Prevalence and reproduction of Tropilaelaps mercedesae and Varroa destructor in concurrently infested Apis mellifera colonies
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1 Prevlence nd reproduction of Tropilelps mercedese nd Vrro destructor in concurrently infested Apis mellifer colonies Buwngpong, N., de Guzmn, L. I., Khongphinitunjong, K., Frke, A. M., Burgett, M., & Chntwnnkul, P. (2015). Prevlence nd reproduction of Tropilelps mercedese nd Vrro destructor in concurrently infested Apis mellifer colonies. Apidologie, 46(6), doi: /s /s Springer Version of Record
2 Apidologie (2015) 46: * INRA, DIB nd Springer-Verlg Frnce, 2015 DOI: /s Originl rticle Prevlence nd reproduction of Tropilelps mercedese nd Vrro destructor in concurrently infested Apis mellifer colonies Nint BUAWANGPONG 1, LiliI.deGUZMAN 2, Kitiphong KHONGPHINITBUNJONG 1, Amnd M. FRAKE 2, Michel BURGETT 3, Pnuwn CHANTAWANNAKUL 1 1 Deprtment of Biology, Fculty of Science, Ching Mi University, Ching Mi 50200, Thilnd 2 Honey Bee Breeding, Genetics nd Physiology Lortory, USDA-ARS, 1157 Ben Hur Rod, Bton Rouge, LA 70820, USA 3 Deprtment of Horticulture, Oregon Stte University, Corvllis, OR 97331, USA Received 19 June 2014 Revised 25 Mrch 2015 Accepted 14 April 2015 Astrct The prevlence of Tropilelps mercedese nd Vrro destructor in concurrently infested A. mellifer colonies in Thilnd ws monitored. We lso ssessed the fecundity of T. mercedese nd V. destructor in nturlly infested rood nd in rood cells deliertely infested with oth mite gener. Results showed tht the nturl co-infesttion of n individul rood cell y oth mite gener ws rre (<0.1 %). Overll, T. mercedese ws the more dominnt rood prsite of A. mellifer thn V. destructor. In nturlly infested rood, the proportion of nonreproductive Tropilelps (29.8±3.9 %) ws lower thn tht of Vrro (49.6±5.9 %). Both mites produced similr numers of progeny (T. mercedese =1.48±0.05; V. destructor =1.69±0.14). The two mite gener lso reproduced normlly when they were deliertely introduced into the sme rood cells. In two seprte ssessments, the verge worker rood infesttions of T. mercedese (19.9 %) were significntly higher thn tht of V. destructor (0.7 %). Our results on the higher prevlence nd reproductive ility of T. mercedese in concurrently infested colonies reffirm Tropilelps competitive dvntge over V. destructor nd their reported negtive impct to A. mellifer colonies. Apis mellifer / Tropilelps mercedese / Vrro destructor / concurrent infesttion / sesonl undnce 1. INTRODUCTION Vrro destructor nd Tropilelps hve een co-infesting A. mellifer colonies for out 50 yers in Asi (Delfindo 1963). However, infesttions of T. clree (likely referring to T. mercedese ) were higher thn those of V. jcosoni (likely referring to V. destructor )in Thilnd (Burgett et l. 1983). Similr trends were oserved in Afghnistn nd Vietnm (Woyke 1987, 1989). However, in the Philippines, those Corresponding uthor: P. Chntwnnkul, pnuwn@gmil.com Hndling Editor: Yves Le Conte A. mellifer colonies tht hd higher infesttions of T. clree thn Vrro in April hd higher Vrro thn T. clree infesttions in Septemer (Fjrdo nd Cervnci 2004). In Northern Thilnd, Kvinseksn et l. (2003) monitored T. clree (proly referring to T. mercedese ) infesttions in mite-inoculted colonies of Primorsky ees (=Russin honey ees, RHB) nd Thi A. mellifer. The uthor found tht RHB colonies (men=18.5 %) supported higher rood infesttion thn the locl ees (men= 11.4 %) with the highest infesttions oserved in My (RHB=33 %, Thi A. mellifer =21 %). Fctors tht influence popultion fluctutions of oth mites in concurrently infested colonies hve not een studied.
3 780 N. Buwngpong et l. Although oth V. destructor nd T. mercedese re oserved in infesting colonies, T. mercedese is considered to e more serious prolem of A. mellifer colonies thn Vrro mites in Northern Thilnd (Burgett et l. 1983; Anderson nd Morgn 2007). This discrepncy in severity my e due to differences in their ilities to compete for honey ee hosts nd reproduce within rood cells. In this study, we monitored the uild-up nd synchroniztion in the popultions of oth V. destructor nd T. mercedese in concurrently infested A. mellifer colonies. Reproduction ws lso ssessed in nturlly infested rood nd in rood cells deliertely infested with oth mite gener to determine if vrition in reproduction exists. Knowledge on differentil reproduction my help explin popultion fluctutions, competitive dvntge, or virulence of one mite species. 2. MATERIALS AND METHODS 2.1. Experiment 1: rood infesttions of V. destructor nd T. mercedese in concurrently infested A. mellifer colonies Oservtions were conducted using 16 colonies housed in 10-frme Lngstroth hives from Septemer 2011 to Septemer No cricidl tretments were pplied to the colonies during the course of the study. All queens were hyrids sed on n Itlin honey ee (A. m. ligustic ). The rood re (cm 2 ) ws determined y visul estimtion of com re covered y cpped rood (Rogers et l. 1983). Mite infesttion prmeters were determined y rndomly exmining worker rood cells from ech colony on monthly schedule (de Guzmn et l. 2007). Stges of mite progeny were differentited nd recorded. Since the results of the 13-month oservtion showed rre co-infesttions of oth Tropilelps nd Vrro mites, we decided to confirm our oservtion y exmining three dditionl concurrently infested A. mellifer colonies. For ech colony, different stges of worker nd drone rood were exmined for the presence or sence of these two prsitic mites. Adult ee infesttion ws lso determined y smpling out ees per colony nd wshed with sopy wter to remove mites (Rinderer et l. 2004). The mites were collected nd then differentited ccording to species Experiment 2: comprtive reproduction of V. destructor nd T. mercedese in rtificilly inoculted rood During the conduct of experiment 1, we rrely oserved rood cells tht were infested with oth Tropilelps nd Vrro. This experiment sought to investigte mite reproduction when oth Tropilelps nd Vrro were deliertely introduced into the sme rood cells. To provide colonies s free of mites s possile, eight previously cricide-treted A. mellifer colonies were used in this study (tufluvlinte ws used s cricide in the ee colonies). To otin rood of the sme ge, ech queen ws cged over n empty com for 24 h y using push-in cge (8 mesh screen) providing rood re of out 400 rood cells. On the eighth dy when rood cells were cpped, one foundress T. mercedese nd one V. destructor were introduced into the sme rood cell. All inoculum foundress mites (drk in color) were collected from tn-odied pupe of highly infested A. mellifer colonies. Inoculum Tropilelps were first exmined under dissecting microscope to exclude mles. To inoculte newly seled lrve, the mite trnsfer technique ws used (Grrido nd Rosenkrnz 2003; Kirrne et l. 2011; Khongphinitunjong et l. 2013). Nine dys following mite inocultion, the rood cells contining tn-odied pupe were opened to ssess mite reproduction. All stges of mites were differentited Mite reproductive sttus For experiment 1, reproductive foundress Tropilelps nd Vrro mites were those tht hd t lest one progeny. Experiment 2 used two criteri to ssess the proportions of nonreproductive foundress mites in order to compre the results of previous studies (de Guzmn et l. 2007; Khongphinitunjong et l. 2013). For criteri 1, reproductive foundress Vrro mites were those tht produced n dult mle nd young dughter or vile offspring (de Guzmn et l. 2008). Since Tropilelps mites hve shorter life cycle when compred to Vrro, it is possile tht Tropilelps foundress my ly more eggs which cn develop to dult offspring y the time of the ee emergence (Sihg 1988; Smmtoro et l. 2000). Woyke (1987) reported tht Tropilelps ws lso le to copulte outside the ntl cell. Thus, reproductive foundress
4 Prevlence nd reproduction of Asin mites in Apis mellifer 781 Tropilelps mites were those tht hd t lest one progeny (Khongphinitunjong et l. 2013). For criteri 2, regrdless of the mites mting ehvior, reproductive foundress Vrro or Tropilelp s were those tht produced 1 progeny Dt nlyses For experiment 1, only rood cells infested with either T. mercedese or V. destructor were considered for sttisticl nlyses. Prior to nlyses, dt on the percentge infesttion nd percentge nonreproduction (NR) were trnsformed using n rcsine squre-root trnsformtion. A repeted mesures nlysis of vrince (ANOVA) with oservtion dtes nd mite type s the min effects ws performed to determine differences in infesttions of oth mite types through time. A z -test for proportions ws used to compre the overll nonreproductive sttus for oth mite species. A one-wy ANOVA ws used to determine infesttion trends of V. destructor nd T. mercedese nd the mount of rood in the colony through time. For experiment 2, z -test for two proportions ws used to compre reproduction success etween the two mite gener. Differences in the reproductive sttus for ech tril were compred using the Mrscuillo procedure for multiple proportions ( div898/hndook/prc/section4/prc474.htm). A pired smple t test ws used to compre differences in the numer of progeny produced y foundress Tropilelps nd Vrro mites. 3. RESULTS 3.1. Experiment 1: infesttions of V. destructor nd T. mercedese in concurrently infested A. mellifer colonies The test colonies rered rood continuously during the experimentl period. The highest numers of seled rood cells were recorded in Mrch to June 2012 (Figure 1) (F 11,178 =4.63, P <0.0001). Of the 18,250 worker rood cells exmined throughout this experiment, only 13 rood cells (<0.1 %) were found to e concurrently infested with oth V. destructor nd T. mercedese. Of the 970 infested rood cells, 24 % were infested with Vrro,while76%were infested y Tropilelps.Onlyninecolonies(out of 16 colonies) produced drone rood during the experiment. In totl, 506 drone rood cells were produced throughout the experiment, nd ll were exmined. Only 13 drone cells (2.6 %) were infested with Tropilelps, nd 78 (15.4 %) were infested with Vrro mites. Our results showed significnt effects of oth mite type (F 1,13 =42.75, P <0.0001) nd dte of oservtions (F 12,137 =5.80, P <0.0001) for the prevlence of oth mite gener. Since there ws significnt interction etween mite type nd dte of oservtion (F 12,136 =4.39, P <0.0001), the differences in infesttion rtes etween mite gener were determined for ech dte of oservtion. Initilly in Septemer 2011, the colonies egn with significntly higher infesttion of Tropilelps (10.6±2.8 %) thn Vrro (2.1± 1.0 %) (F 1136 =20.94, P <0.0001) (Figure 2). Therefter, infesttion levels of oth mite gener decresed significntly lthough Tropilelps infesttions remined higher thn those of Vrro from Octoer, Novemer, nd Decemer 2011 (F 1136 =23.55, P <0.0001; F 1136 =8.76, P = ; F 1136 =4.74, P =0.0311, respectively). Infesttion y Tropilelps significntly decresed in Jnury 2012, slightly incresed in Ferury 2012 with smll pek in Mrch 2012, grdul decrese in April 2012 nd steep decline in My However, infesttions y Tropilelps nd Vrro were similr during these months (Jnury, F 1136 =0.22, P =0.6374; Ferury, F 1136 =0.41, P =0.5253; April, F 1136 = 3.06, P =0.0823; My, F 1136 =0.72, P =0.3987) except in Mrch 2012 when Tropilelps hd higher infesttion thn Vrro mites (F 1136 = 4.24, P =0.0413). Infesttions y oth mite species remined similrly low in June 2012 (F 1136 = 5.26, P =0.0233). At this time, only four of the 15 surviving colonies were infested. Although infesttion y Vrro incresed in July 2012, no difference in the rtes of infesttion etween the mite species ws oserved (F 1136 =2.54, P =0.1135). Infesttion y oth mite species similrly decresed in August (F 1136 =2.82,P =0.0957) when only 11 colonies were smpled ecuse severl colonies were too wek to smple. Infesttions incresed gin in Septemer 2012 with Tropilelps hving higher rte of infesttion
5 782 N. Buwngpong et l Brood Cells (Thousnds) d c Sep-11 Oct-11 Nov-11 Dec-11 Jn-12 Fe-12 Mr-12 Apr-12 My-12 Jun-12 Jul-12 Aug-12 Sep-12 Figure 1. The verge numer (men±se) of seled worker rood cells for the 16 colonies monitored for 13 months. thn Vrro (F 1136 =15.21, P =0.0002). However, there were only four colonies remined live or strong enough to smple t this time. There ws significnt negtive correltion etween rood re (cm 2 )ndtropilelps infesttion (r = 0.248; P =0.0007). No correltion etween rood re nd Vrro infesttion ws detected (r =0.023; P =0.752). 25 Tropilelps Only Vrro Only 20 Percentge of infesttion Sep-11 Oct-11 Nov-11 Dec-11 Jn-12 Fe-12 Mr-12 Apr-12 My-12 Jun-12 Jul-12 Aug-12 Sep-12 Figure 2. Prevlence (men±se) of T. mercedese nd V. destructor in worker rood cells of concurrently infested A. mellifer colonies through time.
6 Prevlence nd reproduction of Asin mites in Apis mellifer 783 A seprte exmintion of three concurrently infested colonies showed similr trend. Out of the 1230 worker rood cells exmined, only four cells (0.3 %) were concurrently infested. Tropilelps ws the more predominnt mite species thn Vrro mites in worker rood cells with n verge infesttion of 19.9 % (Tropilelps ) nd 0.7 % (Vrro ). Vrro (2.5 %) infesttion ws numericlly higher thn tht of Tropilelps (1.9 %), nd no concurrent infesttion ws oserved in the drone rood (n =481 cells). Adult ee infesttion ws lso low: Tropilelps = 0.31 % nd Vrro =0.16 %. Proportion of nonreproductive mitesanova reveled significnt mite type (F 1, 13 =15.05; P = ) nd dte of oservtion (F 12, 95 =3.29; P =0.0005), ut no two-wy interction (F 11, 24 = 1.41; P =0.2311) for the proportion of NR foundresses ws detected (Figure 3). Regrdless of mite type, the highest proportion of NR foundresses were oserved in Jnury 2012 nd the lowest NR in Novemer Overll, there were more Vrro mites tht did not reproduce s compred to Tropilelps. Further, oth mites produced similr numer of progeny when oserved in purple-eyed nd tn-odied pupe (Tropilelps =1.48±0.05; Vrro =1.69±0.14 progeny per foundress) (t =0.88, P =0.381) Experiment 2: reproduction of V. destructor nd T. mercedese in deliertely infested worker rood Our results showed tht the reproduction of Tropilelps nd Vrro ws similr in rood cells (n =254 tn-odied pupe) deliertely infested with oth mite species (z =1.84, P <0.01). In ddition, 45 % (criteri 1: Vrro mites hd one dult mle nd dughter, while Tropilelps mites hd t lest one progeny) or 52 % (criteri 2: Vrro or Tropilelp s hd those which produced 1 progeny) supported reproduction of oth mites (Tle I). Only 15 % of the inoculted rood cells hd oth mites tht did not 100 Proportion of non-reproductive foundress c c c c * c c c 0 T. mercedese V. destructor Figure 3. Proportion (men±se) of nonreproductive foundress (did not produce ny progeny) in nturlly infested rood cells. Blck rs indicte the proportions of nonreproductive (NR) foundress regrdless of mite species, gry rs for NR T. mercedese,ndwhite rs for NR V. destructor for ech month of oservtion. Striped rs represent the verge NR for T. mercedese nd V. destructor (infested colonies=16). June ws nonestimle in the mens comprison ecuse of low smple size (infested colonies=4) (sterisk ).
7 784 N. Buwngpong et l. Tle I. Reproduction of T. mercedese (T) nd V. destructor (V) when co-inhiting single host pup (n =254 rood cells tht were deliertely infested). Reproductive sttus Criteri 1 Criteri 2 VNR, TNR 18.1 % (n =46) 15.0 % (n =38) VNR, TR 24.0 % (n =61) 17.3 % (n =44) VR, TNR 13.0 % (n =33) 16.1 % (n =41) VR, TR 44.9 % (n =114) 51.6 % (n =131) Criteri 1 =reproductive Vrro produced dult mle nd young dughter; reproductive Tropilelps hd 1 progeny. Criteri 2 = reproductive Vrro nd Tropilelp s produced 1 progeny R reproductive; NR nonreproductive; VNR, TNR oth V. destructor nd T. mercedese foundress re nonreproductive; VNR, TR V. destructor foundress is nonreproductive ut T. mercedese is reproductive; VR, TNR V. destructor foundress is reproductive ut T. mercedese is nonreproductive; VR, TR foundress of oth mite species re reproductive produce ny progeny. V. destructor produced more progeny per foundress (2.2±0.1) thn did T. mercedese (1.5±0.1) (t =5.31, P <0.0001) in concurrently infested hosts. 4. DISCUSSION V. destructor nd Tropilelps hve een coinfesting A. mellifer colonies for out 50 yers in Asi (Delfindo 1963). Our investigtion demonstrtes tht T. mercedese is competitively superior to V. destructor mites in concurrently infested A. mellifer colonies in Northern Thilnd. The infesttion rtes y oth mite gener fluctuted throughout the study nd showed lmost identicl ptterns. Bsed on our two ssessments, the undnce of Tropilelps thn Vrro oserved in this study greed with previous oservtions stting tht Tropilelps mites outcompete Vrro mites in A. mellifer colonies (Burgett et l. 1983; Pettisetl.2012). However, our oservtion is in contrst to wht hs een shown in South Kore where V. destructor infesttion rtes re greter thn Tropilelps infesttion (Lee et l. 2005). It is lso possile tht the drmticlly different climtic conditions for Kore (temperte) compred to Thilnd (tropicl) re lrgely responsile for this discrepncy in prevlence. For exmple, the environmentl conditions in Pkistn llow continuous rering of rood nd thus survivl of Tropilelps (Wghchoure-Cmphor nd Mrtin 2009). According to these uthors, T. clree (likely referring to T. mercedese sed on species distriution reported y Anderson nd Morgn 2007) infesttions coincide with the increse in rood production (April to My). In our study, we found negtive correltion etween the mount of rood nd Tropilelps infesttion, which corroorted the findings of Kvinseksn et l. (2004)). This decrese in infesttions with the increse in rood production my reflect the Bdilution^ effect oserved in the cse of Acrpis mites (de Guzmn nd Burgett 1991). These uthors explined tht the prsite infesttion rte cnnot increse t the sme rte s the host popultion. The dominnce of Tropilelps over Vrro my lso e influenced y their ility to reproduce. Overll, oth mites produced similr numers of progeny on verge. However, higher proportion of Tropilelps (70 %) thn Vrro (50 %) produced t lest one progeny. This ility to reproduce even just one progeny my increse the popultion of Tropilelps fster thn Vrro mites. Vrro is known to prefer drone rood out three to eight times more thn worker rood (Fuchs nd Lngench 1989). Thus, the overll low infesttion of Vrro mites my e ssocited with the miniml production of drone rood during this study. In contrst, T. clree infests
8 Prevlence nd reproduction of Asin mites in Apis mellifer 785 worker rood out1.5 times more thn drone rood (Woyke 1987). When infesting its indigenous host, A. dorst, T. mercedese did not exhiit host sex preference, i.e., drone nd worker rood experienced similr infesttion rtes (Buwngpong et l. 2013). In this study, only few of the colonies produced drone rood (totl= 506) throughout the experiment. Nevertheless, the infesttion rte of drone rood y Vrro mites ws 3.6 times more thn worker rood. For Tropilelps mites, the infesttion rte of worker rood ws 9.4 times greter thn tht of drone rood. However, we cnnot conclude whether or not Tropilelps prefer worker over drone rood ecuse of limited production of drone rood. The co-infesttion of single host y Tropilelps nd Vrro is rre, n oservtion lso reported y Ritter nd Schneider- Ritter (1988) nd Burgett et l. (1989) with the Acrpis species complex. In generl, insect frss nd its voltile components provide cues in hitt loction (Weiss 2006). In this study, voidnce of n infested cell my e one of the resons for such low mixedgener infesttion. It is possile tht lend of chemicls or voltiles produced y the resident Tropilelps itself or from their feces nd wounds of honey ee hosts deters Vrro mites from invding. For Vrro mites, they sumerge in the lrvl food of L4 lrve fter invsion. Thus, we re unsure if they too re le to produce these voltiles while eing sumerged. It is lso unlikely tht the mites re competing for food or spce since infesttions y oth mites were generlly low nd tht rood ws ville for infesttion. We found tht oth mite species reproduced similrly when introduced together in the sme rood cell. This reproductive fecundity of T. mercedese my contriute to their higher prevlence, n indiction of incresed virulence of this mite species for A. mellifer colonies in Thilnd. Also, possile infections from other pthogens vectored y Tropilelp s, e.g., DWV virus (Dint et l. 2009; Khongphinitunjong et l. 2015), tht cn hve synergistic effects on the overll helth of infested colonies should e of considertion for further studies. ACKNOWLEDGMENTS We cknowledge the Thilnd reserch fund (BRG ), nd the Grdute School of Ching Mi University, Ph.D. Progrm, for finncil support. We lso thnk the Agriculturl Extension nd Development Center, Ching Mi, for providing honey ee colonies nd piry spce. Prévlence et reproduction de Tropilelps mercedese et Vrro destructor dns des colonies d Apis mellifer infestées simultnément Apide / eilles / criens / infesttion simultnée / ondnce sisonnière / Thïlnde Verreitung und Fortpflnzung von Tropilelps mercedese und Vrro destructor in gleichzeitig efllenen Völkern von Apis mellifer Apide / Honigiene / Milen / gleichzeitiger Befll / sisonle Häufigkeit / Thilnd REFERENCES Anderson, D.L., Morgn, M.J. (2007) Genetic nd morphologicl vrition of ee-prsitic Tropilelps mites (Acri: Lelpide ): new nd re-defined species. Exp. Appl. Acrol. 43,1 24 Buwngpong, N., Khongphinitunjong, K., Chntwnnkul, P., Burgett, M. (2013) Tropilelps mercedese : does this honey ee rood mite prsite exhiit sex preference when infesting rood of the dpted host Apis dorst? J. Apic. Res. 52, Burgett, M., Akrtnukul, F., Morse, R.A. (1983) Tropilelps clree : prsite of honey ees in south-est Asi. Bee World 64,25 28 Burgett, D.M., Royce, L.A., Iy, L. (1989) Concurrence of the Acrpis species complex (Acri: Trsonemide ) in commercil honey-ee piry in the Pcific Northwest. Exp. Appl. Acrol. 7, Dint, B., Ken, T., Berthoud, H., Neumnn, P. (2009) The ectoprsitic mite Tropilelps mercedese (Acri: Lelpide ) s vector of honeyee viruses. Insectes Soc 56,40 43 de Guzmn, L.I., Burgett, D.M. (1991) Sesonl undnce of the A. mellifer L. ectoprsites Acrpis dorslis
9 786 N. Buwngpong et l. Morgenthler nd Acrpis externus Morgenthler (Acri: Trsonemide) in Oregon. Bee Sci 1, de Guzmn, L.I., Rinderer, T.E., Frke, A.M. (2007) Growth of Vrro destructor (Acri: Vrroide )popultion in Russin honey ee (Hymenopter: Apide ) colonies. Ann. Entomol. Soc. Am. 100, de Guzmn, L.I., Rinderer, T.E., Frke, A.M. (2008) Comprtive reproduction of Vrro destructor in different types of Russin nd Itlin honey ee coms. Exp. Appl. Acrol. 44, Delfindo, M.D. (1963) The Mites of the honeyee in South Est Asi. J. Apic. Res. 2, Fjrdo Jr., A.C., Cervnci, C.R. (2004) The growth of the Philippine ee industry. Buzz Philippines 4,3 17 Fuchs, S., Lngench, K. (1989) Multiple infesttion of Apis mellifer L. rood cells nd reproduction in Vrro jcosoni Oud. Apidologie 20, Grrido, C., Rosenkrnz, P. (2003) The reproductive progrm of femle Vrro destructor mites is triggered y its host, Apis mellifer. Exp. Appl. Acrol. 31, Kvinseksn, B., Wongsiri, S., de Guzmn, L.I., Rinderer, T.E. (2003) Asence of Tropilelps infesttion from recent swrms of Apis dorst in Thilnd. J. Apic. Res. 42,49 50 Kvinseksn, B., Wongsiri, S., Rinderer, T.E., de Guzmn, L.I. (2004) Comprison of the hygienic ehvior of ARS Russin nd commercil honey ee in Thilnd. Am. Bee J. 144, Khongphinitunjong, K., de Guzmn, L.I., Buwngpong, N., Rinderer, T.E., Frke, A.M., Chntwnnkul, P. (2013) Oservtions on the removl of rood inoculted with Tropilelps mercedese (Mesostigmt: Lelpide ) nd the mite s reproductive success in Apis mellifer colonies. Exp. Appl. Acrol. 62, Khongphinitunjong K, de Guzmn L.I, Trver M, Rinderer TE, Chntwnnkul P (2015) Interctions of Tropilelps mercedese, honey ee viruses, nd immune response in Apis mellifer. J. Apic. Res. In press Kirrne, M.J., de Guzmn, L.I., Rinderer, T.E., Frke, A.M., Wgnitz, J., Wheln, P.M. (2011) Asynchronous development of honey ee host nd Vrro destructor (Mesostigmt:Vrroide ) influences reproductive potentil of mites. J. Econ. Entomol. 104, Lee, M.L., Prk, Y.M., Lee, M.Y., Kim, Y.S., Kim, H.K. (2005) Density distriution of prsitic mites, Vrro destructor Anderson nd Truemn nd Tropilelps clree Delfindo nd Bker on honey ee pupe (Apis mellifer L.) in utumn seson in Kore. Koren JApic.20, Pettis, J.S., Rose, R., Lichtenerg, E.M., Chntwnnkul, P., Buwngpong, N., Somn, W., Sukumlnnd, P., VnEngelsdorp, D. (2012) A rpid survey technique for Tropilelps mite (Mesostigmt: Lelpide ) detection. J. Econ. Entomol. 106, Rinderer, T.E., de Guzmn, L.I., Sylvester, H.A. (2004) Reexmintion of the efficcy of detergent solution for Vrro mite detection. Am Bee J. 144, Ritter W, Schneider-Ritter U (1988) Differences in iology nd mens of controlling Vrro jcosoni nd Tropilelps clree, two novel prsitic mites of Apis mellifer. In: Needhm GR, Pge RE, Delfindo- Bker M, Bowmn CE (eds), Africnized honey ees nd ee mites, New York, pp Rogers, L.E., Gilert, R.O., Burgett, M. (1983) Smpling honeyee colonies for rood production: doule smpling technique. J. Apic. Res. 22, Smmtoro, D., Gerson, U., Needhm, G. (2000) Prsitic mites of honey ees: life history, implictions, nd impct. Annu. Rev. Entomol. 45, Sihg, R.C. (1988) Incidence of Vrro, Euvrro nd Tropilelps mites in the colonies of honey ees Apis mellifer L. in Hryn (Indi). Am Bee J 128, Wghchoure-Cmphor, E.S., Mrtin, S.J. (2009) Popultion chnges of Tropilelps clree mites in Apis mellifer colonies in Pkistn. J. Apic. Res. 48, doi: /ibra Weiss, M.R. (2006) Defection ehviour nd ecology of insects. Annu. Rev. Entomol. 51, Woyke, J. (1987) Length of successive stges in the development of the mite Tropilelps clree in reltion to honeyee rood ge. J. Apic. Res. 26, Woyke, J. (1987) Comprtive popultion dynmics of Tropilelps clree nd Vrro jcosoni mites in honeyees. J. Apic. Res. 26, Woyke, J. (1989) Chnge in shpe of Tropilelps clree femles nd the onset of egg lying. J. Apic. Res. 28,
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