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Huffmanela sp. (Nematoda: Trichosomoididae: Huffmanelinae) encountered in the whitecheek shark (Carcharhinus dussumieri) in the Arabian Gulf Cover

Huffmanela sp. (Nematoda: Trichosomoididae: Huffmanelinae) encountered in the whitecheek shark (Carcharhinus dussumieri) in the Arabian Gulf

Helminthologia
Volume 58 (2021): Issue 3 (September 2021)
By: M. M. Attia,  M. M. Ibrahim,  M. A. Mahmoud and  M. N. S. Al-Sabi  
Open Access
|Sep 2021

Figures & Tables

Fig. 1

Gross external lesions on skins of whitecheek shark (Carcharhinus dussumieri) showing the presence of (A) Black irregular lines with very minute black spots in the ventral aspect of head region and near the snout. (B) Prominent black irregular lines in the dorsal region of the head.
Gross external lesions on skins of whitecheek shark (Carcharhinus dussumieri) showing the presence of (A) Black irregular lines with very minute black spots in the ventral aspect of head region and near the snout. (B) Prominent black irregular lines in the dorsal region of the head.

Fig. 2

Eggs of Huffmanela sp. isolated from skins of whitecheek shark (Carcharhinus dussumieri) and examined using light microscope. (A) Immature stage of the eggs, stage 1, showing dark brown eggshell, slightly protruding polar plug (p), vitelline mass (vm), and outer shell layer (ol). (B) Mature eggs, stage 2, showing the brown-shelled egg containing developing larva (dl), markedly protruding polar plugs (p), and outer shell layer (ol). (C) Mature eggs, stage 2, showing fully developed brown-shelled egg containing an outer layer, missing polar plugs, and ready to hatch a fully developed larva (l). Scale bar in A, B, and C = 25μm.
Eggs of Huffmanela sp. isolated from skins of whitecheek shark (Carcharhinus dussumieri) and examined using light microscope. (A) Immature stage of the eggs, stage 1, showing dark brown eggshell, slightly protruding polar plug (p), vitelline mass (vm), and outer shell layer (ol). (B) Mature eggs, stage 2, showing the brown-shelled egg containing developing larva (dl), markedly protruding polar plugs (p), and outer shell layer (ol). (C) Mature eggs, stage 2, showing fully developed brown-shelled egg containing an outer layer, missing polar plugs, and ready to hatch a fully developed larva (l). Scale bar in A, B, and C = 25μm.

Fig. 3

Scanning electron micrographs of Huffmanela sp. eggs (Nematoda, Trichosomoididae, Huffmanelinae) recovered from whitecheek shark (Carcharhinus dussumieri). (A) Infected skin of shark showing crowns of placoid scales (ps). (B) Skin scraping from a shark showing the nematode egg (arrows). (C, D, and E) Eggs recovered from skin scraping of a shark showing smooth shell (sh) and slightly protruding plug (p). (F) Posterior end of Huffmanela sp. eggs, showing ready to hatch larvae (l).
Scanning electron micrographs of Huffmanela sp. eggs (Nematoda, Trichosomoididae, Huffmanelinae) recovered from whitecheek shark (Carcharhinus dussumieri). (A) Infected skin of shark showing crowns of placoid scales (ps). (B) Skin scraping from a shark showing the nematode egg (arrows). (C, D, and E) Eggs recovered from skin scraping of a shark showing smooth shell (sh) and slightly protruding plug (p). (F) Posterior end of Huffmanela sp. eggs, showing ready to hatch larvae (l).

Fig. 4

Histopathology of skins of whitecheek shark (Carcharhinus dussumieri) showing the pathology induced by the presence of eggs of Huffmanela sp..(A) Apparently normal epidermal region (ep) and affected epidermis with multiple eggs (e) of Huffmanela sp. between the placoid scales. (B) Affected epidermis with eggs of Huffmanela sp. (e), desquamated epithelial cells (ec), and detached placoid scales (ps). (C) Multiple eggs of Huffmanela sp. containing developing larvae (la), desquamated epithelium and pyknotic nuclei in stratum laxum. (D) congested blood vessel (co), area of hemorrhage (h) and edema (ed) with no presence of parasitic eggs in the underlying musculature (m). (H&E staining).
Histopathology of skins of whitecheek shark (Carcharhinus dussumieri) showing the pathology induced by the presence of eggs of Huffmanela sp..(A) Apparently normal epidermal region (ep) and affected epidermis with multiple eggs (e) of Huffmanela sp. between the placoid scales. (B) Affected epidermis with eggs of Huffmanela sp. (e), desquamated epithelial cells (ec), and detached placoid scales (ps). (C) Multiple eggs of Huffmanela sp. containing developing larvae (la), desquamated epithelium and pyknotic nuclei in stratum laxum. (D) congested blood vessel (co), area of hemorrhage (h) and edema (ed) with no presence of parasitic eggs in the underlying musculature (m). (H&E staining).

Fig. 5

Tansmission electron micrographs of semi-thin and ultra-thin sections of skin of whitecheek shark (Carcharhinus dussumieri) affected with egg of Huffmanela sp.. (A) Semi-thin image showing an egg in the epidermis with non-lamellated eggshell (es), with polar plugs (pp), the eggs were embedded between placoid scales (ps) and desquamated epithelial cells (ec). (B-D): Transmission electron micrographs showing (B) Epithelial cell (ec) and lymphocyte (lc) in the affected area, (C) A parasitic egg (e) surrounded with macrophages (ma), and (D) Melanophores containing melanin pigments appearing near a red blood cell (r). Scale bar in B and C = 2μm, and in D = 500nm.
Tansmission electron micrographs of semi-thin and ultra-thin sections of skin of whitecheek shark (Carcharhinus dussumieri) affected with egg of Huffmanela sp.. (A) Semi-thin image showing an egg in the epidermis with non-lamellated eggshell (es), with polar plugs (pp), the eggs were embedded between placoid scales (ps) and desquamated epithelial cells (ec). (B-D): Transmission electron micrographs showing (B) Epithelial cell (ec) and lymphocyte (lc) in the affected area, (C) A parasitic egg (e) surrounded with macrophages (ma), and (D) Melanophores containing melanin pigments appearing near a red blood cell (r). Scale bar in B and C = 2μm, and in D = 500nm.

Fig. 6

Transmission electron micrographs of Huffmanela sp. eggs (Nematoda, Trichosomoididae, Huffmanelinae) recovered from skin scrapings from whitecheek shark (Carcharhinus dussumieri). (A) Cross section of eggs with mature larva. (B) Ultrastructure of eggs layers showing all parts of the eggshell. The vitelline layer (v) was thin and smooth and had no projections, spines, ridges or filaments. The chitinous layer (cl) had two different electron densities or parts identified as an external and an internal homogenous part that was not lamellated nor contained ridges. (C) Ultrastructure of eggs layers showing the presence of a third, thin lipid layer (lp) that was translucent and homogeneous. (D) Higher magnification showing larva (l) inside the eggs with appearance of its intestine (i) and larval tissues. Scale bar in A = 2μm; in B, C, and D = 500nm.
Transmission electron micrographs of Huffmanela sp. eggs (Nematoda, Trichosomoididae, Huffmanelinae) recovered from skin scrapings from whitecheek shark (Carcharhinus dussumieri). (A) Cross section of eggs with mature larva. (B) Ultrastructure of eggs layers showing all parts of the eggshell. The vitelline layer (v) was thin and smooth and had no projections, spines, ridges or filaments. The chitinous layer (cl) had two different electron densities or parts identified as an external and an internal homogenous part that was not lamellated nor contained ridges. (C) Ultrastructure of eggs layers showing the presence of a third, thin lipid layer (lp) that was translucent and homogeneous. (D) Higher magnification showing larva (l) inside the eggs with appearance of its intestine (i) and larval tissues. Scale bar in A = 2μm; in B, C, and D = 500nm.

Fig. 7

Seasonal prevalence (%) of Huffmanela sp. in whitecheek shark (Carcharhinus dussumieri) during 2017 in El-Jubail, Saudi Arabia. Black line with *** on top indicates statistical significant difference (p-value < 0.001) in prevalence rates between the two lined, adjacent seasons.
Seasonal prevalence (%) of Huffmanela sp. in whitecheek shark (Carcharhinus dussumieri) during 2017 in El-Jubail, Saudi Arabia. Black line with *** on top indicates statistical significant difference (p-value < 0.001) in prevalence rates between the two lined, adjacent seasons.

Fig. S1

Supplementary materials
Supplementary materials
DOI: https://doi.org/10.2478/helm-2021-0030 | Journal eISSN: 1336-9083 | Journal ISSN: 0440-6605
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Language: English
Page range: 281 - 291
Submitted on: Dec 23, 2020
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Accepted on: Jul 12, 2021
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Published on: Sep 30, 2021
Published by: Slovak Academy of Sciences, Institute of Parasitology
In partnership with: Paradigm Publishing Services
Publication frequency: 4 issues per year
Keywords:
Egg morphology,
shark,
skin parasite,
prevalence
Related subjects:
Life sciences,
Zoology,
Ecology,
Life sciences, other,
Medicine,
Clinical medicine,
Microbiology, virology and infection epidemiology

© 2021 M. M. Attia, M. M. Ibrahim, M. A. Mahmoud, M. N. S. Al-Sabi, published by Slovak Academy of Sciences, Institute of Parasitology
This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 License.

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