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, 106 (20), 8251-5

Chemical Signals Associated With Life Inhibit Necrophoresis in Argentine Ants

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Chemical Signals Associated With Life Inhibit Necrophoresis in Argentine Ants

Dong-Hwan Choe et al. Proc Natl Acad Sci U S A.

Abstract

One of the most conspicuous and stereotyped activities of social insects such as ants and honey bees is necrophoresis, the removal of dead colony members from the nest. Previous researchers suggested that decomposition products such as fatty acids trigger necrophoric behavior by ant workers. However, fatty acids elicit both foraging and necrophoric responses, depending on the current nest activities (e.g., feeding or nest maintenance). Furthermore, workers often carry even freshly killed workers (dead for <1 h) to refuse piles before significant decomposition has a chance to occur. Here, we show that the cuticular chemistry of Argentine ant workers, Linepithema humile, undergoes rapid changes after death. When the workers are alive or freshly killed, relatively large amounts of 2 characteristic ant-produced compounds, dolichodial and iridomyrmecin, are present on the ants' cuticle. However, these compounds disappear from the cuticle within about 1 h after death. We demonstrate how this phenomenon supports an alternative mechanism of ant necrophoresis in which the precise recognition and rapid removal of dead nestmates are elicited by the disappearance of these chemical signals associated with life.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.
Fig. 1.
Responses of Argentine ant workers to dead ants and inanimate objects. (A) Box plots of the times between introduction and removal of different test items from the nest. Boxes are bounded by the first quartile, median, and third quartile; whiskers (error bars) above and below the box indicate the 90th and 10th percentiles; and points outside the whiskers are outliers. A group of 10 items was observed for 15 min after introducing the items into the nest entrance. Freshly killed ants were removed more slowly by workers than other test items (Kruskal-Wallis ANOVA for the 4 groups: H = 40.6, df = 3, P < 0.0001). Removal times for corpses 1 h and >24 h old and pieces of filter paper were not significantly different at α = 0.05. All the dead ants were eventually carried to refuse piles, whereas the filter papers were dropped around the nest entrance. (B) A typical necrophoric response of workers to a nestmate corpse. (Scale bar, 1 mm.)
Fig. 2.
Fig. 2.
Worker responses to live pupae treated with cuticular extracts from 1-h-old dead ants. (A) A worker carrying a pupa to the refuse pile. (Scale bar, 1 mm.) (B) Live pupae treated with 1-h-old dead ant extract being carried to the refuse pile (arrows show locations of 9 pupae). (Scale bar, 10 mm.)
Fig. 3.
Fig. 3.
Chemical analyses of ant extracts. (A) TLC plate showing differences in cuticular extracts of live and dead L. humile workers at different times post mortem. L, live ant; L-G, live ant without gaster; F, freshly killed ant; 1h, 1-h-old dead ant. Hydrocarbons (HCs) migrated to the top of the plate. Dolichodial (Dol) and iridomyrmecin (Irid) were found in extracts of live or freshly killed ants but not in extracts from 1-h-old corpses. The absence of Dol and Irid in L-G indicates that these compounds originated from the gasters of workers. All extracts were made from 30 ants extracted in 0.3 mL of methylene chloride, with 10 μL of each extract being applied to the silica gel TLC plate. (B) Chemical structures of dolichodial and iridomyrmecin from Argentine ants, with relative configurations as shown (15, 32). The absolute configurations were not determined. (C) Gas chromatogram showing dissipation/degradation of dolichodial (Dol) and iridomyrmecin (Irid) on the body of ants (split injection, DB-5 column). Extracts were prepared by extracting live or dead ants (n = 30) at different times post mortem (10, 20, 30, 40, 50, and 60 min old) in 0.3 mL of methylene chloride. The amount of Dol and Irid decreased quickly after death, resulting in >50% reduction within the first 10 min after death. The compounds were not detected in extracts of 40-min-old dead ants, whereas the internal standard (St, n-dodecane) in the solvent remained unchanged. Retention times are expressed in minutes.
Fig. 4.
Fig. 4.
Box plots of retrieval times for pupae treated with the dolichodial/iridomyrmecin (Dol+Irid) fraction or solvent controls. Five pupae were observed in each replicate until all had been removed. Workers took longer to retrieve pupae treated with Dol+Irid than solvent-treated controls (Wilcoxon rank-sum test: z = 4.96, P < 0.0001).

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