HETEROSPECIFIC AGGRESSION AND DISPERSION IN TWO SPECIES
OF SEA ANEMONES IN THE FLORIDA KEYS
by
Edward Mark Barham
A Thesis Submitted to the Faculty of the
College of Science in Partial Fulfillment of the Requirements for the Degree of
Master of Science
Florida Atlantic University
Boca Raton, Florida
August 1991 HETEROSPECIFIC AGGRESSION AND DISPERSION IN TWO SPECIES
OF SEA ANEMONES IN THE FLORIDA KEYS
by
Edward Mark Barham
This thesis was prepared under the direction of the candidate's thesis advisor, Dr. Godfrey R. Bourne, Department of Biological Sciences, and has been approved by the members of his supervisory committee. It was submitted to the faculty of the College of Science and was accepted in partial fulfillment of the requirements for the degree of Master of Science.
SUPERVISORY COMMITTEE: K23~ . Bourne, Chairman
~~-~~~aiPh rcJfiaffiS 2/£'~ -z;u~:;__:_ Dr. Sheldon Dobkin
Dr. Michael S
Sheila Mahoney Qflte I Acting Dean, Graduate
ii ACKNOWLEDGEMENTS
I sincerely thank the members of my thesis committee -
Dr. Ralph M. Adams and Dr. Sheldon Dobkin for their critical reading of the manuscript. I acknowledge Dr. w. R. Brooks for helping me get started. I especially thank Dr. Godfrey R.
Bourne for assuming the role of thesis chair at a critical time. He was also generous with access to his laboratory, computer, and most importantly with time he spent sharpening my research focus, and reviewing and improving my thesis. I also thank Eileen Garcia for help in slide preparation; Cathy
Owen for critically reading a draft, and Ann Broadwell, JoAnne
Hansen, MaryBeth Mihalik and Jeff Rathgeb for their assistance in the field. Two Marine Biology Research Grants through the
Department of Biological Sciences, and Dr. Dobkin's financial assistance during my last year at FAU made this thesis possible. Finally, I am grateful to my parents for their love, patience and support.
iii ABSTRACT
Author: Edward Mark Barham
Title: Heterospecific aggression and dispersion in two species of sea anemones in the Florida Keys.
Institution: Florida Atlantic University
Advisor: Dr. Godfrey R. Bourne
Degree: Master of Science
Year: 1991
The relationship between heterospecific aggression and dispersion in sea anemones is poorly understood. This relationship was elucidated for Bartholomea annulata Leseur and Aiptasia pallida Verrill at a quarry in the Florida Keys.
Laboratory experiments indicated that B. annulata was the aggressor. Individuals of both species moved to avoid contact under both laboratory and field conditions. Field assessment of dispersion revealed aggregated patterns, as well as vertical segregation between the species. Bartholomea annulata was most abundant at a depth of 0.75 m, while ~- pallida dominated at the surface. Heterospecific aggression may be just one but probably an important one of several factors mediating the spatial distribution of these two sea anemones.
iv TABLE OF CONTENTS
ACKNOWLEDGEMENTS ...... • . • • ...... iii
ABSTRACT ...... •...... •...... i v
LIST OF TABLES ...... vi
LIST OF FIGURES ...... vii
INTRODUCTION ...... 1
MATERIALS AND METHODS ...•...... 4
Natural history of study animals ...... 4
Study site ...... 5
Collection and maintenance of study animals ...... 7
Laboratory experiments on aggressive interactions ...... 7
Laboratory experiments on spatial dispersion .....••••.... 9
Field observations of spatial dispersion ...... 10
Field transplant experiments ...... 11
RESULTS ...... 12
Laboratory aggressive interactions ...... •...... 12
Laboratory dispersion patterns ...•...... •.....•••...... 12
Spatial distribution of anemones in the field ...... 15
Aggressive interactions in the field ...•••••••••.••••..• 26
DISCUSS ION ...... 2 9
Aggression ...... 29
Aggression and dispersion patterns ...... 31
Aggression and vertical zonation ...... 33
LITERATURE CITED ...... 37
v LIST OF TABLES
I. Nearest-neighbor analysis of dispersion for sympatric ~· annulata and ~· pallida in an experimental aquarium ...... 13
II. Nearest-neighbor analysis of dispersion for ~· annulata and ~· pallida in separate experimentalaquariums ...... 14
III. Analysis of vertical distributions for B. annulata and ~· pallida from transect samples at the Craw 1 Key quarry ...... 16
IV. Analysis of vertical distributions for ~· annulata at each of seven depths from transect samples at the Crawl Key quarry ...... 17 v. Analysis of vertical distributions for ~· pallida at each of seven depths from transect samples at the Crawl Key quarry ...... 18
VI. One-way ANOVA for the difference in abundance between ~· annulata and ~· pallida at the Crawl Key quarry ...... 19
VII. One-way ANOVA for differences in~· annulata's abundance at different depths at the Crawl Key quarry ...... 2 0
VIII. One- way ANOVA for differences in~· pallida's abundance at different depths at the Crawl Key quarry ...... 2 0
IX. Comparisons of paired abundance means for ~· annulata at different depths using the post hoc Tukey test ...... 21
X. Comparisons of paired abundance means for ~· pallida at different depths using the post hoc Tukey test ...... 23
vi LIST OF FIGURES
1. Inset map of southern Florida showing the location of Crawl Key. Enlarged map of the Crawl Key area of Monroe County, Florida, indicating the location of the quarry (X) where field work was conducted ...... 6
2. Scatter plots and regressions of the abundances of anemones as a function of depth (a)~· pallida and (b)~· annulata ...... 27
vii INTRODUCTION
An important goal of evolutionary ecology is to discover
how specific processes affect patterns observed in nature.
The process of dispersion is usually the result of behavioral
interactions among individuals. Analysis of the patterns and
behavioral interactions of individuals is important to
comprehending the behavioral ecology of these organisms (Brown
& Downhower, 1988). Furthermore, the spatial arrangement of
individuals may be central to understanding the structural and
functional relationships of population density, persistence
and gene flow in ecological communities. Competition among
con- and heterospecifics may be a major factor determining
spatial distributions. Aggressive behavior (i.e., any hostile
act or threat made to protect territory, the family group or
offspring, or to establish dominance [Lincoln et al. 1982]) is
a primary facet of interference competition.
Connell (1961) pioneered studies that examined the
relationship between heterospecific competition and dispersion
under field conditions. He found that the lower limits of the
intertidal barnacle Chthamalus stellatus were restricted by
competition for space with another barnacle, Balanus
balanoides, which occurs lower in the intertidal zone.
Aggression and its effect on dispersion has also been studied
1 2 in many anthozoans (Lang, 1973; Sheppard, 1979; Cope, 1981; Bradbury & Young, 1983; Logan, 1984; Chadwick, 1991). However, most of the studies with anemones examined conspecific interactions (Francis, 1973a, b, 1976, 1988;
Purcell & Ki tting, 1982; Quicke & Brace, 1983; Dorsett & Turner, 1986). Few studies have addressed heterospecific interactions and their relationships to dispersion in sea anemones. Chao
(1975) reported that the dispersion of Anthopleura elegantissima was limited, in part, by heterospecific competition with Metridium senile and Corynactis californica.
Likewise, Sebens (1976) found a hierarchy of species aggressiveness in laboratory experiments. This correlated with dispersion in the field; the more aggressive anemones occupied stable areas of the reef. Less aggressive anemones occupied unstable substrates such as areas of rapid coral growth and collapse, thereby avoiding competition with anemones and other organisms. Additional work is needed in order to elucidate life history diversity, and to better understand the relationships between heterospecific competition and spatial distribution in sea anemones living in different environments, and therefore, under different selective forces. 3
I employed a combination of field and laboratory observations and experiments to define and describe the local spatial distribution of two sympatric sea anemones,
Bartholomea annulata Leseur and Aiptasia pall ida Verrill, found in the Florida Keys. These data were used to test the following a priori hypotheses as suggested by the earlier findings outlined above, that: (1) B. annulata is more aggressive than A. pallida; (2) heterospecific individuals capture space and minimize contact through aggressive interactions; ( 3) dispersion patterns for both species are clumped; and (4) ~· annulata and~· pallida exhibit vertical zonation. MATERIALS AND METHODS
Natural history of study animals
Bartholomea annulata is distributed from Florida to
Texas, and from the Bahamas southwards through the West Indies
(Carlgren, 1951; Amos & Amos, 1988). This species can reproduce by sexual, or asexual means through pedal laceration
(Jennison, 1981). Bartholomea annulata is usually found in large aggregations on vertical walls down to 30m (J. Rathgeb, pers. comm.), but is sometimes found individually on turtle grass (Thalassia testudinum) flats and on sandy substrates
(pers. obs.). The color of the column varies from white to light brown while the tentacles are brown with cream colored transverse rings (McMurrich, 1889; Carlgren, 1951; pers. obs.). Individuals with fully extended columns are up to 13 em along the oral-aboral axis, with a diameter of 2.5 em
(pers. obs.).
Aiptasia pallida is distributed from Maine to southern
Florida (Cary, 1911; Carlgren, 1951; Kaplan, 1988). Only asexual reproduction by pedal laceration has been reported thus far (Cary, 1911; Chia, 1976; pers.obs.). Individuals are
4 5
found in large aggregations attached to mangrove roots, rocks,
or sometimes to sponges, algae, and other sessile marine organisms which may already cover rocks (Carlgren, 1951; pers. obs.). Aiptasia pallida is not usually found below depths of
3m (pers. obs.). Its tentacles are usually light reddish brown and may have pale spots, and the column is fawn colored
(Carlgren, 1951; pers. obs.). Individuals with fully extended columns can measure up to 5 em along the oral-aboral axis, with a diameter of 0.75 em (pers. obs.).
Study site
I conducted field work at an abandoned quarry on the northern (gulf) side of Crawl Key, Monroe County, Florida, USA
(24°44 I 45"N; 80°58 I 55"W) (Fig. 1). Descriptions of climate are available in Chen & Gerber (1990), geology in Brown et al.
(1990), and vegetation in Odum & Mcivor (1990). This limestone quarry was mined during the early 1900s. Its southern, western and eastern walls are z 200m long; however, the western wall is overgrown by a stand of red mangroves
( Rhizophora mangle) . The walls are mostly vertical and disappear into a mud and detritus bottom at an average depth of 3 m. These limestone walls are partly covered by green 6
FLORIDA
I 50km,
1.6 km
Figure 1. Inset map of southern Florida showing the location of Crawl Key. Enlarged map of the Crawl Key area of Monroe
County, Florida, indicating the location of the quarry (X) where field work was conducted. 7
algae (e.g., Caulerpa spp., Halimeda spp., Acetabularia calyculus), boring sponges (Cliona spp.), and the polychaete
(Sabella melanostigma).
Collection and maintenance of study animals
I collected specimens of ~· annulata and ~· pallida from the Crawl Key quarry for laboratory experiments. I either
pried animals off the substrate by gently peeling back the
pedal disc with a flat knife, or alternately, I removed the
attached anemones on pieces of the substrate. Each animal was placed in its own 3.8-1 capacity "Ziploc" bag with ::::: 2-1 sea water, and transported to the laboratory. I conducted
laboratory experiments from 1 October 1990 to 31 May 1991 at
Florida Atlantic University, Boca Raton, Florida. I maintained the anemones in six closed system 38-1 aquaria with circulating sea water at a constant 24 ° C, a salinity of
0 , 29 I 00 and a light regime of 12 h L: 12 h D. I kept each species in separate holding tanks, into which I introduced adult brine shrimp (Artemia salina) as food, weekly. 8
Laboratory experiments on aggressive interactions
I investigated the possibility of aggressive interactions within and between species, by placing pairs of individuals in close contact. I selected anemones at random from the holding tanks and weighed them to the nearest 0.01 g. When I tested conspecific pairs, one of the anemones was identified by the vital stain Neutral Red (Fisher Scientific Corp.) (Anstensrud,
1989). Forty-eight hours prior to a trial, I placed individuals, to be stained in a 1-1 glass bowl containing a
0. 02 g/1 solution of Neutral Red for 24 h. I placed five pairs of anemones into separate 100 ml beakers in a 76-1 aquarium for each trial. Initially, I fitted each beaker with a plastic divider to prevent the two anemones from touching.
After the anemones attached themselves to the beaker (usually in z 3 min) I removed the divider to begin the trial.
The sea anemones were observed twice daily for the duration of the trial, which ended when one of the anemones left the beaker or 5 d had elapsed. I recorded the following data for each anemone: (1) position of the pedal disc in the beaker, (2) whether the column and tentacles were expanded or contracted, and (3) whether or not individuals were touching.
I considered the winner of an encounter to be the anemone that remained in the beaker if one left, or that consistently 9 retained its position in the beaker, or that consistently had expanded tentacles. If I could not declare a winner, the trial was considered a draw. Each anemone was used in only one trial.
I used Chi square (X 2 ) analysis (Sokal & Rohlf, 1981) to test for differences among distributions in the outcomes for all trials combined . These results were used to rank the species by the degree of aggression.
Laboratory experiments on spatial dispersion
To determine spatial dispersion of _!!. annulata and A. pallida, I randomly placed a variable number of individuals ranging from 17-44 anemones of each species in either a 5, 10 or 38-1 aquarium. After 1-to-3 wk the distance to nearest neighbor (Clark & Evans, 1954) was recorded. The observed mean nearest-neighbor distance for each trial was compared to the Donnelly (1978) modified expected mean nearest-neighbor distance (for a randomly distributed population) using the
Clark & Evans (1954) index. Dispersion patterns were then categorized as either random, aggregated or regular. The significance test was based on the difference between the observed and expected means (Krebs, 1989). 10
Field observations of spatial dispersion
I quantified patterns of vertical zonation and abundance
for B. annulata and A. pall ida along a randomly selected
transect on the southern wall of the Crawl Key quarry (Fig.
1). I recorded the number of individuals of each species at
seven different depths (depth from high tide mark) by using a
0.5 m2 quadrat (made of 1.9 em PVC pipe). I chose this
quadrat size which was large enough to enclose an aggregation,
yet small enough to exclude a second aggregation. Each sample
unit was located along the transect by using two random
numbers and a randomly selected depth. The first random
number dictated the side of the transect I worked on (the
right for an even digit or the left for an odd digit); the
second random number determined the distance measured from the
transect (Wiens, 1969); and the randomly determined depth
specified the actual placement of the quadrat along the wall.
I determined the degree of aggregation by using the
variance-to-mean ratio (s 2 /X) and the standardized Morisita
index of dispersion (Ip) (Krebs, 1989). I then compared the observed distribution of each species to that expected in the random Poisson distribution, and also to that expected in the aggregated negative binomial distribution (Ludwig & Reynolds, 1988). 11
I transformed the abundance data by square root
transformation [~(X+O.S)] to achieve homogeneity of the variances (Soka1 & Rohlf, 1981). I then used transformed data in comparisons of overall abundances and at the seven
different depths between and within species using 1-way ANOVAs
and Tukeys post hoc test (Sokal & Rohlf, 1981). I used
stepwise regression to test the null hypothesis that the slope of the line relating abundance and vertical dispersion for
each species was equal to zero.
Field transplant experiments
To investigate aggression in the field, I removed individuals from their attached substrates and transplanted them so that they initially touched heterospecific non
neighbors. I attached orange plastic flagging tape to the
rocks next to the transplant site with masonry nails to
facilitate subsequent recognition of the transplant site. The
anemones were observed twice daily for two days by SCUBA. I
recorded and analyzed similar data already described for the
laboratory experiments on aggression. The transplanted anemone was scored a winner if it held its position and did not avoid the resident anemones. RESULTS
Laboratory aggressive interactions
Aggressive interactions were evident in 67 of 77 pairings between B. annulata and A. pallida, with ten interactions ending in draws. Bartholomea annulata was the dominant
2 aggressor, winning 48 (62%) of the conflicts (X 2 = 30.8, P < 0.001). An individual's whole wet mass apparently had little effect on the outcome of an aggressive encounter, because when
B. annulata won, it weighed more than A. pallida in 23 of 35 trials (X\ = 2.86, P > 0.05). When A. pallida won, it
2 weighed more than B. annulata in 8 of 17 trials (X 1 = 0.24, p > 0.05).
Conspecifics tended not to engage in aggressive encounters. In 27 pairings of A. pallida, 20 showed no signs
2 < of aggression (X 1 = 5.33, P 0.03). In B. annulata, of 21
2 pairings, 18 showed no signs of aggression (X 1 = 10.71, P < 0.005).
Laboratory dispersion patterns
Dispersion patterns based on nearest-neighbor distance measurements are given in Tables I & II for each species.
12 13
TABLE 1
Nearest-neighbor analysis of dispersion for sympatric B.
annulata and A. pallida in an experimental aquarium.
Replicates 1 2
Species B. annulata A. pallida B. annulata A. pallida
N 33 28 17 17
r a 3.32 3.95 2.78 1. 61 f' * e 4.10 4.39 2.69 2.69 R 0.81 0.39 1. 03 0.60
* s r 0.41 0.49 0.33 0.33 z * l-1.88lns l-5.48la 0. 27°8 3. 32a
Dist R A R A
* ns Donnelly modification (Krebs 1 1989) . accept Ho: The a individuals were randomly distributed. reject (P<0.01) Ho.
1 N number of measurements of distance (em); r a I mean of
series of distance to nearest-neighbor; I r e mean distance to
nearest-neighbor expected in a random distribution; R 1
departure from random expectations (ra /r e ) ; s r 1 standard error
of mean distance in a randomly distributed population; Z 1
standard deviate of normal curve; Dist, distribution type (R, random; A, aggregated) (Clark & Evans, 1954). 14
TABLE II
Nearest-neighbor analysis of dispersion for B. annu1ata and A. pallida in separate experimental aquariums.
Species B. annulata A. pallida
Replicates 1 2 1 2
N 23 24 35 44
r a 3.08 5.51 1.19 1. 84 * :r e 2.27 3.03 1. 70 1.51 R 1. 36 1. 88 1.12 1.22 * s r 0.27 0.38 0.17 0.12 z * 2. 96a 6. 74 a 1. 17ns 2. 80a
Dist R Reg R R
ns * Donnelly modification (Krebs, 1989). accept Ho: The a individuals were randomly distributed. reject (P<0.01) Ho.
N, number of measurements of distance (em); r a ' mean of series of distance to nearest- neighbor; r e , mean distance to nearest-neighbor expected in a random distribution; R, departure from random expectations ( r a /f e ) ; s r , standard error of mean distance in a randomly distributed population; z, standard deviate of normal curve; Dist, distribution type (R, random; Reg, regular) (Clark & Evans, 1954). 15
Here I tested the null hypothesis that in the presence of heterospecifics, individuals do not exhibit an aggregated or clumped pattern. Dispersion of ~- annulata did not depart from a random distribution when in the presence of ~- pallida
(Table I), thereby supporting the null hypothesis. In contrast, ~- pallida exhibited an aggregated dispersion (P <
0.01) when in the presence of B. annulata (Table I).
When I tested the null hypothesis that in the presence of conspecifics, individuals do not exhibit an aggregated pattern
(Table II), no clumped patterns were observed (P < 0.01).
These results suggest that in the presence of B. annulata, individuals of A. pallida aggregate.
Spatial distribution of anemones in the field
The vertical distributions for ~- annulata and ~- pallida along the southern wall of the quarry are summarized in Tables III - v. The degree of aggregation for the two species is indicated by the variance-to-mean ratio (s 2 /~) and the standardized Morisita index of dispersion (Ip). Since the s 2 /x substantially exceeded 1, and Ip differed significantly
(P < 0.05) from a random distribution for each species, I Table III
Analysis of vertical distributions for ~· annulata and ~· pallida from transect
samples at the Crawl Key quarry.
Species ~ (anemones s 2 /x Ip Poisson Negative binomial
/0.05 m2 ) (n-2) X2 (n-3) X2 K
B. annulata 6.47 8.42a 0.506a 34 7 . 99+E5b 33 35.18 0.6532
A. pallida 22.6 3 44.20a 0.512a 98 1.55+E11b 97 797.14c 0.1452
C'> a ind icates a significant (P<0.05) deviation from random. b indicates a significant (P<0.001) deviation from the Ho: The Poisson distribution
was an adequate descriptJon of the clumped pattern in these data. c indicates a significant (P<0.001) deviation from the Ho: The negative binomial
distribution was an adequate description of the clumped pattern in these data. s 2 /x, variance-to-mean ratio ; Ip, standardized Morisita index of dispersion; K, is an exponent used to describe a negative binomial. Table IV
Analysis of vertical distributions for ~· annulata at each of seven
depths from transect samples at the Crawl Key quarry.
Quadrat depth (m) 0 0.25 0.50 0.75 1.0 1. 25 1.5
No. quadrats 16 17 14 16 15 12 10 x 1. 88 4.77 7.86 9.56 8.87 7.25 5 .00
SE of x 0.60 1. 72 2.75 1. 59 2.04 2.09 2.14 ...... • • • -....J s 2 /x 3.05 . 10.61 . 13.47 4.22 7.04 7.25 . 9.16 • • • . • . • Ip 0.522 0.556 0.554 0.508 0.520 0.530 0.574 .
significant deviation from random (P Analysis of vertical distributions for ~- pallida at each of seven depths from transect samples at the Crawl Key quarry. Quadrat depth (m) 0 0.25 0.50 0.75 1.0 1.25 1.5 No. quadrats 16 17 14 16 15 12 10 X 63.94 47.12 29.50 9.31 5.93 4.50 0 CXl SE of x 6.46 14.08 12.31 5.09 4.48 2.59 . • • . • • s 2 /x 10 . 44 71.48 71.94 44.45 50.34 17.92 . • . . • Ip 0.504 0.544 0.585 0.645 0.778 0.653 . significant deviation from random (P<0.05). 2 ~' average number of anemones/m ; SE of x, standard error of the mean; s 2 /x, variance-to-mean ratio; Ip, standardized Morisitas index of dispersion. 19 Table VI One way ANOVA for the difference in abundance between B. annulata and A. pall ida at the Crawl Key quarry. Source df ss MS F ratio Prob>F Between species 1 91.71 91.71 12.59 0.001 Within species 198 1442.42 7.29 Total 199 1534.13 20 Table VII One-way Anova for differences in~· annulata's abundance at different depths at the Crawl Key quarry. Source df ss MS F ratio Prob>F Between depths 6 24.68 4.11 2.47 0.05 Within depths 93 155.21 1. 67 Total 99 179.89 Table VIII One-way ANOVA for differences in~· pallida's abundance at different depths at the Crawl Key quarry. Source df ss MS F ratio Prob>F Between depths 6 593.95 98.99 13.77 0.001 Within depths 93 668.59 7.19 Total 99 1262.53 21 Table IX Comparisons of paired abundance means for B. annulata at different depths using the post hoc Tukey test. Depth Comparison (m) q q0.05 [ 60, 7 ) Conclusion 0.75 - 0 4.550 4.314 reject Hoa 0.75 - 0.25 3.299 4.314 accept Hob 0.75 - 1.50 2.497 4.314 accept Ho 0.75 - 0.50 1.585 4.314 accept Ho 0.75 - 1.25 1.433 4.314 accept Ho 0.75 - 1.00 0.548 4.314 accept Ho 1. 00 - 0 3.928 4.314 accept Ho 1. 00 - 0.25 2.688 4.314 accept Ho 1. 00 - 1.50 1. 984 4.314 accept Ho 1. 00 - 0.50 1. 036 4.314 accept Ho 1. 00 - 1.25 0.904 4.314 accept Ho 1.25 - 0 2.779 4.314 accept Ho 1.25 - 0.25 1.597 4.314 accept Ho 1. 25 - 1.50 1. 073 4.314 accept Ho 1.25 - 0.50 0.083 4.314 accept Ho 22 Table IX contd. 0.50 - 0 2.810 4.314 accept Ho 0.50 - 0.25 1.577 4.314 accept Ho 0.50 - 1. 50 1. 031 4.314 accept Ho 1. 50 - 0 1.493 4.314 accept Ho 1.50 - 0.25 0.357 4.314 accept Ho 0.25 - 0 1. 320 4.314 accept Ho a reject the null hypothesis that the paired means are equal. b accept the null hypothesis that the means are equal. 23 Table X Comparisons of paired abundance means for ~· pallida at different depths using the post hoc Tukey test. Depth Comparison (m) q q0.05[60,7] Conclusion 0 - 1.50 9.381 4.314 reject Hoa 0 - 1.25 8.700 4.314 reject Ho 0 - 1. 00 9.201 4.314 reject Ho 0 - 0.75 8.741 4.314 reject Ho 0 - 0.50 5.087 4.314 reject Ho 0 - 0.25 3.604 4.314 accept Ho b 0.25 - 1.50 6.339 4.314 reject Ho 0.25 - 1.25 5.484 4.314 reject Ho 0.25 - 1. 00 5.791 4.314 reject Ho 0.25 - 0.75 5.270 4.314 reject Ho 0.25 - 0.50 1. 681 4.314 accept Ho 0.50 - 1.50 4.637 4.314 reject Ho 0.50 - 1.25 3.713 4.314 accept Ho 0.50 - 1. 00 3.889 4.314 accept Ho 0.50 - 0.75 3.358 4.314 accept Ho 24 Table X contd. 0.75 - 1.50 1. 714 4.314 accept Ho 0.75 - 1.25 0.607 4.314 accept Ho 0.75 - 1. 00 0.602 4.314 accept Ho 1. 00 - 1.50 1.163 4.314 accept Ho 1. 00 - 1.25 0.041 4.314 accept Ho 1.25 - 1.50 1. 072 4.314 accept Ho a reject the null hypothesis that the paired means are equal. b accept the null hypothesis that the means are equal. 25 concluded that B. annulata and A. pallida were clumping (Tables III - V). The sample distributions for ~· annulata and ~· pallida did not fit a random Poisson distribution (Table III). However, when the data for the two species were fitted to the negative binomial distribution (Table III), that of B. annulata was adequately described (i.e., as predicted by the null hypothesis of a clumped negative binomial distribution), but A. pallida's was not. A 1- way ANOVA considering all depths, revealed a significant difference (P < 0.001) between the abundances of B. annulata and~- pallida (Table VI). Aiptasia pallida was more abundant, with an average of 22.63 anemones/0.5 m2 , while ~. annulata had 6. 4 7 anemones/0. 5 m2 • One-way ANOVAs for each species also indicated significant differences in abundances at the different depths (Tables VII & VIII). Tukeys test suggested that the abundances of B. annulata were significantly different between the surface ( 0 m) and the other six depths (Table IX). It also revealed a significant difference for ~- pallida between the 1. 5 m depth and the other six depths (Table X). Overall, ~- annulata had a maximum abundance at 0.75 m with 9.56 anemones/0.5 m2 , and a minimum abundance at 0 m with 26 1.88 anemones/0.5 m2 (Table IV). Likewise, Table V reveals a maximum abundance for A. pallida at 0 m with 63.94 2 anemones/0.5 m , and a minimum at 1.5 m with 0 anemones/0.5 Linear regression relating the slope of abundance versus depth for each species, suggests significant linear relationships (Fig. 2). The abundance of A. pallida decreased with depth as shown in the scatter plot (y = 56.167 - 45.241 x; R2 = 0.30; P < 0.001 [Fig. 2a]). Abundance of B. annulata versus log transformed depth values (to improve the linearity of the relationship) increased with depth and yielded the equation: y = 6.19 + 8.798 x; R2 = 0.055; P 0< 0.03 (Fig. 2b). Aggressive interactions in the field All of 22 transplants initially resulted in aggressive interactions between the two species. After this initial aggression, all conflicts were reduced or avoided by one of the combatants moving away or contracting its tentacles. There was a significant deviation from the null hypothesis, that individuals of the two species do not avoid contact with 2 each other (X 1 = 20.05, P < 0.001). In 14 of the 22 trials, B. annulata was the transplanted anemone, and in 11 of those it moved out of tentacular contact with A. pallida. In the 27 (a) 195 y=56.167 -45.241x 2 R =0.304 156 -'0 c * -w 117 * * u :z -"0 c * * - 21 * * * wu * z * * Figure 2. Scatter plots and regressions of the abundances of the anemones as a function of depth (a) A. pallida and ). (b) _!!. annulata (Depth log10 28 other three trials, ~· annulata attached themselves to the substrate, and their ~· pallida neighbors leaned away from contact. Eight of the trials had A. pallida as the transplant either as an individual or group. In all eight trials, A. pallida either moved out of tentacular contact with B. annulata, or contracted their tentacles for the duration of the trials. DISCUSSION Aggression In this study B. annulata was more aggressive than A. pallida in both laboratory and field experiments. Heterospecific aggression was initiated through tentacular contacts, which usually caused ~· pallida to withdraw its tentacles or move away from ~· annulata. The dominant B. annulata remained attached during these encounters. Similar findings were reported with other species by Brace et al. (1979) and Dorsett & Turner (1986). Brace et al. (1979) found that there was a dominance hierarchy among the different color morphs in the anemone Actinia eguina. The least aggressive morph responded as Aiptasia pallida did in this study, by withdrawing or retreating. In the animal kingdom, large size usually confers an advantage to individuals during aggressive conflicts with smaller con- or heterospecifics for access to resources such as space, food, or mates (Wittenberger, 1981; Alcock, 1984; McFarland, 1985). However, I detected no significant size advantage during heterospecific aggressive interactions. Smaller anemones won almost as many encounters 29 30 as their larger opponents. Moreover, I found no other studies that evaluated the relationship of size to the outcomes of heterospecific conflicts in anemones. However, my results, although obtained for heterospecific pairs, are similar to Ayre's (1982), who found no advantage to size in conspecific conflicts in the anemone Actinia tenebrosa. These findings differ from Brace's & Pavey's (1978) who reported a large size advantage for Actinia equina. I observed no significant aggression among conspecifics. The phenomenon of reduced aggression among conspecifics was reported for other anemones (Ayre, 1982; Bigger, 1976; Brace & Pavey, 1978; Chao, 1975; Francis, 1973a,b; Sebens, 1984) and other anthozoans (Chadwick, 1987; Lang, 1973). For example, Francis (1973a,b) found that in clonal aggregations of the sea anemone Anthopleura elegantissima aggression was only toward non-clonemates. Colonies of ~· elegantissima apparently use aggression when competing for space with other conspecific clumps (Francis, 197 3b). Likewise, Sebens ( 1984) reported that conspecific non-neighbors were aggressive toward each other, while neighbors in close contact were not, in the sexually reproducing Anthopleura xanthogrammica. Sebens (1984) concluded that these data support the hypothesis that nearest neighbor interactions are more important for 31 communication than aggression, because non-neighbors, when forced to interact, reduced or extinguished their aggressive behavior. However, Sebens' (1984) data are not inconsistent with hypotheses of kin recognition (Trivers, 1985). Aggression and dispersion patterns In this study, laboratory dispersion patterns can be related to aggression between and among ~· pall ida and B. annulata. When only conspecifics were tested, they did not aggregate, but maintained random or regular patterns of dispersion (Table II). However, in the presence of heterospecifics, the less aggressive A. pallida tended to aggregate (Table I). Thus, clumping by~· pallida may be a response to the presence of other more aggressive anemone species. Field transplant experiments also suggested that when individuals of both species were forced to interact, they chose to reduce spatial conflicts by one of the anemones relocating, or bending away from the other. The anemone that relocated was usually the transplanted individual. Yet, in a few trials, transplanted ~· annulata attached themselves to the substrate, but the ~· pallida in tentacular contact with them maintained their positions. These individuals probably 32 could not relocate because there was no available space nearby, so they were forced to bend away from the transplanted ~· annulata to minimize physical damage. It's apparent that resident anemones, who were firmly attached to the substrate, had the advantage over transplanted intruders, as exhibited by the anemone Actinia tenebrosa, where 80% of the residents maintained their positions (Ottaway, 1978). Chadwick (1987) reported that when heterospecific contacts were induced between actiniarians and the corallimorpharian Corynactis californica, the actiniarians responded by bending away, relocating or attacking. However, the corallimorpharians eventually killed any actiniarians that remained in contact. She concluded that f. californica may use heterospecific aggression in competition for space. Similarly, Lang (1973) found that heterospecific aggression was important in competition for space among several scleractinian corals at Discovery Bay, Jamaica. Her laboratory experiments demonstrated an "aggressive pecking order" among the species. Moreover, these results correlated with field observations, since the more aggressive corals used extruded mesenterial filaments to prevent heterospecifics from occupying space in their immediate vicinity. Heterospecific aggression also affects spatial dispersion in other marine invertebrates such as barnacles (Connell, 1961). 33 The spatial distribution of many marine species can usually be assigned to one of three dispersion patterns: random, regular, or aggregated (Langton et al., 1990). The spatial patterns exhibited by ~· annulata and ~· pallida are best described as aggregated, as indicated by the variance-to mean ratio and the standardized Morisita index of dispersion (Tables III- V). Lewis (1970) and Langton et al. (1990) made similar conclusions after applying these indices to the distributions of corals and sea pens (Pennatula aculeata) respectively. In my study, ~· annulata's dispersion was best described by the aggregated negative binomial distribution (Table III). Aiptasia pallida's dispersion was closer to the aggregated distribution than the random Poisson distribution (Table III). Aggression and vertical zonation The 1-way ANOVA revealed a difference in the abundance of each species (Table VI), with~· pallida being most abundant (Table III). There were also significant differences in the abundances of each species at different depths. However, because Tukeys test is very conservative, it only identified the largest differences in abundances with depth (Tables IX & 34 X) . Furthermore, B. annulata was least abundant at the surface and most abundant at 0. 7 5 m (Table IV), while A. pallida's abundance was greatest at the surface and decreased as depth increased (Table V). Linear regression (Fig. 2) indicated inverse relationships between the vertical distributions of these species. Chadwick (1987) reported similar relationships for Corynactis californica and a coral, Astrangia lajollaensis. Additionally, Chao (1975) described vertical zonation among sea anemones where dispersion limits of Anthopleura elegantissima were restricted by heterospecific aggressive interactions with Metridium senile and c. californica. He also concluded that the upper limits of M. senile's and c. californica's distributions were controlled by abiotic factors such as light, desiccation and wave action. Aiptasia pallida, which aggregated in the presence of ~· annulata in laboratory tests (Table I), and is smaller than B. annulata, may be better able to occupy and maintain space at surface depths. Francis (1979) discussed the advantages and disadvantages of large and small body sizes in anemones. She concluded that smaller individuals may be better able to live near the surface where wave forces are greater then at lower depths. At the surface, larger indi victuals (e.g., Bartholomea 35 annulata) may be unable to endure the increased hydrodynamic forces, and may not be able to support their own weight during low tides. Aiptasia pallida was found at the surface in aggregations as large as 195 anemones/0. 05 m2 • The advantages to small individuals living in aggregations were specified by Francis (1973a) as follows: (1) contacts among anemones decrease their effective surface areas, thereby minimizing the area exposed to hydrodynamic forces; ( 2) large numbers of individuals covering an area of rock reduces the ability of other organisms from settling and competing for space; and (3) a group of small anemones has a better chance of catching and holding on to prey than single individuals. Under laboratory conditions A. pallida prefers to attach near the surface (pers. obs.). This behavior as well as its smaller size and clumping behavior may give A. pallida an advantage in exploiting and maintaining space at the surface when in the presence of the larger ~· annulata. Bartholomea annulata was the more aggressive of the two species. Sebens ( 1976) reported that the more aggressive anemones were found on the more stable areas of Panamanian reefs. At the Crawl Key quarry the most stable area of the ledge appeared to be at mid-depth. At the surface hydrodynamic forces are probably greater due to wave action 36 and tidal changes, and a greater risk of desiccation. At the bottom, smothering effects of siltation are probably greater (pers. obs). It was at mid-depth (0.75 m) that B. annulata was the most abundant. Although aggressive behavior was observed in the field under induced situations, it may be only one of a number of factors which could also influence the spatial dispersion of these anemones in the quarry. These factors include biotic ones such as reproductive rates and mode, immigration and emigration rates, and growth and predation rates; or abiotic factors such as wave action, siltation and light penetration, as already documented for corals (Jackson, 1991). The effect of aggression on dispersion might be better understood if transplant experiments were conducted at different depths and observed for longer periods, and abiotic factors quantified and correlated with vertical anemone abundances. LITERATURE CITED Alcock, J., 1984. Animal behavior an evolutionary approach. Sinauer Associates, Inc., Sunderland, Mass. 596 pp. Amos, W.H. & S.H. Amos, 1988. Atlantic and Gulf Coasts. Alfred A. Knopf, Inc. N.Y. 670 pp. Anstensrud, M., 1989. A vital stain for behaviour and ecology of the parasitic copepod Lernaeocera branchialis (Pennellidae). Mar. Ecol. Prog. Ser. 53: 47-50. Ayre, D.J., 1982. Inter-genotype aggression in the solitary sea anemone Actinia tenebrosa. Mar. Biol. 68: 199-205. Bigger, C.H., 1976. The acrorhagial response in Anthopleura krebsi: intraspecific and interspecific recognition. Pp. 127-136. In Coelenterate ecology and behavior. Ed. by G.O. Mackie, Plenum Press, N.Y. Brace, R.C. & J. Pavey, 1978. Size dependent dominance hierarchy in the anemone Actinia equina. Nature, Lond. 273: 752-753. Brace, R.C., J. Pavey, & D.L.J. Quicke, 1979. Intraspecific aggression in the colour morphs of the anemone Actinia equina: the 'convention' governing dominance ranking. Anim. Behav. 27: 553-561. Bradbury, R.H. & P.C. Young, 1983. Coral interactions and community structure: an analysis of spatial pattern. Mar. Ecol. Prog. Ser. 11: 265-271. Brown, L. & J.F. Downhower, 1988. Analyses in behavioral ecology: ~manual for lab and field. Sinauer Associates, Inc. Sunderland, MA. 194 pp. Brown, R.B., E.L. Stone & v.w. Carlisle, 1990. Climate. Pp. 11-34 in Ecosystems of Florida, Myers, R.L. & J.J. Ewel, eds. University OfCentral Florida Press, Orlando. 37 38 Carlgren, 0., 1951. Actiniaria from North America. Arkiv For Zoologi 3(30): 373-390. Cary, L.R., 1911. A study of pedal laceration in Actinians. Biol. Bull. 20: 81-108. Chadwick, N.E., 1987. Interspecific aggressive behavior of the Corallimorpharian Corynactis californica (Cnidaria: Anthozoa): effects on sympatric corals and sea anemones. Biol. Bull. 173: 110-125. Chadwick, N.E., 1991. Spatial distribution and the effects of competition on some temperate Scleractinia and Corallimorpharia. Mar. Ecol. Prog. Ser. 70: 39-48. Chao, c., 1975. Inter-specific aggression between three sympatric sea anemones; Anthopleura elegantissma, Metridium senile, and Corynactis californica at the Monterey Wharf. Unpublished MS. on file at Hopkins Marine Station Library. Chen, E. & J.F. Gerber, 1990. Soils. Pp. 35-69 in Ecosystems of Florida, Myers, R.L. & J.J. Ewe!, eds. University of Central Florida Press, Orlando. Chia, F.S., 1976. Sea anemone reproduction: patterns and adaptive radiations. Pp. 261-270 in Coelenterata ecology and behavior, G.O. Mackie, ed. Plenum Press. N.Y. Clark, P.J. & F.C. Evans, 1954. Distance to nearest neighbor as a measure of spatial relationships in populations. Ecology 35: 445-453. Connell, J.H., 1961. The influence of interspecific competition and other factors on the distribution of the barnacle Chthamalus stellatus. Ecology 42(4): 710-723. Cope, M., 1981. Interspecific coral interactions in Hong Kong. Proc. 4th. Int. Coral Reef Symp. 2: 357-361. Donnelly, K., 1978. Simulations to determine the variance and edge-effect of total nearest neighbor distance. Pp. 91-95 in Simulation Methods in Archaeology, I. Hodder ed. Cambridge University Press, London. 39 Dorsett, D.A. & R. Turner, 1986. Colour-morph dominance and avoidance responses of Anemonia sulcata. Mar. Behav. Physiol. 12: 115-123. Francis, L., 1973a. Clone specific segregation in the sea anemone Anthopleura elegantissima. Biol. Bull. 144: 64- 72. Francis, L., 1973b. Intraspecific aggression and its effects on the distribution of Anthopleura elegantissima and some related sea anemones. Biol. Bull. 144: 73-92. Francis, L., 1976. Social organization within clones of the sea anemone Anthopleura elegantissima. Biol. Bull. 150: 361-376. Francis, L., 1979. Contrast between solitary and colonial lifestyles in the sea anemone Anthopleura elegantissima. Amer. Zool. 19: 669-681. Francis, L., 1988. Cloning and aggression among sea anemones (Coelenterata: Actiniaria) of the rocky shore. Biol. Bull. 174: 241-253. Jackson, J.B.C., 1991. Adaptation and diversity of reef corals. BioScience 41: 475-482. Jennison, B.L., 1981. Reproduction in three species of sea anemones from Key West, Florida. Can. J. Zool. 59: 1708- 1718. Kaplan, E.H., 1988. A Field Guide to Southeastern and Caribbean Seashores. Houghton Mifflin Company, Boston. 423 pp. Krebs, C.J., 1989. Ecological Methodology. Harper and Row, Publishers, N.Y. 654 pp. Lang, J.C., 1973. Interspecific aggression by scleractinian corals. 2. Why the race is not only to the swift. Bull. Mar. Sci. 23: 260-279. Langton, R.W., Langton, E.W., Theroux, R.B. & J.R. Uzmann, 1990. Distribution, behavior and abundance of the sea pens, Pennatula aculeata, in the Gulf of Maine. Mar. Biol. 107: 463-469. 40 Lewis, J.B., 1970. Spatial distribution and pattern of some Atlantic reef corals. Nature 227: 1158-1159. Lincoln, R., G.A. Boxshall & P.F. Clark, 1982. A dictionary of ecology, evolution and systematics. Cambridge University Press, Cambridge. 298 pp. Logan, A., 1984. Interspecific aggression in hermatypic corals from Bermuda. Coral Reefs 3: 131-138. Ludwig, J.A. & J.F. Reynolds. 1988. Statistical Ecology: A Primer on methods and Computing. Wiley, N.Y. McFarland, D., 1985. Animal behavior. The Benjamin/Cummings Publishing Company, Inc. Menlo Park, Cal. 576 pp. McMurrich, J.P., 1889. The Actiniaria of the Bahama Islands, W.I. J. Morph. 3: 42-82. Odum, W.E. & c.c. Mcivor, 1990. Mangroves. Pp. 517-548, in Ecosystems of Florida, Myers, R.L. & J.J. Ewe!, eds. University of Central Florida Press, Orlando. Ottaway, J.R., 1978. Population ecology of the intertidal anemone Actinia tenebrosa. I. Pedal locomotion and intraspecific aggression. Aust. J. Mar. Freshwat. Res. 24: 103-126. Purcell, J.E. & C.L. Kitting, 1982. Intraspecific aggression and population distributions of the sea anemone Metridium senile. Biol. Bull. 162: 345-359. Quicke, D.L.J. & R.C. Brace, 1983 . Phenotypic and genotypic spacing within an aggregation of the anemone Actinia equina. J. Mar. Biol. Ass. U.K. 63: 493-515. Sebens, K.P., 1976. The ecology of caribbean sea anemones in Panama: Utilization of space on a coral reef. Pp. 67-77 in Coelenterata ecology and behavior, G.O. Mackie, ed. Plenum Press. New York. Sebens, K.P., 1984. Agonistic behavior in the intertidal sea anemone Anthopleura xanthogrammica. Biol. Bull. 166: 457-472. 41 Sheppard, C.R.C., 1979. Interspecific aggression between reef corals with reference to their distribution. Mar. Ecol. Prog. Ser. 1: 237-247. Sokal, R.R. & F.J. Rohlf, 1981. Biometry. W.H. Freeman and Co., San Francisco. 776 pp. Trivers, R., 1985. Social evolution. The Benjamin/Cummings Publishing Company, Inc. Menlo Park, Cal. 462 pp. Wiens, J .A. 1969. An approach to the study of ecological relationships among grassland birds. Ornthological Monographs No. 8. The American Ornithologists' Union. 93 pp. Wittenberger, J.F., 1981. Animal social behavior. Wadsworth, Inc., Belmont, Cal. 722 pp.