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Corresponding author: Scott L. Gardner ( slg@unl.edu ) Academic editor: David Gibson
© 2023 Altangerel T. Dursahinhan, Daniel A. Kenkel, Scott L. Gardner.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Dursahinhan AT, Kenkel DA, Gardner SL (2023) Helminth and protozoan parasites of subterranean rodents (Chordata, Mammalia, Rodentia) of the world. ZooKeys 1151: 159-203. https://doi.org/10.3897/zookeys.1151.97126
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Published studies and ten new unpublished records included herein reveal that approximately 174 species of endoparasites (helminths and protozoans) are known from 65 of 163 species of rodents that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.
Bathyergidae, Cricetidae, Ctenomyidae, Endoparasite, Geomyidae, Heterocephalidae, Octodontidae, Spalacidae
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 (
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 (
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 |
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 |
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 |
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 |
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 (
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
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 (
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 (
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 (
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.
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
Ethiopian subterranean rodent endoparasites
See graphical summary in Fig.
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) |
|
Ortleppstrongylus bathyergi Ortlepp, 1939 |
|
|
Paralibyostrongylus bathyergi (Ortlepp, 1939) |
|
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Rodentolepis Spasskii, 1954 |
|
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Taenia Linnaeus, 1758 |
|
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Trichostrongylus Looss, 1905 |
|
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Trichuris Roederer, 1761 |
|
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Cryptomys hottentotus (Lesson, 1826) | Ascarops africana (Sandground, 1933) |
|
Heligmonina Baylis, 1928 |
|
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Inermicapsifer madagascariensis (Davaine, 1870) |
|
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Mammalakis macrospiculum (Ortlepp, 1939) |
|
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Mathevotaenia Akhumyan, 1946 |
|
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Neoheligmonella Durette-Desset, 1971 |
|
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Protospirura Seurat, 1914 |
|
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Raillietina Fuhrman, 1920 |
|
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Trichuris Roederer, 1761 |
|
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Fukomys anselli (Burda et al., 1999) | Hexametra Travassos, 1920 |
|
Inermicapsifer Janicki, 1910 |
|
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Mammalakis zambiensis |
|
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Protospirura muricola (Gedoelst, 1916) |
|
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Protospirura numidica Seurat, 1914 |
|
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Protospirura Seurat, 1914 |
|
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Rodentolepis cf. microstoma (Dujardin, 1945) |
|
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Fukomys kafuensis (Burda et al., 1999) | Inermicapsifer madagascariensis (Davaine, 1870) |
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Protospirura muricola (Gedoelst, 1916) |
|
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Fukomys mechowii (Peters, 1881) | Capillaria Zeder, 1800 |
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Inermicapsifer madagascariensis (Davaine, 1870) |
|
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Protospirura muricola (Gedoelst, 1916) |
|
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Raillietina Fuhrman, 1920 |
|
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Georychus capensis (Pallas, 1778) | Coenurus spalacis Diesing, 1864 |
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Echinococcus Rudolphi, 1801 |
|
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Trichuris Roederer, 1761 |
|
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Heliophobius argenteocinereus Peters, 1846 |
Eimeria burdai |
|
Eimeria heliophobii |
|
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Eimeria nafuko |
|
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Eimeria yamikamiae |
|
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Inermicapsifer arvicanthidis (Kofend, 1917) |
|
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Protospirura muricola (Gedoelst, 1916) |
|
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Heterocephalus glaber Rüppell, 1842 | Eimeria heterocephali Levine & Ivens, 1965 |
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Tachyoryctes splendens (Rüppell, 1835) | Taenia brauni Setti, 1897 |
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Tachyoryctes macrocephalus (Rüppell, 1842) | Ascarops africana (Sandground, 1933) |
|
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%).
Several years later,
Just one year later,
See graphical summary in Fig.
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) |
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Ellobius fuscocapillus (Blyth, 1843) | Syphacia obvelata (Rudolphi, 1802) |
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Ellobius lutescens Thomas, 1897 | Eimeria lutescenae Musaev & Veisov, 1963 |
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Ellobius talpinus (Pallas, 1770) | Aprostatandrya macrocephala Douthitt, 1915 |
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Catenotaenia pusilla Goeze, 1782 |
|
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Echinococcus multilocularis Leuckart, 1863 |
|
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Eimeria ellobii Svanbaev, 1965 |
|
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Eimeria kazakhstanensis Levine, 1965 |
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Eimeria tadshikistanica Veisov, 1964 |
|
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Eimeria talpini Levine, 1965 |
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Hymenolepis diminuta (Rudolphi, 1819) |
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Mesocestoides Vaillant, 1863 |
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Moniliformis moniliformis Bremser, 1811 |
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Nomadolepis ellobii |
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Physocephalus ellobii Schulz, 1927 |
|
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Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) |
|
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Ellobius tancrei Blasius, 1884 |
Arostrilepis batsaikhani |
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Echinococcus multilocularis Leuckart, 1863 |
|
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Eospalax baileyi (Thomas, 1911) |
Eimeria baileyii |
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Eimeria fani |
|
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Eimeria menyuanensis |
|
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Eimeria myospalacensis |
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Ransomus qinghaiensis |
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Versteria (syn. Taenia) mustelae Gmelin, 1790 |
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Eospalax fontanierii (Milne-Edwards, 1867) | Echinococcus multilocularis Leuckart, 1863 |
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Heligmoptera giraudouxi |
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Heligmoptera querei |
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Myospalax myospalax (Laxmann, 1773) | Echinococcus multilocularis Leuckart, 1863 |
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Heligmoptera sibirica Shakhmatova, 1990 |
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Heligmosomum myospalaxi Nadtochii, 1970 |
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Hymenolepis rymzhanovi Makarikov & Tkach, 2013 |
|
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Moniliformis clarki (Ward, 1917) |
|
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Paranoplocephala Lühe, 1910 |
|
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Versteria mustelae (Gmelin, 1790) |
|
|
Myospalax psilurus (Milne-Edwards, 1874) | Ascarops strongylina (Rudolphi, 1819) |
|
Nannospalax ehrenbergi Nehring, 1898 | Eimeria adiyamanensis Sayin, 1980 |
|
Eimeria anzanensis |
|
|
Eimeria carmelensis |
|
|
Eimeria celebii Sayin, 1980 |
|
|
Eimeria haranica Sayin, 1980 |
|
|
Eimeria marasensis Sayin, 1980 |
|
|
Eimeria microspalacis Golemansky & Darawish, 1992 |
|
|
Eimeria oytuni Sayin, 1980 |
|
|
Eimeria spalacensis |
|
|
Eimeria torosicum Sayin, 1980 |
|
|
Eimeria urfensis Sayin, 1980 |
|
|
Ganguleterakis spalaxi Kozlov & Yangolenko, 1963 |
|
|
Gongylonema longispiculum Schulz, 1927 |
|
|
Heligmonella Mönnig, 1927 |
|
|
Heligmonina nevoi Wertheim & Nevo, 1971 |
|
|
Isospora spalacensis |
|
|
Microcephaloides nevoi ( |
|
|
Trichuris muris (Schrank, 1788) |
|
|
Nannospalax leucodon (Nordmann, 1840) | Aprostatandrya Kirshenblat, 1938 |
|
Ascaris spalacis Shults & Aloyan, 1950 | Shults and Aloyan 1950 | |
Coenurus parviuncinatus Kirschenblatt, 1939 |
|
|
Eimeria celebii Sayin, 1980 |
|
|
Eimeria elliptica |
|
|
Eimeria lalahanensis |
|
|
Eimeria leucodonica Veisov, 1975 |
|
|
Eimeria maralikiensis Veisov, 1975 |
|
|
Eimeria oytuni Sayin, 1980 |
|
|
Eimeria spalacis |
|
|
Eimeria talikiensis Veisov, 1975 |
|
|
Eimeria torosicum Sayin, 1980 |
|
|
Eimeria turkmenica |
|
|
Eimeria tuzdili |
|
|
Heligmosomum spalacis Kirsenblat, 1965 |
|
|
Heligmosomum moldovensis Andreiko, 1963 |
|
|
Isospora anatolicum |
|
|
Longistriata spalacis Sharpilo, 1973 |
|
|
Mammalakis spalacis Marcu, 1930 |
|
|
Moniliformis moniliformis Bremser, 1811 |
|
|
Taenia straminea (Goeze, 1782) Spasskii 1954 |
|
|
Prometheomys schaposchnikowi Satunin, 1901 | Dicrocoelium dendriticum (Rudolphi, 1819) |
|
Heligmosomum halli (Schulz, 1926) |
|
|
Microcephaloides Haukisalmi et al., 2008 |
|
|
Taenia polyacantha Leuckart, 1856 |
|
|
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) |
|
|
Rhizomys pruinosus (Blyth, 1851) | Mammalakis spumosa (Schneider, 1866) |
|
Rhizomys sinensis Gray, 1831 | Cryptosporidium occultus Kváč, 2018 |
|
Cryptosporidium parvum Tyzzer, 1912 |
|
|
Spalax arenarius Reshetnik, 1939 | Longistriata spalacis Sharpilo, 1973 |
|
Spalax graecus Nehring, 1898 | Heligmosomum spalacis Kirsenblat, 1965 |
|
Spalax microphthalmus Güldenstädt, 1770 | Ganguleterakis spalaxi Kozlov & Yangolenko, 1963 |
|
Gongylonema longispiculum spalacis Schulz, 1927 |
|
|
Longistriata spalacis Sharpilo, 1973 |
|
|
Mammalakis spalacis Marcu, 1930 |
|
|
Hydatigera (syn. Taenia) taeniaeformis (Batsch, 1786) |
|
|
Trichuris spalacis (Petrov & Potechina, 1953) |
|
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
Somewhat later,
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.
More recently in China,
Soon after,
In 2017, a flurry of activity resulted from workers in the field.
See graphical summary in Fig.
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 |
|
Vexillata convoluta Caballero & Cerecero, 1943 |
|
|
Cratogeomys planiceps (Merriam, 1895) |
Hymenolepis cratogeomyos |
|
Geomys attwateri Merriam, 1895 |
Monoecocestus centroovarium |
|
Protospirura ascaroidea Hall, 1916 |
|
|
Vexillata geomyos |
|
|
Geomys breviceps Baird, 1855 | Eimeria geomydis Skidmore, 1929 |
|
Litomosoides westi Gardner & Schmidt, 1986 |
|
|
Monoecocestus anoplocephaloides (Douthitt, 1915) |
|
|
Protospirura ascaroidea Hall, 1916 |
|
|
Geomys bursarius (Shaw, 1800) | Andrya macrocephala Douthitt, 1915 |
|
Anoplocephaloides infrequens (Douthitt, 1915) |
|
|
Anoplocephaloides variabilis (Douthitt, 1915) |
|
|
Calodium americanum (Read, 1949) |
|
|
Calodium hepaticum (Bancroft, 1893) |
|
|
Cittotaenia perplexa Stiles, 1897 |
|
|
Eimeria geomydis Skidmore, 1929 |
|
|
Hymenolepis diminuta (Rudolphi, 1819) |
|
|
Hymenolepis geomydis Gardner & Schmidt, 1988 |
|
|
Hymenolepis weldensis Gardner & Schmidt, 1988 |
|
|
Litomosa filaria (Beneden, 1873) |
|
|
Litomosoides westi Gardner & Schmidt, 1986 | |
|
Moniliformis clarki (Ward, 1917) |
|
|
Monocercomonoides Travis, 1932 |
|
|
Monoecocestus anoplocephaloides (Douthitt, 1915) |
|
|
Oochoristica Lűhe, 1898 |
|
|
Ostertagia Ransom, 1907 |
|
|
Paranoplocephala infrequens (Douthitt, 1915) |
|
|
Physaloptera limbata Leidy, 1856 |
|
|
Protospirura ascaroidea Hall, 1916 |
|
|
Protospirura muris ascaroides (Hall, 1916) |
|
|
Pseudocittotaenia praecoquis (Stiles, 1985) |
|
|
Ransomus rodentorum Hall, 1916 |
|
|
Geomys jugossicularis Hooper, 1940 | Anoplocephaloides variabilis (Douthitt, 1915) | Present study |
Geomys lutescens Merriam, 1890 | Hymenolepis weldensis Gardner & Schmidt, 1988 |
|
Litomosoides westi Gardner & Schmidt, 1986 | Present study | |
Physaloptera limbata Leidy, 1856 | Present study | |
Ransomus rodentorum Hall, 1916 | Present study | |
Monoecocestus anoplocephaloides (Douthitt, 1915) |
|
|
Geomys personatus True, 1889 | Litomosoides westi Gardner & Schmidt, 1986 |
|
Protospirura ascaroidea Hall, 1916 |
|
|
Geomys pinetis Rafinesque, 1817 | Mastophorus muris ascaroides (Gmelin, 1790) |
|
Geomys texensis Merriam, 1895 | Eimeria geomydis Skidmore, 1929 |
|
Hymenolepis Weinland, 1858 |
|
|
Protospirura ascaroidea Hall, 1916 |
|
|
Heterogeomys heterodus (Peter, 1865) |
Hobergia irazuensis |
|
Orthogeomys grandis (Thomas, 1893) | Eimeria orthogeomys Lainson, 1968 |
|
Thomomys bottae (Eydoux & Gervais, 1836) | Arostrilepis horrida (von Linstow, 1901) |
|
Catenotaenia dendritica (Goeze, 1782) |
|
|
Catenotaenia linsdalei McIntosh, 1941 |
|
|
Eimeria thomomysis |
|
|
Heligmosomoides thomomyos Gardner & Jasmer, 1983 |
|
|
Hymenolepis citelli (McLeod, 1933) |
|
|
Litomosoides thomomydis Gardner, 1986 |
|
|
Monocercomonoides Travis, 1932 |
|
|
Monoecocestus anoplocephaloides (Douthitt, 1915) |
|
|
Ransomus rodentorum Hall, 1916 |
|
|
Trichuris fossor Hall, 1916 |
|
|
Thomomys bulbivorus (Richardson, 1829) | Arostrilepis horrida (von Linstow, 1901) |
|
Arostrilepis schilleri |
|
|
Heligmosomoides thomomyos Gardner & Jasmer, 1983 |
|
|
Hymenolepis tualatinensis Gardner, 1985 |
|
|
Ransomus rodentorum Hall, 1916 |
|
|
Trichuris fossor Hall, 1916 |
|
|
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) |
|
Trichuris Roederer, 1761 |
|
|
Thomomys talpoides (Richardson, 1828) | Andrya macrocephala Douthitt, 1915 |
|
Anoplocephaloides infrequens (Douthitt, 1915) |
|
|
Anoplocephaloides variabilis (Douthitt, 1915) |
|
|
Arostrilepis horrida (von Linstow, 1901) |
|
|
Ascaris laevis Leidy, 1856 |
|
|
Calodium hepaticum (Bancroft, 1893) |
|
|
Catenotaenia linsdalei McIntosh, 1941 |
|
|
Eimeria fitzgeraldi Todd & Tryon, 1970 |
|
|
Eimeria jemezi |
|
|
Eimeria thomomysis |
|
|
Hymenandrya thomomyis Smith, 1954 |
|
|
Hymenolepis citelli (McLeod, 1933) |
|
|
Hymenolepis diminuta (Rudolphi, 1819) |
|
|
Litomosoides carinii (Travassos, 1919) |
|
|
Litomosoides thomomydis Gardner, 1986 | Gardner and |
|
Nippostrongylus muris (Yokogawa, 1920) |
|
|
Protospirura ascaroidea Hall, 1916 |
|
|
Pseudocittotaenia glandularis Beveridge, 1978 |
|
|
Pseudocittotaenia praecoquis (Stiles, 1985) |
|
|
Ransomus rodentorum Hall, 1916 |
|
|
Trichuris fossor Hall, 1916 |
|
|
Versteria mustelae (Gmelin, 1790) |
|
|
Vexillata vexillata (Hall, 1916) |
|
|
Thomomys umbrinus (Richardson, 1829) | Arostrilepis horrida (von Linstow, 1901) |
|
Ascaris laevis Leidy, 1856 |
|
|
Hymenolepis citelli (McLeod, 1933) |
|
|
Moniliformis clarki (Ward, 1917) |
|
|
Paruterina candelabraria (Goeze, 1782) |
|
|
Ransomus rodentorum Hall, 1916 |
|
|
Trichuris fossor Hall, 1916 |
|
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
Soon after,
The next year,
Gardner and
Shortly after this work,
Using molecular methods,
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.
See graphical summary in Fig.
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 |
Paraspidodera Travassos, 1914 |
|
Ctenomys australis Rusconi, 1934 | Pudica ctenomydis Rossin et al., 2006 |
|
Taenia talicei Dollfus, 1960 |
|
|
Trichuris pampeana Suriano & Navone, 1994 |
|
|
Ctenomys azarae Thomas, 1903 | Trichuris pampeana Suriano & Navone, 1994 |
|
Ctenomys boliviensis Waterhouse, 1848 | Ancylostoma ctenomyos Drabik & Gardner, 2019 |
|
Paraspidodera Travassos, 1914 |
|
|
Eimeria opimi |
|
|
Ctenomys conoveri Osgood, 1946 |
Eimeria opimi |
|
Paraspidodera Travassos, 1914 |
|
|
Ctenomys erikacuellarae |
Paraspidodera Travassos, 1914 |
|
Ctenomys andersoni |
Paraspidodera Travassos, 1914 |
|
Ctenomys australis Rusconi, 1934 | Pudica ctenomydis Rossin et al., 2006 |
|
Taenia talicei Dollfus, 1960 |
|
|
Trichuris pampeana Suriano & Navone, 1994 |
|
|
Ctenomys azarae Thomas, 1903 | Trichuris pampeana Suriano & Navone, 1994 |
|
Ctenomys boliviensis Waterhouse, 1848 | Ancylostoma ctenomyos Drabik & Gardner, 2019 |
|
Paraspidodera Travassos, 1914 |
|
|
Eimeria opimi |
|
|
Ctenomys conoveri Osgood, 1946 |
Eimeria opimi |
|
Paraspidodera Travassos, 1914 |
|
|
Ctenomys erikacuellarae |
Paraspidodera Travassos, 1914 |
|
Raillietina Fuhrman, 1920 |
|
|
Ctenomys frater Thomas, 1902 |
Eimeria opimi |
|
Paraspidodera Travassos, 1914 |
|
|
Ctenomys fulvus Philippi, 1860 | Trichuris fulvi Babero & Murua, 1987 |
|
Trichuris robusti Babero & Murua, 1990 |
|
|
Ctenomys lewisi Thomas, 1926 |
Eimeria opimi |
|
Paraspidodera Travassos, 1914 |
|
|
Ctenomys leucodon Waterhouse, 1848 | Pudica pujoli Durette-Casset & Tcheprakoff, 1990 |
|
Ctenomys magellanicus Bennett, 1836 | Paraspidodera americana Khalil & Vogelsang, 1931 |
|
Ctenomys maulinus Philippi, 1872 | Monoecocestus torresi Olsen, 1976 |
|
Paraspidodera uncinata Rudolphi, 1819 |
|
|
Trichuris Roederer, 1761 |
|
|
Ctenomys nattereri Wagner, 1848 | Paraspidodera Travassos, 1914 |
|
Trichuris Roederer, 1761 |
|
|
Ctenomys opimus Wagner, 1848 |
Eimeria granifera |
|
Eimeria montuosi |
|
|
Eimeria opimi |
|
|
Eimeria oruroensis |
|
|
Litomosoides andersoni Brant & Gardner, 1997 |
|
|
Litomosoides ctenomyos Brant & Gardner, 1997 |
|
|
Mathevotaenia Akhumyan, 1946 |
|
|
Ctenomys pearsoni Lessa & Langguth, 1983 | Strongyloides myopotami Artigas & Pacheco, 1933 |
|
Ctenomys steinbachi Thomas, 1907 | Ancylostoma ctenomyos Drabik & Gardner, 2019 |
|
Eimeria opimi |
|
|
Paraspidodera Travassos, 1914 |
|
|
Ctenomys talarum Thomas, 1898 | Graphidiodes subterraneus Rossin et al., 2005 |
|
Heligmostrongylus Travassos, 1917 |
|
|
Paraspidodera uncinata Rudolphi, 1819 |
|
|
Pudica ctenomydis Rossin et al., 2006 |
|
|
Strongyloides myopotami Artigas & Pacheco, 1933 |
|
|
Ctenomys talarum Thomas, 1898 | Hydatigera (syn. Taenia) taeniaeformis Batsch, 1786 |
|
Taenia talicei Dollfus, 1960 |
|
|
Trichostrongylus duretteae Rossin et al., 2006 |
|
|
Trichuris Roederer, 1761 |
|
|
Trichuris bursacaudata Suriano & Navone, 1994 |
|
|
Trichuris pampeana Suriano & Navone, 1994 |
|
|
Ctenomys torquatus Lichtenstein, 1830 | Taenia talicei Dollfus, 1960 |
|
Spalacopus cyanus (Molina, 1782) | Graphidioides yañezi Babero & Cattan, 1980 |
|
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%).
Continuing work on tucos,
During an ecological study of helminth parasite infection parameters in two species of South American subterranean rodents of the genus Ctenomys,
From Bolivia,
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.
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.