MARINE ECOLOGY PROGRESS SERIES

Vol. 161: 155 — 163, 1997 Pu blished Dece m ber 31

Mar Ecol Prog Ser

Nutrient control of estuarine macroalqae:

growth strategy and the balance between
nitrogen requirements and uptake
Morten Foldager Pedersen', Sens Borum
Fresh water-B iologica I Laboratory. University of Copenha gen, Hel sin 9 o rsgade 51, D K- 3400 H il lera d, Denmark

ABST R ACT: The a bility to sust a in g roivth at low ava ila bility of n it r ogen (N) v› as examine d in 6 species
of ma cr oalgae wit h different growth strategies by com pa riny s u bstrate depen den t gr o vth kinetics. The
N r‹ qu ire d to support opti mat growth and the N upta ke kinetics of 2 slow - g rowing algae, In cas i ‹ siCii -
losus and Codi um mo gilr, and 4 fast- g rowing species, CL‹s etoinorp/4 a /Jn um, Cls clo pmore seiico,
Cert m mm ru hrtim and Uh a la cI uca, we re expe rim en tafly determined in summer iv hen the a1q ae we re
N limited. The N required to su pport na a xinn um g ro vt h va ried 16 -Iold amo ng species, with Iast- g row -
ing a lg ae having the highest N d ma nds. The hig h N requirements of ep Item r‹i1 ml gae » ‹'re cause d by
up to 13-f old hig her g r o«Cth ra I r> a nd 2- to 3-f old hig her N co ntent at ma x inn u n i g r oxv th. Als o, the
Iast- qro wing speci es took up amm on ium and nitrate 4 to 6 tirn es las te r per unit of biorn ass th a ia slow - y
row - ing specics at both low and hig h s u bst rate concentrations, but the ratios of mv xirn u in ii ptako
to req uireuse nts we re lv rger among the sIovv -g rov ing all ae. Th us, the fast- g ro u ing species tended to
requ i re relatively hig her exte r na1 coned ntra tio ns of in or ga nic N to sa turate the ir g roxv t h. Under N
lim - ited conditions, all 6 ITU croa lgae vver e able to exploi t pulses of high con centrations of a mmoni um by
taking u p amm oni um at tra nsiently en h‹q n C£°d rates {i.e. s urge uptake). tJpta ke wes, however, o n ly
marg inally en h‹q need at low, ‹q nd natu ra lly occurring, concentrations of am rn on rum, suggesting tha t
su rge uptake is of min or eco logical inn porta nce. Our resul ts show that large, slow- growing m acroa1g ae
may be better able to meet I hi ir N requirements at low N ava tea b ilit y than fast-yro vin g species. Th is
is consistent wit h the commu.n observation that n utfie nt-poor coa sta I areas are dominated b\ sloPv-
t r o sv ing mv croalg ae rather tha n ephemer ml species, alt h on g h eplc e rn eral species have hi The r upta
ke ca pa cities.

KE Y \\'OR DS: Ma ri ne ma c r oalg ae Nitrogen req u ir eme nt N itr o9 en upto ke Competition

INTRODUCTION
of the dif Ierent plent types to total o utotrophic biomass
and prod uction is regulatect by several Iactors that
Nutrient avail a bility is an tmp or ta n t Iactor control-
influen ce g r o vth and loss processes (Sand-Jensen &
liig plant performance and species composition of
Borum 1991, D ua r te 1995). The distribution of macro-
pldnt communities in sh Allow coastal v‹qters (Bor u m
alqae a lony nutrient g radients is typically ch‹qr a cter-
1983, Orth fi Moore 1983, Tivilley et at. 1985, Ne un -
ized by slow-growing species in nutrient-poor regions
dorfer & Kemp 1993, Tay lor et al. 1995, Borum 1996)
or se‹qsons, while fast-qro ving, ephemeral species
These shallow wk ter plant communities are composed
dominate under nutrient-rich conditions (KButsky ct al
of a large number of species representing various
1986, Sf riso et at. 1987, Ménes g uen & Piriou 1995, Tay-
growth str‹q te gies and life forms, and the contribution
lor et at. 1995, Bor um & Sand -Ie nsen 1996)
The association between high nutrient avail a b ility
’ Present ad d ress: Depart meia t of Life Sciences and Chemistr y and increased dominance of e phemeral macr oaI qae
17.2, Ros kilde University I onter, Box 260, DK-4000 Ros -
suggests that fast-growing species requH e high n uti i.-
kilde, De mm ar k. E -mail: mls .' "virg i1. rue. dk
ent inputs to sustain growth, while large, sl ow-grow-
0 I nte r- Research 1997
Reesie of full ‹a rticle not permit.tecl
 13 b M ar Ecol P rog Se r 161: 156 — 163, 1997
ing t °cies are better ‹ i rl r ited to nut ri en t-poor cont i-
tie Ans. I ii s u} ›o i I r›f this id co , Pedersen ñ Boru.m ( 1596)
demon.str a ted that eph r merd1 ma croa lgae suffered
i o rn lim station during loner c r periocls of lot N avail-
ability in summer t hen did slow-growing species. The
observed va Fid tion in N limitation among alq ae of dif-
ferent growth s I rate gy could partly be explained by
species-specific differences in N requir emen Is and
storage capacity However, the wo rk also indict ted
that, compared to ephemeral species, slow-growing
ma cr oa lgae overe better able to .meet their N require -
ments by exploiting low exter n‹q1 N concentrO tions
(Pedei sen & Borum 1996)
E phemeral ma crOd lyae with thin thalli and. simple
morph ology t‹qke up N Ias ter per unit of biomass and,
further , have hiy her of finl ties for upta ke It low N con-
t un I rations th‹q.n large, st.ow-growing species (Wal-
lentin us 1584, Fujita 1985, Hein et Al. 1995) . Fast N up-
ta ke ‹ind h iqh affinity among ephemeral a lg ae has
Iormerly been used to imply that these alg be were well
suited to compete for nutrients It low availability of N
It has Also been hypothesized that ephemeral species
utilize short-term puJses of ammonium by taking it up
at transient.1y enhanced rates (i.e surge upt‹q ke),
thereby compensatin q for low up tCt ke during su bse-
quent periods of lOw N ava it iq bility (Fujita 1985). Surge
uptake has been documen ted for a lar ge n umber of
ma croalgae (e.g Fujita 1985, Thom.a s & Harrison 1987,
Harrison et Al. 1989, Pedersen 1994, McG lather y ct a1.
1996), and McG lathery et a1. ( 1996) sh o wed that the
length and rnag nitude of the surge upt‹q ke were in-
versely related to the size of intra cell star pools of am -
monium in the ep h emeral rnt croalg a CAo etomo pha
lie tim. If this mechanism is fi ge ner‹q1 feature among Ol-
yve, we expect all Algal species to be able to perform
surge uptake inde pendently of growth strategy
The adva.ntage of fast u pts ke at low availability of N
gained by ephemeral algae may, however, be offset if
the N requirem.ents of these species Are compar‹q bly
higher than the requirements for large, slow- g ro ving
species. The only way to e valuate species-specific dif-
feren ces in sensitivity to n utnent stress is to combine
the kinetics for N uptake And N dependent yro myth into
su bs trate depenclent g row th kinetics (Dugdale 1967)
and then comp Mr e the ability of dif her ent species to
sustain g rowth. at low substrate concentrations (Turpin
1988)
The objective of this st ud y was to test the hypothesis
that large, slow-growing macroalqae are better
adapted to grow under low N avai1‹q bility than fast-
grout rig, ephemeral species, because their N r equire-
ments and uptake of N are better bala nced at poten-
tially limiting N conce ntr‹qtions. We Addr essed this
question by compr ring subscrate depend ent growth ki-
netics, ruocl of ed from experimentall y determined kinet-
ics of N uptake and N reqri irements for pro vth among 6
species of macro‹q1gae with in herentl y different m•dxi-
mum g ro wth r‹q tes. \Ve also tested « h ether the pres-
ence and magnitude of surge up th ke dif fe red sig nifi-
cantly between fast- and slow -growing rna croalga e.
METHODS
\Vhole thalli of 6 macroalqal species with different
gi osvth strategies were collected in Roskilde Fjord,
Denmd rk, during ltte July and Aug us1 1991, iv hen the
algae were N limb tecl (Pedersen 1995, Pedersen & Borum
1996), Fucus vesicu7osus L. and Codi um Ii‘ocfile
(Suringar) Ha not. Lucks are slow-growing, perennial
macroalqae with thick and structurally complex thalli,
while Ulva toctuco L., Clodoph ore serico (Huds.) Lhtz ,
CA ae tom orDhd /in um I O. F M u11. ) Lh tZ. d FI Cl Uf° P6 D4 i
rubrum (Hu ds. ) C. Ag. are a nnua I species hayin g thin
thdlli and high maximum g ro vth rates. The a lyae were
rinsed of sediment, debris and epiph ytes and kept in
laborator y cultures for 5 to 7 d before beinq used for
ossessmen I of N requirements for growth or for uptake
experiments. The cultur e tanks contained f reshly col-
lected water from the sdmplin g site salinity = 17 "..
dissolved inorganic N (DIN) < 1 p M; dissolved inor-
ganic P (DIP) = 4 to 6 PM J and were kept o I constant
irradiance (300 Mmol m " s ’ PAR in a 16 h light: 8 h
dark cycle) and temper‹qtur e 15°C).
Nitr ogen dependent growth. Data for g ro vth of
Fu cus vesiculos us, Ulvo la ctuca, Ce armun1 r u b um,
Cha etomoryha he mm and Cla dophora serica as func-
tions of inter na1 N contents in the algal tissues overe
obtained from Pedersen & Borum ( 1996), while N
dependent grow th of Code urn ! ayile Eva s experimen-
tally determined in the present study, using the same
method os in Pedersen & Borum ( 1996) . All 6 species of
ma croa lqae over e grown in la born tory cultur es under
constant lit h t (300 mm of m s ' PAR in a 16 h light 8 h
dark cy cle) and temper‹qtur e (15°C). Nitrogen loadings
were ve ried to o btain specimens with a range of differ-
ent tissue N conce ntr‹qtions, Growth rates (p) overe
meastired as the increase in biOlTl Ass assuming expo-
nentidl growth:
where Bz and B are the dry weight biomass of a1g‹qe at
the beginning (F ) a nd at the end (T,) of the experi-
mental period. Observed growth rates were plotted
against tissue N concentr‹q tions (N) and the Droop
equation (Droop 1983} wks fitted to the data using non -
linear, least squares regression
p ,„Q1-(N /N)| (2)
where p „, is the ma x imuir grovvth ra te at infirnte
 Pede rse n & Borum: N utrie nt contr o1 of estu‹qrine macr oaly we
tissue N concentrations, N„ is the minimum tiss ue N
content needed to sustain growth (the subsistence N
quota), and N is the actud I tiss ue N co ncentration. The
ci‘itica1 N concentration (N ) needed to sustain gro wth
It maximum rates was estimated as the intercept
between the initial slope of the curve and the mlxi -
mum g roivtla rate (p, ,), whil‹ N requirements for
max imum gro wt h (N ,.q) were ‹ stimated as the prod uct
of the ma xim u m growth rate and critical N conce ntra-
tion (i.e p„„, x N ).
Uptake experiments. 1 0th ke of a namorn um may ini -
ti‹qlly be enha need and nitrate upta ke suppr essed,
when N depleted rig be are exposed to sudden pu1ses
of in orqa nic N McGlathe ry et Al. 1996) , To discern the
different phases of N uptake, we measured upIN ke
rates of annua oni u m and nitrate by several time-course
depletion expe riments, las ting 4 to 10 h each. The
depletion of substrate due to upta ke wks measured
over different time intervals and substrate concentra -
tions in each experiment, so that Any transient pfiases
‹q ppearing duriny the initial stage of the experiments
could be separated from the more constant u pts ke
rates occur rin q subseq uently (referred to as 'assimila-
tion rates’, for details see Pedersen 1994, McGlo thery et
al. 1996)
The upta ke experime nts vere ca rried out in tra nslu
cent plexigl As cham hers conta ininy 2.1 of medrum and
1
kept under constant ir radian ce (400 Mmol m s PAR)
And temperature (15°C). Water cir culation was gener-
ated by su but e rsible pumps {6 I min ' ) . Filtere d (Whit-
man GF/C) sea wk tOr wks enriched with N b/ ddding
either NH4Cl or Na NOT from stock solutions. The
upta ke expe riments were ce rried out with at least
6 different starting concentrations of N, ranging f rone
3.5 to 85 pM a mm on rum or Irorn 3.5 to 4.5 p M nitrate.
Algal material (0.1 to 0.7 g DCV) was fixed on d N itex
mesh and s u bmersed in the mediulTl ‹q t time = 0 Top-
locate wk ter siqmp leS (5 ml) were collecte d every 15 min
during the Iirs t 90 min and su bseq uen thy every 30 min
until all inorganic N had been depleted from the
medi urn (within 240 to 600 min). Ammonium was ina-
m ediately analyzed using the phenol-hypochlorite
method (Solor zano 1969), while nitrate samples were
frozen for IN ter analysis on an Alp h iq Chem° Auto Ana-
lyzer. Algal dry weigh t was determined Of ter drying to
constant weigh t at 90°C for 4.8 h
Uptake r‹q tes | U (pmol g ' DW h ’)] were calculated
for each time inter vd1 during the depletion accord in g
to:
V = jS, x vol,) -(S,x vol,)/(ix B) (3)
where S and St are the su bstrate concentrations and
vo1 and vol, the volumes bef ore d nd after a sampling
period t›, and B is Algal dry iv eig h I biorn ass Uptake
rates (V) over e plotted against the mean su bstrote con-
137
centration (N) for each time inter v‹q1, .q nd the Michaelis-
Menten fun ction was fitted to the data using non -
linear, least squares regression
where \ ., „, is the maximu m u pta ke i ate and N„ the half-
saturdtion constant for unto ke. The ini t)dl Slope of the U
versus S curve, equal to U„„„/K„„ was calculd ted and used
As In index of N uptake a f fi n it y at low sub- strate
concentrd tions (Healy 1980)
Estimation of substrate dependent growth. The
association betwee n growth rate and the conce ntrd tion
of ammonium or n it rate in the water was estimated for
each spcci es using th e uptake kinetics (Eq. 4) for eithe r
a mmonium (the ‘assimilati on' kinetics) or nitrate and the
relations hip between qroivth rate a nd tissue N con - tent
(Ed. 2), assuming steady sta te co editions. The reI‹q
tion betwee n growth rate and substrate concentra- tion
under steady state conditions can be described by a
Monod type equation
(3)
where p‘ , is the ma xirnum growth rate under steady-
state conditions, K„ is the half-SP turation constant for
g row th, ctnd S’ is the stead y-state substr‹q te conce ntra -
tion. Ects (2) & (4) can be combined And solved for
N„ which is then su bstituted into Eq. {2) to estimate the
constants q‘„„ and K , of Eq. (5). Turpin ( 1988) provide
d detailed description for the derivation of the equ‹q -
tions def in my q‘„„ and K„.
and
where \ „„, K„, u„„„ and Nt, are defined as described
for Eqs. 12) & (4). Both q’q„ and K, o I Eq (5) we re esti-
mated from measured values ot U„,.i x' na' And N¿,
0„ y
and used to model growth rates at typi ca l in site con-
centrations of ‹q mmonium and wit ra te, respectively.
The compute tion was performed Iss urn ing no effects
of stored N in the algae.
Error estimation. The substrate dependent growth
rate (p‘) and the half-SP t eration constant for gro vth
(K,) were both c‹qlC ul ate d as combinfi tion of several
individual va ri a bles, each measured wit h ther r own
error. The bootstra p procedure (Ef ron & Tibs hirani
1986) was, ther ef ore, applied to estinâ‹q te medns and
confidence limits for the combs ned results. All the indi-
vidual variables were assumed to be normally distrib-
uted with observed means a nd standard deviations. Bias-
adjusted bootstrapped mean values (x , , ) of q’q„ and
K, were computed from the individual vari- ables (E qs.
6 & 7) using Monte Carl o resanipling ( 100 mean
values were estimated), ‹qcco rding to Meyer
158 Mar Eco1 Prog Ser 1 61 155 — 163, 1597

et a1, ( 1586) . Bias - adjusted 9.5 " confident ‹• limits wei e 0.12
Co dium fra gile
fine11 computed from the 2.5 and 97.5 " per centiles

(d"')
of the bo o tstrappe d data sets Iollowing the procedure
0.08
presented b› Jeyer et at. 1986)

Gro w t h r a t e
RES ULTS

Nitrogen requirements
Maximum growth rates (qp„}, subsistence quotas
(N ) And critical tissue N concentrations (Nt) obtained
in the laborn tory experiments (this study and Pedersen
& Borum 1996) are summ‹qrized in Table 1. In General,
‹growth rates increased as functions of tissue N concen -
tration as exemplified by the r elationship between
growth and tissue N in Codi mm /rayiJe (Fig. 1). The
ma ximum growth rate at infinite tissue N concentra - tion
varied 13-Iold among species and was lowest for Fu
cus vesicufos us and C. /rayi?e (0.039 a nd 0.088 d‘ ' ) and
highest among the 4 ephemeral species (0.2 l8 to
0.313 d ' : Table 1).
The subsistence quota (N, ) ranged from 0.38 % N
of DW in Chr etomorpll o lin um to 1.02 % of DW in
Ceromium rub um, with the remaining values being
clustered around 0.6% N of D\V. The critical tissue N
0.00
0 1 2 3
Tissue N (¥ of DW)
Fig. 1 €“odd nut fragile. Relations hip between g r oivth rite and
tissue N concentration as deteriti rued in laboratory experi-
ments
concentration (Nt) ranged from 1.15 % N of DW in C. lin
non to 3.1 *ñ N of D\V in C. ru bran ITable 11. Bet h
Nq and Np tended to increase with incree siny maxi-
mum yrowth rate of the alyal species, but the pat-
terns were not consistent since Nq and Nt were low
for the relati vely fast-growing C. Min mm. The amount
of N required to sustain maximum algal growth var-
ied 16-fold, from 48 pmol N g ' D W d ' in Mucus
vesiculosus to 795 Mmol N q ' DW d*‘ in Evo Jocfuca
(Table 1)

Table 1 Maxim um growth rates (pq„), su bsistence quotas (Np), critical tissue N concentrations (N¿) and estimated N req uire-
ments for growth under lv borator y conditions in 6 spec.i es ot ma croalgae , Estimates ot q,. and N„ overe obtained by non-linear
least squares regression. Numbers are mean values wi th 95 % confidence inter va1s in paren theses. Data for at I algae except for
Code um fragile are from Pedersen R Borum ( 1996}

Nq ("ñ N of DW) N, (”. of DW) (pmol N g— ’ DCV d-

’j
focus esiculosus 0,039 (0.003 — 0.127) 055(03â-064) 1 71 (—1.48 4.38) 4 8 (—95 — 219)
Codlurn fragile 0.083 {0.072 — 0.094) 012(040-064) 1.58 (0.45 2.61) 96 (25 — T 69)
Chr etonl orpha lin um 0. 218 (0.176 — 0.260) 038(037-039) 115 {0.96 138) t79 (I 43 — 229j
Cladophord serico 0.251 {0.189 — 0.313) 0.68 (0.57 — 0 79) 2 05 (0.93 33l 364 (T 57 — 607)
Geranium rubrtirn 0.223 (0.176 - 0.270) 1. 02 (0. 97 — 1.08) 3I 0 2 /9 364) 4 93 (379 — 614 j
Ulva 1s ctuco 0 513 {0.479 - 0.b47) 0.71 (0.66 0.76) 2 17 (L33 - 2.93) 795 (595 — 987)

Ta ble 2. Attr ogen u ptake kinetics. The kinetic parami'ters \ ’ , (pmol N g DCV h 1 ), Nq { UI) and the affinity for rlpta ke at In v
concentrations (\ , ’K, 1 Ir aly 1980) for surge uptaki of ammonium (surye; I'“ i uptake and assir i1‹ition of ammonium (\ )
anct uptake of nitrate (I ) for 6 species of m acroa lyae Parameter estim.ates were o Stained by non -1ine‹M least squares regression.
Numbers are mean v d lues + 55 '?• conf idence inte r vals The coefficient of determination (r"} is also give n; all regression s vere
hiyhly significa nt (p < 0.001)

S urge uptake of ammonium (U’) Assimilation of a mmoni um (¥ j Nitrate uptake t \' )

\ Kg \ „,.,IK„ r2 „¥ , K„ \’ 'Np r'

Fu cus yesic ufos as 4 1 + 7 21 + 10 2.0 0 99 22 + J 14 + ’7 1.6 0.‘7 8+1 11 + 5 0.7 0.91

Codi um fragile 81 + IN 25 * 12 3.3 0.94 44+5 12t 3 3.8 0.93 9*1 5+1 2.0 0.92
Cho etom oipho lin um 132 + 29 I. 3 * 12 10. 2 0.89 47*5 3z1 13. 6 0.89 30 i 5 3i1 9.9 0.95
Cfc dophore serico 122 * 33 i 3 z 10 9.8 0.94 43 z 6 5z3 9. 4 0.87 17 * 2 5+2 3.5 0.84
Cert ml um rubrum 271 z 81 29 z 21 9.4 O.S5 59 6 5+2 12. 3 0 89 —
UJ v6 J6 ct c 240 * 61 21 + 16 11 3 0 88 72 -r 6 6›2 12. 4 0 95 20 + 8 5z2 4.5 0 86
 Pedersen & Borum: Nutrient control of estuarine ma croalgae 1â9

Uptake rates 250

200
The uptake o1 Ammonium xvds initially
enhanced w hen N depleted algae overe 190
suddenly exposed to ammonium. Uptake 100
rates a re, therefore, rep resente d by 2 sets

Up take r a t e ( / Jmo I N1 gDW h"')

50
of u ptake kinetics: (1) one representing
transiently en henced uptake (i.e. surge
u th ke), medsu i ed d uring the fi rst 15 min
after exposure to ammonium, and (2) one 200
representing the uptake rates o bt lined 150
later thin 120 min ‹qfte r exposure (here
denoted As the 'assimilation rate' ; see Ped- 100
ersen 1994, McG lather y et at. 1996). The 50
surge uptake prob‹q bly represents a co m-
bin‹q tion of adsorption of ions onto the 0
plant surfsce and the absorption of ions
20
into the plant tissue, while assimi1‹q tion 0
uptake most li kely represents the rate of
amino acid synthesis within the algae 150
(McG lather y et al 1996). The rate of surge 10D
uptake increased and tended to saturate
with incr e‹qsing substrate concentration 50
a mong All the alg a1 species examined 0
(Fiy. 2), b ut the kinetic cons t‹q nts exhibited
1‹qrge species-s pecific variations {Table 2).
Fuc us ve sic ulos us

0 20 40 60 80

Conce ntra tion of

Cla dophora s erica

C er a mium r u brum
 0 20 40 60 80 1 00

ammonium (PM)

The ma xim u m i ate of s urqe uptake (V‘" „) Fig. 2. Upta ke rates of ammoni um as a I u n ction of substrate concentration .
ranged 6-fold, from 41 pmol N g DW h ’ Surge upto kc (o) was measured o eI the initial 15 min atter exposu re to
in Fa cus vest culos us to 271 pmol N q ' DW ammonium, i^ hil e assimilation rates (o) were measured lat er th an 120 min
i after th ‹ experiments we re ini tia ted
h in Cera ml um rubr um. The half-satura-
tion constant (K„) ran qed from 13 pM in
Cla dophore series to 29 pM in C. rubrum, but all ni 1‹qtion during the surge phase at high ammonium con -
values were characterized by large errors, making inter- centrations. The N gained during the surge phase
specific dif ferences non-significant at the 5 % ranged f rom 9.6 pmol N q ' D\V in Mucus vesic ufosus
level. The V„„.Kg ratios for ammonium ti.e. the a I fin- to
ite fOr ‹q mm on rum u pt‹q ke It low su bs tr‹q te concentr d - 106.1 pmol q* ' DW in Cessmi um ru Drum lTa ble 31, a
tions) we re higher among the ephemer‹q1 alga e than for nd the ephemeral species a ecu mutated in ge neral more
slow - gro win q species (9 to 11 vs 2 to 3; Table 2) N per unit of biomass than the slow- growing algae, The
The assimilation rate of a mmoni um ( U"’) also higher gain by e phemeral ‹qlg be Eva S, however, bal-
increased ‹q nd satur‹q ted wit h increasing substrate con- anced by highe r N requirements for growth, a nd the N
centration, but rates vere yenerall y 2- to 5-fold lower pool accumulated during the surge phase could sup-
thin surg e u pta ke rates at high substrate concentra -
tions (Fig 2) . Md X11T1 tllTl ossilTltlation rates (V“"„„)
Ta ble 3. Role of surge uptake. Am on nt of a mm onium taken
ranged from 2 2 q mol N g ' DW h ’ in Fucus vesicuJo- up in excess of assimil ation upta ke during th e sir rye phase (N
sus to 7 2 pmol N g ’ DW h ' in Ulva 1s ct uCH (Table 2). gain), and the pe riod of groivth ut maxim um rates the t can be
The half-saturation constants for assimilation were also s uppor ted by the ammonium ta ken u p d urin9 the surge
lower than those for surge uptake, so the U„„: Kg ratios phdse to r b different species of macroalga e
for surge And assimilation uptake remained rou qhly Ngan Growth period
the same. Identical Uq„: Nq ratios of surge and assimi- pmolNg (h)
'DW)
lation uptake indicate that the rates of ammonium 46
uptake overe not initially enhanced at low subs tr‹q te . 4.8
concentrations. Chr etomorpho 11’n 6 6 0
We evaluated the potential gain of N achieved by the uin Cha dophora t8.7 2.9
serice Cerami um r 42.6
algae during surqe uptake, by comparing the amounts ?9.3
ubrum UI va 1sc’t
of N that could be accumulate d in excess of N assimi- uco T 06. I
840
 160 Mar Ecol Prog Set 161. 155 — 1 63, 1997

40
exposure to n i trite, Thc u p ta ke rates of ni-
Fu c u s v e si c ulo s u s
30 trate vere, like I hose of anim onium, h per-
bolically related to substrate conc‹cn.bra tion
20 but lower than the upta ke rates of ammonium
{To ble 2). As for cmm onium, maximum
10 uptake r‹a tes of nitrate were re- lated to
Upt ake r a t e ( jumol g"’ DW h"' )

species -specific differences in max- imum g

rowth rate, And maxim um upta ke rates for
Cla dophora s erica Ch a etom o pha li n nut, U1s'a to c- t uco,
30 end Cla dopho a serf cv overe 3 - to 4 - fold
higher thin those for Code rim frayile and
20
Fu cue vesiculo sus. The half-satur‹q tion constd
n ts varied 4 -f Old am on g species, and the
10
ratio of I i ' in tende d to be hiq hes t
0 among the fast-growing a1yee (Table 2)
The ratio between U„„ and the a.mount
C e ra mium rub r um
of N required to sustain maximum growth
30
vameet s sts fur.!ia 11;' emo*.p sp ci s. A!l
20 macroalqae could potentia fly take up
N o t d e t e r min e d ‹q mm onium and nitrite faster than needed
10 for max imum gro vth, given thCt I SU bstrd te
concentration.s were hich enon yh . hi i t t h
0 slow - g rowiny species had ratios of \’
0 10 20 30
0 10 20 30 40 N requirement the I were approximately
Conc en tr a t ion 2 -fold higher than for ephe rnerd1 species,
of nit r a t e (jJM)
sugqes ting that slow-growing speci es have
Fig. 3. Uptake re tes of nitr‹q tC- as a function of su bstro te c on centre tion
‹q higher capacity for taking up N in excess
Uptake rates (o1 vere measured I a ter than 60 min after the experiments
were ink tinted to avoid the initia I phase of su ppr esse d ni trate uptake of inn me did te demands for groivth

port growth for approximately the same periOd of time Balance between N availability and algal growth
for all species (range: from 2.6 to 5.7 h; Ta ble 3)
Uptake of nif rate was initia lly suppressed and was, The estimated maximum growth riq tes (q‘ ,; Table 4)
therefore, taken as the retes measured af ter the initial were sligh tly lower than the m.q x im um growth ra tes
lkg p hdse had ceased, usually within 15 to 60 min after estimated from the labOl d tOry experiments (p

Table 4 Car oivth kine tics. Pr edicted va Sues or maxim um gro wtb rates (p’„„„), hal I-sa tn re tion constants for q r ow th (K I and of the
su bstrate concentrations needed to so turat' 9 rowth I.S‘ „,) under str ady state conditions in 6 dif ter ent species of mac roalqa e with
either ammonium or nitrate as inorganic N so ur ce. umbers a re bi‹is -a dj u sted bootstra p mea ns with US '?. per centric-0 ased con-
fidence intervals in parenth escs

Species bitrate
p’(d ')(q%l S’. (lñ])

Fucus vesicuJosus 0040 0.29 2.66 U.038 0 81 7.32

(0.032-O05/ (074-111) (-658-1368) (0.03 T — 0.048) (0.02 1.77] (0.18 — 15.94)
0.083 0.25 2.22 0.074 0.3-/ 5. I I
(0.OF T — 0.093) (0.00 — 0.38) (0.03 — 5.19) 0 055 — 0.086) (0.36 — 0.92) (3.24 — 8.3 I )
Cha e I omorpha Jin um 0.142 0.11 1.00 0.139 D. 1 S I lS
(0. 13S — 0 150] (0 00 — 0. 21 ) (0.01 — 1.91 ) (0 134 — 0.148) (0.OU 0.28) (0.0*J 2. 4 9)
0. 208 0.36 3. 28 0.188 0.83 ? 45
(0.1 84 — 0231 ) {0.11 — O. 71) (0.99 — b.4 0) (0. 1 J7 — 7‹J l (- 0.02 — 1 7 7) (-0.19 — 13.97 j
0.
Cera mium ru brum 0. 299 0.63 5.65
(0.284 — 0.317) (0. 07 — 1 26) (0.67 1 1 31)
0.452 0. 75 6.7 1 0.34S 1.4 5 1.3. 02
(0.4 22 — 0. 4 (0.52 — 1. 10) (4.61 — 9.90) (0.322 — 0 373) (0.87 — 2.10) (7. b4 - 18.89)
82)
 Pedersenm Bo rum: N utrie n I co ntrol of cs In a rin n4 o cr only ac
Table 1). Mean values of the half-satu ra tion constant
for g ro myth K„ with dmmoni um as the N source ringed
from 0.11, 0. 25, and 0.29 pM in Cha etomo pha hnum,
bolt tiir !ra Qlle, and Fu cus vesicufos us, i espectively,
to 0.3b, 0.63, and 0.75 p M in Old doph ore series,
Cement inut ru hi cm, and UI ve 1s ctu cv, respectivel} .
K„ ranged from 0.13 pM in Cha etomor pho lin
um to
1.45 p M in Upvc Incl ace when nitrate was the N source
Hence, K, ten dcd to mcrease youth in ci easing maxi -
m um a1y Al growth rd te, b u t the mean values have
qu ite wide confidence limits (Table 4) been use K„ wcs
estimated f rona several in depende nt Ia ctor s (Eq. 7)
each measured ith its ow n er ror. The a bility to con-
vert availa ble D IN in the wate r into g ro wth through
uptoke (represented by the p‘ :k„ ratio) was highest
among the ephe me rat algae, but the predicted co ncen -
tr‹q tions of amm onium and nitrite needed to s‹q tui a te
algal g rowth were higher for U. Ja ctuca, C. r ubr mm and
C. serlca tha n for C. tin um, C. bra file o n 3 F. vesicuJos as
(!S“, , To ble 4). These results sug gest that ephemeral
algae are less tolerant of low concentrations of in-
organic N.
DISCUSSION
The ecolog icdl success of large, slow-growing
md c row lga e in nutrient-poor coas tfi1 Mr eas could seem
porddoxical because the relatively low ratios of surfo ce
area to volume (SA: V) of these species rna y confer less
'efficient' nutrient uptake. Indeed, d bsolute rates of N
upta ke Ore higher per unit of biomass and time for thin
than for thick algae (Rosenberg & Ram us 1984, Hein ct
d1. 1995, this study). When rates Are ex pressed per unit
of surface ‹q rea, however, nutrient u ptoke 'efficiency'
of thick a lgae te nds to be hug h er than for thin species
(Hein et at. 1995) . The results p resentecl here s t ron qly
support the suggestion th dt potenti at competitive suc-
cess ‹q mon9 algal species mv st be evaluated fr oiaa the
Ability of their N u pts ke i ‹ites to meet the requii eme nts
for y roivth {D ugd‹qle 1967, Turpin 1988) . Such discus-
sions of size-rel‹qted algal competition v ithin commu-
i4ltiCS Of micro - or macro‹q1go e are of ten confused by
inc ppropria te comparison of the ef f icien cy of nutrient
upIa ke a lone
The present study classifies the thick, sIo v - growing
mac roalgae as being It leo st as efficient As the thin,
Iast-9 r owing species in exploiting firm ted N resources
to meet their requirements. The ve riable N require-
men ts among species were caused prima i ily by differ-
ences in qrow th rates And second‹qrily by differences in
ci‘it1Ca1 N concentrations. Species-specific maximum
growth rites obtained in the laboratory experiments
voried 13-f old and resemble d rates measui ed for the
st me species in st tu durin y summer (Pedersen &
161
Borum 199b). The observed variations in ma xim um
growth i a tes iv ith ch a nging alg d1 morp hology (i.e thin
vs thick I hall us) agreed with the ge neral pattern to und
among algae of different size and I ha llus comp lex ity
te.q. Littles & Wittier 1980, Nielse n R S And -Jensen
1990)
The ex pen me ntally O b thine d subsistence N qu otas
(N ) dFld critiCcll tissue N concen t rations (N ) also
ten ded to cha nqe with algal mod pholOy Mild max i -
na um q r o th rate. Subsistence quotas a nd ci iti cal tis-
sue L' course ntro tions resembled da to from the litera-
ture (e.q. i-Ianisak 197.9, Gordon e t al. 1981 , Rosen leer q
et a1. 1984, Fun ita et al. 198S, Lave r y & McComb 1991)
\\*ith the exception of Cho etone o pha /ir mm, ephem-
eral species had slig h fly higher subsistence cell q not as
and critical N conce ntrfi tions than slow - growing spe-
cies and, hence, species -specific N requir ements to
support maximum growth became several-fold larger
among fast- than slow- gro vin g m‹qcroalgae This sug-
9 ests that f ast- growing species Iace d higher risk of N
limitation when exposed to low N concen f rati ons, un-
less their requirem ents are met by proportions lly Ias ter
N LU td ke
The uptake experiments confir med that the ephe-
rner al o1y ae were so pertor to the sl ow- growing species
in te rms of nu trient up la ke per unit of I iomoss end
time, The ma x im um rate of surge d nd assimilation
uptake of a mmonium, the maximu m uptake rate of
nitrate and the affinity for both ammonium And nitrate
were several-fold hiyher in the 4 ep hemerdl macroal-
gae than in the 2 slow-gro wing species. Such system-
atic vari‹qtions in uptake kinetics are related to differ-
ences in alg a1 mor pholog y as t hill ITU cr oalg ae take up
nutrients Ias ter per unit of biomass than larger species
with thick thalli (Rosen Berg ct ml 1984, Walle ntin us
1984, Fujita 1985, Hein et at. 1995). This is because the
S ITIa11 species have h igh er r elf tive su rfaCe Mr eas (i.e.
SA: V) than large, thick my ae, o nd upta ke rates are pri -
marily scaled to the exposed surface a rea relative to
volu me or biomass (Rosen berg R Ram us 1984, 1-fern et
at t993)
The 6 alga1 species all took up o.mmonium at tran-
siently enhd nced re tes when sudden ly exposed to high
Ammonium concentrate ons a fte r d ]OC fiOd of N deple-
tion. Surge u ptok e of a mm oni um seems to be con-
ti oiled by srun11 pools of intro cel1u la r amm onium,
which may exe r t a neg ative feed back control on
uptake rates as the pools are filled (Pederse n 1994,
McGlather y et a1. 1996 ) . I nity al upta ke rates of dmmo-
nium are, the ref ore, enhanced for a sh ort period of
time only, ther eafter rates are reduced to ir ore con-
stant levels li kely contr olled by the re tes of amino acid
synthesis tassimi1‹q tion). The presen ce of surge uptake
has been sug gested to constitute a competitive advan-
tage to ephemeral micro- and macr oa lgae li ving un der
 162 Mar Ecol Prog Ser 1 b I : 15—5 163, 1997

low, but fl uctu‹q ting, N availabilit› (e. g. Conw a y & Har-

rison 1977, Fujita 1985) . Our data show, hosveve r,
that surg e upIa ke is not a special fe.qtur e exclusive for
ephemeral species
The ph Use of surye upta ke was short—lived, typicall)
1.as ting for 60 to 120 fTIin, And provided On extra uptake
and accumulation of N in the range of 9 to 106 Mmol N
g ’ DCV. This short-term N storage could, howev er,
only support rn axim um growth for 3 to 6 h ind epen-
dently of dillere nces in intrinsic maximum growth
rates among species. The Adv qntage of faster surge up-
take kmo ng ephemeral alg‹qe was offset by their higher
N requirements. Furthermore, shOrt-term stOrag e of N
gained through surge uptake could only be realized at
high DIN concentrations (> 10 pM) rarely experienced
under fie Id conditions. At low, and more natural, con-
centrations (0 to 10 pM DIN in Ros kilde Fjord; Peder- sen
R Borum 1996) , no significant differences ap -
peared between rates of surge and assimi1‹qtion u ptake
as reffected by the similar Vz,, K„ ratios. Hence, surge
u ptake may not be as ecoloqiciqlly important for algal
N acquisition As f or merly suggested in the literatur e.
Model in g steady-state g roivth, by combining the
kinetics I or growth and N uptake of each Al gal species,
showed that the differences in the ability amon g spe -
cies to sus td in g rowth As a function of exter naI N con-
centrations were small. The half-saturation const‹q nts
for growth were gen erally low (K„ = 0.11 to 0.75 p M for
ammonium, 0. 13 to 1.45 p M for rntrate but comparable
to experimentally determined values for other species
of macroalqae (De Boer et al. 1978, Gordon et Al. 1981,
Rose nberg et al. 1984 ) . The low Kg va lues sug yest that
all the species examined are well suited to sustain high
growth rates at low D IN concentr‹q tions. The ratio
between the half-saturation constants for growth and
upta ke (K,/Kq) cm been used As an index of sensitivity
to nutrient stress; th e lower N, is relative to K„, the
higher is the capacity for ‹q given species to grow under
low exte rna 1 nutrient concentr‹qtions beea u se of vari-
abl e cell quota (see Turpin 1988 for details). The ratio
ot K,: K„ for a mmoni um was su bs tantially I ower for
Fu cue vesiculos us, Code um mo gile and Shae tomorpho
lin um (0.022 to 0.033) tha n io I Cld do phore series,
Cerami um rri hmm and Ulva In ct oco 0.076 to 0. J. 27),
And the 3 former species should, therefore, be better
suited to sustain growth ‹q t low exter naI N con centra-
tions than th e latter Accor ding to o ur calculations of
substr‹q te depend ent growth, the algal species would
become N limited in the following sequence as the
OVdllabihty of DIN decreases: U. Inctu co, C. re hmm, C.
serica, F. vesicufos us, C. bra gile, and finally C. lie uai
Hence, our data suggest th dt e phemeral algae, with
the exception of C. Jin mm, will experience N limitation
at higher DIN concentric tions than slow-growing spe-
cies, mak inq them more sensitive to N stress
Overall, the present stud \’ has demonsti ated that slow-
growing macroalgae chin e xploit inimedia te N re- sources
through uptake as ef ficientls cfs, or even more efficiently
th‹q n, fast-growing algae The slow-gi owing species have,
in addition, a higher capacity for utilizing inter na1 N stores
to cover their re quir em ents for growth at low exter na1
N availa bility tha n the e phem- eral ma crOO lg Oe or
phytoplankton (Pedersen & Borum 1996). In com bi
rliqtion, these Abilities suggest that plants with inherently
low maximum growth r.q tes are better able to sustain
maximum (i.e. non-nutrient lim - ited) gro vth than
ephemeral species in areas or sea- sons of low N a
Valliqbility. This is consistent with the observed differences
in the temporal extent of N limi- tation observed among
algae of different growth strat- egy in Ros kilde Fjord
(Peder se n & Borum 1996) , where ephemeral ma croalgae
exhibited N limited growth for longer periods in sum mo r I
h or st oiv- y row in-y species
Since species -specific rates of biomass losses are
almost directly Selled to intrinsic plant growth rates
Cebrian & Dua rte 1994, D uar te 1995), we assume that
the algae best able to sustain maximum growth rates
under conditions of N limitation will have the competi-
tive Odvant‹qge to become dominant in mixed alg Al
communities. At high and non-limiting N availability,
ephemera 1 algae will be favored simply beea use of
their high growth rates and will flourish It the expense
of more slow-growing species (Sand-Jensen & Borum
1991, D uarte 1995). At low and potenti.q1l/ limiting N
availability, the slow-growing species should be
favored, while fast-gro wing species struggle to bal-
ance the continuously high biomass losses. These sce-
n‹qrios ay ree with the characteristic changes in plant
communities described from a broad v‹qriety of natural
and d£tificial coastal systems suffering from eutrophi-
cation (Borum 1983, Orth & Nlo ore 1983, Ka utsk y et at.
1986, Sf riso et aI, 1987, Neundor ter & Kemp 1993,
Ménesg uen & Pin ou 1995, Tiqylor et at. 1995, Boro.m &
Sand-Jensen 1996) , A ccordingly, we have provided a
plausible, I unctiona I explanation for the effect of nuts-
ents on the biqlan ce ‹q mong algae of different g row th
strategy in coas ta1 waters. Although we have prim+qril y
compar ed growth and nutrient kinetics of marine
macroa lgae, we expect that the functional explan‹q tion
will be valid for size -rem ted competition among a lgfi1
species within micro - and m‹qcroalya l communities in
general,
Ackno vledyem en ts. This study was supported by a HAV-90
grant from the Da nish National Ayenr} of En vironmental
Protection. We than k K. Sa nd -Jensen, W. M. Kemp, and 3
anonymoi is ref o rees for valu a ble comments, and Bir g it
Kjaller for technical s u ppor t d un ng the experiments.
Contribution #1053 trom the Freshwater-Biological La borator
y, University of Copcnh ag en
 Ped e rsen & Borum: Nutrient contr ct of es th arine macroalgae
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