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      Sensory Drive Mediated by Climatic Gradients Partially Explains Divergence in Acoustic Signals in Two Horseshoe Bat Species, Rhinolophus swinnyi and Rhinolophus simulator

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          Abstract

          Geographic variation can be an indicator of still poorly understood evolutionary processes such as adaptation and drift. Sensory systems used in communication play a key role in mate choice and species recognition. Habitat-mediated (i.e. adaptive) differences in communication signals may therefore lead to diversification. We investigated geographic variation in echolocation calls of African horseshoe bats, Rhinolophus simulator and R. swinnyi in the context of two adaptive hypotheses: 1) James’ Rule and 2) the Sensory Drive Hypothesis. According to James’ Rule body-size should vary in response to relative humidity and temperature so that divergence in call frequency may therefore be the result of climate-mediated variation in body size because of the correlation between body size and call frequency. The Sensory Drive Hypothesis proposes that call frequency is a response to climate-induced differences in atmospheric attenuation and predicts that increases in atmospheric attenuation selects for calls of lower frequency. We measured the morphology and resting call frequency (RF) of 111 R. simulator and 126 R. swinnyi individuals across their distributional range to test the above hypotheses. Contrary to the prediction of James’ Rule, divergence in body size could not explain the variation in RF. Instead, acoustic divergence in RF was best predicted by latitude, geography and climate-induced differences in atmospheric attenuation, as predicted by the Sensory Drive Hypothesis. Although variation in RF was strongly influenced by temperature and humidity, other climatic variables (associated with latitude and altitude) as well as drift (as suggested by a positive correlation between call variation and geographic distance, especially in R. simulator) may also play an important role.

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          Most cited references12

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          Measurements of atmospheric attenuation at ultrasonic frequencies and the significance for echolocation by bats.

          The absorption of sound propagating through the atmosphere under laboratory conditions of 25 degrees C and 50% relative humidity was measured at frequencies from 30 to 200 kHz. The attenuating effect on the passage of ultrasonic sounds through air ranged from 0.7 dB/m at 30 kHz. These measurements confirm theoretical expectations and earlier observations that atmospheric attenuation is progressively more severe at higher frequencies and that the atmosphere acts as a low-pass filter for conducting sounds in the frequency range used for echolocation by bats. Different species of bats use different portions of this range of frequencies, and bats emitting sonar signals predominantly above 100 kHz encounter especially severe attenuation of over 3 dB/m. With the greatly restricted operating distances for echolocation at such high frequencies, bats using these higher frequencies must be under compelling ecological pressures of a higher priority than long-range detection of targets.
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            Estimation of the acoustic range of bat echolocation for extended targets.

            Extended natural structures of the bat environment such as trees, meadows, and water surfaces were ensonified in distances from 1 to 20 m and the echoes recorded using a mobile ultrasonic sonar system. By compensating the atmospheric attenuation, the attenuation of the reflected echo caused by diffraction, energy absorption of the target, and two-way-geometric spreading was calculated for each distance. For each target type the attenuation of the compensated echo sound pressure level was fitted over distance using a linear function which yields simple laws of reflection loss and geometric spreading. By adding to this function again variable atmospheric attenuation, the overall attenuation of a signal reflected from these targets can be estimated for various conditions. Given the dynamic range of a sonar system, the acoustic maximum detection distance can thus be estimated. The results show that the maximum range is dominantly limited by atmospheric attenuation. Energy loss in the reflecting surface is more variable than geometric spreading loss and accounts for most of the differences between the ensonified targets. Depending on atmospheric conditions, echolocation frequency, and the dynamic range of the sonar system, the maximum range for extended backgrounds such as a forest edge can be as short as 2.4 m.
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              Scaling of echolocation call parameters in bats.

              I investigated the scaling of echolocation call parameters (frequency, duration and repetition rate) in bats in a functional context. Low-duty-cycle bats operate with search phase cycles of usually less than 20 %. They process echoes in the time domain and are therefore intolerant of pulse-echo overlap. High-duty-cycle (>30 %) species use Doppler shift compensation, and they separate pulse and echo in the frequency domain. Call frequency scales negatively with body mass in at least five bat families. Pulse duration scales positively with mass in low-duty-cycle quasi-constant-frequency (QCF) species because the large aerial-hawking species that emit these signals fly fast in open habitats. They therefore detect distant targets and experience pulse-echo overlap later than do smaller bats. Pulse duration also scales positively with mass in the Hipposideridae, which show at least partial Doppler shift compensation. Pulse repetition rate corresponds closely with wingbeat frequency in QCF bat species that fly relatively slowly. Larger, fast-flying species often skip pulses when detecting distant targets. There is probably a trade-off between call intensity and repetition rate because 'whispering' bats (and hipposiderids) produce several calls per predicted wingbeat and because batches of calls are emitted per wingbeat during terminal buzzes. Severe atmospheric attenuation at high frequencies limits the range of high-frequency calls. Low-duty-cycle bats that call at high frequencies must therefore use short pulses to avoid pulse-echo overlap. Rhinolophids escape this constraint by Doppler shift compensation and, importantly, can exploit advantages associated with the emission of both high-frequency and long-duration calls. Low frequencies are unsuited for the detection of small prey, and low repetition rates may limit prey detection rates. Echolocation parameters may therefore constrain maximum body size in aerial-hawking bats.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                27 January 2016
                2016
                : 11
                : 1
                : e0148053
                Affiliations
                [1 ]Animal Evolution and Systematics Group (AES), Biological Sciences Department, University of Cape Town, Cape Town 7701, South Africa
                [2 ]Centre for Statistics in Ecology, Environment and Conservation (SEEC), South African National Biodiversity Institute (SANBI), Cape Town, South Africa
                University of Arkansas, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Conceived and designed the experiments: GLM DSJ. Performed the experiments: GLM DSJ. Analyzed the data: GLM HW. Contributed reagents/materials/analysis tools: DSJ. Wrote the paper: GLM DSJ HW.

                Article
                PONE-D-15-35946
                10.1371/journal.pone.0148053
                4729529
                26815436
                45b5a9a8-5301-49de-aecb-dca1d708068b
                © 2016 Mutumi et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 15 August 2015
                : 11 January 2016
                Page count
                Figures: 4, Tables: 1, Pages: 16
                Funding
                This research was supported by grants to DSJ from the University of Cape Town ( www.uct.ac.za) and the South African Research Chair Initiative of the Department of Science and Technology ( http://www.dst.gov.za), administered by the National Research Foundation ( http://www.nrf.ac.za), grant number—GUN 64798. GLM also received funding (Research Associateship award) from the University of Cape Town's Postgraduate Centre and Funding Office ( www.uct.ac.za). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Migration
                Animal Navigation
                Echolocation
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Migration
                Animal Navigation
                Echolocation
                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Signaling and Communication
                Echolocation
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Signaling and Communication
                Echolocation
                Biology and Life Sciences
                Physiology
                Sensory Physiology
                Auditory System
                Echolocation
                Medicine and Health Sciences
                Physiology
                Sensory Physiology
                Auditory System
                Echolocation
                Biology and Life Sciences
                Neuroscience
                Sensory Systems
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                Organisms
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                Physiological Parameters
                Physical Sciences
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                Acoustics
                Acoustic Signals
                Earth Sciences
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                Biology and Life Sciences
                Behavior
                Animal Behavior
                Animal Signaling and Communication
                Biology and Life Sciences
                Zoology
                Animal Behavior
                Animal Signaling and Communication
                Physical Sciences
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                Acoustics
                Bioacoustics
                Biology and Life Sciences
                Bioacoustics
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