Lepidoptera

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There are a number of butterflies that live at least part of their life in close association with ant species.

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
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. © Alex Wild.
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.).

Species Associations

Sortable table
Ant Species Butterfly Interaction Stage Reference Remarks
Formica gerardi Purple hairstreak (Favonius quercus) Obregon et al. 2015
Pheidole pallidula Purple hairstreak (Favonius quercus) Obregon et al. 2015
Iberoformica subrufa Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Myrmica scabrinodis Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Crematogaster auberti Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica cinerea Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica selysi Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica fusca Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica pratensis Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica sanguinea Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica forsslundi Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Camponotus aethiops Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Camponotus pilicornis Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Camponotus cruentatus Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Lasius alienus Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Camponotus piceus Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Lasius niger Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Lasius brunneus Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Plagiolepis schmitzii Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Tapinoma erraticum Green Underside Blue (Glaucopsyche alexis) Obregon et al. 2015
Formica gerardi Spanish Purple Hairstreak (Laeosopis roboris) Obregon et al. 2015
Lasius niger Spanish Purple Hairstreak (Laeosopis roboris) Obregon et al. 2015
Lasius grandis Spanish Purple Hairstreak (Laeosopis roboris) Obregon et al. 2015
Aphaenogaster gibbosa Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Camponotus compressus Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Camponotus cruentatus Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Camponotus sylvaticus Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Camponotus foreli Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Nylanderia clandestina Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Anoplolepis gracilipes Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Crematogaster auberti Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Crematogaster sordidula Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Tapinoma melanocephalum Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Tetramorium forte Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Linepithema humile Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Tapinoma nigerrimum Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Iberoformica subrufa Long-tailed blue (Lampides boeticus) Obregon et al. 2015
Crematogaster sordidula Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Iberoformica subrufa Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Plagiolepis schmitzii Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Tapinoma nigerrimum Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Tetramorium forte Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Plagiolepis pygmaea Lang's Short-tailed Blue (Leptotes pirithous) Obregon et al. 2015
Myrmica schencki Large Blue (Phengaris arion) Sielezniew et al. 2010b
Myrmica lonae Large Blue (Phengaris arion) Sielezniew et al. 2010b
Myrmica sabuleti Large Blue (Phengaris arion) Radchenko and Elmes 2010
Myrmica schencki Mountain Alcon Blue (Phengaris rebeli) Sielezniew et al. 2010a
Camponotus fallax P. ¿ celina Obregon et al. 2015
Myrmica sabuleti Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Myrmica lobulicornis Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Myrmica tenuispina Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Lasius alienus Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Lasius niger Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Iberoformica subrufa Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Formica subpilosa Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Formica rufibarbis Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Plagiolepis pygmaea Polyommatus icarus + Polyommatus celina Obregon et al. 2015
Plagiolepis schmitzii False Baton Blue (Pseudophilotes abencerragus) Obregon et al. 2015
Plagiolepis pygmaea False Baton Blue (Pseudophilotes abencerragus) Obregon et al. 2015
Crematogaster auberti False Baton Blue (Pseudophilotes abencerragus) Obregon et al. 2015
Crematogaster auberti Provence hairstreak (Tomares ballus) Obregon et al. 2015
Aphaenogaster gibbosa Provence hairstreak (Tomares ballus) Obregon et al. 2015
Camponotus pilicornis Provence hairstreak (Tomares ballus) Obregon et al. 2015
Crematogaster sordidula Provence hairstreak (Tomares ballus) Obregon et al. 2015
Iberoformica subrufa Provence hairstreak (Tomares ballus) Obregon et al. 2015
Lasius grandis Provence hairstreak (Tomares ballus) Obregon et al. 2015
Tapinoma nigerrimum Provence hairstreak (Tomares ballus) Obregon et al. 2015
Plagiolepis pygmaea Provence hairstreak (Tomares ballus) Obregon et al. 2015
Tetramorium forte Provence hairstreak (Tomares ballus) Obregon et al. 2015
Lasius niger African Grass Blue (Zizeeria knysna) Obregon et al. 2015
Formica cunicularia African Grass Blue (Zizeeria knysna) Obregon et al. 2015
Pheidole pallidula African Grass Blue (Zizeeria knysna) Obregon et al. 2015
Camponotus terebrans Ogyris sp. Braby 2000

Species Accounts

Favonius quercus

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.

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.

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).

Mountain Alcon Blue (Phengaris rebeli)

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.

Obregon et al. 2015. Larva of Zizeeria knysna attended by Pheidole pallidula. Córdoba (Spain).

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

  • Obregon, R., M. R. Shaw, J. Fernandez-Haeger, and D. Jordano. 2015. Parasitoid and ant interactions of some Iberian butterflies (Insecta: Lepidoptera). Shilap-Revista De Lepidopterologia. 43:439-454.
  • Radchenko, A.G. & Elmes, G.W. 2010. Myrmica ants of the Old World. Fauna Mundi 3:1-789.
  • Sielezniew, M., Włostowski, M. & Dziekańnska, I. 2010a. Myrmica schencki (Hymenoptera: Formicidae) as the primary host of Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae) at heathlands in eastern Poland. Sociobiology. 55, 95–106.
  • Sielezniew, M., Patricelli, D., Dziekańska, I., Barbero, F., Bonelli, S., Casacci, L.P., Witek, M. and E. Balletto. 2010b. The first record of Myrmica lonae (Hymenoptera: Formicidae) as a host of the socially parasitic large blue butterfly Phengaris (Maculinea) arion (Lepidoptera: Lycaenidae). Sociobiology. 56:465–475.