Bumble Bee Colony Maintains Nest Site despite High Disturbance Level

Abstract

During the 2021 spring a Bombus terricola Kirby queen initiated a nest in the hollow iron front axle of a 1950 John Deere 40U tractor that was being repaired outside in Bowdoinham, Maine. The tractor was not moved during the lengthy repair period, from 15 April–10 June. Seven workers were observed flying out from the tractor axle upon starting it up on 10 June. The tractor was used 1–3 times a week between 15 June and 15 August, usually for 15–90 min at a time. The tractor was always returned to the same location after use. Based upon observed adults issuing from the tractor upon startup throughout the summer, the colony appeared to have survived long enough to produce gynes (next year’s queens).

1. Introduction

Bumble bees are key pollinators in both natural and agricultural landscapes. One reason that they are so important is that they can fly and pollinate plants in north temperate regions where the spring weather is cold and wet [1]. They can even fly and pollinate flowers when it is snowing (personal observation). The physiological basis behind this is the ability to produce an internal body temperature that can exceed the air temperature in which they forage in the spring [2]. This is done by shunting blood to the thorax and heating from the metabolic heat produced by “shivering” the large wing muscles. Another reason that they are important is that they are efficient pollinators of plants with poricidal anthers. Bumble bees possess a behavior linked to a physiological mechanism that sonicates floral anthers (often referred to as buzz pollination). This allows them to extract pollen from flowers that many bees have difficulty with [3,4].

Bumble bees appear to be opportunistic in their nesting and colony founding. The major landscapes that they have been reported to nest in are predominantly grasslands, forests, and non-tilled agricultural landscapes [5]. Other landscapes of lesser importance are urban, forest edges, alpine and tropical forests [5]. Apparently, these nest construction habitats are characterized by soils that are well drained agricultural field edges, pastures, meadows, forest edges and openings, but not the more water saturated soils in wetlands. However, the predominance of agricultural habitats as nesting habitat is thought to be due to a sampling bias that has not equally included other habitats in bumble bee nest surveys [5].

Nesting sites that they have been reported are locations underground in gardens, flower beds, short grass meadows, under woody hedges and fence rows, in bird nest boxes, compost piles and bins, tree holes in forests, under patio stones, in cracked house foundations, old car seats, mattresses, and many more substrates [5,6,7,8,9,10]. The predominant nest site is underground [5]. Many of the underground nesting sites are associated with abandoned rodent nests [5,10]. In addition to soil habitats, some species nest above ground in tree holes. Bombus spp. will also use artificial nests constructed for the purpose of attracting bumble bee queens for commercial colony production, although the occupation of these artificial nests can be quite low [11,12]. Bumble bees, of various selected species, are commercially sold throughout the world for pollination [13]. These colonies are shipped in artificially constructed hives that are placed within the crop field or greenhouse. These hives are sometimes moved from crop to crop to service multiple locations [14]. In Maine, bumble bees are important pollinators in lowbush blueberry, Vaccinium angustifolium Aiton. Both commercially reared bumble bees [14,15,16] of the species Bombus impatiens Cresson and between 11 and 17 naturally occurring wild bumble bee species are important in lowbush blueberry pollination in Maine, the Canadian Maritimes, and the province of Quebec [17,18,19]. Bumble bees are the most efficient pollinators of lowbush blueberry [20,21] because they sonicate or “buzz” the poricidal anthers of lowbush blueberry, a necessary mechanism for releasing pollen. In addition, bumble bees are active foraging in inclement weather such as when air temperatures are below 10º C and precipitation in the form of snow occurs. Unfortunately bumble bee diversity and abundance is threatened in Europe and North America [22]. Almost 35% of bumble bee species are in decline globally [23]. Causes for the decline in bumble bees are pesticide exposure, climate change, pathogen spillover, habitat loss, competition with invasive species, and destruction of plant/pollinator networks [24,25]. In Maine there were 17 species of bumble bees recorded as residents historically [26], but a recent statewide survey suggests that only 11 species are common enough to be detected visiting flowers in the landscape [27]. It is unknown if any of the 6 species are no longer resident in Maine. Therefore, insight into bumble bee species’ biology and ecology is paramount to conserving biodiversity [5,28]. This is especially true regarding the lack of general knowledge in bumble bee nesting ecology. Although, a recent investigation reviewed 51 nesting habitat studies, the authors state that further research is needed to understand bumble bee nesting if conservation is to be improved [5].

In 2021, an unusual nesting site occupied by a Bombus terricola Kirby colony was observed in Bowdoinham, Sagadahoc County, Maine. This communication describes season-long nesting in a farm tractor used frequently for mowing and logging on an organic mixed vegetable farm. Bombus terricola is a species that has been in decline in New England, and this decline has been documented in Maine and New Hampshire [29,30].

2. Materials and Methods

2.1. Site

Observations were carried out at Six River Organic Farm in Bowdoinham, Maine, USA, 44°00′17″ N latitude, 69°5′15″ W longitude. The site where the observations were made is a farmed flood plain on the western bank of the Abagadasset River at an altitude of 3.0–3.5 m above sea level. This river flows into Merrymeeting Bay in the Kennebec River watershed in Sagadahoc County. This growing region has a humid continental climate (according to the Köppen climate classification) averaging 125 cm of rain, 170 cm of snow, and an average of 205 sunny days per year. The soil is a silt loam. A 1952 John Deere model 40U tractor was parked while undergoing electrical ignition system repairs approximately 105 m from the Abagadasset River, 13 m W of a mixed wildflower 0.08 ha pollinator reservoir, 15 m W from a 0.5 ha organic fruit tree orchard, 9 m SW from a 0.24 ha sweet clover pollinator reservoir, 11 m N of a 0.35 ha agricultural crop field planted to buckwheat, and 14 m E of a mixed Acadian Forest stand (all linear and area measurements were estimated on Google Earth^®, Google LLC, Mountain View, CA, USA). The stand was primarily populated by Red Maple (Acer rubrum L.), Red Oak (Quercus rubra L.), Black Spruce (Picea mariana (Mill.) Britton, Sterns and Poggenb.), Red Spruce (Picea rubens Sarg.), Balsam Fir (Abies balsamea (L.) Mill.), and White Pine (Pinus strobus L.), with an understory of Lowbush (Vaccinium angustifolium Aiton) and Highbush blueberry (Vaccinium corymbosum L.).

2.2. Data Collection

In the spring of 2021, a 1952 John Deere model 40U tractor was immobilized out in the field under a tarp while the electrical system was being repaired (Figure 1 left). Sometime during the period between 15 April when the first Bombus spp. queens were observed foraging on early spring flowers and 15 June, a B. terricola queen took up residence and made a nest in the hollow front axle of the tractor. Entrance into the axle was made through axle expansion holes (19.2 mm in diameter) in the axle (Figure 1 right). It is assumed that rodents had been nesting in the hollow axle previously providing nesting material. The tractor was fixed and started running on 15 June. From 15 June until 15 August B. terricola workers were observed using the tractor as a nest site while the tractor was used 1–3 times per week for 15–90 min. The tractor was never driven more than 300 m from its parking location and at the end of use, it was always returned to the same location. On seven dates the number of B. terricola adults exiting the tractor upon starting the motor was counted and recorded. The dates observations were made were: 22, 25 June, 1, 8, and 15 July, and 9, 11 August. These observations were not considered measures of colony strength as they were made in the late morning or early afternoon after foraging had commenced for the day. On 15 August at 10:15 AM, three pairs of gynes and males were noted mating on the outside of the front and side of the tractor. A transect along the length of each of the two pollinator reservoirs was conducted from 10:30–11 AM to count the number of B. terricola workers, gynes (newly emerged queens), and males on flowers.

3. Results and Discussion

The axle holes are wide enough (>6 mm diameter [31]) for the white-footed deer mouse, Peromyscus leucopus (Rafinesque) to crawl through. This is one of the more common rodents in Maine west of the Penobscot river [32]. Many bumble bee queens utilize abandoned rodent nests to build their own nests within [5,10]. Peromyscus leucopus feeds on seeds and insects. Therefore, this rodent may also present a threat to colonies utilizing nest sites that are easily accessed. The numbers of B. terricola adults observed leaving the tractor upon initial use were: 4, 8, 3, 12, 9, 9, and 5; respectively for the dates 22, 25 June, 1, 8, 15 July, and 9, 11 August. These numbers do not necessarily reflect colony strength because it is not known how many workers were already foraging when the tractor started up and also how many adults in the nest left upon the start of the motor. However, adults issuing from the tractor over time up to when gynes were first observed suggests that the disturbance of starting the tractor and moving it for up to 90 min did not collapse the colony. It is assumed that the males or gynes, or both observed mating on the tractor on 15 August were produced in the tractor nest, although there is no certainty of this, there might have been other B. terricola nests on the farm or close by. It is common to see gynes mate on human-constructed Bombus impatiens Cresson hives when they emerge from commercial pollination colonies (unpublished data). The transects walked on 15 August revealed the following numbers of B. terricola foraging in the two pollinator reservoirs: 5 males, 19 workers, and 7 gynes (assumed gynes due to their size). Most of the B. terricola were found visiting in order of abundance, Butterfly Weed (Asclepias tuberosa L.) (Figure 2), Bee Balm (Monarda fistulosa L.), White Sweet Clover (Melilotus albus Medik.), and Plains Coreopsis (Coreopsis tinctoria Nutt.). The activity of bumble bees around the tractor dropped off precipitously after 15 August, by September no bumble bees were observed in the tractor axle. This is not surprising because colonies in Maine suffer very high levels of Nosema bombi (Fantham and Porter) and thus tend to rapidly dwindle between mid-late August [25,26].

4. Conclusions

Bombus terricola used to be one of the most abundant bumble bees in Maine making up about 25–35% of the total bumble bee species’ relative abundance [29]. Populations declined in Maine from 2009–2010, but have been in recovery increasing across the state of Maine since 2012 [27]. Despite this increase, B. terricola individuals still only make up 3–10% of total bumble bee relative abundance [27,33]. B. terricola current populations carry high pathogen loads [29,33], but it does possess relatively high levels of heterozygosity which is a favorable sign for a recovering species [33].

This study suggests that B. terricola is similar to other bumble bee species in that it is opportunistic in nest founding and that the queen and colony are reluctant to abandon a nest and young once a significant energy investment has been made in colony initiation. The movement of the tractor nesting site may not be that unusual in that, as previously mentioned, commercial bumble colonies are moved in agricultural settings from field to field. However, the movement combined with the noise level, about 90 decibels [34], does create a very unusual habitat for bumble bee nesting. This observation of such an unusual nesting behavior suggests that bumble bees may be attracted to above-ground pipes for nesting, although it may have been a prior utilization of the tractor axle by rodents that provided the attraction. Liczner and Colla [5] did find that up to about 30%, depending on the bumble bee species, nested above ground. Viewing this phenomenon from a conservation perspective, if bumble bee nest sites are found to be limited in a region, artificial pipe nests can be constructed and deployed easily throughout a landscape. Nest site limitation has been documented for Osmia spp. mason bees [35]. Providing artificial nest sites along agricultural fields enhance their densities. This might be especially important in building up colony densities of endangered bumble bee species, a phenomenon that is, unfortunately, becoming a common occurrence globally. The high tolerance to nest disturbance and nest movement has implications for commercial pollination if this behavior is also exhibited in managed species used in agriculture such as B. impatiens and B. terrestris L. Moving bumble bee colonies between temporally or spatially separated crops in bloom, either within or between farms and regions, can greatly increase the pollination benefit from individual colonies.