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357
http://journals.tubitak.gov.tr/zoology/
Turkish Journal of
Zoology Turk J Zool
(2013) 37: 357-361
© TÜBİTAK
doi:10.3906/zoo-1210-9
First record of the schizomid Stenochrus portoricensis
(Schizomida: Hubbardiidae) in Poland, with DNA barcode data
Krzysztof ZAWIERUCHA1, Paweł SZYMKOWIAK1,*, Miroslawa DABERT2, Mark Stephen HARVEY3
1
Department of Animal Taxonomy and Ecology, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
2
Molecular Biology Techniques Laboratory, Faculty of Biology, Adam Mickiewicz University, Umultowska 89, 61-614 Poznań, Poland
3
Department of Terrestrial Zoology, Western Australian Museum, Welshpool DC, Western Australia 6986, Australia
* Correspondence: pawel.szymkowiak@amu.edu.pl
1. Introduction
Many dierent types of arachnids have successfully
dispersed to new locations around the globe via passive
associations with humans. e majority of these successful
introductions result from their predatory lifestyle and
their predominance in terrestrial habitats (Nedvĕd et
al., 2011). Some species are able to become acclimatized
to their new situation and live in natural or seminatural
environments. Others, however, cannot survive without
environmental conditions that mimic their original habitat,
of which greenhouses represent the most obvious example.
Greenhouses create adequate conditions (temperature,
light, moisture, and soil) and protected habitats for the
acclimatization of alien species. Moreover, in the absence
of natural enemies and pathogens, alien species are capable
of developing and spreading successfully (Teodorescu and
Matei, 2010). Among 3805 species of known arachnids
inhabiting natural environments in Poland, only 10 are
considered to be alien species (Głowaciński and Pawłowski,
2010). e rst comprehensive studies of the alien arachnids
(including only Acari) of greenhouses in Poland took place
in upper Silesia. Skubała et al. (2001) revealed that only
13% of the detected mites (Oribatida) were alien species. In
contrast, approximately 50% of the ptyctimous mites in the
Poznań Palm House were alien (Niedbała, 2010).
e Palm House in Poznań was founded in 1910–1911.
e plant collection contains more than 1000 species.
At present, the Palm House is divided into 9 pavilions
where representatives of dierent groups of vegetation are
displayed (e.g., tropical, subtropical, temperate, aquatic).
Specimens of Stenochrus portoricensis were found in
pavilions with tropical rainforest undergrowth vegetation.
e plants in the Palm House have been imported from
other greenhouses located in Poland, as well as from
the Netherlands, Germany, and from natural habitats
elsewhere, e.g., Copernicia macroglossa H. Wendl. ex
Becc. from Cuba. e rst studies on the invertebrate
fauna of the Poznań Palm House were performed in
1932 by Moszyński and Urbański, whose ndings were
extended by other researchers. e studies focused on
fauna in general (Urbański, 1950; Brzezińska, 1952),
on soil fauna (Michalak, 2006), and on individual taxa:
Isopoda (Urbański, 1947), Formicidae (Pisarski, 1957),
Araneae and Opiliones (Woźniczko, 1966), Turbellaria
and Nemeritini (Kolasa, 1973), aquatic Oligochaeta
(Legeżyński, 1974), and ptyctimous mites (Niedbała,
2010). Additionally, Wiśniewski and Hirschmann (1991a,
1991b) described 3 new species of mites. Although 12
papers on the invertebrate fauna of the Poznań Palm
House have been published so far, our knowledge of the
biodiversity of the greenhouses in general is still very poor.
Abstract: Several specimens of the tropical schizomid Stenochrus portoricensis Chamberlin, 1922 (family Hubbardiidae) were found in
the Poznań Palm House, representing the rst record of micro-whip scorpions (Schizomida) from Poland. Stenochrus portoricensis is an
alien species in temperate climates, and has been accidentally introduced to greenhouses via potted plants. Its parthenogenetic lifestyle
allows for the easy transfer of populations to new locations and the successful founding of new colonies. New DNA sequence data for
Stenochrus portoricensis are presented, which comprise a fragment of the cytochrome c oxidase subunit I gene (DNA barcode sequence)
from mitochondrial DNA, and a fragment of the 28S rRNA gene (D1–D3 regions) from nuclear DNA.
Key words: Micro-whip scorpions, alien species, articial habitat, greenhouse, introduced animals, DNA barcode, COI, 28S rDNA
Received: 11.10.2012 Accepted: 19.01.2013 Published Online: 29.04.2013 Printed: 29.05.2013
Research Article
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ZAWIERUCHA et al. / Turk J Zool
During further investigations into the invertebrate fauna
of the Palm House, several specimens of schizomids were
found amongst leaf litter and rotting wood. Schizomida,
also known as micro-whip scorpions, are small arachnids
mainly inhabiting the tropical and subtropical regions
of the world (Reddell and Cokendolpher, 1995; Harvey,
2003; Beccaloni, 2009). Currently, the order contains 286
species in 53 genera (updated from Harvey, 2003, 2007),
but only 3 species have been reported from Europe, and all
3 represent exotic introductions. Schizomus crassicaudatus
(O.P. Cambridge, 1872) was originally described from Sri
Lanka and later recorded from greenhouses in the Muséum
national d’Histoire naturelle, Paris, France (Simon, 1896).
Zomus bagnallii (Jackson, 1908) was originally described
from greenhouses in the Royal Botanic Gardens, Kew,
England (Jackson, 1908), and has since been found to
be widespread throughout the Indo-Pacic region (e.g.,
Reddell and Cokendolpher, 1995; Harvey, 2001, 2010;
Villarreal, 2010). Stenochrus portoricensis Chamberlin,
1922 is widespread throughout tropical North and South
America, ranging from Florida to southeastern Brazil (e.g.,
Rowland and Reddell, 1980; Reddell and Cokendolpher,
1995; Harvey, 2003; Santos et al., 2008), with populations
also recorded from the Canary Islands, United Kingdom,
and the Czech Republic (Cloudsley-ompson, 1949;
Oromi and Martin, 1992; Reddell and Cokendolpher,
1995; Korenko et al., 2009; Sentenská and Líznarová,
2010). Jackson (1910) reported on an apparently new
species of schizomid from a hothouse in Penrith, northern
England, the identity of which has not yet been conrmed.
It is likely to also be a population of S. portoricensis.
e specimens collected in Poznań represent the rst
record of the order Schizomida from Poland. Apart from
recording their presence, we also report on newly obtained
mitochondrial and nuclear molecular sequence data of S.
portoricensis.
2. Materials and methods
2.1. Materials
Twenty-four specimens of S. portoricensis were collected
from soil, wood, and leaf litter by handpicking, sieving, and
Barber pitfall sampling in 3 pavilions containing tropical
vegetation in the Poznań Palm House. All specimens were
preserved in 75% ethanol, and are now deposited in the
Department of Animal Taxonomy and Ecology, Adam
Mickiewicz University, Poznań, Poland (AMUP), and the
Western Australian Museum, Perth, Australia (WAM).
2.2. Molecular methods
We selected the 3 best preserved specimens from which
to obtain sequence data. Total genomic DNA was
extracted from the specimens using a nondestructive
method, as described by Dabert et al. (2008). A 681-bp
fragment of the mitochondrial cytochrome c oxidase
subunit I (COI) gene was amplied with primers bcdF01
(5’-CATTTTCHACTAAYCATAARGATATTGG-3’) and
bcdR04 (5’-TATAAACYTCDGGATGNCCAAAAAA-3’)
(Dabert et al., 2010); an 850-bp fragment of the nuclear
28S rDNA was amplied with primers 28SF0001
(5’-ACCCVCYNAATTTAAGCATAT-3’) and 28SR0990
(5’-CCTTGGTCCGTGTTTCAAGAC-3’) (Mironov et al.,
2012). PCRs were carried out in 5-µL reaction volumes
containing 2.5 µL Type-it Microsatellite PCR Kit (Qiagen,
Hilden, Germany), 0.25 µM of each primer, and 1 µL of
DNA template, using a thermocycling prole of 1 cycle of
5 min at 95 °C followed by 35 steps of 30 s at 95 °C, 90 s at
50 °C, 1 min at 72 °C, with a nal step of 5 min at 72 °C.
Aer amplication, the PCRs were diluted with 10 µL of
water, and 5 µL of the diluted PCR reaction was analyzed
by electrophoresis on a 1% agarose gel. e amplicons
were directly sequenced in the forward direction by using
1 µL of the PCR reaction and 50 pmol of sequencing
primer. Sequencing was performed with a BigDye
Terminator (v. 3.1) on an ABI Prism 3130XL Analyzer
(Applied Biosystems). Contigs were aligned and manually
assembled in ChromasPro v. 1.32 (Technelysium Pty,
Ltd.), and converted to amino acids in GeneDoc v. 2.7.000
(Nicholas and Nicholas, 1997). e resulting sequences
were compared with the GenBank database (blast.ncbi.
nlm.nih.gov) using the blastn and discontiguous megablast
programs (Zhang et al., 2000).
3. Results
Stenochrus portoricensis Chamberlin, 1922
(Figures 1, 2, 3)
Stenochrus portoricensis Chamberlin, 1922: 11–12.
Schizomus antilus Hilton, 1933: 91–92 (synonymized
by Rowland and Reddell, 1980: 14).
Schizomus cavernicolens Chamberlin and Ivie, 1938:
102, gures 4–7 (synonymized by Rowland and Reddell,
1977: 87).
1000 µm
Figure 1. Stenochrus portoricensis dorsal view.
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ZAWIERUCHA et al. / Turk J Zool
Schizomus oridanus Muma, 1967: 18–20, gures 13–
15 (synonymized by Rowland and Reddell, 1977: 87).
Schizomus longimanus Rowland, 1971: 119–120,
gures 4–6, 17 (synonymized by Rowland and Reddell,
1977: 87).
Schizomus loreto Armas, 1977: 5–7, gures 3, 4a–d
(synonymized by Armas, 1989: 23).
Full synonymy to 2002 can be found in Harvey, 2003:
125.
Specimens examined: POLAND: Poznań Palm House
(pavilions: V, VI, and VIII), January–April 2012, 18
specimens (11 females and 7 juveniles) in AMUP and 6
specimens (1 female and 5 juveniles) in WAM.
Diagnosis: Stenochrus portoricensis diers from all
other species of the genus, except S. davisi (Gertsch, 1940),
S. guatemalensis (Chamberlin, 1922), S. leon Armas,
1995, S. mexicanus (Rowland, 1971), S. mulaiki (Gertsch,
1940), S. palaciosi (Reddell and Cokendolpher, 1986), S.
pecki (Rowland, 1973), and S. reddelli (Rowland, 1971),
by the presence of only 2 pairs of dorsal propeltidial setae.
Females can be distinguished from those of these species
by the heavily sclerotized median spermathecae, which are
visible through the cuticle of sternite II, and males by seta
dm4 of the agellum being situated on approximately the
same level as dl1 (Rowland and Reddell, 1980; Reddell and
Cokendolpher, 1986; Armas, 1995).
Sequence data: We sequenced a 681-bp fragment of
the mitochondrial cytochrome c oxidase subunit I (COI)
gene (DNA barcode region chosen by the Consortium
for the Barcode of Life, http://barcoding.si.edu) and an
850-bp fragment of the nuclear 28S rDNA, including
the hypervariable D1–D3 regions of 3 females of S.
portoricensis (GenBank Acc. numbers JX280413–15,
JX280416, respectively). No intraspecic variation was
found in the COI nucleotide sequences, and no frame
shi was observed aer conversion of these sequences into
amino acids. Sequence data for S. portoricensis have been
previously reported for several gene regions (e.g., Giribet
and Ribera, 2000; Giribet et al., 2002; Regier et al., 2010),
but our data represent the rst records of DNA barcodes for
this species: a fragment of COI from mitochondrial DNA,
and hypervariable regions D1–D3 from 28S ribosomal
RNA gene. e sequences generated for S. portoricensis
showed nucleotide identities higher than 80% (COI)
and 90% (28S rDNA) compared to the other schizomid
sequences published in GenBank. One or both of these
genes have been obtained for other schizomids including
Hubbardia pentapeltis Cook, 1899 (Giribet et al., 2002),
Bamazomus sp., Brignolizomus woodwardi (Harvey, 1992),
Draculoides spp. and Paradraculoides spp. (Harvey et al.,
2008), and an unidentied schizomid (Arabi et al., 2012).
4. Discussion
e specimens of S. portoricen sis recorded from the Poznań
Palm House represent the rst record of this species
from Poland, and one of the few records of Schizomida
from Europe. Previous records include populations from
the Canary Islands (Oromi and Martin, 1992), United
Kingdom (Cloudsley-ompson, 1949; Reddell and
Cokendolpher, 1995), and the Czech Republic (Korenko
et al., 2009; Sentenská and Líznarová, 2010). While the
Canary Island population seems to be free-living in natural
ecosystems, the other records are conned to hothouses
and other articial habitats.
While many populations of S. portoricensis consist only
of females and juveniles, populations with adult males have
been reported from southern Mexico (Campeche, Chiapas,
and Yucatán states), Guatemala, Cuba, Dominican
1000 µm
Figure 2. Stenochrus portoricensis lateral view.
100 µm
Figure 3. Flagellum of Stenochrus portoricensis.
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ZAWIERUCHA et al. / Turk J Zool
Republic, and Puerto Rico (Armas, 1977; Rowland
and Reddell, 1980; Reddell and Cokendolpher, 1995).
Like the European and Brazilian populations, it seems
likely that many other populations represent accidental
introductions, presumably originally stemming from a
bisexual Central American source. e lack of males from
most populations led Reddell and Cokendolpher (1995) to
suggest that S. portoricensis is a facultative parthenogen.
A parthenogenetic lifestyle would also allow for the easy
transfer of populations to new locations as only single
female individuals, either adult or immature, would be
needed to found new colonies.
e occurrence of S. portoricensis in Poznań is likely
to have begun with soil and litter of plants introduced
into the Palm House from external sources, similar to
the hypothesis suggested by Tourinho and Kury (1999)
and Kobelt and Nentwig (2008), who claimed that alien
arachnids are most probably introduced with garden plants
and container shipments. Greenhouses constitute isolated,
inland islands for introduced local populations, and a
study using molecular data focusing on migration routes
of this species within Europe may prove benecial. e
molecular data presented in this paper of S. portoricensis
is a rst step in this process.
Acknowledgments
We wish to express our sincere thanks to members of the
Student Naturalist Society (Invertebrate Section) of Adam
Mickiewicz University for their assistance in the collection
of specimens. We also thank Michał Śmiłowski and the
sta of the Poznań Palm House for their kindness and
support during the collection of the samples. e present
study was partially supported by the Polish MSHE grant
No. N N303 017937.
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