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Helminth and protozoan parasites of subterranean rodents (Chordata, Mammalia, Rodentia) of the world
expand article infoAltangerel T. Dursahinhan, Daniel A. Kenkel, Scott L. Gardner
‡ University of Nebraska State Museum, Lincoln, United States of America
Open Access

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Published studies and ten new unpublished records included herein reveal that approximately 174 species of endoparasites (helminths and protozoans) are known from 65 of 163 species of rodents that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 Thomomys atrovarius J. A. Allen, 1898 NA NA
2 Thomomys bottae (Eydoux & Gervais, 1836) NA NA
3 Thomomys bulbivorus (Richardson, 1829) NA NA
4 Thomomys clusius Coues, 1875 NA NA
5 Thomomys idahoensis Merriam, 1901 NA NA
6 Thomomys mazama Merriam, 1897 NA NA
7 Thomomys monticola J. A. Allen, 1893 NA NA
8 Thomomys nayarensis Mathis et al., 2013 NA NA
9 Thomomys sheldoni Bailey, 1915 NA NA
10 Thomomys talpoides (Richardson, 1828) NA NA
11 Thomomys townsendii (Bachman, 1839) NA NA
12 Thomomys umbrinus (Richardson, 1829) NA NA
Geomyini 13 Geomys arenarius Merriam, 1895 NA NA
14 Geomys attwateri Merriam, 1895 NA NA
15 Geomys breviceps Baird, 1855 NA NA
16 Geomys bursarius (Shaw, 1800) NA NA
17 Geomys jugossicularis Hooper, 1940 NA NA
18 Geomys knoxjonesi Baker & Genoways, 1975 NA NA
19 Geomys lutescens Merriam, 1890 NA NA
20 Geomys personatus True, 1889 NA NA
21 Geomys pinetis Rafinesque, 1817 Nt Nt
22 Geomys streckeri Davis, 1943 NA NA
23 Geomys texensis Merriam, 1895 NA NA
24 Geomys tropicalis Goldman, 1915 NA NA
25 Zygogeomys trichopus Merriam, 1895 Nt Nt
26 Orthogeomys grandis (Thomas, 1893) NA Nt
Castorimorpha Geomorpha Geomyidae Geomyinae Geomyini 27 Heterogeomys cavator (Bangs, 1902) Nt Nt
28 Heterogeomys cherriei (J. A. Allen, 1893) Nt Nt
29 Heterogeomys dariensis (Goldman, 1912) Nt Nt
30 Heterogeomys heterodus (Peters, 1865) Nt Nt
31 Heterogeomys hispidus (Le Conte, 1852) Nt Nt
32 Heterogeomys lanius Elliot, 1905 Nt Nt
33 Heterogeomys underwoodi Osgood, 1931 Nt Nt
34 Pappogeomys bulleri (Thomas, 1892) Nt Nt
35 Cratogeomys castanops (Baird, 1852) NA Nt
36 Cratogeomys fulvescens Merriam, 1895 NA Nt
37 Cratogeomys fumosus (Merriam, 1892) Nt Nt
38 Cratogeomys goldmani (Merriam, 1895) NA Nt
39 Cratogeomys merriami (Thomas, 1893) Nt Nt
40 Cratogeomys perotensis Merriam, 1895 NA Nt
41 Cratogeomys planiceps (Merriam, 1895) NA Nt
Hystricomorpha Histricognathi Ctenomyidae 42 Ctenomys andersoni Gardner et al., 2014 Nt Nt
43 Ctenomys argentinus J. R. Contreras & Berry, 1982 Nt Nt
44 Ctenomys australis Rusconi, 1934 Nt Nt
45 Ctenomys azarae Thomas, 1903 Nt Nt
46 Ctenomys bergi Thomas, 1902 Nt Nt
47 Ctenomys bicolor Miranda-Ribeiro, 1914 Nt Nt
48 Ctenomys boliviensis Waterhouse, 1848 Nt Nt
49 Ctenomys bonettoi J. R. Contreras & Berry, 1982 Nt Nt
50 Ctenomys brasiliensis de Blainville, 1826 Nt Nt
51 Ctenomys colburni J. A. Allen, 1903 Nt Nt
52 Ctenomys coludo Thomas, 1920 Nt Nt
52 Ctenomys coludo Thomas, 1920 Nt Nt
53 Ctenomys conoveri Osgood, 1946 Nt Nt
Hystricomorpha Histricognathi Ctenomyidae 54 Ctenomys coyhaiquensis Kelt & Gallardo, 1994 Nt Nt
55 Ctenomys dorbignyi Contreras & Contreras, 1984 Nt Nt
56 Ctenomys dorsalis Thomas, 1900 Nt Nt
57 Ctenomys emilianus Thomas & S. Leger, 1926 Nt Nt
58 Ctenomys erikacuellarae Gardner et al., 2014 Nt Nt
59 Ctenomys famosus Thomas, 1920 Nt Nt
60 Ctenomys flamarioni Travi, 1981 Nt Nt
61 Ctenomys fodax Thomas, 1910 Nt Nt
62 Ctenomys fochi Thomas, 1919 Nt Nt
63 Ctenomys frater Thomas, 1902 Nt Nt
64 Ctenomys fulvus Philippi, 1860 Nt Nt
65 Ctenomys goodfellowi Thomas, 1921 Nt Nt
66 Ctenomys haigi Thomas, 1919 Nt Nt
67 Ctenomys ibicuiensis Freitas et al., 2012 Nt Nt
68 Ctenomys johannis Thomas, 1921 Nt Nt
69 Ctenomys juris Thomas, 1920 Nt Nt
70 Ctenomys knighti Thomas, 1919 Nt Nt
71 Ctenomys lami Freitas, 2001 Nt Nt
72 Ctenomys latro Thomas, 1918 Nt Nt
73 Ctenomys lessai Gardner et al., 2014 Nt Nt
74 Ctenomys leucodon Waterhouse, 1848 Nt Nt
75 Ctenomys lewisi Thomas, 1926 Nt Nt
76 Ctenomys magellanicus Bennett, 1836 Nt Nt
77 Ctenomys mariafarelli Azurduy, 2005 Nt Nt
78 Ctenomys maulinus Philippi, 1872 Nt Nt
79 Ctenomys mendocinus Philippi, 1869 Nt Nt
80 Ctenomys minitus Nehring, 1887 Nt Nt
81 Ctenomys nattereri Wagner, 1848 Nt Nt
82 Ctenomys occultus Thomas, 1920 Nt Nt
83 Ctenomys opimus Wagner, 1848 Nt Nt
84 Ctenomys osvaldoreigi J. R. Contreras, 1985 Nt Nt
85 Ctenomys paraguayensis J. R. Contreras, 2000 Nt Nt
86 Ctenomys pearsoni Lessa & Langguth, 1983 Nt Nt
87 Ctenomys perrensi Thomas, 1896 Nt Nt
88 Ctenomys peruanus Sanborn & Pearson, 1947 Nt Nt
89 Ctenomys pilarensis J. R. Contreras, 1993 Nt Nt
90 Ctenomys pontifex Thomas, 1918 Nt Nt
91 Ctenomys porteousi Thomas, 1916 Nt Nt
92 Ctenomys pundti Nehring, 1900 Nt Nt
93 Ctenomys rionegrensis Langguth & Abella, 1970 Nt Nt
94 Ctenomys roigi J. R. Contreras, 1988 Nt Nt
95 Ctenomys rondoni Miranda-Ribeiro, 1914 Nt Nt
96 Ctenomys rosendopascuali J. R. Contreras, 1995 Nt Nt
97 Ctenomys talarum Thomas, 1898 Nt Nt
98 Ctenomys torquatus Lichtenstein, 1830 Nt Nt
99 Ctenomys tuconax Thomas, 1925 Nt Nt
100 Ctenomys tucumanus Thomas, 1900 Nt Nt
101 Ctenomys tulduco Thomas, 1921 Nt Nt
102 Ctenomys saltarius Thomas, 1912 Nt Nt
103 Ctenomys scagliai J. R. Contreras, 1999 Nt Nt
104 Ctenomys sericeus J. A. Allen, 1903 Nt Nt
105 Ctenomys sociabilis Pearson & Christie, 1985 Nt Nt
106 Ctenomys steinbachi Thomas, 1907 Nt Nt
107 Ctenomys validus J. R. Contreras et al., 1977 Nt Nt
108 Ctenomys viperinus Thomas, 1926 Nt Nt
109 Ctenomys yatesi Gardner et al., 2014 Nt Nt
110 Ctenomys yolandae J. R. Contreras & Berry, 1984 Nt Nt
Hystricomorpha Histricognathi Octodontidae 111 Spalacopus cyanus (Molina, 1782) Nt Nt
Heterocephalidae 112 Heterocephalus glaber Rüppell, 1842 E E
Bathyergidae 113 Heliophobius argenteocinereus Peters, 1846 E E
114 Bathyergus janetta Thomas & Schwann, 1904 E E
115 Bathyergus suillus (Schreber, 1782) E E
116 Georychus capensis (Pallas, 1778) E E
117 Cryptomys hottentotus (Lesson, 1826) E E
118 Fukomys amatus (Wroughton, 1907) E E
119 Fukomys anselli (Burda et al., 1999) E E
120 Fukomys bocagei (de Winton, 1897) E E
121 Fukomys damarensis (Ogilby, 1838) E E
122 Fukomys darlingi (Thomas 1895) E E
123 Fukomys foxi (Thomas, 1911) E E
124 Fukomys kafuensis (Burda et al., 1999) E E
125 Fukomys mechowii (Peters, 1881) E E
126 Fukomys ochraceocinereus (Heuglin, 1846) E E
127 Fukomys vandewoestijneae Van Daele et al., 2013 E E
128 Fukomys whytei (Thomas, 1897) E E
129 Fukomys zechi (Matschie, 1900) E E
Myomorpha Cricetidae Arvicolinae Prometheomyini 130 Prometheomys schaposchnikowi Satunin, 1901 P P
Ellobiusini 131 Ellobius alaicus Vorontsov et al., 1969 P P
132 Ellobius fuscocapillus (Blyth, 1843) P P
133 Ellobius lutescens Thomas, 1897 P P
134 Ellobius talpinus (Pallas, 1770) P P
135 Ellobius tancrei Blasius, 1884 P P
Spalacidae Myospalacinae 136 Myospalax armandii (Milne-Edwards, 1867) P P
137 Myospalax aspalax (Pallas, 1776) P P
138 Myospalax epsilanus Thomas, 1912 P P
139 Myospalax myospalax (Laxmann, 1773) P P
140 Myospalax psilurus (Milne-Edwards, 1874) P P
141 Eospalax baileyi (Thomas, 1911) P P
142 Eospalax cansus (Lyon, 1907) P P
143 Eospalax fontanierii (Milne-Edwards, 1867) P P
144 Eospalax rothschildi (Thomas, 1911) P P
145 Eospalax rufescens (J. A. Allen, 1909) P P
146 Eospalax smithii (Thomas, 1911) P P
Rhizomyinae Rhizomyini 147 Rhizomys pruinosus (Blyth, 1851) P O
148 Rhizomys sinensis Gray, 1831 P O
149 Rhizomys sumatrensis (Raffles, 1821) O O
150 Cannomys bodius (Hodgson, 1841) O O
Tachyoryctini 151 Tachyoryctes macrocephalus (Rüppell, 1842) E E
152 Tachyoryctes splendens (Rüppell, 1835) E E
Spalacinae 153 Spalax antiquus Méhely, 1909 P P
154 Spalax arenarius Reshetnik, 1939 P P
155 Spalax giganteus Nehring, 1898 P P
156 Spalax graecus Nehring, 1898 P P
157 Spalax istricus Méhely, 1909 P P
158 Spalax microphthalmus Güldenstädt, 1770 P P
159 Spalax uralensis Tiflov & Usov, 1939 P P
160 Spalax zemni (Erxleben, 1777) P P
161 Nannospalax ehrenbergi Nehring, 1898 P P
162 Nannospalax leucodon (Nordmann, 1840) P P
163 Nannospalax xanthodon (Nordmann, 1840) P P

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). Rhizomys pruinosus (Blyth, 1851) and Rhizomys sinensis 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 Rhizomys sumatrensis (Raffles, 1821) and Cannomys bodius (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 Spalacopus cyanus (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.

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
Bathyergus suillus (Schreber, 1782) Mammalakis macrospiculum (Ortlepp, 1939) Lutermann et al. 2012
Ortleppstrongylus bathyergi Ortlepp, 1939 De Graaff 1964
Paralibyostrongylus bathyergi (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
Cryptomys hottentotus (Lesson, 1826) Ascarops africana (Sandground, 1933) Lutermann et al. 2013
Heligmonina Baylis, 1928 Viljoen et al. 2011
Inermicapsifer madagascariensis (Davaine, 1870) De Graaff 1981
Mammalakis macrospiculum (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
Fukomys anselli (Burda et al., 1999) Hexametra Travassos, 1920 Lutermann et al. 2018
Inermicapsifer Janicki, 1910 Lutermann et al. 2018
Mammalakis zambiensis Junker et al., 2017 Junker et al. 2017
Protospirura muricola (Gedoelst, 1916) Lutermann et al. 2018
Protospirura numidica Seurat, 1914 Lutermann et al. 2018
Protospirura Seurat, 1914 Lutermann et al. 2018
Rodentolepis cf. microstoma (Dujardin, 1945) Lutermann et al. 2018
Fukomys kafuensis (Burda et al., 1999) Inermicapsifer madagascariensis (Davaine, 1870) Scharff et al. 1997
Protospirura muricola (Gedoelst, 1916) Scharff et al. 1997
Fukomys mechowii (Peters, 1881) Capillaria Zeder, 1800 Scharff et al. 1997
Inermicapsifer madagascariensis (Davaine, 1870) Scharff et al. 1997
Protospirura muricola (Gedoelst, 1916) Scharff et al. 1997
Raillietina Fuhrman, 1920 Scharff et al. 1997
Georychus capensis (Pallas, 1778) Coenurus spalacis Diesing, 1864 Diesing 1864
Echinococcus Rudolphi, 1801 De Graaff 1964; Hüttner and Romig 2009
Trichuris Roederer, 1761 Lutermann et al. 2012
Heliophobius argenteocinereus Peters, 1846 Eimeria burdai Koudela et al., 2000 Koudela et al. 2000
Eimeria heliophobii Modrý et al., 2005 Modrý et al. 2005
Eimeria nafuko Modrý et al., 2005 Modrý et al. 2005
Eimeria yamikamiae Modrý et al., 2005 Modrý et al. 2005
Inermicapsifer arvicanthidis (Kofend, 1917) Baruš et al. 2003; Tenora et al. 2003
Protospirura muricola (Gedoelst, 1916) Baruš et al. 2003; Tenora et al. 2003
Heterocephalus glaber Rüppell, 1842 Eimeria heterocephali Levine & Ivens, 1965 Levine and Ivens 1965
Tachyoryctes splendens (Rüppell, 1835) Taenia brauni Setti, 1897 Fain 1956
Tachyoryctes macrocephalus (Rüppell, 1842) Ascarops africana (Sandground, 1933) Schmidt and Canaris 1968
Figure 1. 

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%).

Diesing (1864) reported the first helminth parasite species from a subterranean rodent host, where Taenia spalacis (Diesing, 1864) was reported from Georychus capensis (Pallas, 1779) collected from Port Natal, South Africa.

Ortlepp (1939) described three new nematode species from the Cape dune mole-rat, Bathyergus suillus (Schreber, 1782) (Bathyergidae: Rodentia) collected from Strandfontein and Cape Town, South Africa including: Libyostrongylus bathyergi Ortlepp, 1939, Longistriata bathyergi, and Mammalakis macrospiculum (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 Paralibyostrongylus bathyergi, Ortleppstrongylus bathyergi, and Mammalakis macrospiculum, (see De Graaff 1964; Lutermann and Bennett 2012).

Fain (1956) reported Taenia brauni Setti, 1897, from Tachyoryctes splendens (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 Bathyergus suillus, 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, Eimeria heterocephali from the mucosal epithelial cells of the cecum of a Heterocephalus glaber specimen collected at Somaliland or Kenya, South Africa.

Schmidt and Canaris (1968) reported Ascarops africana (Sandground, 1933) from Tachyoryctes macrocephalus (Rüppell, 1842) collected from Njoro, Kenya, East Africa.

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

Scharff et al. (1997) reported Inermicapsifer madagascariensis from the small intestine, and Protospirura muricola (Gedoelst, 1916) from the colon of Fukomys kafuensis (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 Fukomys mechowii (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 Eimeria burdai, as a new species of coccidian from the subterranean African silvery mole-rat, Heliophobius argenteocinereus 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 Inermicapsifer arvicanthidis (Kofend, 1917) and Protospirura muricola, 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: Eimeria heliophobii, 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 Cryptomys hottentotus, 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 Bathyergus suillus at Cape Town International Airport, Cape Town, South Africa, found these rodents infected with three species of nematodes, including: Mammalakis macrospiculum, Paralibyostrongylus bathyergi, 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 Ascarops africana from the small intestine of Cryptomys hottentotus collected from KwaZulu-Natal, South Africa.

Archer et al. (2017), in a seasonal comparative study between two Common mole-rat populations found Mammalakis macrospiculum, Neoheligmonella Durette-Desset, 1971, and Trichuris sp. in Cryptomys hottentotus 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, Mammalakis zambiensis acquired from the large intestine and cecum of Ansell’s mole-rat, Fukomys anselli (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, Protospirura muricola, Protospirura numidica Seurat, 1914, and Rodentolepis cf. microstoma (Dujardin, 1945).

Palearctic subterranean rodent endoparasites

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

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
Cannomys bodius (Hodgson, 1841) Hymenolepis diminuta (Rudolphi, 1819) Malsawmtluangi and Tandon 2009
Ellobius fuscocapillus (Blyth, 1843) Syphacia obvelata (Rudolphi, 1802) Arzamani et al. 2017
Ellobius lutescens Thomas, 1897 Eimeria lutescenae Musaev & Veisov, 1963 Musaev and Veisov 1965a
Ellobius talpinus (Pallas, 1770) Aprostatandrya macrocephala Douthitt, 1915 Tokobaev 1960
Catenotaenia pusilla Goeze, 1782 Zanina and Tokobaev 1962a
Echinococcus multilocularis Leuckart, 1863 Tokobaev 1960
Eimeria ellobii Svanbaev, 1965 Musaev and Veisov 1965a
Eimeria kazakhstanensis Levine, 1965 Levine and Ivens 1965
Eimeria tadshikistanica Veisov, 1964 Musaev and Veisov 1965a
Eimeria talpini Levine, 1965 Levine and Ivens 1965
Hymenolepis diminuta (Rudolphi, 1819) Zanina and Tokobaev 1962a
Mesocestoides Vaillant, 1863 Tokobaev 1960
Moniliformis moniliformis Bremser, 1811 Zanina and Tokobaev 1962a
Nomadolepis ellobii Makarikov et al., 2010 Makarikov et al. 2010
Physocephalus ellobii Schulz, 1927 Schultz 1927
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Zanina and Tokobaev 1962a
Ellobius tancrei Blasius, 1884 Arostrilepis batsaikhani Dursahinhan et al., 2022 Dursahinhan et al. 2022
Echinococcus multilocularis Leuckart, 1863 Afonso et al. 2015
Eospalax baileyi (Thomas, 1911) Eimeria baileyii Cao et al., 2014 Cao et al. 2014
Eimeria fani Cao et al., 2014 Cao et al. 2014
Eimeria menyuanensis Cao et al., 2014 Cao et al. 2014
Eimeria myospalacensis Cao et al., 2014 Cao et al. 2014
Ransomus qinghaiensis Ming et al., 2004 Ming et al. 2004
Versteria (syn. Taenia) mustelae Gmelin, 1790 Zhao, et al. 2014
Eospalax fontanierii (Milne-Edwards, 1867) Echinococcus multilocularis Leuckart, 1863 Craig 2006
Heligmoptera giraudouxi Elias et al., 2002 Elias, et al. 2002
Heligmoptera querei Elias et al., 2002 Elias, et al. 2002
Myospalax myospalax (Laxmann, 1773) Echinococcus multilocularis Leuckart, 1863 Shaykenov and Mahmutov 1968
Heligmoptera sibirica Shakhmatova, 1990 Shakhmatova 1990
Heligmosomum myospalaxi Nadtochii, 1970 Nadtochii 1970
Hymenolepis rymzhanovi Makarikov & Tkach, 2013 Makarikov and Tkach 2013
Moniliformis clarki (Ward, 1917) Vlasenko and Krivopalov 2017
Paranoplocephala Lühe, 1910 Vlasenko and Krivopalov 2017
Versteria mustelae (Gmelin, 1790) Vlasenko and Krivopalov 2017
Myospalax psilurus (Milne-Edwards, 1874) Ascarops strongylina (Rudolphi, 1819) Ganzorig et al. 1999
Nannospalax ehrenbergi Nehring, 1898 Eimeria adiyamanensis Sayin, 1980 Sayın 1980
Eimeria anzanensis Couch et al, 1993 Couch et al. 1993
Eimeria carmelensis Couch et al, 1993 Couch et al. 1993
Eimeria celebii Sayin, 1980 Sayın 1980
Eimeria haranica Sayin, 1980 Sayın 1980
Eimeria marasensis Sayin, 1980 Sayın 1980
Eimeria microspalacis Golemansky & Darawish, 1992 Golemansky and Darwish 1992
Eimeria oytuni Sayin, 1980 Sayın 1980
Eimeria spalacensis Couch et al, 1993 Couch et al. 1993
Eimeria torosicum Sayin, 1980 Sayın 1980
Eimeria urfensis Sayin, 1980 Sayın 1980
Ganguleterakis spalaxi Kozlov & Yangolenko, 1963 Wertheim and Nevo 1971
Gongylonema longispiculum Schulz, 1927 Wertheim and Nevo 1971
Heligmonella Mönnig, 1927 Wertheim and Nevo 1971
Heligmonina nevoi Wertheim & Nevo, 1971 Wertheim and Nevo 1971
Isospora spalacensis Couch et al, 1993 Couch et al. 1993
Microcephaloides nevoi (Fair et al., 1990) Haukisalmi 2009 Fair et al. 1990; Haukisalmi 2009
Trichuris muris (Schrank, 1788) Wertheim and Nevo 1971
Nannospalax leucodon (Nordmann, 1840) Aprostatandrya Kirshenblat, 1938 Andreiko 1963a
Ascaris spalacis Shults & Aloyan, 1950 Shults and Aloyan 1950
Coenurus parviuncinatus Kirschenblatt, 1939 Korniushin and Sharpilo 1986
Eimeria celebii Sayin, 1980 Nalbantoğlu et al. 2010
Eimeria elliptica Sayin et al., 1977 Sayin et al. 1977
Eimeria lalahanensis Sayin, et al., 1977 Sayin et al. 1977
Eimeria leucodonica Veisov, 1975 Veisov 1975
Eimeria maralikiensis Veisov, 1975 Veisov 1975
Eimeria oytuni Sayin, 1980 Nalbantoğlu et al. 2010
Eimeria spalacis Sayin et al., 1977 Sayin et al. 1977
Eimeria talikiensis Veisov, 1975 Veisov 1975
Eimeria torosicum Sayin, 1980 Nalbantoğlu et al. 2010
Eimeria turkmenica Sayin et al., 1977 Sayin et al. 1977
Eimeria tuzdili Sayin, et al., 1977 Sayin et al. 1977
Heligmosomum spalacis Kirsenblat, 1965 Mészáros 1968
Heligmosomum moldovensis Andreiko, 1963 Andreiko 1963a
Isospora anatolicum Sayin, et al., 1977 Sayin et al. 1977
Longistriata spalacis Sharpilo, 1973 Sharpilo 1973a
Mammalakis spalacis Marcu, 1930 Andreiko 1963a
Moniliformis moniliformis Bremser, 1811 Murai 1968
Taenia straminea (Goeze, 1782) Spasskii 1954 Andreiko 1963a
Prometheomys schaposchnikowi Satunin, 1901 Dicrocoelium dendriticum (Rudolphi, 1819) Razumova 1957
Heligmosomum halli (Schulz, 1926) Razumova 1957
Microcephaloides Haukisalmi et al., 2008 Razumova 1957
Taenia polyacantha Leuckart, 1856 Razumova 1957
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Razumova 1957
Rhizomys pruinosus (Blyth, 1851) Mammalakis spumosa (Schneider, 1866) Chaisiri et al. 2017
Rhizomys sinensis Gray, 1831 Cryptosporidium occultus Kváč, 2018 Wei et al. 2019
Cryptosporidium parvum Tyzzer, 1912 Wei et al. 2019
Spalax arenarius Reshetnik, 1939 Longistriata spalacis Sharpilo, 1973 Sharpilo 1973a
Spalax graecus Nehring, 1898 Heligmosomum spalacis Kirsenblat, 1965 Kirshenblat 1965a
Spalax microphthalmus Güldenstädt, 1770 Ganguleterakis spalaxi Kozlov & Yangolenko, 1963 Kozlov and Yangolenko 1963a
Gongylonema longispiculum spalacis Schulz, 1927 Schultz 1927
Longistriata spalacis Sharpilo, 1973 Sharpilo 1973a
Mammalakis spalacis Marcu, 1930 Marcu 1930
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) Sharpilo 1976
Trichuris spalacis (Petrov & Potechina, 1953) Petrov and Potechina 1953
Figure 2. 

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%.

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, Physocephalus ellobii Schulz, 1927 was found from the stomach of Ellobius tancrei Blasius, 1884 collected from Kotlyrevsky, the northern Caucasus region of Russia. Second, Gongylonema longispiculum spalacis Schulz, 1927 was described as the first subspecies found under the mucous membrane of the stomach of Spalax microphthalmus 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 Mammalakis spalacis Marcu, 1930 also obtained from S. microphthalmus collected from Romania.

Somewhat later, Schulz and Aloyan (1950), described Ascaris spalacis Schulz & Aloyan, 1950 from Lesser mole-rat, Nannospalax leucodon (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 Trichuris spalacis 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, Prometheomys schaposchnikowi Satunin, 1901, captured from Ossetia, Russia. These include Dicrocoelium dendriticum (Rudolphi, 1819), Heligmosomum halli (Schulz, 1926), Microcephaloides Haukisalmi et al., 2008, Taenia polyacantha Leuckart, 1856, and Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786).

Tokobaev (1960) reported the collection of Ellobius talpinus (Pallas, 1770) from the Kyrgyz Republic and found larvae of Echinococcus multilocularis from the liver. In the same report, he reported Aprostatandrya macrocephala 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 Catenotaenia pusilla Goeze, 1782, Hymenolepis diminuta Rudolphi, 1819, Moniliformis moniliformis 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, (Nannospalax leucodon) collected from the central part of Moldova, Romania had the following helminths: Mammalakis spalacis from the cecum, Taenia straminea (Goeze, 1782) Spasskii, 1954 and unidentified species of Aprostatandrya Kirshenblat, 1938 from the small intestine. In addition, she described Heligmosomum moldovensis Andreiko, 1963 from the small intestine of N. leucodon.

Kozlov and Yangolenko (1963) described Ganguleterakis spalaxi Kozlov & Yangolenko, 1963 from Spalax microphthalmus collected from Ukraine.

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

Levine and Ivens (1965) described two species of Eimeria Fischer, 1814 from the Northern mole vole, including: Ellobius kazakhstanensis Levine & Ivens, 1965, and Ellobius talpini Levine & Ivens, 1965 from the fecal of Ellobius talpinus collected from Kazakhstan.

Musaev and Veisov (1963) described Eimeria lutescenae Musaev & Veisov, 1963 from Ellobius lutescens Thomas, 1897 from Nakhichevanskaia, Azerbaijan. In addition, two Eimeria (Schneider, 1875) species were reported with their descriptions, including: Eimeria ellobii Svanbaev, 1965 and Eimeria tadshikistanica Veisov, 1964 from Ellobius talpinus collected from Tajikistan.

Shaykenov and Mahmutov (1968) reported Echinococcus multilocularis found in Myospalax myospalax (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 Heligmosomum spalacis recovered from the Lesser mole-rat, Nannospalax leucodon, collected from Hungary.

Murai (1968) recorded the Lesser mole-rat, N. leucodon, as a new host of Moniliformis moniliformis. The acanthocephalid parasite was extracted from the small intestines of two individuals of Lesser mole-rats. Also, Heligmosomum spalacis 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 Heligmosomum myospalaxi Nadtochii, 1970 obtained from the small intestine of Myospalax myospalax 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, Nannospalax ehrenbergi Nehring, 1898 including Ganguleterakis spalaxi, Gongylonema longispiculum Schulz, 1927, Trichuris muris (Schrank, 1788), and one unidentified nematode in the genus Heligmonella Mönnig, 1927. They also described Heligmonina nevoi Wertheim & Nevo, 1971 from the same host species.

Sharpilo (1973) described Longistriata spalacis from the small intestine of Lesser mole-rat, Nannospalax leucodon. He reported that this nematode species was also found from Spalax arenarius Reshetnik, 1939, and Spalax microphthalmus. 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 Spalax microphthalmus.

Veisov (1975) described three new species of coccidia of the genus Eimeria Schneider, 1875 from Nannospalax leucodon, including Eimeria maralikiensis Veisov, 1975 and Eimeria talikiensis Veisov, 1975 collected from Talnisk and Maralik Aniisk regions, Armenian, also, describing Eimeria leucodonica Veisov, 1975 from the Talinsk region only.

Sayin et al. (1977), during a survey of Lesser mole-rats, Nannospalax leucodon, in Lalahan district in Ankara, Turkey, described six new species of coccidia in the genus Eimeria Schneider, 1875 including E. elliptica Sayin et al., 1977, E. lalahanensis Sayin et al., 1977, E. spalacis Sayin et al., 1977, E. turkmenica Sayin et al., 1977, E. tuzdili Sayin et al., 1977, and Isospora anatolicum Sayin et al., 1977.

Sayın (1980), during a survey conducted from 1976 through 1978, studied 41 individuals of the Middle East blind mole-rats, Nannospalax ehrenbergi, 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 Coenurus parviuncinatus Kirschenblatt, 1939 obtained from Nannospalax leucodon collected from Armenia.

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

Shakhmatova (1990) described Heligmoptera sibirica Shakhmatova, 1990 found from the Siberian zokor, Myospalax myospalax, collected from the Gorno-Altai autonomous region of Russia.

Golemansky and Darwish (1992) described Eimeria microspalacis Golemansky & Darwish, 1992 from the Middle East blind mole-rat, Nannospalax ehrenbergi, 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, Nannospalax ehrenbergi, collected from 12 different localities in Israel including Eimeria anzanensis Couch et al., 1993, E. carmelensis Couch et al., 1993, E. spalacensis Couch et al., 1993, and Isospora spalacensis Couch et al., 1993.

Ganzorig et al. (1999) redescribed Ascarops strongylina (Rudolphi, 1819) from the Transbaikal zokor, Myospalax psilurus (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, Eospalax fontanierii (Milne-Edwards, 1867) including: Heligmoptera giraudouxi Elias & Durette-Desset, 2002, and Heligmoptera querei Elias & Durette-Desset, 2002 with the new description of the genus.

More recently in China, Ming et al. (2004) described Ransomus qinghaiensis Ming et al., 2004 from the cecum of the Plateau zokor, Eospalax baileyi (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, Eospalax fontanierii as one of the intermediate hosts of Echinococcus multilocularis.

Malsawmtluangi and Tandon (2009) reported Hymenolepis diminuta attained from the Lesser bamboo rat, Cannomys bodius (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, Nannospalax leucodon, collected from the Eryaman district of Ankara, Turkey. Those are Eimeria celebii , E. oytuni Sayin, 1980, and E. torosicum Sayin, 1980. In the same year, Makarikov et al. (2010) described the cestode Nomadolepis ellobii Makarikov et al., 2010, simultaneously establishing a new genus for the tapeworm that was obtained from the small intestine of the Northern mole vole, Ellobius talpinus, collected from southwestern Siberia, Russia.

Soon after, Makarikov and Tkach (2013) described Hymenolepis rymzhanovi Makarikov & Tkach, 2013 from the small intestine of the Siberian zokor, Myospalax myospalax collected from eastern Kazakhstan.

Cao et al. (2014) described four new species of Eimeria from the Plateau zokor, Eospalax baileyi, collected from Haibei area, Qinghai Province, China. The parasites include Eimeria baileyii Cao et al., 2014, Eimeria fani Cao et al., 2014, Eimeria menyuanensis Cao et al., 2014, and Eimeria myospalacensis Cao 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, Eospalax baileyi 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 Echinococcus multilocularis from the livers of Eastern mole voles, Ellobius tancrei 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 Moniliformis clarki (Ward, 1917), Paranoplocephala Lühe, 1910 and larvae of Versteria mustelae (Gmelin, 1790) from Myospalax myospalax collected from the southern Tomsk region, Russia. Then, Arzamani et al. (2017) reported Syphacia obvelata (Rudolphi, 1802) (probably a misidentification as S. obvelata occurs only in species of Mus) obtained in the Southern mole vole, Ellobius fuscocapillus (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 Mammalakis spumosa (Schneider, 1866) from Rhizomys pruinosus in Cambodia.

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

Dursahinhan et al. (2022) described Arostrilepis batsaikhani from the Zaisan mole vole, Ellobius tancrei 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.

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
Cratogeomys castanops (Baird, 1852) Calodium americanum (Read, 1949) Present study
Eimeria geomydis Skidmore, 1929 Present study
Monoecocestus sp. Beddard, 1914 Present study
Vexillata convoluta Caballero & Cerecero, 1943 Present study
Cratogeomys merriami (Thomas, 1893) Paraspidodera uncinata Travassos, 1914 Lamothe-Argumedo et al. 1997
Vexillata convoluta Caballero & Cerecero, 1943 Caballero and Cerecero 1943
Cratogeomys planiceps (Merriam, 1895) Hymenolepis cratogeomyos Gardner et al., 2020 Gardner et al. 2020
Geomys attwateri Merriam, 1895 Monoecocestus centroovarium Dronen et al., 1994 Dronen et al. 1994
Protospirura ascaroidea Hall, 1916 LeBrasseur 2017
Vexillata geomyos Falcón-Ordaz et al., 2006 Falcón-Ordaz et al. 2006
Geomys breviceps Baird, 1855 Eimeria geomydis Skidmore, 1929 Upton et al. 1992
Litomosoides westi Gardner & Schmidt, 1986 Pitts et al. 2000
Monoecocestus anoplocephaloides (Douthitt, 1915) Douthitt 1915
Protospirura ascaroidea Hall, 1916 Hall 1916; English 1932
Geomys bursarius (Shaw, 1800) Andrya macrocephala Douthitt, 1915 Douthitt 1915; Hansen 1950; Ubelaker and Downhower 1965; Bartel and Gardner 2000
Anoplocephaloides infrequens (Douthitt, 1915) Douthitt 1915; Ubelaker and Downhower 1965; Bartel and Gardner 2000; Rausch 1976
Anoplocephaloides variabilis (Douthitt, 1915) Douthitt 1915; Rausch 1976
Calodium americanum (Read, 1949) Bartel and Gardner 2000
Calodium hepaticum (Bancroft, 1893) Ubelaker and Downhower 1965
Cittotaenia perplexa Stiles, 1897 Burnham 1953
Eimeria geomydis Skidmore, 1929 Skidmore 1929; Levine and Ivens 1965
Hymenolepis diminuta (Rudolphi, 1819) Burnham 1953
Hymenolepis geomydis Gardner & Schmidt, 1988 Gardner and Schmidt 1988
Hymenolepis weldensis Gardner & Schmidt, 1988 Gardner and Schmidt 1988; Bartel and Gardner 2000; Haukisalmi et al. 2010
Litomosa filaria (Beneden, 1873) Burnham 1953
Litomosoides westi Gardner & Schmidt, 1986 Gardner and Schmidt 1986
Moniliformis clarki (Ward, 1917) Bartel and Gardner 2000
Monocercomonoides Travis, 1932 Rissky 1962
Monoecocestus anoplocephaloides (Douthitt, 1915) Burnham 1953
Oochoristica Lűhe, 1898 Douthitt 1915
Ostertagia Ransom, 1907 Burnham 1953
Paranoplocephala infrequens (Douthitt, 1915) Ubelaker and Downhower 1965
Physaloptera limbata Leidy, 1856 Bartel and Gardner 2000
Protospirura ascaroidea Hall, 1916 English 1932; LeBrasseur 2017
Protospirura muris ascaroides (Hall, 1916) Burnham 1953
Pseudocittotaenia praecoquis (Stiles, 1985) Stiles 1895
Ransomus rodentorum Hall, 1916 Bartel and Gardner 2000
Geomys jugossicularis Hooper, 1940 Anoplocephaloides variabilis (Douthitt, 1915) Present study
Geomys lutescens Merriam, 1890 Hymenolepis weldensis Gardner & Schmidt, 1988 Gardner et al. 2020
Litomosoides westi Gardner & Schmidt, 1986 Present study
Physaloptera limbata Leidy, 1856 Present study
Ransomus rodentorum Hall, 1916 Present study
Monoecocestus anoplocephaloides (Douthitt, 1915) Burnham 1953
Geomys personatus True, 1889 Litomosoides westi Gardner & Schmidt, 1986 Pitts et al. 2000
Protospirura ascaroidea Hall, 1916 LeBrasseur 2017
Geomys pinetis Rafinesque, 1817 Mastophorus muris ascaroides (Gmelin, 1790) Hubbell and Goff 1939
Geomys texensis Merriam, 1895 Eimeria geomydis Skidmore, 1929 Upton et al. 1992
Hymenolepis Weinland, 1858 LeBrasseur 2017
Protospirura ascaroidea Hall, 1916 LeBrasseur 2017
Heterogeomys heterodus (Peter, 1865) Hobergia irazuensis Gardner et al., 2020 Gardner et al. 2020
Orthogeomys grandis (Thomas, 1893) Eimeria orthogeomys Lainson, 1968 Lainson 1968
Thomomys bottae (Eydoux & Gervais, 1836) Arostrilepis horrida (von Linstow, 1901) Schiller 1952; Voge 1955; Gardner 1985
Catenotaenia dendritica (Goeze, 1782) Voge 1955
Catenotaenia linsdalei McIntosh, 1941 McIntosh 1941
Eimeria thomomysis Levine et al., 1957 Levine et al. 1957; Levine and Ivens 1965
Heligmosomoides thomomyos Gardner & Jasmer, 1983 Gardner and Jasmer 1983
Hymenolepis citelli (McLeod, 1933) Voge 1955; Jasmer 1980
Litomosoides thomomydis Gardner, 1986 Gardner and Schmidt 1986
Monocercomonoides Travis, 1932 Gardner and Jasmer 1983
Monoecocestus anoplocephaloides (Douthitt, 1915) Hansen 1950
Ransomus rodentorum Hall, 1916 Jasmer 1980
Trichuris fossor Hall, 1916 Jasmer 1980; Douglas 1969
Thomomys bulbivorus (Richardson, 1829) Arostrilepis horrida (von Linstow, 1901) Gardner 1985
Arostrilepis schilleri Makarikov et al., 2012 Makarikov et al. 2012
Heligmosomoides thomomyos Gardner & Jasmer, 1983 Gardner 1985; Gardner and Jasmer 1983
Hymenolepis tualatinensis Gardner, 1985 Gardner 1985
Ransomus rodentorum Hall, 1916 Gardner 1985
Trichuris fossor Hall, 1916 Gardner 1985
Thomomys clusius Coues, 1875 Ransomus rodentorum Hall, 1916 Present study
Trichuris fossor Hall, 1916 Present study
Thomomys monticola J. A. Allen, 1893 Arostrilepis horrida (von Linstow, 1901) Howard and Childs 1959
Trichuris Roederer, 1761 Ingles 1952
Thomomys talpoides (Richardson, 1828) Andrya macrocephala Douthitt, 1915 Rausch and Schiller 1949
Anoplocephaloides infrequens (Douthitt, 1915) Frandsen and Grundmann 1961; Todd et al. 1971
Anoplocephaloides variabilis (Douthitt, 1915) Rausch 1976; Frandsen and Grundmann 1961; Todd et al. 1971; Lubinsky 1957
Arostrilepis horrida (von Linstow, 1901) Grundmann, et al. 1976; Frandsen and Grundmann 1961
Ascaris laevis Leidy, 1856 Grundmann et al. 1976; Frandsen and Grundmann 1961
Calodium hepaticum (Bancroft, 1893) Ubelaker and Downhower 1965; Lubinsky 1957; Dikmans 1932; Tryon 1947; Lubinsky 1956; Rausch 1961; Tryon and Cunningham 1968
Catenotaenia linsdalei McIntosh, 1941 Todd et al. 1971
Eimeria fitzgeraldi Todd & Tryon, 1970 Todd et al. 1971; Todd and Tryon 1970
Eimeria jemezi Wilber et al., 1994 Wilber et al. 1994
Eimeria thomomysis Levine et al., 1957 Levine and Ivens 1965; Levine et al. 1957
Hymenandrya thomomyis Smith, 1954 Smith 1954
Hymenolepis citelli (McLeod, 1933) Frandsen and Grundmann 1961
Hymenolepis diminuta (Rudolphi, 1819) Rankin 1945
Litomosoides carinii (Travassos, 1919) Lubinsky 1957
Litomosoides thomomydis Gardner, 1986 Gardner and Schmidt 1986
Nippostrongylus muris (Yokogawa, 1920) Frandsen and Grundmann 1961
Protospirura ascaroidea Hall, 1916 Todd et al. 1971
Pseudocittotaenia glandularis Beveridge, 1978 Beveridge 1978
Pseudocittotaenia praecoquis (Stiles, 1985) Grundmann et al. 1976; Frandsen and Grundmann 1961; Smith 1951
Ransomus rodentorum Hall, 1916 Grundmann et al. 1976; Frandsen and Grundmann 1961
Trichuris fossor Hall, 1916 Hall 1916; Grundmann et al. 1976; Frandsen and Grundmann 1961; Lubinsky 1957; Todd and Lepp 1972
Versteria mustelae (Gmelin, 1790) Lubinsky 1957
Vexillata vexillata (Hall, 1916) Todd et al. 1971
Thomomys umbrinus (Richardson, 1829) Arostrilepis horrida (von Linstow, 1901) Frandsen and Grundmann 1961
Ascaris laevis Leidy, 1856 Frandsen and Grundmann 1961
Hymenolepis citelli (McLeod, 1933) Frandsen and Grundmann 1961
Moniliformis clarki (Ward, 1917) Frandsen and Grundmann 1961
Paruterina candelabraria (Goeze, 1782) Frandsen and Grundmann 1961
Ransomus rodentorum Hall, 1916 Frandsen and Grundmann 1961
Trichuris fossor Hall, 1916 Frandsen and Grundmann 1961
Figure 3. 

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%.

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 Pseudocittotaenia praecoquis (Stiles, 1895) from Geomys bursarius (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 Thomomys fossor 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. Anoplocephaloides variabilis (Douthitt, 1915), A. infrequens (Douthitt, 1915), and Andrya macrocephala Douthitt, 1915 were all described from specimens taken from G. bursarius collected from Illinois, Minnesota, and North Dakota. Monoecocestus anoplocephaloides (Douthitt, 1915) was described from some specimens taken from Geomys breviceps 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 Geomys personatus True, collected in Texas.

Hall (1916) described the following nematodes from Thomomys fossor J. A. Allen [syn. T. talpoides (Richardson, 1828)]: Trichuris fossor Hall, 1916, from specimens collected near both Crested Butte and Livermore, Colorado and Vexillata vexillata (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 Protospirura ascaroidea Hall, 1916 was described from specimens recovered from the stomachs of Geomys bursarius collected near Norman, Oklahoma by Herman Douthitt and sent to MC Hall for study.

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

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

McIntosh (1941) described Catenotaenia linsdalei McIntosh, 1941 from Thomomys bottae bottae (Eydoux & Gervais, 1836) collected near Monterey, California on the Hastings Natural History Reservation.

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

Chandler (1945) redescribed Trichuris fossor Hall, 1916 from Thomomys bottae bottae 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 Hymenolepis diminuta (Rudolphi, 1819) from Thomomys talpoides, 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, Thomomys bottae.

Tryon (1947) reported both cestodes and nematodes in Thomomys talpoides 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 Andrya macrocephala Douthitt, 1915 as occurring in Thomomys talpoides tenellus Goldman from the Jackson Hole Wildlife Park in Wyoming.

Hansen (1950), during a study of the tapeworms of rodents, recorded Andrya macrocephala Douthitt, 1915 as occurring in 5 of 5 Geomys bursarius examined with up to 12 cestodes per host. Hansen (1950) also recorded Monoecocestus anoplocephaloides (Douthitt, 1915) from Thomomys bottae 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 Thomomys talpoides collected from Carbon County, Wyoming, reported the following cestodes: Pseudocittotaenia praecoquis (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 Thomomys monticola 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 Thomomys bottae from near O’Neals California as a host.

Burnham (1953), during a study of the parasites of Geomys bursarius, collected from four counties in Oklahoma reported the following species of parasites: Protospirura muris ascaroides (Hall, 1916) (syn. Mastophorus muris) from the stomachs of 18 hosts; Litomosa filaria 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; Hymenolepis diminuta (Rudolphi, 1819) from the small intestines of ten hosts (see discussion below for clarification of the problem concerning H. diminuta in geomyids); Monoecocestus anoplocephaloides (Douthitt, 1915) from 25 hosts, with a range of infection of 1–100 worms per host; and Cittotaenia perplexa Stiles, 1897 from two gophers.

Soon after, Smith (1954) described Hymenandrya thomomyis from the small intestine of Thomomys talpoides collected in Colorado and in this same publication, he recommended that Catenotaenia linsdalei 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 Catenotaenia dendritica (Goeze, 1782), Hymenolepis citelli (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 Trichuris fossor 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 Thomomys talpoides: Versteria (syn. Taenia) mustelae (larvae) from the mesenteries, lungs, liver, and kidneys of gophers collected in northern and middle Alberta: Anoplocephaloides variabilis (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; Trichuris fossor from the cecum of gophers collected from central Alberta; Protospirura ascaroidea Hall, 1916 from the stomachs of gophers from middle Alberta; Litomosoides carinii (Travassos, 1919) from the coelom of pocket gophers from middle and southern Alberta. In the same year, Levine, et al. (1957) described Eimeria thomomysis from specimens of T. bottae collected in the Grand Canyon of Arizona.

Howard and Childs (1959) during a study of the ecology of Thomomys monticola reported Hymenolepis horrida (von Linstow, 1901) to occur commonly in adult pocket gophers. They stated, “Most of the adults had several tapeworms (Hymenolepis horrida), 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 Trichuris fossor Hall, 1916 and Ransomus rodentorum Hall, 1916 from Thomomys talpoides 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 Thomomys talpoides tenellus 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, Thomomys talpoides, and the Southern pocket gopher Thomomys umbrinus (Richardson, 1829). These species include Ascaris laevis Leidy, 1856, Hymenolepis citelli, Ransomus rodentorum, and Trichuris fossor. However, Anoplocephaloides infrequens (Douthitt, 1915), A. variabilis (Douthitt, 1915), Pseudocittotaenia praecoquis (Stiles, 1985), Arostrilepis horrida, and Nippostrongylus muris (Yokogawa, 1920) have been reported from T. talpoides. In addition, Paruterina candelabraria (Goeze, 1781) and Moniliformis clarki are only reported from T. umbrinus.

Stock (1962) reported three males and one female of the nematode Ransomus rodentorum from the cecae of two specimens of Thomomys talpoides fossor, 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, Geomys bursarius, collected from Clay County, South Dakota.

Ubelaker and Downhower (1965) in a study of the endo and ectoparasites of Geomys bursarius in Kansas, reported Calodium (syn. Capillaria) hepaticum from the cecum of a single pocket gopher and Andrya macrocephala Douthitt, 1915 and Anoplocephaloides infrequens (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 (Eimeria orthogeomyos) was described from the Giant pocket gopher, Orthogeomys grandis (Thomas, 1893) collected from Baking Pot, El Cayo District, Central America (Lainson, 1968).

Tryon and Cunningham (1968) in a study of Thomomys talpoides 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 Trichuris fossor Hall, 1916 and Cuterebra cf. cyanella (bot fly larvae) from Thomomys bottae aureus Douglas (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 Eimeria fitzgeraldi Todd & Tryon, 1970 from Thomomys talpoides 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 (Thomomys talpoides) from Park County, Wyoming, reported the following species of parasites from a total of 46 specimens of T. talpoides examined: Eimeria thomomysis 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 Catenotaenia linsdalei McIntosh, 1941 were found in the body cavities of two animals (this is a dubious body location record); Anoplocephaloides variabilis (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; Vexillata vexillata was recovered from the small intestines of two gophers; Protospirura ascaroidea was found in the stomachs of two animals; Trichuris fossor 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 Trichuris fossor 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 Thomomys talpoides in Utah: Trichuris fossor, Vexillata vexillata, Ascaris laevis Leidy, 1856. Hymenolepis horrida, 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 Anoplocephaloides infrequens (Douthitt, 1915) from Geomys bursarius collected by Douthitt in Brainerd, Minnesota, and specimens of A. variabilis (Douthitt, 1915) collected by Douthitt in central Illinois from Geomys bursarius. Also studied by Rausch (1976) were seven specimens of A. variabilis from Thomomys talpoides 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 Thomomys talpoides 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 Pseudocittotaenia praecoquis (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 Pseudocittotaenia praecoquis from T. talpoides tenellus 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 Thomomys bottae (Eydoux & Gervais): Ransomus rodentorum, Trichuris fossor, Hymenolepis citelli, 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 Heligmosomoides thomomyos Gardner & Jasmer, 1983 from Thomomys bottae (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 Hymenolepis tualatinensis from the duodenum of the Camas pocket gopher, Thomomys bulbivorus (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 Arostrilepis horrida also from the small intestine, Trichuris fossor from the cecum, Ransomus rodentorum from the cecum, and Heligmosomoides thomomyos from the duodenum.

Gardner and Schmidt (1986) described Litomosoides thomomydis from the abdominal cavity of the Northern pocket gopher, Thomomys talpoides, and Botta’s pocket gopher, Thomomys bottae, from Huerfano County, Colorado. Also, L. westi was described from the abdominal and pleural cavities of the Plains Pocket Gopher, Geomys bursarius, 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, Geomys bursarius, collected from Weld County, Colorado.

Pitts et al. (1990) reported Litomosoides westi Gardner & Schmidt, 1986 from Geomys personatus True, 1889 collected from Duval and Zapata counties in Texas.

Upton et al. (1992) reported Eimeria geomydis Skidmore, 1929 from Baird’s pocket gopher, Geomys mericanu, and Llano pocket gopher, Geomys texensis Merriam, 1895 collected from Texas.

Dronen et al. (1994) described Monoecocestus centroovarium found in Attwater’s pocket gopher, Geomys attwateri Merriam, 1895 collected from Atascosa County, Texas. In the same year, Wilber et al. (1994) described Eimeria jemezi found in the Northern pocket gopher, Thomomys talpoides collected from El Cajete crater, Jemez Springs, Sandoval County, New Mexico.

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

Pitts et al. (2000) reported the additional occurrence of the filarioid nematode, Litomosoides westi from the pleural cavities of Baird’s pocket gopher, Geomys mericanu 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, Geomys bursarius captured near Aubrey, Grubbs Road, same county.

Bartel and Gardner (2000) reported the helminth parasites from the Plains pocket gopher, Geomys bursarius, from seven localities in the northern boundary range, Minnesota. The report includes the following: Physaloptera limbata Leidy, 1856 from the stomach, Ransomus rodentorum from the cecum and large intestine and Calodium (syn. Capillaria) mericanum (Read, 1949), Anoplocephaloides infrequens, A. variabilis (Douthitt, 1915), Andrya macrocephala, Hymenolepis weldensis Gardner & Schmidt, 1988 and Moniliformis clarki from the small intestines.

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

Using molecular methods, Haukisalmi et al. (2010) documented Hymenolepis weldensis from Geomys bursarius collected from Illinois and Indiana.

Makarikov et al. (2012) described Arostrilepis schilleri obtained from the Camas pocket gopher, Thomomys bulbivorus, 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, Geomys bursarius, 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, Protospirura ascaroidea, 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 Hobergia irazuensis from the small intestine of Heterogeomys heterodus (Peters, 1865), collected from Potrero Cerrado, Cartago, Costa Rica, and Hymenolepis cratogeomyos from the small intestine of the Volcán De Toluca pocket gopher, Cratogeomys planiceps (Merriam, 1895) collected from Parque Nacional Nevado de Toluca, México. Also, H. weldensis Gardner & Schmidt, 1988 has been documented from many individuals of Geomys lutescens 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, Cratogeomys castanops (Baird, 1852), collected by a local landowner from Black Mesa, Oklahoma in 2016 (NP2779). Anoplocephaloides variabilis (Douthitt, 1915) was found from the small intestine of Hall’s pocket gopher, Geomys jugossicularis Hooper, 1940 collected from Grama grass habitat, Keith County, Nebraska in 2016 (NP2661). Also, from 2009–2016, necropsies of Geomys lutescens Merriam, 1890 yielded many individuals of Litomosoides westi Gardner & Schmidt, 1986 from their abdominal cavities with individuals of Ransomus rodentorum from the cecum, and from two pocket gophers Physaloptera limbata 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, Thomomys clusius 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.

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
Ctenomys andersoni Gardner, et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys australis Rusconi, 1934 Pudica ctenomydis Rossin et al., 2006 Rossin et al. 2010a
Taenia talicei Dollfus, 1960 Rossin et al. 2010b
Trichuris pampeana Suriano & Navone, 1994 Rossin et al. 2010a
Ctenomys azarae Thomas, 1903 Trichuris pampeana Suriano & Navone, 1994 Suriano and Navone 1994; Rossin and Malizia 2005a
Ctenomys boliviensis Waterhouse, 1848 Ancylostoma ctenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Paraspidodera Travassos, 1914 Gardner et al. 2021
Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Ctenomys conoveri Osgood, 1946 Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys erikacuellarae Gardner et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys andersoni Gardner, et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys australis Rusconi, 1934 Pudica ctenomydis Rossin et al., 2006 Rossin et al. 2010a
Taenia talicei Dollfus, 1960 Rossin et al. 2010b
Trichuris pampeana Suriano & Navone, 1994 Rossin et al. 2010a
Ctenomys azarae Thomas, 1903 Trichuris pampeana Suriano & Navone, 1994 Suriano and Navone 1994; Rossin and Malizia 2005a
Ctenomys boliviensis Waterhouse, 1848 Ancylostoma ctenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Paraspidodera Travassos, 1914 Gardner et al. 2021
Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Ctenomys conoveri Osgood, 1946 Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys erikacuellarae Gardner et al., 2014 Paraspidodera Travassos, 1914 Gardner et al. 2021
Raillietina Fuhrman, 1920 Gardner et al. 2021
Ctenomys frater Thomas, 1902 Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys fulvus Philippi, 1860 Trichuris fulvi Babero & Murua, 1987 Babero and Murua 1987
Trichuris robusti Babero & Murua, 1990 Babero and Murua 1990
Ctenomys lewisi Thomas, 1926 Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys leucodon Waterhouse, 1848 Pudica pujoli Durette-Casset & Tcheprakoff, 1990 Gardner et al. 2021
Ctenomys magellanicus Bennett, 1836 Paraspidodera americana Khalil & Vogelsang, 1931 Khalil and Vogelsang 1931
Ctenomys maulinus Philippi, 1872 Monoecocestus torresi Olsen, 1976 Olsen 1976
Paraspidodera uncinata Rudolphi, 1819 Torres et al. 1976
Trichuris Roederer, 1761 Torres et al. 1976
Ctenomys nattereri Wagner, 1848 Paraspidodera Travassos, 1914 Gardner et al. 2021
Trichuris Roederer, 1761 Gardner et al. 2021
Ctenomys opimus Wagner, 1848 Eimeria granifera Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeria montuosi Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeria opimi Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Eimeria oruroensis Lambert et al., 1988 Lambert et al. 1988; Gardner and Duszynski 1990
Litomosoides andersoni Brant & Gardner, 1997 Brant and Gardner 1997
Litomosoides ctenomyos Brant & Gardner, 1997 Brant and Gardner 1997
Mathevotaenia Akhumyan, 1946 Gardner et al. 2021, 2023
Ctenomys pearsoni Lessa & Langguth, 1983 Strongyloides myopotami Artigas & Pacheco, 1933 Rossin et al. 2009
Ctenomys steinbachi Thomas, 1907 Ancylostoma ctenomyos Drabik & Gardner, 2019 Drabik and Gardner 2019
Eimeria opimi Lambert et al., 1988 Gardner and Duszynski 1990
Paraspidodera Travassos, 1914 Gardner et al. 2021
Ctenomys talarum Thomas, 1898 Graphidiodes subterraneus Rossin et al., 2005 Rossin et al. 2005b; Rossin et al. 2010b
Heligmostrongylus Travassos, 1917 Rossin and Malizia 2002
Paraspidodera uncinata Rudolphi, 1819 Rossin et al. 2004b; Rossin et al. 2010b
Pudica ctenomydis Rossin et al., 2006 Rossin et al. 2006a; Rossin et al. 2010b
Strongyloides myopotami Artigas & Pacheco, 1933 Rossin et al. 2010b; Rossin et al. 2009
Ctenomys talarum Thomas, 1898 Hydatigera (syn. Taenia) taeniaeformis Batsch, 1786 Rossin et al. 2004a
Taenia talicei Dollfus, 1960 Rossin et al. 2010a; Rossin et al. 2010b
Trichostrongylus duretteae Rossin et al., 2006 Rossin et al. 2006b; Rossin et al. 2010a
Trichuris Roederer, 1761 Rossin and Malizia 2002; Rossin and Malizia 2005a
Trichuris bursacaudata Suriano & Navone, 1994 Suriano and Navone 1994
Trichuris pampeana Suriano & Navone, 1994 Rossin et al. 2010a; Rossin and Malizia 2005a
Ctenomys torquatus Lichtenstein, 1830 Taenia talicei Dollfus, 1960 Dollfus 1960
Spalacopus cyanus (Molina, 1782) Graphidioides yañezi Babero & Cattan, 1980 Babero and Cattan 1980
Figure 4. 

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%).

Khalil and Vogelsang (1931) described the first helminth parasite from a subterranean host from Neotropical region, Paraspidodera americana Khalil & Vogelsang, 1931 from the cecum of a single individual of what they called Ctenomys magellanicus 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 Taenia talicei Dollfus, 1960 from the abdominal cavity of the Collared tuco-tuco, Ctenomys torquatus Lichtenstein, 1830, collected from Uruguay and in 1986, multistrobilate larvae of T. talicei were collected from several Ctenomys opimus 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 Monoecocestus torresi obtained from the small intestine of Maule’s tuco-tuco, Ctenomys maulinus Philippi, 1872 collected near Lonquimay, Chile. Meanwhile, Torres et al. (1976) reported Paraspidodera uncinata Rudolphi, 1819, and unidentified Trichuris are reported from Maule’s tuco-tuco, Ctenomys maulinus, collected from Chile.

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

Babero and Murua (1987) described a new species of whipworm, Trichuris fulvi obtained from the cecum of the Tawny tuco-tuco, Ctenomys fulvus 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, Ctenomys opimus 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 Trichuris robusti from the cecum and large intestine of the Tawny tuco-tuco, Ctenomys fulvus, collected from La Hauyca, Tarapaca province, Chile.

Gardner and Duszynski (1990), during a study on morphometric comparison of a coccidian species, Eimeria opimi Lambert 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, Ctenomys lewisi Thomas, 1926, collected from the areas of the high-altitude region in Tarija; the Reddish tuco-tuco, Ctenomys frater Thomas, 1902, collected from medium latitude region of Tarija; the Conover’s tuco-tuco, Ctenomys conoveri Osgood, 1946, collected from Chaco thorn forest area in Chuquisaca; the Bolivian tuco-tuco, Ctenomys boliviensis Waterhouse, 1848, and the Steinbach’s tuco-tuco, Ctenomys steinbachi 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, Ctenomys opimus. These species include Eimeria opimi, E. granifera Lambert et al., 1988, E. oruroensis Lambert et al., 1988, and E. montuosi Lambert et al., 1988 collected from the Oruro region E. opimi and E. granifera collected from the Potosi region.

Suriano and Navone (1994) described Trichuris bursacaudata obtained from the cecum of the Talas tuco-tuco, Ctenomys talarum Thomas, 1898 collected from Punta Indio, Buenos Aires, and T. pampeana found in the cecum of the Azara’s tuco-tuco, Ctenomys azarae 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 Litomosoides andersoni and L. ctenomyos from the abdominal and thoracic regions of the Highland tuco-tuco, Ctenomys opimus, 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, Ctenomys talarum, 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, Ctenomys talarum, 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 Paraspidodera uncinata (Rudolphi, 1819) from a large number of specimens obtained from the cecum and large intestine of the Talas tuco-tuco, Ctenomys talarum, collected from Mar de Cobo, Buenos Aires province, Argentina.

Rossin and Malizia (2005a) redescribed Trichuris pampeana Suriano & Navone, 1994 found in the cecum of the Azara’s tuco-tuco, Ctenomys azarae, 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 Graphidiodes subterraneus from the stomach of the Talas tuco-tuco, Ctenomys talarum, collected from Mar de Cobo, Partido de Mar Chiquita, Mar del Plata, Argentina.

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

Rossin et al. (2009) reported Strongyloides myopotami Artigas & Pacheco, 1933 found in the small intestines of the Talas tuco-tuco, Ctenomys talarum, collected from Mar de Cobo, Buenos Aires province, Argentina, and from Pearson’s tuco-tuco, Ctenomys pearsoni 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 Trichuris pampeana in the cecum, Pudica ctenomydis Rossin et al., 2006 in the small intestine, and larvae of Taenia talicei in the abdominal cavity. Moreover, C. talarum had four additional species of helminths, including Graphidiodes subterraneus Rossin et al., 2005 in the stomach, Paraspidodera uncinata in the large intestine, and Strongyloides myopotami and Trichostrongylus duretteae Rossin et al., 2006 in the small intestine.

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

From Bolivia, Drabik and Gardner (2019) described Ancylostoma ctenomyos Drabik & Gardner, 2019 from the small intestine of the Bolivian tuco-tuco, Ctenomys boliviensis 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, Ctenomys steinbachi 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, Ctenomys opimus, 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, Ctenomys andersoni Gardner et al., 2014, the Bolivian tuco-tuco or Cajuchi, Ctenomys boliviensis Waterhouse, 1848, Conover’s tuco-tuco, Ctenomys conoveri Osgood, 1946, Erica’s tuco-tuco, Ctenomys erikacuellarae Gardner et al., 2014, the little Andean forest tuco-tuco, Ctenomys frater Thomas, 1902, Lessa’s tuco-tuco, Ctenomys lessai Gardner et al., 2014, Lewis’s tuco-tuco, Ctenomys lewisi, Steinbach’s tuco-tuco, Ctenomys steinbachi, and Natterer’s tuco-tuco, Ctenomys nattereri 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, Ctenomys leucodon Waterhouse, 1848.

The present study reports that during a biodiversity survey in Bolivia in 1986, Pudica pujoli Durette-Desset & Tcheprakoff, 1990 was found in a single specimen of the White-toothed tuco-tuco, Ctenomys leucodon 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.

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