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Morphological and molecular characterisation of the nematode parasite Graphidioides affinis (Secernentea: Trichostrongylidae) in Patagonian maras, Dolichotis patagonum, kept in a zoo in Sofia, Bulgaria Cover

Morphological and molecular characterisation of the nematode parasite Graphidioides affinis (Secernentea: Trichostrongylidae) in Patagonian maras, Dolichotis patagonum, kept in a zoo in Sofia, Bulgaria

Open Access
|Aug 2024

Figures & Tables

Fig. 1.

An egg of Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria
An egg of Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria

Fig. 2.

Graphidioides affinis adult worm found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – anterior end, papillae around the oral opening (arrows); b – cuticular striations on the body; c – oesophagus
Graphidioides affinis adult worm found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – anterior end, papillae around the oral opening (arrows); b – cuticular striations on the body; c – oesophagus

Fig. 3.

Posterior body end of male Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – common view; b – 1- pre-bursal papillae, 2 - anteroventral ray of copulatory bursa, 3 - posteroventral ray of copulatory bursa; c – copulatory bursa, 1 – anterolateral ray, 2 – mediolateral ray, 3 – posterolateral ray, 4 – exterodorsal ray; d – dorsal ray of copulatory bursa (arrow)
Posterior body end of male Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – common view; b – 1- pre-bursal papillae, 2 - anteroventral ray of copulatory bursa, 3 - posteroventral ray of copulatory bursa; c – copulatory bursa, 1 – anterolateral ray, 2 – mediolateral ray, 3 – posterolateral ray, 4 – exterodorsal ray; d – dorsal ray of copulatory bursa (arrow)

Fig. 4.

Spicules of Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – proximal parts; b – distal parts
Spicules of Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – proximal parts; b – distal parts

Fig. 5.

Female Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – ovijector; b and c – vulva; d – posterior end; anus (arrow)
Female Graphidioides affinis found in the faeces of Dolichotis patagonum from the Sofia Zoo, Bulgaria; a – ovijector; b and c – vulva; d – posterior end; anus (arrow)

Fig. 6.

Phylogenetic tree of parasitic nematodes based on SSU rDNA partial sequences, constructed with the use of Bayesian inference analysis using MrBayes version 3.2.0. The general time-reversible model with estimates of invariant sites and gamma-distributed among-site variation model was chosen based on jModelTest version 2.1.4 using the Akaike information criterion. The analysis was run for 2,000,000 generations
Phylogenetic tree of parasitic nematodes based on SSU rDNA partial sequences, constructed with the use of Bayesian inference analysis using MrBayes version 3.2.0. The general time-reversible model with estimates of invariant sites and gamma-distributed among-site variation model was chosen based on jModelTest version 2.1.4 using the Akaike information criterion. The analysis was run for 2,000,000 generations

Fig. 7.

Phylogenetic tree of parasitic nematodes based on ITS2 partial sequences, constructed with the use of Bayesian inference analysis using MrBayes version 3.2.0. The gamma-distributed among-site variation model was chosen based on jModelTest version 2.1.4 using the Akaike information criterion. The analysis was run for 2,000,000 generations. Bold indicates isolates examined in the present investigation
Phylogenetic tree of parasitic nematodes based on ITS2 partial sequences, constructed with the use of Bayesian inference analysis using MrBayes version 3.2.0. The gamma-distributed among-site variation model was chosen based on jModelTest version 2.1.4 using the Akaike information criterion. The analysis was run for 2,000,000 generations. Bold indicates isolates examined in the present investigation

List of taxa included in the molecular analysis of Graphidioides affinis using sequence data of the SSU rDNA

GenBank accession no.SpeciesHostLocation
AY268117.1Caenorhabditis elegansNot applicableUSA
AJ920341.1Chabertia ovinaOvis ariesCanada
AJ920350.1Trichostrongylus colubriformisOvis ariesCanada
AJ920359.1Tetrabothriostrongylus mackerrasaeAntechinus stuartiiCanada
EU086374.1Haemonchus contortusGiraffa camelopardalisUSA/Lion Country Safari/region of origin: Africa
L04152.1H. similisNot providedUSA
OP288108.1Globocephalus urosubulatusSus scrofaBrazil
AY295811.1Necator americanusHomo sapiensGuatemala
DQ094176.1Strongylus equinusNot providedGreat Britan
AJ920342.1Cylicocyclus insignisEquus caballusCanada
LC415112.1Oesophagostomum muntiacumMuntiacus reevesiJapan
AJ920340.1Cyclodontostomum purvisiRattus sordidusCanada
OP288110.1Stephanurus dentatusSus scrofaBrazil
MN218457.1Uncinaria stenocephalaCanis latransCanada
AJ920351.1Ostertagia leptospicularisBos taurusCanada
AJ920352.1Ostertagia ostertagiBos taurusCanada
AY295820.1Troglostrongylus wilsoniLynx rufusUSA
KC771250.1Dictyocaulus viviparus bisontisBison bonasusPoland
KM374671.1Dictyocaulus cerviCervus elaphusPoland
MH756629.1Dictyocaulus skrjabiniCervus elaphusPoland
MH688454.1Lamanema chaveziLama lamaGermany/region of origin: South America
JX877671.1Travassostrongylus orloffiDidelphis marsupialisMexico
JX877677.1Travassostrongylus callisDidelphis marsupialisPanama
AJ920355.1Heligmosomoides polygyrusMus musculusCanada
JX877678.1Carolinensis perezponcedeleoniNyctomys sumichrastiUSA
JX877672.1Vexillata convolutaCratogeomys merriamiMexico
AJ920360.1Nematodirus battusOvis ariesCanada
OR611714.1Graphidioides affinisDolichotis patagonumBulgaria/Sofia Zoo/region of origin: South America
OR611716.1Graphidioides affinisDolichotis patagonumBulgaria/Sofia Zoo/region of origin: south America

List of taxa included in the molecular analysis of Graphidioides affinis using sequence data of ITS2 rDNA

GenBank accession no.SpeciesHostLocation
KF765464.1Heligmosomoides polygyrusApodemus sylvaticusNorway
MH688454.1Lamanema chaveziLama lamaGermany/region of origin: South America
Y10789.1Chabertia ovinaOvis ariesAustralia
LC415112.1Oesophagostomum muntiacumMuntiacus reevesiJapan
OQ773550.1Uncinaria stenocephalaUrsus arctosTurkey
OR353426.1Graphidioides affinisDolichotis patagonumBulgaria/Sofia Zoo/region of origin: South America
AF194138.1Nematodirus battusNot providedUK
KX358861.1Cooperia oncophoraBison bonasus caucasicusSweden/Avesta Visentpark
KX358862.1Ostertagia ostertagiBison bonasus caucasicusSweden/Avesta Visentpark
X86025.1O. leptospicularisBos taurus
KX358860.1Haemonchus contortusBison bonasus caucasicusSweden/Avesta Visentpark
AJ577460.1Spiculopteragia boehmiNot providedFrance

Comparative morphometry of Graphidioides affinis nematodes in materials from Patagonian maras (Dolichotis patagonum) investigated in different studies

Origin / References
ParameterSofia Zoo, Bulgaria (Present data)Argentina (1)London Zoo, UK (7)Barcelona Zoo Spain (5)
RangeMean ± SD
Adult male nematodes (n = 7)Body length (cm)1–21.5 ± 0.350.9–1.71.11.1–1.3
Body width at the end of the oesophagus (μm)130–155144 ± 8.97---
Maximum body width (μm)250–340291.67 ± 32.5300350350
Oesophagus length (μm)505–558537.6 ± 21.18-650-
Maximum oesophagus width (μm)82–9589 ± 5.79---
Spicule length (μm)1,930–2,7002365 ± 266.082,8003,4002,400–2,700
Gubernaculum length (μm)159–172167.29 ± 4.6115012060
Gubernaculum width (μm)48–5752.29 ± 3.86807568
Adult female nematodes (n = 7)Body length (cm)1.4–2.41.7 ± 0.331.6–2.12.12–2.5
Body width at the end of the oesophagus (μm)185–244207 ± 19.86---
Maximum body width (μm)260–440360 ± 72.34500700750
Oesophagus length609–714642 ± 37.22-650-
Maximum oesophagus width (μm)97–124114 ± 10.46---
Ovijector total length (μm)1110–14481,230 ± 117.411,2001,525-
Vulva-tail tip distance (mm)4.8–6.05 ± 0.4865.5-
Anus-tail tip distance (μm)321–442355 ± 40.54500--
Length of eggs in the uterus (μm)107–171133 ± 26.02140135-
Width of eggs in the uterus (μm)60–9475 ± 11.257575-
Language: English
Page range: 363 - 371
Submitted on: Jan 8, 2024
Accepted on: Aug 1, 2024
Published on: Aug 9, 2024
Published by: National Veterinary Research Institute in Pulawy
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year

© 2024 Mariana Panayotova-Pencheva, Zdzisław Laskowski, Anna Maria Pyziel, published by National Veterinary Research Institute in Pulawy
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 3.0 License.