morfometria de varroa

8/3/2019 morfometria de varroa

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Original article

Varroa destructor infestation impact on Apis melliferacarnica capped worker brood production, bee

population and honey storage in a Mediterranean climate

Antnio Manuel MURILHAS*

Instituto de Cincias Agrrias Mediterrnicas, Universidade de vora, 7000 vora, Portugal

(Received 15 June 2001; revised 20 December 2001; accepted 2 January 2002)

Abstract This study investigated the impact ofVarroa destructorinfestation on the amount ofcapped worker brood, the adult bee population and honey production of authenticated Apis melliferacarnica colonies kept in a Mediterranean climate. For this purpose, colonies were set-up and eithermaintained mite-free or artificially mite-infested and allowed to develop an infestation. Periodicalevaluations of those colonies unravelled the pattern of the previously mentioned variables across theseason, and allowed for comparative numerical analyses. Progressive reductions on the amount ofcapped worker brood, bee population and honey storage in mite-infested colonies only became in-creasingly evidentduring spring and summer, apparently associated with impressive mite populationincreases. By theendof theexperiment,mite-infested colonies showeda unitary averagereductionof45% in the amount of capped honey theystored, meaning an average annual loss of 24kgofhoney

percolony.However,theamountofcappedhoneystoredperbeeanddaywasfoundtobeindependentfrom colony V. destructorstatus, indicating a lack of direct effect of mite infestation on honey hoard-ing behaviour.

Varroa destructor /Apis mellifera /population dynamics / honey production

1. INTRODUCTION

Since Varroa destructor Anderson &Trueman (Anderson and Trueman, 2000)was first found in Portugal, in 1987(Belchior, 1996), it has been associatedwith both increased honey bee colony mor-

tality and decreased honey production.However, this is the first study quantifyingthe impact ofV. destructor infestation oncapped worker brood, bee population andhoney production of honey bee colonies inPortugal. Studies of this nature, conductedin a single environment (Bchler, 1992,

271

Apidologie 33 (2002) 271281 INRA/DIB-AGIB/EDP Sciences, 2002DOI: 10.1051/apido:2002013

* Correspondence and reprintsE-mail: [email protected]


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1994) and covering an entire annual colonycycle (Echazarreta and Paxton, 1997), havebeen rare.

In temperate climates, the general pat-tern of colony growth throughout the yearhas been well described (Jeffree, 1955;Seeley, 1984; Winston, 1987). However,theuninterruptedpresence of brood (exceptperhaps for a short period associated withswarming) in Mediterranean climates(Vieira et al., 1990; Puerta et al., 1993;Ferrer-Dufol et al., 1994; Calatayud andVerdu, 1995; Branco et al., 1999) is a majorqualitative difference to that pattern. The

milder winter conditions in Mediterraneanclimates and the availability of food duringaconsiderablepartofthewinteraccountforthis difference in the brood-rearing cycle,which, in turn, is relevant to the intrinsicgrowth rate ofV. destructor. Thus, the pur-pose of this study was to investigate the rel-ative impact of mite infestation on cappedworker brood, bee population and, particu-larly, on honey production of honey beecolonies kept in a common Mediterranean

environment.

2. MATERIALS AND METHODS

2.1. Colony establishmentand management

Field work was started in July 1992 andranuntillateAugust1993.Atthebeginning

of this experiment, 12 young (less than twomonth old) mated queens designated by theseller as Apis mellifera carnica Pollmannwere imported from the USA. All queenswere wing-clipped, colour coded and intro-duced into 1 kg ( 50 g) packages ofA. m. iberica Goetze workers, which hadbeen previously treated with Folbex VA(bromopropylate). After queen introduc-tion, these packages of bees were kept infive-frame Langstroth hives and receivedsix litres of sucrose solution (50%, w/v)during the four weeks after colony set-up

(which occurred during early May). InJune, these colonies were moved into10 frame Langstroth hives and allowed todevelop for approximately eight weeks, so

that the progeny of the introduced queenscould replace most of the initial Apismellifera iberica workers [before beingevaluated (mid July)]. By this time, sevenhoney bee colonies existed. They were keptat the Research Station of vora University(southern Portugal; N38o34, W07o54)and were all morphometrically authenti-cated, based upon standards provided bythe Institut fr Bienenkunde (Oberursel,Germany), as A. m. carnica (Graa, 1996).

Thisverifiedthattheintroducedqueenshadreplaced most of the initial A. m. ibericaworkers with their own offspring.

Colony management was conservative,meaning that no strategies or managementtechniques were followed to improve col-ony productivity or population growth. Themajor concern was to prevent swarmingduring the spring, mainly by making areasof honey storage and egg laying space

(drawn comb) available approximately twoweeks before it was probably needed.

No prophylactic or therapeutic actionswere carried out, other than the one appliedto colonies intended to be mite-free. Also,no feeding was carried out during the ex-perimental period and no honey was re-moved from the experimental colonies.

2.2. Artificial V. destructor infestation

Three colonies were randomly selectedto be kept virtually mite-free (control colo-nies, hereafterreferred tobynon-infestedcolonies), while the remaining four colo-nies were artificially infested with V. de-structor (treatment colonies, hereafterreferred to as infested colonies).

To ensure comparable initial infestationlevels (in relative terms), the number ofmites received by each infested colonyranged from 50 to 102 (77.0 13.4,

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x s.e.m.) and was kept proportional(2.91 0.003%) to the area of cappedworker brood (cm2) that these colonies hadat that time(mid July, 11707 2028 capped

worker brood cells).V. destructorindividuals were collected

from honey bees of highly mite-infestedcolonies (by dusting with powdered sugar)and pooled together before being randomlydistributed to experimental colonies previ-ously selected to be artificially infested.Only dark-brown motile mites were se-lected for artificial infestation. They wereintroduced into colonies at sunset, onto

frames with open and capped worker brood.The few individual mites (1.14 0.40) thatfell onto hives bottom boards overnightwere recovered on next day early morningand replaced by equal numbers of mites atsunset time.

2.3. Maintenance of non-infestedcolonies

Non-infested colonies were continu-ously treated with two strips of Apistan

(Fluvalinate, 800 mg per strip) to kill mostincoming mites before they could start re-producing (Milani et al., 1993). Apistan

strips were replaced approximately everyeight weeks, according to manufacturersinstructions.

2.4. Data collection

Data were collected on (i) areas ofcapped worker and, if existent, dronebrood; (ii) honey bee colony population es-timatesand(iii)areasofcappedhoney.Col-onies were assessed approximately everythree weeks (except during the months ofNovember, December and January).

All comb areas occupied with brood orcapped honey were drawn onto transparentacetate sheets and were later digitized bycomputer assisted image analysis. All mea-sured areas, of a given type, in every colony

frame,were added perexperimental colonyand observation date.

Conversion of measuredareas of cappedbrood, into number of capped brood cells,

were achieved by using the factors of 2.90and 4.42 brood cells cm2, for drone andworker brood respectively. A colonys adultpopulationwas roughly estimated by visualcomparison of each frame occupied withhoney bees with a set of eight calibratedphotographs (Jeffree, 1951). Evaluationswere always made by the same observer inearly morning or late afternoon, when mostof the forager bees were expected to be in

the hive. The aim of this methodology wasto gain an approximation to adult bee popu-lations, with a view to comparing amongcolonies.

In assessing the amount of honey storedin colonies, only areas of operculatedhoney were considered. Because bothbrood nest boxes and honey supers were ofthe same type and filled with ten frameseach, variation in comb depths was reducedand randomly distributed between mite sta-tus.Bystudyingeightsamples(twoperboxtype and mite status) of 25 cm2 each ofcappedhoneyandfullydrawnemptycomb,itwasconcludedthateachcm2 of registeredcapped honey held 1.79 0.06 g of honey.Honey hoarding behaviour (daily honeygainperbee)wascalculatedbasedonanes-timated mean adult population at the mid-point between to consecutive observationdates, assuming linear population varia-

tions between observation dates.Also, to follow the population dynamics

ofV. destructorwithout interfering exces-sively with mite population growth orhoney bee colony development, samples ofcapped worker brood and adult honey beeswere also collected on 15.07.92 (controlsampling carried just before artificial infes-tation), 01.11.92, 26.02.93, 20.05.93 and28.07.93. As far as capped drone brood wasconcerned, samples were only collected on20.05.93, whenmostexperimentalcolonieshad sufficient capped drone brood to be

Varroa destructorinfestation impact on worker brood, bee population and honey storage 273


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assessed without interfering excessivelywith drone production. These samples al-lowedtheassessmentofapparentmite infes-tation levels of capped brood and of adult

honey bees (Pappas and Thrasyvoulou,1988).Thetotalmitepopulationinallexper-imental colonies were then obtained, acrossall sampling dates, by adding up the esti-mated numbers of mites in capped (workerand drone) brood and on adult bees.

Lossofbeesbyswarmingwasappraisedby checking for the presence of the youngcolour-coded queensduring theregularvis-itstothecolonies.Wherelossofqueensoc-

curred (either by swarming, supersedure oraccident), colonies were removed from theexperiment.

2.5. Statistical analyses

Assumptions inherent to parametric sta-tistics, namely variables independent nor-mal distributions of errors (with a mean ofzero andconstant variance) andexperimen-tal group (mite status) homoscedasticity(Fry, 1993), were confirmed before carry-ing out statistical tests. Levels of cappedworker brood in the colony, adult popula-tions, amounts of capped honey and honeyhoarding behaviour were analysed by atwo-way repeated-measures analysis ofvariance (repeated-measure ANOVA),where (i) honey bee colonies representedthe subjects upon which measures were re-peated, (ii) mite status was the between-

subject effect and (iii) the observation datewas the within-subjects effect.

3. RESULTS

When colonies were first assessed (midJuly),no significant differences were foundin te rms o f capped worker b rood(F[1,5] < 0.001, P = 0.995), honey bee col-ony population (F

[1,5]= 0.038, P = 0.853),

or capped honey (F[1,5] = 0.037, P = 0.856)that could be associated with mite status.

Although no V. destructor were foundestablished in brood or on adult bees ofnon-infested colonies, these colonies re-ceived 0.8 0.2 invading mites day1,

throughout most of the experiment. A ma-jor increase (21 6 mites day1) in V. de-structor infestation pressure occurredduring the second half of December 1992,apparently related with robbing of collaps-ing mite-infested colonies. Across the ex-periment, non-infested colonies received atotal number of 414 16 incoming mites.

In infested colonies, mean increases ofapproximately 1344% in established mite

populations were observed within 195 daysafter artificial infestation (late February1993).Coloniesmeanmite population wasthen 1083 131 (Fig. 1), corresponding todaily finite rates of mite population in-crease (Calatayud and Verdu, 1993) of1.0138. On middle May 1993, infested col-onies hosted an average absolute peak of9616 3877 V. destructor, decreasing inmite population (7505 854) towards lateJuly 1993 (Fig. 1). This corresponds to an

overall experimental daily finite rate ofmite population increase of 1.0123.

Compared with non-infested colonies,only moderated capped worker brood andhoney bee population growths wereachieved by infested colonies, particularlythroughout spring and summer 1993(Fig. 1). Considering all estimates of beecolony populations carried out across theexperiment, statistically significant differ-

ences were associated with both mite status(F[1,5] = 36.73, P = 0.002) and its interactionwith observation date (F[12,60] = 11.24,P < 0.001). Mite infested colonies only be-came significantly associated with reducedcolony populations from April onwards. Aslower accumulation of honey stores wasobserved in infested colonies (Fig. 2). In-deed,a repeated-measure ANOVA revealedstatistically significant differences in theamounts of capped honey related to bothmite status (F[1,5] = 72.42, P < 0.001) andits interaction with observation date

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Figure 1. Adult bee populations, capped worker brood cells and Varroa destructorpopulations.

Figure 2. Capped honey and mean honey reduction associated with Varroa destructorinfestation.


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(F[12,60] = 9.83, P < 0.001). Again, an asso-

ciation between mite infested colonies andlower amounts of capped honey only be-came statistically significant from Aprilonwards. Althoughtheinfested coloniesar-rived at the end of the experiment with only45.2% ( 20 kg) of the capped honeystored in non-infested ones ( 44 kg), adirect effect of mite infestation on honeyhoarding behaviour was not observed(Fig. 3), neither through the whole experi-ment ( repeated-measure ANOVA;

F[1,5] = 3.35, P = 0.14) nor across the last sixobservation dates (repeated-measureANOVA; F[1,5] = 2.52, P = 0.19), whenhigher colony honey gains were observed.

4. DISCUSSION

This study meant to look into the impactof V. destructor infestation on cappedworker brood, bee population and, particu-larly, on honey production of honey beecolonies maintained in a common Mediter-

ranean environment. Considering that all

colonies entered this experiment in similarconditions, the results obtained are essen-tially related to the interaction betweenmite population growth and their host col-ony development, rather than with largesources ofuncontrolledinitial variation.Onthe other hand, non-infested colonies wereprobably weakened by the negative effectof repeated fluvalinate applications(Barbattini et al., 1989; Slabezki et al.,1991; Liu, 1992), meaning that the magni-

tude of the differences between non-in-fested and infested colonies may have beenunderestimated. Considering the entireexperimental period, thedaily finite rates ofmite population increase were slightlylower (1.0123) than the ones also obtainedin Mediterranean conditions by Kraus andPage [(1995);1.0137 to 1.0214],CalatayudandVerd [(1993, 1995); 1.021 to 1.027] orBranco et al. [(1999); 1.0189 to 1.0347].These differences may have arisen fromenvironmental [e.g. geographical location,honey bee colony management or mite

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Figure 3. Mean amount of capped honey stored per bee and day.


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immigration rates (Branco et al., 1999;DelaplaneandHood,1999)]orgenetic(beestrain) variations.

Continuous increases in V. destructorpopulations in infested colonies were ob-served up to the penultimate observation,decreasing afterwards towards the last ob-servation date (as colonies were collaps-ing). Some of the reasons that can partlyexplain this fact [also mentioned by Brancoet al. (1999)] include limitations imposedby host conditions upon mite reproductionand survival rates and, eventually, a consid-erable increase in desertion of highly mite-

infested adult honey bees (that may occurmuchmorefrequentlyintheterminalphaseofV. destructorinfestation). Thisfeed-backmechanismofhostterminalconditioninre-stricting mite population growth has beenignored by relevant models of mite popula-tion dynamics (Fries et al., 1994; Fries,1996; Martin, 1998). Furthermore, the ob-served pattern ofV. destructorpopulationdynamics is incongruent with the exponen-tial growth / decay cycles hypothesised to

occur in A. mellifera colonies in temperateclimates (Fries et al., 1994; Fries, 1996). InMediterranean climates, there are no suchsuccessive cycles and most acaricide-un-treated mite-infested colonies can be ex-pected to die within approximately oneyear after becoming infested (Calatayudand Verd, 1992; Rinderer et al., 1993;Murilhas, 1994; Branco et al., 1999).

The particularly rapid increase in V. de-structorpopulations in honey bee coloniesinMediterraneanclimates,morethanbeingcaused by fast mite population growth dur-ing the summer [even in cold climates, thenumberofmitescanincreaseupto100timesduring one summer (Fries et al., 1991)],seems to be determined by the lack of a pe-riod of non-reproduction and high mitelosses associated with clustered broodlesscolony overwintering (Korpela et al.,1992). It is known that, in temperate cli-mates, a large proportion of mites [ran-domly distributed among honey bees in

broodless overwintering colonies (Ritteret al., 1989)], die over winter along withnumerous adu lt bees (Kovac andCrailsheim, 1987; Fries et al., 1991; Fries

and Perez-Escala, 2001). In regions withcold winters, at least a 50% reduction in acolonys honey bee population can be ex-pected to occur during winter (Avitabile,1978) and one can therefore expect that, inthese conditions, approximately half theVarroa destructor individuals will also dieover winter. This situation does not happenin Mediterranean climates and thus thehoney bee colony life cycle places fewer re-straints on mite population growth before

colonies approach collapse (Branco et al.,1999). Under such a context, infested colo-nies tended to hold considerably less cappedworker brood, to be significantly less popu-lous (from lower egg laying rates, higherbrood mortality or shorter mean life expec-tancies) and to store less honey than non-in-fested ones (particularly during spring andsummer).However,aneffectofV. destructorinfestation on honey hoarding behaviour

was eithernon-existent or insignificant.Thissuggests that mites do not directly interferewith average variations in the amounts ofhoney daily stored perbee, independently ofthe over-riding indirect effect it plays(through colony adult bee population reduc-tions)on colony foraging potential. The rea-sons for thismay be related with the fact thatsevere mite infestations frequently lead ei-ther to the death of individuals or to an in-creased probability for them to become

detached from their colonies earlier (by ex-pulsion, predation or disorientation). In thiscase, V. destructor infestations can induceconsiderable colony population reductionswithout directly interfering with the honeyhoarding behaviour of its remaining popula-tion. On the other hand, in low to moderatemite infestations, many of the parasitizedworkers survive long enough to forage fortheir colonies. In this case, Schneider andDrescher (1987) reported decreases in sur-vival rate of bees beyond 25 days, propor-tionally related to the level of infestation



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they suffered during their immature stagesandparticularlyduring late summer(DeJongand De Jong, 1983; Kovac and Crailsheim,1988; Moretto et al., 1991). Nevertheless,

no firm relationship has been demonstratedbetween the level ofmiteparasitismand themean life expectancy of a bee. Somegroupsof severely infested workers may show longmean life expectancies and equal foragingcapacity (in terms of frequency and meantime of flight duration) compared with non-infested workers of the same colony (Kovacand Crailsheim, 1988). As Ball (1994)pointed out, this suggests that the level ofmite infestation is not the only (and perhaps

not the primary)cause contributing to the re-duction of life expectancies ofV. destructor infested workers. Factors such as climate,forage availability, season of the year, andthe presence and level of secondary infec-tions may all interact and contribute deci-sively to theoutcomeof infested individuals.Apparently, colony effects of all these indi-vidual outcomes should have been relevanttoexplainwhynodirecteffectwasfoundbe-

tween colony mite status and the amount ofcapped honey they stored per bee per day.

ACKNOWLEDGEMENTS

I wish to acknowledge the funding supportgiven to this work by the Portuguese Fundao

para a Cincia e Tecnologia, as well as all thefacilities made available by both the Institutode Cincias Agrrias Mediterrnicas and theUniversidade de vora.

Rsum Impact de linfestation parVarroa destructor sur la production decouvain douvrires opercul, la popula-tion dabeilles et les rserves en miel chezApis mellifera carnica en climat mditer-ranen. En climat mditerranen, lesconditions hivernales douces et la possibili-t de rcolter de la nourriture durant unegrande partiede lhiver expliquentque lac-tivit dlevage du couvain soit permanentedanslescoloniesdabeilles,cequienretour

autorise un taux de croissance intrinsquelev des populations de lacarien Varroadestructor. Dans ce contexte ltude visait rechercher limpact de linfestation par

lacarien sur la quantit de couvain opercu-l, la populationdabeilles adultes et la pro-duction de miel chez des colonies dApismellifera carnica authentifies et levesen climat mditerranen typique (N38o34,W07o54). Pour ce faire, des colonies ontt tablies et soit maintenues indemnes deV. destructor, soit artificiellement infestespar lacarien avec dveloppement libre delinfestation. Des valuations priodiquesontclairci les relations entre le dveloppe-

ment de la colonie, le couvain opercul, lapopulation dabeilles adultes et les provi-sions de miel selon la saison et permis desanalyses numriques comparatives. Toutesles colonies exprimentales ont montr undroulement dans le temps semblable avecun fort accroissement des variables tu-dies seulement en dbut du printemps(Fig. 1). Simultanment les colonies infes-tes ont vu des rductions croissantes du

couvain douvrires opercul, de la popula-tion dabeilles et de la production de mielaucoursduprintempsetdeltparrapportaux colonies non infestes (Figs. 1 et 2).Ces rductions taient apparemment asso-cies des augmentations impressionnan-tes de la population dacariens dans cescoloniesl(Fig.1).Alafindelexprience,les colonies infestes par V. destructorpr-sentaientdes rserves de miel diminues enmoyenne de 45 % (Fig. 2), ce qui corres-

pond une perte annuelle de 24 kg de mielpar colonie, par rapport aux 44 kg engran-gs par les colonies non infestes. Nan-moins la quantit de miel opercul stockpar abeille et par jour tait indpendante deltat dinfestation de la colonie (Fig. 3).Ceci indique que linfestation par V. des-tructorna pas deffet direct sur le compor-tement damassement du miel.

Varroa destructor / Apis mellifera /dynamique des populations / rendementen miel

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Zusammenfassung Auswirkungen desBefalls durch Varroa destructor auf dieProduktion vonverdeckelterArbeiterin-nenbrut, Bienenpopulation und Honig-

vorrat bei Apis mellifera carnica imMittelmeerklima. Die milderen Winterbe-dingungen des Mittelmeerklimas und dieMglichkeit, whrend eines erheblichenTeils des Winters Futterquellen zu besam-meln bedingt eine durchgehende Brutttig-keit derBienenvlker, diewiederum fr diehoheintrinsische Wachstumsrate der Popu-lationen von Varroa destructor in diesenGegenden verantwortlich zu machen ist. Indiesem Zusammenhang war es das Ziel der

vorliegenden Untersuchung, die Auswir-kung des Milbenbefalls auf die Menge ver-decke l ter Arbe i ter innenbru t , d iePopulation adulter Arbeiterinnen und dieHonigproduktion in authentisierten A. m.carnica Vlkern zu erfassen, die in einemtypischen Mittelmeerklima gehalten wur-den (N38o34, W07o54). Hierzu wurdenVlker aufgestellt und entweder milbenfreigehalten oder knstlichmitMilbeninfiziert

und die Entwicklung einer Milbenpopulati-on zugelassen. In regelmigen Zeitab-schnitten wiederholte Untersuchungenzeigten das Muster der VolksentwicklunginBezugaufverdeckelteBrut,diePopulati-on adulter Bienen und Honigvorrte berdie Saison und ermglichten eine numeri-sche Analyse. Alle Versuchsvlker zeigteneinen hnlichen zeitlichen Verlauf, whren-dessen nur im frhen Frhjahr ein starkerZuwachs der Untersuchungsvariablen zu

beobachten war (Abb. 1).Gleichzeitigwur-den bei den varroabefallenen Vlkern imVergleich zu den unbefallenen Vlkernwhrend des Frhjahres und Sommers zu-nehmende Einschrnkungen bei verdeckel-ter Arbeiterinnenbrut, Bienenpopulationund Honigvorrten beobachtet (Abb. 1 and2). Augenscheinlich waren diese mit ein-drucksvollen Zuwchsen der Milbenpopu-lationen in diesen Vlkern verbunden(Abb. 1). Zu Ende des Experiments zeigtendie milbeninfizierten Vlker eine gleichm-igeReduktion von 45 % bei den Honigvor-

rten (Abb. 2), was einem jhrlichen Verlustvon 24 kg Honig im Vergleich zu den 44 kgHonig in nichtinfizierten Vlkern ent-spricht. Nichtsdestoweniger war die Menge

von Honig pro Bienen und Tag unabhngigvon dem Befallstatus des Volkes (Abb. 3),was darauf hindeutet, dass es keinen direk-ten Effekt des Befalls durch Varroa destruc-torauf das Honigeintragverhalten gibt.

Varroa destructor / Apis mellifera /Populationsdynamik / Honigproduktion

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