<?xml version="1.0" encoding="UTF-8"?>
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<article xmlns:xlink="http://www.w3.org/1999/xlink" xmlns:mml="http://www.w3.org/1998/Math/MathML" xmlns:oasis="http://docs.oasis-open.org/ns/oasis-exchange/table" xml:lang="en" dtd-version="3.0"><?xmltex \bartext{Short communication}?>
  <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-7-13-2020</article-id><title-group><article-title>Unintended importation of tropical jumping spiders (Salticidae) into a laboratory monkey<?xmltex \hack{\break}?> colony via banana supply</article-title><alt-title>Unintended importation of tropical spiders via banana supply</alt-title>
      </title-group><?xmltex \runningtitle{Unintended importation of tropical spiders via banana supply}?><?xmltex \runningauthor{R. Plesker and J. Berger}?>
      <contrib-group>
        <contrib contrib-type="author" corresp="yes" rid="aff1">
          <name><surname>Plesker</surname><given-names>Roland</given-names></name>
          <email>roland.plesker@pei.de</email>
        </contrib>
        <contrib contrib-type="author" corresp="no" rid="aff2">
          <name><surname>Berger</surname><given-names>Jürgen</given-names></name>
          
        </contrib>
        <aff id="aff1"><label>1</label><institution>Paul-Ehrlich-Institut, Paul-Ehrlich-Str. 51-59, 63225
Langen, Germany</institution>
        </aff>
        <aff id="aff2"><label>2</label><institution>Max-Planck-Institut für Entwicklungsbiologie, Tübingen,
Germany</institution>
        </aff>
      </contrib-group>
      <author-notes><corresp id="corr1">Roland Plesker (roland.plesker@pei.de)</corresp></author-notes><pub-date><day>4</day><month>September</month><year>2020</year></pub-date>
      
      <volume>7</volume>
      <issue>2</issue>
      <fpage>13</fpage><lpage>17</lpage>
      <history>
        <date date-type="received"><day>19</day><month>June</month><year>2020</year></date>
           <date date-type="rev-recd"><day>28</day><month>July</month><year>2020</year></date>
           <date date-type="accepted"><day>3</day><month>August</month><year>2020</year></date>
      </history>
      <permissions>
        <copyright-statement>Copyright: © 2020 Roland Plesker</copyright-statement>
        <copyright-year>2020</copyright-year>
      <license license-type="open-access"><license-p>This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit <ext-link ext-link-type="uri" xlink:href="https://creativecommons.org/licenses/by/4.0/">https://creativecommons.org/licenses/by/4.0/</ext-link></license-p></license></permissions><self-uri xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020.html">This article is available from https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020.html</self-uri><self-uri xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020.pdf">The full text article is available as a PDF file from https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020.pdf</self-uri>
      <abstract><title>Abstract</title>
    <p id="d1e95">This report describes a case of unintended importation of tropical baby
jumping spiders to a laboratory monkey colony. The spiders were detected in
a cocoon attached to a banana for monkey consumption. In identifying the
family of spiders as jumping spiders (Salticidae), it turned out that these spiders
would not have been venomous to humans and they most likely would not have
had the potential to establish a new spider colony in the facility.</p>
  </abstract>
    </article-meta>
  </front>
<body>
      

<sec id="Ch1.S1" sec-type="intro">
  <label>1</label><title>Introduction and literature</title>
      <p id="d1e107">In a laboratory monkey colony, food is not only used as the necessary
fulfilment of nutritional needs of the monkeys, but it is also an important
tool in environmental enrichment (Newberry, 1995). In addition, food is used
in training procedures (Westlund, 2015). Therefore, often not only pellets
are offered to the monkeys, but also fruits and vegetables to make life more
interesting for the animals in a laboratory setting.</p>
      <p id="d1e110">These fruits and vegetables are often delivered from a central market, where
fruits and vegetables are offered for human consumption. Sometimes, the
covering boxes <?xmltex \hack{\mbox\bgroup}?>unintendedly<?xmltex \hack{\egroup}?> contain unwanted domestic vermin (Plesker,
2005). In addition, on the internet as well as in newspapers and in scientific
literature, reports are given
on the appearance of unwanted animals –
mostly spiders – in bulks of fruits (often bananas or grapes), originating
from tropical countries  (Nentwig, 2015; Vetter et al., 2014; Bosselaers,
2013; Nentwig and Kobelt, 2010; Van Keer, 2010, 2007; Reed, 2004).
This happens although, for example, bananas are washed and disinfected
before packing, cooled during transportation, and treated with ethene before
they reach the markets.</p>
      <p id="d1e117">In principle, every spider with venom glands must be considered as venomous,
not always for humans, but also for other animals or insects (Maretic, 1987).
However, only few spiders are of medical and veterinary importance (Mullen and
Vetter, 2019; Vetter and Isbister, 2008; Wilson and King, 1990). Despite this
fact, internet and newspaper reports often deal with the possibility that the
imported individuals might be venomous to humans (e.g.
<uri>https://www.nationalgeographic.com/news/2014/11/141110-spiders-bananas-fruit-food-world-toxic-animals/</uri>, last access: 31 August 2020). As a consequence of
these reports, when imported spiders are detected, the fear often arises
that they might be venomous to humans (Lucas and Meier, 2017; White, 2000;
Maretic, 1987).</p>
      <p id="d1e123">In order to raise the awareness of the problem of importing unwanted
tropical spiders via food supply for persons in contact with laboratory
primates, we here report a case of importation of tropical spiders
(Salticidae) via bananas to our colony.</p>
</sec>
<sec id="Ch1.S2">
  <label>2</label><title>Material and methods</title>
      <p id="d1e134">The monkey colony currently contains 12 African green monkeys
(<italic>Chlorocebus aethiops</italic>), 7 pig-tailed macaques (<italic>Macaca nemestrina</italic>) and 2 rhesus macaques (<italic>Macaca mulatta</italic>) for experimental,
vaccine-related research.</p>
      <?pagebreak page14?><p id="d1e146">At the institute, the monkeys are housed in groups in an indoor area with controlled access. There
is only one monkey species per room. The cages are made of steel with a
basic size of <inline-formula><mml:math id="M1" display="inline"><mml:mrow><mml:mn mathvariant="normal">300</mml:mn><mml:mspace linebreak="nobreak" width="0.125em"/><mml:mrow class="unit"><mml:mi mathvariant="normal">cm</mml:mi></mml:mrow><mml:mo>×</mml:mo><mml:mn mathvariant="normal">375</mml:mn><mml:mspace linebreak="nobreak" width="0.125em"/><mml:mrow class="unit"><mml:mi mathvariant="normal">cm</mml:mi></mml:mrow><mml:mo>×</mml:mo><mml:mn mathvariant="normal">225</mml:mn><mml:mspace linebreak="nobreak" width="0.125em"/><mml:mrow class="unit"><mml:mi mathvariant="normal">cm</mml:mi></mml:mrow></mml:mrow></mml:math></inline-formula> (or up to triple the size). Large
windows allow the monkeys to observe the outside environment. Natural
branches, ropes, nets, bedding, mirrors, KONG toys, puzzle feeders, Prima-Hedrons, music and television are supplied for environmental enrichment.
The housing is in accordance with European and German animal welfare
legislation.</p>
      <p id="d1e177">The monkeys' diet in our colony consists of monkey pellets ad libitum (Trio
Munch<sup>®</sup>, Special Diet Services/Mazuri, Witham,
England) in the morning and seasonal vegetables and fruits twice weekly in
the afternoon. Some fruits (like bananas) are not peeled off before they are
offered to the monkeys, in order to keep the monkeys busy with the food.</p>
      <p id="d1e183">The bananas in this case were delivered from the Frankfurt
central food market via a local fruit dealer. Their origin could be traced
back to a food dealer in Medellín, Colombia, with the help of information
given on a label of the covering carton.</p>
      <p id="d1e187">When bananas reach the institute, they
are routinely unpacked from the cartons, visually inspected and stored in a
refrigerator until use. This happens inside the monkey unit, in a
separate kitchen.</p>
      <p id="d1e190">When the particular banana was detected in this case, first, pictures were
taken. The banana was then placed into an air-tight glass filled with a
4 % formaldehyde solution to prevent the spread of vermin. After 24 h,
the cocoon was opened and, again, pictures were taken. Individual baby
spiders were then photographed and identified using a stereomicroscope
(Zeiss Stemi 2000-C, Oberkochen, Germany) together with a digital camera
(AxioCam Color, Oberkochen, Germany).</p>

      <?xmltex \floatpos{t}?><fig id="Ch1.F1"><?xmltex \currentcnt{1}?><label>Figure 1</label><caption><p id="d1e195">Banana delivered with a spider cocoon on the surface (scale bar <inline-formula><mml:math id="M2" display="inline"><mml:mo>=</mml:mo></mml:math></inline-formula> 4 cm).</p></caption>
        <?xmltex \igopts{width=236.157874pt}?><graphic xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020-f01.jpg"/>

      </fig>

      <p id="d1e211">After washing, the formalin-fixed spiders were
dehydrated in a graduated series of ethanol followed by
critical point drying with <inline-formula><mml:math id="M3" display="inline"><mml:mrow class="chem"><mml:msub><mml:mi mathvariant="normal">CO</mml:mi><mml:mn mathvariant="normal">2</mml:mn></mml:msub></mml:mrow></mml:math></inline-formula> in a critical point dryer (Polaron E
3000, Polaron Equipment Ltd, Watford, UK). Finally, the spiders were
sputter coated with a 10 nm layer of Au / Pd (Bal-Tec MED 010, Balzers Union
AG, Balzers, Liechtenstein) and examined with a Hitachi S-800 field emission
scanning electron microscope (Hitachi High-Tech Europe GmbH, Krefeld,
Germany) at an accelerating voltage of 15 kV.</p>
</sec>
<sec id="Ch1.S3">
  <label>3</label><title>Results</title>
      <p id="d1e233">When taken out of the covering carton, a flat oval
beige-white cocoon (5 cm <inline-formula><mml:math id="M4" display="inline"><mml:mo>×</mml:mo></mml:math></inline-formula> 2.5 cm) was discovered on the surface of one banana
(Fig. 1). Within the cocoon, one could adumbrate multiple small black
silhouettes. Unfortunately, we could not confirm whether these
silhouettes were
moving or not.</p>
      <p id="d1e243">When the cocoon was opened after 24 h of formaldehyde fixation,
approximately 100 well-preserved black baby spiders became visible (Fig. 2). They were up to 4 mm in body length. Their black body was divided into a
larger (two-thirds) more rectangular prosoma (cephalothorax) and a smaller
(one-third) oval opisthosoma (abdomen). Both were separated by a slim
petiolus. In front and on the dorsal part, the prosoma contained eight eyes
(four pairs) of different sizes, with the anterior median pair of eyes being
the largest. Four pairs of ochre haired legs were seen in a prograde
position (two legs to the front, two legs to the back). On the dorsal part
of the abdomen, prominent white hairs were located in two double lines
(Fig. 3). These characteristics identified the baby spiders as members of
the family of jumping spiders (Salticidae). Unfortunately, since all individuals were
babies, it was not possible to further determine a particular genus or
species.</p>
      <p id="d1e246">In scanning electron microscopy, the spiders
displayed flat faces with a large anterior median pair of eyes (Fig. 4) and
small posterior median eyes. The legs contained no spines.</p>

      <?xmltex \floatpos{t}?><fig id="Ch1.F2"><?xmltex \currentcnt{2}?><label>Figure 2</label><caption><p id="d1e252">Closer view of an opened spider cocoon at the surface of a banana after formalin fixation: about 100 black individuals (scale bar <inline-formula><mml:math id="M5" display="inline"><mml:mo>=</mml:mo></mml:math></inline-formula> 1 cm).</p></caption>
        <?xmltex \igopts{width=236.157874pt}?><graphic xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020-f02.jpg"/>

      </fig>

      <?xmltex \floatpos{t}?><fig id="Ch1.F3"><?xmltex \currentcnt{3}?><label>Figure 3</label><caption><p id="d1e270">Single tropical baby spider of a cocoon on a banana surface: note the larger rectangular cephalothorax and the smaller oval abdomen (0.4 cm in total body length).</p></caption>
        <?xmltex \igopts{width=236.157874pt}?><graphic xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020-f03.jpg"/>

      </fig>

</sec>
<?pagebreak page15?><sec id="Ch1.S4">
  <label>4</label><title>Discussion</title>
      <p id="d1e287">If spiders are found in boxes of imported bananas, the first impulse is to
call them “banana spiders” and to assume that they are venomous to humans.
However, two out of the three types of “typical” banana spiders are not
dangerous: the golden silk orb weaver (<italic>Nephila</italic>) and the Hawaiian garden spider
(<italic>Argiope appensa)</italic>. Only the Brazilian wandering spider (<italic>Phoneutria nigriventer</italic>) is venomous. However, it is
obvious that the spiders presented in this case do not belong to these
larger banana spiders; they belong to the family of the jumping spiders
(Salticidae).</p>
      <p id="d1e299">The family of jumping spiders is very large and contains currently about 600
genera and 6000 species. This means this family covers 13 % of all
spiders. They can easily be identified by their rectangular cephalothorax,
their large anterior median pair of eyes, their flat faces and the missing
spines on the legs (Richman et al., 2005).</p>

      <?xmltex \floatpos{t}?><fig id="Ch1.F4"><?xmltex \currentcnt{4}?><label>Figure 4</label><caption><p id="d1e304">Scanning electron microscopical image of a baby spider from a cocoon on a banana: large anterior median pair of eyes indicating jumping spiders
(Salticidae).</p></caption>
        <?xmltex \igopts{width=236.157874pt}?><graphic xlink:href="https://pb.copernicus.org/articles/7/13/2020/pb-7-13-2020-f04.jpg"/>

      </fig>

      <p id="d1e314">When the cocoon was first discovered, it was intuitively assumed that
spiders might be inside. In addition, three questions for our institution
were raised immediately:
<list list-type="order"><list-item>
      <p id="d1e319">Is there a possibility that the spiders might leave the cocoon?</p></list-item><list-item>
      <p id="d1e323">Are these spiders venomous to humans/the staff?</p></list-item><list-item>
      <p id="d1e327">Is there a possibility that the spiders might establish a spider colony
within the animal unit?</p></list-item></list>
In order to rigorously exclude any of these possibilities, the banana was
deposited in formaldehyde solution and in an air-tight glass. However, due
to this reflex, we were unable to find out whether the baby spiders within
the cocoon were alive or already dead at the time of discovery. However, the
very good preservation of their bodies might be a hint that they might still
have been alive when the bananas entered the animal unit. So, probably, they
would have had the potential to leave the cocoon under appropriate
conditions. Since, in our case, the kitchen where the fruits and vegetables
are unpacked and handled is part of the monkey unit, it is absolutely
realistic to be concerned about a potential spread of imported spiders in
the whole area.</p>
      <p id="d1e331">When the spiders were identified as jumping baby spiders, it was clear that
they would not have been venomous to humans since jumping spiders in
general are not venomous to humans (Mullen and Vetter, 2019; Vetter and
Isbister, 2008). In addition, it seems to be unlikely that these jumping
spiders would have had the potential to establish a new spider colony within
the animal unit, since – with the spiders originating from a banana
plantation in Columbia – the climate in the animal unit would not be moist
enough. In addition, daily cleaning in the facility would reduce both the
amount of available food for the spiders and the number of places to hide.
Finally, living as a spider in a monkey room would not be desirable,
since monkeys have the tendency to grasp and consume anything that moves. In addition, the grooming behaviour among monkeys would increase
the risk of being detected and consumed.</p>
      <p id="d1e334">When a cocoon is discovered on a banana, it must be considered whether the
cocoon was attached to the fruit in the banana plantation itself or whether
it was secondarily<?pagebreak page16?> attached to the banana during transportation. In
principle, spiders have been detected in banana plantations (Harrison, 1968),
and the first author himself has seen similar cocoons on banana bunches in
Vietnam. Therefore, the attachment definitely could have happened in the
banana plantation itself. On the other hand, ships as well as (more modern)
containers are cleaned (and in part disinfected) on a regular basis; this
makes it unlikely for the cocoon to be attached to the banana during
transportation.</p>
      <p id="d1e337">Since this report documents the occurrence of tropical spiders in banana
cartons delivered from food markets in Germany, it stresses the following:
<list list-type="custom"><list-item><label>a.</label>
      <p id="d1e342">the need for a separate “arrival” room for incoming fruits and vegetables,</p></list-item><list-item><label>b.</label>
      <p id="d1e346">the need for the proper storage of fruits and vegetables until they are
consumed,</p></list-item><list-item><label>c.</label>
      <p id="d1e350">consistent peeling and washing of fruits and vegetables,</p></list-item><list-item><label>d.</label>
      <p id="d1e354">the need for an accurate visual control of fruits and vegetables (especially
bananas and grapes) before offering them to the animals.</p></list-item></list></p>
</sec>
<sec id="Ch1.S5" sec-type="conclusions">
  <label>5</label><title>Conclusions</title>
      <p id="d1e366">This report describes a case of unintended importation of baby jumping
spiders attached to a banana to a laboratory monkey colony. In identifying
the family of spiders as jumping spiders (Salticidae), it turned out that
these spiders would not have been venomous to humans and they most likely
would not have had the potential to establish a new spider colony in the
facility. This finding stresses the importance of accurate visual control
and storage of vegetables and fruits reaching laboratory animal colonies.</p>
</sec>

      
      </body>
    <back><notes notes-type="dataavailability"><title>Data availability</title>

      <p id="d1e373">Pictures of the spiders are available via the corresponding author.</p>
  </notes><notes notes-type="authorcontribution"><title>Author contributions</title>

      <p id="d1e379">RP performed the literature research, the spider description and the
discussion. JB performed the scanning electron microscopy.</p>
  </notes><notes notes-type="competinginterests"><title>Competing interests</title>

      <p id="d1e385">The authors declare that they have no conflict of interest.</p>
  </notes><ack><title>Acknowledgements</title><p id="d1e391">The work was carried out at the Paul-Ehrlich-Institut in Langen and at the
Max-Planck-Institut für <?xmltex \hack{\mbox\bgroup}?>Entwicklungsbiologie<?xmltex \hack{\egroup}?>, Tübingen.</p></ack><notes notes-type="reviewstatement"><title>Review statement</title>

      <p id="d1e400">This paper was edited by Eberhard Fuchs and reviewed by Alf Theisen and Stefan Schlatt.</p>
  </notes><ref-list>
    <title>References</title>

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<abstract-html><p>This report describes a case of unintended importation of tropical baby
jumping spiders to a laboratory monkey colony. The spiders were detected in
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had the potential to establish a new spider colony in the facility.</p></abstract-html>
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