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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Budker, P. 1971. The life of sharks. XVII, 222pp. London: Weidenfeld and Nicolson.

Castro, Jose I., Patricia M. Bubucis, and Neal A. Overstrom. 1988. The reproductive biology of the Chain Dogfish, Scvliorhinus retifer. Copeia 1988:740-746.

Clark, E. 1963. The maintenance of sharks in captivity, with a report on their instrumental conditioning. In-.Sharks and Survival (ed. P. W. Gilbert), chapter 4, 145-6. Boston :D.C. Heath and Co.

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46

Klimley, A. Peter. 1980. Observations of courtship and copulation in the nurse shark, Ginglvmostoma cirratum. Copeia 1980 (4): 878-882.

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Luer, Carl A. and Perry W. Gilbert. 1985. Mating behavior, egg deposition, incubation period, and hatching in the clearnose skate, Ra.ia eglanteria. Env. Biol. Fishes 13(3):161-171 .

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Price, Kent S. Jr., 1967. Copulatory behavior in the clearnose skate, Ra.ia eglanteria. in lower Chesapeake Bay. Copeia 1967:854-855.

Reed, John C. and R. Grant Gilmore. 1981. Inshore occurrence and nuptial behavior of the roughtai 1 stingray, Dasvatis centroura (Dasyatidae), on the continental shelf, east central Florida. Northeast Gulf Science. 5(1):59-62.

Schmidtlein, R. 1878. Beobachtungen uber die Lebenweise einger Seethiere innerhalb der Aquarien der zoologischen Station. Mitt. Zool. Stn. Neapel 7:1-27.

Springer, Stewart.1960. Natural history of the sandbar shark, Eylamia miIberti. Fishery Bull. Fish. Wildl. Ser. U.S. 61:1-38.

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Stevens, 1974. The occurrence and significance of tooth cuts on the blue shark (Prionace glauca L.) from British waters J. Mar. Biol. Assoc. U.K. 54:373-378.

Suda, A. 1953. Ecological study on the Blue shark (Prionace glauca Linne). South Sea Area Fish. Res. Lab. Rep. 26:1-11.

Taylor, L.R., Jr., 1971. Shark sex. Fish Life 2:17-24.

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Tricas, Timothy C. 1980. Courtship and mating-related behaviors in Myliobatid rays. Copeia 1980:553-556.

Tricas, T. C., and E. M. Le Feuvre. 1985. Mating in the reef white-tip shark Triaendon obesus. Mar. Biol. 84:233-237.

Wourms, John P. 1977. Reproduction in Chondrichthyan Fishes. Amer. Zool. 17:379-410