As I’ve previously discussed on the blog, when species are moved to a different part of the world they lose many of the ‘enemies’ – such as predators, herbivores and pathogens – that would normally keep their populations in check. This can have implications for the likelihood of a species becoming invasive, and it’s called the Enemy Release Hypothesis (ERH) and has been well studied. Less well researched is the flip side of the ERH, the Missed Mutualist Hypothesis (MMH), in which species lose their ‘friends’, such as pollinators, seed dispersers, symbiotic fungi, and so forth. It’s a topic I’ve worked on with my colleagues at the University of New South Wales, principally Angela Moles and her former PhD student Zoe Xirocostas.
Another paper from Zoe’s PhD work has just been published and in it she carried out a comparison of European plants that have been transported to Australia, and asked whether they had fewer pollinators in their new range. It turns out that they do!
Here’s the full reference with a link to the paper, which is open access:
Many studies seeking to understand the success of biological invasions focus on species’ escape from negative interactions, such as damage from herbivores, pathogens, or predators in their introduced range (enemy release). However, much less work has been done to assess the possibility that introduced species might shed mutualists such as pollinators, seed dispersers, and mycorrhizae when they are transported to a new range. We ran a cross-continental field study and found that plants were being visited by 2.6 times more potential pollinators with 1.8 times greater richness in their native range than in their introduced range. Understanding both the positive and negative consequences of introduction to a new range can help us predict, monitor, and manage future invasion events.
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The summer of 2019, before the COVID-19 pandemic turned the world on its head, feels like a very long time ago. Early in that summer, as I recounted on this blog, Zoe Xirocostas joined my research group for a while in order to collect data for her PhD on the comparative ecologies of plants that are native to Europe but invasive in Australia. That work has proven to be very successful, and the latest paper from Zoe’s PhD has just been published.
The paper focuses on the “enemy release hypothesis” (ERH), a well-studied concept in invasion ecology that nonetheless generates significant debate and disagreement. In essence, the ERH posits that the reason why so many species become invasive is that they leave their consumers, pathogens and parasites behind when they move to a new locality. Those “enemies” would normally reduce the fecundity of the invader, putting a brake on their population growth. But in their absence, the invader can become far more successful. Of course, as well as leaving “enemies” behind the invader also loses its “friends”, such as pollinators, seed dispersers, and defensive or nutritional partners. This “Missed Mutualist Hypothesis” is something that I’ve recently explored with Angela Moles, who was Zoe’s main supervisor, and other collaborators in Australia. Expect to hear more about this from Zoe’s work in the near future.
But back to the enemies. Drawing on the most extensive set of standardised comparisons yet collected of the same plants in native and invasive habitats, Zoe found that plants in the invasive populations suffer on average seven times less damage from insect herbivores, as predicted by the (ERH). Rather remarkably, however, the amount of enemy release enjoyed by a plant species was not explained by how long the species had been present in the new range, the extent of that range, or factors such as the temperature, precipitation, humidity and elevation experienced by the native versus invasive populations.
In other words, it’s extremely hard to predict the extent of enemy release based on historical and ecological considerations that one might expect to impose a strong influence.
The study has just appeared in Proceedings of the Royal Society series B and is open access. Here’s the reference with a link to the paper:
When a plant is introduced to a new ecosystem it may escape from some of its coevolved herbivores. Reduced herbivore damage, and the ability of introduced plants to allocate resources from defence to growth and reproduction can increase the success of introduced species. This mechanism is known as enemy release and is known to occur in some species and situations, but not in others. Understanding the conditions under which enemy release is most likely to occur is important, as this will help us to identify which species and habitats may be most at risk of invasion. We compared in situ measurements of herbivory on 16 plant species at 12 locations within their native European and introduced Australian ranges to quantify their level of enemy release and understand the relationship between enemy release and time, space and climate. Overall, plants experienced approximately seven times more herbivore damage in their native range than in their introduced range. We found no evidence that enemy release was related to time since introduction, introduced range size, temperature, precipitation, humidity or elevation. From here, we can explore whether traits, such as leaf defences or phylogenetic relatedness to neighbouring plants, are stronger indicators of enemy release across species.
All organisms – be they plants, animals, fungi, or whatever – interact with other species throughout their lives, in relationships that include predation, parasitism, commensalism, and the many and varied forms of mutualism. But when species are transported to a different part of the world, as has happened often during the Anthropocene, these interactions typically break down because usually only one of the participants moves. This loss of ecological relationships can play a role in whether or not a species becomes established in its new home, and has been mostly explored in the “Enemy Release Hypothesis” (ERH) which predicts that, by leaving behind predators or parasites or herbivores, a species becomes more ecologically successful and ultimately invasive in its novel range.
Less well studied, though potentially just as important, is the “Missed Mutualist Hypothesis” (MMH) which in a sense is the twin of the ERH. As well as leaving behind “enemies”, introduced species leave behind “friends” such as pollinators, seed dispersers, mycorrhizal fungi, defensive partners, and other mutually beneficial associates. Negative effects arising from the loss of these relationships could potentially balance the positive impacts arising from the ERH.
In a new quantitative review just published, we review what’s known about the MMH (currently much less than the ERH) and suggest some fruitful lines of enquiry. The study is led by Angela Moles, my collaborator at the University of New South Wales where I spent time as a Visiting Research Fellow in 2019/20 (see my blog posts about that visit starting here). The paper has had a long gestation and gone through several iterations and revisions since we started writing it in late 2019, not least caused by the covid pandemic, but I think that it’s all the better for it.
Here’s the full reference with a link to the paper:
Introduced species often benefit from escaping their enemies when they are transported to a new range, an idea commonly expressed as the enemy release hypothesis. However, species might shed mutualists as well as enemies when they colonize a new range. Loss of mutualists might reduce the success of introduced populations, or even cause failure to establish. We provide the first quantitative synthesis testing this natural but often overlooked parallel of the enemy release hypothesis, which is known as the missed mutualist hypothesis.
Meta-analysis showed that plants interact with 1.9 times more mutualist species, and have 2.3 times more interactions with mutualists per unit time in their native range than in their introduced range. Species may mitigate the negative effects of missed mutualists. For instance, selection arising from missed mutualists could cause introduced species to evolve either to facilitate interactions with a new suite of species or to exist without mutualisms. Just as enemy release can allow introduced populations to redirect energy from defence to growth, potentially evolving increased competitive ability, species that shift to strategies without mutualists may be able to reallocate energy from mutualism toward increased competitive ability or seed production. The missed mutualist hypothesis advances understanding of the selective forces and filters that act on plant species in the early stages of introduction and establishment and thus could inform the management of introduced species.
The question of whether interactions between different species are more specialised in tropical environments (as theory predicts) has intrigued me for a couple of decades. In fact it’s just occurred to me that August 2022 was the 20th anniversary of my paper in Oikos co-authored with Louise Cranmer entitled: Latitudinal trends in plant-pollinator interactions: are tropical plants more specialised? That paper was one of the first to seriously challenge an idea that was long-embedded in the scientific and (especially) popular literature, that tropical ecology was in a sense “special” and that the ways in which species parasitised, consumed, or engaged in mutualistic relationships in the tropics was different to what was happening in the subtropics and temperate zones.
Since then I’ve written about this subject in a number of publications, most recently in my book Pollinators & Pollination: Nature and Society and it’s inspired some other researchers to address the topic.
One of the real challenges with asking questions about how plant-pollinator relationships change over large geographical areas is obtaining good, robust data to analyse. It’s a challenge to convince science funding agencies to give money to spend many years travelling the world and collecting the kind of data that are needed. However we can gain some idea of the patterns, and potential processes, that drive the macroecology of plant-pollinator interactions by piecing together databases of interactions for particular taxa, gleaned from published and unpublished sources.
That’s what we have done for the family Cactaceae in a new study led by Pablo Gorostiague from the Universidad Nacional de Salta in Argentina. This collaboration started when Pablo visited Northampton back in 2018 and spent some time with my research group, including helping out with field work in Tenerife. Since then the usual issues (work, COVID, etc.) have delayed publication of our paper, but now it’s finally out. Amongst other results we find that, yes, tropical cacti are pollinated by fewer species on average (though it’s hugely variable – see the figure above) but that functional specialisation (i.e. the number of pollinator guilds that are used by species) is no different in the tropics compared to the extra-tropics (that’s the figure at the end of this post).
The full reference with a link to the paper is below; if anyone wants a PDF, please send me a message via the Contact page:
Biotic interactions are said to be more specialized in the tropics, and this was also proposed for the pollination systems of columnar cacti from North America. However, this has not yet been tested for a wider set of cactus species. Here, we use the available information about pollination in the Cactaceae to explore the geographic patterns of this mutualistic interaction, and test if there is a latitudinal gradient in its degree of specialization.
We performed a bibliographic search of all publications on the pollination of cacti species and summarized the information to build a database. We used generalized linear models to evaluate if the degree of specialization in cacti pollination systems is affected by latitude, using two different measures: the number of pollinator guilds (functional specialization) and the number of pollinator species (ecological specialization).
Our database contained information about the pollination of 148 species. The most frequent pollinator guilds were bees, birds, moths and bats. There was no apparent effect of latitude on the number of guilds that pollinate a cactus species. However, latitude had a small but significant effect on the number of pollinator species that service a given cactus species.
Bees are found as pollinators of most cactus species, along a wide latitudinal gradient. Bat and bird pollination is more common in the tropics than in the extra-tropics. The available information suggests that cacti pollination systems are slightly more ecologically specialized in the tropics, but it does not support any trend with regard to functional specialization.
Most of us have at some time stared in fascination at the life contained within the pools that form on rocky shores at low tide. But none of us realized that a whole new class of ecological interaction was taking place!
The 12,000 or so described (and many un-named) seaweeds are incredibly important organisms. Their diverse and abundant photosynthesizing fronds make them one of the main primary producers in coastal seas, creating food and habitat for a huge range of animals. Not only that, but some – the coralline seaweeds – lock up vast amount of CO2 as calcium carbonate and help to create reef systems in the same way as coral.
Although scientists have studied seaweeds for hundreds of years, many aspects of their ecology are still unknown. Their detailed mode of reproduction, for example has only been studied in a small proportion of species.
In a newly published study in the journal Science, French PhD researcher Emma Lavaut and her colleagues have shown that small isopod crustaceans – relatives of woodlice and sea slaters – facilitate the movement of the equivalent of seaweed sperm (termed “spermatia”) from male to female reproductive structures in just the same way that bees and other pollinators move pollen between flowers, so fertilizing female gametes.
Your read that correctly: some seaweeds have pollinators!
It’s an incredible finding! And the implications of this are enormous: Emma and her colleagues have added a whole new branch of life to the examples of sedentary (fixed-place) organisms that require a third party to enable their reproduction. In addition to being a fascinating biological discovery, it has significant environmental and sustainability implications.
Seaweeds are a diverse group of macroalgae that appeared more than one billion years ago, at least 500 million years before the evolution of what we think of as “true” plants, such as the flowering plants, conifers, cycads, ferns and mosses. Sexual reproduction in the brown and green seaweeds, which include kelps, wracks and sea lettuces, involves spermatia that are mobile and use a flagellum to swim through the water to seek out female reproductive structures. However, Emma studied a seaweed, Gracilaria gracilis, which belongs to the Rhodophyta or red seaweeds, and none of the species in this group have these swimming sperm equivalents.
Sexual reproduction in the red seaweeds has therefore always been something of a mystery. Three quarters of species have separate male and female individuals and so they cannot mate with themselves. It was assumed that the gametes were just released into water currents that haphazardly transported them to the female reproductive organs, much as wind pollinated grasses and pine trees release their vast clouds of pollen on land. The authors of this new study, however, point out that most sexual reproduction by these red seaweeds takes place in the relatively still waters of rock pools, a habitat that they mimicked in the laboratory in a series of elegant aquarium experiments.
The isopod crustaceans are attracted to the seaweed because they provide a habitat away from predators and a supply of food: they graze on the microalgae that colonise the seaweed’s fronds. Picking up spermatia and moving them between fronds is a side-effect of this activity by the small invertebrates. As you can see from the illustration above, the isopods and the seaweed are engaged in a “double mutualism“: a plus sign (+) indicates a positive effect of one species on another, while a minus sign (-) indicates a negative impact.
What I find especially fascinating about this research is that both the seaweed (Gracilaria gracilis) and the isopod (Idotea balthica) were originally described as species more than 200 years ago. They also have an extremely wide distribution. The isopod is found around the coasts of Europe and down the eastern seaboard of the Americas. The seaweed is pretty much found globally. These are not rare, unusual species, yet the interaction between them has only just been discovered! This is a point that I made in my recent book Pollinators & Pollination: Nature and Society: quite often, species that are well known interact in previously undocumented ways because no one has had the time or inspiration to look closely at them.
Although the idea that small sea creatures might be helping seaweeds to reproduce sounds very fanciful, there is a precedence for this discovery. Back in 2016, in a paper published in Nature Communications, a group of Mexican researchers led by Brigitta van Tussenbroek showed that a species of seagrass is pollinated by a diverse assemblage of small crustaceans and polychaete worms. Seagrasses are flowering plants, not seaweeds, but clearly this type of mutually beneficial relationship can exist between different species in the oceans.
Rhodophyta are the most diverse group of seaweeds, with more than 7,000 known species. They are especially abundant on coastal shores, oceanic habitats that are under huge pressure from infrastructure development, pollution, and climate change. At the same time, these seaweeds are economically important and millions of tonnes of them are collected every year as food, as nutritional and pharmaceutical supplements, and to produce agar. In order to conserve these seaweed populations, we need to better understand their ecology and their environmental requirements.
The work by Emma Lavaut and colleagues suggests that interactions with their “pollinators” may be a critical aspect of this understanding. In the same way that “Save the Bees” has been a rallying call for conserving interactions between species on land, we may soon hear this message echoed in “Save the Isopods”. At the very least, I have to add a new section to the second edition of my book!
Full disclosure: I was one of the reviewers of the original manuscript submitted to Science by Emma and her co-authors. It’s a rare privilege to review a study and think: “Wow! This is a game-changer!” and including this paper it’s happened to me only a handful of times. The editors at Science kindly invited my colleague Dr Zong-Xin Ren and myself to write a Perspective piece about the work and we were delighted to do so.
Image credits: Isopod and diatom images from Lavaut et al (2022). Gracilaria image by Emoody26 at English Wikipedia CC BY 3.0 https://commons.wikimedia.org/w/index.php?curid=3455016. Design by Shijia Wen and Jeff Ollerton.
I love going to botanic gardens and I keep a “life list” of those that I have visited. So on a visit to Lund University last week, to give a seminar and take part in an MSc defence, I was delighted to be able to add another one to that list. Lund University Botanical Garden is quite small, like many such urban gardens, and this is not the best time of the year to visit. But there was a good show of early spring plants in flowers, the sun was shining, and quite a number of people were enjoying the peace and calm in the middle of a city.
The glasshouses were especially busy, and they have a nice collection of cold-sensitive plants arranged by habitat and taxonomy, such as cacti and succulents, ferns, orchids, and so forth. One of the reasons why I enjoy botanic gardens so much is that I always, without exception, see plants that I have never previously encountered, often doing unexpected things.
Lund was no exception, and I was particularly intrigued by a plant called Monolena primuliflora which was being grown in a hanging basket, as is often the case with epiphytic plants. It’s a species of Melastomataceae, a family that I know well from tropical field work. But this one looked unlike any melastome that I’d ever seen. In particular, I was drawn to the large rhizome or caudex from which the leaves emerge:
This immediately reminded me of some of the epiphytic “ant plants” such as species of Myrmecodia and Hydophytum and especially ferns such as Lecanopteris. All of these myrmecophyte genera have evolved swollen stems or rhizomes which house colonies of ants. The ants in turn defend the plants against herbivores, in a mutualistically advantageous relationship.
Sure enough, when I searched online for information about Monolena primuliflora, it’s widely described in the house plant community as an “ant plant” – see here and here for example. After I tweeted about this, biologist Guillaume Chomicki (who has been researching these ant-plant interactions) was intrigued but asked about the evidence for it being a myrmecophyte:
What's the evidence for it being an ant-plant? It's not obvious based on these photos. If you are anyone has more info or list, please let me know so that I can update my database!
That got me thinking, so I dug around in the botanical literature for the evidence and found…..nothing. The standard monograph on the genus by Warner (2002) doesn’t mention it and as far as I can tell (please someone will correct me if I am wrong) there’s no documented study of this species or genus having a myrmecophytic relationship with ants.
If I’m correct, how has the idea of Monolena primuliflora as an ant plant come about? This is a relatively new introduction to the houseplant trade and I suspect that plant sellers have made assumptions about the swollen rhizome (as I did!) to make the plant sound more interesting. There’s no doubt that the rhizome is fascinating and unusual in the family, but its function may be to store water (as found in many epiphytic orchids) rather than to house ants.
In my recent book Pollinators & Pollination: Nature and Society, and in this article last year in the magazine British Wildlife, I discussed how the world of plants (and pollinators) is full of myths and misunderstandings. This seems to be another one and by writing this blog post I’m hoping that we can clarify the situation with regard to Monolena primuliflora. So if you have any further information about it, please do comment below.
My thanks to everyone on Twitter who commented about the plant, especially Guillaume for asking the question!
A couple of weeks ago we visited Karin’s family in Jutland and went for a couple of long walks around the area. One of these took us through some very nice mixed pine, oak, and birch forest close to a river. The forest was anchored into a thin horizon of mulchy topsoil, beneath which was almost pure sand, a post-glacial legacy of the wider, wilder rivers that ran through the region at the end of the last Ice Age.
Where our path ran parallel to the river I noticed that the exposed vertical sections were far from lifeless: the sandy faces had been colonised by algae, lichens, fungi, cyanobacteria, and mosses. These biological crusts had stabilised the sand and prevented it from eroding further back into the bank. On a miniature scale they were doing what forests and other vegetation does in mountainous areas all over the world: preventing landslides.
Biological crusts in turn provide opportunities for ferns and seed plants to germinate and gain a foothold: they are often the starting point for further ecological succession.
Not only are these crusts acting as substrate stabilisers and seed beds, but all of the usual ecological processes of photosynthesis, nutrient acquisition, decomposition, carbon storage, symbiosis and competition are taking place in just a few millimetres of biodiversity. There’s a lot going on in these thin veneers of life.
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.
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
References
Index
Prof. Jeff Ollerton - ecological scientist and author 