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Timestamp: 2019-04-25 23:02:53+00:00

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colonies. However, how brood cell width affects the number of foundress mother mites per cell and its reproduction under natural conditions has not been studied previously. The choice of a bee brood cell to begin reproduction is an important and critical moment in the life of the Varroa mite. In addition, the various reports of interaction between cell size and reproduction of the mite, in the interaction between V. destructor and it host A. mellifera; provide an excellent opportunity to study how selective pressures physical cues (in this case variability in cell width) can modify the reproductive behavior of an ectoparasite. Our objectives were to examine the natural variability in brood cell width in combs of A. mellifera and to analyze whether this factor affects the number of foundress mother mites per cell and its reproduction rate under natural conditions. The hypothesis tested was that brood cell width of A. mellifera is a key factor that affects the reproductive behavior of V. destructor under natural conditions. This hypothesis would be supported if infestation or reproduction rates vary with brood cell width.
Materials and methods The study was conducted at the Laboratorio de Apicultura, J.J. Na´gera coastal station (388100 0600 S; 578380 1000 W) and at the Laboratorio de Artro´podos (Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata in Argentina. Drone cells were limited during the sampling period because we carried out the sampling during fall and spring 2007, when cold weather induces the bee colonies to restrict the brood area, especially the drone brood. Eleven colonies of A. mellifera maintained in Langstroth-type beehives were used for the experiments. Population distribution of Varroa destructor We examined the population distribution of V. destructor within brood cells of A. mellifera. One sealed brood comb from each colony was intensively sampled. All of the brood cells of each comb were opened and the number of foundress mother mites (parasitic intensity) inside each cell was registered. Morisita’s index (Brower and Zar 1977) was estimated according to the following equation: X X X 2 X  X  X X Is ¼ N X2  where: Is = Morisita’s dispersion index N P= Number of cells of A. mellifera inspected. X = Sum of the number of V. destructor foundress mother mites found within the inspected cells. Based on the characteristics of this dispersion index, if: Is = 1, the population distribution of V. destructor was adjusted to Poisson. Is \ 1, the population distribution of V. destructor was normal. Is [ 1, the population distribution of V. destructor was distributed according to negative binomial law.
To evaluate if the value of Is was significantly different from 1, the following equation was employed:  hX  i X  F0 ¼ Is X 1 þN X =N  1 If the value of F0 was greater than the tabulated F with n - 1 grades of freedom and 95% of confidence, it was concluded that Is was significantly different from 1. Infestation rate and mite distribution were analyzed for each colony. Infestation rate was estimated following De Jong (2005). Brood cell width and its effect on the number of foundress mother mites invading cells and on its reproduction rate Six colonies of A. mellifera were used. A drone brood comb was collected from one colony, while a worker brood comb (with no drone brood) was sampled from the remaining five colonies. Photographs of each comb were taken with a Kodak Easy Share C340 camera. The inner width of each sealed brood cell (distance between two parallel walls) was measured in each photograph using Image J software. Diameter distributions of worker and drone cells were graphed in frequency histograms. All of the brood cells of each comb were opened and the number of foundress mother mites inside each cell was registered. To facilitate recording the data, a colored pin of different color was assigned to each opened cell according to the following criteria: green—zero mites; yellow—one mite; light blue—two mites; red—three or more mites. The combs were photographed again with the pins. Using Image J software the two types of photographs (combs with sealed cells and those with opened cells with pins) were superimposed in order to relate the width of each sealed cell measured with the number of foundress mother mites and its reproduction rate. Reproduction rate of V. destructor was estimated only in worker brood cells. Only worker brood cells invaded by a single mother mite were analyzed, since multiple infestations can affect mite reproduction (Fuchs and Langenbachs 1989). Whenever possible, only brood that had been sealed for longer than 230 hours (at least at the yellow thorax stage of development) was collected. Mite eggs and protonymphs were not sexed, as this cannot be done reliably using external characteristics (Steiner 1988). Protonymphs and deutonymphs were distinguished by counting the number of sternal setae, according to Nannelli (1986). Reproduction rate was calculated for foundress mother mites according to Ifantidis (1984), by dividing the total progeny of the mites by the number of mites of the parental generation. To determine whether brood cell width affected the number of V. destructor foundress mother mites in the brood, a generalized additive model (GAM) (Hastie and Tibshirani 1990; Zuur et al. 2007), which is based on Binomial and Poisson distributions, was used for both worker and drone cells. To determine whether brood cell size affected V. destructor reproduction rate, we used a Pearson’s correlation and a Tukey test to calculate the relationship between the total number of mites infesting each brood cell (original adult and offspring) and the width of the brood cell. Each foundress mother mite was classified into one of the following three categories: (1) viable mother mite (a mother mite that produced live female and male offspring); (2) inviable mother mite progeny (a mother mite that produced incomplete offspring due to dead female or male offspring or only a male produced); (3) infertile mother mite (mother mite did not reproduce). Tukey test was used to compare cell width means whenever a one-way ANOVA indicated significant differences between cell width means for the three categories of mother mites.
singly-infested worker cells had viable offspring, 26% had inviable offspring and 16% contained infertile mother mites. The rate of increase for viable mother mites was 0.96 viable female descendants. Mean cell width was significantly different among the categories of mother mite progeny (ANOVA, F = 6.343, P = 0.003); the mean widths of cells with infertile females, and viable and inviable progeny were 4.92, 5.4 and 5.38 mm, respectively.
(e.g., nutrition effect) could be the connection between the lack of mite reproduction and the size of the cell that we found. Previous researches have reported that the nutrition quality improves mite reproduction (Rodriguez et al., 1961; Steiner et al., 1995). It was reported that Varroa mite reproduction can be suppressed under stress conditions due to severe reproductive competition, which can result in egg resorption by the foundress mother mite (Steiner et al., 1995). Also, Alberti and Hanel (1986) showed that mites that had not laid eggs often had problems with prosperm maturation in the reproductive tract of the female mites. Like egg resorption, problems with prosperm maturation could be due to stress conditions. Tewarson (1983) reported that reproduction of this parasite occurs only after intake of a number of blood meals; some bee hemolymph proteins are absorbed without digestion. Steiner et al. (1995) demonstrated that oogenesis is faster in drone brood cells than in worker brood cells, probably due to greater food availability for the foundress mother mite. Based on this line of reasoning, the smaller cells could contain smaller larvae, which would provide a smaller quantity of nutritients for the initiation of mite reproduction. Harris and Harbo (1999) suggested that mites that had not laid eggs had problems with mating or a failure of the prosperm to mature in the reproductive tract of the female mites. However, they were not able to distinguish between nonmating and failure of sperm maturation. If the cell width distributions found in this study (where bigger cells are less numerous) are considered, there could be a trade-off between the time necessary to search for optimal cells and the higher reproductive success obtained in such cells: Varroa females try to find bigger cells because they do not reproduce as efficiently in the small ones (probably because of a food stress factor); although finding big brood cells would insure better conditions for parasite reproduction, the associated costs with searching for infrequent cells would not be compensated by the benefits of finding such cells, making this strategy inefficient (Optimal Foraging, Charnov 1976). This hypothesis is supported by the evidence presented by Boot et al. (1994), who found that the invasion rate increases with the number of brood cells available. Moreover, to search for bigger cells, with the higher number of foundress mother mites inside, as we report here, could result in a reduction in the reproductive success of Varroa female mites because of a negative density-dependent effect (Eguaras et al. 1994; Fuchs and Langenbach 1989). These hypotheses could be tested in future experiments. This study is the first report that cell width can restrict the reproduction of V. destructor. Moreover, we demonstrated that an aspect of the physical environment can modulate the reproductive behavior of this parasite, resulting in new hypotheses on relations between nutrition and reproductive success of the mites. Acknowledgments The authors thank the UNMDP and CONICET for financial support. This research was supported by an ANPCyT, Pict 07 grant to M. E. We thank Dr. Norma Sardella for her criticisms and suggestions and to Dr. Elena Ieno for her help in the statistical analysis.
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