The Beetles and the Bees: Interactions Between Herbivores and Pollinators

Check out our newly published article in the open access journal PeerJ: A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination.

Figure 2: Mechanisms of damage by herbivores that can impact pollination and therefore seed set.
Solid lines represent direct interactions and dotted lines indirect interactions. The two main pathways are direct (direct damage to floral tissue influences pollinators; shown lighter in orange) and indirect (damage to vegetative tissue indirectly effects floral traits; shown darker in blue). Lines and boxes in black represent interactions and steps shared by both pathways. The dotted lines represent the net indirect interaction of plant damage on pollinators (and pollination) that was the focus of this review.

Any gardener knows the havoc that herbivores can have on their plants; whether it’s the rabbits eating their cabbage or beetles damaging their prized roses. Herbivores can devastate a floral display or chew away at the leaves until a plant is too sickly to produce flowers or fruit. However, a discerning gardener will know that not all insects are bad for their vegetable garden; rather they should hope for some bees if they expect to see a good yield of tomatoes or strawberries. Both herbivores and pollinators can influence the yield of fruits and seeds for many plants worldwide and therefore impact both crop yields and plant reproduction. The effects of both types of interactions have been repeatedly tested by the scientific community; however, by their nature, these types of studies must simplify things in order to isolate the specific effect of one species on another and therefore neglect the multitude of other species present that might change this interaction. A caterpillar may chew the petal of a flower that a bee then passes over because the flower is no longer perfect or a rabbit may eat the leaves of a plant that, in consequence, only produces one small flower that is easily overlooked. Bees and other pollinators make choices when they choose flowers to visit, and damage to the plant (whether the flower or not) can result in flowers that are less attractive to pollinators. Similarly, the part of the plant attacked (i.e. leaves, roots, stem, or flowers) should certainly impact this choice differently. Damaging flowers directly reduces the appeal of the flower, and removing it entirely certainly eliminates the possibility of pollination; but how does damage to the leaves, roots and stem change the flowers? Damage to these parts can reduce the overall quality of a flower, whether the flower is smaller or produces less nectar, or if there are simply fewer flowers overall.

This dance between herbivores and pollinators is the subject of the review we recently published in the journal PeerJ: “A systematic review of the direct and indirect effects of herbivory on plant reproduction mediated by pollination.” We collected peer-reviewed studies that examined the effects of herbivores and pollinators on plant reproduction. One of our conclusions is evident simply by the number of studies we found; out of a total of 4,304 studies that turned up in a search on the search engine Web of Science, only 59 studies fit our criteria. That is, not many studies look at both herbivores and pollination. Half of these studies looked at damage to flowers and only about a third looked at damage to any of leaves, roots, and stems (the remainder looked at general damage to any tissue). When tightening our criteria to studies that compare damage to flowers and other parts of the plant, we only found three studies. In our paper we discuss in depth the ways herbivores and pollinators interact can call for more studies to compare damage to both flowers (direct damage) and other parts of plants (indirect damage).

Reflections

While Chris (my co-author) has completed and published many systematic reviews, this was my first. Gathering and sifting through this much data was certainly an experience and quite the grind. However, I have learned many lessons from this process, both about systematic reviews in general and about handling data. One lesson is to make sure to well-document everything in your process, because you will end up going back to look, months or even years later. So, document it, organize it, and if you can, automate it! However, the most important lesson I learned was the importance of a clear question and idea in advance. By the time I had collected all my data and knew the studies well, I felt as though I had lost the entire point of the review. I didn’t have a clue what to do next. It took going back to my original notes and having a discussion with Chris to remember why we had started off on this journey to begin with and to identify what questions we were trying to answer.

Overall, this systematic review gave me an excellent insight into the review process, both what to do and what not to do. However, the content itself provided a firm basis for my own practical field research. I have been in the process of implementing some of my own experiments contrasting the effects of damage to different plant tissues both in the field and in the greenhouse.

Do native shrubs facilitate exotic species equally??

I just returned from some exciting desert fieldwork! Last year, I sampled the annual plant community under shrubs and in the open at six sites across the Mojave and San Joaquin Deserts, and here’s the gist of what I found:

RII values (negative values indicate negative associations with native shrubs; positive values indicate positive associations) for nine vegetation measures taken at six study sites across the Mojave (Mesquite, Mojave, and Vegas) and San Joaquin (Panoche, Cuyama, Carrizo) Deserts. Panels are arranged in ascending order of relative aridity. Data currently in review at Diversity and Distributions.

Spatial association with native foundation shrubs strongly and consistently increased the abundance, biomass, cover, and fitness of the dominant invader Bromus rubens but not the native annual community. This is interesting because positive interactions mediated by native species are seldom invoked to explain the success of exotic invaders. Very cool, but what about the system’s many other exotic, invasive species? Is facilitated invasion species-specific?

To tackle this question, I returned to the desert and sampled the annual plant community at nine study sites scattered across the Mojave and San Joaquin Deserts. Six are repeats from last year, three (Yuc, Cna, Hea) are new:

The three leftmost sites are in the San Joaquin Desert. The six rightmost sites are in the Mojave Desert.

At each site, I sampled the annual plant community at 20 pairs of shrub and open microsites with a 0.5m x 0.5m quadrat. Shrub microsites were the area immediately beneath the canopies of foundation shrubs, and open microsites were areas >1m from any shrub canopy. In each microsite, I estimated the abundance of the native annual community as a whole and the exotic annual community as a whole. I collected species-specific measurements for the abundance, biomass, and fitness of the following exotic plant species: Bromus rubens, B. tectorum, B. diandrus, Erodium cicutarium, Schismus spp., and Brassica tournefortii. Each of these exotic invaders can contribute to biodiversity loss and diminished ecosystem function.

Strong facilitation of Bromus rubens near Las Vegas, NV. Bummer, but cool.

We’ll have to wait for the official stats, but it seemed that B. rubens, B. tectorum, and B. diandrus formed strong and consistent positive associations with native shrubs. Each of the other exotic species ( E. cicutarium, Schismus spp., and B. tournefortii ) associated with native shrubs more sporadically. The most interesting observation was this: it seemed that B. rubens controlled the game — when it was super abundant under shrubs, nothing else (except other bromes) strongly associated with shrubs. When it was less abundant, other exotic (and sometimes native!) species apparently associated with shrubs more strongly. This suggests a competitive hierarchy in which exotic bromes, and especially B. rubens, rule the understory, followed by other exotic species, followed by native species. Again, the stats will give us the official story, but I think that’s what I saw! Very cool.

More cool stuff:

There was a crazy flash flood on Tues, April 14. This is the road I was driving on!
That’s 1/2″ of hail. Did it hurt? Hail yes (sorry).
Sunday, April 12 was a glorious morning! Cholla and Fouquieria near Turtle Mountain, NV. Did I mention glorious?

We Want a Shrubbery! The direct and indirect influence of Shrubs on Flowering Annual plants in an Arid Ecosystem

A progress report by Stephanie Haas

Shrubs frequently have positive interactions with annuals in desert ecosystems. This facilitative effect has been seen repeatedly with plant density, but the effect of shrubs on flowering is less studied. Shrubs also impact other species that interact with annuals, including both herbivores and pollinators. These direct and indirect interactions exist in a complex network that we attempt to tease apart through both manipulation and observation.

To see the slide deck click here.

To see the presentation click here.

Climatic scaling effects of foundation plant species interactions with vertebrate species.

Positive interactions are key to many systems worldwide. Foundation species such as shrubs are able to benefit other taxa through various mechanistic pathways. The canopy of these species is also an structural agent, able to reduce light intensity and temperature variation experienced by vertebrates. But, do the instances of animal near a shrub increase as temperature and light intensity increase? Can artificial shelters be as good as shrubs when comes to lowering the variation in the above parameters? Disturbances such as land use and climate change are the current reality of many regions. To be able to artificially restore these systems post-disturbance while new vegetation is grown is thus key.

Click here to find out more!

Panoche Hills, California
(Chateaugrief, 2019)

Shrub-animal density dependence in desert ecosystems

By: Mario Zuliani

Positive interactions between plant and animal species have been reported in most ecosystems globally. Most literature that looks at these interactions, particularly in arid ecosystems, reports the facilitative interactions occurring between shrub and animal species. With these types of interactions being present, one begs to question; does the density of these foundational shrub species have a relationship with the animal abundance present near them? That being said, understanding this relationship could potentially be used for remediation efforts, for many of the animal species using these shrubs.

For access to my March 2020 Progress report presentation click here

For access to the slide show click here

An examination of interactions between bird and foundation plants in an arid ecosystem.

Malory Owen’s Second-year Masters Progress report

March 19th, 2020

Malory Owen & Christopher Lortie

Wilson’s Warbler (Cardellina pusilla) in Creosote Bush (Larrea tridentata)

Positive interactions between plants and animals create habitat infrastructure on which many species rely, especially when the promotion of foundation species is involved. Mutualistic interactions between plants and birds (like pollination or seed dispersal) are dependent on both plant and bird phenology or cyclic/seasonal changes. However, phenology is plastic as photoperiod and temperature largely determine flowering & fruiting for plants and migration & breeding for birds. As our climate changes and habitats degrade, we must understand what interactions are at risk. That’s why, in this study, we examined the relationships between birds, their community, their behavior, and their microhabitat associations.

Follow this link to view my progress report presentation for March 2020, or follow this link to view the slide deck of the presentation.

Annual plant neighbourhoods

As a team, we are discussing the fine-scale grain of sampling for estimating annual-annual plant interactions in deserts. We are particularly interested in the Mojave Desert to examine pollinator-herbivore interactions with annuals that are mediated by the other immediately adjacent congeneric species. Here is a brief compilation of key papers examining this challenge.

scale matters, a plant’s eye view

Publications describing the fine-scale annual plant neighbourhood concept

Mack, R. N. and Harper, J. L. 1977. Interference in dune annuals: spatial pattern and neighbourhood effects. – Journal of Ecology 65: 345-363.

Holzapfel, C. and Mahall, B. E. 1999. Bidirectional facilitation and interference between shrubs and annuals in the Mojave desert. – Ecology 80: 1747-1761.

Schiffers, K. and Tielbörger, K. 2006. Ontogenetic Shifts in Interactions among Annual Plants. – Journal of Ecology 94: 336-341.

Lortie, C. J. and Turkington, R. 2008. Species-specific positive effects in an annual plant community. – Oikos 117: 1511-1521.

Emery, N. C., Stanton, M. L. and Rice, K. J. 2009. Factors driving distribution limits in an annual plant community. – New Phytologist 181: 734-747.

Luzuriaga, A. L., Sánchez, A. M., Maestre, F. T. and Escudero, A. 2012. Assemblage of a Semi-Arid Annual Plant Community: Abiotic and Biotic Filters Act Hierarchically. – PLOS ONE 7: e41270.

Underwood, N., Inouye, B. D. and Hambäck, P. A. 2014. A Conceptual Framework for Associational Effects: When Do Neighbors Matter and How Would We Know? – The Quarterly Review of Biology 89: 1-19.

Underwood, N., Hambäck, P. A. and Inouye, B. D. 2020. Pollinators, Herbivores, and Plant Neighborhood Effects. – The Quarterly Review of Biology 95: 37-57.

Personal vote

I am a fan of the 15cm scale for fine-scale but often sample with a 15cm ring nested within a second 30cm metal ring. I construct using wire.

Jacob’s schedule — let’s be friends!

Here’s my [approximate] travel schedule for this summer. It’d be great to connect any time we happen to be in the same place at the same time!

  • April 6-20: Veg sampling and experimental site selection in Cali/Nevada
  • May 20(ish): B. rubens seed collection in Cali/Nevada
  • May 25-June 2: E. lobata sampling in Toronto
  • August 2-7: ESA in Salt Lake
  • Sept 16-21: E. lobata sampling in Toronto
  • Sept. 25-Oct. 11: Install facilitation x granivory experiment in Cali/Nevada.

Biotic interactions in the native and non-native ranges of invasive Bromus rubens

One of the most powerful approaches for understanding biological invasions by non-native species is to examine ecological patterns and processes in both the native and non-native ranges of invasive species. Here’s a great article on the subject:

https://doi.org/10.1111/j.0022-0477.2004.00953.x

The number of articles published on biological invasions has increased exponentially over the last 20 years, but biogeographically explicit studies replicated in the native and non-native ranges of invasive species are still VERY rare. This hampers our mechanistic understanding of the invasion process and therefore our ability to explain, predict, and manage biological invasions.

Bromus rubens (i.e., red brome) invasion in the Mojave Desert provides a great opportunity to address this knowledge gap. We are planning to examine the individual and joint effects of shrub facilitation and post-dispersal seed predation on the abundance of B. rubens in its native (Israel) and non-native (California and Nevada) ranges. This experiment is broadly interesting because it allows us to test the relative importance of the effects of two fundamental biotic interactions on two continents. Here’s a cartoon of our experimental design:

Solid circles represent functional exclosures that effectively exclude seed predators; dashed circles represent non-functional exclosures that admit seed predators. Note the control treatment that monitors recruitment from seed banks. This is a full-factorial design that crosses shrub facilitation (open vs. shrub microsites) with seed predation (functional vs. non-functional exclosures). Pretty cool.

We will replicate this setup at 5 shrub-open pairs per site at 6 sites across the Mojave (GPS coordinates are preliminary):

Sitelatlong
Veg36.44603-114.96
Mes36.75986-114.07
Bak35.40529-115.797
HOM34.71012-115.689
Need34.49663-114.733
Palm34.16122-115.714

We will replicate the experiment at 5 sites in the Negev Desert of Israel with the help of Dr. Merav Seifan of the Ben Gurion University of the Negev. She rocks! Site locations and GPS coordinates in Israel are forthcoming.

The biogeographic contrast of the effects of seed predation can be considered a test of the enemy release hypothesis, which has only been examined once in the context of seed predation:

https://doi.org/10.1002/ece3.5314

However, the biogeographic contrast of the effects of shrub facilitation is COMPLETELY NOVEL…I think 🙂

We begin work this spring! We’ll keep you posted.