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Light, Zonation and Biomass of Submerged Freshwater Macrophytes
Light, Zonation and Biomass of Submerged Freshwater Macrophytes D. H. N. S P E N CE Department of Botany, University of St. Andrews, Scotland 1. Introduction . . . . . 2. Light, Specific L e a f Area and Zonation 3. Depth Limits of Colonization 4. Biomass M a x i m a and Depth Distribution Acknowledgements . . . . References . . . . . .
335 336 340 342 345 345
1. Introduction This chapte r is concerne d with the freshwate r analogue s of attache d marine angiosperm s and algae, the fully submerge d macrophytes , which mainly compris e floweringplants but include mosse s and larger algae (Characea e or stoneworts) . In it, a look is taken at the extent to which light may determin e the vertica l distributio n of thes e plants and their biomas s This is part of a broade r study of factor s controllin g the genera l distributio n and performanc e of freshwate r macrophyte s (Spence , 1964, 1967; Spenc e and Crystal , 1970a, b; Spenc e et aL, 1973) that has include d analysi s of underwate r spectra l intensit y (Spenc e et aL, 1971). Loch Uanaga n in Inverness-shir e provide s an exampl e of the vertica l distributio n of submerge d vegetatio n in terms of biomas s per unit area at various depth s of water (Fig. 1). Data were collecte d in Augus t 1967 by diving, mostly with snorkel . Figure 1 (a) show s total biomas s of all submerge d specie s in relation to increasin g rooting depth , or the depth of water above the soil surfac e in which each plant is rooted , along a transec t while Fig. 1 (b) indicate s zonatio n with increasin g rooting depth in terms of the relative maxima l performanc e of each of a serie s of species . Potamogeton praelongus Wulff has a peak in deepe r water than Littorella uniflora L. and it may be asked whethe r this is typical of thes e specie s and if so whethe r there exist habitua l deep-wate r species ; Fig 2 which is base d on data from an extensive , earlier, surve y of Scottis h lochs (Spence , 1964) show s that there are. For example , Potamogeton 335
336
D. H. N. SPENCE
obtusifolius Mert. and Koch is rooted in significantl y deepe r water than Potamogeton polygonifolius Pourr . 400 300
Loch Uanagan
A
-
Ï σ
100 80 60 40
M.alterniflorum
y \ Pperfoliatus
"Lobelia —
8
ι
Rzizii
40
-
I
100 80 60 40 20
/
/
\
\
J.bulbosus var.f lui tone
n^r" ι ι ι ι L 4 0 80 120 160 200 240 280 320 360 4 0 0 Depth of water cm 2 FIG. I. (a) Biomass in g oven-dry weight per m of all submerged species in relation to rooting depth, or depth of water (cm) above the surface of the soil where they were rooted ; sample areas exclude reedswamp. Loch Uanagan 13 August 1967. Arrow indicates base of littoral shelf, (b) Biomass of named species at sampled rooting depths as percentage of total biomass of all species at that sample depth (All data collected by hand by P. Denny and author; redrawn from Spence 1972). 0
2. Light, Specific Leaf Area and Zonation Flowering plants have the capacit y in varying degre e to adjus t leaf morpholog y to sun and shad e condition s by altering their thicknes s 2 and their specifi c leaf areas ( S L A: cm leaf area/mg leaf dry weight) (Evans and Hughes , 1961). Sun leaves are thick with a low S LA while shad e leaves are thin and have a high S L A. In additio n to their
LIGHT,
337
ZONATION A N D BIOMASS O F M A C R O P H Y T E S
mutuall y exclusiv e rooting depth s in nature , Spenc e and Chrysta l (1970) found that P. obtusifolius and Ρ. polygonifolius produce d mutuall y exclusiv e specifi c leaf areas when grown in sun and shad e condition s in a glasshouse , and that the larger was the S LA the smalle r was the dark e leaf achieve d a respiratio n rate per unit area. As a result a shad , in the higher net photosyntheti c rate per unit area at low irradiance . range 400-750 nm, than a sun leaf at that irradiance R polygonifolius
I—I—I—I
P notons
1
I— I
P fil liformis
1
hi
Rx zizii
1 I
R gramineus
1
1
1
1
I—I
R obtusi f olius
1
1
1
1 1
1
I-1
·
"
1
1
Ρ praelongus
-40
Ο
40
80
120
160
200
240
280
320
360
Depth (cm)
F I G . 2. Mean, standard deviation and range in depth of water at which a number of Potamogeton species are rooted in Scottish lochs (redrawn from Spence and Chrystal 1970a).
These observation s suggeste d that range in S LA is an intrinsi c characteristi c of a specie s which can in nature relate directly to zonation (Spenc e and Chrystal , 1970b). Using SCUBA, whole shoot s of selecte d specie s were subsequentl y collecte d from precisel y measure d depth s in five lochs (Table 1) and specifi c leaf areas were estimate d on 10 cm stem segments . Analysis and discussio n of thes e data have been publishe d (Spenc e et aL, 1973) and only some of the findingsare outlined here. The relationshi p betwee n S LA and depth of water is illustrate d in Fig. 3 for pairs of species , on single samplin g dates in two lochs , as a serie s of regressio n lines for each of which the correlatio n coefficien t betwee n S LA and depth is significan t at the 5% level or less. The regressio n lines of Potamogeton χ zizii Roth, and P. perfoliatus L . in Loch Bailie na Ghobhain n show that the slope of S LA with depth is typical of the loch and not of the species . There is a seasona l increas e of S LA of P. obtusifolius over the water depth 210-270 cm in the brown-wate r Loch of Lowes (Fig. 4) but no such increas e in S LA of Potamogeton praelongus in the much less brownwater Loch Lanlish (Fig. 5). Such attenuatio n data as there are indicat e
338
D. H. N. SPENGE
a seasona l increas e of Ee, 400-750 nm, in Loch of Lowes over this period but little chang e in Loch Lanlish (by Loch Croispol , Table 1), which suggest s that variatio n in shadin g rathe r than in other environmenta l or ontogeneti c factors cause s seasona l drift in S L A. The S LA field range for P. obtusifolius (Fig. 4), is 1.43 to 1.98, compare d with a laborator y range of 1.60 to 2.05. For P. perfoliatus. T A B L E 1. Lochs in which specific leaf areas have been measured, with m a p references and, where appropriate, attenuation coefficients (Ee), 400-750 nm, or EB, EG, ER.
1
M a p ref.
E.
Bailie na Ghobhainn, Lismore Croispol, Durness
N M 860425 N C 390680
0.50 0.56 0.55 0.57
Lanlish, Durness Lowes, Dunkeld
N C 388680 N O 050440
U a n a g a n , Fort Augustus
N H 370070
— 0.76 1.20 1.30 1.50
Loch
Ε In units
EB E G
2
ER
0.29 0.18 0.43
0.77 0.360.56
0.97 0.60 0.59 0.62 0.37 0.43
1 Measured
Date
24.6.69 19.6.70 4.8.70 16.9.70 August 1974 30.4.70 14.5.70 18.8.70 15.7.70 2
with spectroradiometer over 1 m (Spence et aL, 1971) or, , with blue(OB), green(OG) or r e d ( O R ) Chance filters, J u n e - A u g u s t (Spence 1975).
2
Specific leaf area ( c m mg ') 0-6
0-8, , 0 - 4
0·6
0-8
ΙΌ
1-2
1-4
80 £ - 160 \_ ω i 240 ο i 320 Q
400 480
.
v~
.
F I G . 3. Linear regressions of specific leaf area upon depth of water, of which the correlation coefficients are significant at the 5% level or less. Least and greatest error mean square are indicated. Loch Bailie na Ghobhainn: Potamogeton crispus (\/),P. perfoliatus ( • ) 24 June 1969. Loch Uanagan: P. χ zizii (A), P. perfoliatus ( Π • )» 12 August 1969; P. perfoliatus (• • ) , 14 July 1970. (Redrawn from Spence et al, 1973.)
LIGHT, ZONATION AND BIOMASS OF MACROPHYTES
A
M
J
J
A
339
S
Month F I G . 4. Seasonal variation in mean SLA (with standard errors) of Potamogeton obtusifolius over the water depth 210-270 cm in Loch of Lowes, 1970, a brown-water loch. (Redrawn from Spence et al, 1973.)
F I G . 5. Linear regressions of specific leaf area upon depth of water, of which correlation coefficients are significant at the 5% level or less, for Potamogeton praelongus in Loch Lanlish on various sampling dates in 1970. (Redrawn from Spence 1972.)
340
D. H. N. SPENCE
field values extend from 0.55 to 1.75 and, in the glasshouse , from 0.80 to 2.20. Thus the range in S LA of each specie s overlap s with the other and is matche d in laborator y and field. Since any two such specie s have differen t capacitie s for shoo t extension , they may have mutuall y exclusive rooting range s in a particula r site like P. χ zizii and P. perfoliatus in Loch Uanaga n (Fig. 3) or both their rooting range s and their specifi c leaf areas may overlap , as with P. crispus L . and P. perfoliatus in Loch Bailie na Ghobhain n or P. obtusifolius and P. perfoliatus in Loch of Lowes, when substratu m rathe r than irradianc e must determin e their zonation . We still canno t directly test the hypothesi s that, subjec t to modificatio n on many shore s by factor s like turbulenc e or substratu m or competitio n which are not strictl y depth-controlled , light determine s the potentia l depth range of a specie s (Spence , 1967), since we lack field measurement s of any two specie s that do not have overlappin g specifi c leaf areas in the laboratory . P. polygonifolius for instanc e was absen t from all our sites . Moreover , presentl y availabl e evidenc e concerns specie s from the same genus . However , using indirec t evidenc e it would seem certain that if the specifi c leaf areas at least of two related specie s do not overlap then neithe r can their rooting range s which, given the known relationshi p betwee n S LA and function , would then be a direct caus e of zonation . 3. Depth Limits of Colonization The photic zone in freshwate r is very much shallowe r than in the sea and it is seldo m necessar y in the United Kingdom to dive below 10 m to study attache d plants which rarely penetrat e anywher e nearly as deep as this. A brief outline follows of limits of colonization , and of biomass , in relation to depth of water. The limeston e Loch Bailie na Ghobhain n on Lismore was visited becaus e West (1910) reporte d "dens e beds " of the aquati c moss Fontinalis antipyretica L . at 13.1 m depth , suggestin g that this loch was colonize d to amongs t the greates t depth s of any in Scotland . Diving reveale d howeve r that while plants occurre d to a depth of 13.1 m thes e were only fragment s below 6 m, excep t at the very narrow ends of the loch. In J u ne 1969, the loch was thermall y stratifie d with a clear epilimnio n down to 6 m and, below, both thermo cline and hypolimnio n containe d large quantitie s of suspende d matter which produce d opaqu e layers with considerabl e attenuatio n but there was no stratificatio n in Augus t 1974. As determine d by diver surve y the shore again exceptin g its narrow ends has a gradien t of 1 in 4 to a depth of 5 m ; there, 1 m above the lower limit of continuou s vegetation , it suddenl y steepen s to 1 in 1.05. Either the instabilit y of this marl slope , or the existenc e at 6 m of the intermittent , opaqu e thermocline , cause s
LIGHT, ZONATION AND BIOMASS OF MACROPHYTES
341
an apparentl y prematur e limit to downwar d penetratio n of macrophyte s in most of this loch. Data are also availabl e for two more limeston e lakes, Lochs Borralie and Croispo l at Durnes s in Sutherlan d which are unstratifie d and of the same water colour , clarity and homogeneit y (Spence , unpublishe d data), resemblin g the epilimnio n in Loch Bailie na Ghobhain n and the clear coasta l waters of the Moray Firth describe d by Hemming s (1966). Vascula r plants do not grow in either loch below 6 m depth of
Plant cover: per cent
F I G . 6. Temperature profiles for Loch Spiggie, Shetland, (July), Loch of Lowes (August) and Loch Bailie na Ghobhainn (June), together with available data on depth of colonization, 2 percent plant cover, and oven dry weight of crop in g/m ( # — · ) (all data obtained by diving).
water; as in Loch Bailie na Ghobhain n this is also the downwar d limit for all attache d macrophyte s in Loch Croispol , wherea s in Loch Borralie specie s of Charophyta , mainly Nitella opaca, which is absen t from Loch Croispol , have been found by diving to form beds of vegetatio n down to 1 1m depth of water. Our experimenta l evidenc e is insufficien t as yet to explain the difference s in depth s of colonisatio n in these three limestone lochs or the fact that the angiosperm s {Potamogeton species ) ceas e to grow at the same depth in each. Furthe r example s are given in Fig. 6 of the commone r situatio n where there is no therma l stratificatio n even in relativel y calm weathe r or, if it is present , where the epilimnio n extend s well below the lower
342
D. H. N. SPENGE
limits of attache d vegetation . On anothe r count this may be the commoner situatio n at least in the United Kingdom , becaus e Loch Spiggie and Lowes represen t the brown coloure d water of low alkalinity 1 ( < 0 .3 m eq à H G 0 3 + C 0 3= + O H ") on the greates t length of shorelin e in Scottis h freshwate r lochs (Spence , 1964) and indicate , therefore , the sort of depth s to which attache d plants usuall y penetrate . I t is not of cours e as simple as that since there are also nutrient-poo r waters of great clarity like Ennerdal e in the English Lake District where vegetatio n is reported , by using a grab, at 10 m (Pearsall , 1921) or Lake Grane Langso in Denmar k (Nygaard , 1958) where vegetatio n was found by diving at 11 m (Fig. 7). Biomass: dry weight
F I G . 7. Depth profiles of biomass in Lake Grane Langso (Denmark), Loch Uanagan, (Inverness-shire) (August), Loch Croispol (Sutherland) (June) and Lake Weber (Wisconsin). (Data for first three obtained by diving; data for Lake Weber obtained with a grab and expressed as percent weight per 1 metre depth interval; lower graph for Loch Uanagan also on this basis for comparison.) Lake Grane Langso data adapted from Nygaard (1958), Lake Weber data from Potzger and Van Engel (1942).
4. Biomass Maxima and Depth Distribution I t may be noted in Fig. 7 that biomas s tends to reach a maximu m in about 1.0 to 1.5 m depth of water while in the clear limeston e Loch Borralie this maximum is reache d betwee n 3 and 4 m. Biomas s in Loch Uanagan along with the intrinsi c statur e of the specie s (Fig. 1) decrease s steadil y with depth; biomas s decreas e is in fact logarithmi c (Fig. 8) suggestin g that, for the given level of nutrient s in this moderate ly alkaline loch, biomas s is limited by irradiance , which is also reduced or attenuate d logarithmicall y with depth in this opticall y homogeneou s medium (Spenc e et aL, 1971). Data are insufficien t so far
L I G H T , Z O N A T I O N A N D BIOMASS OF M A C R O P H Y T E S
343
to confirm or refute the existenc e of such a biomas s trend from maximal values as the depth increase s in Loch Borralie or, indeed , in general . The water depth at which maximal biomas s occur s is worth a comment. In Loch Uanaga n this lies at and below the base of the littoral shelf (Fig. 1, arrow) while in Loch Borralie it coincide s with the slope of a less obvious , thoug h still discernible , littoral shelf in deepe r water. I t seem s likely that aspec t expresse d as excessiv e turbulenc e may directly , IOOO ι
—
1
500L-
Oepth of water ( c m ) F I G . 8. Semi-logarithmic plot of biomass weight in relation to water depth in Loch Uanagan. (Data as in Fig. 1.)
or indirectl y throug h soil particle size and substratu m chemistry , affect summe r growth of winter surviva l of macrophyte s and thus caus e limitation s in shallo w water. Unpublishe d data indicat e that the seasona l maximal biomas s is reach in August . Such maxima, (Fig. 7) are only exceede d by values of 2 Forsber g (1960) of 400 g over-dr y weight per m for nutrient-ric h Lake Osby in Swede n and approximatel y the same value for Loch Borralie . Even in water with the least attenuation , like that of Lochs Borralie and Croispol , biomas s is low relative to that in opticall y comparable , clear
344
D. H. N. SPENGE
coasta l seawate r (Fig. 9). This to an unknow n extent reflect s difference s in growth-form s and, therefore , in winter biomas s which, for some Potamogeton specie s that survive as overwinterin g buds , is as little as 1 /20th the summe r biomass . In situ productio n figures sugges t a more meaningfu l compariso n and are given in anothe r paper (Campbel l and Spence ) in this volume . I conclud e with an attemp t to summariz e thes e inter-relationships, , particularl y with regard to the role of light. The most bulky submerge d macrophyte s like Potamogeton praelongus produc e shoot s up to 3.5 m tall in the United Kingdom so that in standin g as oppose d to runnin g
40
F I G . 9. Comparison of submerged macrophyte biomass in Loch Uanagan and a marine site off Cornwall {Laminaria hyperborea forest) (Loch Uanagan data as for Fig. 1. Laminaria data from Bellamy and Whittick, 1968.)
water the zone of maximu m submerge d biomas s shoul d occur in not less than 3.5 m depth of water. In shallowe r standin g water, the submerge d biomas s is inevitabl y the produc t of smalle r plants . Excessiv e turbulenc e will directly or indirectl y limit this furthe r while the downward extensio n of crop maxima and indeed the depth s that any plant can grow depend s primarily on the degre e of light attenuation . This leads to the propositio n that the resultan t of the opposin g factor s of increasingl y excessiv e turbulenc e and high light attenuatio n determine s the rooting depth at which maxima l submerge d biomas s occur s on any shore . The chemistr y of the substratu m and the extent of grazing , and of periphyto n and sedimentar y cover on leaves , will thereafte r set the limits of the actua l submerge d maxima on a particula r shore .
L I G H T , Z O N A T I O N A N D BIOMASS O F M A C R O P H Y T E S
345
Acknowledgements T h e work on which this paper is based is supported by grants from the NaturalEnvironment Research Council. Thanks are due to Dr. Patrick Denny for his help in collecting the data presented in Fig. 1.
References Bellamy, D . a n d Whittick, A. (1968). K e l p forest ecosystems as a "phytometer" in marine pollution. Underwater Ass. Rep. 1967-68. Evans, G . C . and Hughes, A. P. (1961). Plant growth and the aerial environment I . Effect of artificial shading on Impatiens parviflora. New Phytol. 60, 150-180. Forsberg, R . (I960), Subaquatic macrovegetation in Osbyjôn, Djursholm. Oikos 10, 233. Hemmings, C . C . (1966). Factors influencing the visibility of objects underwater.
Light as an Ecological Factor (Eds. R . Bainbridge, G. G. Evans and O. Rackham), 359-374. Blackwell Scientific Publications, Oxford. Nygaard, G . (1958). O n the productivity of the bottom vegetation in L a k e Grane
Langso. Verh. int. Verein. iheor. angew. Limnol 13, 144.
Pearsall, W. H . (1921). T h e development of vegetation in the English Lakes, considered in relation to the general evolution of glacial lakes a n d rock-basins.
Proc. Roy. Soc. B, 92, 259-284.
Potzger, J . E . and Engel, W. A. V a n (1942). Study of the rooted aquatic vegetation
of Weber Lake, Vilas County, Wisconsin. Trans. Wis. Acad. Sci. Arts Lett. 34, 149.
Spence, D . H . N . (1964). T h e macrophytic vegetation of freshwater lochs, swamps and associated fens. The Vegetation of Scotland (Ed. J . H . Burnett), 306-425. Oliver and Boyd, Edinburgh. Spence, D . H . N . (1967). Factors controlling the distribution of freshwater macrophytes with particular reference to the lochs of Scotland. J. Ecol. 55, 147-170. Spence, D . H . N . (1972). Light on freshwater macrophytes. Trans. Bot. Soc. Edinb. 42, 491-505. Spence, D . H . N. (1975). Light and plant response in fresh water. Light as an Ecological Factor II. (Eds. R . Bainbridge, G . C . Evans and O . R a c k h a m ) . Blackwell Scientific Publications, Oxford. Spence, D . H , N . and J e a n Chrystal (1970a). Photosynthesis a n d zonation of freshwater macrophytes I. Depth distribution a n d shade tolerance. New Phytol. 69, 205-216. Spence, D . H . N . and J e a n Chrystal (1970b). Photosynthesis and zonation of freshwater macrophytes. I I . Adaptability of species of deep a n d shallow water. New
Phytol. 69,217-227.
Spence, D . H . N., J e a n Chrystal and Campbell, R . M . (1973). Specific leaf area a n d zonation of freshwater macrophytes. J. Ecol. 61, 317-328. Spence, D . H . N., Campbell, R . M . and J e a n Campbell (1971). Spectral intensity in some Scottish freshwater lochs. Freshw. Biol. 1, 321-327. West, Geo. (1910). A further contribution to the comparative study of the dominant phanerogamic a n d higher cryptogamic flora of aquatic habit in Scottish lakes.
Proc. Roy. Soc. Edinb. 25, 967-1023.
335 336 340 342 345 345
1. Introduction This chapte r is concerne d with the freshwate r analogue s of attache d marine angiosperm s and algae, the fully submerge d macrophytes , which mainly compris e floweringplants but include mosse s and larger algae (Characea e or stoneworts) . In it, a look is taken at the extent to which light may determin e the vertica l distributio n of thes e plants and their biomas s This is part of a broade r study of factor s controllin g the genera l distributio n and performanc e of freshwate r macrophyte s (Spence , 1964, 1967; Spenc e and Crystal , 1970a, b; Spenc e et aL, 1973) that has include d analysi s of underwate r spectra l intensit y (Spenc e et aL, 1971). Loch Uanaga n in Inverness-shir e provide s an exampl e of the vertica l distributio n of submerge d vegetatio n in terms of biomas s per unit area at various depth s of water (Fig. 1). Data were collecte d in Augus t 1967 by diving, mostly with snorkel . Figure 1 (a) show s total biomas s of all submerge d specie s in relation to increasin g rooting depth , or the depth of water above the soil surfac e in which each plant is rooted , along a transec t while Fig. 1 (b) indicate s zonatio n with increasin g rooting depth in terms of the relative maxima l performanc e of each of a serie s of species . Potamogeton praelongus Wulff has a peak in deepe r water than Littorella uniflora L. and it may be asked whethe r this is typical of thes e specie s and if so whethe r there exist habitua l deep-wate r species ; Fig 2 which is base d on data from an extensive , earlier, surve y of Scottis h lochs (Spence , 1964) show s that there are. For example , Potamogeton 335
336
D. H. N. SPENCE
obtusifolius Mert. and Koch is rooted in significantl y deepe r water than Potamogeton polygonifolius Pourr . 400 300
Loch Uanagan
A
-
Ï σ
100 80 60 40
M.alterniflorum
y \ Pperfoliatus
"Lobelia —
8
ι
Rzizii
40
-
I
100 80 60 40 20
/
/
\
\
J.bulbosus var.f lui tone
n^r" ι ι ι ι L 4 0 80 120 160 200 240 280 320 360 4 0 0 Depth of water cm 2 FIG. I. (a) Biomass in g oven-dry weight per m of all submerged species in relation to rooting depth, or depth of water (cm) above the surface of the soil where they were rooted ; sample areas exclude reedswamp. Loch Uanagan 13 August 1967. Arrow indicates base of littoral shelf, (b) Biomass of named species at sampled rooting depths as percentage of total biomass of all species at that sample depth (All data collected by hand by P. Denny and author; redrawn from Spence 1972). 0
2. Light, Specific Leaf Area and Zonation Flowering plants have the capacit y in varying degre e to adjus t leaf morpholog y to sun and shad e condition s by altering their thicknes s 2 and their specifi c leaf areas ( S L A: cm leaf area/mg leaf dry weight) (Evans and Hughes , 1961). Sun leaves are thick with a low S LA while shad e leaves are thin and have a high S L A. In additio n to their
LIGHT,
337
ZONATION A N D BIOMASS O F M A C R O P H Y T E S
mutuall y exclusiv e rooting depth s in nature , Spenc e and Chrysta l (1970) found that P. obtusifolius and Ρ. polygonifolius produce d mutuall y exclusiv e specifi c leaf areas when grown in sun and shad e condition s in a glasshouse , and that the larger was the S LA the smalle r was the dark e leaf achieve d a respiratio n rate per unit area. As a result a shad , in the higher net photosyntheti c rate per unit area at low irradiance . range 400-750 nm, than a sun leaf at that irradiance R polygonifolius
I—I—I—I
P notons
1
I— I
P fil liformis
1
hi
Rx zizii
1 I
R gramineus
1
1
1
1
I—I
R obtusi f olius
1
1
1
1 1
1
I-1
·
"
1
1
Ρ praelongus
-40
Ο
40
80
120
160
200
240
280
320
360
Depth (cm)
F I G . 2. Mean, standard deviation and range in depth of water at which a number of Potamogeton species are rooted in Scottish lochs (redrawn from Spence and Chrystal 1970a).
These observation s suggeste d that range in S LA is an intrinsi c characteristi c of a specie s which can in nature relate directly to zonation (Spenc e and Chrystal , 1970b). Using SCUBA, whole shoot s of selecte d specie s were subsequentl y collecte d from precisel y measure d depth s in five lochs (Table 1) and specifi c leaf areas were estimate d on 10 cm stem segments . Analysis and discussio n of thes e data have been publishe d (Spenc e et aL, 1973) and only some of the findingsare outlined here. The relationshi p betwee n S LA and depth of water is illustrate d in Fig. 3 for pairs of species , on single samplin g dates in two lochs , as a serie s of regressio n lines for each of which the correlatio n coefficien t betwee n S LA and depth is significan t at the 5% level or less. The regressio n lines of Potamogeton χ zizii Roth, and P. perfoliatus L . in Loch Bailie na Ghobhain n show that the slope of S LA with depth is typical of the loch and not of the species . There is a seasona l increas e of S LA of P. obtusifolius over the water depth 210-270 cm in the brown-wate r Loch of Lowes (Fig. 4) but no such increas e in S LA of Potamogeton praelongus in the much less brownwater Loch Lanlish (Fig. 5). Such attenuatio n data as there are indicat e
338
D. H. N. SPENGE
a seasona l increas e of Ee, 400-750 nm, in Loch of Lowes over this period but little chang e in Loch Lanlish (by Loch Croispol , Table 1), which suggest s that variatio n in shadin g rathe r than in other environmenta l or ontogeneti c factors cause s seasona l drift in S L A. The S LA field range for P. obtusifolius (Fig. 4), is 1.43 to 1.98, compare d with a laborator y range of 1.60 to 2.05. For P. perfoliatus. T A B L E 1. Lochs in which specific leaf areas have been measured, with m a p references and, where appropriate, attenuation coefficients (Ee), 400-750 nm, or EB, EG, ER.
1
M a p ref.
E.
Bailie na Ghobhainn, Lismore Croispol, Durness
N M 860425 N C 390680
0.50 0.56 0.55 0.57
Lanlish, Durness Lowes, Dunkeld
N C 388680 N O 050440
U a n a g a n , Fort Augustus
N H 370070
— 0.76 1.20 1.30 1.50
Loch
Ε In units
EB E G
2
ER
0.29 0.18 0.43
0.77 0.360.56
0.97 0.60 0.59 0.62 0.37 0.43
1 Measured
Date
24.6.69 19.6.70 4.8.70 16.9.70 August 1974 30.4.70 14.5.70 18.8.70 15.7.70 2
with spectroradiometer over 1 m (Spence et aL, 1971) or, , with blue(OB), green(OG) or r e d ( O R ) Chance filters, J u n e - A u g u s t (Spence 1975).
2
Specific leaf area ( c m mg ') 0-6
0-8, , 0 - 4
0·6
0-8
ΙΌ
1-2
1-4
80 £ - 160 \_ ω i 240 ο i 320 Q
400 480
.
v~
.
F I G . 3. Linear regressions of specific leaf area upon depth of water, of which the correlation coefficients are significant at the 5% level or less. Least and greatest error mean square are indicated. Loch Bailie na Ghobhainn: Potamogeton crispus (\/),P. perfoliatus ( • ) 24 June 1969. Loch Uanagan: P. χ zizii (A), P. perfoliatus ( Π • )» 12 August 1969; P. perfoliatus (• • ) , 14 July 1970. (Redrawn from Spence et al, 1973.)
LIGHT, ZONATION AND BIOMASS OF MACROPHYTES
A
M
J
J
A
339
S
Month F I G . 4. Seasonal variation in mean SLA (with standard errors) of Potamogeton obtusifolius over the water depth 210-270 cm in Loch of Lowes, 1970, a brown-water loch. (Redrawn from Spence et al, 1973.)
F I G . 5. Linear regressions of specific leaf area upon depth of water, of which correlation coefficients are significant at the 5% level or less, for Potamogeton praelongus in Loch Lanlish on various sampling dates in 1970. (Redrawn from Spence 1972.)
340
D. H. N. SPENCE
field values extend from 0.55 to 1.75 and, in the glasshouse , from 0.80 to 2.20. Thus the range in S LA of each specie s overlap s with the other and is matche d in laborator y and field. Since any two such specie s have differen t capacitie s for shoo t extension , they may have mutuall y exclusive rooting range s in a particula r site like P. χ zizii and P. perfoliatus in Loch Uanaga n (Fig. 3) or both their rooting range s and their specifi c leaf areas may overlap , as with P. crispus L . and P. perfoliatus in Loch Bailie na Ghobhain n or P. obtusifolius and P. perfoliatus in Loch of Lowes, when substratu m rathe r than irradianc e must determin e their zonation . We still canno t directly test the hypothesi s that, subjec t to modificatio n on many shore s by factor s like turbulenc e or substratu m or competitio n which are not strictl y depth-controlled , light determine s the potentia l depth range of a specie s (Spence , 1967), since we lack field measurement s of any two specie s that do not have overlappin g specifi c leaf areas in the laboratory . P. polygonifolius for instanc e was absen t from all our sites . Moreover , presentl y availabl e evidenc e concerns specie s from the same genus . However , using indirec t evidenc e it would seem certain that if the specifi c leaf areas at least of two related specie s do not overlap then neithe r can their rooting range s which, given the known relationshi p betwee n S LA and function , would then be a direct caus e of zonation . 3. Depth Limits of Colonization The photic zone in freshwate r is very much shallowe r than in the sea and it is seldo m necessar y in the United Kingdom to dive below 10 m to study attache d plants which rarely penetrat e anywher e nearly as deep as this. A brief outline follows of limits of colonization , and of biomass , in relation to depth of water. The limeston e Loch Bailie na Ghobhain n on Lismore was visited becaus e West (1910) reporte d "dens e beds " of the aquati c moss Fontinalis antipyretica L . at 13.1 m depth , suggestin g that this loch was colonize d to amongs t the greates t depth s of any in Scotland . Diving reveale d howeve r that while plants occurre d to a depth of 13.1 m thes e were only fragment s below 6 m, excep t at the very narrow ends of the loch. In J u ne 1969, the loch was thermall y stratifie d with a clear epilimnio n down to 6 m and, below, both thermo cline and hypolimnio n containe d large quantitie s of suspende d matter which produce d opaqu e layers with considerabl e attenuatio n but there was no stratificatio n in Augus t 1974. As determine d by diver surve y the shore again exceptin g its narrow ends has a gradien t of 1 in 4 to a depth of 5 m ; there, 1 m above the lower limit of continuou s vegetation , it suddenl y steepen s to 1 in 1.05. Either the instabilit y of this marl slope , or the existenc e at 6 m of the intermittent , opaqu e thermocline , cause s
LIGHT, ZONATION AND BIOMASS OF MACROPHYTES
341
an apparentl y prematur e limit to downwar d penetratio n of macrophyte s in most of this loch. Data are also availabl e for two more limeston e lakes, Lochs Borralie and Croispo l at Durnes s in Sutherlan d which are unstratifie d and of the same water colour , clarity and homogeneit y (Spence , unpublishe d data), resemblin g the epilimnio n in Loch Bailie na Ghobhain n and the clear coasta l waters of the Moray Firth describe d by Hemming s (1966). Vascula r plants do not grow in either loch below 6 m depth of
Plant cover: per cent
F I G . 6. Temperature profiles for Loch Spiggie, Shetland, (July), Loch of Lowes (August) and Loch Bailie na Ghobhainn (June), together with available data on depth of colonization, 2 percent plant cover, and oven dry weight of crop in g/m ( # — · ) (all data obtained by diving).
water; as in Loch Bailie na Ghobhain n this is also the downwar d limit for all attache d macrophyte s in Loch Croispol , wherea s in Loch Borralie specie s of Charophyta , mainly Nitella opaca, which is absen t from Loch Croispol , have been found by diving to form beds of vegetatio n down to 1 1m depth of water. Our experimenta l evidenc e is insufficien t as yet to explain the difference s in depth s of colonisatio n in these three limestone lochs or the fact that the angiosperm s {Potamogeton species ) ceas e to grow at the same depth in each. Furthe r example s are given in Fig. 6 of the commone r situatio n where there is no therma l stratificatio n even in relativel y calm weathe r or, if it is present , where the epilimnio n extend s well below the lower
342
D. H. N. SPENGE
limits of attache d vegetation . On anothe r count this may be the commoner situatio n at least in the United Kingdom , becaus e Loch Spiggie and Lowes represen t the brown coloure d water of low alkalinity 1 ( < 0 .3 m eq à H G 0 3 + C 0 3= + O H ") on the greates t length of shorelin e in Scottis h freshwate r lochs (Spence , 1964) and indicate , therefore , the sort of depth s to which attache d plants usuall y penetrate . I t is not of cours e as simple as that since there are also nutrient-poo r waters of great clarity like Ennerdal e in the English Lake District where vegetatio n is reported , by using a grab, at 10 m (Pearsall , 1921) or Lake Grane Langso in Denmar k (Nygaard , 1958) where vegetatio n was found by diving at 11 m (Fig. 7). Biomass: dry weight
F I G . 7. Depth profiles of biomass in Lake Grane Langso (Denmark), Loch Uanagan, (Inverness-shire) (August), Loch Croispol (Sutherland) (June) and Lake Weber (Wisconsin). (Data for first three obtained by diving; data for Lake Weber obtained with a grab and expressed as percent weight per 1 metre depth interval; lower graph for Loch Uanagan also on this basis for comparison.) Lake Grane Langso data adapted from Nygaard (1958), Lake Weber data from Potzger and Van Engel (1942).
4. Biomass Maxima and Depth Distribution I t may be noted in Fig. 7 that biomas s tends to reach a maximu m in about 1.0 to 1.5 m depth of water while in the clear limeston e Loch Borralie this maximum is reache d betwee n 3 and 4 m. Biomas s in Loch Uanagan along with the intrinsi c statur e of the specie s (Fig. 1) decrease s steadil y with depth; biomas s decreas e is in fact logarithmi c (Fig. 8) suggestin g that, for the given level of nutrient s in this moderate ly alkaline loch, biomas s is limited by irradiance , which is also reduced or attenuate d logarithmicall y with depth in this opticall y homogeneou s medium (Spenc e et aL, 1971). Data are insufficien t so far
L I G H T , Z O N A T I O N A N D BIOMASS OF M A C R O P H Y T E S
343
to confirm or refute the existenc e of such a biomas s trend from maximal values as the depth increase s in Loch Borralie or, indeed , in general . The water depth at which maximal biomas s occur s is worth a comment. In Loch Uanaga n this lies at and below the base of the littoral shelf (Fig. 1, arrow) while in Loch Borralie it coincide s with the slope of a less obvious , thoug h still discernible , littoral shelf in deepe r water. I t seem s likely that aspec t expresse d as excessiv e turbulenc e may directly , IOOO ι
—
1
500L-
Oepth of water ( c m ) F I G . 8. Semi-logarithmic plot of biomass weight in relation to water depth in Loch Uanagan. (Data as in Fig. 1.)
or indirectl y throug h soil particle size and substratu m chemistry , affect summe r growth of winter surviva l of macrophyte s and thus caus e limitation s in shallo w water. Unpublishe d data indicat e that the seasona l maximal biomas s is reach in August . Such maxima, (Fig. 7) are only exceede d by values of 2 Forsber g (1960) of 400 g over-dr y weight per m for nutrient-ric h Lake Osby in Swede n and approximatel y the same value for Loch Borralie . Even in water with the least attenuation , like that of Lochs Borralie and Croispol , biomas s is low relative to that in opticall y comparable , clear
344
D. H. N. SPENGE
coasta l seawate r (Fig. 9). This to an unknow n extent reflect s difference s in growth-form s and, therefore , in winter biomas s which, for some Potamogeton specie s that survive as overwinterin g buds , is as little as 1 /20th the summe r biomass . In situ productio n figures sugges t a more meaningfu l compariso n and are given in anothe r paper (Campbel l and Spence ) in this volume . I conclud e with an attemp t to summariz e thes e inter-relationships, , particularl y with regard to the role of light. The most bulky submerge d macrophyte s like Potamogeton praelongus produc e shoot s up to 3.5 m tall in the United Kingdom so that in standin g as oppose d to runnin g
40
F I G . 9. Comparison of submerged macrophyte biomass in Loch Uanagan and a marine site off Cornwall {Laminaria hyperborea forest) (Loch Uanagan data as for Fig. 1. Laminaria data from Bellamy and Whittick, 1968.)
water the zone of maximu m submerge d biomas s shoul d occur in not less than 3.5 m depth of water. In shallowe r standin g water, the submerge d biomas s is inevitabl y the produc t of smalle r plants . Excessiv e turbulenc e will directly or indirectl y limit this furthe r while the downward extensio n of crop maxima and indeed the depth s that any plant can grow depend s primarily on the degre e of light attenuation . This leads to the propositio n that the resultan t of the opposin g factor s of increasingl y excessiv e turbulenc e and high light attenuatio n determine s the rooting depth at which maxima l submerge d biomas s occur s on any shore . The chemistr y of the substratu m and the extent of grazing , and of periphyto n and sedimentar y cover on leaves , will thereafte r set the limits of the actua l submerge d maxima on a particula r shore .
L I G H T , Z O N A T I O N A N D BIOMASS O F M A C R O P H Y T E S
345
Acknowledgements T h e work on which this paper is based is supported by grants from the NaturalEnvironment Research Council. Thanks are due to Dr. Patrick Denny for his help in collecting the data presented in Fig. 1.
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Light as an Ecological Factor (Eds. R . Bainbridge, G. G. Evans and O. Rackham), 359-374. Blackwell Scientific Publications, Oxford. Nygaard, G . (1958). O n the productivity of the bottom vegetation in L a k e Grane
Langso. Verh. int. Verein. iheor. angew. Limnol 13, 144.
Pearsall, W. H . (1921). T h e development of vegetation in the English Lakes, considered in relation to the general evolution of glacial lakes a n d rock-basins.
Proc. Roy. Soc. B, 92, 259-284.
Potzger, J . E . and Engel, W. A. V a n (1942). Study of the rooted aquatic vegetation
of Weber Lake, Vilas County, Wisconsin. Trans. Wis. Acad. Sci. Arts Lett. 34, 149.
Spence, D . H . N . (1964). T h e macrophytic vegetation of freshwater lochs, swamps and associated fens. The Vegetation of Scotland (Ed. J . H . Burnett), 306-425. Oliver and Boyd, Edinburgh. Spence, D . H . N . (1967). Factors controlling the distribution of freshwater macrophytes with particular reference to the lochs of Scotland. J. Ecol. 55, 147-170. Spence, D . H . N . (1972). Light on freshwater macrophytes. Trans. Bot. Soc. Edinb. 42, 491-505. Spence, D . H . N. (1975). Light and plant response in fresh water. Light as an Ecological Factor II. (Eds. R . Bainbridge, G . C . Evans and O . R a c k h a m ) . Blackwell Scientific Publications, Oxford. Spence, D . H , N . and J e a n Chrystal (1970a). Photosynthesis a n d zonation of freshwater macrophytes I. Depth distribution a n d shade tolerance. New Phytol. 69, 205-216. Spence, D . H . N . and J e a n Chrystal (1970b). Photosynthesis and zonation of freshwater macrophytes. I I . Adaptability of species of deep a n d shallow water. New
Phytol. 69,217-227.
Spence, D . H . N., J e a n Chrystal and Campbell, R . M . (1973). Specific leaf area a n d zonation of freshwater macrophytes. J. Ecol. 61, 317-328. Spence, D . H . N., Campbell, R . M . and J e a n Campbell (1971). Spectral intensity in some Scottish freshwater lochs. Freshw. Biol. 1, 321-327. West, Geo. (1910). A further contribution to the comparative study of the dominant phanerogamic a n d higher cryptogamic flora of aquatic habit in Scottish lakes.
Proc. Roy. Soc. Edinb. 25, 967-1023.