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).