Not to be· cited without prior reference to the author

ICESAnnual Science Conference(83rd Statutory Meeting)

CM 1995/01 I;Theme Session 0:Ballast Water: Ecologicaland Fisheries Implications

Non-Indigenous Organisms Introduced via Ships intoGerman Waters

S. GoI/asch 1, M. Dammer 2, J. Lenz 2 & H.G. Andres 3

• 1 Universität Hamburgj Zoologisches Institut und MuseumMartin-Luther-King-Platz 3, 20146 Hamburg, Germany

2 Institut für Meereskunde, Düsternbrooker Weg 20,24105 Kiel, Germany

3 Taxonomische Arbeitsgruppe an der Biologischen AnstaltHelgoland, c/o Universität Hamburg, Zoologisches Institutund Museum, Martin-Luther-King-Platz 3, 20146 Hamburg,Germany

Abstract

• Ballast water has been recognized as a major vector for the iritroductionof non-indigenous organisms. Commissioned by the Federal EnvironmentalAgency, Berlin, a joint research project between the Institut fürMeereskunde Kiel and the University of Hamburg was initiated to provideinformation on possible harmful effects of non-indigenous organismsintroduced into German waters by ship traffic. The study aims at athorough taxonomic assessment of planktic and benthic organisms foundin ballast water, tank sediment and on ship hulls. Over aperiod of threeyears about 300 vessels calling at German ports were yisited. So farabout 350 botanical and zoological taxa were found, of which roughly 30percent comprised f~reign organisms, non-indigenous to the Baltic andNorth Sea. In addition, the survival of plankton organisms in ballastwater tanks was studied by accompanying a container vessel on itsvoyage from Singapore to Bremerhaven. Initial results are reported here.

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Introduction

CarIton (1985) has given a comprehensive review of ballast water as amechanism for dispersing aquatic organisms and has provided evidencethat thereby a world-wide transfer of organisms between the continentstakes place. Recently observed mass developments of non-indigenousspecies in various parts of the world, causing severe ecological and eveneconomical damage, have brought the problem of ballast water transportinto general focus (Carlton & Geiler 1993, Hedgpeth 1993). Examples arethe Zebra Mussei (Dreissena polymorpha) (Roberts 1990), the cladoceranBythotrephes cederstroemi (Sprules et aJ. 1990) and the European RiverRuffe (Gymnocephalus cernuus) (Waldichuk 1990), which have invaded theGreat Lakes in North America. While the two laUer species affect theoriginal food web structure by outcompeting indigenous species,Dreissena causes high economical damage by clogging pipes in waterpumping and discharge systems. The ctenophore Mnemiopsis leidyi, aspecies from the southern east coast of North America, has become adominant member of carnivorous zooplankton in the Slack Sea ecosystem,affecting the recruitment of commercial fish stocks by predation on fishlarvae and their prey organisms (Harbison & Volovik 1993). Another NorthAmerican species, the spionid polychaete Marenzellaria viridis, hasestabJished itself in the Saltic Sea (Norkko et aJ. 1993) and almostentirely replaced the indigenous polychaete Nereis diversicolor in someareas (Zmudzinski 1993). Marine aquaculture is threatened by the world­wide transport of toxic phytoplankton species in ballast water tanks,especially of cyst-forming dinoflagellates which are able to survive longperiods of unfavourable conditions (Hallegraeff et aJ. 1988, 1990).

After the occurrence of new toxic algal blooms in AustraJian waters,evidently established there by ballast water transport from Japan,AustraJian scientists have taken the lead in intensifying ballast waterresearch (Hallegraeff & Solch 1991, 1992) and urging the IMO(International Maritime Organisation) to take up the ballast waterproblem as an official issue in regulating international ship traffic. As afirst reaction the 'International guidelines for preventing theintroduction of unwanted aquatic organisms and pathogens trom ships'ballast water and sediment discharges' were adopted by IMO (1991), themain recommendation being to exchange ballast water. as tar as weatherand safety conditions permit. when crossing deep open ocean waters. Thismeasure would greatly reduce the danger of transferring freshwater or

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near-shore marine organisms to other areas, as clear nutrient-exhaustedopen ocean water is usually characterized by a sparse planktoncomrriuhity, the members of which are unable to survive under the farmore changeable environmental conditions in coastal areas.

In 1992, a joint research project between the Institut für MeereskundeKiel and {he University of Hamburg commissioned by ihe FederalEnvironrriental Agency in Berlin was launched to investigate flora andfauna earried by international ship traffie. to German ports and to assessthe ecological risk arising. from the introduction of non-indigenousspecies to German waters. The flora is identified in Kiel and the fauna inHamburg. The practical work and rriain burden of the project is sharedbetween two junior scientists, S.G. and M.D.; while two senior scientists,J.L. and G;A., are the advisors bearing the main responsibility.

Material and Methods .

A large variety of ocean-going vessels calling at German ports wereinvestigated for their ballast water content. in addition, newly doekedvessels were inspecied for the presemce .of sediment and largerorganisms in emptied ballast water tanks as weil as for foulingorganisms on the hull. The majority of sampies were eollected at theoverseas harbours of Hamburg (76 %) and Bremerhaven (18 %). Other portswhich were only occasionally visited ineh..ide Rostoek and Kiel (WesternBaitic), Rendsburg (Kiel Canal), Brake, Elsfletl1, Bremen (River Weser) andWilhelmshaven (North Sea). The vessels invesÜgated were mai':l'Y cargoships, the most frequent type being container vessels followed by, eombiships, bulk carriers and car transporters. A few passenger liners,research vessels and even navy ships were visited as weil.

Three methods w~re employed for sampling ballast water. The first wasopening a manhole permittirig direct access to the tank and taking asampie with a small plankton net (rriesh size 10' Jlm). Such an lide,al'sampie taking was, however, very rarely possib!e,. a mere 6 tim~s out of atotal of 136 inspeetions. The reasons usually given by the ship's crewwere inaccessibility of suitable manholes because of overlying eargo, asti"id interpretation of safety. regulations and lack of manpower neededfor opening and ciosing a tank during the short and busy schedule in theport.

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The second method, which was employed 69 times, was to pump ballastwater through asounding pipe in the tank with the help of a hand-pump.These sounding tubes have a diameter of about 6 cm and a length of up to20 m. The maximum depth of water level that could be reached by thehand-pump was 9 m. Very modern vessels do not have sounding tubes anymore, since nowadays water content in the tanks is solely controlled byelectronical meters.

The third method, employed 43 times, was drawing water from a smalltap on the ballast water pump. Water obtained by the second and thirdmethods were filtered through a 10 Jlm plankton net, usually 100 I persampie, and preserved for phytoplankton and 'zooplankton analysis in 4 %formalin and 70 % ethanol, respectively. Depending on time and distance •from the laboratory, small subsampies were left unpreserved forinspection of living organisms. On 18 occasions, when emptied tankswere inspected, it was possible to take plankton sampies out of theresidual bottom water.

The abiotic factors regularly measured in ballast water weretemperature, salinity and oxygen by means of portable electrochemicalprobes and pH with a portable pH-meter.

As already mentioned, sediment and hull sampies were obtained fromnewly docked vessels. Entering emptied tanks sometimes needs specialprecautionary measures, as non-ventilated tanks may contain toxic gasessuch as methane or hydrogen sulphide. At the beginning of the project itwas therefore decided to purchase a breathing apparatus and to undergo aspecial training course with the local fire-brigade. Agas mask alsoprovides protection against pathogenic germs, e.g. cholera bacteria,which might be present in ballast water. It turned out later that in mostcases the inspected tanks were well-ventilated.

Sediment sampies were take"n from the tank bottom and fromconstruction frames on the walls. Fouling organisms were scraped fromthe walls, too. Sometimes it was possible to catch larger organisms suchas crabs and fish in the residual water by means of a small landing net.Preservation methods were the same as with plankton sampies.Unpreserved sediment sampies were stored in a refrigerator for futurecyst-hatching experiments. For making a semiquantitative comparisori offouling sampies possible, a patch measuring roughly 10 x 10 cm wasusually scraped off the hull.

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In May 1995 the German container ship 'DSR America' was accompaniedduririg a 23 day cruise from Singapore to Bremerhaven in order toinvestigate the survival of tropical plankton in ballast water tanks ontheir way to northern Europe through a daily check of environmentalconditions (temperature, salinity, oxygen and pH value) and planktoncantent. Environmental conditions were recorded in 4 tanks, in theforepea~ and aftpeak tank and in iwo opposite side tanks on starboard andport side. The first tank was filled after departure from Singapore andthe three others after a stop in Colombo (Sri Lanka). Plankton survivaiwas controlIed in two tanks, in the aftpeak tank and ane of the lateriii'ed side tanks., 100 I sampies were ta~en daily througl1 openedmanholes and filtered through a 10 Jlm plankton net. Speciesdetermination and counting were, as far as possibie, completad on board.

Results

Fig. 1 shows the positon of ballast water tanks in a modern containervessel. They consist of aseries, of double bottom tanks, topside tariks anda forepeak and aftpeak tank. The ballast water capacity of large vesselsmay' .exceed 20,000 1. Bulk carriers, when travelling without cargo, cantransport more than 100,000 1.

Vessels from almost all parts of the world connected throughinternational ship traffic were investigated (Fig. 2). 308 vessels wereinspected between March 1992 and JUly 1995, yielding a total of 335plankton, sediment arid huli sampies (Fig. 3). Their geographicai origin isshown in Fig. 4.

Altogether, over 350 different taxa were found; more than 100 comprisedunicellular algae and about 250 zoological species or taxa. Even with thehelp of experts, an exact systematical identificatio~ was rather difflcultin a number of cases. Therefore the genus could only be Iisted. The numberof organisms found in 100 I ballast water v~uied betweeri one and severalhundred specimens. A total of 15,000 specimens have been analysed sofar, about two-thirds comprising plankton organisms and 1,000 and 4,000specimens from sediment and hull sampies, respectively.

. .The mairi phytoplankton groups recorded are diatoms, dinoflagellates,chloro- and cyanophytes. Diatoms arid chlorophytes were more common

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than dinoflagellates. Fig. 5a shows the regional distribution of thesampies and presence of the main groups. It is interesting to note that inquite a number of cases no phytoplankton was found at all, especially insampies from the Indian Ocean, South-West America and the open ocean.

Sediment sampies analysed so far showed the presence of empty cysts ofdinoflagellates belonging mainly to the genus Protoperidinium. It isunknown where the hatchirig took place, in the tank or before ballasting.

The main group of organisms recorded in ballast water from all regionsare planktic crustaceans (Fig. 5b). Mollusc, polychaete and fish larvaeoccurred quite frequently. What is interesting is the occurrence ofrotifers and nematods. Rotifers inhabit mainly freshwater and low-saline •brackish water. Their presence can be taken as an indication of the originof the ballast water. Nematods are benthic organisms. Their presencepoints to the fact that ballasting occurred in a nearshore shallow areawhere the sediment was stirred up. The presence of chlorophytes (Fig. 5a)may be interpreted in the same way. A classification of the salinity ofthe ballast water shows that in 3 % salinity was below 5 % 0 , 32 % fellinto the range 5-30 %0 and 65 % contairied high-saline water above 30% 0 •

The dominance of crustaceans recorded is also mirrored in their speciesdiversity. Of 250 taxa recorded in total for the organisms, 152 species(62 %) were crustaceans with 57 copepod species encountered primarilyin plankton sampies. Molluscs rank second with 57 species (23 %).Cirripeds and bivalves were the predominant hull organisms. • .Foraminiferids occurred mainly in sediment sampies.

A first estimate shows that about 30 % of the 350 species recorded areto be regarded as non-indigenous. Tab.1 gives an overview of thesystematical groups where foreign species were encountered. It isinteresting to note that the plankton sampies contained only 4 groupswith non-indigenous species, while the number of groups found insediment and hull sampies was almost twice as high.

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Tab. 1 Systematical groups in which non-indigenous taxa were recordedand location of records

Systematical unit Plankton Sediment Hull

---------------------------------------------------------Diatomophycea + +Dinophycea + +Foraminifera + + +Turbellaria +

• Rotifera +Gastropoda + +8ivalvia + +Cladocera + +Ostracoda + +Copepoda +Cirripedia + +Decapoda + +8ryozoa +

The study on the survival rate of plankton in ballast water tanks on boardthe container vessel 'DSR America' on its way from Singapore viaColombo to 8remerhaven focussed on two tanks. Fig. 6a shows the

• concentration of phytoplankton cells in the aftpeak tank filled close toSingapore. After some oscillations during the first few days, there was astrang decrease resulting in an about 90 % reduction in cell number on thetenth day after departure. The bulk were diatoms of which 30 specieswere identified at the beginning, whereas dinoflagellates, represented by13 species, started with a much lower concentration and disappeared onday 13. On arrival in 8remerhaven after a 23 day cruise, only 4 species ofdiatoms had survived.

Zooplankton exhibited a similarly sharp decrease in the aftpeak tank asphytoplankton. Of 24 taxa recorded on the second day after filling, only 4survived the cruise. These were a few specimens of the benthicharpacticoid copepod Tisbe graciloides, a turbellarian, a gastropod and

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a bivalve larva. Juvenile copepods constituted the predominantzooplankton component at the beginning. Their abundance decreasedrapidly during the first 5 days (Fig. 6b).

A similar decrease in diversity from 16 to 4 species was observed in thesecond tank filled after departure from Colombo on the way to8remerhaven. Surprising in this case, however, was the observation thatTisbe graciloides had considerably increased in concentration after the14 day cruise.

Fig. 7 shows the temperature records for the 4 tanks with the sea surfacetemperature for comparison. Tank temperatures followed seatemperature with a delay of one to two days. It is interesting to note thatapparently it was not the temperature drop that was responsible for thesharp fall in species number and concentration of phyto- and zooplanktonobserved in the aftpeak tank, as this occurred before temperaturechanged. Oxygen and pH showed comparatively Iittle variation over thewhole cruise. An oversaturation of up to 126 % was recorded trom thetourth to the seventh day, when the vessel was pitching and rolling due toan increased wind force of 6-7 81. Since the tank was not completelyfilled, the overlying air was mixed into the water, leading to theobserved oversaturation with oxygen. Although the rolling of the water inthe tank could have had an adverse effect on delicate plankton organisms,the main concentration drop (Fig. 6a, b) had already occurred before, sothat this effect can also be ruled out. A third possible explanation couldlie in the organisms having been damaged through the pumping system,causing a subsequent high mortality.

The transition trom warm to cold temperature will generally harmballast water organisms to a lesser extent than the other way round,since a temperature decrease is physiologically easier to tolerate than anincrease. To show how strong the temperature increase is that ballastwater organisms may be exposed to the seasonal change of sea surfacetemperature during a cruise trom the west coast of North America tonorthern Europe and vice versa is shown in Fig. 8. The year-round hightropical temperatures met in passing the 'Panama Canal will probably inmost cases act as a barrier tor the transport of boreal and temperateorganisms trom one area to the other.

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Discussion

The investigation of ballast water tanks and hulls of ocean-going vesselstor the presEmce of, Iiving organisms ciS proot ot a possible tran~ter

mechanism by which non-indigfülOus species are able to establishthemselves in foreign ecosystems is the first step in assessing theecological and also economical risks involved. Therefore after the pioneerwork by CarIton (1985) on organisms and that by Australian researeherson phytoplankton (Hallegraeff et ai. 1988, 1990, Hallegraeff & Solch1991, 1992), turther studies in other eountries were initiated, e.g. inCanada (Subba Rao et al. 1994).

lrivestigation of ballast water proved, however, much more difficult, thaninitially thought. The main problem is opening the manhole of a tank foradequate sampling. Ouring our study, we only sueeeeded a tew times inpersuading a ship's crew to open a manhole. Since we had no olficiaibacking trom iocal governmental or harbour authorities, we first had topolitely approach shipping agencies and shipyards before being allowed totake sampies at all. The two other sampling methods employed, hand­pumping through sounding pipes arid tapping of the pump system,constitute a compromise which did not work satisfactorily in 811 eases.

More iriformation on environmental eonditions in ballast water tanks andon survival of organisms wiU help to evaluate the risks of transport(Rigby & Hallegraeff 1994). Following the fate of the organisms tromballasting to deballasting through repeated checking of the eonditions onboard wili yield interesting results. Our study showed a rapid decline ofplankton eoncentration ,during the first days after filling the tanks. Thereason, however, is not yet clear.

The second step in evaluating the ecological and ecoriomical risk hwolvedin transportirig non-indigeü10us species by ship, traffic is to study theirgeographical distribution and range of tolerable environmentalconditions, their trophic relationships and behaviour by rrieans of athorough literature review. If experimental conditions permit, it may insome cases be possible to successfully eulture such organisms in thelaboratory for conducÜng detailed studies ori their ecologleal toleranceduring their Iife cycle.

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Acknowledgements

We thank the Federal Environmental Agency, Berlin for funding thisproject and Dr. A. Künitzer for her advice as weil as all shippingcompanies, agencies, dockyards, port offices and ship crews who kindlysupported this project. Technical help and information were given by Dr.M. Rolke (Bundesamt für Seeschiffahrt und Hydrographie), H.J. Golchert(Verband Deutscher Reeder) and Germanischer L1oyd. This paper is partlybased on a doctoral thesis by S. Gollasch, Fachbereich Biologie,Universität Hamburg, Germany.

References

Carlton, J.T. 1985: Transoeeanie and interoeeanie dispersal ofeoastal marine organisms: The biology of ballast water.Oeeanogr. Mar. Biol. Ann. Rev. 23: 313-371.

Carlton, J.T., GeIler, J.B. 1993: Eeologieal roulette: The globaltransport of non-indigenous marine organisms.Seienee 261:78-82.

Hallegraeff, G.M., Boleh, C.J., Koerbin; B., Bryan, J. 1988:Ballast water a danger to aquaeulture. Aust. Fish. 47: 32-34.

Hallegraeff, G,M., Boleh, C.J., Bryan, J., Koerbin, B. 1990:Mieroalgae spores in ships' ballast water: A danger toaquaeul ture. In: Graneli, E. et al. (eds . ): Toxie MarinePhytoplankton. New York: Elsevier. p. 475-480.

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Hallegraeff, G.M., Boleh, C.J. 1991: Transport of toxiedinoflagellate eysts via ships' ballast water. Mar. PoIl. Bull. •22: 27-30.

Hallegraeff, G.M., Boleh, C.J. 1992: Transport of diatoms anddinoflagellate resting spores in ships' ballast water:Implieations for plankton biogeography and aquaeulture. J.Plankton Res. 14: 1067-1087.

Harbison, G.R., Volovik, S.P. 1994: The ctenophore Mnemiopsisleidyi in the Black Sea: a holoplanktonic organism transportedin the ballast water of ships. In: Cottingham, D. (ed.): Non­indigenous and introdueed marine species. NOAA Tech. Rep.

Hedgpeth, J.W. 1993: Foreign invaders. Science 261: 34-35.

IMO (International Maritime Organization) 1991: Internationalguidelines for preventing the introduetion of unwanted aquatieorganisms and pathogens from ships' ballast water and sedimentdiseharges. MEPC 31/21, Annex 16.

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Norkko, A., Bonsdorff, E., Boström, C. 1993: Observations of thepolychaete Marenzellaria viridis (VERRIL) on a shallow sandybottom of the south coast of Finland. Memor. Soc. Fauna FloraFennica 69: 12-113.

Rigby, G., Hallegraeff, G.M. 1994: The transfer and control ofharmful organisms in shipping ballast water: Behaviour of marineplankton and ballast water exchange trials on the MV 'IronWhyalla'. J. Mar. Env. Engg. 1: 91-110.

Roberts, L. 1990: Zebra mussei invasion threatens U.S. waters.Science 249: 1370-1372.

Sprules, W.G., Riessen, H.P., Jin, E.H. 1990: Dynamics of theBythotrephes invasion of the St. Lawrence Great Lakes. J. GreatLakes Res. 16: 346-351 .

Subba Rao, D.V., Sprules, W.G., Locke, A., Carlton, J.T. 1994:Exotic phytoplankton from ships' ballast waters: Risk ofpotential spread to mariculture sites on Canada's east coast.Can. Data Rep. Fish. Aquat. Sci. 397: 1-51.

Waldichuk, M. 1990: Invading fish a threat to Great Lakesfisheries. Mar. PoIl. Bull. 21: 266-267 ... .

Zmudzinski, L. 1993: Long-term changes in macrozoobenthos of theVistula lagoon. (Poster abstract), Second Estuary Symposium:Estuarine Environments and Biology of Estuarian Species. Gdansk,Poland .

Fig. 1: Chematic-cross-section through a modern container vesseI showing

the positiop ofthe ballast water tanks (shaded).

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• • • • • • - • - •••••••~"',.,s...... _------._ _..Fig. 2: Geographic~ 'origin ofvesseIs investigated.

400

300

Num

~ 200rs

100

o

335

Vessels Total Sampies Plankton Hull Sediment

. Fig. 3: Nwnber ofvessels investigated, total number of sampIes and

specification ofsampIes (March 1992 - July ·1995).• e

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Mediterranean Sea

North Africa

South Africa

Indonesia

Australia

North AmerieaEast Coast

North America'Vest Coast

South AmericaEast Coast

South America'Vest Coast

Open Oeean

o 5 10 15 20 25 30 35 40 45

• Plankton o Sediment [iJ HuB

, ,

Fig. 4 : Number of plankton, sediment and buH sampiesaccordirig {o their geographical origin

Mediterranean Sea

Middle East

North Africa

South Afriea

India

FarEast

Indonesia

Australia

North AmerieaEast Coast

North America\Vest Coast

Central America

South AmericaEast Coast

South America'Vest Coast

Open Oeean

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•

20% 40% 60% 80% 100%

• Diatoms11 Cyanophyta

oDinoflagellateso Negative

(3 Chlorophyta

Fig. 5a : Unicellular algae present (O~) in ballast watersampIes according to their geographical origin

Mediterranean Sea

l\fiddle East

North Africa

I.~ I 1111111111111

I~III', ": "~' " ,I '.' 1111

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•

South Africa

India

FarEast

Indonesia

Australia

Nortb AmericaEast Cmist

North America'Vest Coast

Ceritral America I~~~~Soutb AmericaEast Coast

Soutb AmericaWest Coast

Open Ocean

1 I :

00/0 20% 40% 60% 80% 100%

D ForaminiH::ra8 Fish

D Rotatoria

.Crustacea

ElIMoIluscafZ.) Nematoda

DJ AßnellidaDNegative

Fig. Sb : Organisms present (%) in ballast water sampIesaccording to their geographical origin

trio00-

trior'-

trio\Ci-

Cellsll

.900

800

700

600

500

_B_r_em__er_h_av_e_n --J~~Iantic_.l __ ... Me~:~rran~~... / .

Indian Ocean ___~re

Fig. 6a : Concentration of phytoplankton cells in the aftpeak ballast water of 'DSR-America'

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n11001

700

600

500

400

Indian Ocean I Singapore...............- _......._...._-....._., ...-.._....... ....... . ...

IRed Sca

'no'l5-

If'lor-:-

'no00_.

Mediterranean

If'lo

'"-If'lociN

Atlantic

'noNN

If'l If'lo 0vi -iN ·N

If'lo'l5N

Bremerhaven

Total

juv. copepods

adu1tcopepods:l~~~~~~'~~~~!~~~~~~~~~~~!~~~~~~~~~~ill~~~~

Fig. 6b : Conccntration of zooplanldon organisms inthc aftpc411{ IUllinst watcr of 'DSR-Amcrica'

Sidetank. 4 P.

~Forepeak:

Ocean

triq....M

triociN

trio0\....

trior..:....

trio\li....

trio00....

oe31,0

29,0

27,0

25,0

23,0

21,0

19,0

Bremcrhaven Atlantie Mediterr:mcan IRed Sca Indian Occan LSingaporc-- ._---_._._--_. .._.._. ... ..

Fig. 7 : Temperature variation in different ballast tanks and the open ocean during the cruise fromSingapore to Bremerhaven on bO.dthe 'DSR America' e

-+-Spring-Summer-.-Autumn~Winter

14000Distance [NM]

12000100008000600040002000

0,00 +------+------+-----+------+--------+-----+------1o

5,00

20,00

25,00

15,00

30,00

10,00

Fig. 8 : North-west American shipping route (Vancouver - Bremerhaven)Seasonal mean ocean surface temperature(data from Climatological Atlas ofthe World Ocean, NOAA 1983)