103
Department of Natural Resources (Fisheries Division), Isfahan University of Technology, Isfahan, 84156-83111, Iran.
*Email: [email protected]
Abstract: Osteological plasticity of Garra rufa (Heckel, 1843) populations inhabiting 29 rivers in four basins were described and compared. The skeletal elements of G. rufa specimens were stained, cleared and photographed. Studied populations have 12 differences in the head skeleton, four in jaw elements, three in suspensorium, two in opercular series, two in circumorbital series, four in hyoid arches, one in the branchial apparatus, three in Weberian apparatus, three in dorsal fin skeleton, one in anal fin skeleton, one in pectoral fin girdle, three in ventral fin skeleton and two in caudal fin skeleton. These differences could be results of evolutionary adaptations to new habitat conditions and can be used in comparative and phylogenetic studies.
Keywords: Cyprinidae, Osteology, Plasticity, Fish skeleton.
Citation: Zamani-Faradonbe, M.; Keivany, Y. & Dorafshan, S. 2020. Osteological plasticity of Garra rufa populations in Iranian inland waters (Teleostei: Cyprinidae). Iranian Journal of Ichthyology 7(1): 103-119.
Introduction
The genus Garra Hamilton, 1822, with 126 valid species is one of the most diverse genera of the subfamily Labeoninae (Cypriniformes, Cyprinidae) and widely distributed from East Asia to the middle East and Africa (Sayyadzadeh et al. 2015; Mousavi- Sabet & Eagderi 2016; Mousavi-Sabet et al. 2016;
Froese & Pauly 2018; Esmaeili et al. 2018; Çiçeket al. 2018). After the first revision of the genus Garra by Menon (1964), recent revision based on morphological characters, squamation pattern, molecular approach, resulted in describing more than ten species from Iranian freshwaters (Esmaeili et al.
2016) and 16 described and four undescribed species from the Middle East (Hashemzadeh Segherloo et al.
2017). Thus, more studies are needed to validate and clarify the status of Garra spp. in Iranian freshwaters.
Osteological studies provide important and valid data for description and classification of fish species and understanding biological features of fishes such as feeding, respiration and swimming (Helfman et al.
2009; Nasri et al. 2016; Jalili et al. 2015a;
Keivany 2014a, b, c, 2017a, b). In addition, the skeletal structures contain much biological information that researchers use to distinguish species type, age, sex, size, and even environmental conditions of their habitats (Helfman et al. 2009;
Jalili & Eagderi 2014). Therefore, the skeletal variation in Garra during evolution present an adaptation to new ecosystem conditions. In this regard, relationships between populations of G. rufa from different habitats provides a proper case to understand the skeletal changes to adapt to different habitats. Since there is no information on the osteology of most populations of Garra, therefore, this study was conducted to provide a detailed and comparative osteological description for G. rufa populations living in different rivers and basins of Iran to understand the evolution of osteological features. The results of this study will provide basic osteological data for phylogenetic study of Iranian cyprinid species, particularly the members of the
genus Garra as well as help in better understanding of their biological features.
Materials and Methods
Specimens of G. rufa from 29 sites in four Iranian inland basins (Table 1) were collected using a seine net and electrofishing device, fixed in 10% buffered formalin after anesthetizing in 1% clove oil and transferred to laboratory for further experiments.
These specimens were cleared and stained following Taylor & van Dyke (1985) and Sone & Parenti (1995) protocols. The cleared and stained specimens were studied using a stereomicroscope (SMP-120 model) and their skeletal elements were dissected and drawings of the bones were done using CorelDraw
X7 software. The terminology of skeletal elements is based on Rojo (1990) and Helfman et al. (2009).
Results
Syncranium: In the neurocranium, the ethmoid, vomer, parasphenoid, supraoccipital and basioccipital were present; connection state between the orbitosphenoid with pterosphenoid, connections among lateral-ethmoid, vomer, orbitosphenoid and parasphenoid were different between the studied populations (Fig. 1). Connection between the orbitosphenoid and pterosphenoid could be complete (Fig. 2A) (Kheirabad, Shiv, Shour-Bushehr, Aks-e- Rostam (b), Maroun, Davod-e arab, Sartang, Bazoft, Zoherh, Shour-Karun, Siahgav, Seimareh, Shavour,
Mazaii (b) 26°50'31.1" 57°25'11.4"
Aks Rostam (a) 28°57'12" 54°22'48"
Aks Rostam (b) 28°57'12" 54°22'48"
Bushehr Ahram 28°52'22" 51°19'37"
Zohreh-Kheirabad 30°24'51.6" 50°19'57.4"
Shahpour 29°35'10" 51°26'15"
Shiv 30º18'32" 51º14'00"
Mond 28°18'09" 52°26'51"
Bahoush 28°55'44" 51°26'17"
Shour-Bushehr 28°33'00" 52°22'04"
Tigris Alvand 34º30'28" 45º34'33"
Maroun-Jarahi 31°00'40" 49°44'51.3"
Davoud-Arab 34º16'13" 45º48'18"
Doiraj 32º35'36" 47º24'11"
Sartang 33º39'16" 45º49'32"
Bazoft 32°12'40.5" 50°02'8.7"
Zoherh 30°19'04" 50°13'58"
Shour-Karun 32°00'3.8" 49°06'40.7"
Karun 33º28'22" 49º03'52"
Siahgav-Karkheh 32º46'28" 47º43'18"
Seimareh-Karkheh 33º11'51" 47º23'11"
Shavour-Karkheh 32°10'54.9" 48°14'27.7"
Kashkan-Karkheh 33º22'31" 47º57'49"
Kangir 33º53'53" 45º42'13"
Kouh Gari 34º46'41" 45º47'01"
Semirum- Karun 31°09'37" 51°26'09"
Chaghalvandi-Karkheh 33º41'27" 48º29'42"
Fars Pirbano-Maharloo 29°31'09" 54°27'57"
Kashkan, Kangir, Kouh gari and Semirum populations) or incomplete (Fig. 2B) (Ahram, Shahpour, Mond, Bahoush, Pirbano-Maharloo, Mazaii (a,b), Aks-e-Rostam (a), Alvand, Doiraj, Karun and Chaghalvandi populations).
The lateral-ethmoid connection to the vomer, orbitosphenoid and parasphenoid is complex. This connection among these four elements could be complete (Fig. 2C) (Kheirabad, Shiv, Shour- Bushehr, Aks-e-Rostam (b), Maroun, Davod-e arab, Sartang, Bazoft, Zoherh, Shour-Karun, Siahgav, Seimareh, Shavour, Kashkan, Kangir, Kouh gari and Semirum populations), the lateral-ethmoid only connected to vomer and parasphenoid (Fig. 2D) (Ahram, Shahpour, Mond, Bahoush, Pirbano, Mazaii (a, b), Aks-e-Rostam (a) and Alvand populations), or the lateral-ethmoid connection to vomer and parasphenoid is complete or incomplete to orbitosphenoid (Fig. 2E) (Doiraj, Karun and Chaghalvandi populations).
The anterior part of the vomer is fully concaved (Fig. 3A) (Ahram, Maroun, Davod-e arab, Doiraj, Zoherh, Kangir and Semirum populations) or slightly concaved (Fig. 3B) (Mazaii (a,b), Aks-e-Rostam (a,b), Kheirabad, Shahpour, Shiv, Mond, Bahoush,
Shour-Bushehr, Alvand, Sartang, Bazoft, Shour- Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Kouh gari, Chaghalvandi and Pirbano populations). In Mazaii (a, b), Shiv, Bahoush, Alvand, Doiraj, Seimareh, Kashkan, Kangir, Kouh gari and Chaghalvandi populations, the posterior part of the vomer is pointed (Fig. 3C), but in Ahram, Kheirabad, Shahpour, Mond, Shour-Bushehr, Pirbano, Aks-e-Rostam (a,b), Maroun, Davod-e arab, Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Shavour and Semirum populations, the posterior part of the vomer is blunt (Fig. 3A, B, D).
The lateral margin of the vomer in Shour-Bushehr, Mazaii (a), Bahoush, Sartang, Zoherh, Siahgav, Seimareh, Kashkan, Kangir, Kouh gari and Semirum populations bears a distinct depression (Fig. 3D), but a shallow depression is found in those of Ahram, Kheirabad, Shahpour, Shiv, Mond, Pirbano, Mazaii (b), Aks-e-Rostam (a,b), Alvand, Maroun, Davod-e arab, Doiraj, Bazoft, Shour-Karun, Karun, Shapour and Chaghalvandi (Fig. 3A,B,C).
The anterior edge of the ethmoid bears a deep fossa in Kheirabad, Shiv, Aks-e-Rostam (b), Davod- e Arab, Zoherh, Kashkan, Seimareh and Karun populations (Fig. 3E), but a shallow one is found in Fig.1. Dorsal (left), ventral (right) and lateral view of the neurocranium in Garra rufa populations in iranian rivers:
1: supraethmoid, 2: lateral ethmoid (parethmoid), 3 & 4: supraorbital, 5: frontal, 6: parietal, 7: sphenotic, 8: pterotic, 9:
epiotic, 10: supraoccipital, 11: exooccipital, 12: basioccipital, 13: vomer, 14: preethmoid, 15: orbitosphenoid, 16: pterosphenoid, 17: parasphenoid, 18: prootic, 19: ethmoid.
Ahram, Mond, Shour-Karun, Bahoush, Shour- Bushehr, Pirbano, Mazaii (a,b), Aks-e-Rostam (a), Alvand, Maroun, Doiraj, Sartang, Bazoft, Shour, Siahgav, Kangir, Semirum, Chaghalvandi, Shapour and Kouhgari populations (Fig. 3F).
In some specimens, a distinct bulge-like process or crest is seen on the vomer. In lateral view, the crest edge is angled in Ahram, Kheirabad, Shiv, Mond, Bahoush, Pirbano, Mazaii (a,b), Alvand, Maroun, Davodarab, Doiraj, Sartang, Shour-Karun, Siahgav, Seimareh, Kashkan and Semirum populations (Fig.
3A), but straight in Shahpour, Shour-Bushehr, Aks- e-Rostam (a,b), Bazoft, Zoherh, Karun, Kangir, Kouh gari and Chaghalvandi populations (Fig. 3B).
The crest in Shiv, Mazaii (b), Shour-Karun, Maroun, Doiraj, Sartang, Shour and Shavour populations is long (Fig. 3C), but short in Ahram, Kheirabad, Shahpour, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a), Aks-e-Rostam (a,b), Alvand, Davod-e arab, Bazoft, Zoherh, Karun, Siahgav, Seimareh, Kashkan, Kangir, Kouh gari, Semirum and Chaghalvandi populations (Fig. 3D).
Distal end of the pharyngeal process of the basioccipital has remarkable morphological variation in shape between the studied populations. It has a pointed or triangular end in Shiv, Mond, Bahoush, Karun, Shavour, Kashkan and Kangir populations
(Fig. 4A), rounded or convex in Kheirabad, Mazaii (b), Shour-Karun, Seimareh and Chaghalvandi populations (Fig. 4B) and concave in Bazoft, Ahram, Shahpour, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a), Aks-e-Rostam (a,b), Alvand, Maroun, Davod-e arab, Sartang, Zoherh, Siahgav, Kouh gari and Semirum populations (Fig. 4C).
The ventromedial ridge of the pharyngeal process of the basioccipital in Ahram, Shahpour, Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (b), Aks- e-Rostam (b), Alvand, Maroun, Davod-e arab, Doiraj, Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Fig.2. Ventral view of the neurocranium in Garra rufa populations in Iranian Rivers.
Fig.3. Ventral view of the vomer in Garra rufa populations.
Kangir, Semirum and Chaghalvandi populations is long (Fig. 4D), but in those of Kheirabad, Mazaii (a), Aks-e-Rostam (a) and Kouh gari populations is short (Fig. 4E).
The ventral masticatory plate of the basioccipital in Ahram, Kheirabad, Shahpour, Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a,b), Aks-e-Rostam (a), Alvand, Davod-e arab, Maroun, Doiraj, Sartang, Bazoft, Shour-Karun, Seimareh, Shavour, Kangir, Kouh gari and Semirum populations is large (Fig. 5A,B,C), but in Aks-e- Rostam (b), Zoherh, Karun, Siahgav, Kashkan and Chaghalvandi populations is small (Fig. 5D,E).
In some populations, broadened anterior portion of the parasphenoides is distinctive (Ahram, Shahpour, Shiv, Pirbano, Mazaii (a,b), Aks-e- Rostam (a,b), Alvand, Davod-e arab, Zoherh, Karun, Seimareh, Shavour and Semirum (Fig. 6A), but in Kheirabad, Maroun, Mond, Bahoush, Shour-
Bushehr, Doiraj, Sartang, Bazoft, Shour-Karun, Siahgav, Kashkan, Kangir, Kouhgari and Chaghalvandi populations is narrow (Fig. 6B).
Width and height of the antero-dorsal process of premaxillae in Ahram, Shour-Bushehr, Pirbano, Mazaii (b), Aks-e-Rostam (a), Alvand, Davod-e arab, Doiraj, Shapour, Maroun, Kashkan and Chaghalvandi populations is small (Fig. 7A), but in Kheirabad, Shahpour, Shiv, Mond, Bahoush, Mazaii (a), Aks-e-Rostam (b), Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Seimareh, Kangir, Kouhgari and Semirum populations, the width and height of antero-dorsal process is remarkable larger (Fig. 7B,C).
The antero-dorsal portion of the maxilla could be elevated and extended or not, the medial portion of the maxilla may bear a marked or slightly broadened ventral edge, antero-ventral process of the maxilla could be present and remarkable or absent. In Shiv, Fig.4. Lateral (A and B) and dorsal (C and D) view of the supraoccipital crest in Garra rufa populations
Fig.5. Ventral (A, B, C) and lateral (D and E) views of the basioccipital in Garra rufa populations. 1: ventral masticatory plate, 2: ventromedial ridge, 3: posterior pharyngeal process.
Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a,b), Alvand, Davod-e arab, Doiraj, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Kashkan, Kouh gari, Semirum and Chaghalvandi populations, the antero- dorsal portion of the maxilla is elevated and extended (Fig. 8A) and in Ahram, Kheirabad, Shahpour, Aks- e-Rostam (a, b), Sartang, Seimareh, Shavour and Kangir populations is small (Fig. 8B, C, D).
The ventral edge of medial portion of the maxilla in Ahram, Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a), Aks-e-Rostam (a,b), Alvand, Davod-e arab, Doiraj, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Kashkan, Kouh gari, Semirum and Chaghalvandi populations is remarkable (Fig. 8D) but in Kheirabad, Shahpour, Mazaii (b), Sartang, Seimareh, Shavour and Kangir populations is unremarkable (Fig. 8A,B,C).
A remarkable antero-ventral process in Shahpour,
Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (b), Aks-e-Rostam (b), Alvand, Davod-e arab, Doiraj, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Seimareh, Kashkan, Kouhgari, Semirum and Chaghalvandi populations is present (Fig. 8A,C), Fig.6. Ventral view of the parasphenoides; 13: Vomer, 17: parasphenoides
Fig.7. Lateral view of premaxillae in Garra rufa populations.
Fig.8. Lateral (A-D) and ventral views of the Jaw maxillae (E) in Garra rufa populations. 1: Dentary, 2: angular, 3:
retroarticular.
Fig.9. Internal view of the suspensorium and opercular series. 1: Palatine, 2: endopterygoid, 3:
metapterygoid, 4: ectopterygoid, 5: quadrate, 6:
symplectic, 7: hyomandibular, 8: opercular, 9:
subopercle, 10: preopercle, 11: interopercle.
but in Ahram, Kheirabad, Mazaii (a), Aks-e-Rostam (a), Sartang and Kangir populations is absent or insignificant (Fig. 8 C,D). The shape of lower jaw elements as dentary, angular and retroarticular in all populations are almost similar (Fig. 8E).
The suspensorium has seven and opercular series four elements (Fig. 9) and those elements are different among populations in shape of the endopterygoid, notch in the quadrate, anterior margin of the hyomandibular, the preopercle and dorsal edge of the opercle. The endopterygoid in Kheirabad, Shiv, Pirbano, Mazaii (b), Aks-e-Rostam (a,b), Doiraj, Zoherh, Shour-Karun, Karun, Seimareh, Shavour, Kheirabad, Kangir, Kouh gari and Semirum populations is triangular (Fig. 10A), but in those of Mond, Bahoush, Ahram, Mazaii (a), Shour-Bushehr, Alvand, Shahpour, Davod-e arab, Sartang, Bazoft, Siahgav, Kashkan and Chaghalvandi populations is belt-like or rectangular (Fig. 10B).
The junction point between the quadrate and the symplectic have a notch with different depth; in Ahram, Kheirabad, Mond, Bahoush, Shour-Bushehr, Mazaii (a), Davod-e arab, Zoherh, Siahgav, Seimareh, Kouh gari and Chaghalvandi populations the notch is deep (Fig. 11A), but in Shahpour, Shiv, Pirbano, Mazaii (b), Aks-e-Rostam (a,b), Alvand, Doiraj, Sartang, Bazoft, Shour-Karun, Karun, Shavour, Kashkan, Kangir and Semirum populations is shallow (Fig. 11B).
The anterior margin of the hyomandibular is round or triangular in G. rufa populations; in Mazaii (a),
Aks-e-Rostam (a,b), Ahram, Shahpour, Shiv, Mond, Bahoush, Shour-Bushehr, Alvand, Davod-e arab, Doiraj, Shour-Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Kangir, Kouh gari, Semirum and Pirbano populations anterior margin is slight or round (Fig. 11C) and in Mazaii (b), Kheirabad, Sartang, Bazoft, Chaghalvandi and Zoherh populations is triangular (Fig. 11D).
The specimens of Shahpour, Shiv, Bahoush, Shour-Bushehr, Pirbano, Mazaii (b), Aks-e-Rostam (b), Alvand, Sartang, Shour-Karun, Siahgav, Shavour, Kashkan, Semirum and Chaghalvandi bear a straight dorsal edge of the opercle (Fig. 11E), but the dorsal edge of the opercle in Ahram, Kheirabad, Mond, Mazaii (a), Aks-e-Rostam (a), Alvand, Doiraj, Bazoft, Zoherh, Seimareh, Kangir, Kouh gari, Davod-e Arab and Karun is concave (Fig. 11F).
The preopercle, which approximates a right- angled triangle, is thick and low, and its height is greater than its width in Ahram, Kheirabad, Shahpour, Shiv, Mond, Bahoush, Pirbano, Mazaii (a,b), Aks-e-Rostam (a,b), Alvand, Davod-e arab, Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Shavour, Kashkan, Kangir and Chaghalvandi populations (Fig. 11G) but thin and less in Shour-Bushehr, Doiraj, Seimareh, Kouhgari and Semirum populations (Fig. 11H).
The lachrymal (Fig. 12A), in Ahram, Kheirabad, Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii (a), Aks-e-Rostam (a,b), Alvand, Davod-e arab, Doiraj, Sartang, Bazoft, Zoherh, Shour-Karun, Fig.10. Lateral view of the endopterygoid (2), metapterygoid (3) and Ectopterygoid (3) in suspensorium.
Karun, Siahgav, Seimareh, Shavour, Kashkan, Kouhgari, Semirum and Chaghalvandi population is elongate (Fig. 12B), but in Shahpour, Mazaii (b) and Kangir populations is square (Fig. 12C). Also, the second infraorbital in Ahram, Kheirabad, Shiv, Mond, Bahoush, Shour-Bushehr, Pirbano, Mazaii
(a), Aks-e-Rostam (a), Alvand, Davod-e arab, Doiraj, Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Kouh gari, Semirum and Chaghalvandi populations is square (Fig. 12D), but in Shahpour, Mazaii (b), Aks-e- Rostam (b) and Kangir populations is elongate Fig.11. Lateral view of the quadrate (A and B), hyomandibular (C and D), Operculum (E and F) and preopercle (G and H) in Garra rufa.
Fig.12. Internal view of the circumorbitals (a); 1: lachrymal (B and C) 2: infraorbital 2, 3: infraorbitals 2-5.
(Fig.12E).
Hyoid and Branchial arches: Among the hyoid arch elements, the urohyal is different in shape in the lateral view of the vertical plate and dorsal view of the horizontal plate between the populations (Fig.
13). The posterior margin of the vertical plate of the urohyal in Ahram, Shahpour, Shiv, Mond, Shour- Bushehr, Mazaii (a,b), Aks-e-Rostam (b), Alvand, Sartang, Zoherh, Siahgav, Seimareh, Kashkan, Kangir, Kouh gari, Semirum and Chaghalvandi populations is distinctly concave (Fig. 14A), but in Kheirabad, Bahoush, Pirbano, Aks-e-Rostam (a), Davod-e arab, Doiraj, Bazoft, Shour-Karun, Karun and Shavour populations is truncate or slightly concave (Fig. 14B).
The posterior margin of the horizontal part of the urohyal in dorsal view in Ahram, Kheirabad, Shahpour, Shiv, Mazaii (a), Aks-e-Rostam (a), Alvand, Doiraj, Bazoft, Zoherh, Karun, Seimareh, Kangir and Semirum populations is slight (Fig.
15A,D), in Mond, Shour-Bushehr, Pirbano, Mazaii (b), Davod-e arab, Sartang, Siahgav, Shavour,
Kouhgari and Chaghalvandi populations (Fig. 15B), is highly notch (V-shaped), but in Bahoush, Aks-e- Rostam (b), Shour-Karun and Kashkan populations is convex (Fig. 15C).
The posterior free angle of the vertical plate of the urohyal in dorsal view in Shiv, Mond, Siahgav, Seimareh, Chaghalvandi, Pirbano, Zoherh, Kangir and Karun populations is simple (Fig. 15C,D), but in Mazaii (a,b), Aks-e-Rostam (a,b), Ahram, Kheirabad, Shahpour, Bahoush, Shour-Bushehr, Alvand, Davod-e arab, Doiraj, Sartang, Bazoft, Shour-Karun, Shavour, Kashkan, Kouhgari and Semirum populations is bifurcated (Fig. 15A,B).
The posterior margin of the vertical plate of the urohyal in lateral view is truncate (Bahoush, Maroun, Davod-e arab, Doiraj, Bazoft, Shour-Karun, Karun, Shavour, Pirbano, Kheirabad and Aks-e-Rostam (a) populations (Fig.16A), or concaved (Mazaii (b), Ahram, Shahpour, Shiv, Mond, Shour-Bushehr, Alvand, Sartang, Siahgav, Seimareh, Kashkan, Kangir, Kouh gari, Semirum, Chaghalvandi, Zoherh, Mazaii (a) and Aks-e-Rostam (b) populations) (Fig.
Fig.13. Dorsal view of the hyoid arches (A) in Garra rufa. 1: Basihyal, 2: Dorsal Hypohyal, 3: Ventral Hypohyal, 4: Anterior Ceratohyal, 5: Posterior Ceratohyal, 6: Interhyal, 7: Branchiostegals 1-3, 8:
Urohyal.
Fig.14. Lateral view of the urohyal in Garra rufa populations.
Fig.15. Dorsal view of the urohyal in Garra rufa populations.
Fig.16. Lateral view the posterior margin of the vertical plate in Garra rufa populations.
16B).
There are differences among populations in numbers of the basibranchials, but other branchial apparatus elements are similar. There are three basibranchials in Aks-e-Rostam (b), Shour-Karun, populations (Fig. 17A), but four in Mazaii (a,b), Ahram, Kheirabad, Mond, Bahoush, Alvand, Maroun, Doiraj, Sartang, Bazoft, Seimareh, Shavour, Kashkan, Kangir, Kouh gari, Semirum, Chaghalvandi, Pirbano, Zoherh, Shahpour, Shiv, Shour-Bushehr, Davod-e arab, Karun, Siahgav, Aks- e-Rostam (a) populations (Fig. 17B).
Vertebral columns: The supporting base for Weberian apparatus is the three first vertebras and their related bones (Fig. 18A). Populations of G. rufa are different in shape and size in some of these elements. The height of the neural spine in Mazaii (b), Aks-e-Rostam (a, b), Shahpour, Bahoush, Davod-e arab, Doiraj, Sartang, Bazoft, Shour-Karun, Seimareh, Kouh gari, Chaghalvandi and Zoherh populations is equal with the height of supraneural (Fig. 18A), in Kheirabad and Shiv populations is higher than the upper supraneural (Fig. 18C) and is lower in Mazaii (a), Ahram, Mond, Alvand, Maroun, Shavour, Kashkan, Kangir, Semirum, Pirbano, Shour-Bushehr, Karun and Siahgav populations (Fig.
18B).
The anterior margin of the upper supraneural in Mazaii (a,b), Aks-e-Rostam (a), Ahram, Shahpour, Alvand, Maroun, Doiraj, Shour-Karun, Karun,
Siahgav, Kashkan, Kangir, Kouh gari, Semirum, Pirbano and Zoherh populations is round (Fig.
18A,C), but angular in Aks-e-Rostam (b), Kheirabad, Mond, Bahoush, Sartang, Bazoft, Seimareh, Shavour, Chaghalvandi, Shiv, Shour-Bushehr and Davod-e arab populations (Fig. 18B).
The space between the two supraneurals in the Weberian apparatus in Mazaii (a), Aks-e-Rostam (b), Ahram, Shiv, Mond, Bahoush, Shour-Bushehr, Alvand, Davod-e arab, Bazoft, Karun, Siahgav, Seimareh, Shavour, Kashkan and Chaghalvandi populations is distinct (Fig. 18B), but in Mazaii (b), Aks-e-Rostam (a), Kheirabad, Maroun, Doiraj, Sartang, Shour-Karun, Kangir, Semirum, Pirbano, Zoherh, Shahpour and Kouh gari populations is Fig.17. Ventral view of the branchial apparatus in Garra rufa populations. 1: basibranchial, 2: hypobranchial, 3:
ceratobranchial, 4: epibranchial, 5: infrapharyngobranchial.
Fig.18. Lateral view of Weberian apparatus in Garra rufa populations 1: neural spine, 2 and 3: supraneural, 4: claustrum, 5: scaphium, 6,8,10: vertebra centrum, 7: tripus, 9: ribs.
insignificant (Fig. 18A, C).
Appendicular skeleton
Median fins: The dorsal fin has nine pterygiophores and one stay. Each pterygiophore as a base of fin ray consists of three fused elements, the distal, medial and proximal. The first dorsal fin pterygiophore is the largest one and its tip is overlapping with the neural spine of the vertebra 9 or 10 and tip of the last pterygiophore is over the vertebra 14-15. There are 2-3 unbranched dorsal fin rays which are attached to the first pterygiophore. The two first unbranched
dorsal fin rays are covered by skin and cannot be seen by superficial observation (Fig. 19). The differences in examined populations are in the number of supraneurals, present or absent of space between first pterygiophore and last supraneural, size of the supraneurals and size of the stay.
Some populations like Mazaii (b), Shahpour, Kangir and Kouh gari lack the supraneurals (Fig.
19A), some like Aks-e-Rostam (a), Ahram, Kheirabad, Mond, Bahoush, Alvand, Sartang, Bazoft, Shour-Karun, Shavour, Chaghalvandi, Fig.19. Lateral view of dorsal fin skeleton in Garra rufa populations; 1: proximal pterygiophore, 2: fin spine, 3: median pterygiophore, 4: distal pterygiophore, 5: stay, 6: supraneural.
Fig.20. Lateral view of anal fin of Garra rufa populations. 1: proximal pterygiophore, 2: fin spine, 3: median pterygiophore, 4: distal pterygiophore, 5: stay.
Pirbano, Shour-Bushehr, Karun and Kashkan populations have four supraneurals (Figure 19B) and some such as Aks-e-Rostam (b), Maroun, Doiraj, Seimareh, Semirum, Zoherh, Shiv, Davod-e Arab, Siahgav and Mazaii (a) populations have five supraneurals (Fig. 19C).
In Bahoush, Shavour and Shour-Bushehr populations there are two neural spines between first pterygiophore and last supraneural (Fig. 19B), but they are missing in Ahram, Aks-e-Rostam (a, b), Mazaii (a, b), Maroun, Shiv, Davod-e arab, Doiraj, Kheirabad, Shour-Karun, Bazoft, Sartang, Chaghalvandi, Pirbano, Kashkan, Mond, Seimareh, Karun, Zoherh, Alvand, Semirum and Siahgav populations (Fig. 19C).
The size of the stay in Aks-e-Rostam (b), Mazaii (a), Maroun, Shiv, Davod-e arab, Kangir, Kouh gari, Shahpour, Shour-Bushehr and Shavour populations is large (Figure 19B), but in Bazoft, Kheirabad, Aks- e-Rostam (a), Sartang, Chaghalvandi, Pirbano, Mond, Karun, Zoherh, Semirum, Siahgav, Bahoush, Kashkan, Alvand, Seimareh, Shour-Karun, Doiraj, Ahram and Mazaii (b) populations the size of stay elements is distinctly small (Fig. 19C).
Six pterygiophores and one stay comprises the anal fin skeleton. The two first unbranched rays of
the anal fin are connected to the first pterygiophore (Fig. 20). The proximal tip of the first pterygiophore touches the tip of the hemal spine of the 19th vertebra and the proximal tip of the last pterygiophore is under the 24th vertebra. The main differences among the studied populations is in size of the first pterygiophore. In Mazaii (a, b), Aks-e-Rostam (a, b), Ahram, Kheirabad, Shahpour, Shiv, Mond, Bahoush, Shour-Bushehr, Alvand, Maroun, Doiraj, Sartang, Bazoft, Zoherh, Shour-Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Kangir, Kouh gari, Semirum, Chaghalvandi and Pirbano populations the first pterygiophore is very large and wide (Fig. 20A), but in Davod-e arab population is small (Fig. 20B).
The caudal fin skeleton that supports all rays in this fin comprises four vertebrae (Fig. 21). The urostyle are formed by fusion of the two last vertebrae and two others and their neural and hemal spins support them and rays. The populations of G. rufa have divers shape and number in caudal fin skeleton elements, as the Shavour population have the two pairs uroneural, Mazaii (a), Aks-e-Rostam (a, b), Ahram, Kheirabad, Shahpour, Shiv, Mond, Bahoush, Shour-Bushehr, Alvand, Maroun, Davod-e arab, Doiraj, Sartang, Bazoft, Shour-Karun, Karun, Siahgav, Seimareh, Kashkan, Kangir, Kouh gari, Fig.21. Lateral view of caudal fin skeleton of Garra rufa populations, 1: preural 2-3, 2: neural spine, 3: rudimentary neural arch, 4: epural, 5: pleurostyle, 6: uroneural, 7: hypurals 2-5 or 6, 8: hypural 1, 9: parhypural, 10: hemal spine.
Chaghalvandi, Pirbano and Zohreh populations have one pair of Uroneural (Fig. 21A) and Semirum population lacks these elements (Fig. 21B). One population i.e. Alvand River, lacks hypural 6 (Fig.
21A), but others do have it (Fig. 21B). Other elements of caudal fin are similar in all populations.
Paired fins; The supporting bones of the pectoral fin are shown in Figure 22. The first unbranched ray is
directly connected to the scapula, but others are connected to actinosts. There are five actinosts in the pectoral fin girdle. In the populations, shape of ventral edge of the Cleithrum is different; in Mazaii (a, b), Ahram, Kheirabad, Shahpour, Shiv, Bahoush, Shour-Bushehr, Alvand, Davod-e arab, Sartang, Bazoft, Karun, Siahgav, Shavour, Kashkan, Kangir, Kouh gari, Pirbano and Zoherh populations this edge Fig.22. Lateral view of pectoral fin girdle Garra rufa populations. 1: supra cleithrum, 2: cleithrum, 3: mesocoracoid, 4:
scapula, 5: coracoid, 6: actinost.
Fig.23. Dorsal view of pelvic girdle of Garra rufa population. 1: basipterygium, 2: distal process, 3: mid lateral process, 4: actinosts, 5: pelvic splint, 6: post pterygium.
has no direct connection with other skeletal elements (Fig. 23). Populations of G. rufa have varied pelvic girdle, the diversity is in depth of bifurcated anterior portion of the basipterygium, size of extended tail of the anterior portion of the basipterygium, size and shape of the posterior process.
Depth of the bifurcated anterior portion of the basipterygium in Mazaii (a), Aks-e-Rostam (a,b), Shahpour, Shiv, Mond, Alvand, Maroun, Davod-e arab, Doiraj, Sartang, Bazoft, Shour-Karun, Siahgav, Seimareh, Shavour, Kashkan, Kangir, Semirum, Chaghalvandi, Pirbano, Zoherh and Shour-Bushehr populations of G. rufa is equal to less than total length of the basipterygium (Fig. 23A), but in Mazaii (b), Ahram, Kheirabad, Bahoush, Karun and Kouh gari, populations this depth is more than total length of the basipterygium (Fig. 23B).
The shape of end of the post pterygium in Mazaii (a), Aks-e-Rostam (a,b), Shahpour, Shiv, Mond, Shour-Bushehr, Alvand, Maroun, Davod-e arab, Doiraj, Sartang, Shour-Karun, Seimareh, Kashkan, Pirbano and Zoherh populations is pointed (Fig.
23A), but in Mazaii (b), Ahram, Kheirabad, Bahoush, Bazoft, Shavour, Kangir, Kouh gari, Semirum, Chaghalvandi, Karun and Siahgav populations is rounded (Fig. 23B). Furthermore, the length of the post pterygium in Mazaii (a), Aks-e-Rostam (a,b), Shahpour, Shiv, Mond, Shour-Bushehr, Alvand, Maroun, Davod-e arab, Doiraj, Sartang, Bazoft, Shour-Karun, Karun, Siahgav, Seimareh, Shavour, Kashkan, Kangir, Kouh gari, Semirum, Chaghalvandi, Pirbano and Zoherh populations is as twice as its width (Fig. 23A), but in those of Mazaii (b), Ahram, Kheirabad and Bahoush populations is equal with the width (Fig. 23B).
Discussion
Members of the genus Garra is distinguished by having mental disk shape, dorsal, anal and caudal fin
are different environmental conditions in these ecosystems such as variations in water properties and substrate features. These conditions show ability of these species to adapt to various environmental conditions and to show plasticity in morphology, osteology, feeding and swimming (Zhang et al.
2002).
The genus Garra has ten reported species in freshwaters of Iran, viz. G. rufa, G. persica, G. rossica, G. variabilis, G. nudiventris, G. mondica, G. lorestanensis, G. gymnothorax, G. typhlops, G. amirhosseini; G. tashanensis; and G. roseae' (Esmaeili et al. 2016; Hashemzadeh Segherloo et al.
2017; ;Mousavi Sabet et al. 2019). Most members of this genus are found in mountain streams and other flowing waters (Coad 2018); while some species such as G. lorestanensis and G. typhlops inhabit subterranean stagnant waters (Coad 2018; Mousavi- Sabet & Eagderi 2016; Esmaeili et al. 2016). Garra rufa populations inhabit many rivers in Iran, Iraq and Turkey.
Survivorship is related to adaptations that can be measured as the performance of functions in the context of the interaction between an organism and its environment maintained over generations (Brock 2000). In this regard, the skeletal system and its integration in the functioning of the skull can be considered as a highly important patterns for giving rise to evolutionary specializations by means of natural selection (Eagderi 2010). For example, Jalili
& Eagderi (2014) suggested that the skeletal adaptation of Iran cave barb during evolution as a result of response to a new habitat, i.e. a subterranean system can help better understanding of the evolutionary process due to adaptation to such ecosystems.
The differences in the lower jaw and reduction of the ventral masticatory plate may be a result of adaptation to a new feeding pattern in different rivers
hyoid series to buccal cavity expansion and large opercular series (Geerinckx et al. 2007), this mechanism can be used to adhere to substrates as a hydrological and feeding advantages (Geerinckx et al. 2007); in this study existing differences in suspensorium series (like shape of the endopterygoid, anterior margin of the hyomandibular), opercular series (size and extent of preopercle) and hyoid series among populations may be related to habitat conditions, because of the wide extent of sampling areas in this study probably has diverse habitats that lead G. rufa populations to display different and proportional structures in skeletal elements.
Vladykov (1954) showed that in the taxonomy of chars (Salmonidae), the most important of the skeleton is the tail and head elements. The reduction of the number of independent bones by fusion and hence the simplification of the caudal skeleton is an evolutionary advanced (Kotalawala & Jinadasa 991).
In this study, the populations have differences in presence or absent of the hypural 6 and number of the uroneural bones. The work of Gosline (1961) clearly demonstrates that evolution of the caudal skeleton in modern teleost is towards reduction and simplification by fusion of elements. Therefore, in the evolution of the Cyprinidae the reduction of the number of the epurals may have occurred by the fusion of spines. However, our results could be fully resolved only after a study of other populations and species of Garra.
Acknowledgements
We would like to thank S. Asadollah, M. Nasri, A. Nezamoleslami and A. Roozdar for their help in fish collection. This study was financially supported
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119
ناشفارد رلااس ، یناویک نادزی ،هبندارف ینامز رهاظم
یبط عبانم هدکشناد یع
( هورگ تلایش ) ، هاگشناد یتعنص ناهفصا ، ناهفصا ناریا ،
، 83111 - 84156 .
:هدیکچ
فاطعنا یذپ ر ی ناوختسا یتخانش عمج ی ت یاه فلتخم سنج Garra rufa (Heckel, 1843) زا
29 هسیاقم و فیصوت زیخبآ هضوح راهچ هب قلعتم هناخدور
.دندش هنومن یتلکسا یاهراتخاس G. rufa یاه
گنر فافش ،یزیمآ و یزاس
نآ زا سپس سکع اه
تیعمج .دیدرگ یرادرب شخب رد هعلاطم دروم یاه
لکسا فلتخم یاه ت
ی
توافت :هلمج زا دنداد ناشن ار ییاه 12
کف رد توافت راهچ ،رس هیحان تلکسا رد توافت رد توافت هس ،اه
کف آ رد توافت ود ،زیو رد توافت ود ،یششبآ شوپرس هعومجم
رد توافت راهچ ،یمشچ رود هعومجم فت هس ،یششبآ نامک هعومجم رد توافت کی ،یملا نامک هعومجم
ا ،ربو مادنا رد تو رد توافت کی ،یتشپ هلاب تلکسا رد توافت هس
جرخم هلاب تلکسا هنیس هلاب دنبرمک رد توافت کی ،ی
توافت نیا .یمد هلاب تلکسا رد توافت ود و یمکش هلاب تلکسا رد توافت هس ،یا اه
یراگزاس یشان تسا نکمم یاه
تیعمج یلماکت هاگتسیز هب فتلخم یاه
هسیاقم تاعلاطم رد تاعلاطا هنوگ نیا و دشاب توافتم یاه .دنراد یرثوم و دیفم شقن ینژولیف و یا
تاملک :یدیلک نایهامروپک ،
ناوختسا یسانش ، فاطعنا یریذپ ، یهام تلکسا .
