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

Published studies and ten new unpublished records included herein reveal that approximately 174 species of endoparasites (helminths and protozoans) are known from 65 of 163 species of rodents that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.

Tapping into natural history collections to assess latitudinal gradients of parasite diversity.

Parasites are key components of the biosphere not only due to their huge diversity, but also because they exert important influences on ecological processes. Nevertheless, we lack an understanding of the biogeographical patterns of parasite diversity. Here, we tap into the potential of biodiversity collections for understanding parasite biogeography. We assess species richness of supracommunities of helminth parasites infecting mammal assemblages in the Nearctic, and describe its relation to latitude, climate, host diversity, and land area. We compiled data from parasitology collections and assessed parasite diversity in Nearctic ecoregions for the entire parasite supracommunity of mammals in each ecoregion, as well as separately from carnivores and rodents to explore the effect of host taxonomic resolution on observed patterns. For carnivores, we found evidence of a negative latitudinal gradient, while parasites of rodents displayed no clear pattern. We found that parasite diversity was positively correlated with mean annual temperature and negatively correlated with seasonal precipitation. Parasite richness shows a diversity peak at intermediate host richness values and in carnivores correlates with temperature and seasonal precipitation. Rodent parasite diversity did not correlate with explored factors. Other researchers are encouraged to use parasitology collections to continue exploring patterns of parasite biogeography and macroecology.

Intercontinental comparisons of subterranean host-parasite communities using bipartite network analyses.

Rodents living in a subterranean ecotope face a unique combination of evolutionary and ecological pressures and while host species evolution may be driven by the selective pressure from the parasites they harbour, the parasites may be responding to the selective pressures of the host. Here, we obtained all available subterranean rodent host­parasite records from the literature and integrated these data by utilizing a bipartite network analysis to determine multiple critical parameters to quantify and measure the structure and interactions of the organisms present in host­parasite communities. A total of 163 species of subterranean rodent hosts, 174 parasite species and 282 interactions were used to create 4 networks with data well-represented from all habitable continents. The results show that there was no single species of parasite that infects subterranean rodents throughout all zoogeographical regions. Nevertheless, species representing the genera Eimeria and Trichuris were common across all communities of subterranean rodents studied. Based on our analysis of host­parasite interactions across all communities studied, the parasite linkages show that community connectance (due to climate change or other anthropogenic factors) appears to show degraded linkages in both the Nearctic and Ethiopian regions: in this case parasites are acting as bell-weather probes signalling the loss of biodiversity.

HOST-SWITCHING EVENTS IN LITOMOSOIDES CHANDLER, 1931 (FILARIOIDEA: ONCHOCERCIDAE) ARE NOT RAMPANT BUT CLADE DEPENDENT.

The genus Litomosoides Chandler, 1931, includes species that as adults occur in the thoracic and abdominal cavity of mammalian hosts and are presumably vectored by mites. The vertebrate hosts include a variety of Neotropical mammals such as phyllostomid and mormoopid bats; cricetid, sciurid, and hystricognath rodents; and didelphid marsupials. It has been suggested that Litomosoides is not a monophyletic group and that rampant horizontal transfer explains their presence in disparate groups of mammals. Herein we present a phylogenetic reconstruction including mitochondrial genes of 13 vouchered species. This phylogeny is used to reconstruct the evolutionary history of these parasites and the ancestral states of key characters used in species classification, namely, the configuration of the spicules. The historical association of these filarioids with 6 groups of mammals, as well as their ancestral geographic distributions, were reconstructed using Bayesian statistical approaches comparing alternative models of biogeography and evolution and fossil states in selected nodes of the phylogeny. The optimal reconstruction suggests a model of dispersal, extinction, and cladogenesis (DEC) driving the evolution of Litomosoides; the results suggest an origin of Litomosoides in South America and association of ancestors with phyllostomids, and strong evidence of at least 2 host-switching events: 1 of these involving cricetid rodents and the other mormoopid bats. The latter event included a simultaneous geographic expansion of the parasite lineage across South and North America. The host-switching event from phyllostomid bats into cricetid rodents occurred once these rodents diversified across South America; subsequent diversification of the latter clade resulted in 2 branches, each showing expansion of the parasites back into North America. This result suggests that both parasites and cricetid rodents established an association in South America, underwent diversification, and then dispersed into North America. Further, this clade of cricetid-dwelling species includes parasites featuring the "sigmodontis" spicule type. The identification of a single host-switching event involving the disparate lineages of Chiroptera and Rodentia offers a framework to reconstruct the gene evolution and diversification of this lineage after the host-switching event. This will help in predicting the ability of these parasites to infect sympatric mammals.

A new genus and two new species of unarmed hymenolepidid cestodes (Cestoda: Hymenolepididae) from geomyid rodents in Mexico and Costa Rica.

Two new cestodes of the family Hymenolepididae are described from two species of rodents of the family Geomyidae collected in Mexico and Costa Rica. One new species of Hymenolepis is described from Cratogeomys planiceps Merriam 1895 from near Toluca, Mexico and another that we allocate to a new genus is described from Heterogeomys heterodus (Peters, 1865) from near Irazú Volcano, Costa Rica. Hymenolepis s. str. includes those Hymenolepididae with an apical organ, with no hooks on suckers or apical organ, and three testes. Hobergia irazuensis n. gen., n. sp. includes a hymenolepidid with an apical organ, unarmed scolex, small pockets termed foveolae, in which the suckers completely retract, and extremely bi-lobed ovary. Multivariate morphometric analysis showed good separation of these species from all other hymenolepidids possessing an apical organ and lacking a well developed rostellum and rostellar hooks in the Nearctic and Neotropical regions.

Host relationships and geographic distribution of species of Acanthobothrium Blanchard, 1848 (Onchoproteocephalidea, Onchobothriidae) in elasmobranchs: a metadata analysis.

Species of Acanthobothrium have been documented as parasites of the spiral intestine of elasmobranchs. Results of a metadata analysis indicate that 114 species of elasmobranchs have been reported as hosts of 200 species of Acanthobothrium. The metadata analysis revealed that 3.7% of species of sharks and 14.9% of species of rays that have been reported as hosts to date; some species are parasitized by more than one species of Acanthobothrium. This work provides a Category designation, as proposed by Ghoshroy and Caira (2001), for each species of Acanthobothrium. These Category designations are a tool to facilitate comparisons among members of Acanthobothrium for descriptions of new species in the future.

Gaharitrema droneni n. gen., n. sp. (Digenea: Zoogonidae) from the Pudgy Cuskeel, Spectrunculus grandis (Ophidiiformes: Ophidiidae), from Deep Waters Off Oregon, with Updated Keys to Zoogonid Subfamilies and Genera.

Gaharitrema droneni n. gen., n. sp. (Digenea: Zoogonidae: Lepidophyllinae) is described from the intestine of the pudgy cuskeel, Spectrunculus grandis (Günther, 1877) (Ophidiiformes: Ophidiidae), collected at 2,800 m depth from the northeastern Pacific Ocean off Oregon. The new genus is distinguished from BrachyenteronManter, 1934 and SteganodermaStafford, 1904, the 2 closest lepidophylline genera, and from 4 other zoogonid genera erected since 2007, the last major revision of the family, by a combination of diagnostic features including a pyriform or spindle-shaped body, smooth testes and ovary, narrow ceca that reach with the vitellarium into the hindbody, an unspecialized ventral sucker, non-filamented eggs, a claviform cirrus pouch, and an unpocketed ejaculatory duct and metraterm, and the new genus lacks circumoral spines. We present updated keys to the 3 subfamilies of the Zoogonidae Odhner, 1902, as well as to the genera of the Cephaloporinae Yamaguti, 1934 and the Lepidophyllinae Stossich, 1903. A listing of the parasites known from S. grandis also is presented. This study documents the third family of digeneans (Zoogonidae) known to parasitize S. grandis, and it is a new host record (i.e., the first zoogonid reported from this host species). We discuss the relatively impressive presence of the Zoogonidae and their hosts within the deep sea. Specifically, of the 35 genera we recognize within this digenean family, 14 (40%) have deep-sea representatives. At least 37 species within 27 genera and 19 families within 11 orders of deep-sea fish are known to harbor zoogonids. Furthermore, of the 37 known deep-sea fish species parasitized by zoogonids, only 5 (13.5%) harbor 2 or more zoogonid species; the remaining 32 (86.5%) harbor only 1 parasite species each, indicating strong host specificity. Finally, the dietary ecology of S. grandis is presented, allowing us to speculate that Gaharitrema droneni may be utilizing gastropods and polychaetes as well as S. grandis to complete its life cycle in the deep sea.

A New Species of Ancylostoma (Nemata: Strongylida: Ancylostomatidae) from Two Species of Ctenomys in Lowland Bolivia.

From the small intestines of both Ctenomys boliviensis and Ctenomys steinbachi collected from August 1984 through June 1990 from the eastern lowlands of the Department of Santa Cruz, Bolivia a total of 36 specimens of Ancylostoma were recovered. Morphological investigation and comparisons with known species described and reported from mammals in the Neotropical Region show that this is an undescribed species, herein described as new. These nematans were collected from individuals of C. steinbachi collected from near a locality called Caranda (northwest of Santa Cruz de la Sierra) and from C. boliviensis from near Santa Rosa de la Roca (northeast of Santa Cruz de la Sierra) and from cajuchis collected from 3 km west of Estación El Pailón, 30 km east of Santa Cruz de la Sierra. The new species of Ancylostoma differs from all other species of Ancylostoma known from the Neotropical Region in the presence of paired sub-terminal papillae on the dorsal ray of males.

Building an integrated infrastructure for exploring biodiversity: field collections and archives of mammals and parasites.

Museum specimens play an increasingly important role in predicting the outcomes and revealing the consequences of anthropogenically driven disruption of the biosphere. As ecological communities respond to ongoing environmental change, host-parasite interactions are also altered. This shifting landscape of host-parasite associations creates opportunities for colonization of different hosts and emergence of new pathogens, with implications for wildlife conservation and management, public health, and other societal concerns. Integrated archives that document and preserve mammal specimens along with their communities of associated parasites and ancillary data provide a powerful resource for investigating, anticipating, and mitigating the epidemiological, ecological, and evolutionary impacts of environmental perturbation. Mammalogists who collect and archive mammal specimens have a unique opportunity to expand the scope and impact of their field work by collecting the parasites that are associated with their study organisms. We encourage mammalogists to embrace an integrated and holistic sampling paradigm and advocate for this to become standard practice for museum-based collecting. To this end, we provide a detailed, field-tested protocol to give mammalogists the tools to collect and preserve host and parasite materials that are of high quality and suitable for a range of potential downstream analyses (e.g., genetic, morphological). Finally, we also encourage increased global cooperation across taxonomic disciplines to build an integrated series of baselines and snapshots of the changing biosphere. Los especímenes de museo desempeñan un papel cada vez más importante tanto en la descripción de los resultados de la alteración antropogénica de la biosfera como en la predicción de sus consecuencias. Dado que las comunidades ecológicas responden al cambio ambiental, también se alteran las interacciones hospedador-parásito. Este panorama cambiante de asociaciones hospedador-parásito crea oportunidades para la colonización de diferentes hospedadores y para la aparición de nuevos patógenos, con implicancias en la conservación y manejo de la vida silvestre, la salud pública y otras preocupaciones de importancia para la sociedad. Archivos integrados que documentan y preservan especímenes de mamíferos junto con sus comunidades de parásitos y datos asociados, proporcionan un fuerte recurso para investigar, anticipar y mitigar los impactos epidemiológicos, ecológicos y evolutivos de las perturbaciones ambientales. Los mastozoólogos que recolectan y archivan muestras de mamíferos, tienen una oportunidad única de ampliar el alcance e impacto de su trabajo de campo mediante la recolección de los parásitos que están asociados con los organismos que estudian. Alentamos a los mastozoólogos a adoptar un paradigma de muestreo integrado y holístico y abogamos para que esto se convierta en una práctica estándarizada de la obtención de muestras para museos. Con este objetivo, proporcionamos un protocolo detallado y probado en el campo para brindar a los mastozoólogos las herramientas para recolectar y preservar materiales de parásitos y hospedadores de alta calidad y adecuados para una gran variedad de análisis subsecuentes (e.g., genéticos, morfológicos, etc.). Finalmente, también abogamos por una mayor cooperación global entre las diversas disciplinas taxonómicas para construir una serie integrada de líneas de base y registros actuales de nuestra cambiante biosfera.

Pseudopecoelus mccauleyi n. sp. and Podocotyle sp. (Digenea: Opecoelidae) from the deep waters off Oregon and British Columbia with an updated key to the species of Pseudopecoelus von Wicklen, 1946 and checklist of parasites from Lycodes cortezianus (Perciformes: Zoarcidae).

Pseudopecoelus mccauleyi n. sp. (Opecoelidae: Opecoelinae) is described from the intestine of the bigfin eelpout, Lycodes cortezianus (Gilbert, 1890) (Perciformes: Zoarcidae), collected at 200-800 m depths in the Northeastern Pacific Ocean off Oregon and Vancouver Island, British Columbia. The new species is distinguished by possessing a unique combination of the following diagnostic characters: vitelline fields that extend to the posterior margin of the ventral sucker; a slender, tubular and sinuous seminal vesicle that extends some distance into the hindbody; an unspecialized, protuberant ventral sucker; a genital pore at pharynx level; lobed to deeply multilobed testes; a lobed ovary; and an egg size of 68-80 µm × 30-46 µm. A single specimen of Podocotyle Dujardin, 1845 (Digenea: Plagioporinae) is also described from the intestine of an individual Coryphaenoides sp. (Gadiformes: Macrouridae) collected at 2,800 m depth off Oregon. A listing of parasites from the bigfin eelpout as well as observations of parasite diversity within relevant hosts are offered, new host and locality records are noted, and a brief discussion of Pseudopecoelus von Wicklen, 1946 in the deep sea is presented taking note of the low level of host specificity recorded (i.e. spp. of Pseudopecoelus are now known to parasitize deep-water fish from at least 20 piscine families). A new dichotomous key to the 39 recognized species of Pseudopecoelus is introduced.

Discovery of a 240 million year old nematode parasite egg in a cynodont coprolite sheds light on the early origin of pinworms in vertebrates.

BACKGROUND: We report the discovery of a nematode parasite egg (Nemata: Oxyurida) from a coprolite closely associated with the remains of several species of Cynodontia, dated to 240 million years old. This finding is particularly significant because this is the oldest record of an oxyurid nematode yet discovered, and because the cynodonts are considered a stem-group of the mammals. METHODS: We extracted material from a fully mineralized coprolite by both scraping the surface, and removing fragments from its interior with clean dental instruments used a single time. A single drop of glycerol from a new vial was added as a clearing reagent. Each slide was sealed with wax and examined with an optical microscope at 100× to 400× magnification. RESULTS: From one coprolite, 550 slides were examined; from 275 of these slides, sediment was examined that was scraped from the surface of the coprolite, and from the other 275 slides, material was examined that was extracted from the interior of the coprolite. All microscopic structures encountered were photographed, measured, and identified when possible. CONCLUSIONS: From the coprolite examined, we discovered an egg representing a new species of pinworm that, based on the egg structure, clearly places it in the family Heteroxynematidae. Nematodes of the order Oxyurida have very constrained life-histories, occurring only in animals that are not strictly carnivorous and also ingest large amounts of plant material. This fact enabled us to determine which species of cynodont, from several collected at the site in Brazil, are most likely the depositors of the coprolite, and therefore were the putative host of the parasite.

History of echinostomes (Trematoda).

Echinostomatidae (Trematoda) is the largest family within the class Trematoda. Members of this family have been studied for many years in relation to their utility as basic research models in biodiversity and systematics and also as experimental models in parasitology since they offer many advantages. Echinostomes have contributed significantly to numerous developments in many areas studied by parasitologists and experimental biologists. In this review, we examine the history of the echinostomebased studies from the beginnings to the present. For this purpose, we have divided the history of echinostomes into four periods (i.e. 18(th) and 19(th) centuries, first half of the 20(th) century, second half of the 20(th) century and the late 20(th) and 21(th) century) according to the types of studies performed in each of them. Moreover, we also briefly review the history of echinostome infections in humans.

Aspidodera kinsellai n. sp. (Nematoda: Heterakoidea) from nine-banded armadillos in Middle America with notes on phylogeny and host-parasite biogeography.

Aspidodera kinsellai n. sp. (Heterakoidea: Aspidoderidae) from the 9-banded armadillo, Dasypus novemcinctus , is herein described. This nematode occurs from Costa Rica north through central Mexico where it can be found causing co-infections with Aspidodera sogandaresi . Aspidodera kinsellai n. sp. can be discriminated from this and all other species in the family based on 3 key features, including (1) conspicuous lateral grooves with no lateral alae starting immediately after the hood and terminating at the cloacal/anal region; (2) long hoods in both male (360 µm) and female (401 µm), and (3) a relatively long (152 µm) terminal spine or terminus that gradually tapers to a point from the last pair of papillae. This is the 18th recognized species of the family and the 3rd in the genus present outside of South America. A phylogenetic analysis of the species in the genus with the use of the mitochondrial partial genes cytochrome C oxidase subunit 1 (cox1), the ribosomal large subunit (rrnL), and the internal transcriber spacer (ITS) shows that 2 species of Aspidodera may have entered into North America from the south via 2 independent events.

Parasitism of the Zweeloo Woman: Dicrocoeliasis evidenced in a Roman period bog mummy.

We undertook the analysis of Zweeloo Woman, a bog mummy from the Netherlands, to assess her parasitic state. Evidence of infection came from two areas: (1) liver paraffin sections and (2) microfossils washed from an intestinal section. Although the liver had shrunken considerably, objects consistent with operculated trematode eggs were found. After evaluating the range of trematode species that produce eggs in liver tissue, we arrived at the diagnosis of Dicrocoelium dendriticum. Although only 0.1ml of sediment was recovered from an intestinal section, eggs of Ascaris lumbricoides and Trichuris trichiura were also identified. No eggs of D. dendriticum were revealed by the intestinal wash although they were observed in the liver. The lancet fluke, D. dendriticum, is a zoonosis that usually infects ruminants such as cattle. Eggs of D. dendriticum may be found in human coprolites if infected cow liver, for example, was eaten. This is false parasitism. Since eggs of D. dendriticum were found in the liver of Zweeloo Woman, we are assured this was a true infection. This find is especially significant because it is the oldest known, patent infection of D. dendriticum in humans.

A new genus and species of lungworm (Nemata: Metastrongyloidea) from Akodon mollis Thomas, 1894 (Rodentia: Cricetidae) in Peru.

Akodonema luzsarmientae n.g., n.sp. (Nemata: Metastrongyloidea) is described from the pulmonary arteries and heart from several individuals of "soft grass mouse," Akodon mollis (Rodentia: Cricetidae), collected in the region of Ancash, Peru. The new genus and species is distinguished by a reduction of the dorsal ray to 2 small widely separated papillae.

Four events of host switching in Aspidoderidae (Nematoda) involve convergent lineages of mammals.

The Great American Interchange resulted in the mixing of faunistic groups with different origins and evolutionary trajectories that underwent rapid diversification in North and South America. As a result, groups of animals of recent arrival converged into similar habits and formed ecological guilds with some of the endemics. We present a reconstruction of the evolutionary events in Aspidoderidae, a family of nematodes that infect mammals that are part of this interchange, i.e., dasypodids, opossums, and sigmodontine, geomyid, and hystricognath rodents. By treating hosts as discrete states of character and using parsimony and Bayesian inferences to optimize these traits into the phylogeny of Aspidoderidae, we reconstructed Dasypodidae (armadillos) as the synapomorphic host for the family. In addition, 4 events of host switching were detected. One consisted of the switch from dasypodids to hystricognath rodents, and subsequently to geomyid rodents. The remaining set of events consisted of a switch from dasypodids to didelphid marsupials and then to sigmodontine rodents. The reconstruction of the ancestral distribution suggests 3 events of dispersal into the Nearctic. Two of these invasions would suggest that 2 different lineages of dasypodid parasites entered the Northern Hemisphere at different times, which is consistent with the presence of 2 lineages of armadillos in Mexico.

A new species of Molinema (Nematoda: Onchocercidae) in Bolivian rodents and emended description of Litomosoides esslingeri Bain, Petit, and Diagne, 1989.

We report the distribution of 2 species of filarioid nematodes occurring in different hosts in the central region of South America. Molinema boliviensis n. sp. was recorded as a parasite of sigmodontine and echymyid rodents in Bolivia, and Litomosoides esslingeri was recorded in sigmodontine and ctenomyid rodents from Bolivia and Argentina. Molinema boliviensis n. sp. shares several similarities with other species reported in spiny rats; however, it can be easily differentiated by the presence of a flat anterior end, gradually tapering lappets and a tubercle present in posterior end, a short, uniform buccal capsule, an oval-shaped vagina vera, and a ratio of spicules of 1:1.44. An account for the morphological variability of L. esslingeri is presented that allows the identification of the buccal capsule, the tail tip in females, and the shape of spicules as reliable diagnostic traits. A complete set of head papillae is also described. The finding of these parasites in phylogenetically unrelated hosts suggests that host capture may be a frequent phenomenon in these filarioids. Researchers should focus efforts in surveying mammals within the same ecological guild to understand the distribution and host specificity of these nematodes.

Details of the paranephridial system of a species of Prohyptiasmus (Cyclocoelidae: Hyptiasminae) from an American coot, Fulica americana (Rallidae) in Oklahoma.

During a study of the endohelminths of aquatic birds from the central flyway of North America, the details of the paranephridial systems of 3 immature specimens of Prohyptiasmus sp. were examined; the worms had been collected by the late Dr. J. Teague Self, former Professor, Department of Zoology, University of Oklahoma, Norman, Oklahoma from an American coot, Fulica americana (Raillidae), from the Cheyenne Bottoms, Roger Mills County, Oklahoma and deposited in the Harold W. Manter Laboratory of Parasitology. The excretory vesicle was Y-shaped and had a reduced stem. There were 3 main excretory canals on each side that, in the case of the most lateral 2 pairs, reached anteriorly to the level of the oral sucker. The most lateral canals entered the excretory vesicle about halfway down the stem on each side; the middle canals entered the vesicle at the tips of the branches of the vesicle; and the most medial canals entered the vesicle on the anterior edge about halfway between the branch point and the tips of the branches. There were numerous smaller secondary canals that interconnected with each other and with the 6 main paranephridial canals, forming a net-like system.