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.2011 Mar 29;6(3):e17958.
doi: 10.1371/journal.pone.0017958.

Specialized learning in antlions (Neuroptera: Myrmeleontidae), pit-digging predators, shortens vulnerable larval stage

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Specialized learning in antlions (Neuroptera: Myrmeleontidae), pit-digging predators, shortens vulnerable larval stage

Karen L Hollis et al. PLoS One..

Erratum in

  • PLoS One. 2011;6(4). doi:10.1371/annotation/06bf5d20-9308-4502-ae52-05cb16ac5f11

Abstract

Unique in the insect world for their extremely sedentary predatory behavior, pit-dwelling larval antlions dig pits, and then sit at the bottom and wait, sometimes for months, for prey to fall inside. This sedentary predation strategy, combined with their seemingly innate ability to detect approaching prey, make antlions unlikely candidates for learning. That is, although scientists have demonstrated that many species of insects possess the capacity to learn, each of these species, which together represent multiple families from every major insect order, utilizes this ability as a means of navigating the environment, using learned cues to guide an active search for food and hosts, or to avoid noxious events. Nonetheless, we demonstrate not only that sedentary antlions can learn, but also, more importantly, that learning provides an important fitness benefit, namely decreasing the time to pupate, a benefit not yet demonstrated in any other species. Compared to a control group in which an environmental cue was presented randomly vis-à-vis daily prey arrival, antlions given the opportunity to associate the cue with prey were able to make more efficient use of prey and pupate significantly sooner, thus shortening their long, highly vulnerable larval stage. Whereas "median survival time," the point at which half of the animals in each group had pupated, was 46 days for antlions receiving the Learning treatment, that point never was reached in antlions receiving the Random treatment, even by the end of the experiment on Day 70. In addition, we demonstrate a novel manifestation of antlions' learned response to cues predicting prey arrival, behavior that does not match the typical "learning curve" but which is well-adapted to their sedentary predation strategy. Finally, we suggest that what has long appeared to be instinctive predatory behavior is likely to be highly modified and shaped by learning.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Pit-digging antlions (Myrmeleon sp.).
A larval antlion exposed on the sand surface (top left), and in the process of burying itself under the sand (top right). Bottom: Funnel-shaped antlion pits in fine sand; the winding furrows on the right side of the photograph are the characteristic tracks made by antlions as they search for a suitable pit location. Photography by Cheryl McGraw.
Figure 2
Figure 2. Days to pupation.
Kaplan-Meier survival curves for matched pairs of Learning and Random subjects (n = 36). The data were analyzed using the standard statistic for Kaplan-Meier survival analysis, namely a Mantel-Cox log rank chi-square analysis. That analysis revealed that Learning antlions pupated in significantly less time than Random antlions, χ2 (1,N = 36) = 7.66,p<0.01. Following 70 days of treatment, 79% of Learning antlions pupated (15 of 19), while only 35% of Random antlions pupated (6 of 17). Median survival time, here median days to pupation, corresponding to the time point at which half of the animals remained (i.e., 50% cumulative survival), was 46 days for Learning antlions; median survival time was not reached in Random animals, even by the end of the experiment on Day 70.
Figure 3
Figure 3. Cue-elicited sand-tossing during training.
The mean number of trials (± SEM) per block in which Learning and Random subjects exhibited sand tossing behavior in response to the vibratory cue. Because each subject received 6 days of training per week until it pupated, or until the experiment concluded after 10 weeks (blocks) of training, whichever came first, a score of 6 was the maximum score a subject could obtain. However, each data point represents mean performance based only on those subjects receiving training and, thus, remaining in the experiment because they had not yet pupated.
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References

    1. Topoff H. The pit and the antlion. Nat Hist. 1977;86:64–71.
    1. Mansell MW. Specialized diversity: the success story of the antlions. The Phoenix. 1992;5:20–24.
    1. Mansell MW. Predation strategies and evolution in antlions (Insecta: Neuroptera: Myrmeleontidae). In: Canard M, Aspöck H, Mansell MW, editors. Pure and applied research in neuropterology: Proceedings of the fifth international symposium on neuropterology. Toulouse: Sacco; 1996. pp. 161–169.
    1. Mansell MW. Evolution and success of antlions (Neuropterida: Neuroptera, Myrmeleontidae). Stapfia. 1999;60:49–58.
    1. Griffiths D. Pit construction by ant-lion larvae: A cost-benefit analysis. J Anim Ecol. 1986;55:39–57.

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