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First report in Brazil of Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) in colonies of Africanized honey bees (Apis mellifera L.)/Primer reporte en Brasil de Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) en colonias of abejas meliferas africanizadas (Apis mellifera L.)/Primeiro relato no Brasil de Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) em colonias de abelhas africanizadas (Apis mellifera L.).


The first report of mites in ancient honeycombs was given by Aristotle in 350 B.C., when for the first time was used the name 'akari', a term officially established in 1778 for mites by DeGeer (Moraes and Flechtmann, 2008). Several mites associated with honeybees have been identified (De Jong et al., 1982); their relationship to the bees varies from commensalism to endoparasitism and ectoparasitism (Flechtmann, 1980). A cosmopolitan species, Tyrophagus putrescentiae (Schrank) (Acari: Acaridae), has been reported previously as attached to the body of bumblebees (Maggi et al., 2011), and in Guatemala the mite was reported after being detected in samples of dead honeybees stored in alcohol solution (Baker and Delfinado-Baker, 1983). Species of the genus Tyrophagus have also been reported parasitizing in the laboratory other groups of insects in various stages of development, such as beetles (Brust and House, 1988; Kumar, 1997; Papadopoulou, 2006; Canevari et al., 2012) and flies (Serpa et al., 2004), in addition to being present in cereals and stored food products (Kheradmand et al. 2007). From the medical and veterinary standpoint, if ingested, the mite can cause poisoning in humans and animals (Blanco et al., 1997; Matsumoto et al., 2001; Sanchez-Borges et al., 2005; Liao et al., 2009; Canfield and Wrenn, 2010), such as acute enteritis, and may be related to the transmission of bacteria, yeasts and pathogenic fungi through food (Serpa et al., 2004). This work represents the first report of the presence of the mite Tyrophagus putrescentiae (Schrank) (Acari: Acaridae) in hive combs of Africanized honey bees in Brazil.

Brazilian honey bees reflect decades of introgression between the European honey bee subspecies Apis mellifera mellifera and Apis mellifera ligustica, imported during the 17th century, and the African subspecies Apis mellifera scutellata, introduced in 1956 (Vandame et al., 2002). Now widely distributed in the American continents, these 'Africanized' honey bees (AHBs) represent the predominant type of honey bee in tropical and subtropical regions of South and Central America, and in some regions of North America (Rosenkranz et al., 2000). AHBs were highly successful in Brazil, spreading to all parts of the country by the late 1970s (Teixeira et al., 2008).

Because of the mortality records in colonies of AHBs (A. mellifera) in Rio Negrinho, Santa Catarina State, Brazil (26[degrees]24'56"S, 49[degrees]34'3"W), samples of combs from rational colonies (standard Langstroth beehives) were collected by veterinarians of the official veterinary defense service of the State, on September 6, 2011 and sent to the Honey Bee Health Research Laboratory/APTA, Department of Agriculture and Food Supply, Sao Paulo, Brazil, in order to investigate the possible causes involved. There were no dead adult bees inside or near the hives during the sampling time.

Using a Carl Zeiss Jena stereo microscope, we found mite populations in three samples from different colonies. Samples of the mites were kept in microtubes containing 70% alcohol, for subsequent identification. The mites were studied at the Acarology Laboratory of the Biological Institute, in the same Institution (APTA) and the species T. putrescentiae (Schrank, 1781) was identified based on Zhang and Fan (2005).

Mites were found in three colonies of Africanized honey bees (A. mellifera), among the 20 hives that made up the apiary. In the colonies where the infestation was noticeable, there was a small population of adult bees with abundant food and offspring. The other colonies were also sparsely populated, although without the apparent presence of mites. Thousands of mites (T. putrescentiae) (Schrank, 1781) were found in their different development stages covering basically all the brood area in the three samples (Figures 1 and 2). Mites were found on the larvae, pupae, bee bread (fermented pollen mixture stored in the honeybee combs) and in the empty cells. Besides the mites (T. putrescentiae), hyphae of unidentified fungus were also observed abundantly on the combs, along with the young larvae and pupae of A. mellifera. The ectoparasitic mite Varroa destructor (Acari: Varroidae) was also found parasitizing adult bees (4.1%) and brood cells (4%) in the same combs.

This is the first record of T. putrescentiae in colonies of Africanized honey bees (A. mellifera) in an apiary in Brazil. It is possible that due to the great diversity of environments it inhabits, the mite was introduced into the infested colonies by foraging bees, similar to the report by Schwarz and Huck (1997). Baker and Baker-Delfinado (1983) studied populations of phoretic organisms on A. mellifera in Guatemala and identified T. putrescentiae in the samples of bees which had been placed in alcohol, suggesting that the mite is phoretic.

The finding of abundant hyphae covering the combs of the analyzed samples of AHBs, supports previous findings that the mite is fungivorous (Parkinson et al., 1991; Hubert et al., 2003; Zhang and Fan, 2005). Tyrophagus species prefer environments already infested by fungi. Indoor bee colonies under certain circumstances, such as when the humidity is high, there is protein food stored as pollen and the colonies are sparsely populated, become conducive to the development of fungi and provide a food source and favorable environment for the development of mite populations (Hughes, 1961; Duek et al., 2001). It should be noted that the peak losses of colonies (>50%) in the studied location occurred in winter (season with low temperatures and rainfall and abundant pollen and nectar from flowering plants), with a considerable amount of condensation of water inside the hives. While the grooming behavior of the bees is an important factor in the population dynamics of the mite Varroa destructor in Africanized honey bees, it may not be as effective against individuals of T. putrescentiae, due to their small size (~0.4mm in adulthood), in addition to the fact that the affected colonies were weakened, which may have had a detrimental effect of their grooming behavior, and thereof provided more favorable conditions for the development of the mite population. Although in some studies an interspecific relationship and harmonic phoresy between mites and bees has been observed (Eickwort, 1997), it is not possible to determine whether the relationship of T. putrescentiae and the bees is parasitic or phoretic. It is likely that the mites are introduced into the honey bee colonies by worker bees foraging for pollen and nectar in the environment, or even by mere contact with the moist soil in search of water (OConnor and Klimov, 2003). The sparsely populated colony and high humidity conditions are conducive to the proliferation of fungi and protein food stock, which provides food and a favorable environment for the mite populations to develop.

This is the first report of the presence of the mite Tyrophagus putrescentiae in Africanized honey bee hives. Detailed studies that evaluate the relationship of these bees with these mites should be conducted, not only for the health of the bee colonies, but also for the possible damage caused to human health through the consumption of contaminated bee products. The role of Tyrophagus putrescentiae or other species on bee products needs further studies and evaluation, as these mites have been associated with human allergies and digestive problems (VanDer Heid et al, 1998), can affect people indirectly as a potential vehicle of dissemination of pathogen, parasites, decomposers (Gorham, 1979) or can be potential vectors for prion infections (Lupi, 2003, 2006).

Received: 09/03/2013. Modified: 09/22/2014. Accepted: 09/23/2014.

Erica Weinstein Texeira. Doctor of Science. Researcher. Researcher, Address: Departamento de Descentralizacao do Desenvolvi-mento (DDD), Agencia Paulista de Tecnologia dos Agronegocios (APTA). Secretaria de Agricultura e Abastecimento do Estado de Sao Paulo (SAA-SP). Caixa Postal 07. 12400-970. Pinda monhangaba, SP, Brazil. email:

Lubiane Guimaraes dos Santos. Doctoral student in Entomology, Universidade Federal de Vicosa, Brazil.

Andre Luiz Matioli. Doctor of Science. Researcher, Instituto Biologico, APTA, SAA. Campinas, Brazil.

Dejair Message. Doctor of Science, Universidade Federal Rural do Semiarido, Brazil.

Maria Luisa Teles Marques Florencio Alves. Master of Science. Researcher, DDD, APTA, SAA Pindamonhangaba, SP. Brazil


The authors thank the Companhia Integrada de Desenvolvimento Agricola de Santa Catarina (CIDASC) for the samples and Fabio A. Pinto for laboratory assistance. This work was supported by National Council for Scientific and Technological Development (CNPq), Ministry of Science and Technology, Brazil (CNPq/ MAPA/SDA N[degrees] 064/2008 to E.W.T.).


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Title Annotation:texto en ingles
Author:Teixeira, Erica Weinstein; dos Santos, Lubiane Guimaraes; Matioli, Andre Luiz; Message, Dejair; Alve
Date:Oct 1, 2014
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