Do fungus-farming leaf cutter ants smell like fungus?

Figure 1

Superficial view of an Atta bisphaerica leaf-cutting ant nest, in the Brazilian savannah. Photo: Lohan Valadares

A blog post highlighting the article by L. Valaderes and F.S. do Nascimento in Insectes Sociaux

By Lohan Valadares  (@valadareslohan, @lo.han.792)

About 30 million years ago, in the South American savannahs, ants that cultivate fungus have over evolutionary time become the leaf-cutting ants (genera Atta and Acromyrmex). These ants reside in large subterranean nests of the Neotropical region, with galleries and fungus chambers that shelter thousands to millions of individuals, where they farm the fungus Leucoagaricus gongylophorus. The fungus has never been found free-living without the ants, and it is generally accepted that both organisms have co-evolved into an obligate mutualism, which means that one organism cannot live without the other. For the ants, the fungus is priceless as it serves as a rearing site and unique nutritional substrate for brood development. In exchange, the ants protect the fungus against parasites and forage for fresh vegetation, which is used as substrate for fungal growth. Recently, chemical analyses of the fungus gardens of Acromyrmex species have revealed the presence of hydrocarbons, a class of chemical compound found commonly on the cuticle of insects (Viana et al., 2001, Richard et al., 2007). These two species are so intertwined, however, that whether it is the ants or the fungus which are the ultimate producers of these hydrocarbons is not yet clear.

Cuticular hydrocarbons (CHCs) are of particular importance for social insects, and decades of studies have demonstrated that they are important as nestmate recognition cues. Consequently, variations in these substances have been associated with caste, age, dominance hierarchy, worker subcastes, and developmental stages. Furthermore, the leaves used as the fungus substrate seem to be an important source of CHCs for leaf-cutting ants (Richard et al., 2004, Valadares et al., 2015). This leads us to hypothesise that the intermediate organism in this process – the symbiotic fungus – is actually the one promoting the transference of these substances, or may actually be involved in the synthesis of hydrocarbons itself.

To explore the resemblance between the chemical compounds of both organisms involved in this symbiotic association, we studied the resemblance between the CHC profile of fungal cultivars with those of the ants, focusing on the changes in the CHC composition during the ants’ larval-to-adult moulting in the leaf-cutting ant Atta sexdens and its associated fungus. Our main question was: how do the changes in the CHC profile associated with the moulting cycle correlate with the hydrocarbon profile of the fungus cultivated by the ant Atta sexdens? To assess it, we collected pieces of fungal mycelium, and ant larvae, pupae and adult workers from laboratory populations, and soaked them in a solvent to extract their hydrocarbons, which later on were injected into a gas chromatography–mass spectrometry (GC–MS) for separation and identification of hydrocarbons.

Figure 2

An excavated fungus chamber of an Acromyrmex subterraneus leaf-cutting ant nest, in the Brazilian savannah. Photo: Lohan Valadares

Our analyses demonstrated that ant and fungus shared 58% of hydrocarbons, and the rest were all ant-specific hydrocarbons that were absent from the symbiotic fungus. Our comparative analyses revealed a great similarity between the hydrocarbon profiles of larva and fungus, due to the fact that both groups shared mainly highly concentrated linear hydrocarbons. As individuals progressed through developmental stages, the chemical profiles between ant and fungus became increasingly different. As the moulting cycle progressed, the hydrocarbon profile was characterised by a great shift from the ‘less pronounced’ state of the brood’s chemical profile towards a more diverse chemical profile of adult workers comprised of highly concentrated branched hydrocarbons.

Our findings coincide with the observations made for Acromyrmex leaf-cutting ants (Vianna et al. 2001, Richard et al. 2007), strengthening the evidence for the intimate relationship between brood and fungus as a variable shaping the hydrocarbon profile of both species. However, because we don’t know in detail how the hydrocarbons are biologically synthesised and transferred between these organisms, it is difficult to interpret whether the ants or the fungus (or even both organisms) are the ones actually synthesising hydrocarbons. However, we believe that our descriptive and comparative analyses indicating such strong resemblances has suggested new exciting opportunities of research tha­t will help us to understand how this co-evolutionary relationship has shaped the chemical profile of both organisms. If we consider the optimistic scenario where the fungus is actually the one to be transferring these compounds to the ants, how does this transference impact colony odour? Do these substances play a role in nestmate recognition? Several questions remain to be answered and hopefully our work has contributed to the journey towards the understanding of the chemo-ecology between leaf-cutting ants and their fungal cultivars.

 

References

Branstetter, M.G., Jesovnik, Aa, Sosa-Calvo, J., Lloyd, M.W., Faircloth, B.G., Brady, S.G., Schultz, T.R. (2017). Dry habitats were crucibles of domestication in the evolution of agriculture. Proceedings Royal Society B. 284: 20170095.

Richard, F.J., Heftz, A., Christides, J.P., Errard, C. (2004) Food influence on colonial recognition and chemical signature between nestmates in the fungus-growing ant Acromyrmex subterraneus subterraneus. J Chem Ecol 14: 9–16

Richard, F.J., Poulsen, M., Hefetz, E.C., Nash, D.R., Boomsma, J.J. (2007). The origin of the chemical profiles of fungal symbionts and their significance for nestmate recognition in Acromyrmex leaf-cutting ants. Behav Ecol Sociobiol 61(11):1637-1649

Valadares, L., Nascimento, D., Nascimento, F.S. (2015) Foliar substrate affects cuticular hydrocarbon profiles and intraspecific aggression in the leafcutter ant Atta sexdens. Insects 6: 141-151

Viana, A.M., Frézard, A., Malosse, C., Della Lucia, T.M., Errard, C., Lenoir, A. (2001) Colonial recognition of fungus in the fungus-growing ant Acromyrmex subterraneus subterraneus (Hymenoptera: Formicidae). Chemoecol 11(1): 29-36

Interview with a social insect scientist: Mary Jane West-Eberhard

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Polistes fuscatus, a representative of Mary Jane West-Eberhard’s favourite genus. Photo: John Brandauer/flickr

IS: Who are you and what do you do?

MJWE: Mary Jane West-Eberhard, retired research scientist, Smithsonian Tropical Research Institute. Retired = working as usual for less pay.

IS: How did you end up researching social insects?

MJWE: The answer started when I was a little kid. My first pet (or so I thought) was a beautiful sweat bee that looked like a jewel. It landed on my arm when I was about nine years old. I thought it liked me. But then it stung me and flew away! That did it for the solitary Hymenoptera. But I liked wasps – they are perky and beautiful. I first paid attention to them when making an insect collection for a 4-H entomology project. Then, in college I wanted to do something on insect behaviour for my honors thesis at the University of Michigan. Henry Townes, a taxonomist of parasitoid Hymenoptera, suggested that I do it on Polistes. It was the dead of winter but I found some hibernating females and put them in a terrarium. They woke up immediately and immediately started to antennate each other and fight. I figured I couldn’t go wrong with those.

IS: What is your favourite social insect and why?

MJWE: My favourite is still Polistes. Every Polistes species has distinctive visible social displays, and they are always active. Seeing a new species always rewards you with something new and interesting. They never disappoint. I have worked on MANY species of wasps. Some, like Mischocyttarus, are very common in the tropics where I have lived, and they have open nests like Polistes. There are many species and I have tried looking at lots of them but they are unbearably dull compared to Polistes.

IS: What is the best moment/discovery in your research so far? What made it so memorable?

MJWE: I guess there are two kinds of excitement – discoveries during fieldwork, and making new connections (having new ideas). Maybe I can get away with giving more than one example, one for each decade of my fieldwork on social insects:

  • [as an undergrad] Seeing a mother cricket, who was caring for her nymphs, lay a tiny egg and then feed it to one of her nymphs! A trophic egg, like those of ants, but never before seen in a cricket.
  • [As a grad student] Seeing some marked Polistes females return to their single-queen natal nest site after hibernation, and start building nests together (the first direct field confirmation of the relatedness aspect of kin selection theory).
  • Discovering the complex dominance displays of Metabolybia queens toward each other, and the displays of workers toward them that indicated worker choice of queens – they actually dominated some of the queens into becoming workers!
  • Finding a nest of Zethus miniatus the very species studied long ago by Ducke in Brazil, famously a group living eumenine wasp used by Wheeler as a model transitional species.
  • Realizing (in the 1980s) that most alternative states considered “genetic polymorphisms” are actually condition-dependent polyphenisms and other kinds of non-genetically determined alternative forms – just like workers and queens. This undermined some assumptions of genetics and, within behaviour studies, ESS game theory, that predominated at the time.

IS: If teaching is part of your work, what courses do you teach? Has your work on social insects helped to shape your teaching?

MJWE: As a grad student I planned to become a college professor. But my job with the Smithsonian Tropical Research Institute has been a research job; and my husband Bill has taught the courses I might have taught in the places we have lived. But I like to think that the general-scope writing I have done is a kind of teaching – “courses” on the evolution of insect societies, sexual and social selection, and development (including of behaviour) in relation to genetic evolution. I like to think that it helps researchers working on real organisms to see the general significance of their work.

IS: What is the last book you read? Would you recommend it? Why or why not?

MJWE: “Hillbilly Elegy,” by J.D. Vance. I recommend it because it describes some truly forgotten, especially by academics and politicians, elements of US society – their deep problems and why ignorance (including bigotry) is entrenched and difficult to deal with, for those (victims and idealists) who would try to find a way out of it.

IS: Did any one book have a major influence in shaping your career? What was the book and how did it affect you?

MJWE: Mayr 1963, “Animal Species and Evolution.” A grad-student seminar (led by R.D. Alexander) read that book and we critically examined every page – every sentence. The book was mainly about speciation, but it was a summary of organismic evolutionary biology at that time. I still use it for history and references – as a marker of what was understood when I was a student, and what was not.

IS: Outside of science, what are your favourite activities, hobbies or sports?

MJWE: My favourite activity is good conversation. “Good” means intelligent and entertaining (this does not necessarily mean intellectual and can be with small children or people without earphones on airplanes). It means open as well as considerate. Travel. Watching behaviour including of people, and trying to figure out what is going on in different settings, and why. My work and my family have always been my hobbies. Aerobics 3 times a week.

 

IS: If you were on an island and could only bring three things, what would you bring? Why?

MJWE: A flashlight, a bottle of water, and a helicopter. The “why” seems self explanatory.

IS: Who do you think has had the greatest influence on your science career?

MJWE: Richard Alexander, my professor at the University of Michigan. He encouraged critical thinking and independence, and encouraged thinking about the general importance of my discoveries. He didn’t expect his students to work on aspects of his own research. He was bursting with original ideas and always talked about them. He didn’t worry about getting ripped off because he was publishing as fast as he talked.

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

MJWE: Choose a species or a taxon and resolve to become the world expert on it – to learn everything that is known about it, including classification, physiology, behaviour, evolutionary history. Then do whatever you have the greatest patience for. For example, I have no patience for making apparatus work in a lab. But I can watch animal behaviour for hours and hours without getting bored. Whatever you do, whether it is ecology, or library work, or laboratory experiments, or microscopic studies of morphology, be sure to spend SOME time observing behaviour, because that will give you clues about whatever you are trying to understand.

 

 

Interview with a social insect scientist: Corrie Moreau

Moreau_Rome_2017

IS: Who are you and what do you do?

CSM: I am Dr. Corrie Moreau (@CorrieMoreau), Associate Curator/Professor at the Field Museum of Natural History. I oversee a very large scientific collection and run an active research program using molecular and genomic tools to study the evolution of social insects.

IS: How did you end up researching social insects?

CSM: Since a young age I have always wanted to study ants. Growing up in New Orleans, Louisiana, there were always ants everywhere and they completely fascinated me.

IS: What is your favourite social insect and why?

CSM: Ants! There are so many closely related species that look and behave differently and even distantly related species that have converged on their morphology and behaviors. These differences and similarities provide an excellent system to understand how and why these traits evolve.

IS: What is the best moment/discovery in your research so far? What made it so memorable?

CSM: For me there are two moments in my research so far that have stood out. One came when I inferred the first large-scale molecular phylogeny of the ants and found striking diversification that corresponded to the rise of the flowering plants. The second came when I started to realize the key role that host-associated bacteria can have on the ecology and evolution of social insects. For me what made these both so memorable is they helped explain the ecological and evolutionary success of the group of organisms I had been studying so intimately.

IS: If teaching is part of your work, what courses do you teach? Has your work on social insects helped to shape your teaching?

CSM: Being at a large natural history museum, I have the opportunity to share my research and educate a very diverse audience on a daily basis. This is really rewarding. Since everyone has at least seen an ant, this opens the door to be able to talk about cutting-edge research and how this informs other aspects of science. I have also taught a phylogenetics course at the University of Chicago and enjoy being in the more formal classroom setting too. Being able to share the theoretical framework and analytical skills that allow students to address their own research questions is very gratifying.

IS: What is the last book you read? Would you recommend it? Why or why not?

CSM: I am currently reading “Time, Love, Memory: A Great Biologist and His Quest for the Origins of Behavior” by Jonathan Weiner. It was sent to me as a gift from Dr. Hopi Hoekstra, behavioural geneticists at Harvard University. The book follows the research career of Dr. Seymour Benzer to tell the history of behavioral genetics. The book is very well written and provides insights into not only the scientific highlights of this field, but the opportunity to learn a little about the lives of several scientists that helped develop this field.

IS: Did any one book have a major influence in shaping your career? What was the book and how did it affect you?

CSM: One book that I consistently return to is “Ants: Their Structure, Development, and Behavior” by William Morton Wheeler. This book was published in 1910 and is still one of the most insightful and complete books on ants. Of course, many things we know about ants has changed in the last 100 years, but this book still has so many inspiring insights into ant biology. And the figures and diagrams on ant internal and external anatomy are excellent!

IS: Outside of science, what are your favourite activities, hobbies or sports?

CSM: Reading, running, yoga, hiking, and traveling the world for research and fun with my husband, Dr. Christophe Duplais.

IS: How do you keep going when things get tough?

CSM: I wish I had some words of wisdom here since I know everyone has difficult times or obstacles to overcome. For me I try to return to what excites me, which is often enough to help push me through the tough times.

IS: If you were to go live on an uninhabited island and could only bring three things, what would you bring? Why?

CSM: This is a tough question. I would bring an avocado seed to grow lots of avocados to eat. A hand lens to be able to try to identify all the cool insects I find. And, lastly, a field notebook (and lots of pencils – I know that is more than one thing, but you need pencils if you have a notebook) to record all my observations.

IS: Who do you think has had the greatest influence on your science career?

CSM: I don’t think any scientist can attribute their careers to one person and that is certainly true for me. My advisors and mentors from undergraduate, master’s, Ph.D. and postdoc all deserve very special thanks. In addition there are a myriad of teachers and scientists that have had a big impact on the way I think and try to solve problems. I thank them all.

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

CSM: Follow your passions. Working in science is really rewarding, and I believe it is important to do what you love everyday. So if you are passionate about some aspect of social insect science then you should absolutely go for it! There are more questions and species than people on the planet so we need all the social insect scientists we can get.

 

 

Interview with a social insect scientist: Elizabeth Tibbetts

E TibbetsIS: Who are you and what do you do?

ET: My name is Elizabeth Tibbetts and I am a professor in Ecology and Evolutionary Biology at the University of Michigan.

IS: How did you end up researching social insects?

ET: I’m not one of the those people who always loved insects. In fact, I was pretty scared of them as a child. I decided to study social insects in graduate school because they seemed more tractable than vertebrates. I’m glad I did. I fell in love with wasps and haven’t looked back.

IS: What is your favourite social insect and why?

ET: My favourite social insects are Polistes paper wasps. I’ve become quite attached to them over the years. I love the way their social organization combines cooperation and conflict. Polistes form stable societies, but each wasp also has its own agenda. Sometimes individuals fight for supremacy within their group or leave their natal nest to reproduce independently. Polistes are also a great group to study my favourite topics: communication and cognition.

IS: What is the best moment/discovery in your research so far? What made it so memorable?

ET: My best moment of scientific discovery happened in graduate school when I figured out that Polistes fuscatus use their facial patterns for individual recognition. In my second year of graduate school, I noticed that Polistes fuscatus wasps have highly variable facial patterns. I followed up the observation with a few behavioural experiments. I still remember the thrill of analysing the data and realizing my experiment worked. Wasps really are capable of individual face recognition.

As a new graduate student, I wondered whether I could ever discover something new. People have been studying social insects for hundreds of years, so how could I hope to contribute anything? Over time, I’ve learned that there is no lack of exciting research questions in even the most common organism.

P fuscatus individual recognition

The distinctive facial markings of Polistes fuscatus. Photo: E. Tibbetts

IS: If teaching is part of your work, what courses do you teach? Has your work on social insects helped to shape your teaching?

ET: I teach animal behaviour classes at introductory and advanced levels. I’m sure I include more insect examples than many animal behaviour instructors. However, I try to limit myself. For some reason, introductory students tend to be more interested in whales than bees.

IS: What is the last book you read? Would you recommend it? Why or why not?

ET: I recommend “Lab Girl” by Hope Jahren. It’s a beautifully written memoir about her life as a plant geobiologist . The book does a great job of describing the ups and downs of life as a research scientist.

IS: Did any one book have a major influence in shaping your career? What was the book and how did it affect you?

ET: In high school, I read all the books in the ‘Nature’ section of our public library. Some were great (“The Selfish Gene”, “Gorillas in the Mist”), while others were not so great (“The Naked Ape”). That section of the library is probably responsible for my decision to study biology as an undergrad and animal behaviour as a grad student.

IS: Outside of science, what are your favourite activities, hobbies or sports?

ET: Most of my time outside of work is spent with my two kids (4 and 7 years old). We spend a lot of time playing Legos, pretending to be superheros, reading, and swimming.

IS: How do you keep going when things get tough?

ET: I remind myself that a scientific career is a marathon rather than a sprint, so there is no need to panic about a failed experiment or a rejected grant. There is usually lots of time to overcome challenges and turn things around.

IS:  If you were to go live on an uninhabited island and could only bring three things, what would you bring? Why?

ET: I would bring a satellite phone to call for help, fresh water, and a book to read while I wait.

IS: Who do you think has had the greatest influence on your science career?

ET: I’m grateful to my dad for instilling an early love of science. My graduate experience at Cornell was also very influential. There was a large, enthusiastic group of graduate students who had a big effect on my scientific development. My advisor, Kern Reeve, and committee, Tom Seeley, Elizabeth Adkins-Regan, and Cole Gilbert were also wonderful.

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

ET: Having a life outside work (hobbies, family) is compatible with being a successful scientist. Don’t let anyone convince you otherwise.

Get in the habit of writing every day. You need to get your ideas into the world and effective writing is the best way to do it.

 

Interview with a social insect scientist: Juliana Rangel

juliana

IS: Who are you and what do you do?

JR: My name is Juliana Rangel, Assistant Professor of Apiculture at Texas A&M University in College Station, TX, USA. I run a research and teaching program focusing on the health and biology of managed and feral Apis mellifera colonies.

IS: How did you end up researching social insects?

JR: When I was an undergraduate student at the University of California, San Diego, I emailed Dr. James Nieh, who had just started his position as Assistant Professor in the unit of Ecology, Behavior and Evolution, which was also my major. Coming from Colombia, I wanted to get experience with research, especially in projects that were being conducted in the tropics. Coincidentally Dr Nieh had a research project in Brazil studying communication mechanisms in stingless Melipona bees. I worked for a semester analysing sound pulses produced by Melipona mandaçaia foragers upon being trained to feeders… I really liked what I was doing! Then Dr. Nieh invited me to be his research assistant in Brazil working with actual colonies… the rest is history. I worked with stingless honey bees for the rest of my undergraduate years, and in 2004 I started a doctoral degree in the department of Neurobiology and Behavior at Cornell University still working with stingless bees. My project wasn’t going fast enough so a couple of years into it my Ph. D. advisor, Dr. Tom Seeley, suggested that I switched to working with Apis mellifera. I have worked on several research projects exploring various aspects of reproductive biology of queens and drones ever since, and I love it.

drone with varroa

Left: a male honey bee (drone) with a varroa mite on its back. Right: a queen honey bee.

IS: What is your favourite social insect and why?

JR: Of course Apis mellifera. Despite being widely studied, there are still so many fascinating discoveries about its biology that never stop to amaze me… the way that colony organization is decentralized and yet so meticulously timed and executed is a feat difficult to top by any other organism… and the rules applied in decision-making processes are just as captivating. I am particularly amazed at how sperm storage is maintained for so long in honey bee queens after mating… overall there are just too many factoids about honey bee biology that make it the ideal organism to study and love.

IS: What is the best moment/discovery in your research so far? What made it so memorable?

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A honey bee swarm taking off.

JR: I have had many great moments of discovery, but my favorite one happened in 2009. I was on Appledore Island, Maine, studying with Tom Seeley the signals (and signallers) that initiate a swarm’s departure from the parental nest. We set up glass walled observation colonies and artificial boxes that nest-site scouts soon discovered and started recruiting nest mates to. Upon arrival to the boxes our assistant Sean Griffin (who still also studies pollinators) would label scouts with paint on their thorax so that we could identify their arrival back at the observation colony. We soon discovered that indeed, nest-site scouts start the house hunting process days before a swarm leaves the parental nest, a great discovery of its own. Even though Sean had labelled a few hundred bees from one colony that was preparing to issue a swarm in a couple of days, we did not find that many labelled bees back in the colony. Something was off… when the swarm left a couple of days later, we suspected something weird and opened the nest box, only to find hundreds of labelled bees “guarding” it by staying inside until the swarm movedinto the box. This exciting discovery led us to conduct a follow up study the next summer in which we set up pairs of swarms on stands (we could distinguish the two form the color of their cuticle) and video taped what happened inside nest boxes. Indeed swarms compete for high quality nest sites by keeping guard inside the coveted boxes, and engage in overt aggression ranging from behavioural escalation of intent, to direct stinging and lethal combat. Really cool stuff…

IS: If teaching is part of your work, what courses do you teach? Has your work on social insects helped to shape your teaching?

JR: I teach three courses. Two undergraduate courses are focused on honey bees: Honey Bee Biology which is a course for juniors and is solely lecture-based. And my favorite, Introduction to Beekeeping, which is a field, hands-on ‘laboratory’ course that teaches students how to start their own colonies and how to manage them throughout the year. I also teach a graduate-level course on “Professional Contract and Grant Writing” which helps students understand the “art” of grant writing and award management.

IS: What is the last book you read? Would you recommend it? Why or why not?

JR: I am currently reading “Bee Genetics and Breeding” by Tom Rinderer. It’s a very thorough book on all aspects of honey bee breeding. I would highly recommend it to people studying honey bee reproductive biology. Although it was written in the late 80s, it still has a lot of pertinent information about queen and drone biology, some of which has not been advanced much since the book was written.

IS: Did any one book have a major influence in shaping your career? What was the book and how did it affect you?

JR: Yes, “The Wisdom of the Hive” by my Ph.D. advisor Tom Seeley. I had to read it for my oral exams, and it gave me a lot of insights into what we knew and didn’t know (then) about colony organization. Oh, and of course “Honey Bee Biology” by Mark Winston, because even though it has not been updated since 1987, it shows how much we still don’t know about honey bee biology. The are “must reads” by anyone studying Apis mellifera.

IS: Outsisde of science, what are your favourite activities, hobbies or sports?

JR: I love to travel and to go camping. Now that I am a new mother of a six-month old baby, I love spending time with my husband and kid just walking and traveling with them… and with our red heeler dog, Max. I also love to cook and to entertain friends and family at our home… and I play the guitar and sing Latin American folk songs, especially during gatherings.

IS: How do you keep going when things get tough?

JR: I rely on my family for support, and try to communicate with colleagues and mentors who have always supported me. I have always found that talking about what is going on, regardless of how difficult the situation might be, is very positive for resolution. As my wise mother always says, “no two days are alike” and “each day comes with its own rush,” both of which are true. Taking life one day at a time but with a good plan for the future has worked well for me.

IS: If you were to go live on an uninhabited island and could only bring three things, what would you bring? Why?

JR: This one is very tough. Would I be alone or with my family? If I was alone I would bring my baby, my husband, and my mother… but what about the rest of my family? And Max? Oh this question is tough. If it had to be things, not people… tools to seek and cook food and/or to make a shelter. That’s all. Maybe a pen and paper.

IS: Who do you think has had the greatest influence on your science career?

JR: Of course it has to be my PhD advisor, Tom Seeley. I am just so lucky to have been accepted in his lab and to have worked so closely with him during my years at Cornell. I could not have asked for a better advisor. I still keep in touch with Tom and ask for advise on life-changing opportunities… his words are always wise and accurate. He also finds joy in seeing me progress in my academic and personal life, which is always a plus.

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

JR: I would say go for it. You know that if you’re in an academic life, you will never be rich. We don’t do this for the money. As the late Dr Tom Eisner said, we do it “for love of insects.” I would encourage students to explore questions that have a basic biology aspect to their research… too much of the current research focuses on next-generation “-omics” work that often overlooks past the importance of knowing basic biology: behaviour, ecology… which are the studies that I find most fascinating still to date. Learn a wide set of experimental tools to be competitive in the current job market, be flexible with your job expectations, and do good, ethical work, always. Oh, and have fun while doing it!

 

Do persistent ants work better together?

A blog post highlighting the article by H.F. McCreery in Insectes Sociaux

By Helen McCreery (@HelenMcCreery)

Ants are famous for their ability to carry heavy things. But some food items are too large and heavy for an ant to carry alone. In some species, ants that come across these large food items will return to the nest to recruit help to carry it home.

Ant species differ dramatically in how effective groups are at cooperatively transporting these items. A small number of species – such as weaver ants and crazy ants – can rapidly carry extremely heavy objects many thousands of times the mass of each individual. On the other hand, most ant species are relatively uncoordinated, and may not succeed at all.

What makes some ant species excel at cooperative transport? One major challenge of cooperative transport is that the group must agree on a travel direction. I hypothesized a behavioral trait possessed by individual ants – persistence – affects groups’ ability to coordinate their efforts in a particular travel direction, and thus, to succeed.

Persistence is a measure of how likely an individual is to change the direction she’s trying to move an object – or even to give up – if she’s unsuccessful. Highly persistent ants will keep pulling in the same direction for a long time, even if it’s not working. If a group is full of highly persistent individuals, they may fail because they pull in opposing directions for a long time. On the other hand, if a group is full of low-persistence individuals, they may change direction too frequently or simply not try for long enough to get going. Some previous work (McCreery et al. 2016) showed that in most cases high persistence improves coordination, at least in a theoretical context. I tested this hypothesis experimentally, by comparing cooperative transport ability in species that differ in persistence, and by manipulating persistence in groups of one species.

For the first part of this project, I worked with four ant species that ranged from impressively successful at cooperative transport (crazy ants: Paratrechina longicornis) to poor cooperative transporters (Formica pallidefulva), with Formica podzolica and Formica obscuripes making up the middle ground – groups in these two species seem to be moderately effective at carrying objects together (see video below). I measured persistence for dozens of individuals in each of these species by watching them complete an impossible task – trying to move a dead cricket I pinned to the ground. Separately, I measured the degree of coordination of groups in each of these species by recording groups engaged in cooperative transport. I measured two aspects of their coordination: success fraction (in what proportion of attempts did groups move at least 10 cm?) and path directness (did they move in a straight line or did they change direction frequently?). If species with highly persistent individuals were also more successful, it would support my hypothesis.

 

Video: H. McCreery

In the four species that I compared, I found just that pattern. Importantly, I found that there was substantial variation among species in both persistence and in coordination. P. longicornis individuals were the most persistent by far, and formed groups that were the most coordinated, succeeding in over 97% of attempts. On the other hand, F. pallidefulva individuals had dramatically lower persistence and were the least coordinated – F. pallidefulva groups only succeeded in about a quarter of attempts. The two other species, F. podzolica and F. obscuripes, both had individuals that were moderately persistent, and formed groups that were moderately coordinated – these groups succeeded most of the time, but with relatively indirect paths, they tended to travel about twice the distance they needed to because they frequently changed direction. High individual persistence is correlated with high group coordination in these four species.

ant pulleyIn the second part of this project, I wanted to test whether coordination could be improved by increasing persistence so I manipulated persistence in groups of F. podzolica. I did this by measuring the path-directness of groups, and then adding one or two infinitely persistent “fake ants,” and measuring path-directness again. I added fake ants by mimicking the pulling force that such ants would apply on an object. I gave groups of ants heavy baits attached to string. Using a pulley system, I could add a pulling force on the baits by adding weight on the end of the string (see above figure). Check out the video below to see how I measured the pulling force of these ants.

 

I measured the pulling force of F. podzolica workers by recording them pulling on coiled chains. They enthusiastically pulled on these chains without bait!
Video: H. McCreery

The fake ants that I added to these transport groups were infinitely persistent, because the string would never stop pulling and never change direction. While the force of one ant made no difference, adding the pulling force of two ants going the same direction seemed to moderately improve coordination. These groups tended to move with more direct paths after I added the fake ants. I was surprised to see even a moderate effect, given that I only mimicked a single possible cue (the pulling force); my fake ants did not mimic anything else about real ants. Together with the results from the first part of this project (species comparison), these results suggest an important role of individual persistence in coordination during cooperative transport.

I found that species with more persistent individuals formed more coordinated transport groups, and that artificially increasing persistence moderately improved coordination. It can be difficult to draw strong conclusions when comparing across species, and indeed, the four species I evaluated differ in many more traits than just persistence. It is possible that another difference among these species, instead of persistence, has a more important effect on coordination. Despite this difficulty, comparing cooperative transport across species that dramatically differ is an important step in understanding the mechanisms of coordination. I would be interested to see if other species, beyond these four, fit a similar pattern with respect to persistence and coordination. The results of this study further suggest additional, targeted experiments that could get at the specifics a causal relationship between persistence and coordination.

Reference

McCreery HF, Correll N, Breed MD, Flaxman S (2016) Consensus or Deadlock? Consequences of Simple Behavioral Rules for Coordination in Group Decisions. PLOS ONE 11:e0162768. DOI: 10.1371/journal.pone.0162768

Interview with a social insect scientist: Raghavendra Gadagkar

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IS: Who are you and what do you do?

RG: My name is Raghavendra Gadagkar and I am currently a Professor in the Centre for Ecological Sciences at the Indian Institute of Science, Bangalore, India.

I do several things:

I research questions concerning the evolution of cooperation and conflict in animal societies, using the Indian paper wasp Ropalidia marginata for my empirical research.

I teach evolutionary biology, behavioural ecology, sociobiology and organismal biology to doctoral, masters and undergraduate students.

As President of the Indian National Science Academy (until recently) and with other similar affiliations, I contribute toward the promotion of science and good science policy in India and elsewhere.

IS: How did you end up researching social insects?

RG:  I was fond of catching and watching insects, frogs and other moving creatures as a child. In college I encountered several colonies of Ropalida marginata on the windows of the zoology department. I could not help watching them out of curiosity and have not since looked back. R. marginata also converted me from a catcher (they sting) to a watcher (their behaviour is fascinating). At first I watched them merely as a layman. Then I began to study them scientifically, but only as a week-end hobby. After my PhD in molecular biology, I converted my hobby into my full-time profession.

IS: What is your favourite social insect and why?

RG:  The tropical primitively eusocial wasp, Ropalidia marginata. I have been studying it for over 40 years and it continues to present me with new intellectual challenges and continues to give me great delight. I have not felt the need to look beyond, with the exception of occasionally studying the congeneric Ropalidia cyathiformis, but only to understand R. marginata better.

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Ropalidia marginata.

IS: What is the best moment/discovery in your research so far? What made it so memorable?

The discovery of behavioural caste differentiation into Sitters, Fighters and Foragers through the use of multivariate statistical analysis of quantitative behavioural data, in the early 1980’s remains, to this day the most exciting and memorable moment. Several factors have contributed to the special status of this early work. It was my first scientific discovery outside of molecular biology, it was made entirely by following my instincts rather than by following the literature and it has remained the starting point for almost everything I have done since.

IS: If teaching is part of your work, what courses do you teach? Has your work on social insects helped to shape your teaching?

RG: I teach courses in evolutionary biology, behavioural ecology, sociobiology and organismal biology to doctoral, masters and undergraduate students. During the last five years my undergraduate students regularly perform field and laboratory experiments with ants, bees and wasps.

IS: What is the last book you read? Would you recommend it? Why or why not?

RG: The most recent book I have read is “Half-Earth: Our Planet’s Fight for Life” by EO Wilson. I would strongly recommend it to any and all persons. It is a remarkably well-written and passionate plea to treat the planet responsibly. Besides, it is brimming with the most recent scientific discoveries, described in Wilson’s inimitable style and laced with Wilson’s priceless wisdom.

IS: Did any one book have a major influence in shaping your career? What was the book and how did it affect you?

RG: Two books that I read as a first-year undergraduate changed my life: King Solomon’s Ring by Konrad Lorenz and The Double Helix by James Watson. Both books described great science but their real magic came from the fact that they described the process of doing science.

IS: Outside of science, what are your favourite activities, hobbies or sports?

RG: When I was doing molecular biology, watching wasps was my hobby. When watching wasps became my profession, I needed a new serious hobby, besides reading book and watching movies. My new hobby is to break the boundaries of scholarship and bring together the natural sciences, social sciences, humanities and arts, both in research and in teaching.

IS: How do you keep going when things get tough?

RG: Just keep going – there is no other way! My science itself is a hobby so that things never really get that tough.

IS: If you were to go live on an uninhabited island and could only bring three things, what would you bring? Why?

RG:  The answer to this depends on where the island is located and how long I would have to be there. Besides, today, this question has become a bit trivial – most people on the planet would say: “my smartphone is enough”. That would be my first choice with or without internet, as long as I can power it with batteries. I am not that much of a field biologist and my passion is more in watching than in catching. I suspect that I could spend endless time watching all kinds of animals, especially insects for which I need almost nothing.

IS: Who do you think has had the greatest influence on your science career?

RG:  My science teacher in sixth grade inspired me to become a scientist, my biology teacher in 8th grade inspired me to become a biologist, WD Hamilton and EO Wilson have been my role models.

IS: What advice would you give to a young person hoping to be a social insect researcher in the future?

RG: The same advice that I would give to any young researcher hoping to do any kind of science – avoid fashions and try to do something original and creative and minimize your dependence on what is hard to get (funding, equipment or whatever is hard to get). In the context of social insect research today this translates into studying behaviour in the field.

Invasive Social Wasps

Highlighting the article written by T. Takeuchi, R. Takahashi, T. Kyoshi, M. Nakamura, Y. Minoshima, J.-I. Takahashi in Insectes Sociaux

Written by Insectes Sociaux Editor-in-Chief, Michael Breed

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Vespa velutina attacking a honey bee. Photo: Danel Solabarriela/flickr

In this issue of Insectes Sociaux, Takeuchi and colleagues reveal the genetic origins of an invasive population of Vespa velutina (the yellow-legged hornet) in the western islands of Japan. This invasive wasp is a predator on the honey bee species Apis cerana in its native range and can prey on Apis mellifera outside of its normal range (Monceau et al 2013). Native to the southern part of Asia and to Indonesia, it has also been introduced into Korea and Europe. They use mitochondrial DNA sequences to generate a cladogram for populations of this wasp and are also able to draw conclusions about genetic variation in the invasive population in Japan. Genetic variation may support the phenotypic flexibility exhibited by some invasives and consequently it is an important feature to characterize in invasive populations.

The role of social insects, such as this hornet, as biologically invasive species is well known, principally because of the prominence of invasive ants through the last 100 years in ecological studies and their creation of important issues in public health and agriculture. The numerous exemplars of high-impact invasive ants include the red imported fire ant, Solenopsis invicta, the pharaoh ant, Monomorium pharaonis and the Argentine ant, Linepithema humile. The Formosan termite, Coptotermes formosanus, is a major pest in many habitats.   The western honeybee, Apis mellifera, is invasive throughout the Americas, first as an introduction by European colonialists on the east coast of North America in the 1600s, and then by the introduction of a more aggressive form in the 1950s in Brazil.

In some cases invasive social insects, such as the fire ant and the Argentine ant, are perceived to have essentially overrun an entire ecosystem. These species cause massive shifts in the terrestrial invertebrate fauna, impact the reproductive success of ground nesting birds, and have ripple effects on other trophic levels. However, many social insect invasions occur quietly and go largely unnoticed because the ecological impacts of the invasion are subtle and there are no apparent public health or agricultural implications of the invasion. Whether the impacts are large or small, understanding the processes of biological invasions is a key question in evolution, ecology and behavior.

What makes some social insects such effective invasive species? Ecological flexibility, high reproductive rates, and ability to disperse within the landscape all must be important factors. But many populations of invasive species, social insect or otherwise, survive very narrow genetic bottlenecks. Introductions of species to new areas often involve the transport (typically by humans) of a very small number of individuals or colonies. This may translate into invasive populations with low genetic diversity.

Takeuchi et al (2017) sequenced three mitochondrial genes, COI, Cytb, and 16S rRNA, from samples of V. velutina collected across its natural range, plus invasive populations in Japan and Korea. Their results show that this species is likely monophyletic, but that there are two relatively distinct geographical clades, one in Indonesia and Malaysia, the other more broadly distributed in continental Asia. The invasive Korean population nests within the populations from China, and the invasive Japanese population probably derives from the geographically nearby Korean population.

Significantly, Takeuchi et al (2017) found no genetic variation in these genes in the Japanese population. While their finding is unusually low, even for an invasive that has gone through a genetic bottleneck, it is by no means out of the ordinary to observe invasive social insect populations that derive from a few individuals or a few colonies. In the case of V. velutina, Takeuchi et al. (2017) argue that fertilized queens could easily be carried along in goods transported by humans and that, in a practical approach to regulation of invasions, vigilance for fertilized queens might be useful. It would be very interesting to compare the social flexibility and ecological adaptability of the Japanese population of V. velutina with Chinese populations to see if these features have been affected by the bottleneck.

These findings raise the very interesting question of how invasive social insects are able to retain ecological and social flexibility, keys to being successful invasive species, through periods of small population size. Mechanisms for carrying characteristics that are key to invasiveness through a bottleneck could include having multiple queens in colonies mating more than once, plasticity in phenotypic expression, or rapid evolution of genetic diversity via mutation. Each of these strategies could be effective, and future work building on approaches like those of Takeuchi et al (2017) should help to explain the properties that make some social insects such effective invasive species.

 

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Vespa velutina, the yellow-legged hornet. Photo: Danel Solabarriela/flickr

References

Monceau K, Arca M, Leprêtre L, Mougel F, Bonnard O, Silvain J-F, et al. (2013) Native Prey and Invasive Predator Patterns of Foraging Activity: The Case of the Yellow-Legged Hornet Predation at European Honeybee Hives. PLoS ONE 8(6): e66492. https://doi.org/10.1371/journal.pone.0066492

Takeuchi T, Takahashi R, Kyoshi T, Nakamura M, Minoshima Y, Takahashi J-I. (2017) The origin and genetic diversity of the yellow-legged hornet, Vespa velutina introduced in Japan. Insect Soc DOI: 10.1007/s00040-017-0545-z

 

Unexpected stop signaling in a foraging honey bee colony

A blog post highlighting the article by  P. M. Kietzman, P. K. Visscher, J. K. Lalor in Insectes Sociaux

By Parry Macdonald Kietzman

The remarkable system of communication used by honey bees to coordinate their daily activities is well known, though most people are primarily aware of the waggle dance. This positive feedback signal is one that communicates the distance and direction of some item of interest, most commonly a food source, to a worker bee’s nestmates. Perhaps less well-known is the stop signal, an acoustic negative feedback signal that can be used as a counter to the waggle dance, inhibiting recruitment and decreasing foraging (reviewed in Kietzman and Visscher 2015).

One use of the stop signal occurs when foragers encounter danger, such as an attack from other bees or a predator, at a food source (Nieh 2010). Nieh (2010) simulated such attacks at a feeding station by pinching foragers’ legs with forceps. Back at the hive, these foragers were then much more likely to use the stop signal on other bees advertising that same location with the waggle dance than they were on dancers advertising other food sources.

parry

Parry observing the honey bee dance floor in her two-frame observation hive.

Our experiment was originally intended as a pilot study with the goal of practicing a method similar to Nieh’s (2010) technique of pinching bees’ hind femurs during their visits to a feeding station so that we could then use that technique in a later study. We established a colony of bees in a two-frame observation hive (1/4 or 1/5 a regular-sized hive with observation windows on the sides) on the premises of the University of California, Riverside’s Agricultural Operations. We trained the bees to visit a feeding station baited with sugar water 100m away from the hive, and an observer there gently caught visiting foragers in a small net and marked them on the thorax with one of two colors of paint pen depending on which treatment they received.

Using a coin toss to help randomize the treatments, approximately half the visiting foragers were “attacked” with a pinch to the hind femur and the other half were not. I watched the marked bees’ waggle dances back at the hive and recorded them using an HD video camera. A detailed analysis of the video recordings revealed that bees that had not been pinched at the feeder performed significantly more and longer waggle dances than the bees that had been pinched. Additionally, the pinched bees produced significantly more stop signals upon their return to the hive than the unpinched bees.

These results were very much in line with what we expected based on Nieh’s (2010) findings, however, we also made the surprising observation that most of the stop signals we recorded—about 70%–were performed by unmarked bees that had probably never visited the feeding station at all.

Though we don’t have a definitive answer for why so many unmarked bees used the stop signal on dancers advertising the feeding station, there are a few possible explanations. One is that the unmarked bees may have been foraging at another location and were not promptly unloaded upon their return to the hive because the unloader bees were overwhelmed by the influx of food coming from the feeding station. Stop signaling has often been found to increase when the bees have access to a feeding station (reviewed in Kietzman and Visscher 2015), and most of this stop signaling is produced by tremble dancers. Foragers perform the tremble dance when they are not unloaded quickly (Seeley 1992), so if there were insufficient unloader bees available due to the large amount of food coming from the feeding station then this could account for the stop signaling performed by unmarked bees.

A second explanation is that the stop signalers could have been unloader bees rather than foragers, and that these bees were using the stop signal in an attempt to decrease what had become an unmanageable number of foragers exploiting the feeding station. This use of the stop signal, while plausible, has not yet been measured and would likely be an interesting and productive area of study.

Finally, a rich, unlimited source of food such as a feeding station can readily be compared to hive robbing rather than typical foraging on flowers. Johnson and Nieh (2010) modeled a robbing event and showed that the stop signal could successfully be used to quickly shut it down, which would be beneficial if the robbed hive were very strong and an excessive number of robbing foragers were being killed. It is possible that the pinched bees from our experiment were emitting alarm pheromone (signaling a threat to the other bees), and that other bees in the colony interpreted this as evidence that they had been present during a robbing situation. If this were the case, the stop signaling we observed could have been an attempt to shut down what was perceived as an unfavorable robbing event.

Clearly, we have yet to decipher all the meanings of what is a versatile and effective communication signal.

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Photo: Rachael Bonoan/flickr

 

References

Johnson, BR and Nieh, JC. 2010. Modeling the adaptive role of negative signaling in honey bee intraspecific competition. Journal of Insect Behavior 23: 459-471.

Kietzman, PM and Visscher, PK. 2015. The anti-waggle dance: use of the stop signal as negative feedback. Frontiers in Ecology and Evolution 3: 54-58.

Nieh, JC. 2010. A negative feedback signal that is triggered by peril curbs honey bee recruitment. Current Biology 20: 310-315.

Seeley, TD. 1992. The tremble dance of the honey bee: messages and meanings. Behavioral Ecology and Sociobiology 31: 375-383.

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

Figure 1: observing waggle dances and stop signals.

The smell of a brand new house

A blog post highlighting the article by M.F. Torres and A. Sanchez in Insectes Sociaux

By María Fernanda Torres

Perhaps one of the most astonishing features of ants is their ability to establish mutualistic associations with plants, myrmecophyte plants in particular. About 110 ant species nest exclusively inside hollow structures in leaves, stems or roots the host plant produces (Chomicki and Renner 2015). The mutualism is beneficial for the ants because the host plant provides the colony with housing and food. This food can be obtained directly from the plant or honeydew secreted from the ant-tended hemipterans living on the plant. For the plant, hosting an ant colony is comparable to having its own defense army for a lower cost than producing extensive chemical defenses.

For both members of a mutualism, identifying and locating (or attracting) the right partner is a crucial step in the establishment of the mutualism. Fertile founding queens (alates) emerge from the colony and, after the nuptial flight, they start their quest for a host for her new colony. Finding a place as fast as possible contributes to the survival of the both queens and host plants. For the ant queen, flying towards the wrong plant species or finding a colony already occupying a host translates into wasted energy and increased competition.

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Alate P. mordax queens running away from the researchers after a branch was cut open. Photo: M.F. Torres

So, how do plants advertise available spaces to the founding queens, especially when host plants are dispersed over large areas? What signals are queens recognising? Communication between plants and ants is mostly mediated by volatile chemical compounds (Heil and McKey 2003; Edwards et al. 2006). In our study, we wanted to test if the plant chemical signals that attract ant queens vary depending on the plant’s developmental stage and if queens respond to such variation. Every new generation of founding queens must be capable of distinguishing the most suitable available host from a pool of hundreds of other plants across large distances. It is a question of survival for both ants and hosts, requiring that the mechanisms of recognition and attraction are precise and informative to be successful.

To help us understand ant-plant communication, we studied Pseudomyrmex mordax queens to test their preferences between young and mature leaves or seedling and adult Triplaris americana plants. Pseudomyrmex is a genus of ants restricted to the Neotropics. Some species of the aggressive Pseudomyrmex nest inside myrmecophyte plants like Acacia, Cordia, Tachigali, and Triplaris, (Ward 1991, 1999) and tend coccids (Hemiptera) to obtain sugar. To survive, P. mordax must form a mutualism with T. americana and it is such a good guardian that has made Triplaris earn the name of “vara santa” (or holy rod) as the colony members will painfully sting however comes into the plant’s proximity.

P. mordax

P. mordax worker patrolling T. americana flowers. Photo: M.F. Torres

study site

Location of Guamo, Tolima-Colombia, where we performed the experiments.

For the experiments, we collected young and mature leaves from both seedling and adult T. americana trees from a population in Colombia. We also collected alate P. mordax queens from the branches of nearby T. americana trees that were not used for the experiment (as we were subject of the ants’ aggressiveness). In an experiment conducted in the field, we placed the leaves of the young and mature T. americana on opposite sides of a two-sided olfactometer and recorded the time each queen spent on each side. We also performed the experiment leaving one of the sides empty as a control. We then compared the differences between the time on each side across all the queens used in the experiment to establish whether the young ant queens had a significant preference for a particular leaf age or plant age.

We found that while queens do not show a preference for young and mature leaves from the same plant, they do prefer leaves from T. americana seedlings over adults. Queens also spent more time in the arm of the olfactometer containing T. americana leaves when the other arm was left empty. Our findings show that P. mordax queens are attracted by volatile chemical compounds produced by T. americana and discriminate signals produced by its seedlings from other signals. The ability to distinguish between plant development stages, along with the use of chemical cues to find a mutualist plant partner increases the chances of a queen’s survival. For the seedling, the ant queen and her future colony provide early protection against herbivores and competition by pruning competing plants, enhancing seedling survivorship. Knowing the age of plant that the queens prefer is only one part of the story. Comparing the relative abundance of the chemical volatiles from each type of leaf will provide more information about how the plant uses odors to signal the queen to her new home.

References

Chomicki G, Renner SS (2015) Phylogenetics and molecular clocks reveal the repeated evolution of ant‐plants after the late Miocene in Africa and the early Miocene in Australasia and the Neotropics. New Phytol 207(2):411-424

Edwards DP, Hassall M, Sutherland WJ, Yu DW (2006) Assembling a mutualism: ant symbionts locate their host plants by detecting volatile chemicals. Insect Soc 53:172–176

Heil M, McKey D (2003) Protective ant-plant interactions as model systems in ecological and evolutionary research. Annu Rev Ecol Evol S 34:425–553

Ward PS (1991) Phylogenetic analysis of Pseudomyrmecine ants associated with domatia-bearing plants. In: Huxley CR, Cutler DF (eds) Ant-plant interactions. Oxford University Press, Oxford, pp 335–352

Ward PS (1999) Systematics, biogeography and host plant associations of the Pseudomyrmex viduus group (Hymenoptera: Formicidae), Triplaris– and Tachigali-inhabiting ants. Zool J Linn Soc 126:451–540