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Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematoda: Trichostrongyloidea)
331
COtfrinary Parasitology, 45 (1993) 331-335 Elsevier Science Publishers B.V.. Amsterdam
Short Communication
Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematoda: Trichostrongyloidea) Lora G. Rickard College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331-4802, USA (Accepted
11 August 1992)
ABSTRACT Rickard, L.G., 1993. Parasitic gastritis in a llama (Lama grama) associated with inhibited Teladorsagia spp. (Nematoda: Trichostrongyloidea). Vet. Parasitol., 45: 33 l-335.
larval
A 7-year-old female llama was experimentally infected with 500 Fasciola hepatica metacercariae then turned out onto pasture also grazed by domestic sheep. The llama was necropsied approximately 22 weeks post infection. Routine examination of the gastrointestinal tract revealed diffusely coalescing. umbilicated nodules covering the caudal one-fifth ofthe third stomach compartment. Microscopically, the mucosa was irregularly thickened. Numerous nematode larvae were present in glandular lumens, often extending to the base of the glands. Where nematodes were most numerous, decreased numbers of parietal cells, attenuation of glandular epithelium and increased collagen within the lamina propria were evident. Of a total of 65 10 adult nematodes in the third stomach compartment, 5 1% were Teladorsagia spp., 47% were Trichostrongylus axei, and 2% were Camelostrongylus men&la&s. Except for C. mentulatus, three sheep that had grazed with the llama and were necropsied at approximately the same time, harbored the same nematode species. The total number of larvae in the llama was 56 7 10, with more than 97% being ostertagiine early fourth-stage larvae. Ostertagiine larvae were also present in the sheep. Based on the composition of the adult populations in the llama and sheep, the larvae were considered to be species of Teladorsagia. Additionally, the larger numbers of early fourth-stage larvae indicated that the development of Teladorsagia spp. in the llama is inhibited.
Few studies concerning the parasite fauna of llamas in North America exist (Rickard and Bishop, 199 1). Of these, the pathologic changes associated with parasitism have been addressed only for Fasciola hepatica (Rickard and Foreyt, 1992), Fascioloides magna (Conboy et al., 1988; Foreyt and Parish, 1990) Correspondence to: L.G. Rickard, Corvallis, OR 97331-4802, USA.
College of Veterinary
0 1993 Elsevier Science Publishers
B.V. All rights reserved
Medicine,
Oregon
State University,
0304-4017/93/$06.00
332
L.G. RICKARD
and Parelaphostrongylus tenuis (Baumgartner et al., 1985; Krogdahl et al., 1987; Foreyt et al., 1991). This report presents the lesions associated with Teladorsagia spp. from a naturally infected, adult llama. Evidence for arrested larval development of Teladorsagia spp. occurring in the llama is also presented. In August 1989, a 7-year-old female llama was donated to the Oregon State University (OSU) College of Veterinary Medicine because of reproductive problems. Fecal examination using saturated NaCl 4 days after arrival, revealed 440 strongyle and 20 Capillaria eggs per gram of feces. The llama was infected with metacercariae of Fasciola hepatica (Baldwin Enterprises, Monmouth, OR) per OS 10 days after arrival and transported to a pasture at the OSU Veterinary Medical Animal Isolation Laboratory (see Rickard et al., 1989). With the exception of four horses and 12 Holstein calves, the pasture had been grazed only by domestic sheep over the previous 4 years. At the time the llama was turned onto the pasture, no other animals were present. She remained alone in this pasture until September 1989 when between three and six domestic sheep (also experimentally infected with Fasciola hepatica metacercariae per OS) were grazed on the pasture intermittently. The three sheep released in October remained in the field continuously until necropsy (4 January 1990 for Sheep 486 and 3 1 January for Sheep 485 and 487). The llama was necropsied on 12 January 1990. Necropsy procedures were as previously described (Rickard and Bishop, 199 1). Tissues for microscopic examination were fixed in 10% neutral buffered formalin, processed routinely and stained with hematoxylin and eosin. In comparison with the four compartment stomach of the true ruminant, the llama has a three compartment stomach. In the third compartment, there is a division between the initial four-fifths and the terminal one-fifth. The epithelium of the initial four-fifths is similar to that of the first and second compartments while that of the terminal one-fifth contains gastric and pyloric glands and is considered to be the ‘true stomach’ (Vallenas et al., 197 1). During necropsy, gross examination of the third compartment of the llama revealed numerous lesions confined to the terminal one-fifth of the segment. The lesions consisted of diffusely coalescing, umbilicated nodules involving the entire surface of the affected area. Microscopically, the mucosa was irregularly thickened as a result of hyperplasia of glandular epithelial cells, primarily those near the surface. These latter cells were increased in height and cytoplasmic volume. Numerous nematode larvae (and some adult worms) were in glandular lumens, sometimes extending to the base of the glands. Where nematodes were most numerous, decreased numbers of parietal cells, attenuation or absence of glandular epithelium and increased collagen within the lamina propria were evident. Near the surface, the lamina propria was also edematous. Lymphoid nodules were present, primarily at the junction of the mucosa and submucosa. Aggregates of eosinophils as well as individually
GASTRITIS AND TELADORSAGIA
333
IN A LLAMA
scattered eosinophils, lymphocytes and plasma cells were also present. These gross and histologic lesions are identical to those present in ostertagiasis of sheep and cattle (Reid and Murray, 1973; Armour et al., 1973). The total number of adult nematodes in the llama was 65 10 (Table 1). Species of Teladorsagia (Teladorsagia circumcincta and Teladorsagia trifurcata) and Trichostrongylus axei comprised the bulk of the population. These same species were the only ones present in the sheep (Table 1). The genus Teladorsagia was established to accommodate a species of abomasal nematode (Teladorsagia davtiana) found in domestic sheep (Ovis aries) and goats (Capra hircus) (Skrjabin et al., 1954). Teladorsagia circumcincta was originally described as Strongylus circumcinctus but was later transferred to the genus Ostertagia prior to being assigned to its present status (Drozdz, 1965 ). Teladorsagia trifircata was originally described as a species of Ostertagia prior to its transfer to Teladorsagia (DroZdz, 1965 ). While the validity of the genus Teladorsagia is accepted by many (Durrette-Desset, 1989) others retain both species within the genus Ostertagia (Lancaster et al., 1983). The total number of larvae in the llama was 56 7 IO,more than 97% of which were ostertagiine early fourth-stage larvae (Table 2 ) . Ostertagiine early fourthstage larvae were also present in the sheep, although the numbers varied. Because the majority of the adult nematodes in the population were species of TABLE 1 Species of adult nematodes recovered (expressed as a percentage of the total) from the third compartment of a naturally infected llama and abomasa of naturally infected sheep Parasite
Llama
Teladorsagia spp.’ Trichostrongylus axei Camelostrongylus mentulatus
Total number
Sheep 486
50.8
67.4
47.2 2.0
32.6 0
6510
21500
Sheep 485 0 100
Sheep 487 57.9 42.1
0
0
440
2520
‘Consisted of Teladorsagia circumcincta and Teladorsagia trifircata. TABLE 2 Larval nematodes recovered (expressed as a percentage of the total) from the third compartment a naturally infected llama and abomasa of naturally infected sheep
of
Parasite
Llama
Sheep 486
Sheep 485
Sheep 487
Teladorsagia EL: Teladorsagia DL:
91.5 2.4 0.1 56710
49.2 50.1 0.1 44060
0.4 99.6 0 9340
60.1 39.1 0.8 5720
Trichostrongylus Total number
DL4
‘EL,, early fourth-stage larvae. ‘DL4, developing fourth-stage larvae.
334
L.G. RICKARD
Teladorsagia in both the llama and sheep, the larvae were considered to belong to the same genus. The absence of ostertagiine third-stage larvae in the llama negated the possibility of recent acquisition of these large numbers of larvae. The large number of early fourth-stage larvae along with the low number of developing fourth-stage larvae and adults in the llama strongly suggest that the early fourth-stage larvae represented an inhibited population as delined by Michel ( 1974). It can be concluded that the development of species of Teladorsagia is inhibited in the llama during winter in Oregon. The significance of this finding is unknown at present. Infections of Teladorsagia spp. in sheep are associated with reduced weight gains and/or weight loss (Reid and Murray, 1973). However, in camelids, the role of hypobiosis has not been studied (Leguia, 199 1). Because the gross and histologic lesions observed in the llama were identical to those described in ostertagiasis of cattle and sheep, it is conceivable that these lesions represent a condition similar to pre-Type II ostertagiasis. However, it is not known whether these larvae would resume development and precipitate disease similar to Type II ostertagiasis. ACKNOWLEDGMENTS
The cooperation of Dr. G.L. Zimmerman help and advice of Dr. S. Snyder.
is greatly appreciated as is the
REFERENCES Armour, J., Jennings, F.W., Murray, M. and Selman, I., 1973. Bovine ostertagiasis-clinical aspects, pathogenesis, epidemiology and control. In: G.M. Urquhart and J. Armour (Editors), Helminth Diseases of Cattle, Sheep and Horses in Europe. The University Press, Glasgow, UK, pp. 1 l-27. Baumgartner, W., Zajac, A., Hull, B.L., Andrews, F. and Garry, F., 1985. Parelaphostrongylosis in llamas. J. Am. Vet. Med. Assoc., 187: 1243-l 245. Conboy, G.A., O’Brien, T.D. and Stevens, D.L., 1988. A natural infection of Fascioloides magna in a llama (Lamaglama). J. Parasitol., 74: 345-346. Drozdz, J., 1965. Studies on helminths and helminthiases in Cervidae. I. Revision of the subfamily Ostertagiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitol. Pol., 13: 445-48 1. Durrette-Desset, M.-C., 1989. Nomenclature proposee pour les expecies decrites dans sa lousfamille des Ostertagiinae Lopez-Neyra, 1947. Ann. Parasitol. Hum. Comp., 61: 356-373. Foreyt, W.J. and Parish, S., 1990. Experimental infection of liver flukes (Fascioloides magna) in a llama (Lama glarna). J. Zoo. Wildl. Med., 21: 468-470. Foreyt, W.J., Rickard, L.G., Dowling, S., Parish, S. and Pipas, M., 1991. Experimental infections of two llamas with the meningeal worm (Parelaphostrongylus tenuis). J. Zoo. Wild]. Med., 2 I: 468-470. Krogdahl, D.W., Thilsted, J.P. and Olsen, S.K., 1987. Ataxia and hypermetria caused by Pure(aphostrongylus tenuis infection in llamas. J. Am. Vet. Med. Assoc., 190: 191-193.
GASTRITIS AND TELADORSAGIA
IN A LLAMA
335
Lancaster, M.B., Hong, C. and Michel, J.F., 1983. Polymorphism in the Trichostrongylidae. In: A.R. Stone, H.M. Platt and L.F. Khalil (Editors), Concepts in Nematode Systematics Academic Press, London, pp. 293-302. Leguia, G., 199 1. The epidemiology and economic impact of llama parasites. Parasitol. Today, I: 54-56. Michel, J.F., 1974. Arrested development of nematodes and some related phenomena. Adv. Parasitol., 12: 279-366. Reid, J.F.S. and Murray, M., 1973. Ovine parasitic gastro-enteritis-clinical aspects and pathology. In: G.M. Urquhart and J. Armour (Editors), Helminth Diseases of Cattle, Sheep and Horses in Europe. The University Press, Glasgow, UK, pp. 32-35. Rickard, L.G. and Bishop, J.K., 199 1. Helminth parasites of llamas (Lama gluma) in the Pacific Northwest. J. Helminthol. Sot. Wash., 58: 110-l 15. Rickard, L.G. and Foreyt, W.J., 1992. Experimental fascioliasis in llamas. J. Helminthol. Sot. Wash., 59: 140-144. Rickard, L.G., Hoberg, E.P., Bishop, J.K. and Zimmerman, G.L., 1989. Epizootiology of Nematodirus buttus, N. jlicollis, and N. spathiger (Nematoda: Trichostrongyloidea) in western Oregon. Proc. Helminthol. Sot. Wash., 56: 104-l 15. Skrjabin, K.I., Shikhobalova, V.P. and Shults, R.S., 1954. Essentials of nematodology. Vol. 3. Trichostrongylids of Animals and Man. Academy of Sciences of the USSR, Moscow. (Translated by the Israeli Program for Scientific Translations, 1960, 704 pp.) Vallenas, A., Cummings, J.F. and Munnell, J.F., 1971. A gross study of the compartmentalized stomach of two new-world camelids, the llama and guanaco. J. Morphol., 134: 399-424.
COtfrinary Parasitology, 45 (1993) 331-335 Elsevier Science Publishers B.V.. Amsterdam
Short Communication
Parasitic gastritis in a llama (Lama glama) associated with inhibited larval Teladorsagia spp. (Nematoda: Trichostrongyloidea) Lora G. Rickard College of Veterinary Medicine, Oregon State University, Corvallis, OR 97331-4802, USA (Accepted
11 August 1992)
ABSTRACT Rickard, L.G., 1993. Parasitic gastritis in a llama (Lama grama) associated with inhibited Teladorsagia spp. (Nematoda: Trichostrongyloidea). Vet. Parasitol., 45: 33 l-335.
larval
A 7-year-old female llama was experimentally infected with 500 Fasciola hepatica metacercariae then turned out onto pasture also grazed by domestic sheep. The llama was necropsied approximately 22 weeks post infection. Routine examination of the gastrointestinal tract revealed diffusely coalescing. umbilicated nodules covering the caudal one-fifth ofthe third stomach compartment. Microscopically, the mucosa was irregularly thickened. Numerous nematode larvae were present in glandular lumens, often extending to the base of the glands. Where nematodes were most numerous, decreased numbers of parietal cells, attenuation of glandular epithelium and increased collagen within the lamina propria were evident. Of a total of 65 10 adult nematodes in the third stomach compartment, 5 1% were Teladorsagia spp., 47% were Trichostrongylus axei, and 2% were Camelostrongylus men&la&s. Except for C. mentulatus, three sheep that had grazed with the llama and were necropsied at approximately the same time, harbored the same nematode species. The total number of larvae in the llama was 56 7 10, with more than 97% being ostertagiine early fourth-stage larvae. Ostertagiine larvae were also present in the sheep. Based on the composition of the adult populations in the llama and sheep, the larvae were considered to be species of Teladorsagia. Additionally, the larger numbers of early fourth-stage larvae indicated that the development of Teladorsagia spp. in the llama is inhibited.
Few studies concerning the parasite fauna of llamas in North America exist (Rickard and Bishop, 199 1). Of these, the pathologic changes associated with parasitism have been addressed only for Fasciola hepatica (Rickard and Foreyt, 1992), Fascioloides magna (Conboy et al., 1988; Foreyt and Parish, 1990) Correspondence to: L.G. Rickard, Corvallis, OR 97331-4802, USA.
College of Veterinary
0 1993 Elsevier Science Publishers
B.V. All rights reserved
Medicine,
Oregon
State University,
0304-4017/93/$06.00
332
L.G. RICKARD
and Parelaphostrongylus tenuis (Baumgartner et al., 1985; Krogdahl et al., 1987; Foreyt et al., 1991). This report presents the lesions associated with Teladorsagia spp. from a naturally infected, adult llama. Evidence for arrested larval development of Teladorsagia spp. occurring in the llama is also presented. In August 1989, a 7-year-old female llama was donated to the Oregon State University (OSU) College of Veterinary Medicine because of reproductive problems. Fecal examination using saturated NaCl 4 days after arrival, revealed 440 strongyle and 20 Capillaria eggs per gram of feces. The llama was infected with metacercariae of Fasciola hepatica (Baldwin Enterprises, Monmouth, OR) per OS 10 days after arrival and transported to a pasture at the OSU Veterinary Medical Animal Isolation Laboratory (see Rickard et al., 1989). With the exception of four horses and 12 Holstein calves, the pasture had been grazed only by domestic sheep over the previous 4 years. At the time the llama was turned onto the pasture, no other animals were present. She remained alone in this pasture until September 1989 when between three and six domestic sheep (also experimentally infected with Fasciola hepatica metacercariae per OS) were grazed on the pasture intermittently. The three sheep released in October remained in the field continuously until necropsy (4 January 1990 for Sheep 486 and 3 1 January for Sheep 485 and 487). The llama was necropsied on 12 January 1990. Necropsy procedures were as previously described (Rickard and Bishop, 199 1). Tissues for microscopic examination were fixed in 10% neutral buffered formalin, processed routinely and stained with hematoxylin and eosin. In comparison with the four compartment stomach of the true ruminant, the llama has a three compartment stomach. In the third compartment, there is a division between the initial four-fifths and the terminal one-fifth. The epithelium of the initial four-fifths is similar to that of the first and second compartments while that of the terminal one-fifth contains gastric and pyloric glands and is considered to be the ‘true stomach’ (Vallenas et al., 197 1). During necropsy, gross examination of the third compartment of the llama revealed numerous lesions confined to the terminal one-fifth of the segment. The lesions consisted of diffusely coalescing, umbilicated nodules involving the entire surface of the affected area. Microscopically, the mucosa was irregularly thickened as a result of hyperplasia of glandular epithelial cells, primarily those near the surface. These latter cells were increased in height and cytoplasmic volume. Numerous nematode larvae (and some adult worms) were in glandular lumens, sometimes extending to the base of the glands. Where nematodes were most numerous, decreased numbers of parietal cells, attenuation or absence of glandular epithelium and increased collagen within the lamina propria were evident. Near the surface, the lamina propria was also edematous. Lymphoid nodules were present, primarily at the junction of the mucosa and submucosa. Aggregates of eosinophils as well as individually
GASTRITIS AND TELADORSAGIA
333
IN A LLAMA
scattered eosinophils, lymphocytes and plasma cells were also present. These gross and histologic lesions are identical to those present in ostertagiasis of sheep and cattle (Reid and Murray, 1973; Armour et al., 1973). The total number of adult nematodes in the llama was 65 10 (Table 1). Species of Teladorsagia (Teladorsagia circumcincta and Teladorsagia trifurcata) and Trichostrongylus axei comprised the bulk of the population. These same species were the only ones present in the sheep (Table 1). The genus Teladorsagia was established to accommodate a species of abomasal nematode (Teladorsagia davtiana) found in domestic sheep (Ovis aries) and goats (Capra hircus) (Skrjabin et al., 1954). Teladorsagia circumcincta was originally described as Strongylus circumcinctus but was later transferred to the genus Ostertagia prior to being assigned to its present status (Drozdz, 1965 ). Teladorsagia trifircata was originally described as a species of Ostertagia prior to its transfer to Teladorsagia (DroZdz, 1965 ). While the validity of the genus Teladorsagia is accepted by many (Durrette-Desset, 1989) others retain both species within the genus Ostertagia (Lancaster et al., 1983). The total number of larvae in the llama was 56 7 IO,more than 97% of which were ostertagiine early fourth-stage larvae (Table 2 ) . Ostertagiine early fourthstage larvae were also present in the sheep, although the numbers varied. Because the majority of the adult nematodes in the population were species of TABLE 1 Species of adult nematodes recovered (expressed as a percentage of the total) from the third compartment of a naturally infected llama and abomasa of naturally infected sheep Parasite
Llama
Teladorsagia spp.’ Trichostrongylus axei Camelostrongylus mentulatus
Total number
Sheep 486
50.8
67.4
47.2 2.0
32.6 0
6510
21500
Sheep 485 0 100
Sheep 487 57.9 42.1
0
0
440
2520
‘Consisted of Teladorsagia circumcincta and Teladorsagia trifircata. TABLE 2 Larval nematodes recovered (expressed as a percentage of the total) from the third compartment a naturally infected llama and abomasa of naturally infected sheep
of
Parasite
Llama
Sheep 486
Sheep 485
Sheep 487
Teladorsagia EL: Teladorsagia DL:
91.5 2.4 0.1 56710
49.2 50.1 0.1 44060
0.4 99.6 0 9340
60.1 39.1 0.8 5720
Trichostrongylus Total number
DL4
‘EL,, early fourth-stage larvae. ‘DL4, developing fourth-stage larvae.
334
L.G. RICKARD
Teladorsagia in both the llama and sheep, the larvae were considered to belong to the same genus. The absence of ostertagiine third-stage larvae in the llama negated the possibility of recent acquisition of these large numbers of larvae. The large number of early fourth-stage larvae along with the low number of developing fourth-stage larvae and adults in the llama strongly suggest that the early fourth-stage larvae represented an inhibited population as delined by Michel ( 1974). It can be concluded that the development of species of Teladorsagia is inhibited in the llama during winter in Oregon. The significance of this finding is unknown at present. Infections of Teladorsagia spp. in sheep are associated with reduced weight gains and/or weight loss (Reid and Murray, 1973). However, in camelids, the role of hypobiosis has not been studied (Leguia, 199 1). Because the gross and histologic lesions observed in the llama were identical to those described in ostertagiasis of cattle and sheep, it is conceivable that these lesions represent a condition similar to pre-Type II ostertagiasis. However, it is not known whether these larvae would resume development and precipitate disease similar to Type II ostertagiasis. ACKNOWLEDGMENTS
The cooperation of Dr. G.L. Zimmerman help and advice of Dr. S. Snyder.
is greatly appreciated as is the
REFERENCES Armour, J., Jennings, F.W., Murray, M. and Selman, I., 1973. Bovine ostertagiasis-clinical aspects, pathogenesis, epidemiology and control. In: G.M. Urquhart and J. Armour (Editors), Helminth Diseases of Cattle, Sheep and Horses in Europe. The University Press, Glasgow, UK, pp. 1 l-27. Baumgartner, W., Zajac, A., Hull, B.L., Andrews, F. and Garry, F., 1985. Parelaphostrongylosis in llamas. J. Am. Vet. Med. Assoc., 187: 1243-l 245. Conboy, G.A., O’Brien, T.D. and Stevens, D.L., 1988. A natural infection of Fascioloides magna in a llama (Lamaglama). J. Parasitol., 74: 345-346. Drozdz, J., 1965. Studies on helminths and helminthiases in Cervidae. I. Revision of the subfamily Ostertagiinae Sarwar, 1956 and an attempt to explain the phylogenesis of its representatives. Acta Parasitol. Pol., 13: 445-48 1. Durrette-Desset, M.-C., 1989. Nomenclature proposee pour les expecies decrites dans sa lousfamille des Ostertagiinae Lopez-Neyra, 1947. Ann. Parasitol. Hum. Comp., 61: 356-373. Foreyt, W.J. and Parish, S., 1990. Experimental infection of liver flukes (Fascioloides magna) in a llama (Lama glarna). J. Zoo. Wildl. Med., 21: 468-470. Foreyt, W.J., Rickard, L.G., Dowling, S., Parish, S. and Pipas, M., 1991. Experimental infections of two llamas with the meningeal worm (Parelaphostrongylus tenuis). J. Zoo. Wild]. Med., 2 I: 468-470. Krogdahl, D.W., Thilsted, J.P. and Olsen, S.K., 1987. Ataxia and hypermetria caused by Pure(aphostrongylus tenuis infection in llamas. J. Am. Vet. Med. Assoc., 190: 191-193.
GASTRITIS AND TELADORSAGIA
IN A LLAMA
335
Lancaster, M.B., Hong, C. and Michel, J.F., 1983. Polymorphism in the Trichostrongylidae. In: A.R. Stone, H.M. Platt and L.F. Khalil (Editors), Concepts in Nematode Systematics Academic Press, London, pp. 293-302. Leguia, G., 199 1. The epidemiology and economic impact of llama parasites. Parasitol. Today, I: 54-56. Michel, J.F., 1974. Arrested development of nematodes and some related phenomena. Adv. Parasitol., 12: 279-366. Reid, J.F.S. and Murray, M., 1973. Ovine parasitic gastro-enteritis-clinical aspects and pathology. In: G.M. Urquhart and J. Armour (Editors), Helminth Diseases of Cattle, Sheep and Horses in Europe. The University Press, Glasgow, UK, pp. 32-35. Rickard, L.G. and Bishop, J.K., 199 1. Helminth parasites of llamas (Lama gluma) in the Pacific Northwest. J. Helminthol. Sot. Wash., 58: 110-l 15. Rickard, L.G. and Foreyt, W.J., 1992. Experimental fascioliasis in llamas. J. Helminthol. Sot. Wash., 59: 140-144. Rickard, L.G., Hoberg, E.P., Bishop, J.K. and Zimmerman, G.L., 1989. Epizootiology of Nematodirus buttus, N. jlicollis, and N. spathiger (Nematoda: Trichostrongyloidea) in western Oregon. Proc. Helminthol. Sot. Wash., 56: 104-l 15. Skrjabin, K.I., Shikhobalova, V.P. and Shults, R.S., 1954. Essentials of nematodology. Vol. 3. Trichostrongylids of Animals and Man. Academy of Sciences of the USSR, Moscow. (Translated by the Israeli Program for Scientific Translations, 1960, 704 pp.) Vallenas, A., Cummings, J.F. and Munnell, J.F., 1971. A gross study of the compartmentalized stomach of two new-world camelids, the llama and guanaco. J. Morphol., 134: 399-424.