Estuarine, Coastal and Shelf Science (1995) 40, 239-247

The Osmotic Significance of the Heteroside

Floridoside in the Mangrove Alga Catenella
nipae (Rhodophyta: Gigartinales) in
Eastern Australia

U l f K a r s t e n a'b, K e v i n D . B a r r o w c, A n l k a S. M o s t a e r t a
a n d R o b e r t J. K i n g ~
~School of Biological Science, University of New South [Vales, Kensington,
N.S. I~. 2033, Australia and CSchool of Biochemistry and Molecular Genetics,
University of New South [Vales, Kensington, N.S. W. 2033, Australia
Received 19 August 1993 and in revised form 18 March 1994

Keywords: floridoside; mangrove alga; organic osmolyte; osmotic acclimation;

Catenella nipae

The effect of salinity on the intracellular floridoside concentration in the

mangrove alga Catenella nipae (Rhodophyta: Gigartinales) was investigated
using laC nuclear magnetic resonance spectroscopy (13C-NM_R), and gas-
liquid and high pressure liquid chromatography (GLC, HPLC). The florido-
side content increased linearly with increasing salinity, and hence is strongly
involved in osmotic acclimation in this species. In addition, during 13C-NMR
analysis isethionic acid was identified as a new metabolite in C. nipae. The
concentration of this compound also varied as a function of salinity. The
steady-state contents of floridoside were also recorded in various geographically
isolated field populations of C. nipae t~om mangroves along New South Wales
coastline of Australia. All isolates contained very high floridoside levels. From
these data, together with the physiological capability to accumulate floridoside
under hypersaline conditions for osmotic acclimation, it is interpreted that
floridoside is essential for survival in the extreme mangrove habitat.

Introduction
O r g a n i c osmolytes in m a r i n e algae have b e e n investigated intensively with a t t e n t i o n to
low m o l e c u l a r weight c a r b o h y d r a t e s (Kirst, 1990; R e e d , 1990). Different algal divisions
have characteristic c a r b o h y d r a t e c o m p o s i t i o n s , a n d are therefore o f t a x o n o m i c interest.
All r e d algae except those in the o r d e r C e r a m i a l e s u n i f o r m l y synthesize a n d a c c u m u l a t e
the h e t e r o s i d e floridoside [ a - D - g a l a c t o p y r a n o s y l - ( 1 - 2 ) - g l y c e r o l ] as a m a j o r p h o t o -
synthetic p r o d u c t (Kirst, 1980). K r e m e r a n d Vogl (1975) investigated several m e m b e r s
o f the C e r a m i a l e s w h i c h were s h o w n to p r o d u c e the chemically r e l a t e d digeneaside
[ a - D - m a n n o p y r a n o s y l - ( 1 - 2 ) - g l y c e r a t e ] as the m a i n c a r b o n storage c o m p o u n d . T h e s e

bPresent address: Max-Planck Institute for Marine Microbiology, Fahrenheitstrasse 1,

D-28359 Bremen, Germany.
0272-7714/95/030239+09 808.00/0 © 1995 Academic Press Limited
240 U. Karsten et al.

authors considered the occurrence of digeneaside to be a chemosystematic character

separating the Ceramiales from all other Rhodophyta. Recently, however, many excep-
tions to this pattern have been reported in members of Ceramiales growing in association
with mangroves (Karsten et al., 1992a, b). This ecosystem has a very characteristic red
algal flora dominated by genera in the Ceramiales, Bostrychia, Stictosiphonia and
Caloglossa (King & Puttock, 1989) and the genus Catenella (Gigartinales). In place of
digeneaside, Bostrychia synthesizes the isomeric polyols D-sorbitol and D-dulcitol, while
Stictosiphonia species contain D-sorbitol only (Karsten et al., 1992a). In contrast to these
genera Caloglossa synthesizes another polyol, D-mannitol (Karsten et al., 1992b). The
biosynthesis and accumulation of these polyhydric alcohols which are otherwise unusual
in red algae can be interpreted as adaptations allowing Bostrychia, Stictosiphonia and
Caloglossa to grow, reproduce and consequently to survive in the ecological extremes of
the mangrove environment. In this habitat the algae grow epiphytically in the eulittoral
zone on the bases of mangrove trees and their modified roots, where they are exposed to
wide fluctuations in abiotic factors, in particular desiccation and osmotic pressures. The
ability to synthesize and accumulate polyols as compatible solutes and osmolytes is of
vital importance to compensate for the corresponding stresses (Kirst, 1990).
In the mangrove habitat Catenella is often intermixed with Bostrychia, Stictosiphonia
and Caloglossa as a component of the so-called ' Bostrychia-Caloglossa association ' (Post,
1968; King & Puttock, 1989), and is therefore subjected to fluctuating salinities. As a
consequence, Catenella must have developed some metabolic strategy for osmotic
acclimation. Floridoside was reported in Catenella nipae (Kirst, 1980), but its potential in
osmotic acclimation was not investigated. In this paper floridoside is shown to be the
major organic osmolyte in C. nipae using ~3C nuclear magnetic resonance spectroscopy
(~3C NMR). The amount of this heteroside at a range of salinity treatments was
quantified using gas-liquid (GLC) and high pressure liquid chromatography (HPLC).
Of special interest were the steady-state concentrations of floridoside in geographically
isolated field populations of C. nipae, collected in mangrove communities on the
coastline of New South Wales, Australia.

Materials and methods

Plants of C. nipae Zanardini were collected in September 1992 from the upper eulittoral
zone in the mangrove community at Georges River estuary, Sydney, Australia. The
salinity of this location was measured at 10.5 during tidal outflow. All samples used for
the salinity experiments were briefly rinsed with tap water to remove epibionts, sand
grains and mud. The algae were then incubated for 72 h in 500 ml Pyrex Petri dishes at
a range of salt concentrations (5, 15, 34.5, 50 and 70). For the 13C-NMR measure-
ments, plants were collected from the same location in March 1993, and a restricted
range of salinity was used: 10, 34.5 and 60. All other conditions were the same. Diluted
seawater was prepared by mixing natural seawater with glass-distilled water. Concen-
trated seawater was obtained by adding artificial sea-salt (SEA-SALT, Sigma). All
experimental media were enriched with PES/2 (Starr & Zeik-us, 1987) and 3-4 m M
N a H C O 3. The plants were maintained in a growth cabinet at 25 °C, and illuminated
with 30 ~tmol photons m - 2 s - ~ provided by cool-white fluorescent tubes under a
light-dark rhythm of 16:8 h. This photon fluence rate corresponded very well with the
light conditions in the mangrove habitat where the algae are generally protected from full
sun exposure by the covering canopy. Light measurements in the field near the shaded
 Effect of salinity on floridoside concentration 241

32°S

New South Wales

33 °

!~,~/Sydney
34 °

Pacific Ocean

35 °

11 36 °

12 | I

13 100 km

37 °

151°E 152° 153 °

Figure 1. Map of the collection locations for the different populations of Ca~enellanipae
from mangroves along the coastline of New South Wales, Australia. The numbers refer
to those in Table 1.

substrata of Catenella gave readings on s u n n y days in s u m m e r b e t w e e n 60 a n d 100 ~tmol

p h o t o n s m 2 s - ~ (data n o t shown). T h i s preference for shaded habitats is also reflected
by the growth p a t t e r n in the laboratory, because m o s t red algae from mangroves show
in culture i n h i b i t i o n of growth already at irradiance < 5 0 - 7 0 ~tmol p h o t o n s m - 2 s - ]
(J. West, pers. c o m m ) .
Before analysis plants were repeatedly blotted dry u s i n g paper tissue to remove
extracellular m e d i u m a n d then oven-dried at 60 °C for 24 h.
Collections were m a d e from a range of p o p u l a t i o n s along the coastline of N e w South
Wales d u r i n g J a n u a r y - M a r c h 1993 (Figure 1) a n d these were analysed for comparative
purposes. C u l t u r e material isolated in Q u e e n s l a n d in 1987 was also i n c l u d e d in this
study.
T h e extraction a n d analytical c o n d i t i o n s for the G L C analysis offloridoside along with
the procedure for the isolation of a pure floridoside s t a n d a r d from the red alga Delisea
pulchra are described in detail by K a r s t e n et al. (1993). Q u a n t i t a t i v e floridoside
242 U. Karsten et al.

(a)

(b)
R

R
Fk
/
(c) F F \

100 90 80 70 60
Chemical shift (ppm)
Figure 2. J3C-NMR spectra of the 70% ethanol extracts of Catenella nipae treated for
72 h with salinities of (a) 60, (b) 34 and (c) 10. For each extraction exactly the same
dry weight (150 rag) was utilized. R is the resonance for the internal standard dioxane.

determinations were m a d e using H P L C with a refractive index d e t e c t o r (Karsten et al.,

1991). Both c h r o m a t o g r a p h i c m e t h o d s gave identical results.
Samples used for the ~ C - N M R m e a s u r e m e n t s were prepared as follows. A b o u t
150 m g of algal dry wt were extracted in B ml 70% ethanol (v/v) for 3 h in a w at er b at h
at 70 °C. After centrifugation at 5000 g the s u p e m a t a n t was evaporated to dryness and
re-dissolved in 0'5 ml D 2 0 (99"98%) for N M R spectroscopy. 1 3 C - N M R spectra were
recorded on a Bruker AM-B00 s p e c t r o m e t e r at 125-77 m H z . Typically a sweep w i d t h o f
30 000 Hz, 16 000 time d o m a i n points and a 60 ° pulse o f 3.5 ~ts were used for
acquisition, with c o m p o s i te pulse decoupling. T h e free i n d u c t i o n decay was zero-filled
to 32 000 data points and processed with a line b r o a d e n i n g o f 1.5 Hz. Samples were r u n
at 27 °C and referenced from dioxane (salinity 67-4).
 Effect of salinity on floridoside concentration 243

800

600

~_ 400

T-
i

"~
"r. 200
o

0 / II B
5 15 34"5 50 70
Salinity
Figure 3. T h e effect of salinity on the intracellular concentrations of floridoside in
Catenella nipae. Algae were treated for 72 h with salinities 5, 15, 34.5, 50 and 70. Data
are expressed as mean ( + S D ) values (n=4).

Results
The i SC_NM R spectra of C. nipae extracts after 72 h treatment at different salinities are
shown in Figure 2. The chemical shifts at 61"3, 61.9, 62.3, 69"3, 70.1, 70.2, 71"9, 79.6
and 98"9 ppm belong to floridoside. Especially the signals of the a-substituted anomeric
C-1 atom ofgalactose at 98.9 ppm and that of the C-2' atom of glycerol at 79.6 ppm are
very characteristic markers for this molecule. The peaks at 53.7 and 57.8 ppm are the
resonances of isethionic acid (2-hydroxyethane sulphonic acid). The spectra show a
strong increase in intracellular floridoside concentrations as well as a moderate rise in
isethionic acid contents as the salinity increases (Figure 2).
The effect of salinity on the intracellular floridoside concentrations in C. nipae are
presented in Figure 3. The floridoside content increased linearly 2.2-fold from about
300 mmol kg I dry wt at salinity 5 up to about 650 mmol k g - ' dry wt at salinity 70.
In Table 1 the floridoside concentrations of geographically different summer popu-
lations of C. nipae from the coastline of New South Wales are given. These isolates
contained floridoside values ranging from 402 to 887 mmol k g - ~ dry wt, which equals
about 10-23% of the dry weight. The culture material from Queensland, however,
revealed a significantly higher content of 1291 mmol floridoside k g - 1 dry wt. In this
isolate the heteroside contributed to one-third of the dry weight (Table 1).

Discussion
The intracellular floridoside concentration in C. nipae linearly increased with increasing
salinities, and hence has an important role in the osmotic acclimation (Figures 2 and 3).
The biological function of this heteroside as cellular osmoticum is further supported by
the high floridoside contents found in the field populations which ranged between 140
and 310 mmol k g - ~ fresh wt (Table 1). These values already equal osmotically
significant 215-477 m M on a cell water basis (tissue water content 65% of fresh wt). If
floridoside is exclusively located in the cytoplasm as suggested by Reed (1981), the
244 U. Karsten et al.

TABLE 1. The floridoside concentration (mean + SD; n=4) in different field popula-
tions of Catenella nipae from mangroves along the coastline of New South Wales,
Australia. The content of one culture sample isolated in Queensland, Australia is also
given for comparative purposes

Floridoside Floridoside
Nor Location and date (mmol kg i dry wt) (mmol kg i fresh wt) % Dry weight

I Port Macquarie, Settlement Point, 564.7 + 62.6 197.6 + 21.9 14.3 + 1.6
13 March 1993
2 Harrington, 887.1 + 45.2 310.5 + 15.8 22.5 + 1.I
13 March 1993
3 Tuncurry, 684.2 + 115.3 239.5 + 40-4 17.3 4- 2.9
13 March 1993
4 Salamander Bay, Port Stephens, 457.7 + 54.5 160.2 + 19.1 11-6 + 1-4
13 March 1993
5 Newcastle, Fullerton Cove, 731-7 + 89.4 256.1 + 31.3 18"5 + 2.3
13 March 1993
6 Newcastle, Stockton Bridge, 402.3 + 10.1 140.8 + 3.5 10.2 + 0.3
13 March 1993
7 Hawkesbury River, Sydney, 886-6 + 16.1 310.3 + 5"6 22.5 4- 0.4
14 March 1993
8 Minnamurra River, 677.5 + 27.7 237.1 + 9.7 17.2 ± 0'7
11 January 1993
9 Broughton Creek, Shoalhaven, 763-7 + 55.4 267.3 + 19-4 19.3 5- 1.4
11 January 1993
10 Moruya River, Garlandtown, 645.2 + 41-1 225.8 + 14"4 16'3 + 1"0
12 January 1993
11 Turlinjah, Tuross Lake, 704.6 + 50.0 246.6 + 17.5 17-8 + 1.3
12 January 1993
12 Wapengo Creek, 590.9±46.0 206-8± 16.1 15-0+ 1-2
13 January 1993
13 Nelson Lagoon, 533.3 ± 75.5 186.7 ± 26-4 13.5 + 1.9
13 January 1993
14 Pambula Lake, 588.3 ± 83.2 205.9 ± 29.1 14.9 ± 2.1
13 January 1993
Culture sample, Cowie Beach, Queensland, 1291.0 ± 108.6 451-9 ± 38.0 32.7 ± 2.8
13June 1987

"The numbers refer to those in Figure 1.

c o n c e n t r a t i o n o f this c o m p o u n d would increase even further. However, data on the

ultrastructure and the cytoplasmic/vacuolar v o l u m e ratios of Catenella are still l a c k i n g .
T h e role o f f l o r i d o s i d e as o r g a n i c o s m o l y t e w a s first d e m o n s t r a t e d b y ~4C i n c o r p o r a t i o n
s t u d i e s o n t h e r e d alga Porphyra perforata ( K a u s s , 1968). K a u s s s h o w e d t h a t t h e c o n t e n t s
o f this h e t e r o s i d e i n c r e a s e d m a r k e d l y w i t h i n c r e a s i n g salt t r e a t m e n t s o v e r t h e r a n g e
0 . 5 - 2 t i m e s s e a w a t e r c o n c e n t r a t i o n . T h e f u n c t i o n o f f l o r i d o s i d e as o s m o t i c u m h a s s i n c e
o f t h e B a n g i o p h y c i d a e : Bangia
b e e n i n v e s t i g a t e d f u r t h e r , p a r t i c u l a r l y in m e m b e r s
atropurpurea ( R e e d , 1985), Porphyra columbina ( K a r s t e n et al., 1993), Porphyra purpurea
( R e e d et al., 1980) a n d Porphyra umbilicalis ( W i e n c k e & I A u c h l i , 1981), a n d also in s o m e
F l o r i d e o p h y c i d e a e ( K i r s t & B i s s o n , 1979). A s in C. nipae, the f l o r i d o s i d e c o n c e n t r a t i o n
o f all t h e s e s p e c i e s v a r i e d as a f u n c t i o n o f t h e e x t e r n a l salinity.
W h i l e in e s t u a r i n e e n v i r o n m e n t s o f N e w S o u t h W a l e s s o m e Caloglossa s p e c i e s c a n b e
f o u n d o v e r a w i d e r a n g e o f salinities f r o m p e r m a n e n t f r e s h w a t e r c o n d i t i o n s u p to full
seawater concentrations (Karsten et al., 1992b), C. nipae g r o w s m a i n l y b e t w e e n salinities
10 a n d 35. H o w e v e r , Catenella a n d o t h e r i n t e r m i x e d m a n g r o v e r e d algae are n o t o n l y
 Effect of salinity on floridoside concentration 245

subjected to wide variations in external salt concentration due to the prevailing ebb and
flow of the tides and the freshwater runoff, but also due to rainfall and evaporation Which
may exert extreme stress conditions. T o cope with these salinity extremes the mangrove
algae carry out a metabolically active osmotic acclimation. T h e synthesis and accumu-
lation of floridoside in C. nipae is an important part of this process (Kirst, 1980, 1990).
T h e 13C-NMR spectra prove the presence of isethionic acid in extracts of C. nipae
(Figure 2). This metabolite was recently, and for the first time, identified as a m a j o r
anion in a plant: the marine red alga Ceramium flaccidum (Barrow et al., 1993). T h e
increase of the isethionic acid concentration with increasing salinities as well as the
chemical structure of this c o m p o u n d point to a potential osmoregulatory organic solute.
However, the size of the signals indicates moderate contents and hence isethionic acid
can play only a minor role in osmotic balance in C. nipae. Data on its metabolic
formation and the biological function of isethionic acid are lacking, as well as an
analytical method for precise quantification. Other populations of Catenella do not
always show the isethionic acid resonances, but often exhibit small peaks (inter alia)
broadened by coupling at 53-55 p p m (data not shown) that are characteristic of the
methylated amino functions of betaines (Blunden et al., 1986). It is unlikely that these
metabolites contribute to the osmotic acclimation of this species.
Besides the role as osmolyte, floridoside is thought to function as a comp/ltible solute
(Kirst, 1990). Compatible solute is a term for various low molecular weight organic
compounds of different chemical classes such as sugars (sucrose, trehalose), polyols,
amino acids (proline), quaternary a m m o n i u m compounds (glycine betaine, homarine),
and the tertiary sulphonium c o m p o u n d dimethylsulphoniopropionate (DMSP). These
substances have in c o m m o n macromolecular protective effects: protein function and
enzyme activity are adversely affected by increased electrolyte concentration and the
accumulation of compatible solutes permits the generation of low water potentials
without incurring metabolic damage (Kirst, 1990). T h e underlying mechanisms are
considered to be due to solute interactions between compatible solutes and the
biomolecules (Arakawa & Timasheff, 1985). Polyols, for example, are thought to act as
' water-like ' substances mimicking the water structure and thus maintaining an artificial
and stabilizing water sphere around proteins (Gekko & Morikawa, 1981). Such a
protective role can be assumed for floridoside. However, biochemical and physico-
chemical studies on this fimction are still missing mainly due to a lack of sufficient
quantity of purified floridoside.
Floridoside is the main photosynthetic product of m a n y Rhodophyta, and hence in
addition to the role as osmolyte and compatible solute it may also serve as a rapidly
available substrate for respiration coupled to the storage of fixed carbon. Especially in
the littoral zone of the mangroves C. nipae is often emersed, and consequently plants
experience strong gradients of salinity and long period of desiccation. Under such
extreme conditions the high concentrations of respiratory substrates, here floridoside,
may guarantee survival, because respiration is m u c h more resistant against elevated
salinities and desiccation than photosynthesis (Wiltens et al., 1978).
All field samples of C. nipae had much lower floridoside concentrations than the
culture material (Table 1). Similar results have been shown for the D-sorbitol and
D-dulcitol contents of various Bostrychia species both from field and culture (Karsten
et al., 1992a). All Bostrychia culture samples contained higher polyol concentrations than
algae from the field. T h e lower organic solute concentration in Catenella from the field is
rather puzzling in view of the greater osmotic stress and the long periods of desiccation
246 U. Karsten et al.

to which the organisms are subjected a n d the p r e s u m e d value o f floridoside in osmotic

acclimation. Perhaps floridoside a c c u m u l a t i o n in culture materials m a y simply b e due to
photoassimilate storage and occurs preferentially in stable abiotic culture conditions
u n d e r p e r m a n e n t immersion, which are m o r e suitable for photosynthesis a n d growth.
Catenella, very often intermixed with Bostrychia, Stictosiphonia a n d Caloglossa, is
characteristic of the m a n g r o v e habitat. It is instructive then to consider the steady-state
concentrations of the m a i n photosynthetic p r o d u c t in freshly collected materials, which
serve as osmolyte and c o m p a t i b l e solute. Field samples o f Bostrychia from various
geographical regions synthesize polyol concentrations ( D - s o r b i t o l plus D - d u l c i t o l )
between 50 and 400 m m o l kg i dry wt, while Caloglossa species p r o d u c e D - m a n n i t o l in
a similar o r d e r of m a g n i t u d e between 200 and 400 m m o l kg I dry wt (Karsten et al.,
1992a; W e s t et al., 1992). In field p o p u l a t i o n s o f C. nipae, however, the floridoside
contents are generally significantly higher b e t w e e n 400 a n d 880 m m o l kg ~ dry wt
(Table 1). It m a y be a s s u m e d that in e q u i m o l a r concentrations the polyols are b e t t e r a n d
m o r e efficient as osmolytes and c o m p a t i b l e solutes than floridoside due to the size and
structure of the molecules. While the floridoside molecule consists o f nine c a r b o n atoms,
the isomeric hexitols are smaller with six carbons only and hence are m u c h m o r e
' w a t e r - l i k e ' (Kirst, 1990). Borowitzka (1986, and references therein) argued that a
flexible, linear polyol which is c o m p l e t e l y r e d u c e d by the presence of - O H moieties
could ' m i m i c ' the structure o f the H - O H molecules in water, fitting into the structure
of the solvent, rather than relatively p e r t u r b i n g it, as ring-form sugars a n d heterosides
would do. Therefore, a p r o p o r t i o n a l l y higher heteroside c o n t e n t in Catenella as r e p o r t e d
in this study is necessary to reach a capacity similar to that of the polyhydric alcohols in
Bostrychia, Stictosiphonia and Caloglossa. The energy costs for the biosynthesis a n d
a c c u m u l a t i o n of floridoside are also higher than the hexitols. T h e ability o f Bostrychia,
Stictosiphonia and Caloglossa to p r o d u c e these unusual polyols which provide osmotic
protection m a y explain their a b u n d a n c e in the eulittoral zone of mangroves. In contrast,
the occurrence of Catenella in this habitat seems to be related to m u c h higher m e t a b o l i c
activities and energy investments for the p r o d u c t i o n and a c c u m u l a t i o n o f floridoside.
Nevertheless, species of this genus often form high a m o u n t s o f b i o m a s s in the m a n g r o v e s
of N e w South Wales, and thus contribute significantly to the p r i m a r y energy p r o d u c t i o n
of this ecosystem.

Acknowledgements
U l f Karsten thanks the D e u t s c h e F o r s c h u n g s g e m e i n s c h a f f for a generous p o s t - d o c t o r a l
fellowship. H e and Anika M o s t a e r t were also s u p p o r t e d by two grants from the Joyce W.
Vickery Scientific Research F u n d of the L i n n e a n Society of N e w S o u t h Wales, Australia.
T h e authors acknowledge the help of John A. West, University of California, Berkeley,
U.S.A. for providing culture samples, and the help of Irene D u n k e r a n d B r o n w y n
H o u l d e n for collecting C. nipae in the field.

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