Identification and comparison of species infesting honey bees Lilia I. de Guzman, Thomas E. Rinderer

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Lilia I. de Guzman, Thomas E. Rinderer. Identification and comparison of Varroa species infesting honey bees. Apidologie, Springer Verlag, 1999, 30 (2-3), pp.85-95. ￿hal-00891570￿

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Identification and comparison of Varroa species infesting honey bees

Lilia I. de Guzman Thomas E. Rinderer

ARS, USDA, Breeding, Genetics and Physiology Laboratory, 1157 Ben Hur Road, Baton Rouge, LA 70820, USA

(Received 26 July 1998; accepted 21 February 1999)

Abstract - Oudemans, V. underwoodi Delfinado-Baker and Aggarwal and V. rindereri de Guzman and Delfinado-Baker are obligatory parasites of honey bees. The key mor- phological characters, host range and geographic distribution of these three species are reviewed. The occurrence of different genotypes of V. jacobsoni, their geographic distribution and virulence on honey bee hosts are discussed. © Inra/DIB/AGIB/Elsevier, Paris

Varroa jacobsoni / Varroa underwoodi / Varroa rindereri / morphology / genotype / host range / distribution

1. INTRODUCTION covery of still more species of Varroa. This review compares the key morphological characters, host and distribution of There are three known species of Var- range the three known Varroa In addi- roa (Acari: Varroidae) parasitizing honey species. bees (Apis spp.), namely: Varroa jacobsoni tion, the genetic diversity of V. jacobsoni Oudemans 1904, V. underwoodi Delfinado- and its possible correlation to the virulence Baker and Aggarwal 1987 and V. rindereri of mites on infested hosts are also discussed. de Guzman and Delfinado-Baker 1996. The recent identification of V. rindereri from the cavity dwelling honey bee, Apis kosche- 2. VARROA JACOBSONI vnikovi Buttel-Reepen, in and the identification of different varieties of The general morphology and chaetotaxy V. jacobsoni indicate the need for further of V. jacobsoni, V. rindereri and V. under- investigations which may lead to the dis- woodi are very similar. However, V. jacob-

* Correspondence and reprints E-mail: [email protected] soni and V. rindereri are transversely oval as R and J genotypes were established by using opposed to the ellipsoidal shape of V. under- two RAPD primers [15]. In the R genotype, woodi. V. jacobsoni can be distinguished primer OPE-07 produced a 766-bp band from V. rindereri by several characters which was absent in the J genotype (figure 1) including small size, short and sharp-looped [ 15]. Similarly, using primer OPP-03, the peritreme, fewer endopodal setae and pres- R genotype produced a band at 442 bp not ence of a seta on the palpal trochanter (table I). found in the J genotype. The J genotype pro- A more detailed description of characters duced two distinct bands at 675 and 412 bp of the adult female, nymphal stages and that were absent in the R genotype. adult male of V. jacobsoni are described by Oudemans [45] and Delfinado-Baker [26], The PCR amplification and subsequent respectively. restriction enzyme digestion of a portion of the mtDNA CO I region [4] was also used to Delfinado-Baker and Houck [28] found distinguish between the R and J genotypes some morphological differences between [16]. When the PCR products were digested populations of V. jacobsoni, especially with Sst I, the fragment amplified from mites regarding body size. In general, V. jacob- with the R genotype did not undergo diges- soni that infests A. cerana F. is smaller than tion (producing a single band of 519 bp). those infesting A. mellifera L. These differ- Sst I digestion of the fragment from the ences may be due to the existence of at least J genotype produced fragments of 236 and three genotypes of V. jacobsoni: Russian (R), Japanese (J) and Papua New Guinea (PNG) genotypes [4, 14-17]. We use the term ’genotype’ to indicate mites having common DNA variations within the native range of V. jacobsoni. This definition fol- lows that of King [34]. The R genotype is also referred to as the GER genotype by Anderson and Fuchs [4]. In a previous anal- ysis using random amplification of poly- morphic DNA (RAPD), Kraus and Hunt [37] found bands that were shared by Ger- man and US V. jacobsoni but absent in Malaysian mites. Using the same technique, 338 bp in length, similar to the pattern observed in PNG (figure 2). Digestion with Xho I did not show any differences between R and J genotypes (fragments of 269 and 300 bp). However, the PNG type lacked the restriction site, producing a single band of 519 bp [4].

2.1. Host range

V. jacobsoni was first discovered infest- ing A. cerana in Java, . It has since successfully extended its host range to dif- ferent honey bee species, including intro- duced A. mellifera in Asia (table II). 2.2. Distribution Recently, V. jacobsoni was observed in drone brood of A. nigrocincta Smith in Since its discovery in 1904 by Oude- Sulawesi, Indonesia [32]. Infestation of mans, V. jacobsoni has been found through- V. jacobsoni has also been reported in out the world except Australia, New colonies of A. koschevnikovi in Borneo [29]. Zealand, Hawaii and parts of Africa [40]. However, it is possible that this report may However, recent genetic studies revealed be referring to V. rindereri instead of V. that the R genotype is actually the predom- jacobsoni. V. jacobsoni was also found inant genotype of V. jacobsoni. The PNG infesting mixed populations of the newly or ’NRP’ strain, which is currently found described honey bee species, A. nuluensis only in Asia, is the type of V. jacobsoni that Tingek, Koeniger and Koeniger and A. cer- Oudemans described in 1904 [1, 4]. There- ana in Borneo [13]. With this mixed bee fore, the PNG genotype found in Java, species condition, the actual colony source Indonesia is not the type that has spread of the V. jacobsoni is unclear. worldwide as originally thought. This was supported by further DNA analyses, which The reported global differences in the revealed that the R and J genotypes had a virulence of V. jacobsoni toward A. mellif- wider distribution than the PNG type era may suggest that some genotypes of V. [14-17]. The R genotype was the most pre- jacobsoni have reduced virulence. DNA dominant type being found in much of analyses revealed variable genotypes of Europe, Russia, South and North America, V. jacobsoni infesting A. mellifera and Africa, and Asia. The J genotype has been A. cerana in Asia [4, 14-17] (table III). Lack recorded in South and North America, and of virulence of the PNG genotype of Asia (table III). V. jacobsoni has been documented in PNG and Indonesia [1, 4]. This V. jacobsoni reproduces in A. cerana drone brood, but 2.3. Virulence not in drone and worker brood of A. mellif- era [4]. Whether or not this characteristic is specific to the PNG genotype has yet to be V. is known to be the most jacobsoni seri- investigated. The PNG genotype was also ous parasite of A. mellifera worldwide. It recorded in Borneo and the Philippines causes abnormalities, reduced weight and infesting A. cerana colonies (de Guzman, longevity of workers and drones, reduced unpublished data). mucus gland and seminal vesicle weights, In contrast, tremendous losses of A. mel- reduced number of spermatozoa, death of due to V. infestations were brood and death of adult lifera jacobsoni young premature recorded in the and Korea [10, bees [5, Enormous losses Philippines 18, 23, 30, 47, 49]. 11]. Both countries have the R of managed honey bee colonies in Europe genotype. The R genotype was a recent introduction [38, 48] and the United States have [33] into Java, Indonesia [2, 4] but the level of been reported. Likewise, the establishment virulence in A. mellifera colonies has not of V. jacobsoni in the US resulted in the been monitored. Both R and J genotypes of apparent loss of much of the feral population V. jacobsoni were found in [15]. of honey bees. However, Tropilaelaps clareae which pre- Different honey bee species and sub- dominates in the colonies could mask the effects of V. in species of A. mellifera vary in response to jacobsoni A. mellifera V. jacobsoni [9, 20, 22, 43, 44, colonies. T. clareae is reported to be a more 46, 48]. For instance, in Asia, where the injurious parasite to A. mellifera than V. V. is also a indigenous A. cerana and introduced A. mel- jacobsoni [6, 8]. jacobsoni for A. lifera are now sympatric, effects of V. jacob- major problem mellifera beekeeping in In A. soni parasitism on these two honey bee [31]. Vietnam, mellifera colonies have the R while colonies species are quite different. While A. cerana genotype, of A. cerana have the J regulates V. jacobsoni infestations success- genotype [15]. This observation the differential fully, A. mellifera seems to be very suscep- may explain tible to V. jacobsoni infestations. This resis- reproduction of V. jacobsoni observed in A. and A. cerana colonies in Viet- tance of A. cerana is due to their ability to mellifera nam The J was confine mite reproduction to drone brood, in [7]. genotype found in both A. addition to having good grooming and mellifera and A. cerana japonica in Japan [14]. Since the 1970s, no extensive hygienic behavior [35, 46]. However, repro- colony duction of V. jacobsoni has been observed in mortality has been reported in Japan (T. Yos- worker brood of A. cerana in Korea and hida, pers. comm.). Japan [19, 51]. Whether or not mite geno- V. jacobsoni also is a serious problem in type influences the ability of V. jacobsoni Europe [38, 48] and the US [33] but not in to reproduce in A. cerana worker brood is Brazil where Africanized honey bees are unknown. abundant [20, 24]. This disparity in viru- lence may be due to the genotypic differ- 3. VARROA UNDERWOODI ences of the mites rather than the genotypic differences of the honey bees [9, 41 ] or cli- V. underwoodi can easily be distinguished matic reasons [25]. European honey bees from V. jacobsoni and V. rindereri by its have survived V. jacobsoni infestations with- small size, ellipsoidal shape and long lateral out treatment for more than 12 years in marginal setae radiating outward. Among Brazil [22] and Puerto Rico (D. Pesante, populations of V. underwoodi, size variation pers. comm.). Only the R genotype has been has been reported, although some measure- found in Europe and this same genotype ments are well within the range reported by also predominates in the US. Both Brazil Delfinado-Baker and Aggarwal [27] for the and Puerto Rico have the J genotype of type specimen (table IV). The smallest V. jacobsoni [14, 16, 17]. The virulence of V. underwoodi was recorded in PNG from V. jacobsoni in A. nigrocincta and A. nulu- A. mellifera colonies [3]. The one specimen ensis colonies has yet to be investigated. collected from Borneo, [13] was the largest. This mite from Borneo also has Our knowledge on the genetic diversity fewer endopodal setae when compared to of V. jacobsoni raises questions regarding V. underwoodi from Korea. the basis of honey bees’ resistance to this parasite. It also opens taxonomic issues which need to be carefully examined. Fur- 3.1. Host range and distribution ther studies may result in the identification of other species of Varroa, and a clarifica- V. underwoodi was first described in tion of genetic differences in V. jacobsoni 1987 infesting colonies of A. cerana in that may explain varied reports of the sever- Nepal [27]. Knowledge of its host range and ity of V. jacobsoni infestation. Certainly, as geographic distribution is rapidly expand- mites continue to be spread about the world, ing. This parasitic mite has been detected opportunities for mites from different geo- on A. cerana in Korea [50], and A. cerana graphic origins to interbreed increase. New and A. mellifera in Papua New Guinea [3, combinations of genetic markers may pro- 39]. In 1996, V. underwoodi or a similar vide evidence of hybridization. However, species was observed parasitizing A. nulu- this is likely to occur very slowly, since ensis or A. cerana in Borneo [13]. The mite V. jacobsoni has a life history that only occa- was found tightly tucked in between the sionally leads to out-crossing. sternites of A. nuluensis collected from mixed populations of A. nuluensis and not present in V. jacobsoni while one band A. cerana. The coincidence of its collection present in V. jacobsoni was not found in with A. nuluensis workers suggested that it V. rindereri. There were two bands shared likely came from the A. nuluensis colony. between the two Varroa species. V. underwoodi was also observed in A. cer- The biology of V. rindereri has not been ana and on A. newly recognized nigrocincta studied. However, this mite species may be colonies in Indonesia [3]. V. under- Recently, specific to A. koschevnikovi. This was sup- woodi was observed in Vietnam in drone ported by the absence of cross infestation brood of A. cerana de (L. Guzman, unpub- between the A. koschevnikovi and A. cer- lished data), which is the first record on the ana colonies in the same apiary. DNA anal- occurrence V. in of underwoodi Vietnam. ysis showed that all mites collected from Little is known about the biology of this the A. koschevnikovi colonies were V. rin- parasite. The mite reproduces on drone dereri while those mites collected from the brood of A. cerana [50] and A. nigrocincta A. cerana colonies at the same apiary were [3]. Although V. underwoodi has been all V. jacobsoni. In addition, differences in observed on A. mellifera, no reproduction the phoretic behavior of the two mite species was noted. The potential of this Varroa during the collection were also observed. species to become a serious parasite of When pupae were removed from their cells, A. mellifera and other Apis species needs to V. jacobsoni tended to hang onto the pupal be studied. hosts while V. rindereri remained inside the cells [13]. 4. VARROA RINDERERI 4.1. Host range and distribution V. rindereri is a parasite of A. kosche- vnikovi, another cavity nesting honey bee V. rindereri has been only reported in commonly known as the red bee, which is colonies of A. koschevnikovi in Borneo, sympatric with A. cerana in Borneo, Malaysia Malaysia. [13]. Adult females of V. rindereri are sim- ilar to V. jacobsoni females. However, V. rindereri is x 1 698 than larger (1 180 μm) ACKNOWLEDGEMENTS V. jacobsoni from Indonesia, mean: 1 065 x 1 575 μm [45]; Europe, mean: 1 117 x We thank numerous colleagues and bee- 1 677 μm or SW Asia, mean: 1 108 x 1 660 μm keepers for collecting Varroa samples for DNA [28]. Although V. rindereri is larger than analyses, and T. Stelzer for his technical help. V. jacobsoni ( 1 077 x 1 596 μm) from Bor- This manuscript is completed in cooperation with neo, the numbers of setae and pores on the Louisiana Agricultural Experiment Station. sternal shield of V. rindereri are fewer (table I). Likewise, V. rindereri differs from V. jacob- soni or V. underwoodi by its long and wide- Résumé - Identification et comparaison looped peritreme. The trochanter of the pal- des espèces de Varroa, parasites des pus lacks a seta. A seta is always present on abeilles mellifères. Il existe trois espèces palpal trochanters of V. jacobsoni and de Varroa parasitant les abeilles mellifères V. underwoodi. (Apis spp.) : Varroa jacobsoni Oudemans De Guzman and Delfinado-Baker [ 13] 1904, V. underwoodi Delfinado-Baker et also showed that V. rindereri is genetically Aggarwal, 1987 et V. rindereri de Guzman different from the V. jacobsoni from Bor- et Delfinado-Baker, 1996. V. jacobsoni est neo. Using RAPD primer OPD-01, V. rin- l’espèce la plus importante du point du vue dereri showed two specific bands that were économique. Ces trois espèces ont une mor- phologie et une chétotaxie (nomenclature espèces de Varroa et la clarification des dif- et répartition des soies) semblables. Néan- férences entre biotypes pourrait conduite à moins V. jacobsoni et V. rindereri ont une un jugement nuancé sur les conséquences forme ovale transversale contrairement à la d’une infestation par V. jacobsoni. forme elliposoïdale de V. underwoodi. V. underwoodi se distingue facilement des V. jacobsoni se distingue de V. rindereri par deux autres espèces par sa petite taille, sa sa petite taille, son péritrème court et enroulé forme ellipsoïdale et par les longues soies à boucles serrées, des soies de l’endopode latérales rayonnant vers l’extérieur. On a moins nombreuses et la présence d’une soie signalé une variation de taille parmi les sur le trochanter palpal (tableau I). V. jacob- populations de V. underwoodi, bien que cer- soni a été signalé comme parasite d’Apis taines mesures entrent bien dans les limites mentionnées Delfinado-Baker et cerana, A. mellifera, A. koschevnikovi, par Aggar- A. nigrocincta et A. nuluensis [13, 29, 32] wal [27] pour le spécimen type (tableau IV). (tableau II). V. jacobsoni est présent dans V. underwoodi a été décrit pour la première le monde entier à l’exception de l’Australie, fois en 1987 comme parasite dans des colo- nies d’A. cerana au Cet acarien de la Nouvelle-Zélande, d’Hawaï et de cer- Népal [27]. taines régions d’Afrique [40]. Des études parasite a été signalé sur A. cerana en Corée sur A. cerana et A. en génétiques récentes ont montré que l’un des [50], mellifera Papoua- génotypes de V. jacobsoni prédominait [4, sie Nouvelle-Guinée [3, 39], sur A. nuluensis 14-17]. Parmi les trois génotypes de V. jacob- ou A. cerana à Bornéo [13] et sur A. cerana et A. nigrocincta en Indonésie [3]. On a soni connus, le russe (R), le japonais (J) et celui de Papouasie Nouvelle-Guinée (PNG), récemment observé V. underwoodi dans des cellules de couvain de mâles d’A. cerana le génotype R a une répartition plus large au Vietnam. C’est la première fois qu’il est que les deux autres [14-17]. Il a été trouvé signalé au Vietnam. La biologie de ce para- dans la majeure partie de l’Europe, en Rus- site est peu connue. Il se reproduit sur le cou- sie, en Amérique du Nord et du Sud, en vain de mâles d’A. cerana [50] et d’A. nigro- Afrique et en Asie (tableau III). Le géno- cincta [3], mais aucune sur J a été en du Sud et reproduction type signalé Amérique A. mellifera n’a été signalée. du Nord et en Asie. Le PNG n’est génotype V. rindereri A. koschevnikovi à Bor- actuellement Asie. Le parasite présent qu’en géno- néo, Malaisie [ 12]. Les femelles adultes de R est aussi GER type appelé génotype par V. rindereri ressemblent à celles de V. jacob- Anderson et Fuchs [4]. Les R et génotypes soni. V. rindereri est pourtant plus grand et J ont été déterminés par deux amorces RAPD possède moins de soies et de pores sur le et l’endonucléase de restriction Sst I [15, bouclier sternal que V. jacobsoni (tableau I) 16]. Le PNG a été Ander- type séquencé par [28]. V. rindereri a un péritrème long et son et Fuchs et vraisemblable- correspond enroulé à boucles lâches, son trochanter pal- ment au de V. décrit type jacobsoni par pal est dépourvu de soies. Sur le plan géné- Oudemans en 1904 Le PNG [1, 4]. génotype tique aussi, V. rindereri a pu être différentié l’on trouve à n’est donc que Java, Indonésie, de V. jacobsoni de Bornéo par l’utilisation pas le type répandu sur tout le globe comme de l’amorce OPD 01 RAPD [12]. Jusqu’à on le à Notre connaissance pensait l’origine. présent la biologie de V. rindereri n’a pas été de la diversité de V. génétique jacobsoni étudiée. Il n’a été signalé que dans des colo- soulève des questions concernant les bases nies d’A. koschevnikovi à Bornéo, Malai- de la résistance des abeilles mellifères à ce sie. © Inra/DIB/AGIB/Elsevier, Paris parasite. Elle débouche aussi sur des pro- blèmes taxonomiques qui nécessitent d’être Varroa jacobsoni / Varroa underwoodi / étudiés avec soin. De futures études pour- Varroa rindereri / morphologie / distribution raient aboutir à l’identification de nouvelles géographique / génotype Zusammenfassung - Bestimmung und Indonesien gefundene Genotyp PNG nicht Vergleich der Arten von Varroa auf wie ursprünglich angenommen der, welcher Honigbienen. Von der Gattung Varroa sind sich weltweit verbreitet hat. Unsere Kennt- drei verschiedene auf Honigbienen parasi- nis der genetischen Vielfalt von V. jacob- tierende Arten bekannt: Varroa jacobsoni soni wirft einige Fragen bezüglich der Oudemans, V. underwoodi Delfinado - Grundlage der Resistenz von Honigbienen Baker and Aggarwal, und V. rindereri de gegen diesen Parasiten auf. Ebenso eröff- Guzman and Delfinado - Baker. Von diesen net sich ein taxonomisches Feld, das sorg- ist V. jacobsoni wirtschaftlich am bedeu- fältig untersucht werden muß. Zukünftige tendsten. Generell sind diese drei Arten mor- Studien könnten zur Identifikation weiterer phologisch und chaetotaxonomisch sehr Arten von Varroa führen, und eine Klärung ähnlich. Jedoch sind V. jacobsoni und der Unterschiede zwischen den Biotypen V. rindereri queroval, im Gegensatz zu der könnte eine differenzierte Beurteilung der elliptischen Form von V. underwoodi. Folgen eines Befalls mit V. jacobsoni V. jacobsoni kann von V. rindereri durch ermöglichen. die geringere Größe, durch kurze und scharf- V. underwoodi kann durch seine geringere geschlungene Peritreme, eine geringere Größe, ellipsoide Form und die langen seit- Anzahl von endopodalen Borsten und das lich ausstrahlenden Borsten von V. jacob- Fehlen einer der Borsten am palpalen Tro- soni und V. rindereri unterschieden werden. chanter unterschieden werden (Tabelle I). Es wurde über eine Variation der Größe V. jacobsoni wurde parasitierend auf zwischen verschiedenen Populationen von A. cerana, A. mellifera, A. koschevnikovi, V. underwoodi berichtet, obwohl einige der A. nigrocincta und A. nuluensis gefunden Messungen noch innerhalb des von Delfi- [13, 29, 32] (Tabelle II), und ist auf der nado-Baker und Aggrawal [27] für den ganzen Welt verbreitet außer in Australien, Holotypus angegebenen Bereichs liegen Neuseeland, Hawaii und Teilen Afrikas [40]. (Tabelle IV). V. underwoodi wurde 1987 Neuere Studien belegen, daß hierbei einer zuerst aus Völkern von A. cerana in Nepal der Genotypen von V. jacobsoni vorherr- beschrieben [27]. Diese parasitische Milbe schend ist [4, 14-17]. Unter den drei bekann- wurde bislang in Völkern von A. cerana und ten Genotypen von V. jacobsoni [Russisch A. mellifera in Papua Neu Guinea [3, 39], (R), Japanisch (J) und Papua Neu Guinea A. nuluensis und A. cerana in Borneo [13], (PNG)] hat der Genotyp R eine weitere Ver- A. cerana und A. nigrocincta in Indonesien breitung als J oder PNG [14-17]. Der Geno- entdeckt [3]. Kürzlich wurde A. underwoodi typ R wurde in den meisten Teilen von in Drohnenbrutzellen von A. cerana in Viet- Europa, Russland, Süd- und Nordamerika, nam beobachtet, dies war der erste Bericht Afrika und Asien gefunden (Tabelle III). über das Vorkommen von V. underwoodi Der Genotyp J wurde in Süd- und Norda- in Vietnam. Über die Biologie dieses Para- merika und in Asien, der Genotyp PNG bis- siten ist nur wenig bekannt. Die Milbe repro- lang nur in Asien gefunden. Der Genotyp duziert in Drohnenbrut von A. cerana und R wurde von Anderson und Fuchs [4] als A. nigrocincta, eine Fortpflanzung in A. mel- Genotyp GER bezeichnet. Die Genotypen lifera wurde nicht festgestellt. R und J wurden durch RAPD Primer (ran- V. rindereri ist ein Parasit von A. koschev- dom amplification of polymorphic DNS) nikovi in Borneo, Malaysia [12]. Die adulten und Sst I Restriktionsendonucleasen [ 15, Weibchen von V. rindereri ähneln denen 16] etabliert. Der PNG Typus wurde von von V. jacobsoni. V. rindereri ist allerdings Anderson und Fuchs [1] sequenziert und ist größer und besitzt eine geringere Anzahl aller Voraussicht nach identisch mit dem von Borsten und Poren auf dem Bauchschild 1904 von Oudemans beschriebenen Typus als V. jacobsoni (Tabelle I) [28]. V. rindereri von V. jacobsoni [4]. Daher ist der auf Java, hat lange und weitgeschlungene Peritremen und es fehlt eine der Borsten auf dem Tro- [11] Choi S.Y., Chemical control of Varroa mites in chanter der Bei des Korea, in: Needham G.R., Page R.E., Delfinado- Palpen. Benutzung Baker M., Bowman C.E. (Eds.), Africanized RAPD Primers OPD 01 kann V. rindereri Honey Bees and Bee Mites, Ellis Horwood Lim- auch genetisch von V. jacobsoni von Borneo ited, Chichester, 1988, pp. 413-416. unterschieden werden [12]. Die Biologie [12] de Guzman L.I., Delfinado-Baker M., A new von V. rindereri wurde bisher nicht unter- species of Varroa (Acari: Varroidae) associated with Apis koschevnikovi (: sucht. wurde V. rindereri nur in ) Bislang in Borneo, Int. J. Acarol. 22 (1996) 23-27. Völkern von A. koschevnikovi in Borneo [13] de Guzman L.I., Rinderer T.E., Whiteside R., gefunden. © Inra/DIB/AGIB/Elsevier, Paris Scientific note on the infestation of Varron on Apis nuluensis, Apidologie 27 (1996) 429-430. 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