Other army ant symbionts

Since 2008, I have studied arthropods that are associated with ants - so called 'myrmecophiles' (deriving from Greek: ‘myrmex’ = ant; ‘philos’ = loving). More specifically, I study myrmecophiles of army ants, which are host to a particularly diverse fauna of such symbiotic arthropods. For example, several hundred animal species are obligate associates of the infamous swarm-raiding army ant Eciton burchellii (Westwood, 1842), representing one of the largest-known species assemblages centered on a single animal species. This faunistic diversity entailed many problems of species identification, so much so that I regularly came across major deficiencies in the taxonomy and naming of myrmecophile species. This is the reason why I started to get involved in taxonomic work and why I realized that a revision of the genus Vatesus is urgently needed. 

Myrmecophiles search for close contact with ants. As a social insects, however, ants are rarely alone and cooperating ant workers fiercely defend colony resources against any animal trying to sneak into their nest. This implies serious problems to myrmecophiles. A successful invasion of an ant society offers access to plentiful resources but always at the risk of being detected and killed. To avoid the latter myrmecophiles have evolved adaptations in anatomy, behavior, chemistry - which is why there are so many cool critters among them. In the following I will introduce some myrmecophile species and their adaptations to the life with ants. They have amazed me in the last couple of years and I hope I can transfer some of the fascination in the following chunks of myrmecophile stories.

Acquisition of chemical recognition cues - The video above by P. Hönle shows ant-shaped staphylinid beetles in a laboratory nest setup of Eciton burchellii foreli. These beetles not only mimic ant workers visually, but also smell like workers. Through chemical mimicry of ant nestmate recognition cues (cuticular hydrocarbons, CHCs) these myrmecophiles lower the risk of being detected as intruders. Chemical mimicry is an ubiquitous strategy among myrmecophiles. To acquire the cuticular hydrocarbons from ant workers many myrmecophiles intensivley groom ant workers, either with their mouth (see above) or with their legs (see spider Sicariomorpha maschwitzi below). Others like silverfish specimens (species Malayatelura ponerophilarub their entire body intensively on ant workers. The spider and silverfish are myrmecophiles of the Southeast Asian ponerine army ant Leptogenys distinguenda.  

Video at the right: Another nice video by P. Hönle showing a specimen of the histerid beetle Euxenister wheeleri grooming intensively on an injured major worker of Eciton hamatum in a laboratory nest. With an artficial, deuterium-labeled hydrocarbon that we transferred to host workers, we were able to show that the great majority of Eciton myrmecophiles acquired the CHC label, indicating that they generally acquire host CHCs via physical host contact  (unpublished data; but see here). This individual stayed for a while in close contact to the major not stopping to rub its legs on the major worker and itself. During emigrations, these beetles can run themselves but are often attached on the underside of workers in an upside down position like partly in this video (see here).  

©  Brant Backlund

see full movie here

The cowboy beetle - The discovery of the "cowboy beetle" - one among many funny names for the beetle Nymphister kronaueri invented by journalists and bloggers - made quite some press in 2017 and 2018 and it was finally voted to be among the top ten new species discoveries in 2018. In 2014 Daniel Kronauer and me discovered this little beetle during an emigration of its host ant Eciton mexicanum at La Selva Biological Station in Costa Rica. We first realized that some ants had weird looking gasters (the abdomen of ants), because they were darker and reflected the light of our headlights differently. We collected a few individuals with our aspirators (see video how we do this here) and were surprised that it looked like the ants had two gasters. I knew phoretic mites that sometimes attach to ant gasters and therefore shook the vial to see whether the "mite" detaches. The creature indeed detached and to our great surprise legs and antennae extended from the little brownish ball. I still remember how both of us were thrilled at this moment. These are the moments of why being a naturalist in the tropics is so gainful - there are surprises and new discoveries in each field trip to the tropics.

It was Alexey Tishechkin, a taxonomic expert of the beetle family Histeridae, who instantly realized that this is a new species with a remarkable and exceptional mechanism of phoresy. Phoresy means passive transport in which one organism travels on the body of another organism - thus saving energy. Like other army ants, the host species of this beetle Eciton mexicanum is nomadic, i.e. colonies frequently move to a new nesting site. Myrmecophiles exploiting army ant societies thus need to track their host colonies during these frequent colony emigrations. Many associated arthropods follow host colonies during the frequent colony emigrations by following the ants’ pheromone trail on foot (e.g. Vatesus beetles) or by attaching to ants or the brood/prey being carried by ants (e.g. many ptiliid beetles including Cephaloplectus mus). The new beetle species achieves to follow its host ants during emigrations by using a highly specific and fascinating mechanism: it attaches to the trunk between the ants’ thorax and abdomen using its long mandibles as gripping pliers. Eciton-associated arthropods have been studied extensively by several generations of researchers. Despite these enduring efforts to document army ant parasite diversity a large proportion of unknown biodiversity still exists today. In the beetle subfamily Haeteriinae, for example, the number of undescribed species can be estimated to be between 1-2 times the number of described species. New species discoveries are therefore not surprising. However, the new histerid is a very conspicuous new species, and it is indeed surprising for us that it had been overlooked previously. I think army ant-symbiont communities other than those of the most prominent host ants, E. burchellii and E. hamatum, have not been as intensively studied, and thus I think many more species with fascinating adaptations still await scientific discovery. See below some photographs of attached N. kroanueri beetles and a photo of the holotype. To find out more check out our article in BMC Zoology.

© D. Kronauer

© D. Kronauer

© D. Kronauer

© M. Maruyama

© M. Maruyama

Here is a fun video showing the cowboy beetle N. kronaueri mounting an Eciton mexicanum worker in a laboratory nest. Apparently, the worker dislikes it. Note that other army ant workers started to lick the cowboy beetle's abdomen, indicating that appeasing chemical compounds are involved in social integration. The video was taken by Philipp Hönle.

Snails catching a ride- The work on organism that associate with ants is full of surprises and adaptations to this lifestyle  are divers and sometimes more than surprising. You can imagine how weird it must have been for my PhD supervisor Volker Witte when he discovered that a snail participated in colony emigrations of the Southeast Asian army ant Leptogenys distinguenda (for species status of L. distinguenda see here). I was enthused when Volker showed me this astonishing ant guests - snails of the species Allopeas myrmekophilos Janssen & Witte 2002. The number of snails per colony emigration was low, ranging from no snails to nine snails. In a single exceptional event we found more than 20 snails. It took some practice to distinguish the snails from workers carrying larvae and I am sure I missed some snails in the first emigrations I collected myrmecophiles from. We kept some snails in laboratory nests and discovered that they feed on army ant booty as well as on army ant brood. When workers got excited in laboratory nests snails started to produce a foam that was attractive to workers, who finally picked up snails and transported them to the new bivouac site. One hypothesis that I wanted to test during my PhD thesis was that they produce a chemical compound that mimic larval pheromones of host ants. Unfortunately, we did not discover any chemical compound in hexane nor in methanol extractions of the foam, which we analyzed with a GCMS. Neither did we uncover a larval pheromone. The snails' attractiveness to the ants might also be caused by a protein or another rather volatile compound that we did not detect with our methods. It would be thrilling to go back to Malaysia at some point to solve this mystery. The snails also carry relatively large eggs in the lower part of their shell and we kept a few laid eggs till they hatched from the eggs, which took about 20-28 days. We never saw any aggressive behavior of ants towards snails (see here). It would surely be worth to study these exceptional myrmecophiles in more detail. 

©  Brant Backlund

see full movie here

Parasitoid mites hidden in pupal cocoons- Only a lucky coincidence led to the recent description of two new mite species that parasitize army ants. In 2008 I inspected alcohol samples of brood of Leptogenys army ants to search for immature stages of myrmecophiles. I did not find any immatures, but my efforts were nonetheless rewarded.  I saw large black bulbs inside of pupal cocoons (see right image), then opened the silk cover and found a beautiful, huge uropodine mite inside. I was thrilled and immediately  ran to the office of my PhD supervisor Volker, who was, I think, happy to leave his desk and rather look at some specimens under the microscope. "Wow, cool discovery" he said. 

Apparently the uropodine mites fed on the ant pupae, because the developing pupae looked nonviable (see images below). I was not able to identify the species myself and therefore decided to send specimens to several taxonomic experts. And this could have been the end of the story...and here comes the lucky part:

I got an e-mail from one of my new colleagues at Darmstadt, Adrian Brückner, in June 2016 from Ohio where he participated in the Acarology summer school with the following attachment:

And here it was back on the table again. Adrian came back from the summer school and decided we should describe this beautiful species - and that's what we did together with Hans Klompen -  a taxonomic expert of this mite group (see article here; and a blog about the discovery by Adrian here). It turned out that we actually discovered two distinct species, both parasitoids that fulfilled their entire development by sucking hemolymph of developing Leptogenys distinguenda pupae. I should note here that it was a bit tricky to decide whether the mites should be defined as parasites or parasitoids because they are associated with a social insect host. When host colonies are considered a superorganism - killing a few developing ant worker is more like loosing a few "cells" in an organism - so some authors would rather define them as parasites. Anyhow, I hope you now enjoy the beauty of the mites and please note their destructiveness exemplified by two infected pupae.

The photos show ant pupae (cocoon removed) of L. distinguenda and deutonymphs of Macrodinychus hilpertae. The ant specimens with mites removed expose the abnormal intrusion in the ants’ gasters and the brownish feeding scars. Larval exuviae of M. hilpertae are still sticking to the ants (dashed squares), showing that the whole development of the mites take place inside the pupal cocoon. In fact we found exuviae of all development stages inside the cocoons. Other Macrodinychus species have a quite similar lifestyle. Check out the nice article of Lachaud et al. (2016). Ant pupae with adult Macrodinychus specimens enclosed showed an even larger intrusion and clearly appeared to be nonviable. 

And finally here they are the two beauties. Left is Macrodinychus hilpertae, which we named after Andrea Hilpert for her advice, long lasting skillful technical assistance and support of Adrian and me. Right is Macrodinychus derbyensis referring to the fact that both new species co-occur in the same host species. Furthermore, we picked this name to honor one of the most diversity-loving, integrative and awesome sports—roller derby. Here are the holotypes...

...and a short video about the ants' behavior, which regularly pick up mites and dump them at their refuse sites.