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Lepidoptera
There are a number of butterflies that live at least part of their life in close association with ant species.
Photo Gallery
Podomyrma adelaidae tends to a Lycaenid caterpillar. These caterpillars secrete substances that the ants find attractive, and the ants in turn provide protection from parasites. Poochera, South Australia. Photo by Alex Wild.
The Lankan Large Oakblue (Arhopala amantes, family Lycaenidae) and the attending ant Oecophylla smaragdina. Photo by Kalesh Sadasivan, April 2022, Trivandrum, Kerala, India.
Introduction
Obregon et al. (2015) provide an overview and introduction to this topic. Caterpillars of butterflies have evolved defensive adaptations to limit attack from natural enemies, including parasitoids. The most striking mechanism of this kind is probably the mutualistic relationship that lycaenid larvae have developed with ants (Pierce et al., 2002; Seymour et al., 2003). Various scenarios have been proposed to explain this complex behavior. Thomann (1901) first suggested that the ants keep parasitoids away, thereby benefiting the larval instars (see also Pierce and Eastal 1986; Pierce et al., 1987). Larvae seek to attract ants by secreting sugary and nutritious exudates highly appreciated by ants, through exocrine glands - myrmecophilous organs - first described by Newcomer (1912). Lenz (1917) proposed another interpretation of the origin of these exudates, as adaptation of Lepidoptera larvae to produce a sugary liquid to prevent aggression by ants. In this case, any effect those ants have in protecting the caterpillars would be a secondary consequence, but equally effective. In addition, caterpillars and pupae of myrmecophilous Lycaenidae can use acoustic signals (stridulatory organs) to attract the ants (Pierce, 1995; Pirce et al., 2002). Recently, in Álvarez et al. (2012, 2014) the stridulatory organs are found in myrmecophilous and nonmyrmecophilous lycaenids that supported the idea that sound production is not necessarily related with myrmecophily within the Lycaenidae. Commensalism that becomes a mutualistic relationship is a common process in the evolution of many interactions (Margalef, 1974). But in some cases the larvae of certain butterfly species exploit ant nests as food resource and shelter, and behave as specialized social parasites (Witek et al., 2008). In the genus Phengaris Doherty, 1891 some species prey on ant brood and are called predatory species, while others, termed “cuckoo” species, mimic ant larvae and are fed directly by workers (Witek et al., 2008). Whatever the origin may be, the caterpillars are at least to some extent protected through the presence of ants from predators and parasitoids (Fiedler et al., 1993; Jordano et al., 1992.), although some parasitoids have successfully specialized on Lycaenidae and may inflict heavy mortality (Bink, 1970, Shaw, 1996, Shaw et al., 2009), and some extraordinary associations and behaviors have resulted (Thomas and Elmes, 1993; Thomas et al., 2002). Thus many Lycaenidae have associations with ants, which can be both facultative and obligatory, ranging from mutualism to parasitism (Pierce et al., 2002). As a result, more than half the species of the family Lycaenidae may have an association with ants at some stage of their development (Pierce, 1987; Fiedler, 1996, 2006).
For many of the Iberian Lycaenidae, interactions with ants constitute a facultative and slack mutualism and, therefore, this association is not strictly necessary for the full development of the larva. Just in a few species, such as Plebejus argus (Linnaeus, 1758) (Thomas, 1985; Seymour et al., 2003), an obligate myrmecophily occurs and, in the most extreme case, mutualism becomes obligate parasitism, as in genus Phengaris, regarded as social parasitism (Thomas et al., 1991; Munguira and Martín, 1997; Als et al., 2001; Witek et al., 2008.).
Morphology
A recent finding suggests some butterfly taxa with larvae that are thought to be associating with ants, despite a lack of direct observation of ant-butterfly interactions, need to be investigated more thoroughly. Nielsen and Kaminski (2018): The function of tentacle nectary organs (TNOs) in Mesosemiina. Symbiotic interactions between butterflies and ants are mediated by sophisticated morphological adaptations generically called ant-organs (DeVries 1991b, Fiedler 1991, Pierce et al. 2002). In myrmecophilous Riodinidae there are several kinds of larval ant-organs, including organs related to: chemical signaling (DeVries 1988, DeVries et al. 2004, Kaminski et al. 2013); production of substrate born vibrational signals for ant recruitment (DeVries 1990, 1991c; Travassos et al. 2008); and release of nectar rewards for tending ants in exchange of protection against natural enemies (DeVries & Baker 1989, DeVries 1991a). These rewards play a critical role in the maintenance of ant/butterfly mutualisms and in ant-tended riodinids this function is performed by the tentacle nectary organs (TNOs), a pair of eversible glands on the abdominal segment A8 found in the Nymphidiini and Eurybiina (DeVries 1991b, 1997; DeVries & Penz 2002). All known species in the “Mesosemia section”, including the species of Mesosemia, Leucochimona, Semomesia and Perophthalma have TNOs and lack anterior tentacle organs (ATOs) on the metathorax like the Eurybiina larvae (see Horvitz et al. 1987, DeVries 1997, Campbell & Pierce 2003).
Nevertheless, “Mesosemia section” caterpillars have been described as nonmyrmecophilous (Harvey 1987; DeVries 1991c, 1997; Vélez-Arango et.al. 2010) and there is not a single account of true ant-caterpillar symbiosis for this group. Our observations and experiments with larvae of the “Mesosemia section” indicate a new, unexpected defensive function for TNOs in this lineage of Riodinidae. In Mesosemia cippus these glands were promptly everted in all instars when the larvae were molested or experimentally touched by objects, while the solitary larvae were more reluctant and for the most part only everted the TNOs when contacted by ants. Due to the high metabolic cost of producing rewards, myrmecophilous caterpillars release secretions only when properly antennated by tending ants (Fiedler 1991, DeVries & Penz 2002, Kaminski & Rodrigues 2011). In this way, the mechanism of TNO activation in Mesosemiina is somewhat different from what is usually recorded for ant-tended caterpillars. Moreover, rewards produced by myrmecophilous larvae are droplets of a clear fluid (Fiedler 1991, Daniels et al. 2005). In the “Mesosemia section”, the everted TNOs release a conspicuous drop of opaque and viscous liquid on the tip of the tentacle that was reabsorbed after 2–3 seconds followed by tentacle retraction. This drop is sticky and quite resistant, enough to resist the procedures of fixation and critical-point-drying performed for the scanning electron microscopy (Figs. 60–61). Ants mostly ignored the larvae although some ants were observed approaching a TNO (Fig.48, 77) and immediately breaking off contact with the larva without touching the liquid; ants that did contact the secretion engaged in typical cleaning behavior after and further avoided the caterpillar. What can be seen in these examples is that the interactions are not mutualistic and the TNOs do not facilitate stable symbiotic interactions between the caterpillars and ants. A similar situation is found in caterpillars of the sister lineage “Napaea section” (G. J. Nielsen & L. A. Kaminski, in prep.), which explains the controversial previous records of myrmecophily in this group (see Barcant 1970, Brévignon 1992a). A probable explanation of this behavior is that these ant-organs have evolved from a symbiotic context to a defensive function and the TNO secretions now appear to block the ant’s prey response or recognition of the caterpillar as a food source. Analysis of the liquid produced by the TNOs and controlled experiments with ants and caterpillars may help explain this newly described relationship.
Species Associations
Species Accounts
Favonius quercus
Obregon et al. (2015) - Favonius quercus (Linnaeus, 1758) is a univoltine and monophagous butterfly feeding on various species in the genus Quercus (oak). It has been recorded to be attended by Lasius sp. (Fiedler, 2006). In June 2012, several pupae were found sheltered under large stones in nests of Formica gerardi and Pheidole pallidula (Nylander, 1849). Fully grown caterpillars presumably drop from the branches of the oaks or go down the trunk before finding shelter in ant nests at the base of trees; however, it is unknown if the caterpillars are carried to the nest by ants or if the caterpillars can find the nest by themselves.
Glaucopsyche alexis
Obregon et al. (2015) - Glaucopsyche alexis (Poda, 1761) is a univoltine, rare and local lycaenid species in the southern Iberian Peninsula, only present in habitats with limestone soils in the Betic mountains where its food plants of the genus Onobrychis Miller, 1754 grow. It has been recorded associated with many ants species: Myrmica scabrinodis, Crematogaster auberti, Tapinoma erraticum, Formica cinerea, Formica selysi, Formica fusca, Formica pratensis, Formica sanguinea, Formica forsslundi, Iberoformica subrufa, Camponotus aethiops, Camponotus pilicornis Camponotus cruentatus, Lasius alienus (Fiedler, 2006) and Camponotus piceus, Lasius niger and Lasius brunneus (Álvarez et al., 2012). In the present study, caterpillars were attended by Plagiolepis schmitzii, and we also confirmed its interaction with Iberoformica subrufa. Larvae were found feeding on Onobrychis argentea Boissier, 1840. It is clearly a lycaenid that can be attended by many different ant species, having therefore a strong and facultative interaction with all of them.
Hallonympha paucipuncta
Kaminski (2008) - This study analyzes host plant use and obligate myrmecophily in Hallonympha paucipuncta, an endemic butterfly of the Cerrado. Larvae of H. paucipuncta are polyphagous, using at least 19 species of plants in 10 families. All larvae found were being tended by Crematogaster ants. Spatial distribution of larvae and tending ants were strongly aggregated, suggesting an influence of ants on oviposition and/or larval survival. Implications of obligate myrmecophily in the evolution of polyphagy in Riodinidae are discussed.
Lampides boeticus
Obregon et al. (2015) - Lampides boeticus (Linnaeus, 1767) is also a multivoltine and migratory species, which feeds on many species of legumes. Its life cycle has been described by Martin-Cano (1984) and Obregon (2011). It is considered a facultative myrmecophilous lycaenid (Martin-Cano, 1984) and has been observed attended by the ants Camponotus compressus, Camponotus cruentatus, Camponotus sylvaticus, Camponotus foreli, Nylanderia clandestina, Lasius sp., Anoplolepis gracilipes, Plagiolepis sp., Tapinoma melanocephalum, Linepithema humile, Iberoformica subrufa and Crematogaster auberti (Fiedler, 2006; Obregon & Gil-T., 2011; Álvarez et al., 2012). We provide new records of attending ants: Tapinoma nigerrimum, Crematogaster auberti, Tetramorium forte, Aphaenogaster gibbosa and Crematogaster sordidula, all of them observed on larvae feeding on Erophaca baetica in Sierra Morena (southern Spain).
Laeosopis roboris
Obregon et al. (2015) - Laeosopis roboris (Esper, [1793]) is a univoltine and monophagous species on different species of ash trees (Fraxinus spp.). Interaction of the pupal stage with the ant Lasius grandis has been recorded, through which the pupa is protected until adult emergence (Obregon & Gil-T., 2012). Munoz-Sariot, 2011 records Lasius niger as pupa-attending ant. In this study, we found several (n=26) pupa inside Formica gerardi nests, located under large stones at the base of ash trees (Fraxinus angustifolia Vahl, 1804) in June, in Sierra Madrona, southern Ciudad Real province.
Lampides argyrognomon
Mizuno et al. (2018) - Myrmecophilous lycaenid caterpillars have close relationships with their ant hosts by means of various myrmecophilous organs, most of which are usually lost after pupation. However, some lycaenid species, including Lycaeides argyrognomon, maintain such relationships at the pupal stage and go so far as to pupate in ant nests. This invokes the hypothesis that these myrmecophilous lycaenid pupae might have alternative tactics to retain myrmecophilous interactions without ant attacks. Camponotus japonicus, Formica japonica, and Lasius japonicus exhibited distinctive aggressive behaviors against ant cuticular hydrocarbons (CHCs) from different colonies of the same species but few attacks against the crude extract of L. argyrognomon pupae. GC–MS analysis revealed that the pupal cuticular lipids contain not only CHCs but also several long-chained aliphatic aldehydes, including 1-octacosanal and 1-triacontanal, which are absent from larval cuticular lipids. With the addition of synthesized 1-octacosanal and 1-triacontanal to ant CHCs from different colonies of the same species, the aggressive behavior decreased in Camponotus japonicus, and the duration of physical contact shortened in Camponotus japonicus and Formica japonica. However, the behavior of Lasius japonicus remained unaffected after the addition of those aldehydes. These results suggest that the pupae-specific cuticular aldehydes of L. argyrognomon suppress ant aggression even after the loss of certain myrmecophilous organs, though the effects varied depending on the attending ant species. Since L. argyrognomon occasionally pupate in the nests of C. japonicus in the field, the lycaenids might be better adapted to associations with Camponotus japonicus than with the other two ant species studied.
Leptotes pirithous
Obregon et al. (2015) - Leptotes pirithous (Linnaeus, 1767) is a multivoltine, polyphagous and migratory lycaenid (Tolman & Lewington, 1997). For this reason, probably, its association with ants is considered to be loose and facultative (Martin-Cano, 1984). In southern Spain the larvae are frequently found feeding on Erophaca baetica and other legumes during the winter and early spring, although host plants change throughout the year. In November 2013, several third instar larvae attended by Plagiolepis pygmaea and Crematogaster sordidula, were observed on flowering buds of Rosmarinus officinalis Linnaeus, 1753 in Cordoba, on which they fully developed to the adult stage. Interactions with Lasius sp. has been recorded (Maravalhas, 2003), in addition to Crematogaster auberti and Plagiolepis pygmaea (Obregon & Gil-T., 2011).
Phengaris
Sielezniew et al. (2015) - Phengaris (=Maculinea) (Lycaenidae) - Caterpillars develop on specific host plants (depending on species: Thymus or Origanum, Gentiana and Sanguisorba) and complete their development inside the nests of specific red ants (Myrmica sp.) as social parasites feeding on the hosts’ brood, or being fed by trophallaxis (Thomas, 1995).
Polyommatus celina
Obregon et al. (2015) - Polyommatus celina (Astaut, 1879) is a multivoltine lycaenid distributed through the centre and south of the Iberian Peninsula, Balearic Islands, Sicily, Sardinia and Northern Africa (including the Canary Islands). This species was recently separated from P. icarus, a species widely distributed in the Palearctic region (Dinca et al., 2011). Both are common species in Spain and their larvae feed on a wide range of legumes (Fabaceae). Because of its wide distribution, the unresolved aggregate taxon (P. icarus + P. celina) has been recorded (as P. icarus) attended by many species of ants: Myrmica sabuleti, Myrmica lobulicornis, Myrmica tenuispina, Lasius alienus, Lasius niger, Iberoformica subrufa, Formica subpilosa, Formica rufibarbis and Plagiolepis pygmaea (Fiedler, 2006). In the present study the larvae of P. ? celina (tentatively determined as this species and not P. icarus on the basis of wing colour and genitalia of specimens, and also because P. icarus has not been found in the immediate area) were located feeding on Medicago sativa Linnaeus, 1753 and were attended by Camponotus fallax.
Pseudophilotes abencerragus
Obregon et al. (2015) - Pseudophilotes abencerragus (Pierret, 1837) is a univoltine lycaenid with a fragmented distribution and very loose interactions with ants. It has been observed attended by Plagiolepis pygmaea (Obregon & Gil-T., 2012; Obregon et al., 2013) and Crematogaster auberti (Álvarez et al., 2012; Garciabarros et al., 2013). In this work we found Plagiolepis schmitzii attending larvae feeding on Cleonia lusitanica (L.).
Tomares ballus
Obregon et al. (2015) - Tomares ballus (Fabricius, 1787) is a univoltine species, with an early flight period in the south of the Iberian Peninsula where the adults are on the wing in early February (or even in late January), and it is considered a facultatively myrmecophylous species (Downey, 1987; Tolman & Lewington, 1997). Its life cycle has been extensively studied by Jordano et al. (1990) and Obregon (2011). Its association with ants has been previously cited: Plagiolepis pygmaea (Fiedler, 2006) and Crematogaster auberti, Crematogaster sordidula, Iberoformica subrufa, Lasius grandis and Tapinoma nigerrimum (Nylander, 1856) (Obregon & Gil-T., 2011). In this work, it was found in association with other ants: Tetramorium forte, Aphaenogaster gibbosa and Camponotus pilicornis, and we can also confirm its association with P. pygmaea and C. auberti. Larvae and the attending ants were located inside the fruit pods of Erophaca baetica.
Zizeeria knysna
Obregon et al. (2015) - Zizeeria knysna (Trimen, 1862) is a bivoltine lycaenid. The flight period lasts from April toNovember in two generations, and it is most abundant in early autumn. It is a Mediterranean species, flying mostly in wetlands and grasslands near water-courses, reservoir edges and urban parks and gardens. We found several caterpillars at the base of a Tribulus terrestris Linnaeus, 1753 (Zygophyllacea) plant in an urban garden in Córdoba, attended by Lasius niger from a nearby nest. In addition, a final instar caterpillar attended by a major ant of Formica cunicularia was also observed. This lycaenid species was previously recorded attended by Pheidole pallidula (Obregon & Gil-T., 2011), a eurytopic species, and one of the most frequent and abundant ants in the Iberian Peninsula. It seems to be associated with Z. knsyna very often, probably influenced by similar habitat requirements. We observed females actively seeking Fabaceae plants (i.e. Medicago sativa or Trifolium repens) for oviposition near P. pallidula nests, or with the nests at the base of the host plant in the case of T. terrestris.
Notes
Obregon et al. (2015) - Most of the ant species associated with lycaenid caterpillars included in this paper are polyphagous or nectarivorous, which probably facilitates this interaction. Other species of ants with granivorous feeding regimes or with a strictly carnivorous diet are less often found interacting with lycaenid larvae.
The data provided in this paper are valuable for understanding the key ecological interactions of Lepidoptera preimaginal stages with parasitoids and ants, for which detailed and reliable overall information necessarily accrues from many studies such as the one presented here. Interactions between 17 parasitoid taxa with 17 species of Lepidoptera, and nine lycaenid species and 15 ant species are recorded here, for just one relatively small corner of Europe. While some of these biological observations for parasitoids and ants are apparently not previously recorded in the literature, the concept of “new records” is not of great value: what is far more important is that quantitative records are made, as here, with careful evaluation and, crucially, with the deposition of voucher specimens in named depositories that thus allows for the scrutiny of others in cases of doubt. Only through these means will the vast amount of incorrect and questionable data, often replicated by unreferenced transcription, that has accrued in the literature for example for the host ranges of parasitoids (see Shaw, 1993, 1994; Noyes, 1994; Shaw et al., 2009) gradually become marginalized. There is still a long way to go before the strength and specialization, or otherwise, of interactions such as the ones recorded in this paper become as clearly known on as broad a front as - for example - the food plants of butterflies. Nevertheless, we regard that as a highly worthy aim, and progress towards it makes a real contribution to the knowledge necessary for the conservation of these most fragile and vulnerable aspects of biodiversity (Shaw & Hochberg, 2001).
In addition to new data recorded in the ant interactions, it is interesting to note that two of the species of ants, Tetramorium forte and Aphaenogaster gibbosa, had not previously been recorded attending lycaenid caterpillars. The association of the genus Tetramorium and Lycaenidae was previously cited by Fiedler (2006) but he had not identified any Tetramorium species. Some authors have reported that some species of the genus Tetramorium also interact with other insect groups that produce honeydew, such as aphids (Krombein et al., 1979). Regarding the genus Aphaenogaster, there are only two other records of attending caterpillars, Aphaenogaster subterranea and Aphaenogaster japonica (Fiedler, 2006). Our observations of Aphaenogaster gibbosa represent the first records of this species attending lycaenid larvae.
References
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