Journal of Bryology

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Responses of photosynthesis to irradiance in

bryophytes of the Azores laurel forest

Rosalina Gabriel & Jeffrey W. Bates

To cite this article: Rosalina Gabriel & Jeffrey W. Bates (2003) Responses of photosynthesis
to irradiance in bryophytes of the Azores laurel forest, Journal of Bryology, 25:2, 101-105, DOI:
10.1179/037366803235001760

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Published online: 18 Jul 2013.

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 Journal of Bryology (2003) 25: 101–105

Responses of photosynthesis to irradiance in bryophytes of the

Azores laurel forest

1
ROSALINA GABRIEL and 2JEFFREY W. BATES

1
Universidade dos Açores, Terceira, Portugal and 2Imperial College London, Ascot, U.K.

SUMMARY

Photosynthetic responses to light intensity were studied under laboratory conditions in seven bryophyte
species from evergreen laurel forest, a threatened habitat, on Terceira island in the Azores. Four mosses (Andoa
berthelotiana, Echinodium prolixum, Fissidens serrulatus, Myurium hochstetteri) and three liverworts (Bazzania
azorica, Frullania tamarisci, Lepidozia cupressina) were selected to encompass a range of potential responses
to variations in the forest light environment. Carbon dioxide exchange measurements were made, using
an infra-red gas-analyser, at photosynthetic photon flux densities (PPFD) of 0–900 µmol m-2 s-1 and a mean
temperature of 21°C in fully hydrated shoots. Most species achieved light saturation of photosynthesis below
30 µmol m -2 s-1, the lowest value being for A. berthelotiana (20 µmol m-2 s-1) and the highest for M. hochstetteri
(68 µmol m-2 s-1). The liverwort F. tamarisci had the highest maximum photosynthetic rate (Pmax, 23 µmol CO2
g-1 h-1) whereas Pmax was lowest in the mosses E. prolixum and M. hochstetteri (10 µmol CO2 g-1 h-1). Dark
respiration rate, a critical factor in toleration of shade by forest floor plants, was highest in the species with the
highest values for Pmax. Compensation point was extremely low (7 µmol photons m-2 s-1) in Fissidens serrulatus,
a species found in the deep shade of forest ravines and caves, and highest in M. hochstetteri a moss restricted to
better illuminated habitats within and outside the forest. No photoinhibition was detected during the relatively
short exposures to high irradiances. Comparison of these responses with data on the forest light environment
indicates that, despite the possession of considerable shade adaptations, during winter in the evergreen laurel
forest, low light levels may often limit photosynthetic rates of the bryophytes.

KEYWORDS: Azores, laurel forest, bryophytes, photosynthesis-illumination curves, compensation point,

photoinhibition.

INTRODUCTION of the predominant trees and shrubs the RH is ca 94% in

August and light levels are only 5–10 % of those of the exter-
The natural evergreen forests of the Azores island group
ior (Gabriel, 2000). Removal of the forest can be expected to
support a species-rich and luxuriant bryophyte flora includ-
be damaging to its bryophytes by greatly increasing their
ing both archipelago and Macaronesian endemics (Sjögren,
exposure to light and desiccation as well as by removal
1978; Sérgio, 1984; Bates & Gabriel, 1997; Gabriel, 2000).
of specific habitats (Gradstein, 1992). This study is part of
Regrettably, the extent of these forests continues to diminish
owing to felling to provide land for agriculture and commer- a wider investigation of the physiological and ecological
cial forestry, and several of their distinctive bryophytes are features of some of the characteristic oceanic bryophytes of
becoming threatened (ECCB, 1995). The original richness the native forests of the Azores undertaken as an aid to their
of the bryophyte flora is linked to a favourable combination effective conservation (Gabriel, 2000). Although oceanic
of climatic and microclimatic factors. These include the bryophytes have received some attention from an ecological
relative warmth and extremely high rainfall owing to the point of view (e.g. Ratcliffe, 1968; Sjögren, 1978; Edwards,
mid-Atlantic position, the mountainous character of the 1986), there have been very few studies of their physiological
larger islands stimulating rainfall and mist formation, and limitations. In this paper we report on the photosynthetic
shading and trapping of humidity inside the forest by the responses to light intensity in a range of Azorean forest
dense canopy (Sjögren, 1978). Under the evergreen canopy bryophytes.

© British Bryological Society 2003 Received 3 May 2002. Revision accepted 5 December 2002
DOI: 10.1179/037366803235001760

Published online 18 Jul 2013

102 R. GABRIEL AND J. W. BATES

MATERIALS AND METHODS was placed in a cylindrical perspex assimilation chamber

(volumes 98–117 cm3) with removable lid and with the block
Plant material and cultivation conditions in contact with free distilled water to help maintain hydra-
tion of the shoots during the incubation. Some evidence
Seven bryophyte species, four mosses (Andoa berthelotiana was obtained that blotting of surface water from the shoots
(Mont.) Ochyra, Echinodium prolixum (Mitt.) Broth., Fis- with absorbent paper is damaging (lowered photosynthetic
sidens serrulatus Brid. and Myurium hochstetteri (Schimp.) rates), therefore the gentler expedient of shaking off the
Kindb.) and three liverworts (Bazzania azorica Buch & excess water prior to planting in ‘oasis’ was adopted.
Perss., Frullania tamarisci (L.) Dum. and Lepidozia cup- The assimilation chambers were immersed in a shallow
ressina (Sw.) Lindenb.) were chosen for study. They were water bath maintained at 21ºC (± 2ºC). Photosynthetically
selected to encompass a range of tolerances to drought and active radiation (PPFD) was provided by four 100 W
to low and high light levels inferred from field observations. tungsten spot lamps in a reflector hood placed above the
It was hypothesized that obligate forest species (Bazzania waterbath. A range of PPFD was achieved by switching
azorica, Lepidozia cupressina) would be the most sensitive to on different combinations of the four lamps, and by placing
high light and low water availability. Other species (Andoa layers of white and black cheesecloth over the chambers.
berthelotiana, Echinodium prolixum, Myurium hochstetteri), Ten points were below 100 µmol photon m-2 s-1 and eight
although frequent in the forest, may occasionally be found approximately evenly distributed upwards to 900 µmol m-2
outside and are presumably less demanding of extreme s-1. Each chamber was incubated in the water bath for
shelter and shade. Fissidens serrulatus is a common species 20 min at each PPFD, and also for 10 min in the dark (cham-
in the Azores wherever shaded conditions are present but is ber covered with aluminium foil) to determine respiration
not restricted to forest. In comparison with these, Frullania rate. Immediately prior to each incubation the CO2 concen-
tamarisci is a generalist. It is found in exposed habitats and tration was brought to a known value (usually 350 v.p.m.)
on all kinds of substrata within a wide altitudinal range by flushing for 1 min at a flow rate of 1200 cm3 min-1 and
in the Azores, and also has a wide distribution in Europe. sealing at ambient air pressure. At the end of the incubation
Healthy material of these species was collected from exten- a 5 cm3 sample of the chamber air was withdrawn by hypo-
sive colonies in natural laurel forest habitats at Pico Alto dermic syringe and injected into the CO2-free airstream lead-
(UTM 1-km grid square 8289; altitude 600 m) in the centre ing to the sample cell of the IRGA. Peak height was recorded
of Terceira. A. berthelotiana, E. prolixum, F. tamarisci, and on a chart-recorder. The bryophyte shoots were freeze-
M. hochstetteri were collected from the bark of Laurus dried to obtain dry weight. Net photosynthesis and dark
azorica (Seub.) Franco, L. cupressina from bark of Juniperus respiration rates were expressed as moles of carbon dio-
brevifolia (Seub.) Antoine, B. azorica was sampled from xide absorbed or released per gram dry weight per hour
lava walls of a ravine with some soil, and F. serrulatus was (µmol CO2 g-1 h-1).
taken from basaltic rocks. Three species bore sporophytes:
A. berthelotiana, F. tamarisci, and M. hochstetteri. Curve fitting
The plants were transported to the laboratory at Imperial
College in a fully hydrated condition within one week in July Photosynthesis-illumination curves were fitted using the
1996. In the laboratory, the shoots were spread on horticul- equations of Baly (1935) modified by Titus & Wagner
tural capillary matting that had been saturated with distilled (1984). This function is a two-parameter hyperbola,
water within seed trays (60 × 30 cm) covered with trans- bounded by zero and one.
parent plastic propagator lids. They were regularly watered
with distilled water but care was taken to avoid flooding. Pgn = (Pmax * b * L) / (Pmax + b * L),
The closed trays were placed in a constant temperature (CT) where, Pgn is the normalized rate of photosynthesis
room at 15°C, 80% RH and 16 h photoperiod at 40 µmol (Titus & Wagner, 1984; Alpert & Oechel, 1987), Pmax is the
photon m-2 s-1 for about one month prior to use. This maximum photosynthetic rate, b is the slope of the initial
period was considered desirable to avoid effects caused proportional increase and is a constant, and L is the
by any desiccation or by high or low temperature stresses photon flux density. Pgn accounts for the respiration and
suffered during transportation. transforms the data so they fall between zero and one,
Pgn = (given rate of net photosynthesis - R) / (Pmax - R),
Gas exchange measurements
where, R is the respiration rate. The coefficient b was
Net photosynthesis and dark respiration were measured estimated by non-linear regression in SYSTAT 8.0. Light
with an infrared gas analyser (IRGA, Series 225, Analytical saturation point (IS) was considered to have been achieved
Development Co. Ltd. England), using a method similar to when net photosynthesis was at least 90% of the maximum
that of Larson & Kershaw (1975). Thirty or more fully value of photosynthesis for the species. Light compensation
hydrated shoots (10–20 mm fully green apical segments point (IC) was estimated using the linear part of the relation-
depending on species) were inserted at their bases into a ship between photon flux density and net photosynthesis.
piece (5 mm height) of saturated florist’s ‘oasis’. The shoots The averages of three replicate datasets were used to fit the
were arranged evenly to avoid self-shading. Each such unit curve for each species.
 PHOTOSYNTHESIS -IRRADIANCE RESPONSES OF AZORES BRYOPHYTES 103

Figure 1. Dependence of net photosynthesis on photosynthetically active radiation at 20ºC for: Andoa berthelotiana; Bazzania azorica; Echinodium
prolixum; Fissidens serrulatus; Frullania tamarisci; Lepidozia cupressina; Myurium hochstetteri.
104 R. GABRIEL AND J. W. BATES

RESULTS points (Table 1). Fissidens serrulatus exhibited a remarkably

low compensation point (7 µmol photon m-2 s-1) compar-
The species investigated responded differently to increasing able to those reported in Marchantia foliacea and Monoclea
PPFD in their CO2 assimilation rates (IC, IS, Pmax), photo- forsteri (Green & Snelgar, 1982). F. serrulatus is normally
synthetic efficiencies (b, slope of the curve), and dark respi- found in deep shade in ravines, cave entrances, and on
ration rates (Fig. 1, Table 1). Fissidens serrulatus exhibited other shaded rocks and soil. Myurium hochstetteri had the
the lowest compensation point values (7 µmol photon highest compensation value (31 µmol photon m-2 s-1) which
m-2 s-1), while other species presented intermediate figures matches its prevalence in well-illuminated habitats, espe-
(8 to 12 µmol m-2 s-1) and Myurium hochstetteri the highest cially as an epiphyte on Laurus azorica, (generally above
(31 µmol m-2 s-1). Light saturation (IS) was generally 60 cm height), or on rocks in clearings or even outside the
achieved below 30 µmol m-2 s-1, the lowest value being for forest. The other species have very low compensation points
Andoa berthelotiana (20 µmol m-2 s-1) and the highest for (8 to 12 µmol photon m-2 s-1) which may permit net pho-
Myurium hochstetteri (68 µmol m-2 s-1). The highest values tosynthetic gains in shaded forest habitats (Kershaw &
of net Pmax were obtained for Frullania tamarisci (23 µmol Webber, 1986). Values of light saturation for the species
CO2 g-1 h-1) among the liverworts and for Andoa berthe- studied here lay between 20 and 69 µmol photon m-2 s-1,
lotiana (15 µmol g-1 h-1) among the mosses. The species with with Andoa berthelotiana and Fissidens serrulatus showing
the lowest values of Pmax were the mosses Myurium the lowest values, and Myurium hochstetteri the highest.
hochstetteri and Echinodium prolixum (10 µmol g-1 h-1). Comparable light saturation levels have been found in
There was no inhibition of photosynthetic rates at the other forest bryophytes (Green & Snelgar, 1982; Bakken,
highest PPFD provided (900 µmol m-2 s-1). Dark respira- 1995), whereas non-forest bryophytes usually exhibit
tion rates were highest for the species that yielded the highest much higher values (300–600 µmol photon m-2 s-1; Larcher,
photosynthetic rates, Andoa berthelotiana (28 µmol CO2 1995). Somewhat higher light saturation values have been
g-1 h-1), Frullania tamarisci (25 µmol g-1 h-1), and Fissidens reported on the basis of chlorophyll fluorescence estimates
serrulatus (23 µmol g-1 h-1). Respiration rates were lowest of relative electron flow rate in two pendulous epiphytes of
for Echinodium prolixum and Myurium hochstetteri (15 and tropical African forests and in a range of British woodland
16 µmol g-1 h-1, respectively). The slopes of the photo- bryophytes (Proctor, 2002). Comparison of our IC and IS
synthesis-illumination curves for each species (estimated results with the actual irradiances experienced in native ever-
parameter b) and their associated standard errors are given green forest (Gabriel, 2000) indicates that sufficient irradi-
in Table 1. Two groups of values were observed, those ance is available for some bryophyte growth in all months.
around 0.10 (F. tamarisci, L. cupressina, and M. hochstetteri) However, from November until March, plants may often
and those higher than 0.22 (A. berthelotiana, E. prolixum, photosynthesize under light levels that are below those
and F. serrulatus). The proportions of the variation that was needed to saturate the photosystems.
explained by the fitted curves were high, r2 varying from High respiration rates are characteristic of heliophytes
0.986 in Bazzania azorica and Frullania tamarisci to 0.999 in and rapidly growing species. Mosses, herbaceous plants,
Fissidens serrulatus. deciduous trees, and evergreen trees form a series of increas-
ing respiration rates (Larcher, 1995). Respiration of mosses
DISCUSSION proceeds at a low rate, from 1–4 mg CO2 g-1 h-1 (Skre &
Oechel, 1981; Sveinbjörnsson & Oechel, 1992). The highest
Two aspects of the responses to light that may be especially dark respiration rates observed in this investigation were
important to forest bryophytes are the ability to maintain a achieved by Andoa berthelotiana (28 µmol g-1 h-1 or, in units
positive carbon balance under deep shade, and susceptibil- allowing comparison with the figures above, 1.2 mg CO2 g-1
ity to photoinhibition at high irradiance (Seel, Hendry & h-1) and Frullania tamarisci (25 µmol CO2 g-1 h-1 or 1.1 mg
Lee, 1992), e.g. through removal of the forest canopy. The CO2 g-1 h-1), and most of the other species exhibited similar
species investigated appear well adapted to low light levels, values. Echinodium prolixum and Myurium hochstetteri,
exhibiting low compensation points and low saturation however, exhibited lower respiration values (16 and 15 µmol

Table 1. Comparison of species photosynthetic attributes based on the data in Fig. 1. See text and Fig. 1 for explanation. Figures are means of three
replicates and their standard errors.

Species Compensation Saturation Net Pmax Respiration b r2

Point, Ic Point, Is rate

(µmol photon m-2 s-1 ) (µmol CO2 g-1 dw h-1 )

Andoa berthelotiana 8 ± 0.2 20 ± 4.7 15 ± 0.5 28 ± 3.0 0.22 ± 0.03 0.996

Bazzania azorica 9 ± 0.5 29 ± 0.0 16 ± 0.3 19 ± 3.7 0.14 ± 0.03 0.986
Echinodium prolixum 9 ± 1.1 27 ± 12.5 10 ± 0.2 15 ± 1.7 0.28 ± 0.04 0.997
Fissidens serrulatus 7 ± 0.5 24 ± 4.7 12 ± 0.3 23 ± 3.8 0.24 ± 0.02 0.999
Frullania tamarisci 10 ± 0.7 36 ± 6.4 23 ± 0.6 25 ± 2.6 0.09 ± 0.01 0.986
Lepidozia cupressina 12 ± 0.7 30 ± 0.7 13 ± 0.5 19 ± 3.3 0.10 ± 0.02 0.991
Myurium hochstetteri 31 ± 2.8 68 ± 0.0 10 ± 0.3 16 ± 3.3 0.10 ± 0.02 0.996
 PHOTOSYNTHESIS -IRRADIANCE RESPONSES OF AZORES BRYOPHYTES 105

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ROSALINA GABRIEL, Departamento de Ciências Agrárias. Universidade dos Açores,

9700-851 Angra do Heroísmo, Portugal. E-mail: [email protected]
JEFFREY W. BATES, Department of Biological Sciences, Imperial College London,
Silwood Park Campus, Ascot, Berkshire SL5 7PY, U.K.
E-mail: [email protected]