Research Article |
Corresponding author: Taiki Ito ( qqx36bd@gmail.com ) Academic editor: Sven Kullander
© 2017 Taiki Ito, Toyoaki Fukuda, Toshihiko Morimune, Kazumi Hosoya.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ito T, Fukuda T, Morimune T, Hosoya K (2017) Evolution of the connection patterns of the cephalic lateral line canal system and its use to diagnose opsariichthyin cyprinid fishes (Teleostei, Cyprinidae). ZooKeys 718: 115-131. https://doi.org/10.3897/zookeys.718.13574
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The cephalic lateral line canal systems were compared among 12 species of the cyprinid tribe Opsariichthyini. All species were characterized by the separation of the supraorbital canal from both the infraorbital and the temporal canals, and the left side of the supratemporal canal from the right side of the canal. In species of Candidia, Opsariichthys, Parazacco, and Zacco, and Nipponocypris sieboldii the temporal canal was separated from the preoperculomandibular canal. In Nipponocypris temminckii and N. koreanus, the temporal canal was connected to the preoperculomandibular canal. Separation of the left and right sides of the supratemporal canal is a possible synapomorphy of the opsariichthyin cyprinids. Opsariichthys uncirostris and O. bidens are unique among the opsariichthyins in that the connection between the infraorbital and temporal canals is retarded. The variation in arrangement of the cephalic lateral line canal system can be used as diagnostic characters for the opsariichthyin species.
Candidia , heterochrony, morphology, Parazacco , sensory organs, Zacco
The cyprinid tribe Opsariichthyini, of the subfamily Xenocypridinae (
Variations in the connection pattern of the cephalic lateral line canals, and the number and the distribution of canal pores on the head have often been used in the study of interrelationships within the family Cyprinidae (
The objectives of the present study are to: (a) describe the connecting patterns of the cephalic lateral line canal system in the opsariichthyins, (b) provide diagnostic characters for the opsariichthyin species, (c) discuss the evolution of the connecting patterns observed.
The genus level classification of the Opsariichthyini follows
Classification | Species | Source | Accession no. |
Xenocypridinae | |||
opsariichthyin | |||
Candidia barbata |
|
AY958200 | |
Candidia pingtungensis*1 |
|
AY958201 | |
Nipponocypris koreanus |
|
NC025286 | |
Nipponocypris sieboldii |
|
AY958198 | |
Nipponocypris temminckii |
|
AY958199 | |
Opsariichthys bidens |
|
AY958197 | |
Opsariichthys evolans*2 |
|
AY968191 | |
Opsariichthys kaopingensis*3 |
|
AY958189 | |
Opsariichthys pachycephalus |
|
AY958190 | |
Opsariichthys uncirostris |
|
AY958193 | |
Parazacco spilurus |
|
NC023786 | |
Zacco platypus |
|
AY958194 | |
others | |||
Culter alburnus | unpublished | GU190362 | |
Ctenopharyngodon idella |
|
EU391390 | |
Hemigrammocypris rasborella |
|
AP011422 | |
Hypophthalmichthys nobilis | unpublished | EU343733 | |
Ischikauia steenackeri |
|
AF375862 | |
Macrochirichthys macrochirus |
|
AP011234 | |
Metzia lineata |
|
HM224305 | |
Ochetobius elongatus |
|
AF309506 | |
Parachela siamensis |
|
HM224300 | |
Paralaubuca typus |
|
AP011211 | |
Squaliobarbus curriculus |
|
HM224308 | |
Xenocypris macrolepis*4 |
|
HM224310 | |
Acheilognathinae | |||
Acheilognathus typus |
|
AB239602 | |
Rhodeus ocellatus |
|
AB070205 | |
Tanakia limbata |
|
HM224309 | |
Gobioninae | |||
Hemibarbus barbus |
|
AB070241 | |
Pseudorasbora parva |
|
HM224302 | |
Leuciscinae | |||
Scardinius erythrophthalmus | unpublished | NC031561 | |
Tribolodon hakonensis |
|
NC018820 |
The connection states of the cephalic lateral line canal system in the opsariichthyins and out-group.
Classification | Species | SO-IO | IO-TC | TC-POM | ST-ST | Source |
Xenocypridinae | ||||||
opsariichthyin | ||||||
Candidia barbata*1 | – | + | – | – | This study | |
Candidia pingtungensis | – | + | – | – | This study | |
Nipponocypris koreanus | – | + | + | – | This study | |
Nipponocypris sieboldii | – | + | – | – | This study | |
Nipponocypris temminckii | – | + | + | – | This study | |
Opsariichthys bidens | – | ± | – | – | This study | |
Opsariichthys evolans | – | + | – | – | This study | |
Opsariichthys kaopingensis | – | + | – | – | This study | |
Opsariichthys pachycephalus | – | + | – | – | This study | |
Opsariichthys uncirostris | – | ± | – | – | This study | |
Parazacco spilurus*2 | – | + | – | – | This study | |
Zacco platypus | – | + | – | – | This study | |
others | ||||||
Culter alburnus | + | + | + | + |
|
|
Ctenopharyngodon idella | + | + | + | + |
|
|
Hemigrammocypris rasborella | – | + | – | + |
|
|
Hypophthalmichthys nobilis | – | + | + | + |
|
|
Ischikauia steenackeri | + | + | + | + |
|
|
Macrochirichthys macrochirus | + | + | + | † |
|
|
Metzia lineata | – | + | + | + |
|
|
Ochetobius elongatus | + | + | + | + |
|
|
Parachela siamensis | + | + | + | † |
|
|
Paralaubuca typus | + | + | + | + |
|
|
Squaliobarbus curriculus | + | + | + | + |
|
|
Xenocypris macrolepis | + | + | + | + |
|
|
Acheilognathinae | ||||||
Acheilognathus typus | – | + | – | – |
|
|
Rhodeus ocellatus | – | + | – | – |
|
|
Tanakia limbata | – | + | – | – |
|
|
Gobioninae | ||||||
Hemibarbus barbus | + | + | + | + |
|
|
Pseudorasbora parva | – | + | – | + |
|
|
Leuciscinae | ||||||
Scardinius erythrophthalmus | + | + | + | + |
|
|
Tribolodon hakonensis | – | + | – | + |
|
Methods used for observation of the cephalic lateral line canal systems followed those of
Furthermore, the canaliculi branching from each canal are defined as “bridges,” whereas the junctions connecting canals were termed “joints.” The three bridges and one joint were as follows: “frontal bridge” between SO and IO; “centroparietal bridge” recognizing that ST meets the opposite side ST; “infratemporal bridge” between POM and TC; and “anteropterotic joint” between IO and TC (Fig.
In some species in cyprinid subfamilies such as Gobioninae and Leuciscinae, development of the cephalic lateral line canal system is generally completed when the fish is approximately 60 mm in total length (= TL) (
To obtain a hypothesis about the branching pattern of the opsariichthyin species, we analyzed mitochondrial cytochrome b (cyt b) gene sequences downloaded from GenBank. This is because molecular data for the cyt b gene sequence of all the species examined in the present study have been accumulated by previous studies (Table
Specimens studied are deposited in the following institutions: Chonbuk National University, Jeollabuk-do, Korea (CNUC); Department of Fisheries, Faculty of Agriculture, Kyoto University, Kyoto, Japan (
Candidia barbata (Regan, 1908): FKUN 34180, 1, 94.8 mm standard length (= SL), Tamsui River, Taipei, Taiwan; FKUN 35264–35272, 9 , 49.3–94.8 mm SL, Shueili River, Nantou, Taiwan; KUN-P 44430–44433, 4 , 94.7–103.0 mm SL, Houlong River, Miaoli, Taiwan.
Candidia pingtungensis Chen Wu & Hsu, 2008: FKUN 35214–35215, KUN-P 44492, 44515–44516, 5, 53.3–112.9 mm SL, Kaoping River, Pingtung, Taiwan.
Nipponocypris koreanus (Kim, Oh & Hosoya, 2005): KUN-P 40584–40591, 8, 69.3–111.9 mm SL, Nakdong River, Yeongwol, Korea; KUN-P 44463, 44475–44476, 3, 111.3–137.2 mm SL, Nakdong River, Gyongnam, Korea.
Nipponocypris sieboldii (Temminck & Schlegel, 1846): KUN-P 40564–40573, 10, 81.3–105.0 mm SL, Yamato River Nara Pref., Japan; KUN-P 44764–44767, 4, 63.7–85.8 mm SL, Kizu River, Kyoto Pref., Japan.
Nipponocypris temminckii (Temminck & Schlegel, 1846): KUN-P 40574–40581, 40583, 9, 85.2–100.9 mm SL, Kizu River, Kyoto Pref., Japan; KUN-P 45003, 45005–45006, 3, 79.1–145.3 mm SL, Shiomi River, Saga Pref., Japan; KUN-P 45104–45105, 45109, 3, 110.8–130.9 mm SL, Kawatana River, Nagasaki Pref., Japan.
Opsariichthys bidens Günther, 1873:
Opsariichthys evolans (Jordan & Evermann, 1902): FKUN 35196–35199, 35255, 35256, 6, 50.9–81.1 mm SL, Fengshan River, Hsinchu, Taiwan; KUN-P 44427–44429, 3, 69.5–80.6 mm SL, Houlong River, Miaoli, Taiwan.
Opsariichthys kaopingensis Chen, Wu & Huang, 2009: KUN-P 40545–40547, 44402, 44404–44405, 44407, 7, 69.2–83.0 mm SL, Kaoping River, Pingtung, Taiwan.
Opsariichthys pachycephalus (Günther,1868): FKUN 35179–35183, 35194, 35195, 7, 69.4–95.4 mm SL, Fengshan River, Hsinchu, Taiwan; FKUN 35245, 35250, 35252, 3, 56.0–70.3 mm SL, Keelung River, Taipei, Taiwan.
Opsariichthys uncirostris (Temminck & Schlegel, 1846): FKUN 16487–16488, 16492, 16495, 4, 211.5–228.0 mm SL, Ishida River, Shiga Pref., Japan; FKUN 16561, 16569, 16574, 3, 83.9–139.6 mm SL, Lake Biwa, Shiga Pref., Japan; KUN-P 40548–40554, 40592, 44528, 44529, 10, 145.1–231.8 mm SL, Mano River, Shiga Pref., Japan; FKUN 31878–31880, 3, 65.8–80.7 mm SL, Bukhan River, Korea; KUN-P 40636, 1, 206.5 mm SL, Gupo fish market, Korea; CNUC 37632, 1, 213.1 mm SL, Mangyeong River, Korea.
Parazacco spilurus (Günther, 1868):
Zacco platypus (Temminck & Schlegel, 1846): KUN-P 40555–40563, 9, 79.1–93.0 mm SL, Yamato River, Nara Pref., Japan; KUN-P 44379, 44381, 44383, 44386–44388, 6, 114.5–123.4 mm SL, Mono River, Shiga Pref., Japan.
The cephalic lateral line canal system is comprised of five canals, three bridges, and one joint in all opsariichthyin specimens examined (Fig.
Diagram of the cephalic lateral line canal systems in the opsariichthyin fishes. A Candidia barbata, FKUN 34180, 94.8 mm SL B C. pingtungensis, FKUN 35215, 72.9 mm SL C Nipponocypris koreanus, FKUN 40587, 94.1 mm SL. Scale bar 5 mm. D N. sieboldii, FKUN 40571, 90.5 mm SL E N. temminckii, FKUN 40575, 94.5 mm SL F Opsariichthys bidens,
The canals were usually well ossified, although part of the POM (see below), the frontal bridge, the infratemporal bridge, and the anteropterotic joint were cutaneous tubes. The SO was housed in the nasal and frontal bones. This canal was separated from the IO and TC in all the opsariichthyin fishes (with the exception of one specimen of P. spilurus in which the SO and IO were connected:
Connecting patterns of the cephalic lateral line canal system of the out-groups are shown in Table
The number of pores on each canal are shown in Table
Mode, average ± standard deviation, and range of the number of pores in each part of the cephalic lateral line canal in the opsariichthyin cyprinids.
Species | SO | IO | TC | POM | ST |
Candidia barbata | 8, 8.00 ± 0, 8 | 12, 11.91 ± 0.30, 11–12 | 4, 4.00 ± 0, 4 | 14, 14.27 ± 1.27, 12–16 | 3, 3.00 ± 0, 3 |
Candidia pingtungensis | 8, 8.20 ± 0.45, 8–9 | 12, 12.60 ± 0.89, 12–14 | 4, 4.00 ± 0, 4 | 15, 14.20 ± 0.84, 13–15 | 3, 2.80 ± 0.45, 2–3 |
Nipponocypris koreanus | 8, 8.00 ± 0, 8 | 12, 11.82 ± 0.60, 11–13 | 4, 3.91 ± 0.30, 3–4 | 15, 14.91 ± 0.83, 13–16 | 3, 3.00 ± 0, 3 |
Nipponocypris sieboldii | 8, 8.00 ± 0, 8 | 12, 11.93 ± 0.83, 10–13 | 4, 4.11 ± 0.31, 4–5 | 14, 13.79 ± 0.97, 12–15 | 3, 3.00 ± 0, 3 |
Nipponocypris temminckii | 8, 8.00 ± 0, 8 | 12, 11.67 ± 0.49, 11–12 | 4, 4.07 ± 0.26, 4–5 | 15, 14.53 ± 0.99, 13–17 | 3, 3.00 ± 0, 3 |
Opsariichthys bidens | 8, 8.00 ± 0, 8 | 12, 12 ± 0.37, 11-13 | 4, 4 ± 0.37, 3-5 | 14, 14.33 ± 0.70, 13–16 | 3, 3.00 ± 0, 3 |
Opsariichthys evolans | 8, 8.00 ± 0, 8 | 12, 11.56 ± 0.73, 10–12 | 4, 4.00 ± 0, 4 | 12, 13.00 ± 0.87, 12–14 | 3, 3.00 ± 0, 3 |
Opsariichthys kaopingensis | 8, 8.00 ± 0, 8 | 12, 11.57 ± 0.53, 11–12 | 4, 4.00 ± 0, 4 | 13, 13.43 ± 0.79, 13–15 | 3, 3.00 ± 0, 3 |
Opsariichthys pachycephalus | 8, 8.00 ± 0, 8 | 12, 12.22 ± 0.67, 11–13 | 4, 4.11 ± 0.33, 4–5 | 14, 13.22 ± 0.83, 12–14 | 3, 3.00 ± 0, 3 |
Opsariichthys uncirostris | 8, 8.05 ± 0.22, 8–9 | 12, 11.95 ± 0.51, 11–13 | 4, 4.05 ± 0.22, 4–5 | 14, 14.95 ± 1.10, 14–17 | 3, 3.00 ± 0, 3 |
Parazacco spilurus | 8, 8.00 ± 0, 8 | 11, 11.25 ± 0.50, 11–12 | 4, 4.00 ± 0.82, 3–5 | 14, 13.50 ± 1.00, 12–14 | 3, 3.00 ± 0, 3 |
Zacco platypus | 8, 8.07 ± 0.27, 8–9 | 12, 11.79 ± 0.43, 11–12 | 4, 4.00 ± 0, 4 | 13, 13.00 ± 0.55, 12–14 | 3, 3.00 ± 0, 3 |
The topology of the ML tree is shown Figure
Parsimonious ancestral state reconstruction of the connecting states of the cephalic lateral line canal systems of the opsariichthyin fishes and their out-groups from the maximum likelihood tree inferred from cytochrome b sequences (InL = 12054.39). A The connecting states between the supraorbital (SO) and infraorbital (IO) canals B the connecting states between the temporal (TC) and preoperculomandibular (POM) canals C the connecting states between the left and right sides of the supratemporal canals (ST). The color of each node indicates the connecting states of the cephalic lateral line canal system: black, continuity; white, discontinuity; gray, both sides of the ST connected and extending anteriorly.
Significant differences were found in the number of pores on the POM among some opsariichthyin species. However, the number of pores on these canals was found to vary within each species, and there was an overlap of ranges among all observed species (Table
In contrast, the connecting pattern of the cephalic lateral line canals provides useful diagnostic character states for some species of the opsariichthyins. Nipponocypris temminckii and N. koreanus are clearly distinguished from the very similar species N. sieboldii by the connection between the POM and TC through the infratemporal bridge. Similarly, O. uncirostris can be distinguished from O. bidens on the basis that the two species have different sizes at which the connection between the IO and TCattains completion (ca. 180 mm SL vs. ca. 100 mm SL, respectively), although many investigators have indicated that these two species can only be distinguished by the number of scales in the lateral series (e.g.,
All opsariichthyin species share the canal separation between the left and right sides of the ST. Although, this character state also occurs at the root of the Acheilognathinae, this characteristic strongly supports the monophyly of the opsariichthyins, because the characteristic was derived only once from the common ancestor of the opsariichthyins in the Xenocypridinae. The opsariichthyins have been defined in terms of a single shared character state, viz. a long anal fin (
Opsariichthys uncirostris and O. bidens have a unique ontogeny of the cephalic lateral line canal system. In the Cyprinidae, the cephalic lateral line canal systems are generally completed at 40–60 mm in TL (
This study was funded in part by a Grant-in-Aid for Scientific Exploratory Research (20657019). We are grateful to I. S. Chen, his students at the National Taiwan Ocean University, M. K. Oh, H. T. Lai (National Chia-Yi University: NCU), C. H. Tung (NCU), C. C. Han (National Museum of Marine Biology & Aquarium), M. Nitta (Hiroshima University) and S. Kunimatsu (Osaka University) for their cooperation in collecting materials. We are greatly indebted to C. H. Kim (National Fisheries Research and Development Institute), J. Y. Park (CNUC), S. Kimura (