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Foraging strategies, craniodental traits and interaction in the bite force of Neotropical frugivorous bats (Phyllostomidae: Stenodermatinae)

Citation

García Herrera, Leidy Viviana et al. (2022), Foraging strategies, craniodental traits and interaction in the bite force of Neotropical frugivorous bats (Phyllostomidae: Stenodermatinae), Dryad, Dataset, https://doi.org/10.5061/dryad.2v6wwpzmf

Abstract

1. Bats in the family Phyllostomidae exhibit great diversity in skull size and morphology that reflects the degree of resource division and ecological overlap in the group. In particular, the subfamily Stenodermatinae has high morphological diversification associated with cranial and mandibular traits that is associated with the ability to consume the full range of available fruits (soft and hard).

2. Was analyzed craniodental traits and their relationship to the bite force in 343 specimens distributed in seven species of stenodermatine bats with two foraging strategies: nomadic and sedentary frugivory. We evaluated 19 traits related to feeding and bite force in live animals by correcting bite force with body size.

3. We used a generalized linear model (GLM) and post hoc tests to determine possible relationships and differences between cranial traits, species, and sex. We also used Blomberg's K to measure the phylogenetic signal and Phylogenetic generalized least-squares (PGLS) to ensure the phylogenetic independence of the traits.

4. We found that smaller nomadic, A. anderseni and A. phaeotis have a similar bite force to the large species A. planirostris and A. lituratus; furthermore, P. helleri registered a bite force similar to that of the sedentary bat, S. giannae. Our study determined that all the features of the mandible and most of the traits of the skull have a low phylogenetic signal. Through the PGLS we found that the diet and several cranial features (mandibular toothrow length, dentary length, braincase breadth, mastoid breadth, greatest length of skull, condyloincisive length and condylocanine length) determined bite force performance among Stenodermatiane.

5. Our results reinforce that skull size is a determining factor in the bite force, but also emphasize the importance of its relationships with morphology, ecology, and phylogeny of the species, which gives us a better understanding of the evolutionary adaptions of this highly diverse Neotropical bat group.

Methods

We followed two procedures for collecting data. The first involved fieldwork in selected areas of the Colombian tropical dry forest (TDF) in the department of Tolima (Figure 1; Appendix 1) from February 2019 to January 2020. Conventional survey methodology was used, including mist-nets placed along trails within forest areas, at the edge of forest remnants, and near waterbodies. Each sampling night consisted of four standard-size mist nets (12 x 2.5 m) in the forest understory, eight nets (6 x 2.5 m) in the sub-canopy and a triple high net (30 x 7 m) in clearings, with a sampling intensity of 36,288 m2 nets/h, corresponding to 864 h in 144 nights. The captured bats were handled according to the American Society of Mammalogists guidelines for the use of wild animals for research purposes (Sikes et al., 2016). After capture, the age, sex, and reproductive status were evaluated, and only adult males and adult non-pregnant, non-lactating females were used for measurements. Age was based on the degree of ossification of the wing joints. Reproductive status in females was determined by examining the nipples and palpation of the abdomen. Forearm length and body mass were recorded before euthanasia. Specimens were deposited in the biological collection of the University of Tolima CZUT-M (Ibagué, Colombia) and skulls were cleaned for craniodental morphometry (Table S1).

The bite force of bats was measured using a portable digital fruit hardness tester Lutron FR 5120 (made in Taiwan) with a capacity of 196.10 Newton and precision ± 0.05 that corresponded to in vivo measurements of the maximal force. Bite force was recorded at the molars and measurements were repeated five times for each bat with a trial interval of at least 5 min following the method of Freeman & Lemen (2008). The maximum value of the five measurements was considered as the maximum bite force produced by that individual. The bite force of the species was calculated by averaging the maximum bite force of each individual.

The second procedure for collecting data consisted of measurements of 16 craniodental traits and two body traits (Table 1, Figure 2) from voucher specimens in the Zoological Collection of the University of Tolima (CZUT; Ibagué, Colombia), Museo Javeriano de Historia Natural "Lorenzo Uribe, SJ" (MPUJ; Bogotá, Colombia) and Royal Ontario Museum (ROM; Ontario, Canada). The specimens from these biological collections are from 24 localities in Colombia (Figure 1; Table S1). We verified that all were adult specimens based on the ossification of the phalange epiphyses in the wing (Dietz et al., 2007).

Among frugivorous bats, two foraging categories adapted to fruit consumption were distinguished based on Soriano (2000): nomadic frugivorous, species whose strategy consists of feeding on trees with massive production of short-lived fruit, while sedentary bats have search itineraries more or less fixed every night and focus the consumption of fruits in plants with continuous production throughout the year. This classification involves a specialization towards a group of plants, reducing competition and generating a coevolution with plants and bats (Fleming, 1986; Giannini and Kalko, 2004).

Stenodermatinae is the only subfamily with species that are either nomadic sedentary; therefore, these organisms constitute an excellent model to evaluate the skull traits involved in the consumption of contrasting fruits. We classified in our data set large-sized nomadic species with weight 55-65 g and medium to small-sized nomadic with weight 10-18 g. Although our size limit is arbitrary, it may have some biological relevance because Artibeus planirostris and A. lituratus are large bats with high dispersal capacity (Trevelin et al., 2013). Individuals captured in mistnets were placed in a clean cloth bag for up to four hours to obtain fecal samples, which were analyzed at a later date in the laboratory for seeds. The seeds were washed, examined with a dissection microscope and identified at the lowest possible taxonomic level (Table S2), and supplemented with bibliographic information from the registry (García-Herrera et al., 2019b).

Funding

University of Tolima

University of Tolima