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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Decaying toxic wood as sodium supplement for herbivorous mammals in
Gabon</title><author><name sortKey="Iwata, Yuji" sort="Iwata, Yuji" uniqKey="Iwata Y" first="Yuji" last="Iwata">Yuji Iwata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nakashima, Yoshihiro" sort="Nakashima, Yoshihiro" uniqKey="Nakashima Y" first="Yoshihiro" last="Nakashima">Yoshihiro Nakashima</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Tsuchida, Sayaka" sort="Tsuchida, Sayaka" uniqKey="Tsuchida S" first="Sayaka" last="Tsuchida">Sayaka Tsuchida</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nguema, Pierre Philippe Mbehang" sort="Nguema, Pierre Philippe Mbehang" uniqKey="Nguema P" first="Pierre Philippe Mbehang" last="Nguema">Pierre Philippe Mbehang Nguema</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Ando, Chieko" sort="Ando, Chieko" uniqKey="Ando C" first="Chieko" last="Ando">Chieko Ando</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Ushida, Kazunari" sort="Ushida, Kazunari" uniqKey="Ushida K" first="Kazunari" last="Ushida">Kazunari Ushida</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Yamagiwa, Juichi" sort="Yamagiwa, Juichi" uniqKey="Yamagiwa J" first="Juichi" last="Yamagiwa">Juichi Yamagiwa</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">25994487</idno><idno type="pmc">4638291</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4638291</idno><idno type="RBID">PMC:4638291</idno><idno type="doi">10.1292/jvms.15-0111</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000019</idno><idno type="wicri:explorRef" wicri:stream="Pmc" wicri:step="Corpus" wicri:corpus="PMC">000019</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Decaying toxic wood as sodium supplement for herbivorous mammals in
Gabon</title><author><name sortKey="Iwata, Yuji" sort="Iwata, Yuji" uniqKey="Iwata Y" first="Yuji" last="Iwata">Yuji Iwata</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nakashima, Yoshihiro" sort="Nakashima, Yoshihiro" uniqKey="Nakashima Y" first="Yoshihiro" last="Nakashima">Yoshihiro Nakashima</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Tsuchida, Sayaka" sort="Tsuchida, Sayaka" uniqKey="Tsuchida S" first="Sayaka" last="Tsuchida">Sayaka Tsuchida</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Nguema, Pierre Philippe Mbehang" sort="Nguema, Pierre Philippe Mbehang" uniqKey="Nguema P" first="Pierre Philippe Mbehang" last="Nguema">Pierre Philippe Mbehang Nguema</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Ando, Chieko" sort="Ando, Chieko" uniqKey="Ando C" first="Chieko" last="Ando">Chieko Ando</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Ushida, Kazunari" sort="Ushida, Kazunari" uniqKey="Ushida K" first="Kazunari" last="Ushida">Kazunari Ushida</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author><author><name sortKey="Yamagiwa, Juichi" sort="Yamagiwa, Juichi" uniqKey="Yamagiwa J" first="Juichi" last="Yamagiwa">Juichi Yamagiwa</name><affiliation><nlm:aff>NONE</nlm:aff></affiliation></author></analytic><series><title level="j">The Journal of Veterinary Medical Science</title><idno type="ISSN">0916-7250</idno><idno type="eISSN">1347-7439</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>African rainforest harbors herbivores at high density. However, because plants and soils
typically lack in some essential minerals, rainforest is not always a suitable habitat for
herbivores. How they fulfill the mineral requirements is therefore an important question
to animal ecology and conservation. Although large marshes, called ‘bais’, are often
mentioned as efficient mineral-resource, little information on other sodium resources has
still been available. Our laboratory works and field surveys found that a peculiar item,
decaying wood stumps of <italic>Anthostema aubryanum</italic>, played as a major sodium
resource for herbivores in Moukalaba-Doudou National Park, Gabon. When <italic>A.
aubryanum</italic> is alive, the sodium content of its bark is low and its latex is
toxic. Sodium is accumulated in decaying stumps (mean=1,343 mg/kg dry matter). Eight
herbivores visited stumps to ingest the dead wood. Fecal sample analysis revealed that
western lowland gorillas, a species most-frequently using the stumps, consumed large
amount of the dead wood as regular food. Our findings suggest that decaying <italic>A.
aubryanum</italic> is critical sodium-resources and is a key species for herbivores in
our study area. Importance of the <italic>A. aubryanum</italic> may be particularly large
there, because it is a limited sodium-rich material that is available year round. Our
study site is known as the site where the densities of several herbivores are among the
highest at Central Africa. The relatively high herbivores density in our study site may
partly depend on decaying <italic>A. aubryanum</italic> as sodium resources.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Ando, C" uniqKey="Ando C">C. Ando</name></author><author><name sortKey="Iwata, Y" uniqKey="Iwata Y">Y. Iwata</name></author><author><name sortKey="Yamagiwa, J" uniqKey="Yamagiwa J">J. Yamagiwa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Baier, W" uniqKey="Baier W">W. Baier</name></author><author><name sortKey="Kosmus, W" uniqKey="Kosmus W">W. Kosmus</name></author><author><name sortKey="Heinrich, G" uniqKey="Heinrich G">G. Heinrich</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Botkin, D B" uniqKey="Botkin D">D. B. Botkin</name></author><author><name sortKey="Jordan, P A" uniqKey="Jordan P">P. A. Jordan</name></author><author><name sortKey="Dominski, A S" uniqKey="Dominski A">A. S. 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Reynolds</name></author><author><name sortKey="Lloyd, A W" uniqKey="Lloyd A">A. W. Lloyd</name></author><author><name sortKey="Babweteera, F" uniqKey="Babweteera F">F. Babweteera</name></author><author><name sortKey="English, C J" uniqKey="English C">C. J. English</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Robbins, C T" uniqKey="Robbins C">C. T. Robbins</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rogers, M E" uniqKey="Rogers M">M. E. Rogers</name></author><author><name sortKey="Abernethy, K" uniqKey="Abernethy K">K. Abernethy</name></author><author><name sortKey="Bermejo, M" uniqKey="Bermejo M">M. Bermejo</name></author><author><name sortKey="Cipolletta, C" uniqKey="Cipolletta C">C. Cipolletta</name></author><author><name sortKey="Doran, D" uniqKey="Doran D">D. Doran</name></author><author><name sortKey="Mcfarland, K" uniqKey="Mcfarland K">K. McFarland</name></author><author><name sortKey="Nishihara, T" uniqKey="Nishihara T">T. Nishihara</name></author><author><name sortKey="Remis, M" uniqKey="Remis M">M. Remis</name></author><author><name sortKey="Tutin, C E" uniqKey="Tutin C">C. E. Tutin</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Rothman, J M" uniqKey="Rothman J">J. M. Rothman</name></author><author><name sortKey="Van Soest, P J" uniqKey="Van Soest P">P. J. Van Soest</name></author><author><name sortKey="Pell, A N" uniqKey="Pell A">A. N. Pell</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Sienne, J M" uniqKey="Sienne J">J. M. Sienne</name></author><author><name sortKey="Buchwald, R" uniqKey="Buchwald R">R. Buchwald</name></author><author><name sortKey="Wittemyer, G" uniqKey="Wittemyer G">G. Wittemyer</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Takenoshita, Y" uniqKey="Takenoshita Y">Y. Takenoshita</name></author><author><name sortKey="Yamagiwa, J" uniqKey="Yamagiwa J">J. Yamagiwa</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Tsukahara, T" uniqKey="Tsukahara T">T. Tsukahara</name></author><author><name sortKey="Bukawa, W" uniqKey="Bukawa W">W. Bukawa</name></author><author><name sortKey="Kan, T" uniqKey="Kan T">T. Kan</name></author><author><name sortKey="Ushida, K" uniqKey="Ushida K">K. Ushida</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Ushida, K" uniqKey="Ushida K">K. Ushida</name></author><author><name sortKey="Fujita, S" uniqKey="Fujita S">S. Fujita</name></author><author><name sortKey="Ohashi, G" uniqKey="Ohashi G">G. Ohashi</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Van Vliet, N" uniqKey="Van Vliet N">N. van Vliet</name></author><author><name sortKey="Nasi, R" uniqKey="Nasi R">R. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">J Vet Med Sci</journal-id><journal-id journal-id-type="iso-abbrev">J. Vet. Med. Sci</journal-id><journal-id journal-id-type="publisher-id">JVMS</journal-id><journal-title-group><journal-title>The Journal of Veterinary Medical Science</journal-title></journal-title-group><issn pub-type="ppub">0916-7250</issn><issn pub-type="epub">1347-7439</issn><publisher><publisher-name>The Japanese Society of Veterinary Science</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">25994487</article-id><article-id pub-id-type="pmc">4638291</article-id><article-id pub-id-type="publisher-id">15-0111</article-id><article-id pub-id-type="doi">10.1292/jvms.15-0111</article-id><article-categories><subj-group subj-group-type="heading"><subject>Wildlife Science</subject><subj-group><subject>Full Paper</subject></subj-group></subj-group></article-categories><title-group><article-title>Decaying toxic wood as sodium supplement for herbivorous mammals in
Gabon</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>IWATA</surname><given-names>Yuji</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref ref-type="author-notes" rid="con"><sup>#</sup></xref></contrib><contrib contrib-type="author"><name><surname>NAKASHIMA</surname><given-names>Yoshihiro</given-names></name><xref ref-type="aff" rid="aff3"><sup>3</sup></xref><xref ref-type="author-notes" rid="con"><sup>#</sup></xref></contrib><contrib contrib-type="author"><name><surname>TSUCHIDA</surname><given-names>Sayaka</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref></contrib><contrib contrib-type="author"><name><surname>NGUEMA</surname><given-names>Pierre Philippe Mbehang</given-names></name><xref ref-type="aff" rid="aff4"><sup>4</sup></xref></contrib><contrib contrib-type="author"><name><surname>ANDO</surname><given-names>Chieko</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><contrib contrib-type="author"><name><surname>USHIDA</surname><given-names>Kazunari</given-names></name><xref ref-type="aff" rid="aff2"><sup>2</sup></xref><xref rid="cor1" ref-type="corresp"><sup>*</sup></xref></contrib><contrib contrib-type="author"><name><surname>YAMAGIWA</surname><given-names>Juichi</given-names></name><xref ref-type="aff" rid="aff1"><sup>1</sup></xref></contrib><aff id="aff1"><label>1)</label>Kyoto University, Graduate School of Science, Kitashirakawa, Kyoto 606–8502, Japan</aff><aff id="aff2"><label>2)</label>Kyoto Prefectural University, Graduate School of Life and Environmental Sciences, Shimogamo, Kyoto 606–8522, Japan</aff><aff id="aff3"><label>3)</label>Nihon University, College of Bioresource Science, Kameino, Fujisawa, Kanagawa 252–0880, Japan</aff><aff id="aff4"><label>4)</label>Institute des Recherches en Ecologie Tropicale, BP 13354, Libreville, Gabon</aff></contrib-group><author-notes><corresp id="cor1"><label>*</label>Correspondence to: Ushida, K., Graduate School of Life
and Environmental Sciences, Kyoto Prefectural University, Shimogamo Sakyo-ku, Kyoto
606–8522 Japan. e-mail: <email xlink:href="k_ushida@kpu.ac.jp">k_ushida@kpu.ac.jp</email></corresp><fn id="con"><label>#</label><p>These authors contributed equally to this work.</p></fn></author-notes><pub-date pub-type="epub"><day>21</day><month>5</month><year>2015</year></pub-date><pub-date pub-type="ppub"><month>10</month><year>2015</year></pub-date><volume>77</volume><issue>10</issue><fpage>1247</fpage><lpage>1252</lpage><history><date date-type="received"><day>27</day><month>2</month><year>2015</year></date><date date-type="accepted"><day>08</day><month>5</month><year>2015</year></date></history><permissions><copyright-statement>©2015 The Japanese Society of Veterinary Science</copyright-statement><copyright-year>2015</copyright-year><license license-type="open-access" xlink:href="http://creativecommons.org/licenses/by-nc-nd/3.0/"><license-p>This is an open-access article distributed under the terms of the Creative
Commons Attribution Non-Commercial No Derivatives (by-nc-nd) License. </license-p></license></permissions><abstract><p>African rainforest harbors herbivores at high density. However, because plants and soils
typically lack in some essential minerals, rainforest is not always a suitable habitat for
herbivores. How they fulfill the mineral requirements is therefore an important question
to animal ecology and conservation. Although large marshes, called ‘bais’, are often
mentioned as efficient mineral-resource, little information on other sodium resources has
still been available. Our laboratory works and field surveys found that a peculiar item,
decaying wood stumps of <italic>Anthostema aubryanum</italic>, played as a major sodium
resource for herbivores in Moukalaba-Doudou National Park, Gabon. When <italic>A.
aubryanum</italic> is alive, the sodium content of its bark is low and its latex is
toxic. Sodium is accumulated in decaying stumps (mean=1,343 mg/kg dry matter). Eight
herbivores visited stumps to ingest the dead wood. Fecal sample analysis revealed that
western lowland gorillas, a species most-frequently using the stumps, consumed large
amount of the dead wood as regular food. Our findings suggest that decaying <italic>A.
aubryanum</italic> is critical sodium-resources and is a key species for herbivores in
our study area. Importance of the <italic>A. aubryanum</italic> may be particularly large
there, because it is a limited sodium-rich material that is available year round. Our
study site is known as the site where the densities of several herbivores are among the
highest at Central Africa. The relatively high herbivores density in our study site may
partly depend on decaying <italic>A. aubryanum</italic> as sodium resources.</p></abstract><kwd-group><kwd><italic>Anthostema aubryanum</italic></kwd><kwd>decaying wood</kwd><kwd>herbivores</kwd><kwd>sodium resource</kwd><kwd>toxic plant</kwd></kwd-group></article-meta></front><body><p>In African rainforest, large herbivores (including frugivores/folivores), such as elephants
and gorillas, occur sympatrically and constitute a major component of the mammalian biomass
[<xref rid="r27" ref-type="bibr">27</xref>]. Sodium availability directly influences the
distribution of herbivores and regulates their population size [<xref rid="r3" ref-type="bibr">3</xref>, <xref rid="r26" ref-type="bibr">26</xref>], but rainforest is typically
sodium-deficient habitats because tropical plants and soils are generally lower in nutrients
than temperate plants are [<xref rid="r8" ref-type="bibr">8</xref>, <xref rid="r25" ref-type="bibr">25</xref>], and heavy rainfall readily leached minerals from the ecosystems [<xref rid="r16" ref-type="bibr">16</xref>]. How these large herbivores fulfill the sodium
requirements is therefore an interesting and important question to animal ecology and
conservation, but has not still been well-elucidated one. Our study site seemingly lacks large
sodium-resources, although sodium-rich (mean=823 mg/kg dry matter, range=339–1,293 mg/kg, see
<xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>)
<italic>Sacoglottis gabonensis</italic> fruits are seasonally available. Previous studies
have reported that herbivores in Central Africa have specific mineral resources [<xref rid="r6" ref-type="bibr">6</xref>]. Especially, large marshland, called “bai”, covered with
year-round herbaceous vegetation supplies important mineral resources, such as mineral rich
aquatic herbs, soil and water, for herbivores [<xref rid="r4" ref-type="bibr">4</xref>, <xref rid="r7" ref-type="bibr">7</xref>, <xref rid="r10" ref-type="bibr">10</xref>, <xref rid="r19" ref-type="bibr">19</xref>]. For example, western gorillas in Ndoki forest in
Republic of the Congo consumed the root of <italic>Hydrochari</italic>s sp., which showed
higher sodium concentration (1,080 mg/kg) than other herbs year-round in “bais” [<xref rid="r13" ref-type="bibr">13</xref>].</p><p>Here, we report that decaying wood stumps of a particular toxic plant are critical sodium
resources for herbivores in Moukalaba-Doudou National Park (PNMD), Gabon, where lacks “bai”.
This toxic plant, once dead, supports among the highest densities of herbivores, such as
duikers [<xref rid="r12" ref-type="bibr">12</xref>], gorillas [<xref rid="r20" ref-type="bibr">20</xref>] and elephants [<xref rid="r24" ref-type="bibr">24</xref>], in Central
Africa.</p><p>The forest of PNMD is characterized by the abundance of <italic>Anthostema aubryanum</italic>(Euphorbiaceae) [<xref rid="r23" ref-type="bibr">23</xref>]. Logging business was conducted
between the 1960s and the 1980s in PNMD, but <italic>A. aubryanun</italic> was worthless as
lumber. Then, <italic>A. aubryanum</italic> trees were not logged and still abundantly exist
in PNMD. One single decayed stump of <italic>A. aubryanum</italic> could only last for several
weeks after the first bit by herbivores. It is confirmed by direct observation that herbivores
in PNMD feed on large amount of decaying wood of <italic>A. aubryanum</italic> (local name:
Nzanzala). Especially, western lowland gorillas (<italic>Gorilla gorilla gorilla</italic>)
showed high attachment to decaying <italic>A. aubryanum</italic> (see <xref ref-type="fig" rid="fig_001">Fig. 1</xref><fig orientation="portrait" fig-type="figure" id="fig_001" position="float"><label>Fig. 1.</label><caption><p>Gorillas rushed to feed on decaying <italic>Anthostema aubryanum</italic> stump.</p></caption><graphic xlink:href="jvms-77-1247-g001"></graphic></fig> and <xref rid="video_003" ref-type="supplementary-material">Supplementary Video</xref>).
Interestingly enough, <italic>A. aubryanum</italic> was only species that herbivores consumed
decaying wood, although <italic>A. aubryanum</italic> latex is toxic and caustic which deter
animals from feeding on live wood; in fact, local people sometime use small amount of this
latex as purgative [<xref rid="r14" ref-type="bibr">14</xref>].</p><p>Some researchers reported that decaying wood of particular tree plays an important roll for
great apes as sodium resource [<xref rid="r15" ref-type="bibr">15</xref>, <xref rid="r18" ref-type="bibr">18</xref>]. Therefore, we hypothesized that decaying stumps of
<italic>A. aubryanum</italic> might be critical sodium resources not only for great apes but
also for other herbivorous animals in our study site. To test this hypothesis, we conducted
the following three researches. First, we performed chemical analyses on wood bark and latex
of <italic>A. aubryanum</italic>, and confirm that <italic>A. aubryanum</italic> has high
sodium concentrations. Second, we revealed which species ingest decaying <italic>A.
aubryanum</italic> by using camera traps in the field. Third, we analyzed the frequency of
appearance of <italic>A. aubryanum</italic> debris in fecal samples of gorillas to confirm
that decaying <italic>A. aubryanum</italic> wood was regular food material for gorillas in
PNMD.</p><sec sec-type="materials|methods" id="s1"><title>MATERIALS AND METHODS</title><p><italic>Study site</italic>: Our field study site, PNMD, covers an area of 5,028
km<sup>2</sup>, and its southwestern boundary abuts the Atlantic Ocean. The study area
covers about 120 km<sup>2</sup> in the southeastern part of the park at an altitude of
50–800m. This area typically experiences 2 seasons: the rainy season from October to May and
the dry season from June to September. Mean annual rainfall was 1,777 mm (range: 1,583–2,163
mm). The mean monthly minimum and maximum temperatures varied from 21.3 to 24.1°C and 29.3
to 33.7°C, respectively. Seasonal fluctuations in fruit production are distinct in our study
site. Fruit production is peaked between December and February and is the bottom between
April and July (see <xref rid="pdf_002" ref-type="supplementary-material">Supplementary Fig.
2</xref>).</p><p><italic>Collection of wood bark, latex samples and fruits</italic>: Live wood bark with
cambium (ca. 3~5 × 5~10 × 1 cm) was collected from <italic>A. aubryanum</italic> (local
name: nzanzala), <italic>Ficus</italic> sp. (divevengui rouge), <italic>Ficus</italic> sp.
(divevengui blanc), <italic>Ficus</italic> sp. (ditsanda), <italic>Milicia excelsa</italic>(kambala), <italic>Mitragyna ciliata</italic> (tobu), <italic>Myrianthus arboreus</italic>(mububa) and <italic>S. gabonensis</italic> (musuga) in February 2012. Decaying bark with
cambium and a surface portion of sapwood (ca. 3~5 × 5~10 × 1 cm thick) were collected from
<italic>Anthonotha macrophylla</italic> (ibora; dingandu), <italic>Berlinia
macrophylla</italic> (ibora), <italic>Diospyros manii</italic> (kingu nzibu),
<italic>Klainedoxa gabonensis</italic> (mugoma), <italic>M. excelsa</italic> (kambala),
<italic>M. cecropioides</italic> (dibala), <italic>Nauclea diderrichii</italic> (ivala
kumu) and <italic>S. gabonensis</italic> (musuga) found adjacent to decaying stumps of
<italic>A. aubryanum</italic> in August 2012.</p><p>Samples of bark with a surface portion of sapwood (ca. 3~5 × 5~10 × 2 cm) were taken from
every decaying <italic>A. aubryanum</italic> stump found along streams within the study site
in November 2011 and August 2012. These samples were placed in plastic bags with silica gel
for transportation. Samples of latex were collected from two live <italic>A.
aubryanum</italic> trees in February 2012. The liquid latex (10 m<italic>l</italic>) was
collected and preserved in 30 m<italic>l</italic> of ethanol to avoid decomposition.</p><p>Following fruits were subjected to mineral analysis; <italic>S. gabonensis, M.
cecropioides, Cissus dinklagei</italic> and <italic>Aframomum giganteum.</italic> Three
fruits species, except for <italic>S. gabonensis</italic>, were top 3 fruits which were
contained at the highest frequency in fecal samples collected from August 2004 to July 2008
(<italic>M. cecropioides</italic>=64.2% of fecal samples, <italic>C.
dinklagei</italic>=32.3% and <italic>A. giganteum</italic>=26.4%). We collected intact
fruits from the ground in July and August 2012. The fruits were seemingly freshly fallen
from the tree, and some of them were actually showed signs of feeding of gorillas. Fruits
samples were air dried at 60°C and stored in desiccation until analysis.</p><p><italic>Chemical analyses on wood bark, latex and fruits</italic>: Portions of samples were
dried to a constant weight at 80°C and digested with nitric acid and perchloric acid
following standard methods [<xref rid="r21" ref-type="bibr">21</xref>]. Metals (Mg, Ca, P,
Fe, Cu, Zn, Mo, Cd, Ni, Co, Mn, Cr and Al) were analyzed in duplicate with inductively
coupled Argon plasma spectrograph, and two macro-elements (Na and K) were analyzed in
duplicate by atomic absorption as indicated elsewhere [<xref rid="r22" ref-type="bibr">22</xref>]. The latex in ethanol was well mixed, and subsamples were dried to a constant
weight at 80°C before digestion. Comparison was made by Student <italic>t</italic>-test or
Welch <italic>t</italic>-test for metal concentrations between decaying <italic>A.
aubryanum</italic> and live <italic>A. aubryanum</italic> or decaying wood of other
varieties.</p><p><italic>Camera Trap</italic>: To determine the animal species that utilize the decaying
stumps of <italic>A. aubryanum</italic>, and to estimate the frequency of visits and stay
duration at decaying <italic>A. aubryanum</italic> stumps by these species, camera traps
with an infrared triggering system (Bushnell Trophy Cam 2010, Bushnell Outdoor Product,
Overland Park, KS, U.S.A.) were set up in front of five <italic>A. aubryanum</italic> stumps
from November to December 2012. The focal stumps were selected from the decaying woods
sampled for chemical analysis and located at least 50 m from each other. Cameras were
installed on the nearest tree trunk at a height of ca. 70 cm. We used ‘Video mode’ of
cameras, which takes 60-sec videos after the sensors are triggered and thus allows
behavioral observations of animals. Medium and large-sized, ground-dwelling mammals (>1
kg) were targeted, and the species that consumed the decaying stumps from the videos were
determined.</p><p>A video was considered to indicate a single visit by a given species, if the picture was
obtained <30 min after the previous picture of that species. Mean stay duration (hr) of
each animal species was estimated from the start time of the first video to the end time of
the last video. Because it was impossible to recognize individuals for group-living animals
(e.g. gorillas), visitation frequencies and stay durations as a group were estimated.
Capture rates (the number of videos/100 camera-trapping days) and mean visit duration for
each species at <italic>A. aubryanum</italic> sites were compared with the results from ten
camera traps (as controls) located at 200-m intervals along the 2 km-transect. All the
control sites were positioned within 1-km from the nearest <italic>A. aubryanum</italic>sites. For camera-trapping data, Wilcoxon rank sum tests were used to compare the capture
rates and mean stay duration of each animal species at <italic>A. aubryanum.</italic></p><p><italic>Fecal sample analysis for Western Lowland Gorillas</italic>: We analyzed the fecal
sample data to test the frequency of decaying <italic>A. aubryanum</italic> consumption by
the western lowland gorilla group. Fresh fecal samples (<48 hr) were collected from the
nest sites of a habituated gorilla group. Fecal samples were washed in water through 1-mm
mesh sieves and dried in sunlight within 1 day of collection. Remnants were visually
identified together with live observatory information. Remnants of decaying wood and live
wood in the feces were easily distinguishable. Decaying wood in fecal samples was much
smaller than that of living wood, because bark of living wood split lengthwise but dead wood
became fragments.</p><p>Fecal sample data at the same study period with camera trap are not available. However, we
monitored diet of gorillas for 4 years (Aug, 2004–July 2008) and ascertained that is a
highly consistent pattern of diet, with fruit consumption by gorillas peaking three months
between December to February (See <xref rid="pdf_002" ref-type="supplementary-material">supplementary Fig. 1</xref>). We used the fecal samples collected between November and
December, as the same months with camera trap, in 2004 to 2007 for the analysis.</p></sec><sec sec-type="results" id="s2"><title>RESULTS</title><p><italic>Mineral concentration in decaying A. aubryanum and other foods</italic>:
Concentrations of macro- and oligo-elements are summarized in <xref ref-type="fig" rid="fig_002">Fig. 2</xref><fig orientation="portrait" fig-type="figure" id="fig_002" position="float"><label>Fig. 2.</label><caption><p>Comparison of the mineral content (mg/kg dry matter) in live and decayed wood of
<italic>Anthostema aubryanum</italic> and other plants. The numbers in parentheses
are the number of samples. **<italic>P</italic><0.01,
*<italic>P</italic><0.05.</p></caption><graphic xlink:href="jvms-77-1247-g002"></graphic></fig> and <xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table
1</xref> in which the bark from decaying <italic>A. aubryanum</italic> was compared with
bark from live <italic>A. aubryanum</italic>, other live wood species or other decaying wood
species adjacent to decaying <italic>A. aubryanum</italic> stumps. Macro-elements, sodium,
potassium, magnesium, calcium and phosphorus were detected in all samples. Among the
oligo-elements, zinc, copper and iron were detected in all samples, while other minerals,
such as molybdenum, cadmium, nickel, cobalt, manganese, chromium and aluminum, were detected
only in trace amounts (see <xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>). Therefore, these trace elements were omitted from
consideration.</p><p>Mean sodium concentrations recorded in decaying <italic>A. aubryanum</italic> stumps were
1,343 mg/kg dry matter (range=357–4,318 mg/kg) with a relatively high variation and the
highest of all the samples analyzed (<xref ref-type="fig" rid="fig_002">Fig. 2</xref> and
<xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>).
Similar trends were observed for magnesium and phosphorus; decaying <italic>A.
aubryanum</italic> had the highest levels of all the samples analyzed. However, decaying
<italic>A. aubryanum</italic> did not necessarily have the highest levels of potassium and
calcium. <italic>A. aubryanum</italic> dead wood also did not show higher concentrations of
zinc, iron and copper than the other samples.</p><p>Latex from live <italic>A. aubryanum </italic>(n=2) contained ca. 199 mg (293 and 104)
Na/m<italic>l</italic>, ca. 11,988 mg (14,332 and 9,644) K/m<italic>l</italic>, ca. 494 mg
(417 and 517) Mg/m<italic>l</italic>, 117 mg (132 and 104) Ca/m<italic>l</italic> and 173 mg
(184 and 161) P/m<italic>l</italic>. Although the sample size was small (n=2), the variation
between two samples seems to be small in comparison with dead <italic>A.
aubryanum</italic>.</p><p>The fruits were seemingly freshly fallen from the tree on the ground, and some of them were
actually showed signs of feeding of gorillas. Among them, fruits of <italic>S.
gabonensis</italic> showed higher Na concentration (mean=823 mg/kg dry matter,
range=339–1,293 mg/kg than other fruits (from 0 to 70 mg/kg) (<xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>).</p><p><italic>Frequency of animal visiting to A. aubryanum stumps</italic>: During the study
period, our camera traps captured eight species, including <italic>Cephalophus</italic>spp., at decaying wood sites (<xref ref-type="fig" rid="fig_003">Fig. 3a and 3b</xref><fig orientation="portrait" fig-type="figure" id="fig_003" position="float"><label>Fig. 3.</label><caption><p>Capture rate (a) and stay duration (b) of herbivorous species (N of video/100
camera-days, Mean ± SD) at decaying wood of <italic>A. aubryanum</italic> wood sites
(n=5) and at control sites (n=10). *<italic>P</italic><0.05.</p></caption><graphic xlink:href="jvms-77-1247-g003"></graphic></fig>). All animal species captured at decaying wood sites were herbivorous species. In
contrast, insectivores/ carnivores were never observed to consume decaying <italic>A.
aubryanum</italic> stumps. The species that visited most frequently was the blue duiker
(<italic>Philotomba monticola</italic>), followed by gorillas, yellow-backed duiker
(<italic>Cephalophus silvicultor</italic>) and chimpanzees (<italic>Pan troglodytes
troglodytes</italic>) (<xref ref-type="fig" rid="fig_003">Fig. 3a</xref>). Blue duikers,
gorillas, yellow-backed duikers, chimpanzees and red-capped mongabey (<italic>Cercocebus
torquatus</italic>) stayed significantly longer at decaying <italic>A. aubryanum</italic>sites than at control sites (<xref ref-type="fig" rid="fig_003">Fig. 3b</xref>). Our camera
trap results show that, two species of great apes visited <italic>A. aubryanum</italic>stumps significantly more frequently (<xref ref-type="fig" rid="fig_003">Fig. 3a</xref>) and
stayed longer than at control sites (<xref ref-type="fig" rid="fig_003">Fig. 3b</xref>).
These results indicate that great apes were strongly attracted to decaying <italic>A.
aubryanum</italic>.</p><p><italic>Decaying A. aubryanum as regular food material for gorillas</italic>: In total, 704
fecal samples (monthly mean=88, range=40–161) were analyzed (<xref ref-type="fig" rid="fig_004">Fig. 4</xref><fig orientation="portrait" fig-type="figure" id="fig_004" position="float"><label>Fig. 4.</label><caption><p>Proportions of fecal samples of <italic>Gorilla gorilla gorilla</italic> containing
<italic>A. aubryanum</italic> debris in November to December from 2004 to 2007.
Numbers in parentheses are total number of fecal samples collected in each month.</p></caption><graphic xlink:href="jvms-77-1247-g004"></graphic></fig>). Debris from decaying <italic>A. aubryanum</italic> wood was found in 28.9% of the
fecal samples. During the study period, only December 2007 showed low (6%) proportion of
<italic>A. aubryanum</italic> occurrence in fecal samples. In contrast, <italic>A.
aubryanum</italic> occurrence rates were more than 10% in other seven months. Especially,
the proportions of fecal samples containing <italic>A. aubryanum</italic> in November 2004
and November 2006 were more than 40%. Thus, it can be said that <italic>A.
aubryanum</italic> dead wood is one of a regular food for western lowland gorillas in
PNMD.</p></sec><sec sec-type="discussion" id="s3"><title>DISCUSSION</title><p><italic>A. aubryanum wood as sodium resource for herbivores</italic>: Our chemical analysis
confirmed that decaying woods of <italic>A. aubryanum</italic> have high cations, especially
sodium concentrations was much higher than those of other live/dead trees or fruits (<xref ref-type="fig" rid="fig_002">Fig. 2</xref> and <xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>). Thus, decaying wood stump
of <italic>A. aubryanum</italic> is an important mineral resource for diverse herbivores in
PNMD. Herbivores should selectively ingest it to compensate specifically for a shortfall in
sodium. To our knowledge, this is the first report indicating the tight relationship between
herbivores and a particular plant species whose latex is toxic and caustic when it is alive.
When <italic>A. aubryanum</italic> is alive, the sodium content of the bark of this tree is
low, although its latex contains cations at relatively high concentrations. Latex produced
by Euphorbiaceae is known to carry higher quantities of cations [<xref rid="r2" ref-type="bibr">2</xref>]. The higher cation content of latex may contribute to cation
accumulation in decaying <italic>A. aubryanum</italic> wood. But, latex of <italic>A.
aubryanum</italic>, as a component of live plant, contained potassium as the major cation
(<xref rid="pdf_001" ref-type="supplementary-material">Supplementary Table 1</xref>).
Other mechanisms would be involved in sodium accumulation in dead <italic>A.
aubryanum</italic>.</p><p><italic>Difference of selectivity of A. aubryanum among mammals</italic>: We detected clear
difference of selectivity of <italic>A. aubryanum</italic> consumption among mammals
inhabiting in PNMD. These differences of decaying <italic>A. aubryanum</italic> consumption
reflected the difference of dietary feature or ecological conditions among them. We did not
detect carnivores and omnivores visiting to <italic>A. aubryanum</italic> stumps, because
they can acquire sodium from animal food. On the contrary, all mammals captured by camera
trapping were limited to forest herbivores. Because sodium concentration of regular diet for
herbivores is low, so herbivores consumed <italic>A. aubryanum</italic> as sodium resource
in PNMD. We detected at least two duikers, blue duikers and yellow-backed duikers, visited
with high frequency (more than 10 captures/ 100 camera-days), but duration of staying was
much shorter than gorillas (<xref ref-type="fig" rid="fig_003">Fig. 3b</xref>). Duikers’
short retention time at decaying stumps was to decrease the possibility to be found by their
predator, such as leopards.</p><p>Our results indicate that <italic>A. aubryanum</italic> decaying wood is the critically
important sodium resource for gorillas. Gorillas showed the second highest frequency and the
longest duration of visit (<xref ref-type="fig" rid="fig_003">Fig 3a and 3b</xref>). Fecal
sample analysis showed that <italic>A. aubryanum</italic> is one of a regular food for
gorillas. Chimpanzees also showed significantly higher frequency and longer duration to
visit <italic>A. aubryanum</italic> stumps than control sites, but gorillas showed higher
frequency and longer duration than chimpanzees. Great apes are known that their main diet
consists of fruits and leaves, but previous reports showed that chimpanzees occasionally
hunt other animals or fishing ants or termites [<xref rid="r9" ref-type="bibr">9</xref>]. In
contrast, gorillas do not hunt other animals, and frequency of insect consumption is low in
PNMD (5% of fecal samples; Iwata <italic>et al</italic>. unpublished data). The longest
duration of staying at <italic>A. aubryanum</italic> decaying wood by gorillas might be
caused by lack of predator for them. Furthermore, chimpanzees have fission-fusion group
structure and forage in smaller parties or alone [<xref rid="r5" ref-type="bibr">5</xref>],
but large body-sized gorillas are group living animal, and our research group has more than
20 individuals [<xref rid="r1" ref-type="bibr">1</xref>]. Thus, it should take long duration
for gorillas that plural individuals consume enough amount of decaying wood, because of
higher feeding competition than chimpanzees.</p><p>Herbivores which inhabiting in the forest which lacks “bai” have alternative mineral
resources. In Petit Loango, Gabon, elephant often used the coastal habitat for the
consumption of salt-coated vegetation [<xref rid="r11" ref-type="bibr">11</xref>]. In Lopé
National Park, Gabon, western lowland gorillas depend on sodium-rich <italic>Marantochloa
cordifolia</italic> [<xref rid="r17" ref-type="bibr">17</xref>]. Although further chemical
analysis on other food items is necessary, <italic>A. aubryanum</italic> showed almost the
same level of sodium concentration with <italic>Hydrocharis</italic> sp. which is an
important sodium resource for gorillas in Ndoki forest (<italic>Hydrocharis</italic> sp.:
1,080 mg/kg vs. <italic>A. aubryanum</italic>: 1,343 mg/kg). <italic>A. aubryanum</italic>which abundantly exists in PNMD might play an important roll for herbivores as sodium
resource, which is available year-round for herbivores in our study site.</p></sec><sec sec-type="supplementary-material"><title>Supplementary Material</title><supplementary-material content-type="local-data" id="pdf_001"><caption><title>Supplement table</title></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jvms-77-1247-s001.pdf" orientation="portrait" xlink:type="simple" id="d35e829" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="pdf_002"><caption><title>Supplement figure</title></caption><media mimetype="application" mime-subtype="pdf" xlink:href="jvms-77-1247-s002.pdf" orientation="portrait" xlink:type="simple" id="d35e834" position="anchor"></media></supplementary-material><supplementary-material content-type="local-data" id="video_003"><caption><title>Supplement Video</title></caption><media mimetype="video" mime-subtype="avi" xlink:href="jvms-77-1247-s003.avi" orientation="portrait" xlink:type="simple" id="d35e839" position="anchor"></media><media mimetype="video" mime-subtype="avi" xlink:href="jvms-77-1247-s004.avi" orientation="portrait" xlink:type="simple" id="d35e840" position="anchor"></media></supplementary-material></sec></body><back><ack><p>This study was conducted in cooperation with the Centre National de la Recherche
Scientifique et Technologique (CENAREST, Gabon). We thank the Agence National des Parcs
Nationaux of the Gabon government for permission and support for our research project in
Gabon. We are also indebted to all field assistants of Moukalaba-Doudou National Park for
their kind support and hospitality. We thank Professor Junta Yanai, Laboratory of Soil
Science, Kyoto Prefectural University, for his kind helps for mineral analyses. This study
was financially supported in part by the Japan Science and Technology Agency/ Japan
International Cooperation Agency, Science and Technology Research Partnership for
Sustainable Development. This research complied with PACUC regulations and regal requirement
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