AN ABSTRACT OF THE THESIS OF
Michael S. Webster for the degree of Doctor of Philosophy in Zoology presented on
September 11,2001.
Title: Factors Affecting the Dynamics and Regulation of Coral-reef Fish Populations
Abstract approved:
Redacted for Privacy
MarK A. 1-lixon
Ecologists have long questioned why fluctuating populations tend to persist
rather than go extinct. Populations that persist indefinitely are regulated by
mechanisms that cause demographic density dependence, which works to bound
fluctuation above zero. In a series of studies, I have sought to determine the processes
and mechanisms that regulate local populations of coral-reef fish. In the Exunia Keys,
Bahamas, fairy basslets (Gramma loreto) live in aggregations on the undersides of
coral-reef ledges. These aggregations often constitute local populations because
movement between aggregations is rare. The largest individuals occupy prime feeding
positions near the front of ledges and force smaller individuals remain near the back
where they have lower feeding rates. Based on these initial observations, I designed
two experimental studies of the demographic consequences of variation in basslet
density. In the first study, I manipulated the density of newly-settled fish to explore the
effects of high recruitment on population size. Populations with experimentally
elevated recruitment converged in density with unmanipulated populations, primarily
due to density-dependent mortality. I found no evidence that density dependence was
caused by intraspecific competition; rather it appeared to be due to a short-term
behavioral response by predators (aggregative andlor type 3 functional response). In a
second study, I manipulated the densities of adults among populations with a standard
average density of newly-settled fish. Two measures indicated that the intensity of
competition increased at higher densities of adults, which likely made small fish more
susceptible to predation, thereby causing density-dependent mortality. Long-term
observations indicated that basslet populations were regulated at temporal scales
exceeding two generations. At Lizard Island on the Great Barrier Reef, I also
examined how patterns of recruitment of coral-reef fishes were modified across a range
of natural recruit densities in the presence and absence of resident predators. Predators
decreased recruitment and increased mortality for all species, but these effects varied
considerably among species. The results of each of these studies stress the importance
of both competitive and predatory mechanisms in modiIying patterns of abundance
established at the time of larval settlement, as well as regulating local population size.
ght by Michael S. Webster
;eptember 11, 2001
11 Rights Reserved
Factors Affecting the Dynamics and Regulation of Coral-Reef Fish Populations
by
Michael S. Webster
A THESIS
submitted to
Oregon State University
in partial fulfillment of
the requirements for the
degree of
Doctor of Philosophy
Presented September 11, 2001
Commencement June 2002
Doctor of Philosophy thesis of Michael S. Webster presented on September 11, 2001
APPROVED:
Redacted for Privacy
Redacted for Privacy
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Dean of
I understand that my thesis will become part of the permanent collection of Oregon
State University libraries. My signature below authorizes release of my thesis to any
reader on request.
Redacted for Privacy
Michael S. Webster, Author
Acknowledgments
My thesis benefited most significantly from three people: Mark Hixon, Glenn
Almany and Tess Freidenburg. As my advisor, Mark played a central role in my
development as a scientist from conducting fieldwork, to writing papers, to giving
talks. I thank him for his immense patience listening to my research ideas, and wading
through my rough drafts, and for his endless good suggestions. With any luck some of
his skill has rubbed off in the last five years.
Glenn has been my primary scientific peer from the day I started graduate
school. I acknowledge him for the hours of help underwater, in the boat, revising
papers and discussing ideas, but most of all I thank him for being a true friend. I look
forward to being colleagues and friends for the rest of our lives. Thank you Glenn,
may you never again run face first into fire coral while chasing a basslet.
I met Tess when I first came to graduate school. Since then we've been nearly
inseparable (barring field seasons). I thank her for help and support at so many
different levels that I don't know where to start. Perhaps it will suffice to thank her for
being my dearest friend and companion.
The graduate students of OSU, and especially those on the fifth floor, have
been a fantastic source of advice and friendship. Karen Overholtzer and Barb Byrne
have been especially important as colleagues and friends. I thank Barb for always
being sunshine in the Bahamas, and Karen for the unique experience of building
Overkill.
My graduate committee has played an active role in the preparation of my
thesis. I am grateful to all of you. In particular, I thank Bruce Menge for teaching me
so much about science and for being a friend, Fred Ramsey for helping me muddle
through a stats minor and for answering my endless stats questions, Sue Sogard for
constant good advice on my research, Paul Risser for always taking the time to read
my papers and discuss my progress, and Alix Gitelman for joining my committee one
week before my final defense.
I thank G. Almany, T. Anderson, B. Byrne, T. Freidenburg, E. Kast, J.
Lubchenco, K. Overholtzer and my graduate committee for constructive reviews on
manuscripts. I am very grateful to A. Kaltenberg, who was instrumental in gathering
the data for Chapter 2. Many thanks to the staff of the Caribbean Marine Research
Center, Lizard Island Research Station and the OSU Zoology Department. Thanks
also to all who helped me with fieldwork.
Financial support was provided by an NSF Pre-Doctoral Fellowship, Zorf
grants to the author, and NSF grants (OCE-96-17483 and OCE-00-93976) and NURPNOAA grants (CMRC-95-3042 and 97-3 109) to M. Hixon.
Contribution of Authors
Dr. Mark A. Hixon was directly involved in the data collection, analysis and
writing of Chapter 2 and is therefore included as an author.
I
Table of Contents
Chapter 1: Introduction.
1
Chapter 2: Mechanisms and Individual Consequences of Intraspecific Competition in a
Coral-reef Fish .............................................................................................................. 6
Abstract............................................................................................................. 6
Introduction...................................................................................................... 7
Methods .......................................................................................................... 10
Fish Size and Feeding Position................................................................... 10
Removal Experiment .................................................................................. 11
Results............................................................................................................ 16
Fish Size and Feeding Position................................................................... 16
Removal Experiment .................................................................................. 16
Discussion....................................................................................................... 24
Chapter 3: Temporal Density Dependence and Population Regulation in a Marine
Fish ............................................................................................................................. 31
MainText ....................................................................................................... 31
Methods ..........................................................................................................
37
DensityExperiment .................................................................................... 37
VideoMonitoring ....................................................................................... 38
GenerationTime ......................................................................................... 39
TimeSeries ................................................................................................. 40
Chapter 4: Regulatory Effects of Intraspecific Competition in a Coral-reef Fish ...... 41
Abstract ........................................................................................................... 41
Introduction.................................................................................................... 42
Methods ............................................................................................................ 44
Table of Contents, continued
StudySpecies .............................................................................................. 44
Monitoring .................................................................................................. 45
1999 Experiment ........................................................................................ 45
2000 Experiment ........................................................................................ 47
Video.......................................................................................................... 50
Results............................................................................................................ 50
Monitoring .................................................................................................. 50
1999 Experiment ........................................................................................ 51
2000 Experiment ........................................................................................ 51
Video.......................................................................................................... 59
Discussion ....................................................................................................... 59
Chapter 5: Role of Rredators in the Early Post-settlement Demography of Coral-reef
Fishes .......................................................................................................................... 66
Abstract ........................................................................................................... 66
Introduction.................................................................................................... 67
Methods .......................................................................................................... 70
StudySystem .............................................................................................. 70
ExperimentalDesign .................................................................................. 71
DataAnalysis .............................................................................................. 74
Results............................................................................................................ 76
Recruitment ................................................................................................
Mortality .....................................................................................................
Abundance ..................................................................................................
Recruitmentlabundance Relationships .......................................................
Recruitment/mortality Relationships ..........................................................
76
80
82
83
86
Discussion....................................................................................................... 86
Chapter 6: General Conclusions ................................................................................. 92
LiteratureCited .......................................................................................................... 97
List of Figures
Figure
Page
2.1
Feeding positions of Gramma loreto on a typical reef
12
2.2
The relative feeding position ( ± SE) of each size class
of Gramma loreto.
17
Aggression between size classes of Gramma loreto on
control ledges.
19
The average relative feeding position and relative
position when chased for each size class of Gramma
loreto on control ledges (± SE, N=7 ledges each).
20
The frequency of aggressive interactions directed
toward smaller size classes of Gramma loreto on
control and removal ledges ( + SE, N=7 ledges each).
21
The relative feeding position (± SE, N=7 ledges each)
of smaller size classes of Gramma loreto before and
after removal of larger fish on (a) removal ledges
versus (b) unmanipulated control ledges.
22
The average change in feeding position and difference
in feeding rate for 3-cm Gramma loreto, after
experimental removals of larger fish, relative to
unmanipulated controls.
25
3.1
Summary of demographic rates and predator behavior.
34
3.2
Gramma density (± SE) in density-increase and
unmanipulated control populations (n = 8 each) over
three years.
36
The density of adult basslets (fish >4cm) versus the
size of ledges in June 1998, 1999, and 2000.
48
2.3
2.4
2.5
2.6
2.7
4.1
ledge.
List of figures, continued
Figure
4.2
4.3
4.4
4.5
4.6
4.7
4.8
4.9
5.1
5.2
Page
Net per capita mortality of transplanted, recentlyrecruited basslets versus the density (A) and population
size (B) of resident fish from a pilot study in 1999.
52
The change in density (± SE) of transplanted recruits in
each treatment during the 2000 experiment.
53
Final density (A) and net per capita mortality (B) of
new recruits as a function of adult density.
55
The average per capita rate of aggressive chases (+SE)
involving transplanted recruits in each treatment.
56
The relative frequency of feeding positions of
transplanted recruits in each adult treatment.
57
The size frequency of N transplanted recruits from each
treatment at the end of the 2000 experiment.
58
The average densities of new fish (+SE) that recruited
to each of the three experimental treatments and to five
additional ledges from which all basslets were
removed.
The relative frequency (+SE) of spatial positions of (A)
all basslet predators, (B) trumeptfish, Aulostomus
maculatus, and the groupers, (C) Cephalopholisfulva,
and (D) C. cruentata, on unmanipulated ledges.
Map of Lizard Island, Great Barrier Reef, Australia
showing the location and spatial arrangement of the
experimental array of transplanted Porites cylindrica
reefs.
The total number of new recruits observed on 18
experimental reefs over a 50-day period.
60
61
71
79
List of Figures, continued
Figure
5.3
5.4
6.1
Page
The effect of predators on a total recruitment, b
mortality, and c final abundance (mean ± SE) or all
species and families over 50 days.
82
The relationship between recruitment and both final
abundance and net per capita mortality for a,b N.
cyanomos, c,d P. amboinensis, and e,f all pomacentrids
using least squares regression.
85
Qualitative summary of density-dependent factors
affecting population dynamics of basslets.
94
List of Tables
Table
5.1
5.2
5.3
5.4
Page
Total number of recruits observed during the 50-day sampling period
of each species from three families and the number of reefs on which
they were observed (N = 18 reefs total).
78
Summary statistics for the effect of predators on recruitment, mortality,
and abundance of each species and family.
81
Summary statistics for slopes from multiple linear regressions of final
abundance as a function of the number of recruits.
84
Summary statistics for slopes from multiple linear regressions of per
capita mortality as a function of the number of recruits.
86
Dedication
I dedicate my thesis to E.J. Kast. She taught me to love nature and she always
encouraged me to follow my dreams.
Factors Affecting the Dynamics and Regulation of Coral-reef
Fish Populations
Chapter 1: Introduction
For more than a century, ecologists and fisheries biologists have tried to
understand the factors that determine the abundance of marine fishes (Smith, 1994).
This issue is particularly pertinent today since the majority of the world's fisheries are
already either fully or over exploited (Botsford et al., 1997). In the studies below, my
goal was to better understand the mechanisms driving the population dynamics of
marine fishes by studying fishes on coral reefs, which are both easy to observe directly
and manipulate. Coral reef fishes can serve as model systems for understanding
demersal marine fishes in general because they are likely subject to similar factors that
determine abundance.
The study of the ecology of coral-reef fishes began in earnest in the 1960's
with the beginnings of widespread use of SCUBA. In the subsequent four decades,
marine ecologists have participated in a lively debate about the relative importance of
processes that drive population and community dynamics of coral-reef fishes. Some of
the earliest studies of coral-reef fishes argued that competition was the predominant
factor affecting the abundance and distribution of fishes (Smith and Tyler, 1972,
Roughgarden, 1974, Ehrlich, 1975, Smith, 1978), which was consistent with the
prevailing view among ecologists that populations and communities were structured
2
by competition. Proponents of this model argued that the rate of arrival of new
individuals was relatively unimportant because post-settlement competition modified
settlement patterns. In the 1970's this view was challenged by the lottery model,
which contended that, while reef fish communities were still subject to intense
competition, community structure changed via the chance process of new recruits
locating vacant habitat patches (Sale, 1974, 1977, 1 978b). In this model, prior
residency, not competitive dominance, was the primary determinant of population and
community dynamics. While the lottery model did fit some data sets (e.g. Sale and
Dybdahl, 1975, 1978, Sale, 1 978a, 1979), its assumption that reef-fish communities
were saturated was questioned in the 1980's by researchers who argued that population
sizes were limited by chronically low levels of larval settlement (Williams, 1980,
Doherty, 1981). Subsequently, a flurry of studies documented apparent cases of such
recruitment limitation (e.g. Doherty, 1982, 1983, Victor, 1983, 1986, Doherty and
Fowler, 1994ab, review by Doherty and Williams, 1988). However, many of these
studies suffered from methodological limitations (Caley et al., 1996, Can, 1998,
Forrester, 1998, Hixon, 1998). Furthermore, a series of well-executed studies did not
support the central tenet of the recruitment limitation model that populations were
undersaturated (e.g. Jones, 1987a, 1990, Forrester, 1990). In light of this new
evidence, researchers more thoroughly explored other potentially important factors,
most notably predation (review by Hixon, 1991).
Most recently, reef-fish ecologists have largely shifted their focus away from
single-process explanations of population and community dynamics in favor of a
3
pluralistic view that recognizes the importance of multiple processes (e.g. Hixon,
1991, Jones, 1991, Caley et al., 1996, Schmitt and Holbrook, 1999b). This change has
been fueled in part by the observation that factors that are important in one place or
time seem relatively unimportant in another even for the same species. Several
examples illustrate the potential for the relative importance of a given factor to vary in
space including studies of post-settlement mortality of the damselfish Pomacentrus
moluccensis (Doherty and Fowler, 1 994a,b vs. Beukers and Jones, 1997) and the
wrasse Thalassoma bfasciatum (Victor, 1986 vs. Hunt von Herbing and Hunte, 1991,
Tupper and Hunte, 1994, Caselle, 1999). Variability in time is best exemplified by
researchers that repeat the same or similar studies over subsequent field seasons. For
example, Booth (1995) found that group size and probability of survival to adulthood
were positively related one year and showed no relationship another year for the
damselfish Dascyllus albisella. The lesson learned from observations such as these is
that a single simple model is insufficient to explain population and community
dynamics on coral reefs.
In the studies below, I have combined methods to explore the roles of
competition, recruitment and predation in an attempt to more thoroughly understand
the population dynamics of coral-reef fish. By maintaining a multifactorial
perspective, I have found that populations are driven by a suite of factors that vary in
importance depending on a host of factors including density, size-structure,
recruitment rate, and the presence of predators.
4
In Chapter 2, I described the social organization of populations of fairy basslets
(Gramma loreto) in the Bahamas. Basslets live on the undersides of caves and coralreef ledges where they feed on zooplankton while swimming upside-down. Within
basslet populations, fish are arranged according to size, with the largest individuals
towards the front and progressively smaller individuals towards the back. Larger fish
maintain this size segregation by forcing smaller fish to the back, which reduces the
feeding rate of smaller fish.
In Chapter 3, I examined how the rate of recruitment of new basslets affected
population dynamics. By experimentally manipulating recruit density, I determined
that higher recruitment did not lead to an increase in the subsequent population density
because density-dependent mortality dampened variability among populations.
Density-dependent mortality was not correlated with increases in the intensity of
within-species competition. Using automated time-lapse video, I examined whether
predators were responsible for density dependence by undergoing either an aggregative
or type 3 functional response. I found the predators were more common in
populations with higher densities of recruits and that when present, these predators
spent a greater proportion of time hunting in these populations. These results
implicated predators as the cause of density dependence, which contributed to
population regulation. I observed further evidence for population regulation in a longterm (two generation) time series of basslet population dynamics, which showed
regular annual and inter-annual cycles of abundance.
5
I explored the demographic consequences of variation in adult density in
Chapter 4. I found that new recruits suffered from intraspecific competition with
adults. Competition likely contributed to higher mortality rates by making new
recruits more susceptible to predators. Hence intraspecific competition also led to
density-dependent mortality, which may have helped regulate these populations.
In Chapter 5, I examined the effects of recruit density and predator presence on
the early post-settlement demography of coral-reef fishes on the Great Barrier Reef,
Australia. Predators both decreased recruitment and increased post-recruitment
mortality for every species that I studied. However, the magnitude of these effects
varied widely among species. The most common species in this study suffered from
density-dependent mortality while another abundant species did not.
The common thread linking each of these studies is that interactions both
within and among species drive and regulate population and community dynamics of
fishes on coral reefs. Predators played a key role in post-settlement modification of
local abundance in both the Bahamas and Australia, although the mechanisms by
which mortality rates changed differed among studies and species. These studies
contribute to a growing awareness of the multifactorial nature of population and
conmiunity dynamics of marine fishes.
Chapter 2: Mechanisms and Individual Consequences of
Intraspecific Competition in a Coral-reef Fish
Abstract
Species of coral-reef fish that exhibit dominance hierarchies provide
opportunities for experimental studies of intraspecific competition within discrete
social groups. The fairy basslet, Gramma loreto (Grarnmatidae), lives in dominance
hierarchies that occupy the undersides of open reef ledges in the Caribbean region.
Each hierarchy is maintained by aggression between size classes such that larger fish
occupy prime plankton-feeding positions closer to the outer edge of the ledge. We
conducted a removal experiment in the central Bahamas to determine the role of larger
fish in maintaining the hierarchy and the resultant consequences to smaller fish. When
larger fish were removed, smaller individuals quickly occupied these prime feeding
positions and were the recipients of less aggression compared to controls. As a result,
the average feeding rates of smaller fish were more than 60% higher in aggregations in
which larger fish had been removed. Differences in feeding rates were the result of
two types of competitive effects: between-position and within-position. The betweenposition effect was the result of differential feeding rates associated with different
feeding positions within an aggregation. The within-position effect was due to
interactions within a given feeding position. Although both effects strongly influenced
basslet feeding rate, the magnitude of the within-position effect was roughly three
times that of the between position effect. Together, these two components of
competition may affect demographic rates and ultimately contribute to local
population regulation.
Introduction
The role of competition for limiting resources in the ecology of coral-reef
fishes is controversial, and the prevailing view on the importance of competition has
shifted historically (reviews by Ebeling and Hixon, 1991, Jones, 1991). Before the
mid-i 970s most reef fish ecologists accepted the then dominant view of terrestrial
ecologists that competition was ubiquitous and substantial (e.g., Smith and Tyler,
1972). By the mid-i 980s, this conventional wisdom was overturned and the paradigm
became that competition was unimportant. This view, the recruitment limitation
hypothesis, asserted that larval supply is so low that populations rarely reach levels
where resources become limiting (e.g., Doherty, 1981, Doherty and Williams, 1988).
Reviewing the empirical evidence, Jones (1991) noted that, even for territorial or
obviously aggressive reef fishes, the role of interference competition in limiting adult
numbers or structuring populations was uncertain. He concluded that the major effect
of competition in general is to limit individual growth rates (Jones 199 i).
In the past decade, evidence for ecological consequences of competition in reef
fishes has increased, but has mostly involved territorial species. For example,
Robertson (1996) demonstrated experimentally that interspecific competition affects
8
the abundance and habitat use of territorial Caribbean damselfishes. Unlike
competition between species, intraspecific competition may be most pronounced when
individuals form social groups. Although membership in an aggregation may enhance
feeding success and predator avoidance, intraspecific competition between group
members for food or other resources may partially offset these benefits (Betram, 1978,
Rubenstein, 1978, Mange!, 1990, Pitcher, 1993). Intraspecific competition may be
manifest as size or dominance hierarchies, whereby the largest or most aggressive
individuals utilize a greater proportion of a resource than smaller or subordinate
individuals. Among reef fishes, dominance hierarchies have been documented
primarily in several species of damselfish (e.g. Coates, 1980, Doherty, 1982, Shulman,
1985, Forrester, 1991, Booth, 1995).
Competitive hierarchies can occur when access to food resources is determined
by relative position within a group. Among planktivorous coral reef fishes,
individuals may maintain relatively fixed positions in currents and feed on passing
plankton (Hobson, 1978, Coates, 1980, Booth, 1991, Forrester, 1991, Hobson, 1991).
This pattern is often explained in terms of predator avoidance, where feeding position
is based on an individual's ability to reach shelter quickly as a predator approaches.
Larger fish swim faster, so they can feed farther from the reef with no increase in the
time required to reach shelter relative to smaller, slower fish that remain closer to the
reef (Hobson, 1978, 1991).
The fairy basslet (Gramma loreto, family Granimatidae) is a common coral
reef fish in the Caribbean and Bahamas (Bohlke, 1993). Basslets range in size from
about 1.0 cm standard length (SL) at settlement to large adults about 7 cm SL. G.
loreto are typically found oriented upside-down on the ceilings of open caves and
ledges, where they feed on passing zooplankton (Randall, 1967, Luckhurst, 1977,
Bohike, 1993). This species occurs in size-structured aggregations, with the largest
individuals near the front of an aggregation and progressively smaller individuals
toward the back (Freeman, 1983). Within aggregations, the largest individuals chase
smaller individuals, and each fish tends to remain within a restricted area (Freeman,
1983).
The goal of this study was to examine the competitive mechanisms that
maintain size hierarchies, and the consequences of these hierarchies for small fish
within Gramma loreto aggregations. Specifically, we examined the size structure of
aggregations and the role of aggressive interactions in maintaining a size-based
dominance hierarchy. We hypothesized that feeding position was related to feeding
rate, whereby individuals closer to the front of an aggregation have first access to
planktonic food, depleting this resource and leading to depressed feeding rates for
individuals toward the back of an aggregation. To test this hypothesis, we
experimentally measured how feeding behavior of smaller individuals within an
aggregation was affected by the removal of larger individuals. We measured two types
of competitive effects: between-position and within-position. The between-position
effect is manifest as differential feeding rates associated with different feeding
positions within an aggregation. The within-position effect is due to interactions
within a given feeding position. We assessed the relative magnitude of these two
10
effects of competition and then determined the net costs to smaller individuals in terms
of feeding rate.
Methods
This study was conducted during August and September 1994 in an area of
continuous coral reef (6-10 m deep) in the Exuma Keys, Bahamas, near the Caribbean
Marine Research Station on Lee Stocking Island. Fourteen ledges (rock overhangs)
were chosen based on their relatively large size, their isolation from other ledges, and
the presence of Gramma loreto aggregations. Ledges were 1 to 2 m deep, ledge
surface area ranged from 1.4 to 10.4 m2 and G. loreto aggregation size ranged from 17
to 71 individuals. Aggregation size was strongly related to ledge area (Webster,
unpublished data). Because these ledges were not identical in terms of their area, size
distributions or densities of fish, any patterns that were consistent across ledges were
likely to be fairly general for a wide range of ledges.
Fish Size and Feeding Position
On each ledge, we visually assigned each fish to a 1-cm SL size class for a total
of 7 size classes (1.0-1.9 cm, 2.0-2.9 cm, etc.). For our first survey, we used 0.5 cm
size classes (1.0-1.4 cm, 1.5-1.9 cm, etc.). Periodic tests of the accuracy of visual
censuses were conducted by estimating the size and then capturing individual fish. In
11
every case, these fish could be estimated accurately within 0.5 cm of their actual
length.
On each ledge, the feeding position of each Gramma loreto was measured on
three consecutive days. Absolute feeding position was measured as the distance
between a fish and the front of a ledge. Absolute position thus ranged from 0, at the
front of the ledge, to 0.8-1.7 m (the range observed) at the back of the ledge (Fig. 2.1).
We standardized absolute position by calculating relative feeding position as 1 -
(absolute position / ledge depth). This permitted us to make comparisons among
ledges that were not influenced by differences in ledge size or shape. For example, a
fish at the back of a small ledge could have had the same absolute position as a fish
near the middle of a large ledge. The relative positions of these two fish better reflect
their positions with respect to the dominance hierarchy at their home ledge.
Removal Experiment
To examine the effects of larger Gramma loreto on smaller individuals, we
conducted a controlled removal of larger fish. Each ledge was randomly assigned to
one of two treatments: unmanipulated control (N=7 ledges) and removal (N=7 ledges).
On removal ledges, all fairy basslets 4-cm standard length or larger were removed by
divers using hand nets and the anaesthetic quinaldine. To maintain statistical
12
\
\ Front
Ledge
Figure 2.1. Feeding positions of Gramma loreto on a typical reef ledge. Relative
position = 1 - (absolute position / ledge depth). Therefore, relative position equals 1 at
the front of a ledge and 0 at the back.
independence, ledges were treated as experimental units; therefore, throughout the
analysis we combined multiple measurements taken from a given ledge into a single
mean response for that ledge. The statistical comparisons throughout the analysis
were directional (except when comparing regression slopes between treatments), thus
we examined one-tailed p-values. However, for completeness, we also calculated twotailed p-values. Using one-tailed tests affected only one of our conclusions: that
regarding the location of aggressive interactions (see Results). During the experiment,
13
we made comparative observations of aggressive interactions, feeding positions and
feeding rates.
Aggressive Interactions
Aggressive interactions were observed on each ledge for three days. Each day,
all chases between individuals on each ledge were noted during a six-minute
observation period conducted during midday. We recorded absolute position at the
initiation of the interaction as well as the size class of the aggressor (individual
chasing) and the recipient (individual being chased). We used these estimates to
compare how the relative frequency of aggressive interactions varied with fish size and
experimental treatment, and to determine whether the chase frequency rate of small
fish (1, 2, and 3 cm SL) varied on control and fish-removal ledges.
To determine whether smaller fish were chased more often when they were
closer to the front of a ledge, we calculated relative position chased for size classes 2,
3, 4, and 5 cm SL for each control ledge (size classes 1, 6, and 7 cm SL were not used
due to small sample sizes; N 1, 3 and 0 respectively). This value was then subtracted
from the average feeding position (from the initial survey) for these size classes on
each control ledge. Values from each size class were then averaged for each ledge,
providing a single measurement describing where individuals were chased relative to
where they were typically found. Values greater than zero indicated that fish were
chased more frequently than average when they were closer to the front of a ledge.
14
Feeding Position
Following the removal of larger basslets, the absolute feeding position of all
remaining fish on each ledge was again measured on three subsequent dates. We
converted these measurements to the average relative feeding position for each size
class for each ledge. Pre-removal feeding position was then subtracted from postremoval position for size classes 1, 2 and 3 cm SL. These values were then averaged,
providing a single value describing any change in feeding position for each ledge.
Feeding Rate
To examine the effects of larger fish on the feeding rates of smaller fish, we
compared feeding rates of small fish on control and removal ledges. Focal fish
feeding rates (sensu Forrester, 1991) were observed for 3-cm SL basslets on each ledge
on three days. Feeding was defined as bites directed at planktonic organisms in the
water colunm. On each occasion, feeding rate was measured for four individuals
distributed throughout each ledge (for a total of 12 observations per ledge).
Individuals were chosen to represent the full range of possible feeding positions. Each
ledge was roughly divided into four sections (front, front-mid, back-mid, and back),
and one individual was chosen haphazardly from each of these four sections for
observation. When no individuals were present in a given section, the closest
15
individual in a neighboring section was observed. Once an individual was chosen, its
absolute position was recorded, and a diver observed its feeding frequency for 1-2
minutes.
To combine individual feeding rate measurements within a given ledge into a
single parameter, we fit simple linear regression models (feeding rate as a function of
relative position) separately for each ledge. Because there was a positive linear
relationship between feeding position and feeding rate, a simple ledge average would
not accurately describe all feeding rates on a given ledge. Therefore, we used the
slopes as our parameter to test whether the relationship between feeding rate and
relative position varied between treatments, i.e., an interactive treatment effect. Note
that if there were no differences in slope, a difference in the intercept would indicate
an additive treatment effect.
We then used the linear regression models to estimate feeding rates for each
treatment. From each regression model, we calculated point estimates of feeding rate
at various feeding positions. The seven resulting estimates of feeding rate per
treatment (one from each ledge) were then used to estimate mean feeding rate and
variance for a given feeding position. Note that the confidence intervals reported are
based on the variance in our point estimates, not the variance in individual
measurements of feeding rate at that position. By using average regression parameters,
we constructed linear estimates of the relationship between feeding rate and feeding
position for control and removal ledges.
16
Results
Fish Size and Feeding Position
There was a strong relationship between fish size and relative feeding position
on a ledge (Fig. 2.2). Individuals larger than approximately 5 cm SL were more likely
to be found near the front of the ledge. Below 5 cm, feeding position decreased
dramatically with decreasing individual size.
Removal Experiment
Aggressive Interactions
Aggressive interactions were strongly size-dependent. During every observed
aggressive interaction, the aggressor was the same size or larger than the recipient
(Fig. 2.3a). Virtually all aggression was directed toward fish of the same size as the
aggressor or of the next smaller size class. Nearly all aggressive interactions were
directed toward fish smaller than 5 cm SL; the majority were toward 3-cm and 4-cm
fish. Three-cm to 6-cm fish were the most frequent aggressors. Between 4 and 5 cm
SL, fish shifted from being primarily recipients to being primarily aggressors (Fig.
2.3b).
17
1.0
Front
'4
:08
0.2
Back
1
2
3
4
5
6
7
Size Class (cm SL)
Figure 2.2. The relative feeding position (X ± SE) of each size class of Gramma
loreto. Error bars are based on mean position measurements from each ledge (N = 14
ledges).
Aggressive interactions tended to occur when fish were further forward on a
ledge than their average feeding position (Fig. 2.4). While not statistically significant
(one tailed paired t-test: t61 .80, p=O.O63), this trend was consistent for all size
classes.
18
The frequency at which 3-cm SL fish received aggression was significantly
higher on control ledges than on ledges where larger fish had been removed (Fig. 2.5,
one-tailed t-test: t123.42, p0.003). The 3-cm fish were recipients of aggression more
than twice as frequently on control ledges than on removal ledges. There was no
difference between treatments for 1-cm or 2-cm fish (one-tailed t-test: t12=-0.74,
p=O.23 for 1 cm fish and t12=-O.46, p=O.32 for 2 cm fish).
Feeding Position
Fish 3 cm SL and smaller moved forward on ledges following the removal of larger
fish (Fig. 2.6a, one-tailed paired t-test: t63.55, p = 0.006). On average, the fish
remaining on removal ledges moved forward 11% of the ledge depth (95% CI: 3
to 17%, N=7); 3-cm fish, in particular, moved forward 14% (95% CI: 9% to 23%,
N=7). All remaining fish continued to maintain distinct size segregation (Fig. 2.6a).
There was no evidence of any movement forward for fish 3 cm and smaller on control
ledges (Fig. 2.6b, one-tailed paired t-test: t6=1 .27, p = 0.13).
19
(a)
1
u Aggressor
(b)
N=0
U Recipient
rID
'-3
N=72
(.)
cd
N=55
I
N=127
I
N=4
'1
I
1
2
3
4
5
6
Recipient Size Class
(cm SL)
7
0.1
I _ I
0.2 0.3 0.4 0.5
Relative Frequency
Figure 2.3. Aggression between size classes of Gramma loreto on control ledges. (a)
Each plot is the relative frequency of N chases by a single size class (aggressor)
directed toward each size class (recipient). For each plot the total area of the bars
equals one (except for size class 1, which was never observed as an aggressor). (b) The
relative frequency at which each size class acted as an aggressor and as a recipient of
aggression (X + SE, N=7 ledges each).
20
1.0
Front
C
.,-
0
.a)
a)
iI
0.7
-.- Position chased
a)
Average position
Back
2
3
4
5
Size Class (cm SL)
Figure 2.4. The average relative feeding position and relative position when chased
for each size class of Gramma loreto on control ledges (X ± SE, N=7 ledges each).
Points are offset to clarify error bars.
21
p=O.003
control removal
,-
0.10
p=0.32
r
rfj
0
0.05
pO.23
:ixii
2
3
Size Class (cm SL)
Figure 2.5. The frequency of aggressive interactions directed toward smaller size
classes of Gramma loreto on control and removal ledges (X + SE, N=7 ledges each).
22
1.0
(a) Removal
Front
0.8
0.6
0.4
-o-- Post-removal
-.-- Pre-removal
0
..
rd)
0
V
Back
1.0
(b) Control
Front
I.
I,
j4
1
2
3
Size Class (cm SL)
Figure 2.6. The relative feeding position (X ± SE, N=7 ledges each) of smaller size
classes of Gramma loreto before and after removal of larger fish on (a) removal ledges
versus (b) unmanipulated control ledges. The points are offset to clarify error bars.
23
Feeding Rate
The slope of the relationship between feeding rate and relative feeding position
differed between control and removal ledges (two-tailed t-test: t12=2.89, p=O.Ol 4).
The slope estimates were positive for all aggregations, indicating that feeding rate
invariably increased with distance toward the front of the ledge. For both treatments,
average slope values were significantly larger than zero (one-tailed t-test: t6=8.42,
p<O.0001 for control and t6=13.36, p<O.0001 for removal).
We used the regression results to estimate feeding rate for 3-cm fish in each
treatment. We estimated the between-position effect of competition on feeding rate by
calculating the change in feeding rate associated with movement forward on a ledge.
By moving forward 14% of the ledge depth (as was observed for 3-cm fish), the
average feeding rate of a 3-cm fish increased an estimated 0.62 bites per minute (Fig.
2.7, 95% CI: 0.28 to 1.22, N=7). We also used regression point estimates to evaluate
the within-position effect by calculating the difference in feeding rate between control
and removal ledges. At the average post-removal feeding position of 3-cm fish on
removal ledges, feeding rate was estimated to be 2.12 bites per minute greater on
removal ledges than on control ledges (Fig. 2.7, 95% CI: 1.17 to 3.07, N=14).
Considering both increased feeding rates within a position (2.12 bites/minute), and
increased feeding rate between positions (0.62 bites/minute), an average 3-cm fish on a
removal ledge fed an estimated 2.74 bites per minute (95% CI: 1.86 to 3.62 bites per
minute, N=14) or 63% (95% CI: 43 to 84%, N14) more frequently than an average 3cm fish on a control ledge (Fig. 2.7).
24
Discussion
Dominance hierarchies provide opportunities to examine experimentally the
mechanisms and consequences of intraspecific competition in reef fish (e.g. Coates,
1980, Forrester, 1991, Booth, 1995). We measured the magnitude of intraspecific
competition in basslets directly in terms of effects on feeding rate, as well as the
relative contribution of two different components of competition. Reduced feeding
rate of smaller fish was caused by larger, dominant individuals. Similar patterns may
be widespread in fishes where dominance is often function of size and related to
foraging success (e.g. Coates, 1980, Koebele, 1985, Forrester, 1991, Robertson, 1998).
For example, Coates (1980) and Forrester (1991) found that the feeding rate of a
damselfish (Dacyllus aruanus) was partially determined by individual position within
an aggregation, which in turn was related to individual size. The largest, most
dominant individuals tended to remain at the up-current edge of the aggregation,
presumably acquiring first access to planktonic food. Koebele (1985) observed that
dominant cichlids consumed a greater proportion of available prey, thereby
exploitatively depressing the food supply of subordinates. Further, dominant
individuals behaviorally inhibited the feeding rate of subordinates. Jenkins (1969)
observed that, like basslets, feeding position among stream salmonids was determined
by social dominance. When dominant individuals were removed, subordinate
individuals quickly occupied the vacant feeding positions.
25
8
Post-removal
-
,_6
63%:
.E4
42%
14%
0E
2
0
0 Control
I
0.0
Back
I
0.2
0.4
I
I
0.6
tO.8 t
Pre-removal
1.0
Front
Post-Removal
Relative Feeding Position
Figure 2.7. The average change in feeding position and difference in feeding rate for
3-cm Gramma loreto, after experimental removals of larger fish, relative to
unmanipulated controls. Control and removal regression lines are each based on the
average parameters from seven aggregations (for control ledges feeding rate = 1.36 +
6.26 * [feeding position]; for removal ledges feeding rate = 1.05 + 4.28 * [feeding
position]). On average, 3-cm fish were 14% closer to the front of a ledge after the
removal of larger fish. Moving this distance on a control ledge is estimated to have
resulted in a 14% increase in feeding rate (between-position effect). However, at the
mean post-removal position, individuals on removal ledges were estimated to feed
42% more frequently than on control ledges (within-position effect). The net result is
an average increase of 63% in the feeding rate of 3-cm fish on ledges where larger fish
were removed.
26
Within fairy basslet aggregations, we found a strong relationship between
individual size and feeding position on a ledge: larger fish were closer to the front of
the ledge, where they apparently had first access to passing planktonic food. Our
results indicate that aggressive interactions maintained this relationship through a rigid
dominance hierarchy. Consequently, smaller fish were prevented from moving
forward, thus reducing crowding at a given feeding position on a ledge. However,
individuals larger than 4 cm SL were typically at the front of the ledge. The range of
4-5 cm SL appeared to be a transitional size, where fish switched from primarily
receiving aggression to being aggressors. This is roughly the size at which individuals
become reproductively mature (Asoh, 1 992b). Therefore, it appears that aggressive
interactions prevent individuals from gaining access to the front of the ledge until they
are adults.
We observed a decrease in the frequency of aggressive interactions after larger
fish were experimentally removed. However, a decrease was evident only for 3-cm
fish, not for 1-cm or 2-cm fish. This is consistent with observations that individuals
usually chase fish of equal size or one size class smaller. When all fish were present,
3-cm, 4-cm and 5-cm fish were the primary aggressors towards 3-cm fish. Removals
of fish 4 cm and larger eliminated the between-size-class component of aggressive
interactions, leaving only within-size-class effects. As a result, 3-cm fish were chased
far less frequently where larger fish were removed. The frequency at which 1-cm and
2-cm fish were chased did not differ between control and removal ledges because the
size classes most frequently aggressive towards these individuals (2 and 3 cm,
27
respectively) remained after the removal of 4-cm and larger fish.
After the removal of larger fish, smaller fish moved toward the front of the
ledge, a pattern that was not observed on control ledges. The removal of larger fish
facilitated forward movement by eliminating between-size-class aggression directed
towards 3-cm fish. This shift, in turn, permitted the forward movement of 1-cm and 2cm fish behind the 3-cm fish. Size segregation was maintained for these individuals
because the between-size-class component of competition was not reduced for 1-cm
and 2-cm fish. This pattern further supports the hypothesis that an individual's
position on a ledge is determined by aggressive interactions between size classes.
The behavioral interactions observed between fairy basslets imply that
maintaining a position near the front of a ledge affords some advantage and that
crowding at a given position results in a disadvantage. Our results implicate
intraspecific competition for feeding positions as the driving force behind these
patterns. Intraspecific competition in fairy basslet aggregations is probably a
consequence of their feeding mode. Basslets maintain relatively fixed positions under
ledges and feed on passing plankton (Randall, 1967, Luckhurst, 1977, Bohlke, 1993).
Water masses containing relatively abundant zooplankters are likely to first pass the
front of a ledge via surge or tidal currents in the same way that they first pass reef
edges (Hobson, 1978, 1991). As the water moves toward the back of the ledge,
zooplankters are probably depleted by the largest basslets (see Coates, 1980, Forrester,
1991). This situation likely creates a gradient of decreased food abundance towards
the back of the ledge. Consistent with our results, such a pattern would create an
28
advantage for individuals near the front of the ledge and an incentive to prevent others
from moving forward.
We measured two effects of intraspecific competition, between and within
feeding positions. The between-position effect is the result of differential feeding rates
based on an individual's distance from the front of a ledge. Such an effect is likely a
result of depletion of food by larger fish that aggressively deny smaller fish access to
the front of a ledge. The within-position effect is due to interactions between larger
fish and smaller fish at a given position on a ledge. Thus both between-position and
within-position effects can involve both non-aggressive exploitative and aggressive
interference competition (sensu Schoener, 1983).
Although both components strongly affected basslet feeding rate, the
magnitude of the within-position effect was roughly three times that of between-
position effect. This result indicates that the competitive effect of larger fish is due
mostly to aggressively reducing the feeding rates of smaller fish at a given position
rather than preventing smaller fish from moving their feeding positions forward on a
ledge. However, smaller fish are not likely to be able to reduce the within-position
effect, whereas they may be able to reduce the between-position effect. A reduction in
the within-position effect would require a reduction in the number of larger fish
toward the front of a ledge. A smaller fish could accomplish this only by emigrating to
a ledge with a lower density of larger fish. However, the habitat requirements of
basslets are quite specific (Randall, 1967, Luckhurst, 1977, Bohlke, 1993) and suitable
habitat is patchy. Consequently, emigrating individuals would need to cross
29
considerable distances to find suitable habitat of uncertain quality, all the while being
relatively vulnerable to predation. In fact, emigration is rare (Webster, unpublished
data). It appears to be more advantageous for individuals to remain on a ledge in the
presence of strong competition than to risk predation and uncertain habitat quality
associated with emigration.
Unlike the within-position effect, individual basslets may reduce the betweenposition effect simply by moving toward the front of a ledge. Such movement
explains our behavioral observations. It appears that smaller fish consistently initiated
movements toward the front of a ledge, thereby gaining access to greater food
availability. At the same time, larger fish prevented this movement, thereby
monopolizing passing prey. It is unclear whether fish simply move forward as they
grow larger or if fish that maintain better feeding positions grow faster. Growth and
change in position are likely a combination of these two processes.
The effects of intraspecific competition on small basslet feeding rates were
large: in the absence of both components of intraspecific competition, the average
feeding rate of a 3-cm basslet was over 60% higher. Ultimately, such a strong effect
may regulate fairy basslet populations by leading to density-dependent changes in
demographic rates. Strong intraspecific competition for food can indirectly regulate
adult populations of damselfish by affecting growth rate and maturation time (Jones,
1987a, 1990, Forrester, 1990, Jones and Hixon in
prep.).
Indirect density regulation
could occur in fairy basslets if larger individuals negatively affect the rates at which
smaller fish grow and mature. Intense competition could also lead directly to density-
30
dependent changes in demographic rates by influencing immigration and emigration,
or by increasing susceptibility to predators. We are currently investigating such
possibilities.
31
Chapter 3: Temporal Density Dependence and Population
Regulation in a Marine Fish
Main Text
Accelerated loss of species and populations worldwide has led to renewed
focus on understanding and conserving the natural mechanisms regulating populations.
Losses of biodiversity are particularly severe on coral reefs, which are the ocean's
most diverse ecosystems (Shenk et al., 1998). Approximately 27% of coral reefs are
already degraded worldwide, and an additional 32% are at high risk of degradation
during the next three decades (Wilkinson, 2000). Ultimately, species persistence
depends on mechanisms that regulate populations by causing demographic density
dependence, the negative feedback loops necessary to bound population fluctuations
above zero (Murdoch, 1994, Turchin, 1995). One likely regulating process in reef fish
is density-dependent mortality, whereby the per capita death rate increases with
population size. Although there is ample evidence for spatial density dependence
based on comparisons of mortality rates of multiple local populations at the same time
(Hixon and Webster, in press), population regulation requires temporal density
dependence within a single population through multiple generations (Stewart-Oaten
and Murdoch, 1990, Myers and Rothman, 1995). Here, I provide the first experimental
demonstration of strong temporal density dependence in a coral-reef fish, as well as
evidence for the mechanism causing density dependence.
32
The fairy basslet (Gramma loreto) is a common planktivorous fish in the
Caribbean and Bahamas. Gramma live on the ceilings of reef caves and ledges in local
populations that range in size from about ten to more than a hundred individuals.
Movement between isolated aggregations in the Bahamas is sufficiently rare that each
aggregation can be considered a separate local population (approximately 0.7% of
tagged residents emigrated per month during the experiment, indicating that site
fidelity was extremely high). I used 16 replicate populations to determine whether any
demographic rates were spatially density-dependent by comparing unmanipulated
populations with populations in which I experimentally increased recruitment. All
individuals in each population were tagged subcutaneously using elastomer (Buckley
et al., 1994, Beukers et al., 1995) and demographic rates were monitored over 50 days.
When examined as total rates (per area rather than per capita see Hixon and Webster,
in press), natural recruitment and immigration were independent of density
(Recruitment: paired T7 = 0.42, one-sided P = 0.35; immigration: paired
T7 =
0.13,
one-sided P = 0.45.). In contrast, per capita mortality and emigration rates were
significantly density-dependent (Fig. 3.1A, B). Differences in mortality between
unmanipulated and experimentally increased populations were 5.9 times greater than
differences in emigration, indicating that mortality was the major source of density
dependence.
Density-dependent mortality could have been an artifact of the experimental
design if either transplanted fish were more prone to mortality or augmented
populations had higher mortality because they had a greater proportion of small fish
33
than control ledges. However, four lines of evidence argue that density-dependent
mortality was not an artifact: (i) a transplant-effect experiment revealed no increase in
mortality rates for transplanted relative to resident fish at the same density
(T57
= 0.07,
one-sided P = 0.47), (ii) the proportion of transplanted fish in augmented populations
did not change between the beginning of the experiment in June 1998, August of 1998,
and spring of 1999
(F2,21
= 0.70, P = 0.51) indicating that these fish did not suffer
disproportionately from predation, (iii) mortality rates tended to increase for prior
resident fish in augmented populations (paired
T7
= 1.44; one-sided P = 0.096)
indicating that the negative effects of density extended beyond transplanted fish, and
(iv) the observational pattern in 1999/2000 was identical to the experimental pattern
the previous year except that natural recruitment was relatively high on reefs that were
previously used as controls (Fig. 3.2, see below).
What mechanism resulted in increased mortality at high densities? Based on
previous evidence, the candidate processes were within-species competition (Freeman,
1983, Webster and Hixon, 2000) or predation (Hixon, 1991, Hixon and Carr, 1997).
Competition was discounted because neither of two potential manifestations occurred
at high densities (at higher densities, aggression rates did not increase
(T7 =
0.17, one-
sided P = 0.43) and growth rates did not decrease (T7 = 0.05, one-sided P = 0.48). I
therefore designed an additional experiment to determine whether predators induced
density dependence by behaviorally responding to different densities of Gramma.
Using automated time-lapse video, I observed that predators, primarily the groupers
Cephalopholisfulva and C. cruentata, and the trumpetfish Aulostomus maculatus,
34
spent significantly more time in populations with experimentally elevated recruitment
(Fig. 3.1 C). When present, predators also spent a significantly greater proportion of
time hunting in these populations (Fig. 3.1D). Together, these observations implicated
predators as the cause of spatial density dependence over the relatively short time
period of this experiment.
0.012
0.10
O.08c
A
0.008
8)
0.06
0.04
0.004
(0
(0
a-
0.0 12
B
(0
0
0.008
0.004
ii ii
0.02
0
0.000
0.00
E0
0.5
a.
0.3
04
D
0.2
0.1
0 000
0.0
Control
Control Increase
Increase
Treatment
Figure. 3.1 Summary of demographic rates and predator behavior. Daily per capita
rates (+SE) of(a) emigration (paired T7 = 2.12, one-sided P = 0.036) and (b) mortality
aired T7 = 2.12, one-sided P = 0.03 6) of Gramma in control and density-increase
populations (n = 8 each) over 50 days. Proportion of time (+SE) that predators were
(c) present (paired T8 = 2.01, one-sided P = 0.04) and (d) hunting while present (paired
T8 = 3.01, one-sided P = 0.008) in control and density-increase populations (n 9
each).
By examining fluctuations in these populations over multiple generations,
patterns emerged that indicated temporal regulation. Over three years
generations
roughly 2
Gramma density showed a consistent annual cycle in which density
35
increased in late spring and summer with the arrival of newly settling larvae and then
declined gradually until reaching an annual minimum by the beginning of the
following spring (Fig. 3.2). Prior to any experimental manipulation, 16 populations
tracked each other closely. Densities diverged sharply when I experimentally increased
recruitment in half of the populations in 1998. Subsequently, density declined steadily
in the augmented populations resulting in convergence with control populations during
the ensuing months. By the following spring, when all fish that recruited during the
previous summer were large enough to be reproductively mature (Asoh, 1 992a), there
was no difference in density between augmented and control populations (Test for
differences in density in spring 1999:
T7 =
0.48, two-sided P = 0.65). Since Gramma
spawn in spring and early summer (Asoh, 1 992a), enhanced recruitment the previous
summer had no impact on either the density of spawning adults or, consequently,
reproductive output. In the spring of 1999, density naturally rose higher in populations
previously used as unmanipulated controls due to spatial variability in larval
recruitment. Nonetheless, just as in 1998, densities later converged until the two sets
of populations were again indistinguishable the following spring (Test for differences
in density in spring 2000: T5 = 0.07, two-sided P = 0.95.). The regularity of these
annual cycles is due in part to the seasonality of recruitment in the Bahamas. However,
density early each spring was virtually identical for both manipulated and control
populations both within years (stats
spring density among years:
F2,36
above)
and among years (Test for differences in
= 0.47, P = 0.63.). This offers compelling evidence
36
that these populations were subject to strong density dependence that regulated adult
population size over generations.
16
Increase
o Control
12
E
0
U,
C
aa,
4
o
4-
7-97
1-98
7-98
1-99
7-99
1-00
7-00
Time
Figure 3.2. Gramma density (±SE) in density-increase and unmanipulated control
populations (n 8 each) over three years. The dotted line in July 1998 represents
experimental enhancement of recruitment. Some dates include data from fewer than 8
populations in each treatment because all populations were not censused on all dates:
control n = 2 on 7/15/97 and 9/7/97, n = 5 on 5/1/98, and n = 6 on 5/1/00 and 6/10/00;
increase n = 3 on 7/15/97 and 9/7/97, n = 6 on 5/1/98, 5/1/00 and 6/10/00.
Evidence for density dependence comes primarily from two types of studies:
observational time series analyses and manipulative experiments. Time series analysis
tests for temporal density dependence statistically, but is both problematic
operationally (Shenk et al., 1998) and provides no causative mechanisms (Myers and
Rothman, 1995). In contrast, experiments allow determination of causal mechanisms,
37
but are typically spatial in design (Harrison and Cappuccino, 1995). This study
combined these approaches by experimentally demonstrating spatial density
dependence and its likely mechanism, while concurrently providing evidence for
temporal density dependence.
Any attempt by natural resource managers to ensure the long-term persistence
of populations must preserve mechanisms responsible for natural regulatory feedback
loops. Since population regulation of this fish species, and potentially many others,
appears to hinge on the maintenance of an intact food web, an ecosystem approach
may be necessary to meet conservation goals. Piscivores have an important regulatory
role in this and other systems (Hixon, 1991). Because piscivores are often primary
targets for fisheries exploitation (Pauly et al., 1998), efforts to conserve coral-reef
species may be in direct conflict with fishing practices, so that effective management
will require careful balancing of fishery and conservation goals.
Methods
Density Experiment
I identified 8 pairs of similar-sized reef ledges near the Caribbean Marine
Research Center, Bahamas, that ranged in population size from 8 to 55 individuals and
in area from 0.8 to 7.3 m2. One ledge in each pair was randomly assigned to an
unmanipulated control treatment. On the other ledge, I incrementally increased density
38
by transplanting small groups of tagged, recently-settled fish (S20 mm TL) daily for
two weeks to mimic a natural settlement pulse. I began monitoring demographic rates
in each population 24 hours after the final addition of recently-settled fish.
Recruitment was measured by searching for newly-settled, untagged fish in each
population every morning. I measured emigration by conducting weekly searches for
tagged fish within -40m of each experimental Gramma population. When emigrants
were found, they were invariably <3m away, so it is unlikely fish emigrated beyond the
1 Om search radius. I measured both net immigration and net mortality by recapturing
all fish in each population at the end of the experiment, and comparing that census to
my original, pre-manipulation census. Untagged fish that were present at the end of the
experiment, but had not recruited during the experiment, were considered immigrants.
Mortality was measured as the disappearance of tagged fish that could not be located
during emigration searches. Aggressive interactions were measured weekly as chases
between Gramma and were recorded for each population over a four-minute
observation period during each of four weeks. I measured growth by recapturing
tagged individuals at the end of the experiment.
Video Monitoring
I reestablished the treatments from the experiment in 1998 on 9 pairs of
populations, 4 in 1999 and 5 in 2000. Each population was filmed from morning to
evening over a two-day period with a digital camcorder in an underwater housing. The
39
camera filmed for 2 seconds every 30 seconds over an 8-10 hour period daily. The
video was then analyzed by identifying what proportion of time Gramma predators
were present. I also distinguished between predators that were simply present and
predators that appeared to be actively hunting Gramma. This distinction was based
largely on the orientation of the predators relative to Gramma: those predators
associated with the floor of the ledge or swimming past the ledge were scored as
present, while predators positioned on the ceiling of the ledge facing Gramma were
scored as present and hunting.
Generation Time
The three-year time series spanned approximately two generations based on a
standard life-table estimate of mean generation time of 1.44 years. Since population
growth via recruitment occurs during a relatively brief period each year, generation
time was estimated based on annual time intervals with all individuals reaching
reproductive maturity at age 1 (see Asoh 1992). Calculation of mean generation time
requires two sets of parameters: age-specific survivorship and relative fecundity.
Annual survivorship for each age class was estimated using empirically derived
growth rates and size-specific survivorship. The relative fecundity of females of
different ages is known to be directly related to body volume, which varies with the
cube of age-specific length.
40
Time Series
For each of the three years, the spring minimum population size was estimated
from adult densities in June. Size distributions in June were bimodal with no overlap
between modes, which corresponded to adults that recruited the previous year or
earlier (>35mm) and new recruits from that year (<35mm). Therefore, the density of
adults in June was likely to closely reflect the density in the aggregations prior to any
spring recruitment. I estimated May 1 as the pre-recruitment date because most of the
new recruits observed in June were <1 month post-recruitment based on their size.
While this technique does slightly underestimate pre-recruitment density, it was
unbiased among years and treatments.
41
Chapter 4: Regulatory Effects of Intraspecific Competition in a
Coral-reef Fish
Abstract
Within-species competition is inherently density-dependent, and thus it is likely to
have regulatory effects on local population dynamics. In this study, I examined how
intraspecific competition between adult and newly recruited individuals of a coral-reef
fish, the fairy basslet (Gramma loreto), affected the demography of new recruits. In an
initial experiment, I manipulated the density of resident adults and juveniles by
thinning some populations by 1/3 or 2/3, while leaving others unmanipulated. Once I
had established a range of resident densities, I transplanted a standard density of recent
recruits. The results suggested that residents negatively affected recruit survival, but
the results were equivocal due to high between-population variability. Therefore, I
conducted a second experiment in which I transplanted a cohort of new recruits to
local populations with three treatments of adult density: adults absent, average adult
density, and high adult density (2x average). By following the fate of the transplanted
recruits, I determined that recruit mortality increased as a function of adult density; in
high-density aggregations mortality rates were more than double those in aggregations
without adults. Increased mortality rates were correlated with two manifestations of
intraspecific competition: (1) adults forced new recruits to the back of aggregations
where (2) they experienced slower growth. Using automated time-lapse video, I
observed that predators were found most frequently toward the back of aggregations. I
42
conclude that competition ultimately increased predation risk for new recruits both
through depressed growth rates and by forcing recruits to overlap spatially with
predators. Thus, intraspecific competition between new recruits and adults influenced
the demography of subsequent generations in ways that promoted local population
regulation.
Introduction
Ecological studies of competition have largely focused on the consequences of
competition between species (e.g. reviews by Connell, 1983, Schoener, 1983). While
intraspecific competition has perhaps received less attention, its intensity is often
comparable to that of interspecific competition (Goldberg and Barton, 1992, Gurevitch
et al., 1992). Intraspecific competition is an inherently density-dependent process
whereby the magnitude of its negative effects tends to intensify at progressively higher
densities (Begon et al., 1996). Thus intraspecific competition can help regulate
populations if it is sufficiently strong that it translates into density-dependent changes
in the birth or death rate (see Cappuccino and Price, 1995).
Competition was once thought to be the predominant factor determining
community and population dynamics for fishes on coral reefs (e.g. Smith and Tyler,
1972, Roughgarden, 1974, Ehrlich, 1975, Smith, 1978). Recently, marine ecologists
have begun to explore other potentially important factors, notably recruitment (review
by Doherty, 1991) and predation (review by Hixon, 1991). Despite this shift in focus,
43
studies have continued to identify important competitive interactions between (e.g.
Jones, 1988, Robertson, 1996) and within (e.g. Jones, 1987a,b, 1988, Forrester, 1990,
Booth, 1995) species. The most commonly observed consequence of intraspecific
competition is reduced growth rates of small individuals (Doherty, 1982, 1983, Victor,
1986, Jones, 1987a,b, 1988, 1990, Forrester, 1990, Booth, 1995, review by Jones,
1991). For example, Jones (1987a,b, 1990) observed depressed growth due to
competition within aggregations of the damselfish Pomacentrus amboinensis that
tended to delay the maturation ofjuveniles and thus contributed to the regulation of
adult population size.
For fishes on coral reefs, the proximate source of mortality is likely to be
predation (Hixon, 1991). Therefore, density-dependent mortality due to intraspecific
competition in reef fishes is likely to be mediated via increased susceptibility to
predators. However, few studies have shown that intraspecific competition among
coral reef fish results in decreased survivorship. Forrester (1990) detected weak
density-dependent mortality in aggregations of the damselfish Dascyllus aruanus, but
it is unclear whether this was due to competition because adults actually enhanced the
survival of new recruits. Several recent studies by Schmitt and Holbrook have
explored the effects of density on survivorship of three species of damselfish (Schmitt
and Holbrook, 1996, 1 999a,b). While the mechanism responsible for decreased
survivorship at high densities is uncertain, their observation that mortality rates of new
recruits increased more rapidly in the presence of older conspecifics (Schmitt and
44
Holbrook, 1 999a) suggests that intraspecific competition was at least partly
responsible for density-dependent mortality.
Most studies of intraspecific competition in coral-reef fish have focused on
aggregating damselfish. This taxonomic specificity raises the question of whether
similar interactions occur in other families. The goal of this study was to explore how
intraspecific competition between adult and new recruit fairy basslets (Gramma loreto;
Grammatidae) affected the demography of new recruits. Specifically I asked four
questions: (1) Is there evidence of intraspecific competition between adult and new
recruits basslets? (2) Does the density of adults affect the recruitment of new
individuals? (3) Is survivorship of new recruits a function of adult density? (4) By
what mechanism does adult density affect recruit survival?
Methods
Study Species
Fairy basslets are common coral-reef fish found throughout the Caribbean and
the Bahamas (Randall, 1967, Bohlke, 1993). Basslets are small (<8 cm) planktivorous
fish that are usually found in aggregations along vertical drop-offs, in caves or under
ledges (Randall, 1967, Luckhurst and Luckhurst, 1978, Bohlke, 1993). Near the
Caribbean Marine Research Center in the Bahamas, basslets are found on discrete
ledges in aggregations that typically range from 10 to 70 fish. Isolated ledges
45
constitute local populations because movement between ledges is rare (Webster,
thesis). Under ledges, basslets typically swim inverted, with their ventrum aligned
with the ceiling. From this position, they feed diurnally on planktonic organisms that
flow past the ledge (Randall, 1967, Freeman, 1983, Bohike, 1993).
Basslets are social, living in strongly size-structured aggregations (Freeman,
1983, Webster and Hixon, 2000). Large individuals remain near the front of the ledge,
where they have first access to passing zooplankton prey, while smaller fish are forced
through aggressive interactions to remain near the back (Webster and Hixon, 2000).
For smaller fish, the consequence of segregation is a lower feeding rate. Feeding rate
is further depressed by the presence of larger fish, presumably due to food exploitation
by larger fish and reduced feeding time as a result of aggressive interactions.
Monitoring
I measured the density of a variable number of basslet populations in June
1998, 1999, and 2000. In each year, the size distribution of basslets was bimodal. The
larger mode (including fish 4-7 cm TL) was comprised of adults that settled the
previous year or earlier while the smaller mode (fish <4 cm) was comprised of fish
that had probably settled in May or June of that year.
1999 Experiment
In June 1999, I identified 15 isolated populations that are part of a continuous
coral reef near Lee Stocking Island in the Bahamas. These populations were in 5-7m
of water and they ranged in surface area from 1.5 to 4.1
m2.
To examine the effects of conspecifics on the survival of recent recruits, I
established a range of conspecific densities. I randomly assigned the populations to
one of three treatments: ambient density, 1/3 and 2/3 resident removal. In removal
populations, I removed individuals of all sizes based on their relative abundance to
maintain the pre-existing size distribution, which included both adults (>4 cm TL) and
juveniles (2-4 cm TL). Because initial density varied between populations, density did
not conform to three discrete treatments, but rather density was a continuous variable
that ranged from 0.76 to 14.2
fishlm2.
Once I had thinned resident conspecific density, I introduced a cohort
of recently-recruited (<2.0 cm) basslets. These fish were captured nearby, tagged
subcutaneously using elastomer (see Buckley et al., 1994, Beukers etal., 1995),
measured and released on experimental ledges. I added new fish each day until I
achieved a density of approximately 3.0 recruits/rn2, which was roughly the density of
new recruits present in these populations prior to any manipulation. At the same time,
I removed any similarly sized individuals that were already present on each ledge to
avoid confusing them with transplanted fish.
By June 26 the densities of transplanted fish had remained near target densities
for 24 hours, marking the beginning of the experiment. I censused the reefs every
week until August 14, for a total of 49 days. During each census, I recorded both the
47
total population size and the number of tagged recruits. I conducted emigration
searches for tagged recruits on all surrounding populations. Any new recruits that
appeared during the experiment were removed during each census to ensure that
differential recruitment between populations did not confound the results. Net per
capita mortality rate was calculated as the proportion of the original cohort that
disappeared from each experimental population, but was not located in emigration
searches.
2000 Experiment
In June 2000, I identified 20 additional isolated populations on continuous
coral reefs near Lee Stocking Island in the Bahamas. These ledges were in 5-7m of
water and they were larger than those used in 1999, ranging in surface area from 2.1 to
7.0m2. I excluded all populations occupying ledges with a surface area smaller than
2m2 because they are more variable than larger populations (Figure 4.1).
I randomly assigned five populations to each of four treatments: total removal,
adults absent, average adult density and high adult density. All resident adults were
removed from the total removal and adult absent treatments. I manipulated adult
densities in the remaining two treatments by adding or removing fish until I
established an intermediate density of 2
fishlm2 or
a high density of 4 fish/rn2. These
densities were chosen to span the range of densities that I observed during censuses in
48
12
10
A. June 1998
I
S
8
6
4
2
I.
S
I..'
I
0
("I
a
B. June 1999
12
10
>8
Cl)
C
a)
4
<0
:.
S
.
.
SI
.S
!.
C. June2000
12
10
8
.1
6
SI
4
2
U
I
I
5
$5
ir :.
2
4
6
8
Ledge area (m2)
Figure 4.1. The density of adult basslets (fish >4cm) versus the size of ledges in June
1998, 1999, and 2000. The dashed line at 2m2 represents an arbitrary division between
small, variable populations and larger, less-variable populations.
49
June 1998, 1999, and 2000 (Figure 4.1). In addition to manipulating adult density, I
also removed all recent recruits and juveniles from each population.
Once I established the adult density treatments, I introduced a cohort of
recently-recruited (<2.0 cm) basslets to all populations except those in the total
removal treatment. Total removal populations were used to determine whether
basslets require cues from conspecifics while settling. Basslets recruit at about 1.5 cm.
The recruits that I added were approximately 1-2 weeks post-settlement based on their
average size of 1.7 cm. These fish were captured nearby, tagged, measured and
released in experimental populations. I added new fish each day until I achieved a
density of approximately 3.7 recruits/rn2, the average density of recruits in these
populations prior to any manipulation. I began the experiment 24 hours after the final
addition of new fish.
I censused each population every two days for 36 days, from June 21 to July
27. During each census I recorded the number of tagged basslets and the number of
larger adults. Tagged basslets could disappear from a population through either
mortality or emigration. To determine if transplanted fish had emigrated, I searched
all populations within a 5m radius of each experimental population every week. I also
recorded and removed any newly settled basslets during each census. I measured net
per capita mortality as above.
I examined three potential manifestations of intraspecific competition between
adults and new recruits. First, I measured the feeding position of each transplanted
recruit relative to the ledge depth every four days (see Webster and Hixon 2000).
Second, I recorded all aggressive chases involving tagged fish during four-minute
observation periods in each population every four days. Finally, I recaptured all of the
tagged fish in late July to determine if the adult treatments had any effect on the
growth of survivors.
Video
I measured the within-population spatial distribution of basslet predators using
automated time-lapse video. I filmed 9 unmanipulated populations (4 in 1999 and 5 in
2000) for two days each. Each day, the camera filmed for two seconds every 30
seconds over a total of 8 -10 hours. I analyzed the film noting the species of all basslet
predators and their location relative to the front and back of the ledge. Whether or not
a given species was likely to prey on basslets was determined based on published
accounts of piscivory (Randall, 1967) and personal observations of feeding strikes
towards basslets.
Results
Monitoring
In June of 1998, 1999 and 2000, the density of adult basslets was typically
between 0 and 4 fishlm2 in populations with an area greater than 2m2 (Figure 4.1).
Smaller populations had much greater variability in density.
51
1999 Experiment
Thinning of conspecific density had weak effects on the survivorship of new
recruits (Figure 4.2). The mortality rate of new recruits increased slightly at high
densities of larger conspecifics. However, this relationship was not statistically
significant and conspecific density explained little variation in mortality rate. The
number, rather than the density, of larger conspecifics better predicted the mortality
rate of new recruits. No emigration of tagged recruits was observed during the
experiment
2000 Experiment
Population change
Recruit density declined steadily in each treatment following the start of the
2000 experiment (Figure 4.3). The sharpest decline occurred in populations with high
densities of adults. In contrast, recruit density changed the least in populations where
adults were absent. Consequently, there was a significant negative relationship
52
[IL]
IA.
0.4
I..
a)0.2
I..
n_fl
I-
0
4
2
6
8
10
12
14
16
Density of larger conspecifics
0.8
0.6
a)
0.4
r037
0.2
0.0k
0
5
10
15
20
25
Number of larger conspecifics
Figure 4.2. Net per capita mortality of transplanted, recently-recruited basslets versus
the density (A) and population size (B) of resident fish from a pilot study in 1999.
Lines were fit using least-squares regression.
53
4.0
(N
3.5
0
C
3.0
U)
C
a)
I...
C.)
a)
1.5
0
5
10
15
20
25
30
35
Time (d)
Figure 4.3. The change in density (± SE) of transplanted recruits in each treatment
during the 2000 experiment.
54
between final recruit and adult density (Figure 4.4A). The net per capita mortality rate
of new recruits was positively related to adult density although mortality varied
considerably within each treatment (Figure 4.4B).
Aggressive interactions
Aggressive chases involving new recruits were more common in populations
with adults, however the differences between treatments were not statistically
significant (Figure 4.5). Overall rates of aggression were low in all treatments.
Feeding position
The density of adults negatively affected the feeding position of new recruits
(Figure 4.6). When adults were present, new recruits fed significantly farther back on
the ledge and this was most pronounced at high densities of adults.
Growth rates
Relative growth rates of new recruits were estimated by examining the lengths
of recruits at the end of the experiment. The average size of transplanted recruits was
comparable among populations, thus differences in final length should be indicative of
differences in growth. Growth rates were highest in the absence of adults (Figure 4.7).
While some new recruits in populations without adults had growth rates comparable to
55
4
>,
4-,
Cl)
('4
I-
1
r2=0.30
P=O.036
Li
1.0
12=0. 26
0.8
P=0.051
(
0.6
0 0.4
E
S
0
2
4
Adult density
(noim2)
Figure 4.4. Final density (A) and net per capita mortality (B) of new recruits as a
function of adult density. Lines were fit using least-squares regression.
56
a)
4-.
C
E
0.04
0.03
Cl)
II
0.02
I-C.)
D)
0.01
<a.
0.00
1:
Adults density (no./m2)
Figure 4.5. The average per capita rate of aggressive chases (+SE) involving
transplanted recruits in each treatment. Differences between treatments were not
statistically significant (ANOVA: F2,12 = 1.74, P = 0.22).
57
!A1
0.2
0.1
0.0
C)
L1
0.2
L.
0.1
0.0
C.
0.3
0.2
0.1
0.0
0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Front
Back
Feeding position
Figure 4.6. The relative frequency of feeding positions of transplanted recruits in
each adult treatment. Dashed lines represent the average feeding position. A feeding
position of 0 is at the very back of the ledge, while 1 is at the very front. N is the
number of individual observations in each treatment. Average feeding position
differed significantly between treatments (ANOVA: F2,12 = 3.89, P = 0.047).
58
0.2
0.1
>.
C)
0.0
0.2
a)
ci)
I-.
4-
a,
>
0.1
(5
ci)
0.0
0.2
0.1
20
25
30
35
40
Total length (mm)
Figure 4.7. The size frequency of N transplanted recruits from each treatment at the
end of the 2000 experiment. The dashed line represents the average size in each
treatment. Growth rate was significantly different between populations with and
without adults (T13 = 2.03, P = 0.03), however, a regression between adult density and
average size was not significant (R2 = 0.33, P = 0.24).
those of recruits in populations with adults, the fastest growing recruits were all in
populations where adults were absent (Figure 4.7).
Recruitment rates
Recruitment did not differ between the three treatments with experimental
additions of new recruits, nor did recruitment to these populations differ from
populations with no conspecifics (Figure 4.8)
Video
Overall, predators of basslets were found most frequently towards the back of
ledges (Figure 4.9A). Trumpetfish (Aulostomus maculatus), and two groupers, the
coney (Cephalopholisfulva) and the graysby (C. cruentata), were the most commonly
observed predators. All were most frequently observed in the back half of ledges
(Figure 4.9B,C,D).
Discussion
Adult basslets negatively affected new recruits both through intraspecific
competition and by increasing new recruit mortality rates. These two phenomena were
probably not independent; competition with adults likely translated into greater
susceptibility to predators. Both of the manifestations of intraspecific competition
c1
E
0
4
conspecifics'
absent :
conspecifics
present
>
Cl)
U)
2
0
I-
U)
0
0
Adults density
2
4
(no./m2)
Figure 4.8. The average densities of new fish (+SE) that recruited to each of the three
experimental treatments and to five additional ledges from which all basslets were
removed. Differences in recruitment between treatments were not significant
(ANOVA: F2,12 = 3.24, P = 0.50).
61
0.6
A.
All Predators
0.4
0.2
I
0.0
0.6
B.
A. maculatus
C.
C. fulva
D.
C. cruentata
0.4
>
C-)
)
0.2
a9-
0.0
a)
> 0.6
CI)
0.4
0.2
0.0
1.0
0.8
0.6
0.4
0.2
0.0
0.1 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 1.0
Back
Front
Location on ledge
Figure 4.9. The relative frequency (+SE) of spatial positions of (A) all basslet
predators, (B) trumeptfish, Aulostomus maculatus, and the groupers, (C)
Cephalopholisfulva, and (D) C. cruentata, on unmanipulated ledges.
62
observed in this study, changes in growth rate and feeding position, likely contributed
to increased mortality rates of new recruits at high adult densities. Since smaller fish
are generally more susceptible to predators (Shepherd and Cushing, 1980, Houde,
1987, Sogard, 1997), depressed growth rates can result in higher mortality rates. For
new recruit basslets, this effect may have been exacerbated by their spatial
distribution; in the presence of adults, recruits were forced farther back on the ledge,
where predators were most abundant. While increased spatial overlap with piscivores
alone may have caused higher mortality rates, basslets may have been at an additional
disadvantage due to relatively dim light near the back of ledges. Piscivores tend to
have a visual advantage over their prey only at dawn and dusk (McFarland, 1991),
conditions that may be approximated diurnally at the back of ledges.
Adults increased recruit mortality during both a pilot study in 1999 and a more
thorough study in 2000. The results in 1999 were equivocal, probably for at least two
reasons. First, in 1999 the resident fish population was composed of both juveniles
and adults. Differences in the relative proportion of adults and juveniles may have
increased among-population variability in the response of new recruits. Second, the
study in 1999 included small ledges, which can support much higher densities of fish
than large ledges (Figure 4.1). Therefore, it is not clear whether a given density is
comparable between very small and large ledges. In the 2000 experiment, I sought to
address these two issues by using only relatively large ledges and by manipulating only
adults. Despite the differences in methods, both studies observed the same general
pattern: recruit mortality increased as a function of adult density.
63
Basslets could attempt to minimize the negative effects of intraspecific
competition by settling disproportionately to low-density populations. However, such
density-dependent recruitment was not observed. Instead, recruitment of new basslets
was independent of both the presence of conspecifics and the density of adults,
suggesting that basslets identify settlement sites based on habitat type rather than cues
from conspecifics. Since adult density can vary substantially among populations, the
intensity of intraspecific competition experienced by new recruits is also likely to vary
spatially. As with the basslets, the majority of published examples have not observed
density-dependent recruitment, but rather they have observed either no relationship or
a positive relationship between recruitment and adult density (review by Hixon and
Webster, in press). The latter pattern of recruitment facilitation would tend to
intensify, rather than dampen, intraspecific competition.
In this study, the outcome of intraspecific competition was a dampening of
between-population variation in basslet density. As a consequence, intraspecific
competition may work to help regulate population size in basslet aggregations.
Intraspecific competition is not the only mechanism by which basslet populations may
be regulated. Predators, in particular, may help regulate populations by altering their
behavior to consume a disproportionately large number of prey in high-density
patches. However, in this study, predator behavior was not monitored, so it is
uncertain whether increases in mortality at high adult density were partly due to
behavioral responses by predators. Whether or not predators responded to basslet
density, competition likely played an important role in increasing basslet mortality
rates by making fish more susceptible to predators.
In a related study (Webster unpublished manuscript), I demonstrated that
predators did respond to different densities of new recruit basslets, apparently causing
density dependence. However, altering the density of new recruits did not intensify
intraspecific competition with adults. Apparently, only increasing adult density, not
recruit density, intensifies competition within the ranges of densities used. By
working in concert, these two mechanisms of density dependence, intraspecific
competition and responses by predators, likely impart a strong regulatory effect on
local basslet populations.
Most of the published demonstrations intraspecific competition in coral-reef
fish involve aggregating damselfish (e.g. Doherty, 1982, 1983, Jones, 1987a,b, 1988,
1990, Forrester, 1990, Booth, 1995). Whether or not this indicates that damselfishes
are particularly prone to experience intraspecific competition is unclear because of the
relative dearth of studies involving species from other taxonomic families. There is
evidence for intraspecific competition in other families of coral-reef fishes, but most of
it is indirect. Victor (1986) found evidence for decreased growth of bluehead wrasses
at high densities using otolith ageing techniques. For a species of blenny in the
Caribbean, individuals appear to compete for shelter holes (Buchheim and Hixon,
1992). Two studies of gobies suggested that residents may competitively inhibit the
recruitment of new fishes (Forrester, 1995, Steele et al., 1998). However, the study by
Forrester (1995) detected no post-recruitment effects of residents on new recruits.
65
Combined with the current study, these examples suggest that intraspecific
competition does occur across a wide range of coral-reef fish species.
This study demonstrated intraspecific competition in basslet populations that
was sufficiently severe that it led to differences in growth and density-dependent
mortality. As a consequence, intraspecific competition may help regulate local basslet
populations. These results extend our understanding of intraspecific competition in
coral-reef fishes beyond the damselfishes and raise the question of how frequently
similar interactions occur among the multitude of species on coral reefs.
Chapter 5: Role of Predators in the Early Post-settlement
Demography of Coral-reef Fishes
Abstract
Populations with dispersive larvae are often demographically open such that
local reproduction and subsequent larval settlement are not linked. Thus,
understanding whether and how settlement patterns are established and subsequently
modified is central to understanding local demography. Settlement is typically not
measured directly, but rather it is estimated by recruitment, which is the observation of
new individuals sometime after settlement. At Lizard Island on the Great Barrier
Reef, I examined how patterns of recruitment of coral-reef fishes were modified across
a range of natural recruit densities in the presence and absence of resident predators.
Resident predators decreased recruitment and increased mortality for all species, but
these effects varied considerably among species. The effects of predators on
recruitment were at least partly due to mortality within two days after settlement. At
their most extreme, predators caused recruitment failure of several species of
butterflyfish. For one species of damselfish (Pomacentrus amboinensis), predators
both induced weak density-dependent mortality and obscured any relationship between
recruitment and subsequent abundance, while for another damselfish (Neopomacentrus
cyanomos) mortality was density-independent and subsequent abundance was a
function of recruitment. These contrasting results may reflect differences in prey
67
behavior. P. amboinensis tended to feed near or within the branches of coral inhabited
by resident predators, while N. cyanomos tended to feed higher in the water column
above the reefs, and thus farther away from resident predators. These results highlight
the speed and extent to which patterns of settlement are modified, indicating that
caution should be exercised when attributing patterns of recruitment to patterns of
settlement. Tremendous between-species variation in how patterns of recruitment, and
presumably settlement, were modified by predation indicates that generalizations or
between-species extrapolations about the magnitude of these effects may be
unwarranted.
Introduction
Many marine organisms have a bipartite life history in which individuals have
a planktonic larval stage before settling to habitats on or near the sea floor. This
phenomenon can result in demographically open populations at spatial scales that are
small relative to dispersal distances. In such local populations, the birth rate is not a
function of local reproduction, but instead depends on the settlement of new
individuals that originated elsewhere. This situation presents unique challenges for
understanding population dynamics, especially regarding how patterns of settlement
are established, and whether and how these patterns are subsequently modified
(Keough and Downes, 1982, Luckenbach, 1984, Connell, 1985). While settlement
typically cannot be measured directly, it can be estimated by measuring recruitment,
which is the observation of individuals shortly after settlement. Because settlement
68
patterns can be modified before the observation of recruitment, it is impossible to say
with certainty whether recruitment accurately reflects settlement. It is therefore
unknown whether the observed distribution of new recruits reflects patterns
established at settlement or sometime thereafter (Hixon, 1998).
There has been considerable debate among marine ecologists about the role of
post-settlement processes in either maintaining or modifying settlement patterns.
While some have observed that settlement patterns persist, and thus proportionally
determine adult abundance (e.g. Doherty and Williams, 1988, Gotelli, 1988,
Sutherland, 1990), others have documented modification of settlement patterns (e.g.
Luckenbach, 1984, Forrester, 1995, Hixon and Carr, 1997). Recently, ecologists have
explored the relative importance of settlement patterns and post-settlement
modification rather than simply focusing on one factor or the other (e.g. Jones, 1991,
Caley et al., 1996, Steele, 1997, Schmitt and Holbrook, 1999a,b). This shift in focus
has been spurred by the increasingly common observation that patterns established at
settlement tend to persist at lower settlement rates, but are modified by post-settlement
processes when settlement rates are relatively high (e.g. Gaines and Roughgarden,
1985, Jones, 1987a, Minchinton and Scheibling, 1991, Bertness et al., 1992, Forrester,
1995, Menge, 2000).
For local populations where emigration is negligible, any modification of
settlement patterns is due to mortality. Rigorously identifying which sources of
mortality are important requires experimental manipulation of putative sources.
Predation is often implicated as the most important source of post-settlement mortality
for coral-reef fishes (e.g. Shulman et al., 1983, Hixon, 1991, Connell, 1996, 1997,
2000, Nemeth, 1998). However, studies that manipulated the presence and absence of
predators have shown varied results. Shpigel and Fishelson (1991) suggested that the
removal of Cephalopholis spp. had little effect on reef fish communities in the Red
Sea. In this case, however, once these predators were removed, other predator species
promptly took their place. Steele et al. (1998) found that resident predators had either
a positive or no effect on gobies while transient predators had no effect. Hixon and
Carr (1997) observed density-dependent mortality of a damselfish in the presence of
both resident and transient predators, but not when either or both suites of predators
was excluded. Other studies have consistently shown negative effects of predators on
abundance (Caley, 1993, Can and Hixon, 1995, Beukers and Jones, 1997, Eggleston et
al., 1997, Connell, 1998), recruitment (Shulman et al., 1983) and species richness
(Caley, 1993, Eggleston et al., 1997).
The goal of this study was to understand how patterns of recruitment of coral-
reef fishes were modified by predation. Specifically, I asked four questions: (1) Is
there evidence that settlement patterns are modified before recruitment is observed?
(2) What is the net effect of resident predators on recruitment rates, per capita
mortality rates, and subsequent abundance? (3) Is there evidence for density-dependent
mortality for coral-reef fishes in either the presence or absence of resident predators?
(4) Are patterns of recruitment good predictors of subsequent abundance?
70
Methods
Study System
This study was conducted at the Lizard Island Research Station in the northern
Great Barrier Reef, Australia. Previously, researchers consolidated patches of live
Porites cylindrica
coral in the 9m deep sandy area of the lagoon, creating an array of
54 patch reefs of similar size and isolation (Figure 5.1, Jones and Hixon in prep.).
Each reef was approximately 3.2m (SE = 0.05m) long by O.6m (SE = 0.Olm) wide
with a surface area of 2.0m2 (SE = O.05m2) and was 30m from both the nearest
transplanted reef and the source reef. Prior to this experiment, these reefs were left
unmanipulated for several years.
I assumed that fish did not move between reefs in this study because similar
isolation distances have been shown to effectively hinder between-reef movements of
small fishes (Doherty, 1982, Hixon and Beets, 1989). I also assumed that isolation of
this magnitude did not affect larval supply (i.e. larval supply was even among reefs).
It is possible that some regions of the array experienced higher larval supply due to
their relative proximity to pelagic sources of larvae (Figure 5.1). If this were the case,
recruitment should vary spatially, which was not observed during this study.
Furthermore, since treatments were assigned randomly to reefs, any spatial patterns
would not be likely to impact the results systematically.
71
N
Lizard
1km
IsIand
o
Land
o
Shallow reef(<5m)
fl Lagoon and open ocean
Experimental reef
C?ExPenm.ntaij
i
/ */
Om
Figure 5.1. Map of Lizard Island, Great Barrier Reef, Australia showing the location
and spatial arrangement of the experimental array of transplanted Porites cylindrica
reefs.
Experimental Design
In November 1999 I censused the resident fish community of 34 of the patch
reefs. I randomly selected 18 of these reefs and assigned them to one of two
treatments: control (n = 9 reefs) and resident predator removal (n = 9 reefs). On
72
predator-removal reefs, I captured all resident piscivores (primarily Cephalopholis
boenak and Pseudochromis fuscus using clove oil and hand nets (see Munday and
Wilson, 1997). On control reefs, I manipulated predator abundance to a standard
density of 4-6 C. boenak and 1-2 P. fuscus per reef. This assemblage represents a
density slightly above the average (2.8 C. boenak and 0.9 P. fuscus) but below the
maximum (9 C. boenak and 3 P. fuscus) that I observed during the initial census.
During every subsequent census (see below), I searched each reef for piscivores. Any
immigrant or newly recruited predators were promptly captured on predator removal
reefs to maintain predator-free treatments. On control reefs, I censused piscivores to
ensure that densities remained similar to the standard initially established.
During the initial census of the reefs, I noted considerable variation in the
number of cardinalfishes (Apogonidae) between reefs. On some reefs cardinalfishes
were absent, while on others there were as many as 2000 individuals, primarily
Apogonfragilis and A. doederleini. Since cardinalfishes represented a potentially
important alternate source of prey for predators, variation in abundance of these
species could cause between-reef differences in the effect of predators on other species
(Stewart 1998). To minimize this possibility, I removed all cardinalfish initially and
once each week thereafter using a BINCKE net (Anderson and Carr, 1998).
Prior to beginning this experiment, I removed all recently-recruited fishes from
each reef using hand nets and clove oil. By removing these fishes, I could more
accurately distinguish fishes that settled once the experiment began from those already
present on each reef. Moreover, starting the experiment with all reefs recruit-free
73
ensured that any prior residency effects did not confound subsequent patterns of
settlement between predator treatments. Once the experiment began on 26 November
1999, I censused the recently-recruited fishes on each reef every two days until 15
January, 2000 (50 days total). During each census, I carefully examined the reef for
recently-recruited fishes, noting new recruits, previously-recruited fishes, and
disappearances. Therefore the operational definition of recruitment in this study is the
observation of a new fish within 48 hours of settlement to the reef. Note that because
of the time interval between settlement and subsequent recruitment, settlement
patterns may have been modified by the time I first observed new recruits (see
Discussion). Any previously-recruited individuals that were missing were recorded as
mortalities because, given the isolation distances between reefs, emigration was likely
tantamount to mortality for newly recruited fish.
This census method is prone to errors if a fish disappears and is replaced by a
new recruit of the same species and size on the same reef between censuses. This type
of replacement error would tend to underestimate both recruitment and mortality. I
attempted to minimize such replacement errors in two ways. First, I sought to
distinguish between new recruits and previously recruited individuals by size and
coloration; new recruits are frequently lightly pigmented and visibly smaller than
individuals that recruited only a few days earlier (Victor, 1991). Second, for siteattached species, I marked the location of each new recruit with labeled flagging tape.
If one fish did replace another, it would not likely occupy the exact same location as
the missing fish and could therefore be distinguished. These census techniques
74
worked well for damselfishes (Pomacentridae), and reasonably well for more vagile
butterflyfishes (Chaetodontidae) and surgeonfishes (Acanthuridae). Therefore, data
were examined only for these three families.
Data Analysis
Comparisons were made for both individual species and taxonomic families,
using reefs as replicates. The family-level comparisons assumed that common factors
influenced the demography of species within a family. Typically all the species within
a family had recruits of similar size and trophic status. Exceptions to this included a
few species of pomacentrids that are largely herbivorous as adults rather than
planktivorous like the majority of pomacentrid species that I observed. I have
included these herbivorous species in pomacentrid-level comparisons because, as new
recruits, they likely had similar diets to planktivorous species; herbivorous fishes may
pass through a period of carnivory as juveniles and later make a transition to herbivory
(Choat, 1991). Furthermore, these species were relatively rare (Table 5.1), so they did
not strongly impact any of the comparisons.
Census data were used to calculate total recruitment and net per capita
mortality rates for each reef for the 50-day duration of the study.
Total
recruitment is
simply the number of new recruits counted on a reef during the study. The "net per
capita mortality rate" was calculated by dividing the total number of disappearances by
the total recruitment during the study for each reef. Because individuals were
75
continuously arriving to and disappearing from reefs, the density of new recruits
(number per reef) varied through time. Consequently, total recruitment provides a
fairly coarse measure of density, limiting the power of tests for spatial density
dependence.
I examined relationships between recruitment and both per capita mortality and
final abundance for two species (Pomacentrus amboinensis and Neopomacentrus
cyanomos) and one family (Pomacentridae). I excluded such comparisons for all other
taxa for two reasons. First, I excluded all comparisons with a sample size smaller than
five reefs in either treatment. Although I often observed recruitment of a species or
family to a sufficient number of reefs where predators were removed, I also usually
observed too few reefs with recruits where predators were present. Second, I excluded
comparisons where the range of recruitment values was insufficient to warrant fitting a
linear relationship between recruitment and either mortality or abundance. For
example, P. nagasakiensis recruited to many reefs in both treatments; however, I
observed a maximum recruitment of three individuals on predator-present reefs.
I fit multiple linear regression models to determine whether final abundance
was a function of recruitment both in the presence and absence of predators.
Theoretically, these relationships pass through the origin
when recruitment equals
zero subsequent abundance will also equal zero. However, if the relationship is
curved, a simple linear regression could predict a non-zero y-intercept. Based on
initial data analysis, there was no evidence that these relationships were either curved
or linear with positive intercepts, with the exception of P. amboinensis when predators
76
were present (see Results). Therefore, I forced the intercept to be zero in all but one
comparison and used straight lines in all analyses.
I examined the data for evidence of density dependence between total
recruitment and net per capita mortality. I fit multiple linear regression models with
net per capita mortality as the response variable and recruitment, predator treatment,
and an interaction of the two as explanatory variables. In this model, a significant
effect of either recruitment or the recruitment by treatment interaction would indicate
that mortality rate varied with recruitment for at least one of the treatments.
Results
Recniitment
Over the 50-day duration of the experiment, 686 new recruits were
observed from the families Pomacentridae, Chaetodontidae and Acanthuridae. I
observed 12 pomacentrid species, totaling 552 new recruits (Table 5.1). Only the most
abundant species, Pomacentrus amboinensis, recruited to all 18 reefs. Recruits in the
family Chaetodontidae were the next most abundant, totaling 69 individuals from six
species. I observed 65 individuals from the family Acanthuridae. Acanthurids were
considered only at the family level because I could not accurately distinguish between
the recruits of several species. Overall, I examined 7 of the most abundant species
(Pomacentrus pavo, Pomacentrus nagasakiensis, P. amboinensis, Neopomacentrus
77
cyanomos, Hemiglyphidodon plagiometopon, Chaetodon auriga, Chaetodon
ephippium) as well as all 3 families.
Temporal patterns of recruitment varied substantially among species
and families (Figure 5.2). Some species recruited primarily during a single pulse (P.
pavo, H plagiometopon, N cyanomos), while others showed a more bimodal
recruitment pattern (P. nagasakiensis, P. amboinensis) during the 50 days of the study.
Chaetodontids and acanthurids recruited at low levels throughout the study period.
The majority of pomacentrids recruited in pulses during the first half of the
study. Therefore, the mortality rates observed after recruitment were largely estimates
for relatively discrete cohorts, and thus were probably not strongly affected by
differences in the timing of recruitment between reefs. In contrast to pomacentrids,
chaetodontids and acanthurids recruited at low rates throughout the study.
Consequently, age distributions may have differed substantially among reefs, which
could amplify between-reef variability in mortality rates. However, since so few
chaetodontids and acanthurids recruited to predator-present reefs, between-treatment
comparisons of survivorship were impossible. While the timing of recruitment may
have affected final abundance, such temporal variation probably did not bias any
general conclusions in light of the clear differences in abundance between the two
treatments (Table 5.2, Figure 5.3).
78
Table 5.1. Total number of recruits observed during the 50-day sampling period of
each species from three families and the number of reefs on which they were observed
(N = 18 reefs total).
Family
Species
Recruits
Reefs
Pomacentridae
Dascyllus Irimaculatus
1
1
Dascyllus aruanus
3
2
Dischistodus prosopotaenia
3
2
Pomacentrus moluccensis
3
3
5
4
Pomacentrus wardii
Dischistodus perspicillalus
13
8
Neopomacentrus azysron
21
6
Pomacentrus pavo
22
12
Hemiglyphidodonpiagionwlopon
47
17
Pomacentrus nagasakiensis
108
16
Neopomacentrus cyanomos
128
15
Pomacentrus amboinensis
198
18
All Pomacentrids
552
18
Chaetodontid
Chaetodon melanotus
1
1
Chaeiodon ulitensis
2
2
Chaetodon lunulatus
4
3
Heniochus acuminulatug
4
3
Chaetodon auriga
13
8
Chaetodon ephippium
45
9
All Chaetodontids
69
12
65
11
686
18
Acanthuridae
All Acanthurids
Total
79
L1
16
15
10
5
0
2C
10
P. nagasa
ns
20
10
5
30
0
P. amboinensis
20
10
a)
9-
0
:AUpomaceoUds
0
60
40
a)
.0
20
E
Z
0
C. aunga
2
0
6
C. ephippium
4
2
0
6
Lilthaetodonis
4
0
10
0
10
jIIanthus
20
30
40
Day
Figure 5.2. The total number of new recruits observed on 18 experimental reefs over a
50-day period. Each panel represents a different species or family. Circles in the top
panel denote moon phase: closed circles represent the new moon and the open circle
represents the full moon. Note that the scale of the y-axis changes between panels.
80
For all species and families, recruitment was higher in the absence of predators
(Table 5.2, Figure 5.3 a). This difference was significant for all but three species (P.
pavo, H plagiometopon, N. cyanomos). The magnitude of the effect of predators on
recruitment was calculated as the ratio of the number of recruits in the absence and
presence of predators (Table 5.2). For example, there were 22.0 times as many
chaetodontid recruits on predator removal than control reefs; however, there were only
1.4 times as many P. pavo.
Mortality
Net per capita mortality rates were higher in the presence of predators for all
species of pomacentrids (Table 5.2, Figure 5.3b). Similar comparisons could not be
made for chaetodontids or acanthurids because too few individuals recruited to
predator reefs to calculate mortality rates. Among the pomacentrids, the differences in
mortality rates were significant for all comparisons except H plagiometopon and P.
pavo, which were the least abundant pomacentrid recruits analyzed (Table 5.1). The
effect of predators on mortality, examined as the ratio of the net per capita mortality
rate in the presence and absence of predators, ranged from 1.1 times higher mortality
for H plagiometopon to 3.7 times higher mortality for P. nagasakiensis (Table 5.2).
For all pomacentrids combined, mortality rates were 2.3 times higher in the presence
versus absence of resident predators.
81
Table 5.2. Summary statistics for the effect of predators on recruitment, mortality, and
abundance of each species and family.
Family
Species
Pomacentridae
P. pavo
H. plagiomelopon
P. nagasakiensis
N. cwnomos
P. amboinensis
All pomacentnds
Chaetodontidae
C. auriga
C. ephippium
All chaetodontids
Acanthuridae
All acanthurida
P+
Recruitment
PRatio
P-value
P+
P-
0.244
0.072
<0.001
0.129
<0.001
<0.001
0.70
0.90
0.90
0.82
0.62
0.74
0.29
0.79
0.24
0.38
0.22
--
22.0
0.002
<0.001
<0.001
-
0.16
0.37
4.9
0.002
----
0.42
1.0
1.4
1.4
2.0
3.2
1.6
1.6
10.4
6.7
5.1
9.1
1.8
6.0
16.7
16.0
44.7
2.7
2.7
0.1
1.3
12.0
0.0
0.3
5.0
7.3
l.2
6.0
0.31
0.81
Mortality
Ratio P-value
2.4
1.1
3.7
2.2
2.8
2.3
---
N
0.064
0.221
<0.001
0.001
<0.001
<0.001
P+
0.2
0.3
0.2
Abundance
Ratio
P-
P-value
0.006
0.260
<0.001
0.038
<0.001
<0.001
1.0
4.5
0.6
1.7
18
2.1
1.9
8.1
6.1
12.7
18
5.2
31.2
36.5
2.9
6.7
6.0
- -
0.0
0.0
0.2
0.3
4.2
4.8
21.5
0.031
<0.001
<0.001
--
0.6
3.6
6.4
0.003
12
17
16
15
-
-----
-
Note: P+ denotes the predator present treatment and P- denotes the predator removal
treatment. Recruitment values given are the average number of new recruits per reef
over the entire study. Mortality was calculated as the average net per capita mortality
with and without predators. Abundance is the average number of recruits per reef at
the end study with and without predators. Ratios are P-/P+ for recruitment and
abundance and P+/P- for mortality. All P-values are from two-sample t-tests (N=l 8
for each test except as noted for mortality). Missing values indicate calculations that
were not possible due to insufficient data.
In total, five species of pomacentrids were sufficiently abundant to calculate
both recruitment and mortality rates. For these species, the effects (expressed as ratios)
of predators on recruitment were positively, although not quite significantly, correlated
with effects on mortality (correlation coefficient = 0.82; p=O.O86). The suggested
trend is that the species for which recruitment was most strongly modified by predators
were the same species that suffered the greatest post-recruitment mortality due to
predation.
82
50
(I)
2
40
-
30
0
a)
9-
0
j3
a.
Predators:
present
absent
20
10
0
1 00
075
0. 050
0
a) 025
aa)
Z 000
40
0
C.
a)
C
0
Co
30
20
Co
10
U0
,'
cf
Figure 5.3. The effect of predators on a total recruitment, b mortality, and c final
abundance (mean ± SE) or all species and families over 50 days. Dotted vertical lines
separate taxonomic families. A "0" indicates that net per capita mortality values
could not be calculated due to insufficient data.
Abundance
The combined effects of predators on both recruitment and net per capita
mortality resulted in substantial differences in final abundance (Table 5.2, Figure
5 .3c).
For all species and families, the final abundance of recruits was higher in the
83
absence of predators. This pattern was statistically significant for all families and all
species except H plagiometopon. The ratios of abundance in the presence versus the
absence of predators varied considerably: P. nagasakiensis was most affected,
resulting in 36.5 times as many individuals in the absence of predators, whereas H
plagiometopon was the least affected, with only 1.7 times as many individuals in the
absence of predators. The ratio could not be calculated for C. auriga or C. ephippium
because no individuals were present on reefs with resident predators.
Recruitment/abundance Relationships
Initially, I fit each abundance versus recruitment regression using a full model
that included both y-intercepts and slopes. For the family Pomacentridae and for N
cyanomos, there was little evidence for non-zero intercepts, and since final abundance
must equal zero when recruitment equals zero, I re-fit the models forcing the lines
through the origin. This adjustment had little impact on the fit of the model or the
slopes (Table 5.3, Figure 5.4), and allowed the ratio of the slope in the presence and
absence of resident predators to be used as a measure of how intensely recruitment
patterns were modified. During the 50-day study period, predators reduced the final
abundance of N. cyanomos by 25% and the final abundance of all pomacentrids
combined by 49%. For P. amboinensis, the slope in the predator-present treatment
was not significantly different from zero, indicating that predators eliminated any
relationship between recruitment and subsequent abundance (Table 5.3, Figure 5.4).
84
Table 5.3. Summary statistics for slopes from multiple linear regressions of final
abundance as a function of the number of recruits
Predators present
Predators absent
Species
Slope
P-value
n
Slope
P-value
n
Predator effect
N. cyanomos
0.71
<0.001
6
0.54
<0.001
8
0.25
P. amboinensis
0.88
<0.001
9
0.11
0.453
9
n/a
All Pomacentrids
0.72
<0.001
9
0.37
<0.001
9
0.49
Note: Reported P-values test for differences from a slope of zero. The "predator
effect" on abundance is the proportion of recruits lost due to the presence of predators
[1- (slope in the presence of predators / slope in the absence of predators)] in models
where both lines pass through the origin.
85
N cyanomos
N. cyariomos
30
25
20
1£
a.
Predators:
0 absent
b.
O
S
o
present
0.6
0
0.
O--- _______
0.2
0
0.0 o
20
25
30
0
P. amboinensis
5
10
20
15
25
30
P. amboinensis
25
ci
20
d.
0.6
cø
0
ioF
0.4
Th
20
25
0
All pomacentrids
80
60
o.
-
0.2
5
10
15
0
0
20
25
Alt pomacentrids
e.
1.0
0.8
S..
0.6
40
oo
0
0.4
20
000
0.2
01020304050607080
0.0
0 1020304050607080
Number of recruits
Figure 5.4. The relationship between recruitment and both final abundance and net per
capita mortality for a,b N. cyanomos, c,d P. amboinensis, and e,f all pomacentrids
using least squares regression. Dashed lines indicate relationships with non-significant
slopes. Note that the scale of the y-axis changes between panels.
86
Recruitment/mortality Relationships
I found no evidence for density dependence for N. cyanomos, or pomacentrids
as a whole in either treatment (Table 5.4, Figure 5.4). For P. amboinensis mortality
was density-independent in the absence of predators, but weakly density-dependent in
their presence. Although statistically significant, the strength of this relationship was
dependent on a single influential data point.
Table 5.4. Summary statistics for slopes from multiple linear regressions of per capita
mortality as a function of the number of recruits.
Predators absent
Species
Slope
P-value
Predators present
ii
Slope
P-value
a
N cyanomos
-0.006
0.696
6
-0.020
0.092
8
P. amboinensis
-0.013
0.4 16
9
0.046
0.042
9
All Pomacentrids
-0.004
0.098
9
-0.001
0.710
9
Note: Reported P-values test for differences from a slope of zero.
Discussion
The substantial effect of predators on recruit abundance occurred via two
demographic rates: predators both decreased recruitment rates and increased post-
recruitment mortality rates. Negative effects on recruitment were species-specific,
ranging from little effect on Hemiglyphidodonpiagiometopon to apparent recruitment
failure for Chaetodon ephippium. Predators may have affected recruitment rates in
87
two ways: indirectly, by altering the behavior of settling fishes such that they
preferentially settled on predator-removal reefs, or directly, by preying on fish after
settlement, but before recruitment was measured. The former settler-avoidance
hypothesis would require that settlers detect a cue from predators prior to settlement
and use this information to select a settlement site. Some coral-reef fishes can
apparently detect the presence of conspecifics (Sweatman, 1988, Booth, 1992),
potential competitors (Sweatman, 1988), and settlement habitat (Elliott et al., 1995,
Danilowicz, 1996). However, few studies have examined whether settling larvae
detect the presence of predators. Recent work by Almany (in prep.) demonstrates that
settlers do not respond to cues from caged predators on Bahamian coral reefs. If
predators are ubiquitous on coral reefs (see Hixon, 1991), then there may be few
predator-free patches at the time of settlement. Even if predator-free patches could be
detected and found, they would not likely remain predator-free for long since predators
are far more mobile than newly settled fish and tend to aggregate where predators are
abundant (Hixon and Can, 1997, Hixon, 1998). Therefore, settlement to predator-free
patches would be a relatively short-term strategy. It may be more advantageous to
make settlement choices on the basis of longer-term characteristics of a site such as
habitat type (including prey refugia) or the presence of site-attached conspecifics (with
associated reproductive and prey-defense benefits).
Alternatively, the differences in recruitment that I observed between reefs with
and without predators may have resulted from differential mortality between the time
of settlement and the time I censused the reefs (recruitment) up to 48 hours later.
88
Because mortality rates were substantially higher in the presence of predators after
recruitment, one would predict that mortality rates were also higher after settlement
but before recruitment. This extrapolation explains at least some of the differences in
recruitment rates. However, for this predation hypothesis to explain all of the
observed differences in recruitment, mortality must have been much higher within the
first day or two on the reef than during subsequent weeks. Since mortality rates are
often highest immediately following settlement (Doherty and Sale, 1985, Victor, 1986,
Meekan, 1988, Sale and Ferrell, 1988, Booth, 1991, Hixon and Carr, 1997, Schmitt
and Holbrook, 1 999a), the hypothesis that differences in recruitment were entirely due
to post-settlement mortality remains viable. A direct effect of predators on recruitment
is further supported by the observation that, among pomacentrids, the magnitude of the
effect of predators on recruitment was weakly correlated with the magnitude of their
effect on mortality. In other words, the species that were most affected by predators
after recruitment were the same species that were most affected before recruitment.
In the presence of resident predators, mortality rates were high for all species
(62-90% over 50 days). While the magnitude of the effect of predators varied
considerably, resident predators increased mortality rates for all species and families.
Mortality rates were always greater than zero on predator-removal reefs, which
indicates these reefs were subject to predation by species other than those manipulated.
These piscivores may include highly cryptic scorpionfishes (Scorpaenidae),
invertebrate predators such as stomatopods, or transient predators such as jacks
(Carangidae) or lizardfishes (Synodontidae). The reefs in this experiment were
89
frequented by jacks and lizardfishes, which probably represented a substantial source
of predation (see Hixon and Carr, 1997).
Mortality was always density-independent in the absence of resident predators.
However, with resident predators present, the effect of recruit density on mortality was
density-dependent for P. amboinensis, but not for N cyanomos or for all pomacentrids
combined. While the evidence for density-dependent mortality of P. amboinensis was
weak, predators nonetheless eliminated any relationship between recruitment and final
abundance for this species. This paftern is especially noteworthy given that
relationships between recruitment and subsequent abundance tend to be significantly
positive whether mortality is density-dependent or not (McGuinness and Davis, 1989,
Caley et al., 1996, Hixon, 1998).
Different responses by P. amboinensis and N cyanomos to resident predators
may reflect ecological differences between these species. N cyanomos recruits
typically fed above the reef in schools that mixed with adult damselfishes and
cardinalfishes. Feeding in this exposed location may have made them more
susceptible to transient predators, especially jacks, and less susceptible to the resident
predators that were manipulated in this experiment. In contrast, P. amboinensis
recruits typically remained closely associated with the branches of the coral, which
probably made them more susceptible to resident rather than transient predators.
Resident predators may have reacted with a type III (sigmoid) functional response to
higher densities of P. amboinensis, thus inducing weak density dependence and
obscuring any relationship between recruitment and abundance (see Murdoch and
Oaten, 1975). Why then did transient predators not have a similar effect on N
cyanomos? Based on qualitative observations, transient predators may have
responded primarily to densities of cardinalfishes, which varied independently of N
cyanomos densities and were often far more abundant than N cyanomos despite
repeated removals (see Stewart, 1998).
Because predators strongly modified the abundance of recruits in both speciesand family-dependent ways, caution should be exercised when interpreting end-of-
season recruitment patterns as an index of settlement (e.g. Doherty and Fowler,
1 994a,b). These results echo similar findings in other systems (e.g. Eggleston and
Armstrong, 1995). In contrast to these results, Williams et al. (1994) found that
recruitment was a good predictor of end of season abundance for many species of reef
fish. I believe that these two opposing conclusions are due largely to differences in
methods, especially the measurement of recruitment. Williams et al. (1994) defined
recruitment as the maximum number of recruits observed on a reef during one of four
censuses over an entire recruitment season. This estimate did not incorporate any
measure of persistence or mortality of individual recruits. In this experiment, I
estimated settlement more accurately by measuring recruitment every two days and by
distinguishing between new and previously observed fish. Despite sampling every 48
hours, I still probably underestimated settlement, as evidenced by differences in
recruitment between predator present and removal reefs. The speed and magnitude by
which predators affected abundance highlights the inherent danger in hindcasting the
magnitude of settlement based on abundance ofjuveniles or adults.
91
The results of this study underscore the importance of predators to both
recruitment and post-recruitment mortality of coral-reef fishes. Although predators
negatively affected all species in this study, the magnitude of these effects varied
tremendously among species. Furthermore, while early post-settlement densitydependent mortality is emerging as a common feature of the population dynamics of
coral reef fishes (reviewed by Hixon and Webster, in press), this study highlights that
mortality patterns can be variable between species subject to the same suites of
predators on the same reefs.
92
Chapter 6: General Conclusions
In the above studies, a variety of factors affected the population dynamics of
coral-reef fishes. In Chapter 2, I described the social structure of basslet populations.
Adult basslets had strong effects on new recruits, forcing them to the back of ledges
where they experienced depressed feeding rates. Feeding rate was depressed by both
interference and exploitation competition that combined to reduce feeding rate by over
60%. This study raised the question of whether these competitive effects regulate
population dynamics.
In Chapter 3, I explored how high recruitment affected local population
dynamics of fairy basslets. Prior to conducting this experiment, I anticipated that
during periods of high recruitment, competition with adults would intensify, thus
leading to demographic density dependence. While strong density-dependent
mortality was observed, I found no evidence that intraspecific competition was the
source. Using automated time-lapse video, I determined that predators spent more
time present and hunting while present in high-density populations, apparently causing
density dependence. Density dependence was sufficiently strong to eliminate any
effect of increased recruitment by the following spring. A similar pattern was
observed the following year in unmanipulated populations, suggesting that density
dependence acts on these populations consistently through time.
93
In Chapter 4, I further examined the effects of competition within basslet
populations. By manipulating adult density while holding recruit density constant, I
observed that adults negatively affected recruits. Competition with adults apparently
increased the susceptibility of new recruits to predators, resulting in density-dependent
mortality. Predation risk probably increased for at least two reasons: (1) recruits grew
more slowly in the presence of adults, and (2) adults forced recruits to the back of
ledges where predators were most common.
The above studies identified two likely mechanisms for density-dependent
mortality: (1) increased susceptibility to predation due to competition with adults, and
(2) behavioral responses by predators during periods of high larval sefflement. These
two mechanisms probably work in concert to stabilize basslet populations.
Competition with adults may cause a convergence in total density among populations
throughout the recruitment season in spring and summer (Figure 6.1). Subsequent
variability among populations in recruitment may be dampened by behavioral
responses by predators that cause convergence among populations (Figure 6.1). The
combined effects of these two processes likely results in the regular annual cycles of
abundance that I observed in basslet populations.
94
HI
>
Cl)
a)
a
C
0
0
0
HI
0
AV(
LO
Winter
1?:-.
Summer
Spring
Fall
Time
Figure 6.1. Qualitative summary of density-dependent factors affecting population
dynamics of basslets. Bold arrows represent experimental manipulations of density
and dashed lines represent the trajectories of post-manipulation populations.
Competition with adults in spring leads to a convergence in density among populations
and variability due to differential recruitment in summer is dampened by behavioral
responses by predators.
The population dynamics of basslets are complex, depending on interactions
both within species (competition) and among species (predation). While my studies
have identified some key factors influencing and regulating population dynamics, they
likely oversimplify the complete suite of mechanisms and processes that determine
population size. In particular, social organization may have more widespread
consequences br local and metapopulation dynamics. Promising avenues for future
study include examining whether behavioral interactions work to determine the density
of adults each spring and how these interactions affect reproductive output. During the
years of these studies, recruitment was consistently high. Years of low recruitment are
virtually certain affect basslet population dynamics. Finally, the interaction between
competition and susceptibility to predation could be further explored by designing
experiments that can effectively exclude predators (a manipulation that I was unable to
manifest).
In Chapter 5, I examined the role of recruitment and resident piscivores on the
demography of a variety of species of coral-reef fish on the Great Barrier Reef,
Australia. Resident predators decreased recruitment and increased mortality for all
species, but these effects varied considerably among species. These results highlight
the speed and extent to which patterns of settlement are modified, indicating that
caution should be exercised when attributing patterns of recruitment to patterns of
settlement.
Each of these chapters addressed the factors that determine the dynamics and
regulation of marine fish populations. When looking at each of these studies together,
several general conclusions emerge. First, density-dependent mortality was
consistently most pronounced for newly recruited fish. Such early post-settlement
mortality is likely to be a key bottleneck for a wide variety of marine fish populations
ranging from small coral reef species like this to larger, commercially important
species. Second, these studies highlighted the importance of predators in the
regulation of populations. Since such multi-species interactions were necessary for
regulation, a community, rather than single species, approach may be needed to meet
conservation goals. Finally, the world is currently facing a fisheries crisis where the
majority of marine fisheries are already fully or over-exploited (Botsford et al., 1997).
If we are to effectively manage and conserve marine fish populations we must first
know what are the mechanisms driving their population dynamics.
97
Literature Cited
Anderson, T. W. and Can, M. H. (1998). BINCKE: A highly efficient net for
collecting reef fishes. Environmental Biology of Fishes, 51, 111-115.
Asoh, K. (1992). Reproductive biology of the fairy basslet, Gramma loreto Poey,
Master's thesis, University of Puerto Rico, Mayaguez, pp 202.
Begon, M., Mortimer, M. and Thompson, D. J. (1996). Population Ecology, Blackwell
Science Ltd., London.
Bertness, M. D., Gaines, S. D., Stephens, E. G. and Yund, P. 0. (1992). Components
of recruiment in populations of the acorn barnacle Semibalanus balanoides
(Liimaeus). Journal of Experimental Marine Biology and Ecology, 156, 199215.
Betram, B. C. R. (1978). Living in groups: Predators and prey. In Behavioural
Ecology: an Evolutionary Perspective (Eds, Krebs, J. R. and Davies, N. B.)
Sinauer Associates Inc., Sunderland, MA, pp. 64-96.
Beukers, J. S. and Jones, G. P. (1997). Habitat complexity modifies the impact of
piscivores on a coral reef fish population. Oecologia, 114, 50-59.
Beukers, J. S., Jones, G. P. and Buckley, R. M. (1995). Use of implant microtags for
studies on populations of small reef fishes. Marine Ecology Progress Series,
125, 61-66.
Bohlke, J. E., and C.G. Chaplin (1993). Fishes of the Bahamas and adjacent tropical
waters, Livingston Publishing Co., Wynnewood, PA.
Booth, D. J. (1991). Larval settlement and juvenile group dynamics in the domino
damsel/Ish (Dascyllus albisella), Ph. D. thesis, Department of Zoology, Oregon
State University, Corvallis, OR.
Booth, D. J. (1992). Larval settlement patterns and preferences by domino damselfish
Dascyllus albisella Gill. Journal of Experimental Marine Biology and Ecology,
155, 85-104.
Booth, D. J. (1995). Juvenile groups in a coral-reef damselfish: Density-dependent
effects on individual fitness and population demography. Ecology, 76, 9 1-106.
98
Botsford, L. W., J. C. Castilla, and C. H. Peterson (1997). The management of
fisheries and marine ecosystems. Science 277:509-5 14
Buchheim, J. R. and Hixon, M. A. (1992). Competition for shelter holes in the coralreef fish Acanthemblemaria spinosa Metzelaar. Journal of Experimental
Marine Biology and Ecology, 164, 45-5 4.
Buckley, R. M., West, J. E. and Doty, D. C. (1994). Internal micro-tag systems for
marking juvenile reef fishes. Bulletin of Marine Science, 55, 848-857.
Caley, M. J. (1993). Predation, recruitment and the dynamics of communities of coralreef fishes. Marine Biology, 117, 33-43.
Caley, M. J., Carr, M. H., Hixon, M. A., Hughes, T. P., Jones, G. P. and Menge, B. A.
(1996). Recruitment and the local dynamics of open marine populations.
Annual Review of Ecology and Systematics, 27, 477-500.
Cappuccino, N. and Price, P. W. (1995). Population Dynamics: New Approaches and
Synthesis, Academic Press, San Diego.
Carr, M. H. (1998). Defining and measuring 'recruitment': is the bandwagon headed
straight to hell? In Reef Fish '95: Recruitment and Population Dynamics of
Coral Reef Fishes (Eds, Jones, G. P., Doherty, P. J., Mapstone, B. D. and
Howlett, L.) CRC Reef Research Center, Townsville, Australia, pp. 132-134.
Carr, M. H. and Hixon, M. A. (1995). Predation effects on early post-settlement
survivorship of coral-reef fishes. Marine Ecology Progress Series, 124, 31-42.
Caselle, J. E. (1999). Early post-settlement mortality in a coral reef fish and its effect
on local population size. Ecological Monographs, 69, 177-195.
Choat, J. H. (1991). Biology of herbivorous fishes on coral reefs. In The ecology of
fishes on coral reeft (Ed, Sale, P. F.) Academic Press, San Diego, California,
pp. 120-155.
Coates, D. (1980). Prey-size intake in humbug damselfish, Dascyllus aruanus (Pisces,
Pomacentridae) living within social groups. Journal ofAnimal Ecology, 49,
335-340.
Connell, J. H. (1983). On the prevalence and relative importance of interspecific
competition: evidence from field experiments. American Naturalist, 122, 661696.
Connell, J. H. (1985). The consequences of variation in initial settlement vs. postsettlement mortality in rocky intertidal communities. Journal ofExperimental
Marine Biology and Ecology, 93, 11-45.
Connell, S. D. (1996). Variations in mortality of a coral-reef fish: links with predator
abundance. Marine Biology, 126, 347-3 52.
Connell, S. D. (1997). The relationship between large predatory fish and recruitment
and mortality ofjuvenile coral reef-fish on artificial reefs. Journal of
Experimental Marine Biology and Ecology, 209, 261-278.
Connell, S. D. (1998). Effects of predators on growth, mortality and abundance of a
juvenile reef-fish: evidence from manipulations of predator and prey
abundance. Marine Ecology Progress Series, 169, 25 1-261.
Connell, S. D. (2000). Encounter rates of a juvenile reef fish with small and predatory
fishes. Copeia, 2000, 36-41.
Danilowicz, B. S. (1996). Choice of coral species by naive and field-caught
damselfish. Copeia, 1996, 735-739.
Doherty, P. and Fowler, A. (l994a). Demographic consequences of variable
recruitment to coral reef fish populations: a congeneric comparison of two
damselfishes. Bulletin of Marine Science, 54, 297-3 13.
Doherty, P. and Fowler, A. (l994b). An empirical test of recruitment limitation in a
coral reef fish. Science, 263, 935-939.
Doherty, P. J. (1981). Coral reef fishes: recruitment-limited assemblages? Proceedings
of the Fourth International Coral Reef Symp, 2, 465-470.
Doherty, P. J. (1982). Some effects of density on the juveniles of two species of
tropical, territorial damselfishes. Journal of Experimental Marine Biology and
Ecology, 65, 249-261.
Doherty, P. J. (1983). Tropical territorial damselfishes: is density limited by aggression
or recruitment? Ecology, 64, 176-190.
Doherty, P. J. (1991). Spatial and temporal patterns in recruitment. In The ecology of
fishes on coral reefs (Ed, Sale, P. F.) Academic Press, San Diego, California,
pp. 26 1-293.
Doherty, P. J. and Sale, P. F. (1985). Predation on juvenile coral reef fishes: an
exclusion experiment. Coral Reefs, 4, 225-234.
100
Doherty, P. J. and Williams, D. M. (1988). The replenishment of coral reef fish
populations. Oceanogr. Mar. Biol. Annu. Rev., 26, 487-551.
Ebeling, A. W. and Hixon, M. A. (1991). Tropical and temperate reef fishes:
comparison of community structures. In The ecology offishes on coral reefs
(Ed, Sale, P. F.) Academic Press, San Diego, California, pp. 509-563.
Eggleston, D. B. and Armstrong, D. A. (1995). Pre- and post-settlement determinants
of estuarine dungeness crab recruitment. Ecological Monographs, 65, 193-216.
Eggleston, D. B., Lipcius, R. N. and Grover, J. J. (1997). Predator and shelter-size
effects on coral reef fish and spiny lobster prey. Marine Ecology Progress
Series, 149, 43-59.
Ehrlich, P. R. (1975). The population biology of coral reef fishes. Annual Review of
Ecology and Systematics, 6, 211-247.
Elliott, J. K., Elliott, J. M. and Marsical, R. N. (1995). Host selection, location, and
association behaviors of anemonefishes in field settlement experiments.
Marine Biology, 122, 377-389.
Forrester, G. E. (1990). Factors influencing the juvenile demography of a coral reef
fish. Ecology, 71, 1666-1681.
Forrester, G. E. (1991). Social rank, individual size and group composition as
determinants of food consumption by the humbug damselfish, Dascyllus
aruanus. Animal Behaviour, 42, 701-711.
Forrester, G. E. (1995). Strong density-dependent survival and recruitment regulate the
abundance of a coral reef fish. Oecologia, 103, 275-282.
Forrester, G. E. (1998). Definitions and tests of recruitment limitation. In Reef Fish
'95: Recruitment and Population Dynamics of Coral Reef Fishes (Eds, Jones,
G. P., Doherty, P. J., Mapstone, B. D. and Howlett, L.) CRC Reef Research
Center, Townsville, Australia, pp. 13 5-139.
Freeman, S., and W. Alevizon (1983). Aspects of territorial behavior and habitat
distribution of the fairy basslet Gramma loreto. Copeia, 1983, 829-832.
Gaines, S. and Roughgarden, J. (1985). Larval settlement rate: a leading determinant
of structure in an ecological community of the marine intertidal zone. Proc.
Nat. Acad. Sci. (US.), 82, 3707-3711.
101
Goldberg, D. E. and Barton, A. M. (1992). Patterns and consequences of interspecific
competition in natural communities: a review of field experiments with plants.
American Naturalist, 139, 771-801.
Gotelli, N. J. (1988). Determinants of recruitment, juvenile growth, and spatial
distribution of a shallow-water gorgonian. Ecology, 69, 157-166.
Gurevitch, J., Morrow, L. L., Wallace, A. and Walsh, J. S. (1992). A meta-analysis of
competition in field experiments. American Naturalist, 140, 539-572.
Harrison, S. and Cappuccino, N. (1995). Using density-manipulation experiments to
study population regulation. In Population dynamics: new approaches and
synthesis (Eds, Cappuccino, N. and Price, P. W.) Academic Press, San Diego,
pp. 13 1-147.
Hixon, M. A. (1991). Predation as a process structuring coral reef fish communities. In
The ecology offishes on coral reefs (Ed, Sale, P. F.) Academic Press, San
Diego, California, pp. 475-508.
Hixon, M. A. (1998). Population dynamics of coral-reef fishes: controversial concepts
and hypotheses. Australian Journal of Ecology, 23, 192-201.
Hixon, M. A. and Beets, J. P. (1989). Shelter characteristics and Caribbean fish
assemblages: experiments with artificial reefs. Bulletin of Marine Science, 44,
666-680.
Hixon, M. A. and Can, M. H. (1997). Synergistic predation, density dependence, and
population regulation in marine fish. Science, 277, 946-949.
Hixon, M. A. and Webster, M. S. (in press). Density dependence in marine fishes:
Coral -reef populations as model systems. In Coral reeffIshes. Dynamics and
diversity in a complex ecosystem (Ed, Sale, P. F.) Academic Press, San Diego,
California.
Hobson, E. S., and J.R. Chess (1978). Trophic relationships among fishes and
plankton in the lagoon at Enewetak Atoll, Marshall Islands. Fishery Bulletin,
76, 133-153.
Hobson, E. S. (1991). Trophic relationships of fishes specialized to feed on
zooplankters above coral reefs. In The ecology offishes on coral reefs (Ed,
Sale, P. F.) Academic Press, New York, pp. 69-95.
Houde, E. D. (1987). Fish early life dynamics and recruitment variability. American
Fisheries Society Symposium Series, 2, 17-29.
102
Hunt von Herbing, I. and Hunte, W. (1991). Spawning and recruitment of the bluehead
wrasse Thalassorna bfasciatum in Barbados, West Indies. Marine Ecological
Progress Series, 72, 49-58.
Jenkins, T. M. (1969). Social structure, position choice and microdistrubution of two
trout species (Salmo trutta and Salmo gairdneri) residents in mountain streams.
Animal Behaviour Monographs, 2, 57-123.
Jones, G. P. (1 987a). Competitive interactions among adults and juveniles in a coral
reef fish. Ecology, 68, 1534-1547.
Jones, G. P. (1987b). Some interactions between residents and recruits in two coral
reef fishes. Journal of Experimental Marine Biology and Ecology, 114, 169182.
Jones, G. P. (1988). Experimental evaluation of the effects of habitat structure and
competitive interactions on the juveniles of two coral reef fishes. Journal of
Experimental Marine Biology and Ecology, 123, 115-126.
Jones, G. P. (1990). The importance of recruitment to the dynamics of a coral reef fish
population. Ecology, 71, 1691-1698.
Jones, G. P. (1991). Postrecruitment processes in the ecology of coral reef fish
populations: a multifactorial perspective. In The ecology offishes on coral
reefs (Ed, Sale, P. F.) Academic Press, San Diego, California, pp. 294-328.
Keough, M. J. and Downes, B. J. (1982). Recruitment of marine invertebrates: the role
of active larval choices and early mortality. Oecologia, 54, 348-352.
Koebele, B. P. (1985). Growth and the size hierarchy effect: an experimental
assessment of three proposed mechanisms; activity differences, disproportional
food acquisition, physiological stress. Environmental Biology of Fishes, 12,
181-188.
Luckenbach, M. W. (1984). Settlement and early post-settlement survival in the
recruitment of Mulinia lateralis (Bivalvia). Marine Ecology Progress Series,
17, 245-25 0.
Luckhurst, B. E., and K. Luckhurst (1977). Recruitment patterns of coral reef fishes on
the fringing reef of Curacao, Netherlands Antilles. Canadian Journal of
Zoology, 55, 68 1-689.
103
Luckhurst, B. E. and Luckhurst, K. (1978). Analysis of the influence of substrate
variables on coral reef fish communities. Marine Biology, 49, 3 17-323.
Mange!, M. (1990). Resource divisibility, predation and group formation. Animal
Behavior, 39, 1163-1172.
McFarland, W. N. (1991). The visual world of coral reef fishes. In The ecology of
fishes on coral reefs (Ed, Sale, P. F.) Academic Press, San Diego, California,
pp. 16-38.
McGuinness, K. A. and Davis, A. R. (1989). Analysis and interpretation of the recruitsettler relationship. Journal of Experimental Marine Biology and Ecology, 134,
197-202.
Meekan, M. G. (1988). Settlement and mortality patterns of juvenile reef fishes at
Lizard Island, northern Great Barrier Reef. Proceedings of the Sixth
International Coral Reef Symposium, 2, 779-784.
Menge, B. A. (2000). Recruitment vs. postrecruitment processes as determinants of
barnacle population abundance. Ecological Monographs, 70, 265-288.
Minchinton, T. E. and Scheibling, R. E. (1991). The influence of larval supply and
settlement on the population structure of barnacles. Ecology, 72, 1867-1879.
Munday, P. L. and Wilson, S. K. (1997). Comparative efficacy of clove oil and other
chemicals in anaesthetization of Pomacentrus amboinensis, a coral reef fish.
Journal of Fish Biology, 51, 93 1-938.
Murdoch, W. W. (1994). Population regulation in theory and practice. Ecology, 75,
27 1-287.
Murdoch, W. W. and Oaten, A. (1975). Predation and population stability. Advances
in Ecological Research, 9, 1-132.
Myers, J. H. and Rothman, L. D. (1995). Field experiments to study regulation of
fluctuating populations. In Population dynamics: new approaches and
synthesis (Eds, Cappuccino, N. and Price, P. W.) Academic Press, San Diego,
California, pp. 229-250.
Nemeth, R. S. (1998). The effects of natural variation in substrate architecture on the
survival of juvenile bicolor damselfish. Environmental Biology of Fishes, 53,
129-141.
104
Pauly, D., Christensen, V., Dalsgaard, J., Froese, R. and Tones Jr., F. (1998). Fishing
down marine food webs. Science, 279, 860-863.
Pitcher, T. J., and J.K. Parrish (1993). Functions of shoaling behaviour in teleosts. In
Behaviour of teleost fishes (Ed, Pitcher, T. J.) Chapman and Hall, New York,
pp. 363-439.
Randall, J. E. (1967). Food habits of the reef fishes of the West Indies. Studies in
Tropical Oceanography, 5, 665-847.
Robertson, D. R. (1996). Interspecific competition controls abundance and habitat use
of territorial Caribbean damselfishes. Ecology, 77, 885-899.
Robertson, D. R. (1998). Implications of body size for interspecific interactions and
assemblage organization among coral-reef fishes. Australian Journal of
Ecology, 23, 252-25 7.
Roughgarden, J. (1974). Species packing and the competition function with
illustrations from coral reef fish. Theoretical Population Biology, 5, 163-186.
Rubenstein, D. I. (1978). On predation, competition, and the advantages of group
living. In Perspectives in Ethology 3 , Vol. 3 (Ed, P.P.G. Bateson and P.H.
Klopfer) Plenum Press, New York, pp. 205-23 1.
Sale, P. F. (1974). Mechanisms of co-existence in a guild of territorial fishes at Heron
Island. Proceedings of the Second International Coral Reef Symposium, 1,
193 -206.
Sale, P. F. (1977). Maintenance of high diversity in coral reef fish communities.
American Naturalist, 111, 337-359.
Sale, P. F. (1 978a). Chance patterns of demographic change in populations of
territorial fish in coral rubble patches at Heron Reef. Journal of Experimental
Marine Biology and Ecology, 34, 233-243.
Sale, P. F. (1978b). Coexistence of coral reef fishes - a lottery for living space.
Environmental Biology of Fishes, 3, 85-102.
Sale, P. F. (1979). Recruitment, loss and coexistence in a guild of territorial coral reef
fishes. Oecologia, 42, 159-177.
Sale, P. F. and Dybdahl, R. (1975). Determinants of community structure for coral reef
fishes in an experimental habitat. Ecology, 56, 1343-1355.
105
Sale, P. F. and Dybdahl, R. (1978). Determinants of community structure for coral reef
fishes in isolated coral heads at lagoonal and reef slope sites. Oecologia, 34,
57-74.
Sale, P. F. and Ferrell, D. J. (1988). Early survivorship ofjuvenile coral reef fishes.
Coral Reefs, 7,117-124.
Schmitt, R. J. and Holbrook, S. J. (1996). Local-scale patterns of larval settlement in a
planktivorous damselfish: Do they predict recruitment? Marine & Freshwater
Research, 47, 449-463.
Schmitt, R. J. and Holbrook, S. J. (1999a). Mortality of juvenile damselfish:
implications for assessing processes that determine abundance. Ecology, 80,
35-50.
Schmitt, R. J. and Holbrook, S. J. (1999b). Settlement and recruitment of three
damselfish species: larval delivery and competition for shelter space.
Oecologia, 118, 76-86.
Schoener, T. W. (1983). Field experiments in interspecific competition. American
Naturalist, 122, 240-285.
Shenk, T. M., White, G. C. and Burnham, K. P. (1998). Sampling-variance effects on
detecting density dependence from temporal trends in natural populations.
Ecological Monographs, 68, 445-460.
Shepherd, J. G. and Cushing, D. H. (1980). A mechanism for density-dependent
survival of larval fish as the basis of a stock-recruitment relationship. .1 Cons.
i. Expior. Mer, 39, 160-167.
Shpigel, M. and Fishelson, L. (1991). Experimental removal of piscivorous groupers
of the genus Cephalopholis (Serranidae) from coral habitats in the Gulf of
Aqaha (Red -Sea). Environmental Biology of Fishes, 31, 131-138.
Shulman, M. (1985). Coral reef fish assemblages: Intra- and interspecific competition
for shelter sites. Environmental Biology of Fishes, 13, 8 1-92.
Shulman, M. J., Ogden, J. C., Ebersole, J. P., Mcfarland, W. N., Miller, S. L. and
Wolf, N. G. (1983). Priority effects in the recruitment ofjuvenile coral reef
fishes. Ecology, 64, 1508-15 13.
Smith, C. L. (1978). Coral reef fish communities: a compromise view. Landscape
Ecology, 3, 109-128.
106
Smith, C. L. and Tyler, J. C. (1972). Space resource sharing in a coral reef fish
community. Bull. Vat. Hist. Mus. Los Angeles Co., 14, 125-170.
Smith, T. D. (1994). Scaling Fisheries: The Science of Measuring the Effects of
Fishing, 1855-1955, Cambridge University Press, Cambridge, England.
Sogard, S. M. (1997). Size-selective mortality in the juvenile stage of a teleost fish: a
review. Bulletin of Marine Science, 60, 1129-1157.
Steele, M. A. (1997). The relative importance of processes affecting recruitment of
two temperate reef fishes. Ecology, 78, 129-145.
Steele, M. A.. Forrester, G. E. and Almany, G. R. (1998). Influences of predators and
conspecifics on recruitment of a tropical and a temperate reef fish. Marine
Ecology Progress Series, 172, 115-125.
Stewart, B. D. (1998). Interactions between piscivorous coral reeffishes and their
prey, Ph.D. Thesis. Department of Marine Biology, James Cook University.,
Townsville, Australia.
Stewart-Oaten, A. and Murdoch, W. W. (1990). Temporal consequences of spatial
density dependence. .Journal ofAnimal Ecology, 59, 1027-1045.
Sutherland. J. P. (1990). Recruitment regulates demographic variation in a tropical
intertidal barnacle. Ecology, 25, 1-45.
Sweatman, H. P. A. (1988). Field evidence that settling coral reef fish larvae detect
resident fishes using dissolved chemical cues. Journal of Experimental Marine
Biology and EcoIo', 124, 163-174.
Tupper, M. and Hunte, W. (1994). Recruitment dynamics of coral reef fishes in
Barbados. Marine Ecology Progress Series, 108, 225-23 5.
Turchin, P. (1995). Population regulation: old arguments and a new synthesis. In
Population dynamics: new approaches and synthesis (Eds, Cappuccino, N. and
Price, P. W.) Academic Press, San Diego, California, pp. 19-40.
Victor, B. C. (1983). Recruitment and population dynamics of a coral reef fish.
Science, 219, 419-420.
Victor, B. C. (1986). Larval settlement and juvenile mortality in a recruitment-limited
coral reef fish population. Ecological Monographs, 56, 145-160.
107
Victor, B. C. (1991). Settlement strategies and biogeography of reef fishes. In The
Ecology of Fishes on Coral Reefs (Ed, Sale, P. F.) Academic Press, San Diego,
pp. 23 1-260.
Webster, M. S. and Hixon, M. A. (2000). Mechanisms and individual consequences of
intraspecific competition in a coral-reef fish. Marine Ecology Progress Series,
196, 187-194.
Wilkinson, C. (Ed.) (2000) Status of coral reefs of the world: 2000, Australian
Institute of Marine Science, Townsville, Australia.
Williams, D. M. (1980). Dynamics of the pomacentrid community on small patch reefs
in One Tree Lagoon (Great Barrier Reef). Bulletin of Marine Science, 30, 159170.
Williams, D. M., English, S. and Milicich, M. J. (1994). Annual recruitment surveys
of coral reef fishes are good indicators of patterns of settlement. Bulletin of
Marine Science, 54, 314-331.