Zool. J. Linn. Soc.. 55: 193-224. With 2 plates and 26 figures
November 1974
Evolution of larval head-fans in Simuliidae
(Diptera) as inferred from the structure and
bioiogy & Crozetia crozetensis (Womerstey)
compared with other genera
LEWIS DAVIES
Department of Zoology, University of Durham
Accepted for publication April I974
The life stages of C. crozetensis whose larvae have raking head-fans are described.
Functional anatomical study of the fans compared with the filtering fans of normal
Simuliidae together with SEM study of first instar larvae of Gymnopais, Twinnia and
Prosimulium enable the evolution of cephalic fans to be inferred as follows: a group of
lateral labral bristles evolved in two directions:
1. To complete loss in Gymnopais and hvinnia whose ancestors therefore never
possessed fully developed fans.
2. Elaboration of the group of bristles first into raking organs, as in Crozetia, and later
into even more complex filtering organs.
It is shown that unflexing of Simuliid fans depends on elastic energy stored in
resilin-containing components deformed during flexin .
Adults of Crozetia mate on stones in streams on le de la Possession, ?les Crozet. The
females are non-biting and rest near streams while their eggs mature, thus forming a
sub-Antarctic parallel to certain sub-Arctic Simuliidae.
fi
CONTENTS
Introduction
. . . . . . . . . . . . . . . . . . . .
.
Structure of the life stages of Crozetia crozetensis
. . . . . . . . . . . . . .
Mature larva
. . . . . . . . . . . . . . . . .
. .
Pupa
. . . . . . . . . . . . . . . . . . . . . .
Male
. . . . . . . . . . . . . . . . . . . . . . .
Female
. . . . . . . . . . . . . . . . . . . . .
Significance of certain characters and the affinities of the genus
. . . . . . .
Structure and functioning of the larval head-fan of Crozetia compared with that of
normal Simuliidae
. . . . . . . . . . . . . . . . . . .
Labral region in Crozetia
. . . . . . . .
. . . . . . .
Head-fan base in normal Simuliidae
. . . . . . . . . . . .
Flexing and unflexing movements of head-fans
. . . . . . . . . .
Crozetia
. . . . . . . . . . . . .
. . . . .
Normal Simuliidae
. . . . . . . . . . . . . . . .
Comparison of Oozeria with normal Simuliidae
. . . . . . . . .
Labral region in first instar larvae and the condition of the anterior palatal bar in them
and later instars
. . . . . . . . . . . . . . . . . . . .
Biology of Crozetia o n h e de la Possession, fles Crozet
. . . . . . . . . .
-
-
I
-
14
193
194
194
194
197
198
200
200
202
202
206
208
208
209
213
21 3
216
L. DAVIES
194
. .
Discussion
Summary . . .
Acknowledgements
. .
References
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
.
218
221
222
223
INTRODUCTION
Crozetia crozetensis is known only from iles Crozet (47"S, 5 1' E), part of
the French sub-Antarctic Territories, and is probably the black-fly species that
is most geographically remote from any other Simuliidae, the nearest of which
occur some 2000 miles away in South Africa. It is the sole simuliid known
from truly oceanic sub-antarctic islands and was discovered by the late Dr
J. W. S. Marr on the B.A.N.Z.A.R. Expedition on a brief visit to iles Crozet in
1929 en route to Antarctica.
The larva of this black-fly is aberrant in structure, principally in possessing a
pair of short head-fans that have a raking function, in contrast t o the
homologous larger head-fans of normal Simuliidae where they function as
filtering organs in running water. The main purpose of this paper is to give the
results of a functional anatomical comparison of the raking fans of Crozetia on
the one hand, with the filtering fans of normal simuliid larvae on the other. The
results of this comparison in conjunction with an SEM study of the first instar
larvae of various genera together with the recent comprehensive study of the
labral region in larval Simuliidae published by Craig (1974), enable an
interpretation of events in the evolution of head-fans throughout the family to
be presented.
In 1968 and 1972-3 I spent several months on ile de la Possession, one of the
easterly islands of the Crozet group, and was able t o study this interesting
black-fly in the field in all its stages, and to collect abundant material for
anatomical study. Since I am the first student of the family t o have had an
opportunity to observe Crozetia alive in the field, one of the purposes of this
paper is to record biological observations of this insect in its remote
sub-Antarctic home. The hitherto unknown pupal stage is described and
existing incomplete descriptions of the other stages (Womersley, 193 7 ; Stguy,
1940: Dumbleton, 1962; Davies, 1965) are modified and amplified.
STRUCTURE OF THE LIFE-STAGES OF CROZETIA CROZETENSIS
Mature larva
Length 7.5-1 3 .O mm. Body uniformly brownish grey, some muscle insertions
forming small paler marks. Shape in life unusual (Fig. l ) , abdomen differentiated into a highly flexible concertina-like anterior part and an evenly swollen
convex posterior part; first four abdominal segments in the form of swollen
annulae separated by deep intersegmental constrictions, expanded posterior
part characterized by a large dorsal swelling with smooth shining cuticle
delimited ventrally by a ridge and furrow from the undistended venter (unique
shape of body usually much less evident in preserved material).
Thoracic proleg slender, without differentiated lateral sclerites and spines,
and with the circlet hooks extremely fine (not resolved at magnification x 50).
Abdominal apex rather elongate and slender, posterior circlet unusually small
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
195
Imm
Figure 1. Crozetiu crozerensis, mature larva.
0
;”[
3
2
4
Figures 2 to 4. C.crozetensis. 2 . Posterior attachment organ and anal sclerite. 3. Lateral view of
larval head. 4. Postero-dorsal view of mature larval head.
in relation to larval size and formed of about 160-180 rows of 20-28 hooks per
row. Anal sclerite (Fig. 2) with anterior arms expanded distally with two
unsclerotized “windows” near bases of posterior arms and with the latter
extending around the end of the abdomen to a variable extent (from two-thirds
196
L. DAVIES
0.5 m m
Figure 5. C. crozetensis. Head of mature larva viewed from slightly ventral to direct head-on
plane. The fan on the left is fully unflexed. that on the right partly flexed. The mandibles
whose rectangular tips almost meet medially are shown fully adducted. For details of other
parts represented see text.
to full encirclement regardless of mature larval size); if posterior arms forming
full circle then frequently narrowly interrupted symmetrically at two points
(each side of the mid-ventral break in the posterior circlet). Anal gills simple
finger-like, peri-anal cuticle bare; cuticle surrounding anal sclerite also bare.
Head capsule dark brown to black, in dorsal view approximately parallelsided for anterior two-thirds, then rapidly and evenly narrowed in a convex
curve to the occipital edge; no spots marking muscle insertions on apotome,
but insertions sometimes visible as area with higher shine than surrounding
cuticle. In side view (Figs 1 and 3 ) head particularly convex postero-dorsally,
giving appreciable degree of hypognathy; in this view (Fig. 3) the black
occipital collar, the very wide sclerotized buttress extending ventrally from
behind the short antennae to posterior part of hypostomium, and the massive
mandibles are conspicuous. Cephalic apotome in posterodorsal view of head
slightly widened about halfway from its anterior end, then rapidly narrowed on
posterior half, sometimes as narrow as shown in Fig. 4; this narrower part of
the apotome relatively wider in earlier instars, but its width varies in undoubted
last instars from that shown in Fig. 4 to about one-third of posterior head
width. Post-genal cleft, absent in younger instars, a small rectangle with
rounded corners in mature larvae. Cervical sclerites firmly attached to occipital
collar (Fig. 4). Maxilla of normal form, the extensively haired lobe rather long;
palp 2.7-2.9 x as long as its basal width. Hypopharynx normal in form, but
with medial hair tuft (shown in Fig. 5 ) that occupies the space between the
lateral tooth groups of the hypostomium when the hypopharynx is protracted.
Details of the massive mandible and its setae as described previously (Davies,
1965); corresponding details of hypostomium given in Womersley (1937).
EVOLUTION OF SIMULIID LARVAL HEAPFANS
197
Detailed description of the head-fans and associated median part of the
labrum is deferred until p. 202; here the appearance of the fans and their
interrelations with other head components are described, as these facts will
assist in understanding their functioning as will be seen later.
Figure 3 shows the fans in flexed position in side view of head, with the
mandibles half-adducted when the group of strong spines on the distal internal
face of the latter are in contact with the fan rays; also shown is the extensive
hairy maxillary lobe lying medially to the palp. When fans are fully unflexed,
the tips of the rays form an approximate straight vertical line when head
viewed laterally, instead of the curved line of the flexed position shown in
Fig. 3.
In head-on view with fans fully unflexed, the serried inner edges of the rays
form a large flat surface whose outer edges are bounded by a raised rim formed
by the regular array of the curved, toothed distal portions of the rays (Fig. 5 ,
left fan). The relatively narrow space between the two unflexed fans is
occupied by the median portion of the labrum whose soft median palatal brush
hairs are displaced into a flattened mat when the head and fan assemblage are
in contact with the substratum, so that the palatal brush fills the median space
between the fans, and is flush with the flat surface mentioned above formed by
the inner edges of the rays.
Other features seen in head-on view (Fig. 5 ) are as follows. The high
hypostomium is markedly curved upwards partly closing medially the space
leading to the cibarium and meeting the bottom part of the palatal brush and
its epipharyngeal lobe when the latter is fully protracted (the lobe is shown in
Fig. 5 as the median finely-haired portion just dorsal to the blunt tips of the
adducted mandibles); the elongate hairy maxillary lobes occupy the space
ventral t o each fan, and the tips of the palps are seen at the outer end of each
lobe.
Pupa
Figures 6 t o 8. Length 2.7-4.8 mm. Cocoon very slight, of sparse irregular
but tough strands around distal third of abdomen. Wing cases and leg sheaths
projecting ventrally considerably below line formed by underside of abdomen
(Fig. 7) which in life is gently curved ventrally particularly towards its tip.
Respiratory filaments varying from 10 to at least 40 in number (although some
may be accidentally lost this variation is real) arising from the foot of two
tuberculated processes one larger than the other, with scattered strong, short
spines on surrounding cuticle (Fig. 8). Dorsum of thorax with short soft hairs
of variable density, always more numerous anteriorly. Antenna1 sheaths less
flush with pupal head surface than normal; face of sheath that is applied to
head capsule cuticle thin and unsclerotized as is normal, but the tract of head
cuticle is fully sclerotized. (In pupae of all other Simuliidae that I have
examined, both cuticular surfaces are transparent and unsclerotized.)
In cast skins, cuticle of whole abdomen brown and fully sclerotized, not
paler and less sclerotized than that of the thorax to varying degrees as in all
other Simuliidae examined; cuticle of abdominal segments 3-8 forming almost
complete stiff hoops, only very narrowly interrupted by tracts of striated
cuticle ventro-laterally ; seventh sternum divided medially by longitudinal tract
of striated cuticle; eighth sternum sometimes with weaker median division.
198
L. DAVIES
Imm
Figures 6 and 7 . C. crozerensis pupa. 6. Dorsal view 7 . Lateral view.
Abdominal chaetotaxy mainly of long, almost straight rather weak spines,
variable in number and forming a row running near middle of each tergum;
segment 7 with a group of irregularly arranged long spines ventro-laterally,
continuing the tergal spine row; two terminal segments with simple hooks
irregularly arranged ventrally, totalling 18-23 on segment 8, and 5-8 on segment
9; although some hooks arise from elongate elevated bases, none have more
than one arm. N o other hooks, spines or spinelets present, so that segments 3-7
are naked ventrally; the fine short lines shown at anterior edges of the terga in
Fig. 6 represent cuticular striations and folds, not rows of fine spinelets such as
are present in many pupal Simuliidae, and which are quite absent in Crozetia.
Male
Wing length 3.0-4.7 rnm. Head with extensive long-haired occiput; eyes with
division between large and small faceted regions forming a sloping line in side
view (Fig. 9), so that the two regions are sub-equal in area; large eye facets
barely twice the size of small facets. Antennae 11-jointed, scape and pedicel
only with several irregularly arranged setae (a few shown on scape only in
Fig. 9). Palps short, sense organ of third segment fairly small; fourth segment
short, little longer than third segment.
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
b
"
_
;
'
\
199
I
-
%
b
9
1
0 Imm
8
r
0 Imm
13
Figures 8 to 14. C. crozetensis. 8. Base of pupal respitatory organ. 9. Side view of male head
(left) and that of female (right). 10. Wing with macrotrichia omitted. 11. Ventral view of male
hypopygium. 12. Internal view of style. 1 3 . Lateral view of ventral plate. 14. Ventral view of
ventral plate and associated parts.
Thorax dorsum low-arched in side view, of similar profile to female, with
erect dark hairs; whole thorax blackish brown with bare pleural membrane.
Halteres dark brown; katepisternum short and deep in side view, mesepisternal
suture open and shallow, evanescent anteriorly (figured in Davies, 1965).
Wing (Fig. 10) parallel-sided and rather narrow, reflecting the fact that anal
area up to tip of Cu 1 is slightly less extensive than for example in Prosimulium
sensu stricto. Wing membrane slightly brown because microtrichia are dark;
200
L. DAVIES
wing veins dark. Spiniform macrotrichia clearly distinct from hair-like ones,
distributed as follows: on distal four-fifths of C and distal half of R 1, none on
Rs which along with R has a few hairs on dorsal surface only. Spiniform
macrotrichia on C very sparse basal to entry of Sc to it, but numerous from
that point onwards; basal section of R and its continuation R 1 naked
ventrally. Articulation of Rs with R with distinct interruption of the former
(The varying state of this junction in other simuliid genera is discussed by
Davies, 1965.) Rs curves distally to run close to R for considerable length and
shows no sign of a second branch. Submedian fork and A 1 very faint, not
visible in some specimens; sinuation of Cu 2 very slight, A 2 very distinct and
basal cell present.
Legs unicolorous blackish brown with sparse, longish hairs; claws not
unusual in size or attitude for male Simuliidae, contary to the tentative
suggestion of Davies (1965);hind basitarsus without calcipala, 6.0-5.5x as long
as wide; pedisulcus absent.
Abdominal tergites and scale blackish brown, slightly shining, with rather
sparse long dark hairs; membranous areas slightly paler. Genitalia. In ventral
view of whole hypopygium (Fig. 11) ventral cuticular hoop of segment nine is
wide (twice as wide as in Prosimulium sensu. stricto. spp. examined and three
times as wide as in Simuliini where segment nine ventrally is a narrow cuticular
band. Carinate ventral plate projects slightly between the coxites. Styles in
ventral view (Fig. 1 1 ) with narrow tips polished black; in internal (medial) view
(Fig. 12) style tip appears less pointed and bears two blunt spine-teeth. Ventral
plate (Figs 13 and 14)medially carinate, with short hairs on lateral faces clearly
arranged in rows. Median sclerite and parameres weakly sclerotized (dotted
outlines Fig. 14),parameral arms stronger.
Female
Very variable in size, range as given for male. Head with rather small eyes
and thus extensive occiput and upper frontal regions (Fig. 9). Palps short,
mandibles and maxillary blades toothed (the former on both sides) but weakly
sclerotized, non-biting in form. Cibarium unarmed. Hind basitarsus 7.0-7.5 x as
long as wide. Claws with largish basal tooth (Fig. 15). Para-procts rather small
and gonapophyses in side view of genitalia rather drooping, with dense long
setae (Figs 16 and 18). Spermatheca rather large, as large as gonapophyses,
slightly elongate, with fine wrinkles running along long axis, and small
unsclerotized area where the duct joins it. Other parts of the female as
described for male.
SIGNIFICANCE OF CERTAIN CHARACTERS AND THE AFFINITIES
OF THE GENUS
The larva and pupa of Crozediu present suites of characters in general so
different from other Simuliidae that they provide no clear indication of the
affinities of the genus to other Prosimuliini. The adults, on the other hand,
possess very few features differentiating them from other Prosimuliini, and so
do not help significantly in a tribe in which adult characters alone are, in any
case, insufficient for reliable assessment of phyletic affinity.
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
201
;[
--c
3
15
16
17
J
18
0.2mm
Figures 1 5 to 18. C. crozerensis female. 15. Claw. 16. Tip of abdomen. 17. Cerci, paraprocts
and genital fork. 18. Gonapophyses with most of long setae omitted.
The extension of the posterior arms of the anal sclerite of the larva around
the tip of the abdomen is a character that occurs elsewhere in Prosimuliini only
in certain Southern Hemisphere forms, in Giguntodux Enderlein of southern
South America, and certain Australian species of Cnephiu of authors (not
Enderlein).
The extraordinary series of long straight abdominal spines of the pupa can
perhaps with equal plausibility be regarded, relative to normal Simuliidae, as a
plesiomorphic or as an apomorphic feature peculiar to Crozetia. The condition
of the antenna1 sheaths, the way in which the wing and leg sheaths extend
ventrally well below the ventral line of the abdomen, the heavily sclerotized
abdomen as a whole and the absence of anterior tergal spinule rows can perhaps
all be regarded as plesiomorphic features. In adults, the rather steeply sloping
line delimiting the large from small eye-facets in the male is a feature that
202
L. DAVIES
recurs in many Prosimuliini in many parts of the world. The decidedly gentle
curve of Cu 2 in the wings of both sexes suggest affinities with the same taxa
mentioned above with regard to the larval anal sclerite feature. The relatively
small eye area in the female leading to wide frons and extensive occiput, the
relatively small upper eye facets and reduced total eye area landing to
feminization in overall appearance of the male with its low-arched mesonotum,
zogether with the wing shape, are all features that I regard as relatively recent
apomorphisms developed in situ since Crozetia arrived on iles Crozet, and
correlated with its non-biting female mouthparts and concomitant adult
biology involving reduced flight activity of which details are given in the later
section on the biology of the species. But the exceptional width of the ventral
hoop of the ninth abdominal segment in the male (Fig. 11) seems a
plesiomorphic feature and not an apomorphism correlated with the groundmating habits of Crozetia since in Cnephia (C.)
dacotense D. and s., which
mates in a similar way, the corresponding part is a normal narrow cuticular
band.
On adult features alone Crozetia would fit near the African subgenus
Procnephia of Prosimulium sensu lato of Crosskey (1969), while the gently
curved Cu 2 and the larval analsclerite form are features that d o not occur in
any African Simuliidae, Although these features of Crozetia occur in
Gigantodax and the Australian forms mentioned earlier, these differ from
Crozetia in very many other features. We are left with little indication of
affinities. South America would appear to be a plausible source of a colonizer
black-fly for iles Crozet, supported by the existence of a few other Diptera on
the islands of probably South American origin.
STRUCTURE AND FUNCTIONING OF THE LARVAL HEAD-FAN OF
CROZETIA COMPARED WITH THAT OF NORMAL SIMULIIDAE
Labral region in Crozetia
The complete labral region of the late instar Crozetia larva is shown in
Fig. 19. It should be noted that the fan rays are shown near the flexed position
at the end of the active or raking stroke; in the completely unflexed position,
ready for the start of the raking action, the rays are rotated outwards through
75-85", pivoted of course at their articulation with the end of the main base
sclerite. The approximate angle of the ray base in this latter position is shown
by the dashed outline on the right organ in Fig. 19. For clarity this drawing
does not show the full number (25-33) of rays actually present.
Following the detailed studies of the labral region of larval Simuliidae made
by Craig (1974) and related to the components of the labral complex in other
Nematocera Culiciformia, the homologies of various sclerites in the Crozetia
labrum are clear and are followed in this account. Contrary to my previous
uncommitted view (Davies, 1965) the large complex sclerite within the base of
normal Simuliid head-fans is accepted as undoubtedly the main part of the
torma. To the torma is inserted the apodeme of the fan-flexing muscle (muscle
61, posterior fronto-labral in the nomenclature of Matsuda, 1965) which the
present work confirms to be interdigitated as shown by Craig.
In Crozetia the torma (Fig. 19) is a rather large sclerite, with a plate-like
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
pb
I
tr
I
I
I
I
I
203
u
25pm
I
Figure 19. C. crozetensis. Ventral view of labral complex of mature larva.
posterior extension (et) which articulates with the heavily sclerotized posttorma (pt). The apodeme of muscle 61 is inserted on the narrower portion of
the torma within the fan base, and thus beyond the line joining its two
articulations, namely with the post-torma on the one side and with the anterior
palatal bar (ap) on the other. The narrower main part of the torma continues
within the fan base as a rod curving through 90°, this curved part running close
to the cuticle covering the ventral-internal face of the fan base; it seen in
Fig. 19 as the more heavily shaded inside end of the torma, since in the drawing
the terminal part is seen end-on, in a plane normal to the paper.
The anterior articulation of the torma with what is identified, in agreement
with Craig (1974), as the anterior palatal bar (ap) is achieved through a
distinctly differentiated part of the torma, namely a more lightly sclerotized
band of striated cuticle (sb). In Fig. 19 this is visible on the left fan only; when
the torma is rotated, as it has been unintentionally through pressue in the right
fan, this striated cuticle band virtually disappears because it is seen end-on
against the more heavily sclerotized part of the torma and the posterior end of
the anterior palatal bar.
Details of the articulations of the torma seen in another preparation are
shown in Fig. 20. The ventral end of the post-torma (pt) is seen to fit into a
partial socket on the underside (i.e. dorsal to) the edge of the posterior tormal
extension. Also shown is the striated portion of the torma articulating with the
204
L. DAVIES
....
.et
Figure 20. Fan base of Crozeria showing insertion of apodeme of muscle 61 and articulation of
posterior extension of torma with post-toma.
end of the anterior palatal bar, and the insertion of the apodeme of muscle 61.
Other features of the Crozefia fan (Figs 19 and 20) to which attention is
drawn are as follows. The convex area of mainly transparent cuticle covering
the internal aspects of the fan base and connecting the internal angles (ia) of
the rays with each other, with the main base sclerite (mb) and the remainder of
the labral region of the head, bears two features. Firstly a sharply curved lightly
sclerotized band (1s) the proximal end of which approaches but does not appear
actually to meet a second dorsally situated short knob-like extension (ep) of
the anterior palatal bar. Secondly, on the ventral face the cuticle bears an area
with small separated sclerotized plaques giving a “crocodile-skin” appearance
(pa).
The median portion of the labrum between the two head-fans is relatively
narrow and bears a well developed, palatal median brush (pb) of simple soft
bristles. Completing support of the labrum is a transverse rod (tr) running
ventral to the anterior ends of the anterior palatal bars of each side. This
transverse rod is sometimes straighter and thinner than in the specimen shown
in Fig. 19, but some transverse labral stiffening, connecting the fan region of
each side is always present in late instar larvae; it is not differentiated in earlier
instars. Further support of the median part of the labrum is provided ventrally
by the intertorma (it), the ends of the Ushape approaching the front ends of
the anterior palatal bars. Medially the intertorma bears a descending rod (ti) of
variable shape, but usually expanded at its tip and bearing four sclerotized
teeth that lie behind the four basiconic sensilla (bs) that themselves are slightly
separated from the intertorma.
From the anatomical facts given above and displayed in Fig. 19 it is seen that
in Crozetiu there exists a continuous chain of interconnected and articulated
EVOLUTION OF SIMULIID LARVAL HEADFANS
205
Figure 21. Fan base of Prosimulium ferrugineum Wahlberg viewed ventrally. Anterior side is to
left of drawing.
sclerotized parts across the whole labral region from the post-torma of one side
to that of the other, while the post-tormae are themselves firmly connected to
strong cuticle running back to the post-antenna1 buttresses (Fig. 3). In this
chain of sclerites it is only the element termed the torma (dr), to which muscle
61 is inserted that is free to make the considerable independent movements
which result in the raking action of the fan rays discussed later. The intertorma
to which muscle 62 is attached (muscle not shown in Fig. 19) mediates
movement in a postero-ventral direction (i.e. protraction) of the median part of
the labrum with its palatal brush.
The significance of these arrangements will be discussed later (p. 214) in
relation t o the raking action of the head-fans in Crozetia and compared to the
feeding by brushing or raking with the anterior palatal brush carried on in the
head-fan-less larvae of Gymnopais Stone and Twinnia Stone & Jamnback.
206
L. DAVIES
To complete the anatomical account of the head-fans of Crozetia the
following facts are presented. The basal comers of the rays (Fig. 19, bc) are
close together, forming a short gently curved line, not a longer deep curve of a t
least 230” as in the corresponding ray bases in the head-fans of normal
black-fly larvae (Fig. 21). When the fan is unflexed at the start of the raking
stroke, the internal angles (ia) of each blade or ray are more widely separated
than are the fixed basal comers; when the fan is flexed, the internal angles of
the rays are drawn appreciably closer together, resulting in their distal toothed
ends coming closer together as the fan completes the raking stroke. There is
thus an opening and closing movement of the ray tips relative to each other,
simultaneously with the raking stroke (and conversely on the return movement) but the amount of angular movement in the former action is minute
compared to the latter. Further consideration of the feeding movement of the
fan is deferred until the morphology of the fan of normal Simuliidae has been
considered.
Head-fan base in normal Simuliidae
A functional anatomical study of the filtering head-fan base was made using
dissection, sectioning, staining and manipulation of the relevant parts of larvae
of various European, North American and Australian species of both
Prosimuliini and Simuliini. The head-fan bases of this diversity of species are
remarkably similarly constructed and the account given below applies broadly
to most Simuliidae with filtering larval head-fans. Since the anatomy of these
parts has been described previously, among others by Fortner (193 7), Grenier
(1949) and Chance (1970), attention is confined here to structural features and
inter-relationships that were either omitted or incompletely described by these
investigators. Also attention is given to direct comparison where possible of
homologous parts in these filtering fans on the one hand, with those in the
raking fan of Crozetia on the other, since this is a necessary preliminary to the
comparative account of the flexing and unflexing movements in the two types,
given in the next section.
Figure 21 shows the head-fan base of Prosimulium ferrugineum Wahlberg.
The expanded distal plate (dp) of the torma bears an accessory plate (cp) with
a thickened edge (ta), the latter termed the ‘‘sclirite prolongeant l’ar2te
interne” by Grenier, and also has a basally directed rod (ra) bearing the medial
rays (mf) or “Cventail marginal” of Grenier. In addition to being very narrowly
hinged at its posterior corner to the edge of the distal plate, the accessory plate
is connected to the torma by a fine tendon-like structure (tn) difficult to locate
in many preparations because i t lies for much of its length close to the
thickened edge (ta).
The distal and accessory plates of the torma form part of the ventral
cuticular surface of the fan-base, and their edges are connected to the
apophyses (as) of all main fan rays by a thin, strong, flexible, transparent
cuticular sheet. This cuticular sheet can only be seen properly in sections and is
completely inelastic (as is shown by direct manipulation with needles of pieces
detached by appropriate dissection). A fact not mentioned by previous workers
is that membranous cuticle also occurs as a narrow connection between each
ray and its neighbour on either side from the apophyses to the extreme bases
(Fig. 21, rc).
EVOLUTION OF SIMULIID LARVAL HEADFANS
207
The narrower basal half (tb) of the torma bears heavy external ridges, and at
its base articulates broadly with the stongly sclerotized post-Torma (pt) which is
itself firmly connected to the large plate (mb) covering the dorsal face of the
fan-base. Proximally the post-torma meets the base plate (bp), the “plaque
basale” of Grenier of “basaler Chitinring” of Fortner, which makes broad
qrticulatory connections both with the large plate and with the head capsule
proper, on the dorsal side of the fan-base, well shown by Fortner (1937, fig. 2).
The torma bears at its base two prolongations: first, a deeply situated broad
transparent process (np) with no muscles attached to it, and longer and more
complex in shape in many Simuliini than in P. ferrugineurn and other
Prosimulium species; secondly, a superficial, longitudinally striated cuticular
band (sb) firmly attached to the torma itself and not moveably articulated to
it. This functionally important feature (shown in figures but not labelled by
Fortner and Grenier) bears longitudinal striations due to its being corrugated
throughout its thickness when viewed in sections. It traverses the thin cuticle
connecting the fan-base ventrally to the remainder of the head capsule, and is
slightly widened distally and curved t o run alongside the defined posterior edge
of the lightly sclerotized cuticle of the lateral labral region anterior to the
fan-base (Fig. 21). Adjacent to the expanded distal part of the striated band,
the edge of the labral cuticle is more heavily sclerotized in a darkened zone
without sharply defined anterior edge (se), and is familiar to entomologists who
have examined black-fly larvae as a dark streak on either side of the labrum
when the head is viewed ventrally. Part way along its length the striated band is
connected by an internal tendon-like transparent apodeme (te) to the distal
expanded region of the torma.
At this stage the following comparisons and resultant conclusions can be
made between the structural features of the filtering fan (Fig. 21) and the fan
of Crozetia (Fig. 19):
(1) The long striated band (sb) firmly attached to the base of the main part of
the torma in the filtering fan is clearly homologous with the short striated
cuticle band differentiated from, but clearly part of, the torma in Crozetia
(Figs 19 and 20, sb) in which it forms the connection between the torma
itself and the aterior palatal bar (ap). In Crozetia the latter is a well
developed sclerite with sharply defined edges running anteriorly and
slightly ventrally from the anterior end of the torma proper as shown in
Fig. 19. In the filtering fan the anterior palatal bar seems to be missing.
Instead of the elongate striated band (Fig. 2 1) making connection with an
anterior palatal bar, it runs distally beside a sclerotized area of the edge of
the labral cuticle (se). This sclerotized area may be the reduced or
under-developed palatal bar, but this seems unlikely for two reasons. First
it runs almost transversely instead of anteriorly, and second it is not a
defined sclerite but a sclerotized area without defined anterior edge.
(2) The main part of the torma articulates basally and posteriorly with the
superficial broad sclerite identified as the post-torma in both forms (Figs
19 and 21). But the basal plate of the filtering fan (Fig. 21) interposed
between the head capsule and the main plate (bp) has no counterpart in
Croze tia.
( 3 ) In the filtering fan the expansion of the torma into a distal (dp) and an
2 08
L. DAVIES
accessory plate (cp) together with the existence of associated medial (mf)
and accessory (af) fans (the rays of the latter forming a straight row in
Prosimulzum and a U-shaped series in many Simuliini), all lack counterparts
in Crozetia where the torma, albeit sharply bent, is still rod-like distally,
and where but a single fan-ray series is present.
(4) The main rays in the filtering fan together form a long, deeply-curved
series, in which the extreme bases form a curve with a sweep of about
230". In Crozetia the fan rays have their bases close together forming a
short and very gently curved line (Fig. 19). These differences functionally
dictate the differences in the form of the distal parts of the tormae in the
two types of fan as discussed below.
(5) The sharply curved lightly sclerotized band in Crozetia (Fig. 19,ls) appears
to have no homologue in the filtering fan. However, the plaque-bearing
area on the ventral face of the base in Crozetia (pa) (with its crocodile-skin
appearance) has a counterpart in various Prosimulium species in which
exactly similar plaques are present on the cuticle adjoining the accessory
plate (not shown in Fig. 21 to avoid obscuring other features shown).
Flexing and unjlexing movements of head-fans
Croze tia
Study of slide-mounted heads as well as manipulation of fans in situ on
intact head capsules shows that fan movements during raking are produced as
follows. In the flexing action, contraction of muscle 61 causes partial rotation
of the main part of the torma about its two basal articulations which are
respectively that with the post-torma via the posterior extension of the torma
(Figs 19 and 20, et) with the anterior palatal bar (ap) via the striated cuticle
band. The results of this movement of the torma are as follows. The inner
rod-like part of the torma within the fan base moves laterally, that is towards
the main plate (mb) supporting the ray series, resulting in considerable bending
and distortion of. the mainly transparent cuticle t o which the torma is
connected (fc) and which covers the ventral or inner face of the fan base,
bringing the inner comers (ia) of the rays inwards thus moving the rays and
producing the flexing or raking stroke. This inward bending of the transparent
cuticle results in further bending of the already curved lightly sclerotized band
(Is), as seen on comparing right and left fan bases in Fig. 19. Simultaneously,
the plaque-bearing area (pa) on the ventral face of the fan base is caused to
bulge outwards.
Movements of the above components of the Crozetia fan base are amplified
by comparing Fig. 22 (unflexed) with Fig. 23 (partly flexed position). It is
clear from manipulation of the head-fans that the muscle-induced flexing
action, as outlined above, causes distortions of certain parts resulting in storage
of elastic energy that is largely responsible for the restoration of the fan parts
to the unflexed position. The distorted parts, as displayed in Fig. 19, are the
striated band connecting the torma to the anterior palatal bar, and the
transparent cuticle covering the inner face of the base, with its differentiated
band (Is) and plaque-bearing area (pa). These parts must therefore contain
elastic cuticle, probably of resilin-like properties as in the filtering fan (see
following section).
EVOLUTION OF SIMULIID LARVAL HEADFANS
209
I
dr
Figure 22. Diagrammatic representation of fan of Crozetia in unflexed position.
Figure 23. Diagrammatic representation of fan of Crozetia in partly flexed position (cf.
Fig. 22).
In the living Crozetia larva in still water under the microscope, the fans are
seen to be very rapidly flicked in flexing and unflexing actions, up to 2-3
cycles/sec, often but not always with the front of the head applied to the
substratum. The very rapidity of the fan movements suggests elastic restoration
during unflexing, after the muscle-powered flexing action. In the laboratory
and in situ on rocks in streams on fie de la Possession, larvae were observed
raking the substratum. Making use of the flexibility of the deeply annulated
anterior abdomen, the body can be bent into a tight n shape, so that the head
can reach the stone surface for the whole radius around the point of posterior
attachment, from the two extremes where the head lies adjacent t o the
attachment point, on its left and its right respectively.
Normal Simuliidae
Microscopic observations of manipulated intact filtering fans of various
species together with appropriate stained whole preparations and serial sections
enables the flexing and unflexing actions to be more completely described and
understood than hitherto, particularly the distribution and role of elastic
cuticle components important in fan unflexing. As seen below the movements
of the filtering fan form a very precisely controlled and integrated mechanism,
much more elaborate and elegant than that constituted by the Crozetia fan, but
15
2 10
L. DAVlES
I
te
I
,
,’
sb
I
Figure 24. Diagrammatic representation of base of filtering fan in unflexed position.
Figure 25. Diagrammatic representation of base of filtering fan in partly flexed position (cf.
Fig. 24).
basically similar in essentials. In the following account reference should be
made to Fig. 21 and to the diagrammatic representation of the positions of
parts given in Figs 2 4 (unflexed) and 25 (partly flexed).
In the flexing action, contraction of muscle 61 produces distal depression of
the torma when the fan is viewed on its ventral face, that is to say the tormal
plates move into the plane of the paper in Fig. 21. Also slight elevation is
produced at the extreme base of the torma at its articulation with the
post-torma, as seen by comparing Figs 24 with 25. These movements result in
displacement of other components as follows:
(1) The transparent cuticle connecting the edges of the torma plates transmits
their motion to the apophyses of the main fan rays, resulting in their
flexion as shown in the figures.
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
211
(2) Elevation of the extreme tormal base causes distortion of the striated
cuticle band (sb) producing an observable increase in its curvature so that
the band rises slightly from the thin cuticle surrounding it. This must result
in storage of elastic energy in the band.
( 3 ) Downward motion of the distal plate is accompanied by inward swing of
the accessory plate on its basal hinge. (In order to show this movement, in
Figs 24 and 25 the accessory plate has been shown in broken line as
suspended from the main plate, while in reality it lies in the same plane as
the main plate, normal to the plane of the paper, as shown in Fig. 21.)
Inward swing of the accessory plate causes erection of the medial fan rays
(mf) which thus, as previous workers have noted, are erected as a series
simultaneously with the folding of the main ray series, a remarkable and
ingenious arrangement whose functional significance is unknown.
(4) The accessory fan rays, forming a short linear series in Prosimulium species,
move closer together when the fan flexes, but remain largely erected.
Movement of the corresponding rays in Simuliini is more complex and has
not been fully observed in the present work.
Since there is no muscle responsible for the unflexing of the fan, relaxation
of muscle 6 1 is accompanied by unflexing which, as shown below, is partly a
result of release of forces initially generated by distortion of elastic
components. One such component, the striated cuticle band (Fig. 21), has been
shown above to undergo visible distortion during flexing. Restoration of this
band to its original form on relaxation of muscle 6 1 will lift the distal parts of
the torma to their original position in the unflexed fan. Perhaps the tendon-like
band (tn) connected to the accessory plate, if it is elastic, restores that plate to
the position shown in Fig. 21, but this is uncertain.
Whole preparations and isolated components have been examined in the light
of the work of Weis-Fogh (1960) who first reported the rubber-like protein,
resilin, forming particular elastic components in parts of the wing mechanisms
of flying insects. The striated cuticle band stains differentially to the remainder
of the torma and associated parts when treated with dilute methylene blue in
M/20 buffer, a blue approaching but not identical to sapphire blue being
produced throughout its length, and retained when transferred to dilute buffer
alone. Further, in sections stained by Mallory’s triple method, the band is
differentially stained reddish, showing fuchsinophilic cuticle. Both colour
observations suggest that resilin or a resilin-like protein is an important
component of the striated band. Sections also show clearly that the striated
appearance seen in surface view is not merely due to external ridges but is
caused by the fact that the band is truly corrugated throughout its thickness,
and so built to resist transverse bending.
Restoring the distal plates of the torma to the unflexed position as described
above would not cause movement of the main rays to their original extended
position since the transparent cuticle connected to their apophyses is flexible
and cannot transmit a pushing force from the plates to the rays. Previous
workers have concluded that unflexing of the main fan is solely due to
increased blood-pressure, on the basis of the readily-made observation that
when pressure is applied to the larval body, a flexed fan will promptly unflex.
That the above conclusion is at most only partly true is shown below.
212
L. DAVIES
Details of the form of the basal parts of the main rays must be described in
order to delineate the mechanism whereby they return to the unflexed
position.
As shown in Fig. 24 the basal part of a main ray, from a distance beyond the
apophysis equal to the distance of the latter from the extreme base, is
constructed as follows. The sclerotized distal shaft of the ray continues basally
as a curve (sr) on the inner (ventral) side of the ray to meet the apophysis and
then continues as a thinner but still sclerotized part on the same inner side until
the extreme base is reached. There is thus a curved sclerotized basal portion to
the ray, curved in the reverse direction to the long curve of the distal shaft,
omitted in Fig. 24 where the rays have been truncated. Each complete main ray
is thus a largely straightened out S, the bottom part of the S being formed by
the parts shown in the figure. The inside of this curve is occupied by the
unsclerotized transparent expansion of the ray, the “processus aliforme” of
Grenier (1949). These basal expansions on the main rays, as noted by previous
workers, grade in size from one side of the ray series to the other.
The methylene blue in dilute buffer test, mentioned earlier, produces
differentially a bright blue in this flat expansion, showing that it contains
elastic resilin-like material. It is thus possible to deduce that during flexing of
the fan, the pull transmitted to the apophyses via the transparent cuticle by the
tormal movement described earlier tends to increase the basal curvature of each
main ray which will cause longitudinal compression in the elastic material of
the expansion. Because the expansions lie tightly packed against each other and
individually compressed longitudinally when the fan is fully flexed, as deduced
above, on relaxation of muscle 61 and its concomitant events, the expansions
will tend to push each other apart and move in graded sequence in relation to
each other on release of elastic energy. This means that each ray will then
individually tend to return to the unflexed position, an elegant mechanical
solution to the problem of ensuring precise sequential movements of a long
series (up to 60 main rays or so) through a large angular distance, without
failure of any individual ray movement during the many thousands of fan
flexions that must occur in the life of a fan during a complete larval instar. I t is
a more reliable arrangement mechanically than if the rays as a complete group
was entirely passively pushed back into place solely by straightening of the
folded transparent cuticle caused by blood-pressure increase.
The above mechanism involving storage of elastic energy in each main ray
during flexing and its release during unflexing, does not mean that blood-pressure within the fan base is unimportant. Fan unflexing fairly certainly
depends on maintenance of blood-pressure in the base within a certain range.
The figures show that inevitably there are large differences in the volume of the
fan base between the extreme positions, and explains why mechanical pressure
on the dead larval body causes fan unflexing. But that blood-pressure change
alone (as opposed to absolute blood-pressure) does not fully account for the
mechanism of unflexing is shown by the fact that in the living larva flexing of
one fan while the other is unflexing is frequent; to explain this would involve
postulating opposite pressure changes on the two sides of the head, which seem
unlikely to occur. Furthermore the fact that filtering fans can be observed to
flick at frequencies of at least 2-3 cycleshec suggest that blood-pressure
changes that would take time to be transmitted cannot be the whole
mechanism.
EVOLUTION O F SlMULlID LARVAL HEADFANS
213
Comparison of Crozetia with normal Simuliidae
Comparing the flexing and unflexing mechanism of the filtering fan of
normal Simuliidae with that in the raking fan of Crozetia leads to the following
considerations. Movements of the torma in fan flexing induced by muscle 61
and its return travel powered by release of elastic energy stored during flexing
through distortion of the striated band attached to the base of the torma,
constitute basically similar mechanisms in the two forms. However, the striated
band is short in Crozetia and makes contact with the anterior palatal bar, while
the band is much longer in the filtering fan and does not make contact with
such a bar.
The more distal parts of the torma are very different in the two forms and
the functional requirements dictating the differences can be set out as follows.
In Crozetia the fans rays form a short series lying on a line with only gentle
curvature. Therefore simultaneous movement of all rays can be produced from
a rod-like distal tormal end, aided by the fact that the flexible cuticle
transmitting the movement to the rays is much less flexible than the
corresponding cuticle attached to the apophyses of the rays in the filtering fan.
In the latter on the other hand, the bases of the main rays form a long curve
with a 230” sweep. In order to produce simultaneous controlled flexing of such
a deeply curved series of rays, the distal end of the torma must enter deeply
within this incomplete (230”) circle, and it must also be plate-like so that the
distance from the end of the torma to the apophyses is not too long while
being approximately equal for all rays. There is then a problem constituted by
the fact that in flexing, not only must the horizontal distance be reduced in the
plane of the long axis of the fan base (distance A-A in Fig. 21) but also
reduction of distance B-B (Fig. 21) must be achieved. The problem has been
resolved by having the distal tormal plate divided into two, one (the accessory
plate) being hinged to the other, and reduction in B-B produced by swinging of
the accessory plate until it meets, or even slightly under-rides the edge of the
main plate on complete fan flexion.
A remaining contrast between the two fan types is that the differentiated
resilin-containing region forming the “processus aliforme” near the base of each
main ray of the filtering fan, producing the elastic mechanism partly
responsible for moving the rays during unflexing, has no counterpart in
Crozetia. Here the rays consist of uniformly sclerotized plates of simpler
construction, and which are passively propelled back into position during
unflexing by elastic energy stored in the flexible cuticle of the fan base and its
differentiated parts as already described.
LABRAL REGION IN FIRST INSTAR LARVAE AND THE CONDITION
OF THE ANTERIOR PALATAL BAR IN THEM AND LATER INSTARS
First instar larvae of the species listed below have been studied using
Scanning Electron Microscopy. Larvae were freeze-dried after quenching in
liquid nitrogen: Gymnopais sp. near dichopticus Stone, Twinnia tibblesi Stone
and Jamnback, Prosimulium hirtipes Fries, P. travisi Stone, and C. crozetensis.
Since Craig (1974) has recently published a full anatomical analysis based on
serial sectioning and SEM microscopy, only brief treatment is necessary here;
my results are broadly in agreement with his.
214
L. DAVlES
As Craig has shown, first instar larvae of the above species, except Crozetiu,
bear 1-4 bristles, one or more of which has a flattened shaft and is terminally
pectinate on one side, situated laterally on the labral cuticle close t o the seta
numbered 3-C (Craig, 1974, fig. 34; and Plate 1 in the present paper). These
bristles which are not borne on a differentiated elevated base, are constantly
accompanied by 3 3 campaniform organs (co) and lie close to the insertion of
muscle 61 via the tormal apodeme. Craig terms these bristles the cephalic fan
but I prefer to term them the proto-fan bristles to emphasize the fact that as an
assemblage they d o not constitute a fan either in structure or function. Craig,
however, has convincingly demonstrated that these bristles, with the area of
cuticle with campaniform organs on which they stand, constitute the
homologues of the cephalic fans present in second and later instar Prosimulium
and in all instars of the great majority of other Simuliidae.
Study of SEM photomicrographs suggests that the proto-fan bristles can do
no other in life than form part of the substratum-brushing mechanism
constituted by the anterior palatal brush, composed in these first instar larvae
of bristles remarkably modified into fringed plates (Plate 1). The position and
mounting of the proto-fan bristles precludes any considerable independent
movement of them and their minor functional importance is supported by their
apparent absence in some species of Twinniu and Gymnopais (Craig, 1974).
In the Crozetiu first instar (Plate 2 and Fig. 26) the proto-[an bristles of the
above forms are represented by four true fan-rays borne on a fan-base within
which the torma, now short and knobbed instead of elongate, is situated. In
succeeding instars as shown by Craig (1974: fig. 1 3 ) these rays become more
numerous and broad-based as shown in Fig. 19 of the present work. These fans
in the first instar Crozetiu clearly rake in the substratum as in succeeding
instars, and so largely perform the brushing function done by the palatal brush
in first instar Twinniu and Gymnopais, since this brush as an assemblage of
bristles is relatively weakly developed in the Crozetia first instar (Fig. 26).
The elegant micro-anatomical work of Craig has shown that the homologue
of the complete torma of other nematocerous larvae, in the first instars of the
Simuliid genera listed above (p. 21 3), shows division into two parts, namely a
more posterior part to which the term torma is applied, and a more anterior
part that extends antero-ventrally termed the anterior palatal bar. This
terminology of Craig is followed here and seems appropriate in the light of the
terms used by workers on other nematocerous larvae (Knight & Laffoon, 1971;
Anthon, 1943a, b). (Cook, 1944, 1949), however, empldys different terms since
he considers the palatum to be a quite different part of the labral region.)
The present study of the head-fans of later instar Crozetiu larvae shows that
the anterior palatal bar is present and massively developed (Fig. 19), in
agreement with Craig’s (1974: fig. 1 5 ) findings. There is no doubt that this
sclerite in later instar Crozetiu larvae can be reliably identified as the
homologous equivalent of the anterior palatal bar of first instar Prosimulium,
Twinniu and Gymnopais. In Crozetiu later instars the torma makes connection
with the anterior palatal bar through the small striated cuticle band (Figs 19
and 20, sb), the latter being clearly a differentiated part of the torma itself to
which it is firmly soldered and not articulated. The articulatory movement
when the torma rotates on fan flexing is solely between the striated band and
the anterior palatal bar (Fig. 19, ap). The striated band is much longer in
EVOLUTION OF SIMULIID LARVAL HEAD-FANS
215
10 prn
Figure 26. Dorsal view of labral region of first instar larva of Crozeriu. In this specimen only
three fan-rays could with certainty be detected. The wide nature of the rays is shown in the left
fan (cf. Plate 2A). The knobbed torma within each fan base, the apodeme of muscle 61 and the
tip of the right mandible, are shown.
Prosimulium post-first instars (Fig. 21, sb) but it is clearly an enlargement of,
and homologous with, the small striated band in Crozetia late instars. Detailed
study of the head-fan bases of various middle and late instars of Prosimulium
and many Simuliini in the present work shows, contrary to Craig’s findings,
that the anterior palatal bar is absent. Craig stated that in Prosimulium this bar,
present in the first instar, is not fully re-expressed until late instars, and that in
Cnephia, Metacnephia and Simulium is only re-expressed in later instars, and
furthermore that in these instances the re-expressed anterior palatal bar is not
in the plesiomorphic condition. Examination of Craig’s figs 11 and 17 for P.
susunae shows, particularly in the latter figure, that the striated cuticle band is
apparently mistaken for the anterior palatal bar. The form of the supposed bar
in his fig. 17 corresponds exactly t o its appearance in slide mounts of last instar
Prosimulium spp., where it is frequently relatively sclerotized despite its
bending functions, and where if pressure is applied in slide-making the curve in
the band in my Fig. 21 becomes accentuated to the sharper bend shown in
Craig’s fig. 17.
The striated band of late instar Prosimulium and all normal Simuliidae thus
cannot be the reexpressed anterior palatal bar as concluded by Craig, since in
all Crozetia post-first instars the anterior palatal bar and the striated band (the
latter albeit small) are both simultaneously present. The striated band of late
instar Prosimulium and all normal Simuliidae has been shown in this paper to
be a development of, and homologous with, the striated band in Crozetiu,
where it is a part of the torma which is clearly separated from the anterior
palatal bar as is the torma in first instar Crozetia, Gymnopais, Twinnia and
Prosimulium. The conclusion is reached therefore that the anterior palatal bar
216
L. DAVIES
is lost in all Simuliid larvae with filtering head-fans; also that the bar is fully
retained in all instars in Crozetia in agreement with Craig's findings.
BIOLOGY OF CROZETIA ON ~ L EDE LA POSSESSION, ims CROZET
The following observations were made from January-April 1968 and from
December 1972-April 1973. An outline of the relatively warm sub-Antarctic
climatic conditions and habitats available for the depauperate terrestrial
arthropod fauna is given elsewhere (Davies, 1973). The constantly cool windy
climate with heavy precipitation leads to abundant run-off ranging from small
trickles and peat runnels, to many tumbling streams and one 20 m wide 8 km
long stony river (Rivikre Moby Dick). Outside the microscopic interstitial
fauna, the macroscopic stream fauna of the island is extraordinarily simple,
consisting in full of two species of Turbellaria, larvae and pupae of one
Podonomid midge and the stages of Crozetia. In both seasons Crozetia vastly
predominated in numbers and biomass over the remaining animals in all
watercourses from sea-level upwards, and were numerous even in spring-fed
trickles at 800 m altitude. When observations started (early January 1968,
mid-December 1972) larvae of all post-second instars were present and a few
pupae, and by late January 1968 and 1973, large larvae and pupae were
numerous, and adult emergence in progress. In both years pupae remained
abundant throughout February, while large larvae became scarce and by April
pupae and final instar larvae could not be found, and small and medium sized
larvae were abundant. To give an idea of numbers it may be noted that single
stones of about 30 cm length yielded the following: 1 5 January 1968, 88
pupae, 52 last instar and c. 300 other instars ranging down to probable second
instars; and on 25 February 1968, 1 5 pupae, 8 last instars and c.300 other
instars.
In both seasons the picture obtained was one of extended and unsynchronized pupation from about mid-December (mid-summer) t o early
March (early southern autumn), with larvae hatching from eggs over approximately the same period and growing slowly until a year later, probably with
some retardation but not cessation in winter since winter monthly mean screen
temperatures (2"-4" C) are not much lower than those in summer months
(5" -8"C). Stream temperatures measured during the summer work ranged from
4"-7' C on normal cloudy days to 10.5" in a small stream on a cloudless sunny
day. In winter the streams are probably at 0.5"-5" C with intermittent icecover
depending on altitude and short-term weather conditions. Stream temperature
conditions on ile de la Possession therefore seem to be broadly similar t o those
in streams in hill areas in northern and western Britain.
During January to February in both years while considerable emergence was
in progress, male flies were observed in flight up to 2 m above streams on days
when wind-speeds were low enough to permit flight. These males were making
short flights, mainly along the streams, frequently alighting on boulders on
which they crawled to and fro down to the water-line and often attempting to
copulate with other males. Single females that appeared from their incomplete
darkening to be freshly emerged, were repeatedly observed to alight on such
boulders and they immediately mated with one of the males, which constantly
outnumbered females by a factor of 10 or more.
EVOLUTION OF SIMULllD LARVAL HEADFANS
217
During the same period moderate numbers of females (1-3 per 5 minutes of
effort) were swept with a net from stream-side grassy vegetation, and also
aspirated from beneath nearby boulders. These females were dissected and their
ovaries and spermathecae examined. The latter invariably contained sperm, and
the ovaries contained developing oocytes from early stages (I) to approaching
maturity (Stage IV of Wanson & Lebied, 1948). The females seemed to be
disinclined to make flights even on calm days, since they could be swept from
vegetation when net-sweeps at 1-2 m above the low tussocky grassland yielded
only males. Net-sweeping of vegetation away from streams yielded no Crozetia
adults.
No Crozetiu egg-masses were found on or near the water-line of stream
boulders, nor on trailing vegetation in small peat streams, despite considerable
searching on many days. The eggs of Simuliidae that alight on the substratum
to lay egg masses are (from experience in British hill-streams) easily found; it is
concluded that Crozetia females either drop their eggs while in flight, or lay
them singly or in small groups while repeatedly dipping the abdominal tip in
the water as in many Prosimulium spp. (Davies & Peterson, 1956). Actual
oviposition by Crozetia females was, however, not observed, probably because
in larger streams there were always so many males present flitting from boulder
to boulder, that detection of a small number of females ovipositing at any one
time became difficult. Single eggs and first instar larvae were, however, found
on two occasions scattered along trailing grass in small peat streams, and this is
consistent with oviposition by either of the two methods mentioned.
The above observations, together with the fact that the mouth-parts are
weakly sclerotized, show that Crozetia females are autogenous and non-biting,
that mating takes place on stones in streams, and that adults remain close to
streams. Flight activity therefore is limited and nondispersive, and considerable
time is spent by males crawling about on stones and by females in quiescence
among stream-side vegetation and stones. In adult biology therefore Crozetia
constitutes a close parallel in a sub-Antarctic context, to the non-biting ground
mating Simuliidae of the sub-Arctic (Downes, 1962). These biological features
in Crozetiu have doubtless evolved independently from those in the northern
species in response to similar environmental conditions in higher latitudes in
the two hemispheres.
Three other biological features of Crozetia deserve mention. The first
concerns the site of pupation. Many of the stones and boulders in h e de la
Possession streams bear deep tubular holes, arising probably from gas escape
when rock formations were in a viscid condition during the volcanic periods
that gave rise to the island in Miocene and later times. Most larvae pupate
within such holes and for this reason are difficult to remove from stones
without damage. Although the cocoons are very small and hardly cover more
than the posterior quarter of the abdomen, the silk is tough, and because of the
long abdominal spines and numerous hooks present on the last two segments
even those pupae on exposed surfaces are usually damaged on removal (so that
not more than 10%produce adults when kept in containers on moist filter
paper in the standard way of rearing black-fly adults).
The second feature concerns the unusually large size-range in mature larvae,
pupae and adults noted in the descriptions of these stages. Undoubted last
instar larvae, as shown by possession of black pupal filament histoblasts,
218
L. DAVIES
occurred whose body length and capsule size were extremely variable. Smaller
such individuals had wider posterior portions to their cephalic apotomes, over
one-third the width of the posterior end of the head capsule, while large
individuals had much narrower posterior apotomes as shown in Fig. 4.
Measurement of head capsule widths of over 600 larvae of all sizes showed a
complete gradation of sizes without any identifiable peaks in the frequency of
any size-group. These facts suggest tentatively that in Crozetia the number of
instars undergone during larval development is variable in different individuals,
and that this leads to the large size-range in pupae and adults. Adults of both
sexes were equally variable in size. At one stage I thought that two species were
present, but measurements showed no bimodality in adult size-distribution, nor
were any structural differences found between smaller and larger adults.
The third feature concerns the apparent absence in this species of the larval
parasites common in continental Simuliidae. Neither Microsporidia nor
mermithids were found in several hundred larvae collected.
DISCUSSION
The facts presented in this paper on the structural features of the head-fans
and their functioning in flexing and unflexing in Crozetiu on the one hand, and
in filtering fans of normal Simuliid larvae on the other, seem to me to confirm
the view put forward previously (Davies, 1965) that the raking Crozetia fan
represents an evolutionary stage antecedent to the filtering fan. The very
complexity and perfection of the filtering fan make it difficult to envisage how
it could evolve directly for this function without an antecedent stage when it
was a raking organ. The Crozetia fan fulfils the role of an intermediate and
therefore plesiomorphic fan admirably and shows by its structure that the
raking function requires an organ of considerable complexity but nevertheless
very appreciably simpler in anatomy and mechanics than the filtering fan.
Further arguments in support of this interpretation of the significance of the
state of the Crozetiu fan, and therefore for rejecting the view put forward by
Craig (1974)that this fan is apomorphically reduced, are presented later. But
two interrelated problems raised by my interpretation, firstly when the
Simuliidae are considered as a whole, and secondly when the family is viewed
in the light of the larval head anatomy of related families of Nematocera
Culiciformia, must be considered.
In view of the considerable uniformity (apart from one or two species
discussed later) in the structure of the filtering fan throughout the family I
think it unlikely that the filtering fan independently evolved more than once in
Simuliidae. If this is accepted, there arises the problem that if the raking fan in
Crozetiu is plesiomorphic in relation to the filtering fan of post-first instar
Prosimulium, how is it that the adults of the two genera present character
assemblages where the above relations are reversed, that is those of adult
Prosimulium plesiomorphic relative to those of Crozetia?
This question can be resolved if it is admitted that the agreed apomorphic
states of certain pupal and adult characters in adult Crozetiu and some other
Prosimuliini (Procnephiu Crosskey, Cnephiu sensu lato), and universal in
Simuliini, have evolved more than once from the supposed plesiomorphic state
seen today in Prosimulium sensu strict0 and in Twinniu. These apomorphic
EVOLUTION OF SIMULlID LARVAL HEAD-FANS
219
states are, in adults, spiniform macrotrichia additional to hair-like ones on C
and Rs, various types of shortened female gonapophyses instead of elongate
leaf-like ones, and in pupae reduction of or development of regular shaped
cocoons instead of large shapeless ones, and the reduction, loss or modification
of the two long terminal abdominal spines and of other elements of the
chaetotaxy in pupae. The very variety in form of the gonapophyses and pupal
characters suggess their multiple individual origins from a plesiomorphic
condition, while the loss of an Rs branch was demonstrated by Edwards
(193 1) to be a double independent apomorphism relative to the two-branched
condition, in that in some forms it is R2 + 3 that is lost, in others R4 + 5 . !
suggest that also the appearance of spiniform macrotrichia on C and R also
evolved more than once.
If the above is accepted, it would be expected that larvae, pupae and adults
of single genera or subgenera would display disharmonic assemblages of
apomorphic and plesiomorphic characters as is postulated here for Crozetia,
namely the larval fans being plesiomorphic, while certain pupal and adult
characters are in an apomorphic condition. The sequence of evolutionary
events in Simuliidae I would envisage to have occurred as follows:
( 1 ) The unique evolution of filtering head-fans from raking fans within a
widely distributed taxon of possibly generic rank whose adults had the
Prosimulium sensu strict0 assemblage of characters or their equivalent at
that time. This evolutionary step is supposed to have taken place in one
area while contemporaneous congeneric species retained raking fans over
the remainder of continental areas.
(2) Species with raking fans and others with filtering fans, orginally with
similar pupal and adult as well as larval characters, would radiate and
diverge, some being conservative, others acquiring apomorphic characters
in all stages in both raking and filtering larval types.
( 3 ) The presumed and probable competitive superiority of filtering over raking
forms would lead broadly t o forms with filtering larvae supplanting those
with raking larvae. Before this displacement reached its resent state of
completeness on all continental areas, it is supposed that les Crozet were
colonized by long distance dispersal, sometime since Miocene times,
possibly from South America, b y a form with raking larvae but more
apomorphic adults which has remained substantially unchanged
morphologically but not biologically since its arrival.
F
If lack of synchronization in geological time of larval, pupal and adult
evolutionary changes, the multiple origin of various apomorphic character
states leading to parallel and convergent evolution particularly in adults,
coupled with the survival in certain places of rare products of these processes, is
accepted as likely, then various possibilities including the above interpretation
for the origin of Crozetia must be considered or at least not rejected without
further study. These possibilities include the moderately plesiomorphic and not
apomorphic state of the peculiar head-fans in Simuliurn (Phoretomyiu) copleyi
(Gibbins) and the concomitant view that the resemblance of adults of this
species t o certain others placed in this subgenus by Crosskey (1969) is an
extreme case of convergence. Another case is Simulium oviceps Edwards whose
larvae possess small filtering head-fans, and which if my view is correct (Davies,
220
L. DAVIES
1965) possess adults whose characters have independently come to resemble
the widespread Holarctic, Ethiopian, Oriental and Australasian subgenus
Eusimulium.
The interpretation of the Crozetia raking fan as essentially plesiomorphic
relative to the filtering fan, with raking as ancestral to filtering in Simuliid
larvae, elaborated in this paper, must be placed in relation to the condition of
the labral region in other Culiciform larvae. Craig (1974) has greatly clarified
the position of Simuliidae relative to Chironomidae by the fact that he has
identified, correctly in my view, the vestigial messors in Gymnopais and
Twinnia larvae. I t seems clear that the head-fans, and their homologues in
certain first instar larvae (the proto-fan bristles) are quite separate in origin
from the messors in the refined sense of Chaudonneret (1963) and that
therefore Simuliidae are not necessarily evolutionarily close to Chironomidae,
contrary to my previous view (Davies, 1960, 1965).
Identification of head-fan homologues in the first instar Prosimulium sensu
stricto, Twinnia and Gyrnnopais by Craig and confirmed in the present work,
removes difficulty in placing elements of the labral complex of Simuliidae into
conformity with those of Culicidae and Dixidae. My interpretation therefore is
that the development of complex homologous lateral labral organs involving
the tormae, from simple original components has proceeded in two directions
in Simuliidae, one of which parallels the direction undergone in Culicidae and
Dixidae. Thus in Simuliidae, the proto-fan bristles, the simple lateral labral
organs, evolved in one direction towards obsolescence and loss in all post-first
instar Twinnia and Gymnopais and, in the other direction, initially into
complex raking organs as seen in Crozetia supplementing the median palatal
brush used exclusively by the two first-named genera, and secondarily into even
more complex filtering organs in the majority of remaining Simuliidae. The
homologous lateral labral organs in Culicidae and Dixidae have in parallel to
Simuliidae developed into complex structures moved in one direction by
homologues of muscle 61 and depending on elastic mechanisms for return
movements (Christophers, 1960; Cook, 1949).
The comparative anatomical evidence presented in this paper comes nearest
to definite disproof of the interpretation of the Crozetia fan as secondarily
reduced from the filtering condition in the finding, invoking the principle of
irreversibility of evolution, that the anterior palatal bar is lost in all filtering fan
forms, and fully retained in Crozetia. Two further considerations support the
views elaborated in this paper on the significance of the latter form, and are
given below.
The first is that there is no known ecological circumstance for supposing that
a form with filtering larvae, with all that that implies in terms of the precise fan
machinery and presumed energetically economical feeding method available to
it, should be subject to selection pressure to abandon this feeding method and
modify its fans for the cruder and probably energetically more expensive raking
method. The food sources exploited by filtering, namely unicellular algae and
bacteria, have occurred and flourished at a wide range of temperatures and at
all times in streams and on the soil and rock surfaces from which they draw
their run-off. In any case, various authors have shown (not only by direct
observation but also by examination of gut contents of numbers of normally
developing individuals) that larvae with complete filtering fans can readily
EVOLUTION OF SlMULllD LARVAL HEAD-FANS
22 1
support themselves by scraping the substratum in streams where suspended
matter is known to be scarce (Peterson, 1956; Serra-Tosio, 1967; Davies,
unpubl. obs.).
The second fact concerns the geological history of iles Crozet. Prior to my
work on ile de la Possession I supposed that the island had been entirely
ice-covered during one or other of the Quaternary glaciations (Davies, 1965).
Since then familiarity with its topography shows that it has never been
extensively glaciated, but probably had corrie glaciers of limited extent on the
higher parts during the coldest periods. This conclusion is confirmed by
consultation with Dr J. P. Bloch, geologist and chief scientist of Terres
Australes et Antarctiques Franqaises, who also reports dating (by the K-Ar
method) of the oldest volcanic formations of Crozet as Miocene. Since that
time therefore, the island has probably been continuously suitable for Crozetiu
to exist there, with only moderate cooling of perhaps 2' -3" C below its present
mean temperatures during Quaternary glaciations. The Miocene age of h e de la
Possession extends back the period within which Crozetiu could have arrived,
possibly from South America, and thus extends the possibility that this took
place at a time when the continents contained a greater number of more
archaic Simuliidae than they do at present.
Two matters concerning the Simuliidae as a whole and their relationships
with other Culiciformia are raised by the results and conclusions of this paper,
They are:
(1) The lack of synchronization of past evolutionary change in larvae, pupae
and adults, and the multiple origins of various pupal and adult characterstates in particular, leading to marked convergences, is a conclusion already
realized by many and unlikely to be rejected by any student of the family.
The condition in Crozetiu emphasizes this state of affairs. It therefore
would appear unlikely that at present we can construct a classification
making a clearcut tribal division of the subfamily Simuliinae into
Prosimuliini and Simuliini, because these are horizontal divisions confounded by the disharmonic suites of characters possessed by certain
forms. This conclusion supports that of Wygodzinsky & Coscaron (1973)
resulting from their extensive and detailed work on Neotropical Simuliidae
where both tribes are heavily and complexly represented.
(2) The apparent happy accident that Crozetiu has survived and thus yielded
valuable information on evolution in Simuliidae emphasizes again the great
desirability that the unknown larva of Purmimulium furcuturn Malloch be
discovered and minutely described. This insect, known only in the adult
stage and so disjunct as t o justify a subfamily of its own, can reasonably be
expected to yield not only radically important information on the
Simuliidae but also on the relationships of the family to the whole of the
remainder of Culiciformia. It is to be hoped that entomologists working in
western North America, an area with an appreciable density of workers,
will assiduously search for an aquatic larva that may not at first sight be
clearly a black-fly larva.
SUMMARY
The larva, adults and the previously undescribed pupa of Crozetia crozentensis (Womersley) from ile de la Possession, iles Crozet, French sub-Antarctic
222
L. DAVIES
Territories, are described. No clear identification of the affinities of this
monotypic genus is obtained, mainly because the larva and pupa are
structurally so disjunct from ail other Simuliidae.
Study of the larval head-fans that are used to rake the substratum, compared
with the filtering head-fans of normal Simuliidae, shows that the former are
much simpler than the latter although basically similar in design and in the
importance of elastic forces in powering the unflexing of the fan after the
muscle-powered flexion. In the filtering fan elastic energy is stored by
deformation of components containing resilin-like material. I t is suggested that
the fan of Crozetia represents a form with raking functions that evolutionarily
preceded filtering fans in Simuliidae.
Results of an SEM study of the labral region of first instar larvae of certain
Simuliidae is consistent with the above interpretation. A group of bristles of
the lateral labral region of these first instar larvae are the homologues of the
cephalic fans, and are postulated to have evolved in two directions, one
involving loss, seen in the head-fan-less post-first instars of the northern genera
Twinnia and Gymnopais, the other into raking organs, as seen in Crozetia, and
later into filtering organs seen in remaining Simuliidae. For the features of a11
stages of existing Simuliidae to be consistent with this view, it is necessary to
postulate that certain evolutionary changes in pupae and adults were not
always synchronized with larval changes and that many adult features of more
advanced Simuliidae evolved more than once in the family.
Field work on he de la Possession showed that C. crozetensis adults emerge
over two to three months, with aquatic stages present in all types of water
courses. Males perform short flights over streams, alighting on stones projecting
from the water where they crawl and mate with freshly emerged females. These
are non-biting and rest near streams while their ovaries mature.
ACKNOWLEDGEMENTS
This work has depended on help and kindness given by many people and
organizations and I express sincere thanks to the following: Monsieur Pierre
Rolland, then Administrateur Superieur of Terres Australes et Antarctiques
Franqaises for permitting both visits to iles Crozet and providing sea transport
and hospitality; Dr J . P. Bloch, Chef des Laboratoires Scientifiques, for much
aid and helpful discussion; Commandant Bilhaut and crews of the supply ships
Gallieni and Marion Dufresne for making me welcome during four voyages;
Capitaines Lemoine and Laloix and helicopter crews, Armke de I’Air de la
France, for many flights over iles Crozet; Messieurs Claude Dousset and Alain
Duret, respectively Chef de District de Crozet during my two visits, for
unfailing courtesy and hospitality; Drs Jacques PCnnaneac’h and Michel France,
medical officers at Crozet for unstinting provision of laboratory facilities; the
Royal Society, Trans-Antarctic Assoc. and Sabbatical Leave Fund of Durham
University for financial help towards costs; Dr Brian Roberts, C.M.G. (Scott
Polar Research Institute and Polar Regions Section of the Foreign Office) for
his help, interest and knowledge on all sub-Antarctic matters; Dr D. A. Craig,
Department of Entomology, University of Alberta, for allowing me to see his
paper in manuscript t o the great benefit of the present paper and for the gift of
EVOLUTION O F SIMULIID LARVAL HEAD-FANS
223
invaluable black-fly material; Dr Roger W. Crosskey (Br. Mus. N.H.) for
facilitating examination of material in his care; to Miss K. Flower, Mr Derek M.
Roberts and Mr J. Richardson for technical assistance and t o the latter for
drawing Figs 3, 5 , 22-25; and finally t o my wife Alice for typing many drafts
and for ably coping with all family responsibilities during my prolonged
absences.
REFERENCES
ANTHON, H.. 1943a. Der Kopfbau der Larven einiger nematoceren Dipterenfamilien. Spolia tool. Mus.
haun.. 3: 1-61.
ANTHON. H., 1943b. Zum Kopfbau der primitivsten bisher bekannten Dipterenlarve: Olbiogaster sp.
(Rhyphidae). Ein Beitrag zur Phylogenie der nematoceren Dipteren. Ent. Meddr., 23: 303-20.
CHANCE, M. M., 1970. The functional morphology of the mouthparts of blackfly larvae (Diptera:
Simuliidae). Quaest. Ent., 6: 245-84.
CHAUDONNERET, J., 1963. Le problkme des ‘messores’ des l a n e s de DiptPres n6matocPres e t la
musculature labrale des insectes. Bull. SOC.
tool. Fr., 88: 369-78.
CHRISTOPHERS, S. R., 1960. A i d e s aegypti (L). The yellow fever mosquito, 721 pp. Cambridge.
COOK, E. F., 1944. The morphology of the larval heads of certain Culicidae (Diptera). Microenromology,
9: 38-68.
COOK, E. F., 1949. The evolution of the head in the larvae of t h e Diptera. Microentomology, 14: 1-57.
CRAIG, D. A., 1974. The labrum and cephalic fans of larval Simuliidae (Diptera: Nematocera). Can. J.
ZoOl. 52: 13 3-59.
CROSSKEY, R. W., 1969. A reclassification of the Simuliidae (Diptera) of Africa and its islands. Bull. Br.
Mus. nut. Hist. (Ent.), 14: 4-195.
DAVIES, D. M. & PETERSON, B. V., 1956. Observations on the mating, feeding, ovarian development
and oviposition of adult blackflies (Simuliidae, Diptera). Can. J. Zool.. 34: 615-55.
DAVIES, L., 1960. The first-instar larva of a species of Prosirnulium (Diptera: Simuliidae). Can. Ent., 92:
81 -4.
DAVIES, L., 1965. The structure of certain atypical Simuliidae (Diptera) in relation t o evolution within
the family, and the erection of a new genus for the Crozet Island black-fly. Proc. Linn. SOC. Lond.,
1 7 6 : 159-80.
DAYIES, L., 1973. Observations o n the distribution of surface-living land arthropods o n the Subantarctic
Ile de la Possession, iles Crozet. J. nu?. Hist., 7: 241-53.
DOWNES, J. A., 1962. What is an arctic insect? Can. Ent., 94: 143-62.
DUMBLETON, L. J., 1962. Aberrant head-structure in larval Simuliidae (Diptera). Pucif Insects, 4:
77-86.
EDWARDS, F. W., 1931. Simuliidae. In Diptera of Pafugoniu and South Chile, Part 11: 121-54. London:
Br. Mus. (Nat. Hist.).
FORTNER, G., 1937. Zur Emahrungsfrage der Simulium-larve. Z. Morph. iikol. Tiere. 32: 360-83.
GRENIER, P., 1949. Contribution
I’Ctude biologique des simuliides de France. Physiologia cornp.
Oecol., 1 : 168-325.
KNIGHT, K. L. & LAFFOON, J. L., 1971. A mosquito taxonomic glossary. VIII. Larval chaetotaxy.
Mosquito Syst. Newsletter, 3: 160-94.
MATSUDA, R., 1965. Morphology and evolution of the insect head. Mem. A m . ent. Ins?., 4: 1-334.
PETERSON, B. V., 1956. Observations o n the biology of Utah blackflies (Diptera: Simuliidae). Can. Ent.,
88: 496-507.
SEGUY. E., 1940. Section DiptPres. In Jeannel, R.. Croisike du Bougainuille aux lles Australes
Francaises. Mkm. Mus natn. Hist. nut. Paris (N.S.), 14: 203-68.
SERRA-TOSIO, B., 1967. La prise d e nourriture chez la larve de Prosimulium inflaturn Davies 1957
(Diptera, Simuliidae). Trav. Lab. Hydrobiol. Piscic. Univ. Grenoble, 57-8: 97-103.
WANSON, M. & LEBIED, B., 1948. Note sur le cycle gonotrophique de Simulium damnosum. Revue
2001.Bot. afr., 41: 66-82.
WEIS-FOGH, T., 1960. A rubber-like protein in insect cuticle. J. exp. Blol., 37: 889-906.
WOMERSLEY, H., 1937. Diptera. Rep. Brit. Aust. N.Z. Antarctic Res. Exp. 1929-31 (Series Bj. 4: 57-79.
57-79.
WYGODZINSKY, P. & COSCARON, S., 1973. A review of the Mesoamerican and South American black
flies of the Tribe Prosimuliini (Simuliinae, Simuliidae). Bull. A m . Mus nut. Hist., I51 (2): 131-99.
224
L. DAVIES
ABBREVIATIONS USED IN PLATES AND FIGURES
af
am
aP
as
ar
bc
bP
bs
co
Cp
dP
dr
eP
f
fc
fr
et
ia
it
hP
IS
mb
mf
accessory fan ray
apodeme of muscle 61
anterior palatal bar
apophysis
ray near anterior end of main series
basal corner of ray
base plate
basiconic sensilla
campaniform organs
accessory plate of t o m a
distal plate of torma
distal rod-like part of torma
knob-like extension of anterior palatal bar
fringed plates forming anterior palatal
brush
flexible cuticle
fan rays
posterior tormal extension
internal angle of ray
intertorma
hinge between accessory and main distal
tormd plates
lightly sclerotized band
main supporting sclerite of fan base
medial fan rays
“P
Pa
Pb
Pf
P‘
Pt
ra
rc
sb
se
sr
ta
tb
te
ti
tn
tT
2-c,
3-c
deep transparent process of base of torma
plaque bearing area of cuticle
median palatal brush
proto-fan bristles
elastic area of processus aliforme
post-torma
rod of accessory plate
thin cuticle connecting adjacent main
fan rays
striated cuticle band
sclerotized area of edge of labral cuticle
sclerotized inner part of base of main ray
thickened edge of accessory plate
slender basal part of torma
tendon-like apodeme connecting striated
band with torma
teeth on end of descending rod of
intenorma
tendon-iike structure connecting accessory
to main tormal plate
transverse rod supporting median part of
labrum
identified setae used as land marks
EXPLANATION OF PLATES
PLATE 1
A. Dorsal view of labral region of first instar larva of Prosimulium sp. indet. ( x 1920).
B. Dorso-lateral view of part of labral region of first instar larva of Gymnopais sp. near
dichopticus ( x 1900).
PLATE 2
A. Dorsal view of labral region of first instar larva of C. crozefensis (x 2400). B. Corresponding
view of second instar larva of C.croretensis (x 1 1 5 0 ) .
Zoo1.J. Linn. SOC.,55 (1974)
L. DAVIES
Plate 1
(Facing p . 224)
Zool. J. Linn. SOC.,
55 (1974)
L. DAVIES
Plate 2