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.