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University of the Pacific Theses and Dissertations Graduate School

1973

Larval development and life history of Phyllaplysia taylori dall (Opistobranchiata: anaspidea)

Cecilia Blackwell Bridges University of the Pacific

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Recommended Citation Bridges, Cecilia Blackwell. (1973). Larval development and life history of Phyllaplysia taylori dall (Opistobranchiata: anaspidea). University of the Pacific, Thesis. https://scholarlycommons.pacific.edu/ uop_etds/1798

This Thesis is brought to you for free and open access by the Graduate School at Scholarly Commons. It has been accepted for inclusion in University of the Pacific Theses and Dissertations by an authorized administrator of Scholarly Commons. For more information, please contact [email protected]. LARVAL DEVELOPMENT AND LIFE HISTORY

OF PHYLLAPLYSIA TAYLORI DALL

(OPISTOBRANCHIATA: ANASPIDEA)

A Thesis

Presented to the Faculty of the Graduate Sc_hool

University of th~ j?q.cific

In Partial Fulfillment of the Requirements for the Degree

Master of Science

------

by =-=-----

Cecilia Blackwell Bridges

June 1973

.. This thesis, written and submitted by

Cecilia Bridges

is approved for recommendat1on-tcf~-tne~--- ~~--~--~- ~------~-

Graduate Council, University of the Pacific.

Department Chairman or Dean:

1besis Committee:

:y-, ~Chairman

Dated ____J~un~e::::..._, --=.19;;..7L3.2.- ___ CONTENTS

ACKNOWLEDGEMENTS . . . . . • • • • • • • • • • • • i

LIST OF TABLES • • • • • • • . . • • • • • • • • • ii

LIST OF FIGURES ...... •. . • • ·iii

INTRODUCTION ...... • • • • • • 1

~ iiD1,1JGY~OF-PHYI.;LltPI.;YSTA~TA-'iLOR.i'---.-.--.------~• "------~ ------Review of Previous Studies . 2

General Biology 3

Larval Development 5 Methods and Materials 5 Results ...... 7

l. Egg Mass •...... 7 2. -Early Development . . . . 9 3. Organ Morphology to Metamorphosis 10 a. Velum ...... 10 b. Foot . . . . . 13

c. Shell Gland . . . . • . . . 14

d. Excretory Organs . . . . • . . 14

e. Statocysts ...... • . 17

f. Alimentary System • . . . . 18

g. Heart and Eyes . • . . . . . 20 h. Nervous System and Larval Musculature . . . 21 i. Nutritional Body . • . . . . • • 22 4. Hatching and Settlement 23

a. Hatching . . . ' . . . 23

b. Feeding . • . • 23

c. Morphology • . . . . . 25

d. Shell . . • . . • ...... 27

Effect of tempera ure on developmental-ra~e . . 30

Aplysiid Larval Development . . • . 32

Ecology ...... • 35

Methods and Materials 35 Results . . . 37

DISCUSSION . . . . ' . . • • • • • • • • • • • • • • 40

.Sm4MARY • • • • • • • • • • • 47 LITERATURE CITED •. .. 48

---

.... ACKNOWLEDGEMENTS

Sincere appreciation is expressed to Dr. Victor

Loosanoff for·his continued aid and criticism of the

manuscript. Thanks are given to Dr. James Blake for aid

in obtaining equipment and reading of the manuscript.

Thanks are also expressed to Dr. Steven Obrebski and

Dr. D11ight Taylor for criticism of the manuscript. 1 Collecting on the Bodega Bay Marine Reserve was permitted by the University of California Bodega Lab .

•

i LIST OF TABLES Page

Table I. Spawning of P. taylori Reported in

Literature ...... 57

0 II. P. taylori Developmental Times at 10 C, 14.5°C, and 17.5°C ...... III. Summary of Aplysiid Larval Development in

Literature ...... 59 IV. Literature on Opisthobranch Development 64

~.~ ~~~~ .. ·~

ii LIST OF FIGURES

Page

Figure

1. Phyllaplysia taylori range and recorded

spawning sites • . • • t------~2~.--~P~h~y~l,l~a~p~l~y~s~i~a~t~a~y~l~o~r~i-ce~g~g'"m~a~s~s.------68~------~

3. Early veliger of P. taylori

lt. Late veliger of P. taylori • 70 I 5. Metamorphosed veliger of P. taylori 71 1 6. Veliger musculature of P. taylori 72 7. Cephalic nervous system of P. taylori 73 8. Hatched veliconch of P. taylori 74- 9. Veliconch shell of P. taylori 75 10. Regression analysis of post-hatching shell growth of P. taylori veliconchs • • • • . • ...... 76 11. Comparison of developmental times of P. taylori ---- 77 ;;;--===-= 12. Effect of culture temperature on progressive developmental stages of P. taylori .• 78 13. Location of P. taylori sampling sites 79

iii Page

Figure

14. Regression analysis of Zostera sampling unit

and P. taylori abundance . . • • . . • • . • So

15. Regression analysis of P. taylori abundance

16. P. taylori sample mean lengths and 95% -~~~------~~c~o~n~f~~~·d~e~n~c~e~i~n~t~e~r=v=a~l~s~-.~.--.--.--.--.--.--.--.------84------

~ 17. P. taylori size frequency distribution 85 ,, 18. Zostera marina abundance measurements. 86 19. Inter-relationship of P. taylori and z. marina 87

----

----~---

iv INTRODUCTION

Taxonomic studies involving only adult forms of organisms may not necessarily provide complete information about differentiation of species or about the evolutionary relationships between species grouped in higher taxa. The taxonomic importance of embryonic or larval morphology as been limited only by the lack of detailed comparative morphological work on development (D 1 Asaro, 1966). Fretter

(1967) has shown that larval shell characteristics are reliable for taxonomic identification of some British prosopranchs. Ostergaard (1950) proposed using the structure of egg masses, larval shell type and developmental character­ istics to confirm adult taxonomic position. In recent literature reviews of the larval biology of opisthobranchs

(Thorson, 1946; Thorson, 1950; Ostergaard, 1950; Thompson,

1967), it has become apparent that a considerable amount of plasticity occurs with respect to patterns of development.

Often, closely related species have radically different developmental types (Rasmussen, 1944 and 1951). Even different populations of a single species may exhibit different develop­ ment (Mileikovsky, 1971). Often the ecology of the adults of closely related species is also differnet. However, it

1 2 is not possible to make meaningful correlations between the biology of the adults and the larvae unless additional ecological and developmental information is available.

There is a clear need for studies of larval development and the ways in which larval characteristics and embryology are correlated with adult biology in marine organisms.

Aspects of arval-de velopment--and-a;duj:t-ec-oicogy·------of Phyllaplysia. taylori Dall, are reported in this study.

BIOLOGY OF PHYLLAPLYSIA TAYLORI

Review of Previous Studies

The genus Phyllaplysia was established by Fischer (1870) for the type species P. lafonti (Fischer), and presently consists of 14 species in tropical and temperate waters

(Beeman, 1968). Information on most specj_es has been sparse and specimens rare. The first complete description of a species was given for P. engeli by Marcus 01nd Marcus, ---- (1957). Dall (1900) described the one species of Phlllaplysia known on the northeast Pacific coast, P. taylori. P. taylori is a small green patterned specj_es which lives on blades of

Zostera~~~ L., the common eelgrass occurring along shores of eastern Pacific estuaries. Mac Ginitie (1930) extended the range from British Columbia to t~onterey Bay, California. 3

Specimens of P. taylori are now known from Nanaimo, British

Columbia (49°9'N, 123"57'W) to San Diego, California

(32"42 1N, ll7°ll'W) (Beeman, 1963) (fig. 1). McCauley

(1960) discusses morphology of ~ taylori under the name

P. zostericola. Following a physiological study, Beeman

(1963) established f· zostericola as a junior synonym of P.

~aylori. P. zostericola was originally separated from f· taylori primarily on the basis of lack of a shell. However, Beeman was able to demonstrate that the presence of a shell is variable and may be present or absent. In a revie~1 of the order Anaspidea, Beeman (1968) states that although the sheLl is often lacking, it is still the single most important generic characteristic. This suggests a need for taxonomic review of the genus.

General Biology

The entire life of P. taylori is spent on blades of

----- Zostera. Eggs are laid, the veliconchs hatch, settle, conwence feeding and develop into adults. Protective green coloration and a brown longitudinal and lateral striping pattern camouflage the animals and make it nearly impossible to distinguish them from Zostera without close examination of the blades, es'pecially at sizes less than 2 em. The only 4

observed method of locomotion is that of crawling on the

blades, first attaching the posterior end, lengthening the

body and then attaching the anterior end and shortening the

body (McCauley, 1960). Movement is slow and accounts for

a supposed lack of mixing between populations of the species

(Beeman, 1970a). However, I have observed P. taylori l----"f'l-=o-=a"t>ic::n-:cg=---=o:-::n=->b:-:r=-o"'kc:-e=-n=-z""'o-=s"'t-=e-=r=-=a----.:b'"l.-:accd"'e::cs=--f"r=occm----:co=n-=e-=a-=r=-=ec=a~ccoc-caccnc-ooct""hcce~r~.------

This method of locomotion is not under control by the animal,

but appears to be not infrequent, especially during the

winter months. Also small Phyllaplysia adults have been

taken in plankton tows in Tomales Bay, California (D.B.L.

Smith, personal communicatj_on; J.A. Blake, personal communi-

f- • ) Cav~On • These observations suggest that P. taylori may

be able to colonize other areas by floating to them.

Populations may not be as isolated as previously believed.

The species is hermaphroditic and copulation is

reciproca.l. A detailed study of the anatcmy and morphology

of the reproductive system and aspects of spermatogenesis ----- has been provided by Beeman (l970b; 1970c; l970d).

Examinations of the gut contents show that.P. taylori feed

unselectively on the film of diatoms and other organisms

growing on the Zostera (Beeman, 1970a). A report of stomach

tooth replacement rate in P. taylori was the first such study 5

in opisthobranchs (Beeman, 1969). During the present

study, Phyllaplysia was observed to have no natural predators,

although Mac Ginitie and Mac Ginitie (1949) record

observing two Conus californicus feeding on a single P.

taylori.

Larval Development j-----='-'-~=-=----==~------~------

Methods and Materials

During June, 1972, to September, 1972., adults were

collected in areas adjacent to the sampling sites in order

to obtain fresh egg masses for larval studies. A total of

16 adult animals 'trere kept in the sea water tables and pro-

vided twice 1~eekly with fresh Zostera on which they grazed

on the diatom cover. Studies by Beeman (1970b) show that

the diatom cover which develops in holding tanks and cul-

tures alone is sufficient to feed the animals. Egg masses

were spawned in the laboratory, collected, and cultured

individually at 10 0 , 1 4 .5 0 , 17.5 • and 22 0 C. Each egg mass

1-ras divided into four equal sections and one section cultured

at each temperature to eliminate effects of differences in

developmental rate between egg masses for comparisons of

effects of temperature. Egg cultures were continuously

illuminated but not aerated. Customary precautions were 6 taken with double filtering of the sea water supply.

Because of possible effects of antibiotics on larval cultures (struhsaker and Costlow, 1969) an alternate method to prevent contamination was chosen as a precaution. Double filtered sea water was boiled in a five gallon closed vessel for 10 minutes and then maintained at the appropriate temperature for 24 hours before use in curture~INB:t-e-r·------­ was changed daily to hatching and every other day thereafter.

A total of 30 egg masses were examined and cultured.

No difference in time of development or stage of the embryo was detected throughout the egg mass. Additional food was not provided for the larvae after hatching, as they are immediately capable of grazing on the diatom cover which developed in the culture dishes from the Zostera and the egg masses.

At hatching the larvae crawl from the egg capsule on to the immediately available substrate. Preliminary experiments ---- on substrate preference for settlement showed no selection ;;;== for Zostera, algae, sand or glass substrate. Therefore further substrate selections were discontinued. 7

Results

1. Egg Mass

Beeman (1970a) provides a detailed description of the

physiology of oviposition of f· taylori. The egg string

leaves the common genital aperture and is pushed along the

-~~:-____.external genital groove to the area of the mouth. The li egg mass is deposited as the animal continuously moves its head from side to side laying parallel rows of the string.

The animal gradually moves backward, laying the egg string

and pressing it to the substrate with the aid of the lips,

labial lappets, and the anterior edge of the foot.

The egg mass or nidosome, is well compacted and ·forms

a rectangular egg packet. The egg string is applied to the

substrate, a~· marina blade, in successive tightly compressed,

parallel, double layered rows, thus forming an egg mass with

two layers of egg capsules. This double layered character-

istic has not been previously described but has been found

by this author to occur in every egg mass examined. In the

laboratory egg masses were laid on substrate other than

Zostera. Egg masses examined were from approximately

5 to 35 mm long and the width of the Zostera leaf on which

they are laid. Beeman (1970b) kept some adult Phyllaplysia 8

in laboratory outdoor tanks. These became very obese and

laid egg masses 20 x 50 mm in size. Egg masses laid in

the laboratory in this study were of normal size as were

the adults. Fresh laid egg masses are light golden in

color but progressively become darker as detritus accumulates

on them. Each egg capsule of the string is connected by the

twist of the albumen membrane. These connections-o-e-tw·e-e·n----e-gg----­

capsules are no longer visible after the complete formation

of the nidosome. All of the rows of the egg string are then

covered by a gel-like s_ecretion. The capsules have a mean

length of 4L~l ..... ±4o.63 (41) and are compressed by others

parallel to them (fig. 2). Each capsule contains a single

embryo and a single spherical body which is believed to ] be a nutritional body. Fertilized ova have a mean diameter of 150.7A±6.o8 (25) and the egg mass contains an average

of 27.0 egg capsules per mm2 in the two layers. The exactness

of the formation of the egg mass of P. taylori is a ----- characteristic not present in most anaspidean species which

;;~-~--~---co-~ have been studied, as shown by Table III. The usual

anaspidean egg mass is an egg string, at least somewhat

tangled or laid down irregularly and the majority have more

than one ovum per compartment. This is an indication that

Phyllaplysia is one of the more advanced species of this 9

primitive group.

Notations of abundance of P. taylori egg masses during

the year vary greatly from area to area (Table I). In

January, 1931, Mac Ginitie (1935) records finding "thousands"

of!· taylori nidosomes in Humboldt Bay, California. The

present study at Tomales Bay and Bodega Bay, California t---~found-e&g-massE~'>-pr_e_s_e_nt_f_:r_om April to early September

during 1972. Egg masses were not observed in the field

from October to March in either Bodega or Tomales Bays.

Beeman (1966) records finding few egg packets from December

to February and then in large numbers, from March to October

at Elkhorn Slough, California. Mac Ginitie and Mac Ginitl.e

(1949) again later noted the presence of Phyllaplysia ·egg ] masses at Newport Bay, California, from October to June with the height of the egg-laying season in November.

2. Early Development

Spiral cleavage proceeds in the follm1ing manner:

first cleavage, equal; second cleavage, unequal; third

cleavage, equal. This results in an eight cell stage of

two large macromeres, two small macromeres and four slightly

smaller micromeres. Further cleavage, blastula formation

and gastrulation continue as is normal in opisthobranchs and 10 will not be discussed further. Emphasis is on the post- gastrula development through settlement, beginning with differentiation into the characteristic molluscan trochophore.

From beginning of the recognizable trochophore until hatching there is little increase in actual size of the embryo while internal differentiation is taking place.

3. Organ Morphology to Metamorphosis a. Velum

A circular band of ciliated cells forms the anterior prototroch of the trochophore, As the prototroch becomes more prominent the trochophore begins a slight rotational motion. 'rhe shape of the prototroch changes into a circular velum with growth of the cephalopedal region of the body, primarily involving the differentiation of the metapodium.

As is characteristic in opisthobranch larvae, the velum invaginates mid-dorsally and becomes bi-lobed. At this point the embryos are termed veligers. The velum differentiates further into a pre-oral velum with large cilia and a post- oral velum with smaller ciliation (fig. 3). The velum becomes very granular in appearance containing numerous large refractile cells which form the base of the ciliation .

• 11

The structure and function of the velum is not further altered until immediately preceeding metamorphosis. Larvae which are near metamorphosis can be identified by a change in velar activity. At the end of the late veliger stage the steady, metachronal ciliary beat changes to a jerky, uneven, and stronger activity. Through vigorous spasmodic extensions and contractions of the velar musculature the pre-oral velar cilia are all simultaneously thrust outward and then tightly withdrawn into the velar shell as the lobes are pulled in. This activity continues repeatedly and may occur periodicaJ.ly for a time varying up to 24 hours prior to metamorphosis.

Similar ciliary activity has been described by Fretter

(1972) in reference to pre-metamorphosis activities of some prosobranch veligers. The activities she describes result in the velum being either ingested as in Crucibulum spinosum

(Sowerby), Crepipatella lingulata {Gould) and Lacuna vincta

(Montagu), completely cast off as in Calyptraea chainsis

(L.) and Nassarius incrassatus {Strom), or absorbed with some cells cast off as in Mangeli

(1958 and 1962) reports partial absorption of the velar apparatus in the opisthobranchs Adlaria proxima (Alder and

Hancock) and Tritonia ~ombergi Cuvier. Fretter (1972) 12

relates the fate of the velum to the position of the

odontophore at pre-metamorphosis and shows that in the three

species which ingest the velum the odontophore is immediately

moved forward to its adult position after the velum is swal- i! lowed. In both species which completely cast off the velum, i: 1: 1' the process of ingestion would be blocked by developing

~~--===------,o:~~=~=--= organs. In Calyptraea the odontophore develops in tlre-a.-d-ali-7'c------

~ position and Nassarius develops an acrembolic proboscis. I! i: Fretter assumes that velar absorption in Mangelia is a

similar strategy. As the odontophore in Phyllaplysia

larvae has begun development at this stage in the adult

position, it appears probable that absorption of the velar

lobes may be attributed similar to that in Calyptraea.

This activity, however, appears to serve an additional

purpose in Phyllaplysia, namely breaking up of the spherical

nutritional body present in the egg capsule throughout

development. Repeated observations v1ere made of this activity.

The sphere is broken into several smaller particles which

are ingested by the veliconch just before hatching. Thus,

a nutritional function has been attributed to this body.

Refractile characteristics suggest that it may be of lipid

content. 13

Metamorphosis in Phyllaplysia thus commences with the

gradual resorption of the velar lobes resulting in the

protrusion of two lobes of tissue which are the precursors

of the cephalic tentacles of the adult.

b. Foot

The foot rudiment begins as an anterior cellular

prot r us i on-----o-r-t--rre-t-r-oc-ho-p-ho-r-e-. -I-n-t-h-e-l-a-t--e-t-r-se-he-t=:ft-eF-e-t-Re-----

cephalopedal region begins differentiation into a metapodium.

The foot elongates dorso-ventrally and becomes flattened

antero-posteriorly. Minute cilia develop along the edge

of the metapodium. Simultaneous with development of the

pre-oral and post-oral velum the operculum is secreted by

the posterior surface of the metapodium (fig. 3). In the

late veliger·the propodium grows anteriorly and begins as

a ciliated and flexible "hump" area on the anterior metapodium

(fig. l.J.). The pro podium continues to increase in size and

flexibility. This development results in the presence of

------sensory cilia on both dorsal and ventral surfaces of the foot

(fig. 5). After hatching, these sensory cilia become active

and important in veliconch feeding behavior. This behavior will be described in the hatching section of this paper.

With metamorphosis the veliconch uses the foot to crawl

within the capsule and at hatching for crawling onto the 14

immediate substrate. The operculum is cast off prior to

hatching and remains in the capsule.

c. Shell Gland

The shell gland begins as an invagination in the early

trochophore. At approximately the same time, .the velum

invaginates into two lobes and the shell gland everts from

the dorsal side of the embryo form1ng a derinr~ive ~arval______

shell (fig. 3). The mantle cavity is very shallow, as the

visceral mass fills almost the entire shell. Size and struc-

ture of the velar shell remains constant throughout develop-

ment to the point of hatching. P. taylori has a type one

velar shell according to revised classification (Thompson,

1961). There is no characteristic sculpturing of the larval

I shell. At hatching, additional layers are visible marking l 1 I new shell growth. If the larva hatches soon after resorption I of the velum and development of the propodium then the new

shell growth begins after hatching. However, if hatching -·----- is delayed, then shell growth will begin while the larva

~-~------is still encapsulated. Hatching was in all cases observed

to.occur shortly after advent of shell growth.

d. Excretory Organs

The excretory function of larval opisthobranchs through

development ·is assumed by two types of larval kidneys: 15

(1) the primitive kidneys or nephrocysts and (2) the secondary kidney (Raven, 1958). A third organ, the anal cells, may also serve in excretion as indicated in A. punctata (Saunders and Poole, 1910). The excretory function is gradually transferred from the larval primitive kidney· to the secondary kidney which continues to function in the

. p t 1 • present ln _. ay~orl. The anal cells are formed pro- truding on the posterior end of the trochophore and with the velum serve to orient the animal. As cell division continues and the trochophore develops they migrate laterally and anteriorly. As development proceeds they decrease in size, simultaneous with appearance of the primitive and secondary kidneys {fig. 4). Saunders and Poole (1910) correlate this decrease in size with growth of the larval kidneys and assumption of the excretory function by them.

Ries and Gersh (1936, according to Raven, 1958) showed an

------~-- accumulation in the anal cells of trypan blue and basic ------a-~--~~--~ vital dyes, thus indicating an excretory function. When first observed, the cells of the primitive kidney lie within the body cavity in an antero-dorsal location. The primitive kidney in Phyllaplysia is a single, bi-lobed organ rather than two U!];icellular ones as in Aplysia (Saunders and Poole, 16

1910). However, its bi-lobed shaped with a central

constriction indicates a possible origin from two cells

as in Aplysia. These cells in living Aplysia contain

~I brightly colored globules and similarly in Phyllaplysia the

single structure is densely packed with small globules,

imparting a granular appearance. Saunders and Poole (1910)

~~i----a~nccaor-R·aven (19-:58) agree 'ffiarthe cells of---crhe primrtJ:ve

kidneys are characteristic of opisthobranch larvae and

presumably function as temporary excretory organs. Saunders

and Poole (1910) discuss at some length, the differentiation

between primitive and secondary kidneys and clarify the

confus:i.on of terminology that has resulted from other works,

including that of Carazzi (1905) on Aplysia embryology. II i The terminology and definitions used here are those estab- I '! lished originally by Mazzarelli and adopted by Saunders and

Poole ( 1910) •

In the late veliger, the secondary kidney (fig. 4) ·----- starts development to the right of and lateral to the primitive

kidney. By post-hatching this becomes the permanent excretory

organ. Also in the late veliger the anal cells are observed

to sink posterior to their original site and gradually

disappear by the time of metamorphosis (fig. 4). The

secondary kidney in Phyllaplysia is originally a paired 17

organ with two unequal size lobes both of which converge

to form a single duct opening into the mantle cavity. As

development proceeds the left lobe becomes larger and the

right smaller. Both lobes possess cavities and fluid move-

ment can be observed. A. punctata possesses a single

unpaired secondary kidney, as is characteristic of opisthobranchs f-~~-,(S--aund-e-r-s-arrd~F-ooi-e--,------J:~X0-)-.~T-h-e-e-r1-g-1-:-n-e-f-t-he-s-ee-ena-a-~y'----~-~~~-

kidney of P. taylori is more similar to that in Umbraculum

which also has an originally paired organ (Heymons, 1893

according to Saunders and Poole, 1910). According to Saunders

and Poole (1910), Mazzarelli ascribes a mesodermal origin

to both the primitive and secondary kidneys. They, however

feel it more likely that in A. punctata both are of ectodermal

origin, as are the anal cells.

e. Statocysts

In the early veliger a pair of statocysts develop at

the posterior base of the foot. These presumably develop

-~~~ as ectodermal invaginations, as j_s true in A. punctata ---- (Saunders and Poole, 1910). They are at first, closed

clear vesicles which lie posterior to and on each side of

the anterior end of the esophagus. They each quickly

develop a centered dark spherical statolith which is seen

to rotate in the enclosure. The statocysts remain visible ' 18

throughout development and hatching but are obscured 48

hours after hatching. In adult Phyllaplysia statocysts

are embedded in the dorsal surface of the pedal ganglia

(McCauley, 1960).

f. Alimentary System

Differentiation of the digestive system takes place ~ ·1":---~~=.r~itn----r ormation of--the gurand-:rt-s-ac_c_e_s_s-ory-organs-(-fig. 3) . 1 The foregut does not open directly into the mouth, rather, I a highly ciliated channel, forming the esophagus, connects the mouth to the foregut opening. Saunders (1910) describes·

this ciliation as very numerous in A. punctata. The foregut

enters the oblong shaped stomach antero-dorsally. Evidence

of torsion is present in the early veliger, as the foregut I is twisted Nhen first visible (fig. 3). Further torsion I is evidenced by a dorsal to ventral change in position of I the foregut entrance to the stomach. The entire alimentary canal is shifted ventrally and to the right with the veliger

----- becoming asymmetrical. This rotation is somewhat different

from that of the prosobranchia in which the stomach and liver

are shifted ventrally and to the left side (Raven, 1958).

The results of torsion are visible primarily in the gut and

liver and no asymmetrical grov1th occurs in the shell. This

is also true of Aplysia. Ciliary current in the stomach is 19

in a clockwise direction. The internally ciliated intestine

leaves the stomach posteriorly and left of the midline.

After torsion it comes to lie almost parallel and to the

left of the foregut with the anus opening antero-dorsally

into the right side of the mantle cavity. Torsion is a

process of differnetial growth beginning in the late troche-

!------'------~•• ------phore and is completed by the late veliger. At 17.5 C water

temperature the whole process of torsion lasts approximately

5 days. According to Raven (1958) this is a relatively long

time as compared to some other gastropods.

The liver, or digestive diverticula, arises from the

right and left sides of the midgut. It consists of two

unequal lobes surrounding the stomach and is easily distin-

guished by large numbers of vacuoles in the cells. The

left diverticulum is larger and ovoid in shape, while the

right is smaller and rounded. In some gastropods, the liver

is strictly a larval organ and is replaced by the definitive

liver. In Phyllaplysia, however, the larval liver becomes

the adult structure. Until hatching the larva feeds on

yolk stored in the left diverticulum in which a lumen is

- -- visible. The right lobe lies more anteriorly with the

twisted foregut passing to its right before entrance to the

stomach. No lumen is distinguishable in the right diverticulum 20

and presumably it is only secretory. The radula develops

as an evagination of the foregut in the late veliger. In

the recently metamorphosed veliger the radula is not

~! always clear because of the presence of the egg capsule,

but back and forth movement of the structure can be observed.

g. Heart and Eyes

~~------,T"h::-:e:;-cl'a;:;ct~e~vc;;o;e-,l'i-;;g"'ec;;;r;-os"to-;aocgc;;eo;-o=f de ve lopment 1 s ~den t-rrJ. e d

by the presence of a pair of spherical red pigmented eyes,

located anterior and mid-dorsal to each of the cerebral

ganglia (fig. 4). \-Jith continued development, the pigment

becomes progressively darker and eventually turns black.

Saunders and Poole (1910) do not mention either the

larval or adult hearts in their treatment of A. punctata. j This is rather surprising when the detail of the study is 1 considered. The larval heart of P. taylori was observed ' I only as a small vesicle anterior and dorsal in the mantle ' cavity. Such details as the valve structure noted by i'Terner

(1955) in the larval heart of Crepidula were not observed.

The definitive heart develops as an accumulation of cells

posterior and dorsal to the primary kidney of the early

veliger. By the late veliger these cells have formed the

rudiment of the adult heart, a pear shaped organ with a

clear cavity. The pericardium begins active irregular 21

rhythmic contractions at this stage, but these do not

become steady until metamorphosis.

h. Nervous System and Larval Musculature

Velar musculature of the late veliger consists of

three large extensions of the retractor muscle branching

to the cephalic region (fig. 6). The large larval retractor u-----:m-a-s-e--l-e-a-t--t--a-e-PJ;e-s---t-e-t-ae-13-eEl-y-"t·J'-a--l-l-ElG-s-te-r-i-G-r-1--y-_,-1e-t-t-o-t-t-he:------______

mid-line and slightly to the ventral surface. The fibers

pass dorsal to the left liver and are distributed to the

velum, foot and secondary kidney. A small retractor muscle

with three fibers also originates at the dorsal side of

' the shell but is more anterior and inserts on the secondary

kidney. II The paired cerebral ganglia lie dorsal and lateral to lI the esophagus, posterior to the eyes and anterior to the statocysts (fig. 7). The rudiment of the cerebral commissure,

which will lie dorsal to the esophagus, can be seen between

the two ganglia in the late veliger stage. In adult

Phyllaplysia there are four pairs of bifurcated nerves·

~Thich arise from the cerebral ganglia (McCauley, 1960).

Three of these pass to the tentacles and rhinophores and one

laterally. Rudiments of these are present in the velum by

the late veliger (fig. 7). The pedal ganglia themselves ' 22

were not visible, owing to their position posterior to the

cerebral ganglia. Eight rami of the paired anterior pedal

nerves are observed passing to the anterior portion of

the foot.

i. Nutritional Body r~ ! The nutritional body is a transparent, refractile -~1----~sph---e-re-----oc--c---ur-r±:n-g--:tn-t-he-e-g-g-c-a-p-s-u-Ie_..w-i-t-h-t-he-e-m-b-r-";}.,._o •

' Capsules deposited ',iithout ova do contain the sphere, I indicating it is not a polar body or other product of cell division. Mean diameter of the nutritive body is 49.2~~4.8

i (25). Size of the nutritional body remains constant through-

out development of the embryo until prior to hatching Vlhen IH i velar activity changes. By means of this strong velar

beat the nutritional body is thrust around in the egg capsule l and fragmented into several smaller particles. After meta- I I morphosis, the particles are then drawn into the velar shell cavity dorsal to the cephalic region of the body

---- and are kept in continuous rotation by ciliary action (fig. 5).

This activity further fragments the sphere. Immediately

prior to hatching, the veliconch engulfs the particles.

Histochemical ana.lysis of the nutritive body was not possi-

ble with existing facilities, hm-Iever the particles were dis-

sected and removed from capsules and freeze dried for later study. 23

4. HatchinG; and Settlement a. Hatching

Hatching of veliconchs is spread over a 5-18 day period at a water temperature of 17.5°C in the laboratory. This time period may be much shorter in the natural habitat due to external action on the egg mass by the water. Hatched veliconc s break their way out or--trre-eg;g-c~-p-su-1-e---.~h:tch------­ has already been softened by the strong ciliary activity before resorption of the velum. Enzyme activity probably softens the capsules as has been shown in other opisthobranch hatchings supplemented by mechanical means (Davis, 1968).

This ciliary activity, previously described in the section on morphology of the velum is very similar to that described

for Haminea antillarum d'Orbigny, a Jamaican opisthobranch

(Davis, 1967). H. antillarum softens the capsule membrane by a series of "violent back-and-forth movements" within the egg capsule. Contrary to past speculation (Beeman, 1968)

------no free s11imming larval period occurs in P. taylori. The

veliconchs settle directly upon hatching. Preliminary

experiments showed no substrate preference for settlement. b. Feeding

Upon settlement the veliconchs begin immediately to crawl and ~ctively feed. At hatching the radular formulae 24 is 7 x 2•1'2 and the activity of the radula is predominant· in the veliconch anatomy. The radular ribbon and the two large muscles which operate the odontophore are continually in motion. Food can be visually followed through the foregut and in the intestine by the ciliary currents, Feeding activity of P. tavlori is characterized by a distinct

whether on Zostera or glass, attaches itself to the substrate by the metapodium and leaves the anterior propodium free.

As previously described, the anterior propodium is rounded on the end, flattened dorso-ventrally and densely ciliated.

The anterior propodium folds itself in on each side forming a ciliated channel to the mouth and simultaneously is moved dorso-ventrally through the water. This activity is continuous as the veliconch is feeding. This same pattern of activity has been described by Engel and Eales (1957) as a "habit of many species of Aplysia." They specifically

------describe this behavior as "search movements 11 and cite that the same activity has been described for Aplysia fasciata

Poiret, A. depilans L., A. grandis (Pease), Syphonata punctata

(= Aplysia peasei), and A. tryonii. Engel and Eales (1957, p. 85)

' 25 actually go on to establish a subgenus Tullia for species

.which have developed "a distinct sucking disk in the posterior part of the foot". A study by Frings and Frings (1965) on Aplysia juliana Q,uoy and Gaimard also notes this feeding activity and reports tests showing the oral tentacles and mouth to be areas. of chemical stimulation and the adult rhinophores as areas sensitive to mechanical stimuli. c. Morphology

Gradual post-hatching changes (fig. 8) occur in the cephalic end resulting in the cephalic tentacles being more separately defined. Body pigmentation of the hatched veliconch consists of four red pigmented areas on the four corners of the dorsal edge of the foot and five smaller golden-brown pigmented areas on each cephalic protrusion. This latter pigmentation may be a precursor of the dark brown lateral and longitudinal striping pattern of the adult. However, the red marking does not occur on the adult animal. The odontophore and radula lie in the center of the oral cavity set back from the mouth. The muscles which operate them are inserted posteriorly on the cartilaginous odontophore.

The odontophore is spherical in shape and covered dorsally by the radular sac which medially contains the radula. The esophagus emerges dorsally from the buccal mass and then 26

passes dm·m~mrd under the heart to the crop and gizzard.

All of the gizzard is obscured by the lobes of the digestive

diverticula. The intestine leaves the gizzard and rises

dorsally to make four loops leading posteriorly to the anus.

The two lobes of the digestive diverticula increase in size

to fill the majority of the original velar shell and cover

two chambered heart is located dorsally and slightly to the

left of the body center. It lies dorsal and perpendicular

to the esophagus and visceral mass. At this point there is

no distinction in size between the tv10 chambers. The right I chamber of the heart, the atrium, receives the efferent ~ branchial vessel into its right-most side and opens into the ventricle on the left. The heart as observed with

transmitted light shows alternate contraction of each chamber.

I The ctenidium develops as a convoluted transparent sac

J.ying obliquely and dorsal to the visceral mass. The left

end passes posteriorly into the visceral mass presumably

to the connection with the efferent branchial vessel. This

connection could not be clearly observed. Distal to the

connection of the ctenidium is a clump of transparent cells.

At present, the fate of this group of cells is not. determined.

The mantle cavity is highly ciliated on the right side of 27 the body. A total of eleven muscles originate at the veliconch body and attach it to the shell, three on the right side and eight smaller ones on the left side. d. Shell

The status of the shell of £.· taylori is presently one of the basic problems of the taxonomy of the group. Beeman

(196B, p. 94) reports, ;;at present, the most important~------­ generic character ~f the genus PhyllaplysiaJ is the nature of the shell. It is, however, very often lacking". It is obvious that the primary taxonomic character of a group cannot be one that is often absent, and that the criteria should be re-evaluated.

Development of the velar shell up to hatching has been previously discussed. Additional shell growth begins after metamorphosis has taken place. Continuous growth rings v1ere observed to be added to the central nuclear velar shell for 60 days post-hatching, forming a visor or hood-like projection (fig. 9). Up to this time the animal body grew at approximately the same rate as the shell, becoming longer than the shell only when fully extended. Data on veliconchs indicate that post-hatching shell growth is highly linear with time (fig. 10). This type of shell is considered aplysiform as defined by Beeman (1968). 28

The largest settled larvae cultured in these experiments

had a shell of l. 25 mm. No future loss of the shell was

suggested at that stage. The fate of the larval shell in

P. taylori. is unknmm. Beeman (1970b, p. 206) makes a

short reference to the primary shell "pop [ping] off the

young animal's back" after growth to 2 mm and leaving only

a scar. However, this reference does not state whe~her

the adults of these juveniles did or did not possess shells.

lvinkler (1958) reports the larval shell of Aplysia californica

forms the nucleus of the adult shell.

Thompson (1962) suggests a mechanism whereby the shell

may have become internal through enclosure by the mantle

folds. He speculates that loss of the larval shell was

pushed back further into development in each generation

until the nudibranch larval shell is presently cast off without an internal stage. Considering the evolutionary

path of the shell in opisthobranchs from an external shell

in Akera, to an internal shell in Notaspideans, and finally

to complete absence of an adult shell in the Nudibranchia,

it seems questionable that the larval shell would be lost

and another secondary structure develop internally in

Phyllaplysia. 29

Phyllaplysia has usually been characterized by absence of an adult shell (Pilsbry, 1896; Eales, 1944; Cooke, 1922). Kay (1964) published a shell description for Phyllaplysia petalifera and P. albomaculata, from the Hawaiian Islands.

The presence of a shell has been noted in three other species:

P. inornata Bergh (Bergh, 1905), P. engeli Marcus (Marcus,

separation of P. zostericola from P. taylori was based on the absence of a shell and color characteristics. The t110 species ~Jere later synonymized (Beeman, 1963). Beeman (1968, p. 94) characterized the adult shell of P. taylori when present as a "thin, fragile, calcareous, dorsally concave, secondary structure.'' He states that it is not aplysiform, but gives no details to support this statement.

No data concerning formation of the proposed secondary shell is given. Detailed examination of the P. taylori adult shell is required to determine 'N"hether it may accurately be

c-.- termed secondary. Further post-larval groHth studies v1ould indicate the fate of the larval shell and determine if the adult shell, when present, is secondary. The most prominent characteristic of the adult shell as photographed

(Beeman, 1968) is a large flat apex. Larval studies have proven P. taylori to have direct development and as a large, 30 irregular apex is an jndication of non-pelagic development

(Thorson, 1946) this explanation of adult shell form is distinctly possible. Dissection of ten adults which spawned egg masses used in this study resulted in no adults with shells. Specimens examined varied from 23 mm to 30 mm body length.

Effect of Temperature

As shown by many studies on molluscan development,

(Davis, 1963; Struhsaker and Costlow, 1969; Scheltema,

1967; Dehnel, 1955) the rate of larval growth is affected by environmental parameters, some of which may be controlled in the laboratory. In order to determine the effect of water temperature on the rate of larval growth of P. taylori cultures were maintained at 10°, 14.5•, 17.5°, and 22°c.

These temperatures span mean yearly water temperature at

Tomales Bay, California, 13.23 0 C, from which the adult

~~-·--·

animals were collected. Cultures at 10•, 14.5•, and ;:__ -

17.5•c all finally reached metamorphosis and settled.

Hm~ever, the original six cultures at 22°C did not develop past the four cell stage and thus no further cultures were carried at this temperature. More larvae should be cultured at this temperature to determine its effect. lvater tempera- 31

0 tures along the California coast do not reach 22 C. Thus,

it seems doubtful that larval cultures would develop at

such a temperature.

Cultures maintained at 17.5 0 C were used for descrip-

tion of larval and post-hatching morphology. No observable

difference was noted between the development of cultures f------a-t-l-4---.--5 ° a-n-d-l-7----.~G----ot-h-e-r-t-h-a-n-t-h-e-r-a-t-e-ef-6.-e-v-e-l-epme-n+tr.---~-----

Cultures at 100 C showed more abnormal grov1th than the other

two temperatures. The most prominent of the abnormalities

'\'ras in velar shell growth. The shell was thin and not distinct

f·rom the mantle tissue. The development of the foot and

velum also lagged behind development of other structures.

Abnormalities present in the 10 0 C cultures were not present

in a:!.l of the larvae. Some larvae of each culture did go

on and develop normally as in the 14.5° and 17.5°C cultures.

Because there is not appreciable size increase of

the larvae of P. taylori from trochophore to the beginning

of hatching, some other means of measuring growth of the ---- larvae had to be used. After preliminary study it was

determined that this grm~th could best be described in seven

stages, each having definite characteristics, thus making it

possible to investigate the effect of temperature on the

rate of larval growth. The stages were as follows : 32

{1) zygote, the fertilized, undivided ovum, {2) blastula,

(3) gastrula, (4) trochophore, characterized by the begin- ning shell gland, anal cell formation and prototroch,

(5) early veliger, with a definitive larval shell and bi-lobed velum, (6) late veliger, defined by the appearance of a pair of eyes, and (7) hatching. The majority of

veliger stages as described in the section on larval morphology.

Differences in development along the temperature gradient were as expected. Lower temperatures resulted in an increase in hours required to reach a certain stage of development (Table II, fig, 11). Total developmental time to hatching was more than twice as long at l0°C than at 17, 5 0 C. The effect of temperature on the developmental time was greater with progressive developmental stages

(fig. 12). ----·------

Aplysiidae Larval Development

Marcus {1972) adopts the classification established by

Pruvot-Fol (1954) dividing the Anaspidea into families

Aplysiidae and Notarchidae. The former contains the sub-

families Aglysiinae and Dolabellinae and the latter contains 33 the Dolabriferinae and Notarchinae. The Notarchinae consist of a single genus, Notarchus, with all the other genera transferred to the Dolabriferinae. According to the characters considered, however, position of the genera may be disputed. This classification does not change

Phyllaplysia from the position adopted by Eales (1960).

will be folloHed in this review of Aplysiidae larval develop- ment. The classification of the Anaspidea is as follows:

(Eales, 1960; Beeman, 1968).

Order - Anaspidea

Family - Akeridae

Genus - Akera

Family - Aplysiidae • Subfamily (1) Aplysiinae

Genus - (a) Syphonata (b) Aplysia

(2) Dolabellinae ------

(a) Dolabella

(3} Dolabriferinae

(a) Dolabrifera .. (b) Petalifera (c) Phyllaplysia (4) Notarchinae

(a) Notarchus (b) Stylocheilus (c) Barnardaclesia (d) Bursatella

The Aplysiidae are considered the most modified of the

"tectibranchs" with no present species closely resembling

their primitive ancestors (Pilsbry, 1896). The largest genus :------~------~-- -- of the aplysiids is Aplysia, containing more then 35 species

(Eales, 1960). Information in the literature on aplysiid

larval development is available for only 17 species, in-

eluding the present study of P. taylori. Ten of these

species are Aplysiinae, four are Dolabriferinae and three

Notarchinae. Results of aplysiid development studies are

compiled in Table III.

Examination of egg mass structure of all species

indicates advanced characteristics in the Dolabriferinae.

Egg mass formation in the species of Aplysia and the

Noatarchinae consists of a tangled mass of filament, some------

times not even continuous. Structure of the mass in the

Dolabriferinae is more advanced, a rectangular band

of compacted parallel rows of the egg string. There appears

to be no distinct pattern regarding the number of ova

per capsule. This number varies from 43 to a single ovum. 35

Type of development has been determined in 10 of the 17

species, 9 of which have pelagic development, with only

P. taylori developing directly.

The most insurmountable problem in opisthobranch larval

development study has been the successful culturing of

animals through metamorphosis. This has equally been true

1----in-t-ne-stmiy-oi'----th--e---a-p-l-ysi.-j_-Q.-s-;--I:;errgth-of----rre-e=swi-umriiYg------­

Period for pelagic species has not been determined and

metamorphosis has not been observed. The direct development

and settlement of P. taylori is thus the first record of

metamorphosis in this group. P. taylori is the only

recorded anaspj.dean to have direct development and thus

should be added to the recorded minority of opisthobranchs

developing directly. .

Ecology

Methods and Materials

~-~------K!:Yllapl.ysia taylori were collected from Zostera marina

beds in two localities: (1) one-half mile southeast from

the mouth of Tomales Bay at La1tlson's Flat, Marin County,

. California (122"57 1 15"W, 38°l3 1 4L~"N) and (2) in the Bodega

Bay harbor on the University of California Berkeley-Davis

marine rese,rve, Sonoma County, California ( 123" 3 '33"W, 38°18'45"N} (fig. 13). Each sampling site was located

within a Zostera bed and consisted of an area 20 meters

long and 10 meters wide. Sampling areas were approximately

at -1 foot below Jv!LLW. Samples were taken within twenty

randomly chosen square meter quadrats once each month at

low tide. (0.1 tide or less) Each individual sample consisted il----ur------a-r-rand--fu-i-o-f------z-u-s-t:-e-r-a-e-l-i-f)-!3e-Ei-e-~f-a-t-t-he-Qas-e-_,-le_ELVi _ng, ______

the rhizomes, vlithin a quadrat. The Tomales Bay population

was sampled monthly from October, 1971, to March, 1972.

Sampling was discontinued because of damage to approximately i 75% of the sampling area by clam diggers. Sampling was

subsequently concentrated in area (2}, a sampling area

somewhat similar to the original site. However, site (2}

differed from (1} in the following respects: slope of the

bottom, depth and density of the Zostera bed, and strength

of the water current through the site. In area (2} samples

were taken from July, 1972, to March, 1973. Because of

winter storms, reliable ecological data was not obtained

from this area and is therefore not included.

In the laboratory, each sample was examined to

determine the number of P. taylori per sampling unit of

Zostera. All specimens were removed and the foot of each

was measured. The animals were then placed in 75% isopropyl 37 alcohol for one month and dried. Measurements of the total length and dry weight of the blades were taken. Dry weights of animals and eelgrass were obtained on a Mettler balance.

Results

Changes in abundance were determined from counts of numbers of ~· taylori per unit of Zostera. Numbers of

P. ta:tlori are plotted against the length of the Z. marina from which they were collected in figure 14. Regression analyses of the data shol~ no significant correlation between the length of the plants and the numbers of

Phyllaplysia on them. The results suggest that the abundance of the opisthobranch can be simply expressed in terms of numbers per handful of Zostera.

In figure 15 the mean numbers of Phyllaplysia per sample are plotted against sampling time in days. The regression fitted to the observed abundance for October ----~- to March, inclusive, is significant. This indicates that the Phyllaplysia population declines at a relatively constant rate during this period.

Data on the changes in size and growth were analysed by plotting the size frequency distributions of all the specimens collected at each sampling time (fig. 16). The 38

data from October, 1971, to January, 1972, show that during

these months, individuals of the population increase in

size in conjunction with the high mortality rates. February

and March samples had no specimens at all. The smallest

specimens in the October, 1971, sample were 2 em.

In figure 17 the average Phyllaplysia lengths and t----+-'1le±r-§i5%-c--on-fi-d-e-nc-e-J.:-n-t-e-r-v-a-l-s-a-r-e-~±et-t-e-9.-t-e-s-Gmpa-!!-e------

sizes at the different sampling times, The results indicate

clearly significant trends in size from October to November

and December, but the data from January are not significantly

different from the October when a t-test is applied ( p)O .4).

This lack of significance may be partly due to small sample

size from the January data. However, inspection of the

size frequency data does indicate that the smaller size

groups of Phyllaplysia are absent in January. As February

and March samples had no specimens they are of no value in

estimating growth. It is concluded from these data that

--· ·------a significant increase in size occurred in the fall but

in the ~linter grm~th is probably arrested simultaneous

with a rapid mortality.

The information obtained from sampling for P. taylori

also permits some interesting observation concerning the

ecology of Zostera, the sole substrate for the entire life 39

cycle of the species. Plots of the mean lengths against time

show a rapid decrease in the amount of Zostera from November

to February and a large increase in March (fig. 18). The

Phyllaplysia abundance data also show a similar decrease

from October to March. Unfortunately, continued sampling

at this site was interrupted. However, these limited f------,--u-s-e-rvat-±-orrs-s-li-g-g-e-s-t-t-ha-t-c-ha-n-g-e-s-:i:-n-a-b-a-nd-a-nc-e of

are probably highly correlated 1'1ith events in the annual

life history of Zostera.

Plots of the natural log of the abundance of Phyl1aplysia

against the mean length of Zostera from November to February

show high positive correlation (fig. 19). However, when

the March data is considered this no longer holds true

because the Zostera abundance increases in March while P.

taylori abundance remained at zero. There are not enough

points to warrant statistical analysis but, the data available

suggest that either the mortality rate of P. taylori is

------strongly correlated to the decline in overall biomass of

Zostera or that some other factor such as water and air

temperature strongly influences events in both P. taylori

and Zostera populations. 40

DISCUSSION

Study of opisthobranch larval development is especially

valuable as a means of providing further information to

resolve the problems of opisthobranch phylogeny (Ghiselin,

1966). A few detailed works on larval development were

produced in the late 1800's and the early 1900's, in- r----c~------eluding one on the sea hare, Aplysia punctata (Cuvier)

(Saunders and Poole, 1910). Most studies dealt only with

cell lineage and seldom treated the post-trochophore develop­

ment (Casteel, 1904; Carazzi, 1905). Interest in inverte­

brate larval development blossomed in the 1940's and 1950's

with the appearance of large and comprehensive works-by

Gunnar Thorson and Eric Rasmussen. Studies of planktotrophic,

lecithotrophic and direct developmental types in opistho­

branchs have been summarized by Thompson (1967). Studies

not included in this work and those more recently published

are listed in Table IV. ------

Although information on Scandinavian and Japanese

species has amassed in the last thirty years, study on

the eastern Pacific species has barely begun (McGowan and

Pratt, 1954; Bridges and Blake, 1970; Williams, 1971).

The majority of recent ~10rk on the opisthobranchs has been on nudibranchs. 41

Of that done on the more primitive opisthobranchs, the

anaspideans, most has concentrated on species of Aplysia,

the sea hare (Saunders and Poole, 1910; Ostergaard, 1950;

Thompson and Bebbington, 1969). Members of the Aplysiidae

along the northeastern Pacific coast consist of four species:

Aplysia californica Cooper, Aplysia vaccaria Winkler, u-----A/I_p-l-y-s-:t-a-re-t-i-e-ct-J:-e;-r-sa-a-B-e-e-ma-n-a-nG!.-P-R-y-l-1a-pJ..-Y-s-i-a-ta-y-l-o-ri ··------

The most literature is on A. californica, as it has especially

large neurons on which many neurophysiological studies have

been performed (Bullock and Horridge, 1965). The previous

description of developmental pattern for P. taylori is the

first for any of these species.

The preceding data on P. taylori in combination with

the qualitative data obtained by Beeman (1970b) represent

a still incomplete picture of its life history. Two genera- I tions per year, each with different life times have been observed. Thompson (1964) states that nudibranchs which

pass through more than one generation in a year are all

species which have a transitory food supply. Only incomplete

life histories have been analysed on several opisthobranchs

of this type. Thompson proposes that this type of opistho-

branch, like the annual species, have the ability of pre-

ferentially selecting a specific substrate, i.e., the adult ' 42

food. This enhances the establishment of populations in

areas favorable for post-larval development and maintenance

of the adult population. Swennen (1961) observed that the

veligers of Trinchesia aurantia (Alder and Hancock) will

metamorphose only if allowed access to a substrate composed

of the adult diet. Thompson states that this ability of

adult food substrates is proven in many species and

supported by circumstantial evidence in others. However,

all of the species he considers have a planktonic develop-

ment. Direct development, as in P. taylori, afford the

larvae a substrate favorable for the adult population

\'li thout requiring a searching phase and the loss of effi- I ciency in reproductive numbers which accompany it.

Observations on larval settling preferences of P.

taylori in the laboratory were,made. Zostera blades were

available to metamorphosing larvae in glass stender dishes.

------No quantitative observations on the degree of substrate

preference ~1ere made. However, once settled on glass, the

larvae were not observed to attempt to move on Zostera.

But, often, the larvae ~1ere observed to crm-11 from the

Zostera onto glass. These observations suggest that

specificity for Zostera as a substrate for larval settlement is not great. Thompson (1964) stresses the importance of post-larval diet as a factor in substrate preference in opisthobranchs. Phyllaplysia, unlike Aplysia, is not ' herbivorous on its substrate. The specificity of Zostera as a substrate for P. taylori may rather be accounted for from the casual observation that other large plants do not have the heavy growths of. diatoms on the~r surface that~------are found on eelgrass. Indeed, it is possible that R· taylori may enhance Zostera growth by grazing on its epiphytes and reducing the shading effect accruing from their growth on the blades. Shading and self shading is an important factor affecting the growth of plants (North,

1967; Horn, 1970). Because of the dependence of P. taylori on Zostera epiphytes for food, it is not surprising that decline of the eelgrass also results in reduction of the opisthobranchs abundance.

As mentioned, P. taylori reproduce in the spring,

-~------during a period of increasing groVJth of Zostera and again in the summer prior to the beginning of annual decline of the plant. The second generation of the opisthobranch thus faces a period during which its substrate declines to much loNer levels of abundance. It is possible that the shelled, crawling veliconch stage of P. taylori, present in late 44

August to November, during Zostera decline, may be able

to exist as a demersal juvenile stage, feeding on the bottom

and on remaining Zostera blades. It would be of interest

to examine the biology of P. taylori during its overwintering

generation in greater detail. The arrest in growth rate

of overwintering P. taylori suggest at the very least, that

food availabillty lS much reduced-.--Reducea-lrr~~~ati~n-in·------

winter months 'tlould certainly reduce growth rates of

microalgae and the lower winter temperatures would affect

growth rates of both P. taylori and its food. Further

studies on the ecology and feeding habits of early stages

of the opisthobranch would be needed to test the foregoing

1 hypotheses. I ] P. taylori is the first species of the Aplysiomorpha

to be shown to develop directly. Reviewing Opisthobranchia

species exhibiting direct development, Thompson (1967)

concludes they are all species of either small adult size

~------or boreoarctic distribution. P. taylori does not fit

either of these criteria and is thus an exception. A list

of fate of velar structures, in accordance with the summary

set up by Thompson (1967) for the other ten direct developing

species follows: Velum Subvelum Shell Operculum present in present appears appears in embryo, in embryo embryo, cast regresses and after before hatching before hatching hatching up to 60 days

Larval retractor Larval kidney muscle appears irrt:mbTy-o.-----..a.weaTI>~-u-e-mb-ry-o·-,------­ regresses after hatching

Ghiselin (1963) suggests that direct development is a response to partial isolation from the sea and the minute size of adult animals. P. taylori fits the former explanation and contradicts the latter. He also suggests that laying few eggs is a characteristic of directly developing species.

However, examination of the data on species reviewed by

Thompson (1967) shows P. taylori not to be a single exception to this criterion. Direct development is advantageous to species which feed on an isolated, fast reproducing food source (Hadfield, 1963) and P. taylori most appropriately fits this criterion.

Direct development, such as that observed in P. taylori, may lead to genetic isolation of populations providing that migration of adults between them is not too great. In 46

a species having two generations per year, isolation

resulting from selective pressures in particular environments

may develop rapidly. Different populations, of P. taylori

differ in the presence and absence of the adult shell.

Populations studied by Beeman (1968) had a shell. Those

studied by Dall (1900), McCauley (1960), and the populations l----,o-b-s-e-r-ve-S.-i-n-'Pem-a-l-e-s-a-nEi-BeEl-e-g--a.-Ba-y-flaQ-ne-s-ke-l-1-.-'r-he-s-e------

differences may be due to selection pressures affecting

development in isolated populations in different types of

environments. In view of the fact that a general trend

in the evolution of opisthobranchs has been the loss of

the adult shell, further studies of P. taylori populations

differing in shell presence may shed light on the selective

factors that have affected this characteristic.

------

' 47

SUMMARY

1. P. taylori forms a highly organized, compacted, o-... -.. -.-

double layered egg nidosome.

2. Egg capsules contain a single ova and a nutritional

body, unknown in any opisthobranch development.

3. Larval development is direct, with no pelagic stage. r------.:__-===--:-==--::_::__:_::_::~-=-=-=--==-=----=--=--=-=--~--=-:.:__-~==-::--=----=--~---- - .. -· . Cultures at 17.5 • C hatch 27 days after oviposition.

4. Larval morphology is described from oviposition to

60 days post-hatching.

5. Veliconch growth continues up to 60 days post-

hatching. Final fate of the larval shell vvas not

determined.

6. Temperature experiments indicate that P. taylori can

develop at temperatures between 1o•c and 17.5•c.

7. P. taylori has two generations per year \'rith spa1,ming

periods in early spring and late summer.

8. Ecological data indicate a complex inter-relationship -----

existing among P. taylori, ~· marina, and diatom cover.

9. Other aspects of ecology and opisthobranch develop-

ment are discussed. 48

LITERATURE CITED

Baba, K. and I. Hamatani. 1952. Observations on the spawning habits of the Japanese Opisthobranchia t------__j~L)~ Publ. Seto. Mar. Biol. Lab. 2 (~,_:'----_8_.7_-"-9_0_. _____

Baba, K., I. Hamatani, and K. Hisai. 1956. Observations on the spawning habits of some of the Japanese Opisthobranchia (II). Publ. Seto. Mar. Biol. Lab. 5(2): 209-220.

Beeman, R.D. 1963. Variation and synonymy of Phyllaplysia in the north-eastern Pacific (Mollusca: Opisthobranchia). Veliger. 6(1): 43-47.

Beeman R.D. 1966. The biology of reproduction in Phyllaplysia taylori Dall, 1900 (Gastropoda: Opisthobranchia: Anaspidea). Ph. D. dissertation, Stanford Univ. 231 p.

Beeman, R.D. 1968. The order Anaspidea. Veliger. 3(suppl.): 87-102.

Beeman, R.D. 1969. An autoradiographic demonstration of stomach tooth renewal in Ph~llaplysia taylori Dall, 1900. Biol. Bull. 13 (2): 141-146.

Beeman, R.D. 1970a. The anatomy and functional morphology of the reproductive system in the Opisthobranch mollusk Phyllaplysia taylori Dall, 1900. Veliger. 13(1): 1-31.

Beeman, R.D. 1970b. An ecological study of Phyllaplysia tay1ori Dall, 1900 (Gastropoda: Opisthobranchia) with an emphasis on its reproduction. Vie et milieu. 2l(la): 189-211. Beeman, R.D. 1970c. An autoradiographic study of sperm exchange and storage in a sea hare, Phyllaplysia taylori, a hermaphroditic gastropod. J. Exp. Zool. 175(1): 125-132.

Beeman, R.D. 1970d. An autoradiographic and phase contrast study of spermatogenesis in the anaspidean Opisthobranch Phyllaplysia taylori Dall, 1900. Arch. Zool. exp. gen. lll(l): 5-22.

Bergh, R. 1905. Opisthobranchiata der Siboga Exp. Res; Expl. Siboga, 50(1): l-248. il------'__.______------Bridges, C. and J.A. Blake. 1972. Embryology and larval development of Coryphella trilineata O'Donoghue, 1921 (Gastropoda: Nudibranchia). Veliger. 14(3): 293-297.

Bullock, T.H. and G.A. Herridge. 1964. Structure and function in the nervous system of invertebrates. W.H. Freeman and Co., San Francisco. Vol. I and II.

Carazzi, D. 1905. L'embriologia dell 1Aplysia e i problemi fondamentali. Arch. Ital. de Anat. e Embriol. 4: 231-305.

Casteel, D.B. 1904. The cell lineage and early development of Fiona marina. Proc. Acad, nat. Sci. Phila­ delphia. 56: 325-405.

Chia, F.C. 1970. Oviposition, fecundity, and larval development of three Sacoglossan Opisthobranchs from the Northumberland Coast, England. Veliger. 13(4): 319-325.

Cooke, A.H. A.E. Shipley and F.R.C. Reed, 1922. The Cambridge Natural History Vol. 3.

DiAsaro, C.N. 1966. The egg capsules, embryogenesis, and early organogenesis of a common oyster predator, Thais haemastoma floridana (Gastropoda: Prosobranchia). Bull. Mar. Sci. 16(4): 884-914.

Dall, W.H. ,1900. On a genus (Phyllaplysia) new to the Pacific coast. Nautilus. 14: 91-~2. 50

Davis, C.C. 1967. Emergence of veliger larvae from eggs in gelatinous masses laid by some Jamaican gastropods. Malacologia. 5: 299-309.

Davis, C.C. 1968. Mechanisms of hatching in aquatic invertebrate eggs. Ocenaography and Marine Biology Annual Review. H. Barnes (ed.), G: 325-376.

Davis, H.C. 1963. The effect of salinity on the temperature tolerance of eggs and larvae of some lamellibranch molluscs. Proc. XVI Int. Cong. of Zool. 1: 226 p.

Dehnel, P.A. 1955. Rates of growth of gastropods as a function of latitude. Physiological Zool. 282(2): 115-144.

Eales, N.B. 1921. Aplysia. Proc. Trans. Liverpool Biol. Soc. 35, memoir 24. Liverpool University. 184-266.

Eales, N.B. 1944. Aplysiids from the Indian Ocean, with a review of the family Aplysiidae. Proc. malac. Soc. London. 26(1): 1-22.

Eales, N.B. 1960. Revision of the world species of Aplysia (Gastropoda: Opisthobranchia). Bull. Brit. Mus. (Nat. Hist.). Zool. 5(10): 267-404.

Engel, H. and N. Eales. 1957. Species of Aplysia belonging to the subgenus Tullia. Beaufortia. 6(69): 83-114.

Fischer, P. 1870. Observations sur les Aplysies. Ann. Sci. Nat. Zool. 5(13): 1-8.

Fretter, V. 1967. The prosobranch veliger. Malacol. Soc. London, Proc. 37(6): 357-366.

Fretter. V. 1972. Metamorphic changes in the velar musculature, head and shell of some prosobranch veligers. J. mar. biol. Ass. U.K. 52: 161-177. 51

Frings, H. and C. Frings. 1965. Chemosensory bases of food-finding and feeding in Aplysia juliana (Mollusca: Opisthobranchia). Biol. Bull. 128(2): 211-217. Ghiselin, M.T. 1963. On the functional and comparative anatomy of Runcina setoensis Babe, an Opisthobranch gastropod. Publ. Seto. Mar. Biol. Lab 11(2): 389-399. Ghiselin, M.T. 1966. Reproductive function and the phylogeny of opisthobranch gastropods. 1------i:-,aracologia. J{3_)_:_3~i-378~.------

Habe, T. 1953. Studies on the eggs and larvae of the Japanese gastropods (4). Publ. Seto. Mar. Biol. Lab. 3(2): 161-167.

Hadfield, M.G. 1963. The biology of nudibranch larvae. Oikos. 14(1): 85-95. Hamatani, I. 1962. Notes on the veligers of Japanese Opisthobranchs V. Publ. Seto. Nar. Biol. Lab. 10(2): 283-292. Hamatani, I. 1963. Notes on the veligers of Japanese opisthobranchs VI. Publ. Seto. Mar. Biol. Lab. 11(1): 125-130.

Hamatani, I. 1967. Notes on the veligers of Japanese Opisthobranchs VII. Publ. Seto. Mar. Biol. Lab. i5(2): 121-131.

Horn, H.S. 1970. The Adaptive Geometry of Trees. ------Monographs on Population Biology. 3. Princeton.

Hurst, A. 1967. The egg masses of veligers of thirty Northeast Pacific opisthobrancha. Veliger. 9(3): 255-287. Kay, E.A. 1964. The Aplysiidae of the Hawaiian Islands. Proc. malac. Soc. London. 36: 173-190. 52

Mac Ginitie, G.E. 1930. Notice of extension of range and of a new species of various invertebrates. Ann. Mag. Nat. !1ist. ser. 10, 6: 68. ---- ~: Mac Ginitie, G.E. 1935. Ecological aspects of a California marine estuary. Amer. Midl. Natur. 16(5): 629- 765. Mac Ginitie, G.E. and N. Mac Ginitie. 1949. Natural History of Marine Animals. McGraw-Hill, New York. 473 p. t------==~=--~--::-:=-p-~-==-c:-=-----.~r-----,c::-:;---.::-::=:;-::~----;:-o~----;:c,--,--,~-----Marcus, E. and E. Marcus. 1955. Sea hares and side-gilled - -- -~­ slugs from Brazil. Bol. Inst. Oceanogr. Sao Paolo. 6: 3-48.

Marcus, E.D.B.R. and E. Marcus. 1957. On Phyllaplysia engeli. Basteria. 21(4-5): 53-88. Marcus, E.D.B.R. 1972. On the Anaspidea (Gastropoda: • 1 Opisthobranchia) of the warm t~aters of the western Atlantic. Bull. Mar. Sci. 22(Lq: 841-874.

McCauley, J.E. 1960. The morphology of Phyllaplysia zostericola, new species.· Proc. California Acad, Sci. Ser. 4.29(16): 549-576. McGowan, J.A. and I. Pratt. 1954. The reproductive system and early embryology of the nudibranch Archidoris montereyenais (Cooper). Bull. Mus. comp. Zool. Harv. 3: 261-276. Mileikovsky, S .A. 19"(1. Types of larval development in

marine botton invertebrates, their distribution ,------~ and ecolor:;ical significance: a re-evaluation. Marine Biology. 10: 193-213.

Moritz, C.E. 1936. The development of Tethys (Aplysia) protea. Yearb. Carnegie Inst. of Washington. 3~: 90. Morse, M.P. 1971. Biology and life history of the nudibranch mollusc, Coryphella stimnsoni (Verrill, 1879). Biol. Bull. 140(1): 84-~4. 53

North, 117. J. 1967. Intes;ration of environmental conditions by marine organisms. In Olson and Burgess (ed. ), Pollution and Marine Ecology. Interscience Publications. pp. 195-224 .

. Ostergaard, J.M. 1950. Spawning and development of some Hawaiian marine gastropods. Pacif. Sci. 4: 75-115.

Pilsbry, H.A. 1896. Aplysiidae. In Manual of Conchology. ed. G.11l. Tryon, Jr., Philadelphia. 16.

Pruvot-Fol, A. 1954. Mollusques opisthobranches. Faune de France. 58: l-46o.

Rasmussen, E. 1951. Faunistic and biological notes on marine invertebrates I. Vidensk. Medd. dansk naturh. Foren. Kbh. 1G7: 207-233.

Rasmussen, E. 1951. Fauni.stic and biological notes on marine invertebrates II. Vidensk. Meddr. dansk naturh. Foren. Kbh. 113: 202-249.

Raven, C.P. 1958. Morphogenesis: The Analysis of Molluscan Development. Pergamon Press, New Yorlc 311 p.

Saunders, A.M.C. and M. Poole. 1910. The development of Aplysia punctata. Q. J. microsc. Sci. 55: 497-539.

·scheltema, R.S. 1967. The relationship of temperature to the larval development of Nassarius obsoletus (Gastopoda). Biol. Bull. 132(2): 253-265. ------

Struhsaker, J.VJ. and J.D. Costlow. 1969. Some environmental effects on the larval development of Littorina cicta (Mesogastropoda) reared in the laboratory. Malacologia. 9(2): 403-419.

Swennen, C. 1961. Data on distribution, reproduction and ecology of the nudibranchiate molluscs occurring in the Netherland. Netherl. J. Sea Research. 1(1-2): 191-240. Thompson, T.E. 1958. The natural history, embryology, larval biology and post-larval development of Adlaria proxima (Alder and Hancock) (Gastropoda: Opisthrobranchia). Phil. Trans. R. Soc., London B., 242: 1-58.

Thompson, T.E. 1961. The importance of the larval shell in the classification of the Sacoglossa and the Acoela (Gastropoda: Opisthobranchia). Proc. malac. Soc. London. 34: 233-238.

Thompson, T.E. 1962. Studies on the ontogeny of Tritonia hombergl Cuvier (Gastrup-o-a-a:-:-ep:ts-t-h-o-b-raa;:n.:C-ei-h~i~a~1~.;-______Phil. Trans. Roy. Soc. B 245: 171-218.

Thompson, T.E. 1964. Grazing and the life cycles of British nudibranchs. 275-297. In D.J. Crisp (ed.) Grazing in terrestrial andmarine environ­ ments. Brit. Ecol. Symposium No. 4, Blackwell, Oxford. 322 p. ] Thompson, •r. E. 1967. Direct development in a nudibranch Cadlina J.aevis, with a discussion of develop­ mental processes in opisthobranchia. Jour. mar. biol. Ass. U.K. 38: 239-248.

Thompson, T.E. and A. Bebbington, 1969. Structure and function of the reproductive organs of three species of Aplysia. Malacologia. 7(2-3): 347-:380.

Thorson, G. 1946. Reproduction and larval development of Danish marine botton invertebrates, with special reference to the planktonic larvae in the

Sound (Oresund). Meddr. Kommn. Danm. Havunders. o_·_-----~ Ser. Plankton. 4(1): 523 p.

Thorson, G. 1950. Reproduction and larval ecology of marine botton invertebrates. Biol. Rev. 25: 1-45.

Werner, B. 1955. Uber die Anatomie, die Entwicklung und biologie des veligers und der veliconcha von Crepidula fornicata L (Gastropoda: Prosobranchia). Helga. wissenscn. Meersunters. 5: 169-217. 55

Williams, L.G. 1971. Veliger development in Dendrontous frondosus (Ascanius, 1774) (Gastropo~a: Nudibranchia), 14 ( 2) : 166-171.

Winkler, L.R. 1958. Metamorphosis of the shell in the ------California sea here, Aplysia californica, ------Cooper. Pacif. Sci. 12(4): 348-349.

--

-

' TABLES 57

TABLE I

SPAWNING OF P. TAYLORI REPORTED IN LITERATURE

Locality Numbers observed Month(s) Reference ------spawn observed

Humboldt Bay "thousands" January Mac Ginitie 1930

------Bodega Bay abundant April- present early study Sept.

Tomales Bay abundant April-· present early study Sept.

Elkhorn Slough nfe1/Jn Dec.- Beeman Feb. 1966

--- "large numbers" March- Beeman Oct. 1966

Newport Bay Oct.- Mac Ginitie June, 1935 height at Nov.

------TABLE II ------

P, TAYLORI DEVELOPMENTAL TIMES ----

AT 10°, 14.5° and 17.5°C ------Total Mean Hours Age

Stage l0°C 14.5•C 17.5•c

1-- Zygote o.oo hours 0.00 hours 0.00 hours ------2-- Blastula 3·17. days 3.06 days 2.30 days

3-- Gastrula 9.22 days 5.47 days 3.48 days

4-- Trochophore 17.20 days 8.34 days 5.32 days

5-- Early Veliger 23.24 days 10.43 days 7.66 days 6-- Late Veliger 43.59 days 17.16 days 13.02 days ------

7-- Hatching 69.38 days 39.16 days 26.98 days ----

~~-~:-__o __ _ 59 TABLE III

SUMMARY OF APLYSIID LARVAL DEVELOPMENT IN LITERATURE

Characteristics

species Aplysia punctata A. elongata {cuvier) - (Pease) A. Egg Mass

1. Shape filament, tangled filament, tangled

2. Size 0.5 mm diam.

+------~~ ._C_Ql_o_r~-----'------'Qr_ange -pink_____ gr_e_an ______

4. Ribbon length

5. Av. # ova per mm 200

6. Total # ova 135,180; severai 100,000 7. Ovum diameter 85 ;.<.

8. Capsule diameter 0.125 mm

9. # ova/capsule 4; 8-12 1

B. Larvae

1. Development type pelagic pelagic 1 2. Velar shell a. Color, yellow-brown; gold; red col. markings red col. .------b. Length

3. Embryonic period 11 days to hatching

C. Authority Thompson.l969; Ostergaard 1950 Thorson 1946; Eales 1921 60

A. bipes A. g·randis A. fasciata A. depilans (Pease) (Pease) Poiret L. A. ------

l. filament, filament tangled 2. 15 em circum. 3 em thick ye-1--J:-ev;-; ye--l-1-sv: ; brown brown 4. 5.25 m 5. 507 4oo 6. 742,720 25,877,400 3,308,000 7. 0.085 mm 8. triangular shape ---- 9. 7-15 43 25 B.

l. pelagic 2.

a. gold-brown; dark col. ------

b. 0.125 mm

3. 14-16 14-16 ------days; 25°C days; 25°C c. Ostergaard Ostergaard Thompson Thompson 1950 1950 1969 1969 61

------

------

--- '~ A. ,erotea A. parvula A. californica

Morch Cooper ~~ ··~ . ·~~ A. ------~-

l. filament, filament, filament, tangled tangled tangled 2. 1 mm width 0.5 mm diam.

~ ye-l-1-ow------pink 4. 5. 6. 10,000- 50,000 7. 100""" 8. ------9. 2-8 1-3 B. ---- l. pelagic pelagic

2.

a. ~-~

--- __ , ___ ii--~~-~-.

---- b. 250 Jl- 150,.c<.

3. 8-9 ------days c. Moritz Baba Winkler 1936 1956 1957

- -~---~~

------62

A. kurodai Dolabrifera Petalifera Phyllapl;y:sia (Baba) olivacea J2Unctulata ta;y:lori Dall A. Pease flat band flat band flat band 1. filament 10 mm wide 2. 1 mm diam. 4 mm wide

~ p±-n-k--- C-J.P._A, r ;y-e_ll_oJ'I ; gold; yellow brown brown 4. 24 mm 5-35 mm 27 per mm2 5. 6.

150.7 .,<-<- 7.

318 A"- 8. 1 9· 15-30 1-3 B. direct 1. pelagic pelagic

2.

a. yellow- gold

b. 0.125 mm 112,u.. 27 days 3. 9 days 5-6 days

present work c. Baba Ostergaard Hamatani 1956 1950 1962 63

P. engeli Notarchus N. leachii Bursatella Marcus striatus leachii var. pleii A. Q,uoy & freeri Rang Gaimard 1. flat band filament, filament filament, tangled tangled 2. 0.7 mm diam. 1 mm diam. 1.2 mm wide

3-. ye-1-~o:\hr- e:r_e_e_n :,c_e_llow brown 4. 8-18 mm 10 em 5. 6. 20,000 7. 6o..._ 0.07 mm 70-85 ""'- 8. 365-425 """'- 9. 1 15-25 12-14 B. . .

. 1. pelagic pelagic 2.

a. red-

brown ------

--- b. 0.09 mm 3. 6 days

c. Marcus Ostergaard Baba Davis 1972 1950 1956 1967 ·- ·----·· ______...._ __~-~~--~~~~~~~'""""'f~~~---...... - ...... --...... _ _ _...._

TABLE I:V

LITERATURE ON OPISTHOBRANCH DEVELOPMENT

Information Number of Locality ~luthority species

I description of eggA 41 Hawaii, USA C)stergaard, 1950 and larvae

I description of eggs 27 Japan llaba, 1952, 1956 and larvae

description of eggs 6 Japan Lbe, 1953 and larvae

description of eggs 8 kamatani, 1962, 1963, 1967 and larvae

I relating opisthobranch general world-wide ~.rhompson, 1967 life cycles to review diet

I egg masses & 4 Jamaica ])avis, 1967 veligers

egg masses & 30 USA-northeast J!urst, 1967 veligers Pacific

I 0\ development of 1 California, J3ridges & Blake, 1972 ~ Coryphella trilineata USA O'Donoghue

iii

11

1111 •

I Information Number of Locality ]Authority species

development of 1 Maine, USA ]Morse, 1971 Coryphella stimpsoni (Verrill)

description of 3 England IChia, 1971 ovisposition & development

development of 1 California, ]Williams, 1971 Dendronotus USA frondosus

0\ \Jl

ll I I •' I I !·'I'" -'1' "I , ii: 'i I '

I , il , 'I II Ill I 'I'· , I •

FIGURES

··-~------·--- 66

LIST OF ABBREVIATIONS USED IN FIGURES 1------~ --~--~-

Figure 1. Phyllaolysia taylori range and recorded spawning sites. • = range extremities; spawning sites = 1, Humboldt Bay; 2, Bodega Bay and Tomales Bay; 3, Elkhorn Slough; 4, Newport Bay.

------~---- .::··; .·:·· .· ·. f •.. ·...... f ------/. ~... ·.· ______:______r PACIFIC 1 USA OCEAN f.;:::.·.. .··...... f 2

..

... · .... :~:MEXICO .·. --- :'

Figure 2. Phyllaplysia taylori egg mass.

------68

nb

0.16mm

------1------~------

Figure 3. Early veliger of P. taylori. prv

pov

pk mo

Is fg

0

rmd

;; -- st lmd

0.1mm "------~------

Figure 4. Late veliger of P. taylori.

-----··-- 70

sk e

h ac

mp

0.1 mm 1------··

Figure 5. Metamorphosed veliger of P. taylori. 71

nb h

Is

st

sc lmd

0.1mm ~------

Figure 6. Veliger musculature of P. taylori.

] ]

~-- 72

st

\arm

-·~------.0.1mm 1------

Figure 7. Cephalic nervous system of P. taylori.

1

------~-- - 73

Is cg stat

e

0 mp

0.1 mm -- ...

F'igure 8. Hatched veliconch of P. taylori. od

= _ .....

- - . -----c_-- dd

it ~------

Figure 9. Veliconch shell of P. taylori. (A) dorsal view (B) ventral view. 75

co

E E (I) .-- > d

<( ~------

Figure 10. Regression analysis of post-hatching shell growth of P. taylori veliconchs.

--- X: !{) ,.-- ,.-- 0 0 • 0 co + (Y) ,- 0 en (Y) 0 0 c (Y) (j) 0 " • 10 ..c·- d 0 0 u • II II v +-' ~ L a. 0 • 0 ..c -- I

+-' ------""' (/) 0 ------0. 0 (Y) (/) 6' -o 0 C\1

~~

-----

--~-~--

------,-0

------

------

!{) 0 0 !{) 0 C\1 !{) C\1 ~-- --~--~-~ 0 • • !------~------

Figure 11. Comparison of developmental times of P. taylori at lO"C, 14.5•c and 17.5"C. 0 0 o ~, 17 .5•c; o = 1 4 .5 C; A= 10 C.

------

------I! .. I I' I ii I. '""'"" !!

hate hi ng

['-­ ['-- I. veliger

e. veliger trochophore

gastrula

blastula

zygote

I , ...... -- 0 2d0 400 600 ' 800 1000 1200 1400 1600 mean tota I hours age

·~------~·"·····--·-.... Figure 12. Effect of culture temperature on progressive developmental stages of P. taylori. 1800

1600

1400

~---~-t2c-o-

~. 1000 ::J 0 .r;

-0 800 0 +' i hatching 1 c 600 I I $ 1 E

400 late veliger

200 early veliger trochophore ·-----·--.. ...•blastuta 8 10 12 14 16 18 temperature oc Figure 13. Location of P. taylori sampling sites. (A) Tomales Bay and Bodega Bay, (B) Tomales Bay sampling location, (c) Bodega Bay sampling location. 79

122 0 56' w N i

36.16'N

5 km

l A

-

5km

::· ... ·· B

-

. -

c --"------­

...

Figure 14. Regression analysis of Zostera sampling unit and P. taylori abundance {a) November, 1971 data (b) December, 1971 data (c) January, 1972 data.

.. so

(a)

--~ 1800 0

0 y=817.72 +37.98x 1600 r=0.20 0.4 > p-::::.._0,2 E u 1400 I i ' !L ..c ...... 1200 0 Ol I' c @ 0

1000

~· -- @ ...... ~ N 800

0 0 ------600 0 -

0 0

0 1 2 3 4 5 6 Phyllaplysia abundance .81

(b)

- 0 1 2 3 4 5 G =~-~---- Phyllaplysia abundance Figure 15. Regression analysis of P. taylori abundance. ,______5.0 0 - • d u (/) 4.5 c 4.0 ,...... r- +c ...... , 3.5 0. I I"' y- t-46--e~e~-x • r= -0.95 u 3.0 ·- p<0.01 (/) ~ 0.. 1 u 2.5 I ..c~ 0...

L 2.0 - ..a D E • J ::I z

~ 1 .5 -- ~ - - 0 --- --

15 45 75 105 days L_ __

Figure 16. P. taylori sample mean lengths and 95% confidence i.ntervals. O=Oct.; N=Nov.; D=Dec.; J=Jan. 84

13 J

12 E ~----~E~~-;------~-----1------~---- 11 N

D 10 cg E. 9 0 ·-(/) ~ 0. 8 -0 - 0

f ------7

6

0 40 80 120 days Figure 17. P. taylori size frequency distribution.

--- ~ --~- -:::= -

15 - -

- ~ 10 - Oct. - r- ,-- 5 - r- f--- I . .-h ' 0 ' 5 10 ' 15

u 20 (/) >. 15 0.. u 10 Nov. >. _c 5 (L

L 0 .5 10 15 Q) _Q E z:::J 20 15

10 Dec.

··--~----- ·- ,~--- 5 - .

0 5 10 15

10 Jan.

5

0 10 15 SIZG em Figure 18. Zostera marina abundance measurements.

,

. 86

.~.i~------,.---1o_o_o1_l------l E u ·900 . o Nov. ..c: ...... , 800 oMar. cO'l (!) oDec. c 700 0 (!) ; E I 600 ' 0 I t.. (!) ~I ...... , 500 I II) oJon. ' 0 N 400 oFeb.

0 30 60 90 120 150 doys .

Figure 19. Inter-relationship of P. taylori and Z. marina.

. 87

4------~·~-'-~1~0 ...~J·--~------g- · • Nov. >. ..c (L 0.5 L (!) ..a E ::J c o.o c • De c. d (!) E -0.5

-c --

-1.0 eJ an.

400 GOO 800 1000

mean length Zostera em