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Aquatic Invasions (2012) Volume 7, Issue 1: 2 9 -3 6
W
doi: 10.3391/ai.2012.7.1.004(Open Access)
© 2012 The Author(s). Journal compilation © 2012 REABIC
D C A ß in
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A IC
y IV - / \ l
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Proceedings o f the 17th International Conference on Aquatic Invasive Species (29 August-2 September 2010, San Diego, USA)
R esea rc h A rtic le
Re-growth of potential invasive phytoplankton following UV-based
ballast water treatment
V io la L ieb ich * , P e te r P au l S teh o u w er an d M arcel V eldhuis
D epartm ent o f B iological Oceanography, R oyal N etherlands Institute fo r Sea R esearch, P .O .B ox 59, N L -1790 AB, D en Burg,
Texel, The N etherlands
E-mail: V iola.Liebich@ nioz.nl (VL), P eterPaul.Stehouw er@ nioz.nl (PPS), M arcel.Veldhuis@ nioz.nl (MV)
*Corresponding author
Received: 31 March 2011 / Accepted: 27 August 2011 / Published online: 11 October 2011
E d ito r ’s n ote:
This special issue o f Aquatic Invasions includes papers from the 17th International Conference on Aquatic Invasive Species held
in San Diego, California, USA, on August 29 to September 2, 2010. This conference has provided a venue for the exchange o f
information on various aspects o f aquatic invasive species since its inception in 1990. The conference continues to provide an
opportunity for dialog between academia, industry and environmental regulators within North America and from abroad.
A b stra c t
Ballast water contains organisms which can survive the ship’s journey and become established in the recipient w ater body when
discharged. Phytoplankton species can become invasive and might be harmful by producing toxins or anoxic conditions following
their blooms. Different technologies exist to treat ballast w ater in order to reduce the spread o f invasive species. The effectiveness of
a UV-based ballast water treatm ent system was tested in an incubation experiment over 20 days. After an initial decline in cell
numbers, re-growth could be observed o f certain phytoplankton taxa, namely the diatoms Thalassiosira, Skeletonem a, Chaetoceros,
P seudo-nitzschia, and N itzschia (order represents rank o f abundance). The conclusion o f this study is that a variety o f taxa are able
to survive UV-treatment. These may include harmful and potential invasive phytoplankton species. Long-term incubation
experiments should be considered when testing the effectiveness o f UV-based treatm ent systems. The dominant re-growing
phytoplankton group was Thalassiosira which could be a suitable indicator organism for testing the efficiency o f UV-units.
K e y w o rd s : UV-treatm ent, bioinvasion, Thalassiosira, Skeletonem a, Chaetoceros, HAB
In tro d u c tio n
O rganism s are transported v ia the b allast w ater
o f ships (C arlton and G eller 1993;W illiam s et al.
1988). W hen non-indigenous species are released
at the port o f destination, they may becom e
established in the recipient ecosystem and spread
(K olar and Lodge 2001). These invasive species
can pose a risk to b io diversity (M cG eoch et al.
2 010) and, in som e cases, also to hum an health
(R uiz et al. 2000). Presently, different m ethods
exist to treat b allast w ater (T solaki and
D iam adopoulos 2010) to reduce num bers o f
contained organism s in accordance w ith the
B allast W ater C onvention adopted by the
International M aritim e O rganization (IM O)
(IM O
2004).
The
convention
includes
requirem ents (D2 standard) w hich refer to the
discharge o f certain concentrations and size
classes o f organism s. To reduce num bers o f
viable organism s in b allast w ater, one option is
the use o f certain w avelengths o f ultraviolet light
(UV-C). U V -radiation penetrates through cell
m em branes
of
organism s
and
dam ages
deoxyribonucleic acids (Q uek and H u 2008). F or
this reason, U V -treatm ent is com m only used fo r
disinfection o f drinking w ater (C hoi and Choi
2010). The lethal U V -dose is an im portant issue
o f research as phytoplankton and b acteria are
able to recover. The m arine diatom C yclotella
sp. fo r instance w as able to repair the DN A
dam age caused by UV-B radiation w ithin hours
(G ieskes and Bum a 1997). E ven w hen UVtreatm ent (U V-C) reduced the viable count o f
m icroorganism s, rem aining bacteria w ere able to
grow again (W aite et al. 2003).
29
V. Liebich et al.
The effectiveness o f U V -dosages depends
largely on the organism , its size and pigm ents
(G regg et al. 2009). P otential survival and re­
grow th o f (harm ful) organism s after treatm ent
should be considered w hen exam ining the
effectiveness and efficiency o f b allast w ater
treatm ent system s (BW TS), although this is not a
standard requirem ent o f IM O ’s guidelines for
approval o f B allast W ater M anagem ent System s
G 8 (A nonym ous 2008). H ow ever, only a few re­
grow th studies have b een conducted so far. F or
exam ple, Stehouw er et al. (2010) show ed that
after usin g different dosages o f U V -radiation,
several unidentified p hytoplankton groups did
survive U V -treatm ent and re-grew in long-term
incubation experim ents. H ow ever, no fu rth er
taxa specification o f re-grow ers w as given.
The p resen t study aim ed at exam ining survival
and re-grow th o f phytoplankton after UVtreatm ent in long-term incubation experim ents
over 20 days. Flow cytom etry w as applied to
exam ine tim ing o f re-grow th and to indicate
num bers and size o f cells. Specifically, it w as the
aim to identify p hytoplankton genera and species
by usin g light m icroscopy. Special focus was
draw n on diatom s due to th e ir high ecological
relevance as a m ajor group o f the phytoplankton,
the presence o f some invasive and harm ful
species (N ehring 1998), th eir ability to survive
several w eeks in the dark (Peters 1996), and the
form atio n o f resting stages (Sugie and K um a
2008). Several studies confirm th at diatom s are
com m only found in b allast w ater (O lenin et al.
2000; M cC arthy and C row der 2000).
R e-grow th after U V -treatm ent may occur
related to quantitative or qualitative causes.
Q uantitative causes include a b etter chance o f re­
grow th based on m ore surviving individuals o f
species w ith in itial high num bers. Q ualitative
causes include p hysiological cell properties
w hich support survival and re-grow th. A
com parison b etw een species th at survive and regrow and those that do not may reveal especially
U V -resistan t species. These species could then
be considered as indicator organism s fo r testing
the effectiveness o f U V -treatm ent. So far, a large
diversity o f p hytoplankton organism s has b een
used (T solaki and D iam adopoulos 2010). U sing
different
phytoplankton
species
m akes
com parison and com pliance control com plicated
as differences in sensitivity to U V -dosage m ight
affect test results. A standard phytoplankton
species w ould therefore sim plify the testin g o f
U V -based BW TS.
30
P hytoplankton species w hich are more
resistant to U V -treatm ent and are faster to
recover (repair potential dam age) could re-grow
and becom e invasive in th eir new environm ent
after discharge. It is o f special interest to
exam ine the re-grow th potential o f harm ful or
invasive m icroalgae. To specify these re-grow ers
and th eir functional aspects is essential fo r risk
assessm ent and m itigation strategies. The
identification o f the re-grow ing phytoplankton
groups is also crucial to determ ine effectiveness
and efficiency o f U V -treatm ent. F o r U V -units it
m ight be more efficient to reduce the intensity if
the required reduction o f organism concentration
is already achieved w ith low er dosages.
Methods
B allast w ater treatm ent tests w ere conducted at
the harbor o f the R oyal N etherlands Institute for
Sea R esearch (N IOZ, Texel, The N etherlands).
F or fu rther inform ation on this land-based test
facility fo r BW TS see V eldhuis et al. (2006).
The treatm ent system in the present study used a
20 pm m esh-size filte r and low -pressure UV radiation (fixed w avelength o f 254 nm). W ater
from the W adden Sea (a turbid estuary) was
filtered and processed w ith U V -radiation at
intake (ballasting) and discharge (deballasting).
In betw een, the w ater w as stored in holding
tanks fo r five days sim ulating conditions during
a ship journey. Tanks had a size o f 300 m3 and
w ere either located underground or at the
surface. The tem perature difference betw een the
tanks
w as
negligible
(unpublished
data).
E xperim ents w ere conducted based on norm al
scheduled test runs according to the G 8
guidelines (A nonym ous 2008). They w ere
carried out in duplicate resulting in two tanks (I
and II). A fter filling tank I w ith treated water,
the system w as shut dow n and pipes were
em ptied. T hen a control tank w as filled and after
another tem porary shutdow n, w ater w as treated
and pum ped into tank II. F or b o th replicate
tanks, the w ater w as new ly treated. The first
incubation experim ent started 1st o f A pril 2010
and the second one 13th o f M ay 2010, latter w ith
two bottles fo r each tank. F or the control, harbor
w ater w as pum ped (200 m 3/h) into a holding tank
w ithout passing through the treatm ent system . At
day zero o f the intake series w ater w as pum ped
up, filtered by the system and processed w ith
U V -radiation. The w ater w as treated a second
tim e after five days w hich is day zero o f the
discharge series. E ach series w as incubated for
Re-growth of potential invasive phytoplankton
20 days. Sam ples w ere co llected from the control
C, I Intake (filter+U V ), II Intake (filter+U V ), I
D ischarge (filter+U V +U V ), and II D ischarge
(filter+U V +U V ).
The sam ples w ere incubated in clean 10 L iter
N algene (R ochester, U SA ) b o ttles and w ere kept
in a clim ate-controlled room w ith a tem perature
o f 15°C (+/-2°C) and a 16:8 hour light/dark
period,
sim ilar to
local, natural grow th
conditions. The b o ttles w ere placed o n m agnetic
stirrers,
w hich
m aintained
gentle
w ater
m ovem ent to p revent the phytoplankton from
settling. N utrients w ere added at concentrations,
w hich are typical fo r the W adden Sea in early
spring (PO 4 1,6 pm ol/L , N 0 3 20 pm ol/L , S i0 3 20
pm ol/L). Sam ples w ere tak en daily fo r analyzing
phytoplankton concentration and com position.
P hytoplankton w as quantified by flow cytom etry
(C oulter E pics X L-M CL w ith a 488 nm argon
laser, M iam i, USA ). The flow cy to m eter
m easures various properties o f individual cells
including size and chlorophyll fluorescence
(V eldhuis and K raay 2004). Sam ples o f one
m illiliter w ere m easured in triplicate, u sing the
red autofluorescence o f the chlorophyll signal to
differentiate b etw een phytoplankton and other
particles. Sam ples fo r species identification
(H oppenrath et al. 2009) w ere exam ined u sing an
inverted light m icroscope (Zeiss A xiovert, 400 x,
O berkochen, G erm any). These sam ples had a
volum e o f five m illiliters, they w ere w ell-m ixed,
and not preserved. A ll cells and p articles in these
sam ples w ere allow ed to settle fo r at least 30
m inutes.
Results
Flow cytom etry
U V -treatm ent decreased phytoplankton cell
num bers (Figure 1). The decline in total cell
num bers occurred during the first w eek o f the
treated intake and discharge sam ples o f b o th
replicate tanks in A pril as w ell as in M ay. R e­
grow th, indicated by an increase o f cell num bers,
occurred com parably in all incubation bottles
after day seven. The num erical trend over the
first tw o w eeks is com parable fo r all replicates in
both experim ents. In M a y ’s discharge sam ples,
num bers in different b o ttles range in extrem e
cases from 17200 cells p er m illiliter after three
w eeks in tank I bottle one to 300 cells p er
m illiliter after three w eeks in tank II bottle two,
b u t in the series them selves the overall trend
(first decline and re-grow th after seven days)
was again com parable. In b o th experim ents,
phytoplankton cell num bers in the control
sam ples w ere considerably different from the
treated sam ples.
L ig h t m icroscopy
In A pril, Thalassiosira w as the m ost abundant
p hytoplankton group in the control sam ple;
additional phytoplankton included the diatom s:
A ste rio n ello p sis, C haetoceros, C oscinodiscus,
D itylum , G uinardia, N itzschia, P seudo-nitzschia,
and Skeletonem a (Figure 2). The control sample
o f M ay contained the above m entioned taxa as
w ell as M ediopyxis, O dontella, and P haeocystis.
In M a y ’s control sam ple, M ediopyxis w as the
m ost abundant species. In the incubation
experim ents, the follow ing five taxa re-grew
after U V -treatm ent: Thalassiosira, Skeletonem a,
C haetoceros, P seudo-nitzschia, and N itzschia
(this order represents rank o f abundance
estim ated from all light m icroscopy sam ples).
Thalassiosira cells w ere re-grow ing in every
series o f the first and second experim ent. In all
four discharge sam ples o f the M ay series,
Thalassiosira w as the only phytoplankton group
com ing back. Skeletonem a w as the m ost
abundant re-grow ing phytoplankton group in the
intake and discharge sam ples o f A pril and in all
four intake sam ples o f M ay. P seudo-nitzschia
was the m ost abundant group in the A p ril’s
discharge sam ple o f the second tank. N itzschia
cells w ere re-grow ing in two intake sam ples, one
from each experim ent. In M ay, C haetoceros regrew in b o th bottles o f tank I after being treated
once w ith U V -radiation.
A ll intake sam ples contained, at day zero a
few hours after U V -treatm ent, som e intact
Thalassiosira
cells
but
rarely
other
phytoplankton. A t day eight, all intake sam ples
from A p ril’s and M a y ’s replicates looked
com parably em pty, containing single diatom cell
w alls w ithout cell content. A t day tw o or four,
sam ples appeared in a sim ilar way em pty like
sam ples at day eight. T en and tw elve days after
U V -treatm ent, the A pril intake sam ples o f tank I
contained few Thalassiosira cells b u t more
Skeletonem a. T ank II sam ples at th at tim e
contained m ostly Thalassiosira cells. In all o f
M ay ’s intake sam ples, Skeletonem a w as the m ost
abundant phytoplankton b u t only occurred after
day ten. In intake sam ples o f tank I in M ay,
C haetoceros cells w ere nearly as abundant as
Skeletonem a cells.
31
V. Liebich et al.
100000
100000
10000
10000
Control
- A - Control
M—Intake
M—Intake
A Discharge
A Discharge
Figure 1. Phytoplankton cell concentrations after UV -treatm ent at intake (day 0) and discharge (day 5), analyzed by flow cytometry.
Incubation experiment one was perform ed in April (A) and experiment two in May (B). Data points show mean o f incubation
samples, error bars indicate standard deviation, no error bars are given for M ay’s discharge samples due to distinct numerical
differences (see text).
r
Control
Asterionellopsis
Chaetoceros
Coscinodiscus
Ditylum
Guinardia
Nitzschia
Pse udo- nitzschia
Skeletonem a
Intake (lx UV)
I
II
Discharge (2x UV)
Skeletonem a
Skeletonem a
Thalassiosira
Thalassiosira
Nitzschia
Skeletonem a
Pseudo-Nitzschia
Skeletonem a
Thalassiosira
Thalassiosira
Thalassiosira
o
1—1
o
See Control
Chaetoceros
Nitzschia
A p r il
]-l
Thalassiosira
1-2
Thalassiosira
¡II-1
Thalassiosira
! II-2
Thalassiosira
Skeletonem a
+Mediopyxis
Thalassiosira
+Odonteila
+Phaeocystis
Chaetoceros
Skeletonem a
Thalassiosira
\ __________________________________ y
Pseudo-nitzschia
Skeletonem a
Thalassiosira
[ II-2
11
Skeletonem a
i
Thalassiosira
ji
Figure 2. Overview o f identified phytoplankton groups in re-growth experiments after UV-treatment. Control = untreated water,
Intake = filtered and once UV-treated in replicate tanks I and II, Discharge = Intake with second UV -treatm ent after five days and
two bottles for each tank in May. Taxa in bold letters m ark the dominant group o f this sample.
32
Re-growth of potential invasive phytoplankton
D ischarge sam ples out o f tanks I and II, a few
hours after the second treatm ent, show ed no
intact cells. Sam ples o f the A pril series at day
ten
contained
m ore
Skeletonem a
than
Thalassiosira cells (tank I) w hich w as still the
case at day 20. P seudo-nitzschia w as m ore
abundant than Skeletonem a (tank II), and by day
20 this in cubation sam ple additionally contained
some Thalassiosira. D ischarge sam ples in M ay
contained nearly no cells at days one and ten, but
several Thalassiosira cells by day 15 and even
m ore at day 2 1 .
Discussion
B allast w ater is the m ain v ecto r fo r invasions in
m arine environm ents (G ollasch 2006). P h y to ­
plankto n is know n to be transported v ia b allast
w ater, to becom e invasive, and in some cases to
pose a th reat to ecosystem fu n ctio n o f the
recipien t environm ent. The objectives o f this
study w ere ( 1) to identify if and w hich
phytoplankton groups are re-grow ing after UVtreatm ent; (2) to find possible success factors for
the survivorship o f phytoplankton groups
regarding usability as indicator organism s fo r
treatm ent effectiveness; and (3) to evaluate if
there is a risk through invasive (harm ful)
m icroalgae even though the b allast w ater is
treated.
R e-grow th o f id en tified phyto p la n kto n g roups
D ata o f the flow cytom eter indicate cell size and
num bers b u t the various clusters could not refer
to species level. A size range from 10 pm up to
50 pm is accurately detected by the flow
cytom eter. H ow ever, there is a chance that
b ig g er and less com m on cells, chains or colonies
are not in the m easured volum e w hich is only a
p art o f the entire sam ple. This could explain that
cell num bers in the treated sam ples outnum ber
cell counts o f the control after approxim ately ten
days. C ontrol w ater w as unfiltered, thus
contained larger organism s like D itylum cells,
A sterio n e llo p sis, and M ed io p yxis chains. These
w ere seen u sing the light m icroscope, b u t w ere
not m easured by the flow cytom eter.
The m ain re-grow ing phytoplankton groups
w ere:
Thalassiosira,
Skeletonem a,
and
C haetoceros. F o r Thalasiosira and Skeletonem a
it w as not possible to identify at the species level
(w ith only a light m icroscope). C haetoceros
could be identified as C. socialis due to its
characteristic colony form ation. Skeletonem a
costatum is a species m entioned in several
b allast w ater (treatm ent) studies (e.g. Sutherland
et al. 2001; K ang et al. 2010). There is how ever
evidence th at “w ithin the species com plex once
perceived as “ Skeletonem a co sta tu m ,” there are
cases o f very clear distinction am ong species for
m orphological, phylogenetic, and ecological
traits.” (Sarno et al. 2005 p. 174). F or the exact
species o f Skeletonem a, as w ell as fo r the other
m entioned diatom s in our study, additional
genetical studies or identification w ith an
electron m icroscope w ould be needed.
In A pril, Thalassiosira w as the dom inant
phytoplankton group in the control sam ple. It
was also re-grow ing in every incubation sample.
These results could lead to the assum ption that
this re-grow th is only occurring as a m atter o f
chance, resulting from high initial num bers.
Skeletonem a w as found in the control sam ple in
num bers com parable to species w hich did not regrow. H ow ever, if it w as present as a re-grow er
it w as m ost often (six out o f eight tim es) also
dom inant. These results could indicate certain
advantages o f Skeletonem a over the other
p hytoplankton groups. P seudo-nitzschia was
p resent in only one discharge sam ple as m ost
abundant taxa b u t w as not found before the
second treatm ent; m aybe it w as present as
resting cells (O rlova and M orozova 2009). In
M ay ’s control sam ple, M ediopyxis helysia is the
m ost abundant species b u t it did not show re ­
grow th at all. It w as the largest species in A pril
and M ay, w ith single cells having length
m easurem ents o f 44-1 2 5 pm (apical axis or
w idth o f chain) and 2 7 -7 8 pm (pervalvar axis)
(H oppenrath et al. 2009). It is therefore unlikely
th at M ediopyxis helysia w as able to pass the 20
pm m esh sized filter lined in fro n t o f the UVunit.
Success fa c to rs fo r the survivorship and usability
as indicator organism s
The identified re-grow ers in the present study
w ere all diatom s, w hich are ideal candidates for
successful b allast w ater transport (M cC arthy and
C row der 2000). This is because they are small,
robust as vegetative cells or resting stages, and
able to survive dark and unfavorable conditions
in the tank. M ost diatom s also have a broad
tem perature range; species o f the genus
C haetoceros, Skeletonem a, and Thalassiosira
33
V. Liebich et al.
grew from -1,5°C up to at least 20°C (Baars
1979). V iable cultures o f P seudo-nitzschia w ere
collected from b allast w ater tanks underlining
the ability to survive darkness fo r days
(H alleg raeff
1998).
C haetoceros
and
Thalassiosira species w ere not only found as
v egetative cells in b allast w ater b u t also as
resting stages (K lein et al. 2009). Skeletonem a
resting form s are also know n (D urbin 1978). The
form atio n o f resting stages could facilitate
survival o f U V -treatm ent.
R e-grow th o f p o tential invasive organism s
m ight be supported by optim al light and nutrient
conditions and does not necessarily m ean that re­
grow th occurs in dark ballast w ater tanks. M ost
invasive organism s fail also to estab lish after
introduction (W illiam son and F itter 1996). F or a
successful establishm ent habitat invasibility and
propagule pressure play an im portant role as w ell
as invasiveness (L onsdale 1999). Invasiveness is
the ability to be successful in new environm ents
and depends on species traits (C olautti et al.
2006). A h ig h grow th rate is considered to be a
functional trait o f a successful plant invader (van
K leunen et al. 2010). In general, sm aller cells
show h igher grow th rates th an large ones
(K agam i and U rabe
2001).
C haetoceros ,
Skeleto n em a, and Thalassiosira are sm all sized
taxa and by th eir high grow th rates could have an
advantage w hen recovering and re-grow ing.
Species o f the three re-grow ing genera have a
broad tem perature tolerance, restin g form s, and
high grow th rates. T herefore, they appear to have
g reater p o tential to survive treatm ent and
becom e invasive than the other id entified
m icroalgae.
Some non-native Thalassiosira
species are know n to be already established in
the N orth Sea (R eise et al. 1998). Thalassiosira
cells w ere dom inant as re-grow ers, are easy to
culture (unpublished data), and com m only found
in the m arine environm ent. T herefore we
consider them as suitable indicator organism s for
testing the effectiveness and efficiency o f UVunits.
R isk evaluation fo r (harm ful) algae invasions despite U V-treatm ent
H arm ful diatom s like toxic P seudo-nitzschia
species causing A m nesic S hellfish P oisoning can
be transported v ia b allast w ater (Zhang and
D ickm an 1999). H ow ever, harm ful diatom s are
not only those producing toxins. Species o f the
genus C haetoceros have spines w hich are
thought to cause m echanical dam age to fish gills
34
(Bell
1961).
E cological
im plications
of
phytoplankton invasions may include changes in
the biodiversity o f the food-w eb after successful
establishm ent.
Species
of
C haetoceros ,
S keletonem a, and Thalassiosira are know n to
form bloom s (T iselius and K uylenstierna 1996),
thus may increase local bloom ing events leading
to anoxic conditions follow ing th eir decay.
Species o f the identified re-grow ing genera
m ight not only get invasive but also cause
negative effects on the recipient ecosystem .
C onclusion
It should be noted that the tested U V -treatm ent
system in the present study caused a decline o f
phytoplankton num bers in com pliance w ith the
D2 standard. Incubation experim ents are not
required fo r the G8 guidelines but help to
evaluate
effectiveness
and
efficiency
of
treatm ent system s. O ther studies also exam ined
plankton com position in incubation experim ents
after U V -treatm ent. W aite et al. (2003) show ed
the decline o f phytoplankton after 18 hours. The
present study proves how ever, that possible re ­
grow th could only be seen after seven days.
Sutherland et al. (2001) conducted incubation
studies lasting fo r 16 days. They focused on the
three dom inant phytoplankton taxa C haetoceros
g ra c ile , Skeletonem a costatum and Thalassiosira
sp.: our results validate the choice o f the tested
genera. If incubation experim ents show that
there is a chance o f introducing invasive
(harm ful) species despite treatm ent, additional
tests should be considered.
A cknow ledgem ents
This work has been co-funded by the North Sea Region
Programme under the ERDF o f the European Union. The PhD
scholarship for this work is gratefully appreciated and was
provided by the Max Planck Institute for Comparative and
International Private Law/International Max Planck Research
School for Maritime Affairs. We would like to acknowledge
the team o f Aquaworx for providing their AquaTriComb™
system. Two anonymous reviewers provided comments
helping to improve this paper.
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