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. 2023 Mar 1;1151:159–203. doi: 10.3897/zookeys.1151.97126

Helminth and protozoan parasites of subterranean rodents (Chordata, Mammalia, Rodentia) of the world

Altangerel T Dursahinhan 1, Daniel A Kenkel 1, Scott L Gardner 1,✉
PMCID: PMC10207929  PMID: 37235179

Abstract

Published studies and ten new unpublished records included herein reveal that approximately 174 species of endoparasites (helminths and protozoans) are known from 65 of 163 species of rodents that occupy the subterranean ecotope globally. Of those, 94 endoparasite species were originally described from these rodents. A total of 282 host-parasite associations are summarized from four major zoogeographic regions including Ethiopian, Palearctic/Oriental, Nearctic, and Neotropical. Thirty-four parasite records from the literature have been identified to only the level of the genus. In this summary, ten new records have been added, and the most current taxonomic status of each parasite species is noted. Interestingly, there are no data on endoparasites from more than 68% of described subterranean rodents, which indicates that discovery and documentation are at an early stage and must continue.

Keywords: Bathyergidae, Cricetidae, Ctenomyidae, Endoparasite, Geomyidae, Heterocephalidae, Octodontidae, Spalacidae

Introduction

Subterranean rodents are animals adapted to live underground with minimal dependency on surface resources. They exhibit numerous adaptations to maintain their life activities in this niche including almost no externally visible neck, small eyes and ears, short legs, and very loose skin with soft fur that enables them to turn in their burrows with ease (Maser et al. 1981; Lacey et al. 2000). Conditions within the burrow systems are characterized by complete darkness, constant temperatures, relative humidity of 100% with low levels of air circulation, elevated carbon dioxide levels, and usually closed tunnels.

In contrast to mammals that live on the surface of the soil, subterranean rodents are completely acclimated to live in complex burrow systems below the surface. These animals have the capability to dig burrow systems through many types of friable soils (Lessa et al. 2008). The underground habitat has been invaded by rodents utilizing specialized digging methods in all zoogeographic regions of the world. However, rodents with the ability to dig tunnels underground by utilizing strong digging limbs as well as other morphological and physiological traits occur in all zoogeographic regions except Australia and Antarctica and adaptations by non-phylogenetically related groups to a subterranean existence are considered a product of convergent evolution (Losos 2011). Approximately 40% of the 6,500 mammal species of the world are rodents. Even though only 6.5% of all rodent species occupy the subterranean ecotope, these mammals play an essential part of the ecology in the areas in which they live, functioning as biological plows, cycling the earth, changing the landscape, promoting plant growth and ecological succession, and playing a critical role in cycling carbon and other nutrients through the soil. In the order Rodentia, a total of 163 extant subterranean species across 23 genera, within seven families, has been recognized with distributions throughout all continents except Antarctica and Australia (see Table 1) (Van Daele et al. 2007; Wilson et al. 2016, 2017).

Table 1.

List of subterranean rodents. NA = Nearctic, Nt = Neotropical, E = Ethiopian, P = Palearctic, O = Oriental.

Suborder Infraorder Family Subfamily Tribe # Genus/Species Region
Castorimorpha Geomorpha Geomyidae Geomyinae Thomomyini 1 Thomomysatrovarius J. A. Allen, 1898 NA NA
2 Thomomysbottae (Eydoux & Gervais, 1836) NA NA
3 Thomomysbulbivorus (Richardson, 1829) NA NA
4 Thomomysclusius Coues, 1875 NA NA
5 Thomomysidahoensis Merriam, 1901 NA NA
6 Thomomysmazama Merriam, 1897 NA NA
7 Thomomysmonticola J. A. Allen, 1893 NA NA
8 Thomomysnayarensis Mathis et al., 2013 NA NA
9 Thomomyssheldoni Bailey, 1915 NA NA
10 Thomomystalpoides (Richardson, 1828) NA NA
11 Thomomystownsendii (Bachman, 1839) NA NA
12 Thomomysumbrinus (Richardson, 1829) NA NA
Geomyini 13 Geomysarenarius Merriam, 1895 NA NA
14 Geomysattwateri Merriam, 1895 NA NA
15 Geomysbreviceps Baird, 1855 NA NA
16 Geomysbursarius (Shaw, 1800) NA NA
17 Geomysjugossicularis Hooper, 1940 NA NA
18 Geomysknoxjonesi Baker & Genoways, 1975 NA NA
19 Geomyslutescens Merriam, 1890 NA NA
20 Geomyspersonatus True, 1889 NA NA
21 Geomyspinetis Rafinesque, 1817 Nt Nt
22 Geomysstreckeri Davis, 1943 NA NA
23 Geomystexensis Merriam, 1895 NA NA
24 Geomystropicalis Goldman, 1915 NA NA
25 Zygogeomystrichopus Merriam, 1895 Nt Nt
26 Orthogeomysgrandis (Thomas, 1893) NA Nt
Castorimorpha Geomorpha Geomyidae Geomyinae Geomyini 27 Heterogeomyscavator (Bangs, 1902) Nt Nt
28 Heterogeomyscherriei (J. A. Allen, 1893) Nt Nt
29 Heterogeomysdariensis (Goldman, 1912) Nt Nt
30 Heterogeomysheterodus (Peters, 1865) Nt Nt
31 Heterogeomyshispidus (Le Conte, 1852) Nt Nt
32 Heterogeomyslanius Elliot, 1905 Nt Nt
33 Heterogeomysunderwoodi Osgood, 1931 Nt Nt
34 Pappogeomysbulleri (Thomas, 1892) Nt Nt
35 Cratogeomyscastanops (Baird, 1852) NA Nt
36 Cratogeomysfulvescens Merriam, 1895 NA Nt
37 Cratogeomysfumosus (Merriam, 1892) Nt Nt
38 Cratogeomysgoldmani (Merriam, 1895) NA Nt
39 Cratogeomysmerriami (Thomas, 1893) Nt Nt
40 Cratogeomysperotensis Merriam, 1895 NA Nt
41 Cratogeomysplaniceps (Merriam, 1895) NA Nt
Hystricomorpha Histricognathi Ctenomyidae 42 Ctenomysandersoni Gardner et al., 2014 Nt Nt
43 Ctenomysargentinus J. R. Contreras & Berry, 1982 Nt Nt
44 Ctenomysaustralis Rusconi, 1934 Nt Nt
45 Ctenomysazarae Thomas, 1903 Nt Nt
46 Ctenomysbergi Thomas, 1902 Nt Nt
47 Ctenomysbicolor Miranda-Ribeiro, 1914 Nt Nt
48 Ctenomysboliviensis Waterhouse, 1848 Nt Nt
49 Ctenomysbonettoi J. R. Contreras & Berry, 1982 Nt Nt
50 Ctenomysbrasiliensis de Blainville, 1826 Nt Nt
51 Ctenomyscolburni J. A. Allen, 1903 Nt Nt
52 Ctenomyscoludo Thomas, 1920 Nt Nt
52 Ctenomyscoludo Thomas, 1920 Nt Nt
53 Ctenomysconoveri Osgood, 1946 Nt Nt
Hystricomorpha Histricognathi Ctenomyidae 54 Ctenomyscoyhaiquensis Kelt & Gallardo, 1994 Nt Nt
55 Ctenomysdorbignyi Contreras & Contreras, 1984 Nt Nt
56 Ctenomysdorsalis Thomas, 1900 Nt Nt
57 Ctenomysemilianus Thomas & S. Leger, 1926 Nt Nt
58 Ctenomyserikacuellarae Gardner et al., 2014 Nt Nt
59 Ctenomysfamosus Thomas, 1920 Nt Nt
60 Ctenomysflamarioni Travi, 1981 Nt Nt
61 Ctenomysfodax Thomas, 1910 Nt Nt
62 Ctenomysfochi Thomas, 1919 Nt Nt
63 Ctenomysfrater Thomas, 1902 Nt Nt
64 Ctenomysfulvus Philippi, 1860 Nt Nt
65 Ctenomysgoodfellowi Thomas, 1921 Nt Nt
66 Ctenomyshaigi Thomas, 1919 Nt Nt
67 Ctenomysibicuiensis Freitas et al., 2012 Nt Nt
68 Ctenomysjohannis Thomas, 1921 Nt Nt
69 Ctenomysjuris Thomas, 1920 Nt Nt
70 Ctenomysknighti Thomas, 1919 Nt Nt
71 Ctenomyslami Freitas, 2001 Nt Nt
72 Ctenomyslatro Thomas, 1918 Nt Nt
73 Ctenomyslessai Gardner et al., 2014 Nt Nt
74 Ctenomysleucodon Waterhouse, 1848 Nt Nt
75 Ctenomyslewisi Thomas, 1926 Nt Nt
76 Ctenomysmagellanicus Bennett, 1836 Nt Nt
77 Ctenomysmariafarelli Azurduy, 2005 Nt Nt
78 Ctenomysmaulinus Philippi, 1872 Nt Nt
79 Ctenomysmendocinus Philippi, 1869 Nt Nt
80 Ctenomysminitus Nehring, 1887 Nt Nt
81 Ctenomysnattereri Wagner, 1848 Nt Nt
82 Ctenomysoccultus Thomas, 1920 Nt Nt
83 Ctenomysopimus Wagner, 1848 Nt Nt
84 Ctenomysosvaldoreigi J. R. Contreras, 1985 Nt Nt
85 Ctenomysparaguayensis J. R. Contreras, 2000 Nt Nt
86 Ctenomyspearsoni Lessa & Langguth, 1983 Nt Nt
87 Ctenomysperrensi Thomas, 1896 Nt Nt
88 Ctenomysperuanus Sanborn & Pearson, 1947 Nt Nt
89 Ctenomyspilarensis J. R. Contreras, 1993 Nt Nt
90 Ctenomyspontifex Thomas, 1918 Nt Nt
91 Ctenomysporteousi Thomas, 1916 Nt Nt
92 Ctenomyspundti Nehring, 1900 Nt Nt
93 Ctenomysrionegrensis Langguth & Abella, 1970 Nt Nt
94 Ctenomysroigi J. R. Contreras, 1988 Nt Nt
95 Ctenomysrondoni Miranda-Ribeiro, 1914 Nt Nt
96 Ctenomysrosendopascuali J. R. Contreras, 1995 Nt Nt
97 Ctenomystalarum Thomas, 1898 Nt Nt
98 Ctenomystorquatus Lichtenstein, 1830 Nt Nt
99 Ctenomystuconax Thomas, 1925 Nt Nt
100 Ctenomystucumanus Thomas, 1900 Nt Nt
101 Ctenomystulduco Thomas, 1921 Nt Nt
102 Ctenomyssaltarius Thomas, 1912 Nt Nt
103 Ctenomysscagliai J. R. Contreras, 1999 Nt Nt
104 Ctenomyssericeus J. A. Allen, 1903 Nt Nt
105 Ctenomyssociabilis Pearson & Christie, 1985 Nt Nt
106 Ctenomyssteinbachi Thomas, 1907 Nt Nt
107 Ctenomysvalidus J. R. Contreras et al., 1977 Nt Nt
108 Ctenomysviperinus Thomas, 1926 Nt Nt
109 Ctenomysyatesi Gardner et al., 2014 Nt Nt
110 Ctenomysyolandae J. R. Contreras & Berry, 1984 Nt Nt
Hystricomorpha Histricognathi Octodontidae 111 Spalacopuscyanus (Molina, 1782) Nt Nt
Heterocephalidae 112 Heterocephalusglaber Rüppell, 1842 E E
Bathyergidae 113 Heliophobiusargenteocinereus Peters, 1846 E E
114 Bathyergusjanetta Thomas & Schwann, 1904 E E
115 Bathyergussuillus (Schreber, 1782) E E
116 Georychuscapensis (Pallas, 1778) E E
117 Cryptomyshottentotus (Lesson, 1826) E E
118 Fukomysamatus (Wroughton, 1907) E E
119 Fukomysanselli (Burda et al., 1999) E E
120 Fukomysbocagei (de Winton, 1897) E E
121 Fukomysdamarensis (Ogilby, 1838) E E
122 Fukomysdarlingi (Thomas 1895) E E
123 Fukomysfoxi (Thomas, 1911) E E
124 Fukomyskafuensis (Burda et al., 1999) E E
125 Fukomysmechowii (Peters, 1881) E E
126 Fukomysochraceocinereus (Heuglin, 1846) E E
127 Fukomysvandewoestijneae Van Daele et al., 2013 E E
128 Fukomyswhytei (Thomas, 1897) E E
129 Fukomyszechi (Matschie, 1900) E E
Myomorpha Cricetidae Arvicolinae Prometheomyini 130 Prometheomysschaposchnikowi Satunin, 1901 P P
Ellobiusini 131 Ellobiusalaicus Vorontsov et al., 1969 P P
132 Ellobiusfuscocapillus (Blyth, 1843) P P
133 Ellobiuslutescens Thomas, 1897 P P
134 Ellobiustalpinus (Pallas, 1770) P P
135 Ellobiustancrei Blasius, 1884 P P
Spalacidae Myospalacinae 136 Myospalaxarmandii (Milne-Edwards, 1867) P P
137 Myospalaxaspalax (Pallas, 1776) P P
138 Myospalaxepsilanus Thomas, 1912 P P
139 Myospalaxmyospalax (Laxmann, 1773) P P
140 Myospalaxpsilurus (Milne-Edwards, 1874) P P
141 Eospalaxbaileyi (Thomas, 1911) P P
142 Eospalaxcansus (Lyon, 1907) P P
143 Eospalaxfontanierii (Milne-Edwards, 1867) P P
144 Eospalaxrothschildi (Thomas, 1911) P P
145 Eospalaxrufescens (J. A. Allen, 1909) P P
146 Eospalaxsmithii (Thomas, 1911) P P
Rhizomyinae Rhizomyini 147 Rhizomyspruinosus (Blyth, 1851) P O
148 Rhizomyssinensis Gray, 1831 P O
149 Rhizomyssumatrensis (Raffles, 1821) O O
150 Cannomysbodius (Hodgson, 1841) O O
Tachyoryctini 151 Tachyoryctesmacrocephalus (Rüppell, 1842) E E
152 Tachyoryctessplendens (Rüppell, 1835) E E
Spalacinae 153 Spalaxantiquus Méhely, 1909 P P
154 Spalaxarenarius Reshetnik, 1939 P P
155 Spalaxgiganteus Nehring, 1898 P P
156 Spalaxgraecus Nehring, 1898 P P
157 Spalaxistricus Méhely, 1909 P P
158 Spalaxmicrophthalmus Güldenstädt, 1770 P P
159 Spalaxuralensis Tiflov & Usov, 1939 P P
160 Spalaxzemni (Erxleben, 1777) P P
161 Nannospalaxehrenbergi Nehring, 1898 P P
162 Nannospalaxleucodon (Nordmann, 1840) P P
163 Nannospalaxxanthodon (Nordmann, 1840) P P
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Based on macroevolutionary patterns derived from the study of the fossil record, subterranean rodent species diversity has appeared to have oscillated since early Oligocene time [ca. 36 million years ago, (mya)]. The Geomyidae Bonaparte, 1845 and the Bathyergidae Waterhouse, 1841 have the greatest diversity among all subterranean rodent families relative to the number of genera found throughout evolutionary time and identified thus far as fossil taxa (Cook et al. 2000). Fluctuation cycles in diversification, known as taxon pulses (Erwin 1985) appear to have been driven by local, regional, and global climate oscillations, and explained by the Stockholm Paradigm, which seeks to provide an understanding of the evolution of host-parasite/pathogen systems via the evolutionary process of species diversification following mass extinctions (Brooks et al. 2019).

Ethiopian subterranean rodents

Subterranean rodents in the Ethiopian zoogeographic region are represented by twenty species in seven genera across three families (Heterocephalidae, Bathyergidae, and Spalacidae) including Heterocephalus Rüppell, 1842, Heliophobius Peters, 1846, Bathyergus Illiger, 1811, Georychus Illiger, 1811, Cryptomys Gray, 1864, Fukomys Kock et al., 2006, and Tachyoryctes Rüppell, 1835 (see Landry 1957; Patterson and Upham 2014; Wilson et al. 2016).

Nearctic subterranean rodents

Species of the family Geomyidae are endemic to the Nearctic and northern Neotropics and are known collectively as pocket gophers due to presence of fur-lined cheek pouches in all species. They are a monophyletic group of subterranean rodents that share common ancestry with rodents of the family Heteromyidae (Wilson et al. 2016). Pocket gophers inhabit a wide geographic range, extending from a northernmost limit in southwest and south-central Canada through the central and western United States, southeast into central Florida, and south into Mexico and through Central America into Panama and near the Rio Atrato in northern Colombia (Hall 1981; Alberico 1990; Solari et al. 2013). As in most subterranean rodents, pocket gophers are fusiform in shape, having a naked and sensitive tail (they can run backwards as fast as they can forwards, using their tail as a rear-guide sensor (Gardner, pers. obs.). They have small pinnae, loose skin, and their fur-lined cheek pouches are used only for food transport (Howard and Childs 1959; Maser et al. 1981; Hafner 1982; Honeycutt and Williams 1982; Hafner et al. 1994). The family consists of seven extant genera and 41 species (Wilson et al. 2016). The genus Thomomys Wied-Niewied, 1839, has 12 species and many subspecies, making this genus the most speciose of the family Geomyidae (see Patton 2005).

Palearctic subterranean rodents

Thirty-two species of subterranean rodents of seven genera in two families, including Cricetidae Fischer, 1817, and Spalacidae Gray, 1821, occur in the Palearctic region. Those include Prometheomys Satunin, 1901, and Ellobius Fischer, 1814, in the family Cricetidae, which includes the subfamily Arvicolinae Gray, 1821. The genera Myospalax Laxmann, 1769, Eospalax Allen, 1938, Rhizomys Gray, 1831, Cannomys Thomas, 1915, Spalax Guldenstaedt, 1770, and Nannospalax (Nordmann, 1840) are in the family Spalacidae which includes the subfamilies Myospalacinae Lilljeborg, 1866, Rhizomyinae Winge, 1887, and Spalacinae Gray, 1821. Among all subterranean forms of the Rodentia, those occurring in the Palearctic region have the most extensive geographic distribution. Based on fossil evidence, the first known subterranean species of rodents appeared in the early Pliocene of Asia (Repenning 1984; Repenning et al. 1990). Rhizomyspruinosus (Blyth, 1851) and Rhizomyssinensis Gray, 1831 occur in the Palearctic and Oriental zoogeographic regions. At the current time, only two species of subterranean rodents are known from the Oriental region, and those include Rhizomyssumatrensis (Raffles, 1821) and Cannomysbodius (Hodgson, 1841).

Neotropical subterranean rodents

The Neotropical subterranean rodents are represented by two hystricognath Caviomorph families, the Ctenomyidae Lesson, 1842 and Octodontidae Waterhouse, 1839. The family Ctenomyidae currently includes only species in the genus Ctenomys Blainville, 1826 which are known as the tuco-tucos, with approximately 69 described species. These rodents occur in suitable habitats with a geographic distribution from southern Peru and southwestern Brazil south to Tierra de Fuego through Chile, Argentina, Bolivia, Paraguay, and Uruguay (Reig et al. 1990; Gardner et al. 2014). The fossil record indicates that species that can be allocated to the family Ctenomyidae originated ca. 10 mya (Cook et al. 2000), with rapid diversification in the genus Ctenomys commencing at ca. 3 mya (Parada et al. 2011). Interestingly, the single subterranean species in the Octodontidae which are the sister taxon of the Ctenomyidae includes the monotypic Spalacopuscyanus (Molina, 1782) and these occur only in central Chile.

Endoparasites

Our analysis shows that endoparasites have been found and reported from fewer than 40% of known species of subterranean rodents world-wide. There are several factors that could potentially explain this lack of reported data as researchers face several challenges when trapping subterranean rodents; without prior training, just finding and then determining active subterranean mammal burrow mounds is difficult. There could be thousands of burrow mounds, but researchers need acute field expertise to identify freshly dug burrows to capture these animals. Moreover, setting subterranean rodent traps is labor intensive and time-consuming, demanding lots of patience, physical strength, and luck.

Another problem is that sampling of species of subterranean rodents has not been systematically carried out and most collecting was done over time that was rather scattered and sporadic, and very few collections included parasites in their investigations. Many previous studies have failed to record comprehensive data during their collections of mammals and other vertebrates, discarding the internal organs of collected mammals without further examination. This practice resulted in significant gaps in parasite data with black holes regarding their faunas of both ecto- and endoparasites. Parasites discovered in research projects contain vital information about themselves and their host life history, consisting of information that we cannot ignore. The work presented here represents a synthesis of all available literature on the endoparasites of subterranean rodents of the world, as such, some references and works may have been missed, but we hope that this list provides a starting point for other researchers interested in this area of study.

Materials and methods

The current checklist was created by accumulating all published references arranged in a chronologically ordered tabular form representing globally each continent. The taxonomic status of each host and parasite species are up to date and represent the most current classifications. Most of the early literature was located in the reprint library of the H.W. Manter Laboratory of Parasitology in the University of Nebraska State Museum. Some of the literature was obtained from the Digital Commons at University of Nebraska-Lincoln Libraries while several rare international references were obtained through interlibrary loan. For new records presented herein, some samples were collected during the field Parasitology class in western Nebraska and others were included from field work by S.L. Gardner in the 1980’s the 1990’s and earlier. Except for a few instances that we detail in the results, we used the original taxonomic names of both the hosts and parasites as published in the original literature. Throughout this paper, we used the zoogeographic terminology first established by Wallace (1876) (Rueda et al. 2013).

Results

Literature review

Ethiopian subterranean rodent endoparasites

See graphical summary in Fig. 1 and endoparasite diversity list in Table 2.

Figure 1.

Figure 1.

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Pie diagram representing percentage taxon composition of the higher classification of endoparasite diversity found infecting subterranean rodents from the Ethiopian zoogeographic region derived from records in the literature published from 1864 through 2018. The Nemata are the most speciose representing 54% of the total endoparasite fauna, followed by Cestoda (34%), and Protozoa (12%).

Table 2.

Endoparasite species diversity of Ethiopian subterranean rodents and their known original hosts. Authorities are given for parasite and host species.

Host species Parasite species References
Bathyergussuillus (Schreber, 1782) Mammalakismacrospiculum (Ortlepp, 1939) Lutermann et al. 2012
Ortleppstrongylusbathyergi Ortlepp, 1939 De Graaff 1964
Paralibyostrongylusbathyergi (Ortlepp, 1939) Lutermann et al. 2012
Rodentolepis Spasskii, 1954 Lutermann et al. 2012
Taenia Linnaeus, 1758 Lutermann et al. 2012
Trichostrongylus Looss, 1905 De Graaff 1964
Trichuris Roederer, 1761 Lutermann et al. 2012
Cryptomyshottentotus (Lesson, 1826) Ascaropsafricana (Sandground, 1933) Lutermann et al. 2013
Heligmonina Baylis, 1928 Viljoen et al. 2011
Inermicapsifermadagascariensis (Davaine, 1870) De Graaff 1981
Mammalakismacrospiculum (Ortlepp, 1939) Archer et al. 2017
Mathevotaenia Akhumyan, 1946 Viljoen et al. 2011
Neoheligmonella Durette-Desset, 1971 Archer et al. 2017
Protospirura Seurat, 1914 Viljoen et al. 2011
Raillietina Fuhrman, 1920 Lutermann et al. 2013
Trichuris Roederer, 1761 Archer et al. 2017
Fukomysanselli (Burda et al., 1999) Hexametra Travassos, 1920 Lutermann et al. 2018
Inermicapsifer Janicki, 1910 Lutermann et al. 2018
Mammalakiszambiensis Junker et al., 2017 Junker et al. 2017
Protospiruramuricola (Gedoelst, 1916) Lutermann et al. 2018
Protospiruranumidica Seurat, 1914 Lutermann et al. 2018
Protospirura Seurat, 1914 Lutermann et al. 2018
Rodentolepiscf.microstoma (Dujardin, 1945) Lutermann et al. 2018
Fukomyskafuensis (Burda et al., 1999) Inermicapsifermadagascariensis (Davaine, 1870) Scharff et al. 1997
Protospiruramuricola (Gedoelst, 1916) Scharff et al. 1997
Fukomysmechowii (Peters, 1881) Capillaria Zeder, 1800 Scharff et al. 1997
Inermicapsifermadagascariensis (Davaine, 1870) Scharff et al. 1997
Protospiruramuricola (Gedoelst, 1916) Scharff et al. 1997
Raillietina Fuhrman, 1920 Scharff et al. 1997
Georychuscapensis (Pallas, 1778) Coenurusspalacis Diesing, 1864 Diesing 1864
Echinococcus Rudolphi, 1801 De Graaff 1964; Hüttner and Romig 2009
Trichuris Roederer, 1761 Lutermann et al. 2012
Heliophobiusargenteocinereus Peters, 1846 Eimeriaburdai Koudela et al., 2000 Koudela et al. 2000
Eimeriaheliophobii Modrý et al., 2005 Modrý et al. 2005
Eimerianafuko Modrý et al., 2005 Modrý et al. 2005
Eimeriayamikamiae Modrý et al., 2005 Modrý et al. 2005
Inermicapsiferarvicanthidis (Kofend, 1917) Baruš et al. 2003; Tenora et al. 2003
Protospiruramuricola (Gedoelst, 1916) Baruš et al. 2003; Tenora et al. 2003
Heterocephalusglaber Rüppell, 1842 Eimeriaheterocephali Levine & Ivens, 1965 Levine and Ivens 1965
Tachyoryctessplendens (Rüppell, 1835) Taeniabrauni Setti, 1897 Fain 1956
Tachyoryctesmacrocephalus (Rüppell, 1842) Ascaropsafricana (Sandground, 1933) Schmidt and Canaris 1968
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Diesing (1864) reported the first helminth parasite species from a subterranean rodent host, where Taeniaspalacis (Diesing, 1864) was reported from Georychuscapensis (Pallas, 1779) collected from Port Natal, South Africa.

Ortlepp (1939) described three new nematode species from the Cape dune mole-rat, Bathyergussuillus (Schreber, 1782) (Bathyergidae: Rodentia) collected from Strandfontein and Cape Town, South Africa including: Libyostrongylusbathyergi Ortlepp, 1939, Longistriatabathyergi, and Mammalakismacrospiculum (see Ortlepp 1939; Inglis 1991). These represent the first known reports of parasitic nematodes from African subterranean rodents. Interestingly, all these species have been reclassified into different genera and are currently known as Paralibyostrongylusbathyergi, Ortleppstrongylusbathyergi, and Mammalakismacrospiculum, (see De Graaff 1964; Lutermann and Bennett 2012).

Fain (1956) reported Taeniabrauni Setti, 1897, from Tachyoryctessplendens (Rüppell, 1835) collected in Ruanda-Urundi, East Africa. After a period of several years, De Graaff (1964) mentioned that in a personal communication that he had with Ortlepp an unidentified tapeworm was obtained by Ortlepp from Bathyergussuillus, collected at Houtbay, near Cape Town. Also, De Graaff (1964) wrote that Ortlepp told him that he found cysts of an unidentified species of Echinococcus Rudolphi, 1801 obtained from the muscles of the abdominal cavity as well as liver of G.capensis collected at Wynberg, near Cape Town, South Africa (Hüttner and Romig 2009).

Levine and Ivens (1965) described the first coccidian parasite, Eimeriaheterocephali from the mucosal epithelial cells of the cecum of a Heterocephalusglaber specimen collected at Somaliland or Kenya, South Africa.

Schmidt and Canaris (1968) reported Ascaropsafricana (Sandground, 1933) from Tachyoryctesmacrocephalus (Rüppell, 1842) collected from Njoro, Kenya, East Africa.

Several years later, De Graaff (1981) reported Inermicapsifermadagascariensis (Davaine, 1870) from the Common mole-rat, Cryptomyshottentotus (Lesson, 1826) (Bathyergidae: Hystricomorpha), collected from Shingwedzi, South Africa.

Scharff et al. (1997) reported Inermicapsifermadagascariensis from the small intestine, and Protospiruramuricola (Gedoelst, 1916) from the colon of Fukomyskafuensis (Burda et al., 1999) collected from Itezhi-Tezhi, Zambia. They also found an unidentified species of Calodium Moravec, 1982 (syn. Capillaria Zeder, 1800) (eggs only), I.madagascariensis, and an unknown Raillietina Fuhrman, 1920, from the small intestine, and P.muricola from the abdominal cavity of Fukomysmechowii (Peters, 1881) collected from Ndole, Zambia. The discovery of P.muricola in the abdominal cavity was probably a result of these nematodes moving from the stomach during or after the necropsy event of the individual F.mechowii mentioned.

Koudela et al. (2000) described Eimeriaburdai, as a new species of coccidian from the subterranean African silvery mole-rat, Heliophobiusargenteocinereus Peters, 1846, collected from Lubalashi Province, central Zambia.

Baruš et al. (2003) studied the relative concentration of heavy metals in helminth parasites; several Silvery mole-rats, H.argenteocinereus, were necropsied for their internal parasite tissues collected from the Blantyre-Limbe region of Malawi, southeastern Africa. As a result, two species of helminths were found, including Inermicapsiferarvicanthidis (Kofend, 1917) and Protospiruramuricola, and these specimens were later examined for four heavy metal elements (cadmium, copper, lead, and zinc), and compared against the liver and muscle tissues of their hosts. The same species of parasites from these same hosts were reported by Tenora et al. (2003).

Modrý et al. (2005) described three new species of Eimeria from the Silvery mole-rat H.argenteocinereus from Malawi, including: Eimeriaheliophobii, E.nafuko, and E.yamikamiae extracted from the fecal samples from the host specimens.

Viljoen et al. (2011), in an ecological study of the role of host traits, season, and group size on parasite burdens in a cooperative breeding mammal, captured 87 individual mole-rats were from the Tshwane region of South Africa in different seasons. Three helminths that were not identified to the species level were obtained from the small intestine of Cryptomyshottentotus, including Heligmonina sp. Baylis, 1928, Mathevotaenia sp. Akhumyan, 1946, and Protospirura sp. Seurat, 1914.

Lutermann and Bennett (2012), during a year-long joint research and eradication project for Bathyergussuillus at Cape Town International Airport, Cape Town, South Africa, found these rodents infected with three species of nematodes, including: Mammalakismacrospiculum, Paralibyostrongylusbathyergi, and Trichuris sp. Roederer, 1761, and two species of tapeworms, Rodentolepis sp. Spasskii, 1954, and Taenia sp. Linnaeus, 1758.

Just one year later, Lutermann et al. (2013), during the study on energetic benefits and costs of parasitism in a cooperative mammal identified Raillietina sp., and Ascaropsafricana from the small intestine of Cryptomyshottentotus collected from KwaZulu-Natal, South Africa.

Archer et al. (2017), in a seasonal comparative study between two Common mole-rat populations found Mammalakismacrospiculum, Neoheligmonella Durette-Desset, 1971, and Trichuris sp. in Cryptomyshottentotus collected from two different habitats, including an arid site, 25 km outside of Kamieskroon, the Northern Cape and a mesic site near Darling, western Cape, South Africa.

Junker et al. (2017) described a new species of ascaridid nematode, Mammalakiszambiensis acquired from the large intestine and cecum of Ansell’s mole-rat, Fukomysanselli (Burda et al., 1999), captured from west of Lusaka at Mukulaikwa Farm Block, Zambia.

Lutermann et al. (2018) reported the following gastrointestinal parasites from Ansell’s mole-rat, F.anselli in Zambia. Those include Hexametra sp. Travassos, 1920, Inermicapsifer sp. Janicki, 1910, Protospiruramuricola, Protospiruranumidica Seurat, 1914, and Rodentolepiscf.microstoma (Dujardin, 1945).

Palearctic subterranean rodent endoparasites

See graphical summary in Fig. 2 and endoparasite list in Table 3.

Figure 2.

Figure 2.

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Pie chart showing percentage of infection summary of the higher-level classification of endoparasite diversity among Palearctic subterranean rodents derived from a survey of published records from 1927 through 2022. Protozoa constitute the greatest diversity of endoparasites accounting for 39% of the total parasite species recovered followed by Nemata (30%), Cestoda (27%), Acanthocephala (3%), and the Trematoda coming in at only 1%.

Table 3.

Endoparasite species diversity of Palearctic subterranean rodents and their known original hosts. Authorities are given for parasite and host species.

Host species Parasite species References
Cannomysbodius (Hodgson, 1841) Hymenolepisdiminuta (Rudolphi, 1819) Malsawmtluangi and Tandon 2009
Ellobiusfuscocapillus (Blyth, 1843) Syphaciaobvelata (Rudolphi, 1802) Arzamani et al. 2017
Ellobiuslutescens Thomas, 1897 Eimerialutescenae Musaev & Veisov, 1963 Musaev and Veisov 1965a
Ellobiustalpinus (Pallas, 1770) Aprostatandryamacrocephala Douthitt, 1915 Tokobaev 1960
Catenotaeniapusilla Goeze, 1782 Zanina and Tokobaev 1962a
Echinococcusmultilocularis Leuckart, 1863 Tokobaev 1960
Eimeriaellobii Svanbaev, 1965 Musaev and Veisov 1965a
Eimeriakazakhstanensis Levine, 1965 Levine and Ivens 1965
Eimeriatadshikistanica Veisov, 1964 Musaev and Veisov 1965a
Eimeriatalpini Levine, 1965 Levine and Ivens 1965
Hymenolepisdiminuta (Rudolphi, 1819) Zanina and Tokobaev 1962a
Mesocestoides Vaillant, 1863 Tokobaev 1960
Moniliformismoniliformis Bremser, 1811 Zanina and Tokobaev 1962a
Nomadolepisellobii Makarikov et al., 2010 Makarikov et al. 2010
Physocephalusellobii Schulz, 1927 Schultz 1927
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Zanina and Tokobaev 1962a
Ellobiustancrei Blasius, 1884 Arostrilepisbatsaikhani Dursahinhan et al., 2022 Dursahinhan et al. 2022
Echinococcusmultilocularis Leuckart, 1863 Afonso et al. 2015
Eospalaxbaileyi (Thomas, 1911) Eimeriabaileyii Cao et al., 2014 Cao et al. 2014
Eimeriafani Cao et al., 2014 Cao et al. 2014
Eimeriamenyuanensis Cao et al., 2014 Cao et al. 2014
Eimeriamyospalacensis Cao et al., 2014 Cao et al. 2014
Ransomusqinghaiensis Ming et al., 2004 Ming et al. 2004
Versteria (syn. Taenia) mustelae Gmelin, 1790 Zhao, et al. 2014
Eospalaxfontanierii (Milne-Edwards, 1867) Echinococcusmultilocularis Leuckart, 1863 Craig 2006
Heligmopteragiraudouxi Elias et al., 2002 Elias, et al. 2002
Heligmopteraquerei Elias et al., 2002 Elias, et al. 2002
Myospalaxmyospalax (Laxmann, 1773) Echinococcusmultilocularis Leuckart, 1863 Shaykenov and Mahmutov 1968
Heligmopterasibirica Shakhmatova, 1990 Shakhmatova 1990
Heligmosomummyospalaxi Nadtochii, 1970 Nadtochii 1970
Hymenolepisrymzhanovi Makarikov & Tkach, 2013 Makarikov and Tkach 2013
Moniliformisclarki (Ward, 1917) Vlasenko and Krivopalov 2017
Paranoplocephala Lühe, 1910 Vlasenko and Krivopalov 2017
Versteriamustelae (Gmelin, 1790) Vlasenko and Krivopalov 2017
Myospalaxpsilurus (Milne-Edwards, 1874) Ascaropsstrongylina (Rudolphi, 1819) Ganzorig et al. 1999
Nannospalaxehrenbergi Nehring, 1898 Eimeriaadiyamanensis Sayin, 1980 Sayın 1980
Eimeriaanzanensis Couch et al, 1993 Couch et al. 1993
Eimeriacarmelensis Couch et al, 1993 Couch et al. 1993
Eimeriacelebii Sayin, 1980 Sayın 1980
Eimeriaharanica Sayin, 1980 Sayın 1980
Eimeriamarasensis Sayin, 1980 Sayın 1980
Eimeriamicrospalacis Golemansky & Darawish, 1992 Golemansky and Darwish 1992
Eimeriaoytuni Sayin, 1980 Sayın 1980
Eimeriaspalacensis Couch et al, 1993 Couch et al. 1993
Eimeriatorosicum Sayin, 1980 Sayın 1980
Eimeriaurfensis Sayin, 1980 Sayın 1980
Ganguleterakisspalaxi Kozlov & Yangolenko, 1963 Wertheim and Nevo 1971
Gongylonemalongispiculum Schulz, 1927 Wertheim and Nevo 1971
Heligmonella Mönnig, 1927 Wertheim and Nevo 1971
Heligmoninanevoi Wertheim & Nevo, 1971 Wertheim and Nevo 1971
Isosporaspalacensis Couch et al, 1993 Couch et al. 1993
Microcephaloidesnevoi (Fair et al., 1990) Haukisalmi 2009 Fair et al. 1990; Haukisalmi 2009
Trichurismuris (Schrank, 1788) Wertheim and Nevo 1971
Nannospalaxleucodon (Nordmann, 1840) Aprostatandrya Kirshenblat, 1938 Andreiko 1963a
Ascarisspalacis Shults & Aloyan, 1950 Shults and Aloyan 1950
Coenurusparviuncinatus Kirschenblatt, 1939 Korniushin and Sharpilo 1986
Eimeriacelebii Sayin, 1980 Nalbantoğlu et al. 2010
Eimeriaelliptica Sayin et al., 1977 Sayin et al. 1977
Eimerialalahanensis Sayin, et al., 1977 Sayin et al. 1977
Eimerialeucodonica Veisov, 1975 Veisov 1975
Eimeriamaralikiensis Veisov, 1975 Veisov 1975
Eimeriaoytuni Sayin, 1980 Nalbantoğlu et al. 2010
Eimeriaspalacis Sayin et al., 1977 Sayin et al. 1977
Eimeriatalikiensis Veisov, 1975 Veisov 1975
Eimeriatorosicum Sayin, 1980 Nalbantoğlu et al. 2010
Eimeriaturkmenica Sayin et al., 1977 Sayin et al. 1977
Eimeriatuzdili Sayin, et al., 1977 Sayin et al. 1977
Heligmosomumspalacis Kirsenblat, 1965 Mészáros 1968
Heligmosomummoldovensis Andreiko, 1963 Andreiko 1963a
Isosporaanatolicum Sayin, et al., 1977 Sayin et al. 1977
Longistriataspalacis Sharpilo, 1973 Sharpilo 1973a
Mammalakisspalacis Marcu, 1930 Andreiko 1963a
Moniliformismoniliformis Bremser, 1811 Murai 1968
Taeniastraminea (Goeze, 1782) Spasskii 1954 Andreiko 1963a
Prometheomysschaposchnikowi Satunin, 1901 Dicrocoeliumdendriticum (Rudolphi, 1819) Razumova 1957
Heligmosomumhalli (Schulz, 1926) Razumova 1957
Microcephaloides Haukisalmi et al., 2008 Razumova 1957
Taeniapolyacantha Leuckart, 1856 Razumova 1957
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Razumova 1957
Rhizomyspruinosus (Blyth, 1851) Mammalakisspumosa (Schneider, 1866) Chaisiri et al. 2017
Rhizomyssinensis Gray, 1831 Cryptosporidiumoccultus Kváč, 2018 Wei et al. 2019
Cryptosporidiumparvum Tyzzer, 1912 Wei et al. 2019
Spalaxarenarius Reshetnik, 1939 Longistriataspalacis Sharpilo, 1973 Sharpilo 1973a
Spalaxgraecus Nehring, 1898 Heligmosomumspalacis Kirsenblat, 1965 Kirshenblat 1965a
Spalaxmicrophthalmus Güldenstädt, 1770 Ganguleterakisspalaxi Kozlov & Yangolenko, 1963 Kozlov and Yangolenko 1963a
Gongylonemalongispiculumspalacis Schulz, 1927 Schultz 1927
Longistriataspalacis Sharpilo, 1973 Sharpilo 1973a
Mammalakisspalacis Marcu, 1930 Marcu 1930
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Sharpilo 1976
Trichurisspalacis (Petrov & Potechina, 1953) Petrov and Potechina 1953
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Interestingly, even though helminthology began in Europe (the western Palearctic) in the late 1800’s with the work of Leuckart, it was not until the 1920’s when Schulz (1927) described the first two species of helminth parasites from two species of subterranean rodents from the Palearctic region. First, Physocephalusellobii Schulz, 1927 was found from the stomach of Ellobiustancrei Blasius, 1884 collected from Kotlyrevsky, the northern Caucasus region of Russia. Second, Gongylonemalongispiculumspalacis Schulz, 1927 was described as the first subspecies found under the mucous membrane of the stomach of Spalaxmicrophthalmus Güldenstädt, 1770 collected from the village Kurichya Kosa near the Don River region north of the coast of the Sea of Azov, Russia. Soon after, Marcu (1930) described Mammalakisspalacis Marcu, 1930 also obtained from S.microphthalmus collected from Romania.

Somewhat later, Schulz and Aloyan (1950), described Ascarisspalacis Schulz & Aloyan, 1950 from Lesser mole-rat, Nannospalaxleucodon (Nordmann, 1840). Kirshenblat collected the materials included in the description from near the small towns of Amamla and Chandura, of the Spitakskii and Akhalkalakskii regions of Armenia, in 1947. All these nematode samples were found from the small intestines of the hosts, necropsied by Aloyan in 1948.

Petrov and Potechina (1953) described Trichurisspalacis from S.microphthalmus collected from an unspecified locality in Ukraine.

Razumova (1957) reported the following helminth parasites found in specimens of the Long-clawed mole vole, Prometheomysschaposchnikowi Satunin, 1901, captured from Ossetia, Russia. These include Dicrocoeliumdendriticum (Rudolphi, 1819), Heligmosomumhalli (Schulz, 1926), Microcephaloides Haukisalmi et al., 2008, Taeniapolyacantha Leuckart, 1856, and Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786).

Tokobaev (1960) reported the collection of Ellobiustalpinus (Pallas, 1770) from the Kyrgyz Republic and found larvae of Echinococcusmultilocularis from the liver. In the same report, he reported Aprostatandryamacrocephala Douthitt, 1915, from the small intestine and larvae of Mesocestoides Vaillant, 1863 from the body cavity, liver, and small intestines. In work on mole voles just a short time later, Zanina and Tokobaev (1962) reported Catenotaeniapusilla Goeze, 1782, Hymenolepisdiminuta Rudolphi, 1819, Moniliformismoniliformis Bremser, 1811, and Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) from E.talpinus collected in Tajikistan.

Andreiko (1963) reported that from 1959 through 1962, 70 Lesser mole-rats, (Nannospalaxleucodon) collected from the central part of Moldova, Romania had the following helminths: Mammalakisspalacis from the cecum, Taeniastraminea (Goeze, 1782) Spasskii, 1954 and unidentified species of Aprostatandrya Kirshenblat, 1938 from the small intestine. In addition, she described Heligmosomummoldovensis Andreiko, 1963 from the small intestine of N.leucodon.

Kozlov and Yangolenko (1963) described Ganguleterakisspalaxi Kozlov & Yangolenko, 1963 from Spalaxmicrophthalmus collected from Ukraine.

Kirshenblat (1965) described a new species of nematode Heligmosomumspalacis from the small intestine of the mole-rat Spalaxgraecus Nehring, 1898 collected from Chernivtsi, Ukraine.

Levine and Ivens (1965) described two species of Eimeria Fischer, 1814 from the Northern mole vole, including: Ellobiuskazakhstanensis Levine & Ivens, 1965, and Ellobiustalpini Levine & Ivens, 1965 from the fecal of Ellobiustalpinus collected from Kazakhstan.

Musaev and Veisov (1963) described Eimerialutescenae Musaev & Veisov, 1963 from Ellobiuslutescens Thomas, 1897 from Nakhichevanskaia, Azerbaijan. In addition, two Eimeria (Schneider, 1875) species were reported with their descriptions, including: Eimeriaellobii Svanbaev, 1965 and Eimeriatadshikistanica Veisov, 1964 from Ellobiustalpinus collected from Tajikistan.

Shaykenov and Mahmutov (1968) reported Echinococcusmultilocularis found in Myospalaxmyospalax (Laxmann, 1773) collected from eastern Kazakhstan. This record is considered a new intermediate host for this tapeworm. Also in the same year, Mészáros (1968) reported the occurrence of Heligmosomumspalacis recovered from the Lesser mole-rat, Nannospalaxleucodon, collected from Hungary.

Murai (1968) recorded the Lesser mole-rat, N.leucodon, as a new host of Moniliformismoniliformis. The acanthocephalid parasite was extracted from the small intestines of two individuals of Lesser mole-rats. Also, Heligmosomumspalacis was found in the host. The study has conducted near Hajdubagos village, Hajdu-Bihar, in Hungary.

Nadtochii (1970), during a study of helminth parasites of rodents in far eastern Russia, the author described Heligmosomummyospalaxi Nadtochii, 1970 obtained from the small intestine of Myospalaxmyospalax collected from the seashore of eastern Russia.

Wertheim and Nevo (1971), during a study of helminths of birds and mammals from Israel recovered several species of helminth parasites from the Middle East blind mole-rat, Nannospalaxehrenbergi Nehring, 1898 including Ganguleterakisspalaxi, Gongylonemalongispiculum Schulz, 1927, Trichurismuris (Schrank, 1788), and one unidentified nematode in the genus Heligmonella Mönnig, 1927. They also described Heligmoninanevoi Wertheim & Nevo, 1971 from the same host species.

Sharpilo (1973) described Longistriataspalacis from the small intestine of Lesser mole-rat, Nannospalaxleucodon. He reported that this nematode species was also found from Spalaxarenarius Reshetnik, 1939, and Spalaxmicrophthalmus. These specimens were all collected from Ukraine.

Sharpilo (1976), during a study of helminth parasites of rodent fauna in Ukraine, reported Hydatigera (syn. Taenia) taeniaeformis from Spalaxmicrophthalmus.

Veisov (1975) described three new species of coccidia of the genus Eimeria Schneider, 1875 from Nannospalaxleucodon, including Eimeriamaralikiensis Veisov, 1975 and Eimeriatalikiensis Veisov, 1975 collected from Talnisk and Maralik Aniisk regions, Armenian, also, describing Eimerialeucodonica Veisov, 1975 from the Talinsk region only.

Sayin et al. (1977), during a survey of Lesser mole-rats, Nannospalaxleucodon, in Lalahan district in Ankara, Turkey, described six new species of coccidia in the genus Eimeria Schneider, 1875 including E.ellipticaSayin et al., 1977, E.lalahanensisSayin et al., 1977, E.spalacisSayin et al., 1977, E.turkmenicaSayin et al., 1977, E.tuzdiliSayin et al., 1977, and IsosporaanatolicumSayin et al., 1977.

Sayın (1980), during a survey conducted from 1976 through 1978, studied 41 individuals of the Middle East blind mole-rats, Nannospalaxehrenbergi, from Urfa, Adiyaman, and Maras provinces in Turkey. As a result, seven new species of coccidia of the genus Eimeria Schneider, 1875 were described. Those include E.adiyamanensis Sayın, 1980, E.celebii Sayın, 1980, E.haranica Sayın, 1980, E.marasensis Sayın, 1980, E.oytuni Sayın, 1980, E.torosicum Sayın, 1980, and E.urfensis Sayın, 1980.

Korniushin and Sharpilo (1986) reported a larval Taenia which they reported as Coenurusparviuncinatus Kirschenblatt, 1939 obtained from Nannospalaxleucodon collected from Armenia.

Fair et al. (1990) described a new species of tapeworm, MicrocephaloidesnevoiFair et al., 1990 from the Middle East blind mole-rat Nannospalaxehrenbergi in Masada, Golan Heights, Israel. This species has been redescribed by Haukisalmi (2009).

Shakhmatova (1990) described Heligmopterasibirica Shakhmatova, 1990 found from the Siberian zokor, Myospalaxmyospalax, collected from the Gorno-Altai autonomous region of Russia.

Golemansky and Darwish (1992) described Eimeriamicrospalacis Golemansky & Darwish, 1992 from the Middle East blind mole-rat, Nannospalaxehrenbergi, collected from the regions of Damascus and Latakia, western Syria.

Couch et al. (1993) described four coccidian parasites obtained from the Middle East blind mole-rat, Nannospalaxehrenbergi, collected from 12 different localities in Israel including EimeriaanzanensisCouch et al., 1993, E.carmelensisCouch et al., 1993, E.spalacensisCouch et al., 1993, and IsosporaspalacensisCouch et al., 1993.

Ganzorig et al. (1999) redescribed Ascaropsstrongylina (Rudolphi, 1819) from the Transbaikal zokor, Myospalaxpsilurus (Milne-Edwards, 1874) collected from near the Halh Gol River, Dornod province, eastern Mongolia.

Elias et al. (2002), during a joint program of French, British, and China on echinococcosis screening in Zhang County, China (Gansu), two new species of Heligmoptera Nadtochiy, 1977 were described from the small intestines of the Chinese zokor, Eospalaxfontanierii (Milne-Edwards, 1867) including: Heligmopteragiraudouxi Elias & Durette-Desset, 2002, and Heligmopteraquerei Elias & Durette-Desset, 2002 with the new description of the genus.

More recently in China, Ming et al. (2004) described RansomusqinghaiensisMing et al., 2004 from the cecum of the Plateau zokor, Eospalaxbaileyi (Thomas, 1911) collected from Qilian County, Qinghai province.

Craig (2006), in a survey and epidemiological assessment of human alveolar echinococcosis in 33 provinces of China, listed the Chinese zokor, Eospalaxfontanierii as one of the intermediate hosts of Echinococcusmultilocularis.

Malsawmtluangi and Tandon (2009) reported Hymenolepisdiminuta attained from the Lesser bamboo rat, Cannomysbodius (Hodgson, 1841) collected from Mizoram, northeast India.

Nalbantoğlu et al. (2010) reported three species of coccidia acquired from the feces of the Lesser mole-rat, Nannospalaxleucodon, collected from the Eryaman district of Ankara, Turkey. Those are Eimeriacelebii , E.oytuni Sayin, 1980, and E.torosicum Sayin, 1980. In the same year, Makarikov et al. (2010) described the cestode NomadolepisellobiiMakarikov et al., 2010, simultaneously establishing a new genus for the tapeworm that was obtained from the small intestine of the Northern mole vole, Ellobiustalpinus, collected from southwestern Siberia, Russia.

Soon after, Makarikov and Tkach (2013) described Hymenolepisrymzhanovi Makarikov & Tkach, 2013 from the small intestine of the Siberian zokor, Myospalaxmyospalax collected from eastern Kazakhstan.

Cao et al. (2014) described four new species of Eimeria from the Plateau zokor, Eospalaxbaileyi, collected from Haibei area, Qinghai Province, China. The parasites include EimeriabaileyiiCao et al., 2014, EimeriafaniCao et al., 2014, EimeriamenyuanensisCao et al., 2014, and EimeriamyospalacensisCao et al., 2014. In the same year, Zhao et al. (2014) identified Versteria (syn. Taenia) mustelae (Gmelin, 1790) using DNA sequencing of larval cysts found in the Plateau zokor, Eospalaxbaileyi collected from Datong County, east of Qinghai province, China. In this study, no data were provided on number of individuals infected.

Afonso et al. (2015) reported Echinococcusmultilocularis from the livers of Eastern mole voles, Ellobiustancrei which acts as the intermediate host for this cestode, collected from Sary Mogol, Alay valley, Kyrgyzstan. The authors also noted that the definitive hosts were local domestic dogs, whose feces were examined for E.multilocularis. The parasite samples from the dogs were genetically identical to those found in the intermediate host.

In 2017, a flurry of activity resulted from workers in the field. Vlasenko and Krivopalov (2017) reported Moniliformisclarki (Ward, 1917), Paranoplocephala Lühe, 1910 and larvae of Versteriamustelae (Gmelin, 1790) from Myospalaxmyospalax collected from the southern Tomsk region, Russia. Then, Arzamani et al. (2017) reported Syphaciaobvelata (Rudolphi, 1802) (probably a misidentification as S.obvelata occurs only in species of Mus) obtained in the Southern mole vole, Ellobiusfuscocapillus (Blyth, 1843), collected from north Khorasan province of northeast Iran. Finally in 2017, Chaisiri et al. (2017), during an ecological study of host-parasite associations, reported Mammalakisspumosa (Schneider, 1866) from Rhizomyspruinosus in Cambodia.

Wei et al. (2019) reported Cryptosporidiumparvum Tyzzer, 1912 and C.occultus Kváč, 2018 found in the Chinese bamboo rat, Rhizomyssinensis, collected from south-central China.

Dursahinhan et al. (2022) described Arostrilepisbatsaikhani from the Zaisan mole vole, Ellobiustancrei collected from Baitag Bogd, Hovd province, western Mongolia.

Endoparasites of Nearctic and northern Neotropical subterranean rodents

See graphical summary in Fig. 3 and endoparasite list Table 4.

Figure 3.

Figure 3.

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Percentage taxon composition pie diagram of the higher classification of endoparasite diversity occurring in Nearctic subterranean rodents (Family Geomyidae) derived from literature records published from 1857 through 2020. Among these endoparasites, the Nemata represent 46% of the species found followed by Cestoda (41%), Protozoa (11%), and Acanthocephala at just 2%.

Table 4.

Endoparasite species diversity of Nearctic and Neotropical regions of subterranean rodents in the family Geomyidae and their known hosts. Authorities are given for parasite and host species. The new host-parasite associations recorded in this work are denoted by ‘Present study’ in bold.

Host species Parasite species References
Cratogeomyscastanops (Baird, 1852) Calodiumamericanum (Read, 1949) Present study
Eimeriageomydis Skidmore, 1929 Present study
Monoecocestus sp. Beddard, 1914 Present study
Vexillataconvoluta Caballero & Cerecero, 1943 Present study
Cratogeomysmerriami (Thomas, 1893) Paraspidoderauncinata Travassos, 1914 Lamothe-Argumedo et al. 1997
Vexillataconvoluta Caballero & Cerecero, 1943 Caballero and Cerecero 1943
Cratogeomysplaniceps (Merriam, 1895) Hymenolepiscratogeomyos Gardner et al., 2020 Gardner et al. 2020
Geomysattwateri Merriam, 1895 Monoecocestuscentroovarium Dronen et al., 1994 Dronen et al. 1994
Protospiruraascaroidea Hall, 1916 LeBrasseur 2017
Vexillatageomyos Falcón-Ordaz et al., 2006 Falcón-Ordaz et al. 2006
Geomysbreviceps Baird, 1855 Eimeriageomydis Skidmore, 1929 Upton et al. 1992
Litomosoideswesti Gardner & Schmidt, 1986 Pitts et al. 2000
Monoecocestusanoplocephaloides (Douthitt, 1915) Douthitt 1915
Protospiruraascaroidea Hall, 1916 Hall 1916; English 1932
Geomysbursarius (Shaw, 1800) Andryamacrocephala Douthitt, 1915 Douthitt 1915; Hansen 1950; Ubelaker and Downhower 1965; Bartel and Gardner 2000
Anoplocephaloidesinfrequens (Douthitt, 1915) Douthitt 1915; Ubelaker and Downhower 1965; Bartel and Gardner 2000; Rausch 1976
Anoplocephaloidesvariabilis (Douthitt, 1915) Douthitt 1915; Rausch 1976
Calodiumamericanum (Read, 1949) Bartel and Gardner 2000
Calodiumhepaticum (Bancroft, 1893) Ubelaker and Downhower 1965
Cittotaeniaperplexa Stiles, 1897 Burnham 1953
Eimeriageomydis Skidmore, 1929 Skidmore 1929; Levine and Ivens 1965
Hymenolepisdiminuta (Rudolphi, 1819) Burnham 1953
Hymenolepisgeomydis Gardner & Schmidt, 1988 Gardner and Schmidt 1988
Hymenolepisweldensis Gardner & Schmidt, 1988 Gardner and Schmidt 1988; Bartel and Gardner 2000; Haukisalmi et al. 2010
Litomosafilaria (Beneden, 1873) Burnham 1953
Litomosoideswesti Gardner & Schmidt, 1986 Gardner and Schmidt 1986
Moniliformisclarki (Ward, 1917) Bartel and Gardner 2000
Monocercomonoides Travis, 1932 Rissky 1962
Monoecocestusanoplocephaloides (Douthitt, 1915) Burnham 1953
Oochoristica Lűhe, 1898 Douthitt 1915
Ostertagia Ransom, 1907 Burnham 1953
Paranoplocephalainfrequens (Douthitt, 1915) Ubelaker and Downhower 1965
Physalopteralimbata Leidy, 1856 Bartel and Gardner 2000
Protospiruraascaroidea Hall, 1916 English 1932; LeBrasseur 2017
Protospiruramurisascaroides (Hall, 1916) Burnham 1953
Pseudocittotaeniapraecoquis (Stiles, 1985) Stiles 1895
Ransomusrodentorum Hall, 1916 Bartel and Gardner 2000
Geomysjugossicularis Hooper, 1940 Anoplocephaloidesvariabilis (Douthitt, 1915) Present study
Geomyslutescens Merriam, 1890 Hymenolepisweldensis Gardner & Schmidt, 1988 Gardner et al. 2020
Litomosoideswesti Gardner & Schmidt, 1986 Present study
Physalopteralimbata Leidy, 1856 Present study
Ransomusrodentorum Hall, 1916 Present study
Monoecocestusanoplocephaloides (Douthitt, 1915) Burnham 1953
Geomyspersonatus True, 1889 Litomosoideswesti Gardner & Schmidt, 1986 Pitts et al. 2000
Protospiruraascaroidea Hall, 1916 LeBrasseur 2017
Geomyspinetis Rafinesque, 1817 Mastophorusmurisascaroides (Gmelin, 1790) Hubbell and Goff 1939
Geomystexensis Merriam, 1895 Eimeriageomydis Skidmore, 1929 Upton et al. 1992
Hymenolepis Weinland, 1858 LeBrasseur 2017
Protospiruraascaroidea Hall, 1916 LeBrasseur 2017
Heterogeomysheterodus (Peter, 1865) Hobergiairazuensis Gardner et al., 2020 Gardner et al. 2020
Orthogeomysgrandis (Thomas, 1893) Eimeriaorthogeomys Lainson, 1968 Lainson 1968
Thomomysbottae (Eydoux & Gervais, 1836) Arostrilepishorrida (von Linstow, 1901) Schiller 1952; Voge 1955; Gardner 1985
Catenotaeniadendritica (Goeze, 1782) Voge 1955
Catenotaenialinsdalei McIntosh, 1941 McIntosh 1941
Eimeriathomomysis Levine et al., 1957 Levine et al. 1957; Levine and Ivens 1965
Heligmosomoidesthomomyos Gardner & Jasmer, 1983 Gardner and Jasmer 1983
Hymenolepiscitelli (McLeod, 1933) Voge 1955; Jasmer 1980
Litomosoidesthomomydis Gardner, 1986 Gardner and Schmidt 1986
Monocercomonoides Travis, 1932 Gardner and Jasmer 1983
Monoecocestusanoplocephaloides (Douthitt, 1915) Hansen 1950
Ransomusrodentorum Hall, 1916 Jasmer 1980
Trichurisfossor Hall, 1916 Jasmer 1980; Douglas 1969
Thomomysbulbivorus (Richardson, 1829) Arostrilepishorrida (von Linstow, 1901) Gardner 1985
Arostrilepisschilleri Makarikov et al., 2012 Makarikov et al. 2012
Heligmosomoidesthomomyos Gardner & Jasmer, 1983 Gardner 1985; Gardner and Jasmer 1983
Hymenolepistualatinensis Gardner, 1985 Gardner 1985
Ransomusrodentorum Hall, 1916 Gardner 1985
Trichurisfossor Hall, 1916 Gardner 1985
Thomomysclusius Coues, 1875 Ransomusrodentorum Hall, 1916 Present study
Trichurisfossor Hall, 1916 Present study
Thomomysmonticola J. A. Allen, 1893 Arostrilepishorrida (von Linstow, 1901) Howard and Childs 1959
Trichuris Roederer, 1761 Ingles 1952
Thomomystalpoides (Richardson, 1828) Andryamacrocephala Douthitt, 1915 Rausch and Schiller 1949
Anoplocephaloidesinfrequens (Douthitt, 1915) Frandsen and Grundmann 1961; Todd et al. 1971
Anoplocephaloidesvariabilis (Douthitt, 1915) Rausch 1976; Frandsen and Grundmann 1961; Todd et al. 1971; Lubinsky 1957
Arostrilepishorrida (von Linstow, 1901) Grundmann, et al. 1976; Frandsen and Grundmann 1961
Ascarislaevis Leidy, 1856 Grundmann et al. 1976; Frandsen and Grundmann 1961
Calodiumhepaticum (Bancroft, 1893) Ubelaker and Downhower 1965; Lubinsky 1957; Dikmans 1932; Tryon 1947; Lubinsky 1956; Rausch 1961; Tryon and Cunningham 1968
Catenotaenialinsdalei McIntosh, 1941 Todd et al. 1971
Eimeriafitzgeraldi Todd & Tryon, 1970 Todd et al. 1971; Todd and Tryon 1970
Eimeriajemezi Wilber et al., 1994 Wilber et al. 1994
Eimeriathomomysis Levine et al., 1957 Levine and Ivens 1965; Levine et al. 1957
Hymenandryathomomyis Smith, 1954 Smith 1954
Hymenolepiscitelli (McLeod, 1933) Frandsen and Grundmann 1961
Hymenolepisdiminuta (Rudolphi, 1819) Rankin 1945
Litomosoidescarinii (Travassos, 1919) Lubinsky 1957
Litomosoidesthomomydis Gardner, 1986 Gardner and Schmidt 1986
Nippostrongylusmuris (Yokogawa, 1920) Frandsen and Grundmann 1961
Protospiruraascaroidea Hall, 1916 Todd et al. 1971
Pseudocittotaeniaglandularis Beveridge, 1978 Beveridge 1978
Pseudocittotaeniapraecoquis (Stiles, 1985) Grundmann et al. 1976; Frandsen and Grundmann 1961; Smith 1951
Ransomusrodentorum Hall, 1916 Grundmann et al. 1976; Frandsen and Grundmann 1961
Trichurisfossor Hall, 1916 Hall 1916; Grundmann et al. 1976; Frandsen and Grundmann 1961; Lubinsky 1957; Todd and Lepp 1972
Versteriamustelae (Gmelin, 1790) Lubinsky 1957
Vexillatavexillata (Hall, 1916) Todd et al. 1971
Thomomysumbrinus (Richardson, 1829) Arostrilepishorrida (von Linstow, 1901) Frandsen and Grundmann 1961
Ascarislaevis Leidy, 1856 Frandsen and Grundmann 1961
Hymenolepiscitelli (McLeod, 1933) Frandsen and Grundmann 1961
Moniliformisclarki (Ward, 1917) Frandsen and Grundmann 1961
Paruterinacandelabraria (Goeze, 1782) Frandsen and Grundmann 1961
Ransomusrodentorum Hall, 1916 Frandsen and Grundmann 1961
Trichurisfossor Hall, 1916 Frandsen and Grundmann 1961
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Leidy in (1857), at a meeting of the Academy of Natural Sciences of Philadelphia, displayed some warbles taken from an evidently incapacitated pocket gopher by the side of the road, identified as T.borealis [probably a synonym of T.talpoides] near the Bridger’s pass summit of the Rocky Mountains. This record represents the first known report of an endoparasite from a member of the rodent family Geomyidae. Soon after the groundbreaking work by Leidy, Charles Wardell Stiles (1895) reported the first helminth parasite from a geomyid when he described Pseudocittotaeniapraecoquis (Stiles, 1895) from Geomysbursarius (Shaw, 1800) collected near Ames, Iowa (Stiles, 1897).

Hall (1912) reported on the parasite fauna of Colorado and recorded several nematodes and some unidentified cestodes from Thomomysfossor J.A. Allen (probably a syn. of T.talpoides). Soon after, Herman Douthitt (1915) described four new species of anoplocephalid cestodes from pocket gophers collected from the central United States. Anoplocephaloidesvariabilis (Douthitt, 1915), A.infrequens (Douthitt, 1915), and Andryamacrocephala Douthitt, 1915 were all described from specimens taken from G.bursarius collected from Illinois, Minnesota, and North Dakota. Monoecocestusanoplocephaloides (Douthitt, 1915) was described from some specimens taken from Geomysbreviceps Baird collected near Norman, Oklahoma. Douthitt (1915) also reported one unidentified species of Oöchoristica Luhe, 1898, and one immature form of Cittotaenia, now known as Pseudocittotaenia, Tenora, 1976 from G.bursarius. Douthitt (1915) also reported numerous individuals of eight different species of Hymenolepis from two species of pocket gophers including: G.bursarius collected in Illinois, Wisconsin, Minnesota, North Dakota, and Manitoba, Canada; G.breviceps collected in Oklahoma and Texas; and Geomyspersonatus True, collected in Texas.

Hall (1916) described the following nematodes from Thomomysfossor J. A. Allen [syn. T.talpoides (Richardson, 1828)]: Trichurisfossor Hall, 1916, from specimens collected near both Crested Butte and Livermore, Colorado and Vexillatavexillata (Hall, 1916) from gophers collected from mountain meadows near Livermore, Colorado. These nematodes were described from the same material that Hall (1912) had previously studied. Additionally, the nematode Protospiruraascaroidea Hall, 1916 was described from specimens recovered from the stomachs of Geomysbursarius collected near Norman, Oklahoma by Herman Douthitt and sent to MC Hall for study.

Skidmore (1929) described a species of Coccidia named Eimeriageomydis Skidmore, 1929 from the intestinal tract of Geomysbursarius Shaw, collected near Lincoln, Nebraska while Dikmans (1932) reported Capillaria (syn. Calodium) hepaticum (Bancroft, 1893) as a parasite of Thomomysfossor (syn. T.talpoides) collected in the Medicine Bow Mountains of Wyoming. In that same year, English (1932) examined 161 specimens of Geomysbursarius collected in Brazos County, Texas and found 23 infected with the stomach nematode Protospiruraascaroidea Hall, 1916, and eight infected with an unknown species of Hymenolepis.

Hubbell and Goff (1939) reported Mastophorusmurisascaroides (Gmelin, 1790) to occur commonly in the stomach of Geomys sp. (most likely G.pinetis) collected near Leesburg, Lake County, Florida.

McIntosh (1941) described Catenotaenialinsdalei McIntosh, 1941 from Thomomysbottaebottae (Eydoux & Gervais, 1836) collected near Monterey, California on the Hastings Natural History Reservation.

Caballero and Cerecero (1943) described Vexillataconvoluta from the small intestine of the Merriam’s pocket gopher, Cratogeomysmerriami (Thomas, 1893), collected from the state of Michoacan, Mexico.

Chandler (1945) redescribed Trichurisfossor Hall, 1916 from Thomomysbottaebottae from specimens collected on the Hastings Natural History Reservation near Monterey, California. This was the first good description of the eggs of T.fossor, and the first report of T.fossor from T.bottae. In the same year during an ecological study of the small mammals collected from Northrup Canyon in eastern Washington State, Rankin (1945) recorded Hymenolepisdiminuta (Rudolphi, 1819) from Thomomystalpoides, see discussion below. The next year, Wenrich (1946) recorded a species of Monocercomonoides Travis, 1932 as a cecal commensal (flagellate) of Botta’s pocket gopher, Thomomysbottae.

Tryon (1947) reported both cestodes and nematodes in Thomomystalpoides from Montana, with most of his field work occurring in the Bridger Mountains. Less than one percent of the gophers necropsied contained an unidentified species of cestode. Nematodes identified as belonging to the family Trichuridae were found in 100% of the pocket gophers examined for endoparasites. In areas of low pocket gopher density, the prevalence of infection was low (approximately 10%); however, in areas of high gopher density, the prevalence of infection approached 80%. Tryon (1947) speculated that the young gophers became infected before leaving the parental burrows, and by August, the prevalence of infection for the young pocket gophers was ca. 50%. Nematodes, probably of the genus Protospirura were found in the stomachs of some gophers, with as many as 42 in an individual pocket gopher’s stomach. Concerning the presence of warbles in the pocket gophers examined during the study, Tryon stated “only 15 out of over a thousand animals examined showed warbles. Of these, ten were juveniles indicating that they may be above ground more than the adults, probably during migration from the parental burrows.”

Rausch and Schiller (1949), during a study of cestodes of the genus Andrya Railliet, 1893, mentioned Andryamacrocephala Douthitt, 1915 as occurring in Thomomystalpoidestenellus Goldman from the Jackson Hole Wildlife Park in Wyoming.

Hansen (1950), during a study of the tapeworms of rodents, recorded Andryamacrocephala Douthitt, 1915 as occurring in 5 of 5 Geomysbursarius examined with up to 12 cestodes per host. Hansen (1950) also recorded Monoecocestusanoplocephaloides (Douthitt, 1915) from Thomomysbottae collected in the region of Sacramento, California. Interestingly, this cestode has not since been reported from any members of the genus Thomomys.

Smith (1951), in a study of the cestodes of Thomomystalpoides collected from Carbon County, Wyoming, reported the following cestodes: Pseudocittotaeniapraecoquis (Stiles, 1895) from the small intestine; P.megasacca (Smith, 1951) also from the small intestine (see below for clarification of the taxonomy of these two species). Smith (1951) also included a list of the cestodes reported from pocket gophers up to that time and attempted to clarify the taxonomic relationships between Schizotaenia Janicki, 1904 and Monoecocestus Beddard, 1914.

Ingles (1952) reported Trichuris sp. (probably T.fossor) as a common parasite of the cecum of Thomomysmonticola J. A. Allen, 1893. All specimens that Ingles examined came from an elevation of ca. 7,000 feet in the Sierra Nevada of California. In the same year, Everett Schiller (1952), in a study of the morphological variation in Hymenolepis (syn. Arostrilepis) horrida (von Linstow, 1901) reported Thomomysbottae from near O’Neals California as a host.

Burnham (1953), during a study of the parasites of Geomysbursarius, collected from four counties in Oklahoma reported the following species of parasites: Protospiruramurisascaroides (Hall, 1916) (syn. Mastophorusmuris) from the stomachs of 18 hosts; Litomosafilaria Beneden, 1897 from the pleural cavities of 19 gophers (this is probably a misidentification, see discussion below regarding the filarioid nematodes of pocket gophers); Ostertagia sp. from the stomachs of five gophers; Hymenolepisdiminuta (Rudolphi, 1819) from the small intestines of ten hosts (see discussion below for clarification of the problem concerning H.diminuta in geomyids); Monoecocestusanoplocephaloides (Douthitt, 1915) from 25 hosts, with a range of infection of 1–100 worms per host; and Cittotaeniaperplexa Stiles, 1897 from two gophers.

Soon after, Smith (1954) described Hymenandryathomomyis from the small intestine of Thomomystalpoides collected in Colorado and in this same publication, he recommended that Catenotaenialinsdalei McIntosh, 1941 be considered a synonym of C.dendritica (Goeze, 1782) Janicki 1904.

Voge (1955) in a catalogue of the cestode parasites of California mammals, listed Catenotaeniadendritica (Goeze, 1782), Hymenolepiscitelli (McLeod, 1933), and an unidentified species of Hymenolepis from T.bottae.

The next year, Voge (1956), in a list of the nematode parasites of California mammals, reported Trichurisfossor Hall, 1916 as a parasite of T.bottae and in the same year, Lubinsky (1956) reported Calodium (syn. Capillaria) hepaticum from T.talpoides in Alberta, Canada. Soon after, continuing his work on small mammals, Lubinsky (1957) in a list of the helminth parasites of rodents from Alberta included the following as parasites of Thomomystalpoides: Versteria (syn. Taenia) mustelae (larvae) from the mesenteries, lungs, liver, and kidneys of gophers collected in northern and middle Alberta: Anoplocephaloidesvariabilis (Douthitt, 1915) recovered from the colon (which is a doubtful location for a cestode) from six localities in middle and southern Alberta; Calodium (syn. Capillaria) hepaticum from the livers of gophers collected from central and southern Alberta; Trichurisfossor from the cecum of gophers collected from central Alberta; Protospiruraascaroidea Hall, 1916 from the stomachs of gophers from middle Alberta; Litomosoidescarinii (Travassos, 1919) from the coelom of pocket gophers from middle and southern Alberta. In the same year, Levine, et al. (1957) described Eimeriathomomysis from specimens of T.bottae collected in the Grand Canyon of Arizona.

Howard and Childs (1959) during a study of the ecology of Thomomysmonticola reported Hymenolepishorrida (von Linstow, 1901) to occur commonly in adult pocket gophers. They stated, “Most of the adults had several tapeworms (Hymenolepishorrida), and one animal had 108 immature tapeworms with short strobila. None of the five juvenile gophers examined had tapeworms.” Based on recent work by Dursahinhan et al. (2022), it appears now that the species identified as H.horrida may be referred to the genus Arostrilepis.

Frandsen and Grundmann (1960) discussed the geographic distribution of Trichurisfossor Hall, 1916 and Ransomusrodentorum Hall, 1916 from Thomomystalpoides and T.umbrinus in the Lake Bonneville basin of Utah. They speculated that the distribution of these two species of nematodes in Thomomys sp. in this area supports the contention that competition occurred between the two species of pocket gophers resulting in the present-day distribution patterns of the pocket gophers and their respective helminths.

Rausch (1961) reported Calodium (syn. Capillaria) hepaticum from Thomomystalpoidestenellus Goldman from near Moran, Wyoming, collected in June of 1948 and Frandsen and Grundmann (1961) reported the following helminth parasite species from several subspecies of both Northern pocket gopher, Thomomystalpoides, and the Southern pocket gopher Thomomysumbrinus (Richardson, 1829). These species include Ascarislaevis Leidy, 1856, Hymenolepiscitelli, Ransomusrodentorum, and Trichurisfossor. However, Anoplocephaloidesinfrequens (Douthitt, 1915), A.variabilis (Douthitt, 1915), Pseudocittotaeniapraecoquis (Stiles, 1985), Arostrilepishorrida, and Nippostrongylusmuris (Yokogawa, 1920) have been reported from T.talpoides. In addition, Paruterinacandelabraria (Goeze, 1781) and Moniliformisclarki are only reported from T.umbrinus.

Stock (1962) reported three males and one female of the nematode Ransomusrodentorum from the cecae of two specimens of Thomomystalpoidesfossor, collected at the junction of Dry Gulch and the Gunnison River, Colorado, at ca. 7,400 feet altitude.

Rissky (1962) reported Monocercomonoides from the cecum of the Plains pocket gopher, Geomysbursarius, collected from Clay County, South Dakota.

Ubelaker and Downhower (1965) in a study of the endo and ectoparasites of Geomysbursarius in Kansas, reported Calodium (syn. Capillaria) hepaticum from the cecum of a single pocket gopher and Andryamacrocephala Douthitt, 1915 and Anoplocephaloidesinfrequens (Douthitt, 1915) were found to occur in seven and six of the pocket gophers examined, respectively.

Lainson (1968), during a parasitological study in El Cayo District British Honduras, a new species of coccidian parasite (Eimeriaorthogeomyos) was described from the Giant pocket gopher, Orthogeomysgrandis (Thomas, 1893) collected from Baking Pot, El Cayo District, Central America (Lainson, 1968).

Tryon and Cunningham (1968) in a study of Thomomystalpoides along an altitudinal transect in the Beartooth Mountains of Wyoming reported Calodium (syn. Capillaria) hepaticum from the livers of 5%, 37%, and 8% of the gophers from the Alpine, the Canadian, and the transition life zones, respectively.

Douglas (1969) studied the ecology of the pocket gophers of Mesa Verde, Colorado. He reported Trichurisfossor Hall, 1916 and Cuterebracf.cyanella (bot fly larvae) from ThomomysbottaeaureusDouglas (1969) stated that, “Of the gophers infected with bot fly larvae, the highest prevalence of infection occurred during September, with no gophers carrying larvae during the spring.” Douglas (1969) also stated “Specimens of Cestoda currently are being studied and will be reported elsewhere.” To our knowledge, no report has ever been published.

Todd and Tryon (1970) described Eimeriafitzgeraldi Todd & Tryon, 1970 from Thomomystalpoides collected from the Beartooth Mountains, Park County Wyoming. Oocysts were recovered from the feces of two of ten juvenile males and one of 31 adult females (pocket gophers).

Todd et al. (1971) in a study of the endoparasites of the Northern pocket gopher (Thomomystalpoides) from Park County, Wyoming, reported the following species of parasites from a total of 46 specimens of T.talpoides examined: Eimeriathomomysis Levine, Ivens & Kruidenier, 1957 was found to occur in the fecal pellets of 24 of the individual gophers; E.fitzgeraldi Todd & Tryon, 1970 was found in the feces of two gophers; cestode cysticerci of the family Taeniidae were found in the mesenteries near the stomach and cecum of one gopher; fragments of the cestode Catenotaenialinsdalei McIntosh, 1941 were found in the body cavities of two animals (this is a dubious body location record); Anoplocephaloidesvariabilis (Douthitt, 1915) was present in the small intestines of 18 gophers; A.infrequens (Douthitt, 1915) was recovered from the small intestine of seven gophers; Anoplocephaloides sp. was recovered from the small intestines of 22 gophers R.rodentorum was found in the cecum of 34 gophers, and in the large intestine of one; Vexillatavexillata was recovered from the small intestines of two gophers; Protospiruraascaroidea was found in the stomachs of two animals; Trichurisfossor was found in the ceca of 30 gophers; and Calodium (syn. Capillaria) hepaticum was recovered from the livers of 18 of the gophers examined.

Todd and Lepp (1972) redescribed Trichurisfossor from specimens recovered from T.talpoides from Park County, Wyoming.

Grundmann et al. (1976), in a paper discussing the mechanisms of parasitic helminth population regulation in rodents, listed the following parasites as occurring in Thomomystalpoides in Utah: Trichurisfossor, Vexillatavexillata, Ascarislaevis Leidy, 1856. Hymenolepishorrida, and T.fossor were reported from T.bottae in the same paper.

Rausch (1976) in a study of the rodent cestode genera Paranoplocephala Luhe, 1910 and Anoplocephaloides Baer, 1923 examined the type material of Anoplocephaloidesinfrequens (Douthitt, 1915) from Geomysbursarius collected by Douthitt in Brainerd, Minnesota, and specimens of A.variabilis (Douthitt, 1915) collected by Douthitt in central Illinois from Geomysbursarius. Also studied by Rausch (1976) were seven specimens of A.variabilis from Thomomystalpoides collected at Emerson, Manitoba, 10 km north of Prince Albert, Saskatchewan, Canada and from 5 km south of Saskatoon, Saskatchewan, Canada. Rausch (1976) stated “I also obtained it (A.variabilis from T.talpoides) in two of 11 of these rodents at Moran, Wyoming, in 1949.”

Beveridge (1978) in a revision of the genus Pseudocittotaenia Tenora, 1976, listed the synonyms of P.praecoquis (Stiles, 1895) and described P.glandularis Beveridge, 1978 from some specimens taken from Thomomystalpoides in Utah by Frandsen and Grundmann (1961), and from some specimens from T.talpoides in Wyoming. Frandsen and Grundmann (1961) evidently misidentified P.glandularis Beveridge, 1978 and had determined that the specimens that they found in T.talpoides were Pseudocittotaeniapraecoquis (Stiles, 1895). The specimens from the Wyoming pocket gophers were from material that Smith (1951) had mistakenly identified and redescribed as P.praecoquis. Beveridge (1978) also listed as synonyms: P.megasacca (Smith, 1951) with P.praecoquis (Stiles, 1895). Also reported by Beveridge (1978) and not reported elsewhere in the literature was Pseudocittotaeniapraecoquis from T.talpoidestenellus Goldman, collected by Robert L. Rausch near Moran, Wyoming in June of 1948.

Jasmer (1980) in a thesis written at Humboldt State University listed the following parasites from Thomomysbottae (Eydoux & Gervais): Ransomusrodentorum, Trichurisfossor, Hymenolepiscitelli, and an unidentified species of Heligmosomoides Hall, 1916. He also discussed the biological characteristics and taxonomy of R.rodentorum (some of his specimens are now in the Manter Laboratory Parasite Collection).

Gardner and Jasmer (1983) described Heligmosomoidesthomomyos Gardner & Jasmer, 1983 from Thomomysbottae (Eydoux & Gervais) and T.bulbivorus (Richardson) from Humboldt County, California and Benton County, Oregon, respectively. They included some measurements and remeasurements of two other species of Heligmosomoides: H.longispiculatus (Dickmans, 1940) and H.montanus Durette-Desset, 1968.

Gardner (1985) described Hymenolepistualatinensis from the duodenum of the Camas pocket gopher, Thomomysbulbivorus (Richardson, 1829) collected near the Tualatin River in the Willamette Valley of Oregon. In the report, several helminth species were documented during the study including Arostrilepishorrida also from the small intestine, Trichurisfossor from the cecum, Ransomusrodentorum from the cecum, and Heligmosomoidesthomomyos from the duodenum.

Gardner and Schmidt (1986) described Litomosoidesthomomydis from the abdominal cavity of the Northern pocket gopher, Thomomystalpoides, and Botta’s pocket gopher, Thomomysbottae, from Huerfano County, Colorado. Also, L.westi was described from the abdominal and pleural cavities of the Plains Pocket Gopher, Geomysbursarius, collected from Weld County, Colorado.

Shortly after this work, Gardner and Schmidt (1988) described two new species in the genus Hymenolepis Weinland, 1858, including H.weldensis and H.geomydis from the small intestines (duodenum) of the Plains pocket gopher, Geomysbursarius, collected from Weld County, Colorado.

Pitts et al. (1990) reported Litomosoideswesti Gardner & Schmidt, 1986 from Geomyspersonatus True, 1889 collected from Duval and Zapata counties in Texas.

Upton et al. (1992) reported Eimeriageomydis Skidmore, 1929 from Baird’s pocket gopher, Geomysmericanu, and Llano pocket gopher, Geomystexensis Merriam, 1895 collected from Texas.

Dronen et al. (1994) described Monoecocestuscentroovarium found in Attwater’s pocket gopher, Geomysattwateri Merriam, 1895 collected from Atascosa County, Texas. In the same year, Wilber et al. (1994) described Eimeriajemezi found in the Northern pocket gopher, Thomomystalpoides collected from El Cajete crater, Jemez Springs, Sandoval County, New Mexico.

Lamothe-Argumedo et al. (1997) reported Paraspidoderamerican Travassos, 1914 from the intestine of Merriam’s pocket gopher, Cratogeomysmerriami (Thomas, 1893) first collected from Morelos, Cuernavaca, Mexico in 1984.

Pitts et al. (2000) reported the additional occurrence of the filarioid nematode, Litomosoideswesti from the pleural cavities of Baird’s pocket gopher, Geomysmericanu collected at the entrance of Isle, Du Boris unit, Lake Ray Roberts State Park, Denton County, Texas while L.westi was also documented from the pleural cavities of the Plains pocket gopher, Geomysbursarius captured near Aubrey, Grubbs Road, same county.

Bartel and Gardner (2000) reported the helminth parasites from the Plains pocket gopher, Geomysbursarius, from seven localities in the northern boundary range, Minnesota. The report includes the following: Physalopteralimbata Leidy, 1856 from the stomach, Ransomusrodentorum from the cecum and large intestine and Calodium (syn. Capillaria) mericanum (Read, 1949), Anoplocephaloidesinfrequens, A.variabilis (Douthitt, 1915), Andryamacrocephala, Hymenolepisweldensis Gardner & Schmidt, 1988 and Moniliformisclarki from the small intestines.

Falcón-Ordaz et al. (2006) described Vexillatageomyos from Attwater’s pocket gopher, Geomysattwateri from the Welder Wildlife Refuge of San Patricio County, Texas.

Using molecular methods, Haukisalmi et al. (2010) documented Hymenolepisweldensis from Geomysbursarius collected from Illinois and Indiana.

Makarikov et al. (2012) described Arostrilepisschilleri obtained from the Camas pocket gopher, Thomomysbulbivorus, captured southeast of Corvallis, Oregon and originally reported as H.horrida by Gardner (1985).

LeBrasseur (2017) in an unpublished master’s thesis reported a study focused on the endoparasites of four species of pocket gophers in the genus Geomys collected from eight counties in Texas. These host species included the Plains pocket gopher, Geomysbursarius, Attwater’s pocket gopher, G.attwateri Merriam, 1895, Texas pocket gopher, G.personatus True, 1889, and the Central Texas pocket gopher G.texensis Merriam, 1895. In addition, she found an unidentified Hymenolepis Weinland, 1858 obtained from G.attwateri, G.bursarius, and G.texensis and another tapeworm, Monoecocestus was obtained from G.bursarius¸ and G.texensis. Finally, a nematode species, Protospiruraascaroidea, was found from all four species of Geomys mentioned above; the specimens were verified by HWML personnel (LeBrasseur 2017).

Gardner et al. (2020) described two new species of unarmed hymenolepidid tapeworms, including Hobergiairazuensis from the small intestine of Heterogeomysheterodus (Peters, 1865), collected from Potrero Cerrado, Cartago, Costa Rica, and Hymenolepiscratogeomyos from the small intestine of the Volcán De Toluca pocket gopher, Cratogeomysplaniceps (Merriam, 1895) collected from Parque Nacional Nevado de Toluca, México. Also, H.weldensis Gardner & Schmidt, 1988 has been documented from many individuals of Geomyslutescens Merriam, 1890 collected in the Sandhills, on the north side of the North Platte River near Cedar Point Biological Station in western Nebraska.

The present study reports an unidentified Monoecocestus sp. Beddard, 1914 (probably M.anoplocephaloides) from the small intestine of the Yellow-faced pocket gopher, Cratogeomyscastanops (Baird, 1852), collected by a local landowner from Black Mesa, Oklahoma in 2016 (NP2779). Anoplocephaloidesvariabilis (Douthitt, 1915) was found from the small intestine of Hall’s pocket gopher, Geomysjugossicularis Hooper, 1940 collected from Grama grass habitat, Keith County, Nebraska in 2016 (NP2661). Also, from 2009–2016, necropsies of Geomyslutescens Merriam, 1890 yielded many individuals of Litomosoideswesti Gardner & Schmidt, 1986 from their abdominal cavities with individuals of Ransomusrodentorum from the cecum, and from two pocket gophers Physalopteralimbata Leidy, 1856 was found (NP2297, NP2298). Also, during general collecting in the area of Nebraska, we found two nematode species (R.rodentorum, and T.fossor – refer to NP1524) from the cecum of the Wyoming pocket gopher, Thomomysclusius Coues, 1875, collected from 5 miles east of Woods Landing, Albany County, Wyoming in 2013. All specimens mentioned in this work are deposited in the HW Manter Laboratory of Parasitology Museum collection where NP refers to the field collection number.

Endoparasites of Neotropical subterranean rodents

See graphical summary in Fig. 4 and endoparasite list Table 5.

Figure 4.

Figure 4.

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Percentage taxon composition of endoparasite diversity pie diagram shown by higher classification of bothprotozoa and helminths occurring in subterranean rodents (Family Ctenomyidae) in the southern Neotropical region. All records of parasites presented were derived from a review of the literature published from 1931 through 2021. Approximately 67% of the total endoparasite fauna of these rodents consists of Nemata, followed by Protozoa (19%), and Cestoda (14%).

Table 5.

Endoparasite species diversity from Neotropical subterranean rodents (Ctenomyidae and Octodontidae). Authorities are given for parasite and host species.

Host species Parasite species References
Ctenomysandersoni Gardner, et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomysaustralis Rusconi, 1934 Pudicactenomydis Rossin et al., 2006 Rossin et al. 2010a
Taeniatalicei Dollfus, 1960 Rossin et al. 2010b
Trichurispampeana Suriano & Navone, 1994 Rossin et al. 2010a
Ctenomysazarae Thomas, 1903 Trichurispampeana Suriano & Navone, 1994 Suriano and Navone 1994; Rossin and Malizia 2005a
Ctenomysboliviensis Waterhouse, 1848 Ancylostomactenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Paraspidodera Travassos, 1914 Gardner et al. 2021
Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Ctenomysconoveri Osgood, 1946 Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomyserikacuellarae Gardner et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomysandersoni Gardner, et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomysaustralis Rusconi, 1934 Pudicactenomydis Rossin et al., 2006 Rossin et al. 2010a
Taeniatalicei Dollfus, 1960 Rossin et al. 2010b
Trichurispampeana Suriano & Navone, 1994 Rossin et al. 2010a
Ctenomysazarae Thomas, 1903 Trichurispampeana Suriano & Navone, 1994 Suriano and Navone 1994; Rossin and Malizia 2005a
Ctenomysboliviensis Waterhouse, 1848 Ancylostomactenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Paraspidodera Travassos, 1914 Gardner et al. 2021
Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Ctenomysconoveri Osgood, 1946 Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomyserikacuellarae Gardner et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Raillietina Fuhrman, 1920 Gardner et al. 2021
Ctenomysfrater Thomas, 1902 Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomysfulvus Philippi, 1860 Trichurisfulvi Babero & Murua, 1987 Babero and Murua 1987
Trichurisrobusti Babero & Murua, 1990 Babero and Murua 1990
Ctenomyslewisi Thomas, 1926 Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomysleucodon Waterhouse, 1848 Pudicapujoli Durette-Casset & Tcheprakoff, 1990 Gardner et al. 2021
Ctenomysmagellanicus Bennett, 1836 Paraspidoderaamericana Khalil & Vogelsang, 1931 Khalil and Vogelsang 1931
Ctenomysmaulinus Philippi, 1872 Monoecocestustorresi Olsen, 1976 Olsen 1976
Paraspidoderauncinata Rudolphi, 1819 Torres et al. 1976
Trichuris Roederer, 1761 Torres et al. 1976
Ctenomysnattereri Wagner, 1848 Paraspidodera Travassos, 1914 Gardner et al. 2021
Trichuris Roederer, 1761 Gardner et al. 2021
Ctenomysopimus Wagner, 1848 Eimeriagranifera Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeriamontuosi Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeriaopimi Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeriaoruroensis Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Litomosoidesandersoni Brant & Gardner, 1997 Brant and Gardner 1997
Litomosoidesctenomyos Brant & Gardner, 1997 Brant and Gardner 1997
Mathevotaenia Akhumyan, 1946 Gardner et al. 2021, 2023
Ctenomyspearsoni Lessa & Langguth, 1983 Strongyloidesmyopotami Artigas & Pacheco, 1933 Rossin et al. 2009
Ctenomyssteinbachi Thomas, 1907 Ancylostomactenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Eimeriaopimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomystalarum Thomas, 1898 Graphidiodessubterraneus Rossin et al., 2005 Rossin et al. 2005b; Rossin et al. 2010b
Heligmostrongylus Travassos, 1917 Rossin and Malizia 2002
Paraspidoderauncinata Rudolphi, 1819 Rossin et al. 2004b; Rossin et al. 2010b
Pudicactenomydis Rossin et al., 2006 Rossin et al. 2006a; Rossin et al. 2010b
Strongyloidesmyopotami Artigas & Pacheco, 1933 Rossin et al. 2010b; Rossin et al. 2009
Ctenomystalarum Thomas, 1898 Hydatigera (syn. Taenia) taeniaeformis Batsch, 1786 Rossin et al. 2004a
Taeniatalicei Dollfus, 1960 Rossin et al. 2010a; Rossin et al. 2010b
Trichostrongylusduretteae Rossin et al., 2006 Rossin et al. 2006b; Rossin et al. 2010a
Trichuris Roederer, 1761 Rossin and Malizia 2002; Rossin and Malizia 2005a
Trichurisbursacaudata Suriano & Navone, 1994 Suriano and Navone 1994
Trichurispampeana Suriano & Navone, 1994 Rossin et al. 2010a; Rossin and Malizia 2005a
Ctenomystorquatus Lichtenstein, 1830 Taeniatalicei Dollfus, 1960 Dollfus 1960
Spalacopuscyanus (Molina, 1782) Graphidioides yañezi Babero & Cattan, 1980 Babero and Cattan 1980
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Khalil and Vogelsang (1931) described the first helminth parasite from a subterranean host from Neotropical region, Paraspidoderaamericana Khalil & Vogelsang, 1931 from the cecum of a single individual of what they called Ctenomysmagellanicus Bennett, 1836 collected from Carrasco near Montevideo, Uruguay in 1927. The identification of this mammal specimen was probably erroneous as C.magellanicus occurs only near the Strait of Magellan in southern Argentina). Unfortunately, no hosts or parasite specimens were deposited in any collection that we can find up to the current time.

Dollfus (1960) described Taeniatalicei Dollfus, 1960 from the abdominal cavity of the Collared tuco-tuco, Ctenomystorquatus Lichtenstein, 1830, collected from Uruguay and in 1986, multistrobilate larvae of T.talicei were collected from several Ctenomysopimus at 7 km S: 4 km E. Cruce Ventilla, Oruro, Bolivia by a party from the American Museum of Natural History and the Museum of Southwestern Biology (Anderson 1997).

Olsen (1976) described Monoecocestustorresi obtained from the small intestine of Maule’s tuco-tuco, Ctenomysmaulinus Philippi, 1872 collected near Lonquimay, Chile. Meanwhile, Torres et al. (1976) reported Paraspidoderauncinata Rudolphi, 1819, and unidentified Trichuris are reported from Maule’s tuco-tuco, Ctenomysmaulinus, collected from Chile.

Babero and Cattan (1980) described Graphidiodes yañezi from the small intestine of a coruro, Spalacopuscyanus (Rodentia: Octodontidae), collected from near Concón, Chile.

Babero and Murua (1987) described a new species of whipworm, Trichurisfulvi obtained from the cecum of the Tawny tuco-tuco, Ctenomysfulvus Philippi, 1860, collected from San Pedro Atacama, Tarapaca province, Chile.

Lambert et al. (1988) described four new coccidian parasites in the genus Eimeria Schneider, 1875 recovered from the feces of the Highland tuco-tuco, Ctenomysopimus Wagner, 1848, trapped from several localities of the Department of Oruro, Bolivia, South America. Those species are E.granifera from Rancho Huancaroma, near the Rio Desaguadero, E.montuosi, from the north of Pomata Ayte, Rio Barros, E.opimi, and E.oruroensis, from the northeast and east of Rancho Huancaroma.

Babero and Murua (1990) described Trichurisrobusti from the cecum and large intestine of the Tawny tuco-tuco, Ctenomysfulvus, collected from La Hauyca, Tarapaca province, Chile.

Gardner and Duszynski (1990), during a study on morphometric comparison of a coccidian species, EimeriaopimiLambert et al., 1988, in different regions of Bolivia, the following host species were detected positive for this protozoan parasite. Those hosts include Lewis’s tuco-tuco, Ctenomyslewisi Thomas, 1926, collected from the areas of the high-altitude region in Tarija; the Reddish tuco-tuco, Ctenomysfrater Thomas, 1902, collected from medium latitude region of Tarija; the Conover’s tuco-tuco, Ctenomysconoveri Osgood, 1946, collected from Chaco thorn forest area in Chuquisaca; the Bolivian tuco-tuco, Ctenomysboliviensis Waterhouse, 1848, and the Steinbach’s tuco-tuco, Ctenomyssteinbachi Thomas, 1907 collected from the Tropical palm/savanna region of Santa Cruz, Bolivia. In addition, the following coccidian parasites were reported from the Highland tuco-tuco, Ctenomysopimus. These species include Eimeriaopimi, E.graniferaLambert et al., 1988, E.oruroensisLambert et al., 1988, and E.montuosiLambert et al., 1988 collected from the Oruro region E.opimi and E.granifera collected from the Potosi region.

Suriano and Navone (1994) described Trichurisbursacaudata obtained from the cecum of the Talas tuco-tuco, Ctenomystalarum Thomas, 1898 collected from Punta Indio, Buenos Aires, and T.pampeana found in the cecum of the Azara’s tuco-tuco, Ctenomysazarae Thomas, 1903, collected from Santa Rosa, La Pampa, Argentina (Suriano and Navone 1994). However, T.pampeana has been redescribed from its original voucher specimens (Rossin and Malizia 2005).

Brant and Gardner (1997) described Litomosoidesandersoni and L.ctenomyos from the abdominal and thoracic regions of the Highland tuco-tuco, Ctenomysopimus, collected from near Rancho Huancaroma, Departamento de Oruro, Bolivia.

Rossin and Malizia (2002), during a study of the relationship between helminth parasites and demographic attributes of a population, two unidentified helminth parasites were reported. Those include Heligmostrongylus Travassos, 1917 found in the small intestine, and Trichuris recovered from the cecum of the Talas tuco-tuco, Ctenomystalarum, collected from Necochea, Buenos Aires province, Argentina.

Rossin et al. (2004a) reported larvae of Hydatigera (syn. Taenia) taeniaeformis from the peritoneal cavity and liver of the Talas tuco-tuco, Ctenomystalarum, trapped in the urban areas of Mar de Cobo, Buenos Aires province, Argentina. These authors experimentally infected dogs with this species of tapeworm from the tucos and recovered adult cestodes.

Rossin et al. (2004b) redescribed Paraspidoderauncinata (Rudolphi, 1819) from a large number of specimens obtained from the cecum and large intestine of the Talas tuco-tuco, Ctenomystalarum, collected from Mar de Cobo, Buenos Aires province, Argentina.

Rossin and Malizia (2005a) redescribed Trichurispampeana Suriano & Navone, 1994 found in the cecum of the Azara’s tuco-tuco, Ctenomysazarae, collected from Santa Rosa, La Pampa province, and reported new voucher material, the Talas tuco-tuco, C.talarum Thomas, 1898, collected at the Necochea, coastal dunes of Buenos Aires province. Also, an unidentified Trichuris found in C.talarum collected from Buenos Aires province, Argentina was reported. Simultaneously, Rossin et al. (2005b) described Graphidiodessubterraneus from the stomach of the Talas tuco-tuco, Ctenomystalarum, collected from Mar de Cobo, Partido de Mar Chiquita, Mar del Plata, Argentina.

Continuing work on tucos, Rossin et al. (2006a) described Pudicactenomydis from the small intestine of the Talas tuco-tuco, Ctenomystalarum, collected from Mar de Cobo, Partido de Mar Chiquita, Argentina. In the same year, Rossin et al. (2006b) described Trichostrongylusduretteae obtained from the small intestine of the Talas tuco-tuco, Ctenomystalarum, collected from Mar de Cobo, Buenos Aires province, Argentina.

Rossin et al. (2009) reported Strongyloidesmyopotami Artigas & Pacheco, 1933 found in the small intestines of the Talas tuco-tuco, Ctenomystalarum, collected from Mar de Cobo, Buenos Aires province, Argentina, and from Pearson’s tuco-tuco, Ctenomyspearsoni Lessa & Langguth, 1983, collected from Penino, Departamento de San José, Uruguay.

During an ecological study of helminth parasite infection parameters in two species of South American subterranean rodents of the genus Ctenomys, Rossin et al. (2010a) documented seven species of Endoparasites from two collection localities, species of hosts studied included the Southern tuco-tuco, C.australis Rusconi, 1934, from Necochea, Buenos Aires Province, and Talas tuco-tuco, C.talarum Thomas, 1898, from Mar de Cobo, Buenos Aires province, Argentina. Both species of tuco-tuco’s harbored Trichurispampeana in the cecum, Pudicactenomydis Rossin et al., 2006 in the small intestine, and larvae of Taeniatalicei in the abdominal cavity. Moreover, C.talarum had four additional species of helminths, including Graphidiodessubterraneus Rossin et al., 2005 in the stomach, Paraspidoderauncinata in the large intestine, and Strongyloidesmyopotami and Trichostrongylusduretteae Rossin et al., 2006 in the small intestine.

Rossin et al. (2010b) redescribed the metacestode form of Taeniatalicei obtained from the peritoneal cavity of two tuco-tuco species including the Southern tuco-tuco, Ctenomysaustralis Rusconi, 1934, and the Talas tuco-tuco, Ctenomystalarum, from Necochea, Paraje Las Grutas, Buenos Aires Province in Argentina.

From Bolivia, Drabik and Gardner (2019) described Ancylostomactenomyos Drabik & Gardner, 2019 from the small intestine of the Bolivian tuco-tuco, Ctenomysboliviensis collected from two localities in the Department of Santa Cruz, 3.5 km west of Estación el Pailón and 2 km SSE of Santa Rosa de la Roca, and from Steinbach’s tuco-tuco, Ctenomyssteinbachi Thomas, 1907 collected from 2 km S. of Caranda by road in the Department of Santa Cruz.

Gardner et al. (2021) mentioned discovery of a new species of Mathevotaenia from the Highland tuco-tuco, Ctenomysopimus, collected in 1986 from Huancaroma, Department of Oruro, Bolivia (Gardner et al. 2023). Also from Bolivia, Gardner et al. (2021) also reported Paraspidodera nematodes including individuals from the cecae of Anderson’s tuco-tuco, CtenomysandersoniGardner et al., 2014, the Bolivian tuco-tuco or Cajuchi, Ctenomysboliviensis Waterhouse, 1848, Conover’s tuco-tuco, Ctenomysconoveri Osgood, 1946, Erica’s tuco-tuco, CtenomyserikacuellaraeGardner et al., 2014, the little Andean forest tuco-tuco, Ctenomysfrater Thomas, 1902, Lessa’s tuco-tuco, CtenomyslessaiGardner et al., 2014, Lewis’s tuco-tuco, Ctenomyslewisi, Steinbach’s tuco-tuco, Ctenomyssteinbachi, and Natterer’s tuco-tuco, Ctenomysnattereri Wagner, 1848. In addition, an undescribed species of Raillietina was found in the small intestine of C.erikacuellarae collected on the experiment station grounds near Monteagudo, Bolivia and Pudica sp. Travassos & Darriba, 1929 was also reported from the White-toothed tuco-tuco, Ctenomysleucodon Waterhouse, 1848.

The present study reports that during a biodiversity survey in Bolivia in 1986, Pudicapujoli Durette-Desset & Tcheprakoff, 1990 was found in a single specimen of the White-toothed tuco-tuco, Ctenomysleucodon Waterhouse, 1848, collected from near San Andreas de Machaca, Bolivia.

Acknowledgements

We thank the members of Manter Laboratory Parasitology at the University of Nebraska-Lincoln, University of Nebraska-Lincoln State Museum. Special thanks to all the landowners in the area of Cedar Point Biological Station, especially the Haythorn Land and Cattle Company and Jody Haythorn, for allowing us to collect mammals and parasites over the many years of our studies there. Special thanks go to Zeiss U.S.A. for 25 years of continuous support of the Manter Laboratory. The current research was made possible through the support of the U.S. National Science Foundation via grants DEB-0717214, DBI-0646356, DBI-9631295, and DBI-9411976 to SLG. All specimens collected at Cedar Point Biological Station were done under UNL IACUC No. 652.

Citation

Dursahinhan AT, Kenkel DA, Gardner SL (2023) Helminth and protozoan parasites of subterranean rodents (Chordata, Mammalia, Rodentia) of the world. ZooKeys 1151: 159–203. https://doi.org/10.3897/zookeys.1151.97126

Funding Statement

U.S. National Science Foundation via grants DEB-0717214, DBI-0646356, DBI-DBI-9631295, and DBI-9411976.

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