CONTRIBUTIONS '110 THE BIOLOGY

OF~ bEONJ.!ifi (GOULD)

(MOIJI,USCA, OPIS'I1HOBRANCIA)

A Thesis

Presented to

the Faculty of the Department of Biology

California State College at Hayward

In Partial Fulfillment

of the Requirements for the Degree

Master of Arts

by

Richard Antone Ajeska

May 1971

ACKNOvlLEDGMENTS

It is to my loving y,rife, Ingrid, that this work

is dedicatedJ for it represents the culmination of all

that we have both strived for.

For making this undertaking a rewarding experience

I wish to thank the members of my committee, Dr. James

Nybakken, Dr. John Harville and Dr. Jack Tomlinson. A

special debt of gratitude is due Dr. Nybakken, who has

unselfishly offered his advice, encouragement and

assistance throughout the past five years.

I also wish to express my thanks to the director,

Dro Robert Arnal, the staff and the faculty of the

Moss ~anding Marine Laboratories, who have willingly

made available to me the full use of the facilities

at their disposal.

TABLE OF CONTENTS

INTRODUCTION ••••••

STUDY AREA ••••••.•••••••..•••••.. e o o • b o e • e e G e e e e

POPULATION STUDIES ••••••••••••• o e e e e • 0 o e • • o e • e e

PAGE 1

4

8

MATING AND FEEDING POSITIONS••••••••••••••••e0o 13

RESPIRATION RATES •• e•••o••••••••••••••••••••••• 17

FEEDING BEHAVIOR AND DIET•••••e>••••e"••••••e····18

PREDATION ON M. LEONINA•••o•••••••••••• -- ---~~· 25

COMMENSALISM e e ••••••• " •• ~ •••••••••••••••••• ·• •• • 27

DEFENSE MECHANISMS OF M. LEONINA •.•••••. 30

DISCUSSION ••••••• ¢••••••••• & e o e e e ' e a e c e c o e e e e • 1 31

SUMMARY AND CONCLUSIONS. • • o • • eo • o eo e • • • e • • • o • • • 33

LITERATURE CITED •• o e o e o e e e t & • o o o a o e & e e e e e t • o s e o 37

APPEriDIXc Cl €' e e a e G. 0 •• 0 ... e 0 •• 0 •• 0 0 •• $. 0 •• 11J 0 Cl 0 Cl •• c 38

iv

LIST 01" FIGURES

FIGURE PAGE

Melibe leonina on its normal substratum 3

2. Study area· map ••••••.•• e •• Q................... 6

3. Abundance of Macroq_y~~is ini~gri:(olia in a

25 square meter quadrat from study area A ••• 7

4. Maximum number of M. leonina at fifteen

stations fr·om area B • G ••••••••• e •• 0 •• 0 •• ". • • ]_l.,L

5· Resting and mating positions of !Vi. le_Q_n~_na_ •••• 16

6. Respiration rates of M· leol'}_tn?:. plotted

against vvet body weight ••••.••••••••••••••• " 19

7• Beginning of the feeding movement (adult

Nl@ l~onina) e••••"••• •• •• •••••• • • • •• • ••• • • • • • 21

8. Downward sweep of the hood during feeding

(adult M. leonina) ••••• o ~ •••••••••••• ~ •••••• 21

9· Oral hood about to close ou:ring feeding

(adult M. leonina) ••••••••••~ce••••••••••••• 22

lOe Position at completion of feeding movement

(adult M. leonina) •••••••••••••••••••••••••• 22

11. Characteristic feeding position of juvenile

IV1 e ]~ e 0 nina •.. e 0 • e 0 • e • 1ft • • • •• G $ Cl 0 G • c $ e 0 e • fJ 0 $ • • 2 3

12. Diet composition of three size classes of

M • 'l e 0 nina 9 C Q Ci 0 0 9 II t'O G 0 e t- 0 G Q 0 0 llJ G t1 G ~ e C & 0 It! t C 41 I e Cl 26 ....,..,=-=....,_--

to a iv1.. leonina 29

v

LIST OF TABLES

TABLE PAGE

1. Population statistics from a sample of

fifteen stations in study area B ••••G•••• 9

2s Number of M. leon~2 marked with methylene

blue dye in study area B •••••••••••••••~· 11

J.. Raw data showing total number of !'1· ~ina

at each of fifteen stations in study

area B •• e ., •• c • e ~ •••• c ., • • • • • • • • • • • • • • • • • • .. l,tQ

vi

1

INTRODUCTION

Melibe leonina Gould, (Nudibranchia, Tethyidae) is a

nudibranch evolved to exploit a prey which is planktonic$

Originally described from Puget Sound by Gould (1852) as

Chioraera leonina, it occurs from Alaska to the Gulf of

California (MacFarland, 1966). The type of the genus was

described from the Cape of Good Hope by Rang (1829) and

since that time eleven species of Melibe have been

described from the Pacific and Indian Oceans (Agersborg,

192J). Melibe leonina is the only species found on the

west coast of North America$

The literature dealing with M. leonina is primarily

descriptivee Bergh (1892, 1904), one of the earliest

workers, dealt with the systematics and some of the

morphology of six new species of Melibe. One of those

dcsc:ribcd, M. ,pcllucida is now considered to be a synonym

of M• leonin§:• Heath (1917) described a new species,

Chioraer~ dalli (also a synonym of M. leonina) giving its

complete anatomy, including, for the first time, many

details of ihe nervous system. Agersborg (i919) reviewed

the early literature on the genus Mel~j:>e and provided some

natural history notes on the species M. l~~na. In later

papers (1921, 1923) he dealt with the systematics and

morphology of 1!1• leo!l!rl§) the latter paper included a good

deal of histological worke O'Donoghue (1921, 1922), in a

survey of nudibranchs of the Puget Sound area~ offered

2

some natural history notes on M. leq_~_, referring to it

as Chioraera leonina. MacFarland (1966) was the first

author to give a morphological description of M· leonina

from the Monterey Bay area. His work affirmed its

synonymy with M. pellucida and c. ~ and described some

morphological characteristics not covered by the earlier

workers. Hurst (1968) was the first to describe, in detail,

the feeding behavior of adult M. leonina from the Puget

Sound area.

The family Tethyidae comprises two genera, Teth;y_§.

Linneaus and ~ibe Rang and includes some of the few

known plankton-feeding nudibranchse Melibe leonina has a -"""""'~~~~-

typical limaciform body and five to six pairs of dorsal

cerata into which the digestive gland has ramified. The

anterior portion of the body (presumably the ancestral

frontal veil) has been tremendously expanded into a hollow,

hemispherical organ, the oral hood, capable of entrapping

planktonic prey. The outer and inner margins of the oral

hood$ respectively, are supplied with a series of long and

short cirri which serve to prevent the escape of prey from

the oral hood during feeding (figure 1). The oral hood

and cirri are richly innervated and are extremely sensitive

to tactile'stimuli (Hurst, 1968)o M. leonina lacks both --~~~-

radula and mandibles although stomach plates are present

(Agersborg, 1923) and probably serve as a protective

lining as well as masticatory sturctures.

3

FIG. 1. Melibe leonina on its normal substratum (in Monterey Bay) the-kelp ~ysti..§. in~r~.foli.?.:_.

4

In Puget Sound the animal frequents Zostera beds and

can be collected by hand or dip net at low tide (Agersborg,

1921; Hurst~ 1968)e In Monterey Bay, however, M. ~na

appears restricted to the subtidal beds of the kelp

Macrocystis ~ifolia Bory. The nudibranch was found

to be restricted to the M. i~tegrifolia blades in an area

extending from the bottom to eight meters above the bottom.

The purpose of this study was to determine certain

aspects of the ecology of ~~ le~nina from Monterey Bay

occurring in M$ in}.§:_gri=r~ kelp bedso To correlate

labor-atory and field data so that one would complement the

other I attempted to observe the nudibranch~ as often as

possible, in its natural habitat. By doing so I hoped to

augment the literature by presenting facts not always

obtainable through laboratory observations alone. This

study covered a period of twenty months (July 1969 to

March 1971).

STUDY AREA

The. field study of Melibe leonina was carried out

exclusively in the extensive kelp beds of Macrocystis

~_gr~.Jol~~ which surround municipal wharf number tv10,

of the city of Monterey, Monterey, California (longitude

121° 53t 18" VI, latitude 36° 36' 24" N). The principle

study areas are shown in figure 2 as points A and B.

5

Areas A and B do not differ with respect to M.

inte~ifolia abundance or bottom topography. The average

depths of areas A and B were approximately ten meters and

twelve meters respectively. The extent of the M.

int~£_~ community is outlined in figure 2; this area

may shrink or enlarge according to prevailing seasonal

conditions. All observations were made between the bottom

and eight meters above the bottom.

The bottom within the study areas consisted of sandy

mud with very few projecting solid objects for algal

attachment. Other than Macro_s=:_ysti_s i~-~foJ::Ja the only

other conspicuous macro-algae were an occasional Costaria

costata (Turner) Saunders and Dess~§.lli .ill.~ Setchell

and Gardner. The M. i.D.!.EU?;:cifQ.!._i§:. beds near municipal

wharf number two are productive throughout the year with a

slight dying back of the upper portions of the pJants

during the vdnter months. However, during the study period

new growth was always apparent and replacement of spent

plants seemed quite regular. This is probably one of the

main reasons why .M.• J.eon~I.§_ regularly frequents these kelp

beds. Not only was this loc~lity well protected from the

open ocean, but it also afforded M. leo~ a suitable

substratum throughout the year.

An example of the abundance of fllas:x:Qs~ystif?_ .i.Ll_i§K~ililli

may be seen in figure 3 which is a diagram of a randomly

chosen twenty-five square meter quadrat within study

FIG. 2. wharf number outlines the kelp beds.

Study areas A and B adjacent to municipal 2, Montereyj California. The dotted line extent of the Macrocystis integrifolia

--=--=..-.-.1----"~ __ __,_:L ____ _

6

I I

/

.... -- ......

I (!} I B

'

j

\ \ \ I I I I I I I ! I I

I

0 I I I I yds 500

7

. FIG. 3· Abundance of M9:_S:!roc:tstJ:~ i!!~e~rifo];.ia plants 1n a 25 square meter quadrat from study area A. Each dot represents one M. iDJ;el!:J:i..:f_o_l:t~ plant consisting of a hold­fast and at least one stipe which lies 2 meters or more above the bottom.

@ 2

0 7

@j 3

I'~ w 8

@g ~----~~-----+-------r------~·----~

~ \;;,;)'

10

Q . 13

@ 11

~--------------5m--------------~

8

area A. A similar quadrat was established in study area B$

The area A quadrat was established April 22, 1970 and is

representative of both study areas with respect to M• integr).f2lia abundance. The plants within the quadrat were

cou11ted if they consisted of a holdfast and at least one

stipe projecting at least two meters above the bottom; it

was not necessary for the stipe to extend all the way to

the surface.

POPUIJATION STUDIES

As is the case with many nudibranchs, the relative

abundance of Mo leonina ranges in any single locality from

extreme abtmdance to complete absence" This appearance

and disappearance of entire populations has been doct:unented

by Swennen (1961) who studied distributions and occu1·rences

of nudibranchs of the Netherlands, and by Miller (1962) who

described the annual cycles of several species of

nudibranchs from the Isle of Man.

Rapid appearance and disappearance of entire popula­

tions of M. leonina within study areas A and B was to

happen often throughout the study period. Table 1 docu­

ments one instance of the events described abovee

It is well known the M· leonina· is a capable swimmer,

(Heath 1917; Agersborg9 1919, 1921; Hurst, 1968) and at one

time this nudibranch was thought to be a pelagic animal.

This, however, is not true. As stated by Hurst (1968)

.9

TABLE 1. Data tabulated from the total number of

M,illbe leg~ at 15 stations within area B.

Mean per Standard Estimated plant deviation Range populationC

Date xb

8~ 6-70 729 8- 9=70 722 8-15-70 726 8~23=70 723 8-30-70 708 9~10=70 712 9-15~70 716

10- 4~·70 7 30 10-11~70 713 10-18-70 700 11- 1=70 688 11- 8-70 698 11-22-70 0 11-29-70 0 12-13-70 0 12-29-70 0

1-10-71 77 1-24=71 106 2-13=71 126 2-27-71 136 3-18-71 133

48.6 48.1 Lj,8. 4 48.2 47~2 47 01~ 47o7 48.6 47e5 46.6 45.8 46.5 o.o o.o o.o o.o 5-l 7o0 8.4 9·0 8.8

s

44.9 44.8 45.3 44.1+ lf.le6 43.9 44.7 42.3 42.0 42.4 41.1 41.4 o.o o.o o.o o.o 4.2 5.0 4.5 4.9 4.9

R

1Ll·5 147 141 139 143 137 139 141 138 127 122 128

0 0 0 0

13 14 16 15 15

aCompiled from data--table 1 (appendix).

. bsum of the individuals on 15 Macrocxstis ~grifoli§:. plants.

EP

21,773 21,549 21,683 21,594 21, lLI-6 21:235 21, 3'70 21,773 21,280 20,877 20,518 20,832

0 0 0 0

2,285 3,136 3·763 4,032 3,942

cTotal population estimated on the basis of 14 M':lcr<;>cysti~ in.tegr.ifoJ_ia plants pE)r 25 square meters w~th~n an area of 800 square meters.

10

M• le~mina is rather reticent to leave its substratum and

will swim only when repeatedly irritated by tactile

stimulatiori to the posterior portion of the foot.

A similar behavior pattern was observed in the field.

During fifty SCUBA hours of field observations M. J-eg~

was seen freely swimming only rarely, and never during

daylight hours.

Since M .. leonina showed such fluctuations in abun-

dance it is pertinent to ask three questions: do individ-

uals move freely throughout a population, if so, where does

most of the movement occur, arid how do entire populations

move with such apparent ease?

To answer the first question five M• Jn~e_grj.folia

plants in study area A were marked with plastic, numbered

tags. The M. leonina found on these five plants were then

injected with methylene blue dye (table 2). The injections

were made, using a Yale 10 cc hypodermic syringe and

27 guage needle, into the heart region and also into at

least one of the larger cerata. The number of individuals

and their relative sizes were then recorded (small = 1

30 mm, medium = 31 to 80 mm, large = 80 to 120+ mm).

Prior to field marking, twenty M. leonina were --~-

injected with methylene blue dye in the laboratory,

following the same procedure described above. The sur­

vival rate three weeks after injection was eighty-five

per cente

to

11

TABLE 2. Total number of Melibe leonina marked with

1

2

3

4

5

methylene blue dye at five stations in area B.

3

4

2

2

1

3

3

0

2

1

2

4

0

1

1

3

3

1

2

1

12

Subsequent sampling at one week intervals for a four

week period showed that the marked M. ~ did move from

plant to plant~ although frequent mobility was not indi­

cated. It is most probable that the movement takes place

at night since no swimming !Y!• leonin8:. werEi observed during

daylight hours. Only five SCUBA hours of observation were

spent during night time hours and it was at this time that

the nudibranch was observed swimming freely, but only

rarely.

To determine where the movements within a population

took place$ careful records were kept of the number of

Me .,leonina at fifteen separate stations within study

area B<> Each station represented one !Y!• ~ri~

plant, consisting of a holdfast and at least one stipe

which extended to the surface. The plants were marked

with nQmbered; plastic tags.

Station number one was established at the outskirts

of the population with each successive station being

nearer the center. Station fifteen approximated the

center of the population. The plants were tagged along

an imaginary line by following a predetermined compass

heading.

During a seven month period the number of M. leoniD§.

at each station was counted at least twice a month. The

results indicate that the greatest amount of movement

takes place at the outer edges, while those more densely

populated central areas remain relatively stable with

respect to total number of individuals per plant

(figure 4).

13

The answer to the third question: "hovv do entire

populations move about with such apparent ease?" remains

unanswered& The population present in area B from

August 6, 1970 to November 11, 1970, in terms of numbers

of individuals; was the largest of any studied between

July 1969 and March 1971. The total population covered

an estimated eight-hundred square meters and numbered,

conservatively, twenty thousarid individuals (based on data

from table 1). This group was studied for a seventeen~week

period. Within eight days after the last observation

period (November 11, 1970) the entire population dis­

appeared, and was never again located. There was no

evidence of atrophy of individuals prior to the dis­

appearance and n~ indications of a massive die-off in the

wake of the disappearance. There is only conjecture as to

what happened in such an instance since there are no

substantive data available.

ffillTING AND FEEDING POSITIONS

The feeding behavior of M· ~ has been described

by Hurst (1968) and the mating behavior by Agersborg

(1921), both from laboratory observations. My own field

observations showed no apparent differences in either

14

FIG. 4. The maximum number of Melibe leonina at each of fifteen stations; expressed as a per cent of t~e range. (Data collected from August 6, 1970 to November 11, 1970).

1 0 0 ~--~-c--o---..

80

~ 0 60 0 -

40

20

o~~~--~_J--~~--~_J--~_J--~~--~~~

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 Station No.

15

behavior pattern from that described by the above authors.

No note has been made until now, however, as to the

animal~s physical attitude both during feeding and mating.

· While feeding the adult M. leonina holds its cerata

somewhat erect 9 the foot is firmly attached to the

substratum and the body is rather elongated. The oral hood

at this time reaches the full extent of its expansion

(figure 8). In successive feeding motions the hood is not

always cast directly in line with the body, but is extended

first to one side and then to the other. There is,

however, no set pattern, such as a right-to-left movement.

The direction of each feeding extension seems to be random,

both in the laboratory and field. The feeding behavior is

not a fixed action patternp for it is most definitely

dependent upon environmental cues for successful

completion. In the laboratory M• leonina will carry out

feeding movements even though there is a complete absence

of food. The mechanism which releases the feeding

behavior is probably contained within the digestive system.

The mating position differs in many r~spects from the

feeding position. While mating the cerata are pressed down

laterally along either side of the body, the cirri of the

oral hood are turned inward and the hood itself is pressed

close to the substratum (figure 5). As in most

nudibranchs copulation occurs in a head-to-tail manner,

since both the male (nd female reproductive organs of this

FIG. §., Typical position assumed by adult M~l~ }e.2ll,~ 'vvhile "resting" or mating.

16

17

hermaphroditic animal are located on the right side of the

body just below and in front of the base of the first cera.

Mating pairs must remain quiescent, and in the position

described above only a minimum of.effort is needed by the

animal to maintain its position in the environment.

A position similar to that of mating has often been

observed in solitary animals both in the laboratory and

field. This is most probably the resting position.

Mating seemed restricted to the daylight hours with

the evening hours devoted to feeding, but ju.veniles fed

actively during both daylight and night time hours.

RESPIRATION RATES

While observing M· leoJli!2.~ in the field and labora=

tory it was apparent that the young were much more active

than the adults. This fact has also been mentioned by

Hurst (1968). Several series of respiration determina-

tions were conducted to determine if this activity was

reflected in higher metabolic rates in the juveniles.

The respiration rates were made on a Gilson

Differential Respirometer. Standard methods were used.

The reaction vessels utilized (16 ml "ttotal volume) were ( .

filled with 10 to 12 ml of sea water, the potass1um

hydroxide was· placed in the side arm as a carbon dioxide

absorbent and one animal was placed in each flask.

Respiration was allowed to proceed for a minimum of 180

18

minutes. During this period the temperature was kept at

15 C ±0.5 C and the flasks were oscillated horizontally at

a rate of 78 oscillations per minute. At the end of each

series the microliters of 02 respired, total time of

respiration, (wet) weight of animal, temperature of

reaction flask liquid and barometric pressure were

recorded. The values of microliters of o2 respired per

gram-wet body weight per hour at standard temperature and

pressure (20 C and 760 mm Hg) were then computed.

The data sho"V"m in figure 6 indicate a higher

metabolic rate for the juvenile animals and a rate decrea.se

with an increase in size. These results, showing a higher

metabolic rate in the younger animals are in agreement with

laboratory and field observations of activity. A higher

metabolic rate in the young is reflected in their feeding

behavior which is different from the adult's and is

discussed below.

FEEDING BEHAVIOR AND DIET

The feeding behavior of M.· leonina has attracted the

attention of many investigators (Eliot, 1902; Heath, 1917;

Agersborg, 1919, 1921; Hurst, 1968; furchon, 1968). The

most definitive work on the feeding behavior of adult

NI. leont[la is that of Hurst ( 1968) in which she describes

in detail the nervous and muscular .systems involved in the

feeding process.

19

FIG. 6. Respiration rates of M. leonina expressed in microliters of Oz respired per gram-wet\ve"ight per hour~

D (]) L Q_

50

40

U) 30 (])

0:::

L .c

I

Ol I

::!... 20

10

Wet Body Weight (grams)

20

·While observing M· l~QP~ in the field a difference

between the feeding behavior of the very young (less than

25 mm) and the larger, more mature animals was noted~ The

mature animals feed, as noted by Hurst (1968), by pulling

back the oral hood so that it is nearly perpendicular to

the long axis of the body, the hood is opened widely and

thrust forward through the water. When contact is made

between any planktonic object and the inner surface of the

hood the hood is closed medially~ the inner and outer rows

of cirri interlocking to prevent the escape. of any entrap-

ped prey. The hood is then further contracted, forcing the

water out$ at the same time forcing the prey items toward

the mouth area where they are ingested. This feeding

pattern allows the animal to contact a maximum volume of

water through the sweeping motion of the oral hood (figures

.., 8 9 ~~~, , ,.., ' ( g $ , cu 1\.L ..... vI •

The smaller animals (2.5 mm to ?5·0 mm) show a

feeding pattern quite different from that described above.

The oral hood begins the feeding cycle nearly parallel to

the substratum, or at a maximum angle of 45° with respect

to the substratum. The hood is then extended out directly

in front of the body at a slight angle to the substratum.

As the animal moves forvvard the outstrea tched hood is

brought down against the substratum. Once contact is made

with the substratum the hood closes medially and the remain­

der of the pattern is identical to the ady.l t 's (figure 11)..

21

FIG~ 7• The beginning of the feeding movement of the oral hood (adult M· leQ_rina).

FIG. 8. The forward and downward sweep of the fully expanded oral hood (adult £1• leonir~~._).

22

(

FIG. 9· The oral hood, at the completion of foward movement$ about to close medially (adult !fl.o ,1eoninaJ.

FIG. 10. The oral hood has closed medially and is being drawn back to the starting position. At this point the cirri have interlocked and the water is being forced out of the hood (adult l'il. le_gnina).

23

\

FIG. 11~ Characteristic feeding position of juvenile M. leonina with the hood pressed close against the sub­stra turn.-·--

\'.........

214-

The latter pattern indicates that for the juveniles

it is more advantageous to dine directly from the

substratum rather than from the surrounding waters. The

M. j.nteg.r_ifolia blades provide an. ample supply of food

throughout most of the year in the form of crustaceans

and bivalve spat. During the winter and spring months

large numbers of harpactacoid copepods are found upon the .

M. integrifolia blades.

It appears that the juveniles are unable to encompass

a large enough volume of water, due to the ~mall size of

the oral hoodD to obtain sufficient food to satisfy their

energy needs. As a result the young~· leoniQ~ utilize the

M. in:t~g.ri:f~-assoc ia ted cope pods as their main food

source.

This method requires the juveniles to actively seek

out their prey~ unlike the semi~sedentary feeding method

of the adults. As a consequence the metabolic rate of the

young is higher than that of the adults. This is borne

out by the respiration data presented above.

To correlate metabolic rate and feeding behavior with

M. k.Qni.na's diet, gut analyses were made to determine

whether or not the diet of the young differed from that of

the adults.· The animals used for gut analyses were

collected from study area B and immediately preserved in

70% ethanol. Each individual was then measured along the

long axis of the foot. These measurements were made

before the tissues had hardened and shrunk.

25

After measurement the digestive tract was dissected

out and the contents tabulated. Thirty-seven animals were

dissec~ed, the largest was 80 mm in length and the smallest

was 3·5 mm. The diet was broken dovm into nine categories:

planktonic Ostracoda$ planktonic Copepoda, M. ~lj.§:.­

associated harpactacoid copepods, veliger larvae, zoea

larvae, megalops larvae" immature Bivalvia; immature

Gastropoda and Tintinnidae.

The results show a decided difference between the diet

of the young animals and the adults (figure 12). The

imrna ture M. 1~.2.llin.~ feed primarily upon the M o

inte.B;!:ifol.;...~§.=associa ted crustaceans~ whereas the adults

utilize the surrounding waters as their main food resource.

The change from a M· ,tn:f;e_gpl~9_;~associated diet to a

planktonic diet is dependent, in part, upon the size of

the animal and appears to take place between a size of

10 mrn and 25 mm. Once the animal reaches a size of 25 mm,

which is roughly equivalent to a weight of nine grams,

presumably it is large enough to begin feeding upon the

plankton.

PREDA':eiON ON M· LEONI!:!f.:

There have been no reports of· predation on M •. l~

in any of the past literature. In over fifty SCUBA hours

26

:F'IG. 12~ Diet composition of three Me leonipa size classes,.representing juvenile (0.5 to 9.9 m~inter~ mediate (10.0 to 24-.9 mm) and adult (25.0 to 80o0 mm).

aonly Me }j}tP:,_gr,ifQlli-associa.ted harpacticoid copepods.

bplanktonic copepods.

CPlanktonic ostracods.

100

roo +-'

+-' Q)

80 r- u 0 0 .D 0. 0 u 0 ll) u u 0 +-' 0 0 u 0.

u 0 > 0 0.

Q) - L L 0. 0 +-' 0 0 > lfl

I u CD 0 0

60 0 -0 +-' c: Q)

u L

(~

Q)

0... 40, 4~

c~ 4~ -

(

20

<

(

0

Symbol

0

0

®

(]) 0 >

Q) L

0 0

> (/') L 0 0. - 0 -0 0 Q) Ol 0 Q)

N 2

~ ~

Siz cia

e Number of ss individuals

o. 5-9 g.

10 24

0-9

25. 0-0 80.

Q) 0 > L 0

L (]) Ol

Q)

>

12

11

14

0

"8 0. 0 L +-' ll)

0 <.9

Q) 0 D c: c: +-' c: t--

27

of observation only five occurrences of predation were

notedc Three sightings were at night and two during

daylighto While five instances are certainly not con­

clusive it is of. interest that the observed incidence of

predation appears to be very low.

In all five cases the predator was the common kelp

crab E£g~ia ~ Randall. In each instance the

crab was actively feeding upon a M. leonj.n~$

Two captures by P. Q'fQS.Y~ were observede In each

instance the crab merely approached the nudibranch and

began tearing bits of tissue from the body until the

nudibranch left the Me ]:n:!&._gctf£lla blade. When that

happened the crab grasped its prey in one chela and

co11t_inued feeding with the other. P. Q.£QdUf:_t§.. showed no

preference for one part of the body over any other.

COMMENSALISM

Two organisms have been fotmd attached to the body of

M. leo:QillSJ:.• Once a single unidentified decapod megalops

was seen clinging to the body between the first and second

ceras on the right side. It was apparently dislodged

during collection.

The polynoid polychaete worm HaJ~pna ~§V~§eto~a

Kinberg has also been collected attached to the body, hood

and cera ta of M. 1ELPJ1i!}£ •. li. b:rev:.~!Q..§l\ is a cosmopol­

itan species which may be free~living or commensal with

28

other polychaete worms (Ricketts and Calvin, 1968). When

associated with M. J.~nin2!;_ the worm is an eggshell-white

color and blends fairly well with the color of the

nudibranch (figure lJ). The polychaete moves with ease

about the body of M. l§onin21:, and does not seem to prefer

one position over any other.

H. brevisetosa feeds directly upon the fecal matter

of Me 1£2~ and the digestive tract of the polychaete

assumes the same coloration as that of the lower digestive

tract of the nudibranch. Several laboratory observations

we,re made of He brevi.setosa feeding on the fecal matter '------ - -

of Mo ~~<1· This was accomplished by starving a

M. leonina and its commensal H. ~SE:tosa for two or

thiee days and then feeding the nudibranch the common

brine shrimp Arj;~ sal_ina. Prior to feeding both

digestive tracts were empty. After feeding upon A. sal_iQ_~

the digestive tract of the nudibranch took on a dark rust­

colored hue and as digestion proceeded the digestive tract

of H. breviseto3a also became a dark rust color.

When removed from M· leonina and placed in a one

gallon aquari.u..m with another M• le~mina the worm assumed

its position among the cerata as soon as a meeting took

place. This procedure was repeated ten times. The worm

did not appear to home to the nudibranch and all meetings

seemed fortuitous.

29

FIG. lJ. The commensal polynoid polychaete Halos:vdna brev isetosa attached to a ceras of Ill. leonina. ~-~-- ----- - -----

30

DEFENSE MECHANISMS OF MELIB];_ _I;~

M. _!eonina's main means of defense is its ability to

secrete a substance odorous to man and apparently repugna-

tory to ~me organisms. This secretion was first mentioned

by Agersborg (1921) who referred to the glands which

secrete this substance as the odoriferous glands.

In both study area A and B the most common large in-

vertebrate, other than M. leoY}ina and the kelp crab

P. J2TOdt~:9ta~ is the sunstar fycno:Q..~. h.§l.i~pthoides

Brandt. Since it was often observed attached to M ..

inte&rif.2lli.: plants well up on the stipe this starfish

could be a predator on M. Je~oniua. Experiments were

carried out in the field to determine whether or not

M. leonina would be palatable to I> bBianthoid~. Physical contact was made between a large hl• 1~9~~1

and a 43 mm f .. helianthoides. The starfish at once began

to move away. Repeated stimulation about the arms caused

them, in the area of contact, to be curled upwards and

towards the center of the aboral surface as P.

helianthoides retreated. This procedure was repeated

fourteen times, with different nudibranchs and starfish

each time. The results were identical for all fourteen

trials.

Next a large glass stirring rod (6 mm diameter) which

had been passed over the cerata and body of a ~1· l~912_ina~

was used to make contact with a P. helianthoides. The

results obtplined were the same as reported above. This

procedure was also repeated fourteen times.

As a control, a glass stirring rod which had not

31

made contact with M. leonina was used to stimulate P.

helianthoides. This procedure ·was repeated fourteen times

and although the contact elicited a response from the

starfish it was much weaker than the escape response

described above.

Edmunds (1968) reported pH factors as low as one for

certain dorid nudibranchso Secretions such as this would

certainly be repugnatorial to predators.

Determinations of the pH of the ectodermal secretion

of Mo 1&2.!'lirl§~ were made using Hydrion pH papers applied to

the body, hood and cerata. The pH was between 6oO and 6.4,

hardly acidic enough to be repugnatory to other organismsc

DISCUSSION

To gain a total understanding of a marine animal such

as M.§..L.ll?.~ J.e9-Dl:IL~ observations must not be restricted to

a single field area or to the laboiatory alone. In the

case of M,e l~52.r1ina it appears that there are important

behavioral differences between animals from the Puget

Sound area and those from Monterey Bayc Differences have

been observed in feeding behavior and habitat occupation.

32

As stated by previous authors {Heath, 1917; Agersborgp

1921; O'Donoghue 1921) Melibe leonina in the Puget Sound

region characteristically inhabit Zoster~ beds in

relatively shallow waters and feed directly upon Zostera-

associated crustaceans such as gammarids and other

amphipods. In contrast, in Monterey Bay the nudibranch is

found subtidally in beds of the kelp Ma_£:r;_oc;y_§tis

integr~foli~ and feeds~ in the case of the adults, directly

from the plankton-filled waters. The diet consists of

planktonic crustaceans such as copepods, ostracods and

various decapod larval stages.

Since the original description of Me leon.i!l_§: by Gould

(1852)f as QhiQ.rMra ~$ its taxonomic position has

been disputed& Morphological errors, related to the

nervous and reproductive systems, by Heath (1917) and

(Agersborg (1923) were corrected by MacFarland (1966).

However, it has not yet been decided as to which genus the

animal belongs 9 All knovvn members of the genus .M.§_li125l

contain strong mandibles except M. ksmina. MacFarland

(1966) contended that a character as obvious as this

should serve to place M. leoriina in a separate genus.

The matter remains to be resolved by a competent

systematist.

Even though the M· l~ni03! pop·ulations of Monterey

Bay and Puget Sound areas have no gross morphological

differences it seems that the different behavioral

patterns would serve to separate M. ~ into two

distinct geographical groups~

33

A more detailed survey of the Puget Sound region is

neeaed to determine the exact feeding habits of both im=

mature and mature animals before any comparisons can be

made with the animals of the Monterey Bay region.

One important question concerning ±!'!· ~.id1.§:. still

remains unansvvered: 11 How do entire populations move about

vdth such apparent ease?" There would seem to be a

releasing mechanism which initiates such "migrations", \ for sornt:~ means of communication is necessary to simulta=

neously cause the movement of an entire population.

Swennen (1961) and Miller (1962) described similar,

simultaneous appearances and disappearances of several

opisthobranch speciese These authors offered food availa-

bility and misrration to deeper waters as possible

explanations for population movements. However~ neither

of these seem likely as applicable to a sublittoral,

plankton=feedi.ng organism such as Me leQninc;,.

SUMIVIARY AND CONCIJUSIONS

The nudib:eanc:h Melib~ leonin:1Jl originally described

from the Puget Sound area where it iri.habi ts shallov1-water

Z2§.1§j:'a beds, occurs in Monterey Bay associated v;i th the

rather small groups. or it may be found in large

populations with very high densities of individuals per

plant. These two characteristic populations mentioned

above were studied in Monterey Bay near municipal wharf

number two, Monterey, California ..

34

It was shown, through field studies, that the nudi-

branch is mobile within a population and changes its

position within the group occasionally. The densities

of 1individuals per ~· integrifoli~ plant were measured

I

within a very large population.

Fluctuations in the number of ~· leon~ per plant

are greatest at the outskirts of a population and

decrease as the center of the population is approached.

The movement of individuals within a population probably

takes place during the night time hours by means of

swimrning.

Adl)J t M~ 1eonJ-n8. exhibit two characteristic positions~

feeding and mating/resting. The feeding position is

characterized by an erection of the cerata and a "casting"

of the oral hood in an attempt to capture planktonic prey.

During feeding the body remains in a fixed position while

the oral hood performs the feeding movements.

In the mating and resting position the nudibranch's

cera ta are ·pressed close against the body, the oral hood

is held down against the substratum with the cirri folded

inwards and the animal remains stationary.

35

Metabolic demands differ between young and adult

M. leo~., The immature animals, due to a more active

feeding behavior, have a metabolic rate which is higher

than that of the adults. The young, feeding directly from

the substratum must constantly change position in order to

encounter 11 fresh" areas" On the other hand, the adults

assume a semi-sedentary state when feeding, moving only

the oral hood., (

The young feed during daylight and evening hours,

whereas the adults seemingly feed only during the evening.

Differences in feeding behavior, which reflect

differences in metabolic rate, were substantiated by gut

analyses of young and adult animals. The diet of the

young consists mainly of M .. int~_grif2.1Ja-associated

organisms while the adults depend upon planktonic

organisms for the gt'"'ea ter part of their diet.

Predation upon M> ~ appears restricted to only

one invertebrate, the kelp crab pugetti~ nroducta. No

incident involving predation by vertebrates, such as

fishes~ which at times are in great abundance, was

observed.

On the other hand, the only other large, common

invertebratE) within M. leoni_na's habitat, ,Pycg.op2~

he].J..§l.Ehoides exhibits an escape response which is

released by physical contact with the nudibranch. This

is probably caused by a secretion of the odoriferous

glands which cover the epidermise

36

A commensal relationship between the polynoid poly­

chaete worm ~9~Xd~~ Q~Vi.~etosa and Melibe leo1~na

exists in which the worm feeds on the fecal matter of the

nJdibranch.

LITERATURE CITED

Agersborg, H.P.K~, 1919e Notes on Melibe leonina ' (Gould). Publications of the Pugetsounct--Marine Biolggic?-1. Station, 2; 2b9-277•

( ______ , 192le Contribution to the knowledge

37

of the nudibranchiate mollusk Melibe leonina (Gould). American ~~tur~~is1, 55, 222-253· -------

-----~--- , 1923o The Morphology of the nudibranchiate mollusca Melibe (syn. Chioraera) leonina (Gould). Quarterty Journal Mi9.rosc.Qi?icaJ: ~9e, 67$ 507~592.

Bergh, L.S.R., 1892. Die Nudibranchiata holohepatica porostomata. Verhandl~n~en __ g~r Zoolq_gJsehe -Botanischen Gesellschaft Wie1~»~ 1-1~

-~--~-~--~ , 1904. Nudibranchiata k1adohepatica l\'1elibe pellucida. In Sem~l'___,_,Rei~g_l_l_im _ _!.rehll?..~.1 der PhiliJJpinen ~ Wissenschaftich Resultate, 9(~5. -----~---~----

Edmunds, M., 1968. Acid secretion in some species of Doridacea (Mollusca D Nudihranchia). E.rQ_ceedtn;g& of the Malacologi<;:al $OQJ..§!~SL_o;f LondonJ 38, 121-133.

Eliot, C.N.E., 1902e On Some nudibranchs from Zanzibar. ]?ro~eeding&__QJ' the Zoo~.ogJcaJ~ __ $oc ie_!~ of London, 2, o2-72.

Heath, H., 1917. The anatomy of an eo1id Chioraera 2:fLill.. Procee~ of the Academy of Na~u:tib Science 9f Ph~ladel£hi~, 69, 137~148.

Hursta A., 1968. The feeding mechanism and behavior of the opisthobranch Mt~lib~~ 1.§':.2I!J:Da. ~JI!2.§J];1Jn o Ub.§~Q]..,SJ_gj~§:]:_§o cj e t L_2_f __ 1Q.D:§~9n , 22 , 151 ~-16 6 o

MacFarland!' F.Moli 1966Q Studies of opisthobranchiate mollusks of .the Pacific coast of North America. Memoirs of the California Academv of Science, b;l.:s"I~6.· .. 11------. -

Miller, M.c., 1962o Annual cycles of some Manx nudibranchs with a discussion of the problem of migration. Jourral of Animal EcolQ_gy, 31, 51.1-5= 569.

( O'Donoghue, C.H., 1921. Nudibranchiate mollusca from

the Vancouver Island region. Transactions of the _Boy'!l Can?J.diaD._lnstitute, Br 147='209.

38

, 1922. Note from the~Vancouver Island species and distribution. R9yal Canadian .]nstit}lt§_,

on nudibranchiate.mollusca region, III. Records of Transactions of the

14;l45=~fb7.

Purchon, R.D., 1968. Feeding methods in th~ Gastropoda, PP· 41-99· In R. D. Purchon, Th~__l?l_gl:Q.b;y~~ ~1o~.9.a. Pergamon Press: New York.

Rang, S.J 1829. Manuel des Mollusques, Paris, pp. 129=1)0.

Swem1en, c., 1961. Distributionp reproduction and ecolog-y- of the nudibranchiate molluscs occurring in the Netherlands. Netherlands Journal of Sea Research, 1, 191-240.

APPENDIX

40

( DATA-TABLE 1~ Raw data representing the number of

adult Me1i1:Je J.eqnir@ per station.a

-~ .. ~=- .......... _ -~--===-=-,...~---~~ -·

Station ntunber 1 2 3 l.r 5 6 7 8 9 10 11 12 13 14 15

--· ---~~ -·----="'~""·~-=<>===-----~---=.,...,.,..~

-~ 8- 6=70 3 0 Lj. 3 19 l.J.8 16 37 32 lOLl. 50 lh5 '78 109 81 8- 9-70 3 1 Lj. 3 18 l.t-8 16 38 30 100 53 1L!-8 76 101 83 8~16-70 2 0 1 3 16 46 12 36 31 98 6Lt· 14·1 81 111 84 8-23~'10 2 0 0 2 18 4·'·1· 1'2 -·.) Jl} 31~. 102 63 139 79 113 80 8~30-70 0 0 0 0 15 41 11~. 35 32 99 58 143 83 107 81 9=10=70 0 0 0 0 9 l~O 12 39 3.3 100 56 137 91 108 87 9=15-70 0 0 0 1 9 lH 11 41 Jl4. 102 53 139 90 1.10 85

10- 4-70 0 0 0 0 10 4.3 12 40 36 107 61 141 88 103 89 10-11-70 0 0 0 0 8 38 13 43 33 104 58 138 82 105 91 10-18=70 0 0 0 1 6 32 12 45 35 99 64 127 79 103 97 11- 1-70 0 0 0 0 2 27 13 hl.J. 36 10.3 59 122 83 1 n'/ 92 ~~,

11= 8-70 0 0 0 0 3 28 14 46 35 99 62 128 80 108 95 11-22-70 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 11-29=70 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12~·13-70 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 12-29-70 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 1-10~71 0 0 1 0 3 6 2 8 1 13 10 9 3 11 10 1-2l~-7l 1 3 0 3 4 2 7 14 6 17 11 5 8 13 12 2-13-71 0 0 2 4· 5 6 8 10 13 16 12 1.3 9 12 16 2-27-71 2 3 2 l~ 8 7 6 11 14 ll.t· 10 16 11 11 17 3-18=71 2 4 1 3 6 7 8 10 14 16 11 16 10 12 1.3

- ~~·--=-~--~-------

aEach station represents one ~.E:Qg.Y_~:tis ~.§:_t?,l-:_~foJJ.a.:. plant with a holdfa~t and at least one stipe which extends to the surface.