Title: Singing strategies are linked to perch use on foraging territories in heart-nosed bats
Grace C. Smarsh*1, Ashley M. Long2, and Michael Smotherman3
Author Affiliation : 1 Department of Neurobiology, Weizmann Institute of Science, Rehovot, IL 7610001;2School of Renewable Natural Resources, Louisiana State University, Baton Rouge, LA, USA, 70803;3Department of Biology, Texas A&M University, College Station, TX, USA, 77843
Corresponding Author : Grace C. Smarsh, Department of Neurobiology, Weizmann Institute of Science, Rehovot, IL, 7610001, gc.smarsh@gmail.com
ACKNOWLEDGEMENTS
We thank Felix Mpelembwa, Nuhu Bahaty Mhapa, Alfred Absolem Mollel, Nickodemasy Obeid, and Rogers Eliau for their assistance in data collection. The Village, Ward, and District Officers provided crucial support. We thank Dassa Nkini of the Tanzania Conservation Resource Centre and Dr. Kim Howell for logistic support. Tim Divoll provided Geospatial Modeling Environment coding and analysis advice. We thank Dr. Markus Peterson for advice on sampling designs, Dr. Bruce Patterson and Dr. Merlin Tuttle for advice on working with African megadermatid bats, and Dr. Yossi Yovel for comments on an earlier version of the introduction. This research was possible due to a National Science Foundation Graduate Research Fellowship, and Bat Conservation International Student Scholarships with additional funding from Wildlife Acoustics.
COMPETING INTERESTS
We declare no competing interests.
AUTHORS’ CONTRIBUTIONS
G.S and M.S designed the study. G.S. carried out the study. G.S. analyzed the data. A.M. guided analysis and reviewed the results. G.S. wrote the manuscript. M.S. and A.M. edited the manuscript.
DATA AVAILABILITY
Data will be made available upon acceptance of manuscript.
ABSTRACT
Acoustic communication allows animals to coordinate and optimize resource utilization in space. Cardioderma cor , the heart-nosed bat, is one of the few species of bats known to sing during nighttime foraging. Previous research found that heart-nosed bats react aggressively to song playback, supporting the territorial defense hypothesis of singing in this species (Smarsh et al 2017). By tracking 14 individuals nightly during the dry seasons in Tanzania we further investigated the territorial defense hypothesis from an ecological standpoint, which predicts singing should be associated with exclusive areas containing a resource. We quantified the singing behavior of individuals at all perches used throughout the night. Using home range analysis tools, we quantified overall use night ranges and singing ranges, as well as areas used in early and later time periods at night. Males engaged in antiphonal singing from small (x̄ = 3.48 ± 2.71 ha), largely exclusive areas that overlapped with overall night ranges used for gleaning prey. Individuals varied in singing effort; however, all sang significantly more as night progressed. Subsequently, areas used earlier at night and overall use areas were both larger than singing areas. Individuals varied in singing strategies. Some males sang for long periods in particular trees and had smaller core areas, while others moved frequently among singing trees. The most prolific singers used more perches overall. The results support the hypothesis that acoustic communication repertoires evolved in support of stable foraging territory advertisement and defense in some bats.
Keywords : Cardioderma cor , heart-nosed bat, space use, antiphonal singing, social behavior, territoriality
INTRODUCTION
Vocal signaling can be used by territorial individuals to defend resources such as food and mates (Hinde 1956, Tinbergen 1957), and may encode important information to conspecifics regarding the signaler’s identity, age, sex, location, motivational state, energenetic condition, and more (Bradbury and Vehrencamp 2011). Singing (multisyllabic sequences with stereotyped patterns produced in bouts) is a common signaling mechanism used by songbirds to defend resources such as food and mates (Catchpole and Slater 2008). Songs range from simple to complex, and can change in duration and rate (Linhart et al. 2013, Cardoso 2014, Funghi et al. 2015), composition (Galeotti et al. 1997, DuBois et al. 2009), or type (Stoddard 1992, Akçay et al. 2013) to express heightened motivation during territorial contests, thus contributing to the fitness of individuals (Catchpole and Slater 2008); carrying capacity of populations (Ahlering and Faaborg 2006); maintenance of local populations in fragmented, degraded, or restored landscapes (Campomizzi et al. 2008); and distributions of territories or home ranges (Farrell et al. 2012). Given sampling bias and technical constraints, the degree to which non-avian taxa use singing as a behavioral mechanism to coordinate and optimize resource utilization, particularly access to foraging opportunities, is still relatively unknown. However, research on mammals such as gibbons (e.g. (Ham et al. 2016) and rodents (e.g. (Pasch et al. 2013) has demonstrated that animal use of vocalizations classified as songs to maintain or defend territories extends beyond birds.
Primarily nocturnal, bats rely heavily on acoustic signals for survival, including echolocation to navigate and locate prey, and various social calls for behavioral interactions (Altringham and Fenton 2003). Their broad communication repertoires include singing, which has been observed in five families (Smotherman et al. 2016b). Athough there are over 1400 species of bats (Simmons and Cirranello 2020), we know very little about how bats use vocal communication, including singing, as a spacing mechanism or to defend resources. Territoriality is established from an ecological standpoint (home range analysis showing repeat use of an exclusive area), and a behavioral standpoint (defensive behavioral interactions) (Burt 1943, Maher and Lott 1995). Bat studies generally focus on either the ecology (e.g. (Winkelmann et al. 2003, Jessica Hillen and Veith 2009, Egert-Berg et al. 2018) or behavior of the species (e.g. (Rydell 1989, Barlow and Jones 1997, Wright et al. 2014, Götze et al. 2020). We examined territorialilty in bats from both an ecological and a behavioral standpoint by quantifiying the spatial and temporal relationships between singing behavior and foraging areas used by heart-nosed bats (Cardioderma cor ), one of the few species known to sing during nighttime foraging bouts ( (Vaughan 1976, McWilliam 1987, Smarsh and Smotherman 2015a, 2017).
The heart-nosed bat is endemic to East Africa (Vaughan 1976). They use quiet echolocation to navigate, but ultimately rely on prey-generated noises to glean frogs, beetles, and other arthropods off surfaces. Individuals forage by perching in Acacia trees and bushes listening for prey items nearby (Ryan and Tuttle 1987, Kanuch et al. 2015, Smarsh and Smotherman 2015b), a passive gleaning strategy that is often associated with dispersed and defensible food resources (Egert-Berg et al. 2018). Researchers have observed individuals in Acacia trees broadcasting loud, multisyllabic, individualistic songs from different foraging areas (Vaughan 1976, McWilliam 1987, Smarsh and Smotherman 2015a), and responses to song playback show that heart-nosed bats actively defend these nocturnal perches using songs (Smarsh and Smotherman 2015a, 2017). In the morning heart-nosed bats return to their communal day roosts, which are located in the cavities of baobob trees (Adansonia digitata ) and can range in size from 30–100 conspecifics (Vaughan 1976).
We hypothesized that heart-nosed bats sing to defend their food resources on a discrete, exclusive territory and, based on criteria for territoriality, we predicted that (1) singing areas should occur in the same locations as food resources, (2) foraging areas should be used repeatedly by the same individual, and (3) foraging areas should have minimal overlap with neighbors (Burt 1943, Maher and Lott 1995). We used telemetry data and behavioral observations of heart-nosed bats from our study site in Tanzania to link foraging areas with singing locations. We examined nightly variation in singing behavior, the overlap between home ranges and singing areas, and the extent of spatial overlap between neighbors. Furthermore, we examined variation in individual singing and perch use to understand how behavior may influence space use.
MATERIALS AND METHODS
Study Area
We conducted our research in the open areas of the Kikavuchini, Mkalama, and Longoi Villages in the Hai District of northern Tanzania (3◦27’18. 324”S, 37◦16’51. 312”E; Fig. 1). This rocky, dry ecosystem is characterized by Acacia-Commiphera scrub vegetation (A. tortilis and Commiphera africana) scattered with baobab trees and is fragmented by agricultural fields. We worked in the vicinity of a known heart-nosed bat colony in a boabob tree with ~70–80 individuals of mixed sex and age. Mean yearly temperature in the region is 23.4o C and mean yearly precipitation is 856 mm. There are two rainy seasons each year (March–May and November–December), with the greatest amount of precipitation in April (mean 282 mm) and the least amount of precipitation in August (14 mm). We conducted our research under Texas A&M University AUP 2012-087; Tanzania Commission for Science and Technology, 2014-53-ER-2012-58, 2013-65-NA-2012-58, and NA-2012-58.
Target netting and tagging individuals
In 2013 and 2014 we target-netted heart-nosed bats at singing perches and at one roost within our ~1500 ha study area. Because previous research found that heart-nosed bat singing is most prevalent during the long, dry season (May–October), we focused our sampling efforts within this time period (Vaughan and Vaughan 1986, McWilliam 1987). We located individuals to net based on aural detections of their loud, conspicuous songs (Vaughan 1976, McWilliam 1987, Smarsh and Smotherman 2015a). We deployed single-high mist nets around trees that we observed were frequently used for singing (38 mm mesh, 75-denier/2-ply black polyester, 2.6 m high, 4 shelves, 6 m wide from Avinet, Inc., Dryden, NY). In 2013, all of the bats we captured around singing trees were male. In 2014, we captured females by placing mistnets near the baobab roost. We only deployed radiotrasmitters (see below) on adult females that did not show signs of pregnancy or nursing (Brunet-Rossinni and Wilkinson 2009).
We recorded the following for each individual: weight (g), forearm length (cm), sex, reproductive status, and age (Brunet-Rossinni and Wilkinson 2009). We also measured testes length and width for adult males. In 2013, we marked bats using lipped forearm bands (2.9 mm wide, alloy, Porzana Limited) (Kunz and Weise 2009), but given minor forearm irritation, we used passive integrated transponder (PIT) tags (HPT8 134.2 tag, Biomark) in 2014. We then affixed a radiotransmitter (Model SOPB-2012, 1.0 g, Wildlife Materials Inc.) on the dorsal region with Ostobond (2013) or Permatype surgical cement (2014).
We used a 3-element folding yagi antenna and receiver (TRX-48, Wildlife Materials) to track individuals one at a time post roost emergence during the hours of 20:00–23:00 and 0:00–3:00. We used homing with multiple readings taken around the perch to target individuals (Amelon et al. 2009), assisted by their audible singing. We marked perches with a Global Positioning Systems (GPS) unit (3m accuracy; Magellan, San Dimas, CA). We gave each marked perch an identifying number and recorded how long the individual stayed at this location, and the times of movements to perches. We recorded the times and locations of singing. We identified the end of a bout when an individual stopped singing for approximately one minute (Smarsh and Smotherman 2017). While opportunistically recorded songs during tracking with an SM2BAT+ recorder and SMX-US microphone (Wildlife Acoustics), held approximately 3 m from the individual (96 kHz sample rate, 64 dB gain).