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Natural infections of tetrathyridia of Mesocestoides species in deer mice, Peromyscus maniculatus, from New Mexico.

Adult Mesocestoides species are parasites of carnivorous mammals and birds. Although 27 species of Mesocestoides were recognized by Schmidt (1986) the life cycles of none of them are known. Encapsulated and free tetrathyridia are often found in the body cavities and various organs of amphibians, reptiles and rodents Padgett and Boyce (2004). In recent surveys of foxes in New Mexico adult Mesocestoides have been reported (Ubelaker et al. 2013; 2014a, 2014b). Surveys of rodents in the northern mountains of New Mexico have found asexually reproducing tetrathyridia of Mesocestoides in a rodent species that we report here.

During the summers of 2008-2012, we collected Peromyscus maniculatus from buildings and surrounding grounds on the Southern Methodist University campus in Taos, New Mexico (36[degrees]16'27N, 105[degrees]34'31.6"W). We collected 129, 98, 112, 88, and 86 mice in 2008, 2009, 2010, 2011, and 2012, respectively. Mice were trapped in Sherman live traps (H. B. Sherman Traps, Tallahassee, Florida) baited with peanuts and examined for parasites under animal protocols SMU 80708 and 80711. We collected parasites as described by Gardner (1996).

Three of 129 deer mice (one adult male collected 24 July 2008, one adult female collected 23 June 2010, and one adult female collected on 8 July 2012) contained actively dividing tetrathyridia of Mesocestoides in the body cavity and liver. We collected all infected mice among the foundations of a former saw mill (that operated 19401950) in a field dominated by sagebrush (Artemisia tridentata tridentata) with clumps of Wood's rose (Rosa woodsii) and the grasses wildrye (Elymus canadensis and Elymus longifolius) June grass (Koeleria macrantha) and sleepy grass (Achnatherum robustum). We deposited two of the infected mice and their tetrathyridia in the Museum of Southwestern Biology, Department of Biology, University of New Mexico, as MSB PARA 174 and MSB PARA 175.

The morphology of the tetrathyridia we collected was similar to that described by Etges (1991). Tetrathyridia that we observed with a dissecting microscope were asexually proliferative by means of multiple and binary fission. We observed small numbers (approximately 20) of tetrathyridia free in the body cavity of the male mouse collected in 2008 and they were divided and injected into the peritoneal cavity of four laboratory white mice, Mus musculus under SMU animal protocol numbers 30108-30111. Our examination of the laboratory mice 6-9 mo later revealed heavy infections with an estimate of several hundred tetrathyridia continuing to reproduce asexually. They have been maintained in laboratory mice since 2008. A specimen of laboratoryreared M. musculus with tetrathyridia present has been deposited in the University of Nebraska State Museum, Manter Laboratory of Parasitology, number HWML 686671.

Kegley et al. (1970) were the first to report that tetrathyridia isolated from P maniculatus in Coos County, Oregon, could be laboratory-propagated by interperitoneal transfer of tetrathyridia in laboratory mice, although they never authenticated their work with voucher specimens or continued propagation. The authors referred to the tetrathyridia as Mesocestoides corti although M. corti was described as an adult cestode from the intestine of M. musculus by Hoeppli (1925) based on specimens collected earlier by Cort. Beaver (1989) questioned that M. musculus was the actual host because adult Mesocestoides occur in carnivores, and adult Mesocestoides have never been recovered from rodents. Conn (1990) stated that asexual reproduction was confirmed by continual propagation of laboratory clones only in tetrathyridia isolated from lizards, as reported by Specht and Voge (1965). Hanson and Widmer (1985) and Widmer et al. (1995) reported asexual proliferation in snakes. Working with the strain isolated by Specht and Voge (1965), Etges (1991) named and described the proliferative tetrathyridia from lizards as Mesocestoides vogae (see also Rausch 1994).

Another report of tetrathyridia isolated from rodents in North America is Mesocestoides carnivoricolus (Grundmann, 1956). Grundmann (1956) reported finding tetrathyridia in body cavities, liver, and lungs of P. maniculatus and Peromyscus crinitus from Toole County, Utah (Grundmann 1958; Grundmann and Frandsen 1959, 1960). The presumed adults for these tetrathyridia were found in American badger (Taxidea taxus), coyote (Canis latrans), and bobcat (Lynx rufus) in the same county. Padgett and Boyce (2004) reported that 8% of P. maniculatus on San Miguel Island, California, had infections of Mesocestoides tetrathyridia and foxes (Urocyon littoralis littoralis) contained adult tapeworms. The authors were not successful in infecting ants with eggs from tapeworms taken from the foxes. Shults (1970) reported tetrathyridia of Mesocestoides kirbyi in red-backed voles (Clethrionomys rutilus) from Alaska and adults in arctic foxes (Alopex lagopus). Our report supports the observation by Kegley et al. (1970) that asexually reproducing tetrathyridia occur naturally in deer mice. In New Mexico, Mesocestoides species in foxes have been reported. Ubelaker et al. (2013) reported adult Mesocestoides variabilis in red foxes (Vulpes vulpes). Ubelaker et al. (2014b) found M. variabilis in swift foxes (Vulpes velox) and Ubelaker et al., (2014a) also found M. variabilis in kit foxes (Vulpes macrotis). Ubelaker et al. (in litt.) report M. kirbyi in gray foxes (Urocyon cinereoargenteus).

Several researchers have reported nonproliferative Mesocestoides tetrathyridia from nonmammalian hosts in North America. This was supported by failure to reproduce asexually in repeated laboratory infections of mice (Conn and Etges, 1984; McAllister and Conn 1990; McAllister et al., 1992) and by lack of morphology consistent with asexual reproduction (see Conn 1986; Conn and McAllister 1990; McAllister et al., 2005). These reports were all documented by deposition of voucher specimens in museums. Conn (1986) and Conn et al. (2002) examined Mesocestoides tetrathyridia both morphologically and ultrastructurally and noted marked differences between asexually proliferative and nonproliferative tetrathyridia. They have also reported nonproliferating Mesocestoides tetrathyridia from European rodents, although some of these do possess morphological aberrancies (Conn et al., 2010, 2011). The present report provides important new information on the prevalence of asexuality among tetrathyridia and underscores the need for further study of this variation among metacestodes of this cosmopolitan genus.

Sincere thanks are extended to W. Wilson, S. V. Brant, and J. Dunnum at the Museum of Southwestern Biology, The University of New Mexico, Albuquerque, for making possible the deposition of deer mice and parasites. S. Gardner and G. Racz deposited laboratory mice with tetrathyridia in the Museum of Parasitology, Harold W. Manter Laboratory of Parasitology, Lincoln, Nebraska, and accepted several infected live animals for additional studies on the life cycle. A. Nozaleda from Southern Methodist University provided the Spanish translation of the abstract. We also thank two anonymous reviewers for comments that greatly improved the manuscript.

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Submitted 6 February 2014.

Acceptance recommended by Associate Editor, Jerry L. Cook, 30 April 2014.

John E. Ubelaker, * Nora Abdullah, Aya Mouhaffel, Rashmi Ananadampillair, Caitlyn Emigh, and Scott L. Gardner

Department of Biology, Southern Methodist University, Dallas, TX 75275 (JEU, NA, AM, RA, CE)

Department of Biology, University of Nebraska, Lincoln, NE 68588 (SLG)

* Correspondent: ubelaker@smu.edu
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Author:Ubelaker, John E.; Abdullah, Nora; Mouhaffel, Aya; Ananadampillair, Rashmi; Emigh, Caitlyn; Gardner,
Publication:Southwestern Naturalist
Article Type:Report
Geographic Code:1U8NM
Date:Sep 1, 2014
Words:1955
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