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California Fish and Game is a journal devoted to the conser-
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JULY 1968


Published Quarterly by







NORMAN B. LIVERMORE, JR., Adminisfrator


WILLIAM P. ELSER, Presidenf, San Diego

JAMES Y. CAMP, Vice Presidenf C. RANSOM PEARMAN, Member

Los Angeles Huntington Pork


Redding San Francisco



1416 9th Street
Sacramento 95814

Editorial StafF

LEO SHAPOVALOV, Editor-in-Chief Sacramento

ALMO J. CORDONE, Editor for Inland Fisheries - - Sacramento

WM. E. SCHAFER, Acting Editor for Inland Fisheries - -. - Sacramento

CAROL M. FERREL, Editor for Wildlife _. - Sacramento

HERBERT W. FREY, Editor for Marine Resources — - - - Terminal Island

DONALD H. FRY, JR., Editor for Salmon and Steelhead Sacramento


Retirement, -/. B. Phillips 132

The Embryology of the English Sole, Parophrys vctulus

James J. Or si 133

Organogenesis in the Walleye Surf perch, Hyperprosopon arfjenienm
(Gibbons) Paul C. Engen 156

Eeeords of Some Native Freshwater Fishes Transiilanted Into
Various Waters of (California, Baja California, and Nevada

Robert Rush Miller 170

The Aquatic Oligocliaeta of tlie San Francisco Bay System

Ralph 0. Brinkhurst and Mary L. Simmons 1 80

Jack Mackerel Yield Per Area From California Waters, 1955-56
Through 1963-64 /. M. Dujfy 195


Intestinal Growths in the European Flat Oyster, Osfrca eehilis

Stanley C. Katansky 203

Fecundity of the BroAvn Eagfish, Icosteus aenigmaticus Lockington,
From Northern California George H. Allen 207


The 1967 Shark Kill in San Francisco Bay

Ronald A. Russo and Earl S. Herald 215

Northern Range Extension for the Kelp Bass, Paralahrax cla-
thratus (Girard) Michael J. Hosie and Carl E. Bond 216

Northern Range Extension for the Yellow Crab, Cancer anthonyi

Mel Willis 217

Book Reviews 218


Tomlinson. Patrick K. Mortality, growth, and yield per recruit for I'ismo clams.
54(2) : 1(X)-107, 19G8.

The formula near the bottom of i)a,i;e 101 should be

M = -4\oge{N,/No)

and the formula at the lower left corner of Table 1, page 102 should read




Tlie Depart liiriit lost one of its most esteemed employees when Julie
Pliillips retired on May 1, 1968. The extent of the regard in whidi he
was held is well demonstrated by the action of the State AssiMiibly
Kules Committee whicli adopted this resolution prepared by tlie lion.
Alan G. Pattee, assemblyman of the thirty-fourth district in wiiicli
•hilie lived:

AViiEKEAS, Mr. Julius B. Pliillips, Marine Biologist of the
Department of Fish and Game, will retire on May 1, 1968,
after a career of dedicated service to the people of Califor-
nia ; and

WiiEKEAS, Julius B. Phillips entered state service on August
6, 1928, as a deputy, and was appointed a fishery biologist in
1929 at Pacific Grove, a research zoologist in 1931, an assistant
aquatic biologist in 1945, and an associate marine biologist in
1947 ; and

Whereas, During the past four decades he has continued to
serve the people of Pacific Grove, jMonterey County, and the
entire state in these capacities, and in others, Avith great dis-
tinction, dedication and integrity ; and

Whereas, His scientific studies and publications on tlie im-
portant marine resources of this state, most notably those on
roekfish aiid sardine, have earned him a worldwide reputation
and brought great credit to the State of California ; and

AVhereas, Over this period of four decades his friendly
counsel, unassuming attitude, quiet manner, and devotion to
duty have earned him the respect of all those who came in con-
tact with him ; and

Whereas, Julius B. Phillips richly deserves the pleasures of
retirement by his significant contribution to the conservation
of tlie marine" resturces of this stat(>; now, therefore, be it

Frsolrrd hii the AfiscmhUi Rules Committee, That the ]\Iem-
bers (•(iiiihicihI .lulius 15. Pliilli])s on llic occasion of his i-etii'e-
ment and express their sineere thanks for his important con-
tributions to the wi>lfare of the marine resources of the state;
and be it further

Resolved, That the Chief Clerk of the Assembly transmit a
suitably prepared copy of this resolution to Julius B. Phillips.

There is little we in the Department can add to this tribute save to
exjiress our own feeling of loss at his departure and to wish him and
his wife a long and happy retirement. — /'. M. Roidcl.

( 132 )

Calif. Fish and Game, 54(3) : 133-155. 1068.


Delta Fish and Wildlife Protection Study
California Department of Fish and Game

Mature fish were artificially spawned and the eggs incubated at
10.6 C ± 0.4 C, and the larvae were raised in 2-liter beakers or quart
jars at the same temperature.

Egg samples were preserved and sectioned to study changes not visible
in living material. Photomicrographs were taken.

The unfertilized eggs average 0.98 mm in diameter. They are trans-
parent and spherical, lacking oil globules and pigment. They have nu-
merous small oil droplets and the surface of the egg membrane is
pierced by many small pores and is thrown into fine ridges.

Fertilized eggs average 0.99 mm in diameter. They have a very small
perivitelline space, a thickened fertilization membrane, and float with
the animal pole down. Early cleavages conform to the typical teleost
pattern. They begin 2 hours after fertilization and continue at 1-hour
intervals. No segmentation cavity exists because the periblast adheres
to the lower surface of the blastomeres. Gastrulation begins at 25 hours
and produces a Ittrge subgerminal cavity. Blastopore closure is ot 48—49
hours, when the eye vesicles, olfactory sacs, neural cord, notochord,
KupfFer's vesicle, and 11 somites have formed.

An unusual caudal vesicle arises at this time and becomes located
behind Kupffer's vesicle. Its history end significance in P. ve'fulus is dis-

Hatching begins at 98 hours and continues for 10 hours more. Newly
hatched larvae are 2.85 mm TL, have unpigmented eyes, and float with
the yolk sac up. Eye pigmentation is completed bet>veen 6 and 9 days.
The yolk sac is absorbed at 9 or 10 days, and an average length of 4.6
mm is reached between 9 and 12 days. In the absence of food, the last
surviving larvae die at 14 days.


Few detailed embryologies of teleost fishes have been written. In addi-
tion, sometimes omissions and involved discussions make it difficult for
the fisheries biologist to obtain a clear picture of teleost development.
Nelsen (1953) and Balinskv (1965) describe the embryologies of all
vertebrate groups, but their treatment of teleosts is sketchy. Tlierefore,
I decided to trace the development of all the organs of a teleost fish to
hatching and to describe the appearance of the larvae until the yolk was

I chose the Englisli sole, Parophriis vetulns. because it was easily
obtained and spawned and, aside from the pelagic adaptations of its
eggs, appeared to be relatively unspecialized embryologically. A brief
description of this species' embryology has been published (Budd, 1940).

1 Submitted for publication August 1967. Revision of Master of Science Tliesis, Uni-
versity of Wasliington, College of Fisheries, 1965.




Eipe Eiifrlisli soles were otter trinvlcd Iroiu I'uget Souml. \V;isliing-
ton, from January to IMareli of ]9(i4 and 1965 by the College of Fish-
eries vessel 31 V Commando. The fish were held in an aquarium until
spawned (usually 1 to 3 days).

The egfrs from two or three females were spawned into a (|uart jar of
sea water and fertilized immediatel\' hy s])erm from one or two males.
After 5 minutes, the eontents of the jar were decanted into an incubator
(a glass funnel or quart jar). Approximately 200 ('<zgs were ])laced in
the jars and 1,000 in tlie funnel. The latter, with a mouth diameter of
1 foot and a capacity of 5.9 liters, was tilled with '1:1 liters of \vater and
floated in a 2()0-gallon tank. A plastic ring with a ])iece of plankton
netting sewed over it was fitted inside tlie fuiniel well below the surface
of the water to prevent the loss of living eggs when the water was
changed and to catch dead eggs when they sank. Water was i-eiiioved
through a plastic hose connected to the neck of the funnel and replaced
by pouring, which also provided some aeration.

The water in the quart jars was neither changed noi- aerated. This liad
no apparent ill effect on the eggs.

A constant circulation of water in the 200-gallon tank kept the tem-
perature at 10. 6C ± 0.4C during incubation.

The larvae were raised in 2-liter beakers or (|uai't jars float iiig in the
tank with the eggs, at the same temperature, and in semi or total dark-
ness. There were approximately 50 larvae in each jar and 100 in each
beaker. No attempts were made to insure their survival otiier tlian giv-
ing them an initial sujiplj" of clean water.

Three hundred and fifty living, unfertilized eggs and 100 li\iim- fertil-
ized eggs from 14 females of varying sizes were measured with a filar
micrometer. Newly hatched larvae Avere also measured with a filar mi-
crometer. For older larvae, an ocular micrometer on a dissecting nncro-
scope was used. Twenty-five larvae were measured at each stage, unless
otherwise noted in the text.

I preserved 10 to 20 eggs hourly until the formation of the germ ring.
After this, I took samples at 2- or 3-hour intervals until hatcdnng.

Stockard's solution was used as a preservative, since it caused much
less distoi-tion and shrinkage than the usual 5% formalin. I i'eiuo\-ed the
yolk and egg membranes with microneedles, end)edded the germ tissues
in paraplast, sectioned them at o^u,, and stained them in haemato.xylin
and eosin.


Unfertilized Eggs

The unfertilized eggs of the English sole are t rans])arent. spliei-ical.
lack oil globules and pigment, and average 0.98 mm (0.!ll-1.04i in
diameter. When first extruded, they float at the surface but if not fei'tii-
ized within 15 to 30 minutes, usually sink to the bottom.

The eggs faintly resemble a ball of yarn because of numei-ous low
ridges traversing their surfaces. These ridges vai-y considerably iu ap-
pearance and concentration. In general, the ridges, wliich are folds of
the zona radiata or o^;:^ membran(\ are short and straight or slightly


curved and run at rio:ht angles to the egg equator. Tn some eggs, the
ridges appear eross-hiitelied, while in others they are nearly absent.

The egg membrane is pierced by many fine pores, arranged in a regu-
lar, even pattern. In the cytoplasm beneath the egg membrane are many
small clear oil droplets of varying sizes, linked into roughly circular,
anastomosing chains. Just below these chains are a few scattered drop-
lets, twice as large as tlie biggest ones above them.

Even in the unfertilized egg, the cytoplasm can be seen as a thin layer
ensheathing the yolk, and a small blastodisc with a micropyle already
has formed at the animal pole. Tlie micropyle is a sliallow depression
0.032 mm in diameter, and only slightly deeper than the egg membrane
is thick.

Fertilized Eggs

Fertilized ova average 0.99 mm (0.93-1.05) in diameter. These meas-
urements are greater than those from California fish (Budd, 1940),
wliicli averaged 0.9 mm (0.89-0.93).

Tlie eggs float with the animal pole, the region of the forming blasto-
disc, downwards. After fertilization, no changes take place in the sur-
face ridges or in the oil droplets, but a perivitelline space appears, and
the egg membrane thickens and becomes the fertilization membrane.

The perivitelline space of the English sole is very small. It is widest
near the edges of the blastodisc, becomes gradually thinner toward the
egg equator (Figure 2A), and virtually disappears at the vegetal pole.

Budd (1940) attributes the formation of tlie perivitelline space to the
compression of the yolk by the forming blastodisc. The present theory
(Kusa, 1956; Yamamoto, 1962) states that the cortical alveoli (spheres
10-40;u. in size, located in the cytoplasm) break down on fertilization
and release a hydrophilic colloid (a polysaccharide). The high osmotic
pressure of this colloid causes the uptake of Avater, usually from the
cytoplasm (more rarely from the environment), and this separates the
fertilization membrane from the cytoplasm and fills the perivitelline
space. If the cytoplasm contributes the water, it shrinks, but the eleva-
tion of the fertilization membrane increases the egg diameter. I do not
know the source of the perivitelline fluid in P. vetulus, since I never
observed an egg at the moment of fertilization. Such observation is nec-
essary, because any loss in cytoplasm volume would be slight and diffi-
cult to measure.

The egg membrane tliickens when some of the material expelled from
the cortical alveoli fuses with it (Rothschild, 1958). This causes the
water hardening of the egg. Tlie resulting fertilization membrane in the
English sole is three times as thick as the original. It is divided into two
parts : a thin outer layer, the former zona radiata, and a thicker inner

Early Cleavage

The yellow-tinted blastodisc slowly increases in size from its ])re-
fertilization condition witliout visible streaming of cytoplasm. Tlie
whitish yolk underlying the blastodisc changes in shape as the cyto]>lasm
accumulates above it. A saucer-shaped depression appears in it, be-
comes progressively larger, and then fluctuates in size.

At the onset of cleavage, 2 hours after fertilization, the blastodisc has
increased from one-twentieth to one-sixth the diameter of the egg and


the yolk dcpi-cssid)! ]i;is (lis;ip|)c;ii-c(l. 'I'lir l)lastodise 's sides are genci-jilly
smootli antl flow <rra(lually into tlic protoplasm siirroini(lin<r the e<j:<>:.
Tlie first C'loavap:(> furi-ow bcjjfins in llic ci'iitcr of the blast odisc's top.
Next, a sceoiidaiy furrow arises on llir liuitdin of tlic blastodisc and
forces till' foriiiiiitr blastomeres to aidi upwin'ds. 'I'liis secoii<lai-y fui'i-ow
diminislies and disappears as tlie primary one cuts tlii'on<rIi ; it dors no
actual cleavinu'. The blastomeres do not separate comjdetely. A strand
of prot()])lasm unites tliem at their bases and more ])i-otoj)lasm remains
around them (Figure 2A). This forms the periblast.

As eleavagfe progresses, the sides of the blastomeres become more dis-
tinct and rounded. This process continues after tlie furrow has been
completed. I used the rounding up of the blastomeres as a critei'ion for
the completion of this and subsequent stages. At a temperature of 10. 9C
the tAvo-cell stage requires 20 minutes for completion.

The second cleavage furrow begins 3 hours after fertilization. Placed
at a right angle to its predecessor, it starts in the center of both cells
simultaneously and proceeds outwards, inwards, and downwards. It
reaches the first cleavage furrow before it touches the outer edges of
the blastomeres. A secondary furrow also exists in this stage.

The four blastomeres are flat on their inner sides (those touching
each other) and round on the outer edges. They are elongated in the
direction of the second cleavage furrow and are undercut so that they
jut out a bit over the periblast, which swells underneath the margins of
the cells. It takes 14 minutes to complete this stage at 10. OC.

The eight-cell stage begins 4 hours after fertilization and is complete
10 minutes later. Four furrows arise on the outer edges of each blasto-
mere at right angles to the second cleavage furrow and cut inwards.
The elongation of the blastomeres, noted in the four-cell stage, persists
in this stage as an elongation of the blastoderm and small oil droplets
can still be seen over and around the blastomeres. They are apparently
carried to tlie blastodisc by the migrating cytoplasm.

Tlie fourth cleavage begins 5 hours after fertilization. The furrows
run at right angles to the third cleavage furrows and hence are parallel
to and on either side of the second furrow. Cleavage is not sinudtaneous
in all cells. Approximately 8 minutes is required to form the Kl-eidl
blastoderm. Tins blastoderm is still slightly elongated, aitliough dif-
ferent blastoderms vary considerably in shape. Some 16-cell blasto-
derms are well rounded up or even square.

In another hour, the fifth cleavage forms the two-layered 32-cell
blastoderm. The 4 central cells of the l(i-cell group cleave in the hori-
zontal rather than the vertical plane, creating a core of eight cells,
around Avhich the remaining 24 cells are grouped in a single layer.
Sometimes, the corner cells of the 16-cell blastoderm divide inei-idi<tnally
and the others split parallel to the sides of the blastoderm. I'sually,
however, the cleavage planes are irregulai* ami dillicult to determine.


Focusing through the blastomeres, the ])eriblast emei'ges as a dark,
irregular i-ing uiuler and around the ])ei-ipheral cells of the blastoderm.
It cannot be seen under the central cells in living eggs; however, in
sections the periblast continues under the central cells as an extremely
thin strip, which explains its invisibility in living material.


The periblast adheres to the bottoms of the blastomeres and the mar-
ginal blastoderm cells are eontiimons with it.

In time, the central, subblastodermic periblast thickens and nuclei
appear on it. Nuclei also appear in the peripheral, extrablastodermic
periblast (Figure 2F). They are derived, at about 10 hours after fer-
tilization, from the breakdown of the marginal cells of the blastodermal
cap. At this time, the edges of the cap are broken and irregular. Small
tongues of cells stretch into the periblast and occasional isolated cells
or cell clusters are adrift in it. Sections reveal that the marginal cells
have lost their lower boundaries.

The marginal cells contribute nuclei to the periblast until shortly
before gastrulation begins ; at this time the connection between the
marginal cells and the periblast is severed. If the connection persisted,
cells attempting to invaginate over the blastoderm lip would either be
blocked by the i:)eriblast or would carry it along with them.

Initially, the elongated periblastic nuclei are strewn haphazardly
about. Later, they form as many as 6 rings around the blastodermal
cap (Figure 2F). These nuclei become extremely large, rivalling the
blastomeres in size. Their function is to metabolize the yolk to provide
material for the grow'th of the embryo (Balinsky, 1965).

Blastodermal Cap

Continued cell multiplication transforms the 32-cell blastoderm into
the many celled and layered blastodermal cap. Although the number of
cells greatly increases, the size of the cap does not. It reaches a maxi-
mum height of approximately 10 cells at 15 hours and resembles a dome
resting on the yolk. Its cells are polygonal, with the exception of the
roofing layer of apithelial cells which have begun to flatten out (Figure
lA). After 15 hours, the cap hollows out in the center and becomes
concave on the yolk side (Figure 2B). It pulls away from the fertiliza-
tion membrane and spreads a short way down over the yolk surface.
The blastoderm center is reduced to half its original thickness by 25
hours and the epithelial layer is complete. Now the germ ring forms
and invagination begins.

Subgerminal Cavity

Up to this point, no space exists between the blastomeres and the
periblast. The periblast clings to the blastomeres even when the blasto-
derm's undersurface becomes concave. Shortly before invagination,
small scattered spaces gape o]ien between the two tissues and they
become very loosely connected. The invaginating tongue of cells thrusts
under the blastodermal cap and pushes the periblast in front of it away
from the blastoderm. In a short time, periblast and blastoderm are com-
pletely separated over the entire central region of the blastoderm, even
where the invaginating laj'ers have not penetrated. The late segmenta-
tion or subgerminal cavity so formed is shallow and ends at the invagi-
nated cell plate, to which the periblast firmly adheres.


Gastrulation transforms the small, single-layered blastoderm into a
larger, multi-layered embrjo. This is accomplished by two simultaneous


processes: inva^'iii;it ion inul cpilxily. I ii\ ;iL;iii;i1 Idii hkixcs cells IVdiii llic
exterior to tlir iiilci-ioi- of the hl.islodcnn lo foi-in the mull i-l;iycred
embryo. \\y i'|)ibol\'. the blaslodcrm ovci-y-rows the yolk. Il ciiiiblcs the
cmbi-yo to rcjicii a greater size lliau it could if restricted to the ai'ca
around t lie animal i)ole.

lu preparation for uast rulat ion. the cdu'c of the bbistodcrni becomes
thicker than tlie central re;^ion. This I'iny- of cells is calli'd tin- rand
u'ttlst (Fi^'ure lA). Gastrulation begins when blastotlerm cells roll over
the blastoderm edge and grow inward from the iinier tip of the raitd
ickIsI. The starting point f(»r this ingrowth is tlie dors;d lip ol' the
blastopore fthe future ])ostei'ior end of the embryo). The |»i'e\iously
mentioned hollowing of the blastoderm leaves one half thicloM- than the
other. The midpoint of this half becomes the doi'sal li|). Invagination
then oceui's all aronnd the circuiiif<'rence of the blastoderm, creating a
zone of invagination termed the gei-m ring (Figure 2('). Looking at the
blastoderm from below during early gastrulation, the inner edge of
the newly formed germ ring is visible aronnd the blastoderm (Fig-
nre 2F).

The dorsal lip of the blastopore is the main as well as the initial
point of invagination. From it, the overwhelming bulk of the embryo
is derived. A second gateway for ingrowing cells is the blastopore's
ventral lip (Figure 2C), which furnishes a small amount of matei-ial to
the tail at blastopore closure. Invagination at other points produces
only the germ ring.

The invagination at the blastopore's dorsal lip becomes a broad
])oiii1ed plate of cells that moves inward between the ])eriblast aiul tlu'
blastoderm, folloAving the curve of the blastodei-m over the yolk. This
plate is one cell thick at its tip and two cells thick at its b:ise. Tlu' long
axes of these cells are ])arallel to their direction of growth and ai'c at
right angles to the axes of the blastomeres above them.

As tlH> invaginated cells migrate toward the future anterior end of
the embryo, the germ ring moves in the opy)osite direction and sjireads
down the yolk, covering it with a single-celled sheet of ectoderm.

The broad plate of invaginated material and the thickened ectoderm
above it are termed the embryonic shield (Figure 2C) ; around it are
the thinned-out extra-embryonic areas. Endoderm and mesoderm arise
from the invaginated cells; ectoderm and neural ectoderm arise from

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