Risk identification of non-native freshwater fishes in four countries of the Balkans Region using...

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Transcript of Risk identification of non-native freshwater fishes in four countries of the Balkans Region using...

Medit. Mar. Sci., 14/2, 2013, 369-­376 369

1 1 + 2 3 4 5

1 1 6 and 7

1 University of Belgrade, Faculty of Biology, Studentski trg 16, PO Box 550, 11000 Belgrade, Serbia

2

+deceased

3 University of Montenegro, Faculty of Sciences and Mathematics, PO Box 211, 81000 Podgorica, Montenegro

4 University “St. Ciril and Methodius”, Faculty of Sciences and Mathematics, Gazi Baba bb., 1000 Skopje,

Former Yugoslav Republic of Macedonia

5 University “St. Ciril and Methodius”, Institute of Animal Science - Fisheries Department, Bul. Ilinden 92a, 1000 Skopje,

Former Yugoslav Republic of Macedonia

6 Murray-Darling Freshwater Research Centre, PO Box 991, Wodonga Vic 3689, Australia

7

Peterborough, Canada

Corresponding author: [email protected]

Handling Editor: Argyro Zenetos and Alkiviadis Economou

Received: 2 February 2013;; Accepted: 20 May 2013;; Published on line: 21 June 2013

of medium and high risk sensu lato

risk, 10 as medium risk, and 30 as high risk, with the latter category comprised of 26 moderately high risk, three high risk, and

amongst assessors.

Research ArticleMediterranean Marine Science

Delminichthys, Economidichthys and Pelasgus sensu Aulopyge, Phoxinellus and Roman-­

ichthys, as well as many endemic species of otherwise Barbus, Cobitis, Eudontomyzon,

Gobio, Knipowitschia, Rutilus and Zingel

et al.,

et al., 2010, 2011ab;; Ristovska et al.,

et al.,tially overlaps with the Croatian and Romanian sections,

et al.,

2002;; Copp et alterised by a high level of endemism such as the Mediter

et al

et al., et al.

et al

Medit. Mar. Sci., 14/2, 2013, 369-­376

represents a remarkable biodiversity hotspot within the

et al., et al. et al

et al., 2001;; Grigorovich et al

species, some of which have become highly invasive

et al

et al comprising more

et al.,The state of inland waterways described above

et al.,

risks as well as implementation of appropriate manage

ment and control measures in order to ensure compliance

along with the strong pressure it sustains from the intro

tion, but so far this has been lacking despite an increased

awareness of the risks and potential adverse effects posed

To address this problem, the aim of the present study was

determine the threshold value for distinguishing between

et al,. assessments were car

based on the criterion of introduction applied to check

et al. et al.,

tov et al.,et al.,

et al.,hardt et al.,

and terminology given in Copp et al.Salmo letnica Scardin-­

ius knezevici Alburnus scoranza

et al., Salmo cf. macedonicus

et alduction of grayling Thymallus thymallusenian part of the River Danube catchment to the River

perch from the River Danube catchment

ferent number of species, resulting from one to four repli

et al.,

a priori as either invasive

http://www.

issg.org

vs vs

Medit. Mar. Sci., 14/2, 2013, 369-­376

of two straight lines, one vertical from 0,0 to 0,1 and the

species.

J

et al. and a smoothed

n = 2000 default bootstrap replicates.

i ii i

sensu lato

et al.

the remaining 30 as high risk sensu lato, of which 26

Carassius gibelio, followed by the three high risk species, brown bullhead

Ameiurus nebulosus Pterygopli-­chthys pardalis Gambusia af-­

Coregonus lavaretus, the Polyodon spatula and the Arc

tic char Salvelinus alpinus

a priori catego

Mean certainty in response for all species was

Scardinius knezevici to a Perca

Fig. 1:

Medit. Mar. Sci., 14/2, 2013, 369-­376

and the Atlantic strain of brown trout Salmo trutta trutta.

The threshold value that distinguishes between medi

Fig. 2: nsensu lato

http://www.issg.org and www.iucnredlist.org

Common name

Acipenser gueldenstaedtii Danube sturgeon

endangered

mk 16.0 MH

Acipenser ruthenus sterlet mk MH

Alburnus scoranza rs M

Ameiurus melas black bullhead rs MH 0.92

Ameiurus nebulosus brown bullhead mk ,me, rs 29.0 31.0 H 0.90

Babka gymnotrachelus racer goby rs MH 0.96

Carassius gibelio gibel carp mk, me, rs 2.2 1.00 0.03

Coregonus lavaretus bg 0.90

Coregonus peled peled rs 3.0 M

Ctenopharyngodon idella grass carp bg, mk, me, rs 21.0 MH 0.93 0.03

mk H

Gambusia holbrooki bg, me 19.0 12.0 26.0 MH 0.90 0.01

Gymnocephalus cernua ruffe mk MH

Hypophthalmichthys molitrix

silver carp bg, mk, me, rs 12.0 2.1 MH 0.93 0.03

Hypophthalmichthys nobilis bighead carp bg, mk, me, rs 13.9 3.3 MH 0.93 0.03

(continued)

Medit. Mar. Sci., 14/2, 2013, 369-­376

et al et al.,

et al.,

is probably due to the elevated number of translocations

within countries of this region, in particular to closed,

As such, many species were evaluated for invasiveness

even though they are not normally classed as particularly

graphical scale.

mtDNA molecular lineages assigned to ginbuna Caras-­

Carassius auratus and gibel carp, which were recently recorded using the cytochrome b

et al.erstwhile unintentional introduction of gibel carp into the

and has been blamed for declines of native crucian carp

Carassius carassius, common carp Cyprinus carpio and tench Tinca tinca et alresponsible for gibel carp invasiveness are its ability to

its adaptability to various, including harsh, environmen

et al., et al.,

Common name

Ictalurus punctatus bg 10.0 MH

Lepomis gibbosus pumpkinseed bg, mk, rs 21.3 MH 0.01

Megalobrama terminalis black Amur bream me MH

Micropterus salmoidesbass

rs MH

Mugil soiuy bg 12.0 MH

Mylopharyngodon piceus black carp bg 11.0 MH

monkey moby rs MH 0.91

Neogobius melanostomus round goby rs MH

Oncorhynchus mykiss rainbow trout bg, mk, me, rs 12.0 1.6 MH 0.93 0.99 0.02

Oxynoemacheilus bureschi mk M

Pachychilon macedonicum Macedonian roach rs M

Eurasian perch me 23.0 MH 0.99

Perccottus gleniisleeper

bg, rs 19.0 0.2 MH

Polyodon spathulaendangered

bg, rs 0.0 3.0 0.03

Ponticola kessleri bighead goby rs MH 0.91

Proterorhinus semilunaris western tubenose

goby

rs 13.0 MH

Pseudorasbora parva topmouth gudgeon bg, mk, me, rs 12.0 26.0 MH 0.02

Pterygoplichthys pardalis rs 29.0 H

Rutilus sp. Adriatic roach rs M

Salmo letnica rs M

Salmo macedonicus Macedonian trout rs MH 0.90

Salmo trutta trutta brown trout me 22.0 MH 0.99

Salvelinus alpinus Arctic char rs 0.0 0.90

Salvelinus fontinalis brook trout bg, mk, rs 0.0 12.0 M 0.90 0.01

Sander lucioperca pikeperch mk MH 0.91

Scardinius knezeviciendangered

rs 9.0 M

Syngnathus abaster rs M

Thymallus thymallus grayling me M

Medit. Mar. Sci., 14/2, 2013, 369-­376

et al.,

et al.,tion process in gibel carp appears to be complete in the

The second most invasive species in the region,

spread of brown bullhead has been through human ac

logical traits with brown bullhead and the climate in the

a priori categories of invasive species, suggests that the introduc

to native species and ecosystems, especially when the cli

matic and environmental conditions in the recipient area

match those in the donor area. This result also suggests

that a priori invasiveness assigned for particular species

This is because a number of alien species have been es

et al.,

et al.,not in others. This appears to be in accordance with their

The high risk of invasiveness revealed by the Ama

Pterygoplichthys pardalis was a result of its previous history of introductions, impacts posed to the

recipient ecosystems, lack of natural predators, environ

mental versatility and reproductive features. However, the

ances to environmental factors and its ecosystem impacts

et al.,

son for future environmental surveillance.

grass carp, pumpkinseed, rainbow trout and Amur sleeper

Perccottus gleniiless of their a prioriThis may be attributed to their similar introduction history

certain species such as gibel carp, both western and east

level, and the variability of risk assessment was very high,

ranging from medium to high. The uniformity and low

variability in CF values in particular countries indicates

a similar level of familiarity amongst assessors concern

ing these species. Finally, no clear relationship was found

between the interval of the time since the introduction of a

ing their traits in the recipient ecosystems.

Environment, Food and Rural Affairs.

References

Risk Analysis http://

Zoogeography of Fresh Waters.General Distribution and Dispersal of Freshwater Animals.

er operating characteristic curves. Critical Care

rope. Canadian Journal of Fisheries and Aquatic Sciences,

Biology and Wildlife of the Medi-­terranean Region

ing species responses to warming temperatures in a temperate

region. Freshwater BiologyThe ecologi-­

cal and socio-­economic impacts of invasive alien species in

Medit. Mar. Sci., 14/2, 2013, 369-­376

inland water ecosystems.

and perspectives on protocols for the UKhttp://

www.cefas.co.uk/ publications/ techrep/ tech129.pdf

et al., Journal of Applied Ichthyology,

et al.,Risk Analysis

of black bullhead Ameiurus melasbian waters. Archives of Biological Sciences

paring the areas under two or more correlated receiver operat

ing characteristic curves: a nonparametric approach. Biomet-­rics

et al., 2009. Carassius carassius

Proceedings of the IV International Conference “Fishery”, Belgrade, 27–29 May 2009. Faculty

. Prefectural

A.G., et al.,

analyses. Canadian Journal of Fisheries and Aquatic Sci-­ences

erence to its Central and Eastern part. Canadian Journal of Fisheries and Aquatic Sciences

Italian Journal of Zoology,

Canadian Journal of Fisheries and Aquatic Sciences

New mtDNA data reveal a wide distribution of the Japanese

ginbuna in Europe. Journal of Fish Bi-­ology

Science

Hypophthalmichthys molitrix Hypophthalmichthys no-­bilis

3rd

International Conference “Fishery”, Belgrade, 1–3 Febru-­ary 2007. ,

.

1st Symposium for Protection of Natural Lakes in Republic of Macedonia, Ohrid, 31 May–3 June 2007.

Acipenser ruthenus

1st Symposium for Protection of Natural Lakes in Republic of Macedonia, Ohrid, 31 May–3 June 2007. Ministry of Educa

report about common ruffe Gymnocephalus cernua

Proceedings papers devoted to Cyril Apostolski

BALWOIS, Conference on water observation and infor-­mation system for decision support, Ohrid, 25–29 May 2010.

nia,

lic of Macedonia. Macedonian Journal of Animal Science

2011b. Assessement of the ecological status of the Crna River

the monitoring system of rivers in R. Macedonia. Macedo-­nian Journal of Animal Science,

case study. Macedonian Journal of Animal Science

Proceedings of the IV International Conference ”Fishery”, Belgrade, 27 – 29 May 2009. Faculty of Agricul

Biologia

to peninsular Florida. Risk Analysis

M., et al.,Reviews

in Fish Biology and Fisheries

et al.,Carassius gibelioJournal of Applied Ichthyology

Carassius au-­ratus gibelio

Vodoprivreda

Medit. Mar. Sci., 14/2, 2013, 369-­376

via. Acta Biologica Iugoslavica – Ekologija D., 2011. Katalog slatkovodnih riba (Os-­

teichthyes) Crne Gore -­teichthyes) of Montenegro

chondrial DNA control region analysis. Genetique, Selection, Evolution

Aquatic Invasions,

Conser-­vation Biology

et al.,

Ichthyological Research,

G.H., et al., Interim protocols for risk assessment of aquatic invasive species introductions via European inland waterways;; ALARM Project, Project Website. www.alarm

Lepomis gibbosusAtlas of River Nestos Fish Fauna.

reproduction and growth in Mongolian populations of Caras-­sius auratus gibelio Folia Zoologica 36,

Carassius auratus gibeliomember of our ichthyofauna. Ribarstvo Jugoslavije, 22, 6.

Acta Zoologica Bulgarica

R Development Core Team, 2010. R: A language and environment

Ictalurus nebulosus Annales , 10

Journal of International Environmental Application & Science

et al., 2012. Scardinius knezeviciand Alburnus scoranza

Arch. Biol. Sci. Belgrade

Ribe Srbije Fishes of Serbia

Phlogiston,

Carassius auratus gibelio Acta biologica Iugoslavica – Ichthyologia Belgrade

considerations. Bios Thessaloniki

The Danube in Serbia – The Results of National Program of the Second Joint Danube Survey

Pterygoplichthys pardalis

Biotechnology and Biotechnological Equipment

Morphology, feeding and reproduction of the round goby, Neogobius melanostomusvia. Journal of Great Lakes Research,

Gdansk Neogobius Neogobius melanostomusBulletin of the Sea Fisheries Institute

et al., 2012. Are introduced gibel carp Carassius gibelio in

Fisheries Management & Ecology

nã nativos cultivados na região cisteura do Rio Grande du

Boletim do In-­stituto de Pesca, São Paulo,

Acta Ichthyologica et Piscatoria,

Acta Zoologica Bulgarica,

Carassius gibelioJournal of

Applied Ichthyology

Risk Anal-­ysis

Directive of the European Parliament and of the Council 2000/60/EC establishing a framework for commu-­

Cancer,