MARINE ECOLOGY PROGRESS SERIES
Mar. Ecol. Prog. Ser.
Published May 19
Recruitment dynamics of coral reef fishes in
Barbados
'Bellairs Research Institute of McGill University. St. James, Barbados
'Biology Department, University of the West Indies, Cave Hill, Barbados
ABSTRACT: Recruitment and population density of coral reef fishes were studied on artificial and natural reefs on the west coast of Barbados. Recruitment of all species combined and of 3 common species
(Thalassoma bifasciatum, Stegastes partitus and Halichoeres garnoti) occurred mostly from May to
November. Recruitment rate varied little across reef types and reef locations. Population density of all
species combined and of the 3 common species varied little throughout the year, but did vary across
reefs and locations. The observation that patterns of seasonal and spatial variation in densities did not
reflect the patterns of seasonal and s p a t ~ a variation
l
in recruitment suggests that reef fish populations
in Barbados may be primarily regulated by post-settlement events. Recruitment of all species combined
and of the 3 common species was not affected by the density of all species combined. No evidence
could be found for interspecific competition, i.e. a n e g a t ~ v erelat~onshipbetween the density of one species and the recruitment of another. However, recrultrnent of H garnoti was inhibited on some reefs by
high dens~tiesof conspecifics. Post-recruitment mortality of all species combined was not affected by
denslty of all species. However, post-recruitment mortality of T bifasciatum and S. partitus was higher
on reefs of hlgher conspecific density. These results provide e v ~ d e n c efor the regulation of reef fish populat~onsIn Barbados by post-settlement processes, and suggest that intraspecific interactions may be
particularly important in limiting population size.
KEY WORDS: Recruitment. Reef fishes. Density dependence
INTRODUCTION
Coral reef fish assemblages are characterized by
high species diversity and high population densities
(Sale 1980). All but one of the several thousand fish
species known to inhabit coral reefs exhibit a bipartite
life cycle with a pelagic larval stage (Robertson 1973).
During the larval stage there is potential for widespread dispersal but mortality is extreme. The mechanisms whereby larvae return to the vicinity of reefs are
unknown (Sale 1980, Williams et al. 1986) but are
assumed to be largely passive. After recruitment to the
reef, movement of fishes between reefs is assumed to
'Present address and address for correspondence: PO Box
412, Woods Hole, Massachusetts 02543, USA
O Inter-Research 1994
Resale of full article not permitted
be negligible (e.g. Sale & Ferrell 1988, Connell &Jones
1991).
There are 2 major hypotheses on the population
dynamics of coral reef fishes, each emphasizing a different life history stage. These are the equilibrium (or
'space-limitation') hypothesis and the non-equilibrium
(or 'recruitment-limitation') hypothesis (Doherty &
Williams 1988).The former states that population densities of reef fishes and the structure of reef fish assemblages are regulated by post-recruitment competition for resources on the reef (Shulman et al. 1983,
Shulman 1984, 1985a, b, Jones 1986, 1987a, 1990).
This competition may take 2 forms. The 'single-species
equilibrium' model suggests that interspecific competition has led to the evolution of species-specific
resource requirements which allow stable coexistence
of many species on one reef (Ogden & Ebersole 1981,
Bohnsack 1983). The consequence is a reef fish assem-
Mar. Ecol. Prog. Ser. 108: 225-235, 1994
blage in which individual species populations are controlled by intraspecific density-dependent mechanisms, and therefore remain relatively constant
through time (Hunt von Herbing & Hunte 1991). The
'multi-species equilibrium' model suggests that several
species have similar resource requirements and that
competition is therefore both intraspecific and interspecific (Sale 1977, 1978). The consequence is that
whole species groups are controlled by density-dependent competitive mechanisms, and therefore that the
total standing stock of fishes on the reef remains relatively constant even though the population size of individual species may vary due to recruitment variability.
It is not clear how the processes envisaged by this
model facilitate species coexistence.
The non-equilibrium or 'recruitment-limitation'
hypothesis suggests that stochastic pre-recruitment
(planktonic) processes limit the numbers of larvae
available for settlement to reefs (Doherty 1982, 1983,
Victor 1983, 1986, Milicich et al. 1992). Population densities of reef fishes are therefore below numbers set by
available reef resources, and variation in species population densities on reefs reflects variation in the abundance of conspecific recruits. The consequence is that
both population numbers of individual species and the
total standing crop of reef fish will vary both spatially
and temporally (Sale 1991).
While the above models have been dealt with separately for the sake of convenience, they should not be
considered mutually exclusive. Both recruitment and
post-recruitment events influence the demography of
reef fishes (Forrester 1990). The relative importance of
each of these processes may vary between populat i o n ~or
, within a population from year to year or location to location (Jones 1991). Below a certain level of
recruitment, populations will be limited by larval supply; above that level, post-recruitment processes such
as predation and competition become increasingly
important (Jones 1990).
One approach to addressing the issue of whether
reef fish populations are 'space-limited' sensu the
single-species equilibrium model, 'space-limited'
sensu the multi-species equilibrium model, or 'recruitment-limited' is the investigation of 'prior resident
effects' (Shulman et al. 1983). Two types of prior resident effects may occur. First, residents may interfere
with settlement through aggression or by pre-empting
resources; second, residents may increase post-recruitment mortality to the point of density-dependence
either by preying on recruits or out-competing them
for resources (Shulman et al. 1983, Forrester 1990,
Jones 1990). Under 'single-species space-limitation',
prior resident effects should be evident but should
occur within species; under 'multi-species spacelimitation', prior resident effects should be evident
but should also occur between species; and under
'recruitment-limitation', prior resident effects should
be negligible.
The objective of this paper is to assess which of the 3
models described above is most applicable to reef fish
populations in Barbados, by investigating (l.) temporal
and spatial variation in recruitment and population
density of reef fishes in Barbados, (2) the effects of
recruitment on older juvenile and adult population
density (i.e.are patterns of recruitment reflected in the
adult population?), and (3) the effects of resident density on rates of recruitment and post-recruitment mortality (i.e. do high densities of resident conspecifics
inhibit recruitment and/or increase post-recruitment
mortality?).
METHODS
Census techniques. Recruitment and population
density of reef fishes were monitored using SCUBA on
a large (100 m2) artificial reef and an equal area of
nearby natural reef, at each of 2 sites (Miramar & Heywoods) on the west coast of Barbados (see Hunte 1987,
Tupper 1989). Many studies of reef fish recruitment
have used artificial reefs exclusiveIy (e.g. Ogden &
Ebersole 1981), while others have used only natural
coral or rock reefs (e.g. Hunt von Herbing & Hunte
1991). This design allowed us to compare artificial and
natural reefs, in order to investigate the possibility that
the type of reef used influences the results of a recruitment study.
Each artificial reef consisted of 10 derelict cars and
was deployed within 20 m of the nearest natural reef in
April 1986. The reefs were censused twice monthly
from July 1987 to June 1988. At each census, demersal
species were counted while the diver swam slowly
across the reef about 1 m above the surface. Benthic
and cryptic species and newly settled individuals were
counted by carefully searching holes and crevices in
the reef substrate. All individuals of all species were
recorded on a Perspex slate and grouped according to
size/age as follows:
Recruits: Post-larvae or very young juveniles,
recently settled and metamorphosed. Information
on typical sizes of newly recruited individuals of
each species was obtained from the literature where
possible.
Juveniles: Individuals larger than those as defined
by the above category, but smaller than the size at
sexual maturity for the species. Typically, recruits in
any one census would be recorded as juveniles by the
time of the following census.
Adults: Individuals larger than the size at sexual
maturity for the species.
Tupper & Hunte: Recruitment dynamics of coral reef fishes
Statistical analyses. The null hypothesis that recruitment and population density did not vary temporally
was tested using the Kolmogorov-Smirnoff OneSample analysis to determine significant differences
between the distribution of recruits (or juveniles and
adults) among censuses from a hypothetical discrete
uniform distribution (Wilkinson 1990). Where no significant d~fferenceswere found, recruitment or density
could not be said to vary significantly over time. The
test was carried out separately for each reef in order to
determine the effects of reef type (artificial vs natural)
a n d reef location (Heywoods vs Miramar).
Spatial variation in recruitment and population density was analyzed using the Kruskal-Wallis nonparametric analysis of variance, since various transformations failed to normalize the data or stabilize the
variance (Bartlett's test for homogeneity of variance,
p < 0.05 for all census data). For this analysis, reefs
were considered fixed treatment effects, while censuses were considered random effects a n d a repeated
measure. Where significant results were obtained by
Kruskal-Wallis tests, multiple comparisons of means
were performed using the simultaneous test procedure
(STP; Sokal & Rohlf 1981).
Effects of resident density on recruitment were analyzed by Spearman rank correlations of the number of
resident fishes in a given census versus the number of
new recruits in that census. A significant positive correlation would indicate that the presence of resident fishes
facilitates recruitment; a significant negative correlation
Table 1. Kolmogorov-Smirnoff One-Sample test of uniformity
in the temporal distribution of recruitment of reef fishes to the
2 artificial and 2 natural reefs in Barbados. D- Kolmogoro\iSmirnoff test statistic, a measure of departure from uniformity. MA: Miramar artificial; MN: Miramar natural; HA: Heywoods artificial; HN: Heywoods natural. ns: not significant
Species
Reef
D
P
All species combined
MA
MN
0.38
0.4 1
0.29
0.34
0.31
0.20
0.18
0.49
0.40
0.44
0.52
0.48
0.30
0.35
< 0.05
HA
Thalassoma bifasciatum
HN
MA
MN
Stegastes partitus
HA
HN
MA
MN
HA
Halichoeres garnoti
HN
MA
MN
HA
HN
< 0.05
< 0.05
< 0.05
< 0.05
ns
ns
< 0.05
< 0.05
< 0.05
< 0.01
< 0.05
< 0.05
< 0.05
Insufficient data
0.32
< 0.05
would indicate that the presence of resident fishes
inhibits recruitment. Where multiple comparisons
were made (i.e between groups of specres), probability
values were adjusted using the Dunn-Sidak method for
experimentwise error rates (Sokal & Rohlf 1981).
Effects of resident density on post-recruitment mortality were investigated by Spearman rank correlations
of density of residents versus a n index of post-recruitment mortality. The index of post-recruitment mortality used (I,,,)was the decline in recruit density from its
maximum value in any recruitment period to its value
at the end of the recruitment period (see Hunt von
Herbing & Hunte 1991). I, is calculated as:
where Dpr represents the density at the time of peak
recruitment a n d DeV represents the density at the e n d
of the recruitment period. Note that this index underestimates mortality since it does not discount for
recruits added to the reef during the latter part of the
recruitment period.
RESULTS
Temporal variation in recruitment rates
Srxty-seven species belonging to 26 families were
observed on the car reefs and their nearest natural
reefs. However, 3 common resident species accounted
for over 90% of all recruitment on the 4 reefs. These
were the bluehead wrasse Thalassoma bifasciatum,
the bicolor damselfish Stegastes partitus, a n d the yellowhead wrasse Halichoeres garnoti. Recruitment of
all species pooled was not uniform throughout the year
(Table 1). O n all 4 reefs, recruitment was low between
December a n d April, a n d high between May a n d
November (Fig. l a ) .
Temporal variation in recruitment of the 3 common
species can be considered separately. Recruitment of
Thalassoma bifasciatum was not uniform throughout
the year on 2 of the 4 study reefs (Table 1).Recruitment
on these 2 reefs peaked in J u n e to September a n d remained low from December until April (Fig. l b ) . Recruitment to the Heywoods artificial reef a n d Miramar
natural reef did not differ from uniform. Recruitment of
Stegastes partitus was also not uniform throughout the
year on any of the reefs (Table 1 ) . Recruitment of this
species peaked during J u n e to September a n d was low
from November to April (Fig. l c ) . Recruitment of Halichoeres garnoti on the Heywoods artificial reef was too
low to justify analysis. On the other 3 reefs, recruitment was not uniform throughout the year (Table 1).
Recruitment was highest from J u n e to October a n d
lowest from November to April (Fig. I d ) . The results
Mar. Ecol. Prog. Ser. 108: 225-235, 1994
ciatum (Fig. 2b) was not significantly different from uniform throughout the year, although there was a trend towards temporal
variation on Heywoods artificial reef
' bifasciatum, density of
(Table 2). As with K
Stegastes partitus (Fig. 2c) was not significantly different from uniform throughout the
year on any of the 4 reefs (Table 2). Density
of Halichoeres garnoti (Fig. 2d) on the Heywoods artificial reef was too low to justify
analysis. Density of H. garnoti on the Miramar natural reef was not uniform throughout
the year, showed some variation on the Miramar artificial reef, but was uniform throughout the year on the Heywoods natural reef
(Table 2). On the Miramar reefs, recruitment
was high relative to the density of resident
juveniles and adults. Consequently, the density of the total population tended to reflect
the seasonal variation in recruitment. In
summary, for most species on most reefs,
population density over the 12 mo study
period did not differ significantly from a uniform distribution, i.e. did not vary significantly over time.
Spatial variation in recruitment rates
Biweekly recruitment is expressed as the
mean number of recruits observed in the
A
S
O
D
F
M
A
M
biweekly censusesconductedover the 12mo
1987
1988
study period. The effect of reef location on
Month
biweekly recruitment of all species combined and
the
was
Fig. 1. Temporal variation in recruitment of fish (no. of recruits per 100 m2
per biweekly census) to 2 artificial and 2 natural reefs in Barbados, from
investigated over the recruitment season
July 1987 to J u n e 1988. M A : Miramar artificial; MN: Miramar natural;
(May to November). Recruitment of all speHA: Hepvoods artificial; HN: Heywoods natural. Missing data in May
cies combined and Thalassoma bifascjatum
and June are due to spring storms. ( a ) All species combined, (b) Thalasdid not differ significantly between the 4
soma bifasciatum, (c) Stegastespartitus, (d) Halichoeres garnoti
study reefs [Kruskal-Wallis Test, H = 23.2,
p > 0.05, and H = 27.0, p > 0.05, respectively
(Table 3 ) ] .Recruitment of Stegastespartitus was negliindicate that on most reefs, the temporal pattern of regible on the Heywoods artificial reef, but did not differ
cruitment of combined species and of the 3 common
species differed significantly from a uniform distribubetween the other 3 reefs (H= 18.1,p > 0.05). Recruitment of Halichoeres garnoti was also negligible on the
tion, i.e. recruitment varied significantly over time.
Heywoods artificial reef, but again did not differ
between the other 3 reefs ( H =29.4, p > 0.05). The low
recruitment of these 2 species to the Heywoods artifiTemporal variation in population densities
cial reef may be due to that reef's greater isolation from
In contrast to recruitment rates, the population denthe nearest natural reef (see Tupper 1989).
sity of all species combined (Fig. 2a) did not differ sigIn summary, recruitment strength for all species
nificantly from uniform throughout the year on any of
combined and for 2 of the 3 common species did not
the reefs (Table 2). Temporal variation in population
differ significantly between the 4 study reefs over the
densities of the 3 common species can be considered
recruitment season. This suggests that seasonal patseparately. On all 4 reefs, density of Thalassoma bifasterns in recruitment are coherent on a scale of several
229
Tupper & Hunte: Recruitment dynamics of coral reef fishes
kilometers (Heywoods vs Miramar sites) or
several meters (artificial vs natural reefs at
each site), and that the type of reef (artificial
vs natural) does not markedly influence
recruitment.
Spatial variation in population densities
The juvenile and adult density on each
reef, expressed as the mean number of juveniles and adults in the biweekly censuses for
100 m2 of reef over the post-recruitment
period (December to April), is shown for all
species combined and for common species
separately in Table 4. The population density
of all species combined differed significantly
across reefs during the post-recruitment
period (Kruskal-Wallis Test, H = 59.1, p c
0.05). Comparing sites separately for artificial and natural reefs, density of combined
species was lower on the Heywoods artificial
reef than on the Miramar artificial reef, but
was lower on the Miramar natural reef than
on the Heywoods natural reef. Comparing
artificial a n d natural reefs, density of combined species was lower on the Miramar natural reef than on the Miramar artificial reef,
but did not differ between the Heywoods
artificial reef a n d the Heywoods natural reef.
OI
.+,*".$.v
l ".+
f v $ 7 . k c + F
: 1 7 1
Population density of Thalassoma bifasciaJ
A
S
O
N
D
J
F
M
A
M
J
J
turn was not uniform across reefs, being par1987
1988
ticularly high on the Heywoods natural reef
Month
(Kruskal-Wallis Test' H = 44.71 p < 0.051
Fig. 2. Temporal variation in density of fish (no. of juveniles a n d adults
4 ) , In paired
between
per 100 mZper biweekly census) on 2 artificial a n d 2 natural reefs in Barsites, density was higher on Heywoods artifibados, from July 1987 to J u n e 1988. M i s s ~ n gdata in May a n d J u n e a r e
d u e to spring storms. (a) All species combined, (b) Thalassoma bifasciacial than Miramar artificial reef, but Miramar
tum, (c) Stegastes partitus, (d) Halichoeres garnoti
natural reef had a lower density than Heywoods natural reef. Comparing artificial with
Heywoods artificial reef. In paired comparisons of
natural reefs, density of T bifasciatum was lower on
Heywoods artificial reef than on Heywoods natural
sites, population density on the Heywoods artificial
reef, but was lower on the Miramar natural reef than
reef was lower than that on the Miramar artificial reef,
on Miramar artificial reef. Population density of Stebut was lower on the Miramar natural reef than on the
gastes partitus was also not uniform across reefs ( H =
Heywoods natural reef. Comparing artificial with natural reefs, density of H. garnoti was lower on Hey57.3, p < 0.05; Table 4 ) . In pairwise comparisons of
sites, population density was lower on the Heywoods
woods artificial reef than on Heywoods natural reef,
artificial reef than on the Miramar artificial reef, but
a n d did not differ between reef types a t Miramar. In
was lower on the Miramar natural reef than on the
summary, population density of combined species a n d
Heywoods natural reef. Comparing artificial with natof the 3 common species differed across the 4 study
reefs over the 12 mo period. The differences in populaural reefs, density of S. partitus was lower on the Heywoods artificial reef than on the Heywoods natural
tion densities could not b e attributed to reef location or
reef, but was lower on Miramar natural reef than on
reef type (artificial vs natural), but may b e partly
Miramar artificial reef. Population density of Halichoexplained by the differences in substrate conlplexity
eres garnoti was again not uniform across reefs (H =
a n d isolation of the study reefs (see Tupper 1989).
39.5, p c 0.05; Table 4 ) , and was particularly low on the
Since the study reefs did not differ in recruitment for
l
Mar. Ecol. Prog. Ser. 108: 225-235, 1994
230
Table 2. Kol.mogorov-Smirnoff One-Sample test of uniformity
in the temporal distribution of population density of reef fishes
on the 2 artificial and 2 natural reefs in Barbados. D: Kolmogorov-Smirnoff test statlstlc, a measure of departure from
uniformity. VIA: Miramar a r t ~ f ~ c i aMN:
l ; Miramar natural, HA
Heywoods artificial, Hhr: Heywoods natural. ns: not significant
Species
Reef
All species combined
Thalassoma bifasciatum
Stegastes partitus
Halichoeres garnoti
MA
MN
HA
HN
MA
MN
HA
HN
MA
MN
HA
HN
D
P
0.04
0.07
0.11
0.15
0.05
0.13
0.28
0.22
ns
ns
ns
ns
ns
ns
0.19
0.20
0.07
0.03
0.27
0.41
Species
All species combined
ns
ns
ns
ns
ns
0.08
<0.05
Insufficient data
0.18
ns
Prior resident effects
Spearman rank correlation coefficients of number of
recruits in each biweekly census versus the juvenile and
adult density of all species combined at the time of the
census are shown for the 12 mo study period in Table 5.
Table 3. Kruskal-Wall~s Test of among-reef variation In
recruitment rates of reef fishes (no. of recruits per 100 m' per
biweekly census) over the recruitment period (May to
November) on the Miramar and Heywoods artificial and natural reefs. MA: Miramar artificial reef; MN: Miramar natural
reef; HA: Heywoods artificial reef; HN: Heywoods natural
reef; ns: not significant. Lines connect recruitment strengths
of no significant difference, a s determined by STP
All species com.bined
MA
HN
23.0 33.0
40.1
Thalassoma bifasciatum MN
HA
HN
MA
HA
22.2
MN
9.4
14.9
17.5
19.2
Stegastes partitus
HA
MA
MN
HN
Halichoeres garnoti
HA
M
10
3.2
3.4
4.6
MA
HN
MN
8.7
9.1
9.3
p
MN HN HA
a 4 3 6 . 1 451.Q <0.05
Thalassorna bifasciatum MN HA MA HN
76.3 <0.05
35.2
Stegastes partitus
HA MN HN MA
71.8 75.2 102.9 103.0 c 0 0 5
Halichoeres garnoti
HA MA MN HN
0.1 14.6 17.3 29.4 <0.05
0.06
Mean biweekly recruitment
Mean biweekly recruitment
MA
&&$!
any of the species studied but did differ in population
densities, the variation in density of a species across
reefs cannot be the consequence of variation in its recruitment, but must be due to post-settlement events.
Species
Table 4. Kruskal-Wallis Test of Comparison of among-reef
variation in the density (no. per 100 m2 per biweekly census)
of reef fishes over the post-recruitment period (December to
April) on the Miramar and Heywoods artificial and natural
reefs. MA: Miramar art~ficlalreef; MN: Miramar natural reef,
HA: Heywoods artif~cialreef, HN: Heywoods natural reef
Lines connect densit~esof no significant difference, as determ ~ n e dby STP
p
ns
ns
10.05
<0.05
The coefficients are presented separately for each reef,
and for combined recruits, recruits of Thalassoma bifasciatum, recruits of Stegastes partitus and recruits of
Halichoeres garnoti. We chose the 3 most common species for these analyses for 2 reasons. First, agonistic interactions between these species were seen on almost
every dive; juveniles and adults of the 2 labrid species
were often observed chasing heterospecific recruits
Table 5. Spearman rank correlation coefficients (rS)of number
of recruits in each biweekly census during the recruitment
period (May to November) versus juvenile and adult density
of all species combined at the time of the census. Data are
presented separately for each reef, and separately for
combined recruits of all species and for recruits of Thalassoma bifasciatum, Stegastes partitus, and Halichoeres garnoti. Probabilities have been adjusted usina the Dunn-Sidak
method for experimentwise error rate. MA: Miramar artificial:
MN: Miramar natural, HA. Heywoods artificial; HN: Heywoods natural. ns. not significant
-
Species
All species combined
Reef
IMA
MN
HA
HN
Thalassoma bifasciatum MA
MN
HA
HN
MA
Stegastes partitus
MN
HA
HN
Halichoeres garnoti
Tupper & Hunte: Recruitment dynamics of coral reef fishes
away from shelter sites, and adult S, partitus were observed chasing labrid recruits away from e g g clutches.
Second, the fact that these 3 species are the most common means that they will have higher encounter rates
among each other than with less common species. For
all species combined and for the 3 common species separately, the number of recruits at each biweekly census
d u r ~ n gthe recruitment period (May to November) was
not affected by the density of juveniles a n d adults of all
species on any of the study reefs (Table 5).
Spearman rank correlation coefficients of the number of Thalassoma bifasciatum recruits in each
biweekly census and the juvenile and adult density of
each of the 3 common species during that census a r e
shown for the recruitment period in Table 6. Recruitment of ?: bifasciatum was not correlated with juvenile
and adult density of conspecifics on any of the study
reefs. Recruitment was not affected by density of Stegastes partitus or Halichoeres garnoti on any of the
study reefs. Similarly, recruitment of S. partitus was
not correlated with density of juvenile and adult conspecifics on any of the study reefs (Table ?). Recruitment of S. partitus was also not affected by density of
T bifasciatum or H. garnoti on any of the study reefs.
For Halichoeres garnoti, recruitment was negatively
correlated with juvenile and adult density of conspecifics on Miramar artificial reef (rS= -0.89, p < 0.05),
Heywoods artificial reef (rs = -0.89, p < 0.05; analysis
was restricted to those weeks during which H. garnoti
was present) and Heywoods natural reef (rs = -0.78,
Table 6. Thalassoma bifasciatum. Spearman rank correlation
coefficients of number of recruits in each b~weeklycensus
d u r ~ n gthe recruitment period (May to November) versus the
juvenile and adult density of each of the 3 common species
(7: bifasciatum, Stegastes partitus, and Halichoeres garnoti)
at the time of the census. Data are presented separately for
each reef Probabilities have been adjusted using the DunnSidak method for experimentwise error rate. MA: Miramar
artificial; MN: Miramar natural; HA: Heywoods artificial;
HN: Heywoods natural, ns: not significant
p < 0.05; Table 8) Interestingly, there was no relationship between the density of H. garnoti on a given reef
and the presence or absence of significant negative
interactions. For example, density of H. garnoti did not
affect recruitment of conspecifics on Miramar natural
Table 7. Stegastespari~tus.Spearman rank correlation coefflcients of number of recruits in each biweekly census during
the recruitment penod (May to November) versus the juvenile
and adult density of each of the 3 common species ( S .partitus,
Thalassoma bifasdaturn, and Halichoeres garnoti) at the time
of the census. Data are presented separately for each reef.
Probab~lities have been adjusted uslng the Dunn-Sidak
method for experimentwise error rate. MA: Mirarnar artificial;
MN: Miramar natural; HA: Heywoods artificial; HN: Heywoods natural. ns: not significant
Recruit
species
Resident
species
Reef
rs
P
S. partitus
S. partitus
MA
MN
HA
HN
MA
MN
HA
HN
MA
MN
HA
HN
-0.69
-0.01
-0.69
0.20
0.49
0.07
0.14
0.10
-0.38
0.46
0.07
-0.34
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
T b~fasciatunl
H.garnoti
Table 8. Hallchoeres garnoti. Spearman rank correlation coefficients of number of recruits in each biweekly census during
the recruitment period (May to November) versus the juven~le
and adult density of each of the 3 common species (H.
garnoti,
Thalassoma bifasciatum, and Stegastespartjtus) at the time of
the census. Data are presented separately for each reef. Probabilities have been adjusted using the Dunn-Sidak method for
expenmentwise error rate. MA: Miramar artificial; MN: Miramar natural; HA: Heywoods artificial; HN: Heywoods natural.
ns. not significant
Recruit
species
Resident
species
Reef
rs
P
Recruit
species
Resident
species
Reef
rs
T bifasciatum
T bifasciatum
MA
MN
-0.21
0.13
-0.67
0.45
-0.19
0.78
-0.05
0.03
0.03
-0.55
0.05
-0.54
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
ns
H. garnoti
H.garnoti
MA
MN
HA
HN
MA
MN
HA
HN
MA
MN
HA
HN
-0.89
-0.23
-0.89
-0.78
0.03
0.28
-0.26
0.19
-0.12
0.50
0.54
-0.29
HA
HN
MA
MN
HA
HN
MA
MN
HA
HN
7 bifasciaturn
P
<0.05
ns
~0.05
<0.05
ns
ns
ns
ns
ns
ns
ns
ns
Mar. Ecol. Prog Ser. 108: 225-235, 1994
reef, which supported the highest density of that species. However, recruitment was inhibited by residents
on Heywoods artificial reef, which supported the lowest density. It is possible that each reef has a different
'threshold density' or carrying capacity above which
negative effects of residents on recruitment occur. This
level may vary with factors such as substrate type
(which can influence the abundance and quality of
shelter), food or other resources. Recruitment of H. qarnoti was not affected by density of Thalassoma bifasciatum or Stegastes partitus on any of the study reefs.
In summary, only H. garnoti displayed density-dependent recruitment, and recruitment was only inhibited
by conspecifics. Density of combined species or sympatric species did not affect recruitment of all species
combined or of the 3 species individually. This observation suggests that the competitive interactions
affecting recruitment of H. qarnoti are primarily
intraspecific.
An index of post-recruitment mortality, reflecting the
decline in density following peak recruitment (see
'Methods'), was calculated for all species combined
and separately for the 3 common species on each study
reef (Table 9). Possible effects of resident density on
post-recruitment mortality were investigated by correlating the index of mortality with the density of juveniles and adults at the time of peak recruitment. Postrecruitment mortality of all species combined was not
correlated with density of juveniles and adults of all
Table 9. Index of post-recruitment mortality (I,) and density
at peak recruitment (Dpr)on each reef for all species combined and for Thalassoma bdasciatum. Stegastespartitus, and
Halichoeres garnoti. I, is calculated as described in the
'Methods' MA: Miramar artificial reef; MN: Miramar natural
reef; HA: Heywoods artificial reef; HN: Heywoods natural
reef
Species
Reef
I.
(S,,)
All species combined
Thalassoma bifascia turn
Stegastes partitus
Halichoeres garnoti
MA
HA
MN
HN
MA
HA
MN
HN
MA
HA
IMN
HN
MA
HA
MN
HN
D,,
(no. per 100mL)
-B
X
S. partitus
30
Density (no./100 rn2)
Fig. 3. Index of post-recruitment mortality of fishes on a reef
versus density of juvenile and adult conspecifics on that reef
at the time of peak recruitment. Data are presented separately for Thalassoma bifasciatum. Stegastes partitus and
Halichoeres garnoti
species combined (Spearman rank correlation, rs =
0.32, p > 0.05). Similarly, post-recruitment mortality of
Thalassoma bifasciatum, Stegastes partitus and Halichoeres garnoti was not significantly correlated with
density of all species combined (rs = -0.2, p > 0.05; rs =
0.8, p > 0.05; and rs = 0.4, p > 0.05, respectively). For
7: bifasciatum, post-recruitment mortality was significantly correlated with density of juvenile and adult
conspecifics (rs = 1.0, p = 0.0; Fig. 3). Post-recruitment
mortality of S. partitus was significantly correlated
with increasing density of juvenile and adult conspecifics (rs = 1.0,p = 0.0; Fig. 3). There was a trend for
post-recruitment mortality of H. garnoti to increase
with density of juvenile and adult conspecifics, but the
result was not significant with only 3 degrees of freedom (rs = 0.8, p = 0.11). It is interesting that on 3 of 4
reefs, recruitment of H. garnoti was strongly densitydependent, while post-recruitment mortality was less
evidently density-dependent. Recruitment of 7: bifasciatum and S. partitus displayed no density-dependence, while post-recruitment mortality of these species was strongly density-dependent. This suggests
that the post-settlement processes regulating adult
population size may vary with species.
In summary, the results suggest that post-recruitment mortality increases with increasing resident conspecific density, and that the processes resulting in the
increased post-recruitment mortality are speciesspecific. It was not possible to determine the effects of
interspecific competition on post-recruitment mortality
Tupper & Hunte. Recruitment dynamics of coral reef fishes
among the 3 common species, as similarities between
species in spatial patterns of recruitment, density, and
mortality (probably in response to physical characteristics of the reef habitat; see Tupper 1989) would lead to
spurious correlations of mortality of one species with
population density of another
DISCUSSION
Temporal variation in recruitment
Although conclusions cannot be drawn from only
1 yr of data, recruitment of the common reef fishes in
Barbados appeared to show seasonal variation. Most
species studied recruited primarily from J u n e to
November. Thalassoma bifasciatum in Barbados
recruited mainly in the summer months in 1984, 1985,
and 1987-88, with a consistent seasonal peak from
July to September (Tupper 1989, Hunt von Herbing &
Hunte 1991). Seasonal recruitment is widespread in
reef fishes. For example, Williams & Sale (1981) and
Williams (1983) found strong seasonal variation in
recruitment for a guild of pomacentrids on the Great
Barrier Reef, and Williams (1983) commented on the
'remarkable constancy' in the timing of the annual
mid-summer recruitment peak. Likely causes of seasonal recruitment include increases in adult spawning
activity (Powles 1975, Hunt von Herbing & Hunte
1991), seasonal changes in current patterns (Johannes
1978. Talbot et al. 1978, McFarland 1982), and/or seasonal variation in survival of planktonic larvae (Sale
1980, McFarland et al. 1985, Victor 1986). Note however that variation of survival in the plankton is
believed to be highly stochastic (Victor 1986).
Several authors have found spawning and recruitment to follow similar seasonal patterns, separated by
a period of time approximating the larval life of a typical reef fish (Munro et al. 1973, Watson & Leis 1974,
Luckhurst & Luckhurst 1977). This suggests that seasonal variation in spawning may be the principal cause
of seasonal variation in recruitment of reef fishes
(Doherty 1991). Robertson et al. (1988) found that
spawning and recruitment of Stegastes partitus in
Panama were coupled, a n d that both spawning activity
a n d recruitment followed a lunar cycle. Similar coupling of spawning and recruitment has been observed
in S. partitus in Barbados (Tupper 1989). Hunt von
Herbing (1988) suggests that recruitment of Thalassoma bifasciatum in Barbados also follows spawning
by a time lay that complements the duration of the
planktonic larval phase. These data indicate that temporal variation in recruitment of these 2 species results
from variation in spawning rather than from variation
in survival of planktonic larvae. Coupling of spawning
233
a n d recruitment of T bifasciatum (Hunt von Herbing
1988, Hunt von Herbing & Hunte 1991) and S. partitus
in Barbados is circumstantial evidence for the maintenance of primarily discrete island populatlons (see
Hunt von Herbing 1988, Tupper 1989). I f , in Barbados,
reef fishes were maintained in relatively discrete
island stocks, one might expect a consistent seasonal
spawning regime to b e coupled to a consistent seasonal recruitment regime. Interannual variation in the
strength of the seasonal recruitment, rather than in the
timing of recruitment, might then be attributed to
processes in the plankton, such as predation or starvation, or to oceanographic processes such as wind and
current anomalies.
Spatial variation i n recruitment
Results of this study indicate that peaks of recruitment of several species are coherent over sites separated by distances ranging from meters to tens of kilometers. Doherty (1987) suggested that pre-settlement
fish larvae a r e aggregated on a t least 2 spatial scales,
microscale patches of a few meters a n d mesoscale
patches of tens of kilometers. Microscale patches a r e
probably primarily influenced by the aggregation of
schooling fishes such as Haemulidae (McFarland et al.
1985, Shulman 1985a). In Barbados, the tomtate
Haemulon aurolineatun~has been observed to settle in
schools of up to several hundred, occupying a n area of
only 1 or 2 m2 (author's pers. obs.). Doherty (1987)
found recruitment of a pomacentrid on the Great Barrier Reef to b e coherent over a distance of 70 km.
Recruitment peaks in this study were coherent at the
Heywoods and Miramar sites, about 10 km apart. It
therefore appears that, as suggested by Powles (1975),
fish larvae a r e aggregated off the west coast of Barbados in a mesoscale patch greater than 10 k m in width.
Note that the occurrence of a mesoscale larval patch
does not preclude the possibility of microscale patch
structure within it.
Temporal and spatial variation in
population densities
A key issue in determining whether reef fish populations a r e space-limited or recruitment-limited is
whether post-settlement events such a s competition,
disease and predation exert sufficient influence to
override the effects of spatial and temporal variation in
settlement patterns (Robertson 1988). In support of
recruitment-limitation, Victor (1983, 1986) suggested
that settlement controls patterns of adult densities in
Thalassoma bifasciatum. Likewise, Doherty & Williams
Mar. Ecol. Prog. Ser. 108: 225-235, 1994
234
(1988) reported that temporal patterns in adult and
juvenile density of Pomacentrus amboinensis
appeared to reflect successive peaks in recruitment.
However, Jones (1991) states that in the majority of
recent studies, changes in adult population size do not
reflect the history of recruitment. In the present study,
temporal variation in population density did not differ
significantly from uniform. The observation that
recruitment varies temporally but population density
does not suggests that post-settlement processes following recruitment pulses are strong enough to
quickly return total population numbers to pre-settlement values. In addition, although mean recruitment
over the 12 mo period did not differ on different reefs,
mean population density did. This suggests that mean
population density on a reef is not primarily controlled
by recruitment strength to the reef. Together the
results imply that over the course of this study, reef fish
populations in Barbados were close to carrying capacities of the reefs, i.e. that they were more typically
'space-limited' than 'recruitment-limited'.
Prior resident effects
Victor (1983, 1986) argued that Thalassoma bifasciaturn in Panama is recruitment-limited, and hence that
there are consistently fewer fish than the habitat can
support. He therefore suggested that effects of residents on recruitment rates and post-settlement mortality should be negligible. Doherty (1982, 1983),working
on territorial pomacentrids on the Great Barrier Reef,
concluded that recruitment and juvenile survivorship
were independent of resident density. In contrast to the
above results, Shulman et al. (1983) found that density
of resident fishes on reefs in the Virgin Islands
(Caribbean) affected settlement in at least 2 ways; first,
settlement of 3 species decreased in the presence of a
territorial pomacentrid, and second, prior settlement of
a juvenile predator lowered successful recruitment of 2
prey species. Shulman et al. (1983) suggested that such
processes would influence the population size and fish
assemblage structure on reefs. High densities of resident conspecifics have been shown to reduce growth
rates of newly settled fish in a number of studies (Jones
1987a, b, 1988, Forrester 1990). Hunte & C6te (1989)
found that territory size of resident blennies Ophioblennius atlanticns on Barbados reefs decreased significantly following recruitment pulses, and that postrecruitment mortality was density-dependent. They
therefore suggested that populations of 0.atlanticus in
Barbados were space-limited. In the present study, the
density of combined species did not affect the recruitment of all species to the reef, or post-recruitment mortality of any species on the reef. However, significant
negative interactions were detected between recruitment rate and conspecific resident density of Halichoeres garnoti on 3 of 4 reefs. Moreover, post-recruitment
mortality of 'I: bifasciatum and Stegastes partitus was
significantly correlated with juvenile and adult density
at the time of peak recruitment. These results suggest
that competitive interactions at or following settlement
may limit the number of successful recruits to reefs and
hence affect fish population size. The results also suggest that post-recruitment processes regulating adult
population size may vary among species or from reef to
reef. The fact that the significant competitive interactions are intraspecific may be interpreted as supporting the hypothesis that coral reef fishes have evolved
specialized, species-specific niche requirements,
arguably in response to past interspecific competition.
These specific niche requirements now reduce interspecific interactions, and thereby promote species
coexistence and high species richness. In summary,
given that significant prior resident effects were
detected in this study in certain circumstances and not
in others, it appears, as discussed by Jones (1991),that
limitation of reef fish populations by interactions on the
reef or by recruitment is a matter of degree, i.e. that the
opposing theories of space limitation and recruitment
limitation should be perceived as extremes on a continuum. Further investigations into the processes regulating populations of reef fishes should adopt a more
pluralistic perspective, addressing both pre- and postrecruitment events.
Ackno~~ledgernents.
Assistance in the field was provided by
lone Hunt von Herblng and Ronald Hlnds. Funding for the
research was provided by Natural Sclences and Englneenng
Research Council Operating Grant no. A0264 to W.H. and by
a Metcalf Foundation Postgraduate Fellowship to M.T Critical reviews by I. Hunt von Herbing and 3 anonymous reviewers greatly improved the quality of this paper.
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This article waspresented by P J. Wangersky (Senior
Editorial Advisor), Victoria, B.C., Canada
Manuscript first received: J u n e 17, 1993
Revised version accepted: February 15, 1994