Echolocating bats prefer a high risk-high gain foraging strategy to increase prey profitability

  1. Laura Stidsholt
  2. Antoniya Hubancheva
  3. Stefan Greif
  4. Holger R. Goerlitz
  5. Mark Johnson
  6. Yossi Yovel
  7. Peter T. Madsen

  • Curated by eLife

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    eLife assessment

    This study presents important findings on the hunting strategies and energy intake of a bat in the wild. It combines several methods (biologging, captive experiment, and DNA metabarcoding) to provide convincing evidence for the claims. While relevant for researchers in the broad field of animal ecology, in its the current form, the significance of the results may be hard to appreciate for a general audience.

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Abstract

Most bats catch nocturnal prey during active flight guided by echolocation but some species depart from this ancestral behaviour to capture ground prey using passive listening. Here, we explore the costs and benefits of these hunting transitions by combining high-resolution biologging data and DNA metabarcoding to quantify the relative contributions of aerial and ground prey to the total food intake of wild greater mouse-eared bats. We show that these bats use both foraging strategies with similar average nightly captures of 25 small, aerial insects and 30 large, ground-dwelling insects per bat, but with higher capture success in air (78 % in air vs 30 % on ground). However, owing to the 3 to 20 times heavier ground prey, 85 % of the estimated nightly food acquisition comes from ground prey despite the 2.5 times higher failure rates. Further, we find that most bats use the same foraging strategy on a given night suggesting that bats adapt their hunting behaviour to weather and ground conditions. We conclude that prey switching matched to environmental dynamics plays a key role in covering the energy intake even in specialised predators.

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  1. eLife

    Author Response

    Reviewer #1 (Public Review):

    This study combines the biologging method with captive experiments and DNA metabarcoding to detail the hunting behavior of a bat species in the wild. Specifically, it shows that bats use two foraging strategies (echolocating small prey in the air and capturing large ground prey with passive listening) with different success rates and energetic gains. This result highlights that a species believed to be a specialist forager can, in fact, have mixed strategies depending on the condition and environment.

    The detailed foraging behavior they show for such a small animal is impressive. A combination of several different methods, including captive experiments, is a major strength of the paper. I especially like the mastication sound analysis, although I don't know how new it is. However, I have a major concern about the presentation of this study. The manuscript is apparently written for a bat community, and it's hard to understand the significance of the results in the field of animal ecology.

    Thank you for your helpful feedback. We agree that the framing of the ms was too narrow for the audience of eLife, and we have framed the introduction for a broader audience of animal ecology.

    Reviewer #2 (Public Review):

    This paper has huge potential for influencing the way we think about bats as foragers. But, I think that it can be improved.

    Specifically, there is no clearly articulated hypothesis underlying the work. Second, there should be specific testable predictions arising from the hypothesis. This change, while relatively minor, will vastly improve the focus of the work, and hence its impact on the reader.

    Thank you highlighting the need for clear hypotheses. We have added three specific hypotheses to guide the reader (line: 54-56) in the introduction. We have also reformatted the discussion section to address each hypothesis in succession using subheadings with clear take home messages (line: 223-224, 271-272, 293, 318)

    Reviewer #3 (Public Review):

    The study addresses a tough question in the study of wild bats: what and where they eat, using both acoustic bio-logging and DNA metabarcoding. As a result, it was found that greater mouse-eared bats made more frequent attack attempts against passively gleaning prey with lower predation success but higher prey profitability than aerial hawking with higher predation success. This is a precious study that reveals essential new insights into the foraging strategies of wild bats, whose foraging behavior has been challenging to measure. On the other hand, the detection of capture attempts, success or failure of predation, and whether it was by passively gleaning prey or aerial hawking were determined from the audio and triaxial accelerometer analysis, and all results of this study depend entirely on the veracity of this analysis. Also, although two different weights and a tag nearly 15% of its weight were used, it is essential for the results of this data that there be no effect on foraging behavior due to tag attachment. Since this is an excellent study design using state-of-the-art methods and very valuable results, readers should carefully consider the supplemental data as well.

    Thank you for the kind words. We agree that it is critically important that the two foraging strategies are un-affected by tagging effects. In the revised ms, we have added tag weights, tag types and change in body weight during instrumentation as explanatory factors in out statistical models and found no effect of the tag weight on our results. We have also addressed this important issue in the method section (model 1: line 520-539, model 3: 568-590).

  2. eLife

    eLife assessment

    This study presents important findings on the hunting strategies and energy intake of a bat in the wild. It combines several methods (biologging, captive experiment, and DNA metabarcoding) to provide convincing evidence for the claims. While relevant for researchers in the broad field of animal ecology, in its the current form, the significance of the results may be hard to appreciate for a general audience.

  3. eLife

    Reviewer #1 (Public Review):

    This study combines the biologging method with captive experiments and DNA metabarcoding to detail the hunting behavior of a bat species in the wild. Specifically, it shows that bats use two foraging strategies (echolocating small prey in the air and capturing large ground prey with passive listening) with different success rates and energetic gains. This result highlights that a species believed to be a specialist forager can, in fact, have mixed strategies depending on the condition and environment.

    The detailed foraging behavior they show for such a small animal is impressive. A combination of several different methods, including captive experiments, is a major strength of the paper. I especially like the mastication sound analysis, although I don't know how new it is. However, I have a major concern about the presentation of this study. The manuscript is apparently written for a bat community, and it's hard to understand the significance of the results in the field of animal ecology.

  4. eLife

    Reviewer #2 (Public Review):

    This paper has huge potential for influencing the way we think about bats as foragers. But, I think that it can be improved.
    Specifically, there is no clearly articulated hypothesis underlying the work. Second, there should be specific testable predictions arising from the hypothesis. This change, while relatively minor, will vastly improve the focus of the work, and hence its impact on the reader.

  5. eLife

    Reviewer #3 (Public Review):

    The study addresses a tough question in the study of wild bats: what and where they eat, using both acoustic bio-logging and DNA metabarcoding. As a result, it was found that greater mouse-eared bats made more frequent attack attempts against passively gleaning prey with lower predation success but higher prey profitability than aerial hawking with higher predation success. This is a precious study that reveals essential new insights into the foraging strategies of wild bats, whose foraging behavior has been challenging to measure. On the other hand, the detection of capture attempts, success or failure of predation, and whether it was by passively gleaning prey or aerial hawking were determined from the audio and triaxial accelerometer analysis, and all results of this study depend entirely on the veracity of this analysis. Also, although two different weights and a tag nearly 15% of its weight were used, it is essential for the results of this data that there be no effect on foraging behavior due to tag attachment. Since this is an excellent study design using state-of-the-art methods and very valuable results, readers should carefully consider the supplemental data as well.

  6. Version 1 published on bioRxiv