Receiver bias and the acoustic ecology of aye-ayes (Daubentonia madagascariensis)
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Auteurs : Marissa A. Ramsier [États-Unis] ; Nathaniel J. Dominy [États-Unis]Source :
- Communicative & Integrative Biology [ 1942-0889 ] ; 2012.
Abstract
The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.
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DOI: 10.4161/cib.21509
PubMed: 23739157
PubMed Central: 3541336
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Receiver bias and the acoustic ecology of aye-ayes (<italic>Daubentonia madagascariensis</italic>)</title><author><name sortKey="Ramsier, Marissa A" sort="Ramsier, Marissa A" uniqKey="Ramsier M" first="Marissa A." last="Ramsier">Marissa A. Ramsier</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Anthropology; Humboldt State University; Arcata, CA USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Anthropology; Humboldt State University; Arcata</wicri:cityArea></affiliation></author><author><name sortKey="Dominy, Nathaniel J" sort="Dominy, Nathaniel J" uniqKey="Dominy N" first="Nathaniel J." last="Dominy">Nathaniel J. Dominy</name><affiliation wicri:level="2"><nlm:aff id="A2">Department of Anthropology; Dartmouth College; Hanover, NH USA</nlm:aff><country>États-Unis</country><placeName><region type="state">New Hampshire</region></placeName><wicri:cityArea>Department of Anthropology; Dartmouth College; Hanover</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Biological Sciences; Dartmouth College; Hanover, NH USA</nlm:aff><country>États-Unis</country><placeName><region type="state">New Hampshire</region></placeName><wicri:cityArea>Department of Biological Sciences; Dartmouth College; Hanover</wicri:cityArea></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">23739157</idno><idno type="pmc">3541336</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3541336</idno><idno type="RBID">PMC:3541336</idno><idno type="doi">10.4161/cib.21509</idno><date when="2012">2012</date><idno type="wicri:Area/Pmc/Corpus">001C57</idno><idno type="wicri:Area/Pmc/Curation">001C57</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Receiver bias and the acoustic ecology of aye-ayes (<italic>Daubentonia madagascariensis</italic>)</title><author><name sortKey="Ramsier, Marissa A" sort="Ramsier, Marissa A" uniqKey="Ramsier M" first="Marissa A." last="Ramsier">Marissa A. Ramsier</name><affiliation wicri:level="2"><nlm:aff id="A1">Department of Anthropology; Humboldt State University; Arcata, CA USA</nlm:aff><country>États-Unis</country><placeName><region type="state">Californie</region></placeName><wicri:cityArea>Department of Anthropology; Humboldt State University; Arcata</wicri:cityArea></affiliation></author><author><name sortKey="Dominy, Nathaniel J" sort="Dominy, Nathaniel J" uniqKey="Dominy N" first="Nathaniel J." last="Dominy">Nathaniel J. Dominy</name><affiliation wicri:level="2"><nlm:aff id="A2">Department of Anthropology; Dartmouth College; Hanover, NH USA</nlm:aff><country>États-Unis</country><placeName><region type="state">New Hampshire</region></placeName><wicri:cityArea>Department of Anthropology; Dartmouth College; Hanover</wicri:cityArea></affiliation><affiliation wicri:level="2"><nlm:aff id="A3">Department of Biological Sciences; Dartmouth College; Hanover, NH USA</nlm:aff><country>États-Unis</country><placeName><region type="state">New Hampshire</region></placeName><wicri:cityArea>Department of Biological Sciences; Dartmouth College; Hanover</wicri:cityArea></affiliation></author></analytic><series><title level="j">Communicative & Integrative Biology</title><idno type="eISSN">1942-0889</idno><imprint><date when="2012">2012</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Perry, Gh" uniqKey="Perry G">GH Perry</name></author><author><name sortKey="Reeves, D" uniqKey="Reeves D">D Reeves</name></author><author><name sortKey="Melsted, P" uniqKey="Melsted P">P Melsted</name></author><author><name sortKey="Ratan, A" uniqKey="Ratan A">A Ratan</name></author><author><name sortKey="Miller, W" uniqKey="Miller W">W Miller</name></author><author><name sortKey="Michelini, K" uniqKey="Michelini K">K Michelini</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Erickson, Cj" uniqKey="Erickson C">CJ Erickson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Erickson, Cj" uniqKey="Erickson C">CJ Erickson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Erickson, Cj" uniqKey="Erickson C">CJ Erickson</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Erickson, Cj" uniqKey="Erickson C">CJ Erickson</name></author><author><name sortKey="Nowicki, S" uniqKey="Nowicki S">S Nowicki</name></author><author><name sortKey="Dollar, L" uniqKey="Dollar L">L Dollar</name></author><author><name sortKey="Goehring, N" uniqKey="Goehring N">N Goehring</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Oxnard, Ce" uniqKey="Oxnard C">CE Oxnard</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Milliken, Gw" uniqKey="Milliken G">GW 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Ildari, Ad" uniqKey="Gosselin Ildari A">AD Gosselin-Ildari</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Lebrun, R" uniqKey="Lebrun R">R Lebrun</name></author><author><name sortKey="De Le N, Mp" uniqKey="De Le N M">MP de León</name></author><author><name sortKey="Tafforeau, P" uniqKey="Tafforeau P">P Tafforeau</name></author><author><name sortKey="Zollikofer, C" uniqKey="Zollikofer C">C Zollikofer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sterling, Ej" uniqKey="Sterling E">EJ Sterling</name></author><author><name sortKey="Povinelli, Dj" uniqKey="Povinelli D">DJ Povinelli</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ramsier, Ma" uniqKey="Ramsier M">MA Ramsier</name></author><author><name sortKey="Cunningham, Aj" uniqKey="Cunningham A">AJ Cunningham</name></author><author><name sortKey="Finneran, Jj" uniqKey="Finneran J">JJ Finneran</name></author><author><name 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Waser</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Mitani, J" uniqKey="Mitani J">J Mitani</name></author><author><name sortKey="Stuht, J" uniqKey="Stuht J">J Stuht</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Iwano, T" uniqKey="Iwano T">T Iwano</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Stanger, Kf" uniqKey="Stanger K">KF Stanger</name></author><author><name sortKey="Macedonia, Jm" uniqKey="Macedonia J">JM Macedonia</name></author></analytic></biblStruct><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Schlaepfer, Ma" uniqKey="Schlaepfer M">MA Schlaepfer</name></author><author><name sortKey="Runge, Mc" uniqKey="Runge M">MC Runge</name></author><author><name sortKey="Sherman, Pw" uniqKey="Sherman P">PW Sherman</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Perry, Gh" uniqKey="Perry G">GH Perry</name></author><author><name sortKey="Melsted, P" uniqKey="Melsted P">P Melsted</name></author><author><name sortKey="Marioni, Jc" uniqKey="Marioni J">JC Marioni</name></author><author><name sortKey="Wang, Y" uniqKey="Wang Y">Y Wang</name></author><author><name sortKey="Bainer, R" uniqKey="Bainer R">R Bainer</name></author><author><name sortKey="Pickrell, Jk" uniqKey="Pickrell J">JK Pickrell</name></author></analytic></biblStruct></listBibl></div1></back></TEI><pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Commun Integr Biol</journal-id><journal-id journal-id-type="iso-abbrev">Commun Integr Biol</journal-id><journal-id journal-id-type="publisher-id">CIB</journal-id><journal-title-group><journal-title>Communicative & Integrative Biology</journal-title></journal-title-group><issn pub-type="epub">1942-0889</issn><publisher><publisher-name>Landes Bioscience</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">23739157</article-id><article-id pub-id-type="pmc">3541336</article-id><article-id pub-id-type="publisher-id">2012CIB0069R</article-id><article-id pub-id-type="doi">10.4161/cib.21509</article-id><article-id pub-id-type="pii">21509</article-id><article-categories><subj-group subj-group-type="heading"><subject>Article Addendum</subject></subj-group></article-categories><title-group><article-title>Receiver bias and the acoustic ecology of aye-ayes (<italic>Daubentonia madagascariensis</italic>)</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Ramsier</surname><given-names>Marissa A.</given-names></name><xref ref-type="aff" rid="A1"><sup>1</sup></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><contrib contrib-type="author"><name><surname>Dominy</surname><given-names>Nathaniel J.</given-names></name><xref ref-type="aff" rid="A2"><sup>2</sup></xref><xref ref-type="aff" rid="A3"><sup>3</sup></xref><xref ref-type="corresp" rid="cor1">*</xref></contrib><aff id="A1"><label>1</label>Department of Anthropology; Humboldt State University; Arcata, CA USA</aff><aff id="A2"><label>2</label>Department of Anthropology; Dartmouth College; Hanover, NH USA</aff><aff id="A3"><label>3</label>Department of Biological Sciences; Dartmouth College; Hanover, NH USA</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Correspondence to: Marissa A. Ramsier, Email: <email xlink:href="marissa.ramsier@humboldt.edu">marissa.ramsier@humboldt.edu</email> and Nathaniel J. Dominy, Email: <email xlink:href="nathaniel.j.dominy@dartmouth.edu">nathaniel.j.dominy@dartmouth.edu</email></corresp></author-notes><pub-date pub-type="ppub"><day>01</day><month>11</month><year>2012</year></pub-date><pub-date pub-type="pmc-release"><day>01</day><month>11</month><year>2012</year></pub-date><pmc-comment> PMC Release delay is 0 months and 0 days and was based on the
<volume>5</volume><issue>6</issue><fpage>637</fpage><lpage>640</lpage><permissions><copyright-statement>Copyright © 2012 Landes Bioscience</copyright-statement><copyright-year>2012</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc/3.0/"><license-p>This is an open-access article licensed under a Creative Commons Attribution-NonCommercial 3.0 Unported License. The article may be redistributed, reproduced, and reused for non-commercial purposes, provided the original source is properly cited.</license-p></license></permissions><abstract><p>The aye-aye is a rare lemur from Madagascar that uses its highly specialized middle digit for percussive foraging. This acoustic behavior, also termed tap-scanning, produces dominant frequencies between 6 and 15 kHz. An enhanced auditory sensitivity to these frequencies raises the possibility that the acoustic and auditory specializations of aye-ayes have imposed constraints on the evolution of their vocal signals, especially their primary long-distance vocalization, the screech. Here we explore this concept, termed receiver bias, and suggest that the dominant frequency of the screech call (~2.7 kHz) represents an evolutionary compromise between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers.</p></abstract><kwd-group kwd-group-type="author"><title>Keywords: </title><kwd><italic>Daubentonia madagascariensis</italic></kwd><kwd>lemur</kwd><kwd>audiogram</kwd><kwd>auditory sensitivity</kwd><kwd>receiver bias</kwd><kwd>vocalization</kwd><kwd>sensory trap</kwd></kwd-group></article-meta></front><body><p>The aye-aye (<italic>Daubentonia madagascariensis</italic>) is a nocturnal primate endemic to Madagascar. It is an enduring source of fascination, both because of its many unique features and because it is the only survivor of a lineage with an origin ~70 million years ago.<xref ref-type="bibr" rid="R1"><sup>1</sup></xref> As a result, <italic>Daubentonia</italic> is allocated to its own family (Daubentoniidae) and infraorder (Chiromyiformes). The aye-aye is perhaps best known for its acoustic foraging behaviors, termed percussive foraging or tap-scanning,<xref ref-type="bibr" rid="R2"><sup>2</sup></xref><sup>-</sup><xref ref-type="bibr" rid="R5"><sup>5</sup></xref> and suite of unusual anatomical specializations, particularly in the hand, skull, and central nervous system.<xref ref-type="bibr" rid="R6"><sup>6</sup></xref><sup>-</sup><xref ref-type="bibr" rid="R15"><sup>15</sup></xref> For example, aye-ayes have elongated hands with long, thin middle fingers that have been described as villiform, filamentous, gracile, or grotesquely attenuated.<xref ref-type="bibr" rid="R6"><sup>6</sup></xref><sup>-</sup><xref ref-type="bibr" rid="R9"><sup>9</sup></xref> This singular digit is highly mobile<xref ref-type="bibr" rid="R10"><sup>10</sup></xref> due to a unique ball-and-socket metacarpophalangeal joint.<xref ref-type="bibr" rid="R12"><sup>12</sup></xref> Such morphology enables rapid tapping and the detection, localization, and extraction of embedded foods such as the wood-boring larvae of cerambycid beetles.<xref ref-type="bibr" rid="R13"><sup>13</sup></xref></p><p>For aye-ayes, the importance of percussive foraging (5–41% of foraging time<xref ref-type="bibr" rid="R13"><sup>13</sup></xref>) and the functional demands of integrating two sensory modalities -haptic touch and audition- appear to be linked with the evolution of large and elaborate ear structures<xref ref-type="bibr" rid="R16"><sup>16</sup></xref><sup>-</sup><xref ref-type="bibr" rid="R19"><sup>19</sup></xref> and the expansion of cerebral cortical regions associated with auditory processing, such as the inferior colliculus.<xref ref-type="bibr" rid="R11"><sup>11</sup></xref> As a result, aye-ayes are relatively encephalized and reported to have high levels of sensorimotor intelligence.<xref ref-type="bibr" rid="R20"><sup>20</sup></xref> Such attributes suggest that aye-ayes might also have exceptional hearing abilities, yet the auditory sensitivities of strepsirrhine primates are relatively unstudied.</p><sec><title>Aye-ayes as auditory specialists</title><p>Recently, Ramsier et al.<xref ref-type="bibr" rid="R21"><sup>21</sup></xref> used the auditory brainstem response (ABR) method to generate audiograms from 11 strepsirrhine primates, and they confirmed that aye-ayes have relatively enhanced auditory sensitivity between 2.8 and 22.6 kHz, with 2.8–15.9 kHz being the 10-dB bandwidth (the bandwidth across which thresholds are within 10 dB of the threshold of the frequency of best sensitivity).<xref ref-type="bibr" rid="R22"><sup>22</sup></xref> Although ABR-derived thresholds are sometimes elevated in comparison with behavioral tests of primates, especially for frequencies ≤ 2.0 kHz, the two methods produce audiograms with similar shapes, high-frequency limits, frequencies of best sensitivity, and upper-frequencies of the 10-dB bandwidth.<xref ref-type="bibr" rid="R22"><sup>22</sup></xref> Our estimate for the low-frequency end of the 10-dB bandwidth of aye-ayes appears robust given the close agreement between two individuals for all low-frequency thresholds (0.2–1.6 dB difference, depending on frequency), and the very steep incline for frequencies ≤ 1 kHz (already > 30 dB above the threshold of best sensitivity at 1 kHz).<xref ref-type="bibr" rid="R21"><sup>21</sup></xref></p><p>If we accept this region of best auditory sensitivity, we must now ask if it corresponds with the acoustic properties of percussive foraging. To explore this premise, we used a studio condenser microphone (Sennheiser, Old Lyme, Connecticut; frequency response 0.03–50 kHz) and a solid-state recorder (PMD-671, Marantz, Mahwah, New Jersey; sampling frequency 96 kHz, 24-bit) to analyze the percussive foraging of an adult male aye-aye, Merlin, housed at the Duke Lemur Center. We recorded tap-scanning on a typical stimulus used for enrichment purposes: 2x4-inch (5.1x10.2-cm) boards of Eastern white pine (<italic>Pinus strobus</italic>) permeated with food rewards. The rate of tapping was consistent across recordings (97.7 ± 19.9 ms) and each tap had a dominant energy of 6–15 kHz contained between 2 and 27 kHz (<xref ref-type="fig" rid="F1">Fig. 1A</xref>). The percussive tapping of aye-ayes is thus a broadband sound that corresponds well to their frequency region of best auditory sensitivity (<xref ref-type="fig" rid="F1">Fig. 1B</xref>); however, the acoustic attributes of a temperate softwood should be interpreted with caution. In the wild, extractive foraging is most strongly associated with the decaying stumps of trees, but aye-ayes do sometimes excavate living tissues (e.g., branches of <italic>Protorhus</italic> sp.; trees of <italic>Anthocleista</italic> spp.).<xref ref-type="bibr" rid="R3"><sup>3</sup></xref> The acoustics of percussive foraging on these woods are unknown.</p><fig id="F1" fig-type="figure" orientation="portrait" position="float"><caption><p><bold>Figure 1.</bold> (A) Adult aye-aye and spectrogram of percussive foraging behavior. Each tap of the third digit is discernable with a dominant energy of 6–15 kHz. (B) Mean audiogram of two aye-ayes and the region of best auditory sensitivity (modified from Ramsier et al.<xref ref-type="bibr" rid="R21"><sup>21</sup></xref>). Insert: spectrogram of the aye-aye’s primary long-distance vocalization, the screech (‘aack’ variant), with a dominant frequency of 2.66 kHz (modified from <xref ref-type="fig" rid="F1">Figure 1J</xref> in Stanger and Macedonia<xref ref-type="bibr" rid="R30"><sup>30</sup></xref>). Photograph of aye-aye by D.M. Haring, reproduced with permission.</p></caption><graphic xlink:href="cib-5-637-g1"></graphic></fig></sec><sec><title>Receiver bias and the vocal ecology of aye-ayes</title><p>Receiver bias, or preexisting bias, is a model of animal communication that emphasizes bias in the sensory systems of signal receivers.<xref ref-type="bibr" rid="R23"><sup>23</sup></xref> For aye-ayes, the auditory demands associated with percussive foraging might drive, or bias, the evolution of their vocal signals. According to this model, the dominant frequencies of aye-aye vocalizations are predicted to fall in the range of best auditory sensitivity, ca. 2.8–15.9 kHz (<xref ref-type="fig" rid="F1">Fig. 1B</xref>). Yet aye-ayes are solitary foragers with extensive home ranges (females: 30–40 ha; males: 120–215 ha),<xref ref-type="bibr" rid="R13"><sup>13</sup></xref> and population densities are sparse.<xref ref-type="bibr" rid="R24"><sup>24</sup></xref> Thus vocal signals must propagate through relatively vast expanses of forest. Under these conditions, environmental noise can exert a significant selective pressure on the acoustic structure of vocal signals,<xref ref-type="bibr" rid="R25"><sup>25</sup></xref> including those of primates.<xref ref-type="bibr" rid="R26"><sup>26</sup></xref> In fact, most primates have evolved long-distance calls with dominant frequencies < 1.5 kHz,<xref ref-type="bibr" rid="R27"><sup>27</sup></xref> probably because they propagate farther and are less susceptible to masking by forest noise.</p><p>The primary long-distance vocalization, or contact call, between aye-ayes has been described onomatopoetically (<italic>creee</italic> or <italic>nee-a</italic>) and prosaically (screech).<xref ref-type="bibr" rid="R28"><sup>28</sup></xref><sup>-</sup><xref ref-type="bibr" rid="R30"><sup>30</sup></xref> The screech is a variable signal with a dominant frequency of 2.66 kHz and a peak frequency of 8.45 kHz.<xref ref-type="bibr" rid="R30"><sup>30</sup></xref> In addition, two types of alarm call, or screams, have dominant frequencies of 2.80 and 3.25 kHz and peak frequencies of 8.58 and 9.20 kHz.<xref ref-type="bibr" rid="R30"><sup>30</sup></xref> The similar acoustic properties of these calls is puzzling given their different functions. Long-distance calls normally have low dominant frequencies,<xref ref-type="bibr" rid="R27"><sup>27</sup></xref> whereas alarm calls have much higher dominant frequencies.<xref ref-type="bibr" rid="R31"><sup>31</sup></xref> For aye-ayes, it is plausible that a dominant frequency close to ~2.7 kHz represents an evolutionary tradeoff between the opposing adaptive advantages of long-distance sound propagation and enhanced detection by conspecific receivers (<xref ref-type="fig" rid="F1">Fig. 1B</xref>). Yet the elegance of this potential compromise is deceptive in part because it raises the possibility that aye-ayes are caught in a sensory trap.<xref ref-type="bibr" rid="R23"><sup>23</sup></xref></p></sec><sec><title>Sensory traps and the reproductive ecology of aye-ayes</title><p>Sensory traps are part of a broader concept, the evolutionary trap,<xref ref-type="bibr" rid="R32"><sup>32</sup></xref> which holds that animals can experience reduced fitness, or become ‘trapped’, by their own sensory adaptations.<xref ref-type="bibr" rid="R23"><sup>23</sup></xref> Here we hypothesize that the auditory demands of percussive foraging resulted in a receiver bias that precluded the evolution of lower-frequency contact calls. This constraint is expected to become increasingly suboptimal (i.e., contact calls will be increasingly inaudible) as aye-ayes become more widely dispersed as a result of habitat fragmentation. Indeed, the exceedingly low genetic diversity of aye-ayes is puzzling given their large geographic distribution.<xref ref-type="bibr" rid="R33"><sup>33</sup></xref> These recent findings suggest that aye-ayes are quite vulnerable to extinction, not least, perhaps, because they have a limited ability to communicate over large distances.</p><p>In sum, we suggest that the unique acoustic ecology and auditory adaptations of aye-ayes have partly contributed to their low genetic diversity. Although speculative, this concept of a sensory trap invites testing; if true, it has profound conservation implications for a unique and highly endangered primate.</p></sec></body><back><ack><title>Acknowledgments</title><p>We thank D.M. Brewer, A.J. Cunningham, E. Ehmke, D.M. Haring, A.D. Melin, G.L. Moritz, G.H. Perry, A.D. Yoder, and S. Zehr for their comments and contributions to this research, and the David and Lucile Packard Foundation for funding (Fellowship no. 2007–31754). Data were collected at the Duke Lemur Center (Durham, USA) under protocols approved by the Institutional Animal Care and Use Committees of Dartmouth College, Duke University, and the Duke Lemur Center (approval nos. 10–11–02, A209–08–08, and M-5–08–1, respectively). This is Duke Lemur Center publication no. 1229.</p></ack><fn-group><fn fn-type="other"><p>Previously published online: <ext-link ext-link-type="uri" xlink:href="http://www.landesbioscience.com/journals/cib/article/21509/">www.landesbioscience.com/journals/cib/article/21509</ext-link></p></fn></fn-group><notes><p><related-article id="d37e363" related-article-type="article-reference" ext-link-type="doi" xlink:href="10.1098/rstb.2011.0219" journal-id="Philos Trans R Soc Lond B Biol Sci" vol="367" page="1860"><person-group person-group-type="author"><name><surname>Ramsier</surname><given-names>MA</given-names></name><name><surname>Cunningham</surname><given-names>AJ</given-names></name><name><surname>Finneran</surname><given-names>JJ</given-names></name><name><surname>Dominy</surname><given-names>NJ</given-names></name></person-group><article-title>Social drive and the evolution of primate hearing</article-title><source>Philos Trans R Soc Lond B Biol Sci</source><year>2012</year><volume>367</volume><fpage>1860</fpage><lpage>8</lpage><pub-id pub-id-type="doi">10.1098/rstb.2011.0219</pub-id></related-article></p></notes><ref-list><title>References</title><ref id="R1"><label>1</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Perry</surname><given-names>GH</given-names></name><name><surname>Reeves</surname><given-names>D</given-names></name><name><surname>Melsted</surname><given-names>P</given-names></name><name><surname>Ratan</surname><given-names>A</given-names></name><name><surname>Miller</surname><given-names>W</given-names></name><name><surname>Michelini</surname><given-names>K</given-names></name><etal></etal></person-group><article-title>A genome sequence resource for the aye-aye (<italic>Daubentonia madagascariensis</italic>), a nocturnal lemur from Madagascar</article-title><source>Genome Biol Evol</source><year>2012</year><volume>4</volume><fpage>126</fpage><lpage>35</lpage><pub-id pub-id-type="doi">10.1093/gbe/evr132</pub-id><pub-id pub-id-type="pmid">22155688</pub-id></element-citation></ref><ref id="R2"><label>2</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Erickson</surname><given-names>CJ</given-names></name></person-group><article-title>Percussive foraging in the aye-aye, <italic>Daubentonia madagascariensis.</italic></article-title><source>Anim Behav</source><year>1991</year><volume>41</volume><fpage>793</fpage><lpage>801</lpage><pub-id pub-id-type="doi">10.1016/S0003-3472(05)80346-X</pub-id></element-citation></ref><ref id="R3"><label>3</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Erickson</surname><given-names>CJ</given-names></name></person-group><article-title>Feeding sites for extractive foraging by the aye-aye, <italic>Daubentonia madagascariensis.</italic></article-title><source>Am J Primatol</source><year>1995</year><volume>35</volume><fpage>235</fpage><lpage>40</lpage><pub-id pub-id-type="doi">10.1002/ajp.1350350306</pub-id></element-citation></ref><ref id="R4"><label>4</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Erickson</surname><given-names>CJ</given-names></name></person-group><article-title>Cues for prey location by aye-ayes (<italic>Daubentonia madagascariensis</italic>)</article-title><source>Folia Primatol (Basel)</source><year>1998</year><volume>69</volume><fpage>35</fpage><lpage>40</lpage><pub-id pub-id-type="doi">10.1159/000052697</pub-id><pub-id pub-id-type="pmid">9429314</pub-id></element-citation></ref><ref id="R5"><label>5</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Erickson</surname><given-names>CJ</given-names></name><name><surname>Nowicki</surname><given-names>S</given-names></name><name><surname>Dollar</surname><given-names>L</given-names></name><name><surname>Goehring</surname><given-names>N</given-names></name></person-group><article-title>Percussive foraging: Stimuli for prey location by aye-ayes (<italic>Daubentonia madagascariensis</italic>)</article-title><source>Int J Primatol</source><year>1998</year><volume>19</volume><fpage>111</fpage><lpage>22</lpage><pub-id pub-id-type="doi">10.1023/A:1020363128240</pub-id></element-citation></ref><ref id="R6"><label>6</label><mixed-citation publication-type="book">Owen R. Monograph on the aye-aye (<italic>Chiromys madagascariensis</italic>, Cuvier). London: Taylor and Francis, 1863.</mixed-citation></ref><ref id="R7"><label>7</label><mixed-citation publication-type="book">Cartmill M. <italic>Daubentonia, Dactylopsila</italic>, woodpeckers and klinorhynchy. In: Martin RD, Doyle GA, Walker AC, eds. Prosimian Biology. Gloucester: Duckworth, 1974:655-70.</mixed-citation></ref><ref id="R8"><label>8</label><mixed-citation publication-type="book">Jouffroy FK. Osteology and myology of the lemuriform postcranial skeleton. In: Tattersall I, Sussman RW, eds. Lemur Biology. New York: Plenum Press, 1975:149-92.</mixed-citation></ref><ref id="R9"><label>9</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Oxnard</surname><given-names>CE</given-names></name></person-group><article-title>The uniqueness of <italic>Daubentonia.</italic></article-title><source>Am J Phys Anthropol</source><year>1981</year><volume>54</volume><fpage>1</fpage><lpage>21</lpage><pub-id pub-id-type="doi">10.1002/ajpa.1330540102</pub-id></element-citation></ref><ref id="R10"><label>10</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Milliken</surname><given-names>GW</given-names></name><name><surname>Ward</surname><given-names>JP</given-names></name><name><surname>Erickson</surname><given-names>CJ</given-names></name></person-group><article-title>Independent digit control in foraging by the aye-aye (<italic>Daubentonia madagascariensis</italic>)</article-title><source>Folia Primatol (Basel)</source><year>1991</year><volume>56</volume><fpage>219</fpage><lpage>24</lpage><pub-id pub-id-type="doi">10.1159/000156551</pub-id><pub-id pub-id-type="pmid">1937286</pub-id></element-citation></ref><ref id="R11"><label>11</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kaufman</surname><given-names>JA</given-names></name><name><surname>Ahrens</surname><given-names>ET</given-names></name><name><surname>Laidlaw</surname><given-names>DH</given-names></name><name><surname>Zhang</surname><given-names>S</given-names></name><name><surname>Allman</surname><given-names>JM</given-names></name></person-group><article-title>Anatomical analysis of an aye-aye brain (<italic>Daubentonia madagascariensis</italic>, primates: Prosimii) combining histology, structural magnetic resonance imaging, and diffusion-tensor imaging</article-title><source>Anat Rec A Discov Mol Cell Evol Biol</source><year>2005</year><volume>287</volume><fpage>1026</fpage><lpage>37</lpage><pub-id pub-id-type="doi">10.1002/ar.a.20264</pub-id><pub-id pub-id-type="pmid">16211637</pub-id></element-citation></ref><ref id="R12"><label>12</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Soligo</surname><given-names>C</given-names></name></person-group><article-title>Anatomy of the hand and arm in <italic>Daubentonia madagascariensis</italic> : a functional and phylogenetic outlook</article-title><source>Folia Primatol (Basel)</source><year>2005</year><volume>76</volume><fpage>262</fpage><lpage>300</lpage><pub-id pub-id-type="doi">10.1159/000088034</pub-id><pub-id pub-id-type="pmid">16230860</pub-id></element-citation></ref><ref id="R13"><label>13</label><mixed-citation publication-type="book">Sterling EJ, McCreless EE. Adaptations in the aye-aye: A review. In: Gould L, Sauther ML, eds. Lemurs: Ecology and adaptation. New York: Springer, 2006:159-84.</mixed-citation></ref><ref id="R14"><label>14</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Melin</surname><given-names>AD</given-names></name><name><surname>Moritz</surname><given-names>GL</given-names></name><name><surname>Fosbury</surname><given-names>RAE</given-names></name><name><surname>Kawamura</surname><given-names>S</given-names></name><name><surname>Dominy</surname><given-names>NJ</given-names></name></person-group><article-title>Why aye-ayes see blue</article-title><source>Am J Primatol</source><year>2012</year><volume>74</volume><fpage>185</fpage><lpage>92</lpage><pub-id pub-id-type="doi">10.1002/ajp.21996</pub-id></element-citation></ref><ref id="R15"><label>15</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Moritz</surname><given-names>GL</given-names></name><name><surname>Dominy</surname><given-names>NJ</given-names></name></person-group><article-title>Thermal imaging of aye-ayes (<italic>Daubentonia madagascariensis</italic>) reveals a dynamic vascular supply during haptic sensation</article-title><source>Int J Primatol</source><year>2012</year><pub-id pub-id-type="doi">10.1007/s10764-011-9575-y</pub-id></element-citation></ref><ref id="R16"><label>16</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Coleman</surname><given-names>MN</given-names></name><name><surname>Ross</surname><given-names>CF</given-names></name></person-group><article-title>Primate auditory diversity and its influence on hearing performance</article-title><source>Anat Rec A Discov Mol Cell Evol Biol</source><year>2004</year><volume>281</volume><fpage>1123</fpage><lpage>37</lpage><pub-id pub-id-type="doi">10.1002/ar.a.20118</pub-id><pub-id pub-id-type="pmid">15470672</pub-id></element-citation></ref><ref id="R17"><label>17</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Masali</surname><given-names>M</given-names></name><name><surname>Cremasco</surname><given-names>MM</given-names></name></person-group><article-title><italic>Hoc alterum auditus organi ossiculum est</italic>: Ear ossicles in physical anthropology</article-title><source>Hum Evol</source><year>2006</year><volume>21</volume><fpage>1</fpage><lpage>17</lpage><pub-id pub-id-type="doi">10.1007/s11598-006-9000-2</pub-id></element-citation></ref><ref id="R18"><label>18</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Kirk</surname><given-names>EC</given-names></name><name><surname>Gosselin-Ildari</surname><given-names>AD</given-names></name></person-group><article-title>Cochlear labyrinth volume and hearing abilities in primates</article-title><source>Anat Rec A Discov Mol Cell Evol Biol</source><year>2009</year><volume>292</volume><fpage>765</fpage><lpage>76</lpage><pub-id pub-id-type="doi">10.1002/ar.20907</pub-id><pub-id pub-id-type="pmid">19462443</pub-id></element-citation></ref><ref id="R19"><label>19</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Lebrun</surname><given-names>R</given-names></name><name><surname>de León</surname><given-names>MP</given-names></name><name><surname>Tafforeau</surname><given-names>P</given-names></name><name><surname>Zollikofer</surname><given-names>C</given-names></name></person-group><article-title>Deep evolutionary roots of strepsirrhine primate labyrinthine morphology</article-title><source>J Anat</source><year>2010</year><volume>216</volume><fpage>368</fpage><lpage>80</lpage><pub-id pub-id-type="doi">10.1111/j.1469-7580.2009.01177.x</pub-id><pub-id pub-id-type="pmid">20039977</pub-id></element-citation></ref><ref id="R20"><label>20</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Sterling</surname><given-names>EJ</given-names></name><name><surname>Povinelli</surname><given-names>DJ</given-names></name></person-group><article-title>Tool use, aye-ayes, and sensorimotor intelligence</article-title><source>Folia Primatol (Basel)</source><year>1999</year><volume>70</volume><fpage>8</fpage><lpage>16</lpage><pub-id pub-id-type="doi">10.1159/000021669</pub-id><pub-id pub-id-type="pmid">10050062</pub-id></element-citation></ref><ref id="R21"><label>21</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ramsier</surname><given-names>MA</given-names></name><name><surname>Cunningham</surname><given-names>AJ</given-names></name><name><surname>Finneran</surname><given-names>JJ</given-names></name><name><surname>Dominy</surname><given-names>NJ</given-names></name></person-group><article-title>Social drive and the evolution of primate hearing</article-title><source>Philos Trans R Soc Lond B Biol Sci</source><year>2012</year><volume>367</volume><fpage>1860</fpage><lpage>8</lpage><pub-id pub-id-type="doi">10.1098/rstb.2011.0219</pub-id><pub-id pub-id-type="pmid">22641824</pub-id></element-citation></ref><ref id="R22"><label>22</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Ramsier</surname><given-names>MA</given-names></name><name><surname>Dominy</surname><given-names>NJ</given-names></name></person-group><article-title>A comparison of auditory brainstem responses and behavioral estimates of hearing sensitivity in <italic>Lemur catta</italic> and <italic>Nycticebus coucang.</italic></article-title><source>Am J Primatol</source><year>2010</year><volume>72</volume><fpage>217</fpage><lpage>33</lpage><pub-id pub-id-type="doi">10.1002/ajp.20780</pub-id><pub-id pub-id-type="pmid">19938053</pub-id></element-citation></ref><ref id="R23"><label>23</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Endler</surname><given-names>JA</given-names></name><name><surname>Basolo</surname><given-names>AL</given-names></name></person-group><article-title>Sensory ecology, receiver biases and sexual selection</article-title><source>Trends Ecol Evol</source><year>1998</year><volume>13</volume><fpage>415</fpage><lpage>20</lpage><pub-id pub-id-type="doi">10.1016/S0169-5347(98)01471-2</pub-id><pub-id pub-id-type="pmid">21238370</pub-id></element-citation></ref><ref id="R24"><label>24</label><mixed-citation publication-type="book">Mittermeier R, Hawkins F, Louis EE. Lemurs of Madagascar, 3rd Edition. Arlington: Conservation International, 2010.</mixed-citation></ref><ref id="R25"><label>25</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Brumm</surname><given-names>H</given-names></name><name><surname>Slabbekoorn</surname><given-names>H</given-names></name></person-group><article-title>Acoustic communication in noise</article-title><source>Adv Stud Behav</source><year>2005</year><volume>35</volume><fpage>151</fpage><lpage>209</lpage><pub-id pub-id-type="doi">10.1016/S0065-3454(05)35004-2</pub-id></element-citation></ref><ref id="R26"><label>26</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Brown</surname><given-names>CH</given-names></name><name><surname>Gomez</surname><given-names>R</given-names></name><name><surname>Waser</surname><given-names>PM</given-names></name></person-group><article-title>Old world monkey vocalizations: Adaptation to the local habitat?</article-title><source>Anim Behav</source><year>1995</year><volume>50</volume><fpage>945</fpage><lpage>61</lpage><pub-id pub-id-type="doi">10.1016/0003-3472(95)80096-4</pub-id></element-citation></ref><ref id="R27"><label>27</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Mitani</surname><given-names>J</given-names></name><name><surname>Stuht</surname><given-names>J</given-names></name></person-group><article-title>The evolution of nonhuman primate loud calls: Acoustic adaptation for long-distance transmission</article-title><source>Primates</source><year>1998</year><volume>39</volume><fpage>171</fpage><lpage>82</lpage><pub-id pub-id-type="doi">10.1007/BF02557729</pub-id></element-citation></ref><ref id="R28"><label>28</label><mixed-citation publication-type="book">Petter J-J. The aye-aye. In: HSH Prince Rainier III of Monaco, Bourne GH, eds. Primate Conservation. New York: Academic Press, 1977:37-57.</mixed-citation></ref><ref id="R29"><label>29</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Iwano</surname><given-names>T</given-names></name></person-group><article-title>An ecological and behavioral study of the aye-aye (<italic>Daubentonia madagascariensis</italic>)</article-title><source>Afr Study Monogr</source><year>1991</year><volume>12</volume><fpage>19</fpage><lpage>42</lpage></element-citation></ref><ref id="R30"><label>30</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Stanger</surname><given-names>KF</given-names></name><name><surname>Macedonia</surname><given-names>JM</given-names></name></person-group><article-title>Vocalizations of aye-ayes (<italic>Daubentonia madagascariensis</italic>) in captivity</article-title><source>Folia Primatol (Basel)</source><year>1994</year><volume>62</volume><fpage>160</fpage><lpage>9</lpage><pub-id pub-id-type="doi">10.1159/000156773</pub-id><pub-id pub-id-type="pmid">7721203</pub-id></element-citation></ref><ref id="R31"><label>31</label><mixed-citation publication-type="book">Caro T. Antipredator defenses in birds and mammals. Chicago: University of Chicago Press, 2005.</mixed-citation></ref><ref id="R32"><label>32</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Schlaepfer</surname><given-names>MA</given-names></name><name><surname>Runge</surname><given-names>MC</given-names></name><name><surname>Sherman</surname><given-names>PW</given-names></name></person-group><article-title>Ecological and evolutionary traps</article-title><source>Trends Ecol Evol</source><year>2002</year><volume>17</volume><fpage>474</fpage><lpage>80</lpage><pub-id pub-id-type="doi">10.1016/S0169-5347(02)02580-6</pub-id></element-citation></ref><ref id="R33"><label>33</label><element-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Perry</surname><given-names>GH</given-names></name><name><surname>Melsted</surname><given-names>P</given-names></name><name><surname>Marioni</surname><given-names>JC</given-names></name><name><surname>Wang</surname><given-names>Y</given-names></name><name><surname>Bainer</surname><given-names>R</given-names></name><name><surname>Pickrell</surname><given-names>JK</given-names></name><etal></etal></person-group><article-title>Comparative RNA sequencing reveals substantial genetic variation in endangered primates</article-title><source>Genome Res</source><year>2012</year><volume>22</volume><fpage>602</fpage><lpage>10</lpage><pub-id pub-id-type="doi">10.1101/gr.130468.111</pub-id><pub-id pub-id-type="pmid">22207615</pub-id></element-citation></ref></ref-list></back></pmc></record>Pour manipuler ce document sous Unix (Dilib)
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