MITE PESTS OF HONEY BEES

Transcription

1 Ann. Rev. Entomol E Copyright O 1982 by Annual Reviews Inc. AC rights reserved MITE PESTS OF HONEY BEES David De Jong, Roger A. Morse, and George C. Eickwort Department of Entomology, Cornell University, Ithaca, New York INTRODUCTION Mites that affect honey bees or are found in bee hives may be divided into three groups: parasites, phoretic mites, and house guests. The number of species of parasitic mites are few, but some are the causes of serious diseases of bees. The primary problem mites are Varroa jacobsoni, Acarapis woodi, and Tropilaelaps clareae. Phoretic mites are flower or leaf-feeding mites that use honey bees for transport from one plant to another and arrive accidentally in a beehive. Among the many house guests are species that feed on old provisions and a few species that feed on other mites. Mites rarely feed on stored pollen in active hives, although large numbers of pollen-feeding mites are often found in stored combs. There are four species of honey bees on earth. Apis mellifera is native to Europe and Africa; A. cerana, A. dorsata, and A. florea are native to Asia. Apis mellifera has been transported to all areas where men reside. They have been successfully established everywhere except in tropical Asia where mites that prey on some of the three Asian species are apparently responsible for their demise. In the past few decades one species of mite native to Europe and one native to Asia have been spread by men to other continents and pose a threat to the beekeeping industry. The only major honey-producing areas uninfested by one or both at present are the United States, Canada, Australia, and New Zealand. Beekeepers in these four countries are alert to the dangers these mites pose; however, given the rate at which people move around earth and the laxity of customs officials in most countries, these mites will eventually be as ubiquitous as their hosts. VARROA JACOBSON1 Varroa Jacobsoni, once a relatively obscure mite of Asian bees, has emerged as the foremost problem for the world beekeeping community. In 1971

2 230 DE JONG, MORSE & EICKWORT varroa damage to colonies of Apis mellflera was recognized outside of Asia, and by 1975 had spread to eastern and western Europe, northern Africa, and much of South America (33,38,44). The thoroughness with which this mite covers an area is shown by a Brazilian survey in which 520 colonies selected from 26 apiaries representing most of Sao Paulo State were all found to be infested (56), although a little over a year before the survey, the mite had not yet been reported from that country. As was the case in nearly every country, the mite was not discovered until long after the possibility of eradication through bee colony destruction had passed. K jacobsoni is a large (length of idiosoma approximately pm, width 1600 pm), dorsoventrally flattened, pilose, reddish-brown mite (2, 48). It is an ectoparasite of A. cerana and A. mellvera adults and brood in the late larval and older stages (2, 109). Varroa feeds by sucking hemolymph from its host (146). Signs of infestation include reduced weight of emerging bees (7; De Jong, submitted for publication) and damage in the form of small or missing wings and other appendages and a shrunken abdomen when the number of mites per brood cell is high (7, 31, 53, 143). The mites prefer drone brood (59, 140), and drone cells have a greater number of mites and are infested at a greater frequency (up to 15 times) than worker brood in the same colony (6, 64, 85). This preference for drone brood has been a severe problem where A. mellijera colonies exist in low densities, because of the mite-induced depression of drone populations available for mating. When a colony swarms or otherwise attempts to replace its queen, the virgin queen remains uninseminated and the colony subsequently dies (107, 108). K jacobsoni and another Asian mite species, Tropilaelaps clareae, are considered the primary cause for the repeated failure of A. mellvera-based beekeeping in Asia (45, 108). Distribution Before man began moving bees internationally, there was no area of contact between A. cerana, the original host, and A. mellifra. V. jacobsoni was described in 1904 from A. cerana in Sumatra (120) and redescribed as Myrmozercon reidi from the same species on Singapore Island in 1951 (61). It was not until the early 1960s, when it was discovered in the Philippines, that K jacobsoni was recognized as a parasite of A. mellifra (46, 151). A. mellfera had been imported into the Philippines; it became contaminated through close contact with A. cerana, perhaps through mutual robbing (59, 111, 113) or the efforts of beekeepers to strengthen their A. mellvera colonies by giving them sealed A. cerana brood, which has been done in other areas of Asia (152). ~ lintroduced l A. mellfira colonies, though they were good producers initially, succumbed to the Asian mites (108). Beekeepers from European Russia moved to the Primorie region of far-

3 HONEY BEE MITES 23 1 eastern USSR in the early part of the century, where they encountered and worked with the Asian hive bee A. cerana. Later, beekeepers from the Ukraine brought in colonies of A. mellifera. It is not clear when varroa first moved to A. mellifera in the USSR, but the mites were observed on A. cerana in far-eastem USSR in 1952 (85). Also, two female K jacobsoni in the State University of Moscow. collection were collected in 1949 from colonies of A. cerana in Moscow that had been moved from the Primorie region (88). More recently, reports of high honey yields in this far eastern area prompted rumors that the bees there were especially productive. As a result, many A. mellifera queens were imported into western USSR and they apparently carried varroa (37). In 1965 widespread varroa infestation of A. mellifera colonies in western USSR was reported, with as many as 5,000 mites per colony and up to 70% of the brood infested (85). By 1967, varroa was reported frbm Bulgaria, apparently imported with queens from the Balkans (81, 148). The next European country to report the presence of varroa was Rumania in 1975 (38, 119), though varroa had undoubtedly entered Rumania and Bulgaria at least three to five years before discovery (33, 117). Apparently their governments were not aware of the seriousness or the extent of the infestations, and, as part of a foreign aid program, Rumania sent hundreds of colonies of honey bees to Tunisia in Varroa was first noticed in Tunisia in 1978 (66). A similar shipment from Bulgaria to Libya in 1976 (38) also resulted in the establishment of varroa. Presently all of eastern Europe is infested (37, 62, 81, 91), apparently through international movement of queens and colonies. A separate focus was initiated in 1971 near Frankfurt, West Germany, from colonies of A. cerana imported for research (33, 136, 141). The infestation there was not recognized until There is some possibility that the mites arrived in 1975 or 1976 with queens imported by private beekeepers from Rumania, the USSR, and northern Greece (141). Japanese beekeepers moved A. mellifera bees into Paraguay in 1971, marking the entry of varroa into South America (44,56, 112). In 1972 some infested bees from a Japanese bee company in Paraguay were moved to Sao Paulo State in Brazil (1 l2), and varroa was found in Argentina and Uruguay in 1975 and 1976 respectively (59). All of the infestations in South America apparently originated in Paraguay. The remarkable rate at which varroa has spread throughout most of the world is due both to the particular biology of the mite and to the nature of modem beekeeping (see Table 1). Generally the infestations have been detected relatively late after introduction of the mites. The mites are in an area for 2-6 years before the colonies show obvious signs (21, 44, 54, 75, 117). In the early stages of an infestation, while the population of mites is

4 232 DE IONG, MORSE & EICKWORT still low, there is very little damage to the bee colonies (1 17). This leads some apicultural officials to indicate that varroa is not detrimental (172), though they generally revise their opinion as infestations increase. Most of the life cycle takes place within bee brood cells, where the beekeepers seldom look, and the mites are difficult to see on the adult bees. Many "hide" under the abdominal sclerites (21, 158). Even when the mites are seen they are often confused with the relatively harmless bee lice, Braula spp. (18, 42, 112, 117, 167). Most of the large jumps in distribution have been due to migratory beekeeping and shipment of bees and queens (1 17). Once varroa becomes Table 1 Known infcstations of Varroa jacobsoni Year Con tinen t discovered Country Reference Asia 1904 Java (Indonesia) Sumatra (Indonesia) Singapore USSR Japan People's Republic of China India Philippines Hong Kong Malaya Vietnam Korea Cambodia Thailand 87 ', 1974 Taiwan Iran 37 Europe 1978 Pakistan USSR Bulgaria West Germany Rumania Poland Yugoslavia Turkey Greece Czechoslovakia Hungary 24 Africa 1975 Tunisia Libya 38 South America 1971 Paraguay Brazil Argentina Uruguay 56

5 HONEY BEE MITES 233 established in an area it becomes widely distributed very rapidly (39,44,59). In eastern Europe and West Germany the rate of natural movement of the mites has been estimated at about 3 km per year (33, 39, 117, 141), though in the USSR the mites moved km in 3 months (59). Migration of the mites is attributed to the movement of swarms (122, 126); robbing bees also can transport mites (101). A few researchers have observed the mites transferring onto bees at flowers (59, 81), though others indicate that they find no mites on flowers near heavily infested apiaries (69). As I/: jacobsoni is an obligate parasite and cannot live much more than a day without bees (152, 158), it is unlikely that they would leave the host bee outside of the hive. Drifting bees (which accidentally go into the wrong hive), especially drones, may be an important means of inter-colony transmission (2, 158). Mites have been found on drones collected at congregation areas (69), and it is possible that when drones are closely following a queen, mites can move from one drone to another, or to the queen, though a preliminary investigation of the latter possibility showed that no young queen returning after a mating flight was infested (69). Life Cycle Adult female varroa live on adult worker and drone honey bees. They are most commonly found on the abdomen, often under the abdominal sclerites or between the thorax and abdomen. Occasionally they are seen on or under the thorax. They hold on to the bee tightly with their legs, though they are capable of moving rapidly over the surface of the bee. They feed by making a hole in the intersegmental membranes and sucking hemolymph. The chelicerae are modified for this purpose. There is no fixed digit, and the movable digit is sharply pointed and has short spines on the cutting edge (2). The mites begin their reproductive cycle by entering the cell of a 5- to 5-'/2-day-old bee larva (59) shortly before it is sealed. They may feed on the larva initially, but they quickly crawl underneath the larva and immerse themselves in the brood food, at least some of which they ingest. They remain in the brood food, oriented ventral side towards the opening of the cell, until the larva eats the food and thereby cleans off and frees the mites. As many as 21 adult female mites may be seen, apparently immobilized, immersed in the brood food in one cell. Unless the larva cleans off the mites, most of them die (De Jong, unpublished data). After the mites are freed, they begin feeding on the hemolymph of the larva and later the pupal bee (2). The mites swell noticeably so that there are spaces between the ventral plates (127). Eggs are laid one at a time on the cell walls (158). The larval stage of the mite develops within the first 24 hr, but remains inside the egg (2, 88), molting to a protonymph that hatches about 48 hr after the egg is laid. The protonymph feeds on hemqlymph of the bee pupa

6 234 DE JONG, MORSE & EICKWORT for several days and molts to a deutonymph. The deutonymph continues to feed on hemolymph for several more days before molting to the adult stage (88, 145, 158). Males are small (7 15 pm long, 700 pm wide) and pale colored. Their chelicerae are highly modified for sperm transfer and they do not feed (2, 48). Mating takes place within the cell. Development time from egg to adult is 6-7 days for males, 8-9 days for females (59). Males and the many mites that do not reach maturity remain in the cell and die, while the mature females leave the cell with the emerging bee (89). The rate of reproduction has not been well established. The average number of eggs laid per mite is variously given as 2-3 (158), 2-5 (148), 3-4 (63), and 7-8 with a range of 1 to 38 (59). Some mites live in the sealed brood cells without laying any eggs (158). There have been several attempts to rear the mites under controlled conditions. Mites taken from recently sealed cells and placed into cells just before sealing were most productive (70, 145). Mites raised on worker larvae in queen cell cups kept in an incubator laid an average of 1.5 to 2 eggs, though few protonymphs and deutonymphs and no new adults were s"uccessful1y reared (145). Brood cells artificially infested with marked mites and then sealed manually produced some new female adults, but the success rate was low (24-30% of the number of introduced females) (70). Male and female protonymphs are white and similar in appearance. The anal plate of the male is less well defined than that of the female, and the male pilose system is developed only in the preanal region whereas that of the female is more uniformly distributed (59, 88). Female deutonymphs are white, large, and wider than long as in the adult, whereas the male deutonymph is about the same size as the protonymph (88). The adult male has a spherical yellowish body, only slightly sclerotized (88), and short, unlooped peritremes that adhere to the idiosoma (2, 88). The adult female is reddish-brown and pilose, with many long setae on the dorsum (48, 59). Peritremes are large, with most of the length free of the idiosoma. The specialized peritremes apparently enable the mites to adjust to the large difference in C02 atmosphere between the interior of the brood cells and that encountered while attached to free-flying bees (40, 41, 152). Internal anatomy and histology are described by Sadov (144) and Ionescu-Varo & Suciu (72). In the winter the malpighian tubules contain large amounts of guanine (72). In an immunological study of hemolymph proteihs in K jacobsoni (166), honey bee proteins were found relatively unchanged in female mites and eggs, indicating that the mites absorb many honey bee proteins with little digestive degradation. The adult female mites normally live about 24 hr without food (158), though they may survive up to five days under favorable conditions (59, 152). Their life is extended several days when they have access to dead bees

7 HONEY BEE MITES 235 (158) and up to 30 days in sealed brood held at room temperature (152). The length of life in bee colonies is not well established, though females do stay on adult bees through the long, winter, broodless period in the northern temperate zone. The life span on adult bees in summer is two months and at least five months in winter (88, 152). The number of mites in an infested colony can be quite high, from 3,000-5,000 (75, 85) to 11,000 or more (158). An infested adult worker may carry up to 5 mites and a drone up to about 12 (59, 64, 123, 148). Up to 12 mites may be found in worker brood cells and 20 in drone cells (59, 64, 112, 148). Diagnostic Procedztres A number of diagnostic measures are available to determine the presence and extent of varroa infestations. The most reliable detection method is to open drone brood cells and remove the pupae with forceps (42,43,96, 134). In colonies lacking drone brood, worker cells can be opened instead, but worker brood has relatively few mites when drone larvae are available in the same colony (56, 58). A sheet of strong white paper or plastic with a screen (holes greater than 2 mm) held 6 mm above, mounted on a wooden frame, can be placed under the brood combs to continuously monitor colonies in the areas of suspected infestations (43, 95). Dead mites fall onto the paper, where the screen prevents the bees from removing the bodies. This method is most useful in fall and winter when most adult mite mortality occurs (134). It has been used extensively in combination with several acaricides, both to increase the probability of detection in lightly infested colonies (134, 168) and to allow an evaluation of chemical controls by counting fallen dead mites (26, 134, 1 47). Adult bees can be sampled directly by brushing them from the brood combs into jars filled with some liquid, shaking for one to thirty minutes, straining the bees out and passing the filtrate through a white cloth where the mites can be seen. A per-bee infestation rate can be estimated by counting the mites and bees. The solutions used for "shaking" have included various detergent solutions (42, 162), hexane or gasoline (l34), diesel fuel (39), and 96% ethanol (44, 55, 56). Gasoline or hexane will remove 100% of the mites when the bees are shaken for 30 min in a laboratory shaker, but these liquids are dangerous and have an objectionable odor. Alcohol is equally effective, safer, and less unpleasant (56). Damage Due to Varroa There have been many reports of lost honey production and weakened or killed colonies as a result of varroa infestations. A small but developing

8 236 DE JONG, MORSE & EICKWORT beekeeping industry of about one thousand colonies of A. mellifera in the Philippines was eliminated by varroa in a period of about 12 to 15 years (112), though it has since been reestablished with bees from the United States. Shung (154) reported that many bee colonies have been killed by the mite in the People's Republic of China. In 1971 an estimated 55,000 colonies were lost to the mite in the USSR (101). In Japan and China there has been a total loss of colonies in many apiaries (32, 132). Untreated colonies die within 3-4 years of discovery of the mites (132), and the highest death rate of colonies occurs during the winter (59). In 3-5 years 20-30% of the bees may be infested, yet productivity stays high a long time (59). In the USSR, comparison of heavily (14%) and lightly (2%) infested colonies showed no difference in honey production (148). However, in Bulgaria, there was up to 100% mortality in apiaries 3-4 years after the discovery of varroa mites (152). In heavy infestations one finds damaged bees and pupae on the bottom board (95). Immature bees with up to about 6 mites develop normally; when more than 6 mites per cell are present many bees will be deformed or killed (1 12, 152). As a result, during the first few years of an infestation, when the average number of mites per brood cell is low, a very small percentage of bees will show obvious signs such as damaged wings (and many of these are quickly discarded by house-cleaning bees), even though 50% or more of the brood cells are infested (De Jong et al, submitted for publication). Distribution Within Apiaries Although varroa is normally thoroughly distributed throughout all the colonies in an apiary, not all colonies are equally infested (56); weak or queenless colonies are more severely affected (19, 59, 114, 121, 158). This is also true of Tropilaelaps clareae on Apis dorsata (86) and Euvarroa sinhai on ApisJIorea (2). The increase in the mite population within the colonies was less than 100% in one season in Tunisia for colonies with normal queens, while it increased more rapidly in those colonies that lost their queens or otherwise had their development disturbed (19). Some authors have attributed the higher rate of increase in weak colonies to lower brood nest temperatures that favor mite development (59, 158). Recently it has been demonstrated that loss of the qbeen and subsequent queen-cell production increases significantly the number of mites beginning reproduction (De Jong, manuscript in preparation). Control CHEMICAL Chemical control of K jacobsoni is difficult. The mites are always found associated with their hosts, so only mite-specific chemicals

9 HONEY BEE MITES 237 that do little or no harm to the bees can be used. Except during occasional broodless periods in winter in temperate areas, a large percentage of the mites are sealed inside bee brood cells where it is impossible to reach them with most pesticides. At present there is no accepted, satisfactory chemical means of eliminating varroa from a colony, though there are many chemicals that will reduce the number of mites. Nearly every country affected has initiated some efficacy studies with various acaricide sprays and fumigants. Since 1974, research on chemical controls has been done at 22 institutes in the USSR with over 100 chemicals tested (158). Although the number of reportedly effective chemicals is large (1, 5, 6, 21, 31, 35, 49, 59, 60, 71, 78, 84, 90, 93, 94, 106, 116, 128, 133, 149, 155, 159, 165, 175), there is a lack of uniform testing procedures, and chemicals reported to kill nearly all the mites in one country are found unsatisfactory by apicultural workers in other countries. Phenothiazine and chlorobenzilate have been used extensively (10, 14, 35, 78, 85, 87, 113, 115, 116, 123, 137, 146, 147, , 169), but Japanese beekeepers have reported phenothiazine resistance (132, 159), and the chemical sometimes kills queens (133). Chlorobenzilate, while it kills some mites, is not an effective control (87, 128, 133). A Japanese product, VarostanQD (Bayer), is reported as very effective at killing the mites (33, 35, 133, 136); unfortunately it also causes considerable bee mortality (129, 136), and some workers have found it ineffective in controlling mite populations (6). In Greece, malathion is used as a dust with powdered gypsum as a carrier. Ifantidis (71), however, found the 1% level in gypsum too toxic to bees; he reduced it to 0.05% and substituted powdered sugar for gypsum, as the latter killed unsealed brood. Another widely acclaimed chemical control is SineacaF(35, 56, 62, 93), a Rumanian product produced by the Apicultural Research Institute of Bucharest. Sineacar consists of 1.5% chlor- and brompropylate (Ciba- Geigy) and 0.3% TedionQD (Sandoz) with cellulose or powdered sugar as a carrier (133, 163). However, several researchers have indicated that Sineacar gives poor control (62, 80), and in Brazil there was no difference in mite survival between Sineacar-treated colonies and controls (163). Kitaoka & Higasi (78) and Ritter & Ruttner (133) give data on mite and bee mortality for a large number of chemicals. The experience with chemical controls in West Germany is particularly instructive, as the infestation there is isolated and well defined. In 1977 all colonies in the suspect area were treated with Varostan as a control and as a diagnostic tool. In that year 350 colonies were found infested. In 1978, KelthaneQD (Dicofol) was used and 927 colonies were reported to have varroa. In 1979 formic acid was used as a fumigant, and 1638 colonies had the mites (141). Each chemical at the time' was supposed to be the most

10 238 DE JONG, MORSE & EICKWORT thorough control available, yet the number of infested colonies increased each year. Kelthane has been widely used (35,78,94, 124, 131, 134, 158), and it does kill many mites, but it is a very persistent chemical and could easily contaminate honey and wax (110). Formic acid is somewhat dangerous to use as it is very caustic and can cause severe burns to skin and eyes (135). It is difficult to regulate the dose, since it is applied as a fumigant from a wick -.O in a bottle placed in the hive (174), and there is some danger of bee mortality or absconding (1 10) if the bottle is tipped over and the acid evaporates too quickly. Formic acid also absorbs strongly into honey, so any honey in the -.t hive cannot be used for human consumption (79, 135). Late in the winter of and in the fall of 1980 the Germans field tested K-79 (Galekron@ = chlordimeform hydrochloride) on several thousand colonies (138). K-79, fed to the bees in a sugar solution, has a systemic action, and the mites take up the chemical when they suck the hemolymph of the bees (142). The dose must be regulated according to the number of bees; 25 pg per bee is the LDSO for bees, and 4 pg per bee is an effective mite-killing dose (125). K-79 fed in syrup is evenly distributed throughout a colony through the medium of food exchange inherent in honey bee society (106, 142). The susceptibility of mites was recently found to be age specific (105); old mites have an LDSO of 1.25 pghee while young mites have an LDSO of 5 pghee. The availability of this and other acaricides for use in honey bee colonies depends on whether any residues are found in honey harvested from the hives (15, 138). HEAT TREATMENTS The Japanese and the Russians have determined that hot air blown into the hive will dislodge many mites from the bees (77). There is a Japanese patent for a hot-air device to treat adult bees (59), in which the bees are rolled in a large metal drum with hot air (41 C) circulating for 5 minutes. In the USSR the bees are placed in an insulated chamber kept at 4648OC for 10 min (130), during which time 90 to 95% of the mites drop off. Some of the Russian bee journals contain plans for construction and use of thermal chambers (77, 83). BROOD REMOVAL In several countries the preference of mites for drone brood has been used to "trap" them (59, 140). Combs containing drone sized cells are introduced, and later destroyed, after the drone cells are sealed. A more intensive control of brood was attempted in Germany (139). All brood from four caged colonies was removed. Emerging bees were examined individually and only uninfested bees returned to the colony. At the end of the experiment one colony was left without mites and the others had very few. In other colonies, the last brood reared in the summer was

11 HONEY BEE MITES 239 removed (139), which reduced the level of infestation. Gnadinger (54) suggested that an effective means of controlling the mites would be to remove and treat the adult bees and destroy all brood in infested colonies. VARROA IN NORTH AMERICA The announcement in 1979 of?? jacobsoni from Maryland (US) (160, 170) caused a great deal of consternation throughout the world. The US had been considered one of the last "safe" places to buy queens and bees (20). Between collection and identification, over 400 colonies of bees had been moved from Maryland to Florida, where about 200,000 colonies are moved every winter from at least 12 states and Canada. If varroa was in the colonies moved to Florida, it could be spread throughout the ITS in one season. The Canadian Honey Council strongly considered a ban of all imports of bees from the US. Annual sales of package bees and queens to Canada are normally $900,000 from the southern Gulf States and $6,000,000 from the entire US, and an additional $3,000,000 of live bee exports goes to the rest of the world. Fortunately, after an intensive survey that included killing and examining all of the bee colonies within 5 km of the discovery, no further mites were found and Maryland was declared free-of K jacobsoni (25). The vial in which the original "infested" bee had been collected had previously been used in the USDAacarology laboratory, so it is possible that the vial had been previously contaminated with mites sent in for identification from outside the US (De Jong et a1 in manuscript). Despite the US Federal Bee Disease Act (99), which prohibits importation of bees into the US from any country except Canada, a few beekeepers continue to smuggle queens from other countries into North America. As K jacobsoni continues to spread throughout South America and western Europe, it is perhaps inevitable that it will eventually become established in North America (44). TROPILAELAPS CLAREAE Tropilaelaps clareae was described by Delfinado & Baker (47) from Apis mellifra in the Philippines. It is a large (length of idiosoma 960 pm, width 550 pm), fast-moving, light reddish brown ectoparasite of honey bee brood and adults. Its life cycle is similar to that of Varroa jacobsoni. The larval stage is confined to the egg; protonymphs and deutonymphs of both sexes are free-moving and feed on hemolymph of bee brood. All stages of the male and the nymphal stages of the female are found only associated with honey bee pupae and prepupae; adult females are phoretic on and feed on the hemolymph of adult bees (P. Akratanakul, personal communication). The original host is Apis dorsata, on which it has been found in the Philippines

12 240 DE JONG, MORSE & EICKWORT (86) and India (17). Delfinado & Baker (48) reported finding 5? clareae on field rats nesting in the vicinity of infested apiaries, but Sevilla (151) could find no evidence of such a relationship. Signs of an infestation by 7: clareae are an irregular brood pattern; dead and malformed larvae, pupae, and adult bees in the brood combs; damaged or missing wings and shrunken abdomens on developing bees; and wingless bees crawling in front of the hive (10). The adult mites are very fast moving and, in heavy infestations, many are observed running in and out of cells in brood combs (10, 81, 86, 161). T clareae can reach high populations on its native host A. dorsata. Laigo & Morse (86) found T clareae in seven of eight A. dorsata colonies examined. Some infested nests contain so much dead brood that there is detectable putrid odor. Queenless (laying worker) colonies have larger infestations than queenright ones. The other Asian bee species, A. cerana and A. jorea, are not attacked (9; Akratanakul, personal communication). T. clareae has been found in A. mellijera colonies in the Philippines (46, 48, 87, 98, 113, 151), Java, Malaya, Hong Kong (46), Vietnam (161), India (8-1 1, 161), and Thailand (82). The mites were probably transmitted to A. mellifra by interspecific robbing between A. dorsata and A. mellijera (86, 114). There have been reports from India and Thailand that infestations of T. clareae increase to a prejudicial level faster than do V; jacobsoni (10, 52; P. Akratanakul, personal communication). Chlorobenzilate (Folbexm) kills many of the mites when applied to infested colonies; nevertheless, it has not proved to be an effective control (10, 86). Atwal & Goyal (10) indicated that they successfully eliminated T clareae by dusting the brood nest with fine powdered suphur. BUVARROA SINHAI Euvarroa sinhai is a large (length of idiosoma 1040 pm, width 1000 pm), brown, broadly pear-shaped, setaceous mite (48). Delfinado & Baker (48) based their taxonomic description on preserved females collected from nests of A. JIorea in India. They note the lack of a fixed cheliceral digit as in V; jacobsoni. Akratanakul (2) made a further study of the biology and morphology of all life stages, based on live material he examined in Thailand. He found the life cycle similar to that of V; jacobsoni except that the mites attack only drone brood. He attributed this to the fact that the drones have a longer development time and that the disparity in size between the drones and workers is much greater than is true for the other species of Apis. The adult male mite has chelicerae modified for sperm transfer, and it is not able to feed. The adult female and the protonymphal and deutonymphal stages

13 HONEY BEE MITES 241 of both sexes feed on drone brood. Only adult females leave the cells; they are phoretic on adult drones, but it is not known whether they are able to take hemolymph from the adult bee (4). ACARAPIS WOODI AND ACARINE DISEASE There are three species of Acarapis mites: Acarapis woodi, originally described as Tarsonemus woodi (67), A. externus, and A. dorsalis. A. woodi is found in the prothoracic spiracles and occasionally in the abdominal and thoracic air sacs of bees. Until recently this was considered the major mite pest of honey bees. The remaining two species of Acarapis live externally on honey bees and are not considered serious pests. These three closely related mites are morphologically distinct species. Each attaches to a specific, restricted part of the bee. The "neck mite," A. externus, is found only in the area where the head and thorax join. A. dorsalis lives on the thorax in a groove between the mesoscutum and mesoscutellum. It may also be found at the base of the wings, on the forewings, and on the propodeum and the forepart of the abdomen. Acarapis vagans has been called a distinct fourth species, but most modern authors (e.g. 12) consider vagans to be a synonym of externus. We do not have detailed life histories of the two external species. For each species, eggs and larvae have been observed on the same body locations where the adults reside (103, 104). When congo red, a dye, is injected into the hemolyrnph of bees infested with any of the three species of Acarapis, the gastrointestinal tracts of the mites turn red (1 18). No one has suggested that the mites feed on anything other than hemolymph. It is agreed that the two species of external mites do little serious damage, although A. externus has been reported to cause wing loss or malfunction. Distribution The two externally feeding mite species are apparently found everywhere honey bees are found (50, 102, 153), even in so geographically isolated a spot as the Kingdom of Tonga (34). In their long association with honey bees, they have apparently been moved everywhere men have taken their bees. The distribution of A. woodi, however, is limited. It was discovered in England in 1921, though it probably had been present earlier,. and soon thereafter it was found in Switzerland, Czechoslovakia, and France. It was not until many years later that it was found in southern Europe and it still has not been found in the Scandinavian countries. It has been spread by man to India (1957), the Belgian Congo (1959), Argentina (1968), and in 1980 was found in Colombia and six states inmexico (16, 76, 97, 100, 156;

14 242 DE JONG, MORSE & EICKWORT personal communication, A. Zozaya, Mexico Department of Agriculture, and H. Shimanuki, USDA Bioenvironmental Bee Laboratory). Several people have been struck by the fact that the external mites are everywhere bees are kept, whereas the internal feeding A. woodi is limited in distribution. Jeffree (73, 74) has written most extensively about this. He thought that temperature limited the distribution of A. woodi and that it could survive in few places outside the British Isles. The fact that it has now widened its distribution suggests this is not true. It seems likely that A. woodi evolved more recently (perhaps as recently as 1900), probably in England, from one of the closely related external species, and has since spread. If this is the case, then A. woodi could have been the cause of the reported loss of great numbers of honey bee colonies between 1900 and 1920, a widely debated topic (13, 22). While it is obvious that an A. woodi infestation may remain hidden for many years, the mites have been sought by so many investigators that we feel they are not present in certain major honey-producing areas, including the US, Canada, Australia, and New Zealand. These four countries have had protective legislation since about 1923 to deter the mite's introduction. Bailey (12, 13) has questioned whether the mite is as serious a honey bee pest as it was originally reported to be, suggesting that acarine disease flourishes only in colonies under stress. Life Cycle The life cycle of A. woodi is described in detail by Bailey (12,22) and is only summarized here. Mated female mites leave the tracheae in which they developed and migrate to the tip of a bee's body hair, from which they grasp a hair of a passing bee. Most bees probably become infested when only a day or two old; after a bee is nine days old, the spiracular openings remain closed, preventing the entry of the mites. The female mite moves immediately to the spiracles and into the tracheae, in which five to seven eggs are laid after three or four days. The males are mature after 11 to 12 days and the females on the fourteenth or fifteenth day. Diagnosis The only method of detecting A. woodi is to remove a bee's prothoracic collar to expose the two largest tracheae in the body. The infestation may be bilateral or unilateral. Early infestations probably go undetected, but as the population in a trachea builds it darkens because of the accumulation of feces, so the mite population is detectable without the aid of a microscope. Although mites may sometimes be found in air sacs in the thorax and abdomen, diagnosis can usually be made by checking only the prothoracic tracheae. All stages-eggs, larvae, and adults-may be found in a trachea at one time.

15 HONEY BEE MITES 243 Control Much has been written about control of acarine disease; however, there is divergence of opinion over the need and efficacy of control methods, leading us to be suspicious of many of the recommendations. It has been claimed that certain bees show resistance, but there are no supporting data. It does appear that populous colonies are less likely to have heavy infestations. Fumigation of colonies with materials that would kill (or weaken) mites without having an adverse effect on the bees has been popular. Among these, chlorobenzilate has been most popular, but its use is not universal. OTHER MITES Table 2 lists the mites that have been encountered on honey bees and in hives, largely from intensive surveys in Europe (27-30,57,65,68). A careful survey of beehives in any part of the world would undoubtedly add many species to this list. Most of the species in Table 2 have been rarely collected and are of no ecological or practical concern, as their usual hosts or habitats do not involve Apis. Included in this category are plant-inhabiting mites (Tetranychidae, Eriophyidae, Tydeidae, Anystidae) that are very rarely phoretic on honey bees. Others are primarily associates of vertebrates or of other insects, including other Hymenoptera (most Laelapidae, Macrochelidae, Parasitidae, Pyemotidae, Pygmephoridae, Scutacaridae, Trombidiidae, Aeroglyphidae, Chaetodactylidae, Histiostomatidae, Pyroglyphidae, and Winterschmidtiidae). Neocypholaelaps (Ameroseiidae) is an Old World genus of fl~wer~inhabiting mites that often occur on honey bees. The mites are pollen feeders (100a) and apparently have little or no adverse effect on the bees, which are used by the mites to move from flower to flower (13a, 65). Up to 3000 Neocypholaelaps favus have been found in one hive without noticeable damage to the colony or to stored provisions [Ishikawa, cited in (65)l. A related genus, Edbarellus, was described in 1974 from three hives in the Kingdom of Tonga (92). The mite apparently is not a frequent associate of honey bees; M. V. Smith (University, of Guelph, personal communication) inspected the 1200 colonies and nuclei on the main island of Tongatapu in 1980 and found no signs of a strange or unknown bce disease. The mite's mouthparts resemble those of Neocypholaelaps, and its association with Apis is probably much like that of Neocypholaelaps. E. W. Baker (USDA, Beltsville, personal communication) states the mites' mouthparts indicate they may be pollen feeders. Nevertheless, New Zealand officially refuses to admit queen honey bees from Tonga pending determination of whether or not the mite poses a threat, thus affecting Tonga's fledgling beekeeping industry that had hoped to develop a queen-rearing business.

16 244 DE JONG, MORSE & EICKWORT Table 2 Acari associated with honey bees (Apis spp.) Family Mesostigmata Ameroseiidae Ascidae Eviphididae Laelapidae Macrochelidae Parasitidae Varroidae Veigaiidae Prostigmata Anystidae Cheyletidae Eriophyidae Pyernotidae Pygmephoridae Scu tacaridae Name Edbarellus ronganus Mason Neocypholaelaps africana Evans Neocypholaelaps arnpullula (Berlese) Neocypholaelaps favus Ishikawa Neocyphloaelaps indica Evans Neocy piiolaelaps novaehollandiae Evans Blattisocius den triticus (Berleses) Blattisocius rnuli (Oodemans) Blattisocius tarsalis (Berlese) Lasioseius muricatus (Berlese) Lasioseius penicillinger (Berlese) Lasioseius sp. Melichares agilis Hering Proctolaelaps pygrnaeus (Miiller) Alliphis halleri (Canestrini) "Iphis" sp. Androlaelaps casalis (Berlese) Androlaelaps fahrenholzi (Berlese) Haernogamasus nidi Michael Holostaspis bornbicolens (Canestrini) Holostaspis rnarginepilosa (Sellnick) Laelaps algericus Hirst Mellitiphis alvearius (Berlese) Tropilaelaps clareae Delfinado & Baker Macrocheles glaber (Miiller) Macrocheles rnuscaedornesticae (Scopoli) Parasitus coleoptratorurn (Linnaeus)' "Parasitus" fucorurn (DeGeer) Parasitus sp. Pergamasus crassipes (Linnaeus) Pergarnasus diversus Halbert Euvarroa sinhai Delfinado & Baker Varroa jacobsoni Oudemans Veigaia nernorensis (Koch) Anystis sp. Acaropsis sollers Rohdendorf. Cheyletus aversor Rohdendorf Cl~eyletus eruditus (Schrank) Eucheyletia jlabellifera (Michael) Eriophyes tilia Nalepa Pyemotes anobii Krczal Pyemotes ventricosus (New port) Pygrneplrorus spinosus Kramer Sccttacarus acarorurn (Goeze)

17 HONEY BEE MITES 245 Table 2 (Continued) Family Prostigmata (continued) Tarsonemidae Tetranychidae Trombidiidae Tydeidae Astigmata Acaridae Aeroglyphidae Carpoglyphidae Chaetodactylidae Glycyphagidae Histiostomatidae Pyroglyphidae Winterschmidtiidae Cryptostigmata Oribatulidae Pediculochelidae Name Acarapis dorsalis Morgenthaler Acarapis externus Morgenthaler Acarapis woodi (Rennie) Tarsonemus apis Rennie Tarsonemus indoapis Lindquist Tarsonemus sp. Tetranychus urticae Koch sp. complex Allothrombium fuliginosum (Hermann) nombidium holosericum (Linnaeus) Ddeus sp. Acarus farris (Oudemans) Acarus gracilis Hughes Acarus immobilis Griffiths Acarrrs siro Linnaeus Acarus sp. Cosmoglyphus sp. Forcellinia galleriella Womersley Rhizoglyphiis robini Claparede Sancassania berlesei (Michael) Sancassania rhizoglyphoides (Zachvatkin) Schwiebea tshern~)shevi Zachvatkin Thyreophagus en tomophagus (Laboulbene) 7)volichus casei Oudemans prophagus longior (Gervais) Drophagus putrescentiae (Schrank) Aeroglyphits peregrinans (Berlese) Carpoglyphys lactis (Linnaeus) Carpoglyphus mcinroi Hughes Chaetodactylus osmiae Dufour Dermacarus sp. Glycyphaglis destructor (Schrank) Glycyphagus domesticus (DeGeer) Anoetus sp. Myianoetus setipes (Koch) Dermatophagoides farinae Hughes - Dermatophagoides pteronyssinus (Trouessart) Saproglyphus sp. Scheloribates latipes (Koch) Pediciilochelus~raulti Lavoipierre

18 246 DE JONG, MORSE & EICKWORT Two species of Tarsonemus, a genus related to Acarapis, are known only from honey bees (90a). Tarsonemus apis has been collected from several species of Apis, both on the bees and in stored pollen, while 7: indoapis has only been found on the neck region of workers of A. cerana. The structure of their mouthparts suggests that the mites are not parasites and are possibly pollen-feeding commensals, of little or no adverse effect on the bees (90a). Honey bees are efficient in protecting their hive and the brood nest from vermin. They coat the combs and the top and side walls with propolis (the name given the gums and resins bees collect from tree wounds and buds) but usually make little effort to do so on the hive bottom (150). Mites, representing a variety of saprophytic and predatory species, are often found in the debris in the bottoms of hives. The "stored products" Astigmata, widespread contaminants of human foods, invade hives where they feed on stored pollen and honey, or fungal contaminants thereof. They may become serious contaminants of the provisions (13b, 29, 57, 171, 173). Acarus, Tyrolichus, Tyrophagus, Carpoglyphus, and GIycyphagus are the most common genera of these mites in beehives. Feeding on these mites are a variety of ptedatory species, especially Mesostigmata and Cheyletidae. Mellitiphis alvearius (?Laelapidae) is known only from bee hives and appears to be a specialized associate of Apis. Its significance in the hive is not known; no evidence of damage to bees or brood has been found and it may be a predator on other mites (148a). The most practical way of collecting mites in the field is with a Berlese funnel. However, when surveying for mites by checking mailed-in samples from beekeepers, a flotation method is more satisfactory. One technique (65) may be summarized as follows: Debris from three to five hives are placed in a tightly sealed polyethylene bag that is shipped by mail. The bags are stored at 4OC upon receipt. The material is sieved, and one gram of the sieved material placed in 32 ml of lactic acid for 10 min. This is centrifuged and 32 ml of saturated sodium chloride added. The supernatant is filtered and the filter paper examined for mites, which are then mounted for identification. Writing of portions of this review, and certain observations cited, were supported by NSF grant DAR , concerning biology and control of Varroa jacobsoni. The authors thank Beth French, whose assistance in editing and preparing the final manuscript was invaluable. Lois Bower assisted in the preparation of the manuscript; we appreciate her assistance and advice.

19 HONEY BEE MITES 247 Literature Cited 1. Acosta, F. N An experiment in chemical control of Varrw acobsoni. Honeybee Sci. 1:21-22 (In fapanese) 2. Akratanakul, P Biology and systematics of bee mites of the family Varroidae Acarina: Mesostigmata). MS thesis. 6 reg. - State Univ., Corvallis. 64 PP- 3. Akratanakul, P., Burgett, M Varroa iacobsoni. a ~rosnective ~est of honey Gees in many barti of the'world. Bee World 56: Akratanakul, P., Burgett, M Euvarroa sinhai Delfinado and Baker (Acarina: Mesostigmata): a parasitic mite of Apis Jnrea. J. Apic. Res. 15: All-Union Scientific-Research Institute of Veterinary Sanitation Honeybee parasite-controlling agent. Japanese Kokai Tokyo Koho 78,139,722. Chem. Abstr. 90: (Abstr.) (In Japanese) 6. Alpatov, V. V., Langhe,A. B., Tatsii, V. M., Natskii, K. V The selection and development of substances for use against varroa. In Varroa Infestation of HoneyBees, ed. V. V. Alpatov et al, Izd. Nauk. pp IBRA Transl. No. E I Gshakova, 0. V., Bobkova, V. V., Grobov, 0. F., KO jova, L. M Langhe, A. B., Mikitiuk, V. V., ~atsl;!li, K. V., Stolbov, N. M., Tatsii, V. M Contributions to biological study of Varroa jacobsoni and its influence on honey bees. Apimondia Adelaide 26: Atwal, A. S Serious infestations of Apis mellifera L. bees by the ecto arasitic mite Tro ilaelaps clareae..2&d Int. Beekeep. dngr. Summ. 22: InR 9. Gal, A. S., Dhaliwal, G. S Some behavioural characteristics of A is indica F. and Apis mellifra L. Ind" ran Bee J. 31:l Atwal, A. S., Goyal, N. P Infestation of honey bee colonies with Tropilaelaps and its control. J. Apic. Res. 10: Atwal, A. S., Sharma, 0. P Brood rearing activity of the Italian honey bee Apis mellifem L. in the Punjab lains at Ludhiana. Indian Bee J. 32:& Bailey, L Infectious Diseases of the Honey-Bee. London: Land Books. 176 pp. 13. Bailey, L The 'Isle of Wight Disease': The origin and significance of the myth, Bee World 45:32-37, 18 13a. Baker, E. W., Delfmado, M. D Notes on the bee mite Neocypholoelaps indica Evans, Am. Bee J. 116:384, b. Baker, E. W., Delfinado. M. D Notes on the driedfruit mite Car gly phus lactis (Acarina: ~arpo~l~~rpdae) Infesting honevbee combs. J. Aoic. Res. 17:52-f; Basan, I. N Equipment for treating Braula and Varroa infestations of honey bees. Veterinariya Moscow (4):81 (In Russian) 15. Becker, W Problems of the legal acceptance of drugs for control of bee diseases in FRG, In Apimondia Bee Biol. Bee Pathol. Int. Symp., Oberursel- Bad Homburg, FRG In press 16. Benoit, P. L. G The occurrence of the acarine mite, Acarapis woodi in the honeybee in the Belgian Congo. Bee World 40: Bharadwaj, R. K A new record of the mite Tropilaelaps clareae from Apis dorsata colonies. Bee World 49: ~keck, R., Lavie, P Informations pratiques sur la Varroatos ou Varroase. Rev. EZ. Apic. (348): Bretschko, J Observations on Varroa infestation throughout a vegetation period in Tunisia. See Ref. 15. In press 20. British Beekeepers Association Rebort of the delegates of the British ~eekee~ers ~ssocigion. Editorial. Br. Bee J. 107: Brizard, A Fiche Technique, La Varoose. Bull. Tech. Apic. 6(1>: Butler. C. G The incidence and distribbtion of some diseases of the adult honeybee (Apis mell$era L.) in England and Wales. Ann. Appl. Biol. 32: Buttel-Reepen, H. V Die neue(?), verheerende Milbenkrankheit der Bienen. Arch. Bienenkd. 2: Buza, L Control of varroa disease in Hungary. Apiacta Bucharest 13: ,"., 25. Caron, D. M Bee disease scare over i;~ Maryland. Glean. Bee Cult.. 108: Cheung, M. L The experiences of killing mites infecting honeybee colonies. J. Bee Cub China (]):I5 (In Chinese) 27. Chmielewski, W Charakterystyka morfologiczna i biologicznoekologiczna Carpoglyphus lactis (L.)- Gatunku wystepujacfgo na miodzie naturalnym w przechowalniach i w vlach

20 248 DE JONG, MORSE & EICKU pszczelich. Pszcze/nicze Zesz. Nauk 14(1-3): Chmielewski, W Roztoczek suszowy-szkodnik wystepujacy rowniez na miodzie. Pszczelarshvo 21 (10): Chmielewski, W Roztocze (Acarina) wystepujace w zbieranym przez pszczoly i przechowywanym pylku kwiatowym. Zen Probl. Postepow Nauk Roln. 171 : Chmielewski, W Wyniki obserwacji powiazan rostoczy z owadami (Acari-Insecta). Bull. Entomol. Pol. 47: -, $ Choi, S. Y., Woo, K. S Studies on the bionomics of the bee mite, Varroa jacobsoni Oudemans, and its chemical control (11.). Res. Rep. Ofl Rural Dev. Suwon Korea I6 (Livestock), pp (In Korean) 32. Chun, L Beekeeping in China. Glean. Bee Cult. 93: Claerr, G La Varroase, Beau imminent pour l'apiculture europbenne? Rev. Fr. Apic. (358): Clinch, P. G Examination of bees from Tonga reveals a new ascid mite. N. Z. Beekeep. 33(4): Colin, M. E La Varroase, Methodes de diagnostic-etude des acaracides specifiques. Abeille Fr. Apic. (620): Crane, E h4ites infesting honeybees in Asia. Bee World 49: Crane, E The Varroa mite. Bee World 59: Crane, E Fresh news on the Varroa mite. Bee World 60:8 39. Cromroy, H. L The Asian honeybee mite-a new threat to American beekeepers. Flu. Coop. Exf. Ser. Entomol. Leafl. No Cromroy, H. L., Kloft, W. J Probleme der Milbensauche der Honiebienen, betrachtet aus weltweiteh Sicht. ADIZ (12): Cromroy, H. L., Kloft, W. J problem-s raised by invasion of honey bees by acarine mites in the world. Apiacta Bucharest 15: De Jong, D Field identification of Varroa jacobsoni, a parasitic mite of honey bees. Glean. Bee Cult. 107:639-40, De Jong, D Varroa jacobsoni, a parasitic mite of honey bees: Survey Techniques. Univ. Md. Entomol. Leafl. No De Jong, D., Gonqalves, L. S The Varroa problem in Brazil. Am. Bee J. 121: De Jong, D., Morse, R. A Annotated bibliography on Varroa jacobsoni, Tropilaelaps clareae, Euvarroa sinhai. Int. Bee Res. Assoc. Bibliogr. No p. 46. ~eknado, M. D Mites of the honeybee in South-East Asia. J. Apic. Res. 2: Delfinado, M. D., Baker, E. W Tropilaelaps, a new genus of mite from the Philippines (Laelapidae (S. Lat.): Acarina). Fieldiana, Zool Delfinado, M. D., Baker, E. W Varroidae, a new family of mites on hone bees Mesostigmata: Acarina). J. ~ask Acad. Sci. 64: Dimitriev, N Varroasis in Plodiv region: appearance, evolution and control. In Varroasis, a Honeybee Disease, pp Bucharest: Apimondia 50. Eckert. J. E Acara~is mites of the honey bee, Apis mellif&a L. J. Insect Pathol. 3: Ehara, S On two mites of economic importance in Japan (Arachnida: Acarina). AppL Entomol : Flechtmann, C. H. W Acaros associados a abelha melifera. V. Congr. Bras. Auio. 3rd Connr. Lac-1ber.-Am. Apic. 53. Galton, D Varroatosis. Am. Bee J. 111: Gnadinger, F Preventing infroduction of the Varroa disease in uninfecfed countries. Presented at Apimondia Int. Symp. Varroa Dis., Bucharest 55. Gonqalves, L. S., Morse, R. A., Stort, A. C Incidence of the mite Varroa jacobsoni in the colonies of Africanized bees in the State of Sao Paulo. Apimondia Athens 27: Gonpalves, L. S., Morse, R. A., Stort, A. C., Buriolla, A. H., Issa, M. R. C., Steiner, J., Veloci, M. E. P. V Estudo sobre o acaro parasita de abelhas Varroa jacobsoni. I. Grau de infesapao em apiarios do estado de Sao Paulo (Nota Preliminar). V. Congr. ' Bras. Apic. 3rd Congr. Lai.-1ber.-Am. Apic. 57. Grobov, 0. F Mite fauna in Apis nest and its significance. Apimondia Grenoble 25:36& Grobov, 0. F Varroa disease in honey bees. Apiacfa Bucharest 11: Grobov, 0. F Varroasis in bees. See Ref. 49, pp Grobov, 0. F., Mikitiuk, V. V., Likhotin, A. K The use of purified sul- -

21 HONEY BEE MITES 249 fur during Varroatosis of bees. Veterinariya Moscow (1):71-73 (In Russian) 61. Gunther, C. E. M A mite from a beehive on Singapore Island (Acarina: Laelapidae). Proc. Linn. Soc. N. S K 76: Hanko, J Varroa disease in Czechoslovakia. Apiacta Bucharest 13: ~ansson, A Nya ron om binas parsiter och smittsamma sjukdomar. Bitidningen 75: Haragsim, The mite Varroa jacobsoni as a threat to beekeeping in Europe. Zmkerfreund 28: Haragsim, O., Samsinik, K., Vobrhzkova, E The mites inhabiting the bee-hives in CSR. Z. Angew. Entomol. R7: , 66. Hicheri, K Varroa jacobsoni in Africa. Apiacta Bucharest 13: Hirst, S On the mite Acarapis woodi, associated with the Isle of Wight disease. Ann. Mag. Nut. Hist. 7: Homann, H (1934). Die Milben in gesunden Bienenstocken. Z. Wbs. BioL Abt. Z. Parasitenkd. 6: Huttinger, E., Pechhacker, H., Sulimanovic, D., Tomac, I Spread of Varroa jacobsoni Oudemans. See Ref. 15. In press 70. Ifantid~s, M Attempts of controlled rearing of Varroa mites. See Ref. 15. In press 71. Ifantidls, M Malathion-a contact substance for control of Varroa disease. See Ref. 15. In press 72. Ionescu-Varo, M., Suciu, S Preliminary results of the anatomical and histological examination of the Varroa jacobsoni Oud. mite. Presented at Apimondia Int. Symp. Varroa Dis. Bucharest 73. Jeffree, E. P Acarine disease of the honeybee and temperature. Nature 175: Jeffree, E. P The world distribution of acarine disease of honeybees and its probable dependence on meteorological factors. Bee World N Kamburov, G., Kantchev, K., Yanev, D Varroa disease in bees in Bulgaria. Apimondia Grenoble 25: Katzenelson, M Debe preocu ar nos la acariosis de la abeja. Gac. &; nar. 30: Khrust, I. I Thermal treatment during Varroatosis. Pchelovodstvo (6): 5-8 (In Russian) 78. Kitaoka, S., Higasi, M Research of methods of control of the mite Varroa jacobsoni, a parasite of honey bees. Anim. Husb. 22: (In Japanese) 79. Koeniger, N., Held, T., Vorwohl, G Possible effects on honey of treatments with formic acid. See Ref. 15. In press 80. Koeniger, N., Ritter, W., Ruttner, F Varroa jacobsoni and its control in the FRG. Abstr. 16th Znt. Congr. Entomol., Kyoto, Japan, p. 425 (Abstr.) 81. Koivulehto, K Varroa jacobsoni -a new mite infesting honeybees in Europe. Br. BeeJ. 104: Koivulehto, K Tropilaelaps clareae-another mite threatening world beekeeping. Br. Bee J. 108: Kornissar, A. D An installation for thermal treatment during Varroatose. Pchelovodstvo (11): (In Russian) 84. Kramer, K Zur Varroa-Situation. Die Biene (2): Kulikov, N. S Varroasis of bees. Pchelovodstvo (11): (In Russian) 86. Laigo, F. M., Morse, R. A The mite Tropilaelaps clareae in Apis dorsata colonies in the Philippines. Bee World 49: Laigo, F. M., Morse, R. A Control of the bee mites, Varroa jacobsoni Oudemans and Tropilaelaps clareae Delfinado and Baker with chlorobenzilate. Philipp. Entomol. 1: Langhe, A. B., Natskii, K. V The mite varroa and the methods of controlling it. Pchelovodstvo (3):16-20 (In Russian) 89. Langhe, A. B., Natskii, K. V., Tatsii, V. M Biology of varroa mites. Veterinariya Moscow (7):74-77 (In Russian) 90. Langhe, A. B., Natskii, K. V., Tatsii, V. M Evaluation of preparations against Varroatosis of bees. Veterinariya Moscow (9):73-77 (In Russian) 90a. Lindquist, E. E An unusual new species of Tarsonemus (Acarina: Tarsonemidae) associated with the Indian honey bee. Can. Entomol. 100: Lolin, M PN~ primer varoatoze ueotovlien v nasi drzavi. Slovenski &bela; 79(1): 15; Apic. Abstr L/79 (Abstr.) 92. an son, D. C. M A new genus and species of mesostigmatid mite (Acarina: Ameroseiidae) associated with honey bee from Tonga. J. R. Soc. N, Z. 4: Marin, M Diagnosis and treatment of Varroasis. See Ref. 49, pp AMaul, V., Peterson, N., Wissen, W Peldversuche zur klinischen Er-

22 250 DE JONG, MORSE & EICKWORT probung von Kelthane und Brompropylat. ADIZ (5): Mautz, D Gemulluntersuchung zur fruhzeitigen Erkennung. ~mke; freund 34: Mautz, D Untersuchungsergebnis: Erster bayerischer Varroa-Befall. Imkerfreund 34: Menapace, D. M., Wilson, W. T Acarapis woodi mites found in honey bees from Colombia, South America. Am. Bee J. 120:761-62, Michael, A. S Tropilaelaps clareae, a mite infesting honeybee colonies. Bee World 43: Michael, A. S United States Federal and State Bee Disease Laws. In Honey Bee Pesrs, Predators, and Diseases, ed. R. A. Morse, pp Ithaca, NY: Cornell Univ. Press 100. Milne, P. S Acarine disease in Apis indica. Bee World 38: a. Mo, C.-F Studies on the lifehistow of Neocvoho/aelaos indica ~vani (Acarina, ~meroseiidae). New Asia Acad. Ann. 13: Montiel, J. C., Piola, G. A A new enemy of bees. See Ref. 49, pp Morgenthaler, Bienenkrankheiten im Jahre Schweiz. Bienen- Ztg. 49: 17680, Morgenthaler, Problems on acarine disease. Scott. Bee J. 27: Morison, G. D An Acarapis living externally on the honey-bee. Bee World 12: Moritz, R. F. A Altersabhangige Empfindlichkeit von Vorroa jacobsoni Oudemans gegen K-79 (Chlordimeformhydrochloride). See Ref. 15. In press 106. Moritz, R. F. A., Koeniger, N., Maul, V Verteilung systemisch wirksamen Praparate im Bienenvolk (Apis mellqera L.). See -Ref In press 107. Morse, R. A The beekeeping potential in the Philippines. Glean Bee Cult. 94: Morse, R. A Asian bee mites. Glean. Bee Culr. 97:287, Morse, R. A Arachnids: Acarina (mites and ticks). See Ref. 99, pp Morse, R. A Research Review. Glean. Bee Cult. 107: Morse, R. A., Benton, A. W Venom collection from species of honeybees in south-east Asia. Bee World 48: Morse, R. A.,.Goncalves, L. S Varroa disease, a theat to world bee- keeping. Glean. Bee Cub. 107: , Morse, R. A., Laigo, F. M Beekeeping in the Philippines. Univ. Philipp. Coll. Agric. Farm Bull. 27:l Morse, R. A., Laigo, F. M The potential and problems of beekeeping in the Philippines. Bee World 50: Nakano, S Flowers, bees and people. Pt. 2. Chemical control of mites. Jpn. Bee J. 23(2):41-44 (In Japanese) 116. Nedealkov, S Protection of bees health in the Bulgarian People's Republic. Apimondia Bucharest 24: Nedealkov, S Varroasis in Bulgaria, experience gained from controlling this bee parasitosis. See Ref. 49, pp rosi-Pal, Experiments on the feeding habits of the Acarapis mites. Bee World 15: Orosi-Pal, Identifying the bee louse Braula and the big mite in Asia. See Ref. 49, pp Oudernans, A. C Acarologische Aanteekeningen XII. Entomol. Ber. Uitgegeven Door Ned. Enromol. Verh. 1 : Pandey, R. S Varroajacobsoni: a new mite infesting honeybees (Apis indica) colonies in India. Bee World 48: Phadke, K. G., Bisht, D. S., Sinha, R. B. P Occurrence of the mite Varroa jacobsoni Oudemans in the brood cells of the honey bee, Apis indica F. Indian J. Enromol. 28: Poltev, V. I., Davydova, M. S., Sapchenko, V. L Varroa disease and its control. Int. Bee Congr. Prelim. Sci. Meet. 21 : Poltev, V. I., Likhotin, A. K Diagnosis and treatment of Varroa disease in honey bees. Veterinariya Moscow '(11):60-61 (In Russian) 125. Rademacher, E Control of Varroa disease with K-79. See Ref. 15. In press 126. Rangarajan, A. V Occurrence of the mite Vorroa jacobsoni Oudemans on the Indian honey bee in South India. Sci Cult. 37: Rau, C Varroa-Weibchen von der Unterseite. Photographs. - - ADIZ (5):168a 128. Renninghoff, V., Ritter, W Erfahrung mit der Varroatosc+Therapie in Tunesien. ADIZ (5): Ritter, W Varroa disease control in Taunus region atpresent: Results of "thetreatment with Varostan applied in

23 HONEY BEE MITES '251 Autumn Apiacta Bucharest 13: kiter, W Neueste Erkenntnisse uber die Varroatose. ADIZ (12): Ritter, W Versuche mit Kelthane. ADIZ (5): Ritter, W., Kakai, T., Takeuchi, K The development and control of Varroatosis in Japan. See Ref. 15. In press 133. Ritter, W., Ruttner, F Chemotherapie (Varroa). ADIZ (5): Ritter, W., Ruttner, F Diagnoseverfahren (Varroa). ADIZ (5)- : Ritter, W., Ruttner, F Neue Wege in der Behandlung der Varroatose. 1. Ameisensaure. ADIZ (5): Ruttner, F Die Varroa-Milbe, Erkennung und Behandlung. Bienenvater 99(4): Ruttner, F Varroa-Bericht Nr. 2. Die Biene (1): Ruttner, F Field experiments with K-79. See Ref. 15. In press 139. Ruttner, F., Koeniger, N Experiments to eliminate Varroa mites by biological methods. Apiacta Bucharest 14:159-60, Ruttner, F., Koeniger, N., Ritter, W Brutstop und Brutentnahme. ADIZ (5): Ruttner, F., Ritter, W Das Eindringen von Varroa jacobsoni nach europa im Ruckblick. ADIZ (5): Ruttner, F., Ritter, W., Gotz, W Chemotherapie der Varroatose uber die Haemolymphe der Biene. ADIZ (5): Sadov, A. V Study of female varroa. Pchelovodstvo (8):15-16 (In Russian) 144. Sadov, A. V Anatomy of the female varroa mite. Pchelovodsrvo (7): (In Russian) 145. Sakai, T., Takeuchi, K., Hara, A Studies on the life history of a honey bee mite, Varroa jacobsoni Oudemans, in laboratory rearing. Bull. Fac. Agric. Tamagawa Univ. No : (In Ja anese) 146. ~af'chenko. V. L The bioloev of the mode of life of the mite V&oa jacobsoni Bull. Apic. Doc. Sci. Tech. InJ 9: Sal'chenko. V. L Diagnosis and treatment of varroa infestation. Veterinariya Moscow (8):62-64 (In Russian) 148. Samsinak, K., Haragsim, The mite Varroa jacobsoni imported into Europe. Vcelarstvi 25:268-66' ' (In Czech) 148a. Samsinhk, K., Vobrhzkovh, E., Haragsim, Melittiphis alvearius Berlese, a little known bee mite. J. Apic. Res. 17: Sarian, Z. B Beekeeping in the Philippines. Glean. Bee Cult. 94:486-91, Seeley, T. D., Morse, R. A The nest of the honey bee (Apis mellifra L.).. Insectes SOC. 23: Sevllla, V. J Observations of the life histov and habi~s of three new acarine pests of honey bees in the Philippines. BS thesis. Univ. Philipp. Los Banos. 42 pp Shabanov, M., Nedealkov, S., Toshkov, A Varroatosis-a dangerous parasitic disease of bees. Am. Bee J. 118:402-3, Shaw, F. R., Fischang, W. J., Balboni, E. R., Eversole, J. W External mites on honeybees in U.S. Glean. Bee Cult. 89:402-3, Shung, C. C Recommendations for treating mites infecting honeybee colonies. J. Bee Cult. China (1): 13-14, IBRA Transl. No. E Simetskii, M. A., Smirnov, A. M., Kudriavtsev, E. A The struggle with Varroatosis of bees. Veterinariya Moscow (4):78-80 (In Russian) 156. Singh, S Acarine disease in the Indian honey bee (Apis indica F.). Indian Bee J. 19: Smirnov, A. M Prophylaxis of infestation with Varroa and Acarapis mites: methods of treatment. Pchelovodstvo (7):27-30 (In Russian) 158. Smirnov, A. M Research results obtained in USSR concerning aetiology, pathogenesis, epizootiology, diagnosis and control of Varroa disease in bees. Apiacta Bucharest 13: Smirnov. A. M.. Chernov. K. S (In ~ussian) 160. Smith, I. B Varroa acobsoni in Maryland? Glean Bee Cul. 108: Stephen, W. A. 1968:Mites: a beekeeping problem in Vietnam and India. Bee World 49: Stolbov, N. M., Vasikov, N. A An apparatus for discovering the varroa mite. Pchelovodstvo (8): 17 (In Russian) 163. Stort, A. C., Gon$alves, L. S., Malaspina, O., Duarte, F. A. M Study of the efficacy of Syneacar for control of Varroa jacobsoni. Apidologie. In press

24 252 DE JONG, MORSE & EICKWORT 164. Subhapradha, C. K Enemies and pests of bees encountered in this area. Indian Bee J. 23(3): Takeuchi, K., Ichljii, O., Sakai, T The bee and the environment in Japan. Apimondia Grenoble 25: Tewarson. N. C Imrnunolonical studies on the role of honeybee himolymph proteins for nutrition and reproduction of Varroa jacobsoni. See Ref. 15. In press 167. Toscano, H Varroasis. Peligrosa Enfermedad de las Abejas. Bol. InJ Minist. Agric. Pesca 11(8): Tverdyi, P. G A trap for varroa mites. Pchelovodsrvo (1):21 (In Russian) 169. Tzivilev, I. V Phenothiazine for controllin varroa and the bee louse. PcheIovod%o (6):17 (In Russian) 170. US Department of Agriculture Honey Market News. 64(1): Veitch, R Rpt. Chief Entomol. De t. Agric. Stock, Queensl ~eftchkov, V., Natchev, P Investigation of Varroa jacobsoni and of its iduence on the development of bee colonies. Apimondia 24: Weide, W The significance. of the house mite in beekeephg and its control. Leioz. Bienetizta. - 74:9 (In German) 174. Wissen, W., Maul, V Experiments concerning procedures of application of the formic acid to control Varroa disease. See Ref. 15. In press 175. Zahariev, N The experience gained by the district apicultural council of Plevna in controlling Varroasis. See Ref. 49, pp