Ant, Caterpillar Association

The Nature of the Association


Larvae of species in at least 10 families of the Lepidoptera order associate with ants, and the majority of these are members of the Lycaenidae (second-largest family of butterflies). According to Baylis and Pierce, about half of the Lycaenidae have life histories that are described as being myrmecophilous, or associating with ants. In a review by Konrad Fiedler, he describes that “thus far, representatives of 21 ant genera (30% of the total generic diversity of [the ant genus]) have been found in association with 98 lycaenid butterfly species” (Fiedler 81). Ant association is also commonly found among the species of the closely related taxon, the riodinids, although the frequency may not be as great as in the Lycaenidae. Larval association with ants is clearly a significant component of butterfly ecology, considering Lycaenidae and the riodinids comprise about 30% of the some 17,280 species of butterflies. Lycaenids vary considerably in the strength of their associations with attendant ants. The diets of the lycaenids include fungi, blue-green algae, lichens, ferns, cycads, conifers, bamboos, mistletoes, oaks, and legumes. Because they decide where to lay their eggs, female butterflies ultimately determine the ant environment of the larvae.

With regard to intimacy and specificity of the relationship, lycaenid-ant interactions cover a continuum between 2 extremes. Most lycaenid species do not depend essentially on ant-attendance, although mortality may be significantly reduced through the attendance of ants. In these cases, the relationship is “facultative myrmecophiles.” In these relationships, the dominance pattern within an ant community will determine which ants attend and protect the caterpillars. Essentially, these caterpillars are able to successfully appease a wide range of ant taxa. At the other hand of the continuum are the obligate myrmecophiles which entirely depend on their host ants. In these situations, the caterpillars suffer so intensely from mortality that the populations would most likely go extinct without help from their ant attendants. The obligate relationships are more common with ecologically dominant species of ants that form large, long-lived colonies. (Fiedler). These obligate associations are less common in temeperate zones than in tropical or subtropical realms. An example of this obligate myrmecophilic relationship is one between Plebejus argus attended by Lasius niger.


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Ant feeding off the caterpillar's nectar
http://www.alexanderwild.com/Ants/Taxonomic-List-of-Ant-Genera/Podomyrma/adelaidae2/622273552_6eg3G-S.jpg

Parasitism, Commensalism, or Mutualistism?



The Lycaenid-ant relationship can be parasitic, commensal, or mutualistic. According to the University of Arizona, 97% of interactions are mutualistic. In this association, the larvae have specialized glands that secrete droplets of food that the ants consume. In return, the ants protect the larvae against other potential enemies.
There has been evidence of certain lycaenid species that parasitize ants because they feed on the internal tissue of plants. They do this by chemically mimicking aspects of their recognition signals and fool the ants in to accepting them into the brood chamber of the nest, where they then set about devouring the tissue. Fiedler also emphasizes how sometimes the relationship can turn negative in his review “Ant-associates of Palaerctic lycaenid butterfly larvae.” He states that sometimes the relationship can be asymmetric, when the caterpillars only supply marginal food rewards, yet escape ant and other predator attacks by exploiting the communication system. There has been evidence of the larvae preying on ant brood (young stage of the ant) (Fiedler). In a much simpler form of parasitism, the ant can eat the lycaenid, or the lycaenid can eat the ant.







Communication between the Lycaenid and Ant


The larvae of lycaenids have evolved in several ways in order to properly communicate with their ants. The can produce sounds in the form of stridulations or squeaks that are not always audible to humans. They are transmitted to the ant through the plant that both organisms are on. The pore cupolas of the caterpillar are glands that are thought to alert the ants to the fact that the caterpillar is not prey. The dorsal nectar organ is the specialized gland that secretes the nectar-like substance and the tentacular organs also function in the communication between ant and caterpillar. The caterpillar can “inflate” these organs, causing the structure to be pushed out. When this occurs, a volatile, airborne substance is produced, attracting more ants or retaining them. Another hypothesis of the tentacular organ proposes that they make ants more aggressive or vigilant towards potential predators (University of Arizona).

Lycaenids larvae that are in symbiotic relationships with ants have remarkably thick cuticles that are contoured in ways that protect the vital organs against occasional bites by attendant ants. The larvae stridulate, and these vibrations send important communication signals for their attendant ants. Caterpillars have a pair of tentacular organs found on the eighth abdominal segment which secrete volatile chemicals that appear to mimic ant alarm signals. When researchers studied the secretions, they found they contained a large amount of carbohydrates, including fructose, glucose, sucrose, and trehalose. When researchers looked at the secretions from larvae of Polyommatus hispana, these concentrations ranged from about 13 to 19% by weight, and trace amounts of the amino acid methionine were also found in the secretions. This dorsal organ that secretes nectar droplets provides energy for the ants. This nectar appeases the ants, and in exchange, they gain protection against predators, and the ants themselves that might otherwise be threatening predators (Baylis, Pierce).
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Ant Drinking from the Nectary Organ of the Caterpillar















Ant- Associated Lycaenid vs. Lycaenid


According to researchers, the presence of attending ants was estimated to make a four to 12-fold difference in survival to pupation of the larvae of the lycaenid, Glaucopsyche lygdamus. The degree of protection must take into account the characteristics such as the species of the attendant ant, the density of predators and parasitoids in the occupied habitat, and the life cycles of the different interacting parties. However, ant-associated lycaenid must live with dietary constraints because they not only consume food for their own development, but they must supply a food source for the ant. Some larvae are competing for the attention of ant mutualists with other nectar-secreting sources. Some of these include Homoptera, which are insects that secrete honeydew. With this competition, the larvae may be under pressure to produce rewards that are “more attractive” to ants than the carbohydrates found in most honeydews. This fact is supported by of J. evagoras, where researchers found them to secrete concentrated free amino acids as well as simple sugars. These amino acids have been shown to act as powerful phagostimulants for the attendant ant species, and may ensure that the larvae are continuously protected and tended by the ants, even in the presence of other honeydew-secreting insects.

The presence of attending ants has allowed the larvae to occupy what has been called “enemy-free space,” areas in which the threat of predation has been reduced because of the activities of the ants. As a result of the attendant ant’s presence, the larvae are able to feed in places, or at times of day, which would not be possible without ant protection. Feeding on leaves that are more nutritious and feeding during the day with increased visibility to predators can be a significant advantage to the larvae: the consumption of more nutritious food consistently throughout the day permits shorter development times.

http://www.alexanderwild.com/Ants/Natural-History/Insect-Symbionts/occidentale3/638908572_LFybK-S.jpg
http://www.alexanderwild.com/Ants/Natural-History/Insect-Symbionts/occidentale3/638908572_LFybK-S.jpg


In research conducted by Pierce and Elgar, they compared the diet breadth of 282 species of ant-associated and non-ant-associated lycaenids and found that, in most cases, lycaenids that have a relationship with ants feed on a greater number of host plant families and genera than their non-ant-attended counterparts.
When looking at the growth rate of the caterpillars that are attended by ants and those who are not, Baylis and Pierce state that the final instar larvae reared with ants had a significantly lower growth rate than the larvae reared alone. It appears that “they simply bear the loss by growing less” (Baylis and Pierce 412). This suggests that some species are unable to compensate for the nutrient loss, when they provide the nectar for the ant.

Larvae on plants where ant densities are high pupate (certain life stage of the butterfly) in higher locations than larvae on plants where ant densities are low.


http://eebweb.arizona.edu/animal_behavior/lycaenids/lycaen13_DNO1.htm





Further Research


In a study conducted at the University of Toronto in Canada, researchers discovered that when Lycaenid caterpillars feel threatened, they increase their production of nectar to entice the ants to stick around and protect them. In this study, the team gently squeezed the lycaenid caterpillars with tweezers that were meant to mimic an ant attack. Caterpillars surrounded by an ant oozed twice as much sugar as they normally do when being “groomed.” The ants, in turn, spent 30% more time tending to the caterpillars than their peers grooming the unsqueezed caterpillars. This activity demonstrates an “inducible defense” found in the caterpillar-ant relationship (Erdmann).


Sources:

"Animal Behavior: Caterpillar-Ant Communication." Ecology & Evolutionary Biology at the University of Arizona. The University of Arizona, n.d. Web. 8 Apr. 2011. <http://eebweb.arizona.edu/animal_behavior/lycaenids/lycaen1.htm
Baylis, Matthew, and Naomi Pierce. "12." The Effects of Ant Mutualism. 1993. 405-417.
Erdmann, Jeanne. "Ants Welcome at Caterpillar Picnics." ScienceNOW (2000)
Fiedler, Konrad. "Ant-associates of Palaearctic lycaenid butterfly larvae (Hymenoptera: Formicidae; Lepidoptera: Lycaenidae)-a Review." Myrmecologische Nachrichten 9 (2006): 77-87