Humans affect the land on which they live in many different ways, and this in turn influences local biodiversity. Sometimes this has positive effects on local wildlife: consider the diversity of birds to be found in well-managed suburban gardens, for example. But often the effect is negative, especially when the land is intensively managed or habitats are destroyed, for example via deforestation or urban development.
This is not a new phenomenon – according to a recent study, most of the habitable parts of the planet have been shaped by humans for at least 12,000 years (see Ellis et al. 2021). What is new, however, is the scale and the speed with which land-use is changing, which are far greater than they have been historically. An important question is the extent to which this change in land-use intensity is affecting pollinator diversity in different parts of the world. Over the past 18 months I’ve been collaborating on a project led by Joe Millard (as part of his PhD) and Tim Newbold which uses the Projecting Responses of Ecological Diversity In Changing Terrestrial Systems (PREDICTS) database to address that very question.
The study was global in scale and used data from 12,170 sites to assess the affect of land-use intensity on 4502 pollinating species. The findings are really fascinating; highlights include:
In comparison to natural vegetation, low levels of land-use intensity can have a positive effect on the diversity of pollinators.
For most land categories, greater intensity of land-use results in significant reductions in diversity and abundance of pollinators, however. For example, for urban sites there’s a 43% drop in number of species and a drop in 62% pollinator abundance from the least to the most intensive urban sites.
On cropland, strong negative responses of pollinators to increasing intensity are only found in tropical areas, although different taxonomic groups vary in their responses.
The latter finding is especially concerning given that: (i) most pollinator diversity is found in the tropics; (ii) the majority of tropical crops are insect pollinated; and (3) tropical agriculture is becoming increasingly intensive and land use is likely to rapidly change in the coming decades.
The full reference for the study, with all authors, is:
Millard, J., Outhwaite, C.L., Kinnersley, R., Freeman, R., Gregory, R.D., Adedoja, O., Gavini, S., Kioko, E., Kuhlmann, M., Ollerton, J., Ren, Z.-X. & Newbold, T. (2021) Global effects of land-use intensity on local pollinator biodiversity. Nature Communications 12, 2902. https://doi.org/10.1038/s41467-021-23228-3
The distribution of plants, animals and other organisms that we see around us is clearly influenced by climate: all species have limitations in terms of temperature, rainfall, etc., that affects where they can live and reproduce. As well as these contemporary “climatic niches” however, there are much more subtle effects of historical climate on species, and the ways in which they interact with one another. These are harder to study because it requires us to know about what climatic conditions were like in a particular region thousands or millions of years ago. But as our knowledge of paleoclimates grows, we can apply it to understand how contemporary ecology is shaped by the past. This in turn may tell us how species will react to future climate change.
In a new study that I’ve just published with Brazilian, Danish and American colleagues, we’ve shown that the frequency with which a South American savannah tree self-pollinates is determined mainly by the climatic stability experienced by a population since the Last Glacial Maximum. In contrast, and perhaps surprisingly, the current diversity and abundance of pollinators plays a much smaller role in how often plants self-pollinate.
The work was led by André Rodrigo Rech and formed part of his original PhD research. Here’s the full citation:
The abstract is below, first in English then in Portuguese. If anyone wants a PDF please add a comment or send me a message via my Contact page.
Patterns in ecology are the products of current factors interacting with history. Nevertheless, few studies have attempted to disentangle the contribution of historical and current factors, such as climate change and pollinator identity and behavior, on plant reproduction. Here, we attempted to separate the relative importance of current and historical processes on geographical patterns of the mating system of the tree species Curatella americana (Dilleniaceae). Specifically, we asked the following: (a) How do Quaternary and current climate affect plant mating system? (b) How does current pollinator abundance and diversity relate to plant mating system? (c) How does mating system relate to fruit/seed quantity and quality in C. americana? We recorded pollinators (richness, frequency, and body size) and performed pollination tests in ten populations of C. americana spread over 3,000 km in the Brazilian savannah. The frequency of self‐pollination in the absence of pollinators was strongly influenced by historical climatic instability and not by present‐day pollinators. In contrast, seed set from hand‐cross and natural pollination were affected by pollinators (especially large bees) and temperature, indicating the importance of current factors on out‐cross pollination. Two populations at the Southern edge of the species’ distribution showed high level of hand‐cross‐pollination and high flower visitation by large bees, but also a high level of autogamy resulting from recent colonization. Our results indicate that historical instability in climate has favored autogamy, most likely as a reproductive insurance strategy facilitating colonization and population maintenance over time, while pollinators are currently modulating the level of cross‐pollination.
Os padrões em ecologia são o produto de fatores contemporâneos interagindo a partir de uma bagagem histórica. Apesar desse reconhecimento, poucos estudos se ativeram em separar as contribuições dos fatores históricos e atuais como o clima, a identidade e comportamento de polinizadores sobre a reprodução de plantas. Neste trabalho nós decompomos a importância relativa dos processos contemporâneos e históricos no padrão geográfico do sistema reprodutivo da árvore comum no Cerrado, Curatella americana (Dilleniaceae). Especificamente nós perguntamos a) como o clima do presente e do quaternário afetam o sistema reprodutivo? b) Como a abundância e diversidade de polinizadores afeta o sistema reprodutivo da planta atualmente. c) Como o sistema reprodutivo se relaciona com a quantidade e qualidade dos frutos produzidos em C. americana? Para responder estas questões, nós registramos os polinizadores (riqueza, frequência e tamanho corporal) e realizamos testes de polinização em 10 populações de C. americana distribuídas em mais de 3.000 km de Cerrado no Brasil. A frutificação com autopolinização foi fortemente influenciada pela instabilidade climática do passado e não teve relação com os polinizadores no presente. Em contraste, a frutificação com polinização cruzada manual e natural foi afetada pelos polinizadores (especialmente abelhas grandes) e pela temperatura atual, revelando o papel de fatores ecológicos sobre a polinização cruzada. Duas populações na borda sul da distribuição de C. americana apresentaram alto nível de frutificação com polinização cruzada manual e altas taxas de visitação floral por abelhas grandes, mas também apresentaram alto nível de autogamia interpretadas como resultado da recente colonização dessas áreas. Nossos resultados indicam que a instabilidade climática do passado promoveu a autogamia como uma estratégia de segurança reprodutiva capaz de facilitar a colonização e manutenção de populações nesses locais com polinizadores imprevisíveis. Em contrapartida, nos locais com disponibilidade de polinizadores a polinização cruzada foi intensificada revelando a como processos históricos e contemporâneos atuam de forma sinérgica sobre o sistema reprodutivo das plantas.
2 More than just bees: the diversity of pollinators
3 To be a flower
4 Fidelity and promiscuity in Darwin’s entangled bank
5 The evolution of pollination strategies
6 A matter of time: from daily cycles to climate change
7 Agricultural perspectives
8 Urban environments
9 The significance of gardens
10 The shifting fates of pollinators
11 New bees on the block
12 Managing, restoring and connecting habitats
13 The politics of pollination
14 Studying pollinators and pollination
As you can see it’s a very wide-ranging overview of the subject, and written to be accessible to both specialists and non-specialists alike. To quote what I wrote in the Preface:
“While the book is aimed at a very broad audience, and is intended to be comprehensible to anyone with an interest in science and the environment, and their intersection with human societies, I hope it will also be of interest to those dealing professionally with plants and pollinators. The subject is vast, and those working on bee or hoverfly biology, for example, or plant reproductive ecology, may learn something new about topics adjacent to their specialisms. I certainly learned a lot from writing the book.”
The book is about 100,000 words in length, lots of illustrations, and there will be an index. My copy editor reckons there’s 450 references cited, though I haven’t counted. I do know that they run to 28 pages in the manuscript, and that’s with 11pt text. All going well it will be published before Christmas.
As I near completion of the copy-editing phase of my forthcoming book it’s frustrating to see all of the great research that’s been produced in recent weeks that I probably won’t be able to cite! Here’s a few things that caught my eye:
In the journal New Phytologist, Rhiannon Dalrymple and colleagues, including Angela Moles who hosted me during my recent stay in Australia, have a great study entitled Macroecological patterns in ﬂower colour are shaped by both biotic and abiotic factors. The title pretty much sums it up: in order to fully understand how flowers evolve we need to consider more than just their interactions with pollinators. It’s another demonstration of how we must look beyond simplistic ideas about pollination syndromes to fully understand the complexities of the relationship between flowering plants and pollinators…..
…..talking of which, again in New Phytologist, Agnes Dellinger asks: Pollinationsyndromes in the 21st century: where do we stand and where may we go? It’s an insightful and far-reaching review of a topic that has intrigued me for more than 25 years. There are still a lot of questions that need to be asked about a conceptual framework that, up until the 1990s, most people in ecology and biology accepted rather uncritically. One of the main unanswered questions for me is how further study of largely unexplored floras will reveal the existence of new pollination systems/syndromes. Which leads nicely to….
…..an amazing paper in Nature this week by Rodrigo Cámara-Leret etal. showing that New Guinea has the world’s richest island flora. The described flora includes 13,634 plant species, 68% of which are endemic to New Guinea! And the description of new species each year is not leveling off, there’s still more to be discovered. A commentary on the paper by Vojtech Novotny and Kenneth Molem sets some wider context to the work, and quite a number of media outlets have covered the story. Why is this relevant to pollinators and pollination? Well, we actually know very little about this critical aspect of the ecology of the island: there’s only a handful of published studies of plant-pollinator interactions from New Guinea, mostly focused on figs, bird-flower interactions, and a couple of crops. For such a biodiverse part of the world that’s a big gap in our understanding.
Finally, James Reilly, Rachael Winfree and colleagues have a paper in Proceedings of the Royal Society series B showing that: Crop production in the USA is frequently limited by a lack of pollinators. Most significant findings to me were that of the seven crops studied, five of them have their yields limited by lack of pollinators, and that even in areas of highly intensive farming, wild bees provided as much pollination service as honeybees.
That’s a few of the things that I spotted this week; what have you seen that’s excited or intrigued you? Feel free to comment.
In the next few months my new book Pollinators & Pollination: Nature and Society will be published. As you can imagine, I’m very excited! The book is currently available to pre-order: you can find full details here at the Pelagic Publishing website. If you do pre-order it you can claim a 30% discount by using the pre-publication offer code POLLINATOR.
As with my blog, the book is aimed at a very broad audience including the interested public, gardeners, conservationists, and scientists working in the various sub-fields of pollinator and pollination research. The chapter titles are as follows:
Preface and Acknowledgements
1. The importance of pollinators and pollination
2. More than just bees: the diversity of pollinators
3. To be a flower
4. Fidelity and promiscuity in Darwin’s entangled bank
5. The evolution of pollination strategies
6. A matter of time: from daily cycles to climate change
7. Agricultural perspectives
8. Urban environments
9. The significance of gardens
10. Shifting fates of pollinators
11. New bees on the block
12. Managing, restoring and connecting habitats
13. The politics of pollination
14. Studying pollinators and pollination
Natural history records of plant flowering and pollinator foraging, much of them collected by well informed amateurs, have huge scientific importance. One of the values of such records to ecology is that it allows us to document where these species occur in space and when they are active in time. This can be done at a range of spatial and temporal scales, but large-scale patterns (for example at a country level) are, I think, especially useful because they provide scientific evidence that can inform national conservation strategies.
During 2017 I collaborated with a young early career researcher at the University of Sussex, Dr Nick Balfour, on an analysis of the phenologies of British pollinators and insect pollinated plants. That study was recently published (see citation below) and I think that the results are fascinating.
Nick did most of the leg work on this, which involved assessing more than one million records that document the activity times of aculeate wasps, bees, butterflies and hoverflies held in the databases by three of the UK’s main insect recording organisations, the Bees, Wasps and Ants Recording Society (BWARS), the UK Butterfly Monitoring Scheme (UKBMS) and the Hoverfly Recording Scheme (HRS). Information on flowering times was taken from a standard British flora (Clapham et al. 1990 – Flora of the British Isles. Cambridge University Press).
As well as looking at annual flight periods and flowering trends for these organisms we also focused on pollinator and plant species that were endangered or extinct. Here are some headline results and thoughts on what the work shows:
About two-thirds (62%) of pollinator species peak in their flight times in the late summer (July and August), though there was some variation between the different groups – see the figure from the paper above). Particularly noticeable was the double peak of the bees, with the first peak denoting the activity of many early-emerging solitary bees, such as species of the genus Andrena, whilst the second peak is other solitary bees plus of course the bumblebees which by that time have built up their colonies.
A rather fixed phenological pattern with respect to different types of plants was also apparent, which I was not expecting at all: insect pollinated trees tend to flower first, followed by shrubs, then herbaceous species (again, refer to the figure above). This might be because larger plants such as trees and shrubs can store more resources from the previous year that will give them a head start in flowering the following year, but that idea needs testing.
Putting those first two points together, what it means is that trees tend to be pollinated by those earlier emerging bees and hoverflies, whereas the herbs are mainly pollinated by species that are active later.
When looking at the extinct and endangered pollinators, the large majority of them (83%) were species with a peak flight times in the late summer, a much larger proportion than would be expected given that 62% of all species are active at that time. However this was mainly influenced by extinct bee species and the same pattern was not observed in other groups.
The obvious explanation for that last point is that historical changes in land use have led to a dramatic reduction in late summer flowering herbaceous species and the subsequent loss of floral resources has been highly detrimental to those bees. But intriguingly no such pattern was apparent for the endangered pollinators and clearly there are complex reasons why pollinators should become rare or extinct, a point that I have discussed previously on the blog.
The long-term decline of wild and managed insect pollinators is a threat to both agricultural output and biodiversity, and has been linked to decreasing floral resources. Further insight into the temporal relationships of pollinators and their flowering partners is required to inform conservation efforts. Here we examined the
phenology of British: (i) pollinator activity; (ii) insect-pollinated plant flowering; and (iii) extinct and endangered pollinator and plant species. Over 1 million records were collated from the historical databases of three British insect monitoring organisations, a global biodiversity database and an authoritative text covering the national flora. Almost two-thirds (62%) of pollinator species have peak flight observations during late-summer
(July and August). This was the case across three of the groups studied: aculeate wasps (71% of species), bees (60%), and butterflies (72%), the exception being hoverflies (49%). When species geographical range (a proxy for abundance) was accounted for, a clear late-summer peak was clear across all groups. By contrast, there is marked temporal partitioning in the flowering of the major plant groups: insect-pollinated tree species blossoming predominantly during May (74%), shrubs in June (69%), and herbs in July (83%). There was a positive correlation between the number of pollinator species on the wing and the richness of both flowering insect pollinated herbs and trees/shrubs species, per calendar month. In addition, significantly greater extinctions occurred in late-summer-flying pollinator species than expected (83% of extinct species vs. 62% of all species). This trend was driven primarily by bee extinctions (80% vs. 60%) and was not apparent in other groups. We contend that this is principally due to declines in late-summer resource supplies, which are almost entirely provisioned by herbs, a consequence of historical land-use change. We hypothesize that the seasonality of interspecific competition and the blooming of trees and mass-flowering crops may have partially buffered spring flying pollinators from the impacts of historical change.
If any of you are near Wageningen University on 31st May I’m giving a talk about some of our recent research called “The macroecology and macroevolution of plant-pollinator interactions”. It’s preceded by a workshop on the whys and hows of science blogging. Details are in the poster.
Here are the abstracts for the talk and the workshop:
Macroecology and macroevolution of plant-pollinator interactions
Plant-pollinator relationships are an ecologically critical form of interaction that ensures the long-term survival of the majority of the world’s plants species, and contribute to a large fraction of global agricultural output. In additiondiversity and abundance of biotically pollinated plant species can be an important determinant of the diversity of animals at higher trophic levels.
Despite that global significance, most studies of plant-pollinator interactions are done at a local level, involving populations and communities of species, over modest time scales. The ways in which these local sets of interactions scale up to produce global macroecological and macroevolutionary patterns, and the processes underpinning them, will be explored using two case studies.
The first is a data set of 67 plant communities, ranging from 70ºN to 34ºS, with which we investigated the roles of biotic and abiotic factors as determinants of the global variation in animal versus wind pollination. Factors such as habitat type, species richness, insularity, topographic heterogeneity, current climate and late-Quaternary climate change were investigated. The predictive effects of these factors on the proportion of wind- and animal-pollinated plants were examined (see: Rech et al. 2016 – Plant Ecology & Diversity 9: 253-262).
Since these results were published we have increased the number of plant communities in our database to >90, and our findings seem to be robust to these additional data. The dominant influence of contemporary climate on the relative importance of wind-pollinated species suggests that communities may be sensitive to future climate change. Communities in areas that are predicted to become drier may in time contain more wind-pollinated plants which may in turn reduce the diversity of pollinator species that are present. There may also be implications for the prevalence of human pollen allergies. Future work will focus on these two areas.
The second case study uses a newly assembled database of pollinators of the family Apocynaceae (one of the ten largest families of flowering plants), supported by a molecular phylogeny of the major clades. This database has been used to explore phylogenetic and biogeographic patterns of pollinator exploitation (Ollerton et al. in review). The findings from this study challenge some long-held assumptions about convergent evolution, the role of rewards such as nectar, and the notion that some specialised pollination systems are evolutionary “dead ends”. It also highlights the function of novel floral features in determining pollinator type and behaviour, such as the fused gynostegium and pollinia found in the subfamily Asclepiadoideae. In summary, Apocynaceae is emerging as an important model family for understanding the ecology and evolution of plant-pollinator interactions.
Blogging for EEB: why bother?
A growing number of scientists in Ecology and Evolutionary Biology (EEB) have their own blogs or post as guests on others’ blogs. In this workshop we will explore motivations and strategies for blogging, and its advantages for early career researchers. Why blog? What does it do for one’s career? Is it a distraction from actually doing science? How does one build a blog readership? We will also focus on two aspects that are sometimes seen as mutually exclusive: blogging as science outreach to the general public (sci-communication), versus blogging with other professional scientists in mind (sci-community). As preparation for the seminar please read Saunders et al. (2017) Bringing ecology blogging into the scientific fold: measuring reach and impact of science community blogs
As an ecologist who has carried out field work in the temperate zone (UK), the subtropics (Tenerife and South Africa) and the tropics (parts of South America, Africa and Australia) I’ve always found the idea that the study of ecology can be divided into “tropical” and “non-tropical” a bit odd. It’s as if the way that the natural world works somehow changes at about 23 degrees north or south of the equator, making things “different” around the equator. The tropics are a very special, diverse place, it’s true, but so are many places outside the tropics.
With this in mind I was pleased when I was asked by some of my Brazilian colleagues to contribute to a chapter in a new book entitled Ecological Networks in the Tropics. It was an opportunity to review what is known about plant-pollinator networks in the tropics and the ways in which they are very similar to such networks at lower latitudes. Here’s the details of the chapter, followed by the abstract. If anyone wants a copy please drop me an email:
Vizentin-Bugoni J, PKM Maruyama, CS Souza, J Ollerton, AR Rech, M Sazima. (2018) Plant-pollinator networks in the tropics: a review. pp 73-91 In Dáttilo W & V. Rico-Gray. Ecological networks in the Tropics. Springer.
Most tropical plants rely on animals for pollination, thus engaging in complex interaction networks. Here, we present a global overview of pollination networks and point out research gaps and emerging differences between tropical and non-tropical areas. Our review highlights an uneven global distribution of studies biased towards non-tropical areas. Moreover, within the tropics, there is a bias towards the Neotropical region where partial networks represent 70.1% of the published studies. Additionally, most networks sampled so far (95.6%) were assembled by inferring interactions by surveying plants (a phytocentric approach). These biases may limit accurate global comparisons of the structure and dynamics of tropical and non-tropical pollination networks. Noteworthy differences of tropical networks (in comparison to the non-tropical ones) include higher species richness which, in turn, promotes lower connectance but higher modularity due to both the higher diversity as well as the integration of more vertebrate pollinators. These interaction patterns are influenced by several ecological, evolutionary, and historical processes, and also sampling artifacts. We propose a neutral–niche continuum model for interactions in pollination systems. This is, arguably, supported by evidence that a high diversity of functional traits promotes greater importance of niche-based processes (i.e., forbidden links caused by morphological mismatching and phenological non-overlap) in determining which interactions occur, rather than random chance of encounter based on abundances (neutrality). We conclude by discussing the possible existence and direction of a latitudinal gradient of specialization in pollination networks.
A fundamental feature of the natural world is that no species exists in isolation: all organisms interact with other organisms during their lives. These interactions take many forms and the outcome varies with the type of interactions. For example predator-prey interactions are clearly negative for the prey species, but positive for the predator. Other interactions result in positive outcomes for both species, including relationships between pollinators such as bees, birds and flies, and the flowers that they pollinate. An important feature of such interactions is how specialized or generalized it is; that is, how many different pollinators are actually involved in pollinating a particular type of flower, or how many types of flower does a specific pollinator visits.
In a newly published study, I have collaborated with colleagues from Denmark and Brazil to assess how local specialization (within a community) relates to regional specialization (across communities) using two separate data sets from the Brazilian rupestrian grasslands and Canary Island/North African succulent scrub vegetation.
Here’s the citation with a link to the paper (drop me a line if you can’t access it and need a PDF):
“Specialization of species is often studied in ecology but its quantification and meaning is disputed. More recently, ecological network analysis has been widely used as a tool to quantify specialization, but here its true meaning is also debated. However, irrespective of the tool used, the geographic scale at which specialization is measured remains central. Consequently, we use data sets of plant–pollinator networks from Brazil and the Canary Islands to explore specialization at local and regional scales. We ask how local specialization of a species is related to its regional specialization, and whether or not species tend to interact with a non-random set of partners in local communities. Local and regional specialization were strongly correlated around the 1:1 line, indicating that species conserve their specialization levels across spatial scales. Furthermore, most plants and pollinators also showed link conservatism repeatedly across local communities, and thus seem to be constrained in their fundamental niche. However, some species are more constrained than others, indicating true specialists. We argue that several geographically separated populations should be evaluated in order to provide a robust evaluation of species specialization.”
This is what those two different habitats look like:
In a new review paper that’s just been published in the Annual Review of Ecology, Evolution and Systematics I have looked at the question of just how diverse the pollinators are, and why pollinator biodiversity is ecologically important and therefore worthy of conservation. I’ve taken a deep time and wide space approach to this, starting with what the fossil record tells us about when animal pollination evolved and the types of organisms that acted as pollinators in the past (the answer may surprise you if you’re unfamiliar with the recent paleontological literature on this topic). Some of the most prominent biogeographical patterns have been highlighted, and I have tried to estimate the global diversity of currently known pollinators. A conclusion is that as many as 1 in 10 described animal species may act as pollen vectors.
As well as this descriptive part of the review I’ve summarised some recent literature on why pollinator diversity matters, and how losing that diversity can affect fruit and seed set in natural and agricultural contexts. Extinction of pollinator species locally, regionally, and globally should concern us all.
Although I was initially a little worried that the review was too broad and unfocused, having re-read it I’m pleased that I decided to approach the topic in this way. The research literature, public policy, and conservation efforts are currently moving at such a fast pace that I think it’s a good time to pause and look at the bigger picture of what “Saving the Pollinators” actually means and why it’s so important. I hope you agree and I’d be happy to receive feedback.