European Journal of Phycology

ISSN: 0967-0262 (Print) 1469-4433 (Online) Journal homepage: http://www.tandfonline.com/loi/tejp20

Minimum spectral light requirements and

maximum light levels for long-term germling
growth of several red algae from different water
depths and a green alga

Petra Leukart & Klaus Lüning

To cite this article: Petra Leukart & Klaus Lüning (1994) Minimum spectral light requirements
and maximum light levels for long-term germling growth of several red algae from different
water depths and a green alga, European Journal of Phycology, 29:2, 103-112, DOI:
10.1080/09670269400650551

To link to this article: https://doi.org/10.1080/09670269400650551

Published online: 17 Feb 2007.

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 Eur, ]. Phycol.(1994), 29: 103-112. Printed in Great Britain 103

Minimum spectral light requirements and maximum light levels

for long-term germling growth of several red algae
from different water depths and a green alga

PETRA LEUKART 1. A N D KLAUS L U N I N G 2

~Biologische Anstalt Helgoland, Meeresstation, D-2192 Helgolar~, Germany

2Biologische Anstalt Helgoland, Zentrale Hamburg, Notkestrasse 31, D-2000 Hamburg 52, Germany

Spores and germlingsof six red algal species were cultivatedfor 15 weeks in coloured light fieldsat low intensities.The photon fluence
rates at which growth exceeded growth in dark-kept controls were, in green light, 0-1 #mol m-2s-1 in Audouinella daviesii, 0.5 #mol
m-2s -1 in Halarachnion ligalatum, Pterothamnion plumula, Chondrus crispus and Plumaria elegans, and I'0/~mol m-2s -~ in Ceramium rubrum.
In blue or red light, at least 1-0 #mol m-2s -1 was required for germling growth in these species, except for P. elegans which required
0"5 #mol m-Zs -I in blue light. The advantage of green light for growth was particularly evident in A. daviesii which formed no more
than two cells in darkness and in photon fluence rates up to 1 #tool m-Zs -~ of blue or red, but one further cell after 15 weeks at 0"1 #mol
m-2s -1 in green. Germling growth of the green alga Ulva pseudocurvata required at least 3/zmol m-2s -1 in green, but only 1"0/zmol
m-2s -1 in blue or red light. White fluorescent light levels permitting growth in red algae were higher than those in green light and equal
to minimum requirements in blue or red light in the majority of species investigated. Settled spores of H. ligulatum and the green alga
Chaetomorpha melagonium survived for at least 1 year in darkness, whereas spores of C. crispus survived only 39 weeks and those of 11
other red algae and U. pseudocurvata survived 26 weeks or less. Light saturation and light inhibition of growth occurred at higher photon
fluence rates in the lower eulittoral species Ceramium rubrum, C. crispus and U. pseudocurvata (saturation, 200-300 #tool m-2s-1;
inhibition, 300-500/zmol m-2s -1) than in the strictly sublittoral species H ligulatum and P, plumula (saturation, 10-20 #mol m-2s-~;
inhibition, 50-100 #mol m-2s-1).

Key words: Growth, Light quality, Minimum light requirements, Photoinhibition, Red algae.

Introduction
The dim light available for algal photosynthesis and
photomorphogenesis near the lower limit of autotrophic
life in the sea is purely green in turbid coastal waters,
and blue in clear, oceanic waters (Jerlov, 1976; Dring,
1981; Kirk, 1983; Glover el al., 1986, 1987). Measured
or expected photon fluence rates near the lower limit of
observed algal life in the sea range from 0"03 to 1/zmol
m --2 s--I (Littler et al., 1985, 1986; Ltining, 1990). In the
laboratory, minimum light levels for growth of sea-
weeds have only been determined for broad-band,
white fluorescent light and range from 0"18 to 1"0 #tool
m --2 s--1 for the deep-water red alga Atractophora hyp-
noides P. Crouan et H. Crouan (Maggs & Guiry, 1987)
to 2-5/zmol m - 2 s -1 for the green alga Ulva lactuca L.
(Sand-Jensen, 1988).
Few algae have been tested in the laboratory for
growth performance in pure blue or green light at low
light levels, i.e. at tens of #mol m - 2 s - I or lower. Early
data on red algal growth rates in blue, green and red
*Present address: Forschungsinstitut Senckenberg, Lochmfihle, D-6465
Biebergemfind, Germany.
light were provided by Harder & Bederke (1957) for the
unicellular red alga Porphyridium sp., and for the fila-
mentous Trailliella-phase of Bonnemaisionia hamifera
Hariot. Growth rates, based on cell counts, were much
higher in the green than in the blue and red light. This
supports the notion that spectral growth in red algae
follows spectral photosynthesis, with maximum effi-
ciency in the green as shown by the earliest photosyn-
thetic action spectra by Engelmann (1884), by the
classic work of Haxo & Blinks (1950), and later by
Lfining & Dring (1985) for thin and thick red algae.
Other findings demonstrating a parallel behaviour of
growth and photosynthetic action spectra in phycobilin-
rich algae relate to deep-water ultraphytoplankters and
various phytoplankton clones which were tested for
spectral growth and photosynthetic demands at low
light levels (Glover et al., 1986, 1987; Hauschild et al.,
1991). Phycoerythrin-rich Synechococcus, a cyanobacter-
ium with growth saturation at around 50/zmol m-Zs -1,
grew and photosynthesised most efficiently in dim
green light, and Synechococcus clones with phycourobilin
chromophores increased the ability for growth and
photosynthesis in dim blue light (but see discussion in
Dring, 1990). One objective of the present investigation

Published online 17 Feb 2007

P. Leukart and K. Lf,ining
was to obtain spectral growth data at very low photon
fluence rates for red algal species from different water
depths and, for a simple comparison, for one green algal
species from shallow water.
With respect to the spectral aspects of upper light-
controlled occurrence limits of sublittoral seaweeds, data
are available from action spectra for light inhibition of
photoynthesis in several marine macroalgae (Nultsch et
al., 1987, 1990; Hanelt et al., 1992). These investigations
showed that photosystem II is most sensitive to strong
light and represents the "weak" part of the photosynthetic
apparatus, as is known for unicellular algae and higher
plants. The inhibition of red algal growth by high-
intensity green light was discovered by Boney &
Comer (1963), who were able to increase growth rates
in the phycoerythrin-rich algae Pterothamnion plumula and
Plumaria elegans by removing green light with dilute
solutions of eosin yellow, at high white light intensities
that bleached the algae and reduced growth without the
eosin filter.
As to growth-reducing light levels in deep-water red
algae, it is known that the growth rate of Atractophora
hypnoides becomes inhibited at the rather low photon
fluence rate of 30 #mol m-2s -1 in white fluorescent light,
and lethal damage occurs at 50 #mol m-2s -I after a few
weeks (Maggs & Guiry, 1987). The present paper
complements these aspects with data for growth toler-
ance to photon fluence rates of up to 500#mol m-2s I
for six red algal species and an Ulva species, which were
also treated with regard to minimum light requirements as
mentioned above.
Materials and methods
Algal material
The algal species investigated and their vertical distribu-
tion ranges near Helgoland, North Sea, are shown in
Table 1. Spores were obtained from several fertile thalli
from the sublittoral zone by placing these into seawater
and waiting for spontaneous spore release. The spores
of Audouinella daviesii (Dillwyn) Woelkerling originated
from laboratory culture. The exact depth distribution of
this sublittoral species near Helgoland is unknown.
Algal culture
The spores were pipetted onto coverslips in plastic Petri
dishes (50ram diameter) and were permitted to settle
overnight. Subsequently, the Petri dishes were filled with
15 m[ enriched seawater and placed into the experimental
light fields. Enriched seawater according to Provasoli (PES;
Provasoli, I968; Starr & Zeikus, 1987) with the addition of
potassium iodide (Tatewaki, 1966) was used as a growth
medium. During the first week of cultivation, one drop of a
saturated solution of germanium dioxide (Lewin, 1966) in
distilled water was added to each Petri dish to suppress the
growth of diatoms. The medium was changed every 2
104
weeks. Temperature for culturing and all treatments was
10°C.
Broad-band, low-intensity light fields with fluorescent tubes
and various filter types
White fluorescent tubes (Osram, L65W/25S) and blue,
green or red fluorescent tubes (Thorn 65W) were used for
long-term growth measurements at low light levels. Blue,
green or red fluorescent tubes were combined with blue
Cinelux foil (no. 419), green Cinemoid foil (no. 23A;
Strand Lighting, Wolfenb/ittel, Germany) or red Plexiglas
(R6hm no. 501, 3 mm thick), respectively. Neutral filters
(Schott), grey Plexiglas (R6hm no. 807, 3 mm) and/or
transparent paper were used to reduce photon fluence
rates to the required values. Spectral distributions of the
blue, green and red light fields were measured by means
of an LI-1800 UW spectroradiometer (LI-COR, Lincoln,
Nebraska, USA) and are shown in Fig. I. Photon fluence
rates used were measured by means of a flat LI-COR
190SA quantum sensor.
Narrow-band light fields with interference filters for
effectiveness spectra of growth
Leitz Prado Universal projectors (24V 250W quartz
iodine lamps; 5 mm KG 3 heat filter) were combined
with narrow-band interference filters (type IL, half-band
width 10-15 nm; Schott, Mainz, Germany), with max-
imum transmissions at 413, 434, 452, 460-5, 481, 498,
547, 603, 654, 674"1 or 688 nm. Photon fluence rate was
10 #mol m-2s -~, and algal spores and germlings were
exposed in Petri dishes filled with PES for 2 weeks, or
only 6 days in the case of the fast-growing Audouinella
daviesii.
High-levd projector light fields for studies on growth
saturation and inhibition
Schott glass filters 2mm BG38 and 4ram GG4 were
combined with Leitz Prado projectors to imitate under-
water light type 17 (Lfining, 1980). This combination
corresponds to Jerlov water type 7 (Jerlov, I976) at
moderate water depths, which prevails in Helgoland
during summer (LOning & Dring, 1979). For coloured,
higher-intensity light fields, Leitz Prado projectors were
combined with coloured foil or Plexiglas filters, as
described above for low-intensity coloured light fields.
Maximum photon fluence rates obtained in the projector
fields on an area of approximately 5 x 5 cm were 500 #mol
m --2 s- - I , or only 300 #mol m-2s -I in the case of blue light.
Experimental design for survival in the dark
A light-tight box made from black PVC (50 x 30 x 20 cm)
was placed in a constant-temperature room at 10°C. The
spores of the algae were pipetted onto coverlips in plastic
Petri dishes and immediately moved into the light-tight
Light requirements for growth in red algae 105

Table 1. Algal species investigated for their growth versus light curves (GRO) or sporeling dark tolerance

Spore and Depth range (m) Dark survival

Speciesa investigationtypesb or zonec span (weeks)`/

R Ceramiumrubrum (Huds.)C. Ag. CS/GRO 0-3 8

R Polysiphonianigrescens(Huds.)Grev. TS SL 8
R Polysiphoniaelongata(Huds.)Spreng. CS SL 8
R Audouinella (=Acrochaetium)daviesii (Dillwyn)Woelk. MS/GRO SL 12
R Delesseriasanguinea(Huds.)Lamour. TS 2-ll 12
G Ulva pseudocurvataKoemanet Hoek ZO/ZG/GRO o-9 18
R Rhodomelavirgata Kjellm. TS SL I8
R Rhodomelaconfervoides(Huds.)Silva TS 0-7 26
R Polysiphoniaurceolata(Lightf.ex Dillwyn)Grev. CS 0-10 26
R Plumariaetegans(Bonnem.)Scbmitz~ PS/GRO SL 26
R Pterothamnion(= Ant#hamnion) pIumula (Ellis)Naeg. TS/GRO SL 26
R Brongniartellabyssoides(Good. et Woodw.) Schmitz CS 4-11 26
R ChondruscrispusStackh. CS/GRO 0-2 39
G Chaetomorphamelagonium(Web.et Mohr) Kuetz. ZO 0-7 52
R Halarachnionligulatum (Woodw.)Kuetz. CS/GRO 5-7 52

dR, red alga; G, green alga.

bSpores used as startingmaterialfor experiments:TS, tetraspores;CS, carpospores;MS, monospores;PS, paraspores; ZO, zoospores;ZG, zygotes.
CDepth distributionin metres below mean low water of spring tides near Helgoland according to Lfining(1970). In cases of unknownexact vertical
distribution,SL designatessublittoralzone.
°/Theperiods in darknessafter which some algal germlingswere still able to grow in subsequentlight. Specieshave been ordered accordingto their dark
survivalspan.
eNow Plurnariaplumosa (Hudson)O. Kuntze.

box. After I day of settlement in the water drops on the
coverslips the Petri dishes were filled with PES. After 4
weeks, 8 weeks, 12 weeks, 16 weeks, 6 months, 9 months
and 12 months, one coverlip with adhering spores was
removed and cultivated at 10 #tool m-Zs -1 in cool white
fluorescent light. Successful survival in darkness was
considered to have occurred if the germlings were able
to grow in subsequent light. After the absence of survival,
further dark treatments were tested for up to 8 weeks after
the first non-surviving culture in order to confirm the
maximum survival time. Bacteria were not a problem
during these long periods of dark exposure, The PES
medium was renewed each month, which involved
cultures being exposed for a few seconds to the green
light of a torch, with a fluence rate of approximately
5/zmol m-2s - I .
Growth measurements

The minimum light requirement for growth was defined

I
as the photon fluence rate at which cell numbers of
E
t-
filamentous germlings or the area of crustaceous germ-
lings exceeded the cell numbers or area of dark controls.
Y Cell number was determined b y means of an Olympus
¢~ 0.018 CH-2 microscope equipped with a x 25 Leitz seawater
I
immersion objective. In crustose germlings the diameter
E blue
was measured from outline drawings produced b y means
o
of a drawing mirror on a Wild M20 microscope. Mea-
~0.012- surements were made every 2 weeks. Standard deviations
green
ID were calculated from values of 20 germlings. Statistically
significant deviation of mean values from means of dark
controls was tested b y single classification analysis of
~U 0 . 0 0 6 - variance (Sokal & Rohlf, 1981).
C
G)

o
r,-
f
I I
\
/ ill
Measurements of photosynthetic action spectra

Thallus pieces were cut from thalIi of Audouinetla daviesii,

O 400 500 600 700
t"
13_ Wavelength (nm) Halarachnion ligulatum or Pterothamnion pIumu[a grown at
Fig. 1. Spectral distributions in broad-band coloured light fields 10 #mol m-2s -~ (white fluorescent light, 16h light per
achieved with fluorescent tubes and filters of coloured Plexiglas day) and 10°C. The measurements were made at the
or foil. University of Marburg with a measuring system accord-
P. Leukart and K. Lfining 106

ing to Huppertz et al. (I990). The plants were directly
fixed on the membrane of an oxygen electrode (WTW
Oxi 92) which was mounted in a flow-through cuvette.
The temperature of the seawater in the flow-through
system was 16 (3-0.I)°C. The interference filter light
fields were achieved as described above, and Schott
interference filters 522 and 572nm were used in addi-
tion. For each wavelength, fluence rate-effect curves were
measured at I2 different photon fluence rates obtained by
inserting Schott neutral glass filters. One measurement at
each wavelength, including all 12 photon fluence rates,
lasted for about 20 rain. The action spectra of photo-
synthesis were obtained by calculating the fluence rate for
obtaining 50% of the maximum photosynthetic rate. The
reciprocals of these values are shown in the action spectra.
The absorption spectra of Audouinella daviesii, Halarach-
nfon ligulatum and Pterothamnion plumula were measured
by means of a Shimadzu UV-2100 spectrophotometer.
Results
The minimum spectral light requirements for growth
(Tables 2, 3) were lower in green than in blue or red
light in the lower sublittoral red algae Audouinella daviesii,
Halarachnion ligulaturn and Pterothamnion plumula and in
the upper sublittoral/lower eulittoral Chondrus crispus.
Growth in green light started at 0-5 #tool m-2s -1 in
these species, except for A. daviesii which started growing
at 0'1 #tool m-Zs -1. Plumaria elegans, from the sublittoral
and shadowed lower eulittoral zones, started to grow at
0"5#mol m-Zs -1 in blue as well as in green light.
Ceramium rubrum, a lower intertidal and upper sublittoral
alga, required at least 0-5#mol m-2s -1 in all three
spectral ranges. In white fluorescent light the minimum
requirements for growth were higher than those in green
light in A. daviesiL H. Iigulatum, P, plumula and C. crispus,
but equal in C. rubrum and lower in P. elegans (Tables 2, 3).
The small epiphytic species Audouinella daviesii pro-
duced a maximum of two cells after I5 weeks in darkness,
while the first three-celled germlings were observed at
0"l#mol m-2s -I in green light (Table 2). The rapid
increase in cell number with rising light levels in green
light, as compared with blue, red or white light, is
illustrated in Fig. 2. This is an example of the general
trend observed for the majority of the red algal species
investigated (Table 2).
The filamentous red algae grown under low-light
conditions exhibited a reduced morphology, irrespective
of spectral range. Long and scarcely branched filaments
were formed, without any sign of the species-specific
ramification patterns, In Pterothamnion plumula the secre-
tory cells were missing.
The effectiveness spectra for growth (size or cell
number) and the action spectra for photosynthesis in

T a b l e 2. M e a n cell n u m b e r or size of algal g e r m l i n g s (n = 20) at I 0 ° C and 16 h l i g h t per d a y in b r o a d - b a n d c o l o u r e d or w h i t e l i g h t

fields at l o w p h o t o n fluence rates or in darkness, as ascertained after 15 w e e k s in culture

Photon fluence rate (#mol m 2s-1)

Size
Species parameter Dark 0"0I 0"05 0"I 0"5 i'0

Audouinella daviesii C 1"6 B 2'0 1"8 1"9 5"5***

G 1"7 2"5* > 30 > 30
R 1"9 1"9 2'1 9"8***
W 2.0 2'0 4"9 27"8***
Halarachnion ligulatum D 10"0 B 10-2 10"4 10"5 12"0"*
G 10"5 10"4 15"6"* 32"0**
R 9"3 I0"0 9'9 9"7
W 9"5 9"5 9"9 19"I***
Pterokhamnion plumula C 4"6 B 4'2 4.8 5.3 5'9***
G 4'9 5"2 6"3*** 17"5"**
R 5'2 4"5 4"1 5"9***
W 3'9 3.3 5"2 5.3
Chondrus crispus D 13'9 B 13-4 14"3 I4"7 17'9"**
G 13"6 14'5 17"3"** 32'3***
R 14-2 14"0 14"9 19"5"**
W 11.9 11.9 13"1 20"3***
Plumaria elegans C 4'0 B 4.4 4'2 5"9* 6'9***
G 4"5 3.9 10"7"** I5'2"**
R 5"0 4"3 5'4 7'1"**
W 4'8 5"5* 6"9*** 14.6"**
Ceramium rubrum C 7'3 B 7'2 7'9 8"4 17'6"**
G 6"8 7"4 9"0 29"5***
R 7"7 7"5 10"1 12'2
W 9"6 9"1 8"4 12"0"*

B, blue; G, green; R, red; W, white. See Fig. I for spectral distributions. Size is given as cell number (C) or maximum diameter (D; in #m) of crustaceous
germlings. Mean values followed by *(p < 0.1), **(p < 0"1) or ***(p < 0"001) are significantly greater than the mean value of dark control (single
classification analysis of variance; Sokal & Rohlf, 1981; program GraphPad InStat).
Light requirements for growth in red algae 107

Table 3. Minimum light requirements (#mol m-Zs-1) for 16

growth of algal germlings in broad-band blue, green, red or 141
white fluorescent light at 16 h light per day and 10°C,
12
as ascertained after 15 weeks in culture.
10
8
Species Blue Green Red White Jes ,," 0.5
6. %/ I x 0.1
Audouinella daviesii 1"0 0"I I"0 1"0 L4 0.01
Z 41
Halarachnion ligulatum 1-0 0.5 > 3['0 1-0
Pterofhamnion plurnula 1"0 0"5 1'0 > 1"0 2.
Chondrus crispus 1"0 0"5 1"0 1"0
0
Plumaria elegans 0"5 0"5 1"0 0"1
0 4 8 12 16 20 24 28 32
Ceramium rubrum 1'0 1"0 > 1"0 1"0
T i m e (weeks)

8
the sublittoral red algae Halarachnion ligulatum and • 1.0
- - - c~ - - o.5 Blue ligh!
Pterothamnion plumula and Audouinella daviesii exhibited x 0.1
maxima only in the green part of the spectrum, in spite of •~ 6 ---o--- 0.01
high absorption peaks also in the blue and red ranges (Figs
3-5). $4
The germlings of the intertidal and upper sublittoral E
green alga Ulva pseudocurvata produced one cell in z
darkness after i1 weeks of cultivation. Germlings with 2
more than one cell were found from l # m o l m-Zs -1
onwards in blue or red light, but 2 or 3 #tool m-Zs -1 0
were required for this in white or green light, respectively 0 4 8 12 16
T i m e (weeks)
(qualitative data, not shown; 10°C, 16 h light per day).
Prolonged cultivation of 6 months in white fluorescent
light at 0'01 and 0-1 #mol m-2s - I did not increase the 12
diameter of the zygotes of Ulva pseudocurvata, compared : - , . o0.5 y/// /
with the diameter of arotmd 3 # m in continuous darkness. 10. - - - c ~ - - [ G r e e n light
A -- 0.l ~]/
Zygotes at 0"5 or 1"0 #tool m-2s -1 increased in diameter ---o--- 0.01 ~/
~o 8_
up to 5 or 8 #m, respectively, but did not form a second
cell. 6.
The survival span of algal spores and resulting germ- E ,/
4.
lings in darkness is given in Table 1. Maximum dark z
survival was detected in spores of the lower sublittoral 2.
red alga Halarachnion ligulatum and the deep-water green
alga Chaetomorpha melagonium. Their spores were still 0
alive in darkness after 1 year, when the experiment was 0 4 8 12 16
Time (weeks)
ended. Spores of lower eulittoral and upper sublittoral
species such as Ceramium rubrum and Polysiphonia nigres-
12
cens were at the other end of the scale, surviving 8 weeks
but not 12 weeks. Twelve weeks in darkness were 10 e 1.o R e d light l l
---°--- o.5 [ ~._~
survived by the mid- and lower sublittoral Delesseria • o.1 ~ I
sanguinea, and 18 weeks by Ulva pseudocurvata, which 8 ---~-- o.ol /[ 1
g,#
can form conspicuous thalli in summer also in the mid-
6
sublittoral zone (Lfning, 1970). The spores of red algal
species with a wide distribution range within the sub- E 4.
littoral, such as Polysiphonia ~rceolata or Rhodomela con-
fervoides, survived for 6 months in the dark. It was 2
surprising to find that the spores of the lower eulittoral 0
and upper sublittoral Chondrus crispus could survive 9 0 4 8 12 16
months in darkness. T i m e (weeks)
The spores of all red algal species germinated in
Fig. 2. Audouinelladaviesii. Time course of increase in cell
darkness. The number of dark-produced cells varied number in germlings from monospores in broad-band coloured or
according to species and to individual germlings in the white light fields at 0-1 #mol m-2s-1, 16h light per day and
same species, and ranged, for example, from I to 2 in 10°6 Vertical lines indicate standard deviations (n = 20). See
Audouinella daviesii from monospores, from 1 to 8 in Fig. I for the spectral composition of blue, green and red lights.
P. Leukart and K. Lfining 108

24.
-0.09 "~'~
8.
0.08 "~~
T Halarachnion ligulatum . ~ ?, IAudouinella daviesii
22.
~ \ ; "0.08 ~,.~ 7. /~J~.~, o,a_
20. 0.07 ~" =" ~6
x

m
i 18 .~="
0.06
.! 16 GI
!4.
k/V~ 'o......o %.4-Or04
~'~
B.%"
14. !o,o4 U,=..
AB* ....
3,
12. -0.03 ~ g 0.02 ~ ~
10 2. AB ,2-
b
"oF
0,2- -0.02 ~ =
8 1 0.00 g
0.01
400 500 600 700 500 600 700
Wavelength (nm) Wavelength (nm)
Fig. 3. Halarachnionligulatum.Size versus spectral photon fluence
rate (GR; filled symbols) in germlings from carpospores, and Fig. 5. Audouinelladaviesii.See legend to Fig. 3 for further
action spectrum of photosynthesis (PS; open symbols) in details. Size was measured as cell numbers achieved after 6 days
interference filter light fields at half-band widths of I0-15 nm, (n = 20).
and in vitro absorption spectrum (AB; continuous line). Size was
measured as the diameter of crustaceous germlings after 2 weeks
at 10 #mol m-~s 1. Vertical lines indicate standard deviations for
growth measurements (n = 20). Photosynthetic rates were
measured at 12 different photon fluence rates per interference
filter and are expressed as the reciprocal of the photon fluence
rate at which 50% of the maximum photosynthetic rate was
obtained.
24

Pterothamnion plumula from tetraspores, and from 1 to 13

in Ceramium rubrum from carpospores. The m a x i m u m
i 16
12
number of cells, more than 30 in one plane, were
4
produced b y tetraspores of Rhodomela oirgala. Since
0
Audouinella daviesii never formed more than t w o cells in
darkness, this species offered the best m o r p h o l o g i c a l l y "~ 24 Halarachnion ligulatum
defined criterion for the start of light-dependent growth.
,- 20
N o cell divisions t o o k place in the dark in spores of the O

green algae Ulva pseudocurvata and Chaetomorpha mela- E

gonium. ~ 12
Inhibition of growth in simulated underwater projector 8 , = , , J , = • =
light fields occurred from 20 #tool m - 2 s -1 onwards in the T

Pterothamnion plumula
lower sub]ittoral Plumaria elegans (Fig. 6), which is also '-
" 18 [
..a
found as an understorey species in lower eulittoral to mid- E 14
sublittoral locations. The next most sensitive alga was C
-- 1(1
Halarachnion ligulatum from the lower sublittoral, with light
saturation of g r o w t h starting at 10/~mol m - 2 s -~ and light O 6
inhibition from 50 # m o l m - 2 s -~ onwards (Fig. 6). In the
•_ 10 [ Audouinella daviesii
I6
/~ ~ ~ , :erothamnoin plumula 0.12 = "~
-~
E
8

¢.. 12
14
1,0- i
-0.10

0.08 ~ '
r~-~
O
c 6

lO 0
-~ I\\', / il 0.06 ~.%" 0 1;0 2;0 3;0 4;0 500
8 0.04 ~ Photon fluence rate (prnol m-Zs -1}
R 0,5-
Fig. 6. Size versus photon fluence rate in simulated underwater
6: 0.02 ! ~ light 15 (projector combined with Schott glass filters 2 mm BG38
4 and 4 mm GG4), at 10°C and 12 h light per day. Crustaceous
o.oo
400 500 600 700 germlings of Halarachnion ligulatumwere cultivated from
Wavelength (nm) carpospores for 9 days, filamentous germlings of Plumariaelegans
Fig. 4. Pterothamnionplumula. See legend to Fig. 3 for further from paraspores, and Pterothamnionplumula from tetraspores for
details. Size was measured as cell numbers achieved after 2 weeks 14 days, Audouinelladaviesiifrom monospores for 5 days.
(n = 20). Vertical lines indicate standard deviations (n = 20).
Light requirements for growth in red algae 109

48 lower eu]ittoral/upper sublittoral species Ceramium rubrum,

42 Chondrus crispus and Ulva pseudocurvata (Fig. 7). In all red
a6
algae studied, pigmentation was weak in light fields of high
E 3O
photon fluence rate and strong in those of low photon
" 24
~ 18 fluence rate.
O In Audouinella daviesii, light saturation and inhibition of
12
~l m" I m I = 1 = 1 = growth were studied additionally in blue, green and red
Chondrus crispus light fields (Fig. 8). The number of newly formed cells was
E
:=L 36 highest in green and lowest in red light. In all colours,
~ 3O growth inhibition started above 100-200 #mol m-Zs -I
1 1
~ 24
E
a
N 18 Discussion
12 The minimum light requirements were lowest in green
Ulva pseudocurvata light for all red algae investigated (Fig. 2, Tables 2 and 3).
~ 8 The minimum photon fluence rate for light-dependent
.a
E 6 growth at 0'l#mol m-2s -1 for Audouinella daviesii
c confirms other reported lower light limits for algal life
m 4
O (L~ning, 1990), and could be clearly ascertained by
O 2
formation of a third ceil, since more than two cells were
0 never formed in dark-grown germlings by this species.
6 160 260 360 460 S00
The narrow-band effectiveness spectra of growth mea-
Photon fluence rate {pmol m-as -1) sured at 10 #tool m-Zs -~ for three red algae followed
their photosynthetic action spectra, with maximum effi-
Fig. 7. Size versus photon fluencerate in simulatedunderwater
light 17 (projector combinedwith Schott glass filters2 mm BG38 ciency in the green range. These results point to the
and 4 mm GG4), at I0°C and 12 h light per day. Crustaceous importance of light quality for survival at low photon
germlings of Chondruscrispuswere cultivatedfrom carpospores fluence rates and corroborate the findings of Harder &
for 14 days, filamentousgermlingsof Ceramiumrubrum from Bederke (1957), Beer & Levy (1983) and Glover et al.
carpospores for 7 days, and Ulva pseudocurvatafrom zoospores (1986, 1987) on optimal growth of phycoerythrin-rich
for 9 days. See legend to Fig. 6 for further details. algae in green light at photon fluence rates in the order of
tens of #tool m-2s -~ or lower. The lower growth rates of
sublittoral species Pterothamnion plumula and AudouineUa Ulva pseudocurvata in green, as compared with blue or red
daviesii, a tendency for growth reduction appeared beyond light, are well known for other green algae, such as
100 or 200 #mol m-2s -1, respectively (Fig. 6). No inhibi- Chlorella sp. (Harder & Bederke, 1957) or Chlamydomonas
tion of growth up to 500/zmol m-2s -1 was apparent in the sp. (Brown & Green, 1974).
It might be expected that such data, although relevant
only to the lowermost part of the euphotic zone in the
sea, may contribute to the long-lasting discussion of
12 Engelmann's (1883) hypothesis on phylogenetic chro-
matic adaptation in seaweeds and Oltmanns' (1892)
1081 / ~ Audouinella daviesii
view that light intensity is more important than light
T - - -[3--- blue quality (see discussions by Dring, 1981, 1990; Ramus
"~ T/! ~ • green 1981, 1983; Ramus & van der Meet, 1983; Kirk, 1983).
Possible ecological conclusions from the present study
are, however, restricted due to the fact that a highly
~Z 6 ~"~ ~
selected group of species was used for the growth studies
in coloured light fields, without any deep-water green or
4 brown alga included.
Ramus (1983) and Ramus & van der Meer (1983)
measured growth rates with regard to different light
qualities and light quantities in adult thalli of several
seaweed species held in outdoor tanks at photon fluence
0 100 200 300 400 500 rates one to two orders of magnitude higher than used in
Photon fluence rate (pmol photons m-2s -t) the present investigation. These studies had shown that,
Fig. 8. Audouinella daviesii. Size versus photon fluencerate in at photon fluence rates of 100-200 #tool m-Zs -~ during
germlings from monospores in blue, green and red light fieldsat midday, or 13% of incident daylight, light-limited growth
10°C and 12 h light per day. Size was measured as cell numbers depended more on photon fluence rate than on spectral
achieved after 5 days (n = 20). composition. Grinnellia americana (C. Agardh) Harvey and
P. Leukart and K. Lfining
Gracilaria tikvahiae McLachlan were included in these
studies as examples of red algae, but both occur in the
sublittoral zone at moderate water depths. Deep-water
red algae would possibly not have survived long-term
exposure under the light levels used by Ramus (1983) and
Ramus & van der Meer (1983). Hence, a possible
importance of light quality for red algal growth at very
low levels was missed. The fading importance of phyco-
bilins at increasing light intensity had been stressed by
Larkum & Weyrauch (1977). These authors had found
from photosynthetic action spectra in the red alga
Griffithsia monilis that at low intensity the phycobilins
are the major light-harvesting pigments, while at increas-
ing light intensity chlorophyll and carotenoids contribute
proportionately more to the spectrum since the phycobi-
lin activity becomes light-saturated.
Action spectra of growth may be more conclusive for
the ecological success of a seaweed species in different
spectral environments than photosynthetic action spectra,
particularly at depths characterised by chronic lack of
light. The parallel behaviour of effectiveness spectra for
growth and action spectra for photosynthesis (Figs 3-5)
in phycoerythrin-rich red algae, with maximum efficiency
in the green, would mean that both photosynthetic and
possible growth-regulating photomorphogenetic require-
ments are optimally fulfilled exclusively in this part of the
spectrum. The present results are not quite conclusive in
this respect because the broad-band green light field with
fluorescent tubes and green foil filter contained also some
blue light, down to wavelengths of 450nm (Fig. i).
Recent indications of a green-light sensor, in addition to
phytochrome-like pigments and cryptochrome, regulat
ing photosynthetic pigment and/or protein concentration
in red algae have been presented by L6pez-Figueroa &
NieU (1990, 1991). Further experiments on long-term
growth of phycoerythrin-rich red algae in pure green
light are required. It seems clear, however, that the
phylogenetic adaptation of pigments in deep-water
algae adapted to low light of a particular spectral
character in the sense of Engelmann (1883) and Kirk
(I983) should refer to spectrally controlled evolution of
photosynthetic as well as photomorphogenetic pigments
for a particular environment.
The minimum white fluorescent light levels for red
algal growth determined in this study (Tables 2, 3) are
consistent with previously published data that indicate
minimum photon fluence rates ranging from 0'2 to
l'O/zmol m-2s -I in red algae (Jones & Dent, 1971;
Maggs & Guiry, 1987) and in a brown alga (Orfanidis,
1992). Culture experience with unicellular algae indicates
that representatives of all major algal groups can be
cultivated at photon fluence rates of the order of
1 #mol m-2s -1 (Geider et al., 1985). The minimum level
of 0"1 #tool m-2s -1 at 12 h light per day allowing first
microscopic hints of growth after 15 weeks of cultivation
in the filamentous red alga Audouinella daviesii (Tables 2,
3) converts to l'6mol photons m-2year - I . Liining &
Dring (1979) calculated an annual quantum input of 6 tool
110
photons m-2year -1 for the deepest-occurring, macrosco-
pically visible coralline crusts near Helgoland - of a
similar order as the present result.
The minimum requirements for growth and cell divi-
sions of Ulva pseudocurvata (2"0#mol m-2s-1; 16 h light
per day) were similar to the value of 2.5 #mol m-2s -I (in
continuous light) reported for thallus disks of Ulva lactuca
(Sand-Jensen, 1988). The surprisingly low values of
minimum light requirement for the lower eulittoral/
upper sublittoral species Ceramium rubrum and Chondrus
crispus (Table 2) suggest that, even at moderate water
depths, germlings may have to tolerate low photon
fluence rates under the cover of the algal vegetation.
Even a red alga from the supralittoral zone, Bangia
atropurpurea, had a minimum light requirement as low as
2-5 #mol m-2s -I (Orfanidis, 1992).
A critical question relates to daylength, which was
uniformly provided at 16 h light per day in the long-term
treatments. Would the sizes or cell numbers achieved at
1.0 #mol m-Zs -I for 8h per day be the same as those at
0"5 #mol m-2s -1 for 16 h? This cannot be answered, since
daylength was not altered in the present study, but some
reciprocity at very low photon fluence rates may be
expected. Maintenance light levels (Pirt, 1982; Raven,
1984, 1986) have to be surpassed for the first hints of
growth to be observable. The photon fluence rate for
maintenance respiration rate in photoautotrophic growth
may be almost zero and practically unobservable (Geider
et al., 1985, 1986). It may thus be expected that, at light
levels allowing first growth, photons absorbed at any
daylength and low photon fluence rates are important.
Photon exposure ( #mol m -2) rather than photon fluence
rate (#mol m-2s -1) may, hence, be more meaningful for
characterising light levels dominating the onset of
growth.
It should be emphasised that none of the species
cultivated at very low light intensities formed thalli of
typical morphology after several months of cultivation, or
even after 1 year in Pterothamnion plumula. Neither
sporangia nor gametangia were developed. It is possible
that photon fluence rates near to 1 #mol m-2s -I enable
growth only in order to bridge times of low light and do
not permit normal development and reproduction. The
survival of algal spores or thalli in continuous darkness is
obviously tied to vertical distribution. Dark survival spans
of the order of a few months or a year, in upper or lower-
shore species, respectively (Table 1), are consistent with
previously published data (Boalch, 1961, Moss & Sheader,
1973; McLachlan, 1974; Sheader & Moss, 1975; Char-
nofsky et al., 1983).
All spores of red algae investigated in the present
study germinated in darkness, but not the spores of Ulva
pseudocurvata and Chaelomorpha melagonium which seem
to require light for cell germination and cell division. The
monospores of the protofloridean Bangia atropurpurea
have also been reported to require light for several days
for germination, with green light being most effective;
this is probably a photosynthetic rather than an inductive
Light requirements for growth in red algae
or photomorphogenetic effect (Chamofsky et al., 1983).
Light-dependent germination is also known for the
cyanophyte Anabaena, with maximum germination of
akinetes at 620-630 nm, C-phycocyanin being probably
the main photoreceptor (Braune, 1979).
Known saturation levels of growth for seaweeds in
white fluorescent light were compiled by Lfining (1990),
with values of 10-20/zmol m-2s -1 for the lower
sublittoral, or around 300 for upper sublittoral and
eulittoral species. These levels are also reflected by the
present results (Figs 6, 7). The low saturation level for
Pterothamnion plumula, 20 #tool m-2s -I at 12 h light per
day (Fig. 6), had previously been detected by Boney &
Comer (1963) in continuous light at approximately
10#tool m-Zs -1 or 500 lux, and by Sundene (1959),
again at around 500 lux.
The rather low light levels for growth inhibition in
white fluorescent light in Plumaria elegans or Halarachnion
ligulatum (20 or 50 #mol m-2s -I, respectively; Fig. 6), are
close to the value of 30 #mol m-2s -1 which was found to
inhibit the growth of the deep-water red alga Atractophora
hypnoides (Maggs & Guiry, 1987). The much higher light
tolerance of the eulittoral and upper sublittoral algae
Ceramium rubrum, Chondrus crispus and Ulva pseudocur-
vata in white fluorescent light (Fig. 7) reflects earlier
results of Biebl (1956) on survival of adult thalli of
species from the deeper sublittoral zone compared with
species from habitats where the thalli are exposed to full
sunlight at low tides. One of the few field determinations
of growth-inhibiting irradiation levels showed an inhibit-
ing photon fluence rate of 500#mol m-Es -1 for the
sublittoral, shade-loving understorey red alga Plocamiurn
cartilagineum (Kain, 1987).
The findings of Nultsch et al. (1987, 1990) and Hanelt et
al. (1992) on the selective strong-light sensitivity of
photosystem II in red and brown seaweeds added a
new light quality component to the discussion about
the structuring effects of light on the vertical zonation
of seaweeds. Deep-water red algae cannot exist at
moderate water depths because excessive irradiances,
mainly in the green part of the spectrum, would consis-
tently reduce their photosynthetic rate and thus even-
tually eliminate them, and only high-light tolerant red
algae have overcome this problem. The only experiment
addressing the possibility that growth inhibition is higher
in green than in blue or red light did not reveal significant
spectral differences (Fig. 8). The species used, Audouinella
daviesii, is, however, not a typical deep-water red alga,
and further experiments are required in this respect.
In conclusion, it may be expected that each species will
occur in the depth range at which sufficient light is
available for its growth and where the maximum
photon fluence rate can be tolerated, or compensated by
photorecovery. Strong light tolerance had to evolve
among those other red algae which managed to colonist
upper sublittoral and eulittoral habitats, where ample
green light and photodamaging short-wave radiation
are available.
Ill
Acknowledgements
Thanks are due to Hans Reichenberger for technical
assistance, and Dr Dieter Hanett for help in measuring
action spectra of photosynthesis. This study has been
supported by grants Lu 198/6-1 and 6-2 from the
Deutsche Forschungsgemeinschaft.
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