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

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.


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).

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

  1. Stuart Roberts

    This is a very vexed question I think. Jaboury has been outspoken on this subject for ages . He wrote an article in TrEE about 10 years ago questioning the pollination crisis – however, I think he does make a number of valid points. The Biesmeijer at al paper of 2006 (I was a co-author) is probably the most cited paper in the canon and there are flaws. For instance, because of the scarcity of historic data all the sites looked at were from places where there were rich faunas in the past and which now show degrees of impoverishment. No sites were looked at which were poor in the past and which today might be rich.

    At the country level, I suspect that the number of species in Britain today is pretty well the same as it was 100 years ago – with some losses, balanced with some gains (these latter species are often overlooked). Add to this the clear increase in abundance and range of species like Andrena cineraria, Andrena flavipes, Lasioglossum malachurum and L. pauxillum (the latter species are regular nesters in arable field entrances and tramlines). The bumblebees B. pascuorum, B. lapidarius and B. terrestris (not to mention B. hypnorum) are expanding their ranges (all these species are also regularly found in farmland).

    Even among the rarer bumbles there has been some better news in the last few years. B. rupestris is now as common as it was in the 1940’s (I didn’t see one for the first 8 years I studied bees), B. monticola has colonised Ireland (twice), B. humilis is doing much better that it was 20 years ago (as is B. ruderatus) and B. sylvarum is reoccupying parts of Kent and Essex from which it became absent. Most (but by no means all) rare species of bees in UK have always been rare and difficult to find (and identify).

    None of this is to suggest that we should be complacent or anything less than vigilant. More than ever we need to keep an eye on what is happening to our wildlife and wild places, and melissophiles need to be alert and get involved with monitoring.

    1. jeffollerton Post author

      Thanks Stuart, you raise some interesting points. I’d question whether the UK really has as many pollinator species now as it had 100 years ago though. Losses include the 23 bees & wasps that we assessed (minus the species that’s re-colonised) plus about 60 butterflies and moths, makes over 80 species. Have we really gained 80 new species in that time?

    2. Pale Blue Dot

      Hi Stuart
      The crux of the issue is “How good is the evidence base …….” so “I suspect” isn’t helpful in the interest of wider public understanding and leaves you open questions about ‘belief’. We’re working with Dave and other UK environmental scientists to bring their work to a wider public audience. 🙂

      1. Stuart Roberts

        I used “I suspect” because extinction is, of course, notoriously difficult to prove. Andrena lathyri (on Jeff’s list) is a case in point, and although it hasn’t been seen since I found one in 1990, very few people have looked for it in its former stronghold near Wolfhall (in central Wilts) where the principal forage plants remain plentiful. Andrena vaga (also on the list) has reappeared in Hampshire and in at least 3 sites in Kent in the last couple of years

  2. Ian Lane

    A somewhat recent paper by Bartomeus adds some support for winners and losers in the bee world. Here is the citation:

    Bartomeus, I., Ascher, J. S., Gibbs, J., Danforth, B. N., Wagner, D. L., Hedtke, S. M., & Winfree, R. (2013). Historical changes in northeastern US bee pollinators related to shared ecological traits. Proceedings of the National Academy of Sciences of the United States of America, 110(12), 4656–60. doi:10.1073/pnas.1218503110

      1. ibartomeus

        Thanks both, I do think is important to think about winner and losers and not to treat all pollinators equal. However, our data on the above cited paper is about relative abundances. This means we don’t know absolute changes, unfortunately.

      2. jeffollerton Post author

        Thanks Nacho. Yes, agreed, winners and losers should both be assessed. But an unanswered quetion to my mind is: are some species winners because we have forced others to become losers? So for example, have the tree bumblebee and the ivy bee successfully colonised and spread in the UK because we have extirpated populations of bees that would otherwise compete with them?

  3. Pollinator

    The US Department of Agriculture submitted a report in 1946, indicating a decline on native pollinators (“Dependence of agriculture on the beekeeping industry –: a review”. Although there are not enough references, the observations are strong enough that they are worth considering. Among the conclusions; “In many places the depletion of wild pollinators is so acute that honeybees have to be brought in especially for pollination.”

  4. standingoutinmyfield

    Sam Droege gives an interesting presentation about the difficulty of quantifying bee declines because the coefficient of variation is so high between years and sites. We still don’t have a really strong grasp on how to measure bee population sizes reliably, especially for the rarer solitary bees.

  5. Manu Saunders

    Great post! As you say, complex issues like this are harder to do justice to within the short space (and reference limits!) that you have in journal articles.
    I think there is plenty of localised evidence beyond the big reviews & meta-analyses. Of course, it can be harder to translate this to the bigger picture, but I think they paint a pretty convincing picture about how changes in habitat/mgmt are affecting pollinators. Here’s an interesting one I found this week: potential for bee declines with changing forest mgmt in US: (discussion is interesting)
    – feral honey bee densities in Aus:
    – And an older one on bird pollination of native plants in Aus:

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  8. ibartomeus

    I can’t reply on the thread, but my answer here. Are some species winners because we have forced others to become losers? My guess is that this is a likely mechanism. Jim Cane has surveys in blueberry fields from the 80’s where B. affinis is the dominant visitor, and after its disappearance, B. impatiens and bimaculatus toke over (unfortunately data is not good enough to properly analyse the change, as we don’t have abundance data for the 80’s). Still, is nice to have this back up pollinators that are less sensitive to the human induced changes.

    1. jeffollerton Post author

      Thanks Nacho. Your comment about “back up pollinators” emphasises the importance of maintaining pollinator biodiversity as well as abundance: we can’t predict what we’re likely to lose in the future and a diversity of species can act as an ecological insurance.

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