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Ants, Cataglyphis Cursor, Use Precisely Directed Rescue Behavior to Free Entrapped Relatives

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Ants, Cataglyphis Cursor, Use Precisely Directed Rescue Behavior to Free Entrapped Relatives Ants, Cataglyphis cursor, Use Precisely Directed Rescue Behavior to Free Entrapped Relatives Elise Nowbahari1*, Alexandra Scohier1, Jean-Luc Durand1, Karen L. Hollis2 1 Laboratoire d’E´thologie Expe´rimentale et Compare´e EA 4443, Universite´ Paris Nord, Villetaneuse, France, 2 Interdisciplinary Program in Neuroscience & Behavior, Mount Holyoke College, South Hadley, Massachusetts, United States of America Abstract Although helping behavior is ubiquitous throughout the animal kingdom, actual rescue activity is particularly rare. Nonetheless, here we report the first experimental evidence that ants, Cataglyphis cursor, use precisely directed rescue behavior to free entrapped victims; equally important, they carefully discriminate between individuals in distress, offering aid only to nestmates. Our experiments simulate a natural situation, which we often observed in the field when collecting Catagyphis ants, causing sand to collapse in the process. Using a novel experimental technique that binds victims experimentally, we observed the behavior of separate, randomly chosen groups of 5 C. cursor nestmates under one of six conditions. In five of these conditions, a test stimulus (the ‘‘victim’’) was ensnared with nylon thread and held partially beneath the sand. The test stimulus was either (1) an individual from the same colony; (2) an individual from a different colony of C cursor; (3) an ant from a different ant species; (4) a common prey item; or, (5) a motionless (chilled) nestmate. In the final condition, the test stimulus (6) consisted of the empty snare apparatus. Our results demonstrate that ants are able to recognize what, exactly, holds their relative in place and direct their behavior to that object, the snare, in particular. They begin by excavating sand, which exposes the nylon snare, transporting sand away from it, and then biting at the snare itself. Snare biting, a behavior never before reported in the literature, demonstrates that rescue behavior is far more sophisticated, exact and complexly organized than the simple forms of helping behavior already known, namely limb pulling and sand digging. That is, limb pulling and sand digging could be released directly by a chemical call for help and thus result from a very simple mechanism. However, it’s difficult to see how this same releasing mechanism could guide rescuers to the precise location of the nylon thread, and enable them to target their bites to the thread itself. Citation: Nowbahari E, Scohier A, Durand J-L, Hollis KL (2009) Ants, Cataglyphis cursor, Use Precisely Directed Rescue Behavior to Free Entrapped Relatives. PLoS ONE 4(8): e6573. doi:10.1371/journal.pone.0006573 Editor: Frederick R. Adler, University of Utah, United States of America Received January 27, 2009; Accepted June 19, 2009; Published August 12, 2009 Copyright: ß 2009 Nowbahari et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: The authors have no support or funding to report. Competing Interests: The authors have declared that no competing interests exist. * E-mail: [email protected] Introduction directed toward any conspecific. In another recent paper [14], ants demonstrated what the authors aptly termed ‘‘cooperative self- Despite the fact that numerous forms of helping behavior have defense’’. That is, when attacked by driver ants, victimized been observed in countless vertebrate species [1], actual rescue of Pachycondyla analis ants engage in counterattack behavior; however, one animal by another, even a conspecific, is extremely rare. In the this counterattack behavior appears to be directed toward all driver earliest, often-cited example of vertebrate rescue behavior, ants, not only to attackers clinging to nestmates’ bodies, but also to dolphins assisted injured conspecifics by supporting them to the driver ants that have not yet attacked. In all other studies to date, the sea surface so that the victims could breathe more easily [2]. rescue behavior was not experimentally studied and the effect of Surprisingly, however, the first published evidence of rescue relatives on rescue behavior remains a mystery – surprisingly so behavior in coalition-forming capuchin monkeys, animals well- given the important explanatory power of kinship in countless other known for their helping behavior, appeared only three years ago forms of cooperative behavior [15,16], as well as newer predictive and was an observational report of a single interaction [3]. models of cooperation and altruism [17]. Indeed, knowledge of In ants, however, invertebrates well known for their highly kinship relations has revolutionized the field of behavioral ecology integrated and complex cooperative behavior, anecdotes of a simple [18]. We therefore studied whether the rescue behavior that we form of rescue behavior, namely sand digging, was described as observed in the field when collecting C. cursor ants would be early as 1874 [4]. Subsequent reports of digging behavior did not re- delivered indiscriminately to all ants in close proximity, only to appear until the mid-1900s [5–11]; however, many of these authors members of the same C. cursor species, or only to nestmates – a described digging as a simple alarm reaction, not rescue per se. question that, at its core, addresses whether the ‘‘call-for-help’’ is Recently, rescue behavior has been reported in Formica workers species-specific or is unique to each ant colony. Using an artificial entrapped in an antlion pit [12], a common predator of many ant nylon snare that simulated a situation in which ants become species [13]. Not only digging, but also limb pulling behaviors were entrapped by collapsing sand and debris, we systematically varied observed; however, both behavioral patterns appeared to be the relationship between victims and rescuers to determine the PLoS ONE | www.plosone.org 1 August 2009 | Volume 4 | Issue 8 | e6573 Rescue Behavior in Ants specificity of a potential victim’s ability to elicit rescue attempts, as nestmate victim than toward any of the remaining test stimuli, well as different strategies of rescuers to free them. namely an ant from a different colony (heterocolonial test), an ant belonging to a different species (heterospecific test), a larval cricket Results (prey test), or, in the two control tests, either a motionless (chilled) nestmate, or an empty snare apparatus (Wilcoxon-Mann-Whitney The behavior of separate, randomly chosen groups of 5 C. cursor U test using Bonferroni’s sequential adjustment method, a = 0.05). nestmates (the potential ‘‘rescuers’’) was observed under one of five Neither condition 5 nor condition 6, both control conditions, conditions in which a test stimulus (the ‘‘victim’’) was ensnared and elicited any behavior from ants and so are combined in Figure S1 held partially beneath the sand, namely (1) a C. cursor nestmate/ (but, of course, not in any of the statistical analyses). relative from the same colony as the potential rescuers (homo- In stark contrast to the rescue behavior elicited by nestmates, C. colonial test), (2) a C. cursor individual from a different colony cursor subjects were highly aggressive toward all other live test (heterocolonial test), (3) an ant from a sympatric (living in close stimuli, except the motionless (chilled) nestmate (Figure. S2), proximity), unrelated species, Camponotus aethiops (heterospecific test), namely an ant from a different colony (heterocolonial test), an ant (4) a larval cricket (prey test), and (5) an ensnared motionless (chilled) belonging to a different species (heterospecific test), or a larval nestmate. A final test (6) consisted of an empty snare apparatus. The cricket (prey test). Here, too, neither condition 5 nor condition 6, snare consisted of a nylon thread, wrapped around the victim’s both control conditions, elicited any behavior from ants and so are pedicel in conditions 1–5, and secured to a 1-cm-diameter round of combined in Figure S2 (but, again, were not combined in any of filter paper. In all conditions the filter paper was concealed beneath the statistical analyses). These aggressive behavior patterns, easily the sand. In conditions 1–5, the head, antennae and thorax were recognizable and observed in previous work with other species of visible above the sand and the victim could move these body parts Cataglyphis [19,21], included threatening with open mandibles, freely; in condition 6, only the nylon snare was visible. Each test formic acid projection (in which formic acid poison was sprayed in stimulus was left in place for 7 minutes and videotaped for later the direction of the test stimulus), dismemberment attempts, and analysis. For each of these six test conditions, in which we varied the biting. Although several rescue and aggressive behavior patterns nature of the test stimulus victim, we conducted 9 independent involved the use of the mandibles, biting and attempts to observations, namely 3 separate samples from each of 3 different C. dismember a body part were easily distinguished from limb cursor colonies. Thus, we conducted a total of 54 tests. For each test, pulling: In aggressive contexts, the gaster (abdomen) was always the group of 5 potential rescuer ants constituted a single statistical flexed, namely curved under the body, in preparation for formic unit. That is, potential ant rescuers were marked individually
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