Category Archives: Mutualism

Trait evolution, resource specialization and vulnerability to plant extinctions among Antillean hummingbirds – a new study just published

Hummingbird bowl from BM

Hummingbirds are fascinating creatures and important pollinators for a wide range of plants in the New World (and, historically, possibly in the Old World – see this post from 2014: There were hummingbirds over the White Cliffs of Dover).  During the last decade I have been involved in some hummingbird-related research with several colleagues, particularly Dr Bo Dalsgaard and Dr Stella Watts, and it’s generated some really interesting findings about the biogeography, macroecology, and interactions with plants of these most elegant of birds.

The latest installment of this work is a test of some ideas relating to the vulnerability of hummingbirds on islands to the extinction of their plant partners.  It’s just been published and the reference is:

Dalsgaard B., Kennedy J.D., Simmons B.I., Baquero A.C., Martín González A.M., Timmermann A., Maruyama P.K., McGuire J.A., Ollerton J., Sutherland W.J. & Rahbek C. (2018) Trait evolution, resource specialization and vulnerability to plant extinctions among Antillean hummingbirds. Proceedings of the Royal Society series B (in press)

Here’s the abstract:

Species traits are thought to predict feeding specialization and the vulnerability of a species to extinctions of interaction partners, but the context in which a species evolved and currently inhabits may also matter. Notably, the predictive power of traits may require that traits evolved to fit interaction partners. Furthermore, local abiotic and biotic conditions may be important. On islands, for instance, specialized and vulnerable species are predicted to be found mainly in mountains, whereas species in lowlands should be generalized and less vulnerable. We evaluated these predictions for hummingbirds and their nectar-food plants on Antillean islands. Our results suggest that the rates of hummingbird trait divergence were higher among ancestral mainland forms before the colonization of the Antilles. In correspondence with the limited trait evolution that occurred within the Antilles, local abiotic and biotic conditions—not species traits—correlate with hummingbird resource specialization and the vulnerability of hummingbirds to extinctions of their floral resources. Specifically, hummingbirds were more specialized and vulnerable in conditions with high topographical complexity, high rainfall, low temperatures and high floral resource richness, which characterize the Antillean Mountains. These findings show that resource specialization and species vulnerability to extinctions of interaction partners are highly context-dependent.

As always I’m happy to send a PDF to anyone who drops me an email.

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Plant-pollinator networks in the tropics: a new review just published.

P1080615

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.

Abstract:

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.

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Local and regional specialization in plant–pollinator networks: a new study just published

Euphorbia canariensis pollinators 2016-04-29 17 58 00

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):

Carstensen, D.W., Trøjelsgaard, K., Ollerton, J. and Morellato, L.P.C. (2017) Local and regional specialization in plant–pollinator networks. Oikos (in press) doi:10.1111/oik.04436

The abstract is as follows:

“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:

If you would like more information on plant-pollinator networks, including details of an edible game for Christmas (!), follow this link to the standingoutinmyfield blog.

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Pollinators, flowers, natural selection and speciation: a virtual conference

Ashy Mining Bee 2017-06-17 10.55.45

It’s been a couple of years since I posted my previous “virtual conferences” on Pollinators, Pollination and Flowers and Ecology and Climate Change, a lapse that has largely been due to lack of time (my default excuse for most things these days….).  However Judith Trunschke at Uppsala University in Sweden has risen to the challenge of guest-curating her own virtual conference*.  The theme here is how pollinators impose (or sometimes don’t impose) natural selection on flowers that results in the formation of new plant species:

Timo van der Niet (IIASA 2010): Plant-diversification through pollinator shifts

Timo van der Niet (Congresos UCA 2014): Disentangling the contribution of pollinators in shaping angiosperm orchid genus Satyrium

Anne Royer (Evolution 2016): Plant-pollinator association doesn’t explain disruptive selection & reproductive isolation

Brandon Campitelli (Evolution 2016): Pollinator-mediated selection and quantitative genetics

Yuval Sapir (Evolution 2016): Rethinking flower evolution in irises: are pollinators the agents of selection?

Ruth Rivken (Evolution 2014): The mechanisms of frequency-dependent selection in gynodiocious Lobelia siphilitica

Gonzalo Bilbao (Botany 2017): Pollinator-mediated convergent shape evolution in tropical legumes

My grateful thanks to Judith for curating this great set of talks; if anyone else would like to do the same, please get in touch.

Feel free to discuss the talks in the comments section and to post links to other talks on the same topic.

 

*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.

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Pollinator biodiversity and why it’s important: a new review just published – download it for free

P1110763

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.

You can download a PDF of the review entitled Pollinator Diversity: Distribution, Ecological Function, and Conservation by following that link.

Pollination ecologists should also note that in this same volume of Annual Review of Ecology, Evolution and Systematics there’s a review by Spencer Barrett and Lawrence Harder called The Ecology of Mating and Its Evolutionary Consequences in Seed Plants.  If you contact those authors I’m sure they’d let you have a copy.

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Generalist pollination can evolve from more specialised interactions: a new study just published

2013-11-24 15.44.01

There’s a long-standing idea in biology that ecological specialisation is an evolutionary “dead end” from which species can never emerge.  In other words, if a species becomes so adapted to a particular ecological strategy (could be feeding or habitat requirements or how it interacts with other species ) then no amount of natural selection will result in its descendants evolving different strategies, thereby diversifying into new species.  In particular it’s traditionally thought that evolving broader, “generalist” strategies from narrower, “specialised” ones is highly unlikely.

This has been much discussed in the literature on the ecology and evolution of pollination systems, where traditionally this “dead end” scenario has been accepted.  However a small number of case studies have shown that generalised pollination systems can evolve within much more specialised clades, beginning with Scott Armbruster and Bruce Baldwin’s study of Madagascan Dalechampia (Euphorbiaceae), published in Nature in 1998.

To this limited body of examples we can now add another case study: in the genus Miconia (Melastomataceae), generalist nectar/pollen rewarding strategies can evolve within a clade of plants that predominantly uses a more specialised, buzz-pollinated strategy involving just bees.

The work is part of the PhD research of Vinicius de Brito who is one of the researchers I was privileged to do some field work with in Brazil when I was there in 2013 – see my post: “It’s called rainforest for a reason, right?  Brazil Diary 6“.  Vini is the guy on the left of the photo accompanying this post.  Here’s the citation and a link:

de Brito, V.L.G., Rech, A.R., Ollerton, J., Sazima, M. (2017) Nectar production, reproductive success and the evolution of generalised pollination within a specialised pollen-rewarding plant family: a case study using Miconia theizans. Plant Systematics and Evolution doi:10.1007/s00606-017-1405-z 

Here’s the abstract:

Generalist plant–pollinator interactions are prevalent in nature. Here, we untangle the role of nectar production in the visitation and pollen release/deposition in Miconia theizans, a nectar-rewarding plant within the specialised pollen-rewarding plant family Melastomataceae. We described the visitation rate, nectar dynamics and pollen release from the poricidal anthers and deposition onto stigmas during flower anthesis. Afterwards, we used a linear mixed model selection approach to understand the relationship between pollen and nectar availability and insect visitation rate and the relationship between visitation rate and reproductive success. Miconia theizans was visited by 86 insect species, including buzzing and non-buzzing bees, wasps, flies, hoverflies, ants, beetles, hemipterans, cockroaches and butterflies. The nectar produced explained the visitation rate, and the pollen release from the anthers was best explained by the visitation rate of pollinivorous species. However, the visitation rates could not predict pollen deposition onto stigmas. Nectar production may explain the high insect diversity and led to an increase in reproductive success, even with unpredictable pollen deposition, indicating the adaptive value of a generalised pollination system.

As always, I’m happy to send a PDF to anyone who wants a copy, just drop me an email.

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Research seminar: Dr Hazel Chapman – “Conservation ecology of West Africa’s montane forest habitats – seed dispersers and their substitutes”

We start the new term with a guest speaker from New Zealand – Dr Hazel Chapman – who is coming to give a research seminar this Friday at 1pm in Newton NW205, University of Northampton, Avenue Campus. Here’s the details:
 
Conservation ecology of West Africa’s montane forest habitats – seed dispersers and their substitutes.
 
The Nigerian Montane Forest Project (NMFP) is a conservation and biodiversity research program founded on a field station located on the Nigeria-Cameroon border. Run out of the University of Canterbury, New Zealand, the Project is aimed at understanding the ecology of Nigeria’s montane forest fragments for informed management of this fragile ecosystem. The research focus is predominantly plant-animal mutualisms and forest restoration. This talk will introduce the NMFP and present research aimed at understanding how seed dispersal processes are changing in response to forest fragmentation and hunting.
 
Hazel Chapman is an Associate Professor at the University of Canterbury (UC) NZ, where she lectures in evolutionary ecology. Hazel’s research focus is tropical forest conservation and she is the Founder and Director of the NMFP. Since 2004, the Project has seen a stream of international and Nigerian postgraduate students enrolled at UC doing their field research in Nigeria. In addition the NMFP trains undergraduate Nigerian students in conservation biology, and works with local schools and the community. The Project is run almost entirely by the local community. It is home to a 20ha Smithsonian CTFS Forest Geo Plot.
 
All welcome.

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Insect pollinators boost the market price of holly and mistletoe: a new study just published

Holly and mistletoe 20161211_103252.png

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)

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Filed under Bees, Biodiversity, Biodiversity and culture, Ecosystem services, Hedgerows, Mutualism, Pollination, University of Northampton

Managing for Pollinators – a special issue of the Natural Areas Journal

Inula at Ravensthorpe 20160710_145426The 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 Full Access

Introduction by USFS Chief Tidwell – Pollinators and Pollination open access

pg(s) 361–361

Citation : Full Text : PDF (227 KB)

National Seed Strategy: Restoring Pollinator Habitat Begins with the Right Seed in the Right Place at the Right Time Full Access

Peggy Olwell and Lindsey Riibe
pg(s) 363–365

Citation : Full Text : PDF (1479 KB)

Hummingbird Conservation in Mexico: The Natural Protected Areas System Full Access

M.C. Arizmendi, H. Berlanga, C. Rodríguez-Flores, V. Vargas-Canales, L. Montes-Leyva and R. Lira
pg(s) 366–376

Abstract & References : Full Text : PDF (1302 KB)

Floral Guilds of Bees in Sagebrush Steppe: Comparing Bee Usage of Wildflowers Available for Postfire Restoration Full Access

James H. Cane and Byron Love
pg(s) 377–391

Abstract & References : Full Text : PDF (1500 KB)

The Role of Floral Density in Determining Bee Foraging Behavior: A Natural Experiment Full Access

Bethanne Bruninga-Socolar, Elizabeth E. Crone and Rachael Winfree
pg(s) 392–399

Abstract & References : Full Text : PDF (1219 KB)

Common Methods for Tallgrass Prairie Restoration and Their Potential Effects on Bee Diversity Full Access

Alexandra Harmon-Threatt and Kristen Chin
pg(s) 400–411

Abstract & References : Full Text : PDF (300 KB)

Status, Threats and Conservation Recommendations for Wild Bumble Bees (Bombus spp.) in Ontario, Canada: A Review for Policymakers and Practitioners Full Access

Sheila R. Colla
pg(s) 412–426

Abstract & References : Full Text : PDF (420 KB)

Conserving Pollinators in North American Forests: A Review Full Access

James L. Hanula, Michael D. Ulyshen and Scott Horn
pg(s) 427–439

Abstract & References : Full Text : PDF (1711 KB)

Dispersal Limitation, Climate Change, and Practical Tools for Butterfly Conservation in Intensively Used Landscapes Full Access

Laura E. Coristine, Peter Soroye, Rosana Nobre Soares, Cassandra Robillard and Jeremy T. Kerr
pg(s) 440–452

Abstract & References : Full Text : PDF (4647 KB) : Supplementary Materials

Revised State Wildlife Action Plans Offer New Opportunities for Pollinator Conservation in the USA Full Access

Jonathan R. Mawdsley and Mark Humpert
pg(s) 453–457

Abstract & References : Full Text : PDF (249 KB)

Diet Overlap of Mammalian Herbivores and Native Bees: Implications for Managing Co-occurring Grazers and Pollinators Full Access

Sandra J. DeBano, Samantha M. Roof, Mary M. Rowland and Lauren A. Smith
pg(s) 458–477

Abstract & References : Full Text : PDF (1537 KB)

The Role of Honey Bees as Pollinators in Natural Areas Full Access

Clare E. Aslan, Christina T. Liang, Ben Galindo, Hill Kimberly and Walter Topete
pg(s) 478–488

Abstract & References : Full Text : PDF (467 KB)

Food Chain Restoration for Pollinators: Regional Habitat Recovery Strategies Involving Protected Areas of the Southwest Full Access

Steve Buckley and Gary Paul Nabhan
pg(s) 489–497

Abstract & References : Full Text : PDF (732 KB)

Forbs: Foundation for Restoration of Monarch Butterflies, other Pollinators, and Greater Sage-Grouse in the Western United States Full Access

R. Kasten Dumroese, Tara Luna, Jeremiah R. Pinto and Thomas D. Landis
pg(s) 499–511

Abstract & References : Full Text : PDF (1716 KB)

Using Pollinator Seed Mixes in Landscape Restoration Boosts Bee Visitation and Reproduction in the Rare Local Endemic Santa Susana Tarweed,Deinandra minthornii Full Access

Mary B. Galea, Victoria Wojcik and Christopher Dunn
pg(s) 512–522

Abstract & References : Full Text : PDF (2880 KB)

Save Our Bats, Save Our Tequila: Industry and Science Join Forces to Help Bats and Agaves Full Access

Roberto-Emiliano Trejo-Salazar, Luis E. Eguiarte, David Suro-Piñera and Rodrigo A. Medellin
pg(s) 523–530

Abstract & References : Full Text : PDF (463 KB)

The Importance of Phenological Diversity in Seed Mixes for Pollinator Restoration Full Access

Kayri Havens and Pati Vitt
pg(s) 531–537

Abstract & References : Full Text : PDF (2208 KB) : Supplementary Materials

Stewardship in Action Full Access

Sarah Riehl
pg(s) 538–541

Citation : Full Text : PDF (595 KB)

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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)

Watts et al Figure 1

The second paper from the PhD thesis of my former student Dr Stella Watts has just been published in Annals of Botanyhere’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.

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