HONEY BEE MITES (ACARINA), A CHALLANGE TO BEEKEEPING INDUSTRY-A REVIEW

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1 Agric.Re~.22(3/4l: ,2001 HONEY BEE MITES (ACARINA), A CHALLANGE TO BEEKEEPING INDUSTRY-A REVIEW B.N. Putatunda, K. Aggarwal and R.B. Mathur Acarology Section, Deptt. of Zoology Haryana Agric. University, Hisar , India ABSTRACT There is a large array of mites tht has been found to be associated with bees, but it is a fact that out of the large number of bee mites known only a few of them are really a serious pest. The most important bee mites are Varroa jacobsoni, Tropilaelaps cjareae and Euvarroa' sinhaithat are external parasites whereas Acarapis woodi is the internal parasite that infests the respiratory organ of bees. Extensive research is called for, for better understanding of bee and bee mites so as to chalk out an Integrated Pest Management programme of bee parasitic mites with the incorporation of predatory mites. Also intensive training of bee farmers in the proper management of healthy bee colonies and in detection and control of mites with simple preventive and hygienic method is essential. A honeybee hive harbours a wide di- these are, ~hort flight range, tendency to swarm versity of acarofauna, largely because of the and abscond, susceptibility to predators like wax diverse food and microhabitats it offers. A large moth and poor honey guthering capacity. To number of the mites encountered in a bee-hive overcome these problems, the more producare mere incidentals (e:g. some Ascids, tive EuropeanspeciesA. melli/era was repeat Scutacarids etc.), while some are facultativeedly introduced <iuring the last century in Tropiassociates, for instance Acarids. Still others cal Asia instead of improving the.native speform parasitic associations with their Apis cies. However, these attem~ failed because host(s) and are obiligatory in nature. The lat- rather unexpectedly A. melli/era -fell prey to ter constitute an economically important group local pests and predators, of which T. c1areae since they cause extensive damage to their has turned out to be the most dangerous. On hosts. Of late, the phrase 'honeybeen mites' the other hand A. cerana showed resistance to is being restricted to only the obligatory para- local pests and predators mainly because over sites and includes three most important spe- the time, they co-evolved in nature. With the cies- VarroaJacobsoni, TropUaelapsdareaeand introduction of A. melli/era in Asia and V. Euvarroa sinhai. While varroa achieveda pest Jacobsoni in Europe, theasian mites having a statusin Europeduring seventies, Tropilaelaps benign existence with their Asian hosts, sudcame into lime light when it was identified as a denly proliferated and became virulent. As a causative agent behindthe failure of newly es- result Varroa achieved a post status in Europe tablished Apis melli/era based bee-keeping in and Tropilaelaps in Asia. The victim in both South-East Asia. Tropical Asia is rich in Apis the geographical regions is A. mellifera. Table species, however, the sole native hive bee A. 1 shows the mite species and their known honcerana suffers from many handicaps. Some of eybee parasites. Retired Table 1. Honeybee mites and their known Apishosts. Mite species Apishosts 1. Ikrroa jucobsoni Apis cerana, A. Koschevnikovi, A. mel/ifera. 2. V. underwoodi A. cerana 3. Tropi/ae/aps c1areae A. dorsata, A. mel/ilera, A. cerana, A. /aboriosa, A. Dorea. 4. T. koenigerum A. dorsata, A. /aboriosa A. me/ulera, A. cerana 5. Euvarroa sinhai A. Dorea, A. andrenilormis, A. mel/ilera, A. cerana. 6. E. haryanensis A. Dorea

2 206 AGRICULTURAL REVIEWS According to Koeniger (1990), mites that the suborder Astigmata (Table 2) includes form natural associations with some of their only facultative associates as scavengers. On honeybee hosts, for instance cave dwelling spe- the other hand, the Prostigmatid (Table 2) and cies A. cerana and A. Koschevnikovi playing Mesostigmatid mites (Table 2) are either faculhostto V jocobsoni, thetwo dwarf honeybees tative/obligatory associates or are phoretic A. florea anda. andreniformis sharing E. sinhai and/or parasitic in nature. He has also reand the two gaint honeybees A. dorsata and viewed the mites associated with stingless bees A. laboriosa harbouring closely related (Table 3), where also the mites have the same Tropilaelaps species. This natural distribution type of ecological interactions with the bees. of mites which corresponds to the known sys- However, the work done at the Departmentof tematic position of their honeybee hosts indi- Zoology, Haryana Agricultural University, Hisar cates a long co-evolution between bees and has not been included in the above report (Abrol their parasitic mites. Koeniger(1990) consid- and Putatunda 1995, 1996, Abrol etai., 1994, ers E. sinhaito be the most advanced because Bhaskar and Putatunda 1989, Putatunda it breeds only inside the drone brood cells. Also, 1996}. A survey of ectoparasites/associated A. florea workers appear to recognize the in- mites of social and solitary bees in Haryana festation to some extent. Sometimes heavily (Kapil etai., 1985 Putatunda and Kapil 1998, infested combs were found to be abandoned 1995, Putatunda et al., 1983) has yielded 49 and sometimes both the mites and the be~ species new to science out of a total of 90 stageswerefound dead inside the sealed brood species (Table 4). An important information celkls (Aggarwal and Mathur, 1990). The mite that emerges out of the above surveys is that E. sinhai was postulated as being capable of Xylocopa species in India and bumble bees elseinfesting A. mellifera by Aggarwal and Mathur where constitute bee mite pools. Through vari (1990) and now the laboratory experiments ous interactions with flowers, other insects and have shown that the mite can survive and re- other bees during robbery, the mites are transproduce on worker brood of A. mellifera mitted from one kind of beeto another. These (Mossadegh, 1990). This adds a nbew dimen- inter-transmissions, in the long run, are likely sion to the economic importance of E. sihnai. to establish solitary bee parasitic mites on the b. h h h d h social bees as well. The above surveys, though V. Jaco som on t e ot er. an sows compreh' enslve are not exh' austlve and there a three-pronged host-parasite relationship. may be many more associated mites which are T. calareae also has a multi-faceted yet to be discovered. relation~hip with i~s A1?i~ host (s). Contr~ry to Interactions of bee mites between the earher held behef, It IS equally damaging to themselves and with Apis host(s): As menits adaptive and natural hosts. The difference tioned earlier sometimes two species of mites lies in the modes of defence, A. dorsata being share a common host while at othe times the wild ~ee, can aban?on an heavily infested mites remain host spe~ific. Simultan:ous incombwhtle thedomesticated A. melli/era stays f. f A 1''''. b 1.. h hi d ff 1 (A al 1990) estabon 0. melljera colomes y T. c areae In t e ve.an su ers osses ggarw,. and V. jacobsoniwas noted by Delfinado (1963) Taxonomic status: The relationship and Burgett etai. (1983).. It was observed that of mites with honey bees is highly variable be- in cases of multiple parasitism occurring in cause of the diverse acarofauna drawn from single brood cells, only T. clareae could prosuborders Astigmata, Prostigmata and duce a viable progeny. In recent surveys A. Mesostigmata. In a survey of existing litera- melli/era colonies in Haryana were found to ture on honeybee mites, Eickwort (1988) shows be infested with three species of ectoparasitic

3 Vol. 22, No. 3/4, mites viz. T. clareae, E sinhaiand V. jacobsoni. florea by T. clareae and E Sinhai, the level of In all the cases, T. clareae population was most T. clareae infestation was always very low, genpredominant followed by low population of E erally not exceeding 0.1 per cent, that of E sinahi and V. jacobsoni(sihag, 1988). In some sinhai was somewhat higher (Kapil and instances of concurrent parasitization of A. Aggarwal, 1987). Table 2. Mites associated with honey bees (Api.sj Taxon Hosts (Api.sj Ecology Range ACARIFORMES-ASTIGMATA Glycyphagidae Glycyphagus domesticus mellifera f,s cosmopolitan G. destructor mellifera f,s cosmopolitan Carpoglyphidae Carpoglyphis lactis mellifera f,s cosmopolitan Suidasiidae Suidasia pontifica (=medanensis) cerana, florea f,s pantropical Acaridae Ac.:rrussiro mellifera f,s cosmopolitan A. immobilis mellifera f,s cosmopolitan A. farris mellifera f,s cosmopolitan Tyrophagus putrescentiae mellifera f,s cosmopolitan T. longior mellifera f,s cosmopolitan T. palmarum mellifera f,s cosmopolitan Tyrolichus casei mellifera f,s cosmopolitan Forcellinia gal/erie/la mellifera o?,s cosmopolitan Pyroglyphidae Dermatophagoides pteronyssinus mellifera,cerana f,s cosmopolitan ACARIFORMES-PROSTIGMATA Cheyletidae Cheyletus eruditus mellifera. f,pr cosmopolitan Erythraeidae Leptussp. mellifera i,pa cosmopolitan Tarsonemidae Acarapis dorsalis mellifera o,pa cosmopolitan A. extemus mellifera o,pa cosmopolitan A. woodi mellifera,cerana o,pa almost cosmopolitan Pseudacarapis indoapis cerana o,ph Asia Tarsonemus apis mellifera o,ph cosmopolitan Scutacaridae Imparipes apicola mellifera i,s American Scutacarus acarorum mellifera i,s almost cosmopolitan Pyemotidae Pyemotes ventricosus mellifera i,pa cosmopolitan PARASITIFORMES-MESOSTIGMATA MacrocheUdae Macrocheles glaber mellifera i,pr Europe M. muscadomesticae melhfe~a i,pr cosmopolitan Ascidae Melichares agilis mellifera i,pr cosmopolitan Proctolaelaps phygmaeus mellifera i,pr cosmopolitan Lasioseius berlesei (=muricatus) mellifera i,pr cosmopolitan (Contd.

4 208 AGRICULTURAL REVIEWS 1 Blattisocius dentriticus B. tarsalis Parasitidae Parasitus fucorum Ameroseiidae Neocypholaelaps apicola N. ampuuula N. indica N. novaehollandie N. favus Afrocypholaelaps africana Edbarellus tonganus Laelapidae MeUttiphis a/vearius Tropilaelaps cjareae T. Koenigerum Varroidae (=Laelapidae s.l.) Euvarroa sinahi Ikrroa jacobsoni mellifera i,pr cosmopolitan mellifera i,pr cosmopolitan mellifera i,pr Europe carana f,ph Asia carana f,ph Asia cerana, dorsata, f,ph Asia florea, mellifera mellifera f,ph New Zealand mellifera f,ph Asia, Europe mellifera f,ph Africa, Asutralia mellifera f,ph Tonga mellifera Europe New Zealand mellifera, florea, o,pa Asia dorsata, cerana dorsata o,pa Asia florea cerana, mellifera o,pa o,pa i= incidental, f= facultative, o=obligatory, s-scavenger, pa=parasite, pr=predator, ph=phoretic. Asia Asia,, Africa, Europe Table 3. Mites associated with stingless bees (Meliponinael Taxon Hosts Ecology Range PARASITIFORMES-MESOSTIGMATA Macrochelidae Trigonholaspis salti Grafia trigonarum G.. ama/theae G. columbiana HolostaspeUa polyornata Family? MeJiponapachy pauidus Ameroseiidae Neocypholaelaps phooni Afrocypholaelaps africana Laelapidae Hypoaspis meliponarum H a/phabeticus H favosus Stevelus amiculus Melittiphisoides apiarium spis debijipes EumeUitiphis mejlitus Zontia meliponensis Uro~ercon meuttophilus Neohypoaspis ampliseta. Meliponine Lestrimellita f?,ph f,ph o?,pr? o,pr Asia Africa Mexicon, Panama Africa Panama (Contd.

5 Vol. 22, No. 3/4, Hunteria brasiliensis BisternaUs mexicanus B. rettenmeyeri B.lormosus B. camargoi B. trigonarum,. Lestrimellita o,pr Mexicon, Panama, Uropodidae UropUtana meliponarum Urcx:JisceUa centroamericana Diplogyniidae Calaenosthanus trigonophilus Triplogyniidae Triplogynium irapora ACARWORM~ASTIGMATA GaudieIlidae Platyg/yphus maiayanus Gaudiella minuta Partamonacoptes brasiliensis coptes camargoi Meliponopus palpiler Hemisarcoptidae MeUponocoptes nidicolus M. Scutatus M. orphanus MBJjponoecius flechtmanni ACARIFORMES-PROSTIGMATA Tydeidae Proctoydeus therapeutikos P. partamonae P. alveari MeUssotydeus macrosolenus Ereynetidae Ereynetes meliponae 'bee nest" o?,?. o,s O,s O,s Asia i= incidental, f=facultative, o=obligatory, s=scavenger, pa=parasite, pr=predator, ph=phoretic. Table 4. Parasite (Mite) - Host (Bee) relationship in India Mrre Ho& 1 2 Astigmatid Mites CaIoglyphus indica' Tyrophagus similis vologen Sennertia (RobustieUa) Sennertia. (Sennertia) Sennertia (RoundieUa) Sennertia (AnterosuckereUa) Sennertia (E1ongatieUa) Sennertia (A) asiaticus Sennertia (A) frjdolini Sennertia (E) haryanaensis Sennertia (E) hissarensis Sennertia (E) orientaus Sennertia (E) tropicaus..:.. Megachile lanata cumb (1) M. lanata (2) X. fenestrata Pithitis smaragdula X. pubescens Bee Bee Xylocopa' pubscens Xylocopa lenestrata XylocQpa pubescens Xylocopa pubscens Xylocopa lenestrata (Contd.

6 210 AGRICULTURAL REVIEWS 1 5ennertia (Rob) bilashi Sennertia (Rob) boharti 5ennertia (Rob) cannamelai 5ennertia (Rob) karli Sennertia (Rob) kerri 5ennertia (Rob) megachili Sennertia (Rob) miechenari 5ennertia (Rob) oldrichi 5ennertia (Rob) parkeri 5ennertia (Rob) sardari Sennertia (Rob) stechei 5ennertia (Rob) thomasi Sennertia (Round) atwali Sennertia (Round) engelsi 5ennertia (Round)!reei Sennertia (Round) koenigeri 5ennertia (Round) nunezae 5ennertia (Round) sakagami 5ennertia (Round) shueli 5ennertia (5) gordoni 5ennertia (5) parasiticus 5ennertia (5) pithiti Kuzinia evae Kuzina woykei Acaridae Acaridae Acaridae Carpoglyphus lactis Sennertia sp. Vidia muttooi Vidia fletcheri 5chulzea halicti 5chulzea sp. Schulzea indica Schulzea orientalis Cryptostigmata Obribatidae Bdellidae Stigmaidae Cheletophyes deodikari Cheletophyes harnaji CheJetophyes haryanaensis Cheletophyes newtoni Cheletophyes orientalis Cheletophyes ruttneri Cheletophyes shendi Chelletus malaccensis Parascutacarus indicus Paracultacarus indicus Euteranychus sp. Pyemotidae Prostlgmata 2 Megachile lanata Megachile lanata Xylocopa finestrata Meqachile lanata Xyiocopa fenestrata Megchile lanata Pithitis smaragdula Pithitis smaragdula Pithitis smaragdula Pithitis smaragdula Bumble bees Apis florea Ceratina sp. Halictussp. Megachile flavipes Megachile sp. of Bee Halictus sp. Hanctine bees Halictus sp. Hoelictreis sp. Megachile cephalotus Halictus sp. (Contd.

7 VoL 22, No. 3/4, Tarsonemus confuses Acarapsis sollers Acarapsis sollers Parascutacarus indicus Parascutacarus indicus Eutetranyches sp. Leptussp. Cheletophyes sp. Cheletophyes sp. Trombidaidae Eutetranychus sp. Euvarroa sinhai Tripilaelaps clareae Tripilaelaps clareae Tripilaelaps clareae Phytoseiidae lhlrroa jacobsoni Macrocheles sp. Allodinychus flagelliger Euvarroa haryanensis Delfinadoidae Delfinado Delfinado bhaskeri Delfinado kapili Delfinado indica Delfinado bakeri Melliliphis alvearius Mesostigmatid 2 Halictine bees Malictus sp. Apis florea Apis mellifera Apis mellifera Apisflorae Apis cerana indica (Allahabad) Xylocopa spp. Xylocopa spp. Xylocopa aestuenis Apis mellifera The mites are known haemolymph feeders. When the mite sucks haemolymph 30 to 40 per cent of which is protein, it reduces the host bee's resistance to diseases. In ValToa diseased bees the total protein content was found to be 20.4 per cent lower than in healthy bees (Sadov, 1976). In case of parasitized A.. melfifera drone brood there was a reduction in the content of total protein in the haemolymph that was related to the intensity of Varroa invasion (Glinski and Jarosz, 1984). Worker and drone brooos were found to react differently to mite infestation (Weinberg and Madel, 1985). Varroa shows a high degree of adaptation, since it was found to selectively resorb honeybee haemolymph proteins without any digestive degradation. Also, the host proteins could be localized in the growing mite oocytes (Tewarson, 1985). According to some reports, mite depends upon host juvenile hormone (JII III) for its reproduction ( Honel and Koeniger, 1986). All the three mite species exhibit some degree of host-specificity as reflected in hostparasite relationships. It has been contended byt Griffiths et al. (1983) that the exclusive association of ValToa with drone brood of A. cerana probably has a physiological basis and resistance factors in bee haemolymph may be important. Koeniger (1985) believes that A. melfikra has no natural resistance to be mites like U jacobsoni and T. clareae. On the basis of observations in Sri Lanka where A. melli/era is not present and where V jacobsoni is restricted to A. cerane, T. koenigerum to A. dorsata and E. sinhaito A. florea, it is felt that the natural barriers which prevent transmission between host species are effective here, although contact between the three mite species occurs frequently. It is, therefore, pos-

8 212 AGRICULTURAL REVIEWS sible that mites are adapted e.g. to the species specific structure of the bee's cuticle or haem6lymph composition and that this contributes to other (as yet unknown) natural barriers (Koeniger and Koeniger, 1985). Control: Chemicals like chlorobenzilate (Folbex R) were not found to be effective control for mites like V. jacobsoni and T c1areae, though it killed many mites (Laigo and Morse, 1968; Atwal and Goyal, 1971). Terramycin also did not give effective control but a light dusting with sulphur every month was found to controlthe infestations completely. (Atwal and Goyal, 1971). In Thailand, terramycin proved virtually inffective though 1: 1 mixture of sulphur and napthalene had limited success (Burgett et al., 1983). Formic acid exposed in honeybeecolonies infested with T c1areae eliminated this mite within 6 to 13 days (Garg et al., 1984). Chlorobenzilate and Menthol fumigations of infested A. melliiera colonies did not eradicate the mite even after 4 fumigations, althoughthe mite population was considerably reduced. This treatment should be carried out in July or August, when the mite population is lowest and there is less brood in the colonies (Garg and Sharma, 1988). Woyke (1985) described three methods for controlling T c1areae in A. meiiiiera colonies without medication. \ A fee control studies have been carried outin coloniesinfested with both T c1areae and V. jacobsoni. An integrated control method. was described by Nyein and Zmarlicki (1982) which involved caging the queen for 21 days, uncapping dead brood, feeding to stimulate hive cleaning, and fumigating with phenothiazine. Woyke (1987) reported that Amitraz was more effective than Phenothiazine against both the mite species, killing 95.7 per cent of V. jacobsoni and 79.2 per cent of T c1areae. For V. jacobsoni, the interest has shifted from chemical to non-chemical biocontrol methods. Similar is the case with T c1areae. As far as E. sinhai is concerned, no control methods have yet been tried. Problems associated with honeybee mites: The honeybee mites mainly V. jacobsoni and T c1areae have caused extensive damage to beekeeping industry in many parts of the world. The losses are particularly well documented for V. jacobsoni. There are no recorded observations of the damagecaused by T dareae to its native. host A. dorsata. However, when A. meiiifera was introduced in 1960s into the plains of Punjab and lower hills of Himachal Pradesh, it was found to be heavily infested with T c1areae (Stephen, 1968). In some of the introduced colonies in Punjab upto 50 per cent of the brood was found dead (Atwal and Goyal, 1971). T c1areae has now been reported from almost all those beekeeping areas of India, where A. mellifera has been introduced (Sihag, 1988; Suryanarayana and MUjumdar, 1988; Shah and Shah, 1988). According to Suryanarayana (1988), Tropilaelaps causes serious production losses in Jammu and Kashmir as its number in a colony grows with increase in brood during preflow and flow seasons. Another report mentions that Tropilaelaps infestation affects 'lahi' production of A. meiiifera in Golapar near Haldwani (U.P.). In 12 of the 26 colonies in this area, brood strength was reduced from 6 frames to 2 frames and hundreds of new born bees were wingless and underdevebped and died soon (Suryanarayana and MUjumdar, 1988). In Afghanistan, 90 per cent of the A. meiiiiera colonies were lost due to T c1areae parasitism (Woyke, 1984). In Thailand, 10 to 90 per cent of the worker brood was parasitized in infested A. melliiera colonies. Parasitized larvae were usually unable to complete development to the adult stadium and infested bees on emergence as adults often had de-

9 - formed or vestgial wings. In populous colonies of A. melli/era, heavily infested larvae and pupae were seen abandoned near the hive entrance apparently by the house-cleaning bees (Burgett etal., 1983). Future projections: Despite several - papers onhoney been mites especially VaJToa, there are still many gaps in our knowledge particularly in the areas of biology, reproductive potential, resistance mechanism, biocontrol methods, dispersal etc. Future studies should concentrate on some of the following areas: i) Reproductive capacity of the female mites. ii) Resistance mechanism that results in differential infestation of the honeybee colonies. iii) Search for efficient predators for eventual use as biological control agents. A recent report by Sudarsanam and Murthy (1990) mentions that pseudoscorpion, Ellingsenius Vcl.22,No.3/4, indicus is a voracious feeder of the adults of VaJToa Jacobsoni. It also reportedly feeds on wax moth larvae in the bee-hives. There is a need for more detailed research in this area. iv) Mechanisms involved in mite dispersal. v) Taxonomy of the mites associated with bee vi) hives shall have to be continued. Sulphur dusting is largely recommended for control of Tropilaelaps. It is feared that liberal and indiscriminate use of sulpnur can contaminate honey, bee-wax etc. beyond permissible limits. Thus, there is a need to monitor honey and wax samples for sulphur residue. ACKNOWLEDGEMENTS Authors are thankful to authorities of CCS HAU and rcar New Delhi for providing facilities and funds. REFERENCES Abrol, D.P. and Putatunda, B.N.(1995). Curro Sci. 68:90. Abrol, D.P. and Putatunda, B.N. (1996). Sci. Cult. 62 (1&2):59. Abrol, D.P. etal. (1994). Curro Sci. 66:105. Aggarwal, K. (1990). Ph. D. Thesis, Haryana Agric. Univ., Hisar. Aggarwal, K. and Mathur, R.B. (1990). In: Euvarroa sinhai and Apis f1orea. In Social Insects and the Environment (Eds. Veeresh et al.) Oxford & IBH Pub!. Co. Pvt. Ltd. New Delhi. pp Atwal, A.S. and Goyal, N.P. (1971). J. Apic. Res. 10: Bhaskar, S. and Putatunda, B.N. (1989). In: Progress in Acarology-II. In: (Channabasavanna, G.P. and Viraktumath, CA Ed.) Oxford and IBH New Delhi 484 pp Burgett. M., Akratannakul, P. and Morse, R.A. (1983). Tropilaellfps c1areae: a parasite of honebees in Sout-East Asia. Bee WId. 64: Delfinado, M.D. (1963). J. Apic Res. 2: Eickwort, G.C. (1988). The origin of mites associated with honeybees. In"Africanized honeybeesand bee mites" (Needham et a/. Ed.) Ellis Horwood Ltd., England, pp Garg, R. and Sharma, O.P. (1988). Indian Bee J. 50: Garg, R. eta/. (1984) Am. BeeJ. 124: Glinski, Z.E and Jarosz, J. (1984). Apidologie. 15: Griffiths, DA (1983). In: IkJJro:l jacobsoro Otd. affecting hol'je!}jees: present status arxi needs (Cavalloro, R. Ed.) pp Hanel, H. and Koeniger, N. (1986). J. Insect Physiv/. 32: :--. Kapil, R.P. and Aggarwal, K (1987). Expt/. App/. Acarol. 3: Kapil, R.P., Putatunda. B.N. and Aggarwal, K. (1985). In: Fifth Ann. Rep., Dept. of Zoo!., HAU, Hisar, pp Koeniger, N (1985). Bee WId. 66: Koeniger, N. (1990). In: Social Insects and the Environment. (Veetesh et a/. Eds.) Oxford & IBH Pub!. Co. Pvt. Ltd. New Delhi pp Koeniger, N. and Koeniger, G. (1985). In: Proc. 3rd Int. Con! Apic. Trop.Climate. Nairobi, Laigo, EM. and Morse, RA (1968). Bee WId. 49: Mossadegh, M.S. (1990). Expt/. Appl. Acaro/. 9: Nyein, M.M. and Zmarlicki, C. (1982). Am. BeeJ. 122:

10 214 AGRICULTURAL REVIEWS Putatunda, B.N. (1996). Bee mites in India. National Beekeeping Experience Exchange Conference Ludhiana (India) pp Putatunda, B.N. and Kapil, RP. (1988) Seven New species of Cheletophyes (Acari: Prostigmata: Cheyletiae) associated with carpenterfees in India. In: Progressin Acarology-I (Channabasavanna, G.P. and Viraktamath, CA Ed.) Oxford and IBH, N. Delhi pp Putatunda, B.N. and Kapil, RP. (1995). J. Acarol13 (1&2): 15-2I. Putatunda, B.N. Aggarwal, K. and Kapil, RP. (1983). Indian J. Acarol. 8: Sadov, A.V. (1976). Pehelovodstvo, 8: Shah, FA and Shah, T.A. (1988). Am. Bee. J. 128: Sihag, RC. (1988). Am. Bee J. 128: Stephen, W.A. (1968). Bee WId. 49: Sudarsanam, D. and Murthy, V.A. (1990). In: Social insects andthe Environment(Veeresh etal. Eds.) Oxford and IBH Pub!. Co. Pvt. Ltd. New Delhi. pp Suryanarayana, M.e. (1988). Indian Bee J. 50: 122. Surayanarayana, M.e. and MUjumdar, S.M. (1988). Indian Bee J. 50: 100-lOI. Tewarson, N.e. (1985). Ph. D. Dissertation (Unpublished), pp Weinberg, K.P. and Madel, G. (1985). Apidologie. 16: Woyke, J. (1984). Apidologie. 15: Woyke, J. (1985). J. Apic. Res. 24: Woyke, J. (1987). J. Apic. Res. 26:

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