Larval morphology of the lesser housefly, Fannia canicularis

Abstract

The morphology of all larval instars of Fannia canicularis (Linnaeus) (Diptera: Fanniidae) is documented using a combination of light and scanning electron microscopy. The following structures are documented for all instars: antennal complex; maxillary palpus; facial mask; cephaloskeleton; ventral organ; anterior spiracle; Keilin's organ; posterior spiracle; fleshy processes, and anal pad. Structures reported for the first time for all instars include: two pairs of lateral prominences on the prothoracic segment; additional ventrolateral prominences on the second thoracic segment, and a papilla at the base of the posterior spiracle. Other structures reported for the first time are anterior spiracles in the first instar and a serrated tip on the mouthhook in the second instar. A trichoid sensillum on the posterior spiracular plate, representing a sensory organ otherwise unknown in the Calyptratae, is described in the second and third instars. Results are discussed and compared with existing knowledge on dipteran larval morphology.

Full text

Medical and Veterinary Entomology (2012) 26, 70– 82 doi: 10.1111/j.1365-2915.2011.00968.x
Larval morphology of the lesser housefly, Fannia
canicularis
A. G R Z Y W A C Z1,T.PAPE
2and K. S Z P I L A1
1Department of Animal Ecology, Institute of Ecology and Environmental Protection, Nicolaus Copernicus University, Toru´
n,
Poland and 2Department of Entomology, Natural History Museum of Denmark, Copenhagen, Denmark
Abstract. The morphology of all larval instars of Fannia canicularis (Linnaeus)
(Diptera: Fanniidae) is documented using a combination of light and scanning
electron microscopy. The following structures are documented for all instars: antennal
complex; maxillary palpus; facial mask; cephaloskeleton; ventral organ; anterior
spiracle; Keilin’s organ; posterior spiracle; fleshy processes, and anal pad. Structures
reported for the first time for all instars include: two pairs of lateral prominences on
the prothoracic segment; additional ventrolateral prominences on the second thoracic
segment, and a papilla at the base of the posterior spiracle. Other structures reported
for the first time are anterior spiracles in the first instar and a serrated tip on the
mouthhook in the second instar. A trichoid sensillum on the posterior spiracular plate,
representing a sensory organ otherwise unknown in the Calyptratae, is described in the
second and third instars. Results are discussed and compared with existing knowledge
on dipteran larval morphology.
Key words. Fannia canicularis, larval instars, light microscopy, morphology,
scanning electron microscopy.
Introduction
The Fanniidae represent a small dipteran family with world-
wide distribution, the highest diversity of which is found in the
Holarctic region (Carvalho et al., 2003). To date, about 285
species within the four genera of Fannia Robineau-Desvoidy,
Euryomma Stein, Piezura Rondani and the Australian endemic
Australofannia Pont have been described. Domínguez & Roig-
Ju˜
nent (2008) recently argued for the existence of a fifth, unde-
scribed genus, endemic to New Zealand. For several decades
the Fanniidae were classified as a subfamily within the Musci-
dae (e.g. Hennig, 1952; Chillcott, 1961, 1965; Ishijima, 1967;
Huckett & Vockeroth, 1987) and this description can still be
seen in the applied literature, especially in textbooks (Moon,
2002; Robinson, 2005; Byrd & Castner, 2009). Based on
unique features of larval morphology, Roback (1951) raised
the Fanniidae (from Fanniinae) to family rank in a move that
has gained wide acceptance among more recent specialists
(e.g. Pont, 1977, 2000; Rozkoˇ
sn´
yet al., 1997; Carvalho et al.,
Correspondence: Andrzej Grzywacz, Department of Animal Ecology, Institute of Ecology and Environmental Protection, Nicolaus Copernicus
University, Gagarina 9, 87-100 Toru´
n, Poland. Tel.: +48 56 611 4469; Fax: +48 56 611 4443; E-mail: hydrotaea@gmail.com
2003; Moores & Savage, 2005; Domínguez & Roig-Ju˜
nent,
2008). The Fanniidae’s status as a family is fully supported
by recent molecular phylogenetic analyses (Kutty et al., 2008,
2010). McAlpine (1989) listed the following larval features
as Fanniidae autapomorphies: a flattened body with usually
branched fleshy processes, and posterior spiracles on raised
processes. The form and arrangement of the fleshy processes
characteristic of the Fanniidae are useful for species identifi-
cation (Lyneborg, 1970; Duˇ
sek, 1971; Rozkoˇ
sn´
yet al., 1997).
Fannia canicularis (Linnaeus), known as the lesser (or little)
housefly, is a eusynanthropic, cosmopolitan species (Rozkoˇ
sn´
y
et al., 1997; Bisby et al., 2009). It is common in the temperate
regions of the world and less common in or even absent from
tropical regions (Pont, 1977). Larvae of this species are associ-
ated with decomposing organic matter such as dung and rotting
vegetables and fruits, but the species has also been bred in dead
fungi, rotting wood, nests of insects (bumblebees, hornets, yel-
low jackets), nests and lairs of birds and mammals, decaying
seaweed, and carcasses of insects, molluscs and vertebrates
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Fannia larval morphology 71
(Ferrar, 1987; Rozkoˇ
sn´
yet al., 1997). Of all species of Fanni-
idae, F. canicularis is most often involved in cases of myiasis
(Zumpt, 1965; Ferrar, 1987). Larvae (Nuorteva et al., 1967;
Benecke & Lessig, 2001; Benecke et al., 2004; Grassberger &
Frank, 2004) and puparia (Vanin et al., 2007) of F. canicularis
have been found on corpses during crime scene investiga-
tions and on animal carcasses used as models for decomposing
human bodies. In such experiments larvae were even able to
colonize buried bodies in favourable conditions (VanLaerhoven
& Anderson, 1999).
Descriptions of the morphology of F. canicularis lar-
vae have been published by several authors. Tao (1927)
described the first and second instars without providing any
figures. Descriptions of the third instar with line draw-
ings or photographs were provided by Hewitt (1912), Zimin
(1948), Chillcott (1961), Ishijima (1967), Lyneborg (1970)
and Holloway (1984). Additional figures representing the
F. canicularis third instar, but without a description of lar-
val morphology, were provided by Hennig (1952) and Huckett
& Vockeroth (1987).
Scanning electron microscopy (SEM) has been used pre-
viously in Fanniidae by Hinton (1981) to study egg mor-
phology, by Couri (1992) to investigate the egg, third instar
and puparium of Fannia pusio (Wiedemann), and by Al Gazi
et al. (2004) to examine the eggs, third instars, puparia and
adults of F. pusio and Fannia trimaculata (Stein). The aim of
this study is to provide detailed morphological documentation
of all larval instars of F. canicularis. For this purpose, both
light microscopy and SEM were applied; the results are com-
pared with previous descriptions of fanniid larvae and existing
knowledge of the larvae of calyptrate flies.
Materials and methods
Larvae of F. canicularis were obtained by keeping wild-caught
females in the laboratory until oviposition. Females were col-
lected indoors on the campus of Nicolaus Copernicus Univer-
sity, Toru´
n, Poland, in August 2009, using an entomological
net and were kept in 120-mL transparent plastic containers with
wet sand in the bottom. Glucose and decomposed pork liver
were used as food sources for adults and larvae, respectively.
The cap of each container was perforated with small holes to
allow for aeration.
During the period after capture, the containers were
examined twice per day to establish whether females had
spontaneously oviposited. Some of the first instars were
immediately preserved as described below. Remaining larvae
were raised and preserved successively as older instars. Larvae
of adequate age were transferred from the rearing containers
to a Petri dish, killed by immersion in hot water (≈95 ◦C),
cleaned in distilled water with a fine brush and preserved in
70% ethanol.
For light microscopy, larvae were slide-mounted in Hoyer’s
medium. Cavity slides were used for first and second instars
and for the cephaloskeleton of third instars. Larvae were
photographed using a Nikon 8400 digital camera mounted on a
Nikon Eclipse E200 microscope (Nikon Corp., Tokyo, Japan).
Material prepared for SEM was dehydrated through 80.0%,
90.0% and 99.5% ethanol, processed in a Bal-Tec CPD 030
critical point drier, mounted on aluminium stubs with double-
sided tape and sputter-coated with platinum for 140 s (20 nm
of coating) using a JEOL JFC 2300HR high-resolution fine
coater (JEOL Ltd, Tokyo, Japan). Images were taken with
a JEOL scanning microscope (JSM-6335F; JEOL Ltd). Scale
bars on SEM images are given in micrometres.
Terminology follows Courtney et al. (2000) for general
morphology and Lyneborg (1970), Holloway (1984) and Ferrar
(1987) for family-specific structures with a few modifications
proposed by Szpila & Pape (2005). We denote segments
1–3, 4–10 and 11 sensu Lyneborg (1970) as, respectively,
T1–3 (thoracic segments), A1 –7 (abdominal segments) and
the anal division (the terminal part of the body posterior to
A7 and probably composed of several segments). Particularly
for the prominences and processes of the body wall that
encircle most segments, we follow Lyneborg (1970) in using
the positional terms ‘dorsomedian’ (DM), ‘dorsolateral’ (DL),
‘laterodorsal’ (LD), ‘lateroventral’ (LV), ‘ventrolateral’ (VL)
and ‘ventromedian’ (VM). The processes of the anal division
do not conform to the pattern of the regular segments and
we follow Lyneborg (1970) in using the terms ‘lateral’ (L),
‘sublateral’ (SL) and ‘subapical’ (SA). Long fleshy structures
covering the larval body are named ‘processes’. The term
‘prominences’ is reserved for small structures, usually with
a papilla in the middle, which can be wart-like or surrounded
by a ring of short projections.
Results
The general morphology of the F. canicularis larval instars
has been described previously in some detail, in particular
by Hewitt (1912), Tao (1927) and Lyneborg (1970). The
current study concentrates on features that were insufficiently
described, wrongly interpreted or entirely omitted.
Pseudocephalon
According to the position of the pseudocephalon (retracted,
partly or fully extended), 11 or 12 body segments are visible
(Figs 1A, 2A, 3A, 3D, 4A). The pseudocephalon is bilobate
(Figs 1C, 2A, 3D) and the anterior of each lobe carries the
antenna (Figs 1F, 2F, 3F), maxillary palpus (Figs 1D, 2E, 3E)
and ventral organ (Figs 1E, 2H, 3G). The maxillary palpus
consists of three sensilla coeloconica, three sensilla basiconica
and one or more small additional sensilla, all in a tight cluster,
as well as two additional sensilla coeloconica possibly of non-
maxillary origin (Figs 1D, 2E, 3E). The antennal complex
includes a basal pore and a lateral pore with a sensillum
(Figs 1F, 2F, 3F).
Cephaloskeleton
The cephaloskeleton of the first instar significantly differs
from those observed in second and third instars. The first-
instar cephaloskeleton is typical of the schizophoran type
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72 A. Grzywacz et al.
(A) (B)
(C)
(D)
(E)
(F) (G)
Fig. 1. First instar of Fannia canicularis. (A) Anterior end of body, dorsolateral view. (B) Respiratory aperture. (C) Pseudocephalon, ventral view.
(D) Maxillary palpus. (E) Ventral organ. (F) Antennal complex. (G) Keilin’s organ on T1. AP, anterior process; DL, dorsolateral process; DM,
dorsomedian process; LD, laterodorsal process; LV, lateroventral process; LP, lateral process; MH, mouthhook; NS1 [NS2], first [second] additional
sensillum coeloconicum; RA, respiratory aperture; SB1 [SB2/SB3], first [second/third] sensillum basiconicum; SC1 [SC2/SC3], first [second/third]
sensillum coeloconicum.
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Fannia larval morphology 73
(A) (B)
(C)
(D)
(E)
(F) (G) (H)
Fig. 2. Second instar of Fannia canicularis. (A) Anterior end of body, ventral view. (B) Anterior spiracle. (C) Posterior spiracle, dorsal view.
(D) Second thoracic segment, ventral view. (E) Maxillary palpus. (F) Antennal complex. (G) Keilin’s organ on T2. (H) Ventral organ. AVL,
additional ventrolateral prominence; KO, Keilin’s organ; LP, lateral process; LV, lateroventral process; MH, mouthhook; NS1 [NS2], first [second]
additional sensillum coeloconicum; P, papilla; S, posterior spiracle plate sensillum; SB1 [SB1/SB2], first [second/third] sensillum basiconicum;SC1
[SC2/SC3], first [second/third] sensillum coeloconicum; VL, ventrolateral prominence; VMA, anterior ventromedian prominence; VMP, posterior
ventromedian prominence.
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74 A. Grzywacz et al.
(A) (B)
(C)
(D)
(E)
(F) (G) (H)
Fig. 3. Third instar of Fannia canicularis. (A) Anterior end of body, lateral view. (B) Lateral base of anterior process. (C) Anterior spiracle.
(D) Anterior end of body, ventrolateral view. (E) Maxillary palpus. (F) Antennal complex. (G) Ventral organ. (H) Keilin’s organ on T1. LP, lateral
process; NS1 [NS2], first [second] additional sensillum coeloconicum; P, papilla; SB1 [SB2/SB3], first [second/third] sensillum basiconicum; SC1
[SC2/SC3], first [second/third] sensillum coeloconicum.
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Fannia larval morphology 75
(A)
(B)
(C)
(D)
(E)
(F)
Fig. 4. Fannia canicularis larvae. (A) First instar, habitus, lateral view. (B) First instar, cephaloskeleton, lateral view. (C) First instar,
cephaloskeleton, ventral view. (D) Second instar, facial mask, ventral view. (E) Second instar, cephaloskeleton, lateral view. (F) Third instar,
cephaloskeleton, lateral view.
and consists of an unpaired labrum, paired mouthhooks, an
unpaired intermediate sclerite, paired parastomal bars and
paired vertical plates, each with ventral and dorsal cornua and
connected by a dorsal bridge (Figs 4B, 4C, 5A). The entire
cephaloskeleton is weakly sclerotized except for the anterior
part of the labrum and the vertical plates (Fig. 4A–C). The
mouthhook is shaped like a long, upwardly curved rod, with a
slightly widened basal part carrying a lateral arm-like process
(Fig. 5A). The mouthhook is apically equipped with a single
tooth directed ventrally (the weak sclerotization makes the
precise recognition of its shape difficult). The unpaired labrum
is shaped like a broad knife blade (Figs 4B, 5A). The labrum
is rigidly fused with the tips of the parastomal bars. Each
parastomal bar is long and slender. The intermediate sclerite
is elongated and H-shaped (Fig. 5A). The crossbeam of the
intermediate sclerite is perforated by an oval aperture. The
vertical plate is slightly broader than the ventral cornu. The
dorsal cornu is very short and about half as long as the ventral
cornu.
The cephaloskeletons of the second and third instars are very
similar (Fig. 5B, C). The basal sclerite is long and consists
of a very broad lateral plate, a rather short dorsal cornu and
a longer ventral cornu that is very broad at its base. The
dorsal bridge is massive and has characteristic perforations
(Figs 4E, 4F, 5B, 5C). The parastomal bars are not developed.
The intermediate sclerite is slightly elongated and H-shaped
with a broad crossbeam (Fig. 5B). In the lateral view the
crossbeam is visible as a distinct process on the ventral surface
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76 A. Grzywacz et al.
(A)
(B)
(C)
Fig. 5. Cephaloskeleton of Fannia canicularis larvae. (A) First instar, ventral and lateral view. (B) Second instar, ventral and lateral view. (C) Third
instar, lateral view. DB, dorsal bridge; DC, dorsal cornua; DS, dental sclerite; IS, intermediate sclerite; LA, lateral arm; LB, labrum; LS, labial
sclerite; MH, mouthhook; PB, parastomal bar; VC, ventral cornua; VP, vertical plate.
directed posteroventrally (Figs 4E, 4F, 5B, 5C). A paired
sclerotization (labial sclerite?) is visible between the anterior
arms of the intermediate sclerite. The paired mouthhooks are
the anteriormost sclerites of the cephaloskeleton. The basal part
of the mouthhook is robust and has a ventrolateral extension.
The posterodorsal angle or corner of the mouthhook is drawn
out into a distinct process. In the second instar, the middle part
of each mouthhook is slender and straight, and the distal part
is broader, slightly curved laterally, and equipped with several
(about eight) teeth along the ventral margin. The connection
between the slender part and the serrated apical part is difficult
to observe and the serrated part may be mistaken as a separate
sclerite (Fig. 4E). In the third instar, the apical part of each
mouthhook takes the form of a down-curved, pointed hook.
Below the massive basal part of the mouthhooks are paired
dental and labial sclerites.
Keilin’s organ
Keilin’s organ consists of two trichoid sensilla (Figs 1G,
2G, 3H, 6C). The distances between pairs of pits with trichoid
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Fannia larval morphology 77
(A) (B)
(C) (D)
(E)
(F) (G) (H)
Fig. 6. First instar of Fannia canicularis. (A) Abdominal segments, dorsolateral view. (B) Anal division, lateral view. (C) Third thoracic segment,
ventral view. (D) Ventromedian prominences on A1. (E) Posterior spiracle stalk, anterior view. (F) Anal pad, ventral view. (G) Ventrolateral
prominence. (H) Posterior spiracle, dorsal view. KO, Keilin’s organ; L, lateral process on anal division; P, papilla; SA, subapical process on anal
division; SL, sublateral process on anal division; ST, spiracular tuft; VL, ventrolateral prominence.
sensilla of Keilin’s organ are variable (Figs 1G, 6C): on T1 this
distance decreases (in relative terms) from the first to the third
instar, and is especially markedly reduced from the second
to the third instar, in which the pits become almost adjoined
(Fig. 3H). The relative distance between pits is larger in T2–3
than in T1.
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78 A. Grzywacz et al.
Pattern of processes
Two pairs of minute prominences with spine-like projections
are present in all instars to the front of the anterior spiracle
(Figs 1B, 2B, 3C). These prominences are barely visible in
standard light microscopy.
Two pairs of ventromedian prominences are present on
T2–A7. On T2 –3 these are arranged as an anterior and a
posterior pair (Figs 2D, 7C, 7D), whereas on A1–7 they
are arranged in a transverse line (Fig. 7E, F). One pair of
additional ventromedian prominences is seen on A1–7 in
the first and second instars and on A2–7 in the third instar
(Fig. 7F). The ventromedian prominences of the first instar
are simple wart-like structures without any visible central
papilla or associated projections (Fig. 6D). In the second and
third instars, the ventromedian prominences are equipped with
spine-like projections surrounding the central papilla (Figs 2D,
7D–F), except for those on T2 in the third instar and the
posterior ventromedian prominences on T2–3 in the second
and third instars, which are simple papillae (Fig. 7C). The
ventrolateral prominences present on T2–A7 have similar
spine-like projections in all instars (Fig. 6G).
On T2 between the lateroventral and ventrolateral promi-
nences, in the middle of the segment, an additional ventro-
lateral prominence with spine-like projections can be seen
(Fig. 2D); this is barely visible in standard light microscopy.
No such additional structure was observed on any other seg-
ment. In the third instar, this additional structure is present
as a papilla without surrounding projections, similar to the
ventromedian prominences of this segment (Fig. 7C).
The sublateral processes on the anal division are shorter than
the lateral and subapical processes. The difference in length
in the sublateral process is most distinct in the first instar
(Fig. 6B).
Anterior and posterior spiracles
The anterior spiracle in the first instar is present as a simple
respiratory aperture (Fig. 1B), which is invisible in standard
light microscopy. The anterior spiracles on subsequent instars
are similar in shape, have about seven lobes, and are longer
in the third instar. The posterior spiracles are raised on robust
stalks, each of which has a papilla in the anterolateral position
(Figs 2C, 6B, 6E). The first instar shows two slits, the second
instar shows three slits on small baton-like projections and the
third instar demonstrates each of the three slits on a small
finger-like lobe. The plate of each of the posterior spiracles
has four simple spiracular tufts in the first instar (Fig. 6H), one
trichoid sensillum in the second instar (Fig. 2C), and a complex
of two trichoid sensilla in the third instar (Fig. 7G, H).
Integumental sculpture
The surface of the first instar lacks any trace of a polygonal
pattern (Figs 1A, 6A–C); the body is covered with spines,
which are more numerous on the anterior of each segment.
Spines located to the posterior of each segment often have
branched tips. Ventrally, spines are limited to the anterior part
of each segment (Fig. 6C) and the highest numbers of spines
occur on T1–3. Dorsally and laterally, the middle and anterior
parts carry simple spines, whereas the remaining part of each
segment carries branched spines (Fig. 6A). In the second instar,
the body is partly smooth, with a faint polygonal pattern, and
is covered with a few wart-like prominences and small spines
that are less numerous in comparison with those on the first
instar. Ventrally, the spines are limited to the anterior part of
each segment. The serrated tip of each mouthhook is exposed
on the surface of the pseudocephalon and constitutes a part of
the facial mask (Figs 2A, 5B).
The third instar cuticle is pebbled with a polygonal pattern
on the thorax (Fig. 3A) and shows an increasing number
of wart-like projections to the posterior (Fig. 7A), some of
which, especially those distributed laterally on the body, have
pointed tips. T1 is without spines, whereas T2 and subsequent
segments have simple spines located anterodorsally and
anterolaterally (Fig. 7B, C). Segments A1–7 posterodorsally
and posterolaterally show bands of spines and warts (Fig. 7A).
The anterior processes and lateral parts of the body near their
base are equipped with papillae (Fig. 3B).
Discussion
Comparison with previous works
The terminologies used by earlier authors differ from that
proposed by Lyneborg (1970) and accepted by the present
authors. Hewitt (1912), Tao (1927) and Ishijima (1967)
numbered the segments from 1 (pseudocephalon) to 12 (anal
division), and the ‘cephalic region’ described by Chillcott
(1961) represents the combined pseudocephalon +T1–3,
which explains why Chillcott (1961) denoted the anterior
process on T1 as a ‘cephalic process’.
Tao (1927) described five pairs of processes per segment
in the first and second instars, but did not observe any
ventromedian processes. Tao (1927) used the terms ‘lateral
dorsal’ and ‘dorso-lateral’ interchangeably for laterodorsals
and stated that ‘sessile branched appendages are situated
near and slightly posterior to the base of the dorso-lateral
appendages’ in a description that clearly refers to the
dorsolateral prominences. Tao (1927) also mentioned that the
laterodorsals ‘consist of 11 pairs of processes commencing on
segment 3 and continued to the posterior end of the body’.
Hewitt (1912) described a ‘latero-dorsal series of ten pairs of
processes which commences on segment 3 and is continued
to the posterior end of the body’. Assuming that the third
segment sensu Hewitt (1912) and Tao (1927) is T2 and that
the three pairs of processes on the anal division can be treated
as laterodorsals (Tao, 1927; Lyneborg 1970), F. canicularis
possesses 12 pairs of laterodorsals (nine on T2–A7 and three
on the anal division), not 10 (Hewitt, 1912) or 11 (Tao,
1927). Zimin (1948) described four pairs of processes in the
third instar, but did not describe dorsolaterals and did not
differentiate ventromedians and ventrolaterals.
Hewitt (1912), Zimin (1948) and Holloway (1984) noticed
that the pseudocephalic segment is often withdrawn into the
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Fannia larval morphology 79
(A) (B)
(C) (D) (E)
(F) (G) (H)
Fig. 7. Third instar of Fannia canicularis. (A) First and second abdominal segments, laterodorsal view. (B) Posterior end of body, dorsal view.
(C) Second thoracic segment, ventrolateral view with position of papillae in place of additional ventrolateral process and ventromedian processes.
(D) Third thoracic segment, ventral view. (E) First abdominal segment, ventral view. (F) Second abdominal segment, ventral view. (G) Posterior
spiracle, dorsal view. (H) Posterior spiracle plate sensillum. AVL, additional ventrolateral process; AVM, additional ventromedian process; DL,
dorsolateral process; DM, dorsomedian process; L, lateral process on anal division; LD, laterodorsal process; LV, lateroventral process; P, papilla;
SL, sublateral process; SA, subapical process; VL, ventrolateral process; VM, ventromedian process.
prothoracic segment. Rozkoˇ
sn´
yet al. (1997) and Pont (2000)
mentioned that 11 visible segments can be found in larvae
of Fanniidae, which can lead to the erroneous supposition
that the pseudocephalon is reduced or is always retracted into
the prothoracic segment. Retraction of the pseudocephalon
has been observed in response to factors such as mechanical
stimulae in live larvae of all instars. In preserved material,
configurations ranging from a fully extended to a fully retracted
pseudocephalon were observed. Adams & Hall (2003) studied
the influence of methods used for killing on the general
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80 A. Grzywacz et al.
shrinking of larvae and found significant differences in larval
body length depending on water temperature and time of
soaking. Similar influences may be suspected to affect the
relative position of the pseudocephalon. Descriptions based
on late third instars often stress the presence of 11 visible
segments because the pseudocephalon is retracted during
puparial formation in Fanniidae (Ferrar, 1987). It should be
emphasized, as Hewitt (1912) did, that larvae of F. canicularis
(and evidently other Fanniidae species) ‘consist of twelve
segments, of which the first, or pseudocephalic segment, is
often withdrawn’. In our opinion, the pseudocephalon should
be included except in simple figures that show only species-
specific patterns of processes.
Of the three pairs of processes present on the anal division
in F. canicularis, the sublateral is distinctly shortest (Fig. 7B).
The length of this process is one of the characters upon which
the identification of F. canicularis is based (Lyneborg, 1970;
Rozkoˇ
sn´
yet al., 1997). However, in Huckett & Vockeroth
(1987; Fig. 50), the sublateral process appears to be at least
as long as the lateral process. In Hennig (1952; Fig. 5),
the sublateral processes are shown as only slightly shorter
than the subapical pair. According to Hewitt (1912) and
Lyneborg (1970), the sublateral process is localized closer to
the lateral than to the subapical process. We observed such a
position in the first instar (Fig. 6B), whereas, in the second
and third instars, the sublateral process is positioned midway
between the lateral and apical processes (Fig. 7B). This is in
agreement with Zimin (1948; Fig. D3), Hennig (1952; Fig. 5)
and Ishijima (1967; Fig. B).
The posterior spiracles in the third instar of F. canicularis
were described by Ishijima (1967) as ‘raised on [a] long stalk
and with 3 or 4 branches’. However, describing the posterior
spiracles of Fannia prisca Stein and Fannia scalaris (Fabri-
cius), Ishijima (1967) mentioned only three branches. The pos-
terior spiracle of third-instar Fanniidae, except in a few New
Zealand species (Holloway, 1984), are known to have three
more or less protruding lobes (Ferrar, 1987). The most probable
explanation for such a description is that Ishijima (1967) mis-
interpreted the spiracular scar as a separate lobe (see Fig. 7G).
Al Gazi et al. (2004; Fig. 5E, F) also mentioned four openings
on the posterior spiracle of F. pusio and F. trimaculata, but
used the term ‘openings’, not ‘branches’ or ‘lobes’.
In Pont (2000; Figs 15, 16) the captions under the figures
representing larvae of F. canicularis and fellow fanniid
Piezura graminicola (Zetterstedt) (as Piezura boletorum Ron-
dani) have probably been switched around in error. The figure
representing F. canicularis refers to a Piezura and vice versa.
Anterior spiracles
Generally, anterior spiracles are described as absent in first-
instar Cyclorrhapha (Ferrar, 1987). Couri (1992) described
first-instar anterior spiracles in F. pusio as consisting of
seven lobes. We consider that this opinion was based on
a misinterpretation of a pharate second instar (i.e. an early
second instar within the still-intact exoskeleton of a late
first instar). Kitching (1976), studying first-instar larvae of
several species of Calyptratae, reported the presence of a
simple, open orifice in a position at which the anterior
spiracle might be expected. A similar feature has been found
in species of the families Calliphoridae (Leite & Guevara,
1993), Muscidae (Grzywacz & Pape, unpublished data, 2010),
Oestridae (de Filippis & Leite, 1997), Sarcophagidae (Cantrell,
1981; Leite & Lopes, 1989; Szpila, 2010; Szpila & Pape,
unpublished data, 2010), Tephritidae (Elson-Harris, 1988) and
Agromyzidae (Dempewolf, 2001). The respiratory aperture in
F. canicularis would seem to resemble that described by Leite
& Lopes (1989) in Peckia chrysostoma (Wiedemann) (Diptera:
Sarcophagidae), although the wrinkles reported by the latter
authors are possibly an artefact of their methods of preparation.
A simple orifice without accessory structures has been reported
in other species. We consider it very likely that a pair of very
indistinct (but probably fully functional) spiracles will be found
on T1 in other families of Cyclorrhapha. The common belief
that anterior spiracles are absent in the first instar may have led
students to ignore the possible presence of respiratory openings
during SEM studies (e.g. Liu & Greenberg, 1989; Bonatto &
Carvalho, 1996; Szpila & Pape, 2008; Draber-Mo´
nko et al.,
2009). Should a first-instar anterior spiracle be widespread in
the Cyclorrhapha, methods of distinguishing first instars from
subsequent instars should be modified as suggested by Kitching
(1976), who described the anterior spiracles as ‘minute, not
papillose, barely distinguishable using light microscopy’.
Serrated mouthhooks
In his description of the morphology of second-instar
F. canicularis, Tao (1927) did not report the presence of
sclerotized structures on the facial mask, as were revealed
here. We consider these sclerotized structures to be integral
parts of the mouthhooks, although the connection with the
remaining mouthhook is weakly sclerotized and difficult to
observe in light microscopy. It should be mentioned that some
authors (e.g. Skidmore, 1985) have treated such structures
located apically on the cephaloskeleton as separate sclerites
named ‘suprabuccal teeth’. No similar mouthhooks have been
reported in any other Fanniidae (Lyneborg, 1970; Holloway,
1984; Couri, 1992).
Additional ventrolateral prominences
Although they are positioned very closely to the lateroventral
processes, we decided to name these prominences ‘additional
ventrolaterals’ because of their similarity in shape to the
prominences on the ventral surface. They are probably
not serially homologous with any of the other processes
as all six groups of processes are present on T2. It is
more likely that these represent a seventh pair of sense
organs that are fully developed and surrounded by spine-like
projections only on T2 and present in the third instar only
as a sensillum. Holloway (1984) also observed the structures
we call ‘additional ventrolateral prominences’, but described
them as lateroventrals, whereas lateroventrals sensu Lyneborg
(1970) and previous authors were considered to be additional
processes on T2. Given this contradictory information, and
©2011 The Authors
Medical and Veterinary Entomology ©2011 The Royal Entomological Society, Medical and Veterinary Entomology,26, 70–82

Fannia larval morphology 81
based on the positions of lateroventrals sensu Holloway (1984)
and sensu Lyneborg (1970)—the middle and anterior parts
of the segment, respectively—we prefer to follow Lyneborg
(1970) and treat the lateroventrals described by Holloway
(1984) as additional ventrolateral prominences.
Like Holloway (1984), we observed the presence of anterior
and posterior ventromedians on third-instar T2–3, of which
only the anterior ventromedians on T3 had surrounding
projections. Similarly, in second-instar larvae, the anterior
ventromedians and, in a few cases, even the posterior
ventromedians, possess spine-like projections.
To summarize earlier descriptions and the findings of
recent data, all instars of F. canicularis have ventrolateral
prominences on T2–A7, pairs of anterior and posterior
ventromedians on T2–3 and two pairs of ventromedians on
A1–7. An additional pair of prominences are found on A1 –7
(on A2–7 in third instars).
Posterior spiracle
According to Ferrar (1987), spiracular tufts are found in
Fanniidae only in the first instar; this claim is corroborated
by the present study. The spiracular plates in second and
third instars show one and two trichoid sensilla, respectively
(Figs 2C, 7G, 7H). Holloway (1984) reported the presence
of circular sensilla on the posterior spiracular plate in three
undescribed New Zealand endemics, but Couri (1992) and Al
Gazi et al. (2004) did not report any such sensilla in their SEM
studies of two species of Neotropical Fannia. No additional
information on the presence of such sensilla in other calyptrate
species has been reported (Courtney et al., 2000). Such sensilla
might be expected to occur in families in which the larvae
have posterior spiracles that are similarly raised on stalks (e.g.
in Platypezidae and Phoridae). However, no such sensilla were
reported by Tkoˇ
c&Va
ˇ
nhara (2008) in Lindneromyia hungarica
Chandler (Diptera: Platypezidae) or by Boonchu et al. (2004)
in Megaselia scalaris (Loew) (Diptera: Phoridae).
Lateral prominences on T1
The small, lateral spine-like prominences present on T1
(Figs 1B, 2B, 3C) bear considerable similarity in structure
and position to the laterodorsal and lateroventral processes
present on successive segments. Using light microscopy,
Holloway (1984) described the presence of one pair of minute
processes consisting ‘of a ring of simple projections’ in
F. canicularis. Despite describing two pairs of such minute
lateral prominences on T1 in other New Zealand Fanniidae,
Holloway (1984) did not observe a second pair of minute
prominences in F. canicularis, as we observed below the
anterior spiracle in the third instar.
Acknowledgements
We thank Dr A. C. Pont, (Oxford University Museum
of Natural History, Oxford, U.K.) for comments on this
manuscript and Professor M. S. Couri, (Museu Nacional,
Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ,
Brazil) for help with important literature.
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Accepted 25 February 2010
First published online 24 June 2011
©2011 The Authors
Medical and Veterinary Entomology ©2011 The Royal Entomological Society, Medical and Veterinary Entomology,26, 70–82