Comparative reproduction of Varroa destructor in different types of Russian and Italian honey bee combs

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1 Exp Appl Acrol (2008) 44: DOI /s Comprtive reproduction of Vrro destructor in different types of Russin nd Itlin honey ee coms Lili I. de Guzmn Æ Thoms E. Rinderer Æ Amnd M. Frke Received: 19 Decemer 2007 / Accepted: 13 Mrch 2008 / Pulished online: 8 April 2008 Ó US Government 2008 Astrct Erlier studies showed tht Russin honey ees support slow growth of vrro mite popultion. We studied whether or not com type influenced vrro reproduction in oth Russin nd Itlin honey ees, nd whether Russin ees produced com which inhiited vrro reproduction. The mjor differences found in this study concerned honey ee type. Overll, the Russin honey ees hd lower (2.44 ± 0.18%) levels of vrro infesttion thn Itlin honey ees (7.20 ± 0.60%). This decresed infesttion resulted in prt from reduced numer of vile femle offspring per foundress in the Russin (0.85 ± 0.04 femle) compred to the Itlin (1.23 ± 0.04 femles) honey ee colonies. In ddition, there ws n effect y the com uilt y the Russin honey ee colonies tht reduced vrro reproduction. When compring coms hving Russin or Itlin colony origins, Russin honey ee colonies hd more non-reproducing foundress mites nd fewer vile femle offspring in Russin honey ee com. This difference did not occur in Itlin colonies. The ge of com in this study hd mixed effects. Older com produced similr responses for six of the seven vrro infesttion prmeters mesured. In colonies of Itlin honey ees, the older com (2001 drk) hd fewer (1.13 ± 0.07 femles) vile femle offspring per foundress thn were found in the 2002 new (1.21 ± 0.06 femles) nd 1980s new (1.36 ± 0.08 femles) coms. This difference did not occur with Russin honey ee colonies where the numer of vile femle offspring ws low in ll three types of coms. This study suggests tht honey ee type lrgely influences growth of vrro mite popultion in colony. Keywords Resistnce Vrro destructor Reproduction Drk com New com L. I. de Guzmn (&) T. E. Rinderer A. M. Frke USDA/ARS, Honey Bee Breeding, Genetics nd Physiology Lortory, 1157 Ben Hur Rod, Bton Rouge, LA 70820, USA e-mil: lili.deguzmn@rs.usd.gov

2 228 Exp Appl Acrol (2008) 44: Introduction Mngement of vrro mites generlly requires the use of cricides. However, injudicious use of cricides my pose residue prolems, especilly in wx nd honey (Lodesni et l. 1992; Bogdnov et l. 1998; Kochnsky et l. 2001; Mrtel nd Zeggne 2002). It my lso led to the development of mites resistnt to cricides. In the United Sttes, resistnce to mitrz, fluvlinte nd coumphos y vrro mites hs een reported (Bxter et l. 1998; Elzen et l. 1999; Elzen nd Westervelt 2002). Thus, the implementtion of sound Integrted Pest Mngement (IPM) progrms involving the use of honey ees resistnt to mites nd non-chemicl mite control techniques my e the key to mnging prsitic mite popultions. One possile contriution to successful IPM progrm is the com type provided to colonies for rood production. One ttriute of com, which vries, is cell size. Different honey ee su-species uild cells of different sizes. Lrger cells uilt y Europen honey ees (EHB) supported greter vrro reproduction when compred to the smller cells uilt y Africnized honey ees (Messge nd Gonclves 1995). However, study compring smll nd lrge cells oth uilt y EHB showed no differences in vrro reproduction (J. Berry, personl communiction). Coms of different ges lso hve different sizes. Older com tht hs repetedly een used for rood rering hs n ccumultion of lyers of cocoons, which reduces cell size (Chuvin 1962 s cited y Hepurn nd Kurstjens 1988). In contrst to the report of Messge nd Gonclves (1995), higher vrro reproduction hs een reported in old com hving smller size thn in new com with AHB in Brzil (Piccirillo nd de Jong 2004). Coms lso contin voltile chemicls. For exmple, the odor of com increses ees hording ehvior (Rinderer nd Bxter 1978). Semiochemicls occur in lrvl food (Nzzi et l. 2001) which proly help regulte lrvl feeding ut lso ttrct vrro mites. Other voltiles ssocited with cocoons (Donzé et l. 1998) nd generl nest odors proly ccumulte in older coms. Perhps ees tht re resistnt to vrro mites produce com with voltiles tht inhiit vrro reproduction. Owing to the lipophylic nture of its wx, com tht remins in nests during cricidl tretments for vrro is known to retin nd ccumulte trces of cricides (Lodesni et l. 1992). These cricide residues present in treted coms re known to ffect vrro mite popultion growth (Krus nd Pge 1995). Acricides lso re retined in wx used to produce commercil wx foundtions (Lodesni et l. 2003; Jiménez et l. 2005; Leníček et l. 2006). High contmintion levels (100 ppm fluvlinte, nd 10 nd 100 ppm coumphos) cused drmtic vrro mite mortlity during the first rood cycle (Fries et l. 1998). However, the ccumultion of cocoons cn prevent mite mortlity even t high contmintion levels (Fries et l. 1998). The Russin honey ees progrm egn in 1997 when queens from the Primorky region were imported into the United Sttes (Rinderer et l. 2000). Series of experiments were then conducted nd showed tht Russin ees re resistnt to vrro mites (Rinderer et l. 2000, 2001). Growth of vrro mites in Russin honey ee colonies is consistently slow which ws supported y lower percentges of infested worker nd drone rood cells, lower frequency of rood cells infested with multiple mites, lower mite reproduction nd n extended phoretic period (de Guzmn et l. 2007). Other mechnisms such s com type or cell size my lso e involved. To explore these possiilities, we studied whether or not older com supported less vrro reproduction in oth Russin nd Itlin honey ees, nd whether Russin ees produced com which inhiited vrro reproduction.

3 Exp Appl Acrol (2008) 44: Mterils nd methods Experiment 1 Reproduction of vrro in different types of coms uilt nd used y the sme honey ee type through four rood-rering cycles Thirty colonies (15 Russin nd 15 Itlin) were estlished on My 1, 2002 using the lrge pckge technique (Hro nd Hoopingrner 1997). Russin queens were otined from the Russin honey ee reeding progrm while the Itlin queens were purchsed from queen reeder in Cliforni who dvertises Itlin queens. All colonies used coms tht were drwn nd used y the honey ee type tht produced them such tht Itlin colonies only used coms drwn y the Itlin ees nd Russin colonies exclusively used coms tht were produced y Russin ees. When drwn coms were unville, frmes with wx foundtion were used. All colonies received one drone com to ccelerte vrro popultion growth. The initil mite infesttion of pckges ws 81 ± 6 mites (men ± SD) per 1.4-kg pckge. This experiment egn in July 2002 when test ees populted the hives. Ech colony received three types of test coms: () drk com (cell size = 5.38 mm) which strted from wx foundtion (purchsed in 2001), uilt nd then used extensively for rood rering y the sme honey ee types during the 2001 seson, () new com (cell size = 5.35 mm), drwn y the sme honey ee type using wx foundtion purchsed in 2002, nd (c) new com (cell size = 5.35 mm), drwn y the sme honey ee type from wx foundtion purchsed in the erly 1980s efore the discovery of trchel (1984) nd vrro (1987) mites in the U.S. All drk coms were in storge for out 6 months prior to use. None of the coms used in test colonies received ny form of chemicl tretment. For ech com type, vrro mite reproduction ws monitored during four rood cycles. Ech rood cycle requires out 17 dys from egg oviposition to tn-odied pupe. We presumed tht ll cells exmined supported four rood cycles since ll test coms hd out 85 90% seled rood during ech oservtion period. Evlution ws conducted from July to Septemer Experiment 2 Reproduction of vrro in coms uilt nd used y other honey ee type Colonies from Experiment 1 were lso used in this study. Ech colony received two test coms from the other honey ee type eing tested: Russin honey ee colonies received coms used nd uilt y Itlin colonies nd vice vers. The two test coms were introduced simultneously in the middle of the rood nest for egg-lying. For comprison, reproduction of vrro mites in ech host colony ws lso ssessed using two coms tht contined rood of similr ge s the introduced test coms. Two trils were conducted. Mite reproduction evlution For oth experiments, rood cells were exmined until infested cells contining purple-eyed or tn-odied pupe were otined per com type per smpling time or until 500 rood cells were exmined. For Experiment 1, the totl numers of cells exmined were s follows: () 2001 drk com, Itlin = 20,618 (971 infested; 906 singly-infested) nd Russin = 23,142 cells (516 infested; 498 singly-infested); () 2002 new com, Itlin = 18,730 (977 infested; 898 singly-infested) nd Russin = 20,353 cells (424

4 230 Exp Appl Acrol (2008) 44: infested; 400 singly-infested); nd (c) 1980s new com, Itlin = 20,901 (1,060 infested; 989 singly-infested) nd Russin = 21,358 cells (560 infested; 538 singly-infested). During exmintion, vriety of dt relted to reproduction were recorded. Nonreproduction ws mesured s descried y Hro nd Hrris (2001). Mites re considered non-reproductive when they enter the cells ut: () produce no progeny, () produce mles only, (c) produce progeny too lte to mture, or (d) when the foundress dies efore she cn reproduce. Proportions of non-reproductive femles, numers of progeny, numers of vile femle offspring nd ded mites were estimted using rood cells infested with only single foundress mite. For the totl numer of mites per infested cell, oth singly- nd multiply-infested cells were nlyzed. Colonies with less thn eight singly-infested cells were excluded from the nlyses of the proportion of nonreproductive mites. Dt nlyses Dt from Experiment 1 were sujected to ANOVA for repeted mesures using compound symmetry covrince structure using the MIXED procedure. Honey ee type, com type nd rood cycle were included in the model with rood cycle eing the repeted effect. No prmeter hd significnt three-wy interction for com type, honey ee type nd rood cycle. Men seprtions were conducted y Tukey s test for multiple men comprisons while t-test ws used to compre mens of the two honey ee types (SAS version 8.2, SAS Institute Inc 2001). For Experiment 2, dt were nlyzed using one-wy ANOVA compring the four honey ee type-y-com comintions. Before nlyses, dt on the proportion of rood infested nd non-reproductive mites were trnsformed using the rcsine trnsformtion. Men seprtions were conducted y Tukey s test (SAS version 8.2, SAS Institute Inc 2001). Results Experiment 1 For the percentge of rood infested (PI), ANOVA reveled no significnt differences mong com type (F = 1.23; df = 2, 236; P = 0.296). However, significnt interction etween honey ee type nd rood cycle ws detected (F = 13.29; df = 3, 235; P \ ) (Fig. 1). PI vried mong the four rood cycles within the Itlin (F = 47.77; P \ ) nd Russin (F = 4.14; P = 0.007) honey ee colonies. For oth honey ee types, the highest infesttions were oserved in the 3rd nd 4th cycles with the lowest infesttion recorded in the first cycle. Within rood cycles, oth honey ee types hd similrly low levels of infesttion during the 1st cycle. Therefter, PI significntly incresed with the Itlin honey ees hving higher infesttions thn the Russin honey ees. On verge, the Itlin honey ees hd higher PI thn the Russin honey ees (F = 13.47; df = 1, 28.4; P \ ). Anlysis of the proportion of multiply-infested cells (MI) showed no significnt effect of com type (F = 1.8; df = 2, 235; P = 0.168). However, significnt interction etween honey ee type nd rood cycle (F = 2.91; df = 3, 234; P = 0.035) ws detected (Fig. 2). For the Itlin honey ee colonies, the highest MI ws oserved during the 3rd

5 Exp Appl Acrol (2008) 44: % Infesttion c Cycle 1 Cycle 2 Cycle 3 Cycle 4 c c Itlin Russin 0 Itlin Russin Averge Fig. 1 Averge percentge (men ± SE) of worker rood infested in colonies of Itlin nd Russin honey ees through four rood cycles nd overll verge for ech honey ee type. For ech honey ee type, mens followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test. In totl, 60,249 Itlin nd 64,853 Russin worker rood cells were exmined Cycle 1 Cycle 2 Cycle 3 Cycle 4 Itlin Russin % Multiple Infesttion Itlin Russin Averge Fig. 2 Averge percentge (men ± SE) of multiply-infested worker rood in colonies of Itlin nd Russin honey ees through four rood cycles nd overll verge for ech honey ee type. For ech honey ee type, mens followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test nd 4th cycles while the 1st nd 2nd cycles showed the lowest MI. In the Russin honey ees, MI remined consistently low throughout the four rood cycles. MI ws comprle etween the two honey ee types during the 1st nd 2nd cycles. The Itlin honey ees hd more MI thn the Russin honey ees in oth the 3rd nd 4th rood cycles. Overll, Itlin honey ees hd higher MI thn Russin honey ees (F = 9.07; df = 1, 24.6; P = 0.006). For the proportion of non-reproductive (NR) mites, no two-wy interctions nd no com type (F = 0.38; df = 2,175; P = 0.684) or rood cycle (F = 2.41; df = 3,172; P = 0.069) effects were detected. NR etween the two honey ee types diverged ut not

6 232 Exp Appl Acrol (2008) 44: Avg # Progeny / Foundress Cycle 1 Cycle 2 Cycle 3 Cycle 4 Itlin Russin Fig. 3 Averge numer (men ± SE) of progeny per foundress through different rood cycles nd in Itlin nd Russin honey ee colonies. Mens for the four rood cycles followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test significntly (F = 2.67; df = 2,21.7; P = 0.117) with the Itlin nd Russin honey ees hving mens of ± 1.30% nd ± 2.03%, respectively. No two-wy interctions or no com type (F = 0.82; df = 2, 238; P = 0.44) effect were detected for the verge numer of living progeny per femle. However, significnt honey ee type (F = 16.98; df = 1, 23.8; P = ) nd rood cycle (F = 4.07; df = 3, 236; P = 0.008) effects were oserved (Fig. 3). Overll, mites infesting Itlin honey ees produced significntly more progeny thn the mites infesting Russin honey ees. More mite progeny were recorded during the first three rood cycles thn in the 4th cycle, which ws similr to tht of cycle 1. The numer of vile femle offspring per foundress lso showed significnt interction etween honey ee type nd com type (F = 4.35; df = 2, 240; P = 0.014) (Fig. 4). Within com type, oth honey ee types hd similr numer of vile femle offspring in the drk coms (F = 2.29; P = 0.133). In the 2002 new (F = 20.73; P \ ) nd 1980s new (F = 28.96; P \ ) coms, the Itlin honey ees supported more vile femle offspring thn did the Russin honey ees. Within honey ee type, the numer of vile femle offspring differed significntly mong the com types (F = 3.61; P = 0.029). In the Itlin honey ees, 1980s new coms hd the highest numer of vile femle offspring per foundress nd the drk coms hd the lowest. In the Russin honey ee colonies, drk coms hd more vile femle offspring thn the two new (2002 nd 1980s) coms. However, the difference ws not strong (F = 2.59; P = 0.077). Overll, Itlin honey ees hd more (F = 44.32; df = 1, 23.9; P \ ) vile femle offspring per foundress thn the Russin honey ees. Brood cycle hd no effect on the numer of vile femle offspring per foundress (F = 2.05; df = 3, 236; P = 0.108). When numers of mites per infested cell were nlyzed, no significnt com effect (F = 0.55; df = 2, 240; P = 0.576) or two-wy interctions were detected. However,

7 Exp Appl Acrol (2008) 44: Avg # Vile Femle Offspring / Foundress Drk 2002 New 1980's New Itlin Russin 0.0 Itlin Russin Averge Fig. 4 Averge numer (men ± SE) of vile femle offspring per foundress in different com types of Itlin nd Russin honey ees. For ech honey ee type, mens followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test Avg # Mites / Infested Cell c c 0 Cycle 1 Cycle 2 Cycle 3 Cycle 4 Itlin Russin Fig. 5 Averge numer (men ± SE) of mites per infested cell through different rood cycles nd in Itlin nd Russin honey ee colonies. Mens for the four rood cycles followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test significnt influence of rood cycle (F = 3.16; df = 3, 238; P = 0.025) on the numer of mites per infested cell ws detected (Fig. 5). The highest numers of mites were recorded during the 2nd nd 3rd cycles with the lowest numer recorded in the 4th cycle. Honey ee type effect ws lso detected with the Itlin honey ees hving higher numers of mites per infested cell thn the Russin honey ees (F = 14.88; df = 1, 23.5; P = ). For the verge numer of ded mites, no honey ee type (F = 0.19; df = 1, 25; P = 0.665), com type (F = 0.16; df = 2, 238; P = 0.854) or two-wy interction effects were

8 234 Exp Appl Acrol (2008) 44: Avg # Ded Mites / Infested Cell c Cycle 1 Cycle 2 Cycle 3 Cycle 4 Itlin Russin Fig. 6 Averge numer (men ± SE) of ded mites per infested cell (only singly-infested) through different rood cycles nd overll verge for ech honey ee type. Mens for the four rood cycles followed y different letters re significntly different t P \ 0.05 ccording to ANOVA for repeted mesures followed y Tukey s test. Mens for the two honey ee types were compred using t-test oserved. The numer of ded mites ws influenced y rood cycle (F = 10.73; df = 3,237; P \ ) (Fig. 6).The highest mite mortlity ws recorded during the 4th cycle, followed y 2nd nd 3rd cycles with the lowest mortlity oserved during the 1st cycle. Experiment 2 Anlyses showed significnt differences mong the four honey ee type-y-com comintion groups for PI, NR, nd numers of progeny nd vile offspring per foundress (Tle 1). After exmining [50,000 rood cells, we found tht Itlin honey ee colonies hd higher PI thn the Russin honey ees regrdless of com origins (P \ ). For NR, the Russin coms in the Russin colonies supported the highest NR (P = 0.008) with the other three groups hving similrly lower NR. Vrro mites reproduced more in the Itlin colonies (whether in foreign or locl coms) nd in the Itlin coms hosted y Russin honey ee colonies s indicted y hving more progeny (P = ) nd vile femle offspring (P = ) per foundress. The coms uilt y Russin ee colonies in the Russin honey ee colonies supported the lowest reproduction of vrro. No differences mong the four groups for the numer of ded mites per infested cell (P = 0.304) were detected. Discussion The mjor differences found in this study concerned honey ee type nd generlly confirmed tht Russin honey ees re more resistnt to vrro mites thn Itlin honey ees (Rinderer et l. 2001; de Guzmn et l. 2007). The Russin colonies hd lower percentge of rood cells tht were infested. This proly led to lso hving lower percentge of multiply-infested rood cells. One fctor tht contriuted to Russin colonies hving fewer mites ws the comprtively reduced numer of vile femle offspring per foundress. This comprison ws sed only on rood cells hving single foundress. Since non-reproducing foundress mites were included in the estimtion of the numer of vile

9 Exp Appl Acrol (2008) 44: Tle 1 Vrro infesttion prmeters (men ± SE) in coms hving Russin or Itlin colony origins Com type Totl numer of cells exmined (# cells infested) % Infesttion % Non-reproduction (# infested cells with one foundress) # Progeny per foundress # Vile femle offspring/foundress # Ded mites Russin coms in Itlin colonies 13,267 (1,275) ± ± 1.72 (1,136) 3.26 ± ± ± 0.04 Itlin coms in Itlin colonies 11,096 (973) ± ± 2.57 (882) 3.00 ± ± ± 0.03 Itlin coms in Russin colonies 13,272 (726) 5.75 ± ± 2.97 (696) 2.85 ± ± ± 0.04 Russin coms in Russin colonies 12,564 (509) 5.33 ± ± 3.44 (484) 2.31 ± 0.18 c 0.82 ± ± 0.05 P \ * P = 0.008* P \ * P = * P = ns * For ech column, mens followed y different letters re significntly (P \ 0.05) different using one-wy ANOVA followed y Tukey s test ns Not significnt

10 236 Exp Appl Acrol (2008) 44: femle offspring, non-reproduction is chief contriutor to the difference etween the two honey ee types for the numer of vile femle offspring per foundress. Regrdless of the mechnism, the com uilt y Russin honey ees contriutes to the increse in the rte of non-reproduction nd decrese in the verge numer of vile femle offspring. In the comprison of coms hving Russin or Itlin colony origins in Experiment 2, Russin honey ee colonies hd fewer numers of vile femle offspring in Russin honey ee com. This difference did not occur in Itlin colonies. Hence, there my e n interction etween chrcteristics of the com nd rood rering. Perhps the effect results from the comined ction of inhiitory compounds emnting from oth the com nd the rood. It hs een reported tht chemicls tht ttrct or influence vrro mite reproduction my come from lrvl food (Nzzi et l. 2001). Therefore, it is possile tht semiochemicls from the lrvl food cn e found in the cocoon. Cocoons hve lso een documented to contin semiochemicls, which is used for the deposition of vrro feces used for ggregtion, egg lying nd molting y nymphs (Donzé nd Guerin 1994). Russin com in Russin honey ee colonies lso ws ssocited with n increse in the percentge of non-reproductive mites. Mesures of non-reproduction re known to e incresed y vrro sensitive hygienic ehvior (Hro nd Hrris 2005). The Russin com in Russin honey ee colonies my hve: (1) stimulted n increse in the rte of hygienic ehvior, (2) through some interctive effect involving rood directly incresed the rte of non-reproduction in infesting mites, or (3) stimulted oth hygienic ehvior nd non-reproduction. Differences in the ge of com (=cell size) in this study hd mixed effects. Older com with cocoons produced similr responses for six of the seven vrro infesttion prmeters. In colonies of Itlin honey ees, the older com hd fewer vile femle offspring per foundress thn were found in oth new (2002 nd 1980s) coms.this difference did not occur with Russin honey ee colonies where the numer of vile femle offspring ws low in ll three types of coms. In AHB, higher vrro infesttions were recorded in old rood coms tht hve reduced cell size due to ccumultion of cocoons thn in new rood coms (Piccirillo nd de Jong 2004). However, EHB coms (lrger cells) re reported to support higher vrro reproduction thn AHB coms which hve smller cells (Messge nd Gonclves 1995). These discrepncies suggest tht honey ee genotype lrgely influences vrro mites ility to reproduce in the rood cells. Perhps, AHB produces com tht negtively ffects vrro reproduction through mens not relted to cell size. Acricide residues hve een detected in commercil wx foundtions (Lodesni et l. 2003; Jiménez et l. 2005; Leníček et l. 2006) nd cn hve negtive effects on vrro mites. Fries et l. (1998) documented tht com drwn from foundtions treted with 100 ppm fluvlinte, nd 10 nd 100 ppm coumphos cused drmtic vrro mortlity during the first rood cycle. In this study, no residue nlysis ws conducted. However, the low numer of ded mites we oserved during the first rood cycle my suggest either the sence of residues in the foundtions or their presence t levels tht did not cuse high mortlity of vrro mites. Fries et l. (1998) oserved low vrro mortlity in foundtions treted with 1 nd 10 ppm fluvlinte, nd 1 ppm coumphos. The uthors lso oserved tht the presence of two lyers of cocoons prevented deths of foundress mites even t the highest contmintion level of 100 ppm. Thus, the increse in the percentge of rood cells infested, percentge of multiple infesttions nd numer of progeny per foundress throughout the four rood cycles mye ccelerted y the ccumultion of C4 lyers of cocoons inside the rood cells. The only com difference ws older com hving fewer vile femle offspring per foundress in Itlin honey ee colonies. This difference did not occur with Russin honey

11 Exp Appl Acrol (2008) 44: ee colonies where the numer of vile femle offspring ws low in ll three types of coms. Our oservtions confirm erlier reports tht honey ee type lrgely influence growth of vrro mite popultion in colony. Acknowledgments We thnk Gry Deltte, Lorrine Bemn, Tony Stelzer nd Ahline Angeles for their technicl help. Chrlie Hrper of Hrper s piries provided wx foundtions from the erly 1980s. This reserch ws completed in coopertion with the Louisin Agriculturl Experiment Sttion. References Bxter JR, Eischen F, Pettis J, Wilson WT, Shimnuki H (1998) Detection of fluvlinte-resistnt Vrro mites in the United Sttes. Am Bee J 138:291 Bogdnov S, Kilchenmnn V, Imdorf A (1998) Acricide residues in some ee products. J Apic Res 37:57 67 de Guzmn LI, Rinderer TE, Frke AM (2007) Growth of Vrro destructor Anderson nd Truemn (Acri: Vrroide) popultions in Russin honey ee (Apis mellifer L.) (Hymenopter: Apide) colonies. Ann Entomol Soc Am 100: Donzé GS, Guerin PM (1994) Behviorl ttriutes nd prentl cre of Vrro mites prsitizing honey ee rood. Behv Ecol Socioiol 34: Donzé GS, Schnyder-Cndrin S, Bogdnov S, Diehl PA, Guerin PM (1998) Aliphtic lcohols nd ldehydes of the honey ee cocoon induce rrestment ehvior in Vrro jcosoni (Acri: Mesostigmt), n ectoprsite of Apis mellifer. Arch Insect Biochem Physiol 37: Elzen PJ, Westervelt D (2002) Detection of coumphos resistnce in Vrro destructor in Florid. Am Bee J 142: Elzen PJ, Bxter JR, Spivk M, Wilson WT (1999) Amitrz resistnce in Vrro: new discovery in North Americ. Am Bee J 139:362 Fries I, Wllner K, Rosenkrnz P (1998) Effects on Vrro jcosoni from cricides in eeswx. J Apic Res 37:85 90 Hro JR, Hrris JW (2001) The reltionship etween nonreproduction of vrro nd the quntity of worker rood. Am Bee J 141: Hro JR, Hrris JW (2005) Suppressed mite reproduction explined y the ehviour of dult ees. J Apic Res 44:21 23 Hro J, Hoopingrner RA (1997) Honey ees (Hymenopter: Apide) in the United Sttes tht express resistnce to Vrro jcosoni. J Econ Entomol 90: Hepurn HR, Kurstjens SP (1988) The coms of honey ees s composite mterils. Apidologie 19:25 36 Jiménez JJ, Bernl JL, del Nozl MJ, Mrtín MT (2005) Residues of orgnic contminnts in eeswx. Eur J Lipid Sci Technol 107: Kochnsky J, Wilzer K, Feldlufer M (2001) Comprison of the trnsfer of coumphos from eeswx into syrup nd honey. Apidologie 32: Krus B, Pge RE Jr (1995) Popultion growth of Vrro jcosoni Oud in Mediterrnen climtes of Cliforni. Apidologie 26: Leníček J, Sekyr M, Novotná AR, Vášová E, Titěr D, Veselý V (2006) Solid phse microextrction nd gs chromtogrphy with ion trp detector (GC-ITD) nlysis of mitrz residues in eeswx fter hydrolysis to 2,4-dimethylniline. Anl Chim Act 571:40 44 Lodesni M, Pellcni A, Bergomi S, Crpn E, Ritti T, Lsgni P (1992) Residue determintion for some products used ginst Vrro infesttions in ees. Apidologie 23: Lodesni M, Cost C, Biglirdi M, Colomo R (2003) Acricide residues in ee wx nd orgnic eekeeping. Apict 38:31 33 Mrtel A, Zeggne S (2002) Determintion of cricides in honey y high-performnce liquid chromtogrphy with photodiode rry detection. J Chromtogr 954: Messge D, Gonclves LS (1995) Effect of the size of worker rood cells of Africnized honey ees on infesttion nd reproduction of the ectoprsitic mite Vrro jcosoni Oud. Apidologie 26: Nzzi F, Milni N, Vedov GD, Nimis M (2001) Semiochemicls from lrvl food ffect the locomotory ehviour of Vrro destructor. Apidologie 32: Piccirillo GA, de Jong D (2004) Old honey ee rood coms re more infested y the mite Vrro destructor thn re new rood coms. Apidologie 35: Rinderer TE, Bxter J (1978) Effect of empty com on hording ehvior nd honey production of the honey ee. J Econ Entomol 71:

12 238 Exp Appl Acrol (2008) 44: Rinderer TE, de Guzmn LI, Hrris J, Kuznetsov V, Deltte GT, Stelzer JA, Bemn L (2000) The relese of ARS Russin honey ees. Am Bee J 140: Rinderer TE, de Guzmn LI, Deltte GT, Stelzer JA, Kuznetsov V, Bemn L, Wtts R, Hrris J (2001) Resistnce to the prsitic mite Vrro destructor in honey ees from Fr-estern Russi. Apidologie 32: SAS Institute Inc (2001) SAS user s guide, version 8.2. SAS Institute, Cry, NC