Original article
Cymiazole, a systemic acaricide that controls Acarapis woodi (Rennie) infesting honey bees. II. An apiary test*
F. A. Eischen D. Cardoso-Tamez A. Dietz 1 G. O. Ware
1
Department
ofEntomology, University
ofGeorgia, Athens,
GA30602, USA;
2
Apicultura Cardoso, Apdo.
Postal No.1,
BuenavistaAllende,
NuevoLeon, Mexico;
3
Agriculture Experiment Station, University
ofGeorgia, Athens,
GA30602,
USA(received 1-12-1987, accepted 1-8-1988)
Summary — Honey
bee colonies located in northeastern Mexico weregrouped according
to theprevalence
ofAcarapis
woodiparasitizing
their workers.Lightly (: 5 10%), moderately (20—60%),
andheavily (90—100%)
infested colonies(N
= 30 eachgroup)
wererandomly assigned
to control ortreated
subgroups (N
=15).
Controls received 50% sucrose syrup, and treated colonies received syrup medicated with 0.3mg/ml
ofcymiazole (2-[2,4-dimethylphenyl-imino]-3-methyl-4-thiazoline- hydrochloride, Apitol s , GRA,
17.5%cymiazole, Ciba-Geigy Ltd.). Small, medium,
andlarge
coloniesreceived 300, 600, and 1 000 ml of syrup,
respectively. Syrup
was fed 3 times atweekly
intervals.At the end of treatment, the
parasite
load scores in medicated colonies were0.53, 0.84,
and 0.63 in thelightly, moderately,
andheavily
infested groups,respectively.
Thiscompared
with2.25, 3.43,
and 1.13parasite
load scores in the control colonies of the same groups,respectively (all
P <0.05).
In each group some colonies did not
respond typically
to medication. Mitepopulations
at the end ofthe test were
positively
associated withcolony
sizes and food reserves at thebeginning
of the test.Increased
dosages,
as well as redistribution/reduction of food reserves are recommended forgreat-
er
efficacy.
Unexpectedly,
medicated colonies hadsignificantly larger
beepopulations
than controls at the end of the test(P
<0.05).
Increased beelongevity
due toparasite
load reduction issuggested
as thecause.
Acarapis
woodl-cymiazole
-dosage
Résumé — Le
cymiazole (Apitol ® ),
un acaricidesystémique
contreAcarapis
woodi(Rennie), parasite
de l’abeille. Il. Test au rucher. On a choisi 3 groupes de coloniesdabeilles (N
=30)
situées dans le nord-est du
Mexique (lat.
25112’N, long.
99° 58’0)
en fonction de leurparasitisme
par
Acarapis
woodi :léger (5 10°l),
moyen(20-60%),
fort(90-100 , Y.). Chaque
groupe a été ensuite subdivisé defaçon
aléatoire en sous-groupes traités et sous-groupes témoins(N
=15).
Lestémoins ont reçu un
sirop
de saccharose à 50% et les colonies traitées unsirop supplémenté
avec0,3
mglml
decymiazole (hydrochlorure
de2-(2,4-diméthylphényl-iminoj-3 méthyl-4-thiazoline; spé-
cialité
Apitol O
deCiba-Geigy
Ltd. sous forme degranulés
dosés à17,5%
decymiazole).
Lespetites colonies,
les moyennes et les grosses ont reçurespectivement
300, 600 et 1 000 mi desirop
3 foisde suite à une semaine d’intervalle.
’ Mention of a commercial or
proprietary product
in this paper does not constitute an endorsement of theproduct by
theUniversity
ofGeorgia
or the Food and Drug Administration."
Present address : Department of
Entomology,
Pullman, WA 99164, USAA la fin du traitement le taux de
parasitisme
des colonies traitées étaitrespectivement
de0,53, 0,84
et0,63
dans les groupeslégèrement, moyennement
et fortementinfestés,
contre2,25, 3,43
et 1,13 chez les témoins des mêmes groupes(P
<0,05).
Danschaque
groupequelques
coloniesn’ont pas
réagi
au traitement defaçon typique.
Lespopulations
d’acariens en fin de test étaientpositivement
corrélées avec la taille de la colonie et les réserves de nourriture en début de test.Pour une
plus grande efficacité,
on recommande des dosesplus
fortes ainsiqu’une
redistribution ou une réduction des réserves de nourriture.Contre toute attente, les colonies traitées avaient en fin de test une
population significativement plus
forte(P
<0,05)
que les témoins. On pense que lalongévité
accrue des abeilles due à la dimi- nution duparasitisme
en est la cause.Acarapis
woodi -cymiazole
-dosage
2usammenfassung - Cymiazol (Apitol ® ),
einsytemisches
Akarizid zurBekämpfung
vonAcarapis woodl (Rennie)
beiHonigblenen.
11. Ein Freilandversuch. DreiGruppen
von Völkernder
Honigbiene (N
=30)
in Nordost-Mexiko(lat.
25°12’N, long.
99°58’W)
wurdengemäß
ihremBefall mit
Acarapis
woodi(Rennie) ausgewählt.
Leicht( S 10%),
mittel(2-60 % )
und stark(90—
100%)
befallene Völker wurden anschließend wahllos auf Kontroll- oderVersuchsuntergruppen (N
=15)
verteilt. DieKontrollgruppen
erhielten50°ligen Saccharosesirup,
die VersuchsvölkerSirup
mit 0.3
mglmi Cymiazol (2-[2,4-Dimethylphenyl-iminoJ-3-methyl-4-thiazolin-hydrochlorid, Apitol g
17.5%
Cymiazol Granulat, Ciba-Geigy Ltd.).
Diekleinen,
mittleren undgroßen
Völker erhielten drei- mal300,
600 oder 1 000 mlSirup
in wöchentlichem Abstand.Nach der
Behandlung
war die Befallsrate derleicht,
mittel und stark befallenen Völker 0.53, 0.84 und0.64,
imVergleich
zu einer Befallsrate von2.25,
3.43 und 1.13 bei den Kontrollvölkern derglei-
chen
Gruppe (P
<0.05). In jeder Gruppe gab
esVölker,
die nichttypisch
auf die Medikation anspra- chen. DieMilbenpopulation
war am Ende des Versuchspositiv
korreliert mit derVolksgröße
undden Futterreserven am
Anfang
des Tests. Um die Wirksamkeit des Mittels zu erhöhen wirdempfoh- len,
stärker zu dosieren und die Futterreserven umzuverteilen bzw. zu reduzieren.Entgegen
denErwartungen
hatten die behandelten Völker imVergleich
zu den Kontrollvölkernam Ende des Tests eine
größere Bienenpopulation (P
<0.05).
Vermutlich ist die Ursache dafür in einerlängeren
Lebensdaueraufgrund
des reduziertenBefallsgrades
zu suchen.Acarapis
woodi —Cymiazol — Dosierung
Introduction
The
rapid spread of the honey bee
trea-cheal
miteAcarapis woodi (Rennie) throughout much of Mexico and the Uni- ted States has complicated and frustrated normal containment procedures (Guz-
man-Novoa and Zozaya-Rubio, 1984;
Anon., 1985; Anon., 1986b). The situation has been exacerbated by
its recentdiscovery in Canada (Anon., 1986c;
Gruszka, 1987).
Anumber of Canadian
provinces have responded by closing
their border
toUS shipments
ofqueens
andpackage bees (Anon., 1986d). These
events
left
most sectorsof North Ameri-
can
beekeeping
in adifficult position. Safe
and efficacious control measures
would offer
relief toinfested
areasand provide
assurance to
uninfested regions that this parasite
ismanageable.
Recently the systemic
acaricidecymia-
zole has been found efficacious
incontrol-
ling the parasitic honey bee mite, Varroa jacobsoni Oudemans (Ritter, 1985;
Schmid, 1985). Additionally,
wehave
found it effective
incontrolling
A.woodi
inlaboratory
testsinvolving caged worker
bees (Eischen
etal., 1989). This report describes
theperformance of cymiazole
when fed
tohoney production
coloniesin
Mexico.
Materials
andMethods
The
following
terms are used to describe infes- tations :prevalence(w),
thepercentage
of workers infested within acolony; parasite load,
the numbers of mites in an individual
bee;
parasite
load score, an estimate of theparasite
load. These terms are in
keeping
with currentparasitological terminology (Margolis
etal., 1982).
During early February
1987, 90 colonies ofhoney
bees located near Soto laMarina, Tamaulipas,
Mexico(lat.
23°46’N, long.
98°12’W)
were selected fortesting. Only
colonieswith a
laying
queen, brood in allstages,
and bees across at least 3 frames were chosen.Colonies were
grouped according
to the preva- lence(w)
of infestedbees, viz., Group 1,
<10%, Group II,
2D-60%, andGroup 111,
90—100%(N 30).
Infestation levels were determinedby removing
20 bees from the inner surface of the hive cover,placing
them in 80%ethyl
alcoholand
dissecting
themaccording
to thetechnique
described
by
Eischen(1987). Bradbury (1924a, b)
has shown that a 20 beesample gives
reas-onable accuracy
except
for the lowest infesta- tions. Colonies were moved on 20February
1987 to the test site near El
Naranjo,
NuevoLeon
(lat.
25°12’N, long.
99°58’W).
This loca-tion lies in the foothills of the Sierra Madre Oriental and was chosen for its isolation from other
managed
colonies and distance from citrus orchards. The latter wasimportant
because citrus trees in the
general region
wereexpectad
to flower in lateMarch,
and we wished to ensure that the bees would not be diverted from the medicated syrup.Colonies within infestation groups
(I,
II andIII)
wererandomly assigned
to either medicatedor unmedicated
subgroups (N = 15).
Coloniesin the 3 untreated
subgroups
were located ca.100 m from the 3 treated
subgroups.
Distancebetween
subgroups ranged
from 10—50 m.Intercolony
distance withinsubgroups
was= 2 m. These distances were chosen to reduce
intercolony drifting by
workers.A few
days prior
to treatment, colonies were examined and estimates of thequantities
ofbees, brood, honey,
andpollen
made in termsof standard
Langstroth
frames(Kulincevic
et al., 1982). Additionally,
asample
of 20 beeswas taken from each
colony, placed
in 80%ethyl
alcohol andsubsequently
an estimate of theirparasite
loadmade, using
thetechniques
described
by
Eischen(1987).
Based on the number of adult
bees,
the 5 median colonies of eachsubgroup
were selec-ted for
monitoring
while the test wasbeing
conducted. Ten bees from each of these col- onies were removed
weekly
from the inner sur-face of the hive cover. Bees were dissected and the number of
living
and dead mites coun-ted
according
to thetechniques
describedby
Eischen et al.
(1987).
Our purpose in monito-ring
these colonies was to determine how selecteddosages
wereaffecting
mite popu- lations. This information gave us theoption
ofaltering
the dose if conditions warranted it.However,
nochanges
were made.Colony
treatmentbegan
on 28February.
Allmedicated colonies received syrup
containing
0.3
mg/ml
ofcymiazole (2-[2,4-dimethylphenyl- imino]-3-methyl-4-thiazoline hydrochloride, Api- tot’
S
, GRA,
17.5%cymiazole, Ciba-Geigy Ltd.).
One liter of medicated syrup was
prepared by dissolving
1.714 g ofApitol ©
in one liter ofwarm
(ca. 30°C)
50% sucrose syrup(vol/vol).
Enough
medicated or unmedicated syrupwas
prepared
to treat onesubgroup daily.
Thequantity
of syrup that eachcolony
received wasbased on the
quantity
of adult bees. Two small colonies(<
3 frames covered withbees,
both inGroup III, medicated)
received 300ml,
medium-sized colonies(3—7 frames)
received600
ml,
andlarge
colonies(>
7frames)
receiv-ed 1000 ml.
Syrup
wasplaced
in metal cans(1600 ml)
fitted with frictiontop
lids in which several holes had beenpunched.
These canswere inverted and
placed
over thetop
bars ofthe
uppermost
frames of thecolony.
Bees nor-mally
removed the syrup within 48 h. A few colonies wereslower,
in which case after 72 h theremaining
syrup wassprinkled
over thebees. Colonies were fed 3 times at
7-day
inter-vals. At the end of treatment, a
light
nectar flowoccurred. One standard shallow and one
deep
super were
given
to all but the 2extremely
small colonies in
Group 111,
medicated.Twenty-
five
days later,
these supers wereweighed.
The average of 5 supers of each size were used to tare filled supers.
Thirty days
after thelast
feeding,
colonies were reexamined and estimates ofquantities
ofbees, brood, honey
and
pollen made, along
with an estimate of theparasite
load.Colony
estimates and mite data were eval- uated withanalysis
of covariance(Snedecor
and
Cochran, 1967).
Theobjective
was todetermine how the medication affected each infestation group, i.e.
Groups I, II,
and 111. Mean differences betweenbeginning
andending
values within each group were tested for
signifi-
cance after
adjusting
for initialstarting
treat-ment
subgroup
means.Additionally,
infestationpercentages
weregiven
an arcsine transforma- tion.Results
One colony died
ineach of the medicated colonies of Groups 11
and111. These deaths
werefrom queenlessness and
extreme
dwindling, respectively, and
werenot
associated with the medication. Data from these colonies have
notbeen inclu- ded in
theanalysis.
Near the end of the treatmentperiod (15—25 March)
severalcolonies raised varying numbers
of queencells, probably
inpreparation for
swarm-ing. None
werefound
inthe colonies of
Group 111. Approximately
50%of the medi- cated colonies
inGroups I and
IIraised
queens, while about
30%of the control colonies of these groups did
so.All col- onies
were examinedweekly
for queencells and when found
weredestroyed.
One
swarm wasfound
nearthe Group
Icontrol colonies. Medicated colonies took about
24 hlonger
to remove their syrupthan did controls.
Wehave
since learnedthat Apitol e may have reacted
withthe metal containers.
If so,palatability (but
not
effectiveness) of treated syrups
mayhave been reduced (W.J. Schmid, pers.
comm.).
When
initially
selected on 7February 1987,
thepercentages
of beesparasitized by
A. woodi inGroups I,
II and III aver-aged
6.0 ±1.5,
42.4 ±3.9,
and 91.8 ±1.6%, respectively. However, by
28February
whenthe
testbegan, mite popu- lations in the
samegroups averaged
21.0 ±
1.8,
47.3 ±3.6, and
76.4 ±3.9%, respectively.
Thatis, populations of
A.woodi
had increased
inGroup I, remained
about
the
same inGroup II, and had decreased in Group
III.This pattern of change continued during the
testperiod
inthe untreated controls.
Mite population changes in
the 5median indicator colonies
areshown
inFigure
1. Ingeneral,
A. woodipopulations
stabilized
or declined in themedicated colonies,
whilethey
rose in the untreatedcolonies. The relative level of control
observed in the 5colonies
wasindicative of the entire subgroup (see Table I for comparison). Seven days after the last medication (28th day), infestations
in the 5 controlcolonies of Groups I,
IIand III, averaged 13.9,
15.6and
10.5mites/tra- chea, respectively. Medicated colonies of the
same groups atthe end of the
test had onaverage 2.5,
8.9 and 5.1 mites in theirtrachea, respectively.
A.
woodi populations
at thebeginning
and end
of
the test are morecompletely
described by the data presented
inTable
I.Parasite load
scores show thatduring the test, mite populations
rose255.7% in the control colonies of
Group
I.Populations
in themedicated colonies
ofthis group declined
to 76.8%of their
star-ting numbers (P
<0.01 Group
IIdata
were similar.
Mite populations
in controlcolonies
rose137%,
whilemedicated colonies declined
to 39.4%of their
start-ing population (P
<0.01 in contrast, parasite load
scoresdeclined
in boththe
control
and medicated colonies of Group
III. The decline
wasgreatest in the medi-
cated colonies(P
<0.01 Though
para-site
load scores cannotbe converted
toprecise mites/bee, the data indicate that in the control colonies of Groups I,
IIand III, there
wereroughly 22.5,
34.3 and 11.3mites/bee, respectively
at the end of the test. Medicatedcolonies
ofthe
samegroups
hadroughly 5.3,
8.4 and 6.3mites/bee, respectively.
Similar
shifts in the mitepopulations
were
observed
in theprevalence(w) of
infested bees. That is, in the untreated colonies
ofGroups
Iand II, populations
rose to 173 and 143%
respectively,
whilepopulations fell in the medicated colonies
to 94and
74%of
theirstarting values, respectively (both
P <0.01, Table I). The
number of infested bees
inboth the control and medicated colonies dropped
in
Group 111,
with the declinebeing grea-
test in themedicated colonies (P
<0.01 ).
The percentage of bees harboring bilat-
eral infestations underwent changes simi-
lar
tothose described above.
As with theparasite
load score andprevalence (w), the number of bilateral infestions declined
in all the treatedsubgroups. Downward
shifts
were mostpronounced
incolonies bearing
the heaviest infestations(Table I).
During
thetest, colony size,
i.e. num-ber of adult bees, increased
inall
treat- mentgroups (Table II). Medicated
col-onies attained
agreater
size thancontrols
in all
groups and
weresignificantly larger
in
Groups
II(P < 0.05)
andIII (P < 0.01 ).
The percent increase in colony size
wasgreatest
inGroup
111.This
may reflect the increasedreproductive efficiency
of smal-ler colonies (Michener, 1964;
Eischenet al., 1983).
No
significant
differences were obser-ved
in broodproduction between control
andmedicated colonies (Table II). The quantity of honey
in medicated and controlcolonies did
notdiffer significantly
at
the
startof the
test orafter the surplus honey
washarvested (Table II). Medica-
ted colonies and
greater pollen
storesthan did controls. Differences
weresignifi-
cant for
Groups
I and II(both
P <0.05).
Honey production during
thelight
nectarflow
by
control coloniesaveraged 9.9, 8.7,
and 4.3
kg
forGroups I,
II andIII, respec- tively. Medicated
coloniesof
the samegroups produced 12.6,
7.7and
5.2kg, respectively.
These differences were notsignificant. Though medicated colonies had significantly
morebees,
more ofthem attempted
to swarm.This may have redu- ced honey production.
At the beginning of the test, parasite
load scores were
negatively correlated
with
thequantity of bees (r
=-0.54,
P <
0.01 brood (r
=-0.48,
P <0.01 ), honey (r
=-0.23, P
<0.05), and pollen (r
=-0.29,
P <0.01; Table 111). Similar but
smaller correlation coefficients were found for boththe prevalence(w)
ofinfested bees,
andthe percentages
of bees thatwere
bilaterally infested (Table 111). The smaller r-values
for these measuresprob- ably
reflect aless
accurateestimate
of theparasite
loads.In an
attempt
toidentify
factors affect-ing
theperformance
ofcymiazole,
correla-tions were calculated between
colony populations
atthe
startof the
testwith
those
found 30days after the last
treat- ment. Incontrol colonies, ending parasite
load scores in
Group
II werepositively
correlated
with thequantities of bees and
broodand
atthe beginning
of the test(P
<0.05, Table IV). Similar correlations
were
found for medicated
colonies inGroups
IIand III (P < 0.05, Table V). Initial quantities
ofhoney and pollen
wereposi- tively correlated with ending parasite load
scores in
Group
III(P < 0.05).
Anegative
correlation
wasfound between the initial
andending parasite loads of medicated colonies (P < 0.01 ).
Discussion
Medication with cymiazole resulted in
significant mite reduction.
The level of control achieved wasabout
the same inthe
3infestation groups.
Ineach group
= 20%of the colonies did
notrespond typi- cally
tothe medication. Why
thisoccured
is not
clear.
A seriesof
correlations wasmade
in anattempt
toidentify associated
factors. In general, larger colonies had
higher parasite levels, suggesting that
more medicated
syrup should
have beenfed. Additionally, colonies
withlarger honey
reserves at thebeginning of the
test
had higher ending mite populations.
Perhaps
notneeding the additional food,
the
medicated
syrup wasonly stored (Moritz, 1982). This suggests that honey
reserves may
need
to beredistributed
or evenreduced before treating. Should this be imprudent,
atopical application could
be employed (Anon., 1986a).
The rather dramatic mite
population changes
inthe control colonies affected
theefficacy estimates. Mite populations expanded in both the lightly
and moder-ately
infestedcolonies,
butdropped
inthe heavily infested colonies.
Eischen etal.
(1989) observed similar shifts during late winter-early spring. The drop in heavily
infested colonies has
been attributed to thedifferential mortality of severely parasi-
tized worker bees (Eischen
etal., 1989).
A. woodi populations dropped in all medi-
cated colonies. Differences between
trea-ted
andcontrol colonies
werelargest in
the moderately infested
colonies andsmallest in those that
wereheavily infes-
ted. That is, cymiazole
was mosteffective
in
moderately infested colonies and least effective in heavily infested
ones.Why heavily infested colonies should be less
responsive is
notclear. Perhaps
differen-tial mortality of heavily infested workers
simply obscured cymiazole’s potential effi-
cacy.
If this istrue,
itmay
beadvant- ageous
tomedicate infested colonies
inautumn, thereby reducing spring mortality.
Unexpectedly,
treatmentwith cymia-
zole
wasassociated with significant
increases
in beepopulations. Ending
brood
nestsizes
were notdifferent, sug-
gesting that cymiazole promoted longevity
in
bees.
This couldhave been effected by alleviating the
stress of theparasite load
or
by the lengthening life
in a moredirect
way. Eischen (1987) also observed
thatinfested colonies medicated with oxytetra- cycline HCI and fumagillin
in autumnhad
larger overwintering
beepopulations.
In summary,
the level
of controlachie- ved, while
notcomplete, did reduce A.
woodi populations
to at orbelow
the sus-pected
economicthreshold,
viz. 30%of bees infested (Bailey, 1961; Eischen, 1987; Eischen
etal., 1989). Based
onthese observations and others (Dietz
et tal., unpublished)
webelieve colony
dosages could
beraised 20—25%
without risk. This could
probably be best accomplished by raising
theconcentration of cymiazole, along with somewhat grea-
terquantities of syrup, especially
forlar-
ger
colonies. Application
times andtech- niques that foster consumption of treated
syrups should also enhance efficacy.
Acknowledgments
We wish to thank W.G.
Hart,
USDA-ARS Sub-tropical
InsectsLaboratory,
W.T.Wilson,
USDA-ARSHoney
BeeLaboratory,
and H. Shi-manuki,
USDA-ARS Beneficial Insects Labora-tory,
for advice and assistance while in Mexico.Dorset
Hurley provided
technical assistance.We are also
grateful
to the staff and families ofApicultura Cardoso,
whoprovided
agreat
dealof assistance as well as
making
ourstay
in Mexico informative and memorable.Special
thanks are due to W.J.
Schmid, Ciba-Geigy Switzerland,
whoarranged
for financialsupport through
Research Grant 25-21-RC293-108.References
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