Effect of the size of worker brood cells of Africanized honey bees on infestation and reproduction of the ectoparasitic mite Varroa jacobsoni Oud

Abstract

An investigation was made of the influence of honey bee worker brood cell size on infestation by the mite Varroa jacobsoni. Pieces of combs constructed by Africanized (small cells) and pure Italian (large cells) honey bees were placed within the same frame and eggs were laid by a single queen in each trial. Two queens, one Africanized and the other Italian, were mated with Africanized drones, and their respective colonies were used in 16 trials. The frequency of infested brood cells was higher in the large worker brood cells built by European races than in the small worker brood cells built by Africanized bees (15.7 vs 7.3%, respectively), though other factors, including egg origin and colony, were equal. The same was true for frequency of cells with female deutonymphs (which represent effective reproduction) (11.9 vs 4.7%, respectively).

Full text

Original
article
Effect
of
the
size
of
worker
brood
cells
of
Africanized
honey
bees
on
infestation
and
reproduction
of
the
ectoparasitic
mite
Varroa
jacobsoni
Oud
D
Message
LS
Gonçalves
1
Depto
Biologia
Animal,
Universidade
Federal
de
Viçosa,
36571-000
Viçosa,
MG;
2
Depto
Biologia,
FFCLRP,
USP,
14049-901
Ribeirão
Preto,
SP,
Brazil
(Received
28
October
1993;
accepted
28
March
1995)
Summary —
An
investigation
was
made
of
the
influence
of
honey
bee
worker
brood
cell
size
on
infes-
tation
by
the
mite
Varroa
jacobsoni.
Pieces
of
combs
constructed
by
Africanized
(small
cells)
and
pure
Italian
(large
cells)
honey
bees
were
placed
within
the
same
frame
and
eggs
were
laid
by
a
sin-
gle
queen
in
each
trial.
Two
queens,
one
Africanized
and
the
other
Italian,
were
mated
with
Africanized
drones,
and
their
respective
colonies
were
used
in
16
trials.
The
frequency
of
infested
brood
cells
was
higher
in
the
large
worker
brood
cells
built
by
European
races
than
in
the small
worker
brood
cells
built
by
Africanized
bees
(15.7
vs
7.3%,
respectively),
though
other
factors,
including
egg
origin
and
colony,
were
equal.
The
same
was
true
for
frequency
of
cells
with
female
deutonymphs
(which
rep-
resent
effective
reproduction)
(11.9
vs 4.7%,
respectively).
Apis
mellifera/Varroa jacobsoni/Africanized
bees
/ mite
reproduction
/ brood
infestation
INTRODUCTION
Although
the
ectoparasite
Varroa jacobsoni
Oud
has
maintained
itself
in
equilibrium
for
a
long
time
with
its
original
host
Apis
cer-
ana
Fabr,
in
A
mellifera
L
this
adaptation
has
not
been
established
and
the
mite
nor-
mally
causes
serious
losses
for
the
bee-
keeping
industry
(De
Jong
et al,
1982a).
However,
in
Brazil,
where
most
beekeep-
ing
is
based
on
Africanized
bees,
infesta-
tion
has
not
reached
alarming
levels,
with
no
reports
of
colony
losses
exclusively
attributable
to
varroosis.
In
contrast,
in
Argentina,
where
European
bees
predomi-
nate,
the
infestation
has
reached
high
levels
(De Jong
et al,
1984).
This
difference
observed
between
Euro-
pean
bees
and
African
or
Africanized
bees
has
stimulated
a
great
deal
of
research
to
determine
what
factors
influence
Varroa
populations.
The
race
of
honey
bees

(Camazine,
1986;
Moretto
et al,
1991
a)
and
climatic
conditions
(Moretto
et al,
1991 b)
appear
to
play
a crucial
role
in
the
resis-
tance
of
bees
in
Brazil,
though
Rosenkranz
et
al
(1984)
did
not
attribute
the
low
rate
of
reproduction
to
the
high
tropical
ambient
temperatures.
Hygienic
and
grooming
behavior,
the
shorter
post-capping
phase
of
the
brood
and
the
higher
rate
of
infertile
females
are
some
racial
factors
that
could
contribute
to
this
higher
resistance
of
African
and
Africanized
bees
(Moritz
and
Hänel,
1984;
Ritter
and
De
Jong,
1984;
De
Jong,
1990;
Moritz
and
Mautz,
1990;
Moretto
et
al,
1991a).
Increase
in
worker
infestation
has
also
been
observed
in
reared
cells
inde-
pendently
of
the
race
of
bees
(De
Jong
and
Morse,
1988;
De
Ruitjer and
Calis,
1988).
In
the
present
study,
the
influence
of
the
smaller
worker
cells
built
by
Africanized
bees
in
relation
to
larger
cells
built
by
European
races
on
the
infestation
and
reproduction
of
the
mite
V jacobsoni was
investigated.
MATERIALS
AND
METHODS
We
used
specially
built
(mosaic)
combs
contain-
ing
2
pieces
of
comb
each
about
7 x 10
cm,
inserted
into
the
center,
one
made
up
of
cells
built
by
Africanized
bees
(small
cells)
and
the
other
with
cells
built
by
A
m
ligustica
(large
cells).
The
smallest
width
and
the
volume
(measured
by
filling
the
cells
with
water
from
a
calibrated
pipette)
of
these
cells
varied
from
4.5
to
4.6
mm
and
from
175
to
195
μl,
respectively,
in
small
cells,
and
from
4.9
to
5.1
mm
and
from
240
to
260
μl
in
large
cells.
Two
queens
and
their
respective
colonies
were
utilized
for
egg
laying
and
brood
develop-
ment.
One
was
a
wild-type
Africanized
honey
bee
queen
and
the
other
an
Italian
queen,
which
was
open
mated
in
an
Africanized
bee
region,
therefore
producing
F,
hybrid
Africanized/Italian
workers.
Combs
with
the
2
types
of
cells
with
eggs
of
one
queen
were
placed
in
the
same
colony
or
in
the
colony
of
the
other
queen,
and
vice
versa.
Egg
laying
by
the
queens
in
the
2
types
of
cells
occurred
with
only
a
small
variation
in
time,
so
that
brood
of
practically
the
same
age
and
from
the
same
queen
was
available
in
each
of
the
composite
combs.
The
brood
cells
were
ana-
lyzed
individually
at
17-18
d,
for the
presence
of
adult
mite
females,
deutonymphs
and
other
off-
spring
(eggs,
female
protonymphs
and
males
at
the
various
developmental
phases)
of
Varroa.
Sixteen
trials
were
made
for
a
total
of
1
572
pupae
developed
in
small
cells
and
1
642
pupae
in
large
cells.
The
data
were
analyzed
statistically
by
the
Student’s
t-test
for
paired
samples.
RESULTS
AND
DISCUSSION
No
significant
effect
of
the
queen
or
colony
was
found
(P
> 0.4),
and
so
the
data
were
pooled.
The
Varroa
infestation
rate
was
2-
fold
higher
in
brood
developed
in
large
cells
in
relation
to
brood
developed
in
small
cells
(table
I).
The
significantly
(P
< 0.01)
higher
brood
weight
observed
in
large
cells
(aver-
age
of
108.2
mg)
in
relation
to
the
small
cells
(average
99.2
mg)
should
promote
differential
feeding.
Worker
brood
devel-
oped
in
large
cells
should
receive
more
vis-
its
from
nurse
workers,
increasing
the
prob-
ability
of
the
mites
transferring
to
the
cells
to
infest
the
brood.
Fuchs
(1990)
found
a
decrease
in
the
intensity
of
the
attraction
of
the
drone
larvae
when
they
are
nursed
less
intensively
towards
the
end
of
drone
production.
Besides
physical
stimuli,
lar-
vae
from these
cells
could
also
contribute
with
other
stimuli,
such
as
kairomones.
Le
Conte
et al (1989)
have
isolated
and
iden-
tified
some
esters
(eg,
methyl
palmitate)
promoting
a
strong
attractive
response
in
the
Varroa
female.
This
substance
was
iso-
lated
from
drone
brood
but
is
also
present
in
worker
brood
in
smaller
amounts.
The
prolonged
and
intensive
capping
activity
(Fuchs,
1990;
Wieting
and
Ferenz,
1991)
should
be
related
to
the
phoresis
hypoth-
esis,
due
to
the
large
amount
of
time
that
nurse
workers
spend
near
the
brood
dur-
ing
this
activity,
increasing
the
chance
for
mites
to
move
from
cell
capping
workers
to
the
host brood.

During
the
experiments
we
did
not
observe
any
drone
brood
in
the
colonies,
and
so
the
mites
had
only
the
worker
cells
available.
There
were
slightly
more
original
adult
females
in
large
infested
cells
than
in
infested
small
cells
(table
II).
We
found
29
cells
with
2
adult
females
and
7
cells
with
3
adult
females
among
large
cells,
whereas
among
small
cells
only
6
cells
had
2
adult
females
and
none
had
3
or
more.
The
number
of
female
deutonymphs
pro-
duced
did
not
differ
significantly
between
infested
large
and
small
cells
(table
I).
How-
ever,
a
greater
percentage
of
all
large
cells
had
deutonymphs
(table
II).
If
we
consider
that
the
female
deutonymphs
encountered
in
this
experiment
on
17-18
d
pupae
are
effective
reproductions,
the
large
cells
con-
tributed 2.6-fold
more
to
the
population
increase
of
Varroa.
In
this
experiment
we
also
observed
a
high
proportion
of
original
adult
females
that
entered
into
the
cells
with
brood
and
left
no
offspring
(tables
I and
II).
This
pro-
portion
was
the
same
for
both
type
of
cells.
This
suggests
that
the
infertility
rate
is
not
due
to
the
size
of
cells
built
by
European
or
Africanized
bees,
but
to
other
factors.
A
high
rate
of
mite
infertility
has
been
shown
in
Africanized
bees
(De
Jong
et al,
1982b;
Ritter and
De Jong,
1984;
Camazine,
1986)
and
in
European
bees
in
South
America
(Ruttner
et al,
1984;
Marcangeli
et al,
1992).
We
conclude
that
small
comb
cell
size
affects
the
infestation
and
reproduction
of
V jacobsoni
in
worker
brood
of
Africanized
bees
in
Brazil.
Other
factors
observed
in
Africanized
bees,
including
shorter
devel-
opment
time
(19-20
d)
of
worker
brood
(Message,
1986),
grooming
and
hygienic
behavior;
climatic
conditions
(Moretto
et al,
1991
a,
b)
and
higher
frequency
of
temper-
ature
peaks
during
the
thermal
regulation
of
the
brood
chamber
of
Africanized
bees
(Le
Conte
et
al,
1990)
also
contribute
to
the
greater
resistance
of
Africanized
bees
to
V
jacobsoni
in
Brazil
and
other
tropical
and
subtropical
countries
compared
with
Euro-
pean
races
of
bees.

ACKNOWLEDGMENTS
We
wish
to
thank
D
De
Jong
for
providing
useful
discussions,
reviewing
the
manuscript
and
for
writing
the
summary.
This
work
was
funded
by
CNPq
(Brazil)
and
NSF
(USA).
Résumé &mdash;
Effet
de
la
taille
des
cellules
de
couvain
d’ouvrières
d’abeilles
africa-
nisées
sur
l’infestation
et
la
reproduc-
tion
de
l’acarien
parasite
Varroa
jacob-
soni.
La
parasitose
par
Varroa
jacobsoni
est
un
problème
grave
pour
l’apiculture.
Cependant,
au
Brésil,
où
l’apiculture
est
basée
sur
l’utilisation
de
l’abeille
africani-
sée,
l’épidémie
n’a
pas
atteint
un
niveau
alarmant,
et
il
n’y
a
pas
eu
de
pertes
de
colonies
dues
exclusivement
à
l’acarien.
Puisque
l’abeille
africanisée
est
plus
petite
que
l’abeille
européenne,
à
la
fois
au
stade
adulte
et
aux
stades
larvaires,
nous
avons
analysé
l’influence
de
la
taille
des
cellules
de
couvain
d’ouvrières
d’abeilles
africanisées
sur
l’infestation
et
la
reproduction
du
para-
site.
Des
morceaux
de
rayon
construits
par
des
abeilles
africanisées
(petites
cellules)
et
de
race
italienne
(grandes
cellules)
ont
été
placés
dans
le
même
cadre.
Une
seule
reine
a
pondu
au
cours
de chacun
des
16
essais.
La
fréquence
des
cellules
de
cou-
vain
infestées
(tableau
I)
a
été
significati-
vement
plus
élevée
dans
les
grandes
cel-
lules
(15,7%)
que
dans
les
petites
(7,3%).
Le
nombre
de
femelles
de
Varroa
a
été
légè-
rement
supérieur
dans
les
grandes
cellules
(298/258
=
1,15
femelle
adulte
par
cellule)
que
dans
les
petites
(120/115
= 1,04 femelle
adulte
par
cellule).
Le
nombre
de
deuto-
nymphes
a
été
2,6
fois
plus
grand
dans
les
grandes
cellules.
Le
poids
plus
grand
des
nymphes
élevées
dans
les
grandes
cellules
(108,2
mg)
par
rapport
à
celles
élevées
dans
les
petites
cellules
(99,2
mg)
suggère
que
les
ouvrières nourrices
s’occupent
davan-
tage
des
premières,
ce
qui
augmente
donc

la
probabilité
d’apporter
des
acariens
au
contact
des
larves.
Les
données
obtenues
dans
ce
travail,
sur
l’effet
de
la
taille
des
cel-
lules,
le
nombre
de
cellules
infestées
et
le
temps
de
développement
du
couvain
d’ou-
vrières
d’abeilles
africanisées,
aussi
bien
que
les
données
de
la
littérature
concernant
le
comportement
de
nettoyage,
les
condi-
tions
climatiques
et
la
régulation
thermique
de
la
colonie,
contribuent
à
expliquer
la
plus
grande
résistance
des
abeilles
africanisées
à
Varroa
jacobsoni
au
Brésil
et
dans
d’autres
régions
tropicales
et
sub-tropicales,
par
rap-
port
aux
races
européennes.
Apis
mellifera
/
Varroa
jacobsoni
/
abeilles
africanisées
/ reproduction
de
Varroa /
infestation
du
couvain
Zusammenfassung &mdash;
Einflu&szlig;
der
Grö&szlig;e
von
Arbeiterinnenbrutzellen
der
afrika-
nisierten
Honigbiene
auf
Befall
und
Reproduktion
der
ectoparasitischen
Milbe
Varroa jacobsoni Oud.
Durch
Varroa
jacobsoni
ist
für
die
Bienenhaltung
ein
gefährliches
Problem
entstanden.
In
Brasi-
lien
werden
afrikanisierte
Bienen
gehalten
und
dort
hat
der
Milbenbefall
nicht
so
alar-
mierende
Raten
erreicht
wie
zB
in
Europa.
Es
gibt
keine
Verluste
von
Bienenvölkern,
die
nur
auf
dem
Befall
durch
Varroa
jacob-
soni beruhen.
Afrikanisierte
Bienen
sind
klei-
ner
als
Bienen
der
europäischen
Rassen.
Grö&szlig;enunterschiede
finden
sich
auch
bei
den
Arbeiterinnenbrutzellen.
Deshalb
wurde
der
Einflu&szlig;
der
Zellgrö&szlig;e
auf
den
Befall
und
die
Reproduktion
der
Milbe
Varroa
jacob-
soni
untersucht.
Wabenstücke,
die
entweder
von
afrika-
nisierten
(kleine
Zellen)
oder
von
reinen
Ita-
lienerbienen
(gro&szlig;e
Zellen)
gebaut
waren,
wurden
gemeinsam
in
einen
Rahmen
ein-
geschnitten.
Die
Eier
stammten
in
allen
16
Versuchen
von
derselben
Königin.
Die
grö&szlig;eren
Zellen
der
Italienerbienen
waren
statistisch
gesichert
häufiger
befal-
len
(15,7%)
als
die
kleinen
der afrikanisier-
ten
Bienen
(7,3%,
Tabelle
I).
Es
befanden
sich
geringfügig
mehr
Muttermilben
in
gro&szlig;en
befallenen
Zellen
(298/258
= 1,15
Muttermilben/Zelle)
als
in
den
kleinen
Zellen
(120/115
=
1,04
Muttermilben/Zelle).
Die
Anzahl
der
Deutonymphen
in
Zellen
mit
Nachkommen
zeigte
keine
grö&szlig;enabhän-
gigen
statistischen
Unterschiede.
Insgesamt
aber
befanden
sich
in
gro&szlig;en
Zellen
2,6
mal
mehr
Deutonymphen.
Der
signifikante
Unterschied
im
Gewicht
der
17
bis
18
Tage
alten
Brut
in
gro&szlig;en
und
kleinen
Zellen
lä&szlig;t
vermuten,
da&szlig;
unterschiedlich
häufig
gefüt-
tert
wird
und
damit
auch
die
Wahrschein-
lichkeit
unterschiedlich
ist,
da&szlig;
eine
Milbe
in
die
Zelle
getragen
wird.
Die
hier
gewonnenen
Daten
über
den
Einflu&szlig;
der
Zellgrö&szlig;e,
die
Anzahl
der
befal-
lenen
Zellen
ohne
Reproduktion
(43%)
und
die
kürzere
Entwicklungsdauer
(19-20
Tage)
der
afrikanisierten
Arbeiterinnenbrut
tragen
im
Zusammenhang
mit
Literaturdaten
über
Putzverhalten,
über
Klimabedingun-
gen
und
über
häufiges
Vorkommen
von
Temperaturpeaks
bei
der
Thermoregulation
zur
Erklärung
der
höheren
Resistenz
der
afrikanisierten
Bienen
in
Brasilien
und
ande-
ren
tropischen
und
subtropischen
Ländern
im
Vergleich
zu
europäischen
Rassen
bei.
Zellgrö&szlig;e
/
Arbeiterinnenbrut
/
Varroa
jacobsoni/afrikanisierte
Honigbienen
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