Roosting ecology and the evolution of bat landing maneuvers

  1. David B. Boerma
  2. Sharon M. Swartz

  • Curated by eLife

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    Evaluation Summary:

    Bat landings are remarkable because they are typically inverted and can involve two, three or four limbs securing the substrate, ranging from cave ceilings to leaves. How different bat species accomplish landing in such a remarkable dynamic fashion and how this ability may have evolved is a mystery. Boersma and Swartz resolved this question by studying how a wide range of bat species land in a unique biomechanics field study conducted across the world, which they complemented with a phylogenetic analysis that provides new insights into how bat landing behavior may have evolved in relation to substrate mechanics. The new evolutionary insight into how bat landing style relates to peak substrate contact force will be of interest to comparative biomechanists, movement ecologists and evolutionary biologists alike. Finally, the markedly different landing strategies for complex natural surfaces may inspire roboticists to design more effective landing and grasping solutions for complex surfaces.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

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Abstract

Biomechanics is poised at the intersection of organismal form, function, and ecology, and forms a practical lens through which to investigate evolutionary linkages among these factors. We conducted the first evolutionary analysis of bat flight dynamics by examining the phylogenetic patterning of landing mechanics. We discovered that bats perform stereotyped maneuvers that are correlated with landing performance quantified as impact force, and that these are linked with roosting ecology, a critical aspect of bat biology. Our findings suggest that bat ancestors performed simple, four-limbed landings, similar to those performed by gliding mammals, and that more complex landings evolved in association with novel roost types. This explicit connection between ecology and biomechanics presents the opportunity to identify traits that are associated with a locomotor behavior of known ecological relevance, thus laying the foundation for a broader understanding of the evolution of flight and wing architecture in this extraordinarily successful mammalian lineage.

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  1. eLife

    Evaluation Summary:

    Bat landings are remarkable because they are typically inverted and can involve two, three or four limbs securing the substrate, ranging from cave ceilings to leaves. How different bat species accomplish landing in such a remarkable dynamic fashion and how this ability may have evolved is a mystery. Boersma and Swartz resolved this question by studying how a wide range of bat species land in a unique biomechanics field study conducted across the world, which they complemented with a phylogenetic analysis that provides new insights into how bat landing behavior may have evolved in relation to substrate mechanics. The new evolutionary insight into how bat landing style relates to peak substrate contact force will be of interest to comparative biomechanists, movement ecologists and evolutionary biologists alike. Finally, the markedly different landing strategies for complex natural surfaces may inspire roboticists to design more effective landing and grasping solutions for complex surfaces.

    (This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. The reviewers remained anonymous to the authors.)

  2. eLife

    Reviewer #1 (Public Review):

    This study provides an evolutionary analysis of the diversity of landing maneuvers performed by bats. The authors describe the distribution of these maneuvers across a range of species in this group, and relate the diversity of landing styles (defined by the number of contact points used) to two other aspects of bat landing behaviours: (1) the impact forces experienced, and (2) the preferred landing substrate. A major strength of this study is the extent of sampling across a wide range of extant bat species, with careful quantification of key features of landing behaviours. The results provide support for two conclusions: (1) bats that make landings with lower impact forces are able to use landing styles with more tenuous contact (i.e., presumed based on there being fewer points of contact between the bat and the landing substrate), and (2) different landing styles exhibited by divergent bat species are associated with the use of different roosting substrates.

    The authors also attempt to use these data to draw conclusions about the origins of bat flight from a gliding ancestor, however, a major weakness is that no alternatives or falsifiable predictions are presented to link origin hypotheses to distinguishing predictions. Without a clearly laid out logic of alternatives (i.e., that there are different predictions that would allow us to distinguish between competing origin models), the present data do not allow us to support or refute these models.

    A second weakness of this article is that the putative causal pathway for the relationship between impact forces and landing style (# of points of contact) is unclear, and needs further setup and interpretation. One might predict that the kinematics of a bat's approach would dictate both the number of points of contact needed, as well as the impact forces experienced upon landing. It is unclear whether this relationship is driven by the fact that slow approaches require few contact points and have lower impact forces, on average. This would align with the authors' findings of the relationship (1) above.

    A third weakness is that the analysis evaluating which substrate categorization best predicts landing style is not fully explained. To begin, the authors could provide a clearer explanation of the aggregation of the roost categories, which I believe is based on descriptions of landing structure geometry. It would strengthen this analysis to include a model with no substrate predictors at all. It was not clear from Table 2 whether the authors had indeed done that already. Including such a model would help establish whether a model with any substrate predictors is better supported than one with no substrate predictors at all. Finally, it was not clear from Table 2 why there are 6 AIC values, but only 2 models described in the Methods text.

  3. eLife

    Reviewer #2 (Public Review):

    In this paper, the authors focus on an often overlooked, but important, aspect in the evolution of flight: the transition from moving in air to the standstill on the landing substrate and how landing strategies are related to the substrate's properties. They do so by studying the landing dynamics (substrate reaction forces) and landing strategies (use of the number of body-parts in landing) in bats in relation to the roosting ecology (substrate type, orientation, mechanical features), while taking account for the phylogenetic constraints. They reconstruct the ancestral state of the landing behaviour, and put the origin of bat flight in this perspective.

    For this purpose, they collected and analysed 3D-high speed video recordings together with 3D substrate reaction forces on an impressive number of species, specimens and trials (665 landings, 96 bats, 35 species, 9 families). The landing strategy and maximal forces at landing were extracted from the raw data and combined with information from the literature on the roosting ecology and the physical substrate properties (categorized). A time-calibrated molecular phylogeny is pruned to the focal taxa.

    The answers provided to the three main questions [i.e., i) are relationships between landing style and impact force consistent across the diverse sample of bats, ii) what is the evolutionary history of bat landing maneuvers, iii) is landing style linked to roosting ecology?] are convincing and conclusive.

    It was suggested to the authors to guide the non-specialist reader a bit more by defining important key-terms and concepts somewhat better.

  4. eLife

    Reviewer #3 (Public Review):

    This study examines bat landing across species and habitats. The data were collected at multiple, international field sites using wild bats which were trained to land at a testing device. An impressive 35 bat species across nine families were measured. Peak force during landing was recorded as the number of appendages that were used during landing (two to four "point" landings). The peak force data (corrected for body weight) and landing points data were analyzed in the context of the phylogenetic relationships of the bats. The roosting ecology was coded for phylogenetic analysis based on the published literature. The authors found that four-point landings had a higher peak force when compared to three-point and two-point landings. The latter had the most consistent and lowest peak forces. Based on phylogenetic reconstruction, they found that four-point landings were the ancestral condition, and two-point landings were more recently evolved. Based on the phylogenetic correlations and model comparisons between landing type and roost type, they found that the two-point landings were more likely to occur in horizontal roosts with stiff materials (e.g., caves), whereas three-point landings were more closely associated with small areas (e.g., leaf tents). They associate the number of points per landing with flight dynamics through the idea that two-point landings are more complex to navigate aerodynamically than four-point landings and three-point landings also require complex aerodynamics associated with navigating tightly constrained landing sites.

    The major strengths of this study are in the rigorous comparative, experimental dataset, the integration with phylogenetic approaches, and the robust and thoughtful manuscript structure that both sets the stage for the complex, and highly integrative study and contextualizes it based on the current literature and the strengths/weaknesses of their analysis approach.

    The major weakness of the study is in the use of peak force as a proxy for landing velocity or, more generally, for the bat's ability to land in a complex aerodynamically controlled way. A minor weakness of the study is the secondary connection of the study to flight aerodynamics.

    Ultimately, the authors do achieve the primary aims of their study and the careful writing of the manuscript largely does appropriately interpret their findings.

    The study is likely to be impactful for the field, given the impressive example of field-based data collection of live animals integrated with phylogeny-based analyses. These kinds of studies are extremely challenging and it is rare to find them integrated within a single study.

  5. Version published to 10.1101/2021.10.21.465259v1 on bioRxiv