Flight behaviour during foraging of the social wasp Vespula vulgaris (Hymenoptera: Vespidae) and four mimetic hoverflies (Diptera: Syrphidae) Sericomyia silentis, Myathropa florea, Helophilus sp. and Syrphus sp.
1 Faculty of Life Sciences, University of Manchester, 3.614 Stopford
Building, Oxford Road, Manchester M13 9PT, UK
2 Department of Environmental Management, University of Central Lancashire,
Preston PR1 2HE, UK
* Author for correspondence (e-mail: r.ennos{at}manchester.ac.uk)
Accepted 14 October 2005
![]() |
Summary |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Key words: flight, mimicry, Syrphidae, behaviour
![]() |
Introduction |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Rettenmeyer (1970) predicted that behavioural mimicry would be especially
important among mimics of Hymenoptera because the behaviour of their model is
so conspicuous. Hoverflies that are Batesian mimics of Hymenoptera should
therefore be expected to exhibit close behavioural convergence with their
models. Such similarities have indeed been detected in the foraging behaviour
of droneflies Eristalis tenax and their supposed model the honeybee
Apis mellifera ; they spend similar amounts of time foraging on
individual flowers and flying between flowers
(Golding and Edmunds, 2000).
Films of insects flying between flowers also showed that the droneflies
behaved more like honeybees than like other flies, despite their very
different ecology; they flew at similar speeds, took similar routes, and
performed similar loops in their flight path.
(Golding et al., 2001
).
Golding et al. (2001
)
concluded that droneflies may have adapted their behaviour to appear more like
their models at a time when they are particularly vulnerable to predation (as
had earlier been suggested by Dlusski,
1984
), and that this is a clear case of mimetic flight
behaviour.
Many other hoverflies are thought to be Batesian mimics of social wasps,
gaining protection from their predators by their mimicry
(Howarth et al., 2000). Some
species such as Temnostoma vespiforme or the tropical Milesia
vespoides are considered very precise morphological mimics of social
wasps (Wickler, 1968
;
Torp, 1994
). In Britain there
are no such perfect mimics, but there are several species that have been
described as specific or non-specific wasp mimics
(Howarth et al., 2000
) of
which four are common and widespread. Sericomyia silentis, is
considered to be a specific wasp mimic
(Howarth et al., 2000
). It is
a large fly of wing length 11 to 14 mm (Stubbs and Falk, 2002) which has
conspicuous black and yellow markings and a pigmented leading edge to its
wings. It looks particularly wasp-like when hanging upside down whilst
foraging on flowers (M.E., Y.G., personal observation) and is especially
abundant in August and early September when workers of social wasps
Vespula vulgaris are most numerous and reach their maximum size, with
a wing length, like Sericomyia of 1114 mm
(Zahradnik, 1991
).
Three other common hoverflies: Syrphus sp. (wing length
7.2511.5 mm), Helophilis sp. (wing length 8.511.25 mm)
and Myathropa florea (wing length 712 mm) are considered to be
non-specific mimics of wasps (Howarth et
al., 2000). They are all smaller than social wasps (Stubbs and
Falk, 2002) but have similar black and yellow markings on the abdomen and
yellow and black legs, while Helophilus also has yellow longitudinal
stripes on the thorax.
It might be expected that all these flies, and especially the better mimic,
Sericomyia, would show mimetic flight behaviour to wasps: in
particular that they might mimic the slow speed, and characteristic zigzag
orientation movements which wasps use when leaving their nest or approaching
foraging sites (Gaul, 1951;
Collett and Lehrer, 1993
).
There are indeed many anecdotal reports that some hoverfly species appear
wasp-like in flight (Wickler,
1968; Stubbs and Falk,
1983
; Morgan and Heinrich,
1987
; Azmeh, 1999
;
Howarth et al., 2000
), but few
studies have empirically measured these behaviours. In this study, therefore,
we compared the flight behaviour when foraging on flowers of the social wasp
Vespula vulgaris and the four supposed hoverfly mimics to determine
whether these species showed mimetic flight behaviour. We analysed gross
aspects of flight, including velocity, flight routes and time spent hovering;
such behaviours will all be highly visible to potential predators.
![]() |
Materials and methods |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The insects were social wasps (Vespula vulgaris L.) and their
black and yellow hoverfly mimics: Sericomyia silentis Harris;
Myathropa florea L.; Helophilus (two very similar species,
pendulus L. and the much rarer hybridus Loew); and
Syrphus (two very similar species, ribesii L. and the much
rarer vitripennis Meigen). Because it proved impossible to
distinguish between the sister species in the field, they were classified as
either Helophilus sp. or Syrphus sp. This is justified
because, as other authors (Stubbs and
Falk, 1983; Howarth et al.,
2000
) have noted, these species not only look similar but behave
in a similar manner. In total 109 flights between flowers 10 cm apart were
captured that were performed by 53 individuals of the five species. For
analysis, each flight was taken as an independent observation. This was
justified because for all but Helophilus (where one individual made
nine flights) each individual made only one to four flights. Because different
individuals behaved in similar ways, a separate analysis, using mean figures
for individual insects, gave almost identical results.
The flight trajectories that insects took between the flowers were
established by stopping the film frame by frame and marking the position of
the head on transparent OHP film. From the OHP films the total distance flown
between each flower was measured by following the path with a digital map
measurer. The precise straight-line distance between the point the insect took
off from one flower and landing on an adjacent flower 10 cm away was also
measured. This allowed the ratio of distance travelled by the insect to the
shortest distance between flowers (the deviation) to be calculated (see also
Chai and Srygley, 1990). The
average speeds at which the insects flew between flowers were calculated by
dividing the total distance by the time spent flying, knowing that each frame
represented a time lapse of 0.04 s. Time spent hovering was excluded from the
calculations of flight velocities. Hovering was identified as episodes when
the insects moved less than 2 mm per frame (a speed of less than 5 cm
s1).
Results were tested for normality using the Kolmogorov-Smirnov test. All except hovering time proved to be normally distributed. The means for the different species were compared using a one-way ANOVA. A post hoc Dunnett C test was then carried out to detect which, if any, of the fly genera showed different flight behaviour from their presumed wasp model.
![]() |
Results |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
|
Do insects take different routes between flowers?
Mean deviations of the five genera are shown in
Fig. 2. The ANOVA showed that
there was a significant difference between species
(F4,105=6.633; P=<0.001). The Dunnett C test,
comparing each hoverfly mimic with the model, failed to show a significant
difference between the wasp and Syrphus (P=0.305) but did
show significant differences between the wasp and Sericomyia
(P=<0.001); Helophilus (P=0.003) and
Myathropa (P=0.016).
|
|
How much time do insects spend in hovering?
Helophilus hovered on three occasions out of 25 flights, each bout
of hovering occupying three to five frames (i.e. 0.120.16 s), whereas
Syrphus hovered on 17 occasions out of 35 flights with each bout
taking between five and 15 frames (0.20.6 s). Sericomyia and
Myathropa were never observed to hover during 20 and 18 flight
sequences, respectively. Wasps were classed as hovering only once in 21
flights, i.e. when the side-to-side movements of the insect in front of
flowers were so small that it appeared to be hovering. A Chi-squared test
showed that these differences in frequency of hovering between genera were
indeed significant (24=50.3;
P<0.001).
![]() |
Discussion |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
The results were very clear. Syrphus sp. showed more similar flight behaviour to its wasp model than did the other three hoverfly mimics, both in the speed flown between flowers, and in the routes taken; it flew more slowly and deviated more from a straight line, like the wasp. In particular there were similarities between Syrphus and Vespula in their behaviour just before landing. The wasps moved from side to side in front of flowers before alighting on them to feed, giving an overall impression of a jerky zigzag movement (see Fig. 1). This is consistent with orientation flights of social wasps approaching a feeder as described by Collet and Lehrer (1993). Syrphus individuals also invariably hesitated before alighting on flowers, sometimes moving from side to side as if inspecting the flowers before landing (see Fig. 1), at other times moving so little that these episodes were recorded as hovering. Syrphus was the only hoverfly in this study to do this, although it can also be observed in the smaller black and orange-yellow hoverfly Episyrphus balteatus. Our other hoverflies rarely hovered, seeming to fly without hesitation from one flower to another.
There is no obvious reason why Syrphus (and E. balteatus)
should adopt this zig zagging behaviour as they are neither predatory (as
adults) nor aposematic. They may be inspecting the flowers for predatory crab
spiders which sit about on flowers waiting for prey, or indeed for wasps, but
if this was the case we should also expect Helophilus and
Myathropa, which are similar-sized flies, to hover more frequently.
An obvious remaining explanation is that Syrphus has modified its
flight behaviour to resemble that of wasps, just as droneflies have modified
their flight behaviour to resemble that of honeybees
(Golding et al., 2001). The
zigzagging behaviour could be readily achieved by both the wasp and the fly by
altering the dorsal and ventral end points of their wingbeat without having to
alter the orientation of their bodies
(Ennos, 1989
;
Dudley, 2000
). There is
certainly no reason to believe that, as in mimetic butterflies, the flight
resemblance is due to their morphological resemblance. Syrphus is
much smaller than social wasps; Diptera have a quite different flight
apparatus from Hymenoptera; and Syrphus is capable of extremely
precise flight (Ellington,
1984
).
So why should an apparently imprecise mimic of wasps show such good flight
mimicry while the three other hoverflies, of which at least one
(Sericomyia) appears a better morphological mimic, did not? One
reason might be that the bird predators of hoverflies see them in a different
way from entomologists. Dittrich et al.
(1993) demonstrated, for
instance, that to pigeons that were shown slides of insects, Syrphus
ribesii appeared more similar to wasps than Helophilus
pendulus. Clearly, pigeons are not insectivorous birds, so these results
may not be very relevant to real life, but it could be that Syrphus
ribesii is to insectivorous birds an excellent mimic both morphologically
and behaviourally.
Another reason may be that different aspects of mimicry, both morphological and behavioural, may not be closely linked. Syrphus may compensate for a poor resemblance to its model by showing better flight mimicry. In contrast, the specific mimic Sericomyia, may be protected adequately by its morphological resemblance and its extremely wasp-like behaviour when foraging on flowers. Taking faster more direct paths between flowers, which would increase the speed and efficiency of foraging, may not, therefore, significantly compromise its mimicry.
Several pieces of evidence make this explanation plausible. First,
droneflies, which are also non-specific mimics, in their case of honeybees
(Howarth et al., 2000), also
show good flight mimicry (Golding et al.,
2001
). Second, it fits in with observations of the behaviour of
these flies when startled. Sericomyia adopts jerky zig-zag flight
when alarmed, so it may adapt its flight behaviour to appear more wasp-like
only when directly threatened. Howarth et al.
(2000
) suggest this is also
the case for Helophilus. By contrast, Syrphus will fly off
very rapidly if threatened by a sudden movement, showing it has retained its
ability for fast flight; we recorded a mean velocity of 1.47 m
s1 over the first 29 cm of one such escape flight, and an
acceleration of over 20 m s2. We plan to further investigate
alarmed flight behaviour of hoverflies to test this hypothesis.
This line of argument suggests that in hoverflies the evolution of
behavioural mimicry may precede, as well as follow, the evolution of precise
morphological mimicry. Kassarov
(2003) suggested in relation
to butterfly mimicry, that birds may detect movement better than the fine
details of pattern and coloration. Therefore a hoverfly that shows a small
degree of morphological similarity, may face stronger selection pressure for
behavioural convergence than morphological convergence. It may also be
`easier' genetically to change behaviour than to change morphology. An
individual animal can alter its behaviour as a result of some experience (e.g.
birds can learn to avoid wasps), and some altered behaviours may result in
behavioural mimicry. Only later does such an acquired behaviour become
incorporated into the animal's genome.
That behavioural mimicry may be unlinked to morphological mimicry is also suggested by a behavioural convergence shared by all four of these quite different hoverfly species; they all make large amplitude dorsoventral movements of their abdomen while they are foraging on flowers. These movements, which are absent in non-mimetic flies, superficially resemble the ventilation movements of the abdomens of Hymenoptera (Heinrich, 1979). A probable explanation for these movements in hoverflies is that they improve their resemblance to hymenopterans and that by emphasising the abdomen and further displaying their warning coloration, they suggest that they might also be able to sting. Clearly, further studies of other mimetic hoverflies and other mimetic behaviours are required to uncover the relative roles of morphological and behavioural mimicry.
![]() |
References |
---|
![]() ![]() ![]() ![]() ![]() ![]() ![]() |
---|
Azmeh, S. (1999). Mimicry in the hoverflies. PhD thesis, University of Nottingham.
Bates, H. W. (1862). Contributions to an insect fauna of the Amazon Valley, Lepidoptera: Heliconidae. Trans. Linn. Soc. Lond. 23,495 -566.
Brower, A. V. Z. (1995). Locomotor mimicry in butterflies? A critical review of the evidence. Phil. Trans. R. Soc. Lond. B 347,413 -425.
Carpenter, G. D. H. and Ford, E. B. (1902). Mimicry. London: Methuen.
Chai, P. (1986). Field observations and feeding experiments on the responses of rufous-tailed jacamars (Galbula ruficauda) to free-flying butterflies in a tropical rainforest. Biol. J. Linn. Soc. 29,161 -189.
Chai, P. and Srygley, R. (1990). Predation and the flight, morphology, and temperature of neotropical rain-forest butterflies, Am. Nat. 135,748 -765.[CrossRef]
Collett, T. S. and Lehrer, M. (1993). Looking and learninga spatial pattern in the orientation flight of the wasp Vespula vulgaris. Proc. Roy. Soc. Lond. B 252,129 -134.
Cott, H. (1940). Adaptive Colouration in Animals. London: Methuen.
Dittrich, W., Gilbert, F., Green, P., McGregor, P. and Grewcock, D. (1993). Imperfect mimicry: a pigeon's perspective. Proc. R. Soc. Lond. B 251,195 -200.
Dlusski, G. M. (1984). Are dipteran insects protected by their similarity to stinging Hymenoptera? Bull. Mosk. O-Va Ispytatelei Otd Biol. 89,25 -40.
Dudley, R. (2000). The Biomechanics of Insect Flight. Princeton: Princeton University Press.
Ellington, C. P. (1984). The aerodynamics of hovering insect flight. III. Kinematics. Phil. Trans. R. Soc. Lond. B 305,41 -78.
Edmunds, M. (1974). Defence in Animals. Harlow: Longman.
Ennos, A. R. (1989). The kinematics and aerodynamics of free flight of some Diptera. J. Exp. Biol. 142,49 -85.
Fisher, R. A. (1930) The Genetical Theory of Natural Selection. Oxford: Clarendon Press.
Gaul, A. T. (1951). Additions to vespine biology VII. Orientation flight. Bull. Brooklyn Ent. Soc. 46,54 -56.
Golding, Y. C. and Edmunds, M. (2000). Behavioural mimicry of honeybees (Apis mellifera) by droneflies (Diptera: Syrphidae: Eristalis sp.). Proc. R. Soc. Lond. B 2677,903 -909.
Golding, Y. C., Ennos, A. R. and Edmunds, M.
(2001). Similarity in flight behaviour between the honeybee
Apis mellifera (Hymenoptera: Apidae) and its presumed mimic, the
dronefly Eristalis tenax (Diptera: Syrphidae). J. Exp.
Biol. 204,139
-145.
Heinrich, B. (1978). Bumblebee Economics. Cambridge: Harvard University Press.
Howarth, B., Clee, C. and Edmunds, M. (2000). The mimicry between British Syrphidae (Diptera) and Aculeate Hymenoptera. Br. J. Ent. Nat. Hist. 13, 1-40.
Kassarov, L. (2003). Are birds the primary selective force leading to evolution of mimicry and aposetmatism in butterflies? An opposing point of view. Behaviour 140,433 -451.[CrossRef]
Mallet, J. and Gilbert, L. E. (1995). Why are there so many mimicry rings? Correlations between habitat, behaviour and mimicry in Heliconius butterflies. Biol. J. Linn. Soc. 55,159 -180.[CrossRef]
McIver, J. D. and Stonedahl, G. (1993). Myrmecomorphy: Morphological and behavioural mimicry of ants. Annu. Rev. Entomol. 38,351 -379.[CrossRef]
Morgan, K. R. and Heinrich, B. (1987). Temperature regulation in bee- and wasp-mimicking syrphid flies. J. Exp. Biol. 133,59 -71.
Mueller, F. (1879). A remarkable case of mimicry in butterflies. Proc. R. Ent. Soc. Lond. 1879,20 -24.
Oliveira, P. S. (1988). Ant-mimicry in some Brazilian salticid and clubionid spiders (Araneae: Salticidae; Clubionidae). Biol. J. Linn. Soc. 33,1 -15.
Rettenmyer, C. W. (1970). Insect mimicry. Annu. Rev. Ent. 15,43 -74.[CrossRef]
Srygley, R. B. (1994). Locomotor mimicry in butterflies? The associations of positions of centre of mass among groups of mimetic, unprofitable prey. Phil. Trans. R. Soc. Lond. B 343,145 -155.
Srygley, R. B. (1999a). Locomotor mimicry in Heliconius butterflies: contrast analyses of flight morphology and kinemetics. Phil. Trans. R. Soc. Lond. B 354,203 -214.[CrossRef]
Srygley, R. B. (1999b). Incorporating motion into investigations of mimicry. Evol. Ecol. 13,691 -708.[CrossRef]
Srygley, R. B. and Dudley, R. (1993).
Correlations of the position of centre of body mass with butterfly escape
tactics. J. Exp. Biol.
174,155
-166.
Srygley, R. B. and Ellington, C. P. (1999a). Estimating the relative fitness of local adaptive peaks: the aerodynamic costs of flight in mimetic passion-vine butterflies Heliconius. Proc. R. Soc. Lond. B 266,1 -7.[CrossRef][Medline]
Srygley, R. B. and Ellington, C. P. (1999b). Discrimination of flying mimetic, passion-vine butterflies Heliconius.Proc. R. Soc. Lond. B 266,2137 -2140.[CrossRef]
Stubbs, A. E. and Falk, S. J. (1983). British Hoverflies. London: The British Entomological and Natural History Society.
Torp, E. (1994). Danmarks Svirrefluer (Diptera: Syrphidae). Stenstrup: Apollo Books.
Turner, J. R. G. (1965). Evolution of complex polymorphism and mimicry in distasteful South American butterflies. Proc. Int. Congr. Ent. 12,267 -291.
Wickler, W. (1968). Mimicry in Plants and Animals. London: World University Library.
Zahradnik, J. (1991). Bees, Wasps and Ants. London: Hamlyn.