Bull 409 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Bilal and Ahmed Bull. Iraq nat. Hist. Mus. (2023) 17 (3): 409-421. https://doi.org/10.26842/binhm.7.2023.17.3.0409 ORIGINAL ARTICLE COMPARATIVE ULTRASTRUCTURAL STUDY OF THE SALIVARY GLANDS OF TWO HEMATOPHAGOUS LEECHES (ANNELIDA, CLITELLATA, ARHYNCHOBDELLIDA) IN IRAQ Huda Sdiq Bilal* and Sherwan Tayeb Ahmed Department of Biology, College of Science, Salahhadin University, Erbil, Iraq. *Corresponding author: sherwan.ahmed@su.edu.krd Recived Date: 26 November 2022, Accepted Date 26 Feberuary 2023, Published Date:20 June 2023 This work is licensed under a Creative Commons Attribution 4.0 International License ABSTRACT During July - August of 2021, thirty-one leeches were collected from two localities in Erbil and its suburbs for studying the morphological features of jaws, denticles, and salivary gland cells. Leeches were two blood-sucking species; Hirudo orientalis (Utevsky & Trontelj, 2005) (Family, Hirudinidae) and Limnatis paluda (Tennent 1859) (Family, Praobdellidae). The investigations conducted using a stereomicroscope (SM) and scanning electron microscopy (SEM). H. orientalis jaws were white and rigid, bearing sharp teeth, while L. paluda jaws were gray and soft bearing fewer blunt teeth with plentiful papilla and both are monostichodont. In the present study, the salivary glands of adult leeches were examined by SEM. They are composed of unicellular glands arranged in grape patterns with spherical, ovoid, and pear shapes in various cell sizes; the cell bunches of gland cells were highly developed and interconnected to one another by tiny channels. A bigger canal that led to the jaws was created by combining channels from each bunch. Keywords: Annelida, Hirudo, Leeches, Limnatis, Salivary gland. INTRODUCTION Leeches are cylindrical, flattened ectoparasites that feed on blood or are carnivorous members of the phylum Annelida, class Clitellata; despite the numerous terrestrial and marine species, freshwater leeches predominate (Sawyer, 1986). Leeches are segmented, hermaphrodites, blood-feeding worms that can infect humans, pets, wildlife, and invertebrate species; these are distinguished by two distinct suckers, the anterior and posterior, and inside the front sucker is where the leech's mouth is situated (Daniel and Swayer, 1975; Ayhan et al., 2021). Jaws and velum are typically found in the buccal cavity of hematophagous species, which also have large mouths; having either one (monostichodont) or two (distichodont) rows of denticles, three muscular jaws are present. The animal may extract blood and lymph from wounds by cutting through the body surface of hosts with its calcified teeth and continue BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Iraq Natural History Research Center & Museum, University of Baghdad https://jnhm.uobaghdad.edu.iq/index.php/BINHM/Home Copyright © Bulletin of the Iraq Natural History Museum Online ISSN: 2311-9799-Print ISSN: 1017-8678 https://doi.org/10.26842/binhm.7.2023.17.3.0409 https://orcid.org/0009-0004-3118-0515 https://orcid.org/0000-0002-3338-3971 mailto:sherwan.ahmed@su.edu.krd https://creativecommons.org/licenses/by/4.0/ https://jnhm.uobaghdad.edu.iq/index.php/BINHM/Home 410 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Comparative ultrastructural study of the salivary sucking blood with the help of the secretion of their salivary glands (Fretter and Graham, 1976; Orevi et al., 2000). Bioactive chemicals found in the saliva of vampire leeches, such as Hirudo sp., enable the feeding and preservation of eaten blood as well as the possibility of significant medical advantages to the host. Due to their hematophagous nutrition habits, medicinal leeches have been used for centuries in bloodletting for treating numerous diseases (Hirudotherapy). By transmitting different bioactive compounds to their hosts, leeches have developed the capacity to regulate many mechanisms within their hosts (Joslin et al., 2017). Saliva is produced by single-celled salivary glands in the frontal region of the body of jawed medicinal leeches; these glands are positioned between the muscle fibers that link the jaws to the body wall. From the cell body to the jaw, the individual salivary cell sends a single duct, which terminates in a small aperture between the calcified denticles of the jaw (Wuttke et al., 1989). There are 6 species of medicinal leeches in the genus Hirudo (Linnaeus, 1758), involving Hirudo medicinalis Linnaeus, 1758 (European medicinal leech), which has been studied in detail but others do not get sufficient importance including Hirudo oreintalis (Bahmani et al., 2013; Saglam et al., 2020). Nasal leeches belong to the taxon identified as Limnatis Moquin-Tandon, 1827. Mammals, particularly humans, have been observed to have this genus' leeches invade their nasopharynxes (Almallah, 1968; Boye and Joshi, 1994). Only three species belonging to Limnatis: L. nilotica (Savigny, 1822), L. bacescui Manoleli, 1972, and L. paluda (Tennant, 1860) were identified (Sawyer, 1986). In spite of the fact that this species cannot puncture the dermis of humans and animals , it inflames and damages the oral or nasal mucosa by sucking blood (Bahmani et al., 2013). They typically adhere to the animal's buccal cavity or pulmonary tracts after ingesting infected water; the species in this genus are crucial for research in parasitology, veterinary science, and medicine (Arfuso et al., 2019). Among these three species, L. nilotica gets much investigation due to their dominant distributions (Utevsky et al., 2022). The purpose of the current study is to clarify the detailed structure of the two hematophagous leeches' salivary glands H. oreintalis and L. paluda which differ in their rote of blood feeding, moreover discuss the structure and appearance of their jaws which are related to their feeding mode also. MATERIALS AND METHODS Specimens' collection: During July and August of 2021, many water bodies in Erbil Province and its suburbs were searched for collection. Seventeen specimens of Hirudo orientalis (Utevsky & Trontelj, 2005) were observed in springs in the Hassan Bag Mountain (N 36° 43’ E 44° 38’) as mentioned by Alishah (2016), While fourteen specimens of Limnatis paluda (Tennent, 1859) were gained inside springs, streams, and small lakes in Debaga Township (N 411 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Bilal and Ahmed 35° 30’ E 43° 45’). Adult active leeches were hand-collected and placed in glass jars, covered with a smooth minute porous cloth to prevent escape. Leeches were kept alive in the laboratory and transferred to a glass aquarium of 30cm (W) x 27cm (H) size, filled with non- chlorinated water. The water was regularly maintained by replacing it every day. Specimens' identification: The adult leeches were anesthetized in 10% ethanol for about 5 min. Identification of the worms was done under an Olympus SM depending on their the following external characters; general shape of body, size of mouth, form of suckers, number and arrangement of eyespots (ocelli), papillae, sensillae, copulatory gland pore, the number of annuli per somite (segments), shape and location of male and female gonogpores (Sawyer, 1986; Schenkova ́ et al., 2021). For detecting their feeding organs including salivary glands, four specimens of each species were dissected and then cleaned with distilled water (Ayhan et al., 2021). Dissection started from anterior to the posterior part along the ventral side on paraffin wax blocks, exposing three rigid jaws and one dorsomedial and two ventrolateral salivary glands. The salivary gland cells have to be as clear as possible and visible, the area around them was cleared from cerebral ganglia, crop, overlying muscle, and connective tissues. Photographs of whole specimens were taken using digital camera adapted to the eye lense. SEM technique: Anesthetized leeches had their jaws and salivary glands dissected, after which they were fixed overnight at 25° c in 2.5 percentages of glutaraldehyde PH 7.2. After being cleaned 3 times with phosphate buffer solution for 20 minutes, the fixed tissues were subsequently dehydrated using alcohol at increasing concentrations (thirty, fifty, sixty, seventy, eighty, ninety, ninety-five, and hundred) percentages for each concentration in twenty minutes. Step-by-step , concentrated solutions were applied to the dehydrated tissues (EtOH 1:3, 1:1, 3:1)of acetone for 15 minutes per step, and then transferred to 100 % acetone for 30 minutes. Every specimen was dried in a hood for three days. Ultimately, drying specimens were placed on SEM stubs with both-sided tape, and the specimens were gold coated by DSR1 desk sputter coater in 200 Angstrom for 30 minutes, some samples were silver coated with DSR1 desk sputter coater in 250 angstroms for an hour (Kwak et al., 2021). Map (1): Map of Iraq presenting specimens' collection sites ( ). Hasan Bag Debaga 412 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Comparative ultrastructural study of the salivary Coated samples were viewed with QUANTUM 450 SEM in the Scientific Research Center, Soran University, Erbil, Iraq. RESULTS AND DISCUSSION Kingdom: Animalia Phylum: Annelida Class: Clitellata Order: Arhynchobdellida Family: Hirudinidae 1. Genus: Hirudo Linnaeus, 1758 Species: Hirudo orientalis (Utevsky & Trontelj, 2005) 2. Genus: Limnatis Moquin-Tandon, 1827 Species: Limnatis paluda (Tennent, 1859) 1. Jaws Hirudo orientalis: Jaws are located in a large preoral chamber occupies the anterior sucker, the posterior wall of this chamber is a transverse sheet of tissue known as the vellum, this sucker harbors a small mouth which is a triradiate opening in the center of the vellum (Pl. 1). Two symmetrical ventrolateral and single dorsomedial jaws have been seen, comprising an isosceles, triangle, bright white, smooth and rigid jaws (Pl. 2). The bladelike sharp jaws were seen bearing sharp teeth at the average 80 (range 70-91) per jaw. The jaws are trignathous, monosticodont coated with cuticles except for denticles (Pl. 3). Scant papillae are dispersed on both sides of each jaw (Pl. 3). Limnatis paluda: Anterior sucker occupies a long narrow cut or depression transverse sheet of tissue as three lobes are called median ventral furrow on the ventral surface of the oral sucker which is not observed in Hirudo (Pl. 1). Three jaws are situated in the oral cavity; an equilateral triangle is made by a symmetrical couple of ventrolateral jaws and single dorsomedial jaw, and smaller than those of Hirudo (Pl. 2). Jaws are gray with black specks that are circular and flexible, they fluctuate toward and away from each other and activated by muscle attached to their bases. Each jaw bearing a line of denticles with bumpy surfaces and flat tops at an average of 43 (range 37- 48) per jaw was seen on their edges (Pl. 3) There were abundant papillae detected on the jaws' double sides. In agreement data with Kovalenko and Utevsky (2015), Hirudo's jaws are stiff, milky white, and glow. It has a line of sharp, pyramid-shaped denticles that are positioned next to one another. The bite of Hirudo is a characteristic triradiate or Y-shape incision made by the three scalpel-like jaws (Sawyer, 1986). Arfuso et al. (2019) mentioned that the jaws of Limnatis nilotica, closely related to L. paula, seemed spherical, spongy, pale grey, and had more distinct knots. Disparity, Hirudo is an ectoparasite due to its pointed teeth and stiff jaws; it will puncture its host's dermis to feast on repletion itself when the opportunity presents itself because meals may not always be accessible (Orevi et al., 2000). 413 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Bilal and Ahmed On the jaw of H. medecinalis and H. orientalis, the size of the denticles and the quantity they are inversely associated with are observed, therefore the tiny denticles they have, the more teeth are there, while in H. verbana was quite different from them, with larger denticles and fewer numbers which allows an efficient piercing of the thick dermis of human and animals. It shows a representation of Limnatis jaws with papillae on both sides, a line of tiny denticles on the edge, and a salivary cell ductulus at the termination (Moquin-Tandon, 1827). While Orevi et al. (2000) did not detect openings in the teeth of L. nilotica but suggested that the papillae might be added to the discharge of salivary secretion of Hirudo's denticle pore; the opposite was found in this study, we detected apertures between the teeth of L. paluda (Pl. 3). cv cv 1 c m 1 c m Plate (1): Adult leeches, dorsal and ventral view; (A) H. orientalis, (B) L. paluda. Buccal cavity (cv). B A 414 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Comparative ultrastructural study of the salivary E B m o u t h H i r u d o o r i e n t a l i s : u 500.0 mµ C OC F OC A A s e c t e d m o u t h H ir u d o o ri e n t a li s : u n fi x e d D m o u t h H ir u d o o ri e n t a li s : u n fi x e d j a w , w it j sg sg j sg sg Plate (2): Jaws (j) and salivary glands (sg); (A, B, C) H. orientalis, (D, E, F) L. paluda. [OC: oral cavity; (B, C, E, F) SEM photographs]. 415 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Bilal and Ahmed 2. Salivary glands Hirudo orientalis: Three separated glands appear as clusters or grapes or strips that are extended from each jaw, spread around the cerebral ganglia, few anterior the crop, located approximately between segments V to XII, they are surrounded by muscles and connective tissues (Pl.4). Limnatis paluda: General appearance is the same as H. orientalis but it is located near position in segments (V - XI) (Pl. 4). Lemke et al. (2013) reported that the mature H. verbana conical-shaped salivary cells are positioned within segments V to IX, while those of H. medicinalis are observed in segments (V - XI) (Marshall and Lent, 1988). Plate (3): SEM photographs showing; Jaw (J), Denticles (d), Papillae (p) and salivary gland pores (gp) of (A, B, C) H. orientalis and (D, E, F) L. nilotica. 416 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Comparative ultrastructural study of the salivary A B C D F E gc gc d d ne ne Plate (4): SEM photographs representing; Salivary gland cells(gc), ducts(d) and network (ne), (A, B, C) H. oreintalis, (D, E, F) L. paluda. 417 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Bilal and Ahmed 3. Salivary gland cells Hirudo orientalis: When examined with SEM, thousands of single-celled and 3 of the detected glands were encased in a capsule of connective tissue (Pl.4). The individual gland has indentation cells that were connected to the ducts in a grape-like manner. The cells are arranged in grape-like patterns, spherical, ovoid, and pear-shaped with cell sizes 16 to 78 micrometers after, unconnected to each other. Sulci on the smooth outside surface of the cell were visible, and it appeared as a collection of different-sized cells with system channels interconnecting salivary gland cells to ducts in addition to the thousands of secretory cells. Three different duct configurations were seen in the salivary glands: thin ducts connecting the salivary gland cells and the salivary canal, bigger ducts that appear to travel toward the jaws, and fibrils ducts that appear as tiny capillaries on the outside of gland cells (Pl. 4). Limnatis paluda: Same appearance and arrangement as of Hirudo, but while they had different cell diameters of 13 to 65 micrometers (Pl. 4). Based on the current observational and multiple prior histological investigations (Van der Lande,1968; Mishra and Dev, 1976), it is evident that these jawed leeches' salivary cells are single cells and free cells of different measurements that are assembled in grape-like designs and are matching with other representations of leech salivary glands (Lemke et al., 2013; Saglam et al., 2020). Marshall and Lent (1988) and Lemke et al. (2013) observed that the somata of Hirudo medicinalis are typically circular or elliptical and have a dimension of thirty to two- hundred micrometers. A soma projects a solitary ductule, toward the base of each of the three jaws. However, the H. verbana salivary gland cells ranged in size from sixty to a hundred micrometers (Lemke et al., 2013); while described as nourished leeches have similar cells, they are significantly tiny and hardly distinguishable. Salivary glands of the enormous amazonian leech, Haementeria ghilianii, are ten times bigger than those of H. verbana and have a coarser outer layer (Walz et al., 1988). In comparison, the salivary gland of H. verbana has developed an interconnected network of fibers and saliva ducts (Wuttke et al., 1989). In their study, Saglam et al. (2020) mentioned the fact that mature H. verbana salivary glands presented as a collection of oval cells of various sizes, with a network of channels tying salivary cells to the ducts and three distinct duct morphologies. The salivary gland cells produce various bioactive compounds that makeup saliva, which is subsequently combined in the previously reported complicated channel system (Marshall and Lent, 1988). CONCLUSION The precise morphology of the jaws and salivary glands of Hirudo orientalis and Limnatis paluda were determined. Both species have in a grapes designed salivary glands that are extended from the jaws and surrounded by muscle fibers between crops and the body wall. Salivary gland cells are unicellular and vary in shape and size, the salivary gland of Hirudo in length is longer than Limnatis but in general, Limnatis cells are smaller than Hirudo. The jaws of Hirudo are firm, white, larger than Limnatis grey and soft and, both species are papillated but Limnatis papilla is more than Hirudo. Limnatis paluda comparatively has a 418 BULLETIN OF THE IRAQ NATURAL HISTORY MUSEUM Comparative ultrastructural study of the salivary small number of denticles so due to unable to pierce the skin, while Hirudo orientalis have larger and numerous denticles therefore are able to incision. CONFLICT OF INTEREST STATEMENT The results of the current study are part of the requirements of MSc thesis in Invertebrate Zoology, Department of Biology/College of Science-Salahaddin University/Erbil-Iraq for the first author. We declare that there is no conflict of interest between the authors. We confirm that all the pictures in the manuscript belong to us. We note, in this study, that there is no conflict of interest regarding the use of the laboratory of College of Science. LITERATURE CITED Alishah, R. J. 2016. Biological Study of Oriental Medicinal leech (Hirudinea; Annelida) Based on Morphological and Molecular Characterization in Kurdistan Region/ Iraq. M. Sc.Thesis. Salahaddin University-Erbil, Iraq, 90 pp. Almallah, Z. 1968. Internal hirudiniasis in man with Limnatis nilotica, in Iraq. The Journal of Parasitology, 54(3): 637-638. [Click here] Arfuso, F., Gaglio, G., Ferrara, M. C., Abbate, F., Giannetto, S. and Brianti, E. 2019. First record of infestation by nasal leeches, Limnatis nilotica (Hirudinida, Praobdellidae), from cattle in Italy. Journal of Veterinary Medicine Science, 81(10): 1419-1423. [CrossRef] Ayhan, H., Koçakoğlu, N. Ö. and Candan, S. 2021. 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(2023) 17 (3): 409-421. املاصة للدم دراسة مقارنة للتركيب الدقيق للغدد اللعابية إلثنين من ديدان العلق (Annelida, Clitellata, Arhynchobdellida) في العراق هدى صادق بالل و شيروان طيب احمد العراق ،اربيل ،نة، كلية العلوم، جامعة صالح الديقسم علوم الحيا 20/6/2023، تأريخ النشر: 26/2/2023القبول: ، تأريخ 26/11/2022تأريخ االستالم: الخالصة ين مننوعاملورفولوجية للفكين واألسنان وخاليا الغدد اللعابية ل سماتالدرست عائلة Hirudo orientalis (Utevsky & Trontelj, 2005) : املاصة للدمديدان العلق Hirudinidae وLimnatis paluda (Tennent 1859) عائلة Praobdellidaeستخدام أب s. at.eiro .H(. كانت فكوك MESاملاسح )( واملجهر اإللكتروني MSاملجهر املجسم ) رمادية وناعمة a. lo .oبيضاء وصلبة ، وتحمل أسنانا حادة ، بينما كانت فكوك . في صفوتحمل عددا أقل من األسنان الحادة مع حليمة وفيرة وكالهما أحادي ال ف من وهي تتأل ؛MESاللعابية للعلق البالغ بواسطة الدراسة الحالية، تم فحص الغدد الشكل و يةكمثر غدد وحيدة الخلية مرتبة في أنماط العنب بأشكال كروية وبيضاوية أو بأحجام مختلفة. ومجموعات الخاليا من خاليا الغدة متطورة للغاية ومترابطة مع بعضها البعض بواسطة قنوات صغيرة. ثم يتم إنشاء قناة أكبر تؤدي إلى الفكين من كل مجموعة.خالل الجمع بين القنوات من