Phytophagous mites (Acari: Eriophyoidea) recorded from Svalbard, including the description of a new species

Abstract

Eriophyoid mites (Eriophyoidea) are minute
phytophagous mites with great economic importance and
great invasive potential. In spite of their demonstrated
impact on ecosystem functions, knowledge of eriophyoid
mite fauna in the Arctic is lacking. To date, only eight
eriophyoid mite species have been recorded from the entire
region north of the Arctic Circle. The Svalbard archipelago
is one of the most biologically investigated Arctic areas.
Despite the fact that studies on invertebrates on Svalbard
have been conducted for more than one hundred years,
eriophyoids have never been recorded before from this
place, except for one likely accidental record of a single
specimen belonging to the genus Eriophyes. Thus, each
new study of eriophyoid mite fauna in this region is
important. In this paper, a new species of eriophyoid mite,
Cecidophyes siedleckii n. sp., is described and illustrated.
Nucleotide sequence data (D2 region of 28S rDNA) were
employed to complement traditional morphological taxonomy.
The first record of Aceria saxifragae (Rostrup
1900) from Svalbard is also provided, with supplementary
morphological descriptions and illustrations. Eriophyoid
mites represent an important and underutilized taxon that is
available to ecologists studying the effects of changing
climatic conditions on Svalbard.

Full text

ORIGINAL PAPER
Phytophagous mites (Acari: Eriophyoidea) recorded
from Svalbard, including the description of a new species
Agnieszka Kiedrowicz
1
•Brian G. Rector
2
•Krzysztof Zawierucha
1
•
Wiktoria Szydło
1
•Anna Skoracka
1
Received: 4 May 2015 / Revised: 20 November 2015 / Accepted: 3 December 2015 / Published online: 4 January 2016
ÓThe Author(s) 2016. This article is published with open access at Springerlink.com
Abstract Eriophyoid mites (Eriophyoidea) are minute
phytophagous mites with great economic importance and
great invasive potential. In spite of their demonstrated
impact on ecosystem functions, knowledge of eriophyoid
mite fauna in the Arctic is lacking. To date, only eight
eriophyoid mite species have been recorded from the entire
region north of the Arctic Circle. The Svalbard archipelago
is one of the most biologically investigated Arctic areas.
Despite the fact that studies on invertebrates on Svalbard
have been conducted for more than one hundred years,
eriophyoids have never been recorded before from this
place, except for one likely accidental record of a single
specimen belonging to the genus Eriophyes. Thus, each
new study of eriophyoid mite fauna in this region is
important. In this paper, a new species of eriophyoid mite,
Cecidophyes siedleckii n. sp., is described and illustrated.
Nucleotide sequence data (D2 region of 28S rDNA) were
employed to complement traditional morphological tax-
onomy. The first record of Aceria saxifragae (Rostrup
1900) from Svalbard is also provided, with supplementary
morphological descriptions and illustrations. Eriophyoid
mites represent an important and underutilized taxon that is
available to ecologists studying the effects of changing
climatic conditions on Svalbard.
Keywords Arctic biology Eriophyidae Extreme
environments Molecular taxonomy Herbivorous mites 
DNA barcoding
Introduction
In polar regions, invertebrates occupy virtually all eco-
logical niches, from the deep ocean floor to the surfaces
of glaciers, including extreme environments, such as
nunataks, tundra, and polar deserts, and they often con-
stitute significant components of these harsh ecosystems
(e.g., Dastych 1985; Janiec 1996; Dastych and Drummond
1996; Porazin
´ska et al. 2004; Coulson et al. 2014b;
Go
´rska et al. 2014; Zawierucha et al. 2015). The past two
decades have seen a rapid increase in research interest
toward invertebrates in the Svalbard archipelago (e.g.,
Lippert et al. 2001; Coulson et al. 2003,2014a; Johnsen
et al. 2014; Pilskog et al. 2014; Zawierucha et al. 2015).
Currently, the terrestrial invertebrate fauna of Svalbard
consists of over 1000 species (Coulson et al. 2014b), and
invertebrates are still being discovered in this region as
both new records and new species to science (e.g.,
Kaczmarek et al. 2012; Zawierucha 2013; Zawierucha
et al. 2013; Dabert et al. 2014; Coulson et al. 2014a,b;
Coulson et al. 2015). However, while the invertebrate
fauna of Svalbard is among the best known for any Arctic
region (Hodkinson 2013), only about 115 mite (Acari)
species have been recorded so far from the Svalbard
archipelago, with the majority of them being soil-inhab-
iting Mesostigmata and Oribatida (Coulson et al. 2014b).
Mites occupy almost every habitat on Earth and are an
important component of every environment. Many mite
species have evolved in associations with other organisms
(i.e., plant or animal hosts) that function as their
&Agnieszka Kiedrowicz
kiedra@amu.edu.pl
1
Department of Animal Taxonomy and Ecology, Institute of
Environmental Biology, Adam Mickiewicz University,
Umultowska 89, 60-687 Poznan
´, Poland
2
USDA-ARS, Great Basin Rangelands Research Unit,
920 Valley Road, Reno, NV 89512, USA
123
Polar Biol (2016) 39:1359–1368
DOI 10.1007/s00300-015-1858-x
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permanent or temporary habitats (Walter and Proctor
2013). Studies of parasitic or phytophagous organisms can
provide insights into ecosystem functions. On Svalbard,
for example, a thorough understanding of the biotic con-
straints to the proliferation and spread of plant species,
particularly non-native species, is important when con-
sidering their ability to compete for available habitat with
other plant species.
Previous studies on the parasitic invertebrates in the
Svalbard archipelago have focused mostly on Nematoda,
Cestoda, Acanthocephala, and Insecta (e.g., Hackman and
Nyholm 1968; Halvorsen and Bye 1999; Kuklin et al.
2004; Stien et al. 2010), while a few studies have focused
on parasitic Acari associated with birds (Gwiazdowicz
et al. 2012; Dabert et al. 2014) and polyphagous Bryobia
species (Coulson and Refseth 2004). Among phytophagous
mites, only two species, both Tetranychidae (viz., Bryobia
borealis Oudemans, 1930, and Bryobia praetiosa Koch,
1836), have been recorded from Svalbard (Summerhayes
and Elton 1928;Thor1930,1934; MacFadyen 1954;
Coulson and Refseth 2004), notwithstanding the well-de-
scribed flora of the Svalbard archipelago, which includes
173 recorded vascular plant species, as well as 373 moss
and 597 lichen species (Jo
´nsdo
´ttir 2005). Only one plant-
feeding mite in the family Eriophyidae has ever been
recorded from Svalbard, a possibly accidental record of a
single specimen belonging to the genus Eriophyes (Thor
1934). In that case, neither the mite species nor its host
plant were identified.
The eriophyoid mites are among the most economically
important groups of phytophagous Acari (Lindquist and
Amrine 1996). They cause direct damage to their host
plants and often transmit plant viruses (Duso et al. 2010).
Moreover, they have great invasive potential (Navia et al.
2010) due to their ability to spread undetected via wind-
borne or human-mediated dispersal (Michalska et al.
2010). Given that the Arctic tundra is influenced by cli-
mate change (e.g., Walkera et al. 2006; Coulson 2013),
greater knowledge of new phytophagous organisms and
potential vectors of plant disease in this region is urgently
needed.
Eriophyoid mite identification is often hampered by
their minute size and structural simplicity (Lindquist and
Amrine 1996), as well as the occurrence of cryptic lineages
(Skoracka et al. 2012,2013,2014; Miller et al. 2013). In
this paper, we describe a new species of eriophyoid plant-
feeding mite, Cecidophyes siedleckii n. sp., using DNA
data (D2 region of 28S rDNA) to complement traditional
morphological taxonomy. In addition, we provide the first
record of Aceria saxifragae (Rostrup, 1900) from Svalbard
with supplementary morphological data to augment the
original description.
Materials and methods
A sample of Saxifraga oppositifolia L. 1753 was collected
in August 2011 from the northern coast of Hornsund,
Wedel Jarlsberg Land, near the Stanisław Siedlecki Polish
Polar Station ‘‘Hornsund’’ (Fig. 1). The plant was allowed
to dry slowly, and dried plant parts were examined in the
laboratory under a stereomicroscope (Olympus SZ40) to
check for the presence of eriophyoid mites or deformations
of plant tissues typical of some eriophyoid mite infestations
(e.g., galls and enlarged buds). The dried plant parts were
then soaked in water for several hours and then re-exam-
ined under a stereomicroscope. No plant deformations were
noted. During examination, all parts of plants were
destroyed to search for mites, including inside flowers and
buds. Several eriophyoid mite specimens were found in this
way; these were collected and mounted on microscope
slides in Heinze and Hoyer media according to a standard
protocol (de Lillo et al. 2010), and then studied taxonom-
ically using a phase-contrast microscope (Olympus BX41).
Morphological nomenclature follows Lindquist (1996),
data measurements follow de Lillo et al. (2010), and sys-
tematic classification follows Rostrup (1900), Liro (1940)
and Amrine et al. (2003). Measurements refer to the
lengths of a given structure in micrometers unless other-
wise stated. In the description of the new species, the
holotype female measurement precedes the corresponding
range for paratypes (given in parentheses). Micrographs
were made using an Olympus BX41 microscope and
Olympus Camedia C-5050 camera.
Several of the collected eriophyoid mite specimens were
rinsed in 98 % alcohol and stored in 180 ll of ATL buffer
for several days. A nondestructive method of DNA
extraction was applied, as described by Dabert et al.
(2008), using the DNeasy Blood & Tissue Kit (Qiagen,
Hilden, Germany). Post-extraction, specimen cuticles were
transferred to 70 % ethanol and mounted on slides for
identification. A fragment of the D2 region of 28S ribo-
somal DNA (28S rDNA) was amplified using the primers
D1D2fw2 (Sonnenberg et al. 2007) and 28SR0990 (Mir-
onov et al. 2012). PCR was conducted in a 10 ll reaction
volume containing 5 ll of Type-it Multiplex PCR Master
Mix (Qiagen, Hilden, Germany), 50 pM of each primer,
and 4 ll of DNA template.
The thermal cycling profile consisted of an initial
denaturation step of 5 min at 95 °C, followed by 35 cycles
of 30-s denaturation at 95 °C, 30-s annealing at 50 °C, and
1-min extension at 72 °C, with a final step of 15 min at
72 °C. The reaction products were diluted by half, and 5 ll
of each diluted PCR product was stained with the GelRed
Nucleic Acid Gel Stain (Biotium, Hayward, CA, USA) and
checked by electrophoresis on a 1 % agarose gel. The
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samples were sequenced with the following primers to
obtain the D2 region of the 28S rDNA: universal forward
primer D1D2fw2, specific forward primer Er28SF05, and
specific reverse primer Er28SR05 (Szydło et al. 2015).
Sequencing was performed using BigDye Terminator ver-
sion 3.1 on an ABI Prism 3130XL Genetic Analyzer
(Applied Biosystems, Foster City, CA, USA). The forward
and reverse sequences were aligned and assembled with
BioEdit version 7 software (Hall 1999). Trace files were
aligned and edited with MEGA6 (Tamura et al. 2013). Four
obtained sequences of 627 bp were deposited in NCBI
(National Center for Biotechnology Information) GenBank
database under Accession Numbers KR072631, KR072632,
KR072633, and KR072634.
The taxonomic identification of specimen cuticles
showed that DNA sequences were obtained from only one
of the two collected species, belonging to the genus Ce-
cidophyes Nalepa, 1887. Identification of the study subject
to the genus Cecidophyes was confirmed by the Basic
Local Alignment Search Tool (Standard Nucleotide
BLAST; NCBI), optimized for blastn (somewhat similar
sequences) and megablast (highly similar sequences). Two
sequences of Cecidophyes spp. from the NCBI GenBank
database (Accession Numbers: KF782480 and KF782481)
were aligned with the Cecidophyes n. sp. sequences to
calculate the Kimura-2-parameter (K2P) distances between
sequences with MEGA6 software.
Results
Two different eriophyoid species were identified from the
samples of S. oppositifolia based on morphological study:
A. saxifragae (Rostrup, 1900) and C. siedleckii n. sp. The
description of C. siedleckii n. sp. is provided below with
DNA data, and the description of A. saxifragae is
supplemented.
Family Eriophyidae Nalepa, 1898
Subfamily Cecidophyinae Keifer, 1966
Tribe Cecidophyini Keifer, 1966
Genus Cecidophyes Nalepa, 1887
C. siedleckii n. sp. Kiedrowicz, Szydło & Skoracka
(Figs. 2,3)
Female (holotype and seven paratypes): body spindleform,
195 (163–203); width 67 (63–70). Gnathosoma 20 (25–30),
projecting forward and down, dorsal pedipalpal genual
setae d5 (4–7), setae ep 4 (3–4), chelicerae 25 (22–25).
Prodorsal shield 38 (41–42), 50 (48–49) wide, subrectan-
gular, anterior lobe 12 (11–13) long, 21 (20–22) wide.
Fig. 1 Studied area: aSvalbard Archipelago, scale bar 100 km; bStudy area, scale bar 4km
Polar Biol (2016) 39:1359–1368 1361
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Shield pattern with complete median line and admedian
lines; submedian lines incomplete and appear as six short
lines. Lack of scapular setae sc. Legs with all usual
segments and setae present. Leg I 32 (27–34); femur 10
(8–11), seta bv 14 (10–15); genu 5 (4–5), seta l’’ 32
(30–34); tibia 8 (8–9), seta l’ 8 (7–10); tarsus 7 (6–8),
setae: ft’’ 20 (18–25), ft’ 18 (14–22), u’ 4 (3–5); solenidion
x6 (5–7); empodium simple 5 (4–6) with 5 (4–5) rays. Leg
II 29 (27–31); femur 11 (9–11), seta bv 12 (10–13); genu 5
(4–5), seta l’’ 6 (6–8); tibia 7 (6–7); tarsus 7 (6–7), setae:
ft’’ 21 (20–26), ft’ 5 (5–8), u’ 4 (3–4); solenidion x6 (6–8);
empodium simple 4 (4–6) with 5 (4–5) rays. Coxae
smooth. Setae 1b 4 (4–5), tubercles 1b 11 (8–11) apart;
setae 1a 17 (12–18), tubercles 1a 14 (13–14) apart; setae 2a
36 (32–35), tubercles 2a 27 (23–28) apart; distance
between tubercles 1b and 1a 5 (5–6), distance between
tubercles 1a and 2a 9 (7–10). Genital opening 15 (15–17),
28 (26–28) wide, genital coverflap with 24 (22–30)
longitudinal ridges in two rows; setae 3a 10 (7–11),
tubercles 3a 19 (18–19) apart. Opisthosoma spindleform;
50 (48–52) dorsal annuli, 53 (52–57) ventral annuli with
minute, oval microtubercles situated near rear margin of
the annuli. Opisthosomal setae: c2 34 (25–29), tubercles 58
(58–67) apart, on 8th (6–8) ventral annulus; d50 (45–51),
tubercles 43 (43–44) apart, on 17th (16–18) ventral
annulus; e7 (7–9), tubercles 25 (25–26) apart, on 29th
(27–31) ventral annulus; f22 (21–26), tubercles 25 (25–26)
apart, on 48th (46–51) ventral annulus, 5th (5–7) annulus
from rear. Setae h1 absent; setae h2 48 (48–68), 10 (10)
apart.
Fig. 2 Cecidophyes siedleckii
n. sp. female: aventral view;
bcoxogenital region;
canterodorsal mite; scale bar
10 lm
Fig. 3 Cecidophyes siedleckii n. sp. female: aventral mite; ban-
terodorsal mite; cinternal genitalia; dempodium; eposterodorsal
mite; fanterolateral mite; scale bar a,b,e,f—20 lm; c—25 lm; d—
6lm
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Type material: Holotype female [SVERCEC01], para-
types females—seven females [SVERCEC02, SVER-
CEC03, SVERCEC04, SVERCEC05, SVERCEC06,
SVERCEC07, SVERCEC08] from northern coast of
Hornsund, Wedel Jarlsberg Land, 77°000N, 15°19.80,
August 2011 from S. oppositifolia (Saxifragaceae), leg.
K. Zawierucha. Material is deposited in the collection of
the Faculty of Biology, Adam Mickiewicz University—
AMU, Poznan
´, Poland, and in the collection of Department
of Applied Entomology, Faculty of Horticulture, Biotech-
nology and Landscape Architecture, Warsaw University of
Life Sciences—SGGW, Warsaw, Poland.
Relation to the host: Free-living on upper part of leaves.
Mites were not found inside flowers or buds. No plant
deformations were noted.
Etymology: The specific name is the noun in genitive
case derived from the surname of the founder of the Polish
Polar Station on Svalbard, where these specimens were
collected.
DNA data: A 627-bp fragment of the D2 region of 28S
rDNA was amplified and sequenced from four female
specimens of C. siedleckii n. sp. (GenBank Acc.
KR072631, KR072632, KR072633, KR072634). This
DNA marker has been utilized successfully in phylogenetic
studies at the species level and has been proposed as a
DNA bar code for taxonomic differentiation of animal
species (Sonnenberg et al. 2007). This DNA fragment has
also been successfully applied to the delimitation of species
(including cryptic species) in eriophyoid mites (e.g., Sko-
racka et al. 2013,2014; Lewandowski et al. 2014). No
variability between obtained sequences was detected.
Interspecific K2P divergence between new species and two
other Cecidophyes spp., namely Cecidophyes hirsutes Xue,
Song and Hong, 2011 and Cecidophyes truncatis Xue,
Song and Hong, 2011, was 12.3 and 18.1 %, respectively,
which corresponded to divergences between congeneric
eriophyoid species reported in other studies (e.g., Lewan-
dowski et al. 2014).
Differential diagnosis:Cecidophyes siedleckii is the first
Cecidophes species found on plants belonging to the family
Saxifragaceae. Cecidophyes glaber (Nalepa, 1892) has
been described from Sedum reflexum L., Crassulaceae,
which together with Saxifragaceae belongs to the same
order, Saxifragales. The new species is similar to C. glaber
in having complete median and admedian lines on the
prodorsal shield; however, these lines are composed of
short dashes in C. glaber, whereas they are continuous in
C. siedleckii. Additionally, these two species can be dif-
ferentiated by the shapes of the submedian lines and dorsal
microtubercles. Cecidophyes glaber has regular and com-
plete submedian lines and large dorsal microtubercles.
Cecidophyes siedleckii has irregular and interrupted sub-
median lines and minute dorsal tubercles. The new species
can be also differentiated from Cecidophes galii (Kar-
pelles, 1884) described from Galium aparine L. (Rubi-
aceae) by the shapes of submedian lines (which are
complete and regular in C. galii and irregular and inter-
rupted in C. siedleckii) and the number of opisthosomal
annuli (near 70 in C. galii and fewer than 60 in C. sie-
dleckii). The prodorsal shield design, composed of longi-
tudinal lines, and the knotless tarsal solenidion in the new
species differentiate it from Cecidophyes truncatis (Xue,
Hong and Song, 2001) and Cecidophyes hirsutes (Xue,
Hong and Song, 2001), which both have network shield
designs and knobbed tarsal solenidions. Cecidophyes hir-
sutes also differs from the new species by having elliptical
microtubercles (compared to minute microtubercles in C.
siedleckii). Many North American Cecidophyes species
have network shield designs, which differentiate them from
the new species (Baker et al. 1996). One example is Ce-
cidophyes tampae Keifer, 1966, which differs from the new
species in having elongate dorsal microtubercles, a genital
coverflap with 16 ridges, coxae with curved lines, and a
6-rayed empodium. By contrast, C. siedleckii has minute
microtubercles, a genital coverflap with 22–30 ridges,
smooth coxae, and a 4- to 5-rayed empodium.
Family Eriophyidae Nalepa, 1898
Subfamily Eriophyinae Nalepa, 1898
Tribe Aceriini Amrine and Stasny, 1994
Genus Aceria Keifer, 1944
A. saxifragae (Rostrup, 1900)
(Figs. 4,5)
Female (six specimens): body vermiform 186–268; 63–80
wide. Gnathosoma 29–32, projecting forward and down,
dorsal pedipalpal genual setae d5–7, setae ep 4, chelicerae
22–26. Prodorsal shield 32–40, 42–45 wide, subrectangu-
lar, without anterior lobe. Shield pattern: incomplete
median line, which appears as a long line in the front 3/4
with a transverse line in the rear 1/3 and two short arcs at
the rear shield margin; admedian lines complete; subme-
dian lines form a mosaic pattern. Scapular setae sc 19–24,
tubercles sc 25–30 apart. Legs with all usual segments and
setae present. Leg I 30–35; femur 9–10, seta bv 7–8; genu
5–6, seta l’’ 25–30; tibia 7–8, seta l’ 7–8; tarsus 8, setae:
ft’’ 22–26, ft’ 12–17,u’3-6; solenidion x8–9; empodium
simple 6–7 with 5 rays. Leg II 26–31; femur 8–10, seta bv
8–12; genu 4–6, seta l’’ 10–11; tibia 4–6; tarsus 6–7, setae:
ft’’ 21–27, ft’ 6–9, u’ 5–6; solenidion x8–9; empodium
simple 6–8 with five rays. Coxae with spots. Setae 1b 6–8,
tubercles 1b 14–15 apart; setae 1a 20–22, tubercles 1a
11–12 apart; setae 2a 20–35, tubercles 2a 27 apart;
distance between tubercles 1b and 1a 7–9, distance
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between tubercles 1a and 2a 8. External genitalia 17–18,
22–24 wide, genital coverflap with 9–11 longitudinal
ridges; setae 3a 15–16, tubercles 3a 18–20 apart. Opistho-
soma vermiform; 62–63 dorsal annuli, 61–65 ventral
annuli. Microtubercles near rear margin of the annuli;
rounded. Opisthosomal setae: c2 25–33, tubercles 55–69
apart, on 8–9 ventral annulus; d35–41, tubercles 46–54
apart, on 20–24 ventral annulus; e12–13, tubercles 23–28
apart, on 33–37 ventral annulus; f20–25, tubercles 22–27
apart, on 54–59 ventral annulus, 5–6 annulus from rear.
Setae h1 4–5, 7–8 apart; setae h2 40–58, 10–11 apart;
distance between h1 and h2 2–3.
Material: Six females from northern coast of Hornsund,
Wedel Jarlsberg Land, 77°000N, 15°19.80, August 2011
from S. oppositifolia (Saxifragaceae), leg. K. Zawierucha.
Material is deposited in the collection of the Faculty of
Biology, Adam Mickiewicz University, Poznan
´, Poland.
Relation to the host: Free-living on leaves. According to
previous observations (Rostrup 1900; Liro 1940; James
Amrine personal communication), A. saxifragae has been
found both free-living and inhabiting buds. In the course of
our study, we did not found any mite specimens inside
buds. All recorded specimens observed in dried samples
were associated with plant leaves.
Remarks: Female A. saxifragae specimens collected in
South Spitsbergen National Park in this study differed
morphologically both from the specimens presented in the
original description (Rostrup 1900) and a subsequent
description by Liro (1940) due to their shorter sc setae [as
can be observed in the line drawings provided by Liro
(1940)] and 5-rayed empodium (it is four-rayed in the
earlier descriptions). Moreover, the prodorsal shield pattern
(not described, but only presented in figures by previous
authors) is more striking and complicated compared to
earlier descriptions. The prodorsal shield pattern of speci-
mens in this study is composed of an incomplete median
line, which appears as a long line in the front 3/4 with a
transverse line in the rear 1/3 and two short arcs at the rear
shield margin; admedian lines are complete, and the sub-
median lines form a mosaic pattern. The prodorsal shield
pattern presented by Liro (1940) lacks the transverse line
and mosaic pattern. Despite considerable effort made to
find type material of A. saxifragae (James W. Amrine,
West Virginia University and Nikolaj Scharff, Natural
History Museum of Denmark, personal communication),
we were not able to confirm neither the type collection still
exists nor where it was deposited. Therefore, we were only
able to compare our complementary description to the
descriptions by Rostrup (1900) and Liro (1940). Unfortu-
nately, such situations are common for type materials of
many eriophyoid species (James W. Amrine personal
communication). Nevertheless, the differences observed
between the original descriptions and material examined by
us may be the result of (1) human perception bias, (2)
limitations in the state of the art, and/or (3) phenotypic
Fig. 4 Aceria saxifragae
female: aventral view;
banterodorsal mite;
ccoxogenital region; scale bar
10 lm
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variation among populations of A. saxifragae. A century
ago, microscopy was not as precise or discriminating as
today, thus the descriptions of eriophyoid species of that
time lacked detail and accuracy, the result being sub-op-
timal measurements and drawings. Thus, it is possible that
some lines on the prodorsal shield of A. saxifragae may
have been missed in the initial descriptions. Quantitative
morphological traits can also vary in eriophyoid mites, and
this variation may exist between populations separated
geographically or by host association (e.g., Navia et al.
2009; Shen et al. 2014). Thus, the observed differences in
the length of sc setae and the number of empodial rays may
reflect intraspecies variation.
Discussion
There is undoubtedly a general lack of knowledge of erio-
phyoid mite distributions in Arctic regions. A small number
of eriophyoid mite species have been reported from
Greenland, Iceland, and Arctic Russia, e.g., A. saxifragae
(Rostrup, 1900); A. reykjaviki Szydło, Skaftason and Skoracka,
2010;A. thomasi (Nalepa, 1889); Aculops pedicularis
(Nalepa, 1892); A. thymi (Nalepa, 1889); Aculus groen-
landicus (Rostrup, 1900); A. tetanothrix (Nalepa, 1889);
Phyllocoptes empetri Rostrup, 1900 (Amrine 2003; Szydło
et al. 2010), as well as one possibly accidental specimen
from Svalbard belonging to the genus Eriophyes (Thor
1934). The study described here represents an important
contribution to taxonomic research on Eriophyoidea on
Svalbard, and reports one new species of eriophyoid mite
with bar-code data and one new record of A. saxifragae with
a supplementary morphological description.
Aceria saxifragae was originally described from S.
oppositifolia in Greenland (Rostrup 1900). It has subse-
quently been recorded on the same host plant in Finland,
Sweden, and mainland of Norway (Amrine 2003), although
these faunistic records imply neither a definitive place of
origin of this mite species nor any conclusions about the
possible changing distribution of A. saxifragae.Saxifraga
oppositifolia is not listed as a native of Svalbard (Jo
´nsdo
´ttir
2005). However, it is listed as native to nearby Greenland,
as well as Canada, Alaska, and the northern continental
USA (USDA-NRCS 2015). Given that most eriophyoid
species are host specialists (Skoracka et al. 2010), it is
likely that both eriophyoid species found on S. oppositifolia
in this study, A. saxifragae and C. siedleckii n. sp., arrived
to Svalbard with their host plant. To better understand
where these mite species originated and how they are
distributed, more comprehensive studies comparing mite
populations and their host plants from different localities
(e.g., Greenland, Canada, Alaska, mainland Scandinavia),
as well as surveys of mites on close relatives of S.
oppositifolia that are present on Svalbard, would be useful,
preferably including DNA marker data that can discrimi-
nate between intraspecific populations. Moreover, to
explain possible routes of mite dispersal and how they
arrived on Svalbard, it would be useful in particular to
collect populations found near transport hubs to/from
Svalbard, such as in mainland Norway.
Overall, there has been a lack of comprehensive sam-
pling effort for phytophagous mites in the Arctic. Of those
locations that have been surveyed, many were only sam-
pled on one occasion, often by non-specialists (Coulson
et al. 2014a), resulting in sub-optimal sampling methods
that yield incomplete data. The paucity of knowledge
regarding eriophyoid mites inhabiting the Arctic likely
results in part from methodological difficulties. Eriophyoid
mites are minute organisms, and their detection and iden-
tification require specialized training.
Effects of changing climates will vary from region to
region (Hodkinson 2013). Climate warming in the Arctic is
expected to modify regional plant communities. For
example, warmer and longer growing seasons are leading
to an overall increase in the abundance of deciduous woody
Fig. 5 Aceria saxifragae female: aventral mite; banterodorsal mite;
cinternal genitalia; dempodium; eposterodorsal mite; scale bar a,b,
e—20 lm; c—25 lm; d—8 lm
Polar Biol (2016) 39:1359–1368 1365
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

shrub species such as dwarf birch (Betula nana L. 1753)
and willows (Salix spp. L.) (Sturm et al. 2001; Tape et al.
2006; Forbes et al. 2010). The number of invasive species
is also increasing globally, in part as a result of intensified
and accelerated human trade and travel (e.g., Kobelt and
Nentwig 2008; Coulson 2013). This is especially true for
plants in Svalbard (Alsos et al. 2007). The frequency and
abundance of phytophagous arthropods associated with
these plants, both native and introduced, are also likely to
increase as a result of these changes. Eriophyoid mites can
be very damaging to their host plants (Lindquist and
Amrine 1996). Although most eriophyoids are highly host-
specific, numerous eriophyoid species are generalist pests
of a variety of crop species (e.g., Aceria tulipae, Aceria
tosichella, Abacarus hystrix; Skoracka et al. 2010). This,
combined with the known ability of many eriophyoids to
vector plant diseases (Oldfield and Proeseler 1996),
underlines the urgent need to fill gaps in knowledge of
phytophagous mite ecology and taxonomy in high Arctic
habitats. This is particularly true of the Svalbard archipe-
lago, whose location near the confluence of ocean currents
and air masses of varied thermal characteristics (Humlum
et al. 2007) makes it one of the most climatically sensitive
regions in the world (Rogers et al. 2005).
Acknowledgments The study was financially supported by Faculty
of Biology, Adam Mickiewicz University (AMU), Poznan
´, Poland,
and partially by the Polish Ministry of Science and Higher Education
via the ‘‘Diamond Grant’’ programme (Grant No. DIA 2011035241 to
K.Z.). The authors are grateful to Prof. James Jr. Amrine for helpful
information regarding eriophyoid mites occurring in Arctic, Dr.
Nikolaj Scharff for information about type material of Aceria sax-
ifragae, Dr. Ziemowit Olszanowski (AMU) for the assistance
regarding taxonomical nomenclature, and Prof. Karol Latowski
(AMU) for the confirmation of the botanical taxonomic identification.
Compliance with ethical standards
Conflict of interest The authors declare that they have no conflict
of interest.
Open Access This article is distributed under the terms of the
Creative Commons Attribution 4.0 International License (http://crea
tivecommons.org/licenses/by/4.0/), which permits unrestricted use,
distribution, and reproduction in any medium, provided you give
appropriate credit to the original author(s) and the source, provide a
link to the Creative Commons license, and indicate if changes were
made.
References
Alsos IG, Eidesen PB, Ehrich D, Skrede I, Westergaard K, Jacobsen
GH, Landvik JY, Taberlet P, Brochmann C (2007) Frequent
long-distance plant colonization in the changing arctic. Science
316:1601–1608
Amrine JW Jr (2003) Catalog of the Eriophyoidea. A working catalog
of the Eriophyoidea of the world. Ver. 1.0. http://insects.tamu.
edu/research/collection/hallan/acari/eriophyidae. Accessed 1
Apr 2015
Amrine JW Jr, Stasny TAH, Flechtmann CHW (2003) Revised keys
to the world genera of the Eriophyoidea (Acari: Prostigmata).
Indira Publishing House, West Bloomfield
Baker EW, Kono T, Amrine JW Jr, Delfinado-Baker M, Stasny TA
(1996) Eriophyoid mites of the United States. Indira Publishing
House, West Bloomfield
Coulson SJ (2013) The terrestrial invertebrate fauna of the Svalbard
Archipelago in a changing world; history of research and
challenges. Can Entomol 145:131–146
Coulson SJ, Refseth D (2004) Chapter 3. The terrestrial and
freshwater invertebrate fauna of Svalbard (and Jan Mayen). In:
Prestrud P, Strøm H, Goldman HV (eds) A catalogue of the
terrestrial and marine animals of Svalbard. Tromsø, Norwegian
Polar Institute, pp 57–122
Coulson SJ, Hodkinson ID, Webb NR (2003) Aerial dispersal of
invertebrates over a high-Arctic glacier foreland: Midtre Love
´-
nbreen, Svalbard. Polar Biol 26:530–537
Coulson SJ, Schatz H, Gwiazdowicz DJ, Solhøy T (2014a) On the
oribatid and mesostigmatid mites (Acari) of the high arctic
Island of Hopen. Pol Polar Res 35:133–139
Coulson SJ, Convey P, Aakra K, Aarvik L, A
´vila-Jime
´nez ML,
Babenko A, Biersma EM, Bostro
¨m S, Brittain JE, Carlsson AM,
Christoffersen K, De Smet WH, Ekremj T, Fjellberg A, Fu
¨reder
L, Gustafssonm D, Gwiazdowicz DJ, Hansen LO, Holmstrup M,
Hulle
´M, Kaczmarek Ł, Kolicka M, Kuklin V, Lakka HK,
Lebedeva N, Makarova O, Maraldo K, Melekhina E, Ødegaard
F, Pilskog HE, Simon JC, Sohlenius B, Solhøy T, Søli G, Stur E,
Tanasevitch A, Taskaeva A, Velle G, Zawierucha K, Zmud-
czyn
´ska-Skarbek K (2014b) The terrestrial and freshwater
invertebrate biodiversity of the archipelagoes of the Barents
Sea; Svalbard, Franz Josef Land and Novaya Zemlya. Soil Biol
Biochem 68:440–470
Coulson SJ, Fjellberg A, Melekhina EN, Taskaeva AA, Lebedeva
NV, Belkina O, Seniczak S, Seniczak A, Gwiazdowicz DJ
(2015) Microarthropod communities of disturbed or imported
soils in the High Arctic; the abandoned coal mining town of
Pyramiden. Biodivers Conserv, Svalbard. doi:10.1007/s10531-
015-0885-9
Dabert J, Ehrnsberger R, Dabert M (2008) Glaucalges tytonis sp. n.
(Analgoidea, Xolalgidae) from the barn owl Tyto alba (Strigi-
formes, Tytonidae): compiling morphology with DNA barcode
data for taxon descriptions in mites (Acari). Zootaxa 1719:41–52
Dabert M, Coulson SJ, Gwiazdowicz DJ, Moe B, Hanssen SA,
Biersma EM, Pilskog HE, Dabert J (2014) Differences in
speciation progress in feather mites (Analgoidea) inhabiting the
same host: the case of Zachvatkinia and Alloptes living on arctic
and longtailed skuas. Exp Appl Acarol 65:163–179
Dastych H (1985) West Spitsbergen Tardigrada. Acta Zool Crac
28:169–214
Dastych H, Drummond AE (1996) Notes on limnic water-bears
(Tardigrada) from the Robertskollen nunataks, Dronning Maud
Land, Antartica. Entomol Mitt Zool Mus Hamburg 12:111–117
de Lillo E, Craemer C, Amrine JW, Nuzzaci G (2010) Recommended
procedures and techniques for morphological studies of Erio-
phyoidea (Acari: Prostigmata). Exp Appl Acarol 51:283–307
Duso C, Castagnoli M, Simoni S, Angeli G (2010) The impact of
eriophyoids on crops: recent issues on Aculus schlechtendali,
Calepitrimerus vitis and Aculops lycopersici. Exp Appl Acarol
51:151–168
Forbes BC, Fauria MM, Zetterberg P (2010) Russian Arctic warming
and ‘‘greening’’ are closely tracked by tundra shrub willows.
Glob Change Biol 16:1542–1554
Go
´rska B, Grzelak K, Kotwicki L, Hasemann Ch, Scheweb I,
Soltwedel T, Włodarska-Kowalczuk M (2014) Bathymetric
1366 Polar Biol (2016) 39:1359–1368
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

variations in vertical distribution patterns of meiofauna in the
surface sediments of the deep Arctic ocean (HAUSGARTEN,
Fram strait). Deep-Sea Res I 91:36–49
Gwiazdowicz DJ, Coulson SJ, Grytnes JA, Pilskog HE (2012) The
bird ectoparasite Dermanyssus hirundinis (Acari, Mesostigmata)
in the High Arctic: a new parasitic mite to Spitsbergen, Svalbard.
Acta Parasitol 57:378–384
Hackman W, Nyholm ES (1968) Notes on the arthropod fauna of
Spitsbergen II. 9. Mallophaga from Spitsbergen and Bear Island.
Ann Entomol Fenn 34:75–82
Hall TA (1999) BioEdit: a user-friendly biological sequence align-
ment editor and analysis program for Windows 95/98/NT.
Nucleic Acids Symp Ser 41:95–98
Halvorsen O, Bye K (1999) Parasites, biodiversity, and population
dynamics in an ecosystem in the High Arctic. Vet Parasitol
84:205–227
Hodkinson ID (2013) Terrestrial and freshwater invertebrates. In:
Meltofte H (ed) Arctic biodiversity assessment. Status and
Trends in Arctic biodiversity. Conservation of Arctic Flora and
Fauna, Akureyri, pp 194–223
Humlum O, Christiansen HH, Juliussen H (2007) Avalanche-derived
rock glaciers in Svalbard. Permafrost Periglac 18:75–88
Janiec K (1996) The comparison of freshwater invertebrates of
Spitsbergen (Arctic) and King George Island (Antarctic). Pol
Polar Res 17:173–202
Johnsen G, Candeloro M, Berge J, Moline M (2014) Glowing in the
dark: discriminating patterns of bioluminescence from different
taxa during the Arctic polar night. Polar Biol 37:707–713
Jo
´nsdo
´ttir IS (2005) Terrestrial ecosystems on Svalbard: hetero-
geneity, complexity and fragility from an Arctic Island
perspective. Biol Environ 105:155–165. doi:10.3318/BIOE.
2005.105.3.155
Kaczmarek Ł, Zawierucha K, Smykla J, Michalczyk Ł (2012)
Tardigrada of the Revdalen (Spitsbergen) with the descriptions
of two new species: Bryodelphax parvuspolaris (Hetero-
tardigrada) and Isohypsibius coulsoni (Eutardigrada). Polar Biol
35:1013–1026
Kobelt M, Nentwig W (2008) Alien spider introductions to Europe
supported by global trade. Divers Distrib 14:273–280
Kuklin VV, Galkin AK, Marasaev SF, Marasaeva EF (2004) The
characteristics of the helminthofauna of sea birds of the Svalbard
Archipelago. Dokl Biol Sci 395:124–126
Lewandowski M, Skoracka A, Szydło W, Kozak M, Druciarek T,
Griffiths D (2014) Genetic and morphological diversity of
Trisetacus species (Eriophyoidea: Phytoptidae) associated with
coniferous trees in Poland: phylogeny, barcoding, host and
habitat specialization. Exp Appl Acarol 63:497–520
Lindquist EE (1996) External anatomy and notation of structures. In:
Lindquist EE, Sabelis MW, Bruin J (eds) Eriophyoid mites: their
biology, natural enemies and control. Elsevier, Amsterdam,
pp 3–31
Lindquist EE, Amrine JW (1996) Systematics, diagnoses for major
taxa, and keys to families and genera with species on plants of
economic importance. In: Lindquist EE, Sabelis MW, Bruin J
(eds) Eriophyoid mites: their biology, natural enemies and
control. Elsevier, Amsterdam, pp 33–87
Lippert H, Iken K, Rachor E, Wiencke C (2001) Macrofauna
associated with macroalgae in the Kongsfjord (Spitsbergen).
Polar Biol 24:512–522
Liro JI (1940) Neue Eriophyiden aus Finland. Ann Zool Soc Zool-Bot
Fenn Vanamo 8:1–67
MacFadyen A (1954) The invertebrate fauna of Jan Mayen Island
(East Greenland). J Anim Ecol 23:261–297
Michalska K, Skoracka A, Navia D, Amrine JW (2010) Behavioural
studies on eriophyoid mites: an overview. Exp Appl Acarol
51:31–59
Miller AD, Skoracka A, Navia D, de Mendonca RS, Szydło W,
Schultz MB, Smith CM, Truol G, Hoffmann A (2013) Phylo-
genetic analyses reveal extensive cryptic speciation and host
specialization in an economically important mite taxon. Mol
Phylogenet Evol 66:928–940
Mironov SV, Dabert J, Dabert M (2012) A new feather mite species
of the genus Proctophyllodes Robin, 1877 (Astigmata: Procto-
phyllodidae) from the Long-tailed Tit Aegithalos caudatus
(Passeriformes: Aegithalidae)—morphological description with
DNA barcode data. Zootaxa 3253:54–61
Navia D, Moraes G, Querino R (2009) Geographic pattern of
morphological variation of the coconut mite, Aceria guerreronis
Keifer (Acari: Eriophyidae), using multivariate morphometry.
Braz J Biol 69:773–783
Navia D, Ochoa R, Welbourn C, Ferragut F (2010) Adventive
eriophyoid mites: a global review of their impact, pathways,
prevention and challenges. Exp Appl Acarol 51:225–255
Oldfield GN, Proeseler G (1996) Eriophyoid mites as vectors of plant
pathogens. In: Lindquist EE, Sabelis MW, Bruin J (eds)
Eriophyoid mites: their biology, natural enemies and control.
Elsevier Science BV, Amsterdam, pp 259–273
Pilskog HE, Solhøy T, Gwiazdowicz DJ, Grytnes JA, Coulson SJ
(2014) Invertebrate communities inhabiting nests of migrating
passerine, wild fowl and sea birds breeding in the High Arctic,
Svalbard. Polar Biol 37:981–998
Porazin
´ska DL, Fountain AG, Nylen TH, Tranter M, Virginia RA,
Wall DH (2004) The biodiversity and biogeochemistry of
cryoconite holes from McMurdo Dry Valley glaciers, Antarctica.
Arct Antarct Alp Res 36:84–91
Rogers JC, Yang L, Li L (2005) The role of Fram Strait winter
cyclones on sea ice flux and on Spitsbergen air temperatures.
Geophys Res Lett. doi:10.1029/2004GL022262
Rostrup S (1900) Gronlandske Phytoptider. Vidensk Medd naturhist
Foren Kobenharn 6:241–249
Shen TJ, Kuo CC, Wang CF, Huang KW (2014) Delimitation of a
continuous morphological character with unknown prior mem-
bership: application of a finite mixture model to classify scapular
setae of Abacarus panticis. Exp Appl Acarol 63:361–375
Skoracka A, Smith L, Oldfield GN, Cristofaro M, Amrine JW (2010)
Host- plant specificity and specialization in eriophyoid mites and
their importance for the use of eriophyoid mites on biocontrol
agents of weeds. Exp Appl Acarol 51:93–113
Skoracka A, Kuczyn
´ski L, de Mendonca R, Dabert M, Szydło W,
Knihinicki D, Truol G, Navia D (2012) Cryptic species within
the wheat curl mite Aceria tosichella (Keifer) (Acari, Eriophy-
oidea) revealed by mitochondrial, nuclear and morphometric
data. Invertebr Syst 26:417–433
Skoracka A, Kuczyn
´ski L, Szydło W, Rector B (2013) The wheat curl
mite Aceria tosichella (Acari: Eriophyoidea) is a complex of
cryptic lineages with divergent host ranges: evidence from
molecular and plant bioassay data. Biol J Linn Soc 109:165–180
Skoracka A, Kuczyn
´ski L, Rector B, Amrine JW Jr (2014) Wheat curl
mite and dry bulb mite: untangling a taxonomic conundrum
through a multidisciplinary approach. Biol J Linn Soc
111:421–436
Sonnenberg R, Nolte AW, Tautz D (2007) An evaluation of LSU
rDNA D1-D2 sequences for their use in species identification.
Front Zool. doi:10.1186/1742-9994-4-6
Stien A, Voutilainen L, Haukisalmi V, Fuglei E, Mork T, Yoccoz NG,
Ims RA, Henttonen H (2010) Intestinal parasites of the arctic fox
in relation to the abundance and distribution of intermediate
hosts. Parasitology 137:149–157
Sturm M, Racine C, Tape K (2001) Climate change: increasing shrub
abundance in the Arctic. Nature 411:546–547
Summerhayes VS, Elton CS (1928) Further contributions to the
ecology of Spitsbergen. J Ecol 16:193–268
Polar Biol (2016) 39:1359–1368 1367
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

Szydło W, Skaftason JF, Skoracka A (2010) Eriophyoid mites
(Prostigmata: Eriophyoidea: Eriophyidae) from Iceland: one new
species, and three new mite records. Ann Zool 60:139–157
Szydło W, Hein G, Denizhan E, Skoracka A (2015) Exceptionally
high levels of genetic diversity in wheat curl mite (Acari:
Eriophyidae) populations from Turkey. J Econ Entomol
108:2030–2039
Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013)
MEGA6: molecular evolutionary genetics analysis version 6.0.
Mol Biol Evol 30:2725–2729
Tape K, Sturm M, Racine C (2006) The evidence for shrub expansion
in northern Alaska and the pan-Arctic. Glob Change Biol
12:686–702
Thor S (1930) Beitrage zur Kenntnis der invertebraten Fauna von
Svalbard. Skrifter om Svalbard og Ishavet 27. Norwegian Polar
Institute, Oslo
Thor S (1934) Neue Beitrage zur Kenntnis der invertebraten Fauna
von Svalbard. Zool Anz 107:114–139
USDA, NRCS (2015) The PLANTS database (http://plants.usda.gov,
27 April 2015). National Plant Data Team, Greensboro, NC
27401-4901 USA
Walkera MD, Wahrenb CH, Hollisterc RD, Henryde GHR, Ahlquistf
LE, Alatalog JM, Bret-Harteh MS, Calefh MP, Callaghani TV,
Carrolla AB, Epsteinj HE, Jo
´nsdo
´ttirk IS, Kleinl JA, Magnu
´s-
sonm B, Molaug U, Oberbauerf SF, Rewan SP, Robinsono CH,
Shaverp GR, Sudingq KN, Thompsonr CC, Tolvanens A,
Totlandt Ø, Turneru PL, Tweediev CE, Webberw PJ, Wookeyx
PE (2006) Plant community responses to experimental warming
across the tundra biome. PNAS 103:1342–1346
Walter DE, Proctor HC (2013) Mites: ecology, evolution &
behaviour: life at a microscale, 2nd edn. Springer, Netherlands,
pp 1–494
Xue XF, Song ZW, Hong XY (2011) Three new species of
Cecidophyinae (Acari: Eriophyidae) from China. J Nat Hist
45:1200–1203
Zawierucha K (2013) Tardigrada from Arctic tundra (Svalbard,
Spitsbergen) with a description of Isohypsibius karenae (Eu-
tardigrada: Isohypsibiidae). Pol Polar Res 34:383–396
Zawierucha K, Coulson S, Michalczyk Ł, Kaczmarek Ł (2013)
Current knowledge of the Tardigrada of Svalbard with the first
records of water bears from Nordaustlandet (High Arctic). Polar
Res 32:20886. doi:10.3402/polar.v32i0.20886
Zawierucha K, Smykla J, Michalczyk Ł, Gołdyn B, Kaczmarek Ł
(2015) Distribution and diversity of Tardigrada along altitudinal
gradients in the Hornsund, Spitsbergen (Arctic). Polar Res
34:24168. doi:10.3402/polar.v34.24168
1368 Polar Biol (2016) 39:1359–1368
123
Content courtesy of Springer Nature, terms of use apply. Rights reserved.

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