Occurrence of the Sinus Nematode Skrjabingylus sp. (Nematoda: Metastrongyloidea) Inferred from Sinus Lesions in Arkansas Mustelidae and Mephitidae, with Review of Relevant Literature R. Tumlison1* and T. L. Tumlison2 1Department of Biological Sciences, Henderson State University, Arkadelphia, AR, 71999 2367 Mt. Zion Rd., Arkadelphia, AR 71923 *Correspondence: [email protected] Running Title: Sinus Nematodes in Arkansas Mustelidae and Mephitidae Abstract 2005). The infective third stage larvae of Skrjabingylus may be ingested when a host species consumes an Nasal nematodes of the genus Skrjabingylus occur intermediate host (such as snails) or consumes paratenic in the mammalian families Mustelidae and Mephitidae, hosts such as frogs, snakes, or mice (Lankester and and in North America occur from Canada to Costa Rica. Anderson 1971; Hansson 1967; Gamble and Riewe Ingestion of infected snails, frogs, snakes, or mice can 1982; Jennings et al. 1982; Weber and Mermod 1985). infect mammalian hosts. Infection often causes Skrjabinglyus nasicola is the most widely pathology to bones in the sinus region, which may lead distributed species of the genus (Santi et al. 2006), and to discoloration, enlargement, and fenestrations of the is common and cosmopolitan. The definitive hosts of S. bone. Examination of museum specimens for evidence nasicola are members of the genus Mustela (then of infection has been used to detect prior infection, but including mink, which is now in the genus Neovison) prevalence and intensity cannot be interpreted without (Hawkins et al. 2010). Other species of Skrjabingylus actually recovering the parasite. We examined appear also to have host specificity; S. petrowi of the Mustelids and Mephitids in collections of mammals genus Martes (Heddergott et al. 2015b), S. housed at Arkansas State University (ASU), Henderson chitwoodorum of the skunks Mephitis and Spilogale State University (HSU), and the University of Arkansas (Hill 1939, Hobmaier 1941; Goble 1942), and S. lutrae at Little Rock (UALR) to evaluate the possible of river otters (Lankester and Crichton 1972). occurrence of nasal nematodes in Arkansas mammals. In mink, up to 63 worms were counted in an Evidence of infection was found in skulls of the Striped individual from Minnesota (Kinsey and Longley 1963), Skunk (Mephitis mephitis), Spotted Skunk (Spilogale but the average infection was 4.1 worms per cavity in putorius), Mink (Neovison vison), Long-tailed Weasel Ontario (Santi et al. 2006). Significant infection often (Mustela frenata), and North American River Otter causes bone pathologies of the sinus region, which may (Lontra canadensis) from Arkansas. We report for the present as discoloration, swelling or enlargement, and first time evidence of the presence and distribution of fenestrations of bone in the region of the sinuses (Santi Skrjabingylus sp. infecting mammals in Arkansas. et al. 2006). Lesions, known as local rarefying osteomyelitis, result from a reaction to the worms in the Introduction sinuses, which eventually can result in damage to bone (Kierdorf et al. 2006). Significance of the infection, The trematode Troglotrema acutum and species of suggested by hypotheses of a relatively smaller the nematode Skrjabingylus can cause cranial lesions in braincase caused by swelling of the frontal sinsues in skulls of certain mammals (Heddergott et al. 2015a), but older, infected animals, was supported for striped T. acutum occurs only in Europe so does not affect New skunks (Mephitis mephitis) (Maldonado and Kirkland World mammals. In North and Central America, only 1986), older male mink (Bowman and Tamlin 2007), nasal nematodes of the genus Skrjabingylus have been and also occurred with a bias toward males in river identified from several geographic locations and in otters (Scherr and Bowman 2009). several members of the mammalian families Mustelidae and Mephitidae. Records are known from as far north as Methods the Northwest Territories of Canada (Dougherty and Hall 1955) to as far south as Costa Rica (Carreno et al. Because no data exist about occurrence of Journal of the Arkansas Academy of Science, Vol. 73, 2019 6 Sinus Nematodes in Arkansas Mustelidae and Mephitidae Skrjabingylus in Arkansas, we sought to determine minks and 10 weasels and found infections in 4 of each which Arkansas members of the Mustelidae and species, but no external enlargement or abnormality was Mephitidae might show evidence of infection. We observed. On the other hand, they found no worms on examined skulls housed in collections of mammals at opening the sinuses of a Bonaparte weasel that had an Arkansas State University (ASU), Henderson State enlarged frontal region. Levine et al. (1962) also University (HSU), and the University of Arkansas at reported that these parasites were present in the brain Little Rock (UALR). We examined skulls of the Striped cases of skunks that did not show the characteristic Skunk (Mephitis mephitis), Spotted Skunk (Spilogale lesions. Thus, damage in the sinuses may indicate that putorius), Mink (Neovison vison), Long-tailed Weasel infection has occurred, but not that it is current, and (Mustela frenata), and North American River Otter absence of damage does not mean no infection is (Lontra canadensis), all of the members of the present. Mustelidae and Mephitidae in Arkansas with the Considerable variation exists with respect to exception of the American Badger (Taxidea taxus). We reported patterns of occurrence and manifestation of collected data regarding the county of origin of each infection. Several studies report evidence that both specimen to examine distribution within Arkansas. prevalence and intensity of infection tend to be higher in older host animals (Dougherty and Hall 1955; Results and Discussion Gamble and Riewe 1982; Fuller and Kuehn 1984), but other studies find this in juveniles (Santi et al. 2006). The apparent oldest skull from Arkansas exhibiting Both prevalence and intensity of infection were damage from infection with Skrjabingylus was a new observed to be higher in male ermine (Dubay et al. subspecies of ermine named by Brown (1908) after 2014), and male otters were found to suffer greater collection from the Conard Fissure in Newton County. damage to their skulls due to these parasites (Scherr and Originally named Putorius cicognanii angustidens, and Bowman 2009). Skulls of male Least Weasels (Mustela now known as Mustela erminea angustidens, one nivalis) were more severely damaged in England (King specimen shown in plate XVII of Brown (1908) had a 1977), as were skulls of male Long-tailed Weasels circular lesion on the left side just behind the postorbital (Mustela frenata) in Manitoba (Gamble and Riewe process of the skull. The lesion is consistent with 1982). In contrast, Debrot and Mermod (1980) reported infection by Skrjabingylus. no sex- or age-related differences in mustelids from In the modern species we examined, we detected Switzerland. Santi et al. 2006 summarized studies in lesions in all species. Skulls of smaller species appeared which an infection bias to one sinus was believed to to be more likely to demonstrate lesions, and to have have caused asymmetrical damage to the sinus region, larger openings, likely due to the thinner bones whereas other studies found no difference in damage constituting the frontal region. Bones of the North between the sinuses (Hansson 1967; Lewis 1967). American River Otter are more substantive, and were Therefore, we present data only to demonstrate the deemed less likely to show lesions (Scherr and Bowman inferred presence of the nematode in mustelids and 2009). mephitids from Arkansas, the distribution of such Examination of museum specimens for bone occurrences, and relevant literature to elucidate how our pathologies in the sinuses often has been used to provide observations fit with other North American information. evidence of occurrence, prevalence, and intensity of infection. Stegeman (1939) found bone lesions in New Spotted Skunk (Spilogale putorius)- Hill’s (1939) York Mephitis and suggested infection by description of a new species of sinus nematode, Skrjabingylus, and Tiner (1946) used occurrence of Skrjabingylus chitwoodorum, was based partly on lesions to infer the presence of this nematode in Texas specimens collected from Spilogale interrupta collected skunks. Reliance on observation of damage in museum in Oklahoma. In California, S. chitwoodorum was specimens to determine prevalence and intensity of reported to occur frequently in spotted skunks taken infection have added confusion, however, due to from the Davis area (Mead 1963). Lesions assumed to problems in inferring levels of parasite burden without have been cause by an infestation by S. chitwoodorum actually recovering the parasite (Dougherty and Hall were found in skulls of 3 Spilogale from Texas, wherein 1955). damage varied from bulging and osteitis to holes in the Presence or absence of osteological damage may frontal sinuses (Tiner 1946). not be a good index of the incidence of these parasites. Spotted Skunks are not well represented in Goble and Cook (1942) examined the sinuses of 10 collections in Arkansas. We examined 5 specimens, Journal of the Arkansas Academy of Science, Vol. 73, 2019 7 R. Tumlison and T. L. Tumlison originating from Franklin, Izard, Pulaski, and Sebastian appearance with tiny perforations, numerous small Counties. Those from Franklin, Pulaski and Sebastian perforations, and a remodeled forehead with a high rise Counties, showed evidence of infection (Fig.