Contributions to the Biology of the Leopard Shark, Triakis semifasciata
(Girard) in Elkhorn Slough, Monterey Bay, California.
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 leopard shark (Triakis semifasciata).
Figure 2--Elkhorn Slough, California, showing that portion in which leopard sharks 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 embryos 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 embryo 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 crabs 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 crab 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 Oregon (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 Monterey Bay,
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 tide 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 animals 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 uterus (ovisac) which opens into the cloaca. The ova are very large, consisting of a mass of yolk-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 (.() 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 Chondrichthyes Order Squaliformes Family Carcharhinidae Triakis semifasciata Order Rajiformes Family Rhinobatidae Rhinobatos productus ass Osteichthyes Unidentified fish eggs rder Perciformes Family Sciaenidae 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 REFERENCES Clothier, Charles R. 1950. A Key to some southern california fishes based on vertebral characters. California Division of Fish and Game, Bureau of Marine Fisheries, Fish Bulletin No. 79, 83 pp. DeW i t t, John W. 1955. A record of an attack by a leopard shark (Triakis semi fasciata Girard). California Fish and Game, val. 41, no. l, page 348. Fisher, W. K. and G. E. MacGinitie. 1928. A new echiuroid worm from California. Annual magazine of Natural History, Ser. 10, val. l, pp. 199-203; also, The natural history of an echiuroid worm. Ibid., pp. 204-213. Hildebrand, Milton. 1968. Anatomical preparations. 100 pp. University of California Press. Herald, Earl S. 1953. The 1952 shark derbies at Elkhorn Slough, Monterey Bay and at Coyote Point, San Francisco Bay, California Fish and Game, val. 39, no. 2, pp. 237-243. Herald, Earl S. and Robert R. Dempster. 1952. The 1951 shark derby at Elkhorn Slough, California. California Fish and Game, val. 38, no.l, pp. 133-134. 53 Herald, EarlS. and William Ellis Ripley. 1951. The relative abundance of sharks and bat stingrays in San Francisco Bay. California Fish and Game, vol. 37, no. 3, pp. 315-329. Herald, Earl S., Walter Schneebel i, Norval Green, and Kenneth Innes. 1960. Catch records for seventeen shark derbies held at Elkhorn Slough, Monterey Bay, California. California Fish and Game, vo 1 . 46, no. 1 , pp. 59-6 7. Kato, Susumu, Stewart Springer, and Mary H. Wagner. 1967. Field Guide to Eastern Pacific and Hawaiian Sharks. United States Department of the Interior, Fish and Wildlife Service, circular 271, 47 pp. Limbaugh, Conrad. 1963. Field notes on sharks. In Perry W. Gilbert (editor), Sharks and survival, pp. 63-94. D. C. Heath and Company. MacGinitie, G. E. 1935. Ecological aspects of a California marine estuary. American Midland Naturalist, vol. 16, no. 5, pp. 629-765. MacGinitie, G. E. and Nettie MacGinitie. 1949. Natural history of marine animals. 473 pp. Mcliraw Hill Book Company. Miller, Daniel J., Dan Gotshall, and Richard Nitsos. 1965. A field guide to some common ocean sport fishes of California. California Department of Fish and Game, Marine Resources Operations, special publication, 87 pp. 54 Jarker, T. Jeffrey and William A. Haswell. 1963. A text-book of zoology. Vol. I I, Revised by A. J. tlarshall. MacMillan and Co. 952 pp. Ricketts, Edward F. and Jack Calvin. 1968. Between pacific tides. Revised by Joel Hedgpeth. 614 pp. Stanford University Press. Roedel, Phil M. and William ElI is Ripley. 1950. California sharks and rays. California Fish and Game, Fisheries Bulletin no. 75, 88 pp. Rounsefel 1, George A. and W. Harry Everhart. 1953. Fishery science, its methods and applications. 444 pp. John Wiley and Sons, New York. Russo, Ronald A. and Earl S. Herald. 1968. The 1967 shark kill in San Francisco Bay. California Fish and Game, val. 54, no. 3, pp. 215-216. Schott, Jack W. 1964. Chromatic patterns of the Leopard Shark, Triakis semifasciata Girard. California Fish and Game, val. 50, no. 3, pp. 207-214. Weichert, Charles K. 1965. Anatomy of the chordates. 758 pp. McGraw Hill Book Co.