Aquatic Botany, 5 (1978) 355

(1)

Aquatic Botany, 5 (1978) 355--364 355

THE RELATIONSHIP BETWEEN ABOVEGROUND AND BELOWGROUND BIOMASS OF FRESHWATER TIDAL WETLAND MACROPHYTES

D.F. WHIGHAM

Chesapeake Bay Center for Environmental Studies, Smithsonian Institution, Route 4, Box 622, Edgewater, MD 21037 (U.S.A.)

R.L. SIMPSON

Biology Department, Rider College, Lawrenceville, NJ 08648 (U.S.A.) (Received 13 February 1978)

A B S T R A C T

Whigham, D.F. and Simpson, R.L., 1978. The relationship between aboveground and belowground biomass of freshwater tidal wetland macrophytes. Aquat. Bot., 5: 355--364.

Aboveground and belowground biomass relationships of 15 annual and perennial freshwater tidal wetland macrophytes were examined. T h e data showed that regression equations m a y be used with confidence to estimate belowground biomass from aboveground biomass for most species. The linear regression model was suitable except for one species which had a large belowground c o m p o n e n t and for which the exponential model was more appropriate. Belowground:aboveground biomass ratios were significantly different for the 8 annual species examined. At peak biomass, all annuals allocated less than one third of the total net annual production into belowground structures. They exhibited distinct seasonal patterns of biomass allocation with more biomass incorporated into belowground components during the early part of the growing season. Perennial species exhibited 4 patterns of biomass allocation with Peltandra virginiea (L.) Kunth having a significantly greater m e a n belowground:

aboveground biomass ratio than other perennials. Factors that m a y control biomass allocation patterns include depth of rooting and life history strategies.

INTRODUCTION

Estimates of biomass and primary production of emergent herbaceous macrophytes in freshwater wetlands rarely include data on belowground ma- terials (Bernard, 1974; Bernard and Bernard, 1973; Bernard and Gotham, 1978;

Boyd, 1969, 1970, 1971) even though subterranean components may account for a large percentage of the total biomass and annual net primary production (Bernard and Gorham, 1978; Jervis, 1969; Likens, 1976). There have been even fewer studies of the partitioning of net primary production between aboveground and belowground components of freshwater tidal wetland macrophytes (Good and Good, 1975; McCormick, 1970; McCormick and Ashbaugh, 1972;

Whigham and Simpson, 1977). In a recent review of biomass and primary pro-

(2)

duction of freshwater tidal wetlands (Whigham et al., 1978), it was shown that most investigators have underestimated biomass and net production because, in part, they did not estimate belowground production.

Freshwater tidal wetlands are highly diverse and include species that range from typical emergent herbaceous perennial macrophytes (Pontederia cordata L., Peltandra viriginica (L.) Kunth, Nuphar advena (Ait.) Ait. f. Thypha sp., Sparganium sp. and Scirpus sp.) to a number of annuals of which Zizania aquatica var. aquatica L., Bidens sp. and several species of Polygonum are commonly dominant. Most of those species are taxonomically unrelated and, while much is known about convergence of leaf shape, heterophylly and types of belowground structures, primarily rhizomes and turions

(Hutchinson, 1975), there is little information on how they allocate their resources.

Considering the unifying effect of natural selection, one might expect, however, that there would be convergence of biomass allocation patterns between species that occur in wetland environments where environmental selection pressures would appear to be similar. In this situation, environmental similarity might exist within the substrate where, at most, only the first few centimeters of substrate are aerobic. In this paper, we test that hypothesis by considering the relationships between belowground and aboveground components of 15 annual and perennial species that are widely distributed in freshwater tidal wetlands. Additionally, we consider the value of regression equations in esti- mating belowground biomass from aboveground biomass data. Nomenclature follows Gleason and Cronquist (1963) with the exception of Acnida cannabi- nus (L.) J.D. Sauer which follows Radford et al. (1968) and Zizania aquatica var. aquatica L. which follows Dore (1969).

METHODS

Plants were collected from five sites in the Hamilton Marshes, a Delaware River freshwater tidal wetland near Trenton, New Jersey, and previously de- scribed by Whigham and Simpson (1976). Perennials were harvested in 1975, 1976 and/or 1977 when aboveground and belowground biomass of each species was near peak standing crop. Entire plants of annuals and non-rhizome- forming perennials [Peltandra virginica, Pontederia cordata, Sagittaria latifolia Willd. and Scirpus fluviatilis (Tort.) Gray] were individually hand extracted while rhizome-forming perennials (Acorus calamus L., Nuphar advena, Spargan- ium americanum Nutt. and Typha latifolia L.) were extracted using 0.25 m 2 quadrats. The quadrats almost always enclosed entire clumps of the rhizome- forming species, but there were occasions when the samples underestimated belowground biomass because rhizomes extended beyond the quadrat boun- dary. Annuals were sampled on 4 dates in 1975 chosen to represent the following growth phases: (1) seedling, (2) shoot growth initiation following seedling establishment, (3) period of maximum net production and (4) mature plants. All samples were washed several times in the field and laboratory and then separated into aboveground (including stems, leaves and reproductive

(3)

357 structures) and belowground components. The samples were dried at 105 ° C and weighed. Data for each species were subjected to regression analysis using both linear ( Y = a + bX) and exponential ( Y = ae bx) models ( where Y was the belowground biomass and X was the aboveground biomass) for the purpose of developing a series of regression equations to estimate belowground standing stock f r o m aboveground biomass.

RESULTS

Linear regressions provided the best fit for all species except Peltandra vir- ginica where the exponential model produced a larger correlation coefficient.

Regression equations for all perennials except Sparganium americanum were significant at the ~ = 0.01 level and, except for Polygonum sagittatum L., were generally significant at the ~ = 0.05 level or higher for the annuals (Figs.1 and 2).

The perennials exhibited 4 distinct biomass allocation patterns (Fig.l). The percentages of belowground biomass of Acorus calamus and Typha latifolia only varied slightly across t h e range of clone sizes sampled. Belowground biomass a c c o u n t e d for approximately 53% of the total biomass of Acorus and 36%

for Typha. For Pontederia cordata, the percentages of belowground biomass increased as the aboveground biomass c o m p o n e n t increased. Small plants (aboveground biomass of 15 g) had 40% of the total biomass allocated into belowground structures while large individuals (aboveground biomass of approximately 50"g) allocated nearly 50% of their resources into belowground structures. The opposite allocation pattern was f o u n d for Nuphar advena, Sagittaria latifolia, Scirpus fluviatilis and Sparganium americanum where individuals with smaller shoots allocated larger percentages of their biomass into belowground c o m p o n e n t s than did individuals with larger shoots. Peltandra virginica displayed a fourth allocation pattern. Both small and large individuals (aboveground biomass of 10 g and 100 g, respectively) allocated approximately 90% of their total biomass to underground structures while individuals with intermediate sized shoots (approximately 50 g) had less biomass (84%) in their belowground structures.

Belowground:aboveground biomass ratios (R:S) were calculated for each species (Table I). There were significant (~ = 0.01) differences between species and species comparisons made using Newman Keuls Tests (Sokal and Rohlf, 1969) showed that Peltandra virginica was the only species with an R:S signifi- catnly greater than all other species. The R:S of Scirpus fluviatilis was significantly less than that of Peltandra virginica but significantly greater than the values of the other species. The R: S of Sparganium americanum was significantly greater than that of Typha latifolia and Sagittaria latifolia but n o t significantly different f r o m the values of Nuphar advena, Acorus calamus and Pontederia cordata.

Most of t h e n e t production of the annual species was allocated to shoot production and only during the seedling phenophase were relatively large per-

(4)

,00 TYPHA -IOO 50- ACORU$ -1oo Y= 1.24 + .5272X /Y=I.3"I" ,.0489X ~/1 80 R Z = . , , , 0 4 0 ~ : Z = . ~ O . / I 8 0

6 0 . 6 0 30 liii~:Tr ... . , ~ _ . . . J - 6 0

============================================================================= 4 o ZO ] / i 4 o

20- 2o IO 20

,

2 ' o , o ,oo ,o 20 30 ;o

$ C I R P U $ $ P A R G A N I U M (SO

50" ~ Y=II.9 + 1.1082X F I00 50- Y=II.6 + 5406 X I00 O0

,,o. / 8 o ' " 2 : . ' 9 . o

!i!i ili~iii!?:!i] il !!!'~2. ~ : : : : : : : : : .

:::::::::::::::::::::::::: ~:. il 60 3o-liiiii:iii::~ 6o m

00 i i:::,::!iiiiill iiii::::i~i:: ::~ ~ i : : :~!il

CO 2 0 - , . ~ " / f 4 0 20- 40 t~

I0- . ' ' . • 20 I0' "" 20 Z)

0 : , 0

- - , , , ~ r Y

CD 4 8 12 16 20 'lO 210 310 40 50 (_9

>

a ~ 5 - $AGITTARIA , - - NUPHAR I00 0

. ~ i-,,~,, ioo- Y= I o . 4 + .5531 x -

Z Y: 1.3-1" .7559 X

2 0 ~,l R2=.39 • F eo 80-I, R 2 = . 5 5 80 13DILl

60 60- ...

(D i ~ : : - r :~iiii::i::~ ============================================= I'-

" IO] ~ ' ~ ' S ? ~ 40 40- ~ = ~ . ~ 40 Z

0 t.U

.__1 51 ~ . . .. F20 2 0 - 20 (-) n-"

IJ.J L . . . / ~ / bJ

i i i f

m 4 • ,;' ,e zo z'o 4'o ~'o o'o ,oo o_

I00- PONTEOERIA .100 I000~,,.. PELTANDRA ~ 1 0 0

Y = - 4 . 8 4 I. 0 2 2 8 } f ~ . . . ~l . : ~

80 R Z : . 94 / • 80 800 ::::iii::i::ii~;- 024 $ X :: 80 Iiy= 77.7 e ~ i I

20- 20 2 0 0 ~ , , 20

I 0 1 i i

2 40 60 80 I00 20 4 0 ~60,,80 I00

A B O V E G R O U N D F I I O M A S S ( G )

X

Fig. 1. A b o v e g r o u n d a n d b e l o w g r o u n d b i o m a s s r e l a t i o n s h i p s o f 8 p e r e n n i a l f r e s h w a t e r t i d a l w e t l a n d m a c r o p h y t e s . W i t h t h e e x c e p t i o n o f Sparganium, all r e g r e s s i o n e q u a t i o n s a r e signi- f i c a n t a t t h e a = 0 . 0 1 level. S h a d e d p o r t i o n s r e p r e s e n t t h e d i f f e r e n c e b e t w e e n t h e o b s e r v e d a l l o c a t i o n o f b e l o w g r o u n d b i o m a s s a n d a 5 0 % a l l o c a t i o n p a t t e r n . R e f e r t o T a b l e I f o r a l i s t i n g o f s p e c i e s n a m e s .

(5)

359

I0 ACNIDA I0 ZIZANIA

1 :l

8 .1I

Y 6 Y I // ~ ~ I~

4 ~.'rJ~z

2 4 6 8 I0 2 4 6 8 I0

i P. S A G I T T A T U M I0 P. A R I F O L I U M

~ 8

~ 6 z

< 2 -~2;'2":~

, , ,

rn 2 4 6 8 I0 2 4 6 8 I0

rm

zlO] IMPATIENS/ IO 7 BIDENS

° / . ; , 64

/ lit

~ 4 J J ~ Y 4 4 / ' I ~

m / . . . . " 2

1 i ,

2 4 6 8 I0 2 4 6 8 I0

IO-,R P U N C T A T U M X

81 / T l r ACNIbA ZIZANIA

~ / j . / ' - - Z Y=.O02 +.238X** Y =-.,9+ 9 0 9 X - T**

• Y = - . I O + . 7 7 8 X * Y= 5 1 + . 3 4 4 X - m *

t / : P / Y . , + , .

Y 4 Y = .13 + .I 58X** Y = - 2 . 0 7 + . 6 4 3 X - T ~ " * *

2J S ~ _~.~-~

~ : ~ ~ ' - - - t, ]'~r P SAGITTATUM P A R I F O L I U M

2 4 6 8 IO Y : .01 + . 1 6 2 X Y = - I O + 5 6 7 X - : X * * ABOVEGROUND Y = o 4 + 0 9 I x Y = 0 2 + 2 8 4 x - n * *

Y= .08 + 040X Y : 06+ 3 5 9 x - T i T * *

BIOMASS (G) Y : . I B t .129x-'I'~"

X

I M P A T I E N S B I D E N S P. P U N C T A T U M

Y = - 0 3 - ' t - 5 3 6 X** Y = . 0 3 + . 5 0 9 X * * Y= 0 0 1 + 5 1 4 X - I * * Y = - . 3 I - I - . 7 4 9 X** Y ' ' . 3 9 - P I 8 0 9 X * * Y = , I 6 " + " 1 7 3 x - ' r ' [ * * Y= i 2 0 - 1 - . 4 1 2 X** Y = - . 8 8 4 - 7 7 9 X * * Y = - . 3 3 + 7 8 0 X -Trr**

Y : . 3 5 + . 3 0 4 X'" Y = - . 8 5 - t - . 5 • 7 X * * Y = . 8 2 + I 0 5 X - 1 V

Fig. 2. A b o v e g r o u n d a n d b e l o w g r o u n d b i o m a s s r e l a t i o n s h i p s o f 7 f r e s h w a t e r tidal w e t l a n d annuals. R e g r e s s i o n e q u a t i o n s are f o r t h e f o l l o w i n g 1 9 7 5 s a m p l i n g d a t e s : I = J u n e 7; II = J u n e 21; I I I = J u l y 3; IV = A u g u s t 18. T h e u n m a r k e d line o n e a c h g r a p h r e p r e s e n t s a 1:1 d i s t r i b u t i o n o f b e l o w g r o u n d t o a b o v e g r o u n d b i o m a s s . S i g n i f i c a n c e levels are d e s i g n a t e d at

= 0.05 ( * ) a n d a = 0.01 ( * * ) , r e s p e c t i v e l y . R e f e r t o T a b l e I f o r a listing o f s p e c i e s names.

(6)

TABLE I

Belowground:aboveground biomass ratios at peak standing crop for annual and perennial species

Species Mean -+ 1 S.E. Maximum Minimum Sample

size Perennials

Acorus calamus 1.11 _+ 0.36 2.13 0.63 17

Nupharadvena 0.86 + 0.28 1.39 0.48 10

Peltandra virginica 8.42 ± 5.05 21.37 2.79 13

Pontederia cordata 1.30 ± 1.14 3.86 0.54 7

Sagittaria latifolia 0.94 ± 0.38 1.91 0.42 25

Scirpus fluviatilis 3.64 _+ 1.92 9.33 1.28 20

Sparganium americanum 1.92 + 1.01 4.23 0.64 16

Typha latifolia 0.55 ± 0.17 0.91 0.42 10

Annuals

Acnida cannabinus 0.24 ± 0.07 0.39 0.18 10

Bidens laevis 0.41 _+ 0.17 0.78 0.17 15

Impatiens capensis 0.37 ± 0.17 0.79 0.10 20

Polygonum arifoliuTn 0.15 -+ 0.14 0.50 0.03 15

Polygonum punctatum 0.46 ± 0.31 0.90 0.15 10

Polygonum sagittatum* 0.14 ± 0.11 0.40 0.04 10

Zizania aquatica var. aquatica 0.41 ± 0.19 0.66 0.20 10

*Data from 3 July were used for this species.

c e n t a g e s o f t h e t o t a l b i o m a s s f o u n d in t h e r o o t c o m p o n e n t s . T h e p e r c e n t a g e s o f r o o t s y s t e m b i o m a s s o f P o l y g o n u m sagittatum, P o l y g o n u m arifolium L.

and Zizania aquatica vat. aquatica d e c r e a s e d c o n t i n u a l l y t h r o u g h o u t t h e s a m p l i n g p e r i o d . W h i g h a m a n d S i m p s o n ( 1 9 7 7 ) h a v e r e p o r t e d s i m i l a r results f r o m a n o t h e r s t u d y o f Zizania. T h e p e r c e n t a g e s o f r o o t b i o m a s s o f Acnida cannabinus, Bidens laevis (L.) BSP. a n d Impatiens capensis Meerb. i n c r e a s e d a f t e r t h e seedling p h e n o p h a s e a n d t h e n d e c l i n e d t o m i n i m u m values in A u g u s t . Initial d e c r e a s e s in t h e p e r c e n t a g e o f b i o m a s s o f t h e r o o t c o m p o n e n t s o f Poly- g o n u m p u n c t a t u m Ell. w e r e f o l l o w e d b y increases in J u l y a n d d e c r e a s e s in

August. A t p e a k a b o v e g r o u n d s t a n d i n g c r o p , R: S r a t i o s f o r t h e a n n u a l s aver- a g e d less t h a n 0.5 ( T a b l e I) a n d t h e r e w e r e s i g n i f i c a n t d i f f e r e n c e s (~ = 0.01) b e t w e e n species, A l t h o u g h P o l y g o n u m arifolium a n d P. sagittatum h a d s m a l l e r r a t i o s t h a n t h e o t h e r species, f u r t h e r t e s t i n g failed t o s h o w w h i c h m e a n s w e r e s i g n i f i c a n t l y d i f f e r e n t .

DISCUSSION

O u r initial p r e d i c t i o n was t h a t s p e c i e s f o u n d in s i m i l a r h a b i t a t s s h o u l d h a v e similar p a t t e r n s o f b i o m a s s a l l o c a t i o n b e c a u s e o f t h e s i m i l a r i t y in e n v i r o n m e n - tal s e l e c t i o n p r e s s u r e s . While a t p e a k b i o m a s s t h e a n n u a l s p e c i e s did h a v e sig- n i f i c a n t l y d i f f e r e n t R: S r a t i o s , a clear c o n v e r g e n c e is a p p a r e n t b e c a u s e t h e

(7)

361 R: S ratios were always less than 0.5. The annuals exhibited seasonal patterns of biomass allocation {Fig.2) and the patterns may be related to several factors.

Survival strategy may be an important factor for most species allocated more biomass t o r o o t structures during the seedling establishment phenophase when individuals were competing for rooting space. Following establishment, the plants entered a phase of rapid shoot growth and then began to allocate most of their net biomass into that c o m p o n e n t . This p h e n o m e n o n has been verified by the work of McCormick (1970), McCormick and Ashbaugh {1972) and G o o d and G o o d (1975) who have shown that annuals have very high rates of s h o o t height growth following seedling establishment. Reproductive strategy is a second factor that contributes to the biomass allocation patterns of the annuals. Annuals are almost all r strategists which, according to Harper and White (1974), are species that allocate most of their net primary p r o d u c t i o n in- to s h o o t growth that, in turn, supports high levels of seed production. Whig- ham and Simpson (1977), for example, concluded that wild rice had to be an r strategist because of very high seed mortality. Thirdly, substrate conditions may be an abiotic factor that is, in part, responsible for the allocation patterns exhibited b y the annuals. Only the upper few centimeters of substrate are aerobic for e x t e n d e d periods (Simpson et al., 1978) and any species that roots below that zone must be able to withstand anaerobic conditions. Wild rice is the only annual species studied that tolerates anaerobic conditions and is also the only annual that has an extensive aerenchyma tissue which is usually associated with the ability to withstand anaerobic conditions (Hutchinson, 1975).

The annuals which lack extensive aerenchyma are thus restricted to a very shallow rooting zone. In the Hamilton Marshes, almost all annual roots are concentrated very near to the surface (Whigham et al., 1978). Because the annuals have their roots in the aerobic zone, t h e y are able to produce more stem and leaf biomass per unit of r o o t biomass (Shaver and Billings, 1975).

The perennials also exhibited distinct biomass allocation patterns (Fig.l) but, with the exception of Peltandra virginica and Scirpus fluviatilis, t h e y all had rather similar R:S ratios (Table I). R:S values for Acorus calamus were similar to those reported by Dykyjov~ et al. (1972). However, our Typha R:S values were lower than those reported by B o y d (1971), Jervis (1969) and McNaughton (1974). They f o u n d that Typha roots and rhizomes represented a b o u t 50% of the total biomass in non-tidal wetlands. Our estimate may be low because our sampling technique, based on an area sampling rather than extraction of entire clumps, did n o t always account for all of the belowground material.

The significant difference b e t w e e n the R:S of Peltandra virginica and the other perennials is obviously n o t related to division of the substrate into aerobic and anaerobic zones because all species possess extensive aerenchyma (Hutchinson, 1975). The differences may, however, be related to physiological adjustments associated with exploitation of different portions of the substrate.

Peltandra is the only species that has a b e l o w g r o u n d system that may extend d o w n w a r d to b e t w e e n 1 and 3 m. The other perennials are all r o o t e d in the

(8)

upper 50 cm of substrate and only have a few a e r e n c h y m a t o u s roots that penetrate deeper strata. Peltandra exploits deeper sediments than the other species b u t it must also pay an energetic price for having roots that are in a continuously waterlogged and anaerobic substrate. Both of those conditions inhibit efficient u p t a k e of nutrients and cause plants to p r o d u c e larger amounts of r o o t surface per unit of leaf surface (Shaver and Billings, 1975). The belowground:aboveground ratios of Peltandra may, therefore, be caused by a physiological response. We would expect that both the shallower r o o t e d perennials and annuals would have smaller R:S ratios because t h e y occur in that portion of the substrate where conditions are not always anaerobic and where there is some drainage during each tide cycle. Scirpus fluviatilis was the only species that did n o t follow this prediction. The perennials that r o o t near the surface had R: S ratios that are rather similar even though they are taxonomically unrelated and represent a wide spectrum of morphological types. Typha latifolia, Acorus calamus, Scirpus fluviatilis and Sparganium americanum have linear leaves and either rhizomateous or creeping r o o t s t o c k s for underground structures (Muenscher, 1944). Nuphar advena, Sagittaria latifolia and Pontederia cordata have arrowhead-shaped leaves, b u t dissimilar belowground structures.

Nuphar is rhizomateous and Pontederia and Sagittaria have small non-rhizome- forming stems.

Sagittaria latifolia is interesting because it behaves like an annual for most of the growing season. The species overwinters with rootless turions that are usually f o u n d at a depth of b e t w e e n 10 and 30 cm in the substrate. In the spring, each turion produces a s h o o t that grows to the wetland surface where a plant begins to develop. Shortly after development begins, the turion and connecting shoot decay rapidly so that each individual plant consists of leaves, a stem and roots that are p r o d u c e d during the current growing season. New turions are n o t p r o d u c e d until very late in the growing season. If we eliminate turion biomass from the R:S calculations, the R:S of Sagittaria averaged 0.39 rather than 0.94 as shown in Table I. The former value is very similar to the ratio of the annuals (Table I). Physiological adaptations of species to rooting depths may, therefore, be important in regulating the allocation of biomass.

While this study has focused on the biomass allocation patterns of freshwater tidal wetland macrophytes, it has i m p o r t a n t implications for studies of primary productivity in freshwater wetlands dominated by m a c r o p h y t e s that are n o t grasses or sedges. Our data show clearly that regression equations can be used to estimate belowground biomass from aboveground biomass for perennials and most annuals using a relatively small (7--25) sample size. Gener- ally, the linear regression model is most suitable b u t for species with an ex- tremely large belowground c o m p o n e n t , such as Peltandra, an exponential model is more appropriate. With the use of regression equations, it is possible to accurately estimate belowground standing crop -- indeed, net belowground production for annual species -- thus greatly enhancing future wetland primary productivity studies. The need for inclusion of the belowground c o m p o n e n t in wetland productivity studies is urgent (de la Cruz, 1978) and as future studies

(9)

363 f o c u s o n this c o m p o n e n t , t h e specific f a c t o r s t h a t g o v e r n t h e p a t t e r n s o f biomass a l l o c a t i o n r e p o r t e d h e r e will be m o r e fully e l u c i d a t e d .

ACKNOWLEDGEMENTS

We w o u l d like t o t h a n k o u r s t u d e n t s a n d r e s e a r c h assistants f o r t h e i r help a n d R a l p h G o o d , J o h n F a l k a n d Steve T u r i t z e n f o r t h e i r c o m m e n t s o n t h e m a n u s c r i p t . This w o r k was s u p p o r t e d , in part, b y grants f r o m t h e H a m i l t o n T o w n s h i p E n v i r o n m e n t a l C o m m i s s i o n , H a m i l t o n T o w n s h i p P l a n n i n g D e p a r t - m e n t , H a m i l t o n T o w n s h i p D e p a r t m e n t o f Water P o l l u t i o n C o n t r o l a n d U.S.

D e p a r t m e n t I n t e r i o r Office o f Water R e s e a r c h a n d T e c h n o l o g y ( G r a n t B-060- NJ).

REFERENCES

Bernard, J.M., 1974. Seasonal changes in standing crop and primary production in a sedge wetland and an adjacent dry old-field in central Minnesota. Ecology, 55: 350--359.

Bernard, J.M. and Bernard, F.A., 1973. Winter biomass in Typha glauca and Sparganium eurycarpum ecosystems. Bull. Torrey Bot. Club, 100: 125--127.

Bernard, J.M. and Gorham, E., 1978. Life history aspects of primary production insedge wetlands. In: R.E. Good, D.F. Whigham and R.L. Simpson (Editors), Freshwater Wet- lands: Ecological Processes and Management Potential. Academic Press, New York, pp.

34--52.

Boyd, C.E., 1969. Production, mineral nutrient absorption and biochemical assimilation by Justicia americana and Alternanthera philoxeroides, Arch. Hydrobiol., 66: 139--160.

Boyd, C.E., 1970. Production, mineral accumulation and pigment concentrations in Typha latifolia and Scirpus americanus. Ecology, 51: 285--290.

Boyd, C.E., 1971. Further studies on productivity, nutrient and pigment relationships in Typha latifolia populations. Bull. Torrey Bot. Club, 98: 144--150.

de la Cruz, A., 1978. Primary production: summary and recommendations. In: R..E Good, D.F. Whigham and R.L. Simpson (Editors), Freshwater Wetlands: Ecological Processes and Management Potential. Academic Press, New York, pp. 79--86.

Dore, W.G., 1969. Wild rice. Publ. No. 1393. Canada Dept. Agric., Ottawa, Canada. 84 pp.

Dykyjov~, D., Ondok, P.J. and Hradeck~, D., 1972. Growth rate and development of the root/shoot ratio in reedswamp macrophytes grown in winter hydroponic cultures. Folia Geobot. Phytotaxon., 7: 259--268.

Gleason, H.A. and Cronquist, A., 1963. Manual of Vascular Plants of Northeastern United States and Adjacent Canada. van Nostrand, Princeton, N.J., 810 pp.

Good, R.E. and Good, N.F., 1975. Vegetation and production of the Woodbury Creek-- Hessian Run freshwater tidal marshes. Bartonia, 43: 38--45.

Harper, J.L. and White, J., 1974. The demography of plants. Annu. Rev. Ecol. Syst., 5:

419--463.

Hutchinson, G.E., 1975. A Treatise on Limnology. Vol. III, Limnological Botany. Wiley- Interscience, New York, 660 pp.

Jervis, R.A., 1969. Primary production in the freshwater marsh ecosystem of Troy Meadows, New Jersey. Bull. Torrey Bot. Club, 96: 209--231.

Likens, G.E., 1976. Primary productivity of inland aquatic ecosystems. In: H. Lieth and R.H. Whittaker (Editors), Primary Productivity of the Biosphere. Springer-Verlag, New York, pp. 185--202.

(10)

McCormick, J., 1970. The natural features o f Tinicum Marsh, with particular emphasis on the vegetation. In: J. McCormick, R.R. Grant, Jr. and R. Patrick (Editors), Two Studies o f Tinicum Marsh, Delaware and Philadelphia Counties, Pa. The Conservation Foundation, Washington, D.C., 104 pp.

McCormick, J. and Ashbaugh, T., 1972. Vegetation of a section of Oldmans Creek tidal marsh and related areas in Salem and Gloucester Counties, New Jersey. Bull. N.J. Acad.

Sci., 17: 31--37.

McNaughton, S.J., 1974. Developmental control of net productivity in Typha latifolia ecotypes. Ecology, 55: 864--869.

Muenscher, W.C., 1944. Aquatic Plants of the United States. Cornell University Press, Ithaca, N.Y., 374 pp.

Radford, A.E., Ahles, H.E. and Bell, C.R., 1968. Manual of the Vascular Flora of the Carolinas. University of North Carolina Press, Chapel Hill, N.C., 1183 pp.

Shaver, G.R. and Billings, W.D., 1975. R o o t production and r o o t turnover in a wet tundra ecosystem, Barrow, Alaska, Ecology, 56: 401--409.

Simpson, R.L., Whigham D.F. and Walker, R., 1978. Seasonal patterns of nutrient move- ment in a freshwater tidal marsh. In: R.E. Good, D.F. Whigham and R.L. Simpson (Editors), Freshwater Wetlands: Ecological Processes and Management Potential.

Academic Press, New York, pp. 243--258.

Sokal, R.R. and Rohlf, F.J., 1969. Biometry. Freeman, San Francisco, 776 pp.

Whigham, D. and Simpson, R.L., 1976. The potential use of freshwater tidal marshes in the management of water quality in the Delaware River. In: J. Tourbier and R.W. Pierson, Jr. (Editors), Biological Control of Water Pollution. University of Pennsylvania Press, Philadelphia, Pa., pp. 173--186.

Whigham, D. and Simpson, R.L., 1977. Growth, mortality, and biomass partitioning in freshwater tidal wetland populations of wild rice (Zizania aquatica var. aquatica). Bull.

Torrey Bot. Club, 104: 347--351.

Whigham, D.F., McCormick, J., Good, R.E. and Simpson, R.L., 1978. Biomass and primary p r o d u c t i o n in freshwater tidal wetlands of the Middle Atlantic Coast. In: R.E. Good, D.F. Whigham and R.L. Simpson (Editors), Freshwater Wetlands: Ecological Processes and Management Potential. Academic Press, New York, pp. 3--20.