Category Archives: Pollination

How do artificial nectar feeders affect hummingbird abundance and pollination of nearby plants? A new study in the Journal of Ornithology

Back in November 2013, during my research and teaching trip to Brazil, I discussed an amazing garden that we visited in which the owner had set up around a dozen hummingbird feeders that were attracting hundreds of individual birds from over 20 species. As I mentioned, one of the owner’s concerns was that by feeding the birds he might be negatively affecting the reproduction of hummingbird-pollinated plants in the surrounding forest. I thought it unlikely but there have been very few tests of this idea, and none in that part of South America.

After I left, a Master’s student called Jesper Sonne, based at the Center for Macroecology and Climate in Copenhagen, worked with my Brazilian and Danish colleagues on collecting data to address this question. Between us we analysed and wrote up the results, and have recently published the paper in the Journal of Ornithology under the title “Spatial effects of artificial feeders on hummingbird abundance, floral visitation and pollen deposition“.

The abstract is below and if anyone wants a PDF, please drop me a line. But the take home message is that although these feeders have a significant local effect on hummingbird abundance, there’s no evidence that they affect plant reproduction in the vicinity. It’s nice when predictions prove correct….

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Abstract

Providing hummingbirds with artificial feeders containing sugar solution is common practice throughout the Americas. Although feeders can affect hummingbird foraging behavior and abundance, it is poorly understood how far this effect may extend. Moreover, it remains debated whether nectar-feeders have a negative impact on hummingbird-pollinated plants by reducing flower visitation rates and pollen transfer close to the feeders. Here, we investigated the effects of distance to nectar-feeders on a local hummingbird assemblage and the pollination of Psychotria nuda (Rubiaceae), a hummingbird-pollinated plant endemic to the Brazilian Atlantic Rainforest. At increasing distance (0–1000 m) from a feeding-station, where hummingbirds have been fed continuously for the past 13 years, we quantified hummingbird abundance, and rates of flower visitation and pollen deposition on P. nuda. We found that hummingbird abundance was unrelated to distance from the feeders beyond ca. 75 m, but increased steeply closer to the feeders; the only exception was the small hummingbird Phaethornis ruber, which remained absent from the feeders. Plants of P. nuda within ca.125 m from the feeders received increasingly more visits, coinciding with the higher hummingbird abundance, whereas visitation rate beyond 125 m showed no distance-related trend. Despite this, pollen deposition was not associated with distance from the feeders. Our findings illustrate that artificial nectar-feeders may locally increase hummingbird abundance, and possibly affect species composition and pollination redundancy, without necessarily having a disruptive effect on pollination services and plants’ reproductive fitness. This may apply not only to hummingbirds, but also to other animal pollinators.

How much do we really understand about pollination syndromes?

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Ecologists and evolutionary biologists have, for many years, sought to document repeated patterns that they see in nature; to understand the processes that determine these patterns; and to make predictions about how and when they are going to be observed in the future or in other parts of the world. There are many examples of such patterns, including: cyclical population dynamics of species such as lemmings; the occurrence of specific types of plant communities (e.g. rainforest, grasslands) in areas with particular climates; and convergent evolution of unrelated species to similar ecological niches, such as large, predatory placental and marsupial mammals (e.g. the dog and wolf family compared to the Tasmanian “wolf”).

An example of convergent evolution that has fascinated botanists since the 19^th century is the idea of “pollination syndromes”, which are sets of flower characteristics that have repeatedly evolved in different plant families due to the convergent selection pressures applied by some groups of pollinators. Thus, red, scentless flowers producing lots of nectar are typical of many hummingbird pollinated plants in the New World, whilst white, night-scented flowers often signify moth pollination. Good examples of plant species possessing these archetypical flower traits are have been used as text book examples for decades, repeatedly used to illustrate the predictable and specialised nature of some plant-pollinator interactions.

The problem is that until recently the pollination syndromes have rarely been subjected to critical tests of their frequency and predictive value (Ollerton et al. 2009 and references therein). It’s been tacitly assumed that (after more than 150 years of study) we clearly know all there is to know about them, even though there have been criticisms levelled at the syndromes since their inception, a fact that has been subsequently ignored (Waser et al. 2011).

However in the last 20 years biologists have begun to seek answers to questions such as: How often do plant species conform to the expectations of the classical pollination syndromes? How good is our ability to predict the pollinators of a plant based just on its flower characteristics? What is the role played by flower visitors that do not conform to the predictions of the pollination syndromes? Similarly, what is the role of animals that steal nectar or pollen, or act as herbivores, in shaping flower traits? What new examples of convergent evolution of flower traits remain to be discovered?

Research conducted in many different parts of the world has addressed these questions, questions which some biologists had assumed were already answered or which were not worth asking in the first place. And the answers to them are proving to be both surprising and controversial.

For example, the most comprehensive test of the frequency and predictability of pollination syndromes that has been conducted to date (Ollerton et al. 2009) concluded that only a small proportion of the 352,000 species of flowering plants could be categorised into the pollination syndromes as classically described. Likewise, they estimated that the predictive power of the pollination syndromes was about 30%. Other studies have shown that “secondary” flower visitors can be just as, or more, effective pollinators than the “primary” pollinator predicted by the syndromes (e.g. Waser & Price 1981,1990, 1991); that floral antagonists can play an important a role in shaping flower traits (e.g. Junker and Parachnowitsch 2015 and references therein); and that there are still examples of convergent evolution to “unexpected” pollinators waiting to be discovered in less well researched parts of the world, which in fact is most of the world (Ollerton et al. 2003).

Recently the very prestigious journal Ecology Letters published a paper that has challenged the challengers. Rosas-Guerrero et al (2014), by using a statistical technique called meta-analysis underpinned by a review of the available literature, suggested that pollination syndromes are much more predictable than Ollerton et al. (2009) concluded, and perhaps as high as 75%. However some of my collaborators and I see problems with their approach to studying pollination syndromes that have biased the conclusions that they draw, and therefore undermined the robustness of those conclusions, which we set out in a response to their original paper (Ollerton et al. 2015). We originally tried to publish this in Ecology Letters but for some reason the journal was not interested; it’s therefore freely available from Journal of Pollination Ecology if you follow that link.

I won’t go into the detail of what we perceive as problems in Rosas-Guerrero et al.’s approach to testing the syndromes (you can read the paper for yourself) but in summary they relate to how the literature review was conducted (which failed to include all of the studies that could have provided data for their meta-analysis); the significant bias in the current literature because plant-pollinator interactions are not studied randomly (biologists are often drawn to large-flowered plants possessing those archetypical, classical flower traits associated with particular syndromes); the variation in how different researchers determine the effectiveness of the pollinators in their system, meaning that these studies are not always comparable; and issues around annual variation in pollinator identity and presentation of data.

Despite providing a focus and framework for understanding pollination biology for over 150 years, the pollination syndromes continue to surprise us and to provide a vital antidote to scientific hubris: we really do not understand nearly as much about them as we assume.

In an era when we are more and more concerned about loss of pollinator diversity, including extinction at both a species- and country-level, do these debates really matter or are they of purely academic concern, of interest to a few botanists and ecologists? As you might expect, I’d argue that they do matter: there are still some fundamental aspects of pollination ecology that we don’t completely understand, or have only recently been seriously addressing, some of which I’ve worked on myself and which I’ve highlighted in this blog. These include the number of flowering plants that require animal pollination, the diversity of pollinators at a global and regional level, the relative importance of different types of pollinators, and whether or not plants and pollinators are more specialised in tropical compared to temperate communities. Without some of this fundamental knowledge we are unable to make effective arguments, policies and strategies for conserving pollinators.

References

Junker RR, Parachnowitsch AL (2015) Working towards a holistic view on flower traits—how floral scents mediate plant–animal interactions in concert with other floral characters. Journal of the Indian Institute of Science 95:43–67.

Ollerton J, Johnson SD, Cranmer L, Kellie S (2003) The pollination ecology of an assemblage of grassland asclepiads in South Africa. Annals of Botany 92:807–834.

Ollerton J, Alarcón R, Waser NM, Price MV, Watts S, Cranmer L, Hingston A, Peter CI, Rotenberry J (2009) A global test of the pollination syndrome hypothesis. Annals of Botany 103:1471–1480.

Rosas-Guerrero V, Aguilar R, Marten-Rodriguez S, Ashworth L, Lopezaraiza-Mikel M, Bastida JM, Quesada M (2014) A quantitative review of pollination syndromes: do floral traits predict effective pollinators? Ecology Letters 17: 388–400.

Waser NM, Price MV (1981) Pollinator choice and stabilizing selection for flower color in Delphinium nelsonii. Evolution 35:376–390.

Waser NM, Price MV (1990) Pollination efficiency and effectiveness of bumble bees and hummingbirds visiting
Delphinium nelsonii. Collectanea Botanica (Barcelona) 19:9–20.

Waser NM, Price MV (1991) Outcrossing distance effects in Delphinium nelsonii: pollen loads, pollen tubes, and seed set.
Ecology 72:171–179.

Waser NM, Ollerton J, Erhardt A (2011) Typology in pollination biology: lessons from an historical critique. Journal of Pollination
Ecology 3:1–7.

Garden pollinators for PAW no. 6 – Buff-tailed bumblebee (Bombus terrestris)

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It would be impossible to write a series of blog posts about garden pollinators for Pollinator Awareness Week without considering the bumblebees (genus Bombus) and I intend to devote the last two posts to that group of bees. The bumblebees are arguably the UK’s most important pollinators of both wild and crop plants, certainly later in the season when colony numbers have increased. Earlier in the season it’s the solitary bees such as the Orange-tailed mining bee that are predominant.

Although common and widespread in gardens, the Buff-tailed bumblebee (Bombus terrestris) belongs to a group of bees in which the workers are rather variable in appearance and can be very difficult to distinguish from those in the Bombus lucorum group, which includes two other species (B. cryptarum and B. magnus).

This is a truly social species with an annual nest comprising workers and a queen. Nests are founded by queens that have mated the previous year and hibernated. They usually choose old rodent nests in which to begin their colonies, which is why they are sometimes found in garden compost bins. An interesting question that I’ve not seen answered is whether the queens actively displace mice or voles from such nests: does anyone know? This association between bumblebees and mice led Charles Darwin and Thomas Huxley into some speculation as to the role of spinsters in the British Empire.

In my garden the Buff-tailed bumblebee pollinates a range of crops including strawberries, squashes, courgettes, blackberries, runner beans, french beans, tomatoes, and raspberries. As the photo above shows they also visit the flowers of passion fruit, where they seem to be more effective than the smaller honey bees and solitary bees.

Garden pollinators for PAW no. 5 – Orange-tailed mining bee (Andrena haemorrhoa)

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The Orange-tailed mining bee (Andrena haemorrhoa) is also referred to as the Early mining bee due to its habit of emerging from over-wintered nests as early in the year as March. In truth, however, many Andrena species put in an early appearance, making them important pollinators of orchard fruit such as apples, which you can see from the photograph above, taken in my urban garden earlier this year. So “Orange-tailed” is a more descriptive name.

Thanks to the Orange-tailed mining bee and other early bees, this unnamed apple variety (which Karin and I rescued from the bargain area of a local garden centre) has gone on to produce a heavy crop of eating apples (see below). There’s considerable interest in the role of wild bees such as these as pollinators of fruit in commercial orchards, not just in Europe but in the USA too, where other Andrena spp. also pollinate apples.

The epithet “Mining bees” refers to the fact that these solitary species of the genus Andrena usually make their nests in soil, excavating deep tunnels in which to construct individual cells. It’s another generalist, taking pollen and nectar from a wide variety of garden and wild flowers. Dandelions are particularly important early in the year – so don’t over-manage your lawn and allow some to flower!

Garden pollinators for PAW no. 4 – Gatekeeper butterfly (Pyronia tithonus)

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For my fourth contribution to Pollinator Awareness Week I’m going to highlight the Gatekeeper (Pyronia tithonus), a butterfly that I featured on this blog last year. As I noted in that post, it’s fairly rare to have Gatekeepers in an urban garden which indicates that the shrubs and hedges grown by myself and my neighbours are providing the right microclimate for the adults. In addition the overgrown lawns of some adjacent gardens give opportunities for egg laying as the caterpillars are grass feeders.

Adult butterflies are very well camouflaged when resting with their wings folded. They take nectar from a range of plants in my garden but particularly love the dark, heavily scented infloresences of the buddleia variety pictured here. They also visit the wild blackberries scrambling through the hedge that separates us from next door’s garden and probably pollinate those flowers. Although it’s often said that butterflies are poor pollinators compared to bees, due to their general un-hairiness and habit of holding themselves above the stamens and stigmas in a flower, it very much depends on the type of flower. We have an unpublished manuscript that I hope to submit to a journal later this year showing that butterflies are actually better pollinators of one grassland plant than bumblebees.

Garden pollinators for PAW no. 2 – Marmalade hoverfly (Episyrphus balteatus)

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One of the most frequently encountered of hoverfly species in urban gardens is the beautifully named Marmalade hoverfly (Episyrphus balteatus). This insect is a “true fly” of the order Diptera that is sometimes confused with superficially similar wasps (order Hymenoptera), though (as the common name suggests) the species is translucent orange and black in colour rather than waspish yellow and black. It also has a very flat abdomen whereas wasps are rounded, and they certainly don’t sting.

Individual insects are relatively ineffective as pollinators – they are small and not very hairy, so carry little pollen compared to bumblebees for instance. However they can be extremely abundant and that abundance makes up for any individual ineffectiveness. It’s a real generalist, visiting lots of different types of flowers, and in my garden they visit radishes (as I noted last year) and raspberries.

I often see individuals patrolling crops such as runner beans, not visiting the flowers but laying eggs on leaves and stems: the larvae of the Marmalade hoverfly is carnivorous and feeds on aphids, so it plays an interesting dual role of both pollinator and pest controller. Definitely a gardener’s friend!

Garden pollinators for PAW no. 1 – Patchwork leaf-cutter bee (Megachile centuncularis)

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As promised, here’s the first of my posts for Pollinator Awareness Week and I’m going to start with one of my favourite groups of bees – the leaf-cutters of the genus Megachile. The UK has only nine Megachile species recorded, several of which are quite frequently found in gardens.

In my urban garden in Northampton I’ve often encountered the Patchwork leaf-cutter (Megachile centuncularis) this summer. As you can see from the link to Steve Falk’s excellent photographs and description of the species, it’s quite distinctive with a brush of orange hairs that extends right to the tip of the abdomen (see the first picture, though the colour of this can fade with age so it’s not always so apparent). The brush is used for collecting pollen from flowers to take back to provision its nest, which is constructed from leaf segments lining a tubular cavity in old walls, wood or occasionally soil (hence “leaf-cutter” bees). The leaf-cutters (as with 90% of bee species) are “solitary” in the sense that they don’t have a social structure with a communal nest, a queen, etc. It’s the female bees that are solely responsible for nest building; the purpose of the males is simply to mate.

I’ve seen this species visiting my runner beans in the garden and, given their size, they probably pollinate that crop, though not as effectively as bumblebees which are much more abundant.

In the image above you can clearly see the pollen that’s been collected by this bee under its abdomen.

In my garden the Patchwork leaf-cutter is very fond of Lamb’s ear (Stachys byzantina), but I’ve seen it collecting nectar and pollen on a wide range of other plants too.

Pollinator Awareness Week – 13th – 19th July 2015

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Next week has been designated Pollinator Awareness Week (PAW) by Defra and there are events and profile-raising activities going on all over the country.

The motivation behind the PAW is (quote) “to bring attention to the essential needs of pollinators and the simple actions that we can all take to help pollinators survive and thrive”.

With that in mind, next week I intend to produce one blog post a day that highlights, with photographs, a pollinator (or group of pollinators) that I’ve found in my own urban garden in Northampton. The purpose is to illustrate the diversity of pollinators that even a town garden can support, something about their fascinating life histories, and the different ecological requirements of these pollinators that our gardens can provide. For some of them I’ll even discuss the garden crops that they pollinate. First post will be on Monday.

If you, or the group you work with, are doing something for Pollinator Awareness Week feel free to share it in the comments section below.

How can an understanding of plant–pollinator interactions contribute to global food security? A new discussion paper

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A new discussion/review paper that I contributed to has just been published in the journal Current Opinion in Plant Biology. Entitled “How can an understanding of plant–pollinator interactions contribute to global food security?” the paper was written in collaboration with Professor Beverley Glover and her PhD students Emily Bailes and Jonathan Pattrick at the University of Cambridge.

The abstract and highlights are copied below; if anyone wants a PDF of the full paper, send me an email or ask in the comments section.

Abstract:

Pollination of crops by animals is an essential part of global food production, but evidence suggests that wild pollinator populations may be declining while a number of problems are besetting managed honey bee colonies. Animal-pollinated crops grown today, bred in an environment where pollination was less likely to limit fruit set, are often suboptimal in attracting and sustaining their pollinator populations. Research into plant–pollinator interactions is often conducted in a curiosity-driven, ecological framework, but may inform breeding and biotechnological approaches to enhance pollinator attraction and crop yield. In this article we review key topics in current plant–pollinator research that have potential roles in future crop breeding for enhanced global food security.

Highlights:

Animals are globally, and increasingly, important for the improved yield and quality of many crops.
Floral traits are a promising and little explored avenue for the improvement of crop yields.
Work surrounding plant–pollinator interactions can inform us on the best strategies to do this.
Coordinating crop flowering time with key lifecycle stages of pollinators could benefit both crop yields and pollinators.

How good is the evidence base for pollinator declines? A comment on the recent Ghazoul and Goulson Science correspondence

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In a recent issue of the journal Science, Dave Goulson and colleagues presented a review entitled “Bee declines driven by combined stress from parasites, pesticides, and lack of flowers”. This stimulated Jaboury Ghazoul to submit a letter to Science criticising the Goulson et al. paper from a number of perspectives, but particularly the paucity of the evidence base for pollinator declines. Dave and his co-authors robustly responded to that letter, as you might imagine. In some respects this was an unsatisfactory exchange, however, as the focus was largely on agricultural pollinators, rather than pollinators of all plants (including the majority non-cultivated species) and I think that (perhaps with more space?) Dave could have outlined the evidence in more depth.

The most striking statement in Jaboury’s letter was that the “evidence for pollinator declines is almost entirely confined to honeybees and bumblebees in Europe and North America”.

Now, even given the fact that Jaboury was possibly referring specifically to agricultural pollinators, that is a very extreme statement to make. Underlying it is the suggestion that global concerns about declining pollinator biodiversity (a subject I’ve discussed repeatedly on this blog) is underpinned by a taxonomically and geographically thin evidence base. Is that really true? I don’t believe so and I think it’s worth presenting a brief overview of the evidence, not least because Dave’s review and the resulting correspondence is pay-walled at the Science site (though if you Google the titles you might, just might, find copies posted on the web…)

Let me state from the outset that I have considerable respect for both Jaboury and Dave, as individuals and as scientists. I’ve known Dave since we were postgrads together in the early 1990s, and have had occasional contact with Jaboury through conferences and via email. So this isn’t meant to be a criticism of either of them. But I do believe that the evidence for pollinator declines is considerably more robust than Jaboury acknowledges, and even more wide ranging than Dave and colleagues describe in their response (though in fairness, most of the bee evidence was cited in their original review).

Here’s a summary of where I see the evidence base at the moment; it’s not meant to be a full review, by any means, but rather to give a flavour of the taxonomic and geographical breadth and depth of the evidence as it currently stands:

Wild bees (including bumblebees, and solitary and primitively eusocial bees) – significant reduction of abundance and diversity at local, regional and country-levels documented in Britain (Biesmeijer et al. 2006, Ollerton et al. 2014), Holland (Biesmeijer et al. 2006), Europe as a whole (Kosier et al. 2007, the recent IUCN Red List by Nieto et al 2014), North America (Grixti et al. 2007, Cameron et al. 2011, Burkle et al. 2013), South America (Morales et al. 2013; Schmid-Hempel et al. 2013), China and Japan (Xie et al. 2008; Williams et al. 2009; Matsumura et al. 2004; Inoue et al. 2008), and South Africa (Pauw 2007).

Honey bees – colony declines documented in Europe and North America (see reviews by NRC 2007, Potts et al. 2010) and evidence that global demand for honey bee pollination services is outstripping supply (Aizen and Harder 2009).

Hoverflies (Syrphidae) – diversity declines documented in Holland and Britain (Biesmeijer et al. 2006).

Butterflies and moths – diversity and abundance of Lepidoptera has declined in the UK (Gonzalez-Megias et al. 2008, Fox 2013), whilst in North America some 50 species are IUCN criteria Red Listed and there is particular concern about the iconic Monarch butterfly. Likewise a significant fraction of butterflies in other parts of the world are of conservation concern, e.g. Southern Africa, Australia, and Europe.

Flower-visiting wasps – reduction in country-level diversity in Britain (Ollerton et al. 2014).

Birds and mammals – the major vertebrate pollinators have recently been assessed at a global level by Regan et al. (2015) using IUCN Red List criteria. They concluded that: “overall, pollinating bird and mammal species are deteriorating in status, with more species moving toward extinction than away from it. On average, 2.5 species per year have moved one Red List category toward extinction in recent decades, representing a substantial increase in the extinction risk across this set of species”.

Of course a number of the studies cited above have shown that some species are doing better than others and a proportion of the taxa they have assessed are stable or even increasing in abundance (including managed honey bee colonies in some parts of the world). But the current evidence base, as I see it, is pointing towards significant declines in pollinator abundance and diversity at multiple spatial scales across all regions that have so-far been assessed with any rigour, for a wide range of taxa.

I’m happy to receive comments on this topic, particularly pointing me to major sources of evidence that I’ve not covered, or if you disagree with my conclusions.

References

Aizen and Harder (2009) The global stock of domesticated honeybees is growing slower than agricultural demand for pollination. Current Biology 19: 915–918.

Biesmeijer et al. (2006) Parallel declines in pollinators and insect-pollinated plants in Britain and the Netherlands. Science 313: 351–354.

Burkle et al. (2013) Plant-pollinator interactions over 120 years: Loss of species, co-occurrence, and function. Science 339, 1611–161.

Cameron et al. (2011) Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. U.S.A. 108: 662–667.

Fox (2013) The decline of moths in Great Britain: a review of possible causes. Insect Conservation and Diversity 6: 5–19.

Gonzalez-Megias, A. et al. (2008) Changes in the composition of British butterfly assemblages over two decades. Global Change Biology, 14: 1464-1474.

Grixti (2009) Decline of bumble bees (Bombus) in the North American Midwest. Biol. Conserv. 142, 75–84 (2009).

Inoue et al. (2008). Displacement of Japanese native bumblebees by the recently introduced Bombus terrestris (L.) (Hymenoptera: Apidae). J. Insect Conserv. 12: 135–146.

Kosior (2007) The decline of the bumble bees and cuckoo bees (Hymenoptera: Apidae: Bombini) of Western and Central Europe. Oryx 41, 79–88.

Matsumura et al. (2004) Invasion status and potential ecological impacts of an invasive alien bumblebee, Bombus terrestris L. (Hymenoptera: Apidae) naturalized in Southern Hokkaido, Japan. Glob. Environ. Res. 8, 51–66.

National Resource Council (2007) Status of Pollinators in North America. National Academies Press, Washington, DC.

Nieto et al. (2014) European Red List of Bees. Publication Office of the European Union.

Ollerton et al. (2014) Extinction of aculeate pollinators in Britain and the role of large-scale agricultural changes. Science 346: 1360-1362.

Pauw (2007) Collapse of a pollination web in small conservation areas. Ecology 88: 1759-1769.

Potts et al. (2010) Declines of managed honey bees and beekeepers in Europe. Journal of Apicultural Research 49: 15–22.

Regan et al. (2015) Global Trends in the Status of Bird and Mammal Pollinators. Conservation Letters DOI: 10.1111/conl.12162

Schmid-Hempel et al. (2013) The invasion of southern South America by imported bumblebees and associated parasites. Journal of Animal Ecology 83: 823–837.

Williams et al. (2009) The bumblebees of Sichuan (Hymenoptera: Apidae, Bombini). Syst. Biodivers. 7: 101–189.

Xie et al. (2008) The effect of grazing on bumblebees in the high rangelands of the eastern Tibetan Plateau of Sichuan. Journal of Insect Conservation 12: 695–703 (2008).