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Revue Marocaine de Protection des Plantes, 2016, N° 9: 17-37
17
Comparative Biology and Life Cycle of The Barley Stem Gall
Midge and Hessian fly (Diptera: Cecidomyiidae) in Morocco
Comparaison de la Biologie et du cycle de vie de la cécidomyie à
galle de l’orge et de la mouche de Hesse (Diptères: Cecidomyiidae)
au Maroc
LHALOUI S.1, 2, ELBOUHSSINI M.2, OTMANE R.1, 3,
OURINICHE S.1,3 & ALAMI A.1, 2,
1Institut National de la Recherche Agronomique, Centre Régional de Settat
2: International Center for Agricultural Research in the Dry Areas, Rabat, Morocco
3: Faculté des Sciences et Techniques, Université Hassan I, Settat, Maroc
ABSTRACT
The barley stem gall midge, Mayetiola hordei (Keiffer) is the most serious pest of barley in
Morocco. The biology and life cycle of this insect were studied in a laboratory and under
natural weather conditions. The results showed that similarly to Hessian fly, barley stem gall
midge has two feeding instars and a third non-feeding instar. The generation time was
longer for barley stem gall midge than for Hessian fly (45 vs 32 days at 18 ± 1°C, and a
12:12 (L: D) h photoperiod). The eggs of barley stem gall midge hatched in 7 days
compared to 4 days for Hessian fly. The largest discrepancy in developmental time was for
second instar and pupa. Second instars and pupae of barley stem gall midge required twice
as long as those of Hessian fly to develop and molt into next stage (12 vs. 6 days). The first
and third instars of barley stem gall midge also required a little bit longer to complete
development (9 and 10 days vs. 7 and 8 days for Hessian fly). Like for Hessian fly, barley
stem gall midge reproduces mostly by unisexual progenies. Four progeny classes were
observed; unisexual female progenies, unisexual male progenies, predominantly female
progenies, and predominantly male progenies. The proportion of unisexual female and male
progenies and the proportion of predominantly female and predominantly male progenies
were similar. Overall, the sex ratio of both species was about 1:1. Under field weather
conditions that prevail in the Chaouia region of Morocco, barley stem gall midge has two
complete generations and a third partial one. The first generation starts late October, and
ends late December. The second generation develops from January until early March. A
high proportion of third instars of this generation fail to pupate (35%). The third generation
is only partial; adults of the second generation emerge during March, oviposit and larvae
develop to third instars but all go into summer diapause.
Key words: Barley stem gall midge, Hessian fly, biology, life cycle.
RESUME
La cécidomyie à galle de l’orge, Mayetiola hordei (Keiffer), est le ravageur le plus
destructif de l’orge au Maroc. La biologie et le cycle de développement de l’insecte ont été
étudiés au laboratoire et sous des conditions climatiques naturelles. Les résultats ont montré
18
que similairement à la mouche de Hesse, la cécidomyie à galle de l’orge possède deux
stades larvaires qui s’alimentent et un troisième ne s’alimentant pas. Cependant, la durée de
génération était plus longue que celle de la mouche de Hesse (45 contre 32 jours à une
température de 18 ± 1°C et une photopériode de 12:12 heures (L:O)). Le stade œuf de la
cécidomyie de l’orge s’est développé en 7 jours au lieu de 4 pour la mouche de Hesse. La
plus grande différence dans la durée de développement fut enregistrée pour le deuxième
stade larvaire et le stade pupe. Ils ont nécessité deux fois plus de temps pour compléter leur
développement que pour la mouche de Hesse (12 contre 6 jours). Les premier et troisième
stades larvaires ont aussi nécessité un peu plus de temps; 9 et 10 jours pour la cécidomyie
de l’orge contre 7 et 8 chez la mouche du blé.
De même que pour la mouche de Hesse, la cécidomyie à galle de l’orge se reproduit
principalement par progénitures unisexuées. Quatre classes de progénitures ont été
observées; progénitures unisexuées femelles, progénitures unisexuées mâles, progénitures à
prédominance femelles, et progénitures à prédominances mâles. La proportion des
progénitures unisexuées femelles et mâles était similaire à celle des progénitures à
prédominance femelles et mâles, donnant ainsi un sexe ratio de 50:50.
Sous les conditions climatiques de la région de Chaouia, la cécidomyie à galle de l’orge
passe chaque année par 2 générations complètes et une troisième partielle. La première
génération commence en automne, vers fin octobre et s’achève vers fin décembre. La
deuxième s’étale entre janvier et mars. Une proportion pouvant arriver à 35% des individus
de troisième stade larvaire de cette deuxième génération ne passe pas au stade pupe, et
rentre immédiatement en diapause. La troisième génération est partielle; les adultes de la
deuxième génération émergent et procèdent à la ponte, mais les larves qui en sont issues se
développent jusqu’au 3eme stade larvaire, et rentrent toutes en diapause estivale, bouclant
ainsi le cycle de développement.
Mots Clés: Cécidomyie à galle de l’orge, mouche de Hesse, biologie, cycle de vie.
INTRODUCTION
Cereals are the major food and feed crops
in Morocco. They occupy more than 5
million hectares annually. Bread wheat is
grown over 2 million ha, durum wheat
over 1 million ha, and barley over 2
million ha. However, these crops are far
from nearing their yield potential because
of adverse weather conditions and
negative effects of biotic stress resulting
from attacks of Mayetiola species.
Mayetiola (Cecidomyiidae) is a paleartic
genus of gall midges that contains 29
species, all of which evolved on and are
restricted to particular genera and tribes
of the grass family Poaceae (Gramineae)
(Skuhrava 1986, Gagné & Jaschhof,
2014). Mayetiola species are mono-
phagous, restricted to one host, or
oligophagous, restricted to a few closely
related hosts. Adults do not feed, are
short-lived, and are narrowly adapted to
and synchronized with their hosts (Gagné
1989). Females spend most of their short
life-span searching for host plants and
laying eggs. Like some other plant-
feeding cecidomyiid groups, Mayetiola
females have preferences for hosts that
are suitable food for their offspring
(Harris & Rose 1989, Lhaloui 1995).
Among Mayetiola species, the Hessian
fly, M. destructor (Say) (H. fly) and the
barley stem gall midge, M. hordei
(Keiffer) (BSGM), are the most serious
pests of cereal crops. The H. fly has been
Lhaloui & al.
Revue Marocaine de Protection des Plantes, 2016, N° 9: 17-37
19
recognized for many years as a major
pest of wheat in the United States and
Morocco, and in many other wheat-
growing regions of the world (Jourdan
1938a, Barnes 1956, Miller & al., 1989,
Ratcliffe & Hatchett 1997, Lhaloui & al.,
2005). Originally from West Asia, the
Hessian fly has spread to several
countries of Europe, North Africa and
North America. The BSGM is indigenous
to Mediterranean countries. In Morocco,
losses caused by these pests have been
estimated to an annual average of more
than a third of the wheat and barley
yields (Lhaloui & al. 1992a), and could
amount to total crop loss when heavy
infestations coincide with young plant
tillers such as in the case of late seeding.
Studies conducted using Carbofuran
applications to keep H. fly and BSGM
free plots and compare their yield to that
obtained from infested plots, showed an
estimated 42% loss for bread wheat, 32%
for durum wheat, and 45 % for barley
(Lhaloui & al., 1992b). Similar studies
using near-isogenic H. fly
resistant/susceptible bread wheat lines
indicated an average 36% yield loss
(Amri & al., 1992).
On the other hand, surveys conducted in
Morocco between 1986 and 1990 showed
average infestation levels of 88, 85 and
80% of bread wheat, durum wheat, and
barley, respectively (Lhaloui & al.
1992b, Lhaloui & al. 2005). Recent
studies indicated that these pests are more
severe in drought prone areas, but are
omnipresent all over the cereal growing
regions of the country (Lhaloui & al.,
2014). Economically, losses dues to H.
fly were estimated at a value of 200
million DH per year on bread wheat in 5
major regions of Morocco. This indicates
that losses are much heavier when all
cereals and regions are included. The
same study revealed that investing in
research for developing resistant varieties
has an internal rate of return of 39%
(Azzam & al., 1997).
Because of the great economic
importance of H. fly, much is known
about the insect's biology, life cycle, and
bionomics relative to its hosts, and
several control methods have been
identified. The mechanisms of resistance
have largely been investigated. They are
mostly expressed as larval antibiosis
controlled by single partially or
completely dominant genes. So far, 34
Hessian fly resistance genes have been
identified (Li & al., 2013), and a large
number of wheat cultivars carrying
resistance to this pest have been released.
However, research on the BSGM is very
limited, although 3 barley cultivars
(Fleet, WPBS, and Gwylan) have been
identified as carrying antibiosis to H. fly
(Lhaloui & al., 1996). No resistance has
so far been identified in cultivated barley
for the BSGM, but two wild accessions
of H. bublbosum were reported as
carrying antibiosis to this pest (Lhaloui,
1995).
The BSGM has long prevailed as a
destructive pest of barley in the barley-
growing regions adjacent to the
Mediterranean Sea, particularly in North
Africa (Roberti 1953, Alfaro 1955,
Lhaloui & al., 1992b, Lhaloui & al.,
2000, Lhaloui & al., 2005). Although
now recognized as a distinct species, M.
hordei [=M. mimeuri (Mesnil)], the
taxonomic status of the BSGM had been
in question since it was described as M.
mimeuri (Mesnil 1934). Mesnil believed
that M. mimeuri was a new species
different than H. fly that attacks not only
barley but also wheat and oats. Mesnil
also believed that H. fly did not occur in
Morocco. Later, Balachowsky and
Mesnil (1935) using illustrations to
describe the differences between M.
mimeuri and M. destructor, concluded
20
that M. mimeuri was a pest of both wheat
and barley in Morocco and Algeria, but
caused galls only on barley. Jourdan
(1937, 1938b) compared the biology of
Mayetiola specimens combined from
wheat and barley in Morocco to
Mayetiola in Europe and found no
difference between the two populations.
In another paper, Jourdan (1938a)
compared morphological characters of
larvae and adults taken from various
fields of wheat and barley in Morocco.
Based on illustrations of male genitalia
and posterior segments of larvae, he
concluded that the variations observed
were too small to give any clear-cut
differences between the descriptions of
M. mimeuri and M. destructor provided
by Mesnil (1934). He rejected the notion
that M. mimeuri was a distinct species
and concluded that M. destructor was a
largely variable species that occurred in
Morocco as well as in Europe. The
results of Jourdan (1938a) were later
supported by Hudault & Zelensky (1939),
who stated that M. destructor was a pest
of both wheat and barley, but galls were
only formed on barley.
To check their hypothesis, Hudault &
Jourdan (1954) made crosses between
Mayetiola adults reared from wheat and
barley and found that females reared
from wheat mated with males reared
from barley, and vice versa, and
produced viable offspring. They
concluded that since flies were
interfertile, they may be the same species.
Later, Coutin & al., (1974) found that
Mayetiola adults from wheat and barley
were not interfertile. Moreover, they
reported that the puparia from barley
were more variable and corresponded to
either M. destructor or M. mimeuri, while
puparia from wheat always corresponded
to M. destructor. They concluded that
Mayetiola on wheat and barley
represented at least two well isolated
biotypes.
Outside of Morocco, Roberti (1953)
presented accurate illustrations of Italian
Mayetiola spp. from wheat and barley.
He conclusively demonstrated that
specimens from wheat (as M. destructor),
and from barley (as M. mimeuri) were
distinct. Alfaro (1955) also demonstrated
the existence of two distinct species, M.
destructor on wheat, and M. mimeuri on
barley in Spain. Barnes (1956) treated M.
mimeuri as a separate species that infests
wheat and barley in North Africa, but
doubted its validity. He also questioned
the findings of Roberti (1953). Finally,
Ertel (1975) classified M. mimeuri among
species of uncertain origin; and Shuhrava
(1986) listed it as a synonym of M.
destructor.
In their study, Gagné & al., (1991)
redescribed the Moroccan Mayetiola
species from wheat and barley with fine
illustrations of the spicules of the
posterior abdominal sternites of puparia,
the shape of the female postabdominal
tergites, and the shape of male genitalia.
They demonstrated conclusively that
Mayetiola populations on wheat and
barley in Morocco are two distinct
species that are sympatric in the major
cereal growing regions. The BSGM
infests barley but not wheat, whereas the
H. fly infests wheat and, to a lesser
extent, barley. Gagné & al., (1991) also
noticed that M. hordei puparia were
always embedded in galls and associated
with plant stunting, whereas H. fly
puparia were associated with plant
stunting but caused no stem swellings.
No intermediates were found; all
specimens collected clearly belonged to
one or the other species. Gagné & al.
(1991) concluded that BSGM, the
dominant species on barley, rarely
reproduces on wheat and may be host
specific to barley and other Hordeum
Lhaloui & al.
Revue Marocaine de Protection des Plantes, 2016, N° 9: 17-37
21
species, while H. fly has a distinct
preference for wheat, but can also
reproduce on barley. Because the
Mayetiola species found on barley was
first described by Keiffer (1909) and
given the name of M. hordei (Keiffer),
Gagné & al.,(1991) resurrected the name
M. hordei and considered mimeuri as a
junior synonym of hordei.
Gagné & al. (1991) stated that the
taxonomic confusion of Mayetiola
species was created by failure of earlier
authors to correctly identify the hosts of
specimens or isolate specimens from
individual host plants. Also, failure to
recognize that the BSGM and the H. fly
may occur together on barley led to
erroneous conclusions concerning species
variability and host preference.
Therefore, much of the information
previously published on the biology and
life cycle of the two species on barley in
North Africa may be invalid (Gagné &
al., 1991).
The objectives of this study were 1) to
redefine the biology and life cycle of
BSGM in the field and under controlled
environmental conditions, 2) compare the
developmental time of life stages of the
BSGM and H. fly, 3) determine the sex
ratios of BSGM and H. fly, and 4)
determine the number and durations of
the generations.
MATERIALS AND METHODS
The experiments were conducted at the
National Institute of Agronomic
Research, Regional Center of Settat,
INRA-CRRA-Settat, Morocco. BSGM
females used in the tests conducted under
controlled environmental conditions were
obtained from a pure culture that had
been reared in isolation on 'Tamelalt'
barley in a greenhouse. The culture had
been purified by rearing individual
progenies of single females on barley for
three generations and selecting only
individuals that produced galls. Females
used for the tests conducted under natural
weather conditions emerged from
infested barley stubble and plants
collected from the field at the Jemaa
Shaim Experiment Domain. H. fly
females were also obtained from a pure
culture that had been reared in isolation
for two generations on 'Nesma' wheat in a
greenhouse.
Description of Life Stages and
Generation Time of Barley Stem Gall
Midge under Controlled Environmental
Conditions.
To study the life stages of the BSGM,
'Kanby', a susceptible barley, was seeded
in a standard wooden flat (54 x 36 x 8
cm) containing a mixture of 1/3 peat and
2/3 soil, at a rate of 10 rows per flat and
50 seeds per row. The flat was kept in a
greenhouse, and when the plants were at
the one or two-leaf stage, the flat was
moved to an environmental chamber
programmed for 18 ± 1°C and a 12:12
(L:D) h photoperiod, with the photophase
from 0600 to 1800 h. The flat was caged
with a cheesecloth tent and about 200
newly emerged and mated females were
released under the tent. Releases were
made between 0830 and 0900 h. To
obtain offspring of similar age, females
were allowed to oviposit for 8 h then
removed. Relative humidity was not
controlled in the environmental chamber,
but the flat was watered regularly to
provide adequate moisture for the plants
and maintain high humidity.
Starting the third day after infestation, 10
plants were randomly selected and
removed daily from the flat. Plants were
examined under a microscope (10x) to
determine the number of eggs laid on the
adaxial and the abaxial leaf surfaces and
22
the stems. For the first and second
instars, plants were dissected and the
number of larvae on each plant was
recorded. The size (length) of larvae was
measured using an ocular micrometer.
For third instars and pupae, a dissecting
needle was used to remove the puparia
and the number and development stage of
each stadium were recorded. When adults
began to emerge, they were removed
daily from the flat. When adult
emergence ceased, plants that remained
in the flat were removed, and the puparia
were dissected to determine the number
of third instars that had not pupated.
Comparative Developmental Time of
Life Stages of Barley Stem Gall Midge
and Hessian fly.
From earlier field observations (Lhaloui
&al. 1992b), it was noted that the life
cycle of BSGM was somewhat longer
than that of H. fly. The objective of this
study was to compare the developmental
time of the life stages of both species.
'Nesma', a wheat cultivar susceptible to
H. fly, and 'Kanby', a barley cultivar
susceptible to BSGM, were seeded in
separate standard greenhouse flats at a
rate of ten rows per flat and fifty seeds
per row. Flats were kept in a greenhouse
until plants were at the two-leaf stage.
Flats were then moved to an
environmental chamber programmed for
18 ± 1°C and a 12:12 (L:D) h photo-
period, with the photophase from 0600 to
1800 hours. Flats were caged with
cheesecloth tents, and about 200 newly
mated H. fly females were confined for
oviposition on wheat, and 200 BSGM
females were confined for oviposition on
barley. Females were allowed to oviposit
for only eight hours to obtain eggs of
similar age. Starting on the third day after
infestation, random samples of 10 plants
were taken daily from each flat. The
plants were examined under a
stereoscopic microscope (10x) and the
number of eggs on the leaves and the
stems and the number of larvae and their
developmental stages were recorded. At
the end of the experiment, data were
interpreted to estimate the developmental
time of the egg stage, feeding-stage
larvae (first and second instars), and the
non-feeding or puparial stage (third instar
and pupa).
Estimation of maximum potential
fecundity and achieved fecundity
To estimate the maximum potential
fecundity of the two species, 50 females
each of H. fly and BSGM were randomly
collected 15 to 20 minutes after eclosion,
placed individually in petri dishes
containing moistened filter paper, then
dissected under a stereoscopic
microscope (10x). The number of eggs in
the ovaries of each female was counted.
The eggs were crushed as they were
counted to avoid errors.
To estimate the achieved fecundity, post
reproductive females were dissected and
examined for eggs that remained in their
ovaries. The difference between the
maximum potential fecundity and the
number of eggs remaining in the ovaries
of spent females was used to estimate the
achieved fecundity.
Determination of Sex Ratios of Barley
Stem Gall Midge and Hessian fly.
The sex ratio of H. fly has been
extensively investigated in the United
States (Painter 1930, Gallun & al. 1961,
Stuart & Hatchett 1991). The H. fly
reproduces by unisexual families; most
progenies are either all males or all
females. Families of bisexual
predominantly female or predominantly
male progenies are produced at low
frequencies. However, the sex ratio of
BSGM has not been studied. Although
the sex ratio is species specific and the
sex ratio of H. fly in Morocco should be
Lhaloui & al.
Revue Marocaine de Protection des Plantes, 2016, N° 9: 17-37
23
similar to that of H. fly in the United
States, where it has already been studied,
the sex ratio of the Moroccan H. fly was
investigated for comparison with that of
BSGM.
To determine the sex ratio of BSGM,
single newly mated females were
confined individually on seedlings of
'Kanby' barley grown in small plastic
pots. Pots were covered with clear plastic
cages having a cheesecloth top for
ventilation and placed in an
environmental chamber programmed for
18 ± 1°C and a 12:12 (L:D) h
photoperiod with the photophase from
0600 to 1800 hours. The females were
allowed to oviposit until they died. The
pots were caged throughout the
experiment. When adults began to
emerge, they were removed from the
cages daily, counted, and sexed. The
progenies of 200 randomly mated
females were examined. Data were
analyzed to determine the sex ratios for
each progeny and the proportion of the
progenies that were unisexual or
bisexual.
To determine the sex ratio of H. fly, the
same experiment was repeated confining
single mated females of H. fly on
‘Nesma’ wheat seedlings for oviposition.
Data were recorded and the progenies
were classified in the same way as
described for BSGM.
Duration of Life Cycle and Number of
Generations of BSGM under Field
Weather Conditions.
This experiment was conducted to
determine the duration of the life cycle
and the number of BSGM generations per
year under natural weather conditions.
Females used in this experiment emerged
from infested barley stubble and plants
collected from the field. Barley stubble
infested with puparia was collected from
the field in early October, taken to the
laboratory and examined for BSGM
puparia. Puparia not embedded in galls
were removed from the stems.
Afterwards, the infested stems were
placed in empty wooden flats and
covered with cheesecloth. The flats were
placed outdoors and exposed to natural
weather conditions. The stubble was
sprinkled daily with water to prevent
puparia from desiccating.
After the first significant rainfall in mid-
October, adult emergence of the
oversummering generation was
monitored daily in the collected stubble
and by examining newly emerged barley
seedlings in the field for eggs. At the
same time, 'Kanby' barley was seeded in
standard wooden flats and grown in a
greenhouse. When first eggs were
observed on field plants, three flats of
barley in the one-or two-leaf stage were
placed outdoors, near the greenhouse.
The flats were caged with a cheesecloth
tent, and the newly mated females that
emerged from the stubble were collected
and confined for oviposition on the
plants. To simulate natural conditions,
the flats were infested over 5 days and
females were allowed to oviposit until
they die. A total of about 200 females
were confined for oviposition on each
flat. The flats were kept caged throughout
the experiment to prevent infestation
from field populations of Mayetiola
species. Plants were exposed to all
natural weather conditions, although flats
were watered as needed to maintain
healthy plants.
Starting on the third day after infestation,
plants were sampled for eggs and larvae.
When adults of this generation began to
emerge, they were removed from the flats
each morning to prevent new oviposition.
At the same time, a new set of three flats
24
seeded to barley were again taken out of
the greenhouse and placed close to the
first set. Also infested barley plants were
again collected from the field and
examined to eliminate all puparia that
were not associated with galls. Plants
were placed in flats and observed for
adult emergence in the same way as
described for the oversummering
generation. Females that emerged from
these plants were used to infest the new
set of flats. Plants were infested,
sampled, and observed in the same way
as described for the first generation. Data
were taken in the same way as described
previously.
At the end of the second generation, three
other flats seeded to barley were again
taken out of the greenhouse and placed
close to the first flats. Plants of the new
flats were infested and sampled and data
were recorded in the same way as
described for the second generation.
These data were used to describe the
third generation.
For all three generations, after the peak of
adult emergence, the plants remaining in
the flat were removed and dissected in
the laboratory to estimate the number of
third instars that did not emerge (went
into diapause). This experiment was
repeated over 3 seasons, representing
average weather conditions of the
Chaouia region. Data is summarized in
this work.
Statistical analysis
All Data were analysed using proc GLM
(SAS Institute). Angular transformation
was performed on all the percentages,
pre-transformed data is reported. Means
were separated using Fisher's Least
Significant Difference (LSD) test at
P=.05.
RESULTS AND DISCUSSION
Description of Life Stages and
Generation Time of Barley Stem Gall
Midge under Controlled Environmental
Conditions.
Description of Egg Stage
Eggs of BSGM are very similar in
appearance to H. fly eggs. The egg is
approximately 0.5 mm in length, slender,
glossy, and pale red in color, becoming
deeper red near eclosion. Eggs are laid in
the grooves between the longitudinal
veins of leaves. Larvae that eclose from
eggs laid on the adaxial leaf surface
migrate down behind the leaf sheath to
the base of the stem where they feed.
Under the environmental conditions of
this experiment, a few eggs hatched 7
days after oviposition and neonate larvae
were observed migrating down the leaves
and stems, but none had reached the base
of the stem. Most of the eggs hatched 8
days after oviposition (Table 1).
Description of Feeding-Stage Larvae
First instar.
At eclosion, first instars are the same size
and color as the eggs. After eclosion,
neonates were observed crawling down
the leaves, guided by the grooves
between the leaf veins. When larvae
reached the leaf sheath, they moved over
or around the sheath collar and crawled
behind and downward between the leaves
until they reached the base of the stem
where they began to feed. Some first
instars were not able to get beyond the
leaf ligule and were found dead at this
site. Also, many larvae were found dead
on the outside surface of the stem. These
larvae eclosed from eggs that were either
laid on the stem itself or on the abaxial
leaf surface. The first instar required
about 9 days to complete development
(Table 1) and most larvae molted to
Lhaloui & al.
Revue Marocaine de Protection des Plantes, 2016, N° 9: 17-37
25
second instars 10 days after they eclosed
from the eggs. After the first 3 days of
feeding, first instars turned completely
white and were about 1.0 mm in length
(Fig. 1). The larvae gradually increased
in size and reached about 1.4 mm in
length as full-grown first instars. At this
time, a small depression and a
discoloration of plant cells were observed
at the feeding sites, but larvae were not
firmly attached to the plant tissue.
Second instar.
Newly molted second-instar larvae
measured 1.6 to 1.8 mm, but soon after
molting, they increased in size to about
2.0 mm. Also, these larvae had deep, well
defined metameres, but became
completely smooth and cylindrical after 3
to 4 days of feeding. Depending on larval
density, second instars gradually
increased in size and were 2.5 to 4.0 mm
in length. The second instars completed
development in 11 to 12 days. During
this stadium, gall tissue gradually formed
around the larvae and each larva became
completely embedded in a pea-sized gall.
Second instars were also able to survive
on leaves. Apparently, some first instars
initiate feeding on leaves while still
enclosed inside the whorl. As these
leaves grow, larvae are carried upward
with the emerging leaf and continue to
feed and develop normally. These larvae
also formed galls on leaves. The gall
tissue may protect the exposed larvae
from desiccation which allows the larvae
to survive and develop on the leaves. H.
fly larvae have never been reported to
survive on leaves.
Second instars of BSGM are also
morphologically similar to the second
instars of H. fly when observed with the
naked eye. But microscopic examination
revealed that the second instar of BSGM
has no spicules on the anterior abdominal
sternites, whereas the second instar of H.
fly has dense spicules. These findings
suggest that the almost complete lack of
spicules on BSGM larvae may explain
why larvae adhere tightly to the plant
tissue (Gagné & al., 1991).
Description of Non-feeding Stage.
This stage contains the third instar and
the pupa, both of which are enclosed in a
puparium (the hardened cuticle of the
second instar), thus the name flaxseed
given to this stage.
Third instar.
This instar had well defined segments
and was shorter than the second instar,
measuring 2.5 to 3.5 mm (Fig. 1). Similar
to that observed for H. fly third instar, the
larva reverses its position in the puparium
so the adult will be oriented head upward
for emergence and escape from the plant.
Most nondiapausing third instars
developed into pupae 10 days after they
molted (Table 1). About 7% of the larvae
failed to pupate. This suggests that even
in a favorable environment, a small
proportion of third instars enter diapause.
This behavior may be a genetic trait that
prevents all individuals of a specific
brood from emerging. Diapausing third
instars may survive more than a year and
pupate only during the next favorable
cropping season. The same behavior has
also been observed for Hessian fly
(McColloch 1930, Painter 1930). The
termination of diapause in cecidomyiids
is usually well timed to the host's biology
(Gagné 1989).
Pupa
The developmental period for the pupa
was about 12 days. During this time, the
pupa gradually transforms into an adult.
The puparium of the BSGM (being the
second instar cuticle) also differs from
that of H. fly by the absence of spicules
at the posterior ventral end (Gagné & al.
26
1991). The puparia of H. fly are covered
entirely with spicules. The lack of
spicules allows the puparia to adhere
tightly to the plant tissue, in contrast to
puparia of H. fly which readily come
loose from plant tissue (Gagné & al.,
1991). This difference in puparia
attachment to plant tissue is very reliable
in distinguishing the two species without
having to utilize a microscope.
Adult
Adults of the BSGM resemble adults of
H. fly in many ways. They are grey and
have a mosquito-like form. The adults do
not feed and are short-lived. Mated
females live for 2 to 3 days, although
unmated females may live for 5 to 7
days. Males also live for 4 to 7 days.
Males have two peaks of eclosion; some
eclose in the afternoon between 1600 and
1800 h and some eclose the next morning
at the same time as the females. Females
eclose in the morning between 0700 and
0930 h. If males are present, mating may
occur within 30 to 60 minutes after
eclosion. After mating, females sit for
two to four hours before they start
ovipositing. The oviposition period
usually lasts over two days (Lhaloui
1995). BSGM adults can be readily
distinguished from H. fly adults in the
morphology of the gonostyli in males and
the morphology of the sixth through
eighth abdominal tergites in females
(Roberti 1953, Alfaro 1955, Gagné & al.,
1991).
Results indicated that the generation time
for non-diapausing BSGM (from egg to
adult) is about 45 days at 18 ± 1°C, and
12:12 (L:D) h photoperiod. However,
adult emergence occurred over an
extended period after peak emergence.
Adults continued to emerge for more than
one month after peak emergence, which
indicates that third instars vary
considerably in their developmental time.
The condition of the plant and the site on
the plant where the second instar feeds
may play a role in the duration of third
instar development. It was noted that
when larvae were present at high
densities (10 to 15 larvae per plant) and
plants were in poor condition, the larvae
developed into third instars and pupae
much faster than when larvae were at low
densities and plants were in good
condition. Similar results were described
by El Bouhssini & al. (1996) who
reported that growth and development of
H.fly larvae are density dependant.
Table 1. Duration of Developmental Stages of Barley Stem Gall Midge.
Stage or instar No. days to complete development
Egg 7.2 ± 0.5 d*
First instar 8.7 ± 0.7 c
Second instar 11.7 ± 0.8 a
Third instar 10.1 ± 0.8 b
Pupae 11.6 ± 1.1 a
Adults Females 5-7
a
Males 4-7
a
*Means ±SD, No. of days for instars (stages) to complete development and molt into next instar
(stage). Means within the column followed by the same letter are not significantly different (Fisher's
Least Significant Difference (LSD) test. P = 0.05 [SAS Institute]).
aNumber of days adults lived.
Lhaloui & al.
27
Comparative Developmental Time of
Life Stages of BSG Midge and H. Fly.
Egg Stage.
Under the conditions of the experiment,
70% of the eggs of H. fly developed and
eclosed into first instars in 4 days, and by
the next day, 100% of the fertile eggs had
eclosed and first instars had migrated to
their feeding position. Eggs of barley
stem gall midge took longer to complete
their development. Ninety-two percent of
the eggs eclosed after 7 days of
development and the remaining eggs
eclosed on the next day (Fig. 1 & 2).
First instar.
The developmental time of first instars of
both species were significantly different
(Fig. 1 & 2). A few first instars of H. fly
molted to second instars 7 days after egg
eclosion, and 100% of the larvae had
molted 8 days after egg eclosion. Gagné
& Hatchett (1989) reported that at 20 ±
1°C the developmental period of the first
instar was 6 to 7 days. For BSGM, 92.5%
of the first instars reached second instars
10 days after egg hatch and about 10%
after 9 days (Fig. 1 & 2).
However, first instars of both species
increased in size to 1.5 mm before they
molted into second instars. Neonates of
both species grew to almost twice their
size after feeding for 3 days. At this time,
they became translucent white and lost
their reddish color. Larvae became more
cylindrical and their body segments were
less distinct. Second instar.
At 20°C, Gagné & Hatchett (1989)
reported that the second instar developed
over 4 to 5 days. Second instars of
BSGM developed over 12 days (twice as
long as for H. fly). These results indicate
that under the environmental conditions
of this experiment, the feeding stage of
BSGM lasts from 20 to 21 days, while
that of H. fly lasts for about 14 days (Fig.
1 & 2).
The Non-feeding Stage.
Third instar.
H. fly third instars developed over a
period of 8 days. BSGM third instars
developed over a period of 10 days.
Larvae of both species reversed their
position inside the puparia, so the
emerging adults would be oriented with
their heads upwards (Fig. 1 & 2).
Pupa.
The pupal stage took 6 days to complete
development for the H. fly, while the
pupal stage of the BSGM required 12
days (Table 4). These results indicate that
like for the feeding stage, the non-feeding
stage of BSGM develops over a longer
period than that of H. fly (22 vs. 14
days). (Fig. 1 & 2).
In summary, at a constant temperature of
18 ± 1°C, 12:12 (L:D) h photoperiod,
BSGM requires 45 days to develop from
egg to adult, but the H. fly requires only
32 days. The largest difference in the
developmental time was recorded for the
egg stage, the second instar, and pupa.
Second instars of H. fly developed over 6
days and the cuticles became brown on
the seventh day (puparia).
28
Comparative duration of development time of life stages of Barley Stem Gall Midge
and Hessian fly
4,1
7,1
6,2
7,9
5,6
7,1
8,9
11,5
10,3
11,8
0
1
2
3
4
5
6
7
8
9
10
11
12
13
Egg L1 L2 L3 Pupa
Life Stages
No. Day s
Hessian fly
Barley stem gall midge
Figure1. Comparative duration of developmental time of life stages of BSGM and H. fly at
18 ± 1°C and 12:12 (L:D) h photoperiod
Figure 2. Development of eggs and instars (L1, L2, and L3) and size (length) of instars of
BSGM and H. fly.
Distribution of Eggs on Host Plants.
BSGM and H.fly females have very
different behaviors in selecting
ovipositional sites on their host plants.
BSGM females deposited 61.5% of their
egg complements on the adaxial leaf
surface, 20.8% on the abaxial surface,
and 17.7% on the stem. In contrast, H. fly
females laid 91.4% of their egg
complements on the adaxial leaf surface,
7.1% on the abaxial surface and only
1.5% on the stem (fig. 3). This indicates
Lhaloui & al.
29
that, unlike H. fly females, BSGM
females lay a high proportion of their
eggs on the abaxial leaf surfaces and
stems of their hosts. Thus, BSGM
females have a much lower ovipositional
efficiency than H.fly because only first
instars from eggs laid on the adaxial leaf
surface survive. BSGM females are less
able to discriminate between the adaxial
and the abaxial leaf surface or the stem as
ovipositional sites than H. fly females.
BSGM females laid about 40% of their
total egg complement either on the
abaxial leaf surface or on the stem.
Larvae emerging from these eggs would
crawl down to the ground and perish.
These results corroborate those described
by Ming & al. (2009) that indicate that
Barley is a less suitable host for H. fly
and that a high proportion of eggs is laid
on the abaxial leaf surface and the stem.
Tamer & al., (2015) also showed that
BSGM populations in Syria lay a high
proportion of their egg complement on
the abaxial leaf surfaces and stems of
barley.
Figure 3. Comparative distributions of Barley stem gall midge and Hessian fly eggs on host
plants
Fecundity.
The maximum potential fecundity of
BSGM was 190.2 ± 81.3 eggs per female
and significantly lower than the fecundity
of H. fly, which averaged 230.1 ± 61.4
eggs per female (Table 2). For both
species, the actual fecundity was the
same as the maximum potential
fecundity. Dissection of post-
reproductive females (spent females)
revealed that no significant numbers of
eggs remained in the ovaries. A few
females still carried one or two eggs, but
most had none. Harris and Rose (1989)
also reported that H. fly females lay their
full egg complement before they die.
Table 2. Maximum Potential Fecundity of Barley Stem Gall Midge and Hessian fly.
Species of Mayetiola Barley stem gall midge Hessian fly
Mean no. of eggs 190.2 ± 75.91 b* 230.1 ± 61.4 a
*means ± SD. Means within the row followed by the same letter are not significantly
different [Fisher's Least Significant Difference (LSD) Test at P=0.05 (SAS Institute)].
Distribution of Barley Stem Gall Midge Eggs on host
plants
61%
21%
18%
% eggs laid on adaxial
surface
% eggs laid on abaxial
surface
% eggs laid on ste m
Distrubustion of Hessian fly Eggs On host plants
91%
7% 2%
% eggs laid on adaxial
surface
% eggs laid on abaxial
surface
% eggs laid on stem
30
Sex Ratios of Barley Stem Gall Midge
and Hessian fly.
BSGM.
Results revealed that like many other
cecidomyiids, the BSGM breeds mostly
by unisexual progenies. Four progeny
classes were observed. Of the 189
progenies examined, 64 (33.9%) were all
female progenies, 60 (31.8%) were all
male progenies, 36 (19.1%) were
predominantly female progenies, and 29
(15.3%) were predominantly male
progenies. Of the unisexual progenies,
about half were female (51.6%) and half
were male (48.4%). Similarly, 55.4% of
the bisexual progenies were
predominantly female progenies and
44.6% were predominantly male
progenies (Tables 3 & 4). The mean
number of females per female progeny
was similar to that of males in the male
progenies. The average number of males
in the predominantly female progenies,
and number of females in the
predominantly male progenies were also
similar (Table 3). In general, females
produced an average of 54.2 adults per
progeny; and overall, 54.4% of all
individuals were females, and 45.6%
were males. This indicates that even
though BSGM reproduces mostly by
unisexual progenies, the sex ratio is about
1:1. H. fly.
The sex ratio of H. fly was similar to that
observed for BSGM. Of the 196
progenies examined, 75 (38.3%) were all
female progenies, 62 (31.6%) were all
male progenies, 31 (15.8%) were
predominantly female progenies, and 28
(14.3%) were predominantly male
progenies. Like for BSGM, about half of
the unisexual progenies of H. fly were
female (54.7%), and half were male
(45.3%). Also, 52.5% of the bisexual
progenies were predominantly female
progenies and 47.5% were predominantly
male progenies (Tables 3 & 4). The
average number of females per female
progeny was similar to that of males per
male progeny. The average number of
males in the predominantly female
progenies and number of females in the
predominantly male progenies were also
similar (Table 3). Overall, females
produced an average of 63.1 adults per
progeny; and of the total number of
individuals produced by all females,
56.5% were females, and 43.5% were
males, indicating that the sex ratio was
also about 1:1.
Overall, results showed that the sex ratio
of BSGM is similar to that of H. fly.
BSGM also breeds mostly by unisexual
progenies and has a sex ratio of about
1:1. These results corroborate those
described earlier by many authors on H.
fly in the United States (Gallun & al.,
1961; Stuart & Hatchet 1991).
Table 3. Sexual characteristics (numbers and sex of adults) of progenies of randomly mated
females of Barley Stem Gall Midge and Hessian fly in Morocco.
Progeny Class
Mayetiola
Species Unisexual progenies Bisexual progenies*
Female Male No. female > male No. male > female
Barley Stem
Gall Midge 57.1 ± 18.3a 52.8 ± 16.9 47.6 ± 17.5 > 5.8 ± 3.5 44.7 ± 19.4 > 7.1 ± 4.2
Hessian fly 68.1 ± 22.4 58.9 ± 15.1 51.7 ± 15.9 > 7.2 ± 3.1 53.6 ± 19.9 > 9.8 ± 4.8
*Female > male designates predominantly female progenies; male > female designates predominantly
male progenies.
aNumbers represent mean ± SD of individuals per progeny
Lhaloui & al.
31
Table 4. Frequencies (percentages) of progeny classes of randomly mated females of Barley
Stem Gall Midge and Hessian fly progenies in Morocco
Progeny Class
Mayetiola Species Unisexual progenies Bisexual progenies*
% Female
progenies % Male
progenies % progenies with
No. female > male % progenies with
No. male > female
Barley Stem Gall Midge 51.6
a
48.4 55.4 44.6
Hessian fly 54.7 45.3 52.5 47.5
*Female > male designates predominantly female progenies; male > female designates
predominantly male progenies.
aNumbers represent percentages.
Duration of Life Cycle and Number of
Generations under Field Weather
Conditions.
Under the prevailing weather conditions
of the Chaouia region of Morocco,
BSGM has three generations, two
complete and a third partial one.
First generation.
The first generation starts late October,
about two weeks after the first significant
rainfall. The first infested barley
seedlings are observed in the field at the
end of October. However the rate of adult
emergence and seedling infestation is
very slow. The peak of adult emergence
in the field and collected stubble was
observed during the second week of
November. Sampling of infested plants
showed that 100% of BSGM population
was in the egg stage until mid-November
when the first egg eclosion occurred.
First instars were observed for about two
weeks, until the end of November. Few
larvae developed into second instars
around November 25 (2.1%), and the
percent of second instars in the
population increased and reached 100%
around the end of November. For about a
week, all the population was in the
second instar. The earliest third instars
were observed by the end of first week of
December. However, not all second
instars completed development at the
same time; many required a longer
developmental time and were observed
20 days after the first third instar was
observed. Gradually, the population of
second instars decreased and that of third
instars increased. This suggests that in
addition to the five days difference in age
that the population started with at the egg
stage, second instars had different growth
rates. The exposure to fluctuating day
and night temperatures, the various larval
densities, and the condition of the plants
on which larvae were feeding may have
been the major factors affecting the
growth rate of these larvae. The
developmental time of third instars were
also stretched over a long period. Even
though the highest percent of third instars
was observed from second to third week
of December, third instars were observed
all through the generation time and after
one hundred days since infestation
(around mid February), about 6% of the
population was still as third instars that
failed to emerge. The first pupa was
observed on mid December, and the first
adult emerged at the end of December.
Adult emergence peaked during the
second week of January (Fig. 4).
Likewise, the pupal stage and adult
emergence were stretched out over a long
period. Adults emerged for about a
month after the peak emergence
occurred. The remaining plants were
examined by the end of June, and results
32
showed that about 6% of the population
was still at the third instar.
Figure 4: Developmental time for first generation of the barley stem gall midge in the
Chaouia region, Morocco.
Second generation.
The second generation started early
January. The peak of first generation
adult emergence in the field was
observed during the second week of
January. Infested plants were collected
from the field and adults that emerged
from these plants were used to infest
three new flats.
The earliest first instars of the second
generation were observed starting the
third week of January, about 11 days
after infestation. This indicates that eggs
required longer to complete development
under the colder temperatures and shorter
days of January than under the warmer
temperatures of November. Most eggs
eclosed during the fourth week and by
the end of January, 100% of the
population was in the first instar. First
instars developed for about 10 days; and
individuals issued from the earliest
eclosions turned into second instars by
about February 10. However, first instars
are observed until about the end of third
week of February. These individuals may
have issued from later infestations (eggs
laid by late emerged adults). At this time,
all larvae in the experiment had turned
into second instars. The earliest third
instars were observed starting fourth
week of February. But most second
instars developed over a longer period
than during the first generation; few were
observed until mid-March, thus required
about one month to complete
development (Figure 5). Like discussed
for the first generation, the
developmental time of third instars was
stretched over a long period, and about
80% of the population was in the third
instar by mid march, the other 20% were
already in the pupal stage. The first pupae
were, however, observed during first
week of March, and the first adults
emerged at the end of second week. By
the end of March, all pupae had turned
into adults and adult emergence stopped
completely. All larvae that remained in
the plants were third instars that failed
to pupate, and apparently went into
Lhaloui & al.
33
diapause. The examination of the puparia
by the end of April revealed that
aboutone third of the population were in
the third instars. These constitute the
proportion of individuals that did not
emerge as adults.
Figure 5. Developmental time for second generation of the barley stem gall midge in Settat
region, Morocco.
Third generation.
Since the second generation adults were
abundant during fourth week of March,
plants designated to study the third
generation were infested during the end
of third week. The eggs of this generation
eclosed in 7 to 8 days like for those of the
first generation. First instars were
observed from late march until mid April,
when almost 100% of the population
turned into second instars. The earliest
second instars were, however, observed
at the end of first week of April. The
earliest third instars were observed
starting the third decade of April, and
near the end of April, more than 85% of
the population was in the third instar.
Unlike for the first two generations, the
growth rate of second instars was less
stretched out in time. All the population
turned into thirds instars by the end of
April. Also all third instar failed to
pupate; none developed into pupae
(Figure 6). This indicates that third
instars of this generation all go into
summer diapause. Plants of this
generation were examined through the
end of June, and results revealed that all
individuals were third instar. This
indicates that all larvae of the third
generation would diapause as third
instars, and not resume development until
the next fall, when the environmental
conditions are favorable for the host
growth. However, the rate of parasitism
started building up from early May and
reached a mean of 64.2% of the
population by the end of June. Only
35.8% of the population was not
parasitized (third instars). The
examination of the puparia collected
from the field just before emergence of
adults of the oversummering generation
revealed that 8.7% of the puparia existing
on all stems had either third instars or
pupae, the remaining puparia were
34
empty, and had either BSGM adult
emergence splitting, or parasite
emergence holes.
In the field, it was noticed that the third
generation of barley stem gall midge was
very light; only very rare larvae were
found on the youngest barley tillers. This
could mainly be explained by the fact
that most barley plants were in the full
maturity phase by the end of March,
when adults of the second generation
were emerging. In Morocco, barley
cultivars grown in the coastal plains have
spring growth habits, and mature
completely by late April. Oversummering
larvae of barley stem gall midge
terminate diapause and resume
development only in the following fall
after the first significant rainfall, when
barley seedling of new barley crops or
volunteer barley, are emerging in the
field.
Figure 6. Developmental time for third generation of barley stem gall midge in Settat
region, Morocco.
In summary, these results clearly show
that the life cycle of the BSGM is very
well synchronized with its host, barley.
Gagné (1989) has reported that in deed,
the life cycle of all Cecidomyiids is very
well synchronized with that of their
hosts. In the field, the peak of adult
emergence of the oversummering BSGM
generation was observed when barley
seedlings were emerging in the fall, after
the first significant rainfall. This behavior
shows that BSGM is closely linked to its
host, barley, and is active in the field only
when this host is available (Gagné & al.,
1991). Similar behavior was reported for
H. fly, demonstrating host specificity of
this pest (Harris & Rose 1989). The
timing and duration of the BSGM
developmental generations were also
similar to those described for H. fly
(Coutin 1974, Lhaloui 1986, Lhaloui &
al., 2005), as both wheat and barley
grown in Morocco have similar
physiology and habits; both are spring
crops with winter habits, seeded in the
fall. BSGM and H. fly are sympatric
species of these two crops in Morocco
(Gagné & al., 1991).
CONCLUSION
This study revealed several
developmental similarities between the
BSGM and H. fly. Like for H. fly, the
Lhaloui & al.
35
BSGM has 2 feeding instars and a third
non-feeding one, reproduces mostly by
unisexual progenies, and has a sex ratio
of about 1:1. The BSGM also develops
over 2 complete generations and a third
partial one because most barley matures
by late April and is no longer a suitable
host. However, few discrepancies were
recorded; some life stages take longer to
grow and complete development than for
H. fly
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