Mainland fieldwork tales: of ants, earthquake, and fish cake

Guest post by PhD student Gaurav Agavekar.

One of the things I like about my PhD work is that I get to do a little bit of everything: fieldwork, molecular lab work, and bioinformatics. This helps keep monotony at bay and supplies a variety of interesting problems to solve. Although I like switching back and forth between these tasks, I probably enjoy fieldwork the most. Unfortunately, due to the pandemic, I haven’t had much of an opportunity to conduct fieldwork outside of Okinawa. Now that things are getting better pandemic-wise, I jumped on the opportunity to collect ants in mainland Japan.

Meeting the myrmecology legends in Japan
The week before last, lab technician Fumika Azuma and I embarked on a small field expedition to Manazuru forests in Kanagawa Prefecture, just south of Tokyo. My main goal was to collect some Strumigenys hexamera colonies, an Asian species without the iconic trap-jaw mandibles, but rather having the ancestral “gripping” mandibles. It’s known to reproduce parthenogenetically, which is why I wish to establish its colonies in the lab for our Strumigenys comparative genomics work. I was also hoping to collect some species that would serve as outgroups for this project, especially those not found in Okinawa. 

Although S. hexamera occurs in Okinawa, I haven’t had luck so far in collecting this rather cryptic, soil-dwelling species. I thus reached out to Dr Keiichi Masuko, who I knew had collected it in the past, to seek advice for where I could collect some colonies. He generously offered to help us and tremendously facilitated the trip. Keiichi, a senior professor at the Senshu University, has been studying Strumigenys ants since before I was born! I was thus delighted to have an opportunity to discuss Strumigenys biology with him; over the years, he has made tons of interesting ecological and natural history observations on this fascinating group of ants, among others. Although Keiichi couldn’t join us in the field, he graciously requested Dr Mamoru Terayama to accompany us, who in turn obliged. Mamoru is a now-retired professor, who has vast experience in the systematics and taxonomy of Japanese ants and wasps. I was thrilled to be collecting ants with and visiting such giants in the Japanese myrmecology community.

Strumigenys hexamera, our target species for this trip. (Photo by Mari,

Fieldwork at Manazuru forests in Kanagawa
Boarding the blazing-fast Shinkansen train at Tokyo, we headed to Cape Manazuru, a 30-min drive south of the small city of Odawara in central Japan. Along the way to the cape is a forest patch of moderate size with trails built for adventurous citizens. Although the trails are rather short and not difficult to walk, the forest supports several species of evergreen trees that are quite huge in size. “The trees are at least 300 years old”, I was told by Keiichi. The difference in forests between mainland Japan and Okinawa was stark—the latter, although being more diverse, typically lacks such huge old growth trees because of widespread deforestation and frequent typhoons. The broadleaf evergreen trees in Manazuru forests are primarily camphor, black pine, Itaaji chinkapin, and cane.

Fumika Azuma (left) and I with Mamoru Terayama, at the end of our first day in the field.

The soil arthropod community of the Manazuru forest is rich and abundant. As soon as we began searching, we found several colonies of CarebaraNylanderia, and Hypoponera, the usual suspects in the ant world. Keiichi had told me that S hexamera nests ~10-20cm deep in the soil. It creates tunnels inside the soil and feeds on the abundant soil arthropods of the forest. Although I had never dug this deep before while looking for Strumigenys, and had mainly been focusing on taking apart rotten logs and flipping rocks, I quickly realized what kind of soil Keiichi was talking about. After digging through 10-15cm of loose soil, I began to find large soil lumps that had clay-like consistency. This type of soil seems ideal for the ants to make tunnels and create compartments to house their brood. Sure enough, within the first hour of beginning fieldwork, I found my first Strumigenys colony. Because Strumigenys species are rather tricky to identify in the field if you haven’t collected them before, I showed it to Mamoru, who immediately confirmed its identity as S hexamera. How exciting! Another highlight of the day included a Discothyrea sauteri colony, which unfortunately only had a queen and one worker, so raising this colony is probably going to be a challenge, not to mention their peculiar diet of arthropod eggs.

The next day we continued our efforts to find more Strumigenys colonies. We succeeded in collecting 5 more colonies, which included S canina and S incerta, neither of which I had collected before. We collected a bunch of other colonies, including a Myrmecina nipponica and Cryptopone sauteri, which might prove useful outgroups. We also collected a worker of Stigmatomma silvestrii, but unfortunately couldn’t locate the colony.

Meeting the members of the Myrmecological Society of Japan
Besides meeting Keiichi and Mamoru, we also had the great fortune of having dinner with Dr M Kondoh, the 87-year-old co-founder and current president of the Myrmecological Society of Japan. Dr Yamaguchi, a member of the Society, and his wife, both residing in Odawara, also joined us for the dinner.

Back row: Keiichi Masuko, M Kondoh, me, Fumika. Front row: Mr & Mrs Yamaguchi and Mamoru Terayama. Odawara’s famous Kamaboko fish cake on the right.

It was wonderful to get plugged into the Japanese myrmecologists community and hear stories about their work. The izakaya served a menagerie of delicious food, complete with Kamaboko fish cake, for which Odawara is famous in Japan. All in all, we had a great and productive time in the mainland. Besides these wonderful memories, the M6.1 earthquake I experienced in Tokyo will remain unforgettable. This was the most intense earthquake I have ever experienced and being on the 10th floor didn’t help either. Thankfully there was no tsunami or any damage from the earthquake, but those few seconds were unarguably the scariest of my life. Now back to the lab sorting those ant colonies…

We collected 6 Strumigenys colonies in total and managed to collect one colony of S hexamera. Here they are in their artificial lab nest.

All about those mandibles

One of the most striking features of ant diversity is the sheer variety and ingenuity of mandibles. Mandibles are a primary way that ants interact with the world, and are used as diverse tools for many tasks and purposes.  Ant mandibles are cutters and carriers, but also trap-jaws, snap-jaws, millipede shavers, seed millers, wood borers, and beyond.  There are truly a huge number of mandible shapes and functions to explore from ecological, evolutionary, biomechanical, and developmental perspectives.  We have a number of projects with collaborators ongoing about these interesting structures, here’s a little tour:

First up here’s a broad look at the diversity of ant mandibles, segmented from micro-CT scans by our PhD student Julian Katzke.  Julian is doing his thesis surveying the diversity of mandibles, building a massive dataset across the tree of life, and analyzing their evolution.  How many morphotypes are there, how many times have they evolved?  Are there macroevolutionary pathways for their evolution (i.e. certain shapes tending to evolve into other shapes)?  Julian is working on it.

ant mandible diversity visualized by Julian Katzke

A related topic is the structure of the muscles inside the head and its supporting endoskeleton. In scanning ants, we have found there is at least as much diversity in these structures inside the head as the mandible outside. Julian is working on analyzing that too.

The mandibles are supported and controlled by endoskeleton and muscle inside the head-image by Julian Katzke

Within that diversity, there are some really interesting innovations and adaptations. A major project in the lab in the past years is the evolution of Strumigenys trap jaw ants.  Strumigenys are a globally distributed, hyperdiverse group with a variety of mandible types. 

Booher et al. 2021 PLoS Biology (Plos Biology cover based on original image from J. Katzke)

We found the trap-jaw mechanism has evolved between 7-10 times, and identified functional stepping stones that could explain how it may have evolved.  Read the paper (Booher et al. 2021, PLoS Biology) and see Evan’s twitter thread to dig into this more.

Tracing the parallel evolution of short and long form trap-jaw mandibles in Strumigenys (Booher et al. 2021, PLoS Biology)

PhD student Gaurav Agavekar is following this up by investigating the genomic and developmental basis of this convergent evolution.

Another recent collaborative study focused on the wood-boring ant, Melissotarsus, the only ant to live completely in tunnels it carves in living wood, and one of the wildest ants out there. We found a number of adaptations to help chew through living wood, including changes to head musculature and interesting conical mandibles. This study was led by Adam Khalife and the late Christian Peeters, was published in Frontiers in Zoology

Melissotarsus head and mandibles adapted for boring through living wood (Khalife et al. 2018)

And there are other mysterious species, such as Protanilla lini which has a very odd mandibular articulation with the head.  Some think it may have a power-amplifying function, however this is still unclear.  We recently looked at this species in a study led by Adrian Richter in collaboration of our lab.  Julian made an animation of head movement to try to understand it.

3D model of a Protanilla lini head and mandible articulation, from Richter et al. 2021, image by J. Katzke

Aside from these more exotic examples, we still lack a basic understanding of what axes of morphological and functional variation underlie normal triangular mandibles.  How does shape vary with ecology and performance?  Two recent studies help shed light on this.  

First, our now postdoc Ale Casadei-Ferreira and colleagues analyzed ecology-mandible correlations and integration in the evolution of mandibles and head shape, focusing on Pheidole majors and minors.

Pheidole major and minor worker mandible and head shape variation (from Casadei-Ferreira et al. 2021).

Second, Christian Klunk and colleagues used finite element analysis to analyze Pheidole mandibles, helping to understand how different mandible shapes reflect tradeoffs in force vs. speed, and how stress moves through the mandible shapes.

Force and stress in ant mandibles, from Klunk et al. 2021 J. Roy. Soc. Int.

For more general discussion of the mandibles in context of the head, recent papers by Adrian Richter and various collaborators surveying the head anatomy of different ants are a must-read.

Of course there is lots of other great work going on out there by other labs, for example a terrific recent study by David Labonte’s lab on bite force allometries in Atta leafcutter ants.

There’s much more to come from our lab and others on the morphology, functional ecology, evolution, and development of these diverse tools ants use to interact with the world.

[New Paper] Regular is irregular? Seeking for theoretical understanding of the role of complex landscape in driving biodiversity

Our new paper From species sorting to mass effects: spatial network structure mediates the shift between metacommunity archetypes published in Ecography explores the role of landscape structure in driving biodiversity. Landscape structure becomes important when organisms of interest have ability to move from one place to another, from insects, plants, and animals on terrestrial habitats to marine organisms.

How species are distributed in landscape – how many species inhabit where – and what processes determine the distribution is a big question. Especially, when a large space is considered, this question becomes more complicated, because we need to consider a wider variety of environment and how species distribution differs between places, in addition to the total number of species coexisting, both of which further affect the processes of generating and maintaining biodiversity.

It sounds reasonable to assume simple and regular landscape structures as the first step of exploring the role of spatial structure in ecosystems, expecting that such assumptions would output biodiversity patterns that is average across many different landscape structures. Thus, many theoretical studies addressed this question based on the simple and regular landscape assumption. However, what we found is that such simple and regular assumption generates rather extreme outputs. Check out the paper and find out more details about how this new theory bridges different metacommunity archetypes (species-sorting and mass-effect) and how landscape structure affects the transition between the two archetypes, which then determines what biodiversity patterns emerge.

Yuka Suzuki, PhD Student

New study on some mysterious Pheidole

If you look hard enough in the field, you are guaranteed to uncover cool stuff.  Such is the case in Madagascar, where Brian Fisher and colleagues have been surveying the island intensively for 20+ years, uncovering a huge and mostly endemic ant fauna.  Georg Fischer has been working for some years on the collections of Malagasy Pheidole, and, in the process found something very strange.  There is an extremely rare, and unusual group of social parasites with workers that seem to look like their hosts.  Working with Sasha Mikheyev’s lab and other colleagues, we found they belong to a single clade, a mini-radiation of parasites within the broader endemic Malagasy radiation, rather than (as is typical) each parasite being closely related to their host.  Using micro-CT and a comparative analysis (led by Nick Friedman), we found they have evolved size and shape to match their hosts.  Parasites more generally evolve to resemble their hosts because they aim to fool predators (Batesian mimicry) or they aim to fool the hosts themselves (Wasmannian mimicry).  It is hard to invoke Batesian mimicry here, which leaves Wasmannian as the putative mechanism, and this is not known for ants that parasitize other ants (although is known for other insects like beetles to parasitize ants).  If true, it implies ants may sense morphology to some degree to distinguish friend from foe, and these abilities are very sensitive.   There are other potential explanations too, as we discuss in the paper, just out in Current Biology. This is definitely a study that raises as many questions as answers, hopefully it will inspire some follow up experiments.

Birds have beaks that are a compromise of many functions

Birds use their beaks for foraging, but also for regulating their temperature, singing and a variety of other functions. Do beaks and other multifunctional traits have characteristics that are specialized for each function, or are they an evolutionary compromise? To test this, we examined beak shape and size in a family of Australian songbirds, and compared the influence of each function on the evolution of species differences. We found that foraging behaviour and climate both have an effect on the evolution of bird beaks and their characteristics, and that this also affects features of the songs these birds perform.

Read the paper led by Nick here.
Read the article OIST published on this paper: English / Japanese.

Listen to the call of Philemon corniculatus (commonly known as the Noisy Friarbird) below!