1. science
2. mathematics
3. statistics

77(1), 2007, pp. 3-18
Ecological Monographs,
? 2007 by the Ecological Society of America
THE DEMOGRAPHICS OF A 15-YEARDECLINE IN COVER OF THE
CARIBBEAN REEF CORAL MONTASTRAEA ANNULARIS
Peter
Department
State
California
of Biology,
and
J. Edmunds1
Robin
18111 Nordhoff
University,
Elahi
Street,
USA
91330-8303,
California
Northridge,
in
the decline
trend of the last 25 years has been
On Caribbean
reefs, a striking
a species
that has dominated
coral Montastraea
annularis,
framework-building
but
such losses are important
for millennia.
the region
reefs throughout
Clearly,
ecologically,
causes
to be placed
of the proximal
in the context
to evaluate
their significance
they need
fully,
In this
and recruitment.
in cover
the potential
for gains
and balanced
growth
through
against
Abstract.
cover
of the
was
a population
in St. John, U.S.
censused
annularis
of M.
Islands,
annually
Virgin
a size-based
to quantify
The
model.
1988 to 2003
coral cover and construct
demographic
cover
to ascertain
was
to explore
in coral
and
of change
the mechanisms
model
developed
of M.
the cover
Over
the study
for future
period,
growth.
population
likely
trajectories
to ?12%
41%
in 1988,
but
remained
from
1999
declined
annularis
by
(a 72% decline)
study,
from
Between
for the last five years
of the study.
1988 and 2003,
colony
to 20 colonies/m2),
47 colonies/m2
and
the losses were
by 57% (from
to large colonies
and fission
driven mostly
of medium
(i.e., >151
by the death
cm2). By 2003,
more
<50
the population
small colonies
had proportionally
(70% were
large
cm2) and fewer
in
in 1988 (60% and 6%, respectively),
and
the changes
>250
than
colonies
(3% were
cm2)
structure
>14%
in terms of the rate of change
in population
size
had accelerated
population
statistically
declined
unchanged
abundances
to attain
of colony
size structure.
the time necessary
equilibrium
an ongoing
and
imminent
decline
coincident
population
cover.
coral
indicate
stable
Fifty-year
projections
apparently
and
this analysis
Importantly,
the recent
with
of
period
revealed
of M.
extirpation
of constant
at
annularis
this
the
likelihood
strong
to a continuation
(in contrast
structure
cannot
1988 population
be restored
reverse
until
decline
will
there is an amelioration
site
particular
that the
and suggest
cover)
It is unlikely
that the population
conditions
that kill individual
colonies.
low
recruitment.
of
the
marine
Caribbean;
coral; demographics;
Key words:
U.S. Virgin Islands; Yawzi Point.
Scleractinia;
Introduction
The
reefs
et al.
decline
of coral
ecological
widespread
et al. 2003, Pandolfi
et al. 2003, Bellwood
one of the best-known
of
examples
provides
global,
(Gardner
2004)
contemporary
Decreases
earliest
in coral
degradation
(Woodruff
cover were
recorded
in some
of coral
analyses
et al. 1981),
losses
in some
quantitative
1969, Woodley
the
century,
(Stoddart
the 20th
coining
from
biome
the
coral
Knowlton
become
(Roberts
more
have
Berkelman
et
uncertainty
concerning
Buddemeier
al.
1987),
frequent
2004).
et
1992,
al.
of
2004),
consensus
through
entirely
shifts
in
(Hughes
et
coral
there
by
St. John;
that
they will
change
et al. 2003),
(Hughes
relative
of
abundances
some
with
2003),
even
as
the
bellwether
of
reef
rather
than
most
likely
coral
species
their
altering
condition
et al. 2004).
Typically,
as "bad,"
with
interpreted
Bellwood
is
"good"
(Hughes
but
such
inferences
cover
nistic
1991)
provides
basis of
and
little
2000,
a decline
an
Gardner
can be misleading
information
regarding
the changes
serve
as
can
1984,
(Hughes
an ambiguous
(Connell
of coral
increase
being
et al. 2003),
coral
because
the mecha
1996, Babcock
indicator
of
A
and community
of population
dynamics.
as
cover
the
the
of
of
limitations
of
metric
good
example
comes
from
where
reefs
abundance
Jamaica,
species
as the poster
have
child
of Caribbean
reef
served
long
trajectories
still
reefs
is a
decline
revised
received
20 July 2005;
Manuscript
2 June 2006. Corresponding
Editor: M.
accepted
1E-mail:
[email protected]
al.
annularis;
and Tanner
events
(Hoegh-Guldberg
there
is
Although
the fate
growing
disappear
1997,
cover
region
the
throughout
similar
episodes
and
area; Montastraea
protected
serving
first-known
occurred
episode
1999,
2001,
the
attention,
of
justified
the switch
to describe
change"
"phase
to macroalgal
dominance
(Done
these
before
1992,
2004).
Shortly
since
(Knowlton
the end
of
John
and Aronson
ranges
(Precht
2004).
ecological
tool
in coral
for describing
The
changes
principal
cover
structure
of
is
the
percentage
community
analysis
the cover
of live scleractinian
coral
of benthic
taxa, with
2001).
of the
communities
by
locations
term
gained
widespread
wide
coral-bleaching
in 1987
Caribbean
much
reef
but
in St.
In
this
(Hughes
1994,
and
1996, Aronson
of community
location,
analyses
on both
16 years,
based
led at times
approaches,
1 June 2006;
H. Carr.
coral
cover
to dissimilar
3
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All use subject to JSTOR Terms and Conditions
Precht
structure
2001a).
over
and demographic
outcomes
(Hughes
4
PETER
Tanner
and
of
trajectory
traea annularis
changing
was
for
explanations
employing
population
of
1973,
assessing
the
communities,
Sheppard
structure
than
community
frame-building
wide
losses
1980s
200\b)
of reefs
20016).
traea
has
and Meesters
Bak
roles.
Changes
(sensu Goreau
on coral
effect
corals
in
greater
in cover of secondary
changes
For
the Caribbean
example,
Aronson
1982,
(Gladfelter
a long and
had
enduring
the
throughout
Caribbean
Among
(Aronson
region
these
Jackson
like M.
and
Tanner
2000)
et al.
Bythell
The
et al.
and
elsewhere
Edmunds
of
area
Rogers
which
of
at 9-m
is the
annual
cover
and
adverse
small
by
charac
and
(Dustan
Halas
1987,
over
and
dynamics
of St.
reefs
(see Plate
last
the
surveys
the fate
of
as
of
years
(Collet?
Beets
Edmunds
2001,
in cover
is the decline
changes
off Yawzi
depth
subject
43
Point
the present
study.
a source
of data
colonies,
here
we
recruitment
(Edmunds
and
2002).
of M.
2002),
15 years
Using
on percentage
present
our
to project
the population
an
for
test
effect
the
for
structure
the
varying
selected
We
because
investigation
the
demo
of
structure.
population
throughout
et al.
Rogers
1979,
which
of
representative
we
extend
and
rare
are
species
is
Second,
dynamics.
graphic
approach
over
50 years
on
recruitment
recruits
Caribbean
of
this
and
(Bak
and Tanner
1984, Hughes
an
the possibility
that this represents
trait whereby
organ
important
life-history
long-lived
isms "store"
the effects
of infrequent
successful
recruit
Engel
2000),
ment
a
raises
and Chesson
(Warner
as
at
Edmunds
1985,
is well
trait
life-history
a "masting
known
tree
many
over
where,
large
trees
synchronously
strategy,"
intervals,
irregular
Such
2002).
for
of seeds
1994, Koenig
produce
large quantities
(Kelley
and Knops
and
has considerable
relevance
2005),
clearly
cover
to understanding
the basis
of M.
of declining
annularis
Unfortunate
1992, Edmunds
2002).
(Jackson
the occurrence
a masting
time scales
of
the mismatch
by
of
effect
is
of most
vs.
to decades)
like M.
annularis
years
(from
organisms
of M.
that populations
even within
deteriorate,
recruitment
colonies
until
rate,
will
annularis
this MPA
and
rates
mortality
to
continue
of
regardless
of established
decline.
Methods
Estimates
The
coral
analyses
depth
along
using
three
(Appendix
positioned
each
sects,
contiguously
in
10 m
were
transect)
1989) from
a Nikonos
35-mm
film
1988
V
990,
(Nikon
Coolpix
In both
2000 onward.
strobe
(Nikonos
SB
at
to
3.34
cases,
off Yawzi
Point
photoquadrats
tran
permanent
(10/
in a
photoquadrats
statistical
for
replicates
differences
among
in 1988
(twice
annually
were
The pictures
taken
testing
least
to 2003.
camera
1988
from
The
length.
as
treated
measures
design
repeated
times and were
recorded
and
cover
of coral
at 9-m
community
was
A)
quantified
with
of the reefs
1). Most
a marine
within
have
been
protected
and
1962
since
Teytaud
(MPA)
(Rogers
Beets
but
have
still
and
2001),
they
Islands
changed
extensively
Earle
1972, Rogers
of these
One
aspect
annularis
corals
these
2002).
the population
study addresses
on
the shallow
annularis
John, U.S.
Virgin
in this
location
1988,
characterized
1995).
1993,
present
of Montastraea
protected
species
cover
changing
indicates
large colonies,
of
periods
survived
goals.
to
1967,
(Mesolella
record
fossil
form
of
suggest
Montas
terms
we
a demo
First,
develop
causes
the
of the
identify
proximal
of M.
and to test whether
annularis
the
two
approach
in cover
changes
trend
Monographs
Vol. 77, No. 1
results
to centuries)
1992). The
(Jackson
(from decades
the
of
limitations
underscore
of the present
analyses
to assess
and
condition
coral-reef
coral cover as a means
Precht
Together,
the negative
consequences
ecological
in cover of
declines
of the ongoing
novelty
in Jamaica
and
1994, Hughes
(Hughes
temporal
annularis
M.
than
(Johnson
underscore
teristics
that
have
better
colonies
the
corals
annularis,
conditions
millennia
Moreover,
1992).
Caribbean
that
for
roles
accomplish
ecological
investigations
to long-lived
those
relevant
provides
cover
this species
critical
in coral
because
plays
changes
in reef
construction
and
roles
community
ecology
1959, Barnes
1973, Knowlton
1992) and has
(Goreau
fulfilled
to
graphic
Ecological
ELAHI
ly, demonstrating
made
difficult
the ecology
and Precht
corals,
case
in
reef-building
a special
annularis
and
on
effect
ROBIN
populations
areas
and
1999).
trends
in coral
temporal
of changes
in cover
varies
species.
corals
of
the
frame-building
Acropora
to white
A. cervicornis
band
due
disease
and
palmata
in the
corals
frame-building
a
have
1982)
primary
2003,
the
general,
still remains
in
significance
and
their
ecological
species
of
1984,
(Hughes
1988, Babcock
1987,
and Miller
scleractinian
(Connell
terms
1959,
of
biology
known
poorly
In
cover
Lirman
2000,
et al. 2005),
Glynn
Smith
2005,
in part by
Cas well
2001).
(sensu
in
have
been
used
approaches
to investigate
the causes
and
in coral
changes
Jackson
1985, Done
AND
population
cover,
projections
of
and
Fong
Edmunds
in coral
changes
population
consequences
and
Hughes
among
cover
the
demographic
studies
designed
1991,
a downward
1987,
2000). More
importantly,
Hughes
were
a demographic
to use
able
(2000)
as possible
evaluate
several
mechanisms
to
Although
several
and
coral Montas
reef-building
to the upward
of
trajectory
number
of
(i.e.,
colonies)
contrary
size
population
Tanner
and
(Hughes
and Tanner
approach
1986
2000).
During
cover
of the
J. EDMUNDS
and
(Nikon,
Tokyo,
Japan)
camera
a digital
1999 and
megapixel
the camera
105) and
to the
attached
from
resolution)
was fitted
with
to a framer
a
that
35-mm
it perpendicular
reef so that each
a photoquadrat
in size and
1 X 0.75 m
recorded
a photoquadrat
in
1 X 1m
recorded
each digital
frame
were
to determine
the percentage
used
size. The pictures
held
frame
cover
of
grid
on
coral
a
each
image with
overlaying
and
the
dots
dots
counting
randomly
placed
on M.
were
tissue.
Dots
scored
annularis
scleractinians
of 200
by
to quantify
the contribution
separately
structure.
Because
coral
community
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of
this
statistical
species
indepen
to
POPULATION DYNAMICS OF MONTASTRAEA
2007
February
5
M%%
*jj&&toea&*i
w^rnm
'
?
-:*
fc?'-,;
Plate
1. View across
the study reef at Yawzi
St. John, U.S. Virgin
has a coral fauna dominated
Point,
Islands, which
by
Montastraea
annularis. The photograph
shows a portion
that have been monitored
of the reef that lies along one of the transects
since 1987, and which provide
records within photoquadrats
of the fates of individual
colonies
lobes) that are the
(= autonomous
core of the present analysis.
Photo credit: P. Edmunds.
dence
the
among
assumption
of
assumption
was
(1988) and
examined
for
(2003) of
Neumann's
test
for
serial
Rohlf
and
the
important
this
applied,
transect
at the
each
the end
1995)
as
annularis
an
is
photoquadrats
statistical
procedures
the
the study using
von
and
(Sokal
of Montastraea
independence
cover
percentage
a dependent
variable.
start
For
all
transects
at
were
the quadrats
times,
statistically
independent
=
<
<
n
not
and were
2.468,
10, P > 0.05)
r|
(0.979
autocorrelated
significantly
B).
(Appendix
both
Demographic
The
density
colonies
time,
a demographic
autonomous
areas
photographic
cm diameter
also
were
Colonies
analysis.
of living
coral
were
to
used
the results
the
quantify
annularis
used
were
tissue
determined
to complete
as
defined
(after Connell
over
intervals
of
and
The
1993-1998,
1998-2003).
as small
as 1
allowed
colonies
sampling
to be resolved,
the five-year
and
interval
the temporal
to
resolution
detect
necessary
in colony
and
sizes (i.e., growth
was quantified
structure
changes
The
population
images,
which,
scanning
to
the originals.
The
used
digital
images were
abundance
and size-frequency
distribu
colony
as
the start and end of each five-year
interval,
over
the fate
of colonies
the same
intervals.
quantify
tion at
well
as
for
the
color
slides,
statistical
were
shrinkage).
using
digital
obtained
by
the
from
which
number
of
as
served
size was
and
as
assessed
a
the
replicate,
colony
area of coral
tissue as measured
planar
using NIH
Image
1.63 software
Institutes
of Health,
Bethesda,
(National
was
The
distribution
USA).
Maryland,
size-frequency
prepared
consecutive
the
by measuring
size
measured.
using
four
range
of
of
until
photoquadrats
all
colonies
Size-frequency
size classes
were
that
were
and
size-based
using
to
selected
encountered
within
were
colonies
?500
distributions
sizes
colony
of populations
dynamics
Montastraea
individual
and
1973), and their fates
five years
(1988-1993,
provided
were
photoquadrats
and
size of
over
analysis
was
determined
density
in each
photoquadrat,
Colony
colonies
models).
Demographic
were
Population
dynamics
quantified
at the start
whether
the colonies
present
prepared
the
span
the
capture
matrix
models
{Methods:
were
they
were
Colonies
those
or dead
alive
whether
from
assess
the
at
the end
had
grown,
tracked
using
and end
start
of
the
shrunk,
the
of
by
recording
of each
interval
interval
if alive,
and,
or
fused,
split.
with
digital
pictures,
the intervals
to
serving
changes
in size
variations
in position
the photoquadrat,
of
or uncertain
fate
quality,
colony
(e.g.,
or fusion).
For
colonies
undergoing
and
those
from
the intervening
to ensure
used
of
being
unequivocal
tracking
not possible
It was
to track all colonies
in the
colonies.
as some
not be relocated
to
could
due
photoquadrats,
years
slight
impaired
image
complex
shapes
fusion
the
during
intervening
were
fusing,
years
with
the pictures
intervals,
study
were
to determine
which
used
the size of
the fused
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colony
from
colonies
determined
the
6
PETER
from
at the end of
the picture
in a similar way,
tracked
were
determined
products
interval.
To
from
traea
at 9-m depth
between
and
screened
for
At
the
among
sibling
the high abundance
although
reefs suggests
that most
nearby
pooled
<40-mm
those
fission
or
(after Weil
not possible
and
by
this
in
on
the
annularis
recruits
to
taxon
belonged
abundance
of
juvenile
1994 and 2004
between
annually
were
and
2002,
(Edmunds
2004)
using
completed
X
at multiple
0.5
located
(0.5
m)
randomly
quadrats
coral
sites
>200
Juvenile
per year).
(mostly
quadrats
corals
was
recorded
density
to species,
identified
M.
annularis
juvenile
the data
pooling
was
among
Density
years
among
compared
sites.
occurs.
In
at a rate of four
year
was
period,
to the
25th
added
smallest
size
The
year).
was projected
the population
and high
recruitment
episodic
at a rate of 20 recruits
per
These
period.
in the fifth
class
for
the
no
models
Demographic
based matrix
procedure
The
intervals.
five-year
as
defined
categories
(>50 cm2 but <150
<250
and
cm2),
transition
in the Yawzi
that
recruitment
Point
given
is probably
too low to detect,
than absent.
rather
In contrast,
rates applied
in the second
the recruitment
estimate,
habitat
third projection
the effects
(i.e., testing
were
recruitment,
episodic
respectively)
extreme
to the known
relative
recruitment
the
and
class,
rate
intrinsic
at
characterized
in each
nies
X and
(available
of sexual
and
necessary
of colonies
class
fates.
Because
colonies
were
formed
for
one
any
of
fate
rate
of consistent
to
by
size
size
four
classes
each
size
calculate
(i.e.,
a
exceeds
for
2000);
a population
in each
using
transition
probabilities
population
growth
unless
<1,
the
rate
mortality
(Hughes
related
p is inversely
the
stable
to achieve
size
class.
PopTools
had
(X).
of
size
numbers
matrices
Elasticity
2.4 to determine
the
greatest
asexual
1984, Hughes
to the time
constant
provide
of the
were
on
this
recruitment
of M.
annularis.
of M.
annularis
analyses
using
times with
among
arcsine-transformed
overall
effect
sures
of
were
intervals
were
completed
Systat
using
Illinois,
Evanston,
(SPSS,
USA)
estimation
for
the matrix
parameters
cover was
2000. Coral
Excel
compared
bootstrap
completed
a repeated-measures
percentage-cover
time was
detected,
with
compared
ANOVA
data.
consecutive
separate
ANOVA
using
an
When
sample
repeated-mea
was
used
to
One-way
of Montastraea
annularis
colonies
density
with
hoc multiple
among
years,
post
comparisons
a Bonferroni
with
For
all AN
completed
procedure.
of normality
the assumptions
and homoscedas
OVAs,
ANOVAs.
the
compare
were
of
graphical
analyses
were
non
not met,
assumptions
were
used.
contin
parametric
procedures
Chi-square
to compare
tables were
used
the size-frequency
gency
ticity
tested
through
the
residuals;
where
distributions
among
of fission
which
effect
for
of
the
analyses
software
9.2
version
frequency
In order
population
estimation
(www.cse.csiro.au/cdg/poptools)
from
Statistical
with
to be
scaled
rates
serve
area
to
shallow
nearby
an ecological
context
within
which
the veracity
can be evaluated.
recruitment
scenarios
tested
recruitment
Statistical
the colonies
for
to explore
the potential
species,
simply
to restore
structure
the 1988 population
In all cases,
estimates
the empirical
was
fission
p were
a value
has
calculated
2
II
online)2
proliferation
and Tanner
also
four
2.4
calculated
using
PopTools
in Excel
In the absence
2000.
running
X measures
the rate of population
recruitment,
structure);
decline
size
the
growth
(X) and the rate (p)
to a structure
converged
of colo
relative
abundances
population
by constant
the
on
based
cm2),
size
of
and
the
(>250
cm2),
size classes
calculated
the mortality
were
used
matrices
of
I (<50
probabilities
to > 1. The
of population
the
which
among
calculate
the
using
for each
1984)
were
IV
colony
(i.e., new
summed
to
class
class
transition
splitting),
class
sometimes
used
size
size
common
relatively
prepared
(Hughes
matrices
a
cm2),' size class III (>150 cm2 but
probabilities
from
the
empirically
was
were
(i.e.,
rates
In brief,
however,
is a conservative
recruitment
and
models
were
recruits
iteration
recruitment
in the discussion.
of
the population
that
consistent
projection,
rationale
is presented
assumption
to the
is similar
and
Demographic
by
population
recruit
steady
per square meter
per five
to the smallest
size class of the
this
Third,
population
with
the assumption
that
25 years
occurred
every
square meter
per 25-year
the
annularis
vector
the population
the
with
starting
recruits
vector.
tested
by
of Montastraea
and
of this analysis
the final
year
(2003)
for 50 years.
Three
increments
in five-year
were
the
First,
population
completed.
was
with
of no
the assumption
projected
recruitment
ment,
the
of
Monographs
Vol. 77, No. 1
a scenario
that apparently
recruitment,
recent history
reef. Second,
of the study
was
with
the assumption
projected
added
were
several
genus,
although
M.
annularis.
including
by
matrices,
population
structure
in
projections
structure
2004])
by multiplying
the
for all juvenile
and one
were
structure
population
proceeding
of
the
of
the
for
species.
Surveys
were
out
carried
the
Ecological
ELAHI
projected
of Montas
2000,
(i.e.,
created
species
of M.
situ,
The
at 5 m,
not
clearly
annularis
complex
this small size, it was
of M.
distinguish
this
rate
Point
colonies
of
end
ROBIN
was
the fission
the
in Edmunds
juvenile
were
that
fragmentation)
Knowlton
1994).
to
at
and White
Horn
events
Fission
size of
recruitment
[described
Cabritte
diameter
the
the study
reef, surveys
sites (five sites
shallower
at mostly
corals
interval.
with
the picture
the
into
insight
gain
on
annularis
the
AND
J. EDMUNDS
describing
to
as well
sampling
periods,
events
size classes.
among
calculate
variance
estimates
parameters
procedure
the
fate
X, and
(mortality,
was
to
applied
of
colonies.
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All use subject to JSTOR Terms and Conditions
These
as
for
the
the
p), a bootstrap
raw
data
the
data
were
7
POPULATION DYNAMICS OF MONTASTRAEA
2007
February
Census
period
B
1988
100
1993
1998
2003
I
IV
Size
class
on a reef at 9-m depth at Yawzi Point, St. John, U.S. Virgin
trends in coral community
Islands.
Long-term
dynamics
of coral cover at each survey period between March
1988 and August
2003. Note
that two surveys were completed
(A) Percentage
? SE (vertical lines above bars) are shown for sample sizes of n = 30 quadrats/survey
in 1988 and 1989. Means
1989
except October
=
1990 (n = 29), and April
1992 (n = 20). Montastraea
annularis accounted
for 94.2% ? 0.9% (mean ? SE, n = 18)
(n 28), September
structure of M. annularis at the start and end of each five-year
of the coral cover in all surveys. (B) Population
interval (1988-1993,
used to construct
the matrix models
is based on the surveys completed
in
1993-1998,
1998-2003)
(Appendix C). The 1988 analysis
March
1988. The size-frequency
show the percentage
distribution
of colonies
the size classes
among
analyses
(I-IV, Appendix
B)
= 571 colonies
the matrix models
used to construct
in 1988, 499 in 1993, 501 in 1998, and 510 in 2003). Inset graphs show the
(n
= 15-30
mean
per year).
colony densities
(?SE, n
quadrats
Fig.
1.
with
replacement
using
added
into Excel
{available
online)3
sets were
with
this
data
generated
a
resampled
was
to calculate
used
classes
to calculate
1000 values
a mean
and
The
confidence
and
97.5th
evaluate
significance
vals.
3
One
procedure,
rate by size
mortality
Results
routine
thousand
and
class
Estimates
and
to
matrix
of four
population
consisting
as previously
that was used
(I-IV,
described)
X and p using
2.4. The
resulting
PopTools
to calculate
for mortality,
X, and p were used
95%
were
of
percentiles
differences
between
based
(www.resample.com)
on
for
intervals
confidence
intervals
determined
the
data
mean
nonoverlapping
each
from
metric.
the 2.5th
and
were
used
values
for
statistical
confidence
inter
to
cover
of coral
each
a size-based
create
size
software
2000.
on
cover
the coral
2003, much
lost
of
several
study
during
periods
rapid
with
the aftermath
of Hurricane
decline
Hugo
beginning
between
1994
and
and
(September
1989)
continuing
1999 (Fig.
coral cover differed
1A). Overall,
significantly
across
the annual
df = 14, 406; P <
surveys
50.438;
(F=
the results
from October
0.001;
1989, September
1990,
Between
1988
and
of
reef was
the
1992 were
to incomplete
omitted
due
data
April
ANOVAs
sets).
Separate
repeated-measure
comparing
consecutive
revealed
declines
between
years
significant
and
April
increased
1989 (P < 0.001), and for all
1989 and October
of
pairs
between
years between
1997
and
between
1994
1999
1996
and
(P
and
1996
<
(P <
0.013).
=
1997
(P
This content downloaded from 130.166.34.124 on Thu, 07 May 2015 19:17:37 UTC
All use subject to JSTOR Terms and Conditions
and
0.008),
cover
Coral
0.004),
but
all
8
PETER
J. EDMUNDS
ROBIN
AND
The
best
estimate
annularis
to
juvenile
shallower
corals
the
reefs
In
these
of
and
relatively
detected
easily
of reef
large areas
1994 and
between
surveys,
to 60 m2) annually
colonies
of the M.
juvenile
at densities
found
from
ranging
annularis
complex
0 colonies/10
m2 to
densities
did not vary
1.5 colonies/10
m2
(Fig. 2). These
11 years
the
among
significantly
surveyed
n > 80 quadrats/yr,
Wallis
test, H=
10.365,
n?i?i?i?i?i?i?r
1994
1996
On
1998
2000
2002
2004
Fig.
2. Density,
of juvenile
colonies
number
(<4 cm
of Montastraea
annularis
in St.
per 10 m
diameter)
complex
were
John between
1994 and 2004. Values
obtained
from
at two sites in 1995 (n = 80), five
(0-25 m2) censused
quadrats
=
sites in 1994 and 1996-1998
(?
200), and six sites in 1999-2004
=
the sixth
(n
240). Five of the sites were at 5-m depth, with
? SE
in the surveys from 1994) at 9-m depth; means
(included
are shown.
the actual
ity of
colonies
made
reef,
study
the
recruits.
However,
each
(30 quadrats
annularis
colonies
of M.
diameter
colonies
are
that
topographic
abundance
high
of
of
0.25-m2
between
1996
this
consecutive
indistinguishable,
Between
1988
out
of
intervals,
including
those
and
to
(from 43.4%
most
the five
annularis
sampling
but
remained
sampling
the dominant
remained
the
for
study,
accounting
the coral cover
in the
The
of
(94.7%)
majority
of M.
annularis
in March
declined
cover
coral
2003,
12.3%),
recent
Demographic
of
density
estimates
over
varied
due
with
both
annularis,
reduced
number
>1215
varied
trends
5.632,
in
through
? 0.9%
94.2%
and
by
this
2003,
intervals
67.837,
number
of
in cover
occur
at densities
products)
to the highest
which
is similar
reduction),
smaller
four
pairwise
small
in
density
the 11 years of surveys
2). Overall,
a mean
water
in shallow
density
provide
population
?
M.
of 0.36
of juvenile
annularis
0.08
colonies(10
?
n =
2316
SE,
(mean
quadrats
[pooled
m2)-1-yr-1
we conservatively
and therefore
estimate
among
times]),
m2,
shallower
water
(Fig.
and
size-frequency
in the more
colonies
both
small
found
(1-2
in all
recent
and
cm2)
annularis
declined
from
the
of
densities
colonies
a mean
of
47
in 2003 (a 57%
in
1998
and
2003 differing from the density in 1988 (P < 0.040). No
other
plus
colonies/10
recorded
of Montastraea
distribution
in 1988 to 20 colonies/m2
with
of ?1.8
1993,
1998, 2003)
(1988,
df = 9, P < 0.001),
largely
an
of
colonies
and
larger
were
of M.
colonies/m2
suggest
<40-mm
had
(>700
intervals,
cm2)
were
three
of the 499
colonies
tracked
1993,
cm^ in area. Additionally,
the density
of colonies
the four years
of
that are representative
among
=
across
cover
in coral
the three
intervals
(F
P = 0.001).
df = 3,100,
the population
Overall,
density
juvenile
analysis
decline
IB). However,
(Fig.
colonies
of
for
2004
years
(?SE,
?=18).
cover was
composed
size-frequency
The
changed.
at five-year
time (%2=
intervals
large
and
the
the
colonies
a
to
increased
scleractinian
1988,
72%
by
area)
and
to 90.3%.
slightly
In concert
declined
2003.
among
unchanged
Montastraea
years.
a mean
18 sampling
the coral
were
statistically,
to
1999
from
complex
of
small
(i.e., colonies
of juveniles
species
a combination
fission
other
(Kruskal
P = 0.409).
3),
produced
by fission
(Fig.
to unequivocally
sexual
identify
to survey
small areas on this
attempts
reef
small
the high
the
substratum,
annularis
of M.
it problematic
that
the
juveniles
smooth
are
and
2004,
were
for
surveys
facilitated
recruits
coral
of large areas
corals
small
consist
(Edmunds
2000).
were
sampled
(up
bay.
shallow
of
from
in mostly
diameter)
In comparison
to the
same
detection
of Montastraea
comes
<40-mm
the
which
upon
Monographs
Vol. 77. No. 1
recruitment
reef
study
areas,
unambiguous
because
they
rock
the
of
(i.e.,
of the
areas
reef
deeper
Ecological
ELAHI
comparisons
were
significant
(P
>
0.069).
1988-1993
1993-1998
Census
1998-2003
period
Fig.
3. Percentage
of Montastraea
annularis
colonies
fusion or fission over three survey intervals between
undergoing
1988 and 2003. Sample sizes are 326 colonies between
1988 and
1993 and 1998, and 250 between
1998 and
1993, 309 between
2003. Inset graphs
show the percentage
allocation
of colonies
fission among four size classes (I-IV; Appendix
undergoing
C).
1988 and 1993, 44 between
Sample sizes are 30 colonies between
1993 and 1998, and 24 between
1998 and 2003.
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POPULATION DYNAMICS OF MONTASTRAEA 9
February 2007
that
the
rate
recruitment
not
did
exceed
this
of
this
to the
species
100
reef
study
value.
models
Demographic
Analyses of the photoquadrats identified 326 colonies
that could be tracked between 1988 and 1993, 309
colonies between 1993 and 1998, and 250 colonies
between 1998 and 2003. Most colonies (>75%) were in
size
I and
classes
II for
all
time
were
fewer
intervals;
found in the larger size classes (III and IV), especially in
the final time interval (Appendix C). The reduction
across
the
three
time
in number
intervals
could be tracked reflects
colonies as the population
the
1). For
varied
(Fig.
fates
stasis,
or
13.5%
of
that
colonies
were
but
of colonies
could
be
biased
strongly
their
tracked,
towards
death,
and
4.7%
C). Between
(Appendix
in the smaller
size classes
shrinkage
the colonies
that
the difficulty of locating
density declined by 57%
II III
I, II,
(i.e.,
and III) grew into larger size classes between 1988 and
1993, but <5.3% of the colonies in the smaller size
classes
into
grew
intervals
numbers
in some
and
numbers
colony
each size class
When
subsequent
However,
C).
relatively
large
were
affected
and fusion,
by fission
resulted
in a net
in
fission
increase
cases,
so
the
that
transition
to >
summed
C).
of
colonies
fusion
undergoing
five-year
means
?
procedure
of Montastraea
annularis
mortality
Percentage
in four size classes
C) over three
(I-IV; Appendix
shown are
intervals between
1988 and 2003. Values
95% CI that were obtained
by a bootstrap
sampling
of the original data.
(1000 iterations)
was
declining
values
show
population
These
(1988-1993),
C]).
3.3% (11 colonies) of the colonies fused, and this rate
remained largely unchanged (3.2% [10 colonies]) over
the next interval (1993-1998), finally declining to 0.4%
(one colony) between 1998 and 2003 (Fig. 3). The
proportion
4.
Fig.
colonies
for
probabilities
1 (Appendix
were
highest
abundances
colony
two
in the
size classes
larger
(Appendix
of colonies
the
among
to
compared
significant
confidence
resampling
colonies
the
three
number
undergoing
intervals
of
colonies
of
the
The
small
numbers
number
relative
of
fission was
among
iadistinguishable
=
P = 0.088),
df =2,
and the
(%2 4.856,
was
fission
undergoing
independent
of the size class and study intervals (Fig. 3; x2 = 6.807, df
=
=
6, P
Mortality
0.339).
rates
(per
five-year
period)
were
highest
(>36%) for size classes I and II for each of the three
intervals
The
still were
but
highest
I over
the final
on
Based
C).
Appendix
for mortality
rates
the
95%
III and
classes
(56%) was
rate
mortality
in size class
in size
>11%
recorded
interval
IV.
for corals
(1998-2003;
confidence
intervals
obtained
by bootstrap
resampling,
rates displayed
size classes
differences
among
mortality
intervals
that differed
between
(i.e., there was a
sampling
interval
sampling
appears
to be
X
size
caused
class
largely
by
This
interaction).
the mortality
effect
rates
for
size classes III and IV in the 1993-1998 interval, both of
which
have
confidence
are
that
intervals
non-overlap
ping with those for size class I in all sampling intervals
(Fig. 4).
The
transition
matrices
were
of mortality
and
shrinkage,
rates
of population
change
dominated
and
(k)
therefore
all
are
rates
by high
the intrinsic
<T
(i.e.,
the
the
as
=
2, P
0.043),
between
fusing
because
largely
1998 and 2003.
over
each
interval
that
the
population
[Appendix
decline
slowed by 2% over the second interval (X = 0.673)
=
compared to the first interval (X, 0.661), but the decline
accelerated by 14% in the final interval (X = 0.581)
= 6.266, df
three study intervals changed significantly (%2
=
class
Size
second
a
reveals
X,
obtained
measure
to a stable
converges
analysis
the
The
D).
(Appendix
a relative
provides
from
for
intervals
this
interval;
assessed
size
overlapping
by
bootstrap
ratio
damping
structure,
and
increase
in
(p)
a cohort
in the present
tempo
over
the
of
increases)
not
95%
the rate at which
of
slight
was
trend
p
(i.e.,
dynamics
15-year
population
on the replicate
values
of p obtained
Based
by
period.
for p were
similar
the mean
values
resampling,
bootstrap
two sampling
but a 7% increase
in the first
intervals,
between
occurred
trend
was
not
the
significant
and
second
as
the
assessed
third
interval;
from
the
this
overlap
ping 95% confidence intervals (Appendix D).
The elasticity matrices
(Appendix C) reveal
sensitivities
proportional
transition
probabilities,
the transition
cating
on X. The
the
(i.e.,
three
the
relative
intervals^
II?II
of X to changes
with
the largest
in each
elasticity
with
the greatest
probability
values
of the elasticities
vary
with
transition
the
stasis
of
probability)
size class
having
the
the
of
indi
effect
among
II colonies
the greatest
effect on X for the first (elasticity = 0.224) and third
intervals
(elasticity
IV colonies
having
interval
(elasticity
intervals,
a
ity would
=
the stasis of size class
and
0.326),
the greatest
effect on X, for the second
=
10% change
0.215).
in the
In the first and
II?II
transition
third
probabil
alter X by 2% in the first interval, and 3% in
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Ecological Monographs
Vol. 77, No. 1
PETER J. EDMUNDS AND ROBIN ELAHI
10
150
400
Size
class
I
II
class
Size
Years
Years
that recruitment
annular is, assuming
Fig. 5. Fifty-year
C) for Montastraea
by size class (I-JV; Appendix
projection
population
structure in 25 m2 of the study
are based on an initial population
from the population
vector determined
does not occur. Projections
and trajectories were
in each of size classes I, II, III, and IV, respectively),
reef in 2003 (Fig. IB; 355, 118, 21, and 16 colonies
=
from 1998-2003
in five-year
increments
calculated
0.581; Appendix
C), as well as the
(for which X
using the transition matrix
to the 95% confidence
intervals (CI) for X (Appendix D). For size classes I?III, the projections
matrices
corresponding
bootstrapped
for the upper 95% CI
For size class IV, the projection
based on the actual matrix.
based on the 95% CI for X flank the projections
were lower than the projection
and therefore are not shown.
for the actual matrix
the
third
the
IV?IV
To
in
transition
better
the
in the
interval;
understand
the
population
continued
projection
without
future,
The
years.
first
conditions
traea
annularis
defined
by
2003:
355,
I, II,
III,
second
probability
the
how
the
of
regarding
the reliability
different
site with
areas
shallower
to
density
areas
that
of
vector
reef
in
size classes
recruitment
rate
estimated
from
of
uncertainty
to a
these data
annularis
recorded
an outcome
2]) revealed
with
0 recruitment
Edmunds,
data).
unpublished
from
the matrix
using
pleted
two
matrices
additional
and
in
very
(P. J.
was
com
projection
1998-2003
C)
(Appendix
to the X
corresponding
The
intervals
confidence
the upper
and
lower
95%
marking
the percentage
Even
of
for this metric.
though
coral
cover
values
appeared
to
have
stabilized
at
over
?12%
this
2003
and
period
second
and,
to
taken
projection
addition
the
years,
cm2) will be dead,
of colonies
density
(>250
be
or
0,
rate
of population
intervals
(Figs.
near-zero,
(X)
growth
5 and 6).
projections
of recruitment
were
calculated
using
were
for
to gain
ameliorate
place
was
of
corals-m~2-(5
than
higher
the
again,
was
projections
recruitment
rate
third
scenarios
significantly
an
reveals
to
selected
of Montastraea
the matrix
1998 to 2003 (Appendix C). The goal of these
from
has
and
two
change
projection
25
Within
size
of the intrinsic
regardless
within
the 95% confidence
incorporate
annularis
the
the population
will
classes
three
other
not
did
1),
collapse.
annularis
population
of M.
largest colonies
50 years,
and within
the
and
(Fig.
imminent
The
to 0
a
characteristics;
set to 0.04/m2
the recruitment
M.
1999
between
in
substratum
juvenile
[Fig.
obtained
of
set
(Fig. 2) because
of extrapolating
with
completed
projection
(the mean
population
in 25 m2 of
in each
We
IV; respectively.
the
recruitment
using
shallower
similar
colonies
and
instead
the
the
16 colonies
118, 21, and
of Montas
recruitment
with
of
number
nearby
deeper
change
study reef might
over
was
50
projected
that
the
2003
assumed
started
and
a 10% change
in
alter X by 2%.
interval,
would
this
surveys
between
into
the
insight
the population
2003.
1988 and
to
identical
recruitment
to
rate
yr)_1. This
the best
estimate
species
for
the
size
of
The
but
first,
I at
class
recruitment
of
the mean
to the study reef,
corals
juvenile
class
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that
second
with
a
the
rate
of
to
4
is ~20-fold
recruitment
as determined
nearby
of corals
the number
augmented
of a near-stable
the formation
I, with
at
initial
value
?52%
after ?30
of
the
density
Recruitment
for
potential
decline
size
years.
from
areas.
in
size
class
Size
I
A) No
600
11
POPULATION DYNAMICS OF MONTASTRAEA
2007
February
recruitment
recruitment
B) Steady
recruitment
C) Episodic
4 colonies-rrr2-(5
20 coloniesnrr2-(5
yr)~1
yr)_1
of
Fig. 6. Fifty-year
annularis, under three scenarios
by size class (I-IV; Appendix
C) for Montastraea
population
projections
at 4 coloniesm~2(5
shown in Fig. 5), (B) steady recruitment
recruitment:
(the same projection
(A) no recruitment
yr)_1, and (C)
are based on an initial population
vector determined
from the
at 20 coloniesm~2(25
recruitment
episodic
yr)_1. Projections
in five-year
structure in 25 m2 of the study reef in 2003 (described
in Fig. 5), and trajectories were calculated
increments
population
added to size class I at each iteration.
for 1998-2003 with recruitment
(where appropriate)
using the transition matrix
a near-stable
II reached
class
initial
density.
failed
however,
at ?13%
density
recruitment
Steady
to return
a
at
of
the
rate,
high
of the
the population
density
III and
to the
class
levels
(size
IV)
or the start of the
start of the third interval
largest
colonies
marking
the
study (1988). The third projection was
identical to the
that
first,
except
number
of recruits
added
I after
(20 coralsm~2(25
yr)_1)
was
This
level of recruitment
25 years.
a
a
career
working
of marine
as
important
researchers
it allows
not
have
to
corals
size
of
colonies
Following
episodic
declined
size
population
size
high
rapidly
classes
at
(Fig.
projection
are that (a)
projections
annularis
in 2003) of M.
imminent
prevent
colonies
population
transition
collapse
the collapse
that were
structure.
probabilities
is
that
of
this
recruit
Episodic
of
large numbers
and
III,
the
of
the
on
effect
II,
recruitment,
to <3%
(510 colonies)
6). The notable
2002)
the
scale
possibility
recruitment
infrequently.
in
of
the
high
to
selected
time
year added
transiently
class
I, but had a negligible
number
density
recorded
it occurs
because
species
ment
in the 25th
This
ecologists.
a test of
large
class
to size
of this species
(Edmunds
putative
masting
with
time
scale
the
length
compatible
mimic
on
recruitment
episodic
end
of
outcomes
of
replace
the
size
class
III and
IV
of the 1988
components
important
in the
This
will
require
changes
the fate of established
describing
Discussion
Globally
declining
et
Bellwood
anthropogenic
corals
actinian
meier
et al.
coral
al.
disturbances
2004)
(Brown
have
abundances
2004)
that
continue
revealed
large
and
continue
1997, Knowlton
occurred
against
(Gardner
a
diversity
to kill
et al.
of
scler
Budde
2001,
a backdrop
of
that
result
of
and
was
analysis
to determine
stabilized
at
analysis
the
and
revealed
a
how
the
and
The
in coral
cover
was
rather
than
decline
high
mortality
by
accompanied
in the abundance
reduction
accentuated
even
end
of
the
1988
cover,
Hurricane
with
and
the demographic
but
of population
decline
at
change
(p) continued
the
2003,
rapid
occurring
and Witman
and
warm
of unusually
The
trend
of
2004).
(Edmunds
of
representative
al.
1991,
Rogers
unpublished
cover has
data),
occurred
other
and
lost
reef
study
in 1995
sites
Miller
{X)
the
over
statistically
was
there
(i.e.,
declines
Hugo
(Edmunds
and between
1994
hurricanes
density
cover
had
rate
overall
Between
(affecting
level,
the
of
tempo
same pace
(i.e., X and p did not vary
even
and perhaps
accelerated
years),
trend for X and p to increase).
coral
low
a disproportion
of big colonies
by fission
the population
coral
study,
while
reduced
that
15-year
has
species
changed
to change
in the near
future.
the
that was
cm2)
of the colonies),
52%. By the
declined
al. 1991)
by two serious
a year
(1998)
colonies.
2003,
population
it might
how
(>250
>9%
50-year
these three
a demographic
was
designed
structure
of this
for
a
largely
recruitment
al.
provided
of Montastraea
that
analysis
a
et al. 2004).
In the present
study,
cover
on one
reef in St. John
context
ately
the present-day
population
(i.e.,
in Great
is facing
Lameshur
Bay
cannot
alone
and
(b) recruitment
or
the
et
Bellwood
2003,
coral
annularis
the
the
of
al.
are
to ask which
corals
beginning
their populations
this onslaught
and how
et al. 2003,
2002,
(McClanahan
Hughes
change
Buddemeier
record
et
Gardner
2001,
scientists
will
IV.
population
the
starting
exploitation
state
in a pristine
then, the prognosis
surprisingly
(Knowlton
that
2004)
will
survive
has left
that, arguably,
et al. 2001). Not
(Jackson
for coral
reefs is so poor
human
century-scale
no coral reef
1999,
72%
15
a
of
its
in 1989 due
to
et
1991, Rogers
a period
marked
et al. 1997) and
(Smith
seawater
temperatures
cover
coral
is
declining
around
2006;
St.
John
P.
J.
a slight
increase
although
over a similar
on at
period
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All use subject to JSTOR Terms and Conditions
et
(Rogers
Edmunds,
in coral
least
one
12
PETER
J. EDMUNDS
reef <1
km from Yawzi
Point
(Edmunds
2002).
reflect
the biases
may
discrepancies
are
when
not
sites
chosen
develop
study
but in the case of
1992, Lewis
(Hughes
2004),
in St. John,
it is important
that the dissimilar
In part,
can
such
cover
coral
changing
at
occurred
two
that
trends
of
both chosen in 1987 based on high coral cover (>32%)
(Edmunds
that
the
entirely
This
also
15-year
of the
The
2002).
illustrate
trajectories
were
not
constrained
contrasting
community
dynamics
initial
condition
by their
was
true within
decline
in coral
(sensu Hughes
1992).
a site, for at Yawzi
the
Point,
cover was more
two
rapid along
cover
where
coral
declined
from
transects,
35-45%
in 1988 to 3-6%
in 2003,
to the third,
compared
cover
coral
where
from
50% in 1988 to 27% in
declined
2003
J. Edmunds,
(P.
It is unknown
unpublished
data).
are
small-scale
patterns
biologically
within
of
the framework
interpreted
these
when
significant
region-wide
some
that
of
majority
further.
et al. 2003),
but signs
(Gardner
are doing
reef
than
the
better
is cause
to study
such patterns
enough
reef
decline
areas
of
reefs
placed
Yawzi
Point
is equivalent
Jamaica
from
reported
the Caribbean
(Gardner
the
context,
to
the
losses
of
that
have
and
1994)
(Hughes
et al.
loss
at
coral
been
this site in St.
?
12% during
coral
John,
cover
at
stabilized
apparently
recent
the most
interval.
five-year
This
that were
(1998-2000)
et al.
of Gardner
into
the meta-analysis
incorporated
in
to
and
their
conclusion
that
contributed,
part,
(2003)
cover
the rate
of
loss of coral
has
slowed
recently
interval
included
but
significantly,
and
2002)
3.3%
(from
by preventing
too far apart
coral
linear
cover,
could
years
St.
be
the
John,
death
of M.
it
reduced
because
important
it also
vacant
created
by macroalgae
preempted
Edmunds
five
In
region.
was
colonies
cover,
of fusion
years
the
throughout
annularis
that was
three
space
et al.
(Rogers
1997,
the frequency
depressed
probably
over
to 0.4% over
1988-1993
1998
contacts
conspecific
(i.e., colonies
to touch). After
11 years of declining
from
recent
the most
extrapolation
as
construed
for
support
"guarded
the
likelihood
of further
coral
optimism"
concerning
et al. 2003). However,
losses
be
may
(Gardner
optimism
on
for this reef. Population
based
premature
projections
the dynamics
between
that
the
extirpated
There
coral
reported
2000).
of
colonies
the
and
conditions
1998 and 2003 demonstrate
local
within
are
strong
community
parallels
structure
for
previously
Notably,
of M.
population
50 years.
the
reefs
dominated
study periods
suffered
large losses of
the
between
in
Jamaica
in both
prevailing
the high likelihood
annularis
St.
John
(Hughes
locations
by Montastraea
coral on a decadal
will
be
in
changes
and
those
and
Tanner
started
annularis,
scale,
hurricane
as
population
the largest
size
over
the
time,
skewed
positively
are
also
there
However,
these studies,
that
namely
water
than
(9-m depth)
and the St. John
(35-m depth),
study
a decade
the Jamaican
initiated
after
study
began
it was
when
?50%
in
reductions
already
recording
the Jamaican
and
their
they
in part
displayed
deter
and
annularis,
became
structure
and Tanner
2000).
differences
between
important
reef is in shallower
the St. John
was
both
trajectories
More
demographic
analyses.
here for St. John,
in Jamaica,
the
most
to the mortality
sensitive
of
of M.
colonies
and
community
vs.
is reported
was
decline
population
Monographs
Vol. 77, No. 1
damage,
coral
cover
coral
by
just
reef
cover
coral
St.
and Tanner
(Hughes
reef
is
John
et
Mittelbach
set
al.
a
in
2000).
local-scale
that
2001)
the
Additionally,
context
(sensu
an
within
is protected
and is substantially
MPA
internationally-recognized
than many
degraded
less
in Jamaica
reefs
1994,
(Hughes
a
and Precht
this backdrop,
200\d).
Against
the
in both
of
dynamics
community
a poor prognosis
for other Caribbean
provides
Aronson
comparison
locations
are
annularis
of M.
populations
in this context
is the observation
large
Most
important
"Jamaican-like"
did
not
occurring
underwater
in
reef
throughout
~
is
1.4-fold
it
2003);
on parts
than the ~50%
loss that has occurred
of
higher
et al. 2004). While
the Great
Barrier
Reef
(Bellwood
1988 and
of coral
died between
1999 at
large amounts
2003)
were
of
between
reefs where
in a global
When
coral
result
(Hughes
three
whether
a
Ecological
ELAHI
disconnects
over,
were
that
as
ROBIN
mined
randomly
our work
sites
AND
with
on
a
that
the St.
of
(Hughes
1994)
collapse
occur
contemporaneously
at
least
based
Jamaica,
found.
John
that
anecdotal
from
St.
John
that were
taken
pictures
1970s
loaned
early
by C. Birke
(generously
in Lee et al. 1975), but instead
45-48
land; see also Figs.
a decade
it began
later with
Hurricane
nearly
Hugo
the
during
(Fig. 1).
the causal
Although
identical
in
Edmunds
most
of
appears,
the
a "patch"
1980s,
of reef
John
outcome
the
2002),
cover
coral
with
to have
broadly,
the study
that
reef decline
of
processes
and
St.
Jamaica
been
in St.
reef
John
not
1994,
overall
similar.
For
represented
in condition
differed
apparently
were
(Hughes
to
regard
the north
reef along
of apparently
healthy
patches
at various
reef still occur
coral
scales
spatial
throughout
at the Dairy
Bull
site
in
the Caribbean,
for example
et
Bruno
al.
Jamaica
and
1996, Idjadi
2006)
(Edmunds
the
reef in St. John
and at the Tektite
(Edmunds
2002),
compared
coast
of
to
the
Jamaica.
larger
While
that
present
suggests
study
on
at different
points
reef
condition
disturbance
trajectory.
tions on
method
the
and may
histories
Demographic
such "healthy
to
test
are
this
of
patch
be located
may
patches
of
downward
trajectory
in their
from one another
such
same
differ
that
them
propel
of
analyses
the
patches"
provide
hypothesis
the same
explicitly
this
along
coral
popula
one potential
that the
(i.e.,
at different
following
it is likely that
rates), although
to some extent,
be unique
will,
In St.
the mortality
John,
trajectories
the demographic
annularis
classes
patches
varied
differed
among
among
sample
of the larger
mortality
III and
for size classes
size
to each
colonies
IV) was
1988).
(Done
of Montastraea
rates
intervals,
patterns
reef
in a pattern
because
that
per five
between
years
1993
largely
(11-39%
reduced
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All use subject to JSTOR Terms and Conditions
the
and
least
Smaller
rates
ity
to
the other
sample
compared
colonies
(<150
cm2) had high mortal
The
in all three
intervals.
per year)
at
1998,
intervals.
(35-56%
rates of massive
mortality
greatly
corals
on
depending
and
size
regime,
DYNAMICS
POPULATION
2007
February
in other
class
studies
projection
annularis
outcome
1991,
et al. 2000, Hughes
Bythell
2000). Mortality
rates as low as < 1% per year have been
for M.
reported
as
as
et
annularis
for
and
90%
al.
2000)
(Bythell
high
cm diameter)
small
colonies
of massive
Porites
(<30
to
exposed
censuses
Acanthaster
6-7
completed
1988).
Typically,
Babcock
instance,
on
pr?dation
(based
Done
after
the outbreak;
planci
years
declines
mortality
found
(1991)
Goniastrea
for
size;
colonies
with
small
that
on the Great
Barrier
?spera
32% per year, while
larger colonies
at a rate
died
5% per
In the
of
year.
(>120
cm2)
Jamaican
annularis
and Tanner
study of M.
by Hughes
cm2) of
died at a rate of
(<40
Reef
(2000),
rates
mortality
(per five
years)
1977
between
and
1982 ranged from 43% to 3% for the smallest (<50 cm2)
to largest
1987 and
to 86%
(>200
1993,
and
colonies,
rates had
cm2)
these
38%,
but
respectively,
accelerated
between
dramatically
by
conferring
of disturbance
growth
rapid
resilience
(the
and
rate
recruitment,
of
regrowth)
Rodenhouse
is accentuated
of M.
years
by the >100
required
to grow
at a typical
rate of
annularis
in the
colony
and a height
of
size
largest
?
1m
class
(with
[P. J. Edmunds,
an
1-1.5
1985) into a
and Jackson
1981, Hughes
cm/yr (Hudson
a
for
area
>250
unpublished
cm2
and the high chance (>17% per five years) that itwill die
in
this
size
affects
massive
1987,
1988).
class.
A
similar
on
Porites
Given
the
demographic
the Great
Barrier
of
plethora
there
is clearly
inequality
Reef
(Done
are
events
that
an
corals,
currently
killing
to evaluate
need
the ecological
significance
a demographic
context.
death within
of
The
projected
collapse
Montastraea
annularis
effectively
the paucity
0. The
Caribbean
and
(Bak
for instance,
including,
Hughes
annularis
and
of
the
study
that
assumes
rationale
for
this
important
of coral
of
population
recruitment
assumption
is
lies
in
of this species
the
throughout
et al.
1979, Rogers
Engel
1984)
at 35-m depth
in Jamaica
where
found
of M.
(2000)
only one recruit
recruits
Tanner
16 years
of annual
of 12 m2 of
surveys
during
reef. In the present
recruitment
of
study, we estimated
M.
annularis
from
in
reefs,
yet even
adjacent
fringing
areas where
to detect
these
it is relatively
small
easy
corals
(Edmunds
2000),
we
have
rarely
encountered
the
of M.
recruitment
et
nature
open
with
organisms
for manipulation
coral populations
2000,
would
of
would
be loosely
only
recruitment
Nevertheless,
link with
a
have
1988).
Caribbean
the brooding
coral,
the stock-recruitment
an
at
coral
in
al.
recruitment
population
one weedy
least
Porites
astreoides,
to
appears
relationship
et
1984,
(Hughes
commensurate
varying
on
effect
For
al.
the
et
(Caley
inevitable
defined
has
with
developed,
et
of
relationship
scale
trickle-down
1987,
(Done
marine
(Levitan
size
population
demographic
on a time
Caswell
therefore,
2001);
with
the lifespan
of coral
colonies,
should
Given
(Caley
members
the broadcasting
spawning
annularis
species
complex
it is likely that any stock-recruitment
species
size
population
like
1996),
Montastraea
1996).
1988, Caley
and Morse
larvae
pelagic
to
controlled
relationship.
of most
populations
dispersive
are
increase
in
to
approach.
in order
1987,
(Done
Raimondi
al.
this
contributing
two
tested
we
collapse,
a projection
if elevated,
of a stock-recruitment
2000), which,
as a function
be well
to
sensitive
population
growth
being
rates
of
recruitment
(Lirman
and
Miller
2003).
For
like massive
corals,
long-lived
and Montastraea
Barrier
Reef
Great
on
Porites
annularis
the
the
in
recruitment
is intriguing
theoreti
Caribbean,
because,
need produce
cally, a colony
living for centuries
only one
recruit
to sustain
its lifespan
the population
size.
during
This
data]),
that
the hypothesis
to some
extent
by
et al.
1996, Hughes
changes
found
population
the factors
explore
selected
test
structure
and
In the
(Andres
1993).
rates of the larger colonies
the mortality
present
study,
were
to the slow
rate at which
relative
smaller
high
colonies
transitioned
into
these
size
(i.e., grew)
larger
a
classes
five
per
(<11%
years),
thereby
creating
The
of
this
in
demographic
inequality.
significance
equality
recruit
was
Recruitment
rates
thereby
to the effects
to further
population
projected
recruitment
scenarios
using
al.
respectively.
have
recruitment,
50 years,
within
will
with
disappear
unaffected
altered
slightly
being
(although
the use of different
matrices
corresponding
confidence
intervals
for X.
the
the
that we
those
Without
0.04/m2.
that
the 2003
only
revealed
a means
As
to
2004),
for this
the biological
of high mortality
However,
significance
on
rates
to
the demographic
process
depends
acting
can be
the colonies.
The effects
of coral mortality
replace
offset
rate) by
the 95%
with
annularis,
to
amounting
vary
Babcock
1988,
(Done
and Tanner
of M.
juveniles
disturbance
location,
species,
13
OF MONTASTRAEA
assertion
of recruitment
and
massive
et
Hughes
annularis,
common
to be consistent
with
the low rates
appears
of both M.
annularis
discussed
previously
Porites
and
Johnson
1998,
(Dunstan
al.
to M.
in contrast
1999);
although
colonies
juvenile
on Pacific
of
massive
are
Porites
reefs
A
(Done
1987).
life-history
a
with
rare
adult
but
strategy
large
population
has
been
as
recruitment
in a general
described
form
a population
the
of
old
effect,
storage
whereby
individuals
a
event
recruitment
In what
non,
may
sexual
Populus
Mountains
time
scale
"windows
corals
(e.g., many
recruitment
historic
be
occurs
an
certain
trees)
another
until
(Warner
extreme
recruitment
tremuloides
and
signal
and
Chesson
of
example
the common
of
this
"stores"
episodic
1985).
phenome
tree
native
in the Rocky
aspen)
on a
to occur
is thought
to thousands
rare
of hundreds
of years during
of
et al.
(Romme
opportunity"
2005).
Unfortunately,
of a storage
of North
(quaking
America
it is difficult
effect
because
to demonstrate
the
This content downloaded from 130.166.34.124 on Thu, 07 May 2015 19:17:37 UTC
All use subject to JSTOR Terms and Conditions
passage
the existence
of
years
or
14
PETER
decades
to
without
the
recruitment
that
occur.
not
does
the
annularis,
sexual
significant
conclusion
incorrect
available
J. EDMUNDS
contain
are
summer
late
et
al.
to early
Levitan
1997,
fall
et
in
results
rates
et al. 2004).
fertilization
relatively
(Levitan
high
Successful
recruitment,
poor
yet
by
reproduction,
the consequence
Montastraea
of
annularis
could
reflect
processes
multiple
and
Roughgarden
influencing
and
1985)
and
(Gosselin
these possibilities
Qian
available
However,
the
mediating
likelihood
on
a
scale
further
comes
at
from
years
products
annularis
(i.e.,
are
1989).
evidence
(Fairbanks
cores
contain
of M.
populations
time scale as
long as
asexual
the
Because
1989,
the
of M.
of populations
the
of
(Fairbanks
which
reveals
of
centuries
three
support
offshore
Empirical
cores
taken
stratigraphy
reestablishment
least
the
is ecologically
significant
to centuries
of decades
(or
independent
temporally
on a
that are separated
annularis
?
10000
1989).
or small
of M.
lobes)
fragments
to disperse
too
large
generally
heavy
see Edmunds
the
and Witman
1991),
(but
of M.
annularis
reestablishment
populations
distances
periodic
is
that
(Fairbanks
colony
cores
the Barbados
by
(Fairbanks
If
sexual
recruitment.
occurred
through
events
is correct,
then the large recruitment
suggested
1989) probably
this assertion
of M.
the mechanism(s)
of M.
annularis,
Barbados
of
and
disappearance
annularis
within
several
Moreover,
of multiple,
of
attention.
rock
the
1992),
result
time
among
of the
distinguishing
the scope
beyond
regardless
success
end
the
warrants
longer)
this possibility
for
the reef
through
Jackson
but
1997),
recruitment
that
recruitment
post-settlement
is currently
data.
(Gaines
events
pre-settlement
annularis
in Barbados
occur
indeed
did
at
such
events
intervals
(i.e., with
by at
separated
infrequent
in the 20th
occurred
least
had
that,
centuries)
they
have
detection
would
avoided
century,
by
easily
our work
in St. John,
From
it is clear
that
ecologists.
of M.
recruits
annularis
we
and
numbers,
have
are
available
used
DNA
to demonstrate
techniques
on
colonies
of M.
annularis
(P. J. Edmunds,
of
products
distinct
are
at
that
the
study
at
very
low
fingerprinting
10 nearby
least
reef are genetically
data)
unpublished
recruitment.
sexual
and
therefore
sexual
Thus,
occurs
in the study
magnitude
at some
scale.
It
of M.
annularis
temporal
populations
was our intention
to explore
further
this possibility
using
the
recruitment
of unknown
additional
The
first
one
aspect
recruitment
tested
projection
elevated
recruitment
recorded
projections
population
scenarios.
recruitment
on
of
the
27-fold
shallow
the storage
and
[Warner
the
effect
above
the
and
the
reefs,
effect hypothesis
Chesson
differing
employing
1985])
of
yearly
we
density
second
tested
(episodic
by
high
elevating
above
100-fold
it once
applying
Monographs
Vol. 77, No. 1
that
in shallow
recorded
over
25 years. However,
neither
of
these
scenarios
after
structure
of either
characteristic
2003 (the start of the projection) or 1988 (the start of this
Szmant
1997,
which
>
recruitment
and
Ecological
ELAHI
the
50-year
projections,
restored
the population
that
1991)
event
in the
et al.
(Knowlton
al.
2004),
ROBIN
water
populations
sub
allocates
this
recruits,
yet
species
resources
to reproduction
(Szmant
in an annual
released
mass-spawning
rarely
stantial
lead
meaningful
for M.
Interestingly,
indicate
that
data
can
recruitment
biologically
AND
Stable
recruitment
study).
a population
but created
and
(<50
episodic,
cm2),
transient
of
pulse
prevented
dominated
collapse
colonies
recruitment
high
colonies
small
population
by small
a
created
did
but
not
prevent
illus
outcomes
Both
collapse.
population
of the transition
that
influence
matrix
strong
was
used
in the projections
C), or in other
(Appendix
was
structure
the projected
words,
relatively
population
subsequent
trate
the
to
insensitive
of
fate
recruitment,
affected
yet strongly
This
conclusion
colonies.
existing
was
the
by
supported
that
which
demonstrated
analyses,
elasticity
of colonies
to the proportion
sensitive
remaining
interval.
for the duration
of each
size classes
specific
the
by
was
the
and
1988-1993
in size class
remaining
between
1993
and
IV had
class
measure
indirect
1998-2003
the
intervals,
X
in
For
colonies
effect on X, but
the greatest
in size
colonies
remaining
on X. Because
X is an
influence
II had
the
1998,
the greatest
of fitness
and Peckarsky
1998,
(McPeek
can be used
to indicate
elasticities
1999),
high
that are under
the strongest
of the life cycle
portions
be best
and which
selective
pressure,
by
targeted
might
Ebert
resource
these
portions
cm2 and
(51-150
and
Jamaica
(Hughes
of coral
The dominance
the Class
>250
cm2)
and
Tanner
(i.e.,
population
is a common
skewing)
to environmental
positive
populations
1998, Done
interpreted
stage
(Done
annularis,
can also
1999). For
trend with
a
their
(i.e.,
colonies
of
coral
and Glynn
which
has
2000),
earlier
successional
like Montastraea
size
colony
of asexual
advantages
crowded
of a habitat
decreasing
the demographic
the constraints
within
coral
IV
John
colonies
small
(Fong
species
for
St.
by
to an
reflect
proliferation
with
conspecific
some
contrast,
mental
time
Class
in both
response
Tanner
massive
population
For M.
2001).
II and
2000).
assaults
and
1999, Hughes
as a skewing
been
of
purpose
Caswell
1999,
are
(Ebert
annularis,
colonies
the
for
managers
conservation
and
(Lasker
Sanchez
respond
populations
to
In
2002).
environ
is with
that
the opposite
direction,
structure
skewed
negatively
becoming
habitats
in disturbed
by big colonies)
in
assaults
population
dominated
or when
et al. 2001)
1999, Meesters
(Bak and Meesters
and Rodenhouse
is accelerated
1993),
(Andres
growth
as by
to rising
seawater
such
exposure
temperature
reasons
for
and Glynn
2000, Edmunds
2005). The
(Fong
but it is likely that the
trends are unclear,
these opposing
to new distur
the response
disturbance
affects
history
with
distur
bances
and Glynn
varying
2000),
(Fong
distinct
and disturbance
bance
histories
types
creating
An
structure.
in coral population
and dissimilar
signals
acute
small
larger
and more
Rogers
caused
disturbance
destroy
1993);
and
robust
for
by
delicate
colonies
branching
a
severe
storm
but
corals,
(Massel
corals,
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All use subject to JSTOR Terms and Conditions
will
to
is likely
behind
leave
and Done
negative
skewing
1993,
of
2007
February
POPULATION
can
structure
the population
of
effects
temperature
rising
(Edmunds
could
Bak
2005).
from
data
empirical
to suggest
stimulatory
calcification
from
Florida
pattern
(i.e., negative
skewing)
effects
of deteriorating
conditions
and recruitment
(see also Lirman
patterns
positive
annularis
skewing
under
of
the
adverse
as
and previously
described
here,
reported
for Jamaica
and Tanner
reflect
the
2000), might
(Hughes
effects
of chronic
caused
mortality
by disease,
physio
or algal
in reducing
stress,
overgrowth
colony
logical
conditions,
the
and fission.
Given
partial
mortality
to
structure
of
coral
responses
population
the likelihood
that coral populations
and
disturbances,
will be affected
both
by events
favoring
simultaneously
an
and negative
research
positive
skewing,
important
sizes
through
differing
goal must
of coral
conditions
to understand
be
of
Regardless
size structure
has
positive
how
the demographic
abiotic
and
with
interact
populations
to shape
traits
of coral
causes,
skewing
In particular,
important
implications.
has
for sexual
implications
important
skewing
because
reproduction,
to colony
size
tively
coral
is related
fecundity
posi
and Hughes
1977, Hall
(Jackson
at a finite
is typically
attained
maturity
a potentially
Szmant
with
1991,
1991),
and
sexual
1996),
size
(Soong
interactive
effect
in mean
reduction
level
fecundity,
structure
may
a
and Quinn
(Kojis
1985). Thus,
the
size
will
lower
colony
population
a positive
and
of
the
size
skewing
result
in the majority
of
colonies
of age
to a sexually
In the
immature
size class.
belonging
at ?100
is achieved
of M.
sexual maturity
annularis,
1991), and
(Szmant
therefore by 2003,
41%
the
functionally
probably
in 1988,
I). In contrast,
that
classes
(>50
cm2)
in the
and 7% were
individuals,
sexually mature
fecund
category
(i.e., >250
to what
it is unknown
Although
included
cm2; cf. 3% in 2003).
extent M.
annularis
most
are
self-replenishing
et al. 2000),
and
are affected
populations
populations
1991, Cowen
local
success,
reduction
probably
Black
(sensu
to what
therefore
by
in
local
depress
a potential
thereby
creating
rates of population
decline.
the present
While
analyses
positive
et
al.
extent
reproductive
will
fecundity
population-level
rates at some spatial
recruitment
feedback
scale,
on
loop
Some
of
events
these
example,
1989 (Edmunds
while
other
of
episode
out to have
and Witman
conspicuous
1987
(Roberts
surprisingly
are
for
unambiguous,
in
Hurricane
by
Hugo
et al. 1991),
1991, Rogers
like
the bleaching
events,
caused
the destruction
of
St.
have
as
John,
played
have
important
elsewhere
they
seen
of M.
examples
killed
annularis
colonies
that
had
were
the
skeletons
stark
(i.e.,
as a result
II Disease
of Plague
possibly
Type
land et al. 2004),
which
has been
colonies
killing
recently
been
white),
(Suther
of M.
on the nearby
et al. 2003).
annularis
Tektite
Reef
(Miller
we often
have
found macroalgae,
mostly
Additionally,
ta spp. and Halimeda
and
with,
Dietyo
spp., competing
can
annularis
in interactions
that
over, M.
growing
to
contribute
et
McCook
water,
temperatures
there
is clearly
declining
to determine
reefs
For
have
large-scale
et
meier
tissue
including
2004)
of
phenomena
roles
strongly
of
of
investigations
by the goal
of
in
Karlson
1978,
is
it
each
disturbances
major
(Connell
most
organization
yet
of
populations,
relative
importance
ecological
abiotic
warming
and
turbid
coral
the
2001,
(Lirman
adverse
with
(Edmunds
a plethora
influenced
the
community
Hurd
1993,
and
on
recently
focusing
Budde
(Fitt et al. 2001,
episodes
Now
is an urgent
need
for
there
to elucidate
studies
the effects
of
designed
Rogers
1993),
bleaching
al. 2004).
demographic
will
coral
decades,
been
understanding
chronic,
on coral
of
to
impossible
of these factors.
coral
death
2001).
Together
the
reef,
study
on
conditions
seawater
the
al.
cumulative,
change
populations
in the
and
subtle
potentially
in order
to understand
disturbances
how
reefs
centuries.
coming
Acknowledgments
Over
the years, this research has been funded from multiple
but
the most
consistent
has come
from
sources,
support
California
State University,
and the Virgin
Islands
Northridge,
National
Park. The demographic
analysis of the long-term data
described
here was
supported
by grants from the Sea Grant
of the University
of Puerto Rico
and
Program
(#R-101-2-02)
the National
Science Foundation
thank R.
(DEB 0343570). We
our research
and C. Rogers
Boulon
for supporting
in St. John
two decades
for nearly
and
the Virgin
Islands
Ecological
our visits.
P. J. Edmunds
Resource
Station
for hosting
thanks his graduate
students
for assisting
with
particularly
S. Prosterman
for providing
scuba facilities,
and V.
fieldwork,
an
Powell
for on-site
from
Comments
support.
logistical
an earlier draft of this paper.
reviewer
anonymous
improved
This
is contribution
number
130 of the CSUN
Marine
Biology
Program.
into the
provide
insights
a population
of Mon
processes
causing
demographic
tastraea
to decline,
it provides
annularis
little informa
events
the success
of
tion on the proximal
determining
colonies.
reefs
cm2
70% of
on the study
reef were
in size class
(i.e., they were
were
in size
of the colonies
colonies
sterile
case
events
destructive
the
contributing
the proximal
15
and Hurd
of the
1993, Rogers
(Karlson
1993), but many
recent
to be
the study
reef appear
phenomena
affecting
or complete
or
events
chronic
causing
partial
mortality,
over
we
For
the
have
years
impaired
growth.
example,
biotic
structure.
the population
OF MONTASTRAEA
Infrequent
roles on
used
(1999)
and
Cura?ao
In contrast,
2003).
structure
of M.
population
the
coral
and Meesters
both
the
from
on mortality
and Miller
from
on
a similar
that
result
result
DYNAMICS
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1987, Glynn
1993),
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2002).
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APPENDIX A
the location of the study
showing
Map
Archives M077-001-A1).
(Ecological
site (18?18.910'
N,
64?43.501'
W)
on
the south
coast
of St. John, U.S.
Virgin
Islands
APPENDIX B
Autocorrelation
positioned
John, U.S.
the results of statistical
plots displaying
along each of the three transect lines (Transects
Archives M077-001-A2).
Islands (Ecological
Virgin
tests for independence
10 of which
among contiguous
quadrats,
the core of the long-term
1-3) forming
study site off Yawzi Point,
are
St.
APPENDIX C
Transition
1993-1998,
matrices
and elasticity
analyses
and 1998-2003
at St. John, U.S.
for a population
Islands
Virgin
of Montastraea
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Archives M077-001-A3).
Point
(9-m depth)
for
1988-1993,
(Ecological
APPENDIX D
rate (X) and damping
growth
Population
Archives M077-001-A4).
(Ecological
ratios
(p) for Montastraea
annularis
at 9-m depth
in St. John, U.S.
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All use subject to JSTOR Terms and Conditions
Virgin
Islands