Limnol. Oceanogr., 26(2), 1981,271-284 @ 1981, by the American Society of Limnology and Oceanography, Inc. Chromatic adaptation of photosynthesis in benthic marine algae: An examination of its ecological significance using a theoretical model M. J. Dring Department of Botany, The Queen’s University, Belfast, BT7 lNN, Northern Ireland Abstract All available action spectra of photosynthesis for benthic marine algae have been multiplied by the spectral distribution of the light at different depths in all Jerlov water types to predict the photosynthesis per unit quantum irradiance of each species in each habitat. Comparison of the predictions indicates that red algae are best adapted chromatically to photosynthesize at all depths (including 0 m) in all except the clearest oceanic waters. The results show little correlation with the patterns of vertical distribution of green, brown, and red algae in benthic marine habitats, and suggest, therefore, that light quality is not a major factor in the control of that distribution. A review of physiological evidence supports the hypothesis that the changes in pigment composition that are observed with increasing depth in marine algae are largely adaptations to low irradiance, and not to the spectral composition of underwater light. The theory of complementary chromat- ic adaptation as applied to marine algae (Engelmann 1883) provides one of the simplest and most attractive examples of the physiological adaptation of plants to the environmental conditions in which they live. It is almost certainly for this reason that the theory appears in many elementary textbooks on botany and ecol- ogy, and is so often expounded in under- graduate lectures on these subjects. The frequency with which it reappears in ex- amination answers indicates that the the- ory is also very popular with students and is readily assimilated by them. In view of this wide dissemination and apparent popularity of the theory, it is disconcerting to find that the supporting evidence is rather thin. The most fre- quently cited evidence involving marine algae is a study by Levring (1947), in which the photosynthesis of green algae was shown to decrease with depth in coastal waters more rapidly than the un- derwater irradiance, whereas that of red algae decreased less rapidly, and that of brown algae decreased at about the same rate as the irradiance, In a similar, later study in oceanic waters, Levring (1968) was able to show that the photosynthetic responses of green and red algae to depth in clear, “bl ue” waters were the opposite of those in more turbid, “green” waters nearer the coast. These results were said to provide “good support for the theory of . . * chromatic adaptation” (Lcvring 1966, p. 311), but the basis on which the results are expressed prevents direct comparison of absolute photosynthetic rates in different species. They cannot, therefore, be used to provide evidence that, for example, the photosynthesis of a red alga at depth is greater than that of a green alga at the same depth or that this situation is reversed near the surface. We must also remember that Levring’s orig- inal work, far-reaching and remarkable as it was for its time, was undertaken before a real understanding of the mechanism of photosynthesis was available, and it also preceded the comprehensive optical classification of coastal and oceanic waters by Jerlov (1951), which forms the basis for so much modern work on light in the sea. Doubts have occasionally been raised about chromatic adaptation, stimulated by field observations (e.g. Crossett et al. 1965; Doty et al. 1974), by experimental results (e.g. Jones and Myers 1965), and by a study of the pigments and photosyn- thesis of oceanic phytoplankton from dif- ferent depths (Shimura and Ichimura 1973). Some recent workers have con- cluded that “today, even the most casual algologist recognises that pigmentation bears very little relationship to the the- ory” (Yentsch 1974, p. 53) and have sus- 271
Transcript
Limnol. Oceanogr., 26(2), 1981,271-284 @ 1981, by the American Society of Limnology and Oceanography, Inc.
Chromatic adaptation of photosynthesis in benthic marine algae: An examination of its ecological significance using a theoretical model
M. J. Dring Department of Botany, The Queen’s University, Belfast, BT7 lNN, Northern Ireland
Abstract
All available action spectra of photosynthesis for benthic marine algae have been multiplied by the spectral distribution of the light at different depths in all Jerlov water types to predict the photosynthesis per unit quantum irradiance of each species in each habitat. Comparison of the predictions indicates that red algae are best adapted chromatically to photosynthesize at all depths (including 0 m) in all except the clearest oceanic waters. The results show little correlation with the patterns of vertical distribution of green, brown, and red algae in benthic marine habitats, and suggest, therefore, that light quality is not a major factor in the control of that distribution. A review of physiological evidence supports the hypothesis that the changes in pigment composition that are observed with increasing depth in marine algae are largely adaptations to low irradiance, and not to the spectral composition of underwater light.
The theory of complementary chromat- ic adaptation as applied to marine algae (Engelmann 1883) provides one of the simplest and most attractive examples of the physiological adaptation of plants to the environmental conditions in which they live. It is almost certainly for this reason that the theory appears in many elementary textbooks on botany and ecol- ogy, and is so often expounded in under- graduate lectures on these subjects. The frequency with which it reappears in ex- amination answers indicates that the the- ory is also very popular with students and is readily assimilated by them.
In view of this wide dissemination and apparent popularity of the theory, it is disconcerting to find that the supporting evidence is rather thin. The most fre- quently cited evidence involving marine algae is a study by Levring (1947), in which the photosynthesis of green algae was shown to decrease with depth in coastal waters more rapidly than the un- derwater irradiance, whereas that of red algae decreased less rapidly, and that of brown algae decreased at about the same rate as the irradiance, In a similar, later study in oceanic waters, Levring (1968) was able to show that the photosynthetic responses of green and red algae to depth in clear, “bl ue” waters were the opposite of those in more turbid, “green” waters nearer the coast. These results were said
to provide “good support for the theory of . . * chromatic adaptation” (Lcvring 1966, p. 311), but the basis on which the results are expressed prevents direct comparison of absolute photosynthetic rates in different species. They cannot, therefore, be used to provide evidence that, for example, the photosynthesis of a red alga at depth is greater than that of a green alga at the same depth or that this situation is reversed near the surface. We must also remember that Levring’s orig- inal work, far-reaching and remarkable as it was for its time, was undertaken before a real understanding of the mechanism of photosynthesis was available, and it also preceded the comprehensive optical classification of coastal and oceanic waters by Jerlov (1951), which forms the basis for so much modern work on light in the sea.
Doubts have occasionally been raised about chromatic adaptation, stimulated by field observations (e.g. Crossett et al. 1965; Doty et al. 1974), by experimental results (e.g. Jones and Myers 1965), and by a study of the pigments and photosyn- thesis of oceanic phytoplankton from dif- ferent depths (Shimura and Ichimura 1973). Some recent workers have con- cluded that “today, even the most casual algologist recognises that pigmentation bears very little relationship to the the- ory” (Yentsch 1974, p. 53) and have sus-
271
272 Dring
petted that “the classical picture was conceived by observers who were re- porting what was visible at low tide at hip-boot depth” (Doty et al. 1974, p. 345). Others seem convinced that chromatic adaptation is still a valid concept, Much of the discussion about chromatic adap- tation, both before and since Levring’s work, has centered around an alternative theory of “intensity adaptation,” origi- nally put forward by Berthold (1882) and Oltmanns (1892). The major problem in distinguishing between these two theo- ries is that, in the sea, natural changes in light quality are invariably confounded with changes in light quantity, and any critical assessment must find a way of separating these two variables and ex- amining their effects independently of one another.
I report here an attempt to achieve this by calculating the photosynthesis of dif- ferent algal species in natural light fields of different spectral composition, but of identical quantum irradiance. This is es- sentially the same approach as that adopt- ed by Levring (1947) in the theoretical parts of his work, but I have been able to make use of more recently measured ac- tion spectra for photosynthesis and of more extensive data on the spectral trans- mission of light through the different “water types” defined by Jerlov (1976). I also review the experimental evidence concerning the effects of light quality on the pigment composition of benthic ma- rine algae.
This paper was written on a study visit to the Biologische Anstalt Helgoland. I thank K. Liining for discussions and the Royal Society for financial support.
The model A simple theoretical model, relating
the spectral composition of the incident light to the action spectrum of photosyn- thesis for each species, forms the basis of this investigation. The spectral composi- tion was expressed as the percentage of total visible (400-700 nm) quanta in each 25-nm waveband, and the action spec- trum as the relative photosynthesis per quantum in the same wavebands. The
contribution of each waveband to the to- tal photosynthesis of the plant was then calculated by multiplying the percentage of quanta in that waveband by the cor- responding value for photosynthesis and adding these products for all wavebands to obtain a prediction of the total photo- synthesis per unit of quantum irradiance in that light field. The model can be ex- pressed pseudo-mathematically as
400
where P,. is gross photosynthesis per quantum of incident light (400-700 nm), Ph is gross photosynthesis per incident quantum in waveband A, and Eh = pro- portion of total quanta (400-700 nm) in waveband A. The source of the values to be used in the model is explained below.
Spectral composition-Data for the spectral transmission of seawater of dif- ferent optical types (Jerlov 1976) have been used to calculate the spectral com- position of the light reaching various depths in all water types. The effects of variations in the spectral composition of light at the surface of the sea were al- lowed for by performing all calculations for clear sky conditions (i.e. sun + sky, with a solar altitude of 45”) and for cov- ered sky conditions, using data from Jer- lov (1954). The broad curves for the spec- tral transmission of different water types (fig. 69: Jerlov 1976) are rapidly intensi- fied with depth in coastal waters (Fig. 1, left), so that, at 10 m, about 70% of the total visible quanta are concentrated within a waveband 100 nm wide. The peak of this waveband varies consider- ably with water type (Fig. 1, right), rang- ing from a broad peak at 500-550 nm in clear coastal waters (type 3) to a sharp peak at 575 nm in the most turbid coastal waters (type 9). In the clearest oceanic waters (types I-III), light penetrates much deeper and, therefore, benthic al- gae are able to grow at greater depths. The spectral compositions calculated for such depths in oceanic water type I show that the same concentration of quanta within a narrow waveband occurs, but at greater depths than in coastal waters. The
Chromatic adaptation 273
Wavelength (nm) Wavelength (nm)
Fig. 1. Spectral distribution of underwater light in coastal water types, calculated from spectral trans- mission data (Jerlov 1976). Left-variation with depth (O-10 m) in coastal water type 5. Right-variation with coastal water type (3-9) at 10-m depth. Surface conditions: sun + sky, 45” (Jerlov 1954).
spectral peak in oceanic waters is at 475 nm, and, even at 30 m, only 0.3% of the total quanta will be at wavelengths >600 nm.
Action spectra of photosynthesis- Two main sources of action spectra data for this investigation were the classic work of Haxo and Blinks (1950) and a se- ries of action spectra recently measured by Liining and Dring (unpubl.), but most other published action spectra relating to marine algae have also been tested in the model. Nearly all of these spectra plot “relative photosynthesis” per quantum against wavelength, so that it is impossi- ble to calculate absolute photosynthetic rates, or to make direct comparisons be- tween species. All action spectra used, therefore, have been converted to a com- mon relative base by dividing all of the measured values for any one spectrum by the mean value for that spectrum. Thus, in all of the spectra used, the photosyn- thesis in each waveband was expressed as a proportion of the mean photosynthe-
sis in all wavebands, so that, for every action spectrum, the mean of the values used was 1.0 (see Fig. 3). These correc- tions make direct comparisons between species possible and have the additional advantage that variations between species in the efficiency of light utilization (i.e. the initial slope in P vs. 1 curves), which result, for example, from differences in pigment concentration per unit area of thallus, do not affect the calculations. Thus, the effects of such variations are not confounded with the effects of vari- ations in the action spectrum, which re- sult from differences in pigment compo- sition. The final result of the model calculations, P7’, therefore, is a measure of the total photosynthesis per quantum of incident light and per unit of chloro- phyll, relative to that in other light fields or to that of other species.
Two extreme examples may help to make the biological interpretation of P, clear. A totally absorbing, black algal thallus will have a completely flat action
274 Dring
spectrum with a value for relative pho- tosynthesis of 1.0 in each waveband. Any spectral distribution multiplied by such a flat action spectrum and integrated over all wavebands will give a value of 1.0 for the total photosynthesis I?,.. The impli- cation of this result is that a black alga will achieve the same photosynthesis per quantum in any light field, regardless of its spectral content. At the other extreme, consider a perfectly “white” light field with a flat spectral distribution, The val- ues for the spectral distribution used in the model will be the same for each waveband, and, therefore, when this spectral distribution is multiplied by any action spectrum and integrated, the re- sult will also be 1.0. Thus, in a perfectly white light field, in which all wave- lengths are equally represented on a quantum basis, all algae will achieve the same photosynthesis per quantum and per unit pigment concentration, regard- less of their pigment composition and ac- tion spectra. Any other spectral distribu- tion multiplied by any other action spectrum will give a value for P,, which may be above or below 1.0, and the de- viation of PT from 1.0 may be interpreted as a measure of the “chromatic adapta- tion” (in an exact sense) of that specific action spectrum to that specific light field. Values above 1.0 indicate that the alga will make more efficient use of the incident wave1 engths than our hypothet- ical black alga, whereas values below 1.0 imply that the species will be less effi- cient and that its pigment composition is a disadvantage- or a negative adapta- tion-in that light field.
Results The photosynthesis, PT, predicted by
the model was calculated for depths at intervals of 1 m down to 10 m in all water types for 29 different action spectra, and the results were plotted as three-dimen- sional graphs by computer. With the aid of these graphs, the action spectra inves- tigated have been divided into six groups on the basis of the way in which Py- changed with depth in each water type.
The changes which characterize each group are summarized in Table 1, togeth- er with the corresponding action spectra, and three-dimensional graphs for two representatives of each group are shown in Fig. 2. The action spectra from which these 12 graphs were calculated are shown in Fig. 3.
The major physiological/taxonomic di- visions between the species investigated are reflected in the groupings in Table 1, in that group 1 consists entirely of green algae, groups 2 and 3 consist of brown algae, and groups 4-6 consist of red and blue-green algae-the phycobilin-con- taining species. The subdivision of the last into three groups corresponds largely to an ecological classification of these species, since group 4 contains red algae (Porphyra spp.) of the upper eulittoral zone, group 6 contains the deep sublit- toral species, and group 5 contains species growing at the intermediate depths, including a species with a thick (and almost black) thallus, Chondrus crisps, and a sublittoral blue-green alga Phormidium.
The brown algae subdivide largely on the basis of thallus structure, with species having thin thalli in group 2, while the mature sporophyte of Lumi- naria falls into group 3. This action spec- trum is the closest that we come to our hypothetical black alga, since Chondrus exhibits large variations in its action spectrum (Fig. 3) in spite of almost com- plete absorption at all wavelengths. Ga- metophytes of Laminaria saccharina grown in red light (Liining and Dring 1975) also exhibit a surprisingly flat ac- tion spectrum-the sharp (and probably exaggerated) peak at 675 nm contributes little to the total photosynthesis in most light fields-and so this action spectrum has been included as a second example in group 3, in spite of the obvious mor- phological affinity of the gametophytes to the other plants in group 2. The calcula- tions based on this spectrum are probably better regarded as a somewhat artificial illustration of how a flat action spectrum affects photosynthetic performance in
Tabl
e 1.
C
lass
ifica
tion
of a
ctio
n sp
ectra
ac
cord
ing
to p
redi
cted
ph
otos
ynth
esis
(P
T) c
alcu
late
d fo
r di
ffere
nt
dept
hs
(O-1
0 m
) in
all
wat
er
type
s.
Det
aile
d re
sults
fo
r fir
st
two
exam
ples
in
eac
h gr
oup
are
give
n in
Fi
gs.
2,4,
5,
6 a
nd
Tabl
e 2,
and
co
rresp
ondi
ng
actio
n sp
ectra
in
Fi
g.
3.
Gro
up
1 G
roup
2
Gro
up
3 G
roup
4
Gro
up
5 G
roup
6
Res
pons
e of
PT
to i
ncre
ase
of d
epth
in
: oc
eani
c gr
adua
l in
crea
se
stee
p in
crea
se
wat
er
clea
r coas
tal
turb
id
coas
tal
grad
ual
decr
ease
stee
p de
crea
se
grad
ual
incr
ease
decr
ease
Exam
ples
* U
lna
taen
iata
l
Uln
a la
ctuc
a2*3
C
oilo
desm
e sp
.1
Lam
inar
ia
sacc
harin
a yo
ung
spor
ophy
te”
L. s
acch
arin
a:
blue
-gro
wn
gam
etop
hyte
s4
Scyt
osip
hon
Eom
enta
ria:
blue
- an
d re
d-
grow
n5
Mem
bers
hip
all
gree
n al
gae
brow
n al
gae
with
te
sted
th
in
thal
li
Abbr
ev.
(Fig
s.
4-6)
G
Bl
rela
tivel
y lit
tle
chan
ge
in
any
wat
er
tn=
Lam
inar
ia
sacc
harin
a m
atur
e sp
orop
hyte
2 L.
sac
char
ina
: re
d-gr
own
gam
etop
hyte
4
brow
n al
gae
with
th
ick
thal
li or
fla
t ac
tion
spec
tra
B2
stee
p de
crea
se
decr
ease
stee
p in
crea
se
Porp
h yr
a pe
rfora
ta
“gre
en
thal
lus”
l P.
um
bilic
alis
”- P.
per
fora
ta
gree
n-gr
own7
C
yan
idiu
m
cald
arum
’
red
or b
lue-
gr
een
alga
e w
ith
PC >
PE
i; up
per
eulit
tora
l
Rl
little
ch
ange
incr
ease
stee
p in
crea
se
Pho
rmid
ium
sp
.’
Cho
ndru
s cr
ispu
s 2
Porp
hyra
pe
rfora
ta
“red
thal
lus”
’ P.
per
fora
ta
blue
-gro
wn7
P.
nai
adum
1
red
or b
lue-
gr
een
alga
e w
ith
PE >
PC
; m
ideu
litto
ral
to u
pper
su
blitt
oral
R2
stee
p in
crea
se
stee
pest
in
crea
se
stee
p in
crea
se
Del
ess
eria
sa
ngui
nea
D.
deci
pien
sl
Gril
ffith
sia
mon
ilis8
Hal
arac
hnio
n SP
.~
Myr
iogr
amm
e sp
.’ O
dent
halia
*
dent
ata9
Po
rphy
rella
sp
.’ Sc
hizy
men
ia
paci
$ca’
Bo
nnem
aiso
nia
sp.1
0
red
alga
e w
ith
little
PC
; su
blitt
oral
on
ly
R3
* R
efer
ence
ke
y:
’ Ha
xo
and
Blin
ks
1950
; *
Liin
ing
and
Drin
g (u
npub
l.);
3 Ha
lldal
lQ
64;
4 Li
inin
g an
d Dr
ing
1975
; 5
Drin
g an
d Li
inin
g 19
75;
6 Ha
lldal
19
69;
’ Yo
cum
an
d Bl
inks
19
58;
a La
rkum
an
d W
eyra
uch
1977
; 9
Halld
al
1974
; lo
Tra
illiel
la
phas
e:
Halld
al
1964
. t
PC-p
hyco
cyan
in;
PEph
ycoe
ryth
rin.
276
1.6~ 1. Ulva taeniata
Dring
2. Ulva lactuca Z Porphyra perforata 8. t? umbilicalis A-5
1 6. Laminaria kg.) 1 tl.&ksse&sqxhea 12. D. decipiens
li, Depth (ml0
5 10
,g 2.0 1. Uiva taeniata
c L E 8 1.0 3
2 a
b a.
Chromatic ndap ta tion
2. Ulva lactuca I Z Pof-phyra petibfata
700 400 500 600 700 400 500 600 700
Wavelength (nm) Fig. 3. Twelve representative action spectra of photosynthesis from benthic marine algae used for
cnlcnlations of photosynthesis. Sources for spectra in Table 1.
different light fields, rather than as a re- alistic prediction of the performance of Luminaria gametophytes in nature.
A critical test of the theory of chromatic adaptation requires that the photosynthe- sis of different species he compared un- der the same spectral conditions. All red algae show a slight positive adaptation (i.e. P,/< > 1.0) to the spectral distribution of Ii&t at the surface of the sea under clear skies, whereas green algae and most browns show a slight negative adaptation (Fig. 4). As depth increases down to 10 m in water types 5 and 9, the predicted photosynthesis of the red algae (groups RI-R3) increases and that of the greens and thin browns (G and Bl) decreases, while the thick browns (B2) show rela-
tively little change with depth (Fig. 4; Table 1). In oceanic water type I, how- ever, the photosynthesis of the green and brown algae increases with depth, whereas two groups of red algae (RI and R2) decrease or show little change. Nevertheless, the third red algal group (R3) increases faster than groups G and Bl down to 10 m (Fig. 4). Thus, at all depths down to 10 m in all water types, red algae show an increased photosyn- thetic lead over the green and brown al- gae compared with the surface, but this lead is much greater in coastal waters (types 5 and 9) than in oceanic waters (type I: Fig. 4).
Another effect of increasing depth is to differentiate between the different groups
Fig. 2. Predicted photosynthesis (Py.) calculated for 12 representative action spectra from marine algae at depths of O-10 m in 14 water types. Surface conditions: sun + sky, 45”. Each graph contains 14 c&es representing oceanic water types I, IA, IU, II, and III, and coastal water types l-9. Sources for spectra in Table 1 (y.s.-young sporophyte; m.s.-mature sporophytc; r.g.-red-grown gametophytes),
278
Depth:
- 1*3- surface
iY “2- Water type: I
Dring
f; C
x 1’2* Water type: 5 ,o g PO- +
73 2 v o+-
z E
l-4- 'h -P
1.2- Water type: 9
l.O- -
OfI- #JiTb
0.6- G 81 82 Rl R2 R3 G Bl B2 Rl R2 R3 G 8182 Rl R2R3 G 81 B2 Rl R2 R3 G BlB2 Rl R2 R3
Fig. 4. Predicted photosynthesis (Pr) for 12 representative action spectra at the surface and at four depths in each of three contrasting water types. Surface conditions: sun + sky, 45”. Each group of histo- grams represents the following spectra, from left to right (details in Table 1): G-green algae (group 1: Ulna taeniata; U. lactuca); Bl-“thin” brown algae (group 2: Coilodesme; Laminaria saccharina-young sporophyte); B2-“thick” brown algae (group 3: Laminaria saccharina- mature sporophyte; L. sacchar- ina-red-grown gametophyte); Rl-upper culittoral red algae (group 4: Porphyra perforata-“green thal- lus”; P. umbi2icaZis); R&red and blue-green algae from intermediate depths (group 5: Phormidium; Chondrus); R3-deep sublittoral red algae (group 6: Delesseria sanguinea; D. decipiens).
of red algae, and particularly between those in which phycocyanin is the dom- inant photosynthetic pigment (Porphyra spp.: Fig. 3) and those which possess al- most no phycocyanin (Delesseria spp.: Fig. 3). At the surface and at 1 m, the species in groups Rl-R3 all show very similar photosynthesis, but, at all depths from 2 to 10 m in clearer waters (types I and S), R3 species (the “phycoerythrin reds” from the deep sublittoral) have the highest values of PT, whereas Rl species (the “phycocyanin reds” from the upper
eulittoral) take the lead at all depths in more turbid waters (type 9: Fig. 4). The effects of different water types on pre- dicted photosynthesis at a single depth (10 m) are shown in more detail in Fig. 5. R3 species have the highest values in oceanic waters and in coastal water types 1-5, but Rl species gradually overtake the sublittoral red algae as the water be- comes more turbid and achieve the high- est values in water types 7-9.
Because of the clarity of oceanic waters, benthic algae are found at depths
Chromatic adaptation 279
Water type: I III 1
_ Sun + sky. 45”
&C
.* E [L 0.6 G 8182RlRZR3 G Bl82RlRZR3 G 8182RiRZR3
3
,.lrl ; B182Rl R2R3 F 8182RlRZR3 G l3182Rl R2R3 G 8182R1,
Fig. 5. Predicted photosynthesis (PT) for 12 representative action spectra at 10 m in each of seven water types. Details as in Fig. 4.
well below 10 m in water types I-III, provided that a suitable substrate is avail- able for their growth (e.g. vertical under- water cliffs: Crossett et al. 1965; coral reefs: van den Hoek et al. 1978), and so the predicted photosynthesis for the same 12 action spectra has been calculat- ed for greater depths (lo-100 m) in type I water (lo-70 m shown in Fig. 6). These results indicate that the photosynthetic lead predicted for the deep sublittoral reds (R3) at 10 m (see Figs. 4, S) gives way to greater photosynthesis by the browns (especially group B 1) at 20 m, and the photosynthesis of the green algae also begins to increase rapidly. As depth increases further, the gap between the green and the brown algae gradually nar- rows, until Ulva taeniata and Coilo- desme are virtually level at 100 m. Even the slower rise in the photosynthesis of Ulva Zuctuca with depth is sufficient to
Water type: I Depth:
10 m 20 m 30 m
enable this species to draw level with the mature Laminaria sporophyte at 50 m and to show greater photosynthesis than Laminaria at 60-100 m.
The high photosynthesis predicted for green and brown algae at extreme depth in oceanic waters is emphasized in Table 2, which shows values of P,. for all 12 ac- tion spectra at the greatest depth at which multicellular algae are known to grow in each water type. Ulva taeniata and Coil- odesme have the highest values in ocean- ic water type I, and almost all red algae have values well below 1.0. Even in type II, however, Delesseria decipiens has the highest value, and the lead of the red al- gae over the greens and the browns is maintained and enlarged throughout the coastal water types.
I have not reported the results of the calculations for clouded sky conditions as they differed little from those for clear
50 m 60m 70 m
% ; 06L GBlstfflRIR3 GW82RlR2R3 G8182RlR2R3 G8182NR2R3 G8182RlR2R3 G B182Rl R2R3 G 8l82RlR2R3
Fig. 6. Predicted photosynthesis (PT) for 12 representative action spectra at depths of lo-70 m in oceanic water type I. Surface conditions: sun + sky, 45”. Details as in Fig. 4.
280 Dring
Table 2. Predicted photosynthesis (PT) for 12 representative action spectra at maximum depths (m) at which multicellular algae are known to grow in each water type (Liining and Dring 1979). Two highest values in each column shown boldface.
skies. The largest differences were re- corded near the surface, where the eco- logical significance of the model is most limited (see discussion).
Discussion The model used here assumes that the
photosynthetic effects of individual wavelengths on any one species are in- dependent of other wavelengths in the same light field and that these effects are additive. The Emerson enhancement ef- fect clearly invalidates this assumption for mixtures of two monochromatic light sources which activate different photo- systems, but recent measurements have indicated that enhancement makes a neg- ligible contribution to the total photosyn- thesis of green, brown, and some red al- gae in “white” light that is similar in quality to underwater light (Liining and Dring unpubl.). McCree (1972) reached a similar conclusion for higher plants photosynthesizing in a variety of white light fields. The measured photosynthe- sis of other red algae (species in groups 4 and 5) was 510% higher than predict- ed values in some light fields and this discrepancy could be attributed to en- hancement, but corresponding correc- tions to the predictions reported here would tend to reinforce, rather than
change, the conclusions that have been reached.
The ecological interpretation of the re- sults from the model is complicated by the fact that the action spectra used only apply to light-limited photosynthesis. As irradiance increases, the action spectrum for an individual plant or culture be- comes progressively flatter until, at com- plete light saturation, photosynthesis is independent of the spectral composition of the light (Smith 1968) and, therefore, of the pigment composition of the plant. Thus, the predictions from the model are only valid under relatively low irradi- antes, in which photosynthesis is strictly light limited, but-it should be stressed- the application of the theory of chromatic adaptation is subject to exactly the same limitations.
This consideration, alone, casts doubt on the standard interpretation of the pat- tern that is so commonly observed in the vertical distribution of benthic marine algae (at least, in coastal water types), with blue-green and green algae largely restricted to the upper eulittoral zone, the brown algae dominating most of the eulittoral and the upper part of the sub- littoral, and the reds penetrating most deeply into the oceans. Each group, it is generally argued, is neatly positioned
Chromatic adaptation 281
just where the color of the light is com- plementary to the color of the thallus and where, therefore, the photosynthetic ap- paratus can make the most efficient use of the incident wavelengths. Since the irradiance at the surface will normally be greater than that required to saturate pho- tosynthesis, the observed dominance of greens and browns over reds near the surface cannot be attributed to their pig- ment composition.
This conclusion is reinforced by the re- sults from the model, which indicate that red algae are better adapted chromatical- ly to photosynthesize at all depths down to 10 m in all water types and that they show a narrow advantage over green and brown algae at the surface (Fig. 4). Thus, the pigment composition of green and brown algae does not adapt them well to the spectral composition of light near the surface, even at low irradiances, and the ecological success of such plants in these habitats may owe more to their ability to utilize high irradiances of light than to their “chromatic adaptation.” Halldal (1974, p. 359) h as also concluded that brown and green algae near the surface are “not particularly adjusted to the pre- vailing light.”
As depth increases, irradiance de- creases exponentially and the photosyn- thesis of benthic plants will become in- creasingly light limited. It is very difficult to define a critical depth-or depth range-below which photosynthe- sis will be controlled by light, but it is fairly certain that, wherever suitable sub- strate is available, the maximum depth at which benthic plants grow will be deter- mined by the prevailing light climate. The model can be used with some con- fidence, therefore, to predict photosyn- thetic rates per incident quantum at these depths (Table 2). The results indicate that the red algae of group 6 (Dehseria spp.) are the best adapted chromatically in a broad central range of water types (oceanic III to coastal 5), and this is in agreement with field observations that such plants-foliose and crustose red al- gae with very little phycocyanin-gen-
erally dominate the flora near the depth limit for benthic plant growth. The pre- dictions (Table 2) suggest, however, that in both extremely clear and extremely turbid water types (oceanic I and II; coastal 7 and 9) the DeZesseria species are less well adapted than other groups of algae and that they should lose their ecological dominance in such waters. Thus, we might expect that green algae or thin brown algae would penetrate most deeply in oceanic waters and that phycocyanin-containing algae (e.g. Por- phyra spp. or blue-greens) would pene- trate most deeply in the more turbid coastal waters. Neither of these predic- tions is supported by field observations. Group 6 reds are the commonest algae at depth in all water types.
It is true that green and brown algae occur at greater depths in oceanic waters than in coastal waters (e.g. Crossett et al. 1965; Gilmartin 1960), and there is recent evidence that deep-water green algae possess an extra photosynthetic pigment, siphonoxanthin (Kageyama et al. 1977; Sears and Cooper 1978), which appears to increase their chromatic adaptation in such waters. No action spectrum of pho- tosynthesis is yet available for a siphono- xanthin-containing alga, but the predict- ed photosynthesis for such algae in deep oceanic waters may well be higher than that predicted for the eulittoral Ulva species tested in this investigation, so that the reds would be at an even greater disadvantage than is suggested by Fig. 6. Nevertheless, red algae penetrate as deeply as, and frequently deeper than, green and brown algae in oceanic waters (Berthold 1882; Larkum et al. 1967; van den Hoek et al. 1978), in spite of their poorer chromatic adaptation, At the other end of the water-type scale, there is no evidence that Porphyra species, for ex- ample, can penetrate the sublittoral in turbid coastal waters, so that, again, group 6 reds appear to be dominant in spite of their relatively poor chromatic adaptation.
The results of this theoretical investi- gation suggest, therefore, that the ecolog-
282 Dring
ical significance of chromatic adaptation may be far more limited than has often been assumed, and we should perhaps consider the current status of its old an- tagonist “intensity adaptation” (Berthold 1882; Oltmanns 1892). It is of interest here that the changes in pigment com- position that have been observed or in- duced in marine algae at increased depths are qualitatively similar to those induced by experimental reductions in light quantity, but there are few reports of parallel changes being induced by al- terations in light quality. This contrasts with the wealth of evidence from labo- ratory studies that the pigment composi- tion of freshwater blue-green algae does adapt to the spectral composition of the light they are grown in (Bogorad 1975; de Marsac 1977).
In red algae, for example, the phycoer- ythrin:chlorophyll a (PE: Chl) ratio of Porphyra and Chondrus has been ob- served to increase with depth (Ramus et al. 1976; Rhee and Briggs 1977), and this change can be--and usually has been- interpreted as a chromatic adaptation, Exposure of Porphyra and Porphyridium to green light in the laboratory, however, resulted in a decrease in the PE:Chl ratio (“inverse chromatic adaptation”: Yocum and Blinks 1958; Brody and Brody 1962), although Porphyridium did exhibit pos- itive chromatic adaptation to very low ir- radiances of green light (Brody and Emerson 1959). When higher red algae (Florideae) were grown in green light for 10 days, no changes in pigment compo- sition could be detected (Yocum and Blinks 1958). A recent claim that Eu- cheuma shows cjhromatic adaptation of its pigment composition (Moon and Dawes 1976) is not supported by the data pre- sented, since the plants were not exposed to different light qualities, but were col- lected from a single depth at different times of the year. There are several re- ports, however, that the PE:Chl ratio of red algae (both Bangioideae and Florid- eae) increases in response to decreased light intensity, both in laboratory exper- iments (e.g. Porphyridium: Brody and Emerson 1959; Gracilaria : Calabrese
and Feli cini 1973; Grifji thsia : Waaland et al. 1974) and in field material (Por- phyra and Chondrus: Ramus et al. 1976; Chondrus: Rhee and Briggs 1977).
Less evidence is available concerning pigment changes in green and brown al- gae, but Ramus et al. (1976) observed that Ulva and Codium which were grown for 7 days at 10 m had a higher Chl b:Chl a ratio than plants grown at 1 m, and a sim- ilar difference was observed between plants collected from shaded and from sunlit habitats. The Chl b :Chl a ratio of other green algae (microscopic freshwa- ter species) has also been found to in- crease as light quantity decreased (Brown and Richardson 1968), and similar obser- vations have been made on higher plants (e.g. Sauberer and Hartel 1959: table 85). Again, therefore, reduction in light quan- tity has the same effect as increasing depth. For the brown algae Fucus and Ascophyllum, Ramus et al. (1977) found that plants grown at 4-m depth had a low- er fucoxanthin: chlorophyll a ratio than plants grown at the surface, although this ratio would be expected to increase with depth if chromatic adaptation was occur- ring. A comparison of plants from shaded and sunlit habitats again showed that the effects of shade were the same as those of depth (Ramus et al. 1977), and a similar decrease in fucoxanthimchlorophyll a ra- tio was observed with decreasing irradi- ance in Sphacelaria and Nitzschia (Brown and Richardson 1968). The pig- ment changes that have been found with depth in Fucus and Ascophyllum are clearly not, therefore, chromatic adapta- tions, but intensity adaptations, and all of the evidence concerning red and green algae is consistent with the same inter- pretation, The only unequivocal evi- dence for chromatic adaptations of the pigment composition of algae would seem, therefore, to come from the Cya- nophyta (e.g. de Marsac 1977), and it was this group which provided the early ex- perimental evidence for Engelmann’s theory (Gaidukov 1903). Even here, we should perhaps question whether the ad- aptation has any ecological significance, since McCarthy and Carpenter (1979)
.
Chromatic adaptation
could detect no differences in the absorp- tion spectra of a marine Oscillatoria from 5-, 25-, and 50-m depth.
The beginning of the end of the pro- longed conflict between chromatic ad- aptation and intensity adaptation may lie in the clarification of the effects of light quality and light quantity on the pigment composition of red algae. The work re- viewed above suggests that phycoery- thrin concentrations increase in response to low irradiances, and not in response to green wavelengths, of light. If this is con- firmed, it will be clear that the increased chromatic adaptation of red algae in deep coastal waters, which was demonstrated by Levring (1947) and has been con- firmed by my investigation, is not the cause of their ecological success in such habitats, but is merely an accidental by- product of their physiological adaptation to low irradiances. Chromatic adaptation in marine algae could then perhaps reap- pear in undergraduate lectures and text- books wearing a new hat-as a cautionary tale illustrating the mean tricks that Na- ture sometimes plays on us, such as dressing up one form of adaptation to look like another.
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Submitted: 26 September 1979 Accepted: 17 September 1980
