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The emergence of Phengaris butterflies from ant nests

The emergence of Phengaris butterflies from ant nests



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The butterflies of the Phengaris genus (also known as Maculinea) are known to be brood parasitic. During the fourth instar, the caterpillars leave their food plant and mimic ant larvae, causing the ants to take them back to their nest as if they were ant larvae that had escaped.

While in the nest, the caterpillars mimic ant larvae by means both of surface chemicals and acoustic mimickry (including, I understand it, mimicking sounds made by queens!) After pupating, the pupa continues to engage in acoustic mimickry, although I can't find any reference to whether it does (or even could!) engage in continued chemical mimickry.

But I can't find anything in the literature regarding the adult butterfly's emergence from the pupa and exit from the ant nest. A non-academic book and some web pages claim that the alcon blue (Phengaris alcon) and mountain alcon blue (Phengaris rebeli) adults are no longer engaged in any form of mimickry at this point, and may be attacked by the ants. These accounts differ as to how likely an attack is, how much danger the butterfly is in, and the level of protection afforded by the butterfly scales.

The webpages I mention belong to a University of Copenhagen researcher (Dr. David Nash) who has published work in this field. This suggests that the claim is probably correct.

That said, none of the peer-reviewed publications coauthored by him appear to mention it, and each of the two webpages creates a different impression as to the level of danger involved:

"If an ant tries to bite the butterfly it will only get a mouthful of scales." states one, suggesting that there is little the ants can do to harm or hinder the butterfly. But the other states "The adult has to get out of the ant nest quickly to prevent the ants killing it."

The book is written by someone else. It cites three papers, which do discuss the larvae/pupae and ants. But none of these have any information regarding this specific topic.

A paper by Elfferich provides some information in the case of Phengaris nausithous, the so-called "dusky large blue". The author states: "The butterflies always emerged between 00.00 and 06.00 and walked out of the nest… During the night there was only a little ant activity and there was no real aggressive behaviour… we may conclude that no pheromone to reduce aggression of the ants is produced by the butterfly."

Some published books (not from the academic literature) claim that the "large blue" (Phengaris arion) continues acoustical, and (according to one book) chemical mimickry. Far from being in danger, two of the books claim that they are escorted outside by ants as though they were acting as a bodyguard!

I believe that this is probably true. The reason for this is that two of the books (pub. 2008 and 2010 were describing discussions between the authors and Jeremy Thomas, an Oxford professor who has published research in this field. In fact, Professor Thomas's research identified the butterfly's dependence on ants, the reasons for its decline in the UK, and he was able to reintroduce the species after it became extinct in the UK. The other book (pub. 2014) mentioned Professor Thomas repeatedly, and described a book by him as "One of the essential wildlife books".

Even so, I don't have access to material in which Professor Thomas or any of his colleagues actually state this instead of just being mentioned by others. So it's still second hand information covering only one Phengaris species.

And to complicate matters further, in a paper that predates the three books, Thomas and other researchers stated that Phengaris arion and Phengaris teleius (scarce large blue) adults "show no interaction with ants after eclosion from pupae in the outer cells of Myrmica nests, from which they emerge while the ants are quiescent in the early morning".

Does anyone know of any peer-reviewed sources which confirm, for the various species, whether:

  • The adult butterfly continues to engage in mimickry?
  • Whether this is chemical, acoustic, or both?
  • The ants are more likely now to realise it's an intruder, and may attack it?
  • How likely this is?
  • How much danger are the butterflies in, if so?
  • Some accounts claim that the alcon/rebeli has scales which make it impossible for attacking ants to grasp them. Others refer to the scales protecting them from being bitten. If these attacks are a risk, how well is the butterfly protected and do attacks from angry ants still get through?

I've looked at too many papers to list here, but my sources include:

Non-paywalled:

Barbero F, Thomas JA, Bonelli S, Balletto E and Schönrogge K. (2009). Queen Ants Make Distinctive Sounds That Are Mimicked by a Butterfly Social Parasite. Science 06 Feb 2009: Vol. 323, Issue 5915, pp. 782-785. DOI: 10.1126/science.1163583

Thomas JA, Schönrogge K and Elmes GW. (2005). Specialization and host associations of social parasites of ants. In: Insect Evolutionary Ecology: Proceedings of the Royal Entomological Society's 22nd Symposium (Fellowes M.D.E., Holloway G.J. and Rolff J., Eds). 475-514

Als TD, Nash DR, and Boomsma JJ. (2001). Adoption of parasitic Maculinea alcon caterpillars (Lepidoptera : Lycaenidae) by three Myrmica ant species. Animal Behaviour, 62, 99-106. https://doi.org/10.1006/anbe.2001.1716

Akino T, Knapp JJ, Thomas JA and Elmes GW. (1999). Chemical mimicry and host specificity in the butterfly Maculinea rebeli, a social parasite of Myrmica ant colonies. 266 Proc. R. Soc. Lond. B. http://doi.org/10.1098/rspb.1999.0796

Elfferich NW. (1998). New facts on the life history of the dusky large blue Maculinea nausithous (Lepidoptera: Lycaenidae) obtained by breeding with Myrmica ants in plaster nests. DEINSEA 4: 97-102. ISSN 0923-9308

Paywalled:

Elmes GW, Thomas JA and Wardlaw JC. (1991). Larvae of Maculinea rebeli, a large‐blue butterfly and their Myrmica host ants: patterns of caterpillar growth and survival. Journal of Zoology, 224: 79-92. doi:10.1111/j.1469-7998.1991.tb04789.x

Elmes GW, Thomas JA and Wardlaw JC. (1991). Larvae of Maculinea rebeli, a large-blue butterfly, and their Myrmica host ants: wild adoption and behaviour in ant-nests. Journal of Zoology, 223: 447-460. doi:10.1111/j.1469-7998.1991.tb04775.x


I've been emailing some of the various researchers who worked on the papers I've cited. Jeremy Thomas and Judith Wardlaw both took time out of their (probably very busy!) schedules to reply, and they sent me very detailed replies as well as copies of papers I didn't have access to. Thanks to their replies, I'm in a position to post an answer to my own question.

Dr. Wardlaw, in the course of her research into the Phengaris rebeli (mountain alcon blue) species, had:

"looked after hundreds of rebeli caterpillars and reared them through pupation to adulthood. I watched their emergence from the ant nests in captivity where they were trapped in chambers together without means to escape. I also encountered many nests in the wild. In natural nests the caterpillars tend to crawl to upper chambers in preparation for pupation and eventual emergence and often these are narrow chambers which do not have huge numbers of workers in attendance. The ants do respond to the squeaks etc of the pupae and attend them; when emergence is imminent - much wriggling and increase in sounds emitted - my clear recollection is that the ants are almost stupefied and disperse away from the pupae - the emerging butterflies are not molested by the ants at all although they may revisit the pupal cases to lick any residual body fluids which may be ejected at the time of eclosion. When they did encounter the emergent butterflies, I never witnessed any hostility shown to them so whether the scales act as protection or not, didn't seem to be an issue."

Professor Thomas had this to say regarding P. alcon, P. arion, and two non-Phengaris blues:

"The best and most natural film of the adult emergence in an ant nest is the Netflix film "From deserts to grasslands" in their 'Our Planet' series… by David Attenborough (NB, some of the script they provided him with has minor inaccuracies so ignore the commentary: I was not shown the final script!). There's a sequence on Alcon large blues about 2/3 in… It shows the ants quite excited as the adult butterfly begins to break through the pupal case - but always benign and non-threatening - and then indifferent to it when it emerges and crawls to the surface to blow up wings, unaccompanied by ants. That's my observation of P. arion too (i.e. very different from Silver-studded blue which is tended throughout eclosion). The behaviour with Large Blues is consistent with the possession of a stridulation organ on the pupal case, which produces sounds that mimic the queen ant's, and this will undoubtedly be broadcasting 'I belong here' sounds to the worker ants as the pupal case splits, but not thereafter. We have recordings of this from the Adonis Blue which has a similar organ to the large."

(The Silver-Studded Blue and Adonis Blue have mutualistic relationships with their ant hosts. They are not parasitic. I don't have Netflix so I can't provide a link to that video.)

In the case of Phengaris nausithous, note that the published research by Elfferich (which I quoted in my question) testifies to the same thing. There is no obvious defence mechanism on the newly emerged adult, but it isn't in any sort of danger from the ants, and doesn't need one. Note also the book quote in which Prof. Thomas states that the same is true for Phengaris teleius.

In a comment on my question, I mentioned Liphyra brassolis. This butterfly species also parasitises ants, and does rely on loose scales to defend itself from the ants after emerging. If you follow the PDF link in that comment, it includes photographs of the newly emerged butterfly with these scales. It also includes one photograph of an ant that has tried to attack the butterfly, and so become covered in scales as well.

Those scales are very conspicuous, both on the butterfly and the ant, and there was certainly nothing like them in any of the videos I saw of the Phengaris emergences:

"The Large Blue Butterfly Adopted By Ants" - BBC Earth. This one focuses on P. arion.

An extract from "Life in the Undergrowth", presented by David Attenborough.

Behind-the-scenes of the filming of ants-nest interiors for the Netflix "Our Planet".

I couldn't find a suitably licensed image of the L. brassolis covered in loose scales, so I can't include one in this answer. But as I say, you can just click on the PDF link to see it. In addition, there are some spectacular photos of the butterfly's underwings at:

https://the-butterfly675.blogspot.com/2009/05/another-re-discovery-for-singapore.html

https://www.ifoundbutterflies.org/sp/1094/Liphyra-brassolis

http://www.butterflycircle.com/checklist/showbutterfly/224

http://www.samuibutterflies.com/insects/butterflies/lycaenidae/liphyrabrassolisbrassolis/

The only credible evidence that the adult Phengaris are threatened by the ants is that one, unsupported statement on David Nash's University of Copenhagen webpage. I have emailed Dr. Nash, but have not received a reply. Nevertheless, I am convinced that the claim is not correct.

By contrast, we have a great deal of evidence that the various Phengaris species are not in any danger from the ants after emerging from their pupae, and neither have nor need a defence mechanism based on loose scales. I am confident enough in this that I am posting it as my answer.

As an aside, I also looked up the Ichneumon eumerus parasitoid wasp species, which lays its eggs in the caterpillars of P. rebeli (and maybe also P. alcon, I'm not sure.) After hatching and eating its pupated host from the inside, the adult wasp eventually emerges from the butterfly's chrysalis.

According to a 1993 paper (cited below), the emerging wasp is attacked by the ants! It emits an allomone which causes most of the ants to attack each other, but those closest to the wasp will still attack it. It relies on its armour plating to keep it safe from these as it leaves the nest.

The ants will later show some form of aggressive behaviour toward the empty chrysalis - something they don't do towards the ones that unparasitized butterflies emerge from.

Reference (paywalled):

  • Thomas JA and Elmes GW. (1993). Specialized searching and the hostile use of allomones by a parasitoid whose host, the butterfly Maculinea rebeli, inhabits ant nests. Animal Behaviour, Vol. 45, Issue 3, pp. 593-602. https://doi.org/10.1006/anbe.1993.1069

Abstract

The specificity of the specialisation of Phengaris Doherty, 1891 caterpillars to their host ants is still not fully understood. In this report, we summarize all available records of Phengaris in ant nests from the Czech Republic. P. alcon (Denis & Schiffermüller, 1775) was found exclusively in nests of Myrmica scabrinodis Nylander, 1846 at four sites, and one P. nausithous (Bergsträsser, 1779) caterpillar was found in a nest of M. scabrinodis . According to published records, P. nausithous may use M. scabrinodis at the edges of its range but should be adapted exclusively to M. rubra (Linnaeus, 1758) in the centre of its range. No records of P. arion (Linnaeus, 1758), P. teleius (Bergsträsser, 1779) and P. alcon populations feeding on Gentiana cruciata ( Gentianaceae ) (“ P. rebeli ”) are available from the Czech Republic.


The emergence of Phengaris butterflies from ant nests - Biology

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Results

The DNA clade of each of the 99 ant colonies collected from the six Phengaris habitats was identified by neighbor-joining (NJ) analysis of 470-bp sequences of the mitochondrial COI gene (Fig. S1). We found that four belonged to the L1 clade, 67 to the L2 clade, and 28 to the L3 clade (Table 1). Thus, L2 was the dominant clade in the P. teleius grassland habitats (86.2–100%), and in the woodland P. arionides habitat, all ant colonies belonged to the L3 clade (Table 1). These habitat preferences of the ant clades are congruent with the findings of Ueda, et al. 18 .

Next we identified the DNA clade of each ant colony parasitized by Phengaris caterpillars. The four ant colonies parasitized by P. teleius belonged to L2, and the three ant colonies parasitized by P. arionides belonged to L3 (Table 1). Although the sample size is too small for statistical testing, based on the habitat preferences of ants and the parasitic frequency of Phengaris caterpillars, we tentatively conclude that P. teleius parasitizes L2 colonies and P. arionides parasitizes L3 colonies under natural conditions. To determine the specificity of the Japanese Phengaris—Myrmica interaction more definitively, additional sampling is essential. During this study, however, we decided not to collect more specimens because we judged that additional collections risked excessively depleting the populations of both butterflies and ants.


Caterpillars Use Ants as Butterfly Babysitters

It’s such wonderful warm weather in the UK at the moment, I thought it was time to celebrate with another butterfly post! I particularly wanted to take a closer look at the butterfly Phengaris arion which is rather unimaginatively known more commonly as the Large Blue.

It's such wonderful warm weather in the UK at the moment, I thought it was time to celebrate with another butterfly post! I particularly wanted to take a closer look at the butterfly Phengaris arion which is rather unimaginatively known more commonly as the Large Blue.

Unfortunately the Large Blue went extinct in the UK in 1979. It's been successfully introduced in south-west England from Sweden but I've never seen one myself. In order for reintroduction to be successful, the butterfly doesn't just need the correct habitat and foodstuffs to flourish, it also needs the presence of a species of red ant called Myrmica sabuleti.

The butterflies need the ants as they use them for free childcare. The Large Blue caterpillars are neither large nor blue but instead closely mimic the appearance of the red ant larvae. They are also able to mimic the sounds of the ant larvae, and secrete chemicals that make the ants believe that the caterpillar is one of their offspring. As a consequence, the ants will carry the caterpillars back into their nest. Some species of blue butterfly mimic ant larvae so well that the ants will bring them food and care for them until they are ready to pupate and turn into a chrysalis. The Large Blue is slightly less sophisticated. Once inside the caterpillar hangs out around the outskirts of the nest, where it is protected from predators, occasionally venturing into the centre of the nest to feast on ant larvae. It is also able to mimic the sound of the queen ant to prevent it being detected.

Despite being protected from external predators in the safety of the ant nest, this strategy is not a perfect one for survival. The relationship is highly species specific if the caterpillar is picked up by the wrong species of red ant it is likely to be killed and eaten inside the nest. Even with the correct host there is an incredibly strong selective pressure towards perfect mimicry, as any caterpillars that make the ants suspicious will be identified as intruders and killed. This becomes more likely as the caterpillar grows, as it ends up far larger than the ant larvae it is trying to mimic.

Research indicates that 230 large larvae and a minimum of 354 Myrmica workers are needed to ensure the survival of one Large Blue butterfly! As these are far more than will be found in one nest, it's likely that the caterpillar can move between ant nests, surviving starvation as it travels. Knowledge and research such as this is vital for conservation efforts, as it gives a better idea of the necessary conditions to introduce endangered and extinct species. A healthy large blue population requires a healthy ant population, and in turn will lead to healthier and more diverse ecosystems.

The views expressed are those of the author(s) and are not necessarily those of Scientific American.

ABOUT THE AUTHOR(S)

A biochemist with a love of microbiology, the Lab Rat enjoys exploring, reading about and writing about bacteria. Having finally managed to tear herself away from university, she now works for a small company in Cambridge where she turns data into manageable words and awesome graphs.


Host-ant specificity of endangered large blue butterflies (Phengaris spp., Lepidoptera: Lycaenidae) in Japan

Large blue butterflies, Phengaris (Maculinea), are an important focus of endangered-species conservation in Eurasia. Later-instar Phengaris caterpillars live in Myrmica ant nests and exploit the ant colony's resources, and they are specialized to specific host-ant species. For example, local extinction of P. arion in the U. K. is thought to have been due to the replacement of its host-ant species with a less-suitable congener, as a result of changes in habitat. In Japan, Myrmica kotokui hosts P. teleius and P. arionides caterpillars. We recently showed, however, that the morphological species M. kotokui actually comprises four genetic clades. Therefore, to determine to which group of ants the hosts of these two Japanese Phengaris species belong, we used mitochondrial COI-barcoding of M. kotokui specimens from colonies in the habitats of P. teleius and P. arionides to identify the ant clade actually parasitized by the caterpillars of each species. We found that these two butterfly species parasitize different ant clades within M. kotokui.

Figures

Figure 1. A Phengaris arionides caterpillar feeding…

Figure 1. A Phengaris arionides caterpillar feeding on larvae belonging to the L3 clade of…


Phengaris (Maculinea) alcon butterflies deposit their eggs on tall plants with many large buds in the vicinity of Myrmica ants

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Research output : Contribution to journal › Article › Academic › peer-review

T1 - Phengaris (Maculinea) alcon butterflies deposit their eggs on tall plants with many large buds in the vicinity of Myrmica ants

N2 - The survival of eggs and larvae is dependent on the oviposition site selection of their mothers. In obligate myrmecophilic butterflies, both host plant phenology and host ant presence are expected to affect the decision where to deposit eggs. The importance of ant nest presence in the oviposition site selection of Phengaris butterflies is, however, highly debated. We studied oviposition in the largest Phengaris (Maculinea) alcon population in Portugal, exploiting Gentiana pneumonanthe as the host plant and Myrmica aloba as host ant. We collected phenological plant data and recorded the presence and number of eggs on plants with and without Myrmica ants nearby during the flight period of the butterfly. Females oviposited on tall plants with many tall buds, while the presence of host ant nests weakly affected oviposition on plants where the probability of finding ants at close range was high. Moreover, larger plants with many tall buds close to host ant nests received more eggs. A density-dependent shift in oviposition was not found as the proportion of buds not infected with eggs did not differ between plants with or without ants, whereas plant characteristics did have an effect. Tall plants with many large buds were associated with earlier oviposition. Our results suggest that females of P. alcon in Portugal choose gentian plants for oviposition mainly based on plant characteristics whereas the vicinity of ants had a weak effect. Moreover, our study shows that testing the ant-mediated oviposition hypothesis requires baiting ants more than once.

AB - The survival of eggs and larvae is dependent on the oviposition site selection of their mothers. In obligate myrmecophilic butterflies, both host plant phenology and host ant presence are expected to affect the decision where to deposit eggs. The importance of ant nest presence in the oviposition site selection of Phengaris butterflies is, however, highly debated. We studied oviposition in the largest Phengaris (Maculinea) alcon population in Portugal, exploiting Gentiana pneumonanthe as the host plant and Myrmica aloba as host ant. We collected phenological plant data and recorded the presence and number of eggs on plants with and without Myrmica ants nearby during the flight period of the butterfly. Females oviposited on tall plants with many tall buds, while the presence of host ant nests weakly affected oviposition on plants where the probability of finding ants at close range was high. Moreover, larger plants with many tall buds close to host ant nests received more eggs. A density-dependent shift in oviposition was not found as the proportion of buds not infected with eggs did not differ between plants with or without ants, whereas plant characteristics did have an effect. Tall plants with many large buds were associated with earlier oviposition. Our results suggest that females of P. alcon in Portugal choose gentian plants for oviposition mainly based on plant characteristics whereas the vicinity of ants had a weak effect. Moreover, our study shows that testing the ant-mediated oviposition hypothesis requires baiting ants more than once.


Myrmica Ants and Their Butterfly Parasites with Special Focus on the Acoustic Communication

About 10,000 arthropod species live as ants' social parasites and have evolved a number of mechanisms allowing them to penetrate and survive inside the ant nests. Myrmica colonies, in particular, are exploited by numerous social parasites, and the presence of their overwintering brood, as well as of their polygyny, contributes to make them more vulnerable to infestation. Butterflies of the genus Maculinea are among the most investigated Myrmica inquilines. These lycaenids are known for their very complex biological cycles. Maculinea species are obligated parasites that depend on a particular food plant and on a specific Myrmica species for their survival. Maculinea larvae are adopted by Myrmica ants, which are induced to take them into their nests by chemical mimicry. Then the parasite spends the following 11–23 months inside the ants' nest. Mimicking the acoustic emission of the queen ants, Maculinea parasites not only manage to become integrated, but attain highest rank within the colony. Here we review the biology of Maculinea/Myrmica system with a special focus on some recent breakthrough concerning their acoustical patterns.

1. Butterflies and Ants

Most myrmecophiles are commensals or mutualists, which live undisturbed or even actively protected within the foraging areas or territories of ants [1–3]. Their functional and evolutionary ecology, as well as their truly amazing diversity, have been reviewed by Wasmann [4], Donisthorpe [5], Hinton [6], Malicky [7], Hölldobler and Wilson [1], DeVries [8, 9], Fiedler [10, 11], Pierce et al. [12], and others.

The interactions that have evolved between insects and ants range from loose facultative associations to obligate dependency (as concerns butterflies, see [3, 11, 13, 14]). The nests of eu-social arthropods, including insects such as ants, bees, wasps, or termites, are aggressively defended from predators and intruders alike. As a consequence, these nests provide very safe havens for any roughly ant-sized organism having evolved the necessary adaptations to penetrate them and to become accepted as “self” by the workers’ caste [4, 5, 15]. Around 10,000–15,000 insect morphospecies have evolved as social parasites of ants, thus accounting for a significant proportion of the world’s biodiversity. Yet, despite the many species, most ant social parasites are exceedingly rare or localized, in comparison to the abundance and distribution not only of their ant hosts but also of other symbionts, which loosely interact with ants [1, 16, 17].

Myrmecophily is widespread among Lepidoptera, most particularly as concerns the Riodinidae and Lycaenidae [9, 12], which are often globally referred to as “lycaenoids” [10], and which make up approximately 30% of all known Papilionoidea [18]. Their relationships with ants can be mutualistic or parasitic and vary from facultative to strictly obligate. In the case of facultative myrmecophiles, the survival of butterfly larvae does not depend on the presence of attendant ants, and associations are unspecific. In other words, these lycaenoids can use ants belonging to several different species, or even subfamilies [11, 12]. On the contrary, in obligate ant associations, butterfly immatures are dependent on ants’ presence, at least in some part of their life cycle and interactions are much more species specific [11, 12].

Achieving a myrmecophilous life style requires evolving numerous special adaptations, which are necessary for avoiding ant aggression and for communicating with ants. The cuticle of many myrmecophilous butterfly larvae is thicker than in other groups of Papilionoidea and the head can be retracted under a sclerotized plate [7, 19]. Frohawk [20] was the first to observe that most myrmecophilous butterfly larvae have dorsal nectar organs (DNOs), whose “honeydew” secretion attracts and pacifies ants, and plays an essential role in the maintenance of ant attendance [12]. Additionally, many lycaenoid caterpillars possess specialized epidermal glands, pore-cupola organs and tentacle organs, whose secretions are apparently not directly used by ants, but can somehow manipulate their behaviour [21–23]. Moreover, some butterfly species produce cohorts of other chemical and/or acoustical signals, which are involved in their interactions with ants [12].

2. The Parasites: Maculinea Butterflies

One of the most intensively studied systems in which both the communication channels are investigated concerns parasitic Maculinea butterfly larvae and their Myrmica host ants (Figures 1(a) and 1(b)) [24–26]. During the past decades butterflies of genus Maculinea (Figure 1(d)) have become “flagships” of European biodiversity conservation [24] and are perceived as umbrella species covering many grassland communities [27–29].


(a)
(b)
(c)
(d)
(a)
(b)
(c)
(d) (a) Forager worker of Myrmica ant. (b) Trophallaxis between attendance worker and Maculinea larva. (c) Maculinea rebeli foodplant: Gentiana cruciata. (d) Mating of Maculinea butterflies.

Some recent publications [30–32], based on both molecular and morphological data, have shown that species of Maculinea and Phengaris form a monophyletic group, where the three Chinese Phengaris species are basal. According to Fric et al. [32] Maculinea Van Eecke, 1915 should be considered a junior subjective synonym of Phengaris Doherty, 1891. Possible alternatives are that Maculinea is, as subjectively, considered subgenus of Phengaris, or a distinct genus in its own right.

On the other end the obligate myrmecophilous life style of Maculinea has attracted a vast number of studies, many of which appeared in leading scientific journals. Maculinea is a model organism for studies on the origin and evolution of parasitic interactions and of host-parasite communication channels [11, 24–26, 30, 33].

Maculinea have also attracted a great deal of attention from a conservationist’s point of view [34–37]. For this reason some of the authors have asked the International Commission on Zoological Nomenclature to conserve the name Maculinea against Phengaris in all cases when the two are considered subjective synonyms. The decision by the ICZN is still pending and we will continue to use Maculinea rather than Phengaris, at least for the moment.

Another point is that no molecular evidence is available to distinguish Maculinea rebeli from Maculinea alcon and some authors have argued that the first of them is an ecotype of M. alcon [32]. Also in this case we have decided to stick to the traditional interpretation that M. alcon and M. rebeli represent separate clades (species) and in this paper we will use the name Maculinea rebeli to designate what might represent the xerophilous ecotype of M. alcon.

European Maculinea species need urgent conservation actions, indeed four are mentioned in the European Red List of Butterflies and three of them are included in the Annex IV of the Habitats Directive [38, 39]. These lycaenids are known for their very complex biological cycles. Maculinea species are all obligated parasites that depend on a particular food plant and on a specific Myrmica species for their survival. After having spent 10–15 days feeding on a species-specific host plant (Figure 1(c)), the 4th instar larvae of all Maculinea species drop to the ground and wait until they are found and carried into an ant nest by a Myrmica worker [40–44]. Once in the ant colony, Maculinea species differ in their alimentary strategy: (i) Maculinea alcon and Maculinea rebeli utilize a “cuckoo” strategy, and are mostly fed directly by attending workers (trophallaxis) [42] (Figures 1(a) and 1(b)), they are known for experiencing “contest” competition at high densities [45], (ii) Maculinea arion and Maculinea teleius are “predatory species” and directly prey on ant brood, experiencing “scramble” competition when overcrowded in the host colony [46], while (iii) the alimentary strategy of Maculinea nausithous has not yet been fully clarified, with some authors suggesting the coexistence of both “cuckoo” and “predatory” strategy and others considering it as a “cuckoo” species [24, 47]. Maculinea larvae spend 11 or 23 months inside their host colonies. In many populations two separate cohorts of larvae spending either one or two years inside the ants’ nest are known to exist [33, 48–50]. The polymorphic growth pattern found in Maculinea populations is likely to have evolved for ergonomic, or perhaps hedge-betting reasons.

Two are the key moments in the life cycle of these butterflies: (i) the choice of an optimal food-plant on which to lay eggs and (ii) the first direct interaction with the host ants. The place where females lay their eggs is crucial for a myrmecophilous butterfly, to ensure its brood the chance to be adopted by a specific host ant. Because the worker ants’ foraging range is limited, selecting an “ideal” oviposition site requires that both the phenological stage of the larval food plant (short-term larval fitness) and the presence of suitable host ants (long-term larval fitness) are taken into account. The female’s selection of a valuable oviposition plant is influenced by a variety of factors. Plants are generally selected by females on the basis of their buds’ phenology, while the presence of the host ants in the near surroundings of the plant may be variously insured depending on local situations and perhaps on the species. In some cases the host-plant and the Myrmica ant share a similar ecological niche, so that their overlap ensures population persistence [51–54]. In other cases, however, female butterflies mostly choose those plants which occur in the ants’ foraging range [55–59]. To the best of the authors’ knowledge, nothing is known about the mechanism providing butterfly females with the ability to discriminate among host plants placed inside/outside the foraging range of a Myrmica colony.

The other hot point of research on Maculinea butterflies is their host specificity with ants, both for its relevance in coevolutionary dynamics and as a background for conservation strategies. While Maculinea caterpillars induce workers of any Myrmica species to retrieve them by chemical and acoustical deception [26, 60], their survival till the adult stage will depend largely on which ant-species has found the larva [41–44, 61].

Before the 1970s a nonextensive study of Maculinea host specificity led scientists to consider all Myrmica species and, in some cases other ant’s genera (e.g., Lasius), as potential host of these butterflies. In the following decades Thomas et al. [61] revealed a clear host specificity pattern involving each of the five European Maculinea species. In their work authors demonstrated that the survival of every Maculinea species was linked to single and different Myrmica ant species, while the adoption by a non-host species caused a large decrease in the survival rate of these butterflies. More recently, the large amount of data collected by many researchers all across Europe, confirmed these general guidelines, but demonstrated that host specificity patterns are much more complex and hosts may vary geographically all along the range of each Maculinea butterfly. The only species that apparently keeps a single host is M. nausithous [34, 62, 63], which shows a clear adaptation to Myrmica rubra all over its distribution [47, 61, 62, 64]. The only known exception to this occurs in Transylvania, where it exploits M. scabrinodis as alternative host [65]. Data on other Maculinea species show a much more complicated pattern, which demonstrates that host specificity occurs at the population or, at least, at the regional scale. Several works have shown that M. teleius, M. arion, M. alcon, and M. rebeli may be locally adapted to some Myrmica species previously considered as nonhost [29, 50, 64–72] and in the case of the latter two species have developed the ability to successfully exploit more than one host species in the same site creating real multiple host populations [25, 73].

3. The Host: Myrmica Ants

Myrmica ants are hosts of Maculinea butterflies, but their colonies are infested by numerous other social parasites such as the larvae of the hoverfly Microdon myrmicae (Diptera Syrphidae see [74, 75]), or by parasitic ant species of the same genus [76]. Reasons for this apparent asymmetry are unclear, but may be related to the biological cycle of these ants. The genus Myrmica has a Holarctic distribution. Most of the species, however, are found in Europe and Asia, while a smaller proportion occurs in North America [77]. Colonies are widespread and can be found in various kinds of habitat, such as meadows, forests, steppes, or mountains [76]. Although the biology of many Myrmica species has not been studied in detail, it seems that a general life style is common to all ants of this genus [76]. Most colonies contain on average 200–500 workers, as well as from one to many functional queens [78, 79]. New nests can be either funded by a single newly mated queen or, more often, by budding pre-existing colonies [45]. Oviposition starts in early spring and lasts throughout the summer, while it stops in autumn when temperature is decreasing [76]. Part of the larvae develop rapidly but others enter diapause and overwinter. The latter group includes both workers and all the gyne-potential larvae [80]. Some of these life history traits of Myrmica ants make them more vulnerable to infestations by social parasites. One of the most important is presence of overwintered ant larvae particularly essential for survival of the predatory Maculinea larvae, which start their intensive growth inside host colony at the beginning of spring and use overwintered ant brood as their food resource [49, 81]. Another significant trait that make Myrmica ants a proper host for many social parasites is that many Myrmica species live in polygynous colonies and some of them such as M. rubra, M. ruginodis, or M. rugulosa may contain a relatively high number of workers [76, 77]. This results in lower relatedness among worker nest mates [78, 82]. Many studies [83–85] showed that high genetic variance may be beneficial for social insects colonies, but it can also increase the likelihood of being infested by social parasites, because of the greater variance in nest mate recognition cues. It was indicated that Microdon mutabilis (Linnaeus, 1758) (Diptera: Syrphidae), a social parasite of Formica lemani ants, more often infests host colonies where genetic relatedness is lower [86]. A similar situation was found for colonies of M. rubra infested by M. alcon [87]. Therefore, a cost of polygyny existing in most of Myrmica species is that their colony communication signals (e.g., chemical or acoustical) tend to be broader and more heterogeneous than in monogynous ant species and their colonies can be more easily invaded by cheats that mimic these signals.

4. Acoustical Pattern in the Maculinea-Myrmica System

The more fine-tuned the host-parasite relationship is, the more intriguing studying how the host’s deception can be achieved is. The communication of social insects is mainly based on chemical cues [1], but also the acoustic channel is used, thus it is clear that the parasite has to bypass the host’s chemical and acoustical system to enter and live in its colonies [88].

Cuticular hydrocarbons have long been assumed to play a fundamental role in the nest mate recognition of social insects. All individuals living in the same society share a bouquet of chemicals, which serves as a “colony odour” and enables them to discriminate between nest mates and strangers. Additional variation in hydrocarbon pattern is associated with differences in sex, caste, and developmental stage [89, 90]. The fact that caterpillars of Maculinea butterflies use chemical mimicry to become adopted and to infiltrate colonies of their hosts was first proposed by Elmes et al. [42], while the first experimental evidence was produced by Akino et al. [43], who found that the chemical profile of Maculinea rebeli resembles that of its host more than those of other Myrmica species.

Even though sound production is not usually the dominant strategy, acoustic communication plays a fundamental role in some groups of insects [91]. Depending on the taxon, sound productions may have a number of functions, ranging from mate attraction to courtship, aggression, defence, or recruitment of foragers, at least in social insects. Recently, it has been suggested that sounds play a role in the modulation of other signals. This was demonstrated to occur at least in honey bees [92–96].

The role of stridulations in ant communication was underestimated for a long time [8, 26], also because of our scant understanding of the structures involved in the production and the reception of the acoustic signals. Stridulations, however, have long been known to occur in 4 ant subfamilies [97, 98]. In these ants, sounds are produced by a minutely ridged stridulating organ (pars stridens) positioned on the middle-dorsal part of the 4th “abdominal” segment and by a spike (plectrum) jutting from the postpetiole’s rear margin [26, 99–103] (Figure 2(b)). When an ant moves its abdomen, the two parts rub on each other and emit a series of “chirps” [1, 103, 104]. Stridulations are variously defined depending on the transmitting medium. They are sounds, when transmitted by air, or vibrations, if transmitted by substrate. Myrmecologists have long believed that ants cannot “hear” the aerial component of a stridulation but perceive substrate-transmitted vibrations [105]. This notion was based on experience obtained in the early 20th century [106, 107], and has been indirectly confirmed ninety years later by the discovery of a subgenual organ in Camponotus ants [108]. More recently, however, a seminal paper by Hickling and Brown [105] provided fresh impulse to studies on the possible perception of air-transmitted sounds heating the debate on this subject [109, 110]. Hickling and Brown [105] maintain that ants cannot perceive the aerial component of sounds over a long distance (i.e., 1 m), but largely use short range acoustic communication (i.e., 1 cm).


Morphology (upper part) and sounds (lower part) of the acoustical organs of (a) Maculinea rebeli pupa and (b) Myrmica schencki queen.

Acoustic communication plays a wide range of roles in the ants’ social behaviour, from reciprocal attraction to intercaste interactions. In most cases, these stimuli are effective only at small range and are mainly used as signals of alarm, for foragers’ recruitment, mating requests, intimidation, and aposematic “threatening”, as well as to modulate other kinds of signals [1, 92, 111–118].

Functions of stridulations have been intensively surveyed in Atta ants, where foragers’ calls are most frequent when leaves of the highest quality for fungal cultures are found [119]. Myrmica workers frequently stridulate during trophallaxis, particularly the receiving worker, when food decreases [120, 121]. Intercaste acoustical communication has been recorded in only a few instances. Mating queens of Pogonomyrmex badius stridulate to signal to males when their spermathecae are full [111] whereas, in Atta, leaf-cutting workers stridulate when they are ready to return to the nest. This behaviour induces individuals of the smallest “minim” caste to climb onto the leaf fragment where from there they protect their larger sisters from attack by phorid flies during the journey home [117]. Until recently, there was no direct evidence that different members of an ant society produced distinctive caste-specific sounds to induce appropriate patterns of behaviour either in fellows or in other castes. At least two studies, however, suggested that different castes produce distinctive signals: the major workers of Atta cephalotes make sounds that are more intense and carry further than those of their smaller nest mates [122], while the space between the ridges of the pars stridens of queens exceeds that of workers in four Messor species [102].

Our own findings demonstrated that Myrmica schencki queens generate distinctive sounds that elicit increased benevolent responses from workers, thereby reinforcing their supreme social status [26, 123]. These findings demonstrated that acoustical communication within the vast subfamily Myrmicinae (to which Messor spp. and Myrmica spp. belong) is more variable and conveys more social information within ant colonies than was previously recognized. In this group, stridulations also fulfil the strict adaptationist definition of biological communication, in which both the signal and the response are adaptive [26, 124, 125].

Since acoustic signals convey quite complex information, not only between worker ants while outside the colony (e.g., during foraging), but also within the nest and between castes, we started research aimed at understanding whether some social parasites, such as butterfly larvae, could interfere with this communication system. Lycaenid larvae, in fact, have long been known to be able to emit stridulations even if their life cycle is not linked at any degree to the ant presence, but sounds produced by myrmecophilous species are more complex and frequent than those emitted by nonmyrmecophilous species [22]. More in general, however, studies aiming at clarifying the function of interspecific acoustic communication in myrmecophilous Lepidoptera are scarce. Most of these studies considered butterfly larva stridulations as a merely defensive signals [6, 126] or, more rarely, as aggregation messages [127]. Sounds produced by lycaenid pupae and caterpillars originate from different organs the former from tooth-and-comb stridulatory organs between the fifth and sixth segments [12, 126, 128, 129] (Figure 2(a)), whereas caterpillar sounds may emanate from muscular contraction and air compression through the tracheae [130]. The acoustics of mutualistic lycaenid species does not obviously mimic ant stridulations, and ants attraction has been demonstrated only in the pupae of one extreme mutualist species (i.e., Jalmenus evagoras see [12, 131]. On the contrary, the larval calls of four Maculinea species are similar in pulse rate and band width to those of their hosts, although the level of apparent mimicry is to the genus Myrmica rather than to individual host ant species [132]. The same study showed that Myrmica larvae are mute, suggesting that in this trait Maculinea caterpillars are mimicking an adult ant cue, but no direct cause-and-effect relationship was revealed (recordings by DeVries et al. [132] were restricted to distressed worker ants and caterpillars, and were not played back to the ants). Studying the Maculinea rebeli/Myrmica schencki system, we recently demonstrated the first case of acoustical mimicry in an ant social parasite [26]. In particular we demonstrated that Maculinea rebeli larvae and pupae are able to mimic the sounds produced by Myrmica schencki queens (Figures 2(a) and 2(b)), thus obtaining a high status in the host colony hierarchy. Queens, that never come out of the nest, produce peculiar stridulations, which attract workers. Ethological experiments revealed that the acoustical signals produced by Maculinea rebeli larvae elicit the same benevolent responses in the worker ants as those emitted by their queen(s). When recordings of unstressed adult M. schencki were played back to laboratory cultures of workers, the sounds of both castes induced benign responses including aggregation and antennation at the speaker. Moreover, when workers were played their queen’s sounds, they stood “on guard” on the speaker to a much greater extent than when worker sounds were played, each holding the characteristic posture adopted by a Myrmica worker when protecting an object of high value to the colony [26]. Maculinea rebeli caterpillars are rescued ahead of the ant brood when a colony is disturbed, and are fed in preference to host ant larvae when food is scarce [48]. Neither chemical mimicry nor their begging behaviour explains why M. rebeli caterpillars are treated in preference to host ant brood. Instead, we have suggested that acoustical cues are employed [26].

Thus it is possible that acoustical mimicry does not occur in Maculinea rebeli only, but rather provides another route for the infiltration of other Maculinea species, as well as for other myrmecophilous insects [26]. Acoustical mimicry can also be related to the level of interaction between host and parasite, or may play a role in host-specificity. In particular, in the Maculinea/Myrmica system the level of host’s integration within the colony results from the two distinct parasites’ foraging strategies. In the so-called “cuckoo” species, Maculinea larvae become perfectly integrated members of the colony, as they need to be tended by worker ants. Larvae of predator species, in contrast, will prey on the ants’ brood and spend much of their life hidden in the remote chambers of the nest. DeVries et al. [132] showed that also the caterpillars of the predatory Maculinea species produce sounds that appear to mimic Myrmica (worker) stridulations, although in nature they are less closely integrated with their host’s society [14], so that they might be less perfect acoustical mimics of their hosts. We tested [124] this hypothesis by comparing the acoustics of unstressed Maculinea arion caterpillars and pupae with those of the queens and workers of its host ant, Myrmica sabuleti, and with data obtained for Maculinea rebeli and Myrmica schencki, but found no evidence that M. rebeli is a closer mimic of M. schencki than M. arion is to M. sabuleti [26]. We also compared the worker and queen sounds of M. sabuleti, and those of two other ants, Myrmica scabrinodis and M. schencki, to determine whether the distinctive acoustical communication system occurring in the different castes of M. schencki exists in its congeners.

We found that stridulating queens from two additional Myrmica species (i.e., M. sabuleti and M. scabrinodis) make distinctive sounds from those of their workers by using morphologically distinct organs [124]. Interestingly, the calls produced by queen from the three Myrmica species were indistinguishable from each other, as were workers’ stridulations even at a less extent. This suggests that acoustics plays little or no part in the cues used by Myrmica to distinguish between kin and nonkin, or other species of ant and members of their own society. Indeed numerous studies demonstrate the predominant role of chemical cues and the gestalt odour in colony recognition or between physiological states within an ant society [1]. However, our recent results suggest that acoustical communication, in isolation, is capable of signalling at least the caste and the status of a colony member, as well as of inducing appropriate behaviour towards it by the attending workers [124]. In other words, acoustical mimicry is genus rather than species specific, as DeVries et al. [132] concluded. We have not yet studied whether different castes of Myrmica ants responded differently when played the same sounds, although this seems probable, because Myrmica schencki queen respond aggressively when introduced to Maculinea rebeli pupae (which mimic queen sounds) whereas the workers tend them gently [26].

5. Concluding Remarks

To our knowledge, although 10,000 species of ant social parasites may exist [24] particularly among the Coleoptera, Diptera and Lepidoptera [1], acoustical mimicry has rarely been examined outside the case of Maculinea. Together with Di Giulio and his collaborators, we recently surveyed the acoustical emissions of Paussus favieri (Coleoptera, Paussinae), a myrmecophilous paussine beetle which lives in the nests of the ant Pheidole pallidula [133]. The presence of stridulatory organs in members of the myrmecophilous ground beetles tribe Paussini has long been known. However, due to the rarity of these beetles and the challenges in rearing them in captivity, sounds emitted by these organs have never been investigated, as well as their biological significance. The complexity of P. favieri’s sound repertoire suggests that it has an important role in its interaction with P. pallidula.

We strongly believe that the implementation of studies on acoustic communication will bring about significant advances in our understanding of the complex mechanisms underlying the origin, evolution and stabilisation of host-parasite relationships. To improve our understanding of how important and how generalised acoustic mimicry is we also need to clarify which sensory structures are involved in sound perception processes, both in queen and worker ants. Nobody, so far, has ever investigated the possibility that the larvae and pupae of myrmecophilous lycaenids may perceive the sounds emitted by conspecifics, or by their host ants. In this respect it is worth noticing that some of the most important research on the role of filiform hairs in sound perception (e.g., [134, 135]) were carried out on Barathra brassicae (Lepidoptera: Noctuidae). The larvae of this moth, indeed, are able to detect the vibrations produced by a parasitoid wasp, by their thoracic hairs.

Acknowledgments

The authors would like to thank all the colleagues of the MacMan project. The research has been carried out within the project CLIMIT (Climate Change Impacts on Insects and Their Mitigation [37]) funded by DLR-BMBF (Germany), NERC and DEFRA (UK), ANR (France), Formas (Sweden), and Swedish EPA (Sweden) through the FP6 BiodivERsA Eranet as well as within the project A Multitaxa Approach to Study the Impact of Climate Change on the Biodiversity of Italian Ecosystems funded by the Italian Ministry of University and Research (MIUR).

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Copyright

Copyright © 2012 F. Barbero et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


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Bacterial communities within Phengaris (Maculinea) alcon caterpillars are shifted following transition from solitary living to social parasitism of Myrmica ant colonies

Bacterial symbionts are known to facilitate a wide range of physiological processes and ecological interactions for their hosts. In spite of this, caterpillars with highly diverse life histories appear to lack resident microbiota. Gut physiology, endogenous digestive enzymes, and limited social interactions may contribute to this pattern, but the consequences of shifts in social activity and diet on caterpillar microbiota are largely unknown. Phengaris alcon caterpillars undergo particularly dramatic social and dietary shifts when they parasitize Myrmica ant colonies, rapidly transitioning from solitary herbivory to ant tending (i.e., receiving protein-rich regurgitations through trophallaxis). This unique life history provides a model for studying interactions between social living, diet, and caterpillar microbiota. Here, we characterized and compared bacterial communities within P. alcon caterpillars before and after their association with ants, using 16S rRNA amplicon sequencing and quantitative PCR. After being adopted by ants, bacterial communities within P. alcon caterpillars shifted substantially, with a significant increase in alpha diversity and greater consistency in bacterial community composition in terms of beta dissimilarity. We also characterized the bacterial communities within their host ants (Myrmica schencki), food plant (Gentiana cruciata), and soil from ant nest chambers. These data indicated that the aforementioned patterns were influenced by bacteria derived from caterpillars' surrounding environments, rather than through transfers from ants. Thus, while bacterial communities are substantially reorganized over the life cycle of P. alcon caterpillars, it appears that they do not rely on transfers of bacteria from host ants to complete their development.

Keywords: 16S amplicon sequencing Lepidoptera Lycaenidae Spiroplasma butterflies myrmecophily.

Conflict of interest statement

Figures

Bacterial community composition within Phengaris…

Bacterial community composition within Phengaris alcon caterpillars and Myrmica schencki workers and larvae.…

Multivariate representations of bacterial community…

Multivariate representations of bacterial community composition (beta diversity), using nonmetric multidimensional scaling (NMDS)…

Heatmap of the 40 most abundant OTUs, with Bray–Curtis clustering of sample types…

Boxplots representing total 16S rRNA…

Boxplots representing total 16S rRNA gene copies per microlitre of DNA extraction in…


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