Beautiful buds beset bumblebees with bad bugs

Sexual liaisons can be difficult to achieve without some type of purposeful motion.  Flowering plants, which are rooted to the ground, are particularly challenged to bring the male close enough to the female to have sex.  One awesome adaptation is pollen, technically the male gametophyte –  or gamete (sperm)-generating plant. These tiny males get to females either by floating through the air, or by being transferred by animal pollinators such as bees. Plants can lure bees to their flowers by producing nectar – a sugar rich fluid – which bees lap up and use as a carbohydrate source.  While nectaring, bees also collect pollen, either intentionally or inadvertently, which provides them with essential proteins. When bees travel to the next flower, they may inadvertently drop some of their pollen load near the female gametophyte – in this case a tiny egg-generating plant (though tiny, the female gametophyte is considerably larger than is the male gametophyte).  We call this process of “tiny boy meets tiny girl” pollination. Once the two gametophytes meet, the pollen produces one or more sperm, which it uses to fertilize an egg within the female gametophyte.  There is more to it, but this will hopefully clarify the difference between pollination and fertilization.

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Bumblebee forages on beebalm, Monarda didyma. Credit: Jonathan Giacomini.

All of this business takes place within the friendly confines of the flower.  The same flower may be visited by many different bees of many different species. While feeding, bees carry on other bodily functions, including defecation.  They are not careful about where they defecate; consequently a bee’s breakfast might also include feces from a previous bee visitor. Bumblebee (Bombus impatiens) feces carries many disease organisms, including the gut parasite Crithidia bombi, which can reduce learning, decrease colony reproduction and impair a queen’s ability to found new colonies. Because pollinators are so critical in ecosystems, Lynn Adler and her colleagues wondered whether certain types of flowers were better vectors for harboring and transmitting Crithidia bombi to other bumblebees.

Antirrhinummajus

Bumblebee forages on the snapdragon, Antirrhinum majus. Credit: Jonathan Giacomini.

The researchers chose 14 different flowering plant species, allowing uninfected bumblebees to forage on inflorescences (clusters of flowers) inoculated with a measured amount of Crithidia bombi parasites.  The bees were reared for seven days after exposure, and then were assessed for whether they had picked up the infection from their foraging experience, and if so, how intense the infection was. The researchers dissected each tested bee and counted the number of Crithidia cells within the gut.

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Researcher conducts foraging trial with Lobelia siphilitica inflorescence. Credit: Jonathan Giacomini.

Adler and her colleagues discovered that some plant species caused a much higher pathogen count (mean number of infected cells in the bee gut) than did other plant species.  For example bees that foraged on Asclepias incarnata (ASC) had four times as many pathogens, on average, than did bees that foraged on Digitalis purpurea (DIG) (top graph below). Bees foraging on Asclepias were much more likely to get infected (had greater susceptibility) than bees that foraged on several other species, most notably Linaria vulgaris (LIN) and Eupatorium perfoliatum (EUP) (middle graph). Lastly, if we limit our consideration to infected bees, the mean intensity of the infection was much greater for bees foraging on some species, such as Asclepias and Monarda didyma (MON) than on others, such as Digitalis and Antirrhinum majus (ANT) (bottom graph).

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(Top graph) Mean number of Crithidia (2 microliter gut sample) hosted by bees after foraging on one of 14 different flowering plant species. This graph includes both infected and uninfected bees. (Middle graph) Susceptibility – the proportion of bees infected – after foraging trials on different plant species. (Bottom graph) Intensity of infection – Mean number of Crithidia for infected bees only. The capital letters below the graph are the first three letters of the plant genus. Numbers in bars are sample size.  Error bars indicate 1 standard error.

It would be impossible to repeat this experiment on the 369,000 known species of flowering plants (with many more still to be identified).  So Adler and her colleagues really wanted to know whether there were some flower characteristics or traits associated with plant species that served as the best vectors of disease.  The researchers measured and counted variables associated with the flowers, such as the size and shape of the corolla, the number of open flowers and the number of reproductive structures (flowers, flower buds and fruits) per inflorescence.

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Flower traits measured by Adler and colleagues (example for blue lobelia, Lobelia siphilitica). CL is corolla length. CW is corolla width. PL is petal length. PW is petal width. Credit: Melissa Ha.

The researchers also wanted to know whether any variables associated with the bees, such as bee size and bee behavior, would predict how likely it was that a bee would get infected.  Surprisingly, the number of reproductive structures per inflorescence stood out as the most important variable. In addition, smaller bees were somewhat more likely to get infected than larger bees, and bees that foraged for a longer time period were more prone to infection.

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Mean susceptibility of bees to Crithidia infection after foraging on 14 different flowering plant species, in relation to the number of reproductive structures (flowers, buds and fruits) per inflorescence.

These findings are both surprising and exciting. Adler and her colleagues were surprised to find such big differences in the ability of plant species to transmit disease.  In addition, they were puzzled about the importance of number of reproductive structures per inflorescence.  At this point, they don’t have a favorite hypothesis for its overriding importance, speculating that some unmeasured aspect of floral architecture influencing disease transmission might be related to the number of reproductive structures per inflorescence.

Penstemondigitalis

Bumblebee forages on Penstemon digitalis. In addition to the open flowers, note the large number of unopened buds.  Each of these counted as a reproductive structure for the graph above. Credit: Jonathan Giacomini.

The world is losing pollinators at a rapid rate, and there are concerns that if present trends continue, there may not be enough pollinators to pollinate flowers of some of our most important food crops. Disease is implicated in many of these declines, so it behooves us to understand how plants can serve as vectors of diseases that affect pollinators. Identifying floral traits that influence disease transmission could guide the creation of pollinator-friendly habitats within plant communities, and help to maintain diverse pollinator communities within the world’s ecosystems.

note: the paper that describes this research is from the journal Ecology. The reference is Adler, L. S., Michaud, K. M., Ellner, S. P., McArt, S. H., Stevenson, P. C. and Irwin, R. E. (2018), Disease where you dine: plant species and floral traits associated with pathogen transmission in bumble bees. Ecology, 99: 2535-2545. doi:10.1002/ecy.2503. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.