Category Archives: Mutualism
Research seminar: Dr Hazel Chapman – “Conservation ecology of West Africa’s montane forest habitats – seed dispersers and their substitutes”
Each year I’ve always added at least one Christmas-themed biodiversity post to the blog, for example: Thank the insects for Christmas, A Christmas vignette, and Six Kingdoms for Christmas. That’s partly because I really like Christmas as a winter festival, with its folklore and customs. But it’s also because these are a great vehicle to demonstrate how pervasive and important is natural capital and the ecosystem services it provides to society.
This year I’ve gone one stage further and actually published some Christmassy research to back up the blog post. Now, in a new study published in the Journal of Pollination Ecology, we have shown how important insect pollinators are in determining the market value of two of the most emblematic of Christmas plants: holly (Ilex aquifolium) and mistletoe (Viscum album). Here’s the full reference with a link to the paper itself, which is open access:
Ollerton, J., Rouquette, J.R. & Breeze, T.D. (2016) Insect pollinators boost the market price of culturally important crops: holly, mistletoe and the spirit of Christmas. Journal of Pollination Ecology 19: 93-97
Holly and mistletoe are two seasonal crops that play a culturally important role as symbols of Christmas across the world, though both also have pre-Christian pagan roots. Now for the first time the role of insect pollinators in determining the commercial value of these plants has been investigated, using sales records going back over the last eleven years from Britain’s largest annual auction of holly and mistletoe, held every year in Worcestershire.
Analysis of the sales records of Nick Champion Auctions in Tenbury Wells shows that insect pollination raises the sale price of these crops by on average two to three times. This is because holly and mistletoe with berries is more sought after than material without berries, with wholesale buyers paying higher prices at auction. These berries in turn are the result of pollination by insects such as flies and bees: both holly and mistletoe are 100% dependent on insect pollination due to their having separate male and female plants.
There is some annual variation to the prices, and in years where berries are scarce (possibly due to low insect numbers) the price difference can be four-fold.
Due to concerns about pollinator declines and food security there is huge interest in the role of bees and other insects in supporting agriculture, and how we can value that role. However we believe that this is the first study showing that insect pollinators play a large part in determining the value of culturally symbolic, non-food crops. Almost all of the economic valuations of insect pollination to agriculture have focused on food crops such as beans, apples, cocoa, coffee, and so forth. Very little is known about how the value of non-food crops (fibres, construction materials, pharmaceuticals, ornamentals, etc.) is enhanced by insect pollination. This is an area where much more research is required.
But in the mean time, where better to end than with a bit of seasonal John Clare?
The shepherd, now no more afraid,
Since custom doth the chance bestow,
Starts up to kiss the giggling maid
Beneath the branch of mistletoe
That ‘neath each cottage beam is seen,
With pearl-like berries shining gay;
The shadow still of what hath been,
Which fashion yearly fades away.
The Shepherd’s Calendar (1827)
The October issue of the Natural Areas Journal is a special one devoted to the topic of “Managing for Pollinators”. All of the papers have a North American focus but I think that they will be of general interest to anyone, anywhere in the world, who is concerned with how best to manage habitats for pollinators. Here’s the contents page of the issue, copied and pasted from the site; I’m not sure if the full text links will work if you or your institution does not have full text access, but you should at least be able to view the abstracts:
Editorial: Pollinators are in Our Nature
Introduction by USFS Chief Tidwell – Pollinators and Pollination
National Seed Strategy: Restoring Pollinator Habitat Begins with the Right Seed in the Right Place at the Right Time
Peggy Olwell and Lindsey Riibe
Hummingbird Conservation in Mexico: The Natural Protected Areas System
M.C. Arizmendi, H. Berlanga, C. Rodríguez-Flores, V. Vargas-Canales, L. Montes-Leyva and R. Lira
Floral Guilds of Bees in Sagebrush Steppe: Comparing Bee Usage of Wildflowers Available for Postfire Restoration
James H. Cane and Byron Love
The Role of Floral Density in Determining Bee Foraging Behavior: A Natural Experiment
Bethanne Bruninga-Socolar, Elizabeth E. Crone and Rachael Winfree
Common Methods for Tallgrass Prairie Restoration and Their Potential Effects on Bee Diversity
Alexandra Harmon-Threatt and Kristen Chin
Status, Threats and Conservation Recommendations for Wild Bumble Bees (Bombus spp.) in Ontario, Canada: A Review for Policymakers and Practitioners
Sheila R. Colla
Conserving Pollinators in North American Forests: A Review
James L. Hanula, Michael D. Ulyshen and Scott Horn
Dispersal Limitation, Climate Change, and Practical Tools for Butterfly Conservation in Intensively Used Landscapes
Laura E. Coristine, Peter Soroye, Rosana Nobre Soares, Cassandra Robillard and Jeremy T. Kerr
Revised State Wildlife Action Plans Offer New Opportunities for Pollinator Conservation in the USA
Jonathan R. Mawdsley and Mark Humpert
Diet Overlap of Mammalian Herbivores and Native Bees: Implications for Managing Co-occurring Grazers and Pollinators
Sandra J. DeBano, Samantha M. Roof, Mary M. Rowland and Lauren A. Smith
The Role of Honey Bees as Pollinators in Natural Areas
Clare E. Aslan, Christina T. Liang, Ben Galindo, Hill Kimberly and Walter Topete
Food Chain Restoration for Pollinators: Regional Habitat Recovery Strategies Involving Protected Areas of the Southwest
Steve Buckley and Gary Paul Nabhan
Forbs: Foundation for Restoration of Monarch Butterflies, other Pollinators, and Greater Sage-Grouse in the Western United States
R. Kasten Dumroese, Tara Luna, Jeremiah R. Pinto and Thomas D. Landis
Using Pollinator Seed Mixes in Landscape Restoration Boosts Bee Visitation and Reproduction in the Rare Local Endemic Santa Susana Tarweed,Deinandra minthornii
Mary B. Galea, Victoria Wojcik and Christopher Dunn
Save Our Bats, Save Our Tequila: Industry and Science Join Forces to Help Bats and Agaves
Roberto-Emiliano Trejo-Salazar, Luis E. Eguiarte, David Suro-Piñera and Rodrigo A. Medellin
The Importance of Phenological Diversity in Seed Mixes for Pollinator Restoration
Kayri Havens and Pati Vitt
The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes – Watts et al. (2016)
The second paper from the PhD thesis of my former student Dr Stella Watts has just been published in Annals of Botany – here’s a link to the journal’s website. It summarises the major findings from her field work on plant-pollinator interactions in the high Andes of Peru:
Watts, S., Dormann, C.F., Martín González, A.M. & Ollerton, J. (2016) The influence of floral traits on specialization and modularity of plant–pollinator networks in a biodiversity hotspot in the Peruvian Andes. Annals of Botany doi: 10.1093/aob/mcw114
This paper represents a major piece of research, including extensive field data collection over multiple sites in a challenging environment at altitude; state-of-the-art data analysis; and then summarising all of this into a single, digestible paper, with some great figures. I’m very proud to have been part of it!
Here’s the abstract; please email me or Stella if you’d like a copy of the full PDF:
Background and Aims: Modularity is a ubiquitous and important structural property of ecological networks which describes the relative strengths of sets of interacting species and gives insights into the dynamics of ecological communities. However, this has rarely been studied in species-rich, tropical plant–pollinator networks. Working in a biodiversity hotspot in the Peruvian Andes we assessed the structure of quantitative plant–pollinator networks in nine valleys, quantifying modularity among networks, defining the topological roles of species and the influence of floral traits on specialization.
Methods: A total of 90 transects were surveyed for plants and pollinators at different altitudes and across different life zones. Quantitative modularity (QuanBiMo) was used to detect modularity and six indices were used to quantify specialization.
Key Results: All networks were highly structured, moderately specialized and significantly modular regardless of size. The strongest hubs were Baccharis plants, Apis mellifera, Bombus funebris and Diptera spp., which were the most ubiquitous and abundant species with the longest phenologies. Species strength showed a strong association with the modular structure of plant–pollinator networks. Hubs and connectors were the most centralized participants in the networks and were ranked highest (high generalization) when quantifying specialization with most indices. However, complementary specialization d’ quantified hubs and connectors as moderately specialized. Specialization and topological roles of species were remarkably constant across some sites, but highly variable in others. Networks were dominated by ecologically and functionally generalist plant species with open access flowers which are closely related taxonomically with similar morphology and rewards. Plants associated with hummingbirds had the highest level of complementary specialization and exclusivity in modules (functional specialists) and the longest corollas.
Conclusions: We have demonstrated that the topology of networks in this tropical montane environment was non-random and highly organized. Our findings underline that specialization indices convey different concepts of specialization and hence quantify different aspects, and that measuring specialization requires careful consideration of what defines a specialist.
Academic conferences are an important part of what makes science function, via the exchange of ideas and information, publicly and in person. The act of sitting and listening to both established and early career researchers discussing their most recent work, sometimes before it’s in print, is stimulating and exciting, and will never be replaced by digital technology. We’re social animals and conferences, as much as anything else, are social events.
But conferences are becoming more expensive, more frequent, and increasingly out of reach to researchers with limited budgets. They are also getting larger: how many times have you attended a big conference and been torn between which of two (or three or four) talks to go to in parallel sessions? Wouldn’t it be nice to be able to see all of them? Or to go back and hear again the talks that you most enjoyed? Likewise, wouldn’t it be great if your students or members of the public could also see what such conference presentations are like?
With this in mind, some time ago I dreamed up the idea of “virtual conferences” in as an experiment that aims to bring together into one place the most interesting recorded seminars, webinars, conference talks and public lectures that are freely available, and present them as a series of themed mini-conferences. All of the videos in these collections are available on sites such as YouTube* and my role is just to curate them and present them in one place for convenience, as a showcase for some of the best research in biodiversity, evolutionary biology, ecology and conservation, very broadly defined, including inter-disciplinary and policy-related presentations. And just as at a conference, there’s an opportunity to discuss the talks in the comments section on each post and to provide links to other talks on the same topic.
As well as being a service to the research community and the wider public, I hope that these conferences will be a useful teaching resource at advanced undergraduate and postgraduate level.
If anyone is interested in guest-curating a set of presentations in their own subject area on this blog, please do get in touch and I’ll be happy to talk about it.
So here’s the first virtual conference, on (naturally) pollinators, pollination and flowers:
Judith Bronstein (University of Arizona)
Peter Crane (University of Chicago)
Jeffery Pettis (USDA Bee Research Laboratory, Maryland)
Linda Newstrom (Landcare Research, New Zealand)
Mace Vaughan and Eric Mader (Xerces Society/USDA/University of Minnesota)
Carlos Vergara, Rémy Vandame, and Peter Kevan (Universidad de las Americas-Puebla/El Colegio de la Frontera Sur/CANPOLIN)
Claire Kremen (University of California, Berkeley)
*I’m assuming that, as all of these videos are in the public domain, none of the presenters or copyright owners objects to them being presented here. If you do, please get in touch and I’ll remove it.
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 19th 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.
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.
Waser NM, Ollerton J, Erhardt A (2011) Typology in pollination biology: lessons from an historical critique. Journal of Pollination
Not strictly bare-foot, most of us are wearing socks and padding around the Tovetorp Research Station in Sweden, where outdoor shoes are banned in the building. The Scandinavian Association for Pollination Ecology is holding its 28th annual meeting here, starting Thursday evening with three initial talks, and continuing all today. I’ve posted about SCAPE previously: it’s my favourite conference by a long margin, friendly and informal and attracting some great science. Although I missed it last year due to my trip to Brazil, coming back this year is a little like coming back to a family gathering, where as well as the elder aunts and uncles, there’s also a large group of younger nieces and nephews, and some long-lost cousins – it’s a great mix of older professors, and newer PhD students.
This is a quick post before we have dinner and the bar opens. In the last 24 hours I have learned a lot about pollination ecology that I didn’t know before, including:
- Vincetoxicum hirundinaria does not vary in its outcrossing rate, regardless of the size of population (Anne Muola, Swedish Agricultural University)
- Arum italicum and Arum maculatum hybridise in some populations (Marion Chartier, University of Vienna)
- variable weather conditions can result in low bumblebee numbers and increased fly pollination in a north American mountain plant community (Diane Campbell, University of California)
- nocturnal pollination by moths is more common than expected in Spanish mountain plant communities (Marcos Mendez, Rey Juan Carlos University)
- “double mutualists” that both pollinate plants and disperse their seeds seem to be more common on islands than elsewhere (Jens Olesen, Aarhus University)
- colour “purity” is more important than other aspects of flower colouration (Klaus Lunau, Heinrich-Heine University)
- there’s very little evidence to support any of the current hypotheses regarding the evolution of andromonoecy (Marcos Mendez, again!)
Those are just a few of the highlights from a conference that’s showcasing some of the best pollination ecology research currently being conducted. Looks like dinner’s ready so I’ll sign off for now. My talk is tomorrow at 4.30pm – wish me luck!
In hushed tones the narrator describes the intricate details of yet another highly specialized relationship between one species of indescribable beauty and a second species with intricate behaviour that is about to eat/infect/cooperate with/exploit it [delete as appropriate].
The camera view pulls back to reveal the green cathedral of a tropical rainforest:
“The tropics” continues the narrator “are special…….…”
Yes, the tropics are special. But how special? Or more to the point, how different are tropical communities to temperate communities? Over at the Dynamic Ecology blog, Jeremy Fox has invited Angela Moles and myself to contribute a guest blog on the subject of whether the idea that species interactions are always stronger and more specialized in the tropics is outmoded and not backed up by the evidence. In Jeremy’s parlance, is it a zombie idea?
The subject of latitudinal variation in species interactions is one that has interested me for a while and I’ve written a few papers on the topic, especially in relation to how plant-pollinator interactions vary with latitude. You’ll find references to some of them in the Dynamic Ecology piece, plus a fuller over view of our arguments.
So what are you doing reading this? Get over to Dynamic Ecology and read that!
Review of “Pollination and Floral Ecology” by Pat Willmer (2011) Princeton University Press. £65. pp. 832.
Some backstory: In early 2012 I was asked by the review editor of the journal Annals of Botany to review this book, and I jumped at the chance as it’s the first major single-author overview of the field of pollination ecology for a number of years, by a well respected academic in the field. Unfortunately the review took a lot longer than I expected, in part because I was also coordinating my department’s Research Excellence Framework submission, on top of other teaching, research and admin duties, and it was taking up quite a bit of my time.
In addition I had mixed feelings about the book and wanted my review to do it justice, not be over-critical but at the same time highlight what I saw as flaws. In the words of the Fairport Convention song, Who Knows Where the Time Goes? – my review was only completed last Christmas and duly submitted. Turns out that the journal has a backlog of book reviews to publish and the editor asked that, given it’s been a couple of years since the book was published, would I mind if the review was posted on the Annals of Botany blog rather than in the printed journal. I happily agreed as it’s likely to get more readers on the blog, and said I’d also post it on my own blog. So here it is:
Any text book that tries to assess and summarise the whole of a multidisciplinary research field such as pollination ecology and floral biology is required to be four things: (1) comprehensive in its scope; (2) up to date in its coverage of the literature; (3) accurate in its assessment of the current state of the field; and (4) authoritative in the conclusions it presents.
This volume by Professor Pat Willmer of the University of St Andrews certainly ticks the first box. It’s a huge book, and covers everything relating to the evolution of flower attraction and reward systems, ecological interactions with pollinators, biochemistry, physiology, agriculture and conservation; all in 29 chapters split into three sections, with 87 pages of references. The literature extends to 2010, which is impressive for a book published in 2011 (though see my comments below about completeness of the literature). Specialist terms are highlighted in bold to direct the reader to the glossary at the back, a useful device even if there are a few inaccuracies, which I’ll mention later.
So far so good, and the author is to be congratulated on putting together such a comprehensive, not to mention timely, single-author book. It’s clearly the summation of a career devoted to studying pollinators and flowers, and the author’s passion for her subject is apparent throughout.
However when we come to points 3 and 4, things are less straightforward. There are some issues with accuracy that are troubling in a book aimed at newcomers to the field as well as established researchers. To give just a few examples:
– on p.18 we are told that asclepiads have “one stamen” (they have five); on p.169 and in the glossary that asclepiad pollinia are the pollen grains from one anther (they are the contents of half an anther); and on p.170 that the pollinaria are “glued” to pollinators (they actually clip on).
– in the glossary, tree ferns are referred to as “cycads”, an error that is repeated on p.89.
– on p.88 there is a statement suggesting that tree fern spores were dispersed by “animal fur” 300 million years ago, long before the evolution of mammals, and that this (and dispersal of spores of fungi and mosses) is the equivalent of pollination: it is not, it equates to seed dispersal.
These are troubling errors of basic botany that are forgivable in an early draft of the book (everyone makes mistakes) but not in the final published version, after it’s been read, reviewed, checked and edited. If the book goes to a second edition I hope that these (and other) mistakes will be fixed. But they do hint at a fundamental problem with a book (and a field) as large and complex as this: a single author is arguably unlikely to be able to do justice to all of the subject matter.
There are parts of the book where it is unclear (to me at least) what the author is actually saying. For example, on p.96 there is a graph which, it is suggested, demonstrates that pollination by animals is “technically uncommon when assessed in terms of the numbers of broad taxonomic groups that use it”, though the legend to the figure claims that “most orders of plants have no families” that possess wind pollination. This is confusing: what is to be concluded by someone new to the field? Is animal pollination common or rare? Likewise, on p.91 we are told that the “first angiosperms…would probably have had their pollen moved mainly by wind…”, but then on p.92 that “an element of insect pollination could be regarded as almost ancestral”. Which is correct?
There are other aspects to the book that are simply out of date; for example the linear, rather deterministic schemes set out in Figures 4.6 and 4.8 showing that Cretaceous flowers were open and radially symmetrical, and only later evolved into complex, bilateral flowers in the Tertiary, ignores fossil discoveries showing that orchids evolved in the Cretaceous (Ramírez et al., 2007). Likewise, discussion of “counterproductive” crypsis in flowers (p.124) neglects recent findings of cryptic, wasp-pollinated plants in South Africa (e.g. Shuttleworth & Johnson, 2009).
There is a theme emerging here: some of the botany that the book presents is inaccurate, confused or out-dated. Fortunately the zoological aspects of the book are much better, as one might hope from a Professor of Zoology.
The final criterion, that the book should be “authoritative in the conclusions it presents”, is however, in my view, the main weakness of this volume. The author is unhappy with recent developments in the field, particularly as they relate to community-scale assessments of plant–pollinator interactions, in terms of network analyses and predictive utility of pollination syndromes. Clearly Professor Willmer is on a mission to rebalance what she perceives as failings within some of the current trends in studying pollination. A book review is not the place for a technical dissection of the author’s arguments, which is best left to the peer-reviewed literature (though I would argue that that’s also the place to present some of the criticisms the author introduces, rather than into a text book such as this). I could focus the whole of this review on these topics because: (a) they take up a large proportion of the book, about one-third of the text pages; and (b) they are highlighted on the cover as being one of the main contributions of the book; specifically, that the author provides a critique of previous work that does not distinguish between “casual visitors and true pollinators” that can in turn result in “misleading conclusions about flower evolution and animal-flower mutualism”. Unfortunately her targets are straw men, and one – I believe quite telling – example will suffice.
On p.447 there is a criticism of the use by Waser et al. (1996) of Charles Robertson’s historical data set, and specifically that the analyses they present “…did not distinguish visitors from pollinators even though Robertson’s database did include information on this”. However Waser et al. clearly state (p.1045 of their paper) that only pollinators were included in the analyses, not all flower visitors, and that “visitation is not a synonym for pollination…non-pollinating visitors are excluded (as in Robertson 1928)” (p.1048).
Why should Professor Willmer make a statement to the contrary? Evidently she wishes to impress upon her readers that (in her opinion) there are fundamental problems in current approaches to studying pollination at a community level. But even if that were the case (and I don’t believe it is) misrepresenting previous studies to suit an argument is poor scholarship at best.
Regardless of whether some of her criticism is well founded, the author does not seem to appreciate that plant–flower visitor interaction networks are ecologically important regardless of whether or not a flower visitor acts as a pollinator. More fundamentally, true pollination networks possess similar attributes to flower visitor networks, for example a nested pattern of interactions, and arguments about level of generalisation of species are a matter of scale, not category (Ollerton et al., 2003).
At the end of her Preface, Professor Willmer reveals to us quite a lot about her personal attitude to research when she states that some readers might find her approach “too traditional” in an “era where ecological modelers [might be claimed to] have more to tell us than old-style field workers”. What the author fails to appreciate is that this is a grossly false dichotomy and that most of the pollination ecologists who have embraced new analytical methodologies for understanding plant–pollinator interactions are also “old-style field workers” with considerable experience of studying the ecology of flowers and their pollinators beyond the computer screen.
In summary this is a book that, for all its good qualities of comprehensiveness and (mostly) up to date coverage, should be read with caution: parts of it are neither as accurate nor as authorative as the field of pollination and floral ecology deserves.
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.
Ramírez SR, Gravendeel B, Singer RB, Marshall CR, Pierce NE. 2007. Dating the origin of the Orchidaceae from a fossil orchid with its pollinator. Nature 448: 1042-1045.
Shuttleworth A, Johnson SD. 2009. The importance of scent and nectar filters in a specialized wasp-pollination system. Functional Ecology 23: 931-940.
Waser NM, Chittka L, Price MV, Williams N, Ollerton J. 1996. Generalization in pollination systems, and why it matters. Ecology 77: 1043-1060.
Relationships involving a “household of three” hold a fascination that is part prurient and part wonderment: prurient for perhaps obvious reasons, and wonderment as it’s sometimes hard enough to make a ménage à deux work! Historically this domestic arrangement has been the lifestyle of choice of a surprisingly large and diverse set of influential thinkers and creative individuals, including Aldous Huxley, Lord Nelson, Carl Jung, Erwin Schrödinger, and Hattie Jacques. Indeed, one of my favourite musicians, David Crosby, wrote a song about such relationships (Triad) which got him kicked out of The Byrds.
In nature, ménage à trois are occasionally encountered and may be more common than we think, and have been on my mind because this week I’ve been talking about mutualistic relationships with my first year undergraduates. Mutualisms are interactions between species in which both benefit, as opposed to exploitative relationships such as predation or parasitism in which one of the partners is at a disadvantage (being eaten is a great disadvantage….) Mutualistic interactions are common and important, and include many (but not all) plant-pollinator interactions, seed dispersal by birds and other animals, mycorrhizal relationships between plants and fungi, and many more. As well as studying plant-pollinator interactions, I’ve a long-standing interest in the full breadth of these examples of “biological barter“, in all their varied forms.
In most cases mutualistic relationships involve pairs of species (for example a plant and a pollinator) although these species pairs are embedded within a larger network of interactions: that plant may have many pollinators, and those pollinators may service other plants. In this sense it requires just two partners to make the interaction work – a “household of two”. More rarely, research on the biodiversity of species interactions throws up examples of “households” involving three species, and a fascinating case has recently been worked out and published by Jonathan Pauli and colleagues. This involves three-toed sloths and their relationship with the algae and moths that colonise the sloth’s fur – you can read the abstract here. In summary, the algae benefit from nutrients provided by the moths living in the fur; the sloths eat the algae to supplement a restricted diet of leaves; the moths benefit from the sloths transporting them to defecation sites where they lay their eggs, then recolonise the sloths. This slothy ménage à trois is a wonderful instance of interdependency within nature.
The other case of a three-part mutualism with which I’m familiar is that between anemonefish, and sea anemones and the algae which are housed in their tentacles. The fish and the anemones provide mutual defence of one another, whilst the algae photosynthesise and provide carbohydrates to the anemone, and benefit from the nitrogenous waste produced by the fish. It’s a system that I’ve done a little work on with marine biologist colleagues, specifically the broad scale biogeography of the interaction and its local assemblage structure, but we’ve not studied the whole three-part system.
What other three-part examples are there in nature? I’d be very interested to hear about any of which you’re aware.
It begs a question as to whether three is an upper limit to the number of species that can engage in such relationships? Are there any four- or five-part mutualisms? Or are these too unstable over evolutionary time, because if one species goes extinct it could cause the extinction of other species? Interesting questions about fascinating interactions!