apiculture in brazil is based on the well adapted and productive africanized honeybee ( silva and freitas , 2004 ) . the world leaders in honey production are china , usa , argentina and mexico ( blke and palmeira , 2006 ) . brazil , according to same authors , is the eleventh largest honey producer and the fifth exporter in worldwide , but has potential to increase both production and productivity . according to aizen and harder ( 2009 ) , the global population of managed honeybee hives has increased 45% during the last 50 years , but no data are available on feral populations . these authors state that increasing demands for agricultural pollination services are driving the increase in honeybee populations , but there has been a much more rapid ( > 300% ) increase in the fraction of agriculture that depends on animal pollination in the same period , stressing a need for global pollination capacity . this implies a need to increase honeybee numbers , survival and productivity , and this can be achieved through applying animal breeding theory to managed populations . however , information on environmental and genetic factors that affect economic traits in the different genotypes of honeybees across the country is limited . the africanized honeybee is considered more resistant to diseases and more tolerant to varroa destructor than the european honeybees , breeding for improvement in productive and resistance / tolerance traits should have significant economic impact on this activity ( bchler et al . , 2010 ) . honey production , production of propolis , foraging behavior , hygienic behavior and lower percentages of mites on adult bees ( or grooming behavior ) should be included in genetic evaluations and selection programs in order to choose the best queens to increase honey or propolis production and productivity ( milne jr , 1985 ; bienefeld and pirchner , 1990 ; thimann and manrique , 2002 ; stanimirovic et al . , 2010 ; wilson - rich et al . , 2010 ) . however , before selection can be carried out , it is necessary to estimate the heritabilities and the genetic correlations between productive and resistance / tolerance traits to predict the response to selection for a given trait . there are few reports on parameter estimates in africanized honeybees in brazil ( faquinello et al . , 2011 ; costa - maia et al . , 2011 . therefore , the objective of this study was to estimate the heritabilities and genetic correlations for honey production , propolis production , syrup - collection rate , hygienic behavior and percentage of mites on adult bees in a population of africanized honeybees in southern brazil . the study was conducted from april 2009 to october 2010 at the agronomic experimental station of the federal university of rio grande do sul ( eea / ufrgs ) , in eldorado do sul , rio grande do sul , brazil . africanized honey bee queens used in this study were donated by a local beekeepers association . a total of 110 queens were evaluated over three generations ( 40 , 40 and 30 queens per generation ) . the queens were raised from each of the first 40 colonies for the second generation , and from each of the second generation colonies for the third one . missing records in the third generation were due to problems in an incubator for queen rearing and loss of some colonies over winter because of falling trees in an apiary . the new queens were marked with enamel paint and introduced into the colonies two days after the laying queen had been removed . the first measurement was carried out at least 65 days after the new queens started to lay eggs . honey production was measured twice , in may 2009 and march 2010 . to measure honey production , syrup - collection rate , used as a proxy for estimating hoarding behavior , was measured in july / august 2009 , february and august 2010 , totalling three measurements . all the hives had the same numbers of empty combs , but syrup storage was not measured , because the objective was to determine the rate of consumption . glass recipients ( 600 ml ) covered by metal lids with eight holes ( 1.5 mm width ) were used . each recipient was completely filled with water : sugar : honey syrup in a 4:4:2 proportion . two ( july / august ) to three ( on february ) recipients were introduced into the hive in the afternoon . measurements of propolis production were carried out in july and august 2009 ( winter ) , april and may 2010 ( autumn ) and september / october 2010 ( spring ) . production was measured using propolis collectors on two sides of the hive ( 22 cm  3 cm ) . the collectors remained in the hives for 25 days before the propolis was cut and weighed . measurement of hygienic behaviour was realized by the needle test ( olszewski and paleolog , 2007 ) . on a comb containing pupae in the initial phase of eye pigmentation or light pink colour ( 10 to 14 days age ) 100 cells were pricked simultaneously with a  brush  containing 100 needles . in cases of irregulary constructed combs , the cells were pricked individually with a single needle . a similar nearby area ( not pricked ) of the comb was used to correct for natural cleaning of parasitized or sick pupae . the comb was photographed before the test and 24 hours thereafter to count the number of perforated cells and ( un)cleaned combs . to guarantee the quality of images , the same comb was photographed in the field four times to evidence the difference between eventual loads of pollen and perforated pupae that were not cleaned by the bees . thus hygienic behaviour was evaluated as : 
 hb={[ec1ec2oc]100}{cba100},where a is the number of cells with operculated pupae ( witness area ; not pricked ) ; b is the number of empty cells of the witness area before the needle test ; c is the number of empty cells of witness area after the needle test ; ec1 is the number of empty cells in the test area 24 h after the needle test ; ec2 is the number of empty cells in test area before the needle test ; oc is the number of operculated cells ( with pupae ) in the test area before the needle test . the measurement of percentage of mites on adult bees was adapted from de jong et al . ( 1982 ) . a solution of a neutral commercial detergent in water was prepared ( 0.5 ml / l ) . recipients ( 250 ml ) were filled with 100 ml of this solution and taken to the field . samples of adult honeybees from the brood area of the combs were picked at the same time as the hygienic behaviour test . the samples were shaken for 1 min in a glass recipient ( 600 ml ) and sieved to separate mites and honeybees . the quantity of honeybees in a hive may influence the performance of the colony ( topal et al . , 2008 ) and is referenced in literature as colony strength ( nasr et al . , 1990 ) . the strengh of the colony was measured by counting the number of frames covered with adult bees . this measurement was taken for all traits to be used as covariate in the statistic models . data were analyzed to verify normality using the univariate procedure of the sas program ( sas institute inc , cary , north carolina ) . phenotypic records were transformed ( square root for honey production , cubic root for propolis production and syrup collection rate , and logarithm of percentage of mite + 1 ) . the glm procedure was used to check the influence of non - genetic effects on traits , and which ones were to be considered in the models to estimate genetic parameters . the description of the data set used in the study is shown in table 1 . the sire - maternal grandsire model ( mgs ) models included non - genetic effects of location of the hive , season - year , and number of frames covered with bees for honey production , syrup collection rate , and percentage of mites on adult bees . for propolis production and hygienic behaviour the localization of the hive and the number of frames covered with bees were considered . the matricial model used to estimate genetic parameters in a single - trait analysis was : 
 y = x+za+,where y is the vector of observations ;  is the vector of non - genetic effects ; a is the vector of animal effects ;  is the vector of residual effects ; x is the design matrix of order n  p , which relates records to non - genetic effects ; z is the design matrix of the order n  q , which relates records to animal effects . the matricial model used to estimate genetic parameters in multi - trait analysis was : 
 [ y1y2]=[x100x2][b1b2]+[z100z2][u1u2]+[e1e2],where yi is the vector of observations to the i - th trait ; b is the vector of non - genetic effects to the i - th trait ; ui is the vector of animal effects to the i - th trait ; ei is the vector of residual effect of the i - th trait ; xi and zi are incidence matrices that relate the observations of the i - th trait to environmental and animal effects . it was assumed that : 
 var  [ a1a2e1e2]=[g11ag12a00g21ag22a0000r11r1200r21r22],where g11 is the additive genetic variance to direct effects of the trait 1 ; g12 = g21 are the additive genetic covariance between traits ; g22 is the additive genetic variance to direct effects of the trait 2 ; rij are the elements of r , the ( co)variance matrix to residual effects . components of variance and genetic parameters were estimated using bayesian inference by mtgsam software ( multiple trait gibbs sampling in animal models ) developed by van tassell and van vleck ( 1995 ) . the initial values for the components of variance were obtained using reml analysis and values published in the literature ( rothenbuhler et al . , 1979 ; bienefeld and pirchner , 1990 ; stanimirovic et al . , 2008 ) . in the mtgsam analyses , the initial distribution was assumed as symmetric and the definition parameter of the initial distribution was assumed as 4 ( single - trait analysis ) and 5 ( multi - trait analysis ) . the models were analyzed , first by generating two  pilot - samples  , which were monitored by the raftery and lewis ( 1992 ) diagnostic test to verify convergence . the test , implemented in the boa software package ( bayesian output analysis ) generated indications of burn - in , number of iterations and thinning interval . these indications were used to generate 20,000,000 ( single - trait ) and 100,000,000 ( multi - trait ) total iterations , a burn - in of 3,000,000 ( single and multi - trait analysis ) and thinning interval of 1,000 ( single - trait ) and 2,000 ( multi - trait ) iterations , which resulted in 48,500 ( single - trait ) and 17,000 ( multi - trait ) final samples . convergence of samples was monitored using values of serial correlation by graphical analysis and diagnostic tests of raftery and lewis ( 1992 ) , geweke ( 1992 ) and heidelberger and welch ( 1983 ) , and values of markov chain error , calculated by the package boa ( bayesian output analysis ) ( smith , 2005 ) , implemented in r software ( r development core team , 2010 ) . the highest probability density interval for estimation of components of variance and genetic parameters was tested . the local effect ( table 2 ) influenced syrup collection rate , propolis production and hygienic behavior ( p < 0.05 ) . the season - year effect was significant ( p < 0.001 ) only for syrup - collection rate . the number of frames with adult bees , fitted as a covariate , was significant ( p < 0.05 ) for honey production , syrup collection rate and propolis production . the effects in the model explained 24% , 32% , 41% , 66% and 74% of the total variation for honey production ( hp ) , percentage of mites on adult bees ( pmab ) , hygienic behavior ( hb ) , propolis production ( pp ) and syrup collection rate ( scr ) , respectively . heritability estimates ( table 3 ) were 0.16 for hp , 0.23 for scr , 0.66 for pp , 0.52 for hb and 0.13 for pmab on non - transformed data , and 0.17 for hp , 0.29 for scr , 0.67 for pp and 0.14 for pmab for transformed data ( table 4 ) . the transformation of data did not influence the results for the mean heritability and highest probability density intervals ( hpdi ) . thus , non - transformed data were used to estimate heritability and genetic correlations . in general these results may be due to the low number of queens evaluated and/or to the natural mating scheme used . the means of the posterior distributions of the genetic correlations ( table 5 ) were negative between hp / scr , hb and pmab . on the other hand the genetic correlations between hp , scr and pp , and between pp with hb and pmab were positive . the genetic correlations between pp and scr and between hb and pmab were more precisely estimated , showing the smallest intervals in hpdi . the same precision was observed in residual correlations between hb and scr , between hb and pp and between pp and pmab . as there is little information on environmental and genetic parameters for africanized honeybees in the literature we compared our results with studies on european honeybees , although these used different methods and number of queens or records . bienefeld and pirchner ( 1990 ) evaluated 5581 records of european bees , using the reml method . in brazil , costa - maia et al . ( 2011 ) used bayesian inference to evaluate 40 and 193 africanized honeybees , respectively . the location of the hive influenced pp , hb and scr and the season - year was an important effect for scr . these effects are related to the distance between the hive and the source of pollen or nectar ( sande et al . , 2009 ) , as well as although the location was not significant for all traits in this study , it was used in all models , because analyses including this effect showed higher precision in the estimates of heritability and hpdi . year - season was included in models for hp and pmab . the number of frames covered with bees influenced pp , hp and scr , which are traits related to production . 2008 ) reported that the number of frames with bees had a significant positive relationship with honey yield . the heritability ( 0.16 ) for hp was lower than the value reported by bar - cohen et al . ( 1978 ) for italian bees ( 0.54 ) , but higher than the low value found by praagh et al . while these parameters were obtained by regression methods , bienefeld and pirchner ( 1990 ) used the restricted maximum likelihood method ( reml ) for apis mellifera carnica and found 0.15 and 0.26 for effects of queen and worker bees , respectively . these differences among parameter estimates may be due to different strains or races of honeybees , different methods of estimation and/or environmental effects considered in the models . honey production is one of many economically valuable traits , being greatly influenced by environmental factors such as a regular supply of pollen and nectar over the season , a hive fully populated with worker bees , the weather , and the quality of care that honeybees receive from beekeepers ( holmes , 2000 ) . the low heritability found in this study may be explained by the residual variance , which was five times higher than the genetic variance ( table 3 ) . the heritability estimate ( 0.23 ) for scr was lower than that reported for rapid ( 0.55 ) and slow ( 0.32 ) lines selected for syrup collection under laboratory conditions by rothenbuhler et al . ( 1979 ) and higher than the heritability ( 0.187  0.029 ) found by milne jr ( 1985 ) for the removal of sugar syrup from vials and the storage in combs by caged honey bees . despite the methodological difference between the field test in the present study and field tests using flight cages or laboratory tests ( olszewski and paleolog , 2005 ) , the result ( heritability ) appears to be quite similar , this indicating that it is possible to obtain genetic progress using this kind of hoarding behavior measure as a selection criterion . some studies have shown that selection for improving propolis production in africanized bees is feasible ( manrique and soares , 2002 ; thimann and manrique , 2002 ) . however , numerous studies have focused mainly on the chemical components of propolis that could be used to treat human diseases ( simone - fingstron and spivak , 2010 ) , and others on the importance of propolis to bee health ( simone et al . , the heritability ( 0.66 ) estimated for pp is high and should permit genetic improvement through selection . the heritability estimate ( 0.52 ) for hb was lower than the value ( 0.63 ) found for carnolian honeybees by stanimirovic et al . costa - maia et al . ( 2011 ) , using bayesian inference , estimated a lower heritability value ( 0.28 ) for africanized bees in brazil . hygienic behavior is widely studied and documented in the literature ( wilson - rich et al . , 2009 ) . there are several breeding programs and/or institutions involved in the selection for more hygienic queens / worker bees to obtain more healthy and productive colonies ( stanimirovic et al . , 2008 ; the low heritability estimated for pmab ( 0.13 ) is explained by the low genetic variance , which was 6.7 times lower than the residual variance . despite the slow genetic progress that may be achieved , the selection of honeybees with low levels of mites or with tolerance to varroa destructor is economically very important ( spivak and reuter , 1998 ; martin and medina , 2004 ; rinderer et al . , while this mite has killed millions of colonies of european honeybees in europe and north america , the africanized bee has a certain tolerance to this mite ( martin and medina , 2004 ) . the genetic correlations between hp , scr and pp ( 0.48 , 0.58 , and 0.67 ) were positive and favorable , which suggests that the selection for scr or pp will increase hp . certain studies in the literature have shown a positive phenotypic correlation between the amounts of syrup gathered or collected by bees ( hoarding behavior ) in the laboratory / field and the honey production in the hives ( olszewski and paleolog , 2005 ; zrate et al . , 2008 ) . another study also found a positive correlation ( pearson ) between pp and hp in africanized honeybees , with r = 0.422 ( p = 0.00001256 ) , showing that the bees that produced more propolis also produced more honey ( manrique and soares , 2002 ) . the negative residual correlations among the same traits ( 0.13 , 0.44 , 0.09 ) indicate that the improvement of environmental conditions will have an antagonistic effect . genetic correlations between hp and hb ( 0.34 ) and between scr and hb ( 0.24 ) were antagonistic , which suggest a negative response in selection . furthermore , the residual correlations ( 0.36 , 0.8 ) were positive , which indicates that environmental conditions were shared . these authors compared naturally mated queens from a hygienic line of italian honey bees ( apis mellifera ligustica ) with colonies of a commercial line of italian bees not selected for hygienic behavior . they found that the hygienic colonies removed more freeze - killed brood ( hygienic behavior ) and produced significantly more honey than the commercial lines . the positive genetic correlation between pp and hb ( 0.15 ) differs from other estimates in this study and was not expected . although the two traits represent different trends , and at least apparently the genetic association is not clear or not documented in the literature , these results suggest that the selection for more hygienic bees may increase propolis production . moreover , the positive residual correlation ( 0.65 ) was high and suggests that environmental effects affect both traits . the genetic correlations between pmab with hp , scr and hb ( 0.52 , 0.66 , 0.82 ) were high and favorable , except between pmab and pp ( 0.49 ) , which was in opposite direction . the results indicate that selection for hb , hp / scr should decrease pmab , but the selection for pp should increase pmab . many studies have shown the same relationship between hb , the tolerance to varroa destructor , and hp ( spivak and reuter , 1998 ; harris , 2008 ) . these same studies reported that hb in general and hb towards to varroa destructor ( varroa - sensitive hygienic behavior ) are mechanisms of tolerance against diseases and varroa mites . spivak and reuter ( 1998 ) reported that hygienic bees ( genetically selected ) also had significantly less chalkbrood , no american foulbrood , fewer mites , and produced more honey than commercial ( not selected ) bees . basically , there are two mechanisms that affect the levels of infestation of mites : grooming behavior ( adult bees detect and remove mites from themselves and from nestmates ) and hb ( the detection and removal of dead / ill or infested pupae from capped brood cells by adult bees ) . residual correlations ( 0.09 , 0.30 and 0.30 ) between pmab with hp , scr and hb were in opposite direction and between pp and pmab ( 0.59 ) they were in the same direction . in conclusion , the studied population of africanized honeybees showed sufficient genetic variation to begin a breeding program . depending on the breeding approach in a future program , commercial stocks of africanized honeybees that produce more propolis and honey may be achieved . moreover , hygienic behavior may be improved as a consequence of selecting for improved propolis production , but additional studies should be realized to better understand the genetic association between these traits . on the other hand , the rate of syrup consumption and propolis production may be used as selection criteria , preferably by including these traits in a selection index to improve traits of honeybees in breeding programs .
heritability and genetic correlations for honey ( hp ) and propolis production ( pp ) , hygienic behavior ( hb ) , syrup - collection rate ( scr ) and percentage of mites on adult bees ( pmab ) of a population of africanized honeybees were estimated . 
 data from 110 queen bees over three generations were evaluated . 
 single and multi - trait models were analyzed by bayesian inference using mtgsam . 
 the localization of the hive was significant for scr and hb and highly significant for pp . 
 season - year was highly significant only for scr . 
 the number of frames with bees was significant for hp and pp , including scr . 
 the heritability estimates were 0.16 for hp , 0.23 for scr , 0.52 for hb , 0.66 for pp , and 0.13 for pmab . 
 the genetic correlations were positive among productive traits ( pp , hp and scr ) and negative between productive traits and hb , except between pp and hb . 
 genetic correlations between pmab and other traits , in general , were negative , except with pp . 
 the study permitted to identify honeybees for improved propolis and honey production . 
 hygienic behavior may be improved as a consequence of selecting for improved propolis production . 
 the rate of syrup consumption and propolis production may be included in a selection index to enhance honeybee traits .