann P, DeLoach N (2002) Reef coral identification, Florida

Caribbean Bahamas including marine plants. New World,

Jacksonville, FL

Hunte W, Wittenberg M (1992) Effects of eutrophication and

sedimentation on juvenile corals. I. Abundance, mortality and

community structure. Mar Biol 114:625–631

Huston MA (1985) Patterns of species diversity on coral reefs. Annu

Rev Ecol Syst 16:149–177

Iglesias-Prieto R, Trench RK (1997) Photoadaptation, photoacclima-

tion and niche diversification in invertebrate-dinoflagellate

symbioses. Proc 8th Int Coral Reef Symp 2:1319–1324

Iglesias-Prieto R, Beltran VH, LaJeunesse TC, Reyes-Bonilla H,

Thome PE (2004) Different algal symbionts explain the vertical

distribution of dominant reef corals in the eastern Pacific. Proc R

Soc Lond 271:1757–1763

324 Coral Reefs (2010) 29:309–327

123

CC IP (2007) Climate Change 2007: The physical science basis.

Miller Contribution of Working Group I to the Fourth Assess-

ment Report of the Intergovernmental Panel on Climate Change.

Cambridge University Press, Cambridge, NY

Jackson JBC, Kirby MX, Berher WH, Bjorndal KA, Botsford LW,

Bourque BJ, Bradbury RH, Cooke R, Erlandsson J, Estes JA,

Hughes TP, Kidwell S, Lange CB, Lenihan HS, Pandolfi JM,

Peterson CH, Steneck RS, Tegner MJ, Warner RR (2001)

Historical overfishing and the recent collapse of coastal ecosys-

tems. Science 293:629–638

Jarrett BD, Hine AC, Halley RB, Naar DF, Locker SD, Neumann AC,

Twichell D, Hu C, Donahue BT, Jaap WC, Palandro D,

Ciembronowicz K (2005) Strange bedfellows-a deep-water

hermatypic coral reef superimposed on a drowned barrier island:

Southern Pulley Ridge, SW Florida platform margin. Mar Geol

214:295–307

Jokiel PL, Coles SL (1977) Effects of temperature on the mortality

and growth of Hawaiian reef corals. Mar Biol 43:201–208

Kahng SE, Kelley CD (2007) Vertical zonation of megabenthic taxa

on a deep photosynthetic reef (50–140 m) in the Au’au Channel,

Hawaii. Coral Reefs 26:679–687

Kahng SE, Garcia R, Spalding HL, Brokovich E, Wagner D, Weil E,

Hinderstein L, Toonen RJ (2010) Community ecology of

mesophotic coral reef ecosystems. Coral Reefs (this issue)

Kjerfve B, Magill KE, Porter JW, Woodley JD (1986) Hindcasting of

hurricane characteristics and observed storm damage on a

fringing reef, Jamaica, West Indies. J Mar Res 44:119–148

Kleypas JA, McManus JW, Menez LAB (1999) Environmental limits

to coral reef development: where do we draw the line? Am Zool

39:146–159

Kobluk DR, Lysenko MA (1992) Storm features on a southern

Caribbean fringing coral reef. Palaios 7:213–221

Kobluk DR, Lysenko MA (1994) ‘‘Ring’’ bleaching in southern

Caribbean Agaricia agaricites during a rapid water cooling. Bull

Mar Sci 54:142–150

Kuhlmann D (1983) Composition and ecology of deep-water coral

associations. Helgol Mar Res 36:183–204

Lang JC, Wicklund RI, Dill RF (1988) Depth- and habitat related

bleaching of zooxanthellate reef organisms near Lee Stocking

Island, Exuma Cays, Bahamas. Proc 6th Int Coral Reef Symp

3:269–274

Lapointe BE (1997) Nutrient thresholds for bottom-up control of

macroalgal blooms on coral reefs in Jamaica and southeast

Florida. Limnol Oceanogr 42:1119–1131

Lapointe BE, Barile PJ, Littler MM, Littler DS, Bedford BJ, Gasque

C (2005) Macroalgal blooms on southeast Florida coral reefs: I.

Nutrient stoichiometry of the invasive green alga Codiumisthmocladum in the wider Caribbean indicates nutrient enrich-

ment. Harmful Algae 4:1092–1105

Leichter JJ, Genovese SJ (2006) Intermittent upwelling and subsi-

dized growth of the scleractinian coral Madracis mirabilis on the

deep fore-reef slope of Discovery Bay, Jamaica. Mar Ecol Prog

Ser 316:95–103

Leichter JJ, Wing SR, Miller SL, Denny MW (1996) Pulsed delivery

of subthermocline water to Conch Reef (Florida Keys) by

internal tidal bores. Limnol Oceanogr 41:1490–1501

Lesser MP, Slattery M, Leichter JJ (2009a) Ecology of mesophotic

coral reefs. J Exp Mar Biol Ecol 375:1–8

Lesser MP, Slattery M, Stat M, Ojimi M, Gates RD, Grottoli (2009b)

Photoacclimatization by the coral Montastraea cavernosa in the

Mesophotic Zone: Light, food, and genetics. Ecology (in press)

Lessios HA (1988) Mass mortality of Diadema antillarum in the

Caribbean: what have we learned? Annu Rev Ecol Syst 19:

371–393

Liddell WD, Ohlhorst SL (1988) Hard substrata community patterns,

1–120 m, north Jamaica. Palaios 3:413–423

Liddell WD, Avery WE (2000) Temporal change in hard substrate

communities 10–250 m, the Bahamas. Proc 10th Int Coral Reef

Symp 1:437–442

Liddell WD, Avery WE, Ohlhorst SL (1997) Patterns of benthic

community structure, 10–250 m, the Bahamas. Proc 8th Int Coral

Reef Symp 1:437–442

Little AF, van Oppen MJH, Willis BL (2004) Flexibility in algal

endosymbioses shapes growth in reef corals. Science 304:

1492–1494

Littler MM, Littler DS, Hanisak MD (1991) Deepwater rhodolith

distribution, productivity, and growth history at sites of forma-

tion and subsequent degradation. J Exp Mar Biol Ecol 150:

163–182

Macintyre IG, Rutzler K, Norris JN, Smith KP, Cairns SD, Bucher

KE, Steneck RS (1991) An early Holocene reef on the western

Atlantic: submersible investigations off the west coast of

Barbados. W.I. Coral Reefs 10:167–174

Maragos JE, Jokiel PL (1986) Reef corals of Johnston Atoll: one of

the world’s most isolated reefs. Coral Reefs 4:141–150

Mass T, Einbinder S, Brokovich E, Shashar N, Vago R, Erez J,

Dubinsky Z (2007) Photoacclimation of Stylophora pistillata to

light extremes: metabolism and calcification. Mar Ecol Prog Ser

334:93–102

McCloskey LR, Muscatine L (1984) Production and respiration in the

Red Sea coral Stylophora pistillata as a function of depth. Proc R

Soc Lond B 222:215–230

Menza C, Kendall M, Rogers C, Miller J (2007) A deep reef in deep

trouble. Cont Shelf Res 27:2224–2230

Menza C, Kendall M, Hile S (2008) The deeper we go the less we

know. Rev Biol Trop 56:11–24

Merks RMH, Hoekstra AG, Kaandorp JA, Sloot PMA (2004) Polyp

oriented modelling of coral growth. J Theor Biol 228:559–576

Morrison D (1988) Comparing fish and urchin grazing in shallow and

deeper coral reef algal communities. Ecology 69:1367–1382

Mundy CN, Babcock RC (1998) Role of light intensity and spectral

quality in coral settlement: Implications for depth-dependent

settlement? J Exp Mar Biol Ecol 223:235–255

Mundy CN, Babcock RC (2000) Are vertical distribution patterns of

scleractinian corals maintained by pre-or post-settlement pro-

cesses? A case study of three contrasting species. Mar Ecol Prog

Ser 198:109–119

Nagelkerken I (2006) Relationship between antrhropogenic impacts

and bleaching-associated tissue mortality of corals in Curacao

(Netherlands Antilles). Rev Biol Trop 54(Suppl. 3):31–43

Pandolfi JM (2002) Coral community dynamics at multiple scales.

Coral Reefs 21:13–23

Phillips NW, Gettleson DA, Spring KD (1990) Benthic biological

studies of the southwest Florida shelf. Am Zool 30:65–75

Polunin NVC, Roberts CM (1993) Greater biomass and value of

target coral-reef fishes in two small Caribbean marine reserves.


Pomar L (2001) Types of carbonate platforms: a genetic approach.

Basin Res 3:313–334

Porter JW (1973) Ecology and composition of deep reef communities

off the Tongue of the Ocean, Bahama Island. Discovery 9:3–12

Proni JR, Huang H, Dammann WP (1994) Initial dilution of Southeast

Florida ocean outfalls. J Hydr Eng 120:1409–1425

Rahmstorf S, Cazenave A, Church JA, Hansen JE, Keeling RF, Parker

DE, Somerville RCJ (2007) Recent climate observations com-

pared to projections. Science 316:709

Reed JK (1985) Deepest distribution of Atlantic hermatypic corals

discovered in the Bahamas. Proc 5th Int Coral Reef Symp 6:

249–254

Rezak R, Gittings SR, Bright TJ (1990) Biotic assemblages and

ecological controls on reefs and banks of the northwest Gulf of

Mexico. Am Zool 30:23–35

Coral Reefs (2010) 29:309–327 325

123

Ridgway T, Hoegh-Guldberg O (2002) Reef recovery in disturbed

coral reef ecosystems. Proc 9th Int Coral Reef Symp 2:1117–

1121

Riegl B, Piller WE (2003) Possible refugia for reefs in time of

environmental stress. Int J Earth Sci 92:520–531

Rivero-Calle S, Armstrong RA, Soto-Santiago FJ (2009) Biological

and physical characteristics of a mesophotic coral reef: Black

Jack reef, Vieques, Puerto Rico. Proc 11th Int Coral Reef Symp

(in press)

Robbart ML, Aronson RB, Duncan L, Zimmer B (2009) Post-

hurricane assessment of sensitive habitats of the Flower Garden

Banks Vicinity. U.S. Department of the Interior, Minerals

Management Service, Gulf of Mexico OCS Region, New

Orleans, Louisiana. OCS Study MMS

Rodriguez-Lanetty M, Krupp D, Weis VM (2004) Distinct ITS types

of Symbiodinium in clade C correlate to cnidarian/dinoflagellate

specificity during symbiosis onset. Mar Ecol Prog Ser 275:

97–102

Rogers CS, Suchanek TH, Pecora FA (1982) Effects of Hurricanes

David and Frederic (1979) on shallow Acropora palmata reef

communities: St. Croix, US Virgin Islands. Bull Mar Sci

32:532–548

Rogers CS, Gilnack MG, Fitz HC III (1983) Monitoring of coral reefs

with linear transects: a study of storm damage. J Exp Mar Biol

Ecol 66:285–300

Rowan R (1998) Diversity and ecology of zooxanthallae on coral

reefs. J Phycol 34:407–417

Rowan R, Knowlton N (1995) Intraspecific diversity and ecological

zonation in coral-algal symbiosis. Proc Natl Acad Sci USA

92:2850–2853

Saunders MA, Lea AS (2008) Large contribution of sea surface

warming to recent increase in Atlantic hurricane activity. Nature

451:557–560

Sampayo EM, Francheschinis L, Hoegh-Guldberg O, Dove S (2007)

Niche partitioning of closely related symbiotic dinoflagellates.

Mol Ecol 16:3721–3733

Selig, ER, Harvell CD, Bruno JF, Willis BL, Page CA, Casey KS,

Sweatman H (2006) Analyzing the relationship between ocean

temperature anomalies and coral disease outbreaks at broad spatial

scales. In: Phinney J, Hoegh-Guldberg O, Kleypas J, Skirving W,

Strong A (eds) Coral reefs and climate change: science and

management. AGU Coastal and Estuarine Series, vol 61

Sheppard C (1981) The reef and soft-substrate coral fauna of Chagos,

Indian Ocean. J Nat Hist 15:607–621

Sheppard CRC (1982) Coral populations on reef slopes and their

major controls. Mar Ecol Prog Ser 7:83–115

Smith TB, Nemeth RS, Blondeau J, Calnan JM, Kadison E, Herzlieb

S (2008) Assessing coral reef health across onshore to offshore

stress gradients in the US Virgin Islands. Mar Pollut Bull

56:1983–1991

Smith T, Blondeau J, Nemeth R, Pittman S, Calnan J, Kadison E,

Gass J (2010) Benthic structure and cryptic mortality in a

Caribbean mesophotic coral reef bank system, the Hind Bank

Marine Conservation District, U.S. Virgin Islands. Coral Reefs

(this issue)

Stafford-Smith MG, Ormond RFG (1992) Sediment rejection mech-

anisms of 42 species of Australian scleractinian corals. Aust J

Mar Freshw Res 43:683–705

Stallings CD (2009) Fishery-independent data reveal negative effect

of human population density on Caribbean predatory fish

communities. PLoS ONE 4:e5333

Stoddart DR (1962) Catastrophic effects on the British Honduras reefs

and cays. Nature 196:512–515

Titlyanov EA (1987) Structure and morphological differences of

colonies of reef-building branched corals from habitats with

different light conditions. Mar Biol (Vladivostok) 1:32–36

Toller WW, Rowan R, Knowlton N (2001) Zooxanthellae of the

Montastraea annularis species complex: patterns of distribution

of four taxa of Symbiodinium across different reefs and across

depths. Biol Bull 201:348–359

Toller W, Lundvall S, Hoetjes P (2008) Some observations made

from ROV on mid-depth habitats and reef fish communities of

Saba Bank, Netherlands Antilles. Saba Conservation Foundation

Tomasik T, van Woesik R, Mah A (1996) Rapid coral colonization of

a recent lava flow following a volcanic eruption, Banda Islands,

Indonesia. Coral Reefs 15:169–175

Trnka M, Moulding AL (2006) Scientific review, compilation, and

assessment of coral spawning time in the Atlantic/Caribbean.

http://www.nova.edu/ncri/research/a21.html

Turner SJ (1994) Spatial variability in the abundance of the

corallivorous gastropod Drupella cornus. Coral Reefs 13:41–48

Underwood JN, Smith LD, van Oppen MJH, Gilmour JP (2007)

Multiple scales of genetic connectivity in a brooding coral on

isolated reefs following catastrophic bleaching. Mol Ecol

16:771–784

Van den Hoek C, Breeman AM, Bak RPM, van Buurt G (1978) The

distribution of algae, corals, and gorgonians in relation to depth,

light attenuation, water movement, and grazing pressure in the

fringing coral reef of Curacao, Netherlands Antilles. Aquat Bot

5:1–46

Van der Land J (1977) The Saba Bank – A large atoll in the

northeastern Caribbean. FAO Fisheries Report No 200, pp 469-

481

Venn AA, Weber FK, Loram JE, Jones RJ (2009) Deep zooxanthel-

late corals at the high latitude Bermuda Seamount. Coral Reefs

28:135

Vermeij GJ (1986) Survival during biotic crises: the properties and

evolutionary significance of refuges. In: Elliott DK (ed)

Dynamics of extinction. Wiley, New York, pp 231–246

Vermeij MJA (2005) A novel growth strategy allows Tubastreacoccinea to escape small-scale adverse conditions and start over

again. Coral Reefs 24:442

Vermeij MJA (2006) Early life-history dynamics of Caribbean coral

species on artificial substratum: the importance of competition,

growth and variation in life-history strategy. Coral Reefs 25:59–

71

Vermeij MJA, Bak RPM (2002) How are coral populations structured

by light? Marine light regimes and the distribution of Madracis.


Vermeij MJA, Bak RPM (2003) Species-specific population structure

of closely related coral morphospecies along a depth gradient

(5–60 m) over a Caribbean reef slope. Bull Mar Sci 73:725–744

Vize PD (2006) Deepwater broadcast spawning by Montastraeacavernosa, Montastraea franksi, and Diploria strigosa at the

Flower Garden Banks, Gulf of Mexico. Coral Reefs 25:169–171

Warner ME, LaJeunesse TC, Robison JD, Thur RM (2006) The

ecological distribution and comparative photobiology of symbi-

otic dinoflagellates from reef corals in Belize: potential impli-

cations for coral bleaching. Limnol Oceanogr 51:1887–1897

Webster PJ, Holland GJ, Curry JA, Chang H-R (2005) Changes in

tropical cyclone number, duration, and intensity in a warming

environment. Science 309:1844–1846

West JM, Salm RV (2003) Resistance and resilience to coral

bleaching: implications for coral reef conservation and manage-

ment. Conserv Biol 17:956–967

Weil E (2004) Coral reef diseases in the wider Caribbean: status and

prognosis. In: Rosenberg E, Loya Y (eds) Coral health and

disease. Springer, New York, pp 35–68

Weis VM, Reynolds WS, deBoer MD, Krupp DA (2001) Host-

symbiont specificity during onset of symbiosis between the

dinoflagellates Symbiodinium spp. and planula larvae of the

scleractinian coral Fungia scutaria. Coral Reefs 20:301–308

326 Coral Reefs (2010) 29:309–327

123

http://www.nova.edu/ncri/research/a21.html

Whitfield PE, Hare JA, David AW, Harter SL, Munoz RC, Addison

CM (2007) Abundance estimates of the Indo-Pacific lionfish

Pterois volitans/miles complex in the Western North Atlantic.

Biol Invasions 9:53–64

Wilkinson CR (2004) Status of coral reefs of the world 2004.

Australian Institute of Marine Science, Townsville

Wilkinson C, Souter D (2008) The status of Caribbean coral reefs

after bleaching and hurricanes in 2005. Coral Reef Monitoring

Network, Townsville

Willis BL, van Oppen MJH, Miller DJ, Vollmer SV, Ayre DJ (2006)

The role of hybridization in the evolution of reef corals. Annu

Rev Ecol Evol Syst 37:489–517

Woodley JD, Chornesky EA, Clifford PA, Jackson JBC, Kaufman

LA, Knowlton N, Land JC, Pearson MP, Porter JW, Rooney

KW, Tunnicliffe VJ, Wahle CM, Wulff JL, Curtis ASG,

Dallmeyer MD, Jupp BP, Koehl MAR, Niegel J, Sides EM

(1981) Hurricane Allen’s impact on Jamaican coral reefs.

Science 214:749–754

Coral Reefs (2010) 29:309–327 327

123

Assessing the ‘deep reef refugia’ hypothesis: focus on Caribbean reefs

Documents