Tuatara: Volume 17, Issue 2, October 1969
A Guide to the Identification of Helminth Parasites Recorded from Wild Ruminants in New Zealand
A Guide to the Identification of Helminth Parasites Recorded from Wild Ruminants in New Zealand
New Zealand has no native land mammals, except for two species of bat. However, the early explorers and settlers brought with them a variety of domestic mammals including pigs, cattle, sheep and goats, to provide food and skins. Some of these animals escaped domestication and returned to the wild state. Also, when European colonisation was established, a demand for game animals was met by a number of mammalian introductions from Europe, England, Australia and America. These introductions continued until 1909 by which time many of the wild mammals had become successfully established.
Thus New Zealand acquired a composite domestic and wild mammal fauna which rapidly expanded its distribution and achieved prime economic significance; the domestic animals as the foundation of an agriculturally- based economy, the wild mammals both as a source of revenue and as pests.
The history and spread of these introductions have been documented by Thomson (1922), Donne (1924), Wodzicki (1950), and de Vos, Manville and Van Gelder (1956).
Beginning in 1961, the author carried out a study of the parasites of red deer (Andrews, 1964) and more recently has examined the following wild ruminants for parasites; chamois (Rupicapra rupicapra L.), tahr (Hemitragus jemlahicus Hamilton-Smith, 1827), goat (Capra hircus L.), sika deer (Cervus nippon mantchuricus Swinhoe, 1864), rusa deer (Cervus timoriensis Blainville, 1822), sambar deer (Cervus unicolor Lydekker, 1913), wapiti (Cervus canadensis Erxleben, 1777), virginia or white tailed deer (Odocoileus virginianus Boddaert, 1875), and fallow deer (Dama dama L.).
Some of the preliminary results of this study have been noted in Christie and Andrews (1964, 1965a, 1965b, 1966) and other results will be published at a later date.
Several of the helminths recorded are species commonly found in domestic animals such as sheep and cattle and may be readily identified with the aid of veterinary tests such as Lapage (1956). page 68 Other species recorded are more commonly associated with the wild ruminants and many of these helminths can only be correctly identified and named with the aid of a rather diffuse literature. Hence it is hoped that this key may provide some assistance to the identification of these worms. Helminths recorded include nematodes (roundworms) cestodes (tapeworms), and trematodes (flukes).
Notes on location, collection and preparation of specimens.
The helminths recorded here are from the alimentary canal lungs, liver and body cavity of the hosts, and the site or sites of infection are given for each species in the key. A number of species may be found in more than one organ, for example, species from the abomasum may sometimes be found in the small intestine and vice versa.
Worms from the alimentary tract may be recovered by placing the contents of each organ in a sieve with a fine mesh (e.g., 0.014 in. aperture) and washing them until the water passing through the sieve runs clear. The residue can then be removed to petri dishes for examination under a low power binocular microscope. Worms from the liver and lungs can be recovered by slitting open the bile ducts and bronchii respectively.
If the worms are alive when they are recovered they can be fixed in formal-acetic-alcohol (trematodes and cestodes) or hot 70% alcohol (nematodes)—see Manter (1951). The worms may be stored in 70% alcohol. Nematodes do not usually require staining but some of the larger specimens may require clearing. This is done by placing the worms in a mixture of four parts of 70% alcohol to two parts of glycerine, concentrating the mixture in a warm (about 46°C) paraffin oven until the alcohol evaporates, and then placing the worms in several changes of glycerine until they become cleared. The specimens can then be mounted in glycerine jelly. Trematodes and cestodes may be stained in aceto-alum-carmine (see Manter, 1951).
To ease interpretation of the key, a short glossary of some of the terms used is provided. This glossary is supplemented by illustrations of some of the diagnostic features of the worms (text fig. 1).
|Accessory bursal membrane||— a small membrane, usually supported by two thin non-muscular ribs or a column-shaped structure, found dorsally in the region of the genital cone.|
|Buccal capsule||— this capsule or cavity opens between the mouth and the oesophagus. It is well developed in some groups, weakly developed in others.page 69|
|Bursal ribs||— a series of muscular ribs that support the cuticular lobes of the bursa.|
|Cephalic vesicle||— a cuticular swelling in the head region.|
|Cervical groove||— a groove (usually more or less circumferential) in the cuticle of the neck region.|
|Copulatory bursa||— the structure formed by the postero-lateral expansion of the body of male nematodes. In the case of Strongylid worms there are usually three lobes — two lateral and one dorsal — supported by bursal ribs.|
Text figure 1 — Nematode morphology
A. Head region. B. Posterior of male. C. Female reproductive structures. al — anterolateral rib; am — accessory membrane; ar — ribs of accessory membrane; av — anteroventral rib; bc — buccal capsule; cg — cervical groove; cp — cervical papillae; cv — cephalic vesicle; d — dorsal rib; ed — externodorsal rib; g — gubernaculum; gc — genital cone; la — lateral alae; m — mouth; ml — mediolateral rib; o — oesophagus; ob — oesophageal bulb; ov-1, ov-2, ov-3, ovijectors; pb — prebursal palillae; pl — posterolateral rib; pv — posteroventral rib; s — spicules; v — vulva.
|Gubernaculum||— a small chitinous structure medial and dorsal to the spicules. This accessory piece guides the spicules during copulation.|
|Lateral alae||— lateral cuticular extensions, sometimes straited running longitudinally.|
|Neck or cervical papillae||— cuticular papillae found in the neck region, normally one either side of the body.|
|Oesophageal bulb||— the swollen posterior portion of the oesophagus seen in some nematodes.|
|Spicules||— chitinous structures, often paired and of equal size.|
It will be seen from the key that, in many cases, emphasis has been placed on the characteristics of the male worms. These characteristics are generally more diagnostic than those of the female, although, where possible, reference has been made to the features of female worms.
Key to the Helminth Parasites of the Wild Ruminants in New Zealand (text figures 2-5).
|Trematodes, Cestodes, Cysts of the latter||—||49|
|2.||Males with well defined copulatory bursa with supporting ribs||—||3|
|Males without well defined bursa||—||44|
|3.||Strongly developed chitinous buccal capsule present||—||4|
|Strongly developed buccal capsule absent||—||5|
|4.||Aperture of buccal capsule directed antero-dorsally, with two ventral cutting plates and a single dorsal tooth. Equal and unbranched spicules in the male are 0.720 mm in length. Gubernaculum absent. Bursal lobe of male asymmetrical. Vulva in female lacks cuticular flap. Male approximately 11 mm in length, female 13 mm to 15 mm in length. Eggs approximately 0.095 mm × 0.058 mm. Found in small intestine.||Bunostomum trigonocephalum (text fig. 2).|
Text figure 2 — Helminths Recorded from the Wild Ruminants
A. Haemonchus contortus spicules.
B. Haemonchus contortus male bursa.
C. Oesophagostomum venulosum male bursa and spicules.
D. Cooperia curticei spicules.
E. Cooperia curticei male bursa.
F. Bunostomum trigonocephalum spicules.
G. Bunostomum trigonocephalum male bursa.
H. Nematodirus filicollis male bursa and spicules.
Abbreviations: al — anterolateral rib; av — anteroventral rib; d — dorsal rib; ed — externodorsal rib; ml — mediolateral rib; pl — posterolateral rib; pv posteroventral rib; s — spicules.
|5.||With transverse ventral cervical groove in cuticle||—||6|
|Without cervical groove||—||7|
|6.||Mouth directed forward, shallow buccal capsule, lateral alae absent. Long slender spicules in male 1.15 mm to 1.35 mm (in length. Gubernaculum absent. Long vagina in female, vulva lacking cuticular flap. Male 12 mm to 17 mm in length, female 13 mm to 25 mm in length. Eggs approximately 0.090 mm × 0.050 mm Found in caecum and large intestine.||Oesophagostomum cenulosum (text fig. 2)|
|7.||Males with asymmetrcial dorsal lobe of bursa.||—||8|
|Males with symmetrical dorsal lobe of bursa||—||9|
|8.||Spicules in male tapering, barbed at their tips, 0.370 mm to 0.570 mm in length, gubernaculum present. Vulva of female with prominent cuticular flap. Male 12 mm to 22.5 mm in length, female 25 mm to 34 mm in length. Eggs approximately 0.080 mm × 0.040 mm. Found in the abomasum.||Haemonchus contortus (text fig. 2)|
|9.||Males with double dorsal rib||—||10|
|Males with single dorsal rib||—||13|
|10.||Mediolateral and posterolateral ribs fused to form single rib||—||11|
|Mediolateral and posterolateral ribs separate for part of their length.||—||12|
|11.||Spicules approximately 0.250 mm in length, gubernaculum present. Female 17 mm to 46 mm in length, male 17 mm to 33 mm in length. Vulva lacks cuticular flap. Eggs 0.080 mm × 0.045 mm. Found in the bronchii of the lung.||Dictyocaulus vivparus (text fig. 4).|
|12.||Male with filiform spicules 0.625 mm to 0.975 mm in length, with lance-like tips. Gubernaculum absent; female with terminal spine. Vulva lacks cuticular flap. Buccal capsule with dorsal tooth. Male 8 mm to 15 mm in length,|
Text figure 3 — Helminths Recorded from the Wild Ruminants
A. Trichostrongvlus capricola male bursa and spicules.
B. T. axei male bursa and spicules.
C. T. vitrinus male bursa and spicules.
D. T. colubriformis male bursa and spicules.
Abbreviations: al — anterolateral rib; av — anteroventral rib; d — dorsal rib; ed — externodorsal rib; ml — mediolateral rib; pl — posterolateral rib; pv — posteroventral rib.
female 14 mm to 25 mm in length. Eggs approximately 0.145 mm × 0.075 mm. Found in the small intestine.
Nematodirus filicollis (text fig. 2)
|13.||Head end with strong transverse striations and cephalic vesicle||—||14|
|Head end without cephalic vesicle||—||15|
|14.||Spicules of male 0.140 mm to 0.155 mm in length, with prominent sculptured fin in mid-line aspect. Gubernaculum absent. Vulva covered by cuticular flap. Male 5 mm to 7 mm in length, female 6 mm to 8 mm in length. Eggs approximately 0.080 mm × 0.040 mm, slightly asymmetrical. Found in the small intestine||Cooperia curticei (text fig. 2).|
|15.||Neck papillae present||—||23|
|Neck papillae absent||—||16|
|16.||Spicules unequal in length||—||17|
|Spicules equal in length||—||18|
|17.||The smaller spicule is 0.085 mm to 0.150 mm in length, the longer spicule is 0.100 mm to 0.130 mm in length. Gubernaculum present. Secondary trunk of dorsal rib of male with lateral and medial offshoots, the latter with a small papilla at its base. Vulva longitudinal, cuticular flap absent. Male 3 mm to 5 mm in length, female 3.5 mm to 5.5 mm in length. Eggs approximately 0.075 mm × 0.035 mm. Found in the abomasum and small intestine.||Trichostrongylus axei (text fig. 3).|
Text figure 4 — Helminths Recorded from the Wild Ruminants
A. Capillaria bovis posterior end of male.
B. Trichuris ovis posterior end of male.
C. Skrjabinema ovis posterior end of male.
D. Skrjabinema ovis 1. En face view of optical section through male oral cavity.
2. En face view of male head.
3. En face view of female head.
E. Taenia hydatigena lateral view of scolex.
F. Dictyocaulus viviparus male bursa and spicules.
G. Fasciola hepatica.
Abbreviations: al — anterolateral rib; at — anterior testes; bm — bursal membrane; c — caeca; cp — caudal palippae; ct — cloacal tube; d — dorsal rib; ed — excretory duct; em — egg mass; edl — externodorsal rib; edt — ejaculatory duct; gp — genital pore; gub — gubernaculum; i — intestine; il — interlabia; l — labia; lm — lateral membrane; mo — mouth; ms — median sucker; os — oral sucker; p — pharynx; pt — posterior testes; ro — rostellum; s — spicule; s — sucker; sg — shell gland; sh — spicule sheath; sp — spicule; t — testis; vd — vas deferens; ve — ventral ribs; yg — yolk glands.
|18.||Secondary trunk divides unevenly||—||19|
|Secondary trunk of dorsal rib divides more or less evenly into three small papilla-like branches||—||20|
|19.||Spicules 0.120 mm to 0.150 mm in length, of tapering, twisted form each with a large triangular barb at its distal end. Gubernaculum present. Vulva longitudinal, cuticular flap absent. Male 4 mm to 6 mm in length, female 5 mm to 6.5 mm in length. Eggs approximately 0.075 mm × 0.040 mm. Found in the small intestine and the abomasum.||Trichostrongylus colubriformis (text fig. 3).|
|21.||Spicules 0.120 mm to 0.180 mm in length, tapering smoothly to sharp points. Gubernaculum present. Male 4.5 mm to 6.5 mm in length, female 5.5 mm to 7.5 mm in length. Eggs approximately 0.085 mm × 0.045 mm. Found in the small intestine and the abomasum.||Trichostrongylus vitrinus (text fig. 3).|
|22.||Spicules 0.125 mm to 0.150 mm in length, slightly twisted tapering to blunt points. Gubernaculum present. Male 4 mm to 5.5 mm in length, female 6 mm to 7 mm in length. Eggs approximately 0.075 mm × 0.035 mm. Found in the small intestine and the abomasum.||Trichostrongylus capricola (text fig. 3).|
|24.||Accessory bursal membrane supported by a columnar structure||—||25|
|Accessory bursal membrane supported by two slender rods||28|
|25.||Column of accessory bursal membrane flanked by two rods to give lyre-shaped appearance||—||26|
|Flanking rods absent||—||27|
|26.||Spicules trifurcate in their distal third, their lateral branch|
Text figure 5 — Helminths Recorded from Wild Ruminants
A. Skrjabinagia lyrata spicules.
B. S. podjapolskyi spicules.
C. Ostertagia leptospicularis spicules.
D. O. ostertagi spicules.
E. Stadelmannia circumcincta spicules
F. S. trifurcata spicules.
G. Spiculopteragia odocoilei spicules.
H. Apteragia quadrispiculata spicules.
I. Spiculopteragia spiculoptera spicules.
J. S. asymmetrica spicules.
K. Rinadia mathevossiani spicules.
|splitting and curving towards the mid-line. Mediolateral branch with transverse ridge. Dorsal rib long. Medio-lateral and posterolateral ribs close together, cuticular flap covering vulva is absent. Male 6 mm to 7.5 mm in length, female approximately 8 mm in length. Eggs approximately 0.080 mm × 0.040 mm. Found in the abomasum.||Skrjabinagia lyrata (text fig. 5).|
|27.||Spicules 0.165 mm to 0.190 mm in length, trifurcate in their distal third, lateral branch split, curved towards midline, mediolateral branch with transverse ridge. Dorsal rib long, mediolateral and posterolateral ribs close together. Cuticular flap covering vulva is absent. Male 6.5 mm to 8.5 mm in length, female approximately 8 mm in length. Eggs approximately 0.075 mm × 0.050 mm. Found in the abomasum.||Skrjabinagia podjapolskyi (text fig. 5).|
|28.||Tip of mediolateral rib of bursa closer to posterolateral than to anterolateral||—||29|
|Tip of mediolateral rib closer to anterolateral or midway between anterolateral and posterolateral.||—||32|
|29.||Gubernaculum with distal extension||—||30|
|Gubernaculum without distal extension||—||31|
|30.||Spicules trifurcate in their distal quarter, 0.200 mm to 0.230 mm in length. Gubernaculum swollen proximally with a thin distal offshoot. Vulva of female with cuticular flap. Male 5 mm to 7.5 mm in length, female 7 mm to 9 mm in length. Eggs approximately 0.070 mm × 0.035 mm. Found in the abomasum.||Ostertagia ostertagi (text fig. 5).|
|31.||Spicules trifurcate in their distal quarters 0.160 mm to 0.200 mm in length, Gubernaculum more or less oval, slightly swollen proximally. Male 5 mm to 6.5 mm in length. Female unknown. Found in the abomasum.||Ostertagia leptospicularis (text fig. 5).|
|32.||Tip of mediolateral rib midway between anterolateral and posterolateral.||—||33|
|Tip of mediolateral close to anterolateral than posterolateral||—||34|
|33.||Spicules slender approximately 0.200 mm to 0.400 mm in length, trifurcate in their distal quarter. Gubernaculum swollen proximally with a thin distal offshoot. Vulva of female with large cuticular flap. Male 5.5 mm to 10 mm in length, female 9 mm to 13.5 mm in length. Eggs approximately 0.090 mm × 0.050 mm. Found in the abomasum.||Stadelmannia circumcincta (text fig. 5).||page 79|
|34.||Spicules trifurcate in their distal third, approximately 0.160 to 0.230 mm in length. Gubernaculum roughly dagger-shaped. Vulva of female lacks cuticular flap. Male 6.5 mm to 10.5 mm in length, female 7 mm to 11 mm in length. Eggs approximately 0.080 mm × 0.050 mm. Found in the abomasum.||Stadelmannia trifurcata (text fig. 5).|
|35.||Accessory bursal membrane absent||36|
|Accessory bursal membrane present||37|
|36.||Spicules 0.160 mm to 0.190 mm in length, each with four branches in their distal quarter. Anterolateral and mediolateral ribs of bursa close together. Male 5.5 mm to 7 mm in length. Female not yet described. Found in the abomasum.||Rinadia mathevossiani (text fig. 5).|
|38.||Mediolateral rib approximately midway between antero-lateral and posterolateral||39|
|Mediolateral rib closer to anterolateral than posterolateral||40|
|39.||Spicules trifurcate in their distal third, 0.165 mm to 0.180 mm in length. Vulva of female with small cuticular flap. Male 6 mm to 7.5 mm in length, female 7 mm to 8.5 mm in length. Eggs approximately 0.080 mm × 0.040 mm. Found in the abomasum.||Spiculopteroides odocoilei (text fig. 5).|
|40.||Spicules 0.185 mm to 0.225 mm in length, each with four branches distally. Male 6 mm to 8.5 mm in length. Female not yet described. Found in the abomasum.||Apteragia quadrispiculata (text fig. 5).|
|41.||Vulva of female with small cuticular flap.||42|
|Vulva of female with large cuticular flap.||43|
|42.||Spicules 0.140 mm to 0.200 mm in length. Male 4.5 mm to 7 mm in length, female 6 mm to 7.5 mm in length. Eggs approximately 0.085 mm × 0.040 mm. Found in the abomasum.||Spiculopteragia spiculoptera (text fig. 5).|
|43.||Spicules 0.180 mm to 0.250 mm in length. Male 4.5 mm to 6 mm in length, female 6 mm to 9 mm in length. Eggs approximately 0.095 mm × 0.050 mm. Found in the abomasum.||Spiculopteragia asymmetrica (text fig. 5).|
|44.||Worms with oesophageal bulb||45|
|Worms with a narrow oesophageal portion and thicker posterior portion.||46page 80|
|45.||Male with single spicule 0.65 mm to 0.75 mm in length. Gubernaculum present. Cuticle of male expanded in the tail region and supported by two pairs of blunt projections. Mouth region of both sexes complex. Lateral alae present. Vulva opens transwersely, lacks cuticular flap. Male 2.5 mm to 3 mm in length, female 6 mm to 6.5 mm in length. Eggs D-shaped, approximately 0.050 mm × 0.025 mm. Found in the large intestine and caecum.||Skrjabinema ovis (text fig. 4).|
|46.||Posterior portion of worm much thicker than oesophageal portion; tail of male coiled spirally||47|
|Posterior portion of worm slightly thicker than oesophageal portion; tail of male not coiled||48|
|47.||Single spicule of male from 4.0 mm to 6.0 mm in length with a small proximal expansion. Gubernaculum absent. vulva of female at the junction of intestine and oesophagus, lacking a cuticular flap. Male 46 mm to 56 mm in length, female 47 mm to 75 mm in length. Eggs 0.080 mm × 0.030 mm, barrel-shaped with polar plugs. Found in the caecum.||Trichuris ovis (text fig. 4).|
|48.||Single unbranched spicule approximately 2.0 mm in length extending well back into the body, tail curved bearing a small membrane on the inside curve. Vulva of female at the junction of intestine and oesophagus, lacking cuticular flap. Male approximately 16 mm in length, female approximately 23 mm in length. Eggs approximately 0.050 mm × 0.025 mm, barrel-shaped with polar plugs. Found in the lower portion of the small intestine.||Capillaria bovis (text fig. 4).|
|Tapeworms, as cysts (Cestoda)||51|
|50.||Flat, leaf-shaped fluke, cone-shaped anterior, ventral sucker, cuticle armed with small spines. Size from 13 mm × 7 mm to 30 mm × 13 mm. Eggs approximately 0.140 mm × 0.080 mm Found in the liver.||Fasciola hepatica (text fig. 4).|
|51.||Cysts bladder-like, more or less translucent, fluid filled, up to 3 cm in diameter. Bladder-worm scolex bears four suckers and from 22 to 44 hooks on the rostellum, the hooks being in two circlets. Found on mesenteries and on the liver.||Taenia hydatigena (Cysticercus tenuicollis) (text fig. 4).|
I would like to thank Dr. G. Gibbs for his comments on this paper and Mrs. P. Johnston for typing the manuscript.
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——, 1965a, Introduced Ungulates in New Zealand (b) Virginia deer. Tuatara 13(1): 1-8.
——, 1965b. Introduced Ungulates in New Zealand (c) Chamois. Tuatara 13(2): 105-111.
——, 1966. Introduced Ungulates in New Zealand (d) Fallow deer. Tuatara 14(2): 82-88.
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