Hydrobiologia 525: 139–155, 2004.

2004 Kluwer Academic Publishers. Printed in the Netherlands. 139

Light-related photosynthetic characteristics of lotic macroalgae

Orlando Necchi Jr
Departamento de Zoologia e Botânica, Universidade Estadual Paulista, Rua Cristóvão Colombo, 2265-
15054-000 São Jose´ do Rio Preto, SP, Brazil
(*Author for correspondence: Tel.: þ55-17-221-2406, Fax: þ55-17-221-2374, E-mail: orlando@dzb.ibilce.unesp.br)

Received 1 October 2003; in revised form 9 February 2004; accepted 10 February 2004

Key words: chlorophyll fluorescence, irradiance, lotic, macroalgae, oxygen evolution, photosynthesis

Abstract
Photosynthetic characteristics in response to irradiance were analysed in 42 populations of 33 macroalgal
species by two distinct techniques (chlorophyll fluorescence and oxygen evolution). Photosynthesis–irradi-
ance (PI) curves based on the two techniques indicated adaptations to low irradiance reflected by low
saturation values, high to moderate values of photosynthetic efficiency (a) and photoinhibition (b), for
Bacillariophyta and Rhodophyta, which suggests they are typically shade-adapted algae. In contrast, most
species of Chlorophyta were reported as sun adapted algae, characterized by high values of Ik and low of a,
and lack of or low photoinhibition. Cyanophyta and Xanthophyta were intermediate groups in terms of
light adaptations. Photoinhibition was observed in variable degrees in all algal groups, under field and
laboratory conditions, which confirms that it is not artificially induced by experimental conditions, but is
rather a common and natural phenomenon of the lotic macroalgae. Low values of compensation irradiance
(Ic) were found, which indicate that these algae can keep an autotrophic metabolism even under very low
irradiances. High ratios (>2) of photosynthesis/respiration were found in most algae, which indicates a
considerable net gain. These two physiological characteristics suggest that macroalgae may be important
primary producers in lotic ecosystems. Saturation parameters (Ik and Is) occurred in a relatively narrow
range of irradiances (100–400 lmol photons m)2 s)1), with some exceptions (higher in some filamentous
green algae or lower in red algae). These parameters were way below the irradiances measured at collecting
sites for most algae, which means that most of the available light energy was not photochemically converted
via photosynthesis. Acclimation to ambient PAR was observed, as revealed by lower values of Ik and Ic and
higher values of a and quantum yield in algae from shaded streams, and vice versa. Forms living within the
boundary layer (crusts) showed responses of shade-adapted species and had the highest values of Pmax, a and
quantum yield, whereas the opposite trend was observed in gelatinous forms (colonies and filaments). These
results suggests adaptation to the light regime rather than functional attributes related to the growth form.

Introduction

Photosynthesis responds both quantitatively and
qualitatively to changes in light and environmental
variation and potentially accounts for much of the
variation in the physiology, population growth
and community structure of benthic algae (Hill,
1996). Light affects algal growth directly via
photosynthesis or indirectly by non-photosyn-
thetic processes. The effect of light on physiologi-
cal characteristics and ecological distribution of
freshwater benthic algae remains a relevant issue.
Most investigations on the relationships of light
and freshwater benthic algae include the simulta-
neous analysis of temperature and irradiance, and
focus on specific groups or individual species of
140
freshwater macroalgae, such as reds (Kremer,
1983; Necchi and Zucchi, 2001), blue-greens
(Collins and Boylen, 1982; Howard-Williams
& Vincent, 1989) and filamentous green algae
(Graham et al., 1982, 1985, 1995, 1996; Ensminger
et al., 2000, 2001; Vieira & Necchi, 2003). Leukart
& Hanelt (1995) is the most comprehensive study
that deals with several macroalgal species and
groups including natural and culture populations.
Photosynthetic parameters derived from photo-
synthesis–irradiance (PI) curves have indicated
acclimation to the ambient light conditions. Plants
kept in culture have shown much lower satura-
tion points (Is, 24–67 lmol photons m)2 s)1), than
those collected from a stream (115–190 lmol
photons m)2 s)1). The same trend has been found
for the initial saturation parameter (Ik) with
lower values for plants in culture (12.5–29.4 lmol
photons m)2 s)1) in comparison to those under
natural conditions (13.3–32.5 lmol photons m)2
s)1). Other relevant studies on lotic algae refer to
periphytic communities, particularly biofilms,
essentially composed by microalgae (Boston &
Hill, 1991; Guasch & Sabater, 1995).
Despite the varied light regimes of benthic algae,
most PI studies indicate that Is occurs in a relatively
narrow range of irradiances (100–400 lmol pho-
tons m)2 s)1, Hill, 1996). However, in some fila-
mentous green algae, saturation occurs at high
irradiances (up to 2000 lmol photons m)2 s)1,
Graham et al., 1995; Ensminger et al., 2001),
whereas some freshwater red algae can reach
saturation at lower irradiances (20–70 lmol pho-
tons m)2 s)1, Leukart & Hanelt, 1995; Necchi &
Zucchi, 2001). Saturation irradiances are often
much higher than the typical irradiances measured
in situ, implying that photosynthesis may be
strongly light-limited under natural conditions
(Hill, 1996). However, this aspect has not been
adequately analysed, particularly in tropical lotic
macroalgae, that are exposed to high irradiances
(650–2000 lmol photons m)2 s)1, Necchi 1997;
Branco & Necchi, 1998; Necchi et al., 1999; Vieira
& Necchi, 2002). Other parameters from PI curves,
such as light compensation point (Ic) and photo-
inhibition have also been poorly investigated. For
instance, it is not clear whether benthic algae
exhibiting photoinhibition in their PI curves actu-
ally experience these inhibitory irradiances in situ
(Hill, 1996). In contrast, absence of photoinhibition
in laboratory PI measurements does not provide
unequivocal evidence that photoinhibition does not
occur. Ic has been scarcely reported in PI studies on
benthic algae, partly because respiration cannot be
directly measured by the 14C technique. Thus, fur-
ther research on light-related photosynthesis in
freshwater benthic algae is strongly needed.
Investigations using in vivo chlorophyll (chl)
fluorescence have proven to be a valuable tool for
in situ estimates of photosynthesis in macroalgae,
both marine (Häder et al., 1998; Beer et al., 2000;
Franklin & Badger, 2001) and freshwater (Ensm-
inger et al., 2000, 2001). However, chl fluorescence
and oxygen (O2) evolution derived photosynthetic
rates of freshwater macroalgae have rarely been
compared.
Despite the progress made by the previous
investigations cited above, information on photo-
synthetic responses to irradiance of lotic macro-
algae is restricted to a few species tested exclusively
under laboratory conditions. This study is carried
out to evaluate the photosynthetic responses to
irradiance of a comprehensive number and diver-
sity of lotic macroalgae using the techniques of chl
fluorescence and O2 evolution aiming at describing
the poorly studied parameters from PI curves in
terms of algal groups and morphological types.
Materials and methods
Forty-two field populations of 33 macroalgal
species were analysed in this study by in vivo chl
fluorescence, including all major groups repre-
sented in lotic ecosystems (Table 1). Ten of these
algae were also measured by the O2 evolution
technique. Populations were collected in five re-
gions from southeastern (Necchi et al., 2000) and
mid-western Brazil: AF – Atlantic Rainforest from
São Paulo State (23 21¢–23 34¢ S, 44 57¢–45
19¢ W); HW – hard water region from São Paulo
State (23 02¢–23 06¢ S, 47 48¢–48 07¢ W); NW –
northwest region of São Paulo State (20 11¢–20
49¢ S, 49 20¢–49 46¢ W); hard water (HW) from
Mato Grosso do Sul State (20 25¢–21 15¢ S, 56
28¢–56 43¢ W); a highland grass field (HG) from
Rio de Janeiro State (22 22¢–22 23¢ S, 44 41¢–44
44¢ W). The species encompass most of the mor-
phological types of lotic macroalgae (Sheath &
Cole, 1992): colony, crust, free filament, gelatinous
Table 1. Macroalgal species measured for chlorophyll fluorescence with indication of biome/region and selected environmental variables at the time of collection

Species Morphological Biome/region Temperature (C) Irradiance Current

type (lmol photons m)2 s)1) velocity
(cm s)1)

Cyanophyta
Blennothirx ganeshii Wat. et Kom. MA HW 23.3 ± 1.3 300b ± 190 26 ± 10
Geitlerinema splendida (Gom.) Anagn. – population 1a MA NW 19.8 ± 0.9 1655 ± 170 27 ± 9
Geitlerinema splendida (Gom.) Anagn. – population 2 MA AF 20.0 ± 0.8 145c ± 90 10 ± 5
Nostochopsis lobatus Born. et Flah. GC AF 19.3 ± 0.6 120 ± 75 30 ± 6
Microcoleus subtorulosus Gom. MA AF 19.3 ± 0.6 120 ± 75 30 ± 6
Phormidium aerugineo-caeruleum (Gom.) Anagn. et MA AF 17.5 ± 0.8 410c ± 165 78 ± 15
Kom.
Stigonema robustum Gardn. FF HG 11.7 ± 0.7 – 44 ± 11

Bacillariophyta
Fragilaria ulna (Nitsch) Lange-Bert. CO NW 23.8 ± 1.8 895b ± 255 23 ± 6
Gomphonema sp./Fragilaria ulna CO AF 17.5 ± 0.8 410c ± 165 78 ± 15
Terpsinoe musica Ehr.a CO NW 23.5 ± 1.1 1420 ± 140 14 ± 10

Chlorophyta
Chaetophora elegans (Roth) C. Ag. GC NW 21.5 ± 1.1 1510 ± 195 14 ± 4
Chara sp. FF HW 23.3 ± 1.3 300b ± 190 26 ± 10
Cladophora glomerata (L.) Kütz. – population 1a FF NW 25.3 ± 1.4 920b ± 140 25 ± 5
Cladophora glomerata (L.) Kütz. – population 2 FF HW 21.8 ± 0.9 105b ± 9 73 ± 13
Cladophora glomerata (L.) Kütz. – population 3 FF HW 21.3 ± 0.8 560 ± 70 14 ± 4
Draparnaldia mutabilis (Roth) Bory GF HG 18.2 ± 0.6 – 10 ± 3
Ecballocystis pulvinata Bohl. CR AF 19.1 ± 0.8 230c ± 45 89 ± 22
Nitella cernua Br. FF NW 23.8 ± 1.8 895b ± 255 23 ± 6
Nitella furcata (Bruz.) C. Ag. var. sieberi (Br.) FF NW 19.8 ± 1.9 1055 ± 155 35 ± 7
Wood – population 1a
N. furcata (Bruz.) C. Ag. var. sieberi (Br.) FF NW 21.3 ± 0.8 560 ± 70 14 ± 4
Wood – population 2
Rhizoclonium hieroglyphicum (C. Ag) FF NW 25.3 ± 1.4 920b ± 140 25 ± 5
a
Kütz. – population 1
Rhizoclonium hieroglyphicum (C. Ag) Kütz. – FF HW 22.1 ± 1.5 105c ± 25 12 ± 5
population 2
Schizochlamys gelatinosa Br. GC NW 27.1 ± 1.7 1750 ± 250 14 ± 3

Continued on p. 142
141
 142
Table 1. (Continued)

Species Morphological Biome/region Temperature (C) Irradiance Current

type (lmol photons m)2 s)1) velocity
(cm s)1)

Schizomeris leibleinii Kütz. FF NW 22.8 ± 1.1 1005b ± 140 76 ± 12

Spirogyra sp. – population 1a FF NW 23.5 ± 1.2 935 ± 115 25 ± 5

Spirogyra sp. – population 2 FF HW 22.5 ± 1.5 1500 ± 175 8±5
Stigeoclonium helveticum Visch. – population 1 TU NW 22.8 ± 1.1 1005b ± 140 76 ± 12
Stigeoclonium helveticum Visch. – population 2 TU NW 21.1 ± 1.5 1655 ± 255 27 ± 12
Tetraspora gelatinosa (Vauch.) Desv. GC HG 18.2 ± 0.6 – 10 ± 3

Rhodophyta
Audouinella eugenea (Skuja) Jao TU HW 21.2 ± 1.2 1050 ± 125 13 ± 6
Batrachospermum atrum (Huds.) Harv. GF HG 18.2 ± 0.6 – 10 ± 3
B. delicatulum (Skuja) Necchi et Entw.a GF NW 21.5 ± 1.1 1510 ± 195 14 ± 4
B. globosporum Isr. GF HW 21.9 ± 1.4 1300 ± 130 17 ± 5
B. macrosporum Mont. GF AF 20.0 ± 0.8 145c ± 90 10 ± 5
a
Compsopogon coeruleus (C. Ag.) Mont. FF NW 23.5 ± 1.6 770 ± 180 14 ± 8
Hildenbrandia angolensis West et West CR AF 19.3 ± 0.6 120 ± 75 30 ± 6
Thorea hispida (Thore) Desv.a GF HW 21.8 ± 0.9 105b ± 9 73 ± 13

Xanthophyta
Vaucheria fontinalis (L.) Christ.a MA NW 23.5 ± 1.1 1420 ± 140 14 ± 10
Vaucheria sp. (sterile) – population 1 MA AF 17.5 ± 0.8 410c ± 165 78 ± 15
Vaucheria sp. (sterile) – population 2 MA AF 19.2 ± 1.5 155c ± 10 66 ± 11
Vaucheria sp. (sterile) – population 3 MA HW 23.3 ± 1.3 300b ± 190 26 ± 10
Vaucheria sp. (sterile) – population 4 MA HW 21.3 ± 0.8 560 ± 70 14 ± 4

Data are expressed as mean ± standard deviation (n = 5) and represent repeated measurements at noon ±2 h in the sampling dates. Biome/region abbreviations (see Materials
and methods for details): AF – Atlantic Rainforest; HG – highland grassfield; HW – hard water region; NW – northwest region. Morphological types abbreviations: CO –
colony; CR – crust; FF – free filament; GC – gelatinous colony; GF – gelatinous filament; MA – mat; TU – tuft.
a
Algae also measured for oxygen evolution.
b
Cloudy or partly cloudy.
c
Overcast.

colony, gelatinous filament, mat and tuft. Mea-
surements were made from field populations, that
were collected or measured (noon ± 2 h) during
the typical period of highest abundance in this
region (May to October, Necchi & Pascoaloto,
1993). Measurements of irradiance, temperature
and current velocity were taken close to the algal
thalli (Necchi, 1997; Necchi et al., 1999).
Experiments by O2 evolution followed the
general procedures described in previous studies
(Necchi & Zucchi, 2001; Vieira & Necchi, 2003).
Photosynthesis and dark respiration rates were
determined by changes in O2 concentration using
the light and dark bottle technique (Littler &
Arnold, 1985; Thomas, 1988). Initial and final O2
concentrations of incubated samples were mea-
sured with an O2 meter (Yellow Springs Instru-
ments, model 5000), equipped with a self-stirring
probe, and calculations were made according to
the formulas provided by Littler & Arnold (1985).
Incubations were made with orbital agitation
(100 ± 5 rpm) and digital temperature control.
Frontal illumination was supplied by one to three
cool-white fluorescent lamps (Osram 15 W).
Plants were incubated in 100 mL borosilicate glass
bottles (98.5% transparency). Dark bottles were
covered with thick black plastic. In order to pre-
vent inorganic carbon depletion during incuba-
tions, culture medium or stream water were
supplied three times with 2 mM NaHCO3 (1 mL/
100 mL).
Photosynthesis–irradiance (PI) curves were
made under constant temperature (20 ± 0.5 C)
using eight increasing irradiance levels within the
range of 0–425 lmol photons m)2 s)1. These are
within the saturation ranges previously reported
for freshwater macroalgae (Leukart & Hanelt,
1995; Hill, 1996). An additional irradiance
(935 lmol photons m)2 s)1, achieved by addition of
one PL fluorescent lamp, Phyllips 30 W) was
measured for some filamentous green algae (e.g.
Cladophora and Spirogyra) with high irradiance
requirements (Graham et al., 1995; Ensminger
et al., 2001). Incubation intervals were of 30 min
for each irradiance level. Parameters from the PI
curves were calculated by the equation proposed
by Platt et al. (1980), as suggested by Henley
(1993), that includes a photoinhibition parameter
because most algae measured in previous studies
exhibited photoinhibition (Necchi & Zucchi, 2001;
143
Vieira & Necchi, 2003). PI curve for one fresh-
water red algal species (Thorea hispida) was pub-
lished in a previous study (Necchi & Zucchi, 2001)
and was incorporated in this analysis.
Measurements of chl fluorescence were per-
formed using a Diving-PAM underwater fluo-
rometer (Walz, Effeltrich, Germany). Apices or
entire algal thalli were placed directly on the tip of
the fluorometer fibreoptic using the supplied
magnet sample holder. Rapid light curves (White
& Critchley, 1999) consisted of the fluorescence
responses to eight increasing irradiance levels
within the range of 0–690 lmol photons m)2 s)1,
using the ‘light curve’ option of the Diving-PAM.
This device used a halogen lamp to provide actinic
and saturating-pulse light. The exposure time at
each irradiance was 15 s, each separated by a 0.8 s
saturating flash (
6000 lmol photons m)2 s)1).
The illumination periods of rapid light curves are
too short to achieve true steady states but provide
sound information on the overall photosynthetic
performance of a plant (White & Critchley, 1999).
Two main parameters were determined from each
sample: (1) effective quantum yield of photosystem
II (PSII), DF/Fm0 , where: DF ¼ Fm0 )Ft; Fm0 is
the maximal fluorescence of an illuminated sam-
ple; Ft – the transient fluorescence (Schreiber et al.,
1994); (2) relative electron transport rate (rETR).
As the amount of absorbed irradiance by PSII in
an optical cross section (generally assumed as
0.84), could not be measured for each alga, rETR
was calculated as DF/Fm0 · PAR · 0.5 (according to
Kromkamp et al., 1998), where PAR is the actinic
irradiance in lmol photons m)2 s)1; 0.5 is a multi-
plication factor (not used by Kromkamp et al.,
1998), because the transport of a single electron
requires the absorption of two quanta. The cal-
culations and terminology followed, respectively,
Schreiber et al. (1994) and van Kooten & Snel
(1990). PI curves were generated on the basis of
rETR and the respective parameters were calcu-
lated by the equation of Platt et al. (1980):
photosynthetic efficiency (aETR), Pmax (rETRmax),
saturation parameter (Ik) and photoinhibition
parameter (bETR). The values of aETR were
determined by linear fitting using the three first
points of the rETR vs. irradiance curve (Conde-
Álvarez et al., 2002).
Data were analysed using one way analysis
of variance (ANOVA), followed by a multiple
144
comparison Newman–Keuls test (Zar, 1999) to
test for significant differences (p < 0.05) in pho-
tosynthetic parameters among the species/popu-
lations, morphological types and algal groups that
were measured using the chl fluorescence and O2
evolution techniques. Relationships among pho-
tosynthetic parameters were evaluated with the
Pearson moment-product correlation coefficient
(Zar, 1999). Statistical tests were performed by
Statsoft Statistica 6.0 software, whereas graphs
and calculations from PI curve parameters were
made by Microcal Origin 5.0.
Results
PI curves based on chl fluorescence (Table 2, Figs
1–3) showed down-regulation of rETR, as indi-
cated by increase in the parameter b under higher
irradiances, in 37% of the species/populations
of Chlorophyta, 57% of Cyanophyta, 60% of
Xanthophyta and 100% of Bacilariophyta and
Rhodophyta. The extreme values were observed in
Chlorophyta species: the highest (b  )0.48) for
two species from organically polluted streams
(Schizomeris leibleinii and Stigeoclonium helveti-
cum) and the lowest (b  0.17) in gelatinous
(Chaetophora and Draparnaldia) or free filamen-
tous forms (Cladophora and Spirogyra). Results of
ANOVA and Newman–Keuls test indicated the
following increasing order of photoinhibition
among algal divisions (Table 3): Rhodophyta
b Bacillariophyta  Cyanophyta  Xan-
thophyta > Chlorophyta. In terms of morpholog-
ical types (Table 4), the highest values of
photoinhibition were found in tufts and colonies
and the lowest in gelatinous colonies. b was posi-
tively correlated (p < 0.001) with Ik (r ¼ 0.81) and
Pmax (r ¼ 0.64).
The lowest values of Pmax (rETR < 12.5) were
observed in species of three different groups (Ta-
ble 2, Figs 1–3, Cyanophyta, Chlorophyta and
Rhodophyta), as well as the highest values (rE-
TR > 70, Cyanophyta, Chlorophyta and Xan-
thophyta). Three groups of algal divisions were
distinguished for Pmax (Table 3): Rhodophyta and
Chlorophyta with the lowest and highest values,
respectively, and Cyanophyta with medium values;
the remaining groups were in intermediate posi-
tions (Table 3). Crusts and free filaments had sig-
nificant higher values of Pmax than the other
morphological types (Table 4). Pmax was positively
correlated with Ik (r ¼ 0.62, p < 0.001) and DF/Fm0
(r ¼ 0.35, p < 0.05).
Values of Ik were mostly associated to the
irradiance in the collecting sites: the lowest values
(<100 lmol photons m)2 s)1) were observed in al-
gae collected in shaded streams, whereas the
highest (>200 lmol photons m)2 s)1) occurred in
species/populations under high irradiances (Tables
1 and 2); however, several species were situated in
an intermediate group (100–200 lmol m)2 s)1) and
did not reveal this trend and led to a lack of sig-
nificant correlation of Ik with irradiance. 74% of Ik
values (Table 2) fall way below (<half) of the
ambient PAR measured at the time of collections
(Table 1). The saturation values (Is), indicated by
the stabilization of the curves after reaching
maximum rETR values, were mostly also below
the ambient irradiances (£400 lmol photons
m)2 s)1) for most species/populations (Figs 1–3).
DF/Fm0 mostly reflected the light conditions of
the collecting sites as well, with the highest values
for algae from sites with low irradiances and the
lowest for those from open stream segments.
However, there was no significant correlation of
DF/Fm0 with irradiance, mostly due to a large
number of species with intermediate values and
also to distinct values of species collected under
similar irradiances. DF/Fm0 was negatively corre-
lated with Ik (r ¼ )0.35, p < 0.05). Photosynthetic
efficiency ranged from very low values (a £ 10) in
some species of Cyanophyta, Chlorophyta and
Rhodophyta to the highest values (a  30) in one
species each of Cyanophyta and Rhodophyta
(Table 2). a was positively correlated to DF/Fm0
(r ¼ 0.41, p < 0.01) and negatively to irradiance
(r ¼ )0.39, p < 0.01). Only Xanthophyta had sig-
nificantly higher values of a than the other groups
(Table 3).
A comparative analysis of the photosynthetic
parameters for algal divisions (Table 3) showed the
lowest values of Pmax and Ik (23.1 rETR and 121.8
lmol photons m)2 s)1) and the highest of b ()0.15
rETR) in the Rhodophyta, whereas the Chloro-
phyta had the opposite trend (47.9, 244.5 and
0.03). The parameters for morphological types
revealed the following trends (Table 4): (1) signif-
icantly different values of Pmax, a and DF/Fm0 with
the highest values in crusts (50.3, 0.28 and 0.76)
Table 2. Parameters of the photosynthesis versus irradiance curves of the macroalgal species measured for chlorophyll fluorescence

Speciesa Pmax (rETR) Ik (lmol photons m)2 s)1) Effective quantum a (rETR) b (rETR)
yield (DF/Fm0 )

Cyanophyta
Blennothirx ganeshii 43.4 ± 1.2 227.2 ± 15.4 0.54 ± 0.04 0.19 ± 0.01 0.10 ± 0.03
Geitlerinema splendida – population 1 9.1 ± 2.3 125.5 ± 48.3 0.30 ± 0.07 0.08 ± 0.01 )0.11 ± 0.06
Geitlerinema splendida – population 2 16.7 ± 0.4 74.0 ± 5.2 0.85 ± 0.06 0.23 ± 0.02 )0.22 ± 0.02
Nostochopsis lobatus 39.8 ± 5.9 163.5 ± 12.2 0.74 ± 0.17 0.25 ± 0.05 )0.07 ± 0.04
Microcoleus subtorulosus 73.8 ± 7.2 228.2 ± 19.1 0.92 ± 0.06 0.32 ± 0.02 0.09 ± 0.10
Phormidium aerugineo-caeruleum 37.7 ± 2.9 136.5 ± 13.1 0.79 ± 0.04 0.28 ± 0.02 )0.15 ± 0.07
Stigonema robustum 34.8 ± 4.1 255.8 ± 61.8 0.56 ± 0.06 0.14 ± 0.02 0.01 ± 0.12

Bacillariophyta
Fragilaria ulna 17.2 ± 0.5 80.5 ± 9.9 0.72 ± 0.06 0.22 ± 0.03 )0.14 ± 0.03
Gomphonema sp./Fragilaria ulna 34.3 ± 2.0 159.3 ± 18.9 0.58 ± 0.01 0.20 ± 0.01 )0.11 ± 0.06
Terpsinoe musica 28.9 ± 6.1 99.7 ± 2.0 0.76 ± 0.01 0.24 ± 0.01 )0.14 ± 0.02

Chlorophyta
Chaetophora elegans 30.1 ± 4.0 358.7 ± 20.3 0.29 ± 0.03 0.10 ± 0.04 0.28 ± 0.12
Chara sp. 27.4 ± 1.8 117.4 ± 6.8 0.64 ± 0.04 0.23 ± 0.01 )0.18 ± 0.07
Cladophora glomerata – population 1 50.6 ± 0.8 231.1 ± 19.6 0.67 ± 0.03 0.22 ± 0.02 0.13 ± 0.01
Cladophora glomerata – population 2 51.2 ± 2.8 223.4 ± 12.0 0.62 ± 0.05 0.23 ± 0.02 0.09 ± 0.06
Cladophora glomerata – population 3 73.4 ± 3.2 282.4 ± 8.9 0.67 ± 0.05 0.26 ± 0.01 0.28 ± 0.04
Draparnaldia mutabilis 49.4 ± 16.1 452.2 ± 87.2 0.38 ± 0.03 0.12 ± 0.01 0.29 ± 0.10
Ecballocystis pulvinata 60.9 ± 3.0 250.5 ± 23.8 0.63 ± 0.03 0.24 ± 0.02 0.02 ± 0.05
Nitella cernua 83.9 ± 4.9 317.2 ± 32.8 0.66 ± 0.02 0.27 ± 0.02 )0.04 ± 0.06
Nitella furcata var. sieberi – population 1 48.0 ± 2.9 171.4 ± 16.0 0.76 ± 0.03 0.28 ± 0.01 )0.08 ± 0.06
Nitella furcata var. sieberi – population 2 40.4 ± 4.0 177.0 ± 18.0 0.62 ± 0.04 0.23 ± 0.02 )0.13 ± 0.09
Rhizoclonium hieroglyphicum – population 1 54.0 ± 4.1 226.4 ± 7.3 0.69 ± 0.04 0.24 ± 0.02 0.09 ± 0.07
Rhizoclonium hieroglyphicum – population 2 50.3 ± 3.0 194.8 ± 14.8 0.72 ± 0.02 0.26 ± 0.01 0.07 ± 0.06
Schizochlamys gelatinosa 31.0 ± 0.9 179.6 ± 8.5 0.60 ± 0.01 0.17 ± 0.01 )0.04 ± 0.03
Schizomeris leibleinii 12.3 ± 0.8 135.9 ± 16.2 0.35 ± 0.05 0.08 ± 0.03 )0.53 ± 0.08
Spirogyra sp. – population 1 76.4 ± 3.4 312.6 ± 19.2 0.75 ± 0.02 0.24 ± 0.01 0.20 ± 0.04
Spirogyra sp. – population 2 70.3 ± 4.2 305.4 ± 33.9 0.60 ± 0.08 0.23 ± 0.03 0.17 ± 0.06
Stigeoclonium helveticum – population 1 20.5 ± 1.2 99.1 ± 2.4 0.64 ± 0.02 0.21 ± 0.01 )0.48 ± 0.06
Stigeoclonium helveticum – population 2 51.3 ± 5.3 233.2 ± 24.6 0.47 ± 0.04 0.22 ± 0.00 0.10 ± 0.10
Tetraspora gelatinosa 24.0 ± 2.2 349.8 ± 49.4 0.32 ± 0.04 0.07 ± 0.01 0.15 ± 0.09
145

Continued on p. 146
 146

Table 2. (Continued)

Speciesa Pmax (rETR) Ik (lmol Effective quantum a (rETR) b (rETR)

photons m)2 s)1) yield (DF/Fm0 )

Rhodophyta
Audouinella eugenea 19.5 ± 0.9 227.2 ± 15.4 0.54 ± 0.04 0.15 ± 0.01 )0.11 ± 0.04
Batrachospermum atrum 12.2 ± 1.3 131.4 ± 27.5 0.27 ± 0.05 0.10 ± 0.02 )0.19 ± 0.11
B. delicatulum 30.6 ± 3.2 131.3 ± 6.6 0.69 ± 0.09 0.22 ± 0.03 )0.12 ± 0.11
B. globosporum 18.9 ± 1.2 118.6 ± 7.0 0.57 ± 0.06 0.16 ± 0.01 )0.12 ± 0.04
B. macrosporum 20.3 ± 2.6 85.0 ± 4.5 0.78 ± 0.03 0.24 ± 0.02 )0.22 ± 0.12
Compsopogon coeruleus 17.0 ± 1.2 103.7 ± 12.0 0.57 ± 0.04 0.16 ± 0.01 )0.16 ± 0.07
Hildenbrandia angolensis 40.2 ± 1.1 127.8 ± 4.6 0.88 ± 0.03 0.31 ± 0.02 )0.14 ± 0.03
Thorea hispida 24.7 ± 1.3 134.2 ± 10.9 0.61 ± 0.01 0.18 ± 0.01 )0.10 ± 0.06

Xanthophyta
Vaucheria fontinalis 28.4 ± 0.2 161.2 ± 3.9 0.70 ± 0.06 0.18 ± 0.01 )0.07 ± 0.01
Vaucheria sp. – population 1 37.7 ± 2.9 136.4 ± 13.0 0.79 ± 0.04 0.28 ± 0.02 )0.15 ± 0.07
Vaucheria sp. – population 2 33.1 ± 1.6 118.9 ± 7.3 0.78 ± 0.02 0.28 ± 0.01 )0.13 ± 0.05
Vaucheria sp. – population 3 51.4 ± 3.5 241.6 ± 31.2 0.63 ± 0.04 0.21 ± 0.02 0.08 ± 0.06
Vaucheria sp. – population 4 73.9 ± 4.1 267.1 ± 18.9 0.75 ± 0.02 0.28 ± 0.01 0.05 ± 0.05

Data are expressed as means ± standard deviations (n = 5).

a
According to Table 1.
 147

Cyanophyta
90 90
Blennothrix ganeshii Geitlerinema splendida (population 1)
80 80

70 70

60 60

50 50
rETR

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

90 90
Microcoleus subtorulosus Nostochopsis lobatus
80 80

70 70

60 60
rETR

50 50

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700
Irradiance (µmol m-2 s-1) Irradiance (µmol m-2 s-1)

Bacillariophyta
90 90
Fragilaria ulna Terpsinoe musica
80 80

70 70

60 60

50 50
rETR

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700
Irradiance (µmol m-2 s-1) Irradiance (µmol m-2 s-1)
Figure 1. Representative photosynthesis–irradiance curves for lotic macroalge (Cyanophyta and Bacillariophyta) based on data of
chlorophyll fluorescence. Bars indicate ±SD (n ¼ 5).

and the lowest in gelatinous colonies and filaments PI curves based on O2 evolution (Table 5,
(26.0–31.2, 0.15–0.17 and 0.49–0.55); (2) similar Fig. 4) revealed the following general trends: (1)
values of Ik among all types (158.5–257.9), except the values of Pmax and gross photosynthesis (GP)
in colonies (116.7). were low to moderate in all species, except in two
148

Chlorophyta
90 90
Chaetophora elegans Cladophora glomerata
80 80
70 70
60 60
rETR

50 50
40 40
30 30
20 20
10 10
0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

90 90
Nitella cernua Rhizoclonium hieroglyphicum
80 80
70 70
60 60
50 50
rETR

40 40
30 30
20 20
10 10
0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

90 90
Schizochlamys gelatinosa Schizomeris leibleinii
80 80
70 70
60 60
rETR

50 50
40 40
30 30
20 20
10 10
0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

90 90
Spirogyra sp. Stigeoclonium helveticum (population 2)
80 80
70 70
60 60
rETR

50 50
40 40
30 30
20 20
10 10
0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

Irradiance (µmol m-2 s-1) Irradiance (µmol m-2 s-1)

Figure 2. Representative photosynthesis–irradiance curves for lotic macroalge (Chlorophyta) based on data of chlorophyll fluores-
cence. Bars indicate ±SD (n ¼ 5).

species of Chlorophyta; (2) Ic values were low values were low to very low (<150 lmol
(£20 lmol photons m)2 s)1) in all species measured, photons m)2 s)1) in Bacillariophyta, Cyanophyta
except in Rhyzoclonium (Chlorophyta); (3) Ik and Rhodophyta (except in Thorea), whereas in
 149

Rhodophyta
90 90
Batrachospermum atrum Batrachospermum delicatulum
80 80

70 70

60 60

50 50
rETR

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

90 90
Hildenbrandia angolensis Thorea hispida
80 80

70 70

60 60

50 50
rETR

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

Irradiance (µmol m s ) -2 -1
Irradiance (µmol m s )-2 -1

Xanthophyta
90 90
Vaucheria fontinalis Vaucheria sp.
80 80

70 70

60 60

50 50
rETR

40 40

30 30

20 20

10 10

0 0
0 100 200 300 400 500 600 700 0 100 200 300 400 500 600 700

Irradiance (µmol m s ) -2 -1 Irradiance (µmol m s )-2 -1

Figure 3. Representative photosynthesis–irradiance curves for lotic macroalge (Rhodophyta and Xanthophyta) based on data of
chlorophyll fluorescence. Bars indicate ±SD (n ¼ 5).

Chlorophyta and Xanthophyta they were high to values (Table 2) fall way below (<half) of the
very high (>200 lmol photons m)2 s)1); 70% of Ik ambient PAR (Table 1), as well as the saturation
150

Table 3. Parameters of the photosynthesis vs. irradiance curves of the macroalgal divisions measured for chlorophyll fluorescence

Divisions Pmax (rETR) Ik Effective quantum a (rETR) b (rETR)

(lmol photons m)2 s)1) yield (DF/Fm0 )

Cyanophyta (n = 30) 36.2 ± 18.7 (b) 172.7 ± 68.9 (b) 0.67 ± 0.22 (bc) 0.21 ± 0.08 (a) )0.05 ± 0.13 (bc)
Bacillariophyta (n = 15) 27.4 ± 8.1 (ab) 116.7 ± 37.9 (a) 0.68 ± 0.09 (bc) 0.22 ± 0.02 (a) )0.13 ± 0.04 (ab)
Chlorophyta (n = 85) 47.9 ± 19.9 (c) 244.5 ± 91.6 (c) 0.58 ± 0.15 (a) 0.21 ± 0.07 (a) 0.03 ± 0.23 (c)
Rhodophyta (n = 35) 23.1 ± 8.5 (a) 121.8 ± 21.6 (a) 0.62 ± 0.18 (b) 0.19 ± 0.07 (a) )0.15 ± 0.08 (a)
Xanthophyta (n = 25) 45.6 ± 16.9 (bc) 186.0 ± 63.2 (b) 0.73 ± 0.07 (c) 0.25 ± 0.04 (b) )0.04 ± 0.11 (bc)

Data are expressed as means ± standard deviations. Distinct letters indicate significant differences (p < 0.05) by Newman–Keuls test.

Table 4. Parameters of the photosynthesis vs. irradiance curves of the macroalgal morphological types measured for chlorophyll
fluorescence

Morphological types Pmax (rETR) Ik Effective a (rETR) b (rETR)

(lmol photons m)2 s)1) quantum yield
(DF/Fm0 )

Colony (n = 15) 27.4 ± 8.1 (a) 116.7 ± 37.9 (a) 0.68 ± 0.09 (c) 0.22 ± 0.02 (b) )0.13 ± 0.04 (a)
Crust (n = 10) 50.6 ± 11.1 (b) 189.1 ± 66.6 (b) 0.76 ± 0.14 (c) 0.28 ± 0.04 (c) )0.06 ± 0.09 (ab)
Free filament (n = 75) 48.5 ± 20.9 (b) 221.1 ± 71.8 (b) 0.63 ± 0.11 (b) 0.22 ± 0.06 (b) )0.01 ± 0.21 (b)
Gelatinous colony (n = 20) 31.2 ± 6.7 (a) 257.9 ± 97.2 (b) 0.49 ± 0.21 (a) 0.15 ± 0.08 (a) 0.13 ± 0.16 (c)
Gelatinous filament (n = 30) 26.0 ± 13.5 (a) 176.6 ± 131.4 (b) 0.55 ± 0.18 (a) 0.17 ± 0.06 (a) )0.08 ± 0.19 (a)
Mat (n = 25) 40.7 ± 20.2 (a) 171.7 ± 65.5 (b) 0.70 ± 0.18 (c) 0.23 ± 0.07 (b) )0.05 ± 0.13 (b)
Tuft (n = 15) 31.2 ± 15.9 (a) 158.5 ± 61.0 (b) 0.55 ± 0.08 (a) 0.19 ± 0.03 (ab) )0.16 ± 0.25 (a)

Data are expressed as means ± standard deviations. Distinct letters indicate significant differences (p < 0.05) by Newman–Keuls test.

values (£200 lmol photons m)2 s)1) for most spe-
cies/populations (Fig. 4); (4) P/R ratios were rela-
tively high (>2) in most algae measured; (5)
photoinhibition was observed in all algae mea-
sured, except in some species of Chlorophyta.
Among the photosynthetic parameters, a was
positively correlated with b (r ¼ 0.71, p < 0.05)
and no significant correlations were found of
irradiance (Table 1) with photosynthetic parame-
ters (Table 5). However, this could be misleading
due to the fact that relatively few species/popula-
tions were analysed.
Discussion
Adaptations to low irradiance were consistently
observed for Bacillariophyta and Rhodophyta in
this study from data based on chl fluorescence and
O2 evolution techniques. These adaptations were
basically reflected by low saturation values, high to
moderate values of photosynthetic efficiency and
the occurrence of photoinhibition. Thus, available
information suggests that these algae are typically
shade-adapted plants. The freshwater red algae
have already been indicated as shade adapted in
previous studies (Leukart & Hanelt, 1995; Necchi
& Zucchi, 2001). PI curves have also shown similar
conditions in periphytic communities of shaded
streams dominated by diatoms (Boston & Hill,
1991; Guash & Sabater, 1995). In contrast, most
species of Chlorophyta are here reported as sun-
adapted algae, characterized by high and low
values of Ik and a, respectively, and lack of or low
levels of photoinhibition, consistent with previous
investigations (Graham et al., 1982, 1985, 1995,
1996; Ensminger et al., 2000, 2001). Cyanophyta
and Xanthophyta can be considered intermediate
groups in terms of light adaptations, with no clear
trends of photosynthetic parameters to low or high
Table 5. Parameters of the photosynthesis versus irradiance curves of the macroalgal species measured for oxygen evolution

Speciesa Pmax GP Ic Ik a b P/R

Cyanophyta
Geitlerinema splendida 2.8 ± 2.3 (b) 3.3 ± 0.6 (a) 3.2 ± 1.7 (ab) 37.6 ± 29.6 (a) 0.09 ± 0.09(bc) )0.17 ± 0.14(a) 4.7 ± 1.1(d)

Bacillariophyta
Terpsinoe musica 2.0 ± 0.2 (a) 3.9 ± 0.2 (a) 16.7 ± 4.7 (d) 45.8 ± 11.6 (a) 0.05 ± 0.01(b) )0.08 ± 0.09(a) 1.0 ± 0.1(a)

Chlorophyta
Cladophora glomerata 5.3 ± 0.6 (c) 7.1 ± 0.6 (b) 5.9 ± 2.5 (b) 196.1 ± 67.6 (bc) 0.02 ± 0.01 (a) 0.13 ± 0.11(bc) 2.9 ± 0.3(c)
Nitella furcata var. sieberi 35.5 ± 1.5 (f) 41.5 ± 1.5 (e) 1.9 ± 0.1 (a) 378. 4 ± 32.1 (d) 0.10 ± 0.01 (c) )0.14 ± 0.04(a) 5.9 ± 0.2(d)
Rhizoclonium hieroglyphicum 6.4 ± 0.7 (d) 13.9 ± 0.7 (d) 36.6 ± 19.9 (d) 397.0 ± 87.3 (d) 0.02 ± 0.01 (a) 0.09 ± 0.05(b) 0.9 ± 0.1(a)
Spirogyra sp. 31.2 ± 3.9 (f) 40.7 ± 3.9 (e) 10.3 ± 1.5 (c) 1776.5 ± 832.4 (e) 0.02 ± 0.01 (a) 0.20 ± 0.02(c) 3.3 ± 0.4(c)

Rhodophyta
Batrachospermum delicatulum 5.4 ± 0.6 (c) 11.4 ± 0.5 (c) 19.9 ± 1.6 (d) 136.4 ± 41.6 (b) 0.04 ± 0.01 (b) )0.08 ± 0.02(a) 0.9 ± 0.1(a)
Compsopogon coeruleus 4.8 ± 0.8 (c) 8.1 ± 0.8 (bc) 5.1 ± 1.3 (b) 46.0 ± 21.5 (a) 0.12 ± 0.04 (c) )0.17 ± 0.10(a) 1.5 ± 0.2(b)
Thorea hispida 11.3 ± 1.4 (e) 15.2 ± 1.4 (d) 6.0 ± 1.6 (b) 224.7 ± 18.1 (c) 0.05 ± 0.01 (b) )0.10 ± 0.07(a) 2.9 ± 0.4(c)

Xanthophyta
Vaucheria fontinalis 7.7 ± 1.0 (d) 10.1 ± 2.0 (c) 23.2 ± 7.2 (d) 844.4 ± 364.2 (e) 0.01 ± 0.00 (a) )0.10 ± 0.23(a) 3.2 ± 0.8(c)
)1 )1
Data (means ± standard deviations, n = 5) are expressed as: mg O2 g dry weight h for maximal photosynthetic rate (Pmax) and and gross photosynthesis (GP);
lmol photons m)2 s)1 for compensation (Ic) and initial saturation (Ik) irradiances; mg O2 g)1 dry weight h)1 (lmol photons m)2 s)1))1 for photosynthetic efficiency (a) and
photoinhibition parameter (b). P/R represents the ratio of Pmax/dark respiration. Distinct letters indicate significant differences (p < 0.05) by Newman–Keuls test.
a
According to Table 1.
151
152

mg O2 g-1 DW h-1 40 Geitlerinema splendida 40 Terpsinoe musica

30 30

20 20

10 10

0 0

-10 -10

0 100 200 300 400 500 0 100 200 300 400 500

Cladophora glomerata Nitella furcata var. sieberi

40 40
mg O2 g-1 DW h-1

30 30

20 20

10 10

0 0

-10 -10

0 200 400 600 800 1000 0 100 200 300 400 500
Net photosynthesis

40 Rhizoclonium hieroglyphicum 40 Spirogyra sp.

mg O2 g-1 DW h-1

30 30

20 20

10 10

0 0

-10 -10

0 100 200 300 400 500 0 200 400 600 800 1000

40 Batrachospermum delicatulum 40 Compsopogon coeruleus

-1

30 30
mg O2 g DW h

20 20
-1

10 10

0 0

-10 -10

0 100 200 300 400 500 0 100 200 300 400 500

40 Thorea hispida 40 Vaucheria fontinalis

-1

30 30
mg O2 g DW h

20 20
-1

10 10

0 0

-10 -10

0 100 200 300 400 500 0 100 200 300 400 500

Irradiance (µmol photons m-2 s-1) Irradiance (µmol photons m-2 s-1)
Figure 4. Photosynthesis–irradiance curves for lotic macroalge based on data of oxygen evolution. Bars indicate ±SD (n ¼ 5).

irradiance. Photoadaptation is here interpreted as of occurrence of photoinhibition in all algal

changes in the genotype, in contrast to photoacc- groups, more evident in the red algae and diatoms,
limation, which refers to phenotypic adjustments and less among the green algal species. According
that arise in response to variations of environ- to Hill (1996), it is not clear if benthic algae that
mental factors (Falkowski & La Roche, 1991). exhibit photoinhibition actually experience these
One relevant aspect of this study was the con- inhibitory irradiances in situ. These results confirm
firmation, under field and laboratory conditions, that the downturn in photosynthesis at high irra-

diances is not artificially induced by experimental
conditions, as discussed by Henley (1993), but is
rather a common and natural phenomenon of the
lotic macroalgae. Two different kinds of photoin-
hibition have been defined, namely dynamic and
chronic (Osmond, 1994). The former, generally
found in sun-adapted plants, is characterized by a
reversible photoprotective mechanism consisting
of a down-regulation of PSII in order to handle
excess energy by increasing thermal energy dissi-
pation. In contrast, the latter (most probable to
occur in shade-adapted plants) involves photo-
damage of PSII reaction centres. Photoinhibition
has been proposed as a strategy of photoprotec-
tion against high irradiance (Osmond, 1994;
Hanelt, 1996) and is mostly related to the degree
and extent of photoinhibition and recovery. Gen-
erally, algae subjected to high irradiances have
higher photoinhibition and recovery capacity than
those inhabiting shaded sites, which tend to pres-
ent chronic photoinhibition (Figueroa & Viñegla,
2001). Future studies dealing with specific mech-
anisms of photoinhibition in stream macroalgae
are necessary to evaluate recovery capacity after
exposure to high (photoinhibitory) irradiances,
followed by a dark recovery period, with simul-
taneous measurements of chl fluorescence para-
meters (particularly quantum yield).
Some general characteristics derived from PI
curves were important to evaluate the role of
macroalgae in lotic ecosystems. The low values of
Ic fit within the range reported for benthic algae
(1–40 lmol photons m)2 s)1, Hill, 1996; Necchi &
Zucchi, 2001; Vieira & Necchi, 2003). They indi-
cate that these algae can keep an autotrophic
metabolism even under very low irradiances. In
addition, the high ratios (>2) of net photosynthe-
sis/dark respiration found in most algae measured
in this and previous studies (Graham et al., 1982,
1985, 1995, 1996; Necchi & Zucchi, 2001; Vieira &
Necchi, 2003) indicate considerable net gain. These
two physiological characteristics, associated to the
fact that these algae can be widespread and
abundant (Sheath & Cole, 1992; Biggs, 1996),
suggest that they may be important primary pro-
ducers in lotic ecosystems, particularly in tropical
regions.
Our results agree with previous studies (sum-
marized by Hill, 1996) which indicate that the
saturation parameters (Ik and Is) occur in a rela-
153
tively narrow range of irradiances (100–
400 lmol photons m)2 s)1). In addition, results
confirmed that saturation can occur at high irra-
diances in some filamentous green algae (up to
2000 lmol photons m)2 s)1, Graham et al., 1995;
Ensminger et al., 2001) or at lower irradiances in
freshwater red algae (20–70 lmol photons m)2 s)1,
Leukart & Hanelt, 1995; Necchi & Zucchi, 2001).
However, data did not support the conclusion that
saturation irradiances are often well beyond the
typical irradiances found in situ, which implies that
photosynthesis is very strongly light-limited under
natural conditions (Hill, 1996). Values for the
saturation parameters (Ik and Is) of most algae
measured were way below the irradiances mea-
sured at collecting sites. This means that most of
the available light energy is not photochemically
converted via photosynthesis by lotic macroalgae.
This is true particularly for tropical species/popu-
lations, that are daily and seasonally exposed to
high irradiances (650–2000 lmol photons m)2 s)1,
Necchi 1997; Branco & Necchi, 1998; Necchi et al.,
1999; Vieira & Necchi, 2002). Thus, these algae
probably have mechanisms to avoid photodamage
of the photosynthetic apparatus due to long-term
exposure to high-light environments. Hill (1996)
stated that PI responses of benthic algae inhabiting
high-light environments should be under consid-
erable selective pressure to develop mechanisms
(e.g. accessory pigments such as carotenoids or
sheath pigments such as scytonemin) that reduce
the potentially damaging effects of high irradi-
ances. The role of these and additional photo-
protective mechanisms to avoid high irradiances,
such as the xanthophyll cycle and the daily up and
down regulation of photosynthetic parameters
(Ensminger et al., 2001) and photoinhibition (Os-
mond, 1994; Hanelt, 1996) deserves better atten-
tion in future studies on light adaptations in lotic
macroalgae.
Variable degrees of acclimation to ambient
PAR were observed, as revealed by lower values of
Ik and Ic and higher values of a and quantum yield
in algae under low irradiances (shaded-stream
segments), and vice versa. Physiological acclima-
tion to changes in both light intensity and spectral
quality has been regarded as an important factor
that determine photosynthetic responses in algae
(Falkowski & LaRoche, 1991). Thus, light accli-
mation is expected to occur but has been little
154
documented in freshwater benthic algae (Hill,
1996). Shade adaptation in phytoplankton and
macrophytes is usually manifested in increased
photosynthetic efficiency, lower photosynthetic
rates (lower Pmax) and decreased saturation
parameter (lower Ik) (Hill, 1996). Results of this
study essentially agree with these trends and can be
viewed as general patterns. However, light accli-
mation needs much more attention in future
studies of lotic macroalgae.
Some trends were evidenced for morphological
types of lotic macroalgae on the basis of chl fluo-
rescence data. Forms living within the boundary
layer (crusts) and, therefore, in a region of reduced
current velocity (Sheath & Hambrook, 1988)
showed characteristic responses of shade-adapted
species revealed by the highest values of Pmax, a
and quantum yield. The opposite trend was ob-
served in gelatinous forms (colonies and fila-
ments), that occur in the water column (semi-erect
forms according to Sheath & Hambrook, 1988)
but are protected from the flow-related stress by
the gelatinous matrix. The lowest values of Pmax,
photosynthetic efficiency and quantum yield can
be interpreted as characteristics related to reduc-
tion of the potentially damaging effects of high
irradiances, presumably provided by the shielding
effect of the gelatinous matrix that can have pro-
tective pigments such as scytonemin (Hill, 1996).
These results suggest adaptations to the light re-
gime rather than functional attributes related to
the growth form.
Acknowledgements
This investigation was supported by FAPESP (01/
06139-3) and CNPq Grants (520551/96-6). I am
indebted to Maria Helena Carabolante for help in
setting up the laboratory experiments and to So-
lange Aranha, UNESP, Brazil, for reviewing the
English.
References
Beer, S., C. Larsson, O. Poryan & L. Axelsson, 2000. Photo-
synthetic rates of Ulva (Chlorophyta) measured by pulse
amplitude modulated (PAM) fluorometry. European Jour-
nal of Phycology 35: 69–74.
Biggs, B. J. F., 1996. Patterns in benthic algae of streams. In
Stevenson, R. J., M. L. Bothwell & R. L. Lowe, (eds), Algal
Ecology: Freshwater Benthic Ecosystems. Academic Press,
San Diego: 31–56.
Boston, H. L. & W. R. Hill, 1991. Photosynthesis-light relations
of stream periphyton communities. Limnology and Ocean-
ography 36: 644–656.
Branco, C. C. Z. & O. Necchi Jr., 1998. Microhabitat and
morphometric variation of populations of two Chaetopho-
racean (Chaetophorales, Chlorophyta) species in tropical
streams of southeastern Brazil. Phycological Research 46:
169–174.
Collins, C. D. & C. W. Boylen, 1982. Physiological responses of
Anabaena variabilis (Cyanophyceae) to instantaneous expo-
sure to various combinations of light intensity and temper-
ature. Journal of Phycology 18: 206–211.
Conde-Álvarez, R. M., E. Pérez-Rodrı́guez, M. Altamirano, J.
M. Nieto, R. Abdala, F. L. Figueroa & A. Flores-Moya,
2002. Photosynthetic performance and pigment content in
the aquatic liverwort Riella helicophylla under natural solar
irradiance and solar irradiance without ultraviolet light.
Aquatic Botany 73: 47–61.
Ensminger, I., M. Xyländer, C. Hagen & W. Braune, 2000.
Strategies providing success in a variable habitat: II. Eco-
physiology of photosynthesis of Cladophora glomerata.
Plant, Cell and Environment 23: 1129–1136.
Ensminger, I., M. Xyländer, C. Hagen & W. Braune, 2001.
Strategies providing success in a variable habitat: III. Dy-
namic control of photosynthesis in Cladophora glomerata.
Plant, Cell and Environment 24: 769–779.
Falkowski, P. G. & J. LaRoche, 1991. Acclimation to spectral
irradiance in algae. Journal of Phycology 27: 8–14.
Figueroa, F. L. & B. Viñegla, 2001. Effects of solar UV radi-
ation on photosynthesis and enzyme activities (carbonic
anhydrase en nitrate reductase) in marine macroalgae from
southern Spain. Revista Chilena de História Natural 74:
237–249.
Franklin, L. A. & M. R. Badger, 2001. A comparison of pho-
tosynthetic electron transport rates in macroalgae measured
by pulse amplitude modulated chlorophyll fluorometry and
mass spectrometry. Journal of Phycology 37: 756–767.
Graham, J. M., P. Arancibia-Avila & L. E. Graham, 1996.
Physiological ecology of a species of the filamentous green
alga Mougeotia under acidic conditions: light and tempera-
ture effects on photosynthesis and respiration. Limnology
and Oceanography 41: 253–262.
Graham, J. M., M. T. Auer, R. P. Canale & J. P. Hoffmann,
1982. Ecological studies and mathematical modelling of
Cladophora in Lake Huron. 4. Photosynthesis and respira-
tion as functions of light and temperature. Journal of Great
Lakes Research 8: 100–111.
Graham, J. M., J. A. Kranzfelder & M. T. Auer, 1985. Light
and temperature as factors regulating seasonal growth and
distribution of Ulothrix zonata (Ulvophyceae). Journal of
Phycology 21: 228–234.
Graham, J. M., C. A. Lembi, H. L. Adrian & D. F. Spencer,
1995. Physiological responses to temperature and irradiance
in Spirogyra (Zygnematales, Charophyceae). Journal of
Phycology 31: 531–540.

Guasch, H. & S. Sabater, 1995. Seasonal variations in photo-
synthesis–irradiance responses by biofilms in Mediterranean
streams. Journal of Phycology 31: 727–735.
Häder, D.-P., M. Lebert, F. L. Figueroa, C. Jiménez, B.
Viñegla & E. Perez-Rodriguez, 1998. Photoinhibition in
Mediterranean macroalgae by solar radiation measured on
site by PAM fluorescence. Aquatic Botany 61: 225–236.
Hanelt, D., 1996. Photoinhibition of photosynthesis in marine
macroalgae. Scientia Marina 60(Suppl. 1): 243–248.
Henley, W. J., 1993. Measurement and interpretation of photo-
synthetic light-response curves in algae in the context of
photoinhibition and diel changes. Journal of Phycology 29:
729–739.
Hill, W. R., 1996. Effects of light. In Stevenson, R. J., M. L.
Bothwell & R. L. Lowe (eds), Algal Ecology: Fresh-
water Benthic Ecosystems. Academic Press, San Diego: 121–
148.
Howard-Williams, C. & W. F. Vincent, 1989. Microbial com-
munities in southern Victoria Land streams (Antarctica) I.
Photosynthesis. Hydrobiologia 172: 27–38.
Kremer, B. P., 1983. Untersuchungen zur Ökophysiologie
einiger Süsswasserrotalgen. Decheniana 136: 31–42.
Kromkamp, J., C. Barranguet & J. Peene, 1998. Determination
of microphytobenthos PSII quantum efficiency and photo-
synthetic activity by means of variable chlorophyll fluores-
cence. Marine Ecology Progress Series 162: 45–55.
Leukart, P. & D. Hanelt, 1995. Light requirements for photo-
synthesis and growth in several macroalgae from a small
soft-water stream in the Spessart Mountains, Germany.
Phycologia 34: 528–532.
Littler, M. M. & K. E. Arnold, 1985. Electrodes and chemicals.
In Littler, M. M. & D. S. Littler (eds), Handbook of Phy-
cological Methods; Ecological Field Methods: Macroalgae.
Cambridge University Press, Cambridge: 349–375.
Necchi, O. Jr., 1997. Microhabitat and plant structure of Ba-
trachospermum (Batrachospermales, Rhodophyta) popula-
tions in four streams of São Paulo State, southeastern Brazil.
Phycological Research 45: 39–45.
Necchi, O. Jr., C. C. Z. Branco & L. H. Z. Branco, 2000.
Distribution of stream macroalgae in São Paulo State,
southeastern Brazil. Algological Studies 97: 43–57.
Necchi, O. Jr., C. C. Z. Branco & R. R. V. Gomes, 1999.
Microhabitat and plant structure of Compsopogon coeruleus
(Compsopogonaceae, Rhodophyta) populations in streams
from São Paulo State, southeastern Brazil. Cryptogamie,
Algologie 20: 75–87.
155
Necchi, O. Jr. & D. Pascoaloto, 1993. Seasonal dynamics of
macroalgal communites in the Preto River basin, São Paulo,
southeastern Brazil. Archiv für Hydrobiologie 129: 231–252.
Necchi, O. Jr. & M. R. Zucchi, 2001. Photosynthetic perfor-
mance of freshwater Rhodophyta in response to tempera-
ture, irradiance, pH and diurnal rhythm. Phycological
Research 49: 305–318.
Osmond, C. B., 1994. What is photoinhibition? Some insights
from comparisons of shade and sun plants. In Baker, N. R.
& J. R. Bowyer, (eds), Photoinhibition of Photosynthesis:
from Molecular Mechanisms to the Field. Bios Science
Publishers, Oxford: 1–24.
Platt, T., C. L. Gallegos & W. G. Harrison, 1980. Photoinhi-
bition of photosynthesis in natural assemblages of marine
phytoplankton. Journal of Marine Research 38: 687–701.
Schreiber, U., W. Bilger, & C. Neubauer, 1994. Chlorophyll
fluorescence as a non-intrusive indicator for rapid assess-
ment of in vivo photosynthesis. In Schulze, E.-D. & M. M.
Caldwell (eds), Ecophysiology of Photosynthesis, Vol. 100.
Springer-Verlag, Berlin: 49–70.
Sheath, R. G. & K. M. Cole, 1992. Biogeography of stream
macroalgae in North America. Journal of Phycology 28:
448–460.
Sheath, R. G. & J. A. Hambrook, 1988. Mechanical adapta-
tions to flow in freshwater red algae. Journal of Phycology
24: 107–111.
Thomas, M. L. H., 1988. Photosynthesis and respiration of
aquatic macro-flora using the light and dark bottle oxygen
method and dissolved oxygen analyser. In Lobban, C. S., D.
J. Chapman & B. P. Kremer (eds), Experimental Phycology:
A Laboratory Manual. Cambridge University Press, Cam-
bridge: 64–77.
van Kooten, O. & J. J. H. Snel, 1990. The use of chlorophyll
fluorescence nomenclature in plant stress physiology.
Photosynthesis Research 25: 147–150.
Vieira, J. Jr. & O. Necchi Jr., 2002. Microhabitat and plant
structure of Characeae (Chlorophyta) populations in streams
from southeastern Brazil. Cryptogamie, Algologie 23: 51–63.
Vieira, J. Jr. & O. Necchi Jr, 2003. Photosynthetic character-
istics of charophytes from tropical ecosystems. Phycological
Research 51: 51–60.
White, A. J. & C. Critchley, 1999. Rapid light curves: a new
fluorescence method to assess the state of the photosynthetic
apparatus. Photosynthesis Research 59: 63–72.
Zar, J. H., 1999. Biostatistical Analysis. Prentice Hall, New
Jersey, 663 pp.