Download Does increased habitat complexity reduce predation and

OIKOS 106: 275 /284, 2004
Does increased habitat complexity reduce predation and competition
in coral reef fish assemblages?
Glenn R. Almany
Almany, G. R. 2004. Does increased habitat complexity reduce predation and
competition in coral reef fish assemblages?. / Oikos 106: 275 /284.
Greater habitat complexity is often associated with a greater abundance and diversity of
organisms. High complexity habitats may reduce predation and competition, thereby
allowing more individuals to occupy a given area. Using 16 spatially isolated reefs in
the Bahamas, I tested whether increased habitat complexity reduced the negative effects
of resident predators and competitors on recruitment and survival of a common
damselfish. Two levels of habitat complexity were cross-factored with the presence or
absence of two guilds of resident fishes: predators (sea basses and moray eels) and
interference competitors (large territorial damselfishes). I monitored subsequent
recruitment and recruit mortality for 60 days. Residents had strong negative effects
on recruitment regardless of habitat complexity. In the presence of residents, recruits
suffered high mortality immediately after settlement that was similar on low and high
complexity reefs, although high complexity reduced mortality of recruits that survived
this early postsettlement period. Comparisons between shelter hole diameters and the
sizes of residents suggest that territorial damselfishes and small resident predators
could access most shelter holes, whereas large resident predators were excluded from
many shelter holes. This study demonstrates that whether habitat complexity reduces
predation and competition may depend on several key factors, such as the availability
of appropriate shelter, behavioral attributes of interactors, and developmental stage of
prey/inferior competitors.
G. R. Almany, Dept of Zoology, Oregon State Univ., Corvallis, OR 97331-2914, USA.
Present address: School of Marine Biology and Aquaculture, James Cook Univ.,
Townsville QLD 4811, Australia ([email protected]).
Habitats with high structural complexity typically support more species and individuals than nearby less
complex habitats (Bell et al. 1991). One mechanism
proposed to explain this general pattern is that high
structural complexity reduces competition and predation
(Holt 1987, Hixon and Menge 1991). For example,
complex habitats may reduce competition when they
provide more competitive refuges or a greater spectrum
of discrete resources (e.g. food and shelter) and microhabitats, thereby allowing for enhanced niche partitioning (MacArthur and Levins 1964). Although these
mechanisms have typically been proposed to explain
positive relationships between local species diversity and
habitat complexity (Schoener 1968, Emmons 1980), an
implicit prediction is that abundance, pooled across
species, will also be greater in high complexity habitats.
Similarly, complex habitats may reduce predation by
providing more prey refuges and/or reducing encounter
rates between predators and prey (Murdoch and Oaten
1975). Predation risk is often lower in complex habitats
for a wide range of taxa (Schneider 1984, Dickman 1992,
Babbitt and Tanner 1998). Prey often increase their use
of high complexity habitats as refugia in the presence of
predators (Holbrook and Schmitt 1988, Sih et al. 1992),
and predators may be less efficient foragers in high
complexity habitats (Greenberg et al. 1995, Beukers and
Jones 1997). Despite the potential importance of habitat
complexity in mediating biotic interactions, few studies
Accepted 23 December 2003
Copyright # OIKOS 2004
ISSN 0030-1299
OIKOS 106:2 (2004)
275
have experimentally examined the combined impacts of
habitat complexity, predation and competition on local
assemblages.
Coral reefs are structurally heterogeneous environments consisting of many microhabitats, which vary in
their complexity depending on coral architecture (Jones
and Syms 1998). Several studies of coral reef fishes have
suggested that habitat complexity is a major determinant
of abundance. For example, abundance is often greater
in high complexity habitats (Hixon and Beets 1993,
McCormick 1994), positively related to the number of
potential shelter sites (Roberts and Ormond 1987,
Friedlander and Parrish 1998), and the availability of
suitably-sized shelter can influence both the abundance
and size distribution of fishes (Hixon and Beets 1989).
Furthermore, reef fish are known to compete for shelter
(Munday et al. 2001, Holbrook and Schmitt 2002).
These patterns illustrate the potential importance of
habitat complexity in coral reef fish communities,
although most studies have not identified causative
mechanisms.
Relationships between habitat complexity and abundance could also arise from several processes. For
example, positive relationships between the abundance
of newly settled fishes (recruits) and habitat complexity
(Tolimieri 1995, Caselle and Warner 1996) could be
caused by larvae selecting specific microhabitats as
settlement sites, although the unequivocal demonstration of active habitat selection by settling larvae is rare
(Elliot et al. 1995, Danilowicz 1996). Relationships
between habitat complexity and recruit abundance could
also arise from postsettlement movement (Frederick
1997, Lewis 1997) and when recruit mortality is influenced by habitat complexity (Jones 1988). Because
experimentally separating the effects of these various
processes has been difficult, we currently know little
about the underlying causes of relationships between
abundance and habitat complexity.
Patterns of abundance can also be influenced by
predation and competition in ways that are independent
of habitat complexity. For example, the presence of
sedentary reef-associated (resident) predators typically
results in lower recruit abundance of most species,
presumably because newly settled fishes are especially
vulnerable to predation (Webster 2002, Almany 2003).
Furthermore, predation by widely-ranging non-resident
(transient) predators, such as jacks and snappers, can
reduce recruit abundance (Hixon and Carr 1997). Prior
residency by interference competitors, such as territorial
damselfishes, can result in both positive and negative
effects on recruit abundance. For example, damselfishes
have been shown to either depress (Shulman et al. 1983,
Jones 1987, Almany 2003) or enhance (Almany 2003)
heterospecific recruit abundance, and either depress
(Sale 1976, Almany 2003) or enhance (Jones 1987,
Booth 1992) conspecific recruit abundance. However,
276
the extent to which predation and competition are
influenced by habitat complexity is not well understood.
In the only previous study to manipulate both predation
and habitat complexity, Beukers and Jones (1997) found
that juvenile damselfishes suffered lower mortality on
high complexity coral.
In a previous study, I demonstrated that prior
residency by predators and territorial damselfishes
negatively affected subsequent damselfish recruitment,
and that effects were due to direct interactions between
recruits and residents rather than differential settlement
(Almany 2003). In the present study, conducted in the
same system, I tested whether effects of predators and
damselfishes differed on reefs of relatively low and high
habitat complexity and explored underlying mechanisms.
I predicted that (1) recruitment would be greatest on
high complexity reefs free of predators and damselfishes
and lowest on low complexity reefs where these fishes
were present, (2) where predators and damselfishes were
present, recruitment would be greater on high complexity reefs, and (3) where predators and damselfishes were
present, recruit mortality would be greater on low
complexity reefs.
Methods
Study site
This study was conducted near the Caribbean Marine
Research Center at Lee Stocking Island, Bahamas (Fig.
1A). I utilized a matrix of live-coral patch reefs that were
translocated to a large sand/seagrass flat on the leeward
side of Norman’s Pond Cay between 1991 and 1994
(Carr and Hixon 1995). The matrix included 32 reefs in
five rows, and water depth varied between 2 and 5 m.
Reefs were separated by 200 m of sand and seagrass, and
the closest naturally occurring reef was /1 km from the
edge of the matrix (Fig. 1B). Prior to habitat manipulations, each reef consisted of 9 /13 coral heads (mean /
10.8, SD /1.5) of primarily three species: Montastrea
annularis (Ellis & Solander), Porites asteroids (Pallas)
and Siderastrea siderea (Ellis & Solander). Each reef had
a surface area of 6.6 m2 (SD /1.0 m2) and height of
0.5 m (SD /0.07 m). A tagging study demonstrated that
resident fishes seldom moved between reefs, although
transient predators, such as jacks (Caranx spp.), snappers (Lutjanus spp.) and barracuda (Sphyraena barracuda Walbaum) did so (M. A. Hixon, pers. comm.). I
assumed that each newly settled recruit arrived via
natural settlement, and that the disappearance of a
recruit was due to mortality rather than postsettlement
movement for two reasons: (1) there is no evidence that
newly settled recruits re-enter the plankton after their
first day on the reef (Kaufman et al. 1992, Holbrook and
Schmitt 1997) and (2) small reef fishes rarely move
OIKOS 106:2 (2004)
Fig. 1. Study site. (A) Position of translocated patch reefs with
respect to nearby islands. (B) Spatial arrangement of reefs and
the blocking scheme of live-coral reefs used in both experiments.
Reefs were separated by 200 meters of sand and seagrass.
growth and mortality was unrelated to microhabitat
(B. A. Byrne, unpubl.). Juvenile beaugregory feed
primarily on benthic invertebrates (Wellington 1992),
and are consumed by both resident and transient
predatory fishes (Emery 1973).
Prior residents consisted of two guilds of fishes:
predators and interference competitors. Resident predators had two defining characteristics: (1) a diet of
]/10% fishes by volume (Randall 1967) and (2) a strong
tendency to retreat to the reef (as opposed to fleeing the
reef) when approached by a diver. Resident predators
consisted of seven species: four diurnally active sea
basses (Cephalopholis cruentata Lacepède [graysby], C.
fulva L. [coney], Epinephelus striatus Bloch [Nassau] and
Serranus tigrinus Bloch [harlequin bass]), one nocturnally active sea bass (Rypticus bistrispinus Mitchill
[freckled soapfish]), and two nocturnally active moray
eels (Gymnothorax moringa Cuvier [spotted] and G.
vicinus Castelnau [purplemouth]). Interference competitors consisted of adults of the study species, Stegastes
leucostictus, and the bicolor damselfish, S. partitus
(Poey). Both species defend exclusive-use, single-owner,
general-purpose territories against conspecifics, congeners, and most other fishes (Itzkowitz 1977, Gronell
1980, Robertson 1996). Adult Stegastes leucostictus are
omnivorous, consuming algae, detritus, polychaetes, and
fish material, whereas adult S. partitus are primarily
planktivorous (Randall 1967, Emery 1973).
Experimental design
between reefs separated by as little as 30 meters
(Doherty 1982, Hixon and Beets 1989).
Study species
I tested whether increased habitat complexity reduced
negative effects of residents on recruitment and mortality of the beaugregory damselfish (Stegastes leucostictus
Müller & Troschel). The beaugregory is found throughout the western Atlantic from Brazil to the southern
United States (Allen 1991) and is the most abundant
damselfish on the shallow (B/6 m) reefs surrounding Lee
Stocking Island (pers. obs.). After approximately one
month of pelagic development (Robertson et al. 1993),
larvae settle to and occupy a wide range of benthic
microhabitats, including live and dead coral, coral
rubble, sponges, mangrove roots, and empty mollusk
shells (Longley and Hilderbrand 1941, Emery 1973,
Itzkowitz 1977). In both laboratory and field choice
experiments, beaugregory recruits did not show a preference for particular coral species or coral morphology,
and in the absence of resident predators in the field,
OIKOS 106:2 (2004)
To test whether habitat complexity modifies the negative
effects of prior residents on recruitment and mortality of
Stegastes leucostictus, I conducted an experiment on 16
of the 32 patch reefs during the 1999 summer settlement
season. I selected the 16 reefs with the most similar fish
communities prior to manipulations based on Cluster
Analysis (Bray /Curtis distance and group average). I
then randomly assigned reefs to one of two habitat
complexity treatments, high or low. On the eight high
complexity reefs, I replaced half of the existing coral
heads with an equal volume of Agaricia tenuifolia
(Dana), a highly-branched foliaceous coral. On the eight
low complexity reefs, I replaced half of the existing coral
heads with an equal volume of low complexity massive
coral of the same three species originally present on
reefs: M. annularis, P. asteroides and S. siderea . After
habitat manipulations, I estimated each reef’s volume as
a cylinder. To obtain quantitative measures of complexity, I established two perpendicular, 1.5-cm wide transects across each reef. Along the length and directly under
each transect, I measured: (1) topographic complexity,
defined as the ratio between the length of a fine-link
chain allowed to conform to coral topography along the
transect and the straight-line length of the transect
277
(Risk 1972), (2) depth of each potential shelter hole, (3)
diameter of each hole, and (4) number of holes (Roberts
and Ormond 1987). I averaged data from the two
transects to obtain a reef average for complexity
measures 1 /3, and estimated the total number of
potential shelter holes on each reef by summing hole
counts from the two transects.
Forty days after habitat manipulations, I crossfactored habitat complexity treatments (high or low)
with the presence and absence of predators and territorial damselfishes (both guilds present or both guilds
absent). I selected four blocks of reefs, each block
containing four reefs (two high complexity and two
low complexity), using two criteria: (1) reefs within each
block had similar fish communities prior to the start of
the experiment, thereby minimizing potential confounding effects of variable species composition, and (2) reefs
within each block were close to each other, thereby
minimizing potential confounding effects of patchy
larval supply (Fig. 1B). To meet the first criterion, I
manipulated the community on each reef via selective
removals such that the relative and total abundance of
each species was similar among the 16 reefs. Within each
block, high and low complexity reefs were randomly
assigned to one of two resident fish treatments, creating
four treatments (n /4 reefs each): (1) predators and
damselfishes present, low habitat complexity; (2) predators and damselfishes absent, low habitat complexity;
(3) predators and damselfishes present, high habitat
complexity; and (4) predators and damselfishes absent,
high habitat complexity. Low complexity reefs with
predators and damselfishes had an average (SE) of 4.8
(0.6) predators and 3.0 (0.4) damselfishes, while high
complexity reefs with predators and damselfishes had an
average of 4.5 (0.3) predators and 3.8 (0.3) damselfishes.
Predator and damselfish densities reflected those found
in the matrix prior to manipulations. All fish manipulations were conducted using the fish anesthetic quinaldine, hand nets, and a BINCKE net (Anderson and Carr
1998).
After removing any existing recruits, I monitored
subsequent recruitment by conducting a visual census
of each reef every three days for 60 days. ‘‘New settlers,’’
recruits observed for the first time, were identified by
their incomplete pigmentation and small size. For each
reef, recruit mortality over the 60 days was calculated as
the number of disappearances (D) divided by the number
of observed new settlers (ONS). Additionally, because
many new settlers were probably consumed before they
were initially recorded on the two treatments where
predators and competitors were present, I assumed that
the average number of new settlers observed on the two
treatments where predators and competitors had been
removed, the estimated number of settlers (ENS), also
settled to the two treatments where predators and
278
competitors were present, and re-calculated mortality
for these two treatments as ((ENS /ONS/D)/ENS).
At the experiment’s conclusion, I estimated the total
length (TL) of each resident predator and territorial
damselfish. To determine whether recruits could use
shelter holes to escape predation and/or interference
competition, I assumed that a fish’s body depth must be
equal to or less than the diameter of a hole for the fish to
enter that hole, and compared the frequency distribution
of resident predator (excluding moray eels) and territorial damselfish body depth with that of hole diameter on
low and high complexity reefs. I converted total length
estimates to body depths using the average ratio of these
two measures from five specimens of each predator and
damselfish species. Variation (SE) in the ratio between
total length and body depth for each species, expressed
as a percentage of the mean, ranged between 0.5% and
1.8% for predators and 1.0% and 1.5% for damselfishes.
Analyses
I compared differences in reef volume, topographic
complexity, hole depth, hole diameter, and number of
potential shelter holes among high and low complexity
reefs using two-sample t-tests. I compared differences in
recruit abundance on the final day of the experiment and
recruit mortality during the experiment among the four
treatments with ANOVA. The full ANOVA model
included the following terms: blocks (random effect),
complexity, prior residents, complexity/prior residents,
block/complexity, and block /prior residents (Sokal
and Rohlf 1995). I found no evidence for significant
block/complexity or block/prior residents interactions in either visual inspections of data or ANOVA
F-tests. I have therefore reported P-values for these
interactions from the full ANOVA model and based
subsequent analyses on the reduced model (blocks
(random effect), complexity, prior residents, and complexity/prior residents). When the complexity /prior
residents interaction was significant (P 5/0.05), I
calculated a parameter estimate and 95% confidence
interval (95% CI), derived from the linear model, for
each fixed effect at each level of the other fixed
effect (Ramsey and Schafer 1997). When the complexity/prior residents interaction was not significant
(P/0.05), I analyzed the additive model (blocks (random effect), complexity, prior residents) to obtain
estimates of the effect size and 95% confidence interval,
derived from the linear model, for each fixed effect. To
insure ANOVA assumptions had been met, I tested for
variance homogeneity using Levene’s F-test and normality by examining normal probability plots (Ramsey and
Schafer 1997).
OIKOS 106:2 (2004)
Results
Recruit mortality
In the following, treatments (n /4 reefs each) are
abbreviated as: (L)/low habitat complexity, (H)/
high habitat complexity, ( /) /predators and damselfishes removed, and (/) /predators and damselfishes
present. The four treatments were L/, L/, H /, and
H/.
In the full ANOVA model, there was no evidence for
significant block /complexity (P /0.932) or block /
prior residents (P /0.774) interactions. In the reduced
ANOVA model, there was a significant complexity/
prior residents interaction (Table 1B, Fig. 3A). Where
prior residents were present, high habitat complexity
reduced recruit mortality (9/95% CI) by 63%9/25%,
while in the absence of prior residents, high habitat
complexity reduced recruit mortality by 22%9/25%. On
high complexity reefs, prior residents increased recruit
mortality by 14%9/25%, and on low complexity reefs,
prior residents increased recruit mortality by 55%9/25%.
However, when per-treatment mortality was re-calculated by assuming that approximately 70 new settlers
recruited to each treatment, there was no interactive
effect of habitat complexity and prior residents (Fig. 3B,
parallel lines indicate no interaction). Summed across
the four reefs in each treatment, the number of
mortalities observed on each treatment during the
60-day experiment was: L/ /33 mortalities, L/ /19
mortalities, H / /10 mortalities and H/ /9 mortalities.
Recruit abundance
I observed 174 newly settled Stegastes leucostictus over
the 60 days. Recruitment was greatest on the two
treatments where resident predators and territorial
damselfishes had been removed (Fig. 2). In the full
ANOVA model, there was no evidence for significant
block/complexity (P /0.634) or block/prior residents (P/0.418) interactions. In the reduced ANOVA
model, abundance was marginally influenced by habitat
complexity, strongly influenced by prior residents, and
there was no evidence for a complexity /prior residents
interaction (Table 1A). Independent of habitat complexity, removing prior residents increased average abundance (9/95% CI) by 10.09/2.3 recruits per reef.
Independent of prior residents, high habitat complexity
increased recruit abundance by 2.39/2.3 recruits per reef.
Summed across the four reefs in each treatment, the total
number of new settlers observed on each treatment over
the 60-day experiment was: L/ /77 new settlers,
L/ /22 new settlers, H / /62 new settlers and
H/ /22 new settlers.
Fig. 2. Differential effects of habitat complexity and prior
residents on recruitment of beaugregory damselfish (Stegastes
leucostictus ). Relationship between recruitment (larval settlement minus mortality) and treatments (n /4 reefs each).
Treatments consisted of habitat complexity (low or high)
cross-factored with the presence (/residents) and absence
( /residents) of resident predators and territorial damselfishes.
Error bars are 9/1 SE.
OIKOS 106:2 (2004)
Habitat complexity and fish body depth
After habitat manipulations, reef volume was similar on
low and high complexity reefs (t-test: t /0.93, P/0.370,
mean [SE] reef volume: L/2.6 [0.1] m3, H /2.8 [0.1]
m3). In contrast, low and high complexity reefs differed
significantly in each measure of habitat complexity. High
complexity reefs had greater topographic complexity
(t-test: t /7.94, PB/0.0001, mean [SE] topographic
complexity: L/1.50 [0.02], H /1.95 [0.05]). Potential
shelter holes were more abundant on high complexity
reefs (t-test: t /10.35, P B/0.0001, mean [SE] hole
abundance: L /4.9 [1.0] holes, H /21.6 [1.3] holes),
deeper on low complexity reefs (t-test: t/2.90, P/
0.012; mean [SE] hole depth: L/12.2 [0.8] cm, H /
9.3 [0.6] cm), and had smaller diameters on high
complexity reefs (Fig. 4A, t-test: t /4.44, P/0.0006,
mean [SE] hole diameter: L/6.5 [0.8] cm, H /2.8 [0.1]
cm). Comparing frequency distributions of shelter hole
diameter and resident fish body depth indicates small
predators and territorial damselfishes could access most
holes on both low and high complexity reefs (Fig. 4B,
D), whereas large predators were excluded from many
holes (Fig. 4C).
Discussion
Relationships between recruit abundance and habitat
complexity could result from several processes, such as
immigration, emigration, differential mortality, and in
279
Table 1. ANOVAs comparing Stegastes leucostictus recruit abundance on the last day of the experiment (day 60), and S.
leucostictus recruit mortality observed during the experiment.
Source
A) Recruit abundance
Block
Complexity
Prior residents
Interaction
Error
B) Recruit mortality
Block
Complexity
Prior residents
Interaction
Error
1
df
SS
MS
F
P
3
1
1
1
9
12.50
20.25
400.00
0.25
42.00
4.17
20.25
400.00
0.25
4.67
0.89
4.34
85.71
0.05
0.481
0.067
B/0.0001
0.822
3
1
1
1
9
0.14
0.71
0.48
0.17
0.21
0.05
0.71
0.48
0.17
0.02
1.90
29.80
20.13
6.97
0.200
0.0004
0.002
0.027
Levene’s
F- test
P
1.409
0.309
0.476
0.811
Levene’s F-test tests the assumption of equal variance among treatments. P /0.05 indicates this assumption has been met.
species with bipartite life histories, habitat selection by
dispersive larvae. In the present study, immigration and
emigration were unlikely due to the spatial isolation of
Fig. 3. Differential effects of habitat complexity and prior
residents on mortality of beaugregory damselfish (Stegastes
leucostictus ) recruits over 60 days. Treatments (n /4 reefs each)
consisted of habitat complexity (low or high) cross-factored
with the presence (/residents) and absence ( /residents) of
resident predators and territorial damselfishes. (A) Observed
mortality of recruits followed via censuses. (B) Observed
mortality plus estimates of unobserved mortality (see Methods).
Error bars are 9/1 SE.
280
experimental reefs, and previous studies indicate that the
focal species settles randomly with respect to microhabitat. I therefore focused on how habitat complexity
influences interactions between newly settled recruits
and residents that affect recruit survival. Factorial
manipulation of habitat complexity and the presence of
resident predators and territorial damselfishes resulted
in uniformly high recruitment where residents had been
removed regardless of habitat complexity, and where
residents were present, recruitment was slightly greater
on high complexity reefs. Prior residency by predators
and damselfishes clearly had a stronger influence on
recruitment than did habitat complexity. These results
support the predictions that recruitment would be
greatest on high complexity reefs free of resident
predators and damselfishes, lowest on low complexity
reefs with residents, and that in the presence of residents
recruitment would be greatest on high complexity reefs.
Recruitment differences among treatments were most
likely caused by (1) differential recruit mortality and/or
(2) differential larval settlement. Is there evidence for
differential settlement? The number of new settlers
observed during the 60-day study was approximately
three times greater on reefs where resident predators and
damselfishes had been removed compared to where they
were present. This suggests that settling larvae may have
selected reefs where residents had been removed as
settlement sites. However, in a previous study in this
system I demonstrated that beaugregory larvae do not
select settlement sites based on the presence or absence
of predators and damselfishes (Almany 2003). As a
result, recruitment differences in the present study were
more likely caused by differential recruit mortality. Such
mortality must have been substantial between settlement
and recruit censuses (up to 72 hours) to generate the
three-fold difference in the number of new settlers
among reefs with and without residents. This conclusion
adds to the growing list of studies demonstrating that
mortality is typically greatest shortly after settlement,
OIKOS 106:2 (2004)
Fig. 4. Frequency distributions of shelter hole diameter and
body depth of resident predators and territorial damselfishes on
high and low complexity reefs. (A) Shelter hole diameter on
high complexity reefs (n/173 holes) and low complexity reefs
(n /39 holes). (B) Body depth of small resident predators (n /
24): Cephalopholis cruentata , C. fulva , Serranus tigrinus, and
Rypticus bistrispinus. (C) Body depth of large resident predators
(n /9): Epinephelus striatus. (D) Body depth of territorial
damselfishes (n/ 25): Stegastes leucostictus and S. partitus.
Note that y-axis scale varies among plots.
and that such mortality can quickly obscure initial
patterns of abundance generated by larval supply (Planes
OIKOS 106:2 (2004)
and Lecaillon 2001, Webster 2002, Webster and Almany
2002, Almany 2003).
On reefs where predators and damselfishes were
present, recruitment was only marginally greater on
high complexity reefs. Why were negative effects of
residents similar on low and high complexity reefs?
Based on comparisons between hole diameter and the
body depths of predators and damselfishes, only large
resident predators (Epinephelus striatus ) were excluded
from most holes on high complexity reefs. In contrast,
small resident predators and territorial damselfishes
likely had access to most holes on both high and low
complexity reefs. As a result, while recruits on high
complexity reefs may have avoided interactions with E.
striatus, recruits on both low and high complexity reefs
were similarly exposed to small predators and damselfishes. If the weak positive effect of high complexity was
due to recruits avoiding E. striatus, recruit mortality was
clearly most strongly influenced by small predators and/
or damselfishes. Consistent with this conclusion, Holbrook and Schmitt (2002) found that damselfish recruits
were five times more likely to fall prey to small predatory
fishes than large predatory fishes.
Besides its possible influence on interactions between
residents and recruits, habitat complexity could affect
interactions between recruits and widely ranging transient predators, which are important sources of recruit
mortality in this system (Hixon and Carr 1997). Because
high complexity reefs had a greater number of smalldiameter shelter holes, transient predators, which are
typically 20 /30 cm TL in this system (pers. obs.), were
likely excluded from more shelter holes on high complexity reefs than on low complexity reefs. Thus, recruits may
have suffered lower mortality from transient predators
on high complexity reefs. Consistent with this hypothesis, where residents had been removed (i.e. where
transient predators were the likely source of most recruit
mortality) recruit mortality was greatest on low complexity reefs.
Previous studies suggest that predator behavior may
determine whether increased complexity reduces predation mortality. For example, increased complexity may
actually improve the capture success and foraging
efficiency of predators that employ ambush tactics by
providing more sites from which predators attack (Janes
1985) and by decreasing the visibility of predators to
prey (Coen et al. 1981). In contrast, predators that
actively search for and pursue prey are often less efficient
in high complexity habitats, presumably because increased complexity interferes with their ability to maneuver and/or visually detect prey (Flynn and Ritz 1999).
Resident predators in the present study typically ambush
prey, whereas transient predators actively pursue prey
(pers. obs.). As a result, resident predators might have
been unaffected by increased complexity, which could
281
explain the relatively weak influence of habitat complexity in this study.
Where predators and damselfishes were present, observed recruit mortality was significantly lower on high
complexity reefs. However, this conclusion is based on
comparing mortality estimates that did not include
mortality occurring between settlement and censuses, a
period of as much as 72 hours. Estimating mortality
during this period by assuming that approximately equal
numbers of new settlers arrived to each of the four
treatments indicates that where predators and damselfishes were present, approximately 70% of new settlers
were consumed before censuses. Adding this estimate of
unobserved mortality indicates that increased complexity did not significantly reduce recruit mortality. However, after some initial period of reef occupancy, recruit
survival was clearly greater on high complexity reefs.
Why might the positive effect of complexity increase
with time on the reef ? The frequent observation that
recruit mortality is greatest immediately after settlement
and quickly declines thereafter (review by Hixon and
Webster 2002) suggests that recruits may acquire behaviors and/or physical capabilities (e.g. improved swimming and sensory systems) that have important
consequences for mortality, perhaps because they allow
recruits to more effectively utilize shelter. Additionally,
recruits may need time to gain ‘‘experience’’ with
predators. For example, mice that have been previously
exposed to predators increase their use of complex
habitats and experience lower predation mortality,
whereas predator-naı̈ve mice remain in the open and
suffer higher mortality (Dickman 1992).
In the only previous coral reef study to manipulate
both predators and habitat complexity, Beukers and
Jones (1997) found that transplanted damselfish recruits
suffered lower mortality on high complexity corals.
Three important differences between their study and
the present study may have led to contrasting conclusions. First, Beukers and Jones (1997) only manipulated
predators, whereas in the present study predators
occurred with territorial damselfishes. Evidence suggests
that aggressive interactions between damselfishes and
recruits make recruits more susceptible to predation
from both resident and transient predators (Carr et al.
2002, Holbrook and Schmitt 2002, Almany 2003). Thus,
the combined effects of predators and damselfishes may
have negated any positive effects of increased habitat
complexity. Second, Beukers and Jones (1997) transplanted recruits that had been on the reef for one or
more days, whereas in the present study recruits settled
naturally to reefs. Early recruit mortality in the present
study was not influenced by habitat complexity, whereas
in both studies mortality after some period on the reef
was reduced by high complexity. Finally, the high
complexity coral species used by Beukers and Jones
(1997), Pocillopora damicornis (L.), is more finely282
branched than the high complexity coral used in the
present study (Agaricia tenuifolia , pers. obs.). Thus, P.
damicornis may provide more refuge space that excludes
predators than A. tenuifolia .
This study suggests that whether habitat complexity
reduces predation and competition likely depends on a
variety of factors. First, relationships between shelter
characteristics (e.g. hole diameter) and interactor size
could determine whether individuals can use shelter to
avoid negative interactions. Second, behavioral attributes
of predators (e.g. ambush vs pursuit predation) or
physical capabilities of prey (e.g. swimming ability)
may influence whether and how interactors respond to
habitat complexity. Finally, indirect effects resulting
from multi-species interactions could obscure effects of
habitat complexity. Further multifactor studies of how
habitat complexity influences species interactions will
improve our ability to predict how anthropogenic
disturbance, which often reduces habitat complexity, is
likely to impact communities. Such investigations are
critical given the ongoing, worldwide degradation of
coral reefs and other systems.
Acknowledgements / I am grateful to Jeanine Almany, Karen
Overholtzer, Denise Piechnik, and Michael Webster for
assistance in the field. For logistical support, I thank the staff
of the Caribbean Marine Research Center. Financial support
was provided by an NSF Graduate Predoctoral Fellowship and
International Research Fellowship, a Fulbright Postgraduate
Award, Oregon State University Zoology Research funds, and
NSF grants (OCE-96-17483 and OCE-00-93976) and NOAANURP grants (CMRC-95-3042 and CMRC-97-3109) to Mark
Hixon. Reviews of this manuscript were provided by Peter
Bayley, Mark Carr, Mark Hixon, Geoff Jones, Bruce Menge,
Philip Munday, Karen Overholtzer, Susan Sogard, and Michael
Webster.
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