2

Eggs

The fly is only an egg's way of making another egg (to paraphrase Samuel
Butler's famous quip about hens).

2.1 INTRODUCTION

The egg is the least studied stage of scuttle flies. Egg production, however, is
the principal function of the adult fly.
The morphology of scuttle fly eggs has not been studied systematically,
but a preliminary review is given by Ferrar (1987). It is evident that phorid
eggs are very varied in form. Detailed studies are likely to be rewarding in
terms of adaptations of form to suit different ecological situations. The
best-known egg is that of Megaselia scalaris (Fig. 2.1). The boat-shaped form,
and gunwale-like palisade of flat platelets surrounding the respiratory
plastron with its scattered tubercles, is associated with deposition of the egg
into relatively liquid media (Ferrar, 1987). A similar egg is produced by the
saprophagous ·M. spiracularis (Furukawa and Kaneko, 1981) and by the
aquatic M. deningi (Fig. 2.2a) (Kaneko and Furukawa, 1983; Disney, 1991i).
A contrasting egg is that of the aquatic M. kovaci. Its plastron is restricted to
the anterior region, in a subterminal position (Fig. 2.2b). It is probably laid in
the meniscus on the wall of the bamboo internode, with its anterior end
upwards (Disney, 1993b). Even relatively simple eggs of closely related
species may vary considerably in shape (length to breadth ratios) (Fig. 2.3).
The eggs of the Termitoxeniinae Clitelloxenia hemicyciia, Javanoxenia
punctiventris and Odontoxenia brevirostris are known to be good mimics of the
eggs of their termite host, Odontotermesjavanicus. Indeed the worker termites
collect the fly eggs and place them among their own. Furthermore they
regularly groom the eggs along with their own, and thus keep them free of
mould (Franssen, 1933b). The relatively enormous size of these eggs, in
relation to the size of the fly (Kemner, 1926; Reichensperger, 1931), may be
related to the curtailment of the larval stages (5.3). Furthermore Michl (1911)
reported that the egg of Termitoxenia havilandi measures 1.15 X 0.40 mm
compared with the egg of its host termite, Odontotermes latericius, which
measures only 0.75 X 0.37 mm.
There is clearly much scope for critical studies of the varieties of form and

R. H. L. Disney, Scuttle Flies: The Phoridae

© R H L Disney 1994
 EGGS

Figure 2.1 Eggs of Megaselia sealaris, wIth antenor ends facing top of page. (a) From
above. (b) From sIde. (Photos by John Lmley.)

relative sizes of phorid eggs in relation to oviposition site and the subsequent
larval habits.
The study of phorid sperm is an almost totally neglected field. Curtis et al.
(1989) have laid the foundations for future comparative studies, with their
detailed account of the ultrastructure of the sperm of Megaselia scalaris. The
spermatozeugmata (spermatophore-like aggregations of sperm) are dis-
cussed by Benner (1991). They lack the capsule, around the sperm mass, of a
true spermatophore.

2.2 FECUNDITY, BATCH SIZE AND CLUTCH

SIZE
Data on fecundity exist for only a few species. These are reviewed below. A
female may lay a succession of egg batches, with a pause after each batch. The
total number of eggs laid, in all the batches added together, represents the
actual fecundity. The eggs of a single batch may be laid together in the same
place, as a single clutch, or divided into a number of separate clutches. In the
former case the batch size and clutch size are the same. A clutch may be as
little as a single egg.

14
 INTRODUCTION

(b)

Figure 2.2 The contrastmg eggs of two aquatIc speCles of Megasella (a) M denmgt
(b) M kovaet, wIth anterIor end to rIght ((a) after Kaneko and Furukawa, 1983 )

• ~ ... • "•• • • r ~

, -,

',' .' :' ..:

. .~. ";' ,
. ;:.:' :" ~

(a)

Figure 2.3 The eggs of Megaselta specIes (a) M halterata (b) M stenoterga
(c) M oxybelorum

15
 EGGS

The number of eggs matured and laid at one time (that is the batch size)
varies from 1 to 100, the number depending on the species and the condition
of the female. Benner (1985) studied oocyte development in Megaselia sealaris
and found that the number of mature oocytes ranged from 12 to 77, with
oocyte development being synchronized in the different ovarioles and with
only one mature oocyte per ovariole.
A low batch size would seem to be associated with two distinct
phenomena. In some cases it is correlated with refined predatory or parasitic
larvae, following accurate placement of each egg in relation to the target host
or prey. The high chance of success compensates for risks associated with a
concentrated investment. In the case of the con flies Diplonevra mortimeri and
D. watsoni, parasitizing termites (3.5.6(£)), the one and only egg matured at
one time is inserted into the comatose termite, which is then concealed with
soil particles and guarded (Disney, 1986d). By contrast Misotermes exenterans
scatters large numbers of eggs in its host-termite's nest, relying on chance
encounters by the soldier termites, their target hosts (Kalshoven, 1938).
The other phenomenon associated with a reduced batch size is accelerated
larval development and suppression of the free-living larval stage. For
example, the larva of Clitelloxenia hemieyclia takes no food after emerging
from the egg. Associated with this is an unusually long duration of the egg
stage (Kemner, 1926; Franssen, 1933b) (5.3). In Assmutherium rostratum
apparently only three eggs are matured at a time, and it seems the embryos
start to develop before the eggs are laid (Fig. 2.4) (Disney, 1991m).
In some cases probably both phenomena are involved in batch-size
reduction. This would seem to be the situation in the genus Pulieiphora. Thus
the polyphagous saprophage P. togata matures only eight eggs at a time,
compared with about two dozen in the polyphagous saprophage P.
borinquenensis. This reduced batch size probably relates to the relatively large
egg size and a rapid larval development. In the specialized predator P. boltoni,
whose adults live in the colonies of their ant hosts, and in P. eollinsi, almost

Figure 2.4 Embryo mSlde egg sull retamed by a gravId female of AssmutheYlum
rostratum, with antenor end to nght.

16
 FECUNDITY, BATCH SIZE AND CLUTCH SIZE

certainly a parasitoid of termites, only four eggs are matured at a time

(Disney, 1988b). A reduced batch size in Rhynchomicropteron nudiventer, ofl-4
eggs (Table 2.1), probably relates to accelerated larval development, as the
larva is known to be a saprophage within the colonies of its ant host (Brown,
1992a).
Some data on fecundity and reported batch or clutch sizes are reviewed
below:

Apocephalus attophilus
The batch size is 10-16 eggs, but only one egg is laid in each ant host (Feener
and Moss, 1990).

Dohrniphora cornuta
Weiss (1911) reported a batch size of30-40 eggs in this species. At 23° ± 1° C,
Barnes (1990a) reported that females laid 9.4-12.0 eggs per day. Fecundity
ranged from 77-535 (mean 368 ± 143) eggs per female.

Megaselia aletiae
Balduf (1928) reported 50 eggs laid by a single female on the back of a
caterpillar (3.5.6(g)).

Megaselia halterata
In captivity this species is reported to lay about 50 (40-60) eggs at a time
(Moreton andJohn, 1955; Hussey, 1960a), and Hussey (1965) reported about
40 mature eggs in wild-caught females. Females parasitized by nematodes
(6.8.2(b)) may lay as few as 2-3 eggs per batch (Hussey and Gurney, 1964a).

Megaselia rubricornis
1-5 (usually 2) eggs are laid on each beetle-host pupa (3.5.6(b)), and 30-40
eggs arelaid within 10 days (Kanervo, 1946).

Megaselia sealaris
Semenza (1953) reported a mean batch size of 32.2 (643 progeny obtained
from 20 pairs) at 23°C. EI-Miniawi and Moustafa (1965) reported a mean
fecundity of 391 eggs (range 42-749) spread over a mean of 10 egg-laying
periods (the first being 38 h after emergence) at 27°C.
A later study only observed an output of two batches, each of9-26 eggs, in
the first seven days (Tumrasvin et al., 1977). Prawirodisastro and Benjamin
(1979) reported a mean of664.8 eggs per female (range 192-1003) spread over
16 egg-laying days at 25°C. The first batch was laid at an age of 45.6 h (1.9
days). The largest batches were laid after 17 days. Mean fecundity decreased
to 591 (± 213.0) at 20°C and 146.9 (± 51.3) at 15°C.
Dias Macieira et al. (1983) reported that this species lays a first batch with a
mean of21.6 (± 11.8) 24-48h after mating, at 25-30°C. Given a constant
supply of fresh medium, the second batch (laid within the next 24 h) averaged
21.5 (± 23.4) eggs; and a third batch (within the next 24 h) averaged 60.0

17
 EGGS

(± 23.2) eggs. The overall average was 103.2 eggs per female within 96 hours
of mating.
Kneidel (1985) reported that this species laid 69.4 (± 7.6) eggs in 24 h at
27 °C, and also that fecundity is affected by body size. The latter was affected
by the amount of competition for food as a larva.
McCrae's (1967) observations on this species breeding in a pot of paint
(3.2) suggested that more than 350 eggs had been laid by a single female. This
is of the same order as the fecundity estimates of EI-Miniawi and Moustafa
(see above).

Other Megaselia species

The predators of gall insects M. chainensis and M. submarginalis lay clutch sizes
of1-3 eggs and 1 egg, respectively, per gall (Robinson, 1970; Robinson and
Brown, 1993). Their batch sizes are not known, but are presumably much
larger.

Pseudohypocera kerteszi
Chaud-Netto (1980) reported fecundity figures of 31-102 eggs per female,
with a mean of66.4.
Some other records of batch sizes are given in Table 2.1.

2.3 DEVELOPMENT

The eggs of Megaselia halterata require a moisture film for successful

development (Hussey and Gurney, 1964a).

2.4 EGG MATURATION

The experiments of Hussey (1960) suggest that Megaselia halterata will

develop mature eggs prior to mating, but M. nigra females will only mature
their eggs after mating. The eggs of M. halterata take 3-5 days to mature,
from the time of eclosion of the adult (Hussey, 1965). Phalacrotophora Jasciata
has been reported to take 15 days to mature sexually in the laboratory
(Hodek, 1973). It is possible that the reported laboratory diet (of sugar, agar,
honey and water) was inadequate when compared with the normal diet of
females. If they normally require a meal of insect haemolymph (6.3) to
mature their eggs, then a lack of such a protein-rich meal might delay
development.
Benner's (1985) studies of oocyte development in Megaselia scalaris showed
that by the age of 34 h, at 25°C, all females had mature eggs. At 24 °C this
species normally starts laying on the second day after emergence. He also
reported that virgin females will lay unfertilized eggs, but not until day 3.
However, Ondraschek (1953) reported that mating did not occur until day 2,
and that oviposition only starts 2-3 days after mating. Dias Macieira et al.

18
 EGG MATURATION

Table 2.1 Some recorded egg batch sizes for Phoridae

Species Batch size Reference

Assmutherium rostra tum 3 Disney (1991m)

Ceylonoxenia bugnioni 6 Bugnion (1913)
Clitelloxenia peradeniyae 2 Bugnion (1913)
Dicranopteron oligoseta 1 Disney and Kistner (1990a)
D. philotermes 4 Disney and Kistner (1990a)
D. setipennis 1 Disney and Kistner (1990a)
Diplonevra florea 30-40 Schmitz (1949c)
D. mortimeri 1 Disney (1986d)
D. watsoni 1 Disney (1986d)
Maculiphora aenictophila 1 Disney and Kistner (1991)
Megaselia brevissima 20 Disney (1988h)
M. curtineura 16 Disney (1991 a)
M. dentata 10 Com pton and Disney (1991)
M. harteni 14 Disney (1991 h)
M. longicostalis 4 Unpublished
M. malvinasensis 2 Disney (1989h)
M. microcurtineura 4 Disney (1991 a)
M. miniseta 28 Disney (1991h)
M.orgaoa 24 Disney (1991 h)
M. oxybelorum 2 Disney (1988h)
M.pagei 60 Disney (1987g)
M. parvorata 16 Compton and Disney (1991)
M. pseudobrevior 10 Disney (1988h)
M. pulicaria 20 Unpublished
M. sembeli 4 Disney (1986b)
M. sinuata 14 Unpublished
M. stenoterga 2 Disney (1988h)
M. verdensis 35 Disney (1991h)
Metopina galeata 6 Unpublished
Puliciphora boltoni 4 Disney (1988b)
P. borinquenensis 25 Paterson (1953)
P. collinsi 4 Disney (1988b)
P. jacobsonorum 8 Disney and Kistner (1989a)
P. malae 4 Disney (1990f)
P. rosei 2 Disney (1988b)
P. rufipes 14 Unpublished
P. tambopata 14 Disney and Kistner (1989a)
P. togata 8 Disney (1988b)
Rhynchomicropteron necaphidiforme 1 Disney (1990c)
R. nepalensis 1 Disney (1991g)
R. nudiventer 1-4 Steghaus-Kovac and Disney
(1990), Disney (1990c, 1992b)

(1983) reported that this species lays its first batch of eggs about 24 h after
mating. These differences probably reflect different temperature regimes or
differences in the condition of the flies. At 22-24 cC, Dohrniphora cornuta starts

19
 EGGS

laying eggs 1-3 days after eclosion, and mating frequently takes place on the
day of eclosion (Barnes, 1990a).

2.5 OVIPOSITION

Most Phoridae oviposit directly onto or into, or at least close to, the larval
pabulum. The well studied pests of cultivated mushrooms are examples.
Having mated within 24h of emergence, Megaselia halterata will start
ovipositing within 2-3 days of emergence and will continue laying for about
10 days (Hussey and Gurney, 1964a). The eggs are laid about 1 mm from the
tips of the growing hyphae (Hussey et al., 1969). M. nigra will only oviposit in
the light (Hussey and Wyatt, 1962). This species and M. bovista oviposit onto
the freshly opened gills of mushroom sporophores (Hussey, 1961a).
Preliminary investigations (Grove and Blight, 1983) suggest that M. halterata
locates Agaricus bisporus by the C 8 aliphatic alcohols and ketones given off as
volatiles by this mushroom.
Dohrniphora cornuta, breeding in trickling filter sewage systems, lays its
eggs loose in protected crevices free from moisture and the sewage film
(Kloter et al., 1977). In laboratory cultures the eggs were randomly scattered
in relatively dry areas of cotton wool (Barnes, 1990a), and are non-adherent
Oones, 1918). Likewise D. diminuens, whose larvae feed on the fungus combs
of its termite hosts, has been observed ovipositing into the general nest debris
(Disney and Kistner, 1989c).
The highly specialized physogastric females of the Termitoxeniinae (see
5.5), such as Clitelloxenia hemicyclia,Javanoxenia punctiventris and Odontoxenia
brevirostris, are restricted to the fungus gardens surrounding the queen cell of
their termite host, and they lay their eggs among the termite eggs.
In the case of Puliciphora borinquenensis, whose females are always flightless,
the male has been reported locating a suitable pabulum for oviposition,
memorizing the site, then searching for females. He then airlifts a female to
the pabulum (Miller, 1984) (6.5).
Donisthorpe (1927) reported that Pseudacteon formicarum females will strike
at one's hand if this is scented by the acid of its ant host. His observations
suggested that the initial attraction to ants was by scent and subsequently it
was by sight. Brown and Feener (1991 b) provide experimental evidence that
Apocephalus paraponerae is attracted to its host ants, Paraponera clavata, by
olfactory cues. It then oviposits into dying or injured worker ants. This
seems to be related to the frequency of aggressive encounters between P.
clavata workers, and a consequent regular supply of maimed ants. Up to 25
eggs are laid into a single ant (Brown and Feener, 191J1a). Whether these
represent single clutches or layings by up to 25 separate females is not known.
Other parasitoid species are reported to be attracted to injured individuals of
their hosts (e. g. Berland, 1933; Disney and Schroth 1989).
Melaloncha females actually oviposit on bees while the latter are in flight,
the larvae being parasitoids of the bees (3.5.6(e)) (Roubik, 1989). Most
parasitoid species oviposit directly into or onto their hosts when the latter are

20
Plate 1 Phalacrotophora foSC/ata female OVlposltmg onto prepupa of the ladyblTd
Adalia 2-punctata (Photo by Michael MaJerus)
 OVIPOSITION

,'~:,~; .. .,.
,
-

Figure 2.5 Dorsal views of ovipositors of Auxanommatidia medleri (above) and

Apocephalus wallerae (below).

not in flight. In the case of Iridophora clarki, which very rapidly darts its eggs at
its ant host as the latter are running up tree trunks or along the ground, the
ovipositor is furnished with the elastic protein resilin (Disney, 1986b).
The con fly termite-parasitoids Diplonevra mortimeri and D. watsoni
(3.S.6(f)) are attracted to exposures of termites, among which wounded
individuals are present, but they only attack healthy workers. In an
extraordinary pre-oviposition routine the female fly lands in the vicinity of
termite workers and runs up to one of them. She prods the termite near its
rear end. The termite normally responds by turning towards the direction
from which the fly approached. The fly then races to the head of the termite
and sets off running away from the termite colony. The termite, apparently
stimulated by some odour emitted by the fly, follows her closely. Termites
have been observed being led more than 2 m distance from the colony. The
victim is then rendered comatose, an egg is laid in its abdomen, and it is

21
 EGGS

Figure 2.6 Ventral views of oVIpositors of Menozz!ola schmttz! (above) and

Pseudacteon grand!s (below)

covered wIth sOlI partIcles and then guarded by the fly In SulawesI mean
attack rates at exposures of termItes have been reported as bemg up to 10 1
per hour m the case of D mort!men and up to 10 9 per hour for D watson!
(DIsney, 1986d) ThIs rapId recrUItment to sudden spIllages of termItes onto
the forest floor probably relates to the strength of the odours emanatmg from
the wounded termItes present on such occaSIOns The pOSSIble evolutIOnary
sIgmficance of attractIOn to wounded hosts IS dIscussed below (3 1)
In some parasItOld phonds the OVIposItor IS remarkably modIfied (FIgS 2 5,
2 6) WhIle the vaned forms of these OVIposItors have proved to be of great

22
 OVIPOSITION

Figure 2.7 SIde vIew of the 'sprmg-Ioaded' (reslhn operated) oVIposItor of

Irtdophora clarki.

taxonomic value, their adaptive significance is almost unexplored. However,

the mode of use of the ovipositor of Iridophora clarki (Fig. 2.7) is described
above. High-speed video might help in determining the mode of use of other
types of ovipositor which are also employed with great speed. By contrast
the ovipositor is only moderat~ly modified in the Phalacrotophora species,
which oviposit onto the static prepupae or pupae of their ladybird beetle hosts
(Plate 1) in a more leisurely manner, taking up to 25 min per host (Disney et
al.,1994).
The access of Conicera tibialis, the coffin fiy, to buried human corpses has
been the subject of controversy (Colyer, 1954a). It is now clear that
oviposition into the coffin before burial cannot explain all the data. It is
significant that bodies buried inJanuary, in England, are as heavily infested as
those buried in July. In the British Isles adults of this species have only been
reported in the months April to November (Disney, 1983a). Colyer (1954e,f)
provided clear evidence that the adults emerging from the corpse of a dog
buried about 1 m deep were able to make their way through the soil to the
surface. The soil in question was moderatly loose, with abundant worm
burrows. Lundt (1964) buried pieces of meat in soil (7.5.1) and recorded C.
tibialis adults up to depths ofO. 5 m after only 4 days from the time of burial. It
seems probable, therefore, that gravid females can make their way down
through the soil to a buried corpse. Adult Triphleba nudipalpis, emerging
from corpses of white mice buried about 0.3 m deep in a heavy clay soil, have
been found throughout the soil between the mice and the surface (Disney,
1991 d). Miller (1979a) has seen the females of Puliciphora borinquenensis

23
 EGGS

forcing their way through sand or among organic matter (such as decompos-
ing insects) by the use of vigorous abdominal peristaltic movements. The
abdomen became alternately long and thin with the ovipositor fully
extended, and short and fat. Contraction rings were seen to pass anteriorly
along the abdomen.

24