J . Aust. ent. Soc.

, 1975, 1 4 363-370 363

ON THE RESPIRATORY SYSTEM OF THE LEMON-BUTTERFLY, PAPILIQ

DEMOLEUS L.* (LEPIDOPTERA PAPILI0NIDAE)T
K. P. SRIVASTAVA
Department of Zoology, Banaras Hindu University, Varanasi-221005 (India)

Abstract
The spiracular and tracheal systems of the lemon-butterfly, Papilio demoleus are described in detail. The
insect has 9 pairs of spiracles of which 2 are located in the thorax and 7 in the abdomen. Only the second
thoracic spiracle has the external closing mechanism, the rest having the internal closing mechanism. The
tracheae of the preabdominal region are largely thin walled, without taenidia and easily collapsible while
those of the abdomen have taenidia and are not easily collapsible. The tracheal air-sacs are largely present in
the preabdominal region. Some tracheae that d o not tracheate any organ but open into another trachea or
air-sac have been referred to as the tracheal shunts. Their possible function is to feed additional air to $he
branches or air-sacs into which they open. The spiracular tracheae maintain a fairly uniform (generalised)
branching pattern throughout different segments.

Introduction
Literature on the adult lepidopterous respiratory system, by and large, is
restricted only to the structure and function of the spiracles (Snodgrass 1935; Beckel
1956; Beckel and Schneiderman 1957; Tonapi 1959; Van der Kloot 1963; Mathur
1967),the tracheal system having been completely neglected. The present studies which
include both the spiracular and tracheal systems of an adult butterfly, Papilio demoleus
may, therefore, be of some interest.

Material and methods

To study the spiracles and their musculature, the specimens were fixed in Bouin’s
fluid. Spiracular areas were cleared of the surrounding tissues and the spiracles
removed from the body. They were then processed, stained in borax carmine and
mounted in Canada balsam. The tracheal system was studied in partially etherised
insects dissected in insect Ringer (Ephrussi and Beadle 1936) under a stereoscopic
binocular microscope. The insect was arranged so that only the portion being studied
was immersed in Ringer in a depression made in the wax dissecting dish. This enabled
the insects to breathe and retain air in their tracheae longer. The tracheae of dead
insects were found to lose air and so their visibility faster than those of the (partially)
living ones. Nevertheless, the tracheae of the preabdominal region, being largely
saccular (thin walled) presented great difficulty and had to be ascertained by repeated
dissections. The abdominal tracheae were more easily traceable in older males than in
younger ones or females which have relatively larger amounts of fat bodies.
Abbreviations used in the figures: AB, anterior branch; AF, flexible arm; AL,
anterior lip; ANT, antenna; AR, rigid arm; ASI, AS. positions of the first and seventh
abdominal spiracles; ASD, dorsal air-sacs (portion cut from metathoracic dorsal air-
sac); ASD,, ASD,, first and second dorsal prothoracic air-sac (portions cut); ASDA,
dorsal abdominal air-sac; ASL, lateral (meso- and meta-thoracic) air-sacs; ASCR,
cranial air-sac; ASV, ventral (prothoracic) air-sac; BB, bilateral branches; CE,
compound eye; CM; cut margin of the cranial air-sac; CP, cuticular process; CR,
cranium; DH, dorsal hinge; FB, fat bodies; FEN, fenestra; FU, mesofurca; FW,
forewing; G,, fourth (last) abdominal ganglion; GM, thoracic ganglionic mass; HT,
heart (portion); HW, hindwing; IM, intervening membrane; KFU, mesofurcal keel;
LS, laterosternite; LV, lever; MA, mcsonotal acrotergite; MDL, dorsal longitudinal
muscles (portion of a bundle); MDT, dorsal tergal muscles; MDV, dorso-ventrally
disposed muscles; MST, sternal muscle; MG, midgut; OM, occlusor muscle; OPB,
optic branches; PL,, PL,, meso- and meta-pleuron; PTM, peritreme; RO, repro-
ductive organ (portion of ejaculatory duct); SC, scales; SO, spiracular orifice; ST,,
eighth (abdominal) sternum; T,, T,, T,, pro-, meso- and meta-thorax; TAB,
*In Australia this species is known as the Checquered Swallowtail.
?Communicated by D r B. P. Moore.
364 K. P. SRIVASTAVA

abdominal trachea; TAS, air-sac trachea; TCB, cerebral trachea; TCD, dorsal tracheal
commissure; TCV, ventral tracheal commissure; TD1, TD2, first and second dorsal
trachea; TGM, ganglionic mass traceha; TG,, TGs, first and eighth (abdominal) terga;
TI, inner trachea; TMT, metathoracic trachea; TO, outer trachea; TOPS, optic-stalk
trachea; TPD, postero-dorsal trachea; TS1, TS2, positions of the first and second
thoracic spiracles; TT, tergal trachea; TTA, anterior tracheal trunk; TTD, dorsal
tracheal trunk; TTL, longitudinal tracheal trunk; TTPL, pleural tracheal trunk; TTV,
ventral tracheal trunk; TTVS, visceral tracheal trunk; V, valva; VPR, ventral process.
Observationsand discussion
1. The Spiracles
The butterfly has 9 pairs of spiracles: 2 in the thorax and 7 in the abdomen. Of these only the second
thoracic spiracle has the external closing mechanism, the rest having the internal closing mechanism.

Thoracic spiracles
The first thoracic spiracle lies in the pleural membrane of the prothorax close to the mesonotal
acrotergite (Fig. 1). The rather shallow atrium of the spiracle communicates with the exterior through the
spiracular (atrial) orifice and internally with the spiracular trachea through the tracheal orifice. The
spiracular orifice is confluent with a narrow annular sclerite, the peritreme, surrounding the orifice (Fig. 2).
The inner margin of the peritreme is prolonged into a number of cuticular and much branched processes
forming a sort of a thatched covering on the spiracular orifice and constituting a filter apparatus which
prevents entry of foreign particles into the spiracle. Beckel (1956) finds such processes to arise from the
bottom of the atrial chamber, Tonapi (1959) from the peritreme and Mathur (1967) from the inner wall of the
atrium. In the present insect, the filter apparatus is distinctly the product of the peritreme and, therefore, is in
agreement with Tonapi’s description. Mathur’s ‘inner wall’ does not make it clear whether the processes arise
from the outer region or the bottom of the atrium. The atrial wall of the present insect has become
differentially sclerotised into an internal closing apparatus. This apparatus has been likened to a bow
(Landois and Thelen 1867)having 3 distinguishable parts: a rigid arm, a flexible arm and an extension of the
latter, the lever or manubrium. The rigidarm (Fig. 3) forms the posterior half of the apparatus and is closely
approximated to the inner surface of the corresponding half of the peritreme. The approximation and
relatively heavier sclerotisation render this arm rigid or immovable. Theflexible arm constitutes the anterior
half of the apparatus and is connected to the corresponding half of the peritreme through a narrow band of
intervening membrane which together form the closing valve of the spiracle. Poorer sclerotisation of the
flexible arm as compared to the rigid arm results in a dorsal hinge which makes the arm flexible or movable.
Mathur’s ‘completely sclerotic semicircles’, obviously the equivalents of the above 2 arms in the present
insect, do not leave any room for a hinge and, therefore, the hinge lines shown by him are rather vague. The
lever is a slightly arched process projecting anteriorly and giving insertion to an occlusor muscle that
originates from the ventral extension of the rigid arm. Mathur describes the origin of this muscle from the
ventral end of the ‘spiracular rim’ which again is vague. The contraction of the occlusor muscle pulls the lever
down which in turn pushes the flexible arm backwards (towards the rigid arm) stretching the intervening
membrane across the tracheal orifice and screening it off from the atrium. A dilator muscle present in the
caterpillars of some insects (Snodgrass 1935)is absent in the adult of this insect so that the spiracle opens by
the relaxation of the occlusor muscle and/or elasticity of the lever.

FIG.1.-Lateral view of a male butterfly showing location of the spiracles.

 RESPIRATORY SYSTEM OF PAPILIO DEMOLEUS 365

c------i t----------r
2 0.2 m m
3 0.2 mm

- 0.2 mm

6
I
-s C

FIGS.2-6.+2) First thoracic spiracle (outer view) after removing the scales from the pleural membrane
(stippled): (3) First thoracic spiracle (inner view) showing the internal closing apparatus: (4) Second thoracic
spiracle (outer view) showing external closing mechanism. Dotted lines indicate internal structures: (5) First
abdominal spiracle (outer view) showing modified body scales surrounding the spiracular orifice: (6)An
abdominal spiracle behind the first (outer view) showing the filter apparatus in the form of scaly-plug.
366 K. P. SRIVASTAVA

The second thoracic spiracle lies in the upper region of the segmental membrane between the meso- and
meta-pleuron but closer to the former (Fig. 1). The spiracular orifice ofthis spiracle is narrow and elongated
with its anterior margin overgrowing into a slightly hardened narrow plate, the anterior lip (Fig. 4). The
lower end ofthe anterior lip is drawn into a small ventral process which gives insertion to the occlusor muscle
originating from the outer surface of the inner end of the mesofurca. On contraction the muscle pulls the
ventral process downwards and forwards which draws the anterior lip backwards over the spiracular orifice
to cover it, thus constituting an external closing mechanism.
Abdominal spiracles
Of the 7 pairs of abdominal spiracles present in this insect, the first pair is located in the pleural
membrane near the base of the laterosternite (Fig. 1) with the remaining ones nearer the tergal margins of
their respective segments. The eighth (free) segment in the male is devoid o f a spiracle while the female which
has only 7 free segments has a spiracle for each segment. The first abdominal spiracle is not provided with a
filter apparatus though modified body scales with long pedicels and deeply notched margins densely
surround the spiracular orifice and seemingly prevent entry of foreign particles into the spiracle (Fig. 5).
Each of the remaining abdominal spiracles is provided with a filter apparatus formed by ordinary body
scales. The scales are inserted in overlapping rows (Fig. 6) on the anterior slightly sunken margin of the
spiracular orifice (Fig. 7) forming a sort of scaly-plug. The structure of the abdominal spiracles is similar to
that of the first thoracic spiracle in every respect except the following: (1) a peritreme is lacking in the
abdominal spiracles. This may be because the filter apparatus in these spiracles is formed by the body scales
and not by the cuticular processes of the peritreme, (2) their closing apparatus is a reversed replica of that of
the first thoracic spiracle i.e., the rigid arm is anterior and the flexible arm posterior so that the lever points
backwards, and (3) their closing apparatus extends much beyond the spiracular orifice at both ends. The
occlusor muscle is present in its normal position.

2. The tracheal system

Whereas the tracheae ofthe abdominal region are cylindrical, taenidiated and non-collapsible (diffusion
tracheae of Krogh 1920), those of the preabdominal region (head and thorax) largely comprise thin walled
(saccular), non-taenidiated and easily collapsible tracheae (ventilation tracheae of Krogh 1920). The
branches of the tracheal trunks are frequently more spectacular in their dimensions than the trunks
themselves and being saccular in the preabdominal region give rise to a number of air-sacs some ofwhich are
fenestrated for giving passage to the dorso-ventrally disposed muscles. The air-sacs are never found to be
(fully) swollen with air but their large size and greater number presumably lower the specificgravity and help
in flight (Imms 1963). The thin walls of the air-sacs make them extremely sensitive to the respiratory
movements of the body and organs around them which enhances the efficiency of their ventilation.
Coalescence and anastomosis between tracheae appear to be the rule in the preabdominal region and are the

FIGS. 7, 8 . 4 7 ) An abdominal spiracle after removing the scaly-plug. Anterior sunken margin of the
spiracular orifice is shown heavily stippled and the internal structures partly dotted: (8) Dorsal mesothoracic
air-sac tracheating the dorsal longitudinal muscles.
 RESPIRATORY SYSTEM OF PAPILIO DEMOLEUS 361

cause of formation of most of the larger air-sacs. A few tracheae that open into other tracheae or air-sacs
instead of tracheating any organ have been designated as the tracheal shunts whose function appears to be
to feed additional air to the branches or air-sacs into which they open. Though there is a fairly uniform
branching pattern of the spiracular tracheae* in different segments, the readiness of the tracheae to branch
off and supply adjacent organs results in occasional overlapping in tracheation. The following paragraphs
carry the description of the tracheation in different segments without considering the homologies of the
tracheae.

Tracheation of the head and prothorax

The head, cervix and prothorax are supplied by tracheae from the first thoracic spiracle (Fig. 8). The
spiracular trachea of this spiracle divides into dorsal, anterior and ventral tracheal trunks?. The dorsal
tracheal trunk divides into 3 tracheae: the first dorsal, second dorsal and postero-dorsal tracheae. The first
dorsal trachea joins its counterpart of the other side to give rise to the first dorsal prothoracic air-sac
occupying the posterior half of the prothorax. The fenestrae present on the air-sac give passage to the dorso-
ventrally disposed muscles of the region. The air-sac tracheates the dorsum above and the anterior part of the
dorsal longitudinal muscles of the mesothorax behind. The second dorsal trachea gives out an anterior
branch from its basal portion and joins its counterpart to form the second dorsal prothoracic air-sac. The
anterior branch runs forwards and opens into the antero-lateral margin of the second dorsal prothoracic air-
sac to become a tracheal shunt. The second dorsal prothoracic air-sac lies under the dorsal longitudinal
muscles of the segment which it tracheates. Anteriorly the air-sac enters the cranium and expands into a
cranial air-sac. The cranial air-sac covers the whole of the dorsal surface of the brain tracheating the eyes
including the optic lobes, antennae and facial muscles (the latter not shown in the Fig.). The optic branches,
numbering 10-12, arise from the ventro-lateral surface of the cranial air-sac and, therefore, are visible only
after the overlying portion of the air-sac is excised (as shown on the right side of the Fig.). The postero-dorsal
trachea, arising from the posterior margin of the dorsal tracheal trunk, runs backwards into the mesothorax
to supply the forewing and tegula. The anterior tracheal trunk runs forwards to supply the overlying muscles
and dividing terminally into 3 tracheae: a cerebral trachea running inwards to supply the protocerebrum, an
optic-stalk trachea going outwards to tracheate the optic-stalk and an air-sac trachea opening into the
cranial air-sac to become a tracheal shunt. The ventral tracheal trunk joins its counterpart of the other side to
form a ventral prothoracic air-sac which supplies the overlying ventral nerve cord, digestive organs, ventral
muscles and the prolegs. From the postero-lateral margin of the air-sac are given out 2 ganglionic mass
tracheae which run into the mesothorax to tracheate the thoracic ganglionic mass.

Tracheation of the mesothorax

The mesothorax is supplied by tracheae from the second thoracic spiracle except the few tracheae that it
also receives from the first thoracic spiracle as described above (Fig. 8). The spiracular trachea of the second
thoracic spiracle divides into dorsal, anterix, pleural and ventral tracheal trunks. The dorsal tracheal trunk
divides again into inner and outer tracheae. The inner trachea runs forwards underneath the dorsal
longitudinal muscles of the segment giving out a number of bilateral branches along its course. The bilateral
branches are taenidiated only basally, their distal portions being non-taenidiated and saccular. Some of these
saccular branches (transversely) brace the ventral surface of the dorsal longitudinal muscles sending
numerous ramifications into them, while others coalesce to give rise to 2 lateral mesothoracic air-sacs lying
one above the other on the inner surface of the dorso-ventral muscles which they profusely tracheate. The 2
air-sacs communicate with each other through connecting branches and the lower one. in addition,
communicates with its counterpart of the other side anteriorly. Their connecting portion tracheates the
underlying thoracic ganglionic mass and the basal portions of the nerve trunks that emerge from the mass.
The outer trachea of the dorsal tracheal trunk divides again into 2 branches: one penetrating the dorsal
longitudinal muscles and the other running outwards and then upwards to occupy the dorsal most region of
the mesothorax where its branchescoalesce with each other and with their counterparts of the other side to
give rise to the dorsal mesothoracic air-sac (Fig. 9) which, in turn, tracheates the dorsal longitudinal muscles
from the dorsal aspect. The anterior tracheal trunk (Fig. 8) runs forwards and joins the ganglionic mass
trachea of the first thoracic spiracle to become a tracheal shunt and also to connect the 2 thoracic spiracles.
The pleural tracheal trunk penetrates the dorso-ventral muscl.es to tracheate their outer layers and other
mesopleural muscles not covered by the lateral mesothoracic air-sacs. The ventral tracheal trunk runs
inwards and then forwards along the mesofurcal keel dividing into 2 tracheae. The 4 tracheae of the two sides
thus formed are interconnected by narrow transverse branches from each other and the outer ones are
additionally connected to the lower lateral mesothoracic air-sac,The branches of the ventral tracheal trunk
supply the overlying ventral nerve cord, nerve trunks, digestive organs and the mesolegs.

*Spiracular trachea refers to the short trachea that arises directly from the spiracle and is generally
inconspicuous.
?For descriptive convenience the immediate divisions of the spiracular tracheae have been
designated as trunks, their subdivisions as tracheae and further divisions as branches.
368 K. P. SRIVASTAVA

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0
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X
a
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0
I
LIn
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2

X
U
112
0
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a
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2
0
0
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FIG.9.-Tracheal system of the preabdominal (head and thoracic) region in dorsal view. Saccular tracheae
and air-sacs are shown without taenidial striations.
 RESPIRATORY SYSTEM OF PAPILIO DEMOLEUS 369

Tvacheaticn of the inetathorax

The inetathorax is supplied by tracheae from the first abdominal sparacle (Fig. 8). The spiracular
trachea ot'this spiracle like that of the second thoracic spiracle divides into dorsal. anterior, pleural and
ventral tracheal trunks. The dorsal tracheal tvimk divides again into a metathoracic and an abdominal
trachea. iioth being saccular in nature. The metathoracic trachea crosses into the metathorax and joins its
c.ounterpart to form an extensive dorsal metathoracic air-sac which tracheates the dorsal longitudinal
irluscles of the segment. Several of its branches penetrate these muscles and come to lie on their ventral
;iirface where they ramify and anastomose to form a tracheal meshwork (not shown in the Fig.). On account
of the projecting phragmata in this region, the air-sac becomes lobed (shown by dotted line). Laterally the
air-sac bears a large fenestra giving passage to the dorso-ventrally disposed muscles and also tracheating
them. Antero-laterally the air-sac sends branchcs into the hindwings. The abdominal trachea of the dorsal
tracheal trunk divides further into a narrower lower branch broader upper branch. The lower branch runs
inwards and joins its counterpart to give rise to the dorsal tracheal commissure which tracheates the portion
of the heart in this region and the ventral surface of the dorsal tergal muscles of the first abdominal segment.

T
T

TTV

FIG.10.--Tracheal system of the abdominal segments in dorsal view with portions of internal organs in a
male butterfly.
370 K. P. SRIVASTAVA

The upper branch ascends the dorsal tergal muscles and joins its counterpart of the other side to form the
dorsal abdominal airsac which tracheates the tergal muscles from the dorsal aspect. The anterior tracheal
trunk is conspicuous on account of its broad cylindrical shape and more strongly cuticularised taenidia. The
trunk curves inwards and then runs forwards joining the second thoracic spiracle. On its way it gives out
lateral tracheae which are saccular and coalesce with each other to give rise to the lateral metathoracic air-sac
tracheating the inner surface of the dorso-ventrally disposed muscles of the segment. The pleural tracheal
rrunk takes a lateral course and tracheates the outer surface of the dorso-ventral and other metapleural
muscles. The ventral tracheal trunk (not shown in the Fig.) is a delicate saccular trunk which descends
ventrad and joins its counterpart to form the ventral tracheal commissure like the ventral tracheal trunks in
other abdominal segments (vide infra). The commissure tracheates the overlying ventral nerve cord and
digestive organs.

Tracheation of the abdominal segments

Each abdominal spiracle tracheates its own segment except the first and the last which respectively
treacheate the metathorax and genital segments in addition to their own (Fig. 10). The spiracular trachea of
each spiracle behind the first follows a generalised branching pattern as described by Snodgrass (1935) and
divides into dorsal, anterior, visceral and ventral tracheal trunks. The trunks themselves are broad and sac-
like but they give out long and narrow supplying tracheae. The size of the trunks in some segments may,
however, vary depending upon the amount of air present in them. The dorsal tracheal trunk divides into 2
tracheae soon after its origin. These tracheae supply the dorsal structures of the segment such as the dorsal
tergal muscles, heart, alary muscles, fat bodies and reproductive organs (gonads and genital ducts) in
appropriate segments. The anterior tracheal trunk is connected to the spiracular trachea of the preceding
segment so as to form a long lateral longitudinal tracheal trunk which not only runs throughout the
abdomen but also extends up to the first thoracic spiracle through the anterior tracheal trunks of the
pterothoracic segments thereby connecting all the spiracles of the body on either side. Behind each spiracle
the trunk gives out 1 or 2 small tergal tracheae to the lower region of the tergum. The visceral troclieal trunk is
obliquely disposed and supplies the gut mostly from the dorsal aspect, fat bodies and reproductive organs in
appropriate segments. The wntral tracheal trunk descends downwards and narrows as it runs inwards to join
its counterpart of the other side to form the ventrai tracheal commissure lying below the ventral nerve cord.
The commissure tracheates the pleuron, sternal muscles, ventral nerve cord and its ganglion, ventral
diaphgram and the ventral surface of the gut in each segment. The last ganglion of the ventral nerve cord
present in the sixth segment is tracheated by the commissures of both the sixth and seventh segments. This
indicates the composite nature of this ganglion. The genital segments, devoid of any spiracle, are tracheated
by the branches from the last spiracle.

Acknowledgments
The author wishes to thank Mr A. N. Singh, the artist of the Department, for his
help in the preparation of the illustrations.
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*Not seen in original.
[Manuscript received April 11, 19751