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  <front>
    <journal-meta>
<journal-id journal-id-type="publisher">PB</journal-id>
<journal-title-group>
<journal-title>Primate Biology</journal-title>
<abbrev-journal-title abbrev-type="publisher">PB</abbrev-journal-title>
<abbrev-journal-title abbrev-type="nlm-ta">Primate Biol.</abbrev-journal-title>
</journal-title-group>
<issn pub-type="epub">2363-4715</issn>
<publisher><publisher-name>Copernicus Publications</publisher-name>
<publisher-loc>Göttingen, Germany</publisher-loc>
</publisher>
</journal-meta>

    <article-meta>
      <article-id pub-id-type="doi">10.5194/pb-4-127-2017</article-id><title-group><article-title>Fur-rubbing with <italic>Piper</italic> leaves in the San Martín titi monkey, <italic>Callicebus oenanthe</italic></article-title>
      </title-group><?xmltex \runningtitle{Fur-rubbing with \textit{Piper} leaves in the San Mart\'{\i}n titi monkey}?><?xmltex \runningauthor{R.~Huashuayo-Llamocca and E.~W.~Heymann}?>
      <contrib-group>
        <contrib contrib-type="author" corresp="no" rid="aff1 aff2">
          <name><surname>Huashuayo-Llamocca</surname><given-names>Rosario</given-names></name>
          
        </contrib>
        <contrib contrib-type="author" corresp="yes" rid="aff3">
          <name><surname>Heymann</surname><given-names>Eckhard W.</given-names></name>
          <email>eheyman@gwdg.de</email>
        <ext-link>https://orcid.org/0000-0002-4259-8018</ext-link></contrib>
        <aff id="aff1"><label>1</label><institution>Proyecto Mono Tocón, Jr. Reyes Guerra No. 430,
Moyobamba, Peru</institution>
        </aff>
        <aff id="aff2"><label>2</label><institution>Facultad de Ciencias Biológicas, Universidad Nacional San Luis
Gonzaga de Ica, Av. Los Maestros s/n, Ica, Peru</institution>
        </aff>
        <aff id="aff3"><label>3</label><institution>Verhaltensökologie und Soziobiologie, Deutsches Primatenzentrum,
Leibniz-Institut für Primatenforschung, Kellnerweg 4, 37077
Göttingen, Germany</institution>
        </aff>
      </contrib-group>
      <author-notes><corresp id="corr1">Eckhard W. Heymann (eheyman@gwdg.de)</corresp></author-notes><pub-date><day>26</day><month>June</month><year>2017</year></pub-date>
      
      <volume>4</volume>
      <issue>1</issue>
      <fpage>127</fpage><lpage>130</lpage>
      <history>
        <date date-type="received"><day>21</day><month>April</month><year>2017</year></date>
           <date date-type="rev-recd"><day>29</day><month>May</month><year>2017</year></date>
           <date date-type="accepted"><day>30</day><month>May</month><year>2017</year></date>
      </history>
      <permissions>
<license license-type="open-access">
<license-p>This work is licensed under the Creative Commons Attribution 3.0 Unported License. To view a copy of this licence, visit <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/3.0/">https://creativecommons.org/licenses/by/3.0/</ext-link></license-p>
</license>
</permissions><self-uri xlink:href="https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017.html">This article is available from https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017.html</self-uri>
<self-uri xlink:href="https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017.pdf">The full text article is available as a PDF file from https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017.pdf</self-uri>


      <abstract>
    <p>We report observations on fur-rubbing with leaves from <italic>Piper aduncum</italic> by a San Martín titi
monkey, <italic>Callicebus oenanthe</italic>. Fur-rubbing occurred during the transition from the dry to the
rainy season in a titi monkey group living in a forest fragment in the Moyobamba
region of Peru. Since <italic>Piper </italic>leaves include very potent compounds that may affect
ectoparasites, we tentatively interpret the observed fur-rubbing as
self-medication.</p>
  </abstract>
    </article-meta>
  </front>
<body>
      

<sec id="Ch1.S1" sec-type="intro">
  <title>Introduction</title>
      <p>Several primate and at least one carnivore species rub their fur with
arthropods or their secretions, plant material (leaves, resin) or other
substances, including man-made substances (tobacco smoke, soap), both in the
wild and in captivity (Birkinshaw, 1999; Bowler et al., 2015; Gasco et al.,
2016; Gompper and Hoylman, 1993; Huffman, 1997, 2011; Morrogh-Bernard, 2009;
Nolte, 1958). Repelling or killing ectoparasites and microbial pathogens is
invoked as the principal function of fur-rubbing (Baker, 1996; Falótico
et al., 2007; Valderrama et al., 2000; Weldon et al., 2003), but it may also
be involved in social bonding and olfactory communication (Campbell, 2000;
Leca et al., 2007; Paukner and Suomi, 2012).</p>
      <p>For titi monkeys, Carrillo-Bilbao et al. (2005) report fur-rubbing with
chewed leaves of <italic>Tetrathylacium </italic>in <italic>Callicebus discolor</italic> (<italic>Plecturocebus discolor</italic>) from Yasuní, Ecuador, and with chewed leaves
of five Annonaceae species and one Bignonaceae species in <italic>Callicebus toppini</italic>
(<italic>Plecturocebus toppini</italic>) from Manu, Peru. In this paper, we report the use of <italic>Piper aduncum</italic> leaves by the
San Martín titi monkey <italic>Callicebus oenanthe</italic> (<italic>Plecturocebus oenanthe</italic>), observed during an ecological study on
this endemic and highly endangered species.</p>
</sec>
<sec id="Ch1.S2">
  <title>Methods</title>
<sec id="Ch1.S2.SS1">
  <title>Study area</title>
      <p>The observations were made in a 4 ha forest fragment surrounded by pastures
and agricultural fields in the district of Yantaló, province of
Moyobamba, department of San Martín (UTM coordinates: 9338221.4 northing,
274918.8 easting, 18M; Fig. 1).
The fragment is located at the periphery of
the protected area “Morro de Calzada”. The vegetation is dominated by
species of Vochysiaceae, Moraceae, Lauraceae and Bignonaceae. It reaches
12–15 m height and includes a dense understory (Romero Herrada, unpublished
data). Average annual temperature is 22.8 <inline-formula><mml:math id="M1" display="inline"><mml:msup><mml:mi/><mml:mo>∘</mml:mo></mml:msup></mml:math></inline-formula>C and annual precipitation
around 1350 mm with &lt; 100 mm per month from May to August
(climate-data.org, 2017). During our study period, September also received
&lt; 100 mm rain (Fig. 2).</p>

      <?xmltex \floatpos{t}?><fig id="Ch1.F1" specific-use="star"><caption><p>Location of the study area.</p></caption>
          <?xmltex \igopts{width=341.433071pt}?><graphic xlink:href="https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017-f01.jpg"/>

        </fig>

      <?xmltex \floatpos{t}?><fig id="Ch1.F2"><caption><p>Mean daily maximum temperature (•), mean daily minimum
temperature (<inline-formula><mml:math id="M2" display="inline"><mml:mrow><mml:mi mathvariant="italic">⧫</mml:mi><mml:mo>)</mml:mo></mml:mrow></mml:math></inline-formula> and total monthly rainfall (bars) during the
study period May–December 2014. Data from
<uri>http://www.senamhi.gob.pe/main_mapa.php?t=dHi</uri> (accessed 5
April 2017).</p></caption>
          <?xmltex \igopts{width=236.157874pt}?><graphic xlink:href="https://pb.copernicus.org/articles/4/127/2017/pb-4-127-2017-f02.jpg"/>

        </fig>

</sec>
<sec id="Ch1.S2.SS2">
  <title>Study group and observational methods</title>
      <p>The study group included one adult male, one adult female, one subadult
female and one juvenile female. It was observed between May and December
2014, for a total of 238 h. We used instantaneous scan sampling for
determining the activity budget and use of space, focal animal sampling for
feeding behaviour and behaviour sampling (for rare but significant
behaviours like the one reported here).</p>
</sec>
</sec>
<sec id="Ch1.S3" sec-type="conclusions">
  <title>Results</title>
      <p>During focal animal observations, the adult male was seen three times in
September and October biting off a leaf from spiked pepper trees, <italic>Piper aduncum</italic>, and
squeezing it with both hands. Then the squeezed leaf was rubbed against the
abdominal area. This behaviour lasted between 5 and 15 min and involved
either a single leaf or up to four leaves.</p>
      <p>The adult female was also observed rubbing the abdominal area, but we never
saw the collection of <italic>P. aduncum</italic> leaves. We could not see whether the female may have
used material smaller than <italic>P. aduncum</italic> leaves for fur-rubbing. Fur-rubbing was not
observed in the subadult and juvenile females.</p>
</sec>
<sec id="Ch1.S4">
  <title>Discussion</title>
      <p><italic>Piper aduncum</italic>, known in Peru as “matico”, is widely distributed in the Neotropics. It
is used in traditional medicine for a broad spectrum of ailments. This
includes both internal and external (topical) use of leaf extracts,
infusions and decoctions (Taylor, 2006). Constituents of <italic>P. aduncum</italic>, like dillapiole
and other phenylpropanoids, are potent insecticides (Fazolin et al., 2014;
Marques and Kaplan, 2015; Pino et al., 2011; Piton et al., 2014; Ribeiro et
al., 2016; Vila et al., 2005; Volpe et al., 2015). Extracts of <italic>P. aduncum</italic> have also
been shown to possess antifungal properties (Santos et al., 2013). While it
is unclear whether extracts obtained by squeezing the leaves render all
these bioactive constituents, it is highly likely that at least some
constituents are released. Therefore, it is plausible to assume that the fur-rubbing with <italic>P. aduncum</italic> leaves observed in <italic>C. oenanthe</italic> functions as a topical self-medication, as
suggested for several other primate species. Wild capuchin monkeys, <italic>Cebus capucinus</italic>, and
captive owl monkeys, <italic>Aotus</italic> spp., have been reported to use leaves from <italic>Piper marginatum</italic> for fur-rubbing (Baker, 1996; Zito et al., 2003).</p>
      <p><?xmltex \hack{\newpage}?>Fur-rubbing was observed in September and October, which are months that mark the fast
transition from the relatively dry to the wet season (Fig. 2). We speculate
that it is related to repelling or killing ectoparasites like ticks,
chiggers or mosquitoes that might increase with the onset of the rainy
season. For instance, the tick <italic>Amblyomma longirostre</italic> that infests a large number of birds, and
terrestrial and arboreal mammals (mainly rodents) throughout the Neotropics,
is known from the Moyobamba region (Nava et al., 2010). <italic>Alouatta guariba</italic> and <italic>Sapajus nigritus</italic> are infested
by different species of <italic>Amblyomma</italic> (Guglielmone et al., 1990; Martins et al., 2015),
and larval <italic>Amblyomma</italic> were the most common ectoparasite of <italic>Leontopithecus rosalia</italic> (Wilson et al., 1989). As
ticks have several life stages (larvae, nymphs, adults), their response to
climatic conditions can be quite complex, but some species may show higher
activity of adults during the rainy season (Labruna et al., 2002; Lacerra de
Souza et al., 2006). In sifakas, <italic>Propithecus edwardsi</italic>, ectoparasite richness was higher in the
wet compared to the dry season in all habitats, as was the intensity of tick
and fly infestations in disturbed habitats (Wright et al., 2009). Mouse
lemurs, <italic>Microcebus griseorufus</italic>, were infested by ticks during the dry season, and males have
higher infestation rates than females due to more frequent use of the ground
(Rodriguez et al., 2015). Infestation by chiggers also varies seasonally
(e.g. Dietsch, 2005), and mosquitoes are more abundant during the rainy
season.</p>
      <p>Although our observations are anecdotal and information on ectoparasites in
the Moyobamba region is scanty, our report expands the number of primate
species that exhibit topical application of leaves with medical potential.</p>
</sec>

      
      </body>
    <back><notes notes-type="dataavailability">

      <p>There are no further data apart from the observations reported in the paper.</p>
  </notes><notes notes-type="competinginterests">

      <p>Eckhard W. Heymann and Dietmar Zinner are employed by different departments of the Deutsches Primatenzentrum.</p>
  </notes><ack><title>Acknowledgements</title><p>We are grateful to Alberto A. Guglielmone (Instituto Nacional de
Tecnología Agropecuaria, Rafaela, Argentina) for help with literature
on ticks and to Jaemy Romero Herrada for botanical identification of the
leaves and for sharing his unpublished data on habitat characterization and
structure in the protected area Morro de Calzada. We are thankful to Michael Huffman, Dietmar Zinner and an anonymous reviewer for constructive comments
on the manuscript. The study during which the observations were made was
conducted under authorization from the Dirección General Forestal y de
Fauna Silvestre of the Ministerio de Agricultura in Lima (authorization no.
0208-2012-AG-DGFFS-DGEFFS) and was
only possible due to financial support from Le Conservatoire pour la Protection, La
Vallée des Singes Primate Park, Blackpool Zoo, Zoo Amnéville, Paris Zoo, London Zoo,
Zoo de la Boissière du Doré, Apenheul Primate Park and Basel Zoo to the Proyecto Mono Tocón.
We are most grateful to these institutions.<?xmltex \hack{\newline}?><?xmltex \hack{\newline}?>
Edited by: Dietmar Zinner<?xmltex \hack{\newline}?>
Reviewed by: Michael Huffman and one anonymous referee</p></ack><ref-list>
    <title>References</title>

      <ref id="bib1.bib1"><label>1</label><mixed-citation>Baker, M.: Fur rubbing: use of medicinal plants by capuchin monkeys (<italic>Cebus capucinus</italic>),
Am. J. Primatol., 38, 263–270, 1996.</mixed-citation></ref>
      <ref id="bib1.bib2"><label>2</label><mixed-citation>
Birkinshaw, C. R.: Use of millipedes by black lemurs to anoint their bodies,
Folia Primatol., 70, 170–181, 1999.</mixed-citation></ref>
      <ref id="bib1.bib3"><label>3</label><mixed-citation>Bowler, M., Messer, E. J. E., Claidière, N., and Whiten, A.: Mutual
medication in capuchin monkeys – Social anointing improves coverage of
topically applied anti-parasite medicines, Scientific Reports, 5, 15030,
<ext-link xlink:href="https://doi.org/10.1038/srep15030" ext-link-type="DOI">10.1038/srep15030</ext-link>,
2015.</mixed-citation></ref>
      <ref id="bib1.bib4"><label>4</label><mixed-citation>Campbell, C. J.: Fur rubbing behavior in free-ranging black-handed spider
monkeys (<italic>Ateles geoffroyi</italic>) in Panama, Am. J. Primatol., 51, 205–208, 2000.</mixed-citation></ref>
      <ref id="bib1.bib5"><label>5</label><mixed-citation>Carrillo-Bilbao, G., Di Fiore, A., and Fernandez-Duque, E.: Dieta, forrajeo
y presupuesto de tiempo en cotoncillos (<italic>Callicebus discolor</italic>) del Parque Nacional Yasuní en
la Amazonia ecuatoriana, Neotro. Primates, 13, 7–11, 2005.</mixed-citation></ref>
      <ref id="bib1.bib6"><label>6</label><mixed-citation>Climate-data.org: Climate: Moyobamba, available at:
<uri>https://en.climate-data.org/location/4364/</uri>, last access: 29 May
2017.</mixed-citation></ref>
      <ref id="bib1.bib7"><label>7</label><mixed-citation>
Dietsch, T. V.: Seasonal variation of infestation by ectoparasitic chigger
mite larvae (Acarina: Trombiculidae) on resident and migratory birds in
coffee agroecosystems of Chiapas, Mexico, J. Parasitol., 91,
1294–1303, 2005.</mixed-citation></ref>
      <ref id="bib1.bib8"><label>8</label><mixed-citation>Falótico, T., Labruna, M. B., Verderane, M. P., De Resende, B. D., Izar,
P., and Ottoni, E. B.: Repellent efficacy of formic acid and the abdominal
secretion of carpenter ants (Hymenoptera: Formicidae) against <italic>Amblyomma </italic>ticks (Acari:
Ixodidae), J. Med. Entomol., 44, 718–721, 2007.</mixed-citation></ref>
      <ref id="bib1.bib9"><label>9</label><mixed-citation>
Gasco, A. D. C., Pérez-Acosta, A. M., and Monticelli, P. F.: Ring-tailed
coatis anointing with soap: a new variation of self-medication culture?,
Int. J. Comp. Psychol., 29, 1–11, 2016.</mixed-citation></ref>
      <ref id="bib1.bib10"><label>10</label><mixed-citation>Gompper, M. E. and Hoylman, A. M.: Grooming with <italic>Trattinnickia </italic>resin: possible
pharmaceutical plant use by coatis, J. Trop. Ecol., 9, 533–540,
1993.</mixed-citation></ref>
      <ref id="bib1.bib11"><label>11</label><mixed-citation>Guglielmone, A. A., Mangold, A. J., and Keirans, J. E.: Redescription of the
male and female of <italic>Amblyomma parvum</italic> Aragao, 1908, and description of the nymph and larva,
and description of all stages of <italic>Amblyomma pseudoparvum</italic> sp. n. (Acari: Ixodida: Ixodidae),
Acarologia, 31, 143–159, 1990.</mixed-citation></ref>
      <ref id="bib1.bib12"><label>12</label><mixed-citation>
Huffman, M. A.: Current evidence for self-medication in primates: a
multidisciplinary perspective, Yearb. Phys. Anthropol., 40,
171–200, 1997.</mixed-citation></ref>
      <ref id="bib1.bib13"><label>13</label><mixed-citation>
Huffman, M. A.: Primate self-medication, in: Primates in perspective, 2nd
edn., edited by: Campbell, C., Fuentes, A., MacKinnon, K., Panger, M., and
Bearder S., University of Oxford Press, Oxford, 563–573, 2011.</mixed-citation></ref>
      <ref id="bib1.bib14"><label>14</label><mixed-citation>
Labruna, M. B., Kasai, N., Ferreira, F., Faccini, J. L. H., and Gennari, S.
M.: Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of
São Paulo, Brazil, Vet. Parasitol., 105, 65–77, 2002.</mixed-citation></ref>
      <ref id="bib1.bib15"><label>15</label><mixed-citation>
Lacerra de Souza, S. S. A., de Souza, C. E., Neto, E. J. R., and do Prado, A. P.: Dinâmica sazonal de carrapatos
(Acari: Ixodidae) na mata ciliar de uma área endêmica para febre maculosa na região de Campinas, São Paulo, Brasil, Ciencia Rural, 36, 887–891, 2006.</mixed-citation></ref>
      <ref id="bib1.bib16"><label>16</label><mixed-citation>Leca, J.-B., Gunst, N., and Petit, O.: Social aspects of fur-rubbing in
<italic>Cebus capucinus</italic> and <italic>C. apella</italic>, Int. J. Primatol., 28, 801–817, 2007.</mixed-citation></ref>
      <ref id="bib1.bib17"><label>17</label><mixed-citation>Marques, A. and Kaplan, M. A. C.: Active metabolites of the genus <italic>Piper </italic>against
<italic>Aedes aegypti</italic>: natural alternative sources for dengue vector control, Universitas
Scientiarum, 20, 61–82, 2015.</mixed-citation></ref>
      <ref id="bib1.bib18"><label>18</label><mixed-citation>
Martins, T. F., Teixeira, R. H. F., and Labruna, M. B.: Ocorrência de
carrapatos em animais silvestres recebidos e atendidos pelo Parque
Zoológico Municipal Quinzinho de Barros, Sorocaba, São Paulo,
Brasil, Braz. J. Vet. Res. Anim. Sci., 52,
319–324, 2015.</mixed-citation></ref>
      <ref id="bib1.bib19"><label>19</label><mixed-citation>Morrogh-Bernard, H. C.: Fur-rubbing as a form of self-medication in <italic>Pongo pygmaeus</italic>,
Int. J. Primatol., 29, 1059–1064, 2009.</mixed-citation></ref>
      <ref id="bib1.bib20"><label>20</label><mixed-citation>Nava, S., Velazco, P. M., and Guglielmone, A. A.: First record of <italic>Amblyomma longirostre</italic> (Koch,
1844) (Acari: Ixodidae) from Peru, with a review of this tick's host
relationships, Syst. Appl. Acarol., 15, 21–30, 2010.</mixed-citation></ref>
      <ref id="bib1.bib21"><label>21</label><mixed-citation>Nolte, A.: Beobachtungen über das Instinktverhalten von Kapuzineraffen
(<italic>Cebus apella</italic> L.) in der Gefangenschaft, Behaviour, 12, 183–207, 1958.</mixed-citation></ref>
      <ref id="bib1.bib22"><label>22</label><mixed-citation>Paukner, A. and Suomi, S. J.: Social after-effects of fur rubbing in tufted
capuchin monkeys (<italic>Cebus apella</italic>): increased antagonism and reduced affiliation, Primates,
53, 297–301, 2012.</mixed-citation></ref>
      <ref id="bib1.bib23"><label>23</label><mixed-citation>Pino, O., Sánchez, Y., Rodríguez, H., Correa, T., Demedio, J., and
Sanabria, J.: Chemical characterization and acaricidal activity of the
essential oil from <italic>Piper aduncum</italic> subsp. <italic>ossanum </italic>against <italic>Varroa destructor</italic>, Revista de Protección Vegetal, 26,
52–61, 2011.</mixed-citation></ref>
      <ref id="bib1.bib24"><label>24</label><mixed-citation>
Piton, L. P., Turchen, L. M., Butnariu, A. R., and Pereira, M. J. B.: Natural
insecticide based-leaves extract of Piper aduncum (Piperaceae) in the control of stink bug brown soybean, Ciência Rural, 44, 1915–1920, 2014.</mixed-citation></ref>
      <ref id="bib1.bib25"><label>25</label><mixed-citation>Ribeiro, N., Camara, C., and Ramos, C.: Toxicity of essential oils of <italic>Piper marginatum</italic> Jacq.
against <italic>Tetranychus urticae</italic> Koch and <italic>Neoseiulus californicus</italic> (McGregor), Chilean Journal of Agricultural Research, 76,
71–76, 2016.</mixed-citation></ref>
      <ref id="bib1.bib26"><label>26</label><mixed-citation>Rodriguez, I. A., Rasoazanabary, E., and Godfrey, L. R.: Seasonal variation
in the abundance and distribution of ticks that parasitize <italic>Microcebus griseorufus</italic> at the Bezà
Mahafaly Special Reserve, Madagascar, I. J.
Parasitol., 4, 408–413, 2015.
</mixed-citation></ref><?xmltex \hack{\newpage}?>
      <ref id="bib1.bib27"><label>27</label><mixed-citation>Santos, M. L., Magalhães, C. F., Rosa, M. B. d., Santos, D. d. A.,
Brasileiro, B. G., Carvalho, L. M. d., Silva, M. B. d., Zani, C. L.,
Siqueira, E. P. d., and Peres, R. L.: Antifungal activity of extracts from
<italic>Piper aduncum</italic> leaves prepared by different solvents and extraction techniques against
dermatophytes <italic>Trichophyton rubrum</italic> and <italic>Trichophyton interdigitale</italic>, Brazil. J. Microbiol., 44, 1275–1278, 2013.</mixed-citation></ref>
      <ref id="bib1.bib28"><label>28</label><mixed-citation>Taylor, L.: Technical data report for matico (<italic>Piper aduncum</italic>,
<italic>angustifolium</italic>), available at:
<uri>http://www.rain-tree.com/reports/matico-tech-report.pdf</uri>  (last access: 30
November 2016), 2006.</mixed-citation></ref>
      <ref id="bib1.bib29"><label>29</label><mixed-citation>
Valderrama, X., Robinson, J. G., Attygalle, A. B., and Eisner, T.: Seasonal
anointment with millipedes in a wild primate: a chemical defense against
insects?, J. Chem. Ecol., 26, 2781–2790, 2000.</mixed-citation></ref>
      <ref id="bib1.bib30"><label>30</label><mixed-citation>Vila, R., Tomi, F., Mundina, M., Santana, A. I., Solís, P. N., Lopez
Arce, J. B., Iclina, B., José, L., Iglesias, J., and Gupta, M. P.:
Unusual composition of the essential oils from the leaves of <italic>Piper aduncum</italic>, Flavour
Frag. J., 20, 67–69, 2005.</mixed-citation></ref>
      <ref id="bib1.bib31"><label>31</label><mixed-citation>Volpe, H. X., Fazolin, M., Garcia, R. B., Magnani, R. F., Barbosa, J. C.,
and Miranda, M. P.: Efficacy of essential oil of <italic>Piper aduncum</italic> against nymphs and adults
of <italic>Diaphorina citri</italic>, Pest Manageg. Sci.,  76, 1242–1249, <ext-link xlink:href="https://doi.org/10.1002/ps.4143" ext-link-type="DOI">10.1002/ps.4143</ext-link>, 2015.</mixed-citation></ref>
      <ref id="bib1.bib32"><label>32</label><mixed-citation>Weldon, P. J., Aldrich, J. R., Klun, J. A., Oliver, J. E., and Debboun, M.:
Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in
capuchin monkeys (<italic>Cebus </italic>spp.), Naturwissenschaften, 90, 301–304, 2003.</mixed-citation></ref>
      <ref id="bib1.bib33"><label>33</label><mixed-citation>Wilson, N., Dietz, J. M., and Whitaker Jr., J. O.: Ectoparasitic Acari found
on golden lion tamarins (<italic>Leontopithecus rosalia rosali</italic>a) from Brazil, J. Wildlife Dis., 25,
433–435, 1989.</mixed-citation></ref>
      <ref id="bib1.bib34"><label>34</label><mixed-citation>
Wright, P. C., Arrigo-Nelson, S. J., Hogg, K. L., Bannon, B., Morelli, T.
L., Wyatt, J., Harivelo, A. L., and Ratelolahy, F.: Habitat disturbance and
seasonal fluctuations of lemur parasites in the rain forest of Ranomafana
National Park, Madagascar, in: Primate parasite ecology: the dynamics and
study of host-parasite relationships, edited by: Huffman, M. A. and
Chapman, C. A., Cambridge University Press, Cambridge, 311–330, 2009.</mixed-citation></ref>
      <ref id="bib1.bib35"><label>35</label><mixed-citation>Zito, M., Evans, S., and Weldon, P. J.: Owl monkeys (<italic>Aotus</italic> spp.) self-anoint with
plants and millipedes, Folia Primatol., 74, 159–161, 2003.</mixed-citation></ref>

  </ref-list><app-group content-type="float"><app><title/>

    </app></app-group></back>
    <!--<article-title-html>Fur-rubbing with <i>Piper</i> leaves in the San Martín titi monkey, <i>Callicebus oenanthe</i></article-title-html>
<abstract-html><p class="p">We report observations on fur-rubbing with leaves from <i>Piper aduncum</i> by a San Martín titi
monkey, <i>Callicebus oenanthe</i>. Fur-rubbing occurred during the transition from the dry to the
rainy season in a titi monkey group living in a forest fragment in the Moyobamba
region of Peru. Since <i>Piper </i>leaves include very potent compounds that may affect
ectoparasites, we tentatively interpret the observed fur-rubbing as
self-medication.</p></abstract-html>
<ref-html id="bib1.bib1"><label>1</label><mixed-citation>
Baker, M.: Fur rubbing: use of medicinal plants by capuchin monkeys (<i>Cebus capucinus</i>),
Am. J. Primatol., 38, 263–270, 1996.
</mixed-citation></ref-html>
<ref-html id="bib1.bib2"><label>2</label><mixed-citation>
Birkinshaw, C. R.: Use of millipedes by black lemurs to anoint their bodies,
Folia Primatol., 70, 170–181, 1999.
</mixed-citation></ref-html>
<ref-html id="bib1.bib3"><label>3</label><mixed-citation>
Bowler, M., Messer, E. J. E., Claidière, N., and Whiten, A.: Mutual
medication in capuchin monkeys – Social anointing improves coverage of
topically applied anti-parasite medicines, Scientific Reports, 5, 15030,
<a href="https://doi.org/10.1038/srep15030" target="_blank">https://doi.org/10.1016/10.1038/srep15030</a>,
2015.
</mixed-citation></ref-html>
<ref-html id="bib1.bib4"><label>4</label><mixed-citation>
Campbell, C. J.: Fur rubbing behavior in free-ranging black-handed spider
monkeys (<i>Ateles geoffroyi</i>) in Panama, Am. J. Primatol., 51, 205–208, 2000.
</mixed-citation></ref-html>
<ref-html id="bib1.bib5"><label>5</label><mixed-citation>
Carrillo-Bilbao, G., Di Fiore, A., and Fernandez-Duque, E.: Dieta, forrajeo
y presupuesto de tiempo en cotoncillos (<i>Callicebus discolor</i>) del Parque Nacional Yasuní en
la Amazonia ecuatoriana, Neotro. Primates, 13, 7–11, 2005.
</mixed-citation></ref-html>
<ref-html id="bib1.bib6"><label>6</label><mixed-citation>
Climate-data.org: Climate: Moyobamba, available at:
<a href="https://en.climate-data.org/location/4364/" target="_blank">https://en.climate-data.org/location/4364/</a>, last access: 29 May
2017.
</mixed-citation></ref-html>
<ref-html id="bib1.bib7"><label>7</label><mixed-citation>
Dietsch, T. V.: Seasonal variation of infestation by ectoparasitic chigger
mite larvae (Acarina: Trombiculidae) on resident and migratory birds in
coffee agroecosystems of Chiapas, Mexico, J. Parasitol., 91,
1294–1303, 2005.
</mixed-citation></ref-html>
<ref-html id="bib1.bib8"><label>8</label><mixed-citation>
Falótico, T., Labruna, M. B., Verderane, M. P., De Resende, B. D., Izar,
P., and Ottoni, E. B.: Repellent efficacy of formic acid and the abdominal
secretion of carpenter ants (Hymenoptera: Formicidae) against <i>Amblyomma </i>ticks (Acari:
Ixodidae), J. Med. Entomol., 44, 718–721, 2007.
</mixed-citation></ref-html>
<ref-html id="bib1.bib9"><label>9</label><mixed-citation>
Gasco, A. D. C., Pérez-Acosta, A. M., and Monticelli, P. F.: Ring-tailed
coatis anointing with soap: a new variation of self-medication culture?,
Int. J. Comp. Psychol., 29, 1–11, 2016.
</mixed-citation></ref-html>
<ref-html id="bib1.bib10"><label>10</label><mixed-citation>
Gompper, M. E. and Hoylman, A. M.: Grooming with <i>Trattinnickia </i>resin: possible
pharmaceutical plant use by coatis, J. Trop. Ecol., 9, 533–540,
1993.
</mixed-citation></ref-html>
<ref-html id="bib1.bib11"><label>11</label><mixed-citation>
Guglielmone, A. A., Mangold, A. J., and Keirans, J. E.: Redescription of the
male and female of <i>Amblyomma parvum</i> Aragao, 1908, and description of the nymph and larva,
and description of all stages of <i>Amblyomma pseudoparvum</i> sp. n. (Acari: Ixodida: Ixodidae),
Acarologia, 31, 143–159, 1990.
</mixed-citation></ref-html>
<ref-html id="bib1.bib12"><label>12</label><mixed-citation>
Huffman, M. A.: Current evidence for self-medication in primates: a
multidisciplinary perspective, Yearb. Phys. Anthropol., 40,
171–200, 1997.
</mixed-citation></ref-html>
<ref-html id="bib1.bib13"><label>13</label><mixed-citation>
Huffman, M. A.: Primate self-medication, in: Primates in perspective, 2nd
edn., edited by: Campbell, C., Fuentes, A., MacKinnon, K., Panger, M., and
Bearder S., University of Oxford Press, Oxford, 563–573, 2011.
</mixed-citation></ref-html>
<ref-html id="bib1.bib14"><label>14</label><mixed-citation>
Labruna, M. B., Kasai, N., Ferreira, F., Faccini, J. L. H., and Gennari, S.
M.: Seasonal dynamics of ticks (Acari: Ixodidae) on horses in the state of
São Paulo, Brazil, Vet. Parasitol., 105, 65–77, 2002.
</mixed-citation></ref-html>
<ref-html id="bib1.bib15"><label>15</label><mixed-citation>
Lacerra de Souza, S. S. A., de Souza, C. E., Neto, E. J. R., and do Prado, A. P.: Dinâmica sazonal de carrapatos
(Acari: Ixodidae) na mata ciliar de uma área endêmica para febre maculosa na região de Campinas, São Paulo, Brasil, Ciencia Rural, 36, 887–891, 2006.
</mixed-citation></ref-html>
<ref-html id="bib1.bib16"><label>16</label><mixed-citation>
Leca, J.-B., Gunst, N., and Petit, O.: Social aspects of fur-rubbing in
<i>Cebus capucinus</i> and <i>C. apella</i>, Int. J. Primatol., 28, 801–817, 2007.
</mixed-citation></ref-html>
<ref-html id="bib1.bib17"><label>17</label><mixed-citation>
Marques, A. and Kaplan, M. A. C.: Active metabolites of the genus <i>Piper </i>against
<i>Aedes aegypti</i>: natural alternative sources for dengue vector control, Universitas
Scientiarum, 20, 61–82, 2015.
</mixed-citation></ref-html>
<ref-html id="bib1.bib18"><label>18</label><mixed-citation>
Martins, T. F., Teixeira, R. H. F., and Labruna, M. B.: Ocorrência de
carrapatos em animais silvestres recebidos e atendidos pelo Parque
Zoológico Municipal Quinzinho de Barros, Sorocaba, São Paulo,
Brasil, Braz. J. Vet. Res. Anim. Sci., 52,
319–324, 2015.
</mixed-citation></ref-html>
<ref-html id="bib1.bib19"><label>19</label><mixed-citation>
Morrogh-Bernard, H. C.: Fur-rubbing as a form of self-medication in <i>Pongo pygmaeus</i>,
Int. J. Primatol., 29, 1059–1064, 2009.
</mixed-citation></ref-html>
<ref-html id="bib1.bib20"><label>20</label><mixed-citation>
Nava, S., Velazco, P. M., and Guglielmone, A. A.: First record of <i>Amblyomma longirostre</i> (Koch,
1844) (Acari: Ixodidae) from Peru, with a review of this tick's host
relationships, Syst. Appl. Acarol., 15, 21–30, 2010.
</mixed-citation></ref-html>
<ref-html id="bib1.bib21"><label>21</label><mixed-citation>
Nolte, A.: Beobachtungen über das Instinktverhalten von Kapuzineraffen
(<i>Cebus apella</i> L.) in der Gefangenschaft, Behaviour, 12, 183–207, 1958.
</mixed-citation></ref-html>
<ref-html id="bib1.bib22"><label>22</label><mixed-citation>
Paukner, A. and Suomi, S. J.: Social after-effects of fur rubbing in tufted
capuchin monkeys (<i>Cebus apella</i>): increased antagonism and reduced affiliation, Primates,
53, 297–301, 2012.
</mixed-citation></ref-html>
<ref-html id="bib1.bib23"><label>23</label><mixed-citation>
Pino, O., Sánchez, Y., Rodríguez, H., Correa, T., Demedio, J., and
Sanabria, J.: Chemical characterization and acaricidal activity of the
essential oil from <i>Piper aduncum</i> subsp. <i>ossanum </i>against <i>Varroa destructor</i>, Revista de Protección Vegetal, 26,
52–61, 2011.
</mixed-citation></ref-html>
<ref-html id="bib1.bib24"><label>24</label><mixed-citation>
Piton, L. P., Turchen, L. M., Butnariu, A. R., and Pereira, M. J. B.: Natural
insecticide based-leaves extract of Piper aduncum (Piperaceae) in the control of stink bug brown soybean, Ciência Rural, 44, 1915–1920, 2014.
</mixed-citation></ref-html>
<ref-html id="bib1.bib25"><label>25</label><mixed-citation>
Ribeiro, N., Camara, C., and Ramos, C.: Toxicity of essential oils of <i>Piper marginatum</i> Jacq.
against <i>Tetranychus urticae</i> Koch and <i>Neoseiulus californicus</i> (McGregor), Chilean Journal of Agricultural Research, 76,
71–76, 2016.
</mixed-citation></ref-html>
<ref-html id="bib1.bib26"><label>26</label><mixed-citation>
Rodriguez, I. A., Rasoazanabary, E., and Godfrey, L. R.: Seasonal variation
in the abundance and distribution of ticks that parasitize <i>Microcebus griseorufus</i> at the Bezà
Mahafaly Special Reserve, Madagascar, I. J.
Parasitol., 4, 408–413, 2015.

</mixed-citation></ref-html>
<ref-html id="bib1.bib27"><label>27</label><mixed-citation>
Santos, M. L., Magalhães, C. F., Rosa, M. B. d., Santos, D. d. A.,
Brasileiro, B. G., Carvalho, L. M. d., Silva, M. B. d., Zani, C. L.,
Siqueira, E. P. d., and Peres, R. L.: Antifungal activity of extracts from
<i>Piper aduncum</i> leaves prepared by different solvents and extraction techniques against
dermatophytes <i>Trichophyton rubrum</i> and <i>Trichophyton interdigitale</i>, Brazil. J. Microbiol., 44, 1275–1278, 2013.
</mixed-citation></ref-html>
<ref-html id="bib1.bib28"><label>28</label><mixed-citation>
Taylor, L.: Technical data report for matico (<i>Piper aduncum</i>,
<i>angustifolium</i>), available at:
<a href="http://www.rain-tree.com/reports/matico-tech-report.pdf" target="_blank">http://www.rain-tree.com/reports/matico-tech-report.pdf</a>  (last access: 30
November 2016), 2006.
</mixed-citation></ref-html>
<ref-html id="bib1.bib29"><label>29</label><mixed-citation>
Valderrama, X., Robinson, J. G., Attygalle, A. B., and Eisner, T.: Seasonal
anointment with millipedes in a wild primate: a chemical defense against
insects?, J. Chem. Ecol., 26, 2781–2790, 2000.
</mixed-citation></ref-html>
<ref-html id="bib1.bib30"><label>30</label><mixed-citation>
Vila, R., Tomi, F., Mundina, M., Santana, A. I., Solís, P. N., Lopez
Arce, J. B., Iclina, B., José, L., Iglesias, J., and Gupta, M. P.:
Unusual composition of the essential oils from the leaves of <i>Piper aduncum</i>, Flavour
Frag. J., 20, 67–69, 2005.
</mixed-citation></ref-html>
<ref-html id="bib1.bib31"><label>31</label><mixed-citation>
Volpe, H. X., Fazolin, M., Garcia, R. B., Magnani, R. F., Barbosa, J. C.,
and Miranda, M. P.: Efficacy of essential oil of <i>Piper aduncum</i> against nymphs and adults
of <i>Diaphorina citri</i>, Pest Manageg. Sci.,  76, 1242–1249, <a href="https://doi.org/10.1002/ps.4143" target="_blank">https://doi.org/10.1016/10.1002/ps.4143</a>, 2015.
</mixed-citation></ref-html>
<ref-html id="bib1.bib32"><label>32</label><mixed-citation>
Weldon, P. J., Aldrich, J. R., Klun, J. A., Oliver, J. E., and Debboun, M.:
Benzoquinones from millipedes deter mosquitoes and elicit self-anointing in
capuchin monkeys (<i>Cebus </i>spp.), Naturwissenschaften, 90, 301–304, 2003.
</mixed-citation></ref-html>
<ref-html id="bib1.bib33"><label>33</label><mixed-citation>
Wilson, N., Dietz, J. M., and Whitaker Jr., J. O.: Ectoparasitic Acari found
on golden lion tamarins (<i>Leontopithecus rosalia rosali</i>a) from Brazil, J. Wildlife Dis., 25,
433–435, 1989.
</mixed-citation></ref-html>
<ref-html id="bib1.bib34"><label>34</label><mixed-citation>
Wright, P. C., Arrigo-Nelson, S. J., Hogg, K. L., Bannon, B., Morelli, T.
L., Wyatt, J., Harivelo, A. L., and Ratelolahy, F.: Habitat disturbance and
seasonal fluctuations of lemur parasites in the rain forest of Ranomafana
National Park, Madagascar, in: Primate parasite ecology: the dynamics and
study of host-parasite relationships, edited by: Huffman, M. A. and
Chapman, C. A., Cambridge University Press, Cambridge, 311–330, 2009.
</mixed-citation></ref-html>
<ref-html id="bib1.bib35"><label>35</label><mixed-citation>
Zito, M., Evans, S., and Weldon, P. J.: Owl monkeys (<i>Aotus</i> spp.) self-anoint with
plants and millipedes, Folia Primatol., 74, 159–161, 2003.
</mixed-citation></ref-html>--></article>
