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Descriptive Study of Some Osteological Parts of Rosy Stone Lapper (Garra rossica) from Mashkid Basin of Iran

Descriptive Study of Some Osteological Parts of Rosy Stone Lapper (Garra rossica) from Mashkid... Hindawi International Journal of Zoology Volume 2021, Article ID 5525109, 7 pages https://doi.org/10.1155/2021/5525109 Research Article Descriptive Study of Some Osteological Parts of Rosy Stone Lapper (Garra rossica) from Mashkid Basin of Iran Mazaher Zamani-Faradonbe and Yazdan Keivany Department of Natural Resources (Fisheries Division), Isfahan University of Technology, Isfahan 84156-83111, Iran Correspondence should be addressed to Mazaher Zamani-Faradonbe; m.zamanif68@gmail.com Received 28 January 2021; Revised 14 June 2021; Accepted 28 June 2021; Published 6 July 2021 Academic Editor: Joao Pedro Barreiros Copyright © 2021 Mazaher Zamani-Faradonbe and Yazdan Keivany. .is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Since osteological structures of fishes provide important biological and ecological information, studying these structures is valuable. On the other hand, due to lack of data on the osteology of stone lappers, the present study was conducted to provide detailed descriptive osteology of Garra rossica from Mashkid basin, southeastern Iran, comparing it with those of G. typhlops from the Bagh-e Loveh cave, Iran, G. rossica from Nahang River, Mashkid Basin, and G. persica from Zahak River, Sistan basin. For this purpose, 15 specimens of G. rossica were captured from Ladiz River, Mashkid Basin, using an electrofishing device, and fixed in 10% buffered formalin. .en, the specimens were cleared and stained with alcian blue and alizarin red for osteological in- vestigations. A detailed description of the osteological features of G. rossica was provided. Based on the results, several differences were observed between the four species. G. rossica can be distinguished from G. typhlops, G. persica, and G. rossica based on the shape of suspensorium and opercular series, pharyngobranchial bones, ventral and pectoral girdles, caudal, dorsal, and anal fins skeleton, and shape and number of infraorbital elements. in streams, rivers, pools, and lakes [9]. .ey are primarily 1. Introduction freshwater species but are also reported from brackish waters .e cyprinid genus Garra Hamilton 1822 has a wide geo- [1]. .is genus is characterized by small-to-moderate body size graphic distribution from Borneo, China, and southern Asia, and elongate and almost cylindrical body shape having a through the Middle East, Arabian Peninsula, and East Africa to rounded snout with an inferior and crescent-shaped mouth, a West Africa [1]. .ere are about 73 species in Garra [2], among horny lower jaw, usually fringed upper lip continuous with the which 14 species are recognized from Iran. Esmaeili et al. [3] snout, and a suctorial disc with a free posterior margin [2]. listed four species G. persica, G. rufa, G. variabilis, and Despite the introduction of modern techniques such as G. rossica [3]; recently, Sayyadzadeh et al. [4] reviewed the DNA sequencing and barcoding, osteology, due to its reliability, members of the genus in the Persian Gulf and Oman Sea basins still plays an important role in the systematic studies of fishes and recognized six epigean species, including G. barreimiae, and comprises a major percent of today’s works. Since osteo- G. longipinnis, G. persica, G. rossica, G. rufa, and G. variabilis, logical characteristics can provide valuable information in tax- and two subterranean species, including G. typhlops and onomy and phylogenetic relationships of fishes [10], the present G. widdowsoni, and described a new species from the region as study was conducted to provide detailed descriptive osteology of G. mondica. Mousavi-Sabet and Eagderi [5] described a new G. rossica from the Ladiz River, Mashkid Basin, Iran. species of G. lorestanensis. Esmaeili et al. [6] reviewed Garra genus species and introduced a new species, G. amirhosseini. 2. Material and Method Mousavi-Sabet et al. [7] described a new species of G. roseae. Moreover, Zamani-Faradonbe et al. [8] described Fifteen specimens of G. rossica were collected from Ladiz G. meymehensis and G. tiam. Species of the genus Garra inhabit River, Mashkid Basin (total length: 60.77± 5.53 mm, a wide range of substrates (muddy, sandy, and rocky bottoms) mean± SD) using the gill net and electrofishing device and 2 International Journal of Zoology square-shaped, and its posterior-lateral margin overlapped anesthetizing in 1% clove oil, then fixed in 10% buffered formalin, and transferred to the laboratory for further asymmetrically and laterally the dorsal part of the pterotic and epiotic bones. .e epiotic is oval-shaped with a posterior examinations. .e specimens were cleared and stained with alizarin red S and alcian blue according to the protocol of process (Figure 1); it is situated between the pterotic and Taylor and van Dyke [11] and Sone and Parenti [12] with supraoccipital bones. .e pterotic is a quarter-circle in shape some modifications for osteological examination. .e (Figure 1) and its posterior-lateral part is well-developed and cleared and stained specimens were studied using a ste- probably fused to the dermopterotic. .e sphenotic bears a reomicroscope (Leybold Didactic GmbH model) and their lateral process that connects the middle process of the skeletal elements were dissected and scanned by a scanner frontal; this bone is ventrally attached to the prootic and (HP Scanjet 3770) equipped with a glycerol bath. Drawing posteriodorsally to the pterotic (Figure 1). .e two prootics of the specimens was performed using CorelDraw X7 are connected to each other ventrally and to the para- sphenoid dorsally by a descending process. .is bone has software. .e terminology of skeletal elements follows Howes [13] and Rojo [14]. .e detailed osteological fea- two pores on its anterior part. .e occipital region is composed of the supraoccipital, tures of Garra typhlops from the Tigris basin were provided by Jalili and Eagderi [15], G. rossica from Nahang River, exoccipital, and basioccipital. .e supraoccipital is pentagon Mashkid Basin, by Saemi-Komsari et al. [16], and G. persica in shape and has a blade-shaped crest; its lateral part is from Zahak River, Sistan Basin, by Zamani-Faradonbe and connected to the epiotic. .e exoccipital bears a large ventral Keivany [17]. foramen on its middle concave part. In the dorsal part of the basioccipital, there are a pointed pharyngeal process and a concaved masticatory plate pointing laterally. .e pharyn- 3. Results geal process has a dorsal fossa and a ventromedial ridge .e ethmoid region of the neurocranium is flat and con- (Figure 1). .e upper jaw is made up of the paired maxilla, pre- tains the kinethmoid, preethmoid-I, lateral ethmoid, supraethmoid, vomer, and nasal bones (Figure 1). .e maxilla, and unpaired kinethmoid. .e two maxillae are located at the dorsal side of the premaxilla; the anterior part supraethmoid is broad and has two vertical and horizontal sections; the vertical section of this bone is located on the of the maxillae is wider than the posterior part. A notch on the lateral edge of the maxillae is marked. .e premaxilla is dorsal part of the vomer and the anterior part of the parasphenoid. .e horizontal section bears two small an- wide, L-shaped, and articulated with the maxillae and terior processes and a shallow middle depression with dentary and the kinethmoid bone is situated between the two cartilaginous lateral margins (Figure 1). .e posterior part maxillae (Figure 2(a)). of the vomer is pointed and overlapped with the anterior .e lower jaw is composed of three bones, including the part of the parasphenoid and its anterior part has a dentary, articular and retroarticular. .e dentary is L-sha- V-shaped notch. .e anterior part of the vomer is thicker ped, and its anterior edge is flat. .e coronoid process situated on the dorsal middle part of the dentary is oriented than its posterior part. .e ventral face of the vomer is smooth. .e preethmoid-I bones are small and semicir- posteriorly. .e middle part of the articular is wide and its posterior part bears an articulatory facet. .e triangular- cular in shape and are present in the anterior-lateral edge of the vomer (Figure 1). .e lateral ethmoid is located as a shaped retroarticular is a small bone situated under the wall between the ethmoid and orbital regions; the lateral posterior part of the articular; the posterior part of the part of the lateral-ethmoid bears two anterior and posterior retroarticular is connected to the interopercle via the ret- processes. A cylindrical kinethmoid exists between the roarticular-interopercle ligament. A small and elongated maxillary bones (Figure 1). coronomeckelian is observed on the medial face of the ar- .e orbital region comprises the frontals, parasphenoid, ticular (Figure 2(a)). ptersphenoids, orbitosphenoids, and circumorbital series. .e suspensorium series is formed of the hyo- .e frontal is a large bony element of the skull roof with a mandibular, ectopterygoid, endopterygoid, metapterygoid, symplectic, quadrate, and palatine (Figure 2(a)). .e hyo- serrated anterior edge and bent ventrally; it bears a mid- lateral pointed process. .e supraorbital canal is enclosed by mandibular bone is almost triangular in shape: its dorsal part is wider and posterior part bears two protuberances; the the lateral margin of the frontal. .e two orbitosphenoids are fused via their ventral process that is also connected to ventral part of the hyomandibular is connected to the the parasphenoid (Figure 1). .e ptersphenoid is concaved interhyal. .is bone is articulated to the posterior part of the in shape with two ventral processes for connecting to the neurocranium with two hyomandibular articulatory con- parasphenoid and bears two pores. .e ptersphenoid is dyles and to the opercle by opercular articulatory condyle. dorsally attached to the frontal, anteriorly to the orbitos- .e ectopterygoid, endopterygoid, metapterygoid, sym- phenoid, and posteriorly to the sphenotic. .e anterior half plectic, and quadrate form a bony complex connecting to the anterior part of the neurocranium via the palatine. A long of the parasphenoid is wider and is of typical shape with a serrated anterior rim and its posterior half has a triangular symplectic is enclosed by the metapterygoid posteriorly, by the quadrate anteriorly and by the preopercle posteriorly. structure that its posterior margin bifurcates via a deep groove and has some pores in its middle part (Figure 1). .e anterior part of the palatine bears three processes and slightly deep depression for connecting to the vomer and .e otic region includes the parietal, epiotic, sphenotic, pterotic, and prootic bones. .e parietal bone is almost preethmoid-I. International Journal of Zoology 3 Sp Pa Pto Ptt Pro So Epo Pts Opi Ps Orb Exo Nas Pe Le Pr-Pp Vo Bo Se Fr Soc 1mm 1mm (a) (b) Figure 1: (a) Dorsal and (b) ventral views of the neurocranium in G. rossica. Bo: basioccipital; Epo: epiotic; Exo: exoccipital; Fr: frontal; Nas: nasal; Orb: orbitosphenoid; Pa: parietal; Pe: preethmoid-I; Ptt: posttemporal; Pr-Pp: posterior pharyngeal process; Pro: prootic; Ps: parasphenoid; Pts: pterosphenoid; Pto: pterotic; Se: supraethmoid; So: supraorbital; Soc: supraoccipital; Sp: sphenotic; Vo: vomer. Sj Io 2–4 Hy P Mtp Ect End Lacrimal Mx Op Sym Pmx Sop Keth Ar Dn Ra 1mm BSR DHY Pop BHY Iop EHY CHY 1mm UHY (a) (b) Figure 2: (a) .e suspensorium, opercular series, and hyoid arch and (b) circumorbital series in G. rossica. Ar: articular; BBR: basibranchial; BHY: basihyal; BSR: branchiostegal; CBR: ceratobranchial; CHY: ceratohyale; DHY: dorsal hypohyal; EBR: epibranchial; Ect: ectopterygoid; End: endopterygoid; EHY: epihyal; HBR: hypobranchial; Hy: hyomandibulare; Io 2-4: infraorbital 2-4; Iop: interopercle; Keth: kinethmoid; Mx: maxillary; Mtp: metapterygoid; Op: opercle; P palatine; PBR: pharyngobranchial; Pmx: premaxillary; Pop: preopercle; Q quadrate; Ra: retroarticular; Sj: spine and socket joint; Sop: subopercle; Sym: symplectic; VHY: ventral hypohyal; UHY: urohyal. .e opercular series consists of four bones including the sections. .e posterior margin of its horizontal section is opercle, preopercle, subopercle, and interopercle bones. .e pointed and its middle part is wider. In addition, the an- opercle bone that is the largest element of this series has an terior part of its horizontal section is branched. .e pos- opercular process in anterodorsal part and this bone has a terior part of the ceratohyal is wider than its anterior part; socket joint that is connected to the hyomandibular. An its anterior part is branched and connected to the dorsal L-shaped preopercle presents in the anterior side of the and ventral hypohyals. .e dorsal and ventral hypohyals are fused. .e basihyal is T-shaped, situated between the opercle and ventral side of the hyomandibular; its vertical part is longer than that of its wider horizontal part. .e hypoyals (Figure 2(a)). ventral part of the preopercle overlaps the dorsal part of the In the circumorbital series, the number of the infraor- interopercle. .e subopercle is long, and its anterior part is bital bones was the same in the studied specimens. .ere are broad (Figure 2(a)). four infraorbital and one supraorbital elements. .e first .e hyoid arch consists of the unpaired basihyal and circumorbital, i.e., lacryamal, is the largest element of this urohyal and the paired epihyals, hypohyals, and ceratohyals series. .e supraorbital is oval-shaped and located at the and three pairs of branchiostegal rays. .e urohyal is the lateral side of the frontal. .e suborbital canal is enclosed by largest element that has two vertical and horizontal the infraorbital bony elements (Figure 2(b)). 4 International Journal of Zoology .e branchial apparatus includes five types of bones, Zahak River, Sistan Basin, and G. typhlops, a closely related including five pairs of the ceratobranchials, four pairs of the species resulting from an evolutionary adaptation to a sub- epibranchials, three pairs of the hypobranchial and two pairs terranean system. Most members of Garra genus are found in of the pharyngobranchial, and three unpaired basibranchial. mountain streams and flowing waters [2], whereas G. typhlops .e fifth ceratobranchial is crescent in shape with a dental. inhabits subterranean habitats with stagnant waters [2]. .ere are three rows of pharyngeal teeth with a dental .ere are differences in the suspensorium and opercular formula of 2.4.5-5.4.2 (Figure 3). series, pharyngobranchial bones, ventral and pectoral gir- .e dorsal fin bears one unbranched ray and nine dles, caudal, dorsal, and anal fins skeleton, infraorbital series branched rays, eight pterygiophores and one stay bone elements, and branchial apparatus between G. rossica of this (Figure 4(a)). .e first pterygiophore is the largest, U-shaped study and G. typhlops provided by Jalili and Eagderi, [15], (bifurcates), and supports unbranched ray and first G. rossica from Nahang River provided by Saemi-Komsari branched ray. .e first pterygiophore is next to the 22th and et al. [16], G. persica from Zahak River, Sistan Basin, studied 23th preural. A tetrangular stay bone supports the last by Zamani-Faradonbe and Keivany [17]. All bones in sus- branched ray. .e anal fine originates at 12th preural. .is pensorium and opercular series in G. rossica are narrower fin has two unbranched and seven branched rays that were and longer than G. typhlops. .e pharyngobranchial bones supported by six pterygiophores and one small stay bone in G. rossica are wide, while these bones are small in (Figure 4(b)). G. typhlops. Garra rossica has four infraorbital and one .e caudal skeleton consists of the last centrum with the supraorbital elements, whereas these bones in G. typhlops epural, parhypural, pleurostyle, uroneural, and six hypurals had six infraorbital elements and in G. rossica from Nahang bones (Figure 5(c)). .e pleurostyle is fused to the last River had five. centrum (urostyle). .e neural arch of the second centrum is .e basipterygium in G. rossica is bifurcate and its consumptive in some specimens. .e first hypural is the posterior process is rounded, whereas in G. typhlops, the largest one and attached to the parhyporal. .e epural is a basipterygium is trifurcate and its posterior process is long bone positioning at the dorsal part of the neural arch of pointed. Garra rossica bears narrow and long cleithrum and the first vertebra. .ere are 31–35 vertebra, including 15–17 coracoid bones in the pectoral girdle, whereas G. typhlops cranial and 16–18 caudal centra. bears broad and wide bones. .e pectoral girdle consists of the cleithrum, coracoid, .e caudal skeleton in G. rossica has 6 hypural plates, mesocoracoid, scapula, posttemporal, and radials long epural, and narrow and a long neural spin, whereas (Figure 6(a)). .e ventral part of the cleithrum is wider with G. typhlops bears 7 hypural plates, a short epural, and neural a lateral process. .is bone bears two wide horizontal and spin. Furthermore, differences were observed between the vertical portions; its ventral part bears an anteromedial osteological structures of the median unpaired fins of downward process connecting to the anterior part of the G. rossica and G. typhlops. .e dorsal fin in G. rossica has one coracoid. .e posterior part of the coracoid is wider than its unbranched ray and nine branched rays and eight pter- anterior part and bears an ascending process for connecting ygiophores, whereas G. typhlops bears three unbranched and to the mesocoracoid. .e posttemporal is a small bone that seven branched rays and nine pterygiophores; G. rossica connects the pectoral girdle to the pterotic (Figure 1(b)). .e from Nahang River had three unbranched ray and nine medial part of the coracoid is bent ventrally and has a small branched rays and eight pterygiophores and G. persica had pore. A semicircular scapula is located between cleithrum two to three unbranched rays and eight to ten branched rays and coracoid bones; this bone bears a large foramen and is and nine pterygiophores. articulated to the first unbranched ray. .e ventral part of .e anal fin in G. rossica has two unbranched and seven the mesocoracoid is V-shaped and attached the coracoid to branched rays and is supported by six pterygiophores and the cleithrum; the dorsal part of the mesocoracoid is one small stay bone, while this fin in G. typhlops had two broadened and attached to the medial surface of the unbranched and six branched rays, seven pterygiophores cleithrum. .e pectoral fin bears four radials; the lateral and one stay bone, G. rossica from Nahang River had two radial is the thickest and three others are long and flat. unbranched and six branched rays and is supported by six Pelvic girdle includes the paired basipterygium, meta- pterygiophores and one small stay bone and one unbranched pterygium, lateral pterygium, and radials (Figure 6(b)). .e and one branched rays that were supported by six pter- anterior part of the basipterygium bone is bifurcate; this ygiophores and one small stay bone in G. persica. bone has a posterior long and a midlateral processes. .e two .e branchial apparatus in G. rossica has five pairs of the L-shaped lateral pterygiums are located at the posterolateral ceratobranchials while G. rossica from Nahang River and side of the pelvic bone. .ere are two paired radial and one G. persica had four pairs; G. persica had three pairs of paired metapterygium in the pelvic girdle. pharyngobranchial, while G. rossica in this study has two pairs; there are three rows of the pharyngeal teeth with a formula of 2.4.5-5.4.2 in G. rossica, whereas the dental 4. Discussion formula was 3.5.6-6.5.3 in G. rossica from Nahang River. .e present study provides a detailed skeletal description of .e osteological features of G. rossica can reflect changes rosy stone lapper (G. rossica) from Ladiz River, Mashkid in its composing structures with a new adaptation to mountain streams that can be described as evolutionary Basin. Rosy stone lapper showed differences compared to G. rossica from Nahang River, Mashkid Basin, G. persica from novelties that gradually accumulated as modified anatomical International Journal of Zoology 5 CBR EBR BBR HBR PBR 1mm Figure 3: Branchial apparatus of G. rossica. BBR: basibranchial; CBR: ceratobranchial; EBR: epibranchial; HBR: hypobranchial; PBR: pharyngobranchial. DFR APT Ppt Sty DFS Mtp Dpt Sty Dpt Mpt Ppt 1mm AFS Dpt 1mm AFR (a) (b) Figure 4: Lateral view of the (a) dorsal and (b) Anal fins of G. rossica. AFR: anal fin ray; AFS: anal fin spine; APT: anal pterigiophor; DFS: dorsal fin spine; DFR: dorsal fin ray; DPt: dorsal pterigiophor; Dpt: distal pterygiophore; Mpt: medial pterygiophore; Ppt: proximal pterygiophore; Sty: stay. C7 C19 EPU NeS NeS C25 Rna Pls NeA NeS NeA PeC Ce Ce AnC Zyg BaP HeC Hp1–6 PIR 1mm HeS Ph 1mm 1mm HeS Uro (a) (b) (c) Figure 5: Lateral view of the (a) and (b) centrum 7, 19 and 25, (c) Caudal skeleton of G. rossica. Abbreviations: AnC: antepenultimate centrum; BaP: basapophysis; Ce: centrum; EPU: epural; HeC: hemal canal; HeS: hemal spine; Hp 1–6: hypural plates 1–6; NeA: neural arch; NeS: neural spine; PeC: penultimat centrum; Ph: parhypurale; PlR: pleural rib; Pls: pleurostyle; Rna: rudimentary neural arch; Uro: urostyle; Zyg: zygopophysis. 6 International Journal of Zoology BPG Mco MDP LPG SCA CLT COR 1mm MPG 1mm POP (a) (b) Figure 6: (a) Internal view of the pectoral girdle, and (b) ventral view of the pelvic girdle of G. rossica. BPG: basipterygium; CLT: cleithrum; COR: coracoid; LPG: lateral pterygium; Mco: mesocoracoid; MDP: medial process; MPG: metapterygium; POP: posterior process; R: radials; SCA: scapula. structures as phenotypic plasticity during about 5 million description of a new species: a morpho-molecular approach (Teleostei: cyprinidae),” Iranian Journal of Ichthyology, vol. 3, years since it is divergent from their common ancestor with no. 2, pp. 82–121, 2016. the other species in Garra genus. [7] H. Mousavi-Sabet, M. Saemi-Komsari, I. Doadrio, and J. Freyhof, “Garra roseae, a new species from the Makran Data Availability region in southern Iran (Teleostei: cyprinidae),” Zootaxa, All the data used for this study were obtained in the “De- vol. 4671, no. 2, pp. 223–239, 2019. [8] M. Zamani-Faradonbe, Y. Keivany, S. Dorafshan, and partment of Natural Resources (Fisheries Division), Isfahan E. Zhang, “Two new species of Garra (Teleostei: cyprinidae) University of Technology” and are available for everyone. from western Iran,” Ichthyological Exploration of Freshwaters, no. 1137, pp. 1–22, 2021. Conflicts of Interest [9] M. Zamani-Faradonbe and Y. Keivany, “Biodiversity and .e authors declare that they have no conflicts of interest. distribution of Garra spp. (teleostei: cyprinidae) in Iran,” Iranian Journal of Fisheries Sciences, vol. 20, 2021. [10] Y. Keivany and J. S. Nelson, “Phylogenetic relationships of References sticklebacks (Gasterosteidae), with emphasis on ninespine [1] A. Getahun, “.e american museum of natural history,” Ph. sticklebacks (Pungitius spp.),” Behaviour, vol. 141, no. 11, D. thesis, Department of Anthropology, University of Colo- pp. 1485–1497, 2004. rado, Boulder, CO, USA, 1999. [11] W. R. Taylor and G. C. Van Dyke, “Revised procedures for [2] B. W. Coad, “Freshwater fishes of Iran,” 2020, http://www. staining and clearing small fishes and other vertebrates for briancoad.com. bone and cartilage study,” Cybium, vol. 9, pp. 107–119, 1985. [3] H. R. Esmaeili, B. W. Coad, A. Gholamifard, N. Nazari, and [12] J. Sone and L. R. Parenti, “Clearing and staining whole fish A. Teimory, “Annotated shecklist of the freshwater fishes of specimens for simultaneous demonstration of Bone, cartilage, Iran,” Zoosystematica Rossica, vol. 19, no. 2, pp. 361–386, 2010. and nerves,” Copeia, vol. 1995, pp. 114–118, 1995. [4] G. Sayyadzadeh, H. R. Esmaeili, and J. Freyhof, “Garra [13] G. J. Howes, “Anatomy and evolution of the jaws in the mondica, a new species from the Mond River drainage with semiplotine carps with a review of the genus cyprinion heckel, remarks on the genus Garra from the Persian Gulf basin in 1843 (teleostei: cyprinidae) bulletin of the British museum Iran (Teleostei: cyprinidae),” Zootaxa, vol. 4048, no. 1, (natural history),” Zoology, vol. 42, no. 4, pp. 299–335, 1982. pp. 075–089, 2015. [14] A. L. Rojo, Dictionary of Evolutionary Fish Osteology, CRC [5] H. Mousavi-Sabet and S. Eagderi, “Garra lorestanensis, a new Press, Boca Raton, FL, USA, 1991. cave fish from the Tigris river drainage with remarks on the [15] P. Jalili and S. Eagderi, “Osteological description of Iran cave subterranean fishes in Iran (Teleostei: cyprinidae),” FishTaxa, barb (Iranocypris typhlops Bruun & Kaiser, 1944),” University vol. 1, no. 1, pp. 45–54, 2016. Journal of Zoology, Rajshahi University, vol. 33, pp. 01–07, [6] H. R. Esmaeili, G. Sayyadzadeh, B. W. Coad, and S. Eagderi, “Review of the genus Garra hamilton, 1822 in Iran with 2014. International Journal of Zoology 7 [16] M. Saemi-Komsari, H. Mousavi-Sabet, M. Sattari, S. Eagderi, S. Vatandoust, and I. Doadrio, “Descriptive osteology of Garra rossica (nikolskii, 1900),” FishTaxa, vol. 16, pp. 19–38, 2020. [17] M. Zamani-Faradonbe and Y. Keivany, “Descriptive osteology of Persian stone lapper (Garra persica) from Sistan basin,” Journal of Animal Researches, vol. 30, no. 3, pp. 346–357, 2018. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png International Journal of Zoology Hindawi Publishing Corporation

Descriptive Study of Some Osteological Parts of Rosy Stone Lapper (Garra rossica) from Mashkid Basin of Iran

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Hindawi International Journal of Zoology Volume 2021, Article ID 5525109, 7 pages https://doi.org/10.1155/2021/5525109 Research Article Descriptive Study of Some Osteological Parts of Rosy Stone Lapper (Garra rossica) from Mashkid Basin of Iran Mazaher Zamani-Faradonbe and Yazdan Keivany Department of Natural Resources (Fisheries Division), Isfahan University of Technology, Isfahan 84156-83111, Iran Correspondence should be addressed to Mazaher Zamani-Faradonbe; m.zamanif68@gmail.com Received 28 January 2021; Revised 14 June 2021; Accepted 28 June 2021; Published 6 July 2021 Academic Editor: Joao Pedro Barreiros Copyright © 2021 Mazaher Zamani-Faradonbe and Yazdan Keivany. .is is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Since osteological structures of fishes provide important biological and ecological information, studying these structures is valuable. On the other hand, due to lack of data on the osteology of stone lappers, the present study was conducted to provide detailed descriptive osteology of Garra rossica from Mashkid basin, southeastern Iran, comparing it with those of G. typhlops from the Bagh-e Loveh cave, Iran, G. rossica from Nahang River, Mashkid Basin, and G. persica from Zahak River, Sistan basin. For this purpose, 15 specimens of G. rossica were captured from Ladiz River, Mashkid Basin, using an electrofishing device, and fixed in 10% buffered formalin. .en, the specimens were cleared and stained with alcian blue and alizarin red for osteological in- vestigations. A detailed description of the osteological features of G. rossica was provided. Based on the results, several differences were observed between the four species. G. rossica can be distinguished from G. typhlops, G. persica, and G. rossica based on the shape of suspensorium and opercular series, pharyngobranchial bones, ventral and pectoral girdles, caudal, dorsal, and anal fins skeleton, and shape and number of infraorbital elements. in streams, rivers, pools, and lakes [9]. .ey are primarily 1. Introduction freshwater species but are also reported from brackish waters .e cyprinid genus Garra Hamilton 1822 has a wide geo- [1]. .is genus is characterized by small-to-moderate body size graphic distribution from Borneo, China, and southern Asia, and elongate and almost cylindrical body shape having a through the Middle East, Arabian Peninsula, and East Africa to rounded snout with an inferior and crescent-shaped mouth, a West Africa [1]. .ere are about 73 species in Garra [2], among horny lower jaw, usually fringed upper lip continuous with the which 14 species are recognized from Iran. Esmaeili et al. [3] snout, and a suctorial disc with a free posterior margin [2]. listed four species G. persica, G. rufa, G. variabilis, and Despite the introduction of modern techniques such as G. rossica [3]; recently, Sayyadzadeh et al. [4] reviewed the DNA sequencing and barcoding, osteology, due to its reliability, members of the genus in the Persian Gulf and Oman Sea basins still plays an important role in the systematic studies of fishes and recognized six epigean species, including G. barreimiae, and comprises a major percent of today’s works. Since osteo- G. longipinnis, G. persica, G. rossica, G. rufa, and G. variabilis, logical characteristics can provide valuable information in tax- and two subterranean species, including G. typhlops and onomy and phylogenetic relationships of fishes [10], the present G. widdowsoni, and described a new species from the region as study was conducted to provide detailed descriptive osteology of G. mondica. Mousavi-Sabet and Eagderi [5] described a new G. rossica from the Ladiz River, Mashkid Basin, Iran. species of G. lorestanensis. Esmaeili et al. [6] reviewed Garra genus species and introduced a new species, G. amirhosseini. 2. Material and Method Mousavi-Sabet et al. [7] described a new species of G. roseae. Moreover, Zamani-Faradonbe et al. [8] described Fifteen specimens of G. rossica were collected from Ladiz G. meymehensis and G. tiam. Species of the genus Garra inhabit River, Mashkid Basin (total length: 60.77± 5.53 mm, a wide range of substrates (muddy, sandy, and rocky bottoms) mean± SD) using the gill net and electrofishing device and 2 International Journal of Zoology square-shaped, and its posterior-lateral margin overlapped anesthetizing in 1% clove oil, then fixed in 10% buffered formalin, and transferred to the laboratory for further asymmetrically and laterally the dorsal part of the pterotic and epiotic bones. .e epiotic is oval-shaped with a posterior examinations. .e specimens were cleared and stained with alizarin red S and alcian blue according to the protocol of process (Figure 1); it is situated between the pterotic and Taylor and van Dyke [11] and Sone and Parenti [12] with supraoccipital bones. .e pterotic is a quarter-circle in shape some modifications for osteological examination. .e (Figure 1) and its posterior-lateral part is well-developed and cleared and stained specimens were studied using a ste- probably fused to the dermopterotic. .e sphenotic bears a reomicroscope (Leybold Didactic GmbH model) and their lateral process that connects the middle process of the skeletal elements were dissected and scanned by a scanner frontal; this bone is ventrally attached to the prootic and (HP Scanjet 3770) equipped with a glycerol bath. Drawing posteriodorsally to the pterotic (Figure 1). .e two prootics of the specimens was performed using CorelDraw X7 are connected to each other ventrally and to the para- sphenoid dorsally by a descending process. .is bone has software. .e terminology of skeletal elements follows Howes [13] and Rojo [14]. .e detailed osteological fea- two pores on its anterior part. .e occipital region is composed of the supraoccipital, tures of Garra typhlops from the Tigris basin were provided by Jalili and Eagderi [15], G. rossica from Nahang River, exoccipital, and basioccipital. .e supraoccipital is pentagon Mashkid Basin, by Saemi-Komsari et al. [16], and G. persica in shape and has a blade-shaped crest; its lateral part is from Zahak River, Sistan Basin, by Zamani-Faradonbe and connected to the epiotic. .e exoccipital bears a large ventral Keivany [17]. foramen on its middle concave part. In the dorsal part of the basioccipital, there are a pointed pharyngeal process and a concaved masticatory plate pointing laterally. .e pharyn- 3. Results geal process has a dorsal fossa and a ventromedial ridge .e ethmoid region of the neurocranium is flat and con- (Figure 1). .e upper jaw is made up of the paired maxilla, pre- tains the kinethmoid, preethmoid-I, lateral ethmoid, supraethmoid, vomer, and nasal bones (Figure 1). .e maxilla, and unpaired kinethmoid. .e two maxillae are located at the dorsal side of the premaxilla; the anterior part supraethmoid is broad and has two vertical and horizontal sections; the vertical section of this bone is located on the of the maxillae is wider than the posterior part. A notch on the lateral edge of the maxillae is marked. .e premaxilla is dorsal part of the vomer and the anterior part of the parasphenoid. .e horizontal section bears two small an- wide, L-shaped, and articulated with the maxillae and terior processes and a shallow middle depression with dentary and the kinethmoid bone is situated between the two cartilaginous lateral margins (Figure 1). .e posterior part maxillae (Figure 2(a)). of the vomer is pointed and overlapped with the anterior .e lower jaw is composed of three bones, including the part of the parasphenoid and its anterior part has a dentary, articular and retroarticular. .e dentary is L-sha- V-shaped notch. .e anterior part of the vomer is thicker ped, and its anterior edge is flat. .e coronoid process situated on the dorsal middle part of the dentary is oriented than its posterior part. .e ventral face of the vomer is smooth. .e preethmoid-I bones are small and semicir- posteriorly. .e middle part of the articular is wide and its posterior part bears an articulatory facet. .e triangular- cular in shape and are present in the anterior-lateral edge of the vomer (Figure 1). .e lateral ethmoid is located as a shaped retroarticular is a small bone situated under the wall between the ethmoid and orbital regions; the lateral posterior part of the articular; the posterior part of the part of the lateral-ethmoid bears two anterior and posterior retroarticular is connected to the interopercle via the ret- processes. A cylindrical kinethmoid exists between the roarticular-interopercle ligament. A small and elongated maxillary bones (Figure 1). coronomeckelian is observed on the medial face of the ar- .e orbital region comprises the frontals, parasphenoid, ticular (Figure 2(a)). ptersphenoids, orbitosphenoids, and circumorbital series. .e suspensorium series is formed of the hyo- .e frontal is a large bony element of the skull roof with a mandibular, ectopterygoid, endopterygoid, metapterygoid, symplectic, quadrate, and palatine (Figure 2(a)). .e hyo- serrated anterior edge and bent ventrally; it bears a mid- lateral pointed process. .e supraorbital canal is enclosed by mandibular bone is almost triangular in shape: its dorsal part is wider and posterior part bears two protuberances; the the lateral margin of the frontal. .e two orbitosphenoids are fused via their ventral process that is also connected to ventral part of the hyomandibular is connected to the the parasphenoid (Figure 1). .e ptersphenoid is concaved interhyal. .is bone is articulated to the posterior part of the in shape with two ventral processes for connecting to the neurocranium with two hyomandibular articulatory con- parasphenoid and bears two pores. .e ptersphenoid is dyles and to the opercle by opercular articulatory condyle. dorsally attached to the frontal, anteriorly to the orbitos- .e ectopterygoid, endopterygoid, metapterygoid, sym- phenoid, and posteriorly to the sphenotic. .e anterior half plectic, and quadrate form a bony complex connecting to the anterior part of the neurocranium via the palatine. A long of the parasphenoid is wider and is of typical shape with a serrated anterior rim and its posterior half has a triangular symplectic is enclosed by the metapterygoid posteriorly, by the quadrate anteriorly and by the preopercle posteriorly. structure that its posterior margin bifurcates via a deep groove and has some pores in its middle part (Figure 1). .e anterior part of the palatine bears three processes and slightly deep depression for connecting to the vomer and .e otic region includes the parietal, epiotic, sphenotic, pterotic, and prootic bones. .e parietal bone is almost preethmoid-I. International Journal of Zoology 3 Sp Pa Pto Ptt Pro So Epo Pts Opi Ps Orb Exo Nas Pe Le Pr-Pp Vo Bo Se Fr Soc 1mm 1mm (a) (b) Figure 1: (a) Dorsal and (b) ventral views of the neurocranium in G. rossica. Bo: basioccipital; Epo: epiotic; Exo: exoccipital; Fr: frontal; Nas: nasal; Orb: orbitosphenoid; Pa: parietal; Pe: preethmoid-I; Ptt: posttemporal; Pr-Pp: posterior pharyngeal process; Pro: prootic; Ps: parasphenoid; Pts: pterosphenoid; Pto: pterotic; Se: supraethmoid; So: supraorbital; Soc: supraoccipital; Sp: sphenotic; Vo: vomer. Sj Io 2–4 Hy P Mtp Ect End Lacrimal Mx Op Sym Pmx Sop Keth Ar Dn Ra 1mm BSR DHY Pop BHY Iop EHY CHY 1mm UHY (a) (b) Figure 2: (a) .e suspensorium, opercular series, and hyoid arch and (b) circumorbital series in G. rossica. Ar: articular; BBR: basibranchial; BHY: basihyal; BSR: branchiostegal; CBR: ceratobranchial; CHY: ceratohyale; DHY: dorsal hypohyal; EBR: epibranchial; Ect: ectopterygoid; End: endopterygoid; EHY: epihyal; HBR: hypobranchial; Hy: hyomandibulare; Io 2-4: infraorbital 2-4; Iop: interopercle; Keth: kinethmoid; Mx: maxillary; Mtp: metapterygoid; Op: opercle; P palatine; PBR: pharyngobranchial; Pmx: premaxillary; Pop: preopercle; Q quadrate; Ra: retroarticular; Sj: spine and socket joint; Sop: subopercle; Sym: symplectic; VHY: ventral hypohyal; UHY: urohyal. .e opercular series consists of four bones including the sections. .e posterior margin of its horizontal section is opercle, preopercle, subopercle, and interopercle bones. .e pointed and its middle part is wider. In addition, the an- opercle bone that is the largest element of this series has an terior part of its horizontal section is branched. .e pos- opercular process in anterodorsal part and this bone has a terior part of the ceratohyal is wider than its anterior part; socket joint that is connected to the hyomandibular. An its anterior part is branched and connected to the dorsal L-shaped preopercle presents in the anterior side of the and ventral hypohyals. .e dorsal and ventral hypohyals are fused. .e basihyal is T-shaped, situated between the opercle and ventral side of the hyomandibular; its vertical part is longer than that of its wider horizontal part. .e hypoyals (Figure 2(a)). ventral part of the preopercle overlaps the dorsal part of the In the circumorbital series, the number of the infraor- interopercle. .e subopercle is long, and its anterior part is bital bones was the same in the studied specimens. .ere are broad (Figure 2(a)). four infraorbital and one supraorbital elements. .e first .e hyoid arch consists of the unpaired basihyal and circumorbital, i.e., lacryamal, is the largest element of this urohyal and the paired epihyals, hypohyals, and ceratohyals series. .e supraorbital is oval-shaped and located at the and three pairs of branchiostegal rays. .e urohyal is the lateral side of the frontal. .e suborbital canal is enclosed by largest element that has two vertical and horizontal the infraorbital bony elements (Figure 2(b)). 4 International Journal of Zoology .e branchial apparatus includes five types of bones, Zahak River, Sistan Basin, and G. typhlops, a closely related including five pairs of the ceratobranchials, four pairs of the species resulting from an evolutionary adaptation to a sub- epibranchials, three pairs of the hypobranchial and two pairs terranean system. Most members of Garra genus are found in of the pharyngobranchial, and three unpaired basibranchial. mountain streams and flowing waters [2], whereas G. typhlops .e fifth ceratobranchial is crescent in shape with a dental. inhabits subterranean habitats with stagnant waters [2]. .ere are three rows of pharyngeal teeth with a dental .ere are differences in the suspensorium and opercular formula of 2.4.5-5.4.2 (Figure 3). series, pharyngobranchial bones, ventral and pectoral gir- .e dorsal fin bears one unbranched ray and nine dles, caudal, dorsal, and anal fins skeleton, infraorbital series branched rays, eight pterygiophores and one stay bone elements, and branchial apparatus between G. rossica of this (Figure 4(a)). .e first pterygiophore is the largest, U-shaped study and G. typhlops provided by Jalili and Eagderi, [15], (bifurcates), and supports unbranched ray and first G. rossica from Nahang River provided by Saemi-Komsari branched ray. .e first pterygiophore is next to the 22th and et al. [16], G. persica from Zahak River, Sistan Basin, studied 23th preural. A tetrangular stay bone supports the last by Zamani-Faradonbe and Keivany [17]. All bones in sus- branched ray. .e anal fine originates at 12th preural. .is pensorium and opercular series in G. rossica are narrower fin has two unbranched and seven branched rays that were and longer than G. typhlops. .e pharyngobranchial bones supported by six pterygiophores and one small stay bone in G. rossica are wide, while these bones are small in (Figure 4(b)). G. typhlops. Garra rossica has four infraorbital and one .e caudal skeleton consists of the last centrum with the supraorbital elements, whereas these bones in G. typhlops epural, parhypural, pleurostyle, uroneural, and six hypurals had six infraorbital elements and in G. rossica from Nahang bones (Figure 5(c)). .e pleurostyle is fused to the last River had five. centrum (urostyle). .e neural arch of the second centrum is .e basipterygium in G. rossica is bifurcate and its consumptive in some specimens. .e first hypural is the posterior process is rounded, whereas in G. typhlops, the largest one and attached to the parhyporal. .e epural is a basipterygium is trifurcate and its posterior process is long bone positioning at the dorsal part of the neural arch of pointed. Garra rossica bears narrow and long cleithrum and the first vertebra. .ere are 31–35 vertebra, including 15–17 coracoid bones in the pectoral girdle, whereas G. typhlops cranial and 16–18 caudal centra. bears broad and wide bones. .e pectoral girdle consists of the cleithrum, coracoid, .e caudal skeleton in G. rossica has 6 hypural plates, mesocoracoid, scapula, posttemporal, and radials long epural, and narrow and a long neural spin, whereas (Figure 6(a)). .e ventral part of the cleithrum is wider with G. typhlops bears 7 hypural plates, a short epural, and neural a lateral process. .is bone bears two wide horizontal and spin. Furthermore, differences were observed between the vertical portions; its ventral part bears an anteromedial osteological structures of the median unpaired fins of downward process connecting to the anterior part of the G. rossica and G. typhlops. .e dorsal fin in G. rossica has one coracoid. .e posterior part of the coracoid is wider than its unbranched ray and nine branched rays and eight pter- anterior part and bears an ascending process for connecting ygiophores, whereas G. typhlops bears three unbranched and to the mesocoracoid. .e posttemporal is a small bone that seven branched rays and nine pterygiophores; G. rossica connects the pectoral girdle to the pterotic (Figure 1(b)). .e from Nahang River had three unbranched ray and nine medial part of the coracoid is bent ventrally and has a small branched rays and eight pterygiophores and G. persica had pore. A semicircular scapula is located between cleithrum two to three unbranched rays and eight to ten branched rays and coracoid bones; this bone bears a large foramen and is and nine pterygiophores. articulated to the first unbranched ray. .e ventral part of .e anal fin in G. rossica has two unbranched and seven the mesocoracoid is V-shaped and attached the coracoid to branched rays and is supported by six pterygiophores and the cleithrum; the dorsal part of the mesocoracoid is one small stay bone, while this fin in G. typhlops had two broadened and attached to the medial surface of the unbranched and six branched rays, seven pterygiophores cleithrum. .e pectoral fin bears four radials; the lateral and one stay bone, G. rossica from Nahang River had two radial is the thickest and three others are long and flat. unbranched and six branched rays and is supported by six Pelvic girdle includes the paired basipterygium, meta- pterygiophores and one small stay bone and one unbranched pterygium, lateral pterygium, and radials (Figure 6(b)). .e and one branched rays that were supported by six pter- anterior part of the basipterygium bone is bifurcate; this ygiophores and one small stay bone in G. persica. bone has a posterior long and a midlateral processes. .e two .e branchial apparatus in G. rossica has five pairs of the L-shaped lateral pterygiums are located at the posterolateral ceratobranchials while G. rossica from Nahang River and side of the pelvic bone. .ere are two paired radial and one G. persica had four pairs; G. persica had three pairs of paired metapterygium in the pelvic girdle. pharyngobranchial, while G. rossica in this study has two pairs; there are three rows of the pharyngeal teeth with a formula of 2.4.5-5.4.2 in G. rossica, whereas the dental 4. Discussion formula was 3.5.6-6.5.3 in G. rossica from Nahang River. .e present study provides a detailed skeletal description of .e osteological features of G. rossica can reflect changes rosy stone lapper (G. rossica) from Ladiz River, Mashkid in its composing structures with a new adaptation to mountain streams that can be described as evolutionary Basin. Rosy stone lapper showed differences compared to G. rossica from Nahang River, Mashkid Basin, G. persica from novelties that gradually accumulated as modified anatomical International Journal of Zoology 5 CBR EBR BBR HBR PBR 1mm Figure 3: Branchial apparatus of G. rossica. BBR: basibranchial; CBR: ceratobranchial; EBR: epibranchial; HBR: hypobranchial; PBR: pharyngobranchial. DFR APT Ppt Sty DFS Mtp Dpt Sty Dpt Mpt Ppt 1mm AFS Dpt 1mm AFR (a) (b) Figure 4: Lateral view of the (a) dorsal and (b) Anal fins of G. rossica. AFR: anal fin ray; AFS: anal fin spine; APT: anal pterigiophor; DFS: dorsal fin spine; DFR: dorsal fin ray; DPt: dorsal pterigiophor; Dpt: distal pterygiophore; Mpt: medial pterygiophore; Ppt: proximal pterygiophore; Sty: stay. C7 C19 EPU NeS NeS C25 Rna Pls NeA NeS NeA PeC Ce Ce AnC Zyg BaP HeC Hp1–6 PIR 1mm HeS Ph 1mm 1mm HeS Uro (a) (b) (c) Figure 5: Lateral view of the (a) and (b) centrum 7, 19 and 25, (c) Caudal skeleton of G. rossica. Abbreviations: AnC: antepenultimate centrum; BaP: basapophysis; Ce: centrum; EPU: epural; HeC: hemal canal; HeS: hemal spine; Hp 1–6: hypural plates 1–6; NeA: neural arch; NeS: neural spine; PeC: penultimat centrum; Ph: parhypurale; PlR: pleural rib; Pls: pleurostyle; Rna: rudimentary neural arch; Uro: urostyle; Zyg: zygopophysis. 6 International Journal of Zoology BPG Mco MDP LPG SCA CLT COR 1mm MPG 1mm POP (a) (b) Figure 6: (a) Internal view of the pectoral girdle, and (b) ventral view of the pelvic girdle of G. rossica. BPG: basipterygium; CLT: cleithrum; COR: coracoid; LPG: lateral pterygium; Mco: mesocoracoid; MDP: medial process; MPG: metapterygium; POP: posterior process; R: radials; SCA: scapula. structures as phenotypic plasticity during about 5 million description of a new species: a morpho-molecular approach (Teleostei: cyprinidae),” Iranian Journal of Ichthyology, vol. 3, years since it is divergent from their common ancestor with no. 2, pp. 82–121, 2016. the other species in Garra genus. [7] H. Mousavi-Sabet, M. Saemi-Komsari, I. Doadrio, and J. Freyhof, “Garra roseae, a new species from the Makran Data Availability region in southern Iran (Teleostei: cyprinidae),” Zootaxa, All the data used for this study were obtained in the “De- vol. 4671, no. 2, pp. 223–239, 2019. [8] M. Zamani-Faradonbe, Y. Keivany, S. Dorafshan, and partment of Natural Resources (Fisheries Division), Isfahan E. 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Journal

International Journal of ZoologyHindawi Publishing Corporation

Published: Jul 6, 2021

References