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230 P. Neumann, P.J. Elzen

dried fruits, plant juices, carrion, crops and onflowers (Lin et al., 1992; Fadamiro et al.,1998; Hepburn and Radloff, 1998; Smart and

Blight, 2000; Wolff et al., 2001). The naturalhistory and morphology ofA. tumida weredescribed by Lundie (1940) and Schmolke(1974).

2.1. Pest status and putative life cyclein Africa (Fig. 2)

Here we focus on the life cycle aspects nec-essary to understand and control the beetle.Other features are reported in more detail

elsewhere (Lundie, 1940, 1951, 1952a, b;Schmolke, 1974; Hepburn and Radloff, 1998;Elzen et al., 2000c; Hood, 2000; Pettis andShimanuki, 2000; Flgge, 2001; Neumannet al., 2001a, b; Swart et al., 2001; Ellis et al.,2002b, c, d). In its native range, the small hivebeetle is usually a minor pest only, becausesuccessful reproduction appears most success-ful in weak, stressed colonies or in recentlyabandoned honeybee nests and is far lesscommon in strong colonies (Lundie, 1940;Schmolke, 1974; Hepburn and Radloff, 1998;

Fig. 2). In Africa, the main problems associ-ated with the beetles are in the destruction ofstored bee products (Lundie, 1940; Schmolke,1974; Fig. 2), which most likely result from a

lack of bee populations to guard against repro-duction. However, neither the beekeepingterms weak/stressed vs. strong/unstressed

colonies nor the actual levels of beetle repro-duction in such colonies have been rigorouslyquantified yet. This appears of prime impor-tance to understand the biology ofA. tumida.

Strong African honeybee colonies, even ifheavily infested (Neumann et al., 2001b;Neumann and Hrtel, 2004), can usually pre-vent or postpone successful beetle reproduc-tion (Hepburn and Radloff, 1998; Fig. 2).In such colonies small hive beetles usuallyhave to wait until non-reproductive swarming

(= absconding or migration, Hepburn andRadloff, 1998; see 4.8) leads to recently aban-doned nests (Fig. 2). Massive aggregations ofsmall hive beetles and/or heavy infestationsappear to induce absconding in Africa (Fig. 2).But neither beetle-induced absconding nor thepotential effects of colony movements on lev-els of infestation and parasite population sizesare well understood (see 4.8). This seemshighly relevant because parasite populationsizes may trigger pest severity. The underlyingreasons for the occurrence of beetle aggrega-

tions are also unclear (see 4.9).Host finding (see 4.1) and intrusion into the

colony (see 4.2) are most relevant for the inva-sion process (Fig. 2), but neither the actual

Figure 1. Records of the small hive beetlein Africa (March 2003): 1- South Africa:Walter (1939a, b); Lundie (1940, 1951,1952a, b); May (1969); Anderson et al.(1983); 2- Botswana: Phokedi (1985); 3-Zimbabwe: Mostafa and Williams (2000); 4-Zambia: Clauss (1992); 5- Angola: RosrioNunes and Tordo (1960); 6- Tanzania: Smith(1960); Ntenga (1970); Ntenga and Mugongo(1991); 7- Democratic Republic of Congo:Aurelien (1950); Dubois and Collart (1950);8- Congo Republic: Castagn (1983); 9-Uganda: Roberts (1971); 10- Kenya: Mostafaand Williams (2000); 11- Ethiopia: Mostafaand Williams (2000); 12- Eritrea: Mostafa andWilliams (2000); 13- Central AfricanRepublic: Lepissier (1968); 14- Nigeria:Mutsaers (1991); 15- Ghana: Gorenz (1964);Adjare (1990); 16- Guinea Bissau: Svensson(1984); 17- Senegal: Ndiaye (1974); 18-Egypt: Mostafa and Williams (2000), prob-ably recently introduced (see Chap. 3.2).

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The biology of the small hive beetle 231

cues nor the underlying mechanisms havebeen identified yet. Female beetles oviposit inthe host colonies (see 4.7). The emerging lar-vae (see 4.7) develop until the wandering stageand then leave the nest for pupation in the soil(Fig. 2). While the adults have little impact onthe colony, the larvae can cause severe dam-age to combs (Lundie, 1940; Schmolke, 1974),often resulting in the full structural collapse ofthe nest (Hepburn and Radloff, 1998). Newlyemerged adults invade host colonies, thereby

completing the life cycle ofA. tumida (Fig. 2).In the laboratory, the life cycle can also becompleted on fruits (see 2.2) and in bumblebee colonies (see 5; Fig. 2). However, the level

of reproduction and feeding on fruits in thewild has not been studied, which seems impor-tant to investigate this potential transmissionpathway. Likewise, the ability of small hivebeetles to infest bumble bee colonies in thefield is unknown. This should be investigatedto evaluate the potential impact of small hivebeetles on wild bumble bee populations.

2.2. Alternative food sources

Small hive beetles may use fruits as alterna-tive food sources (Schmolke, 1974; Eischenet al., 1999; Ellis et al., 2002c) in the absenceof honey bee colonies, e.g. following removal

Figure 2. Putative life cycle of the small hive beetle (dotted lines = rare events or unclear; dashed lines anddashed box = colonies of European honeybee subspecies only).

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of colonies in migratory beekeeping (Eischenet al., 1999). Moreover, a complete life cyclecan be achieved on fruits (Ellis et al., 2002c;Fig. 2). However, although larvae develop

normally on avocado, cantaloupe, grapefruitand some other fruit with over 500 beetlesobserved in one cantaloupe (Eischen et al.,1999), the number of offspring per breedingcouple is significantly lower than on bee prod-ucts such as pollen (Ellis et al., 2002c). Fur-thermore, small hive beetles have never beenobserved to reproduce or even feed on fruits inthe field in South Africa (M.F. Johannsmeier,unpublished data). Likewise, there are noreports that small hive beetles are a croppest in Southern Africa (M.F. Johannsmeier,

unpublished data). Therefore, reproduction onfruits appears to be rare if not absent in naturalpopulations. This might be related to the dif-ferent reproductive success on different diets(Ellis et al., 2002c). Although successfulreproduction is in principal possible on otherdiets, small hive beetles should prefer honey-bee colonies whenever possible to maximizetheir reproductive output. However, the actualamount of small hive beetle reproduction onfruits has never been rigorously investigated inthe field. Therefore, we cannot completelyexclude that the presence of an abundant foodsource other than honeybee colonies mayserve as a refuge for the small hive beetle andas a source of further infestations.

3. CURRENT DISTRIBUTION, PESTSTATUS AND PUTATIVE LIFECYCLE IN POPULATIONSOF EUROPEAN HONEYBEES

3.1. Current distribution and peststatus in the USA

The first confirmed detection of small hivebeetles in the US was in St. Lucie, Florida inJune 1998, as identified by the Florida Depart-ment of Agriculture and Consumer Services(Hood, 2000; Sanford, 2002). Earlier, uniden-tified specimen were collected in Charleston,South Carolina, in November 1996 (Hood,

1999a). The introduction of the small hivebeetle into the USA was thought to have beenthrough South Carolina and from there toGeorgia and Florida (Hood, 2000). Since then,the small hive beetle has extended its rangefrom 18 states by the end of 2001 (Hood,2001), over 25 states in April 2002 (Evanset al., 2003), to 29 states in March 2003(Fig. 3). This rapid spread is likely to resultfrom natural range expansion and movementof infested honeybee colonies, migratory bee-keeping, package bees and beekeeping equip-

ment (Delaplane, 1998). Mt-DNA sequenceanalyses of the small hive beetle from the USand South Africa indicate that the populationson both continents belong to a single species,

Figure 3. Current distribution of the smallhive beetle in the USA (March 2003; J. Pettis[USDA], unpublished data). It has beenreported in 29 states so far (year reported inbrackets): 1- Florida (1998), 2- South Caro-lina (1998), 3- Georgia (1998), 4- NorthCarolina (1998), 5- New Jersey (1999), 6-Maine (1999), 7- Pennsylvania (1999), 8-Minnesota (1999), 9- Iowa (1999), 10- Wis-consin (1999), 11- Massachusetts (1999),12- Ohio (1999), 13- Michigan (1999), 14-Louisiana (2000), 15- New York (2000), 16-North Dakota (2000), 17- Tennessee (2000),18- Indiana (2000), 19- Vermont (2000), 20-

Maryland (2001), 21- Virginia (2001), 22-Delaware (2001), 23- Illinois (2001), 24-Missouri (2001), 25- Mississippi (2001),26- Arkansas (2002), 27- Alabama (2002),28- Kentucky (2002), 29- W. Virginia(2003); dark area = severe damage.

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although it is not clear whether a single or mul-tiple introductions occurred (Evans et al.,2000, 2003). Even strong colonies of Euro-pean honeybee subspecies can be taken over

and killed by small hive beetles in the US(Sanford, 1998; Elzen et al., 1999a, b). Thestate most severely affected by the small hivebeetle has been Florida (Elzen et al., 2002;Fig. 3) and the damage to local apiculture canbe serious (Elzen et al., 2000b). Indeed, onlyin 1998 in Florida losses were estimated to bein excess of $3 million (Ellis et al., 2002c).

3.2. Current distribution and peststatus in Australia and Egypt

In July 2002 beetle damage was noticed ina nucleus colony in New South Wales (M.Duncan, unpublished data). The beetles wereidentified asA. tumida in October 2002 (Ani-mal Health Australia, 2003). In March 2003,the small hive beetle is still fairly restrictedin its occurrence (D. Anderson [CSIRO], M.Beekman, P. Boland [Biosecurity Australia],L. Cook [NSW Agriculture] and M. Duncan,unpublished data; Fig. 4). At present, the beetleis causing no noticeable losses (D. Anderson

[CSIRO], unpublished data). In contrast to theUS, strong colonies dont collapse with the bee-tle (D. Anderson [CSIRO], M. Duncan, unpub-lished data).

In Egypt, small hive beetles were firstdetected in Etaie Al-Baroud (~110 km North-West of Cairo) in Summer 2000 (Mostafa andWilliams, 2000). Since then, the small hive

beetle was also found in other apiaries alongthe Nile Delta (A.M. Mostafa, unpublisheddata). A. tumida is probably not endemic toEgypt (H.R. Hepburn, A.M. Mostafa andB. Schricker, personal communications). Inorder to clarify whether the small hive beetle isnative to Egypt or has been introduced, itseems necessary to investigate its distributionin upper Egypt, which is more close to its sub-Saharan endemic region (Fig. 1). At present,reports on the small hive beetle in both Aus-tralia and Egypt are largely anecdotal andmore detailed studies are urgently required.

3.3. Putative life cycle in coloniesof European honeybees (Fig. 2)

There seems to be two differences in theputative life cycle of small hive beetles incolonies of European honeybee subspecies inthe US (Fig. 2).

3.3.1. Overwintering capacity (Fig. 2)

European honeybee subspecies form a win-ter cluster in colder climates to survive longerperiods of cold weather conditions (Gates,1914; Corkins, 1930), a behaviour which is not

Figure 4. Current distribution of the smallhive beetle in Australia (March 2003;shaded areas and arrow = small hive beetleinfestations; picture courtesy of P. Boland,modified).

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expressed in African subspecies (Hepburn andRadloff, 1998). Despite its tropical origin,adult small hive beetles can overwinter withinsuch clusters (Elzen et al., 1999a; Hood,2000), where >300 beetles have been reportedin small clusters (Pettis and Shimanuki, 2000).This is quite surprising, even in light of lowaggression levels by the European bees (Elzenet al., 2001). It seems as if small hive beetleshave adapted to temperate climates by exploit-ing the cluster behaviour of European subspe-cies. Thus, although 12 C for 24 hours isreported to kill all life stages of the beetle(Hood, 1999b), it is obvious that small hive

beetles are able to survive in colder climatesand have the potential to establish populationsacross a significant part of the US (Evanset al., 2003). Indeed, there are establishedbeetle populations as far North as Ohio(Evans et al., 2003). More detailed studies arerequired to understand how small hive beetlescan survive in the winter clusters. However,the establishment of beetle populations alonecannot explain the severe effects of infesta-tions in US honeybee populations.

3.3.2. Life history short-cut (Fig. 2)In contrast to African subspecies, even

strong colonies of European honeybee subspe-cies can be taken over and killed by small hivebeetles in the US (Sanford, 1998; Elzen et al.,1999a, b; Fig. 2). Weakened and stressed col-onies may even succumb within two weeks(Wenning, 2001). Thus, successful reproduc-tion of the parasite seems to be more commonin strong European colonies in the US (Fig. 2).It seems as if small hive beetles in European

colonies in the US do not have to wait forrecently abandoned nests or for favourabletime windows (see Mutsaers, 1991). This con-stitutes a short-cut in the life history enablingsuccessful reproduction more often than inAfrican host populations.

What are the underlying reasons for such alife history short-cut? It might well be thatEuropean honeybee subspecies lack behav-ioural resistance mechanisms and therefore thesmall hive beetle is a serious threat. Indeed,the presence of large numbers of small hivebeetles in African honeybee colonies does notsignificantly affect adult bee populations,brood area and foraging behaviour althoughsmall hive beetle presence significantly low-

ered all of these variables in European colo-nies (Ellis et al., 2003a). This indicates thatbehavioural characteristics are important tounderstand resistance towards small hive bee-tle infestations. In the following chapters wewill address such behaviours in detail.

4. BEHAVIOURAL INTERACTIONSBETWEEN HOST AND PARASITE

4.1. Host finding (Fig. 2)

Adult small hive beetles are active flyers(Elzen et al., 1999b, 2000c) and individuals oroccasionally swarms (Tribe, 2000) can infest

honeybee colonies. It has been stated (Wenning,2001), that small hive beetles can detect colo-nies under stress, e.g. due to disease or man-agement techniques such as splitting, and thatthey are able to detect such colonies from adistance of about 1316 km. Detection ofstressed colonies might be adaptive in Africa,where reproduction is more likely in such col-onies than in unstressed ones (Hepburn andRadloff, 1998). However, the actual mecha-nism which might allow small hive beetles to

detect stressed colonies over large distances isunclear (see 4.9). Baited trap studies show thata combination of honey/pollen and adult beesis highly attractive to flying beetles, whereasadult bees alone are less attractive and brood,hive products and infested combs alone are notattractive (Elzen et al., 1999b). This indicatesthat an intact honeybee colony with food stor-age is most likely the preferred breeding placeof small hive beetles.

4.2. Host intrusion (Fig. 2)

Honeybee colonies have highly specializedguard bees, that carefully scrutinize incomingindividuals (Ribbands, 1953). However, theadult beetles can intrude strong honeybeecolonies as well as weak ones with equalimpunity (Lundie, 1940). Nevertheless, fewerbeetles intruded into colonies with reducedentrances (Ellis et al., 2002a), suggesting thatguard bees are capable of preventing intrusionat least to some degree. Beekeeping activitiessuch as frequent inspections appear to facili-tate beetle intrusion into host colonies. Somecolonies have been reported to collapse afterbeekeepers have united them with otherhighly-infested supers (Sanford, 2002).

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4.3. Aggression towards adult beetles

4.3.1. Host tactics

A. m. scutellata andA. m. capensis protectthemselves by active aggression towards boththe adults and larvae (Lundie, 1940; Elzenet al., 2001; Neumann et al., 2001b). The beestry to bite or sting the adults but usually withonly little success (Lundie, 1940; Elzen et al.,2001; Neumann et al., 2001b; Swart et al.,2001). In the few cases, when the adult beetlesare decapitated (Neumann et al., 2001b) orextremities are removed (Schmolke, 1974),they are thrown out of the hive (Lundie,

1952b). Observations that small hive beetlescan live for long periods of time even in strongcolonies with relative impunity (Lundie, 1940)also suggest that aggression is not very effec-tive in killing the beetles. This may be partlydue to the hard exoskeleton (Lundie, 1940) butalso due to the following defence tactics of theadult beetles.

4.3.2. Parasite tactics

4.3.2.1. Defence posture

When attacked, the adults can perform aturtle-like defence posture (Lundie, 1940;Schmolke, 1974; Neumann et al., 2001b).While exhibiting this defence posture the beetlestays motionless and tucks its head underneaththe pronotum with the legs and antennaepressed tightly to the body (much like with-drawal in a turtle, Neumann et al., 2001b).

4.3.2.2.Running

Beetles usually move very quickly out ofthe range of bees (Schmolke, 1974; Neumannet al., 2001b).

4.3.2.3.Dropping

The beetles can deliberately drop from thecombs to escape pursuit (Schmolke, 1974).

4.3.2.4.Hiding

Inside of the nest cavity, the adults typicallyhide in small cracks (Schmolke, 1974; Neumannet al., 2001b), under the bottom board ofcommercial hives (Lundie, 1940) or in cells(Schmolke, 1974; personal observations). While

hiding in cells, small hive beetles usuallystay motionless at the bottom (Lundie, 1940;Schmolke, 1974). When field colonies areinspected, the adult beetles are often seen mov-ing from one hiding place to another one nearby(Lundie, 1940; Swart et al., 2001). This alsohappens on a regular basis in observation hives(Neumann et al., 2001b).

Nevertheless, although aggression is notvery effective in killing the beetles, it maycontribute to resistance. African honeybeesshow significantly more investigative contactand aggression behaviour to the adults thanEuropean ones (Elzen et al., 2001). About 1/3

of all encounters between African bees andadult beetles resulted in attacks by the work-ers, whereas this was only 1.4% in Europeanbees (Elzen et al., 2001). Therefore, the adultbeetles are probably under constant harass-ment in an African colony, which may mini-mize beetle reproduction.

4.4. Social encapsulation

4.4.1. Host tactics

Sometimes the bees succeed in corralling(Elzen et al., 2000a, b) or herding (Swartet al., 2001) the adult beetles into specific cor-ners, preventing them from moving freely overthe combs. When such beetles are corralled, orwhen they actively hide in small gaps(Schmolke, 1974; Neumann et al., 2001b),they are often encapsulated in propolis con-finements (A. m. scutellata: Hepburn andRadloff, 1998;A. m. capensis:Neumann et al.,

2001b; Solbrig, 2001; Ellis et al., 2003b). Thisis not an artefact of observation hives becausesocial encapsulation also occurs in normalfield colonies (Neumann et al., 2001b). Cor-ralling behaviour has never been observed infield colonies or natural nests. While it seemslogically to assume that corralling occursbecause it is a necessary part of social encap-sulation, its occurrence can only bee inferredat this point.

During the encapsulation process, workersadd propolis around detected hidden or cor-

ralled beetles and completely encapsulatemost of them (Neumann et al., 2001b). Thebees have a sophisticated tactic for limitingbeetle escape during encapsulation (Neumann

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et al., 2001b). While some workers add propo-lis, one or more others continuously guard thebeetles in both open and closed confinementsday and night for up to 57 days (Neumannet al., 2001b). The guard workers continuouslyattack the beetles when they move to the edgesof still open confinements and thus keep themimprisoned (Neumann et al., 2001b). Socialencapsulation may be an additional factor forpreventing or postponing successful reproduc-tion of the parasite.

However, social encapsulation also occursin susceptible European honeybee subspecies(Ellis et al., 2003c). Because the use of propolis

is more abundant in African subspecies com-pared to European ones (Hepburn and Radloff,1998) social encapsulation may be more effi-cient and/or more common in African honey-bee colonies. Indeed, the number of confine-ments per colony and encapsulated beetles inthese prisons were both lower in European col-onies (Ellis et al., 2003c) than in African ones(Neumann et al., 2001b). Moreover, Europeanhoneybees guard prisons significantly longerthan Cape honeybees (Ellis et al., 2003b).However, the underlying reasons for this or itseffect on beetle survival and/or colony per-formance are unknown. African bees are moreaggressive towards the small hive beetle (Elzenet al., 2001). Therefore, African prison guardsmay be more efficient in preventing beetleescape (Neumann et al., 2001b). Clearly, moredetailed studies are necessary to evaluate towhat extent social encapsulation triggers resist-ance towards small hive beetle infestations.


Some beetles manage to escape encapsula-tion at night (Neumann et al., 2001b), possiblybecause honeybees are generally less active atnight (Moritz and Kryger, 1994). Matings inprisons and cannibalism among small hivebeetles were also observed (Neumann et al.,2001b), which might enhance their survival inlarge prisons. Despite no access to food in thecombs, imprisoned beetles may survive for twomonths or longer (Neumann et al., 2001b).However, their survival is not due to metabolic

reserves, because starved beetles die within afortnight (Flgge, 2001; Ellis et al., 2002c).The beetles approach the prison guard bees,extend their heads towards and make antennal

contact with the bees thus mimicking normalhoneybee trophallaxis (Korst and Velthuis,1982). Often workers respond with aggression,so it may take several attempts before the beesregurgitate food (Ellis et al., 2002d). Thus,long term survival of small hive beetles in pris-ons is probably also derived from behaviouralmimicry (Ellis et al., 2002d).

4.5. Patrolling

Despite frequent searching, only few smallhive beetles can be seen on the combs ofstrong colonies (Schmolke, 1974). This indi-

cates that such colonies are able to preventsmall hive beetle intrusion in the comb area atleast to some degree by guarding this area.This comb guarding behaviour (= patrolling;Swart et al., 2001) seems to be more efficientin strong colonies due to the higher density ofbees in the nest (Lundie, 1952b; Swart et al.,2001). Lundie (1952a) stated: Any factorwhich so reduces the ratio of the population ofa colony of bees to its comb surface that thebees are no longer able to protect the combsurface adequately is a precursor to the rav-ages of both the wax moth and Aethina tum-ida. The patrolling behaviour seems particu-larly well expressed in the brood area of thecolony (Schmolke, 1974; Solbrig, 2001) butless well expressed in the outer frames andhoney supers (personal observations). Thismight explain, why adult beetles may ovipositon outer frames and why larvae can appear onthem after transport to the honey house. Itappears as if the host becomes alerted bynewly intruded beetles (Schmolke, 1974). We

conclude that protection of the combs viapatrolling/high bee density might contribute toresistance. However, this potential impactneeds to be investigated in future studies.

4.6. Worker aggregation and cellcontent removal

When beetles manage to intrude into thecomb area and hide in cells, African workersrapidly aggregate around them (S. Hrteland P. Neumann, unpublished data; W.R.E.

Hoffmann, unpublished data). Then, the work-ers remove the contents of nearby honey, pollenand brood cells to get access to the hidden bee-tles (Schmolke, 1974; personal observations).

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The bees get extremely agitated until the smallhive beetle is finally removed from the combarea (personal observations) or deliberatelyshows the dropping behaviour (Schmolke,1974). This behaviour may minimize smallhive beetle oviposition on the combs.

4.7. Removal of small hive beetle eggsand larvae


Female beetles oviposit in batches or irreg-ular clutches (Lundie, 1940; Schmolke, 1974)

of up to 210 eggs (mean = 14 20 eggs; S.Hrtel and P. Neumann, unpublished data)throughout the hive, but seem to prefer smallgaps and the bottom of cells (Lundie, 1940;Schmolke, 1974). At initial stages of infesta-tion, when no larvae are present, females sig-nificantly oviposit in cracks rather than on thecombs (S. Hrtel and P. Neumann, unpublisheddata). Nevertheless, females can also ovipositon the combs, because super frames of infestedcolonies quickly show larvae after transport tothe honey house (Lundie, 1940). On the combsoviposition seems to preferentially occur inpollen cells (>30 small larvae per cell; Lundie,1940), probably because reproductive successcan be very high on a pollen diet alone (Elliset al., 2002c). The number of eggs laid perfemale is high in the first 24 hours after infes-tation (69 15 eggs; S. Hrtel and P. Neumann,unpublished data). Schmolke (1974) estimatedabout 1000 eggs per female in a three to fourmonth period, after which oviposition declines.Oviposition of many eggs in gaps appears

adaptive because survival chances for the off-spring are enhanced (Neumann and Hrtel,2004).

4.7.2. Host tactics

4.7.2.1.Eggs

It has been reported that African workers doremove small hive beetle eggs (Swart et al.,2001). This removal was recently studied inA. m. scutellata field colonies (Neumann andHrtel, 2004) by introduction of unprotectedand protected eggs (laid in gaps). Whereasall unprotected eggs were removed within24 hours, 66% of the protected eggs remained.

This indicates that unprotected eggs are effi-ciently removed but also shows that eggs laidin gaps are likely to hatch (Neumann andHrtel, 2004).

4.7.2.2. Larvae (jettisoning behaviour)

Bees which get hold of a larvae can carry itout of the hive at some distance (~20 meters;Lundie, 1940; Schmolke, 1974). Sometimesthere is a tug-of-war between two jettisoningworkers tearing apart one larvae and resultingin both bees carrying out of the hive what theyare holding (Schmolke, 1974). This jettisoning

behaviour seems to be efficient (Lundie,1952b) because all introduced larvae wereremoved within 24 hours in an observationhive study (Schmolke, 1974). Likewise, alllarvae (N = 700) introduced into seven A. m.scutellata field colonies were ejected within24 hours (Neumann and Hrtel, 2004). Fieldobservations also indicate that larvae are effi-ciently ejected by jettisoning workers (Lundie,1940; Swart et al., 2001).

African workers respond quickly to thepresence of small hive beetle offspring

because 72% of the non-protected eggs and49% of the larvae were removed within onehour after introduction (Neumann and Hrtel,2004; see also Schmolke, 1974). The removalwas not correlated with colony phenotypes(size, amount of open and sealed brood, pollenand honey area; Neumann and Hrtel, 2004).However, Neumann and Hrtel (2004) onlystudied relatively strong, unstressed colonies.Thus, these studies should be repeated withweak/stressed colonies. We conclude that

removal behaviour plays an important role forthe apparent resistance of African honeybees.However, it is unknown to what extent Euro-pean bees remove small hive beetle eggs andlarvae. Because prevention of beetle reproduc-tion seems crucial, this behaviour should bemore deeply investigated in the future.

4.8. Colony mobility: abscondingand migration

African honeybee subspecies are much

more mobile compared to European bees(Hepburn and Radloff, 1998). One can distin-guish between two forms of non-reproductiveswarming (Hepburn and Radloff, 1998).

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population sizes between the endemic and newranges.

Although absconding is rare in Europeanbees (Ruttner, 1986), it is also induced ininfested European colonies (Ellis et al., 2003a).Because African subspecies are more prone toabsconding than European bees (Hepburn andRadloff, 1998), another reason for better smallhive beetle resistance/less pest severity may bethat African bees are somehow more efficientin preparation for absconding and/or respondearlier with nest abandonment. We recommendmore detailed studies on the effects of abscond-ing and seasonal migration in future studies.

4.9. Small hive beetle aggregationpheromone?

Long range host finding of adults (Wenning,2001) requires efficient cues. Furthermore,small hive beetle swarms can be occasionallyobserved in South Africa (Tribe, 2000). Mas-sive aggregations of adult small hive beetlesprior to the absconding of such heavilyinfested colonies can be found in Africa

(Neumann et al., 2001b; Neumann and Hrtel,2004) and in the US (Elzen et al., 2002; Elliset al., 2003a). In European honey bee hives,A. tumida infestations may consist of as manyas 1000 adults and several hundred larvae perhive (Elzen et al., 1999b). In a single A. m.scutellata colony 491 adult beetles were found(Neumann and Hrtel, 2004), while all othercolonies at the same apiary show low infesta-tion levels (N = 7 colonies; mean infestationlevel = 14 12 beetles; S. Hrtel and P.Neumann, unpublished data). These colonies

with large numbers of beetles are neither par-ticularly weak nor have massive food stores(Neumann et al., 2001b), indicating that cuesother than simple host colony size and foodstores are responsible for their attractiveness.Indeed, aggregation pheromones have beendescribed for a variety of Nitidulidae speciesand are widely used as control agents (Petroskiet al., 1994; James et al., 2000). Such pherom-ones are produced by exceptional large spe-cialized cells within the body cavity of nitid-ulid beetles (Nardi et al., 1996). We consider itvery likely that a similar pheromone plays arole for long range host finding and aggrega-tions of small hive beetles. Observations thatmales tend to infest before females (Elzen

et al., 2000c) indicate that the aggregationpheromone might be male produced as inCarpophilus obsoletus and is attractive toboth sexes (Petroski et al., 1994). Synergisticeffects between food odours and aggregationpheromones for attracting small hive beetlemight also play a role as shown for Car-pophilus lugubris (Lin et al., 1992). However,in another nitidulid beetle, Prostephanus trun-catus, the absence of upwind flight to foodvolatiles, or any synergism between pherom-one and food volatiles suggests that themale-produced pheromone is the only knownsemiochemical for long-range host finding

(Fadamiro et al., 1998). More research isneeded to identify and evaluate the potentialimpact of different compounds such as aggre-gation pheromones, food volatiles, or any syn-ergism between pheromone and food volatileson the short and long-range dispersal and hostselection ofA. tumida.

5. ALTERNATIVE HOSTS (FIG. 2)

Bumblebees do not occur in sub-SaharanAfrica but are native to North America(Michener, 2000). Recent laboratory studiesindicate that a host shift ofA. tumida to bum-blebees may occur in its new range (Stanghelliniet al., 2000; Ambrose et al., 2000). Bumblebeecolonies,Bombus impatiens, artificially infestedwith small hive beetles had fewer live bees,more dead adult bees and greater combdamage than controls (Stanghellini et al., 2000;Ambrose et al., 2000). The bees did not showany aggression either towards the adult beetlesor to the larvae (Stanghellini et al., 2000), indi-cating a lack of behavioural resistance. How-ever, nest defence of bumblebees against smallintruders has been described and speciesvary in their reactions (Michener, 1974). Forexample, B. atratus (Sakagami et al., 1967;Sakagami, 1976) and B. (Robustobombus)melaleucus (Hoffmann et al., 2004) tend to bemore aggressive than other species.

Small intruders are stung and carried out-side by bumblebee workers (Michener, 1974)

similar to the jettisoning behaviour of honey-bees (Lundie, 1940; Schmolke, 1974). Moreo-ver, social encapsulation of small intruders inwax or propolis confinements has also been

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described (Michener, 1974), but it is notknown whether live intruders are also encap-sulated. Colony defensiveness seems to becorrelated with colony size, with smaller colo-nies being less defensive (Michener, 1974).Therefore, there might be considerable vari-ance between bumblebee species and nestsalso with respect to small hive beetle resist-ance. More detailed studies on a variety of spe-cies and on a range of colony sizes are requiredto evaluate the susceptibility of bumblebeestowards small hive beetle infestations.

Nevertheless, a new generation of smallhive beetle was produced from adult to adult in

each of theB. impatiens units which were heldon soil (Stanghellini et al., 2000; Ambroseet al., 2000). Therefore, small hive beetles arein principle able to complete an entire lifecycle in association with bumblebees. How-ever, it is unclear whether adult beetles areable to find bumblebee colonies in the wild.We suggest bait trap studies (Elzen et al.,2000c) and studies of adjacent honeybee andbumblebee colonies (Whitfield and Cameron,1993) to evaluate whether bumblebee colonies

are attractive for adult beetles.

6. DISCUSSION

The introduction ofA. tumida in areas as farfrom its endemic range as North America andAustralia illustrates the high anthropogenictransportation potential of this parasite. How-ever, it appears difficult to trace back theactual transport mechanism into specific areas,

especially if introduction is only detected aftersecondary spread. The small hive beetle isthought to have been transported to the USAaboard ship in 1996 (Wenning, 2001), becauseit first appeared near a major harbour (Hood,2000). Successful alternate feeding on fruitssuggests that the beetles may be transported onfruits (Ellis et al., 2002c). However, fruit ship-ments are usually subject to intensive quaran-tine and small hive beetles have not yet beendetected in such shipments. It seems plausibleto assume that the import of package bees,

honeybee and bumblebee colonies, queens,hive equipment and or even soil (Brown et al.,2002) constitute potential invasion pathwaysof the small hive beetle. Nevertheless, at the

current state of evidence it is still unclear howsmall hive beetles actually reached Australiaand the US. The migratory nature of beekeep-ing is probably the greatest contributor ofsmall hive beetle transmission within its newranges (US: Delaplane, 1998; Australia: M.Duncan, personal communication). Neverthe-less, natural dispersal mechanisms may alsoconsiderably contribute. Thus, the small hivebeetle most likely constitutes an example of abiological invasion that involves multiple dis-persal processes such as long-range transport,migratory beekeeping and natural dispersalabilities. The pattern of small hive beetle

spread is probably dominated by long-distancejump dispersal as in Argentine ants (Suarezet al., 2001). Detailed data and comparativestudies on the invasion dynamics in the newranges seem necessary to evaluate the contri-bution of individual processes to the spread ofA. tumida and to improve the predictive powerof future modelling efforts. Such studies arehowever still lacking.

The environmental requirements of thesmall hive beetle are readily met within a largerange of the distribution ofA. mellifera both interms of survival and completion of its lifecycle (Brown et al., 2002). Indeed, small hivebeetles can establish populations in temperateregions (e.g. Ohio, Evans et al., 2003) due totheir overwintering capacity. The requirementfor lighter sandy soils during pupation can alsobe met within many areas (Brown et al., 2002).Thus, it is likely that, if introduced, the smallhive beetle would swiftly become establishedin most of the range of the Western honeybeewith major implications for apiculture. Also,

the ability of small hive beetles to heavilyinfest the protected environment of honeyhouses may allow severe economic damage inany location worldwide.

A variety of control methods has beendeveloped and discussed (e.g. Baxter et al.,1999; Ellis et al., 2002a; Elzen et al., 1999b;Hood, 1999b, 2000; Lafrniere, 2000; Mostafaand Williams, 2000; Park et al., 2002 amongothers). They range from prevention throughsanitation in apiaries and honey houses (Tho-mas, 1998), over trapping of larvae using flu-

orescent lights and adult beetles using nucleushives (Sanford, 1998; Elzen et al., 1999b) tochemical control in the hive (Elzen et al., 1999b)and insecticide treatment of soil (Baxter et al.,

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1999; Lafrniere, 2000). However, as in thecase of Varroa destructor Trueman andAnderson, resistant strains may develop(Spreafico et al., 2001). Thus, the develop-ment of sustainable control methods seemsdesirable to avoid resistance to chemical treat-ments in the long run (e.g. pheromone trap-ping, biological control agents or breeding ofresistant strains). In general, small hive beetlecontrol should not overlook the control ofother honeybee pests and vice versa. Forexample, grease/antibiotic patties used to con-trol American foulbrood seem to worsen smallhive beetle infestations because larvae readily

accept the patties as food (Westervelt et al.,2001; Elzen et al., 2002).

The development of efficient control meth-ods is likely for managed honeybees sooner orlater, but appears difficult for wild bee popula-tions. Thus, once established, small hive bee-tles may also pose a serious threat to wild beepopulations with potential drastic ecologicalconsequences. Several nitidulid species have aclose association with social insects other thanhoneybees (Morse, 1998), e.g. Lundie (1940),reported aboutBrachypeplus species (B. auti-tus, B. planus, and B. meyricki) associatedwith stingless bees of the genus Trigona.Given that bumblebees may actually serve asan alternative host in nature and resistance islow (Stanghellini et al., 2000; Ambrose et al.,2000), small hive beetles may cause severedamage to bumblebee populations. Other beespecies may also serve as alternative hosts(e.g.Apis cerana). Indeed, the reciprocal hostshift of parasitic V. destructor mites fromA. cerana toA. mellifera has already proven to

cause a global problem for apiculture and wildA. mellifera populations. However, there aredifferences when comparing V. destructorandthe small hive beetle. In case ofV. destructoran interspecific host shift has occurredbetween two species showing clear differencesin their behaviour (e.g. hygienic behaviour)and nesting biology (e.g. drone cell construc-tion). In case of the small hive beetle anintraspecific host shift has occurred betweensympatric and non-sympatric host subspecies.Thus, rather quantitative differences seem to

trigger resistance to this parasite (see Elzenet al., 2001) and breeding programs towardsresistance may be more rewarding than in thecase ofV. destructor.

Several potential reasons may be responsi-ble for the difference between pest severity inAfrica, in the US and in Australia.

6.1. Different beekeeping techniques

There are differences in beekeeping prac-tices which may contribute to the damagecaused by the small hive beetle. For example,African beekeepers tend to minimize theamount of honey stored in hives. However, nocomparative data is available yet.

6.2. Differences between introducedsmall hive beetle populations

The Australian small hive beetle populationsseem to be genetically different from those inthe US and so may not cause the same prob-lems as in the US (D. Anderson, unpublisheddata). In this case one might expect a differentbeetle behaviour and/or reproductive potentialin the US and Australia. Against this, smallhive beetle behaviour appears to be very simi-lar in the US and in Africa (Elzen et al.,2000b). Moreover, the small hive beetlesfound in North America are genetically verysimilar to beetles from Southern Africa (Evanset al., 2003). Thus, differences between beetlepopulations may explain divergent pest sever-ity between Australia and the US but notbetween the US and Africa. However, detailedcomparative studies on the behaviour and/orreproductive potential of small hive beetles inAfrica and its new ranges are lacking.

6.3. Enemy release hypothesis

Invasive species such as the small hive bee-tle might have escaped from important para-sites, predators or pathogens that limit popula-tions in their native ranges (Keane andCrawley, 2002) and release from such enemieshas been implicated in the success of invasivespecies (Huffaker and Messenger, 1997).Indeed, an average invasive species has moreparasites in its native region than in the new

range (Torchin et al., 2003). This point isentirely unclear because neither small hivebeetle parasites nor pathogens have beenfound yet.

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6.4. Climatic differences

The number of beetle generations per year

in temperate regions is likely to be smallerthan in South Africa (five generations; Lundie,1940) because temperature has an effect onbeetle developmental time (Schmolke, 1974;Neumann et al., 2001a). Thus, pest severitymay be less too due to smaller beetle popula-tion sizes (see 6.6. below). However, this hasnot been investigated yet. Very dry conditionsmay also limit beetle reproduction in its newranges (Australia: M. Duncan, personal com-munication; Egypt: A.M. Mostafa, personal

communication). Thus, similar to Africa,where successful reproduction of the smallhive beetle can be enhanced by hot and humidconditions (Swart et al., 2001), climatic differ-ences may play a key role in damage becausesmall hive beetle population growth is smaller(see 6.6. below). This point may explain dif-ferences in pest severity between the US andAustralia/Egypt but not between the US andAfrica. However, the underlying reasons arestill unclear and need further investigation.

6.5. Different strains of honeybees

Differences in African vs. European honey-bee subspecies are numerous (see above).Therefore, we regard it as most likely that thisis the major factor contributing to the differentimpact of small hive beetles on populations ofAfrican honeybees in Africa and Europeanhoneybees in the US. However, the bees whichare apparently less affected in Australia areA. m. ligustica (M. Duncan, personal commu-

nication), one of the predominant subspeciesin the US (Schiff and Sheppard, 1995). Unlessthere are differences between Australian andUSA. m. ligustica strains with respect to bee-tle resistance, this points in the direction thatother factors are important for the apparentdifferences in beetle damage between Aus-tralia and the US.

In the US, the invasion of the Africanizedhoneybee may prove to be an advantage atleast with regard to small hive beetle resist-ance because Africanized bees are likely to be

resistant towards the small hive beetle. How-ever, to our knowledge, the small hive beetle isnot yet found in South America. Thus, Afri-canized bees have not encountered this para-

site since their introduction to South Americain 1956 (Kerr, 1957) and some resistancemight have been lost.

Managed European honeybee populationsare under strong selection pressures due tointense breeding over the past centuries. Traitssuch as absconding, aggression and abundantpropolis usage have been selected against,which are undesirable from a beekeeping per-spective but may trigger small hive beetleresistance. Therefore, the low resistance ofmanaged European honeybees may not neces-sarily reflect actual susceptibility of wild Euro-pean honeybee populations. It is possible

that the susceptibility of managed Europeanhoneybees in the US, is a result of efficientbreeding efforts in the past. This hypothesisremains to be tested with feral/wild colonies ofEuropean honeybee subspecies.

6.6. Different densities of small hivebeetle populations

One potential reason, why Australia havehad little small hive beetle damage so far,might be that it has only been there longenough to establish moderate numbers ofadults in hives (M. Duncan, personal commu-nication). So, it might well be that the beetlepopulations will need some time to build up toa certain size before serious damage occurs(D. Anderson [CSIRO], M. Duncan, personalcommunications). In this case one mightexpect more severe problems in Australia inthe nearby future when small hive beetle pop-ulations have build up. The higher mobilityof African bees, in particular seasonal migra-

tion (see above), may also contribute tosmaller parasite population sizes and conse-quent minor pest severity in Africa.

We conclude that at the current state of evi-dence it appears premature to decide which ofthese factors is important for the differencesbetween beetle damage in the US and Australia.However, the differences between the US andAfrica most likely result from behavioural dif-ferences between African and European sub-species, unless massive host shifts occur in thenew range or unless important small hive beetlepests/parasites have not been identified yet.The known behaviours, which are probablyinvolved in small hive beetle resistance of Afri-can bees, such as absconding (Hepburn et al.,

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1999), aggression (Elzen et al., 2001) andsocial encapsulation (Neumann et al., 2001b)also occur in susceptible populations of Euro-pean honeybees (Ellis et al., 2003a, b, c).Therefore, it is obvious that the susceptibilityof European bees is not due to a lack of behav-ioural resistance mechanisms. Resistance ofAfrican bees is probably due to quantitative dif-ferences in a series of behaviours such asabsconding, aggression, removal of beetle eggsand larvae and social encapsulation. It is likelythat general adaptations to higher predation andparasite loads are responsible for the apparentresistance of African honeybees rather than

specific adaptations towards the small hivebeetle. For example, African bees are in generalmore aggressive than European subspecies(Hepburn and Radloff, 1998). However, manyof the behavioural mechanisms have only beenqualitatively described, have not been testedin comparative studies between African andEuropean bees or may even simply be unknown.Moreover, very important basic features likethe number of beetle offspring per colony in theUS and Africa and levels of infestation of Afri-can and European host populations have notbeen rigorously quantified yet. Therefore, morecomparative studies between parasite and hostpopulations in Africa, Australia and in the USare urgently required. In general, we still havea fragmentary knowledge of the small hive bee-tle, creating demand for more research in allareas of its biology. Joint research efforts of thescientific community seem necessary in thenearby future, becauseA. tumida has the poten-tial to become a serious global problem for api-culture and natural bee populations.

ACKNOWLEDGEMENTS

We wish to thank S. Hrtel, H.R. Hepburn, F.B.Kraus, H.M.G. Lattorff, R.F.A. Moritz, S. Schneider,H. Schlns and S. Spiewok for stimulating discus-sions and/or valuable comments on earlier versionsof the manuscript. M. Beekman, L. Cook, S. Hrtel,H.R. Hepburn, M.F. Johannsmeier and B. Schrickerprovided unpublished information. We are particu-larly grateful to D. Anderson, P. Boland, M. Duncan,A.M. Mostafa and J. Pettis for detailed updates on

the current small hive beetle situation in Australia,Egypt and in the US. Special thanks to P. Boland forkindly providing Figure 4. Financial support wasgranted by an Emmy Nther fellowship of the DFGto P. Neumann.

Rsum Biologie du Petit Coloptre des ruches(Aethina tumida, Coleoptera : Nitidulidae) : lacu-nes dans nos connaissances sur cette espce inva-

sive. Le Petit Coloptre des ruches (PCR), parasiterelativement anodin des abeilles domestiques afri-caines, est indigne en Afrique sud-saharienne(Fig. 1). Dans son aire naturelle de rpartition lareproduction du PCR se limite principalement auxcolonies faibles ou malades et aux nids rcemmentabandonns. (Fig. 2). Il est par contre capable de sereproduire dans des colonies europennes fortes(Fig. 2) et peut alors causer de gros dgts dans lespopulations des sous-espces europennes, commecest le cas par exemple aux tats-Unis depuis 1998(Fig. 3). Il a mme t trouv en gypte (2000) et enAustralie (2002, Fig. 4). En Australie les dgts sem-blent jusqu prsent limits, mais les raisons de cettat de fait restent obscures. Le PCR peut hivernerdans le grappe dabeilles et donc stablir sous deslatitudes de climat tempr. Il peut utiliser les fruitscomme source alternative de nourriture , ce qui nat pourtant ce jour montr quau laboratoire. Larsistance des abeilles africaines linfestation parle PCR repose probablement sur des diffrencesquantitatives dans de nombreux types de comporte-ments, tels que lagression, llimination des ufs etdes larves du coloptre, lencapsulation socialeainsi que lessaimage non li la reproduction. LePCR prsente une gamme de contre-mesures tellesque se laisser tomber du rayon, senfuir, se cacher,

prendre des postures de dfense et mimer la trophal-laxie. Mais de nombreux mcanismes de dfense nesont pas encore suffisamment tudis. Le PCR sepropage avec efficacit (cf. son extension aux tats-Unis, Fig. 3) et est susceptible dutiliser dans les nou-velles rgions des htes alternatifs (par ex. les bour-dons en Amrique du Nord). Il a donc le potentielde devenir un problme global pour lapiculture etles populations naturelles dabeilles. Nos connais-sances actuelles tant encore trs restreintes, il sem-ble donc ncessaire de mener dautres tudescomparatives sur les populations de petits colopt-res des ruches et dabeilles domestiques en Afrique,en Australie et aux USA.

Apis mellifera / Aethina tumida / espce invasive /Petit Coloptre des ruches

Zusammenfassung Die Biologie des kleinenBeutenkfers (Aethina tumida, Coleoptera: Niti-dulidae): Unsere Wissenslcken ber eine inva-sive Art. Der kleine Beutenkfer ist ein relativharmloser Parasit afrikanischer Honigbienen, der inAfrika sdlich der Sahara heimisch ist (Abb. 1). Imnatrlichen Verbreitungsgebiet ist die erfolgreicheVermehrung des Kfers meist auf schwache oder

kranke Vlker und krzlich verlassene Nester be-schrnkt (Abb. 2). Im Gegensatz dazu kann sich derKfer auch in starken europischen Vlkern erfolg-reich vermehren (Abb. 2). Er kann daher groeSchden in Populationen europischer Unterarten

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verursachen, wie z.B. seit 1998 in den USA (Abb. 3).Der kleine Beutenkfer wurde ebenfalls in gypten(2000) und Australien (2002, Abb. 4) gefunden. In

Australien scheinen die Schden bisher nur geringzu sein. Die Grnde hierfr sind jedoch bislangunklar. Der Beutenkfer kann in der Wintertraubeberwintern und somit in gemigten Breiten Popu-lationen etablieren. Frchte knnen als alternativeNahrung dienen, was jedoch bisher nur in Laborver-suchen gezeigt werden konnte. Die Resistenz afri-kanischer Bienen gegenber Infektionen mit demBeutenkfer beruht vermutlich auf quantitativenUnterschieden in mehreren Verhaltensweisen, wiez.B. Aggression, Entfernen von Eiern und Larvendes Kfers, soziale Einkapselung sowie nicht repro-duktivem Schwrmen. Die Kfer zeigen eine Reihevon Gegenmanahmen wie z.B. Fallenlassen vonder Wabe, Flchten, Verstecken, Verteidigungshal-tung und trophallaktische Mimikry. Jedoch sindviele Resistenzmechanismen noch nicht ausrei-chend untersucht worden. Der kleine Beutenkfer isteffizient in der Verbreitung (s. Ausbreitung in denUSA, Abb. 3) und kann mglicherweise auch alter-native Wirte in den neuen Verbreitungsgebieten nut-zen (z.B. Hummeln in Nordamerika). Von daher hatder kleine Beutenkfer das Potential, ein globalesProblem fr die Imkerei und natrliche Bienenpo-pulationen zu werden. Jedoch ist unser bisherigesWissen ber diesen Parasiten noch sehr gering.Weitere vergleichende Untersuchungen an Kfer-

und Bienenpopulationen in Afrika, Australien undden USA erscheinen daher dringend notwendig.

Apis mellifera /Aethina tumida / Honigbiene /invasive Art / kleiner Beutenkfer

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