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Various chemical strategies to deceive ants in three Arhopala species (lepidoptera: Lycaenidae) exploiting Macaranga myrmecophytes.

Inui Y, Shimizu-Kaya U, Okubo T, Yamsaki E, Itioka T - PLoS ONE (2015)

Bottom Line: Macaranga myrmecophytes (ant-plants) are generally well protected from herbivore attacks by their symbiotic ants (plant-ants).Behaviorally, the larvae and dummies coated with cuticular chemicals of A. dajagaka were well attended by the plant-ants, especially by those of the host.Our results suggested that conspicuous variations exist in the chemical strategies used by the myrmecophilous butterflies that allow them to avoid ant attack and be accepted by the plant-ant colonies.

View Article: PubMed Central - PubMed

Affiliation: Department of Arts and Sciences, Osaka Kyoiku University, Kashiwara, Osaka, Japan.

ABSTRACT
Macaranga myrmecophytes (ant-plants) are generally well protected from herbivore attacks by their symbiotic ants (plant-ants). However, larvae of Arhopala (Lepidoptera: Lycaenidae) species survive and develop on specific Macaranga ant-plant species without being attacked by the plant-ants of their host species. We hypothesized that Arhopala larvae chemically mimic or camouflage themselves with the ants on their host plant so that the larvae are accepted by the plant-ant species of their host. Chemical analyses of cuticular hydrocarbons showed that chemical congruency varied among Arhopala species; A. dajagaka matched well the host plant-ants, A. amphimuta did not match, and unexpectedly, A. zylda lacked hydrocarbons. Behaviorally, the larvae and dummies coated with cuticular chemicals of A. dajagaka were well attended by the plant-ants, especially by those of the host. A. amphimuta was often attacked by all plant-ants except for the host plant-ants toward the larvae, and those of A. zylda were ignored by all plant-ants. Our results suggested that conspicuous variations exist in the chemical strategies used by the myrmecophilous butterflies that allow them to avoid ant attack and be accepted by the plant-ant colonies.

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Ant responses to Teflon rods applied with cuticular extract of Arhopala larvae.Responses of the first 10 workers toward Teflon rods applied with cuticular crude extract of (a) Arhopala dajagaka, (b) A. amphimuta, and (c) A. zylda, and (d) n-hexane (control) in each trial are plotted. Green, red and blue symbols indicate plant-ant species on Macaranga rufescens, M. trachyphylla, and M. beccariana, respectively. Overlapping symbols are spread laterally. Filled and open symbols indicate trials for combinations of plant-ant species and Arhopala species on the same host plant species and those on the different host plant species, respectively.
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pone.0120652.g004: Ant responses to Teflon rods applied with cuticular extract of Arhopala larvae.Responses of the first 10 workers toward Teflon rods applied with cuticular crude extract of (a) Arhopala dajagaka, (b) A. amphimuta, and (c) A. zylda, and (d) n-hexane (control) in each trial are plotted. Green, red and blue symbols indicate plant-ant species on Macaranga rufescens, M. trachyphylla, and M. beccariana, respectively. Overlapping symbols are spread laterally. Filled and open symbols indicate trials for combinations of plant-ant species and Arhopala species on the same host plant species and those on the different host plant species, respectively.

Mentions: In the ant behavioral assays, the plant-ant responses toward the Teflon rod differed significantly among the three plant-ant species (multinomial logit model fit, likelihood-ratio LR χ2 = 14.77, p = 0.0052) and also among the four types of applied chemicals, i.e. cuticular extract of larvae of the three Arhopala species and n-hexane only (control) (LR χ2 = 97.26, p < 0.0001). The plant-ant species × chemical type interaction was significant (LR χ2 = 42.79, p < 0.001). The workers of the three ant species chiefly ignored the control rods (82%, 92%, and 95% of them on M. rufescens, M. trachyphylla, and M. beccariana, respectively) and rarely attacked them (7%, 4%, and 5% of them on M. rufescens, M. trachyphylla, and M. beccariana, respectively) (S2 Table). Plant-ants of the host species (M. rufescens) antennated rods applied with cuticular extract from A. dajagaka larvae, whereas those of the nonhost species (M. trachyphylla and M. beccariana) frequently exhibited attacking behavior (Fig. 4A, S2 Table). Toward the rods with cuticular extracts from A. amphimuta larvae, both plant-ant species of the host (M. trachyphylla) and nonhost (M. rufescens and M. beccariana) myrmecophyte species showed more frequent aggression toward rods coated with cuticular extracts from A. amphimuta larvae compared with control rods (Fig. 4B, S2 Table). Toward the rods with cuticular extracts from A. zylda larvae, behavioral responses of plant-ants of the host species (M. beccariana) toward rods coated with cuticular extracts of A. zylda larvae were similar to those toward the control rods. Most workers (87.8%) ignored and fewer workers (6.7%) attacked the rods (S2 Table). In contrast, in the plant-ants on the nonhost myrmecophytes of A. zylda (M. rufescens and M. trachyphylla), the frequency of attack toward the rods with cuticular extracts from A. zylda larvae largely increased (22.5% and 13.3% of ants on M. rufescens and M. trachyphylla, respectively) compared with that toward the control rods (Fig. 4C, S2 Table).


Various chemical strategies to deceive ants in three Arhopala species (lepidoptera: Lycaenidae) exploiting Macaranga myrmecophytes.

Inui Y, Shimizu-Kaya U, Okubo T, Yamsaki E, Itioka T - PLoS ONE (2015)

Ant responses to Teflon rods applied with cuticular extract of Arhopala larvae.Responses of the first 10 workers toward Teflon rods applied with cuticular crude extract of (a) Arhopala dajagaka, (b) A. amphimuta, and (c) A. zylda, and (d) n-hexane (control) in each trial are plotted. Green, red and blue symbols indicate plant-ant species on Macaranga rufescens, M. trachyphylla, and M. beccariana, respectively. Overlapping symbols are spread laterally. Filled and open symbols indicate trials for combinations of plant-ant species and Arhopala species on the same host plant species and those on the different host plant species, respectively.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4390302&req=5

pone.0120652.g004: Ant responses to Teflon rods applied with cuticular extract of Arhopala larvae.Responses of the first 10 workers toward Teflon rods applied with cuticular crude extract of (a) Arhopala dajagaka, (b) A. amphimuta, and (c) A. zylda, and (d) n-hexane (control) in each trial are plotted. Green, red and blue symbols indicate plant-ant species on Macaranga rufescens, M. trachyphylla, and M. beccariana, respectively. Overlapping symbols are spread laterally. Filled and open symbols indicate trials for combinations of plant-ant species and Arhopala species on the same host plant species and those on the different host plant species, respectively.
Mentions: In the ant behavioral assays, the plant-ant responses toward the Teflon rod differed significantly among the three plant-ant species (multinomial logit model fit, likelihood-ratio LR χ2 = 14.77, p = 0.0052) and also among the four types of applied chemicals, i.e. cuticular extract of larvae of the three Arhopala species and n-hexane only (control) (LR χ2 = 97.26, p < 0.0001). The plant-ant species × chemical type interaction was significant (LR χ2 = 42.79, p < 0.001). The workers of the three ant species chiefly ignored the control rods (82%, 92%, and 95% of them on M. rufescens, M. trachyphylla, and M. beccariana, respectively) and rarely attacked them (7%, 4%, and 5% of them on M. rufescens, M. trachyphylla, and M. beccariana, respectively) (S2 Table). Plant-ants of the host species (M. rufescens) antennated rods applied with cuticular extract from A. dajagaka larvae, whereas those of the nonhost species (M. trachyphylla and M. beccariana) frequently exhibited attacking behavior (Fig. 4A, S2 Table). Toward the rods with cuticular extracts from A. amphimuta larvae, both plant-ant species of the host (M. trachyphylla) and nonhost (M. rufescens and M. beccariana) myrmecophyte species showed more frequent aggression toward rods coated with cuticular extracts from A. amphimuta larvae compared with control rods (Fig. 4B, S2 Table). Toward the rods with cuticular extracts from A. zylda larvae, behavioral responses of plant-ants of the host species (M. beccariana) toward rods coated with cuticular extracts of A. zylda larvae were similar to those toward the control rods. Most workers (87.8%) ignored and fewer workers (6.7%) attacked the rods (S2 Table). In contrast, in the plant-ants on the nonhost myrmecophytes of A. zylda (M. rufescens and M. trachyphylla), the frequency of attack toward the rods with cuticular extracts from A. zylda larvae largely increased (22.5% and 13.3% of ants on M. rufescens and M. trachyphylla, respectively) compared with that toward the control rods (Fig. 4C, S2 Table).

Bottom Line: Macaranga myrmecophytes (ant-plants) are generally well protected from herbivore attacks by their symbiotic ants (plant-ants).Behaviorally, the larvae and dummies coated with cuticular chemicals of A. dajagaka were well attended by the plant-ants, especially by those of the host.Our results suggested that conspicuous variations exist in the chemical strategies used by the myrmecophilous butterflies that allow them to avoid ant attack and be accepted by the plant-ant colonies.

View Article: PubMed Central - PubMed

Affiliation: Department of Arts and Sciences, Osaka Kyoiku University, Kashiwara, Osaka, Japan.

ABSTRACT
Macaranga myrmecophytes (ant-plants) are generally well protected from herbivore attacks by their symbiotic ants (plant-ants). However, larvae of Arhopala (Lepidoptera: Lycaenidae) species survive and develop on specific Macaranga ant-plant species without being attacked by the plant-ants of their host species. We hypothesized that Arhopala larvae chemically mimic or camouflage themselves with the ants on their host plant so that the larvae are accepted by the plant-ant species of their host. Chemical analyses of cuticular hydrocarbons showed that chemical congruency varied among Arhopala species; A. dajagaka matched well the host plant-ants, A. amphimuta did not match, and unexpectedly, A. zylda lacked hydrocarbons. Behaviorally, the larvae and dummies coated with cuticular chemicals of A. dajagaka were well attended by the plant-ants, especially by those of the host. A. amphimuta was often attacked by all plant-ants except for the host plant-ants toward the larvae, and those of A. zylda were ignored by all plant-ants. Our results suggested that conspicuous variations exist in the chemical strategies used by the myrmecophilous butterflies that allow them to avoid ant attack and be accepted by the plant-ant colonies.

Show MeSH
Related in: MedlinePlus