Herbivore Chewing Vibrations Induce Plant Defenses

by Kaya Wurtzel (Bowdoin ‘21)

In order to defend themselves from herbivory, plants must be able to detect local herbivores. Herbivory cues can include mechanical damage, chemicals from insect saliva or eggs, and even feeding vibrations. Previous studies demonstrated that Arabadopsis thaliana upregulated defensive chemicals in response to Pieris rapae larvae feeding but not wind or vibrations caused by leafhoppers. In a recently published paper in the journal Oecologia, researchers at the University of Missouri demonstrated that the vibrations patterns from larval feeding induced increases in defensive chemicals in A. thaliana across multiple species. A. thaliana responded with a uniform chemical defense response to larval chewing vibrations between individuals within a species and across the species studied.

Illustration by Kaya Wurtzel (Bowdoin ‘21)

Can bumblebees stimulate flower production by damaging leaves?

Guest Contributor

Kaya Wurtzel

Bowdoin ‘21

Before I talk about this week’s paper, I want to acknowledge that Breonna Taylor would have celebrated her 27th birthday today. Instead, we’re still waiting on the arrests of police officers who shot her, after entering the wrong house in the middle of the night. Breonna was a daughter, a friend, and a first responder—her life mattered, and she should still be here. Breonna’s murder is just one of the recent incidents of police brutality driving Black Lives Matter protests across the country and world. Systemic racism and white supremacy are not just present in our police force--they also permeate just about every part of our society, including Ecology, Biology, and Bowdoin. Black folks are underrepresented in our field, and we have work to do, unpacking white supremacy, to make our communities safe to heal, learn and grow for everyone. This is a long-term process, but, for today, I’ll start by sharing this collection of podcasts, featuring storytelling by Black scientists. Black stories matter, black scientists matter, and black lives matter.

Can bumblebees stimulate flower production by damaging leaves?

 Each spring, bumblebees establish new colonies and have an increased demand for floral resources. Pollen availability during this period can have long term implications for the health of the colony. Under changing environmental conditions, bees may begin establishing new colonies earlier in the spring, when floral resources are still scarce. A recent paper published in Science based on work in the De Moraes Lab, at the Swiss Federal Institute of Technology, suggests that bumblebees may be able to accelerate local flower production by damaging leaves of flowerless plants.

After observing Bombus terrestris damaging plant leaves without feeding on or collecting any leaf material, Pashadilou et al. hypothesized that leaf-damaging behavior could induce flower production. Previous work has shown that abiotic stressors can induce flowering but little is known about the effects of biotic stressors, like insect leaf damage.

 To test whether B. terrestris leaf damaging behavior induced flowering, researchers exposed flowerless tomato and black mustard plants to pollen deprived B. terrestris colonies. They allowed worker bees to make 5-10 leaf holes and then removed the plants. Each bee damaged plant was paired with a mechanically damaged plant, where researched tried to precisely copy bee leaf damage using forceps and a razor. They found that bee-damaged tomatoes flowered an average of 30 days earlier than undamaged plants and 25 days earlier than mechanically damaged pants. Bee-damaged black mustard plants flowered an average of 16 days earlier than undamaged plants and 8 days earlier than mechanically damaged plants. The results of this first experiment indicate that B. terrestris leaf-damaging behavior induces earlier flowering but do not establish the mechanism at work.

Illustration by Kaya Wurtzel

In a series of following experiments, Pashadilou et al. evaluate the influence of pollen availability on leaf-damaging behavior. Laboratory experiments found that rates of leaf-damaging behavior were significantly higher for bees under pollen limitations. Subsequent rooftop studies found that the frequency of damaging behavior declined as local flower resources increased in the spring. When the rooftop study was repeated with the addition of a path of flowers adjacent to the hive, the frequency of damaging behavior decreased. In a final rooftop study in 2019, Pashadilou et al. compared two rooftops: one where B. terrestris hives had access to a patch of flowerless plants and another where hives had access to a garden of wildflowers and a patch of flowering plants, adjacent to the patch of flowerless plants. Bees damaged plants in both flowerless patches but at higher rates on the rooftop without nearby floral resources. When they mowed the flower gardens on the second roof, bee damage rates on the flowerless patch increased significantly. Over the course of the rooftop experiments, researchers also observed wild B. lapidarius and B. lucorum damaging flowerless plants. These rooftop studies demonstrated that local pollen availability influences leaf damaging behavior, even when bumblebees have the option to forage farther away.

Altogether, the results of this study suggest that multiple species of bumblebees, including B. terrestris, B. lapidarius and B. lucorum, use leaf-damaging behaviors to accelerate local flower production, especially when floral resources are scarce. In the face of environmental change threatening our pollinators, these findings highlight the potential for adaptation and resiliency of plant-pollinator interactions.

Kaya Wurtzel

Bowdoin ‘21

Jones Lab Student Researcher

Dramatic Worldwide Declines in Insects

Figure 4 from Lister & Garcia 2018 PNAS 115 (44) E10397-E10406 comparing the biomass of insects captured in ground and canopy traps at the same sites in Puerto Rico 45 years apart.

This week’s paper is on a topic so upsetting that I have been avoiding writing about it. Dave Goulson has published an essay this week in Current Biology entitled “The insect apocalypse, and why it matters”. Goulson is a Professor at the University of Sussex in England who researches bumblebee ecology, and whose popular science books “A Sting in the Tale” and “A Buzz in the Meadow” are wonderful reads that I highly recommend. In his essay this week Goulson reviews the literature on widespread declines in insects. In the 2000’s people anecdotally began noting that car windshields needed to be cleaned of dead insects much less often than they used to. These anecdotes have become known as the “windshield phenomenon” and have sparked interest in finding real data on insect numbers to determine what types of declines may be occurring. The problem is, that unlike birds or mammals, there are not a lot of long-term study systems set up to monitor insect populations across decades. In 2017, data from one of these few long-term study systems was published. It showed that numbers of insects collected in traps in 63 protected areas in Germany had declined 75% from 1989 - 2016. 75%!! That is a lot. Another study last year by Lister & Garcia (see above figure) showed even more dramatic declines in the rainforests of Puerto Rico, of between 75 and 98% depending on the type of sampling. The study from Puerto Rico showed associated declines in the birds, lizards, and frogs that eat insects. As Goulson covers in his review, it is most likely a combination of factors driving these declines, including pesticide usage, climate change, habitat loss, and the introduction of insect diseases and parasites. It should not be a surprise to anyone that the widespread use of pesticides is causing widespread insect declines, that has been, after all, the goal. But it must be noted that the declines are happening beyond agricultural areas where pesticides are being applied, such as the Puerto Rican rainforests in Lister & Garcia (2018). Lister & Garcia (2018) attribute the declines at their study sites to the 2 degree celsius increase in temperature that has occurred over the study period due to human fossil fuel usage worldwide.

These insect declines are terrifying. Insects are the food for most non-human animals on the planet. The animals that don’t eat insects eat other animals (which eat insects) or they eat plants. But insects are required to pollinate 87% of all plants and 75% of our crops. In addition, insects are critical to decomposition. They break down the food waste, the leaf litter, the dead animals, and lots and lots and lots of poop. I have a little baby, and my concerns are not only about the ecological collapse that we are likely to see in his lifetime due to climate change and these insect declines, but that he will not have the joys of watching wild animals in nature that I have had. To quote Goulson:

“Is this the future we would wish for our children, one in which they will never see a monarch butterfly flying overhead, where there are no wildflowers, and where the sound of birdsong and the buzz of insects is replaced by the monotonous drone of robot pollinators? They may be free from malaria, but they will have paid a high price. Once again I am valuing nature for what it does for us humans. There is one final argument, an unselfish one at last. Do not the rest of the organisms on our planet have as much right to be here as we do?”

So what can you do?

1. Get rid of your lawn! In a recent interview May Berenbaum from the University of Illinois suggested this as one of the first things you can do (plus its easy! you actually have to do less). Stop mowing and raking. Let the weeds grow up. Mowing once a year in early October or so will keep the trees down and maintain flowering plant habitat for pollinators and the leaf-litter creates important habitat for insects in your yard.

2. Stop using pesticides, especially ones that include the active ingredients Clothianidin, Imidacloprid, Thiacloprid and Thiamethoxam. These are neonicitinoid pesticides that extensive research has shown have detrimental effects on bees. Many of them are banned in Europe but still legal in the US.

3. Plant native plants. If the thought of an overgrown yard is filling you with anxiety, think instead (or as well) about intentionally planting beneficial plants. The Xerces Society has native plant lists for plants that benefit pollinators suited to your particular region (for example here is the one for my area in Maine). Xerces has worked with Ernst Seeds to create mixes for your region.

Can diet affect bumblebees’ recovery from infections?

Guest Contributor

Ayana Harscoet

Bowdoin ‘21

Bumblebee on sunflower. Photo by Ronda Ryan

When you’re a bumblebee, there’s no CVS-type-one-stop-shop to take care of all your pathogen-related issues. But fortunately for these pollinators, certain food sources have the potential to mitigate infections. This week’s paper, published in Ecological Entomology and led by George Locascio, a professor at UMass Amherst, finds that consuming sunflower pollen can effectively reduce infections of a bumblebee gut pathogen, Crithida bombi, in the bumblebee Bombus impatiens.

Understanding disease dynamics can help us figure out how to combat certain stressors contributing to species decline in pollinators, a necessary endeavor given the crucial role that these organisms play in global ecosystems and food systems. Locascio et al. conducted two experiments to investigate the relationship between sunflower pollen and pathogen transmission, hoping to get at the effects of specific factors like duration and timing of pollen exposure.

In their first experiment, which they refer to as “exposure during foraging,” the authors wanted to see whether sunflower pollen affected the transmission of C. bombi. Would bees be at higher risk of infection if they visited inoculated flowers without pollen versus flowers with pollen? As it turns out, the presence of sunflower pollen had no effect on the pathogen at this point in the infection process—bees were similarly infected regardless of whether they visited flowers with or without pollen.

The second experiment focused on post-infection—could a bumblebee recover from infection with the right diet? Yes! But sunflower pollen isn’t an immediate cure: bumblebees recovered much better when they were consistently consuming sunflower pollen for 7 days after infection than for just 3.5 days. And timing also mattered—if they started consuming sunflower pollen 3.5 days after infection as opposed to immediately after, the pollen didn’t combat the infection as effectively. That said, bumblebees consuming sunflower pollen for 7 days beginning a week after infection still had relatively good recovery rates. So, as Locascio et al. conclude, the effectiveness of sunflower pollen is dependent on both how soon a bumblebee consumes it after infection, coupled with the amount or duration of consumption. For best results, a bumblebee would consistently consume sunflower pollen for at least a week immediately after infection.

That said, sunflower pollen is no nutritious food source for bumblebees—it lacks sufficient amino acid richness and has even been suggested to reduce bee development and growth. Much like we wouldn’t last long on a diet of prescription meds, it’s important for bees to consume pollen from a variety of flowers to receive both adequate nutrition and pathogen defenses.

Ayana Harscoet

Bowdoin ‘21

Doris Duke Conservation Scholar

Jones Lab Student Researcher

Foraging areas of Leach's storm petrels

Petrel burrow on Kent Island, photo by Fred Field

New paper out with data from Kent Island! April Hedd from Environment and Climate Change Canada has published a paper this week in PLOS One. In 2013 and 2014 Dr. Hedd and her team put global location sensors (GLS) on petrels from 7 breeding sites in the Canadian Maritimes including Kent Island. In total, they obtained data from 133 petrels. From Kent Island, 17 petrels produced data (out of 20 tagged) in 2013 and 15 (out of 20 again) in 2014. On average, petrels made 4 day foraging trips which were 400 to over 800 km away from their burrows. Most of the petrels headed out to forage in deep oceanic shelves off the coast. The Kent Island petrels were different, foraging mostly over shallow water closer to shore. As you can see in the map below, they cover the entire Gulf of Maine and Georges Bank! Kent Island birds tended to have longer foraging trips than birds from other sites, but they covered smaller areas. Their foraging ranges overlapped by over 60% across years. Kent Island falls in the southernmost part of the range of storm petrels, and their different foraging behavior is likely to be influenced by their geographic location. It's wonderful to think about the birds we see on Kent Island having foraged off of Cape Cod a few days before!

Figure 2 from Hedd et al. 2018.

Swallow populations across the decades

Swallow boxes on Kent Island. Photo by John Lichter.

New paper lead by graduate student Tara Imlay from the University of Dalhousie in Nova Scotia (and including Professor Nat Wheelwright from Bowdoin and Professor Marty Leonard from Dalhousie) is out in Ecosphere. Imlay and her colleagues are searching for explanations for the dramatic declines that occurred in many swallow populations in the 1980's. They therefore examined breeding success and whether it was related to phenology or climate change for bank, barn, cliff, and tree swallows in datasets (including Kent Island!) that spanned 57 years. Surprisingly, given the declines in swallows, only bank swallows showed consistent declines in breeding success over the decades. In addition Bank swallows were the only species that did not advance their egg laying timing earlier across decades, all other species are laying eggs 8-10 days earlier than they were in the 1960's. This research indicates that for three of these four swallows, population declines do not seem to be driven by declines in breeding success. This highlights the need to examine factors that may be causing bird mortalities during migration or over the winter season. We only had one breeding pair of tree swallows on Kent Island last summer, but the boxes are up and will continued to be monitored. 

Mason Bees and Bee Hotels

One of our native mason bee species, Osmia lignaria, the blue orchard bee. Photo by Brian Buckner

I have been asked a lot of questions the past couple of weeks about mason bees, and specifically mason bee hotels that you can put up in your yard. This coincides with an article about mason bees in Scientific American about the attempts of the almond industry to start commercially producing (and pollinating with) mason bees. The colony collapse disorder in honeybees has hit almond farmers particularly hard. This has led the industry to search for alternative pollinators, and the blue orchard bee, Osmia lignaria, emerged as a likely candidate. Mason bee is a general term usually referring to bees in the genus Osmia which use mud and clay in building their nests (thus the "mason" reference). Here in Maine we have 16 species of mason bee, only one of which, Osmia caerulescens, is non-native. They are often metallic green or blue like the blue orchard bee in the photo above, but are not to be confused with sweat bees which are also usually metallic but in a totally different family (Halictidae). Mason bees will sting if you squeeze them too hard, but the sting is very minor. Mason bees live in holes in wood the stems of reeds and are solitary, which is to say they do not have a single queen and lots of workers, rather each female lays her own eggs and provisions for them. They are however, fairly gregarious, with females laying their eggs in holes right next to other females. The photo below shows a cut-away bird's-eye-view of what the nests of individual females look like in a man-made mason bee home. A female will select a hole, and at the furthest point from the entrance she will put a ball of collected pollen, lay a single egg on that pollen ball, and then build a mud wall to close off that "cell". She will repeat this over and over until it fills up her hole like so:

Each cell therefore contains a mason bee larva feeding on the pollen ball its mother provided.

In Europe and Japan orchards are effectively using mason bee species for pollination of crops like plums, apples, and nuts. They are highly effective pollinators, with some reports of one mason bee female being able to pollinate as many flowers as 100 honeybees. This has to do with differences in their behavior. Mason bees visit more flowers than honeybees in each foraging visit, travel further between trees, and make more contact with the reproductive parts of the flowers than honeybees. The effort to commercial rear blue orchard bees for almond pollination is colossal, as detailed in the Scientific American article. But if you are interested in interacting with some mason bees in your own yard, it's pretty feasible. Mason bee "hotels" or "condos" have become popular recently. These are easy to make, and there are lots of places you can buy them. They do require some annual maintenance to keep pests under control. 

Homemade mason bee house note that this kind is not great (see below)

Mason bee house for sale from gardening shops

The best mason bee houses have removable/replaceable tubes (often made out of reeds or cardboard). This is because pests, parasites and molds can build up in the houses, so you need to replace the reeds on an annual basis. Mason bees overwinter as cocoons and emerge as adults in the spring, so you would want to wait for the bees to emerge in the spring and then replace the wooden blocks or tubes. If you want to be more involved in management of mason bees you can actually remove the cocoons from the tubes in the fall, sort and clean them from infected cocoons, and overwinter them in your fridge (see lots of details on how to do this here). You are likely to get a mixture of native and non-native mason bee species, as well as some leafcutter bee species (Megachile sp):

Leafcutter bee. Photo by Kim Taylor

Leafcutters cut circular pieces out of plant leaves to line their nests. They are also good pollinators, and we have 11 native Megachile species in Maine and two non-natives. They may, however, leave your roses with circular holes in the leaves, but the roses will survive. 

Bee viruses in bee-mimicking flies

The hoverfly (or syrphid fly) Eristalis interrupta (or nemorum), photo by James Lindsey in Belgium.

This week's paper is in Biology Letters, led by post-doc Emily Bailes from Royal Holloway University of London. Dr. Bailes examined the presence of honeybee viruses in hoverflies (also called syrphid flies as they are in the family Syrphidae). Syrphid flies first deserve some introduction of their own. The Syrphidae family is comprised of flies whose adult lifestages predominantly feed on flower nectar and pollen. What is particularly striking about them is their mimicry of other pollinators including a variety of bees and wasps. As a small example, the insects in the photos below are all flies!

Syrphid flies. Photos and layout by Joaquim Alves Gaspar. 

Although syrphid flies fill the same niche as bees (foraging from flowers), and look like bees, there has been little investigation of their role in the spread of pollinator diseases. It has been previously demonstrated that viruses originally found in managed honeybees can spread to wild native bees through visits to shared floral resources . The role of very ecologically similar, but evolutionarily distant, syrphid flies in disease dynamics had remained unexplored. Dr. Bailes and her colleagues collected 20 individuals each of honeybees and four species of syrphid fly at a long-term study site in England called Wytham Woods (famous for its research with great tits). Of the four syrphid flies, two species are honeybee mimics in the genus Eristalis that not only look like honeybees (see the first photo above) but also mimic honeybee behavior at flowers. The other two species were in the genera Episyrphus and Platycheirus and although they forage for nectar and pollen from flowers they do not look or act like honeybees. Dr. Bailes and her colleagues used RNA sequencing to determine the presence or absence of six common bee viruses in the honeybees and flies. They found bee viruses present in the two honeybee mimicking Eristalis, but not in Episyrphus and Platycheirus even though those flies are visiting flowers in the same habitat! The viruses that occured in Eristalis were in lower numbers than in honeybees, and had almost identical RNA sequences to the viruses from honeybees, indicating that the viruses may not be replicating in flies, rather the flies are picking them up from honeybees. The flies, however, may still be able to serve as vectors of the viruses even if they don't infect the flies. The extent to which these viruses are replicating in the flies (and negatively impacting the flies) is an area in need of further investigation. Also I really want to know more about why the viruses only occur in Eristalis. Are they more likely to have the viruses because they share more individual flowers with honeybees? Or is it because of something else about how they behave? I am fascinated by how behavior could be shaping disease transmission. 

More field borders lead to more bees & why we need more bee diversity

A native bee montage by Sam Droege. 

Bee double-header this week! You may be overwhelmed by the bee landscape ecology papers, and honestly so am I. But this is an attempt to keep up with the literature, so here it goes. Two papers this week. The first one I will cover is in Proceedings of the Royal Society of London B, lead by Annika Hass a PhD student at the University of Göttingen in Germany, and examines how field edges and crop diversity affect bee communities and pollination in Western Europe. The second paper is in Science, lead by Rachael Winfree, a professor at Rutgers University, examines the number of bee species necessary for successful crop pollination in the field. 

In the Proc R Soc B paper, Hass and her colleagues examined the pollinator communities in 229 fields in 4 European countries. To examine the pollination services of those pollinators they planted rows of radish, Raphanus sativus, along the edges of the fields and measured seed set. It's a little counter-intuitive to think about radish pollination, as we mostly eat the roots of radishes rather than the fruits. But people do sometimes eat the radish seed pods, and sometimes use the seeds for oil (and they are definitely used for making more radishes). For each field they mapped the field-border density (they call this configurational heterogeneity), as well as the diversity of crops in the field. Hass and her colleagues found that field-border densities were positively correlated with wild bee abundance, and wild bee abundance was positively correlated with radish seed production on the field edges. Interestingly, crop diversity was actually negatively correlated with wild bee abundance. The authors propose that this is because increased crop diversity in their European fields meant more highly managed crops (with associated pesticide applications). It would be interesting to see if these results are the same when you increase diversity without highly managed crops. It's a little hard for me to envision what higher field border densities (configurational heterogeneity) would look like, and I wish that they had included aerial photographs of fields with high and low field border densities. But generally it seems that interrupting monocultures with natural field borders enhances numbers of bees, and that makes intuitive sense. 

In the Science paper, Winfree and her colleagues measured pollination of watermelon, cranberry, and blueberry, by wild bees on 16 farms in New Jersey and Pennsylvania. They collected bees visiting flowers in each of these crops. In addition they bagged fresh flowers until they opened, and then removed the bags. They recorded the first bee species to visit the flower and then recorded the number of pollen grains deposited by that bee, giving them data on the pollination services of different bee species (I think this is very cool!). They found that in order for the crops to receive target levels of 50% pollination at one site alone might take less than 20 bee species, but to achieve that level of pollination over 15 different sites (spread over thousands of kilometers and thereby varying in many different factors) would require to ecosystem to maintain more like 50 different bee species, and 75% pollination would require 80 different species. When people think of crop pollination they mostly think of honeybees, and this study is so important because it highlights that to effectively pollinate our crops we cannot rely on honeybees but rather need a large diversity of bees.

One that note, the honeybee is a managed livestock species introduced from Europe and is not a good solution for loss of our native bees, and in fact is part of the problem (see recent NPR story on this). I love honey as much as I suspect you do, and we currently are dependent on managed honeybees for many of our crops (because of the way we plant them in huge monocultures - but that's for another time, and see the Proc R Soc B paper above). But we need to be clear when we are talking bee conservation we are not talking about honeybees, honeybees have management problems, but that is a livestock management challenge, not a conservation issue. I have made the analogy that focusing on honeybees when we talk about bee conservation is as if a bird conservation discussion was focused on chickens. There is a lot of research needed on honeybee issues (plus they have very cool biology), and they are an important part of our food chain and economy, but these are not conservation issues. 

Floral Shape and bee communities

A honeybee on an open-shaped flower. Photo by George Gray. 

A bumblebee on a tube-shaped flower, photo by Brendan Zwelling.

This week's paper is published in Biology Letters, single-authored by Katherine Urban-Mead, a graduate student in the Department of Entomology at Cornell University. Urban-Mead used network analysis to examine how the shapes of flowers impacted bee species abundance in floral communities. In particular, Urban-Mead compared the availability of flowers with open corollas where the nectar is easily accessible to bees (especially short-tongued bees, but more on that later) with flowers with tube-shaped corollas where the nectar is at the base of the corolla requiring bees to enter the flower (and may therefore be easier for long-tongued bees). 

Urban-Mead worked in six meadows in Connecticut containing diverse flowering plants. In each meadow she selected three 3 x 6 m plots that had similar floral communities. In one plot she removed all the open flowers from one half of the plot, in the second plot she removed all the tube-shaped flowers from one half of the plot, and the third plot was left undisturbed. Urban-Mead then watched these floral plots and recorded the visits made be visiting bees of different morphospecies (bees are quite hard to identify to species in flight - so they are often lumped into identifiable groups). In total she saw more than 500 bees visit more than 3500 flowers. 

The bee community that visited open flowers in all plots was more diverse than the bee communities that visited tube-flowers. In the plots with the open flowers removed, the bees on the remaining tube flowers were not different from the bees on the tube flowers in the undisturbed plots. In the plots with the tube flowers removed, however, the bees on the open flowers were different from the bees on open flowers in undisturbed plots. Part of this shift appears to be due to tongue-length. Bees with longer tongues can more easily access nectar in tube-shaped flowers, and correspondingly, there is a higher proportion of long tongued bees in the control plots and plots with open flowers removed than in plots with tube-shaped flowers removed. It appears, therefore, that the availability of tube-shaped flowers is a more important predictor of bee communities than open flower shapes, but open flowers host higher bee diversity in general. 

Task complexity and social learning in bumblebees

A buff-tailed bumblebee, Bombus terrestris. Photo by Kathleen Purser. 

This week's paper is in Behavioral Ecology, and is lead-authored by David Baracchi, a post-doctoral researcher at the University of Toulouse in France. Baracchi and his colleagues have examined how the difficulty of a foraging discrimination task (being able to tell which flowers are rewarded) affects the use of social information in bumblebees. In bumblebees, one source of social information is the presence of another bee on a flower. The presence of that bee could indicate to an observer that a flower has available resources. Social information comes with costs and benefits (see my previous post about social learning here). For example, the presence of that bee on the flower also could indicate that the observer bee would have to compete with that bee for those floral resources. Researchers have therefore proposed that individuals should only use social information selectively, and should rely on information they have acquired through their own experience the rest of the time. This has lead to the development of "social learning strategies" which are predictions about when animals might be expected to use social information. For example, you might expect an individual to be more likely to use social information when they are inexperienced, or uncertain about the environment. Baracchi and his colleagues have examined how difficulty in discriminating rewarding from unrewarding flowers affects social information use. 

The difficulty in the floral discrimination task was determined by the difference in the number of bars displayed by rewarded and unrewarded flowers (see figure above from Baracchi's paper), such that one bar versus four bars is an easy discrimination task, whereas five bars versus four bars is a hard discrimination task. Bees were first trained to two different stimuli. They were trained to associate the presence of four bars with sugar solution, and to associate the presence of another bee with sugar solution. Then bees were given a range of tests and Baracchi et al. examined the percentage of errors (landings on unrewarded flowers) made by bees. Bees received the flowers alone, the flowers with social information consistent with the floral information (the bee was present on the four bar flower they had been trained was rewarding), or a conflicting information scenario in which the bee (which they had been taught was rewarding) was now present on the other, non-four bar, flower (either one or five, which they had been taught was not rewarding). 

Baracchi et al. show that when the task is easy, bees perform similarly regardless of whether the social information is available, consistent, or in conflict. In contrast, when the task is hard, errors are substantially reduced when the social information is consistent. These results highlight that while social information may not be important to bees when faced with easy discrimination tasks, in the cases of hard discrimination tasks, bees may be able to use additional sources of information to increase their foraging success. 

Fungicides, pathogen infections, and bumblebee declines

The western bumblebee, Bombus occidentalis, whose populations are currently in decline. Photo by Diane Wilson.

This week's paper is lead-authored by Professor Scott McArt at Cornell University, and is published in Proceedings of the Royal Society B. McArt and his colleagues have examined the factors associated with declines in populations of four declining bumblebee species in the US: Bombus occidentalis, Bombus affinis, Bombus pensylvanicus and Bombus terricola. McArt and his colleagues collected over 10,000 bumblebees from 284 sites in the USA. Bees belonged to these species known to be in decline as well as bumblebee species whose populations are currently stable (Bombus bimaculatus, Bombus impatiens, Bombus vosnesenskii). At each of the 284 sites they quantified 24 landscape variables including: latitude and longitude, habitat types, total human population densities, and pesticide usage including insecticides, herbicides, and fungicides. They also screened the collected bees for two parasites: Crithidia bombi and Nosema bombi. These two parasites are suspected to be an important component of bumblebee population declines. McArt and his colleagues then used multi-variate model selection to assess the impact of individual habitat and pesticide variables on infection prevalence and population declines in bumblebees. They found that the best predictor of both N. bombi infection and bumblebee population declines was use of the fungicide Chlorothalonil. Chlorothalonil is frequently used to combat fungi, molds and mildew, on trees, turf, and fruits. The maps below (from McArt et al. 2017) show the prevalence of Chlorothalonil usage overlaid with parasite infection and population declines in bumblebees. 

Chlorothalonil has already been shown to be associated with honeybee parasite infection, and has negative impacts on colony growth in the common eastern bumblebee, Bombus impatiens. The mechanism by which chlorothalonil affects bees is uknown, but one possibility is that it disrupts the bee's normal gut microbiota, making them more susceptible to parasite infection. Other interesting findings from this study include a negative relationship between parasite infection and urbanization. McArt and his colleagues suggest that the diversity of flower resources in urban gardens may actually enhance bumblebee nutrition, buffering them against pathogen infection. 

Kent Island Special! Effects of Climate Change on Reproduction in Storm-Petrels

Bowdoin student and Kent Island fellow, Claire Goffinet ('19) with a Leach's storm-petrel chick summer of 2017. Photo by Fred Field for Bowdoin College

This week's paper is in Global Change Biology and is co-authored by three former Kent Island Directors. It is lead-authored by Bob Mauck of Kenyon College, with Don Dearborn of Bates College, and (posthumously) Chuck Huntington of Bowdoin. The three directors used long-term data collected on Kent Island to study the effects of global temperature on reproductive success in Leach's storm petrels. Data on temperature has been collected on Kent Island since 1939, and the storm-petrel dataset was initiated by Chuck Huntington in 1955. In this week's paper Mauck et al. examined the effects of local (Kent Island) temperature, global mean temperature (a combination of air and sea temperatures), and sea surface temperature on reproduction of storm-petrels using 56 years (1955-2010) of the Kent Island long-term databases on weather and petrel reproduction. The best fitting model for predicting storm-petrel reproductive success included both global mean temperature and local temperature on Kent Island, but global mean temperature is the most important predictor of reproductive success in storm-petrels.

Mauck et al. found that as temperatures rose between 1955 and 1988 storm-petrel hatching success increased (likely due to decreased incubation costs), until in 1988 it appears that global temperatures reached a critical point, and since 1988 hatching success as declined as global temperatures have continued to rise. The decline in hatching success since 1988 is most likely due to the negative impacts of increasing temperatures on food availabilities for petrels as fish move further northward and into deeper waters. 

The effects of increasing temperature, however, were not the same on all birds. Birds with more breeding experience have higher hatching success in general, and appeared to be somewhat buffered against these effects of climate change. The effects of increasing temperatures on hatching success were more strongly observed in less experienced petrels (both positively before 1988 and negatively afterword). Mauck et al. propose that this is because less experienced petrels are less effective foragers, and therefore have benefitted more from reduced incubation costs with increased temperatures, but suffered more from reduced food availabilities. 

Two authors and Kent Island Directors in 2007, Bob Mauck (L) and Chuck Huntington. Photo by another Kent Island Director, Ed Minot.

Kleptopredation in nudibranchs

The nudibranch (a kind of mollusk), Cratena peregrina, on it's prey, a hydroid (which are related to jellyfish - yes! I know it looks more like a plant). Photo by Jean-Marc Kuffer.

This week's paper is in Biology Letters, lead authored by Dr. Trevor Willis who is a Senior Lecturer at the University of Portsmouth in the UK. Willis and his co-authors studied the relationship between nudibranchs and their hydroid prey off the coast of Sicily. Nudibranchs are spectacular little animals. Often referred to as "sea slugs" (which does them no justice) they comprise about 2,300 species of shell-less mollusk distributed worldwide. They vary enormously in color, including bright polka-dots and stripes, as well as in shape. The plumes on their backs are called cerata and are where much of their gas exchange occurs (gills) and also where they defend themselves through nematocysts, stinging cells that they acquire from their prey which includes anemones and the hydroids (more on those soon). Many nudibranch species are also toxic, either via the consumption of toxic sponges or de novo synthesis of toxins. These defenses likely explain the extraordinary warning colorations of many nudibranchs. 

Many nudibranch species, including Cratena peregrina, the subject of this paper, consume hydrozoans. Hydrozoans are small animals related to jellyfish. They have different life stages, one of which is the polyp stage in which they are called hydroids. Hydroids are most commonly colonial, which is to say they live in groups. Hydroids are a bit like upside-down jellyfish that live in little tubes all connected to each other in a branching pattern (which makes them look a bit like a plant). 

The hydroid Eudendrium racemosum. Photo by Fernando Herranz.

Hydroids use the stinging nematocysts on their tentacles to capture zooplankton prey. Hydroids themselves are then prey to nudibranchs. In this week's paper Willis and his colleagues examined this relationship between nudibranchs, hydroids, and the hydroids' feeding on zooplankton. In particular, they tested the hypothesis that nudibranchs prefer to feed on hydroids that have just captured a zooplankton, than on hungry hydroids. To do this they brought nudibranchs and into flowing seawater tanks in the lab and provided them with the choice between feeding on hydroids that were starved versus hydroids that had just been fed zooplankton. They measured nudibranch preferences for fed and starved hydroid polyps as well as how long it took the nudibranchs to consume fed and starved polyps. They also examined the stable isotope ratio of nudibranchs, hydroids, and zooplankton (see my post on "Smashing & Spearing Stomatopods" for more explanation of stable isotope analysis) to assess what nudibranchs are eating in the wild. 

Willis and his colleagues found that nudibranchs preferred to attack hydroid polyps that had just consumed zooplankton over starved hydroids, and it took nudibranchs longer to consume those fed hydroids than starved hydroids. In addition, Willis showed with stable isotope analysis that nudibranchs were not solely consuming hydroids, but that zooplankton made up at least half of their diet. This data suggests that not only are nudibranchs preferentially consuming hydroids that have just captured prey in the lab, they also do so in the field. Willis and his colleagues introduce a novel term for this behavior: "kleptopredation". Kleptopredation is a combination of kleptoparasitism (when animals steal food from other individuals) and predation, as the nudibranch in this case is doing both. It is not clear why nudibranchs do this. The most obvious hypothesis is that polyps with captured zooplankton deliver more calories (and potentially nutritional diversity?) than starved polyps. Willis also suggests that the consumption of fed polyps results in nudibranchs consuming less polyps total, and may prevent them from driving their hydrozoan prey locally extinct. 

The mutualism between bats and pitcher plants

The Bornean bat Kerivoula hardwickii approaching the pitcher plant Nepenthes hemsleyana. 

Bat inside a pitcher plant roost. Photos by Merlin Tuttle.

This week's paper is in Scientific Reports, lead authored by Michael Schöner at the University of Greifswald in Germany. The research focuses on an extraordinary relationship between the woolly bat, Kerivoula hardwickii, and a pitcher plant, Nepenthes hemsleyana. Pitcher plants are believed to have evolved in areas with low soil nitrogen content. To achieve their necessary nutrients these plants have turned to carnivory. The pitcher part is a liquid trap, usually filled with digestive juices. The pitchers emit odors that attract insects who become trapped in the pitcher where they are digested, providing nutrients for the plant. Nepenthes hemsleyana, however, is different. Rather than emitting attractive odors or containing digestive juices, instead the pitcher of N. hemsleyana is a perfect roost for bats. Woolly bats sleep in the pitcher plant during the day, and poop there, providing nitrogen for the plant. These pitchers have an unusual shape that makes them not only ideal for a sleeping bat, but also easily detected by echolocation. Additionally, the inner wall of the pitcher has a waxy texture that deters egg-laying insects, providing a pest-free home for the bats. This is considered a mutualism, because the bat provides poop to the plant, and the plant provides a roost for the bat. 

The pitcher plant is highly dependent on the bat, as this pitcher is not particularly good at catching insects. Woolly bats, however, will roost other places than these pitchers. They will roost in the old pitchers of other pitcher plant species, and in furled leaves. So how can the pitcher plant depend on a bat that does not depend on it? In other words, what stabilizes this mutualism?

The authors speculate that the mutualism is stabilized by the quality of the pitcher plants as roosts for the bats. The pitchers of this species make such superior roosts that bats will continue to use them even if they have the option to go elsewhere. To test this they had to examine whether bats preferentially used pitchers of this species (Nepenthes hemsleyana) in the field. The authors first radiotracked bats in the field to examine which of the available roosts the bats were using. At one site pitchers of N. hemsleyana made up only 5% of the available roosts but were all occupied by bats. Interestingly, they did not see any bats switching between different types of roosts in the field (if a bat was roosting in furled leaves they continued to roost in furled leaves and did not necessarily switch to pitcher roosts). To confirm this roost fidelity they brought the bats into flight arenas and gave them a range of options. Schöner and his colleagues found that bats which had been found in pitchers in the wild always selected to roost in pitchers. But 21% bats that had been found in furled leaves in the field switched to pitchers in the lab. This asymmetry in roost selection indicates that bats preferentially roost in pitcher plants over furled leaves. To confirm that bats roosting in pitchers versus in leaves in the field were not genetically different (excluding the possibility that they were different subspecies of bats roosting in different places), Schöner and his colleagues conducted population genetics on the bats collected from different roosts and confirmed that there were not genetic differences by roost. It appears therefore that bats learn, either socially or individually, a certain roost type and then stick with that roost type over their lives.

The mutualism between woolly bats and pitcher plants is likely stabilized by the high quality of the pitcher plants as roosts, and a general preference of bats to use them when they are available. Interestingly, however, it appears that there are individual bats that will use furled leaves as roosts for their entire lifetimes. This willingness to use other roosts could buffer the populations of woolly bats from environmental perturbations that reduce the availability of pitcher plant roosts. 

What does learning look like in a bumblebee brain?

Figure 1 from Li Li et al. a) the arena set-up with bees exposed to 10 flower colors; b) the different experimental treatments; c) the frontal-view of a whole bumblebee brain; d-f) enlarged views of the portions of bumblebee brains involved in vision; g) enlarged so you can see the labeled microglomeruli; h) microglomeruli structure.

This week's paper is in the Proceedings of the Royal Society of London B, lead-authored by Li Li, a PhD student in the Chittka group at Queen Mary University London. Neurons connect to (and thus communicate) with other neurons at regions called synapses. Microglomeruli are places were lots of synapses come together (synaptic complexes). This study looked at the link between bee learning of flower colors, and the density of microglomeruli in the bee's brains.

Li Li and her colleagues tested bumblebees in five different treatments. All bees were first pre-trained to forage from colorless (clear) artificial flowers. For some of the bees that was it, they were dissected to establish a baseline of microglomeruli density with no exposure to colors (Treatment 1). The next group of bees were trained to distinguish between 10 different colors, five of which had sugar solution and five had nasty tasting quinine (like what's in your tonic water; Treatment 2). The third group of bees were trained to distinguish between only two colors to examine the effect of the number of colors bees had to learn on microglomeruli density (Treatment 3). Group four continued to forage on clear flowers for as long as the other bees were learning flower colors to control for the effect of amount of foraging time on microglomeruli density (Treatment 4). In the final treatment the bees continued to forage on clear flowers, but they were surrounded by the colored flowers (with no rewards) to control for the effect of exposure to lots of flower colors (Treatment 5). In treatments 2-5 after the bees were trained they were then given memory tests to determine how well they performed at learning the task. You can see all these treatments detailed in Fig 1b above. 

In the ten color discrimination task (Treatment 2), Li Li and her colleagues found that learning rate and memory performance correlated with microglomeruli density in the collar part of the bee brain (Fig 1c above). This result, however, does not distinguish between correlation and causation. That is to say, it could be that better learners brains' increase more in microglomeruli density, or that bees with better learning abilities are the ones that already have higher microglomeruli densities. In comparing bees that had color learning versus those with no color learning (Treatments 2 and 1), they found that bees in the color learning treatment had higher microglomeruli densities and larger brain calyxes (the brain part in Fig 1d) in total. There are possibilities other than color learning directly to explain this pattern, however, and using the other treatments Li Li and her colleagues were able to show that the brain size is simply a product of the foraging activity the bees did (comparing treatments 4 and 2), and that the microglomeruli density is a product of exposure to colors not learning necessarily (comparing treatments 5 and 2). So in summary, there is a correlation between density of these microglomeruli and bee learning and memory. But causation is tricky, learning colors does seem to increase microglomeruli density, but this effect may largely be due simply to exposure to the colors. 

Larger soldiers....have a better sense of smell? A lesson from stingless bees

Neotropical stingless bees, Tetragonisca angustula, at the entrance to their nest. Photo by Alex Wild.

This week's paper is in Biology Letters, lead-authored by Christoph Grüter at the Universidade de São Paulo in Brazil. The research is with a stingless bee species, Tetragonisca angustula. "Stingless bee" is actually a technical term that refers to bee species in the tribe Meloponini, which is comprised of >500 species distributed throughout the tropics worldwide. Like other social bees they store floral nectar, and stingless bee honey is actually collected by some human cultures (often referred to as melipona or meliponine honey). In many Hymenoptera (the bees, wasps, ants, termites etc.) colonies need to defend themselves from raids on their food or larvae. Raiders might be individuals of the same species from a different colony, or individuals of other species. In ants and termites, colonies often have some individuals that develop as soldiers, who work in nest defense and often are large, with weapons of some kind such as biting mouthparts. In many of the bees and wasps, there is not this need for soldiers because all of the workers can sting. But in the stingless bees there are some individuals that are larger, but they cannot sting and don't have any biting mouthparts...so how do these larger workers defend the colony?

Grüter and his colleagues hypothesized that larger workers would be better at identifying intruders. In the Hymenoptera individuals recognize each other by scent, particularly by the cuticular hydrocarbon profile on their bodies, which they detect through pore plates on their antennae. Larger individuals have larger antennae, therefore more pore plates and a better sense of smell! Grüter and his colleagues hypothesized that the larger bees would be better at distinguishing between nest-mates and non-nest-mates. 

Grüter et al. had 10 colonies of T. augustula in the lab on campus at São Paolo. Into each colony they introduced bees that were either nest-mates, non-nestmates, or from a different stingless bee species, and recorded the responses of the guarding soldier bees. They also measured the size of the guarding bees. They found that larger bees were more likely to accurately identify and attack non-nestmates, and that the larger bees also had larger antennal surface areas and more pore plates. This confirms Grüter et al.'s hypothesis that larger bees have better senses of smell and are better able to identify intruders. I would think that the larger bees are also better able to cope with the intruders once they identify them, but that has yet to be tested. 

When to migrate south? When there is a good tail wind.

A common noctule, Nyctalus noctula. Photo my own.

This week's paper addresses an age old question, how do animals decide when to migrate? The paper is entitled "Determinants of spring migration departure decision in a bat" lead-authored by Dina Dechmann at the Max Planck Institute. Pregnant female noctules in the spring migrate hundreds of kilometers Northeast from hibernation caves to insect-rich feeding grounds (this might be from Switzerland to Sweden or Bulgaria to Russia). But how do they decide when to leave? 

Over three years Dechmann and her colleagues fitted 29 female noctules with radiotransmitters and then used a small Cessna plane to search for the signals of bats that were migrating. They also obtained detailed weather information for the sites where the bats were tagged. In songbirds, birds tend to decide to migrate once they have put on enough fat. That was not the case for noctule bats, their decision to migrate was not affected by their body condition. Migration decisions in noctules were best explained by wind direction, wind speed, and air pressure. Bats were most likely to migrate on nights with faster tailwinds in the migration direction, and with higher air pressure. The tailwinds make a lot of intuitive sense, and generally high air pressure is associated with more stable weather conditions which might also be to a migrating bat's benefit. Songbirds generally migrate much further than bats, so the lack of putting on fat determining migration is likely due to the shorter migration distance. 

How poison dart frogs don't poison themselves

The little devil frog, Oophaga sylvatica, is one of the poison dart frog species in this study. Photo by Lucas Bustamante.

Poison dart frogs (frogs of the family Dendrobatidae, which as far as I can tell comes from "climbs trees" in Greek), are emblematic of the tropics. They are incredibly brightly colored, from blues to reds, to greens and yellows, in stripes as well as spots. But they are as well known for their poisons as for their colors. Their skins contain toxins such as epibatidine, a general toxin that can kill in doses as small as a microgram. They acquire these toxins from consuming poisonous insects (such as centipedes). Extracts from some species of poison dart frogs were used by indigenous Americans to poison the tips of their blow darts. But how does an animal as poisonous as a poison dart frog not poison itself?

This weeks paper, entitled "Interacting amino acid replacements allow poison frogs to evolve epibatidine resistance" is lead-authored by postdoctoral researcher Rebecca Tarvin (UT Austin) and is in Science. Animals that acquire defensive toxins through their diet are generally thought to have three alternative paths available to them to not poison themselves. 1) They can compartmentalize the toxin in their tissues such that toxin is kept separate from the tissues that would be sensitive to it. 2)  They can metabolize the toxin to reduce its toxicity to themselves. 3) They can be insensitive to the toxin's effect. This third option sounds like the safest. There is a hitch, however, because the best toxins are ones with very general effects on many different potential predators. For a toxin to be effective it needs to bind to a receptor. So what types of receptors do many different, distantly related (birds AND rodents AND snakes for instance) all have? Ones that are crucial for biological function. Such is the case with the poison frog, as epibatidine binds to the receptors for acetylcholine, a widespread nerve signaling molecule (neurotransmitter). But how then does the poison frog cope? It needs to be insensitive to epibatidine but still be sensitive to acetylcholine. 

Tarvin and her colleagues found that in the two groups of poison dart frogs that both make epibatidine, they have a single amino acid substitution that changes an amino acid in their acetylcholine receptor, making them insensitive to epibatidine. Both groups separately evolved this same nucleotide change (millions of years apart!). This change alone would make the two groups also less sensitive to acetylcholine, but each group separately evolved a different secondary amino acid substitution that restores their sensitivity to acetylcholine. This highlights the myriad paths that evolution can travel, parts of the solution are reached by the same paths in different lineages, and other parts of solution are achieved through different paths. 

As molecular, biochemical, and neurophysiology techniques improve we are starting to find insights into how a trait as complicated as resistance to a general toxin can evolve, and this paper is a wonderful example of how exciting those discoveries can be. 

 

Vocal flexibility in geckos

Tokay gecko (Gekko gecko) in Thailand. Photo by Tontan Travel. 

This week's paper is from Proceedings of the Royal Society B, authored by Henrik Brumm and Sue Anne Zollinger at the Max Planck Institute for Ornithology. Brumm and Zollinger are the first to show flexibility in vocalizations by a reptile, and how the geckos do it is pretty cool. When we humans are trying to communicate in a noisy space, we usually yell at each other (i.e. increase our amplitude - technically called the Lombard effect). Tokay geckos, Gekko gecko, are native to Southeast Asia. They have a distinctive call, and in fact both the names "gecko" and "tokay" are onomatopoeia for the way the call sounds. Geckos in noisy environments have a different strategy for being heard. 

What they did

The methods for this study are very simple. They had male geckos in captivity in rooms lined with acoustic absorbing material and a microphone. For 24 hours white noise was broadcast to the geckos in the room, and their calls were recorded, and then for 24 hours there was silence and their calls were recorded. They repeated this to record four total days of calls. They then compared call duration, structure, and amplitude during noise and during silence. 

What they found

Geckos did not increase the amplitude of their calls, but they did increase the duration of the call syllables. This should also make them easier to hear. Additionally, Geckos have two types of calls, a softer cackle and the loud "Gecko!" Geckos in noisy environments make more of the louder gecko and less of the quieter cackle. They therefore are selecting to use more of the call types that are easier to hear when they are in noisy environments. 

The takeaway

Vocal flexibility in the form of the Lombard effect has been demonstrated in birds, mammals and even frogs. This is the first demonstration of vocal flexibility in reptiles, but also importantly, it is a different type of flexibility. Increasing the duration of syllables and perhaps selecting different words are tools that we use to communicate in noisy environments, but have not been reported as much in other animals. I am really interested in the use of these two different strategies, both duration increase and use of different calls. The white noise that the author's used is really broadband noise. I wonder if geckos in different types of noisy environments (next to a rushing stream, or when lots of crickets or cicadas are calling around them) use these two strategies differently in different noise contexts.