Comparative Morphology and Morphometry of the Olfactory Organ of the Six Korean Spined Loaches, Genus Iksookimia, as a New Taxonomic Key
Seung Woon Yun1, Jong Young Park1 and Hyun Tae Kim2*
1Department of Biological Science, College of Natural Sciences, Jeonbuk National University, Jeonju 54896, Republic of Korea
2Department of Science Education, Jeonju National University of Education, Jeonju 54896, Republic of Korea
Seung Woon Yun and Jong Young Park contributed equally to this work.
ABSTRACT
The olfactory structure of Korean spined loaches, Iksookimia koreensis, I. pumila, I. pacifica, I. longicorpus, I. hugowolfeldi, I. yongdokensis, were investigated by anatomical observation and statistical analysis. They share the same olfactory morphology characterized by tubular anterior and flat posterior nostrils and a rosette showing a radial arrangement of finger-like curved lamellae. However, the number of olfactory lamellae (LN) differs by species: 19-25 in I. longicorpus (with standard length, SL, 113.2±11.5 mm, mean±SD), 17-20 in I. yongdokensis (88.1±8.8 mm), 14-20 in I. hugowolfeldi (77.4±8.1 mm), 16-19 in I. koreensis (76.1±6.5 mm), 15-20 in I. pacifica (100.9±17.3mm), 15-19 in I. pumila (77.8±5.5 mm). In particular, I. koreensis (23.0±1.4%) and I. hugowolfeldi (22.4±2.4%) shows higher LN/SL ratios than do I. longicorpus (19.4±1.8%) and I. pacifica (17.5±2.0%). This comparison of LN and LN/SL ratio among species could be used as new taxonomic key of Iksookimia.
Article Information
Received 30 August 2023
Revised 15 February 2024
Accepted 22 February 2024
Available online 08 April 2024
(early access)
Published 03 June 2025
Authors’ Contribution
SWY and JYP wrote the manuscript and made figures and table. HTK edited and approved the manuscript for publication.
Key words
Olfactory organ, Nostril, Rosette, Lamellar number, Iksookimia, Taxonomy
DOI: https://dx.doi.org/10.17582/journal.pjz/20230830034720
* Corresponding author: [email protected]
0030-9923/2025/0004-1581 $ 9.00/00
Copyright 2025 by the authors. Licensee Zoological Society of Pakistan.
This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
INTRODUCTION
In addition to vision, hearing, current and acoustic pressure detection, electroreception, and magnetoreception, most teleost species rely on olfaction for detecting foods, hazardous materials, and pheromones; discriminating same from foreign species; and avoiding predators, migrating, and homing (Hara, 1986; Zielinski and Hara, 2006; Chung-Davidson et al., 2010). Because such chemical reception is conducted by sensory cells on the lamellae of the rosette inside the olfactory chamber, teleost species shows species-specific structure in olfactory rosette based on their habitat environment and ecology (Cox, 2008). Teleosts show considerable morphological variability regarding the shape and location of the olfactory organ, number and arrangement of the olfactory lamellae, the distribution of sensory and non-sensory epithelium in relation to the diverse environments that the fish inhabit (Hara, 1986; Zeiske et al., 1992; Kasumyan, 2004; Ghosh and Chakrabarti, 2016; Ghosh, 2019; Triana-Garcia et al., 2021). In particular, although the number of olfactory lamellae (LN) tends to increase with growth and age, it remains constant upon teleost maturity (Hara, 1994). Accordingly, the number of olfactory lamellae has been used as a species-specific trait for taxonomy (LN 0 in genera Periophthalmus, Boleophthalmus, Oryzias, and Rudarius; LN 1 in Navodon, Hemiramphus, Cheilopogon, and Cololabis; LN > 100 in Angulla and Conger, and up to 200 in Pseudoplatystoma corruscans) among taxa (Matsuura, 1982; Matsuura and Tyler 1997; Tyler, 1997; Kim and Park, 2020), as well as between distant teleost species (Zeiske et al., 1992; Kasumyan, 2004; Kuciel et al., 2013).
The multiple ranges of mountains in Korea have resulted in numerous freshwater streams flowing independently to the sea (Kim et al., 2005). This isolation of Korean water systems has resulted in evolution of Iksookimia into six endemic species: Iksookimia koreensis, Kim (1975); Iksookimia pumila, Kim and Lee (1987); Iksookimia pacifica, Kim et al. (1999); Iksookimia longicorpus, Kim et al. (1976); Iksookimia hugowolfeldi, Nalbant (1993); Iksookimia yongdokensis, Kim and Park (1997), based on habitat preference and morphology (Ko, 2015; Park et al., 2016; Ko et al., 2020). Recently, during Korean fish research to prove allopatric speciation, we have recognized that the olfactory organ of Liobagrus shows morphometrical differences in relation to its microhabitat preference (Kim and Park, 2020). So, we assumed that the olfactory organ of Iksookimia as an example of representative geographical speciation in South Korea also is likely to exhibit different adaptations. The present study focused on comparative morphology and morphometry of the olfactory organ of six Korean loaches based on taxonomy.
MATERIALS AND METHODS
Sample preparation
The six Korean spined loaches (a total of 120 specimens, 20 per species) of Iksookimia (I. koreensis, I. pumila, I. pacifica, I. longicorpus, I. hugowolfeldi, I. yongdokensis) were caught from numerous waterways from May to June 2022 (Table I). The endangered species I. pumila was caught with written permission (Number 2021-18) from the Ministry of Environment. After capture, two specimens per species were fixed with 2.5% glutaraldehyde solution (pH 7.4) for scanning electron microscopy (SEM), and the rest were preserved in 10% neutral formalin solution (pH 7.4) to measure the standard length (SL) and count the LN of the olfactory organ. We used full-grown adults demonstrating sexual dimorphism (Buj et al., 2015).
Anatomical structure
The olfactory organs were carefully dissected from the olfactory chamber on the dorsal side of the head under a stereo microscope (Stemi DV4, Carl Zeiss, Germany); counted and averaged the lamellae numbers; nostril and rosette images of olfactory organ were collected for morphological analysis with a digital camera (TG-3, Olympus, Tokyo, Japan). For SEM, dissected olfactory rosettes of each specimen were postfixed in 1.0% osmium tetroxide-phosphate buffer (pH 7.4) solution for six hours at room temperature, dehydrated with an ascending alcohol series (60% to 100%) for 20 minutes at each concentration, transferred to tert-butyl alcohol, freeze-dried (Vfd-21S, Vacuum Device Co., Ltd., Ibaragi, Japan), coated with white 1 µm thick gold by ion-sputter (HPC-1SW, Vacuum Device Inc., Tokyo, Japan), and filmed with a scanning electron microscope (S-3000N, Hitachi, Tokyo, Japan).
Statistical analysis
SPSS software (IBM® SPSS® Statistics, SPSS version 18.0, USA) was used for interspecies numerical analysis of the SL and LN of Iksookimia. For a parametric test based on the results of Kolmogorov-Smirnov or Shapiro-Wilk test (P > 0.05), one-way ANOVA was followed by Duncan’s multiple range test and used to compare mean SL, LN, and LN/SL ratio between species. ANCOVA was used to analyze the LN difference based on the covariate SL. Pearson’s correlation coefficient was used to identify a possible allometric association between SL and LN.
Table I. Measurements of Korean loaches (genus Iksookimia) and collection localities.
|
SL (mm) |
Weight (g) |
Collection locality (GPS) |
|
|
I. koreensis (n=20) |
76.1±6.5 (67.4~91.0) |
4.8±1.4 (3~9) |
Andeog-ri, Gui-myeon, Wanju-gun, Jeollabuk-do (35○44'34''N, 127○07'15''E) |
|
I. longicorpa (n=20) |
113.2±11.5 (100.6~141.8) |
9.2±2.0 (6~13) |
Dongsan-ri, Bokheung-myeon, Sunchang-gun, Jeollabuk-do (35○26'52''N, 126○55'09''E) |
|
I. hugowolfeldi (n=20) |
77.4±8.1 (61.8~93.8) |
7.4±1.9 (5~12) |
Eojeon-ri, Geumsan-myeon, Goheung-gun, Jeollanam-do (34○26'20''N, 127○09'42''E) |
|
I. pumila (n=20) |
77.8±5.5 (70.3~91.0) |
5.0±1.2 (3~7) |
Cheongnim-ri, Sangseo-myeon, Buan-gun, Jeollabuk-do (35○39'17''N, 126○36'35''E) |
|
I. pacifica (n=20) |
100.9±17.3 (75.3~128.6) |
8.6±4.2 (4~17) |
Sampo-ri, Jugwang-myeon, Goseong-gun, Gangwon-do (38○18'27''N, 128○31'38''E) |
|
I. yongdokensis (n=20) |
88.1±8.8 (75.7~105.0) |
6.9±1.7 (5~11) |
Sangwon-gil, Chuksan-myeon, Yeongdeok-gun, Gyeongsangbuk-do (36○30'23''N, 129○24'35''E) |
Mean±SD (Min~Max); SL, standard length; n, number.
RESULTS
Anatomical structure of the olfactory organ
The Iksookimia species share same structure of anterior and posterior nostrils, rosette and lamellae of the olfactory organ, a paired sensory system located on both sides of the snout, with anterior and posterior nostrils present on each side (Fig. 1). The anterior nostril is a vertical wind-curve entrance tube protruding at differing heights from the skin surface (Fig. 1A). The posterior nostril is in the same level with skin surface and appears as an elliptical vent with a swollen skin edge (Fig. 1B). The two nostrils are separated by a nasal bridge on the skin and open to the outside. The olfactory rosette of the Korean spined loaches is comprised of several lamella originating from the ventral and lateral walls of the olfactory chamber and arranged based on the medium raphe (Fig. 2A-F). Each lamella is a center-bent finger-like structure, and they gradually increase in size from the anterior toward the posterior region. They are positioned parallelly at the front and middle part of the rosette and arranged radially at the posterior part. Each lamella also is thicker in the base and become thinner as getting upward (Fig. 2A-F). The center of the medium raphe is thicker and wider, and it narrows as going up and down (Fig. 2A-F).
Statistical analysis of the olfactory lamellae
The SL showed different measurements: I. longicorpus was the longest (113.2±11.5, 100.6-141.8; Mean±SD,
range); followed by I. pacifica, 100.9±17.3, 75.3-128.6; I. yongdokensis, 88.1±8.8, 75.7-105.0; I. pumila, 77.8±5.5, 70.3-91.0; I. hugowolfeldi, 77.4±8.1, 61.8-93.8; and I. koreensis was the shortest (76.1±6.5, 67.4-91.0). There was a significant difference in SL among the species (one-way ANOVA, F5, 114 = 42.8, P < 0.001; Fig. 3A). The LNs also were different among the six Korean spined loaches: I. longicorpus had the highest number (21.9±1.7, 19-25; mean±SD, range), followed by I. yongdokensis, 18.0±0.9, 17-20; I. hugowolfeldi, 17.2±1.8, 14-20; I. koreensis, 17.4±1.0, 16-19; I. pacifica, 17.4±1.5, 15-20; and I. pumila with the smallest number (16.4±1.4, 15-19).There was a significant difference in LN among species (one-way ANOVA, F5, 114 = 37.0, P < 0.001; Fig. 3B). The LN/SL ratio showed meaningful differences: I. koreensis had the highest ratio (23.0±1.4%, 19.5-24.9); followed by I. hugowolfeldi, 22.4±2.4%, 17.9-26.0; I. pumila, 21.1±1.1%, 19.1-23.8; I. yongdokensis, 20.5±1.4%, 18.4-22.9; I. longicorpus, 19.4±1.8%, 16.6-23.1; and then I. pacifica (17.5±2.0%, 14.8-21.4). The difference among them was significant (one-way ANOVA, F5, 114 = 26.0, P < 0.001; Fig. 3C). The LN difference between species was affected strongly by SL as a covariate (ANCOVA, F5, 114 = 19.5, P < 0.001). The SL and LN had a significant correlation in I. koreensis (Pearson’s correlation coefficient, r = 0.650, P < 0.05), I. longicorpus (r = 0.481, P < 0.05), I. pumila (r = 0.779, P < 0.001), I. pacifica (r = 0.820, P < 0.001), and I. yongdokensis (r = 0.762, P < 0.001) but not in I. hugowolfeldi (r = 0.424, P = 0.063) (Fig. 4).
DISCUSSION
Distinct from the related genus Cobitis with Gambetta’s zones as a pigmentary zone on lateral body but sharing similar habitat (the middle to upper streams with gravels and sandy bottom), genera Iksookimia is currently classified into six endemic Korean species based on (i) geological distribution, and (ii) morphology (the lamina circularis as bony process or plate at the base of the first and second rays of the pectoral-fin and the body pigmentation) (Kim and Park, 1997, 2002; Kim, 2009; Ko, 2015). The organisms in question also demonstrate different reproductive strategies in egg envelope structure (papilla, villi, grapevine, hillock, granule, unadorned form, and sawtooth-like form) in relation to the river bottom structure (Ekmekci and Erk’akan, 2003; Ko and Park, 2010), spawning character (Ko and Won, 2016), and early life history (Ko et al., 2017). These different adaptations of Iksookima are well-correlated with their geographical distribution and are a good example of allopatric speciation (Kim, 1997). The morphological variations, frequent interspecific hybridization, and similar genetic sequences of Korean spined loaches (Family Cobitidae) have interested many ichthyologists (Kim, 2009). However, these overlapping features have been the source of taxonomic debate in recent days. I. pacifica was reclassified from the genus Cobitis into the genus Iksookimia based on rippled pigmentation of its dorso-lateral surface of body (Kim, 2009). Cobitis choii was first described as a new species of Cobitis by Kim and Son (1984), but was reclassified into the genus Iksookimia by Nalbant (1993) before it finally was returned to the genus Cobitis. To clarify the taxonomy of Iksookimia, we described the LN and LN/SL ratio as a suggested new taxonomic key for morphometrical analysis.
All Korean spined loaches share the same olfactory morphology with two openings (tubular anterior nostril and posterior nostril flat against the skin surface) on each side of the snout and the olfactory rosette composed of several finger-like lamellae. The tubular nostril typically appears in bottom-dwelling teleosts is a functional boundary layer between inflow of chemical odors to the olfactory organ (Belanger, 2003; Sarkar et al., 2014; Kim and Park, 2020). Such an olfactory entrance may be related to the benthic habitat of Korean spined loaches, which spends their lifetime on the river bottom (Kim and Park, 2002; Park et al., 2018).
In contrast to this morphological similarity, the olfactory morphometry of Iksookimia shows interspecies variation in that the LN and LN/SL ratio differ by species size. Kim and Park (2020) demonstrated that, although the LN ranges overlap, Liobagrus fish showed significant mean difference: 16-19 in L. andersoni, 14-16 in L. obesus, 22-27 in L. mediadiposalis, 19-24 in L. somjinensis, 14-18 in L. hyeongsanensis, which could be useful to identify species based on microhabitat adaptation. Recently, Silva-Junior and Zanata (2022) reported variability among six geologically diverse species of the genus Parotocinclus based on LN to SL ration and sexual dimorphism that could be used as a new species indicator. Therefore, difference in LN and LN/SL ratio among species of Iksookimia might be a useful taxonomic key to reflect their different geographical distribution.
Regarding LN, I. longicorpus was highest (21.9±1.7), followed by I. yongdokensis, 18.0±0.9; I. hugowolfeldi, 17.2±1.8; I. koreensis, 17.4±1.0; I. pacifica, 17.4±1.5; and then I. pumila (16.4±1.4). However, based on LN/SL ratio, I. koreensis was highest (23.0±1.4%), followed by I. hugowolfeldi, 22.4±2.4%; I. pumila, 21.1±1.1%; I. yongdokensis, 20.5±1.4%; I. longicorpus, 19.4±1.8%; and then I. pacifica, 17.5±2.0%. Considering the correlation between LN and olfactory function, Fishelson et al. (2010) opined that the rosette of abundant lamellae in synodontids (active predator) indicates a more important role of olfaction in their life history compared to benny fishes with a small-sized rosette. Based on this collective finding, larger LN/SL ratio suggest that olfaction of I. koreensis and I. hugowolfeldi may be more important in their life history despite a smaller LN than that of I. longicorpus and I. pacifica. Analysis of correlation between olfactory lamellae and body size has focused on the LN increase with body size (Kudo et al., 2009; Atta, 2013). Herein, we confirmed that the LN/SL ratio among related species could distinguish species, highlight relative importance of olfaction, and is suggested as newly taxonomic key.
CONCLUSION
As a good example of allopatric speciation, the genus Iksookima shows different adaptations well-correlated with geographical distribution among them. They also reveal morphological variations, frequent interspecific hybridization, and similar genetic sequences. However, these overlapping features have been the source of taxonomic debate in recent days. Therefore, we aim to report new morphological taxonomic key using the features of the olfactory rosette morphology and morphometry for species identification. Our findings demonstrated that difference in LN and LN/SL ratio among species of Iksookimia might be a useful taxonomic key to reflect their different geographical distribution. So, LN and LN/SL ratio are recommended as a new and meaningful taxonomic character that distinguishes sympatric species at least in Iksookimia.
ACKNOWLEDGMENT
We are thankful to our laboratory colleagues who helped us collect specimens and conduct fieldwork.
Funding
No funding was received for this work.
IRB approval
This study was approved by the Institutional Review Board at Jeonbuk National University.
Ethical statement
All procedures of animal experiment strictly obeyed the rules of the Jeonbuk National University Institutional Animal Care and Use Committee (Licence Number: CBNU-2022-00060).
Statement of conflict of interest
The authors have declared no conflict of interest.
REFFERENCES
Atta, K.I., 2013. Morphological, anatomical and histological studies on the olfactory organs and eyes of teleost fish: Anguilla anguilla in relation to its feeding habits. J. Basic appl. Zool., 66: 101-108. https://doi.org/10.1016/j.jobaz.2013.10.002
Belanger, R.M., Smith, C.M., Corkum, L.D. and Zielinski, B.S., 2003. Morphology and histochemistry of the peripheral olfactory organ in the round goby, Neogobius melanostomus (Teleostei: Gobiidae). J. Morphol., 257: 62-71. https://doi.org/10.1002/jmor.10106
Buj, I., Šanda, R., Marčić, Z., Ćaleta, M. and Mrakovčić, M., 2015. Sexual dimorphism of five Cobitis species (Cypriniformes, Actinopterygii) in the Adriatic watershed. Folia Zool., 64: 97-103. https://doi.org/10.25225/fozo.v64.i2.a2.2015
Chung-Davidson, Y.W., Huertas, M. and Li, W., 2010. A review of research in fish pheromones. In: Chemical communication in crustaceans (eds. T. Breithaupt and M. Thiel)., Springer, New York. pp. 467–482. https://doi.org/10.1007/978-0-387-77101-4_24
Cox, J.P., 2008. Hydrodynamic aspects of fish olfaction. J. R. Soc. Int., 5: 575-593. https://doi.org/10.1098/rsif.2007.1281
Ekmekci, F.G. and Erk’akan, F., 2003. Preliminary data on growth and reproduction of Cobitis cimplicispina from Turkey. Folia Biol., 51(Suppl.): 183-186.
Fishelson, L., Golani, D., Galil, B. and Goren, M., 2010. Comparison of the nasal olfactory organs of various species of lizardfishes (Teleostei: Aulopiformes: Synodontidae) with additional remarks on the brain. Int. J. Zool., 2010: 1-8. https://doi.org/10.1155/2010/807913
Ghosh, S.K. and Chakrabarti, P., 2016. Morphological and histochemical studies on the olfactory rosette of bagrid catfish, Rita kuturnee (Sykes, 1839). Mesopot. J. Mar. Sci., 31: 14-28. https://doi.org/10.58629/mjms.v31i1.107
Ghosh, S.K., 2019. Histology and surface morphology of the olfactory epithelium in the freshwater teleost Clupisoma garua (Hamilton, 1822). Fish. aquat. Life, 27: 122-129. https://doi.org/10.2478/aopf-2019-0014
Hara, T.J., 1986. Role of olfaction in fish behaviour. In: The behaviour of teleost fishes (eds. T.J. Pitcher). Springer, Boston, M.A. pp. 152-176. https://doi.org/10.1007/978-1-4684-8261-4_6
Hara, T.J., 1994. Olfaction and gustation in fish: An overview. Acta Physiol. Scand., 152: 207-217. https://doi.org/10.1111/j.1748-1716.1994.tb09800.x
Kasumyan, A.O., 2004. The olfactory system in fish: Structure, function, and role in behavior. J. Ichthyol., 44: S180.
Kim, H.T. and Park, J.Y., 2020. Comparative morphology and morphometry of the olfactory organ in the five Korean torrent catfishes, genus Liobagrus, with a taxonomic view. Zool. Sci., 37: 575-579. https://doi.org/10.2108/zs200046
Kim, I.S. and Lee, W.O., 1987. A new subspecies of cobitid fish (pisces: Cobitidae) from the Paikchŏn Stream, Chŏllabuk-do, Korea. Korean J. System. Zool., 3: 57-62.
Kim, I.S. and Park, J.Y., 1997. Iksookimia yongdokensis, a new cobitid fish (Pisces: Cobitidae) from Korea with a key to the species of Iksookimia. Ichthyol. Res., 44: 249-256. https://doi.org/10.1007/BF02678704
Kim, I.S. and Park, J.Y., 2002. Freshwater fishes of Korea. Kyohak Publishing co. Ltd., Korea, pp. 252–259. (in Korean).
Kim, I.S., 1975. A new species of cobitid fish from Korea (Cobitis koreensis). Korean J. Limnol., 8: 51-58.
Kim, I.S., 1997. Illustrated encyclopedia of fauna and flora of Korea. Vol. 37, Freshwater fishes. Ministry of Education, Seoul, 613 pp. (in Korean)
Kim, I.S., 2009. A review of the spined loaches, family Cobitidae (Cypriniformes) in Korea. Korean J. Ichthyol., 21: 7-28.
Kim, I.S., Choi, K.C. and Nalbant, T.T., 1976. Cobitis longicorpus, a new cobitid fish form Korea. Korean J. Zool., 19: 171-178.
Kim, I.S., Choi, Y., Lee, C.L., Lee, Y.J., Kim, B.J. and Kim, J.H., 2005. Illustrated book of Korean fishes. Kyohak Publishing Co Ltd, Seoul, 615 pp. (in Korean)
Kim, I.S., Park, J.Y. and Nalbant, T.T., 1999. The far-east species of the genus Cobitis with the description of three new taxa (Pisces: Ostariophysi: Cobitidae). Trav. Mus. natl. Hist. Nat. Grigore Antipa, 39: 373-391.
Kim, I.S. and Son, Y.M., 1984. Cobitis choii, a new cobitid fish from Korea. Korean J. Zool., 27: 49-55.
Ko, M.H. and Park, J.Y., 2010. Fine structure of oocyte envelopes of diploid and triploid biotypes in Cobitis hankugensis-Iksookimia longicorpa complex. Korean J. Ichthyol., 22: 56-60.
Ko, M.H. and Won, Y.J., 2016. The age and spawning characteristics of the Korean endemic spine loach, Iksookimia pacifica (Pisces: Cobitidae) in the Bukcheon (stream), Korea. Korean J. Ichthyol., 28: 72-78.
Ko, M.H., 2015. Habitat characteristics and feeding ecology of the Korean endemic species, Iksookimia pacifica (Pisces: Cobitidae) in the Bukcheon (stream), Korea. Korean J. Ichthyol., 27: 275-283. (in Korean).
Ko, M.H., Han, M.S. and Kweon, S.M., 2020. Distribution status and extinction threat evaluation of the Korean endemic species, Iksookimia yongdokensis. Korean J. Ichthyol., 32: 1-7. (in Korean). https://doi.org/10.35399/ISK.32.1.1
Ko, M.H., Jeon, Y.S., and Won, Y.J., 2017. Early life history of the eastern Korean tetraploid spined loach, Iksookimia yongdokensis (Pisces: Cobitidae). Folia Zool., 66: 153-162. https://doi.org/10.25225/fozo.v66.i3.a2.2017
Kuciel, M., Żuwała, K. and Satapoomin, U., 2013. Comparative morphology (SEM) of the peripheral olfactory organ in the Oxudercinae subfamily (Gobiidae, Perciformes). Zool. Anz., 252: 424-430. https://doi.org/10.1016/j.jcz.2013.03.002
Kudo, H., Shinto, M., Sakurai, Y. and Kaeriyama, M., 2009. Morphometry of olfactory lamellae and olfactory receptor neurons during the life history of chum salmon (Oncorhynchus keta). Chem. Senses, 34: 617-624. https://doi.org/10.1093/chemse/bjp042
Matsuura, K. and Tyler, J.C., 1997. Tetraodontiform fishes, mostly from deep waters, of New Caledonia. Mem. Mus. natl. Hist. Nat., 174: 173-208.
Matsuura, K., 1982. A new triacanthodid fish, Triacanthodes indicus, from the Indian Ocean. Jpn. J. Ichthyol., 28: 385-392.
Nalbant, T.T., 1993. Some problems in the systematics of the genus Cobitis and its relative (Pisces: Ostariophysi, Cobitidae). Rev. Roum. Biol. Anim., 38: 101–110.
Park, C.W., Kim, H.S., Kim, J.G., Yun, S.W., Kim, H.T., Park, J.S., Choi, W.S., Cho, Y.J. and Park, J.Y., 2016. Microhabitat characteristics of the Korean endemic cobitid species Iksookimia hugowolfeldi inhabited at Geogeum island and Jangheung-gun in Korea. Korean J. Ichthyol., 28: 35-40.
Park, C.W., Kim, J.G., Yun, S.W., Kim, H.T., Park, J.S., Choi, W.S., Cho, Y.J., Lee, Y.J. and Park, J.Y., 2018. Habitat, diet, feeding and resting behaviour of the Korean endemic cobitid Iksookimia hugowolfeldi (Cobitidae, Pisces) in the wild. Folia Zool., 67: 1-8. https://doi.org/10.25225/fozo.v67.i1.a2.2018
Park, J.Y. and Kim, I.S., 1996. Adhesive membranes of egg in five cobitid species of Iksookimia (Pisces: Cobitidae). Korean J. Zool., 39: 419-425.
Sarkar, S.K., Acharya, A., Jana, S. and De, S.K., 2014. Macro-anatomical variation of the olfactory apparatus in some Indian teleosts with special reference to their ecological habitat. Folia Morphol., 73: 122-128. https://doi.org/10.5603/FM.2014.0019
Silva-Junior, D.E. and Zanata, A.M., 2022. A new species of Parotocinclus (Loricariidae: Hypoptopomatinae) from the rio Pardo basin, Bahia State, Brazil, with comments on the sexually dimorphic traits of the nares and olfactory lamellae. J. Fish. Biol., 101: 1582-1590. https://doi.org/10.1111/jfb.15235
Triana-Garcia, P.A., Nevitt, G.A., Pesavento, J.B. and Teh, S.J., 2021. Gross morphology, histology, and ultrastructure of the olfactory rosette of a critically endangered indicator species, the delta smelt, Hypomesus transpacificus. J. comp. Physiol. A, 207: 597-616. https://doi.org/10.1007/s00359-021-01500-7
Tyler, J.C., 1997. New species of Paratriacanthodes spike fish (Triachanthodidae: Tetraodontiformes) from the South China Sea. Proc. biol. Soc. Wash, 110: 310-313.
Zeiske, E., Theisen, B. and Breucker, H., 1992. Structure, development, and evolutionary aspects of the peripheral olfactory system. In: Fish chemoreception (Hara, T.J.), London, UK, Chapman & Hall, pp. 13-39. https://doi.org/10.1007/978-94-011-2332-7_2
Zielinski, B.S. and Hara, T.J., 2006. Olfaction. In: Sensory systems neuroscience (eds. C.J. Brauner and A.P. Farrell), San Diego, California, USA, Elsevier Inc., pp. 1-43. https://doi.org/10.1016/S1546-5098(06)25001-5