Abstract
The inner ear position and structure, related parts of the brain and neurocranium, as well as the morphology of the lapillus, sagitta, and asteriscus, are described in climbing perch, an obligate air-breathing fish capable of terrestrial movements. The olfactory bulbs and telencephalon are well developed. The dorsal protrusion with two symmetrical lobes is observed on the dorsal posterior surface of the telencephalon. The almost triangular rear part of the brain capsule and a narrow posterior region of the neurocranium represent the border of the suprabranchial chamber. The pars superior of the inner ear is located along the internal triangular part of the brain capsule, and both crus communis and ductus semicircularis posterior are located close to each other in the narrow extreme rear region of the brain capsule. The sacculus is enclosed in the large oval bony capsule (saccular swelling), and the sagitta is large with the average otolith length–total body length (TL) ratio equal to 0.06. Linear growth of the lapillus and sagitta is characterized by negative allometry in relation to body length. Despite the slow growth rate of the lapillus, its shape substantially changes during the growth of the fish 36–205 mm TL that, most likely, reflects increasing locomotion complexity. Possible adaptations of climbing perch inner ear to terrestrial movements are discussed.
REFERENCES
Ara, I. and Nabi, M.R., Morphometric and meristic comparison of local and Thai Anabas testudineus, J. Fish., 2018a, vol. 6, no. 2, pp. 599–604. https://doi.org/10.17017/jfish.v6i2.2018.79
Ara, I. and Nabi, M.R., Osteological comparison between local and Thai climbing perch in terms of neurocranium, vertebral column and accessory respiratory organ, Int. J. Fish. Aquat. Stud., 2018b, vol. 6, no. 4, pp. 484–491.
Ari, C., Encephalization and brain organization of mobulid rays (Myliobatiformes, Elasmobranchii) with ecological perspectives, Open Anat. J., 2011, vol. 3, no. 1, pp. 1–13. https://doi.org/10.2174/1877609401103010001
Assis, C.A., The lagenar otoliths of teleosts: Their morphology and its application in species identification, phylogeny and systematics, J. Fish Biol., 2003, vol. 62, no. 6, pp. 1268– 1295. https://doi.org/10.1046/j.1095-8649.2003.00106.x
Assis, C.A., The utricular otoliths, lapilli, of teleosts: Their morphology and relevance for species identification and systematics studies, Sci. Mar., 2005, vol. 69, no. 2, pp. 259– 273.
Bano, F. and Serajuddin, M., Sulcus and outline morphometrics of sagittal otolith variability in freshwater fragmented populations of dwarf gourami Trichogaster lalia (Hamilton, 1822), Limnologica, 2021, vol. 86, 125842. https://doi.org/10.1016/j.limno.2020.125842
Bardhan, I., Roy, S., Mukhopadhyay, A., and Tripathy, B., Ultrastructure of the sagitta otolith in different body size groups of climbing perch Anabas testudineus (Anabantidae), J. Ichthyol., 2021, vol. 61, no. 1, pp. 166–174. https://doi.org/10.1134/S0032945221010033
Barton, R.A., Purvis, A., and Harvey, P.H., Evolutionary radiation of visual and olfactory brain systems in primates, bats and insectivores, Phil. Trans. Res. Soc. London Bull., 1995, vol. 348, no. 1326, pp. 381–392. https://doi.org/10.1098/rstb.1995.0076
Bersa, S., Growth and Bioenergetics of Anabas testudineus (Bloch), an Air Breathing Climbing Perch of South-East Asia, New Delhi: Narendra Publishing House, 1997.
Binoy, V.V., Kasturirangan, R., and Sinha, A., Sensory cues employed for the acquisition of familiarity-dependent recognition of a shoal of conspecifics by climbing perch (Anabas testudineus Bloch), J. Biosci., 2015, vol. 40, pp. 225–232. https://doi.org/10.1007/s12038-015-9529-1
Boyle, R., Ehsanian, R., Mofrad, A., et al., Morphology of the utricular otolith organ in the toadfish, Opsanus tau, J. Comp. Neurol., 2018, vol. 526, no. 6, pp. 1571–1588. https://doi.org/10.1002/cne.24429
Briscoe, S.D. and Ragsdale, S.W., Evolution of the chordate telencephalon, Curr. Biol., 2019, vol. 29, no. 13, pp. R647–R662. https://doi.org/10.1016/j.cub.2019.05.026
Cruz, A. and Lombarte, A., Otolith size and its relationship with color patterns and sound production, J. Fish Biol., 2004, vol. 65, pp. 1512–1525. https://doi.org/10.1111/J.0022-1112.2004.00558.X
Datta, N.C., Saha, A.K., and Das, A., Investigation on the morphology of the olfactory apparatus of Anabas testudineus (Bloch), J. Inland Fish. Soc. India, 1976, vol. 8, pp. 13–18.
Davenport, J. and Abdul Matin, A.K.M., Terrestrial locomotion in the climbing perch, Anabas testudineus (Bloch) (Anabantidea, Pisces), J. Fish Biol., 1990, vol. 37, no. 1, pp. 175–184. https://doi.org/10.1111/j.1095-8649.1990.tb05938.x
de Bruin, J.P.C., Telencephalon and behavior in teleost fish, in Comparative Neurology of the Telencephalon, Ebbesson, S.O.E., Ed., New York: Springer, 1980, pp. 175–201. https://doi.org/10.1007/978-1-4613-2988-6_7
Demski, L.S. and Northcutt, R.G., The brain and cranial nerves of the white shark: An evolutionary perspective, in Great White Sharks: the Biology of Carcharodon carcharias, Klimley, A.P. and Ainley, D.G., Eds., San Diego, CA: Academic Press, 1996, pp. 121–130.
Froese, R. and Pauly, D., Eds., FishBase, World Wide Web Electronic Publication, Version 06/2022. www.fishbase.org.
Gaemers, P.A.M., Taxonomic position of Cichlidae (Pisces, Perciformes) as demonstrated by the morphology of their otoliths, Neth. J. Zool., 1984, vol. 34, no. 4, pp. 566– 595.
Ghanbarifardi, M., Gut, C., Gholami, Z., et al., Possible link between the structure of otoliths and amphibious mode of life of three mudskipper species (Teleostei: Gobioidei) from the Persian Gulf, Zool. Middle East, 2020, vol. 66, no. 4, pp. 311–320. https://doi.org/10.1080/09397140.2020.1805140
Hamdani, E.H. and Døving, K.B, The functional organization of the fish olfactory system, Prog. Neurobiol., 2007, vol. 82, no. 2, pp. 80–86. https://doi.org/10.1016/j.pneurobio.2007.02.007
Hilal, S. and Hilal, F., Morphological variations in the brain of some selected Teleosts, J. Pharm. Innov., 2019, vol. 8, no. 6, pp. 316–320.
Horn, Â.C.M. and Rasia-Filho, A.A., The cytoarchitecture of the telencephalon of Betta splendens Regan 1910 (Perciformes: Anabantoidei) with a stereological approach to the supracommissural and postcommissural nuclei, Anat. Rec., 2018, vol. 301, pp. 88–110. https://doi.org/10.1002/ar.23699
Horodysky, A.Z., Brill, R.W., Fine, M.L., Musick, J.A., and Latour, R.J., Acoustic pressure and particle motion thresholds in six sciaenid fishes, J. Exp. Biol., 2008, vol. 211, pp. 1504–1511.
Huber, R., van Staaden, M.J., Kaufman, L.S., and Liem, K.F., Microhabitat use, trophic patterns and the evolution of brain structure in African cichlids, Brain Behav. Evol., 1997, vol. 50, no 3, pp. 167–182. https://doi.org/10.1159/000113330
Huesa, G., Anadón, R., Folgueira, M., and Yáñez, J., Evolution of the pallium in fishes, in Encyclopedia of Neuroscience, Binder, M.D., Hirokawa, H., and Windhors, U., Eds., Berlin: Springer, 2009, pp. 1400–1404. https://doi.org/10.1007/978-3-540-29678-2_3166
Hussein, M.N. and Cao, X., Brain anatomy and histology in Teleosts, Benha Med. J., 2018, vol. 35, no. 2, pp. 446–463. https://doi.org/10.21608/bvmj.2018.96440
Ito, H., Ishikawa, Y., Yoshimoto, M., and Yamamoto, N., Diversity of brain morphology in Teleosts: Brain and ecological niche, Brain Behav. Evol., 2007, vol. 69, pp. 76–86. https://doi.org/10.1159/000095196
Jaramillo, A.M., Tombari, A.D., Dura, V.B., et al., Otolith eco-morphological patterns of benthic fishes from the coast of Valencia (Spain), Thalassas, 2014, vol. 30, pp. 57–66.
Johansen, K., Air breathing in fishes, in Fish Physiology, Hoar, W.S. and Randell, D.J., Eds., New York: Academic, 1970, vol. IV, pp. 361–411.
Kasumyan, A.O., The vestibular system and sense of equilibrium in fish, J. Ichthyol., 2004, vol. 44, suppl. 2, pp. S224–S268.
Kasumyan, A.O., Structure and function of auditory system in fish, Ibid., 2005, vol. 45, suppl. 2, pp. S223–S270.
Kasumyan, A.O., Sounds and sound production in fishes, Ibid., 2008, vol. 48, pp. 981–1030. https://doi.org/10.1134/S0032945208110039
Kasumyan, A.O. and Mikhailova, E.S., Sound producing in the three-spot gourami Trichopodus trichopterus (Osphronemidae) during feeding, Ibid., 2022, vol. 62, pp. 968–976. https://doi.org/10.1134/S003294522205006X
Kasumyan, A.O., Pashchenko, N.I., and Oanh, L.T., Morphology of the olfactory organ in the climbing perch (Anabas testudineus, Anabantidae, Perciformes), Biol. Bull. Russ. Acad. Sci., 2021, vol. 48, pp. 1298–1313. https://doi.org/10.1134/S1062359021080148
Kiyohara, S., Sakata, Y., Yoshitomi, T., and Tsukahara, J., The ‘goatee’ of goatfish: Innervation of taste buds in the barbels and their representation in the brain, Proc. Biol. Sci., 2002, vol. 269, pp. 1773–1780. https://doi.org/10.1098/rspb.2002.2086
Kumar, K., Lalrinsanga, P., Sahoo, M., et al., Length-weight relationship and condition factor of Anabas testudineus and channa species under different culture systems, World J. Fish Mar. Sci., 2013, vol. 5, no. 1, pp. 74–78. https://doi.org/10.5829/idosi.wjfms.2013.05.01.64201
Ladich, F. and Popper, A.N., Comparison of the inner ear ultrastructure between teleost fishes using different channels for communication, Hear Res., 2001, vol. 154, no. 1–2, pp. 62–72. https://doi.org/10.1016/S0378-5955(01)00217-9
Ladich, F. and Schulz-Mirbach, T., Diversity in fish auditory systems: One of the riddles of sensory biology, Front. Ecol. Evol., 2016, vol. 4, art. ID 28. https://doi.org/10.3389/fevo.2016.00028
Ladich, F., Bischof, C., Schleinzer, G., and Fuchs, A., Intra- and interspecific differences in agonistic vocalizations in croaking gouramis (genus: Trichopsis, Anabantoidei, Teleostei), Bioacoustics, 1992, vol. 4, pp. 131–141. https://doi.org/10.1080/09524622.1992.9753212
Lastein, S., Hamdani, A.H., and Døving K.B., Olfactory discrimination of pheromones, in Fish Pheromones and Related Cues, Sorensen, P.W. and Wisenden, B.D., Eds., Oxford: John Wiley and Sons, Inc., 2015, pp. 159–195. https://doi.org/10.1002/9781118794739.ch8
Liem, K.F., The Comparative Osteology and Phylogeny of the Anabantoidei (Teleostei, Pisces), Urbana: Univ. of Illinois, 1963. https://doi.org/10.5962/bhl.title.50281
Liem, K.F., Functional design of the air ventilation apparatus and overland excursions by teleosts, Fieldiana, Zoology, New Ser., 1987, vol. 37, pp. 1–29.
Lin, C.-H. and Chang, C.-W., Otolith Atlas of Taiwan Fishes, NMMBA Atlas Series, vol. 12, Pingtung: Natl. Mus. Mar. Biol. Aquarium, 2012.
Lychakov, D.V., Otoliths in cyclostomates and fishes: Evolution and some quantitative rations, Sens. Syst., 1994, vol. 8, no. 3–4, pp. 7–15.
Mahé, K., Ider, D., Massaro, A., et al., Directional bilateral asymmetry in otolith morphology may affect fish stock discrimination based on otolith shape analysis, ICES J. Mar. Sci., 2019, vol. 76, pp. 232–243. https://doi.org/10.1093/icesjms/fsy163
Mahé, K., MacKenzie, K., Ider, D., et al., Directional bilateral asymmetry in fish otolith: A potential tool to evaluate stock boundaries?, Symmetry, 2021, vol. 13, Article 987. https://doi.org/10.3390/sym13060987
Makeyeva, A.P., Embriologiya ryb (Embryology of Fishes), Moscow: Mosk. Gos. Univ., 1992.
Mawa, Z., Hossain, M.Y., Hasan, M.R., and Asaduzzaman, M., Reproductive aspects of Anabas testudineus collected from the Gajner Beel wetland in Bangladesh: Implications for its conservation under changing eco-climatic conditions and suggestions for best aquaculture practice, Environ. Sci. Pollut. Res. Int., 2022, vol. 29, no. 44, pp. 66277–66294. https://doi.org/10.1007/s11356-022-20423-7
Mille, T., Mahe, K., Villanueva, M.C., et al., Sagittal otolith morphogenesis asymmetry in marine fishes, J. Fish Biol., 2015, vol. 87, no. 3, pp. 646–663. https://doi.org/10.1111/jfb.12746
Nieuwenhuys, R., The forebrain of actinopterygians revisited, Brain, Behav. Evol., 2009, vol. 73, no. 4, pp. 229–252. https://doi.org/10.1159/000225622
Nikonorov, S.I., Perednii mozg i povedenie ryb (Forebrain and Fish Behavior), Moscow: Nauka, 1982.
Palmer, A.R., Fluctuating asymmetry analyses: A primer, in Developmental Instability: Its Origins and Evolutionary Implications, Markow, T.A., Ed., Dordrecht: Springer-Verlag, 1994, pp. 335–364.
Palmer, A.R. and Strobeck, C., Fluctuating asymmetry: measurement, analysis, patterns, Ann. Rev. Ecol. Syst., 1986, vol. 17, pp. 391–421. https://doi.org/10.1146/ANNUREV.ES.17.110186.002135
Palmer, M., Linde, M., and Morales-Nin, B., Disentangling fluctuating asymmetry from otolith shape, Mar. Ecol. Prog. Ser., 2010, vol. 399, pp. 261–272.
Pavlov, D.A., Otolith morphology and relationships of several fish species of the suborder Scorpaenoidei, J. Ichthyol., 2021, vol. 61, no. 1, pp. 33–47. https://doi.org/10.1134/S0032945221010100
Pavlov, D.A., Feeding-related skull structures of climbing perch Anabas testudineus (Anabantidae), Ibid., 2023, vol. 63, no. 4, pp. 788–796. https://doi.org/10.1134/S0032945223040148
Pavlov, E.D., Movements of climbing perch Anabas testudineus out of the water, 2021. https://disk.yandex.ru/i/T2OL5xXp_EA92Q.
Pavlov, E.D., Pavlov, D.S., Ganzha, E.V., Sharova, M.M., and Tran Duc Dien, Effect of thiourea on behavior of climbing perch Anabas testudineus in water flow, J. Ichthyol., 2018, vol. 58, pp. 710–716. https://doi.org/10.1134/S0032945218050168
Pavlov, E.D., Pavlov, D.S., Ganzha, E.V., et al., Influence of water level on the exit of climbing perch Anabas testudineus out of the water and specific features of its movements, Ibid., 2021, vol. 61, pp. 752–757. https://doi.org/10.1134/S003294522105012X
Popper, A.N. and Fay, R.R., Rethinking sound detection by fishes, Hear. Res., 2011, vol. 273, nos. 1–2, pp. 25–36. https://doi.org/10.1016/j.heares.2009.12.023
Popper, A.N., Fay, R.R., Platt, C., and Sand, O., Sound detection mechanisms and capabilities of teleost fishes, in Sensory Processing in Aquatic Environments, Collin, S.P. and Marshall, N.J., Eds., New York: Springer-Verlag, 2003, pp. 3–38.
Popper, A.N., Ramcharitar, J., and Campana, S.E., Why otoliths? Insights from inner ear physiology and fisheries biology, Mar. Freshwater Res., 2005, vol. 56, no. 5, pp. 497–504. https://doi.org/10.1071/MF04267
Priyatha, C.V. and Chitra, K.C., Evaluation of the reproductive cycle and gonadal development in the climbing perch, Anabas testudineus (Bloch, 1792) in captivity, J. Fish., 2022, vol. 10, no. 1, Article 101206. https://doi.org/10.17017/j.fish.364
Putland, R.L., Montgomery, J.C., and Radford, C.A., Ecology of fish hearing, J. Fish. Biol., 2019, vol. 95, no. 1, pp. 39–52. https://doi.org/10.1111/jfb.13867
Rahmani, A.R. and Khan, S.M., The olfactory organ in a few Indian teleosts, Curr. Sci., 1981, vol. 50, no. 7, pp. 329–331. http://www.jstor.org/stable/24085788
Ramcharitar, J.U., Deng, X., Ketten, D., and Popper, A.N., Form and function in the unique inner ear of a teleost: The silver perch (Bairdiella chrysoura), J. Comp. Neurol., 2004, vol. 475, pp. 531–539. https://doi.org/10.1002/cne.20192
Ramcharitar, J.U., Dennis, M., Higgs, D.M., and Popper, A.N., Audition in sciaenid fishes with different swim bladder-inner ear configurations, J. Acoust. Soc. Am., 2006, vol. 119, pp. 439–443. https://doi.org/10.1121/1.2139068
Samoilov, K.Yu. and Tran Duc Dien, Morphological plasticity and biological patterns of the climbing perch Anabas testudineus from different types of water bodies in Khánh Hòa Province, Vietnam, Inland Water Biol., 2022, vol. 15, no. 3, pp. 217–226. https://doi.org/10.1134/S1995082922020109
Satou, M., Synaptic organization of the olfactory bulb and its central projection, in Fish Chemoreception, Hara, T.J., Ed., London: Chapman and Hall, 1992, pp. 40–59.
Schneider, H., Die Bedeutung der Atemhöhle der Labyrinthfische für ihr Hörvermögen, Z. Vergl. Physiol., 1942, vol. 29, pp. 172–194. https://doi.org/10.1007/BF00304447
Schroeder, D.M., The telencephalon of Teleosts, in Comparative Neurology of the Telencephalon, Ebbesson S.O.E., Ed., New York: Plenum Press, 1980, pp. 99–115.
Schulz-Mirbach, T., Ladich, F., Riesch, R., and Plath, M., Otolith morphology and hearing abilities in cave- and surface-dwelling ecotypes of the Atlantic molly, Poecilia mexicana (Teleostei: Poeciliidae), Hear. Res., 2010, vol. 267, no. 1, pp. 137–148. https://doi.org/10.1016/j.heares.2010.04.001
Schulz-Mirbach, T., Ladich, F., Plath, M., Metscher, B.D., and Heß, M., Are accessory hearing structures linked to inner ear morphology? Insights from 3D orientation patterns of ciliary bundles in three cichlid species, Front. Zool., 2014, vol. 11, Article ID 25. https://doi.org/10.1186/1742-9994-11-25
Secor, D.H., Dean, J.M., and Laban, E.H., Manual for Otolith Removal and Preparation for Microstructural Examination, Washington, DC: Electr. Power Res. Inst., 1991.
Seshagiri, B.V. and Raju, K.V., Validity of Anabas oligolepis Bleeker, 1855 and Coius cobojius Hamilton-Buchanan, 1822 a junior synonym of A. testudineus (Bloch, 1795) (Osteichthyes: Anabantidae), J. Aqua. Biol., 2001, vol. 16, no. 2, pp. 29–31.
Srinu, G., Padmavathi, P., and Chatla, D., Identification and validation of Anabas spp. (Osteichthyes: Anabantidae) through morphology and DNA barcoding from Lake Kolleru, Andhra Pradesh, India, J. Coast. Res., Special Issue, 2019, no. 86, pp. 142–148. https://doi.org/10.2112/SI86-022.1
Talwar, P.K. and Jhingran A.G., Inland Fishes of India and Adjacent Countries, Rotterdam: A.A. Balkema, 1991, vol. 2.
Urick, R.J., Principles of Underwater Sound, New York: McGraw-Hill Inc., 1983.
Van Valen, L., A study of fluctuating asymmetry, Evolution, 1962, vol. 16, no. 2, pp. 125–142. https://doi.org/10.1111/j.1558-5646.1962.tb03206.x
Vinogradskaya, M.I., Mikhailova, E.S., and Kasumyan, A.O., Taste preferences, orosensory food testing, and sound production during feeding by the pearl gourami Trichopodus leerii (Osphronemidae), J. Ichthyol., 2017, vol. 57, no 3, pp. 445–457. https://doi.org/10.1134/S0032945217030122
Zakharov, V.M., Asimmetriya zhivotnykh (populyatsionno-fenogeneticheskii podkhod) (Animal Asymmetry: Population–Phenogenetic Approach), Moscow: Nauka, 1987.
Zworykin, D.D., Are terrestrial movements of amphibious fish lateral migrations?, Biol. Bull. Rev., 2021, vol. 11, no. 5, pp. 520–532. https://doi.org/10.1134/S2079086421050091
ACKNOWLEDGMENTS
We thank L.T.K. Oanh (Coastal Branch of Joint Russia-Vietnam Tropical Science and Technology Research Center, Nha Trang, Vietnam) for help with fish collection. We thank three anonymous reviewers for their valuable comments on the manuscript.
Funding
The study was conducted according to the scientific project of the State target of Moscow State University (CITIS no. 121032300100-5) and was funded by the Russia-Vietnam Tropical Science and Technology Research Center, the project “Ecolan E3.2, task 2”.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
ETHICS APPROVAL AND CONSENT TO PARTICIPATE
The study was conducted in accordance with the Federal Law No. 498-FZ (December 27, 2018) (amended on July 24, 2023) “On responsible treatment of animals and amendments to certain legislative acts of the Russian Federation”. All applicable international guidelines for the care and use of animals were followed (http://oacu.od.nih.gov/regs/index.htm).
CONFLICT OF INTEREST
The authors of this work declare that they have no conflicts of interest.
Additional information
Publisher’s Note.
Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pavlov, D.A., Kasumyan, A.O. Inner Ear and Otolith Morphology of Climbing Perch Anabas testudineus (Anabantidae). J. Ichthyol. 64, 16–29 (2024). https://doi.org/10.1134/S0032945224010090
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0032945224010090