Phycologia ( 1987) Volume 26 ( 1), 88-99

Seasonal growth and photoinhibition in

Plocamium cartilagineum (Rhodophyta)

off the Isle of Man

JO ANNA M. KAIN (JoNES)

Department of Marine Biology, University of Liverpool, Port Erin, Isle of Man, UK

J.M. KAIN (JONES). 1987. Seasonal growth and photoinhibition in Plocamium cartilagineum (Rho­dophyta) off the Isle of Man. Phycologia 26: 88-99 .

Length frequency determinations in subtidal populations of Plocamium cartilagineum provided information on growth of upright thalli in relation to season and depth. At 2 m below lowest astronomical tide (LA T), under the laminarian canopy, growth started in March and was exponential until June, with a relative growth rate in weight of 0 .026 per day. Under wave exposed conditions few mature uprights survived into the following winter. In deeper water, under the laminarian canopy, growth was slower and deeper still (13-17 m) mature uprights survived throughout the year. Clearance of the phaeophycean canopy allowed faster growth over an 8 m depth range but in early summer appeared to reduce the growth at I m below LAT. Uprights held on blocks at 0.5 m below LAT and in tanks exposed to reduced mid-summer daylight grew more slowly than uprights receiving less irradiance. It seemed that 0.5 mmol m-2 S-l was inhibitory. These data agree with the concept of the species as 'shade loving', with a maximum relative growth rate which is slow compared with currently cultivated red algae but probably fairly typical of subtidal undergrowth species. At most depths, however, it is light limited for much of the year.

INTRODUCTION

In temperate waters the conditions that result

from seasonal changes vary considerably in their

favourableness for the growth of subtidal algae.

Some perennial species have become highly

adapted to the seasons so that they effectively

'anticipate' the favourable periods (e.g. Kain

1984). Annual and ephemeral species seem to

respond to these periods as the opportunity aris­

es. Between these strategies is that of perennial

species which appear to respond to, but not 'an­

ticipate', favourable growth conditions. Such a

species is Plocamium cartilagineum (Linnaeus)

Dixon.

Plocamium plants of various species perennate

in patches with creeping stolons (Shepherd 1981).

The upright portions that grow from these, while

clearly not separate plants, can be distinguished

as separate entities. The aim of this study was

to follow the growth of uprights of P. cartilagi­

neum in relation to season, depth and the pres­

ence of the phaeophycean canopy.

88

METHODS

Two sites were studied: the exposed (western)

side of Port Erin (Isle of Man, British Isles) break­

water (54°5. 1'N; 4°46.2'W) at about 2 m below

lowest astronomical tide (LA T) and the steep

boulder bed below Spanish Head (54°3.3'N;

4°46.6'W) offering rock at a depth range down

to 17 m below LAT.

Plants were removed from the rock as gently

as possible, in order to avoid damage to the up­

right portions. The best instrument for this is a

thumb-nail but wear is excessive. An artificial

nail was therefore cut from flexible PVC plate

and held on the thumb with a neoprene cap. On

each occasion plants were scraped systematically

from nine separate patches, transported in sep­

arate net bags and stored in aerated seawater at

lO°C. In the laboratory, all the plants were ex­

amined under a microscope. Provided that an

upright portion had an intact tip on what ap­

peared to be the major axis and was attached to

a creeping portion or bore attachment discs at

Kain: Growth and photoinhibition in Plocamium 89

the base, it was cut just above the attachment

and the length measured. Thalli showing the

morphology of creeping portions, even without

attachment discs, and those of less than I cm

(when the morphology was indistinct) were ig­

nored. Every eligible upright was measured in a

randomly chosen portion of each sample. Mea­surements were discontinued in August because

many of the larger uprights were damaged.

At Spanish Head canopy clearances were per­

formed by cutting each canopy plant at the base

of the stipe. At I m below LAT the species re­

moved were Alaria esculenta (Linnaeus) Gre­

ville, Laminaria digitata (Hudson) Lamouroux

and L. hyperborea (Gunnerus) Foslie, at 5 m L.

hyperborea only and at 9 m L. hyperborea, Hal­

idrys siliquosa (Linnaeus) Lyngbye and Desma­

restia aculeata (Linnaeus) Lamouroux. The

cleared areas included several boulders or rocky

knolls at each depth; the control areas being sim­

ilar undisturbed rocks on either side. Patches were

sampled at random within each area. In order to

avoid bias in selecting intact uprights for mea­

surement, the samples of Plocamium from cleared

and control areas were processed in ignorance of

their origin.

In experiments on the exposure of Plocamium

to high irradiances, the length of each upright

was measured and a small piece of soft plastic

foam wrapped around its base. This was gripped

by a plastic tubing clip through the opening of

which a 5 mm hole had been drilled while it was

closed. The base of the clip embraced the barrel

of a 1 cm3 syringe which bore a numbered tag

and four of these clips as radial arms (Fig. 1).

When exposed in the sea the syringe barrel was

slipped onto a syringe plunger projecting through

an acetate sheet fixed to a concrete block. An

angle iron framework held a canopy of an acrylic

sheet with or without neutral filters over the

plants, with free access to water movement from

the slides. When exposed in tanks on land the

clip assemblies were first held in the laboratory

for 2 days in seawater containing 2.7 mg 1-I of germanium dioxide to inhibit diatom growth and

then placed in polyethylene mesh trays within

425 I polyethylene tanks containing filtered cir­

culating seawater. These in tum were immersed

in a larger polyethylene tank through which sea­

water recently pumped from the sea ran to waste,

as a crude form of temperature control. The tanks

were exposed to daylight through acrylic sheets

and neutral filters.

Fig. 1. The clip assemblage used for holding uprights of Plocamium on concrete blocks or in tanks.

Attempts to measure the reduction in light

caused by the laminarian canopy failed because

of the highly variable readings obtained.

Significance tests between samples of popu­

lations were performed by using the 2 x 2 G-test

of independence (Sokal & Rohlf 1981) on the

proportion of the uprights which were more than

a selected length.

RESULTS

The patchiness of Plocamium on rocky surfaces

precluded sampling from a given area, without

incurring impossibly long diving times. The

length frequencies thus had to be calculated on

a percentage basis, rather than as plant density

on the rock. The disadvantage of this is that if

there is continuous recruitment of uprights, the

percentage of those in the larger size classes, pro­

duced by growth, are diminished. The use of an

upper size limit, upper quartile, etc. for growth

determination was thus precluded. This difficulty

is well known to fisheries biologists so one of

their techniques was adopted.

The percentage frequencies in 5 mm length

classes on Port Erin breakwater in the Laminaria

hyperborea forest at 2 m below LAT at intervals

90 Phycologia, Vol. 26 ( I ), 1987

Length (em)

Fig. 2. Length frequency histograms of Plocamium up­rights at 2 m below LAT on Port Erin breakwater be­tween December 1 982 and August 1 983. Consecu­tively n was 1 89, 3 1 5,466,466,337,48 1 , 292,469, 426 and 360 C ... , identified mode; see text).

of a few weeks are shown in histogram form in

Fig. 2. In December 1982 there were few uprights

over 3.5 cm and it seems likely that these were

survivors from the previous summer. There was

little change by or during February, indicating

that little or no growth took place during mid­

winter under the laminarian canopy. In mid­

March, however, there was a departure from the

stepped reduction in frequency with length and

9 8 7

E 6

.c 5 '" c <U 4

-'

M A M

/e

A

Fig. 3. Mean modal triplet length plotted against time in 1 983.

the first appearance of a mode which probably

represented the group of young uprights making

the initial response to increased irradiance. This

was more apparent in April. (The May sample

may be anomalous: plants from three of the nine

sampled areas had to be discarded because ex­

tended storage under aeration seemed to lead to

breaking.) It is likely that the lowest length class,

which was well represented up until June, in­

cluded new recruits as well as non-growing up­

rights, because most appeared young and healthy,

though in June a few appeared to be degenerat­

ing. After June the lower length classes declined,

indicating a reduction in recruitment.

The mode which appeared in March can be

followed through to August (except in May) and

is marked with triangles in Fig. 2. Using the

'modal triplet' method of Menz & Bowers (1980),

the mean length of the uprights in the three length

classes spanning the mode on each occasion was

calculated and plotted against time on a semi­

logarithmic presentation in Fig. 3. The anoma­

lous May sample was omitted. It seemed that

growth was exponential until July and the cor­

relation coefficient from the points from March

to July was 0.9997. The regression coefficient,

which is mathematically equivalent to the rela­

tive growth rate in length (per day), was 0.0085.

An estimate of the relative growth in biomass

can be obtained from the double logarithmic plot

of fresh weight against length of Plocamium up­

rights shown in Fig. 4. Here the slope of the GM

regression line (Ricker 1973) fitted to the data

covering the length range 3-7 cm was 3.11. The

relative growth rate in fresh weight can thus be

calculated as 0.026 per day, a doubling in 26

days. The GM regression fitted to all the data

had a steep slope of 3.86, indicating a change in

shape reflecting, presumably, the high degree of

branching in larger individuals. The linear growth

Kain: Growth and photoinhibition in Plocamium 9 1

•

I, ·"1 • •

• ... / •

. ": . , .. •• •

•

0.5 : ./ • •

en

:;:: en OJ 3 •

L '" �

u..

0.1

0.05

10

Length (em)

Fig. 4. Fresh weight of Plocamium uprights plotted against their length. Continuous line: GM regression for 3-7 cm (v = 3.1 1 ); dashed line, GM regression for all the data (v = 3.86).

rate between June and July samples was 0.55 mm

per day.

At Spanish Head populations of Plocamium

were sampled at 4 m depth intervals early in the

year. This site is washed by strong tidal streams

as well as being exposed to wave action. The size

frequency histograms are shown in Fig. 5. In Jan­

uary/February 1984 at 1 m there was less pre­

dominance of the shortest uprights than on Port

Erin breakwater at 2 m in 1983. A comparison

with the plants at 5 m seems to indicate that

some winter growth had taken place. It is pos­

sible that the laminarian canopy at 1 m at this

site is thinner than on the breakwater. At 9 m,

there was a predominance of uprights of less than

3 cm, as at 5 m, but there were also a few very

long uprights. The two deepest populations,

however, showed a very different picture. At both

13 and 17 m there were uprights in all length

classes up to 13.5 cm.

A convenient measure of the upper spread of

20

10

% 10

5 10 Length (em)

1m

9m

13m

15

Fig. 5. Length frequency histograms of Plocamium up­rights at various depths below LA T at Spanish Head around February. Dates of collection ( n in brackets): 1 m, 27 Jan. 1 984 (326); 5 m, 10 Feb. 1 984 (298);9 m, 27 Jan. and 1 0 Feb. 1984 (248); 13 m, 10 Feb. 1 984 (423); 1 7 m, 7 Mar. 1 983 and 27 Jan. 1 984 (410).

size frequency plots is the upper quartile. This

was determined for samples (including those

shown in Fig. 5) taken in early 1983 and 1984

at Spanish Head and is shown in Fig. 6. The

difference between the 1-9 m and the 13- 17 m

populations is again obvious. The drop from 1

to 5 m was presumably a result of growth in

shallow water but there was no further drop be­

tween 5 and 9 m in either year, even if fertile (remaining from the previous year) plants were

eliminated from the calculation.

If the Laminaria canopy were limiting the light

supply to the undergrowth, the reduction of light

by the water column could be counteracted by

the reduction in canopy in deeper water (Kain

1971). In order to investigate this, areas were

cleared of canopy plants of Phaeophyceae at the

end of February 1984. These and control areas

were then sampled in April and June. The upper

quartiles are shown in Fig. 7 and significant dif­

ferences in Table 1. Between February and April

there was a significant length increase in the vir­

gin forest (control areas) only at I m. At 5 m

there was a significant increase in the cleared area

and both here and at I m the length was signif­

icantly greater in cleared than in control in April.

At 9 m, however, there was no significant change

in length in either area between February and

92 Phycologia, Vol. 26 (I), 1987

E u

:E '" c � � t '" => cr � '" c. c. :::>

4

• • .. :::::-- . ----- ... .--...

/ /

/

10 15 Depth (m)

• /

Fig. 6. The upper quartile lengths of uprights of Plo­carniurn at five depths below LAT at Spanish Head. .,7 Mar. 1 983; ... , 27 Jan. and 1 0 Feb. 1 984.

April. Between April and June, there was clear

growth in all areas and at each depth the plants

on the cleared areas were significantly different

from the controls, though at 1 m they were small­

er instead of larger. The longest plants in June

were under the laminarian canopy at 1 m. The

only time when plants in cleared or control areas differed between 5 and 9 m was in cleared areas

sampled in April, when there were significantly

more larger uprights at 5 than at 9 m.

At 1 m depth at Spanish Head the greater length

of uprights under the canopy, compared with

those on the cleared area in June, could have

been due to a number of factors. One possibility

E

� '" c. c.

:::>

3 4 5 6 7 8 9 Depth (m)

Fig. 7. The upper quartile lengths of uprights of Plo­carniurn at three depths below LA T at Spanish Head in 1 984. A, 27 Jan. and 10 Feb.;. 0, 10 and 26 April; .0, 1 9 June. Filled symbols, virgin forest; open sym­bols, phaeophycean canopy cleared in February.

Table 1. The significance (2 x 2 G-test of indepen­dence) of differences between the proportions of Plo­carnium uprights over selected lengths in control and phaeophycean canopy cleared areas at different depths below LA T at Spanish Head in different months of 1 984. NS = not significant

More longer uprights: P�

In April than February: Control Cleared

1 m 0.00 1 0.001 5 m NS 0.05 9 m NS NS

In cleared than control: April June

1 m 0.025 (0.005 INVERSE)

5 m 0.025 0.005 9 m NS 0.025

At I m than 5 m:

Control 0.00 1 0.001 Cleared 0.00 1 NS

At I m than 9 m:

Control 0.001 0.00 1 Cleared 0.001 0.005

At 5 m than 9 m:

Control NS NS Cleared 0.00 1 NS

was that high light levels inhibited plants unpro­

tected by the canopy. In order to test this, mea­

sured uprights were exposed to daylight during

the same season the following year, 1985. They

were held on concrete blocks at 0.5 m below LAT

in sheltered water inside Port Erin breakwater

and covered with different densities of neutral

filters, or transparent acrylic sheet. The results

(Experiment I) are shown in Table 2. During the

6 weeks exposure all the plants in full daylight

were lost, while increasing numbers survived with

decreasing light. The mean relative growth rate

in length in 40% daylight, of 0.0086, was for­

tuitously similar to that estimated from the Port

Erin breakwater population. It might appear from

Table 2 that there was clear cut evidence for light

inhibition on this experiment. However, in this

shallow sheltered site the new substrata provided

by the block assemblages were highly favourable

to filamentous diatoms and these covered all the

well lit surfaces including Plocamium uprights.

Beneath the 40% filter there were few diatoms.

These epiphytes could have caused or contrib­

uted to the demise of the uprights exposed to the

higher irradiances. Two further experiments were

performed therefore. In these, uprights were held

in two tanks on land and exposed to two levels

Kain: Growth and photoinhibition in Plocamium 93

Table 2. The effect of various reductions of natural daylight on uprights of P/ocamium held in clips (Fig. I ) on concrete blocks in the sea (Experiment I) or in tanks on land (Experiments 2 and 3). In the calculation of relative growth rate in length (R L) plants which did not grow were included but not those which were lost or damaged

Experiment 3 Experiment I Experiment 2 1 2 July-

3 May-I 4 June 1 985 2-1 5 July 1 985 8 August 1 985 0.5 m below LAT Tanks Tanks

% of incident light 94 75 60 38 48 20 27 1 2 Estimated maximum irradiance 0.80 0.64 0. 5 1 0.32 0.9 1 0.38 0.50 0.22

(mmol m-2 s-')

Number of plants

Lost 40 38 22 6 1 4 1 6 3 5 Damaged 0 I 8 3 1 7 9 I I No growth 0 0 I 0 1 6 9 I 0 Growth 0 I 9 3 1 3 1 6 23 33

Relative growth rate

RL x 1 03 3.4 8.6 0.9 2.4 4.4 6.3 Significance of difference

P� 0.001 0.05 0.05

of daylight. The growth of diatoms was pre­

vented by pretreating with germanium dioxide

and filtration of the circulating seawater medi­

um. Full daylight was not used in either exper­

iment because the plants were only just under

the water surface. In the sea, even at 0.5 m below

LAT, there is always at least 2 m of water within

2 h of mid-day off the Isle of Man. The results

(Experiments 2 and 3) are shown in Table 2. In

both experiments, growth was significantly faster

in the tank with lower irradiance. The hours of

sunlight were almost identical for the two pe­

riods, yet there was lower growth at 20% in Ex­

periment I than at 27% in Experiment 2. This

could have been due to inadequate temperature

control during the first period. It is not possible,

from these results, to designate a precise inhib­

itory irradiance because of variation in natural

daylight and the times for which the plants were

exposed to the estimated maximum irradiance.

This could have been shorter in Experiment I than 2 or 3 because of the tidal height. It is ap­

parent, however, that a maximum irradiance of 0.5 mmol m-2 s-' was inhibitory in both Ex­

periments 1 and 3.

DISCUSSION

There is considerable evidence for frequent lim­

itation of growth of Plocamium cartilagineum

by light. Uprights in the breakwater population

did not appear to grow during the darkest months.

At Spanish Head before April there was almost

no growth at 9 m below LA T and less at 5 than

I m. At all these depths clearance of the lami­

narian canopy enhanced growth at some time.

On the other hand there is strong evidence for

inhibition by summer daylight in shallow water.

Plocamium has been described as a shade lover

(Boudouresque 1969, 1970) merely from the evi­

dence of its habitat: this has now been confirmed

directly. It clearly can inhabit shallow water but

is found under a fairly dense canopy of lami­

narians (Kain 1960; Smith 1967; Luning 1970)

and it can extend into deep water of more than

20 m (Kain 196 1; Norton 1968; Norton et al

1969). Inhibition of photosynthesis by high ir­

radiance has been demonstrated in the Rhodo­

phyta many times (e.g. Mathieson & Dawes 1974;

Mathieson & Norall 1975a, 1975b; King & Schramm 1976; Ramus & Rosenberg 1980). On

the other hand, photosynthesis of Plocamium

te/fairiae Harvey was still maximal at 40 k lux

(approximately 0.7 mmol m-2 s-') (Yokohama

1973) whereas in the present study growth was

clearly suboptimal when P. cartilagineum was

exposed to 0.5 mmol m-2 s-'. Inhibition of ac­

tual growth of red algae seems to have been re­

corded only by Boney & Comer ( 1962, 1963) in

sporelings of three species, by Jones & Dent ( 1971)

in sporelings of five species and by Polne et al

( 198 1) in adult Eucheuma.

The seasonal growth pattern of Plocamium

cartilagineum can be contrasted against those of

the seasonally highly adapted canopy-former

94 Phycologia, Vol. 26 (I), 1987

Laminaria hyperborea (Kain 1976) and two of

its fellow undergrowth species Delesseria san­

guinea (Hudson) Lamouroux and Odonthalia

dentata (Linneaus) Lyngbye (Kain 1984). In the

latter, growth starts in mid-winter, in spite of

low irradiances, when nutrient levels are high.

The reason that the growth of Plocamium is de­

layed until March is presumably because it lacks

stored materials and is reliant on photosynthesis.

The same may apply to Chondrus crispus Stack­

house and Mastocarpus stellata (Stackhouse)

Guiry in the northwest Atlantic which show little

sign of growth before March (Mathieson & Burns

1975; Burns & Mathieson 1972). Tissue loss in

Plocamium is also different from plants such as

Delesseria. In the latter it occurs at a particular

time of year as part of a seasonal pattern (Kain

1984); in Plocamium the longer upright portions

may disappear in autumn if they are subjected

to wave action or they may be present all year

round in deeper water. A very different seasonal

strategy, with several cohorts arising each year,

is shown by Asparagopsis armata Harvey (Ar­

anda et al 1984).

In species growing mainly at the apex one might

expect a linear rather than a logarithmic pattern.

The former has sometimes been observed in red

algae (Jones & Dent 1971; Bird et aI 1977; Simp­

son & Shacklock 1979; Mumford 1979; Guiry

1984). On other occasions, clear logarithmic

growth has been maintained for days (Edwards

1977) or weeks (Waaland 1979; Polne et aI 1981).

As individual plants become larger and the pro­

portion of growing tissue smaller it is surprising

to observe continued logarithmic growth as in

Plocamium on Port Erin breakwater. As the

species was probably light limited, the relative

reduction in growing tissue could have been

counteracted by increasing light until July (Kain

et al 1976). A further consideration may be per­

tinent to explaining logarithmic growth. If light

were limiting then the rate of photosynthesis

rather than an upper limit to the rate of cell di­

vision or expansion would have been limiting.

An increase in the number of photosynthetic cells

could then be the equivalent of an increase in

the number of growing cells, implicit in the con­

cept of logarithmic growth. This, however, pre­

supposes translocation of photosynthate, not yet

demonstrated for Plocamium or its near rela­

tives . . In experiments on cultivation of red algae most

workers assume that growth is logarithmic be­cause they quote the growth rate in per cent per

day (Yoneshigue-Braga & Baeta Neves 1981), as

doublings per day (Lapointe et al 1984; Fried­

lander & Dawes 1984), as log2 weight change per

day (Bird et al 1979) or, in the sense of Evans

( 1972), as the relative growth rate (Morgan et al

1980; Morgan & Simpson 1981a, 1981b; Pat­

wary & van der Meer 1983, 1984). This is un­

derstandable when larger plants are cropped be­

cause the proportion of growing tissue may

remain substantially constant.

There seems to be some confusion between

the relative growth rate R (or specific growth rate

JL) and percentage increase per unit time. The

formula for the former is sometimes used for the

latter (x 100) (DeBoer & Ryther 1977; Braud & Perez 1979; Rosenberg & Ramus 198 1; Rueness

& Tananger 1984; Fujita & Goldman 1985). An

example can illustrate the real difference. If a

plant weighs 100 g at the start of a 24-h period

and 120 g at the end, one might say that it had

grown 20%. The compound interest formula for

one payment per unit time:

% increase = 100 [ (::ft I]

would give this result. The compound interest

formula for continuous interest is mathemati­

cally equivalent to 100 x the relative growth rate

formula:

In Wt - In Wo R = ----''----...::.

t

These would give values of 18.2% and 0. 182

day-I respectively. The discrepancy between the

results given by the two types of formula is great­

er with larger and less with smaller values. As

algae grow more or less continuously it is clearly

preferable to use the latter formula and, to avoid

confusion, call it the relative growth rate, R

(Evans 1972).

For obvious reasons the relative growth rates

of economic red algae under cultivation have

been frequently measured and some are shown

in Table 3. Gracilaria tikvahiae, Hypnea mus­

ciformis, Neoagardhiella baileyi and possibly

Devaleraea ramentosa are the fastest growing

species, each with a recorded R M of over 0. 15 per

day. Genera such as Iridaea, Eucheuma, Gelidi­

um, Gracilaria, Palmaria and Chondrus contain

fairly fast growing species. None of these, of course, are deep subtidal 'shade loving' genera

or they would not have been chosen for culti­

vation which requires 'sun plants' for high pro­

duction rates. Waaland ( 1977), however, cul-

Kain: Growth and photoinhibition in Plocamium 95

Table 3. The maximum relative growth rate in length (R L) or weight (R M) per day of species of F1orideophyceae in tank, raft or rope culture. R calculated from percent increases when necessary. Ranked (using maxima and assuming RM � 2 X RL)

Species

Graci/aria tikvahiae McLachlan Gracilaria tikvahiae Graci/aria tikvahiae (mutant) Gracilaria tikvahiae Graci/aria tikvahiae Gracilaria tikvahiae Graci/aria tikvahiae (polyploid) Graci/aria tikvahiae Graci/aria tikvahiae Gracilaria tikvahiae Graci/aria tikvahiae Gracilaria tikvahiae Graci/aria tikvahiae Graci/aria tikvahiae Devaleraea ramentacea (Linnaeus) Guiry Hypnea musciformis (Wulfen) Lamouroux Hypnea musciformis Neoagardhiella bai/eyi (Kiitzing) Wynne et Taylor Neoagardhiella baileyi Neoagardhiella baileyi Gelidium sp. Gracilaria sjoestedtii Kylin Iridaea cordata (Turner) Bory Iridaea cordata I. cornucopiae Postels et Ruprecht I. heterocarpa Postels et Ruprecht Eucheuma unciatum Setchell et Gardner Gelidium coulteri Harvey Gracilaria edulis (Gmelin) Silva Gracilaria verrucosa (Hudson) Papenfuss Gracilaria verrucosa Palmaria palmata (Linnaeus) O. Kuntze Palmaria palmata Palmaria palmata Palmaria palmata Farlowia mollis (Harvey et Bailey) Farlow et Setchell Gracilaria exasperata Harvey et Bailey Gracilaria exasperata Gracilaria exasperata Chondrus crispus Chondrus crispus Chondrus crispus Chondrus crispus Gracilaria sp.

Plocamium cartilagineum Eucheuma spinosum (Linnaeus) J. Agardh Eucheuma spinosum Hypnea cervicornis J. Agardh H. nidifica J. Agardh Callophyllis jlabullata Harvey Gracilaria arcuata Zandard Hypnea chordacea Kiitzing Furcellaria lumbricalis (Hudson) Lamouroux Furcellaria lumbricalis Pterocladia caerulans (Kiitzing) Santelices Schizymenia pacifica (Kylin) Kylin Pterocladia capillacea (Gmelin) Bornet et Thuret Prionitis lanceolata (Harvey) Harvey

RM

0.35 0.25 0.22 0.20 0. 1 9 0. 1 9 0. 1 6 0. 1 5 0. 1 5 0. 1 3 0. 1 2 0. 1 2 0.078 0.05

0.097 0. 1 9 0. 1 0 0. 1 8 0. 1 7 0.058

0.072 0.090 0.090 0.037 0.083 0.078 0.077 0.076 0.076

0.096 0.052 0.083 0.077 0.059 0.057 0.065 0.080 0.053 0.035 0.074 0.066 0.025 0.004 0.058

0.039 0.052 0.024 0.039 0.036 0.035 0.035 0.032 0.030

0.0 1 7 0.023 0.0 1 7 0.0 1 6 0.0 1 0

Authors

Parker 1 982 Lapointe et al 1 984 Patwary & van der Meer 1 983 Bird et al 1 979 Edelstein et al 1 976 Fujita & Goldman 1 985 Patwary & van der Meer 1 984 DeBoer & Ryther 1 977 Fralick et al 1 98 1 DeBoer 1 979 Edelstein 1 977 DeBoer et al 1 978 Bird et al 1 977 Rosenberg & Ramus 1 98 1 Rueness & Tananger 1 984 Humm & Kreuzer 1 975 Haines 1 97 5 DeBoer et al 1 978 DeBoer & Ryther 1 97 7 Waaland 1 977 Rueness & Tananger 1 984 Hansen 1 983 Waaland 1 977 Waaland 1 98 1 Waaland 1 977 Waaland 1977 Polne et al 1 98 1 Hansen 1 980 Nelson et al 1 980 Rueness & Tananger 1 984 Jones 1 959 Morgan et al 1 980 Morgan & Simpson 1 98 1 a Morgan & Simpson 1 98 1 b Waaland 1 977 Waaland 1 977 Waaland 1 977 Waaland 1 98 1 Waaland 1 979 Bird et al 1 979 Simpson & Shacklock 1979 Braud & Delelpine 1 98 1 Bidwell et al 1 985 Y oneshigue-Braga & Baeta

Neves 1 98 1 Waaland 1 97 7 Braud & Perez 1 979 Soegiarto et al 1 977 Mshigeni 1 978 Mshigeni 1 978 Waaland 1 97 7 Nelson et a l 1 980 Mshigeni 1 978 Bird et al 1 979 Rueness & Tananger 1 984 Santelices 1 976 Waaland 1 977 Santelices 1 976 Waaland 1 977

96 Phycologia, Vol. 26 (1), 1987

Table 4. The maximum elongation rate per day (mm) or relative growth rate in length (RL), area (RA) or weight (R M) per day of species of Florideophyceae in the field. Ranked (approximately)

Species mm

Iridaea cordata Graci/aria tikvahiae Eucheurna acanthonoturn (Harvey) J. Agardh Plocarniurn cartilagineurn 0.55 Gelidiurn robusturn (Gardner) Hollenburg et

Abbott 0.63 Gelidiurn robusturn 0.35 Pterocladia capillacea 0.44 Eucheurna acanthonoturn Chondrus crisp us Calliarthron tuberculosurn (Postels et Ru-

precht) Dawson 0.10

tured some deeper water algae, including

Plocamium cartilagineum. This, with a rate of

0.039, grew faster in tanks, presumably under

optimal conditions, than observed in the sea in

the present study.

Field measurements of red algal growth rates

(Table 4) are much scarcer and, as one would

expect, the rates are slower than those under op­

timum culture conditions. Apart from the fast

growing Iridaea and the slow growing coralline,

Calliarthron, they are remarkably similar to each

other.

Comparison of Plocamium growth rates with

other groups of macroalgae is difficult because

relative growth rates are rarely measured in whole

plants. Clearly its linear increase is slow: rhi­

zomes of Caulerpa paspaloides (Bory) Greville

elongate at 10 mm per day (O'Neal & Prince

1982), Laminaria hyperborea sporophytes at 10.5

mm per day (Kain 1976), L. longissima Miyabe

at 68 mm per day (Sasaki 1969), Pelagophycus

porra (Leman) Setchell at 70 mm per day (Coyer

& Zaugg-Haglund 1982). Macrocystis integrifolia Bory at 95 mm per day (Lobban 1978), M. py­

rifera (Linnaeus) C. Agardh at 140 mm per day

(Zimmerman & Kremer 1986) and Nereocystis

luetkeana (Mertens) Postels & Ruprecht also at

140 mm per day (Kain 1987).

Most of these, of course, are the faster growing,

large species in which linear growth 'would be

maximal. Smaller examples would be Fucus dis­

tichus (Linnaeus) ssp. edentatus (de la Pylaie)

Powell with a rate of 0.36 mm per day (Strom­

gren 1985) and F. spiralis Linnaeus with 0.42

mm per day (Schon beck & Norton 1979), both

slower than Plocamium in the summer.

When the spectacular linear growth rates of

the large algae are expressed in relative terms

RL RA RM Authors

0.088 Hansen 1977 0.075 Penniman et al 1986 0.04 Dawes et al1974

0.0085 0.026 This study Guzman del Proo & de la

Campa de Guzman 1979 Barilotti & Silverthorne 1972 Stromgren 1984

0.020 Dawes et al 1974 0.012 Taylor 1972

Johansen & Austin 1970

they seem quite slow, because of the small pro­

portion of growing tissue. R in length (one third

of R in weight if there is no change in shape) of

juvenile Nereocystis stipes was 0.024 (Nicholson

1970) and of juvenile Macrocystis plants 0.031

(Dean & Jacobsen 1984). Fronds on mature plants

of M. pyrifera showed the highest value of about

0.08 (North 1971). A relative growth rate in

weight for a M. pyrifera 15 m frond can be cal­

culated from a daily fresh weight production of

36 g per frond (Kain 1982) and a weight of 1.2

kg derived from the length/weight relationship

of 0.03 given by Jackson et al (1985): it is 0.03.

One has to go to an opportunistic species with

most of its cells capable of division for one of

the fastest relative growth rates: Viva lactuca

Linnaeus in laboratory culture had an R in the

area of 0.73 (Parker 1981).

The growth rates that have been quoted here

were all the maximum observed by each author,

to give an indication of the species' potential

under optimum conditions. Very young plants

were omitted. Clearly the relative growth rates

of embryos or sporelings can be considerably

faster. The variation in the observed relative

growth rates in plants of the same order of size

(Table 3) is likely to be due to different growth

potentials. The subtidal undergrowth 'shade lov­

ing' species are presumably adapted to low light,

with low saturation levels and low maximum

photosynthesis rates. The result of the latter would

be low relative growth rates. This is clearly not

a strategy adopted by the whole of the division

when the relative growth rate of Gracilaria plants

can substantially exceed that of Macrocystis

fronds. If Plocamium is typical of the 'shade lov­

ing' group the slow maximum growth rate is rare­

ly a disadvantage: for most of the year the pop-

Kain: Growth and photo inhibition in Plocamium 97

ulations observed in this study appeared to be

limited by light.

ACKNOWLEDGMENTS

Michael Bates continued to give invaluable as­

sistance underwater. I am also grateful to my

daughter, Bidda Jones, for help in the laboratory.

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Accepted 30 May 1986