l\IIOSS LANDING MARINE LAB LIBRARY
, " ~OST OFFICE BOX 450
rv:OS;:, LANDING, CALIF. 95039
ASPECTS OF THE AGE, GROWTH, AND REPRODUCTION
OF THE PACIFIC ANGEL SHARK, SQUATINA CALIFORNICA,
OFF SANTA BARBARA, CALIFORNIA
A Thesis
Presented to
The Faculty of the Department of Biology
San Jose State University
In Partial Fulfillment
of the Requirements for the Degree
Master of Arts
By
Lisa J. Natanson
August 1984
TABLE OF CONTENTS
LIST OF TABLES .
iv
LIST OF FIGURES.
v
ACKNOWLEDGE~\ENTS
vi i i
..
ABSTRACT . .
X
INTRODUCTION
1
MATERIALS AND METHODS.
AGE AND GROWTH . . .
Age Determination.
Radiography. . .
Histology. . . .
. ..
Tetracycline Grow-out Study . . . .
Age and Growth Hypothesis Testing.
REPRODUCTION
DEVELOPMENT . .
6
6
8
8
9
RESULTS . . . . .
AGE AND GROWTH
Age Determination.
Histology. .
. .
Tetracycline Grow-out Study.
REPRODUCTION
~\ales . . .
Females . .
DEVELOPMENT.
12
14
16
17
17
18
18
20
21
23
23
24
25
DISCUSSION . . . . . . . . . . . . .
AGE AND GROWTH HYPOTHESIS TESTING.
REPRODUCTION
28
28
34
DEVELOP~\ENT.
36
CONCLUSIONS . .
37
LITERATURE CITED
39
TABLES .
44
FIGURES.
47
iii
LIST OF TABLES
Page
o.
1.
Frequency of histological centrum edge stages by month.
45
z.
Growth characteristics of laboratory grovm specimens . .
46
iv
'·
),
7.
8.
9.
LIST OF FIGURES
Page
Diagram of Sguatina californica showing locations of five
measurements. The first 107 vertebrae in the vertebral
column are shown to exemplify the change in vertebral size
along the column of an adult specimen. These vertebrae are
25% of their original size. . . . . . . . . . . . . . . . .
48
Diagrams illustrating the axes along which histological
sections were cut. a) initial trimming of edges in longitudinal plane. b) position of final longitudinal cut
through the center of the centrum and resulting section.
c) cross section and resulting section. . . . . . . . . .
49
Histological sections of the centrum edges of four specimens
of Sguatina californica. Each picture shows one of the four
stoges of band development used as a standard to judge edge
development. Stages 1 and 2 represent translucent band
development and stages 3 and 4 represent opaque band development. Photos 1•ere taken at 40x with an Olympus photomicroscopy system. . . . . . . . . . . . . . . . .
50
Drawings of head, trunk and ta i 1 vertebrae showing the differences among the vertebrae from _different a'reas. A and B
are from the head end. C and 0 are from the trunk. E and F
are from the beginning of the tail. G, H, and I are from
the tail....
. . . . . . . . . . . . . .
. . . .
51
Graph depicting the relationship of band number and centrum
Wldth with centrum number of every fourth vertebra along
the vertebral column of a) a 225 mm TL specimen, and b) ~850 mm TL specimen. . . . . . . . . . . . . . . . . . .
52
The relationship between centrum width and tota 1 length using
only the number 12 - 14 vertebrae . . .
53
The relationship between centrum width and band number using
only number 12 - 14 vertebrae . .
. .
54
Relationship of histology band counts to radiography band
counts from the same specimens . . . . . .
.
55
The relationship between total length (mm) and weight (kg)
for a)
50 male angel sharks, and b) 68 female angel sharks.
56
v
Page
l.
The relationship between girth (mm) and total lengths for
13 angel sharks with associated linear regressions:
a) Girth #1 -under the pectorals;
b) Girth #2- above the first dorsal;
c) Girth #3 - below the second dorsal. . . . . . .
57
The relationship between total length (mm) and number of
bands for a) 56·male, and b) 87 female angel sharks. .
58
Photograph of tetracycline mark (arrow) and subsequent
band growth to the left of the mark of specimen 00951.
Photograph was taken using an Olympus photomicroscopy
system with a dissecting microscope. Lighting was provided by a U.V. light s o u r c e . . . . . . . . . . .
59
Growth of laboratory grown specimens #285 and 333. Time
of tetracycline injection is indicated b~ arrows. .
60
Photograph of the number 10 vertebra from specimen number
285 showing tetracycline mark (arrow) and three opaque
bands outside of the mark . . . . . . . . . . . . . . .
61
Photograph of the number 12 ·vertebra from specimen #333
showing tetracycline mark (arrow) and seven bands outside
of the mark. . . . . . . . . . . . . . . . . . . . . . . .
62
Curve depicting mean growth in TL (mm) of captive angel
sharks with the solid line representing the first year
of life of 2 captive angel sharks, and the slashed line
representing the growth of one shark for the second year
of life. . . . .
. . . . . . . . . . . . . . •·-······ ..
63
.
5.
6.
.7.
l8.
19.
20.
The relationship of a) inner clasper, and b) outer clasper
lengths (mm) and total length, (mm) of 71 and 72 male
angel sharks, respectively. . . . . . . . . . . . . . .
The relationship between total length (mm) and largest
egg d1ameter (mm) for 75 female angel sharks. . . . . .
Frequency histograms of a) the number of embryos in both
OVlducts, and b) the number .of eggs (>35 mm in diameter)
ln both ovaries. Arrows indicate the mean for each graph.
Rel at 1onsh1p
·
· of mean errbryo length (mm) in pregnant fe1
ma es to month for samples taken in 1983 . . . . . .
vi
. . 64
. . . 65
66
. . 67
flo.
21.
Page
Three views of a 35.40 mm TL embryo. Note the subterminal
mouth, protruding eyes, and external gill filaments.
Picture was drawn using a Wilde camera lucida at 60x . . . .
. 68
b)
Drawing of a 71 mm TL embryo.
Drawing of a 112 mm TL embryo.
69
~3.
a)
b)
Dravling of a 151 mm TL embryo.
Drawing of a 175 mm TL embryo.
70
24.
Ventral view of the internal organs of an embryonic angel
shark. . . . . . . . . . . . . . . . . . . . . . . . . . .
22.
a)
vii
71
ACKNOWLEDGE~1ENTS
I would like to thank the members of my committe, Drs. Greg
cailliet, Robert Lea, and Bernd Wursig for their helpful advice and
comments; also Or. Mike Foster for attending my thesis defense.
I would also like to extend my appreciation to the various students
and staff at Moss Landing for their help and advice in collecting data,
statistics, and technical expertise, especially Signe Lundstrom, Bruce
Welden, Dave Ebert, Kevin Hill, Kevin Lohman, Sheila Baldridge, Susan
Dearn, and Alan Lewitus.
Lynn McMasters and Sara Heimlich-Baran did·the
graphics, and Carol King did the typing.
John Richards, Sea Grant Area Marine Advisor provided help in
collecting, dissecting and communication with the fishermen.
I would
.also like to thank Phil Beghul, captain of the "Hula Girl" for
collecting samples and letting me collect samples and Bobby Reed,
captain of "The Sea" for letting collectors on board to obtain
specimens.
~1ike
Hagner, owner of Seafood Specialties in Santa Barbara,
California and his filleters were also very helpful in s·aving and
storing the "bones".
Finally, I 1·10uld like to extend my thanks to Shane and Ginny
Anderson for putting me and many others up at their house during
our trips to Santa Barbara.
"This 1-10rk is a result of research sponsored in part by NOAA,
National Sea Grant Co11 ege Program, Department of Commerce, under grant
numbers R/F-81, R/F-84 through the California Sea Grant College Program,
viii
and in part by the California State Resources Agency, project number
R/F-81, R/F-84.
The U.S. Government is authorized to produce and
distribute reprints for governmental purposes.''
i
X
ABSTRACT
Specimens of Sguatina californica were collected from commercial
11-net boats off Santa Barbara, California between Gaviota and
1 tura
from September 1979 to November 1983.
Histological and
jiographic techniques were employed to delineate calcified bands on
2
vertebral centra for age determination of 143 specimens.
Evidence
om number of bands in embryos and newborn sharks, growth patterns of
rth measurements and vertebral centrum dimensions, and laboratory
ow-out studies of marked fish support the hypothesis that band
position is related to somatic growth rathef than time.
Sexual maturity in both males and females begins at 900 to 1000 mm
Egg and embryo fecundity estimates indicate that the maximum
tmber of young possible .is 10 to ll per birth.
Once female angel
1arks reached maturity, the number of young did not increase with
\Creasing size of the female.
~males
~n
Embryo size from samples of pregnant
taken in consecutive months increased gradually during a
·-~-
month period from August through July.
Individual developmental
)rphology was described for five embryos ranging in size from 35.4 mm
- to 175 mm TL.
X
1
INTRODUCTION
In 1976, a method was developed for filleting the Pacific angel
shark, Sguatina californica Ayres, 1859, and this
allo~1ed
a commercial
fishery for angel sharks in Santa Barbara to steadily increase.
Prior
to 1976, angel sharks were taken incidental to the California halibut
fishery.
It was hazardous to extract live angel sharks from the nets,
and they were, therefore, generally killed and discarded (J. Richards,
Sea Grant Marine Advisor, pers. comm. ).
At the fishery's inception,
fillets retailed at $0.79 per pound with an ex vessel (directly from thefisherman) price of $0.15 per pound.
Prices have steadily increased,
and in 1982 fillets retailed at $1.60-1.76 per pound with an exvessel
price ranging from $0.35-0.45 per pound.
Angel shark landings in Santa
Barbara have increased from 329 pounds in 1977 to 328,513 pounds in
1983 (J. Richards, pers. comm.).
The Pacific angel shark is a member of the family Squatinidae,
which is represented world~1ide by one genus and eleven species (Bigelow
and Schroeder 1948, Herald 1967).
temperate waters.
Squatinid sharks occur-pr1marily in
The Pacific angel shar.k is the only species of
Squatina found off California, and it ranges from southeastern Alaska
to Baja and the Gulf of California and perhaps also from Peru to south
Chile (Walford 1935, Roedel 1953, Eschmeyer et {!_. 1983).
Sguatina
californica is reported to reach a maximum length of five feet (1524 mm
TL) and a weight of sixty pounds (27 kg) (Beebe and Tee Van 1941,
Miller and Lea 1972, Castro 1983).
2
st species of elasmobranchs studied have a late age at first
iCtion, lov1 fecundity, long gestation period, and slow growth
1
1977).
These factors tombine to make elasmobranchs easily
tible to overexploitation (Holden 1977).
Therefore, to properly
an elasmobranch fishery, it is imperative that aspects of the
luctive biology and growth of the exploited species be known.
;ary information includes age and growth, size and age at
i ty, fecundity, gestation period, and reproductive parameters.
data can then be used to detennine the ability of the population
1stain a fishery or recover from overfishing.
There are major gaps in the knowledge of angel shark life history.
fie angel sharks are known to be sluggish, nocturnal, bottom
lers (Limbaugh 1955, Standora and Nelson 1977).
A telemetric study
.he behavior of the angel shark off Santa Catalina Island,
tfornia showed that they tended to move at night, possibly in
eonse to decreasing light levels, and they kept to a residential
a (Standora and Nelson 1977).
Angel sharks remain buried in-the
d during the day (Limbaugh 1955).
They are found most often at
ths between 3 to 45 meters, on sand or mud bottoms near kelp and
ks (Eschmeyer ~ ~- 1983).
Limbaugh (1955) reported that these
rks have "typical shark teeth" and feed on active fishes such as
enfish (_Seriphus politus) and corbina (Menticirrhus undulatus). _
e lop~rent i
. .
s ovov1v1parous (Bigelow and Schroeder 1948), with 8 to 13
s being
d
pro uced (Pleshner 1983·, P. 8egu hl , commerc1a
· l f'1s herman,
s · comm.).
Other members of the genus have been found to contain
3
up to 25 embryos (Bigelow and Schroeder 1948, Gordon 1956, Breder and
Rosen 1966).
Little else is known about the biology of this shark, and
information is particularly scarce on age, growth and reproduction, or
development.
Vertebrae were first used to age elasmobranchs by Haskel (1949).
Since then, reliable techniques for ageing elasmobranchs by use of
vertebrae have been developed and evaluated (Ishiyama 1951, Jones and
Geen 1978, Cailliet et £.1_. 1983 a, b) and appear promising for ageing
angel sharks.
Most teleosts are aged by use of banding patterns on
paired bony otoliths or on scales; however, in cartilagenous
elasmobranchs the otoliths, or statoconia, are similar to sand grains
and the scales do not grow (Applegate 1967), so that these parts are
not suitable for ageing.
Some elasmobranch species have hard spines
which have been found to contain rings and are suitable ageing
structures (Ketchen 1975\.
However, for species without spines,
vertebrae have been used as the ageing structure (Ishiyama 1951, Holden
and Vince 1973, Holden 1974, Stevens 1975, Cailliet et £.1_. f983a;b).
Several methods have been developed to clarify the concentric pairs of
opaque and translucent vertebral bands; these include radiography
(Cailliet et £.1_. 1983a), celloiden impregnation (lshiyama 1951), and
silver m·t rate impregnation (Stevens 1975). The value of a technique
varies depending on the species being examined. The use of vertebral
bands as possible age indicators in angel sharks was first mentioned by
RideVJood (1921), who also noted a difference in band number in
verteb rae along the·vertebral column.
4
l~any
the
studies on elasmobranch age determination have assumed that
vertebral band pairs are deposited annually (Aason 1963, Richards
63 Taylor and Holden 1964, Stevens 1975, Edwards 1980). Many
et a1 . 19 '
of these studies base their assumption on the few actual validated
--
elasmobranch studies which have been performed on some Rajoid species
(Ishiyama 1951, Holden and Vince 1973, Holden 1974).
Few ageing
studies on either teleosts or elasmobranchs have been validated
(Beamish and McFarlane 1983).
To adequately validate the ages of
individuals of a species, all size classes of that species must be
validated (Beamish and McFarlane 1983).
In most studies in which validation has been accomplished, it has
been shown that one pair of bands is deposited annually throughout the
life of the fish.
Preliminary evidence on angel shark growth indicated
that they did not deposit annual band pairs, since they are born with 6
- 7 band pairs (Cailliet et
~-
1983b).
In contrast, a study by G.
Pittenger (graduate student, California State University, Long Beach,
pers. comm.) on angel sharks greater than 800 mm total length-(TC)
(from the tip of the head to the tip of the tail) at Santa Catalina
Island, California, indicated that angel sharks qrow slowly, at 20 - 25
mm per year and deposit band pairs annually.
Tetracycline was chosen as a method to det~rmine the periodicity
of band formation in angel sharks because its q~~lities make it useful
as a marker of calcified tissues. Injected te''"cycline is absorbed
and dep os1·t e d at sites undergoing calicificaticc while it is
circulat'lOg ln
· the bloodstream (1·1ilch et ~- r;:~. Pearse 1972). The
5
tetracycline mark is visible under fluorescent light, but growth before
and after the injection does not fluoresce (Milch et
and Ridgway 1962, Smith In press).
~-
1958, Weber
All yrowth outside of the mark can
be attributed to deposition over the time period subsequent to the
injection, and growth and deposition rates can be derived.
This
technique has been used to determine the periodicity of band deposition
in the lemon shark (Negaprion brevirostris) (Gruber and Stout 1983),
the leopard shark (Triakis semifasciata) (Smith In press), and the
thornback ray (Raja clavata) (Holden and Vince 1974).
Determination of the periodicity of band formation by use of
histological sections can also be accomplished by observing edge
sections of vertebrae from sharks collected at different times of the
year.
lshiyama (1951) identified the annual periodicity of the
vertebral bands of the Japanese black skate, Raja fusca, with this
technique.
The objectives of this study were to examine the age, growth and
reproduction of the Pacific angel shark.
Ageing studies
~utiTlied
vertebral bands, and temporal periodicity of the bands was examined
With a combination of centrum edge histology and tetracycline injection
laboratory growth experiments.
Resulting growth patterns were
evaluated in conjunction with reproductive characteristics obtained by
examining monthly samples of reproductively active specimens.
Three hypotheses concerning the periodicity of band pair formation
Were generated and tested.·
1 ) band pairs are deposited annually
throughout the life of the s hark; 2 ) band pairs are resorbed or cease
6
1
form in adult sharks and/or at the tail; and 3) band pairs are
!posited in relationship to somatic growth of the individual and not
trictly to a predictable time frame.
MATERIALS AND METHODS
Specimens of Sguatina californica were collected off Santa
arbara, California between Gaviota and Ventura.
Most specimens were
ollected from commercial halibut gill or trammel nets operating at
lepths of 6 to 37 meters.
Esh trammel nets.
~sherman.
The primary capture method involved 20.32 em
Numbers and lengths of neis varied with the
Nets were usually set during the morning and retrieved one
Jr two mornings later.
Samples v1ere also obtained from fishermen using
)tter trawls at depths of 58 to 77 meters.
Large specimens were dissected on board and small specimens were
frozen for dissection at a later date.
Measurements taken on most
,specimens were total length (mm), alternate length (mm) (the distance
from the origin of the first dorsal fin to the origin of the second
'dorsal fin), and inner and outer clasper lengths (mm) of males.
In
~ddition, three girth measurements were taken from several specimens
(Figure 1), at the insertion of the pectorals, just above the first
dorsal fin, and J·ust belo•1' the second dorsal fin.
For many specimens,
weight was taken with a spring scale accurate to ±0.23 kg.
AGE AND GROWTH
After obtaining measurements, the abdominal cavity was opened v1ith
an incision from the cloaca to the pectoral girdle and the gonads and
7
vertebrae were removed.
Gonads, either ovaries and oviducts or
wolffian ducts, were frozen and later transferred to 10% formalin and
then to 40% isopropyl alcohol.
As much of the vertebral column as possible was removed for later
use in ageing studies.
In some specimens, only the head and/or tail
vertebrae were available depending on the person collecting the data
and whether or not the fisherman had prepared the carcasses for the
processors.
In other instances, the entire column was obtained from
the processor.
Only vertebrae numbers 12 to 14 were processed for
ageing since they represented vertebrae with the highest counts (see
results).
The highest count from these vertebrae was accepted.
To
determine which vertebrae were consistently in the region of highest
counts ("plateau region"), counts and centrum width measurements (mm)
were obtained for each vertebra along the column of 14 specimens.
Band
number and centrum width were then plotted against vertebra number for
each specimen.
These graphs were visually compared to determine which
vertebrae v1ere in the plateau region of all specimens.
Vertebrae which were known to have been taken from head and/or
tail regions were e 1·1m1nate
·
d from the ageing analysis.
To determine
whether vertebrae from unknown areas of a specimen should be kept or
discarded, radiographs of head, trunk, and tail vertebrae were examined
for morphologic characteristics which might differ with the body region
from which the vertebrae were taken. Some trunk vertebrae could not be
disting · h
Uls ed morphologically, therefore, the following calculations
'tlere perfor d
me to determine how different the centrum width and band
8
counts of these vertebrae were from the plateau vertebrae.
Mean
percent dl.fferences in centrum diameter and band counts were calculated
for one vertebral column, using vertebrae 12 - 14 as a basis to judge
the deviation of the rest of the vertebrae from the plateau.
Centrum width was plotted against total length and against band
counts for vertebrae from positions 12 - 14, using the highest of the
three centrum width and band count values from each specimen.
A linear
regression was then calculated and fitted to the points (Zar 1974).
Age Determination
Radiography
To prepare the vertebrae for radiography, individual centra were
soaked in water for five minutes, transferred to bleach for one to 20
minutes, depending on size, and then soaked in water to remove the
bleach.
Whole centra were x-rayed with a Hewlett-Packard Faxitron
Series X-ray system (Model No. 43805N) with Kodak Industrex M film
(Readypack ~1-2).
Radiographs were examined under a dissecting
microscope for counts and measurements.
Two readers made separate and
independent counts of the vertebrae on each radiograph.
A band was
defined as a single opaque or translucent concentric circulus, and this
definition is similar to Cailliet et ~.'s (1983a) definition of a
ring.
For coun t s t hat differed by only one, the count of one reader
was accepted for the f 1rst
·
specimen and the count of the other reader
was accepted for the next specimen with a difference of only one band.
This alternation of accepting counts was continued until all the
specimens with a difference of only one band were tabulated.
If counts
9
two or more bands, the specimen was recounted by both
ere off by
.
~aders, using the double blind technique, until a concensus was
•eached.
Histology
Monthly samples of Sguatina vertebral centra taken from June to
October 1982, and weekly samples taken from November to December 1983
were processed histologically to discern the changes in band deposition
patterns over time.
Vertebrae from the head, trunk, and tail regions
of one angel shark were sectioned histologically to see if the edges of
vertebrae from all parts of the body were in the same developmental
stage.
The following procedure was used to process the vertebrae for
histology:
1.
The vertebral column was thawed, one to four vertebrae were
removed and separated, and the rest of the column was refrozen.
The
neural and hemal arches and loose connective tissue were trimmed off
each centrum.
Centra were then preserved in 10% formalin for a minimum
of three hours.
2.
Centra were decalcified in 100% ROO, a commercial decalcifying
agent.
The length of decalcification depended on the size of the
centrum and ranged f rom f.1ve m1nutes
.
to eight hours. The stage of
decalc"f·
·
1 1cat1on
was determined by the ease with which a sharp
razorblade could trim off a section of the centrum.
Two other
decalcifiers, 4% nitric acid and commercially prepared Cal Ex II were
tried but neither worked well.
10
3.
Centrum edges were trimmed longitudinally to approximately 2
mm thick (Figure 2a).
These sections were stored in 70% ethanol (ETOH)
until embedding, from 1/2 hour to several months.
embedded in a 9:1
r~tio
The sections were
of 1450 molecular weight polyethylene glycol
and acetyl alcohol, respectively.
The specimens were soaked for 30
minutes in solutions of 70%, 80%, 95%, and two times in 100% ETOH.
They were next placed for one hour each in a 50:50 and then 75:25
solution of the wax mixture to 100% ETOH.
a 60% oven.
Both of these steps were in
Finally, they were placed in embedding molds that were
filled with 100% wax and placed in the freezer to harden.
Paraffin
embedding, as recommended by Ridewood (1921), was less successful due
to cracking and chipping during slicing.
4.
Sections were sliced on an A.D. rotary microtome between 10
and 15 microns thick, and place·d on albumin covered slides.
were then dried on a warming tray for at least one week.
The slides
Large angel
shark centra were sliced longitudinally through the center, creating a
half bow tie shaped slice (Figure 2b).
The smaller specimens were
sliced transversely along the centrum face (Figure 2c).
5.
Slides containing sections of angel shark centra were stained
in a 5% solution of Congo Red in 95% ETOH as recommended by Ridewood
(1921).
Hematoxylin-Eosin as recommended by Ishiyama (1951) and
Hematoxylin saturated Wl.th Orange Gas recommended by Ridewood (1921)
did not define the cells
as well as Congo Red. Stained slides were
mounted with Pe
rmount and dried on a warming tray for at least one
11
Slides were boxed until completely dried, and then scraped clean
eek.
nd labeled.
Sections were examined under a compound microscope for cell types,
rowth zones, band counts, and measurements.
Measurements to the
earest 0.001 mm with vernier calipers were taken from the focus to the
1
!dge of the growing zone and from the outer edge of successive opaque
Jands.
Edge development was divided into four categories on the basis
Jf the amount of opaque or translucent band formation (Figure
3).
)tage 1 represented the beginning of formation of a translucent band.
The last opaque band has been formed and a few individual cells are
visible after it.
Stage 2 represented further formation of the
translucent band.
At this stage, more cells have filled the band area
and band
~idth
is defined.
band formation.
Clumps of cells are ·now gathering at the cell
proliferation zone.
opaque band.
Stage 3 represented the beginning of opaque
Stage 4 represented the further development of the
At this stage, more cells have become visible and the
band is becoming more dense.
To determine whether or not counts obtained from histology
differed statistically from counts obtained from radiography, a simple
linear regression through the origin was calculated (Zar 1974).
Slopes
of 1ines were compared by t - t es t , an d if the slopes were not
significantly different at the 0.05 probability level, the counts from
each method were considered equivalent.
Total length was plotted against band number. Graphs were plotted
separately for males and females.
Since periodicity of band formation
12
is unknown for this species, actual growth curves, which are dependent
on age information, were not fit to these plots.
Tetracycline Grow-out Study
Whenever possible, small angel sharks were kept alive on board the
fishing boats in a 50 gallon container.
The fish were transported from
the boat to aquaria at the University of California, Santa Barbara
(UCSB) Marine Science Center in ice chests containing seawater and
battery powered aerators.
Some of the sharks remained at UCSB, but the
majority were transported to the Moss Landing Marine Laboratories
(~1U·IL)
ir. similar containers after one to two days.
At MLML, the fish
were maintained in a 2.43 x 1.22 x 0.46 m wooden tank behind a plywood
enclosure.
The tank was equipped with constantly circulating seawater
pumped from a beach well, aerators, and a 5 em deep layer of fine sand.
The sharks were primarily fed thawed anchovies, and occasionally
thawed squid and mackerel, using a method modified from Robert Johnson
(Cabrillo Marine Museum, pers. comm.).
The food was attached by a
rubber band to a 61 em long, 9.5 mm diameter wooden dowel ·;nd was
dangled approximately 5 em above the·shark's head.
If there was no
response after approximately 5 minutes, the food was removed.
attempt was made to feed the sharks once each weekday.
An
If the shark
ate the first fish , it was offered one fish at a time until it stopped
feeding. L'lve Juvenile
·
rockfish, smelt, and sticklebacks, when
available, were placed in the tank so that the sharks could feed on
their own schedule.
13
the live angel sharks were initially measured, weighed on a bench
,ca 1e. sexed ' and injected with a
f~
days af ter ca Pture ·
·n
I!I!USUf€ d l
25 mg/kg dose of tetracycline a
After the initial measurements, the fish were
the tank to reduce trauma.
A measuring tape was stretched
from the head to the tail on the dorsal surface of the fish and the
bn<Jth was directly read from the tape.
Information on total length
and food intake was logged while the sharks were alive.
Upon death, sharks were measured and dissected in the manner
previously described.
Because tetracycline loses intensity with
exposure to light (Weber and Ridgway 1962) the dissections were done in
a darkened area.
To delineate the tetracycline mark as well as the
bands, vertebrae were processed using a resin embedding method (Smith
In press).
Hi~tology
was not used since the chemicals involved in that
method would dest1·oy the tetracycline mark.
in 70% ETOH for a minimum of 3 hours.
Vertebrae were preserved
The vertebrae were then soaked
overnight in a mixture of equal amounts of uncatalysed polyester resin
and acetone.
Next, vertebrae were placed in ice cube trays-containing
catalysed resin, until the resin hardened in a minimum of 24 hours.
The blocks Vlere then roughly trimmed with a band saw and evened out on
a belt sander.
rocesse d blocks were mounted with epoxy on rectangular
Pieces of acetate. 0nee d ried, the acetate-blocks were inserted into a
specially designed chuck wh1c
· h was f itted to a Buehler .Isomet low-speed
SaVI.
Th
p
e vertebrae Vlere sliced down the center longitudinally along
the widest part of the
oval with two diamond blade saws separated by an
approximatley D.Z3 mm acetate spacer. The resulting section was
14
attached to a microscope slide with clear enamel nail polish.
Sections
were viewed under a dissecting microscope in the dark with a short-wave
portable ultraviolet light to illuminate the tetracycline mark.
To determine if tetracycline was incorporated into all vertebrae
'
of an individual, every fourth vertebra along the column of the
successfully-grown laboratory sharks was sectioned and examined for
fluorescence.
The sections were viewed in the dark under a dissecting
microscope with ultraviolet lighting.
For all sections, the presence
and amount of fluorescence were noted.
t·1ean growth rates (mm/month) were calculated for two successfullygrown young sharks.
Growth was added to mean size at birth and plotted
against months, adding the mean value to the lengths at each successive
month, to show growth for the first year of life.
The growth rate of a
shark kept at the Cabrillo Marine Museum for over 24 months during the
second year of life (R. Johnson, pers. comm.) was also used
comparatively.
A mean value for the number of mm grown per band pair deposited
was calculated.
Th is was then superimposed on the total length versus
band number graph starting at the mean total length and number of bands
at birth up to the maximum number of bands laid down by my live sharks.
Age and Growth Hypothesis Testing
The hypothesis that all bands were annual was tested by comparing
the number of bands
after the tetracycline mark to the known time since
injection , and by exa . . th h .
.
.
m1n1ng e 1stolog1cal
sect1ons
of vertebral
15
centra from specimens collected at different times of the year for
seasonal changes in band deposition.
Band resorption and the possibility of cessation of band depostion
in older sharks or at the tail region were evaluated by examining the
growing zone of vertebrae in histological sections for proliferating
cells.
Also, tetracycline uptake along individual columns was examined
to see if there was any difference in uptake at the head, trunk, and
tail regions which wouid indicate a difference in calcium activity at
the different regions.
To evaluate the hypothesis that band deposition was related to
somatic growth, results from the tetracycline-injected, laboratoryreared specimens were analyzed.
Band counts from individuals that grew
substantially for short periods were compared to band counts from an
individual that grew.less during a longer period to see if the
individuals that lived the shorter peirod had more bands than the
longer lived individual.
This would indicate that an increase in bands
was related to an increase in total length.
Each of the three girth
measurements made along three regions of the body were plotted against
total length to give an estimate of relative girth growth along the
body.
Regressions were calculated and an analysis of covariance was
perforwed followed by multiple comparisons among slopes (Zar 1974).
The differences between the lines were then related to the changes in
band number ( see resu 1ts ) at these regions of the body.
16
REPRODUCTION
An attempt was made to collect monthly gonad samples for
reproductive studies of angel sharks taken off Santa Barbara from
January 1983 to December 1983.
However, due to weather conditions and
the unpredictability of fishing, samples were not obtained in April,
June, September, or December.
Maturity in males was determined using three methods:
1. Clasper
length versus total length graphs, where maturity is indicated when
clasper length suddenly increased relative to total length (Holden and-Raitt 1974); 2. Coiling of the wolffian duc't; and 3. Sperm smears taken
from the wolffian duct, stained using the Harleco Diff-Quik stain set
(Pratt 1979), and examined for viable sperm under a dissecting
microscope.
Sexual maturity in females was determined by the number and size
of eggs and embryos and the condition of the ovaries and oviducts.
Once several females were examined, stages of maturity were defined and
were based on the following criteria (Holden and Raitt 1974)~
l.
Imnature:
Ovaries 'and oviducts small, flaccid and
undeveloped.
No discernible eggs.
2.
Maturing:
Ovaries and oviducts enlarging.
3.
containing visible eggs 5-10 mm in diameter.
Mature: Ovaries containing large, heavily yolked eggs 50-60
Ovaries
mm in diameter.
4. Mature/Ripe:
Spent:
Fertilized eggs and/or embryos in the oviducts.
Oviducts and vagl'na fl acc1'd and stretched.
17
All eggs and embryos were counted and measured to the nearest 1 mm
~!Je
either fresh or after having been thawed.
An average of the
number of maturing eggs per individual and an average of the number of
~ryos
per individual were calculated to provide two independent
estimates of average fecundity.
A frequency histogram was drawn to
show number of embryos in both oviducts and another was drawn to show
the number of maturing eggs (>35 mm in diameter) in both ovaries.
The
largest egg diametet· was plotted against total length of all sized
females to show the onset of maturity.
Embryo size per month was
calculated and plotted by month to attain information on gestation
period and pupping season.
DEVELOPMENT
Embryos at different developmen.tal stages were examined for
initial development of adult characteristics such as teeth, mouth
position, coloration, body proportions, and eye position.
Change in
yolk sac from external to internal and change in gill filament5 were
also noted.
RESULTS
A total of 326 angel sharks was collected from August 1979 to
liovember 1983· of ~h
'
c ese, 117 were male and 209 were female.
Sizes
from a 35 · 4 mm TL embryo to an 1180 mm TL adult. Centra from
duals were P.rocessed for age1·ng, an d repro duc t"1ve 1n
· f orma t"10n
on 71 males and 76 females.
18
Angel shark vertebrae were generally oval but varied in shape and
brphology in differing parts of the body (Figure 4).
ere
"squarish" and the basapophyses were directed laterally off the
lidregion of the vertebrae (Figure 4a,b).
~d
Head vertebrae
Trunk vertebrae were oval
the basapophyses were directed laterally off the ventral region of
vertebrae (Figure 4c,d).
Tail vertebrae became somewhat diamond
and the basapophyses were directed ventrally off the ventral
and formed the hemal arch (Figure 4e,f,g,h,i) (tenns following
1975).
The vertebrae from all regions of the column had
istinct evenly spaced bands.
AGE AND GROWTH
Trunk vertebrae could be distinguished from head and tail
by the position of the basapophyses, however, not all trunk
were from the plateau region.
Trunk vertebrae, numbers 8
48, were indistinguishable by morphology.
t
Calculations of
deviation of unknown vertebrae from the plateau vertebrae (12
showed that the range of deviation in band counts of the unknown
would be 0.5 to 2.43 bands in a shark which had 31 bands in
plateau vertebrae (only a 1.6 to 7.8% difference).
This deviation
not substantial and it was felt that the vertebrae that could not
in
fferentiated by mo rp ho1ogy were vnth1n
. . an acceptable range for use
ng.
Age Determination
counts differed along the vertebral column, especially in
Figure 5 for two examples).
Counts were low in
19
vertebrae taken from immediately behind the head, increased to a
plateau, and decreased towards the tail (Figures 1, 5).
In small
individuals, counts only varied by one, but with larger sharks, the
difference~were
higher and more variable.
After examining band counts
along the column of 14 individuals, it was determined that the number
12 to 14 vertebrae were consistently within the plateau of highest
counts.
There was a significant linear relationship between total length
and centrum width ( r 2
centrum width (r 2
=
=
0. 98) ( Figure 6) and between band number and·
0.92) (Figure 7) for vertebrae 12 to 14.
Band counts agreed well on vertebrae processed with both
ra~ographic
and histological techniques (Figure 8).
Two readers
counted vertebrae processed with both methods on 111,samples of.
specimens ranging from 210 to 1170 mm TL.
For radiography, 102 (57%)
of the initial counts were the same, 52 (29%) disagreed by one, and 23
(14%) disagreed by two or more bands.
For histology, 57 (50%) of the
initial counts were the same, 42 (38%) differed by one;· a
ncr l4
(12%)
differed by two or more band counts. There was no significant
d'f
1
ference in counts between the two techniques (t O.OS 110 = 0.379);
, counts made using both methods were combined in data
for all specimens.
Weight increased exponentially with increasing length in both
and females (Figure 9a,b).
Weights become more variable over
attained a greater weight than males.
ght equation for 50 males was y
=
1.33 - 0.00831x +
The
20
0.0000152x2 (r2 = 0.96) and for 68 females was y = 2.095 - 0.0115x +
o.0000182x 2 (r 2 = 0.98).
Girth increased with size more at the region just below the
pectoral fins than at the two tail regions (Figure 10).
The analysis
of covariance revealed that there was a difference among the three
lines (F0.05(1),2,33
=
1180.31).
The results of the multiple
comparisons among slopes indicated that all three slopes were different
(q 1-2 0.05, 33,3
=
9598 ; q 1-3 0.05, 33,2 = 13880 ; q 2-3 0.05, 33,2
=
4282).
For both males and females, the number· of bands increased with
increasing length until 900 mm TL (Figure lla,b).
increase in band number with total length.
Both graphs show an
The male graph is basically
linear but begins to level off after 1000 mm TL.
The female graph is
linear until 700 - 800 mm TL, when a more rapid increase in size is
dent.
After 1000 mm TL there is variability among the points rather
than a leveling off.
Histology
Examination of every fourth vertebrae from the column of a 1180 mm
Tl female collected in January 1983 showed that although there were
differing numbers of bands on each vertebra, a 11 growing edges were in
'><a.ge
L
Edge formation wa s no t pre d'1ctable by t1me
. of year. The maJOrlty
. .
)of the 111 sp ·
ec1mens collected from June 1982 to October 1982 and
19 83, which were examined histologically for band
at the centrum edge, were in developmental stages 1 and 2
21
For all sized fish, stages 3 and 4 (opaque band formation)
observed more often in the winter samples than in the summer
es (Table 1).
No lunar periodicity was noted from the edges of centra from angel
s over 900 mm TL collected weekly.
Only one fish out of 15 taken
the 4 week period was in stage 4; all others were in stage 1.
racycline grow-out study
Three female angel sharks were alive long enough to incorporate
tetracycline into calcifying areas of their vertebrae and to deposit
bands subsequent to the resulting mark.
Specimen 00951 was 592 mm TL on 30 October 1982 when caught and
615 mm TL on 8 December 1982 when it died.
It had grown a total of 23
mm in 5 v1eeks, and had a growth rate of 18.4 mm per month.
This shark
decreased 0.15 kg in weight (from 1:42 kg to 1.27 kg) and it nev~r fed
in captivity.
Sections of vertebra number 12 showed a discrete
fluorescent mark in the 19th opaque band (Figure 12).
The resin
embedded vertebral section showed growth of a translucent and--the
beginnning of an opaque ban9 in the region outside the tetracycline
The second shark (number 285) was born along with 5 other sharks
29 f.larch 1983.
0ne of the young died at birth and had 5 vertebral
on vertebra number 12.
Three more young died within a month
and had 5+ to 6 bands on vertebrae number 12.
Because
approximately the same size and in the same
stage at birth, it is assumed that they were all born
with 5 bands. Specimen #285 was 254 mm TL when first measured on 14
April 1983 and 348 mm TL when it died between 2 and 5 October 1983. It
had grown 94 mm in 6 months and had a growth rate of 15.4 mm per month.
Howeve,r, there was a decrease in growth rate following the tetracycline
injection on 5 July 1983 (Figure 13).
This was followed by a rapid
rate of growth in September and October.
Upon dying, it had 10 total
opaque bands on vertebra number 10, 3 of which were deposited in the
approximately 4 months since the tetracycline mark (Figure 14).
The third shark (#333) was also born on 29 March 1983.
It was 250
mm TL and 168 gm on 14 April 1983 when first measured and 412 mm TL and
462 gm when it was terminated on 21 May 1984.
It had grown 162 mm,
gained 294 gm in weight and had a growth rate of 12.5 mm per month.
The gro.wth of this specimen appeared to be unaffected by the
tetracycline injection (Figure 13).
tetracycline on 24 May 1983.
This shark was injected with
Upon dissection it had a total of 13
opaque bands on vertebra number 12, seven of which were deposited in
12 months after the tetracycline injection (Figure 15).
The latter tv10 sharks started to feed after 41 days in captivity.
feeding was initiated, the sharks generally fed once every two
we<:ks for 1.5 months and then fed once or twice a week.
relationships of number of bands deposited to time and to
for the latter two sharks was compare d to t he same informat1on
·
lr
·
Shark grown at Cal1'forn1·a St at e un1versity,
Long Beach ( Table
2l12:Thi i nd ·
lcated that there was a closer relationship of band
to growth in total length than to time.
23
Tetracycline was incorporated in vertebrae from all regions of the
vertebral column.
The vertebral columns of the three laboratory grown
angel sharks (00951, 285, and 333) were all examined for tetracycline
All had tetracycline in all parts of the column and band
uptake.
gro~tth
'•
following the mark.
It was therefore concluded that all parts
of the column were actively depositing calcium.
The mean growth per month for specimens 285 and 333 (13.54 mm)
multiplied by 12 and added to the average length at birth (260 mm TL)
yields a length of approximately 422 mm TL for a year old shark (Figure
16).
Specimens 285 and 333 added one band pair for every 20 mm TL.
Assuming that this is the rate of band deposition for the first 13
bands (the maximum of #333), the resulting growth curve (Figure 11)
ts closely with the field collected data on size and band number.
REPRODUCTION
Males Males were first sexually mature at 900 to 1000 mm TL -·a{ the 20
males
greater than 1000 mm TL ' all were considered mature by at least
--,
the three maturity criteria.
Clasper length begins to increase
between 900 and 1000 mm TL (Figure 17).
Of the 20 sperm smears
individuals between 690 and 1150 mm TL, 15--all over 1000 m
viable sperm.
Four greater than 1000 mm TL and one 690 mm TL
have viable sperm. Of the fish examined which were larger than
TL, 19 out of 20 individuals had totally coiled ducts. A
24
ight wave of the ducts was first seen in one 690 mm TL individual and
ng was complete in one 865 mm TL individual.
es Females were first sexually mature at approximately 900 to 1000 mm
A total of 74 specimens examined from January 1983 to November
demonstrated an increase in egg diameter at about that size
Figure 18).
The smallest female found with young was 1079 mm TL.
In most specimens, only the left ovary was functional.
In 21 of
the 29 (72%) samples with two ovaries, the right ovary had not
developed.
In one specimen the left ovary had not developed.
The
development of the second ovary did not seem to be correlated with size
as both ]arge and small females were found with and without two
functional ovaries.
Small (<5 mm in diameter) eggs began to appear in the ovaries of
females over BOO mm TL.
The smallest female found with eggs was 810 mm
All females over 1000 mm TL had eggs that ranged from ·res·s than 5
in diameter to 70 mm in diameter.
Most females with developing
had eggs 20 mm or less in diameter.
Those without embryos had
a >tide range of egg sizes.
Egg and embryo fecundity estimates indicate that the maximum
of young possible is 10 to 11 (Figure 19).- The number of large,
ng eggs (>35 mm diameter) seen in the combined ovaries of one
ranged from 1 to 10 with a mean of 7.
The maximum
25
r of embryos observed per female was 11 and the minimum was 1,
a mean of 6.
Once female angel sharks reached maturity the number of young did
increase with increasing size of the female but rather varied a
deal among individuals.
In 13 (19%) of the mature females, the oviducts were filled with
olid yolk.
No membranes divided the yolk in these specimens.
iducts were vascularized and often appeared orange.
These
The ducts were
illed but not overextended.
Mean embryo sizes, from samples of pregnant females taken in
nsecutive months, increased gradually during a 10 month period
(Figure 20) from August 1982 through July 1983.
sampled, individual females had embryos present.
found in various stages within each month.
average size at birth in
In all of the months
The embryos were
Young began to reach the
r~arch.
OEV ELOPMENT
Descriptions of individual developmental morphology for five
of increasing sizes (35.4 mm. TL, 71 mm TL, 112 mm TL, 151 mm
'and 175 mm TL) are as follows:
35 · 4 mm TL embryo:
This embryo was one of four from the right
of a 1130 mm TL specimen caught in August 1983 (Figure 21).
'"'''
At
in development, the skin was transparent with a yellowish
All fins were evident but not well developed.
ible a d
Gill filaments
n extended approximately 2 mm past the gills.
around the subterminal mouth.
Barbels
A broad ridge extended over
26
the dorsal sur f aCe
protruded.
Of
the embryo .
No teeth or secondary
Un~'"e
'
sext...~l
1·n the adult, the eyes
characteristics had developed.
Nutn·t·10n was from an external yolk s'..::ply.
71 mm TL specimen (Figure 22a):
':"his embryo was from a 1138 mm TL
The s~•, was less transpar~nt although
shark caught in October 1983.
the brain and pigmented internal arec.s were visible.
spots vJere located dorsally.
Six brown pigment
All fins were developing but pectoral
fins were small relative to the head,
Gill filaments were present but
barely extended past the gill openin<;s.
position and the eyes protruded.
The mouth was in a subterminal
A l':';mnan,t of the dorsal ridge found
in the 35.4 mm TL specimen was now lc-.::ated over the cranial area.
Claspers appeared to be forming but
development.
~ere
No teeth had developed.
in a very early stage of
Nutrition was by external yolk
supply.
112 mm TL embryo (Figure 22b):
female caught in October 1983.
This specimen was from a 1100 mm
There was still some transparency of
the skin, as the brain and some muscle could still be se.en .... More brown
pigment spots v1ere visible dorsally itlong the tail and onto the fins
than in the previous specimen.
The background skin was yellowish.
The
head was slightly larger relative to the fins than in the adult.
External gill filaments were no longel' present.
The eyes were
protruded somewhat, but not as much ,1s in smaller specimens and the
had moved farther towards the terminal position.
head '<las reduced.
The bulge on
A s1ng
· 1e row of small teeth, approximately 0.124
27
v1er e Present in both jaws.
an external yolk supply.
(Figure 23a):
Claspers were visible.
Nutrition
This specimen was taken from a
TL female caught in November 1983.
rency associated with the skin.
There was no longer any
Spots covered the skin and came
r in a somewhat reticulated pattern with yellowish lines in
Fins had developed and the body proportions were basically as
Teeth were present in rows.
was in the terminal position.
The eyes did not protrude
The external yolk was
1 the means of nutrition; however, an internal yolk sac was
nnning to bud where the external yolk joins the anterior portion of
stomach (Figure 24).
175 mm TL embryo (Figure 23b):
This specimen was taken from a
mmTL female caught in November 1983.
This embryo resembled the
t except for the presence of both internal and external yolk sacs.
the final stages of development, more yolk was stored in the
sac which increased in size; the external sac was eventua"lly
and the connection sealed.
internal yolk sacs.
No free-living young were found to
It was presumed that this was resorbed
Captive young taken from the female prematurely
.feed until the internal yolk sac was completely resorbed.
28
DISCUSSION
AGE AND GROWTH HYPOTHESIS TESTING
Data from tetracycline-injected 1aboratory grow-outs, centrum edge
tology, band numbers on newborn sharks, and results from a
o~Tetric
dating study on two angel sharks do not support the
s that all bands are deposited annually.
Information from a
eld tagging study off Catalina on adult angel sharks, however, does
i;Lipp<Jr t thiS hypothesiS·
Data from the three tetracycline-injected, laboratory-grown young
Iangel sharks indicated that band deposition in these sharks is not
annual.
This is further supported by information on a newborn shark
which was kept in captivity for 11 months at California State
University, Long Beach (CSULB) (J. McKibben, pers. comm.).
initially measured at 240 mm
utt!s.
comm.).
TL~on
This shark
April 8, 1982 (J. McKibben,
At this time, according to my data, the shark would have
approximately six band pairs.
The shark died 11 months later (13
Hay.1983) at a length of 290 mm TL having grown 50 mm.
When it died,
had eight bands, having added only two band pairs in the 11
edge histology results on adult angel sharks indicate
is not possible to predict at what time of year the opaque
translucent bands are forming.
This is in contrast to the study
(1951) who demonstrated an annual band pair formation
the Japanese black skate, Raja fusca.
29
Cailliet ~~- (1983a) found that 6 to 7 band pairs occur in
,wborn angel sharks and my monthly analysis of mean sizes of embryos
uggests a gestation period of approximately 10 months.
Therefore,
mbryonic band p~irs are certainly formed more frequently than once per
ear.
Results from a radiometric dating study on two adult angel sharks
;now that band pairs are deposited more frequently than once per year
[Welden 1984).
The sharks used in this study were 1110 mm TL with 33
1ertebral bands and 1016 mm TL with 31 vertebral bands.
The
radiorretric ages of these sharks were 1 - 6 (± 7) years and 6 - 8 (±
years, respectively.
These data support my results that band pairs
not deposited annually.
In contrast, field data on the growth of larger angel sharks (over
support the hypothesis that band pairs are deposited
Growth rates of angel sharks in a field tagging study off
Island, California were relatively slow (20 - 25 mm/yr) (G.
CSULB, pers. comm.), and suggest that the band pairs- are
annually. ·However, few vertebrae from these tagged sharks
<>·-~~"analyzed in support of this suggestion and no verification
It is possible that the Catalina sharks are from a
than the Santa Barbara sharks, and this may
differnece in growth rate and possible difference in band
It has also been well documented that as animals
ty, their growth slows (Thompson 1942).
This would
the decreased growth rate ,·n the larger sharks.
30
on tetracycline uptake along the vertebral column, histology
edges, and information from the literature do not support
i 5 that bands are resc1·bed or cease to form in older fish
ta.il region.
This hypothesis is supported by evidence from
ationship of total length to band number.
of the relationship between total length and band
change in either growth or band deposition occurs
900 - 1000 mm TL (approxiliiately 28 bands) (Figure 11).
The 900
mm TL area of this curve corresponds to the length when maturity
d by both males and females, but the change in growth is most
e in the female.
One explanation could be resorption of
(and subsequent band loss) to route calcium to the growing
Another possibility is that the high variability in number of
be caused by a decrease in deposition during reproduction.
this.
tetracycline was incorporated into all of the vertebrae of
sharks ranging in size from 248 - 615 mm TL, it can-oeall vertebrae were forming bands.
Injected tetracycline
and deposited at sites actively undergoing calicification
in the bloodstream (~1ilch ~ ~· 1958, Pearse 1972).
If
on Ylere occurring, or if bands were not forming in any
<(vef.tehl'".,
'active tetracycline uptakE would not be occurring and
ld not be incorporated.
Therefore, bands were being
the body of the injected fish.
31
nd formatl· on wa s occurring in all vertebrae examined.
If active
ion was taking place chondroclasts would be required to resorb
lcium from the broken down bands (Urist 1961) and this was not
If bands were not forming, new band cells would not be
hoV~ever,
new cells were found in all sections examined.
All
""''''"a" examined caul d be placed in one of the four formation
es of bands; this also indicates that bands were forming and
ion was not occurring.
overall concensus is that there is no internal remodeling or
n in the cartilaginous skeleton (Ridewood 1921, Urist 1961,
hypothesis that band deposition in the angel shark is related
'"'1111
•t•tr growth and not time is supported by the results of 1 ive
fish, data from a tag and recapture program
~he:/Cata,Jina Island Institute for Marine and Coastal Studies {G.
te1igeffi pers. comm. ), band number at birth as related to gestation
results of girth measurement analysis.
angel shark grown at California State
combined with the grow-out data from this study
te.f..hiltt band deposition is related to body growth rather than to
this shark VIas not lnJected
· ·
with tetracycline, this
buted to the slow deposition of the bands.
By
deposition of my live sharks to the CSULB
that band nurn ber 1s
· dependent on somatic growth.and
One of my sharks {#285) deposited more bands in a
32
r pen·act of time and had a faster growth rate than the CSULB
There was a dip in growth after the tetracycline injection in
rk, but it was most likely due to inaccuracies associated with
(Figure 13).
My other shark (#333) deposited more bands,
longer, and grew more than either #285 or the CSULB shark, but
did not deposit the bands in a temporally predictable manner.
ize and band numbers of all three of these sharks fit perfectly on
band number and size graph (Figure 11), which indicates that
number is more closely related to size than time.
mean number of millimeters per band pair for laboratory grown
285 and 333 fits directly on the field total length versus
nillnbe'r graph (Figure 11), and this indicates that band pair
•v~•~•u"
is related to somatic growth.
Both these sharks deposited
for each 20 mm of total length, but bands were not
any predictable time frame.
This indicates that
s related to somatic growth rather than to time.
An
.!:l!ilc!l.e:of one band for 20 mm for young sharks fits well with the
<i~cJI'!!lgi:h versus band number relationship for field data (Figure
~{0·~:~0<idds support to the hypothesis that band deposition is related
in growth rates in adult sharks, combined with a
band deposit·1on rate, supports the hypothesis that bands
somatic growth.
Greg Pittenger (pers. comm.) has been
:cc-•··~~ growth rates of angel sharks greater than 800 mm TL
~California and finds that they lay down bands
33
and grow at a rate of 2.0 to 2.5 em per year.
These data
vlith data from my grow-out study (16. 2 mm/yr and more than one
ir per year), indicate that there is a change in band pair
tion rate.
It indicates that as the growth rate slows towards
ty, band depostion rate also' slows.
By studying growth rates in
sized individuals it would be possible to obtain size-specific
rates and to relate these back to band numbers to establish age
li~t,te,s.
This would also be helpful in detennining if bands are laid
size classes.
on gestation period, combined with data on size at birth and
at birth, indicate that band deposition is related to
already shown that band pairs are not formed annually
in embryos (see p. 29).
The 6 to 7 bands (Cailliet et
~·
approximately 10 month gestation period may
·~,,.~,-
due to the individual growth of the embryo.
ionship of rate of increase of girth to centrum size also
'~!•tile
hypothesis that band deposition is related to somatic
. area with the highest increase in girth corresponded with
,ji~~~~~all area and the areas of lower increase corresponded to the
de the plateau area.
centrum growth.
This shows a relationship between
Since band number increases linearly
(Figure 7), band number is also related to body
between band pair deposition and somatic growth
been documented in elasmobranchs.
In other
34
linr>nranc:u ageing studies that have been validated, band pair
ition has been found to be related to time.
Tetracycline has been
to validate the annual periodicity of band pairs in the lemon
{Negaprion brevirostris) (Gruber and Stout 1983), the leopard
(Triakis semifasciata) (Smith In press) and the thornback ray
clavata) (Holden and Vince 1974) and histology was used to
date the annual periodicity in the Japanese skate (Raja fusca)
yama 1951).
It has been hypothesized that the bands may be
ted on this annual cycle due to seasonal temperature, food,
ons and/or ion changes in the environment (Ridewood 1921, Jones
In the angel shark's situation, where band pairs
to be deposited relative to somatic growth, it is possible that
heavily calcified bands may be deposited to strengthen the
column (Ridewood 1921).
REPRODUCTION
!"<>1:12tsedon
indicators used in this study (clasper length increase,
~111~;~l!Eilrs, ~iOlffian duct coiling), the male angel shark beg.ins- to
1000 mm TL.
All the males in this study over 1030 mm
Males probably mature fully before this point, but
specimens between 865 and 1030 mm TL.
Males
low documented reproductive development in clasper length
and Raitt 1974) and wolffian duct coiling .(Pratt 1979).
collected at
·
.
var1ous t1mes of the year were all viable and
males may be h . 1
P YSlca ly capable of spawning all year
35
However, there may be other factors controlling the seasonality
n9·
The female angel shark begins maturing between 900 and 1000 mm TL.
to a lack of specimens between BOO and 1000 mm TL it was difficult
determine an accurate size when the ovary first begins to develop
when embryos first appear.
Fifty percent of the females have
and this is 0.7 of the maximum reported length.
5
fits Holden's (1974) generalization that maturity in female
asmobranchs is between 0.6 and 0.9 of their asymptotic length.
By
time the females have reached 1120 mm TL, 100% of them are mature.
The angel shark appears to have an approximately 10 month breeding
le. The definite periodicity exhibited by the females agrees with
IIJ,odd et
~-
's (1983) statement that viviparous species show strict
Parturition seems to take place between March and June and
probably occurs soon after.
to be season~l breeders.
Other species of Squatina are also
~- dumeril, from the Atlantic, is
to pup in June or July (Gordon 1956) and~- sguatina pups in
December through February in the Mediteranean
V£rcede:r and Rosen 1966).
11 pups was seen in one individual, and egg numbers
eggs could become ripe at one time.
The average
Pacific angel shark has been estimated to be
.and 13 (Pleshner 1983, P. Beguhl, pers. comm. ).
it'! run.
The number
seen in this study was probably low due to trauma-induced
2· dumeril has been reported to have up to 25
36
in one individual (Bigelow and Schroeder 1984, Gordon 1956);
high compared to the data on~- californica.
most elasmobranch species with only one functional ovary, the
is reduced (Dodd~~· 1983).
Observations on specimens of
dumeril have shown that only the left ovary is functional
and Olsen 1949, Haese 1962).
Observations on S.
that in most cases only the left ovary is
some cases both ovaries are functional.
lllioe:;e ( 1962) observed that the oviducts in two fema 1e S. dumeri 1
ned with a "cheesy" yellowish fluid.
angel shark.
r~,sri:nfor
This was also observed in
The "cheesy" substance was found to be yolk.
these yolk filled oviducts is unknown; however, they may
t resorption of unfertilized ovulated eggs.
DEVELOPMENT
Dll.l'd!lgthe approximately 10 month gestation, the embryo receives
from an external yolk supply as evidenced by the gradual
··ll.l('~!iEf:llfthis yolk supply over time.
There is a gradual sbifting
an internal sac which occurs after the embryo reaches
150 mm TL.
i~!!!!!:.!!i~
The internal sac which is also found in
is used as a storage area from which yolk is slowly
the intestine for final digestion and absorption
'Wourms 1977).
Angel sharks appear to be born between
TL, which agrees with observations from Cailliet et al.
37
ology of the embryos changes during development from a more
like" form to the adult form.
In the early embryo the jaws are
nal and the pectoral fins are small and non-winglike.
This is
r to the situation seen in the development of Chlamydoselachus
a subterminal mouth in the early embryonic stages
r 1940}.
In this stage, the angel shark embryo ressembles a
feeding shark.
The mouth gradually moves to the terminal
.on and the fins change to the wing-like form seen in the adult by
the embryo reaches 151 mm TL.
CONCLUSIONS
the three proposed hypotheses for band deposition rates in the
the best is that band deposition is related to somatic
than to time.
The results ·from the tetracycline-injected
''"''l:l""sharks conclusively show that band deposition is not
, or lunar in newborn sharks.
These results make it
hypothesis that band deposition is annual
Neither the cessation of band deposition nor
adults and/or at the tail are supported by results from
The length and band number data on
embryonic growth and bands, and the data on
and vertebral centrum dimensions, support the
band deposition is related to somatic growth.
female angel sharks start t o mature between 900 an d
n in the angel shark appears to be on an annual
38
Pupping takes place in spring and each female has an average of
s. Development is ovoviviparous and young increase in size over
h period from August to May.
39
LITERATURE CITED
o. 1963. Length and growth of the porbeagle (Lamna nasus
Bonaterre) in the Northwest Atlantic. Fisk. Dir. Skr. Ser.
Hounders 13(6): 54-72.
,gate, S.P. 1g67. A survey of shark hardparts. In: P.W. Gilbert,
Mathewson and D.P. Rall editors. Chap. 2. Sharks, 'Skates
and Rays. The John Hopkins Press, Maryland. p. 37-67.
·u.
•s, R.H.
1957. Notes on Western North Atlantic sharks.
1957(3): 246-248.
Copiea
1983. The forgotten requirement for
age validation in fisheries biology. Trans. of the Amer. Fish. Soc.
11Z(6): 735-743.
nish; R.J. and G.A. McFarlane.
W. and J. TeeVan; 1941. Eastern Pacific expeditions of the New
·~rk zoological society XXV. Fishes from th~ tropical eastern
ific (from Cedros Island, lower California, south to the
apagos Islands and northern Peru. Part 2. Sharks. Zoologica
15): 121-122.
;be,
H.B. and W.C. Schroeder. 1948. Sharks. In: Fishes of the
Mem. Sears Found. ~1ar-.-Res., Yale
rsity No. 1, Pt. 1 p. 59-546.-
'llo<:+o•·n North Atlantic.
and D.E. Rosen. 1966. Modes of reproduction in fishes.
History Press, Garden City, N.Y. 941 pp.
G.M., L. Martin, D. Kusher, P. Wolf and B. Welden. 1983a.
for enhancing vertebral bands in age estimation on
ia elasmobranchs. In: E. Prince and L. Pulos, ed'ftors.n~s, International Workshop on Age Determination of Oceanic
Flshes--Tunas, Billfishes, Sharks. Spec. Sci. Rep. Fish.
(in press).
·
G.M.,
•
L.K. Martin, J.T. Harvey, D. Kusher and B.A. Welden.
Preliminary studies on age and growth of blue (Prionace
• common thresher (Alopias vulpinus), and shortfin mako
sharks from California waters. In: E. Prince
_
rs. Proceedings, international Workshop on Age
S~~tlon of ?ceanic Pelagic Fishes--Tunas, Billfishes, Sharks.
1. Rep. F1sh.
N.M.F.S. (in press).
tl983. The sharks of North American waters.
Y Press, College Station. 180 pp.
Texas A & M
40
,dd, J.M., M.l-. :cctd and R.T. Duggan. 1983. Control of reproduction
in elasmo~·- ::~fishes. In: J.C. Rankin, T.J. Pitcher and R.
Duggan, e: ·:-~. ControlProcesses in Fish Physiology. J. Wiley
and Sons, : .. N.y. p. 221.
, rds R.R.C. _;:;J. Aspects of the population dynamics and ecology
,wa of' the wr··c ~:otted stingree, Urolophus paucimacul atus Dixon, in
Port p'hil- ·.: '::-~y. Victoria. Aust. J. Mar. Freshwater Res.
31: 459-!!:'-
:chmeyer, W.~-. o-~: Herald and H. Ham~ann. 1983. A field guide to
Pacific c:.-o: c1shes of North Amenca. Houghton ~1iffl in Company,
Bas ton. "-'~ :: ·
~rdon,
B.L. ·::-:.
2(2): 10~- ~~-
The amazing angel shark.
Bull. Int. Oceano. Fnd.
·uber s.H. 0 -: ·.o. Stout. 1983. Biological materials for the study
of age ar: ;-:•th in a tropical marine elasmobranch, the lemon
shark Ne::~-·Jn brevirostris Poey. In: E. Prince and L. Pulos,
edito~s-:-'--:::edings, Internatinal Workshop on Age Determination
:of Ocean~: c~·.lgic Fishes--Tunas, Billfishes, Sharks. Spec. Sci.
~ep. Fisr. UI.F.S.
(in press)
E.W.
:<.
The breeding habits, reproductive organs, and
development of Chlamydoselachus, based on notes
draw'·:;:; :y Bashford Dean. The Bashford Dean Memorial Volume
0
:
'shes. Article VII: 521-646.
ono"'"l ~-:·:.onic
W.L.
::.:~.
An investigation of the possibility of detennining
c' ;-::rks through annuli as shown in cross section of
rae. :~n. Rep. Ma. Lab., Tex. Game Fish Oyster Comm., Fiscal
1948<:.:9: 212-217.
19::. Fishes of the World.
p. ~>'l.
Doubleday and Company, Inc.,
.·-~-- Sharks and rays of Virginia's seaside bays.
pea,,· 3:i. 3(3): 166-172.
:~-~
Problems in the rational exploitation of
r.,-:- populations and some suggested solutions. In: F.R.
p, :~~~~~~:tor. Sea Fisheries Research. J. Wileyand Sons,
~"'""'!'
,,,,
Elasmobranchs In: J.A. Gulland, editor.
J. Wiley and Sons, N.Y. p. 187-215.
c Jynamics.
va·~w
7
41
,n M.J. and M.R. Vince. 1973. Age validation studies on the
·c~ntra of Raja clavata using tetracycline. J. Cons. Int. Explor.
~\ar. 35(1): 13-17.
,n M.J. and D.F.S. Raitt.
1974. Manual of fisheries science, Part
Methods of resource investigation and their application. FAD
Fisheries Technical Paper No. 115, revision 1.
-2~
yama, R. 1951. Studies on the rays and skates belonging to the
familY Rajidae, found in Japan and adjacent regions. 2. On the age
determination of the black-skate Raja fusca Garman (Preliminary
report). Bull. of the Japanese soc:-of Sci. Fish. 16(12): 112-118.
;;, B.C. and G. H. Geen. 1977. Age determination of an elasmobranch
(S{u)lus acanthias) by x-ray spectrometry. J. Fish. Res. Bd. Canada
34 1 : 44-48.
~~.
K.S. 1975. Age and growth of dogfish Sgualus acanthias in
British Columbia waters. J. Fish. Res. Bd. Canada 32(1): 43-59.
1955. Fish life in the kelp bed and the effects of kelp
IMR reference 55-9: 53-54,
Y.H. Olsen. 1949. The angel shark, Sguatina dumeril
New England waters. Copiea 1949(3): 221.
, D.P. Rall and J.E. Tobie.
'"'"eve ine antibiotics in bone.
1958. Fluorescence of
J. of Bone and Joint Surg.
897-910.
and R.N. Lea. 1972. Guide to the coastal marine fishes of
ia. Calif. Fish and Game, Fish. Bull. 157: 1-249. __ _
1972. Histochemistry, Theoretical and Applied, Volume
ill Livingston, Edinburg and London. Third edition.
1983. Fish of the month:
February, 1983: 55-60.
pacific angel shark.
Pacific
Jr. 1979. Reproduction in the blue shark, Prionace
Fish. Bull. 77(2): 445-470.
' 0 ~· Merriman and L. Calhoun.
1963. Studies on the
terces _on southern ~ew ~ngland. IX. _The biology of the
,NRaJa ~nnac.e~ ~\1tch1ll. Bull. B1ngham Oceanog. Coll.
at. H1st. Yale Univ. 18(3): 5-67.
42
On the calcification of the vertebral centra in
Phil. Trans. Roy. Soc. London, Ser. B.
W.G. 1921.
and rays·
311-407.
of the California coast.
p M 1953. Common ocean fishes
Fish
Bull. (91): 1-184p.
if:Dept. of Fish and Game.
,1974. Calcium metabolism of fish in relation to ageing.
T.B. Bagenal, editor. Ageing of Fish. Unwin Bros., Ltd.,
p. 1-12.
1984. Timing of vertebral band deposition and local
of tetracycline-injected leopard sharks (Triakis
tagged in San Francisco Bay. Trans. Alii. Fish. Soc.
~m;nt,s
~~i•n~
D.R. Nelson. 1977. A telemetric study of the
of free-swimming pacific angel sharks of southern
Bull. of the Southern Calif. Acad. of Sci.
1975.
;~~~~1~n
~
Vertebral rings as a means of age determination in
(Prionace glauca L.). J. Mar. Biol. Assoc. U.K.
Holden. 1964. The preparation and use of
age determination in rays. Inter: Coun. Explor. Seas,
Seas Committee, C. M. Pap. and Refs. (145): 1-4 p.
1943. Observations on later phases of embryonic
Squalus acanthi as. J. Morph. 73: 177-205.
1942. On Growth and Form.
p. 106.
Cambridge University
Calc~um and phosphorus in the blood and skeleton of
1.
,,.,•..,~
Endocrinology. 69: 778-801.
The .sharks and rays of California.
F1sh Bull. (45): 1-66 p.
l975~ .Vertebrate Dissection.
l!llpiany · hlladelphia. p. 45.
Calif. Dept.
Fifth edition.
W.B.
a~~d~~w~y. 0 196~. The deposition of tetracycline
Fish ~u~~ ~ f1sh and its possible use for marking.
ur1st 24(4): 150-155.
Reproducti
Zool 17 on and development in chondrichthyan
.
: 379-410.
43
J.H. 1974.
620 PP ·
~
Biostatise:al analysis.
Prentice-Hall, Inc., N.J.
44
TABLES
of histological centrum edge stages by month.
August
1982
July
1982
September
1982
October
1982
November
1983
Percent
June
1982
Stages
1&2
0.94
0. 75
0. 79
0
50
0
Stages
3 &4
0.06
0.25
0.21
0
50
0
N = 16
N=8
N = 19
N=0
N = 14
N= 0
-
210 mm TL - 860 mm TL
.,.
Stages
1 &2
0.92
0.89
0
0
100
0.62
Stages
3 &4
0.08
0.11
0
0
0
0.38
N = 36
N = 18
N= 0
N=0
U1
915 mm TL - 1170 mm TL
N= 1
N=8
characteristics of laboratory grown specimens.
Size
at
8 i rth
11285
#333
CSULB
254 mm
250 mm
240 mm
Number
of Bands
at Birth
5
5
5 - 6
Change
in
Size
+94 mm
+162 mm
+50 mm
Change
in
Band #
+5
+8
+2 - 3
Time
Alive
6 mo.
13 mo.
11 mo.
Number of
Band Pairs/
Month
0.83
0.61
0.18- 0.27
mm/ Band Pair
19
20
25 - 17
en
""'
47
FIGURES
alternate
length
\
:-girth 1
..,.
00
Jlliilliill/11~
111111 ~llllllllllllllllllllllllllllllilllllllllllllllliillil~liliiililliiiilll~ill!llililli~ l ~
1214
22
74
93 107 .,...
I
I
o
.d.A
(til~·tttl
1 em
FIGURE 1.
Diagram of Sguatina· californica sh01·1ing locations of five measurements.
The first 107 vertebrae in the vertebral column are shown to exemplify
the change in vertebral size along the column of an adult specimen. These
vertebrae are 25% of their original size.
~3
b
.-: ..:---:-.'~~,
,.,.
II~;3Ff:¥~§~t~~+~~rR
- ·- - -
'-
7
.c/<
,-) { ;_r ---7>
5
,;;x Liil'
10-15
1-1
/~\<"':;
c
;>
i(
/''
"
FIGURE 2.
mm
.. ·.:,::.:'l
F
·='·"·~<
co
""'
"
7
10-15
1-1
Diagrams illustrating the axes along which histological sections were cut. a) initial
trimmjng of edges in longitudinal plane. b) position of final longitudinal cut
through the center of the centrum and resulting section. 'c) cross section and
resulting section.
50
FIGURE 3. Histological sections of the
centrum edges of four specimens of
Squatina californica. Each picture
shows one of the four stages of band
development used as a standard to judge
edge revel opment. Stages 1 and 2 represent translucent band development and
stages 3 and 4 represent opaque band
development. Photos were taken at 40x
with an Olympus photomicroscopy
system.
51
J{
/~
c--B~APOPHYSIS
«~~ ~
c~
'---- "---"'
12
12 1
(CJ)
lcm
FIGURE 4.
Drawings of head, trunk and tail vertebrae
showing the differences among the vertebrae
from different areas. A and B are from the
head end. C and D are from the trunk. E
and Fare from the beginning of the tail.
G, H, and I are from the tail.
52
a
16
a
7
14
6
12
I
'-
"'
.a
E
5
z
4
I
I
I
I
I
"0
c:
10
1-----------
a
~
a
:l
E
Ill
2
.
!r
4
1
2
0
0
b
\
~--
--,
14
\
I
\
24
"'
.a 22
E
12
\
I
I
I
I
'-
I .
•-,
\
' ' \ ___
J
10
'
a
\
I
-
.<::
18
~
E
I
c:
"'
E
E
"0
\
20
,...
~
"0
Ill
"'
<.:l
16
26
:l
'-
c:
28
z
.<::
"0
I
31
"'
E
E
~
--- -----------------------
:l
~
'
16
6
t\
\
I
\
\
,,
//
I
\
\
4
-"'
:l
. '-
c:
<.:l
I
I
I
'/
14
12
0
a
16 24 32 40 48
56
64 72
so
2
0
88 96 1.0 4 112
Centrum Number
FIGURE 5.
Graph depicting the relationship of band number
and centrum width with centrum number of every
fourth vertebra along the vertebral column of
a) a 225 mm TL specimen, and b) a 850 mm TL
specimen.
1200
...
• •_'§A?•
•
1000
~
E
E
.......
-
•
800
.c
Ol
c:
•
600
••
Ql
...1
<1l
N • 33
Y= 54.55X + 36.16
r2• 0.99
•
400
0
1-
<.n
w
200
0
0
2
4
.6
8
10
12
14
16
18
20
22
Centrum Width (mm)
FIGURE 5.
The relationship between centrum width and total length using only the number
12 - 14 vertebrae.
•"
..
• •
35 4
.. .
•
..............
30
i
.....
E 20
:::l
z
~
•
c
l1l
Ill
N • 30
Y•1.45X + 3.78
. r 2 • 0.92
/
10 -1
I
_,
<.n
/-
151
5
..
... .ve
I
"0
" •
..
/
251
<ll
.0
•
/
/
1
0
2
4
8
8
10
12
14
16
16
20
Centrum Width (mm)
FIGURE 7.
The relationship between centrum width and band number using only
number 12 - 14 vertebrae.
55
40
Sguatina Californica
.._.«>"'
. "'" .
{: o·
30
25
•
l
•
•••
~
•
•
•
•
J
•
••
•
• •
•
•
•
•
•
•
•
•
•
20
•
Jl
~
•
•
0
Ul
•
•
),
~
+"
-I. OJ".>
35
15
I:
•
N=111
r 2 =.85
•
10
5
5
10
15
20
25
30
35
40
Radiography Band Counts
FIGURE 8.
Relationship of histology band counts to radiography band
counts from the same specimens.
56
Male
.. .
a
00
200
400
600
800
1000
1200
15
12
Female
,....
0>
.:i.
9
'-'
...
.c
0>
'i
~
.
6
•
b
3
0 o~~--7
2o~o~~~400~~L--s~o~o~~--a~oo___ L_ _1~oo~o--L--,~2~oo~J
Total Length (mm)
FIGURE 9.
The relationship between total length (mm) and weight
(kg) for a) ~u u.ale angel sharks, and b) 68 female
angel sharks.
57
600
y-0.457x+4.430
~
E
E
~
N~13
500
400
~
-
J::
300
~
CJ
200
•
100
GIRTH 1
~
E
E
~
CIJ
-
300
y-0.267x-26.9708
•
N=13
200
J::
~
100
GIRTH 2
CJ
~
E
E
~
"'
J::
~
300
y-0. 1 7 5 1 X -3 3. 56 7 5
200
N=13
100
•
CJ
0
200
400
600
GIRTH 3
1000
1200
T.ot al Length (mm)
FIGURE 10.
The relationship between girth (mm) and total lengths for
13 angel sharks with associated linear regressions:
a) Girth #1 - under the pectorals;
b) Girth #2- above the first dorsal;
c) Girth #3- below the second dorsal.
58
Male
•• •
.. . ... .. ... . . .
..
:
a
10
Female
)0
•
00
00
.•
..
00
.oo
... ~
!00
•
: l : .
...
l·:t:i'
. .
... .. .
•
N=87
b
0
0
URE ll.
10
20
30
40
Band Number
The relationship bet1'een total length (rrm) and number of
bands for a) 56 male, and b) 87 female angel sharks.
59
FIGURE 12.
Photograph of tetracycline mark (arrow) and
subsequent band growth to the left of the mark
of specimen 00951. Photograph was taken using
an Olympus photomicroscopy system with a
dissecting microscope. Lighting was provided
by a U.V. light source.
400
~
E
E
350
~
.J::
"5
c
"'
..J
-
(ij
0
300
TQ
I
1-
~+285
en
..__.+333
I
250
200
J
/
u
April
0
_.:/
!
k
2-41
June
I a
30/2
August
:udl-<~ 1 21
lr
October
:zal
b. te:z43de
December
1983
13
Ia
February
:zo/
115·
I
21!
April
1984
Date Measured
FIGURE 13.
Growth of laboratory grown specimens #285 and 333.
is indicated by arrows.
Time of tetracycline injection
61
FIGURE 14.
Photograph of the number 10 vertebra from specimen number 285
showing tetracycline mark (arrow)
and three opaque bands outside of
the mark.
62
FIGURE 15.
Photograph of the number 12 vertebra from specimen
#333 showing tetracycline mark (arrow) and seven
bands outside of the mark.
700
600
......
E
E
~
_.... __.. ...... ~- ......
500
.- ... -~.--....- _...... -
.<:
.....
.......--... -~--~_.
-
CJl
c
Ql
_J
l1l
.....
400
300
0
1())
,___. months 1-12: 13.54mm/mo
200
w
.,. - .... months 12-24: 11.20mm/mo
100
0
0
2
4
6
8
10
12
14
16
18
20
22
24
Number Of Months Since Birth
FIGURE 16.
Curve depicting mean growth in TL (mm) of captive angel sharks with the
solid line repr senting the first year of life of 2 captive angel sharks,
and the slashed line representing the growth of one shark for the second
year of life.
64
250
I
I
I
•
I
•
•
I
•
•
I
-
1-
'E
E
";::-
200 1-
.. .
...'=· :
..
p
1-
Q)
c
c 150 1.::::;.
s::.
.....
Ol
c
.3,_
1-
100 11-
Q)
a.
Ul
0
13
. •..• ...
.
•
_a.
. •....·.
50 11I
00
I
400
200
100
I
•
.;.
a
I
600
I
..
I
800
I
I
I
•
1-
....:I
Q)
0
'-'
.r::.
....
Ol
cQ)
...J
I..
Q)
.,0..
0
13
I
I
1000
1200
•
I
80 11-
-
60 11-
40 11-
20 1-
I
. ..·-.. -·.c. : •
1-
..
..
.
b
• •
I
I.
200
I
I '
400
L
I
600
I
-~~
800
~-'-
_l
1000
•
1200
Total Length (mm)
FIGURE 17.
-
-
I
00
-
I
....
....:..·..
....•
r-.
E
E
';::-
-
The relationship of a) inner clasper, and b) outer
clasper i;o;;gt~c. (il111) and total length, (mm) of 71
and 72 male angel sharks, respectively.
80~
I
I
I
I
I
I
I
I
I
I
I
I
,.-...
E
E 60t
..._..,
..-
•
.....
.. I
I
II
(j)
.....(j)
E
0
0
D>
D>
w
401-
.
•
•
.....
CJ)
(j)
D>
.....
0
-
.. .. ···-··
. ·-··
20
0
0
0
-
0
l
-
_.J
~
0
200
400
600
800
1000
1200
Total Length (mm)
FIGURE 18.
The relatjonship between total length {mm) and largest egg
diameter (mm) for 75 female angel sharks.
())
U1
66
a
5
>- 4
0
c: 3 <D
:::J
0'
<D
2
-
1
-
N=14
-X
t
-
I...
u.
1
2
3
Number
4
0~
I
5
6
7
8
9
10
11
I
I
12
Females With Eggs, ,.35mm
X
J
5
b
'
4
>0
c: 3
<IJ
:::J
0'
<IJ
-
2
-
1
-
I...
u.
-
1-1
2
3
4
5
6
7
8
9
10
11
'
Number Of Embryos In Both Oviducts
FIGURE 19.
Frequency histograms of a) the number of embryos in
both oviducts, and b) the number of eggs (>35 mm in
diameter) i11 both ovaries. Arrows indicate the mean
for each gr.lf'h.
32
.....
250
.c
.....
200
E
E
.._.
i
22
T
Ol
Q)
118
...J
L.
..a
E
w
l1l
100
Q)
~
r
150
>.
c
9
f
t
2
21
c
0
-
3
_,._
l
60
t
f's-x.o.
N•number of embryos
1
I
_..range
4
0
N ( !j!' B)
A
1
s
0
0
17
N
3
D
J
0
1
F
4
M
7
A
0
M
1
J
0
J
2
Month
FIGURE 20.
Relationship of mean embryo length (mm) in pregnant females to month for
samples taken in 1983.
en
"
68
.. , ....
.
FIGURE 21.
..:...·-:
. ..
~-..::. ~·
·.:·
..;
.
Three view of a 35.40 mm TL embryo. Note
the subterminal mouth, protruding eyes, and
external gill filaments. Picture was drawn
using a Wilde camera lucida at 60x.
69
co
I
0
~~
S-.0
.oE
E w
w
---'
~~
E E
E
N
............
..... ......
"' "'
4-4-
<(
0
0
en en
<= <=
....... •r-
3
3
"''- "''-
00
I
~~
<>::
N
N
w
"'
:::0
'-"
~
LL
""
70
B
A
FIGURE 23.
A)
B)
Drawing of a 151 1TUll TL embryo.
Drawing of a 175 mm TL embryo.
71
connection of
internal yolk
to yolk stalk
liver
internal
yolk sa
connection
of internal
yolk sac to
intestine
cloaca
intestine
..
FIGURE 24.
Ventral viev1 of the internal organs of an embryonic
angel shark.