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Morphological, molecular, and histopathological studies on Hadjelia truncata from Columba livia domestica and its role as an environmental biological indicator


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Figure 1:

Photomicrographs for the Hadjelia truncata infecting the domestic pigeons. (A–F) Anterior extremity. (G–I) Middle part for female worms. (J–L) The posterior extremity of females. (M) Embryonated egg in feces. (N–Q) The posterior extremity of male worms. Note: L, lips; IL, interlabia, PA, papillae; CU, cuticle; PH, pharynx; MOE, muscular oesophagus; IN, intestine; GOE, glandular esophagus; Black arrow, constriction at the end of pharynx; EG, embryonated eggs; RT, rectum; IN, intestine; T, tail; AN, anal opening; White arrow, vaginal opening, UT, uterus; RSP, right spicules; LSP, left spicules; PCP, pre-cloacal papillae; POCP, post-cloacal papillae; CA, caudal alae; CO, cloacal opening.
Photomicrographs for the Hadjelia truncata infecting the domestic pigeons. (A–F) Anterior extremity. (G–I) Middle part for female worms. (J–L) The posterior extremity of females. (M) Embryonated egg in feces. (N–Q) The posterior extremity of male worms. Note: L, lips; IL, interlabia, PA, papillae; CU, cuticle; PH, pharynx; MOE, muscular oesophagus; IN, intestine; GOE, glandular esophagus; Black arrow, constriction at the end of pharynx; EG, embryonated eggs; RT, rectum; IN, intestine; T, tail; AN, anal opening; White arrow, vaginal opening, UT, uterus; RSP, right spicules; LSP, left spicules; PCP, pre-cloacal papillae; POCP, post-cloacal papillae; CA, caudal alae; CO, cloacal opening.

Figure 2:

A consensus phylogenetic tree constructed with neighbor joining (NJ) and maximum likelihood (ML) methods, showing phylogenetic relationships between Hadjelia truncata and related taxa in NCBI GenBank with Ascaris lumbricoides as an outgroup. The ML and NJ trees are inferred from the 18S rDNA sequences data generated from the H. truncata recovered from Columba livia domestica (OR122274 to OR122276 given in bold) and related taxa from GenBank. Numbers indicated at branch nodes are bootstrap values (ML/NJ). Only bootstraps > 60% are shown.
A consensus phylogenetic tree constructed with neighbor joining (NJ) and maximum likelihood (ML) methods, showing phylogenetic relationships between Hadjelia truncata and related taxa in NCBI GenBank with Ascaris lumbricoides as an outgroup. The ML and NJ trees are inferred from the 18S rDNA sequences data generated from the H. truncata recovered from Columba livia domestica (OR122274 to OR122276 given in bold) and related taxa from GenBank. Numbers indicated at branch nodes are bootstrap values (ML/NJ). Only bootstraps > 60% are shown.

Figure 3:

A consensus phylogenetic tree constructed with neighbor joining (NJ) and maximum likelihood (ML) methods, showing phylogenetic relationships between Hadjelia truncata and related taxa in NCBI GenBank. The ML and NJ trees are inferred from the Cytochrome subunit C oxidase I (COX I) DNA sequences data generated from the H. truncata recovered from Columba livia domestica (OR122277 to OR122279 given in bold) and related taxa from GenBank. Numbers indicated at branch nodes are bootstrap values (ML/NJ). Only bootstraps > 70% are shown.
A consensus phylogenetic tree constructed with neighbor joining (NJ) and maximum likelihood (ML) methods, showing phylogenetic relationships between Hadjelia truncata and related taxa in NCBI GenBank. The ML and NJ trees are inferred from the Cytochrome subunit C oxidase I (COX I) DNA sequences data generated from the H. truncata recovered from Columba livia domestica (OR122277 to OR122279 given in bold) and related taxa from GenBank. Numbers indicated at branch nodes are bootstrap values (ML/NJ). Only bootstraps > 70% are shown.

Figure 4:

Photographs of the gizzards of the domestic pigeons. (A) Non-infected gizzard. (B) Enlargement of the infected gizzard. (C) Normal koilin layer. (D and E) Nematodes infection under the koilin layer of the gizzard.
Photographs of the gizzards of the domestic pigeons. (A) Non-infected gizzard. (B) Enlargement of the infected gizzard. (C) Normal koilin layer. (D and E) Nematodes infection under the koilin layer of the gizzard.

Figure 5:

(A–C) Histopathological sections from the gizzard’s wall infected with Hadjelia truncata, exhibiting the transverse sections of the nematodes (black arrows) with a large number of embryonated eggs (EG). The koilin layer is disrupted and fragmented with multiple clear spaces (asterisks).
(A–C) Histopathological sections from the gizzard’s wall infected with Hadjelia truncata, exhibiting the transverse sections of the nematodes (black arrows) with a large number of embryonated eggs (EG). The koilin layer is disrupted and fragmented with multiple clear spaces (asterisks).

Heavy metals in the gizzard of the domestic pigeons and its parasite

Heavy metals Non-infected pigeon Infected pigeon Parasite
Fe 2.176 ± 0.02 0.741 ± 0.02 a 1.463 ± 0.02 ab
Cu 0.690 ± 0.01 0.120 ± 0.01 a 0.313 ± 0.01 ab
Zn 0.911 ± 0.02 0.409 ± 0.01 a 0.522 ± 0.02 ab
Cd 0.034 ± 0.001 0.010 ± 0.001 a 0.036 ± 0.001 ab
Cr 0.559 ± 0.01 0.267 ± 0.01 a 0.518 ± 0.02 ab
Co 0.166 ± 0.01 0.086 ± 0.001 a 0.114 ± 0.01 ab

Bioaccumulation of heavy metals concerning nematode parasite/pigeon model

Heavy metals C[Hadjelia truncata]/C[pigeon organ]

Liver Muscles Gizzard
Fe 1.431 1.675 1.974
Cu 2.371 2.445 2.608
Zn 2.063 1.611 1.276
Cd 3.272 2.250 3.600
Cr 1.519 5.630 1.940
Co 1.096 1.341 1.325

Morphological characteristics of male worms for Hadjelia truncata from the domestic pigeons

Source of Hadjelia truncata Body Esophagus Distance of nerve ring from anterior end Spicule length Caudal papillae Tail length



Length Width Muscular length Glandular length Right Left
Cram, 1927 5–7 0.220 1.6 Six pairs (4 pre- & 2 post-) of caudal papillae
Baer, 1954 8 0.285 0.033 0.225–0.300 1.320–1.600
Ibrahim et al., 1995 4–8 (6.4) 1.8–2.7 (2.2)
Junker & Boomker, 2007 7–8 0.145–0.160 0.042–0.044 1.750–1.927 0.208–0.212 0.254–0.271 1.346–1.434
Razmi et al., 2007 7–9 0.34 1.26
Sentíes-Cué et al., 2011 6.5–9 0.35 1.27
Naem et al., 2013 6.5–9 0.151 0.35 1.27
Nabavi et al., 2013 1–2 0.320–0.350 1.410–1.470
Al-Moussawi, 2015 7–8 (7.5) 0.204–0.258 (0.231) 0.374–0.386 (0.380) 1.620–1.680 (1.650) 0.198–0.211 (0.204) 0.240–0.270 (0.255) 1.512–1.620 (1.566) 0.127–0.138 (0.132)
Oryan et al., 2016 7.5
Jameel et al., 2016 6.5–9
Khordadmehr et al., 2018 7–11
Present study, 2023 6.201–8.023 (7.270) 0.191–0.219 (0.204) 0.353–0.376 (0.367) 1.599–1.758 (1.623) 0.184–0.201 (0.197) 0.270–0.320 (0.284) 1.332–1.511 (1.416) 0.118–0.127 (0.122

Morphological characteristics of female worms for Hadjelia truncata from the domestic pigeons

Source of Hadjelia truncata Body Esophagus Distance from anterior end Eggs Tail length




Length Width Muscular length Glandular length Nerve ring Vulva opening Length Width Status
Cram, 1927 10–16 0.300 2.6–16 0.027 Numerous embryonated eggs covered with thick-shelled
Baer, 1954 8–16 0.143–0.285 1.640–3.000
Ibrahim et al., 1995 17–22 (20) 2.0–2.4 (2.4) 1.5–2.5 (2) 0.050 0.030
Junker & Boomker, 2007 10–11 0.140–0.217 0.005–0.007 1.948–2.076 0.159–0.185 1.691–2.238 0.050–0.053 0.032–0.035 0.121–0.138
Razmi et al., 2007 13–17
Al-Moussawi, 2008 14–15.22 (14.62) 0.168–0.199 (0.183) 0.512–0.57 (0.54) 0.589–0.622 (0.605) 0.003–0.024 (0.015) 0.113–0.150 (0.132)
Mohammad & Al-Moussawi, 2011 11.10–14.88 (13.15) 0.18–0.28 (0.23) 0.450–0.566 (0.461) 1.47–3.32 (2.435) 1.575–2.730 (2.281) 0.033–0.057 (0.044) 0.015–0.041 (0.034)
Sentíes-Cué et al., 2011 12–16.5
Naem et al., 2013 12 16.5 0.229 2.155
Nabavi et al., 2013 3–5 0.054–0.059 0.030–0.032
Al-Moussawi & Jassim, 2015 23.226–26.156 (24.594) 0.231–0.312 (0.2782) 3.510–3.666 (3.588) 0.260–0.312 (0.291) 3.276–3.413 (3.364) 0.052–0.104 (0.078) 0.021–0.312 (0.026) 0.104–0.234 (0.148)
Al-Moussawi, 2015 8–17 (12) 0.147–0.270 (0.224) 2.750–3.648 (3.379) 2.002–2.835 (2.215) 0.178–0.206 (0.192) 1.501–3.022 (2.108) 0.046–0.048 (0.047) 0.024–0.0408 (0.047) 0.145–0.230 (0.196)
Oryan et al., 2016 19.8 0.045 0.031
Jameel et al., 2016 12–16.5
Khordadmehr et al., 2018 15–20 0.043–0.045 0.020–0.030
Present study, 2023 12.270–18.583 (17.792) 0.256–0.314 (0.287) 3.515–3.759 (3.601) 2.160–2.211 (2.181) 0.198–0.225 (0.211) 3.011–3.054 (3.027) 0.046–0.051 (0.048) 0.029–0.033 (0.031) 0.118–0.132 (0.124)

Heavy metals in the liver of the domestic pigeons and its parasite

Heavy metals Non-infected pigeon Infected pigeon Parasite
Fe 5.907 ± 0.02 1.022 ± 0.02 a 1.463 ± 0.02 ab
Cu 0.608 ± 0.02 0.132 ± 0.01 a 0.313 ± 0.00 ab
Zn 0.935 ± 0.02 0.253 ± 0.02 a 0.522 ± 0.02 ab
Cd 0.046 ± 0.001 0.011 ± 0.001 a 0.036 ± 0.001 ab
Cr 0.617 ± 0.02 0.341 ± 0.01 a 0.518 ± 0.02 ab
Co 0.212 ± 0.01 0.104 ± 0.01 a 0.114 ± 0.01 ab

Heavy metals in the muscle of the domestic pigeons and its parasite

Heavy metals Non-infected pigeon Infected pigeon Parasite
Fe 2.222 ± 0.02 0.873 ± 0.02 a 1.463 ± 0.02 ab
Cu 0.582 ± 0.02 0.128 ± 0.01 a 0.313 ± 0.01 ab
Zn 0.974 ± 0.02 0.324 ± 0.02 a 0.522 ± 0.02 ab
Cd 0.050 ± 0.001 0.016 ± 0.001 a 0.036 ± 0.001 ab
Cr 0.592 ± 0.02 0.092 ± 0.001 a 0.518 ± 0.02 ab
Co 0.473 ± 0.01 0.085 ± 0.01 a 0.114 ± 0.01 ab
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Język:
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Dziedziny czasopisma:
Life Sciences, other