Abstract
Abbreviata baltazardi Chabaud, 1953 (Nematoda: Physalopteridae) is a hitherto poorly known parasitic nematode species reported from Phrynocephalus helioscopus Pallas (Squamata: Agamidae) in Iran. The current knowledge on the morphology of A. baltazardi is still very limited. In the present study, the detailed morphology of A. baltazardi was studied using light microscopy and, for the first time, scanning electron microscopy, based on newly collected specimens from the yarkand toad-headed agama P. axillaris Blanford Pallas (Squamata: Agamidae) in China. Some erroneous or previously unreported morphological features of A. baltazardi were observed using SEM, which include the presence of one large semicircular protrusion and 20–30 denticles on each pseudolabium, the absence of precloacal medioventral papilla in some individuals and the presence of 4–5 postcloacal medioventral papillae in males. SEM observations also clearly showed the detailed morphology of deirids, cloacal ornamentation, caudal papillae, vulva and egg. Abbreviata baltazardi represents the first species of Abbreviata Travassos, 1920 reported in China.
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Introduction
The genus Abbreviata (Nematoda: Spirurida: Physalopteridae), erected by Travassos (1920), currently includes about 47 nominal species, which mainly parasitize the reptiles and mammals worldwide (Morgan, 1945; Skrjabin & Sobolev, 1964; Yeh, 1957; Jones, 1978, 1983, 1988, 2013; Bursey & Brooks, 2011; Johkool et al., 2021). However, most of the Abbreviata species have been described based only on morphological characters using light microscopy, which may prevent a clear observation of some morphological features with taxonomic significance, especially in relation to the details of the cephalic structures. With the success of scanning electron microscopy in the redescription of some physalopterid nematodes (Chen et al., 2017, 2023; Harras & Elmahy, 2019; Tang et al., 2022), many erroneous or previously unreported morphological features were revealed, improving the specific identification.
In the present study, several nematode specimens collected in the yarkand toad-headed agama Phrynocephalus axillaris Blanford Pallas (Squamata: Agamidae) from China, were identified as the poorly known physalopterid species Abbreviata baltazardi Chabaud, 1953. The detailed morphology of A. baltazardi was studied using light microscopy and, for the first time, scanning electron microscopy.
Materials and methods
A total of 90 individuals of the species P. axillaris (Sauria: Agamidae) (mean snout - vent length 44.37±4.38 mm, mean body weight 4.43±1.09 g) were collected from the Tokson County (88.76051979E, 42.82725354N) and Shanshan (89.87067977E, 42.76818498N) County in Xinjiang, China. A total of 141 nematodes found from the stomach and small intestine of the lizards, were washed in saline, and then fixed and stored in 70% ethanol. For light microscopy, nematode specimens were cleared in glycerin, and then examined using a Nikon® optical microscope (Nikon ECLIPSE Ni-U, Nikon Corporation, Tokyo, Japan). For scanning electron microscopy (SEM), the anterior and posterior ends of the specimens were transferred to 4% formaldehyde solution, post-fixed in 1% OsO4, dehydrated via an ethanol series and acetone and critical point dried in CO2. The specimens were coated with gold and examined using a Hitachi S-4800 scanning electron microscope (Hitachi Ltd., Tokyo, Japan) at an accelerating voltage of 20 kV. Voucher specimens were deposited in the College of Life Sciences, Hebei Normal University, Hebei Province, China. Measurements (the range, followed by the mean in parentheses) are given in micrometres unless otherwise stated.
Results
Family Physalopteridae Railliet, 1893
Genus Abbreviata Travassos, 1920
Abbreviata baltazardi Chabaud, 1953 (Figs. 1–3)
Small-sized, whitish nematodes. Cuticle with fine transverse striations. Body cylindrical, tapering at both ends; maximum width at about mid-body. Cephalic cuticular collar absent in most of specimens (only few individuals with slightly cephalic cuticular inflation). Cephalic end dome-shaped, oral aperture dorsoventrally elongate, surrounded by two lateral pseudolabia (Figs. 1A, C, 2A, B). Inner margin of each pseudolabium with row of small pointed denticles (about 20–30 on each row, some apically bifurcated) and single large median tooth, surrounded by one large semicircular protrusion (Figs. 1A, C, 2A, B, D). Each pseudolabium bearing two large cephalic papillae and one median amphid (amphidial papilla-like pore located at proximal edge of semicircular protrusion) (Figs. 1C, 2A, B). Oesophagus divided into anterior short muscular portion and posterior long glandular portion (Figs. 3A-C). Nerve ring encircling posterior part of muscular oesophagus (Figs. 3A-C). Excretory pore situated slightly posterior to junction of muscular and glandular oesophagus in both sexes (Figs. 3A, C). Deirids well developed, finger-like, slightly posterior to nerve ring (Figs. 1B, 3B). Posterior end of body sexually dimorphic.
Male (based on 6 mature specimens): Body 7.73–9.41 (8.54) mm long; maximum width 340–380 (355). Entire oesophagus 1.47–1.91 (1.68) mm long, representing 17.3–21.2 (19.6) % of body length; muscular portion 179–256 (208) long, 48–63 (56) wide; glandular portion 1.27–1.71 (1.47) mm long, 120–150 (130) wide; length ratio of two oesophageal portions 1: 6.20–8.40 (1: 7.10). Nerve-ring, deirids and excretory pore 208–227 (217), 328–410 (361) and 319–396 (348) from cephalic extremity, respectively. Posterior end of body spirally coiled ventrally. Spicules dissimilar in length and shape; left spicule slender, relatively long, basal of left spicule distinctly inflated to bulb, 280–360 (300) long, representing 3.17–3.97 (3.50) % of body length; right spicule robust, relatively short, 180–210 (190) long, representing 1.90–2.56 (2.29) % of body length; spicule (right: left) ratio 1/1.33–2.00 (1/1.54) (Figs. 3J). Posterior expansion of cuticle forming caudal bursa, supported by four pairs of ventro-lateral pedunculate papillae (1 pair precloacal, 2 paracloacal, 1 pair postcloacal) (Figs. 1D, E, F, 3E, F). Cloacal labia ornamented with numerous cuticular tubercles (Figs. 1D, E, F, 3E). Anterior margin of cloaca with two small subventral pedunculate papillae, single medio-ventral sessile papilla may be present or absent; posterior margin of cloaca with 4–5 subventral sessile papillae (Figs. 1D, E, F, 3E). Three additional pairs of ventro-lateral postcloacal papillae present (2 pairs close to each other located at anterior 2/5 of tail, 1 pair located at posterior 1/3 of tail) (Figs. 1D, G, 3E, E). Tail 440–507 (479) long, representing 4.99–5.95 (5.62) % of body length (Figs. 1D, G, 3E, F).
Female (based on 13 mature specimens): Body 6.20–12.8 (10.4) mm long; maximum width 340–640 (514). Entire oesophagus 1.42–2.78 (2.08) mm long, representing 16.6–25.4 (20.4) % of body length; muscular portion 154–260 (208) long, 53–80 (70) wide; glandular portion 1.27–2.56 (1.87) mm long, 120–300 (184) wide; length ratio of two oesophageal portions 1: 7.40–11.6 (1: 9.00). Nerve-ring, deirids and excretory pore 188–246 (223), 348–450 (384) and 275–450 (384) from cephalic extremity, respectively. Vulva with conspicuous protruded labia, situated 1.20–2.31 (1.94) mm from cephalic extremity, at 15.2–24.3 (19.0) % of body length (Figs. 2E, 3A). Vagina long, muscular; uteri with four uterine branches (Fig. 3A, D). Eggs oval, thick-shelled, unembryonated or embryonated, with smooth surface, 33–70 (60.4) × 25–40 (32.9) (n=64) (Figs. 2C, 3H, I). Tail 200–430 (344) long, representing 2.98–4.13 (3.35) % of body length (Figs. 2F, 3G).
Host and locality: Yarkand toad-headed agama Phrynocephalus axillaris Blanford Pallas (Squamata: Agamidae), Tokson County (88.76051979E, 42.82725354N) and Shanshan County(89.87067977E, 42.76818498N) in Xinjiang, China.
Site of infection: Stomach and intestine.
Prevalence and intensity: 20.0% (18 out of 90 individuals of P. axillaris) and 7.45 ± 7.42 (1–20) nematodes.
Voucher specimens: 6 male, 13 females (HBNU–N–R20240422GL), deposited in the College of Life Sciences, Hebei Normal University, Hebei Province, China.
Discussion
Chabaud (1953) described A. baltazardi infecting P. helioscopus Pallas (Squamata: Agamidae) in Iran. Since then, this species has never been reported. Therefore, as far as we know, the present study is only the second record of A. baltazardi. The morphology and measurements of the present specimens collected in P. axillaris are more or less identical to the original description of this species of A. baltazardi in many features, such as the body and oesophageal length, the shape and length of spicules, the number and arrangement of caudal papillae, the morphology and position of vulva, the number of uterine branches, the size of eggs and the length and morphology of tail from the males and females. It should be noted that the present specimens were collected from P. axillaris, which is a congener to the type-host. Therefore, we have no hesitation in considering the present material as A. baltazardi.
Chabaud (1953) reported approximately 24 denticles along the inner margin of each pseudolabium. The present SEM observations showed the presence of 20–30 denticles on each pseudolabium, some of which are apically dichotomous. Additionally, SEM observations revealed the presence of one large semicircular protrusion surrounding the median tooth on each pseudolabium for the first time. Chabaud (1953) illustrated the single medio-ventral, precloacal papilla in the male, which is very common in Abbreviata spp. (Yeh, 1957; Skrjabin & Sobolev, 1964; Jones, 1978, 1983, 1988, 2013; Bursey & Brooks, 2011). However, this feature seems to be inconsistent, because we observed the presence of single medio-ventral precloacal papilla only in some individuals of the present material. Moreover, the detailed morphology of deirids, cloacal ornamentation, caudal papillae, vulva and egg was showed by SEM for the first time.
In the genus Abbreviata, A. baltazardi is similar to A. amaniensis (Sandground, 1928) and A. golvani Le-Van-Hoa, 1961 by having each pseudolabium possessing single large median tooth without bifid submedian tooth, spicules smaller than 0.50 mm and left spicule less than 2 times longer than the right one (Sandground, 1928; Skrjabin & Sobolev, 1964). However, A. baltazardi can be easily distinguished from A. amaniensis based on the pseudolabium with large semicircular protrusion (vs absence in A. amaniensis), different morphology of the left spicule (proximal end of left spicule distinctly bulbous in A. baltazardi vs with conspicuous beak-like protrusion in A. amaniensis) and the presence of 4–5 medio-ventral, postcloacal papillae (vs only two medio-ventral, postcloacal papillae in A. amaniensis). Abbreviata baltazardi is also different from A. golvani by the distinctly smaller body (male 7.73–9.41 mm and female 6.20–12.8 mm long in A. baltazardi vs male 12.0–18.0 mm and female 26.0 mm long in the latter) and different morphology of left spicule (proximal end of left spicule distinctly bulbous in A. baltazardi vs not bulbous in A. golvani). Abbreviata baltazardi represents the first species of Abbreviata reported from China.
Data availability
All data generated or analyzed during this study are included in this published article. For the raw data, please contact the corresponding author.
References
Bursey, C. R., & Brooks, D. R. (2011). Nematode parasites of Costa Rican snakes (Serpentes) with description of a new species of Abbreviata (Physalopteridae). Comparative Parasitology, 78(2), 333–358.
Chabaud, A. G. (1953). Un nouveau physaloptère parasite d’agame. Annales de Parasitologie Humaine et Comparée, 28(4), 305–311.
Chen, H.-X., Ju, H.-D., Li, Y., & Li, L. (2017). Further study on Physaloptera clausa Rudolphi, 1819 (Spirurida: Physalopteridae) from the amur hedgehog Erinaceus amurensis Schrenk (Eulipotyphla: Erinaceidae). Acta Parasitologica, 62, 846–852.
Chen, H.-X., Zeng, J.-L., Gao, Y.-Y., Zhang, D., Li, Y., & Li, L. (2023). Morphology and genetic characterization of Physaloptera sibirica Petrow & Gorbunov, 1931 (Spirurida: Physalopteridae), from the hog-badger Arctonyx collaris Cuvier (Carnivora: Mustelidae), with molecular phylogeny of Physalopteridae. Parasites & Vectors, 16(1), e227.
Harras, S. F., & Elmahy, R. A. (2019). New record of Abbreviata leptosoma Gervais, 1848 (Spirurida: Physalopteridae) infection in two species of lizards in North and South Sinai, Egypt. Egyptian Journal of Zoology, 72, 1–10.
Johkool, M. G., Eslahi, A. V., Badri, M., Hooshmand, E., Pirestani, M., Jablonski, D., Jafari, R., & Dalimi, A. (2021). Molecular and morphological data confirmed first record of Abbreviata kazakhstanica Markov and Paraskiv, 1956 (Spirurida: Physalopteridea) in Iran. Iranian Journal of Parasitology, 16(4), 686–691.
Jones, H. I. (1978). Abbreviata (Nematoda: Physalopteroidea) from Western Australian snakes. Australian Journal of Zoology, 26, 789–807.
Jones, H. I. (1983). Abbreviata (Nematoda: Physalopteridae) in lizards of the Varanus gouldii complex (Varanidae) in Western Australia. Australian Journal of Zoology, 31, 285–298.
Jones, H. I. (1988). Nematodes from nine species of Varanus (Reptilia) from tropical Northern Australia, with particular reference to the genus Abbreviata (Physalopteridae). Australian Journal of Zoology, 36, 691–708.
Jones, H. I. (2013). Gastrointestinal nematodes of the Australian leaf-tailed gecko, Phyllurus platurus (Reptilia: Gekkonidae), with a redescription of Abbreviata bancrofti (Irwin-Smith, 1922) and observations on physalopterid larvae. Comparative Parasitology, 80(2), 217–224.
Morgan, B. B. (1945). The Nematode genus Abbreviata (Travassos, 1920), Schulz, 1927. The American Midland Naturalist, 34(2), 485–490.
Sandground, J. H. (1928). Some new cestode and nematode parasites from Tanganyika Territory. Proceedings of the Boston Society of Natural History, 39, 131–150.
Skrjabin, K. I., & Sobolev, A. A. (1964). Principles of nematology. Vol. XII. Spirurates of animal and man and the diseases caused by them. Part II. Physalopteroidea. Izdat, AN SSSR, Moscow, Russia, 334 pp.
Tang, L.-S., Gu, X.-H., Wang, J.-H., Ni, X.-F., Zhou, K.-F., & Li, L. (2022). Morphological and molecular characterization of Paraleptus chiloscyllii Yin & Zhang, 1983 (Nematoda: Physalopteridae) from the brownbanded bambooshark Chiloscyllium punctatum Müller & Henle (Elasmobranchii: Orectolobiformes). Parasitology International, 87, e102511.
Travassos, L. (1920). Contribuições para o conhecimento da fauna helmintologica brazileira. Memórias do Instituto Oswaldo Cruz, 12, 73–77.
Yeh, L.-S. (1957). On Physaloptera lutnsdeni n. sp. from a bush-baby in Tanganyika, with a note on Abbreviata caucasica. Journal of Helminthology, 31 (1–2), 29–32.
Funding
This study was supported by the National Natural Science Foundation of China (Grant No. 32170442), Natural Science Foundation of Xinjiang Autonomous Region (2022D01A194), and Talent Development Fund of the Autonomous Region “Tianchi Talents” introduction plan project for Dr. Xiao-Fei Yan.
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X.H.G. and L.L. identified the nematode specimens. X.F.Y. collected nematode specimens. X.H.G. and H.X.C. prepared figures 1-3. All authors wrote and reviewed the manuscript.
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Gu, X., Yan, XF., Chen, HX. et al. Further description of the poorly known zooparasitic nematode Abbreviata baltazardi Chabaud, 1953 (Spirurida: Physalopteridae). Syst Parasitol 101, 52 (2024). https://doi.org/10.1007/s11230-024-10176-x
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DOI: https://doi.org/10.1007/s11230-024-10176-x