Spawning Behaviour and the Softmouth Trout Dilemma

Open access

Abstract

Morphological, ecological and molecular data sets do not completely agree on the phylogenetic placement of the softmouth trout, Salmo (Salmothymus) obtusirostris (Heckel). Molecules posit that softmouths are closely related to brown trout, Salmo trutta L. while some morphological, ecological and life history traits place them in the most basal position of the Salmoninae subfamily between grayling (Thymallus) and lenok (Brachymystax). Here we add an additional source of data, behavioural characters based on the first reported observations of softmouth spawning. During spawning softmouth females present three important behaviours not found in the other Salmo members: they continually abandon their nests, rarely staying on them for periods over nine minutes; they expel different batches of eggs at the same nest at intervals of several minutes; and they do not cover their eggs immediately after spawning. These three behaviours are intriguing for two reasons: 1) they are possible homologous to behaviours found in grayling females; 2) when coupled to the nest digging behaviour-widespread in all the salmonines, including softmouths, they seem to be mal-adaptive.

Abstract

Morphological, ecological and molecular data sets do not completely agree on the phylogenetic placement of the softmouth trout, Salmo (Salmothymus) obtusirostris (Heckel). Molecules posit that softmouths are closely related to brown trout, Salmo trutta L. while some morphological, ecological and life history traits place them in the most basal position of the Salmoninae subfamily between grayling (Thymallus) and lenok (Brachymystax). Here we add an additional source of data, behavioural characters based on the first reported observations of softmouth spawning. During spawning softmouth females present three important behaviours not found in the other Salmo members: they continually abandon their nests, rarely staying on them for periods over nine minutes; they expel different batches of eggs at the same nest at intervals of several minutes; and they do not cover their eggs immediately after spawning. These three behaviours are intriguing for two reasons: 1) they are possible homologous to behaviours found in grayling females; 2) when coupled to the nest digging behaviour-widespread in all the salmonines, including softmouths, they seem to be mal-adaptive.

References

  • Beauchamp D.A. 1990 - Movements, habitat use, and spawning strategies of Arctic grayling in a subalpine lake tributary - Northwest Sci. 64: 195-207.

  • Behnke R.J. 1968 - A new subgenus and species of trout, Salmo (Platysalmo) platycephalus, from southcentral Turkey, with comments on the classification of the subfamily Salmoninae - Mitt Hamburg Zool Mus Inst. 66: 1-15.

  • Berg L.S. 1908 - Vorläufige Bemerkungen über die europäi-schasiatischen Salmoninen, insbesondere die Gattung Thymallus - Ann. Mus. Zool, Acad. Sei. St. Petersbourg, 12: 500-514.

  • Crespi B.J., Fulton M. 2004 - Molecular systematics of Salmonidae: combined nuclear data yields a robust phy-logeny - Mol. Phylo. Evol. 31:658-679.

  • Crĉte-Lafrenière A., Weir L.K., Bernatchez L. 2012 - Framing the Salmonidae Family Phylogenetic Portrait: A More

  • Complete Picture from Increased Taxon Sampling - PLoS ONE 7(10): e46662. doi:10.1371/journal.pone.0046662.

  • Darchambeau F., Poncin P. 1997 - Field observations of the spawning behaviour of European grayling - J. Fish Biol. 51: 1066-1068.

  • Esteve M. 2005 - Observations of spawning behaviour in Salmoninae: Salmo, Oncorhynchus and Salvelinus - Rev. Fish Biol. Fish. 15: 1-21.

  • Esteve M., McLennan D.A., Kawahara M. 2011 - Spawning behaviour of amemasu charr, Salvelinus leucomaenis leucomaenis, with a discussion of the macroevolutionary patterns of post-spawning behaviour in the Salmoninae - Ecol. Freshw. Fish. 20: 364-370.

  • Evans D.M. 1994 - Observations on the spawning behaviour of male and female adult sea trout, Salmo trutta L., using radiotelemetry - Fish. Manage. Ecol. 1: 91-105.

  • Fabricius E., Gustafson K.J. 1955 - Observations on the spawning behaviour of the grayling, Thymallus thymallus (L.) - Report of the Institute of Freshwater Research, Drottningholm 36: 75-103.

  • Fleming I.A. 1996 - Reproductive strategies of Atlantic salmon: ecology and evolution - Rev. Fish Biol. Fish. 6: 379-416.

  • Georgiev S.B. 2003 - On the origin of the Balkan Peninsula Salmonids - Ribarstvo 61: 147-174.

  • Groot C. 1996 - Salmonid life histories - In: Principles of Salmonid Culture (Eds.) W. Pennell, A. Bruce, Elsevier, Amsterdam, 97-230.

  • Hadžišče S. 1961 - Zur Kenntnis des Salmothymus ohridanus (Steindachner) (Pisces, Salmonidae) - Internationale Vereinigung für theoretische und angewandte Limnologie Verhandlungen 14: 785-791.

  • Heckel J.J. 1851 - Bericht einer ichthyologischen Reise. II -Beiträge zu den Gattungen Salmo, Fario, Salar, Coregonus, Chondrostoma und Telestes - Sitzungsber. Akad. Wiss. Wien, 347-390.

  • Karaman S. 1927 - Les salmonidés des Balkans. Bull. Soc. Sci. Skoplje - 2: 253-268.

  • Mrdak D., Nikolić V., Tošić A., Simonović P. 2012 - Molecular and ecological features of the soft-muzzled trout Salmo obtusirostris (Heckel, 1852) in the Zeta River, Montenegro - Biologia 67: 222-233.

  • Quinn T.P. 2005 - The Behavior and Ecology of Pacific Salmon and Trout - Univ. Washington Press, Seattle, WA, 328 p.

  • Razpet A., Sušnik S., Jug T., Snoj A. 2007 - Genetic variation among trout in the River Neretva basin, Bosnia and Herzegovina - J. Fish Biol. 70 (Suppl. A): 94-110.

  • Sanford C.P.J. 2000 - Salmonid fish osteology and phylogeny (Teleostei: Salmonoidei) - Theses Zoologicae, Koeltz Scientific Books, 264 p.

  • Scribner K.T., Page K.S., Bartron M.L. 2000 - Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference - Rev. Fish Biol. Fish. 10: 293-323.

  • Snoj A., Melkič E., Sušnik S., Muhamedagić S., Dovč P. 2002 - DNA phylogeny supports revised classification of Salmothymus obtusirostris - Biol. J. Linn. Soc. 77: 399-411.

  • Snoj A., Bogut I., Sušnik S. 2008 - Evidence of a genetically distinct population of Vrljika softmouth trout Salmo obtusirostris Heckel evolved by vicariance - J. Fish Biol. 72: 1945-1959.

  • Stearley R.F., Smith G.R. 1993 - Phylogeny of the pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae - Trans. Am. Fish. Soc. 122: 1-33.

  • Steindachner F. 1874 - Beschreibung einer neuen Art und Gattung aus der Familie der Pleuronectiden und einer neuen Thymallus-Art vor - Anzeiger der Akademie der Wissenschoften. Wien, 11: 171-172.

  • Steindachner F. 1882 - Ichthyologische Beiträge (XII) -Sitzungsberrichte der Akademie der Wissenschoften, Wien, 61-82.

  • Sušnik S., Knizhin I., Snoj A., Weiss S. 2006 - Genetic and morphological characterization of a Lake Ohrid endemic, Salmo (Acantholingua) ohridanus with a comparison to sympatric Salmo trutta - J. Fish Biol. 68: 2-23.

  • Sušnik S., Weiss S., Odak T., Delling B., Treer T., Snoj A. 2007 - Reticulate evolution: ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae) - Biol. J. Linn. Soc. 90: 139-152.

  • Tautz A.F. Groot C. 1975 - Spawning behavior of chum salmon (Oncorhynchus keta) and rainbow trout (Salmo gairdneri) - J. Fish. Res. Board Can. 32: 633-642.

  • Taylor E.B. 2004 - Evolution in mixed company - In: Salmon and their Relatives (Eds) A.P. Hendry, S.C. Stearns, Evolution Illuminated, Oxford University Press, Oxford, 232-263.

  • Vuković T., Ivanović B. 1971 - Slatkovodne ribe Jugoslavije -Zemaljski muzej BiH, Sarajevo, 268 p.

  • Wilson M.V.H., Li G-Q. 1999 - Osteology and systematic position of the Eocene salmonid Eosalmo driftwoodensis Wilson from western North America - Zool. J. Linn. Soc. 125: 279-311.

  • Wilson M.V.H. Williams R.R.G. 2010 - Salmoniform fishes: key fossils, supertree, and possible morphological synapomorphies - In: Origin and phylogenetic interrelationships of Teleosts (Eds) J.S. Nelson, H.P. Schultze, M.V.H. Wilson, Verlag Dr. Friedrich Pfeil, München, Germany: 379-409.

Beauchamp D.A. 1990 - Movements, habitat use, and spawning strategies of Arctic grayling in a subalpine lake tributary - Northwest Sci. 64: 195-207.

Behnke R.J. 1968 - A new subgenus and species of trout, Salmo (Platysalmo) platycephalus, from southcentral Turkey, with comments on the classification of the subfamily Salmoninae - Mitt Hamburg Zool Mus Inst. 66: 1-15.

Berg L.S. 1908 - Vorläufige Bemerkungen über die europäi-schasiatischen Salmoninen, insbesondere die Gattung Thymallus - Ann. Mus. Zool, Acad. Sei. St. Petersbourg, 12: 500-514.

Crespi B.J., Fulton M. 2004 - Molecular systematics of Salmonidae: combined nuclear data yields a robust phy-logeny - Mol. Phylo. Evol. 31:658-679.

Crĉte-Lafrenière A., Weir L.K., Bernatchez L. 2012 - Framing the Salmonidae Family Phylogenetic Portrait: A More

Complete Picture from Increased Taxon Sampling - PLoS ONE 7(10): e46662. doi:10.1371/journal.pone.0046662.

Darchambeau F., Poncin P. 1997 - Field observations of the spawning behaviour of European grayling - J. Fish Biol. 51: 1066-1068.

Esteve M. 2005 - Observations of spawning behaviour in Salmoninae: Salmo, Oncorhynchus and Salvelinus - Rev. Fish Biol. Fish. 15: 1-21.

Esteve M., McLennan D.A., Kawahara M. 2011 - Spawning behaviour of amemasu charr, Salvelinus leucomaenis leucomaenis, with a discussion of the macroevolutionary patterns of post-spawning behaviour in the Salmoninae - Ecol. Freshw. Fish. 20: 364-370.

Evans D.M. 1994 - Observations on the spawning behaviour of male and female adult sea trout, Salmo trutta L., using radiotelemetry - Fish. Manage. Ecol. 1: 91-105.

Fabricius E., Gustafson K.J. 1955 - Observations on the spawning behaviour of the grayling, Thymallus thymallus (L.) - Report of the Institute of Freshwater Research, Drottningholm 36: 75-103.

Fleming I.A. 1996 - Reproductive strategies of Atlantic salmon: ecology and evolution - Rev. Fish Biol. Fish. 6: 379-416.

Georgiev S.B. 2003 - On the origin of the Balkan Peninsula Salmonids - Ribarstvo 61: 147-174.

Groot C. 1996 - Salmonid life histories - In: Principles of Salmonid Culture (Eds.) W. Pennell, A. Bruce, Elsevier, Amsterdam, 97-230.

Hadžišče S. 1961 - Zur Kenntnis des Salmothymus ohridanus (Steindachner) (Pisces, Salmonidae) - Internationale Vereinigung für theoretische und angewandte Limnologie Verhandlungen 14: 785-791.

Heckel J.J. 1851 - Bericht einer ichthyologischen Reise. II -Beiträge zu den Gattungen Salmo, Fario, Salar, Coregonus, Chondrostoma und Telestes - Sitzungsber. Akad. Wiss. Wien, 347-390.

Karaman S. 1927 - Les salmonidés des Balkans. Bull. Soc. Sci. Skoplje - 2: 253-268.

Mrdak D., Nikolić V., Tošić A., Simonović P. 2012 - Molecular and ecological features of the soft-muzzled trout Salmo obtusirostris (Heckel, 1852) in the Zeta River, Montenegro - Biologia 67: 222-233.

Quinn T.P. 2005 - The Behavior and Ecology of Pacific Salmon and Trout - Univ. Washington Press, Seattle, WA, 328 p.

Razpet A., Sušnik S., Jug T., Snoj A. 2007 - Genetic variation among trout in the River Neretva basin, Bosnia and Herzegovina - J. Fish Biol. 70 (Suppl. A): 94-110.

Sanford C.P.J. 2000 - Salmonid fish osteology and phylogeny (Teleostei: Salmonoidei) - Theses Zoologicae, Koeltz Scientific Books, 264 p.

Scribner K.T., Page K.S., Bartron M.L. 2000 - Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference - Rev. Fish Biol. Fish. 10: 293-323.

Snoj A., Melkič E., Sušnik S., Muhamedagić S., Dovč P. 2002 - DNA phylogeny supports revised classification of Salmothymus obtusirostris - Biol. J. Linn. Soc. 77: 399-411.

Snoj A., Bogut I., Sušnik S. 2008 - Evidence of a genetically distinct population of Vrljika softmouth trout Salmo obtusirostris Heckel evolved by vicariance - J. Fish Biol. 72: 1945-1959.

Stearley R.F., Smith G.R. 1993 - Phylogeny of the pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae - Trans. Am. Fish. Soc. 122: 1-33.

Steindachner F. 1874 - Beschreibung einer neuen Art und Gattung aus der Familie der Pleuronectiden und einer neuen Thymallus-Art vor - Anzeiger der Akademie der Wissenschoften. Wien, 11: 171-172.

Steindachner F. 1882 - Ichthyologische Beiträge (XII) -Sitzungsberrichte der Akademie der Wissenschoften, Wien, 61-82.

Sušnik S., Knizhin I., Snoj A., Weiss S. 2006 - Genetic and morphological characterization of a Lake Ohrid endemic, Salmo (Acantholingua) ohridanus with a comparison to sympatric Salmo trutta - J. Fish Biol. 68: 2-23.

Sušnik S., Weiss S., Odak T., Delling B., Treer T., Snoj A. 2007 - Reticulate evolution: ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae) - Biol. J. Linn. Soc. 90: 139-152.

Tautz A.F. Groot C. 1975 - Spawning behavior of chum salmon (Oncorhynchus keta) and rainbow trout (Salmo gairdneri) - J. Fish. Res. Board Can. 32: 633-642.

Taylor E.B. 2004 - Evolution in mixed company - In: Salmon and their Relatives (Eds) A.P. Hendry, S.C. Stearns, Evolution Illuminated, Oxford University Press, Oxford, 232-263.

Vuković T., Ivanović B. 1971 - Slatkovodne ribe Jugoslavije -Zemaljski muzej BiH, Sarajevo, 268 p.

Wilson M.V.H., Li G-Q. 1999 - Osteology and systematic position of the Eocene salmonid Eosalmo driftwoodensis Wilson from western North America - Zool. J. Linn. Soc. 125: 279-311.

Wilson M.V.H. Williams R.R.G. 2010 - Salmoniform fishes: key fossils, supertree, and possible morphological synapomorphies - In: Origin and phylogenetic interrelationships of Teleosts (Eds) J.S. Nelson, H.P. Schultze, M.V.H. Wilson, Verlag Dr. Friedrich Pfeil, München, Germany: 379-409.

Fisheries & Aquatic Life

The Journal of Stanislaw Sakowicz Inland Fisheries Institute

Journal Information


CiteScore 2017: 0.53

SCImago Journal Rank (SJR) 2017: 0.204
Source Normalized Impact per Paper (SNIP) 2017: 0.493

Cited By

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 132 132 13
PDF Downloads 45 45 2