Ambystoma Tschudi 1838

Duszynski, Donald W., Bolek, Matthew G. & Upton, Steve J., 2007, Coccidia (Apicomplexa: Eimeriidae) of amphibians of the world, Zootaxa 1667 (1667), pp. 1-77 : 47-52

Host genus Ambystoma Tschudi 1838

(31 species)

Eimeria ambystomae Saxe 1955 ( Figs. 32, 61)

Type host: Larval Ambystoma tigrinum (Green 1825) , Tiger salamander.

Other hosts: Ambystoma mavortium Baird 1850 , Barred tiger salamander; Ambystoma texanum (Matthes 1855) , Smallmouth salamander.

Type locality: NORTH AMERICA: USA, Iowa, Dickinson County .

Geographic distribution: NORTH AMERICA: USA, Colorado, Indiana, Iowa, Nebraska, New Mexico, Texas .

Description of sporulated oocyst: Oocyst shape: ellipsoidal; wall thickness: 1 layer of uniform thickness, ~1; wall characteristics: smooth, colorless to pale yellow; L x W: 31.2 x 17.7 (24.5–36 x 15–20); M and PG: absent; OR: present; OR characteristics: spheroidal to subspheroidal body consisting of a hyaline sphere surrounded by small refractile granules, 12.7 x 11.4. Distinctive features of oocyst: large size, ellipsoidal shape, and large OR composed of a hyaline sphere with small refractile granules.

Description of sporocyst and sporozoites: Sporocyst shape: lanceolate; L x W: 21.9 x 5.1 (17–24.5 x 4– 6); SB: present; SSB and PSB: absent; SR: present; SR characteristics: scattered refractile granules, sometimes aggregated into 2 groups; SZ: elongate, almost as long and as wide as sporocyst and arranged in sporocyst in a variety of twisted and parallel positions; SZ with 2 large RB, one near posterior end and the other above it near the middle of SZ. Distinctive features of sporocyst: lanceolate shape with a SB at slightly pointed end.

Prevalence: At least 13 of 56 (23%) A. tigrinum from Iowa between 1951–1954 ( Saxe 1955); 1 of 1 (100%) A. tigrinum from Indiana ( Bolek 2000); 17 of 17 (100%) A. mavortium from Colorado (5) and New Mexico (12) ( Duszynski et al. 1972); A. mavortium from Nebraska not given ( Bolek et al. 2003); and 11 of 51 (22%) A. texanum from Texas ( McAllister & Upton 1987a; Upton et al. 1993). Saxe (1955) indicated that oocysts were noted in 1 of 8 Desmognathus quadramaculatus and in 1 of 2 D. monticola obtained from commercial sources, but never identified these oocysts to species.

Sporulation: Exogenous, 25–48 h; in one population, 80% sporulated within 48 h while in a second population 96% sporulated in 25 h ( Saxe 1955).

Prepatent and patent periods: Unknown.

Site of infection: In the cytoplasm of epithelial cells of the small intestine from 2–10 cm above the rectum ( Saxe 1955).

Endogenous stages: Saxe (1955) said he saw merozoites, macro- and microgametocytes in the cytoplasm of epithelial cells in stained sections of the lower small intestine from 3 larval A. tigrinum .

Pathology: Unknown.

Materials deposited: Photosyntypes of sporulated oocysts are deposited in the USNPC (No. 87478).

Remarks: Oocysts from A. mavortia from Colorado and New Mexico ( Duszynski et al. 1972) and from A. tigrinum from Indiana ( Bolek 2000) closely resembled those described from Iowa by Saxe (1955): oocysts from Colorado and New Mexico, 29.8 x 17.3 (24–38 x 15–25); oocysts from Indiana, 27 x 16.5 (27–28 x 15– 17) vs. oocysts from Iowa, 31.2 x 17.7 (24.5–36 x 15–20); sporocysts from Colorado and New Mexico, 22.6 x 5.4 (16–27 x 5–7); sporocysts from Indiana, 15.4 x 5.1 (15–16 x 5–7) vs. sporocysts from Iowa, 21.9 x 5.7 (17–24.5 x 4–6). There were only 2 discrepancies between the 3 accounts: a) the size and composition of the OR: numerous scattered granules vs. a large hyaline structure surrounded by scattered granules; and b) Saxe (1955) did not mention the presence of a SB, while Duszynski et al. (1972) documented photographically that a SB was present. Saxe (1955) also said that the oocysts he saw may increase in size with time.

Eimeria distorta Saxe 1955 ( Fig. 33)

Type host: Larval Ambystoma tigrinum (Green 1825) , Tiger salamander.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA, Iowa, Dickinson County .

Geographic distribution: NORTH AMERICA: USA, Iowa.

Description of sporulated oocyst: Oocyst shape: elongate-ellipsoidal initially, but quickly becomes distorted in 3% K 2 Cr 2 O 7 solution when placed under a coverglass; wall thickness: 1 very thin layer (line drawing); wall characteristics: smooth; L x W: 29.2 x 15.5 (27–31 x 14–16); L/W ratio 1.9; M and PG: absent; OR: present; OR characteristics: scattered refractile granules. Distinctive features of oocyst: very thin wall that distorts easily when prepared for viewing with a light microscope.

Description of sporocyst and sporozoites: Sporocyst shape: elongate ellipsoidal; L x W: 12.4 x 7.3; L/W ratio 1.7; SR: present; SR characteristics: compact mass of small granules; SB, SSB, PSB: all absent; SZ: appear sausage-shaped (line drawing), slightly longer than sporocyst and without visible RB or N. Distinctive features of sporocyst: ellipsoidal shape and absence of SB; also, sporocysts appear tightly packed within confines of oocyst wall (line drawing).

Prevalence: Unknown.

Sporulation: Exogenous, 1/3 of the oocysts sporulated after 76 h, 2/3 sporulated after 5 days; the temperature at which they were maintained was not given.

Prepatent and patent periods: Unknown.

Site of infection: Unknown. Oocysts recovered from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Materials deposited: None.

Remarks: The type host was a larval A. tigrinum . Unsporulated oocysts were about the same size as sporulated ones, 27.5 x 15.5. This species has not been seen since its original description.

Eimeria kingi Saxe 1955 ( Fig. 34)

Type host: Ambystoma tigrinum (Green 1825) , Tiger salamander.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA, Iowa, Dickinson County, near the Lakeside Laboratory .

Geographic distribution: NORTH AMERICA: USA, Iowa.

Description of sporulated oocyst: Oocyst shape: subspheroidal; wall thickness: 1 thin layer (line drawing); wall characteristics: smooth; L x W: 20.4 x 18.3 (16–23 x 14–21); L/W ratio 1.1; M and PG: absent; OR: present; OR characteristics: starts as a compact mass of granules, becomes a single refractile sphere 5.2 wide ~6 days after leaving the host. Distinctive features of oocyst: OR changes from compact mass of granules to a refractile sphere.

Description of sporocyst and sporozoites: Sporocyst shape: ovoidal; L x W: 8.8 x 6.5 (7–10 x 5–8); L/ W ratio 1.3; SB: present, small knob at pointed end of sporocyst; SSB and PSB: both absent; SR: present; SR characteristics: scattered refractile granules; no mention is made of SZ, RB or N. Distinctive features of sporocyst: none.

Prevalence: Unknown.

Sporulation: Exogenous, 4–6 days.

Prepatent and patent periods: Unknown.

Site of infection: Unknown. Oocysts recovered from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Materials deposited: None.

Remarks: This species was found in an adult A. tigrinum , the same host animals from which E. waltoni was described. It has not been seen since its original description.

Eimeria microcapi Duszynski et al. 1972 ( Fig. 35, 62)

Type host: Ambystoma mavortium Baird 1850 , Barred tiger salamander.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA: Colorado, Weld County .

Geographic distribution: NORTH AMERICA: USA: Colorado.

Description of sporulated oocyst: Oocyst shape: ellipsoidal; wall thickness: 1 thin layer of uniform thickness; wall characteristics: smooth; L x W: 38.1–25.3 (35–41 x 23–26); L/W ratio: 1.5 (1.3–1.7); M: present, 3.0 (2–4) wide, covered by a distinct MC; OR: present; OR characteristics: a large mass with no distinct shape, consisting of many small granules; PG: absent. Distinctive features of oocyst: large size, thin wall, presence of M and MC, and large, amorphous OR.

Description of sporocyst and sporozoites: Sporocyst shape: navicular (slightly pointed at both ends); L x W: 18.1 x 7.4 (16–19 x 6–8); L/W ratio: 2.5 (2.1–2.8); SB: if present (?), very small and difficult to distinguish at 1 end of sporocyst; SSB, PSB: both absent; SR: present; SR characteristics: composed of 5–15 scattered granules; SZ: tightly packed in sporocyst, without discernable N or RB visible. Distinctive features of sporocyst: navicular shape.

Prevalence: 1 of 5 (20%) salamanders from Colorado; 0 of 12 salamanders from New Mexico, U.S.A.

Sporulation: Unknown.

Prepatent and patent periods: Unknown.

Site of infection: Unknown, oocysts collected from feces.

Endogenous stages: Unknown.

Pathology: Unknown. Materials deposited: Photosyntypes of sporulated oocysts are deposited in the USNPC (No. 87486). Remarks: Among the oocysts described from salamanders, only those of E. canaliculata Lavier, 1936

( Fig. 51) and E. propria ( Schneider 1881) ( Fig. 52) approach the size of E. microcapi , however, neither has a

M or MC and the sporocysts of both are much longer than those of E. microcapi .

Eimeria opacum Upton, McAllister and Trauth 1993 ( Figs. 36, 63)

Type host: Ambystoma opacum (Gravenhorst 1807) , Marbled salamander.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA: Arkansas, Grant County, 6.4 km SW Sheridan.

Geographic distribution: NORTH AMERICA: USA: Arkansas.

Description of sporulated oocyst: Oocyst shape: spheroidal to slightly subspheroidal; wall thickness: ~1.0; wall characteristics: 2 layers, outer, smooth, ~1/2 of total thickness; L x W: 29.4 x 23.8 (27–32 x 25–31); L/W ratio: 1.0 (1.0–1.1); M, OR, PG: all absent. Distinctive features of oocyst: large size with 2 walls of equal thickness.

Description of sporocyst and sporozoites: Sporocyst shape: ellipsoidal when viewed from one side, but kidney-bean shaped when viewed from another side; L x W: 17.4 x 9.1 (16–21 x 8–11); L/W ratio: 1.7 (1.6– 2.3); SB, SSB, PSB: all absent; SR: present; SR characteristics: composed of 1–2 small clusters of coarse granules; SZ: 20–24 x 4–5, with large posterior RB 7.7 x 4.2 (5.5–9.5 x 4–5) and centrally located N. Distinctive features of sporocyst: each sporocyst is loosely enclosed in a secondary sporocyst wall, with ends of the secondary wall connected by frail, membrane-like material; 1–3 homogeneous globules present between primary and secondary sporocyst walls with other homogeneous globular material flattened against inner portion of secondary wall.

Prevalence: 1 of 5 (20%).

Sporulation: Exogenous. All oocysts were passed unsporulated and became fully sporulated within 1 wk at ~23° C.

Prepatent and patent periods: Unknown.

Site of infection: Unknown. Oocysts recovered from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Materials deposited: Photosyntypes of sporulated oocysts are deposited in the USNPC (No. 83259). The symbiotype host (sensu Frey et al. 1992) was an adult male, 50 mm snout-vent length, collected 20 March 1992, and is deposited in the ASUMZ (Cat. No. 18276).

Remarks: Oocysts of E. opacum are unique among the coccidia because of the double-walled structure of the sporocysts; even the kidney-bean shape itself is rare. Rankin (1937) found unsporulated oocysts in A. opacum that were 17 x 12, measurements identical to those reported for the macrogametes/unsporulated oocysts of E. ranarum ( Laveran & Mesnil 1902a) , a parasite of ranids in Europe. Likewise, Walton (1942) mentioned an eimerian from an unspecified Ambystoma species , which Saxe (1955) later reported through personal communication with Walton as also being from A. opacum , but did not identify it.

Eimeria urodela Duszynski et al. 1972 ( Figs. 37, 64)

Type host: Ambystoma mavortium Barid 1850 , Barred tiger salamander.

Other hosts: Ambystoma tigrinum (Green 1825) , Tiger salamander.

Type locality: NORTH AMERICA: USA: Colorado, Weld County .

Geographic distribution: NORTH AMERICA: USA: Colorado; Indiana .

Description of sporulated oocyst: Oocyst shape: spheroidal; wall thickness: 1.0; wall characteristics: 1 smooth layer, colorless, of uniform thickness; L x W: 22.3–22.1 (14–26 x 14–26); L/W ratio: 1.0 (1.0–1.1); M and PG: absent; OR: present; OR characteristics: consisting of large granules usually in a compact mass, ~5– 7, but sometimes scattered throughout oocyst. Distinctive features of oocyst: spheroidal shape with large OR.

Description of sporocyst and sporozoites: Sporocyst shape: lanceolate; L x W: 16.3 x 5.8 (12–19 x 4– 7); L/W ratio: 2.8 (2.0–3.6); SB: present, small, at pointed end of sporocyst; SSB, PSB: absent; SR: present; SR characteristics: usually compact spheroidal mass in center of sporocyst, but sometimes granules more diffuse in anterior of sporocyst; SZ: longer than sporocyst, crescent-shaped when within sporocyst, and arranged either side-by-side or intertwined with each other; neither N nor RB are visible. Distinctive features of sporocyst: the second largest L/W ratio in any amphibian coccidium, next to E. longaspora (see below).

Prevalence: 5 of 5 (100%) A. mavortium from Colorado during each of 3 collection periods; 0 of 12 A. mavortium from New Mexico (Duszynski, et al. 1972), and 1 of 1 A. tigrinum (100%) salamanders from Indiana ( Bolek 2000).

Sporulation: Unknown.

Prepatent and patent periods: Unknown.

Site of infection: Unknown, oocysts collected from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Materials deposited: Photosyntypes of sporulated oocysts are deposited in the USNPC (No. 87489).

Remarks: Of the oocysts described from salamanders, only those of E. spherica (Schneider) ( Fig. 44) and E. waltoni Saxe ( Fig. 38) resemble E. urodela . Oocysts of E. spherica , redescribed by Lavier (1936), are much larger than those of E. urodela , with a mode of 35, and its sporocysts are much shorter and different in structure than those of E. urodela . Oocysts of E. waltoni , as described by Saxe (1955) are always subspheroidal, whereas those of E. urodela are distinctly spheroidal. Other differences between the 2 species include the size and shape of the OR and of the sporocysts.

Eimeria waltoni Saxe 1955 ( Fig. 38)

Type host: Ambystoma tigrinum (Green 1825) , Tiger salamander.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA, Iowa, Dickinson County, near the Lakeside Laboratory .

Geographic distribution: NORTH AMERICA: USA, Iowa.

Description of sporulated oocyst: Oocyst shape: subspheroidal; wall thickness: not stated; wall characteristics: 1 smooth wall of uniform thickness (line drawing); L x W: 22.2 x 19.2 (20–24 x 17–21); L/W ratio: 1.2; M: absent; OR: probably absent; PG: relatively small disc-like refractile granule described as the OR by Saxe (1955). Distinctive features of oocyst: closely resembles E. kingi in the unsporulated state, otherwise, none.

Description of sporocyst and sporozoites: Sporocyst shape: ovoidal; L x W: 12.2 x 7.2 (11–14 x 6–8); L/W ratio 1.7; SB: present as small knob a pointed end of sporocyst; SSB and PSB: both absent; SR: present; SR characteristics: loose aggregation of refractile granules; SZ, RB and N were not mentioned by Saxe (1955). Distinctive features of sporocyst: none.

Prevalence: Unknown.

Sporulation: Exogenous, ~66 h.

Prepatent and patent periods: Unknown.

Site of infection: Unknown, oocysts recovered from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Material deposited: None.

Remarks: The type host is the same individual as the type host of E. kingi . This species has not been found since its original description.

Isospora jeffersonianum Doran 1953 ( Fig. 39)

Type host: Ambystoma jeffersonianum (Green 1827) , Jefferson salamander, but see Remarks, below.

Other hosts: None reported to date.

Type locality: NORTH AMERICA: USA, Minnesota, near Bemidji , Beltrami County .

Geographic distribution: NORTH AMERICA: USA, Minnesota.

Description of sporulated oocyst: Oocyst shape: spheroidal; wall thickness: ~1.5; wall characteristics: 2 layers, outer, smooth, ~2/3 of total thickness (line drawing); L x W: 18.5–22.5; L/W ratio: 1.0; M: present, about 1.5–2 wide appearing as a small knob on oocyst wall; OR and PG: absent. Distinctive features of oocyst: presence of M.

Description of sporocyst and sporozoites: Sporocyst shape: elongate ovoidal, slightly pointed at one end; L x W: 15.5–16 x 7–8; L/W ratio: not given; SB: a small knob at pointed end of sporocyst; SSB and PSB: both absent; SR: present; SR characteristics: spheroidal, highly granular body, 2–2.7, that appears membranebound (line drawing); SZ: crescent-shaped, 6–7 long, with N equidistant between ends; RB not mentioned or shown in line drawing ( Doran 1953). Distinctive features of sporocyst: membrane-bound SR.

Prevalence: 2 of 7 (29%).

Sporulation: Exogenous, 64–72 h.

Prepatent and patent periods: Unknown.

Site of infection: Unknown, oocysts recovered from feces.

Endogenous stages: Unknown.

Pathology: Unknown.

Material deposited: None.

Remarks: Doran (1953) lists the blue-spotted salamander A. jeffersonianum as the host. However, A. jeffersonianum , the Jefferson salamander, is not known to occur in Minnesota ( Conant & Collins 1991; McAllister et al. 1993). Because the taxonomy of A. jeffersonianum and the blue-spotted salamander A. laterale was in a state of confusion ( Bishop 1943) until Uzzel’s work (1964), we think that the actual host Doran (1953) was dealing with was A. laterale or a hybrid species ( Lowcock et al. 1987; Upton et al. 1993) which occurs commonly in Minnesota ( Oldfield & Moriarty 1994).