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Marble trout
Description and distribution
Marble trout (Salmo marmoratus), characterized by distinctive marbled color pattern and high growth capacity, inhabits some rivers and streams flowing into the Adriatic Sea, i.e. in Italy the Rivers Adige, Brenta, Piave, Livenza, Tagliamento, Natisone and the upper reaches of the Po river system, in Slovenia the Soča river system and the Rivers Rižana and Reka, in Bosnia - Herzegovina and Croatia the Neretva river system, and in Montenegro the Skadar river system.
>Juvenile marble trout from the River Zeta (Montenegro) has yet to develop the distinctive color pattern
Marble trout used to live in the River Krka in Croatia and in some Adriatic Rivers in Albania, where it is apparently extinct.
> Distribution area of marble trout
Natural co-existence with other trout
Most of the existing marble trout populations naturally coexist with native Adriatic brown trout: Salmo cenerinus in Italian rivers and S. farioides and S. obtusirostris in the Neretva and Skadar river systems. It is believed that in Slovenia, marble trout used to be the only naturally present trout until the introduction of non-native brown trout. However, some genetic traces of the Adriatic lineage of brown trout were found in the rivers Rižana and Učja (a direct tributary to the Soča River), which contradicts this notion.
Classification on the basis of mitochondrial DNA
All northern populations of marble trout (from Italy and Slovenia) exhibit marmoratus mtDNA haplotypes (Ma haplotypes), which were initially associated with the marmoratus evolutionary lineage, representing one of five major phylogroups of Salmo trutta complex, the distribution of which corresponds well with major river basins in Europe (see Bernatchez et al., 1992; Bernatchez, 2001 or Snoj et al., 2000, for details about trout evolutionary lineages). However, subsequent studies have shown that south marbled trout populations (from Bosnia-Herzegovina, Croatia and Montenegro) bear Adriatic brown trout haplotypes rather than the expected marmoratus haplotype (Snoj et al., 2010). Marmoratus haplotypes were, on the other hand, found also in native brown trout in several locations across Mediterranean basin (i.e., in Croatia, Albania, Greece, Corsica and central Italy; Splendiani et al., 2006; Snoj et al., 2009; BTRG's observations).
> Native range of marble trout according to early researchers and present day distribution of mtDNA of marmoratus lineage (left;  marble trout described by early researchers,  mtDNA of marmoratus lineage found). Present distribution of trout with marbled color pattern (right;  8 genetically pure marble trout populations,  marble trout x brown trout hybrids,  stocked marble trout,  marbled brown trout from the River Otra).
Interestingly, even a Scandinavian brown trout of the Otra River in Norway (Skaala & Solberg, 1997), which belong to the Atlantic evolutionary lineage, were found to express marbled color pattern, although genetic markers and phenotypic characters of these trout are not similar to those characteristic of the Adriatic marble trout (Delling, 2002).
> Marmorated brown trout from the Otra River, Norway. (photo by Øystein Skaala)
It is thus evident that:
- marmoratus haplotypes are not associated with marble trout.
- mtDNA analysis is not phylogenetically informative for assessing marble and brown trout relationship.
- in the case of marble trout, classification based on mtDNA cannot be conclusive.
Taxonomic status
To clarify taxonomic uncertainties of marble trout (S. marmoratus or S. trutta marmoratus) and determine phylogenetic relationship between the northern and southern populations, a new marker system based on nDNA SNPs was developed (Pustovrh et al., 2012). Using this approach, we found out that north and south populations of marble trout stemmed from a common ancestor and that the marble trout is with high statistic support recognized as a real natural unit of the same rank as brown trout (Pustovrh et al., 2011, 2014); so, according to phylogenetic species concept, marble trout can be recognized as an independent species.
> Molecular phylogeny of Salmo of the western Balkans, based upon multiple nuclear loci (Pustovrh et al., 2014).
Translocations
Several records of marble trout translocation out of its natural range have been reported in the past. For instance, according to unverified information, in Slovenia marble trout have been translocated into many rivers of the Sava catchment area in order to increase the size of native brown trout. And indeed, using molecular genetic analysis, we observed genetic traces of marble trout there (e.g., in the Rivers Krka and Cerkniščica; Jug et al., 2005) and confirmed rumors about marble trout translocations.
A threat of brown trout
Marble trout is one of the most endangered freshwater species. The main threat to marble trout has been hybridization with introduced brown trout. The first recorded stocking in the Soča River was performed in 1906 using brown trout from Bosnia-Herzegovina. Contrary to the popular believe of critical devastation of marble trout during the WWl, marble trout was still abundant in the Soča after the war (Gridelli, 1936; Razpet et al., 2007), however the stocking with brown trout, presumably originating from the Atlantic river basin, continued and reached its peak in the time of Yugoslavia. In late eighties of the previous century, non native brown trout of the Atlantic origin and its hybrids with the native marble trout dominated almost the entire Adriatic part of Slovenian river system (Povž et al., 1996).
> Genetic mixing causes a hybrid swarm with many diversified phenotypes.
Research
To counteract the collapse of marble trout, its investigation in Slovenia was initiated in early nineties started by French researchers Dr. Alain Crivelli and Dr. Patrick Berrebi in a close collaboration with Dušan Jesenšek (Angling Club of Tolmin) and Dr. Meta Povž from Fisheries Research Institute of Slovenia. BTRG joint them a bit later.
The first output of this collaboration was "ACTION PLAN for Marble Trout", a detailed plan outlining actions for marble trout saving, published in 1996.
> This book was published also in Slovenian; both versions were sold out very quickly.
Genetically "pure" populations
The most important milestone in marble trout investigation was a discovery of eight genetically pure marble trout populations, confined to the very upper reaches of small tributaries, and isolated with high waterfalls from downstream hybridization area.
> Genetically pure population of marble trout in Slovenia. 1-Predelica (destroyed by landslide), 2-Zadlaščica, 3-Lipovšček, 4-Huda grapa, 5-Studenc, 6-Sevnica, 7-Idrijca, 8-Trebuščica.
Conservation actions and measures
As revealed later, all of these populations had a very small effective population size and extremely low genetic diversity and exhibited a very high inter-population genetic polymorphism (Fumagalli et al., 2002). Nevertheless, these populations represented the first basis for marble trout restoration. The main idea was to create genitor stocks based on the eight genetically pure populations of marble trout, and use their progeny for stocking the Soča river system in order to eventually replace brown trout non-native genes with the marble trout ones and slowly regain the situation characteristic of the Soča river system before brown trout introduction. Simultaneously, brown trout stocking has been ceased making rehabilitation of marble trout a realistic goal in the next decades (Povž et al., 1996; Berrebi et al., 2000; Crivelli et al., 2000).
> Marble trout have distinctive color pattern. However, some do have red dots. These are two photos of the same specimen from the Studenec stream, one of 8 genetically pure populations.
Genetic markers
The next important step in marble trout research was the development of molecular marker system for differentiation between purebred and hybrid and for assessing population genetic structure (e.g., genetic diversity). We combined numerous microsatellite loci and nDNA SNPs (Pustovrh et al., 2012) and established a powerful tool for quick and reliable discrimination between marble trout, Danubian and Atlantic brown trout and the hybrids.
> Simona is checking new markers using gel electrophoresis (photo A. Hodalič)
Using this marker system, we surveyed a major part of the Soča river system and found out the following facts:
- Genetic diversity of pure populations was extremely low.
- Genetic contamination with brown trout was very high in hybridization zone
- Genetically pure marble trout (or „almost pure“; >95%) can still be found in the hybridization zone meaning that panmixia has not yet been reached in the zone of hybridization
Genetic management in the hybridization zone
Considering low genetic diversity of genetically pure marble trout populations, their offspring may not be able to sufficiently adapt to the environment of their release. So, juveniles to be stocked need to be genetically more polymorphic.
To reinforce genetic diversity of the broodstock, phenotypically appropriate individuals have been each spawning season sorted out from the zone of hybridization and their tissue sent for genetic analysis. Only genetically adequate individuals have been used as genitors and included in repopulation process along with individuals from genetically pure populations.
> As a result of co-operation between RD Tolmin and BTRG, the genetic management of marble trout in hybridization zone has been performed for more than a decade (photos 1, 3 and 4 by A. Hodalič)
Increase of marble trout genes
Comparison of the genetic proportion of marble and brown trout in the zone of hybridization in the upper Soča valley by years 1997 and 2012 reveals that the replacement of foreign alleles with native ones has been taking place, which indicates a very positive impact of ongoing conservation measures and successful marble trout restoration.
> Effective replacement of foreign brown trout alleles with native marble trout ones is evident.
References
Bernatchez L., Guyomard R. & Bonhomme F. 1992. Molecular Ecology 1: 161-173.
Bernatchez L. 2001. Evolution, 55, 2: 351-379.
Berrebi P., Povž M., Jesenšek D., Cattaneo-Berrebi G., Crivelli A.J. 2000. Heredity, 85: 277-287.
Crivelli, A., Poizat, G., Berrebi, P., Jesenšek, P., Rubin, J. F. 2000. Cybium 24: 211–230.
Delling, B., 2002. Cybium 24 (4): 283-300.
Fumagalli, L., Snoj, A., Jesenšek, D., Balloux, F., Jug, T., Duron, O., Brossier, F., Crivelli, A.J. 2002. Molecular Ecology 11 (12): 2711-2716.
Gridelli, E., 1936. Bollettino della Societa Adriatica di Scienze Naturali in Trieste 34: 7-140.
Jug, T, Berrebi, P, Snoj, A. 2005. Biological Conservation 123, p. 381-388.
Povž, M., Jesenšek, D., Berrebi, P., Crivelli, A. 1996. Arles, Station de biologique de la Tour du Valat publication.
Pustovrh, G., Sušnik Bajec, S., Snoj, A. 2011. Molecular Phylogenetics and Evolution, 59: 761-766.
Pustovrh, G., Sušnik Bajec, S., Snoj, A. 2012. Aquaculture, 370-371: 102-108.
Pustovrh, G., Sušnik Bajec, S., Snoj, A. 2014. Genetics Selection Evolution, 7.
Razpet, A., Marić, S., Parapot, T., Nikolić, V., Simonović, P. 2007. Italian Journal of Zoology, 74: 63-70.
Skaala, O., Solberg. G. 1997. Nordic Journal of Freshwater Research 73: 5-15.
Snoj A., Jug T., Melkič E., Sušnik S., Pohar J., Dovč P. & Budihna N. 2000. Journal of Freshwater Biology (Quaderni ETP) 29: 5-11.
Snoj A, Marić S, Berrebi P, Crivelli AJ, Shumka S, Sušnik S. 2009. Genetics Selection Evolution, 41: 22.
Snoj, B. Glamuzina, A. Razpet, J. Zablocki, I. Bogut, E. Lercetau-Köhler, N. Pojskić, S. Sušnik. 2010. Hydrobiologia, 651: 199–212.
Splendiani, A., Giovannotti, M., Cerioni, P.N., Caniglia, M.L., Caputo, V. 2006. Italian Journal of Zoology, 73: 179-189.
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