AN ABSTRACT OF THE THESIS OF
Dwayne W. Meadows for the degree of Doctor of Philosophy
in Zoology presented on 27 September 1994
Title: Patterns, Causes and Conseguences of Clustering of
Individual Territories of the Threespot Damselfish,
Stegastes planifrons.
Abs tract approved:
Redacted for Privacy
Mark A. Hix6n
The threespot damselfish, Stegastes planifrons,
maintains individual territories that are clustered on
coral patch reefs.
My objective was to understand the
effects of territory clustering on behavior and fitness.
Fish with territories in the center of a cluster had
(relative to edge fish): higher mating success (number of
eggs), higher aggressive chase rates with conspecifics,
lower chase rates to heterospecifics, lower overall chase
rates, lower grazing rates by intruders, and smaller
territories.
Feeding rate, survivorship, and age at
maturity did not vary with territory position.
Therefore,
central fish appeared to have higher fitness, which was
probably related to the lower energetic costs of territory
defense there.
Center and edge territories differed in habitat
complexity, and the density of potential algal
competitors, egg predators, and various food and
invertebrate species.
These microhabitat features could
provide different quality shelter, nest or feeding sites
and thus might explain the positional differences in
fitness.
An experiment in which I changed the position of
treatment fish from the center to the edge of a cluster,
without altering microhabitat, showed that position per
Se, and not microhabitat variation, caused the center-edge
differences.
Vacated space in the center of a cluster was fought
over more vigorously and reoccuppied sooner than similar
space on the edge.
Settlement to one of two depopulated
clusters was preferentially to the cluster center.
These
data indicated that threespots compete for the more
desirable central positions.
Therefore, these populations
can be considered simultaneously recruitment limited (in
terms of local population size) and resource limited (in
terms of local reproductive output and perhaps global
population size).
Aggressive chases with conspecifics were lower on the
cluster edge than at any distance toward the center, while
chases to heterospecifics had the opposite pattern.
The
results of chases with conspecifics did not fit the
predictions of the model by Stamps et al.
(1987)
.
discrepancy may be a result of habituation between
territorial neighbors.
This
©Copyright by Dwayne W. Meadows
27 September 1994
All Rights Reserved
Patterns, Causes, and Consequences of Clustering of
Individual Territories of the Threespot Damselfish,
Stecastes Dianifrons
by
Dwayne W. Meadows
A THESIS
submitted to
Oregon State University
in partial fulfillment of
the requirements for the
degree of
Doctor of Philosophy
Completed 27 September 1994
Commencement June 1995
Doctor of Philosophy thesis of Dwayne W. Meadows presented
on 27 September 1994
APPROVED:
Redacted for Privacy
Major Professor, 'representing Zoology
Redacted for Privacy
Heady Department of Zoology
Redacted for Privacy
Dean of Q±aUuate Sclaóbl
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 upon request.
Redacted for Privacy
Dwayne W. Meadows, author
TABLE OF CONTENTS
CHAPTER I: GENERAL INTRODUCTION
........... 1
References................... 5
CHAPTER II: CLUSTERED TERRITORIES: POSITIONAL
DIFFERENCES IN BEHAVIOR, TERRITORY SIZE, AND
FITNESS MEASURES IN A DAMSELFISH
........ 8
.................... 8
Introduction .................. 10
Abstract
Methods..................... 13
..................... 22
Discussion ................... 33
Acknowledgements ................ 49
Results
References................... 50
CHAPTER III: CENTER-EDGE DIFFERENCES IN BEHAVIOR AND
TERRITORY SIZE IN CLUSTERS OF TERRITORIAL
DANSELFISH: GROUPING OR MICROHABITAT VARIATION?
....................
Introduction ..................
Methods .....................
Results .....................
Abstract
56
56
57
63
71
Discussion................... 86
................ 94
................... 95
Acknowledgements
References
CHAPTER IV: COMPETITION WITHOUT RESOURCE
LIMITATION?: EVIDENCE FROM CLUSTERS OF
INDIVIDUALLY TERRITORIAL THREESPOT DANSELFISH,
STEGASTES PLANIFRONS
.............. 99
Abstract .................... 99
Introduction .................. 100
TABLE OF CONTENTS, Continued.
Methods..................... 104
Results..................... 107
Discussion................... 114
Acknowledgements ................ 124
References ................... 125
CHAPTER V: EFFECTS OF HABITAT GEOMETRY ON
TERRITORIAL DEFENSE COSTS IN A DANSELFISH
.
.
.
.
129
Abstract ..................... 129
.................. 130
Methods ..................... 133
Results ..................... 133
Introduction
...................
134
Acknowledgements ................
137
References...................
138
Discussion
CHAPTER VI: DIEL, LUNAR AND SEASONAL PATTERNS IN
REPRODUCTIVE AND TERRITORIAL BEHAVIOR OF THE
THREESPOT DAMSELFISH, STEGASTES PLANIFRONS
.
.
.
140
Abstract .................... 140
Introduction .................. 141
Methods ..................... 144
Results..................... 148
Discussion................... 158
Acknowledgements ................ 166
References ................... 167
CHAPTER VII: SUMMARY ................. 171
BIBLIOGRAPHY ..................... 173
LIST OF FIGURES
Chapter II:
1.
Diagrammatic map of a typical patch reef
supporting a cluster of Stegastes planifrons
territories...................
2.
Persistence of marked
planifrons in each
cluster position on Tiantupo #1W from July 1992
to April 1993
24
Body size (mm SL) of S. planifrons for each
cluster position and site
25
.
.................
3.
4.
............
Growth (mm SL) of marked
planifrons in each
cluster position on Tiantupo #1W from July to
December 1992, December 1992 to April 1993, and
.
overall.....................
5.
7.
30
S. planifrons territory size for each cluster
position and site
32
planifrons agonistic interactions with
conspecific and heterospecific intruders for
each cluster position and site
34
Rate of food stealing by intruders from within
S. planifrons territories for each cluster
position and site
35
.
...............
.
.........
8.
26
Mating success of
planifrons males in each
cluster position in August 1992 and June 1993
from Smithsoniantupo #1
............
6.
15
................
Chapter III:
1.
Diagrammatic representation of the experimental
design on a single patch reef
2.
Habitat complexity in each of the four
microhabitat types
3.
Bray-Curtis ordination of the abundances of the
18 most common benthic taxa for all 96 samples
from the four microhabitat types ........
.......... 68
............... 73
74
LIST OF FIGURES, Continued.
4.
Mean parrotfish feeding rates in S. planifrons
territories belonging to the three experimental
groups..................... 79
5.
6.
Mean territory size (cm2) of
planifrons in
the three treatment groups of the experiment
.
.
.
80
Behaviors of S. planifrons in the three
experimental groups: A) chases with
conspecifics, B) chases with heterospecifics,
C) feeding rates by intruders within
planifrons territories, D) benthic feeding
rates of occupant damselfish
.
.......... 81
7.
Graphical model of the effect of habitat or
cluster edge-to--area ratio on population
density or reproductive output
......... 92
Chapter IV:
1.
A) Intraspecific, and B) interspecific
aggressive chase rates by
planifrons
reoccupying vacated territory sites following
the experimental removal of center vs edge
individuals
.
................... 111
2.
Diagrammatic representation of local vs global
populations in open systems
3.
Limitation of local and global populations
........... 120
.
.
.
.
121
Chapter V:
1.
Chases of S. planifrons with A) conspecifics,
and B) heterospecifics for each of four
positions within a cluster of territories
.
.
.
.
135
Chapter VI:
1.
Benthic feeding rates of
planifrons by time
of day and position within a cluster of
.
territories................... 149
2.
Lunar variation in behaviors of
planifrons by
position in a cluster of territories
......
.
153
LIST OF FIGURES, Continued.
3.
Seasonal variation in behaviors of
planifrons
by position in a cluster of territories .....
.
159
LIST OF TABLES
Chapter II:
1.
AMOVA results for
2.
ANCOVA results for
3.
ANCOVA results for S. planifrons benthic feeding
4.
ANCOVA results and raw data (x and se) for
planktonic feeding of
planifrons
37
ANCOVA results for
planifrons agonistic
interactions with intruders
38
ANCOVA results for feeding by intruders within
S. planifrons territories
40
planifrons body size (SL)
.
.
planifrons territory size
6.
.
28
.
28
.
36
.......
.
5.
.
.
...........
............
Chapter III:
1.
2.
Patch area (cm2) and percent cover (± Se) of
five substrates in each of the four
microhabitat types on patch reefs containing
clusters of threespot damselfish territories
.
.
Percent cover of algal and live invertebrate
taxa in the four microhabitat types on patch
reefs containing clusters of threespot
damselfish territories
.............
3.
4.
5.
Repeated measures ANOVA results for the feeding
rate of parrotfish on the experimental reefs
.
Repeated measures ANOVA results for territory
size of S. planifrons on the experimental reefs
Repeated measures ANOVA results of
behaviors during the experiment
76
.
82
.
83
planifrons
.........
.
75
84
Chapter IV:
1.
Relative frequencies of reoccupation times by S.
planifrons into experimentally vacated
territories by position within a cluster
.
.
.
.
109
LIST OF TABLES, Continued.
2.
3.
Repeated measures ANOVA results for chase rates
by S. planifrons toward conspecifics and
heterospecifics during reoccupation of
experimentally vacated territories
.......
112
Center vs edge frequency distributions of
planifrons on two patch reefs before and after
experimental depopulation, and calculated
frequencies based on random distribution of
actual settlers to available habitat ......
115
.
Chapter VI:
1.
Aggressive interactions and intruder feeding
rates within
planifrons territories with
time of day
150
Mean courtship and foray rates (± Se) by time of
day and position within a cluster of
territories in S. planifrons
151
...................
.
2.
..........
3.
4.
Cross correlations between behaviors and a lunar
cycle represented by a 29 day period sine curve
.
Pearson correlations among behaviors for each
position in a cluster of territories for the
lunar cycle data
157
Pearson correlations among behaviors for each
position in a cluster of territories for the
seasonal data
161
................
5.
155
..................
Patterns, Causes, and Consequences of Clustering of
Individual Territories of the Threespot Damselfish,
Stegastes planifrons
CHAPTER I: GENERAL INTRODUCTION
One of the primary goals of ecological research is to
understand the processes that determine the distribution
and abundance of species.
Moreover, an appreciation of
the behavioral interactions that often cause particular
patterns of distribution and abundance provides knowledge
about the mechanisms and evolutionary significance of
these processes.
This research considers the behavioral
and ecological role of two of these processes:
territoriality and grouping.
Territoriality, the exclusive use of space maintained
by defense against intruders, has long been recognized as
an important process that can potentially limit the
abundance of species (see Brown and Orians 1970, Newton
1992) .
Clearly, the maximum abundance of animals a
particular area can support is determined by the number of
territories that fit inside that area.
Food abundance,
competitor density and nest and shelter availability are
all factors that have been shown to affect territory
presence and/or size (Hixon 1980 and 1981, Mares and
Lacher 1987, Schoener 1983, Temeles 1987, Wolff 1993).
Grouping of individuals is another process affecting
species behavior and ecology.
Examples of such groups
include schools, flocks, herd, colonies and leks.
Grouping can affect the costs and benefits of feeding
(Pitcher 1986, Rayor and Uetz 1990, Burger and Gochfeld
1991), predation rates on young or adults (through the
"selfish herd" theory of Hamilton 1971 in which central
individuals are shielded from predators by more peripheral
neighbors), fluid dynamics and locomotor efficiency
(Pitcher 1986)
,
mate access and reproductive success
(Rippin and Boag 1974), competition (Hoogland and Sherman
1976, Robertson et al. 1976), disease transmission and
cuckoldry risk (Hoogland and Sherman 1976), and heat flux
(Hayes et al. 1992) or water loss (Heinen 1993).
Often
these costs and benefits vary with position in a group as
well as among groups of different sizes.
Center positions
in groups often have higher net benefits than edges.
For
example, predation risk is lower (Coulson 1968, Gross and
MacMillan 1981, Foster 1989, Rayor and Uetz 1990), while
feeding rates (Burger and Gochfeld 1991, McRae et al.
1993) and mating success (Coulson 1968, Rippin and Boag
1973, Rayor and Uetz 1990) are higher in the center of
some groups.
Grouping can be due either to behavioral interactions
and choices or to the patchiness of suitable habitat.
use the term "grouping" for the former case and define
I
3
tclusteringtt as aggregations due to habitat patchiness or
undetermined factors.
In many species, individuals are both territorial and
occur in groups or clusters of territories.
Much less is
known about the effects of grouping or clustering by
territorial individuals on within group patterns in
behavior, territory size and fitness.
Only territorial
bird and fish species which nest for a short part of the
year are well studied for even a few of the potential
costs and benefits (see above), while permanently
territorial species are poorly studied in this regard (but
see Foster 1989, Rayor and Uetz 1990) .
However, long-term
territoriality may prevent rapid adjustment of the various
costs and benefits associated with group position and may
therefore affect fitness more than for species which can
readily alter group position.
Other less direct evidence suggests that grouping of
territorial individuals has important effects.
Theoretical models by Stamps et al.
(1987) predict that
defensive behavior should vary with position in a group of
territorial individuals.
Observational data show that
territory size varies with cluster position, usually edge
territories are larger than central territories (Young
1951, McCartan and Simmons 1956, Delius 1965, Southern and
Lowe 1968, Krebs 1971, Wiens 1973, Seastadt and MacLean
1979), but the causes of this pattern were unstudied
experimentally before I completed my research.
4
Therefore, the main objective of my research was to
examine in detail one species with clustered, individual
territories so as to more comprehensively understand the
role of territoriality and grouping in affecting a species
distribution, abundance and fitness.
I chose the
threespot damselfish, Stegastes planifrons, for this
research.
This species is an ideal subject because it is
found in clear, shallow, and warm waters of the tropical
Atlantic and Caribbean, which permits easy, long-term
observation.
Other useful characteristics of this species
are that territories are small (< 1m2) and maintained
year-round, behaviors are readily observed and unaffected
by the presence of nearby scientists, and reproductive
success is easily monitored because females deposit eggs
in nests on the substrate inside male territories.
The
territories are found clustered together on suitable
patches of coral which, in my study, ranged in size from
10 to over 1000 m2 and were scattered throughout the study
site.
In chapter II, I describe the patterns in aggressive
behavior, feeding, growth, territory size, survival, and
mating success (i.e., fitness measures) between threespot
damselfishes with territories in the center and on the
edge of clusters.
Chapter III documents center-edge
differences in microhabitat features of territorial
clusters.
I then report an experiment designed to test
whether the center-edge differences in behavior and
5
territory size found in chapter I were due to the effects
of an individual's position relative to other cluster
members (i.e., analagous to a selfish-herd effect), or to
the differences in microhabitat between the cluster
positions.
In chapter IV, I test whether there is
competition among the damselfish to obtain residence in
the more desirable central positions of a cluster.
Such
competition may not occur despite the differences in
fitness measures associated with each cluster position,
because, for instance, chance settlement position, strong
prior residence effects, and few opportunites for movement
may not allow it.
Chapter V documents fine-scale spatial
variation in territorial defense against both conspecifics
and heterospecifics in order to test predictions of models
by Stamps et a?.
(1987) on the effects of habitat geometry
on defense costs.
Finally, chapter VI examines temporal
patterns in reproductive and territorial behavior on diel,
lunar, and seasonal scales.
References
Brown, J. L. and G. H. Orians. 1970.
Spacing patterns in
mobile animals. Ann. Rev. Ecol. Syst. 1:239-262.
Burger, J., and M. Gochfeld. 1991.
Vigilance and feeding
behavior in large feeding flocks of laughing gulls,
Larus atricilla, on Delaware Bay. Est. Coast. Shelf
Sci. 32:207-212.
Coulson, J. C. 1968.
Differences in the quality of birds
nesting in the centre and on the edges of a colony.
Nature 217:478-479.
A population study of skylarks,
Delius, J. D. 1965.
Alanda arvensis. Ibis 107:466-492.
The implications of divergence in
Foster, S. A. 1989.
spatial nesting patterns in the geminate Caribbean
and Pacific seargent major damselfishes. Anim. Behav.
37:465-476.
Gross, M. R. and A. M. MacMillan. 1981. Predation and the
evolution of colonial nesting in bluegill sunfish
(Lepomis macrochirus). Behav. Ecol. Sociobiol. 8:163174.
Hamilton, W. D. 1971. Geometry for the selfish herd. J.
Theor. Biol. 31:295-311.
Hayes, J. P., J. R. Speakman and P. A. Racey. 1992. The
contributions of local heating and reducing exposed
surface area to the energetic benefits of huddling by
short-tailed field voles (Microtus agrestis)
Physiol. Zool. 65:742-762.
Aggregations of newly metamorphosed
Heinen, J. T. 1993.
Bufo americanus: tests of two hypotheses. Can. J.
Zool. 71:334-338.
Hixon, M. A. 1980. Food production and competitor density
as determinants of feeding territory size. Am. Nat.
115:510-530.
An experimental analysis of territoriality
1981.
in the reef fish Embiotoca jacksoni (Embiotocidae).
Copeia 1981:653-665.
Hoogland, J. L. and P. W. Sherman. 1976. Advantages and
disadvantages of bank swallow (Riparia riparia)
coloniality. Ecol. Monogr. 46:33-58.
Krebs, J. R. 1971. Territory and breeding density in the
great tit, Parus malor. Ecology 52:2-22.
Social spacing in
Mares, M. A. and T. F. Lacher. 1987.
small mammals: patterns of individual variation. Am.
Zool. 14:81-96.
Territory in the
McCartan, L. and K. E. L. Simmons. 1956.
great crested grebe, Podiceps crustatus, reexamined.
Ibis 98:370-378.
McRae, S. B., P. J. Weatherhead and R. Montgomrie. 1993.
American robin nestlings compete by jockeying for
position. Behav. Ecol. Sociobiol. 33:101-106.
7
Experiments on the limitation of bird
Newton, I. 1992.
Res. Rev. 67:129numbers by territorial behavior.
193.
Functions of shoaling behaviour in
Pitcher, T. J. 1986.
teleosts. pp. 294-337. In: T.J. Pitcher (ed.). The
Behaviour of Teleost Fishes. Johns Hopkins University
Press, Baltimore.
Trade-of fs in foraging
Rayor, L. S. and G. W. Uetz. 1990.
success and predation risk with spatial position in
Behav. Ecol. Sociobiol. 27:77-85.
colonial spiders.
Rippin, A. B. and D. A. Boag. 1974. Spacial organization
among male sharp-tailed grouse on arenas. Can. J.
Zool. 52:591-597.
Simple models of optimal feedingSchoener, T. W. 1983.
territory size: a reconciliation. Am. Nat. 121:608629.
Territory size
Seastadt, T. R. and S. F. MacLean. 1979.
and composition i n relation to resource abundance in
lapland longspurs breeding in arctic Alaska. Auk
96:131-142.
The pattern and
Southern, H. N. and R. W. Lowe. 1968.
distribution of prey and predation in Tawny owl
territories. J. Anim. Ecol. 37:75-97.
The
Stamps, J. A., M. Buechner and V. V. Krishnan. 1987.
effects of habitat geometry on territorial defense
costs: intruder pressure in bounded habitats. Am.
Zool. 27:307-326.
The relative importance of prey
Temeles, E. J. 1987.
availability and intruder pressure in feeding
territory size regulation by harrier, Circus cyaneus.
Oecologia 74:286-297.
Interterritorial habitat variation in
Wiens, J. A. 1973.
Grasshopper and Savanah sparrows. Ecology 54:877-884.
Wolff, J. 0. 1993.
Why are female small mammals
territorial. Oikos 68:364-370.
Territorial behavior in the Eastern
Young, H. 1951.
Robin. Proc. Linn. Soc N.Y. 5:1-37.
[1
CHAPTER II: CLUSTERED TERRITORIES: POSITIONAL DIFFERENCES
IN BEHAVIOR, TERRITORY SIZE AND FITNESS MEASURES IN A
DAMS ELF I SH
DWAYNE W, MEADOWS
Department of Zoology
Oregon State University
Corvallis, OR 97331-2914, U.S.A.
Abstract
The effect of spatial position in a group on
behavior, territoriality, and fitness measures was studied
in the permanently territorial threespot damselfish,
Stegastes planifrons, of the Caribbean.
Threespots have
individual territories, groups of which are clustered on
patches of coral.
Survival did not vary between fish
resident on the center or edge position of a cluster.
Central fish were larger and grew faster than edge fish,
while age did not vary by position.
Central males
received significantly more clutches, eggs/clutch, and
cumulative number of eggs to defend than fish on the
cluster edge.
edge fish.
Central fish had smaller territories than
These patterns suggest that damselfish with
center territories have higher fitness, and that this
position should be preferred.
Since territory position is
maintained for long periods in this species, site
selection may have a substantial impact on lifetime
fitness.
I also examined behaviors that might explain
fitness differences between center and edge territories.
Feeding and courtship rates, and forays away from the
territory, did not differ by position within a cluster.
Aggressive interactions with conspecifics were slightly
more frequent for central fish, but interactions with
heterospecifics (especially parrotfish), and overall
interactions, occurred at much lower rates for fish in
central positions.
Edge fish lost the benthic algal food
in their territories at a significantly higher rate to
heterospecific intruders.
These behavioral data suggest
that the positional differences in fitness measures and
territory size are due to the lower energy costs of
territory defense for central fish, permitting more
investment in growth and reproduction.
These results also imply that the relative impact of
intra- and interspecific competitors on territory size
depends on the position of a territory in a habitat
cluster.
Finally, habitat size and shape may affect the
density and reproductive output of populations by altering
the relative amount of center and edge territories.
This
relative increase in edge territories may be a result of
habitat fragmentation as well.
10
Introduction
The spatial position of an individual in a group of
animals relative to other members may affect that
individual's behavior, ecology, survival and ultimately,
fitness.
For instance, predation risk is often lower in
the center of a group, both for juveniles and adults in a
diversity of taxa (Coulson 1968, Milinski 1977, Okamura
1986, Rayor and Uetz 1990, Krause 1993a; but see Parrish
1989), and also for eggs (Coulson 1968, Hoogland and
Sherman 1976, Gates and Gysel 1978, Gross and Macmillan
1981, Foster 1989).
McKaye et al.
(1992) describe an
interspecific example in which catfish fry have lower
predation rates when in mixed schools with cichlid fry
because the catfish use the central school positions.
In
contrast, feeding may be better on the edge of a group
(Rayor and Uetz 1990, 1993, Black et al. 1992), though
centers can also be favored as feeding positions (Burger
and Gochfeld 1991, McRae et al, 1993) .
Water loss is
thought to be lower in the center of invertebrate groups
at low tide and in frogs (Heinen 1993).
In many lekking
and colonial species, centrally located males achieve
higher mating success (Coulson 1968, Wiley 1973, Rippin
and Boag 1973, Rayor and Uetz 1990, and Gratson et al.
1991)
.
In some cases, positions other than center or edge
are favored.
For instance, the front or back of a group
11
can have greater feeding rates (Krause 1993b) or predation
risk (Parrish 1989)
In most of the above examples, participation in a
group seems to be a behavioral choice of the individual,
though often mediated by interactions with other group
members.
However, grouping and group position may also be
determined by factors external to the individual or group.
For instance, in species that live in habitats where only
some patches are usable, grouping may be a result of
habitat patchiness and not choice.
It may often not be
possible to determine the cause of grouping
priori
(Robertson et al. 1979, Gross and MacMillan 1981, Stamps
1988, Foster 1989, Shapiro 1991).
Therefore, I
distinguish utgroupingt! by behavioral choices and
interactions (e.g., schools, flocks, colonies, leks) from
IclusteringIt, aggregations caused by habitat patchiness,
external or undetermined factors.
The permanence of position or membership in a cluster
or group can vary tremendously (Petit and Bildstein 1987,
Parrish 1989, Rayor and Uetz 1990, Krause l993a), lasting
seconds, minutes or longer in schools and flocks to a
single mating season in leks and colonies.
Rapid position
change permits individuals to alter the relative costs and
benefits of feeding, predation risk and other factors so
as to presumably increase fitness.
However, position in a
group or cluster may also be more permanently fixed if
determined early in life and not readily changed, such as
12
for permanently territorial species.
In these species it
is more difficult to determine whether cluster membership
and position are behaviorally chosen or imposed by habitat
patchiness.
Individual fitness may be less readily
maximized in this case as well because position change is
rare.
As reviewed above, more is known about the effects
of position on behavior and fitness in more dynamic and
behaviorally chosen groups than for clusters where
individuals are more permanently site-attached.
Here, I test the hypothesis that there are
differences between center and edge territories in fitness
measures in a permanently territorial coral-reef
damselfish from the Caribbean.
I then link these position
differences in fitness to more proximate variation in
energy budgets related to feeding and aggressive behavior.
While theoretical studies suggest that behavioral
interactions should vary with position in a cluster of
territorial individuals (Stamps et al. 1987), specific
predictions depend on how each species of intruder is
affected by cluster boundaries.
Each species can respond
differently so that the overall outcome cannot be
predicted a priori.
To comprehensively examine the effect of spatial
position on fitness requires quantifying the success of
all offspring of the individual in question.
course difficult to do in most systems.
This is of
My best estimate
of fitness in this damselfish is lifetime reproductive
13
success.
Lifetime reproductive success is the product of
two basic components: hatching success per mating cycle
and number of mating cycles in a lifetime.
The number of
mating cycles is a function of survival, growth, and age
at maturity.
Hatching success per mating cycle depends on
offspring production (mating success) and offspring
survival until hatching.
It is these latter fitness
measures which I compare between cluster positions.
Methods
Study species
The threespot damselfish, Stegastes planifrons,
maintains individual year-round territories less than 1 m2
in area, within which they feed on various micro- and
macroalgal species cultivated in a
"lawn'1
(Brawley and
Adey 1977, Label 1980, de Ruyter van Steveninck 1984,
Hinds and Ballantine 1987).
Male territories also contain
nests in which the males protect demersally spawned eggs,
which remain in the territory for 4-5 days until hatching
(Robertson et al. 1990).
The planktonic larvae then
develop for a further 17-25 days before settlement back to
a reef as juveniles (Wellington and Victor 1989)
Territories are defended against conspecifics of both
sexes and a variety of other herbivores (e.g.,
parrotfishes, surgeonfishes, sea urchins) , egg predators,
14
and other carnivores (e.g., wrasses)
(Myrberg and Thresher
1974, Thresher 1976 and 1979, Williams 1978 and 1981,
Robertson 1984, Ebersole 1985).
Movement to new territory
locations is rare (see below)
Study site
The research was carried out at the San Bias Marine
Laboratory of the Smithsonian Tropical Research Institute
Many coral patch reefs
on the Caribbean coast of Panama.
within 2 km of the lab were utilized (references to
specific reefs herein can be found in the map of Robertson
1987).
Individual territories were clustered on coral
patch reefs from 1 to 25 m in depth and ranged in size
from 1 to > 1000 m2 (Fig. 11.1) .
I studied reefs from 1-
10 m in depth and 40 to 300 m2 in area.
These patch reefs
consisted mainly of the scleratinian coral Agaricia
agaricites, which comprised the bulk of the substrate, and
the encrusting corals Millepora
p., with smaller amounts
of other typical Caribbean coral species.
The
distribution of coral species was similar in each
position.
The patch reefs were surrounded by sand or
seagrass beds.
.
planifrons occupied all parts of a patch
reef, though all of the substrate is not within damselfish
territories (Robertson et al. 1981)
.
Other territorial
damselfish, notably the bicolor, Stegastes partitus, are
15
Diagrammatic map of a typical patch reef
Figure 11.1.
supporting a cluster of Stegastes planifroflS territories.
See text for details.
IJ
I
0
JI1JJi
K'
'- -I
Territory position:
Centre
EcTge
Buffer (not studied)
Patch reef boundary
C
bicolor damselfish territory
16
also found on these reefs, but in low abundances (e.g.,
Fig. 11.1).
I divided clusters of territories into two parts,
center and edge (Fig. 11.1) .
"Central" areas were greater
than 2.Om from the edge of the cluster, while "edges" were
the edge territories of the cluster and usually coincident
This left a buffer
with the edge of the reef substrate.
zone of territories between the edge and center which were
not examined.
Survival, body size,
and growth
I measured individual life-history features in order
to estimate the positional differences in potential
reproductive lifetime.
Growth and survivorship were
followed for 40 fish in each position on Tiantupo reef
#1W.
Fish were initially caught in July 1992 using small
monofilament hand nets while being distracted by the
presence of a conspecific in a bottle.
Each fish was then
individually measured and marked j, situ with a
subcutaneous injection of alcian-blue dye.
The fish were
then released back onto their territory after an absence
of only 2-3 mm.
Only one fish disappeared in the two
days following tagging, and this fish was replaced by
another tagged individual.
The marked fish were then
censused every 7-10 days for the next five months.
fish was not present in its territory,
If a
I searched the
surrounding area in case the fish had moved.
Such
17
movement occurred once when a fish was found two meters
from its original territory.
Because I could not
distinguish between mortality and emigration, I measured
Ilpersistencet! and not survival per se.
In December 1992
the fish were recaptured and remeasured to obtain growth
over the period and then were remarked and released.
The
fish were then recensused and again measured in April
1993.
This allowed me to also compare wet vs dry season
growth since the two census periods for growth coincided
with these seasons.
I analyzed the growth data with one-
way ANCOVA's with fish size as a covariate.
Survival was
analyzed with the logrank test (Hutchings et al. 1991).
Body size was visually estimated for the same fish on
which behavioral observations were taken (see below)
For aging, 30 center and 25 edge fish were caught
from Smithsoniantupo #1 in June 1993.
All otoliths were
removed and preserved in 90% buffered alcohol.
I counted
increments on the asteriscus otolith from each fish under
a compound microscope after embedding the otolith in
Crystalbond 509 (Aremco Products, Inc., N.Y.).
Because I
did not validate the time period for each increment I
cannot assign an absolute age to each fish.
Nevertheless,
relative comparisons of increment number provided a
reasonable basis for comparing age in the two positions.
I analyzed these data with a two-way ANCOVA with position
and sex as factors and size as a covariate.
Hatchiflg success
I compared hatching success, the second component of
lifetime reproductive success, by monitoring the presence
of egg clutches in male nests every other day during the
monthly spawning cycles in August 1992 and June 1993 on
Smithsoniantupo #1.
In 1992 I monitored 20 males each in
both the center and edge, while in 1993 I followed 20
central and 16 edge males.
A spawning cycle involved a
three-week period during which males can receive eggs
followed by a one-week period before full moon during
which spawning ceases (Robertson et al. 1990) .
Since the
eggs remained in the territories for 4-5 days before
hatching, I was able to monitor the number, size and
survival of clutches because I would see all clutches at
least twice.
Because the eggs were numerous, small and
laid in a fairly uniform monolayer, I used the area of
each clutch as a measure of mating success (Petersen 1990,
Itzkowitz 1991).
Seven clutches examined in the lab
revealed that egg density was 230 ± 14 eggs/cm2 (5 ± Se)
Clutch survival between positions was tested with a G
test-of-independence.
During the November-December 1992 and June 1993
spawning cycles,
I watched actual spawning events daily,
which occur in the first two hours after sunrise.
I
marked the territory location of each member of the mating
pair and measured the distance between their territories.
These data were used to determine whether fish in either
3-9
position had to travel farther (at a potentially greater
cost in energy or extra risk of predation on themselves or
their abandoned food or eggs) to acquire a suitable mate.
I mapped the position of all males and females I could
identify on this reef in December 1992 in order to examine
the spatial distribution of the sexes, which could vary
for example if center positions are preferred male nest
sites with higher offspring survival.
Territory size
I compared territory size in center vs edge of a
cluster by observing the location of each damselfish
continuously for 20 mm.
During that time I marked the
location of all feeding bites and aggressive interactions
on a rough map of the territory.
Since agonism was rare,
I found it more expedient to also use feeding bite
locations to measure territory size.
After the
observation, I placed from 5-9 small aluminum tags around
the edge of the territory based on my map.
I then
measured territory area by placing a series of marked
quadrats over the territory.
My measure of "territory
size" was thus more properly a measure of feeding range,
since territories are usually defined in terms of the
location of agonistic interactions (Kaufmann 1983).
However,
I did measure 18 territories from both central
and edge positions, using both the above method and by
20
marking the location of only agonistic interactions over
separate 40 mm
periods.
There was no significant
difference in territory size measured by these two methods
(t = 0.36, df = 17, p = .72, paired t-test) .
Thus, my
method of territory measurement reflected the actual
defended territory size (but see Robertson et al. 1981).
I quantified territory size during 1991 for 20 fish
in each position, center and edge, on each of 2 patch
reefs, Smithsoniantupo #1 and Tiantupo #lE, for a total of
80 territories.
I analyzed these data with a two-way
ANCOVA with position and reef as factors and fish size as
a covariate.
I include reef as a factor to test whether
the patterns were consistent at the scale of patch reefs.
Behavior
I compared center versus edge differences in behavior
of resident fish in order to examine the proximate factors
that might explain the differences in fitness measures.
My standard method of behavioral observation consisted of
10 mm
focal-animal activity budgets during which I
counted all agonistic interactions (both intra- and
interspecific), benthic feeding bites by residents and
intruders, courtship behavior (consisting of males
approaching females and doing characteristic dipping
motions in front of or around a female, Itzkowitz 1978),
and 'forays" away from the territory (Itzkowitz 1978,
21
Bartels 1984)
.
Forays may have a number of functions:
male forays often end in courtship bouts while other
forays may permit assessment of potential mates,
competitors, or potential territory sites (Itzkowitz 1978,
Bartels 1984)
occurs in
.
.
Planktonic feeding also facultatively
planifrons.
I could not count bites while
.
planifrons was plankton feeding, so I timed all plankton
feeding bouts.
For analysis of benthic feeding rates, I
adjusted benthic feeding bites by standardizing to 10 mm
of benthic feeding time and analyzed both the raw and
adjusted data.
The results did not differ so I present
only the raw data.
I visually estimated body size (SL) to
the nearest 5 mm.
In 1991 I quantified the activity budgets of 50 fish
in each position on each of three reefs (the same two as
for territory size plus Ulagsukun #1E), for a total sample
size of 300.
These samples were stratified into 5 time
periods throughout the day (I discuss the temporal
patterns in chapter VI) .
Courtships and forays were
measured in 1992 for 10 fish in each position at each of
the initial two sites and over six monthly samples, for a
total sample size of 240.
I analyzed these data with two-
way ANCOVA's with position and site as fixed factors and
fish size as a covariate.
All data except occupant
feeding rate were log transformed for analysis.
22
Data analysis and presentation
I used the Statgraphics 5.0 software package to
analyze these data.
In ANOVA's and ANCOVA's I verified
assumptions of normality and equality of variances using
graphical plots (normal probability and residuals vs.
predicted values)
.
Appropiate transformations or non-
parametric tests were used when necessary and are
specified in the results.
1 s.e.
ANOVA's.
All errors and error bars are ±
Tukey post-hoc tests were used after significant
Data for individual sites are only presented if
sites were significantly different.
Results
Survival, body size,
and growth
Persistence (survival) was slightly lower on the edge
but did not differ significantly from the cluster center
(Fig. 11.2, Logrank statistic = 2.69, df = i, P >
despite a 20
.1)
difference on the last sampling date.
These
data suggest a lifespan of about three years, which agrees
with the estimates of Williams (1978)
The number of otolith increments (relative age) was
correlated with size (Y = 75.4 + 4.4X, R2 = 0.09, n = 55,
P = .02) , but did not differ by position or sex (F= o.i, p
>
.7 in both cases), and was not correlated with mating
success (cumulative monthly clutch size) for either males
23
(r = 0.01, t = 0.03, df = 29, p = .98) or females (r =
0.20, t = 0.93, df = 21, P = .36).
Fish body size was significantly larger, though only
by 2-3mm, in central fish at all three sites examined,
although there were also absolute differences among sites
(Fig. 11.3, Table 11.1).
Growth was significantly greater
in the center than on the edge of a cluster (Fig. 11.4) in
both the wet season and overall, but not in the dry
season, when growth was low for all fish.
Total growth
for both positions combined was negatively correlated with
fish size Cr = -.39, t = -2.48, df = 33, p = .018), but
for neither position individually.
In any case, at all
body sizes center individuals grew more than edge
individuals.
Hatching success
I found that the average number of clutches a male
received during a monthly brood cycle was higher in the
center of a cluster of territories (Fig. 11.5), but only
significantly so in 1993 (1992: F = 0.53, df = 1,38, p =
.48, MSE = 5.76; 1993: F = 8.88, df = 1,34, p = .005, MSE
= 1.18) .
Total mating success (cumulative clutch size
over the month) was over 50
higher in the center in both
years (Fig. 11.5), but again, only significant in 1993
(1992: Kruskal-Wallis t = 1.17, p = .28; 1993: F = 6.68,
df = 1,34, p = .014, MSE = 583.3) .
There was high
24
Figure 11.2. Persistence of marked S. pjnifrons in each
cluster position on Tiantupo #1W from July 1992 to April
Initially there were 40 marked fish in each
1993.
position.
100
go
80-
0
z
7060
50401Y
Lii
V
CENTER
vEDGE
302010
0
N
(\J
XD
0)
C'4
('4
1
DATE
('4
//o
25
Figure 11.3. Body size (mm SL) of S. plarifrons for each
cluster position and site. Sites are: SS- Smithsoniantupo
Fish at
#1, TT- Tiantupo #1E, US- Ulagsukun #1E.
than
either
of the
Ulagsukun were significantly smaller
Error
bars
are
se's in
other two sites (see Table 11.1) .
this and all subsequent figures.
65
C)
E
E60
Lii
(/)55
ii
50
SS
IT
US
CENTER
SS
IT US
EDGE
26
Figure 11.4. Growth (mm SL) of marked S. panifrons in
each cluster position on Tiantupo #1W from July to
December 1992, December 1992 to April 1993, and overall.
Sample sizes were: December 1992, 38 center and 35 edge;
Statistical
April 1993 and total, 18 center and 17 edge.
1,70, MSE = 4.8; position: F
results: (1) July-Dec.; df
= 6.0, p = .02; body size: F = 6.9, p = .01, (2) Dec.April; df = 1,32, MSE = 5.0; position: F = 0.5, p = .47;
body size: F = 2.2, p = .15, (3) July-April; df = 1,32,
MSE = 0.2; position: F = 10.8, p = .002; body size: F =
7.0, p = .013.
27
Figure 11.4.
6
JULY-DEC 1992
DEC-APRIL 1993
OVERALL
(dr)
E
4
3
IL
F-
0
1Y
2
1
0
CENTER
EDGE
Table 11.1
ANOVA results for S. planifrons body size
(SL)
Source of
variation
df
MS
P
F
Position (P)
1
300.0
18.9
< .001
Site (5)
2
261.1
16.4
< .001
PxS
2
9.3
0.6
.560
294
15.9
Residual
Table 11.2
ANCOVA results for S. planifrons territory
size.
Source of
variation
df
MS
F
P
covariate
body size
1
26.8
0.7
.424
Position (P)
1
705.2
17.6
< .001
Site (5)
1
166.9
4.2
.045
P x 5
1
12.5
0.3
.584
75
2997.8
Main Effect
Residual
variance in mating success in 1992.
Average individual
clutch size was larger for clutches laid in the center of
a cluster (Fig. 11.5), but only significantly so in 1992
(1992: F = 4.15, df = 1,95, p = .044, MSE = 46.1, data
were log transformed; 1993: F = 1.95, df = 1,103, P = .17,
MSE = 42.3) .
Mating success and size were not
significantly correlated for males (r = 0.31, t = 1.82, df
= 31, p = .08) or females (r = 0.16, t = 0.79, df = 24, P
= .44)
Clutch survival was high, and did not differ by
position.
In 1992, only 4 of 97 nests suffered noticeable
loss of eggs.
The losses were split with 1 of 54 clutches
from central males affected and 3 of 43 from edge nests (G
= 1.63, df = 1, p >
.2)
Again in 1993 clutch survival
did not vary by position, 1 of 58 central clutches and 0
of 29 edge clutches lost eggs (G = 0.81, p >
.2)
The distances females traveled to mate with a male
did not differ significantly either by the position of the
male (F = 1.3, df = 1,95, p = .25, MSE = 0.22, data were
log transformed)
0.24, p = .63).
or by the position of the female (F =
The distance averaged 2.1 ± 0.19 m.
Thirty-four of 48 females (70.8%) and 79 of 121 males
(65.3%) had territories in the center of the
Smithsoniantupo #1 cluster.
No significant spatial
segregation of the sexes existed (G = 0.49, df = 1, p >
.2).
30
Figure 11.5. Mating success of S. planifrons males in
each cluster position in August 1992 and June 1993 from
Smithsoniantupo #1. Average clutch size is for all
clutches laid over a monthly brood cycle in each position.
Cumulative clutch size is the sum of all clutch areas for
the complete monthly spawning cycle. Number of clutches
is the number received during the complete spawning cycle.
60
1992
Average clutch aize
Cumulative clutch size
EEl Number of clutches
50
3
rJI
2
30
20
10
LI
0
LU
T
10
1993
C-)
4
60
-J
0
cr
0
0
LU
F-
50
3
40
30
2
20
0
0
CENTER
EDGE
31
Territory size
Territory size varied significantly by position with
center territories smaller than those on cluster edges
(Fig. 11.6, Table 11.2)
There were also differences
.
between sites, with Smithsoniantupo having smaller
territories than Tiantupo.
These patterns in territory
size and behavior were similar throughout 1992 and 1993
(see Chapter VI).
Behavior
Benthic feeding rates did not vary with position,
site or body size (Table 11.3).
(± 2.4) per 10 mm
2.2) per 10 mm
Bite rates averaged 46.1
in the center of a cluster and 45.1 (±
on the edge.
Time spent feeding on
plankton also did not vary by position or size (Table
11.4), though there was high variation among sites.
Chase rates with conspecifics were greater in the
center of territory clusters, though only significantly so
when the covariate of body size was removed from the
analysis (Fig. 11.7, Table 11.5).
Chase rates toward all
heterospecifics summed were much less in the center (Fig.
11.7, Table 11.5).
The breakdown by species shows that
striped parrotfish (Scarus iserti), bluehead wrasse
(Thalassoma bifasciatum), and other parrotfish were the
most common heterospecific intruders.
The overall rates
of interactions in the center cere about half those on the
32
S. planifrons territory size for each
Figure 11.6.
cluster position and site. Abbreviations as in Fig. 11.3.
4000
E
0
3000
LLi
< 2000
o 1000
ft
w
H-
0
SS
IT
CENTER
SS
TI
EDGE
33
There were a number of
edge (Fig. 11.7, Table 11.5)
significant site differences in these measures of
aggression, but in all cases, the relative center-edge
patterns within a site were the same as the overall
patterns.
There were also no differences with fish size.
The rate of feeding by intruders within damselfish
territories, mostly by striped parrotfish, was
significantly higher on the edge (Fig. 11.8, Table 11.6),
but did not vary with fish size.
Forays from territories
did not vary with position, site or fish size (F = 0.7,
.07, respectively) and averaged
0.0, 3.4; p = .42,
.88,
0.23 forays/b
(± 0.05).
mm
Courtship rates (Kruskal-
Wallis t = o.ii, p = .75) also did not vary and averaged
0.10 courtships/b0 mm
(± 0.06)
Discussion
Center-edge fitness differences
Center positions in clusters of Stegastes planifrons
territories had higher fitness measures for both
components of lifetime reproductive success (i.e., number
of mating cycles in a lifetime and hatching success per
mating cycle)
.
Survival of S. planifrons was not
significantly affected by territory position, at least
over the time scale I was able to follow.
higher for fish in central territories,
Growth was
Since age did not
34
Figure 11.7. 5. planifrons agonistic interactions with
conspecific and heterospecific intruders for each cluster
The striped parrotfish is Scarus
position and site.
iserti, the bluehead wrasse is Thalassoma bifasciatum.
The error bars are for the rates of interaction with
conspecifics (down) and for the rates with all
heterospecifics combined (up) . For interactions with all
heterospecifics Smithsoniantupo was siginficantly greater
Ulagsukun had significantly more
than the other sites.
interactions with conspecifics than Tiantupo, but neither
Tiantupo had
site differed from Smithsoniantupo.
significantly fewer total agonistic interactions than
either of the other sites. Abbreviations as in Fig. 11.3.
Other Bpecies
[-.]
I
6
o
C
E
I
I____
F1
Other wraes
Bluehead wrasse
Other parrotfish
Striped parrot.
(I)
0
Li
0
(1)0
Cl)
LU
LL.
o
o
1_
ILl
0
U)
0
(I)
F
w
C
U)
ILl
0
0
IL
0
2
ILl
0
U,
SS
TI
US
CENTER
SS
IT
US
EDGE
z
0
0
35
Rate of food stealing by intruders from
Figure 11.8.
within S. planifrons territories for each cluster position
Smithsoniantupo had significantly higher levels
and site.
of food stealing than the other two sites. Abbreviations
as in Fig. 11.3.
2.0
1.8
o
1.6
1.4
(I)
ci)
-4-I
1.o
0.8
FLL
w
:i:
i-
o
0
0
06
0.4
0.2
ss
ii us
CENTER
SS
IT US
EDGE
36
Table 11.3
ANCOVA results for S. planifrons benthic
feeding.
Source of
variation
MS
F
P
1
1448.2
1.9
.17
Position (P)
1
78.2
0.1
.75
Site (S)
2
1780.6
2.3
.10
P x S
2
246.2
0.3
.73
293
782.3
df
covariate
body size
Main Effect
Residual
37
Table 11.4
ANCOVA results and raw data (x and se) for
planifrons.
planktonic feeding of
.
Source of
variation
df
MS
1
4.8
1.3
.263
Position (P)
1
0.6
0.2
.690
Site (5)
2
62.9
16.5
PxS
2
6.6
1.7
293
3.8
p
F
covariate
size
Main Effect
Residual
.001
<
.178
planktonic feeding
center
edge
reef
Smithsoniantupo
50.0 (4.5)
42.4
(5.4)
Tiantupo
51.9 (4.2)
63.6
(4.6)
Ulagsukun
135.3 (10.2)
117.2
Note: Data were log transformed for
analysis.
(10.6)
Table 11.5
ANCOVA results for S. planifrons agonistic interactions with intruders.
with heterospecifics
with conspecifics
Source of
variation
df
MS
MS
F
1
062
1.5
.228
1
0.06
0.2
.688
Position (P)
1
1.54
3.6
.058
1
79.98
239.3
< .001
Site
2
3.67
8.6
.001
2
4.78
14.3
< .001
2
0.67
1.6
.209
2
1.01
3.0
.051
293
0.43
293
0.33
df
P
F
P
Main Effect
(5)
PxS
Residual
<
w
Table 11.5, Continued.
Total interactions
Source of
variation
covariate
df
MS
F
body size
Main Effect
1
0.1
0.4
.523
Position (P)
1
26.0
79.9
< .001
Site (5)
2
5.7
17.5
< .001
PxS
2
0.1
0.3
.755
293
0.3
Residual
P
Note: All data were log transformed for analysis.
LU
40
Table 11.6
ANCOVA results for feeding by intruders within
planifrons territories. One-way ANCOVA results are also
given because of the significant interaction.
.
Source of
variation
df
MS
1
0.3
1.3
.250
Position
1
10.0
44.6
< .001
Site
2
0.9
4.2
.016
P x S
2
0.8
3.6
.028
293
0.2
F
P
covariate
body size
Main Effect
Residual
Source of
variation
df
MS
1
0.2
0.8
.388
Position
1
10.3
44.2
< .001
Residual
297
0.2
F
P
covariate
body size
Main Effect
Note: Data were log transformed for
analysis.
41
differ with territory position, these growth rate
differences explain the slightly larger size of central
fish.
While I did not measure the number of mating cycles
in a lifetime, these results suggest that this component
of lifetime reproductive success either is greater for
fish in central positions or at least does not differ with
position.
This is because survival was similar, but
central fish might become reproductively mature sooner
owing to their higher growth rate (Wootton 1990).
Few
other studies have compared any of these fitness measures
between positions in a cluster or group.
In contrast to
my results, Coulson (1968) found that kittiwake mortality
was 60% higher on the edges of territory clusters for
males, but did not differ by position for females.
Rayor
and Uetz (1990) found that peripheral spiders suffered
higher rates of predation.
Itzkowitz (1978) also reported
larger individuals in the center of threespot damselfish
clusters, but did not measure age, growth, or survival.
Okamura (1986) found that central mussels in clusters grew
slower than edge or solitary individuals.
Hatching success per mating cycle, the second
component of lifetime reproductive success, was also
greater in cluster centers.
Individual and cumulative
clutch size were larger in the center of a cluster, as in
other systems (see Introduction)
.
However, clutch
survival did not differ with position, in contrast to many
42
other species (see Introduction)
.
The lack of any
positional difference in clutch survival is consistent
with the observation that there was no segregation of the
sexes by position.
The overall rate of clutch loss was
much lower than reported for any other damselfish (Foster
1989, Petersen and Marchetti 1989, Petersen 1990, Knapp
and Warner 1991)
Since both components of lifetime reproductive
success were greater for fish in cluster centers, lifetime
reproductive success must therefore also be greater in the
center of clusters.
The permanence of territory position
implies that site selection by damselfish may have an
inordinate impact on lifetime fitness.
Linking fitness and behavior
Center-edge differences in fitness within clusters of
territories appear to be caused by differences in
energetic costs associated with living in each position.
These energetic costs, in turn, can be related to two
behavioral measures.
First, based on feeding rates,
energy intake rates did not differ with position.
Second,
fish in the center of clusters chased conspecifics more
frequently than did edge fish, but had to chase
heterospecifics much less commonly.
Overall, rates of
aggressive interactions were lower in the center.
If we
43
assume then that energy expenditure is related to chase
rates (see Hixon 1980) , then fish in the center of a
cluster should have more energy available to devote to
growth and/or reproduction, since energy intake is equal
but energy loss is less for fish in cluster centers.
My
results suggest that central threespot damselfish invest
this extra energy in both increased growth and
reproduction.
Three other studies have compared agonistic
interactions by position in a group.
Robertson et al.
(1979) found that surgeonfish, Acanthurus lineatus, with
territories in the center of a cluster have chase rates
and food loss to interspecific competitors much lower than
fish with edge territories.
Similarly, Inglis and
Isaacson (1978) found that geese on the edge of a flock
spent more time in aggressive interactions.
Shima
(personal communication) found similar patterns to my
study in another damselfish, S. nigricans, in Tahiti.
The qualitative patterns in aggressive interactions
with conspecifics and heterospecifcs each support the
predictions of theoretical models by Stamps et al.
(1987)
Threespot clusters act like 'hard edge' habitats, in
Stamps' terminology, in which habitat boundaries limit
movement of conspecifics out of the cluster.
The basic
idea is that central fish have more conspecific neighbors
and thus interact more frequently with conspecifics than
44
In contrast, many heterospecifics approach the
edge fish.
patch reefs from the edge, where they avoid aggressive
interactions by feeding in surrounding seagrass or sand
beds.
The central damselfish are protected from attack
from these heterospecifics since intruders would have to
first penetrate a gauntlet of more peripheral conspecific
territories.
Thus, heterospecific intruders in this
system, especially parrotfish, resemble the 'soft edge
with reserve' models of Stamps et al.
(1987)
.
In this
situation, the area surrounding the habitat patch is a
source of intruders and habitat edges do not inhibit
movement.
This case is similar to the selfish-herd theory
(Parrish 1989) in that central members of a group are
protected from intruders by peripheral individuals.
Interspecific territoriality complicates the
application of Stamps' models since a different model can
apply to each species.
In this study, the overall balance
of the two types of aggressive interactions, conspecific
vs heterospecific, favors fish with territories in central
positions because interactions with heterospecifics are
more common.
However, it is conceivable that edge
positions may be favored in other situations, particularly
if most interactions occur among conspecifics or other
cluster members.
The fact that other behaviors, such as forays away
from territories and courtship, did not vary by position
45
rules out these behaviors as possible benefits of
occupying central positions in a cluster.
Bartels (1984)
found more foraying by solitary fish than by those in
groups in a related damselfish.
Itzkowitz (1978) found
that S. planifrons on the edge of clusters forayed more
frequently.
He attributed this pattern to coral habitat
quality differences between positions.
I cannot explain
why my results differ from Itzkowitz (1978).
In any case,
central members of a cluster do not appear to compensate
for decreased defense costs by increasing courtship or
feeding activity.
Thus time does not appear to be a
constraint in S. planifrons (see Hixon 1982).
The center-edge differences in
.
planifrons
territory size also appear to be a consequence of the
positional differences in defense costs and food loss.
Central fish seem to have smaller territories than edge
fish because their defensive energetic needs are less (as
indicated by chase rates), and because they do not lose as
much of the food in their territories to intruders.
Smaller central territories is a common, though not widely
recognized, pattern in groups of territorial individuals
(see Stamps et al. 1987)
The proximate cause of the center-edge differences in
behavior and territory size could be due either to a
selfish-herd like grouping effect (see Stamps et al, 1987)
or to positional microhabitat variation in some resource
46
(e.g., quality of food, nest or shelter sites) .
Chapter
III experimentally tests these two possibilities in
.
planifrons and concludes that grouping effects are the
main cause.
In summary, the benefits of living in the center of a
cluster in this system seem to be lower defense costs,
less food loss, and more matings, with more energy being
available for growth and reproduction.
No feeding or
predation risk benefits were evident.
Implications
This study has at least four implications.
First,
when animals defend individual territories in contiguous
clusters, the potential effects of relative territory
position must be considered in any study.
Aggregations
that may result from habitat patchiness or fragmentation
should also be recognized as systems in which group
position may be relevant.
Second, there has been considerable interest in the
relative influence of food availability and intra- and
interspecific aggressive interactions on territory size
(Ebersole 1980, Hixon 1980, 1987, Schoener 1983, Norman
and Jones 1984, Mares and Lacher 1987, Temeles 1987,
Tricas 1989).
Experimental studies have reached opposite
conclusions on the importance of particular factors in
47
different systems.
However, virtually none of the studies
to date, either theoretical or empirical, have considered
the effects of territory position.
My results suggest
that the relative importance of intra- and interspecific
aggression in determining territory size will depend on
which territory position in a cluster is studied.
In
.
planifrons, intraspecific interactions should have a
greater effect on territory size in central positions,
while interspecific interactions should be more important
on the edge.
The abundance, source and interaction rates
of heterospecifics should be an important factor in
determining the role of grouping on territory size.
Third, because of the center-edge differences in
fitness measures, we might expect there to be competition
for the more desirable central positions in a cluster.
I
have tested, and found evidence to support, this
hypothesis for
et al.
.
planifrons (see chapter IV).
Robertson
(1979) and Rippin and Boag (1974) have also found
such competition in coral reef surgeonfish colonies and
grouse leks, respectively.
Fourth, the variation in territory size and mating
success with position in a cluster of threespot damselfish
suggests that habitat (or cluster) size and shape may
alter the densities and reproductive outputs of
populations of territorial species,
Smaller or more
oblong habitats would have relatively more edge
48
territories, and consequently, lower density and per
capita reproductive output.
Habitat fragmentation (which
may result in clustering due to habitat patchiness) may
also affect population density and reproductive output in
the same way because fragmentation decreases the size and
alters the shape of habitats.
Thus, in addition to
reducing suitable habitat, inhibiting migration and gene
flow, increasing edge effects and lowering population
numbers (Shafer 1990, Rolstad 1991), habitat fragmentation
can affect the behavior and fitness of organisms
remaining within the fragment in another, previously
unrecognized, way.
Note that this effect is different
than the edge effects associated with fragmentation
(Rolstad 1991, Rudnicky and Hunter 1993), in that animals
in the centers of habitat fragments could also be directly
affected.
This implication assumes that the center-edge
differences in territory size and mating success are due
to a grouping effect and not microhabitat variation per se
(see above).
Finally, these effects would also be relevant for
managers considering the choice of single large or several
small nature reserves (the SLOSS debate, see Shafer 1990),
in species that form clusters of contiguous territories.
A single large reserve and several smaller reserves of
equal total area will have different population densities
(and hence absolute numbers) and reproductive outputs.
49
Again, this pattern would be due to differences in the
The models of Stamps et
relative amount of edge habitat.
al.
(1987) suggest that this result may be the case even
if the territories in the cluster are not immediately
contiguous.
These potential effects would need to be
considered when managing threatened or endangered species
that form such territory clusters.
Acknowledgements
Working for a pittance, L. Pace, K. Crofoot and B.
Profit were excellent dive buddies and assistants without
whom this project would not have been completed.
C.
Donohoe taught me how to prepare and interpret the
otoliths.
J. Harding, D. Booth, B. Tissot, D.R.
Robertson, K. & L. Clifton provided various support and
advice for which I am grateful.
The comments of A.
Blaustein, M. Carr, M. Hixon, M. Itzkowitz, T. Kaltenberg,
B. McCune, J. Miller, D.R. Robertson, J. Wolff and
anonymous reviewers greatly improved the manuscript.
The
Kuna Indians and the Republic of Panama permitted the
research in their country and the Smithsonian Tropical
Research Institute, especially D. R. Robertson, R. Tapia
and I. Ivancic, provided logistical support.
Finanacial
support was received from an NSF predoctoral fellowship, a
Smithsonian summer graduate student fellowship, Sigma Xi,
50
the ASIH Raney Fund, the Lerner Gray Fund for Marine
Research and the OSU Zoology Department.
This work was
completed in partial fulfillment of a Ph.D. degree in the
Department of Zoology, Oregon State University.
Special
thanks to my major advisor, Mark Hixon, for inumerable
assistance in all phases of this work.
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56
CHAPTER III: CENTER-EDGE DIFFERENCES IN BEHAVIOR AND
TERRITORY SIZE IN CLUSTERS OF TERRITORIAL DAMSELFISH:
GROUPING OR MICROHABITAT VARIATION?
DWAYNE W. MEADOWS
Department of Zoology
Oregon State University
Corvallis, OR 97331-2914, U.S.A.
Abstract
Individual territories of threespot damselfish occur
in clusters of territories on coral reefs.
Previous
research had shown that, relative to edge fish, fish with
territories in the center of a cluster had: smaller
territory sizes, lower aggressive chase rates toward
heterospecific intruders, more chases with conspecifics,
lower overall chase rates, less food loss to intruders (as
measured by feeding rates), faster growth, and center
males obtained more and larger egg clutches.
Here, I
tested whether the positional differences in behavior and
territory size were due to a "selfish-herd" grouping
effect, in which center individuals do better because of
protection from intruders by more peripheral neighbors, or
simply to microhabitat quality variation between these
positions.
The approach was to alter an individual's
position in a cluster (from center to edge) without
changing its actual territory location or microhabitat.
did this manipulation by removing all fish in a cluster
57
If
peripheral to a central treatment individual.
microhabitat quality alone accounts for positional
differences in behavior, this manipulation should have no
effects.
However, if grouping causes positional
differences in behavior and territory size,
I predicted
that after the manipulation treatment fish would (relative
to controls) :
increase territory size, decrease
conspecific chases, increase heterospecific chases, and
lose more food to intruders.
verified.
All predictions were
Thus, territory position relative to neighbors
has a large impact on behavior in this species, and may
secondarily affect other fitness measures that vary by
position, such as growth and mating success.
From the
perspective of conservation biology, these results suggest
that habitat fragmentation, which may result in clustering
of individuals, may lead to alteration in territory size,
and hence population density, as well as per capita
reproductive output, by Increasing the relative amount of
edge habitat.
Introduction
The aggregation of individuals into groups is a
common phenomenon in animals.
Invertebrates such as
bryozoans (Buss 1981), arthropods (Rayor and Uetz 1990),
and molluscs (Okamura 1986) are found in dense clusters.
Tadpole and fish schools (Beiswinger 1975, Krause 1993),
leks of male birds (Rippin and Boag 1974), frog choruses
(Jennions and Backwell 1992), and bird colonies and flocks
(Coulson 1968, Burger and Gochfeld 1990, Black et al.
1992) are other well-known examples.
Here,
I use the term
"clustering" as a term for animal aggregations determined
by habitat patchiness, external or unknown factors.
When
it is known that the cause of the aggregation is
behavioral choice (e.g., schools or flocks), I use
"grouping."
In many cases, behavior or certain measures of
fitness vary with position in a cluster.
For instance,
feeding rates varied with position in a spider cluster, a
geese flock and a fish school (Rayor and Uetz 1990, Black
et al. 1992, Krause 1993, respectively), aggressive
interactions were lower in the center of geese flocks and
surgeonfish clusters (Inglis and Isaacsori 1978, Robertson
et al. 1979), mating success was higher in the center of
grouse leks and spider clusters (Rippin and Boag 1974,
Rayor and Uetz 1990), and predation was lower in the
center for many groups of adults, young, and eggs
(Hoogland and Sherman 1976, Milinski 1977, Gross and
MacMillan 1981, Okamura 1986, Foster 1989, Rayor and Uetz
1993) -
At least two potential causes have been suggested to
explain these positional differences in behavior and
fitness.
"Selfish-herd" ideas, originating with Hamilton
(1971), are most commonly proposed.
According to this
theory, the positional differences are due to the
protection from predators or competitors afforded central
cluster members by more peripheral neighbors.
Related
effects have also been suggested for males in leks or
other mating aggregations where the central positions
might offer females more choices of mates (Bradbury et al.
1986), or where central locations might result in higher
competition (Hoogland and Sherman 1976) or food intake
(Burger and Gochfeld 1991).
I consider all of the above
examples as types of "grouping effects".
The "grouping
effects" hypothesis thus predicts that all center-edge
variation in behavioral or fitness measures is due to the
position of an individual relative to other members of the
group or cluster.
Alternatively, positional differences
within clusters could be due simply to variation in
habitat quality on the same spatial scale (see Robertson
et al. 1979, Stamps et al. 1987) .
That is, the
microhabitat may differ between center and edge positions
in a cluster, directly explaining positional differences
in behavior, territory size and fitness.
I call this the
"microhabitat effects" hypothesis.
Experimental tests to distinguish these hypotheses
are rare, and grouping effects are usually assumed to be
the cause without testing for possible microhabitat
effects (e.g., Gross and MacMillan 1981, Petit and
Bildstein 1987, Foster 1989, Rayor and Uetz 1990).
In
cases where there is obviously little microhabitat
variation by position, such as when groups are mobile so
that all positions experience the same microhabitat, this
assumption may not be unreasonable.
However, in
situations where the aggregations are site attached, such
as in territorial species, grouping or microhabitat
effects can only be distinguished experimentally.
Here I provide such a test in a system of clustered
individual territories of a coral reef damselfish.
I show
that a grouping effect, rather than a microhabitat effect,
explains the positional differences in behavior and
territory size of individuals of this species.
I then
suggest that this grouping effect secondarily has an
impact on other fitness measures (growth and mating
success) that also vary by position.
First I describe the
system and outline the predicted changes that should occur
if grouping causes the center-edge differences in this
species.
Stegastes planifrons, the threespot damselfish,
maintains individual year-round territories less than 1 m2
in area, within which they feed on various micro- and
macroalgal species cultivated in a "lawn" (Brawley and
Adey, 1977, de Rutyer van Steveninck 1984, Hinds and
Ballantine 1987) .
Male territories also contain nests
61
which the males guard, protecting demersally spawned eggs
which remain in the territory for 4-5 days until hatching
into planktonic larvae (Robertson et al. 1990)
Territories are defended against conspecifics of both
sexes and a variety of other herbivores (e.g.,
parrotfishes, surgeonfishes, sea urchins), and egg
predators or other carnivores (e.g., wrasses) (Thresher
1976, Williams 1978 and 1981, Robertson 1984, Ebersole
1985)
At my study site, individual territories were
clustered on coral patch reefs varying in size from 1-
bOOm2.
Meadows (chapter II) found that individuals with
territories in the center of such clusters had slightly
higher intraspecific chase rates, much lower interspecific
chase rates, and overall rates of aggression less than
one-half those of individuals on the edge.
Central
individuals also lost much less of the food in their
territories to intruders (mostly schooling parrotfish)
than edge individuals (as measured by feeding rates), had
similar food intake rates, smaller territory sizes, and
grew faster.
Consequently, central males achieved higher
mating success (number and size of clutches) than edge
males.
There were no positional differences in survival
or age.
The models of Stamps et al.
(1987) provided two
predictions that would support a grouping effect.
The
62
predictions derive from the idea that a grouping effect
should vary in importance with the relative amount of edge
in a cluster, while a microhabitat effect should not.
The
first prediction is that average intraspecific chase rates
among reefs should be negatively correlated with reef
perimeter-to-area ratio.
Conversely, the second
prediction is that average interspecific chase rates among
reefs should be positively correlated with reef perimeterto-area ratio.
I tested these predictions with among reef
observations of chase rates.
I also carried out an experimetal study to determine
the role of grouping versus microhabitat effects.
I
compared behavior and territory size of treatment fish
located in the center of a cluster both before and after
experimental removal of all fish peripheral to these
treatment fish.
Thereby,
I changed the position of the
treatment fish relative to the conspecific cluster of
individuals (in the center before removal and on the edge
after), but not relative to microhabitat since the fish
maintained its original territory.
Thus, I could separate
the effects of position in a group vs. microhabitat (and
also any effects of body size) .
If grouping was the cause
of the center-edge patterns, then I would predict that the
treatment fish in this experiment would (relative to
controls) :
1) decrease intraspecific chase rates, 2)
increase interspecific chase rates,
3)
lose more food to
intruders, and 4)
increase territory size.
If
microhabitat differences alone caused center-edge
patterns, then this manipulation should have no effects.
Methods
Study site
The research was carried out at the San Bias Marine
Laboratory of the Smithsonian Tropical Research Institute
on the Caribbean coast of Panama, from June through
December 1992 and April through June 1993.
Many coral
patch reefs within 2km of the lab were utilized (see
Robertson 1987 for map and reef name references) .
The
coral patch reefs and damselfish clusters were found in
water from l-25m in depth, though I used reefs only 1-10 m
in depth.
The patch reefs and their characteristics are
more fully described in chapter II.
Microhabitat quality
I quantified variation in microhabitat quality in
both center and edge positions, and both inside and
outside of threespot damselfish territories.
I measured
14 center and 14 edge territories, and ten center and ten
edge interterritorial areas, on each of two patch reefs,
Smithsoniantupo #1 and Tiaritupo
lE.
Total sample size
64
was thus 96 microhabitat patches.
I measured the planar
area of each patch parallel to the substrate, counted the
number of sea urchins (mostly Echinometra and Lytechinus
spp.) and brittle stars in each patch, and measured the
percent cover of five substrate types (Agaricia coral,
Millepora coral, rubble, sand, other hard corals
combined), and the percent cover of all living algal and
invertebrate species.
Microalgal turfs making up the lawn
were considered one category.
Thus some coral species
were measured for both their contribution to the substrate
(which could be either living or dead material) and as
living individuals.
To measure planar percent cover, I
used a clear acetate sheet with marks outlining shapes of
known area, which could be readily placed over an object
to determine its area (± 25cm2 accuracy) .
The percent
cover of living sessile taxa were measured in all three
dimensions (without respect to the substrate plane) in
order to account for habitat complexity and to estimate
potential algal food abundance on which S. planifrons
feeds.
The acetate sheets were again used, except for
Agaricia and Millepora which were too rugose or
inaccessible to utilize this method.
Instead, I measured
planar areas of these species and converted to threedimensional cover with a conversion factor obtained from
disarticulating seven to nine samples of the given species
in the lab and accurately measuring their areas by tracing
onto graph paper.
Total cover of all live species could
thus be greater or less than the planar area of the sample
patch, depending on habitat complexity and amount of
inanimate substrate.
Analyses to compare habitat quality between positions
within territory clusters involved one-way ANOVA's of the
four habitat types using the Statgraphics 5 statistical
program.
Habitat quality data were also analyzed using a
Bray-Curtis ordination (Beals 1984) of the 18 most
abundant species of invertebrates and algae using the PCORD statistical package (McCune 1991).
In the
ordinations, I used Euclidean measures for distance,
residual calculation and projection geometry.
Data were
relativized by the norm for samples.
Algal food availability is a function of both
abundance and production.
To measure food abundance and
daily production, I placed two 62 x 62mm ceramic tiles in
each of 20 territories in both central and edge positions
on Tiantupo #1W.
Algal lawns were allowed to develop on
the tiles from July to November of 1992.
Just after dawn
one day in November 1992, I removed one randomly selected
tile from each territory.
These tiles measured standing
crop (abundance) before any damselfish feeding or algal
growth had occurred that day.
The remaining tile in each
territory was placed inside a cage made of 1cm square wire
mesh.
These tiles were then collected just before dusk so
as to obtain algal production during the day by
subtracting the standing crop measured on the other tile
in the same territory.
alcohol.
Each sample was preserved in 90%
In the lab, samples were dried to constant
weight at 60°C to obtain dry weight, then burned in a
furnace at 600°C for 24 hours to remove all organic carbon
(Brinkhuis 1985).
Ash-free dry-weight (AFDW) was the
difference between these two weights and was used to
measure abundance and production.
Among reef behavioral observations
To test whether there was a relationship between
aggressive behavior and reef perimeter/area, as predicted
by Stamps et al.
(1987), I studied 13 different patch
reefs around San Bias during June and July 1992.
For each
reef, I measured the length and width and estimated the
geometric shape of the reef to calculate perimeter and
area.
On each reef I measured a ten-minute activity-
budget for each of 10 center and 10 edge fish between the
hours of 1400 and 1600, the time when these fish are most
active.
From these activity-budgets I obtained mean
intra- and interspecific chase rates for each reef as a
whole, based on the relative amount of center and edge
habitat on each reef.
67
Position manipulation experiment
The experiment was carried out during the 1993 field
season.
Treatment fish were central fish immediately
adjacent to a removal area from which all conspecific fish
peripheral to that treatment individual were removed (Fig.
111.1).
For a control, I monitored undisturbed center
fish on the opposite side of the patch reef from the
removal area.
Undisturbed edge fish were also monitored
This
away from the removal zone as an 'edge-control'.
edge-control was used as a comparison for what the
treatment fish response variables might approach if
grouping was the factor causing the center-edge
differences.
For two days before the removal, I measured
territory size of each individual in the morning (08001100) and quantified behavior from ten minute activitybudgets per individual in the afternoon (1400-1630)
Behaviors measured included chases with con- and
heterospecifics, and feeding bites by both the occupant
and intruders.
Territory size was measured during 20 mm
periods (see chapter II for full details) .
Fish
peripheral to each treatment fish were then removed on the
following day (Fig. 111.1); these were mostly netted by
the method in chapter II or were occassionally speared.
also removed any subsequent immigrants to the removal
areas throughout the course of the experiment.
I removed
an average of 51.4 (± 5.1, se) damselfish from the removal
Diagrammatic representation of the
Figure 111.1.
T- Treatment,
experimental design on a single patch reef.
C- Control and EC- Edge Control territories. Removal zone
is area where fish peripheral to the treatment fish were
removed.
/J
\\
\_7
\ (
)
Remova'
Zone
/
/
-
I
//
\
)
I
-
4
-:
Territory position
Center
Edge
i Buffer (not studied)
Patch reef boundary
zone on the day of removal and 3.4 (± 0.8) individuals
during the remainder of the study.
individuals eluded capture.
Often, one or two
On days 4,
8,
12 and 20 after
the removal, I remeasured territory size in the morning
and behavior in the afternoon of each day.
A total of 20
fish of each of the three experimental groups (treatment,
control, edge-control) were observed over the course of
five runs of the experiment, with each run consisting of
four replicates of each experimental group on a number of
different patch reefs.
In order to assess the reaction of heterospecific
fish to the manipulation, I measured parrotfish feeding
rates around the different treatment areas.
bite rates in a 0.5m2 quadrat during 5 mm
I counted
periods on each
day during the territory-size measuring period.
There
were 2 replicates in the removal area and 1 each in the
control and edge-control areas of each reef, for sample
sizes of 20, 10 and 10 for each treatment on each date.
also censused all parrotfishes, surgeonfishes and
yellowhead wrasses (Halichoeres qarnoti) on each reef on
each sampling date to determine whether population sizes
of potential intruders changed during the experiment.
Thus, these data had only a time factor and no treatment
levels.
Data were analyzed with repeated measures ANOVA using
the Systat 5.02 statistical software package with time and
70
treatment as factors.
Analysis of the raw data themselves
would have presented two difficulties: 1) there would
always be a treatment main effect since the edge-control
should be different from the treatment and control before
the removal and at least the control treatment afterwards,
and 2) if there was a significant treatment effect after
the removal, it would appear in the statistical results as
an interaction.
Therefore, I analyzed the data by
subtracting the mean values of the two pre-removal time
periods from the raw data for each post-removal time
period.
In this way the two control treatments would have
expected mean values of zero (no change after the
removal), and the treatment group would be expected to
differ significantly from zero if the null hypotheses were
false.
The analysis consisted of three treatment levels
replicated 20 times each over each of the four postremoval time periods.
Two edge-control fish disappeared
during the course of the experiment, so the sample size of
this group was 18.
Additional repeated-measures ANOVA's
were carried out on the raw data from the pre-removal
time-periods in order to verify that the control and
treatment groups did not differ initially.
In all cases,
univariate results did not violate the assumption of
compound symmetry and did not differ from the multivariate
results.
Therefore, I present only the univariate
71
results.
Tukey tests were used to determine which
treatment groups differed significantly.
Results
Microhabitat quality
Planar area was larger for territories than for
interterritorial patches, and both types of edge areas
were larger than both types of center areas (Table 111.1).
Central areas both inside and outside of territories had
greater habitat complexity than edge areas (i.e., a higher
percent cover of three-dimensional substrates: living and
dead hard corals of Aqaricia, Millepora, and other taxa
combined, Fig. 111.2).
This pattern was due mostly to
Agaricia, the only of these substrates that differed
significantly when examined separately (Table 111.1).
The
four areas also differed in the composition and abundance
of algal and invertebrate species found within them (Table
111.2).
Urchins and brittle stars were more common in the
center of territory clusters.
Sponges and Agaricia were
common only inside edge territories.
Of the algae,
Halimeda was more abundant on cluster edges while Dictyota
and algal lawns were more common in the central areas.
Other taxa did not differ significantly by position within
the cluster.
72
These differences were also apparent in a Bray-Curtis
ordination of the 96 benthic samples (Fig. 111.3).
The
patches outside of territories were distinct from those
within, and there was also separation of center and edge
territories.
Species that were highly correlated with the
ordination axes were: for axis 1 (which explained 37.3% of
the variation) the coral Agaricia and the algal lawn group
of filamentous algae, and for axis 2 (which explained
17.6%) the alga Dictyota.
Both food abundance and daily food production inside
damselfish territories did not differ with position (t =
1.3, p > 0.1 and t = 1.5, p > 0.1, respectively) and
averaged 2495cm2 (± 175cm2)
algae/territory and 0.009g (±
0.005g) AFDW, respectively.
As a result, bite rates by
fishes provided a reasonable estimate of food intake.
Among reef behavioral observations
Among reefs there were no correlations between
either: 1) average intraspecific chase rates and reef
perimeter/area (n = 13, r2 = 0.07, p = .39), or 2) average
interspecific chase rates and reef perimeter/area (n = 13,
r2 = 0.08, p = .34).
The qualitative differences in
center-edge variation in chase and feeding rates found on
these 13 reefs corroborate those found in chapter II on
73
Habitat complexity (percent cover of threeFigure 111.2.
dimensional substrates, i.e. Agaricia, Millepora and all
other hard corals combined) in each of the four
ANOVA results: df= 3,92, MSE 0.11,
microhabitat types.
Letters
signify groups that did not
F= 9.0, p< 0.001.
differ significantly by Tukey tests. Error bars in this
and all subsequent figures are se's.
1 00
-4-J
90
X
80
-
a
70
E
60
40
_1_J
o
30
'P-'
o
20
10
0
ci)
>
(/,
-f-I
Ii)
>
Q)
-i-'
L
0
4-I
o
cu
41
0
4J
Q)
1)
-4--I
(j)
(])
4-1
ci)
0
C
(1)
0
ci)
74
Bray-Curtis ordination of the abundances of
Figure 111.3.
the 18 most common benthic taxa for all 96 samples from
The taxa included in the
the four microhabitat types.
analysis were: ophiuroids, Echinometra, Lytechinus,
sponges, anemones, Agaricia, Millepora, Porites pprites,
dead
other hard corals, gorgonians, Dictyota, Halimeda
Halimeda with epiphytic algae, Thalassia, crustose red
algae, other green algae, filamentous algal lawns, and
Axis interpretations are based on variable
Jania spp.
loadings.
,
high
fl j r' + i r 1-ri
A
o
center outside
edge outside
center inside
edge inside
A
A
0
A
U)
x
A
A
AL
*IA
A
0
A°
All
A
A
0
S
A
1
low
'
0
:.°°°
:
D i c ty o t a
coral
Axis
0
1
Table 111.1
Patch area (cm2) and percent cover (± Se) of five substrates in each of the four
microhabitat types on patch reefs containing clusters of threespot damselfish
territories.
substrate
type
inside territories
center
(1)
Agaricia
edge
(2)
84.0
(3.0)
Millepora
0.1
(0.1)
0.1
other coral
2.6
(1.2)
2.3
rubble
9.1
sand
4.2
patch area
outside territories
center
(3)
50.0 (4.6)
edge
Tukey
results
(4)
77.5
(9.9)
59.2
(6.4)
2A ._l
(0.1)
3.8
(2.9)
0.0
(0.0)
NS
(0.8)
14.4
(8.2)
0.0
(0.0)
NS
(1.8)
10.7 (2.7)
1.4
(1.4)
0.6
(0.6)
j 21
(1.2)
34.7 (5.1)
2.9
(1.7)
39.8
(7.7)
31 24
2789.3 (79.8)
3617.9 (164.1)
1045.0 (82.9)
1595.0 (145.5)
j 12
Note: "Rubble" is any loose material > 0.5cm in diameter and "sand" is anything < 0.5cm.
Tukey test results from one-way ANOVA's are given; the numbers represent the four data
columns for microhabitat types. Underlined columns do not differ significantly (p >
0.05)
'fl
Table 111.2
Percent cover of algal and live invertebrate taxa in the four microhabitat types on
patch reefs containing clusters of threespot damselfish territories.
taxa
inside territories
outside territories
center
center
(1)
edge
(2)
edge
(3)
Tukey results
(4)
INVERTEBRATES:
sea urchins
23.2 (4.1)
8.0 (3.4)
25.8
(5.2)
9.4
(4.7)
ophiuroids
15.2 (1.3)
7.9 (1.1)
23.4
(4.6)
13.5
(3.3)
sponges
8.1 (3.3)
28.9 (6.8)
1.2
(1.2)
7.6
(5.6)
2413
2413
3412
anemones
4.9 (1.2)
4.2 (1.0)
7.4
(4.2)
4.2
(1.8)
NS
gorgonians
2.4 (1.1)
7.1 (2.8)
1.2
(1.2)
6.7
(5.8)
NS
26.9 (4.7)
54.1 (7.6)
77.9
(16.9)
(16.6)
1234
Milleoora
8.5 (1.4)
8.1 (2.4)
19.9
(8.2)
4.4
(1.9)
NS
Porites
0.3
(0.2)
1.5 (0.4)
4.3
(1.0)
0.6
(0.4)
NS
other coral
0.6 (0.4)
1.0 (0.6)
6.2
(1.8)
0
(0.0)
NS
Aga r i C i a
98.3
Table 111.2, Continued.
ALGAE:
Halimeda spp.
13.1
(3.7)
32.7
(6.4)
4.1
(3.2)
28.8
(6.9)
3
Dictyota spp.
16.8
(3.2)
7.3
(2.2)
33.0
(4.7)
8.9
(2.5)
2 4 1
algal lawn
54.8 (3.2)
31.2
(3.0)
0
(0.0)
0
(0.0)
j.... 2 1
1 4.2
crustose algae
4.6
(0.8)
4.8
(1.7)
3.6
(1.5)
4.2
(1.6)
NS
Jania spp.
8.8
(1.6)
1.9
(1.0)
0.5
(0.5)
2.5
(1.6)
NS
0
(0.0)
1.1
(0.9)
0
(0.0)
6.8
(5.4)
NS
108.3
(16.2)
12 3 4
(9.0)
NS
Thalassia
TOTALS:
live coral
36.3
(4.7)
64.6
(8.6)
live algae
36.9
(3.1)
36.2
(4.7)
(14.6)
41.1 (7.1)
103.3
42.5
Note:
Data of sea urchins and ophiuroids are #/m2. Tukey test results from one-way
ANOVA's are given.
The numbers represent the four data columns f or microhabitat types.
Underlined columns do not differ significantly (p > 0.05).
three other reefs, though among reef variation existed
quantitatively.
Position manipulation experiment
In all cases the pre-removal behaviors and territory
size did not differ between the control and treatment
groups (see Figs. 111.4-111.6) and there were no time
effects in the repeated-measures ANOVA.
Also, the
abundance of all other fish species on the experimental
reefs did not change throughout the course of the
experiment (MSE = 35.9, F
0.05, df = 3,21, p = .99) and
averaged 22.6 ± 2.1 fish per reef.
Parrotfish bite rates
significantly increased in the removal zone after the
removals (Fig. 111.4, Table 111.3) .
Territory size in the
treatment group increased an average of about 700 cm2
after the removal (Fig. 111.5, Table 111.4) .
Chase rates
with conspecifics decreased about 50% and chase rates with
heterospecifics increased over 200% in the treatment group
after the removal (Fig. 111.6, Table 111.5).
The feeding
rate of intruders within the treatment territories also
increased greatly (Fig. 111.6, Table 111.5).
Feeding
rates by the occupant damselfish did not vary among
experimental groups after the removal, but there was a
significant decrease over time among all three groups
(Fig. 111.6, Table 111.5)
79
Figure 111.4.
Mean parrotfish feeding rates in
planifrons territories belonging to the three experimental
groups.
ANOVA results are in Table 111.3 (see methods for
the data transformation used in the analysis and the
is the date on which
following figures).
11Removal
central territories were converted into edge territories.
.
60
T'
50
-
I
E
v
I'
II
'treat.: p=
006
treatment
control
edge control
T
:time: NS
40
I'
II
II
LI)
30
U)
a)
20
cn
10
0
15
0
7
E
Experiment Day
2>0
11
22
Mean territory size (cm2) of S. planifrons
Figure 111.5.
ANOVA
in the three experimental groups of the experiment.
results are in Table 111.4.
5000
(N
E
0
p< .001
time: NS
treat.:
I
4000
0
3000
>
0
-;--J
'v
2000
treatment
control
edge control
L
ci)
H-
1000
1
°
9
7
11
15
Experiment Day
22
Behaviors of S. planifrons in the three
Figure 111.6.
experimental groups of the experiment: A) chases with
conspecifics, B) chases with heterospecifics, C) feeding
rates by intruders within S. planit'rons territories, D)
benthic feeding rates of occupant damselfish. ANOVA
results are in Table 111.6.
Heterospecifics chased
Conspecifics chased
4
treat.: p
''
.015
time: NS
C
treatment
control
edge control
10
9
8
7
0
I
IT
V/Ji
(I)
I
6
5
4
ci)
3
U)
c'
2
-c
0
0
0
Intruder feeding rates
I,-'
treat.: p= .001
Occupant feeding rates
110,
100
go
80
7°
60
50
15
t Day
22
2
E
Experiment Day
Table 111.3
Repeated measures ANOVA results for
the feeding rate of parrotfish on the
experimental reefs.
Effect
treatment
df
MS
.006
1150
1.5
.22
6
517
0.7
.67
111
764
10613
37
1789
time
3
time x treat.
error
p
5.9
2
error
F
Tukey multiple comparisons:
T
C EC
T- treatment, C- control, ECUnderlines signify
edge control.
groups that do not differ
significantly (p > 0.05)
Note:
83
Table 111.4
Repeated measures ANOVA results for
territory size of S. planifrons on the
experimental reefs.
Effect
treatment
df
MS
p
F
30.0
< .001
2
1495
55
49.9
time
3
3.8
0.6
.61
time x treat.
6
3.1
0.5
.81
165
6.3
error
error
Tukey multiple comparisons:
T
C EC
T- treatment, C- control, ECUnderlines signify groups
edge control.
that do not differ significantly (p >
Note:
0.05).
Table 111.5
Repeated measures ANOVA results of S. planifrons behaviors during the experiment.
a) chases with conspecifics
Effect
b) chases with heterospecifics
MS
F
p
2
19.7
4.5
.015
55
4.4
time
3
1.6
1.2
.32
time x treat.
6
1.7
1.2
.31
165
1.4
treatment
error
error
df
Tukey multiple comparisons:
c)
T E
C
treatment
error
time
F
2
1.70
8.0
55
0.21
3
0.18
MS
p
F
357.8
55
30.4
time
3
9.1
1.3
.28
time x treat.
6
11.0
1.6
.16
165
7.0
Tukey multiple comparisons:
11.8
I
< .001
C EC
d) benthic feeding rates of occupant
p
.001
Effect
treatment
error
2.3
df
2
error
MS
df
treatment
error
intruder bites from territories
Effect
Effect
.08
time
df
MS
2
71
55
1630
3
5799
p
F
0.04
9.69
.96
<
.001
Table 111.5, Continued.
time x treat.
error
6
0.14
165
0.08
Tukey multiple comparisons:
1.8
.11
time x treat.
error
813
165
599
1.36
.23
C EC
T- treatment, C- control, EC- edge control
not differ significantly (p > 0.05)
Note:
6
Underlines signify groups that do
Discussion
Potential effects of microhabitat features
Many aspects of habitat quality varied between the
center and edge of clusters, both inside and outside of
threespot damselfish territories.
The differences between
inside and outside of territories suggest that suitable
habitat may be limiting for S. planifrons (but see
Robertson et al. 1981).
Though habitat quality did vary
by position, it is not clear what effect these differences
have on the behavior and ecology of S. planifrons within
territory clusters.
For instance, food density differed
by position with more algal lawn in central territories,
but absolute food abundance per territory and production
did not differ.
Sea urchins were more abundant in the
center of the clusters.
Williams (1981) found that S.
planifrons competes with the sea urchins Diadema and
Echinometra.
Higher competition from urchins in the
center of a cluster could be an additional cost of
occupying this position.
However, Diadema are no longer
abundant on these reefs (Lessios 1984) , and competition
with Echinometra was weak (Williams 1981) .
Ophiuroids are
also more common in the center of the clusters.
Itzkowitz
and Koch (1991) and Knapp (1993) have shown that brittle
stars consume the eggs of other Caribbean damselfish
species.
However, I found little egg loss from any source
[;y
in S. planifrons (chapter II)
.
Some algal species also
differed by position and could provide different quality
food resources.
Central areas had more three-dimensional
substrate which could provide different food resources,
better protection from competitors or predators, or better
nesting or shelter sites.
It is possible these habitat
differences could explain the center-edge variation in
behavior, territory size and fitness measures of
planifrons.
.
Thus, it was necessary to determine whether
"grouping effects" (i.e., position relative to other group
members) or simple microhabitat quality variation were the
cause of the center-edge differences.
Effects of grouping vs. microhabitat variation
The among-reef observations did not support grouping
effects as the cause of the center-edge patterns.
However, the lack of significant correlation does not
necessarily imply a causative role of microhabitat
variation in determining center-edge differences.
This is
because the among-reef predictions assumed that the matrix
environment around the clusters was uniform and that the
clusters themselves had similar damselfish densities.
Neither of these assumptions were likely to hold in this
system.
The reefs were surrounded by varying amounts of
sand and seagrass beds which supported different densities
and compositions of territory intruders.
In addition the
reefs were in water from 1-lOm in depth and varied greatly
in light reception, which has been shown to affect the
rate and type of algal production and hence
densities (Brawley and Adey 1977) .
.
planifrons
Observations alone,
then, were hardly a definitive test of grouping vs.
microhabitat effects.
In contrast, the experimental removal of all fish
peripheral to a treatment individual allowed me to
separate the effects of grouping and microhabitat
variation.
The results of this experiment supported the
role of grouping effects in causing the center-edge
variation in behavior and territory size.
Intraspecific
rates of aggression decreased, and interspecific chase
rates, bite rates by intruders and territory size all
increased, as predicted by the grouping effects
hypothesis.
The treatment group did not differ
significantly from the edge-control after the removals,
suggesting that grouping effects are the main cause of the
center-edge differences.
There were no significant time
effects in the repeated-measures ANOVA results, suggesting
that the behavioral changes were not short-term
manipulation effects.
The data on heterospecific numbers
and parrotfish bite rates on the experimental reefs
indicate that there was no change in the composition or
abundance of potential competitors with the opening up of
new space, only that there was a shift in feeding to the
removal zone.
The grouping effects found here may have secondary
impacts on growth and mating success, two other factors
that are greater in the center of threespot clusters (see
chapter II) .
I was not able to continue the experiments
long enough to determine whether these fitness measures
were also affected by the manipulation, although I predict
that they would have been.
The higher energetic costs of
living on the edge of a cluster (because of increased
chase rates and larger territories to defend) should lead
to less energy being available for growth and
reproduction.
Grouping would then tend to increase the
within-cluster variance in fitness measures.
Chapter IV
shows that there is intense competition for the more
desirable central positions.
In summary, grouping effects are the main cause of
the center-edge differences in territory size and behavior
in S. planifrons clusters.
This system thus seems to
corroborate the models of Stamps et al.
(1987), which
qualitatively predict the positional differences in
aggressive interactions in this system.
For the threespot
damselfish themselves the reef acts as a 'hard edge'
habitat in Stamps et al.'s terminology, in which the patch
boundary prevents movement away.
The heterospecific
intruders act as 'soft-edge with reserve' habitats, in
which the patch boundary does not limit movement and the
area surrounding the patch acts as a source of intruders.
These models may consequently be applicable to other
groups of territorial individuals.
Stamps et al.
(1987)
reviewed a number of cases where territory size varied by
position in a cluster and suggested grouping effects might
cause these differences.
This study supports this
suggestion.
Implications for habitat geometry and fragmentation
These results suggest a previously unrecognized
effect that grouping can have on population density of
territorial species in fragmented habitats or in habitats
of different sizes or shapes.
The important variable is
relative amount of edge habitat in a patch.
Habitat
fragmentation, which may result in clustering of
individuals by habitat patchiness, increases the ratio of
edge to center habitat in a system (Rolstad 1991)
Besides the inevitable loss of individuals from habitat
destruction and the occurrence of edge effects (Shafer
1990, Roistad 1991, Rudnicky and Hunter 1993) , my results
suggest that population density may also be altered in the
remaining habitat fragments because the group members
living there would alter territory size.
The new edge
individuals would probably increase territory size in this
91
situation, as might central individuals, depending on
their proximity to the new edge and the amount of
protection from intruders afforded by peripheral
Changes in density would depend on the
neighbors.
availability of suitable territory habitat within the
cluster.
This scenario is somewhat different than a
strict edge effect as considered in other studies (see
Shafer 1990) ,
since all the members of the group are
potentially affected, not just the individuals in an edge
zone.
This effect on population density can best be
visualized graphically (Fig. 111.7) .
This model shows the
effect changes in patch or cluster edge-to-area ratio may
have on maximum population density or reproductive output.
The scale of the effect will depend on the ratio of the
relevant response variable between center and edge
territories.
The model is derived simply as a geometric
result of considering the average individual territory
size or reproductive output for a group as the relative
proportion of center and edge territories varies with
habitat size or shape.
of cases.
I have plotted lines for a number
For territory size in threespot damselfish the
relevant ratio is 1.2:1 (edge:center, see chapter II).
Using these data as an example, and assuming a square
habitat of 10 x 10 territories (with an edge-to-area ratio
of 0.4), removing all but a 1/4 square part of it (i.e.,
92
Graphical model of the effect of habitat or
Figure 111.7.
cluster edge-to-area ratio on population density or
Values for population density and
reproductive output.
reproductive output are taken from Chapter II. Lines
represent the ratio of values for the response variable of
interest between the two positions, such as territory size
(1.2:1, edge:center) or mating success (1.7:1,
Differences in whether the
center:edge) in this case.
ratio is center:edge or vice versa depend on whether the
relationship of the individual response variable is
positively or negatively associated with the population
Hypothetical 1:1, 2:1 and 3:1 lines are
level character.
also drawn.
7
F-
3:1
IL
F-
Qm
>61
U)
IiI
2:1
5
(I)
LLJO
>cr)
Q)
40
oc1
00
Lii
0
Z"
-
'-I
20
1:1
2
LiJ
-I-
0.2
0.4
0.6
EDGE/AREA
0.8
1.0
IL
IL
93
leaving a 5 x 5 habitat patch with an edge-to--area ratio
of 0.8) would decrease population density by up to 11%.
Models by Stamps et al.
(1987) suggest this population
density effect might occur even if territories are not
immediately contiguous.
If the difference between center
and edge territory sizes were greater, or if the remaining
habitat fragment was more elongate (more edge) this
decrease could be even greater.
Three hypothetical ratios
are also plotted for this model.
The case of 1:1
represents the situation where there is no spatial
variation within a cluster in either territory size or
reproductive output, and thus no effect of habitat size or
shape.
This simplistic model assumes only two levels of
positional variation in the response variable and also
assumes that the value of the response for each level is
independent of edge-to-area ratio.
More complex
situations could also be modeled in this way (e.g., more
levels of positional variation)
These considerations have implications for the design
of habitat reserves for territorial species.
Two reserves
of the same area but of different shape would support
different population densities depending on the relative
amount of edge habitat.
In terms of the single large or
several small ("SLOSS") debate for reserve design (see
Shafer 1990) , several small habitat patches would hold
lower densities and hence lower overall abundance than a
94
single large reserve equalling the combined area of the
smaller patches.
Finally, since mating success in threespot damselfish
also varies with group position (see chapter II), average
individual reproductive output of cluster members may also
depend on the size and shape of habitat patches.
This
effect is similarly dependent on the relative amount of
edge habitat in a patch.
Again, using data from chapter
II, average individual reproductive output would decrease
by about 16%, using the same fragmentation scenario as
above (Fig. 111.7) .
Wildlife managers will need to
consider such effects of grouping when dealing with
territorial species that may cluster either behaviorally
or as a result of habitat patchiness.
Acknowledgements
K. Crofoot and B. Profit were invaluable dive buddies
and assistants.
C. Blanchette, D. Booth, N. Carr, K.
Clifton, J. Harding, K. Kim, A. Kaltenberg, H. Lasker,
D.R. Robertson, P. Sikkel, B. Tissot provided various
useful assistance, encouragement and advice.
Comments
from A. Blaustein, M. Hixon, J. Miller, and J. Wolff
improved the manuscript tremendously.
I. Ivancic, D. R.
Robertosn and R. Tapia of STRI provided support in Panama.
Financial support was provided by an NSF predoctoral
95
fellowship, Sigma Xi, Lerner Gray Fund for Marine
Research, Raney Award from the American Society of
Ichthyologists and Herpetologists, and the OSU Zoology
Department.
This project was part of the requirements for
a Ph.D. degree in the Department of Zoology, OSU,
supervised by N. Hixon.
The Kuna Indians and the
government of the Republic of Panama allowed me to conduct
research in their lands.
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.
CHAPTER IV: COMPETITION WITHOUT RESOURCE LIMITATION?:
EVIDENCE FROM CLUSTERS OF INDIVIDUALLY TERRITORIAL
THREESPOT DAMSELFISH, STEGASTES PLANIFRONS
DWAYNE W. MEADOWS
Department of Zoology
Oregon State University
Corvallis, OR 97331-2914, U.S.A.
Abs tract
On patch reefs off the Caribbean coast of Panama,
threespot damselfish (Stegastes planifrons) defend
Previous
individual territories distributed in clusters.
research has shown that centrally located territory
occupants derive greater fitness-related benefits than
fish on the edge of clusters.
I tested whether there was
competition for the most desirable central positions.
If
competition was occurring, there should be 1) faster
reoccupation and 2) higher rates of intraspecific
aggression in newly opened central space relative to new
edge space in a cluster.
Also, 3) individuals should only
compete for open space that is more centrally located than
their present residence, and 4) settlement or immigration
to cleared clusters should preferentially be to the center
of the original cluster site.
The first two predictions
were supported by a paired removal experiment.
The third
and fourth predictions were weakly supported in the
removal experiment and by addition of fish to denuded
100
reefs, respectively.
Competition thus appears to be an
important factor in determining the distribution of
individual threespot damselfish on these patch reefs.
I
discuss these results in light of the claim by Wellington
and Victor (1988) that there can be competition in
damselfishes even when resources are not limiting.
I
argue that we should consider these populations to be
simultaneously both recruitment limited (in terms of local
population size) and high-quality resource limited (in
terms of local reproductive output and perhaps global
population size)
.
This conclusion permits a more complete
understanding of the dynamics of open populations because
of the role of competition in limiting local vs global
population sizes in open systems.
Introduction
Wellington and Victor (1988) claim to have shown that
intraspecific competition for territories occurred in
populations of the Acapulco damselfish, Stegastes
acapulcoensis, without there being a limited resource in
the population.
deep water sites.
This species occupies both shallow and
Shallow sites supported higher
densities of damselfish than deeper sites and both body
size and female gonosomatic index, measures of fitness,
were larger in shallow sites.
Only removals of shallow
101
water fish were generally replaced within 48 hours;
vacated sites in deeper water were not reoccupied.
Wellington and Victor (1988) interpreted these results to
indicate that competition was occurring for shallow water
territory sites, but that space was not a limiting
resource in the population, since deep water sites were
always available.
Yet, competition is usually defined in
terms of resource limitation, and resource limitation is a
crucial assumption to most models of competition (see
Keddy 1989 and references therein).
Nevertheless, Wellington and Victor's seemingly
controversial claim has generated little discussion in the
literature.
I found only two references to their
assertion (Warner and Hughes 1988, Persson and Johansson
1992)
.
Persson and Johansson (1992) accepted Wellington
and Victor's conclusions, while Warner and Hughes (1988)
pointed out that Wellington and Victor assumed that
resource undersaturation implies no density-dependent
mortality effects occur.
Here,
I consider how another
damselfish system, in which there is also competition for
territory space, relates to this controversy.
I provide
empirical evidence showing that limitation of high quality
resources leads to competition that limits local
reproductive output and possibly also limits global
population size, while local population size is limited by
recruitment.
In my study, competition is for position
102
(center vs edge) within a cluster of individual
territories rather than for shallow vs deep water sites.
Different positions within animal groups or clusters
are often favored because of lower predation rates
(Hoogland and Sherman 1976, Foster 1981, Gross and
MacMillan 1981, Rayor and Uetz 1993), higher feeding rates
(Rayor and Uetz 1990, Burger and Gochfeld 1991, Krause
1993), or better mating opportunities (e.g., Rippin and
Boag 1974, Rayor and Uetz 1990) .
Dominant individuals
often obtain the more desirable position, which is often
the center of the cluster (Rippin and Boag 1974, Fausch
1984, Rayor and Uetz 1990).
However, in situations where
the more dominant individuals do not appear to obtain the
better locations (Gratson et al. 1991), where position in
a group depends on initial order of access (see Stamps
1988, Shapiro 1991), or where clustering is the result of
habitat patchiness, it is less clear whether, or to what
extent, competition will influence the position of
individuals in a group or cluster.
I tested for such intraspecific competition for
residence in more beneficial central positions in clusters
of territories in the threespot damselfish, Stegastes
planifrons.
In this species there is little movement
among territories and clustering may result from habitat
patchiness, though slightly larger individuals are found
in the center of clusters (see chapter II)
.
Chapter II
103
showed that fish occupying central positions in clusters
have (relative to edge fish) : slightly higher
intraspecific chase rates, much lower interspecific chase
rates, and overall rates of aggression less than half of
those of threespots on the edge of a cluster.
Central
individuals also lost much less of the food in their
territories to intruders (mostly schooling parrotfish), as
measured by feeding rates, had similar food intake rates,
smaller territory sizes, grew faster, and males obtained
more and larger clutches of eggs to guard.
There were no
positional differences in age or survivorship.
Therefore,
central cluster positions are considered to be more
desirable.
I predicted that if competition for central territory
space is occurring there should be: 1) faster reoccupation
of newly available central habitat relative to newly
opened edge habitat, 2) higher rates of intraspecific
aggressive chases in the center of a cluster, as more
individuals fight over the newly opened central space or
the fighting there is otherwise more intense, 3)
competition only for locations more desirable (i.e., more
central) than the current residence, and 4) preferential
settlement or immigration to central positions in
completely depopulated habitats.
104
Methods
Study system
Stegastes pianifrons maintains year-round
territories, less than 1 m2 in area, from within which
they feed on various micro- and macroalgal species
cultivated in a 'tlawn"
(Brawley and Adey 1977, de Rutyer
van Steveninck 1984, Hinds and Ballantine 1987) .
Male
territories also contain nests which the males guard,
protecting demersaiiy spawned eggs which remain in the
territory for 4-5 days until hatching into pianktonic
larvae (Robertson et al. 1990)
.
Territories are defended
against conspecifics of both sexes and a variety of other
herbivores (e.g., parrotfishes, surgeonfishes, and sea
urchins), and egg predators or other carnivores (e.g.,
wrasses, Thresher 1976, Williams 1978 and 1981, Robertson
1984, and Ebersole 1985).
At my study site, individual
territories are clustered on coral patch reefs varying in
size from 1-1000 m2.
The research was conducted at the San Bias Marine Lab
of the Smithsonian Tropical Research Institute on the
Caribbean coast of Panama.
reefs see Robertson (1987) .
For a map of specific patch
The patch reefs and their
characteristics are more fully described in chapter II.
105
Experiment removal of individuals
To test for differences in reoccupation rates and
levels of agonistic interaction in newly opened space
(predictions one and two), I conducted the following
experiment in September and October of 1992.
I
haphazardly removed 24 matched pairs of edge and center
individuals from different patch reef clusters of
threespots.
Before removals, the boundaries of each
individual's territory were marked using 6-8 pieces of
colored flagging tape, based on 20 mm
observations.
I
then quantified baseline rates of intra- and interspecific
chases occurring during 10 mm
activity-budgets for these
same fish between the hours of 0800-1000.
Each individual
was then removed from its territory at approximately 1000
using a hand net.
At 1,
6, 24, and 48 hours after the
removal I conducted additional 10 mm
activity-budgets.
counted all intra- and interspecific chases that occurred
within the marked boundaries of the original territories.
Chases did not vary with time of day in a previous study
(see chapter VI).
My criteria for when experimentally
vacated space was reoccupied was when an individual was
defending at least 50% of the space and was actively
feeding in the area.
To test prediction three,
I
fortuitously observed the origins and identities of
potential competitors during monitoring.
I analyzed these data using repeated measures ANOVA's
with cluster position and time as factors.
Because center
and edge positions differed initially in baseline levels
of chase rates, and I was oniy interested in the change
relative to these background levels,
data in the following way.
I transformed the
I subtracted the mean
background difference between center and edge positions,
obtained from the pre-removal time budgets, from the postremoval data for the position with the larger absolute
In other words, I subtracted the mean background
value.
difference from the center position for chases with
conspecifics and from the edge position in chases with
heterospecifics.
Under the null hypothesis, there would
be an expected difference between positions of zero for
each response variable.
Any treatment effect would then
result in a significant main effect.
Experimental deporulation of reefs
To examine preference for immigration or settlement
to central cluster positions (prediction four) ,
I cleared
all adult S. planifrons from three patch reefs (Pico Feo
#4, Pico Feo #14, Aguadargana #4) in April 1993.
Approximately every two weeks through June, I censused all
adult
.
planifrons on these reefs.
Immigration during
this time was too low (1-4 fish/reef) to permit data
107
analysis.
Therefore, in June I experimentally added 44
adult fish to the Aguadargana #4 reef, from a source reef
2km distant, in an attempt to encourage settlement on this
reef.
Only three fish remained from this addition after
two days, possibly because most algae had been eaten by
intruding parrotfishes prior to the arrival of the
damselfish.
Finally,
I added adult fish from distant
source reefs to two patch reefs (Aguadargana #6 and Pica
Feo #16) immediately after removing the prior residents.
This manipulation ensured that algal food was still
available after the removals.
The additions were of an
equivalent number of fish to those that were originally
present on these reefs so that I could detect preference
for a particular position of colonization. These data were
analyzed with G tests to test for preferential
colonization relative to the initial distribution of fish
on these reefs.
Results
Experiment removal of individuals
Prediction 1, relative reoccupation rates of vacated
territories
Reoccupation of experimentally vacated territories
was significantly faster in the center than the edge of
territory clusters (Table IV.l)
All 24 central areas
were reoccupied within six hours of the removal.
However,
five of 24 edge territories were not reoccupied by the end
of the experiment two days later.
On three of those five
occasions, I observed schools of parrotfish, mostly Scarus
iserti, enter the unoccupied territory and feed on the
algal lawn until there may have been too little algae to
support a damselfish.
Prediction 2, relative intraspecific chase rates
Following removals, intraspecific rates of aggression
increased in both cluster positions, but to a much greater
extent in center positions (Fig. IV.1A, Table IV.2) .
was especially true one hour after the removal.
also a significant time effect.
This
There was
Edge areas quickly
returned to background levels, but center areas took
longer to recover.
It may be argued that central areas in
a cluster should have had faster reoccupation rates and
higher chase rates than edge areas solely due to the fact
that the central areas are closer to a larger number of
potential competitors.
Therefore, the differences found
above may not be a result of increased levels of
competition per Se.
Indeed, the number of immediate
neighbors was greater for individuals in the center of a
cluster (df= 1, 216, F
220.5, p< 0.001)
.
Center
109
Table IV.l
Relative frequencies of reoccupation times by
lanifrons into experimentally vacated territories by
position within a cluster.
.
Reoccupation time (hrs.)
cluster
position
>48
1
6
24
48
Center
21
3
0
0
0
Edge
14
2
2
1
5
G= 5.1, df= 1, p< 0.025
Data are the number of individuals meeting the
criteria for reoccupation at each observation time period.
The G test is for only two time categories, 1 hr. and > 1
hr., in order to have a large enough sample size in each
Note:
cell.
110
territories had 5.05 (± 0,09, se) neighbors, while edge
territories had 3.38 (± 0.08) neighbors.
I accounted for
this fact by modifying the data in Fig. IV.1 and Table
IV.l by dividing the raw data for central areas by 1.49,
the ratio of center to edge neighbors, and reanalyzing
these data.
This adjustment did not alter the statistical
conclusions.
Interspecific chases did not vary by position in a
cluster, or with time (Fig. IV.lB, Table IV.2), throughout
the course of the experiment.
Prediction 3, position related competition
I was not able to track the movements of many of the
colonizing individuals during the experiment.
often 50 or more damselfish on a reef.
There were
When individuals
could be tracked, it was usually immediate neighbors that
took over newly opened space and shifted their activity to
this new territory.
In any case, I never saw a central
individual compete for vacated edge space out of about
eight individuals observed.
111
Figure IV.1. A) Intraspecific and B) interspecific
aggressive chase rates by S. planifrons reoccupying
vacated territory sites following the experimental removal
"B"
of center vs edge individuals. Error bars are se's.
See
Table
IV.2
for
= preremoval baseline observations.
ANOVA results.
14
12
Conspecifics
A
\
10
position: p< .001
time: p< .001
8
6
S
-.center
4
2
edge
0
(I)
I
I
1
I
I
B
cD
0)
0
I
I
I
T
0
Heterospecifics
4
center
2
position: NS
time: NS
I
0
B1
E
6
24
Time (His.)
48
Table IV.2
Repeated measures ANOVA results for chase rates by S. planifrons toward
conspecifics and heterospecifics during reoccupation of experimentally vacated
territories.
conspecifics
Source of
variation
Position (P)
error
Time CT)
P x T
error
Note:
df
1
46
3
3
138
MS
F
6.66
0.74
2.76
0.67
0.37
9.0
7.5
1.8
heterospecifics
p
< .001
< .001
.15
df
1
46
3
3
138
MS
F
p
1.5
30.3
7.4
10.5
15.8
0.05
.83
0.47
0.66
.71
.58
See methods for analysis details.
H
H
113
Experimental depopulation of reefs
Prediction 4, position of reoccupation of depopulated
reefs
Twenty-seven and 40 fish were removed from the
An
Aguadargana #6 and Pico Feo #16 reefs, respectively.
equivalent number of potential colonizers were added to
After six days, twelve of the transplanted
these reefs.
fish had settled on each of the reefs (Table IV.3).
The
positional distributions of these settlers did not differ
significantly from the initial distribution of fish
(though the Pico Feo reef was only marginally
insignificant)
.
However, this test may have been over-
conservative because the initial distributions themselves
may have been the result of competition for cluster
positions.
Therefore, 1 also compared the settlement data
to the amount of available habitat in central vs edge
positions.
Availability of habitat was determined by
measuring the length and width of each reef and
calculating its area based on the reef's shape.
All space
less than 1 m from the patch reef boundary was considered
edge habitat.
I then calculated expected distributions of
settling fish based on available space and assuming no
position preferences.
Comparing the settlement
distributions with these data showed that preferential
114
settlement occurred to the center of clusters for the Pico
Feo reef, but not the Aguadargana reef (Table IV.3).
Discussion
Competition for central positions in clusters
Adult threespot damselfish compete for the more
desirable central positions in territory clusters, as
evidenced by the faster reoccupation and greater
intraspecific aggression occurring near newly opened
central territories, as well as by the preferential
settlement to the center of one depopulated cluster.
This
conclusion seems hardly surprising since the relatively
large difference in growth and mating success between the
two positions should select for such behavior (see chapter
II)
fiForayingit behavior, short visits to other parts of a
patch reef, should provide S. planifrons with the
opportunity to assess variation in territory quality in a
cluster (Itzkowitz 1978, chapters II and VI)
Nevertheless, abandoning a usable territory must be a
risky decision for a damselfish.
Males may have to
abandon egg clutches and invest a great deal of energy and
time in preparing a new nest.
Both sexes will have to
fight off other individuals, at risk of serious injury
115
Table IV.3
Center vs edge frequency distribution of
planifrons on
two patch reefs before and after experimental
depopulation, and calculated frequencies based on random
distribution of actual settlers to available habitat.
.
Cluster
reef
AD
PF
position
time
Center
Edge
before
17
10
after
9
3
available habitat
59
6.1
before
24
16
after
10
2
available habitat
6.1
5.9
G
p
0.80
> 0.20
3.07
0.08
3.34
0.07
5.56
0.02
The data are for immediately before depopulation,
and one week after new individuals had been released on
these reefs. Data for available habitat are calculated
using the actual number of settlers to determine an
expected value (see methods)
AD is Aguadargana #4, PF is
Pico Feo #16.
G test results in each case are relative to
the after-removal data for that reef.
Note:
.
116
(personal observation)
,
gaining control of the new
territory while still having to fight off conspecifics at
the original territory site.
My results of interactions
with territory competitors suggest these aggressive costs
may be very high.
During acquisition of a new territory,
algal food supplies in both territories are likely to be
more susceptible to decimation by schools of parrotfish or
surgeonfish (see Results and Robertson et al. 1976), which
could render a territory uninhabitable.
The lack of
reoccupation of some edge areas also suggests that space
per se is not limiting in this system, as was found by
Robertson et al.
(1981) around San Bias.
These results corroborate and extend the results of
Itzkowitz (1978), who removed three central and three edge
S. pianifrons from a cluster and found that only the
central positions were reoccupied after 24 hours.
Itzkowitz did not measure chase rates during his removals
or preferential settlement to unoccupied habitats.
Studies of other species have also found competition for
central cluster positions.
Rippin and Boag (1974) used
sequential removals to show that male grouse competed for
central positions in leks.
However, Gratson et al.
did not find competition in the same species.
et al.
(1991)
Robertson
(1979) found competition for central positions in
surgeonfish clusters.
All ten removals of central
individuals in their study were replaced while only eight
117
of 17 edge removals were replaced.
Finally, Rayor and
tietz (1990) showed experimentally that a spider species
competed for central positions in clusters.
None of these
other studies used behavioral observations of agonistic
interactions to estimate the costs of obtaining a central
territory as was done here.
Interspecific chases did not change in either
position during the removal experiment, suggesting there
was little interspecific competition for these
territories.
Competition without resource limitation?
Wellington and Victor (1988) claim to have found
competition without resource limitation in Stegastes
acapulcoensis.
Although the fish competed for shallow
sites, deep water sites were always available on the reef,
so they concluded that resources were not limiting and the
population was recruitment limited.
damselfish system is similar to
.
The threespot
acapulcoensis, except
that instead of shallow and deep water sites that vary in
quality there is variation between center and edge areas
in territory clusters.
Central areas, which provide
higher fitness measures (see chapter II), are vigorously
contested and rapidly occupied while available edge space
goes unused.
Territory size is smaller (see chapter II)
118
and densities are higher (unpublished data) in cluster
centers.
I argue that resources were in fact limiting in both
systems.
In S. planifrons, central areas are the limiting
resource, while in
are limiting.
.
acapulcoensis, shallow water sites
This may merely seem to be a trivial
semantic distinction about what exactly is the resource in
question.
However, I suggest that this distinction has
important implications.
Wellington and Victor (1988) recognized that resource
quality variation is the crux of the matter.
When
resource quality variation exists, and is correlated with
variation in fitness, it is the high quality subset of the
resource that becomes important in terms of competition.
At population densities below those limited by the high
quality resource, there should be little variation in
fitness due to competition.
At densities above the level
limiting high quality resources, competitive interactions
should occur and lead to greater variation in fitness
within the local population (e.g., a cluster in my study
or a combination of contiguous deep and shallow sites in
Wellington and Victor, see Figure IV.2).
The high quality
resource then is a resource limiting the reproductive
output of the local population if not the local population
size (Figure IV.3).
Locally limited reproductive output
may subsequently limit global population size (i.e., the
119
large-scale population defined by the range of larval
dispersal in open systems, see Figs. IV.2 and IV.3)
Given the open nature of reef-fish populations, where
locally spawned gametes settle as larvae at distant reef,
one cannot simply redefine the population as that area
including only the high-quality resource.
We can conclude
that the reproductive output of the population is limited
by high-quality resources.
However, we can also conclude
that the local population size is simultaneously limited
by recruitment, because living space per se is not limited
(e.g., Doherty 1983, 1991; Doherty and Williams 1988).
By recognizing that different population parameters
of these damselfish can be limited by recruitment and by
high-quality territory sites at the same time, we can gain
a better understanding of these species population
dynamics than by relying on single process explanations
(see also Warner and Hughes 1988; Hixon 1991; Jones 1991).
For instance, by knowing the distribution and abundance of
high-quality resources, we can predict the spatial
distribution of individuals in the population, as well as
the resource abundance and population density at which
competition and density-dependent fitness effects will
occur.
In addition, the presence of high-quality resource
limitation may allow us to adequately model the dynamics
of the population as a whole.
If high-quality resources
120
Figure IV.2.
Diagrammatic representation of local vs
global populations in open systems. The situation
pictured shows high-quality and low-quality subhabitats
arranged as in my clusters, but other distributions are
possible.
LOCAL vs GLOBAL POPULATIONS
Local population
e.g., cluster
Global population
i.e., range of larval dispersal
High quality subhabitat
U Low quality subhabitat
Uninhabitable
121
Figure IV.3.
Limitation of local and global populations.
A) Limitation of local population size (NL) by recruitment
and local reproductive output (RO) by competition for
At local population sizes
high-quality subhabitats.
between KHQ (high quality subhabitat carrying capacity)
(Low quality subhabitat carrying capacity), both
and K
recruirnent and competition simultaneously limit the local
Note that KHQ + KLQ = K, the
population in some way.
standard level of carrying capacity, above which the
population is always limited by competition alone. B)
Standard model of limitation of global population size
Note that
(NG) by larval recruitment and competition.
competition for high quality subhabitats may also limit
global population size at levels of larval recruitment
usually assumed to limit global population size (i.e., on
This would occur because
the left half of the graph) .
such competition may decrease larval recruit levels below
what they might otherwise be through the effect
See text for more details.
demonstrated in A above.
122
Figure IV.3, Continued,
A. LOCAL POPULATION
4-I
4-I
0
C)
>
4-I
C-)
0
0
L.
C)
KLQ
KHQ
Local population size
(NL)
B. GLOBAL POPULATION
4NG Recruitment
Limited
7"
7
NG
Cornpetition
Limited
/
0
/
0
-
/
/
/
/
/
/
/
0
CD
Larval recruitment
123
limit the reproductive output of the population and
recruitment is sufficient to saturate the available highquality resources (as occurs in both Wellington and
Victor's and my studies), then we can approximate the
dynamics of the population as a whole using standard
competition models.
In other words, the global population
may have the characteristics of a density-dependent
system.
This approach may be useful in some
circumstances, such as when we already have long-term data
to indicate that recruitment exceeds the high-quality
resource abundance.
It should be emphasized that only in
open populations is it possible to have situations like
these, in which there is local limitation of reproductive
output by competition, despite recruitment limitation of
local population size, and which may then translate into
global limitation of population size.
Finally, these effects of resource quality variation
make it more difficult to identify a priori what the
potential limiting resource actually is when considering
the occurence of competition in populations.
abundance of a resource may be inadequate.
Simple
The problem is
exacerbated in these two cases by the fact that the
different quality resources are in close proximity.
It is
even conceivable that the different quality resources are
spatially interspersed.
This problem in defining a
resource a priori makes it imperative that resource
124
limitation be shown before competition is inferred (see
Otherwise, apparent
Keddy 1989 and references therein).
competition (Holt 1977) or other indirect effects can be
missed.
It also becomes necessary to understand the
relationship of particular resource levels to fitness,
otherwise the occurrence of competition may not be
For example, if I had not been aware of the
recognized.
spatial variation in territory quality within a cluster,
and had disregarded territory position in the removal
experiment, I would have incorrectly concluded there was
no competition in this system.
In conclusion, by recognizing and considering the
dependence of population dynamics on potentially multiple
simultaneous processes occurring on different spatial
scales we can gain a clearer understanding of the
population ecology of organisms.
Acknowledgements
K. Crofoot and B. Profit were invaluable dive
buddies.
M. Carr, K. Clifton, J. Harding, H. Lasker, D.R.
Robertson, P. Sikkel, B. Tissot provided various useful
assistance
Comments from A. Blaustein, M. Hixon, B.
Menge, B. Miller and J. Wolff improved the manuscript
tremendously.
Special thanks to my major advisor, M.
Hixon, for innumerable assistance.
Financial support was
125
provided by an NSF predoctoral fellowship, Sigma Xi,
Lerner Gray Fund for Marine Research, Raney Award of the
American Society of Ichthyologists and Herpetologists, and
the OSU Zoology Department.
I. Ivancic, D. R. Robertson
and R. Tapia of STRI provided logistical assistance in
Panama.
The Kuna Indians and the government of the
Republic of Panama allowed me to conduct research in their
lands.
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129
CHAPTER V: EFFECTS OF HABITAT GEOMETRY ON TERRITORIAL
DEFENSE COSTS IN A DANSELFISH
DWAYNE W. MEADOWS
Department of Zooloqy
Oregon State University
Corvallis, OR 97331-2914, U.S.A.
Abstract
I measured spatial variation in aggressive chase
rates within clusters of individual territories defended
by threespot damselfish, Stegastes planifrons.
I found
that chases with conspecific intruders were lower on the
edge of a cluster and higher but equal in more centrally
located positions.
In contrast, chases with
heterospecific intruders, mostly parrotfishes, were
highest on the cluster edge and declined toward the center
of the cluster.
These results were compared to
predictions of models proposed by Stamps et al.
(1987).
The chases with conspecifics did not completely match the
model predictions, in that the relative spatial
differences in intrusions was greater than expected and
the location of peak intrusions was more central than
predicted.
This may be due to habituation effects.
Chases with heterospecifics did match predictions of the
model so that the current models may be sufficient to
explain these situations.
130
Introduction
The spatial position of an individual relative to
other group members has long been known to influence both
antipredatory and territorial defense costs (Inglis and
Isaacson 1978, Robertson et al. 1979, Gross and MacMillan
1981)
.
The selfish-herd theory of Hamilton (1971)
proposed that central group members would suffer lower
predation than edge members because of the protective
This effect
screen offered by more peripheral neighbors.
should also apply to territorial defense costs in animal
clusters because central territories could be buffered by
peripheral territories (see Chapter III).
Stamps et al.
(1987) modeled spatial variation in territorial defense
costs in groups under three situations, including one
analogous to the selfish-herd (see below).
Each case
differed both in the suitability of habitat surrounding
the occupied patch of interest and in the effect that the
boundary between the two habitats had on the intruders.
The models make different predictions about spatial
variation in defense costs, what Stamps et al.
"intruder pressure."
(1987) call
At the time, no direct empirical
evidence on fine-scale spatial variation in intruder
pressure was available to test the predictions of these
models, though spatial patterns in territory size in a
number of systems were consistent with the predictions.
131
Here I provide fine-scale data on spatial variation
in territory defense costs in clusters of individuals and
use these data to test two of the models of Stamps et al.
(1987).
I studied the Caribbean threespot damselfish,
Stegastes planifrons.
This species maintains individual
year-round territories less than 1 m2 in area, within
which they feed on various micro- and macroalgal species
cultivated in a "lawn"
(de Rutyer van Steveninck 1984,
Hinds and Ballantine 1987).
Male territories also contain
nests in which the males protect demersally spawned eggs
for 4-5 days until they hatch into planktonic larvae
(Robertson et al. 1990).
At my study site, individual
territories are clustered on coral patch reefs varying in
size from 1 to 1000 m2, which are surrounded by sand.
Territories are defended against conspecifics of both
sexes and a variety of other herbivores (e.g.,
parrotfishes, surgeonfishes, sea urchins), and egg
predators or other carnivores (e.g., wrasses; Thresher
1976, Williams 1978, 1981, Robertson 1984)
Aggressive interactions with conspecific threespots
resemble the 'hard edge' model of Stamps et al.
(1987)
In this model, the habitat surrounding the occupied patch
is inhospitable to the species of interest (i.e.,
threespots) so that movements of cluster members are
confined by the patch boundaries.
The model considers
concentric loops of territories, numbered from the edge
132
towards the center.
The only inputs to the model are the
length and width of the territory clusters, the number of
intruders generated per territory, and P. the probability
that an intruder will stop movement after each territory
intrusion.
The hard edge model predicts that intruder
pressure from conspecifics will be lowest in the outermost
loop of territories (i.e., the edge of the cluster), peak
in the second loop of territories and then gradually
decline towards the center of the territory clusters.
This prediction results from the fact that edge
individuals have relatively fewer neighboring individuals
as potential intruders.
If intruders travel short
distances (i.e., if P is high) then there may be little
spatial variation in intruder pressure within the cluster.
In contrast, aggressive interactions of threespots
with heterospecifics resemble the 'soft-edge with reserve'
model of Stamps et al.
(1987).
In this model, the
boundary between the cluster and surrounding habitat does
not limit movement of the species of interest (i.e.,
heterospecifics).
Additionally, the habitat surrounding
the patch serves as a source of intruders.
This is the
case for intruders in this system, such as parrotfishes,
which feed in seagrass beds surrounding the damselfish
clusters, but make forays onto the patch reef where they
often steal algal food from within the damselfish
territories.
The soft-edge with reserve model predicts
133
that intruder pressure will be greatest in the edge of a
cluster of territories, decline steeply toward the center,
and then gradually level out in the central-most loops.
My goal was to test these predictions by measuring
intruder pressure at four different distances from the
edge of one patch reef cluster of threespot damselfish.
Methods
I worked at the San Bias laboratory of the
Smithsonian Tropical Research Institute on the Caribbean
coast of Panama.
I studied fish at 0, 2, 4, and 6 m from
the edge of Smithsoniantupo reef #1 in August 1992 (see
Robertson 1987 for a map).
to loops 1,
3,
This corresponds approximately
6, and 9 in Stamps et al's.
(1987) models.
My measure of intruder pressure was the number of
aggressive chases occurring in a ten minute activitybudget.
For each distance, I conducted 15 focal-animal
activity-budgets between the hours of 1400 and 1600, for a
total sample size of 60.
These data were analyzed with
one-way ANOVA, after log transformation to meet
assumptions.
Results
I found that chases with conspecifics were lower on
the edge but only differed significantly from the extreme
134
center of the cluster (Fig. V.1; df = 3,56, MSE = 0.45, F
= 2.8, p = .046) .
Chases with heterospecifics were
significantly higher on the edge and then declined in the
central positions (Fig. V.1; df = 3,56, MSE = 0.55, F =
6.4, p < .001), which did not differ significantly from
each other.
Discuss ion
Other studies have also found spatial variation in
defense costs in clusters, though only at a coarse scale.
Inglis and Isaacson (1978) found that geese on the edge of
flocks spent more time in aggressive interactions than
central individuals.
Robertson et al.
(1979) showed that
surgeonfish with territories on the edge of a colony had
twice as many interspecific chases with competitors as
fish with territories in the colony center.
Gross and
MacMillan (1981) found that chase rates by bluegill
sunfish towards egg predators (both conspecific and
heterospecific) were 5006 higher for fishes with nests on
the edge of a colony compared to fish in the colony
center.
The spatial pattern of conspecific chases by
threespots do not completely match the predictions of
Stamps et al's.
(1987) hard edge model.
While the model
correctly predicts that edges should have lower intruder
135
ppjfrop with A) conspecifics
Chases of
Figure V.1.
and B) heterospecifics for each of four positions within a
cluster of territories. Error bars are ± one s.e.
Letters signify groups that did not differ significantly
by Tukey post-hoc tests.
.
5
A
z
CONSPECIFICS
b
4
ab
0
(I-)
LU
2
(1)
0
1
0
1
2
3
4
I
I
5
6
7
10
a
z
HETEROSPECIFICS
B
B
6
(1)
LU
4
(I)
I
0
2
0
1
2
3
4
5
6
DISTANCE FROM EDGE (m)
7
136
pressure, it does not predict the large difference in
chase rates between the edge and the other positions.
The
model predictions are sensitive to P, the probability that
an intruder will stop in any given territory.
In this
system P is probably around 0.3 (based on unpublished
measurements of distance traveled by intruding threespot
damselfish).
Under these conditions the models predict
little spatial variation in intruder pressure.
One reason
for this discrepancy between the model predictions and my
data may be habituation to neighbors, or the dear enemy
effect (Jaeger 1981).
Neighbors may recognize each other
and not chase each other very much since they have already
established known mutual boundaries.
Fish on the edge of
clusters of territories probably interact relatively less
often with strangers than do center fish because they have
fewer neighbors and thus fewer individuals to track.
This
lower amount of habituation for center fish would then
result in higher numbers of conspecific chases for central
individuals.
Alternatively, the assumption that chase
rates equal intruder pressure may be incorrect.
Contrary to the model predictions, the second loop
did not appear to have the highest level of intraspecific
chases.
It is not clear why this is the case, but it may
be related to differences in movement dynamics between the
model organisms and threespot damselfish.
The models
assume random or straight movement that ends in settlement
137
or death in another territory, and also that there is only
one chase per territory crossed.
However, threespot
movements largely involve short round-trip forays to
nearby areas and can include multiple chases per
territory.
The spatial pattern of heterospecif Ic chases
indicates that the soft-edge with reserve model of Stamps
et al.
(1987) is sufficient to predict fine-scale spatial
variation in intruder pressure of heterospecifics in this
system.
Only the above few model inputs are necessary to
predict territory defense costs in these cases.
These results also indicate that there are few finer
scale differences in defense costs than the coarse centeredge patterns documented in chapter II.
Future work
should attempt to accurately measure the parameters of
these models in order to more quantitatively test their
predictions, consider alternative movement patterns,
account for habituation effects, and apply these models to
a wider variety of systems in order to better understand
the role of habitat geometry in affecting defense costs.
Acknowledgements
K. Crofoot was an invaluable dive-buddy.
I. Ivancic,
R. Robertson and R. Tapia provided support in Panama.
Special thanks to my major advisor M. Hixon.
Comments
138
from M. Hixon, J. Miller, and J. Wolff improved the
manuscript.
Financial support was received from an NSF
predoctoral fellowship, Sigma Xi and the Lerner gray Fund
for Marine Research.
The Kuna Indians and the government
of the Republic of Panama allowed me to conduct research
on their lands.
References
The composition of
De Ruyter van Steveninck, E. D. 1984.
algal vegetation in and outside damselfish
territories on a Florida reef. Aquat. Bot. 20:11-19.
Gross, M. R. and A. M. MacMillan 1981. Predation and the
evolution of colonial nesting in bluegill sunfish
(Lepomis macrochirus). Behav. Ecol. Sociobiol. 8:163174.
Hamilton, W. D. 1971. Geometry for the selfish herd. J.
Theor. Biol. 31:295-311.
Hinds, P. A. and D. L. Ballantine. 1987. Effects of the
Caribbean threespot damselfish, Stegastes planifrons
(Cuvier), on algal lawn composition. Aquat. Bot.
27:299-308.
The response of
Inglis, I. R. and A. J. Isaacson. 1978.
dark-bellied Brent geese to models of geese in
various postures. Anim. Behav. 28:634-635.
Jaeger, R. G. 1981.
Dear enemy recognition and the costs
of aggression between salamanders. Am. Nat. 117:962974.
Robertson, D. R. 1984. Cohabitation of competing
territorial damselfishes on a Caribbean coral reef.
Ecology 65:1121-1135.
1987.
Responses of two coral reef toadfishes
(Batrachoididae) to the demise of their primary prey,
the sea urchin Diadema antillarum. Copeia 1987:637.
642.
139
Lunar
C. W. Petersen and J. D, Brawn. 1990.
reproductive cycles of benthic-brooding reef fishes:
reflections of larval biology or adult biology? Ecol.
Monogr. 60:311-329.
-,
N. V. C. Polunin and K. Leighton. 1979. The
behavioral ecology of three Indian Ocean
leucosternum
surgeonfishes (Acanthurus lineatus,
and Zebrasoma scopas) : their feeding strategies, and
social and mating systems. Env. Biol. Fish. 4:125,
.
170.
Stamps, J. A., M. Buechner and V. V. Krishnan. 1987. The
effects of habitat geometry on territorial defense
costs: intruder pressure in bounded habitats. Am.
Zool. 27:307-326.
Thresher, R. E. 1976. Field analysis of the
territoriality of the threespot damselfish,
Eupomacentrus planifrons (Pomacentridae) . Copeia
1976:266-276.
Williams, A. H. 1978. Ecology of threespot damselfish:
social organization, age structure, and population
stability. J.
Exp. Mar. Biol. Ecol. 34:197-213.
1981.
An analysis of competitive interactions in
a patchy back-reef environment. Ecology 62:1107-1120.
.
140
CHAPTER VI: DIEL, LUNAR, AND SEASONAL PATTERNS IN
REPRODUCTIVE AND TERRITORIAL BEHAVIOR OF THE THREESPOT
DANSELFISH, STEGASTES PLANIFRONS
DWAYNE W, MEADOWS
Department of Zoology
Oregon State University
Corvallis, OR 97331-2914, U.S.A.
Abstract
Patterns in feeding, courtship, egg fanning and
territorial defense were examined at various temporal
scales in the coral-reef damselfish Stegastes planifrons.
Feeding rates by residents and egg fanning by nesting
males increased throughout the day, while aggressive
chases with conspecifics and heterospecifics, feeding
rates by intruders inside territories, and courtship and
foray (extraterritorial movements) rates did not vary with
time of day.
Diel variation in food quality or mating
constraints may explain these patterns.
At a larger
temporal scale, all behaviors were significantly lunar
cyclic, but, with one exception, only for fish resident in
the center of a cluster of conspecifics.
This pattern may
result from intense competition by dominant central fish
to spawn at the most beneficial time.
There were
significant correlations among behaviors on a lunar scale
only for intra- and interspecific chases (positive) and
intraspecific chases and occupant feeding rate (negative)
141
because the lunar cycles of the behaviors were not
synchronous.
In both center and edge positions within
clusters of territories there were significant
correlations between rates of courtship and forays,
suggesting that forays are intimately related to mate
Seasonally, there was little
assessment and choice.
significant variation in behavior, except for decreased
benthic feeding rates in August, October and November.
Spawning also decreased toward the end of the year.
These
patterns may be associated with lower nutrient
availability at the end of the rainy season.
Courtship
and intraspecific chases were positively correlated at a
seasonal temporal scale.
Few constraints on behavior were
evident from these data.
Introduction
Variation in behavior can occur at a number of
temporal scales and can be affected by different factors
at each scale.
In damselfish and other herbivorous
fishes, there is often a diel periodicity in foraging,
with feeding rates peaking in the afternoon (Lobel and
Ogden 1981, Polunin and Klumpp 1989, Petersen 1990, Zoufal
and Taborsky 1991, Choat and Clements 1993, Eruggemann et
al. 1994, Hixon unpublished data).
It is generally
thought that this pattern is due to increases in algal
142
quality during daylight hours (Taborsky and Limberger
1980, Polunin and Klumpp 1989, Horn et al. 1990, Zoufal
and Taborsky 1991)
possible.
.
However, other causes are also
For example, courtship and spawning activity,
or territorial defense, may occur in the morning and limit
feeding activity, or low territorial defense before noon
may promote morning spawning as an adaptation to minimize
the time lost to feeding (Kohda 1988, Robertson 1991)
Goulet (unpublished data) found mostly morning spawning in
Amblyglyphodon leucogaster, and dawn spawning is common in
other damselfishes (Thresher 1984)
.
However, Scwartz
(unpublished data) found afternoon spawning in Dascyllus
reticulatus and this pattern is more common in species
with pelagic eggs (Thresher 1984, Cohn and Clavijo 1988).
In damselfishes which defend territories against
intruders, territory defense rates may mirror the diel
periodicity in activity of these intruders.
Many damselfishes spawn on a lunar cycle (Thresher
1984, Robertson et al. 1990, Robertson 1991, Tyler and
Stanton unpublished data), which probably increases adult
or larval survival (Robertson 1991) .
At this temporal
scale, we might expect behavioral variation in courtship
activity or territory (especially nest) defense.
Feeding
or other activities may also be constrained by mating
activity, causing behavioral shifts between feeding time
minimization and energy maximization (Hixon 1982)
143
At larger temporal scales, variation in food
production or environmental conditions may affect feeding
rates, reproductive activity, or other behaviors.
Polunin
and Klumpp (1989) found seasonal differences in foraging
rates in Plectroglyphidodon lacrymatus.
Seasonal spawning
is especially common in temperate damselfishes, though
often there is also seasonal variation in the level of
spawning activity in tropical species (Thresher 1984,
Robertson 1990, Petersen and Hess 1991, Robertson 1991)
Danilowicz (unpublished data) provides evidence that
temperature plays an important role in seasonal spawning
patterns in Dascyllus aruanus.
Territory size may also
respond to changes in these factors, either directly, or
indirectly through changes in other energetic costs
(Ebersole 1980, Hixon 1980, Schoener 1983, Norman and
Jones 1984)
Few data, besides those on diel foraging and diel,
lunar and seasonal spawning periodicity, exist on temporal
patterns in behavior in herbivorous fishes of any kind,
including damselfishes.
I investigated such patterns over
this range of temporal scales in the Caribbean coral-reef
damselfish Stegastes planifrons.
In addition to
quantifying temporal patterns in behavior, it was my
objective to use these data to examine potential causes of
and tradeoffs among these behaviors.
144
Methods
Study species
Stegastes planifrons, the threespot damselfish,
maintains year-round territories less than 1 m2 in area,
within which they feed on various micro- and macroalgal
species cultivated in a "lawn" (Brawley and Adey 1977, de
Rutyer van Steveninck 1984, Hinds and Ballantine 1987)
Male territories also contain nests which the males guard,
protecting demersally spawned eggs which remain in the
territory for 4-5 days until hatching into planktonic
larvae (Robertson et al. 1990),
Territories are defended
against conspecifics of both sexes and a variety of other
herbivores (e.g., parrotfishes, surgeonfishes, sea
urchins), and egg predators or other carnivores (e.g.,
wrasses)
(Thresher 1976, Williams 1978, 1981, Robertson
1984, Ebersole 1985) .
At my study site, individual
territories are clustered on coral patch reefs varying in
size from 1-1000 m2.
Meadows (chapter II) found that
individuals with territories in the center of such
clusters had differences in behavior, territory size and
fitness, relative to threespots with territories on the
edge of a cluster.
I thus consider each position in a
cluster separately, as their temporal patterns in behavior
could also differ and be affected by separate factors.
145
Study site
The research was carried out at the San Bias Marine
laboratory of the Smithsonian Tropical Research Institute
on the Caribbean coast of Panama from June to September
1991, June through December 1992, and April through June
1993.
Many coral patch reefs within 2 km of the lab were
utilized (see Robertson 1987 for a map and reef
references)
.
The patch reefs and damselfish clusters were
found at 1-25 m in depth, though I only used reefs in 1lOm depth.
Patch reef characteristics are more fully
described in chapter II.
Data collection
Data were collected using 10 mm
activity-budgets.
focal-animal
All benthic feeding bites by residents
and intruders, aggressive interactions (chases) by
residents and con- and heterospecif Ic intruders, courtship
behaviors (characteristic dipping movements of males
around and under females), "forays" (extraterritorial
movements, see Itzkowltz 1978, Bartels 1984), and egg
fanning bouts by nesting males, were counted.
Males and
females are not dimorphic so I could only sex those
individuals that were seen engaging in mating behaviors.
Diel behavior patterns in territorial defense and
feeding were examined on three patch reefs
146
(Smithsoniantupo #1, Tiantupo #1E and Ulagsukun #1E) in
1991.
The day was divided into five time periods (0700-
0900, 0900-1100, 1100-1300, 1300-1500, 1500-1700)
Ten
.
individuals were sampled at each position on each reef
during each time period, for a total sample size of 300.
Foray, courtship and egg fanning behaviors were measured
on a different set of individuals in August 1992 on
Smithsoniantupo #1.
Only two time periods were used:
0800-1000 and 1400-1600.
Sample sizes for foray and
courtship data were 26 for both center and edge positions
in the morning, and 45 and 43, respectively, for center
and edge positions in the afternoon.
For the egg fanning
data, sample sizes were nine and ten for the center and
edge positions, respectively, at each time period.
The
data were analyzed by two-way ANCOVA's with position and
time as fixed factors and fish size (visually estimated
SL) as a covariate.
Fish size and position effects are
discussed in chapter II.
Lunar patterns for the same behaviors, minus egg
fanning, were examined using data pooled from all
activity-budgets collected throughout the course of a
wider study.
The total number of activity-budgets per
behavior was between 758 and 1528, depending on the
response variable, as some variables were not measured in
1991 or during other studies.
All activity-budgets
collected on the same lunar day (new moon = day 1) were
147
pooled.
Sample sizes were between 4 and 62 per position
within a territory cluster per lunar day, and averaged
from 12 to 26. Data came from one to eight different lunar
months.
Lunar cycles of behavior were determined by
testing for cross correlations between the behaviors and a
lunar cycle represented by a sine wave with a period of 29
days (Robertson et al. 1990) .
The peak of the lunar sine
cycle was on day 8, so time lags for peak activity are
relative to the first quarter stage of the moon.
The data
were not continuous over time so I could not analyze them
with other time series procedures.
Pearson product-moment
correlations among the 29 daily means for all behaviors in
each position were analyzed to examine potential tradeoffs
and relationships among the behaviors.
Seasonal behavior patterns were examined for June
through November 1992 and April through June 1993.
Ten
individuals were sampled in each position within a cluster
of territories on each of two patch reefs (Smithsoniantupo
#1 and Tiantupo #lE) in 1992 and on Smithsoniantupo 4$1 in
1993, for a total sample size of 300.
Data were collected
between 1400 and 1630 on two or three days during the
month.
Territory size was also measured for five
individuals in each position on each reef during the
mornings of the same day (see chapter II for full
details), for a total sample size of 150.
The data were
analyzed with two-way ANCOVA's with position and month as
148
fixed factors and fish size as a covariate.
Pearson
product-moment correlations for the nine monthly means
among all behaviors within each position were also
analyzed to examine potential relationships among these
variables.
Results
Diel patterns
Feeding rates increased from early morning to peak
during the late afternoon (Fig. VI.l).
Intra- and
interspecific chase rates, and feeding rates by intruders
within territories, did not vary significantly with time
of day (Table VI.1).
Foray and courtship rates were
slightly, but not significantly, higher in the morning
than in the afternoon, while egg fanning bouts by males
were significantly more frequent in the afternoon (Table
VI.2)
Lunar patterns
For all behaviors, the center position within a
cluster of territories was significantly lunar cyclic,
while intraspecific chase rate was the only behavior in
the edge position that was lunar cyclic (Fig. VI.2, Table
VI.3)
.
The time lags of the most significant cross
149
Figure VI.l. Benthic feeding rates of S. planifrons by
time of day and position within a cluster of territories.
All error bars in this and subsequent figures are se's.
AMOVA results: df = 4, 289; F = 139.8, p < .001, MSE =
Tukey test results showed that each time period
1.61.
Data
differed significantly from every other time period.
were square root transformed for analysis.
100
go
80
70
E
center
vedge
T
60
50
Cl)
40
a)
30
in
20
10
0
0800
1000 1200
1400
Time of Day
1600
Table VI.l
Aggressive interactions and intruder, feeding rates within
planifrons territories by
time of day.
Data are means (s.e.) for 30 ten minute activity-budgets per cell. ANOVA
results are (df= 4, 289) : intruder feeding- F = .257, p = .91, MSE = .237; intraspecific
aggression- F = 1.90, p = .11, MSE = 4.81; interspecific aggression- F = 1.68, p = .15,
MSE = .368.
All data were log transformed for analysis.
.
time
behavior
intruder feeding
(bites)
intraspecific
chases
interspecific
chases
position
0700-0900
0900-1100
1100-1300
1300-1500
1500-1700
center
0.1
(0.1)
0.1 (0.1)
0
0
0
edge
0.7
(0.3)
1.2
(0.4)
1.1
(0.4)
0.9
(0.3)
1.3
(0.4)
center
3.1
(0.5)
3.2
(0.5)
2.5
(0.3)
2.4
(0.4)
2.2
(0.3)
edge
2.8 (0.4)
2.1
(0.3)
1.4
(0.3)
2.2
(0.4)
2.4
(0.4)
center
1.0
(0.2)
1.3
(0.3)
0.8
(0.2)
0.5
(0.2)
1.0
(0.2)
edge
4.1 (0.6)
4.9
(0.6)
5.2
(0.8)
3.9
(0.6)
5.3
(0.6)
H
Ui
0
Table VI.2
Mean courtship and foray rates (± se) by time of day and position within a cluster of
territories in
planifrons.
Data are from 10 mm activity budgets.
Sample sizes can
be found in the Methods.
Data for forays and courtship were log-transformed for
analysis.
ANOVA results are for the time effect and are from two-way ANOVA's with
position in a cluster and time of day as factors.
.
time
behavior
foray
courtship
egg fanning
position
0800-1000
1400-1600
center
1.08
(0.27)
0.80
(0.16)
edge
0.58
(0.15).
0.35
(0.13)
center
2.77 (0.69)
1.78
(0.49)
edge
1.38
(0.41)
1.63
(0.63)
center
9.91
(1.95)
14.56
(1.40)
edge
7.30
(1.04)
10.20 (1.02)
df
F
MSE
p
1, 135
3.13
1.01
0.08
1, 135
3.70
0.73
0.06
6.83
20.75
0.01
1,
36
H
01
H
152
correlations varied among behaviors from -3 to +7 days,
relative to first quarter.
In general, the time lags were
not synchronous between positions within the same
behavior, except for occupant feeding (+3 or +4 days) and
courtship (+7 days)
There were significant correlations
.
among some behaviors within position (Fig. VI.2, Table
VI.4)
.
In the center position, intraspecific chase rate
and occupant feeding rate were negatively correlated,
while intraspecific and interspecific chase rate were
positively correlated.
Foray and courtship rates were
highly positively correlated in both positions.
Seasonal patterns
Benthic feeding rates were significantly lower in the
late rainy season months of October and November (Fig.
VI.3, df = 8, 281 in all ANOVA results for this section,
F= 25.5, p <
.001, MSE = 931.9), and also in August.
Feeding by intruders within territories was significantly
more frequent in April 1993 than in other months (Fig.
VI.3, F = 2.4, p = 0.016, MSE = 0.138) .
Intraspecific
chase rates were significantly lower in November and
higher in May (Fig. VI.3, F = 2.2, p = 0.03, MSE = 0.347)
Interspecific chases were siginificantly higher in June of
both years than in any other months (Fig. VI.3, F = 2.3, p
= 0.02, MSE = 0.400)
Courtships were significantly
higher in June 1992 than in all other months (Fig. VI.3, F
153
Figure VI.2.
Lunar variation in behaviors of
planifrons by position in a cluster of territories. Lunar
day 1 = new moon.
See Tables VI.3 and VI.4 for cross
correlations with lunar cycle and correlations among the
behaviors, respectively.
.
154
Figure VI.2.
60
Intruder I ecuirig
Occupant Feeding
i40r
20
E
0
80
60
U)
a)
40
center
20
edge
r)
Intraspecific Aggression
20
Interspecific Aggression
5'
4
15
E
0
'-3
0
XI
(I)
U)
I\
2
0
U
0
0
Co u rt s h i PS
1.0
5
Forays
I
0.8
4
E
C
E3
0.6
0
CI)
'-
A
rr
>'
2
0
0
(I,
0
0
I
0
IL
5
10
15
20
Lunar Day
25
30
0.4
kfA
J
-
0.2
0
5
10
15
i1Jf1O
20
Day
25
Table VI.3
Cross correlations between behaviors (numer of events per 10 mm) and a lunar
cycle represented by a 29 day period sine curve.
Time lags for maximal activity
are in days before (-) or after (+) a sine peak on lunar day 8 (day 1 = new
moon)
> 2 s.e. above 0.
behavior
occupant feeding
intruder feeding
intraspecific aggression
interspecific aggression
position
n
correlation
time lag
.530*
+3
.124
+4
center
632
edge
504
center
835
edge
640
.104
+5
center
869
.614*
+2
edge
659
.506*
-6
center
869
.408*
+3
edge
659
.223
+6
-
4Q5*
-
3
I-a
Ui
Ui
Table VI.3, Continued.
courtship
foray
center
380
.570*
+7
edge
378
.384
+7
center
719
.431*
+5
edge
509
.283
-2
H
(fl
Table VI.4
Pearson correlations among behaviors for each position in a cluster of territories for
Correlations above the diagonal are for the center position,
the lunar cycle data.
p <
p < .01;
p < .05;
those below the diagonal are for the edge position.
.001.
OFeed
Occupant Feeding
IFeed
.096
Inter
Court
Foray
394*
.303
.253
.194
.012
.126
.076
086
.468*
.186
.297
-.053
.020
Intra
Intruder Feeding
.250
Intraspecific aggression
.087
.220
Interspecific aggression
.154
.208
.072
Courtship
.087
.b36
.266
.180
Forays
.217
-.062
.110
.060
.766***
.653***
H
Ui
158
= 2.1, p = 0.04, MSE = 0.059).
Forays did not vary
significantly by month (Fig. VI.3, F = 1.6, p = 0.12, MSE
= 0.098), and averaged 0.23/10 mm
Territory
(± 0.05).
size was significantly lower only in August (Fig. VI.3, F
= 3.2, p = 0.002, MSE = 563147.8) .
For all of these
behaviors, all other months were not significantly
different from each other by Tukey tests.
Only one
significant correlation was found among the behaviors
(Table VI.5), courtships were positively correlated with
intraspecific chases in the edge position only.
Given the
number of correlations made, this significant outcome was
no greater than that expected by chance alone.
Discussion
Diel patterns
Feeding rate increased throughout the day in
.
planifrons as found by Robertson (1984) for this same
species, and in a number of other damselfish and
herbivorous species (Lobel and Ogden 1981, Robertson 1984,
Polunin and Klumpp 1989, Zoufal and Taborsky 1991, Choat
and Clements 1993, Hixon unpublished data).
On the other
hand, Fishelson (1970) mentions that Abudefduf saxatilis,
mainly a planktivore, foraged more in the morning, before
migrating to spawning sites in the early afternoon.
There
was no evidence, however, that time available for feeding
159
Seasonal variation in behaviors of
Figure VI.3.
See
planifrons by position in a cluster of territories.
Table VI.5 for correlations among behaviors and the text
for ANOVA results.
.
160
Figure VI.3.
Occnpon
80
rccdriq
i60
S
70
0
os
80
'
10
i.i
a)
60
m
0
03
ecriri(J
70
"0
'..
Intruder
'S
0.5
20
00
interspecific Aggression
Irstrospecific Aggression
56
[7
0
E
0
6
S
a)
01
U,
4,
0
U,
.0
U
0
U
3
0
F o rays
CourtshipS
0.8
.0
0.6 L
0.6
C
E
0
0
0.6
0.4
>'
0
0.4
a
U
0.2
0.2
00
0.0
1992
Territory Size
5000
5000
E 3000
1)
2000
000
, 3< (OUO1 <5
992
092
1993
3
Table VI.5
Pearson correlations among behaviors for each position in a cluster of territories for
the seasonal data. Correlations above the diagonal are for the center position, those
below the diagonal are for the edge position.
Occupant Feeding
.028
.019
.566
.523
.616
- .190
.301
.072
.178
.091
.655
.393
.245
.473
.007
.254
.455
-.384
.176
.361
Intruder Feeding
.590
Intraspecific aggression
.343
.608
Interspecific aggression
.649
.263
Courtship
.338
.387
.725*
.229
Foray
.167
.576
.664
.086
.422
Territory Size
.024
.235
.155
.334
.492
-.102
.199
.352
H
H
162
was limited by territory defense or courtship activity,
since none of these other behaviors varied with time of
day.
This result suggests that there is no tradeoff
between feeding and other behaviors and that there is
"freet' time available.
Thus, S. planifrons appears to be
a feeding time minimizer rather than a food energy
maximizer (Schoener 1971, Hixon 1982).
It is interesting that defense activity did not
change with time of day, when it is known that other
sympatric damselfish and parrotfish feed more frequently
in the afternoon (Robertson 1984, personal observation)
Moreover, Kohda (1988) found that intruders onto Stegastes
altus territories were less abundant in the morning and
stole less food per successful intrusion in morning versus
afternoon absences of the territory owner.
Shulman (1985)
also found that attacks by and against Stegastes
leucostictus were greater right at dusk than during the
rest of the day.
Increased rates of aggressive
interaction late in the day in laboratory colonies of
Stegastes partitus were found by Myrberg (1972).
Nursall
(1981) found no diel changes in activity associated with
increased feeding rates throughout the day in
Ophioblennius atlanticus.
Thus, spawning in the morning
cannot be to avoid intruders, but may still result in less
food loss if food quality or density inside territories is
low in the morning.
163
Finally, egg fanning by males increased during the
day.
This may reflect the fact that S. planifrons spawns
in the early morning and spends a lot of time in courtship
and mating activity during this time, or may be related to
developmental processes (see Thresher 1984, Reebs and
Colgan 1991).
Lunar patterns
The significant lunar cyclicity of behaviors from
mostly only those fish resident in the center position in
a cluster of territories was unexpected.
Spawning itself
was lunar cyclic in both positions, occurring
approximately in the three weeks after full moon
(Robertson et al. 1990, Meadows unpublished data).
Courtship and intra- and interspecific aggression were
also cyclic on approximately the same lunar period, and
were all positively correlated.
It is known that
competition for residence in the center positions is
intense (see chapter IV) and that center individuals
obtain higher mating success and growth rates (see chapter
II)
.
It may be that there is competition for spawning at
certain times in the lunar cycle, since spawning time may
be related to adult and larval fitness (Robertson 1991).
Center individuals may outcompete edge fish for these
preferred spawning times, which might then lead to similar
164
lunar patterns in courtship and foray behavior, while also
constraining feeding rate during the spawning period.
The
lag in territory defense may represent the time until egg
predators are more abundant.
The significant positive correlations between foray
and courtship rates in both positions provides evidence on
the function of forays.
Itzkowitz (1978) and Bartels
(1984) have suggested that forays may be for either mate
or territory assessment, while Thresher (1980) suggested
that forays facilitate habituation of aggression levels
among neighbors.
My data clearly suggest a strong role
for forays in courtship activity.
However, even on days
when courtship activity was low or zero, there was
significant foraying, suggesting a further role for
foraying in territory assessment, habituation, or longterm mate evaluation.
Seasonal patterns
Threespot feeding rates were lower at the end of the
rainy season than at other times of the year.
Moreover,
while spawning occurred throughout the sampling period, it
was less frequent near the end of the year.
In June 1993
and August 1992 males received an average of 2.41 ± 0.2
and 2.43 ± .37 clutches/month, while in November 1992
males received only 1.56 ± .31 clutches/month (see chapter
165
II)
.
This seasonality of reproduction was corroborated by
a similar pattern in courtship rate.
There was little
other consistent seasonal variation in behavior.
It may
be that the main factor affecting behavior patterns on
this temporal scale is variation in benthic algal food
production resulting from the seasonal cycle of rains and
lentic nutrient input near the study site.
There is a dry
season from January through April and a rainy season the
rest of the year, with rains generally increasing
throughout the season.
This rainy season is when food
production is highest.
Few other correlations existed among these behaviors
on this time scale, except for a positive relationship
between courtship and intraspecific aggression.
This
correlation may represent increased chases from courtship
related extra-territorial movements.
Therefore, little
evidence was found that would indicate constraints or
tradeoffs among behaviors on this time scale.
Temporal variation is evident on a number of
different scales in threespot damselfish.
The factors
determining this variation seem to vary with temporal
scale: food quality or dawn mating diurnally, spawning on
the lunar scale, and food production on a seasonal scale.
These results suggest that we must be careful in pooling
data over large temporal scales where different driving
forces may obscure important patterns.
Experimental
166
studies will need to be conducted to more fully understand
the causal relationships among these behaviors on each
temporal scale.
Of particular interest are the lunar
cycling of behaviors in the center position of clusters of
territories, and the apparent trade-off between feeding
and defense on the lunar scale, which suggests a time
constraint imposing energy maximization (Hixon 1982).
Allocation of time to each of the components of an animals
behavioral repertoire may have a tremendous impact on
individual fitness, and further studies of the trade-of fs
involved should be rewarding.
Acknowledgements
L. Pace, K. Crofoot and B. Profit were invaluable
Special thanks to my major
dive-buddies and assistants.
professor, M. Hixon, for innumerable aid.
R. Robertson,
I. Ivancic, and R. Tapia made my stays in Panama much more
productive.
Comments from M. Hixon, J. Miller, and J.
Wolff improved the manuscript.
Financial support was
provided by an NSF predoctoral fellowship, Sigma Xi
Grants-in-Aid, Lerner Gray Fund for Marine Research of the
American Museum of Natural History, Raney award of the
American Society of Ichthoylogists and Herpetologists, and
the OSU Zoology Department.
The Kuna Indians and the
167
government of the Republic of Panama allowed me to conduct
research in their lands.
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171
CHAPTER VII: SUMMARY
In the preceding chapters I have tried to trace the
links among center-edge differences in fitness measures,
territorial and other behaviors, and territory size for
threespot damselfish residing in groups of individual
territories.
The links are through energetic costs and
benefits associated with these behaviors and are due to a
spatial position effect whereby central residents are
protected from the costs of intrusion by more peripheral
neighbors.
This protection results in higher reproducitve
output for central individuals.
These results suggest
that the size and shape of occupiable habitats should
influence the maximum population density and per capita
reproductive output of populations as a whole.
These
effects may also apply to other territorial species found
in groups which have center edge differences in fitness or
territoriy size.
As expected from the higher fitness in the center of
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these groups to obtain the more beneficial central
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occupied.
These results suggest that at a local scale, a
population of organisms with an open system of population
dynamics can be simultaneously limited by both recruitment
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172
In addition, I have used data on fine-scale patterns
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situations with groups of individual territories.
I found
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result of habituation to territorial neighbors.
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I have shown that there is temporal
variation in behavior and territory size in these
damselfish over diel, lunar and seasonal time scales.
These temporal patterns will require future experimental
tests to determine their cause(s)
173
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