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Spatial aggregation of phoretic mites on Bombus atratus and Bombus opifex (Hymenoptera: Apidae) in Argentina

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Abstract

Mites have been observed on the bumblebee’s body and inside their nest for over 150 years, and parasitic relationships between them have occasionally been reported. One of the most interesting animal associations between mites and bees is phoresy. At present, no study has evaluated the distribution patterns of phoretic mites on bumblebees nor the factors that might be influencing such association. The main goal of this research was to determine whether an aggregation of external mites on bumblebees is influenced by (a) the phoretic mite load per bee, (b) the host species, (c) the caste of bumblebee, (d) the interaction between mite load and bee species, and (e) the presence of a suitable physical place for the mites to accommodate on the bee body. The following mite species were recorded on Bombus atratus and Bombus opifex: Kuzinia laevis, Kuzinia americana, Kuzinia affinis, Kuzinia sp., Pneumolaelaps longanalis, Pneumolaelaps longipilus, Scutacarus acarorum, and Tyrophagus putrescentiae. Our results indicate that Kuzinia mites have a strong preference for a particular region on the propodeum, which has shorter hairs than on most areas of the body. In addition, generalized linear model analysis demonstrated that mite aggregation was influenced by the caste and host species.

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References

  • Abrahamovich, A.H., Bischoff de Alzuet, A.D. (1989) Relaciones foréticas entre ácaros (Acaridae y Chaetodactylidae) e Himenópteros (Anthophoridae, Xylocopinae). Rev. Soc. Ent. Arg. 47(1-4)

  • Abrahamovich, A.H., Tellería, M.C., Díaz, N.B. (2001) Bombus species and their associated flora in Argentina. Bee World 82, 76–87

    Google Scholar 

  • Abrahamovich, A.H., Díaz, N.B., Lucia, M. (2007) Identificación de las “abejas sociales” del género Bombus (Hymenoptera, Apidae) presentes en la Argentina: clave pictórica, diagnosis, distribución geográfica y asociaciones florales. Revista Fac. Agron. Univ. Nac. La Plata. 106, 165–176

    Google Scholar 

  • Allen, G.R., Seeman, O.D., Schmid-Hempel, P., Buttermore, R.E. (2007) Low parasite loads accompany the invading population of the bumblebee. Bombus terrestris in Tasmania. Insectes Soc. 54, 56–63

    Article  Google Scholar 

  • Brandenburg, R., Kennedy, G. (1982) Intercrop relationships and spider mite dispersal in a corn/peanut agroecosystem. Entomol. Exp. et applic. 42, 269–276

    Article  Google Scholar 

  • Bush, A.O., Lafferty, K.D., Lotz, J.M., Shostak, A.W. (1997) Parasitology meets ecology on its own terms: Margolis et al. revisited. J. Parasitol 83(4), 575–583

    Article  CAS  PubMed  Google Scholar 

  • Chmielewski, W. (1971) The mites (Acarina) found on bumble-bees (Bombus Latr.) and in their nests. Ekol. Pol. 19, 57–71

    Google Scholar 

  • Chmielewski, W. (1977) Results of observations on associations of mites with insects (Acari - Insecta). Bull. Ent. Pol. 47, 59–78

    Google Scholar 

  • Chmielewski, W. (1998) Mites (Acarina) occurring on social bees (Hymenoptera: Apidae: Apinae, Bombinae). Wiad. Entomol. 6, 201–206

    Google Scholar 

  • Chmielewski, W., Baker, R. (2008) Mites (Acarina) phoretic on some common bumblebee species (Bombus spp.) from the Pulawy area (South-Eastern Poland). J. Apic. Sci. 52, 37–47

    Google Scholar 

  • Donzé, G., Hermann, M., Bachofen, B., Guerin, M. (1996) Effect of mating frequency and brood cell infestation rate on the reproductive success of the honeybee parasite Varroa jacobsoni. Ecol. Entomol. 21, 17–26

    Article  Google Scholar 

  • Eickwort, G.C. (1994) Evolution and life-history patterns of mites associated with bees. In: Houck, M.A. (Ed.), Mites, Chapman and Hall, New York, pp. 218–251

  • Engel, M.S. (2000) Classification of the bee tribe Augochlorini (Hymenoptera: Halictidae). Bull. Am. Mus. Nat. Hist. 250, 1–89

    Article  Google Scholar 

  • Fain, A., Pauly, A. (2001) Notes on phoretic deutonymphs of mites (Acari) associated with Old World Megachilidae and Anthophoridae (Insecta, Hymenoptera), mainly from Madagascar 1. Families Chaetodactylidae, Acaridae, Histiostomatidae and Winterschmidtiidae (Astigmata). Belg. J. Entomol 3(1), 125–142

    Google Scholar 

  • Fain, A., Engel, M.S., Flechtmann, C.H.W., O’connor, B.M. (1999) A new genus and species of Acaridae (Acari) phoretic on Thectochlora alaris (Hymenoptera: Halictidae: Augochlorini) from South America. Int. J. Acarol. 25(3), 163–172

    Article  Google Scholar 

  • Farish, D.J., Axtell, R.C. (1971) Phoresy redefined and examined in Macrocheles muscaedomesticae (Acarina: Macrochelidae), a predator of the house fly. Acarology 13, 16–29

  • Floris, I. (1991) Dispersion indices and sampling plans for the honeybee (Apis mellifera ligustica Spin.) mite Varroa jacobsoni. Oud. Apicoltura 7, 161–170

    Google Scholar 

  • Goulson, D. (2003) Bumblebees: their behavior and ecology. Oxford University Press, Oxford

    Google Scholar 

  • Hadley, A. (2011) CombineZP - Free image stacking software for depth of field correction. Available from http://www.hadleyweb.pwp.blueyonder.co.uk/CZM/combinezm.htm (accessed 21 September 2011)

  • Houck, M.A., O’Connor, B.M. (1991) Ecological and evolutionary significance of phoresy in the Astigmata. Annu. Rev. Entomol. 36, 611–636

    Article  Google Scholar 

  • Huck, K., Schwarz, H., Schmid-Hempel, P. (1998) Host choice in the phoretic mite Parasitellus fucorum (Mesostigmata: Parasitidae): which bumblebee caste is the best? Oecología 115, 385–390

    Article  Google Scholar 

  • Hughes, A.M. (1976) The mites of stored food and houses, 2nd edn. Technical Bulletin 9, Ministry of Agriculture, Fisheries and Food, London

    Google Scholar 

  • Hunter, P.E. (1966) The genus Pneumolaelaps with description of three new species (Acarina: Laelaptidae). J. Kansas. Entomol. Soc. 39, 357–369

    Google Scholar 

  • Hunter, P.E., Husband, R.W. (1973) Pneumolaelaps (Acarina: Laelapidae) mites from North America and Greenland. Fla. Entomol. 56, 77–91

    Article  Google Scholar 

  • Husband, R.W. (1968) Acarina associated with Michigan Bombinae. Pap. Mich. Acad. Sci. Arts. Lett. 53, 109–112

    Google Scholar 

  • Klimov, P.B., Vinson, S.B., O’Connor, B.M. (2007) Acarinaria in associations of apid bees (Hymenoptera) and chaetodactylid mites (Acari). Invertebr. Syst. 21, 109–136

    Article  Google Scholar 

  • Klompen, H., Lekveishvili, M., Black, W.C. (2007) Phylogeny of parasitiform mites (Acari) based on rRNA. Mol. Phyl. Evol. 43, 936–951

    Article  CAS  Google Scholar 

  • Krantz, G.W., Walter, D.E. (2009) A manual of acarology, 3rd edn. Texas Tech University Press, Lubbock

    Google Scholar 

  • Le Conte, Y., Arnold, G., Desenfant, P. (1990) Influence of the brood temperature and hygrometry variations on the development of the honey bee ectoparasite Varroa jacobsoni. Environ. Entomol. 19, 1780–1785

    Google Scholar 

  • Maggi, M., Ruffinengo, S., Damiani, N., Sardella, N., Eguaras, M. (2009) A First detection of Varroa destructor resistance to coumaphos in Argentina. Exp. Appl. Acarol. 47(4), 317–320

    Article  PubMed  Google Scholar 

  • Maggi, M., Damiani, N., Ruffinengo, S., Principal, J., De Jong, D., Eguaras, M. (2010) Brood cell size of Apis mellifera modifies the reproductive behavior of Varroa destructor. Exp. Appl. Acarol. 50(3), 269–79

    Article  PubMed  Google Scholar 

  • Maggi, M., Lucia, M., Abrahamovich, A.H. (2011a) Study of the acarofauna of native bumblebee species (Bombus) from Argentina. Apidologie 42, 280–292

    Article  Google Scholar 

  • Maggi, M., Ruffinengo, S., Mendoza, Y., Ojeda, P., Ramallo, G., Floris, I., Eguaras, M. (2011b) Susceptibility of Varroa destructor (Acari: Varroidae) to synthetic acaricides in Uruguay: Varroa mites’ potential to develop acaricide resistance. Parasitol. Res. 108, 815–821

    Article  PubMed  Google Scholar 

  • Maggi, M., Medici, S., Quintana, S., Ruffinengo, S., Marcángeli, J., Gimenez Martinez, P., Fuselli, S., Eguaras, M. (2012) Genetic structure of Varroa destructor populations infesting Apis mellifera colonies in Argentina. Exp. Appl. Acarol. 56(4), 309–318

    Article  CAS  PubMed  Google Scholar 

  • McGinley, R.J. (1986) Studies of Halictinae (Apoidea: Halictidae). I: revision of New World Lasioglossum Curtis. Smithson. Contrib. Zool. 429, 1–294

    Article  Google Scholar 

  • Montgomery, D.C., Peck, E.A. (1992) Introduction to linear regression analysis. Wiley, USA

    Google Scholar 

  • O’Connor, B.M. (1988) Coevolution in astigmatid mite-bee associations. In: Needham, G.R., Page, R.P., Delfinado-Baker, R.M., Bowman, C. (eds.) Africanized honey bees and bee mites, pp. 339–346. Ellis- Horwood Ltd, Chichester

    Google Scholar 

  • O’Connor, B.M., Klompen, J.S.H. (1999) Phylogenetic perspectives on mite–insect associations: the evolution of acarinaria. In: Needam, G.R., Mitchell, R., Horn, D.J., Welcourn, W.C. (eds.) Acarology IX, vol 2. Symposia, pp. 63–71. Ohio Biology Survey, Columbus

    Google Scholar 

  • Okabe, K., Makino, S. (2002) Phoretic mite fauna on the large carpenter bee Xylocopa appendiculata circumvolans (Hymenoptera: Apidae) with descriptions of its acarinaria on both sexes. J. Acarol. Soc. Jpn. 11(2), 73–84

    Article  Google Scholar 

  • Okabe, K., Makino, S. (2008) Parasitic mites as part-time bodyguards of a host wasp. Proc. R. Soc. B 275, 2293–2297

    Article  PubMed Central  PubMed  Google Scholar 

  • Putatunda, B.N., Aggarwal, K., Kapil, R.P. (1983) Two new species of Kuzinia (Acarina: Acaridae) associated with bees (Hymenoptera) from India. Indian J. Acarol. 8(2), 57–62

    Google Scholar 

  • Rosenkranz, P., Aumeier, P., Ziegelmann, B. (2010) Biology and control of Varroa destructor. J Invertebr. Pathol. 103(1), 96–119

    Article  Google Scholar 

  • Rózsa, L., Reiczigel, J., Majoros, G. (2000) Quantifying parasites in samples of hosts. J. Parasitol. 86, 228–232

    Article  PubMed  Google Scholar 

  • Sabelis, M., Dicke, M. (1985) Long-range dispersal and searching behaviour. In: Helle, W., Sabelis, M.W. (eds.) Spider Mites, Their Biology, Natural Enemies and Control, vol. IB, pp. 141–160. Elsevier, Amsterdam

    Google Scholar 

  • Sammataro, D., Gerson, U., Needham, G. (2000) Parasitic mites of honey bees: life history, implications, and impact. Annu. Rev. Entomol. 45, 519–548

    Article  CAS  PubMed  Google Scholar 

  • Schwarz, H.H., Huck, K. (1997) Phoretic mites use flowers to transfer between foraging bumblebees. Insectes. Soc. 44, 303–310

    Article  Google Scholar 

  • Schwarz, H.H., Huck, K., Schmid-Hempel, P. (1996) Prevalence and host preferences of mesostigmatic mites (Acari: Anactinochaeta) phoretic on Swiss bumble bees (Hymenoptera: Apidae). J. Kansas. Entomol. Soc. 69(Suppl), 35–42

    Google Scholar 

  • Waiter, D.E., Beard, J.J., Walker, K.L., Sparks, K. (2002) Of mites and bees: A review of mite-bee associations in Australia and a revision of Raymentia Womersley (Acari: Mesostigmata: Laelapidae), with the description of two new species of mites from Lasioglossum (Parasphecodes) spp. (Hymenoptera: Halictidae). Aust. J. Entomol 41(2), 128–148

    Article  Google Scholar 

  • Zachvatkin, A.A. (1941) Tiroglifoidnye kleoeæi (Tyroglyphoidea). Fauna SSSR 6(1), 475

    Google Scholar 

  • Zuur, A., Ieno, E., Smith, G. (2007) Analysing ecological data. Springer, New York

    Google Scholar 

  • Zuur, A., Ieno, E., Walker, N., Saveliev, A., Smith, G. (2009) Mixed Effects Models and Extensions in Ecology with R. Springer, New York

    Book  Google Scholar 

  • Zuur, A., Ieno, E., Elphick, C. (2010) A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evolut. 1, 3–14

    Article  Google Scholar 

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Acknowledgments

The authors wish to acknowledge and thank to Pavel Klimov (University of Michigan, Department of Ecology and Evolutionary Biology), Diana Sammataro (ARS USDA), Victor H. Gonzalez (Southwestern Oklahoma State University and University of Kansas, Lawrence), and four anonymous reviewers for their critical reading and comments that improved an earlier version of the manuscript. We would like to acknowledge the curators of the following museums who provided access to host bee specimens used in this study: Colomo de Correa M.V (FIML), Sergio Roig Juñet (IADIZA), and Norma B. Diaz (MLP). We also wish to thank CONICET and UNDMP for their financial supports.

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Correspondence to Pablo Revainera.

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Manuscript editor: James Nieh

Agrégation spatiale des acariens phorétiques sur Bombus atratus et Bombus opifex (Hymenoptera: Apidae) en Argentine

Bourdon / phorésie / Acari

Räumliche Zusammenballung von phoretischen Milben auf Bombus atratus und Bombus opifex (Hymenoptera: Apidae) in Argentinien

Hummeln / phoretische Milben / Zusammenballung

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Revainera, P., Lucia, M., Abrahamovich, A.H. et al. Spatial aggregation of phoretic mites on Bombus atratus and Bombus opifex (Hymenoptera: Apidae) in Argentina. Apidologie 45, 579–589 (2014). https://doi.org/10.1007/s13592-014-0275-4

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