Reference : Rio!. Diii!.. 153 : 98105.

(August,

THE

EMBRYONIC

1977)

DEVELOPMENT

PHILANISUS

OF

PLEBEJUS

THE

WALKER

MARINE

CADDIS

FLY,

(TRICHOPTERA:

CHATHAMIDAE)
D. T. ANDERSON
Zoology

Building,

Among

the few species

habitats

are

N.S.IV.

of insects

certain

family, the Chathaniidae.

C. LAWSON-KERR

Sc/zoo! of Biological

Sydney,

in marine

AND

caddis

Adult

Sciences,

University

of Sydney,

2006, @-1ustraiia

which
flies.

spend
These

chathamids

all or part

of their

trichopterans

inhabit

life cycle

comprise

coastal vegetation

a single

and their

larvae live and develop in intertidal

rock pools (Mosely and Kininiins,
1953 ; Riek,
1970, 1976) . The family, which includes four species, is confined mainly to New
Zealand
and adjacent
islands
( Chatham
Islands,
Kerniadec
Islands) , but one
species, Philanisus
plebeius Walker
occurs both in New Zealand
and along the
coast of New South Wales
( Riek, 1976) . The larvae of P. 15iebeius are well
known from rock pools in both localities.
The adult feniale of P. plebeius, which
has a strong pointed ovipositor,
was thought to lay its eggs among coralline algae
at periods of low tide (Rick,
1970, 1976).
Anderson,
Fletcher
and Lawson
Kerr ( 1976) , however,
have recently shown that the ovipositor
is used to insert

the eggs into the coelom of one of the arms of a starfish.

eggs of Philanisus
piebeius
at
e.rigua Lamarck.
The embryonic

Cape Banks,
development

The host species for the

N.S.W.,
is the starfish
Patiriella
of the caddis fly is completed within

the starfish coeloni, with escape to a free life as a first instar caddis larva.

The

present

and

paper

describes

the

the seasonal occurrence

embryonic

of oviposition

development

Thirty
Botany

large

January

Bay,

speciniens
to

Deceniber,

N.S.W.

of Patiriella
1976,

on

plcbeius

in the host starfish population.

MATERIALS

froni

of Plzilanisus

AND

METHODS

exigua

were

the

intertidal

In the laboratory,

the starfish

collected
rock

at monthly

platform

were

at

opened

Cape

intervals
Banks,

by removal

of

the aboral body wall, and the coelomic cavities of the arms were inspected for the
presence of Plzilanisus eggs (Fig. 1). The sex of the starfish was also noted.
Batches of Philanisus eggs obtained in this manner were treated in two ways.
After staging by direct observation of the state of development of the living
embryos, the majority of egg masses were fixed in Kahle's fluid (formalin: alcohol:
acetic acid, 6: 16: 1). Sonic batches of eggs were transferred to Petri dishes of
sea water and maintained at 2325
C, the water being changed every two days.
In these culture conditions, the embryos continued to develop normally, allowing
the timing of development and the external changes in the living embryo to be
recorded.
Fixed embryos
and benzene after

of different
stages were dehydrated
through
piercing the chorion with a fine needle.
The

were then mounted unstained iii Eukitt

external structure at each stage.

and used to elucidate

98

methyl
cleared

further

benzoate
embryos

details

of

EMBRYOS

OF

A MARINE

CADDIS

FLY

99

RESULTS

Seasonal

occurrence

Embryos

of Phila.nisus

plebeius

were

ol)tamed

from

starfish

hosts

in every

nionth of the year except the winter nionths of June and July, and the niidsuiiiiiier
month,

January.

individuals

The

nunibers

of host

were as follows : January,

starfish

in each

0 ; February,

nionthly

saiiiple

of 30

6 : March, 8 ; April, 2 ; ?vlay, 6;

Jtine,0 ; July, 0 ; August,2 ; September,8 ; October,8 ; November,8 ; December,1.

In the majority

of hosts,

only one batch

of eggs was found

in each host individual.

The eggs of a batch adhered loosely together and showed synchronous development,
indicating that they had resulted from a single oviposition.
The arm selected for
oviposition was random, showing no fixed relationship with the madreporite and
no discrimination of the sex of the host. In a few host individuals, two batches
of eggs

were

found

in different

arms,

one batch

being

advaiiced

in development,

the other early, clearly the result of separate ovipositions.

None of the starfish
examined were found to contain hatched, first instar larvae of Philanisus, although
on several occasions hatching took place shortly after the host had been opened.
The newly

hatched

host tissue.
immediately

larvae

were

very

active

and voracious,

attacking

It seenis likely that they eat their way out through

after normal hatching.

Embryonic

the dissected

the host body wall

development

In each batch of eggs, 3050eggs are grouped together in short strings (Fig. 2).
adhering loosely by chorionic contact.
When transferred to sea water in a Petri
dish,

the

dissecting

individual

eggs

of a batch

can

be sel)arated

by

light

pressure

with

a fine

needle.

FIGURE 1.
of the oviposition

The eggs of the marine

caddis
fly,
host, the starfish
Patiriella
exigna.

P/zthi;ziszis
/Iebeius, exposed
by
Abbreviations
are:
c, coelom;

dissection
o, ovary;

/e,
egg of Philanisus; and sf, stomach.
FIGURE

and e, egg.

2.

Part

of an egg

string

of P/zilanisus

plebeins.

Abbreviations

are:

cli, chorion;

100

D. T. ANDERSON

AND C. LAWSON-KERR

8.

EMBRYOS

In eggs observed

shortly

CADDIS

after oviposition,

stage of forming

a germ

band,

a long

of 0.27

mm.

diameter

OF A MARINE

101

when the embryos

each egg is ovoid,

The

FLY

yellowish

transparent

are still at the

and densely

chorion

which

yolky,

surrounds

with

the

egg

is, in contrast, almost spherical and has a diameter of 0.39 mm. As development
proceeds, the embryo enlarges to fill the space within the chorion.
The chorionic
diameter increases slightly before hatching takes place.
During the first three days of development, a blastoderm is formed at the
yolk surface

(Fig.

3) , the embryonic

primordium

elongate, segmenting germ band is formed

extends around most of the circumference

gradually

differentiated,

and an

( Fig. 4) . The segmenting germ band

of the egg along the ventral midline,

with the end of the abdominal

rudiment
approaching
the cephalic lobes.
The
mouthpart
segments,
thoracic segments
and first few abdominal
segments
can be
distinguished
at this stage.
During
the fourth
to sixth days of development,
the remaining
abdominal
segments

become

delineated,

the

cephalic

lobes

and limb buds develop on the mouthpart

enlarge,

antenna!

rudiments

and thoracic segments

form

(Fig. 5) . A pair

of large rudiments
of pro!egs also forms on the tenth abdominal
segment.
On the
seventh day, these limb buds increase further in length and begin to show podomere
delineation.
The mouthparts
become more closely grouped
together,
while the
thoracic limbs extend in a posterior
direction
beneath the ventral surface of the
embryo, which retains its convex curvature
( Fig. 6).

The embryo now performs a blastokinetic movement which reverses its curva
ture, from ventrally convex to ventra!ly concave, and is accompanied
in its
later

phases

by dorsal

closure.

This

movement

takes

place

through

the

eighth

to

ninth days.
The first sign of blastokinesis
is a downturning,
tubu!ation,
and for
ward thrust of the posterior end of the abdomen ( Fig. 7) . This movement proceeds
until the entire abdomen is ventra!ly
flexed ( Figs. 8, 9) , the yolk mass being now

confined to the thorax

and anterior

part of the abdomen.

At the same time, the

bases of the thoracic limbs are shifted to a more lateral position on their respective
segments.
The stomodaeum
and the elongating
proctodaeum
also become con
spicuous during blastokinesis.
By the time the blastokinetic
movement
is complete
(Fig. 10), the posterior
end of the ventrally
flexed abdomen
is in contact with the head.
Dorsal closure

is complete,
and

the remaining

secretion

embryo,

of the

from

FIGURE

3.

cuticle

10 days

Philanisus

yolk is confined to the anterior

has

begun.

to hatching

The

reniainder

at 1718 days

plebcius,

blastoderm

plebeius,

segmenting

stage.

part of the abdomen

of the

development

is completed

Abbreviations

of the

in this

are:

bi,

position

blastoderm;

c, chorion; and y, yolk.

FIGURE

first

4.

Philanisus

abdominal

segment;

ci, cephalic

lobe;

germ

band

ib, labium;

stage.

nib,

Abbreviations

mandible;

nix,

are:

maxilla;

and

ab1,

t1,

first thoracic segment.

FIGURE 5.

Philanisus,

plebeiu@, early

limb

bud

stage,

6 days.

Abbreviations

are:

ab3,

third abdominal segment; anz, amnion; ap, anal proleg; ci, cephalic lobe; nib, mandible; and
t@, third thoracic
FIGURE 6.

are:

an, antenna;
FIGURES

tions

segment.
Philanisus

are:

7 and

plebeius.

la, labrum;
8.

ahd, abdomen;

Philanisus

embryo

lb, labium;
plebeius,

an, antenna;

approaching

and t1, first

early

stages

and sdo,

serosal

blastokinesis,

thoracic
in

blastokinesis,

dorsal

7 days.

Abbreviations

segment.
organ.

8 days.

Abbrevia

I). T. ANI)ERSON

102

:\NI)

C. LAWSON-KERR

10.

9.

11.

ti

sg
13.

EMBRYOS

OF

A MARINE

CADDIS

FLY

103

( Figs. 11, 12). The yolk reserves are gradually resorbed, only a small remnant
persisting
capsule,

in the midgut
the first

and

when the larva hatches.

second

thoracic

becomes especially conspicuous

At hatching,

terga,

during

the emerging

larva

Cuticularization

the linibs

and

of the head

the abdominal

prolegs

this period.
(Fig.

13)

is a typical

trichopteran

larva

in

both structure and iiiovenients.

The niouthparts are functional, the larva crawls
actively using the thoracic limbs, and a house is quickly constructed using avail
able materials.

If left among

the tissues

of the dissected

house from pieces of broken starfish ossicle.

from

pieces

of material,

niainly

coralline

host,

Nornially,

alga,

the larva

makes

the larva forms its house

obtainable

in its rock

pool habitat.

DIscussIoN
The present work confirms the fact, first pointed out by Anderson,
Lawson-Kerr

( 1976)

, that

Pizilanisus

plebeius

oviposits

in

the

Fletcher

coeloni

starfish, Patiriella exigua, and completes its embryonic development

coelom before hatching and escaping as a first instar larva.
In the Philanisus
most

of the

summer

year,

for

month, January.

November)

plebeius

months

N.S.W.,
June

to autumn

(February

July

and

is less than three weeks, young

N.S.W.,

which

during
the

mid

( September

Since

to

the duration

larvae might be ex

and autunin.

data on the seasonal occurrence

at Broulee,

occurs

perhaps

the spring

to May) .

in the spring

in the host

oviposition

and

is active during

in the rock pools

Riek ( 1976) provides

Philanisus

winter

Oviposition

development

to be present

of Cape Banks,

the

and late summer

of enibryonic
pected

population

except

and

of a host

support

of larvae and pupae of

the concept

of two breeding

peaks at these tinies. He found that adults were present and young larvae were
abundant during the spring, but that fully grown larvae and pupae predominated
in December

and Jaunary.

sisted through

Gravid

adults

then

reappeared

in February

and

per

the autumn.

It is not known

at the present

time whether

the adults

of P. plebeius

have a short

or an extended breeding life, nor how the species overwinters.

The occurrence of
oviposition in May suggests that a larval population is maintained during the winter
months, emerging as adults in the following early spring. Overwintering by adults
following eniergence in late autumn is also a possibility.
Although the oviposition host of P. /lebeiusin New South Wales is Patiriella
exigua,

it seems

likely

that

another

host

species

of starfish

is utilized

in New

Zealand, since P. exigua does not occur there (Anderson, Fletcher and Lawson
Kerr, 1976). The identity of this species reniains to be established.
The work
FIGURE

9.

abd, abdomen;

P/zilanisus

plebeius,

later

stage

in

blastokinesis,

9 days.

Abbreviations

are:

10 days.

Abbre

ti, thoracic limb; and i', yolk.

FIGURE 10.

P/zilanisus

plebeius,

blastokinesis

and dorsal

closure

complete,

13 days.

Abbreviations

viation is: e, eye.

FIGURE 11. P/zilanisus
hindgut; and v. yolk.
FIGURE 12. Philanisus

plebeius,
plebeins,

embryo
embryo

at

at 17 days,

with

chorion

are:

f, foregut;

removed.

Ii.

Abbreviations

are: he, head capsule; sg, salivary gland; and t', t2, thoracic segments.
FIGURE 13.

Philanisus

plebeins,

newly

hatched

tions are: a/', anal proleg; br, brain; Ii. hindgut;

gland; and t', t@,I', thoracic segments.

larva,

18 days after

oviposition.

izig, midgut; pr, proventriculus;

Abbrevia

sg. salivary

104

D. T. ANDERSON AND C. LAWSON-KERR

of Riek
( 1976)
also shows that the females
of the other
three
species
of
Chathaniidae,
Philanisus
fasciatus
in the Kerniadec
Islands,
the brachypterous
Chathanila
brevipennis
in the Chathani
Islands and Chathamia
integripennis
in

northern New Zealand, all have a strong pointed ovipositor similar to that of
P. plebeius.
It therefore seems likely that each species is associated with one
or more

species

of starfish

as an oviposition

larva similar to that of P. plebeius.

host.

C. brevipennis

has

a rock

pool

The larvae of the other two species have not

yet been described.

It is perhaps significant that the oviposition

has

an unusual

state

breeding

pattern,

of reproductive

opportunistically

in which

maturity

host of P. plebeius, Patiriella

adults

throughout

of both

the year,

from time to time in response

sexes

with

maintain

spawning

to appropriate

exigua,

a constant

taking

place

environmental

con

ditions ( Lawson-Kerr
and Anderson,
unpublished)
. The coelomic cavity of the
host species is thus not subject to the cyclic variation
of gonad expansion
and
reduction
that takes place in starfish species with an annual breeding cycle and a
limited spawning season.
The oviposition
hosts of the other chathamid
species may

or may not show this phenomenon.

In spite of the unusual ovipostion site of P. plebeius, the eggs and mode of
embryonic development of the species retain the typical trichopteran pattern.
The
only trichopteran species whose embryonic development has been studied in detail
is Stenopsyche
grisei@ennis,
recently investigated
by Miyakawa
grisei/'ennis
oviposits on rock surfaces in freshwater
streams.

than that of P. plebeizts, being 0.56 mm in length,

with hatching

markable
of this

taking

place after

invaginate
stage

formation

can be made

12 days

but develops

more

Miyakawa

describes

at 1621C.

of the embryonic

for P. plebeius,

primordiuni,

due to a lack

Once the segmenting

germ band has begun to elongate

yolk

the

mass,

however,

development

of the

manner.

The only notable difference

plebeius,

0.27

onto

the

mm

dorsal

surface

of development
dorsal
space.

closure,
This

P. plebeius.
nient

in length,

son, 1972;
of

pterygote
during

of the yolk

in which
niovenient

Wall,

any

1973),

manner.

but differs

related

position

relationship

problem

of maintaining

germ

stages.

of the

in a similar

egg size in P.

band

in S. griseipennis.

extends

The

by a blastokinesis,

with

further

middle

period

accompanied

enclosed

within

move

(e.g.,

Ander

in that the entire

the

embryo

in

by

the egg
days
in

blastokinetic

Lepidoptera

yolk

the

usual

much of the yolk mass is left outside the embryo

later

through

the mouth

of P. plebeius, therefore,

normally
Possibly

in sea
the

P. plebeius

the

in the

rock

water
major

and
pool

(Anderson

and

shows no special structural

site for development.

between

eggs

proceeds

with the smaller

shared

to its intracoeloniic

dependence.

early

of the embryo
is reversed
within
days
in S. grisei@ennis
and two

to be consumed

to develop

of critical

froni that of Lepidoptera

is

a re

but no comparison

points out, the trichopteran

enibryo

In Lepidoptera,

closure,

continue

nutritional

than

rapidly,

over the surface

species

segmenting

movement

Wood, 1968).
The embryonic development
embryos

mass

(1975)

enibryonic

trichopteran

dorsal

modifications

associated
the

the curvature
occupies
three

As Miyakawa

the

two

in both species is characterized

is a specialized

niass

is that

(1973, 1975).
S.
The egg is larger

also

excludes

adaptive

its starfish
environment

The

fact that

the

possibility

advantage

host

of

of

the

ovi

lies in solving

into

which

the

the

the

larvae

EMBRYOS

hatch.

OF A MARINE

The eggs are loosely agglomerated

CADDIS

FLY

105

and would, if laid among weed, be sub

ject to wave dislodgement

and to dessication
during low tide.
The starfish coelom
provides a stable, protected
environment
for the embryos and eliminates
the pos
sibility of predation.
As far as we are aware, no similar oviposition
and embryonic
development
within
the body cavity
of an intertidal
invertebrate
host has
been reported
for any other species of insect.
A major unsolved problem is how
the newly hatched larvae escape from the host into the rock pool.
Some niodifica
tion of the normally
carnivorous
habit of a trichopteran
larva is presumably
involved.
This investigation
was supported
by a research
grant from the University
of
Sydney.
The advice of Mr. M. J. Fletcher on the taxonomy
of marine caddis flies
is gratefully
acknowledged.
SUM MARY

1. P. plebeius,
coelonl

a trichopteran

of a starfish,

and autumn

Patiriella

with marine
exigua.

intertidal

Oviposition

larvae,

occurs

oviposits

mainly

in

in the

the

spring

months.

2. In spite of tile intracoeloniic location of the embryos, the development of

P. plebeius follows an unmodified trichopteran mode, including the characteristic
blastokinesis.

Nutrients

are not supplied

to the caddis

embryos

by the host starfish.

3. Hatching takes place in the starfish coelonl after 1718days. The newly
hatched caddis larvae quickly escape to tileir rock pooi habitat.
4. The form of the female ovipositor indicates that other species of Chathamidae
utilize starfish species as oviposition hosts.
5. This mode of oviposition offers protection to the caddis embryos in the inter
tidal habitat.
LITERATURE
ANDERSON, D. T., 1972.

The

development

CITED

of hoiometaboious

insects.

Counce, and C. H. Waddington, Eds., Developmental

Academic Press, London and New York.
ANDERSON, D. T., AND E. C. Woon,

1968.

The

morphological

Pages

systems:

basis

of embryonic

in the Light Brown Apple Moth, Epiphyas postvittana

763793.

(Walk.).

ANDERSON, D. T., M. J. FLETCHER, AND C. LAWSON-KERR, 1976.

A marine

piebeins, ovipositing in a starfish, Patiriella exigua.

MIYAKAWA, K., 1973.

The embryology

(Trichoptera:

of the caddis

Stenopsychidae).

165242 in S. J.

insects,

Vol. 1.

movements

Aust. I. Zoo!., 16:

caddis

fly, Philanisus

Search, 7: 483484.

fly Stenopsyche

griseipennis

MacLachlan

1. Early stages and changes in external form of the

embryo. Kontyu, 41: 413425.

MIYAKAWA,

K.,

1975.

The

embryology

of

the

marine

caddis

fly

Stenopsyche

griseipennis

MacLachlan (Trichoptera:
Stenopsychidae).
V. Formation of alimentary canai
and other structures: general considerations and conclusions. Kontyu, 43: 5574.
MOSELY, M.

E.,

AND D.

New Zealand.
RIEK,

E.

F.,

1970.

E.

KIMMINS,

Trichoptera.

Pages

The Division of Entomology,

Melbourne University Press.
RIEK,

E.

F.,

1976.

1953.

The

Trichoptera

(caddis

flies)

of Australia

and

British Museum, London, 550 pp.

The

marine

741764 in

Commonwealth

caddis

fly

family

The

insects

of

Australia,

Scientific and Industrial

Chathamidae

(Trichoptera).

sponsored

by

Organization,
J.

Aust.

Entomol. Soc., 15: 405420.

WALL, C., 1973.

Embryonic

development

J. Zool., 169: 6584.

of two species of Chesias

(Lepidoptera:

Geometridae).