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Acarapidosis or tracheal acar iosisP. Garca Fernndez

J unta de Andaluca, Consejeria de Agricultura y Pesca, Centro de Investigacin y Formacin AgrariaDpto. Produccin Animal, Camino de Purchil s/n, 18004 Granada, Spain

Definit ion of tracheal acariosisAcariosis is a parasitic, contagious diseasef the respiratory apparatusof the adult honeybee due tothe mite Acarapis w oodi Rennie. It is a cosmopolitan disease, ranging as an epizooty in North Americaand as an enzooty elsewhere.

General epidemiologyIn 1919, British researchers, while investigating dramatic honeybee (Ap is mellifera L.) colony lossesoccurring on the Isle of Wight, discovered the bee parasite namedarsonemus woodiby Rennie in 1921,later reclassified as Acarapis woodi. Over the next 30 years, it was dentified n numerous Europeancountries(Switzerland,Russia,Scotland,Czechoslovakia,France,Spain). nSpain,thediseasewasfound for the first time in 1949 in the eastern Mediterranean region and its low incidence in this countrywas recently studiedby Orantes et a/. (1997a,b).The mite then spread to the American continent, first to Argentina in 1968. In 1980, it was found in

Colombia and Mexico. More recently, the mites have been found in the USA by Delfinado-Baker (1984)where the honeybees provedo be more susceptible than European honeybees.Outside heEuropeanandAmericancontinents, A. wood hasbeen dentified n Apismelliferaadansoni in Zaire (Benoit, 1959) and Egypt. Shigh (1957) found the mite in India. It is usually assumedthat the mite was introduced into Africa and Asia by. mellifera imported from Europe. In recent reviewsof the status of world bee health, including parasitic mites (tracheal mite and Varroa), Matheson (1993,1996) reported that only the Australian continent remains free of this parasite.Although always considered a disease, the pathological effects of the mite are the subject of muchcontroversy.According oBaileyandBall 1991),noconclusiveexperimentswereundertaken omeasure the effect of the mite until Bailey (1958, 1961), showed that overwintered nfested bees diedsooner than uninfested ndividuals and that the difference became statistically significant from about

March onwards. Field experiments have shown that infested bees in summer die only a little sooner thanuninfested individuals, but they seemed normal until they died (Bailey and Lee, 1959). Gary and Page(1989) concluded from their experiments that "there is a strong indication that tracheal mite infestationsdo not have a detectable economic effect on honeybee colonies when brood-rearing is active and honeyproduction is under way".In contrast, Morgenthaler1 931) suggested that high infestation levels eventually cause colony death.Giordani 1965,1977)observedashortened ife-span n nfestedhoneybeesand a loss of infestedcolonies in springf 30% or more of individuals were infested. Thus, it is apparent that overwintering beeswill die sooner if high evels of nfestation occur, as has recently been demonstrated by Eischen et a/.(1 989) andOtis and Scott-Dupree (1 992). A three year surveyf the incidence of Varroa and the trachealmite in colonies in Wisconsin, conducted between 1992 and 1995, concluded that the numberf colonies

infested with these mites remained fairly constant, with a very high overwintering mortality rate (between10-45%) (Phibbs, 1996).A fact that is now evident, is a general decline in the prevalence of A. woodi in bees in Europe andAsia.BaileyandPerry 1982) ndicateaprogressivedecrease nthe requencyofparasitisationof

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colonies n England and Wales rom 1925 to 1980. The degree of infestation by this mite has alsocontinued odecreaseprogressivelyover he ast ewyears,evenbefore hewidespreaduse oftreatments against the Varroa mite. However, the importancef the disease isnotthe same all over theworld, because acariosis represents a serious problem in some areas, such as North America. The firstoutbreakswerereportedthere n1980and1984andthemitepopulationsrecorded in these nitialinfestations were greater than those reported later in areas where the mites had been present forlongerperiod of time (Otis et al., 1988; Otis, 1990). The colonies seem more susceptible than European ones.RoyceandRossignol1990) uggesthatpersistentparasitismovercomesa olony'sabilityocompensate or osses, eading to ts sudden decline and death. Parasitism s, almost by definition,associated with morbidity and mortalityof the host, and these authors conclude that mortality occurs atevery levelof infestation and increases with density. However, this pointf view is open to debate.

EtiologyPathogenic agentClassificationAcarapis spp. are included in:

Order: AcariformsSuborder: Actinedida (Prostigmata; Krantz, 1978; Lindquist, 1986)Family: TarsonemidaeGenus: AcarapisSpecies:A. woodi Rennie, 1921A. dorsalis Morgenthaler, 1931A. externus Morgenthaler, 1931

Characteristics of the Acariforms orderMites without a visible stigma posterior to coxae I I , with an idiosomal gland complex next to palps,coxae often fused into the ventral body wall, forming coxisternal regions delimited by epimera; numberof legs occasionally reduced.

Characteristics of the Actinedida suborderThe Actinedidasaargeand omplexgroup of terrestrial,aquaticandmarinepredators,phytophagous, saprophagous, and parasitic mites. These mites are weakly or incompletely sclerotisedforms. When an internal respiratory system exists, it may open out through paired stigmata at or near

the bases of the chelicerae. The genital apparatus and its opening are often close to or contiguous tothe venter of the opisthosoma. Sexual dimorphism s rarely pronounced, minor differences in genitalvalvesizeor in internalgenitalstructureoftenprovidetheonlyclues in differentiatingmales romfemales.The ontogenicdevelopment of thesemitesncludesauniquehexapodarva,he tructuraldevelopment in successive stages (nymphs) tends to be gradual and subtle. Additional characteristicswhich apply to Actinedida are that the coxae of the legs are distinguished by a coxal field or they arejoined to the venter, with specialized sensilla=trichobotria) often present on the back. he Actinedidaeare cosmopolitan mites and are virtually unlimited n habitat, their remarkable morphological variety sreflected in the great numberof families and superfamilies with numerous species (Krantz, 1978).

The characteristics of the Tarsonemidae familyThe Tarsonemids are considered mites associated with nsects, other mites, and plants. They aregrouped in over a dozen genera. We refer only to the mites associated with insects and exclusively tothe Acarapis genus with three recognized species, all parasites of beesApisspp.) (Krantz, 1978).

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Three peciesweredistinguishednhe Acarapis genus: Acarapis woodi (Rennie)originallydescribed asTarsonernus woodi (Rennieet al., 1921)],A. externus andA. dorsalis.Rennie foundA , woodi in the prothoracic spiracles and occasionally in the abdominal and thoracic airsacs of bees. It s the causal agent of tracheal acariosis. The remaining two species of Acarapis live

externally on honeybees and are not considered as serious pests (De J ongt al.,1982).Anatomy

The A. woodifemale (Fig. c,d) is 120-180 pm in length whilst the male (Fig. a,b) is 96-102 pm. Thebody is oval, widest between the second and third pair of legs, and is whitish or shiny pearly white, with asmooth cuticle; a few long hairs are present on the body and legs (Sammataro and Needham, 1996). Themorphology of the gnathosoma consists of two cheliceral stylet digits that are grooved medially alongtheir entire length and can be brought tightly together to form a tube-like structure. The cheliceral styletsand abrum may be clamped together during feeding forming a canal allowing the haemolymph to besucked up. Acarapis woodi is an intermittent feeder and, as such, haemolymph and particulate matterwould tend to dry and stick tor clog the stylets following feeding (Bruce and Kethley, 1993).

Biology and life cycleAcarapis woodi lives n the first thoracic tracheae, opening through the prothoracic spiracles andoccasionally n the abdominal and thoracic air sacs of bees. Mated female mites eave the trachea nwhich they developed and migrate to the tip of the bees body hair, awaiting the hair contact of anotherpassing bee. The most susceptible bees are the youngest.tis generally believed that after a bee is ninedays old, the spiracular opening becomes mpassable, preventing the entry of mites. However, it alsoseems that bees less than 4 daysld, called callow bees, are chemically more attractive to female mitesbecause of the presence of certain hydrocarbons. The female mite moves immediately to the spiraclesand into the trachea. A single female mite lays -7 eggs after 2 days. The eggs hatch after3 or 4 days

into a hexapod larval stage, lasting6 to 7 days (Fig. Ie,f). A nymphal stage follows. The males mature11-12 days after hatching and females after 14-15 days (De J ongt al., 1982; Royce et al., 1988; Baileyand Ball, 1991; Sammataro and Needham, 1996). The total duration of the development cycle (at least21 days) may explain the reduced incidence of severe infestations in summer bees, as these have a lifespan of approximately one month. In contrast, overwintering bees may liveor 6 months and more than6 mite generations may be possible in the tracheae, which represents some hundredsf individuals.

Spread and transmissionAll stages (eggs, larvae, nymphs and adults) live exclusively in the tracheae, except mated females,which can leave them to contaminate another bee. However, the survivalf these free females isf a few

hours duration, depending on the temperature, relative humidity or state of nourishment of the mite(SammataroandNeedham,1996).Consequently,thedisseminationofmites nsideandoutsidethecolony, is only due to direct contact between bees.The spread of the tracheal mite s presumably caused by migratory beekeepers and the sale ofinfested packagesof bees and queens, causing a rapid dispersal of the mite, as occurred recently in theUSAandCanada.Withinapiaries, nfestationofonecolonycan esult n he nfestationofotherneighbouring colonies, presumably via drifting bees. t is known that queens, workers, and drones are allsusceptible to nfestation by A. woodi. The mite has a certain preference for drones, and this favoursdisseminationtoothercoloniesandmitepopulationgrowthwithinthecolony.Agreaternumberofmigratory female mites and a greater total numberf all mite stages are found in drones in comparison toworker bees (Dawicke et al., 1992). It can be said that A. woodi behaves like a parasitic disease of anenzootic nature (Bailey and Lee, 1959), except in North America, wheretspreads as an epizooty.

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Fig. 1 Acarapis woodi Rennie. (a) Maledorsal face. (b) Maleventral face. (c) Female dorsal face.(d ) Female ventral face. (e) Larva within its eggshell. (f ) Larva.

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PathogenesisAshortened ifespan ofbees isgenerally elated o heunilateralorbilateral nfestation of thetracheae. Royce and Rossignol (1990) showed that the parasite load of bees is influencedy stress, theage of the bees, the strengthof the colony and the nectar flow, the intensity of which influences the life

span of the foragers.Several factors may contribute to the pathogenic action of A. woodi: (i) as an endoparasitic mite itwithdraws haemolymph from ts host; (i) mites crowding together may block the first pair of thoracictracheae reducing the diffusion of oxygen to the flight muscles and to the brain; and (iii)because of thevectoring of pathogens, such as bacteria and viruses (Scott-Dupreet al., 1995). Bees parasitised by themitearemore usceptible to infection withotherdiseases uchas epticaemia (Pseudornonasapiseptica)and viruses such as chronic bee paralysis virus (CPV) (Bailey, 1965). More recently, VarroajacobsoniandA. woodi have been implicated as potential vectorsf different bee viruses. The ability of.woodi totransmitbeeviruseshasnotbeendemonstratedbutthepresence of the mitesmay beassociated with an increase in the incidence of certain viruses such as acute paralysis virus (APV), CPVor Kashmir Bee Virus (KBV).Acarapis woodicould bean opportunist, as in weakened colonies, without aqueen, more severe infestations appear. Climate also seems to influence mite population dynamics. Incold climates such as England, Switzerland, etc., young bees born at the end of summer can readilybecome infested, because they often are confined to the hive.

Clinical diagnosis, differential diagnosisThere are no specific clinicalymptoms of acariosis, meaning that infested bees appear very similar tohealthy ones. Infested queens can live for many years (Fyg, 1964). During summer, indications attributedto infestation are that some bees are incapable of flying and remain at the hive entrance, some havedislocated wings, and others crawl around n the surrounding vegetation. Generally, A. woodi causeseconomic losses in colonies when the level of infestation exceeds530% of bees, causing a reduction fthe brood area, an increase in the consumption of honey stores, and increased colony mortality (Eischen

et al., 1988). During winter, acariosis may be suspected when many dead bees are observed in or nearthe hive, several months after cluster formation.The other species of Acarapis (A. externus and A. dorsalis) may be distinguished from each other,although they both live externally on the thorax. These three closely related mites are morphologicallydistinct species. Each one attaches tself to a specific, restricted part of the bee. Acarapis externus,known as "the neck mite", is found only in the area where the head and thorax join. Acarapis dorsalislives on the thorax in a groove between the mesoscutum and mesoscutellum.tmay also be found at thebases of the wings and the forepart of the abdomen. A third speciesf external mite,A. vaganshas beenproposed, but this species has been relegated to a synonym of A. externus (Bailey, 1963). These twoexternal Acarapis species have been virtually ignored as regards their life cycle and pathogenic status(Burgettet al., 1989). These authors reported the concurrence of thecarapis species complex at colonyand ndividual host evels, comparing worker and queen nfestation rates in honeybees in North West

America.

Sample collectionGenerally, 25 carefully selected sick bees are enough to ensure diagnosis. However, the size of thesample shouldbe larger for an epidemiological survey in suspected apiaries.

Laboratory diagnosisThe early stages of nfestation probably go undetected, but as the mite population n the tracheae

increases, these become darker in colour because of the accumulation of mite faeces and feeding scars.This discolouration means that mite population is detectable without the aid of a microscope. Althoughmites may sometimes be found in air sacs in the thorax and abdomen, diagnosis can usuallye made bychecking only the prothoracic tracheae. ll stages of development, eggs, larvae and adults may be foundin a trachea at one time (De J ongt al.,1982).

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The standard methodof detectingA,woodi in an individual bee from a sick colony is to remove theprothoracic trunk by dissection to expose the two largest tracheaef the body. The analysis is based on apooled sample of prothoracic trunks from 25-50 sick bees. To estimate the percentage of individualsinfested,beesmay be collected rom hesurfaces of 2 randomlyselectedcombs nside hehive(Calderone and Shimanuki, 1992).A variant of this technique is a thoracic disk dissection or slicing/KOH (Shimanuki and Knox, 1991),wheretrachealmite nfestation evelsaredeterminedusingathoracicdiskobtainedafter ndividualdissection. Between 25-50 thoracic disks are placed in0%KOH in small vials and incubated at5C fortwo days. Once the discs have become clear, the material is mounted between a slide and cover slip inan alcohollglycerine mixture and observed under the microscope. The mite infestation level is expressedas the numberf bees, out of a sampleof 25, that are infested.A variation on the standard methodof dissection is rapid differential staining, which distinguishes thelive mites from the dead. Liu (1995) uses thiazoly blue tetrazolium (MIT solution: 5 mg of stain / 5 mldistilled water) to perfuse the tracheae mounted on a glass slide, over which a cover slip is placed. Thestaining reaction takes place immediately, or after a few seconds, precipitating at the site where there isenzymatic activity. The live mites take on a bright purple colour because they imbibe the stain solution,

whilst the dead mites turn a greenish yellow.A bulk extraction technique can be used as a general screen for the diagnosis of acarine disease(Colin, 1979). In this method the wings and the legs are removed from the thoraces, which are placed inan homogeniser and ground 3 times for several seconds at 10,000 rpm. A large number of honeybeesamples, comprising 100-200 bees, can readily be examined. The triturate is strained through a.8 mmmesh sieve, which is rinsed through with water, the final volume being about 50 ml. The suspension isthen centrifuged at about500rpm for5 minutes, the supernatant discarded and the sediment observed.A few drops of pure actic acid are added to the preparation and eft for 10 min, causing the ysis ofmuscle cells. The mites can be seen and counted under a microscope. The extraction technique is notonly rapid (15min), making it possible to process a large number of samples of bees, butt is also muchmore sensitive than the dissection technique, revealing the presencef weak infestations and t could beused in epidemiological surveys.More recently other methods have been used in the diagnosisfA. woodi.:(i) A practical enzyme-linked mmunosorbent assay (ELISA) has been developed by Gordon et al.(1 993) using bee samples stored in saturated sodium chloride solution>30% pickling salt). The resultsfthe ELISA showed a good correlation with the dissection method n samples that had over 5% miteinfestation (number of infested bees per 100 bees). This method can analyse large numbers of apiarysamples with approximately one tenth of the abour required by the conventional dissection method.Moreover, the costs are lower and there is more specificity and sensitivityf results.(i) Mozes-KochandGerson 1997)describedamethodbasedonthevisualization of the argeamounts of guanine found in the mite faeces. After grinding the bee thoraces and cell lysis, the extract is

centrifuged and the supernatant deposited on TLC plate. Guanine spots are visualized underV light.The sensitivityof the method is similar to thatf dissection.

Treatment and prophylaxisThe methods of control used against.woodiare those classically used against mites; acaricides arevery effective. However, the applicationf these products has some disadvantages, such as the cost, therisk of contaminating stored honey, the risk to bees and the riskf the development of mites resistant tothe acaricides.In Europebetween 1930 and 1940,nitrobenzeneumigatingmixtureswerewidelyusedbybeekeepers, until their efficacy and safety came to be questioned. In 1960 tests were carried out withnumerous acaricide products; of these, menthol appeared to be the most effective, with the additionaladvantage of being a fairly harmless producto bees and one which does not contaminate honey.



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The spread of A. woodi in North America in 1984 has led to a renewed interest in the applicationofmenthol. Best results are obtained in spring time, with doses of 50 g enclosed in a porous plastic screenpacket being placed over the cluster. This method was adopted by the USA Environmental ProtectionAgency in 1989 andby the Agriculture Ministry f Canada in 1992 (Delaplane, 1996).The use of alternative products against Varroa jacobsoni such as formic acid and menthol (Nelson,1994; Nelsonet al., 1994) or vegetable oils and menthol (Delaplane, 1992) has been successful againstA. woodi.The formula recommended for applying formic acid is 30 ml of 65% acid in three applications atweekly intervals during the spring (Nelsonet al., 1994). Sammataro et al. (1994) proved the efficiency ofoil patties (solid vegetable oil and white sugar) administeredn 300gamounts per colony.The different susceptibilitiesof bees to tracheal acariosis, which presents fairly stabilised infestationsin Europe and Asia, n contrast to the USA and Canada, means that programmes of selection andimprovement in the tolerance f bees to the disease, like those implemented against varroosis, have yetto be established.

ReferencesBailey, L. (1958). The epidemiology of the nfestation of the honey bee Apis mellifera L, by the miteAcarapis modi (Rennie), and the mortality of infested bees.arasitology, 48: 493-506.Bailey, L. (1 961). he natural incidence f Acarapis woodi (Rennie) and the winter mortality of honey beecolonies.Bee World,42: 96-1 O.Bailey, .1963). lnfectiousDiseases fheHoneyBee. LandBooks, ondon.Bailey, L. (1965). Susceptibility of the honeybee, Apis mellifera Linnaeus, nfested with Acarapis wood

(Rennie) tonfection by airborneathogens. Journalfnvertebrateathology, 7:41143.Bailey, .andBall,B.V.1991). HoneyBeePathology. 2ndedn.AcademicPress, ondon.Bailey, L. and Lee, D.C. (1959). The effect of infestation withAcarapis wood (Rennie) on the mortality ofhoney bees. ournal of Insect Pathology,1 15-24.Bailey, L. and Perry, J.N. (1982).Thediminishedncidence of Acarapis woodi (Renne)Acari:Tarsonemidae) in honeybees, Apismellifera L. (Hymenoptera:Apidae),nBritain. Bulletin ofEntomological Research,72: 655-662.Benoit, P.L.G. (1959). The occurrence of the acarine mite,carapis woodi in thehoneybee in the BelgianCongo. Bee World,40: 156.Bruce,W.A.andKethley, .B. 1993).Morphologyofhegnathosomaof Acarapis woodi (Acari:Acaripidae). lnternational Journalof Acarology, 19: 243-247.Burgett, D.M.,Royce, .A.andbay,A.1989).Concurrenceofhe Acarapis species omplex(Acari:Tarsonemidae) in a commercial honey-bee apiary in the Pacific Northwest. Experimental andApplied Acarology,7:251 -255.Calderone, N.W. and Shimanuk, H. (1992). Evaluation of sampling methods for determining infestationrates of tracheal mite (Acarapis woodi R.) in colonies of the honey bee (Apis mellifera): spatial,temporal and spatio-temporal effects.xperimental and Applied Acarology,5: 285-298.Colin, M.E. (1979). A new echnique ordiagnosisofAcarine nfestation nhoneybees. Journal ofApicultura1 Research,18: 222-224.Dawicke, B.L., Otis, G.W., Scott-Dupree, C. and Nasr, M. (1992). Host preference of the honey beetracheal miteAcarapis woodi Rennie). Experimental and Applied Acarology,5: 83-98.

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De ong,D.,Morse,A.andEickwort,G.C. 1982).Mitepestsofhoneybees. AnnualReviewofntomology,27: 229-252.Delaplane,K.S. 1992).Controlling rachealmites Acari:Tarsonemidae) ncoloniesofhoneybees(Hymenotera: Apidae) with vegetable oil and menthol. Journal of Economic ntomology, 85: 2118-21 24.Delaplane, K.. (1996). Practical Science-Research helping beekeepers I.Tracheal mites. Bee World,77: 71 -81.Delfinado-Baker, M. (1984).Acarapis woodi n the United States.merican Bee Journal,124: 805-806.Eischen, F.A., Cardoso-Tamez, D., Wilson, W.T. and Dietz, A. (1989). Honey production of honey beecolonies infested with carapis woodiR. pidologie, 20: 1-8.Eischen, F.A., Wilson, W.T., Hurley, D. and Cardoso-Tamez, D. (1988). Cultural practices that reducepopulations of Acarapis woodiR. merican Bee Journal,128: 209-211.Fyg, W. (1964). Anomalies and diseases of the queen honey bee.nnual Review of Entomology,9: 207-224.Gary, N.E. and Page, R.E. (1989). Tracheal mite (Acari: Tarsonemidae) nfestation effects on foragingand survivorship of honey bees (Hymenoptera: Apidae). Journal of Economic ntomology, 82, 734-739.Giordani, G. (1965). Laboratory research on Acarapis woodi Rennie, the causative agent of acarinedisease of honeybees (Ap is mellifera L.), Note 2.Bulletin Apicole,6: 185-203.Giordani, G. (1977). Facts about Acarine mites. n Proceed ings of he XXVlth nternational CongressApiculture, Adelaide. Apimondia Publishing House, Bucharest, pp. 459-467.Gordon, A.G., Nelson, D.L., Olson, P.E. and Rice, W.A. (1993). The "Elisa" detection of tracheal mites inwhole honey bee samples. merican Bee Journal,133: 652-655.Krantz, G.W. (1 978).Manual of Acarology.2nd edn. Oregon State UniversityBook Stores, Inc., Corvalis,Oregon.Lindquist, E.E. (1986).Theworldgenera of Tarsonemidae(Acari:Heterostigmata):amorphological,phylogenetic,ndystematicevision,witheclassification of family-groupaxanheHeterostigmata.Mem. Entomol. Soc. Canada136, 517 pp.Liu,T.P. 1995).A apiddifferentialstaining echnique or iveanddead rachealmites. CanadianBeekeeping, 18: 155.Matheson, A. (1993). World bee health report.ee World,74: 176-212.Matheson, A. (1 996). World bee health update.ee World,77: 45-51.Morgenthaler,O. (1931). Ein Versuchs-Bienenstand fur Milbenkrankheit m Berner Seeland und einigedort gewonnene Ergebnisse.Schweizerische Bienen-Zeitung,53: 538-545.Mozes-Koch, R. and Gerson, U. (1997). Guanine visualization: a new method for diagnosing trachealmite infestationof honey bees.Apidologie, 28: 3-9.Nelson, D.L. (1994). Control of the honey bee tracheal mite with menthol and formic acid. IX Intern.Acarology Congress(reprint in anadian Beekeeping,18: 136-1 37).Nelson, D., Mills, P., Sporns, P., Ooraikul, S. and Mole, D. (1994). Formic acid application methods forthe controlof honey bee tracheal mites. ee Science,3: 128-134.

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Orantes Bermejo, F.J ., Gonzlez Mejas, A. and Garca Fernndez, P. (1997a).Acariosis Intratraqueal.Incidencia actual en apiarios del Sur de Espaa.ida Apicola,81:30-35.Orantes Bermejo, F.J ., Bentez Rodrguez,R., and Garca Fernndez, P.(1997b). scientific note on thecurrent low levels f honey bee tracheal mite in southern Spain.pidologie,28: 149-1 50.Otis, G.W. (1990). esults of a survey on the economic impactf tracheal mites.American Bee Journal,130: 28-31.Otis, G.W., Bath, .B. Randall, D.L. and Grant,G.M. (1988). tudies of the honey bee tracheal mite(Acarap is woodo (Acari: Tarsonemidae) during winter. anadian Journal of Zoology,6: 2122-2127.Otis, G.W. and Scott-Dupree, C.D. (1992). ffects of Acarapis w oodi on overwintered coloniesof honeybees (Hymenoptera: Apidae) in New-York.ournal of Economic ntomo/ogy,5: 40-46.Phibbs, A. (1996). hree year survey of Varroa mite and Tracheal mite nfestations of honey bees nWisconsin.American Bee Journal, 36: 589-592.Rennie, J ., White, P.B. and Harvey, E.J . (1921).sle of Wight disease in hive bees. Transactions of theRoyal Society of Edinburgh,2: 737-779.Royce, L.A. and Rossignol, P.A. (1990).Epidemiologyof honey bee Parasites. Parasitology Today, 6:348-353.Royce, L.A., Krantz, G.W., bay, L.A. and Burgett, D.M. (1988). ome observations on the biology andbehaviour of Acarapis w oodi and Acarapis dorsalis in Oregon. In Africanized Honey Bees and BeeMites, Needham, G.R. et al.(eds). Ellis Horwood, Chichester, pp.98-505.Sammataro,D.,Cobey, S., Smith,B.H. ndNeedham, G.R. (1994).Controllingrachealmites(Acari:Tarsonemidae) in honeybees (Hymenoptera: Apidae) with vegetable oil. Journal of Economic

ntomology,87: 91 0-91 6.Sammataro, D. and Needham, G.R. (1996).How oil affects the behaviorf tracheal mites.American BeeJournal, 136: 51 1-51 4.Scott-Dupree, C., Ball, B.V.,Welsh, O. andAllen,M. (1995).An investigationntohepotentialtransmission of virusesby hehoneybee rachealmite (Acarapiswoodi R.) to honeybees. InCanadian Honey Council es. Symposium Proc.,pp. 15-24.Shigh, S. (1957). carine disease in the Indian honey beeAp is ndica F.). lndian Bee Journal,19: 27-28.Shimanuki, H. and Knox, D.A. (1991).Diagnosis of honey bee diseases. USDA, Agric. Handbook. No.AH690.

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