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APPARATUSES 0F SPEYERIA
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Thesis for ”no Degree of M. S.
MICHIGAN STATE UNWERSITY

Richard Arthur Arnold ‘
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ABSTRACT

THE COPULATORY.AND OVIPOSITIONAL APPARATUSES
OF SPEYERIA (LEPIDOPTERA; NNMPHALIDAB)

By
Richard.Arthur.Arnold

The morphology of the copulatory and ovipositional mechanisms
of Speyeria are described. The myology of the copulatory and ovi-
positional mechanisms is described, named, and homologized. Finally,
the sequential skeleto—muscular events of copulation and oviposition

are explained.

C\ THE COPULATORY AND OVIPOSITIONAL APPARATUSES
OF SPEYERIA (LEPIDOP'I'ERA: NYMPHALIDAE)

By

RiChard.Arthur Arnold

A.THESIS

Submitted to
Mfichigan State University
in partial fulfilhment of the requirements
for the degree of
IMASTER.OF SCIENCE

Department of Entomology

1975

TABLE OF CONTENTS

Introduction . . . . . . . . ..... . ..............
General Structure of the Abdomen . ....... . . . . . . . . . .
Female Segmentation . . . .................
Female Musculature Segments II-VI . ..... . . . ......
MaleSegmentation.... ........
Male Musculature Segments II—VII. . . ......... . . . .

The Morphology of S e eria Genitalia . . . . . . ..... . . . . .
The Male ExternaT Geni talia . . . . ....... . ..... .
NinthSegnent.......................
TenthSegment....... ..........

The Musculature of the Male External Genitalia. . . . . . . . .
ExtrinsicMuscles........... ......
Intrinsic Muscles . . . . . . . . .............

Skeleto—Muscular Mechanism of Copulation . . . . . . . . . . . . . .
The Fmale. O O O O O O O O O O I O O I O O 0 O O O O O O O O O

The Male. 0 O O O O O O O O O O I O OOOOOOOOOOOOO O
Skeleto—Muscular Mechanism of Oviposition. . ...... . .....
Annotated List of Male and Female Abdominal Muscles ...... . . .

MusclesofSegmentII............ ........ .

Muscles of Segment III ..... . ...............

MusclesofSegnentIV... ..........

Muscles of Segment V. . . . . . ..... . . . . .......

MusclesofSegmentVI.....................

Male Muscles of Segment VII . . . . ........ . . . . . .
Muscles Associated with the Female Genitalia ...... . .....

SegmentVII............ .....

SegmentVIII............. ........
Muscles Associated with the Male Genitalia ............ .

Extrinsic Muscles (Segment VIII). . . . . . . . . . . . . . . .
Intrinsic Muscles (Segment IX). . . . . . . . . . . . . . . . .

Endophallic Muscles . . . . ............. . . . . .
may. 0 O O O O O O O O O O I O O O O OOOOOOOOOO O O O 0
Literature Cited ..... . ....... . . ......... . .

ii

Figure

Figure

Figure

Figure

Figure

Figure

Figure

Figure

LIST OF FIGURES

Internal Right Lateral View of the Male Abdominal Segments
II-VIII and Associated Musculature

Internal Right Lateral View of the Female Abdominal Segments
II-X, Associated Musculature and Reproductive Structures

External Left Lateral View of the Male External Genitalia
and its Associated Musculature

Internal Lateral View of the Right Valve and its Associated
Musculature

Dorsal View of the Articulations of the Juxta, Valve, and
Saccus

Left Lateral View of the Membranous Areas of the Male
Genitalia

Left Lateral View of the Aedeagus and its Associated
Musculature

Internal Right Lateral View of the Posterior Segments (V II-
X) of the Female Abdomen with Associated Musculature

iii

ACKNOWLEDGEMENTS

I would like to express my gratitude to my major professor,
Dr. Roland L. Fischer, who carefully reviewed this dissertation.
His contributions and assistance during this study and my master's
program were most valued.

My guidance committee members should be acknowledged for
their counsel and direction in my master's program: Dr. S. N.
Stephenson, Dr. F.W. Stehr, Dr. R.L. Fischer, Dr. J .E. Bath,
and Mr. M.C. Nielsen.

Finally, I would also like to thank Mrs. Lana Tackett, who

helped me in the preparation of my preliminary drawings.

iv

INTRODUCTION

Lepidopterists have relied heavily upon the structural pecu-
liarities of Lepidoptera genitalia to clearly demarcate species.
The great diversity in structural detail of the genitalia has proved
of inestimable value for the identification of Lepidoptera at the
species level. Yet, little effort had been expended to understand
the operational mechanism of the genitalia during cepulation. Without
a functional analysis of the external genitalia, it is difficult to
determine how its components are interrelated, to properly assess
their adaptive importance, or to deterine their role in the evolu-
tion of the species.

This study reports on the morphology of the male and female
abdominal segments, the myology of the abdomen, and the operational

mechanism of copulation and oviposition in Speyeria atlantis

 

(Edwards), _S_. gy_b_e_l_e_ (Fabricius) and S. aphrodite (Fabricius) .

There have been very few studies on the functional morphology
of the external genitalia of insects. Kullenberg (1947) studies
the copulatory apparatus in Hemiptera. Bonhag and Wick (1953)

studied the common milkweed bug, Oncopeltus fasciatus (Dallas)

 

(Hemiptera: Lygaeidae). Kunze (1959) studied the morphology of the
genitalia in the Cicadidae. Fischer (1956) reported on the morphol-

ogy of the male Megachile fortis (Say) genitalia (Hymenoptera:

 

Megachi lidae) .

The morphology of the male copulatory musculature of relatively

l

few species of Lepidoptera has been described and these often in-
accurately. Snodgrass (1936 and 1957) briefly described the muscu-
lature of Carpocapsa pomonella (L.) and 30111ij mori (L.). Unfor-

 

 

tunately these two species possess rather reduced external genitalia
with some structures having been lost, and others apparently co-
alesced.

Forbes (1939) reported in detail upon the male copulatory

musculature of the noctuid, Septis arctica (Boisduval) , and added

 

some notes on the male copulatory musculature of seven other species.
Santer (1956) did the same for Solenobia, a psychid. Shirozu and
Yamamota (1953) studied the muscles, skeletal and membranous parts
of the male external genitalia of the nymphalid Argyronome 1aodice
j aponica (Menetries). Ehrlich and Davidson (1961) illustrate the
musculature of the male and female external genitalia of _D_a_r_iaus_
plexippus (L.).

Hannemann (1954a and 1954b) studied both the male and female
abdominal and external genitalia musculature of the Nymphalid,

Argynnis paphia (L.). He later (1957) described the male muscu-

 

lature for the microterygid, Micromegx calthella L. For each
species he described what he believed to be the role of the muscles
and components of the male external genitalia and female during
copulation. Steklonikov (1965) briefly described the morphology
of the copulatory apparatus in both sexes of four moth species.

The terminology pertaining to the structure of the male and
female external genitalia of the Lepidoptera has been subject to
much confusion. Several nomenclatural systems, many purely descrip-

tive in nature, have previously been set forth. Others have been

based upon the comparative morphology of the adults. In this paper,
the terminology as set forth by Klots (1970) has largely been fol—

lowed.

GENERAL STRUCTURE OF THE.ABDGMEN

The definitive abdomen of Speyeria consists of ten segments
in both sexes. Segments I4VII constitute the pre-genital area of
the abdomen. Segments'VIII—X, whiCh have been variously modified
to house and Operate the reproductive apparatus, constitute the
genital segments of the abdomen. The first abdominal segment is
partially suppressed and.can be easily overlooked. The pre-genital
area is comparatively rather short, rdbust, rounded and somewhat
depressed ventrally. The genital area is conical, tapering pos-

teriorly (Figs. 1 and 2).

Female Segmentation

 

In the female, only the tergum of the first segment is clearly
present, as the sternum is reduced. Sterna IIJVI are similar to
one another. Eadh is more or less rectangular in shape and slightly
bowed. Each successive sternum decreases slightly in length and
width, until sternum VI which is about half the length of sternum
II (Fig. 2). Sterna VII and VIII are elongate and conical caudally.
Segments IX and.X have fused and become modified to ferm the anal
papillae. The sterna and terga of segments IX and.X are not clearly
distinguishable (Fig. 8).

A well-defined antecosta is feund along the anterior margin

of sternal plates 114VII. The acrosternite, which extends anteriorly

4

from the antecosta as a narrow marginal flange in many insects, is
lacking on all of the sternal plates.

Between each successive sternum and tergum is the intersegnental
membrane, or conjunctiva. The intersegnental membrane is folded upon
itself in a non-extended individual, whereas, in an extended indi-
vidual the membrane becomes taut. This membrane is attached an-
teriorly to the trailing edge of the sclerite, and posteriorly on
the antecosta of the following sclerite, and allows a segment to
slide over the following segment upon two Opposing sclerotic surfaces.

A pleural membrane extends between each sternum and tergum of
the first through seventh segments. The sternum and tergum of seg-
ment VIII closely approximate one another due to the extreme reduc-
tion of the pleural membrane.

Terga II—VII are similar to the sterna in general organization
and appearance. Each tergum is rectangular in shape , successively
decreasing slightly in length and width through tergum VI , which
is about half the length of tergum II. On the anterior lateral edge
of terga VI and VII is a rounded, somewhat produced tergal apodeme,
to which the Tertiary lateral dorsal longitudinal mmscle attaches.

A conspicuous antecosta, onto which the longitudinal muscles
are attached, is found along the anterior margins of terga II-VII.
It is lacking in tergum VIII, and difficult to discern in the fused
ninth and tenth segments. Tergum VIII possesses the anterior
apophyses and segment IX possesses the posterior apophyses (Figs.

2 and 8) .

Female Musculature of Segments II-VI

 

With but minor variations the musculature of the abdominal

segments in the females of Speyeria atlantis, _S_. gbele and

 

S. aphrodite has been found to be essentially the same. Thus if the
above sampling of fritillaries in any manner indicates the myology
of the group, the following discussion on the mechanism of the pre-
genital Imxsculature of these three fritillaries, is likely to be
representative of the genus Speyeria and possibly other closely re-
lated genera. To eliminate the lengthymuscle terminology in the
text and possible confusion with figure references, the mmscles have
been desigiated by numbers in italics. Each muscle has its own
number, which is used throughout the text and figures, and may be
referred to in the annotated descriptive list of muscles found at
the end of this paper.

The pre- genital musculature of female Speyeria follows a definite
pattern which is repeated in segments IV through VI of the terga
and throughout the II through VI sterna (Fig. 2). Modifications in
this general pattern of musculature have occurred in the first ab-
dominal segment, due to its attachment to the thorax, and terga II
and III. The c0pulatory function of segments VII through VI have
likewise resulted in modification of the muscular pattern of these
segments (Fig. 8). There are 32 paired nmzscles in the six pre-
genital segments of these female fritillaries. The muscles of the
pre-genital segments fmction collectively as contractors of the
pre- genital segments, but operate individually as retractors of their

respective segments .

While the musculature of a few of the segments is dissimilar,
there is enough similarity in the various segments to warrant a
discussion of the muscular mechanism of the more generalized seg-
ments (segments IV, V, and VI). Thus, only those muscles of segments
IV, V, and VI are specifically mentioned. The homologs of these
muscles in other segments function in a similar manner, except where
otherwise stated. Variations in the general pattern of muscles in
other segments are noted later.

The contractors of the pre-genital segments all function in
the retraction of the tergal or sternal plates over one another.

The retraction of these individual plates results in the decreased

length or contraction of the pre- genital region. The Median dorsal

 

longitudinal muscles (_l_2_, lg, _2_6_), the Accessory median dorsal

 

 

1ggitudinal muscles 13, Q, _2_7_) , the Primary lateral dorsal

 

 

longitudinal muscles (14, _2_l_, Z._8_) , the Secondary lateral dorsal

 

 

longitudinal muscles (_1__5_, _23, 29) , and the Tertiay lateral dorsal

 

logitudinal muscles (_l_(_>_, g, 39) , all serve as tergal retractors

 

(Fig. 2). The Ventral lglgitudinal muscles (_1_§, _2§_, 3g), and the

Lateral ventral longitudinal muscles (11, _21, 31) , serve as retractors

 

of the sternal plates. (Fig. 2).
The musculature of terga II and III is similar, except that

the Tertiary lateral dorsal longitudinal muscle (the homolog of 16)

 

is lacking in segment III, while in tergum II neither the Secondary

or Tertiary lateral dorsal lorgitudinal rmiscles (the homologs of 9

 

and _16) are present (Fig. 2).

Male Segmentation

 

In contrast with the female, the tergum and sternum of the
first segment are both present. Sterna II through VIII are similar
to one another, although sternum II slopes anteriorly to accommodate
the attachment to the thoracic area. Each is more or less rectan-
gular in shape and slightly bowed. Each successive sternum decreases
slightly in length and width, until the eighth sternum which is about
half the length of sternum II (Fig. 1).

A well-defined antecosta, on which the longitudinal muscles are
attached, is fomd along the anterior margin of the sternal plates.
The acrosternite, which extends anteriorly from the antecosta as a
narrow marginal flange in many insects, is lacking on all of the
sternal plates.

Along the apical margin of segments II through VIII is the
intersegnental membrane as is found in the female.

Sterna IX and X have become modified to form components 'of the
external genitalia.

Terga II through VIII are similar in structure and complemen-
tary to the sterna in general organization. A conspicuous acro-
tergite is found on tergal plates V through VII. Terga IX and X
have likewise become modified to form components of the external

genitalia.

Male Musculature of Segments II—VII

The pre-genital musculature of male Speyeria follows a definite
pattern which is repeated in segments IV through VII of the terga
and sterna II through VII. Modifications in this general pattern
of musculature have occurred in the first abdominal segment, due
to its attachment to the thorax, and the second and third terga.

The copulatory function of segments eight through ten have likewise
resulted in modification of the musculature pattern of these seg-
ments. There are 34 paired muscles in the pre- genital segments

of these male fritillaries. The myology of the pre-genital segments
of the male abdomen is quite similar to the female, muscle homologs
are numbered similarly, and likewise function in a similar manner.

The contractors of the pre-genital segments all function in-
dividually in the retraction of the tergal or sternal plates over
one another. The retraction of these individual plates results in
the decreased length or contraction of the pre- genital region. The
Median dorsal longitudinal muscles (12, _1_9, _g_6_, fl) , the Accessogy
median dorsal longitudinal muscles 13, _2_(_)_, _2_7_, 5;), the Primary

 

lateral dorsal loggitudinal muscles (11, _2_l_, _2__$_, _5_2) and the _S_e_<_:_-

 

ondary lateral dorsal loggitudinal muscles (_1_5, 2_2_, fl, _5_3_), all

 

serve as tergal retractors, whereas the Ventral longitudinal muscles

 

(_l_§_, 35, _3_2_, g) and the Lateral ventral longitudinal muscles (17,

 

_2_4, _31, _5_4_) serve as retractors of the sternal plates (Fig. 1).
The musculature of terga II and III is similar to that of terga

TV through VII. However, in terga II and III, the Secondary lateral

 

dorsal longitudinal muscle is not present. In tergum II, the

 

 

10

Accessory median dorsal longitudinal muscle (_2__) is so closely allied
with the Median dorsal longitudinal mmrscle (_1_) that they appear to be

one muscle rather than two distinct muscles as they do in the suc-

ceeding terga.

THE mRPHOLOGY OF SPEYERIA GENITALIA

A great many entomologists have studied the genitalia, partic-
ularly the male external genitalia, of the Lepidoptera from a tax-
onomic viewpoint. Thus, the terminology pertaining to the structures
of the male and female external genitalia of the LepidOptera has been
subject to much confusion. In fact, an average of more than six dif-
ferent names have been applied to each separate organ of the male
(Beirne, 1942) . Several nomenclatural systems, many purely descrip-
tive in nature, have been set forth. Others have been based upon
the comparative morphology of the adults. In this paper the ter-
minology set forth by Klots (1970) has largely been followed for
naming the components of the external genitalia.

The integumentary genitalic structures used in the taxonomy of
the Lepidoptera are derivatives primarily from the tergites and

sternites of segments VIII through X.

The Male External Genitalia

 

Before discussing the morphology of the different parts of the
male genitalia, it is necessary to describe the non-genitalic struc-
tures of the tenth and eleventh segments. The anus opens at the
apex of the abdomen at the end of a membranous tube, the anal tube
(Fig. 3). The anal tube is sclerotized dorsally, forming a long nar-

row plate, known taxonomically as the scaphium. In the male the

11

12

basal end of the scaphium articulates with the ventral side of the
base of the uncus along the posterior and lateral edges (Fig. 3).
The anal tube is sclerotized ventrally in a similarimanner, the ven-
tral sclerotization being known as the subscaphium (Fig. 3).

Zander (1903) and Mehta (1933) state that ontogenetically, the
uncus (Fig. 3) arises as an outgrowth from the base of the scaphium
and becomes secondarily attached to the caudal margin of the tegumen
(Fig. 3). Hewever, from a study of the male genitalic musculature,
Forbes (1939) showed that the base rather than the distal portion
of the uncus is the tenth tergum. This interpretation of the parts
is prObably correct due to the fact that the anal tube is separated
from the ninth segment by the basal parts of the uncus, representing
the tenth segment. The base of the scaphium articulates with the
base of the uncus and is not fused to, nor forms an adherent part of
the uncus, as is likely to be the case if the uncus was merely an
outgrowth from the scaphium. Presumably, what Zander and Mehta re-
garded as tergum.X was in reality segments X and.XI. Therefore,
it seems likely that the anal tube is a portion of segment XI, as
concluded by both Zander and Mehta. Thus, the scaphium and sub-
scaphium represent remnants of tergum and sternum XI respectively.

The external genitalia.may be considered to have been derived
from abdominal segments IX and.X. The genitalia as a unit are con-
nected to abdominal segment VIII by the intersegmental membrane (the
articular membrane or conjunctiva of some authors). It forms a

protractile base fer the copulatory apparatus.

13

Ninth Segment

 

This is the main genital segment and is highly modified bear-
ing the phallic and clasping organs. The sclerites of the ninth
abdominal segment together with remnants derived from the tenth seg—
ment, form the transverse, sclerotic ring which serves for the attach-
ment of the other parts of the external genitalia. The ring ap-
parent ly developed primarily to form a supportive structure for the
entire external genitalic bulb (Fig. 3) .

The dorsal portion of the ring is composed of the ninth tergum
and is known as the tegumen (Fig. 3) by lepidopterists. It is
quite large, heavily sclerotized, and forms a roof or hood-like
shaped structure which tapers caudally. While it is chiefly derived
from the ninth tergite, Klots (1970) notes that its more caudal por-
tion may consist of the anterior portion of the tenth tergite. The
tegumen is heavily thickened for mmscle attachment around its anterior
edge. Dorsally, there is a poorly sclerotized area which lacks normal
pigmentation in the tegumen, apparently characteristic of the
Argynninae (dos Passes and Grey, 1945).

The ventral portion of the ring is composed of the sternite IX
which gives rise to a large sclerite known as the vinculum and the
saccus (Fig. 3). While it is derived from the ninth stemite, the
vinculum actually is situated between the sclerites of the eighth
and ninth segments. It is typically in the form of a flattened "U".
The dorsal part of the ”U" is attached to the tegumen. Midventrally,
the vinculum is greatly expanded and is extended cephalad to form a

deep trough- shaped inflectionknown as the saccus. The non-sclerotized

14

ventral wall of the saccus is adnate with the eighth sternal surface.
The anterior edge of the gonobase is reflected outwards where it is
connected with the intersegmental membrane originating from the
eighth segment.

The most caudal components of the male genitalia are paired,
movable, clasping structures, known as the valves or gonoforceps
(Fig. 3). These are large, flattened, double-walled lobes, inte-
riorly concave, more or less tapering and bletly pointed distally.
Klots (1970) notes that these appear to be derived in part, at least,
from the styli, coxites or parameres of the gonopods of the ninth
segments. Each valve articulates to the vinculum, from which mus-
cles which operate the gonoforceps take their origin. The dorsal,
basal corner of each valve articulates with the corresponding poster-
lateral margin of the tegumen. The ventral, basal corner of each
valve articulates with the juxta (Fig. 5).

A gonoforcep consists of a number of parts or regions. The
nomenclature of these regions and structures of the valves is ex-
tremely confused because of the difficulty of homologizing, in the
various families, not only the various processes, but also the basic
regions themselves. A paper by Sibatani, e_t_ _a;1_. (1954) is the most
complete attempt to delimit the fundamental regions in various
families. These authors recogiize six fundamental regions as fol-
lows: costa (dorso-proximal) ampulla (central and media-dorsal) ,
cucullus (dorso-distal) , valvula (ventro-distal) , harpe (central
and medio-ventral) , and sacculus (ventro-proximal) . However, these
findings do not agree in part with Forbes' (1939) conclusions. He

studied the valval musculature, especially that of the so-called

15

"clasper" (the harpe of Sibatani, et al. , and other lepidopterists)
which in some groups apparently has a separate musculature which
would seem to infer a separate origin.

The expanded sac- like, ventro-proximal region of the gono-
forceps is known as the sacculus (Fig. 3) . The inner wall is not
continued to the lower edge of the valve, but meets the edge of the
folded-over part of the outer wall. The portion of the outer wall
of the sacculus situated on the inner surface where the inner and
outer walls of the gonoforceps meet is widest at its base. A mem-
brane extends to the juxta, and also to the sacculus from the op-
posite side (Fig. 5).

The harpe is a strongly sclerotized arm in the form of a cur-
ving spine, and is provided with independent musculature. It arises
from the inner surface of the valve in a central position, extending
outwardly and upwardly from the gonoforceps as a free arm.

The terminal, transverse sheet of membrane of the abdomen, known
as the diaphragma, is comected to the posterior margin of the gono-
base and the reflected free margin of the uncus (Figs. 5 and 6) .

From this dorsal point of attachment, it extends to the bases of the
valves and vinculum ventrally. It is probably in large part derived
from the ninth- tenth intersegmental membrane , but according to Klots
(1970) , may contain elements of the eleventh segment. The lower half
of the intermediary area between the tegumen and the anellus is trans-
formed into a pair of fusiform pouches (Fig. 6). Medially, where
perforated by the emerging aedeagus, the diaphragma is doubly folded
around this organ to form an eversible cone, the anellus (Fig. 5).

The inner most'layer of this cone, the manica (Pierce, 1914), is

16

shaped like a.megaphone and enwraps the subzonal portion of the
aedeagus and fastens around the aedeagus at the zone (Fig. 7). It

is connected to the inner reflected edge of the juxta, and anteriorly
attached to the zone of the aedeagus. This membrane allows for the
passage of the genital ducts from the abdomen into the genitalia,

fer the free flow of body fluids, and the extrusion of the genital
bulb at the time of copulation.

The juxta is a sclerite lying on the ventral surface of the
anellus, supporting the aedeagus, heavily sclerotized and shield-
shaped (Fig. 5). Its ventral corners articulate with the basal
portions of the sacculi. The apical margin is connected to the
anellus, the inner portion of which serves as the anterior attach-
ment of the manica.

In Speyeria a.median.membranous penis is nonexistent, rather
it has entirely fused with the penis valves to fonm an.aedeagus
(Fig. 7). The penis arose developmentally in the median conjunctival
membrane (Klots, 1970). In the resting position, the aedeagus lies
retracted completely within the manica.

During development, the distal portion of the aedeagus in-
vaginated cephalad, forming in inner tube known morphologically
as the endophallus and taxonomically as the vescia. Extending
cephalad into the body, this meets the caudal portion of the
ejaculatory duct (Fig. 7) along which the components of the sperma-
tozoa travel from the testis and vas deferens. This invaginated
endophallic tube is commonly, but erroneously referred to by tax-
onomists as the distal end of the ejaculatory duct. .As the vesica,
it is posteriorly continuous with the aedeagus. It is narrow and lies

coiled within the aedeagus. During copulation the greater part of

17

the vesica is uncoiled and thrust through the end of the aedeagus.
It passes up the bursal duct and opens into the base of the bursal
sac. The vesica bears small chitinous teeth, the cornuti. These
can be seen shining through the aedeagus in the resting position.
In Spgyeria, the vesica is evaginated during copulation as far as
the cornuti, which thus guards the opening of the vesica into the

bursa.

Tenth Sggment

 

The tenth abdominal segment is virtually non-existant in
Speyeria. .All that remains of the tenth tergite is the uncus (Fig.
3), a very prominent feature of the genitalia. Its anterior edge is
broadly ankylosed with the caudal edge of the tegumen. It is heavily
sclerotized, with a tapering arm whiCh is sharply accuminate. The
ventral margin is reflected inwardly and its free edge is connected

to the dorso-caudal part of the diaphragma of the abdomen.

The Musculature of the Male External Genitalia

 

In the past, the mechanism.of the extrusion of the genitalia
has not been thoroughly understood. As a result, several possible
explanations fer the extrusion of the male genitalia have arisen.
Perhaps the most widely accepted.the0ry is similar to Hanneman's
(1954a) speculation on the manner of extrusion of the male genitalia.
He noted that with a freshly killed.mele, one can easily protrude the
genitalia from the abdomen by applying pressure with your thumb and

fbrefinger to the last abdominal segment. The same effect could be

18

accorplished if one used a pipette to send a stream of water into
the first abdominal segment. Thus, Hanneman concluded that it was
the rise in interior pressure which effects the evagination. The
male butterfly does this on his own by the contraction of his pleura
muscles, which cormect the side portions of the sternites with the
tergites. Thus, the terga and sterna mutually squeeze together to
create internal pressure, which extrudes the genitalia.

The fact that the genitalia may be protruded by manipulation by
applying pressure upon the abdomen with the finger tips , is apparently
not significant. Fischer (1956) pointed out the analogy that a dis-
tended balloon will break when additional pressure applied upon the
balloon exceeds its elastic limit. Likewise, when pressure is applied
to the abdomen of a butterfly by means of the finger tips, it will
give at its weakest point to release the pressure when the breaking
limit has been attained. Since the weakest point in the body is un-
doubtedly that of the orifice through which the genitalia are ex-
truded, the genitalia are everted, regardless of the presence or ab-
sence of muscles. The assumption that the genitalia in nature are
extruded solely by the action of a build up of internal pressure,
is not tenable. A definite pattern of musculature accounts for the
protraction and retraction of the genitalia.

Since there are no records in the literature which could be
found on the mating behavior of Spieyeria, the following discussion
of the copulatory mechanism must be based in large part upon the
musculature of the male genitalia and associated terga and sterna.
To determine the probable function of the muscles of the genitalia,

three methods have been employed in both living and preserved

19

specimens: deduction, microsmanipulation, and the comparison of mus-
culature of everted and non-everted genitalia.

The Median dorsal longitudinal muscles (25,.59), the.AccessoEy

 

median dorsal loggitudinal muscles (22,.52), the Primary lateral dor-

 

sal longitudinal muscles (25, 52), and the Secondary lateral dorsal

 

loggitudinaltmuscles (25, 55) of the sixth and seventh terga are di-

 

rectly concerned with the extrusion of the genitalia during coition
(Fig. 1). When contracted this set of sixteen muscles accounts for
the contraction of the terga'VI and VII. To a slight extent, they
prdbably also serve to retract tergum'VIII. As a result, tergum VIII
is uplifted somewhat, leaving a caudal opening for the genitalia to
pass through to the outside of the body. Because of the variance in
angle of insertion of the Secondggy lateral dorsal longitudinal mus—
glg§.(25, 55), there is an increase in.the possible movements for
opening the orifice through whiCh the genitalia exit. In a like man-
ner, the contraction of the ventral longitudinal muscles (52, 55),
pull the sterna ferward opening the orifice ventrally (Fig. 1). These
are aided by the Lateral ventral longitudinal muscles (52,552).

Thus the contraction of the longitudinal muscles contracts the
abdominal terga and sterna. This contraction of the terga and sterna
does cause some pressure due to the compression of the abdomen. The
diaphragma is folded upon itself before this build up of internal
pressure. The hemocoel thus expands the diaphragma whiCh exerts a
force on the external genital bulb and causes it to move posterad.
Thus the intromittent organ is slightly extruded from.the abdomen and
ready fer cepulation, It is interesting to note that the muscles

which cause the slight extrusion of the genitalia are not protractors,

20

but retractors and that they do not act upon the genitalia directly
to extrude the genitalia, but contract the terga and sterna cOvering

the genitalia.

Extrinsic Muscles

 

In the Lepidoptera, the male external genitalia is considered
to include only the ninth and following segments though the muscles
of the eighth segment support the genitalia and are listed as ex-
trinsic muscles. Six pairs of extrinsic muscles have previously
been described as associated with the genitalia. All of these muscles
originate on the antecosta of segment VII and insert on the sclero-
tized "ring" of segment IX.

In the genus Speyeria, there are only five pairs of extrinsic
muscles all running from the antecostal part of abdominal segment
VIII to various areas of the ring of segment IX. Four sets of these
muscles, two pairs associated with the terga and two with the sterna,
all are inVolved with the retraction of the genital bulb after copu-

lation. The Median dorsal retractor 95 the genitalia (56) serves to

 

 

pull the dorsal area of the tegumen anterad after extrusion, while

the Ventral retractor 95 the genitalia (55) complements this muscle

 

 

in the sternum pulling the saccus anterad (Fig. 3). The net effect
is to retract the entire genital bulb. Two other muscles, the Lateral

dorsal retractor 95 the genitalia (52) and the Lateral ventral retractor

 

 

 

9_f_ the genitalia (_S_8_) also complement this total effect, but in addi-

 

tion have some rotatory effect upon the action because of their angle

of insertion (Fig. 3).

21

A fifth muscle, the Reflector 95 the genitalia (_6_Q), directs

 

the anterior portion of the saccus posterad and thus indirectly aids
in the extrusion of the aedeagus (Fig. 3).

Forbes (1939) and Stekolnikov (1965) have previously referred to
these extrinsic muscles as tergal and sternal muscles depending upon
their location.

The extrinsic external genital muscles of two other species in
the nymphalid subfamily Argynninae have been studied. Hanneman (1954a)
studied Arwis 9321115 and in addition to the Median dorsal retractor

 

3f the ggnitalia (T1 of Hanneman) and the Lateral dorsal retractor

 

 

 

95 the genitalia (T2), found a third tergal muscle (T3), which origi-
nated near the origin of the lateral dorsal retractor muscle of the
genitalia and inserted upon the anterior edge of the tegumen. This
third muscle has not been found in Speyeria, nor did Shirozu and
Yamamota (1953) locate it in their study of Morrow 1aodice jgponica.
Spgyeria possesses three extrinsic sternal muscles. Each is at-
tached to the anterior portion of sternite VIII. Forbes (1939) states
that the three sternal muscles are attached in a group to the anterior
lateral angle of the sternite. The Median ventral retractor gf _t_hg

genitalia is absent in A_rgyronome 1aodice japonica (Shiroza and Yama-

 

mota, 1953). Hanneman (1954a) found a Median ventral retractor 9_f_

 

the genitalia in Argynnis paphia, just as there is in Spgyeria.

 

 

Intrinsic Muscles

 

Ten paired muscles are found within the external genitalia of

male Speyeria. Eight of these function in the movement of the

22

tegumen, uncus, valves, and the aedeagus. It is difficult to assigr
arbitrarily any one function to a particular muscle because of the
possible effect any muscle or set of muscles may have upon the net
effect of another. Thus the muscles have been named with what is
presumed to be their primary function, but the reader must keep in
mind that these various functions may be materially altered by the
effect of other muscles. The supposed effect of many of these muscles
is outlined in the text along with the primary result of the contraction
of any individual muscle.

The Depressor o_f_ 335g 131995 (51) depresses the ankylosed tegumen
and uncus (Fig. 3).

In Speyeria as well as in Argyronome (Shirozu and Yamamota, 1953) ,

 

the Retractor g the anal tube (52) is represented by only a few

 

stray fibers (Fig. 3). It is more developed in Arm's (Hanneman,
1954a). In other Lepidoptera, this muscle originates on the swollen

anterior edge of the tegumen, loops arourd the Depressor _e_t: 1:213 uncus

 

(52) , and inserts as a large bundle on the sclerotized subanal plate
with several finer fibers inserting on the membranous sides of the
anal tube (Forbes, 1939). It will retract and thus raise the anal
tube. Forbes (1939) suggests that perhaps it was originally a muscle
of the gnathos, a structure which is not present in Speyeria.

Forbes (1939) gives no name to the Extensor 95 the tegumen (53).
This muscle would appear morphologically to be an extensor of the
valve. Yet upon contraction, it raises the tegumen in such a way
that the longitudinal axis of the tegumen occupies an almost vertical

position (Fig. 3) .

23

origin and insertion different from that of other lepidoptera (Fig.
3). Forbes (1939) and Stekolnikov (1965) report that in other lepi-
dOpteran species the Extensor 55 555_y§235_originates on the base of
the tegumen and inserts on a narrow process which is a continuation
of the inner region of the costal margin of the valve. It is inter-
esting to note that the other.Argynninae which have been studied,
Argynnis paphia and Argyronome 1aodice japonica, also have their

 

 

Extensors gf_the valves originating and inserting in the same manner

 

as it does in Speyeria.
The Flexor 5§_the clasper (55) aids the Flexor 55:555_valve (55)

 

since the clasper is fused to the valve (Fig. 3).

The Protractor 55 the aedeagus (55) is responsible for the ex-

 

 

trusion of the aedeagus during copulation, and the Retractor 55:555_
aedeag5§_(52) returns the aedeagus to its normal position after copu-
lation. The saccus thus serves as an apodeme fer the Retractor 55:555_
aedeag5§ (52). Insofar as the saccus and vinculum constitute a single
whole, the vinculum.has the same importance fer the muscles whiCh ex-
trude the aedeagus as the saccus has for the muscles which retract
it (Fig. 3).

Mechanically, the valves are levers and their fulcra are situated

between the planes of the valves so when the Flexors 5£_the valves

 

(55) contract, the valves open. In the case of the Extensors 55:555_
valves (54), the fulcra are situated outside the valves and contrac-

tion of the extensors causes the valves to close.

SIGELETO-MUSCULAR MECHANISM OF COPULATION

There have been several brief descriptions in the literature
of different Lepidoptera species copulating. Unfortunately, there
is rarely any mention of the skeleto-muscular mechanism involved.
One of these brief descriptions was made by Bayard (1944) on a COpu-
lating pair of RIBS. (now Argynnig) pgphia. Hanneman (1954a and 1954b)
described the Operational mechanism of Argynnis paphia, and Steklo-

nikov (1965) described the Operational mechanism of fomr moths.

The Female

 

No true morphological ovipositor, derivatives of podites, as
may be found in many insects, is present in this butterfly. Female
Smyeria, as well as other female Lepidoptera of the suborder Ditrysia,
possess two separate genital Openings (Fig. 2). The ovipositional
Opening, the oviporus, is situated below the anus, posterior to the
ninth segment. The c0pulatory Opening, the ostiun bursae, has moved
ventro-cephalad to a position anterior of the eighth venter, and is
the equivalent of the vulva in those insects having a common Opening
for egg deposition and the COpulatory fimction (Fig. 2). The
ostiun bursae Opens internally into a large, blind sac, the bursa
copulatrix, in which the spermatOphore is initially stored after
copulation. Thus, the understanding of the COpulatory mechanism

in the female is not based upon the morphology of an ovipositor, but
24

25
rather on the manipulative maneuverability of the abdominal segments
themselves. The functions of egg laying and copulation are restricted
to the operability of segments VII through X.

The seventh segment is not unlike preceeding segments except that
it is longer and tapers caudally giving it a cone-like appearance.

The sternal plate is especially strongly sclerotized (Fig. 8). This
strengthening is understandable due to the stress brought about by
the penetration of the aedeagus.

The close approximation of the eighth tergum and sternum has been
attained by the extreme reduction of the membranous pleuron to a
tergal- stergal conjunctiva more typical of most insects with secondary
segmentation. It is a specialization for both oviposition and copu-
lation. The reduction of the amount of membrane has increased the
ability of the segment to work as a unit rather than as separate
sclerites, in effect increasing maneuverability for the copulatory
and egg laying functions (Fig. 8).

The eighth tergum is larger than the sterniml and has its ante-
rior corners produced as a pair of rods, the anterior apophyses (Fig.
8). The anterior lateral margin of the eighth tergum has a greatly
expanded lateral tergal apodeme, a homolog of similar but much smal-
ler apodemes found in segments VI and VII.

The fused ninth and tenth segments are very much reduced. The
sterna of these two segments presumably have evanesced, indistinguish-
ably fused with the terga, or perhaps because of the nature of the
musculature , have expanded dorsally to include what has previously
been termed the terga. At any rate, fusion has occurred to form

the anal papillae (Fig. 8). These form a pair of large, setaceous

26

bearing lobes, one on either side of the anus and oviporus. The
lobes are more or less separate, soft, and somewhat kidney shaped.

From the lateral edges of the ninth segment extend cephalad,
paired, sclerotized, rod- like apodemes. These are the posterior
apophyses used for muscle attachment (Fig. 8).

The intersegmental membrane between the eighth segment and the
fused ninth and tenth is extra long (Fig. 8) . This allows the anal
papillae the extra flexibility required during oviposition.

The tergal musculature of segment VII is homologous with previous
segments but highly modified for the copulatory function and to a
lessor degree egg laying. Four elongate muscles serve collectively

as retractors of tergum VIII (Fig. 8). These are the Median dorsal

 

longitudinal muscle (£6) , Prima_ry lateral dorsal longitudinal muscle

 

 

 

(fl) , Secondary lateral dorsal longitudinal muscle 35 , and Tertiagy

 

lateral dorsal longitudinal muscle (55). Upon their contraction,

 

tergum VIII moves anterad causing the retraction of the tergum.
Muscles 55 and 54 however are extremely long and because of their ori-
gin, have a differentially greater pull on the anterior apophysis,
uplifting the apex of tergum VIII. With the contraction of the wide

banded Compressor 55 sengent VIII (5}) , coupled with the action of

 

55 and 54, sternum VIII is likewise uplifted apically (Fig. 8). This
action is further enhanced by the complete lack of any sternal mus-
cles antagonistic to the four tergal retractors 33, 55, a, 55).

Retractors of the ninth segment, the Median retractor 55 seggent

 

 

IX (45) and the Lateral retractor 5_f_ segrfint IX (45) , contract pulling
the ninth segment anterad (Fig. 8) . The contraction of the Anterior

retractor 5f_ the posterior apophysis (52) raises the anal papillae

 

27

through the leverage action upon the posterior apophysis (Fig. 8) .
These three sets of muscles thus retract and raise the fused IX and

X segments removing it from interfering with the c0pulatory process.
But, what the combined action of these muscles have thus far done

is to Lplift the eighth sternum exposing the ostiun bursae. Further
exposure of the ostiun bursae and most importantly the dilation of the
bursa c0pulatrix, which readies the female for the reception of the
male intromittent organ, is brought about by contraction of six addi-
tional muscles which insert directly on the bursa copulatrix. These
six sets of muscles are involved in the dilation of the bursa copulatrix
(Fig. 8) . Two of these originate anteriorly on the venter and include

the Lateral ventral dilator 55 the bursa copulatrix Q52) and Median

 

 

ventral dilator 55 the bursa cgpulatrix (55); a third which also

 

 

originates ventrally but posteriorly is an extremely large powerful

muscle, the Posterior ventral dilator 55 the bursa copulatrix (59_) .

 

 

All three of these muscles insert ventrally on the bursa copulatrix.
Complementary muscles which originate dorsally and posteriorly include

the Dorsal dilator 55 the bursa copulatrix (fl) , Dorso- lateral dilator

 

 

 

55 the bursa cgpulatrix (47) , and Dorso median dilator _05 t_h_e_ bursa

 

 

copulatrix (58). The combined action of these six muscles is the dilation

 

Of the bursa copulatrix and to a lessor extent the greater exposure
of the ostiun bursae. A total of 20 muscles are thus involved with
the exposure of the ostiun bursae and the dilation of the bursa

copulatrix -- all in preparation for reception of the male.

28

The Male

With the extrusion of the external genital apparatus, the male
raises its tegumen and its ankylosed uncus by the Extensor 95 5519
temn (55) upon approach to the female. As the tegumen and uncus
cover the rear of the female's abdomen, the Depressor 95 1:59 _u_n_g_1_s_
(51) contracts lowering the uncus and tegumen upon the anal papillae

of the female. The Flexors 95 the valves (58) and the Flexors 95 5159

 

claspgrs (_65) contract and spread the valves laterally. The f lexors

then relax and the Extensors 95 the valves (521) contract and move the

 

bases of the valves which embrace the anal papillae , while the claspers
embrace the : anterior of the anal papillae. The anal papillae thus
rest in the membranous fusiform pouches of the male (Fig. 6). This
movement of the valves enables the uncus to move anterad onto the eighth
tergum of the female, where the sharply accuminate tip of the uncus is
able to hook into the intersegmental membrane.

The female is thus secured at three points: the uncus of the
male secures the tergum of segment VIII, the claspers of the male secure
the lateral portions of the anal papillae, and the posterior portion
of the valves secure the seventh sternum of the female.

During the anchoring of the urcus, the anus is also retracted

 

and somewhat raised by the contraction of the Retractors 95 the anal

tube (57.) . At this time, the Protractors 95 the aedeagus (56) contract

 

 

amd direct the aedeagus caudally. Simultaneously, the Reflector 95

the male genitalia (5g) contracts, tipping the anterior portion of

 

the saccus dorsally, and thus also directing the aedeagus somewhat

dorsally. The combined action of 55 and 55 direct the aedeagus

29

dorso-caudally and introduce the aedeagus into the female's bursa
copulatrix. .As this happens, the male is able to grip the female
still more securely with his valves.

The circular Ejaculator muscles (25) squeeze the pouch-like

 

ejaculatory bulb (Fig. 7). The contraction of this muscle is also

employed to evaginate the vesica as the ejaculate passes through it,

after the aedeagus has been introduced into the bursa copulatrix.
Once copulation has been completed, the evaginated vesica is

retracted into the aedeagus by the contraction of the Retractors 95

 

the vesica (59) (Fig. 7). The aedeagus is then returned to its resting

 

position.by the contraction of the Retractors 95 the aedeagus (52)

 

 

and relaxation of 55_(Fig. 3).

The restoration to the resting position of the remainder of the
copulatory apparatus is due to the combined effect of the relaxation
of the external genital muscles and.the retractors of segment VIII.
While the retractors of segment VIII (55, 52, 55 and.59) contract,
thus pulling back the male external genitalia, the Depressor 95 559
99999_(52) relaxes which unhooks the uncus. Then, the Extensor 95

the tegumen (55) contracts, thus raising the combined uncus and

 

tegumen. Simultaneously, the Extensors 95 the valves (55) relax,

 

releasing the anal papillae. Then, the Flexors 95 the valves (55)

 

and the Flexors 95 the claspers (55) contract, spreading the valves

 

laterally. The relaxation of the Retractors 95 the anal tube (52)

 

 

returns the anal tube to its normal position. The dorsal and ventral
longitudinal retractors of the pre—genital segments relax, which
returns the tergal and sternal coverings over the external genitalia

and decreases the haemolymph pressure against the diaphragma.

30

In the female, the dilators of the bursa copulatrix (52, 55,
59, 55, 52 and 55) relax closing the ostiun bursae. The relaxation
of her Retractor 95 the_posterior_§pgphysis (52) lowers her anal
papillae. It is further lowered and returned to its normal position by
the contraction of the Protractor 95 the_posterior,§pgphysis 44 ,
the relaxation of the dorsal longitudinal muscles (55, 54, 55 and 55)
of the eighth segment, and the retractor muscles (55 and 55) of the
ninth segment. The combined effect of these eight pairs of muscles

re-conceals the ostiun bursae.

SKELETOéMUSCULAR.MECHANISM OF OVIPOSITION

Whoever has had the opportunity to Observe a female butterfly
during egg laying is amazed at the maneuverability of its abdominal
segments. .A variety of movements including protraction, retraction,
depression, and lateral movements of the abdomen may be explained on
the basis of the anatomical structure of the terga and sterna, and
their associated muscles.

The skeletoemuscular operational mechanism of oviposition has

been described by Hanneman (1954b) fOr Argynnis paphia. Unfortunately,

 

his description is not entirely accurate because he inaccurately named
some of the muscles involved with oviposition. IMost notable are his
segmental and genital protractors whiCh in reality are retractors.

At the time of oviposition, a fertilized egg lies in the posterior
portion of the membranous common oviduct (Fig. 2). The combined action
of the muscles of the female abdomen literally squeeze the egg out of
the abdomen.

The contraction of the abdomen is brought about by several factors.
The contraction of the dorsal and ventral longitudinal retractor
:muscles in the pre-genital abdominal segments, supported by the draw-
ing together of the muscularis of the pleura, whose threads run dorso-
ventrally, has a reciprocal approadh of the terga and sterna and thus
increases the interior pressure of the abdomen. This forces the

haemolymph.posterad against the supporting membrane of the common

31

32

oviduct, and the last intersegmental membrane. The Compressor 95 seg-

 

_m9p_1_:_ VIII (5_l_) achieves the same effect in the eighth segment (Fig. 8).
This dorsal-ventral compression results in the extension of the anal
papillae.

The fused ninth and tenth abdominal segment is especially moveable.
This is attained by the greatly lengthened last intersegnental membrane
and by the posterior apophysis with its assemblage of muscles. The
anterior apophysis of segment VIII and the posterior apophysis of
segment IX play a special role as the point of departure for the mus-
cles which cause the telescope-like in and out pushing of the segments,
as is manifested dm‘ing egg laying (Fig. 8). The contraction of the

Protractor 95 the posterior apgphysis (_45) , moves segments IX and X

 

 

caudally. This fused segment is thereby thrust out and the interseg-
mental membrane, which lies inside on the caudal edge of the eighth
abdominal segment , evaginates .

The lifting of the last segment occurs by means of the Anterior

retractor 95 the posterior apqrhysis (52) . Contraction of this muscle

 

exerts a diagonal (Oblique) pull ventrally oriented on the anterior
portion of the posterior ap0physis. Since this functions as a lever,
the final segment is raised (Fig. 8). Muscles 55 and 55 flmction

with the movement of the anal papillae similar to their combined
action involved with capulation. In addition, muscle 55, inserting on
the inner wall of the anal papillae, tends to draw the papillae together
upon contraction, contrasting to 55 which pulls the papillae away from
one another. The lowering of the last segment is brought about,

namely by the contraction of the depressors of segments VIII and IX

(59 and fl). At the same time, in addition to this ventrally oriented

33

movement, the final segments experience a somewhat lateral shift through
the contraction of muscles of 59_and.55 (Fig. 8). It is therefore,
moveable in all directions and can.perfOrm.the demands which are re-
quired during oviposition.

The flexibility of segment VIII is by far not so great as that
of the final segment. The eighth segment can also be pulled apart
from the seventh segment somewhat during the everting of the final
segment. .Also, its lengthening is probably somewhat attributable to
the effect of the intra-abdominal pressure and the peristaltic move-
ments of the lateral oviducts. The main function of muscle 52 is to
aid the median and lateral retractors of segment IX (55 and 55) re-
tract the evaginated final segment into the eighth segment, while the
eighth segment itself is retracted by the combined contraction of 55,
‘55,_55, and 55,

In summary, the sequential events involved in oviposition begin
with the contraction of the combined efforts of the dorsal and ventral
longitudinal retractor muscles, and the muscularis of the pleura.

The anal papillae are extruded by the combined effect of the increased

intra—abdominal pressure, the peristaltic contractions of the lateral

 

oviducts, and the Protractor 95 the posterior apgphysis (55).

 

Since the female often oviposits on.the underside of'a.95959
leaf, the apical end of her abdomen must bend and curve under while
she is standing on the upper surface of the leaf. This is accomplished
by the depressors of segments VIII and IX (59 and 55).

Since the female does not possess a true ovipositor, the com-
bined effect of the compression of the anterior segments, the exten-

sion of segments IX and X, the increase in intra-abdominal pressure,

34

the peristaltic movements of the oviducts, plus the compression of
segment VIII by muscle 55, all combine to literally squeeze each egg
out of the common oviduct.

With the conclusion Of each egg being laid, the abdomen returns
to its normal position. The depressors of segments VIII and IX (59
and.55) relax thus raising the rear of the abdomen to its pre-oviposit-

ing position. The Compressor 95_segment VIII (55) relaxes and allows

 

segment VIII to restore its normal expansion. The dorsal and lateral
longitudinal muscles of the first six abdominal segments relax, thus
decreasing the intra-abdominal pressure, and allowing the terga and

sterna to return to their normal position. The Anterior retractor

 

‘95 the posterior apgphysis 42 , plus the Median and Lateral retractors

 

 

.95 seg59nt IX (55 and 55) contract, and thus restore the anal papillae

to their normal position.

ANNOTATED LIST OF MALE AND FEMALE ABDOMINAL MUSCLES

iMuscles of Segment II

 

2, iMedian dorsal loggitudinalzmuscle (Figs. 1 and 2). A.short muscle

 

arising posteriorly on the dorsum of tergum II, extending someWhat
dorso-caudally in the female,lnu:only caudally in the male, and in-

serting on the antecostal ridge of tergum III.

 

2, Accessory median dorsal longitudinal muscle (Figs. 1 and 2). .A
short muscle arising posteriorly on tergum II, extending caudo—mesally
in the female. In the male, although it is lateral of 5, it appears to
be contiguous and.part of_5. In both sexes it inserts on the antecos-
tal ridge of tergum III.

5, Primary lateral dorsal longitudinal muscle (Figs. 1 and 2). .A

 

short muscle arising posteriorly on tergum II, extending ventro-caudally
in the female, while in the male it is an elongate muscle, arising mid-

anteriorly on the sloping face of tergum II, and extends caudo-ventrally.
In both sexes it inserts on the antecostal ridge of tergum III.

_5. Lateral ventral longitudinal muscle (Figs. 1 and 2). .A short

 

muscle arising posteriorly in the female (latero-posteriorly in the
male) on sternum II, extending dorso-laterally in the female (caudally
in the male), and.inserting on the antecostal ridge of sternum III.

.5. ‘Ventral longitudinal muscle (Figs. 1 and 2). .A.short muscle

 

arising posteriorly on sternum II in the female. In the male it is

a short muscle but longer than 5, arising medially on the sloping face

35

36

of sternum II. In both sexes it extends caudo-mesally, inserting

on the antecostal ridge of sternum III.

Muscles of Segment III

 

5. Median dorsal longitudinal muscle (Figs. 1 and 2). A short, fan-

 

shaped muscle in the female, arising posteriorly on the dorsum of ter-
gum III, extending caudo-dorsally, and inserting on the antecostal
ridge of tergum IV. In the male it is similar to _l_.

2. Accessory median dorsal longitudinal muscle (Figs. 1 and 2).

 

Similar to 2, but wider in the female, while it is more extensive
and distinctly separated from 5 in the male.

5. Primary lateral dorsal longitudinal muscle (Figs. 1 and 2) .

 

An elongate muscle arising medially on the lateral wall of tergum
III, and extending caudo-ventrally in the female. In the male it
is an elongate, robust muscle, arising mid- laterally on tergum III
and extending caudally. In both sexes it inserts on the antecostal
ridge of tergum IV.

9. Secondary lateral dorsal longitudinal muscle (Fig. 2) . A short

 

muscle arising posteriorly and ectally of 5 on the lateral wall of
tergum III, extending caudo-ventrally, and inserting on the antecostal
ridge of tergum IV in the female. Not present in the male.

29. Lateral ventral longitudinal muscle (Figs. 1 and 2). Similar

 

to 5, but more elongate, and origin partially hidden beneath _1_l_ in
the female. Similar to 5, but extending more dorso-caudally in the
male.

_1_5. Ventral longitudinal muscle (Figs. 1 and 2). Similar to 5, but

 

arising more medially in both sexes, and more elongate in the female.

37

Muscles of Segment IV

 

52. Median dorsal longitudinal muscle (Figs. 1 and 2). Similar to

 

5 in both sexes, but more robust in the female.

l_3. AccessoDr median dorsal longitudinal muscle (Figs. 1 and 2).

 

Similar to 2 in both sexes, but arising on the mid-dorsal wall of
tergum TV, more robust and elongate, extending caudo-ventrally, and
inserting on the antecostal ridge of tergum V in the female.

_15. Primary lateral dorsal longitudinal muscle (Figs. 1 and 2) .

 

Similar to 5 in both sexes, but more robust, and arising more anteriorly
in the female.

_15. Secondary lateral dorsal longitudinal muscle (Figs. 1 and 2).

 

Similar to 9 in the female. An elongate robust muscle in the male,
arising mid- laterally on tergum III, extending caudally, and inserting
on the antecostal ridge of tergum IV.

_15. Tertiary lateral dorsal longitudinal muscle (Fig. 2). An elongate

 

muscle arising anteriorly on the lateral wall of tergum IV, extending
caudally, and inserting on the antecostal ridge of tergum V in the
female. Not present in the male.

_1_2. Lateral ventral longitudinal muscle (Figs. 1 and 2) . Similar to

 

E in both sexes.

_15. Ventral longitudinal muscle (Figs. 1 and 2). Similar to _1_l_ in

 

both sexes, but arising more anteriorly in the female.

Muscles of 59gment V

 

_19. Median dorsal longitudinal muscle (Figs. 1 and 2). Similar to

 

5 and _J_._2 in both sexes, but much smaller in the male.

38
29. Accessory dorsal longitudinal muscle (Figs. 1 and 2). Similar

 

to _7_ and 25 in both sexes.

22. Primary dorsal longitudinal muscle (Figs. 1 and 2). Similar to

 

25 in both sexes, but more elongate in the male.

22. Secondary lateral dorsal longitudinal muscle (Figs. 1 and 2).

 

Similar to 25 in both sexes.

25. Tertiary lateral dorsal longitudinal muscle (Fig. 2). Similar

 

to 25, but inserting on the tergal apodeme in the female. Not present
in the male.

_25. Lateral ventral longitudinal muscle (Figs. 1 and 2). Similar to

 

10 and 22 in both sexes.

_25. Ventral longitudinal muscle (Figs. 1 and 2). Similar to 22 and

 

25 in both sexes.

Muscles of Segment VI

 

25. Median dorsal longitudinal IllUSCle (Figs. 1 and 2). Similar to 22

 

and 29 in both sexes, but less robust in the female.

22. Accessory median dorsal longitudinal muscle (Figs. 1 and 2).

 

Similar to 25 and 29 in both sexes, but more elongate in the male.

25. Primary lateral dorsal longitudinal muscle (Figs. 1 and 2). Similar

 

to 25 and 21_ in both sexes.

29. Secondary lateral dorsal longitudinal muscle (Figs. 1 and 2).
Similar to 25 and 22 in both sexes.

59. Tertiary lateral dorsal longitudinal muscle (Fig. 2). Similar to
25 in the female. Not present in the male.

51_. Lateral ventral longitudinal muscle (Figs. 1 and 2). Similar to

22 and 25 in both sexes, though smaller in the male.

39

52. Ventral longitudinal muscle (Figs. 1 and 2). Similar to 25

 

and 25 in both sexes.

40

Male Muscles of Segment VII

 

59. Median dorsal longitudinal muscle (Fig. 2). Similar to 29 and

 

52. Accessory median dorsal longitudinal muscle (Fig. 2). Similar

 

 

to 22.

52. Primary lateral dorsal longitudinal muscle (Fig. 2). Similar to
25.

_55. Secondary lateral dorsal longitudinal muscle (Fig. 2). Similar

 

to 29.
55. Lateral ventral longitudinal muscle (Fig. 2). Similar to 52.
55. Ventral longitudinal muscle (Fig. 2). Similar to 52, but because

of reduced size of sternum VII, virtually extends intersegmentally.

MJSCLES ASSOCIATED WITH THE FEMALE GENITALIA

Sggnent VII

 

55. Median dorsal longgtudinal muscle (Fig. 8). Similar to 22 and

 

29, but extending caudally and inserting on the anterior apoplysis.

55. Primary lateral dorsal longitudinal muscle (Fig. 9). Similar to

 

22, but thin and elongate.
2’5. Secondagy lateral dorsal longitudinal muscle (Fig. 8). Similar

 

to 22, but inserting on the greatly expanded lateral tergal apodeme
of segment VIII.
55. Tertiay lateral dorsal longitudinal muscle (Fig. 8). Similar

 

to 25, but inserting on the greatly erpanded lateral tergal apodeme
of segment VIII.

52. Lateral ventral dilator 95 the bursa copulatrix (Fig. 8) . Similar

 

 

to 52 , but inserting on the latero-ventral portion of the bursa

c0pulatrix.

 

 

55. Median ventral dilator 95 the bursa c0pulatrix (Fig. 8). Similar
to 52, but inserting on the medic-ventral portion of the bursa

copulatrix.

 

59. Posterior ventral dilator 55 the bursa copulatrix (Fig. 8) . A

 

massive muscle originating on the antecostal ridge of sternum VIII
and extending latero-ventrally, and inserting on the posterior venter

of the bursa copulatrix.

41

42

Segment VIII

 

59. Depressor 95 segm_9nt 2_X_ (Fig. 8). An elongate muscle arising
mid- laterally on tergum VIII, extending ventrally, and inserting on
the ventral extension of segment IX.

52. Compressor 95 segnent VIII (Fig. 8). A wide muscle arising just

 

 

posterad and ventrad of 59, extending caudo-ventrally, and inserting
on the posterior of sternum VIII.

52 . Anterior retractor 95 the posterior apophysis (Fig. 8) . A short

 

 

muscle originating on the greatly extended lateral tergal apodeme,
extending meso-caudally, and inserting on the anterior portion of
the posterior apophysis .

55. Dorsal dilator 95 the bursa conulatrix (Fig. 8) . It originates

 

 

mid- laterally on sternum VII, extends antero-ventrally, and inserts
on the dorsum of the bursa copulatrix.

55. Protractor 95 the posterior apophysis (Fig. 8). An elongate

 

muscle originating on mid-dorsally on the posterior apophysis, ex-
tending meso—caudally, and inserting on the caudal portion of
segment VIII.

55. Median retractor 95 segEnt 22 (Fig. 8). An elongate muscle

 

originating ventro- anteriorly on the posterior apophysis, extending
meso-caudally, and inserting on the median portion of segment IX.

56_. Lateral retractor 95 segmggnt 2X_ (Fig. 8). An elongate muscle

 

originating medially on sternum VII, extending meso- caudally, and
inserting on the ventral portion of segment IX.

52 . Dorso- lateral dilator 95 the bursa COpulatrix (Fig. 8). A short

 

muscle originating medially on sternum VIII, extending antero-

ventrally, and inserting on the bursa copulatrix.

43

55. Dorso-median dilator 95 the bursa copulatrix (Fig. 8) . A short

 

muscle originating postero-ventrally on sternum VIII, extending

anteriorly, and inserting on the bursa c0pulatrix.

 

4_9_. Depressor 95 segment VIII (Fig. 8). An elongate Imrscle originating
ventro-posteriorly on the posterior apophysis, extending caudo-ventrally,

and inserting on the posterior portion of sternum'VIII.

MUSCLES ASSOCIATED WITH THE MALE GENITALIA

Extrinsic Muscles (Segment VIII)

£9. Median dorsal retractor muscle o_f_ the genitalia (Fig. 3). This

 

is a flattened, several fibered muscle originating near the medio-
dorsal edge of the eighth antecosta and inserts on the anterior edge
of the tegumen just laterad of the medic-dorsal line. It is probably
homologous with the median dorsal longitudinal muscles of the preceeding
segments.

51. Lateral dorsal retractor muscle of the genitalia (Fig. 3). Re-
sembles §_6_ with fibers originating on the eighth antecosta, but in-
serting on the extreme upper angle of the vinculum. It is probably
homologous with the secondary lateral dorsal longitudinal muscles of
the preceeding segments.

_s_§_. Lateral ventral retractor muscle 9f the genitalia (Figs. 1 and 3) .
This is a slender and long muscle originating on the lateral angle

of the eighth sternite and inserting on the vinculum near the in-

sertion of _31 at the base of the tegumen.

 

 

_52. Ventral retractor muscle o_f_ the genitalia (Fig. 3). This is a
small, short muscle, inserting on the venter of the saccus, posterior
to the origin of the large retractor muscle of the aedeagus (_6_7) .

_Qg. Reflector muscle 53f the genitalia (Fig. 3). This is a short,

 

 

massive muscle inserting on the posterior ventral area of the saccus.

44

45

Intrinsic MusclesJSegment IX)

fl. Depressor _o_f the uncus (Fig. 3) . A pair of massive, fan-like mus-
cles originating on the swollen anterior ring edge of the tegumen and
inserting on the inwardly reflected flange of the ventral margin of

the uncus .

 

_6_2_. Retractor gf_ the anal tube (Fig. 3) . Represented by only a few
stray fibers. A median fiber originates from the medic-dorsal point
of the swollen leading edge of the tegumen and terminates at the medio-
dorsal points of the anal tube. Two lateral fibers originate just
laterad of the base of the median fiber and insert on the subanal
plate.

g}. Extensor _o_f_ the tegumen (Fig. 3). Originating on the tegumen near

 

the depressor of the uncus (o_l) but more dorsally. It runs directly
under the articulation of the tegumen and pleuron to insert in the tip
of the valve where it articulates with the vinculum.

_6_41. Extensor 3f 1:112 M (Fig. 4). Originating on the mid- to upper
part of the vinculum, it inserts on a serrate internal ridge of the
valve known as the crista (dos Passos and Grey, 1945) and crowds the

flexor of the clasper (65).

_6_5_. Flexor 9f the clasper (hame) (Fig. 4). It originates in the

 

swollen saccular portion of the valve, mostly along the ventral
posterior edge, but also partly from the ental surface, and inserts
on the lower portion of the sclerite bearing the clasper of the valve.

9.9- Protractor 9f the aedeagus (Fig. 3). This is the most massive

 

 

of all of the intrinsic muscles. Originating on the anterior margin
of the vinculum from its dorsal articulation with the tegumen ventrally

to the saccus, it inserts on the extreme basal half of the subzonal

46

portion of the aedeagus, almost completely enwrapping the latter.

91. Retractor 9f the aedeaggs (Fig. 3). This muscle lies ental to 6_6

 

and is almost equally as massive. It originates on the tip of the
saccus, enwrapping it on both sides, and ms up around the aedeagus
on each side and inserts on the dorsum of the aedeagus just anterad
of the attachment of the ejaculatory duct.

§_8_. £13259; _o_f_ the 32.1372 (Fig. 4). It originates on the basal edge of
the juxta and runs longitudinally and parallel to insert mostly on
the anterior part of the invaginated inner surface of the saccus with

only a few fibers inserting in the extreme base of the valve. It

lies mesad of the flexor of the clasper (_6_5).

Engphallic Muscles

 

pg. Retractor 9f the vesica (Fig. 7). This is enclosed by the

 

tubular aedeagus, originating on the extreme basal portion of the
inner surface of the aedeagus, and circumscribing the cup-shaped
invaginated ves ica.

_7_Q. ”Ejaculator muscle (Fig. 7). This muscle is telescoped in the

 

pouch- like ejaculatory bulb and is composed of circular fibers,

surrounding the ejaculatory duct .

SUMVIARY

The morphology of the copulatory and ovipositional mechanisms
of Smeria are described. The myology of the copulatory and ovi-
positional mechanisms is described, which aids in explaining the skeleto-
muscular Operational mechanisms of copulation and oviposition.

The male and female copulatory apparatuses of Speyeria do not have
to be appreciably everted, as do some other insects, to be ready for
mating. The male's genitalia are everted by the sequential contrac-
tion of the pre- genital segments by the dorsal and ventral longitudinal
muscles of each segment which also creates an increased intra-abdominal
pressure and pushes the haemolymph posterad against the diaphragma.

No true morphological ovipositor, nor external genitalia are
present in the Spgyeria studied. Thus, the understanding of the copu-
latory mechanism in the female is not based upon the morphology of an
ovipositor, but rather on the manipulative maneuverability of the
abdominal segments themselves. The female prepares herself for the
reception of the male by raising and retracting the apical portion of
her abdomen. This exposes her ostium bursae, which has dilated through
the action of six muscle pairs and is ready for the intromittent organ
of the male.

With the extrusion of the male external genital apparatus, he
extends his tegumen and then lowers it and the ankylosed uncus upon
the dorsum of the anal papillae. The valves spread laterally, allowing
the anal papillae to rest in his membranous fusiform pouches and then

47

48

extend to securely fix the position of the female. The aedeagus
is then introduced into the bursa copulatrix and the vesica everted
as the ejaculate passes through it.

At the time of oviposition, a fertilized egg lies in the posterior
portion of the membranous common oviduct. Since the female does not
possess a true ovipositor, the combined effect of the compression of
the anterior segments, the extension of segments IX and X, the increase
in intra-abdominal pressure, the peristaltic movements of the oviducts,
plus the compression of segment VIII, all combine to literally squeeze

each egg out of the membranous common oviduct.

LITERATURE CITED

LITERATURE CITED

Bayard,.A., 1944. Observations sur l'accouplement de Dryas paphia
(L.). Bull. Soc. ent. France 1944:92-95.

 

Beirne, B. P., 1942. The morphology of the male genitalia of the
LepidOptera. Ent. Record 54:17-22, 37-39.

Bonhag, P. F. and J. R. Wick, 1953. The functional anatomy of the male
and female reproductive systems of the Milkweed Bug, Oncopeltus
fasciatus (Dallas) (Heteroptera: Lygaeidae). Jour. Morph. 93:
177-233.

 

dos Passos, C. P., and L. P. Grey, 1945. A genitalic survey of
Argynninae (Lepidoptera: Nymphalidae) . Am. Mus. Novitates
#1296, 29 pp., 54 figs.

Ehrlich, P. R. and S. B. Davidson, 1961. The interal anatomy of the
Monarch butterfly (Danaus lexi us) L. (Lepidoptera:
Nymphalidae). Microent. 24: 5-133, figs. 1-78.

Fischer, R. L. , 1956. The muscular mechanism of the male metasoma
and genitalia of Megachile fortis Cresson (Hymenoptera:
Megachilidae). Can. Ent. 8§z65'7-673.

Forbes, W.T.M., 1939. The muscles of the 'lepidopterous male genitalia.
Ann. Ent. Soc. Amer. 32:1-10.

Hannemann, H. J ., 1954a. Zur funktionellen anatomie des mannlichen
' kopulationsapparates von Argynnis thia (L.). 2001. Anz. 152:
266-274.

 

, 1954b. Zur muskelftmktion der weiblichen genitalsegmente
von Argynnis paphia (L.). (Lepidoptera). Zool. Anz. 153:149-154.

 

, 1957. Die mannlichen terminalia von Micromerygc calthella
L. (Lepidoptera: Micropterygidae). Dtsch. Ent. Ztsch. 4:209-222.

 

Klots, A. B., 1970. Lepidoptera. IN Tuxen, S. L., Taxonomist's
Glossary of Genitalia in Insects. Mundagaard, Copenhagen,
pp. 115-130.

Kullenberg, B. , 1947. Uber morphologie und funktion der

kopulationsorgane der Capsiden und Nabiden. Zool. Bidrag.
fron Uppsala 24:217-418.

49

SO

Kunze, L., 1959. Die funktionsanatomiSChen grundlagen der
kopulation der zergzicaden, untersucht an Euscelis lebe'us
Fall. und einigen Typhocybinen. Deutsch. Ent. ZtscEr. 6:322-387.

Knsnezov, N. Y., 1915. Faune de la Russie. Insectes Lepidopteres.
'VOl. I. .Academy of Sciences of the U.S.S.R., Petrograd, 366 pp.,
204 figs.

Mehta, D. R., 1933. Comparative morphology of the male genitalia in
Lepidoptera. Rec. Indian Mus. 35:197-266, figs. 1-114.

Pierce, F. N., 1914. The genitalia of the group Geometridae of the
Lepidoptera of the British Islands. T. Chelland and Son, Ltd.,
Liverpool, XXIX G 88 pp., 48 pls.

Ruckes, H., 1919. Notes on the male genital system in certain Lepidop-
tera. Ann. Ent. Soc..Amer. 12:192-209. 3 pls.

Sibatani, A., M. Ogata, Y. Okada, and H. Okagaki, 1954. Male genitalia
of Lepidoptera: Mbrphology and.nomenclature I. Divisions of the
valvae of RhOpalocera, Phalaenidae and Geometridae. Ann. Ent.
Soc. Amer. 47:93-106, 2 pls.

Shirozu, T., and.H. Yamamota, 1953. iMOrphology of the male genital
organs of Ar onome 1aodice japonica.Mbnetries (Lepidoptera:
Nymphalidae). Sieboldia..Acta. Biologica, FukuOka 1:161-168,
4 pls.

Snodgrass, R. B., 1935. Principles of Insect Morphology. MtGraw-Hill
Book Co., New York, IX G 667 pp.

, 1957. .A revised interpretation of the external reproductive
organs of male insects. Smith. Mfisc. Coll. 135, No. 6:60 pp.

Steklonikov, A. A., 1965. Functional morphology of the copulatory
apparatus in some Lepidoptera. Ent. Rev. 44:143-149.

Zander, B., 1903. Beitrage zur morphologie der mflnnlichen geschlecht-
sanhange der Lepidopteren. Z. Wiss. 2001. 74:557-615, 29 pls.

FIGURES

51

Figure 1. Internal Right Lateral View of the Male Abdominal Segments
II-VIII and Associated Musculature

Figure 2. Internal Right Lateral View of the Female Abdominal Segments
II-X, Associated Musculature and Reproductive Structures

   
 

   

PlEUHAl

“I, fiwgsfum'm

25 32 55

 

SPIHABLE

”‘16 23 24.30 A

 

2 common
aunsn BUPUlAIRIX ovmucr

53

Figure 3. External Left Lateral View of the Male External Genitalia
and its.Associated Musculature

Figure 4. Internal Lateral View of the Right valve and its Associated
IMusculature

UNBUS

57

/ 31.3.2: _- \fl
/ / -\"-< ’7
vmcuum . , , ' 7:2,
/

AEDEABUS

    
   

SABBULUS 3
SABBUS

BHISTA

 

ANELLUS 65 4

SADBUS

55

Figure 5. Dorsal View of the.Articulations of the Juxta, valve, and
Saccus

Figure 6. Left Lateral View of the Membranous.Areas of the Mble
Genitalia

Figure 7. Left Lateral View of the Aedeagus and its.Associated
ZMusculature

DIAPHRABMA

    
 
    
 
  
 
 
 
  
 
 
  

~/

ANELLUS

VINBULUM

TEBUMEN
SABBUS

ANAL TUBE

VINBULUM

 

FUSIFDHM PUUBHES

Rig; ,:1, EJABULATURY

J, BULB
/

VALVE

PENIS VALVE

EJACULATUHY
DUCT

 

57

Figure 8. Internal Right Lateral View of the Posterior Segments
(VII-X) of the Female Abdomen with Associated Musculature

2:33: 252.35

      

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