Iran. J. Ichthyol. (September 2017), 4(3): 220-230 Received: May 03, 2017 © 2017 Iranian Society of Ichthyology Accepted: June 27, 2017 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: 10.7508/iji.2017 http://www.ijichthyol.org

1-Research Article

Geometric morphometric comparison of trout barb, trutta (Teleostei: ) in the Tigris River basin

Yazdan KEIVANY* & Mohsen ARAB

Department of Natural Resource (Fisheries Division), Isfahan University of Technology, Isfahan 84156-83111, *Email: [email protected]

Abstract: A total of 136 specimens of trout barb, Capoeta trutta (Heckel, 1843) from eight rivers of the Tigris Basin were caught by seine net to compare their shape using geometric morphometrics. After anesthesia, using 1% clove oil solution, the specimens were fixed in 10% buffered formalin and transferred to the Ichthyology Museum of Isfahan University of Technology for further studies. The left sides of the specimens were photographed using a copy-stand equipped with a digital camera. To extract body shape data, 13 homologous landmark-points were digitized using tpsDig2 software. After GPA superimposing, the landmark data, were analyzed using Principal Components Analysis (PCA), Canonical Variate Analysis (CVA) and Cluster Analysis (CA) to explore the patterns of variation in their body shape. All multivariate analyses were computed using PAST software. The consensus configuration of populations was visualized using the wireframe graphs in MorphoJ to compare their shape difference. The PCA, CVA and CA showed differences among the populations, especially, between Konjancham and other populations. This result showed that geometric morphometric methods could separate trout barb populations of the Tigris River Basin from each other to a great extent. Potential factors contributing to the observed variations include differences in physicochemical parameters of rivers and geographic distance among the populations. However, for more details, molecular studies are needed.

Key words: , Geometry, Multivariate Analysis, Procrustes, Persian Gulf.

Citation: Keivany, Y. & Arab, M. 2017. Geometric morphometric comparison of trout barb, Capoeta trutta (Teleostei: Cyprinidae) in the Tigris River basin. Iranian Journal of Ichthyology 4(3): 220-230.

Introduction isolation can provide a crucial information on Identification and recognition of different the evolutionary trend of organisms particularly populations of a is a basic requirement in rivers (Smith & Skulason 1996). River for management and conservation and contains almost half of the species (Froese exploitation of populations (Webb 1982). The & Pauly 2017). Two main factors for such a differences between populations of a single diversity are geographical isolation and species can indicate differences in habitat and diversity of the environmental conditions in behavioral characteristics, because rivers (Nacua et al. 2010; Nelson et al. 2016). require to adapt to their environmental Rivers are highly variable in hydrological and conditions for better functioning of their biological features, which can affect the bio- biological systems (Webb 1982). Therefore, logical characteristics of the aquatic organisms. morphological adaptations to the environ- There are several ways to distinguish the mental conditions along with geographical populations, the geometric morphometric

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Iranian Journal of Ichthyology (September 2017), 4(3): 220-230 method is a relatively modern method with (Heckel, 1870), inhabiting different rivers of many advantages, including being cost the Tigris River basin in Iran. Different effective, fast and useful (Bookstein 1997) and populations with a common origin may show has been used successfully in many studies different local adaptations due to environmental (Razavipour et al. 2013; Jalili et al. 2015; factors (Barlow & Munsey 1976). Therefore, Jamali-Ashtiani et al. 2015; Zamani & Eagderi the results of this study can provide important 2016; Moshayedi et al. 2016; Mouludi-Saleh et information on the evolutionary trend of this al. 2017; Banimasani et al. 2017). species. The trout barb (longspine scraper) is one of the important sport fishes in Iranian rivers and Material and Methods locally used for food. Although there are a few A total of 136 specimens of trout barb, Capoeta studies on the and biology of this trutta, from the Tigris River tributaries (the species in Iran (Poria et al. 2012; Baboli et al. Persian Gulf), in Iran were collected in 2009- 2012; Taghavi Niya et al. 2015; Radkhah & 2011 using seine nets (Fig. 1). The specimens Nowferesti 2016; Keivany et al. 2016; Esmaeili were anesthetized in 1% clove oil and fixed in & Teimori 2016; Esmaeili et al. 2017), this is 10% formalin and transferred to the museum the first work on its body shape variation. This for further studies. The left sides of the study was aimed to compare the body shape of specimens were photographed using a copy- eight populations of trout barb, Capoeta trutta stand equipped with a digital camera.

Fig. 1. Collection sites and number of specimens from each site in the Tigris River basin in parenthesis. 1. Sirvan (33), 2. Zimakan (10), 3. Deireh (11), 4. Karkheh (19), 5. Konjancham (21), 6. Doirej (14), 7. Eivan Abbasi (19), 8. Karun (18).

221 Iranian Journal of Ichthyology (September 2017), 4(3): 220-230

To extract body shape data, 13 homologous along with the specimens of Konjancham landmark-points were digitized using tpsDig2 population were located at negative part of the software (version 2.16) (Rohlf 1999). The PC1 axes showing a similar body pattern (Fig. landmark-points were selected at the specific 4). The specimens of this morph have a deeper points, in which a proper model of fish body body and a longer caudal peduncle. The second shape was extracted (Fig. 2). The landmark data morph type belonged to the specimens of the was submitted to a generalized procrustes other population, was positioned in the positive analysis (GPA) to remove non-shape data part of the PC1 axes. The members of this including scale, direction and position. Since morph type have a lower body depth, a shorter the sexes could not be recognized by caudal peduncle, a pectoral fin with a ventral appearance (Coad 2017); therefore, the data for position and snout and eye with a dorsal all specimens were pooled for all subsequent position. Comparison of the body shape of these analyses. The landmark data after GPA two populations using wireframe diagram superimposing were analyzed using Principal revealed that they differ in the body depth and Components Analysis (PCA), Canonical Variate the position of the snout (Fig. 5). Analysis (CVA) and Cluster Analysis (CA) to Doirej population differnciated from explore the patterns of variation in their body Konjancham and Deireh. In studying the body shape. All multivariate analysis were computed pattern changes, in positive direction of PC1, using PAST software (Hammer et al. 2001). the position of mouth (LM1), pectoral girdle The consensus configuration of populations (LM5,6) and dorsal fin (LM8,9) tend to change were visualized using the wireframe graphs in and head size to reduce (LM1,3-6). In positive MorphoJ 1.01 (Klingenberg 2011) to compare direction of PC2, the position of mouth (LM1) their shape differences. and pectoral girdle (LM5,6) tend to change and body hight to increase (LM8,9) (Fig. 4). Results Canonical variate analysis based on the p The paraposition of the landmarks was value calculated by permutation test indicated acceptable. The first four PC axes extracted significant differences among the populations from the variance-covariance matrix (PC1 = body shapes (Wilks lambda= 0.006, f= 5.93, 34.30%, PC2 = 19.15%, PC3 = 12.08% and p<0.00001). Konjancham, Doirej, Sirvan and PC4 = 7.57%) above the joliffe line (Fig. 3) of Zimakan populations were separated from each Principal components analysis, explained other. Also Karun, Karkheh and Deireh 73.10% of shape variations. Distribution of the populations were separated from each other to specimens in PCA graph showed the presence some extent (Fig. 5). of two morphological types in which first type

Fig. 2. Landmarks used for the analysis on trout barb specimens.

22 2 Iranian Journal of Ichthyology (September 2017), 4(3): 220-230

Fig. 3. Results of scree plot of principal component analysis (PCA) and display of Joullife cut-off point (solid line) that represents the border of principal components (circles) significance.

Fig. 4. Scatter plots of principal components scores for the group centroids of the studied populations. 1. Sirvan (33), 2. Zimakan (10), 3. Deireh (11), 4. Karkheh (19), 5. Konjancham (21), 6. Doirej (14), 7. Eivan Abbasi (19), 8. Karun (18).

In studying the body pattern changes, in distances (Table 2 and 3) indicate the degree of positive direction of CV1, the size of the head differenciatios among the populations. The (LM1,3-6) tend to reduce and body height highest differnce is between Doirej- (LM8,9), caudal peduncle length (LM12,13) konjancham and Doirej-Eivan Abbasi. In CA of tend to increase. In positive direction of CV2, the populations, Copernic Coeficient was the head size (LM1,3-6) tend to increase and 0.7638. Based on CA, Konjancham population caudal peduncle length (LM12,13) tent to was the most highly differenciated population decrease and position of dorsal fin (LM8,9) (Fig. 7). changes (Fig. 6). Mahallanobis and Procrustes

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Fig. 5. Wireframe graph showing the consensus body shape differences of trout barb in Tigris River basin.

Fig. 6. Scatter plots of canonical scores for the group centroids of the studied populations of trout barb in the Tigris River basin. 1. Sirvan (33), 2. Zimakan (10), 3. Deireh (11), 4. Karkheh (19), 5. Konjancham (21), 6. Doirej (14), 7. Eivan Abbasi (19), 8. Karun (18).

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Fig. 7. Wireframe graph showing the consensus body shape differences of trout barb in Tigris River basin.

Table 1. Mahallanobis distance between different populations of trout barb in the Tigris River basin. Populations Deireh Doirej Eivan Abbasi Konjancham Kark Karun Sirvan heh Doirej 5.80 Eivan Abbasi 3.77 6.20 Konjancham 3.27 6.82 3.80 Karkheh 3.76 4.72 3.31 4.34 Karun 3.99 4.10 4.19 5.22 2.68 Sirvan 3.64 5.33 2.32 4.65 3.02 3.29 Zimakan 2.96 5.83 3.06 3.31 3.53 4.30 3.18

Table 2. Procrustes distance between different populations of trout barb in the Tigris River basin. Populations Deireh Doirej Eivan Abbasi Konjancham Karkheh Karun Sirvan Doirej 0.041 Eivan Abbasi 0.028 0.047 Konjancham 0.028 0.061 0.040 Karkheh 0.033 0.032 0.029 0.051 Karun 0.040 0.029 0.037 0.062 0.019 Sirvan 0.029 0.036 0.021 0.051 0.022 0.024 Zimakan 0.018 0.036 0.023 0.038 0.029 0.037 0.022

22 5 Keivany & Arab-Geometric morphometric comparison of trout barb in Tigris River basin

Fig. 8. Graphs of the cluster analysis of the populations of trout barb in the Tigris River basin.

Discussion and Conclussions 2013). Since the habitat factors have a The results of this study showed significant significant effect on morphology of fish species shape differences among populations of trout (Baumgartner et al. 1988; Schluter & McPhail barb in different rivers of Tigris basin in Iran. 1992); therefore, the observed morphological Based on PCA, CVA, CA and Mahallanobis differences in the rivers, can be related to and Procrustes distances, Konjancham and diversity of habitats. Konjancham and Karun Karun were the most divergent populations rivers have different water flow and depth and from each other. The most differences were in a geographical distance which could cause this head height, caudal pecuncle height and body differences (Ghanbarifardi et al. 2014). depth. Generally, plasticity in morphology is a Environmental factors through natural selection response to different environmental conditions can increase the efficiency of a phenotype (Wimberger 1992). For eample, a deeper body among the members of a population and thus is with a thicker caudal peduncle could be an led to morphological isolation in different adaopation for higher speed and habitats (Smith & Skulason 1996; Keeley et al. maneuverability. On the other hand, a stream- 2007). For example, Heidari et al. (2013) found lined body is an adaptation to current and differences in the shape of C. capoeta swimming against runnind waters. Also, populations with the same origin in upstream differences in head shape and position of the and downstram of Manjil Dam in Sefidrud mouth is related to feeding (Langerhans et al. River and Jalili et al. (2015), found shape 2003). Different morphological characteristics differences in Kura bleak living in main strean of a single species populations can be due to and a tributary of Aras River. Anvarifar et al. either genetic differentiation or phenotypic (2012) found a relationship beween RAPD plasticity in response to environmental genetic markers and morphology in C. capoeta parameters of their habitat (Orr & Smith 1998; in Tajan River. There is a reverse relationship Schluter 2000; Guill et al. 2003; Eagderi et al. between variation coeficient and heritability of

226 Iranian Journal of Ichthyology (September 2017), 4(3): 220-230 the traits (Mamuris et al. 1998). morphometric could differentiate different Phenotypic variations among fishes in populations of trout barb, for moe regourous various habitat may be viewed as important conclusions molecular studies are needed. only if any differences in morphology translate into an increased fitness among the groups Acknowledgements (Nacua et al. 2010). Body shape differences The authors wish to express their gratitude to S. amongst the habitats often reflect variations in Dorafshan, M. Nasri, S. Asadollah, S.M.A. the swimming and feeding efficiency of fishes Mousavi, A. Nezamoleslami, A. Mirzaei and A. (Langerhans et al. 2003, Tahmasebi et al. 2017, Rouzdar for their assistance during fish Haghighy et al. 2015). Fishes living in an samplings. This study was financially environment with strong water current will supported by Isfahan University of have to conform to this habit. A fusiform shape Technology. reduces drag (Langerhans et al. 2003) and hence reduces the energy expenditure necessary References to maintain position in flowing water (Videler Anvarifar, H.; Farahmand, H.; Nematollahi, M.A.; 1993; Vogel 1994). In addition, our findings Rahmani, H.; Karami, M. & Khalili, B. 2012. suggest that in a comparative morphological Analytical relationships between study of species populations in different morphometric traits and RAPD markers in habitats, the morphological variations should SiahMahi, Capoeta gracilis, in Tajan River of Sari. Modern Genetics 7(2): 165-173. be considered. Hence, application of an Banimasani, M.; Keivany, Y. & Ebrahimi, E. 2017. exploratory multivariate analysis such as Comparative geometric morphometric study of principal component analysis, to find out the Capoeta fusca populations. Journal of patterns in a dataset, can help to better Environmental Biology: In press. understand the phenotypic variation among Baboli, J.M.; Niya, T.M. & Pazira, A. 2012. Length- organisms (Jolliffe 2002; Jalili et al. 2015; Coad weight relationship and condition factor of 2017). As shown in this study, CVA analysis copoetta trutta in shour river downstream. revealed a significant differences between the Advances in Environmental Biology 1731- populations, but PCA revealed that the two 1735. distinct morphological types are found among Barlow, G.W & Munsey, J.W.1976. The red devil- the members of the population. Midas arrow cichlid species complex in Nicaragua. In: Thorson, T.B. (ed.). Environmental conditions are more Investigations of the ichthyofauna of influential in early development of the traits and Nicaraguan lakes. School of Life Sciences, fishes in the same conditions tend to have University of Nebraska. Lincoln. pp.359-369. similar characteristics. On the other hand, when Baumgartner, J.V.; Bell, M.A. & Weinberg, P.H. fishes encounter new conditions they can 1988. Body Form Differences between the quickly adopt to it (Poulet et al. 2004(. Since the Enos Lake Species Pair of Threespine size affects the morphometric (Tzeng 2004), Sticklebacks (Gasterosteus aculeatus Elliot et al. (1995) and procrustes methods are Complex). Canadian Journal of Zoology 66(2): used to eliminate the size effects, thus it is 467-474. expected that the observed differences to be Bookstein, F.L. 1997. Morphometric tools for real. The trout barb like other barbs is a landmark data: geometry and biology. Cambridge University Press, Cambridge, UK. generalized species and distributed from cold Coad, B.W. 2017. Freshwater fishes of Iran. montain rivers to warm plain rivers www.briancoad.com (accessed 20 April 2017). (Razavipour et al., 2014) so that they are plastic Esmaeili, H.R. & Teimori, A. 2016. Fish Species to adopt to these different habitats and ensure Diversity of Fars. Fars Environment their survival (Soul & Cuzin-Roudy 1982; Department Press, Shiraz, 275 p. [in Farsi]. Soule 1982). Although geometric Esmaeili, H.R.; Mehraban, H.; Abbasi, K.; Keivany,

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22 9 Iran. J. Ichthyol. (September Iranian 2017),Journal 4(3): of Ichthyology 220-230 (September 2017), 4(3): 220Received:-230 May 03, 2017 © 2017 Iranian Society of Ichthyology Accepted: June 27, 2017 P-ISSN: 2383-1561; E-ISSN: 2383-0964 doi: 10.7508/iji.2017 http://www.ijichthyol.org

مقاله پژوهشی

مقایسه ریختسنجی هندسی جمعیتهای سیاهماهی خالدار )Capoeta trutta( در حوضه رودخانه تیگره

یزدان کیوانی* و محسن عرب گروه شیالت، دانشکده منابع طبیعی، دانشگاه صنعتی اصفهان، اصفهان 8415683111، ایران *Email: [email protected]

چکیده: تعداد 136 قطعه سیییاهماهی خالدار، (Capoeta trutta (Heckel, 1843، از هشیی رودخانه حوضییه رودخانه تیگره با ا ستفاده از تور پره به منظور مطالعه تفاوتهای ریختی صید شدند. نمونهها بعد از بیهو شی در محلول 1% گلمیخک، در فرمالین 10% تثبی شدند و برای مطالعات بعدی به موزه ماهیشناسی دانشگاه صنعتی اصفهان منتقل شدند. از طرف چپ ماهیان توسط دوربین مستقر بر پایه عکسبرداری شد. برای استخراج شکل، 13 لندمارک همتا با استفاده از نرمافزار tpsDig2 رقومیسازی شد. پس از پروکراسییی لندمارکها، برای آنالیزهای آماری، آزمونهای تجزیه به مؤلفههای اصیییلی PCA(، تحلیل همبسیییتگی کانونی CVA( و تحلیل خو شهای CA(، مورد ا ستفاده قرار گرف . تمام محا سبات چندمتغیره در نرمافزار PAST صورت گرف . شکل میانگین جمعی ها با ا ستفاده از قاب سیمی آنها برای مقای سه تفاوتهای شکلی آنها، مورد برر سی قرار گرف . آزمونهای PCA، CVA و CA ن شان دادند که بین جمعی ها، خ صو صاً کنجانچم با سایر جمعی ها در حو ضه دجله تفاوت معنیداری p>0/05( وجود دارد. این نتایج نشییان میدهند که روشهای ریخ سیینجی هندسییی قادر به تفکیک جمعی های حوضییه تیگره از یکدیگر هستند. دالیل بالقوه وجود تفاوتهای مشاهد شده میتواند وابسته به عوامل فیزیکوشیمیایی رودخانهها و فاصله جغرافیایی باشد. با این وجود، برای جزییات بیشتر نیاز به مطالعات مولکولی میباشد.

کلیدواژهها: بیومتری، کپورماهیان، ژئومتری، آنالیز چندمتغیره، پروکراس .

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