Contributions to the Biology of the Leopard , semifasciata

(Girard) in , Monterey , .

Lester Timothy Ackerman ~ B. S., University of California, Davis Campus, 1967

THESIS

Submitted in partial satisfaction of the requirements for the degree of

MASTER OF ARTS

in

Biological Sciences

at

SACRAMENTO STATE COLLEGE Moss Landing Marine Laboratory ILLUSTRATIONS

Figure 1--The (Triakis semifasciata).

Figure 2--Elkhorn Slough, California, showing that portion in which leopard occur.

Figure 3--Length frequency distribution, in 2 centimeter incre­ ments, of 694 male and female Triakis captured in Elk­ horn Slough during the month of June 1951 through 1970.

Figure 4--Length frequency distribution, in two centimeter incre­ ments, of all Triakis under 88 centimeters captured in June, lower axis; and October, November and December, upper axis.

Figure 5--Mean weights compared to mean lengths at 10 centimeter length intervals for male and female Triakis.

Figure 6--Range and mean ( ) variations in fecundity with length of 67 Triakis from Elkhorn Slough, California, in 1969 and 1970. Sample sizes in parentheses, refer to numbers of sharks in each length group. Open triangles repre­ sent the mean in each group for all sharks with one or more in each ovisac.

Figure 7--Range and mean (~) variations in fecundity with weight of 64 Triakis from Elkhorn Slough, California, in 1969 and 1970. Sample sizes in parentheses, refer to numbers of sharks in each weight group. Open triangles repre­ sent the mean in each group for all sharks with one or more embryos in each ovisac.

Figure 8--Variations in food habits with length of Triakis in Elk­ horn Slough, as percent frequency of occurrence for major stomach contents, in adjoining 10 centimeter total-length group averages.

Figure 9--Variations in food habits with length of Triakis in Elk­ horn Slough, as percent of food items ingested for major stomach contents, in adjoining 10 centimeter total-length group averages. TABLES

Table 1--Yearly growth increments of four age classes of Triakis in Elkhorn Slough.

Table 2--Maturity of 206 female Triakis from Elkhorn Slough.

Table 3--Maturity of 171 female Triakis from Elkhorn Slough.

Table 4--Summary of sources contributing to prenatal mortality and reduced potential natality b'f Triakis from Elkhorn Slough, 1969 and 1970.

Table 5--Relative positions of 60 unfertilized eggs in the ovi­ sacs of female Triakis from Elkhorn Slough, California 1969 and 1970.

Table 6--Distribution of m~lformed embryos, barren ovisacs, and unfertilized eggs by sizes of parent.

Table ?--Variations in size with increasing numbers of embryos in the ovisacs of female Triakis captured in Elkhorn Slough during November. Embryos were numbered consecutively beginning with the most anterior in the ovisac termed position one, etc ..

Table 8--Variations in the relative abundance of male and female Triakis over 99.9 centimeters in total length captured in Elkhorn Slough in 1969 and 1970.

Table 9--Taxonomic 1 ist of all food organisms identified from the stomachs of 254 Triakis collected in Elkhorn Slough, Cal­ ifornia between June 1968 and January 1971.

Table 10--Variations in food habits with length of Triakis in Elk­ horn Slough, as percent frequency of occurrence for major stomach contents, in 10 centimeter total-length groups.

Table 11--Variations in food habits with length of Triakis in Elk­ horn Slough, as percent of food items ingested for major stomach contents, in 10 centimeter total-length groups. TABLES (Continued)

Table 12--Numerical importance and frequency of occurrence of in the diet of Triakis in Elkhorn Slough, less than 70 cen­ timeters in total lengt'h.

Table 13--Numerical importance and frequency of occurrence of fish in the diet of Triakis in Elkhorn Slough, over 100 centi­ meters in total length.

Table 14--Seasonal variations in food habits of Triakis over 110 centimeters total length in Elkhorn Slough, as percent frequency of occurrence for major groups of stomach con­ tents.

Table 15--Seasonal variation in food habits of Triakis over 110 cen­ timeters total length in Elkhorn Slough, as percent of food items ingested for major groups of stomach contents. ABSTRACT

Growth, reproduction, and food habits of leopard sharks Triakis semifasciata (Girard), were investigated in Elkhorn Slough, Monterey

Bay, California, between June 1969 and January 1971. The research disclosed that most females were mature by the time they reached 120 centimeters in total length and 20 pounds in weight. Males appeared to mature at a somewhat smaller size. The young were born in late spring or very early fall with mating occurring soon afterward. Fec­ undity increa~ed with size of the parent (observed range 7 to 36 em­ bryos). Unfertilized eggs, malformed embryos, and barren ovisacs were occasionally found in females with healthy embryos; the occur­ rence of malformed embryos and unfertilized eggs being lower in lar­ ger parents, the occurrence of barren ovisacs being independent of size of parent.

Triakis were found to be entirely carnivorous feeders, obtain­ ing food from or near the bottom. Composition of the diet varied considerably with size but not significantly with season. Young

Triakis were heavily dependent on the shore Hemigrapsus oreg­ onensis. Principal foods of the larger sharks also included clams

(Tresus nuttalli), other crabs (Cancer spp.), innkeeper worms, (Ure­ chis caupo), and many species of fish. i i

I wish to express my appreciation to the faculty at Sacramento

State College; Dr. Robert L. Livezey, Dr. Emmett C. Thompson, and my major professor, Dr. Martin R. Brittan, without whose support and co­ operation this research would not have been possible. Dr. Edgar L.

Yarberry, Hartnell College, originally suggested the project and con­ tributed valuable suggestions throughout the study. Dr. Jack T. Tom­ linson, Moss Landing Marine Laboratory, provided personal encourage­ ment and advice in my work. Dr. Earl S. Herald, Steinhart Aquarium, was kind enough to allow use of length frequency data gathered from

1951 through 1959. All of these men are gratefully acknowledged for their assistance. Finally, I would 1 ike to thank my loving wife

Janey, without whose encouragement and assistance this work could never have been completed. CONTENTS

Page

Abstract ...

Introduction

Age and Growth 4

Methods of Study. 4

Age .. 6

Growth. 8

Weight-Length Relations ll

Rep rod uct ion. . . 13

Methods of Study. 13

Introduction ... 15

Maturity and Fecundity. 16

Prenatal Mortality and Reduced Potential Natality 20

Embryonic Growth .... 26

Variations in Embryonic Size. 28

Breeding Behavior ... 30

Elkhorn Slough- A Nursery. 33 Food Habits 34

Methods of Analysis 34 Results and Discussion. 34 References. 52 INTRODUCTION

The leopard shark (Triakis semifasciata), a member of the requiem shark family (Carcharhinidae), ranges from Magdalena Bay,

Baja California, to (Roedel and Ripley, 1950). It is com­ mon inshore around jettys, piers and bays in central and southern

California (Miller, et al, 1965). In spite of their general timid­ ity (Limbaugh, 1963), there is one recorded attack upon a skin diver

(DeWitt, 1955).

The unique color pattern of distinct black saddles interspaced with black spots renders the leopard shark (figure 1) easily recog­ nizable (Schott, 1964). The snout appears rather blunt when seen from above, and the teeth are sharply pointed with smaller second­ ary cusps on one or both sides of the main cusp. Triakis reach a maximum length of about 1.5 meters (5.0 ft.) for males and about

1.8 meters (5.9 ft.) for females (Kato, Springer, and Wagner, 1967).

Figure 1--The leopard shark (Triakis semifasciata). 2

Information on the ecology and life history of this species is rather scarce. Herald, et al, (1951, 1952, 1953, 1960, 1968), provided information on comparative distribution and relative abun­ dance, and offered a few notes on food habits and reproduction. Lim­ baugh (1963), noted that Triakis was a nomadic, schooling shark usual­ ly accompanied by the gray smoothhound (Mustelus californicus). This study considers the age and growth, reproduction, and food habits of the leopard shark in Elkhorn Slough.

Elkhorn Slough is located on the east side of ,

California, about halfway between Santa Cruz and Monterey. Origin­ ally it was part of the Salinas river system and served as its out- let until about 1908. Since that time the Slough has received little fresh water and its salinity normally remains close to that of Monte­ rey Bay. However, during periods of heavy rainfall (November-December) the Slough receives runoff from adjacent areas and the salinity may de­ crease significantly (recorded low of 27.95 ppt.) Temperature, in the principal areas of the Slough, is usually within one to two degrees of that in the Bay. The Slough, shown in figure 2, has a maximum depth of about 4.5 meters. It is characterized by extensive mud flats, mod­ erate to fairly strong tidal currents, and soft mud bottom. There is extensive growth of pickleweed (Sal icornia spp.) above the mean high level. The only major ecological study of Elkhorn Slough is that of MacGinitie (1935). His extensive work provides a complete phyletic catalog with natural history notes covering all plants and found in the Slough at that time. SCALE 2000 Ft.

I

(ij a:: w 1-z 0 :E

Methods of Study

Although the skeletal system of embryonic leopard sharks is entirely cartilaginous, increased amounts of calcium are deposited on cartilaginous elements of older individuals. Attempts were made to discover growth rings in these calcium deposits on vertebrae and lower jaw (Meckel's cartilage). The methods used were those describ­ ed by Hildebrand (1968), Clothier (1950), and others, for sectioning and staining bone and cartilage. These calcium deposits were found to be of no value in distinguishing age or growth. Length frequency analysis was therefore employed.

Several shark derbies are sponsored in Elkhorn Slough each year, usually in June, by the Salinas Ike Walton Club and the Pajaro Valley

Rod and Gun Club. During this study, data was collected at one derby in 1969 and at two derbies in 1970. This was combined with length frequency data gathered by students and faculty of Moss Landing Marine

Laboratory during one shark derby in 1966 and one in 1968. Dr. Earl

S. Herald was kind enough to give permission to use length frequency data on 458 leopard sharks taken during June shark derbies from 1951 to 1959. Length measurements of 20 age 0 fish, taken in a seine in

June 1970, were also utilized. This resulted in a length frequency distribution of 694 male and female sharks taken from Elkhorn Slough during the month of June. 5

Employed at various times during this study were nylon and monofilament gill nets, ranging in stretch mesh from one to eight

inches; a fyke net of 3/4 inch stretch mesh; long 1 ines consisting of up to 120 hooks in sizes from 2/0 to 6/0 baited with squid or various fish; and a beach seine of one inch stretch mesh. It was

thus possible to collect specimens representative of all sizes and age classes in the population. All length and weight measurements were made in the field or at the facilities of Moss Landing Marine

Laboratory, from freshly killed specimens. 6

Age Length frequencies for all fish taken in June are presented in

figure 3. Because the young are born in the spring (see Reproduction),

the fish comprising the first group and mode were age 0. Successive modes were age class I, age class I I, etc .. This method of aging appeared satisfactory for the first, and probably second year of life.

ft was however, marginally adequate for the third and fourth years of

life and did not reliably separate the older age groups because of in­ creased overlap in length distribution. This overlap was due to in­ creased dispersion of individuals within each age class and also to the decreased interval between modes. From the data in figure 3, it appears that fish were 9-10 years of age when they reached 120 centi­ meters in total length, and they may (at least the females) live 13-

16 years . w u :z w a: a: ::::> u u 0 lL 0 >- Age 0 Age Age I I Age I I I Age IV u :z w ::::> cl w a: 10 lL

5

TOTAL LENGTH IN CENTIMETERS

Figure 3--Length frequency distribution, in 2 centimeter increments, of 694 male and female Triakis captured in Elkhorn Slough during the month of June l I through 1970. 8

Growth Figure 4 shows length frequency distributions for male and fe- male sharks under 88 centimeters in total length. All fish taken in

June are on the lower axis, and fish captured in October, November, and December are on the upper axis. The data presented in this fig­ ure indicated that 62.54 percent of all growth for age 0 fish, and

58.44 percent of all growth for age I fish, occurred between June and

October-November-December. Yearly growth increments for the deter­ mined age groups are presented in table 1. These data show that re­ lative growth (percentage yearly gain in length) was continually de­ creasing which is characteristic of fish with indeterminate growth patterns (Rounsefell and Everhart, 1953). 5

10

25 Age w u 15 z IV w 0:: 20 0:: ::::> u u 0

lJ... 15 0

>- u z w 10 ::::> d w 0:: lJ... 5

20-21 30-31 TOTAL LENGTH IN CENTIMETERS

Figure 4--Lenoth frequency distribution, in two centimeter increments, of under 88 centimeters captured in June, lovJer axis; and October, December, upper axis. Table !--Yearly growth increments of four age classes of Triakis in Elkhorn Slough.

Age Class

0 II Ill IV

Total Mean June Length (em.) 22. 13 48.84 64.25 74.34 83.52

Mean Increase in Total Length 26.71 15.82 10.09 9. 18

Relative Growth Rate 127.70 31.56 15. 71 12.38 ll

Weight-Length Relations

In figure 5 the relation of weight to length is illustrated on a linear scale for each sex. The general exponential relation n of weight to length W = cL was assumed. Regression lines fitted by least squares to the logarithms of lengths and weights had the following equations:

Log W = 2.9806 Log L-5.01 (males) and 10 10 Log W = 3.1044 Log L-5.24 (females) 10 10 where W = body weight in pounds and L = total length in centimeters.

Correlation coefficients (r) of data in these equations are 0.99429 and 0.99378, respectively.

Males and females had about the same weight to length relat- ion for the first 110 centimeters, after which the weights of females increased more rapidly than that of males (figure 5). This increased weight gain by the females coincided with the onset of maturity (see

Reproduction) and probably was the result of increased metabolism at that time. The weight increase was largely due to development of eggs and embryos, and should not be considered as in increase in growth.

The largest Triakis captured in Elkhorn Slough was a female

151.5 centimeters in total length with a weight of 35.88 pounds. The largest male was 140.0 centimeters in length with a weight of 24.50 pounds. 30 28 0 26 Male • (/) 24 Female 0 0 Cl • z ::::> 22 • 0 CL 20 z 0 18 f- :c • (.!) 16 w 3 14 0 12 • 10 • 8 0 6 o• 4 2 eo tO

TOTAL LENGTH IN CENTIMETERS

Figure 5--Mean weights compared to mean lengths at 10 centimeter length inter­ vals for male and female Triakis. 13

REPRODUCTION

In elasmobranchs the male gonads are separate, except for the ducts which unite and exit through the urogenital opening. In fe­ males, except in exceptional cases, there are always two ovaries

(Parker and Haswell, 1963). The oviducts (Mullerian ducts) are se­ parate from the ovaries and often fuse anteriorly so that a single ostium tubae connects with the coelom. A very narrow, but distensible oviduct leads from the ostium on each side. At one point there is a thickening of the oviduct due to the presence in its wall of the fol­ licles of the shell (nidamentary) gland. Beyond the shell gland the oviduct enlarges on each side to form a (ovisac) which opens into the cloaca.

The ova are very large, consisting of a mass of -spherules held together by a network of protoplasmic threads. The ripe ovum ruptures the walls of the enclosing follicle and so passes into the abdominal cavity to enter one of the oviducts. Impregnation takes place in the oviduct.

Methods of Study

Data on reproduction were gathered by examination of reproduct­ ive tracts of Triakis obtained throughout the study. Maturity of male reproductive organs was extremely difficult to determine. Attempts to establish an index, based on a relation of clasper length and width to body weight, were not successful. Gonads were inspected 14

for the presence of milt, but its absence was not proof of immatur­

ity of the individual. Milt was viewed under laboratory microscopes

on various occasions throughout the study, but viable sperm was never

observed· ovaries were hardened in the ten percent formalin and preserved

in forty percent isopropyl alcohol for later examination. Since there

was significant variation in sizes of normal embryos within a given

ovisac, individual weight and length measurements were taken to de­

scribe development. Before weighing, embryos were separated from

their yolk sac and blotted on paper towels to absorb excess moisture.

All embryo weights used in analysis were from fresh specimens. Weights

of individual embryos in a given ovisac tended to vary more than in­

dividual lengths, and measurements of total length were considered

to be the better indicator of embryo development. Length measure­

ments were made on fresh specimens whenever possible, but it was occasionally necessary to preserve embryos in ten percent formalin for

up to ten days. The term 11 embryo 11 is used in this paper in reference

to the young in all stages prior to birth. 15

I nt roduct ion In male Triakis the milt passes into dorsal (or inner) medial grooves in the claspers after leaving the urogenitial opening. The middle portion of the groove actually serves as a closed tube, since the edges overlap in the manner of a scroll. Clasper lengths were found to increase isometrically with body size. Claspers were easily seen even on pre-term embryos. This sirrplifi·ed sex determination of leopard sharks of all sizes.

The female leopard sharks are ovoviviparous and retain their young until they emerge as minature replicas of the adult. Females ap- peared to have only one ovary, but two ovaries may have fused together to give the singular appearance (Weichert, 1965). The spherical, bright yellow ova attained a maximum observed diameter of 26 mm. before leav- ing the ovary(s). The small heart-shaped nidamentary gland deposited a thin, tough, translucent, amber colored shell around each individual egg as it passed from the oviduct into the ovisac. At that time the eggs had elongated to an average length of 40 mm., and were about 25 mm. in central diameter. The embryos remained attached to their nutrient yolk by an umbilical cord inside the nidamentary shell until birth. By that time all yolk and the umbilical cord had been absorbed. The ovi- sac wall was spongy and laced by a network of capillaries. Some nutri­ ents may have passed from the ovisac through the nidamentary shell to aid ·rn d evelopment of the embryo. 16

Maturity and Fecundity Because of the relative scarcity of large male leopard sharks

in Elkhorn Slough (table 8- Breeding), and inability to establish a criterion of maturity rsee Methods), no positive correlation of

size and first maturity could be established for male Triakis. Pre-

liminary impressions, based on the presence of milt in the gonads, were that males reached maturity at a smaller size than did the fe- males.

Females were considered mature only if they had embryos or eggs

1n at least one ovisac. The smallest mature female was 118 centimet- ers in total length and weighed 16 pounds. The percentages of females that were mature in each size group are presented in tables 2 and 3.

These data indicate that these female Triakis in Elkhorn Slough norm- ally became mature at about 120 centimeters and 18 pound~ and nine out of ten were mature when they reached 21 pounds.

Fecundity was positively correlated with length and weight of fe- males (figures 6 and 7). Females tended to abort some of their embryos under stress of capture, and those known to have aborted one or more em- bryos were not used in determining fecundity or embryo relationships. It is, however, probable that many of the low fecundity ranges in figures

6 and 7 resulted from using data from females that had aborted several

' unknown to the author. The most fecund individual was 144 centi- meters in total length, weighed 34.19 pounds, and contained 36 embryos.

Of 1314 em b ryos examined,· 50.08 percent were female. Table 2--Maturity of 206 female Triakis from Elkhorn Slough.

tength in Number of females Number of females Percent Centimeters examined mature mature

19 to 114.9 106 0 0

115 to 119.9 10 10.0

120 to 129.9 16 15 93.8

130 to 151.5 74 70 94.6

Table 3--Maturity of 171 female Triakis from Elkhorn Slough.

Weight in Number of females Number of females Percent pounds examined mature mature

0. 1 to 14.9 76 0 0

15.0 to 17.9 7 14.3

18.0 to 20.9 10 8 80.0

21.0 to 23.9 34 30 88.2

24.0 to 35.85 44 44 100.0 38 36 34 32 VJ ~ CJ CJ 30 UJ Cl 28 UJ N 26 _I 24 a::f- UJ l.L. 22 z :::J 20 VJ :::J _I 18 CL

(f) 16 0 >- a:: 14 co :::;:: UJ 12

l.L. 0 10 a:: UJ co :::;:: :::J z

(9) (6) (4) ( 1)

0\ 0\ 0\ 0\ 0\ 0\ 0\ 0\ 0\ Lr\ 00 ..::t r--. 0 ("/\ N \.D 0\ N ("/\ ("/\ ("/\ ..::t ..::t ..::t ..::t I I I I I I ("/\ I I \.D 0\ N Lr\ N 00 ..::t r--. N N ("/\ ("/\ ("/\ ..::t ..::t ..::t

TOTAL LENGTH IN CENTIMETERS Figure 6--Range and mean ( ) variations in fecundity with length of 67 Triakis from Elkhorn Slough, California, in 1969 and 1970. Sample sizes in parentheses, refer to numbers of sharks in each length group. Open triangles represent the mean in each group for all sharks with one or more embryos in each ovisac. 38 36 34

(.() CJ CJ 32 w 30 Cl w N 28 ....J 26 ~ a:f- w 24 LL. z ::J 22

- 16 a: co ::::: 14 w LL. 12 0

(.() 10 a: w co 8 ::::: ::J z 6 4 2 (4) (7) (25) ( l l ) (10) (3) ( 1) (3)

CJ\ CJ\. CJ\ CJ\ CJ\ CJ\ CJ\ CJ\ 0 N ..:t \..0 co 0 N ..:t N N N N N ("/"\ ("/"\ ("/"\ I I I I I I I I CJ\ ("/"\ L[\ r-- CJ\ ("/"\ N N N N N ("/"\ ("/"\

WE I GHT IN POUNDS

Figure ?--Range and mean ( ) variations in fecundity with weight of 64 Triakis from Elkhorn Slough, California, in 1969 and 1970. Sample sizes in parentheses, refer to numbers of sharks in each weight group. Open triangles represent the mean in each group for all sharks with one or more embryos in each ovisac. to prenatal mortality and iakis from Elkhorn Slough,

OVISAC Total Left Right

Embryos: Number of ovisacs examined 68 68 136

Total number embryos 664 680 1344

Number dead or malformed embryos 5 15 20

Percent malformed .75 2.2 I .48

Percent ovisacs affected 6.25 3. 13 4.68

Eggs: Number of embryos plus unfertilized eggs 692 722 1414

Number unfertilized eggs 28 42 70

Percent unfertilized eggs 4.04 5.82 4.93

Percent ovisacs affected 32.35 30.88 3 1 . 61 Percent females affected 51 .45

Ovisacs: Number ovisacs barren 6 7

Percent ovisacs barren 8.82 1 .47 5.88 20

Prenatal Mortality and Reduced Potential Natality

Three sources were found that contributed to a real natality

lower t han the Potent .tal natality·. embryo deaths and probable deaths resuiting from malformations, unfertilized eggs, and barren ovisacs

in mature females. These data are summarized in table 4.

Eggs which did not visibly contain embryos were commonly

found in ovisacs of mature females. Examination, under dissecting microscopes, of 16 fresh egg specimens indicated that these eggs did

not have embryos. They probably passed through the shell gland be- fore impregnation. It appeared that eggs not fertilized were notre- sorbed in the ovisac. The unfertilized eggs ranged in weight from

14.0 to 37.5 grams with a mean weight of 23.9 grams and a median weight of 24.0 grams. Lengths varied from 29 mm., to 47 mm., with a median length of 39 mm., and a mean of 36 mm .. Of the females with

rtilized eggs, 48.88 percent had two or more.

The position in the ovisac of 60 of these unfertilized eggs was recorded. Because the number of embryos and unfertilized eggs

each ovisac ranged from 4 to 18 (mean 10.5), the ovisac position

ies for ttnferti lized eggs, presented in table 5, were unnatur­

skewed toward whichever end of the ovisac was used as a reference

int. However, since the minimum number of eggs and embryos in an

isac was four, tllere were f our positions present in every ovisac:

first and second anterior (closest to the nidamentary gland), and

last and next to last posterior (nearest the cloaca). Of these, Table 5--Relative positions of 60 unfertilized eggs in the ovisacs of female Triakis from Elkhorn Slough, California 1969 and 1970.

Anterior Reference Point Posterior Reference Point anterior anterior

8 first

5 second

6

5

3 3

5 5 8 6

r: -' 2

2 4

5 6

3 6

5

5

next to last 6

2 1ast 11

posterior paste r i or 2) an unu Su ally large percentage of the unfertilized eggs, 18.37 percent, in the position most posterior in the ovisac. This may indicate that these eggs were exposed to sperm for relatively shorter periods of time than were the eggs that followed. They may have passed through the oviduct before arrival of sperm.

It was common to find unfertilized eggs in adjoining (38.33 percent) or almost adjoining positions in one ovisac. It was also common to find unfertilized eggs in the same, or almost the same pos­ itions in both left and right ovisacs of the same female. This may in­ dicate that these 11 group i ngs'' of unfertilized eggs were released from the ovary(s) at about the same time.

Of 1344 embryos examined during the study, 20, or 1.48 percent, were malformed or dead. Only one ovisac contained more than two malform­ ed individuals. That ovisac was very dry, the eggs shriveled and hard, and all 14 embryos (70 percent of all malformed or dead embryos) were

The remaining six embryos appeared so severely malformed that

almost certainly would not have been born alive. Two of these did

have eyes, and three were severely stunted (less than half the mean

th of the normal embryos in that ovisac). The last embryo considered

be malformed was an albino, completely lacking coloration even in the

It was also several centimeters shorter than the mean length of

r embryos in that ovisac.

occurrence of malformed embryos and unfertilized eggs appeared

r in the larger parent females (table 6). i rmed embryos, barren ovisacs, and unfertilized eggs by sizes of parent.

Weight in Pounds 19-22.9 23-24.9 25-26.9 27-28.9 29-35.9

Number of females examined 12 25 1 1 10 8

Embryos, total 169 486 249 215 204

Number malformed 3 16 0 0 Females affected 3 2 0 0

Percent malformed .59 .62 6.43 0.00 0.00 Percent females affected 8.33 12.00 18. 18 0.00 0.00

Unfertilized eggs, total 13 21 18 8 7 Females affected 7 14 7 4 Percent unfertilized 7. 14 4. 37 6.74 3.58 3.34

Percent females affected 58.33 53.84 63.63 40.00 12.50 Ovisacs, total 24 50 22 20 16

Number barren 2 0 2

Percent barren .67 2.00 0.00 10.00 6.25 25

of the 68 mature female leopard sharks examined, 7 or nearly

6 percent, had one barren ovisac (table 4). This affected actual natality by lowering the theoretical total mean fecundity from 21.92 to an actual total mean fecundity of 20.80. Occurrence of barren ovi­ sacs appeared unrelated to size of the females (table 6).

Since almost five percent of the eggs produced and released into the oviducts were not fertilized (table 4), (or for other reasons

ailed to produce embryos), actual natality was further reduced from

20.80 to a total mean number of 19.76. A final reduction to a total mean number of embryos for all females of 19.47 was due to embryo malformation and death. 26

Embryonic Growth In 1970, the earliest presence of eggs in the ovisacs, but not visible embryos, was noted during the June shark derbies. They were also found by the author during the June 1969 shark derbies.

Herald (1960), reporting on 17 earlier derbies usually held in June, stated that none of the adult females contained near term embryos.

Examination, under a dissecting microscope, showed that some of the eggs from the two females sampled from the 1970 derbies, contained embryos under 2 mm. in tot a 1 1ength.

Growth of the embryos was nonexponential; by October the embryos had achieved roughly 75 percent of their estimated final length, with a mean total length of 15.4 centimeters. The mean total length incr·eased to 15.9 em. in November and was 16.8 em. in

December. The nutrient source was almost depleted by mid February

\'ias only 3 to 5 mm. in length. The umbilical cord had also been

and the small yolk was almost touching the embryos.

On February 17, both intact ovisacs from a 24 pound, 132 centimeter, femalewere placed into a running sea-water aquarium at

Landing Marine Laboratory. By one P.M. the following day, ten

ing embryos, one unfertilized egg, and one dead embryo had emerged.

embryo was still in the ovisac. These small Triakis were

7.6 em. in total length. Another female leopard shark placed

outside display tank (about 250 gallons) on this same date, also

irth withi n a f ew d ays to about one dozen young. The small sharks 27

uarium were active immediately, but did not begin feeding for in t:he aq several days. At that time they eagerly accepted bits of fish, chicken

beef heart, and assorted minced marine invertebrates. These sharks

,,Jere St ill active on March 1, but unfortunately were transferred to the larger outside display tank, by some trespassing youngsters. They in­ ter-mingled with the other smal 1 Triakis in the display tank and growth could not be followed. The large tank was cleaned in mid-March and the young Triakis released.

Since ten adult females captured in April all contained embryos, it is probable that the earlier (February) births in the tanks at Moss

ing Marine Laboratory resulted from stress, and would not have normally occurred. The April embryos appeared near term, no traces of nutrient yolk were detectable on many of the embryos. The embryos at

is time averaged 19.7 em. in total length.

All leopard sharks captured in May were tagged with surface

oats for behavioral studies, but the four large females tagged May

2 It as if they still held embryos. On the afternoon of May 12,

' l was fortunate enough to observe a school of very young Triakis

to 3 feet of water. The size of these sharks was estimated to

near 20 centimeters. Since the water was rather turbid, the young

rd sharks were visible only when they occasionally came within

4 inches of the surface; no estimate could be made regarding the the schoo 1.

cumulative evidence indicated that, at least in 1970, the

of female sharks in Elkhorn Slough gave birth in late spring,

during the middle or later part of May. Herald's (1960) data cates that this h as probably been the pattern each year. 28

tions in Embryonic Size The size of the embryos in a given ovisac varied relative heir anterior-posterior positions within the ovisac. Table 7

that those embryos most anterior averaged in total length more

six oercent less than the mean total length for all embryos in

iven ovisac. There was greater stunting in the most anterior

total number of embryos in the ovisac increased. This

stunting was a result of crowding. The ovisacs tended

smallest in diameter anteriorly, which resulted in progressively

room and less stunting posteriorly. Although larger females tend­

have more embryos (figures 6 and 7) and increased stunting

orly, their increased overall size, and the corresponding in-

in ovisac width, allowed their embryos to reach a longer mean

length (table 7). n i with increasing numbers of embryos in the ovisacs of Female tured in Elkhorn Slough during November. Embryos were numbered consecutively with the most anterior in the ovisac termed position one, etc.

Number of Embryos 7-8-9-l 0-ll 12-13-14 15-16-1]-18

Median Number Embryos 10 13 15

Mean Embryo Length (em.)

Tota 1 15.32 16.03 16.40 Position #1 14.39 14.66 14.89 Percent stunting -6.06 -8.55 -9.21 Position #2 14.69 15.68 15.44 Percent stunting -4.11 -2. 11 -5.85 Position #3 15.02 15.64 15.57 Percent stunting -1.96 -2.43 -5.05 Position #4 15.38 15.68 16.27 Percent stunting +0.39 -2. 11 -0.80 Position - Last 15.54 16. 10 16.70 Percent stunting +1.43 +0.42 +1.83 30

ing Behavior Data on the breeding behavior of elasmobranchs is very limited

the difficulty of observing such a process under natural condit- lnce s is obvious. One unpublished account relates the mating of two eopard sharks in a display tank at Steinhart Aquarium during the month

February, 1964 (personal communication with Dr. Earl S. Herald).

ting followed about one week of chasing and nipping a 3i foot female 1 s

ns by a 4 foot male (sizes were estimated). The fin nipping contin­

to the point where both the dorsal and caudal fins had bloody open

5 at their bases. Actual mating was preceded by about five min- tes of rapid swimming together with the male holding the female 1 s

pectoral fin in his mouth. During this time the male 1 s left cla-

was turned almost at a right angle over the right clasper, which

ined in position. At first the male swam parallel to the female,

near the end of the five minutes, he twisted his body under hers

estill firmly holding onto her left pectoral. Several brief

on the bottom of the tank were followed by coitus, which apparent­

place while swimming; the male still holding the female 1 s pee­

fin in his mouth, bending his body at the middle and arching it

the female 1 s body. It seems probable that only the left clasper

nserted in the cloaca of the female. They remained in this posit-

bottom, almost motionless for several minutes, before the

off. The left pectoral fin of the female showed no sign of

which might have been inflicted by the male 1 s teeth. 31

Since the field data indicated that many females in Elkhorn

did not give birth unti 1 about May, it is unlikely that mating s l ld normally have occurred there as early as February. However, since some fem ales had fertilized eggs in their ovisacs in early June, mating appo~rently did occur within a relatively short period of time after the les gave birth. This indicates that ovum were released into the

iducts shortly after the females gave birth.

Data on the relative abundance of larger male and female

rks in Elkhorn Slough (table 8) shows an overall ratio of about

females to l male. However, this ratio changed to 8~9 during the

ined months of February through May, approximately a one to one

io. These combined data indicate that the male leopard sharks

tered Elkhorn Slough at that time to mate with the females, and

the hypothesis that mating occurred shortly after the females

birth. By June the ratio of females to males had returned to in le 8--Variations the relative abundance of male and female Triakis over 99.9 centimeters in total length captured in Elkhorn Slough in 1969 and 1970.

Total Females Males t,lon th Captured # % # %

tober 11 9 81.82 2 18.18

r 56 49 89.29 7 10. 7l

r 29 2} 72.41 8 27.59

ruary 4 25.00 3 75;00

r i l 16 10 62.50 6 37.50

14 5 35.71 9 64.29

__]_!_ _J:]_ 71 .06 11 28.94

ls 168 122 72.02 46 27.78 33

rn 1ough - A Nursery E 5 Data on the relative abundance of leopard sharks, under 100

imeters in total length, showed a ration of 99 females to 102

This was a ratio of approximately 1: l. This contrasted

overall ratio of 2.6 females to 1 male for leopards over

. in total length (table 8). These data, when considered

the increased abundance of males during the breeding period,

that Elkhorn Slough has served as an important breeding

ursery area for Triakis off the California Coast. FOOD HABITS

of Ana 1ys is

Food habits data was separated into 10 centimeter total­

groupings, and was also grouped by seasons for leopard sharks liO centimeters in total length. The seasons are defined as

(Harch-May), summer (June-August), fall (September-November), inter (December-February). Analysis was made both as to fre-

occurrence and numerical importance of each food group.

of occurrence for each food group is expressed as percent

stomachs containing some food. Numerical importance is

as a food group percentage of the total food items ingest-

and Discussion

Examinations of 254 stomachs revealed that the fish were

carnivorous. The traces of plant material occasionally were usually attached to mussels or other shell fragments

probably ingested incidentally. Food was derived from

The food organisms found during the study are 1 isted

ically in table 9. All of the invertebrates and the major­

vertebrates are typically benthic or demersal. -Taxonomic 1 ist of al 1 food organisms identified from the stomachs of 254 Triakis collected in Elkhorn Slough, Cal­ ifornia between June 1968 and January 1971.

Annelida Unidentified Polychaeta

Mo 11 usc a lass Lamellibranchia

Order Filibranchia

Family Mytil idae Mytilus edulis

Order Eulamellibranchia Unidentified Eulamell ibranchia

Family Tellinidae Macoma nasuta

M. secta

Family Mactridae Tresus nuttall i

Family Veneridae Saxidomus nuttall i

Family Pholadidae Zirfaea pilsbryi

lopoda

Decapod a Lol igo opalescens

Octopod a Octopus sp. ropoda

ass Crustacea

Malacostraca

lass Eucarida

r Decapoda

r Reptantia Unidentified Reptantia Cancer antennarius

Cancer productus

Hemigrapsus nudus

li.:_ oregonensis

Pachygrapsus crassipes

Pugettia producta

Scleroplax granulata

Emerita analoga

Crago sp.

iurida Urechis caupo

ass

Order

Family Carcharhinidae Triakis semifasciata

Order Rajiformes

Family Rhinobatidae Rhinobatos productus ass Unidentified fish eggs

rder Perciformes

Family Genyonemus lineatus

Family Embiotocidae Cymatogaster aggregata

Embiotoca jacksoni

Family Gobi idae Gillichthys mirabilis

Family Scorpaenidae Sebastodes auriculatus

h paucispinis

Cott i dae Leptocottus armatus Family Atherinidae Atherinops affinis Atherinopsis californiensis r p]euronectiformes

Family Bothidae Citharichthys sordidus Citharichthys stigmaeus

Family Pleuronectidae Platichthys stellatus

Batrachoidiformes

Family Batrachoididae Porichthys notatus 38

frequency of occurrence and numerical importance of

contents for 10 centimeter total-length groups are

in tables 10 and 11, grouped as follows; crabs (true crabs crabs), clam siphons (all bivalves- infrequently including

innkeeper worms (Urechis caupo), fish (Chondricthyes ' chthyes), and fish eggs (Osteichthyes). To facilitate in-

on of trend changes with increasing length, figures 8 and

the frequency of occurrence and numerical importance of

groups in adjoining 10 centimeter group averages.

under stress, the larger sharks often regurgitated food,

onally everted their stomachs. This would lower the fre­

percentages presented in the following tables Total Total Stomachs Food Urechis Clam Fish Len h em. Examined Items Crabs Fish caueo Siphons Eggs 20-29.9 19 20 89.5% 5.3% 5.3% 30-39.9 18 39 100.0 40-49.9 27 47 100.0 50-59.9 18 40 88.9 5.6 5.6 60-69.9 10 49 100.0 10.0 20.0

70-79.9 l3 28 61.5 7.7 38.5 7.7 7.7 80-89.9 24 62 41.7 12.5 29.2 16.7 29.2 90-99.9 5 15 40.0 40.0 60.0 60.0 100-09.9 6 8 33.3 66.7 33.3 110-19.9 17 49 35.3 35.3 35.3 17.6 29.4 120-29.9 27 83 22.2 44.4 37.0 33.3 48.1 130-39.9 57 183 33.3 57.9 24.6 33.3 14.0 140-49.9 13 34 30.7 61.4 23. 1 46.2 To 1 Total Total Stomachs Food Urechis C1am Fish Length Examined Items Crabs Fish caupo Siphons Eggs 20-29.9 19 20 90.0% 5.0% 5.0% 30-39.9 18 39 100.0 40-49.9 27 47 100.0 50-59.9 18 40 95.0 2.5 2.5 60-69.9 10 49 93.9 2.0 4. 1 70-79.9 13 28 53.6 3.6 28.6 7.2 7.2 80-89.9 24 62 51.6 4.8 17.7 12.9 12.9

90-99.9 5 15 26.7 13.3 40.0 20.0 100-09.9 6 8 25.0 50.0 25.0 110-19.9 17 49 24.5 24.5 32.7 8.2 10.2 120-29.9 27 83 10.8 22.9 33.7 16.9 15.7

130-39.9 57 183 14.2 35.0 12.6 33.9 4.4 140-49.9 13 34 11.8 47.1 8.8 32.4 w u z w 0:::: 0:::: 50 ::J u u 0 LL 40 0 >­ u z: w ::J 30 c:J w 0:::: LL 20

10

0 0 0 0 0 0 0 0 0 0 0 0 0 (V'\ ~ LJ'\ \.0 r--.. co 0\ 0 N (V'\ ~ LJ'\ I I I I I I I 0 0 0 0 0 0 0 I I I I I I N (V'\ ~ LJ'\ \.0 r--.. co 0 0 0 0 0 0 0\ 0 N (V'\ ~

TOTAL LENGTH IN CENT I METERS

Figure 8--Variations in food habits with length of Triakis in Elkhorn Slough, as percent frequency of occurrence for major stomach contents, in adjoining 10 centimeter total-length group averages. -.._, 60 u CL ' '\ \ w '\ (,_) so z <( I- 0::: 0 CL 40 :::;:

_J <( (,_) 30

0::: w :::;: :::::> :z: 20

10

0 0 0 0 0 0 0 0 0 0 0 0 0 (V\ ..::t l..J\ \.0 r-- CX) 0\ 0 N (V\ ..::t l..J\ I I I I I I I 0 0 0 0 0 0 0 I I I I I I N (V\ ..::t l..J\ \.0 r-- CX) 0 0 0 0 0 0 0\ 0 N (V\ ..::t TOTAL LENGTH IN CENTIMETERS Figure 9--Variations in food habits with length of Triakis in Elkhorn Slough, as percent of food items ingested for major stomach contents, in adjoining 10 centimeter total­ length group averages. 43

food habits of the smaller sharks differed from those of

fish by the heavy reliance on small crabs, mainly a single

These small shore crabs are abundant

the smaller members of this species provide a

food source eas i 1y captured by young sharks. In 92 sharks

centimeters in total length, crabs had a numerical importance

t and a frequency of occurrence of 95.7 percent (Table 12).

•IS~~~~ was found infrequently in sharks of this size. Other

rarely found in stomach contents.

the fish increased in size, dependence on this single genus

source diminished and was supplemented by larger Cancer spp.,

~~~~s crassipes, and an occasional Pugettia producta. Other

rates, fish, and fish eggs also increased in importance. z--Numerica~ importa~ce. an~ frequency of occurrence of crabs in the d1et of Tr1ak1s 1n Elkhorn Slough, less than 70 centimeters in total length.

Total Total Total Stomachs Total Stomachs Food Containing Crabs Examined Items Crabs Ingested 19 20 17 18 18 39 18 39 27 47 27 47 18 40 16 38 10 47 10 46 92 193 88 188 95.7 97.4 45

arks over 100 centimeters in total length, the most For s ll food group was fish, occurring in 52.50 percent of the

examined and ~omprising 32.20 percent of food items ingested

These figures, especially for frequency of occurrence,

tly high due to the relatively slow digestion of otoliths,

and other bones, and the subsequent

from the stomach into the spiral intestine. This may

the larger crabs whose carapaces had to digest to a

ling the color and consistency of tomato skins before

stomach.

lation of the individual fish identified indicated that

not dependent on a certain few species. These data do

the statement by Herald, et al. (1960), that leopard sharks

idshipman (Porichthys notatus) when available.

instances of cannibal ism were found during the study.

Triakis consummed was a 26.67 centimeter albino re­

and in good condition. --Numerical importance and frequency of occurrence of fish in the diet of Triakis in Elkhorn Slough, over 100 centi- meters in tot a 1 1eng th.

Total Total Total Stomachs Total Stomachs Food Containing Fish Examined Items Fish Ingested

6 8 4 4

17 49 6 12

27 83 12 19

57 183 33 64

_13_ 34 8 16

120 357 63 115

Percent 52.5 32.2 47

tempts to identify the fish eggs eaten by leopard sharks

It was thought that the eggs were from several success f u l · ies of fish. Brief exposure to the stomach acids in

5) made the eggs unviable and the author was unable

The eggs were primarily spherical,

self adhesive. They varied volumetrically in stomach

few eggs to about 118.3 cubic centimeters (t cup).

importance was expressed in terms of egg masses con-

than individual eggs. 48

clam siphons in the leopard sharks' diet were primarily

gaper clam (Tresus nuttalli). These were fairly easily

the two horny valves at the tip--a structure not found

of the common clams. Ricketts and Calvin (1968), report siphons are commonly found in the stomachs of bottom feed­

Other siphons were occasionally identified as those of the clam (Saxidomus nuttalli), and rarely the rough piddock

It was not unusual to find 6 to 8 inches of a

in a shark's stomach. They would apparently grasp the centimeters of siphon visible and pull until the siphon

along its extended(l~ to 3 feet) length. The

pulled free from the mud occasionally for it was

entire gaper body in the stomach of the shark. The

always free of all but small fragments of shell. lt may be

the easily broken shell was crushed between the shark's

body was swallowed. The occurrence of all other bi­

stomachs was rare. 49

The fat innkeeper worm (Urechis caupo) was an important item

in the diet of Triakis in Elkhorn Slough. Our knowledge of the habits

of the fat innkeeper was gained by Fisher and MacGinitie (1928). It

is MacGinitie 1 s (1947) opinion that although 1 iving 11 almost certainly

11 11 11 for twenty-five years or more Urech is never 1eaves its burrow • Inn­

keepers are nevertheless commonly included in the diet of certain elas­ mobranchs. Rays are thought to be able 11 to pop potential prey out of

its burrow by using their broad flattened bodies as a sort of plumber 1 s

friend 11 (Ricketts, Calvin, and Hedgepeth, 1968).

It is not known how leopard sharks capture innkeepers. Aq­

uarium studies of Urechis in artifical plastic burrows were conduct- ed by this author at Moss Landing Marine Laboratory. These studies

indicated that although innkeepers never voluntarily left their bur­

rows completely, they did occasionally allow a few centimeters of their

body to stick out for a brief time. To a leopard shark accustomed to watching for a few centimeters of clam siphon sticking out of the mud,

this would be an open invitation to supplement his diet. 50

The data for seasonal variation in food habits of larger male

lnd female leopard sharks is presented in tables 14 and 15. Several

~rends are indicated but analysis of variance between the seasonal

~roups showed the variations not to be significant. This is a com­

Jined result of the large variation in food items in sharks with each seasonal group and relatively small sample sizes in spring and summer. Table 14--Seasonal variations in food habits of Triakis over l l 0 centimeters total length in Elkhorn Slough, as percent frequency of occurrence for major groups of stomach con- tents. Sample sizes are in parentheses.

Urech is Clam Fish Crabs Fish caueo Siphons Eggs

Spring 9. l 45.5 27.3 9. l 36.6 ( l l )

Summer 15.4 61.5 11.5 34.5 19.2 (26)

Fa 1·1 30.6 53. l 28.6 61.2 12.2 (49)

Winter 40.5 40.5 35.7 35.7 30.9 (42)

Table 15--Seasonal variation in food habits of Triakis over l l 0 centimeters total length in Elkhorn Slough, as percent of food items ingested for major groups of stomach con- tents. Sample sizes are in parentheses.

Urechis Clam Fish Crabs Fish caueo Siphons Eggs

Spring 2.6 28.9 55.3 2.6 10.5 (38)

Summer 9.4 68.8 3. l 3. l 15.6 ( 32)

Fa l l ll. 4 29. l 12.7 4-3.0 3.8 ( 158)

Winter 24. l 22.4 23.3 19.0 11.2 ( 116) 52

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