The ecology and population genetics of a complex of cryptic bumblebee species

Bumblebees are ecologically and economically important as pollinators, but some species are suffering severe declines and range contractions. In this thesis, three cryptic bumblebee species are studied to elucidate differences in their distribution, ecology and population genetics. As a result of their high morphological similarity, very little is known about the lucorum complex species: B. lucorum, B, cryptarum and B. magnus. In this study, their distributions across Great Britain were assessed using molecular methods, revealing that B. lucorum was the most abundant and most generalist of the three species, whereas B. magnus was the rarest and most specialised, occurring almost exclusively on heathland. Additionally, both B. magnus and B. cryptarum were more likely to be present at sites with cooler summer temperatures. Cryptic species represent interesting models to investigate the levels of niche differentiation required to avoid competitive exclusion. Characterising the niches of these species at a single site across the flight season revealed differences along three niche dimensions: temporal activity, weather sensitivity and forage-resource use. These species exhibited asymmetric niche overlap; a combination of ecological divergence and spatio-temporal heterogeneity may contribute to maintaining them in sympatry. Population genetic studies can be highly informative for understanding species ecology and for conservation management. The differences in habitat specialisation exhibited by these bumblebee species provide the opportunity to test conflicting hypotheses about links between dispersal and ecological specialisation: are habitat specialists selected to have low or high dispersal ability? Based on microsatellite analysis, the generalist B. lucorum had high levels of genetic diversity and little population structure across large spatial scales. The habitat specialist B. magnus had the lowest genetic diversity but similar levels of population differentiation to the moderate generalist, B. cryptarum. However, unlike B. cryptarum, B. magnus population differentiation was not affected by geographic distance, suggesting that this specialist species may maintain effective dispersal across large scales despite being restricted to a fragmented habitat. Bergmann’s rule is a well-known ecogeographic rule describing geographical patterns of body size variation, whereby larger endothermic species are found more commonly at higher latitudes. Ectotherms, including insects, have been suggested to follow converse Bergmann’s gradients, but the facultatively endothermic nature of bumblebees makes it unclear which pattern they should adhere to. This thesis reports caste-specific differences in body size between the three lucorum complex species in agreement with Bergmann’s rule: queens and males of B. cryptarum and B. magnus, which were found more commonly at higher latitudes and at sites with cooler temperatures, were larger than those of B. lucorum. Population genetic studies of invertebrates generally require the destruction of large numbers of individuals, which is often undesirable. Testing a variety of faecal collection and DNA extraction methods demonstrated that it is possible to obtain DNA of sufficient quality for genotyping from bumblebee faeces, without harming the individuals. This method would be valuable for studies of rare or declining bee species, for queens in reintroduction projects, and may be applicable to other arthropods. Overall this thesis contributes substantially to our knowledge of the ecology and population genetics of three important pollinator species. It provides data to inform species conservation, as well as understanding of ecosystem functioning and population dynamics. Furthermore, it successfully uses these cryptic species as a model to test several fundamental ecological theories

Bergmann's body size rule operates in facultatively endothermic insects: evidence from a complex of cryptic bumblebee species

According to Bergmann’s rule we expect species with larger body size to inhabit locations with a cooler climate, where they may be well adapted to conserve heat and resist starvation. This rule is generally applied to endotherms. In contrast, body size in ectothermic invertebrates has been suggested to follow the reverse ecogeographic trend: these converse Bergmann’s patterns may be driven by the ecological constraints of shorter season length and lower food availability in cooler high latitude locations. Such patterns are particularly common in large insects due to their longer development times. As large and facultatively endothermic insects, bumblebees could thus be expected to follow either trend. In this investigation, we studied body size of three bumblebee species over a large spatial area and investigated whether interspecific trends in body size correspond to differences in their distribution consistent with either Bergmann’s or a converse Bergmann’s rule. We examined the body size of queens, males and workers of the Bombus lucorum complex of cryptic bumblebee species from across the whole of Great Britain. We found interspecific differences in body size corresponding to Bergmann’s rule: queens and males of the more northerly distributed, cool-adapted, species were largest. In contrast, the mean body size of the worker caste did not vary between the three species. These differences in body size may have evolved under selection pressures for thermoregulation or starvation resistance. We suggest that this case study in facultatively endothermic insects may help clarify the selection pressures governing Bergmann rule trends more generally

Revealing the hidden niche of cryptic bumblebees in Great Britain:Implications for conservation

Bumblebees are ecologically and economically important, and some species have suffered dramatic population declines. The absence of morphological diagnostic characters for the identification of some species creates difficulties for basic ecological studies, and for conservation management. The widespread and commercially exploited bumblebee subgenus Bombus sensu stricto contains a cryptic species complex, known as the lucorum complex, which in Europe comprises B. lucorum, B. cryptarum and B. magnus. Little is known about these species and much of what has been reported is likely to have suffered from incorrect identification. Although the lucorum complex as a whole is common in Great Britain, we aimed to determine whether the populations of the individual species are vulnerable and require conservation action. Using genetic methods to distinguish them, we determined the geographic distribution and abundance of the lucorum complex species in Great Britain, and assessed the extent of niche differentiation between these species. We detected major differences in the geographic range, forage use and sensitivity to summer temperatures of the three species. Bombus lucorum was found to have the broadest distribution and diet, being present throughout mainland Great Britain, whereas B. cryptarum and B. magnus were absent from large areas of central and southern England. Bombus cryptarum and B. magnus were more likely to be found at sites with lower summer temperatures. Bombus magnus, the least abundant species, was found to exhibit an unusually tight biotope association with heathland habitat. This has conservation implications for B. magnus given the current threats to this habitat type

Data from: Niche partitioning in a sympatric cryptic species complex

Competition theory states that multiple species should not be able to occupy the same niche indefinitely. Morphologically, similar species are expected to be ecologically alike and exhibit little niche differentiation, which makes it difficult to explain the co-occurrence of cryptic species. Here, we investigated interspecific niche differentiation within a complex of cryptic bumblebee species that co-occur extensively in the United Kingdom. We compared the interspecific variation along different niche dimensions, to determine how they partition a niche to avoid competitive exclusion. We studied the species B. cryptarum, B. lucorum, and B. magnus at a single location in the northwest of Scotland throughout the flight season. Using mitochondrial DNA for species identification, we investigated differences in phenology, response to weather variables and forage use. We also estimated niche region and niche overlap between different castes of the three species. Our results show varying levels of niche partitioning between the bumblebee species along three niche dimensions. The species had contrasting phenologies: The phenology of B. magnus was delayed relative to the other two species, while B. cryptarum had a relatively extended phenology, with workers and males more common than B. lucorum early and late in the season. We found divergent thermal specialisation: In contrast to B. cryptarum and B. magnus, B. lucorum worker activity was skewed toward warmer, sunnier conditions, leading to interspecific temporal variation. Furthermore, the three species differentially exploited the available forage plants: In particular, unlike the other two species, B. magnus fed predominantly on species of heather. The results suggest that ecological divergence in different niche dimensions and spatio-temporal heterogeneity in the environment may contribute to the persistence of cryptic species in sympatry. Furthermore, our study suggests that cryptic species provide distinct and unique ecosystem services, demonstrating that morphological similarity does not necessarily equate to ecological equivalence

Nondestructive DNA sampling from bumblebee faeces

Genetic studies provide valuable data to inform conservation strategies for species with small or declining populations. In these circumstances, obtaining DNA samples without harming the study organisms is highly desirable. Excrements are increasingly being used as a source of DNA in such studies, but such approaches have rarely been applied to arthropods. Bumblebees are ecologically and economically important as pollinators; however, some species have recently suffered severe declines and range contractions across much of Western Europe and North America. We investigated whether bumblebee faeces could be used for the extraction of DNA suitable for genotyping using microsatellite markers. We found that DNA could be extracted using a Chelex method from faecal samples collected either in microcapillary tubes or on filter paper, directly from captured individuals. Our results show that genotypes scored from faecal samples are identical to those from tissue samples. This study describes a reliable, consistent and efficient noninvasive method of obtaining DNA from bumblebees for use in population genetic studies. This approach should prove particularly useful in breeding and conservation programs for bumblebees and may be broadly applicable across insect taxa. © 2012 Blackwell Publishing Ltd

Data from: Bergmann's body size rule operates in facultatively endothermic insects: evidence from a complex of cryptic bumblebee species

According to Bergmann’s rule we expect species with larger body size to inhabit locations with a cooler climate, where they may be well adapted to conserve heat and resist starvation. This rule is generally applied to endotherms. In contrast, body size in ectothermic invertebrates has been suggested to follow the reverse ecogeographic trend: these converse Bergmann’s patterns may be driven by the ecological constraints of shorter season length and lower food availability in cooler high latitude locations. Such patterns are particularly common in large insects due to their longer development times. As large and facultatively endothermic insects, bumblebees could thus be expected to follow either trend. In this investigation, we studied body size of three bumblebee species over a large spatial area and investigated whether interspecific trends in body size correspond to differences in their distribution consistent with either Bergmann’s or a converse Bergmann’s rule. We examined the body size of queens, males and workers of the Bombus lucorum complex of cryptic bumblebee species from across the whole of Great Britain. We found interspecific differences in body size corresponding to Bergmann’s rule: queens and males of the more northerly distributed, cool-adapted, species were largest. In contrast, the mean body size of the worker caste did not vary between the three species. These differences in body size may have evolved under selection pressures for thermoregulation or starvation resistance. We suggest that this case study in facultatively endothermic insects may help clarify the selection pressures governing Bergmann rule trends more generally

Caste-specific interspecific differences in thorax width across the <i>lucorum</i> complex species.

<p>Caste-specific interspecific differences in thorax width across the <i>lucorum</i> complex species.</p

Differences in body size of the three bumblebee species.

<p>The thorax widths of (a) queens, (b) males and (c) workers of <i>B</i>. <i>lucorum</i>, <i>B</i>. <i>magnus</i> and <i>B</i>. <i>cryptarum</i>. Box and whisker plots compare medians. Numbers give sample sizes. Different letters denote categories for which the means are significantly different (<i>P</i> < 0.01). The plots are based on raw data.</p