J.

~~
Ph)'c./' 28, 723-729 (1992)

MINI REVIEW

THE SPECIES CONCEPT IN PHYTOPLA NKTON ECOLOGY'

A. IVIichelle Wood and Tanya Leatham
Department of Biology. U niversity of Oregon, Eugene, Oregon 97403

among phytoplankton species or species complexes.

It is clear that th ere is tremendous diversity among
morphological types that would be identified as the
same "species" by the practicing ecologist. Over a
wide range of temperatures, Hulburt and Gui llard
( 1968) found more than a 25 % difference in the
growth rate of the two different clones of Skelelonpma
troJiicu III. When two clones of Bellerachea sJiinifera
were exam ined, one required thiamine and one did
not (Hargraves and Guillard 1974). When two clones
of Fragilaria pinnala were examined, one required
BI2 and the other did not (Hargraves and Guillard
1974). When the si licon uptake kinetics and growth
rate of two strains of Asterionella formosa were compared, a nearly two-fold differe nce in both doubling
time and half-saturation constant was observed between the two strains (Kilham 1975). The depend-.
ability of interclonal variation evidenced from the
data in Table I hints at extraordinary diversity in
natural populations, particularly since significant interclonal variation is observed when o nly a few strains
are compared. It could be argued that many of the
studies that involve on ly a few clones exaggerate the
overa ll diversity within taxa because they deliberately utili ze clones from distinctl y different environments. Examples are the work by Underh ill (1977)
on a temperate and a subtropical clone of BiddulJihia
auri/a and the literature from the Guillard laboratory establishing the ocean ic-neritic boundary as a
selective gradient (recentl y reviewed by Brand 1988/
1989). Contraril y, it could be argued that these studies all underestimate genetic diversity within taxa
because they rely on genotypes that can be cultured
and maintained in the laboratory. Regardle ss, it is
remarkable that for nearly every physiological character examined, significant interclonal variability is
found essentiall y every time that strains from the
same putative taxon are compared.
The magnitude of these differences is not trivial.
Data for several ultra phytoplankton taxa show that
accl imated growth rates of genetically different
strains, identified by morphological criteria as members of the same species and isolated from the same
water mass , differ by factors of between 1.2 and 1.6
(Brand 1981). Average growth rates observed in th is
study wereon the order of 1.5-2.2 days, which means
that, within a few months of continuous directional
selection, an initially very rare genotype would become the dominant strain in asexua ll y reproducing
populations (Fig. I). When the direction of selection
changes every few genera lions, as may often happen

Phytoplankton ecology relies heavily on the use

of taxon-insensitive indices like chlorophyll a. concentratio n, "e incubatio ns, and lig ht-da rk boules
for measurement of phytoplankton abundance and
productivity. Even so, phytoplankton ecologists generall y recognize that the species composition or

structure of a phytoplankton commun ity has pronounced effects on ecosystem structure and function. Numerous studies claim to document interspecific differences in important physiological
parameters like nutrient utilization and storage capacity (Dortch 1982), dark nitrogen uptake (Paasche
et al. 1984), fatty acid composition (Thompson et
al. 1990), sensitivity to ultravio let irradiance (Karentz et al. 199 1), or an iron requ irement for growth
(Sunda el al. 1991). However, despite the fact that
these are among the finest and most rigorous studies
in comparative algal ph ysiology, for the reasons explained below, none ojlhelll aclua.II),delllonsirale s/Jecies-

level differences in the traits oj interest.

It has been more than a decade since Gallagher'S
( 1980, 1982) and Brand's ( 198 1, 1982) unequivocal
demonstrations of tremendous genetic diversity in
natural populations of important phytoplankton
species. It is over 40 years since Braarud ( 195 1) first
discussed the ex istence of different ecotypes or races
of phytoplankton and almost 20 years since Doyle
(1975) d iscussed the importance of this problem in
oceanography. Amazingly, as exemplified by the papers cited above, it is sti ll standard practice to characterize the phenotype ofa microa lgal species, however defined, using on ly a single clonal isolate. The
problem with this approach is that it auempts to
identify significant interspecies differences without
estimating the magn itude of within-species variation. This is a problem in basic experimental design,
not a problem that arises because no menclatural
"species" of phytoplankton are not always true biological species [sensu Mayr (1969), that is, composed of a set of potentially interbreeding genotypes]. Without an estim ate of intra-group variation ,
it is impossible to determine whether or not th e
differences observed between nominal phytoplanklOn groups ("species" or otherwise) are any greater
than might be observed in a random sample of different members of the same group.
Table I summarizes much of th e lite rature on
interclonal var iat ion in ecologicall y important traits
I Dedicat ed lO R. R. L. Guillard, who continues to inspire and
promote phytoplankton research e ven in his "retirement."

723

\.

724

A . MI C m : LL E WOOD A N D TA N YA L EATHAM

TARLE

I.

Ill /ne/oual variation ill phJsiological Gild biochf'l1I;cal trails of ph),lo/Jlallktoll sPt'cit's (I lid sPf'cit's comp/,.w s. )' "" )'1'5; N =
C h ar.lCler

Spedc5

Sali nity-depende nt gro \vth r ale

ProroCt'lltrlllll mica"s
Phat'odacl),/ulII (r;COrtlll tulII Bohlin
DitJI1I11I brightwt'llii (West) Grunow
Shelp/OllnT/ a costalulII (Gre",) Cleve
Emiii(l//a h!lx/I)'; (Lo hm .) Hay & Mohle r
T emperature-depe nde nt gro wth ralC
Asln ;o1lt'lla formo sa Hass.
Na uiwla jJrllicu losa (Brc b. ex Klitz) Hilsc
Skrirtollrma t rop iCIWI Cleve

No.ofdollc:1

Varia tion amo ng

dones

2
5
2
2
2

110.

Re ference

Y
Y
Y
Y
Y

Braarud 195 I
Hay ward 1968
Brand 1984
Brand 1984
Brand 1984

Th allassiosira pSf Ile/olla/IU/OCl'anica compl ex

E. IlIlxlt')'i
E. Iwxle;j
Grph),rocapsa oCl'allica Kamptner
Proroct'llirum mica /I s Ehrenb.
C/OS/t'r;um rhrrllbrrgii Meneghin i ex Ralfs

2
10
2
5
6
14
44
73
19
28
33

Y
Y
Y
Y
Y
Y
Y
Y

Runner 193 7
Le win 1955
Hulburt and Cuillard 1968
Ha ywa rd 1968
Goldman and Carpenter 19 74
Bra nd et al. 198 1
Bra nd 198 1
Brand 1982
Bra nd 198 2
Brand 1985
Kasai an d Ichimura 1990

Tox icit y
GOII)'alllax lamarellsisb Lebour
G. III mart I/sis var. excavalab Braarud
G. Ilimlirt'llSis va r. lamarrllsisb Braa rud
G. Ilimart'llSisb Le bou r
PrologOlI),auiax lamarem is/ca lliliriiab compl ex
Gambt'rie/iseus loxieus Adachi & Fukuyo

3
4
5
35
24
17

Y
Y
Y
Y
Y
Y

Alam et al. 19 79
Schm id t and Loeblich 1979
Schmidt and Loeblich 19 79
Maranda et al. 1985
Ccmbe lla et a1. 1986
Bo mber et al. 1989

Vitamin requi rements and hete ro trophic capability

AmlJhora coffaeifo rmis Ag.
NiltSchia frll slulum (Klitz) Grun .
T. PSPlle/o llalia / oceall ica complex
P. Irico nlllllllll
Brl/prochra spillifera Hargraves & Guillard
Brllrrochra pol),morphll Hargraves & Guil1 ar d
Fragililirill pinllll /ll Ehr .

10
6
4
5
2
5
2

Y
Y
Y
Y
Y
Y

Lewin and Lewin 1960

Lewin and Le win 1960
G uillard 1968
Hayward 1968
Hargra ves and G uillard 197 4
Hargra ves and Guillar d 1974
Hargraves and Guill ard 1974

Nitrogen metabo lism

T. Pst'lldolilina/oceallica complex
F. pillna lll
Biddlliphill lIurila (Lyngb.) Breb. & Codey

3
2
2

Y
Y
Y

Car pe nter and Gu ill ard 19 71

Ca rpenter a nd C uill ard 19 71
Underhill 19 77

Sil icon metaboli sm

E. huxlt)j
Aformosa
T. pst'udOllUlili/ oCl'lIlIica complex

2
2
2

Y
Y

Eppley e l a I. 1969
Kilham 1975
Nelso n et al. 1976

Zinc-de pendent gr owth ra te

S. coslalmn

J e nse n et al. 197 4

pH-depende nt growth rate

S)'1wra pelrrslm ij complex

Weect a l. 199 1

3
2
II
6

Y
Y
Y
Y

Fisher ct a1. 19 73
Fisher el a1. 1973
Murph y and Bcla stock 198 0
Mu rph y and BclasLOck 198 0

6
4
2

N'
Y'

Shapir o Cl al. 1989

Shapir o et al. 1989
van Bl eijsw ijk et al. 199 1

Chemical composition; carbon part itioning

P. triconllllll1n
Chlit loarllS mut lleri Lem merman

2
10

Y
Y

T erry el al. 1983

J ohansen e t a\. 199 0

Luminescence
Gon)'lIlllllX txcavlllll (Braarud) Balech

10

Schmidt el al. 19 78

P. triconlll i um
Thalla SS;Qsira pS('IuloII(IIIa/oC('Qllica compl ex

Sensiti vity to po llutants

T. PSwdolllllla /ocea nica complex
F I}imlllili
T. Im u(/ollllllll/OCfllllicli complex
S. cosla/llIIl
Serologica l affin ity
E. hu:d r),i
Micromolllls pusilla (Butcher) Manton & Parke
E. hu:clt)'i

y,

N'

--

------------------~-

725

PI-IYTOI'LA N KTO N SPECI ES CONCE PT

TABLE 1.

Continued .
Characu:r
SI)Ccit.-s

Va ria tion among

No. of clonc~

Kefc:n:nce

clones

PhOloadapli vc parameters
S. cos/atulII

Ga llaghe r el al. 1984

Diel periodicityr
P. triCOn/UIIlIll

Terry

el

tt l. 1983

a Also seen in colony form and osmotic IOlerancc.

Now AIt'xalldr;um spp. (BaJech 1985).

( No heterotrophic ca pability observed in an y clone.
d Antisera to whole cells of o ne of the test d o nes: variation in strength of ant ige nic reac tio n o bserved among test clones.
~ Antisera to coccolith polysaccharide.
r In growth rate . chloroph yll sy nth esis. and biochemic il synth esis.
b

to planktonic populatio ns, considerable genetic diversity can be maintained very easil y. For species
that rarely reproduce sexuall y, selectio n during
asexua l generations wi ll increase hidde n gene tic
variability, and occasiona l recombination is required
to reestabish th e g reatest possible heritable ph enotypic variatio n (Lynch and Gabriel 1983).
Gallagher's work on populatio n genetic change in
Skeleloll ellla coslalwlI (Gallagher 1980, 1982) remains
the premier demonstration that changing environmental conditions are corre lated with changes in th e
genetic compositio n of a phytoplankton populatio n.
Recently, however, there have been additio nal effons to use protein e lectrophoresis to eva luate genetic diversity within populations . Electrophoretic
studies of toxic dinoAagellates show local populations to be much more genetica lly distinct from one
another on the west coast than o n the east coast of
North America (Cembella and Taylor 1986, Hayhome et al. 1989) .
Among freshwater phytoplankto n, there have
been two extensive e lectrophoretic studies of genetic polymorphism in natural populations. Soudek
and Robinson (1983) examined electrophoretic variability among strains of Asierionella!orlllosa fro m 32
different lakes or waterways. Whereas their study
clearly shows a high degree of variation among all
the clones, the autho rs also suggest that the low
genetic variabili(y observed amo ng isolates from the
same site reAects genetic homogeneity in local populations. However, since most si tes were sampled
only once, and since the median numbe r of clones
isolated from each site was less than three, Gallagher's work suggests that the sampling program was
inadequate to evaluate within-site genetic variability. Coesel and Menken (1988) examined genetic
variability within and among 17 populations of the
desmids Closterium ehrenbergii and C. moniliferulII. A
total of 278 clones were isolated from 17 populations in Holland and England, with a median o f mo re
than te n clones per site. This mo re statisticall y rigorous study showed very little genetic variation (but
some) within populatio ns. The Dutch and English
C. ehrenbergii strains were almost as distinct from

each other as the English C. ehrellbergii and the Dutch

C. moniliJerum strains.
T he development of oligonucleotide probes and
random amplified polymorphic DNA (RAPD) assays
for use in phytoplankton population genetics (cf.
Medlin 1991 , Deragon and Landry 1992, McCourt
and Helfgott 1992, companion minireview by Manhart and McCourt 1992) pro mises to make much
mo re detailed studies of population genetic dynamics in natural populations possible. Of particular interest will be comparisons of spatial and tempora l
scales of genetic homogeneity in systems that are
reiatively closed to immigration (e.g. lakes, te mporary ponds) and systems that are relatively open (e.g.
oceans, estuaries, streams).
For phytoplankton ecologists, interest in genetic
diversity within putative species is imponant primari ly because of the possible importance of populatio n genetic change as an adaptive respo nse to
Q)

I~r,--------------------------,

0"0

o>C

:J

0.0
<II

~ ~
~b
om
c

I ()()()

Q)O> ~

Q)

mo

100

>'0

~o
:~
~

o
-

Q)

;)'

--0---

to

I . IX
1.2X
2.0X
4.0X

Q)

:J
CT
~

FE
e
"-

10

12

Doubling time of initially rare genotype (days)

Flc. I . Time for initially rare. but eco logica lly adapted. geno type to become abundant whe n the more abundant genotypes
grow 10% (0) to 400 % (6) more slO\... ly tha n the adapted genotype. Conceptua lly. this cou ld be compared to clona l succession
in a cha ngi ng environment or to th e takeover ora population by
a strain with a new ravorable mutation. Model assumes asexua l
reproductio n (rrom Wood 1989).

726

A. M I C H EL L E WOOD AN D T ANYA LEAT H AM

g rowth rate. Amo ng the Gul f of Maine isolates. three

strains are affected much less by increased tempe rature than th e o th e r strains. T hese were amo ng the

1.2

1.J

a;

'"

slowest-g rowing strains at 22 0 C, and, because of

1.0

t he ir different r eacti on norm , th e differe nt ial in

0.9

grow th rate amo ng the clones is increased at the

higher te mperature. If these data were re presentative of the populatio ns in situ, theory wo uld predict

'"

0.8

that an increase in temper ature would cause th e

0.7

dramat ica ll y after several gene rat ions.

>
v

'"=
0~

re lative ab undance of these genotypes to dec rease

0.6

21

22

23

24

2S

26

27

Temperature

1.2

'"

1.1
1.0

.~

e=

0.9

0~

'"

0.8

0.7
0.6
21

22

2J

24

2l

2.

27

Temperature
FIG. 2. Geno type x environment interaction (G x E) among
clones of ProrocmlrWlllllicans Ehre nb. isolated from George's Bank
(lOp) and the Gulf of M aine (boLlom). Each line conneCtS the
growt h ra te or a given clone at 220 C \\'ith the growth rale of the
same clone at 260 C. Different lines represent different clones.
Signi ficant differences in the slope of the lines ind icate signi ficant
G x E, thal is, sign ificant ge netica ll y determined differences in
the effect of the increase in temperature on different clones. G x
E is more pronounced in the clo nes from the Gulf of Mai ne than
in the clones fro m George's Bank. Data from Brand ( 1985).

chang ing environme nts (cf. Wood 1988, Lynch et

al. 199 1). A character likely to be under selectio n
during t he current period of apparent globa l change
is the "reaction no rm " or respo nse fun ctio n characteristic of each genotype (cf. Parejko and Dodson
199 1. Gomulkiewicz and Kirkpatrick 1992). Differences in the respo nse of two genotypes to the same
e nvironmental change can be identified statistically
as genotype x enviro nment (G x E) interaction using analysis of variance tech niques (Gallag her and
Alberte 1985, Bell 1990) o r graphica lly (Fig. 2) as
sho wn fo r the dino fl agellate Prorocenl rwl/. micans. In
this las t instance, there is little G x E interac tio n.
T he di ffere nce in growth rate at 26 C and 22 C is
abo ut the same fo r all strains from George's Bank ,
e"ve n tho ugh there are differences in the absolute

Where Do We Co Jrom H ere?

Hopefull y, the preceding remarks provide convincing evidence for t he importance of chang ing the
status quo. T he data do not sUPPQrt the conti n ued
ass um ptio n that " clonal di ffe rences in mari ne phytoplank to n in general are believed to be rare" (J ensen et al. 19 74: 155). We suggest that several important steps be taken.
Exercise more caution when interpreting the ecological
significance oj dala obtained Jrom si.ngle strains oj particular taxa. Studies in volving many species, but with
o nly one strain per species, can be used effectively
to compare groups defined at higher taxo no mic levels, assumin g da ta from replicates are ava ilable to
evaluate within-strain variatio n. T his is the approach used by Keller ( 1989) to show that significant
d imeth yl sulfide production is confin ed to only a few
classes of ph ytoplankton and by Brand (199 1) to
show that oceanic phytop lankto n have lower iron
requirements for growth than coastal phytoplankton .
Begi'n to consider the strain designation an essential
part oj the nOlllenclature Jo, phytoplankton that aTe in
wlillre. When discussing the resul ts obtained with
o ne strain of a putati ve species, the strain designatio n, isolation information, and source of cultured
material sho uld always be provided in the tex t. If
the genus is clear ly identifiable, but the species-level
ide ntification has not been confirmed by someone
familiar with published descri ptions of type material, the strain designatio n ca n be substi tuted fo r the
specific epithet in both t he text and title ofthe paper.
If the strain has been fi rmly identified to species,
care should be take n in the tex t and tiLie to avo id
using the species name alone (w ith out strain designatio n) whe n discussing traits or properties that have
o nl y been stud ied in a particular strain . T hese are
all commo n practices in microbio logy and a matter
of required style in some micro bio logical j o urnals.
Since this is becomin g mo re common in the phytoplank to n literature (Kana and Glibert 198 7, Garcia-Pichel and Castenho lz 1990, 199 1), we suggest
that this concept of ide nti fica t ion be extended to
eukar yotic phytoplank to n and adopted mo re generally in our discipline . If mo rphologically similar
o r identica l phytoplank ton can be geneticall y and
ph ysiologically very di ffe rent, we are likely to have

PHYTOPLANKTON SPEC I ES CONCE PT

more realistic insights into the life of a phytoplankter if we begin to think of each clonal genotype as
a very distinct lineage, with differences from other
members of its "species" possibly as great as from
members of another "species" and , for some characters, greater simi larity to me mbers of another
"species" tha n of its own.
Identify the ecological significance of morphological traits
used to dislinguish a.mong species. Morphologica l variation is well known within putative phytoplankton
taxa and is often caused by environmental factors.
At some point, when genetically determined morphological variation among specimens is great
enough. putative species are split into multiple species groups (cf. Theriot 1987, 199 2, Rines and Hargraves 1990, Medlin 199 1, Young and Westbroek
1991). Much of this analysis seems irrelevent to many
phytoplankton ecologists, altho ugh seem ingly minor morpho logical features can play important functional roles (Medl in et al. 1986) and, therefore, affect an individual's fitness. Despite recent advances
in the study of phytoplankton sexual reproduction
(Mann 1984, 1987, 1988, Blackburn and Tyler 1987,
Destombe and Cern bella 1990, Faust 1992), ecologists wi ll probably be relying on morphologica l criteria to describe community structure for some time
to come. For this reason , it would be useful to know
when morphological criteria used to distinguish p hytoplankton species consistently inAuence Aux processes like sinking and grazi ng, optical properties
like scattering coefficient, or other ecologically important variables. For example, permanent attachments can be formed between adjacent cells in chains
of Skeletonellla cosla.lum (Grev.) Cleve but not among
cells in chains of the nearly morphologically identical S. pseudocosta.tum Medlin (Med lin 199 1). The
kind of studies we suggest would dete rmine whet her
or not this difference affects the likelih ood of chain
disintegration in the two species. Does grazing on
Skeletonema produce m OTe intact survivors in populations of S. pseudocoslalUln a nd more dissolved organic carbon from broken cells in S. costatwn? If so,
correct identification of Skelelonema. species in natural populations could provide anci llary information
abo ut the kinds of grazing and detrital pathways
operating in the ecosystem.
Identify ecologicall), important traits consistenil), correlated wilh the morphological features used to distinguish
among species or sub-species. II is also important to
identify ecologically important characters that are
uniquely correlated with the morphological characters used to distinguish amo ng phytoplankton species. For example, the 11tultiseries form of Nitzschia
pungens is identified by the characteristic number of
rows of poroids between the costae on t he valve
(Hasle 1965). However, all strains in the multis...ies
form also make the potent neurotoxin domoic acid,
and other forms of Nitzschia pungens apparently do
not (Bates et al. 1989, Fryxell et al. 1990). T his is
the kind of situation where accurate taxonomy, based

727

on traditional morphological criteria, provides extremely important information about ecosystem-lflVeI processes.
A.M. W. tha nk s R. R. L. Guillard for his willingness to r ide in a
Pinto. We also thank P. Kociolek. E. Therio t. and L. VanValen
for useful d iscuss io n, E. Theriot for access to unpubli shed work ,
T. Kibota for timely assistance . and N. Apelian, S. Brawley. R.
Casl.en hol z, R. Lande. L. Shapiro, and an anonymous r eviewer
for cri tica l review of the manuscript. This work was supponed
by DOE contract DE-FGD6-92ER61417.
(Castenholz): Genic variation, as measu red by enzyme
elec trophoreti c palterns, o ligonucleotide probes, RAPD assays,
and other modern methods, can now be used to characterize a
popu lation referred to as a "species" t hat was originally defined
by phenotypic characte rs. In you r opinions, how does this new
genic information on variabi lity affect spec ies limits and spec ies
concept, panicularly for these eukaryotic groups of phytoplankton that you have bee n discussing?

Qlles/ioll

AlIswn: There are two main wa ys. First , some of these methods

will permit the kind of work Jane Ga ll agher did to be repeated

more easily for other species. Her study (Ga llagher 1980, 1982)
te ll s us that a relativel y loca l population of one d iatom esse nti ally
goes through seasona l succession at th e clona l level; genetica ll y
different clones domi nate th e popu lation of SkelelOI/i'lI/a cos/alulI/
in Naraganseu Bay at different times of the year. It wou ld be
very va luable to know if this is representative of phytoplankton
popu lations genera ll y.
The second way these techniques are influencing species concepts is in the way reflected by Medlin's ( 199 1) paper o n S. cosla/IUII
and S. "mu/oros/alum. Here, molecu lar genet ic data is used with
traditio nal morphologi ca l cr iteria to establish a new species. The
ribosoma l RNA data presented in th is paper lend considerab le
credibi lity to her ident ification of a new species. Since the morphologica l data come from the examination of relatively few isolates, and therefore ver y few individual specim ens from nature,
this is a leve l o f credibility that wou ld have been hard to esta blish
from Ih e morphologica l data alon e.
(Manhart and McCourt): Should the typesofphytoplankton used by ecologists be given formal nomenclatural status?

QIU'Sl ioll

Answer: Presumabl y ecologists do not use generic or specific names

that do not have formal nomenclatural status. We're cenainly
nOt trying to rewrite the International Code of Nomenclature.
What we are really suggesting is that all discussions of a species'
phenotype take intraspecific ge netic va riation into account. If
o nl y one stra in of a species is used in a stud y, it is impossible to
extrapolate to the spec ies at large. In particular, it can not be
assumed that the physiological or biochem ica l phenotype of one
strain is shared by all other strains o r genotypes that share the
same morphology. We're also say ing that when allJolle (systematist, ge neti cist, ecologist, or what have you) uses cultured material , the strai n(s) should be carefull y identified. In something
of a more radical departure from standard approaches with eukaryotic algae. we wou ld also suggest that, for species where there
are ce rtain we ll-stud ied stra ins, the forma l species descript ion
might be amended to incl ude molecular, genetic, ph ysio logical,
and bioche mical features of strains t hat conform to the original
type description . This information could then be used to reso lve
the ta xo nomic pos itio n of morphologica l variants from type.

Alam. M. I. , Hsu. C. P. & Shimizu, Y. 1979 . Comparisons of

toxins in three isolates of Gonyaulax /amamlSis (Dinoph yceae).]. Ph),col. 15: 106- 10.
Bal ech , E. 1985. The genus Ale:mlldriulI! or GOI/Ja ulax of the
tamarensis group. 111 Anderson, D. M. , White , A. W. & Ba-

728

A. MICHELLE WOOD AND TANYA LEATHAM

den, D. G. I Eds. ) Toxic DillojlagelialfS. Elsevier, New York,

pp. 33-8.
Bates, S. S., Bird. S. J, de Freitas, A. S. W. , Foxall, R., Gi lgan,
M. , Hanio, L. A.,Johnson, G. R., McCulloch , A. W., Odense,
P. , Pocklington , R. , Quilliam , M. A., Sim, P. A., Smith, J
C., Subba Rao, D. V., Todd , E. C. D. , Waiter,J. A. & Wright ,
J. L. C. 1989. Pennate diatom Nitucllia /nmgfll s as the primary source of domoic acids, a toxin in shellfish from eastern
Prince Edward Island, Canada. Call)' Fish. Aqual. Sci. 46:
1203- 15.
Bell, G. 1990 . Th e ecology and genet ics of Chlamydolf/onas. I.
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