The golden jackal Canis aureus – a new species in the Baltic countries

Abstract

In the Baltic countries, the golden jackal (Canis aureus) was first recorded in Estonia on 28 February 2013 and three specimens of golden jackal were hunted in Latvia in 2014. The first golden jackal in Lithuania was hunted on 7 February 2015. The species of the golden jackal was identified using morphological and mitochondrial DNA control region (CR1) analysis. In Lithuania, hunting of these animals is permitted throughout the year. Few studies in the past revealed the potential role of the golden jackal as a carrier of intestinal helminths, parasites, and zoonotic diseases. In this study, the presence of tick-borne pathogens and other parasites in golden jackal specimen were investigated. No pathogens (Anaplasma phagocytophilum, Babesia sp., Bartonella sp.) were found in the spleen of the golden jackal. However, the flukes Apophallus donicus, nematodes Uncinaria stenocephala, and unidentified individuals of class Cestoda were detected. Helminths A. donicus and U. stenocephala are not new species for Lithuania and neighbouring territories.

Full text

BIOLOGIJA. 2018. Vol. 64. No. 3. P. 203–207
© Lietuvos mokslų akademija, 2018
e golden jackal Canis aureus–anew
species in theBaltic countries
*Corresponding author. Email: algimantas.paulauskas@vdu.lt
AlgimantasPaulauskas1*,
IrmaRažanskė1,
JanaRadzijevskaja1,
DovilėNugaraitė1,
VaclovasGedminas2
1Vytautas Magnus University,
VileikosSt.8, Kaunas 44404,
Lithuania
2Kaunas Tadas Ivanauskas
Zoological Museum,
LaisvėsAv. 106, Kaunas 44253,
Lithuania
In theBaltic countries, thegolden jackal (Canis aureus) was rst
recorded in Estonia on 28February2013 and three specimens
of golden jackal were hunted in Latvia in 2014. erst golden
jackal in Lithuania was hunted on 7February2015. especies
of thegolden jackal was identied using morphological and mi-
tochondrial DNA control region (CR1) analysis. In Lithuania,
hunting of these animals is permitted throughout theyear. Few
studies in thepast revealed thepotential role of thegolden jackal
as acarrier of intestinal helminths, parasites, and zoonotic diseas-
es. In this study, thepresence of tick-borne pathogens and other
parasites in golden jackal specimen were investigated. No patho-
gens (Anaplasma phagocytophilum, Babesia sp., Bartonella sp.)
were found in thespleen of thegolden jackal. However, theukes
Apophallus donicus, nematodes Uncinaria stenocephala, and uni-
dentied individuals of class Cestoda were detected. Helminths
A.donicus and U. stenocephala are not new species for Lithuania
and neighbouring territories.
Keywords: Canis aureus, mtDNA, helminths, Uncinaria steno-
cephala, Apophallus donicus, Cestoda
INTRODUCTION
e golden jackal (Canis aureus) is a native
Palearctic species with ahistoric range extending
from North Africa and South-eastern and Central
Europe through to Central and East Asia (Jhala
and Moehlman, 2008). epopulation and dis-
tribution of thegolden jackal within Europe has
seen considerable changes over recent decades.
Since themid-twentieth century, thedistribution-
al range of golden jackals has expanded signi-
cantly across Central and Eastern Europe with oc-
casional animals being documented to thenorth
and thewest, far from theestablished populations
in theareas and countries they had not been re-
corded before. Golden jackals have been recent-
ly sighted as far west as Switzerland and as far
north as Estonia (Rutkowskiet al., 2015; Trouw-
borstetal., 2015).
In Estonia and Latvia, golden jackals of un-
known origin have been recorded since 2011 (Ba-
nea, 2013; Toom, 2014; Trouwborstet al., 2015).
erst conrmed case of thegolden jackal in
the Baltic countries was reported in Estonia in
2013. In February 2013, agolden jackal was killed
by hunters in Matsalu National Park, West Estonia
(Männiletal., 2014). In 2014, golden jackals were
recorded in several other widely dispersed locali-
ties across Estonia, including thenorth, north-
east and south of thecountry. Until May 2015,

204 Algimantas Paulauskas, Irma Ražanskė, Jana Radzijevskaja, Dovilė Nugaraitė, Vaclovas Gedminas
a total of nine individuals were killed either
by hunters or in road accidents across Estonia
(Stratford, 2015).
First recorded cases of thegolden jackal in
Latvia were three individuals killed by ahunter
in July and December 2013 (Männiletal., 2014).
Until 2015, atotal of ten golden jackals were shot
or found dead in Latvia (Stratford, 2015).
In Lithuania, therst golden jackal was shot
in February 2015. especies of the hunted
individual was identied through a morpho-
logical examination. Since that time, other un-
conrmed reports of thegolden jackal followed
from thedistricts of Kaunas, Vilnius, Zarasai,
Varėna, and Biržai.
In thepresent study, we used mitochondrial
DNA control region data for theconrmation
of species identication, and as few studies in
thepast revealed thepotential role of thejack-
als as carriers of zoonotic diseases, we investi-
gated thepresence of tick-borne pathogens and
other parasites in thegolden jackal specimen
from Lithuania.
MATERIALS AND METHODS
Genomic DNA from thespecimen spleen was ex-
tracted using theGenomic DNA Purication Kit
(ermo Fisher Scientic, Lithuania) according
to manufacturer’s instructions. DNA was stored
at –20°C until subsequent handlings. A460bp of
hypervariable le domain of themitochondrial
DNA control region was amplied using PCR
and sequencing primers WDLOOPL 5’-TCC-
CTGACACCCCTACATTC-3’, H519 5’-CGTT-
GCGGTCATAGGTGAG-3’ (designed on wolf
mtDNA CR (Canigliaetal., 2013)) as described
in Fabbrietal., 2014. eproducts were separat-
ed on 1.5% agarose gel and visualized by etidium
bromide. PCR amplication product of mtDNR
control region was puried using GeneJET Gel
Extraction Kit (ermo Fisher Scientic, Lithu-
ania) and sequenced. eresulting 460-bp-long
sequence of theCR mtDNA was revised manu-
ally and aligned with golden jackal sequences
from GenBank in MEGA6. esequence of CR
mtDNA was submitted to GenBank and assigned
thefollowing accession number: KT123040.
Conventional PCR and nested PCR methods
were used for thedetection of Anaplasma phago-
cytophilum, Babesiaspp., Bartonellaspp. (Mas-
sungetal., 1998; Raretal., 2005; Normanetal.,
1995).
Prior to helminthological investigation the
material was frozen at –80°C for 10 days for safe-
ty reasons (i.e., to avoid possible infection with
Echinococcusspp.) (WHO/OIE Manual, 2001).
egolden jackal was thawed at room tempera-
ture and separate organs (entire gastrointestinal
tract, lungs, heart, liver, and kidney) were stud-
ied helminthologically according to themethod-
ology of Ivashkinetal. (1971). Examination of
the content of the intestines and of the stomach
was based on the method of consistent ushing.
Helminths were picked out and xed in 70% eth-
anol for later examination. For themicroscopic
study, trematodes and nematodes were mounted
in glycerin and examined under aMotic BA400
Tension microscope. Identication was based on
thekey of Kozlov (1977). ediet of thegolden
jackal was studied using analysis of thestomach
content. Each portion of thestomach content
was mixed with water and individual compo-
nents separated into groups.
RESULTS AND DISCUSSION
Comparison of themtDNA sequence identied
in this study with those deposited in GenBank
conrmed that theanimal hunted in Lithuania
in February 2015 was agolden jackal (accession
number KT123040). egolden jackal haplotype
identied in thepresent study corresponds with
thehaplotype previously identied in Italy, Cro-
atia, Bulgaria, Serbia, and theCaucasus (Fig.1).
egolden jackal is anew species in theBaltic
region. econrmed cases of thegolden jack-
al in Latvia and Estonia were recorded in 2013
(Männiletal., 2014; Stratford, 2015), two years
earlier than in Lithuania.
e Eurasian golden jackal has been reported
as ahost of pathogens of zoonotic and veterinary
importance, including arange of vector-borne
pathogens such as Ehrlichia canis, Anaplasma
phagocytophilum, and others (Waneretal., 1999),
and only one Babesia species (B.canis) was

205
e golden jackal Canis aureus – a new species in the Baltic countries
conrmed by molecular methods in golden jack-
als in Europe, in Romania (Mitkovaetal., 2017).
However, reports of tick-borne pathogens in
C.aureus are scarce. In this study, dierent PCR
methods were used for the detection of tick-
borne pathogens: Anaplasma phagocytophilum,
Babesiaspp., Bartonellaspp. eresults of PCR
analysis were negative for all tested pathogens.
Several hookworm (Ancylostomatidae) spe-
cies have been reported in golden jackals, with
Ancylostoma caninum and Uncinaria stenoceph-
ala commonly reported across the entire geo-
graphical range of these hosts (Gherman, Mihal-
ca, 2017). In thesmall intestine of theLithuanian
golden jackal, 49 ukes of species Apophallus
donicus, 11 nematodes of species Uncinaria
stenocephala (Fig. 2), and 29 unidentied indi-
viduals of Cestoda were found.
e diet of golden jackal was studied through
thestomach content. It was found to consist of
Fig. 1. Phylogenetic tree of mtDNA sequences created using theNeighbor-Joining
method and abootstrap analysis of 1000 replicates. esample from thepresent
study is marked●. Nyctereutes procyonoides are used as an out-group. Abbreva-
tions: BG–Bulgaria, HR–Croatia, IT–Italy, RS–Serbia
Fig. 2. Uncinaria stenocephala, microscopic
examination

206 Algimantas Paulauskas, Irma Ražanskė, Jana Radzijevskaja, Dovilė Nugaraitė, Vaclovas Gedminas
plants, insects (larvae), birds (feathers), rodents
(bones, limbs), and ungulates (hair). In Croatia,
both animal and plant components were found
in thescat of thegolden jackal: themajor com-
ponent was mammals (50.3%), followed by fruit
seeds and vegetables (34.1%), insects (29.5%),
birds (including eggs; 24.8%), articial materi-
als (24%), and branches, leaves, and grass (24%)
(Radovic, Kovačic, 2010).
CONCLUSIONS
Result of analysis of asample of unknown ani-
mal from Lithuania revealed that it was agold-
en jackal. Similar genetic patterns based on
mtDNA control region sequences were iden-
tied in animals from Bulgaria, Croatia, Italy,
Serbia, and theCaucasus. No tick-borne patho-
gens were found in thegolden jackal, however,
theukes Apophallus donicus, nematodes Unci-
naria stenocephala, and unidentied individu-
als of class Cestoda were detected.
ACKNOWLEDGEMENTS
e authors would like to thank thehunters for
thegolden jackal sample.
Received 8 October 2017
Accepted 12 April 2018
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AlgimantasPaulauskas, IrmaRažanskė,
Jana Radzijevskaja, DovilėNugaraitė,
VaclovasGedminas
PAPRASTASIS ŠAKALAS CANIS AUREUS –
NAUJA RŪŠIS BALTIJOS ŠALYSE
Santrauka
Pirmą kartą paprastasis šakalas (Canis aureus)
Estijoje buvo pastebėtas 2013 m. vasario28d.,
Latvijoje pirmieji trys paprastieji šakalai buvo su-
medžioti 2014 metais. Lietuvoje pirmasis šakalas
sumedžiotas 2015m. vasario7d., šio gyvūno rūšies
identikacija atlikta remiantis morfologine ir mole-
kuline (mitochondrinės DNR) analize. Ankstesniais
tyrimais nustatyta, kad paprastieji šakalai gali būti
žarnyno helmintų ir zoonotinės kilmės ligų perne-
šėjai. Dabar buvo atlikti erkių pernešamų patogenų
ir žarnyno parazitų tyrimai. Erkių pernešamų pa-
togenų (Anaplasma phagocytophilum, Babesiasp.,
Bartonellasp.) paprastojo šakalo blužnies pavyzdyje
nerasta, žarnyne buvo aptiktos siurbikės (Apophallus
donicus), apvaliosios kirmėlės (Uncinaria steno-
cephala) ir neidentikuotos rūšies kaspinuočių
(Cestoda) klasės individai.
Raktažodžiai: Canis aureus, mitochondrinė
DNR, helmintai, Uncinaria stenocephala, Apophallus
donicus, kaspinuočiai