North Sea Houting (Coregonus Oxyrinchus) Ecological Risk Screening Summary

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North Sea Houting (Coregonus oxyrinchus) Ecological Risk Screening Summary

U.S. Fish and Wildlife Service, September 2014 Revised, December 2017 Web Version, 7/5/2018

Photo: H. Dupond. Licensed under CC BY-NC-SA. Available: http://www.marinespecies.org/aphia.php?p=image&pic=16978. (December 2017).

1 Native Range and Status in the United States Native Range From Froese and Pauly (2017):

“Northeast Atlantic: Ireland to Netherlands, Germany and the countries along the coast of the Baltic Sea. Also found in several countries in central and eastern Europe. Maritime stocks may be extinct [Robins et al. 1991].”

From Freyhof and Kottelat (2008):

“Southern North Sea basin: Schelde, Rhine and Meuse drainages (exceptionally northern France). Ascended Rhine up to Köln [recorded to have reached Strasbourg (France) but this is probably erroneous]. Occasional records from southeast coast of England.”

Status in the United States This species has not been reported as introduced or established in the United States.

Means of Introductions in the United States This species has not been reported as introduced or established in the United States.

Remarks There is conflicting information about whether or not this species is extinct.

From Jensen et al. (2015):

“Freyhof & Schöter (2005) investigated variation in morphological traits and suggested that C. oxyrinchus was confined to the Rhine and became extinct. This view was adopted by the International Union for the Conservation of Nature (IUCN), and thus the status of C. oxyrinchus on the IUCN Red List is listed as ‘Extinct’. However, some of the traits that Freyhof & Schöter (2005) analysed are known to be homoplastic in whitefish (Østbye et al. 2005, 2006, Etheridge et al. 2012), and their conclusion has been questioned based on comprehensive genetic evidence (Jacobsen et al. 2012).”

From Freyhof and Schӧter (2005):

“[…] C. oxyrinchus must be considered globally extinct, as there is no record after 1940 and no trace of its survival can be found. Now, the only known autochthonous Coregonus in the North Sea basin are found in the River Vida (Denmark) and genetic analyses have shown them to be C. maraena (Hansen et al., 1999), as do the present results. Because the present study indicates C. oxyrinchus is extinct, restocking programmes based on the transfer of fishes from the River Vida to other rivers (England, Rhine, Meuse and Schelde) is counterproductive to effective conservation and management of natural resources, resulting only in the introduction of an exotic species (C. maraena) into drainages outside its native range.”

From Borcherding et al. (2014):

“Since 1996, a re-introduction programme at the River Rhine was established for anadromous North Sea houting (NSH), Coregonus oxyrinchus (L.) that has been considered extinct in the River Rhine (Kranenbarg et al. 2002) as well as in nearly the whole North Sea basin since the 1940s (Lelek 1987). Descendents from the last existing population of NSH in Europe (Jepsen et al. 2012) were used for a re-introduction programme in the River Rhine (Borcherding 2011) […]”

From Poulsen et al. (2012):

“Historically, C. oxyrinchus was found in the entire Wadden Sea area. Due to heavy pollution and eradication of spawning and nursery areas, however, C. oxyrinchus had disappeared from most rivers by the 1970s and 1980s and was on the brink of extinction. The only indigenous population that remains today is found in the Danish River Vida (54˚ 55’ N; 8˚ 52’ E)

(Borcherding et al., 2006; Madsen & Murray, 2007). As a result of a number of stocking programmes in both Denmark and Germany, the species has been reintroduced into several rivers (Borcherding et al., 2006).”

2 Biology and Ecology Taxonomic Hierarchy and Taxonomic Standing From ITIS (2017):

“Kingdom Animalia Subkingdom Bilateria Infrakingdom Deuterostomia Phylum Chordata Subphylum Vertebrata Infraphylum Gnathostomata Superclass Actinopterygii Class Teleostei Superorder Protacanthopterygii Order Salmoniformes Family Salmonidae Subfamily Coregoninae Genus Coregonus Species Coregonus oxyrinchus (Linnaeus, 1758)”

“Synonym(s): Coregonus lavaretus oxyrinchus (Linnaeus, 1758) Salmo oxyrinchus Linnaeus, 1758”

From Eschmeyer et al. (2017)

“Current status: Valid as Coregonus oxyrinchus (Linnaeus 1758). Salmonidae: Coregoninae.”

Size, Weight, and Age Range From Froese and Pauly (2017):

“Max length : 50.0 cm TL male/unsexed; [Muus and Dahlström 1968]; max. published weight: 2.0 kg [Muus and Dahlström 1968]”

Environment From Froese and Pauly (2017):

“Freshwater; brackish; […] 4°C - 20°C [Baensch and Riehl 1991; assumed to be recommended aquarium temperature range]”

Climate/Range From Froese and Pauly (2017):

“69°N - 43°N, 11°W - 58°E”

Distribution Outside the United States Native From Froese and Pauly (2017):

From Freyhof and Kottelat (2008):

Introduced From Borcherding et al. (2006):

“In the 1980s, the last known reproducing population of North Sea houting existed in the Danish River Vidå (Grøn, 1987). A few catches of adult North Sea houting from this river were used to establish a broodstock to support the natural population in the River Vidå (Grøn, 1987). Descendants of this broodstock served as the basis for the reintroduction of North Sea houting into the German rivers Treene and Osterau in 1987 (Jäger, 1999). The first adults were caught on their return migration in the River Treene in 1989. From 1992 onwards, the number of returning adults that were caught in this river was sufficient to produce enough small juveniles for stocking programmes in other parts of Germany (Jäger, 1999). Although a small number of juveniles were stocked in the Lower Rhine in 1992, North Sea houting have been stocked there regularly and with increasing numbers since 1996 […]. The catches of North Sea houting in Lake IJsselmeer, The Netherlands, increased accordingly […], with the fish believed to originate from the stocks in the Lower Rhine (de Groot, 2002; Kranenbarg et al., 2002).”

From Jensen et al. (2015):

“In an attempt to save the species from extinction, a stocking programme was launched in 1982, releasing a total of 1.7 million juvenile North Sea houting into a few Danish rivers. […] The Danish stocking programme ended in 1992 (Jensen et al. 2003), […]”

From Dierking et al. (2014):

“Interviews with resource managers revealed that adults, fertilized eggs, and fry of NSH [North Sea houting], BH [Baltic houting], and EW [European whitefish] have been periodically kept in

the same facilities. Although official records did not indicate stocking of the historic houting ranges with non-native ESUs [evolutionarily significant units], stocking errors therefore appear possible.”

Means of Introduction Outside the United States From Borcherding et al. (2006):

“The juvenile North Sea houting used for the Lower Rhine stocking programme were obtained from a fish hatchery in northern Germany.”

Short Description From Freyhof and Schӧter (2005):

“The anadromous and riverine coregonids examined can be grouped according to the presence or absence of a prominent snout and inferior mouth. By this character C. oxyrinchus is well distinguished from the specimens of C. widegreni Malmgren and C. sp. ‘Rhine’, which do not have a prominent snout and subinferior mouth. Coregonus oxyrinchus collected between 1844 and 1906 from lower Rhine, Maas and Schelde have 38-46 gill rakers on the first branchial arch. In contrast, specimens identified as C. oxyrinchus collected from North Sea tributaries east of the River Rhine and Baltic basin, and in the lower Rhine after 1998, have 23-35 gill rakers on the first branchial arch […].”

“Coregonus oxyrinchus is distinguished from all other species of Coregonus in Europe by having a long, pointed snout, an inferior mouth and 38-46 gill rakers.”

“Large, elongate and strongly laterally compressed coregonid species. Mouth inferior, with maxilla reaching beyond anterior eye margin, often to centre of eye. Upper jaw projecting beyond lower jaw, mandible reaching posteriorly beyond centre of eye. Eye large, its diameter 0.6-1.0 (mean 0.7) times in interorbital width. Caudal peduncle 1.3-1.9 (mean 1.6) times longer than deep. Dorsal fin margin concave. Pelvic fin origin below branched dorsal fin ray 2-3.”

Biology From Froese and Pauly (2017):

“In brackish water and main rivers; no evidence that it enters marine waters [Kottelat and Freyhof 2007]. Also non-migratory freshwater populations [Kottelat 1997]. Feeds on zooplankton, supplemented by benthic invertebrates in adults.”

From Freyhof and Schӧter (2005):

“Ecological data presented by Redeke (1934) suggest that C. oxyrinchus is a planktivorous species not migrating to pure marine waters.”

From Freyhof and Kottelat (2008):

“The species relied upon estuaries and brackish water to forage, where pollution was at it its most concentrated and coregonids are very sensitive to pollution.”

From Borcherding et al. (2006):

“North Sea houting first migrate at an age of c. 2.5 (mainly males) or 3.5 years in November to December from the Wadden Sea to their spawning grounds in the potamal reaches of the rivers, to which they can return several times (maximum age of up to 10 years). In areas with moderate current, houting spawns freely into the water, where the adhesive eggs attach themselves to aquatic plants, stones and gravel. The fry hatch from the eggs in February to March at a size of c. 10 mm. When the fish reaches a total length (LT) of 30–40 mm, its physiology changes so it can withstand the move from fresh to saltwater (Jensen et al., 2003).”

From Poulsen et al. (2010):

“Despite numerous large-scale restoration and stocking programmes aiming at preventing C. oxyrinchus from extinction, little is known about the biology of this species. This is especially true for the behaviour, ecology and habitat requirements during the early freshwater stages that are often associated with severe mortalities (Jensen et al., 2003; Borcherding et al., 2006; Madsen & Murray, 2007)”

Human Uses From Froese and Pauly (2017):

“Fisheries: commercial; aquaculture: commercial”

From Borcherding et al. (2008):

“[…] the North Sea houting, Coregonus oxyrinchus, used to be common in the River Rhine as well as in the whole Wadden Sea area […]. Until the beginning of the 20th century, commercial fisheries in the Dutch reaches of the lower Rhine caught up to 15 tonnes per year (De Groot, 1990).”

Diseases No information available. No OIE-reportable diseases have been documented for this species.

Threat to Humans From Froese and Pauly (2017):

“Harmless”

3 Impacts of Introductions Coregonus oxyrinchus has been reintroduced to rivers where it was previously extirpated (See Distribution Outside the United States). No information is available on the impacts of these reintroductions.

4 Global Distribution

Figure 1. Known global distribution of Coregonus oxyrinchus. Map from GBIF Secretariat (2017). Three points in Italy were excluded from the extent of this map and from the climate matching analysis because they do not match the distribution of C. oxyrinchus stated by other sources (See Native Range). The point in the Baltic Sea was excluded from the climate matching analysis because this species is not known to enter marine waters (Froese and Pauly 2017).

5 Distribution Within the United States This species has not been reported as introduced or established in the United States.

6 Climate Matching Summary of Climate Matching Analysis The Climate 6 score (Sanders et al. 2014; 16 climate variables; Euclidean distance) for the contiguous United States was 0.003, which is classified as low match. The climate match was not high in any states. The climate match was medium in Massachusetts, Michigan and Washington, and low elsewhere in the contiguous United States.

Figure 2. RAMP (Sanders et al. 2014) source map showing weather stations in Europe selected as source locations (red; France, Belgium, the Netherlands, Germany, Sweden) and non-source locations (gray) for Coregonus oxyrinchus climate matching. Source locations from GBIF Secretariat (2017).

Figure 3. Map of RAMP (Sanders et al. 2014) climate matches for Coregonus oxyrinchus in the contiguous United States based on source locations reported by GBIF Secretariat (2017). 0=Lowest match, 10=Highest match. Counts of climate match scores are tabulated on the left.

The “High”, “Medium”, and “Low” climate match categories are based on the following table:

Climate 6: Proportion of Climate (Sum of Climate Scores 6-10) / (Sum of total Match Climate Scores) Category 0.000≤X≤0.005 Low 0.005

7 Certainty of Assessment Because it is part of a taxon that is economically important to Europe, Coregonus oxyrinchus has been well-studied. Despite this, there is still uncertainty regarding the status of this species. There is morphological and taxonomic uncertainty distinguishing between C. oxyrinchus and other European coregonids, and there is dispute as to the status of its population: Some regard it

as critically endangered, and reintroduction programs have been established; others view this species as extinct and claim that the Coregonus species being stocked is not in fact C. oxyrinchus. Certainty of this assessment is low.

8 Risk Assessment Summary of Risk to the Contiguous United States Coregonus oxyrinchus is a fresh- and brackish water whitefish species native to northern Europe. It is not known to enter marine waters. This species has seen a severe decrease in its populations due to habitat loss and pollution. Some (Freyhof and Schöter 2005) assert that this species is extinct. Others claim it is critically endangered, and stocking programs have been established to reintroduce it to rivers in its historical native range. Populations of C. oxyrinchus have been introduced to Germany and Denmark and have established there, but since this is part of the species’ native range, it has no documented history of invasiveness. C. oxyrinchus has a low climate match with the United States. Certainty of this assessment is low due to uncertainty concerning the status of its population. Overall risk assessment category is uncertain.

Assessment Elements  History of Invasiveness (Sec. 3): None Documented  Climate Match (Sec. 6): Low  Certainty of Assessment (Sec. 7): Low  Remarks/Important additional information: Considered extinct by some  Overall Risk Assessment Category: Uncertain

9 References Note: The following references were accessed for this ERSS. References cited within quoted text but not accessed are included below in Section 10.

Borcherding, J., A. Scharbert, and R. Urbatzka. 2006. Timing of downstream migration and food uptake of juvenile North Sea houting stocked in the Lower Rhine and the Lippe (Germany). Journal of Fish Biology 68(4):1271-1286.

Borcherding, J., C. Pickhardt, H. V. Winter, and J. S. Becker. 2008. Migration history of North Sea houting (Coregonus oxyrinchus L.) caught in Lake IJsselmeer (The Netherlands) inferred from scale transects of 88Sr:44Ca ratios. Aquatic Sciences 70(1):47-56.

Borcherding, J., A. W. Breukelaar, H. V. Winter, and U. König. 2014. Spawning migration and larval drift of anadromous North Sea houting (Coregonus oxyrinchus) in the River IJssel, the Netherlands. Ecology of Freshwater Fish 23(2):161-170.

Dierking, J., L. Phelps, K. Præbel, G. Ramm, E. Prigge, J. Borcherding, M. Brunke, and C. Eizaguirre. 2014. Anthropogenic hybridization between endangered migratory and commercially harvested stationary whitefish taxa (Coregonus spp.). Evolutionary Applications 7(9):1068-1083.

Eschmeyer, W. N., R. Fricke, and R. van der Laan, editors. 2017. Catalog of fishes: genera, species, references. Available: http://researcharchive.calacademy.org/research/ichthyology/catalog/fishcatmain.asp. (December 2017).

Freyhof, J., and C. Schöter. 2005. The houting Coregonus oxyrinchus (L.) (Salmoniformes: Coregonidae), a globally extinct species from the North Sea basin. Journal of Fish Biology 67(3):713-729.

Froese, R., and D. Pauly, editors. 2017. Coregonus oxyrinchus (Linnaeus, 1758). FishBase. Available: http://www.fishbase.org/summary/Coregonus-oxyrhynchus.html. (December 2017).

GBIF Secretariat. 2017. GBIF backbone taxonomy: Coregonus oxyrinchus, Linnaeus, 1758. Global Biodiversity Information Facility, Copenhagen. Available: https://www.gbif.org/species/2351155. (December 2017).

ITIS (Integrated Taxonomic Information System). 2017. Coregonus oxyrinchus (Linnaeus, 1758). Integrated Taxonomic Information System, Reston, Virginia. Available: https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=161 955#null. (December 2017).

Jensen, L. F., D. S. Thomsen, S. S. Madsen, M. Ejbye-Ernst, S. B. Poulsen, and J. C. Svendsen. 2015. Development of salinity tolerance in the endangered anadromous North Sea houting Coregonus oxyrinchus: implications for conservation measures. Endangered Species Research 28(2):175-186.

Poulsen, S. B., J. C. Svendsen, L. F. Jensen, C. Schulz, T. Jäger‐Kleinicke, and H. Schwarten. 2010. Effects of food deprivation on refuge use and dispersal in juvenile North Sea houting Coregonus oxyrinchus under experimental conditions. Journal of Fish Biology 77(7):1702-1708.

Poulsen, S. B., Jensen, L. F., Schulz, C., Deacon, M., Meyer, K. E., Jäger-Kleinicke, T. Jäeger- Kleinicke, H. Schwarten, and J. C. Svendsen. 2012. Ontogenetic differentiation of swimming performance and behaviour in relation to habitat availability in the endangered North Sea houting (Coregonus oxyrinchus). Aquatic Living Resources 25(3):241-249.

Sanders, S., C. Castiglione, and M. H. Hoff. 2014. Risk Assessment Mapping Program: RAMP. U.S. Fish and Wildlife Service.

10 References Quoted But Not Accessed Note: The following references are cited within quoted text within this ERSS, but were not accessed for its preparation. They are included here to provide the reader with more information.

Baensch, H. A., and R. Riehl. 1995. Aquarien Atlas, volume 4. Mergus Verlag GmbH, Verlag für Natur-und Heimtierkunde, Melle, Germany.

Borcherding, J. 2011. The successful re-introduction of North Sea houting to the River Rhine System in Europe. Pages 20-23 in P. S. Soorae, editor. Global Re-introduction Perspectives: 2011. More case studies from around the globe. IUCN/SSC Re-introduction Specialist Group and Abu Dhabi, Gland, Switzerland.

Etheridge, E. C., C. E. Adams, C. W. Bean, N. C. Durie, A. R. D. Gowans, C. Harrod, A. A. Lyle, P. S. Maitland, and I. J. Winfield. 2012. Are phenotypic traits useful for differentiating among a priori Coregonus taxa? Journal of Fish Biology 80:387-407.

Grøn, P. 1987. Saving the North Sea Houting. Pages 147-159 in S. Tougaard and S. Asbirk, editors. Proceedings of the 5th International Wadden Sea Symposium, Esbjerg, Denmark, 1986. The National Forest and Nature Agency and The Museum of Fishery and Shipping, Copenhagen.

De Groot, S. J. 1990. Decline of the catches of coregonids and migratory smelt in the lower Rhine, The Netherlands. Journal of Applied Ichthyology 6:247-251.

De Groot, S. J. 2002. A review of the past and present status of anadromous fish species in the Netherlands: is restocking the Rhine feasible? Hydrobiologia 478:205-218.

Jacobsen, M. W., M. M. Hansen, L. Orlando, D. Bekkevold, L. Bernatchez, E. Willerslev, and M. T. Gilbert. 2012. Mito genome sequencing reveals shallow evolutionary histories and recent divergence time between morphologically and ecologically distinct European whitefish (Coregonus spp.). Molecular Ecology 21:2727-2742.

Jäger, T. 1999. Die Wiedereinbürgerung des Nordseeschnäpels. Pages 3-11 in Verband Deutscher Sportfischer, editor. Fisch des Jahres 1999: Der Nordseeschnäpel Verband Deutscher Sportfischer, Offenbach, Germany.

Jensen, A. R., H. T. Nielsen, and M. Ejbye-Ernst. 2003. National management plan for the houting. Ministry of the Environment, Forest and Nature Agency, County of Southern Jutland and County of Ribe, Ribe, Denmark.

Kottelat, M. 1997. European freshwater fishes. Biologia 52(5):1-271.

Kottelat, M., and J. Freyhof. 2007. Handbook of European freshwater fishes. Publications Kottelat, Cornol and Freyhof, Berlin.

Kranenbarg, J., H. V. Winter, and J. J. G. M. Backx. 2002. Recent increase of North Sea houting and prospects for recolonization in the Netherlands. Journal of Fish Biology 61(A):251- 253.

Lelek, A. 1987. The freshwater fishes of Europe – threatened fishes of Europe. AULA Verlag, Wiesbaden, Germany.

Madsen, M., and C. Murray. 2007. Modellering af de hydrauliske konsekvenser samt snæbellarveopvækstbetingelserne ved gennemførelse af snæbelprojekt i Hestholm og Nørresø. Lindet Statsskovdistrikt, Landsdelscenter Sydjylland, Hørsholm, Denmark.

Muus, B. J., and P. Dahlström. 1968. Süßwasserfische. BLV Verlagsgesellschaft, München, Germany.

Østbye, K., P‐A. Amundsen, L. Bernatchez, A. Klemetsen, R. Knudsen, R. Kristoffersen, T. F. Naesje, and K. Hindar. 2005 Evolutionary history of the European whitefish Coregonus lavaretus (L.) species complex as inferred from mtDNA phylogeny and gill-raker numbers. Molecular Ecology 14:4371-4387.

Østbye, K., P‐A. Amundsen, L. Bernatchez, A. Klemetsen, R. Knudsen, R. Kristoffersen, T. F. Naesje, and K. Hindar. 2006. Parallel evolution of ecomorphological traits in the European whitefish Coregonus lavaretus (L.) species complex during postglacial times. Molecular Ecology 15:3983-4001.

Redeke, H. C. 1934. Über den Rheinschnäpel, Coregonus oxyrhynchus L. Verhandlungen der Internationalen Vereinigung für Limnologie 6:352-357.

Robins, C. R., R. M. Bailey, C. E. Bond, J. R. Brooker, E. A. Lachner, R. N. Lea and W. B. Scott. 1991. World fishes important to North Americans. Exclusive of species from the continental waters of the United States and Canada. American Fisheries Society Special Publication 21.