Rapid recent expansion of the round goby (Neogobius melanostomus) and the western tubenose goby (Proterorhinus semilunaris) in Flanders (Belgium)

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Rapid recent expansion of the round goby (Neogobius melanostomus) and the western tubenose goby (Proterorhinus semilunaris) in Flanders (Belgium) Hugo Verreycken, Jan Ostermeyer, Merlijn Mombaerts, Tine Huyse, Luc De Bruyn 18 ICAIS conference Niagara Falls (Canada) 23 April 2013 1

Round and tubenose goby in Flanders Introduction Results Distribution Life-history traits Parasites Phylogeography Conclusions 2

Round and tubenose goby in Flanders Introduction Both species Ponto-Caspian origin Widely distributed over Europe and North America Main vectors probably ballast water and opening Main Danube canal in 1992 Proved to be invasive in introduced regions 3

Round and tubenose goby in Flanders Material and Methods Electrofishing, fyke nets and angling (April May 2012) Ageing: scales Sex determined externally and by dissection Age-at-maturity by formula of DeMaster GSI= 100 x W(gonads)/(W(body)-W(gonads)) Length-weight relationship W=log a + b logl s DNA-sequencing: no. and diversity of haplotypes Maximum Likelihood trees 4

Round goby in Flanders

Distribution round goby The Netherlands Native: Introduced: Black, Caspian and Azov Seas Baltic Sea Laurentian Great Lakes Rest of Europe (The Netherlands, France, Germany, Austria Poland, Czech Republic, Hungary, Slovakia, Bulgaria, Serbia, Romania, Estonia, and Sweden) Maps: Kornis, Mercado-Silva and Vander Zanden (J.Fish.Biol., 2012) Belgium 6

Distribution round goby in Belgium Secondary introduction? 1st specimen (2010) 7

Life-history traits round goby Positive allometric growth (b = 3.2117) Sex ratio (N=50): 1.05 M/F Age-at-maturity: 2.2 years, with males: 2.8 yrs and females: 1.0 yr 3 or 4 years for males and 2 or 3 years females at age in native range (Miller, 2003) Length-at-maturity: males 69.0 mm and females 36.9 mm Mean L s at age (mm)(n = 50) Individuals of ages 1, 2, 3 and 4* were significantly smaller than those in the Black Sea (*not significant but N=2!), and among the smallest reported in Kornis et al. (2012) GSI was high ( = 10.91; = 1.55) 8

Ectoparasite fauna Table: Number of fish (N fish ), number of ectoparasites (N p ), prevalence, abundance and infection intensity per site. 80% of parasites found on fins, rest on gills (4%), head (5%), body (6%) and operculum (5%)(for round and tubenose samples together) Very low parasite prevalence, abundance and intensity which supports Enemy release hypothesis => recently introduced species via ballast water pathway? 3 Gyrodactylus specimens, 4 fungi, 4 unknown N fish N p Prevalence Abundance Intensity TOTAL 44 11 15.91 0.25 1.57 Albertkanaal Hasselt 11 3 9 0.12 3 Albertkanaal Kuringen 14 0 0 0 - Albertkanaal Grobbendonk 4 0 0 0 - Albertkanaal Zandhoven 2 0 0 0 - Zeeschelde 2 0 0 0 - Kanaal Gent-Terneuzen 11 8 54.54 0.72 1.33 Infection intensity = Number of adult parasites per infected round goby Abundance = Total number of parasites per round goby including uninfected specimens Prevalence = Percentage of infected round gobies on total number of round gobies investigated at each site 1 new Gyrodactylus species on round goby (highest similarity with Gyrodactylus kobayashii (from Carassius gibelio)(poland & UK)) 9

Phylogeographic data-analysis # samples # haplotypes H d P i Belgium Albertkanaal 18 2 0,209 ± 0,116 0,00021 Kanaal Gent- Terneuzen 10 3 0,378 ± 0,181 0,00038 Zeeschelde 2 1 0 x Netherlands Waal 18 1 0 x H d = haplotype diversity, P i = nucleotide diversity Low haplotype (gene) diversity (H d : 0,212) and nucleotide diversity (P i : 0.00033) 3 haplotypes => multiple introductions? 10

Phylogeographic data-analysis Low haplotype (gene) diversity (Hd: 0,212) and nucleotide diversity (Pi: 0.00033) 3 haplotypes => multiple introductions? Haplotypes compared with Genbank: 2 known & 1 unique haplotype H1 Haplotype 1: Samples from all Flemish populations except Zeeschelde => matches with haplotypes from Golf of Gdansk (Gdynia, Poland) Haplotype 2: 2 samples from Zeeschelde, 1 from Albertkanaal & 1 from Kanaal Gent-Terneuzen => matches with haplotypes from Black Sea (Mariupol, Ukraine) Haplotype 3: 1 sample from Kanaal Gent- Terneuzen No matches => unique haplotype (related to H1) H3 H2 Brown & Stepien (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns 11

Tubenose goby in Flanders

Distribution tubenose goby Miller, 2004 Native: native Introduced: Black Sea basin; Maritza and Struma drainages in eastern Aegean basin; in South Bug and Dniepr far upriver In Danube, present up to about Vienna, invasive since 1970s, now reaching upstream to southern Germany. Present in many European countries, abundant in the Netherlands Introduced to North America in 1991 13

Distribution tubenose goby in Belgium The Netherlands Flanders 1st specimen (2010) Wallonia 14

Life-history traits tubenose goby Negative allometric growth (b = 2.9561) Sex ratio (N=233): 1.63 M/F Age-at-maturity: 2.3 years, with males: 2.6 yrs and females: 2.1 yrs 1 or 2 years in native range (Miller, 2004) => we had no individuals of age 1! Length-at-maturity: males 38.6 mm and females 36.2 mm Mean L s at age (mm)(n = 233) Mean L s was significantly smaller than in native range GSI was high ( = 5.46; = 4.01) 15

Ectoparasite fauna Table: Number of fish (N fish ), number of ectoparasites (N p ), prevalence, abundance and infection intensity per site. N fish N p Prevalence Abundance Intensity TOTAL 73 166 82,19 2,27 2,77 Monding Kikbeek 37 95 83,78 2,57 3,06 Monding Ziepbeek 7 13 85,71 1,86 2,17 Kanaal van Beverlo 1 0 0 0 x Zuid Willemsvaart 28 58 82,14 2,07 2,52 Much higher parasite prevalence, abundance and intensity which supports Enemy release hypothesis => probably not introduced via ballast water but slower natural spreading through (Danube,) Rhine and Meuse 1 new Gyrodactylus species on tubenose goby (highest similarity with Gyrodactylus cf. niger (from North Sea; undescribed species)) 16

Phylogeographic data-analysis # samples # haplotypes H d P i Belgium Zuid Willemsvaart 20 1 0 x Kik en Ziepbeek 20 2 0,1 ± 0,088 0,00239 Kanaal van Beverlo 1 1 0 x H d = haplotype diversity, P i = nucleotide diversity 2 haplotypes Low haplotype (gene) diversity (Hd: 0.049) and nucleotide diversity (P i : 0.00117) 17

Phylogeographic data-analysis Low haplotype (gene) diversity (Hd: 0.049) and nucleotide diversity (P i : 0.00117) Haplotypes compared with Genbank: 1 known haplotype, 1 unique haplotype Haplotype 1: Samples from all Flemish populations Matches with Genbank haplotypes: Pro9 => Danube (Gorge, Serbia) Haplotype 2: 1 sample from Ziepbeek No matches with Genbank: unique haplotype H2 H1 Neilson & Stepien (2009) Evolution and phylogeography of the tubenose goby genus Proterorhinus (Gobiidae: Teleostei): 18 evidence for new cryptic species'

Conclusions Populations of round and tubenose goby were discovered in 2010 in Flanders and have since spread rapidly over canals and larger rivers Currently, round goby is recorded in at least 20 sites while western tubenose goby is present in over 30 sites in ever increasing numbers Most likely pathways for round goby introduction seem to be ballast water and natural distribution and probably multiple introductions occurred Most likely pathway for tubenose goby introduction through natural distribution Life-history traits show trends to fast population growth: high GSI and early maturity => increased reproductive allocation Two new haplotypes (1 round goby and 1 tubenose goby) were discovered Two new Gyrodactylus species were introduced together with round and tubenose goby 19

Acknowledgments My co-authors Yves, Isabelle, Linde, Adinda and the Groenendaal fishing team for helping with sampling and processing 20