MARINE ECOLOGY PROGRESS SERIESMar Ecol Prog Ser

Vol. 350: 41–54, 2007doi: 10.3354/meps07016

Published November 22

INTRODUCTION

Ballast water, which is carried onboard ships to pro-vide stability and for trimming purposes, is recognisedas a key mechanism for the translocation of non-indigenous marine species to new locations (Carlton1985, Chu et al. 1997, Gollasch et al. 2000, Niimi 2000,Murphy & Ruiz 2001, Wonham et al. 2001). Examplesof this include the zebra mussel Dreissena polymorphain North America and the toxin-producing dinofla-gellate Gymnodinium catenatum in the Derwent andHuon estuaries in Tasmania, which is now responsible

for the regular closure of shellfish harvesting due tohigh levels of Paralytic Shellfish Poisoning (PSP) toxins(Hallegraeff & Bolch 1992).

The only current internationally accepted method ofreducing the risk of new introductions via ballast waterdischarge is open ocean ballast water exchange (BWE).The aim of BWE is to replace all or most of the originalballast water from a port of origin with water from theopen ocean. The open ocean is simply described by theInternational Maritime Organisation (IMO) in its Reso-lution A. 868(20) of 27 November 1997 (IMO 1997) asdeep water as far as possible from shore. Ocean depths

© Inter-Research 2007 · www.int-res.com*Email: mike.taylor@cawthron.org.nz

Trans-Pacific shipboard trials on planktoniccommunities as indicators of open ocean ballast

water exchange

Michael D. Taylor1,*, Lincoln M. MacKenzie1, Timothy J. Dodgshun1, Grant A. Hopkins1, Eykolina J. de Zwart1, Carlton D. Hunt2

1Cawthron Institute, 98 Halifax Street East, Private Bag 2, Nelson 7042, New Zealand2 Battelle, 397 Washington Street, Duxbury, Massachusetts 02332, USA

ABSTRACT: A trans-Pacific voyage from Japan to New Zealand via Singapore was used to assessplanktonic (and sediment-dwelling) communities as indicators of open ocean ballast water exchange(BWE). The research was part of a larger project to develop methods for verifying whether interna-tional shipping has complied with mandatory controls and voluntary BWE guidelines. The dilutionefficiency of exchanges was compared with changes in the composition and abundance of ballasttank phyto- and zooplankton taxa. Changes in the planktonic communities were measured by sam-pling the source port, the ballast water at the source and recipient ports and immediately before andafter BWE, and the open ocean water during exchanges. Although exchanges appeared relativelyeffective at reducing the abundance (90 to 100%) of phyto- and zooplankton indicator taxa (i.e. taxain the ballast water uploaded from the source port that were not present in open ocean samples orwere present at <0.001 the original concentration), such reductions must be considered in the light ofvariation in survivorship in the control tank. Relatively high rates of mortality were associated with arapid warming (i.e. 14.0 to 27.8°C) of the exchanged and control ballast tanks as the vessel enteredthe tropics. The rapid decline in the abundance of indicator taxa after BWE contrasted with a lesseffective reduction (i.e. 30.3 and 25.0% for the first and second exchanges, respectively) in the totalnumber of phyto- and zooplankton taxa. Management controls and guidelines should place greateremphasis on whether the water uploaded during BWE is sufficiently oceanic to minimise the risk ofuploading harmful coastal organisms.

KEY WORDS: Ballast water exchange · Tracer dye · Phytoplankton · Zooplankton · Sediment-dwelling species · Biological indicators · Open ocean · Trans-Pacific voyage

Resale or republication not permitted without written consent of the publisher

Mar Ecol Prog Ser 350: 41–54, 2007

of up to 2000 m have been recommended by variousauthors and agencies (Williams et al. 1988, Dickman& Zhang 1999); however, many shipping routes, e.g.short voyages or those passing through island archi-pelagos, can render BWE at such depths impractical.

In February 2004, IMO member countries adoptedthe International Convention for the Control and Man-agement of Ships’ Ballast Water and Sediments. Theconvention called for BWE to be considered an interimmeasure, to be followed by the adoption of a BWEstandard (Regulation D-1), which specifies an effi-ciency rating of 95% volumetric exchange of ballastwater and a performance standard (Regulation D-2),limiting the number of organisms that ships could dis-charge in their ballast. The latter standard requiresships carrying out ballast water management to dis-charge less than 10 viable organisms ≥ 50 µm in sizem–3 of water and less than 10 viable organisms <50 µmbut >10 µm in size ml–1 of water. In addition, the ballastwater performance standard sets limits on the dis-charge of a number of disease causing pathogens,including Vibrio cholerae and Escherichia coli. Thelegal status of Resolution A. 868(20) is not affected bythe adoption of the Convention.

There are 2 main methods of carrying out BWE:empty-refill and flow-through dilution. The empty-re-fill method involves completely emptying then refillingthe ballast tank (e.g. segregated tanks on containervessels) or hold (e.g. bulk carriers). The flow-throughmethod involves pumping open ocean water into thetank or hold and then allowing the water to overflow.The IMO recommends that the tank volume should bepumped through the tank at least 3 times when usingthe flow-through method. Theoretically, in a perfectmixing environment, approximately 95% of the origi-nal coastal water in a ballast tank should be replacedby open ocean water if volumes of ocean water equalto 3 times the tank volume are pumped through (Rigby& Hallegraeff 1994). Ship design, cargo loading andsafety considerations can limit the extent to which aBWE is carried out, however, particularly during roughsea conditions (Rigby & Hallegraeff 1994, Hay & Tanis1998).

Exchange operations that realistically aim to ex-change at least 95% of the original ballast water alsoaim to remove or kill at least 95% of the organisms inthat water. The dilution of the original water is not thesame as the removal of the organisms, however, asthere is evidence for organisms having been retainedin ballast tanks during exchanges (Rigby & Hallegraeff1994, Wonham et al. 2001). Harvey et al. (1999) re-ported that although BWE has been shown to greatlyreduce the diversity and abundance of planktonicorganisms in the ballast water of ships entering theGreat Lakes, coastal species remained in incoming

vessels that had reported complete exchanges. Thesestudies suggest that during BWE the rate of biologicaldilution may be less than that of the original water. Thebiota may be retained in the tanks either by entrain-ment or sedimentation, or by avoiding the outlets in thecase of some of the larger species.

Most methods used for verifying compliance withballast water controls and voluntary BWE guidelinesare dependent on ships’ documentation and log keep-ing (Hallegraeff 1998). Alternative ways of verifyingcompliance might include cross checking the volume ofwater claimed to have been pumped during the ex-change (e.g. the ‘Newcastle Method’), direct measure-ment of the volume of the original ballast water re-placed (e.g. magnetic flow meters), and automatedelectronic systems (e.g. the ‘black box’) for interrogat-ing variables such as ballast volumes pumped, geo-graphic position and the time of BWE (Hay & Tanis1998). Tracer dye studies have been proposed as a use-ful tool for measuring dilution after an exchange, butwould probably be of relatively little value for routinelytesting compliance (ibid). The optical characteristics ofseawater can be used to distinguish between oceanicand coastal water types, and fluorescence spectra haveconsiderable potential as a tool for verifying compli-ance (Hall et al. 2005, Hunt et al. 2006, Murphy et al.2006). Identifying the different proportions of coastaland oceanic, and tropical and temperate, planktoncommunities present in the ballast water might alsohave potential as a compliance verification tool (Halle-graeff 1998). In the Port of Vancouver, for example, therelative proportions of coastal and oceanic copepodspecies have been used to corroborate claims thatBWEs were made (see Hay & Tanis 1998).

The present study investigated the efficiency of BWEin terms of both the physical dilution of the originalwater and changes in the composition and abundanceof phyto- and zooplankton communities uploaded fromthe source port. The study was part of a wider researchproject aimed at identifying methods for verifyingwhether international shipping has complied with bal-last water controls and voluntary BWE guidelines, andestablishing the effectiveness of ballast exchange atexpelling the resident organisms inside ballast tanks.The research was undertaken for the New ZealandMinistry of Fisheries by the Cawthron Institute (NewZealand) in collaboration with Battelle (USA) between1998 and 1999.

MATERIALS AND METHODS

Sampling design. BWE trials were carried out duringa trans-Pacific voyage of the M/T ‘Iver Stream’ fromKawasaki Harbour, Japan, to Singapore Harbour

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Taylor et al.: Open ocean ballast water exchange

between 23 February 1999 and 8 March 1999 (firstleg), and from Singapore Harbour to New Plymouth(New Zealand) between 8 and 24 March 1999 (secondleg). The ship’s track-line, the locations of BWEs andcoastal and open ocean sampling points during thevoyage are shown in Hunt et al. (2007; their Fig. 1).

The ‘Iver Stream’ is a methanol carrier, which ar-rived in New Zealand fully ballasted. The vessel has adead-weight tonnage (DWT) of 32 000 metric tonnes(t), and has 2 pairs of port and starboard ballast tanks(1435 m3 capacity each: depth 15.0 m, width 6.5 m,length 14.8 m). Although the ballast tanks are not com-partmentalised, they contain internal platforms andframing structures. All exchanges were carried outusing the flow-through dilution method (pump rate170 m3 h–1), and the vessel travelled 900 to 1200 kmduring the 24 to 40 h (depending on the number ofpumps that were available) it took to exchange 3 timesthe volume of 1 ballast tank.

At the beginning of the first leg, all 4 ballast tankswere completely emptied and then cleaned of theremaining sediments to control for variation in sedi-ment levels between tanks. The ship’s ballast waterintakes were located approximately 7.0 m below thewaterline, and during ballasting the seawater depth inKawasaki Harbour was approximately 10 m. The firstexchange on the first leg was carried out from 26 to28 February 1999 in the East China Sea in a gentleswell, over an approximate depth of 6500 m using aport ballast tank, while the second exchange was car-ried out from 1 to 2 March in the South China Sea invery similar sea conditions over an approximate depthof 3700 m using a starboard ballast tank. A second portballast tank was used as a non-exchanged control forboth exchanges; hence, Kawasaki Harbour water re-mained in this tank for the entire first leg and so tra-versed a wide latitudinal range from temperate regionsto the tropics. For both exchanges on the first leg,2 complete exchanges (i.e. 3 times the tank capacity)were carried out by pumping water through 4 to 6large deck hoses into the man-hole at the top of thetank, and out via another pump at the bottom of thetank, near the aft end.

At the beginning of the second leg, a port and star-board tank were partly filled with Singapore Harbourwater, and filling was completed as the ‘Iver Stream’travelled out of the Harbour. The weather during thispart of the voyage was very settled, resulting in verycalm sea conditions. The first exchange, using the porttank, was carried out from 13 to 14 March 1999 in thewest Pacific off the east coast of Irian Jaya over anapproximate depth 1400 m. The second exchange,using the starboard tank, was carried out from 15 to17 March off the north coast of Papua New Guineaover an approximate depth of 900 to 2000 m. The first

exchange was complete (as described above); how-ever, the second exchange was equal to only 2 timesthe tank volume owing to vessel time constraints. Forboth exchanges on the second leg, the water waspumped in at the bottom, near the aft end of the tanks,and allowed to overflow out of the hatches describedabove. No controls tanks were available on the secondleg owing to vessel loading constraints; hence, analy-ses were limited to selected samples only. During thesecond exchange on the second leg of the voyage the‘Iver Stream’ sailed in close proximity (10 to 15 km) tothe mouth of the Sepik River.

Samples were collected from the ballast tanks sev-eral hours before and after exchanges, several hoursafter uplifting ballast, and at the end of each leg. Allsamples were collected via Butterworth hatches loca-ted on the seaward side of the top of the tanks.

Dilution efficiency. Laboratory experiments andpreliminary shipboard trials on a New Zealand domes-tic container vessel, the M/V ‘Spirit of Vision’, wereused to identify a suitable tracer dye for measuring thedilution efficiency of BWE. Rhodamine WT was chosenbecause, unlike histological stains, it is biologically in-active. It is a highly fluorescent material with theunique ability to absorb green light (optimum excita-tion wavelength 556 nm) and emit red light. Very fewcompounds have this property, so interference byother substances is uncommon. The dye is a highlyspecific tracer, and the amount of red light is direction-ally proportional to dye concentration down to at least10–4 ppm for industrial type applications (Turner De-signs 1999). We used Intracid® Rhodamine WT fluores-cent water tracing dye. The active content of the com-mercial dye is 21.3% (or 2.13 × 105 ppm) and it has aspecific gravity of 1.11 to 1.13 at 20°C. Dye fluores-cence was measured using a Turner Designs™ 10-05fluorometer, and Rhodamine WT concentration wascalculated using a linear calibration of fluorescenceand concentration as derived from standards of knownconcentrations of the dye.

The laboratory experiments and shipboard trialsestablished that a Rhodamine WT concentration of0.1 ppm was suitable for measuring the dilution effi-ciency of BWE (detection limit <0.001 ppm). The dyewas also found to be stable over a range of environ-mental conditions (see Taylor & Bruce 1999). Relativelyhigh concentrations of plankton and particulate matterhad little or no effect on fluorescence, and the viabilityof phyto- and zooplankton was not affected by Rho-damine WT at a concentration of 0.1 ppm. It was alsoestablished that adding the dye to the bottom of ballasttanks prior to refilling ensured a high level of mixingprior to exchanges.

On the first leg of the voyage and during the earlystages of filling the ballast tanks with water uploaded

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Mar Ecol Prog Ser 350: 41–54, 2007

from Kawasaki Harbour, Rhodamine WT was addedto the tanks such that the approximate concentrationof the dye on filling was 0.1 ppm. On 24 February1999, after the tanks had been filled and the dye wasthoroughly mixed in the tanks, 1 l samples were col-lected from the surface (0.5 m), mid-depth (7.0 m) andbottom (14.0 m) using a 5 l van Dorn sampler to mea-sure the exact dye concentration after filling thetanks. Replicate samples were taken from the mid-depth stratum to assess sampling variability and aredescribed further in Taylor & Bruce (1999). This sam-pling procedure was also repeated several hoursbefore and after BWE.

On the second leg, Rhodamine WT was added to thetanks in Singapore Harbour and van Dorn samples col-lected as described above. Additional depth-stratifiedtime series samples were collected during the first ex-change after 0.75, 1.5 and 2.25 times the tank volumehad been pumped through the tank to assess the rateof dilution during exchanges. Fluorescence intensitywas used to measure the concentration of RhodamineWT in each sample and the dilution efficiency of eachexchange was determined by calculating the reductionin Rhodamine WT concentration at each depth stratum.

Temperature and salinity. During the voyage, sea-water temperature and salinity measurements weremade of the source port (i.e. Kawasaki and SingaporeHarbours), ballast (1 m depth-stratified sampling, sev-eral hours before and after exchanges on the first leg,and every 2 to 9 h during exchanges on the second leg)and open ocean surface water (daily en route, andevery 1 to 9 h during all exchanges). All measurementswere taken in situ using an Orion 140® temperatureand salinity meter with the exception of the openocean samples, which were collected using a stainlesssteel sampling bottle attached to a light rope.

Biological efficacy. At the beginning of the first leg,50 l surface, mid-depth and bottom phyto- (20 µm fil-tered) and zooplankton (100 µm filtered), and 1 l sur-face, mid-depth and bottom phytoplankton (unfiltered)samples were collected from Kawasaki Harbour (at 0.5,5.0 and 10.0 m) and the exchange and control tanks (at0.5, 7.0 and 14.0 m) to establish the composition andabundance of plankton communities uploaded fromKawasaki Harbour. Five-litre samples were collectedusing a van Dorn sampler and the filtered samples con-sisted of 10 consecutive pooled samples (i.e. 50 l) ateach depth stratum. Replicated 50 l samples were col-lected from the mid-depth stratum to assess samplingvariability of selected taxa and are described further inTaylor & Bruce (1999). Additionally, vertical phyto-(20 µm filtered) and zooplankton (100 µm filtered) nethauls were collected for further qualitative analysesof the plankton communities. This procedure was re-peated immediately before and after BWE and, for the

tank used for the second exchange and the controltank, in Singapore Harbour at the end of the leg imme-diately prior to discharge of the ballast water. Samplescollected from the beginning and end of the leg werepooled across depth strata to reduce processing time.

During BWE, daily 50 l phyto- and zooplanktonsamples were also collected via the deck hydrant toassess the composition and abundance of the planktoncommunities uploaded during the exchange. The deckhydrant was supplied by a pump and plumbing systemsimilar to that of the ballast water system, with noadditional intake or inline filters. Hence, the planktonsamples obtained from the hydrant during each ex-change were assumed to be representative of theplankton communities uploaded during the exchange.A similar sampling procedure to that described abovewas employed on the second leg of the voyage; how-ever, because a control tank was not available for thisleg, presentation of results on the biological efficiencyof BWE is limited to descriptions of observations only.Data from the second leg are presented in Taylor &Bruce (1999).

Immediately after collection, all samples were exam-ined using a light microscope to record key taxonomicfeatures and assess the viability of planktonic taxa.The samples were then preserved using Lugol’s iodinesolution (phytoplankton) or 5% formalin (zooplankton)for identification and enumeration in the laboratory(Cawthron), where all phyto- and zooplankton wereidentified to the lowest taxonomic resolution possible.Identification of phytoplankton taxa followed themethods described in Thomas (1997). Samples wereenumerated using an inverted light microscope andcounts of live phytoplankton cells were based on slightmodifications of the standard procedures described inSournia (1978). Viability was assessed on the basis ofthe integrity of the cell contents. Zooplankton taxawere identified using various literature sources, andsamples were enumerated using a Bogorov tray and abinocular light microscope. Viability was assessed onthe basis of the integrity of each specimen. If the totalzooplankton sample contained in excess of approxi-mately 200 individuals of any one taxa, counts werebased on 4 (1/8 evenly split) subsamples.

The biological efficiency of BWE was assessed bydescribing changes in the composition and abundanceof the plankton communities, and measuring changesin the concentration and richness of the source porttaxa on the first leg of the voyage. To evaluate changesin the composition and abundance of the planktoncommunities, a non-metric MDS (nMDS) ordinationprocedure based on the Bray-Curtis similarity measure(Primer v5.2.2) was used to describe changes in taxarichness and dominance among samples, following alog(x + 1)10 transformation to down-weight the influence

44

Taylor et al.: Open ocean ballast water exchange

of the most dominant taxa (Clarke & War-wick 1994). Similarity thresholds weresuperimposed on the nMDS ordinationpattern using group average clustering(Primer v5.2.2) (Clarke 1993). A SIMPERprocedure (Clarke 1993) was used toidentify the major taxa contributing toeach group.

Indicator taxa, which were used forquantifying changes in phyto- and zoo-plankton concentrations after exchanges,were defined as those taxa present in theballast water uploaded from the sourceport, but not present in open ocean sam-ples or present at <0.001 the original con-centration. Counts of dead planktonmaterial were not carried out owing toconsiderable variation in the level ofdecomposition of dead specimens.

After emptying the ballast tanks at theend of the voyage, the remaining sludgein the control tank was inspected toassess the amount of sediment uploadedin Kawasaki Harbour that had remained in the tankafter deballasting. Also, four 200 ml sediment sam-ples were taken at different locations throughout thebottom of the tank to assess the survival of sediment-dwelling organisms and check for viable dinoflagel-late cysts. Samples were refrigerated and transportedto the laboratory for inspection and culturing of thecysts.

RESULTS

Dilution efficiency

After all 4 BWE, the concentration of Rhodamine WTshowed a reduction equal to, or in excess of, 99% at all3 depth strata. Time series sampling during the firstexchange on the second leg demonstrated stratifica-tion of the dye after 0.75 the tank volume had beenpumped through the tank (Rhodamine WT dilution =47% at 0.5 m, 68% at 7.0 m, and 87% at 14.0 m). Strat-ification of the dye was less apparent after 1.5 times thetank volume had been pumped through, and at thisstage the dye dilution was more than 95% at all 3depth strata. These results provide strong evidencethat, regardless of whether the ballast tanks on the‘Iver Stream’ were filled from the top (first leg) or bot-tom (second leg) of the tanks, exchanges were veryefficient at diluting the original ballast water. Interest-ingly, this was also the case during the second ex-change on the second leg of the voyage, where only2 times the tank volumes were exchanged.

Temperature and salinity

Fig. 1 shows the daily surface seawater temperature(SST) and salinity measurements for the entire voyage.There was a steady increase in SST from 14.0°C inKawasaki Harbour (24 February 1999) to 27.8°C in theSouth China Sea (2 March 1999). SST reached a maxi-mum of 30.0°C in the tropics (10 March 1999), andbegan to decline again southwest of the SolomonIslands (19 March 1999). On the first leg, surface salin-ity increased rapidly from 31.0 on departure fromKawasaki Harbour to 35.5 after 2 d, but declined againduring the time of BWE. This was attributed to theinfluence of land run-off to the South China Sea, possi-bly from the outflow of the Mekong River.

Both exchanges on the first leg resulted in an in-crease in temperature at all 3 depth strata from ap-proximately 15.0°C (immediately prior) to 23.0°C afterthe first exchange, and from 20.0 to 27.5°C after thesecond exchange. Temperatures also increased, how-ever, from approximately 15.0 to 22.0°, and from 20.0to 27.5°C in the control tank at the correspondingtimes. Before and after both exchanges on the first leg,the salinity at all 3 depth strata reflected the salinity inthe coastal water (32.7) and open ocean (35.2 and 34.1for the first and second exchanges, respectively) at thecorresponding times. There was no noticeable changein salinity in the control tank (32.7) during the corre-sponding time intervals.

Depth profiles of salinity during the first exchangeon the second leg demonstrated initial stratification asthe high salinity open ocean water entered the tank,

45

10.0

12.0

14.0

16.0

18.0

20.0

22.0

24.0

26.0

28.0

30.0

32.0

Tem

per

atur

e (°

C)

24 F

eb26

Feb

28 F

eb2

Mar

4 M

ar6

Mar

8 M

ar10

Mar

12 M

ar14

Mar

16 M

ar18

Mar

20 M

ar22

Mar

24 M

ar

Date (1999)

31.0

32.0

33.0

34.0

35.0

36.0

Sal

inity

No

dat

a

Salinity

No

dat

a

Temperature Mid-ocean BWE

Fig. 1. Seawater surface temperature and salinity at approximately 24 h inter-vals during the entire ‘Iver Stream’ voyage. The times that ballast water ex-change (BWE) was carried out for both the first and second legs are also shown

Mar Ecol Prog Ser 350: 41–54, 2007

followed by rapid displacement of the relatively lowsalinity water uploaded from Singapore Harbour. Inthis case, complete mixing occurred before 1.5 timesthe tank volume had been pumped through the tank.Similarly, depth profiles of salinity during the earlystages of the second exchange indicated stratification,followed by rapid displacement of the original coastalwater with open ocean water after 0.9 times the tankvolume had been pumped through the tank (Fig. 2).Off New Guinea (16 March 1999), however, runofffrom the Sepik River contributed lower salinity water,which formed a layer on top of the higher salinitywater and effectively reduced the rate of dilution in thebottom layers of the tank.

Biological efficacy

The nMDS plot from the first leg shows that thephyto- and zooplankton communities uploaded in bal-last water from Kawasaki Harbour closely resembledthe corresponding harbour water (Fig. 3, Table 1).Although the open ocean community was clearly dis-tinct from that found in the ballast tanks, a number ofplanktonic taxa such as Skeletonema spp., Chaeto-ceros spp., Oithona spp., bivalve larvae, Cirripedia lar-

vae and Microsetella novegica were present in boththe Kawasaki Harbour and open ocean samples. Therewas also a relatively high diversity and abundance oftypical coastal taxa in the open ocean samples, such asthe dinoflagellate Dinophysis fortii and several zoo-plankton genera (benthic harpacticoid copepods, andCirripedia and bivalve larvae).

During both exchanges, there was a shift in speciescomposition from a Kawasaki Harbour type commu-nity to a new community (Fig. 3, Table 1), which moreclosely resembled the communities sampled in theopen ocean and was characterised by lower abun-dances overall, fewer dinoflagellate taxa and the ab-

46

32.0 33.0 34.0 35.0Salinity

2.0

6.0

10.0

14.0

0.0

4.0

8.0

12.0

Tank

dep

th (m

)

Volume pumped(tank units)

0

0.3

0.9

1.0

Fig. 2. Depth profiles of salinity after the second exchange(2 times the volume of the tank) on the second leg of the voyage

Stress: 0.06

d

e

Group 1

Group 3

Group 2Group 4

Group 5

a

b

aa a

a

a

b

b

c

c

b

Group 6

Group Tank Sample BWE

1 e Open ocean

2 b 2nd exchange (starboard) After

3 a 1st exchange (control) Beforea 1st exchange (control) Aftera 2nd exchange (control) Beforea 2nd exchange (control) Afterb 2nd exchange (starboard) Beforec 1st exchange (port) Before

4 a Kawasaki Harbour (control)b Kawasaki Harbour (starboard)d Kawasaki Harbour

5 a Singapore Harbour (control)c 1st exchange (port) After

6 b Singapore Harbour (starboard)

Table 1. Description of groups and sample types shown in Fig. 1; BWE: ballast water exchange

Fig. 3. Non-metric MDS ordination (2D stress = 0.06) showingtrajectories of phyto- and zooplankton composition andabundance in depth-stratified ballast water samples collectedfrom Kawasaki Harbour, immediately before and after ballastwater exchange (BWE), and in Singapore Harbour. Groups(indicated by dotted lines) were formed based on approxi-mately 65% Bray-Curtis similarity. See Table 1 for further

details

Taylor et al.: Open ocean ballast water exchange

sence of a number of copepod taxa thatwere relatively abundant in the Kawa-saki Harbour water (e.g. Acartia omorii,Centropages abdominalis and Daniels-senia sp.) However, relatively diversephyto- and zooplankton assemblages,including taxa of coastal origin, wereuploaded during the exchanges. Taxasuch as Clausocalanus spp. and theOncaeidae were sampled in the openocean, but not from Kawasaki Harbour,and were found to be relatively abun-dant in the tanks several hours afterexchanges. The total number of phyto-and zooplankton taxa decreased from 33in samples collected immediately beforethe first exchange to 23 taxa after theexchange (a 30.3% decrease), and from24 to 18 during the time of the secondexchange (25.0%).

Nevertheless, BWE did appear to beeffective at expelling or killing the major-ity of organisms originally uploaded inthe source port ballast water, with amarked reduction in the mean depth-stratified counts of Kawasaki Harbourphyto- and zooplankton source portindicator taxa in the exchanged tanks(Figs. 4 to 7). The reduction in the meanconcentrations of the indicator taxa was90 to 100%, except for the molluscangroup, for which concentrations beforeexchanges were very low (i.e. 0 to 1 ind.per 50 l), and therefore the estimates ofthe change in concentration are un-reliable.

More specifically, certain indicatorplanktonic taxa such as Heterocapsaspp. (Fig. 4) and polychaete larvae andjuveniles (Fig. 5) were almost com-pletely removed after the first exchange,and Gyrodinium spp., Heterocapsa spp.,Prorocentrum spp. (Fig. 6), Acartiaomorii, Centropages abdominalis, Dani-elssenia sp. and sediment-dwelling lar-val and juvenile polychaetes (Fig. 7) ap-peared to be completely removed afterthe second exchange.

Notable was the considerable varia-tion in concentrations among the 3 depthstrata for some taxa prior to both ex-changes (e.g. all indicator copepod spe-cies combined, Figs. 5 & 7). A number ofzooplankton taxa, including harpacti-coid copepods, larval and juvenile mol-

47

0 3330 0 330

2000

4000

6000

8000

10000 Before After

0

2000

4000

6000

8000

10000

Taxa

No

. cel

ls l–

1

(B) 1st exchange (control)

(A) 1st exchange (port)

0

Gyrodinium spp.

Heterocapsa spp.

Dictyocha sp.

Prorocentrum spp.

All dinoflagellates*

0 0

Fig. 4. Concentrations of indicator phytoplankton taxa in ballast water from(A) exchanged and (B) control tanks (means of depth-stratified samples ± SE)immediately before and after ballast water exchange (BWE) on the firstexchange on the first leg of the voyage. Indicator taxa were defined as thosepresent in the ballast water uploaded from the source port, but not present inopen ocean samples or (*) present in open ocean samples at <0.001 the original

concentration. Numbers above the bars are means <50

0 2.5 0 1 1.34 0 0 4 0.7 2 0.7 00

20

4060

80

100

120

0 2.7 4 5.3 00 1.3 1.3 0

Taxa

(B) 1st exchange (control)

(A) 1st exchange (port)

No.

ind

. per

50

l

Before After

0

20

4060

80

100

120

0

0

Acarti

a

om

orii

Centro

pages

ab

domina

lis

Cteno

calan

us

va

nus

Daniel

ssen

ia

sp.

All cop

epod

s

Cladoc

eran

s

M

ollus

c

larva

e/juv

enile

s*

P

olych

aete

larva

e/juv

enile

s*

Bryoz

oans

*

Fig. 5. Concentrations of indicator zooplankton taxa in ballast water from (A)exchanged and (B) control tanks (means of depth-stratified samples ± SE) im-mediately before and after ballast water exchange (BWE) on the first exchangeon the first leg of the voyage. Indicator taxa were defined as those present in theballast water uploaded from the source port, but not present in open ocean sam-ples or (*) present in open ocean samples at <0.001 the original concentration.

Numbers above the bars are means <10

Mar Ecol Prog Ser 350: 41–54, 2007

luscs, and polychaetes uploaded fromKawasaki Harbour, were only found in thebottom stratum of the ballast tanks afterBWE. This stratification may have been theresult of certain sediment-dwelling speciesbeing brought into suspension during theexchange, then settling in the bottom layerof the tank after the exchange. One of theKawasaki Harbour phytoplankton indicatortaxa (Dictyocha sp.) was not collectedbefore the second exchange on the first leg;however, viable Dictyocha sp. cells re-appeared in samples collected after theexchange. Dictyocha spp. are silicioflagel-lates, and stratification in its distributionmay be attributed to buoyancy differentialsresulting from the siliceous skeleton of thisorganism. This signals the importance ofsampling error associated when interpret-ing the results from ballast water sampling(Fig. 5).

Out of the total of 28 phyto- and zoo-plankton taxa identified in samples col-lected from the exchanged tank sampled inKawasaki Harbour, 8 taxa were still present(71.5% decrease) at the end of the first legin Singapore Harbour. Two of the indicatortaxa, both from the dinoflagellate group(Dinophysis fortii and Protoperidinium spp.),remained in the tank. The other taxa pre-sent in the exchanged tank were thediatoms Skeletonema spp., Chaetocerosspp., and Oncaeidae, Oithona spp., Cirri-pedia nauplii and Ascidiacea larvae in thezooplankton.

During both exchanges on the first leg,the nMDS plot grouped samples collectedfrom the control tank immediately beforeand after exchanges closely, indicatingthat the composition and abundance ofthe plankton community did not changemarkedly relative to the other samples(Fig. 3). A total of 30 planktonic taxa werefound in the samples collected from thecontrol tank immediately before and afterthe first exchange (0% decrease), whereasafter the second exchange, the numberdecreased from 30 before to 19 (36.7%decrease).

There was, however, a relatively largedecline in phyto- and zooplankton indicatortaxa in the control tank during exchanges.These included Prorocentrum spp. duringthe first exchange (Fig. 4), and Heterocapsaspp. and all indicator dinoflagellates com-

48

00 00 0 3.7

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Gyrodinium spp.

Heterocapsa spp.

Dictyocha sp.

Prorocentrum spp.

All dinoflagellates*

Fig. 6. Concentrations of indicator phytoplankton taxa in ballast water from(A) exchanged and (B) control tanks (means of depth-stratified samples ±SE), immediately before and after ballast water exchange (BWE) on the sec-ond exchange on the first leg of the voyage, and at Singapore Harbour(depth-strata pooled) immediately prior to discharge (not shown as all val-ues are 0). Indicator taxa were defined as those present in the ballast wateruploaded from the source port, but not present in open ocean samples or(*) present in open ocean samples at <0.001 the original concentration.

Numbers above the bars are means <50

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ollus

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BeforeAfter

0 0 0 0 0 0 00 0 0 0 0 0 00 0 0 0 00 0

2 0 00 0 2.70

1.51.3 0 0 1.3 0 1.1 00 0 00 0

Fig. 7. Concentrations of indicator zooplankton taxa in ballast water from(A) exchanged and (B) control tanks (means of depth-stratified samples ± SE)immediately before and after ballast water exchange (BWE) on the secondexchange on the first leg of the voyage, and at Singapore Harbour (depth-strata pooled) immediately prior to discharge. Indicator taxa were defined asthose present in the ballast water uploaded from the source port, but notpresent in open ocean samples or (*) present in open ocean samples at<0.001 the original concentration. Numbers above the bars are means <10

Taylor et al.: Open ocean ballast water exchange

bined during both exchanges (Figs. 4 & 6), and larvaland juvenile polychaetes, Acartia omorii and all cope-pods combined on the second exchange (Fig. 7).

During the second exchange on the first leg, therewas a more significant decline in the overall diversityand abundance of both phyto- and zooplankton (in-cluding indicator taxa) in samples collected from thecontrol tank compared to the control tank during thefirst exchange. Exceptions were indicator dinoflagellateProrocentrum spp. (Fig. 6) and several (non-indicator)diatoms, e.g. Skeletonema spp., Chaetoceros spp. andPseudonitzschia spp. Several of the indicator taxa inthe control tank incurred particularly high levels ofmortality during the time of the second exchange.For example, phyto- (Heterocapsa spp. and all dino-flagellates combined, Fig. 6); and zooplankton (Acartiaomorii, Centropages abdominalis, Danielssenia sp., allcopepods combined, Fig. 7). In addition, several othernon-indicator taxa (e.g. the diatoms Leptocylindricusspp. and Thalassiosira spp.) also showed a consider-able decline in concentration during exchanges. Othertaxa, such as Gyrodinium spp., Diplopsalis spp. andSkelotonema spp., appeared to increase or remainrelatively stable during the time of BWE.

A total of 33 plankton taxa were present in the con-trol tank in Kawasaki Harbour, with 8 of these stillpresent (75.8% decrease) at the end of the first leg inSingapore Harbour. Of the indicator taxa, no phyto-plankton taxa were present (Fig. 6) and the zooplank-ton were represented by Acartia omorii, copepods, andlarval and juvenile molluscs (Fig. 7). Other taxa pre-sent included diatoms Skeletonema spp., Chaetocerosspp., and Pseudonitzchia spp., and Anthozoa, Oithonaplumifera and Cirripedia nauplii in the zooplankton.

The results from the second leg corroborated themain findings from the first leg. In particular, beforeand after the second exchange (2 times the volume ofthe tank only) there was a significant shift in speciescomposition in the exchanged tank. After the ex-change, the phytoplankton community changed from acommunity dominated by diatoms to one dominated bydinoflagellates, and there was a particularly markedincrease in the richness of zooplankton taxa after theexchange. The relative abundance of both phyto- andzooplankton taxa was much lower prior to this ex-change, however, than was observed before bothexchanges on the first leg. This probably reflects therelatively high (8 d) containment time in the tropicsprior to commencing the exchange.

At the end of the voyage low levels of sediment hadaccumulated in the control tank even though the bal-last tanks were cleaned before the exchange trials. Noinvertebrates were found in the sediments; however,many empty phytoplankton frustules, typical of thespecies that were uploaded from Kawasaki Harbour

(mainly Skeletonema spp., Dinophysis spp., Prorocen-trum spp., and Ceratium spp.), were present. This sup-ports the view that there were high levels of mortalityin the exchanged and control tanks during the voyage.Significant, however, was the presence of a variety ofviable, unidentified dinoflagellate cysts at the end ofthe voyage.

DISCUSSION

Ballast tanks are heterogeneous environments (forexample, top of the water column versus the bottomsediments) with complex interactions between themixing dynamics of the existing water and sediments,the incoming water during BWE, and between thewater and the organisms themselves. This complexityis further increased by variation in the physical, physi-ological and behavioural tolerances of the differentgroups of ballast water organisms.

A trans-Pacific voyage of the ‘Iver Stream’ was usedto test methodologies for assessing (1) the dilutionefficiency of BWE, (2) changes in the composition andabundance of plankton communities in ballast tanksimmediately before and after BWE, and from the timethey had been uplifted in the source port to the time ofdischarge at the recipient port, and (3) the efficacy ofexchanges at expelling source port indicator phyto-and zooplankton taxa that were resident in ballasttanks before BWE.

Dilution efficiency

It was established in a previous study by Taylor &Bruce (1999) that the tracer dye Rhodamine WT is use-ful for measuring dilution efficiency of BWE, includingthe possible retention of the original ballast water inparts of the tank during the exchange. Rhodamine WTwas detected at low concentrations (<0.001 ppm) insamples collected after BWE on the ‘Iver Stream’, indi-cating a very high (>99%) dilution efficiency. In addi-tion, a high rate of dilution was achieved regardless ofthe pumping method used (i.e. the ballast tanks wereeither filled from the top and pumped out via the bot-tom, or tanks were filled from the bottom and allowedto overflow at the top). There was no sign of depthstratification of the tracer dye several hours before andafter BWE. Depth-stratified sampling of physical para-meters (such as temperature and salinity) and phyto-and zooplankton assemblages in the ballast tanks alsoconfirmed that vertical mixing was relatively thoroughafter exchanges.

Time series sampling of salinity during BWE on thesecond leg demonstrated depth stratification in the

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early stages of both exchanges. This was probably dueto the high salinity open ocean water entering the bot-tom of the tanks, which rapidly displaced the relativelylow salinity coastal water. This suggests that salinitydifferentials between the existing ballast water and theopen ocean water contributed to flow behaviours thatcaused an increased rate of dilution. This early stratifi-cation during BWE was confirmed by time series sam-pling of the tracer dye during the first exchange. Rigby& Hallegraeff (1994) reported preferential displace-ment of the original water in the early stages of an ex-change, and attributed this result to flow behavioursbetween ‘perfectly mixed’ and ‘plug flow’ conditions.

A reversal in the salinity differential occurred duringthe second exchange on the second leg. Lower levelsof salinity in the water entered the bottom of the tankas the ‘Iver Stream’ travelled in close proximity to themouth of Sepik River, resulting in the retention of someof the higher salinity water in the bottom layer of thetank during the initial stages of the exchange. Thisresult suggests that in certain situations, salinitydifferentials in ballast tanks may contribute to flowbehaviours that cause a reduced rate of dilution.

Rigby & Hallegraeff (1994) carried out 2 ballastwater exchange trials on the MV ‘Iron Whyalla’ usingthe flow-through dilution method and the tracer dyemethylene blue. Both exchanges resulted in a dilutionefficiency approximating the theoretical value of 95%.In contrast, the unexpectedly high rate of dilutionachieved by BWE on the ‘Iver Stream’ voyage wascloser to that expected when using the reballastingmethod in calm conditions (i.e. 95 to 99%; see Zhang &Dickman 1999).

Selective use of tracer dyes, such as adding the dyeprior to refilling the ballast tanks, may have applica-tion in calibrating indirect measures of dilution (forexample, the use of optical signatures, e.g. Hunt et al.2006), or standardising the dilution efficiency of tankswith different configurations. This would enable im-plementation of BWE compliance requirements fordifferent classes of vessels. In spite of this, given thelogistical constraints of having to add the tracer dye tothe tank before the exchange, it is unlikely that tracerdyes will be useful as practical compliance tools forroutinely verifying that a BWE has taken place. Theusefulness of salinity as a tool for verifying BWE isrestricted to the detection of source port water that isrelatively low in salinity (for example, brackish orfreshwater).

Biological efficacy

Depth-stratified sampling before and after BWE onthe ‘Iver Stream’ voyage showed a shift in the overall

composition and abundance of phyto- and zooplanktonfrom a community closely resembling the source port(Kawasaki Harbour) to a new community consisting ofsource port taxa, as well as taxa from the open ocean.In particular, coastal zooplankton taxa (e.g. bivalveand Cirripedia larvae, and copepods such as Oithonaspp.) as well cosmopolitan phytoplankton taxa (e.g.dinoflagellates such as Diplopsalis spp. and diatomssuch as Skeletonema spp.) appeared to replenish thetanks during exchanges.

Notwithstanding this result, both exchanges on thefirst leg suggest that BWE was effective at reducingthe abundance of the phyto- and zooplankton taxa thatwere originally uplifted from Kawasaki Harbour, asevidenced by a 90 to 100% reduction in the mean con-centrations of nearly all the indicator taxa. However,the rate of dilution of the biota did not always approachthe rate of dilution of the water (i.e. >99%), and BWEwas not as effective at reducing the overall number ofplankton taxa. The total richness of phyto- and zoo-plankton taxa, as derived from depth-stratified sam-pling before and after BWE, decreased by 30.3 and25.0% for the first and second exchanges, respectively.This compared to changes in phyto- and zooplanktonrichness of 0 and 37% for the first and second ex-change, respectively, for the corresponding samplescollected from the control tank.

Our findings are in general agreement with severalother studies on the effectiveness of BWE which havecompared the rate of dilution of the original coastalwater with the rate of removal of the organisms. Ona 16 d trans-Atlantic voyage from Israel to the USA,Wonham et al. (2001) found that although 93 to 100%of the original coastal water was removed from the bal-last tanks during BWE, the removal of the coastalorganisms ranged from 80 to 100%. These researchersalso observed mixed communities of open ocean andcoastal plankton in tanks that had been exchanged.

On a 17 d trans-Pacific voyage from Japan toCanada, Rigby & Hallegraeff (1994) found that understatic conditions (i.e. the vessel was anchored in Singa-pore Harbour) a completed exchange resulted in theretention of 5% of the original water, but 25% of theoriginal phytoplankton material remained. Similarly,Locke et al. (1983) reported that BWE were 67 to 89%effective in eliminating organisms commonly found infreshwater or brackish coastal environments. Dickman& Zhang (1999) claim that BWE by reballasting (i.e.empty-refill method) was 48% effective in reducingthe mean number of diatoms and dinoflagellates. Zhang& Dickman (1999) described that, on average, BWE(also by reballasting) reduced the number of harmfuldiatoms and dinoflagellates from 4235 to 550 cells l–1,i.e. 87% effective. The authors claim that the reasonBWE failed to eliminate all harmful diatoms and

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dinoflagellates was probably due to the ballast tanknot being completely emptied before being reballastedin the open ocean.

The ability of BWE to expel coastal organisms isdetermined by flow behaviours, the mixing character-istics of the ballast tank and the behaviour of theorganisms themselves. Preferential flows and themotion of the ship prior to and during the exchangeaffect the degree of mixing, the behavioural responsesof the various groups of organisms (for example,diatom versus dinoflagellate dominated phytoplanktoncommunities) and the rate of sedimentation (Rigby &Hallegraeff 1994). Mixing characteristics may also beinfluenced by the configuration of the ballast tank, theextent of the internal structures (such as platforms,gussets and drainage girders) and the locations of theballast intake and outlet points.

The first leg of the ‘Iver Stream’ voyage revealedconsiderable variation in the survivorship of phyto-and zooplankton taxa over the first 5 d (after the tankswere filled in Kawasaki Harbour) in both the ex-changed and control tanks. However, there was then amarked decline in the survivorship of the majority oftaxa in both the exchanged and control tanks over thefinal 7 d of the leg. Twenty-eight plankton taxa wereoriginally sampled from the exchanged tank inKawasaki Harbour, and 8 taxa were sampled from thetank (i.e. a 71.5% decrease) in Singapore Harbour.This compared with a reduction from 33 to 8 taxa (i.e. a75.8% decrease) in the corresponding control tanksamples. The concentrations of these remaining taxawere very low, however, for both the exchanged andcontrol tanks. Furthermore, although taxa such as theheterotrophic dinoflagellate Protoperidinium spp., andlarval zooplankton may have been viable at the end ofthe leg, diatoms such as Skeletonema spp. and Chaeto-ceros spp. found in both exchanged and control tanksare unlikely to have been viable, especially in the caseof the control tank.

Wonham et al. (2001) found differential survivalamong ballast tank organisms on the 16 d voyage de-scribed above. Rigby & Hallegraeff (1994) also demon-strated differential survival among taxa, and thatmotile cells of photosynthetic dinoflagellates did notsurvive in ballast tanks for more than 3 d. The rapidmortality was attributed to the movement of the ballastwater under seagoing conditions. In contrast, phyto-plankton species that were non-photosynthetic, pre-sent in resting cyst stages or were able to produce rest-ing cysts and some zooplankton persisted in the ballasttank environment for the duration of the 17 d voyage.

Sampling undertaken during the ‘Iver Stream’ voy-age demonstrated that even when ballast water is notexchanged in open ocean, the contents of relativelylarge (i.e. 1435 m3) ballast tanks can undergo marked

fluctuations in temperature (14 to 26°C) due to travel-ling over a wide range of latitudes. Marked reductionsin the diversity and abundance of ballast water organ-isms resulting from fluctuations in temperature andchanges in other physical parameters (e.g. ballastwater movement and light and oxygen limitation) leadto further effects at the biological level, such as col-lapse of the planktonic food chain.

The mortality rate of planktonic organisms origi-nally uploaded in ballast water from source ports intemperate regions is likely to be particularly high onshipping routes spanning temperate to semi-tropicalor tropical regions (e.g. Kawasaki Harbour to Singa-pore Harbour) and on trans-equatorial routes.Williams et al. (1988) reported a reduction in the sur-vivorship of planktonic taxa on shipping routes (8 to18 d) between Japan and Australia and attributed themortality to temperature or food chain effects. Thisoutcome is consistent with the results from the pre-sent study. The decline in abundance of the originalorganisms after BWE, however, may partly be attrib-uted to mortality during the exchange, rather thanexpulsion from the tanks.

This situation may contrast with much lower mortal-ity rates on voyages during which such changes donot occur; for example, over relatively short voyages(such as Australia to New Zealand) and shippingroutes that lie within a relatively narrow latitudinalrange (e.g. Chile to New Zealand). On a northernhemisphere trans-Pacific shipping route (i.e. no equa-torial crossing), Zhang & Dickman (1999) found thatthe highest number of harmful ballast water organ-isms occurred when sea temperatures in the source(Oakland, California) and the recipient (Hong Kong,China) ports were both low, and was probably due tothe minimal temperature variation between the 2ports at this time. Also, low rates of mortality oncoastal shipping routes may result in relatively highinvasion risks compared to oceanic routes (Claudi &Ravishankar 2006).

While there was a relatively large reduction in theconcentrations of the indicator plankton taxa duringBWE on the first leg of the voyage, it is unclear exactlyhow much of the attrition was due to the exchangesexpelling the biota, and how much was due to mortal-ity in the tanks. Further evaluation of this questionwould require a more intensive sampling effort thanwas feasible in the present study, such as intensivetime series analyses of plankton communities duringexchanges, coupled with a more detailed analysis ofthe viability of ballast tank organisms (for an examplesee Hay et al. 1997).

The present study indicated that the uplift of coastal-type organisms, which may include harmful species,may be enhanced if BWE is carried out relatively close

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to the coast or near the influence of large rivers. Openocean sampling on the first leg of the voyage revealedthe presence of relatively high numbers of coastal-typetaxa, e.g. including coastal phytoplankton genera,benthic harpacticoid copepods, and Cirripedia andbivalve larvae. Furthermore, although BWE on the firstleg achieved a rapid decline in the number of dinofla-gellates in the phytoplankton, an exchange on the sec-ond leg, which was carried out relatively close to thecoast near the mouth of the Sepik River, resulted in amarked shift from a diatom dominated phytoplanktoncommunity to one dominated by dinoflagellates. Dino-flagellates are common in coastal and estuarine areasand often show associations with river plumes andrainfall events (Hallegraeff 1998). This has importantimplications with regard to the implementation of ves-sel ballast water management plans and compliancewith BWE requirements, including specifying openocean regions where BWE will be most effective.Importantly, such a determination of suitable openocean regions for BWE also needs to include a consid-eration of the risk of invasion from where the ballastis discharged (Brickman 2006).

Our assessment of the efficacy of BWE at expellingthe phyto- and zooplankton indicator taxa uploadedfrom the source ports (e.g. Kawasaki Harbour) wasbased on the assumption that none of these taxa wereuploaded during the exchanges. Although samplingof the open ocean plankton communities was carriedout at various times throughout the exchanges, andtaxa that were common in both the source port andopen ocean samples were eliminated as indicators ofsource port taxa, plankton communities are notori-ously patchy in both space and time. This patchinessmay confound quantitative assessments of the dilutionof indicator taxa during BWE; hence, such assess-ments are unlikely to be useful as a direct means ofverifying BWE.

Alternatively, although certain taxa (e.g. cosmo-politan diatom species, and phytoplankton such asDictyocha spp. and invertebrate larvae that are com-mon in both coastal waters and in the open ocean) areunlikely to be useful for directly quantifying changesin concentration during BWE, the open ocean plank-ton as a whole could be sampled during exchanges tocharacterise the composition and abundance of thecommunity, with potential application as a measurefor helping to verify whether exchanges have takenplace.

However, regardless of depth recommendations forBWE (e.g. 2000 m), greater emphasis should be placedon whether the water uploaded in the open ocean is, infact, sufficiently oceanic (that is, without coastal organ-isms) to minimise invasion risks. On some shippingroutes, e.g. Japan to New Zealand (via Singapore),

BWE are likely to be carried out in relatively shallowwaters near the influence of large rivers. Such ex-changes increase the potential to replenish ballasttanks with harmful organisms and salinity differentialsthat may influence the dilution efficiency and effec-tiveness of BWE at expelling the original organisms inthe ballast tank.

In summary, we recommended that the use of phyto-and zooplankton communities as indicators of the effi-cacy of BWE should include assessment of:• changes in species composition and abundance of

the plankton assemblages and sediment-dwellingorganisms brought about by the exchange, includingsampling of the open ocean water;

• the incidence of coastal versus oceanic, and cold ver-sus warm water species found in ballast tanks and,with regard to the survivorship potential of plank-tonic organisms during a ship’s voyage, the incidenceof taxa known to be relatively tolerant of such envi-ronments (e.g. dinoflagellate cysts; see Hallegraeff& Bolch 1992, Hallegraeff et al. 1997, and Mountfortet al. 1999);

• the relative abundance of viable phytoplankton com-munities, which may be indicative of recent BWE(Hallegraeff & Bolch 1992, Hay et al. 1997);

• the presence of selected harmful organisms (e.g.Asterias amurensis).

FUTURE RESEARCH

The biological aspects of this study focused onchanges in the composition and abundance of plank-tonic communities and suspended sediment-dwellingorganisms, e.g. juvenile spionid worms, which arereadily collected in plankton samples. Although suchorganisms are potentially harmful if translocated tosuitable new environments, a greater range of poten-tially harmful organisms (e.g. coastal fish species andpathogenic bacteria) can be translocated in ships’ bal-last water than were sampled here. Future studies onthe efficacy of BWE for expelling unwanted organismsshould consider variation in the effects of exchangeson these additional groups of organisms.

Trading patterns have been shown to have a signi-ficant effect on invasion rates in various parts of theworld, including New Zealand (Taylor et al. 2000).Ruiz et al. (2000) collated information on coastal ma-rine communities in North America and establishedthat the rate of invasions has increased exponentiallyover the last 200 yr, and that shipping has been themain vector. The authors concluded that the sourceregions for invasions corresponded to patterns oftrade. The results of the ‘Iver Stream’ voyage indi-cated that, in certain situations, shipping routes span-

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ning temperate to tropical regions may be as equallyor more effective than conducting BWE. Controlledshipboard trials (ideally on the same ship using thesame ballasting procedures but on different voyages)comparing survivorship rates of ballast water organ-isms on shipping routes that span a range of latitudeswould help to clarify the importance of temperaturechanges within ballast tanks. This would help identifyhigh risk shipping routes, thus facilitating the devel-opment of appropriate ballast water regulations andmanagement options. Studies on the survivorship ofballast water organsims should also consider theimportance of ship type.

Future research on the usefulness of plankton com-munities as indicators of BWE should include the col-lation of baseline information. These include a broadscale biogeographical database on coastal and openocean plankton communities occurring at differenttimes of the year, while encompassing the main ship-ping routes. This would improve our understanding ofthe significance of plankton communities uploadedduring BWE. Data on the phyto- and zooplankton com-munities uploaded on coastal shipping routes alsorequires consideration (Claudi & Ravishankar 2006).Further, the selection of easily applied indicators of thebiological efficacy of BWE requires adequate knowl-edge on the spatio-temporal distributions of a rep-resentative range of ballast water taxa, as well asidentification and quantification of the key factors thatdetermine species survivorship en route. These factorsinclude the physiological tolerances of the organisms,food supply, reproductive capacity and containmenttime, and the interactions between these factors. Thisbaseline information could be used for designingmultiple ship surveys on ballast water risks, includingfurther studies on the effectiveness of BWE, and fortargeting compliance.

The limited efficacy of BWE as a treatment methodfor minimising potential future species introductionsvia ballast water has led to the investigation of tech-nologies to provide more reliable alternatives, some ofwhich show promise, e.g. cyclonic separation, filtra-tion, ultraviolet radiation, oxygen deprivation, heattreatment, ozonation, or a combination of these. Manytechnological challenges remain, however, includingthe design of effective as well as economically robusttreatment systems that are compact enough them to beretrofitted to merchant ships.

Acknowledgements. Thanks to Vroon BV, Ship Managers(the Netherlands), for permission to travel aboard the ‘IverStream’, and Pacifica Shipping for permission to travel aboardthe ‘Spirit of Vision’. We also appreciate the support of theships’ officers and crews. This research was funded by the NZMinistry of Fisheries and the NZ Foundation for Research,Science and Technology.

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Editorial responsibility: Victor de Jonge (Contributing Editor),Haren, The Netherlands

Submitted: March 30, 2005; Accepted: April 24, 2007Proofs received from author(s): November 12, 2007