The synlophe of Nematodirus neotoma from Neotoma spp. is characterized. The cervical synlophe is composed of 30-32 and 36-42 ridges in males and females, respectively. Of these, 14 and 20-22 ridges are continuous in the cervical zone and extend to the base of the cephalic expansion. Six pairs of lateral ridges are discontinuous but extend greater than one-third the length of the cervical region. In both males and females, the number of ridges increases posteriad, terminating near the bursa in the male, and extending the entire length of the body in the female. The synonymy of N. neotoma and N. tortuosus was confirmed

Hoberg, Eric P.

Rickard, Lora G.

Zimmerman, Gary L.

English

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University of Nebraska - LincolnDigitalCommons@University of Nebraska - LincolnFaculty Publications from the Harold W. ManterLaboratory of Parasitology Parasitology, Harold W. Manter Laboratory of1988Synlophe of Nematodirus neotoma(Trichostrongyloidea)Eric P. HobergUnited States Department of Agriculture, Agricultural Research Service, geocolonizer@gmail.comLora G. RickardOregon State UniversityGary L. ZimmermanOregon State UniversityFollow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubsPart of the Parasitology CommonsThis Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University ofNebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorizedadministrator of DigitalCommons@University of Nebraska - Lincoln.Hoberg, Eric P.; Rickard, Lora G.; and Zimmerman, Gary L., "Synlophe of Nematodirus neotoma (Trichostrongyloidea)" (1988).Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 804.http://digitalcommons.unl.edu/parasitologyfacpubs/804J. Parasit., 74(4), 1988, pp. 686-691 ? American Society of Parasitologists 1988 SYNLOPHE OF NEMATODIRUS NEOTOMA (TRICHOSTRONGYLOIDEA) Eric P. Hoberg, Lora G. Rickard*, Gary L. Zimmerman College of Veterinary Medicine, Oregon State University, Corvallis, Oregon 97331 ABSTRACT: he synlophe of Nematodirus neotoma from Neotoma spp. is characterized. The cervical synlophe is composed of 30-32 and 36-42 ridges in males and females, respectively. Of these, 14 and 20-22 ridges are continuous in the cervical zone and extend to the base of the cephalic expansion. Six pairs of lateral ridges are discontinuous but extend greater than one-third the length of the cervical region. In both males and females, the number of ridges increases posteriad, terminating near the bursa in the male, and extending the entire length of the body in the female. The synonymy of N. neotoma and N. tortuosus was confirmed. Studies have indicated the importance of the synlophe as a character in trichostrongyloid sys- tematics (Durette-Desset, 1971, 1985; Lichten- fels and Pilitt, 1983; Rossi, 1983; and others). Among Nematodirus spp. (Trichostrongyloidea: Nematodirinae), detailed studies of the synlophe have largely been limited to those species para- sitic in ruminants (Durette-Desset, 1978, 1979; Lichtenfels and Pilitt, 1983; Rossi, 1983; Hoberg et al., 1986; Hoberg and Rickard, 1988). Nematodirus neotoma Hall, 1916, and N. tor- tuosus Tucker, 1941, were originally described from woodrats in Colorado (Neotoma deserto- rum Cary, N. mexicana fallax Merriam, N. flor- idana baileyi Merriam, and N. cinerea rupicola Allen) and California (N. lepida intermedia Rhoads and N. fuscipes macrotis Thomas), re- spectively (Hall, 1916; Tucker, 1942). Miller and Schmidt (1982) reduced N. tortuosus as a syn- onym of N. neotoma. Although N. neotoma can be differentiated from its congeners based on current descriptions, the synlophe and cephalic structures were never defined in previous studies. In the study reported herein, the synlophe and cephalic structures of N. neotoma are described, and the synlophe is compared with that of other Nematodirus spp. The occurrence of N. neotoma in a host-group not typical of its congeners is discussed with ref- erences to parasite morphology and parasite-host Received 20 October 1987; revised 6 January 1988; accepted 15 February 1988. * Department of General Science, Oregon State Uni- versity, Corvallis, Oregon 97331. biogeography. Additionally, the synonymy of N. neotoma and N. tortuosus is confirmed based on characteristics of the synlope in the cervical re- gion. MATERIALS AND METHODS The description of the synlophe and cephalic struc- tures is consistent with the methodology and termi- nology presented by Lichtenfels and Pilitt (1983). In the description, the cervical region is the zone extend- ing anteriad from the cervical papillae and excretory pore to the posterior margin of the cephalic expansion. Specimens of Nematodirus neotoma were examined using interference contrast microscopy (Leitz) and scanning electron microscopy. Prior to examination, material for light microscopy was transferred to 70% ethanol/5% glycerine and cleared in glycerine by evap- oration. Ten specimens of each sex were prepared as temporary whole mounts, and 5 specimens of each sex were studied in transverse sections cut by hand with a scalpel blade. Eight male and 7 female specimens were examined using SEM (stubs submitted to the USNM Helm. Coll. No. 75507). All measurements are in ,um unless stated otherwise. Specimens examined: Nematodirus tortuosus: 2 male specimens (type) from Neotoma spp. at West Los An- geles, California, USNM Helm. Coll. No. 36717. Ne- matodirus neotoma: male and female specimens from Neotoma cinerea rupicola at northern Weld County, Colorado, and southeastern Laramie County, Wyo- ming, 15 October 1979 (borrowed from collection of G. D. Schmidt, Nos. GK-7 and GK-8). RESULTS Cuticular morphology of N. neotoma (Figs. 1-16) Synlophe: At the level of the esophagus and cervical papillae, the synlophe of N. neotoma consists of a bi- laterally symmetrical system of 30-32 ridges in males and 36-42 ridges in females. The fine lateralmost cer- vical ridges originate 1,000-1,500 from the cephalic FIGURES 1-4. Synlophe of Nematodirus neotoma. Scale = 100 /m, same for Figures 1, 2, and 4. 1. Male, cervical synlophe, right lateral view (excretory pore = exp, cervical papilla = cp, and esophagus = es). Origin of fine lateralmost ridge not shown. 2. Female, cervical synlophe, right lateral view. 3. Schematic of transverse section showing synlophe at level of cervical papilla and esophagus in male (not to scale). 4. Synlophe of N. tortuosus (=N. neotoma), right lateral view in male (type). 686 Hoberg, Rickard & Zimmerman in Journal of Parasitology (1988) 74(4): 686-691. Copyright 1988, American Society of Parasitologists. Used by permission.HOBERG ET AL.-SYNLOPHE OF NEMATODIRUS 687 4 -a m O 3 688 THE JOURNAL OF PARASITOLOGY, VOL. 74, NO. 4, AUGUST 1988 FIGUREs 5-10. Scanning electron microscopy of N. neotoma. All scales = 10 Am. 5. Cervical synlophe, left lateral view, showing left cervical papilla (cp) and excretory pore (ex). 6. Cervical synlophe, right lateral view, showing pattern of discontinuous ridges anterior to cervical papilla. 7. En face view of female, showing 20 continuous ridges extending to the base of the cephalic expansion. 8. Detail of synlophe at base of cephalic expansion showing termination of cervical ridges and transverse striations on cephalic expansion. 9. Caudal extremity of female showing minute cuticular ridges adjacent to tail extending posteriad to the vulva. Arrows indicate points of termination for individual ridges. 10. En face view of cephalic extremity of female showing perioral denticles, papillae of inner circle (ic), and amphids (a). expansion. The right lateral ridge is occasionally in- terrupted at the level of the cervical papilla. The sev- enth and eighth ventral ridge is interrupted at the ex- cretory pore in males and females, respectively. Fourteen ridges in males and 20-22 ridges in females are continuous in the cervical zone and terminate at the base of the cephalic expansion. Six pairs of lateral ridges extend greater than one-third the cervical dis- tance but terminate before reaching the cephalic ex- pansion. All ridges are perpendicular and there is no gradient in height. Posteriad from the cervical zone the numbers of ridges increase in both males and females. Slightly anterior to the midbody in males there are 35-36 ridges; at the midbody, 39-40. At the level of the proximal end of the spicules, there are 47-49 ridges; dorsally, the ridges become markedly reduced in height. The synlophe ter- minates 350-400 from the bursa. At the midbody in females, the synlophe is composed of 47-55 ridges; maximum observed posterior to this region is about 60 ridges. Within a distance of 500 anterior to the vulva, the dorsal ridges become reduced in height. Al- though markedly attenuated posterior to the vulva, and not generally discernible with light microscopy, the synlophe extends to the caudal extremity of females. Cephalic structures: Cephalic expansion longer than wide, with slight swelling in anterior and distinct trans- verse striations in posterior. Papillae of internal circle 6 in number, with sclerotized semicircular supports. Papillae of the external circle indistinct. Perioral den- HOBERG ET AL.-SYNLOPHE OF NEMATODIRUS 689 FIGURES 11-16. Transverse sections of N. neotoma showing distribution of cuticular ridges. All figures are oriented with dorsal toward top; arrows indicate dorsal (d), ventral (v), and lateral ridges (1 = left; r = right); all scales = 30 Am. 11. Cervical region of male with 32 ridges; note small ridges laterally. 12: Midbody region of male with 39 ridges. 13. Posterior region of male at level of proximal end of spicules showing 43 ridges. 14. Cervical region of female with 41 ridges. 15. Midbody region of female (cut at 11.5 mm from anterior in specimen measuring 23.18 mm) showing 53 ridges. 16. Posterior to midbody (12.4 mm from anterior) showing 54 ridges; synlophe is no longer easily discernible in interference contrast beyond this point. ticles 42-52 (46) (n = 4) in number for males, 46-59 (52) (n = 7) for females. Comparison with Nematodirus tortuosus: The numbers of ridges in the type specimens of N. tortuosus could not be accurately determined. However, the pat- tern of the cervical synlophe, particularly the extent of the lateral ridges and origin and form of the lateralmost ridge appeared identical to that observed in specimens of N. neotoma. DISCUSSION present study, as determined by light micros- copy, was generally similar to that reported pre- viously. Although the number of perioral den- ticles was greater (42-52 for males; 46-59 for females) than that reported by Durette-Desset (1979), this and other differences in the numbers of ridges are considered as intraspecific variation. Based on these characters, the synonymy of N. neotoma and N. tortuosus is confirmed. Previous descriptions of Nematodirus spp. from The number and longitudinal extent of ridges cricetids did not consider details of the synlophe. comprising the synlophe of N. neotoma in the Hall (1916), in describing N. neotoma, reported 690 THE JOURNAL OF PARASITOLOGY, VOL. 74, NO. 4, AUGUST 1988 the presence of longitudinal lines in males and females. Tucker (1942) described longitudinal ridges throughout the length of males of N. tor- tuosus, whereas in females, the synlophe was confined to the region anterior to the vulva. Du- rette-Desset (1979) elucidated some details of the synlophe in N. tortuosus. The numbers of ridges increased posteriad attaining a maximum of 40- 56 in males and 52-61 in females. The synlophe terminated within 400 Am of the vulva in females and 1,000 um from the bursa in males. Addi- tionally, about 40 perioral denticles were enu- merated. Recently, Miller and Schmidt (1982) reported 22-48 and 26-68 ridges in males and females of N. neotoma, respectively (presumably a range from anterior to posterior). The synlophe in female specimens was observed to extend pos- teriad to the vulva. Considering the other species of Nematodirus previously examined, N. neotoma is character- ized by a substantially greater number of cervical and midbody ridges. The synlophe in the cervical region (anterior to the cervical papillae) has been characterized for only 8 species of Nematodirus that are parasites of the Bovidae (Lichtenfels and Pilitt, 1983; Hoberg et al., 1986; Hoberg and Rickard, 1988). A bilateral system of 16 ridges was found in N. maculosus Becklund, 1965, an 18-ridge system was typical of N. filicollis (Rud- olphi, 1802), N. davtiani Grigorian, 1949, N. or- atianus (Raevskaia, 1929), N. abnormalis May, 1920, N. spathiger (Railliet, 1896), and N. battus Crofton and Thomas, 1951, and 26 ridges were reported for N. helvetianus May, 1920 (lateral- most extending less than one-third of the cervical distance). The midbody region has been exam- ined in 16 species of Nematodirus from the Bovi- dae, Cervidae, and Camelidae (Becklund, 1963; Durette-Desset, 1978,1979; Rossi, 1983). Among these only 4 species have 30 or more ridges at the level of the midbody, viz. N. helvetianus (30- 36) from bovids, N. europeus Jansen, 1972 (33- 36), N. roscidus Railliet, 1911 (34), from pale- arctic cervids, and N. lamae Becklund, 1963, from neotropical camelids (approximately 40). Addi- tionally, N. odocoilei Becklund and Walker, 1967, from nearctic cervids has 34-42 ridges at the midbody (Hoberg, unpubl. data). Species of Nematodirus generally are parasites of the Artiodactyla and only 2 species are known from rodents (see Kulmamatov, 1974; Durette- Desset, 1979). In addition to N. neotoma from Neotoma spp., N. mugosaricus Schulz, 1926, was described from Citellus in the Soviet Union (Skrjabin et al., 1954). The distribution of these species appears to represent independent events of colonization of cricetids and sciurids by species of Nematodirus typical of ruminants (see Dur- ette-Desset, 1979). The widespread distribution of N. neotoma among Neotoma spp. in western North America could indicate that Nematodirus became para- sites of woodrats prior to geographic isolation resulting in speciation and subspeciation of the host-group in the Pleistocene (see Kurten and Anderson, 1980). Morphologically, the synlophe of N. neotoma appears most similar to some species characterized by a high number of ridges from camelids or cervids (Rossi, 1983; Hoberg, unpubl.). Current evidence thus suggests a pos- sible switch from either of these host-groups to Neotoma. Additional study involving phyloge- netic analyses will be required to evaluate the degree of relationship among N. neotoma and other Nematodirus spp. ACKNOWLEDGMENTS Partial funding for this study was provided by a grant from the General Research Council, Or- egon State University. Dr. J. R. Lichtenfels kind- ly provided specimens of N. tortuosus from the USNM Helminthological Collection, USDA, Beltsville, Maryland. This study would not have been possible without specimens of N. neotoma kindly provided by Dr. G. D. Schmidt. Scanning electon microscopy was conducted with Mr. A. H. Soeldner at the Electron Microscopy Facility, Oregon State University. Published as Oregon Agricultural Experiment Station Technical Pa- per No. 8341, Oregon State University. LITERATURE CITED BECKLUND, W. W. 1963. Lamanema chavezi gen. n., sp. n. and Nematodirus lamae sp. n. (Nematoda: Trichostrongylidae) from the alpaca, Lama pacos, and the vicufia, Vicugna vicugna, in Peru. Journal of Parasitology 49: 1023-1027. DURETTE-DESSET, M. C. 1971. Essai de classification des N6matodes Heligmosomes. Corr6elation avec la paleobiogeographie des h6tes. Memoires Mu- seum National Histoire Naturelle nlle. ser.; s6r. A Zoology 49, 126 p. ? 1978. Nouvelles donn6es morphologiques sur des N6matods Trichostrongyloides des collections du United States National Museum. Bulletin Mu- seum National Histoire Naturelle, Paris, Zoologie 352: 135-147. . 1979. Les Nematodirinae (Nematoda) chez HOBERG ET AL.-SYNLOPHE OF NEMATODIRUS 691 les ruminants et chez les lagomorphes. Annales de Parasitologie Humaine et Comparee 54: 313-329. ? 1985. Trichostrongyloidnematodesandtheir vertebrate hosts: Reconstruction of the phylogeny of a parasitic group. Advances in Parasitology 24: 239-306. HALL, M. C. 1916. Nematode parasites of mammals of the orders Rodentia, Lagomorpha and Hyra- coidea. Proceedings of the United States National Museum 50: 1-258. HOBERG, E. P., AND L. G. RICKARD. 1988. Mor- phology of the synlophe of Nematodirus maculo- sus (Trichostrongyloidea) with comments on the evolution of Nematodirus spp. among the Capri- nae (Artiodactyla). Proceedings of the Helmin- thological Society of Washington 55: in press. , G. L. ZIMMERMAN, D J. R. LICHTENFELS. 1986. First report of Nematodirus battus (Nem- atoda: Trichostrongyloidea) in North America: Redescription and comparison to other species. Proceedings of the Helminthological Society of Washington 53: 80-88. KULMAMATOV, A. 1974. 0 vidovom sostave roda Nematodirus Ransom 1907. Materialy Nauch- nykh Konferentsii Vsesouznogo Obshchestva Gel'mintologov 26: 137-140. KURTEN, B., AND E. ANDERSON. 1980. Pleistocene mammals of North America. Columbia Univer- sity Press, New York. LICHTENFELS, J. R., AND) P. A. PILIT. 1983. Cuticular ridge patterns ofNematodirus (Nematoda: Tricho- strongyloidea) parasitic in domestic ruminants of North America, with a key to species. Proceedings of the Helminthological Society of Washington 50: 261-274. MILLER, G. E., AND G. D. SCHMIDT. 1982. Helminths of bushy-tailed woodrats, Neotoma cinerea subspp. from Colorado, Idaho, and Wyoming. Proceedings of the Helminthological Society of Washington 49:109-117. Rossi, P. 1983. Sur le genre Nematodirus Ransom, 1907 (Nematoda: Trichostrongyloidea). Annales de Parasitologie Humaine et Comparee 58: 557- 581. SKRJABIN, K. I., N. P. SmlKHOBALOVA, AND R. S. SHULTS. 1954. Essentials of nematodology, Vol. 3. Acad- emy of Sciences of the USSR. [English translation by the Israel Program for Scientific Translations, 1960.] TUCKER, H. 1942. Nematodirus tortuosus n. sp. (Nematoda) from the rat, Neotoma. Journal of Parasitology 28: 159-163. 

Synlophe of \u3ci\u3eNematodirus neotoma\u3c/i\u3e (Trichostrongyloidea)

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University of Nebraska - Lincoln
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Faculty Publications from the Harold W. Manter
Laboratory of Parasitology Parasitology, Harold W. Manter Laboratory of
1988
Synlophe of Nematodirus neotoma
(Trichostrongyloidea)
Eric P. Hoberg
United States Department of Agriculture, Agricultural Research Service, geocolonizer@gmail.com
Lora G. Rickard
Oregon State University
Gary L. Zimmerman
Oregon State University
Follow this and additional works at: http://digitalcommons.unl.edu/parasitologyfacpubs
Part of the Parasitology Commons
This Article is brought to you for free and open access by the Parasitology, Harold W. Manter Laboratory of at DigitalCommons@University of
Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Harold W. Manter Laboratory of Parasitology by an authorized
administrator of DigitalCommons@University of Nebraska - Lincoln.
Hoberg, Eric P.; Rickard, Lora G.; and Zimmerman, Gary L., "Synlophe of Nematodirus neotoma (Trichostrongyloidea)" (1988).
Faculty Publications from the Harold W. Manter Laboratory of Parasitology. 804.
http://digitalcommons.unl.edu/parasitologyfacpubs/804
J. Parasit., 74(4), 1988, pp. 686-691 
? American Society of Parasitologists 1988 
SYNLOPHE OF NEMATODIRUS NEOTOMA (TRICHOSTRONGYLOIDEA) 
Eric P. Hoberg, Lora G. Rickard*, Gary L. Zimmerman 
College of Veterinary Medicine, Oregon State University, Corvallis, Oregon 97331 
ABSTRACT: he synlophe of Nematodirus neotoma from Neotoma spp. is characterized. The cervical synlophe 
is composed of 30-32 and 36-42 ridges in males and females, respectively. Of these, 14 and 20-22 ridges are 
continuous in the cervical zone and extend to the base of the cephalic expansion. Six pairs of lateral ridges are 
discontinuous but extend greater than one-third the length of the cervical region. In both males and females, 
the number of ridges increases posteriad, terminating near the bursa in the male, and extending the entire length 
of the body in the female. The synonymy of N. neotoma and N. tortuosus was confirmed. 
Studies have indicated the importance of the 
synlophe as a character in trichostrongyloid sys- 
tematics (Durette-Desset, 1971, 1985; Lichten- 
fels and Pilitt, 1983; Rossi, 1983; and others). 
Among Nematodirus spp. (Trichostrongyloidea: 
Nematodirinae), detailed studies of the synlophe 
have largely been limited to those species para- 
sitic in ruminants (Durette-Desset, 1978, 1979; 
Lichtenfels and Pilitt, 1983; Rossi, 1983; Hoberg 
et al., 1986; Hoberg and Rickard, 1988). 
Nematodirus neotoma Hall, 1916, and N. tor- 
tuosus Tucker, 1941, were originally described 
from woodrats in Colorado (Neotoma deserto- 
rum Cary, N. mexicana fallax Merriam, N. flor- 
idana baileyi Merriam, and N. cinerea rupicola 
Allen) and California (N. lepida intermedia 
Rhoads and N. fuscipes macrotis Thomas), re- 
spectively (Hall, 1916; Tucker, 1942). Miller and 
Schmidt (1982) reduced N. tortuosus as a syn- 
onym of N. neotoma. 
Although N. neotoma can be differentiated 
from its congeners based on current descriptions, 
the synlophe and cephalic structures were never 
defined in previous studies. In the study reported 
herein, the synlophe and cephalic structures of 
N. neotoma are described, and the synlophe is 
compared with that of other Nematodirus spp. 
The occurrence of N. neotoma in a host-group 
not typical of its congeners is discussed with ref- 
erences to parasite morphology and parasite-host 
Received 20 October 1987; revised 6 January 1988; 
accepted 15 February 1988. 
* Department of General Science, Oregon State Uni- 
versity, Corvallis, Oregon 97331. 
biogeography. Additionally, the synonymy of N. 
neotoma and N. tortuosus is confirmed based on 
characteristics of the synlope in the cervical re- 
gion. 
MATERIALS AND METHODS 
The description of the synlophe and cephalic struc- 
tures is consistent with the methodology and termi- 
nology presented by Lichtenfels and Pilitt (1983). In 
the description, the cervical region is the zone extend- 
ing anteriad from the cervical papillae and excretory 
pore to the posterior margin of the cephalic expansion. 
Specimens of Nematodirus neotoma were examined 
using interference contrast microscopy (Leitz) and 
scanning electron microscopy. Prior to examination, 
material for light microscopy was transferred to 70% 
ethanol/5% glycerine and cleared in glycerine by evap- 
oration. Ten specimens of each sex were prepared as 
temporary whole mounts, and 5 specimens of each sex 
were studied in transverse sections cut by hand with a 
scalpel blade. Eight male and 7 female specimens were 
examined using SEM (stubs submitted to the USNM 
Helm. Coll. No. 75507). All measurements are in ,um 
unless stated otherwise. 
Specimens examined: Nematodirus tortuosus: 2 male 
specimens (type) from Neotoma spp. at West Los An- 
geles, California, USNM Helm. Coll. No. 36717. Ne- 
matodirus neotoma: male and female specimens from 
Neotoma cinerea rupicola at northern Weld County, 
Colorado, and southeastern Laramie County, Wyo- 
ming, 15 October 1979 (borrowed from collection of 
G. D. Schmidt, Nos. GK-7 and GK-8). 
RESULTS 
Cuticular morphology of N. neotoma 
(Figs. 1-16) 
Synlophe: At the level of the esophagus and cervical 
papillae, the synlophe of N. neotoma consists of a bi- 
laterally symmetrical system of 30-32 ridges in males 
and 36-42 ridges in females. The fine lateralmost cer- 
vical ridges originate 1,000-1,500 from the cephalic 
FIGURES 1-4. Synlophe of Nematodirus neotoma. Scale = 100 /m, same for Figures 1, 2, and 4. 1. Male, 
cervical synlophe, right lateral view (excretory pore = exp, cervical papilla = cp, and esophagus = es). Origin 
of fine lateralmost ridge not shown. 2. Female, cervical synlophe, right lateral view. 3. Schematic of transverse 
section showing synlophe at level of cervical papilla and esophagus in male (not to scale). 4. Synlophe of N. 
tortuosus (=N. neotoma), right lateral view in male (type). 
686 
Hoberg, Rickard & Zimmerman in Journal of Parasitology (1988) 74(4): 686-691. 
Copyright 1988, American Society of Parasitologists. Used by permission.
HOBERG ET AL.-SYNLOPHE OF NEMATODIRUS 687 
4 
-a 
m 
O 
3 
688 THE JOURNAL OF PARASITOLOGY, VOL. 74, NO. 4, AUGUST 1988 
FIGUREs 5-10. Scanning electron microscopy of N. neotoma. All scales = 10 Am. 5. Cervical synlophe, left 
lateral view, showing left cervical papilla (cp) and excretory pore (ex). 6. Cervical synlophe, right lateral view, 
showing pattern of discontinuous ridges anterior to cervical papilla. 7. En face view of female, showing 20 
continuous ridges extending to the base of the cephalic expansion. 8. Detail of synlophe at base of cephalic 
expansion showing termination of cervical ridges and transverse striations on cephalic expansion. 9. Caudal 
extremity of female showing minute cuticular ridges adjacent to tail extending posteriad to the vulva. Arrows 
indicate points of termination for individual ridges. 10. En face view of cephalic extremity of female showing 
perioral denticles, papillae of inner circle (ic), and amphids (a). 
expansion. The right lateral ridge is occasionally in- 
terrupted at the level of the cervical papilla. The sev- 
enth and eighth ventral ridge is interrupted at the ex- 
cretory pore in males and females, respectively. 
Fourteen ridges in males and 20-22 ridges in females 
are continuous in the cervical zone and terminate at 
the base of the cephalic expansion. Six pairs of lateral 
ridges extend greater than one-third the cervical dis- 
tance but terminate before reaching the cephalic ex- 
pansion. All ridges are perpendicular and there is no 
gradient in height. 
Posteriad from the cervical zone the numbers of ridges 
increase in both males and females. Slightly anterior 
to the midbody in males there are 35-36 ridges; at the 
midbody, 39-40. At the level of the proximal end of 
the spicules, there are 47-49 ridges; dorsally, the ridges 
become markedly reduced in height. The synlophe ter- 
minates 350-400 from the bursa. At the midbody in 
females, the synlophe is composed of 47-55 ridges; 
maximum observed posterior to this region is about 
60 ridges. Within a distance of 500 anterior to the 
vulva, the dorsal ridges become reduced in height. Al- 
though markedly attenuated posterior to the vulva, and 
not generally discernible with light microscopy, the 
synlophe extends to the caudal extremity of females. 
Cephalic structures: Cephalic expansion longer than 
wide, with slight swelling in anterior and distinct trans- 
verse striations in posterior. Papillae of internal circle 
6 in number, with sclerotized semicircular supports. 
Papillae of the external circle indistinct. Perioral den- 
HOBERG ET AL.-SYNLOPHE OF NEMATODIRUS 689 
FIGURES 11-16. Transverse sections of N. neotoma showing distribution of cuticular ridges. All figures are 
oriented with dorsal toward top; arrows indicate dorsal (d), ventral (v), and lateral ridges (1 = left; r = right); all 
scales = 30 Am. 11. Cervical region of male with 32 ridges; note small ridges laterally. 12: Midbody region of 
male with 39 ridges. 13. Posterior region of male at level of proximal end of spicules showing 43 ridges. 14. 
Cervical region of female with 41 ridges. 15. Midbody region of female (cut at 11.5 mm from anterior in specimen 
measuring 23.18 mm) showing 53 ridges. 16. Posterior to midbody (12.4 mm from anterior) showing 54 ridges; 
synlophe is no longer easily discernible in interference contrast beyond this point. 
ticles 42-52 (46) (n = 4) in number for males, 46-59 
(52) (n = 7) for females. 
Comparison with Nematodirus tortuosus: The 
numbers of ridges in the type specimens of N. tortuosus 
could not be accurately determined. However, the pat- 
tern of the cervical synlophe, particularly the extent of 
the lateral ridges and origin and form of the lateralmost 
ridge appeared identical to that observed in specimens 
of N. neotoma. 
DISCUSSION 
present study, as determined by light micros- 
copy, was generally similar to that reported pre- 
viously. Although the number of perioral den- 
ticles was greater (42-52 for males; 46-59 for 
females) than that reported by Durette-Desset 
(1979), this and other differences in the numbers 
of ridges are considered as intraspecific variation. 
Based on these characters, the synonymy of N. 
neotoma and N. tortuosus is confirmed. 
Previous descriptions of Nematodirus spp. from 
The number and longitudinal extent of ridges cricetids did not consider details of the synlophe. 
comprising the synlophe of N. neotoma in the Hall (1916), in describing N. neotoma, reported 
690 THE JOURNAL OF PARASITOLOGY, VOL. 74, NO. 4, AUGUST 1988 
the presence of longitudinal lines in males and 
females. Tucker (1942) described longitudinal 
ridges throughout the length of males of N. tor- 
tuosus, whereas in females, the synlophe was 
confined to the region anterior to the vulva. Du- 
rette-Desset (1979) elucidated some details of the 
synlophe in N. tortuosus. The numbers of ridges 
increased posteriad attaining a maximum of 40- 
56 in males and 52-61 in females. The synlophe 
terminated within 400 Am of the vulva in females 
and 1,000 um from the bursa in males. Addi- 
tionally, about 40 perioral denticles were enu- 
merated. Recently, Miller and Schmidt (1982) 
reported 22-48 and 26-68 ridges in males and 
females of N. neotoma, respectively (presumably 
a range from anterior to posterior). The synlophe 
in female specimens was observed to extend pos- 
teriad to the vulva. 
Considering the other species of Nematodirus 
previously examined, N. neotoma is character- 
ized by a substantially greater number of cervical 
and midbody ridges. The synlophe in the cervical 
region (anterior to the cervical papillae) has been 
characterized for only 8 species of Nematodirus 
that are parasites of the Bovidae (Lichtenfels and 
Pilitt, 1983; Hoberg et al., 1986; Hoberg and 
Rickard, 1988). A bilateral system of 16 ridges 
was found in N. maculosus Becklund, 1965, an 
18-ridge system was typical of N. filicollis (Rud- 
olphi, 1802), N. davtiani Grigorian, 1949, N. or- 
atianus (Raevskaia, 1929), N. abnormalis May, 
1920, N. spathiger (Railliet, 1896), and N. battus 
Crofton and Thomas, 1951, and 26 ridges were 
reported for N. helvetianus May, 1920 (lateral- 
most extending less than one-third of the cervical 
distance). The midbody region has been exam- 
ined in 16 species of Nematodirus from the Bovi- 
dae, Cervidae, and Camelidae (Becklund, 1963; 
Durette-Desset, 1978,1979; Rossi, 1983). Among 
these only 4 species have 30 or more ridges at 
the level of the midbody, viz. N. helvetianus (30- 
36) from bovids, N. europeus Jansen, 1972 (33- 
36), N. roscidus Railliet, 1911 (34), from pale- 
arctic cervids, and N. lamae Becklund, 1963, from 
neotropical camelids (approximately 40). Addi- 
tionally, N. odocoilei Becklund and Walker, 1967, 
from nearctic cervids has 34-42 ridges at the 
midbody (Hoberg, unpubl. data). 
Species of Nematodirus generally are parasites 
of the Artiodactyla and only 2 species are known 
from rodents (see Kulmamatov, 1974; Durette- 
Desset, 1979). In addition to N. neotoma from 
Neotoma spp., N. mugosaricus Schulz, 1926, was 
described from Citellus in the Soviet Union 
(Skrjabin et al., 1954). The distribution of these 
species appears to represent independent events 
of colonization of cricetids and sciurids by species 
of Nematodirus typical of ruminants (see Dur- 
ette-Desset, 1979). 
The widespread distribution of N. neotoma 
among Neotoma spp. in western North America 
could indicate that Nematodirus became para- 
sites of woodrats prior to geographic isolation 
resulting in speciation and subspeciation of the 
host-group in the Pleistocene (see Kurten and 
Anderson, 1980). Morphologically, the synlophe 
of N. neotoma appears most similar to some 
species characterized by a high number of ridges 
from camelids or cervids (Rossi, 1983; Hoberg, 
unpubl.). Current evidence thus suggests a pos- 
sible switch from either of these host-groups to 
Neotoma. Additional study involving phyloge- 
netic analyses will be required to evaluate the 
degree of relationship among N. neotoma and 
other Nematodirus spp. 
ACKNOWLEDGMENTS 
Partial funding for this study was provided by 
a grant from the General Research Council, Or- 
egon State University. Dr. J. R. Lichtenfels kind- 
ly provided specimens of N. tortuosus from the 
USNM Helminthological Collection, USDA, 
Beltsville, Maryland. This study would not have 
been possible without specimens of N. neotoma 
kindly provided by Dr. G. D. Schmidt. Scanning 
electon microscopy was conducted with Mr. A. 
H. Soeldner at the Electron Microscopy Facility, 
Oregon State University. Published as Oregon 
Agricultural Experiment Station Technical Pa- 
per No. 8341, Oregon State University. 
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Synlophe of \u3ci\u3eNematodirus neotoma\u3c/i\u3e (Trichostrongyloidea)

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