The effect of mortality on estimates of net above-ground production by spartina alterniflora

Aquatic Botany, 22 (1985) 121--132

121

Elsevier Science Publishers B.V., Amsterdam - - P r i n t e d in The Netherlands

THE E F F E C T OF MORTALITY ON ESTIMATES OF NET A B O V E - G R O U N D PRODUCTION BY SPARTINA ALTERNIFLORA

R.A. H O U G H T O N

The Ecosystems Center, Marine Biological Laboratory, Woods Hole, MA 02543 (U.S.A.) (Accepted 3 April 1985)

ABSTRACT Houghton, R.A., 1985. The effect of mortality on estimates o f net above-ground production by Spartina alterniflora. Aquat. Bot., 22: 121--132. Monthly changes in the live and dead biomass o f harvested Spartina alterniflora Lois. were compared with the growth and mortality of individual tillers on permanent plots to determine the extent to which estimates of net above-ground primary production (NAPP) based on harvest methods missed the turnover o f plant tissues. Enumeration of live tillers in the harvested samples revealed a 60% reduction in the number of live tillers between May and September. This loss of live biomass never appeared as a positive change in dead biomass during the growing season. Measurements of individual tillers showed that dying tillers had less mass than surviving tillers, and hence that the turnover of tiller biomass was less than the turnover of tiller numbers (15% of NAPP as opposed to 60%). Estimates of the turnover of biomass as a result of leaf mortality were also obt a i n e d from measurements of individual tillers. The mortality of tillers and o f leaves added about 20 and 12%, respectively, to NAPP calculated from the summation of positive changes in live biomass. Other c o m m o n l y used estimates of NAPP based on harvest data were 12 to 27% lower than the more direct estimate provided here based on documented mortality.

INTRODUCTION

Comparisons of different methods for estimation of net above-ground primary production (NAPP) by Spartina alterniflora Lois. have revealed: that the most rapidly obtained estimate, peak standing crop, can either over- or under-estimate NAPP depending on whether the turnover of plant material is less than or more than once per year; that methods involving monthly harvest and separation of live and dead biomass (e.g., SmaUey 1959; Milner and Hughes, 1968; Valiela et al., 1975) underestimate NAPP because they miss turnover of plant parts between sample times (Kirby and Gosselink, 1976; Linthurst and Reimold, 1978; Oallagher et al., 1980; Hopkinson et al., 1980); that methods that modify either the live (Lomnicki et al., 1968) or dead (Wiegert and Evans, 1964) component of field populations seem to account for the turnover of plant parts but, because they

0304-3770/85/$03.30

© 1985 Elsevier Science Publishers B.V.

122 m o d i f y the microenvironment, overestimate NAPP (Shew et al., 1981); and that methods based on detailed analysis of individual plants and plant parts are probably the most direct means for the determination of turnover (Williams and Murdoch, 1972; Hardisky and Reimold, 1977; Hardisky, 1980; Hopkinson et al., 1980; Reidenbaugh, 1983a, b). The general progression from assumptions to direct measurement of turnover in these 4 classes of methods is accompanied b y a requirement for increased effort or time. N o t surprisingly, an improvement in accuracy involves an increase in cost. This paper compares the results of several of these methods in an S. alterniflora marsh on Long Island, New York. The results suggest that modification of the relatively rapid harvest m e t h o d to include enumeration o f live tillers may increase the method's ability to measure turnover with little additional effort. The time-consuming task is determination of the average mass of dying tillers, and a readily obtained approximation for this mass is presented. STUDY AREA Flax Pond is a 57 ha tidal marsh on the southern shore of Long Island Sound about 75 km from N e w York City (40°55'N, 73°05'W). Freshwater input to the marsh is negligible (Woodwell et al., 1977); average salinity is a b o u t 26%o, the same as for Long Island Sound (Woodwell et al., 1977). The most recent opening, in a history of openings and closings b e t w e e n Flax Pond and Long Island Sound, was a b o u t 180 years ago (WoodweU and Pecan, 1973; Flessa et al., 1977). The relatively young age of the system is confirmed b y high rates of accretion on the marsh surface (Armentano and Woodwell, 1975) and b y the large area o f low marsh (below mean high water) dominated b y tall and intermediate Spartina alterniflora (> 120 cm; Houghton, 1979). The tall and intermediate stands cover a b o u t 75% o f the vegetated surface; short S. alterniflora. S. patens (Ait.) Muhl. and Distichlis spicat~ (L.) Green cover a b o u t 25%. Almost half o f the marshe m b a y m e n t system is n o t vegetated, b u t consists of salt ponds, channels and bare sediments. METHODS Ten sites were established in locations representative of S. alterniflora habitats in Flax Pond. Two o f the locations included populations o f short S. alterniflora (< 120 cm) at elevations close to mean high water, and 8 included populations of the tall or intermediate form. Above-ground biomass was harvested from 0.5 m 2 plots in each location m o n t h l y from J u l y 1972 through to N o v e m b e r 1973 and every second month from N o v e m b e r 1973 until S e p t e m b e r 1974. Tillers of S. alterniflora were clipped within 1.0 cm of the ground, separated into live (containing green tissue) and

123 dead categories, dried to a constant mass at 95°C, and weighed. Litter from the ground was included in the dead category. In 1973 and 1974, live tillers were counted. In addition to the ten 0.5-m 2 plots described above, smaller plots {0.03-0.09 m 2) were established at 6 o f the sites. All tillers (approx. 50) of S. alterniflora on these plots were identified through mapping and measured to the nearest centimetre in height each m o n t h from J u l y to November 1973, and from April to September 1974. A total of 688 tillers were tracked during the 2 growing seasons. Each m o n t h 20--30 tillers from a small plot adjacent to these plots were harvested, measured to the nearest centimetre, dried and weighed t o determine height--mass relationships for individual tillers. The number, position, mass and condition of leaves on these stems were also recorded. NAPP was calculated for each 0.5-m 2 plot by summing increments in live biomass (Milner and Hughes, 1968) and adding to these sums losses o f biomass from mortality of tillers and leaves. The loss of biomass from mortality of tillers was calculated each m o n t h as the product of the reduction in the n u m b e r of live tillers and the estimated mass o f individual tillers. The mass o f individual tillers was calculated from linear, log and log--log regressions o f tiller mass as a function of height; the regression producing the highest coefficient o.f variation (r 2) each m o n t h was chosen for t h a t m o n t h ' s calculations. No further testing of these regressions, such as Hardisky (1980) described, was performed. Because the mass of individual tillers suffering mortality is often less than the mass of an average tiller (Mathews and Westlake, 1969), data from the 6 small plots were used to estimate the average mass of dying tillers. That is, the heights o f tillers one m o n t h prior to mortality and the height--mass regressions provided estimates o f the mass o f individual, dying tillers. Three other estimates of the average mass o f dying tillers were compared with this more direct estimate to see if a substitute measurement might make the mapping of tillers unnecessary. One indirect estimate was based on the average mass o f all tillers during the interval between sampling. A second estimate was based on the average mass of all tillers at the start o f the interval. And a third estimate was based on the average mass o f the n smallest tillers at the start of the interval, where n was defined by t h e reduction in tillers during the interval. Losses of biomass as a result o f damage or senescence of leaves during the growing season were estimated from m o n t h l y records o f the n u m b e r o f missing, damaged, or dead (non-green) leaves and the mass of individual, intact leaves for tillers of size classes 1 . 0 - 2 . 9 g, 3 . 0 - 4 . 9 g ... 9 . 0 - 1 0 . 9 g. Leaf scars indicated where leaves were missing; usually some part o f a leaf remained. The differences between the mass of damaged or dead leaves on a tiller and the mass of intact green leaves for the same sized tiller was one estimate o f the loss o f leaf biomass per tiller. However, leaves damaged during the growing season were generally the oldest, lowest leaves on the

124 stem, and, live and intact, they were of lower mass t h a n leaves at intermediate heights. A more accurate estimate of the loss of biomass from leaf mortality was c o m p u t e d by subtracting the mass of a damaged or dead leaf from the average mass of intact leaves at the same position on tillers of the same size class. To calculate the loss per unit area o f marsh, the loss of biomass due to mortality of leaves was related m o n t h l y to the mass of tillers (i.e. to standing crop). RESULTS

The live above-ground biomass of S. alterniflora at Flax Pond followed the pattern typical of seasonal marshes (Figs. l(a) and 2(a)): a gradual accumulation during summer, a m a x i m u m in late August and September, and an abrupt reduction in late fall and winter to a m i n i m u m persisting through March. Dead biomass showed almost the converse of live (Figs. l(a) and 2(a)): a minimum in late summer and a m a x i m u m in late fall or early winter. The m a x i m u m a m o u n t of dead biomass was always less than the m a x i m u m a m o u n t of live biomass, an indication t h a t the tides removed plant material from the marsh surface (Houghton, 1979). The difference between maxim u m live and m a x i m u m dead biomass was greatest for the tall and intermediate stands, where exposure to tidally induced turbulence was greater. The increase in live biomass after May was due almost entirely to the growth of individual tillers (Figs 1(c) and 2(c)), because the .number of tillers declined in b o t h the tall and short stands (Figs. l(b) and 2(b)). In the tall stands the n u m b e r of tillers per m 2 declined from m a x i m a of 836 and 822 in May 1973 and 1974, respectively, to 286 and 296 by September. The number of tillers in short S. alterniflora plots declined from 1573 and 1309 to 630 and 559 in the two years. Samples with greater live biomass generally had fewer tillers. This was true for samples through the growing season at any one plot and for samples from different plots at any one time. The reduction in the number of live tillers was rarely balanced by an increase in dead tillers, indicating that tillers disappeared from the site. Observations of individual tillers on the mapped plots revealed that both live and dead tillers disappeared. Height--mass regressions varied from m o n t h to month. The largest variations were between the growing and non-growing seasons as Hardisky (1980) found. From m o n t h l y height--mass regressions, tillers a b o u t to die weighed, on average, 56% of the mean mass of tillers at the start of the interval. When sampling was every two months (i.e. 1974) the average mass of tillers dying over the sampling interval was 64% of the average tiller mass at the start of the interval. These percentages were used to calculate the loss of biomass as a result of tiller mortality in 1973 and 1974, respectively. Losses averaged 243 and 228 g m -2 for tall S. alterniflora in 1973 and 1974 and 168 and 99 g m -2 for the short form (Table I).

125

SPARTINA ALTERNIFLORA TALL AND INTERMEDIATE FORMS

1200 f

z FF<

E

..,.t"--...,t

8001 ............ ,,//

Onn~ m

I000

_

: ,,

3"

>

"'""-L

:

b

800 I CO E rY~ W

~

--JE

I--

m 12:

600'

:I Ou

cY I,I

-J _I

4.0

i--

u_

3.2

o

'r~ ',..9 i,i

2.4 c~

1.6 I.,IJ (,_9

<

n,-

0.8

S

I,I

> ,<

0.O I

l

i

I

JASONDJ 1972

l

I

I

I

I

I

FMAMJ

I I

I

l

I

I

I

I

J ASONDJ t 9"73

I

I

I

I

I

l

FMAMJ 19'74

I

I

I

I

JAS

Fig. 1. Mean and standard error of (a) live ( - - ) and dead ( ..... ) above-ground biomass, (b) density of tillers, and (c) mass of tillers of tall and intermediate forms of Spartina

alterniflora. T h e loss o f biomass as a r e s u l t o f leaf m o r t a l i t y was e s t i m a t e d t o be 1 4 6 a n d 143 g m -2 y r -1 for t h e tall stands a n d 8 9 a n d 55 g m -2 y r -1 f o r s h o r t S. alterniflora in 1 9 7 3 a n d 1 9 7 4 , r e s p e c t i v e l y (Table I). T h e s e estim a t e s were based o n variations in leaf mass as a f f e c t e d b y p o s i t i o n o n s t e m (i.e. age) a n d tiller size. N A P P in t h e tall a n d i n t e r m e d i a t e stands o f

126 SHORT

(:} z

FORM

o

D oo_

0o0~ n-<~ E

g "-

> __ o', orn v

800 400

m

0 2000

b

1600 u.)~E n- ... ILl h-

-

E

1200

800

c v

4O0

-C 1.6

¢¢ W _J FDo

'-'c~ (_9 o~

,L~ uJ

L~

1.4 1.2

0.8 0.6

,¢:I rr

"> ' <[

\\

1.0

0.4

0.2

/ /.+_.._.I

0.0

lllllIll I I I I I I I I l l l l l l I l l J JA SONDJ FMAM J JASOND J FMAMJ J AS 1972 1973 1974 Fig. 2. M e a n and standard error of (a) live (--) and dead (.....) above-ground biomass, (b) density of tillers,and (c) mass of tillersof short forms of Spartina alterniflora.

S. alterniflora w a s 1 6 5 1 and 1 5 4 2 g m -2 yr -1 in 1 9 7 3 and 1 9 7 4 , respectively. In t h e s h o r t stands N A P P w a s 1 0 1 3 and 6 4 6 g m -2 yr -1 during t h e s a m e t w o years (Table I). T h r e e m o r e readily o b t a i n e d , b u t less reliable e s t i m a t e s o f t h e b i o m a s s

127 TABLE I Components of above-ground net primary production in Spartina alterniflora stands in Flax Pond (g dry wt m -~ yr -1). The means and standard errors are based on eight and two plots of tall and short S. alterniflora, respectively

Sum of changes in live biomass Loss of tillers Loss of leaves Net primary production Total loss as % net production

Tall and intermediate S. alterniflora

Short S. alterniflora

1973

1974

1973

1262 +- 128 243 ± 49 146-+ 14

1171 ± 111 228-+ 53 143-+ 14

756 -+ 215 168-+ 60 89-+ 27

492 ± 136 99-+ 53 55± 22

1651 + 144

1542 ± 136

1013 ± 303

646 ± 211

23.5%

25.4%

24.1%

23.8%

1974

lost t h r o u g h tiller m o r t a l i t y are s h o w n in T a b l e II. E s t i m a t e s b a s e d o n t h e a v e r a g e m a s s o f all tillers o v e r e s t i m a t e d tiller m o r t a l i t y and, h e n c e , overestimated NAPP by 8--47%. The estimate based on the mass of the smallest tillers u n d e r e s t i m a t e d n e t p r o d u c t i o n b y 3--5%. L o s s o f b i o m a s s f r o m d a m a g e d o r s e n e s c e n t leaves, w h e n b a s e d o n t h e a v e r a g e mass o f all leaves o n a s t e m , was 29% higher t h a n t h e e s t i m a t e b a s e d o n t h e average m a s s o f leaves l o w e s t o n t h e s t e m ( T a b l e II). B e c a u s e consideration of leaf mortality increased the estimate of net production by a b o u t 9%, h o w e v e r ( T a b l e I), t h e e f f e c t o f using m e a n l e a f m a s s as o p p o s e d t o m e a n m a s s o f o l d e s t leaves o v e r e s t i m a t e d p r o d u c t i o n b y o n l y 2--3%. Loss o f b i o m a s s d u e t o l e a f d a m a g e a n d s e n e s c e n c e w a s e q u i v a l e n t t o 1 1 - 12% o f p e a k live b i o m a s s ; 38% o f t h e loss o c c u r r e d in J u l y a n d 62% in A u g u s t . L e a f loss w a s negligible b e f o r e J u l y a n d w a s n o t i n c l u d e d in N A P P f o r S e p t e m b e r b e c a u s e tillers s h o w e d n o significant g r o w t h a f t e r A u g u s t (Figs. l ( c ) , 2(c)). DISCUSSION M a n y e s t i m a t e s o f N A P P o f S. alterniflora h a v e i n c l u d e d t h e loss o f leaves (Williams a n d M u r d o c h , 1 9 6 9 ; O d u m a n d F a n n i n g , 1 9 7 3 ; H a t c h e r and M a n n , 1975). M e a s u r e m e n t s o f l e a f m o r t a l i t y in this s t u d y ( 1 1 - - 1 2 % o f p e a k live b i o m a s s ) w e r e less t h a n t h o s e r e p o r t e d in o t h e r s t u d i e s ( 1 5 - 27% o f p e a k live b i o m a s s ) . Use o f t h e average m a s s o f l o w e r , s m a l l e r leaves, r a t h e r t h a n o f all leaves, a c c o u n t e d f o r o n l y a p a r t o f t h e d i f f e r e n c e ( o n l y 2 - - 3 % o f N A P P ; T a b l e II), and s e e m s n o t t o j u s t i f y t h e a d d i t i o n a l e f f o r t r e q u i r e d t o d e t e r m i n e l e a f mass as a f u n c t i o n o f p o s i t i o n o n tiller.

128

+

+,t.. +.t..~

¢'4¢q

t-I ,,,-I

0"0

4-1 +1 ,,-I

+1 +1 LO ~,--I z.~ L'-

+1 +l ~ oO

0

+

~

+1

+i

+ v

r,.D +1 O0

+1 +1 ,0~ 1.0 oo ,..-I

+1

i...4

o"rJ

~.~ ,--,~

C, I O LI"J I,-.I

E

+l

I:l

~

+

-4-

.

+1

~ ¢"J O0 +1

1--4 "--I +1

+1

+1

r~ i,-I

-I•,# t'... I...4

¢b 0'~ I=I

~

,,-I +1

+1

+1

+1

t"... oO I~l oo " ~ ,,-.I

0

",~ O0 I,.-I 1...4

o~

1""4 ,.0

[.-,

e .! ,.,@

o~ ,.q

129

In contrast to measurements o f leaf mortality, only t w o studies o f S.

alterniflora have estimated tiller mortality directly (Hardisky, 1980; Reidenbaugh, 1983a, b) although estimates have been made in other ecosystems (e.g., Mathews and Westlake, 1969; Bernard and Fitz, 1979; Carpenter, 1980). The m e t h o d described here is equivalent to the removal-summation m e t h o d described b y Gillespie and Benke {1979) as one of several cohort m e t h o d s used frequently for animal populations. In Flax Pond the loss o f biomass through tiller mortality was a b o u t twice as high as the loss through leaf mortality and represented a b o u t 15% of above-ground production (Table I). Tiller mortality would have been grossly overestimated had the average mass o f all tillers been used to approximate the mass of dying tillers. In b o t h growing seasons and in both heights of S. alterniflora, mortality affected a b o u t 60% of the tillers, b u t only a b o u t 15% of the biomass of NAPP. The mortality o f tillers and leaves together accounted for 23--25% of net production in this study (Table I). In a Virginia marsh the combined mortality accounted for between 16 and 35% of production (Reidenbaugh, 1983a, b). Hardisky (1980) found in a Georgia marsh that NAPP estimated from tagging individual tillers was less than NAPP estimated from changes in live and dead standing crop (Smalley's method). This result is the reverse of what was found in Flax Pond (this study) and in Virginia (Reidenbaugh, 1983a, b). One difference between the methods used here and b y Hardisky (1980) was the n u m b e r of height--mass regressions used to calculate NAPP. A separate equation was calculated for each m o n t h in this study. Hardisky used one equation for the entire year and noted its p o o r fit for N o v e m b e r April. Another explanation might be the loss of tags. If b o t h live and dead tillers disappeared from the Georgia marsh as t h e y did at Flax Pond, and if Hardisky counted only retrieved tags, his m e t h o d would have underestimated the loss o f tillers. Hardisky's argument that the close agreement b e t w e e n numerical and biomass turnover supported his m e t h o d is n o t valid in Flax Pond where the turnover of tillers was 60% and the turnover of biomass was 15% of NAPP. Numerous other methods have been e m p l o y e d to estimate NAPP by marsh plants. A comparison of four of these methods with the one described here shows that methods based on peak live biomass, on changes in live biomass (Milner and Hughes, 1968), and on changes in live and dead biomass (Smalley, 1959; Valiela et al., 1975) underestimated NAPP by 15--27% (Fig. 3). Figure 1 shows w h y these methods underestimated production at Flax Pond. During the months that live biomass increased, the number of tillers decreased; y e t the loss in live biomass never appeared as a positive change in dead biomass until the end of the season. During the growing season many of the dead tillers were apparently removed from the marsh surface. Figure 3 shows that NAPP based on the sum of positive changes in live

130

biomass (Milner and Hughes, 1968) was larger if based on 12 m o n t h s (Column 3) than if based on the growing season only (Column 2). The latter m e t h o d was used as part of the calculations for Column 6 and Table I. The larger value is closer to the best estimate of NAPP, but the "improvement" is more the result of sample variability than o f accuracy. The higher estimate results from the fact that only positive changes in live biomass are included in the sum. If there were no growth, random fluctuations in biomass due to spatial variation would result in a positive NAPP. Evidence o f the same effect can be seen from a comparison o f the mean NAPP c o m p u t e d from individual calculations of NAPP (8 plots) with NAPP calculated from mean changes in biomass on 8 plots. The columns marked 2* and 5* in Fig. 3 show the latter. When means are used in calculations of NAPP, sampling variation is reduced and NAPP is not inflated by counting only positive fluctuations. The advantage of the method described here is that it accounts for mortality directly. In this study, the mass o f tillers prior to death was calculated from regressions derived from periodically mapped and measured tillers. 1600 Z 0 )-

1400 o 0 OE

n

>n'-

1200 A oJ

'E OE O.

•

o

~

Z

"~

o "" L9 ~ u.I > 0 ao

I000

800

600

400

I-U.I

z

200

0 TALL 1973

TALL 1974

SHORT 1973

SHORT 1974

Fig. 3. Net above-ground primary production by tall and short Spartina alterniflora as estimated by several methods: (1) maximum live standing crop; (2) positive changes in live biomass during the 6-month growing season (April--September; Milner and Hughes, 1968); (3) positive changes in live biomass over 12 months (Milner and Hughes, 1968); (4) changes in live and dead biomass (Smalley, 1959); (5) changes in live and dead biomass (Valiela et al., 1975); (6) positive changes in live biornass plus mortality of tillers and leaves (this study). Asterisks indicate that mean changes in biomass from sampled plots were used to calculate NAPP; the values without asterisks are means of NAPP calculated separately for each plot.

131

In Reidenbaugh's analysis the harvested tillers were divided into 20-cm height classes each with an average mass. Each of these m e t h o d s added considerably to th e e f f o r t o f the harvest technique. If a rapid estimate of t h e mass o f dying tillers could be f ound, t he onl y additional e f f o r t required b y t h e m e t h o d used here is t he counting o f harvested tillers. T h e observat i on t h a t th e mass o f the smallest tillers u n d e r e s t i m a t e d NAPP by o n l y 3--5% (Table II), suggests an a p p r o x i m a t i o n t h a t does n o t require measurements o f individual tillers. I f harvested samples were dried and weighed and th en stored until t he n e x t m o n t h ' s sample revealed the n u m b e r o f tillers lost, t h a t n u m b e r o f the smallest tillers could be selected f r o m t h e stored sample and weighed. T h e mass would be a close a p p r o x i m a t i o n t o tiller m o r t a l i t y during t h a t m o n t h . Such an a p p r o x i m a t i o n would have t o be validated f o r a n o t h e r marsh. T he advantage o f such an a p p r o x i m a t i o n is t h a t it would increase the reliability o f harvest m e t h o d s w i t h o u t m u c h additional e f f o r t -- only the e n u m e r a t i o n o f live stems. T h e advantage of t h e m e t h o d , with or w i t h o u t approximations, is t h a t the loss o f plant material within sampling intervals can be obtained directly. ACKNOWLEDGMENTS Research carried o u t in part at B r o o k h a v e n National L a b o r a t o r y with financial s u p p o r t to G.M. Woodwell f r o m t he Energy Research and Developm e n t Administration and the National Science F o u n d a t i o n (Grant No. AG-375), and in part at t he Ecosystems Center, Marine Biological Laborat o r y , Woods Hole, Massachusetts, with s u p p o r t f r o m the Rockefeller Foundation.

REFERENCES Armentano, T.V. and Woodwell, G.M., 1975. Sedimentation rates in a Long Island marsh d e t e r m i n e d b y ~~°Pb dating. L i m n o l . Oc eanogr., 20: 4 5 2 - - 4 5 6 . Bernard, J.M. and Fitz, M.L., 1979. Seasonal changes in above-ground primary production and nutrient contents in a central New York Typha glauca ecosystem. Bull. Torrey Bot. Club, 106 : 37--40. Carpenter, S.R., 1980. Estimating net shoot production by a hierarchical cohort method of herbaceous plants subject to high mortality. Am. Midl. Nat., 104: 163--175. Flessa, K.W., Constantine, K.J. and Cushman, M.K., 1977. Sedimentation rates in a coastal marsh determined from historical records. Chesapeake Sci., 18: 172--176. Gallagher, J.L., Reimold, R.J., Linthurst, R.A. and Pfeiffer, W.J., 1980. Aerial production, mortality, and mineral accumulatiow-export dynamics in Spartina alterniflora and Juncus roemerianus plant stands in a Georgia salt marsh. Ecology, 61: 303--312. Gillespie, D.M. and Benke, A.C., 1979. Methods of calculating cohort production from field d a t a - some relationships. Limnol. Oceanogr., 24: 171--176. Hardisky, M.A., 1980. A comparison of Spartina alterniflora primary production estimated by destructive and nondestructive techniques. In: V. Kennedy (Editor), Estuarine Perspectives. Academic Press, New York, pp. 223--234.

132 Hardisky, M.A. and Reimold, R.J., 1977. Salt marsh plant geratology. Science, 198: 612---614. Hatcher, B.G. and Mann, K.H., 1975. Above-ground production of marsh cord-grass (Spartina alterniflora) near the northern end of its range. J. Fish. Res. Bd. Can., 32: 83--87. Hopkinson, C.S., Gosselink, J.G. and Parrondo, R.T., 1980. Production o f coastal Louisiana marsh plants calculated from phenometric techniques. Ecology, 61: 1091--1098. Houghton, R.A., 1979. The role of vascular plants in the carbon exchanges of a salt marsh. Ph.D. Dissertation, State University of New York at Stony Brook, New York, 155 pp. Kirby, C.J. and Gosselink, J.G., 1976. Primary production in a Louisiana Gulf Coast Spartina alterniflora marsh. Ecology, 57: 1052--1059. Linthurst, R.A. and Reimold, R.J., 1978. An evaluation of methods for estimating the net aerial primary productivity of estuarine angiosperms. J. Appl. Ecol., 15: 919--931. Lomnicki, A., Bandola, E. and Jankowska, K., 1968. Modification of the Wiegert-Evans method for estimation o f net primary production. Ecology, 49: 147--149. Mathews, C.P. and Westlake, D.F., 1969. Estimation of production by populations of higher plants subject to high mortality. Oikos, 20: 156--160. Milner, C. and Hughes, R.E., 1968. Methods for the Measurement of the Primary Production of Grasslands. IBP Handbook No. 6. Blackwell, Oxford, 70 pp. Odum, E.P. and Fanning, M.E., 1973. Comparison of the productivity of Spartina alterniflora and Spartina cynosuroides in Georgia coastal marshes. Bull. Ga. Acad. Sci., 31 : 1--12. Reidenbaugh, T.G., 1983a. Productivity of cordgrass, Spartina alterniflora, estimated from live standing crops, mortality, and leaf shedding in a Virginia salt marsh. Estuaries, 6: 57--65. Reidenbaugh, T.G., 1983b. Tillering and mortality of the salt marsh cord-grass, Spartina alterniflora. Am. J. Bot., 70: 47--52. Shew, D.M., Linthurst, R.A. and Seneca, E.D., 1981. Comparison of production computation methods in a southeastern North Carolina Spartina alterniflora salt marsh. Estuaries, 4 : 97--109. Smalley, A.E., 1959. The role o f two invertebrate populations, Littorina irrorata and Orchelirnum fidicinium, in the energy flow of a salt marsh ecosystem. Ph.D. Dissertation, University of Georgia, Athens, 126 pp. Valiela, I., Teal, J.M. and Sass, W.J., 1975. Production and dynamics of salt marsh vegetation and the effects of experimental treatment with sewage sludge. J. Appl. Ecol., 12: 973--981. Wiegert, R.G. and Evans, F.C., 1964. Primary production and the disappearance of dead vegetation on an old field in southeastern Michigan. Ecology, 45 : 49--63. Williams, R.B. and Murdoch, M.B., 1969. The potential importance of Spartina alterniflora in conveying zinc, manganese, and iron into estuarine food chains. In D.H. Nelson and F.C. Evans (Editors), Proceedings of the Second National Symposium on Radioecology, CONF-670503, USAEC, (TID-4500). USAEC, Washington, DC, pp. 431-439. Williams, R.B. and Murdoch, M.B., 1972. Compartmental analysis of the production of Juncus roemerianus in a North Carolina marsh. Chesapeake Sci., 13 : 69--79. WoodweU, G,M. and Pecan, E.V., 1973. Flax Pond: an Estuarine Marsh. BNL/50397, Brookhaven National Laboratory, Upton, N e w York, 7 pp. Woodwell, G.M., Hall, C.A.S., Whitney, D.E. and Houghton, R.A., 1977. The Flax Pond ecosystem study: exchanges of carbon in water between a salt marsh and Long Island Sound. Limnol. Oceanogr., 22: 833--838.