Warning signals confer advantage to prey in competition with predators: bumblebees steal nests from insectivorous birds

The study was conducted in the slopes of the Gwanak Mountain that surround Seoul National University campus in Seoul, South Korea. Many bumblebees, including the common Korean bumblebees, Bombus ardens and Bombus ignitus, require cavities for nesting (Sakagami and Katayama 1977), and accept artificial nestboxes made for bumblebees (Yoon et al. 2002). The bumblebee nestboxes resemble bird boxes but they are smaller, have smaller entrance holes, and contain plant material for insulation (Fye and Medler 1954; Goulson 2010; Lye et al. 2011). The queens emerge and search for suitable breeding cavities around the same time when cavity nesting Oriental tits (P. minor) and Varied tits (P. varius) approach their peak of nest building and egg laying activity (Choi et al. 2007; Hannan et al. 1997; Lee et al. 2011; Rhim et al. 2011). By providing avian nestboxes in a forest where natural cavities are rare, we observed the competition between tits and bumblebees for the nestboxes.

Sixty and 122 nestboxes were monitored in the mixed forests of the Gwanak Mountain (N 37 27.46 E 126 56.81; altitude between 102 and 248 m) in 2010 and 2011, respectively. The size of the nestboxes was 11 × 15 × 25 cm, and the entrance hole had a diameter of 3.5 cm. They were hung 2.50–3.50 m above the ground on the tree trunks at least several months before the breeding season. This was a part of ecological research on tits, and nestbox checking schedule differed between the 2 years. In 2010, nestboxes were checked once in 1–2 weeks in April and May. In 2011, they were checked twice a week from early April till the end of June. The breeding status of birds in each nestbox was classified as one of the three categories: Empty—box empty or with only a small amount of mosses, the typical material used by tits (less than 1 cm layer, usually much less), Nest Present—advanced nest-building stage (more than 1 cm layer of mosses; usually almost a full nest present) or egg laying, and Bird Present—eggs or nestlings present. Categories Empty and Nest Present differed clearly in the absence/presence of plant materials required for bumblebees to set up their nests in the nestboxes, but they did not differ in terms of the long-term presence of a bird inside the box (because tits visit the nestbox with plant materials and stay for a short time during nest building, a bird is absent from those nestboxes for most of the day time). Categories Nest Present and Bird Present differed mostly in the presence/absence of a bird (incubating eggs or hatchlings), which may affect bumblebee’s attempts and success in invading the nestbox.

We treated each year separately because of different monitoring schedule (see above). In 2011, we were able to categorize the stage of nesting at the date when the bumblebee was first recorded due to frequent nestbox check. All recorded bumblebee invasions occurred between 20.04.2011 and 23.04.2011. This corresponded to about 1-2 weeks after the first sightings of bumblebee females actively searching for nest sites in our study area. In 2010, we did not check the nestboxes frequently but one of the visits was conducted on the 22nd of April 2010, a date similar to the dates of bumblebee invasions into nestboxes in 2011. Therefore, the nestbox category on the 22.04.2010 was used in the analysis of 2010 data, assuming that the status on this date represented the status at the moment of bumblebee intrusion (unknown to us for 2010). Two weeks after this date, during a consecutive nestbox check, no new invasions were recorded.

We used these data to compare the distribution of nestbox status categories among all nestboxes with the distribution among nestboxes where bumblebees were recorded. The presence of a bumblebee in a nestbox at a given stage (Empty, Nest Present, or Bird Present) indicates that the bumblebee invaded the nestbox at this or the earlier stage(s). To test the idea that bumblebees preferentially attempt to settle in those boxes in which nest material is already present, we compared the frequency of nestboxes with bumblebees at the stage of Empty with the nestboxes at the stage of Nest Present, i.e., when the bird’s presence in the box was minimal but the substantial amount of the nest material was already present.

To evaluate the idea that bumblebees attempt to settle less often in those nestboxes in which the bird is already incubating or brooding than in those at an earlier stage, before the birds are almost constantly present in the nestbox and may defend it, we compared the frequency of nestboxes with bumblebees between nestboxes at the stage of Nest Present with the nestboxes at the stage of Bird Present.

We can be certain that the bumblebee individuals were different each year which assures the independence of our data. However, the tits were not individually marked, and we cannot exclude the possibility that some pairs of tits were recorded twice in two study years. Therefore there is some possibility of lack of independence for a (probably) small portion of our data points that might have been collected from nests of the same birds. Considering this, for each of the two hypotheses, we analyzed the data separately for each year, viewing them as two, fairly (albeit not entirely) independent, tests of the same hypothesis. Because the focal animals, whose behavior is characterized, are the bumblebees and not the tits, we considered that this partial violation of independence may not cause serious problem for our main conclusions. We used Fisher’s exact test in Statistica (StatSoft—Tulsa, USA). All P values are two-tailed.

To test the idea that the warning defensive buzzing by bumblebees contributes to nest abandonment by the birds, in 2012 we conducted field experiments in which we recorded behavioral responses of incubating birds to the bumblebee buzz. However, to minimize the negative effect of research procedures on the breeding success of birds, we decided to conduct experiments in nests that were at the late incubation stage, when birds are less sensitive to disturbance. Typical daily incubation pattern of the Great tit (Parus major), a species very closely related to the Oriental tit (Päckert et al. 2005), involves long bouts of incubation, each lasting for an average 30 min (Bryan and Bryant 1999), and each followed by a short bout (on average 8 min; Bryan and Bryant 1999) of foraging or other activities performed by a female after she leaves the nestbox. Hence, a female who just left a nest at the incubation stage is expected to come back within a relatively short time (about 20 min in our study site), to enter the box and to stay there for a relatively long time (half an hour or more in our study site, if not disturbed). We used this situation to study the effect of a sudden auditory disturbance, combined with the presence of a bumblebee model within the nest material, on the reaction of a female who just entered the nest and started the incubation session. We predicted that any sudden disturbance inside the nest may lead to the disruption of the normal incubation behavior, and that the disturbance consisting of the bumblebee buzz will affect the normal incubation behavior especially strongly.

In the 2012 breeding season, we conducted playback experiments in 11 nestboxes at the stage of late incubation/early feeding (i.e., 1–2 days old nestlings that were brooded by the bird). Each incubating female was tested in two conditions, bumblebee buzz (Buzz treatment) and bird song (Bird treatment, which serves here as a control) separated by 1–2 days. In six nests, the Buzz treatment was the first, while in the remaining five nests the Bird treatment was the first condition. In both treatments, the playback was delivered through a modified speaker (Fig. 1a). In the middle of the speaker, we glued a 1-cm-long toothpick with a dead bumblebee onto its end. This set (speaker with a bumblebee) was hidden in the nest material, such that the bumblebee model was partially visible but the speaker was not visible to the bird (Fig. 1b). We monitored the behavior of the incubating bird using a small video camera located at the ceiling of the box and with a miniature microphone attached to the camera. For the Buzz treatment, we played the buzz of bumblebees recorded in one of the nestboxes occupied by the bumblebees in 2012. For a Bird treatment, we used songs of the birds most commonly heard in the study area: the cuckooing sound of the Little Cuckoo (Cuculus poliocephalus) in May and the vocalizations of Brown-eared bulbul (Hypsipetes amaurotis) in June. The bumblebee and bird recordings (Tsuruhiko and Michio 1996) were edited to last for 3 s and to play at approximately similar amplitude (according to human perception). For each playback experiment a different recording was used (different bumblebee recording or a different section of the commercially available recordings; Tsuruhiko and Michio 1996). For the graphical representation, the observations were scored in the following way: 1 = some reaction, but not flying out; for example, raising the body and keeping it raised, going to the side of the box, going to the entrance but not flying out, pecking at the bee or nearby; 2 = female reacted by flying out. For the statistical analysis we only used the binary variable indicating whether the playback affected the female (1) or not (0), and we used one-tailed McNemar statistics with continuity correction to test the hypothesis that the Buzz treatment affected females more strongly than the Bird treatment did.

Open image in new window

To determine if the reaction to the bumblebee buzz, observed in the nestbox playback experiments, is innate or learned, we tested reactions of 11 hand-raised Oriental tits (age 30–60 days). The experimental birds were hand raised. They were fed with crickets (Acheta domestica), mealworms (Tenebrio molitor), silkworms (Bombyx mori), and seeds (sunflower, walnuts, and peanuts) using tweezers and feeding containers. We tested their reactions in response to the vibration of the buzz being played through the toothpick glued on a speaker (the same speaker that was used in nestbox experiment; Fig. 1a) while the tit touched the toothpick to eat a small amount of butter on the tip (Experiment 1). To determine if tits avoid bumblebees using visual cues, we presented a dead bumblebee, held in the tweezers, to the 11 hand-raised Oriental tit fledglings (Experiment 2). Each presentation lasted 30–45 s.

In both experiments, we classified the response of the bird as “+” if the bird moved away and did not approach the toothpick again (Experiment 1), or if a bird clearly avoided probing/pecking at the dead bumblebee (Experiment 2). Otherwise we scored the bird’s response as “−”, indicating a lack of avoidance to either auditory/tactile (Experiment 1) or visual (Experiment 2) bumblebee-specific cues. Additionally, we described the manner in which the birds behaved during those tests. The same birds were used in both experiments. All birds were first tested with the toothpick and the sound stimulus, and several days later with the dead bumblebee on a toothpick. Every day the birds were fed butter on a toothpick multiple times to erase any possible association with the experimental cue (presented only once to each bird).