Open access

Sexual dimorphism in bat wing morphology — variation among foraging styles

Publication: Canadian Journal of Zoology
14 August 2021


Sexual dimorphism can lead to differences in foraging style among conspecifics due to morphological differences. Within bats, maneuverability and speed of flight are influenced by wing shape and size, which may differ between sexes. Female bats gain about 30% of their body mass during pregnancy, affecting their agility and flight efficiency. To fill the same foraging niche as males, pregnant female bats would require wing size and (or) shape modifications to maintain maneuverability. We investigated sexual dimorphism in bat wing morphology and how it varies among foraging guilds. Wing photos of male and female adult bats (19 species) in Canada, Belize, and Dominica were analyzed using two-dimensional geometric morphometrics, wing loading, and aspect ratios. Nonpregnant female bats had higher wing loading than males, suggesting that they are less maneuverable than males. Additionally, mass increases during pregnancy may not permit female bats to forage as male conspecifics do. Wing shape differed minimally among foraging guilds with only frugivores differing significantly from all other guilds. Further studies should investigate how female bats forage during their reproductive cycle and determine how frugivore wings differ and whether there are individual differences in wing shape that are not consistent among bat species.


Le dimorphisme sexuel peut mener à différents styles de quête de nourriture chez des individus d’une même espèce en raison de différences morphologiques. Chez les chauves-souris, la capacité de manœuvre et la vitesse de vol sont influencées par la forme et la taille des ailes, qui peuvent varier selon le sexe. La masse corporelle des chauves-souris femelles augmente d’environ 30 % durant la gestation, ce qui a une incidence sur leur agilité et l’efficacité de leur vol. Pour occuper la même niche de quête de nourriture que les mâles, des modifications de la taille ou de la forme des ailes des femelles gestantes seraient requises pour leur permettre de maintenir leur capacité de manœuvre. Nous avons examiné le dimorphisme sexuel de la forme des ailes de chauves-souris et ses variations entre différentes guildes de quête de nourriture. Des photos d’ailes de chauves-souris (19 espèces) adultes mâles et femelles au Canada, au Belize et en Dominique ont été analysées en utilisant la morphométrie géométrique bidimensionnelle, la charge alaire et l’allongement. La charge alaire des femelles non gestantes était plus grande que celles des mâles, ce qui indiquerait qu’elles ont une moins grande capacité de manœuvre que les mâles. L’augmentation de leur masse durant la gestation pourrait en outre ne pas permettre aux femelles de chercher de la nourriture de la même manière que les mâles. La forme des ailes variait très peu entre différentes guildes de quête de nourriture, seules les chauves-souris frugivores étant significativement différentes de toutes les autres guildes. D’autres études devraient se pencher sur le mode de quête de nourriture des chauves-souris femelles durant leur cycle de reproduction et déterminer en quoi les ailes de frugivores sont différentes et s’il existe des différences individuelles de la forme des ailes qui ne sont pas uniformes au sein d’espèce de chauves-souris. [Traduit par la Rédaction]


Sexual dimorphism is found in many species, resulting in differences in morphology between sexes (Hedrick and Temeles 1989; Pasinelli 2000). These morphological differences can lead to differences in foraging behaviour, diet, or even habitat use as each sex displays different traits that are better adapted to different conditions and are constrained by different factors (Hedrick and Temeles 1989; Shine et al. 1996; Pasinelli 2000; Safi et al. 2007). The degree of sexual dimorphism that is seen can be influenced by the conditions experienced by species, such as the environment that they are in (Butler and Losos 2002; Spoljaric and Reimchen 2008) or competitive pressures (Slatkin 1984). Within the mammalian order Chiroptera (bats), maneuverability and speed of flight are influenced by morphology, which may differ between sexes and affect aspects of their ecological niche such as foraging style.
Bats are the only mammalian order that has evolved true flight, due to the elongation of the metacarpals and phalanges producing a wing membrane, over which lift and thrust are able to be produced (Hedenstrom and Johansson 2015). Although flight provides many benefits to bats, such as being able to exploit prey and habitats that other mammals cannot, it has many associated challenges, including overcoming drag and gravity, while maintaining locomotor efficiency (Norberg and Rayner 1987; Hedenström et al. 2009; Hedenstrom and Johansson 2015).
Efficient flight is necessary to optimize the amount of energy being consumed through foraging, which will differ among various foraging styles (Norberg and Rayner 1987; Hedenstrom and Johansson 2015). Foraging styles are constrained by limitations on flight speed and maneuverability, which is influenced by wing shape and their body size, affecting their ability to initiate turns (Norberg and Rayner 1987; Barclay and Brigham 1991; Schulz 2000; Hedenstrom and Johansson 2015). Maneuverability is commonly quantified using measures of wing loading (weight divided by wing surface area) and aspect ratio (square of the wingspan divided by wing surface area; Norberg and Rayner 1987).
Wing loading influences maneuverability and the minimum flight speed needed to produce lift, with lower wing loading typically being found among slower flying and more maneuverable bats, as they have a larger surface area for their mass and can maintain lift with slower flight (Norberg and Rayner 1987). Bats with high wing loading are often fast flying bats with poor maneuverability, as there is a heavier mass relative to wing area and fast flight is needed to maintain lift (Norberg and Rayner 1987). Aspect ratio affects flight speed and efficiency, such that bats with a low aspect ratio are often more maneuverable and fly at slower speeds, whereas bats with high aspect ratios are more efficient, produce less induced drag, but must fly faster to maintain lift, and it is metabolically costly to perform complex flight maneuvers (Norberg and Rayner 1987; Voigt and Holderied 2012).
The majority of bats are insectivores (including those that consume various arthropod orders), frugivores (including those that consume plant material other than nectar and pollen), or nectarivores (consume nectar and pollen), with unique maneuverability constraints (Norberg and Rayner 1987; Hourigan et al. 2010; Voigt and Holderied 2012; Bolzan et al. 2015). Insectivorous bats forage in many different habitats, which can be coarsely divided into aerial insectivores, who typically forage in large open spaces, and gleaners, who capture insects off surfaces within cluttered foliage (Schnitzler and Kalko 2001). Insectivorous gleaners need to be maneuverable when foraging to ensure that they do not harm themselves on the clutter or the surface that their prey is on, so they typically have low aspect ratios and wing loading, enabling them to have slow controlled flight through cluttered spaces (Norberg and Rayner 1987; Schulz 2000; Hackett et al. 2014; Hedenstrom and Johansson 2015). In contrast, aerial insectivores often have higher aspect ratios and wing loading, making flight more efficient and faster, but lowering their maneuverability (Aldridge and Rautenbach 1987; Norberg and Rayner 1987). Faster flight associated with higher wing loading also increases prey encounter rate, so that aerial insectivores can encounter a comparable amount of insects as insectivores gleaning in insect-dense foliage do, but this may be to make up for high metabolic costs if aerial insectivores attempt to forage using the complex flight maneuvers that gleaners do (Aldridge and Rautenbach 1987; Kalcounis and Brigham 1995; Voigt and Holderied 2012). Nectarivores and frugivores require enough maneuverability to fly through cluttered areas to access food sources; however, they may need to momentarily hover to access their food source (Vogel 1958; Aldridge and Rautenbach 1987; Norberg and Rayner 1987). If hovering is necessary to their foraging behavior, then it would likely be associated with a lower wing loading and aspect ratios to enable efficient hovering, whereas higher wing loading and aspect ratios would allow fast, efficient flight to cover large distances to access food sources (Norberg and Rayner 1987).
All therian mammals are viviparous, giving birth to live young. Pregnant female bats gain around 30% of their nonpregnant mass as their fetus develops (Norberg and Rayner 1987; Aldridge and Brigham 1988). Increases in mass due to pregnancy will affect the ability of female bats to maneuver because it will lead to an increase in wing loading (Davis 1969; Norberg and Rayner 1987; Aldridge and Brigham 1988; Hughes and Rayner 1993). As the maneuverability of a pregnant female changes, their ability to forage efficiently may change as well. For pregnant female bats to fill the same ecological niche as males, females would require morphologically distinct wings to maintain maneuverability when foraging in cluttered habitats. New research within in a single species (the little yellow-shouldered bat, Sturnira lilium (E. Geoffroy, 1810)) suggests that females have differing wing shapes, which may help to account for maintaining faster, maneuverable flight during pregnancy (Camargo and Oliveira 2012), but how these trends relate to other species, as well as species with differing diets, has not been investigated.
Our study investigated how wing shape varies between male and female bats of various foraging guilds through examination of 19 different species from Belize (n = 7), Canada (n = 5), and Dominica (n = 8). We hypothesized that sex and foraging guild would cause differences in wing morphology among bat species due to different morphological restrictions of flight needed for different diets. We predicted that (i) wings will be shorter and broader for foraging guilds requiring more maneuverability in flight; (ii) shape would differ between male and female bats so that female wings would be shorter and broader, allowing females higher maneuverability to compensate for increased mass during pregnancy; (iii) there will be greater sexual dimorphism in wing morphology within gleaning species compared with non-gleaning species, so females are maneuverable enough to glean during pregnancy; and (iv) female bats would have lower wing loading when they are not pregnant and would have lower aspect ratios to compensate for increased mass during pregnancy.

Materials and methods

Field sites were located in the Orange Walk District near the village of Indian Church, Belize (17°45′07.6″N, 88°39′14.2″W); Kananaskis Country near the Biogeoscience Institute: Barrier Lake Field Station, Kananaskis Country, Canada (51°01′39.9″N, 115°02′03.6″W); Calgary, Alberta, Canada (51°03′01.2″N, 114°03′43.0"W); Castle Provincial Park, Alberta, Canada (49°24′55.9″N, 114°19′09.8″W); and on the island of Dominica (15°18′01.9″N, 61°23′08.7″W). Mist nets were set up in bat flyways, trails, and roads to capture bats. Once captured, bats were placed into cloth bags for approximately 1 h before they were processed to allow for digestion and excretion of previously consumed prey (Kunz and Whitaker 1983; Maucieri and Barclay 2021). This ensured an accurate body mass that would not be influenced by previous feeding. Body mass (battery powered scale or a spring scale), sex, reproductive condition (pregnant if presence of fetus could be detected by feeling each female bat’s abdomen and not pregnant if the female bat’s abdomen felt thin and empty), age (based on the fusion of metacarpal–phalangeal joint epiphyses; Brunet-Rossinni and Wilkinson 2009), and species was determined for each bat (Table 1). Additionally, each bat had a ventral or dorsal wing photo taken of its left wing (unless the left had any healed fractures or breaks in the wing bones, in which case the right wing was photographed; n = 4) and tail wing (tail membrane) stretched out across grid paper with a ruler for scale. Photos and measurements in Belize (Forest Department permit #WL/2/1/18 (20)) and Canada (Alberta Tourism, Parks and Recreation permit #18-461) were collected by D.G. Maucieri (= 155), whereas data from Dominica were collected by L. Sims (n = 50; Table 1; Ministry of Environment Climate Resilience Disaster Management and Urban Renewal permit reference #286).
Table 1.
Table 1. Samples sizes and locations of species analyzed.
Each species was categorized into one of four foraging guilds: insectivore gleaner (1 species, 10 individuals), aerial insectivore (12 species, 158 individuals), or frugivore (5 species, 27 individuals; Table 1). Foraging guild classification was based on current knowledge of the dominant foraging style that is used by each species for the majority of their time foraging. We acknowledge that species can often employ many methods of foraging given various circumstances, so we verified differences in foraging guilds, especially between the insectivore guilds, by testing if wing loading and aspect ratio differed between groups, suggesting differences in morphological constraints and abilities, using permutation tests, as specified below (Norberg and Rayner 1987; Schnitzler and Kalko 2001; Dávalos 2007; Lopez and Vaughan 2007).
Wing length (measured from wingtip, through the elbow to the body axis) and the surface area of the wing (estimated by connecting the outer landmarks and taking the area of that polygon) were also measured for each wing (see Supplementary Fig. S1).1 This estimation of wing surface area based on homologous landmarks was used for efficiency of data processing while still being comparable between individuals and species (see Supplementary Fig. S1).1 Wing loading (N/m2) was calculated for every nonpregnant bat by dividing its weight by the surface area of its wing. Aspect ratio was calculated by dividing the square of the wingspan by the wing surface area of the wing.
Wing photos were landmarked using a pre-determined landmark scheme consisting of 19 landmarks (see Supplementary Fig. S1)1 using Fiji version 2.0.0 (Schindelin et al. 2012). This landmark scheme was developed to capture wing shape through homologous elements among individual bat wings because bat species share the same forelimb, metacarpal, and phalangeal bones (Zelditch et al. 2004). Type I and II landmarks were used in this study (Bookstein 1997), with 11 at hand bone joints, 6 at the distal tips of phalanges or caudal vertebrae, and 2 along the midline at the shoulders and hips (see Supplementary Fig. S1).1 All other analyses were conducted in RStudio (R version 4.0.1; R Core Team 2020).
To ensure that exclusively shape variation was captured in landmark configurations, specimens were translated, rotated, and scaled to a centroid size of zero using Procrustes generalized least squares superimposition with the “geomorph” package (Zelditch et al. 2004; Webster and Sheets 2010; Adams and Otárola‐Castillo 2013; Adams et al. 2020). Following superimposition, static allometry (influence of size on shape variation independent of ontogenetic change; Hallgrimsson et al. 2015) was evaluated in the wing shape data with a multivariate regression of shape against log centroid size (Klingenberg 2016). Significant allometry was accounted for by using allometric regression residuals as size corrected landmark coordinates (Klingenberg 2016).
Principal components analysis (PCA) was performed on superimposed coordinates to visualize the wing shape morphospace among the species studied (Zelditch et al. 2004; Webster and Sheets 2010; Adams and Otárola‐Castillo 2013) and Procrustes ANOVA was used to evaluate differences between sex and foraging guild on wing shape. A subsequent disparity analysis was conducted to examine how foraging guilds differed in shape using the package “dispRity” (Guillerme 2018). Additionally, canonical variate analysis (CVA) from the “Morpho” package (Schlager 2017) was used to determine the accuracy of the landmark scheme for classifying specimens to the correct foraging guild or sex based on wing shape if a significant main effect of sex and (or) diet was found (Zelditch et al. 2004; Webster and Sheets 2010). CVA was also used to visualize the maximum possible between group differences for foraging guilds in morphospace.
A two-sample t test was used to assess the difference in wing loading between pregnant and nonpregnant female bats. There was a significant difference in the wing loading of pregnant and nonpregnant females, so only nonpregnant bats were used in further analyses. To examine variability in aspect ratio and wing loading, we fitted multifactor ANOVAs with sex and foraging guild as factors. To meet assumptions of normality, wing loading was log transformed during analysis. Additionally, species nested in foraging guilds was included as a covariate. Permutation tests were used to analyze a priori hypotheses regarding sexual dimorphism, the differences in aspect ratio and wing loading among foraging guilds, and verify classification of insectivores into two separate foraging guilds based on morphological constraints and abilities.
It is important to note that our landmark scheme evaluated homologous skeletal elements among the bat species studied, not the area of the wing directly. In contrast to this, aspect ratio and wing loading took the area of the wing into account. Aspect ratio, wing loading, and the landmark scheme all represented aspects of wing shape, but they were not directly comparable with one another. The landmark scheme did not take the full area of the wing outline into account because landmark schemes should be based on homology (Bookstein 1997; Zelditch et al. 2004), not characteristics (the area of the wing) that may be due to convergent evolution as a result of foraging strategy (Marinello and Bernard 2014). Additionally, as a result of the Procrustes generalized least squares superimposition, size was removed from the shape analysis, while size was still a component of wing loading and aspect ratio calculations. Therefore, a lack of difference in shape described by the landmark scheme could be accompanied by a significant difference in aspect ratio and (or) wing loading or vice versa. Further study is needed to evaluate whether the outline of the bat wing can be considered a homologous element as a whole before it is considered in a landmark scheme.

Ethics approval

All procedures were approved by the Life and Environmental Science Animal Care Committee at the University of Calgary (#AC17-0094).


The PCA of wing shape for all foraging guilds (for PCA separated by sex and foraging guild see Supplementary Fig. S2)1 show no difference in morphospace occupancy (Fig. 1; for a colour version see Supplementary Fig. S31). Principal component 1 (PC1) explains 34.2% of the variation in wing shape and represents changes in the shape of the wing tip and tail (Fig. 1). Larger but more pointed wing tips and a shorter tail are associated more with insectivore gleaners, whereas other guilds span most of the variation in PC1 (Fig. 1). PC2 explains 19.7% of the variation in wing shape and represents the displacement of the second and third digits medially, increasing the steepness of the most lateral edge of the wing (Fig. 1). Insectivore gleaners are associated with longer second and third digit, whereas other guilds span most of the variation in PC2 (Fig. 1).
Fig. 1.
Fig. 1. Principal components analysis of wing morphology. Specimens are grouped into foraging guilds. Sample sizes are 10 insectivore gleaners (Gleaner), 158 aerial insectivores (Aerial), and 27 frugivores (Frugivore). Warp grids represent the minimum and maximum wing shape observed for the respective principal component (PC). For a colour version see Supplementary Fig. S3.1
Static allometry had a significant effect on wing shape (r2 = 0.25, F[1,203] = 62.9, p = 0.001); therefore, we used allometric regression residuals as size-corrected landmark coordinates. Foraging guild has an effect on shape (F[2,194] = 9.58, p = 0.001), whereas sex does not (F[1,194] = 1.09, p = 0.36). Disparity analyses conducted among foraging guilds reveal that frugivore wing shape is significantly different from aerial insectivores (p < 0.05) and insectivore gleaners (p < 0.01), while there is no difference in wing shape between aerial insectivores and insectivore gleaners (p = 0.060).
The CVA shows high overlap of aerial insectivores with frugivores, and with insectivore gleaners, though there is little overlap between frugivores and insectivore gleaners (Fig. 2; for a colour version see Supplementary Fig. S41). Among the different foraging guilds, 89.7% of specimens were correctly assigned to their respective foraging guild. Nearly all aerial insectivores were identified accurately (97.5%), whereas 80.00% of insectivore gleaners and 48.2% of frugivores were identified accurately (Table 2).
Fig. 2.
Fig. 2. Canonical variate analysis of wing morphology. Specimens are grouped into foraging guilds. Sample sizes are 10 insectivore gleaners (Gleaner), 158 aerial insectivores (Aerial), and 27 frugivores (Frugivore). For a colour version see Supplementary Fig. S4.1
Table 2.
Table 2. Results of the canonical variate analysis (CVA) on wing morphology grouped by foraging guild.
There is a main effect of foraging guild (F[2,173] = 15.1, p < 0.001) on aspect ratio, as well as a significant effect of species (F[16,173] = 13.1, p < 0.001). However, there is no significant effect of sex (F[1,181] = 2.02, p = 0.157) or significant interaction between sex and foraging guild (F[2,173] = 2.42, p = 0.0923). There is a significantly lower aspect ratio in insectivorous bats (aerial insectivores and insectivore gleaners) than non-insectivorous bats (frugivores; z = –0.56, p < 0.001) and a significant difference between aerial insectivores and insectivore gleaners (z = 0.48, p < 0.05), with insectivore gleaners having the lowest aspect ratio (Fig. 3).
Fig. 3.
Fig. 3. Aspect ratio for different foraging guilds and sexes. Females (F) are displayed in white boxes, whereas males (M) are displayed in grey boxes. Sample sizes are insectivore gleaner (Gleaner; F = 4, M = 6), aerial insectivore (Aerial; F = 97, M = 61), and frugivore (Frugivore; F = 11, M = 16). Aspect ratio is calculated by dividing the square of the wingspan by the wing surface area. Foraging guild was found to be significant, but there was no main effect of sex aspect ratio. Additionally, insectivores (Gleaner and Aerial) had a significantly lower aspect ratio than non-insectivores (Frugivore) and insectivore gleaners had a significantly lower aspect ratio than aerial insectivores. Box limits indicate the 25th (lower) and 75th (upper) quartiles; whiskers indicate the last datum within 1.5 interquartile ranges of the box limits; solid circles beyond the whiskers indicate outliers; the horizontal line within the box is the median.
There is a significant difference in wing loading between pregnant and nonpregnant female bats (t = –3.04, p < 0.01), with pregnant bats having higher wing loading (11.9 ± 1.34 N/m2, mean ± SE) than nonpregnant female bats (8.80 ± 0.419 N/m2, mean ± SE). There is a main effect of sex (F[1,158] = 4.19, p < 0.05), foraging guild (F[2,158] = 437, p < 0.001), and species (F[15,158] = 23.6, p < 0.001). However, there is no significant interaction between sex and foraging guild (F[2,158] = 1.66, p = 0.194). There is significantly lower wing loading in insectivorous bats than in non-insectivorous bats (z = –10.3, p < 0.001; Fig. 4), but there is no difference between aerial insectivores and insectivore gleaners (z = –2.1, p = 0.146). There is no significant difference in the magnitude of sexual dimorphism between insectivorous bats and non-insectivorous bats (z = –0.044, p = 0.818) or between aerial insectivores and insectivore gleaners (z = 0.070, p = 0.814), but female bats have higher wing loading than male bats (Fig. 4).
Fig. 4.
Fig. 4. Wing loading (N/m2) for different foraging guilds and sexes. Females (F) are displayed in white boxes, whereas males (M) are displayed in grey boxes. Sample sizes are insectivore gleaner (Gleaner; F = 4, M = 6), aerial insectivore (Aerial; F = 84, M = 61), and frugivore (Frugivore; F = 8, M = 16). Wing loading was calculated by dividing each bat’s weight by the surface area of its wing. Only nonpregnant female bats were analyzed. Sex and foraging guild were found to be significant. Additionally, insectivores (Gleaner and Aerial) had a significantly lower wing loading than non-insectivores (Frugivore) and females have higher wing loading than males. Box limits indicate the 25th (lower) and 75th (upper) quartiles; whiskers indicate the last datum within 1.5 interquartile ranges of the box limits; solid circles beyond the whiskers indicate outliers; the horizontal line within the box is the median.


Our study examined sexual dimorphism in bat wing shapes for various foraging guilds, and our results show that foraging guild, but not sex, influences the shape of the wing. We found that frugivores have different shaped wings compared with gleaners and aerial insectivores. Our classification of insectivorous bats into aerial foragers and gleaners is supported by differences in aspect ratio because insectivore gleaners have the lowest aspect ratio of all guilds. There is no difference in wing loading between insectivore gleaners and aerial insectivores, but non-insectivorous bats (frugivores) have the highest wing loading and aspect ratio. Finally, we found that nonpregnant female bats have a larger wing loading than male bats.
We predicted that foraging guilds that need more maneuverability, such as insectivore gleaners, would have shorter and broader wings and that shapes would differ between male and female bats, with females having shorter and broader wings, to compensate for increases in mass during pregnancy. There are no differences in wing shape between sexes and post hoc pairwise comparisons do not show significant differences in shape for foraging guilds requiring more maneuverability, which does not support our first and second predictions. Regardless of foraging style and the constraints on maneuverability, there are no differences in overall wing shape between male and female bats. There is a significant difference in shape between frugivores and all other guilds; however, the frugivores cluster closely with all other foraging guilds for the first and second principal components. Further studies into additional components of wing shape are needed to better understand what makes frugivore wings uniquely shaped.
Despite no significant difference in overall shape, there was a range of variation in wing shape observed with an emphasized difference between nectarivores and other guilds. Insectivore gleaners show an association with larger but more pointed wing tips and a shorter tail. A longer tail may aid aerial insectivores with prey capture (Kalko 1995), whereas insectivore gleaners may not require as large of a uropatagium. Within foraging guilds, there is a great degree of variation in wing breadth and in the shape of the uropatagium and dactylopatagium (hand wing), which may contribute to intraspecific differences in shape and diet. There may be unique differences in shape, such as subtle changes in the wing tip, between conspecifics that aid females to account for a decrease in maneuverability associated with pregnancy as was found in S. lilium by Camargo and Oliveira (2012), but further investigation into this is needed.
Additionally, we predicted that there would be greater sexual dimorphism in foraging guilds requiring more maneuverability to forage, again to compensate for increases in mass during pregnancy. However, as there are no significant differences in shape between sexes, there is no sexual dimorphism in shape at all, let alone to differing degrees between foraging guilds. This suggests that there are equal selective pressures on wing morphology as captured in our landmark scheme between sexes in all foraging styles examined, leading to the insignificant differences in wing shape. There are no differences in the degree of sexual dimorphism in bat wing loading, and as there is no significant effect of sex on aspect ratio, there is also not sexual dimorphism in aspect ratio. There are no differences in the degree of sexual dimorphism between foraging guilds due to wing shape, aspect ratio, or wing loading, which does not support our third prediction.
Our final prediction was that female bats would have lower wing loading and lower aspect ratio than males of the same foraging guild, so that they would be more maneuverable, and be able to adjust for the increase in mass during pregnancy. We verified that female bats had a higher wing loading when pregnant compared with nonpregnant bats; however, there was also higher wing loading in nonpregnant females compared with male bats. This shows that the species in our study followed similar trends as seen in the literature, with pregnant females having increased wing loading relative to males (Davis 1969; Norberg and Rayner 1987; Aldridge and Brigham 1988; Hughes and Rayner 1993), but they are less maneuverable before they gain mass with pregnancy. This suggests that female bats during pregnancy would become even less maneuverable, directly contradicting our final prediction. For bats that require maneuverable flight to forage, pregnancy may make it more difficult to forage in a cluttered area. This lower maneuverability would just be compounded with pregnancy, further contradicting our fourth prediction.
Insectivorous bats have the lowest aspect ratios and wing loading, suggesting that there is greater maneuverability in insectivore bats compared with non-insectivorous bats. This maneuverability would allow insectivorous bats, especially gleaners which have the lowest aspect ratio, to forage in more cluttered environments and to have slow, controlled flight (Norberg and Rayner 1987). Higher aspect ratio in aerial insectivores compared with insectivore gleaners may allow for a comparable prey encounter rate between foraging locations, so aerial insectivores encounter similar amounts of prey as insectivore gleaners feeding in the more insect-dense foliage (Aldridge and Rautenbach 1987; Kalcounis and Brigham 1995; Voigt and Holderied 2012). In contrast, higher wing loading and aspect ratios for frugivores suggests that they may forage over large distances so fast and metabolically efficient flight has been selected for (Norberg and Rayner 1987; Voigt and Holderied 2012). For non-insectivorous bats, females with higher wing loading and lower maneuverability, especially when their mass increases during pregnancy, would fly faster and may be able to forage efficiently over large distances, compared with their male conspecifics (Norberg and Rayner 1987). Likely this would not affect non-insectivorous bat feeding ecology much, although there may be differences in foraging location or distance between sexes (Safi et al. 2007). With insectivores that forage in and around clutter, the decreased maneuverability in females, especially during pregnancy, may pose as a difficulty if they have the exact same foraging ecology as male conspecifics.
Studies into the diet and foraging styles of female bats often encompasses fecal analysis, which makes it difficult to determine how prey were captured, for example, moths can be caught aerially or gleaned off a surface (Shiel et al. 1991; Kurta and Whitaker 1998; Bernard 2002). Some species have been found to share the same diet between female and male bats, regardless of reproductive condition (Swift et al. 1985), whereas others have differences in diet, differences in foraging location, and different lengths of foraging bouts by pregnant and lactating females (Kurta and Whitaker 1998; Chruszcz and Barclay 2003; Murray and Kurta 2004; Safi et al. 2007). It is difficult to determine how bats are foraging unless it is observed during foraging experiments (Ratcliffe and Dawson 2003); however, it is common for lactating and pregnant bats to be excluded from studies examining foraging behavior because of stress implications for pregnant females and because pups would be deprived of food from a lactating female bat (Barclay 1991; Entwistle et al. 1996). Therefore, as our study suggests that female bats are less maneuverable than males, which would be further exacerbated as they become pregnant, it is likely that female bats are unable to forage in the same ways as male conspecifics, and their ecology may differ from males at all times in their reproductive cycle (Safi et al. 2007), or just during pregnancy when their maneuverability is at its lowest.
The lack of sexual dimorphism shows that shape based on the homologous characters of the wing are not likely responsible for compensating for the changes in mass during pregnancy. Bats have precise wing control due to their phalanges and metacarpal bones forming the wing structure and are able to manipulate the shape of their wing while they fly. However, what changes occur during flight, and how this affects aspects of flight such as maneuverability, are not well understood (Swartz et al. 2007; Hedenstrom and Johansson 2015). With the ability to change the shape of their wings, bats are also able to change characteristics of their wings, such as their aspect ratio and wing loading during flight (Swartz et al. 2007; Hedenstrom and Johansson 2015). Our study analyzed fully extended bat wings to determine measures of wing loading, aspect ratio, and shape; however, when bats fly, they rarely have fully extended wings (Swartz et al. 2007; Hedenstrom and Johansson 2015). Some studies have assessed the effects of wing control during flight in various species, but much is still unknown, and changes in the manipulation of female bat wing surface size or shape may be able to compensate for decreased maneuverability during pregnancy (Hedenstrom and Johansson 2015; Konow et al. 2017).
To conclude, our study investigated the variation in wing morphology that exists among different foraging styles and sexes within bats from Belize, Canada, and Dominica. We found limited differences in shape between foraging guilds, showing that different foraging styles do not necessarily require different shaped wings. Similarly, no difference in wing shape was found between sexes. There was also no significant difference in the degree of sexual dimorphism between sexes and foraging guilds of bats. The employed landmark scheme evaluates only the homologous elements of bat wings, rather than the full extent of wing shape. Future studies could be conducted investigating whether other aspects of the wing shape (outline of the wing membrane, particular regions of the wing) cause significant differences in maneuverability between sexes. In addition to this, individual species wing shape should be examined to learn if there are shape differences between conspecifics that are not consistent among bat foraging guilds. Finally, we report that nonpregnant female bats had higher wing loading than male bats, suggesting that female bats are less maneuverable than male bats, which will be further exacerbated as their wing loading increases with pregnancy. This suggests that during pregnancy, female bats may not be able to forage as efficiently and (or) in the same way as male conspecifics. As female bats increase in mass, they may change their foraging ecology during their reproductive cycle or we speculate that they may be able to manipulate their wings in different ways to maintain maneuverability by changing the useable surface area or shape of their wings. Further studies and observations are needed to better understand how female bats forage during their reproductive cycle and whether this differs from male conspecifics.

Data availability statement

Code and data for figures and analyses are available through GitHub ( and archived through Zenodo (


We thank everyone who helped with the data collection for this project, including R.M.R. Barclay, B. Steed, T. Issler, and L. Sims. We thank J. Fox for statistical advice and the other members of our laboratory for their assistance through this research, including B. Steed, L. Hiles, and S. Robson. Additionally, we thank C. Maxwell-Wilson for providing the bat wing image used to illustrate the landmarking scheme in Supplementary Fig. S1.1


Supplementary figures are available with the article at


Adams D.C. and Otárola‐Castillo E. 2013. geomorph: an r package for the collection and analysis of geometric morphometric shape data. Methods Ecol. Evol. 4(4): 393–399.
Adams, D.C., Collyer, M.L., and Kaliontzopoulou, A. 2020. Geomorph: software for geometric morphometric analyses. Available from
Aldridge H.D.J.N. and Brigham R.M. 1988. Load carrying and maneuverability in an insectivorous bat: a test of the 5% “rule” of radio-telemetry. J. Mammal. 69(2): 379–382.
Aldridge H.D.J.N. and Rautenbach I.L. 1987. Morphology, echolocation and resource partitioning in insectivorous bats. J. Anim. Ecol. 56(3): 763–778.
Barclay R.M.R. 1991. Population structure of temperate zone insectivorous bats in relation to foraging behaviour and energy demand. J. Anim. Ecol. 60(1): 165–178.
Barclay R.M.R. and Brigham R.M. 1991. Prey detection, dietary niche breadth, and body size in bats: Why are aerial insectivorous bats so small? Am. Nat. 137(5): 693–703.
Bernard E. 2002. Diet, activity and reproduction of bat species (Mammalia, Chiroptera) in Central Amazonia, Brazil. Rev. Bras. Zool. 19(1): 173–188.
Bolzan D.P., Pessôa L.M., Peracchi A.L., and Strauss R.E. 2015. Allometric patterns and evolution in Neotropical nectar-feeding bats (Chiroptera, Phyllostomidae). Acta Chiropterol. 17(1): 59–73.
Bookstein, F.L. 1997. Morphometric tools for landmark data: geometry and biology. Cambridge University Press, Cambridge.
Brunet-Rossinni, A.K., and Wilkinson, G. 2009. Methods for age estimation and the study of senescence in bats. In Ecological and behavioral methods for the study of bats. Edited by T.H. Kunz and S. Parsons. Johns Hopkins University Press, Baltimore, Md. pp. 315–325.
Butler M.A. and Losos J.B. 2002. Multivariate sexual dimorphism, sexual selection, and adaptation in Greater Antillean Anolis lizards. Ecol. Monogr. 72(4): 541–559.
Camargo N.F.D. and Oliveira HFM D. 2012. Sexual dimorphism in Sturnira lilium (Chiroptera, Phyllostomidae): Can pregnancy and pup carrying be responsible for differences in wing shape? PLoS ONE, 7(11): e49734–e49737.
Chruszcz B.J. and Barclay R.M.R. 2003. Prolonged foraging bouts of a solitary gleaning/hawking bat, Myotis evotis. Can. J. Zool. 81(5): 823–826.
Dávalos L.M. 2007. Short-faced bats (Phyllostomidae: Stenodermatina): a Caribbean radiation of strict frugivores. J. Biogeogr. 34(2): 364–375.
Davis R. 1969. Wing loading in pallid bats. J. Mammal. 50(1): 140–144.
Entwistle A.C., Racey P.A., Spearman J.R., and Su M. 1996. Habitat exploitation by a gleaning bat, Plecotus auritus. Philos. Trans. R. Soc. B Biol. Sci. 351: 921–931.
Guillerme T. 2018. dispRity: a modular R package for measuring disparity. Methods Ecol. Evol. 9(7): 1755–1763.
Hackett T.D., Korine C., and Holderied M.W. 2014. A whispering bat that screams: bimodal switch of foraging guild from gleaning to aerial hawking in the desert long-eared bat. J. Exp. Biol. 217(17): 3028–3032.
Hallgrimsson, B., Percival, C.J., Green, R., Young, N.M., Mio, W., and Marcucio, R. 2015. Morphometrics, 3D imaging, and craniofacial development. In Current topics in developmental biology. Edited by Y. Chai. Academic Press, London. pp. 561–597.
Hedenstrom A. and Johansson L.C. 2015. Bat flight: aerodynamics, kinematics and flight morphology. J. Exp. Biol. 218(5): 653–663.
Hedenström A., Johansson L.C., and Spedding G.R. 2009. Bird or bat: comparing airframe design and flight performance. Bioinspir. Biomim. 4(1): 015001.
Hedrick A.V. and Temeles E.J. 1989. The evolution of sexual dimorphism in animals: Hypotheses and tests. Trends Ecol. Evol. 4(5): 136–138.
Hourigan C.L., Catterall C.P., Jones D., and Rhodes M. 2010. The diversity of insectivorous bat assemblages among habitats within a subtropical urban landscape: bat diversity in a subtropical city. Austral Ecol. 35(8): 849–857.
Hughes P. and Rayner J.M.V. 1993. The flight of pipistrelle bats Pipistrellus pipistrellus during pregnancy and lactation. J. Zool. 230(4): 541–555.
Kalcounis M.C. and Brigham R.M. 1995. Intraspecific variation in wing loading affects habitat use by little brown bats (Myotis lucifugus). Can. J. Zool. 73(1): 89–95.
Kalko E.K.V. 1995. Insect pursuit, prey capture and echolocation in pipestirelle bats (Microchiroptera). Anim. Behav. 50(4): 861–880.
Klingenberg C.P. 2016. Size, shape, and form: concepts of allometry in geometric morphometrics. Dev. Genes Evol. 226(3): 113–137.
Konow N., Cheney J.A., Roberts T.J., Iriarte-Díaz J., Breuer K.S., Waldman J.R.S., and Swartz S.M. 2017. Speed-dependent modulation of wing muscle recruitment intensity and kinematics in two bat species. J. Exp. Biol. 220(10): 1820–1829.
Kunz T.H. and Whitaker J.O. 1983. An evaluation of fecal analysis for determining food habits of insectivorous bats. Can. J. Zool. 61(6): 1317–1321.
Kurta A. and Whitaker J.O. 1998. Diet of the endangered Indiana Bat (Myotis sodalis) on the northern edge of its range. Am. Midl. Nat. 140(2): 280–286.
Lopez J.E. and Vaughan C. 2007. Food niche overlap among neotropical frugivorous bats in Costa Rica. Rev. Biol. Trop. 55(1): 301–313.
Marinello M.M. and Bernard E. 2014. Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use. Can. J. Zool. 92(2): 141–147.
Maucieri D.G. and Barclay R.M.R. 2021. Consumption of spiders by the little brown bat (Myotis lucifugus) and the long-eared myotis (Myotis evotis) in the Rocky Mountains of Alberta, Canada. Can. J. Zool. 99(3): 221–226.
Murray S.W. and Kurta A. 2004. Nocturnal activity of the endangered Indiana bat (Myotis sodalis). J. Zool. 262(2): 197–206.
Norberg U.M. and Rayner J.M.V. 1987. Ecological morphology and flight in bats (Mammalia; Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos. Trans. R. Soc. B Biol. Sci. 316 (1179): 335–427.
Pasinelli G. 2000. Sexual dimorphism and foraging niche partitioning in the Middle Spotted Woodpecker Dendrocopos medius. Ibis, 142(4): 635–644.
Ratcliffe J.M. and Dawson J.W. 2003. Behavioural flexibility: the little brown bat, Myotis lucifugus, and the northern long-eared bat, M. septentrionalis, both glean and hawk prey. Anim. Behav. 66(5): 847–856.
R Core Team. 2020. A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available from
Safi K., König B., and Kerth G. 2007. Sex differences in population genetics, home range size and habitat use of the parti-colored bat (Vespertilio murinus, Linnaeus 1758) in Switzerland and their consequences for conservation. Biol. Conserv. 137(1): 28–36.
Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., et al. 2012. Fiji: an open-source platform for biological-image analysis. Nat. Methods, 9(7): 676–682.
Schlager, S. 2017. Morpho and Rvcg – Shape analysis in R: R-packages for geometric morphometrics, shape analysis and surface manipulations. In Statistical shape and deformation analysis. Edited by G. Zheng, S. Li, and G. Székely. Academic Press, London. pp. 217–256.
Schnitzler H.-U. and Kalko E.K.V. 2001. Echolocation by insect-eating bats. BioScience, 51(7): 557–569.
Schulz M. 2000. Diet and foraging behavior of the Golden-Tipped Bat, Kerivoula papuensis: a spider specialist? J. Mammal. 81(4): 948–957.
Shiel C.B., McAney C.M., and Fairley J.S. 1991. Analysis of the diet of Natterer’s bat Myotis nattereri and the common long-eared bat Plecotus auritus in the West of Ireland. J. Zool. 223(2): 299–305.
Shine R., Harlow P.S., Branch W.R., and Webb J.K. 1996. Life on the lowest branch: Sexual dimorphism, diet, and reproductive biology of an African twig snake, Thelotornis capensis (Serpentes, Colubridae). Copeia, 1996(2): 290.
Slatkin M. 1984. Ecological causes of sexual dimorphism. Evolution, 38(3): 622–630.
Spoljaric M.A. and Reimchen T.E. 2008. Habitat-dependent reduction of sexual dimorphism in geometric body shape of Haida Gwaii threespine stickleback. Biol. J. Linn. Soc. 95(3): 505–516.
Swartz, S., Iriarte-Diaz, J., Riskin, D., Tian, X., Song, A., and Breuer, K. 2007. Wing structure and the aerodynamic basis of flight in bats. In 45th AIAA Aerospace Sciences Meeting and Exhibit. American Institute of Aeronautics and Astronautics, Reno, Nevada.
Swift S.M., Racey P.A., and Avery M.I. 1985. Feeding ecology of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) During pregnancy and lactation. II. Diet. J. Anim. Ecol. 54(1): 217.
Vogel S. 1958. Fledermausblumen in Südamerika. Osterr. bot. Z. 104(4/5): 491–530.
Voigt C.C. and Holderied M.W. 2012. High manoeuvring costs force narrow-winged molossid bats to forage in open space. J. Comp. Physiol. B, 182(3): 415–424.
Webster M. and Sheets H.D. 2010. A practical introduction to landmark-based geometric morphometrics. Paleontol. Soc. Pap. 16: 163–188.
Zelditch, M.L., Swiderski, D.L., Sheets, H.D., and Fink, W.L. 2004. Geometric morphometrics for biologists. Elsevier, San Diego, Calif.

Supplementary Material

Supplementary data (cjz-2021-0035suppla.docx)

Information & Authors


Published In

cover image Canadian Journal of Zoology
Canadian Journal of Zoology
Volume 99Number 11November 2021
Pages: 953 - 960


Received: 9 February 2021
Accepted: 22 June 2021
Accepted manuscript online: 14 August 2021
Version of record online: 14 August 2021

Key Words

  1. Chiroptera
  2. bats
  3. sexual dimorphism
  4. wing loading
  5. aspect ratio
  6. maneuverability
  7. geometric morphometrics


  1. chiroptères
  2. chauves-souris
  3. dimorphisme sexuel
  4. charge alaire
  5. allongement
  6. capacité de manœuvre
  7. morphométrie géométrique



D.G. Maucieri* [email protected]
Department of Biological Sciences, University of Calgary, Calgary, AB T2N 1N4, Canada.
A.J. Ashbaugh
Department of Biological Sciences, University of Calgary, Calgary, AB T2N 1N4, Canada.
J.M. Theodor
Department of Biological Sciences, University of Calgary, Calgary, AB T2N 1N4, Canada.


Present address: Department of Biological Sciences, University of Victoria, 3800 Finnerty Road, Victoria, BC V8P 5C2, Canada.
© 2021 The Author(s). This work is licensed under a Creative Commons Attribution 4.0 International License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author(s) and source are credited.

Funding Information

We thank our funding sources: the University of Calgary PURE Award to D.G.M. and the Natural Sciences and Engineering Research Council of Canada (NSERC) CGS-M scholarship to A.J.A. and NSERC DG to J.M.T.

Metrics & Citations


Other Metrics


Cite As

Export Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

There are no citations for this item

View Options

View options


View PDF

Get Access

Login options

Check if you access through your login credentials or your institution to get full access on this article.


Click on the button below to subscribe to Canadian Journal of Zoology

Purchase options

Purchase this article to get full access to it.

Restore your content access

Enter your email address to restore your content access:

Note: This functionality works only for purchases done as a guest. If you already have an account, log in to access the content to which you are entitled.





Share Options


Share the article link

Share on social media

Cookies Notification

We use cookies to improve your website experience. To learn about our use of cookies and how you can manage your cookie settings, please see our Cookie Policy.