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Predator and prey the role of the round gobyNeogobius melanostomus in the western Baltic

Daniel Oesterwind Christiane Bock Anja Foumlrster Michael Gabel ChristinaHenseler Paul Kotterba Marion Menge Dennis Myts amp Helmut M Winkler

To cite this article Daniel Oesterwind Christiane Bock Anja Foumlrster Michael Gabel ChristinaHenseler Paul Kotterba Marion Menge Dennis Myts amp Helmut M Winkler (2017) Predator andprey the role of the round goby Neogobiusmelanostomus in the western Baltic Marine BiologyResearch 132 188-197 DOI 1010801745100020161241412

To link to this article httpsdoiorg1010801745100020161241412

copy 2017 The Author(s) Published by InformaUK Limited trading as Taylor amp FrancisGroup

Published online 09 Jan 2017

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ORIGINAL ARTICLE

Predator and prey the role of the round goby Neogobius melanostomus in thewestern BalticDaniel Oesterwinda Christiane Bockab Anja Foumlrsterb Michael Gabelab Christina Henselerabc Paul KotterbaaMarion Mengeb Dennis Mytsb and Helmut M Winklerb

aThuumlnen Institute of Baltic Sea Fisheries Thuumlnen Institute Rostock Germany bAllgemeine amp Spezielle Zoologie Institute of BioscienceUniversity of Rostock Rostock Germany cEnvironmental and Marine Biology Aringbo Akademi University Aringbo Finland

ABSTRACTDifferent studies on the position of the non-indigenous species Neogobius melanostomus withinthe coastal food web of the Pomeranian Bay (western Baltic) were performed resulting in aquantitative and qualitative species list of prey organisms found in the stomachs of theinvader and an estimation concerning the importance of round goby as prey for differentresident predators It seems that the colonization process is not fully completed yet but theresults reveal that the species is already established in the food web 16 years after the firstobservation within the study area The results show that N melanostomus feed upon a widerange of different resident organisms While a direct predation effect on native fish speciesappears rather unlikely indirect effects such as competition cannot yet be excluded Inaddition our results reveal an ontogenetic diet shift and that the round goby itself alreadyserves as an important prey for piscivorous fish and seabirds Finally we formulate differenthypotheses based on our results which will require further research

ARTICLE HISTORYReceived 6 May 2016Accepted 20 September 2016Published online 9 January2017

RESPONSIBLE EDITORDavid Thieltges

KEYWORDSFoodweb invasive speciesbiodiversity colonizationdiet shift

Introduction

Non-indigenous species often pose a severe threat tothe native brackish water fauna in the Baltic Sea (Leppauml-koski amp Olenin 2000 2001) One of the most prominentinvasive species is the euryhaline round goby Neogobiusmelanostomus (Pallas 1814) Native to the Caspian SeaBlack Sea and the adjacent Sea of Azov (Svetovidov1964 Miller 1986) it has been introduced into variouslocations (Kornis et al 2012) In 1990 the round gobywas first recorded in the St Clair River in NorthAmerica and has spread throughout the Great Lakessince then (Jude et al 1992 1995) In Central Europethe species was observed first in the Baltic Sea (Skoacuteraamp Stolarski 1993) in 1990 and later in several river andcanal systems (Wiesner 2005 van Beek 2006 Borcherd-ing et al 2011 Piria et al 2011 Verreycken et al 2011Brunken et al 2012 Hempel amp Thiel 2013 Jacobs amp Hoe-demakers 2013 Schomaker amp Wolter 2014) In the BalticSea round gobies were first caught in the Gulf ofGdansk in 1990 (Skoacutera amp Stolarski 1993 1996) and hadbecome one of the dominant species in the westernpart of the Gulf by 1999 (Sapota amp Skoacutera 2005) The inva-sion expanded in a northeasterly direction towards the

Curonian Lagoon (Rakauskas et al 2013) the Gulf ofRiga and the Gulf of Finland (Ojaveer 2006) as well asin a westerly direction (Winkler et al 2000 Winkler2006 Czugała amp Woźniczka 2010 Schomaker amp Wolter2014) While several studies about the invasive processin the Great Lakes were published within recentdecades (eg Barton et al 2005 Lederer et al 2006Raby et al 2010 Kipp et al 2012 Kipp amp Ricciardi2012) the invasive process in the Baltic has beentreated as a lsquoCinderella subjectrsquo and in comparisonfewer studies were published (eg Janssen amp Jude2001 Barton et al 2005 Lederer et al 2006 Coppet al 2008 Raby et al 2010 Kipp et al 2012 Kipp amp Ric-ciardi 2012 Sapota et al 2014 Kotta et al 2016) This hasled to an opportunity to investigate the invasive andcolonization process of a new species However insome areas the invasion process is still ongoing andshould be investigated One of those regions exhibitingan ongoing invasion process is the western part of theBaltic where our studies were performed The firstoccurrence of N melanostomus in our study area wasobserved in 1999 In recent years the species spreadout rapidly and abundances increased (Winkler et al2015) Presuming that the species must already be

copy 2017 The Author(s) Published by Informa UK Limited trading as Taylor amp Francis GroupThis is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License (httpcreativecommonsorglicensesby-nc-nd40) which permits non-commercial re-use distribution and reproduction in any medium provided the original work is properly cited and is not altered transformed orbuilt upon in any way

CONTACT Daniel Oesterwind danieloesterwindthuenende Thuumlnen Institute of Baltic Sea Fisheries Thuumlnen Institute Alter Hafen Suumld 2 18069Rostock Germany

MARINE BIOLOGY RESEARCH 2017VOL 13 NO 2 188ndash197httpdxdoiorg1010801745100020161241412

Published online 09 Jan 2017

established in the local food web to achieve theobserved successful colonization of the area wepresent a synergistic compilation of several casestudies ndash each focusing on a particular aspect of the tro-phodynamic interactions between the round goby andthe food web in the Pomeranian Bay and adjacentwaters Combining different adapted techniques wefocused on important native components of the investi-gated ecosystem and examined their specific inter-action with N melanostomus

Materials and methods

Top-down effect

To investigate the prey ofNeogobiusmelanostomus twodifferent study sites in the Pomeranian Bay and adjacentwaters were investigated (Figure 1 Case Study 1) includ-ing a semi-enclosed inshore lagoon (Greifswald Bay)and an area close to the Oderbank Plateau At the firstsite (inshore) round goby samples were taken in threedifferent habitat types using a beam trawl in AugustOctober and November 2014 Habitat types includedthe lsquoPotamogeton zonersquo between 1 and 2 m waterdepth the lsquoZostera zonersquo at 3ndash4 m depth and the

lsquoSubphytal zonersquo between 5 and 7 m water depthSpecies from Oderbank Plateau were sampled withmulti-mesh gillnets at around 5 10 and 20 m depthsin May and November 2014 (Figure 1 Case Study 1)

Another round goby sampling was performed fromMay2011 until July 2012 at the inshore lagoon (lsquoPotamo-geton zonersquo) and the area of the Oderbank Plateau atdepths up to 14 mwith a beach seine and trawl respect-ively (Figure 1 Case Study 2) In the laboratory roundgobies for both studies were measured for total lengthand stomach contents were examined Gobies were dis-sected ventrally and the stomachs separated from theremaining digestive tract Only prey organisms thathad been in the stomach were identified to the lowestpossible taxonomic level For samples from 2014 thepresenceabsence of the single prey taxa was notedfor each fish dissected and afterwards the percentageof specific prey taxa was calculated for each individualgoby For samples from 2011 and 2012 the frequencyof occurrence of prey taxa was noted per length class

Bottom-up effect

To examine the bottom-up effect of the invasive Neo-gobius melanostomus stomach content analyses of

Figure 1 Sampling stations of cormorant pellets round gobies and piscivorous fish in the Pomeranian Bay Numbers indicate thecase study number

MARINE BIOLOGY RESEARCH 189

piscivorous fish and analyses of pellets of the cormor-ant Phalacrocorax carbo (Linnaeus 1758) from thePomeranian Bay were investigated The fish weresampled by different techniques (bottom trawlgillnet) at several locations during the year where anoccurrence of round gobies was noted (Figure 1 CaseStudy 3) Total length of piscivorous fish was measuredto the nearest 05 cm individuals were dissected ven-trally and the stomach was separated Afterwardsstomach contents were identified to the lowest poss-ible taxon When prey individuals were intact the wetweight and length were noted otherwise individuallengths and weights were estimated using empiricallycharacterized relations between total lengthbiomassand otoliths or other skeleton fragments from the lit-erature andor the local reference collection (Haumlrkoumlnen1986 Debus amp Winkler 1996 Leopold et al 2001 Myts2012) The diet composition was calculated as Ni ()individual number Wi () as the reconstructedweight and Fi () as the frequency of occurrence ofprey taxon i These three parameters were combinedto calculate the Index of Relative Importance (IRI) asused by George amp Hadley (1979)

IRI = Ni +Wi + Fisum(Ni + Wi + Fi)

times 100

For the prey analysis of piscivorous birds cormorantpellets were sampled between 2010 and 2015 Thepellets were collected during the breeding season(between March and October) near Peenemuumlnde inthe PomeranianBay (Figure 1 Case Study 4)Whenposs-ible 30 or more pellets were collected at least once amonth with fresh and intact pellets being preferred toolder andor damaged pellets After sampling pelletswere washed so that macerated pellet contents andprey items could be identified more efficiently Allprey items were identified to the lowest possibletaxon At least length and biomass of prey individualswere recalculated via published and non-publishedregressions based on the identified otoliths and bonyprey remains Regressions for otoliths and lengths andweights for the round goby were calculated accordingto Menge (2012)

Results

Top-down effect

Roundgobieswere found at each sample site except at adepth of 20 m on the Oderbank Plateau The length andweight of each round goby was measured and individ-uals were assigned to different length classes (le50 mm 51ndash100 mm 101ndash150 mm 151ndash200 mm and

201ndash250 mm) When available a maximum of 10stomachs per length class and haul were analysedfrom the beam trawls and 20 stomachs per lengthclass and depth contour were examined from thegillnet survey A total of 1192 individuals were caughtwith 249 stomachs being analysed in the first casestudy of which 47 were empty (Table I) Individuals atboth study sites from Case Study 1 consumed a varietyof prey organisms In general polychaetes belongingto the family Nereididae Blainville 1818 were identifiedin stomachs Arthropod prey items included insects andcrustaceanswhich comprised several taxonomicgroupsas well Neogobius melanostomus fed on cladocerans(Bosmina) ostracods and copepods but also on amphi-pods such as Gammaridae isopods as Idotea chelipes(Pallas 1766) decapods includingCrangon crangon (Lin-naeus 1758) and Palaemon sp and Balanidae Theround goby diet also included bivalves such asMya are-naria Linnaeus 1758 Cerastoderma spp Limecolabalthica (Linnaeus 1758) and Mytilus sp whereas gas-tropods included hydrobiids Peringia ulvae (Pennant1777) andor Ecrobia ventrosa (Montagu 1803) and Lit-torina spp On the Oderbank Plateau round gobies alsoconsumed Halicryptus spinulosus (von Siebold 1849)which belong to the family Priapulidae In the inshorelagoon (Greifswald Bay) the diet of smaller individuals(lt 50 mm TL) predominantly included ostracods cope-pods and cladocerans Larger round gobies (gt100 mmTL) increasingly consumed polychaetes and molluscsNeogobius melanostomus from the Pomeranian Bay(Oderbank Plateau) with a mean total length of 1113plusmn 135 mm for females and 1505 plusmn 317 mm for malesfed on crustaceans such as C crangon and Palaemonsp However molluscs were consumed more oftenthan all other prey items such as arthropods annelidsand priapulids Mytilus sp and hydrobiid gastropodswere identified as the most important prey itemsfound in the stomachs of fish from the OderbankPlateau From the sampling in 2011 and 2012 (CaseStudy 2) a total of 115 round gobies were randomlyselected depending on their length class so thataround 20 stomachs per length class if available wereanalysed resulting in 17 empty and 98 full or partly fullstomachs In addition to the above results the analysesof prey occurrence of distinct length classes showed anontogenetic diet shift Crustaceans dominated thestomachcontents of smaller individualswhile theoccur-rence of molluscs increased with body length (Figure 2)

Bottom-up effect

In addition to the stomach analysis of round gobies atotal of 321 individuals of piscivorous fish were analysed

190 D OESTERWIND ET AL

Table I Detailed information about investigated round gobies (RG) and respective stomach contents from Case Study 1

Location Littoral zone Oderbank Plateau

August October November May November

Depth (m) sim15 sim25 sim15 sim35 sim6 sim15 sim35 sim6 sim5 sim10 sim5 sim10

RG mean total length (mm) 434 (plusmn229) 346 (plusmn111) 390 (plusmn130) 275 (plusmn41) 243 (plusmn54) 374 (plusmn67) 370 (plusmn70) 293 (plusmn132) 12877 (plusmn3299) 12395 (plusmn3236) 14873 (plusmn2449) 13692 (plusmn2527)Total number of RG 156 89 89 10 25 266 3 4 503 19 15 13Investigated stomachs 19 26 34 9 11 31 3 4 65 19 15 13Empty stomachs 7 4 3 1 3 8 0 0 13 4 4 0Prey presence Polychaeta 26 19 15 0 9 35 0 25 21 7 0 15Nereididae 11 4 3 0 0 32 0 25 13 0 0 15Arthropoda 95 62 88 100 100 84 100 75 44 47 64 38Amphipoda 26 12 3 0 0 19 0 0 0 0 0 0Corophium sp 0 4 0 0 0 6 0 0 0 0 0 0Gammaridae 5 0 3 0 0 10 0 0 0 0 0 0Bosmina sp 0 0 9 0 0 45 0 0 0 0 0 0Copepoda 21 4 59 33 0 77 67 75 0 0 0 0Balanidae 0 0 0 0 0 0 0 0 23 20 55 31Crangon crangon 0 0 0 0 0 0 0 0 0 0 9 15Palaemon sp 0 0 0 15Insecta 21 4 15 0 0 6 33 0 0 0 0 0Chironomidae 16 0 15 0 0 6 33 0 0 0 0 0Isopoda 32 8 21 0 0 0 0 0 0 0 0 0Cyathura carinata 0 0 3 0 0 0 0 0 0 0 0 0Idotea chelipes 32 0 18 0 0 0 0 0 0 0 0 0Ostracoda 11 12 44 100 100 29 67 25 0 0 0 0Mollusca 37 69 21 56 82 0 33 25 98 93 100 100Bivalvia 26 46 9 0 55 0 33 25 85 80 45 62Cerastoderma sp 0 4 0 0 45 0 0 0 27 27 0 31Limecola balthica 5 0 3 0 9 0 0 0 4 7 0 0Mya arenaria 11 4 3 0 9 0 0 0 27 0 27 15Mytilus sp 11 4 3 0 0 0 0 0 67 73 36 31Gastropoda 11 35 15 56 64 0 0 0 92 67 82 92Hydrobiid gastropods 11 31 6 0 0 0 0 0 92 67 82 92Littorina sp 0 0 6 44 64 0 0 0Priapulidae 0 0 0 0 0 0 0 0 12 7 0 0Halicryptus spinulosus 0 0 0 0 0 0 0 0 12 7 0 0

Prey presence is the percentage of the taxa (per line and column) occurring in non-empty stomachs based on presenceabsence analysis

MARIN

EBIO

LOGYRESEA

RCH

191

(Table II Case Study 3) Stomachs from Scophthalmusmaximus (Linnaeus 1758) and Gymnocephalus cernuus(Linnaeus 1758) contained prey items but no Neogo-bius melanostomus were detected However stomachsfrom Perca fluviatilis Linnaeus 1758 and Sander lucio-perca (Linnaeus 1758) included N melanostomusbesides other prey species The IRI shows thatN melanostomus became an important prey item forS lucioperca and P fluviatilis during the last years ofthe invasion process (Figure 3) These results were veri-fied by determining the number the frequency ofoccurrence and the biomass of the food items Further-more N melanostomus was found in the stomachs ofS lucioperca and P fluviatilis at all sampling sitesWhereas S lucioperca caught in the Odra estuary hadthe highest number of N melanostomus in theirstomachs the IRI of N melanostomus calculated forP fluviatilis was highest from this location In thisstudy S lucioperca with a total length of 30ndash38 cmand P fluviatilis with a total length of 20ndash30 cm hadingested the highest number of N melanostomus

Moreover the analysis of 1048 (103ndash263 per year)cormorant pellets (Case Study 4) shows that the

occurrence of N melanostomus in the pellets hasincreased significantly over recent years (Pearsonrsquos rp = 0009) In 2010 the first round gobies wereobserved in the pellets however the percentage of

Figure 2 Frequency of occurrence of different prey taxa for different length classes Case Study 2 Numbers in brackets indicate thenumber of non-empty analysed round goby stomachs

Table II Information about analysed piscivorous fish species (Case Study 3)Species Geographical area Number Total number Non-empty stomachs

Scophthalmus maximus (Linnaeus 1758) Pomeranian Bay 8 8 8Perca fluviatilis Linnaeus 1758 Pomeranian Bay 91 186 104

Greifswald Bay 19Saaler Bodden amp Darss-Zingst Lagoon 44Odra estuary 32

Sander lucioperca (Linnaeus 1758) Greifswald Bay 28 89 57Pomeranian Bay 29Odra estuary 32

Gymnocephalus cernuus (Linnaeus 1758) Greifswald Bay 3 38 12Pomeranian Bay 35

Figure 3 Diet composition of Perca fluviatilis in black (n = 104)and Sander lucioperca in grey (n = 57) expressed as Index ofRelative Importance

192 D OESTERWIND ET AL

biomass was very small Over the following three yearsthe occurrence of N melanostomus within the pelletsincreased considerably especially between 2012 and2013 (Figure 4) In recent years the biomass ofN melanostomus represented about 35 of the esti-mated pellet biomass This shows thatN melanostomus became an important perhaps themost important prey of the cormorants at that locationduring the breeding season In contrast the biomass ofother prey organisms decreased over the last six years

With an occurrence of 20 for example roach Rutilusrutilus (Linnaeus 1758) was the most important preyin 2010 while the percentage was only around 4 in2015 (Figure 5)

Discussion

Despite the emergence of modern techniques such asmeasuring stable isotopes and fatty acid analyses clas-sical stomach content analysis remains an irreplaceablemethod to investigate fish feeding ecology mainly dueto the advantage that prey items can be determined tolower taxonomic levels (Cresson et al 2014) Howeverit has to be considered that prey items are sometimesvery difficult to identify depending on their degree ofdigestion (Hyslop 1980) and that some species couldbe overestimated due to indigestible fractions(Hyslop 1980 Baker et al 2014) In our study the per-centage of bivalves might be overvalued in the dietof round goby because their shells are indigestibleand have a longer retention time in stomachs com-pared to soft-bodied prey Moreover they are easierto identify (Coulter et al 2011 Brush et al 2012)Another critical aspect is that the digestive processcontinues during the catch period (Baker et al 2014)therefore fish were frozen immediately after captureand the fishing time of the gillnets was minimized toless than 24 hours However even if the stomachcontent analyses present only a snapshot of thespeciesrsquo diet and describe what the individual has con-sumed over a certain time span the results of this study

Figure 4 Number of individuals and estimated biomass ofround goby as percentage of the total number and biomassof the cormorant pellets for 2010ndash2015 in Peenemuumlnde(Case Study 4) (Stark 2011 Myts 2012 Winkler et al 2014)Number of analysed cormorant pellets 2010 = 263 2011 =221 2012 = 184 2013 = 164 2014 = 103 2015 = 113

Figure 5 Abundance of fish species in cormorant pellets from 2010 (first appearance of round goby in prey) compared to 2015(Case Study 4) Data for 2010 modified from Stark (2011) Number of analysed cormorant pellets 2010 = 263 2015 = 113

MARINE BIOLOGY RESEARCH 193

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

piscivorous fish and analyses of pellets of the cormor-ant Phalacrocorax carbo (Linnaeus 1758) from thePomeranian Bay were investigated The fish weresampled by different techniques (bottom trawlgillnet) at several locations during the year where anoccurrence of round gobies was noted (Figure 1 CaseStudy 3) Total length of piscivorous fish was measuredto the nearest 05 cm individuals were dissected ven-trally and the stomach was separated Afterwardsstomach contents were identified to the lowest poss-ible taxon When prey individuals were intact the wetweight and length were noted otherwise individuallengths and weights were estimated using empiricallycharacterized relations between total lengthbiomassand otoliths or other skeleton fragments from the lit-erature andor the local reference collection (Haumlrkoumlnen1986 Debus amp Winkler 1996 Leopold et al 2001 Myts2012) The diet composition was calculated as Ni ()individual number Wi () as the reconstructedweight and Fi () as the frequency of occurrence ofprey taxon i These three parameters were combinedto calculate the Index of Relative Importance (IRI) asused by George amp Hadley (1979)

IRI = Ni +Wi + Fisum(Ni + Wi + Fi)

times 100

For the prey analysis of piscivorous birds cormorantpellets were sampled between 2010 and 2015 Thepellets were collected during the breeding season(between March and October) near Peenemuumlnde inthe PomeranianBay (Figure 1 Case Study 4)Whenposs-ible 30 or more pellets were collected at least once amonth with fresh and intact pellets being preferred toolder andor damaged pellets After sampling pelletswere washed so that macerated pellet contents andprey items could be identified more efficiently Allprey items were identified to the lowest possibletaxon At least length and biomass of prey individualswere recalculated via published and non-publishedregressions based on the identified otoliths and bonyprey remains Regressions for otoliths and lengths andweights for the round goby were calculated accordingto Menge (2012)

Results

Top-down effect

Roundgobieswere found at each sample site except at adepth of 20 m on the Oderbank Plateau The length andweight of each round goby was measured and individ-uals were assigned to different length classes (le50 mm 51ndash100 mm 101ndash150 mm 151ndash200 mm and

201ndash250 mm) When available a maximum of 10stomachs per length class and haul were analysedfrom the beam trawls and 20 stomachs per lengthclass and depth contour were examined from thegillnet survey A total of 1192 individuals were caughtwith 249 stomachs being analysed in the first casestudy of which 47 were empty (Table I) Individuals atboth study sites from Case Study 1 consumed a varietyof prey organisms In general polychaetes belongingto the family Nereididae Blainville 1818 were identifiedin stomachs Arthropod prey items included insects andcrustaceanswhich comprised several taxonomicgroupsas well Neogobius melanostomus fed on cladocerans(Bosmina) ostracods and copepods but also on amphi-pods such as Gammaridae isopods as Idotea chelipes(Pallas 1766) decapods includingCrangon crangon (Lin-naeus 1758) and Palaemon sp and Balanidae Theround goby diet also included bivalves such asMya are-naria Linnaeus 1758 Cerastoderma spp Limecolabalthica (Linnaeus 1758) and Mytilus sp whereas gas-tropods included hydrobiids Peringia ulvae (Pennant1777) andor Ecrobia ventrosa (Montagu 1803) and Lit-torina spp On the Oderbank Plateau round gobies alsoconsumed Halicryptus spinulosus (von Siebold 1849)which belong to the family Priapulidae In the inshorelagoon (Greifswald Bay) the diet of smaller individuals(lt 50 mm TL) predominantly included ostracods cope-pods and cladocerans Larger round gobies (gt100 mmTL) increasingly consumed polychaetes and molluscsNeogobius melanostomus from the Pomeranian Bay(Oderbank Plateau) with a mean total length of 1113plusmn 135 mm for females and 1505 plusmn 317 mm for malesfed on crustaceans such as C crangon and Palaemonsp However molluscs were consumed more oftenthan all other prey items such as arthropods annelidsand priapulids Mytilus sp and hydrobiid gastropodswere identified as the most important prey itemsfound in the stomachs of fish from the OderbankPlateau From the sampling in 2011 and 2012 (CaseStudy 2) a total of 115 round gobies were randomlyselected depending on their length class so thataround 20 stomachs per length class if available wereanalysed resulting in 17 empty and 98 full or partly fullstomachs In addition to the above results the analysesof prey occurrence of distinct length classes showed anontogenetic diet shift Crustaceans dominated thestomachcontents of smaller individualswhile theoccur-rence of molluscs increased with body length (Figure 2)

Bottom-up effect

In addition to the stomach analysis of round gobies atotal of 321 individuals of piscivorous fish were analysed

190 D OESTERWIND ET AL

Table I Detailed information about investigated round gobies (RG) and respective stomach contents from Case Study 1

Location Littoral zone Oderbank Plateau

August October November May November

Depth (m) sim15 sim25 sim15 sim35 sim6 sim15 sim35 sim6 sim5 sim10 sim5 sim10

RG mean total length (mm) 434 (plusmn229) 346 (plusmn111) 390 (plusmn130) 275 (plusmn41) 243 (plusmn54) 374 (plusmn67) 370 (plusmn70) 293 (plusmn132) 12877 (plusmn3299) 12395 (plusmn3236) 14873 (plusmn2449) 13692 (plusmn2527)Total number of RG 156 89 89 10 25 266 3 4 503 19 15 13Investigated stomachs 19 26 34 9 11 31 3 4 65 19 15 13Empty stomachs 7 4 3 1 3 8 0 0 13 4 4 0Prey presence Polychaeta 26 19 15 0 9 35 0 25 21 7 0 15Nereididae 11 4 3 0 0 32 0 25 13 0 0 15Arthropoda 95 62 88 100 100 84 100 75 44 47 64 38Amphipoda 26 12 3 0 0 19 0 0 0 0 0 0Corophium sp 0 4 0 0 0 6 0 0 0 0 0 0Gammaridae 5 0 3 0 0 10 0 0 0 0 0 0Bosmina sp 0 0 9 0 0 45 0 0 0 0 0 0Copepoda 21 4 59 33 0 77 67 75 0 0 0 0Balanidae 0 0 0 0 0 0 0 0 23 20 55 31Crangon crangon 0 0 0 0 0 0 0 0 0 0 9 15Palaemon sp 0 0 0 15Insecta 21 4 15 0 0 6 33 0 0 0 0 0Chironomidae 16 0 15 0 0 6 33 0 0 0 0 0Isopoda 32 8 21 0 0 0 0 0 0 0 0 0Cyathura carinata 0 0 3 0 0 0 0 0 0 0 0 0Idotea chelipes 32 0 18 0 0 0 0 0 0 0 0 0Ostracoda 11 12 44 100 100 29 67 25 0 0 0 0Mollusca 37 69 21 56 82 0 33 25 98 93 100 100Bivalvia 26 46 9 0 55 0 33 25 85 80 45 62Cerastoderma sp 0 4 0 0 45 0 0 0 27 27 0 31Limecola balthica 5 0 3 0 9 0 0 0 4 7 0 0Mya arenaria 11 4 3 0 9 0 0 0 27 0 27 15Mytilus sp 11 4 3 0 0 0 0 0 67 73 36 31Gastropoda 11 35 15 56 64 0 0 0 92 67 82 92Hydrobiid gastropods 11 31 6 0 0 0 0 0 92 67 82 92Littorina sp 0 0 6 44 64 0 0 0Priapulidae 0 0 0 0 0 0 0 0 12 7 0 0Halicryptus spinulosus 0 0 0 0 0 0 0 0 12 7 0 0

Prey presence is the percentage of the taxa (per line and column) occurring in non-empty stomachs based on presenceabsence analysis

MARIN

EBIO

LOGYRESEA

RCH

191

(Table II Case Study 3) Stomachs from Scophthalmusmaximus (Linnaeus 1758) and Gymnocephalus cernuus(Linnaeus 1758) contained prey items but no Neogo-bius melanostomus were detected However stomachsfrom Perca fluviatilis Linnaeus 1758 and Sander lucio-perca (Linnaeus 1758) included N melanostomusbesides other prey species The IRI shows thatN melanostomus became an important prey item forS lucioperca and P fluviatilis during the last years ofthe invasion process (Figure 3) These results were veri-fied by determining the number the frequency ofoccurrence and the biomass of the food items Further-more N melanostomus was found in the stomachs ofS lucioperca and P fluviatilis at all sampling sitesWhereas S lucioperca caught in the Odra estuary hadthe highest number of N melanostomus in theirstomachs the IRI of N melanostomus calculated forP fluviatilis was highest from this location In thisstudy S lucioperca with a total length of 30ndash38 cmand P fluviatilis with a total length of 20ndash30 cm hadingested the highest number of N melanostomus

Moreover the analysis of 1048 (103ndash263 per year)cormorant pellets (Case Study 4) shows that the

occurrence of N melanostomus in the pellets hasincreased significantly over recent years (Pearsonrsquos rp = 0009) In 2010 the first round gobies wereobserved in the pellets however the percentage of

Figure 2 Frequency of occurrence of different prey taxa for different length classes Case Study 2 Numbers in brackets indicate thenumber of non-empty analysed round goby stomachs

Table II Information about analysed piscivorous fish species (Case Study 3)Species Geographical area Number Total number Non-empty stomachs

Scophthalmus maximus (Linnaeus 1758) Pomeranian Bay 8 8 8Perca fluviatilis Linnaeus 1758 Pomeranian Bay 91 186 104

Greifswald Bay 19Saaler Bodden amp Darss-Zingst Lagoon 44Odra estuary 32

Sander lucioperca (Linnaeus 1758) Greifswald Bay 28 89 57Pomeranian Bay 29Odra estuary 32

Gymnocephalus cernuus (Linnaeus 1758) Greifswald Bay 3 38 12Pomeranian Bay 35

Figure 3 Diet composition of Perca fluviatilis in black (n = 104)and Sander lucioperca in grey (n = 57) expressed as Index ofRelative Importance

192 D OESTERWIND ET AL

biomass was very small Over the following three yearsthe occurrence of N melanostomus within the pelletsincreased considerably especially between 2012 and2013 (Figure 4) In recent years the biomass ofN melanostomus represented about 35 of the esti-mated pellet biomass This shows thatN melanostomus became an important perhaps themost important prey of the cormorants at that locationduring the breeding season In contrast the biomass ofother prey organisms decreased over the last six years

With an occurrence of 20 for example roach Rutilusrutilus (Linnaeus 1758) was the most important preyin 2010 while the percentage was only around 4 in2015 (Figure 5)

Discussion

Despite the emergence of modern techniques such asmeasuring stable isotopes and fatty acid analyses clas-sical stomach content analysis remains an irreplaceablemethod to investigate fish feeding ecology mainly dueto the advantage that prey items can be determined tolower taxonomic levels (Cresson et al 2014) Howeverit has to be considered that prey items are sometimesvery difficult to identify depending on their degree ofdigestion (Hyslop 1980) and that some species couldbe overestimated due to indigestible fractions(Hyslop 1980 Baker et al 2014) In our study the per-centage of bivalves might be overvalued in the dietof round goby because their shells are indigestibleand have a longer retention time in stomachs com-pared to soft-bodied prey Moreover they are easierto identify (Coulter et al 2011 Brush et al 2012)Another critical aspect is that the digestive processcontinues during the catch period (Baker et al 2014)therefore fish were frozen immediately after captureand the fishing time of the gillnets was minimized toless than 24 hours However even if the stomachcontent analyses present only a snapshot of thespeciesrsquo diet and describe what the individual has con-sumed over a certain time span the results of this study

Figure 4 Number of individuals and estimated biomass ofround goby as percentage of the total number and biomassof the cormorant pellets for 2010ndash2015 in Peenemuumlnde(Case Study 4) (Stark 2011 Myts 2012 Winkler et al 2014)Number of analysed cormorant pellets 2010 = 263 2011 =221 2012 = 184 2013 = 164 2014 = 103 2015 = 113

Figure 5 Abundance of fish species in cormorant pellets from 2010 (first appearance of round goby in prey) compared to 2015(Case Study 4) Data for 2010 modified from Stark (2011) Number of analysed cormorant pellets 2010 = 263 2015 = 113

MARINE BIOLOGY RESEARCH 193

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

Table I Detailed information about investigated round gobies (RG) and respective stomach contents from Case Study 1

Location Littoral zone Oderbank Plateau

August October November May November

Depth (m) sim15 sim25 sim15 sim35 sim6 sim15 sim35 sim6 sim5 sim10 sim5 sim10

RG mean total length (mm) 434 (plusmn229) 346 (plusmn111) 390 (plusmn130) 275 (plusmn41) 243 (plusmn54) 374 (plusmn67) 370 (plusmn70) 293 (plusmn132) 12877 (plusmn3299) 12395 (plusmn3236) 14873 (plusmn2449) 13692 (plusmn2527)Total number of RG 156 89 89 10 25 266 3 4 503 19 15 13Investigated stomachs 19 26 34 9 11 31 3 4 65 19 15 13Empty stomachs 7 4 3 1 3 8 0 0 13 4 4 0Prey presence Polychaeta 26 19 15 0 9 35 0 25 21 7 0 15Nereididae 11 4 3 0 0 32 0 25 13 0 0 15Arthropoda 95 62 88 100 100 84 100 75 44 47 64 38Amphipoda 26 12 3 0 0 19 0 0 0 0 0 0Corophium sp 0 4 0 0 0 6 0 0 0 0 0 0Gammaridae 5 0 3 0 0 10 0 0 0 0 0 0Bosmina sp 0 0 9 0 0 45 0 0 0 0 0 0Copepoda 21 4 59 33 0 77 67 75 0 0 0 0Balanidae 0 0 0 0 0 0 0 0 23 20 55 31Crangon crangon 0 0 0 0 0 0 0 0 0 0 9 15Palaemon sp 0 0 0 15Insecta 21 4 15 0 0 6 33 0 0 0 0 0Chironomidae 16 0 15 0 0 6 33 0 0 0 0 0Isopoda 32 8 21 0 0 0 0 0 0 0 0 0Cyathura carinata 0 0 3 0 0 0 0 0 0 0 0 0Idotea chelipes 32 0 18 0 0 0 0 0 0 0 0 0Ostracoda 11 12 44 100 100 29 67 25 0 0 0 0Mollusca 37 69 21 56 82 0 33 25 98 93 100 100Bivalvia 26 46 9 0 55 0 33 25 85 80 45 62Cerastoderma sp 0 4 0 0 45 0 0 0 27 27 0 31Limecola balthica 5 0 3 0 9 0 0 0 4 7 0 0Mya arenaria 11 4 3 0 9 0 0 0 27 0 27 15Mytilus sp 11 4 3 0 0 0 0 0 67 73 36 31Gastropoda 11 35 15 56 64 0 0 0 92 67 82 92Hydrobiid gastropods 11 31 6 0 0 0 0 0 92 67 82 92Littorina sp 0 0 6 44 64 0 0 0Priapulidae 0 0 0 0 0 0 0 0 12 7 0 0Halicryptus spinulosus 0 0 0 0 0 0 0 0 12 7 0 0

Prey presence is the percentage of the taxa (per line and column) occurring in non-empty stomachs based on presenceabsence analysis

MARIN

EBIO

LOGYRESEA

RCH

191

(Table II Case Study 3) Stomachs from Scophthalmusmaximus (Linnaeus 1758) and Gymnocephalus cernuus(Linnaeus 1758) contained prey items but no Neogo-bius melanostomus were detected However stomachsfrom Perca fluviatilis Linnaeus 1758 and Sander lucio-perca (Linnaeus 1758) included N melanostomusbesides other prey species The IRI shows thatN melanostomus became an important prey item forS lucioperca and P fluviatilis during the last years ofthe invasion process (Figure 3) These results were veri-fied by determining the number the frequency ofoccurrence and the biomass of the food items Further-more N melanostomus was found in the stomachs ofS lucioperca and P fluviatilis at all sampling sitesWhereas S lucioperca caught in the Odra estuary hadthe highest number of N melanostomus in theirstomachs the IRI of N melanostomus calculated forP fluviatilis was highest from this location In thisstudy S lucioperca with a total length of 30ndash38 cmand P fluviatilis with a total length of 20ndash30 cm hadingested the highest number of N melanostomus

Moreover the analysis of 1048 (103ndash263 per year)cormorant pellets (Case Study 4) shows that the

occurrence of N melanostomus in the pellets hasincreased significantly over recent years (Pearsonrsquos rp = 0009) In 2010 the first round gobies wereobserved in the pellets however the percentage of

Figure 2 Frequency of occurrence of different prey taxa for different length classes Case Study 2 Numbers in brackets indicate thenumber of non-empty analysed round goby stomachs

Table II Information about analysed piscivorous fish species (Case Study 3)Species Geographical area Number Total number Non-empty stomachs

Scophthalmus maximus (Linnaeus 1758) Pomeranian Bay 8 8 8Perca fluviatilis Linnaeus 1758 Pomeranian Bay 91 186 104

Greifswald Bay 19Saaler Bodden amp Darss-Zingst Lagoon 44Odra estuary 32

Sander lucioperca (Linnaeus 1758) Greifswald Bay 28 89 57Pomeranian Bay 29Odra estuary 32

Gymnocephalus cernuus (Linnaeus 1758) Greifswald Bay 3 38 12Pomeranian Bay 35

Figure 3 Diet composition of Perca fluviatilis in black (n = 104)and Sander lucioperca in grey (n = 57) expressed as Index ofRelative Importance

192 D OESTERWIND ET AL

biomass was very small Over the following three yearsthe occurrence of N melanostomus within the pelletsincreased considerably especially between 2012 and2013 (Figure 4) In recent years the biomass ofN melanostomus represented about 35 of the esti-mated pellet biomass This shows thatN melanostomus became an important perhaps themost important prey of the cormorants at that locationduring the breeding season In contrast the biomass ofother prey organisms decreased over the last six years

With an occurrence of 20 for example roach Rutilusrutilus (Linnaeus 1758) was the most important preyin 2010 while the percentage was only around 4 in2015 (Figure 5)

Discussion

Despite the emergence of modern techniques such asmeasuring stable isotopes and fatty acid analyses clas-sical stomach content analysis remains an irreplaceablemethod to investigate fish feeding ecology mainly dueto the advantage that prey items can be determined tolower taxonomic levels (Cresson et al 2014) Howeverit has to be considered that prey items are sometimesvery difficult to identify depending on their degree ofdigestion (Hyslop 1980) and that some species couldbe overestimated due to indigestible fractions(Hyslop 1980 Baker et al 2014) In our study the per-centage of bivalves might be overvalued in the dietof round goby because their shells are indigestibleand have a longer retention time in stomachs com-pared to soft-bodied prey Moreover they are easierto identify (Coulter et al 2011 Brush et al 2012)Another critical aspect is that the digestive processcontinues during the catch period (Baker et al 2014)therefore fish were frozen immediately after captureand the fishing time of the gillnets was minimized toless than 24 hours However even if the stomachcontent analyses present only a snapshot of thespeciesrsquo diet and describe what the individual has con-sumed over a certain time span the results of this study

Figure 4 Number of individuals and estimated biomass ofround goby as percentage of the total number and biomassof the cormorant pellets for 2010ndash2015 in Peenemuumlnde(Case Study 4) (Stark 2011 Myts 2012 Winkler et al 2014)Number of analysed cormorant pellets 2010 = 263 2011 =221 2012 = 184 2013 = 164 2014 = 103 2015 = 113

Figure 5 Abundance of fish species in cormorant pellets from 2010 (first appearance of round goby in prey) compared to 2015(Case Study 4) Data for 2010 modified from Stark (2011) Number of analysed cormorant pellets 2010 = 263 2015 = 113

MARINE BIOLOGY RESEARCH 193

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

(Table II Case Study 3) Stomachs from Scophthalmusmaximus (Linnaeus 1758) and Gymnocephalus cernuus(Linnaeus 1758) contained prey items but no Neogo-bius melanostomus were detected However stomachsfrom Perca fluviatilis Linnaeus 1758 and Sander lucio-perca (Linnaeus 1758) included N melanostomusbesides other prey species The IRI shows thatN melanostomus became an important prey item forS lucioperca and P fluviatilis during the last years ofthe invasion process (Figure 3) These results were veri-fied by determining the number the frequency ofoccurrence and the biomass of the food items Further-more N melanostomus was found in the stomachs ofS lucioperca and P fluviatilis at all sampling sitesWhereas S lucioperca caught in the Odra estuary hadthe highest number of N melanostomus in theirstomachs the IRI of N melanostomus calculated forP fluviatilis was highest from this location In thisstudy S lucioperca with a total length of 30ndash38 cmand P fluviatilis with a total length of 20ndash30 cm hadingested the highest number of N melanostomus

Moreover the analysis of 1048 (103ndash263 per year)cormorant pellets (Case Study 4) shows that the

occurrence of N melanostomus in the pellets hasincreased significantly over recent years (Pearsonrsquos rp = 0009) In 2010 the first round gobies wereobserved in the pellets however the percentage of

Figure 2 Frequency of occurrence of different prey taxa for different length classes Case Study 2 Numbers in brackets indicate thenumber of non-empty analysed round goby stomachs

Table II Information about analysed piscivorous fish species (Case Study 3)Species Geographical area Number Total number Non-empty stomachs

Scophthalmus maximus (Linnaeus 1758) Pomeranian Bay 8 8 8Perca fluviatilis Linnaeus 1758 Pomeranian Bay 91 186 104

Greifswald Bay 19Saaler Bodden amp Darss-Zingst Lagoon 44Odra estuary 32

Sander lucioperca (Linnaeus 1758) Greifswald Bay 28 89 57Pomeranian Bay 29Odra estuary 32

Gymnocephalus cernuus (Linnaeus 1758) Greifswald Bay 3 38 12Pomeranian Bay 35

Figure 3 Diet composition of Perca fluviatilis in black (n = 104)and Sander lucioperca in grey (n = 57) expressed as Index ofRelative Importance

192 D OESTERWIND ET AL

biomass was very small Over the following three yearsthe occurrence of N melanostomus within the pelletsincreased considerably especially between 2012 and2013 (Figure 4) In recent years the biomass ofN melanostomus represented about 35 of the esti-mated pellet biomass This shows thatN melanostomus became an important perhaps themost important prey of the cormorants at that locationduring the breeding season In contrast the biomass ofother prey organisms decreased over the last six years

With an occurrence of 20 for example roach Rutilusrutilus (Linnaeus 1758) was the most important preyin 2010 while the percentage was only around 4 in2015 (Figure 5)

Discussion

Despite the emergence of modern techniques such asmeasuring stable isotopes and fatty acid analyses clas-sical stomach content analysis remains an irreplaceablemethod to investigate fish feeding ecology mainly dueto the advantage that prey items can be determined tolower taxonomic levels (Cresson et al 2014) Howeverit has to be considered that prey items are sometimesvery difficult to identify depending on their degree ofdigestion (Hyslop 1980) and that some species couldbe overestimated due to indigestible fractions(Hyslop 1980 Baker et al 2014) In our study the per-centage of bivalves might be overvalued in the dietof round goby because their shells are indigestibleand have a longer retention time in stomachs com-pared to soft-bodied prey Moreover they are easierto identify (Coulter et al 2011 Brush et al 2012)Another critical aspect is that the digestive processcontinues during the catch period (Baker et al 2014)therefore fish were frozen immediately after captureand the fishing time of the gillnets was minimized toless than 24 hours However even if the stomachcontent analyses present only a snapshot of thespeciesrsquo diet and describe what the individual has con-sumed over a certain time span the results of this study

Figure 4 Number of individuals and estimated biomass ofround goby as percentage of the total number and biomassof the cormorant pellets for 2010ndash2015 in Peenemuumlnde(Case Study 4) (Stark 2011 Myts 2012 Winkler et al 2014)Number of analysed cormorant pellets 2010 = 263 2011 =221 2012 = 184 2013 = 164 2014 = 103 2015 = 113

Figure 5 Abundance of fish species in cormorant pellets from 2010 (first appearance of round goby in prey) compared to 2015(Case Study 4) Data for 2010 modified from Stark (2011) Number of analysed cormorant pellets 2010 = 263 2015 = 113

MARINE BIOLOGY RESEARCH 193

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

biomass was very small Over the following three yearsthe occurrence of N melanostomus within the pelletsincreased considerably especially between 2012 and2013 (Figure 4) In recent years the biomass ofN melanostomus represented about 35 of the esti-mated pellet biomass This shows thatN melanostomus became an important perhaps themost important prey of the cormorants at that locationduring the breeding season In contrast the biomass ofother prey organisms decreased over the last six years

With an occurrence of 20 for example roach Rutilusrutilus (Linnaeus 1758) was the most important preyin 2010 while the percentage was only around 4 in2015 (Figure 5)

Discussion

Despite the emergence of modern techniques such asmeasuring stable isotopes and fatty acid analyses clas-sical stomach content analysis remains an irreplaceablemethod to investigate fish feeding ecology mainly dueto the advantage that prey items can be determined tolower taxonomic levels (Cresson et al 2014) Howeverit has to be considered that prey items are sometimesvery difficult to identify depending on their degree ofdigestion (Hyslop 1980) and that some species couldbe overestimated due to indigestible fractions(Hyslop 1980 Baker et al 2014) In our study the per-centage of bivalves might be overvalued in the dietof round goby because their shells are indigestibleand have a longer retention time in stomachs com-pared to soft-bodied prey Moreover they are easierto identify (Coulter et al 2011 Brush et al 2012)Another critical aspect is that the digestive processcontinues during the catch period (Baker et al 2014)therefore fish were frozen immediately after captureand the fishing time of the gillnets was minimized toless than 24 hours However even if the stomachcontent analyses present only a snapshot of thespeciesrsquo diet and describe what the individual has con-sumed over a certain time span the results of this study

Figure 4 Number of individuals and estimated biomass ofround goby as percentage of the total number and biomassof the cormorant pellets for 2010ndash2015 in Peenemuumlnde(Case Study 4) (Stark 2011 Myts 2012 Winkler et al 2014)Number of analysed cormorant pellets 2010 = 263 2011 =221 2012 = 184 2013 = 164 2014 = 103 2015 = 113

Figure 5 Abundance of fish species in cormorant pellets from 2010 (first appearance of round goby in prey) compared to 2015(Case Study 4) Data for 2010 modified from Stark (2011) Number of analysed cormorant pellets 2010 = 263 2015 = 113

MARINE BIOLOGY RESEARCH 193

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

regarding dietary composition of the round goby andround goby predators are assumed to represent areasonably accurate picture within the different casestudies

Our results show that the round goby preys upon avariety of resident species and shifts the choice of itsprey depending on its size The study reveals thatmainly crustaceans and molluscs were impacteddirectly by the introduction of round goby while fishwere rarely found in the stomachs Therefore a signifi-cant and direct impact on fish species appears ratherunlikely while an indirect impact on the resident fishcommunity due to competition could not be excludedat this stage and will be discussed later On the otherhand some piscivorous fish and bird species adaptedto the new food resource so that Neogobius melanosto-mus became an important food item

The percentage of successful invaders is difficult todetermine Statistics are rare and unsuccessful Non-Indigenous Species (NIS) are underrepresented aswell as the more easily observable species being over-represented (Lodge 1993) A review conducted byLodge (1993) presents a minimum rate of NIS establish-ment of 35 but others assume a rate of 10 (William-son amp Brown 1986 Williamson 1989) The colonizationsuccess of NIS depends on different factors but it isassumed that climate and predation are the mostimportant factors influencing the invasion processhowever competition diseases and other factors aredifficult to analyse and could therefore be undervalued(Crawley et al 1986 Lodge 1993) On the other handthe most important impact of introduced mammalson native species for example is caused by predationand habitat changes Ecological changes due to com-petition are less frequently documented probablydue to the challenging task of proving their actual sig-nificance (Ebenhard 1988) Based on different types offishing gear (eg bottom trawls beach seine) and inter-views with fishermen a chronological analysis of theround goby invasion in the eastern German part ofthe Baltic shows that N melanostomus has occurredin the German part of the Pomeranian Bay since 1999and spread out rapidly over recent years with anincreasing abundance at some sites (Winkler 2006Winkler et al 2015) Such a fast and successful coloniza-tion can only be feasible with a successful nichepartitioning together with the factors describedabove In addition our case studies reveal thatN melanostomus is already successfully established inthe food web of our study area and has already or iswell on the way to establishing itself within the ecosys-tem in the investigated area Therefore future workshould focus on the description of the niche and the

direct and indirect influence on native species andhabitats As an example apart from N melanostomuswe identified 12 other fish species within the inshoreand 19 other fish species within the offshore studyarea While our results support the findings of Thielet al (2014) that it can be excluded that roundgobies exert a high predation pressure on native fishspecies it can be assumed that there is already a poten-tial competition concerning space and food resourcesat least with some of the native species As ourresults show smaller N melanostomus feed upon crus-taceans while larger individuals prefer molluscs Asimilar feeding behaviour and therefore a potentialcompetition is assumed for Platichthys flesus (Linnaeus1758) and Vimba vimba (Linnaeus 1758) in the BalticSea Young of the year (YOY) flounders start feedingon small crustaceans larvae of chironomids and oligo-chaetes whereas they switch to polychaetes and mol-luscs at a body length of around 10 cm (Ojaveer ampDrevs 2003) YOY vimba bream feed on small crus-taceans molluscs (Hydrobia) and mainly on the poly-chaete Hediste diversicolor (OF Muumlller 1776) in thePaumlrnu Bay of the Baltic Sea Limecola balthica is domi-nant in the diet of larger vimba bream (Erm et al2003) In addition molluscs are also an importantfood for Rutilus rutilus (Vetemaa et al 2003) wherebya competition with N melanostomus may existKarlson et al (2007) describe a dietary overlapbetween small flounders and round gobies based onstomach contents stable isotope analyses and labexperiments and reveal a decrease of the flounderpopulation following the establishment of roundgoby in the area A comparison between stomach con-tents from 0 age flounders (Andersen et al 2005) andour results in addition to the known temporal andspatial overlap at our study sites supports the potentialdiet competition However besides the indirect dietcompetition with other fish species direct feeding con-sequences exerted by N melanostomus within the eco-system are still unknown As an example our data showthat isopods (Idotea chelipes) and hydrobiid gastropodswere regularly found in stomach contents of roundgoby within the inshore area Both prey species aregrazers within the macrophyte area (Schaffelke et al1995 Schanz et al 2000) and an induced decrease ofthese grazers due to N melanostomus predationcould have extensive consequences for the filamen-tous algae fouling on seagrass and other macrophytesand thus for the whole ecosystem Besides the negativeeffects on the native biodiversity our analyses of thecormorant pellets and stomach contents of piscivorousfishes show that the biomass of native species withinthe prey decreased which may have positive effects

194 D OESTERWIND ET AL

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

on the population of those resident species Forexample round goby is one of the most importantfood items for pikeperch in the Sea of Azov (Maiskij1955) Therefore it is not surprising that round gobyis now the most important food item for pikeperch inthe newly colonized Kiel Canal (Thiel et al 2014)Gobies also serve as an important food especially foryoung sea mammals According to Behnke et al(1998) 50 of the food biomass of the harbour por-poises Phocoena phocoena (Linnaeus 1758) in theBaltic Sea consists of gobies Hepner et al (1976)reviewed literature concerning the diet of harbour por-poises in the Black Sea and found that a total of 36 ofthe porpoisesrsquo food biomass consisted of gobiesincluding N melanostomus However an assumptionabout future consequences would be purely speculat-ive Therefore more fieldwork and experiments arenecessary to rate the consequences of the invasion ofround goby for native biodiversity in the coastal areain order to learn more about the impact of generalinvasion processes

Acknowledgements

We thank the BONUS Inspire project for the chance to samplethe round gobies from gillnets as well as Christoph Stark andDorothee Moll for their work and support We furthermorethank Dr Michael L Zettler for his taxonomic support andadvice as well as two unknown reviewers for their construc-tive criticism

Disclosure statement

No potential conflict of interest was reported by the authors

Funding

This work resulted from the BONUS Bio-C3 project and wassupported by BONUS (Art 185) funded jointly by the EUand national funding from the German Federal Ministry ofEducation and Research (BMBF) (grant no 03F0682B)

References

Andersen BS Carl JD Groslashnkjaeligr P Stoslashttrup JG 2005 Feedingecology and growth of age 0 year Platichthys flesus (L) in avegetated and a bare sand habitat in a nutrient rich fjordJournal of Fish Biology 66531ndash52 doi101111j0022-1112200500620x

Baker R Buckland A Sheaves M 2014 Fish gut contentanalysis robust measures of diet composition Fish andFisheries 15170ndash77 doi101111faf12026

Barton DR Johnson RA Campbell L Petruniak J Patterson M2005 Effects of round gobies (Neogobius melanostomus)on dreissenid mussels and other invertebrates in eastern

Lake Erie 2002ndash2004 Journal of Great Lakes Research 31(Suppl 2)252ndash61 doi101016S0380-1330(05)70318-X

Behnke H Siebert U Lick R Bandomir B Weiss R 1998 Thecurrent status of harbour porpoises (Phocoena phocoena)in German waters Archive of Fishery and MarineResearch 46(2)97ndash123

Borcherding J Staas S Kruumlger S Ondračkovaacute M Šlapanskyacute LJurajda P 2011 Non-native gobiid species in the lowerRiver Rhine (Germany) recent range extensions and den-sities Journal of Applied Ichthyology 27153ndash55 doi101111j1439-0426201001662x

Brunken H Castro J Hein M Verwold A Winkler HM 2012First records of round goby Neogobius melanostomus(Pallas 1814) in the river Weser Lauterbornia 7531ndash37

Brush JM Fisk AT Hussey NE Johnson TB 2012 Spatial andseasonal variability in the diet of round goby (Neogobiusmelanostomus) stable isotopes indicate that stomach con-tents overestimate the importance of dreissenidsCanadian Journal of Fisheries and Aquatic Sciences69573ndash86 doi101139f2012-001

Copp G Kovaacuteč V Zweimuumlller I Dias A Nascimento MBalaacutežovaacute M 2008 Preliminary study of dietary interactionsbetween invading Ponto-Caspian gobies and some nativefish species in the River Danube near Bratislava (Slovakia)Aquatic Invasions 3193ndash200 doi103391ai20083210

Coulter DP Murry BA Webster WC Uzarski DG 2011 Effectsof dreissenid mussels chironomids fishes and zooplank-ton on growth of round goby in experimental aquariaJournal of Freshwater Ecology 26155ndash62 doi101080027050602011553987

Crawley MJ Kornberg H Lawton TH Usher MB Southwood ROrsquoConnor RJ Gibbs A 1986 The population biology ofinvaders Discussion Philosophical Transactions of theRoyal Society B 314711ndash31 doi101098rstb19860082

Cresson P Ruitton S Ourgaud M Harmelin-Vivien M 2014Contrasting perception of fish trophic level from stomachcontent and stable isotope analyses a Mediterranean artifi-cial reef experience Journal of Experimental MarineBiology and Ecology 45254ndash62 doi101016jjembe201311014

Czugała A Woźniczka A 2010 The river Odra estuary ndashanother Baltic Sea area colonized by the round gobyNeogobius melanostomus Pallas 1811 Aquatic Invasions5(1)561ndash65 doi103391ai20105S1014

Debus L Winkler HM 1996 Hinweise zur computergestuumltztenAuswertung von Nahrungsanalysen RostockerMeeresbiologogische Beitraumlge 497ndash110

Ebenhard T 1988 Introduced birds and mammals and theirecological effects Swedish Wildlife Research 13(4)1ndash107

Erm V Turovski A Paaver T 2003 Vimba bream Vimba vimba(L) In Ojaveer E Pihu E Saat T editors Fishes of EstoniaTallin Estonian Academy Publishers p 223ndash25

George EL Hadley WF 1979 Food and habitat partitioningbetween rock bass (Ambloplites rupestris) and smallmouthbass (Micropterus dolomieui) young of the yearTransactions of the American Fisheries Society 108253ndash61doi1015771548-8659(1979)108lt253FAHPBRgt20CO2

Haumlrkoumlnen T 1986 Guide to the Otoliths of the Bony Fishes ofthe Northeast Atlantic Hellerup Denmark Danbiu Aps 256pages

Hempel M Thiel R 2013 First records of the round gobyNeogobius melanostomus (Pallas 1814) in the Elbe River

MARINE BIOLOGY RESEARCH 195

Germany BioInvasions Records 2291ndash95 doi103391bir20132405

Heptner WG Tshapskii KK Arsenev VA Sokolov VE 1976Mlekopitajushtshie Sovietskogo Sojusa Volume 2 Part 3Lastonogie i Zubatye Kity [Mammals of the Soviet UnionPinnipeds and Toothed Whales] Moscow Vysshaja Skola718 pages (in Russian)

Hyslop EJ 1980 Stomach contents analysis ndash a review ofmethods and their application Journal of Fish Biology17411ndash29 doi101111j1095-86491980tb02775x

Jacobs P Hoedemakers K 2013 The round goby Neogobiusmelanostomus (Pallas 1814) (Perciformes Gobiidae) aninvasive species in the Albert Canal (Belgium) BelgianJournal of Zoology 143148ndash53

Janssen J Jude DJ 2001 Recruitment failure of mottledsculpin Cottus bairdi in Calumet Harbor Southern LakeMichigan induced by the newly introduced round gobyNeogobius melanostomus Journal of Great LakesResearch 27319ndash28 doi101016S0380-1330(01)70647-8

Jude DJ Reider RH Smith W 1992 Establishment of Gobiidaein the Great Lakes Basin Canadian Journal of Fisheries andAquatic Sciences 49416ndash21 doi101139f92-047

Jude DJ Janssen J Crawford G 1995 Ecology distributionand impact of the newly introduced round amp tubenosegobies on the biota of the St Clair amp Detroit rivers InMunawar M Edsall T Leach J editors The Lake HuronEcosystem Ecology Fisheries and ManagementAmsterdam SPB Academic Publishing p 447ndash60

Karlson AML Almqvist G Skoacutera KE Appelberg M 2007Indications of competition between non-indigenous roundgoby and native flounder in the Baltic Sea ICES Journal ofMarine Science 64479ndash86 doi101093icesjmsfsl049

Kipp R Ricciardi A 2012 Impacts of the Eurasian round goby(Neogobius melanostomus) on benthic communities in theupper St Lawrence River Canadian Journal of Fisheriesand Aquatic Sciences 69469ndash86 doi101139f2011-139

Kipp R Heacutebert I Lachariteacute M Ricciardi A 2012 Impacts of pre-dation by the Eurasian round goby (Neogobius melanosto-mus) on molluscs in the upper St Lawrence River Journalof Great Lakes Research 3878ndash89 doi101016jjglr201111012

Kornis MS Mercado-Silva N vander Zanden MJ 2012 Twentyyears of invasion a review of round goby Neogobius mela-nostomus biology spread and ecological implicationsJournal of Fish Biology 80235ndash85 doi101111j1095-8649201103157x

Kotta J Nurkse K Puntila R Ojaveer H 2016 Shipping andnatural environmental conditions determine the distributionof the invasive non-indigenous round goby Neogobius mela-nostomus in a regional sea Estuarine Coastal and ShelfScience 16915ndash24 doi101016jecss201511029

Lederer A Massart J Janssen J 2006 Impact of round gobies(Neogobius melanostomus) on dreissenids (Dreissena poly-morpha and Dreissena bugensis) and the associated macro-invertebrate community across an invasion front Journalof Great Lakes Research 321ndash10 doi1033940380-1330(2006)32[1IORGNM]20CO2

Leopold MF van Damme CJ Philippart CJM Winter CJN 2001Otoliths of North Sea Fish ndash Fish Identification Key byMeans of Otoliths and Other Hard Parts WorldBiodiversity Database CD-ROM series Amsterdam ETIBioInformatics CD-ROM

Leppaumlkoski E Olenin S 2000 Non-native species and ratesof spread lessons from the brackish Baltic SeaBiological Invasions 2151ndash63 doi101023A1010052809567

Leppaumlkoski E Olenin S 2001 The meltdown of biogeogra-phical peculiarities of the Baltic Sea the interaction ofnatural and man-made processes AMBIO A Journal ofthe Human Environment 30202ndash09 doi1015790044-7447-304202

Lodge DM 1993 Biological invasions lessons for ecologyTrends in Ecology amp Evolution 8(4)133ndash37 doi1010160169-5347(93)90025-K

Maiskij VN 1955 Pitanie i kormovaja baza sudaka v AzovskomMore [Feeding and food base of pikeperch in the AzovSea] Trudy Vsesojuznyj Naucno-Issledovatelrsquoskij InstitutMorskogo Rybnogo Chozjajstva i Okeanografii (VNIRO)31337ndash55 (in Russian)

Menge M 2012 Untersuchungen zur Oumlkologie derSchwarzmundgrundel (Neogobius melanostomus) inMecklenburg-Vorpommern Diploma Thesis University ofRostock 101 pages

Miller P 1986 Gobiidae In Whitehead PJP Bauchot M-LHureau J-C Nielsen J Tortonese E editors Fishes of theNorth-Eastern Atlantic and the Mediterranean Volume 3Paris Unesco p 1019ndash85

Myts D 2012 Nahrungsoumlkologie des Kormorans(Phalacrocorax carbo sinensis) Diploma Thesis Universityof Rostock 78 pages

Ojaveer H 2006 The round goby Neogobius melanostomus iscolonising the NE Baltic Sea Aquatic Invasions 144ndash45doi103391ai20061111

Ojaveer E Drevs T 2003 Flounder Platichthys flesus trachurus(Duncker) In Ojaveer E Pihu E Saat T editors Fishes ofEstonia Tallin Estonian Academy Publishers p 367ndash68

Piria M Šprem N Jakovlić I Tomljanović T Matulić D Treer Tet al 2011 First record of round goby Neogobius melanos-tomus (Pallas 1814) in the Sava River Croatia AquaticInvasions 6(Suppl 1)153ndash57 doi103391ai20116S1034

Raby GD Gutowsky LFG Fox MG 2010 Diet composition andconsumption rate in round goby (Neogobius melanosto-mus) in its expansion phase in the Trent River OntarioEnvironmental Biology of Fishes 89143ndash50 doi101007s10641-010-9705-y

Rakauskas V Pūtys Ž Dainys J Lesutiene J Ložys L ampArbačiauskas K 2013 Increasing population of the invaderround goby Neogobius melanostomus (ActinopterygiiPerciformes Gobiidae) and its trophic role in the CuronianLagoon SE Baltic Sea Acta Ichthyologica et Piscatoria4395ndash108 doi103750AIP201343202

Sapota M Skoacutera K 2005 Spread of alien (non-indigenous) fishspecies Neogobius melanostomus in the Gulf of Gdańsk(south Baltic) Biological Invasions 7157ndash64 doi101007s10530-004-9035-0

Sapota MR Balazy P Mirny Z 2014 Modification in the nestguarding strategy ndash one of the reasons of the roundgoby (Neogobius melanostomus) invasion success in theGulf of Gdansk International Journal of Oceanographyand Hydrobiology 4321ndash28

Schaffelke B Evers D Walhorn A 1995 Selective grazing ofthe isopod Idothea baltica between Fucus evanescens andF vesiculosus from Kiel Fjord (Western Baltic) MarineBiology 124215ndash18 doi101007BF00347125

196 D OESTERWIND ET AL

Schanz A Polte P Asmus H Asmus R 2000 Currents and tur-bulence as a top-down regulator in intertidal seagrasscommunities Biologia Marina Mediterranea 7278ndash81

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Winkler H Kotterba P Oesterwind D 2015 Round goby astory of invasion success in the Baltic Poster in ICESAnnual Science Conference 2015 21ndash25 SeptemberCopenhagen Denmark

MARINE BIOLOGY RESEARCH 197