Date Published: January 17, 2019
Publisher: Public Library of Science
Author(s): Gabriela Pérez-Lachaud, Franklin H. Rocha, Javier Valle-Mora, Yann Hénaut, Jean-Paul Lachaud, Kleber Del-Claro.
A diversity of arthropods (myrmecophiles) thrives within ant nests, many of them unmolested though some, such as the specialized Eucharitidae parasitoids, may cause direct damage to their hosts. Ants are known to discriminate between nestmates and non-nestmates, but whether they recognize the strength of a threat and their capacity to adjust their behavior accordingly have not been fully explored. We aimed to determine whether Ectatomma tuberculatum ants exhibited specific behavioral responses to potential or actual intruders posing different threats to the host colony and to contribute to an understanding of complex ant-eucharitid interactions. Behavioral responses differed significantly according to intruder type. Ants evicted intruders that represented a threat to the colony’s health (dead ants) or were not suitable as prey items (filter paper, eucharitid parasitoid wasps, non myrmecophilous adult weevils), but killed potential prey (weevil larvae, termites). The timing of detection was in accordance with the nature and size of the intruder: corpses (a potential source of contamination) were detected faster than any other intruder and transported to the refuse piles within 15 min. The structure and complexity of behavioral sequences differed among those intruders that were discarded. Workers not only recognized and discriminated between several distinct intruders but also adjusted their behavior to the type of intruder encountered. Our results confirm the previously documented recognition capabilities of E. tuberculatum workers and reveal a very fine-tuned intruder discrimination response. Colony-level prophylactic and hygienic behavioral responses through effective removal of inedible intruders appears to be the most general and flexible form of defense in ants against a diverse array of intruders. However, this generalized response to both potentially lethal and harmless intruders might have driven the evolution of ant-eucharitid interactions, opening a window for parasitoid attack and allowing adult parasitoid wasps to quickly leave the natal nest unharmed.
Ants are among the most diverse and abundant organisms on earth. Their complex nests and colonies provide both rich, homeostatic microhabitats and available resources that are exploited by other organisms [1–3]. Despite the aggressive behavior and sophisticated defense strategies of most ant species, many organisms (termed in general myrmecophiles) have managed to deal with ant aggressiveness and bypass their defense strategies [2,4–7]. In response, ants have evolved a suite of physiological, immunological and behavioral defensive responses to counter exploitation by micro- and macro-parasites both at the individual and the colony level [8–13].
Recognition is a basic, major component of biological systems, allowing the distinction of self from non-self and the identification of different classes of non-self , and is particularly important in the context of prey/predator discrimination. Like most other social insects, workers of E. tuberculatum discriminate between nestmates and non-nestmates ; they are also able to discriminate their sibling species, the inquiline social parasite E. parasiticum Feitosa & Fresneau, from their conspecifics . In this study we experimentally demonstrated that E. tuberculatum workers were, in addition, able to recognize and discriminate among several distinct potential or actual intruders and that they further adjusted their behavior to the type of intruder encountered in the nest. As expected, workers readily discriminated between potential prey and other types of intruders (almost 90% of potential prey were effectively preyed on during the 15 min observation period). This contrasted with the quick removal of the rest of intruders tested here, including those that represented a sanitary risk (dead ants) as well as filter paper, pentane-washed parasitoid wasps, and adult weevils, i.e., all intruders that apparently were of no value as edible items. Similarly, in a previous study , inedible live eucharitid parasitoids were quickly removed from the nest. Although there was a high variance in response between the colony fragments tested here, the proportion and type of intruders that were removed/predated were consistent across the four colonies tested. Inter-individual and/or colony personality may explain the observed variability [72,73]. A remarkable consistency in the response of ants was similarly observed in a previous study , that included observations on several colonies collected in different years.