Spatial and temporal patterns in abundance of two intertidal seagrasses, Zostera americana den hartog and Zostera marina L.

Aquatic Botany, 12 (1982) 305--320 ]~sevier Scientific Publishing Company, Amsterdam -- Printed in The Netherlands

305

SPATIAL AND TEMPORAL PATTERNS IN ABUNDANCE OF TWO INTERTIDAL SEAGRASSES, Z O S T E R A A M E R I C A N A DEN HARTOG AND ZOSTERA M A R I N A L.

PAUL GARTH

HARRISON

Department of Botany, University of British Columbia, Vancouver, British Columbia, V6T 2B1 (Canada) (Accepted 20 July 1981)

ABSTRACT Harrison, P.G., 1982. Spatial and temporal patterns in abundance of two intertidal seagrasses Zostera americana den Hartog and Zostera marina L. Aquat. Bot., 12: 305--320. The population dynamics o f two temperate seagrasses, Zostera americana den Hartog and Z. marina L., were studied on an intertidal transect in Boundary Bay on the Pacific coast o f Canada. Z. americana grew over most of the study area below the mean higher high water level, but Z. marina grew only below the mean lower low water level. Distributions most likely were restricted by tolerance of exposure to air and were modified by the irregular topography; e.g. two zones o f dense Z. americana were separated by a channel in which Z. marina dominated. Rates o f vegetative growth and flowering were not constant over the intertidal range of either seagrass. In May, vegetative shoots o f Z. americana were more abundant and heavier in the lower intertidal zone than in the upper intertidal, but by the end of September the shoots were more abundant in the upper zone and the mean dry weight was constant over the transect. Flowering spread during the summer from a small portion of the upper zone (in May) both lower and higher on the transect; the heaviest reproductive shoots grew in the lower intertidal zone. In May, Z. marina had a high density and biomass of vegetative shoots in the mid-intertidal channel, but during the summer that population declined and plants lower on the transect flourished. Flowering, too, peaked earlier in the channel than in the lower intertidal zone. From early May to late September, Z. americana contributed 60--85% of the total shoots on the transect but only 37--69% of the dry weight. Overall, the density and biomass were less variable in the perennial Z, marina than in the annual Z. americana which yearly colonized many hectares from seed.

INTRODUCTION

Seagrasses of the genus Zostera often cover many hectares of intertidal sand and mud providing food for migrating waterfowl and for foraging invertebrates and fish at high tide (Kikuchi and P~r~s, 1977; Wyer et al., 1977; Harrison, 1979). Intertidal Zostera beds commonly consist not only of Zostera marina L. (eelgrass) but also of a species in the subgenus Zosterella, either Z. noltii Hornem. in Europe (den Hartog, 1973), Z. japonica Aschers. & Graebn. in

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© 1982 Elsevier Scientific Publishing Company

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Asia (Arasaki, 1950; K. Aioi, personal communication, 1980), or Z. americana den Hartog on the Pacific coast of North America (Harrison, 1979). In the area of this study, south-western British Columbia on the Pacific coast of Canada, Z. americana is spreading quickly, colonizing previously barren intertidal flats as well as areas where Z. marina grows (Harrison, unpublished observations, 1975--1981). These intertidal seagrass beds are vulnerable to damage from human activities such as dredging and filling for port construction yet little is known about the structure of the plant communities or the way they function. The few studies which have been conducted on intertidal beds indicate that their population dynamics differ from those characteristic of the more thoroughly studied subtidal beds (Wyer et al., 1977; Keddy and Patriquin, 1978). Only a few aspects of growth and reproduction in Z. americana have been described (Harrison, 1979). This report presents data on the distribution of Z. marina and Z. americana over a 3.2 km intertidal transect and on changes in the patterns of vegetative growth and flowering related to elevation, time of year, and the presence or absence of the other seagrass species. THE STUDY AREA

The general physical and biological features of Boundary Bay (Fig. la) on the south-western coast of British Columbia, Canada, have been described b y Kellerhals and Murray (1969), Harrison (1979) and Swinbanks (1979). Intertidal fiats consisting of fine sands extend over 3 km seaward and are crossed by irregular drainage channels (Fig. lb). A transect was established running from a point near the dyked shoreline (49 ° 5' N; 122 ° 56' W) due south for 3.2 km to the outer limit of Z. americana which was near the lower end of the intertidal zone (Fig. lb).

~

,

10

Fig. 1. (a) Location of Boundary Bay in south-western British Columbia, Canada. Intertidal fiats are stippled. (Modified after Kellerhals and Murray, 1969.) (b) Location of seagrass beds (shaded), dyked shoreline (hatched line), transect, and bare intertidal areas (blank) in Boundary Bay. (Modified from Swinbanks (1979) using May 1978 satellite (Landsat) photographs supplied by Canada Centre for Remote Sensing, Ottawa.)

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MATERIALS AND METHODS

In April 1978 observations were made on the distribution of two seagrasses, Z. americana and Z. marina, along the transect and then 15 stations were chosen to represent zones o f approximately uniform species composition and density. These zones ranged in length from 100 m (commonly) to 400 m. At 2- to 4-week intervals from early May to the end of September 1978 the shoots were clipped at the level of the youngest root bundles in five randomly placed quadrats (0.25 m 2) at each station. The plants were transported to the laboratory (a 1 h journey) in plastic bags in a cooler and then were washed for a few minutes in fresh water to remove sediment and most epiphytes. Crustose algae and diatoms were not completely removed by the washing, but microscopic observations showed that t h e y never covered more than 5--10% of the leaf surface and so these epiphytes were considered to be a small component of the biomass. Clean vegetative and flowering shoots of each species were counted, dried in a forced air oven at 60°C for 24 h (a time which gave constant weight), cooled in a desiccator and weighed. On each sampling date, the total number and biomass of shoots in a 1 m wide strip along the transect were estimated as follows: the mean value at each station was multiplied by four to give a value per m 2 which was then multiplied by the length of the uniform zone represented by that station, and the zonal values were summed. The largest coefficient of variation for any station was used as an estimate of the maximum variability of the sum for the transect. For average values, the sums were divided by 3200 (the length of the transect in metres). Comparison of the patterns of distribution of each species along the transect from May to September were made with the aid of cumulative frequency curves constructed as follows: the total number or biomass of one type of shoot over the whole transect, for example of vegetative shoots of Z. marina on the May sampling date, was equated to 100%; starting with 0% at the landward end o f the transect, the number (or biomass) of shoots in each zone was added to the total of the previous zones and the new total was expressed as a percent o f the total for the transect. These curves emphasize the changes in relative density or biomass, i.e. the pattern. Survey data from Swinbanks (1979) showing the topography of the transect were studied for help in explaining the patterns of distribution of the two seagrasses. In 1979 three stations on the transect were chosen for study of the patterns of distribution of biomass among different parts of the two plants when each species grew alone or when t h e y co-occurred. Station A, 2.1 km from shore, had a pure population of Z. americana: station B, 2.7 km out, had approximately equal amounts of the two species; and station C, 3.1 km out, had a pure Z. marina population. At 2- to 4-week intervals from May to August, five replicate quadrats (0.25 m 2) were dug to a depth of 30 cm. The plants were cleaned; sorted into leafy shoots, flowering shoots and rhizomes plus roots; dried at 60°C to constant weight; cooled in a desiccator; and weighed. Ratios o f

308

aboveground to belowground biomass and of flowering shoot biomass to total plant biomass (=reproductive effort} were calculated. RESULTS

Average densities and biomass

The coefficients o f variation for means of the quadrat data ranged from 5 to 20% so only seasonal trends (maxima and. minima) will be considered important. The average density of Z. americana shoots increased 200% from May to early June due to the proliferation of leafy shoots (Fig. 2a, b). A smaller

TOTALS

Z. a m e r i c a n a

|a ~

600

Z. m a r i n a

200

SHOOTS600 t

•M-24001

~300

100 I

i

2G

f

DRY WT

(G M"2)

1c

vM

10

t

J

J

A

S

l

J

l

l

M J J A S

M

J

J

A

S

Fig. 2. Average density and biomass of shoots of Z. americana and Z. marina along an intertidal transect, showing changes from early May to end of September. In (a) and (d), the totals for each species are compared; in (b), (c), (e) and (f), the flowering shoots (v), vegetative shoots (~), and totals (e) are compared. Vertical bars represent the maximum coefficient of variation of samples used to calculate the totals for the transect. Note the changes in vertical scales. (20%) increase from late June to August reflected the production o f flowering shoots at that time (Fig. 2b). The densities of both types of shoots decreased quickly during September and masses of drift leaves began to accumulate on the upper intertidal flats. In contrast, the density of Z. marina shoots increased only 28% from May to June and declined thereafter (Fig. 2c). Since vegetative shoots were 80--95% of the totals, the small peak in flowering shoots in July and August had little effect on the decline (Fig. 2c). The maximum densities recorded were 182 Z. marina shoots (96% vegetative) and 634 Z. americana shoots (84% vegetative) in 0.25-m 2 quadrats at different stations. The temporal patterns for shoot biomass of Z. marina paralleled those for

309

densities (Fig. 2f versus c). The biomass of Z. americana, b o t h vegetative and flowering, remained high after shoot numbers declined in late summer (Fig. 2e versus b); for flowering shoots the values from June to September were not statistically different from one another, b u t biomass of vegetative shoots in September was less than in July (using Student's t-test). Although Z. americana made up 60--85% of t h e total n u m b e r of shoots along the transect, it contributed only 37--69% of the total biomass {Fig. 2a, d). The maximum biomass recorded for Z. marina was 28 g dry wt. per 0.25 m 2, 96% of which was vegetative; for Z. americana the maximum was 18.2 g, 57% of which was vegetative. Intertidal distributions

When the total densities of shoots of the two seagrasses in each part of the transect were plotted as in Fig. 3a, a pattern was clear: Z. marina was abundant 100~ Z. a m e r i c a n a

50C SHOOTS M- 2

0

500~-

Z ....

ina

3 SEDIMENT HEIGHT 2

HW .....

(M) 1 0

1 2 3 DISTANCE FROM SHORE (KM) Fig. 3. (a) Bimodal distribution of Z. a m e r i c a n a and Z. m a r i n a along an intertidal transect

in May. (b) Surveyed sediment elevations above chart d a t u m along the transect. MHHW, mean higher high water level; MLLW, mean lower low water level. (Adapted from Swinbanks, 1979.)

in two regions where Zo americana was rare, and vice versa. The pattern lasted throughout the period of the study and re-occurred in 1979 {Harrison, 1979, unpublished data). A similar pattern was observed in biomass data although the relative heights of the peaks were n o t always consistent b e t w e e n graphs for density and for biomass. For comparison with the pattern in distribution of the plants, Fig. 3b provides survey data on the height of the sediment relative to chart datum (lowest water level). A few major features are: (1) no

310

seagrasses grew above the +3.0 m level, but a blue-_green algal m a t and a narrow salt marsh occupied the higher areas; (2) Z. americana was c o m m o n only below the mean higher high water level (+2.7 m); (3) Z. marina grew only below the +2.0 m level and was c o m m o n below the mean lower low water level (+1.9 m); and (4) the gradual decline in height of the sediment with increasing distance from shore was interrupted by troughs at 1.1 km and from 1.6 to 2.2 km from shore. The first trough represented a system of sand waves crossing the upper part of the transect (Swinbanks, 1979). These features have an amplitude of 20 cm or more and a wavelength of up to 100 m; by chance many were missed by the surveyor Who measured heights at 90 m intervals. At its upper limit, Z. americana grew in the troughs of sand waves and in other depressions, but in the region from 1.1 to 1.6 km from shore the plant was common on slightly elevated areas while Z. marina grew in the intervening depressions. The wider trough (1.6--2.2 km) is the head of a drainage channel which crossed the transect at an oblique angle (Fig. lb).

Temporal and spatial patterns Although the general pattern shown in Fig. 3a was found throughout the study period, the relative contribution of the two peaks to the totals, for examples of Z. americana flowering shoot biomass or Z. marina vegetative shoot numbers, varied with time. The patterns of distribution of the vegetative and flowering components of the two seagrasses are shown in Figs. 4 and 5 for 100 SHOOTS %

Z arnerican~

•C

Z marina

:

50 VEGETATIVE

100

/

d

FLOWERING50

1

2

3

DISTANCE FROM

SHORE

2 (KMI

3

Fig. 4. Cumulative frequency curves for shoot numbers, showing changes in the relative abundances of Z. americana and Z. marina along an intertidal transect from early May (solid line) to mid-July (broken line) and late September (dotted line). Arrows indicate the division between upper and lower zones of the two species.

311

100

Z. marina

121

BIOMASS

,,," '

C

%

MAY~,.:..':

50 VEGETATIVE

0 100

b

FLOWERING 50

1

2

3

i

DISTANCE FROM SHORE

2 (KM)

Fig. 5. Cumulative frequency curves for aboveground biomass, showing changes in the relative abundances of Z. americana and Z. marina along an intertidal transect from early May (solid line) to mid-July (broken line) and late September (dotted line). Arrows indicate the division between upper and lower zones of the two species.

early May, mid-July, and the end o f September, representing, the beginning, middle and end of the growing season, respectively. Regions of the graphs with steep slopes correspond to areas of the transect with dense growth of a particular species. The graphs for vegetative components {e.g. Fig. 4a, c) show an upper Z. americana zone approximately 0.4--1.9 km from shore and an upper Z. marina zone from 1.4 to 2.2 km. The numbers of shoots and biomass, both in absolute terms and as a percent of the transect totals, in these upper zones are summarized in Table I. Z. americana vegetative shoots (Figs. 4a, 5a, Table I) In May the upper zone of Z. americana accounted for a larger proportion of the shoots (42%) than of the biomass (31%) because shoots in the upper zone had a lower mean dry wt. (16 mg) than did shoots in the lower zone (26 mg). As the total density of vegetative shoots increased from May to July, twice as m a n y shoots were added in the lower zone as in the upper zone, but the leafy shoots in the upper zone almost doubled in weight (to 29 mg) while shoots in the lower zone remained at 26 mg; thus the contribution of the upper zone to the number of shoots declined while its proportion of the biomass increased. As the total density and biomass declined from July through September, three times more shoots were lost from the lower zone than from the upper zone, and the relative contribution of the upper zone reached 58% of the numbers and 56% of the biomass. The mean dry weight per shoot was 55

312 TABLEI Abundance and biomass of vegetative and flowering shoots of Z. americana and Z. marina in their respective upper zones (a 1 m wide strip along the transect from 0.4 to 1.9 km from shore for Z. americana and 1.4--2.2 km for Z. marina), showing changes during the growing season Z. americana

Vegetative shoots Number (× 103) Percent of transect total Biomass (kg) Percent of transect total Flowering shoots Number (× 103) Percent of transect total Biomass (kg) Percent of transect total

Z. marina

May

July

Sept.

May

July

Sept.

234

501

316

198

169

56

42 3.8

37 14.6

58 16.8

56 9.6

47 13.6

31 8.0

31

40

56

54

38

41

3

212

58

14

12

0

48 7.8

35 1.8

45 1.5

25 1.1

0

40

13

42

20

0

92

0.1 92

0

mg in both zones. The part of the transect from 0.4 to 0.9 km from shore gained importance in September because the relatively small population there remained into early a u t u m n when shoots further out on the transect were lost. Z. americana flowering shoots (Figs. 4b, 5b, Table I) In May flowering of Z. americana was just beginning and was restricted almost totally to a portion of the upper zone (1.2--1.5 km). By July flowering had spread into the lower zone and was almost equally c o m m o n in the two zones although shoots in the upper zone were slightly heavier (mean dry wt. of 36 mg versus 20 mg in the lower zone). In later summer the upper zone lost 72% of its flowering shoots while the lower zone lost only 52%; in addition the maturing reproductive shoots in the lower zone grew very heavy {mean dry wt. of 100 mg compared with only 33 mg in the upper zone). The flowering shoots in the high intertidal region (0.4--1.2 km) gained importance in September only because they persisted while shoots lower on the transect were lost. Z. marina vegetative shoots (Figs. 4c, 5c, Table I) From May to September the number of vegetative shoots of Z. marina in the upper zone declined both in absolute terms and in relation to the transect totals. The tripling of mean dry wt. from 49 to 143 mg was not enough to prevent the relative biomass from declining as well. From May to July, when the

313

total density of vegetative shoots on the transect increased, the upper zone actually lost 15% of its shoots; only in the lower zone did the density increase (by 22% over May values). As the total density and biomass decreased from July through September, twice as many shoots were lost from the upper zone as from the lower zone, b u t the relative biomass in the upper zone did not decline; i.e. mainly smaller shoots were lost. Shoots in the lower zone had a lower mean dry weight (92 mg) than did those in the upper zone (143 mg) in September. Throughout the study the zones o f concentration of Z. marina maintained their original linear limits along the transect. Z. marina flowering shoots (Figs. 4d, 5d; Table I) In May flowering shoots o f Z. marina were found in the whole lower zone but only in a narrow region of the upper zone (1.5--1.9 km). The upper zone held slightly less than half of the numbers and biomass, but b y July this zone was narrower and contributed only 20--25% of the totals. In late summer no flowering shoots were found in the upper zone and the lower zone had shrunk; all the remaining flowering shoots grew b e y o n d 2.7 km from shore. The mean biomass of flowering shoots peaked in May and July (100 mg in the upper zone, 125 mg in the lower zone) and declined to only 55 mg in September. Allocation of biomass Although the early spring biomass of shoots was equally low for Z. americana no matter where it grew, the peak biomass and density of shoots and the peak biomass of rhizomes and roots were greater at station B, where the t w o species grew together, than at station A, where the smalle~ species grew alone (Table II). The ratio of aboveground to belowground biomass was equal at the two sites, b u t the reproductive effort (ratio of biomass of flowering shoots to total plant biomass per quadrat) was higher in the 2-species associations. Z. marina maintained a higher overwintering shoot biomass and grew larger and denser when it grew alone than when it was mixed with Z. americana (Table II, station C versus B). In both situations the reproductive effort of Z. marina was low, b u t the ratio of aboveground to belowground biomass was greater in the 2-species associations. DISCUSSION

Average densities and biomass From spring to autumn the changes in average density and biomass were more pronounced for Z. americana than for Z. marina. In addition, sexual reproduction accounted for a larger proportion of the total biomass in Z. americana than in Z. marina. The biomass of Z. marina shoots in Boundary Bay was only 50% or less of that reported in an intertidal habitat in nearby Puget Sound, Washington State, U.S.A. (Phillips, 1972) and in shallow subtidal habitats in

314 TABLE II Total biomass, density, and allocation of biomass to different parts of Z. americana and Z. marina, showing differences when the two plants grew together or alone' Z. americana

Leafy shoots, dry wt (g) Early spring August (max.) Belowground, dry wt. (g), August Shoot density, August Aboveground: belowground biomass, August Reproductive effort, % (max.) 2

Z. marina

Station A Alone

+ Z. marina

Station B

Station C Alone

Station B + Z. americana

0.0--0.2 (0.1) 1.3--2.5 (1.5) 0.5--1.1

0.0--0.3 (0.1) 3.5--6.9 (5.4) 0.1--3.5

9.0--14.0 (11.0) 8.4--21.1 (14.6) 11.3--19.8

0.2--1.2 (0.4) 2.9--10.7 (4.8) 1.4--6.4

(0.8) 90--225 (162) 2.0--2.6

(1.8) 190--440 (365) 2.0--4.0

(13.0) 140--225 (190) 0.8--1.6

(2.7) 0--150 (47) 1.6--1.8

(2.4) 3.1--10.2

(2.7) 8.1--14.2

(1.1) 0.3--5.4

(1.7) 0.5--6.1

(7.1)

(11.2)

(2.2)

(3.2)

1Data are ranges and means (in parentheses) of five samples (0.25 m2). Pairs of means which are underlined are significantly different at the 95% confidence level using Student's t-test. 2Reproductive effort = ratio of dry wt. of flowering shoots to total plant dry wt. × 100. Denmark (Sand-Jensen, 1975) and south-western British Columbia (Moody, 1978), but the pattern of seasonal growth was similar to that reported in most other studies. In north temperate habitats the time of peak shoot biomass of Z. m a r i n a has been reported as June--September (Phillips, 1972), June--August (Sand-Jensen, 1975), June--September (Nienhuis and de Bree, 1977, 1980), September (Wyer et al., 1977), June--July (Moody, 1978) and August--September (Jacobs, 1979), while in subtropical Japan the peak occurred in May (Arasaki, 1950; Aioi, 1980). The June--July peak in Boundary Bay (Fig. 2f) follows the c o m m o n temperate habitat pattern. New shoots of eelgrass are produced beginning in February--April (Phillips, 1972; Sand-Jensen, 1975; Jacobs, 1979), with peak shoot densities coinciding with peak biomass. In this study the early growth was not monitored, but observations the next year confirmed that new Z. m a r i n a shoots appeared in late March and early April in Boundary Bay and that a substantial overwintering leafy shoot biomass occurred. Flowering shoots averaged less than 10% of the total numbers in Puget Sound (Phillips, 1972) and Japan (Aioi, 1980), about 4% in Denmark (calculated from data of Sand-Jensen, 1975) and from 8 to 15% in Boundary Bay (this study). Taken together, the observations on Z. m a r i n a confirm the generally accept-

315 ed idea that the plant is a perennial seagrass with a marked seasonal cycle of growth characterized b y a large overwintering biomass; rapid leaf growth and shoot proliferation in early spring; flowering in spring and early summer accounting for a small proportion of the total effort of the plants; and a gradual decline in shoot numbers and biomass over the summer and autumn. Major exceptions to this pattern have been reported b y Wyer et al. (1977) and Keddy and Patriquin (1978). In b o t h those studies intertidal Z. marina grew as an annual with, therefore, a dependence on seed production and seedling recruitment In the case of Keddy and Patriquin (1978), the plants grew high in the intertidal and the shift to an annual cycle may be an adaptation to a habitat with extreme conditions of heat and cold, i.e. an r-strategy (Pianka, 1970). The Z. marina population studied by. Wyer et al. (1977) grew in the lower intertidal zone, a habitat normally populated b y perennial Z. marina with a K-strategy suited to a more stable environment (Pianka, 1970; Harrison, 1979); thus the annual cycle of this population is w o r t h y of further study. The seasonal pattern of growth of Z. americana is a marked contrast to that of Z. marina. Although not monitored in this study, the overwintering shoot biomass and density of Z. americana is negligible over most of its intertidal range (Harrison, 1980, unpublished data). Most of the huge increase in both leafy and flowering shoots in spring is the result of seed germination and seedling establishment beginning in March or April. Leaf biomass peaked in June, coincident with the peak in Z. marina, b u t remained high all summer and declined in early autumn long after Z. marina had declined. Flowering began 2 months later than in Z. marina; since flowering shoots are a sink for materials translocated from the mature leafy shoots (Harrison, 1978), the delay may reflect the time needed f o r seedlings to grow before being able to support flowers. There are no published reports on Z. americana with which to compare the results of this study. However, in England Z. noltii, a species in the same subgenus, occupied habitats similar to those of Z. americana in Boundary Bay (Wyer et al., 1977). The seasonal pattern of growth of the two species were quite different; Z. noltii held its leaves into the winter and grew right through a mild winter (Wyer et al., 1977). In Boundary Bay and nearby localities, Z. americana only rarely maintains any aboveground biomass over winter other than dead flowering shoots. Intertidal distributions The outer end of the transect was chosen to coincide with the lower intertidal limit of Z. americana, b u t Z. marina extends into the subtidal region. The lower intertidal peak in Z. marina, therefore, is an artifact of sampling, b u t to explain the patterns in the rest of the transect it is necessary to look carefully at the topography (Fig. 3b). Near the upper limit of Z. marina small variations in sediment level are accompanied b y local variations in the success of the two seagrasses; the result is a mosaic with elevated patches of Z. americana

316

and intervening patches of Z. marina in puddles left by the receding tide. A similar pattern was reported on English beaches (Wyer et al., 1977) and on the European Atlantic coast (den Hartog, 1973), although in those studies the two species were Z. noltii and Z. marina. Limitation of the upper intertidal extent of Z. marina to the mean lower low water level has been attributed to the stresses accompanying exposure to air (Johnson and York, 1915; Phillips, 1972) and it is c o m m o n to find the plants growing only in small pools at their upper limit (Keller and Harris, 1966). It appears from the present study that Z. americana can withstand longer periods of drying than can Z. marina. Morphological differences may account for part of the habitat difference. The base of a Z. marina shoot, containing the meristem, is stiff and does not lie flat on the sediment at low tide. Because the meristem is sensitive to damage by drying (Tutin, 1942), the plant may grow poorly unless it is in depressions in the sediment where water remains at low tide or, if no standing water remains, at least the sediment is muddier than on the elevated areas around. In the latter case, the fine sediments (which are c o m m o n on the surface of these depressions in Boundary Bay) may retain water longer than the coarser sand (Webb, 1958; Shepard, 1973). Shoots of Z. americana, on the other hand, lie closer to the sediment at low tide and may be better protected by even the scant moisture in the surface layers of coarse sediments. Experimental work is required to establish the exact reason for the small-scale pattern in the distribution of the two seagrasses in the upper intertidal zone. The major feature of the distribution of the seagrasses which remains to be explained is the mid-intertidal zone of dense Z. marina between the two zones of Z. americana. The limits of Z. marina corresponded loosely to the drainage channel which crossed the transect (Fig. 3b). To the seaward side of the channel the sediment rose abruptly from 1.4 to 1.6 m above chart datum and Z. americana totally replaced Z. marina. The boundaries of the plant zones did not coincide exactly with the limits of the channel as shown in Fig. 3, but heights were surveyed only every 90 m along the transect, the channel cut obliquely across the transect, and the pattern of ebb and flood tides probably was not symmetrical on both sides of the channel. The channel represents an intrusion of the subtidal zone into the intertidal region. Temporal and spatial patterns The results of this study confirm the reports of den Hartog (1970, 1973) that large intertidal beds o f temperate seagrasses cannot be treated as being uniform in either space or time. Z. marina exhibited different seasonal patterns of vegetative growth and flowering in the mid-intertidal channel and the lower intertidal zone. Early spring leaf biomass per unit area was greater in the channel, where plants were always covered by at least a few centimetres of water, than in the lower intertidal zone, but as the summer progressed more growth and flowering occurred in the more exposed population lower on the

317

transect. With respect t o exposure to air, the channel is really a subtidal habitat and thus the reduced rate of sexual reproduction in the channel agrees with observations b y Phillips (1972) and Harrison (1979) that flowering shoots are less abundant in subtidal than in intertidal habitats. An increase in sexual reproduction often accompanies growth in a less stable habitat (Pianka, 1970) and it can be argued that the intertidal zone is a less stable habitat for a marine plant than is the subtidal zone (Harrison, 1979). If exposure to air were the only factor limiting growth in Z. marina, then the decline of the channel population and the increase in relative and absolute abundance in the lower intertidal zone from spring to summer is puzzling. Water temperature may be the critical factor since excessively high temperatures (above 30--35 ° C) result in lower photosynthetic rates or even defoliation (Biebl and McRoy, 1971; Orth, 1976). In Boundary Bay during the summer the lower of the two daily low tides occurs from mid-morning to mid-afternoon, allowing sunlight to warm the shallow water of the channel. Temperatures of 30--35°C were recorded in the channel in July; surface waters at the edge of the subtidal zone reached only 12--16°C. Thus, the lower intertidal and channel populations of Z. marina were exposed to different temperature regimes even though both were submerged most if not all the time. Another factor which may have contributed to the decline of the channel population is the growth of epiphytes which can reduce the rate of photosynthesis of eelgrass (Sand-Jensen, 1977). Epiphytes were more abundant in the channel than in the lower intertidal zone {Harrison, 1978, unpublished data). The relatively large contribution made b y the channel eelgrass population to the overall biomass during May most probably reflects favourable growing conditions during winter and early spring when the daytime low tides expose only the upper part o f the intertidal zone. In winter the channel may receive sufficient light for growth while the lower intertidal population may be limited b y low light levels. Irradiance is k n o w n to control growth of eelgrass (Burkholder and Doheny, 1968; Backman and Barilotti, 1976). Despite the seasonal fluctuations in density and biomass of Z. marina, the total area covered b y the plant did not change during the period of the study and it remained constant the next year (Swinbanks, 1979). Z. americana exhibited wide variations in both the area covered and the timing of growth and flowering in different parts of its intertidal range. Germination of seeds and the proliferation of shoots from the branching of seedlings may have begun synchronously throughout the intertidal zone, but it ceased first in the higher areas where vegetative shoots continued to add biomass. In the lower intertidal zone, new shoots were added even in mid-summer, b u t the average shoot biomass did n o t increase. Because small shoots were the first to be lost in autumn, the lower intertidal population of Z. americana declined quickly whereas the larger vegetative shoots in the upper population were retained longer. Flowering spread from the mid- and upper-intertidal zones to areas both lower and higher on the shore during the summer. The annual colonization of the intertidal zone via seed germination is similar to the

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pattern of the intertidal populations of Z. marina studied by Wyer et al. (1977) and Keddy and Patriquin (1978), but it is quite distinct from the pattern of the perennial Z. marina in Boundary Bay. Seasonal changes in the areal extent of Z. americana cause the upper limit of seagrass beds in Boundary Bay to migrate about 400 m each year. Because of the time of year in which aerial photographs have been taken or technical difficulties in interpreting the photographs due to the reflectance characteristics of the plants, sediments and water, the migration of the upper boundary has not been detected from the air and thus maps (such as Fig. l b ) which are based on photographs are inaccurate. One factor not yet considered which may affect the abundance of seagrasses is grazing b y waterfowl. The brent goose (Branta bernicla (L.)), which is known elsewhere to eat Z. marina leaves, is a c o m m o n winter inhabitant of Boundary Bay (Taylor, 1970), but no quantitative estimates of grazing on either seagrass are available from the study area. Since the proportion of eelgrass production which is consumed by brent geese varies widely (Nienhuis and van Ierland, 1978; Charman, 1979), the influence of grazing on the distribution of Z. marina and Z. americana in Boundary Bay is unknown. Allocation of biomass Z. americana allocated similar proportions of its biomass to vegetative shoots and rhizomes in areas where it grew alone and where Z. marina also grew, but the proportion of biomass in flowering shoots was significantly higher where Z. americana grew in association with eelgrass. It could be argued that because Z. americana achieved a higher total biomass at station B {mixed) the plants had more energy to use for reproduction, b u t the data of Harrison (1979) suggest that if there is any relationship between reproductive effort and total biomass, it is that higher reproductive efforts occur in areas with lower total biomass. Thus it is likely that Z. americana responded to the co-occurrence of Z. marina by increasing its potential o u t p u t of seeds. Of course, an increase in biomass of flowering shoots does not directly imply an increase in the number of successful seedlings in the next generation. Work is underway in the author's laboratory on the processes affecting the production and germination of seeds. Z. marina had equally low reproductive efforts when growing alone or with Z. americana. The response of Z. marina to the co-occurrence of Z. americana appeared to be an increase in the biomass of leaves relative to other components. The responses of both plants confirm the idea of Harrison (1979), who studied the two species in pure populations and concluded that Z. americana is heavily dependent on sexual reproduction while Z. marina uses leafy growth to monopolize its habitat. It remains to be seen whether the two species are n o w in equilibrium or whether Z. americana is capable of future expansion at the expense of Z. marina.

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ACKNOWLEDGEMENTS

This work was supported financially by the Natural Sciences and Engineering Research Council of Canada through an Operating Grant and by the Canadian National Sportsmen's Fund. Fieldwork would have been impossible without the cheerful assistance of D. Burt, R. Forman, A. Listrum, A. Pearson, B. Reid and K. Rush. Able technical assistance was provided by S. Schwab. Many useful suggestions were provided by two anonymous reviewers of the manuscript.

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