The cestode genus Gastrotaenia Wolffhügel, 1938 (Platyhelminthes: Cyclophyllidea) in Australian waterfowl (Aves: Anatidae)

ABSTRACT

Examination of museum collections revealed the presence of two species of Gastrotaenia Wolffhügel, 1938 (Cestoda: Hymenolepididae) in Australian anatid birds. Gastrotaenia dogieli (Ginetsinskaya, 1944) was found in the gizzard of the following species of Australian ducks from New South Wales: Anas castanea (Eyton), Anas rhynchotis Latham, Anas gracilis Buller, Aythya australis (Eyton), Chenonetta jubata (Latham) and Malacorhynchus membranaceus (Latham). Gastrotaenia cf. paracygni Czapliński & Ryžikov, 1966 was found in the proventriculus of black swans (Cygnus atratus (Latham)) from New South Wales and Victoria. The two species are reported for the first time from Australia. Specimens of Gastrotaenia without scoleces, and therefore not identifiable to species, were present in Anas superciliosa Gmelin and Biziura lobata (Shaw).

KEYWORDS:

• Cestodes
• Anatidae
• Australia
• Gastrotaenia dogieli
• Gastrotaenia paracygni
• new records

Introduction

The cestode (tapeworm) fauna of Australian birds is particularly poorly studied compared with that of other continents (Mariaux & Georgiev, 2018). In the case of Australian anatid birds (ducks, geese, and swans), although a significant series of species of cestodes has been reported, many have been identified to generic level only, or have been listed simply as “unidentified” (Mawson et al., 1986). Among the former group, Gastrotaenia Wolffhügel, 1938 is an unusual genus found in the proventriculus and gizzards of anatid birds. It occurs in both ducks and swans in Australia, but no species has been fully identified (Mawson et al., 1986).

As they lack external segmentation, species of Gastrotaenia, along with those of Nematoparataenia Maplestone & Southwell, 1922, from swans, have been placed in a separate cyclophyllidean order, Aporidea Fuhrmann, 1934 (Schmidt, 1986; Yamaguti, 1959). However, based partially on life cycle studies in which crustaceans were shown to be the intermediate hosts (Egizbaeva & Erbolatov, 1975; Wisniewski, 1971), both genera were subsequently transferred to the Hymenolepididae Ariola, 1899, a family commonly found in anatid birds (Czapliński & Vaucher, 1994) and the order Aporidea has been supressed.

Currently, four species of Gastrotaenia are recognised. Gastrotaenia dogieli (Ginetsinskaya, 1944) is found in a wide array of species of ducks in the Northern Hemisphere (Czapliński & Ryžikov, 1966; Króaczyk & Kavestka, 2019). Egizbaeva and Nasyrova (1979) described G. kazachstanica Egizbaeva & Nasyrova, 1979 based on metacestodes from the copepod crustacean Arctodiaptomus salinus (Daday) which they transmitted experimentally to ducks. Two species are known from swans. Gastrotaenia cygni Wolffhügel, 1938 is found in swans in North and South America (Willers & Olsen, 1969; Wolffhügel, 1938) and G. paracygni Czapliński & Ryžikov, 1966 in swans in Eurasia (Czapliński & Ryžikov, 1966).

In this report, specimens of Gastrotaenia held in museum collections were examined and identified as G. dogieli in ducks and G. cf. paracygni in swans, providing the first records of these species in Australia.

Materials and methods

Specimens of Gastrotaenia from black swans (Cygnus atratus) held in the helminthological collections (AHC) of the South Australian Museum (SAM) were stained in Celestine blue, destained in acid alcohol, dehydrated in an ethanol series, cleared in methyl salicylate, and mounted in Canada balsam. Additional scoleces were mounted in Hoyer’s medium (Pritchard & Kruse, 1982) to illustrate the features of the rostellar hooks. Mounted specimens of Gastrotaenia from swans and ducks were borrowed from the Australian National Wildlife Collection, Canberra (ANWC). The slides had been prepared by Prof. Bogdan Czaplinski in 1984 and had been stained in carmine and mounted in balsam as entire strobilae or strobilae with squash preparations of their scoleces for examination of the rostellar hooks. Drawings were made with a drawing tube attached to an Olympus BH2 microscope. Measurements were made with an ocular micrometer and are presented in millimetres as the range followed by the mean and the number of measurements made in parentheses. To provide additional details on the features of the rostellar hooks, measurements are provided of the blade, guard and handle, indicated in Figure 1a, as well as the total lengths of the hooks. The taxonomic allocation of the genus Gastrotaenia to the Hymenolepididae follows Czapliński and Vaucher (1994). The nomenclature of Australian anatid birds follows Christidis and Boles (2008).

Figure 1. Gastrotaenia dogieli and G. cf. paracygni. (a) Rostellar hook showing measurements reported in text; (b) G. dogieli, entire cestode, from Aythya australis, pre-mature; (c) G. dogieli, scolex with rostellum everted, from Aythya australis; (d) G. dogieli, scolex with rostellum retracted, from Anas gracilis; (e) G. dogieli, hook outline showing short hook blade; (f) G. cf. paracygni, scolex with rostellum everted; (g) G. cf. paracygni, scolex with rostellum retracted;(h) G. cf. paracygni, hook outline showing hook blade longer than guard; (i) G. cf. paracygni, strobila, showing lateral groove and cirrus sacs extending from midline to peripheral testes; (j) G. cf. paracygni, strobila, dorsoventral view, showing cirrus sacs and testes; (k) G. cf. paracygni, strobila, lateral view, showing linear arrangement of testes. Scale-bars: a, e, h, 0.01 mm; b, 0.5 mm; c, d, f, g, i – k, 0.1 mm. Abbreviations: b, hook blade; c, cirrus sac; g, hook guard; h, hook handle; t, testis.

Results

Order Cyclophyllidea van Beneden in Braun, 1900

Family Hymenolepidiae Ariola, 1899

Genus: Gastrotaenia Wolffhügel, 1938

Gastrotaenia dogieli (Ginetsinskaya, 1944)

Synonym: Apora dogieli Ginetsinskaya, 1944

Material examined

From Anas castanea (Eyton) (chestnut teal), 1 strobila with scolex, Lake Cowal, West Wyalong, NSW (33° 40’S 147° 27’E) (ANWC C895); from Anas rhynchotis Latham (Australian shoveler), 2 strobilae with scoleces, Lake Cowal, West Wyalong, NSW (ANWC C490); from Anas gracilis Buller (as A. gibberifrons) (grey teal), 4 scoleces, 2 strobilae without scoleces, Barren Box Swamp, Griffith, NSW (34° 09’S 145° 50’E) (ANWC 432); from Aythya australis (Eyton) (hardhead), 4 strobilae with scoleces, strobilar fragments, Lake Cowal, West Wyalong, NSW (ANWC C478); from Chenonetta jubata (Latham) (Australian wood duck), 1 strobila with scolex, Berembed Weir, Wagga Wagga, NSW (34° 51’S 146° 50’E) (ANWC C447); from Malacorhynchus membranaceus (Latham) (pink-eared duck), 4 scoleces, strobilar fragments, Lake Cowal, West Wyalong, NSW (ANWC C485).

Site in host

Gizzard.

Description (Figure 1b-e)

Small, delicate cestodes, 4.1–8.1 (5.8, n = 5) long, maximum width 0.13–0.21 (0.17, n = 5) wide. Scolex 0.11–0.15 (0.13, n = 7) long, 0.11–0.15 (0.12, n = 7) wide. Four weakly developed oval suckers present, not visible in most specimens, 0.09–0.11 (0.10, n = 5) long; minute hooks present on surface of suckers. Eversible rostellum present; rostellar sac (with rostellum withdrawn) 0.06–0.09 (0.08, n = 7) long, 0.04–0.06 (0.05, n = 17) wide; 2 prominent, darkly staining glands within base of rostellar sac; in few specimens, additional pair of darkly staining glands anterior to posterior pair. Rostellar hooks 10 in number, length 0.030–0.035 (0.033, n = 10) measured on whole mounts; in squash preparations, blade 0.006–0.008 (0.007, n = 5), guard 0.005–0.007 (0.006, n = 5), handle 0.024–0.028 (0.026, n = 5). Length of cestode between scolex and first appearance of genitalia (“neck” region) highly variable, 0.75–2.10 (1.30, n = 5). Prominent groove runs along entire lateral margin of strobila; external segmentation lacking. No fully developed uteri or eggs present in any specimens.

Remarks

Gastrotaenia dogieli has been studied extensively in Russia, former Soviet Republics and Poland. Its host and geographical distribution in this region have been summarised by Czapliński and Ryžikov (1966). The host range included: Anas acuta Linnaeus (northern pintail) (as Dafila acuta); Anas platyrhynchos Linnaeus (mallard); Aythya ferina (Linnaeus) (common pochard) (as Nyroca ferina); Aythya fuligula (Linnaeus) (tufted duck) (as Nyroca fuligula); Aythya rufa (Guldenstadt) (ferrugineous pochard) (as Nyroca rufa); Bucephala clangula (Linnaeus) (common golden-eye) (as Glaucionetta clangula); Mergus merganser (Linnaeus) (common merganser); Nettion crecca (Linnaeus) (common teal); Spatula clypeata (Linnaeus) (northern shoveler); Spatula querquedula (Linnaeus) (garganey) (as Querquedula querquedula). Króaczyk and Kavestka (2019) added Aythya marila (Linnaeus) (greater scaup) from Poland.

Ultrastructural studies of the scolex and tegument have been reported by Davydov et al. (1990) and Pospekhova (2009), while histopathological changes associated with experimental infections have been described by Egizbaeva and Erbolatov (1975).

Gastrotaenia kazachstanica appears to be indistinguishable from G. dogieli based on the relevant descriptions but is not treated as a synonym herein as the relevant specimens have not been examined. Egizbaeva and Nasyrova (1979) gave the lengths of the rostellar hooks for this species as 0.035 mm in the text, within the range for G. dogieli, although the scale bar associated with the drawing of the hook (their Figure 1) appears to be that of the hook length rather than the actual scale which should probably have been 0.01 mm.

Ginetsinskaya (1944) provided few measurements in her description of G. dogieli, noting principally that the strobila was 0.33 mm in width, the scolex was 0.11–0.12 mm in diameter and that the 10 rostellar hooks were 0.037 mm long.

Egizbaeva and Nasyrova (1979, p. 51), in an un-numbered table, provided a few additional measurements for G. dogieli from an apparently unpublished study by Egizbaeva in 1971, but with essentially the same measurements for the rostellar hooks. Consequently, a comparative table of the original and current measurements has not been presented.

All of the specimens from different species of Australian species of ducks were identical morphologically (Table S1) and conformed to the descriptions of G. dogieli from the Northern Hemisphere. Gastrotaenia dogieli differs from G. cygni and G. paracygni primarily in the sizes of the rostellar hooks (Table 1).

Table 1. Comparative measurements of Gastrotaenia cygni and G. paracygni from swans (measurements in millimetres with means in parentheses).

	Gastrotaenia cygni	Gastrotaenia paracygni	Gastrotaenia cf. paracygni
	(from Willers & Olsen, 1969)	(from Czapliński & Ryžikov, 1966)	Current study
Length	3.0–22.6	8.8–19.1 (14.4)	4.8–11.2 (9.7)
Maximum width	0.17–0.34	0.14–0.26 (0.18)	0.10–0.23 (0.19)
Neck, length	–	1.73–3.90 (2.65)	1.20–4.60 (2.71)
Neck, diameter	0.034–0.095	0.09–0.12 (0.11)	0.04–0.11 (0.08)
Scolex, length	0.12–0.18	0.29	0.15–0.23 (0.20)
Scolex, width	0.12–0.16	0.16–0.26 (0.21)	0.10–0.19 (0.14)
Sucker, length	–	0.19	0.16
Rostellar sac, length	–	0.24	0.11–0.17 (0.13)
Rostellar sac, width	–	0.09	0.04–0.09 (0.06)
Rostellar hook, length	0.029–0.037	0.058–0.060	0.045–0.058 (0.054)
Egg	0.024–0.025	–	–
Onchosphere	0.015–0.017	–	–
Embryonic hook, length	0.004–0.007	–	–

Gastrotaenia cf. paracygni Czapliński & Ryžikov, 1966

Material examined

From Cygnus atratus (Latham) (black swan): 19 specimens with scoleces, 21 specimens lacking scoleces, Albert Park, Melbourne, Vic. (37° 49’S 154° 48’E) (SAM AHC 36 988–91); 14 specimens with scoleces, 7 specimens without scoleces, Lake Bookar, Vic. (38° 08’S 143° 07’E) (SAM AHC 36996, 36997; from SAM AHC 19 382); 4 specimens with scoleces, 1 specimen without scolex, Adelaide Zoological Gardens, SA (34° 56’S 138° 36’E) (SAM AHC 36995; from SAM AHC 6646); 12 specimens with scoleces, Barren Box Swamp, Griffith, NSW (34° 09’S 145° 50’E) (ANWC C433).

Site in host

Proventriculus.

Description (Figure 1f-k)

Small, delicate cestodes, 4.8–11.1 (9.7, n = 10) long, maximum width 0.10–0.23 (0.19, n = 10) wide. Scolex 0.15–0.23 (0.20, n = 10) long, 0.10–0.19 (0.14, n = 10) wide. Four weakly developed oval suckers present, not visible in most specimens, c. 0.16 long; minute hooks present on surface of suckers. Eversible rostellum present; rostellar sac (with rostellum withdrawn) 0.11–0.17 (0.13, n = 10) long, 0.04–0.09 (0.06, n = 10) wide; sac with >20 transverse muscle bands; 2 prominent darkly staining glands within base of rostellar sac; in a few specimens, additional pair of darkly staining glands anterior to posterior pair. Rostellar hooks 10 in number, length 0.045–0.055 (0.050, n = 10) measured on whole mounts; in squash preparations, total hook length 0.048–0.053 (0.052; n = 10), blade 0.015–0.018 (0.016, n = 10), guard 0.010–0.013 (0.011, n = 10), handle 0.033–0.038 (0.036, n = 10). Length of cestode between scolex and first appearance of genitalia (“neck” region) highly variable, 1.2–4.6 (2.7, n = 10), average width 0.04–0.11 (0.08, n = 10).

Prominent groove runs along entire lateral margin of strobila; external segmentation lacking. In early development of sexual organs, testes arranged in irregular transverse bands, 0.025–0.030 (0.028, n = 10) in diameter; subsequently, cirrus sacs become evident, c. 0.085 long and c. 0.015 wide, radiating from lateral groove. No fully developed uteri present in any specimens.

Remarks

Currently, two species of Gastrotaenia have been described from swans, G. cygni from swans in North and South America (Willers & Olsen, 1969; Wolffhügel, 1938) and G. paracygni from swans in Eurasia (Czapliński & Ryžikov, 1966). Differentiation of these two species is based primarily on differences of the sizes and morphology of the rostellar hooks (Table 1) as the morphology of the features of the strobilar genital systems is difficult to define without extensive series of transverse histological sections (Willers & Olsen, 1969).

The Australian specimens of Gastrotaenia from an endemic species of swan are described here and found to be closest morphologically to G. paracygni from European swans, based primarily on rostellar hook lengths and differ significantly in this regard from G. cygni found in North and South American swans (Table 1).

Utilising the same criterion, the Australian specimens differ slightly from G. paracygni in that the hook lengths are very similar but do not quite overlap (Table 1). In the case of the Australian material, there was very little variation in hook length, whether the hooks were measured in entire mounts or in squash preparations, and there were no obvious differences in measurements from the four localities from which specimens were available. However, the metrical data available from the original description of G. paracygni are extremely limited. Czapliński and Ryžikov (1966) provided measurements based primarily on three specimens of their new species and gave no indication of the number of hooks upon which the range of measurements they presented was based. Until more morphometric data become available for European specimens of G. paracygni, it is difficult to assess the relationships with the current Australian specimens. In the original description of G. paracygni, Czapliński and Ryžikov (1966) noted that they had also examined eight captive C. atratus in Russia and Poland and found them not to be infected with Gastrotaenia. These data, together with the slight differences in hook sizes, may suggest that the specimens reported here could belong to an independent species, but the evidence available to date is insufficient to support this hypothesis and consequently, the Australian specimens described here are attributed to G. cf. paracygni until additional evidence becomes available to potentially consider them as separate taxa. Czapliński (in Czapliński & Vaucher, 1994, p. 617) provided additional previously unpublished figures of the anatomy of G. paracygni.

Czapliński (in Czapliński & Vaucher, 1994, p. 616) noted the occurrence of Gastrotaenia (species not specified) in Australia, presumably based on collections made in Australia by Czaplinski in 1984 (ANWC C433) but which were never published. However, this record is presumably also the basis for the generic level identifications in Mawson et al. (1986).

The life cycle of this species was elucidated in Poland by Wisniewski (1971) who described the development of the metacestode in the copepod Eudiaptomus vulgaris (Schmeil).

Gastrotaenia sp.

Strobilae clearly belonging to Gastrotaenia but lacking scoleces and therefore not identifiable to species were found in the Pacific black duck, Anas superciliosa Gmelin, from Lake Cowal, New South Wales (ANWC C470) and Berembed Weir, Wagga Wagga, New South Wales (ANWC C446) as well as from the musk duck, Biziura lobata (Shaw) from Lake Cowal, New South Wales (ANWC C479).

Discussion

The species of Gastrotaenia currently identifiable in Australian anatids are referable to two species, G. dogieli from ducks and G. paracygni from swans, both known from Europe, particularly Poland and Russia. Although the morphology of the strobila is difficult to examine other than in transverse histological sections (Willers & Olsen, 1969), the currently known species are readily distinguishable based on the size and morphology of the rostellar hooks. Gastrotaenia cygni and G. paracygni from swans are differentiated primarily based on the length of the rostellar hooks (Table 1), while G. dogieli not only has shorter hooks but also has a hook guard almost as long as the hook blade, while in the species from swans, the guard is shorter than the blade. For this reason, measurements of hook blade, guard and handle as well as total hook length are presented here for the first time to facilitate comparisons. The collections noted here included specimens from some species of ducks (Anas superciliosa and Biziura lobata) in which no scoleces were present, preventing specific identification. It is likely that more extensive studies of the cestodes of Australian ducks could significantly extend the host range of G. dogieli in Australian anatids.

Current records of the cestode parasites of Australian anatids suggest that the fauna consists of a mixture of cosmopolitan and endemic species (Mawson et al., 1986). The two species reported here for the first time in Australia appear to belong to the group of cosmopolitan species. However, with so many incompletely identified cestodes remaining from Australian anatids (Mawson et al., 1986), the eventual composition of the fauna remains to be determined.

Ethics statement

This project was based exclusively on preserved museum material.

Acknowledgments

Thanks are due to Dr L. Chisholm and Dr D. M. Spratt for access to collections held in the SAM and the ANWC, respectively, and to (the late) Prof. Bogdan Czaplinski for making the slide preparations of the duck cestodes in ANWC and for annotating the slides with hook lengths and numbers. Two reviewers are also thanked for their comments on the manuscript.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Supplementary material

Supplemental data for this article can be accessed online at https://doi.org/10.1080/03721426.2023.2295245.

Additional information

Funding

This contribution received no funding support.