Singing caterpillars is a term coined by Philip James DeVries, referring to the fact that the larvae of ant-associated butterfly species of the families Riodinidae and Lycaenidae produce substrate borne sounds that attract ants. The study of these symbiotic associations was pioneered by Phil DeVries in Central America, [1] and Naomi Pierce in Australia. [2] Recently, Lucas Kaminski and collaborators [3] [4] are expanding the studies of riodinid-ant symbioses in Brazil.
Ants that harvest plant secretions also form ecological associations with insects. Several species of such ants tend riodinid and lycaenid caterpillars, and also homopterans (aphids, plant hoppers and relatives). In doing so, ants protect them against potential predators – for example, wasps. Although both riodinid and lycaenid caterpillars attract ants and produce nutritious secretions to reward them, members of the two butterfly families have different structures to perform the same functions.
Typically, ant-associated lycaenid larvae possess a single nectary organ located on the dorsum of the seventh abdominal segment, and a pair of tentacle organs on the eight abdominal segment. [2] Ants imbibe the secretion produced by the nectary organ, and tentacle organs function in chemical communication between caterpillars and ants. The sounds produced by lycaenid caterpillars are similar to those produced by ants, [5] [6] an interesting cross species convergence which facilitates caterpillar-ant communication. Lycaenid caterpillars vary tremendously in their behaviors and level of association with ants. While some species feed on plant tissues, are free-living, and attract ants to their company, others are taken inside ant nests and are fed mouth-to-mouth by ants (trophallaxis), or consume ant brood without being molested. [2]
Ant-associated riodinids have a pair of tentacle nectary organs located dorsally on the eight abdominal segment that produce a secretion rich in sugars and amino acids. [7] [1] When present, anterior tentacle organs seem to release chemical signals to the ants, which in turn become very active. [1] Some species also have balloon setae, inflated structures located on the first segment of the thorax (and projected over the head) that also seem to perform a function in chemical communication. [1] Riodinids are known to make substrate borne sounds in two ways. While most singing riodinid caterpillars produce sound by scraping ribbed vibratory papillae against the rough surface of the head [1] [8] [9] [10] a few riodinids such as E. elvina, achieve the same effect by rubbing the cervical membrane (analogous to a neck) against the head. [11] [12] It has been demonstrated that caterpillars that produce calls are more successful at attracting ants than those of the same species that have been artificially "muted". [13] Furthermore, caterpillars that are guarded by ants have increased survivorship from being effectively protected against predators. [13]
Ecological associations that include the production of a reward are usually interpreted as mutualistic (both partners benefit), but singing caterpillars and their associated ants do not conform to the rule. Secretion-harvesting ants form ecological associations with secretion-producing plants, and typically defend their plant resources from herbivores. However, ant-associated caterpillars successfully wedged themselves between plants and ants: they feed on plant tissue and are nonetheless protected by patrolling ants. Caterpillar secretions have been shown to be more nutritious than those produced by plants, as demonstrated in Thisbe irenea caterpillars and their and Croton host plants; [14] – an efficient way for caterpillars to ensure ant presence and prevent harassment. However, feeding a few individual ants has no measurable benefit to the ant colony as a whole. Caterpillars are actually appropriating individual ants for their own protection, and therefore stopping such ants from performing tasks that would benefit the colony. It could therefore be argued that caterpillar-ant symbioses do not constitute a mutualism as classically defined. Riodinid and lycaenid singing caterpillars are best categorized as ranging from commensal (one partner benefits while the other is not affected) to parasitic.
Caterpillars are the larval stage of members of the order Lepidoptera.
Butterflies are winged insects from the lepidopteran suborder Rhopalocera, characterized by large, often brightly coloured wings that often fold together when at rest, and a conspicuous, fluttering flight. The group comprises the superfamilies Hedyloidea and Papilionoidea. The oldest butterfly fossils have been dated to the Paleocene, about 56 million years ago, though they likely originated in the Late Cretaceous, about 101 million years ago.
Lepidoptera or lepidopterans is an order of winged insects that includes butterflies and moths. About 180,000 species of the Lepidoptera have been described, representing 10% of the total described species of living organisms, making it the second largest insect order with 126 families and 46 superfamilies, and one of the most widespread and widely recognizable insect orders in the world.
A pupa is the life stage of some insects undergoing transformation between immature and mature stages. Insects that go through a pupal stage are holometabolous: they go through four distinct stages in their life cycle, the stages thereof being egg, larva, pupa, and imago. The processes of entering and completing the pupal stage are controlled by the insect's hormones, especially juvenile hormone, prothoracicotropic hormone, and ecdysone. The act of becoming a pupa is called pupation, and the act of emerging from the pupal case is called eclosion or emergence.
The large blue is a species of butterfly in the family Lycaenidae. The species was first defined in 1758 and first recorded in Britain in 1795. In 1979 the species became mostly extinct in Britain but has been successfully reintroduced with new conservation methods. The species is classified as "near threatened" on the IUCN Red List of Threatened Species. Today P. arion can be found in Europe, the Caucasus, Armenia, western Siberia, Altai, north-western Kazakhstan and Sichuan.
The osmeterium is a defensive organ found in all papilionid larvae, in all stages. The organ is situated in the prothoracic segment and can be everted when the larva feels threatened. The everted organ resembles a fleshy forked tongue, and this along with the large eye-like spots on the body might be used to startle birds and small reptiles. The osmeterial organ remains inside the body in the thoracic region in an inverted position and is everted when the larva is disturbed in any way emitting a foul, disagreeable odor which serves to repel ants, small spiders and mantids. To humans, this odour is rather strong but not unpleasant, usually smelling like a concentrated scent of the caterpillar's food plant and pineapple.
Lycaenidae is the second-largest family of butterflies, with over 6,000 species worldwide, whose members are also called gossamer-winged butterflies. They constitute about 30% of the known butterfly species.
Riodinidae is the family of metalmark butterflies. The common name "metalmarks" refers to the small, metallic-looking spots commonly found on their wings. The 1,532 species are placed in 146 genera. Although mostly Neotropical in distribution, the family is also represented both in the Nearctic, Palearctic, Australasian (Dicallaneura), Afrotropic, and Indomalayan realms.
Pyrgus malvae, the grizzled skipper, is a butterfly species from the family Hesperiidae. It is a small skipper (butterfly) with a chequered pattern on its wings that appears to be black and white. This butterfly can be found throughout Europe and is common in central and southern regions of England. The butterfly prefers three major types of habitat: woodland, grassland, and industrial. Referenced as a superspecies, Pyrgus malvae includes three semispecies: malvae, malvoides, and melotis. Eggs are laid on plants that will provide warmth and proper nutrition for development. As larvae, their movement is usually restricted to a single plant, on which they will build tents, unless they move onto a second host plant. Larvae then spin cocoons, usually on the last host plant they have occupied, where they remain until spring. Upon emerging as adult butterflies, grizzled skippers are quite active during the day and tend to favour blue or violet-coloured plants for food. They also possess multiple methods of communication; for example, vibrations are used to communicate with ants, and chemical secretions play a role in mating. Exhibiting territorial behaviour, males apply perching and patrolling strategies to mate with a desired female.
Curetis thetis, the Indian sunbeam, is a species of lycaenid or red butterfly found in Indomalayan realm.
Liphyra brassolis, also known as the moth butterfly, is a butterfly found in South Asia, Southeast Asia and Australia that belongs to the lycaenid family. The larvae are predatory and feed on ant larvae. This is one of the largest species of lycaenid butterflies. Several disjunct populations across its wide distribution range are considered as subspecies. Never a common butterfly, specimens of this species are highly prized by collectors.
Myrmecophily is the term applied to positive interspecies associations between ants and a variety of other organisms, such as plants, other arthropods, and fungi. Myrmecophily refers to mutualistic associations with ants, though in its more general use, the term may also refer to commensal or even parasitic interactions.
Butterfly evolution is the origin and diversification of butterflies through geologic time and over a large portion of the Earth's surface. The earliest known butterfly fossils are from the mid Eocene epoch, between 40-50 million years ago. Their development is closely linked to the evolution of flowering plants, since both adult butterflies and caterpillars feed on flowering plants. Of the 220,000 species of Lepidoptera, about 45,000 species are butterflies, which probably evolved from moths. Butterflies are found throughout the world, except in Antarctica, and are especially numerous in the tropics; they fall into eight different families.
Phengaris rebeli, common name mountain Alcon blue, is a species of butterfly in the family Lycaenidae. It was first found and described in Styria, Austria, on Mount Hochschwab around 1700. Although it was initially classified as a subspecies of P. alcon, a European researcher, Lucien A. Berger, designated it as a separate species in 1946. Genetic similarities between P. rebeli and P. alcon have led many researchers to argue that the two are the same species and differences are due to intraspecific variation.
Philip James DeVries is a tropical biologist whose research focuses on insect ecology and evolution, especially butterflies. His best-known work includes symbioses between caterpillars, ants and plants, and community level biodiversity of rainforest butterflies. DeVries is Professor Emeritus at the University of New Orleans, Research Associate at the American Museum of Natural History (NY), Florida Museum of Natural History (FL), and The Milwaukee Public Museum (WI).
Jalmenus evagoras, the imperial hairstreak, imperial blue, or common imperial blue, is a small, metallic blue butterfly of the family Lycaenidae. It is commonly found in eastern coastal regions of Australia. This species is notable for its unique mutualism with ants of the genus Iridomyrmex. The ants provide protection for juveniles and cues for adult mating behavior. They are compensated with food secreted from J. evagoras larvae. The ants greatly enhance the survival and reproductive success of the butterflies. J. evagoras lives and feeds on Acacia plants, so butterfly populations are localized to areas with preferred species of both host plants and ants.
Eurybia elvina, commonly known as the blind eurybia, is a Neotropical metalmark butterfly. Like many other riodinids, the caterpillars are myrmecophilous and have tentacle nectary organs that exude a fluid similar to that produced by the host plant Calathea ovandensis. This mutualistic relationship allows ants to harvest the exudate, and in return provide protection in the form of soil shelters for larvae. The larvae communicate with the ants by vibrations produced by the movement of its head. The species was described and given its binomial name by the German lepidopterist Hans Stichel in 1910.
Niphanda fusca is a parasitic butterfly primarily found in East Asian countries such as Japan and Korea. It is a "cuckoo-type" parasite of the ant Camponotus japonicus. It utilizes chemical mimicry to trick the host worker ants into adopting it while it is a third-instar caterpillar. From there, it is fed mouth-to-mouth by the worker ants as though it were one of their own young.
Adelotypa annulifera is a species of riodinid butterfly found in South America. It was first described by Frederick DuCane Godman in 1903.