Saving the injured: Rescue behavior in the termite-hunting ant Megaponera analis

Abstract

Predators of highly defensive prey likely develop cost-reducing adaptations. The ant Megaponera analis is a specialized termite predator, solely raiding termites of the subfamily Macrotermitinae (in this study, mostly colonies of Pseudocanthotermes sp.) at their foraging sites. The evolutionary arms race between termites and ants led to various defensive mechanisms in termites (for example, a caste specialized in fighting predators). Because M. analis incurs high injury/mortality risks when preying on termites, some risk-mitigating adaptations seem likely to have evolved. We show that a unique rescue behavior in M. analis, consisting of injured nestmates being carried back to the nest, reduces combat mortality. After a fight, injured ants are carried back by their nestmates; these ants have usually lost an extremity or have termites clinging to them and are able to recover within the nest. Injured ants that are forced experimentally to return without help, die in 32% of the cases. Behavioral experiments show that two compounds, dimethyl disulfide and dimethyl trisulfide, present in the mandibular gland reservoirs, trigger the rescue behavior. A model accounting for this rescue behavior identifies the drivers favoring its evolution and estimates that rescuing enables maintenance of a 28.7% larger colony size. Our results are the first to explore experimentally the adaptive value of this form of rescue behavior focused on injured nestmates in social insects and help us to identify evolutionary drivers responsible for this type of behavior to evolve in animals.

Keywords: Chemical Communication; Evolution of help; Helping behavior; Injured ant; Predator prey interaction; Pro social behavior; Social insects.

Fig. 1. Injury-type frequencies and handicap in injured M. analis ants.

Box-and-whisker plot showing median (horizontal line), interquartile range (box), distance from upper and lower quartiles times 1.5 interquartile range (whiskers), outliers (>1.5× upper or lower quartile), and significant differences (different letters) for (A) distribution of different injury types being carried by helper ants. Lost limb: ant that lost one or more legs or antennas; Termite clinging: ant that still had a termite clinging to its body; Carried unharmed: ant that appears unharmed to the naked eye (Kruskal-Wallis rank sum test, followed by a Dunn’s test with Bonferroni correction; n = 20 trials with 20 colonies with a total of 154 helped ants). (B) Running speed of ants affected by different injuries and healthy individuals as control (Healthy) (Kruskal-Wallis rank sum test, followed by a Dunn’s test with Bonferroni correction; n = 20 trials with 20 colonies). See also table S1 for detailed statistical results and fig. S1 for illustration of injury types.

Fig. 2. Mortality and predation of injured and handicapped individuals if not rescued.

(A) Percentage of injured and handicapped ants dying during the return journey for the three classified carried ant types and control (Termite clinging, Lost limb, Unharmed, and Healthy) if not helped (n = 20 for each type, total n = 80). (B) Percentages of the different mortality causes during the return journey (n = 21 of 80 died); spider (red): killed by a predatory spider; fatigue (blue): ant stops moving during return journey, most likely because of exhaustion; ant (gray): injured minor carried off/killed by another ant. (C) Handicapped minor with a termite clinging on an extremity carried off by a forager of Paltothyreus tarsatus. (D) Handicapped minor with two termite soldiers clinging on extremities stops moving because of exhaustion after a 52-min return journey. (E) Intermediate with a lost extremity returning alone from the hunting ground ambushed by a Salticidae spider (jumping spider).

Fig. 3. Speed of injured ants at different times after injury.

Box-and-whisker plot showing median (horizontal line), interquartile range (box), distance from upper and lower quartiles times 1.5 interquartile range (whiskers), and significant differences (different letters) of the different running speeds 5 min after removing two legs (Fresh injury) and 24 hours later [Old injury (+24 hours)] and of healthy ants (Healthy) (Kruskal-Wallis rank sum test, followed by a Dunn’s test with Bonferroni correction; n = 20 trials with five colonies). See also table S2 for detailed statistical results.

Fig. 4. Distribution of long-term injuries in different size classes of M. analis.

Box-and-whisker plot showing median (horizontal line), interquartile range (box), distance from upper and lower quartiles times 1.5 interquartile range (whiskers), and significant differences (different letters) for the percentage of ants that lost an extremity in previous raids for majors, intermediates, and minors [analysis of variance (ANOVA), followed by Tukey post hoc test; n = 20]. See also table S3 for detailed statistical results.

Fig. 5. Behavioral responses of helper ants toward different treatments of injured individuals or dummies.

Positive values show clear attempts of help by picking up the ant and dropping it again (black) or carrying it back to the nest (gray). Negative values show behavior in which the ant was disposed of (dragged away from the raiding column or attacked) [Fisher’s exact test for count data between neutral treatment (Healthy) and the other categories; n = 20]. (A) Response toward different injury states. (B) Response at different points of the raid (Way out: on the way toward the termites; Hunting: at the hunting ground; Return: on the return journey after the fight). (C) Response toward dummies (dead minors) treated with different glands (Mg dead: mandibular gland applied on a dummy; Mg alive: mandibular gland applied on a healthy/living ant; Dufours: Dufour’s gland applied on a dummy; Poison: poison gland applied on a dummy). (D) Response toward dummies treated with different synthetic compounds (DMDS/DMTS: 50:50 mixture of DMDS and DMTS; Hexane: pure hexane as control). See also table S4 for detailed statistical results. *P < 0.05; **P < 0.01; ***P < 0.001. n.s., not significant.