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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

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Round and tubenose goby in Flanders

Introduction

ResultsDistribution

Life-history traits

Parasites

Phylogeography

Conclusions

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Round and tubenose goby in Flanders

IntroductionBoth 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

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Round and tubenose goby in Flanders

Material and MethodsElectrofishing, fyke nets and angling (April – May 2012)Ageing: scalesSex determined externally and by dissectionAge-at-maturity by formula of DeMasterGSI= 100 x W(gonads)/(W(body)-W(gonads)) Length-weight relationship W=log a + b logLs

DNA-sequencing: no. and diversity of haplotypesMaximum Likelihood trees

Round goby in Flanders

Distribution round goby

6Maps: Kornis, Mercado-Silva and Vander Zanden (J.Fish.Biol., 2012)

Native: Black, Caspian and Azov SeasIntroduced: Baltic Sea

Laurentian Great LakesRest of Europe (The Netherlands, France, Germany, Austria Poland, Czech Republic, Hungary, Slovakia, Bulgaria, Serbia, Romania, Estonia, and Sweden)

The Netherlands

Belgium

Distribution round goby in Belgium

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1st specimen (2010)

1st specimen (2010)

Secondary introduction?

Secondary introduction?

Life-history traits round goby

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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 Ls 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)

Ectoparasite fauna

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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

1 new Gyrodactylus species on round goby (highest similarity with Gyrodactyluskobayashii (from Carassius gibelio)(Poland & UK))

Nfish Np 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

Table: Number of fish (Nfish), number of ectoparasites (Np), prevalence, abundance and infection intensity per site.

Infection intensity = Number of adult parasites per infected round gobyAbundance = Total number of parasites per round goby including uninfected specimensPrevalence = Percentage of infected round gobies on total number of round gobies investigated at each site

Phylogeographic data-analysis

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Low haplotype (gene) diversity (Hd: 0,212) and nucleotide diversity (Pi: 0.00033)

3 haplotypes => multiple introductions?

# samples # haplotypes Hd Pi

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

Hd = haplotype diversity, Pi = nucleotide diversity

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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

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-TerneuzenNo matches => unique haplotype (related to H1)

H3

H2

H1

Brown & Stepien (2009) Invasion genetics of the Eurasian round goby in North America: tracing sources and spread patterns

Phylogeographic data-analysis

Tubenose goby in Flanders

Distribution tubenose goby

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Native: Black Sea basin; Maritza and Struma drainages in eastern Aegean basin; in South Bug and Dniepr

native far upriverIntroduced: 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

Miller, 2004

Distribution tubenose goby in Belgium

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1st specimen (2010)

1st specimen (2010)

The Netherlands

Wallonia

Flanders

Life-history traits tubenose goby

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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 Ls at age (mm)(N = 233)

Mean Ls was significantly smaller than in native range

GSI was high (♀ = 5.46;♂ = 4.01)

Ectoparasite fauna

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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 Gyrodactyluscf. niger (from North Sea; undescribed species))

Nfish Np 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 xZuid‐Willemsvaart 28 58 82,14 2,07 2,52

Table: Number of fish (Nfish), number of ectoparasites (Np), prevalence, abundance and infection intensity per site.

Phylogeographic data-analysis

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2 haplotypes

Low haplotype (gene) diversity (Hd: 0.049) and nucleotide diversity (Pi: 0.00117)

# samples # haplotypes Hd Pi

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

Hd = haplotype diversity, Pi = nucleotide diversity

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Low haplotype (gene) diversity (Hd: 0.049) and nucleotide diversity (Pi: 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

H1H2

Neilson & Stepien (2009) Evolution and phylogeography of the tubenose goby genus Proterorhinus (Gobiidae: Teleostei): evidence for new cryptic species'

Phylogeographic data-analysis

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

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Acknowledgments

My co-authors

Yves, Isabelle, Linde, Adinda and ‘the Groenendaal fishing team’ for helping with sampling and processing