Estimation of the non-seasonal production of Spartina maritima (Curtis) Fernald in a South African Estuary

Estuarine,

Coastal and Shelf Science (1983)

16, 24X-254

Estimation of the Non-seasonal Production of Spartina maritima (Curtis) Fernald in a South African Estuary

Shirley M. Pierce” Zoology Department, University Port Elizabeth, South Africa

of Port

Elizabeth,

Received IO May 1982 and in revised form

Keywords:

Spartina

; production

I

September 1982

; method ; decomposition

; estuaries ;

South Africa Net aerial production of Spartina maritima (Curtis) Fernald, in a warm temperature estuary in Algoa Bay, South Africa, occurring possibly as an exotic, was estimated as 523-680 g dry weight m-* year-l. The method of production measurement designed here used community structure data and accounted for the species’ extremely slow shoot production (3’1-6’7 dry g m-* year-‘) and continuous leaf turnover (516-676 dry g m-’ year-‘). Standard methods of production measurement for other Spmtina species failed by not accounting for the non-seasonal growth of S. maritima. N, C, organic and energy content of live and dead shoots remained constant through the seasons. The P : B ratio is 1.1, which is lower than for other Spartina species, but agrees. with the low vigour shown by negligible regrowth a year after clipping. Decomposition rates were 90 mg g-’ month-’ in winter and 305 mg g-’ month-’ in summer. Monthly decomposition values showed significant correlation with air temperature (Y = 0.86; P
Introduction Sputtina maritima, though possibly an introduced species (Pierce, 1982), is nonetheless a dominant macrophyte in the estuaries on the south-east coast of South Africa. In the Swartkops Estuary it covers about 82 ha of a total 363 ha of intertidal marsh. This estuary lies in the South warm-temperate zone (Figure I) [Koppen 0% (Schulze & McGee, 1978)] with a non-seasonal rainfall (fsoo mm year -‘). The mean annual temperature is 17.3 “C! with a mean range of 10.1 “C. Absolute maximum temperature was 36.3 “C in February 1977 and absolute minimum was 2 “C in June, 1977. The estuarine water is saline (&35x0) and nutrient content fluctuates widely through the year possibly as a result of sewage and industrial pollution. Total N and P values ranged from 349 to 1943 pg 1-l and 43 to 2470 pg 1 -l respectively. Primary production studies on species of Spartina, reputed to be one of the most productive plants in the world (Odum, 1971) have featured widely in the literature (Keefe, 1972; a Present Rondebosch,

0272~7714/83/030241+14

address : Botany South Africa.

803.00/o

Department,

c

University

1983 Academic

of

Press Inc.

Cape

‘Town,

(London)

7700

Limited

242

S. M. Pierce

n l

Figure Africa.

I. Locality

of study

sites

on the

Creek Station River Station

Swartkops

Estuary

in Algoa

Bay,

South

Kirby & Gosselink, 1976; Turner, 1976; Hardisky & Reimold, 1977; Linthurst & Reimold, IC@; White et al., 1978; Eilers, 1979; Smith eZ al., 1979). A method of production measurement was designed in this study to account for the continuous growth and absence of seasonal die-back, peculiar to S. maritima. The method involved detailed measures of shoot and leaf growth and community structure. In addition, three standard methods, namely those advocated by Milner & Hughes (r97o), Smalley (‘959) and Wiegert & Evans (1964) used widely on North American Spartina species were included here for comparative purposes. Nutrient status in terms of N, C, organic and potential energy content were also measured as part of the input into the estuarine ecosystem model currently being prepared by the Zoology Department, University of Port Elizabeth. Methods Sample sites A river station and a creek station were selected as sites to account for some local variation (see Figure I). At both sites Tall and Medium height forms of S. maritima were recognized, in accordance with the same observation for other Spartinu species (e.g. Smart & Barko, 1978). Short form S. maritimu was not sampled due to its scarcity. Production methods Method I devised for this study of S. muritimu, measures net aerial production as the sum of leaf and shoot production. It is a composite method based on detailed analysis of community structure in terms of the relative frequency of size classes throughout the year, and on the shoot and leaf production of the different size classes of shoots. For clarity these parameters, used in this method to derive production, will be described separately. Community structure. Individual live shoots from three Tall and three Medium samples harvested at the river site were dried, weighed and sorted into size classes of o-1-g intervals. These data were expressed as mean monthly frequency histograms. The number of flowering shoots was noted. Shoot production. Measurement involved monitoring shoot height growth of different size classes, and using community structure data for the relative frequency of the size classes to determine monthly shoot production.

Non-seasonal

production

of Spartina maritima

243

Monthly height increasesin 50 Tall and 50 Medium labelled shootsat both the river and creek sites were monitored. The height of shootsof known age was determined from new shoots which appeared adjacent to labelled shoots. Shoot heights monitored at monthly intervals were plotted and three possibletypes of growth curve-exponential, symmetrical and unsymmetrical sigmoid curves-were fitted by least squares regression using the BMDP 3r computer program for non-linear regression(Dieckman, 1978). For conversion of height to mass,individual fresh shoots(227 Tall and 344 Medium) were measuredand their dry massrecorded after 24 h at 80 “C. The data were fitted to power curves by least squares regression. Using this shoot height : weight regressionthe growth curves were divided into size classesof o-1-g dry weight intervals. The growth rate of eachsize classwas determined from the appropriate slope of the growth curve. Community structure data provided the number me2 of individual shoots within each size classeach month. This number was then multiplied by the appropriate growth rate to yield production of a particular size classof shoots.Summing of theseequalled total shoot production m m2month-‘. Briefly, determination of leaf production = number of leaves produced monthly ~mean mass of individual leaves~number of shoots me2 each month. Actual determination was more detailed as leaf production from a range of size classesshootswas measured. The method is similar to that used by Hatcher & Mann (1975) to determine biomasslossprior to peak biomass,but is more detailed. Leaf number wasmonitored eachmonth from December 1976-November 1977 by marking leaveswith a felt-tipped pen. From the range of size classesof shoots(small = 0-0.19 dry g; med = 0x-1.09 dry g; large > 1.1 dry g) leaveswere picked, .dried and weighed. Mean leaf massfor each size classwas calculated. Frequency of shoots within each size classeach month was derived from the community structure data .The products of each size class were summedto equal total leaf production m -2 month-l. Leaf production.

Method z devised by Wiegert & Evans (1964) for grasslandshasbeen usedin North America to measureproduction of Spartina wetlands (Kirby & Gosselink, 1976; Hopkinson et al., 1978; Linthurst & Reimold, 1978a) and was recommendedby Turner (1976). Production is calculated from change in live biomassplus mortality losses,where mortality includes dead production and loss by decomposition. Kirby & Gosselink (1976) summarized the theoretical basisasfollows : 2’

A2

Net production

t Dead production or mortality

-Live biomass

A3 Dead biomass

f Disappearance of dead vegetation

Value A3 = instantaneous loss rate [g lost (g dead vegetation) -l (time)-l] ~mean dead biomassfor sampling period. A2 = A3 + A dead biomass. Net production 2’ = A2 + A live biomass. The parameters of live and dead biomassand instantaneous loss rates are discussed separately below. Biomass. Biomasswas sampledat the river and a creek station (seeFigure I) on a monthly basisfrom October 1976 to January 1978,and bimonthly over the two November-December

244

S. M. Pierce

periods. Five o*25-m2quadrats were sampledin Tall riverside stands and also in Medium height, more elevated standsat both sites. Shoots rooted within the quadrat and all standing dead and litter were collected. Sampleswere washed, sorted into live and dead material, and dried at 80 “C for 48 h. Instantaneouslossrates (rr). These rates were measured using litterbags instead of the paired-plot method describedby Wiegert & Evans (1964) due to repeated vandalism. Dead standing material of known masswas used in litterbags to simulate the stagewhen detritus formation begins. Fifteen litterbags, five eachof meshsizesfine (0.4 mm2),medium (0.5 mms) and coarse(1.5 mm2),were placed for the period of I month on the estuarinemud at mid-tide level (seeFigure I). After the exposureperiod, litterbags were washedand the contents dried at 80 “C for 24 h, cooled in a desiccator and weighed. The procedure was repeated each month during 1977, using fresh standing dead each time. The daily instantaneousrate of disappearance(ri) was calculated as:

where W,, and W, are dry litter at the start and end of the time interval respectively, and t,---t, = time interval of 30 days (from Wiegert & Evans, 1964). Method 3 wasadvocated by Mimer & Hughes (1970) and later usedby Gabriel & de la Cruz and Smith et al. (1979). Production is determined from changesin biomassbetween sampling. Monthly net production = (B,--B,-J(t,--t,-i) (1974)

where B, is live biomassat the nth sampleperiod and t, is time at the nth samplecollection. Annual net production = sum of monthly production. Biomassvalues were collected as described in Method 2. Method 4 was devisedby Smalley (1959) and hasbeenwidely used(Stroud & Cooper, 1969 ; Turner & Gosselink, 1975 ; Gallagher et al., 1980). Production is determined from increases in live biomassduring each sampling interval and accountsfor lossesby death, grazing and removal from the area. The method was summarized by Turner (1976) as follows, where NP is net aerial production, If A live and A dead biomassboth +ve, NP = A live+A dead. If A live and A dead biomassboth -ve, NP = o. If A live biomassis -ve and A dead +ve, NP = A live+A dead if sum is >o; otherwise, if sum -ve, NP = o. If A live biomassis +ve and A dead -ve, NP = A live. Biomassvalues used were collected as describedin Method 2. Nutrient

status

Each month dried, ground subsamplesof live and deadmaterial were analysedfor N content (micro-Kjeldahl sensuHesse, 1971), C content on a CNH Analyser, and ash-free (organic) content by ashing at 450 “C for 5 h. Potential energy content was measuredon an adiabatic bomb calorimeter. All analyseswere duplicated or repeated until error was within 1% of the meanfor energy value and 5% for N and organic contents. Values from three consecutive months were averaged.

Non-seasonal

of Spartina maritima

production

245

Results and discussion Parametersused in the different method for derivation of production values are discussed separately for clarity; a comparisonof the methods is given later. Biomass

Live and dead biomassof Tall and Medium shoots are depicted in Figure 2. Harvested samplesyielded representative results, with percentage error of monthly samplesfor both sites and forms rarely >IO% and never >16%. Biomassresults thus conform to I.B.P. standards (Milner & Hughes, 1970). Although live biomass varied through the year, a seasonalpattern is not clear. Within-sample variation is small (&IoO/~ error); however, between monthly sample variation showsmarked fluctuations which are unaccountable.

SONDJFMAMJJASONSONDJFMAMJJASONO Monfh

Figure z. Seasonal biomass of S. maritima in the Swartkops Estuary. (a) Tall, (b) Medium at the river station; (c) Tall, (d) Medium at the Creek station. Bars = z S.E. units where greater than the mean symbol, and tt = 5. 0 = Live; 0 = dead.

The distinct differences in live biomassbetween Tall, streamside shoots and Medium height, inland plants has been well documented for speciesof Spartim (Stalter & Batson, 1969; Mooring et al., 1971; Nixon & Oviatt, 1973 ; Odum & Fanning, 1973 ; Valiela & Teal, 1974; Steever et al., 1976).The hypothesesto explain the different forms are best summarized by Smart & Barko (1978) who proposethat shorter forms of S. aZternijIora are the result of salinity stresswhich is the cumulative effect of ion exclusion and normally high sediment salinity.

The

tidal

subsidy

theory

of

Odum

&

Fanning

(1973)

is complementary

to

this

246

S. M.

Pierce

hypothesis as it explains how greater tidal flushing at streamsides would alleviate salinity stress. Tidal attenuation, and thus greater salinity stress, in the narrow creek may account for the lower biomass at the creek station (Figure 2). Dead biomass at both sites was aseasonal and showed negligible variation within and between sites and seasons (Figure 2). Tidal effects on dead material have been considered major sources of error (Linthurst & Reimold, 1978a, b; White et al., 1978), .but are not seen as important in this study. A tidal export study on the Swartkops Estuary (Pierce, 1979) showed that removal by estuarine waters is negligible; only 6 dry g me2 catchment area was removed by maximal equinoctial tides. Even after heavy floods in May, dead biomass values remained constant and did not show a decrease (Figure 2). Also, almost all material included in the dead biomass sample consisted of standing dead shoots rather than surface litter. Community structure Community structure of Tall and Medium shoots was similar and remained constant through the year (Figure 3). The following height : mass regressions obtained from individual shoots made conversions possible: Tall shoot mass =

O*OOI~

h1.899,

r2 = 0.95, P>O*OI ;

Medium shoot mass = 0.0042 h1*387,r2 = 0.91, P>o.ox. The community structure data shows that half the total number of shoots of both forms are smaller than 0.2 dry g which is equivalent to 17.5 cm tall. This might suggest that 17.5 cm is the mean height of shoots at death. This is corroborated by the fact that mean height of labelled shoots which died during the growth monitoring period was 17.8 cm. Mortality appeared to be very low and constant throughout the year. S. patens and S. cynosuroides also showed constant mortality throughout their growing season which was attributed to normal maturation and mortality rather than a response to environmental stimuli (Hardisky & Reimold, 1977). Flowering occurred from November to March with a maximum of 78 Tall flowering culms mm2 (&o*I~/~ of total number of shoots) and 40 Medium flowering culms rnw2 (fo*og % of total). Shoot production Von Bertalanffy and Gompertz growth curves were the curves of best fit for growth data on Tall and Medium shoots respectively (Figure 4). Growth of S. maritima shoots in mature stands appears to be exceptionally slow, but no comparable measures on perennial, continuously growing grasses have been made (Tainton, personal communication). The slow growth rate and longevity of the shoots predicted by the graphs (Figure 4) may be comparable to the slow growth and longevity of 25-30 years of another grass, Nardus stricta (Perkins, 1968). Further evidence of the slow growth of S. maritima in the Swartkops Estuary was the absence of any regrowth in harvested plots one year after clipping, in spite of potential vegetative propogation from surrounding plants. This agrees with the findings of Gabriel & de la Cruz (1974) who found no difference between normal production and regrowth after repeated clipping. Hubbard (I 970) reports that regrowth and increased density of S. an&a shoots were stimulated by cutting. The slow growth rate of S. maritima is further shown by transplant experiments carried out by Lubke & Curtis (1977) on the banks of the Kowie Estuary, some IOO km NE. of the Swartkops River. The mean number of shoots produced 9 months after transplant varied with distance from the water’s edge from *2 shoots to a

Non-seasonal

production

of Spartina

247

maritima

m.

tar.

1257

1059

95e

Jay 1

711

lun. 3

10Q -

loll

Jul. 3

99i loec nug. 3

Sep. 3

1293

Oct. 3

NOV. 2-m

Size class intervals Figure 3. Community histograms. (a) Medium,

structure of S. (b) Tall.

(0-l dry g) maritima

expressed

as monthly

frequency

of 14. From the mean rate of increase in area of experimental clumps at r-m intervals, the authors estimated that complete cover by S. maritima would take about 6 years. S. alternzfiora transplants of I-m spacing along the east coast of North America took only two growing seasons to achieve complete cover (Godfrey & Godfrey, 1974; Seneca, 1974). Annual shoot production derived from growth rates was accordingly extremely low: 3.1 and 6.7 dry g m v-2 for Tall and Medium forms of S. maritima respectively.

maximum

S. M. Pierce

248

3c rZ0.97

II=81

2:

hhh /I ii

20

ii

I’

‘iii 3 E 1: .P I”

a

10

I trp 1

5

0

(a)

123456123456

(b)

Time (years) Figure growth Letters

4. Growth curves curve) and (b) denote individual

fitted to height increment data on (a) Tall (Von Bertalanffy Medium (Gompertz growth curve) S. maritima shoots. shoot measured.

Leaf production Mean leaf massesof different shoot size classesare presented in Table I. Number of leaves produced and lost by S. maritima both averaged 12 leaves shoot-r year -I. No seasonal trends in leaf production and loss were detected. Leaf production values have not been tabulated here asthese are equivalent to the production values from Method I (seeTable 3) where production = shoot and leaf production; and shoot production is negligible: &5 g m -s year -1. The number of leaves produced by S. muritima: (I 2 leavesshoot-l year -‘) is TABLE

I. Mean Shoot

Small Medium Large o Error

mass of S.

size class (dry d o-O.19

o’z-r.09 >I.10 within

I I 0/o of mean.

maritima leaves of different Mean (dry

leaf massa ms)

ro~zfo~8 31.7zt3.6 56.4+55

size-class

shoots

Non-seasonal production of Spartina maritima

249

much higher than for S. alterniflora (4.5 leavesshoot -l year -‘) and S. cynosuroides (g-5 leaves shoot -1 year -1) (Hardisky & Reimold, 1977)though I must assume,becauseof the omission of leaf massdata in the literature, and the reported large size of shoots,that leaf massof the latter two speciesis greater than that of S. maritima. S. patenscontinued to produce leaves even after culm elongation ceased(Hardisky & Reimold, 1977). However, this behaviour is shownby S. maritima throughout the year. Instantaneouslossrates Loss rates of S. maritima as litterbag lossesindicated strongly seasonaltrends (Figure 5). Linear regressionsof lossrates to water and air temperature showedsignificant correlation with Y = 0430,P
-26

X2’

1

I

I

,

I

I

I

I

I

I

I

1

JFMAMJJASOND Month Figure 5. Daily instantaneous rates of decomposition of S. maritima ( n) over successive periods of I month from litterbags with mean mesh diameter 0.8 mm’. Bars = z S.E. units where greater than the mean symbol, and n = 15. Water temperature (0) and air temperature (0) over the period are also depicted.

2.50

S. M. Pierce

Nutrient status The lack of any seasonal variation in the nutrient status of S. maritima shoots apparent in Table z may be explained by their continuous growth throughout the year. The N, C and organic content of dead material was consistently lower than in the live material. Almost all dead material sampled consisted of standing dead rather than litter. These results indicate the low nutritional value of shoots at death probably as a result of translocation of substances into the roots prior to death and before the enrichment by microbial fauna during decomposition. The annual mean N content of S. maritima of 1.30% N g-l dry massis approximately the sameasthe meanof S. alterniflora which had a high value of 2.01 y0 N g -l dry mass,dropping to 0.64% N g-l dry massby mid-growing season.Squires & Good (1974) explained these changesas a result of spring accumulation for later peak growth. However, Mendelssohn& Marcellus (1976) explain the summer decreasesimply as a result of a dilution effect of nutrients asthe plants increasein size. S. maritima, which lacks a marked growth season,is not subject to either of theseeffects and nutrients remain constant. Organic content of live material (Table 2) is compatible with values of S. altern$ora: 92.8% (Gabriel & de la Cruz, 1974) and 87.4% (Squires & Good, 1974). Potential energy values of live and dead material showed a slight increasein spring (Table 2) just before the onset of flowering. The suggestedrelationship is tenuous in view of the paucity of inflorescencesproduced. S. alternijlora energy values showedsomeseasonaldifferencesbut, when expressedas ash-freevalues, remained almost constant (Squires & Good, 1974). S. maritima mean energy value is 17 255 J g-l dry mass,which falls within the range of 15 204-20 008 J g-r dry massreported for S. altertzifora in North Carolina (Stroud & Cooper, 1969). Production Net aerial production of S. maritima, derived by all four methods of production measurement, is presented in Table 3. Methods 2, 3 and 4 are all dependent on a marked seasonal growth followed by a conspicuousdie-off. Production must be so great asto excedewithinsample variation. In S. maritima seasonalincreasesand decreasesin production are slight and maskedby stand variation, even though the percentageerror amongfive replicate samples was never greater than 16%. The erratic fluctuations of the monthly production values derived by methods 2, 3 and 4 suggestthese results are spurious products of the methods used. If the annual totals alone are viewed in Table 3, they appearto be reliable, when in fact they are asquestionable asthe monthly values from which they were summed. This shows the danger of using annual totals only, as has been done in other production studies on S. maritima in the Langebaan Lagoon, South Western Cape (Christie, 1976). The lower values derived by methods 2, 3 and 4 are probably the result of ignoring the high leaf turnover of the plant. Method 3 (Milner & Hughes, rg7o) yielded the lowest production values (Table 3) which is consistentwith the warning by Linthurst & Reimold (1978b) that changesinlive biomassof plants showing continuous growth, are too small for use as production measures.Also, this method ignoresmortality and leaf turnover, which is a major sourceof error here. Method 4 (Smalley, 1959) yielded higher production values than Method 3, as, although mortality is included, new shoot growth is ignored (Linthurst & Reimold, 19783). Method 2 (Wiegert & Evans, 1964) has been used widely, but Linthurst & Reimold (1978b) have expressedtheir reservations, mainly concerning the measurementof disappearanceof material. Tidal action as a source of error for dead material has been disputed earlier (see results of Biomass). Also the efficacy of litterbags asmeasuresof lossrates hasbeen shown (seeresults of Instantaneouslossrates).

Non-seasonal production of Spartina maritima

251

S. M. Pierce

252

TABLE Estuary

3. Net

aerial

production

(dry

N/D J

FM

AM

g rnw2)

of S. maritima

on the

Swartkops

Annual Method Tall I. This study 2. Wiegert & Evans 3. Milner & Hughes 4. Smalley (1959)

0

64 292

57

(1964)

0

48 99

64 99

72 79

(1970)

0 o

15.5

o 51

72 72

87 87

6

223

o

51

36

36

35

0105 0 31 0 59

0 0

0 o

33

J

J

+t

60

A

S

0

N/D

5s

SJ

65

68

0

0

0

0

I9

0

0

059

o

o

0

o

15

0

44 54 27

42 99 36

45 76 65

0

92 92

(1977)

680 668 412 559

Medium I. 2.

3. 4.

This study Wiegert 8z Evans Milner & Hughes Smalley (1959)

48 (1964) (1970)

0 0

20

46 96 22 44

080276765

46

0 o 017

47 49 6

47 0 0 0

523 479 187 379

Method I was devised in this study specially to account for the nature of S. maritima growth by measuringleaf and shoot production. Shoot production was negligible so that net aerial production is almost equivalent to leaf production. Flower production is minimal with some0*05-o-1 o/0of the shootsproducing inflorescences.Clearly, almostall energy is allocated into leaf rather than stem production, which is in contrast to energy partitioning in other Spartina species.S. maritima leaf production is almost 100% of the net aerial production. Calculation of leaf production of S. alternifIora in Georgia was possiblefrom the data of Odum & Fanning (1973) (i.e. no. leaf positions stern-l X mean leaf massX no. stemsm -“). Leaf production as a percentage of total production was 45% for Tall shootsand 28% for Medium S. alternifora shoots.The method of measuringproduction devised in this study is consideredthe most reliable method of all four methods asit accountsfor leaf turnover. Differences in growth strategies such as seasonaland continuous growth, different size shootsand densitiesmake comparisonsof production between speciesof Spartina in different environments difficult. S. alterni$ora often reachesa height of 150-200 cm in New Jersey (Squires & Good, 1974) while S. maritima hasa meanmaximum height of 60 cm. Production: biomassratios are a more valid form for comparison. However, the S. maritima P : B ratio =I*I, which is considerably lower than the P : B ratio of 4.6 for S. alternzjIora (Hopkinson et al. 1978). Even S. patens populations which show 25% continuous growth through the winter (Hardisky & Reimold, 1977) have a higher P : B ratio of 6.7 (Hopkinson et al., 1978). Though the genusSpartina hasa reputation for high productivity (Keefe, 1972), reports on S. maritima emphasize its lack of vigour in cool temperate climates (Mobberley, 1956; Marchant, 1967; Marchant & Goodman, 1969).This study showslow vigour in S. maritima even in a warm temperate climate. Acknowledgements The advice of ProfessorT. Erasmus, Dr C. Howard-Williams and Dr R. Lubke is acknowledged. Financial aid was provided by the Department of Water Affairs, Forestry and Environmental Conservation, and a CSIR post-graduate bursary. References Christie, N. D. 1976 Primary production in Langebaan Lagoon. Poster paper, Second National Oceanographic Symposium, University of Port Elizabeth. Die&man, B. S. 1978 Aspects of growth and production of Laminaria pallida (Grev.) J.Ag. off the Cape Peninsula. M.Sc. Thesis, University of Cape Town.

Non-seasonal

production

of Spartina

maritima

253

Eilers,

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