Open Access

A synoptic overview of golden jackal parasites reveals high diversity of species

Parasites & Vectors201710:419

https://doi.org/10.1186/s13071-017-2329-8

Received: 28 April 2017

Accepted: 11 August 2017

Published: 15 September 2017

Abstract

The golden jackal (Canis aureus) is a species under significant and fast geographic expansion. Various parasites are known from golden jackals across their geographic range, and certain groups can be spread during their expansion, increasing the risk of cross-infection with other carnivores or even humans. The current list of the golden jackal parasites includes 194 species and was compiled on the basis of an extensive literature search published from historical times until April 2017, and is shown herein in synoptic tables followed by critical comments of the various findings. This large variety of parasites is related to the extensive geographic range, territorial mobility and a very unselective diet. The vast majority of these parasites are shared with domestic dogs or cats. The zoonotic potential is the most important aspect of species reported in the golden jackal, some of them, such as Echinococcus spp., hookworms, Toxocara spp., or Trichinella spp., having a great public health impact. Our review brings overwhelming evidence on the importance of Canis aureus as a wild reservoir of human and animal parasites.

Keywords

Golden jackal Canis aureus Parasites

Background

The golden jackal, Canis aureus (Carnivora: Canidae) is a medium-sized canid species [1] also known as the common or Asiatic jackal [2], Eurasian golden jackal [3] or the reed wolf [4]. Traditionally, Canis aureus has been regarded as a polytypic species (Table 1), with 14 subspecies distributed across a vast geographical territory in Europe, Asia and Africa [5, 6]. Recently, phylogenetic studies have demonstrated that at least two of the African subspecies need a formal recognition as distinct species. Koepfli et al. [3] suggested that C. aureus anthus forms a distinct monophyletic lineage to C. aureus and should be recognized as a separate species. Similarly, the phylogenetic comparison of the Egyptian jackal (C. aureus lupaster) with other wolf-like canids showed a close relationship with the gray wolf species complex rather than with other subspecies of golden jackals [7]. Nevertheless, because most of the studies dealing with parasites of golden jackals do not mention the subspecies, for the purpose of this review we have considered the entire group, without excluding the two former subspecies.
Table 1

Subspecies and geographical distribution of the golden jackal, Canis aureus

Subspecies

Common name

Range

Synonyms

Canis a. aureus Linnaeus, 1758

Common jackal

Middle Asia; Afghanistan; Iran; Iraq; Arabian Peninsula; Baluchistan; northwestern India

C. balcanicus; C. caucasica; C. dalmatinus; C. hadramauticus; C. hungaricus; C. kola; C. lanka; C. maroccanus; C. typicus; C. vulgaris

Canis a. algirensis Wagner, 1841

Algerian wolf

Algeria; Morocco; Tunisia

C. barbarus; C. grayi; C. tripolitanus;

Canis a. anthus Cuvier, 1820

Senegalese wolf; grey jackal; slender jackal

Senegal

C. senegalensis

Canis a. bea Heller, 1914

Serengeti wolf; Serengeti jackal

Kenya; northern Tanzania

 

Canis a. cruesemanni Matschie, 1900

Siamese jackal; South East Asian jackal

Thailand; Myanmar; East India

 

Canis a. ecsedensis Kretzoi, 1947

Pannonian jackal

Pannonian Basin

C. minor; C. balcanicus; C. hungaricus

Canis a. indicus Hodgson, 1833

Indian jackal; Himalayan jackal

Pakistan; India; Nepal; Bhutan; Burma

 

Canis a. lupaster Hemprich & Ehrenberg, 1833

African wolf; Egyptian wolf; Egyptian jackal

Egypt; Algeria; Mali; Ethiopian Highlands; Senegal

C. lupaster; C. lupus lupaster; C. sacer

Canis a. moreoticus Geoffroy Saint-Hilaire, 1835

European jackal; Caucasian jackal; Reed wolf

Southeastern Europe; Asia Minor; Caucasus

C. graecus

Canis a. naria Wroughton, 1916

Sri Lankan jackal

Southern India; Sri Lanka

C. lanka

Canis a. palaestina Khalaf, 2008

 

Palestine; Israel

 

Canis a. riparius Hemprich & Ehrenberg, 1832

Somali wolf

Somalia; Ethiopia; Eritrea

C. hagenbecki; C. mengesi; C. somalicus

Canis a. soudanicus Thomas, 1903

Variegated wolf; Nubian wolf

Sudan; Somalia

C. doederleini; C. nubianus; C. thooides; C. variegatus

Canis a. syriacus Hemprich & Ehrenberg, 1833

Syrian jackal

Israel; Lebanon; Jordan

 

The distribution of golden jackals is limited to the Old World [8]. Molecular evidence supports an African origin for all wolf-like canids including the golden jackal [8]. It is considered that the colonization of Europe by the golden jackal took place during the late Holocene and early Neolithic, through the Balkan Peninsula [9]. During the last century, the species has recorded at least two geographic expansion events. A notable expansion started in the 1950s, with a second one following during the 1980s. This is particularly evident in Europe. Stable reproductive populations have been recorded in about 20 European countries, while in other nine, vagrant specimens were observed [10]. The factors that facilitate the territorial expansion of golden jackals are unclear, but land use [11], climate change [12, 13], and the lack of intra-genus competition have been suggested [1214].

Golden jackals have an opportunistic nutritional behaviour with an extremely varied diet [15]. They prey or scavenge on small mammals, birds and their eggs, amphibians, reptiles, even invertebrates, and they take carrion when available. Occasionally, jackals also feed on vegetables or fruits. Additionally, their relatively broad home range, varying from 1.1 to 20.0 km2 [16, 17], increases the chance of contact with various parasites but also with other hosts.

All these biological and behavioural features create premises for their infection with a broad range of pathogens, including parasites. Golden jackals are known to host a large spectrum of viral, bacterial and parasitic pathogens [1820]. The literature survey indicates that the studies published on golden jackal parasites are usually limited to a country or, more commonly to a region, and there is no synoptic overview on this potentially important topic. The aim of the present work was to review all the published data on the parasite fauna of golden jackals in a comprehensive and updated list. The goal is consistent with the demographic and territorial expansion tendency of this species and increased contact with domestic animals and humans.

Literature survey methodology

The list of the golden jackal parasites was compiled on the basis of an extensive literature search published from historical times until April 2017. Abstracts in conference proceedings and theses were also considered. The search queries were performed in the several databases: Pub Med [21], Science Direct [22], Web of Science [23], Helminthological Abstracts [24], Biological Abstracts [25], BioOne [26], Host-Parasite Database of the Natural History Museum (London) [27] and the web search engine Google Scholar [28]. Additionally, two Russian databases, namely the Russian Scientific Electronic Library [29] and the Scientific Library Earth Papers [30] were also used as sources of information.

The parasites are listed in tables, organized according to their taxonomic rank, and species within families are alphabetically listed. Taxonomy follows Adl et al. [31] for protists; Gibson et al. [32], Jones et al. [33], and Bray et al. [34] for trematodes; Kahlil et al. [35] and Nakao et al. [36] for cestodes; De Ley & Blaxter [37] for nematodes; Amin [38] for acanthocephalans; and the database “Catalogue of Life: 2016 Annual Checklist” by Roskov et al. [39] for arthropods. The names of the species were updated according to the current taxonomy, but synonyms used by different authors are also indicated. Each species is indexed together with the country of the report, the method of examination and reference. The records within a species are listed according to the alphabetical order of the country name. If two or more reports for the same country are registered, the ranking was made chronologically, according to the year publication. The prevalence, frequency and intensity of infection are also given, when available. The prevalence was provided or calculated only when the sample size was at least 10. In the case of experimental infection studies, the country has not been specified. Articles that report infections in captive jackals and doubtful records are mentioned and/or discussed accordingly.

Protists

Eight families with 21 species were reported in golden jackals in 23 countries. Additionally, several protists were identified only to the generic level or were doubtfully considered as parasites of golden jackals (Table 2) [4085].
Table 2

Protist parasites of the golden jackal, Canis aureus

Family

Species

Origin

Prevalence (%)

Frequency

Method

Reference

Phylum Apicomplexa

Class Aconoidasida

Babesiidae

Babesia canis (syn. Piroplasma canis)

na (as P. canis)

na

na

EI

[40]

Nigeriaa

na

1/6

BS

[41]

Romania

9.2

5/54

MI

[42]

Babesia gibsoni

na

na

na

EI

[43]

India

na

na

BS

[44]

Theileriidae

“Theileria annae”

Romania

3.7

2/54

MI

[42]

Class Conoidasida

      

Eimeriidae

Eimeria sp.b

Bulgaria

5.8

3/56

CO

[45]

Eimeria aurei b

India

na

na

CO

[46]

Isospora sp.

Bulgaria

5.8

3/56

CO

[45]

 

Indiaa

case report

 

CO

[47]

 

Iran

7.1

4/56

CO

[48]

 

Serbia

6.6

4/60

CO

[49]

Isospora dutoiti

former USSR

na

na

CO

[50]

 

Turkmenistan

na

na

CO

[51]

Isospora kzilordiniensis

Kazakhstan

na

2/9

CO

[52]

Isospora neorivolta

Russia

9.3

14/150

CO

[53]

Isospora ohioensis

Russia

5.3

8/150

CO

[53]

Isospora theileri

Azerbaijan

na

na

CO

[54]

Turkmenistan

na

na

CO

[51]

Hepatozoidae

Hepatozoon sp.

Algeria

na

2/5

MI

[55]

Mauritania

25.0

4/16

MI

[55]

Hepatozoon canis

Austria

case report

 

MI

[56]

 

case report

 

MI

[42]

Croatia

30.4

14/46

MI

[57]

Czech Republic

na

1/1

MI

[42]

Hungary

57.9

33/57

MI

[57]

 

60.0

na

MI

[58]

Israel

2.1

1/46

BS

[19]

Montenegro

na

2/2

MI

[57]

Romania

72.2

39/54

MI

[42]

Serbia

67.5

140/206

MI

[57]

Sarcocystidae

Cystoisospora canis

Hungary

15.0

3/20

CO

[59]

Neospora caninum

Israel

1.7

2/114

IFAT

[60]

Sarcocystis sp.

Bulgaria

1.9

1/56

CO

[45]

Sarcocystis cruzi (syn. S. bovicanis)

Russia (as S. bovicanis)

20.0

30/150

CO

[53]

Sarcocystis tenella (syn. S. ovicanis)

Russia (as S. ovicanis)

34.0

51/150

CO

[53]

Sarcocystis tropicalis (syn. Isospora tropicalis)

India (as I. tropicalis)

case report

 

CO

[61]

 

India

case report

 

CO

[62]

Toxoplasma-type oocysts

Hungary

5.0

1/20

CO

[59]

Toxoplasma gondii

Iran

33.3

na

LAST

[63]

 

77.5

31/40

ELISA

[64]

“Flagellates”c

Hexamitidae

Giardia sp.

Iraqa

100

4/4

CO

[65]

Giardia duodenalis (syn. G. canis)

Croatia

12.5

1/8

IF, MI

[66]

Iran

7.1

4/56

CO

[48]

Russia (as G. canis)

1.3

2/150

CO

[53]

Trichomonadidae

Pentatrichomonas hominis (syn. P. canis auri)

India (as P. canis auri)

case report

 

CO

[67]

Trypanosomatidae

Leishmania sp.

Iran

2.5

4/161

SIO

[68]

 

12.5

6/48

IFA

 

Serbia

6.9

15/126

MI

[69]

Spaina

case report

 

H

[70]

Leishmania donovani

Bangladesh

5 cases

na

MI

[71]

Georgia

na

1/4

SIO

[72]

Kazakhstan

na

na

na

[73]

Iran

5.0

1/20

SIO

[74]

na

na

na

EI

[75]

Leishmania infantum

Algeria

case report

 

IFI, MI

[76]

Georgia

2.5

1/39

IA

[77]

Iran

10.0

1/10

DAT, ELISA, IFAT

[78]

 

11.6

7/60

DAT

[78]

 

1.6

1/60

SIO

 

Iraq

59.6

90/151

SIO, Cult, IFAT, ELISA

[79]

Israel

7.6

4/53

ELISA

[80]

 

6.5

3/46

ELISA

[19]

 

1.3

1/77

MI

[81]

Kazakhstan

na

na

na

[82]

Romania

2.7

1/36

MI

[42]

Tajikistan

na

na

na

[83]

Turkmenistan

2 specimens

na

na

[84]

Leishmania major

na

na

na

EI

[85]

Leishmania tropica

Israel

6.5

5/77

na

[81]

Abbreviations: BS blood smear May-Grünwald-Giemsa stained, CO coprological examination, Cult cultures from the viscera, blood and other tissues, DAT direct agglutination test, EI experimental infection, ELISA enzyme-linked immunosorbent assay, H histopathology, IA immunochromatographic assay, IF immunofluorescence assay, IFAT indirect fluorescent antibody test, IFI indirect fluorescent immunoassay, LAST latex agglutination slide test, MI- molecular identification, SIO smears from internal organs stained with standard Giemsa, na not applicable/unknown

aAnimals kept in captivity

bDoubtful record

cVarious opinions on the higher taxonomy of these groups are available, hence we keep the generic term “flagellates”

Leishmania

The sand fly-borne kinetoplastids of the genus Leishmania were reported in golden jackals from 13 countries (Table 2), showing a large geographical distribution in Asia, Africa and Europe. At least three species of Leishmania have been identified by molecular methods in naturally infected golden jackals (L. donovani, L. infantum and L. tropica). Additionally, golden jackals were experimentally shown to be receptive for the infection with L. major [85], but this species has never been found in naturally infected specimens. The multiple records of Leishmania spp. in golden jackals suggest a reservoir role for this carnivore, for both visceral and cutaneous leishmaniasis in humans, as well as for canine leishmaniasis. Infected jackals have been found also at the margin of the endemic area for canine leishmaniasis (i.e. Romania), where this finding has been temporally correlated with the re-emergence of the disease in domestic dogs [86]. Although there is no clear link between the emergence of leishmaniasis in dogs and the spreading of jackals, this is an issue to be further investigated, mainly as the jackal continues to spread into areas at the margin of canine leishmaniasis endemicity. This was previously demonstrated when infected dogs were newly introduced to non-endemic areas in Europe [87].

Tick-borne protists (Babesiidae, Theileriidae and Hepatozoidae)

Experimental evidence showed that golden jackals are receptive to the infection with Babesia canis [40] and B. gibsoni [43]. However, there are surprisingly few records of natural infections with piroplasms in golden jackals (Table 2) despite the large variety and number of studies on ticks (see below). In Europe, the only Babesia species molecularly confirmed in golden jackals is B. canis, recently reported in Romania [42]. The other report of B. canis in jackals is from Nigeria [41], but the species identification was based on blood smears and in captive animals. We consider this record doubtful, as the typical vector for B. canis, Dermacentor reticulatus, does not occur in Nigeria. Probably the species in this case belongs to the same complex group of large canine Babesia known in this area, B. rossi or B. vogeli [88]. Babesia gibsoni, which is widely distributed in Asia, has been reported only once in golden jackals, in India. Although Babesia rossi is common in domestic and wild carnivores in Africa [89], so far there are no records of this species in golden jackals. The scarcity of reports of Babesia spp. in this wild canid is probably related to the low number of studies and the lack of more sensitive/specific methods, as the typical vector ticks [D. reticulatus for B. canis, Rhipicephalus sanguineus (sensu lato) for B. vogeli and Haemaphysalis leachi for B. rossi] have been reported on various occasions on these hosts.

An interesting recent report indicates the presence of “Theileria annae” in golden jackals from Romania [42]. Currently, the taxonomic status of this species is debated and it is most commonly referred to as “Babesia microti-like”. This group has been reported predominantly in red foxes, but also in several other wild carnivores in North America, Asia and Europe [89]. However, so far, the role of golden jackals in its ecology remains unknown.

The first report of Hepatozoon canis in golden jackals is relatively recent [19] and has been followed in the last years by several records, mainly in Europe and North Africa (Table 2). Surprisingly, despite the wide distribution of H. canis in canids [90], this tick-borne apicomplexan has never been found in jackals from sub-Saharan Africa or Asia. Nevertheless, the large number of records and the presence of its main vector, R. sanguineus (s.l.) suggest a reservoir role of golden jackals for H. canis at least in Europe, Middle East and North Africa.

Intestinal homoxenous coccidia (Eimeriidae)

Various species of intestinal coccidia of the family Eimeriidae have been found in, or even described from jackals (Table 2). We consider all records of Eimeria as pseudoparasites, as previously suggested [91]. Three species of the genus Isospora have been described from golden jackals but currently their taxonomic status is listed as doubtful [91]: Isospora dutoiti is a misidentification with Hammondia spp. or Neospora caninum, while I. theileri and I. kzilordiniensis are probably invalid names (as they might be synonyms with other Isospora species from canids). Two other species, I. neorivolta and I. ohioensis, which are known to infect several species of canids [91], were reported in golden jackals. Interestingly, all these Isospora reports in golden jackals are from countries in the former USSR, and this probably reflects a greater interest of researchers from this area for this group of parasites rather than the real geographical distribution. Few reports of unnamed Isospora sp. in golden jackals are known from Asia and the Balkans (Table 2).

Heteroxenous coccidia (Sarcocystidae)

Various records list golden jackals host to Sarcocystidae. Sporocysts of Sarcocystis (S. cruzi, S. tenella and S. tropicalis) and oocysts of Cystoisospora canis have been reported in the faeces of golden jackals in Europe, Russia and India, suggesting their role as definitive hosts (Table 2). Although antibodies against Neospora caninum have been detected in C. aureus in Israel [60], the role of golden jackals as definitive hosts for this parasite has never been demonstrated and needs to be investigated. So far, various canid species were demonstrated to shed oocysts of N. caninum: dogs (Canis familiaris) [92], coyotes (C. latrans) [93], dingoes (C. lupus dingo) [94], and gray wolves (C. lupus) [95]. Interestingly, Takacs et al. [59] reported “Toxoplasma-like” oocysts in the faeces of jackals but, unfortunately, no morphometric data were provided and there was no attempt to characterize them molecularly. We can only assume that these were small oocysts which, in our opinion, could represent any of the small canine coccidia N. caninum, Besnoitia spp. or Hammondia spp., none of them confirmed so far in golden jackals.

Helminths

The highest number of studies on the parasitic fauna of golden jackals are related to helminths. Our literature survey found at least 178 publications in 38 countries reporting helminths in golden jackals, with 119 species belonging to three phyla: Platyhelminthes, Nematoda and Acanthocephala [96119].

Trematodes

The diversity of trematodes in golden jackals is relatively high (27 species from nine families) (Table 3). Most of the studies originate in the countries of the former USSR, Asia and North Africa, with few scattered records in Europe. There are no trematodes recorded in golden jackals in sub-Saharan Africa. This situation reflects probably the impact of the Russian helminthological school and the lack of studies in other regions rather than the influence of ecological factors or feeding behaviour of jackals. Among the various records of trematodes in golden jackals, two groups could be identified: the canid- or Carnivora-specific trematodes and other trematodes (specific rather to other mammal groups or birds).
Table 3

A comprehensive list of trematode parasites of the golden jackal, Canis aureus

Family

Species

Origin

Prevalence (%)

Frequency

Intensity

Method

Reference

Phylum Platyhelminthes

      

Class Trematoda

       

Dicrocoeliidae

Dicrocoelium dendriticum (syn. D. lanceatum)

Russia

5.0

1/20

5.00 ± 4.45

necropsy

[96]a

26.1

na

na

necropsy

[97]

na

na

na

necropsy

[98]

Diplostomidae

Alaria alata

Azerbaijan

22.4

20/89

2–30

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

9.0

na

na

necropsy

[101]

1.9

1/56

na

necropsy

[45]

Croatia

na

na

na

na

[102]

Chechnya

100

16/16

22–268

necropsy

[103]

Greece

20.0

1/5

na

necropsy

[104]

Hungary

10.0

2/20

na

necropsy

[59]

Iran

na

na

na

necropsy

[105]

Russia

10.0

2/20

3.00 ± 2.68

necropsy

[96]

34.8

na

na

necropsy

[97]

na

na

na

necropsy

[98]

13.3

8/60

na

necropsy

[106]

na

na

na

necropsy

[107]

26.0

39/150

2–23

necropsy

[53]

Serbia

0.9

4/447

19.00 ± 3.63

necropsy

[108]

30.0

18/60

na

necropsy

[49]

Uzbekistan

na

na

na

na

[109]

Alaria americana (syn. A. canis)b

Iran

5.0

1/20

34

necropsy

[110]

  

10.0

1/10

na

necropsy

[111]

Pharyngostomum cordatum (syn. P. fausti)

Azerbaijan

na

na

na

necropsy

[100]

Azerbaijan (as P. fausti)

8.3

1/12

2

necropsy

[99]

na

na

na

necropsy

[100]

Russia

6.6

4/60

na

necropsy

[106]

Echinostomatidae

Echinochasmus corvus

India

na

na

na

na

[112]

Echinochasmus schwartzi

Iran

na

na

na

necropsy

[105]

Euparyphium sp.

Iran

na

na

na

necropsy

[105]

Euparyphium melis

Russia

16.6

10/60

na

necropsy

[106]

Heterophyidae

Ascocotyle italica (syn. Parascocotyle italica)

Russia

8.3

5/60

na

necropsy

[106]

Ascocotyle sinoecum (syn. Phagicola sinoecum)

Iran

na

na

na

necropsy

[105]

Cryptocotyle lingua b

Russia

2.7

4/150

3–18

necropsy

[53]

Heterophyes sp.

Egypt

na

3/5

na

necropsy

[113]

Heterophyes aequalis

Egypt

na

na

na

necropsy

[113]

Heterophyes dispar

Egypt

na

na

na

necropsy

[113]

Heterophyes heterophyes

Egypt

2 specimens

na

na

necropsy

[113]

Metagonimus ciureanus (syn. Dexiogonimus ciureanus)

Georgia

na

na

na

necropsy

[114]

Metagonimus yokogawai

Iran

14.2

4/28

na

necropsy

[115]

Italy

case report

 

6

necropsy

[116]

Serbia

1.6

1/60

na

necropsy

[49]

Microphallidae

Microphallus narii (syn. Spelotrema narii)

India

na

na

na

na

[117]

na

na

na

na

[112]

Opisthorchiidae

Metorchis xanthosomus b

Russia

21.8

na

na

necropsy

[97]

Opisthorchis sp.

Bangladesh

na

1/5

na

necropsy

[118]

Pseudamphistomum truncatum

Serbia

0.2

1/447

2

necropsy

[108]

3.3

2/60

na

necropsy

[49]

Plagiorchiidae

Plagiorchis sp.

Iran

na

na

na

necropsy

[105]

Plagiorchis elegans b

Russia

3.3

2/60

na

necropsy

[106]

Plagiorchis massino

Uzbekistan

na

na

na

na

[109]

Schistosomatidae

Schistosoma spindale b

India

case report

 

na

CO

[119]

Troglotrematidae

Nanophyetus salmincola b

India

case report

 

na

CO

[47]

Abbreviations: na not applicable/unknown, CO coprological examination

aUnknown site of infection

bDoubtful record

The most commonly reported and widely distributed trematode in golden jackals is Alaria alata, found in Caucasus, Russia and Central Asia to Middle East and the Balkans (Table 3). We consider the report of Alaria americana in Iran doubtful, as the species is known otherwise only in canids from North America [120].

Jackals have been commonly reported as hosts for fish-borne trematodes typically associated with carnivores. Such examples include species of the genera Ascocotyle, Cryptocotyle, Heterophyes, Metagonimus (Heterophyidae), Echinochasmus, Euparyphium (Echinostomatidae), Pseudamphistomum, Opisthorchis (Opisthorchiidae) mainly in Asia and northern Africa. The fish-borne Nanophyetus salmincola was identified in India, but its geographical distribution is limited to the Pacific Northwest of the USA [121]; with high probability, the report might represent a misidentification with N. schikhobalowi, an Asian troglotrematid [122]. The diversity of trematode species in golden jackals is completed by other groups which use various invertebrates (i.e. arthropods) (Plagiorchis massino, Microphallus narii) or non-fish small vertebrates (i.e. amphibians) (Pharyngostomum cordatum) as second intermediate hosts, reflecting the wide diet composition of this carnivore.

Interestingly, Dicrocoelium dendriticum, a hepatic fluke typically associated with herbivores, has been found on several occasions in the bile ducts of golden jackals [97, 98] in Russia. As the infection source for this parasite is represented by ant second intermediate hosts, the infection of jackals is probably accidental.

Several of these trematodes reported in golden jackals have zoonotic potential. Human alariosis caused by Alaria mesocercariae manifests in various clinical signs which range from cutaneous symptoms to respiratory disorders, a diffuse unilateral neuroretinitis even to an anaphylactic shock with fatal outcome [123]. However, all human cases originate in North America (and are probably caused by A. americanum). The zoonotic potential of A. alata in Eurasia remains unknown. Adults Heterophyes dispar and H. heterophyes may produce diarrhoea, abdominal pain and discomfort in humans [124], while Metagonimus yokogawai is considered to be the most common intestinal trematode infection in the Far East, highly important due to the ability of their eggs to invade the blood stream thus causing serious complications [125]. Hence, golden jackals might have a significant role in the environmental contamination with such parasites and represent an indirect source for human contamination. Hepatic and biliary trematodes D. dendriticum, Pseudamphistomum truncatum and Opisthorchis felineus are also able to infect humans, causing abdominal pain, weight loss, chronic relapsing watery diarrhea and hepatobiliary system damages [126, 127].

However, for many other trematode species, golden jackals, as other carnivores, are probably accidental hosts, or most likely, present a pseudoparasitism following ingestion of birds or rodents, as they typically infect other vertebrate groups. For instance, Cryptocotyle lingua is mainly a parasite of different gull species in Europe, North America and Japan [128]; Plagiorchis elegans is a parasite of raptors, waterfowl, passerines and several mammals as the wood mouse, rat, gerbil and hamster [129]; Metorchis xanthosomus is specific for birds in Anseriformes, Gaviiformes, Podicipediformes and Gruiformes [130]; and Schistosoma spindale has been described in ruminants and rodents in southeastern Asia [131].

Cestodes

Cestode infections in golden jackals have been recorded across all their distribution range, with a relatively high species diversity (Table 4) [132152].
Table 4

A comprehensive list of cestode parasites of the golden jackal, Canis aureus

Family

Species

Origin

Prevalence (%)

Frequency

Intensity

Method

Reference

Phylum Platyhelminthes

       

Class Cestoda

       

Dilepididae

Aelurotaenia cameroni

India

na

na

na

na

[132]

Diphyllobothriidae

Diphyllobothrium sp.

Indiaa

na

na

na

CO

[133]

Diphyllobothrium latum

Bangladesh

20.0

6/30

na

necropsy

[134]

 

India

na

na

na

na

[112]

Spirometra sp.

Indiaa

na

na

na

CO

[135]

Iran

7.1

1/14

4

necropsy

[136]

Spirometra erinaceieuropaei (syn. S. erinacei)

Azerbaijan

25.0

19/76

1–19

necropsy

[99]

 

na

na

na

necropsy

[100]

Azerbaijan (as S. erinacei)

3.5

4/114

2–21

necropsy

[137]

Iran (as S. erinacei)

na

na

na

necropsy

[105]

Spirometra houghtoni

Iran

na

na

na

necropsy

[105]

Spirometra mansoni (syn. Bothriocephalus mansoni)

Italy

case report

na

necropsy

[138]

 

Dipylidiidae

Diplopylidium noelleri

Iran

5.0

na

na

necropsy

[139]

Tunisia

16.0

5/31

1–66

necropsy

[140]

Dipylidium caninum (syns Taenia elliptica, T. cucumerina)

Azerbaijan

na

na

na

necropsy

[100]

Bangladesh

26.6

8/30

na

necropsy

[134]

Bulgaria

3.8

na

na

necropsy

[141]

63.6

7/11

na

necropsy

[142]

Chechnya

100

16/16

3–12

necropsy

[103]

Hungary

5.0

1/20

4

necropsy

[59]

India

na

na

na

na

[143]

 

na

na

na

na

[112]

Indiaa

5.0

3/60

na

CO

[144]

Iran

7.1

1/14

4

necropsy

[136]

10.0

4/40

na

necropsy

[145]

20.0

2/10

na

necropsy

[111]

10.1

8/79

na

necropsy

[139]

33.9

19/56

na

necropsy

[48]

Israel

46.6

7/15

na

necropsy

[146]

5.8

1/17

na

CO

[19]

Italy

na

na

na

necropsy

[138]

Kazakhstan

16.6

3/18

2–8

necropsy

[147]

Russia

47.8

na

na

necropsy

[97]

5.0

1/20

1.00 ± 0.25

necropsy

[96]

10.0

6/60

na

necropsy

[106]

na

na

na

necropsy

[107]

8.0

12/150

1–13

necropsy

[53]

Serbia

1.6

7/447

4.8 ± 0.6

necropsy

[108]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

na

1/5

na

necropsy

[149]

16.0

5/31

4–67

necropsy

[140]

Turkey

na

na

na

necropsy

[150]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Joyeuxiella echinorhynchoides

Azerbaijan

30.2

23/76

1–30

necropsy

[99]

na

na

na

necropsy

[100]

Iran

27.8

5/18

na

necropsy

[334]

7.5

3/40

na

necropsy

[145]

Turkey

na

na

na

necropsy

[150]

Joyeuxiella pasqualei

Iran

30.0

3/10

na

necropsy

[111]

Mesocestoididae

Mesocestoides sp. group A (oval to elongate cirrus-pouch and short cirrus)

Israel

8.1

7/86

na

necropsy, ME

[335]

Mesocestoides sp. group B (broad-oval cirrus-pouch and long, more or less strongly coiled cirrus)

Israel

15.2

13/85

na

necropsy, ME

 

Mesocestoides sp.

Greece

na

3/5

na

necropsy

[104]

Tunisia

na

2/5

na

necropsy

[149]

Iran

na

1/1

na

necropsy

[336]

Bulgaria

34.6

na

na

necropsy

[45]

Mesocestoides corti

Azerbaijan

na

na

na

necropsy

[100]

Tunisia

12.9

4/31

1–10

necropsy

[140]

Mesocestoides lineatus (syn. M. carnivoricolus)

Azerbaijan

2.6

3/114

9–47

necropsy

[137]

37.7

37/98

2–63

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

27.0

na

na

necropsy

[101]

72.7

8/11

na

necropsy

[142]

Hungary

20.0

4/20

na

necropsy

[59]

India

na

na

na

na

[112]

India (as M. carnivoricolus)

na

na

na

necropsy

[337]

Ingushetia

na

1/2

na

necropsy

[338]

Iran

15.0

3/20

na

necropsy

[110]

70.0

7/10

na

necropsy

[111]

36.7

29/79

na

necropsy

[139]

30.3

17/56

na

necropsy

[48]

61.1

11/18

na

necropsy

[334]

Russia

26.1

na

na

necropsy

[97]

5.0

1/20

1.00 ± 0.53

necropsy

[96]

40.0

24/60

na

necropsy

[106]

na

na

na

necropsy

[339]

na

na

na

necropsy

[98]

40.0

60/150

1–128

necropsy

[53]

Serbia

5.8

26/447

69.7 ± 9.3

necropsy

[108]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

74.0

23/31

na

necropsy

[140]

Turkey

na

na

na

necropsy

[340]

Ukraine

na

1/1

5

necropsy

[341]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Mesocestoides litteratus

Serbia

4.7

21/447

64.3 ± 15.1

necropsy

[108]

Tunisia

23.0

7/31

6–130

necropsy

[140]

Mesocestoides petrowi

Azerbaijan

na

na

na

necropsy

[100]

Russia

na

na

na

necropsy

[342]

Mesocestoides zacharovae

Azerbaijan

case report

na

necropsy

[343]

 

Taeniidae

Echinococcus granulosus

Azerbaijan

16.3

16/98

2–400

necropsy

[99]

 

na

na

na

necropsy

[100]

Bangladesh

20.0

6/30

na

necropsy

[134]

Bulgaria

23.0

na

na

necropsy

[101]

 

na

3/3

na

PCR

[344]

 

9.0

1/11

na

necropsy

[142]

 

1.9

na

na

necropsy

[45]

Ceylon

case report

7

necropsy

[345]

 

Chad

1.2

1/82

na

necropsy

[346]

Chechnya

na

na

na

necropsy

[347]

 

12.0

2/16

8–16

necropsy

[103]

Chechnya, Ingushetia

na

2/7

74–217

necropsy

[348]

Hungary

10.0

2/20

na

necropsy

[59]

India

na

na

na

CO

[349]

Iran

5.0

1/20

48

necropsy

[110]

 

na

na

na

necropsy

[105]

 

16.0

na

na

necropsy

[350]

 

2.3

2/86

na

necropsy

[351]

 

40.0

16/40

na

necropsy

[145]

 

40.0

16/40

na

necropsy

[352]

 

8.9

7/79

na

necropsy

[139]

 

20.0

2/10

na

necropsy

[353]

 

66.7

6/9

na

CO

[353]

 

na

1/1

na

PCR

[354]

 

3.5

2/56

na

necropsy

[48]

 

na

na

na

PCR

[355]

Italy

case report

1

necropsy

[356]

 

Kazakhstan

5.9

na

3–29

necropsy

[147]

Kenya

27.2

6/22

< 200

necropsy

[357]

Palestine

na

na

na

na

[358]

Pakistan

9.0

9/100

na

necropsy

[359]

Russia

12.5

2/16

na

necropsy

[360]

 

82.6

na

na

necropsy

[97]

 

69.8

na

na

necropsy

[361]

 

5.0

1/20

4.00 ± 2.36

necropsy

[96]

 

66.0

10/15

na

CO

[362]

 

3.3

2/60

na

necropsy

[106]

 

na

na

na

necropsy

[107]

Tajikistan

30.7

4/13

> 1,000

necropsy

[363]

Tunisia

na

1/5

72

necropsy

[149]

 

na

2/2

na

PCR

[364]

 

9.7

3/31

11–98

necropsy

[140]

E. multilocularis (syn. Alveococcus multilocularis)

Azerbaijan

3.7

2/54

3–5

necropsy

[99]

Hungary

9.0

1/11

412

necropsy

[365]

Ingushetia

na

1/2

na

necropsy

[338]

Iran

16.0

4/25

na

necropsy

[366]

 

50.0

5/10

na

necropsy

[353]

 

na

9/9

na

CO

[353]

Russia (as Alveococcus multilocularis)

18.7

3/16

na

necropsy

[360]

Serbia

14.3

4/28

4–57

necropsy

[367]

Tajikistan

7.7

1/13

na

necropsy

[363]

Uzbekistan

na

1/4

na

necropsy

[368]

Multiceps multiceps (syn. Taenia multiceps

Azerbaijan

8.9

8/89

2–11

necropsy

[99]

 

na

na

na

necropsy

[100]

Bangladesh (as T. multiceps)

10.0

3/30

na

necropsy

[134]

Bulgaria

9.0

na

na

necropsy

[101]

 

9.0

1/11

 

necropsy

[142]

Chechnya

na

na

na

necropsy

[347]

Iran

7.5

3/40

 

necropsy

[145]

India

na

na

na

necropsy

[369]

Kazakhstan

11.1

2/18

4–16

necropsy

[147]

Russia

39.1

na

na

necropsy

[97]

Serbia

1.6

7/447

3.00 ± 0.53

necropsy

[108]

Tajikistan

na

2/6

na

necropsy

[370]

Ukraine

na

1/1

na

necropsy

[341]

Taenia serialis

Kazakhstan

5.5

1/18

10

necropsy

[147]

Kenya

na

2/2

42

PCR

[371]

Serbia

1.1

5/447

2.7 ± 0.2

necropsy

[108]

Taenia sp.

Bulgaria

23.0

na

na

necropsy

[141]

Greece

na

1/5

na

necropsy

[104]

India

na

na

na

na

[143]

Indiaa

11.6

7/60

na

CO

[144]

Irana

na

2/2

11 ± 2 epg

CO

[372]

Kenya

60.0

3/5

na

necropsy

[373]

Tunisia

19

6/31

1–29

necropsy

[140]

Taenia crassiceps

Azerbaijan

na

na

na

necropsy

[100]

Hungary

40.0

8/20

na

necropsy

[59]

Russia

25.0

15/60

na

necropsy

[106]

Taenia hydatigena (syn. T. marginata)

Azerbaijan

15.3

14/91

1–18

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

55.0

na

na

necropsy

[101]

27.2

3/11

na

necropsy

[142]

Chechnya

na

na

na

necropsy

[347]

50.0

8/16

3–6

necropsy

[103]

Hungary

15.0

3/20

na

necropsy

[59]

India

na

na

na

necropsy

[369]

Iran

7.1

1/14

2

necropsy

[136]

40.0

16/40

na

necropsy

[145]

10.0

1/10

na

necropsy

[111]

7.6

6/79

na

necropsy

[139]

7.1

4/56

na

necropsy

[48]

5.6

1/18

na

necropsy

[334]

Italy (as T. marginata)

na

na

na

na

[138]

Kazakhstan

22.0

4/18

2–8

necropsy

[147]

Russia

6.2

1/16

na

necropsy

[360]

36.8

14/38

1–3

necropsy

[374]

34.8

na

na

necropsy

[97]

5.0

1/20

3.00 ± 2.18

necropsy

[96]

1.6

1/60

na

necropsy

[106]

na

na

na

necropsy

[98]

na

na

na

necropsy

[107]

Serbia

0.9

4/447

3.75 ± 1.80

necropsy

[108]

Tajikistan

na

na

na

necropsy

[148]

Uzbekistan

na

na

na

necropsy

[152]

Taenia krabbei

Azerbaijan

0.8

1/114

3

necropsy

[137]

na

na

na

necropsy

[100]

Taenia krepkogorski (syn. Hydatigera krepkogorski)

Azerbaijan

na

na

na

necropsy

[100]

Taenia ovis

Azerbaijan

5.1

2/39

1–2

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

case report

 

na

necropsy

[375]

Iran

5.6

1/18

 

necropsy

[334]

Russia

39.1

na

na

necropsy

[97]

Tajikistan

na

na

na

necropsy

[148]

USSR (former)

na

na

na

necropsy

[376]

Taenia pisiformis (syn. T. serrata)

Azerbaijan

15.7

14/89

1–6

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

18.0

na

na

necropsy

[101]

54.5

6/11

 

necropsy

[142]

Chechnya

100

16/16

3–18

necropsy

[103]

Greece

na

1/5

na

necropsy

[104]

Hungary

20.0

4/20

na

necropsy

[59]

India (as T. serrata)

na

na

na

na

[377]

na

na

na

necropsy

[369]

Iran

na

na

na

necropsy

[105]

Kazakhstan

5.5

1/18

3

necropsy

[147]

Russia

17.4

na

na

necropsy

[97]

3.3

2/60

 

necropsy

[106]

na

na

na

necropsy

[107]

16.7

25/150

1–3

necropsy

[53]

Serbia

1.8

8/447

10.1 ± 2.1

necropsy

[108]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

3.2

1/31

1

necropsy

[140]

Taenia polyacantha (syn. Tetratirotaenia polyacantha)

Azerbaijan (as Tetratirotaenia polyacantha)

na

na

na

necropsy

[100]

Turkey

na

na

na

necropsy

[340]

Taenia taeniaeformis (syn. Hydatigera taeneiformis)

Azerbaijan (as H. taeneiformis)

na

na

na

necropsy

[100]

Tajikistan

na

na

na

necropsy

[148]

Uzbekistan

na

na

na

necropsy

[152]

Abbreviations: CO coprological examination; ME microscopic/morphological examination; PCR polymerase chain reaction; epg eggs per gram faeces; na not applicable/not available

aAnimals kept in captivity

Among all the cestode species, Aelurotaenia cameroni is the only one known exclusively in the golden jackal. However, as the species was only recently described [132], its absence from other carnivores cannot be excluded until further studies. It is not surprising that all other identified tapeworm species are characteristic to carnivores, confirming the low specific affinity of the adult parasites [153]. As such species infect usually a wider range of canid or non-canid carnivores, this demonstrates a close environmental connection between multiple carnivore species and the use of the same trophic source.

The most commonly reported tapeworms in golden jackals are Dipylidium caninum, Mesocestoides spp., Echinococcus granulosus and Taenia spp., found across a wide geographical range (Europe, Asia and Africa). The cosmopolitan character of all these cestodes is attributed to the abundance and diversity of intermediate hosts and the lack of specificity for the definitive hosts [153]. Hence, the jackal, together with other carnivores, represents an important source of environmental contamination. Several of these species are known to be zoonotic, some with a minor impact (i.e. D. caninum), but other being a major public health threat (i.e. E. granulosus).

Dipylidium caninum occurs across the globe, human cases being reported in European and Asian countries after accidental ingestion of the infected cat and dog fleas with cysticercoid larvae [154]. Although the jackal is not a domestic species, hence not a direct source of infection to humans, it may transmit fleas to hunting, shepherd or stray dogs and participates together with other wild canids in the natural cycle of this cestode.

Several species of the genus Mesocestoides have been found in golden jackals in various regions. Mesocestoides lineatus is spread in Africa, Asia and Europe; it was rarely found in humans, with about 20 cases being described to date across the world [155]. Although the main definitive hosts are carnivores, humans can also act as accidental final hosts following ingestion of raw or undercooked meat of birds, amphibians, reptiles or small mammals [156]. The zoonotic potential of the other species of Mesocestoides in unknown.

The most well-represented family of tapeworms found in jackals is the Taeniidae. The high diversity of the Taeniidae in golden jackals reflects furthermore the wide range of mammalian prey species on which they feed. Golden jackals are hosts to both zoonotic species of Echinococcus. Echinococcus granulosus and E. multilocularis have been reported in this wild canid on multiple occasions and across a wide geographical range. The unilocular or cystic hydatidosis produced by larvae of E. granulosus (sensu lato) is a ubiquitous infection with high prevalence in various parts of the world [157]. Human multilocular or alveolar echinococcosis caused by E. multilocularis has recorded a significant increase in the incidence in northern Eurasia since 1990 [157, 158]. In several regions, high prevalences with both species were reported in golden jackals (Table 4). Reports of Echinococcus spp. in areas where this canid has recently spread or increased in abundance (i.e. central and eastern Europe) raise the important question on its role as a potentially new natural reservoir and infection source for humans and livestock.

Among species of genus Taenia and Multiceps, the most commonly reported species in golden jackals are T. hydatigena, T. pisiformis, T. ovis and M. multiceps. Other species (T. polyacantha, T. taeniaeformis, T. krabbei, T. krepkogorski, T. crassiceps and M. serialis) have been also found but only occasionally, mainly within the limited geographical range of Caucasus and central Asia (Table 4). The zoonotic potential of these species is limited, and only few human cases have been reported so far: T. taeniaeformis [159162], T. crassiceps [163], T. hydatigena [164], T. ovis [165, 166], M. multiceps and M. serialis [167]. Taenia krabbei, T. krepkogorski and T. polyacantha are considered non-zoonotic tapeworms [158, 168]. Considering the common findings of a wide range of Taeniidae in golden jackals, the high spatial mobility of these hosts and the high resistance of taeniid eggs in the environment [169], the role of jackals as natural reservoirs and infection source for humans and domestic animals should be considered potentially important.

Species of Spirometra (Diphyllobothriidae) identified in golden jackals from Europe and Asia (S. mansoni, S. houghtoni and S. erinaceieuropaei) cause sparganosis in intermediate hosts. Humans may acquire the infection after drinking water contaminated with infected copepods or by ingestion of uncooked meat, and occasionally may lead to blindness, paralysis, and death [170, 171]. Diphyllobothrium latum is also reported in humans due to consumption of raw or undercooked fish, in cold water areas from the Holarctic Eurasia, overlaid to those regions where the species is recorded in jackal [172]. However, due to the limited number of reports, the role of golden jackals in the natural cycle of these diphyllobothriid cestodes remains unknown.

Tapeworm species with a limited geographic distribution are also reported in jackals. Diplopylidium noelleri and Joyeuxiella spp. are spread only in warm regions from Asia and Europe, probably due to the high abundance and diversity of reptiles, known as common intermediate hosts [173].

Acanthocephalans

Although the diet of golden jackals generally includes invertebrates, wild birds, reptiles and small mammals which are intermediate or paratenic hosts in the life-cycle of thorny-headed worms [174176], compared to other groups of helminths, there are only few and geographically limited reports of acanthocephalans in golden jackals. The diversity of acanthocephalans identified in this canid includes at least six species (Table 5) [176181].
Table 5

Acanthocephalan parasites of the golden jackal, Canis aureus

Family

Species (synonym)

Origin

Prevalence (%)

Frequency

Intensity

Method

Reference

Class Archiacanthocephala

 Oligacanthorhynchidae

Macracanthorhynchus sp.

Iran

10.0

1/10

 

necropsy

[111]

Macracanthorhynchus catulinus

Azerbaijan

0.8

1/114

24

necropsy

[137]

 

17.0

14/82

1–6

necropsy

[99]

 

na

na

na

necropsy

[100]

Bulgaria

3.8

na

na

necropsy

[45]

Kazakhstan

5.5

1/18

3

necropsy

[147]

Russia

6.6

4/60

n/a

necropsy

[106]

 

6.7

10/150

1–6

necropsy

[53]

Tajikistan

na

na

na

necropsy

[148]

Turkmenistan

na

na

na

necropsy

[177]

Macracanthorhynchus hirudinaceus a

Tunisia

na

1/5

na

necropsy

[149]

3.2

1/31

6

necropsy

[140]

Iran

case report

 

na

necropsy

[178]

62.5

25/40

na

necropsy

[179]

30.0

3/10

na

necropsy

[111]

5.0

4/79

na

necropsy

[139]

3.5

2/56

na

necropsy

[48]

Oncicola sp.

Iran

na

na

na

necropsy

[178]

Oncicola canis

Iran

case report

 

na

necropsy

[178]

12.6

10/79

na

necropsy

[139]

Pachysentis canicola

Iran

case report

 

na

necropsy

[180]

Class Palaeacanthocephala

 Centrorhynchidae

Centrorhynchus itatsinis

Azerbaijan

1.4

1/71

na

necropsy

[181]

na

na

na

necropsy

[100]

Incertae sedis

Echinorhynchus pachyacanthus

Italy

na

na

na

necropsy

[138]

Abbreviation: na not applicable/not available/no answer

aDoubtful record

Macracanthorhynchus catulinus has been reported on several occasions in jackals in former USSR and Bulgaria, while the congeneric species M. hirudinaceus was found only in Tunisia and Iran. It is unclear if the reports of M. hirudinaceus (a parasite typically found in pigs; [155]) represent cases of pseudoparasitism or misidentifications with M. catulinus (a parasite typically found in canids), as most papers referring to these findings do not provide details on the identification methods. There are few scattered records of other carnivore-specific acanthocephalan species in golden jackals (Oncicola canis, Pachysentis canicola, Centrorhynchus itatsinis and Echinorhynchus pachyacanthus) in central Asia and Italy (Table 5).

Nematodes

Nematodes constitute the most well-represented group of parasites in golden jackals, with 41 species identified (28 species in Chromadorea and 13 species in Enoplea) (Table 6) [182256].
Table 6

Nematode parasites of the golden jackal, Canis aureus

Family

Species (synonym)

Origin

Prevalence (%)

Frequency

Intensity

Method

Reference

Phylum Nematoda

Class Chromadorea

Ancylostomatidae

Ancylostoma sp.

Indiaa

na

3/3

na

CO

[182]

na

5/5

na

CO

[183]

31.6

19/60

na

CO

[144]

case report

 

700 epg

CO

[184]

case report

 

na

CO

[47]

Irana

na

2/2

10.5 epg

CO

[372]

Ancylostoma/Uncinaria sp.

Bulgaria

84.6

na

na

necropsy

[141]

Indiaa

na

na

na

CO

[135]

India

na

3/6

na

CO

[185]

Iran

na

na

na

necropsy

[105]

Serbia

33.3

20/60

na

necropsy

[49]

Tunisia

na

5/5

na

necropsy

[149]

Ancylostoma braziliense b

India

na

na

na

na

[117]

Ancylostoma caninum

Azerbaijan

17.3

17/98

1–20

necropsy

[99]

na

na

na

necropsy

[100]

Bangladesh

46.6

14/30

na

necropsy

[134]

Bulgaria

54.5

6/11

na

necropsy

[142]

11.5

na

na

necropsy

[45]

Chechnya

50.0

8/16

3–18

necropsy

[103]

Egypt

na

na

na

necropsy

[186]

Greece

na

1/5

na

necropsy

[104]

Hungary

40.0

8/20

na

necropsy

[59]

India

na

na

na

na

[187]

na

na

na

na

[143]

na

na

na

na

[188]

Indiaa

na

na

na

CO

[189]

100

12/12

100–400 epg

CO

[190]

Iran

100

20/20

27.1

necropsy

[110]

7.1

1/14

4

necropsy

[136]

2.5

2/79

na

necropsy

[139]

case report

 

na

necropsy

[155]

3.5

2/56

na

necropsy

[48]

Israel

33.3

5/15

na

necropsy

[146]

76.0

13/17

50–800 epg

CO

[19]

Russia

52.2

na

na

necropsy

[97]

5.0

3/60

na

necropsy

[106]

na

na

na

necropsy

[107]

12.0

18/150

3–265

necropsy

[53]

Serbia

0.2

1/447

2

necropsy

[108]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

9.7

3/31

2–4

necropsy

[140]

Uzbekistan

na

na

na

necropsy

[151]

Ancylostoma guentini

India

na

na

na

necropsy

[191]

Placoconus lotoris (syn. Uncinaria lotoris)b

Russia

16.6

2/12

4

necropsy

[98]

Uncinaria stenocephala

Afghanistan

na

na

na

necropsy

[192]

Azerbaijan

50.0

49/98

1–404

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

64.0

na

na

necropsy

[101]

na

na

na

necropsy

[237]

45.4

5/11

na

necropsy

[142]

84.6

na

na

necropsy

[45]

Chechnya

50.0

8/16

4–23

necropsy

[103]

Greece

na

4/5

na

necropsy

[104]

Hungary

40.0

8/20

na

necropsy

[59]

Iran

85.0

17/20

11.1

necropsy

[110]

6.3

5/79

na

necropsy

[139]

Russia

34.8

na

na

necropsy

[97]

na

na

na

necropsy

[339]

30.0

18/60

na

necropsy

[106]

na

na

na

necropsy

[107]

89.3

134/150

3–550

necropsy

[53]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

68.0

21/31

1–54

necropsy

[140]

Turkey

na

na

na

necropsy

[150, 194]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Ascarididae

Baylisascaris devosi

Azerbaijan

17.7

14/79

1–16

necropsy

[99]

Toxascaris sp.

Kazakhstan

11.1

2/18

2–8

necropsy

[147]

Toxascaris leonina

Afghanistan

na

na

na

necropsy

[192]

Armeniaa

case report

 

na

CO

[195]

Azerbaijan

0.8

1/114

1

necropsy

[137]

31.8

29/91

1–19

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

36.0

na

na

necropsy

[101]

5.8

na

na

necropsy

[141]

Chechnya

100

16/16

1–12

necropsy

[103]

Egypt

na

na

na

necropsy

[186]

Hungary

15.0

3/20

na

necropsy

[59]

Iran

30.0

3/10

na

necropsy

[111]

Irana

na

2/2

166.5 epg

CO

[372]

Kazakhstan

11.1

2/18

2–11

necropsy

[147]

Russia

43.5

na

na

necropsy

[97]

10.0

2/20

4.00 ± 3.14

necropsy

[96]

15.0

9/60

na

necropsy

[106]

na

na

na

necropsy

[98]

na

na

na

necropsy

[107]

4.7

7/150

2–23

necropsy

[53]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

6.5

2/31

1–7

necropsy

[140]

Turkey

na

na

na

necropsy

[150]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Toxocara sp.

Indiaa

21.6

13/60

na

CO

[144]

na

na

na

CO

[196]

na

2/2

40–700 epg

CO

[197]

na

3/6

na

CO

[185]

Toxocara canis (syn. Belascaris marginata)

Azerbaijan

32.6

32/98

1–21

necropsy

[99]

na

na

na

necropsy

[100]

Bangladesh

40.0

12/30

na

necropsy

[134]

na

2/5

na

CO

[118]

Bulgaria

54.5

6/11

na

necropsy

[142]

7.7

na

na

necropsy

[45]

Chechnya

50.0

8/16

3–18

necropsy

[103]

Greece

na

2/5

na

necropsy

[104]

Hungary

20.0

4/20

na

necropsy

[59]

India (as B. marginata)

na

na

na

na

[187]

na

na

na

na

[143]

na

na

na

na

[112]

Indiaa

na

na

na

CO

[189]

Iran

10.0

2/20

na

necropsy

[110]

 

7.1

1/14

10

necropsy

[136]

 

10.0

1/10

na

necropsy

[111]

 

5.0

4/79

na

necropsy

[139]

 

12.5

7/56

na

necropsy

[48]

Irana

na

2/2

25 ± 5 epg

CO

[372]

Russia

60.9

na

na

necropsy

[97]

5.0

1/20

2.00 ± 2.13

necropsy

[96]

6.6

4/60

na

necropsy

[106]

na

na

na

necropsy

[98]

na

na

na

necropsy

[107]

23.3

35/150

1–22

necropsy

[53]

Serbia

1.6

7/447

7.8 ± 2.1

necropsy

[108]

23.3

14/60

na

necropsy

[49]

Tajikistan

na

na

na

necropsy

[148]

Tunisia

16.0

5/31

1–9

necropsy

[140]

Turkey

na

na

na

necropsy

[150]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Toxocara cati (syns Ascaris mystax, T. mystax)b

Italy

na

na

na

necropsy

[138]

Russia

26.1

na

na

necropsy

[97]

5.0

1/20

2.0 ± 1.9

necropsy

[96]

Uzbekistan

na

na

na

necropsy

[152]

Crenosomatidae

Crenosoma vulpis

Azerbaijan

14.6

12/82

1–19

necropsy

[99]

 

na

na

na

necropsy

[100]

Bangladesh

na

1/5

na

necropsy

[118]

Chechnya

100

16/16

10–23

necropsy

[103]

Hungary

30.0

6/20

na

necropsy

[59]

Russia

26.1

n/a

na

necropsy

[97]

10.0

6/60

na

necropsy

[106]

na

na

na

necropsy

[107]

12.0

18/150

6–297

necropsy

[53]

Crenosoma petrowi

Chechnya

37.5

6/16

16–38

necropsy

[103]

Diaphanocephalidae

Kalicephalus schadi fotedari b

India

na

na

na

necropsy

[198]

Dracunculidae

Dracunculus medinensis

India

na

na

na

na

[112]

Kazakhstan

16.6

3/18

2–4

necropsy

[147]

Tajikistan

na

na

na

necropsy

[148]

Gnathostomatidae

Gnathostoma spinigerum

India, Bangladesh, Burma

na

na

na

na

[112]

Bangladesh

26.6

8/30

na

necropsy

[134]

Gongylonematidae

Gongylonema sp.b

Serbia

0.4

2/447

1

necropsy

[108]

Metastrongylidae

Angiostrongylus vasorum

na

na

1/1

na

EI

[199]

Hungary

10.0

2/20

na

necropsy

[59]

Molineidae

Molineus patens

Russia

8.3

5/60

na

necropsy

[106]

26.0

39/150

3–104

necropsy

[53]

Onchocercidae

Acanthocheilonema reconditum (syn. Dipetalonema reconditum)

Bulgaria

30.0

3/10

na

K

[200]

Kenya (as Dipetalonema reconditum)

na

na

na

na

[201]

Dirofilaria immitis

Azerbaijan

na

na

na

necropsy

[100]

Bangladesh

na

4/5

na

necropsy

[118]

Bulgaria

8.9

5/56

2–16

necropsy/K

[202]

9.6

na

na

necropsy

[45]

70.0

7/10

na

K

[200]

37.5

122/325

1–19

necropsy

[203]

Greece

case report

 

4

necropsy

[204]

Hungary

7.4

2/27

1–10

necropsy

[205]

Indiaa

na

na

na

na

[206]

Iran

28.5

4/14

13

necropsy

[136]

na

na

na

necropsy

[207]

11.4

9/79

na

necropsy

[139]

1.7

1/56

na

necropsy

[48]

8.9

4/45

1–10

necropsy, molecular

[208]

Romania

18.52

10/54

1–7

necropsy

[209]

9.26

5/54

na

molecular

[209]

Russia

8.3

1/12

29

necropsy

[98]

8.3

5/60

na

necropsy

[106]

20.0

na

na

necropsy

[339]

22.7

34/150

2–23

necropsy

[53]

Serbia

7.3

32/437

na

necropsy

[210]

Uzbekistan

na

na

na

necropsy

[152]

Dirofilaria repens

Egypt

na

na

na

necropsy

[186]

Iran

10.0

2/20

na

necropsy

[110]

Romania

1.8

1/54

na

molecular

[209]

Russia

3.3

2/60

na

necropsy

[106]

Uzbekistan

na

na

na

necropsy

[152]

Oxyuridae

Syphacia sp.b

Kazakhstan

5.5

1/18

7

necropsy

[147]

Physalopteridae

Physaloptera sp.

Iran

na

na

na

necropsy

[105]

Kazakhstan

5.5

1/18

4

necropsy

[147]

Physaloptera sibirica

Azerbaijan

na

na

na

necropsy

[100]

Kazakhstan

11.1

2/18

1–3

necropsy

[147]

Rictulariidae

Rictularia sp.

Egypt

na

na

na

necropsy

[186]

Greece

na

1/5

na

necropsy

[104]

Rictularia affinis (syn. Pterygodermatites affinis)

Azerbaijan

36.3

28/77

1–29

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

7.7

na

na

necropsy

[45]

India (as P. affinis)

na

na

na

na

[117]

na

na

na

na

[188]

na

na

na

na

[112]

Iran

50.0

5/10

na

necropsy

[111]

5.0

4/79

na

necropsy

[139]

Kazakhstan

11.1

2/18

1–3

necropsy

[147]

Tunisia (as P. affinis)

6.5

2/31

1

necropsy

[140]

Turkmenistan

na

na

na

necropsy

[177]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Rictularia cahirensis

Egypt

na

na

na

necropsy

[186]

Iran

10.0

2/20

na

necropsy

[110]

Turkey

na

na

na

necropsy

[340]

Uzbekistan

na

na

na

necropsy

[151]

Spirocercidae

Spirocerca arctica

Azerbaijan

16.6

2/12

5–14

necropsy

[99]

na

na

na

necropsy

[100]

Spirocerca lupi (syn. Filaria sanguinolenta)

Azerbaijan

23.4

23/98

1–29

necropsy

[99]

na

na

na

necropsy

[100]

India

case report

 

na

necropsy

[211]

na

na

na

na

[112]

Indiaa

case report

 

na

necropsy

[212]

Iran

2.5

2/79

na

necropsy

[139]

Italy (as F. sanguinolenta)

na

na

na

necropsy

[138]

Uzbekistan

na

na

na

necropsy

[151]

Spirocerca sanguinolenta

India

na

na

na

necropsy

[213]

Strongyloididae

Strongyloides sp.

Indiaa

na

na

na

CO

[214]

Irana

na

2/2

5.5 ± 0.7 epg

CO

[372]

Strongyloides stercoralis

Iran

na

na

na

necropsy

[105]

Subuluridae

Oxynema linstowi

Tunisia

3.2

1/31

2

necropsy

[140]

Thelaziidae

Thelazia callipaeda

Romania

1.6

1/64

70

necropsy

[215]

Class Enoplea

       

Capillariidae

Capillaria sp.

Indiaa

na

na

na

CO

[214]

Russia

2.7

4/150

1–45

necropsy

[53]

Eucoleus aerophilus (syn. Thominx aerophilus)

Azerbaijan (as T. aerophilus)

na

na

na

necropsy

[100]

Hungary

5.0

1/20

na

necropsy

[59]

Russia

8.3

5/60

na

necropsy

[106]

37.3

56/150

1–6

necropsy

[53]

Capillaria boehmi

Russia

30.0

45/150

1–11

necropsy

[53]

Capillaria plica

Azerbaijan

14.8

4/27

1–4

necropsy

[99]

na

na

na

necropsy

[100]

Bulgaria

16.4

na

na

necropsy

[45]

Hungary

45.0

9/20

na

necropsy

[59]

Russia

11.6

7/60

na

necropsy

[106]

33.3

50/150

1–123

necropsy

[53]

Capillaria putorii

Azerbaijan

na

na

na

necropsy

[100]

Dioctophymatidae

Dioctophyme renale

Azerbaijan

3.5

4/114

1

necropsy

[137]

Iran

35.0

7/20

na

necropsy

[110, 216]

Russia

3.3

2/60

na

necropsy

[106]

Tajikistan

na

na

na

necropsy

[148]

Uzbekistan

na

na

na

necropsy

[151]

na

na

na

necropsy

[152]

Dioctophyme skrjabini

Russia

17.4

na

na

necropsy

[97]

Trichinellidae

Trichinella sp.

Armenia

33.3

5/15

na

TRIC

[217]

Azerbaijan

30.1

na

na

TRIC

[218]

28.6

na

na

TRIC

[219]

Bulgaria

50.0

na

na

TRIC

[220]

33.3

15/45

na

TRIC

[221]

21.2

7/33

na

TRIC

[222]

Croatia

na

na

na

AD

[102]

Georgia

80.0

na

na

TRIC

[218]

Romania

53.7

29/54

na

TRIC

[223]

Russia

14.3

na

na

TRIC

[224]

case report

 

na

AD

[225]

25.0

75/302

na

TRIC

[226]

case report

 

na

AD

[227]

Tajikistan

na

na

na

TRIC

[228]

Thailand

case report

 

na

TRIC

[229]

case report

 

na

TRIC

[230]

USSR (former)

36.5

na

na

TRIC

[231]

Yugoslavia (former)

25.0

na

na

TRIC

[232]

Trichinella britovi

Algeria

case report

 

na

PCR

[233]

Azerbaijan

case report

 

na

AD

[234]

Iran

11.1

2/18

na

AD, PCR

[235]

Kazakhstan

na

na

na

TRIC

[234]

Lithuania

na

3/4

0.9–1.4 lpg

AD, PCR

[236]

Romania

case report

 

55 lpg

AD, PCR

[237]

Serbia

4.7

2/42

na

AD, PCR

[238]

15.4

2/13

na

AD, PCR

[239]

27.8

25/90

1.1–57.6 lpg

AD, PCR

[240]

Turkmenistan

case report

 

na

AD

[234]

Uzbekistan

case report

 

na

AD

[234]

Trichinella nativa

Kazakhstan

18.9

4/18

7 lpg

AD

[147]

Lithuania

n/a

1/4

0.9–1.4 lpg

AD, PCR

[236]

URSS (former)

61.5

na

na

TRIC

[241]

Trichinella nelsoni

Iran

na

2/2

na

TRIC

[242]

Kazakhstan

16.2

3/18

6 lpg

na

[147]

Trichinella pseudospiralis

Russia

2.7

4/150

na

TRIC

[53]

Trichinella spiralis

Afghanistan

case report

 

214 lpg

TRIC

[243]

Azerbaijan

20.4

17/83

1–7 lpg

TRIC

[244]

21.1

25/114

1–22 lpg

TRIC

[137]

17.5

16/91

1–44 lpg

TRIC

[99]

Bulgaria

na

na

na

TRIC

[245]

45.0

na

na

TRIC

[101]

40.0

na

na

AD

[45]

Georgia

36.6

na

na

TRIC

[246]

Hungary

9.0

1/11

na

AD, PCR

[365]

Iran

60.3

38/63

na

TRIC

[247]

55.5

10/18

na

TRIC

[248]

na

3/3

na

TRIC

[249]

55.7

59/106

na

TRIC

[250]

84.0

na

na

TRIC

[251]

Kazakhstan

5.5

1/18

3 lpg

TRIC

[147]

Russia

43.5

na

na

TRIC

[97]

21.6

13/60

na

TRIC

[106]

55.3

83/150

na

TRIC, AD

[53]

Senegal

33.0

na

na

TRIC

[252]

Serbia

na

3/3

1.9–21.4 lpg

AD, PCR

[253]

8.3

1/12

3 lpg

AD, PCR

[254]

7.9

3/38

3 lpg

AD, PCR

[255]

14.2

6/42

na

AD, PCR

[238]

38.4

5/13

na

AD, PCR

[239]

71.1

64/90

0.59–152.8 lpg

AD, PCR

[240]

Tunisia

na

2/2

na

TRIC

[256]

Trichuroididae

Trichuris sp.

Indiaa

15.0

9/60

na

CO

[144]

Trichuris georgicus (syn. Trichocephalus georgicus)

Azerbaijan

14.4

12/83

1–12

necropsy

[99]

na

na

na

necropsy

[100]

Trichuris vulpis (syn. Trichocephalus vulpis)

Azerbaijan (as Trichocephalus vulpis)

11.2

11/98

1–11

necropsy

[99]

na

na

na

necropsy

[100]

Bangladesh

na

1/5

na

CO

[118]

Bulgaria

30.7

na

1–156

necropsy

[141]

36.3

4/11

na

necropsy

[142]

Russia (as Trichocephalus vulpis)

21.6

13/60

na

necropsy

[106]

35.3

53/150

1–70

necropsy

[53]

Serbia

11.6

4/60

na

necropsy

[49]

Hungary

10.0

2/20

na

necropsy

[59]

Abbreviations: AD artificial digestion, CO coprological examination, EI experimental infection, epg eggs per gram faeces, lpg larvae per gram tissue, K Knott test, PCR polymerase chain reaction, TRIC trichinelloscopy, na not applicable/not available

aAnimals kept in captivity

bDoubtful record

Ascarids

Ascarids, primarily considered heteroxenous nematodes, have lost their intermediate hosts and have adapted to direct transmission or through paratenic hosts [257]. Four species are reported in golden jackals, with Toxocara canis and Toxascaris leonina being ubiquitous. Baylisascaris devosi is a species typically found in mustelids inhabiting the northern hemisphere [258]. Its presence in golden jackals has been reported only once, in Azerbaijan [99]. This broad distribution and common presence of ascarids in this wild canid can be explained by the intervention of numerous paratenic hosts, possible preys for jackals, in the life-cycle of these nematode species (mostly rodents and invertebrates such as earthworms and insects) [259].

Strongyloides

The cosmopolitan and zoonotic Strongyloides stercoralis infects about 200 million people, more commonly in tropical and subtropical climates [260]. Despite the large number of records in domestic dogs from various countries, the species has been reported only once in golden jackals (Table 6). The lack of reports in other parts of the jackal’s range could be explained by a low receptivity of this host or by failures of finding the parasites during necropsy due to their small size. A moderate prevalence of 5.6% is also recorded in dogs from northeastern Iran [261] which is higher than estimated prevalence in humans across the country that ranges between 0.1 and 0.3% [262]. Although carnivores can be a source of infection for humans via larvae that develop in the environment, the principal reservoirs of S. stercoralis are humans. The role of domestic and wild carnivores in the epidemiology of strongyloidiasis remains to be clarified [155].

Hookworms and other digestive tract strongylids

Several hookworm (Ancylostomatidae) species have been reported in golden jackals, with Ancylostoma caninum and Uncinaria stenocephala commonly reported across the entire geographical range of these hosts. Additionally, A. guentini was described from golden jackals in India, being so far the only known host for this parasite [191]. The remaining two records (Placoconus lotoris, known otherwise only from new world procyonids, and Ancylostoma braziliense, typically found in the Americas) we list as doubtful and as these are probably misidentifications of other hookworm species. The opportunistic behaviour of the golden jackals leads them to venture close to human habitats to feed [2]. The proximity with domestic dogs allows interspecific transmission of ancylostomid species, due to the high rate of soil and grass contamination [263]. In this regard, increased prevalence recorded in Russia, ranging between 5.0 and 52.2%, is correlated with similar values in dogs, between 2.06 and 62.3% [264]. Ancylostoma caninum and U. stenocephala possess a zoonotic potential causing dermal larva migrans in humans [260]. Although a direct relationship between the numerous reports in golden jackals and the presence of disease in humans cannot be established, this carnivore species probably contributes to the presence of Ancylostomatidae larvae in rural and periurban areas.

Molineus patens is a hookworm commonly reported in a wide range of carnivores in the Palaearctic and Nearctic [265], including two records from jackals in Russia. However, its zoonotic role has not been documented.

Metastrongyloids

Compared to foxes, little is known about the respiratory and cardiovascular strongylids of golden jackals. Crenosoma vulpis has been reported on several occasions in Asia and Europe, with variable prevalence (Table 6). There is a single report of Crenosoma petrowi in golden jackals, a parasite otherwise known mainly from mustelids in North America [266], one report from bears (also in North America) and another one from stone martens in Italy [267]. Surprisingly, there is only one record of Angiostrongylus vasorum in golden jackals, suggesting either a lack of habitat overlap or a low detection sensitivity during necropsy.

Filarioids

Zoonotic filarioids Acanthocheilonema reconditum, Dirofilaria immitis and D. repens have been all reported in golden jackals in various countries (Table 6). They have been found both as adults during necropsies but also as microfilariae demonstrating the reservoir role of jackals. Dirofilaria spp. are responsible in humans of conjunctivitis, focal pulmonary infarction with granuloma formation and subcutaneous and submucosal lesions in the lung and conjunctiva [268270]. A recent review listed 1782 human Dirofilaria spp. infections, out of which 372 were pulmonary (in Australia, North and South America) and 1410 were subcutaneous/ocular cases (mostly in Europe and Asia) [271]. Acanthocheilonema reconditum is considered non-pathogenic for canids [155], but a single human case is well documented as being caused by this species and at least other two, by other Acanthocheilonema species [270, 272, 273]. The recorded prevalence of D. immitis has significantly varied in different areas between 7.3% in Serbia and 80.0% in Bangladesh, and seems to be consistent with the prevalence registered in dogs, generally between 40 and 70% in endemic areas [155]. The prevalence of D. repens in golden jackals ranged between 3.3 and 10.0%, resembling that recorded in dogs, generally varying from 5 to 20% [155].

The oriental eye-worm Thelazia callipaeda has been identified in golden jackals only in Romania [215], but this is probably due to lack of proper examinations of the eyes during the necropsy in other studies rather than a resistance of this host. Dogs originating in the Far East were initially considered the main host of the nematode [257]. Over the last 15 years, T. callipaeda has shown an increase in the distribution area mainly in Europe, with many new host records [274]. Human thelaziosis followed the same geographical spreading, with recent cases of infection diagnosed [274]. In this epidemiological picture, the golden jackal occurs as a new reservoir host.

Capillariids

Respiratory capillariids of carnivores (C. aerophila, C. boehmi and C. putorii) are considered primarily homoxenous, but the earthworms often act as facultative intermediate hosts [1, 275]. Along with the heteroxenous species Capillaria plica found in the urinary bladder, all species are cosmopolitan [257]. They have been found in golden jackals in Russia and other former Soviet Union countries. Only C. plica and C. aerophila are known to be zoonotic [276, 277], but their public health impact is minor. As the primary source of infection with Capillaria is the soil contaminated by infective eggs [155], the jackal can play an epidemiological role and secondary source of infection for domestic carnivores and humans.

Trichinella

Trichinellids are an important group of meat-borne zoonotic parasites [278] for which the golden jackals represent an important reservoir. Five species, T. britovi, T. nativa, T. nelsoni, T. pseudospiralis and T. spiralis, were recorded in mountainous and lowland regions across the distribution range of the golden jackal in Europe and Asia. However, only three of these (T. britovi, T. nativa and T. spiralis) have been confirmed molecularly (Table 6). We consider all the records by artificial digestion or trichinelloscopy (see Table 6) where the species is named as hypothetic, as there is no reliable morphological means of differentiation between species, hence we recommend to consider these as Trichinella sp. Nevertheless, the zoonotic potential have been shown for most Trichinella species, hence, the golden jackal represents an important natural sylvatic reservoir for these nematodes [240].

Other nematodes

Various other groups of nematodes have been found in golden jackals (families Spirocercidae, Dracunculidae, Gnathostomatidae, Physalopteridae, Rictulariidae, Subuluridae), but the reports are occasional (Table 6). Other groups (Kalicephalus, Syphacia and Gongylonema) are with high probability pseudoparasites, originating in prey hosts.

Spirocerca lupi is a rare zoonotic nematode species also identified in golden jackals in Europe, central and southern Asia (Table 6). Although a single human infection has been reported [279], the jackal may represent a reservoir host that maintains the life-cycle of the parasite in a certain region. Two other species of the genus Spirocerca (S. arctica and S. sanguinolenta, both described from domestic dogs) have been also reported in jackals, but their taxonomic status and biology are unknown.

Dracunculus medinensis has been identified in the golden jackal from several central and southern Asian countries. Currently the disease in humans has been declared extinct in the vast majority of the countries, with only three (Chad, South Sudan and Ethiopia) reporting cases in 2016 [280]. Dogs are considered to be important reservoirs for human infection [155, 281, 282]. In 2016, more than 1000 dogs in Chad, 14 dogs in Ethiopia, and 11 dogs in Mali were reported with guinea-worm [280]. In this context, understanding the role of wild canids (including golden jackals) remains a crucial aspect in the management of the ongoing eradication campaign.

Another zoonotic species identified in golden jackals from tropical Asian countries (India, Bangladesh, Myanmar) is Gnathostoma spinigerum. Gnathostomiasis, a major food-borne parasitic zoonosis and a significant public health problem, is considered an emerging imported disease in Europe and a common human infection in central and South America, and Asia [283]. Domestic and wild mammals are the final hosts and numerous intermediate and paratenic hosts are the source for the human infection. The golden jackals maintain the sylvatic focus of the parasites and interfere with the domestic cycle, at least in several Asian countries (Table 6).

Various other carnivore-specific spirurids have been found in golden jackals (Physaloptera sibirica, Rictularia affinis, R. cahirensis and Oxynema linstowi), but the role of this host species in their natural cycle remains unknown.

The cosmopolitan species Dioctophyme renale causes a severe kidney destruction in the carnivore definitive hosts. Although with limited zoonotic importance, so far around 20 human cases have been reported [284]. American minks seem to be the main reservoirs of the parasite [257], but an increased prevalence is also recorded in other wild and domestic carnivores. In golden jackals, D. renale has been reported in Asia, where the prevalence ranged between 3.3–35.0% (Table 6). Interestingly, this wild canid has shown a twice higher prevalence than stray dogs in the same geographical region [110], demonstrating the role of the jackal in the development of parasite’s cycle in nature.

Trichuris vulpis has been found on various occasions in golden jackals in Europe and Asia (Table 6). The high prevalence of T. vulpis infection in golden jackals (10.0–36.3%) is in line with the value recorded in dogs originating from the same areas: 25% in India [285], 20% in Bulgaria [286] and 8.95% in Russia [264]. Although the prevalence of T. vulpis in domestic and wild canids is generally high, only around 60 human cases have been recorded [155].

Arthropods

A great variety of Arthropods have been found in golden jackals (Table 7) [287328].
Table 7

Arthropod parasites of the golden jackal, Canis aureus

Family

Species

Origin

Prevalence (%)

Frequency

Intensity

(A, ♂, ♀, N, L)b

Reference

Class Arachnida

Demodecidae

Demodex spp.

Israel

na

1/1

na

[287]

Demodex canis

Russia

3.3

5/150

na

[53]

Demodex folliculorum

Bangladesh

na

na

na

[118]

Ixodidae

Amblyomma sp.

Nepal

na

na

na

[288]

Amblyomma varanense (syn. Aponomma gervaisi lucasi)

India

na

na

na

[289]

Amblyomma variegatum

Haute-Volta

na

na

7 N

[290]

Senegal

na

na

54 L

[291]

Dermacentor marginatus

Russia

15.3

23/150

1–26

[53]

Serbia

45.0

9/20

na

[292]

Dermacentor reticulatus

Austria

na

1/1

17 ♂; 2 ♀

[56]

Hungary

na

4/4

10 A

[293]

Italy

na

1/1

na

[116]

Romania

12.6

10/79

46 ♂; 25 ♀

[294]

Russia

62.0

93/150

1–26

[53]

Haemaphysalis sp.

Iran

1.7

1/56

na

[48, 295, 296]

Nepal

na

na

na

[288]

Haemaphysalis adleri

Iraq

na

na

na

[297]

Israel

na

2/2

4 ♂; 1 ♀

[298]

 

na

3/3

na

[299]

Haemaphysalis bispinosa

India

na

na

na

[300]

Nepal

na

na

na

[288]

Haemaphysalis canestrinii

India

na

1/1

9 ♂; 3 ♀,

[301]

 

na

na

na

[300]

Pakistan

na

3/3

3 ♂; 1 ♀

[301]

Haemaphysalis concinna

Austria

na

1/1

1 N

[56]

Hungary

na

4/4

7 N; 4 L

[293]

Romania

1.2

1/79

1 N

[294]

Haemaphysalis flava

India

na

na

A

[289]

Haemaphysalis indoflava

India

na

na

na

[302]

Haemaphysalis intermedia

India

na

2/2

8 ♂; 17♀; 28 N; 13 L

[303]

 

na

na

na

[300]

Haemaphysalis kutchensis

India

na

na

10 ♂; 1 ♀

[348]

Haemaphysalis leachii (syns H. leachii leachii, H. leachii indica)

Egypt (as H. leachii leachii)

na

na

na

[305]

India

na

1/1

9 ♂; 3 ♀

[306]

India (as H. leachii indica)

na

na

na

[289]

 

na

2/2

7 ♂; 2♀; 4 N; 1 L

[307]

Nepal (as H. leachii indica)

na

3/3

6 N

[307]

Haemaphysalis longicornis (syn. H. neumanni)

Ceylon

na

na

na

[308]

Haemaphysalis paraleachi

Sudan

100

10/10

42 ♂; 4 ♀

[309]

Haemaphysalis parva (syn. H. otophila)

India

na

na

na

[310]

Israel

na

3/3

na

[299]

Israel (as H. otophila)

na

6/6

37

[311]

Haemaphysalis punctata

Romania

na

4/4

na

[312]

 

2.5

2/79

1 ♂; 2 N

[294]

Hyalomma sp.

Russia

0.7

1/150

1

[53]

Tajikistan

na

na

na

[148]

Hyalomma aegyptium

USSR (former)

na

na

na

[313]

Hyalomma anatolicum

Tajikistan

na

na

na

[148]

Hyalomma asiaticum

Tajikistan

na

na

na

[148]

Hyalomma scupense

Tajikistan

na

na

na

[148]

Ixodes sp.

Iran

na

1/1

na

[314]

Russia

na

na

na

[339]

Tajikistan

na

na

na

[148]

Ixodes acuminatus (syn. I. redikorzevi theodori)

Israel

na

6/6

1

[311]

Ixodes canisuga

Hungary

na

4/4

1 N

[293]

Ixodes hexagonus

Romania

10.1

8/79

2 ♂; 11 ♀; 24 N; 12 L

[294]

Ixodes ovatus

Nepal

na

1/1

6 ♀

[315]

Ixodes ricinus

Hungary

na

4/4

3 A

[293]

Iran

3.5

2/56

na

[48, 295, 296]

Italy

na

1/1

na

[116]

Romania

na

1/1

na

[316]

 

na

4/4

na

[312]

 

26.5

21/79

54 ♂; 45♀; 3 N; 4 L

[294]

Russia

68.7

103/150

1–62

[53]

Serbia

55.0

11/20

na

[292]

Rhipicephalus sp.

Iran

1.7

1/56

na

[48, 295, 296]

Tajikistan

na

na

na

[148]

Rhipicephalus annulatus (syn. Boophilus calcaratus)

Russia

1.3

2/150

1–2

[53]

Rhipicephalus cuspidatus

Haute-Volta

na

na

na

[290]

Rhipicephalus haemaphysaloides

India

na

na

na

[289]

na

1/1

4 ♂

[306]

na

2/2

1 ♀; 2 N

[303]

na

na

na

[300]

Nepal

na

na

na

[288]

Rhipicephalus leporis

Iraq

na

na

na

[297]

Tajikistan

na

na

na

[148]

Rhipicephalus pumilio

Tajikistan

na

na

na

[148]

Uzbekistan

na

na

na

[152]

Rhipicephalus rossicus

Tajikistan

na

na

na

[148]

Rhipicephalus sanguineus

Algeria

na

2/2

15 ♂; 8 ♀

[317]

Burma, Ceylon, India

na

na

na

[289]

India

na

na

na

[300]

Iran

na

na

na

[314]

Israel

na

6/6

na

[311]

Nepal

na

na

na

[288]

Nigeriaa

na

3/6

na

[41]

Romania

na

1/1

na

[316]

 

na

4/4

na

[312]

 

1.2

1/79

1 ♂

[294]

Serbia

0.5

1/20

na

[292]

Tajikistan

na

na

na

[148]

Turkey

na

na

na

[150]

na

na

na

[318]

Rhipicephalus schulzei

Tajikistan

na

na

na

[148]

Rhipicephalus simus

Kenya

na

na

na

[319]

Rhipicephalus sulcatus

Haute-Volta

na

na

5 ♂

[290]

Rhipicephalus turanicus

Iraq

na

na

na

[320]

 

100

14/14

na

[297]

Tajikistan

na

na

na

[148]

Uzbekistan

na

na

na

[152]

Psoroptidae

Otodectes cynotis

Iran

1.7

1/56

na

[48, 295, 296]

Sarcoptidae

Sarcoptes scabiei

Israel

na

1/1

na

[287]

Class Insecta

Boopiidae

Heterodoxus spiniger

Africa (North, East); Asia (South); Europe (Southeast)

na

na

na

[321]

Uganda

na

1/1

1 ♂; 2 ♀

[322]

Ceratophyllidae

Paraceras melis

Russia

10.0

15/150

1–12

[53]

3.3

5/150

na

[323]

Coptopsyllidae

Coptopsylla lamellifer dubinini

Uzbekistan

na

na

na

[152]

Hippoboscidae

Hippobosca longipennis

Russia

2.7

4/150

1–2

[53]

Linognathidae

Linognathus setosus

Afrotropical Region

na

na

na

[324]

Nepal

na

na

na

[288]

Pediculidae

Pediculus sp.

Bangladesh

na

na

na

[118]

Pulicidae

Pulex irritans

Afghanistan

na

na

2 ♂; 1 ♀

[325]

Iran

na

na

3 ♂; 1 ♀

[326]

Israel

na

6/6

36

[311]

Russia

24.0

36/150

1–15

[53]

14.0

21/150

na

[323]

Tajikistan

na

na

na

[148]

Uzbekistan

na

na

na

[152]

Ctenocephalides canis

Afghanistan

na

na

10 ♂; 38 ♀

[325]

Iran

na

na

13 ♂; 25 ♀

[326]

10.8

6/56

na

[48, 295, 296]

Israel

na

4/6

27

[311]

Nigeriaa

na

1/6

na

[41]

Russia

48.0

72/150

1–28

[53]

17.3

30/150

na

[323]

Tajikistan

na

na

na

[148]

Turkey

na

na

na

[150]

Uzbekistan

na

na

na

[152]

Ctenocephalides felis (syn. C. felis felis)

Ethiopia

na

na

na

[327]

India (as C. felis felis)

na

na

na

[328]

Iran (as C. felis felis)

na

na

2 ♂; 2 ♀

[326]

Israel

50.0

3/6

6

[311]

Russia

3.3

5/150

1–4

[53]

Tajikistan

na

na

na

[148]

Uzbekistan

na

na

na

[152]

Echidnophaga gallinacea

Afghanistan

na

na

1 ♂

[325]

Ethiopia

na

na

na

[327]

Xenopsylla nesokiae

Tajikistan

na

na

na

[148]

Trichodectidae

Trichodectes canis

Russia

13.3

20/150

1–34

[53]

 

Tajikistan

na

na

na

[148]

Vermipsyllidae

Chaetopsylla globiceps

Russia

27.3

41/150

1–19

[53]

6.7

10/150

na

[323]

Class Maxillopoda

Linguatulidae

Linguatula serrata

Romania

1.3

1/73

1 ♂

Our unpublished data

Abbreviation: na not applicable/not available

aAnimals kept in captivity

bA, adults; ♂, male; ♀, female; N, nymphs; L, larvae

Ticks

Due to the large geographical range, the diversity of ticks parasitizing golden jackals is high. Ticks from 37 species belonging to six genera have been recorded in jackals throughout Europe, Asia and Africa. Nevertheless, the number of studies on tick-borne pathogens is surprisingly low. The common tick species found in golden jackals in Europe, i.e. Dermacentor reticulatus, D. marginatus, Haemaphysalis concinna, H. punctata, Ixodes canisuga, I. hexagonus, I. ricinus and Rhipicephalus sanguineus (s.l.), show that they share these ticks with other wild canids, like foxes [329] or with domestic dogs [330]. The two most commonly reported ticks in golden jackals from Europe are D. reticulatus and I. ricinus. These ticks are known to be important vectors for Babesia canis and important tick-borne bacteria, Borrelia burgdorferi (s.l.) and Anaplasma phagocytophilum. However, the reports of these pathogens in C. aureus are scarce (a single report of Babesia canis from Romania [42]). In Asia, the most common ticks on jackals are several species of genus Haemaphysalis, with a high diversity of species reported: H. leachi, H. adleri, H. bispinosa, H. canestrinii, H. flava, H. indoflava, H. intermedia, H. kutchensis and H. parva. However, studies on the pathogens they might transmit are absent. Several of these Haemaphysalis species are shared with domestic dogs or other wild carnivores, raising the question of the reservoir role of jackals for certain tick-borne pathogens. Except for Haemaphysalis ticks, another commonly reported tick on golden jackals from Asia is Rhipicephalus haemaphysaloides, a tick which prefers ungulates and known as vector of several viral and protozoan diseases [331]. Studies in golden jackals from arid regions (northern Africa and Middle East) demonstrated the predominant presence of ticks from the genus Rhipicephalus: R. sanguineus (s.l.), R. turanicus and R. leporis. Surprisingly, there are no reports of ticks on golden jackals in sub-Saharan Africa.

Mites

Compared to foxes, jackals seem to be less affected by mange-causing mites (Table 7). So far, there is a single report of Sarcoptes scabiei in golden jackals, in Israel [287] and a single report of Otodectes cynotis, in Iran [295]. It is unclear if the scarcity of data regarding Sarcoptes is because of the low prevalence or because of the lack of studies and/or reports. Except sarcoptid mites, there are few records of Demodex in golden jackals, but its clinical significance is not known (Table 7).

Fleas and lice

The diversity of fleas reported in golden jackals is relatively high, with at least seven species reported (Table 7), with the most common being Pulex irritans, Ctenocephalides canis and C. felis. Most of the reports of fleas in golden jackals originate in Russia and other former USSR countries and western and southern Asia. Surprisingly, there are no reports of fleas in golden jackals in Europe. The reports of lice in golden jackals are scarce with only three species occasionally reported (Table 7).

Other arthropods

Although relatively common in most wild carnivores and domestic dogs (Mihalca, personal observation), there is only a single report of Hippobosca longipennis in golden jackals (Table 7). This species is an important vector for Acanthocheilonema dracunculoides, a filarioid widely distributed in canids across Africa [332]. However, this vector-borne nematode was never reported in golden jackals.

Conclusions

This is the first comprehensive checklist summarizing the data on parasites of golden jackals. The large variety of parasites reported in golden jackals is caused by multiple factors, including their large geographical range, their extensive territorial mobility and wide food spectrum. Moreover, like in other carnivores, the predator behaviour of golden jackals is the cause of common records of pseudoparasites. Nevertheless, even in such cases, although these parasites do not infect jackals, they can be spread and can remain infective for their natural hosts. Considering that jackals share their habitats with domestic dogs and a wide variety of wild carnivores across their distribution range and the high similarity with canine parasites [333], the risk of interspecific transmission among canid species, and the continued spread of the species, is likely to be associated with future territorial expanding of different parasitic diseases. The vast majority of parasites recorded in golden jackals are shared with domestic dogs or even domestic cats. Other parasites of jackals can use a wide variety of other domestic species, including livestock, as intermediate hosts. Hence, jackals are an important source of infection for domestic animals and might be directly or indirectly responsible for economic losses. Probably the most important aspect regarding the parasites of golden jackal is the large number and common occurrence of zoonotic parasites. Among these, several are with high public health impact: Leishmania, Echinococcus, hookworms, Toxocara, and Trichinella. Our review brings overwhelming evidence on the importance of Canis aureus as wild reservoir of human parasites.

Declarations

Acknowledgements

We are indebted to Cristian Domşa who generated the map of golden jackal distribution.

Funding

Not applicable.

Availability of data and materials

The data supporting the conclusions are provided within the article.

Authors’ contributions

CMG collected the information from databases, systematized information in tables and wrote the manuscript. ADM had the initial idea of this review and critically revised the manuscript for important intellectual content. Both authors read and approved the final manuscript.

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare that they have no competing interests.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.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. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Parasitology and Parasitic Diseases, Faculty of Veterinary Medicine, University of Agricultural Sciences and Veterinary Medicine Cluj-Napoca

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