Niche convergence suggests functionality of the nocturnal fovea
Identifieur interne : 003206 ( Ncbi/Merge ); précédent : 003205; suivant : 003207Niche convergence suggests functionality of the nocturnal fovea
Auteurs : Gillian L. Moritz [États-Unis] ; Amanda D. Melin [États-Unis] ; Fred Tuh Yit Yu [Malaisie] ; Henry Bernard [Malaisie] ; Perry S. Ong [Philippines] ; Nathaniel J. Dominy [États-Unis]Source :
- Frontiers in Integrative Neuroscience [ 1662-5145 ] ; 2014.
Abstract
The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (
Url:
DOI: 10.3389/fnint.2014.00061
PubMed: 25120441
PubMed Central: 4110675
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<front><div type="abstract" xml:lang="en"><p>The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (<italic>Tarsius</italic>
) and scops owls (<italic>Otus</italic>
), taxa united by numerous anatomical homoplasies, including foveate vision. A functional interpretation of these homoplasies predicts dietary convergence. We tested this prediction by analyzing stable isotope ratios that integrate dietary information. In Borneo and the Philippines, the stable carbon isotope compositions of <italic>Tarsius</italic>
and <italic>Otus</italic>
were indistinguishable, whereas the stable nitrogen isotope composition of <italic>Otus</italic>
was marginally higher than that of <italic>Tarsius</italic>
. Our results indicate that species in both genera consumed mainly ground-dwelling prey. Taken together, our findings support a functional interpretation of the many homoplasies shared by tarsiers and scops owls, including a retinal fovea. We suggest that the fovea might function similarly in tarsiers and scops owls by calibrating the auditory localization pathway. The integration of auditory localization and visual fixation during prey detection and acquisition might be critical at low light levels.</p>
</div>
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<pmc article-type="research-article"><pmc-dir>properties open_access</pmc-dir>
<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Integr Neurosci</journal-id>
<journal-id journal-id-type="iso-abbrev">Front Integr Neurosci</journal-id>
<journal-id journal-id-type="publisher-id">Front. Integr. Neurosci.</journal-id>
<journal-title-group><journal-title>Frontiers in Integrative Neuroscience</journal-title>
</journal-title-group>
<issn pub-type="epub">1662-5145</issn>
<publisher><publisher-name>Frontiers Media S.A.</publisher-name>
</publisher>
</journal-meta>
<article-meta><article-id pub-id-type="pmid">25120441</article-id>
<article-id pub-id-type="pmc">4110675</article-id>
<article-id pub-id-type="doi">10.3389/fnint.2014.00061</article-id>
<article-categories><subj-group subj-group-type="heading"><subject>Neuroscience</subject>
<subj-group><subject>Original Research Article</subject>
</subj-group>
</subj-group>
</article-categories>
<title-group><article-title>Niche convergence suggests functionality of the nocturnal fovea</article-title>
</title-group>
<contrib-group><contrib contrib-type="author"><name><surname>Moritz</surname>
<given-names>Gillian L.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="author-notes" rid="fn002"><sup>*</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/102473"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Melin</surname>
<given-names>Amanda D.</given-names>
</name>
<xref ref-type="aff" rid="aff2"><sup>2</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/172595"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Tuh Yit Yu</surname>
<given-names>Fred</given-names>
</name>
<xref ref-type="aff" rid="aff3"><sup>3</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Bernard</surname>
<given-names>Henry</given-names>
</name>
<xref ref-type="aff" rid="aff4"><sup>4</sup>
</xref>
</contrib>
<contrib contrib-type="author"><name><surname>Ong</surname>
<given-names>Perry S.</given-names>
</name>
<xref ref-type="aff" rid="aff5"><sup>5</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/147475"></uri>
</contrib>
<contrib contrib-type="author"><name><surname>Dominy</surname>
<given-names>Nathaniel J.</given-names>
</name>
<xref ref-type="aff" rid="aff1"><sup>1</sup>
</xref>
<xref ref-type="aff" rid="aff6"><sup>6</sup>
</xref>
<uri xlink:type="simple" xlink:href="http://community.frontiersin.org/people/u/163110"></uri>
</contrib>
</contrib-group>
<aff id="aff1"><sup>1</sup>
<institution>Department of Biological Sciences, The Class of 1978 Life Sciences Center, Dartmouth College</institution>
<country>Hanover, NH, USA</country>
</aff>
<aff id="aff2"><sup>2</sup>
<institution>Department of Anthropology, Washington University, St. Louis</institution>
<country>MO, USA</country>
</aff>
<aff id="aff3"><sup>3</sup>
<institution>Research and Education Division, Zoology and Entomology</institution>
<country>Kota Kinabalu, Malaysia</country>
</aff>
<aff id="aff4"><sup>4</sup>
<institution>Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah</institution>
<country>Kota Kinabalu, Malaysia</country>
</aff>
<aff id="aff5"><sup>5</sup>
<institution>Institute of Biology, University of the Philippines Diliman</institution>
<country>Quezon City, Philippines</country>
</aff>
<aff id="aff6"><sup>6</sup>
<institution>Department of Anthropology, Dartmouth College</institution>
<country>Hanover, NH, USA</country>
</aff>
<author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Sharif A. Taha, University of Utah Medical School, USA</italic>
</p>
</fn>
<fn fn-type="edited-by"><p>Reviewed by: <italic>Andreas Reichenbach, University of Leipzig, Germany; Luiz Carlos L. Silveira, Universidade Federal do Pará, Brazil</italic>
</p>
</fn>
<corresp id="fn002">*Correspondence: <italic>Gillian L. Moritz, Department of Biological Sciences, The Class of 1978 Life Sciences Center, Dartmouth College, 78 College Street, Hanover, NH 03755, USA e-mail: <email xlink:type="simple">gillian.l.moritz@dartmouth.edu</email>
</italic>
</corresp>
<fn fn-type="other" id="fn001"><p>This article was submitted to the journal Frontiers in Integrative Neuroscience.</p>
</fn>
</author-notes>
<pub-date pub-type="epub"><day>25</day>
<month>7</month>
<year>2014</year>
</pub-date>
<pub-date pub-type="collection"><year>2014</year>
</pub-date>
<volume>8</volume>
<elocation-id>61</elocation-id>
<history><date date-type="received"><day>25</day>
<month>3</month>
<year>2014</year>
</date>
<date date-type="accepted"><day>08</day>
<month>7</month>
<year>2014</year>
</date>
</history>
<permissions><copyright-statement>Copyright © 2014 Moritz, Melin, Tuh Yit Yu, Bernard, Ong and Dominy.</copyright-statement>
<copyright-year>2014</copyright-year>
<license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by/3.0/"><license-p> This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p>
</license>
</permissions>
<abstract><p>The fovea is a declivity of the retinal surface associated with maximum visual acuity. Foveae are widespread across vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans), which are primarily diurnal. Thus primates have long contributed to the view that foveae are functional adaptations to diurnality. The foveae of tarsiers, which are nocturnal, are widely interpreted as vestigial traits and therefore evidence of a diurnal ancestry. This enduring premise is central to adaptive hypotheses on the origins of anthropoid primates; however, the question of whether tarsier foveae are functionless anachronisms or nocturnal adaptations remains open. To explore this question, we compared the diets of tarsiers (<italic>Tarsius</italic>
) and scops owls (<italic>Otus</italic>
), taxa united by numerous anatomical homoplasies, including foveate vision. A functional interpretation of these homoplasies predicts dietary convergence. We tested this prediction by analyzing stable isotope ratios that integrate dietary information. In Borneo and the Philippines, the stable carbon isotope compositions of <italic>Tarsius</italic>
and <italic>Otus</italic>
were indistinguishable, whereas the stable nitrogen isotope composition of <italic>Otus</italic>
was marginally higher than that of <italic>Tarsius</italic>
. Our results indicate that species in both genera consumed mainly ground-dwelling prey. Taken together, our findings support a functional interpretation of the many homoplasies shared by tarsiers and scops owls, including a retinal fovea. We suggest that the fovea might function similarly in tarsiers and scops owls by calibrating the auditory localization pathway. The integration of auditory localization and visual fixation during prey detection and acquisition might be critical at low light levels.</p>
</abstract>
<kwd-group><kwd>fovea centralis</kwd>
<kwd>stable isotopes</kwd>
<kwd><italic>Otus lempiji</italic>
</kwd>
<kwd><italic>Otus megalotis</italic>
</kwd>
<kwd><italic>Tarsius bancanus</italic>
</kwd>
<kwd><italic>Tarsius syrichta</italic>
</kwd>
<kwd>diet</kwd>
<kwd>visual predation</kwd>
</kwd-group>
<counts><fig-count count="5"></fig-count>
<table-count count="0"></table-count>
<equation-count count="0"></equation-count>
<ref-count count="161"></ref-count>
<page-count count="12"></page-count>
<word-count count="0"></word-count>
</counts>
</article-meta>
</front>
<body><sec><title>INTRODUCTION</title>
<p>The <italic>fovea centralis</italic>
, or fovea, is an avascular declivity of the retinal surface. It is aligned with the visual axis of the eye and contains a disproportionately high density of photoreceptors. The optics of foveae are an enduring interest (<xref rid="B143" ref-type="bibr">Walls, 1937</xref>
; <xref rid="B147" ref-type="bibr">Weale, 1966</xref>
; <xref rid="B76" ref-type="bibr">Locket, 1992</xref>
; <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
) because the fovea has greater spatial resolving power than other retinal specialization (<xref rid="B54" ref-type="bibr">Inzunza et al., 1989</xref>
; <xref rid="B90" ref-type="bibr">Moore et al., 2012</xref>
). A fovea is therefore the site of maximal visual acuity among vertebrates (<xref rid="B144" ref-type="bibr">Walls, 1942</xref>
; <xref rid="B107" ref-type="bibr">Polyak, 1957</xref>
; <xref rid="B109" ref-type="bibr">Provis et al., 2013</xref>
). The energetic cost of high-acuity vision is presumed to be high due to the large volume of cortical tissue devoted to foveal vision (<xref rid="B105" ref-type="bibr">Perry and Cowey, 1985</xref>
; <xref rid="B128" ref-type="bibr">Silveira et al., 1989</xref>
; <xref rid="B47" ref-type="bibr">Hendrickson, 2005</xref>
). Indeed, the tandem concept of sensory specialization and cortical overrepresentation, or magnification, is now practically idiomatic: gymnotid and mormyrid fish have electrosensory “foveas”; (<xref rid="B6" ref-type="bibr">Castelló et al., 2000</xref>
; <xref rid="B3" ref-type="bibr">Bacelo et al., 2008</xref>
); echolocating bats have acoustic “foveas” (<xref rid="B93" ref-type="bibr">Neuweiler, 2003</xref>
); and some haptic species have tactile or somatosensory “foveas” (<xref rid="B106" ref-type="bibr">Pettigrew and Frost, 1985</xref>
; <xref rid="B9" ref-type="bibr">Catania and Remple, 2004</xref>
; <xref rid="B50" ref-type="bibr">Hoffmann et al., 2004</xref>
; <xref rid="B80" ref-type="bibr">Mancini et al., 2013</xref>
).</p>
<p>Foveal vision is assumed to serve a vital adaptive function and the comparative biology of foveate taxa has proven instructive (review: <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
). Foveae are widespread among diurnal vertebrates, but among mammals they are restricted to haplorhine primates (tarsiers, monkeys, apes, and humans). This taxonomic distribution suggests that foveae are an adaptation to diurnal or photopic conditions. The strongest support for this view stems from taxa that shifted or reversed their primary activity pattern. For example, geckos are secondarily nocturnal and a fovea is normally absent (<xref rid="B118" ref-type="bibr">Ross, 2004</xref>
); however, some 15 genera have reverted to diurnality and regained foveate vision (<xref rid="B135" ref-type="bibr">Tansley, 1960</xref>
; <xref rid="B116" ref-type="bibr">Röll, 2001</xref>
). Multiple tertiary origins of foveae within Gekkonidae suggest that the selective advantages of high-acuity vision are strongest under photopic conditions. Yet some nocturnal birds and many deep-sea fish possess rod-dominant foveae (<xref rid="B4" ref-type="bibr">Bowmaker and Martin, 1978</xref>
; <xref rid="B11" ref-type="bibr">Collin, 1999</xref>
; <xref rid="B12" ref-type="bibr">Collin et al., 2000</xref>
), raising the possibility that a nocturnal fovea is not always a scotopic anachronism.</p>
<p>The question of whether nocturnal foveae are adaptations or functionless vestiges is central to the study of primate evolution. Currently, two haplorhine taxa – tarsiers (<italic>Tarsius</italic>
) and night monkeys (<italic>Aotus</italic>
) – are nocturnal, and the former sits at a crucial position in the primate phylogenetic tree (<bold>Figure <xref ref-type="fig" rid="F1">1</xref>
</bold>
). Tarsiers are the basal crown haplorhine primate and their fovea has long informed hypotheses on the origins of anthropoid primates (<xref rid="B137" ref-type="bibr">Treacher Collins, 1922</xref>
; <xref rid="B23" ref-type="bibr">Elliot Smith, 1928</xref>
; <xref rid="B73" ref-type="bibr">Le Gros Clark, 1959</xref>
; <xref rid="B5" ref-type="bibr">Cartmill, 1980</xref>
; <xref rid="B83" ref-type="bibr">Martin, 1990</xref>
; <xref rid="B117" ref-type="bibr">Ross, 2000</xref>
, <xref rid="B118" ref-type="bibr">2004</xref>
; <xref rid="B84" ref-type="bibr">Martin and Ross, 2005</xref>
; <xref rid="B152" ref-type="bibr">Williams et al., 2010</xref>
). And yet, <italic>Aotus</italic>
has been the model taxon for understanding foveal degeneracy.</p>
<fig id="F1" position="float"><label>FIGURE 1</label>
<caption><p><bold>The phyletic relationships of select primates and the sister taxon Dermoptera (the Sunda colugo, <italic>Galeopterus variegatus</italic>
).</bold>
The distinction between nocturnal (black zone) and diurnal (white zone) activity patterns is strongly associated with variation in retinal ganglion cell (RGC) counts (mm<sup>-2</sup>
), cone densities (mm<sup>-2</sup>
), and rod densities (mm<sup>-2</sup>
) in the <italic>area centralis</italic>
or <italic>fovea centralis</italic>
(data sources: <xref rid="B148" ref-type="bibr">Webb and Kaas, 1976</xref>
; <xref rid="B105" ref-type="bibr">Perry and Cowey, 1985</xref>
; <xref rid="B14" ref-type="bibr">Curcio et al., 1990</xref>
; <xref rid="B150" ref-type="bibr">Wikler and Rakic, 1990</xref>
; <xref rid="B127" ref-type="bibr">Silveira et al., 1993</xref>
; <xref rid="B100" ref-type="bibr">Ogden, 1994</xref>
; <xref rid="B151" ref-type="bibr">Wilder et al., 1996</xref>
; <xref rid="B48" ref-type="bibr">Hendrickson et al., 2000</xref>
; <xref rid="B21" ref-type="bibr">Dkhissi-Benyahya et al., 2001</xref>
; <xref rid="B103" ref-type="bibr">Peichl et al., 2001</xref>
; <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
; <xref rid="B136" ref-type="bibr">Tetreault et al., 2004</xref>
; <xref rid="B25" ref-type="bibr">Finlay et al., 2008</xref>
; <xref rid="B91" ref-type="bibr">Moritz et al., 2013</xref>
). Ancestral character states based in part on these values suggest a diurnal ancestry for <italic>Tarsius</italic>
and <italic>Aotus</italic>
; and, by extension, stem anthropoids (e.g., <xref rid="B117" ref-type="bibr">Ross, 2000</xref>
; <xref rid="B152" ref-type="bibr">Williams et al., 2010</xref>
). Accordingly, the foveae of <italic>Tarsius</italic>
and <italic>Aotus</italic>
are most likely vestigial traits. A problem with this view is evident in the densities of RGCs, cones, and rods. Relative to <italic>Tarsius</italic>
, the retina of <italic>Aotus</italic>
has advanced further toward a nocturnal phenotype despite a substantially younger vintage of 5–20 million years (see text).</p>
</caption>
<graphic xlink:href="fnint-08-00061-g001"></graphic>
</fig>
<sec><title>NOCTURNAL HAPLORHINES AND THE CONCEPT OF FOVEAL DEGENERACY</title>
<p>The retina of <italic>Aotus</italic>
has been studied since the 1870s (<xref rid="B107" ref-type="bibr">Polyak, 1957</xref>
; <xref rid="B100" ref-type="bibr">Ogden, 1994</xref>
; <xref rid="B129" ref-type="bibr">Silveira et al., 2001</xref>
), and a rod-dominated fovea is either absent (<xref rid="B159" ref-type="bibr">Woollard, 1927</xref>
; <xref rid="B20" ref-type="bibr">Detwiler, 1941</xref>
; <xref rid="B58" ref-type="bibr">Jones, 1965</xref>
; <xref rid="B24" ref-type="bibr">Ferraz de Oliveira and Ripps, 1968</xref>
), shallow and rudimentary (<xref rid="B71" ref-type="bibr">Kolmer, 1930</xref>
; <xref rid="B107" ref-type="bibr">Polyak, 1957</xref>
; <xref rid="B153" ref-type="bibr">Wolin and Massopust, 1967</xref>
; <xref rid="B127" ref-type="bibr">Silveira et al., 1993</xref>
), or present in 10% of individuals (<xref rid="B100" ref-type="bibr">Ogden, 1994</xref>
). <xref rid="B145" ref-type="bibr">Walls (1953)</xref>
viewed this variation as evidence of functional degeneracy. <xref rid="B148" ref-type="bibr">Webb and Kaas (1976)</xref>
averred, reporting a shallow fovea and displaced ganglion cells; they also suggested that a degenerate fovea is functionally comparable to an <italic>area centralis</italic>
, the retinal specialization of strepsirrhine primates (<xref rid="B115" ref-type="bibr">Rohen and Castenholz, 1967</xref>
; <xref rid="B154" ref-type="bibr">Wolin and Massopust, 1970</xref>
). Indeed, the densities of rods and cones in the foveae of <italic>Aotus azarae</italic>
and <italic>Aotus trivirgatus</italic>
resemble those in the <italic>area centralis</italic>
of <italic>Galago garnetti</italic>
, a lorisid primate (<xref rid="B150" ref-type="bibr">Wikler and Rakic, 1990</xref>
; <xref rid="B25" ref-type="bibr">Finlay et al., 2008</xref>
). The notion of foveal degeneracy in <italic>Aotus</italic>
, together with the absence of a <italic>tapetum lucidum</italic>
, is widely interpreted as evidence of a diurnal ancestry, as illustrated in <bold>Figure <xref ref-type="fig" rid="F1">1</xref>
</bold>
.</p>
<p>A shift to nocturnality could have occurred ∼20 Ma on the basis of phylogenetic affinities with <italic>Tremacebus</italic>
, which was plausibly nocturnal (<xref rid="B62" ref-type="bibr">Kay and Kirk, 2000</xref>
; <xref rid="B61" ref-type="bibr">Kay et al., 2004</xref>
; <xref rid="B119" ref-type="bibr">Ross et al., 2007</xref>
). Recent molecular phylogenies are compatible with this view, suggesting that the stem ancestor of <italic>Aotus</italic>
diverged from diurnal Cebidae ∼19.3 Ma (<xref rid="B104" ref-type="bibr">Perelman et al., 2011</xref>
), whereas crown <italic>Aotus</italic>
diversified ∼5.5 to 4.6 Ma (<xref rid="B89" ref-type="bibr">Menezes et al., 2010</xref>
; <xref rid="B123" ref-type="bibr">Ruiz-García et al., 2011</xref>
). Thus, the antiquity of nocturnality in the aotine lineage is between ∼5 and 20 million years. This span was evidently sufficient to favor degenerate foveae among other distinctive attributes, such as relatively enlarged eyes and orbits (<xref rid="B65" ref-type="bibr">Kirk, 2006</xref>
; <xref rid="B120" ref-type="bibr">Ross and Kirk, 2007</xref>
), disabling mutations of the short-wavelength-sensitive-1 (<italic>SWS1</italic>
) opsin gene (<xref rid="B56" ref-type="bibr">Jacobs et al., 1996</xref>
; <xref rid="B74" ref-type="bibr">Levenson et al., 2007</xref>
), rod photoreceptors with an inverted nuclear architecture (<xref rid="B57" ref-type="bibr">Joffe et al., 2014</xref>
), and large numbers of P retinal ganglion cells (<xref rid="B130" ref-type="bibr">Silveira et al., 1994</xref>
) with high rod convergence to both M and P cells (<xref rid="B160" ref-type="bibr">Yamada et al., 2001</xref>
). These traits differentiate <italic>Aotus</italic>
from all other monkeys and are strongly convergent with nocturnal mammals; hence, the aotine visual system is almost certainly a nocturnal derivation.</p>
<p>The functional anatomy of the tarsier retina is more challenging to interpret (<xref rid="B118" ref-type="bibr">Ross, 2004</xref>
). Early studies of spectral tarsiers (<italic>Tarsius spectrum</italic>
) failed to detect a fovea (<xref rid="B157" ref-type="bibr">Woollard, 1925</xref>
, <xref rid="B158" ref-type="bibr">1926</xref>
), whereas recent investigations report the uniform presence of rod-dominant, concave-sided (concaviclivate) foveae (<xref rid="B48" ref-type="bibr">Hendrickson et al., 2000</xref>
; Hendrickson cited in <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
). Similar foveae are present in Philippine tarsiers (<italic>Tarsius syrichta</italic>
; <xref rid="B107" ref-type="bibr">Polyak, 1957</xref>
; <xref rid="B153" ref-type="bibr">Wolin and Massopust, 1967</xref>
), but variable among Bornean tarsiers (<italic>Tarsius bancanus</italic>
; <xref rid="B8" ref-type="bibr">Castenholz, 1965</xref>
; <xref rid="B7" ref-type="bibr">Castenholz, 1984</xref>
). On the surface, these findings point to an <italic>Aotus</italic>
-like state of foveal degeneracy; however, the fovea of <italic>Tarsius</italic>
is deeper, less variable, and associated with much higher cone densities (50,000–85,000 mm<sup>-2</sup>
; <xref rid="B48" ref-type="bibr">Hendrickson et al., 2000</xref>
; Hendrickson cited in <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
) than that of <italic>Aotus</italic>
(5000–17,000 mm<sup>-2</sup>
; <xref rid="B150" ref-type="bibr">Wikler and Rakic, 1990</xref>
; <xref rid="B25" ref-type="bibr">Finlay et al., 2008</xref>
). Another difference concerns the <italic>SWS1</italic>
opsin gene; it is intact among tarsiers (<xref rid="B134" ref-type="bibr">Tan et al., 2005</xref>
) and a low rate of non-synonymous to synonymous substitutions is consistent with strict purifying selection (<xref rid="B59" ref-type="bibr">Kawamura and Kubotera, 2004</xref>
).</p>
<p>Modest foveal degeneracy and a functional <italic>SWS1</italic>
opsin gene have been interpreted as evidence of a recent transition to nocturnality (<xref rid="B134" ref-type="bibr">Tan et al., 2005</xref>
). Indeed, two recent findings support this premise. First, the rods of <italic>T. spectrum</italic>
have a nuclear architecture that is strongly associated with diurnality (<xref rid="B57" ref-type="bibr">Joffe et al., 2014</xref>
). Second, molecular evidence suggests that the ancestral crown tarsier possessed a cone opsin polymorphism that enabled trichromatic vision (<xref rid="B86" ref-type="bibr">Melin et al., 2013</xref>
). The antiquity of this character trait is uncertain, with crown divergence dates ranging from ∼18.6 Ma (<xref rid="B132" ref-type="bibr">Springer et al., 2012</xref>
) to ∼13 to 9 Ma (<xref rid="B86" ref-type="bibr">Melin et al., 2013</xref>
), but multiple independent losses of trichromatic vision appear to have occurred in the past 5 million years (<xref rid="B86" ref-type="bibr">Melin et al., 2013</xref>
). Such findings suggest a relatively recent history of diurnality; and yet, the fossil record is a testament to committed nocturnality. The hyperenlarged orbits of <italic>Tarsius eoceanus</italic>
(Middle Eocene), <italic>Tarsius sirindhornae</italic>
(Middle Miocene), and living tarsiers are most parsimoniously interpreted as evidence of continuous nocturnality for at least 45 million years (<xref rid="B121" ref-type="bibr">Rossie et al., 2006</xref>
; <xref rid="B10" ref-type="bibr">Chaimanee et al., 2011</xref>
). These discrepant lines of evidence are difficult to reconcile.</p>
<p>The foveae and rod architecture of tarsiers could be adaptations to non-photopic conditions; and, hence not necessarily vestiges of a diurnal ancestor. <xref rid="B86" ref-type="bibr">Melin et al. (2013)</xref>
hypothesized that the hyperenlarged eyes and foveate color vision of ancestral crown tarsiers (and potentially stem tarsiers and anthropoid primates), evolved to support visual predation under dim (mesopic) light levels such as twilight or bright moonlight. These light conditions are predicted to support cone-mediated color vision (<xref rid="B87" ref-type="bibr">Melin et al., 2012</xref>
) and favor enlarged eyes for greater visual sensitivity in the absence of a tapetum lucidum (<xref rid="B5" ref-type="bibr">Cartmill, 1980</xref>
). This attempt at consilience is laudable but difficult to test.</p>
</sec>
<sec><title>COMPARATIVE FUNCTIONAL ECOLOGY OF THE NOCTURNAL FOVEA</title>
<p>It is challenging for humans to observe how tarsiers discern vertebrate and invertebrate prey; they appear to integrate and alternate between auditory and visual cues depending on ambient conditions and prey type (<xref rid="B95" ref-type="bibr">Niemitz, 1979</xref>
, <xref rid="B96" ref-type="bibr">1984</xref>
; <xref rid="B79" ref-type="bibr">MacKinnon and MacKinnon, 1980</xref>
; <xref rid="B34" ref-type="bibr">Gursky, 2000</xref>
, <xref rid="B35" ref-type="bibr">2002</xref>
; <xref rid="B15" ref-type="bibr">Dagosto et al., 2003</xref>
). Such a specialized niche is assumed to have few competitors, a concept that reinforces the perception of tarsiers as “living fossils” in a state of ecological stasis (<xref rid="B55" ref-type="bibr">Jablonski, 2003</xref>
). However, observations of the Sunda scops owl (<italic>Otus lempiji</italic>
), a tarsier-sized faunivore (90–140 <italic>g</italic>
), suggest a comparable niche (<xref rid="B72" ref-type="bibr">König and Weick, 2008</xref>
; <bold>Figure <xref ref-type="fig" rid="F2">2</xref>
</bold>
). Potential niche convergence has attracted attention due to the many homoplasies that unite tarsiers and scops owls, such as (i) hyperenlarged eyes that protrude from the orbit (<bold>Figures <xref ref-type="fig" rid="F3">3A,B</xref>
</bold>
); (ii) orbit-induced displacement of the olfactory tract, which itself is unusually long; (iii) a loss of ocular mobility that corresponds with increased cervical mobility (<bold>Figures <xref ref-type="fig" rid="F3">3C,D</xref>
</bold>
); (iv) acute directional hearing; (v) enlarged semicircular canals; and, (vi) derived feeding morphologies for perforating prey (<xref rid="B97" ref-type="bibr">Niemitz, 1985</xref>
, <xref rid="B98" ref-type="bibr">2010</xref>
; <xref rid="B88" ref-type="bibr">Menegaz and Kirk, 2009</xref>
). <xref rid="B97" ref-type="bibr">Niemitz (1985)</xref>
interpreted this suite of character traits as an adaptation to sit-and-wait ambush predation at low light levels. Evidence of dietary overlap would support this hypothesis and potentially shed light on yet another shared homoplasy, the fovea.</p>
<fig id="F2" position="float"><label>FIGURE 2</label>
<caption><p><bold>(A)</bold>
Orthopteran insects such as katydids are a common prey item in the diet of tarsiers (photograph of <italic>Tarsius lariang</italic>
by Stefan Merker, reproduced with permission). <bold>(B)</bold>
Orthopteran insects are also consumed by scops owls (photograph of <italic>Otus scops</italic>
by Clément and Julien Pappalardo, reproduced with permission). <bold>(C)</bold>
Tarsiers also consume geckos (photograph of <italic>T. spectrum</italic>
by David J. Slater, reproduced with permission). <bold>(D)</bold>
In Singapore, geckos are reported to be the most common food item in the diet of <italic>O. lempiji</italic>
(<xref rid="B77" ref-type="bibr">Lok et al., 2009</xref>
; photograph by Tiah Khee Lee, reproduced with permission).</p>
</caption>
<graphic xlink:href="fnint-08-00061-g002"></graphic>
</fig>
<fig id="F3" position="float"><label>FIGURE 3</label>
<caption><p><bold>(A)</bold>
The skull and eye of <italic>Tarsius bancanus</italic>
(modified from <xref rid="B7" ref-type="bibr">Castenholz, 1984</xref>
; <xref rid="B118" ref-type="bibr">Ross, 2004</xref>
) together with the fovea of <italic>T. spectrum</italic>
(modified from <xref rid="B48" ref-type="bibr">Hendrickson et al., 2000</xref>
). <bold>(B)</bold>
The skull, eye, and fovea of a composite strigiform (modified from <xref rid="B27" ref-type="bibr">Fite, 1973</xref>
; <xref rid="B88" ref-type="bibr">Menegaz and Kirk, 2009</xref>
). Because ocular mobility is constrained by the hyperenlarged eyes of tarsiers and scops owls, an extraordinary degree of cervical rotation is necessary to enable rapid prey localization and fixation. <bold>(C)</bold>
The increased cervical mobility of tarsiers allows them to rotate their head 180° in azimuth (<xref rid="B7" ref-type="bibr">Castenholz, 1984</xref>
; photograph of <italic>T. bancanus</italic>
by Nick Garbutt, reproduced with permission). <bold>(D)</bold>
Owls can rotate their head 270° in azimuth (<xref rid="B43" ref-type="bibr">Harmening and Wagner, 2011</xref>
; photograph of <italic>O. lempiji</italic>
by Paul B. Jones, reproduced with permission). Extreme head rotation is thought to enhance the sit-and-wait ambush mode of predation common to tarsiers and scops owls (<xref rid="B97" ref-type="bibr">Niemitz, 1985</xref>
).</p>
</caption>
<graphic xlink:href="fnint-08-00061-g003"></graphic>
</fig>
<p>Within Strigiformes, there is mixed evidence for foveae in the family Tytonidae (barn and bay owls). For example, a fovea can be present (<xref rid="B99" ref-type="bibr">Oehme, 1961</xref>
) or absent in barn owls (<italic>Tyto alba</italic>
; <xref rid="B146" ref-type="bibr">Wathey and Pettigrew, 1989</xref>
; <xref rid="B75" ref-type="bibr">Lisney et al., 2012</xref>
). In the family Strigidae (“typical” owls) rod-dominant, concaviclivate foveae are uniformly present (<xref rid="B155" ref-type="bibr">Wood, 1917</xref>
; <xref rid="B114" ref-type="bibr">Rochon-Duvigneaud, 1943</xref>
; <xref rid="B99" ref-type="bibr">Oehme, 1961</xref>
; <xref rid="B27" ref-type="bibr">Fite, 1973</xref>
; <xref rid="B28" ref-type="bibr">Fite and Rosenfield-Wessels, 1975</xref>
; <xref rid="B75" ref-type="bibr">Lisney et al., 2012</xref>
); and at least one species, the tawny owl (<italic>Strix aluco</italic>
), has a fovea with three cone classes (<xref rid="B82" ref-type="bibr">Martin and Gordon, 1974</xref>
; <xref rid="B4" ref-type="bibr">Bowmaker and Martin, 1978</xref>
). <italic>Strix aluco</italic>
demonstrates that foveate trichromatic vision can exist in tandem with a nocturnal eye and orbit (<xref rid="B41" ref-type="bibr">Hall and Ross, 2007</xref>
; <xref rid="B119" ref-type="bibr">Ross et al., 2007</xref>
; <xref rid="B40" ref-type="bibr">Hall, 2008</xref>
). Furthermore, at least two strigid species, the scops owl (<italic>Otus scops</italic>
) and little owl (<italic>Athene noctua</italic>
), can make chromatic discriminations at low light levels (<xref rid="B102" ref-type="bibr">Parejo et al., 2010</xref>
; <xref rid="B2" ref-type="bibr">Avilés and Parejo, 2013</xref>
). The retention of foveate color vision in strigids has been associated with foraging under mesopic conditions (<xref rid="B2" ref-type="bibr">Avilés and Parejo, 2013</xref>
), a view that reinforces the possibility of tarsiers behaving similarly.</p>
</sec>
<sec><title>STUDY DESIGN</title>
<p>A controlled experimental approach is preferable for testing foveal function; however, the mortality rate of captive tarsiers is unacceptably high (<xref rid="B26" ref-type="bibr">Fitch-Snyder, 2003</xref>
). Accordingly, we conceived a study premised on abductive reasoning: if tarsiers and scops owls are observed to have similar diets, then the fovea that unites them can be interpreted as a functional dietary trait. A weakness of abduction is that a conclusion can remain false following verification of the initial premise. Even still, such reasoning has practical value when information is limited. Here we focus on data available in the tissues of wild-caught animals. The stable isotope ratios in these tissues can be used to quantify prior behavioral observations of dietary convergence.</p>
<p>Stable isotope ratios are a practical tool for quantifying the diets of difficult-to-observe animals. The isotopic niche of a species is often based on ratios of carbon (<sup>13</sup>
C:<sup>12</sup>
C or <italic>δ</italic>
<sup>13</sup>
C) and nitrogen (<sup>15</sup>
N:<sup>14</sup>
N or <italic>δ</italic>
<sup>15</sup>
N) isotopes in a two-dimensional “<italic>δ</italic>
-space” (<xref rid="B94" ref-type="bibr">Newsome et al., 2007</xref>
). For example, the <italic>δ</italic>
<sup>13</sup>
C values of animals in a savanna-woodland can vary because most plants fix atmospheric CO<sub>2</sub>
via two photosynthetic pathways. The <italic>δ</italic>
<sup>13</sup>
C values of C<sub>3</sub>
and C<sub>4</sub>
plants are ca. -28‰ (range -21 to -35‰) and -14‰ (range -12 to -16‰), respectively (<xref rid="B101" ref-type="bibr">O’Leary, 1988</xref>
), a difference that persists in the isotopic composition of primary and secondary consumers. In a tropical forest, the isotopic baseline of plants varies to lesser extent, although factors such as canopy cover, relative humidity, light availability, tree height, and soil moisture can drive variation in <italic>δ</italic>
<sup>13</sup>
C values (<xref rid="B45" ref-type="bibr">Heaton, 1999</xref>
; <xref rid="B1" ref-type="bibr">Amundson et al., 2003</xref>
; <xref rid="B81" ref-type="bibr">Marshall et al., 2007</xref>
). For example, C<sub>3</sub>
plants under sunny conditions are <sup>13</sup>
C-enriched (high <italic>δ</italic>
<sup>13</sup>
C values: -21 to -27‰), whereas those in the understory are <sup>13</sup>
C-depleted (low <italic>δ</italic>
<sup>13</sup>
C values: <-31‰) due to the recycling of CO<sub>2</sub>
(<xref rid="B70" ref-type="bibr">Kohn, 2010</xref>
). This “canopy effect,” or gradient of decreasing <italic>δ</italic>
<sup>13</sup>
C values from the canopy to the understory (<xref rid="B141" ref-type="bibr">Vogel, 1978</xref>
; <xref rid="B85" ref-type="bibr">Medina and Minchin, 1980</xref>
; <xref rid="B139" ref-type="bibr">van der Merwe and Medina, 1991</xref>
), is reflected in the isotopic composition of consumers (<xref rid="B126" ref-type="bibr">Schoeninger, 2010</xref>
), although with a small offset due to enrichment effects. In general, the <italic>δ</italic>
<sup>13</sup>
C values of herbivores are 2–3‰ more positive than their diet, whereas herbivore-to-faunivore trophic enrichment can range from 0.2 to 4‰ (on the basis of keratin: <xref rid="B18" ref-type="bibr">DeNiro and Epstein, 1978</xref>
; <xref rid="B122" ref-type="bibr">Roth and Hobson, 2000</xref>
; <xref rid="B131" ref-type="bibr">Sponheimer et al., 2003</xref>
; <xref rid="B30" ref-type="bibr">Fox-Dobbs et al., 2007</xref>
; <xref rid="B52" ref-type="bibr">Hyodo et al., 2010</xref>
; <xref rid="B13" ref-type="bibr">Crowley et al., 2011</xref>
). Thus, <italic>δ</italic>
<sup>13</sup>
C values can discriminate trophic position as well as the vertical stratum of foraging within a habitat (<xref rid="B142" ref-type="bibr">Voigt, 2010</xref>
; <xref rid="B112" ref-type="bibr">Rex et al., 2011</xref>
), including the dipterocarp forests of southeast Asia (<xref rid="B60" ref-type="bibr">Kawanishi et al., 2012</xref>
).</p>
<p>Variation in <italic>δ</italic>
<sup>15</sup>
N is a dietary indicator due to the systematic retention of <sup>15</sup>
N at each trophic level (<xref rid="B33" ref-type="bibr">Gannes et al., 1997</xref>
). Thus increasing <italic>δ</italic>
<sup>15</sup>
N values are associated with trophic “steps.” A step can range from 1.3 to 5‰, but 3‰ is typical (<xref rid="B19" ref-type="bibr">DeNiro and Epstein, 1981</xref>
; <xref rid="B125" ref-type="bibr">Schoeninger, 1985</xref>
; <xref rid="B122" ref-type="bibr">Roth and Hobson, 2000</xref>
; <xref rid="B108" ref-type="bibr">Post, 2002</xref>
; <xref rid="B30" ref-type="bibr">Fox-Dobbs et al., 2007</xref>
). In the dipterocarp forests of Borneo, the <italic>δ</italic>
<sup>15</sup>
N values of predators are ca. 2.6‰ higher than those of omnivores, 3‰ higher than those of herbivores, and 3.7‰ higher than those of detritivores (<xref rid="B52" ref-type="bibr">Hyodo et al., 2010</xref>
). These results suggest that variation in <italic>δ</italic>
<sup>15</sup>
N can discriminate trophic levels in the habitats used by tarsiers and scops owls, although the isotopic baseline of tree leaves in northern Borneo can vary slightly as function of soil N availability (<xref rid="B66" ref-type="bibr">Kitayama and Iwamoto, 2001</xref>
) and disturbance history (<xref rid="B156" ref-type="bibr">Woodcock et al., 2012</xref>
). This variation is manifested in the tissues of secondary consumers. For example, <xref rid="B92" ref-type="bibr">Nakagawa et al. (2007)</xref>
showed that the hair of omnivorous rodents in open, degraded forests were <sup>15</sup>
N-enriched (higher <italic>δ</italic>
<sup>15</sup>
N values) relative to conspecifics in primary forest, whereas <italic>δ</italic>
<sup>15</sup>
N values did not differ between treeshrews and squirrels inhabiting different forest types.</p>
<p>Thus <italic>Tarsius</italic>
and <italic>Otus</italic>
are predicted to have similar isotopic niches, or overlapping <italic>δ</italic>
<sup>13</sup>
C and <italic>δ</italic>
<sup>15</sup>
N values. Affirmation of this prediction would be consistent with functional interpretations of the many anatomical homoplasies shared between these two taxa, including the retinal fovea.</p>
</sec>
</sec>
<sec sec-type="materials|methods" id="s1"><title>MATERIALS AND METHODS</title>
<sec><title>SAMPLE ACQUISITION AND PREPARATION</title>
<p>We sampled the contour feathers of Sunda scops owls (<italic>Otus lempiji</italic>
, formerly <italic>O. bakkamoena lempiji</italic>
; <italic>n</italic>
= 8) and Philippine scops owls (<italic>Otus megalotis</italic>
, formerly <italic>O. bakkamoena megalotis</italic>
; <italic>n</italic>
= 11; taxonomy follows <xref rid="B72" ref-type="bibr">König and Weick, 2008</xref>
). We also sampled hair from the shoulders of Bornean tarsiers (<italic>T. bancanus</italic>
; <italic>n</italic>
= 6) and Philippine tarsiers (<italic>T. syrichta</italic>
; <italic>n</italic>
= 28). The specimens, all wild-caught adults, were chosen on the basis of maximum overlapping provenience (<bold>Figure <xref ref-type="fig" rid="F4">4</xref>
</bold>
). The majority of specimens are accessioned in the American Museum of Natural History, the Field Museum of Natural History, the Kinabalu National Park Museum, and the Universiti Malaysia Sabah Museum (Appendix <xref ref-type="supplementary-material" rid="SM1">1</xref>
). We supplemented these samples with hair from a wild population of <italic>T. syrichta</italic>
in the vicinity of Motorpool, Tubod, Surigao del Norte, Mindanao, Philippines (09°38′N; 125°33′E). These tarsiers (<italic>n</italic>
= 12) were hand-caught and anaesthetized as part of a larger study of their sensory ecology (<xref rid="B110" ref-type="bibr">Ramsier et al., 2012</xref>
). For measurements of <italic>δ</italic>
<sup>13</sup>
C and <italic>δ</italic>
<sup>15</sup>
N in keratin, 2–3 feathers or 10–15 strands of hair were cleaned of debris using ethanol, sonicated in ultrapure water, and washed 1–2 times in petroleum ether. The samples were then cut into small fragments (<italic>∼</italic>
1 mm) and weighed (500 ± 15 μg) into precombusted tin capsules.</p>
<fig id="F4" position="float"><label>FIGURE 4</label>
<caption><p><bold>The distribution of sampling localities in Borneo (<italic>Otus lempiji</italic>
and <italic>Tarsius bancanus</italic>
) and in Philippines (<italic>O. megalotis</italic>
and <italic>T. syrichta</italic>
)</bold>
.</p>
</caption>
<graphic xlink:href="fnint-08-00061-g004"></graphic>
</fig>
</sec>
<sec><title>ANALYTICAL PROCEDURES</title>
<p>Isotope ratios are presented as <italic>δ</italic>
values, where <italic>δ</italic>
= 1000 ((R sample/R standard) – 1) and R = <sup>13</sup>
C/<sup>12</sup>
C or R = <sup>15</sup>
N/<sup>14</sup>
N; reference standards are Vienna Pee Dee Belemnite (VPDB) for carbon and atmospheric N<sub>2</sub>
for nitrogen. Units are expressed as parts per thousand (‰). The dried samples were combusted and analyzed with a Thermo-Chemical Elemental Analyzer (TCEA) interfaced with a Delta Plus XP isotope ratio mass spectrometer (IRMS, Thermo Finnigan, Bremen, Germany) located in the Stable Isotope Laboratory, University of California, Santa Cruz. The analytical precision (±1 SD) for <italic>δ</italic>
<sup>13</sup>
C and <italic>δ</italic>
<sup>15</sup>
N was 0.3‰ and 0.05‰, respectively, based on four International Atomic Energy Agency (IAEA) acetanilide replicates.</p>
<p>A potential confounding factor is associated with the steady global decrease in the <sup>13</sup>
C content of atmospheric CO<sub>2</sub>
due primarily to fossil fuel burning during the past 150 years (the Suess effect; <xref rid="B53" ref-type="bibr">Indermühle et al., 1999</xref>
). The total magnitude of this change is ca. 1.5‰ (<xref rid="B78" ref-type="bibr">Long et al., 2005</xref>
), but the effects within 5–10 year intervals are relatively small (ca. 0.1‰). To account for this variation in atmospheric CO<sub>2</sub>
, which in turn is reflected in the tissues of plants and consumers, we applied conservative time-dependent correction factors of –0.004‰ or –0.02‰ per year to samples from specimens collected between 1860 and 1965 and between 1965 and 2010, respectively (<xref rid="B32" ref-type="bibr">Francey et al., 1999</xref>
; <xref rid="B63" ref-type="bibr">Keeling et al., 2005</xref>
).</p>
<p>Another confounding factor stems from geographic and temporal variation in soil N availability, both natural (<xref rid="B51" ref-type="bibr">Högberg, 1997</xref>
; <xref rid="B66" ref-type="bibr">Kitayama and Iwamoto, 2001</xref>
) and anthropogenic (<xref rid="B64" ref-type="bibr">Kendall et al., 2007</xref>
; <xref rid="B49" ref-type="bibr">Hietz et al., 2011</xref>
), and the potential for spatial autocorrelation of <italic>δ</italic>
<sup>15</sup>
N values. To explore this first possibility, we averaged all samples from a given site and calculated Moran’s index of spatial autocorrelation. We detected no evidence of spatial autocorrelation among sample sites (<italic>Otus</italic>
sites: <italic>n</italic>
= 13, Moran’s <italic>I</italic>
= 0.23, <italic>z</italic>
= 1.60, <italic>p</italic>
= 0.11; <italic>Tarsius</italic>
sites: <italic>n</italic>
= 10, Moran’s <italic>I</italic>
= –0.19, <italic>z</italic>
= –0.45, <italic>p</italic>
= 0.65), although the semivariograms are potentially uninformative due to the small number of samples spread over a relatively large spatial scale. Each <italic>δ</italic>
<sup>15</sup>
N value is therefore assumed to have statistical independence for assessing diet.</p>
</sec>
<sec><title>STATISTICAL ANALYSES</title>
<p>We performed all statistical tests in R version 2.14.1 (<xref rid="B111" ref-type="bibr">R Development Core Team, 2011</xref>
). As some of our data violated the assumptions of parametric statistical analysis, we used non-parametric Wilcoxon rank sum (two-sample) and Kruskal–Wallis <italic>χ</italic>
<sup>2</sup>
(multiple comparison) tests to assess whether the carbon and nitrogen isotope compositions differentiate sympatric taxa of <italic>Tarsius</italic>
and <italic>Otus</italic>
. For all normally distributed data, comparisons of significance were investigated using Welch’s Two Sample <italic>t</italic>
-tests. The significance for all tests was set at <italic>α</italic>
= 0.05.</p>
</sec>
</sec>
<sec><title>RESULTS</title>
<p>Appendix 1 summarizes the raw and time-dependent corrections to <italic>δ</italic>
<sup>13</sup>
C. The mean ± SD of all time-corrected samples was –23.76 ± 1.6‰ (range: –27.80‰ to –17.41‰). Within Borneo, the time-corrected <italic>δ</italic>
<sup>13</sup>
C values of <italic>O. lempiji</italic>
(mean: -22.87 ± 1.7‰) were ca. 1.95‰ greater than those of <italic>T. bancanus</italic>
(mean: –24.82 ± 0.2‰), but the difference did not reach statistical significance (Wilcoxon <italic>W</italic>
= 38; <italic>p</italic>
= 0.08; <bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
). Similarly, in the Philippines, the time-corrected <italic>δ</italic>
<sup>13</sup>
C values of <italic>O. megalotis</italic>
(mean: –23.33 ± 2.5‰) were ca. 0.62‰ greater than those of <italic>T. syrichta</italic>
(mean: –23.95 ± 1.1‰), but the difference did not reach significance (Wilcoxon <italic>W</italic>
= 196; <italic>p</italic>
= 0.198; <bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
). Intrageneric comparisons revealed differences between the two species of <italic>Tarsius</italic>
(<italic>W</italic>
= 36, <italic>p</italic>
= 0.03) but not the two species of <italic>Otus</italic>
(<italic>t</italic>
<sub>16.82</sub>
= 0.46, <italic>p</italic>
= 0.648).</p>
<fig id="F5" position="float"><label>FIGURE 5</label>
<caption><p><bold>Bivariate plot of δ<sup><bold>13</bold>
</sup>
C and δ<sup><bold>15</bold>
</sup>
N values (mean ± 1 SD) in the keratin of Bornean tarsiers (<italic>Tarsius bancanus</italic>
), Philippine tarsiers (<italic>T. syrichta</italic>
), Sunda scops owls (<italic>Otus lempiji</italic>
), and Philippine scops owls (<italic>O. megalotis</italic>
).</bold>
To illustrate an approximate full dietary trophic step, the keratin-derived δ<sup>13</sup>
C and δ<sup>15</sup>
N values of a frugivore (Müller’s Bornean gibbon, <italic>Hylobates muelleri</italic>
) and a predator of vertebrates (leopard cat, <italic>Felis bengalensis</italic>
) from Sabah, northern Borneo are also plotted.</p>
</caption>
<graphic xlink:href="fnint-08-00061-g005"></graphic>
</fig>
<p>Appendix 1 summarizes the raw values <italic>δ</italic>
<sup>15</sup>
N. The mean ± SD of all samples was 5.79 ± 2.2‰ (range: 2.39–11.37‰). Within Borneo, the <italic>δ</italic>
<sup>15</sup>
N values of <italic>O. lempiji</italic>
(mean: 7.45 ± 1.7‰) were ca. 1.65‰ greater than those of <italic>T. bancanus</italic>
(mean: 5.80 ± 1.8‰), but the difference did not reach statistical significance (Wilcoxon <italic>W</italic>
= 36; <italic>p</italic>
= 0.142; <bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
). The effect size of this analysis is sufficient to rule out a Type II error (Cohen’s <italic>d</italic>
= 0.95). Within the Philippines, the <italic>δ</italic>
<sup>15</sup>
N values of <italic>O. megalotis</italic>
(mean: 7.04 ± 2.3‰) were ca. 2.22‰ greater than those of <italic>T. syrichta</italic>
(mean: 4.82 ± 1.9‰), indicating significant <sup>15</sup>
N-enrichment (Wilcoxon <italic>W</italic>
= 239, <italic>p</italic>
= 0.008; <bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
); however, the samples from <italic>T. syrichta</italic>
collected in 2010 exhibited systematically low <italic>δ</italic>
<sup>15</sup>
N values, perhaps due to recent anthropogenic changes to the landscape (e.g., <xref rid="B31" ref-type="bibr">Fox-Dobbs et al., 2012</xref>
). When we calculated the mean of these samples, log-transformed all <italic>δ</italic>
<sup>15</sup>
N values, and controlled for specimen year in a general model, there was no statistical difference between <italic>O. megalotis</italic>
and <italic>T. syrichta</italic>
(<italic>t</italic>
= –0.28, <italic>p</italic>
= 0.781). Intrageneric comparisons revealed no differences between the two species of <italic>Tarsius</italic>
(<italic>t</italic>
<sub>7.43</sub>
= 1.19, <italic>p</italic>
= 0.271) or the two species of <italic>Otus</italic>
(<italic>t</italic>
<sub>17</sub>
= 0.44, <italic>p</italic>
= 0.664).</p>
<p><bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
also illustrates the larger food web by including the <italic>δ</italic>
<sup>13</sup>
C and <italic>δ</italic>
<sup>15</sup>
N values of a primary consumer, the frugivorous Müller’s gibbon (<italic>Hylobates muelleri</italic>
; <italic>n</italic>
= 1), and a predator of vertebrates, the leopard cat (<italic>Felis bengalensis</italic>
; <italic>n</italic>
= 1). The isotopic differences (Δ) between these taxa (Δ<sup>13</sup>
C: 2.36‰; Δ<sup>15</sup>
N: 4.93‰) approximate a full trophic step, albeit a rather large one. <xref rid="B52" ref-type="bibr">Hyodo et al. (2010)</xref>
reported a similar Δ<sup>13</sup>
C value of 2.4‰, but a smaller Δ<sup>15</sup>
N value of 3.0‰ between herbivores and predators in Lambir National Park, Sarawak, Borneo. In any case, the magnitude of the isotopic difference (Δ) between <italic>O. megalotis</italic>
and <italic>T. syrichta</italic>
(Δ<sup>15</sup>
N = 2.22) is much less than that between <italic>Felis</italic>
and <italic>Hylobates</italic>
(Δ<sup>15</sup>
N = 4.93‰).</p>
</sec>
<sec><title>DISCUSSION</title>
<disp-quote><p>In many respects, tarsiers are not owls, but almost (<xref rid="B98" ref-type="bibr">Niemitz, 2010</xref>
, p. 953)</p>
</disp-quote>
<p>Our results demonstrate isotopic overlap: the <italic>δ</italic>
<sup>13</sup>
C values of <italic>Otus</italic>
and <italic>Tarsius</italic>
were indistinguishable, whereas the <italic>δ</italic>
<sup>15</sup>
N values of <italic>Otus</italic>
were often higher than those of <italic>Tarsius</italic>
. The low and comparable <italic>δ</italic>
<sup>13</sup>
C values indicate use of the same stratum (the forest floor), a foraging pattern that agrees well with behavioral observations. The differences in <italic>δ</italic>
<sup>15</sup>
N values – a pattern that was a trend in Borneo and temporally variable in the Philippines – are potentially instructive because they indicate a subtle degree of prey partitioning. Yet the magnitude of the isotopic difference (Δ) between <italic>O. megalotis</italic>
and <italic>T. syrichta</italic>
(Δ<sup>15</sup>
N = 2.22) is much less than that between <italic>Felis</italic>
and <italic>Hylobates</italic>
(Δ<sup>15</sup>
N = 4.93‰; <bold>Figure <xref ref-type="fig" rid="F5">5</xref>
</bold>
), suggesting limited partitioning of invertebrate and vertebrate prey (discussed below). However, <xref rid="B52" ref-type="bibr">Hyodo et al. (2010)</xref>
reported a herbivore–predator Δ<sup>15</sup>
N of 3.0‰ on the basis of a much larger data set from Sarawak. Taken together, our isotopic results demonstrate that <italic>Otus</italic>
and <italic>Tarsius</italic>
occupy similar dietary niches, although a trend toward <sup>15</sup>
N-enrichment among scops owls, particularly <italic>O. megalotis</italic>
, suggests some prey partitioning.</p>
<p>For instance, it is plausible that tarsiers consume relatively few insect-eating squamates. Such an interpretation conflicts with early accounts, which stressed the central importance of geckos to the diets of <italic>T. bancanus</italic>
and <italic>T. syrichta</italic>
(captivity: <xref rid="B149" ref-type="bibr">Wharton, 1950</xref>
; <xref rid="B44" ref-type="bibr">Harrison, 1963</xref>
; wild: <xref rid="B29" ref-type="bibr">Fogden, 1974</xref>
). However, our findings corroborate those of <xref rid="B17" ref-type="bibr">Davis (1962)</xref>
, who found a preponderance of large orthopteran insects in the stomachs of seven wild-caught Bornean tarsiers and <xref rid="B96" ref-type="bibr">Niemitz (1984)</xref>
, who observed <italic>T. bancanus</italic>
under seminatural conditions in Sarawak. Niemitz reported that vertebrates (squamates, birds) represented <11% of 133 successful predation events. In Sulawesi, tarsiers seldom consume vertebrates (<xref rid="B79" ref-type="bibr">MacKinnon and MacKinnon, 1980</xref>
; <xref rid="B138" ref-type="bibr">Tremble et al., 1993</xref>
; <xref rid="B38" ref-type="bibr">Gursky, 2007a</xref>
), but geckos can represent 4.2% of the diet (by mass) of tarsiers in captivity (<xref rid="B16" ref-type="bibr">Dahang et al., 2008</xref>
).</p>
<p>A discrepancy between the foraging behaviors of wild and captive tarsiers might indicate a release from predation or competition. Perhaps in the absence of scops owls, tarsiers can shift their foraging preference to vertebrate prey. Still, recent studies of captive tarsiers in the United States report that <italic>T. bancanus</italic>
ignores anoles (<italic>Anolis carolinensis</italic>
) in favor of crickets, whereas <italic>T. syrichta</italic>
exhibits the reverse pattern (<xref rid="B42" ref-type="bibr">Haring and Wright, 1989</xref>
; <xref rid="B113" ref-type="bibr">Roberts and Kohn, 1993</xref>
). These mixed responses to a North American anole are difficult to interpret, and they illustrate the challenge of studying the foraging adaptations of a small nocturnal visual predator. In general, our isotopic results agree well with field observations, although these are sparse – invertebrates appear to represent the great majority prey objects consumed by tarsiers.</p>
<p>Another possible explanation for the <sup>15</sup>
N-enrichment of <italic>Otus</italic>
stems from the consumption of dung-eating (scatophagous) coleopterans:</p>
<disp-quote><p>“Food is usually sought near the ground... in villages (<italic>Otus lempiji</italic>
) habitually hunts nocturnal insects attracted to cow dung or poultry droppings around houses. Some stomachs examined were crammed with cockroaches (Blattidae) and a particular type of black dung beetle (Scarabidae). The Sumatran (Minangklabau) name for this owl is <italic>kuas cirit ayam</italic>
, which means ‘fowl’s-excrement owl”’ (<xref rid="B72" ref-type="bibr">König and Weick, 2008</xref>
, p. 274).</p>
</disp-quote>
<p>The sobriquet “excrement owl” is potentially instructive. Animal waste is often enriched in <sup>15</sup>
N due to the volatilization of <sup>15</sup>
N-depleted ammonia, and subsequent oxidation of the residual waste material can result in nitrate with high <italic>δ</italic>
<sup>15</sup>
N values (<xref rid="B64" ref-type="bibr">Kendall et al., 2007</xref>
). For example, cow dung is typically <sup>15</sup>
N-enriched (∼2.3‰) relative to diet (<xref rid="B133" ref-type="bibr">Steele and Daniel, 1978</xref>
). This effect could be amplified in the dipterocarp forests of Borneo, where extended periods of protein limitation can result in <sup>15</sup>
N-enriched urine among large mammals, e.g., orangutans (<xref rid="B140" ref-type="bibr">Vogel et al., 2012</xref>
). Thus, dung-eating (scatophagous) insects should be enriched in <sup>15</sup>
N relative to their plant-eating (phytophagous) counterparts, and the relative <sup>15</sup>
N-enrichment of <italic>Otus</italic>
could reflect a greater proportion of scatophagous coleopterans or nocturnal squamates, or both, in the diet. To discriminate the relative contributions of these putative food sources, it would be useful to collect food samples and perform a Bayesian multiple source isotopic mixing model (e.g., <xref rid="B161" ref-type="bibr">Yeakel et al., 2009</xref>
; <xref rid="B124" ref-type="bibr">Rutz et al., 2010</xref>
).</p>
<p>A final possibility – that scops owls occasionally consume tarsiers – seems unlikely. <xref rid="B96" ref-type="bibr">Niemitz (1984)</xref>
reported that <italic>Otus</italic>
failed to induce an obvious response among Bornean tarsiers, and <xref rid="B79" ref-type="bibr">MacKinnon and MacKinnon (1980</xref>
, p. 375) observed that spectral tarsiers “paid no attention to an owl <italic>Ninox</italic>
sp. sitting and calling a few yards above them.” However, <xref rid="B36" ref-type="bibr">Gursky (2003a)</xref>
reported that predator-naive infants (aged one and two months) distanced themselves from the calls of raptors (including the Sulawesi owl, <italic>Tyto rosenbergii</italic>
and the speckled boobook, <italic>Ninox punctulata</italic>
) and minimized movement in response to models of an ochre-bellied boobook (<italic>Ninox ochracea</italic>
) and spotted kestrel (<italic>Falco moluccensis</italic>
). Among adult tarsiers, the kestrel elicited the twin antipredator behaviors of mobbing and alarm calling during 47% of encounters, indicating that adults recognized it as a threat (<xref rid="B39" ref-type="bibr">Gursky, 2007b</xref>
). The fact that no similar behaviors were directed toward owls suggests that <italic>Otus</italic>
is an unlikely predator of <italic>Tarsius</italic>
.</p>
<sec><title>THE TARSIER FOVEA – FUNCTIONLESS VESTIGE OR NOCTURNAL ADAPTATION?</title>
<p>In a report to the Zoological Society of London, the preeminent anatomist Grafton Elliot Smith described his charge to Wilfrid Le Gros Clark, who, in 1920, was appointed Principal Medical Officer to the Government of Sarawak. “I impressed upon him,” wrote <xref rid="B22" ref-type="bibr">Elliot Smith (1921</xref>
, p. 184), “the importance of studying the retina of living or freshly-killed examples of <italic>Tarsius</italic>
... a surviving member of the Eocene family from which our own simian ancestors were derived.” This advice from a mentor to a student rings as true today as it did a century ago; and, although the retina of <italic>Tarsius</italic>
has since been examined in detail (<xref rid="B157" ref-type="bibr">Woollard, 1925</xref>
, <xref rid="B158" ref-type="bibr">1926</xref>
, <xref rid="B159" ref-type="bibr">1927</xref>
; <xref rid="B107" ref-type="bibr">Polyak, 1957</xref>
; <xref rid="B8" ref-type="bibr">Castenholz, 1965</xref>
; <xref rid="B153" ref-type="bibr">Wolin and Massopust, 1967</xref>
; <xref rid="B7" ref-type="bibr">Castenholz, 1984</xref>
; <xref rid="B48" ref-type="bibr">Hendrickson et al., 2000</xref>
; <xref rid="B136" ref-type="bibr">Tetreault et al., 2004</xref>
), it continues to yield surprises (<xref rid="B57" ref-type="bibr">Joffe et al., 2014</xref>
). And still, an open question remains: is the fovea a functionless vestige or a nocturnal adaptation? (<xref rid="B118" ref-type="bibr">Ross, 2004</xref>
).</p>
<p>Our isotopic results are germane to this question insofar as they provide empirical evidence of food competition between scops owls and tarsiers. Although this finding entails some resource partitioning, it fails to refute the functional interpretation of the many homoplasies that unite <italic>Otus</italic>
and <italic>Tarsius</italic>
(<xref rid="B97" ref-type="bibr">Niemitz, 1985</xref>
), including, very likely, the fovea. This evidence of anatomical and dietary convergence raises the possibility of parallel learning mechanisms. Perhaps a central function of the fovea is to calibrate the auditory system during development, as shown in barn owls (<italic>T. alba</italic>
). In other words, foveate vision may guide sound localization by verifying the accuracy of auditory orientation to a sound source (<xref rid="B69" ref-type="bibr">Knudsen and Knudsen, 1985</xref>
; <xref rid="B68" ref-type="bibr">Knudsen, 2002</xref>
). This concept of vision-mediated or “supervised” learning (<xref rid="B67" ref-type="bibr">Knudsen, 1994</xref>
) is compelling – Philippine tarsiers have extraordinary hearing abilities (<xref rid="B110" ref-type="bibr">Ramsier et al., 2012</xref>
) and foveate vision could be a contributing factor to the evolution and development of their auditory localization pathway (<xref rid="B46" ref-type="bibr">Heffner and Heffner, 1992</xref>
). Behavioral observations of tarsiers have long stressed the dual importance of auditory localization and visual fixation during prey detection and acquisition (<xref rid="B95" ref-type="bibr">Niemitz, 1979</xref>
).</p>
<p>If instructed learning in the auditory localization pathway is at least partly dependent on foveate vision, then a unified representation of visual and auditory sensory stimuli was potentially a central factor in the enduring success of <italic>Tarsius</italic>
. The initial calibration or subsequent recalibration of this system might require cone activation under non-scotopic conditions. This hypothesis could account for both the high number of cones in the fovea of <italic>Tarisus</italic>
(relative to <italic>Aotus</italic>
; <bold>Figure <xref ref-type="fig" rid="F1">1</xref>
</bold>
) and the phenomenon of lunar philia (increased activity under moonlight) among spectral tarsiers (<xref rid="B37" ref-type="bibr">Gursky, 2003b</xref>
). It might also explain why the photoreceptors of tarsiers have attributes normally associated with mesopic or photopic light levels (<xref rid="B86" ref-type="bibr">Melin et al., 2013</xref>
; <xref rid="B57" ref-type="bibr">Joffe et al., 2014</xref>
). Taken together, the natural history of tarsiers represents a model system for studying how experience might shape the functional organization of the brain and the ensuing functional ecology of an animal.</p>
</sec>
</sec>
<sec><title>Conflict of Interest Statement</title>
<p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p>
</sec>
</body>
<back><ack><p>We thank A. F. Amir, D. Andreasen, J. W. Chipman, B. E. Crowley, A. J. Cunningham, L. D. Dagsaan, T. K. Lee, A. Lok, A. U. Luczon, C. Sendall, and C. V. Williams for practical support in the field and lab. We thank the Mamanwa for their hospitality and knowledge of tarsiers and the National Commission on Indigenous People for facilitating Prior Informed Consent (PIC) for the collection of samples. In Malaysia, permission to sample and export tissues from collections was granted by the Sabah Biodiversity Council [permit nos. JKM/MBS.1000-2/2(26) and JKM/MBS.1000-2/3(30)]. In the Philippines, permission to harvest and export tissues was granted by the Protected Areas and Wildlife Bureau, Department of Environment and Natural Resources (permit no. R13-2010-003). Samples from CITES Appendix I-listed species were imported under certificate no. 09US684773/9. We thank L. R. Heaney, W. T. Stanley, and D. Willard at the Field Museum of Natural History and D. P. Lunde and P. Sweet at the American Museum of Natural History for permission to collect tissue samples. Our protocols (nos. 11-06-07AT and 11-09-02AT) were approved by the Dartmouth Institutional Animal Care and Use Committee. Finally, we thank the David and Lucile Packard Foundation for funding (Fellowship in Science and Engineering no. 2007-31754).</p>
</ack>
<sec sec-type="supplementary-material"><title>SUPPLEMENTARY MATERIAL</title>
<p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="http://www.frontiersin.org/journal/10.3389/fnint.2014.00061/abstract">http://www.frontiersin.org/journal/10.3389/fnint.2014.00061/abstract"></ext-link>
</p>
<supplementary-material content-type="local-data" id="SM1"><media xlink:href="Data_Sheet_1.DOCX"><caption><p>Click here for additional data file.</p>
</caption>
</media>
</supplementary-material>
</sec>
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