Seasonal growth of Laminaria groenlandica as a function of plant age

Seasonal growth of Laminaria groenlandica as a function of plant age

Lours D. DRUEHL AND ERIC L. CABOT Department of Biological Sciences, Simon Fraser University, Burnaby, B.C., Canada V5A 1S6

AND

KATHERINE E. LLOYD Bamfield Marine Station, Barnfield, B.C., Canada VOR 1BO

Received December 1 1, 1986

DRUEHL, L. D., CABOT, E. L., and LLOYD, K. E. 1987. Seasonal growth of Laminaria groenlandica as a function of plant age. Can. J. Bot. 65: 1599-1604.

The seasonal growth of Laminaria groenlandica (Laminariales, Phaeophyta) on the west coast of Vancouver Island, B.C., Canada, was investigated as a function of plant age, using plants maintained at a constant depth on rope structures. First-year plants, which become macroscopically visible in March, had a delayed seasonal peak of maximum blade size relative to the older year classes (April-May) which initiated growth in January. This resulted from the 1st-year plants' lower susceptibility to distal blade erosion and prolonged net growth season. All year classes obtained their greatest wet weight at the same time (July -August). For 1st-year plants, this represented a balance between blade erosion and elongation; for older plants, storage product synthesis and blade thickening and elongation balanced against erosion appeared responsible for determining maximum biomass. The 2nd-year class dominated the other year classes in blade dimensions and few plants survived their 3rd year of growth. The instantaneous growth rates of L. groenlandica were most closely associated with temperature, followed by photon flux density, and changes in growth rates were associated with temperature and salinity.

DRUEHL, L. D., CABOT, E. L., et LLOYD, K. E. 1987. Seasonal growth of Laminaria groenlandica as a function of plant age. Can. J. Bot. 65 : 1599- 1604.

La croissance saisonnibre du Larninaria groenlandica (Laminariales, Phaeophyta) sur la c6te ouest de l'ile de Vancouver, C.-B., Canada, a CtC CtudiCe en fonction de l'bge de l'individu, utilisant des plants maintenus i une profondeur constante sur des charpentes de corde. La taille laminale maximale Ctait atteinte plus tard chez les plants de 1" annCe qui deviennent visibles a l'oeil nu en mars, que chez les groupes annuels supCrieurs (avril -mai) dont la croissance dCbute en janvier. Cela Ctait dii au fait que d'une part, les plants de l C annCe Ctaient moins influences par 1'Crosion distale de la lame et d'autre part, i une saison Ctendue de croissance nette. Tous les groupes ont atteint leur brut en mEme temps (juillet-aoQt). Pour les plants de premibre annCe, cela reprCsente un Cquilibre entre 1'Crosion laminale et l'allongement; pour les plants plus bgCs, la synthbse des produits de rCserve et 1'Cpaississement de la lame et l'allongement opposCs i 1'Crosion ont semblC &re responsables de la dktemination de la biomasse maximum. Le groupe de 2C annCe Ctait supCrieur aux autres groupes en ce qui conceme la taille de la lame, et seul quelques plants ont survCcu a leur 3e annCe de croissance. Les taux de croissance instantanCe du L. groenlandica Ctaient en association la plus Ctroite avec la tempkrature, suivi de la densit6 du flux photonique; les changements dans les taux de croissance Ctaient relies la tempCrature et la salinitC.

[Traduit par la revue]

Introduction Materials and methods

Studies on a variety of Laminaria s~ec ies have demonstrated a characteristic seasonal fluctuation in growth rates (e.g., Parke 1948; Kain 1963; Chapman and Craigie 1977; Liining 1979; Chapman and Lindley 1980; Anderson et al. 1981). Many of these studies have correlated the observed seasonality of growth with such environmental parameters as nutrients, irradiance, and temperature.

It has been shown for some Laminaria s~ec ies that the characteristic initiation of growth in the late winter is aug- mented by stored carbohydrate reserves, or persistent photosynthetic capacity camed over from the previous year (e.g., Chapman and Lindley 1980). In our study area, young sporo- phytes of Laminaria groenlandica Rosenvinge first become macroscopically evident in March. Thus, it would appear that these plants in their 1st year of growth are at a distinct dis- advantage when they initiate growth under low, late-winter irradiances, since they have neither stored reserves nor sub- stantial photosynthetic capacities.

We hypothesized that Laminaria in its 1st year of growth responds to its physical and chemical environment by utilizing a different strategy than subsequent year classes. In the present study we examined selected characteristics of different year classes of L. groenlandica in relation to their seasonally vary- ing physical and chemical environments.

Growth of plants of different year classes was monitored on long- line rope structures maintained in Roquefeuil Bay (48'51' N, 125'08' W), on the west coast of Vancouver Island, B.C., Canada. Holdfasts of the plants were attached to short preweighed lengths of rope, which were inserted into the rope structure. The plants were maintained at an average depth of 4 m below the sea surface.

Individuals of L. groenlandica from different year classes were col- lected onshore near the experimental site. From previous observations on cultivated plants of known age, we were able to distinguish the year class of each plant. Figure 1 depicts the first three year classes as observed in March.

In September 1979, 11 plants in their 1st year of growth and 13 plants in their 2nd year were attached to the rope structure. In April 1980, an additional 17 1st-year plants were attached to the rope to replace the earlier group of ~ s t - ~ e a r plants that had matured intotheir 2nd year.

At approximately monthly intervals from September 1979 until February 1981, wet weight, blade length, surface area, and elongation and erosion rates of the plants were assessed.

Surface area was determined from outlines of each plant traced onto paper, cut out, and weighed. The surface area was calculated using the known weight per area of the paper. Growth rate was assessed by noting the position of a hole punched 10 cm from the blade base the previous month (Parke 1948). Blade erosion rates were measured by calculating the change in distance from the hole punched for growth measurements and the distal end of the blade between measuring dates (Luning 1979).

Printed in Canada I Imprim6 au Canada

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FIG. 1. The first three year classes of Laminaria groenlandica as observed in March. (A) First year; (B) 2nd year; (C) 3rd year. Scale 15 cm.

Environmental monitoring Temperature, salinity, and dissolved nutrient concentrations (NO3,

PO,) were monitored weekly at the study site at 4 m depth, close to midday. Water samples for nutrient analyses were stored in the dark in a cooler during transport to the laboratory, where the water was immediately filtered through a glass-fibre filter. Nitrate samples were analyzed immediately, and part of each water sample was frozen for later analysis of phosphate. All analyses were performed on a Tech- nicon autoanalyzer, using methods described by Strickland and Parsons (1972).

Photon flux density data were provided by Fisheries and Oceans Canada for Carnation Creek, approximately 8 km from our study site.

Multiple regression analysis Multiple regression analysis of instantaneous growth rates and

changes in growth rates with selected environmental variables were completed. Instantaneous growth rates were transformed by Y = In ( (mmlday) + 1.0). The change in growth is defined as the difference in untransformed instantaneous growth rate in two successive growth- measurement periods. Since environmental variables were measured more frequently than growth rates, the means of environmental measurements taken in the period prior to and including a growth measurement were used for analyses. Partial R 2 values for the indi- vidual environmental variables were used to express the amount of variance for a given growth parameter that could be accounted for by

changes in that variable when the other variables were held statis- tically constant.

Results Phenology

For all year classes of Laminaria groenlandica studied, the most rapid growth occurred during the winter and spring, followed by slow growth during summer and fall (Fig. 2). This trend was least pronounced for the 3rd-year class.

Blade erosion rates were greatest during May-August for the three year classes (Fig. 2). For 1980, the length of a blade lost to erosion relative to the blade remaining in December was 1.9 for 1 st-year plants and 2.5 for 2nd-year plants. Most of the 3rd-year plants measured were dead by September.

Other distinct phenological events separated the year classes. First-year plants had delayed seasonal peaks of maximum blade length and surface area relative to the older plants (Figs. 3 and 4). The seasonal peak in wet weight occurred at approximately the same time for all year classes (Fig. 5).

Late in the growth season, 2nd-year plants dominated the other two year classes in all dimensions. As these plants entered their 3rd year of growth, there was a marked reduction

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DRUEHL ET AL

BLADE ELONGATION

BLADE EROSION

-1.0 I I I I I I I I 1 I I I I I I I I I

D J F M A M J J A S O N D J F M 1979 1980 1981

FIG. 2. Seasonal variation in blade elongation and erosion rate (& lSD) as a function of year class.

110 - 3600 --

3200 - YEAR

90 - CLASSES CLASSES

2800 -

2400 -

BLADE LENGTH 70- 3-

60 -

1200 - 2 50 -

0 800 -

10 - 1979 I 1980 I 1981

FIG. 4. Seasonal variation in blade surface area (A 1SD) as a func- ' S O N D J F M A M J J A S O N D J F M A M tion of year class.

FIG. 3. Seasonal variation in blade length (f 1SD) as a function of Linear regression analysis

year class. Multiple regressions revealed that the four environmental variables explained 79 and 54% of the variances of instan-

in all parameters. Similarly, as 1st-year plants entered their 2nd year of growth, they continued this trend by dominating in size characteristics. Most of the plants did not survive their 3rd year, and those that did enter the 4th year were clearly in poor condition.

Environmental monitoring Generally, nutrient concentrations at 4 m depth were high

from September to March and low from April to August (Fig. 6). Seawater temperatures at 4 m ranged from 8 (February) to 14°C (July), whereas salinities did not vary appreciably. Irradiance incident on the surface was low during November and December and high from May to August (Fig. 7).

taneous growth and the change in growth rate, respectively (Table 1). Since ambient levels of phosphate and nitrate were highly correlated, only one of these variables was included in multiple regression at any one time. Regressions with phosphate instead of nitrate (not shown) gave essentially the same results except that the fit was slightly better for instantaneous growth (R2 = 0.81) and worse for change in growth rate (R2 = 0.51).

Temperature and photon flux density were associated with both growth parameters, but temperature correlated most strongly. Salinity was weakly associated with instantaneous growth but more strongly associated with change in growth rates. Nitrate and phosphate had the weakest association with the two growth parameters. They were not significantly asso-

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1602 CAN. J. BOT. VOL. 65, 1987

I ' l l ! !

- YEAR

joo ,

1 -

" I a

I 100 -

FIG. 5. Seasonal variation in whole plant wet weight (+lSD) as a function of year class.

ciated (p > 0.05) with instantaneous growth rates and only weakly associated with change in growth rates.

Discussion When the three year classes of L. groenlandica were viewed

together, a seasonal pattern of rapid growth in the late winter and spring and reduced growth rates in the summer and fall were observed. This general pattern has been noted for L. groenlandica in Alaska, U.S.A. (Calvin and Ellis 1981), and for other Laminaria species elsewhere (e.g., Parke 1948; Hasegawa 1963; Luning 1979; Chapman and Lindley 1980), though certain phenological events distinguished the year classes. Most notably, blade dimensions of 1st-year plants continued to show a net increase 1-2 months longer than did those of older plants. This phenomenon has also been observed for European Laminaria species (Parke 1948; Perez 1969; Luning 1979). Luning (1979) speculated that the delayed peak in maximum blade dimensions of 1st-year plants may be an age-specific seasonal growth pattern. Our data suggest that the prolonged net growth season of 1st-year plants results from relatively high growth and low erosion rates. The growth rate of 1st-year plants exceeded erosion rates until August, whereas the growth rate of older plants only exceeded the erosion rate until May.

The prolonged retention of blade tissue by the 1st-year plants may enhance their photosynthetic and (or) nutrient uptake capacity. Davison and Stewart (1984) have demonstrated that most of the nitrate uptake in L. digitata occurs in the mature blade tissue rather than in the meristematic area. If nitrate is taken up preferentially by mature L. groenlandica blade tissue, the prolonged retention of tissue by 1st-year plants could allow these plants to exploit more efficiently the low summer ambient nitrate conditions. A continuation of this study has shown that 1st-year plants are better competitors for nitrate and ammonium and can take up the nitrogen substrates three times faster than those of 2nd- and 3rd-year plants (Harrison et al. 1986).

All three year classes attained their greatest wet weight at approximately the same time. This point represents a balance between synthetic (growth, storage product synthesis) and degradative (erosion) processes. First-year plants achieved this balance when blade growth and erosion rates were similar. Older plants had been subjected to high erosion rates for 1-2

N J M M J S N J M 1979 1980 1981

FIG. 6. Seasonal variation of nutrients, temperature, and salinity as observed at midday at 4 m depth. Values are means of four weekly observations.

FIG. 7. Seasonal variation in photon flux density (photosyn- thetically active radiation); values are monthly averages of weekly means + 1 SD; and day length as calculated for 48.5" N.

months prior to attaining their greatest wet weight. It would appear that increased storage product synthesis and perhaps blade thickening were important for older plants to obtain their maximum wet weights. Change in wet weight per unit blade area supports this suggestion (Table 2). A seasonal increase in weight per unit area has also been recorded for L. groenlandica in Alaska, U.S.A. (Calvin and Ellis 1981), and an increase with advancing year class for L. angustata in Japan (Kawashima 1972).

The growth strategy of L. groenlandica changed with age, and this was demonstrated by the lag in seasonal peaks for

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DRUEHL ET AL.

TABLE 1. Multiple (partial R2) linear regression analysis of environmental variables on the instantaneous growth rate and the change in growth rate of 2nd-year Larninaria

groenlandica

Change in Instantaneous growth rate instantaneous growth rate

Variable Partial RZ Pa Partial R2 Pa

Temperature 0.488 <0.001 0.318 <0.0001 Salinity 0.021 <0.001 0.239 <0.0001 Nitrate 0.001 NS 0.133 <0.001 Photon flux density 0.162 < 0.0001 0.145 <0.001

Overall R2 0.791 Unexplained X variance 0.209

"P is probability of B # 0. *NS = P > 0.05.

TABLE 2. Wet weight (mg cm2) per unit blade area for two dates and percent change in wet weight per unit area between these dates. Values calculated from

mean values in Figs. 4 and 5

Year class 1 June 1980 1 August 1980 %

blade dimensions of the 1st year class relative to the older plants. The greatest change occurred as individuals entered their second rapid growth season, since the 2nd- and 3rd-year plants demonstrated similar seasonal patterns.

The peak maturity in L. groenlandica, which was indicated by blade dimensions and biomass, was attained during the 2nd year of life; plants in their 3rd year showed a marked reduction in vigour, and our observations on this species indicated that only a small percentage of plants survived for 4 years. Duggins (1980) states that this species in Alaska has a longevity of 6 years or more, on the basis of growth rings observed in the stipe. We have observed no such rings in the Barkley Sound populations. Parke (1948) reported observations similar to ours on longevity for Laminaria saccharina on the British coast. Those plants achieved maximum wet weight and growth rates during the 2nd year and rarely exceeded 3 years in age.

On the basis of our multiple regressions, temperature, followed by photon flux density, and then salinity accounted for 79% of the variance in instantaneous growth rates. Changes in growth rates were most closely associated with temperature, followed by salinity, and then photon flux density; however, all variables accounted for only 54% of the variance. Neither nitrate nor phosphate was significantly associated with instantaneous growth rates and their association with change in growth rates was the least pronounced of all variables studied.

It is well documented that many Laminaria species, when subjected to high summer irradiances and low ambient nitrogen, will demonstrate decreased growth rates and an increase in carbohydrate storage (see GagnC et al. 1982, for a review of kelp response to seasonal nitrogen fluctuations). Elevated temperatures may contribute to the decreased growth rate also. Druehl (1967) has shown that for L. groenlandica the maximum photosynthesis/respiration ratio occurs at temperatures below 7°C and the maximum photosynthetic rate near 10°C.

The seasonal growth cycle of L. groenlandica does not

appear to be regulated by nutrient availability. This suggests that either our data resolution is inadeauate or that some other extrinsic variable, such as day length (see Fig. 7) or a circannual rhythm, is directing the assimilated carbon to either growth or storage. GagnC et al. (1982) suggested that a genetically fixed carbon allocation pattern would be optimal for Laminaria species inhabiting areas that are persistently nutrient rich. They felt such a mechanism would be required to ensure the accumulation of stored carbon, which is important to the survival of the plant during the light-limiting winter period. The possibility of a circannual growth rhythm has also been suggested for Alaria esculenta (Buggeln 1978), Lami- naria saccharina, and L. hyperborea (Liining 1979).

Acknowledgements

We thank S. Pakula, R. Bod, and A. Lindwall for field and laboratory assistance, and Dr. P. J. Hanison, S. Fain, and S. Villeneuve for commenting on the manuscript. Research facili- ties were kindly provided by the Bamfield Marine Station and this study was funded by the Natural Sciences and Engineering Research Council of Canada (grant A29 18).

ANDERSON, M. R., CARDINAL, A., and LAROCHELLE, J. 1981. An alternate growth pattern for Laminaria longicruris. J. Phycol. 17: 405-411.

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Seasonal growth of Laminaria groenlandica as a function of plant age