Relationship between female size, type of egg mass deposited, and description of the oviposition behavior of the sibling species Tabanus nigrovittatus and T. simulans (Diptera: Tabanidae)


Graham N.L.; Stoffolano J.G.

Annals of the Entomological Society of America 76(4): 699-702

1983


Smaller flies (Tabanus nigrovittatus Macquart) deposit double-tiered egg masses on the adaxial surface of leaf blades of Spartina alterniflora Loisel while orienting on the leaf blade with their head directed towards the marsh surface. The larger females (T. simulans Walker) deposit single-layered, shingled eggs with their head oriented toward the sky. T. simulans was observed ovipositing in both the laboratory and field, whereas T. nigrovittatus was only observed laying eggs in the laboratory.

Relationship
Between
Female
Size,
Type
of
Egg
Mass
Deposited,
and
Description
of
the
Oviposition
Behavior
of
the
Sibling
Species
Tabanus
nigrovittatus
and
T.
simulans
(Diptera:
Tabanidae)
1
NANCY
L.
GRAHAM
AND
JOHN
G.
STOFFOLANO,
JR.
Department
of
Entomology,
University
of
Massachusetts,
Amherst,
Massachusetts
01003
Ann.
Entomol
Soc.
Am.
76:
699-702
(1983)
ABSTRACT
Smaller
fl
ies
(Tabanus
nigrovittatus
Macquart)
deposit
double
-tiered
egg
masses
on
the
adaxial
surface
of
leaf
blades
of
Spartina
alterniflora
Loisel
while
orienting
on
the
leaf
blade
with
their
head
directed
towards
the
marsh
surface.
The
larger
females
(T.
simulans
Walker)
deposit
single
-layered,
shingled
eggs
with
their
head
oriented
toward
the
sky.
T.
simulans
was
observed
ovipositing
in
both
the
laboratory
and
field,
whereas
T.
nigrovittatus
was
only
observed
laying
eggs
in
the
laboratory.
There
are
two
species
known
collectively
as
Tabanus
nigrovittatus.
Otherwise
indistinguishable
morpho-
logically,
one
(T.
simulans
Walker)
is
larger
than
the
other
(T.
nigrovittatus
Macquart),
although
there
may
be
some
overlap
in
size
(Jacobson
et
al.
1981).
The
two
species
have
been
separated
electrophoretically
in
New
Jersey
(Jacobson
et
al.
1981)
and
in
our
study
area
of
Wel!fleet,
Mass.
(Sofield,
personal
communication).
Our
objectives
were
to
learn
if
the
two
species
differ
in
oviposition
behavior
and
in
the
correlation
between
body
length
and
egg
mass
type.
Materials
and
Methods
We
studied
egg
-laying
behavior
of
the
two
tabanids,
T.
nigrovittatus
and
T.
simulans,
on
a
salt
marsh
within
the
Cape
Cod
National
Seashore,
where
they
are
sym-
patric.
The
dominant
vegetation
is
Spartina
alterniflora
Loisel
and
S.
patens
(Ait.)
Muhl.
Female
fl
ies
were
removed
from
box
traps
and
fed
to
repletion
on
warmed
(34
to
38
°
C),
citrated
human
blood
(Stoffolano
1979).
Engorged
fl
ies
were
measured
and
were
divided
into
eight
size
groups
of
1
-mm
intervals
from
9
to
17
mm;
each
group
was
placed
into
a
1
-mm,
wooden
-frame,
screened
cage
(61
cm))
and
provided
with
sugar
and
distilled
water.
S.
alterniflora
sod
(30
cm
2
)
was
placed
into
each
cage.
Because
of
the
high
mortality
of
captive
T.
simulans
and
a
scarcity
of
T.
nigrovittatus
in
the
Wellfleet
marshes,
females
were
continually
collected
from
the
traps,
blood
fed,
mea-
sured,
and
placed
into
the
appropriate
cages
until
50
egg
masses
were
collected
from
each
of
the
eight
cages.
S.
alterniflora
was
replaced
when
daily
removal
of
egg
masses
thinned
the
grass
or
when
the
grass
showed
signs
of
drying.
The
structure,
dimensions,
coloration,
and
number
of
eggs
per
mass
for
25
egg
masses
for
each
of
three
groups
(for
T.
nigrovittatus
in
laboratory
and
for
T.
simulans
both
in
the
laboratory
and
field)
were
re-
corded.
The
individual
eggs
were
also
measured.
Flies
were
maintained
at
ambient
temperature,
daylight,
and
relative
humidity.
'Paper
No.
2520,
Mass.
Agric.
Exp.
Stn.,
University
of
Massa-
chusetts
at
Amherst.
Received
for
publication
23
September
1982;
ac-
cepted
7
March
1983.
Oviposition
behavior
was
observed
in
the
field;
the
observers
crouched
at
the
level
of
the
S.
alterniflora
blades;
from
this
angle
fl
ies
were
silhouetted
against
the
sky
and
could
be
seen
ovipositing
from
a
distance
with
field
binoculars
(7
x
35,
wide
angle).
Upon
encoun-
tering
an
ovipositing
female,
the
observers
could
move
to
within
a
few
inches
of
her
and
easily
observe
her
behavior.
Egg
-laying
behavior
of
five
females
was
vid-
eotaped.
Results
Egg
masses
of
the
two
species,
laid
in
the
laboratory,
differed
in
structure,
coloration,
and
dimension,
and
in
the
size
of
the
individual
eggs.
T.
nigrovittatus
females,
the
smaller
of
the
two
species,
deposited
double
-tiered,
gray
masses
(Fig.
1),
like
those
descibed
by
Thompson
et
al.
(1979),
and
Magnarelli
and
Stoffolano
(1980)
(Fig.
2).
T.
simulans
females
deposited
tan,
single
-layered,
shingled
egg
masses
(Fig.
3).
Females
intermediate
in
size
(12
to
14
mm)
deposited
either
gray,
tiered
egg
masses
and
were
considered
T.
nigrovittatus,
or
tan,
shingled
egg
masses
and
were
considered
T.
simulans;
egg
masses
with
intermediate
characteristics
were
never
found
(Fig.
I).
In
the
salt
marsh,
ovipositing
T.
simulans
females
13.9
to
16.3
mm
long
were
found;
they
deposited
tan,
shingled
egg
masses.
These
masses
were
long
and
lan-
ceolate,
tapered
both
apically
and
basally,
and
were
de-
posited
on
the
adaxial
surface
of
the
blade
(Fig.
3).
When
first
deposited
in
the
salt
marsh,
the
masses
were
shiny
white;
however,
within
a
few
hours
they
darkened
to
a
light
tan
and
remained
so
if
removed
to
the
labo-
ratory.
If
allowed
to
remain
in
the
salt
marsh
for
48
h,
the
eggs'
outer
portions
(those
not
overlapped
by
other
eggs,
but
exposed)
darkened
to
a
chocolate
brown.
Egg
masses
deposited
in
the
laboratory
darkened
only
to
a
light
tan.
The
number
of
eggs
in
a
T.
nigrovittatus
egg
mass
deposited
in
the
laboratory
differed
significantly
from
those
deposited
by
T.
simulans
in
the
field
but
was
not
significantly
different
from
those
laid
by
T.
simulans
in
the
laboratory
(Table
1).
T.
simulans
egg
masses
laid
in
the
field
or
laboratory
were
significantly
longer
and
higher
than
those
laid
by
T.
nigrovittatus
in
the
laboratory
(Ta-
699
700
ANNALS
OF
THE
ENTOMOLOGICAL
SOCIETY
OF
AMERICA
Vol.
76,
no.
4
-
GRAY
TIERED
=--
fn
cf)
a
.
50
N
25
2
to
O
z
1111111111111111111111111111111111111111111111111111111
-
TAN
SHINGLED
IIIIIIIIIIIIIII
IIIIIIIIIIIIIII
mommunun
9-10
10-11
11-12
12-13
13-14
14-15
15-16
16-17
FLY
LENGTH
(mm)
FIG.
I.
Relationship
between
fl
y
length
and
the
type
of
egg
mass
deposited.
......
•_,-.„,
-.....,,-
4
:
,
-<4.4.
-
-•;.
?•
'
...t
3
FIG.
2.
Gray,
tiered
egg
mass
deposited
by
T.
nigrovittatus
on
the
frame
of
the
cage,
(5.7
x
).
FIG.
3.
Egg
mass
deposited
by
T.
simulans,
24
h
after
deposition
in
the
salt
marsh
(I
x
).
ble
1).
Measurements
of
four
eggs
from
each
of
25
T.
nigrovittatus
egg
masses
(mean;
length
=
1.56;
width
=
0.28)
and
25
T.
simulans
egg
masses
(mean;
length
=
1.98;
width
=
0.34)
differed
significantly
(P
<
0.01)
in
both
length
and
width.
To
determine
whether
the
fl
ight
from
blade
to
blade
Table
I.
Characteristics
of
the
egg
masses
and
size
of
individual
nigrovittatus
and
T.
simulans"
and
subsequent
scanning
behavior
of
the
plant
was
preo-
viposition
behavior,
35
females
exhibiting
this
behavior
were
dissected
to
see
if
they
had
mated
and
to
determine
stage
of
follicle
development
by
using
Mer's
(1936)
modifications
of
Christophers'
(1911)
classification.
All
35
females
had
mated
and
contained
stage
5
oocytes.
eggs
deposited
on
the
adaxial
surface
of
S.
alterniflora
blades
by
T.
Species
and
site
of
oviposition
Sample
size
Coloration
and
mass
structure
No.
of
eggs/
mass
(z
±
SE)
Dimensions
of
egg
masses
SE
in
mm)
Length
Width
Height
T.
nigrovittatus
(A)
Lab
-deposited
egg
masses
T.
simulans
(A)
Field
-deposited
egg
masses
(B)
Lab
-deposited
egg
masses
25
Gray/tiered
156.8
±
14.0a
6.7
±0.5a
2.7
±
0.2a
2.1
±
0.
Ia
25
Tan/shingled
204.0
±
12.1b
24.7
±
4.4c
2.9
±
0.8a
0.9
±
0.
1b
25
Tan/shingled
178.0
±
1
6.5ab
13.6
±
0.7b
2,8
0.1a
1.1
±
O.
lb
'Within
a
column,
means
which
are
not
followed
by
the
same
letter
are
significantly
different
at
P
<
0.01
.
July
1983
GRAHAM
AND
STOFFOLANO:
T.
nigrovittatus
AND
T.
simulans
OVIPOSMON
701
Other
females
which
we
could
follow
visually
eventu-
ally
laid
eggs.
Preoviposition
behavior
of
T.
simulans
began
with
a
random
fl
ight
from
blade
to
blade
of
numerous
S.
al-
terniflora
plants.
Generally,
females
landed
head
up
on
the
adaxial
surface
near
the
tip
of
the
blade,
turned
180
°
,
and
walked
down
to
the
base
of
the
blade,
whereupon
they
again
turned
180°
and
walked
back
up
the
plant.
If
they
completed
this
sequence
without
locating
a
suit-
able
oviposition
site,
females
fl
ew
to
other
plants
and
repeated
the
sequence.
Occasionally
females
landed
lower
on
the
blades
away
from
the
tip;
in
these
cases,
they
walked
to
the
tip
of
the
blade
and
exhibited
the
previ-
ously
mentioned
sequence.
This
down
-up
sequence
was
usually
performed
on
only
one
of
approximately
six
blades
on
a
plant.
While
walking
on
the
blade
of
grass,
females
arched
the
centers
of
their
abdomens
and
dragged
the
last
few
abdominal
sclerites
along
the
midrib
of
the
blade.
Dur-
ing
abdominal
dragging,
they
scanned
the
width
of
the
blade
by
continuously
bringing
both
forelegs
together
to
the
midline
of
the
blade.
During
oviposition,
T.
simulans
females
faced
head
up
on
the
plants.
Females
gradually
moved
toward
the
tips
of
the
blades
as
deposition
of
the
egg
mass
took
place.
Each
egg
was
laid
individually
by
curling
the
tip
of
the
abdomen
under
and
toward
the
abdominal
ster-
nites.
When
the
abdomen
was
returned
to
its
original
position,
an
egg
was
drawn
out.
After
deposition
of
each
egg,
the
female
scanned
it
and
a
few
of
the
surrounding
eggs
with
the
tip
of
her
abdomen
in
a
forward
-backward
movement.
After
scanning,
she
filled
in
gaps
in
the
egg
mass,
or
moved
toward
the
tip of
the
plant
while
de-
positing
new
sections
of
the
egg
mass.
During
ovipo-
sition,
females
clung
to
the
edges
of
the
blades
with
their
foretarsi.
Eggs
were
attached
to
the
adaxial
surface
of
the
blade
with
a
sticky
exudate
from
the
accessory
reproductive
glands.
Oviposition
sites
were
usually
lo-
cated
on
the
upper
third
of
the
blade.
The
average
length
of
19
blades
bearing
egg
masses
was
61.9
cm,
whereas
the
average
distance
from
the
base
of
the
blade
to
the
first
egg
laid
was
40.4
cm.
Blade
width
averaged
6.0
mm
at
the
site
of
the
egg
mass.
Of
19
females,
only
3
deposited
an
egg
mass
where
the
blade
width
was
wider
than
6.1
mm.
The
egg
mass
width
(mean
=
2.9
mm)
never
exceeded
4
mm.
If
disturbed
during
oviposition,
a
female
did
not
re-
turn
to
complete
the
original
egg
mass,
but
fl
ew
to
other
plants
and
engaged
in
the
preoviposition
sequence
until
she
encountered
a
suitable
oviposition
site.
In
the
salt
marsh,
only
one
egg
mass
was
found on
any
single
blade
of
S.
alterniflora.
Deposition
of
a
complete
egg
mass
took
a long
time.
One
female
took
40
min
to
deposit
200
eggs.
Once
ovipostion
was
completed,
females
fl
ew
to
other
blades
of
S.
alterniflora,
where
they
rested
head
down
on
the
lower
half
of
the
plant.
T.
nigrovittatus
were
rather
scarce
in
the
Wellfleet
area.
Several
females
were,
however,
seen
ovipositing
in
the
laboratory.
T.
nigrovittatus
females
differ
from
T.
simulans
by
facing
head
down
on
the
blades
of
S.
alterniflora
while
ovipositing.
Discussion
In
New
Jersey,
Jacobson
et
al.
(1981)
found
a
mean
total
body
length
of
12.8
mm
for
T.
simulans
and
10.5
mm
for
T.
nigrovittatus;
their
measurements
are
some-
what
smaller
than
ours
(Fig.
1).
Morphological
char-
acteristics
of
egg
masses
are
rather
constant
among
members
of
a
given
species;
thus,
egg
mass
difference
between
the
two
is
further
evidence
that
the
T.
nigro-
vittatus
complex
consists
of
two
species
on
the
marshes
of
the
outer
Cape
Cod
area.
Variation
in
larval
mor-
phology
and
habitat
led
Jamnback
and
Wall
(1959)
in
New
York
and
Freeman
(1962)
in
New
Jersey
to
suspect
that
T.
nigrovittatus
actually
included
two
species.
Although
the
egg
masses
of
the
two
species
are
morphologically
distinct,
there
can
also
be
some
varia-
tion
of
certain
measurements
and
in
the
number
of
eggs
per
mass
within
each
species.
The
tiered
egg
masses
of
T.
nigrovittatus
were
somewhat
larger
in
this
study
than
reported
by
Magnarelli
and
Stoffolano
(1980),
but
smaller
than
those
given
by
Jamnback
and
Wall(1959).
These
variations
in
egg
mass
size
and
in
number
of
eggs
per
mass
may
have
been
indirectly
due
to
a
number
of
fac-
tors,
including
quantity
of
stored
nutrients
carried
over
from
larval
stages,
amount
of
vertebrate
blood
con-
sumed,
number
of
gonotrophic
cycles
completed
(Mag-
narelli
and
Stoffolano
1980),
and
the
substrate
on
which
the
egg
masses
were
deposited.
In
the
salt
marsh,
females
scan
numerous
blades
of
S.
alterniflora
in
search
of
a
suitable
oviposition
site.
Females
in
the
laboratory,
however,
have
a
restricted
fl
ight
range
and
a
limited
selection
of
S.
alterniflora
blades;
this
could
result
in
the
choice
of
egg
-laying
sites
normally
rejected.
No
egg
masses
were
discovered
in
the
field
on
diseased,
dying,
or
damaged
blades,
or
on
blades
which
already
contained
an
egg
mass.
However,
in
the
laboratory,
several
egg
masses
were
often
found
on
the
same
blade
while
other
normal,
healthy
blades
remained
unoccupied.
Several
females
confined
in
a
cage
may
choose
the
same
blade
as
an
oviposition
site
due
to
any
number
of
physical
or
chemical
factors.
This
selection,
as
demonstrated
in
other
dipterans,
may
be
made
through
information
received
from
chemorecep-
tors
on
the
tarsi,
the
antennae,
or
the
ovipositor
(Hudson
1956,
Bar-Zeev
1967,
Haniotakis
and
Voyadjoglou
1978,
Stadler
1978).
Deposition
of
an
egg
mass
occurred
most
frequently
on
the
upper
third
of
the
blade,
where
the
width
was
4
to
6
mm.
Jamnback
and
Wall
(1959)
also
reported
this
for
T.
nigrovittatus.
At
this
width,
females
are
able
to
obtain
the
most
secure
grip
onto
the
edges
of
the
blades
with
their
foretarsi.
The
wind
in
the
salt
marsh
often
sways
the
blades
of
S.
alterniflora,
possibly
dislodging
females.
By
taking
into
consideration
blade
width
when
selecting
oviposition
sites,
females
can
be
assured
that
the
egg
mass
will
fit.
Also,
had
oviposition
occurred
where
the
blade
width
was
wider
or
narrower
than
the
distance
spanned
by
the
legs,
females
would
be
unable
702
ANNALS
OF
THE
ENTOMOLOGICAL
SOCIETY
OF
AMERICA
Vol.
76,
no.
4
to
maintain
a
normal
oviposition
posture.
Egg
masses
deposited
on
the
upper
third
of
the
blades
are
usually
high
enough
to
avoid
fl
ooding
from
all
but
the
spring
tides.
No
information
is
available
on
the
ability
of
eggs
to
survive
fl
ooding.
Oviposition
on
the
adaxial
rather
than
on
the
abaxial
surface
of
S.
alterniflora
may
prevent
the
egg
mass
from
dislodging.
The
adaxial
surface
is
composed
of
vascular
bundles
which
form
vertical
rows
of
deep
furrows
and
ridges.
Also,
small
papillae
are
present
on
the
adaxial
surface
but
are
lacking
on
the
abaxial
surface
(Anderson
1974).
These
furrows
and
papillae
-covered
ridges
on
the
adaxial
surface
may
aid
in
attaching
the
egg
mass
to
the
blade
with
the
accessory
reproductive
gland
fl
uid.
Acknowledgment
We
thank
M.
Soukep
of
the
Cape
Cod
National
Seashore
for
providing
laboratory
facilities
during
the
study,
P.
J.
God-
frey
and
M.
Benedict
for
offering
suggestions
and
criticism,
and
0.
Doane
of
the
Cape
Cod
Mosquito
Control
Association
and
Gail
Motyka
for
their
assistance
throughout
the
duration
of
this
research.
We
arc
grateful
to
L. L.
Pechuman
and
R.
Sofield
for
the
identification
of
adult
fl
ies
and
to
L.
A.
Mag-
narelli
and
H.
J.
Teskey
for
reading
the
manuscript
and
offering
helpful
criticism.
This
study
was
made
possible
in
part
by
re-
search
grant
5R0IA1
15039-02
from
N.I.H.
to
J.G.S.
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