Estimates of the distribution and prevalence of the sinus roundworm (Skrjabingylus chitwoodorum) have been based largely on the inspection of skunk (Mephitidae) skulls showing damage from infections. We examined 595 striped skunks (Mephitis mephitis) and nine hog-nosed skunks (Conepatus leuconotus) that had tested negative for rabies by the Texas Department of State Health Services (US) between November 2010 and April 2015 to determine species of Skrjabingylus, prevalence and intensity of infection, and distribution of infection in Texas by county. We expected ecoregions with more precipitation to have higher rates of infection than more-arid ecoregions. Prevalence of S. chitwoodorum in striped skunks was 48.7%, with a mean intensity of 19.4 (SD=24.44, range=1–181) nematodes. There was a bias for the left sinus. The prevalence of infection varied among ecoregions of Texas, but it was not correlated with precipitation. Infection intensity did not vary among ecoregions. The prevalence of sinus roundworms in rabies-negative skunks suggested that behavioral changes because of skrjabingylosis might have been responsible for the submission by the public of some skunks for rabies testing.

Skrjabingylus chitwoodorum (Rhabditida: Metastrongylidae) is a species of nematode that inhabits the sinus cavities of skunks as adults. It can be distinguished from the other North American species of sinus roundworm (Skrjabingylus nasicola, Skrjabingylus santaceciliae, and Skrjabingylus lutrae) that infect mephitids and mustelids by its longer body and the size and morphology of the copulatory spicules in males (Lankester 1983; Carreno et al. 2005; Santi and Parker 2012). After ingestion by the hosts, the worms penetrate the abdominal wall to reach and follow the perineurium of localized nerves in the vertebral column, eventually reaching the nasal sinuses, where maturation occurs. The migration of the nematodes can result in meningitis and, at times, movement into the ventricles of the brain that may result in neurologic problems for the host (Lankester and Anderson 1971; Santi and Parker 2012).

Since it was first described in striped skunks (Mephitis mephitis) and spotted skunks (Spilogale putorius) from Oklahoma (Hill 1939), S. chitwoodorum has since been reported, based on measurements and morphologic features, from striped skunks in Ontario, Canada (Lankester 1983); Quebec, Canada (Webster 1965); California (Emmons and Johnson 1969); Illinois (Gehrt et al. 2010); Kansas (Ewing and Hibbs 1966); Maryland (Goldberg 1954); Minnesota (Fuller and Kuehn 1984); New York (Goble and Cook 1942); North Dakota (Dyer 1969); and Pennsylvania (Kirkland 1975). The remainder of our knowledge about the distribution of S. chitwoodorum in skunks in North America comes from studies using cleaned and dried skulls because the roundworms can cause noticeable deformations (e.g., bulges and lesions) and/or discoloration in the sinuses of their hosts. Maldonado and Kirkland (1986) used museum and fresh specimens to conclude that inspection of cleaned and dried crania was a reliable method for determining infection status; however, Goble and Cook (1942) reported that skulls of sinus roundworm–infected mink (Vison vison) did not always show signs of damage. Thus, there is disagreement as to the reliability of using museum specimens for determining prevalence of sinus roundworm infections, but many studies have used one or both methods.

Based on the presence of bone damage, degradation, or other signs of nematode infections, Kirkland and Kirkland (1983) concluded the range of sinus roundworms spans most, if not all, of North America in a study in which they examined the crania of 3,055 striped skunks from 42 museum collections across the US and Canada. They estimated 72.2% of the 619 skunks from the Great Plains region of their study (which included Texas) had lesions attributable to skrjabingylosis. Two studies of endoparasites from Texas skunks (Tiner 1946; Neiswenter et al. 2006) reported skull damage attributed to sinus roundworms in both striped and western spotted skunks (Spilogale gracilis). To our knowledge, no study has established the prevalence of skrjabingylosis in Texas skunks using the actual presence of nematodes, and the species of sinus roundworm has not been confirmed there.

Skrjabingylus chitwoodorum has been reported in both rabid (Emmons and Johnson 1969) and nonrabid skunks (Gehrt 2005). Because a large number of skunks are submitted annually for rabies testing in Texas, we were able to obtain a sizeable sample, verify the identification, and determine the prevalence, intensity, and geographic distribution of sinus roundworms and evaluate whether ecoregion type was associated with prevalence or intensity of infections. We proposed that individuals with heavy sinus roundworm infections might have been submitted for rabies testing based on abnormal behavior because of the parasite's presence (Maldonado and Kirkland 1986). Because of larval sensitivity to desiccation in sinus roundworms (Hansson 1974) and the reported higher prevalence in regions with more precipitation (Kirkland and Kirkland 1983), we predicted that prevalence and intensity would vary among ecoregions. We anticipated our findings would be consistent with previous studies in that skunks from arid ecoregions (i.e., those in western Texas) would be less likely to be infected than those from more-humid ecoregions.

Frozen heads of 604 rabies-negative skunks were salvaged from the Texas Department of State Health Services between November 2010 and April 2015 and examined for adult sinus roundworms. The braincase had been excised, and the brain removed from each head before examination. Access to sinuses was available because of the partial removal of the top portion of the cranium. Both portions of the cranium were examined for nematodes in this study. Data on hosts included the date received and the location (to county level). Sex of individuals was undetermined because only the crania of the skunks were available for examination. During examination of each individual, nematodes were extracted and preserved in either 10% buffered formalin or 70% ethanol, or they were frozen. Our host sample comprised 595 striped skunks, and nine hog-nosed skunks. Host vouchers were deposited in the Angelo State Natural History Collection of Mammals (Angelo State University, San Angelo, Texas, USA) after being cleaned in a dermestid beetle (Dermestes sp.) colony. Nematodes were deposited in the Harold W. Manter Laboratory of Parasitology general collection (University of Nebraska-Lincoln, Lincoln, Nebraska, USA; accession no. P-2017-028).

We use the terms prevalence (the percentage of hosts infected with that species/total number of hosts examined) and intensity (number of nematodes/infected host) in accordance with definitions by Bush et al. (1997). For 515 specimens, we recorded the intensity of infection, and for 167 specimens, we recorded the number of nematodes extracted from each left and right sinus. Specimens examined early in the study were scored solely as to presence or absence of sinus roundworms.

To test the accuracy of determining nematode infection based on dried crania, we reexamined a random subset of 100 skulls from this study and attempted to independently identify the infected individuals based on the presence of lesions, discoloration, and bulging of the bone. Determinations were made without knowledge of nematode infections. Eighty skulls were assigned to age classes based on ossification of three sutures in the skull (Kirkland and Kirkland 1983).

We identified Skrjabingylus spp. using spicule measurements and images from Lankester (1983). Nematodes were cleared using lactophenol and examined using an Olympus microscope (Olympus America Corporation, Center Valley, Pennsylvania, USA) equipped with an OMAX camera (OMAX Corporation, Bucheon-si, Gyeonggi-do, Korea). Copulatory bursa, gubernaculum, and/or spicules for some adult males from each county were photographed; when possible, measurements of spicules or the gubernaculum were obtained using the image-processing program ImageJ (US National Institutes of Health, Bethesda, Maryland, USA; Schneider et al. 2012). We were able to measure the complete spicules of 49 nematodes.

We assessed geographic patterns of infection by assigning county samples to ecoregions of Texas (Griffith et al. 2007). Because our collection-locality data were limited to county and because some counties could be divided into multiple ecoregions, we assigned 16 additional ecoregion names for split counties, producing 28 modified ecoregions for analysis. Of those, seven ecoregions had a sample size of less than five and had to be removed for statistical analyses, resulting in 21 ecoregions.

Statistical analyses were performed using R software (R Development Core Team 2015). A paired t-test was used to determine whether a bias existed between left and right sinuses. Because we were modeling a binomial (dichotomous) response variable (presence or absence), we performed randomization tests using generalized linear models with binomial errors to test the effects of age and ecoregion on prevalence. A bootstrap procedure with 10,000 iterations was performed to generate error bars for prevalence within each ecoregion. A permutational analysis of variance (ANOVA) with 1,000 iterations was performed to compare intensity across ecoregions.

Of 595 striped skunks examined, 290 (48.7%) were infected with the sinus roundworm (Table 1). Spicule length for the 49 male nematodes sampled averaged 677.5 μm (SD=84; range=299–871 μm). Gubernaculum measurements and copulatory bursa morphology were also indicative of S. chitwoodorum (Hughes 2016). Skrjabingylus nasicola was never detected. None of the nine hog-nosed skunks inspected had sinus roundworm infections. Skunks from 84 of the 124 counties sampled in Texas were positive for sinus roundworms (Fig. 1).

Table 1

Reported prevalence and mean intensity of sinus roundworms (Skrjabingylus chitwoodorum) in striped skunks (Mephitis mephitis) in North America and the technique used for detection of the infection. Studies with sample sizes less than 10 have been excluded. — = intensity not reported.

Reported prevalence and mean intensity of sinus roundworms (Skrjabingylus chitwoodorum) in striped skunks (Mephitis mephitis) in North America and the technique used for detection of the infection. Studies with sample sizes less than 10 have been excluded. — = intensity not reported.
Reported prevalence and mean intensity of sinus roundworms (Skrjabingylus chitwoodorum) in striped skunks (Mephitis mephitis) in North America and the technique used for detection of the infection. Studies with sample sizes less than 10 have been excluded. — = intensity not reported.
Figure 1

Counties and ecoregions in Texas, USA where skunk carcasses originated from November 2010 to April 2015 and which were sampled for sinus roundworms (Skrjabingylus chitwoodorum).

Figure 1

Counties and ecoregions in Texas, USA where skunk carcasses originated from November 2010 to April 2015 and which were sampled for sinus roundworms (Skrjabingylus chitwoodorum).

Close modal

After tissues had been removed, an infected individual could usually be distinguished by discoloration of the skull. Infections were often apparent even before removing the skull cap because worms could often be seen through the bone. Typically, the greater the intensity of infection, the darker the mass under the bone appeared. Intensity varied from 1 to 181 nematodes/host (mean=19.64, SD=24.44; Fig. 2). Nematodes were rarely recovered outside the sinus cavities, although some were found in the trachea and mouth; one was recovered from the eye, and one skunk had a lesion with a mass of sinus roundworms in the diastema between the canine and first premolar. These could represent the movement of nematodes after the death of the host (Lankester and Anderson 1971).

Figure 2

Intensity (number of nematodes/host) of infection of sinus roundworms (Skrjabingylus chitwoodorum) in 515 striped skunks (Mephitis mephitis) from Texas, USA recovered from November 2010 to April 2015.

Figure 2

Intensity (number of nematodes/host) of infection of sinus roundworms (Skrjabingylus chitwoodorum) in 515 striped skunks (Mephitis mephitis) from Texas, USA recovered from November 2010 to April 2015.

Close modal

Of the 100 specimens reexamined after cleaning to determine infection status based on skull damage or discoloration, 62 were correctly scored (57 true-positives). Twenty-one uninfected individuals appeared to have signs of skrjabingylosis (false-positives), and 17 infected individuals showed no signs of skull damage (false-negatives). Randomization tests confirmed that age was a significant variable of infection status (P=0.001), and an odds-ratio analysis showed that, with each increase in age class, the chances of an S. chitwoodorum infection increased by a factor of 1.38. A paired t-test revealed a bias toward roundworm occupation of the left sinus (t=2.17, df=166, P=0.031; means: 11.16>10.16).

Prevalence of the sinus roundworms by ecoregion varied from 9.1% to 74.1% (Fig. 3). Although sample sizes were low, the initial randomization test for ecoregions also showed variation in prevalence among ecoregions (P=0.001). Post hoc tests, that is, pairwise logistic regression (1,000 iterations) with a Holm adjustment, lacked the power to identify the specific ecoregions that varied in prevalence. In general, ecoregions with prevalence that differed by more than 25% were significantly different. Logistic regression using latitude and longitude coordinates for each county revealed that neither latitude nor longitude were significant predictors of prevalence (P=0.953 and 0.311, respectively). The permutational ANOVA showed intensity did not vary significantly among ecoregions (Fligner-Killeen test of homoscedasticity: P=0.021; permutational ANOVA: P=0.159).

Figure 3

Prevalence (percentage of hosts infected/total hosts examined) of sinus roundworms (Skrjabingylus chitwoodorum) in striped skunks (Mephitis mephitis) recovered from November 2010 to April 2015, as indicated by Texas, USA ecoregion. Error bars are 95% bootstrapped confidence intervals. Numbers displayed on the graph represent sample sizes for that ecoregion.

Figure 3

Prevalence (percentage of hosts infected/total hosts examined) of sinus roundworms (Skrjabingylus chitwoodorum) in striped skunks (Mephitis mephitis) recovered from November 2010 to April 2015, as indicated by Texas, USA ecoregion. Error bars are 95% bootstrapped confidence intervals. Numbers displayed on the graph represent sample sizes for that ecoregion.

Close modal

Spicule measurements from our study were not consistent with those from the Lankester (1983) redescription of S. chitwoodorum but were in agreement with the measurements from the original species description for S. chitwoodorum from Oklahoma (Hill 1939) and those from studies in Minnesota (Fuller and Kuehn 1984) and Canada (Webster 1965). Copulatory bursa of the Texas nematodes closely resembled those in the figures provided by Lankester (1983) for S. chitwoodorum. The difference in spicule lengths could be attributable to geographic variation among S. chitwoodorum from different regions. No S. nasicola were identified in our study, supporting the Lankester (1983) view that this sinus roundworm does not occur in skunks, in contrast to the suggestion of Swales (1938).

Both this study and that by Kirkland and Kirkland (1983) on museum specimens of striped skunks found a bias toward infection of the left sinus. Studies on S. nasicola in mustelids also revealed asymmetrical sinus infections. Hansson (1968) reported a left sinus bias from short-tailed weasels (Mustela erminea) and a right sinus bias in least weasels (Mustela nivalis) and European polecats (Mustela putorius); Weber and Mermod (1985) reported a right sinus bias in ferrets (M. putorius). Hansson (1968) suggested that those biases might be due to “irregularities in the structure of the crania” based on Rosen and Sarnat (1954), who described the sinus maxillaris of dogs. Other studies on S. nasicola in short-tailed weasels (King and Moody 1982; Dubay et al. 2014) and mink (Santi et al. 2006) reported no bilateral asymmetry between left and right sinuses of infected individuals. Nematodes presumably are incapable of movement between left and right sinuses, although damage done to the skull could allow movement in extreme infections. We found no reports suggesting sinus roundworms were capable of doing so.

We documented increased infection with increasing host age, consistent with the findings of Kirkland and Kirkland (1983). As with many parasites, the age of the host is an important factor on status of infection with S. chitwoodorum.

Our samples sizes were relatively small (1–3 skunks) for all counties we reported as negative for sinus roundworms. Hidalgo County was an exception with 14 specimens examined. Although areas of high human density were largely included in our survey, we believe sinus roundworms are likely to be found in skunks throughout Texas, based on the prevalence that we observed. Our study only sampled skunks that had been submitted to the Texas Department of State Health Services and that had tested negative for the rabies virus. Because of that sampling bias, our survey was not necessarily a comprehensive representation of the entire skunk population in Texas, and our results should be interpreted with that distinction in mind.

The percentage (48.7%) of striped skunks with skrjabingylosis we report was less than the estimated prevalence (72.2%) for this region from Kirkland and Kirkland (1983), who only examined museum specimens, likely a less-sensitive technique. Our results suggested that examination of skulls alone may not give a reliable estimate of the prevalence of sinus roundworms. Goble and Cook (1942) also concluded that lesions in the sinuses of specimens may be a less-effective method than using nematode presence for determining infection status. An alternative explanation for the lesser prevalence of sinus roundworms that we reported is that skunks may show skull damage from a previous infection, which is no longer active. We are unaware of any research demonstrating a natural loss of infection. The prevalence of sinus roundworms in Texas skunks that we observed was slightly greater than that reported for infected skunks from California (Mead 1963), Kansas (Ewing and Hibbs 1966), North Dakota (Dyer 1969), and Illinois (Gehrt et al. 2010). Those studies also used nematode presence (instead of skull damage) to determine prevalence (Table 1). The average intensity we found (Table 1) was comparable to that reported for North Dakota (Dyer 1969), Kansas (Ewing and Hibbs 1966), and Ohio (Bailey 1971), but was greater than the average intensity reported for Illinois (Levine et al. 1962) and Pennsylvania (Maldonado and Kirkland 1986). We predicted that skunks that had been submitted for rabies testing but were negative for the virus would have a high intensity of sinus roundworms, causing the skunks to behave abnormally (Lankester and Anderson 1971), yet most of infections we detected were relatively mild (Fig. 2).

Hansson (1974) reported that low humidity and high temperature reduce survival of the first-stage larvae of S. nasicola in feces. Skrjabingylus nasicola larvae can survive freezing for some time in dry conditions but are highly sensitive to desiccation (Hansson 1974). Kirkland and Kirkland (1983) reported a positive correlation between precipitation and the frequency of lesions caused by sinus roundworm in striped skunk skulls from various regions of the US. Because of their findings and what is known about larval sensitivity to desiccation in S. nasicola, we suspected that prevalence or intensity of sinus roundworm infections might also vary among ecoregions of Texas because of differences in precipitation, but we found no direct indication of that. Despite our large sample of skunks in Texas, we had low sample sizes for some individual ecoregions. A larger-scale study might be necessary to address the relationship between sinus roundworm prevalence and precipitation. Kirkland and Maldonado (1988), however, also found no significant relationship between precipitation and cranial damage in striped skunks from Mexico.

Although prevalence of S. chitwoodorum infections of skunks varied among the different ecoregions in Texas, the variations were not clearly correlated with precipitation on a regional scale. For example, skunks from the Chihuahuan Desert ecoregion had the highest prevalence (77%; 20/26), but that area received the least amount of annual precipitation. This lack of an apparent pattern could be confounded by uneven sampling of skunks from residential areas where the public most often encountered skunks and where most recovered skunks were submitted for rabies testing. In the case of the Chihuahuan Desert ecoregion, all 26 skunks came from within the El Paso city limits, an area that likely had greater sources of water and habitat availability, which were considerably different from that of the open desert outside the city. If precipitation influences prevalence of sinus roundworm infections, local factors such as these may have a role. Factors other than precipitation and urbanization may also be important. Specifically, the wide availability of intermediate and paratenic hosts of the parasite also may contribute to the high percentage of infected skunks throughout Texas. The possibility that introduced species of snails have a role in transmission of sinus roundworms should also be considered.

Although we sampled few hog-nosed skunks, none showed any signs of sinus roundworm infections, which is consistent with previous research (Tiner 1946; Kirkland and Kirkland 1983; Neiswenter et al. 2006) based on examination of damage to skulls in museum specimens. The only report of S. chitwoodorum in hog-nosed skunks was from Patton (1974), who based his conclusion on osteitis and bulging of the frontal bones of some individuals from the Trans-Pecos region of Texas. Because the Patton (1974) research was the sole study suggesting sinus roundworm occurs in hog-nosed skunks and was based only on appearance of damage to the skull, we found that report to be suspect. Summaries of the biology of the hog-nosed skunk (e.g., Dragoo and Sheffield 2009) cite Patton (1974) for the presence of S. chitwoodorum in that species. Our data, although limited, refute the hypothesis that S. chitwoodorum occurs in hog-nosed skunks. The frontal sinuses found in striped and spotted skunks are absent in hog-nosed skunks (Van de Graaff 1969), probably accounting for the absence of sinus roundworms in that species (Kirkland and Kirkland 1983).

We could not determine the reason individual skunks we sampled had been submitted for rabies testing; however, it was most likely because of interactions with humans or domestic animals or because of abnormal behavior. Ewing and Hibbs (1966) suggested rabies-like behavior in skunks could be caused by sinus roundworm infections. In an experiment in which striped skunks were given infective S. chitwoodorum larvae, three of six animals showed neurologic disturbance and one experienced partial paralysis 22 d after infection (Lankester and Anderson 1971). The experimentally infected skunks showed signs of lethargy, lack of motor coordination, and suffered brain hemorrhaging. The presence of the worms can also cause the frontal sinuses of their hosts to expand, which could exert pressure on the brain (Maldonado and Kirkland 1986), possibly resulting in abnormal host behavior (Maldonado and Kirkland 1986; Bowman and Tamlin 2007). The effects of the parasite infection on the brain of skunks and their behavior are poorly understood. Two records exist of S. chitwoodorum “found on the brain surface of skunks”; both were part of rabies research projects (Levine et al. 1962). One report stated that the “ante mortem behavior” suggested the individual was rabid, but it was found to be negative after rabies testing (Ewing and Hibbs 1966). Based on those studies, there is reason to believe that some skunks are submitted for testing because of behavioral changes due to sinus roundworms; however, our data are inconclusive in that regard because no behavioral observations were recorded by those submitting skunks for testing. During the full 4 yr (2011–14) that skunks were salvaged for this research, 3,881 skunks were submitted for testing to the Texas Department of State Health Services. Of those, 2,136 (55%) tested negative for rabies (Texas Department of State Health Services 2017). Although speculative, that high number of rabies-negative skunks submitted for testing in Texas suggests that skrjabingylosis is potentially responsible for aberrant behaviors, leading to rabies testing in some striped skunks.

We thank Danielle Smith, Letha Zuckero, and Noirin Ammann of the Rabies Identification Team, Texas Department of State Health Services, for their multiyear effort at saving submitted skunks for this study, and we thank Kenneth Waldrup for his collection efforts in El Paso, Texas. We thank the student volunteers associated with the Angelo State Natural History Collections who helped with specimen preparation. We thank Mary P. Jones for help with statistical analysis and Ben Skipper and James G. Dunn for help with geographic information system aspects of this research. We also thank anonymous reviewers and editors for comments on the manuscript.

Bailey
TN.
1971
.
Biology of striped skunks on a southwestern Lake Erie Marsh
.
Am Midl Nat
85
:
196
207
.
Bowman
J,
Tamlin
AL.
2007
.
The effect of sinus nematode infection on braincase volume and cranium shape in the mink
.
J Mammal
88
:
946
950
.
Bush
AO,
Lafferty
KD,
Lotz
JM,
Shostak
AW.
1997
.
Parasitology meets ecology on its own terms: Margolis et al. revisited
.
J Parasitol
83
:
575
583
.
Carreno
RA,
Reif
KE,
Nadler
SA.
2005
.
A new species of Skrjabingylus Petrov, 1927 (Nematoda: Metastrongyloidea) from the frontal sinuses of the hooded skunk, Mephitis macroura (Mustelidae)
.
J Parasitol
91
:
102
107
.
Dragoo
JW,
Sheffield
SR.
2009
.
Conepatus leuconotus (Carnivora: Mephitidae)
.
Mamm Species
827
:
1
8
.
Dubay
S,
Buchholz
MJ,
Lisiecki
R,
Huspeni
T,
Ginnett
T,
Haen
L,
Borsdorf
P.
2014
.
Prevalence and intensity of nematode parasites in Wisconsin ermine
.
J Parasitol
100
:
616
622
.
Dyer
WG.
1969
.
Skrjabingylus chitwoodorum (Nematoda: Pseudaliidae) from Mephitis mephitis in central North Dakota
.
Bull Wildl Dis Assoc
5
:
140
.
Emmons
RW,
Johnson
HN.
1969
.
Sinus worm Skrjabingylus spp. (Nematoda: Pseudaliidae) from rabid skunks (Mephitis mephitis) in California
.
Am J Vet Res
30
:
1253
1254
.
Ewing
SA,
Hibbs
CM.
1966
.
The sinus worm Skrjabingylus spp. (Nematoda: Pseudaliidae), a common parasite of skunks in Kansas
.
Am J Vet Res
27
:
1783
1785
.
Fuller
TK,
Kuehn
DW.
1984
.
Skrjabingylus chitwoodorum Hill, 1939 (Nematoda: Metastrongyloidea) in striped skunks from Northcentral Minnesota
.
J Wildl Dis
20
:
348
350
.
Gehrt
SD.
2005
.
Seasonal survival and cause-specific mortality of urban and rural striped skunks in the absence of rabies
.
J Mammal
86
:
1164
1170
.
Gerht
SD,
Kinsel
MJ,
Anchor
C.
2010
.
Pathogen dynamics and morbidity of striped skunks in the absence of rabies
.
J Wildl Dis
46
:
335
347
.
Goble
FC.
1942
.
Skrjabingylus chitwoodorum from the frontal sinuses of Mephitis nigra in New York
.
J Mammal
23
:
96
97
.
Goble
FC,
Cook
AH.
1942
.
Notes on nematodes from the lungs and frontal sinuses of New York fur-bearers
.
J Parasitol
28
:
451
455
.
Goldberg
A.
1954
.
Parasites of skunks in the Beltsville, Maryland, area
.
Proc Helminthol Soc Wash
21
:
29
34
.
Griffith
G,
Bryce
S,
Omernik
J,
Rogers
A.
2007
.
Ecoregions of Texas: Project report to Texas Commission on Environmental Quality
.
Hansson
I.
1968
.
Cranial helminth parasites in species of Mustelidae, I: Frequency and damage in fresh mustelids from Sweden
.
Oikos
19
:
217
233
.
Hansson,
I.
1974
.
Seasonal and environmental conditions affecting the invasion of mustelids by larvae of the nematode Skrjabingylus nasicola
.
Oikos
25
:
61
70
.
Hill
WC.
1939
.
The nematode Skrjabingylus chitwoodorum n. sp. from the skunk
.
J Parasitol
25
:
475
476
.
Hughes
MR.
2016
.
Prevalence and intensity of the sinus roundworm, Skrjabingylus chitwoodorum, in rabies-negative skunks from Texas
.
MS Thesis
,
Department of Biology
,
Angelo State University, San Angelo, Texas
,
26
pp
.
King
CM,
Moody
JE.
1982
.
The biology of the stoat (Mustela ermine) in the National Parks of New Zealand, VI: Infestation with Skrjabingylus nasicola
.
N Z J Zool
9
:
131
139
.
Kirkland
GL
Jr.
1975
.
Parasitosis of the striped skunk (Mephitis mephitis) in Pennsylvania by the nasal nematode, Skrjabingylus chitwoodorum
.
Proc Pa Acad Sci
49
:
51
53
.
Kirkland
GL
Jr,
Kirkland
CJ.
1983
.
Patterns of variation in cranial damage in skunks (Mustelidae: Mephitinae) presumably caused by nematodes of the genus Skrjabingylus Petrov 1927 (Metastrongyloidea)
.
Can J Zool
6
:
2913
2920
.
Kirkland
GL
Jr,
Maldonado
JE.
1988
.
Patterns of variation in cranial damage attributable to Skrjabingylus sp. (Nematoda, Metastrongyloidea) in skunks (Mammalia, Mustelidae) from Mexico
.
Southwest Nat
33
:
15
20
.
Lankester
MW.
1983
.
Skrjabingylus Petrov, 1927 (Nematoda: Metastrongyloidea) emended with redescriptions of S. nasicola (Leuckart, 1842) and S. chitwoodorum Hill, 1939 from North American mustelids
.
Can J Zool
61
:
2168
2178
.
Lankester
MW,
Anderson
RC.
1971
.
The route of migration and pathogenesis of Skrjabingylus spp. (Nematoda: Metastrongyloidea) in mustelids
.
Can J Zool
49
:
1283
1293
.
Levine
ND,
Ivens
V,
Barr
TRB,
Verts
BJ.
1962
.
Skrjabingylus chitwoodorum (Nematoda: Metastrongylidae) in skunks in Illinois
.
Trans Ill State Acad Sci
55
:
3
5
.
Maldonado
JE,
Kirkland
GL
Jr.
1986
.
Relationship between cranial damage attributable to Skrjabingylus (Nematoda) and braincase capacity in the striped skunk (Mephitis mephitis)
.
Can J Zool
64
:
2004
2007
.
Mead
RA.
1963
.
Some aspects of parasitism in skunks of the Sacramento Valley of California
.
Am Midl Nat
70
:
164
167
.
Neiswenter
SA,
Pence
DB,
Dowler
RC.
2006
.
Helminths of sympatric striped, hog-nosed, and spotted skunks in West-central Texas
.
J Wildl Dis
42
:
511
517
.
Patton
RF.
1974
.
Ecological and behavioral relationships of the skunks of Trans Pecos Texas
.
PhD Thesis
,
Texas A&M University
,
College Station, Texas
,
199
pp
.
R Development Core Team
.
2015
.
R: A language and environment for statistical computing
.
R Foundation for Statistical Computing
,
Vienna, Austria
.
http://www.R-project.org. Accessed January 2016
.
Rosen
MD,
Sarnat
BG.
1954
.
A comparison of the volume of the left and right maxillary sinuses in dogs
.
Anat Rec
120
:
65
71
.
Santi
SA,
Parker
GH,
Schaffner
NP,
Capodagli
L,
Persinger
MA.
2006
.
Prevalence, intensity and geographic distribution of sinus worm (Skrjabingylus nasicola) infection in mink (Mustela vison) of central Ontario
.
Can J Zool
84
:
1011
1018
.
Santi
SA,
Parker
GH.
2012
.
Biology of sinus worm (Skrjabingylus) infections in mustelid species: Sinus worm (Skrjabingylus) infections in mustelids
.
Lambert Academic Publishing
,
Saarbrücken, Germany
,
157
pp
.
Schneider
CA,
Rasband
WS,
Eliceiri,
KW.
2012
.
NIH Image to ImageJ: 25 years of image analysis
.
Nat Methods
9
:
671
675
.
Swales
WE.
1938
.
Skrjabingylus nasicola (Leuckart, 1842) Petrov, 1927, a nematode parasitic in the frontal sinuses of American Mustelidae
.
In
:
Livre jubilar do Professor Lauro Travassos. Editado para commemorar o 25 anniversario de suas actividades scientificas (1913–1938)
.
Typographia Instituto Oswaldo Cruz
,
Rio de Janeiro, Brazil
,
pp
.
455
458
.
Tiner
JD.
1946
.
Some helminth parasites of skunks in Texas
.
J Mammal
27
:
82
83
.
Texas Department of State Health Services
.
2017
.
Rabies surveillance in Texas
. .
Van de Graaff
KM.
1969
.
Comparative osteology of skunks of the world
.
MS Thesis
,
University of Utah
,
Salt Lake City, Utah
,
272
pp
.
Verts
BJ.
1967
.
The biology of the striped skunk
.
University of Illinois Press
,
Urbana, Illinois
,
218
pp
.
Weber
JM,
Mermod
C.
1985
.
Quantitative aspects of the life cycle of Skrjabingylus nasicola, a parasitic nematode of the frontal sinuses of mustelids
.
Z Parasitenkd
71
:
631
638
.
Webster
WA.
1965
.
Skrjabingylus magnus n. sp. (Nematoda: Trichostrongylidae) from the skunk, Mephitis mephitis
.
Can J Zool
43
:
229
231
.