Journal Article

Skeletal and muscular pelvic morphology of hillstream loaches (Cypriniformes: Balitoridae)

Crawford, C.H., Randall, Z.S., Hart, P.B., Page, L.M., Chakrabarty, P., Suvarnaraksha, A. and Flammang, B.E.

Record Number:
5093
Year:
2020
Journal:
Journal of Morphology
Pages:
1280-1295
Volume:
281
Abstract:
The rheophilic hillstream loaches (Balitoridae) of South and Southeast Asia possess a range of pelvic girdle morphologies, which may be attributed to adaptations for locomotion against rapidly flowing water. Specifically, the connectivity of the pelvic plate (basipterygium) to the vertebral column via a sacral rib, and the relative size and shape of the sacral rib, fall within a spectrum of three discrete morphotypes: long, narrow rib that meets the basipterygium; thicker, slightly curved rib meeting the basipterygium; and robust crested rib interlocking with the basipterygium. Species in this third category with more robust sacral rib connections between the basipterygium and vertebral column are capable of walking out of water with a tetrapod-like lateral-sequence, diagonal-couplet gait. This behavior has not been observed in species lacking direct skeletal connection between the vertebrae and the pelvis. The phylogenetic positions of the morphotypes were visualized by matching the morphological features onto a novel hypothesis of relationships for the family Balitoridae. The morphotypes determined through skeletal morphology were correlated with patterns observed in the pelvic muscle morphology of these fishes. Transitions towards increasingly robust pelvic girdle attachment were coincident with a more anterior origin on the basipterygium and more lateral insertion of the muscles on the fin rays, along with a reduction of the superficial abductors and adductors with more posterior insertions. These modifications are expected to provide a mechanical advantage for generating force against the ground. Inclusion of the enigmatic cave-adapted balitorid Cryptotora thamicola into the most data-rich balitorid phylogeny reveals its closest relatives, providing insight into the origin of the skeletal connection between the axial skeleton and basipterygium. KEYWORDS computed tomography, fish, musculature, pelvic morphology, phylogeny, walking
Times Cited:
3
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Humboldt, F. H. A. (1805)
IVe Memoire, sur une nouvelle espece de Pimelode, jetee par les volcans du Royaume de Quito
Johnson, R.D.O. (1912)
Notes on the habits of a climbing catfish (Arges marmoratus) from the Republic of Colombia
Collette, B. B. (1962)
Astroblepus pholeter, a new species of cave-dwelling catfish from eastern Ecuador
Chardon, M. (1966)
Specialisation anatomique de l'appareil de Weber d'Astroblepus pholeter, Silure cavernicole microphthalme de la Republique de l'Equateur
Chardon, M. (1968)
Anatomie comparee de l'appareil de Weber et des structures connexes chez les Siluriformes
Balazs, D. (1972)
The Jumandi Caves of Ecuador
Balazs, D. (1974)
The Jumandi Caves of Ecuador
Montoriol-Pons, J. (1976)
[A note on the Jumandi Cave (Archidona, Napo Province)]
Reid, G. McG. (1978)
A sytematic study of labeine cyprinid fishes with particular reference to the comparative morphology, functional morphology and morphometrics of African Labeo species
Sket, B. (1979)
[Fauna in the Caverna de Jumandi]
Brown, P (1981)
Southampton University expedition to Ecuador 1979
Hanson, P. D. (1981)
The aquatic fauna
Brown, P. and Hanson, P.D. (1981)
The Jumandi Cave of Ecuador
Reid, G. McG. (1982)
The form, function and phylogenetic significance of the vomero-palatine organ in Cyprinid fishes
Sandford, M. (1983)
Ervaringen met enkele minder bekende holenvissen
Banister, K.E. (1984)
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Sket, B. (1985)
Bogidiella (s.l.) gammariformis sp. n. (Amphipoda) from Ecuador
Peck, S. B. (1985)
The invertebate fauna of the tropical American caves. Part 6:Jumandi Cave, Ecuador
Waltham, A. C., Brown, R. D. and Middleton, T. C. (1985)
Karst and caves in the Jabal Akhdar, Oman
Kottelat, M. (1988)
Two species of cavefishes from northern Thailand in the genera Nemachilus and Homaloptera (Osteichthyes, Homalopteridae)
Fausel, P. (1990)
Das Sozialverhalten der Hohlenbarbe Garra barreimiae (Cyprinidae, Pisces)
Banister, K.E., Bell, J. and Crumpler, M. (1992)
Omani blind cave fish
Peck, S.B. (1994)
Ecuador
Hanna, S.S. and Al-Belushi, M. (1996)
Introduction to the caves of Oman
Buitrago-Suarez, U.A. and Galvis, G. (1997)
Description of some accessory stuctures of the urogenital system in the neotropical Family Astrobelpidae (Pisces, Siluroidei)
Kottelat, M. (1998)
Homaloptera yuwonoi, a new species of hillstream loach from Borneo, with a new generic name for H. thamicola (Teleostei: Balitoridae)
Feulner, GR (1998)
Wadi fish of the UAE
Romero, A. and Paulson, K.M. (2001)
Humbodt's alleged subterranean fish from Ecuador
Nico, L.G. (2001)
Alexander Von Humboldt (1769-1859): Contributions to knowledge of New World fishes
Deharveng, L. and Bedos, A. (2001)
Thailande
Borowsky, R.L. and Vidthayanon, C. (2001)
Nucleotide diversity in populations of balitorid cave fishes from Thailand
Juberthie, C., Magniez, G., Decu, V. and Povara, I. (2001)
Oman
Schaefer, S.A. and Buitrago-Suarez, U.A. (2002)
Odontode morphology and skin surface features of Andean astroblepid catfishes (Siluriformes, Astroblepidae)
Trajano, E., Mugue, N., Krejca, J., Vidthayanon, C., Smart, D. and Borowsky, R. (2002)
Habitat, distribution, ecology and behaviour of cave balitorids from Thailand (Teleostei: Cypriniformes)
Timmermann, M., Schlupp, I. and Plath, M. (2004)
Shoaling behaviour in a surface-dwelling and cave-dwelling population of a barb Garra barreimiae (Cyprinidae: Teleostei)
Aden, E. (2004)
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Kollmann, H., Sattmann, H. and Seeman, R. (2007)
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Timmermann, M and Plath, M (2009)
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Colli, L., Paglianti, A., Berti, R., Gandolfi, G. and Tagliavini, J. (2009)
Molecular phylogeny of the blind cavefish Phreatichthys andruzzii and Garra barreimiae within the family Cyprinidae
Prokofiev, A.M. (2010)
Morphological classification of loaches (Nemacheilinae)
Schaefer, S.A. and Arroyave, J. (2010)
Rivers as islands: determinants of the distribution of Andean astroblepid catfishes
Aden, E. (2010)
Eye development in the cave fish Garra barreimiae
Soares, D. (2010)
Cavefishes as models for sensory adaptation
Schaefer, S.A., Chakrabarty, P., Geneva, A.J. and Sabaj Pérez, M.H. (2011)
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Kruckenhauser, L., Haring, E., Seeman, R. and Sattmann, H. (2011)
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Haspel, G., Schwartz, A., Streets, A., Camacho, D.E. and Soares, D. (2012)
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Conway, K.W., Lujan, N.K., Lundberg, J.G., Mayden, R.L. et al (2012)
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Brancelj, A., Boonyanusith, C., Watiroyram, S. and Sanoamuang, L. (2013)
The groundwater-dwelling fauna of Southeast Asia
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Lujan, N.K. and Conway, K.W. (2015)
Life in the fast lane: A review of rheophily in freshwater fishes
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García, N., Harrison, I., Cox, N. and Tognelli, M.F. (2015)
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Bagheri, M., Goudarzi, F., Zalaghi, A.H. and Savabieasfahani, M. (2016)
Habitat characteristics and population size of Iranocypris typhlops, the Iran cave barb
Esmaeili, H.R., Sayyadzadeh, G., Coad, B.W. and Eagderi, S. (2016)
Review of the genus Garra Hamilton, 1822 in Iran with description of a new species: a morpho-molecular approach (Teleostei: Cyprinidae)
Lyon, R.G., Geiger, M.F. and Freyhof, J. (2016)
Garra sindhi, a new species from the Jebel Samhan Nature Reserve in Oman (Teleostei: Cyprinidae).
Kirchner, S., Sattmann, H., Plan, L., Krenn, H., Victor, R., Haring, E. and Kruckenhauser, L. (2016)
As above, so below? Testing for gene flow between cave and surface-dwelling populations of Garra barreimiae
Kruckenhauser, L., Reginald, V. and Sattmann, H. (2016)
The fauna of the Al Hoota Cave in Northern Oman
Flammang, B.E., Suvarnaraksha, A., Markiewicz, J. and Soares, D. (2016)
Tetrapod-like pelvic girdle in a walking cavefish
Sherwin, F. (2016)
Wall-climbing cave fish: Evolutionary intermediate?
Zimmer, C. (2016)
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Nebeshwar, K and Vishwanath, W (2017)
On the snout and oromandibular morphology of genus Garra, description of two new species from the Koladyne River basin in Mizoram, India, and redescription of G. manipurensis (Teleostei: Cyprinidae)
Robinson, J., Kopp, J., Finocchiaro, A. and Espinasa, L. (2017)
Astroblepus pholeter: Convergent regressive evolution of the mc1r gene in cavefish species
Esmaeili, H.R., Mehraban, H., Abbasi, K., Keivany, Y. and Coad, B. (2017)
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Espinasa, L., Christoforides, S. and Morfessis, S.E. (2017)
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Sánchez, J., Zurita, M., Schwarz, A., Cárdenas, V.,Bonilla, J., Quilumba, D., ... and Monar, M. (2017)
Guía espeleológica de la Provincia de Napo.
Kirchner, S., Sattmann, H., Haring, E., Plan, L., Victor, R. and Kruckenhauser, L. (2017)
Investigating gene flow between the blind cavefish Garra barreimiae and its conspecific surface populations
Constantin, S., Toulkeridis, T., Moldovan, O.T., Villacís, M. and Addison, A. (2018)
Caves and karst of Ecuador – state of the art and research perspectives
Ellis, M. (2018)
The recorded fauna of the limestone caves of Thailand to April 2018
Pichler, A., Ahnelt, H., Kirchner, S., Sattmann, H., Haring, E., Handschuh, S., Freyhof, J., Victor, R. and Kruckenhauser, L. (2018)
The morphological diversity of Garra barreimiae [Teleostei: Cyprinidae]
Espinasa, L., Robinson, J. and Espinasa, M. (2018)
Mc1r gene in Astroblepus pholeter and Astyanax mexicanus: Convergent regressive evolution of pigmentation across cavefish species
Espinasa, L., Robinson, J., Soares, D., Hoese, G., Toulkeridis, T. and Toomey, R. (2018)
Troglomorphic features of Astroblepus pholeter, a cavefish from Ecuador, and possible introgressive hybridization
Espinasa, L., Hoese, G., Toulkeridis, T. and Toomey, R. (2018)
Corroboration that the Mc1rGly/Ser mutation correlates with the phenotypic expression of pigmentation in Astroblepus
Anonymous (2018)
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Anonymous (2018)
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Anonymous (2018)
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Liew, J.H., Chua, K.W.J., Arsenault, E.R, Thorp, J.H., Suvarnaraksha, A., Amirrudin, A. and Yeo, D.C.J. (2019)
Quantifying terrestrial carbon in freshwater food webs using amino acid isotope analysis: Case study with an endemic cavefish
Conde-Saldan, C.C., Souza Cunha, M., Albornoz-Garzo, J.G., Valiati Barreto, C.A., Ibagon, N., Villa-Navarro, F.A. and Abdala Dergam, J. (2019)
Karyotypic divergence of two co-occurring species of Andean climbing catfishes (Siluriformes: Loricarioidei: Astroblepidae)
Willis, J., Burt de Perera, T., Newport, C., Poncelet, G., Sturr, C.J. and Thomas, A. (2019)
The structure and function of the sucker systems of hill stream loaches
Saemi-Komsari, M., Mousavi-Sabet, H., Sattari, M., Eagderi, S., Vatandoust, S. and Doadrio, I. (2020)
Descriptive osteology of Garra rossica (Nikolskii 1900)
Crawford, C.H., Randall, Z.S., Hart, P.B., Page, L.M., Chakrabarty, P., Suvarnaraksha, A. and Flammang, B.E. (2020)
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Ellis, M. (2020)
The caves of northern Thailand
Ochoa, L.E., Melo, B.F., García-Melo, J.E., Maldonado-Ocampo, J.A., Souza, C.S., Albornoz-Garzón, J.G., Conde-Saldaña, C.C., Villa-Navarro, F., Ortega-Lara, A. and Oliveira, C. (2020)
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Zhongming, Z., Linong, L., Xiaona, Y., Wangqiang, Z. and Wei, L. (2020)
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