ArticlePDF Available

Potential host shift of the small hive beetle (Aethina tumida) to bumblebee colonies (Bombus impatiens)

Authors:
  • Pinkernells Whisky Market Salzburg, Austria

Abstract and Figures

Here we explored the potential for host shift from honeybee, Apis mellifera, colonies to bumblebee, Bombus impatiens, colonies by the small hive beetle, a nest parasite/scavenger native to sub-Saharan Africa. We investigated small hive beetle host choice, bumblebee colony defence as well as individual defensive behaviour of honeybee and bumblebee workers. Our findings show that in its new range in North America, bumblebees are potential alternate hosts for the small hive beetle. We found that small hive beetles do invade bumblebee colonies and readily oviposit there. Honeybee colonies are not preferred over bumblebee colonies. But even though bumblebees lack a co-evolutionary history with the small hive beetle, they are able to defend their colonies against this nest intruder by removal of beetle eggs and larvae and stinging of the latter. Hence, the observed behavioural mechanisms must be part of a generalistic defence system suitable for defence against multiple attackers. Nevertheless, there are quantitative (worker force) and qualitative differences (hygienic behaviour) between A. mellifera and B. impatiens.
Content may be subject to copyright.
Research article
Potential host shift of the small hive beetle (Aethina tumida) to bumblebee
colonies (Bombus impatiens)
D. Hoffmann1, J. S. Pettis2and P. Neumann3,4,5
1Department of Zoology, Martin-Luther-Universitt Halle-Wittenberg, Hoher Weg 4, 06099 Halle (Saale), Germany,
e-mail: dorothee.hoffmann@googlemail.com
2USDA-ARS Bee Research Laboratory, Bldg. 476 BARC-E, Beltsville, MD 20705, USA
3Swiss Bee Research Centre, Agroscope Liebefeld-Posieux Research Station ALP, CH-3003 Bern, Switzerland
4Department of Zoology and Entomology, Rhodes University, Grahamstown 6140, South Africa
5Eastern Bee Research Institute of Yunnan Agricultural University, Heilongtan, Kunming, Yunnan Province, China
Received 16 July 2007; revised 16 January 2008; accepted 17 January 2008.
Published Online First 4 February 2008
Abstract. Here we explored the potential for host shift
from honeybee, Apis mellifera, colonies to bumblebee,
Bombus impatiens, colonies by the small hive beetle, a
nest parasite/scavenger native to sub-Saharan Africa. We
investigated small hive beetle host choice, bumblebee
colony defence as well as individual defensive behaviour
of honeybee and bumblebee workers. Our findings show
that in its new range in North America, bumblebees are
potential alternate hosts for the small hive beetle. We
found that small hive beetles do invade bumblebee
colonies and readily oviposit there. Honeybee colonies
are not preferred over bumblebee colonies. But even
though bumblebees lack a co-evolutionary history with
the small hive beetle, they are able to defend their
colonies against this nest intruder by removal of beetle
eggs and larvae and stinging of the latter. Hence, the
observed behavioural mechanisms must be part of a
generalistic defence system suitable for defence against
multiple attackers. Nevertheless, there are quantitative
(worker force) and qualitative differences (hygienic
behaviour) between A. mellifera and B. impatiens.
Keywords: Aethina tumida, bumblebees, host shift, in-
vasive species, parasites.
Introduction
As global travel and transportation of goods increases,
biological invasions are happening more and more
frequently (Mooney and Cleland, 2001; Levine and
DAntonio, 2003; Cassey et al. , 2005). Introduced patho-
gens and parasites may switch hosts, thus posing new
threats to native species. Due to their lack of co-evolu-
tionary history, these new hosts do not possess any
specific defence mechanisms against the new pest, having
to rely entirely on generalistic means, which may or may
not provide them sufficient resistance.
The small hive beetle, Aethina tumida, may be such an
invasive parasite. It is native to sub-Saharan Africa,
where it is a parasite and scavenger of honeybee, Apis
mellifera, colonies (Lundie, 1940; Schmolke, 1974; Hep-
burn and Radloff, 1998; Neumann and Elzen, 2004).
During the past decade the small hive beetle has been
introduced into several countries around the world
(Elzen et al., 1999; Mostafa and Williams, 2002; Animal
Health Australia, 2003; Ritter, 2004 ; Clay, 2006). In North
America and Australia the beetle has become well
established (Evans et al., 2003; Hood, 2004; Neumann
and Elzen, 2004; Spiewok et al., 2007), and its spread in
these new ranges has been facilitated by the managed and
feral populations of European honeybees. European
honeybee subspecies, themselves not native to the New
World and Australia (Goulson, 2003a; Moritz et al.,
2005), appear to be more susceptible to small hive beetles
than African ones, i.e. they suffer greater damage from
beetle infestations and colonies collapse more often
(Elzen et al., 1999, 2000), thus enhancing beetle repro-
duction. However, while honeybee colonies constitute a
good resource for the small hive beetle, switching to
alternate hosts would be a survival strategy where
beehives are less abundant or temporarily unavailable
(e.g. when hives have been moved by beekeepers).
Recent evidence suggests that the small hive beetle
may be less host specific than previously thought. It has
Insect. Soc. 55 (2008) 153 –162
0020-1812/08/020153-10
DOI 10.1007/s00040-008-0982-9
 Birkhuser Verlag, Basel, 2008
Insectes Sociaux
been found to naturally infest commercial bumblebee
colonies in the field in North America (Bombus impa-
tiens, Spiewok and Neumann, 2006a). Moreover, the
beetle can successfully reproduce in laboratory B. impa-
tiens colonies (Stanghellini et al., 2000; Ambrose et al.,
2000) as well as in managed hives of Australian stingless
bees (R.B. Luttrell, pers. comm.).
Studies with honeybees demonstrated that a mixture
of odour cues from bees and hive products are attractive
to small hive beetles (Elzen et al. , 1999, 2000; Suazo et al. ,
2003; Torto et al., 2005). Since hive products such as wax,
honey, pollen and brood, along with bees, can also be
found in bumblebee and stingless bee colonies (Dollin,
1996; Michener, 2000), they are not unlikely to attract the
beetles. Indeed, Spiewok and Neumann (2006a) showed
that small hive beetles are attracted by bumblebee
workers and bumblebee-collected pollen. The similarities
between honeybee and bumblebee colonies also allow
other macroparasites of the Apidae, as for instance the
greater wax moth, Galleria mellonella, and the bumble-
bee wax moth, Aphomia sociella, to switch between
Bombus and Apis hosts (Williams, 1997). As studies on
small hive beetle rearing revealed, the actual foodstuffs
on which the adults and larvae feed do not have to be very
specific, as long as they contain sufficient proteins for egg
production and larval growth (Ellis et al., 2002).
A range of different behavioural defence strategies
against the small hive beetle have been documented in
honeybees: social encapsulation (Neumann et al., 2001a;
Ellis et al., 2003a, 2004a), removal of beetle eggs (Ellis et
al., 2003b, 2004b; Neumann and Hrtel, 2004; Spiewok
and Neumann, 2006b) and larvae (jettisoning behaviour:
Lundie, 1940; Schmolke, 1974; Neumann and Hrtel,
2004; Spiewok and Neumann, 2006b), aggression
(Schmolke, 1974; Elzen et al. , 2001) and absconding
(Hepburn and Radloff, 1998; Hood, 2000). Since all these
mechanisms have been observed not only in African
honeybees, which share a co-evolutionary history with the
small hive beetle, but also in European subspecies that
only recently came into contact with this novel pest, they
must be part of the suite of general defensive behaviours
present in all honeybees (Michener, 1974; Thompson,
1994). Therefore, it appears that only quantitative differ-
ences in these behaviours account for the difference in the
ability of African and European honeybees to deal with
the beetles (Neumann and Elzen, 2004). Other social bee
species may show similar defence mechanisms if con-
fronted with small hive beetles, but to date this has not
been studied.
Although it has been mentioned in the literature that
the small hive beetle may pose a potential threat to the
social insect fauna indigenous to North America (Tonn,
2002; Tonn et al., 2006), the actual attractiveness and
vulnerability of bumblebees, which are not native to sub-
Saharan Africa but occur in North America (Michener,
2000), has not been studied in depth. With the evidence
presented by Ambrose et al. (2000), Stanghellini et al.
(2000) and Spiewok and Neumann (2006a) suggesting
that the small hive beetle could exploit bumblebee
colonies, we decided to further investigate the ability of
small hive beetles to locate and infest bumblebee nests
and the defence mechanisms that counteract such infes-
tations. We conducted these studies to help evaluate the
threat of small hive beetles to native pollinators and to
contribute further knowledge to our understanding of the
general defence mechanisms of social bees against nest
intruders.
Materials and methods
All experiments were conducted in the summer of 2005 in Maryland,
USA.
Experiment A: Transmission and host choice
Four queenright commercial B. impatiens colonies and four small
(nucleus) queenright honeybee colonies of mixed European origin
(predominantly A. m. ligustica) were set up in a greenhouse (Fig. 1).
Honeybee mating nuclei were chosen to match the size of the
bumblebee colonies, so as to provide a similar amount of odour cues
for beetle orientation (Torto et al., 2005; Spiewok and Neumann,
2006a). All colonies were placed in new unused standard single ten-
frame Langstroth hive boxes to give them a similar external appear-
ance, with four empty boxes serving as controls. The boxes were divided
into four groups, each consisting of one bumblebee colony, one
honeybee colony and one control (Fig. 1). These were spaced evenly
within the greenhouse. The distances between boxes within a group
were 40 cm and between groups 143 cm. Distances to the beetle release
box placed in the centre (Fig. 1) were 145 cm and 183 cm, respectively.
For the duration of the experiment, the colony entrances were closed
with wire mesh (3.2 openings per cm2of mesh) allowing passage of small
hive beetles but preventing the bees from flying. Adult small hive
beetles (N =1,000) were released in the beetle release box at dusk
(19:00), in the time window for natural flight activity of small hive
beetles (Schmolke, 1974; Elzen et al., 2000), and given 36 hours to
disperse. During the experiment, mean temperature in the greenhouse
was 328C. For cooling, all colonies and the controls were sprayed at
noon with water using a manual pump sprayer. The experiment was
terminated at dawn on the second day by putting all colonies in
individual plastic bags and deep-freezing them at -808C. All beetles
found in the control boxes, in the beetle release box and outside of the
boxes were collected. The colonies were then systematically dissected
to assess colony phenotype, number of adult beetles, as well as the
presence of small hive beetle eggs and larvae. The following phenotype
data were evaluated: colony weight (nest structure, storage pots, brood
cells, and bees), number of bees and number of brood cells.
Experiment B: Colony defence by removal of small hive beetle life stages
The removal of small hive beetle life stages was investigated in ten
queenright commercial B. impatiens colonies following standard pro-
tocols used with African honeybees (Neumann and Hrtel, 2004;
Spiewok and Neumann, 2006b). Six colonies were set up in the field,
and four colonies were placed in the laboratory. The latter were
connected to individual entrance holes via plastic tubes (length 20 cm ;
14 cm), enabling the bees to fly and forage freely in the field.
1. Removal of eggs: To obtain small hive beetle eggs, 100 adult beetles
were reared in the laboratory (Neumann et al., 2001b; Mrrle and
Neumann, 2004) and introduced into ten plastic jars containing water, a
protein diet made of honey and pollen (1:2), and two double micro-
scope slides spaced by cover slips and held together with paper clips.
Small hive beetle females readily oviposit between microscope slides,
154 D. Hoffmann et al. Host shift of Aethina tumida
as they naturally prefer small cracks (Lundie, 1940) to protect their eggs
from being removed by host bees (Neumann and Hrtel, 2004). One
double microscope slide with protected eggs and two single slides (a
double slide opened up) with now exposed, unprotected eggs (~ 100
eggs/slide; total N =930 protected eggs and 1249 unprotected eggs)
were introduced into each of the ten colonies on top of the involucrum
(cover made of wax and other materials, which is typically found over
the inner nest of bumblebee colonies, Wilson, 1971). After one, three,
five, ten and 24 hours the slides were briefly removed from the colonies
and, before being reintroduced at the same within-box location, the
remaining eggs on the slides were counted.
2. Removal of larvae: Small hive beetle larvae were reared in the
laboratory (see above). Larvae not covered with sticky coating (“dry”
rearing approach, Neumann and Hrtel, 2004) were placed in open
Petri dishes (N =50 larvae each) and introduced into each of the test
colonies on top of the involucrum. After one, two, four, seven, ten and
24 hours the Petri dishes were briefly removed from the colonies and
the remaining larvae were counted before being reintroduced at the
same location. Larvae that were found killed in the Petri dishes were
considered removed, since they did not pose a threat to the colony any
more. To control for the escape rate of larvae, three Petri dishes
containing 50 larvae each were set up in a plastic box and kept in
darkness in the laboratory. The number of remaining larvae in these
control dishes was recorded at the respective time intervals.
3. Colony phenotypes: After the removal experiments, the colonies set
up in the field were euthanized by deep-freezing at -808C and colony
phenotype data were evaluated as described above.
Experiment C: Individual behavioural defence mechanisms of workers
Four queenright commercial B. impatiens colonies set up in the
laboratory were equipped with glass lids to facilitate observations
conducted under red light conditions. One microscope slide with
unprotected small hive beetle eggs (see above; N =100 eggs/slide) was
introduced into each of the four colonies on top of the involucrum. Bare
microscope slides served as controls. The colonies were given 1
2hour to
settle after the disturbance. The behaviour of workers on the slides was
then observed for 20 minutes in each colony and recorded according to
the following categories: 1) ignoring (walking, resting, self grooming or
ventilating on slide), 2) investigating (antennating/licking slide surface
or eggs), 3) attacking (biting/eating of eggs, biting slide). Afterwards,
the remaining eggs on the slides were counted.
Small hive beetle larvae not covered with sticky coating were
reared in the laboratory as described above. An empty Petri dish was
introduced into each test colony on top of the involucrum to serve as a
behavioural arena that could be monitored. Given some time to settle
after the disturbance, bumblebee workers treated the Petri dishes
indifferently (no investigations, no stopping when passing by or running
over the dish). After 1
2hour, a single larva was introduced into the arena
through a hole in the lid, and behavioural interactions were observed
for five minutes. Pieces of rubber band (length =1 cm) resembling
small hive beetle larvae in size and shape served as controls. The
following information was recorded: 1) time to first worker entering the
Petri dish, 2) time to first investigation (antennating/licking), 3) number
of subsequent investigations, 4) time to first attack (grasping, biting or
stinging), 5) number of subsequent attacks, 6) killing or removal. If
larvae or controls were still remaining 1
2hour after introduction, they
were removed from the Petri dishes. Then, colonies were given an
additional 1
2hour to settle before the next larva was introduced. This was
repeated six times for each colony for a total of 24 larvae and 24
controls.
These observations were also conducted in the same fashion in four
three-frame honeybee observation hives that were set up in the
laboratory (population ~ 3000 bees each). Here the eggs, larvae and
controls, respectively, were introduced into the Perspex runways
leading to the combs, which the bees used as the entryway to the hive.
Data analyses
Experiment A: Transmission and host choice
The numbers of workers in honeybee versus bumblebee colonies were
compared using a Mann-Whitney U-test. The numbers of small hive
beetles found in controls, honeybee and bumblebee colonies were
analysed by a Kruskal-Wallis test and multiple comparisons as post hoc
tests. Simple correlations (r-matrix) were performed between the
number of workers in a colony or colony weight, respectively, and
number of small hive beetles found in that colony.
Experiment B: Colony defence by removal of small hive beetle life stages
Mann-Whitney U-tests were performed to test for differences in
removal rates of protected versus unprotected eggs, for differences
between removal rates of larvae and controls and for differences in
removal rates of eggs and larvae between laboratory and field colonies.
Simple correlations (r-matrix) were performed between the colony
phenotype data and the removal rates for small hive beetle life stages.
Experiment C: Individual behavioural defence mechanisms of workers
Mann-Whitney U-tests were performed to test for differences in
removal rates and number of investigations of eggs, larvae and controls
between bumblebees and honeybees, and in removal rates and number
of investigations between treatments and controls. For the behavioural
categories ignoring, investigating and attacking of eggs, behavioural
ratios were calculated for each replicate of the 20 min. observation
period by dividing the number of observations of each specific
behaviour by the mean number of all behaviours observed. These
behavioural ratios were compared between honeybees and bumblebees
and between treatments and controls using Mann-Whitney U-tests.
Before comparing time to first investigation and time to first attack,
respectively, between honeybees and bumblebees and between treat-
ments and controls with Mann-Whitney U-tests, inevitable methodo-
logical differences were accounted for by subtracting from these values
the time to first worker entering the Petri dish in the bumblebee
colonies. All analyses were performed using the programmes SPSS
and Statistica.
Figure 1. Setup for experiment A: transmission and host choice in the
greenhouse (shaded boxes =honeybeecolonies ; striped boxes =bum-
blebee colonies, white boxes =controls, chequered box =beetle
release box).
Insect. Soc. Vol.55, 2008 Research article 155
Results
Experiment A: Transmission and host choice
Mean number of workers did not differ significantly
between honeybee and bumblebee colonies (honeybees
208 71.41 [mean SD], bumblebees 280.25 86.55;
Z=-1.155, p>0.05). Upon termination of the experi-
ment, no small hive beetles were found in the empty
control boxes. We found a total of 121 small hive beetles in
the honeybee nucleus colonies, and 292 in the bumbleACHTUNGTRENNUNGbee
colonies (medians with [1. quartile; 3. quartile]: honey-
bees 18 [7; 42], bumblebees 70 [59; 84]; Fig. 2). Neither
the number of workers (r =0.457, p>0.05) nor colony
weight (r =0.700, p>0.05) were significantly correlated
with the number of beetles found in the colonies. We
found significant differences in the number of small hive
beetles between controls, honeybee and bumblebee
colonies (H (2, N =12) =8.649, p<0.02). Significantly
more small hive beetles were present in the bumblebee
colonies than in the control boxes (p<0.02), but no
significant differences were found between beetle num-
bers in honeybee and bumblebee colonies or between
honeybee colonies and controls (p>0.05). In all four
bumblebee colonies we found several small hive beetle
egg clutches on brood cells (Fig. 3) and in storage pots. In
one honeybee nucleus colony small hive beetle eggs were
found in the debris.
Experiment B: Colony defence by removal of small hive
beetle life stages
1. Removal of eggs: Within 24 hours, 98.14 3.25 %
[mean SD] of the unprotected eggs and 12.11 8.80 %
of the protected eggs were removed from the bumblebee
colonies (Fig. 4). Significantly more protected eggs re-
mained in the colonies as compared to unprotected eggs
(after one hour: Z =–3.785, p<0.001; after 24 hours:
Z=–3.862, p<0.001, Fig. 4).
Figure 2. Experiment A: transmission and host choice. Number of
small hive beetles (boxplot showing medians and quartiles) found in the
control boxes, honeybee and bumblebee colonies (N =4 each)
36 hours after release.
Figure 3. Small hive beetle egg clutch on brood cell in a bumblebee
colony.
Figure 4. Experiment B: Removal of small hive beetle eggs
(means SD) after one, three, five, ten and 24 hours in ten B.
impatiens colonies (diamonds =protected eggs, squares =un-protect-
ed eggs).
156 D. Hoffmann et al. Host shift of Aethina tumida
2. Removal of larvae: In the controls, 100 % of the larvae
remained after 24 hours, whereas in the test colonies a
significant proportion of larvae was removed (after one
hour: Z =–2.090, p<0.04 ; after 24 hours: Z =–2.912,
p<0.005, Fig. 5). In eight out of ten colonies all larvae
were removed after 24 hours. Some of the larvae were
stung by the bumblebee workers (Fig. 6a), but were not
immediately removed. These larvae could be clearly
distinguished by their purplish colour (Fig. 6b) and were
dead. At least 22 stung larvae were found in nine colonies.
3. Differences in removal rates between laboratory and
field colonies: No significant differences were found in
the removal rates of protected or unprotected eggs
between laboratory and field colonies (Z =–1.279,
p>0.05 for protected and Z =–1.574, p>0.05 for
unprotected eggs). Removal rates of larvae were signifi-
cantly higher in the laboratory colonies during the first
seven hours (after one hour: Z =-2.574, p=0.01; after
seven hours: Z =–2.274, p<0.03), but later no signifi-
cant differences could be found (after 24 hours:
Z=–1.217, p>0.2).
4. Colony phenotypes: Colony phenotype data for the B.
impatiens field colonies are shown in Table 1, and the
correlation r-matrix for colony phenotypes and removal
of small hive beetle eggs and larvae in Table 2. After
Bonferroni adjustment, none of the correlations was
significant.
Figure 5. Experiment B: Removal of small hive beetle larvae
(means SD) after one, two, four, seven, ten and 24 hours in ten B.
impatiens colonies (diamonds =field colonies, circles =laboratory
colonies, squares =controls).
Figure 6. a) Bumblebee worker grasping a small hive beetle larva and
attempting to sting. b) Stung small hive beetle larvae in various stages of
discolouration. Arrow: fresh sting mark.
Table 1. Experiment B : Colony defence by removal of small hive
beetle life stages. Colony phenotype data for the tested B. impatiens
field colonies. Colony weight (nest structure, storage pots, brood cells,
bees), number of workers and of brood cells are shown.
Colony Colony weight [g] # Workers # Brood cells
1 110.4 69 19
2 164.9 164 111
3 162.5 119 170
4 182.9 191 176
5 149.2 146 140
6 155.2 105 148
Mean SD 154.2 24.3 132.3 43.7 127.3 57.9
Insect. Soc. Vol.55, 2008 Research article 157
Experiment C: Individual behavioural defence
mechanisms of workers
Within 50 minutes after introduction of unprotected
small hive beetle eggs, 61.88 8.25 % [mean SD] were
removed by the bumblebee workers, whereas the honey-
bees removed only 5.85 8.54 % of eggs within the same
time window. Thus, the bumblebees performed egg
removal significantly faster (Z =–2.323, p=0.02).
Mean behavioural ratios for bumblebees and honeybees
are shown in Table 3. In bumblebees, behavioural ratios of
ignoring were significantly higher towards the controls
(Z =–2.309, p<0.03), whereas behavioural ratios of
attacking were higher towards small hive beetle eggs
(Z =–2.366, p<0.02). Differences in behavioural ratios
of investigating in bumblebees (Z =–1.732, p>0.05) as
well as in all behavioural ratios in honeybees between
eggs and controls were not significant (Z =0.000, p=1
for ignoring and investigating, Z =–0.331, p>0.5 for
attacking). In bumblebees, behavioural ratios of ignoring
were significantly higher (Z =–2.021, p<0.05 for eggs
and Z =–2.309, p<0.03 for controls), and of investigat-
ing significantly lower (Z =–2.309, p<0.03 for eggs and
controls) as compared to honeybees. Behavioural ratios
of attacking were significantly higher in bumblebees
towards eggs (Z =–2.323, p=0.02), but did not differ
significantly towards controls (Z =–0.189, p>0.5).
Within 30 minutes after introduction, the bumblebees
killed or removed 41.67 28.87 % of small hive beetle
larvae (Fig. 6) and removed none of the controls. The
honeybees killed or removed 62.50 15.96 % of larvae
and removed 16.67 13.61 % of controls. The difference
between removal rates of larvae in honeybees versus
bumblebees was not significant (Z =–1.323, p>0.05),
but significantly more controls were removed by the
honeybees as compared to the bumblebees (Z =–2.000,
p<0.05). In bumblebees, no significant difference was
found in the number of investigations between larvae and
controls (Z =-1.732, p>0.05), whereas in honeybees the
controls were significantly more often investigated than
the larvae (Z =–2.309, p<0.03). Honeybees started to
investigate the larvae significantly earlier (29 64 sec-
onds after introduction) than bumblebees (after 90 82
seconds; Z =–3.981, p<0.001), but time to first inves-
tigation of the controls did not differ significantly (honey-
bees: 26 43 seconds, bumblebees: 31 32 seconds;
Z=-1.827, p>0.05). In bumblebees, time to investiga-
tion of the controls was significantly shorter as compared
to treatments (Z =-3.017, p<0.005), whereas in honey-
bees the difference was not significant (Z =–0.077,
p>0.5). While honeybees started to attack treatments
(after 17 39 seconds) significantly earlier than controls
(71 66 seconds; Z =–2.468, p<0.02), bumblebees did
not attack the controls. The difference in time to attack
treatments between honeybees and bumblebees (61 81
seconds) was not significant (Z =–1.093, p>0.2).
Table 2. Experiment B : Colony defence by removal of small hive beetle life stages. Correlation r-matrix for colony phenotype data and removal data
for the tested B. impatiens field colonies. Colony weight, number of workers and of brood cells, removal of small hive beetle protected and
unprotected eggs after three and 24 hours, and removal of small hive beetle larvae after two and 24 hours were considered. After Bonferroni
adjustment (level of significance: a=0.0021), none of the correlations is significant. Asterisks indicate r>0.8.
Colony weight # Workers # Brood cells
Colony weight 1
# Workers 0.864* 1
# Brood cells 0.892* 0.650 1
Egg removal Protected 3 hours 0.251 0.090 0.577
24 hours –0.226 0.023 –0.161
Unprotected 3 hours 0.247 0.237 0.009
24 hours –0.354 –0.219 –0.639
Larva removal 2 hours –0.062 0.129 –0.438
24 hours –0.564 –0.316 –0.859*
Table 3. Experiment C: Individual behavioural defence mechanisms of workers. Behavioural ratios [means SD] of bumblebees and honeybees
towards small hive beetle eggs for the 20 minutes observation period are shown.
Ignore Investigate Attack
Eggs Controls Eggs Controls Eggs Controls
Bumblebees 0.31 0.04 0.50 0.08 0.62 0.03 0.50 0.08 0.07 0.01 0.00 0.00
Honeybees 0.14 0.12 0.12 0.04 0.86 0.12 0.87 0.07 0.01 0.01 0.01 0.02
158 D. Hoffmann et al. Host shift of Aethina tumida
Discussion
Our data clearly show that small hive beetles do invade
bumblebee colonies and readily oviposit there. Contrary
to previous findings, however, bumblebees are not help-
less but show defensive behaviours. Nevertheless, there
are quantitative (worker force) and qualitative differ-
ences (hygienic behaviour) between A. mellifera and B.
impatiens.
Our data confirm that small hive beetles prefer bee
colonies to empty hive boxes (Spiewok and Neumann,
2006a), the latter providing only hiding places from
daylight (Schmolke, 1974), but not emitting odour cues
used by the beetles for orientation (Elzen et al., 1999;
Torto et al., 2005 ; Spiewok and Neumann, 2006a).
Furthermore, the data suggest that bumblebee colonies
are equally or even more attractive to small hive beetles
as honeybee colonies of similar size (Fig. 2). Although
adult honeybees in combination with hive products are
highly attractive for free-flying small hive beetles (Elzen
et al., 1999, 2000; Suazo et al., 2003), the number of bees
in a colony or colony weight did not correlate with the
number of small hive beetles found in that colony. So,
stronger colonies were not necessarily more attractive,
which may be attributed to the rather small differences in
colony strength in our experiment. In the light of similar
results from honeybee field colonies (Spiewok and
Neumann, 2006b; Neumann and Hoffmann, 2007), this
suggests that colony phenotypes are unlikely to trigger
small hive beetle host finding.
Our finding of small hive beetle eggs in the debris of
one honeybee colony confirms cryptic low-level repro-
duction (Spiewok and Neumann, 2006c) as an alternative
to the usual highly destructive mass reproduction (Lun-
die, 1940). In all bumblebee colonies beetles had not only
invaded, seeking shelter or food, but had also started to
lay eggs. This indicates that the bumblebee colonies had
been accepted as a suitable breeding ground, thus serving
as an alternative host for the small hive beetle. Prior to
release, all beetles were kept only on a honey and water
diet, so that the females were not ready to oviposit
immediately, but had to feed on a protein source first.
Hence, protein foraging by small hive beetles is possible
in bumblebee nests, supporting earlier findings on
successful life cycle completion in association with
bumblebee colonies (Ambrose et al., 2000). Considering
that within a time window of 36 hours, the beetle females
had to leave the release box, find and enter a host colony,
locate the food stores and feed on protein diet (e.g.
pollen), mate, and oviposit, the host finding process likely
did not include a prolonged period of searching. This not
only confirms that bumblebee colonies serve as alternate
hosts when infested experimentally in the laboratory
(Ambrose et al., 2000; Stanghellini et al., 2000), but
moreover indicates that small hive beetles, when search-
ing for a host colony, are able to locate and may readily
choose bumblebee nests instead of honeybee hives,
thereby confirming recent findings of natural infestations
of commercial bumblebee colonies in the field (Spiewok
and Neumann, 2006a). However, it has yet to be shown
whether small hive beetles actually infest natural nests of
Bombus species in the field. Clearly, there are differences
between commercial bumblebee colonies (Spiewok and
Neumann, 2006a) and our experimental boxes compared
to natural nests, which are typically underground, pref-
erably in abandoned rodent burrows (Michener, 2000).
Nevertheless, olfactory orientation cues may also enable
small hive beetle host finding of natural nests, analogous
to Antherophagus sp. (Coleoptera: Cryptophagidae),
which is probably a scavenger of B. atratus nests
(Gonzalez et al., 2004). Moreover, naturally occurring
honeybee (A. m. scutellata) nests can also be found
underground having only small entrance tubes, and may
nevertheless be infested with small hive beetles (PN, pers.
obs.). Finally, many small hive beetles were found in feral
honeybee colonies in Australia (Somerville, 2003), which
can also have very small entrances. In conclusion, our data
suggest that bumblebee colonies, be they commercial or
wild, are likely to get infested by small hive beetles and if
so, can serve as alternate hosts.
The removal rates of eggs demonstrate that, like
honeybees (Neumann and Hrtel, 2004), bumblebees are
able to efficiently remove small hive beetle eggs. They
are, however, considerably less efficient if the eggs are
hidden in cracks. While in honeybees it appears that
tongue length may be the limiting factor in the removal of
protected eggs (Neumann et al., 2003), B. impatiens
workers tend to remove such eggs less proficiently even
though in this species tongue length does not differ
substantially from honeybees (Harder, 1985; Durka,
2002). Surprisingly, bumblebees attacked the small hive
beetle eggs more often than honeybees, and removed the
eggs much faster, thereby confirming our finding that
bumblebees are very efficient egg removers given that the
eggs are exposed and easily accessible. Correspondingly,
bumblebees ignored the controls more often than the
eggs. Honeybees, on the other hand, investigated both
eggs and controls more often than bumblebees. While
honeybees usually keep high hygienic standards within
the hive and are thus generally intolerant of foreign
objects (Seeley, 1985), bumblebees tend to ignore inan-
imate items (see below). Since eggs are usually eaten,
however, egg removal is instantly rewarding to the
individual in the form of nutrient gain. Still, although
bumblebee colonies may remove a large proportion of the
small hive beetle eggs present in the nest, there will likely
remain a fair number of protected eggs which will
eventually hatch into larvae.
The removal rates of larvae were also comparable to
the performance observed in honeybees (Neumann and
Hrtel, 2004; Spiewok and Neumann, 2006b). Most
colonies removed all larvae within 24 hours, and tempo-
rary differences in removal rates between field and
laboratory colonies did not persist. Bumblebees thus
quickly respond to the presence of small hive beetle
larvae and are able to dispose of them, thereby preventing
Insect. Soc. Vol.55, 2008 Research article 159
severe damage of the nest. Honeybee workers removed
slightly more larvae than bumblebees, but also removed
some of the controls. Again, general differences in
hygienic behaviour (Seeley, 1985; Goulson, 2003b) likely
account for this. The high number of investigations of
controls in honeybees was probably due to the longer
retention period in the runway, as opposed to the larvae
being removed quickly. Honeybees detected the presence
of larvae earlier (investigate), but did not attack earlier
than bumblebees. Thus, despite some differences in the
sequence of actions, bumblebees are equally responsive
to small hive beetle life stages as honeybees. The
quantitative differences in our data are probably attrib-
utable to the great differences in colony strength between
the two bee species (Michener, 1974). Average colony
size differs between commercial honeybee and Bombus
colonies by two orders of magnitude, i.e. bumblebee
colonies are considerably smaller (Michener, 1974, 2000).
This means that fewer workers can engage in colony
defence (Michener, 1974), especially if the colony is
additionally challenged and many workers are busy with
other tasks (e.g. thermoregulation as in our field colonies,
see differences in removal rates of larvae, Fig. 5). Our
analysis of the colony phenotype data points in the same
direction in that the stronger colonies tend to remove
small hive beetle larvae faster. Furthermore, due to their
different nesting biology, bumblebee hygienic behaviour
may be different compared to honeybees. Most bumble-
bee species nest in the ground (see above) and use nesting
material such as grass, moss, hair or wool (Michener,
2000). Hence they tolerate foreign objects to a greater
extent than honeybees. Indeed, dead adult beetles can
even be included in the involucrum (Gonzalez et al.,
2004) and remained in some of our test colonies after 24
hours (data not shown).
Although we used the same bumblebee species
derived from Koppert Biological Systems and also
housed some of our colonies in the laboratory, our
findings differ substantially from those made by Stan-
ghellini et al. (2000), who did not observe any colony
defence whatsoever. This may be due to differences in
colony size (100200 bees in Stanghellini et al.s as
opposed to 70400 bees in our experiment) or overall
colony health (nest parasite load was not quantified in
either study). While we allowed the bees to fly out to the
field, however, Stanghellini et al. confined them to the
laboratory, so in their study the bees may have not been
able to show the whole range of natural behaviours.
Since small hive beetles do not complete their entire
life cycle within the beehive, but pupate in the soil
(Lundie, 1940), the adults have to find a host colony after
eclosion. The small hive beetle as an active flyer can cover
distances of several kilometres (c.f. Neumann and Elzen,
2004), and can easily find even cryptic wild honeybee
nests following odour cues (see above). However, where
host population size is small, i.e. density of host colonies is
low, a more opportunistic approach may increase the
chances of finding a suitable host within a reasonably
short time (thereby reducing the risks of predation,
desiccation, starvation, etc.). In light of the adaptive value
of lower host specificity, it is not surprising that several
other macroparasites of social insects may also switch
hosts within or even across genera. Indeed, Epuraea
depressa (Coleoptera: Nitidulidae) is reported from the
nests of different bumblebee species (Scott, 1920; Cum-
ber, 1949). Likewise, the greater wax moth Galleria
mellonella, which is normally associated with colonies of
different honeybee species (Williams, 1997), was also
found in nests of meliponids (Nogueira-Neto, 1953) and
bumblebees (Oertel, 1963; Spiewok and Neumann,
2006a). Moreover, the lesser wax moth Achroia grisella,
which usually infests honeybee colonies (Williams, 1997),
has also been reported from stingless bees (Cepeda-
Aponte et al., 2002). A further example is the bumblebee
wax moth Aphomia sociella, which infests various
Bombus species (Free and Butler, 1959; Pouvreau,
1967) but is also rarely found in honeybee colonies
(Toumanoff, 1939). Finally, small hive beetles have also
been reported to naturally infest colonies of stingless bees
(Dactylurina staudingerii) in West Africa (Mutsaers,
2006). Considering that small hive beetles do switch to
non-Apis hosts within their endemic range, it is not
surprising that in their new ranges other social bees may
serve as alternate hosts. In light of these earlier reports
and of our data it appears that small hive beetles are less
host specific than previously thought. In fact, several
transmission events of parasites from invaders to native
species are already known (Prenter et al., 2004). The
taxonomic proximity and ecological similarities within
the family Apidae (Michener, 1974, 2000) seem to
generally facilitate host switches of macroparasites.
Aside from this, there is another reason to expect low
host specificity in the small hive beetle. Originating from
a family of opportunistic scavengers (the sap beetles,
Nitidulidae) with a low level of specialization (Morse,
1998), small hive beetles seem to be pre-adapted for host
switch. They are able to sustain themselves and reproduce
not only on hive products of both intact and absconded
honeybee colonies, in stingless bee and commercial
bumblebee colonies (see above), but also on a variety of
fruits (Ellis et al., 2002), as well as on the sparse resources
contained in the debris of functioning honeybee colonies
(Spiewok and Neumann, 2006c). Thus, the small hive
beetle can be expected to infest still other social bee
species than the ones it has been found in so far.
In conclusion, our findings show that small hive
beetles do not prefer honeybee hives over bumblebee
colonies, so native pollinators may serve as alternate
hosts. Field surveys are therefore necessary to evaluate
the actual infestation status of wild bumblebee colonies
and its impact on the conservation status of bumblebee
species. But even though bumblebees lack a co-evolu-
tionary history with the small hive beetle, they are able to
defend their colonies against this nest intruder consid-
erably well. Thus, the observed defence mechanisms must
be part of a generalistic defence system suitable for
160 D. Hoffmann et al. Host shift of Aethina tumida
defence against multiple attackers (Michener, 1974;
Thompson 1994). This supports general patterns of
host-parasite co-evolution in that specialization is harder
to accomplish for the victims, but it is possible for them to
maintain more general defences towards multiple attack-
ers (Thompson, 1994; see also Jokela et al., 2000).
Acknowledgements
We gratefully acknowledge Rene Ruiter and Koppert Biological
Systems for the gift of bumblebee colonies. Appreciation is also
addressed to the people at the USDA Bee Research Laboratory in
Beltsville for kind support. DH wishes to thank S. Spiewok and K.
Merkel for stimulating discussions and practical advice. Two anony-
mous referees made valuable comments on a previous version of the
manuscript.
References
Ambrose J.T., Stanghellini M.S. and Hopkins D.I. 2000. A scientific
note on the threat of small hive beetles (Aethina tumida Murray) to
bumble bee (Bombus spp.) colonies in the United States. Apido-
logie 31: 455456
Animal Health Australia. 2003. Small Hive Beetle National Manage-
ment Plan. Deakin ACT, 2600, Australia: Animal Health Australia
Council Ltd, ACN071890956. p. 17
Cassey P., Blackburn T.M., Duncan R.P. and Chown S.L. 2005.
Concerning invasive species: Reply to Brown and Sax. Austral.
Ecol. 30: 475 480
Cepeda-Aponte O.I., Imperatriz-Fonseca V.L. and Velthuis H.H.W.
2002. Lesser wax moth Achroia grisella: first report for stingless
bees and new capture method. J. Apic. Res.41: 107– 108
Clay H. 2006. Small hive beetle in Canada. Hivelights 19: 14– 16
Cumber R.A. 1949. Humble-bee parasites and commensales found
within a thirty mile radius of London. Proc. R. Entomol. Soc.
London A 24: 119 127
Dollin A. 1996. Introduction to Australian native bees. Native bees of
Australia series, booklet 1. Australian Native Bee Research Centre,
North Richmond, NSW, Australia. p 7
Durka W. 2002. Blten- und Reproduktionsbiologie. Schriftenreihe fr
Vegetationskunde, Heft 38. Bundesamt fr Naturschutz, Bonn,
Germany. p 164
Ellis J.D. Jr., Neumann P., Hepburn R. and Elzen P.J. 2002. Longevity
and reproductive success of Aethina tumida (Coleoptera: Nitidu-
lidae) fed different natural diets. J. Econ. Entomol.95: 902–907
Ellis J.D. Jr., Hepburn H.R., Ellis A.M. and Elzen P.J. 2003a. Social
encapsulation of the small hive beetle by European honeybees
(Apis mellifera L.). Insect. Soc.50: 286 291
Ellis J.D., Richards C.S. , Hepburn H.R. and Elzen P.J. 2003b.
Oviposition by small hive beetles elicits hygienic responses from
Cape honeybees. Naturwissenschaften 90: 532–535
Ellis J.D. Jr., Hepburn R. and Elzen P.J. 2004a. Confinement of small
hive beetles (Aethina tumida) by Cape honeybees (Apis mellifera
capensis). Apidologie 35: 389 396
Ellis J.D. Jr., Delaplane K.S. , Richards C.S., Hepburn R., Berry J.A.
and Elzen P.J. 2004b. Hygienic behavior of Cape and European
Apis mellifera (Hymenoptera: Apidae) toward Aethina tumida
eggs oviposited in sealed bee brood. Ann. Entomol. Soc. Am.97:
860–864
Elzen P.J., Baxter J.R., Westervelt D. , Randall C., Delaplane K.S.,
Cutts L. and Wilson W.T. 1999. Field control and biology studies of
a new pest species, Aethina tumida Murray (Coleoptera, Nitidu-
lidae), attacking European honey bees in the Western Hemisphere.
Apidologie 30: 361 366
Elzen P.J., Baxter J.R., Westervelt D. , Randall C. and Wilson W.T. 2000.
A scientific note on observations of the small hive beetle, Aethina
tumida Murray (Coleoptera, Nitidulidae), in Florida, USA.
Apidologie 31: 593594
Elzen P.J., Baxter J.R., Neumann P. , Solbrig A., Pirk C. , Hepburn H.R.,
Westervelt D. and Randall C. 2001. Behaviour of African and
European subspecies of Apis mellifera toward the small hive beetle,
Aethina tumida. J. Apic. Res.40: 40–41
Evans J.D. , Pettis J.S., Hood W.M. and Shimanuki H. 2003. Tracking an
invasive honey bee pest : mitochondrial DNA variation in North
American small hive beetles. Apidologie 34: 103 109
Free J.B. and Butler C.G. 1959. Bumblebees. Collins, London, UK.
Gonzalez V.H. , MejiaA. and Rasmussen C. 2004. Ecology andnesting
behavior of Bombus atratus Franklin in Andean Highlands
(Hymenoptera: Apidae). J. Hymenopt. Res.13: 234 242
Goulson D. 2003a. Effects of introduced bees on native ecosystems.
Annu. Rev. Ecol. Evol. Syst.34: 1–26
Goulson D. 2003b. Bumblebees, Their Behaviour and Ecology. Oxford
University Press, Oxford, UK.
Harder L.D. 1985. Morphology as a predictor of flower choice by
bumble bees. Ecology 66: 198 210
Hepburn H.R. and Radloff S.E. 1998. Honeybees of Africa. Springer
Verlag, Berlin, Heidelberg, New York. pp 370
Hood W.M. 2000. Overview of the small hive beetle, Aethina tumida,in
North America. Bee World 81: 129– 137
Hood W.M. 2004. The small hive beetle, Aethina tumida: a review. Bee
World 85: 5159
Jokela J. , Schmid-Hempel P. and Rigby M.C. 2000. Dr. Pangloss
restrained by the Red Queen – steps towards a unified defence
theory. Oikos 89: 267–274
Levine J.M.and DAntonio C.M. 2003. Forecastingbiological invasions,
with increasing international trade. Conserv. Biol. 17: 322– 326
Lundie A.E. 1940. The small hive beetle, Aethina tumida. Science
Bulletin 220, Entomological Series 3. Dept. of Agriculture and
Forestry, Pretoria, South Africa
Michener C.D. 1974. The Social Behaviour of the Bees. Harvard
University Press, Cambridge, MA, USA.
Michener C.D. 2000. The Bees of the World. The Johns Hopkins
University Press, Baltimore, MD, USA. p 913
Mooney H.A. and Cleland E.E. 2001. The evolutionary impact of
invasive species. Proc. Natl. Acad. Sci. USA 98: 54465451
Moritz R.F.A. , Hrtel S. and Neumann P. 2005. Global invasions of the
western honeybee (Apis mellifera) and the consequences for
biodiversity. coscience 12: 289 301
Morse R. 1998. Nitidulids. Bee Culture 126: 17
Mostafa A.M. and Williams R.N. 2002. New record of the small hive
beetle in Egypt and notes on its distribution and control. Bee World
83: 99 108
Mrrle T. and Neumann P. 2004. Mass production of small hive beetles
(Aethina tumida Murray,Coleoptera : Nitidulidae). J. Apic. Res.43:
144–145
Mutsaers M. 2006. Beekeepers observations on the small hive beetle
(Aethina tumida) and other pests in bee colonies in West and East
Africa. 2nd Eur. Conf. Apidology EurBee, Prague, Czech Republic.
p44
Neumann P. and Elzen P. 2004. The biology of the small hive beetle
(Aethina tumida Murray, Coleoptera: Nitidulidae): Gaps in our
knowledge of an invasive species. Apidologie 35: 229 247
Neumann P. and Hrtel S. 2004. Removal of small hive beetle (Aethina
tumida) eggs and larvae by African honeybee colonies (Apis
mellifera scutellata). Apidologie 35: 31 36
Neumann P. and Hoffmann D. 2008. Small hive beetle diagnosis and
control in naturally infested honeybee colonies using bottom board
traps and CheckMite+strips. J. Pest Sci., DOI 10.1007/s10340-007-
0183-8.
Neumann P., Pirk C.W.W., Hepburn H.R., Solbrig A.J., Ratnieks
F.L.W., Elzen P.J. and Baxter J.R. 2001a. Social encapsulation of
beetle parasites by Cape honeybee colonies (Apis mellifera
capensis Esch.). Naturwissenschaften 88: 214 216
Insect. Soc. Vol.55, 2008 Research article 161
Neumann P., Pirk C.W.W., Hepburn R., Elzen P.J. and Baxter J.R.
2001b. Laboratory rearing of small hive beetles, Aethina tumida
(Coleoptera, Nitidulidae). J. Apic. Res.40: 111–112
Neumann P., Hrtel S. and Hepburn H.R. 2003. Small hive beetle
ovipositors vs. honeybee tongues: co-evolutionary arms race
between Aethina tumida Murray (Coleoptera: Nitidulidae) and
Apis mellifera L. 18th meet. German speaking section IUSSI,
Regensburg, Germany. p34
Nogueira-Neto P. 1953. A criażo de abelhas indigenas sem ferr¼o
(Meliponinae). 1st Ed. Chcaras e Quintais, S¼o Paulo, Brazil
Oertel E. 1963. Greater wax moth develops on bumble bee cells. J.
Econ. Entomol.56: 543 544
Pouvreau A. 1967. Contribution  ltude morphologique et biologique
dAphomia sociella L. (Lepidoptera, Heteroneuro, Pyralidoidea,
Pyralididae), parasite des nids de bourdons (Hymenoptera,
Apoidea, Bombus Latr.). Insect. Soc.14: 57 72
Prenter J., MacNeil C., Dick J.T.A. and Dunn A.M. 2004. Roles of
parasites in animal invasions. Trends Ecol. Evol.19 : 385– 390
Ritter W. 2004. Beutenkfer in Portugal. Deutsches Bienen Journal 12:
14
Schmolke M.D. 1974. A study of Aethina tumida: the small Hive-
Beetle. Certificate in Field Ecology Project Report. University of
Rhodesia (Zimbabwe), Salisbury (Harare)
Scott H. 1920. Notes on the biology of some inquilines and parasites in a
nest of Bombus derhamellus Kirby; with a description of the larva
and pupa of Epuraea depressa Illig. (=aestiva Auctt.: Coleoptera,
Nitidulidae). Trans. Entomol. Soc. London, pp 99 –127
Seeley T.D. 1985. Honeybee Ecology – A Study of Adaptation in Social
Life. Princeton University Press, Princeton, NJ, USA. pp 200
Somerville D. 2003. Study of the small hive beetle in the USA. A report
for the Rural Industries Research and Development Corporation.
RIRDC Publication No 03/050, RIRDC Project No DAN-213A
Spiewok S. and Neumann P. 2006a. Infestation of commercial
bumblebee (Bombus impatiens) field colonies by small hive beetles
(Aethina tumida). Ecol. Entomol.31: 623–628
Spiewok S. and Neumann P. 2006b. The impact of queenlossand colony
phenotype on the removal of small hive beetle (Aethina tumida
Murray) eggs and larvae by African honeybee colonies (Apis
mellifera capensis Esch.). J. Insect Behav.19: 601–611
Spiewok S. and Neumann P. 2006c. Cryptic low-level reproduction of
small hive beetles in honeybee colonies. J. Apic. Res.45: 4748
Spiewok S., Pettis J., Duncan M., Spooner-Hart R., Westervelt D. and
Neumann P. 2007. Small hive beetle, Aethina tumida, populations I :
Infestation levels of honeybee colonies, apiaries and regions.
Apidologie, in press.
Stanghellini M.S., Ambrose J.T. and Hopkins D.I. 2000. Bumble bee
colonies as potential alternative hosts for the small hive beetle
(Aethina tumida Murray). Am. Bee J. 140: 71 75
Suazo A., Torto B., Teal P.E.A. and Tumlinson J.H. 2003. Response of
the small hive beetle (Aethina tumida) to honey bee (Apis
mellifera) and beehive-produced volatiles. Apidologie 34: 525–533
Thompson J.N. 1994. The Coevolutionary Process. University of
Chicago Press, Chicago, IL, USA. pp 376
Tonn B.E. 2002. Distant futures and the environment. Futures 34 : 117–
132
Tonn B., English M., Turner R. and Hemrick A. 2006. The future of
bioregional planning in the Southern Appalachian Man and
Biosphere region. Futures 38: 490 504
Torto B., Suazo A., Alborn H., Tumlinson J.H. and Teal P.E.A. 2005.
Response of the small hive beetle (Aethina tumida) to a blend of
chemicals identified from honeybee (Apis mellifera) volatiles.
Apidologie 36: 523 532
Toumanoff C. 1939. Les Enemies des Abeilles. Imprimerie dExtrÞme-
Orient, Hanoi, Vietnam.
Williams J.L. 1997. Chapter 7: Insects: Lepidoptera. In: Honey Bee
Pests, Predators, and Diseases (Morse R.A. and Flottum K., Eds),
3rd Ed, A.I. Root Company, Medina, OH, USA. pp 123, 139
Wilson E.O. 1971. The Insect Societies. Belknap Press, Harvard
University, Cambridge, MA, USA.
To access this journal online:
http://www.birkhauser.ch/IS
162 D. Hoffmann et al. Host shift of Aethina tumida
... The small hive beetle, Aethina tumida Murray (Coleoptera: Nitidulidae), is a pest of Western honeybees (Apis mellifera L.) (Hymenoptera: Apidae) and is economically significant in the USA and Australia . The beetle has also been reported to invade bumblebee, stingless bee, and solitary bee nests (Gonthier et al. 2019;Hoffmann et al. 2008;Neumann et al. 2016). This invasive insect, which originates in sub-Saharan Africa (Lundie 1940), is now recorded on every continent except Antarctica (e.g. ...
Article
Full-text available
The small hive beetle, Aethina tumida (Coleoptera: Nitidulidae), is an economically important pest of the Western honeybee, Apis mellifera (Hymenoptera: Apidae). We investigated the effect of rearing environment on the cuticular chemical profile of adult A. tumida , using hexane to extract the hydrocarbons and other compounds from the cuticles of beetles. Beetles were collected from A. mellifera colonies in Australia as well as reared in single sex laboratory cultures on different diets. We investigated whether rearing environment (laboratory vs. field, different apiaries, access to mating partners, diet) had any effect on cuticular hydrocarbons. Coupled gas chromatography–mass spectrometry analyses of the extracts showed that rearing environment had significant qualitative and quantitative effects on the hydrocarbons detected. The data support the hypothesis that cuticular profiles of A. tumida are contingent on environment, partitioning on the basis of rearing diet and source hives. The finding has implications for the regulation of interactions between A. tumida and honeybees and improvements in targeting of management strategies.
... The small hive beetle has now spread to all continents but Antarctica [9,10]. It can cause substantial damage to apiculture and wild bees [11][12][13]. The economic losses to Florida beekeepers were estimated at USD 3 million in 1998 [14]. ...
Article
Full-text available
The small hive beetle (Aethina tumida Murray) is a serious threat to beekeeping and crops that rely on honeybees for pollination. The small hive beetle not only causes significant damage to honeybees by feeding on pollen and honey, attacking bee brood and causing stored honey to ferment, but also might serve as a vector of diseases. In addition, the small hive beetle has developed resistance to the pyrethroid and organophosphate insecticides registered for control of honeybee pests in the United States. The development of resistance in small hive beetle populations is a great concern to the beekeeping industry; thus, there is an urgent need for strategies to manage that resistance. Therefore, we used synergist probes to determine the mechanisms of resistance in a small hive beetle population to these insecticides. Our studies on the toxicity of insecticides alone or with the synergists piperonyl butoxide (PBO) and S,S,S,-tributyl phosphorotrithionate (DEF) suggested that mixed-function oxidases and esterases were the major resistance factors to these insecticides in a studied population of the small hive beetle. In contrast, there was no synergism with diethyl maleate (DEM), triphenyl phosphate (TPP) and formamidine. Therefore, glutathione-S-transferase, carboxylesterase and target site were not involved in insecticide resistance in the small hive beetle. Rotation of classes of insecticides (with different modes of action) and metabolic synergists were suggested for the development of successful resistance management programs. To the best of our knowledge, this is the first study of the mechanisms of resistance in small hive beetle populations in Florida and suggests an urgent need for alternative control strategies for these serious pests of honeybee colonies.
... The small hive beetle (SHB), Aethina tumida Murray (Coleoptera: Nitidulidae) is an invasive pest of honey bee (Apis mellifera), stingless bees and bumble bees throughout the world [15][16][17], including South Korea [18]. Sub-Saharan African countries are the native habitat of SHB, where the species is a conditional pest of honey bee colonies [19,20]. ...
Article
Full-text available
The small hive beetle (SHB) Aethina tumida Murray, (Coleoptera: Nitidulidae) is now a global invasive pest of honey bees, but its cold tolerance potential has not been yet explored. Therefore, we measured the supercooling point (SCP) of different stages of SHBs and also the impact of acclimation on their SCPs and survival as a measure for cold tolerance. Combinations of different temperatures (0, 3, 5, 7, and 10 ∘C) for different hours (1, 3, 5, 7, 12, 24, 35, and 48 h) were used to assess SHB survival. The supercooling points occurred at lower temperatures (−19.4 ∘C) in wandering larvae than in the other stages (pupae: −12.5 ∘C, and feeding larvae: −10.7 ∘C). A lethal temperature (LT50) of feeding larvae was achieved earlier at 4.9 ∘C after 7 h exposure than the wandering larvae (3.7 ∘C at 48 h) and pupae (5.6 ∘C at 48 h). The sum of injurious temperature (SIT) is the most suitable estimation to describe cold resistance of the SHB immatures. The wandering larvae were the most cold tolerant, followed by pupae and feeding larvae based on SIT values of −286.8, −153.7 and −28.7 DD, respectively, and also showed more phenotypic plasticity after acclimation than feeding larvae and slightly more than pupae. Our results show that all stages, i.e., feeding larvae, wandering larvae and pupae, are chill susceptible. However, these stages, especially wandering larvae and pupae, showed the capacity to acclimate to cold temperatures, which may help them to survive in winter for the continuity of the SHB population, especially in a scenario of climate change.
... The vulnerability of bumblebee colonies (Bombus impatiens) has been known for over a decade, since they can be potential hosts to the SHB, which invades the colonies and lays there easily (Hoffmann et al., 2008). ...
... Once reaching the postfeeding stage, small hive beetle larvae migrate out of a hive and burrow into neighboring soil where they pupate in chambers they excavate (Neumann et al. 2016). Small hive beetles can also reproduce in association with nests of bumble bees, stingless bees, and solitary bees (Hoffmann et al. 2008, Neumann et al. 2016, Gonthier et al. 2019). ...
Article
Full-text available
The small hive beetle, Aethina tumida Murray, is an invasive pest that has spread globally. Western honey bees, Apis mellifera Linnaeus (Hymenoptera: Apidae), are considered the most important host and infestations can lead to collapse of colonies. Larvae feed on honey, pollen, and brood inside the hive and leave the hive as postfeeding wandering larvae to pupate in the surrounding soil. Other host species include bumble bees, stingless bees, and solitary bees, all of which can facilitate small hive beetle reproduction and are used for greenhouse crop pollination worldwide. Here, we investigated if small hive beetles can complete their life cycle when soil is absent by pupating in plant root-supporting substrates commonly used in greenhouses. Wandering small hive beetle larvae were introduced into containers with coconut fiber, perlite, a mixture of both and stone wool substrates to investigate pupation success and development time. Sand was used as control substrate. In all but one substrate (perlite), small hive beetles developed into adults equally well as they did in the sand. Development time ranged between 23 and 37 d and was not different from that of the control. We showed that small hive beetles can pupate in greenhouse substrates. This could constitute a problem for greenhouse pollination as well as it could facilitate small hive beetle survival in areas which otherwise would be deemed unsuitable or marginal environments for small hive beetles to become established. Our study highlights the opportunistic nature of the small hive beetle as an invasive species.
Article
Full-text available
Small hive beetle (Aethina tumida Murray) control has become an issue of increasing importance for North American apiculturists throughout the past two decades. Aethina tumida was discovered in Florida in 1989, presumably transported from its native habitat of sub-Saharan Africa through the shipment of European honey bee (Apis mellifera L) queens. Estimates of damage from A. tumida were as high as $3 million annually in the United States by the year 2004, and A. tumida was found in nearly every state by 2008. When adult beetles emerge from pupation in soil surrounding the hive, they are attracted to A. mellifera hives through a variety of pheromones and volatile organic compounds from bees and hive products. Aethina tumida larvae and adults consume hive products and bee brood, generating fermenting waste (or slime), which can eventually lead to hive abandonment in cases of severe infestation. Pest management efforts for A. tumida have focused on trapping adults, applying lime, diatomaceous earth, pyrethroid soil drenches, and entomopathogenic nematodes to the soil surrounding A. mellifera hives. Understanding the biology and life history of A. tumida, along with current control methods, can aid apiculturists in making informed integrated pest management decisions. Additionally, understanding critical knowledge gaps in the current research is an important step in identifying promising future management tactics in the ongoing efforts to manage this invasive pest.
Article
In recent years, beekeeping has been affected by many factors, including pesticides, monoculture and deforestation as well as pests and diseases, which are causing the death of Apis mellifera and other pollinating species. One of the most recent threats is a parasitic beetle of bee colonies, native to sub-Saharan Africa, called small hive beetle (Aethina tumida Murray). It was first detected in the USA in 1996, and it has continued to expand across the American continent. In 2015, it was first discovered in Brazil, being the nearest country to Chile where it has been reported to date. The aim of this work was to carry out a literature review on small hive beetle (SHB) as it can be a potential threat to honey bee colonies in Chile. Adults of Aethina tumida feed on bee eggs while the larvae consume brood, pollen and honey, causing great damage to bee colonies. In addition, they defecate in honey, where a yeast present in their faeces, Kodamaea ohmerique, causes pollen and honey to ferment. Due to the damage it causes and its rapid advance through different continents, its biology and behaviour are being increasingly studied to explore control techniques and risk factors.
Article
Full-text available
Bumblebees are important natural pollinators due to their services to wild and cultivated plants. They commonly nest in cavities in the ground where they are exposed to numerous organisms or interact with them. One Bombus pauloensis nest in the Sabana of Bogotá (Colombia) was transferred to an artificial nest and relocated close to a honeybee apiary after the original nest was threatened by an intentional fire. The objective was to preserve the colony and simultaneously identify arthropods associated with a bumblebee nest as this is poorly studied in Colombia. Samples of the organisms found in the bumblebees’ nest were collected for taxonomic identification. Several commensal, scavenger and parasitic organisms were found, including Antherophagus sp. (Coleoptera: Crytophagidae), wireworm beetles (Coleoptera: Elateride), Fannia canicularis (Diptera: Fanniidae), and mites of genera Parasitellus and Pneumolaelaps. This is the first report of other organisms besides Antherophagus from a B. pauloensis nest in Colombia.
Article
Pollinators and the environments where they live are experiencing increasing human impacts leading to changes, primarily declines, in species richness and population abundances. The drivers of pollinator decline vary. Almost every type human resource use leads to some level of loss of habitat. The effects of pollution, particularly heavy metals, pesticides and the role of disease are increasingly recognized as important drivers of pollinator declines, however, significant gaps in our knowledge exist. Of particular concern is the feedback loop between decreasing pollination service, plant inbreeding, declines in nectar quality and further pollinator decline. When viewed in the context of the abiotic and biotic shifts associated with climate change, we suggest that focusing on ensuring there is adequate habitat remaining to provide resilience should be a central strategy for preserving pollinators.
Article
The honeybee nest parasite Aethina tumida (small hive beetle), uses behavioural mimicry to induce trophallactic feeding from its honeybee hosts. Small hive beetles are able to induce honeybee workers to share the carbohydrate–rich contents of their crops, but it is not clear whether the beetles are able to induce to workers to feed them the protein-rich hypopharyngeal glandular secretions fed to the queen, larvae and other nest mates. Protein is a limiting macronutrient in an insect's diet, essential for survival, growth and fecundity. Honeybees obtain protein from pollen, which is consumed and digested by nurse bees. They then distribute the protein to the rest of the colony in the form of hypopharyngeal gland secretions. Using ¹⁴ C-phenylalanine as a qualitative marker for protein transfer, we show that small hive beetles successfully induce worker bees to feed them the protein-rich secretions of their hypopharyngeal glands during trophallaxis, and that females are more successful than males in inducing the transfer of these protein-rich secretions. Furthermore, behavioural observations demonstrated that female beetles do not preferentially interact with a specific age cohort of bees when soliciting food, but males tend to be more discriminate and avoids the more aggressive and active older bees.
Article
Full-text available
The small hive beetle (SHB), Aethina tumida Murray, is a newly introduced coleopteran species attacking honey bees (Apis mellifera L.) from mixed European stock, in North America. This species originates in sub-Saharan Africa, where it is not considered an economic pest. This is in stark contrast to the serious damage caused by this beetle in the southeastern U.S. In the present study, we determined that honey bee subspecies may be an important factor as to why the small hive beetle is not a pest in Africa, but is in the U.S. The Cape bee, Apis mellifera capensis, which has co-evolved with the SHB in South Africa, showed significantly more aggressive behavior toward adult SHB in a laboratory bioassay when compared to behavior of A. m. mellifera. The Cape bee also showed significantly more investigative contacts toward the SHB, when compared to A. m. mellifera. When given the opportunity to feed on Cape bee eggs in South Africa in a laboratory study, the SHB consumed all eggs presented, indicating that the SHB will significantly affect Cape bee brood production if left unmolested by bees. Discussion is given on other possible reasons as to the non-pest status of the SHB in southern Africa, based on previous literature.
Article
Full-text available
The neotropical bumble bee Bombus (Fervidobombus) atratus Franklin is widely dis- tributed in South America ranging from tropical and subtropical lowlands to high altitudes in the Andes. Most of its biology is known from studies conducted in Brazilian lowland forests and almost nothing is known from other areas, especially at high altitudes. Here we provide data on the nest architecture, brood development, worker behavior, seasonal cycle and associated organ- isms from seven colonies of B. atratus observed above 2000 m of altitude in Colombia and Ecuador. Then, we compare them with those data from Brazil. All colonies found were located above the ground, in disturbed areas. Most of the nests either lacked a defined entrance or had a single entrance; a single nest had five entrances, one of them more active than the others. Nests had from 1 to 8 active queens and up to 80 workers indicating monogynous and polygynous cycles as reported from the lowlands. Nests initially lacked an involucrum covering the brood but even- tually developed an irregular involucrum of wax mixed with cardboard and carcasses of B. atratus and their associated beetles (Antherophagus sp., Cryptophagidae). Bees also built pollen pockets attached to larval clusters for feeding larvae. The average developmental time from egg to adult (29.6 days) and the percentage of cells with two pollen pockets (63.6%) were significantly greater than those previously reported. The maximum pocket diameter was significantly smaller, about half of the size, than those diameters observed in lowland colonies. The ecological siwcance of such reduction in size is still unclear but could explain the higher frequency of cells with two pockets in our colony. Nests maintained an internal nest temperature about 12°C warmer than external environmental temperature. Several workers were observed constantly scraping and cut- ting litter on top of one of the nests. Previously this behavior had only been known in Bombus (Fervidobombus) transuersalis (Oliver), a closely related Amazonian species. As in the lowlands, B. atratus colonies at high altitudes seem to be active year-round. The beetle Antherophagus sp. was found in two of the seven colonies observed. They are probably scavengers, but nothing is cer- tainly known about their role within tropical Bombus colonies. Resumen.-El abejorro neotropical Bombus (Fervidobombus) atratus Franklin estA ampliamente distribuido en Sur AmQica, encontrAndose desde las tierras bajas tropicales y subtropicales hasta las grandes altitudes en 10s Andes. Gran parte de su biologia es conocida de estudios realizados en las tierras bajas brasileras y casi nada se conoce de otras Areas, especialmente a grandes alturas. Aqui proporcionamos datos sobre la arquitectura de 10s nidos, ciclo de desarrollo, comportamiento de las obreras, ciclo estacional y organismos asociados de siete colonias observadas a mAs de 2000 m de altura en Colombia y Ecuador. Luego, nuestros datos son comparados con 10s datos de Brasil. Todas las colonias encontradas estaban sobre el suelo, en Areas perturbadas. La mayoria de 10s nidos carecian de una entrada definida o presentaban una sola entrada; un solo nido tenia 5 entradas, una de las cuales era mAs activa que las otras. Los nidos tenian de una a ocho reinas
Article
Three bumble bee (Bombus impatiens Cresson) colonies, each containing 100-200 adult bees and enclosed in separate containment chambers, were artificially infested with 20 small hive beetle (Aethina tumida Murray) adults. A fourth colony was not infested and served as a control. Beetle-infested and control colonies were sacrificed on three separate days to evaluate colony status and beetle population over time. At the termination of the study, between 1,900 and 4,200 small hive beetle larvae, pupae, and new adults were recovered from each of the colonies to which adult beetles were introduced. No adult, pupal, or larval beetles were found in the control colony when sacrificed. In addition, beetle-infested colonies had fewer live adult bees, more dead bees (and a greater proportion of which were no longer intact), and more comb damage than did the control colony. Adult beetles were successfully reared from adult to adult, thus demonstrating their ability to complete an entire lifecycle in association with Bombus colonies. The effects of beetle infestation on a nest scavenger, the Indian meal moth [Plodia interpunctella (Hubner)], are also described.
Article
The small hive beetle (Aethina tumida) is a new threat to beekeepers and is spreading from its original location in South Africa. It is now present in the USA and this article reports its first incidence in Egypt.
Article
This paper examines whether the use of 14 plant species as nectar sources by eight species of bumble bees related systematically to differences in bee morphology. I predicted that a particular bee should have fed from a given plant species if the bee was physically more similar to the other bees visiting that plant species than to bees on any other species. Glossa (=tongue) length, body mass, and wing length all influence a bumble bee's foraging ability and its choice of flowers and were therefore included in the analysis. Morphological differences between bees were associated with use of different plant species; however, the role of bee morphology in flower choice was most evident when preferred plant species bloomed abundantly. The interaction between morphology and flower choice was also influenced by plant species richness, season, the plant species visited, and the species of bee; but was not affected by the time of day that the bee was foraging, overall bee density, or the bee's caste. Bee species with long glossae had access to nectar in a greater variety of flowers than those with short glossae, and they tended to feed from a larger number of plant species. Also, their use of a particular species was less predictable. Discrimination between bees using different plant species depended on joint consideration of several morphological characters: no character alone accurately separated the bees.
Article
In this work, the author gives a morphological description ofAphomia sociella at different stages of its life cycle, that permits the identification of these moths among the sub-family ofGalleriinæ. The depredatory behaviour of wax-moth caterpillars inside the Bumble-Bees' nest has been studied. The larvae ofAphomia sociella are dangerous for Bumble-Bees' nests, not only because they ruin the combs and feed on wax, but also because they inhibit the growth of the offspring. The wax-moth larvae build up a network of tunnels of sticky secreted threads, under cover of which the voracious larvae seek their food. The female of bumble-bee wax-moth lays her eggs in masses, so the newly hatched caterpillars begin their lives in close contact with one another. The tendency that impels the female to lay in masses instead of singly is the first requirement of gregarious behaviour. This gregarious behaviour in caterpillars lasts until later larval stages.
Article
This paper assesses the current status and future prospects for bioregional planning in the Southern Appalachian Man and the Biosphere (SAMAB) region in the United States. The SAMAB region is one of the most biodiverse temperate regions in the world. The region's environment is threatened by development, air and water pollution, and invasive species. Numerous institutions in the region have some responsibility for protecting the region's environment, including the National Park Service, the US Forest Service, the US Environmental Protection Agency, the US Fish and Wildlife Service, several states, hundreds of municipalities, and numerous active non-profit organizations. Twenty-seven people associated with bioregional planning were interviewed to gauge their opinions on the state of bioregional planning in the SAMAB region. Overall, the respondents do not believe that the totality of all those efforts comprises bioregional planning because the efforts are limited in scale and scope and somewhat uncoordinated. With respect to the future of the region, the respondents found it difficult to imagine the state of the region 50 and especially 200 years into the future. Additionally, almost all of their definitions of bioregional planning included a spatial dimension but none included a time dimension. Thus, one of our conclusions is that the future of bioregional planning in the region will be hampered by difficulties people responsible for environmental protection have in dealing with ‘the future’. Much effort needs to be expended to inculcate people in the region with the desire to anticipate problems long before they occur. Reactive responses, which characterize the majority of current efforts, are likely to be ‘too little, too late’.