Rhizoglyphus echinopus (Acari: Acaridae) associated with Atta sexdens (Insecta: Formicidae)

Rhizoglyphus echinopus (Acari: Acaridae) associado a Atta sexdens (Insecta: Formicidae)

ABSTRACT

Four deutonymphs of bulb mites (hypopus) from Rhizoglyphus echinopus (Fumouze & Robin) (Acari: Acaridae) were found attached to the head of Atta sexdens in Rio de Janeiro, Brazil. This mite species is commonly associated with ornamental plants and trees with bulbs, corms and tubers. The results of this study provided an insight into the phoretic relationship between mites and ants, indicating the role of the latter in the dispersion of the first. Despite the abundant and diverse mite fauna existing in ants, little is known about their diversity, biology, ecology and the nature of their associations.

KEYWORDS
ant; arthropods; first record; phoresy

RESUMO

Quatro deutoninfas de ácaros do bulbo (hipopus) da espécie Rhizoglyphus echinopus (Fumouze & Robin) (Acari: Acaridae) foram encontradas fixadas na cabeça de formigas da espécie Atta sexdens no Rio de Janeiro, Brasil. Essa espécie de ácaro está comumente associada a plantas ornamentais e plantas com bulbos e tubérculos. Os resultados desse estudo fornecem uma visão sobre a relação forética entre ácaros e formigas, indicando o papel destas últimas na dispersão dos primeiros. Apesar da abundância e da fauna diversa do ácaro em formigas, pouco se sabe sobre a diversidade, a biologia, a ecologia e a natureza dessa associação.

PALAVRAS-CHAVE
formiga; artrópodes; primeiro registro; forésia

Among pest insects of Brazilian agriculture and forestry, leaf-cutting ants are the main agents that cause damage since they attack all cultivated plants (SPIER et al., 2013). The species of the tribe Attini live in symbiosis with basidiomycete fungi, association that is important for the maintenance of the ants colony because it allows them to obtain nutrients and, on the other hand, enables symbiotic fungal growth with the substrates provided by the ants (SILVA et al., 2003). Among the species of the tribe Attini, Atta sexdens, popularly known as leaf cutters, collect fresh vegetation which they use to cultivate a symbiotic fungus inside their nests in order to provide food source to the brood (LUCIA et al., 2014).

Some species of the genus Atta are considered the main agricultural and forest pests in the neotropical region; there is a constant concern with their control in various agroecosystems (LUCIA et al., 2014; DORNELAS et al., 2016).

The association of mites with ants is usually common or mutualist, relying on bacteria, fungi and other resources accumulated within the ant nests. Confirmed parasitic species are rare and largely restricted to the order Mesostigmata (CAMPBELL et al., 2013). The first reference to myrmecophilous mites in Brazil is from SELLNICK (1926).

Mites have radiated into many habitats like phytophagous, mycophagous, saprophagous and parasites, and can be seen in various hosts, as well as in stored products, homes, nests and various types of soils and waste (PHILIPS; DINDAL, 1990).

Species of the family Acaridae are commonly found in humid organic substrates. Rhizoglyphus echinopus (Fumouse & Robin) (Acari: Acaridae) (Robine bulb mite) are typical phoretic mite and widely distributed throughout the world (SILVA et al., 2016). They are known to be good indicators of environmental impact (PAOLETTI et al., 1991) and can accumulate heavy metals in their bodies, making them an important tool as indicators of disturbed sites (VAN STRAALEN, 1996). This mite can cause injuries on plant tissue creating a gateway to diseases (VENEGAS, 2003; FAN; ZHANG 2004), frequently attacking bulbs, roots, tubers and protected crops (DÍAZ et al., 2000; ZHANG, 2003).

Four deutonymphs of R. echinopus (Acari, Astigmata: Acaridae) were taken by the first author of this article from the head of A. sexdens (Linnaeus, 1758) (Insecta, Formicidae) in Cascadura, Rio de Janeiro (22.88.2’62.7”S, 43.33.8’59”W).

One hundred A. sexdens were collected from fresh leaves of the plants Vernonia condensata Baker (Asteraceae) during October of 2018 in the botanical garden of the Laboratório de Zoologia da Fundação Técnico Educacional Souza Marques (FTESM), located in Cascadura, Rio de Janeiro, Brazil. The ants were properly identified by dichotomic keys from MAYHÉ-NUNES (1991) and GONÇALVES (1961) and checked out for the presence of phoretic mites.

The bulb mites removed from A. sexdens were mounted between slide and coverslip in Hoyer’s medium (FLECHTMANN, 1973) and examined under optical light microscopy. Specimens were properly identified following FLECHTMANN (1975), KRANTZ; WALTER (2009) and FAN; ZHANG (2004) and were deposited with the voucher specimen registration (CAVAISC – ACA-4134) at the Coleção de Artrópodes Vetores Ápteros de Importância em Saúde das Comunidades (CAVAISC) of the Laboratório de Referência Nacional em Vetores das Riquetsioses (LIRN), Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ) (Fig. 1).

Figure 1
Ventral view of Rhizoglyphus echinopus (Deutonymph) (50×).

Leaf-cutting ants are a keystone species because of their influence on environmental diversity, productivity, nutrients and energy flow. This species of ants directly and indirectly changes the physical state of biotic and abiotic materials and may cause economic losses (LUCIA et al., 2014).

The correct identification of pathogens that cause damage to species of agricultural importance is fundamental for the development of biological control strategies (JOHANSSON et al., 2013). Rhizoglyphus echinopus deutonymphs have been observed associated with many arthropods, such as ants (BERGHOFF et al., 2009; RETTENMEYER et al., 2011; CAMPBELL et al., 2013), beetles (NORTON, 1973; ROGERS, 1974; DE; PANDE, 1988; POPRAWSKI; YULE 1992; MARAKOVA, 1995), Diptera (GARMAN, 1937; ZAKHVATKIN, 1941) and Siphonaptera (FAIN; BEAUCOURNU, 1993) as well as in some Blattodea Subterranean termite (SILVA et al., 2016). This study is the first record of the association between the bulb mite R. echinopus and Atta sexdens in Brazil.

Mites are the most abundant organisms found in ants nests (CAMPBELL et al., 2013). Four deutonymphs of R. echinopus associated with A. sexdens were found attached to their heads and, according to SILVA et al. (2016), the presence of mites in the head, mouthparts and abdomen of insects make difficult normal feeding behavior. The abundance of mites can also harm the sexual behavior of the phoront (RODRIGUES et al., 2013).

Despite the vast number of mite species that have been described from the association with insects, the study of social insect-mite interactions is still insipient. The mite species that occur in nests of most tropical ants remain totally unknown.

ACKNOWLEDGEMENTS

We are very thankful to The Mycological Collection Trichocomaceae (FIOCRUZ – IOC), which facilitated the use of microscopical image capture and Paulo Vander Ferreira Santana for his help with the English’s revision.

• FUNDING

  This work did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

• ETHICAL APPROVAL

  Not applicable

• AVAILABILITY OF DATA AND MATERIAL:

  Specimens of Rhizoglyphus echinopus were deposited with the voucherspecimen registration (CAVAISC – ACA-4134) at the Coleção de Artrópodes Vetores Ápteros de Importância em Saúde das Comunidades (CAVAISC) of the Laboratório de Referência Nacional em Vetores das Riquetsioses (LIRN), Instituto Oswaldo Cruz, Fundação Oswaldo Cruz (IOC/FIOCRUZ)

REFERENCES

• BERGHOFF, S.M.; WURST, E.; EBERMANN, E.; SENDOVA-FRANKS, A.B.; RETTENMEYER, C.W.; FRANKS, N.R. Symbionts of societies that fission: mites as guests or parasites of army ants. Ecological Entomology, Oxford, v.34, n.6, p.684-695, 2009. https://doi.org/10.1111/j.1365-2311.2009.01125.x
  » https://doi.org/10.1111/j.1365-2311.2009.01125.x
• CAMPBELL, K.U.; KLOMPEN, H.; CRIST, T.O. The diversity and host specificity of mites associated with ants: the roles of ecological and life history traits of ant hosts. Insectes Sociaux, Ontario, v.60, n.1, p.31-41, 2013. https://doi.org/10.1007/s00040-012-0262-6
  » https://doi.org/10.1007/s00040-012-0262-6
• DE, K.; PANDE, Y.D. Bionomics and some behavioral aspects of the mango stone weevil, Sternochetus gravis (Fabricius) (Coleoptera: Curculionidae). Entomon, Thiruvananthapuram, v.13, n.1, p.17-24, 1988. Available from: https://www.cabdirect.org/cabdirect/abstract/19881114365 Access on: 7 Aug. 2019.
  » https://www.cabdirect.org/cabdirect/abstract/19881114365
• LUCIA, T.M.C.D.; GANDRA, L.C.; GUEDES, R.N.C. Managing leaf-cutting ants: peculiarities, trends and challenges. Pest Management Science, London, v.70, n.1, p.14-23, 2014. https://doi.org/10.1002/ps.3660
  » https://doi.org/10.1002/ps.3660
• DÍAZ, A.; OKABE, K.; ECKENRODE, C.J.; VILLANI, M.G.; OCONNOR, B.M. Biology, ecology, and management of the bulb mites of the genus Rhizoglyphus (Acari: Acaridae). Experimental & Applied Acarology, Amsterdam, v.24, n.2, p.85-113, 2000. https://doi.org/10.1023/A:1006304300657
  » https://doi.org/10.1023/A:1006304300657
• DORNELAS, A.S.P.; SARMENTO, R.A.; SANTOS, G.R.; NASCIMENTO, M.O.; SOUZA, D.J. Fungos filamentosos associados às espécies Atta sexdens (Linnaeus) e Atta laevigata (F. Smith) (Hymenoptera: Formicidae). EntomoBrasilis, Vassouras, v.9, n.1, p.26-30, 2016. https://doi.org/10.12741/ebrasilis.v9i1.528
  » https://doi.org/10.12741/ebrasilis.v9i1.528
• VENEGAS, E.G.E. El género Rhizoglyphus su importancia agrícola y como ácaro del suelo In: Nápoles, J.R.; Venegas E.G.E.; Martínez, A.E. (ed). Entomología Mexicana México: Sociedad Mexicana de Entomología, 2003. p.102-107.
• FAIN, A.; BEAUCOURNU, J.-C. Les hypopes des Astigmates (Acari) phorétiques sur les Puces (Siphonaptera) des Mammifères et D’oiseaux. Bulletin de L’ Institut Royal des Sciences Naturalles de Belgique Entomologie, v.63, p.77-93, 1993. Available from: http://biblio.naturalsciences.be/rbins-publications/bulletins-de-linstitut-royal-des-sciences-naturelles-de-belgique-entomologie/63-1993/entomologie-63-1993_77-93.pdf Access on: 1 Aug. 2019.
  » http://biblio.naturalsciences.be/rbins-publications/bulletins-de-linstitut-royal-des-sciences-naturelles-de-belgique-entomologie/63-1993/entomologie-63-1993_77-93.pdf
• FAN, Q.-H.; ZHANG, Z.-Q. Revision of Rhizoglyphus Claparède (Acari: Acaridae) of Australasia and Oceania London: Systematic & Applied Acarology Society, 2004. 374p.
• FLECHTMANN, C.H.W. Lorryia formosa Cooremann, 1958: Um ácaro dos citros pouco conhecido no Brasil. Ciência e Cultura, São Paulo, v.25, n.12, p. 1179-1181, 1973.
• FLECHTMANN, C.H.W. Elementos de acarologia São Paulo: NOBEL, 1975. 344p.
• GARMAN, P. A study of the bulb mite (Rhizoglyphus hyacinthi Banks). In: Bulletin Connecticut Agricultural Experiment Station New Haven: Connecticut Agricultural Experiment Station, 1937. p.889-907. https://doi.org/10.5962/bhl.title.50948
  » https://doi.org/10.5962/bhl.title.50948
• GONÇALVES, C.R. O gênero Acromyrmex no Brasil (Hym: Formicidae). Studia Entomologica, Petrópolis, v.4, n.1-4, p.113-180, 1961.
• JOHANSSON, H.; DHAYGUDE, K.; LINDSTRÖM, S.; HELANTERÄ, H.; SUNDSTRÖM, L.; TRONTTI, K. A Metatranscriptomic Approach to the identification of microbiota associated with the ant Formica exsecta. PloS ONE, San Francisco, v.8, n.11, p.e79777, 2013. https://doi.org/10.1371/journal.pone.0079777
  » https://doi.org/10.1371/journal.pone.0079777
• KRANTZ, G.W.; WALTER, D.E. A manual of acarology: Third Edition. Lubbock: Texas Tech University Press, 2009. 807p.
• MARAKOVA, O.L. Mesostigmatid mites (Parasitiformes, Mesostigmata) on the forest dung beetle Geotrupes stercorosus Zoologichesky Zhurnal, Moscow, v.74, n.12, p.16-23, 1995.
• MAYHÉ-NUNES, A.J. Estudo de Acromyrmex (Hymenoptera: Formicidae) com ocorrência constatada no Brasil: subsídios para uma análise fiogenética 1991. 122f. Dissertation (Masters in Entomology) – Universidade Federal de Viçosa, Viçosa, 1991.
• NORTON, R.A. Phoretic mites associated with the hermit flower beetle, Osmoderma eremicola Knoch (Coleoptera: Scarabaeidae). The American Midland Naturalist, South Bend, v.90, n.2, p.447-449, 1973. https://doi.org/10.2307/2424466
  » https://doi.org/10.2307/2424466
• PAOLETTI, G.M.; FAVRETTO, M.R.; STINNER, B.R.; PURRINGTON, F.F.; BATER, J.E. Invertebrates as bioindicators of soil use. Agriculture, Ecosystems & Environment, Nanning, v.34, n.1-4, p.341-362, 1991. https://doi.org/10.1016/0167-8809(91)90120-M
  » https://doi.org/10.1016/0167-8809(91)90120-M
• PHILIPS, J.R.; DINDAL, D.L. Invertebrate populations in the nests of a screech owl (Otus asio) and an American Kestrel (Falco sparverius) in central New York. Entomological News, Worcester, v.101, n.3, p.170-192, 1990. Available from: https://www.cabdirect.org/cabdirect/abstract/19920503122 Access on: 7 Aug. 2019.
  » https://www.cabdirect.org/cabdirect/abstract/19920503122
• POPRAWSKI, T.J.; YULE, W.N. Acari associated with Phyllophaga anxia Leconte (Coleoptera:Scarabaeidae) in southern Quebec and eastern Ontario. The Canadian Entomologist, Kentville, v.124, n.2, p.397-403, 1992. https://doi.org/10.4039/Ent124397-2
  » https://doi.org/10.4039/Ent124397-2
• RETTENMEYER, C.W.; RETTENMEYER, M.E.; JOSEPH, J.; BERGHOFF, S.M. The largest animal association centered on one species: the army ant Eciton burchelii and its more than 300 associates. Insectes Sociaux, Ontario, v.58, n.3, p.281-292, 2011. https://doi.org/10.1007/s00040-010-0128-8
  » https://doi.org/10.1007/s00040-010-0128-8
• RODRIGUES, M.E., CARRIÇO, C.; PINTO, Z.T.; MENDONÇA, P.M.; QUEIROZ, M.M.C. First record of acari Arrenurus Dugès, 1834 as a parasite of Odonata species in Brazil. Biota Neotropica, Campinas, v.13, n.4, p.365-367, 2013. https://doi.org/10.1590/S1676-06032013000400029
  » https://doi.org/10.1590/S1676-06032013000400029
• ROGERS, C.E. Bionomics of the carrot beetle in Texas rolling plains. Environmental Entomology, Hamden, v.3, n.6, p.969-974, 1974. https://doi.org/10.1093/ee/3.6.969
  » https://doi.org/10.1093/ee/3.6.969
• SELLNICK, M. Alguns novos ácaros (Uropodidae) mirmecófilos e termitófilos. Arquivos do Museu Nacional do Rio de Janeiro, Rio de Janeiro, v.26, p.29-56, 1926.
• SILVA, A.; BACCI JUNIOR, M.; SIQUEIRA, C.G.; BUENO, O.C.; PAGNOCCA, F.C.; HEBLING, M.J.A. Survival of Atta sexdens workers on different food sources. Journal of Insect Physiology, Portici, v.49, n.4, p.307-313, 2003. https://doi.org/10.1016/S0022-1910(03)00004-0
  » https://doi.org/10.1016/S0022-1910(03)00004-0
• SILVA, A.F.; PINTO, Z.T.; CAETANO, R.L.; CARRIÇO, C.; SATO, T.P.; AMORIM, M.; GAZETA, G.S. Bulb Mites Rhizoglyphus echinopus (Fumouze and Robin) Associated with Subterranean Termite (Isoptera) in Brazil. EntomoBrasilis, Vassouras, v.9, n.1, p.65-68, 2016. https://doi.org/10.12741/ebrasilis.v9i1.553
  » https://doi.org/10.12741/ebrasilis.v9i1.553
• SPIER, M.S.; SPIER, E.F.; DALAVÉQUIA, M.A.; FAVRETTO, M.A. Aspectos ecológicos de Atta sexdens piriventris Santschi (1919) (Hymenoptera: Formicidae) no município de Capinzal, Santa Catarina, Brasil. EntomoBrasilis, Vassouras, v.6, n.1, p.94-96, 2013. https://doi.org/10.12741/ebrasilis.v6i1.248
  » https://doi.org/10.12741/ebrasilis.v6i1.248
• VAN STRAALEN, N.M. Critical body concentrations their use in bioindication. In: Bioindicator systems for soil pollution Kluwer Academic Publishers, 1996. 103p.
• ZAKHVATKIN, A.A. Fauna of U.S.S.R. Arachnoidea 1(1) Tyroglyphoidea (Acari). Institute of Zoology. Academy Science, Moscow, v.28, p.1-475, 1941.
• ZHANG, Z.Q. Mites of greenhouses: identification, biology and control Wallingford: CABI Publishing, 2003. 244p. https://doi.org/10.1079/9780851995908.0000
  » https://doi.org/10.1079/9780851995908.0000

Publication Dates

• Publication in this collection
  04 Dec 2020
• Date of issue
  2020

History

• Received
  18 Sept 2019
• Accepted
  01 Oct 2020