The neglected bee trees: European beech forests as a home for feral honey bee colonies

Introduction

The habitat of the western honey bee (Apis mellifera L.) in temperate Europe was deciduous or mixed forest, with trees providing both nest cavities and food resources (Seeley & Morse, 1976; Seeley, 1985; Ruttner, 1988; Crane, 1999). However, since the Middle Ages, the life of honey bees in Central Europe has considerably been affected by man. When people started to take colonies to their homes and manage them in beekeeping hives, the habitat of honey bees shifted from woodland areas to the agro-urban space (Crane, 1999; Banaszak, 2009). The logging of old-grown forests and an increase in land-use intensity further reduced the habitat for wild honey bee colonies (De la Rúa et al., 2009; Küster, 2010; Potts et al., 2010). Advances in beekeeping technique allowed for a better control over honey bee reproduction, altering their life-history and limiting natural selection (Loftus, Smith & Seeley, 2016; Neumann & Blacquière, 2017; Brosi et al., 2017). Lastly, the trade in selected honey bee strains by bee breeders across Europe has led to genetic admixture and spread of pathogens and invasive parasites (De la Rúa et al., 2009; Mutinelli, 2011) challenging the health of these important pollinators (Neumann & Carreck, 2010; Meixner, Kryger & Costa, 2015). Today, among the most harmful pests is the ectoparasitic mite Varroa destructor (Anderson & Trueman, 2000), which is infecting virtually all honey bee colonies across Europe (Le Conte, Ellis & Ritter, 2010; Rosenkranz, Aumeier & Ziegelmann, 2010; Nazzi & Le Conte, 2016). There is consensus among researchers and beekeepers that colonies not treated against the mite will usually die within a few years due to both direct damage and associated virus infections (Sammataro, Gerson & Needham, 2000; Moritz et al., 2010; Neumann & Carreck, 2010; Rosenkranz, Aumeier & Ziegelmann, 2010; Martin et al., 2012; van Dooremalen et al., 2012). The question is: what does that mean for feral honey bee colonies, which nest naturally with no human interference? It is widely assumed that since the arrival of the mite, feral honey bee colonies were all but wiped out (Moritz et al., 2007; De la Rúa et al., 2009; Meixner, Kryger & Costa, 2015). However, it has been reported that naturally nesting honey bees colonies are still abundant in large temperate woodlands in North America and the Southern Ural (Seeley, 2007; Ilyasov et al., 2015), and they regularly occupy cavity trees along rural avenues in Northern Poland (Oleksa, Gawroński & Tofilski, 2013). There are two reasons why we should reconsider the common perception about the status of honey bee colonies living wildly in Central Europe: different host-parasite ecology, and a simple lack of data.

In predicting the fate of feral colonies, we usually consult knowledge about honey bee-parasite relationships that was gathered in the context of managed apiaries. It is long recognized, however, that feral colonies generally experience a reduced parasite pressure due to ecological factors (Bailey, 1958). The crowding of honey bee colonies at bee yards increases the risk of erroneous homing by workers (drifting), which boosts epidemic spread among hives and individual colonies’ parasite loads (Fries & Camazine, 2001; Forfert et al., 2015; Seeley & Smith, 2015). Parasite loads were also found to be positively correlated with the colony density at the landscape scale (Frey & Rosenkranz, 2014; Forfert et al., 2016; Nolan & Delaplane, 2017). Because people tend to have their bee yards near settlements, beekeeping activity is not distributed evenly across space, resulting in high local colony densities. A study on parasite pressure of honey bees along an urbanization and management gradient in the Eastern United States, indeed found that parasite burden was both higher in urban as compared to rural locations, and in managed as compared to feral hives (Youngsteadt et al., 2015). In contrast, worker bees of feral colonies in the UK had higher virus infestations than workers of managed colonies (Thompson et al., 2014). However, the sampling was potentially biased towards locations in urban areas with high overall colony densities. The density of naturally nesting colonies in remote woodlands is low and colonies nest individually in widely separated tree cavities (Visscher & Seeley, 1982; Seeley et al., 2015; Seeley, 2017). In addition, the life-history strategy of feral colonies makes them less vulnerable to parasites than beekeepers’ colonies. Naturally nesting colonies stay smaller, rear less brood and swarm frequently, all of which reduces the reproductive potential of Varroa mites. Beekeepers, however, usually prevent swarming and provide unnaturally spacious hives, resulting in large colonies with continuous brood rearing activity (Loftus, Smith & Seeley, 2016; Seeley, 2017). Both empirical and theoretical studies suggest that these factors alone—the spacing of colonies, and their life-history—can reduce the infection levels of V. destructor considerably (Loftus, Smith & Seeley, 2016; DeGrandi-Hoffman, Ahumada & Graham, 2017; Seeley, 2017). Further, it is predicted that under certain conditions, populations of honey bee colonies not treated against parasites will evolve resistance mechanisms against these pests through natural selection (Neumann & Blacquière, 2017). Selection for resistance against Varroa was indeed documented in several studies of both closed and open managed populations that did not receive treatment against the mites (Rinderer et al., 2001; Le Conte et al., 2007; Locke & Fries, 2011; Locke et al., 2012; Kefuss et al., 2015; Locke, 2016; Oddie, Dahle & Neumann, 2017). So far, however, only one population of feral colonies has been studied with respect to its survival and host-parasite ecology: although the new parasite and its associated viruses evidently led to an initial drop in the population sizes of feral honey bee colonies in North America (Kraus & Page, 1995; Mikheyev et al., 2015), a population of honey bees living in the deciduous forests of New York State was found to be stable over decades (Seeley, 2007; Mikheyev et al., 2015; Seeley et al., 2015; Seeley, 2017). This population exhibits genomic signatures of selection after the arrival of Varroa (Mikheyev et al., 2015) and individual bees were found to show intense hygenic and biting behavior against the mites (D. Peck & T. D. Seeley, 2018, personal communication). Interestingly however, a high winter mortality of founder colonies in new nests suggests that the population is more limited by food supply than by parasites (Seeley, 1978, 1985, 2017).

The fact that we owe our knowledge about forest dwelling temperate honey bees almost exclusively to a feral population outside its natural range, from the deciduous forests of New York State (Seeley, 1985), points to the second problem: there are actually no scientific data available about the ecology of feral honey bee colonies in Europe, neither before nor after the arrival of the Varroa mite (Geldmann & González-Varo, 2018). It is often quoted that feral honey bee colonies have always been rare (Ruttner, 1973), but there is no information about their actual abundance and distribution at earlier times. Further, the density of honey bee colonies in temperate woodlands might naturally be very low and nests are extremely cryptic (Seeley & Morse, 1976; Visscher & Seeley, 1989): discovering a honey bee nest by chance and without using specific searching techniques is hence very unlikely. To overcome the difficulty in directly detecting honey bee nests, genotyping of sampled drones or queen offspring with microsatellite markers was used to estimate honey bee colony densities in different regions across their native range (Moritz et al., 2007; Moritz, Dietemann & Crewe, 2008; Jaffé et al., 2010). At sample sites in Europe, inferred colony densities resembled those of known managed colonies, so it was concluded that wild or feral honey bees do not contribute to the population as a whole (Moritz et al., 2007; Jaffé et al., 2010). However, it is probable that the resolution of the method is not precise enough to detect low densities of feral colonies in regions where many more colonies live in managed hives (Arundel, Oldroyd & Winter, 2012, 2013).

Getting precise information about the presence of feral honey bee colonies is important: they need to be considered when estimating overall wild pollinator abundances or when assessing the role of forest areas in providing pollination services to the surrounding land (Tscharntke et al., 2005; Jaffé et al., 2010; Mitchell, Bennett & Gonzalez, 2014; Decocq et al., 2016). The occurrence of feral honey bee colonies in woodlands would also have special implications for the species itself, for example its legal protection status and its perception among bee researchers, forest ecologists and conservationists. Although feral honey bee colonies can be a rich source for studying the natural interaction of honey bees with the forest environment (Seeley, 1985) and they can represent an important reservoir of genetic diversity (Oleksa, Gawroński & Tofilski, 2013), so far, they have got little attention in Europe.

In most parts of Central Europe, beech dominated forests (Fagus sylvatica L.) represent the major type of natural vegetation (Bohn et al., 2004; Tinner & Lotter, 2006; Bolte, Czajkowski & Kompa, 2007), so that increasing efforts are being devoted to the assessment of biodiversity in these forests and to their conservation (Brunet, Fritz & Richnau, 2010; Scherfose et al., 2007). Little is known about the role of beech forests as a home for pollinating insects (Sobek et al., 2009). At first glance, they actually appear to provide limited nectar resources: beech trees are wind pollinated, and mature stands form dense canopies, which limit light transmission to the forest floor and hence the growth of shrubs and other tree species (Packham et al., 2012). However, the wild bee fauna of the Hainich, an ancient beech forest in central Germany, was found to be quite diverse (Sobek et al., 2009). Further, there are historical reports about people hunting for honey in the Carpathians, a region where today’s last primeval beech forests are situated (Gunda, 1968), and honey bees were repeatedly reported to occupy old black woodpecker cavities (Dryocopus martius L.) in beech trees (Meyer & Meyer, 2001; Sikora, 2008; Sikora, Schnitt & Kinser, 2016).

We assumed that near-natural deciduous forests in Germany could provide enough suitable nest sites to be a home for feral honey bee colonies. Here, we made a first assessment of their occurrence and density by using two methods, the tracing of nest sites based on forager flight routes (beelining technique), and the direct inspection of potential cavity trees. Further, we established experimental swarms at forest edges and decoded dances for nest sites performed by scout bees in order to study how far swarms from beekeeper-managed hives would potentially move into a forest.

Methods

Results

Occurrence and density of feral honey bee colonies in beech forests

In total, we detected nine bee trees in the Hainich forest (Fig. 1). All nest sites were located in areas with dense tree canopies. This hampered the determination of exact flight directions near the nest sites and locating the actual cavity tree was infeasible. We therefore determined the approximate location of each bee tree by taking into account the round trip durations of bees foraging at the last feeder and the information obtained at the previous feeding sites (for detailed examples of how we inferred the bee tree locations see Fig. S2). In 2016, we inferred the bee tree locations A, B, C and D. In 2017, we sampled a slightly different area and detected bee tree location D again plus the bee tree locations E, F, G, H and I. This corresponds to an estimated average colony density of 0.13 colonies per square kilometer (0.13 col/km² in 2016, 0.14 col/km² in 2017). While five bee trees lay within the core zone of the National Park, another two lay within its boundaries, and two just outside the boundaries of the National Park. We got to know that in every village around the National Park there is at least one apiary with around 10 managed colonies each. In one case, the inferred location of a potential bee tree (location H) was near the forest edge, so we specifically searched that area for beekeepers’ hives to be sure that the tracked bees came from a feral colony. The approximate mean ± SD distances of the bee trees to the forest border and to the nearest apiary were 980 ± 830 and 2,660 ± 1,080 m respectively (Table 1).

Table 1:

Distances of the inferred bee tree locations in the Hainich forest to the forest edge and to the next apiary.

Bee tree	Distance to forest edge (m)	Distance to next apiary (m)
A	2,350	4,300
B	700	2,600
C	1,700	3,600
D	2,250	4,000
E	550	2,850
F	150	1,500
G	500	1,500
H	<50	1,150
I	550	2,400
Median	550	2,600
Mean	980	2,660
SD	830	1,080

DOI: 10.7717/peerj.4602/table-1

In the beech forests of the Biosphere Reserve Swabian Alb we inspected 98 habitat trees with old black woodpecker cavities for the presence of honey bee colonies (see Fig. S3 in supplemental information for a map of the region). Many of the habitat trees contained more than one cavity (Fig. 2). Seven trees (7.1%) were found to be occupied by honey bees. Based on the density of mapped woodpecker cavity trees in the region, we estimated the density of feral honey bees to be at least 0.11 colonies per square kilometer.

Potential dispersal distances of honey bee swarms

Nest site scouts of three experimental swarms set up around the Hainich forest apparently covered a large area, dancing for nest sites up to 6.5 km away (Fig. 3). However, the majority of dances indicated sites within a few hundred meters around the swarm mounts. Bees of the swarms in Craula and at Mallinde communicated nest sites located in the Hainich forest, but those of the swarm in Weberstedt did not. Potential nest site hot spots (sites which were advertised repeatedly by scout bees) of the swarms in Weberstedt and Craula lay outside the forest, while the swarm at Mallinde showed preferences for nest site at the forest margin. Average median and 95-percentile nest site range for the three swarms were 472 and 2,112 m respectively. On the swarm at Mallinde, which was located closest to the forest, nest site scouts danced for nearer sites than those of the other swarms (Kruskal–Wallis test: χ² = 10.92, P = 0.0049; Dunn’s multiple comparison: Mallinde vs. Weberstedt (P < 0.05*), Mallinde vs. Craula (P < 0.01**), Craula vs. Weberstedt (P > 0.05)).

Discussion

We set out to address a simple question: are there naturally nesting honey bee colonies living in German beech forests? Our results show that the answer is yes, but at low densities. Through the use of beelining technique in the Hainich National Park, where there is no beekeeping activity, we got a picture of the distribution and density of feral colonies in a near-natural beech forest. We found that honey bee colonies were not confined to the forest edges; they were also living deep inside the wood. We inferred a density of around 0.13 colonies per square kilometer. This estimate must be regarded as conservative because we assumed that we would have kept track of any colony in a large area of 2 km around each sampling site. Especially in the core zone of the National Park, there were no opportunities to sample foraging worker bees, so that we might not have sampled the area exhaustively. Further, as we could not exactly locate the actual cavity trees, there might have been more than one bee tree at their inferred locations. Our direct survey of cavity trees in the beech forests of the Swabian Alb corroborated the findings from the Hainich forest that honey bee colonies are regularly inhabiting old tree cavities in beech forests. Our estimates of the lower limit for the colony densities in both woodland areas are similar and are in accordance with the feral colony density estimated in Northern Poland (0.1 colonies/km²) (Oleksa, Gawroński & Tofilski, 2013). However, it is quite low in comparison to the population density of feral honey bee colonies found in the temperate forests of New York State (1.0 colonies/km²) (Seeley, 2007; Seeley et al., 2015).

It is clear that our data present a “snapshot,” without information about the life-histories of individual honey bee colonies. However, we think that they provide some valuable information:

1. The occurrence of feral honey bee colonies in near-natural beech forests is the norm rather than an exception. We found several honey bee nests in both of the two independent woodlands, and in the Hainich forest there were occupied bee trees in both study years. In a pilot beelining tests in a forest area near Würzburg in 2016, we also found feral honey bee colonies.

2. It is clear that the density of feral colonies in a near-natural deciduous forest in Germany is much lower than the density of beekeeper-managed colonies in rural and urban areas, which is generally between one and three colonies per square kilometer (Jones, 2004). However, when using our estimates to extrapolate the total population size of feral honey bee colonies living in German forest stands older than 80 years, we infer a size of 4,400–5,600 colonies, which we think is a noteworthy number.

3. The data gathered in the beech forests of the Swabian Alb provide valuable information for future studies and conservation. We hypothesize that the abundance and activity of black woodpeckers is a key factor determining the density of cavities that are large enough for honey bee colonies in managed forests. Beech trees with a diameter at breast height of about 40 cm, which start to be attractive for the woodpecker (Taux, 1976), still have intact sapwood and bark. However, the bird is capable of identifying fungal activity in a tree’s central heartwood and can make cavities in trees that would otherwise lack any microhabitat structures (Zahner, Sikora & Pasinelli, 2012). Interestingly, the black woodpecker reached its present day population size in Central Europe not before the 1950s, probably as a response to the recovering forests (Cuisin, 1985; Blume, 1996). This suggests that protecting large habitat trees in managed forests not only helps charismatic forest birds, but can also promote the occurrence and abundance of feral honey bee colonies.

4. We found that scout bees of swarms set out around the Hainich forest advertised several nest sites within short distances, mostly outside the forest. On the swarm which was set up closest to the forest edge, scout bees advertised nest sites at closer distances than those of the other swarms, possibly because there were even more suitable nest sites nearby. Prior studies documented similarly short dispersal distances (modal value: 450 m) (Lindauer, 1955; Seeley & Morse, 1977; Seeley, 2010), suggesting that honey bee swarms will always make the most economical decision and move little when suitable nest sites are close by (Seeley, 2010). Our data suggest that there are suitable nesting sites for honey bee colonies in the agro-urban space, and that a beech forest like the Hainich provides ample, but not necessarily better nesting opportunities. Given that the median distance of advertised nest sites in our swarms was only 470 m, the bee trees in the Hainich forest, which were located at a median distance of 2,600 m from the next apiaries, were probably not colonized by swarms from beekeepers’ hives in single dispersal events.

Forest dwelling feral honey bee colonies live in another environment than managed colonies and are subjected to natural selection: they nest in widely spaced tree cavities, no one treats them against parasites, nor are they fed in times of nectar scarcity. There needs to be a certain network of tree cavities for a noteworthy number of feral colonies to persist in any region. This basic requirement seems to be at least partially fulfilled in near-natural or ecologically managed deciduous forests or where there are networks of forest fragments and rural avenues lined with old trees (Oleksa, Gawroński & Tofilski, 2013). It will be interesting to study the life-history traits of feral honey bee colonies in European landscapes and to pose questions such as the following: What is the average longevity of feral colonies and what is the lifetime reproductive success of their queens? Is the number of feral colonies actually limited by parasites in the first place? Or is it the availability of suitable cavities, or resource limitation that keeps feral honey bee colonies at low densities? Understanding and comparing the drivers of the feral honey bee colony density in different woodland areas will also help to answer the question how frequent honey bees would naturally be in temperate Europe.

Irrespective of the fate of individual colonies, the regular nesting of honey bees in woodlands has ecological impacts. Beekeeping activity is not distributed equally across the country but concentrated in rural and urban areas. Managed hives are usually only occasionally moved into the forests (Banaszak, 2009). Consequently, this leads to an uneven distribution of foraging worker honey bees in the landscape, regardless of differences in resource availability among habitats. However, when there are feral colonies living in a forest, the density of foraging workers in that area will increase, with possible consequences for the pollinator community composition of forest dwelling plants (Steffan-Dewenter & Tscharntke, 2000; Mallinger, Gaines-Day & Gratton, 2017; Hung et al., 2018). This is also relevant if the density of feral colonies is low. Based on their colony size and the proportion of foraging workers, it must be assumed that a single honey bee colony sends out up to 5,000 foraging bees daily (Seeley, 1985). When such colonies live in forest fragments surrounded by arable land, they may also contribute to the pollination of nearby crops (Mitchell, Bennett & Gonzalez, 2014; Decocq et al., 2016). Another point is that feral honey bee colonies will directly or indirectly interact with other organisms that live in hollow trees. They certainly compete for tree cavities that are also attractive to other animals (Johnsson, Nilsson & Tjernberg, 1993; Sikora, Schnitt & Kinser, 2016). Further, as they transport nutrients to their nests, honey bee colonies are hotspots of accumulated biomass: individuals can directly be preyed upon and consumed by birds, mammals and other insects (Morse & Nowogrodzki, 1990). And through the drop of organic matter like wax, pollen, or dead bees, honey bee nests indirectly nourish a whole cosmos of organisms that live from organic detritus inside tree cavities. As tree cavities with dead organic matter are generally rare in managed forests, the presence of honey bees could have a positive effect on the abundance of specialized arthropod communities in European beech forests (Möller, 2009; Müller et al., 2014).

Conclusion

Our study showed that honey bee colonies nesting naturally in tree cavities are more common than it is generally assumed. When assessing the impact of honey bees on ecosystems, or when evaluating the need for their conservation, one should differentiate between managed colonies aggregated in apiaries and feral colonies living singly in natural nests. In Europe, A. mellifera is treated as a domesticated animal and feral honey bee colonies lack any legal protection. There is a lot to be investigated about the life of feral honey bees and their interactions with the (forest) environment. However changing the perspective and recognizing that the honey bee can also live as a wild animal is a prerequisite for achieving a full understanding of its biology.

Supplemental Information