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The courtship and mating behavior ofthe round stingray, Urolophus halleri
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Authors Nordell, Shawn Elizabeth, 1957-
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The courtship and mating behavior of the round stingray, Urolophm halleri
Nordell, Shawn Elizabeth, M.S.
The University of Arizona, 1990
U M I 300 N. Zeeb Rd. Ann Arbor, MI 48106
THE COURTSHIP AND MATING BEHAVIOR OF THE ROUND STINGRAY,
Urolophus halleri
by
Shawn Elizabeth Nordell
A Thesis Submitted to the Faculty of the
DEPARTMENT OF ECOLOGY AND EVOLUTIONARY BIOLOGY
In Partial Fulfillment of the Requirements For the Degree of
MASTER OF SCIENCE
In the Graduate College
THE UNIVERSITY OF ARIZONA
19 9 0
2
STATEMENT BY AUTHOR
This thesis has been submitted in partial fulfillment of requirements for an advanced degree at The University of Arizona and is deposited in the University Library to be made available to borrowers under rules of the Library.
Brief quotations from this thesis are allowable without special permission, provided that accurate acknowledgement of source is made. Requests for permission for extended quotation from or reproduction of this manuscript in whole or in part may be granted by the head of the major department or the Dean of the Graduate College when in his or her judgement the proposed use of the material is in the interests of scholarship. In all other instances, however, permission must be obtained from the author.
This thesis has been approved on the date shown below:
SIGNED:
APPROVAL BY THESIS DIRECTOR
D. A. Thomson D. A. Thomson Professor of Ecology and
Evolutionary Biology
3
ACKNOWLEDGEMENTS
This work started as an Advanced Population Biology class project which then grew and grew and now has finally been laid to rest. Part of this work was funded by a grant from the University of Arizona Graduate Program Development Fund. I would like to thank the faculty, fellow graduate students and friends that made my trips to Punta La Ona, Sonora, Mexico so very enjoyable as well as a gastronomic delight. In particular, I would like to thank my office mate and fellow basement dweller Meriel Brooks for helping me collect stingrays under less than enjoyable conditions.
This manuscript was greatly improved by the comments of Meriel Brooks, Frank Cipriano, Tom Valone and the members of my committee. I thank each for their advice as well as their invaluable friendship. I am indebted to Shawn McLaughlin for his friendship and artistic talent as well as for allowing me to borrow valuable equipment that enabled me to finish this project.
I would like to thank my committee, Marilyn Houck, Rich Strauss, and Don Thomson, for all their guidance, patience, and friendship while I was at the University of Arizona. Each of them contributed uniquely to my development as a graduate student. I thank Marilyn for her thorough editing skills and valuable advice. I thank Rich for his persistant lesson on hypothesis testing (which I will never forget) and his incredulous patience throughout the years. Rich was also kind enough to provide me with his morphometric software package. I would like to especiallly thank my major advisor, Don Thomson or D.A.T. as he is affectionately known. DAT introduced me to the Sea of Cortez through his incessant love of teaching and the sea. I thank him for all his guidance, patience and friendship and putting up with a die-hard CUBS fan as a graduate student. I especially thank him for my faithful field assistant #nd beloved companion, Buck, son of Max.
TABLE OF CONTENTS
4
page
LIST OF ILLUSTRATIONS 5
LIST OF TABLES 6
ABSTRACT 7
CHAPTER ONE
INTRODUCTION 8
METHODS 10
Field Study 10 Dentition Study 13 Statistical Analysis . 15
RESULTS 16
Field Study 16 Dentition Study 26
DISCUSSION 38
LITERATURE CITED 45
LIST OF ILLUSTRATIONS
5
Figure page
1. Diagram of sexually dimorphic male dentition of Urolophus hal leri 14
2. A flow diagram indicating the prevalent sequence of female courtship behaviors 17
3. A flow diagram indicating the prevalent sequence of male courtship behaviors 18
4. Frequency distribution of male biting distribution.. 20
5. The proportion of time males spend in each courtship behavior 22
6. The proportion of time females spend in each courtship behavior 23
7. Projections of the Principal Component Analysis of specimens of male and female Urolophus hal1leri. . . 28
8. Projections of the Principal Component Analysis of specimens of female Urolophus hal leri 31
9. Projections of the Principal Component Analysis of specimens of male Urolophus hal leri .34
10. Projections of the Principal Component Analysis of sexually dimorphic teeth of mature male Urolophus halleri . .37
6
LIST OF TABLES
Tables page
1. Description of male and female courtship behaviors. 1 2
2. Differences in the duration of male and female Urolophus hal leri courtship behaviors 24
3. Results of Principal Component Analysis of all tooth and size data for all males and females 27
4. Results of Principal Component Analysis of all tooth and size data for females only 30
5. Results of Principal Component Analysis of all tooth and size data for males only 33
6. Results of Principal Component Analysis of sexually dimoprhic teeth of all mature males 36
ABSTRACT
7
Biting has been observed to be an important component
of male mating behavior in several elasmobranch species. I
observed male biting during courtship and mating in a
population of Urolophus halleri. the round stingray, in the
Sea of Cortez. Females allow males to bite the posterior
and medial edge of their pectoral fin during courtship yet
often appear to struggle to dislodge the male after they
have been bitten. During mating the male bites the anterior
edge of the females' pectoral fin and the female is passive.
In response to this biting behavior females have relatively
thicker discs than males and males have sexually dimorphic
dentition. Larger adult males have relatively smaller yet
more sharply curved teeth than smaller males that may allow
them to hold on to females better during courtship.
Therefore there is the potential for assortative mating
based on male dentition and his ability to hold a female.
8
INTRODUCTION
The elasmobranchs (sharks, skates, and rays) are
considered to be one of the oldest groups of jawed
vertebrates, yet there are remarkably few studies of
elasmobranch reproductive behavior. The lack of information
on their reproductive behavior may be due to difficulty in
observing these reclusive individuals in their aquatic
habitat. In fact, most recorded accounts have resulted from
chance observations in nature or from observations of
captive individuals.
Biting has been observed to be an important component
of male mating behavior in several species of elasmobranchs.
Male sharks, for example, have been observed biting the
pectoral fins of females during the reproductive period
(Schmidtlein 1878, Gudger 1912, Dempster and Herald 1961,
Clark 1963, 1975, Taylor 1971, Klimley 1980, Castro et al.
1988). Skates (Libby and Gilbert 1960, Price 1967) and rays
(McCourt and Kerstitch 1980, Tricas 1980, Reed and Gilmore
1981) display a similar behavior. Scars on female sharks
(presumably from tooth cuts) have been noted during the
reproductive period (Suda 1953, Springer 1960, 1967, Stevens
1974, Pratt 1979). Stevens (1974) has identified these
wounds as 'courtship scars' and they have been observed only
on females.
9
Sexually dimorphic dentition has been noted in rays
(McCourt and Kerstitch 1980, Bigelow and Schroeder 1953),
sharks (Springer 1967, Budker 1971) and skates (Feduccio and
Slaughter 1974, McEachran et al.1976, McEachran 1977).
Feduccio and Slaughter (1974) originally hypothesized that
the tooth dimorphism indicated differences in male and
female foraging habits and therefore would be subject to
natural selection. McEachran (1977), however, examined the
stomach contents of over 1600 individuals from four species
of skates and found no significant difference in the diets
of males and females. He also noted that the teeth of both
sexes remain blunt until near sexual maturity at which time
the males develop sharp conical cusps. It is therefore
unlikely that dimorphic dentition in these elasmobranchs is
due to foraging differences.
In this paper I will examine the courtship, mating
behavior and dentition of Urolophus halleri. the round
stingray. This work is divided into two parts. First I
will examine the occurrence and significance of biting
during courtship and mating of free-living rays in the Gulf
of California. Second, I will examine the differences in
morphology of the teeth, shape and size between males and
females. Specifically, I will focus on the significance of
biting which occurs during the reproductive period, and will
1 0
provide evidence that this behavior may be used by females
to assess male quality during courtship.
METHODS
Field Study
Urolophus halleri Cooper is a small stingray with a
disc width of approximately 150mm at sexual maturity.
Females tend to grow larger than males which is
characteristic of elasmobranchs in general (Babel 1967).
The dorsal surface is grey or brown with a variable yellow
mosaic pattern superimposed on it. The ventral surface is
white. The mouth is located on the ventral surface about a
quarter of the way from the anterior end of the disc.
Females are easily identified by a lack of claspers,
the rolled portion of the pelvic fin of the male which
serves as an intromittent organ during mating (Wourms 1977).
Claspers are present on males of all size classes. Females
are ovoviviparous and give birth to two or three large, well
developed young annually (Babel 1967).
U. halleri ranges from Point Conception, in California,
south to Panama in Central America and is found throughout
the Gulf of California (Thomson et al. 1979). I observed
free-living rays at Punta La Ona, Sonora, Mexico, from 12-19
March 1988 and 11-18 March 1989. This site is located
approximately 50 km northwest of Bahia Kino. During the
1 1
breeding season in March a large population of U. halleri
congregate in this shallow, protected bay. The bay is
surrounded by a gently sloping, sandy shoreline. Eelgrass,
Zostera marina, dominates the subtidal substrate.
I observed female and male courtship activity and
mating behavior from the hours of dawn until mid-morning.
Data were recorded from shoreline observations as well as
from surface observations while skin-diving. During this
period, U. halleri courted predominantly in the sandy near
shore area.
From initial observable courtship and mating behaviors,
I selected a subset of quantifiable descriptions of male and
female courtship behaviors (Table 1). Behavior, sequence,
and duration of male and female activity were recorded
during the morning observation periods. I observed males
and females as long as possible in order to attain the
maximum amount of information about each individual. During
this period, I also ran 60 meter transects and counted all
individuals observed in order to collect data on male:female
sex ratios.
1 2
Table 1. Description of male and female courtship behaviors.
Cruise parallel
Cruise Z
Change direction
Beach
Stop
Bury
Follow
Chase
Nip
Bite
Pair circles
Pair circles vi gorously
Pair still
Pair separates
Travel a linear path parallel to the shoreline at an unhurried pace
Travel in a zig-zag pattern parallel to the shoreline at an unhurried pace
Turn around 180°
Move toward shoreline and very shallow water
No movement
Settle on substrate and cover back with sand
Male follows female and both travel at an unhurried pace
Male chases female at an accelerated speed
Contact by the males' dentition with the female that lasts < 5 seconds
Bite by the male that last > 5 seconds
Male bites female and the pair circle slowly over the substrate
Male bites female and female struggles
Male bites female and they are lying still with ventral surfaces down
Male no longer bites female
1 3
Dentition Study
To examine the dentition in male and female U. halleri.
I selected ten males and ten females of varying size classes
from the University of Arizona Fish Collection. All
individuals were collected in the Gulf of California during
different times of the year. For each individual I examined
five teeth from the upper jaw and five teeth from the lower
jaw. All teeth were extracted from the seventh tooth row
(this is the row of teeth which would most likely come in
contact with females disc). Each tooth was labelled as to
jaw position and individual ID number and set in putty on an
insect flag mounted on an insect pin. The boundary of the
base view and side view of each tooth was drawn with a
camera-lucida and points were digitized using a Hi-Pad,
Model DT-714, digitizing table and the digitizing program
Digitize (Version 3.0). The perimeter and area of each
tooth were estimated by using the program Polygon, (Version
1.0). In order to approximate tooth curvature, I measured
the distance from the apex of a tooth to the two base points
on all dimorphic teeth of mature males (Figure 1). The
program Distance (Version 2.0) was used to determine these
digitized distances. Distance and Polygon were provided by
Richard Strauss, University of Arizona.
1 4
Figure 1. Diagram of sexually dimorphic male dentition of Urolophus halleri. A and B are distances used to measure curvature of dimorphic teeth.
1 5
I also measured disc width, total length, disc length,
and mouth width on each specimen as estimates of body size.
Any scarring or external damage to a specimens' disc was
noted. In order to examine differences in peripheral disc
thickness in males and females I measured the depth of the
edge of the pectoral fin at two bilateral anterior positions
(in front of each eye), two bilateral medial positions (at
the widest point of the disc), and two bilateral posterior
positions (adjacent to the pelvic fin).
Statistical Analysis
Field Study - I standardized uneven focal length periods by
transforming the data into proportions. All data were
arcsine- transformed to adjust the variance to be
independent of the mean. The means of the time spent on
each behavior were calculated for active (not buried) males
and females. A Kolmogorov-Smirnov two-sample test was used
to test the null hypothesis that males and females spent the
same amount of time engaged in a specific behavior. A G
(log-1ikelihood) test was used to test for significance in
the sex ratio. A t-test was used to determine
significant differences in the duration of male bites on
solitary females versus females in groups.
Dentition Study - All morphometric data (disc width, disc
length, total length, mouth width, disc thickness, tooth
1 6
perimeter, tooth area, and the two tooth tip to base
measurements for mature males) were log-transformed to make
the variance independent of the mean. The bilateral
measures of disc thickness of either side of the body were
averaged. SAS was used to execute a Principal Component
Analysis using the covariance matrix of log transformed
data. SAS was run on a VAX 8600 (C.C.I.T., University of
Ari zona).
RESULTS
Field Study
I will first describe the sequence of courtship
behaviors for Urolophus halleri. Females and males cruise a
linear path parallel to the shoreline or in a zig-zag
pattern parallel to the shoreline (Figures 2 and 3). Once a
male encounters a female while traveling along this path, he
may follow her leisurely or chase her hurriedly. During the
time that the male Ts in close proximity to the female, he
may attempt to bite the lateral or posterior edge of her
pectoral fin. I define a nip as any contact by a male's
dentition with the female fin that lasted less than five
seconds in duration and a successful bite was one that
lasted longer than five seconds.
(.43) (.41) (.43) Cruise _ Cruise Z *Stop ..Bury parallel
Pair
Bitten by male
circles
Pair still
circles vigorously
Figure 2. A flow diagram indicating the female courtship behaviors. The values behavioral transition, (n = 53).
prevalent sequence of are mean percent per
1 8
(.20) Cruise . parallel
(.42) Cruise Z »,Stop
Pair separates
Pair circles
Pair circles vigorously
Figure 3. A flow diagram indicating the prevalent sequence of male courtship behaviors. The values are mean percent per behavioral transition, (n = 26).
1 9
Chasing a female can lead to nipping, but neither
chasing nor nipping is followed by a successful bite.
Following a female only occasionally leads to a successful
bite (13 % of the time). Most successful bites occur after
the female has stopped or buried (Fig 2). Males are able to
locate buried females and will use their snout to uncover
and bite a females' fin. Very few males are able to
successfully bite a female, most males only nip females
(Figure 4).
If a male is successful in biting the female for longer
than five seconds there are several possible behaviors that
may follow. While the male is biting the female the pair
may circle slowly over the substrate or more vigorously up
in the water column. During vigorous circling, it appears
that the female is attempting to dislodge the male. While
the female is struggling with the male, the male's claspers
would sometimes rotate forward and he would move the ventral
side of his body toward the ventral side of the females
body. This may be an attempt at forced copulation. I did
not observe successful insertion of the males clasper into
the females cloaca while the female circled vigorously.
Therefore this mating tactic may only rarely result in
successful sperm transfer.
0-4 6-49 50-99 100-149150-199 250-300
DURATION OF BITING (SEC)
Figure Frequency distribution of male bite duration^ Bite duration is in seconds. (n = 15 males)
2 1
The slow circling behavior alternates with quiescence
with the pair lying still on the sand, ventral surfaces
down. During this time the male is still biting the female
but without attempting copulation. This alternating
sequence of circling and quiescence can continue for up to
40 minutes and, occasionally, more than one male may be
associated with a single female. Finally, the sexes
separate and depart in different directions with no mating
taking place. Females may subsequently bury in the sand but
I have never observed a male burying following a morning
courtship or mating sequence.
I defined behavioral categories and recorded the
sequence and duration of events to determine how males and
females which are active (not buried) spent their time
during the courtship period. Males continually patrol the
shallow sandy areas for females throughout the morning and
are never observed foraging during this time. Males spend
more than half their time engaged in pair-behavior (biting
females) and very little time in solitary cruising (Fig. 5).
Conversely, females spend less than a quarter of their time
engaged in pair-behavior and more than half their time
cruising alone (Fig. 6). These differences are
statistically different (Table 2). This may indicate that
males and females using different strategies during this
Pair behaviors 58.5
Change direction 1.4
Chase 12.8
Pair separates 3
Cruise parallel 2.6
Cruise Z 9.9
Beach Follow 1.3
7.4
Figure 5. behavior. The proportion of time males spend in each courtship
The values are mean percent time, (n = 26).
Pair separates 1.5
Chase 9.6
Cruise Z 28.9
Change direction 1.8 Stop
7
Cruise parallel 22.6
Follow 2.4
Pair Behaviors 23.2
Figure 6. The proportion of time females spend in each courtship behavior. The values are mean percent time, (n = 53).
24
Table 2. Differences in the duration of male and female Urolophus halleri courtship behaviors. A Kolmogorov-Smirnov two sample test was used to test for significance. A (*) indicates a significant difference (P < .01).
Behavior D (unsigned Significant difference) (*)
Cruise Parallel .48 * Cruise Z .44 * Follow .14 Chase .15 Biting Behaviors .44 # Bite Pair circles Pair circles vigorously Pair still
25
pre-copulatory period. It may also indicate a female bias in
the sex ratio. Data from transects indicate a slight female
bias (1.3F:1M). This bias, however, is not statistically
significant (G = 3.26, d.f.=1, NS).
Females tend to form aggregations when burying. The
mean size of a group is 25 females (n=12, s.d.=11.9). The
females range from being slightly covered with sand to being
completely buried and often the body of one female will
overlap several other females. A group usually encompasses
an area of approximately 1m2. Hales swim over these groups
and nudge and bite buried females. There is no statistical
difference (t = 0.50, d.f = 107, NS) in the duration of
bites by males when females were grouped (x=24.6 sec.,
s.d.=45.1, n=67) versus solitary (x=30.2sec., s.d.=72.4,
n=42). The fact that these females are still in the
courtship and mating area where they could be bitten by
males may suggest that they are sexually receptive and not
previously inseminated.
I observed the sequence of courtship behaviors lead to
copulation sixteen times. After the male bites the female
on the lateral or posterior margin of her pectoral fin he
gradually shifts his position anteriorly. He accomplishes
this by biting and releasing the females' fin a number of
times, each time moving his grasp forward dn the females'
26
disc. As he does so, he swings under the female so that the
two are in a ventral-to- ventral position with the males
dorsal surface facing the sandy substrate. The male then
rotates his claspers forward and inserts the left clasper
into the females cloaca. The area around the females' cloaca
often appeared red. Unlike the vigorous movement during
courtship, the pair lies passively during copulation rocking
gently with the waves or moving only slightly. The male
maintains his grasp on the female at the anterior portion of
the female's pectoral fin, as opposed to courtship when the
male bites the medial or posterior portion of the females'
disc. The mean duration of copulation was approximately
four minutes (x=3.55 min., s.d=1.9 min). Following
copulation, the male would release the female and the pair
would separate, each heading in a different direction.
Dentition Study
A Principal Component Analysis was used to examine the
variation in disc thickness and tooth size and shape. An
initial PCA included all tooth measurements and body size
data for males and females. The loadings indicate that PC I
is a good body size vector, as they are positive and similar
in magnitude (Table 3) PCI accounts for 84.4% of the
variance in the data set. PC II accounts for 7.4% of the
variance and is a bipolar shape component as indicated by
27
Table 3. Results of Principal Component Analysis of all tooth and size data for all males and females. PCI accounts for 84.4%, PCII accounts for 7.4* and PCIII accounts for 3.5X of the variance.
Measure Component
I II III Disc Width .325544 .222884 .178048 Disc Length .323796 .227193 .208143 Total Length .308809 .214179 .212584 Mouth Width .417736 .050157 -.292335 Disc Thickness Anterior .424539 -.309048 -
.705044 Disc Thickness Medial .306879 -.213683 .426019 Disc Thickness Posterior .378388 -.596684 .330725 Tooth Perimeter .227228 .404400 -.056921 Tooth Area .223813 .435403 -.055910
/ INCREASING SIZE —>
PRINCIPAL COMPONENT I (84.4%)
Figure .7. Projections of specimens of male and female Uroloohus halleri. First component (PCI) represents variation in body size. Second component (PCII) represents tooth size and disc thickness differences between sexes. Percentages indicate percent total variance accounted for by the components.
Females are represented by thick lines. Males are represented by
thin lines.
29
the assortment of positive and negative coefficients. The
body dimensions (disc width, disc length, total length,
mouth width) as well as tooth area and perimeter are
positively correlated while the three disc thickness
measurements are negatively correlated. The graph of PC I
and PC II (Figure 7) indicates that for a given size, males
tend to have a relatively larger tooth perimeter and area
than females while at the same time females have relatively
thicker discs than males.
Next, I analyzed all data for males and females
separately to determine how disc thickness and tooth size
varied within males and females. In females, PC I shows
coefficients that are all positive and similar in size and
thus indicate a good proxy for size (Table 4). PC I
accounts for 85.8% of the variance. PC II is a bipolar
component and indicates a large positive loading for
posterior disc thickness and as well as a positive loading
for medial disc thickness. All the body dimensions, tooth
perimeter and area, and anterior disc thickness are
negatively correlated. A graph of PCI vs PCII (Figure 8)
shows that as body size increases there is a relative
decrease in the medial and posterior disc thickness in
juveniles and then these increase in adults. At the same
30
Table 4. Results of Principal Component Analysis of all tooth and size data for females only. PCI accounts for 85.8%, PCII accounts for 8.2% and PCIII accounts for 3.6% of the variance.
Measure Component
I II III Disc Width .410823 -.050919 -.201149 Disc Length .408854 -.060798 -.176564 Total Length .396287 -.022700 -.134917 Mouth Width .352383 -.127532 -.178872 Disc Thickness Anterior .310381 -.167632 -.284939 Disc Thickness Medial .301555 .274425 -.045990 Disc Thickness Posterior .274679 .818584 .347956 Tooth Perimeter .247918 -.297309 .452478 Tooth Area .242202 -.339188 .684873
a? CJ CD
z 111 z o Q. 2 o o
I o z a: a.
A
J M as u t-to o a.
o z
C « < wo «H J < tf <
Cd M 0 t* o Z z M < c s
to os ~ -z u n in
M ts] W bl W X Z Z z w m w w as o o s w M M HUSS
>- ? o o a o w w 0 O 1-1 1-1
m E- a o
1 i i 1 i i V V/ V INCREASING SIZE —>
PRINCIPAL COMPONENT I (85.5%)
Figure 8. Projections of specimens of female Uroloohua halleri. First component (PCI) represents variation in body size. Second component (PCII) represents tooth size and disk thicicness differences among females* -Percentages indicate percent total variance accounted for by. the components.
32
time as body size increases there is a relative decrease in
tooth perimeter and area.
In males, PC I accounts for 87.3% of the variance and
is a general size component (Table 5). PC II accounts for
7.4* of the variance and shows the opposite trend as that
shown previously for females. PC II indicates a negative
correlation for all disk thickness measurements and a
positive correlation for all body dimensions and tooth
perimeter and area. In males, as body size increases there
is a relative increase in tooth perimeter and area and a
relative decrease in disc thickness (Figure 9). This is a
different pattern from that seen in females (see Figure 8).
In order to examine the relationship between tooth size
(as measured by tooth area and perimeter), disc thickness,
and body size I performed a series of bivariate (log x log)
plots (Creighton and Strauss 1986). Disc width and disc
thickness (all three measurements) show a log-linear
relationship in both females and males. However, in females
disc width and tooth area or tooth perimeter both show a non
log-linear relationship. It appears that there is a
developmental constraint in females in which the body
continues to grow but teeth stop growing after a certain
size. In males no such non log-linear relationship occurs.
33
Table 5. Results of Principal Component Analysis of all tooth and size data for males only. PCI accounts for 87.2%, PCII accounts for 7.4%, and PCIII accounts for 2.5% of the vari ance.
Measure Component
I II III Disc Width .261280 .200451 -.325205 Disc Length .272760 .220863 -.384687 Total Length .257429 .196395 -.413442 Mouth Width .469272 .023735 -.239540 Disc Thickness Anterior .494888 -.570614 .142014 Disc Thickness Medial .255913 -.036737 .082615 Disc Thickness Posterior .369592 -.303740 .317153 Tooth Perimeter .240603 .451367 .361502 Tooth Area .234745 .498964 .509589
< Ed at <
a a i z i < to a: zun O H W HUld W 2 55 2 H « Ed es o SUH HO.B Q - H >• H O Q O 03 °OH CP E- o
I I v
INCREASING SIZE —>
PRINCIPAL- COMPONENT I (87.2%)
Figure ? . Projections of specimens of male Urolophus halleri. First component (PCI) represents variation in body size. Second component (PCII) represents tooth size and disc thickness differences among males. Percentages indicate percent total variance accounted for by the components.
35
Finally, I evaluated tooth shape and size for mature
males separately. In mature males only the center teeth are
dimorphic. The teeth on the edge of the jaw are flat,
similar to females dentition. A PCA was performed on the
dimorphic teeth of mature males. I included in this data
analysis the distance from the tip of the tooth to each
base. Distance A (Figure 1) is a measure of tooth
curvature. As distance A decreases the tooth becomes more
curved. PC I is a good size vector and accounts for 64.2%
of the variance (Table 6). PC II is a bipolar component
with large positive loadings for tooth area and distance A.
The three body measurements, disc width, disc length, and
mouth width, are all negative. The graph of PC I and PC II
(Figure 10) shows that smaller males have relatively
straighter and less curved teeth, than larger males. As
males increase in body size there is a relative decrease in
tooth size and a relative increase in tooth curvature.
36
Table 6. Results of Principal Component Analysis of sexually dimorphic teeth of mature males. PCI accounts for 64.2*, PCII accounts for 22.2*, and PCIII accounts for 8.3% of the variance.
Measure Component
I II III Disc Width .371861 -.372295 .130836 Disc Length .475769 -.472548 .167387 Mouth Width .217446 -.274796 .223397 Tooth Perimeter .448702 .217001 -.178066 Tooth Area .310391 .491597 -.272493 Distance A .375080 .520173 .625601 Distance B .386936 -.056970 -.638451
37
4R CVI CM 0J
UJ 2 o CL 2 o o
I o z tr Q_
A I 1
<5 W cs < a z <
W OS 2 W ̂ O H I M til I 01= 2 w < m w OJ 2 W M w M &• O O Q Z Z s < <
> g- e* e-O O W OT O O W M OhQQ l I l l v v
INCREASING SIZE —>
PRINCIPAL COMPONENT I (64.2%)
Figure 10. Projections of sexually dimorphic teeth of mature male Urolophus halleri. First component (PCI) represents variation in body 3ize. Second component (PCII) represents tooth size and shape differences among males. Percentages indicate percent total variance accounted for by the components.
38
DISCUSSION
There are several possible explanations for the role of
biting and the existence of fin scars during the
reproductive period. First, fertilization is internal in
elasmobranchs which requires that the male and female be in
physical contact for intromission to occur. Biting may
facilitate maneuvering or in restraint of the female, by the
male, during copulation (McEachran 1977). I have shown that
male biting does occur during mating in U. halleri and this
has also been documented in its congener U. concentricus
(McCourt and Kerstitch 1980). Biting may serve as a
contact\holding mechanism in several elasmobranch species
(Hornshark: Dempster and Herald 1961, Reef white-tip shark:
Tricas and Le Feuvre 1985, Chain dogfish: Castro et al.
1986 and the clearnose skate: Libby and Gilbert 1960, Luer
and Gilbert 1985). During copulation biting may be
particularly important in larger sharks while in smaller
species, such as the Chain Dogfish, males may wrap their
body around the female during copulation (Castro et al.
1988), which also serves to maintain contact with the
female. Springer (1967) reported that minor cuts and scars,
'courtship injuries', are common in mature females of the
larger carcharhinid sharks while such injuries are generally
not evident on smaller cacharhinids.
39
Biting does appear to serve to maintain contact during
copulation in several elasmobranch species including U.
halleri (this study), however, this does not explain the
incidence of pre-copulatory biting throughout the
reproductive period. Pre-copulatory biting has been noted
in U. halleri (this study) as well as other elasmobranch
species. For example, there have been observations of nurse
shark and horn shark males biting females on the pectoral
fin during pre-copulatory courtship (Taylor 1971, Klimley
1980). Tricas (1980) observed male myliobatid rays chasing
and attempting to bite the posterior edge of the pectoral
fin of females. In addition, there have been several
observations where biting did not occur during copulation in
certain carcharhinid and orectolobid sharks (Clark 1963,
Johnson and Nelson 1978, Klimley 1980). There seems to be a
great deal of variation in the expression of this behavior
and physical manipulation of the female during copulation is
only one possible function of this behavior.
Stevens (1974) proposed an additional explanation for
the function of biting. He hypothesized that biting
functions not to hold females in position during copulation
but rather to serve as a pre-copulatory releasing factor to
mating receptance in females. However, females often appear
to struggle to dislodge the male after he has bitten her
40
(Taylor 1971, Castro et al. 1988 McCourt and Kerstitch 1980,
personal observation). This suggests that biting does not
necessarily elicit female cooperation, and is further
corroborated by the courtship behavior observed in U.
halleri. and the types and amount of damage observed to
females. During courtship the male bites the medial or
posterior portion of the female's pectoral fin. Females
appear to use various strategies to avoid being bitten by a
male during courtship. The female can swim quickly away
from the male as he chases her. Chasing a female, without
the female stopping, never leads to the male successfully
biting the female. Females can also try to avoid a male by
heading toward the shoreline and very shallow water. At
this point the female's back may actually be out of the
water and she will stop and turn to face the approaching
male. Males are sometimes successful (14 % of the time) in
biting the female once she has headed toward the shoreline.
In contrast to this females had a 50% chance of being bitten
by a male while they were buried. Males are capable of
locating buried females and will use their snout to uncover
a portion of the buried female to bite her. Therefore,
burying is not a particularly successful strategy to avoid
being bitten by a male, which may indicate that buried
females are receptive females.
41
Females do seem to be able to avoid being bitten by a male,
and therefore it appears that females are choosing whether
or not to allow themselves to be bitten.
If biting is a necessary pre-copulatory releaser, scars
would be expected on all mature females' discs. Stevens
(1974) examined blue sharks caught off the coast of Great
Britain and found tooth cuts only in size classes of females
that were presumably sexually mature. However, only 16* of
the females in the large size classes were found to have
bite scars, and none were found to have ova present in their
oviducts or uteri to indicate that mating had occurred.
This is in contrast to the blue shark population off the
coast of New England, in which tooth cut wounds are
consistently found on subadult females and pregnant females
generally bear older, healed, scars (Pratt 1979). I have
observed damaged and scarred discs on some female U.
halleri. These wounds vary from the disc edge being ragged
in portions to large half-moon shaped pieces of their disc
being missing. Scarring and abrasions around the edge of
the dorsal surface of females are also sometimes observed.
These wounds are found on the posterior and medial portion
of the females' disc which indicate that they occurred
during courtship and not mating when the male bites the
anterior portion of the females' disc. There are also
42
observations of damage occurring to females during courtship
with no evidence of subsequent copulation in sharks (Suda
1953, Springer 1960, Clark 1963, Stevens 1974), skates
(Price 1967) and rays (Tricas 1980, Reed and Gilmore 1981,
this study). Males, therefore, may not gain any immediate
benefit by biting a female in order to induce her to be
receptive to mating at a later time.
I propose that biting ability may be an indicator of
male quality and therefore could be involved in mate choice
by the female. In U. halleri and all other elasmobranch
species, males only contribute sperm in the reproductive
process. Males are not known to defend a territory or
resource and there is no evidence of mate guarding or
parental care (Wourms 1977). Biting may thus be a means by
which females can assess male quality. My data are
consistent with this hypothesis. Females appear to allow
themselves to be bitten and then dislodge the male without
mating with him. They may be using biting to assess some
aspect of male quality.
Females appear to be well adapted for this behavior.
In response to the biting behavior, the skin of mature
females would be expected to be thicker than males in areas
where males bite them during copulation and courtship. This
would allow females to avoid extensive damage due to male
43
biting. This pattern has been documented in the Blue shark
(Pratt 1979) where Pratt found that the skin over mature
females was almost twice as thick as that for males and he
found very little evidence of infection or necrotic tissue
in bitten females. I have found a similar pattern in U.
halleri. As female body size increases, the medial and
particularly the posterior portion of the disc increase
relatively in thickness. The opposite pattern occurs in
males, where disc thickness relatively decreases as body
size increases. This relative increase in disc thickness
may allow females to minimize the amount of damage that
occurs due to male biting during courtship and mating.
Mature U. halleri males have teeth that are pointed and
curved unlike the flat pavement like teeth of mature females
(McCourt and Kerstitch 1980, personal observation). This
same pattern of sexually dimorphic dentition appears in
several species of skates and sharks and does not appear to
be due to foraging differences between the sexes (McEachran
1977, Compagno 1988). In U. halleri larger males have more
sharply curved teeth than smaller males which may allow the
larger males to grasp females better. Therefore there is
the potential for assortative mating based on male dentition
and his ability to hold a female. Very few U. halleri males
are able to successfully bite a female. Most of the biting
44
observed is of a very short duration. This also suggests
differential mating success among males that may be due to
differences in dentition.
To directly test this hypothesis information on the
reproductive success of known individuals would be required.
The curvature of the sexually dimorphic dentition of these
males could be analyzed to determine whether there is a
direct correlation between male reproductive success and
tooth curvature which would suggest that biting is being
used by females as a means of determining male quality.
45
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