CHAPTER IV
THE CHORIONIC COLLAR
The chorionic collar is the distinctly differentiated anterior extension of
the chorionic rim of the egg, presenting a wide range of structural complexity
and to a certain extent could be considered as a taxonomic paradox. In fact,
the chorionic collar invariably assumes the functional responsibility of respi­
ration and fertilization of the egg, since the aeropylar and micropylar systems
are the integral parts of the collar and the rim. In many of the reduviid eggs
examined, air storage and regulation of humidity are mainly attributed to
the spongy, porous texture of the chorionic collar as well as similar structures
of the operculum.
/
The eggs of Harpactorinae are considered unique because of the elabo­
rate development and specialization of their collar, in the form of a veil,
which, together with the operculum, establishes a secondary air storing cephalic
region of the egg (the primary air storing region being the inner aerostatic
layer of the chorion). A typical veil type of chorionic collar has been presented
by rhinocorine eggs, especially Rhinocoris marqinatus. Here, the collar extends
forward as a continuous thin sheet from the chorionic rim, cicumscribing
the opercular crest and then apically reflecting inwardly to fuse with the
peripheral cells of the opercular crest (Fig. I and PI. I : 14 ; PI. XII : 1).
It is around this region of fusion, the veil presents two or three rows of porous
hexagons at which the veil breaks away as the operculum is pushed upward
during eclosion.
Structurally, the collar consists of a thin membrane on which the folli­
cular epithelial cells form elongate hexagonal imprints (PI. V : 6 ). The surface
68
of each cell that appears as milk white absorbent, absorbs water and turns
transparent under wet and high humid conditions but retains its original milk
white form when dry (PI. VI : 1). The chorionic collar of JR. kumarii is also
very rwuch similar to that of JH. marqinatus, except that it is relatively shorter,
since the opercular crest is also short (PI. V :1G).
In
the
other
harpactorine
species
such
as Coranus
obscurus
and
C. spiniscutis, the chorionic collar is of medium height, apically joining with
the peripheral cells of the crest, exposing the central reticulate projection
of the column (PI. VI : 12 & 13) of the opercular crest. The architecture
of this short collar is characterized by more regular pattern of arrangement
of hexagons. The net work of the veil injC. atricapillus (PI. VI : 11) is composed
of cells of varying sizes and shapes. Similar to the Coranus eggs, the chorionic
collar of Harpactor pyqmaeus, H. nilqiriensis, Sphedanolestes variabilis and
S. puldiriventris also apically deflects ' inward and fuses with the peripheral
cells of the opercular crest. The collar cells appear hyaline in _H. pyqmaeus
(PI. VII : 1) whereas in the other three species, 2-3 rows of cells, bordering
the chorionic rim, are apparently distinct and the apical
opaque (PI. VII : 2 - 4).
The
chorionic
collar
in
cells are more
Lophocephala
querini
is
of moderate height and merges with the outer flange of the opercular crest.
Its
surface
pattern
is
not different from those of JH. nilqiriensis
and
Sphedanolestes spp. in being opaque apically and hexagonally sculptured basally
(PI. VII : 8). In Coranus wolffi (PI. I
:20) and Euaqoras plaqiatus (PI VI : 3)
the collar is hyaline and spongy in texture, but not very prominent. Their
cell
markings resemble those of JH. pyqmaeus.
The chorionic collar of
N. therasii is more like that of Coranus spiniscutis. The hexagons are having
minute pores at the corners (PI. VII : 9). In Sycanus spp., the anterior region
69
of the egg is also specialized by the complex development of the chorionic
collar and the operculum. Here, the chorionic collar is a well differentiated
cylindrical net work, circumscribing the operculum. The collar is generally
composed of fine hyaline hexagonal cells.
The basal part of the collar cir­
cumscribing the central 'Columella, between the upper expanded portion of
the columella and the lower opercular crest, is distinguishable by its compactly
arranged small cells. Beyond this region the collar is composed of comparatively
large cells. The line of fusion of the collar with the opercular crest differen­
tiates a circular line of weakness from which the collar breaks away from
the chorionic rim (PI. I : 12; PI. V : 12; PI. XII : 9 & 12) and comes away
with the operculum. The chorionic rim, by its association with the opercular
crest, creates a narrow air space around the lower half of the opercular crest.
The periopercular space in Macracanthopsis nodipes is confined only at
the base of the opercular crest, since the short collar veil fuses with the
basal peripheral cells of the crest (PI. XI : 11). The cell boundaries of the
collar are indistinct (PI. VI : 9). In Rhaphidosoma atkinsoni, the collar presents
three to four longitudinal rows of hexagonal spongy cells. It curves inwards
to fuse with the peripheral border of the opercular plate (PI. VI : 6). Therefore,
the periopercular space is very much narrowed and shifted, towards the peri­
phery of the opercular plate (PI. XI : 12).
The chorionic collar in both species of Endochus (IE. cinqalensis and
JE. inornatus) is unique as it is being described here as a capitulate type of
chorionic collar (PI. XI : 1 & 5). The chorionic rim in these eggs is fairly
broad and it circumscribes the short basal half of the opercular crest enclosing
air space (PI. V : 1 - 3). At this level the chorionic rim gets fused with the
peripheral cells of the crest. This point of attachment forms the line of weak-
70
ness beyond which the chorionic collar converges over the rest of the opercular
crest enveloping it, and extends far beyond as a tubular stalk which distally
expands into a capitulum. At the time of eclosion, as the opercular sealing
bar snaps off from the mouth of the egg,
the chorionic collar also breaks
away along the line of weakness from the chorionic rim. Thus, this capitate
type of chorionic collar cum opercular complex in a hatched egg, when exa­
mined, will reveal the opercular crest retaining the tubular part of the chorionic
collar.
In the case of JE. cingalensis, the capitulum carries a terminal transverse
slit like opening and in ji. inornatus this opening is circular and large (PI. XI :
4 & 8). The tubular stalk of the capitulum in both species presents a texture
of spongy meshwork while the basal broad region of the collar that
circum­
scribes the opercular crest carries hexagonal cells (PI. XI : 3 & 7). The entire
length of the tubular stalk has several rows of longitudinal lamellae, repre­
senting a system of plastronic reticulations within the capitulum (PI. XI : 4).
Therefore, the perforated tubular stalk as well as the capitulum are functionally
concerned with humidity regulation, filtering of the air and serving as an
air store.
The chorionic collar in Cydnocoris qilvus is of special interest. It
develops from the chorionic rim and continues as a loose jacket around the
opercular crest, except at the region of its connection with a few peripheral
cells of the crest (PI. XI : 9). During eclosion, the chorionic collar disconnects
itself from the chorionic rim and retains its attachment with the peripheral
cells of the opercular crest. This collar, like a jacket, apically carries a cir­
cular opening through which the ambient atmospheric air communicates with
the periopercular space (PI. XI : 10). The spongy meshwork of the collar is
71
an effective'air store (PI. VI : 8).
In Platerus pilcheri, the inflexed thick
chorionic rim is beset with dense hairs of moderate length. As a flange, the
collar converges over the operculum, leaving a central opening. This fimbriate
type of collar carries less distinct follicular cell imprints (PI. V : 7). irantha
armipes also has similar fimbriate type of collar (PI. I : 17). But, here these
hairy structures are basally demarcated
by a region of compactly arranged
hexagonal cells and this region is followed by much elongate hexagons (PI. VII : 5).
Though the chorionic collar appears petaloid in Coranus sp, and in JR. fuscipes,
the petal like frills by nature, are extensions of the chorionic rim. In Coranus sp.
(PI. VII :6& 7)the collar components appear lobate apically whereas in JR. fuscipes
they are clavate. In none of these species, except in JR. fuscipes, the collar
frills establish any connection with the operculum. Each frill is composed
of smooth porous material that may, by their compact arrangement, serve
the function of air storage and to a certain extent may exhibit hygroscopic
movement, in a more or less similar way as in JP. affinis (to be described
below) (PI. VII : 6 & 11). In addition to the identification criteria such as
variations of
the
chorionic ornamentation
and opercular architecture, the
architecture of the collar also could be readily used for recognizing the eggs
of -El* pi^heri, L armipes, JR. fuscipes and Coranus sp.
In all the harpactorine eggs, whether the collar is developed in the
form of a veil with its connection with the opercular crest or in the form
of frills, as described above, their function as air transporting medium as
well as humidity regulation is most convincing.
All the Emesinae eggs examined do not present a chorionic collar
as extension of the chorionic rim, structurally corresponding to the collar,
as described in other reduviid eggs. The lameliiform type of chorionic rim
72
found in Ploearia sp. (Pi. VIII : 3), Ploiariola oculata (PI. VIII : 7), Luteva
feana (PI. VIII : 8), Ishnobaena sp. (PI. VIII : 9) and Gardena sp. (PI. VIII : 10)
has a distal hyaline region and a proximal coarse spongy region, traversed
by aeropyles ad micropyles. The micropyles open into the spermgroove that
run along the free edge of the chorionic rim. However, in Ghilianella sp.
alone the collar is represented as filamentous extensions of the chorionic
rim (PI. VIII : 4). These transparent filaments are slender, membranous
and differ in structure from the collar filaments of Piratinae which are com­
posed of complex plastronic meshwork.
The eggs of several reduviid subfamilies such as the Salyavatinae
(Lisarda spT PI. VIII : 16 ; Lisarda annulosa, PI. VIII, 15 and Petalochirus indicus
PI. VIII : 17); and Holoptiiinae (Holoptilus melanospilus, PI. VIII : 1), the
chorionic collar is reduced to
a mere lining, bordering the chorionic rim.
Ectrichodiinae (Vilius sp. PI. VIII : 2), Triatominae (Triatoma rubrofasciata
PI. IX : 16) and Acanthaspidinae (Platymerus laevicollis, PI. IX : 9 and
Acanthaspis sp. (PI. IX : 10), the collar is lost and their narrow lamelliform
type of chorionic rim, with the aero-micropylar system, resembles that of
Emesinae. The length, size and shape of the aeromicropyles and their arrange­
ment characterise the chorionic rim of each species. The fringedtype of collar
in many of the acanthaspidine eggs merges with the chorionic rim without
showing any sharp line of demarcation between the collar and the rim. This
line of demarcation of collar, bordering the mouth of the egg, is composed
of a spongy material that develops circular cavities at regular intervals, into
which the outer opening of the aeropyle is aligned. This has been considered
as a characteristic feature of Acanthaspidinae eggs (PI. IX : 1-7 & 11). The
depth and dimension of such cavities vary in different species. In Centrocnemis
dearmata, the transparent collar, constituted by 2-3 tiers of small hexagons,
73
is well differentiated from the comparatively broad chorionic rim (PI. IX : 6).
Interestingly, the chorionic collar and rim in Brassivola hystrix (PI. V : 3),
a Harpactorinae species, is also similar to the acanthaspidine type.
The micromorphology, of the chorionic collar of stenopodine egg could
be considered for their species identification. The chorionic collar of
Qncocephakis morosus has petaloid elongate hexagons composed of porous,
spongy material (PI. VIII : 11). In JD. kluqi, the cellular units are indistinct
but they all jointly form a low collar region (PI. VIII : 12). The collar in
Diaditus errabundus is produced into club shaped spongy processes of varying
lengths (PI. VIII : 13) whereas in Sastrapada baerensprunqi it has developed
into a narrow flange with small blunt processes (PI. VIII : 14).
Piratine eggs have attained a high degree of complexity in the organi­
zation of collar and opercular apparatus. All the piratine eggs have long fila­
mentous processes of the collar, composed of highly complex plastronic material
(PI. X : 1, 3, 4 & 10). Although similarities do exist in the micromorphology
of collar filaments among species, they are of different lengths. In _P. affinis,
_P. atromaculatus, and Ectomocoris cordiqer these chorionic filaments are
considerably long, extending far beyond the operculum (PI. IV ; 2, 3 & 8),
whereas in Catamiarus brevipennis, Ectomocoris spp. and Sirthenia flavipes
they are found as relatively short processes (PI. IV : 3, 9-11 & 13) almost
of the same length of their similar opercular filaments. The base of the collar
filaments is traversed by numerous grooves and striations and the aeropyles
in between the filaments open at points within the spongy region of the collar.
The cellular element of the collar filaments is aerostatic and hygroscopic.
Under humid condition, the filaments converge over the operculum, trapping
air within for plastron respiration and during dry condition they open and
74
spread out (PI. IV : 2, 3 & 10) exposing the operculum. The chorionic collar
filaments of JP. affinis are different in constitution from the filaments of
other piratine eggs. The dark brown opercular filament is ensheathed by the
exochorionic
collar,
forming
a
compound
filament.
Each of
the opercular
filament, (Fig. 2) forming the core, is intimately associated with the exo­
chorionic filament, ensheathing it. (Fig. 2 ; PI. XV : 11, 14, & 15). This struc­
tural relationship between these two filaments enhance their mobility caused
by the hygroscopic property of the sheath material.
The development of compound collar filament in _P. affinis has been
traced by studying the serial sections of the ovariolar eggs. Each opercular
filament is the intercellular product secreted between two rows of elongate
cells arranged in the longitudinal axis around the operculum (PI. XVI : 9,10
PI. XVII : 1). By the aggregation of the dark brown material secreted by the
two rows of cells, each long opercular filament is formed. Once the opercular
filaments are formed, the follicular cells concerned with their secretion become
obliterated. Outer to these filaments, there is another layer of fairly broad
cells designed for secreting the colourless, porous, collar material that ensheaths
each opercular filament to
form the compound collar filament (PI. XVI: 11).
The endochorionic and exochorionic layers of the chorionic rim are secreted
by the more peripheral follicle cells of the broad abruptly differentiated region
of the egg that lies outer to the cells that secrete the sealing bar (PI. XVII : 5).
Serial
sections
of
the
ovariolar
eggs
of
Sycanus,
Platymeris
and
Petalochirus also reveal that the peripheral cells of this broad abruptly differen­
tiated region undergo differentiation much early during ovarian development
and give rise to the characteristic chorionic rim and the collar.
Thus in Reduviidae, diverse patterns Df chorionic collar, either in asso-
75
ciation with the opercular apparatus or otherwise, could be considered as
ecophysiological specialization within each group.
DISCUSSION
The eggs of Reduviidae excel the eggs of most other insects in the
diversity of their chorionic architecture and elegance of their chorionic collar.
In the case of Harpactorinae and Piratinae more emphasis has been laid on
the structural complexities of the chorionic collar and its more intricate
association with the opercular apparatus.
The cephalic extension of the chorion from the mouth of reduviid
eggs can be readily recognized to have two distinct segments, namely the
chorionic rim and the chorionic collar. For that reason Cobben (1968) rightly
used the term "chorionic rim collar" to represent collectively the chorionic
rim and the collar. The chorionic rim is the strongly structured chorionic
region of the mouth of the egg where both the exo chorionic and endo chorionic
layers are fused to
form a tight surface for the aeromicropylar system and
the opercular sealing bar. The collar could therefore be rightly defined as
the further extension of the chorionic rim. There is no sharp line of delineation
between them, since the aeropyles invariably extend beyond the chorionic
rim and open externally either at the chorionic rim margin or within the
collar.
The chorionic collar of harpactorine eggs has received considerable
attention from several workers. Miller (1953a)and Southwood (1956) have given
general informations on the collar and the rim, while Cobben (1968), Cobben
and Henstra (1968) Salkeld (1972) and Haridass (1986a) by their electron micro­
scopic studiesj have provided their ultrastructural details. Scanning Electron
Micrographs of the veil, provided by these authors, have confirmed the per-
76
forated nature of the hexagonal collar cells. A crown of mushroom like bodies
present within the uniformly spread honeycomb of the opercular outgrowth,
where the veil fuses with it, has also been described by Cobben (1968).
In the present investigation, it is found that the veil of JR. marqinatus
distinctly carries 2-3 rows of hexagonal perforations all around its line of
fusion with the peripheral cells of the opercular crest (PI.- XII : 2 & 3). These
perforations thus directly communicate with the space between the veil and
the
opercular column, here referred to as the periopercular space. Similarly,
the
apical apparatus of the capitulum
spp, Platerus pilcheri and the chorionic
of the chorionic collar in Endochus
collar jacket of Cydnocoris also form
a common passage to communicate with the periopercular space.
Salkeld
(1972) in the harpactorine species Zelus exsanquis
explained
the veil as the extension of the chorionic rim composed of shallow honeycomb
shaped cells, set on a thin layer of chorion and the veil breaking off readily
from the chorionic rim at the point where the ribs become enlarged. The
ribs, according to him, are solid extensions of the chorionic rim that become
enlarged and merge with the cell walls of the veil. Unlike the structure and
function of the collar cells, as described by Southwood (1936) in Rhinocoris sp.,
Salkeld (1972) had suggested that the highly porous walls of the veil cells
in Zelus exsanquis were respiratory and a coating of viscous material on it
was described by him to be hygroscopic. Haridass (1985b)by his earlier mistaken
identity of the exochorionic filaments of the collar in piratine eggs as the
"endochorionic extensions", tried to affirm that the veil in harpactorine eggs
also represent the endochorionic part of the collar. Cobben (1968) considered
that
Harpactorinae,
Apiomerinae,
Physoderinae
and
Phonolibinae
common type of egg by the presence of a continuous net work region.
I
share
a
77
The long filamentous processes of the piratine eggs were considered
earlier by Readio (1926) Miller (1953a) and Southwood (1956) as part of the
net work region. The ultrastructure of these filamentous appendages have
been confirmed to be plastronic and the motility of these filaments has been
suggested by Cobben (1968) as a respiratory control mechanism. A similar
phenomenon was also reported for the first time in Loricula spp.(Microphysidaes)
by Cobben (1968). Earlier, Barber (1923) in Sinea diadema (Harpactorinae)
and Readio (1926) in some Piratinae, reported that their fringe like collar
exhibited a similar mechanism. Haridass (1985b) made certain confusion by
describing the chorionic rim region as a prominent collar consisting of two
distinct regions, "an outer collar rim, composed mostly of exochorion, projecting
away from the central axis and enclosing a ring like spermatic groove on
its inner side and an inner 'J' shaped sealing bar, formed wholly of endochorion,
the basal free edge of which being slightly turned upwards projecting into
the lumen of the egg like a ring". The funnel shaped mouth of the micropyles
are situated within the exochorionic meshwork of the chorionic rim. A ^permgroove connecting these outer openings of micropyles is not so obvious as
in other reduviid eggs, because of numerous grooves and ridges of this region
(PI. X : 9). The sealing bar is the wedge shaped posterior margin of the
opecular plate. The "J" shaped part described by Haridass (1985b) in reality,
is the notch on the inner side of the chorionic rim into which the sealing
bar snugly fits (PI. XVI : 9 & 12). As described by Cobben (1968) the serosal
cuticle wedges itself into the recess between the sealing bar and the main
shell. Since the inner projection of the notch is found closely associated with
the serosal cuticle (Fig. 2) 'a circular ring like projection, projecting
into
the egg', as described by Haridass in piratine eggs is therefore misleading.
The extent of development of the chorionic collar of all the reduviid
78
eggs so far examined, suggests that it has some relationship with the manner
of egg deposition in the respective ecosystem. In Harpactorinae, the eggs
that are deposited by those species in the Tropical Rainforests, Scrub Jungles
as well as Semiarid Zones have been found with such a chorionic collar that
has developed in the form of a veil, enclosing a periopercular air space in
between the veil and the opercular crest. Corresponding to the height
of
the opercular crest, the extent of development of the chorionic collar also
varies. The veil has been found to have reached the maximum height, corres­
ponding to the height of opercular crest, in JR. marqinatus
while in
Sphedanolestis spp., Neohaematorophustherasii, Euaqoras plaqiatus, Macracanthopsis
nodipes etc., of the Scrub Jungles, it shows varying degrees of development
in its height and complexity. An extreme condition of reduction of the collar
height and the extent of the periopercular space has been found in Rhaphidosoma
atkinsoni. Irantha armipes, Rhinocoris fuscipes and Coranus sp. have attained
a fimbriate type of collar, different from the common network collar. In
these species it is of a specialized texture, to meet the demands of the humid
as well as dry conditions of the Scrub Jungles and Semiarid Zones. Interestingly,
in these eggs, the opercular crest is not massive, as it is characteristically
found in most other harpactorine species. However, the existence of chorionic
collar - opercular complex with the complementary periopercular s, ace, the
extension of the aeropyles of the chorionic rim farther along the collar cells
and their external openings into the periopercular space could be regarded
as adaptive modifications, both for humidity regulation and respiration. Such
a condition has been found to prevail among eggs that are cylindrical relatively
smooth and glued vertically, in clusters.
According to Cobben (1968) the excessive enlargement of the network
region and correspondingly the extension of the rim and aeropyles as in Miridae,
79
Tingidae and Harpactorinae are
more recent developments whereas Southwood
(1956) considered the absence or presence of a small network region on the
chorionic rim as a secondary nature. Piratine eggs that are usually buried
in the soil and sand have developed a highly specialized perforated plastronic
collar filament, more efficient than the harpactorine collar veil, in regulating
the humidity and continually restoring air for respiration.
The reduction or absence of a chorionic collar and a reduction of opercular
crest, to almost
a remnant, in the eggs of Emesinae could be considered
as a deviation from the main line of adaptation of the chorionic collar opercular complex, commonly met with as a basic type in Harpactorinae.
The chorionic filaments found in Ghilianella sp. is an intermediate condition
where chorionic collar is broken up into stiff filaments, both the filaments
and rim have
lost its net work and spongy texture.
Considerably short chorionic collar in the eggs of Holoptilinae, Stenopodinae,
Salyavatinae and in several species of Acanthaspidinae may be considered
as the outcome of lesser importance being attributed to a collar in
Scrub
Jungles, Semiarid Zones and other drought prone ecosystems. The chorionic
collar and the opercular filaments of stenopodine eggs appear to be more
similar to piratine collar in structure. While in the eggs of a few species
of Acanthaspidinae, such as the Platymeris laevicollis (PI. IX : 9) and another
Acanthaspis sp. (PI. IX : 10), as well as Triatoma rubrofasciata (PI. IX : 16)
and the ectrichodine species Vilius (PI. VIII : 2), the total absence of the
collar and direct communication of the aeropyles that are confined to the
chorionic rim, with the ambient atmospheric air, as in the eggs of Emesinae,
could be considered to have acquired the greater adaptation, which is deviated
far from the harpactorine type.
80
Thus the development of the chorionic collar with all its complexities,
is diverse and variable from species to species within each genus and not
constant throughout Reduviidae. Its ecophysiological importance in the res­
pective ecosystem however, is beyond any reasonable doubt. Therefore it
will lead to the conclusion that chorionic collar is also a factor providing
ample evidences to draw a line of evolution on its course of development
with respect to the ecosystem.