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Resource allocation at the individual plant level
Aquatic Botany, 41 ( 1991 ) 67-86
67
Elsevier Science Publishers B.V., Amsterdam
Resource allocation at the individual plant level* John D.
Madsen
1
Rensselaer Fresh Water Institute, MRC 203, Rensselaer Polytechnic Institute, Troy, N Y 12180-3590, USA (Accepted for publication 20 December 1990)
ABSTRACT Madsen, J.D., 1991. Resource allocation at the individual plant level. Aquat. Bot., 41: 67-86. Although resource allocation studies are well represented in terrestrial plant ecological literature, such studies have been tangential, at best, for submersed aquatic macrophytes. Utilizing data from published studies, trends in the allocation of resources are examined for sexual and asexual propagation of both annual and perennial macrophytes, seasonal patterns in allocation and storage, specialization of structures for storing carbohydrates, and tissue nutrient allocation. The effect of environmental conditions on allocation patterns, leaf shape, and growth form are also discussed. Finally, a cost/benefit model of leaf construction and maintenance costs vs. lifetime yield is presented as an explanation of high leaf turnover rates in productive species.
INTRODUCTION
Resource allocation consists of difficult 'choices' between what are often competing demands. Generous capital investments into leaves and stems for increased photosynthesis may exceed the ability of the root apparatus to both support shoot mass and acquire necessary mineral building blocks. Too great an investment in root material may create an unacceptable overhead of maintenance respiration. Either excess neglects the importance of perpetuating the species by means of successfully pollinating ovules, or by creating propagules of an adequate size to survive the cruel realities of natural selection. The result of poor investment is not merely bankruptcy, but the extinction of a plant's genome, if not its species. The resources plants allocate to various organs and functions are molecules, the building blocks of matter, and energy, the power to build, converted from light into chemical reserves through plant metabolism. Building blocks include carbon, reduced from the atmosphere or dissolved CO2, and many *Rensselaer Fresh Water Institute Contribution No. 566. JPresent address: AScI Corporation, USAE WES, Lewisville Aquatic Ecosystem Research Facility, RR3 Box 446, Lewisville, T X 75056, USA.
0304-3770/91/$03.50
© 1991 - - Elsevier Science Publishers B.V.
68
J.D. MADSEN
mineral nutrients acquired from the sediment or water column. These resources are necessary to form structures and acquire additional energy, minerals, and carbon, as well as for reproduction (both sexual and asexual). Plant resource allocation studies have examined total energy (calories), dry weight, carbon, nitrogen and phosphorus allocation patterns. Allocation patterns have been shown to vary with the size and age of the plant, season, and environmental conditions. Submersed aquatic macrophytes are particularly interesting in that highly plastic responses may be exhibited within a single population. Cost/benefit analyses applied to resource allocation permit the testing of hypotheses regarding allocation patterns and strategies for plant survival. Analyses of the costs of construction and materials as related to leaf size and longevity are typical of this approach (Orians and Solbrig, 1977 ). In this review, the available data on resource allocation in reproduction and growth of submersed macrophytes are summarized. The role of differing environments is examined, indicating the extent of plastic responses in plant resource allocation. Lastly, the concept of cost/benefit analyses is applied to growth forms of submersed aquatic macrophytes. LIFE CYCLE STRATEGIES
Even though reproductive allocation is strongly affected by environmental conditions, certain trends can be identified among the basic reproductive strategies exhibited by submersed aquatic macrophytes. In this section, I will classify these basic strategies as either annual (A), overwintering strictly by seeds, or perennial, in which vegetative parts overwinter. The perennial strategies can be separated into those using a vegetative propagule for overwintering, such as a turion, tuber, or winter bud, designated as perennial herbaceous (Ph), and those which overwinter using vegetative, non-reproductive biomass designated as perennial overwintering (Po), or evergreen species. The relative advantages of sexual and asexual propagation are quite different. The associated costs of sexual propagation are generally higher than for asexual propagation, and require more specialized structures. Seeds are generally smaller than vegetative propagules, with a more resistant coating. Two obvious advantages of sexual propagation are that the propagules are more resistant to environmental stress than vegetative propagules, and sexual propagation allows for the recombination of genetic traits. Asexual propagules are less differentiated; in some instances they are merely stem fragments and require no specialized allocation. Vegetative propagules have larger reserves, allowing a more rapid initial growth phase. As the aquatic environment is buffered from extremes of the environment, vegetative propagules are generally sufficient to ensure overwintering. Data on the production of seeds and asexual propagules (e.g. tubers or tur-
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
69
ions) per unit area are presented in Table 1. Annual plants produce more seeds per unit area than either of the perennial types, apparently because seed production for annuals is the only means of overwintering. This higher production by annuals may be a function of higher seed production per stalk or a higher number of stalks per unit area. Perennial submersed macrophytes often produce few, if any, seeds. An interesting example of this within a single species is the marine macrophyte, Zostera marina L. Zostera marina may adopt the strategy of either an annual or a perennial, often in adjacent localities. Annual Z. marina produces seven times more seeds per unit area than perennial Z. marina (Keddy, 1987). Annual Z. marina optimizes biomass growth by allocation to structures associated with flowering, at the expense of vegetative structures, in comparison with perennial Z. marina. Although perennial species may produce some seeds, they produce as many as twice the number of vegetative propagules as seeds (Table 1 ). Overall, however, the number of seeds produced by annual species exceeds the number of asexual propagules produced by perennials by as much as two orders of magnitude. In Table 2, data on propagule dry weight and percent germination are presented. In general, the percentage of vegetative propagules achieving reproTABLE l
Propagule production as density (number per square meter) of seeds and asexual propagules for annual ( A ) , perennial herbaceous (Ph), and overwintering perennial (Po) submersed aquatic macrophytes Species
Lepilaena cylindrocarpa
Seed density
Asexual propagule density
(nm -2)
(nm -2)
A
99400
-
6
A
10696
-
7
A A Ph Ph Ph Ph Ph
799630 78000 1445 7000 1985 330 491
1129 544 358 75 322
7 3 4 7 7 2 7
Ph Ph Po Po Po
61 890 14200 11000
109 1963 510 -
7 6 1 5 3
A, Ph or Po
Ref.
(Koern. ex Walp. ) Benth.
Najas guadalupensis (Spreng.) Magn.
Zannichellia palustris L. Zostera marina L. Potamogeton crispus L. Potamogetonfoliosus Raf. Potamogeton nodosus Poir. Potamogeton pectinatus L. Potamogeton richardsonii (A. Benn. ) Rydb.
Potamogeton vaginatus Turcz. Ruppia polycarpa R. M a s o n Hydrilla verticillata (L.f.) Royle Lobelia dortmanna L. Zostera marina L.
~1, Bowes et al., 1979; 2, Kautsky, 1987; 3, Keddy, 1987; 4, Rogers and Breen, 1980; 5, Szmeja, 1987a,b; 6, Vollebergh and C o n g d o n , 1986; 7, Yeo, 1966.
70
J.D. MADSEN
TABLE 2
Propagule type, percentage germination, and weight (mg dry weight) for annual, herbaceous perennial and overwintering perennial submersed macrophytes Species
A, Ph or Po
Propagule type Percent Weight germination (mg DW)
Ref,
Lepilaena cylindrocarpa
A
Seed
12
(Koern. ex Walp.) Benth. Ruppia maritima L. Zannichellia major Boenn. Zannichellia palustris L. Hydrillaverticillata (L.f,) Royle 2 Hydrilla verticillata (L.f.) Royle 3 Potamogeton berchtoldii Fieber Potamogeton crispus L. Potamogeton crispus L. Potamogeton pectinatus L. Potamogeton pectinatus L. Ruppiapolycarpa R. Mason Ruppiapolycarpa R. Mason Lobelia dortmanna L. Myriophyllum spicatum L. Ruppia megacarpa R. Mason
A A A Ph Ph Ph Ph Ph Ph Ph Ph Ph Po Po Po
Seed Seed Seed Tuber Tuber Turion Turion Seed Tuber Seed Seed Turion Seed Seed Seed
85 12 56 100 88 100 45 60 0.001 100 8 35 65 80 69 27.8
0.120 66.66 35.55 11 5.045 0.011 56.2 0.510 1.225 0.6 -
1 10 10 8 8 6 5 3,5 7,11 11 12 12 9 4 2
t l, Agami and Waisel, 1988; 2, Brock, 1982; 3, Hunt and Lutz, 1959; 4, Madsen and Boylen, 1988; 5, Rogers and Breen, 1980; 6, Sastroutomo, 1981; 7, Spencer, 1986; 8, Steward and Van, 1987; 9, Szmeja, 1987a; 10, van Vierssen, 1982; 11, van Wijk, 1983; 12, Vollebergh and Congdon, 1986. 2Dioecious strain. 3Monoecious strain.
ductive success is higher than that of seeds. These observations could result from two different conditions: (i) although most vegetative propagules lack true dormancy (Bartley and Spence, 1987), seeds may have strong dormancy patterns (Agami and Waisel, 1988 ); ( ii ) vegetative propagules are one to two orders of magnitude larger than seeds, as measured by dry weight (Table 2), which confers higher possible propagule viability (Spencer, 1986). To compensate for these differences, seed production may be substantially greater than asexual propagule production, as noted in Table 1. The ecological functions of differing types of propagules must be considered to better understand the relative trade-off between sexual and asexual reproduction. For the perennial herbaceous macrophytes (Ph), seeds allow long-distance dispersal or long periods of dormancy, while asexual propagules are more suited to short-term dormancy (e.g. overwintering) or short-distance dispersal (van Wijk, 1983). Perennial species may then have a small, hardy seed for long-distance dispersal, and a large vegetative propagule for short-distance dispersal and overwintering. Annual macrophytes must utilize seeds for both purposes. For some species, such as Trapa natans L., the pro-
RESOURCEALLOCATIONAT THE INDIVIDUALPLANT LEVEL
71
TABLE 3
Biomass allocation (as a percentage of total dry weight) to sexual and asexual propagation and vegetative growth structures for submersed aquatic macrophytes of annual (A), perennial herbaceous (Ph), and perennial overwintering (Po) forms Species
Hydrilla verticillata
A, Ph or Po
Propagation
Vegetative
Sexual
Asexual Total
Shoot Root
Total
Ref.
Ph
-
40
40
60
-
60
8
A Po Ph Ph
29 7 < 1 -
42 27
29 7 42 27
51 41 52 54
20 52 6 19
71 93 58 73
10 6 5 7
Ph Ph Po
38 22 20
38 26 25
56 74 45
6
4 5
30
62 74 75
7 4 1
Ph Ph Ph Ph
2 21 13 4
66 3 21 34
68 24 34 38
26 54 51 20
6 22 15 42
32 76 66 62
3 1 10 1
Ph
< 1
25
26
61
13
74
9
Ph
10
22
32
61
7
68
2
(L.f.) Royle
Lepilaena cylindrocarpa (Koern. ex Walp.) Benth. Lobelia dortmanna L. Potamogeton crispus L. Potamogeton nodosus Poir. Potamogeton pectinatus L. Potamogeton pectinatus L.
Ruppia megacarpa R. Mason
Ruppia occidentalis Watson Ruppia polycarpa R. Mason Ruppia polycarpa R. Mason Ruppia tuberosa Davis & Tomlinson
Vallisneria americana Michx.
Vallisneria americana Michx.
~1, Brock, 1983; 2, Donnermeyer and Smart, 1985; 3, Husband and Hickman, 1985; Kautsky, 1987; 5, Kunii, 1982; 6, Moeller, 1978; 7, Spencer and Anderson, 1987; 8, Steward and Van, 1987; 9, Titus and Stephens, 1983; 10, Vollebergh and Congdon, 1986.
duction of a small number of large seeds may be adaptive by creating a large, highly viable propagule with large reserves for rapid spring growth. On the other hand, large numbers of small seeds (e.g. Zannichellia palustris L., Table 1) saturate the environment with propagules. The hardiness of seeds increases the probability of survival, particularly for long-term dormancy or long-distance dispersal. Overwintering perennials (Po) are also capable of perennation through their standing biomass, thus either negating the need for asexual propagules, or diminishing the need for specialized structures. For instance, Myriophyllum spicatum L. successfully utilizes stem fragments as an asexual means of short-distance dispersal. Allocation to reproduction varies greatly with extremes in environmental conditions, e.g. ranging from 5 to 42% of the total biomass for Potamogeton pectinatus L. depending on whether it is found in sheltered or partially exposed habitats (Kautsky, 1987). Under typical environmental conditions,
72
J.D. MADSEN
biomass allocation to propagation is quite consistent for annual and perennial submersed macrophytes (Table 3). Generally, 30% of total biomass is allocated to propagation of some form by annuals and herbaceous perennials (A, Ph), a figure consistent with observations made for both annual and perennial terrestrial plants (Fitter, 1986). The allocation between sexual and asexual forms of propagation varies between groups of submersed macrophytes. The one example in Table 3 of allocation to seed production in a true annual (A) indicates 29% of biomass allocated to sexual propagation. Both herbaceous and overwintering perennials allocated only 5%, on average, of total biomass to sexual propagation, with 25% or more of biomass allocated to asexual propagules. SEASONALITY OF ALLOCATION PATTERNS
For most perennial macrophytes, distinct seasonal cycles of carbon and nutrients are characteristic of overwintering strategies. Carbohydrate reserves are important to the overwintering and competitive ability of many macrophytes (Titus and Adams, 1979). A typical seasonal pattern for carbohydrate storage indicates high levels in spring, before intensive plant growth, followed by consumption and dilution of reserves through the early and mid growing season (Fig. 1 ). After active growth has ceased, the plant allocates fixed carbon to storage for overwintering. Although this pattern is from the simplest case in which the plant (Ceratophyllum demersum L. ) has neither roots nor specialized storage organs (Best and Visser, 1987 ), similar patterns are demonstrated for other species (Titus and Adams, 1979). Carbohydrate reserves are often laid down in overwintering stems; however, there is a greater storage efficiency in roots or modified stem tissue (such as tubers), where morphological and anatomical alterations increase the concentrations of carbohydrate reserves (Table 4). Although the production of .~.12 10"
o
86I
~
0
I
I
I
I
F
M
A
M J J A S MONTH OF THE YEAR
I
I
I
I
I
I
I
O
N
D
Fig. 1. Total reserved carbohydrates (as a percentage of dry weight) vs. month of the year for Ceratophyllum demersum (data from Best and Visser, 1987).
73
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
TABLE 4
Total non-structural carbohydrate (TNC) concentrations (as a percentage of dry weight) in tissues of submersed aquatic vascular plant species Species
Tissue
TNC (% DW cone. )
Ref. ~
Ceratophyllum demersum L. Myriophyllum spicatum L. Myriophyllum spicatum L. Potamogeton crispus L. Potamogeton crispus L. Vallisneria americana Michx. Vallisneria americana Michx. Vallisneria americana Michx.
Shoot Shoot Root Stem Turion Shoot Root Tuber
I1 20 20 17 40 15 28 46
1 3 3 2 2 3 3 3
]l, Best and Visser, 1987; 2, Kunii, 1989; 3, Titus and Adams, 1979. 300-
- 5O
0--0
SHOOT BIOMASS
E ] - - ' m BUD BIOMASS
I
I
-40 E
E
o 200. -30 o
-20 r~
N 100-
ffl 0.-..~~ 0
0 M
/
z
0
I
I
!
I
J
J
A S MONTH
I
I
0
N
0
Fig. 2. Shoot biomass and winter bud (tuber) biomass of Vallisneria americana for one growing season (data from Donnermeyer and Smart, 1985).
specialized structures allows for greater concentrations of stored carbohydrates, the lower biomass of these propagules relative to overwintering stems and roots may not compensate for this specialization if only total storage capacity is considered (Titus and Adams, 1979). However, the hardiness and dispersability of specialized propagules may confer other selective advantages. Production of propagules, as with production of reserve carbohydrates, follows a seasonal cycle. In general, propagule development follows the period of active biomass development (Fig. 2 ), and coincides with flower development and seed formation (Kunii, 1982; Donnermeyer and Smart, 1985 ). In many species, the propagule is the only overwintering portion of the plant. Active growth initiates from this propagule, until maximum biomass is approached. Either through environmental or physiological cues, the plant diverts energy and fixed carbon from biomass production to flower and seed production, and the formation of asexual propagules. Senescence follows,
74
J.D. M A D S E N
~-~ 6
0.4
TISSUE NUTRIENT CONCENTRATION o--o N
o--a
P
0.2 o
5
D.
o z
0
BIOMAS~ _
I
I
I
I
I
I
I
0.0
I
0.2 &"
~-" 400 E 300 .~200 o 100
~"10
1 E
8
o
4
NUTRIENT STANDING CROP N
I
.a---~ /
o--0
I
13--t] P
E
,0.1 o
0
I
I
I
I
I
d
d
A MONTH OF 1988
S
0
0.0
N
Fig. 3. Tissue concentration of nitrogen and phosphorus (as a percentage of dry weight), biomass (g dry weight m-2), and standing crop of nitrogen and phosphorus (g m-2) in the biomass of Myriophyllum spicatum (data from Madsen et al., 1989). 6 .~
'-,FLOWERING PLANTS 17-71 STERILE PLANTS
r" 0.5
FLOWERING PLANTS STERILE PLANTS
.0.4 3
~=4. .0.3
E3
.0.2
b_2" 0 Z
.0.1 o.
,0.0
LV
ST FL PLANTORGAN
FIR
LV
ST FL PLANTORGAN
R
Fig. 4. Nitrogen and phosphorus tissue concentrations in Lobelia dortmanna organs: LV, leaves; ST, stems; FL, floweringstalks; FR, fruits (data from Moeller, 1978). leaving only the seeds and asexual propagules to overwinter until the next growing season. Tissue concentrations of essential nutrients (e.g. phosphorus and nitrogen) follow similar patterns to those of reserve carbohydrates. Concentrations o f nutrients are typically high in the spring, before active growth. Plants often
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
75
contain high, 'luxury' levels of nutrients before active growth periods, either through continuous uptake or translocation to overwintering tissues. As growth initiates in the spring, uptake rates of nutrients typically lag behind growth rates of tissue, resulting in 'growth-dilution' of these nutrients (Fig. 3 ). Continued growth necessitates increased uptake rates of nutrients once critical tissue concentrations are approached. At this point, the total standing crop of nutrients within the tissue of the plants must increase to maintain critical concentrations in the plant. After maximum biomass is achieved and senescence of tissue begins, some nutrients may be translocated to overwintering tissues, resulting in higher concentrations in these tissues (Denny, 1980). However, the bulk of these nutrients usually is lost upon decomposition of senescing biomass. The distribution of nutrients within plant tissue is also a significant factor in the allocation of these resources. Photosynthetic tissues require higher levels of nitrogen, for the synthesis of photosynthetic enzymes, than root tissues. Reproductive tissues, seeds and asexual propagules, typically have higher concentrations of nutrients than most other tissues. For example, both sterile (non-flowering) and flowering plants of Lobelia dortmanna L. have been reported to have similar concentrations of nitrogen in leaf and stem material, with lower levels of nitrogen in the flowers (Moeller, 1978; Fig. 4). Fruits were higher in both nitrogen and phosphorus than leaf or stem material. The allocation of increased phosphorus to fruits may cause reduced availability of phosphorus to the vegetative tissues of flowering plants, as compared with sterile plants. It is clear that seasonal allocation patterns of both critical nutrients and carbohydrate reserves follow distinct patterns relative to the growth phases of aquatic plants, responding to environmental or physiological cues that create whole-plant changes. Allocation patterns vary seasonally both for the entire plant, and for individual organs throughout the year. ENVIRONMENT
Changing environmental factors may favor one species over another, or even cause the differential allocation of resources within a single species. For terrestrial plants, this has been observed for the effects of both shading and high winds, and for alterations in water supply or mineral nutrition (Fitter, 1986). For submersed macrophytes, incident light, stand density and selfshading influence allocation to stems and leaves (Duarte and Kalff, 1987). Leaf shape, size, and specific leaf area are influenced by plant depth and shading (Spence et al., 1973 ). Sediment chemistry, wave action, and other factors may also influence allocation patterns in submersed macrophytes.
76
J.D. MADSEN
Leaf shape and the environment Leaf form has often been cited as an adaptive feature in terrestrial plant ecology literature, such as the variation between sun and shade leaves (Fitter, 1986 ). However, little has been done to quantitatively examine leaf form in submersed macrophytes, though some work has been done on macroalgae (Koehl, 1986). The size, shape and number of leaves relate to resource allocation through the expenditure of energy and materials devoted to construct a more or less costly leaf, and their relative expected lifetime. For instance, the production of expensive, large leaves in environments where leaves may have a low life expectancy is a useless expenditure of necessary material. Leaf construction is a trade-off between maximizing photosynthetic area, and avoiding herbivory, stress (e.g. light or nutrient limitation) and disturbance (e.g. wave damage or drag) of these costly structures. Leaf size and shape may vary with environment within a given species. Leaves of Potamogeton pectinatus in still waters are short and fine, while those growing in streams are long and robust in appearance. Tubers ofP. pectinatus from stream populations, grown in still water cultures, will develop the fine leaves characteristic of lake populations (J.D. Madsen, personal observation, 1984). Genetically identical plants will exhibit differing phenotypes in response to water velocity with leaf shapes that are better adapted to the given flow conditions. Leaves of submersed macrophytes can be characterized as one of three groups: entire, dissected, and fenestrate (Sculthorpe, 1967 ). Although of various shapes, entire leaves are typically flattened and not broken into subcomponent leaflets. These leaves are typical of most monocotyledons, and some dicotyledons. Dissected leaves are usually composed of many fine, cylindrical leaflets. Dissected leaves are found only in dicotyledons. Fenestrate leaves have holes or 'windows' in an entire leaf blade, and are found only in some species within the Aponogetonaceae, a monocotyledonous family. A preliminary study of leaf shape and ecological adaptation involved examining data from herbarium specimens, literature sources, and photomicrographs (Madsen, 1986). Leaf type was differentiated into dissected, entire and fenestrate. As the latter form is rare, only dissected and entire leaves were analyzed in depth. By modeling leaf shapes based on simple hydrodynamic models, it was determined that in stagnant waters, dissected-leaved species had greatly reduced boundary-layer resistances, and might be favored under conditions of low flow where the acquisition of carbon and nutrients by diffusion would limit growth rates. However, under moderate flow rates with laminar flows, entire-leaved species were favored through inducing a turbulent boundary layer, thus greatly reducing diffusive barriers. Lastly, under high flows near the point at which turbulent flows would be expected, dis-
R E S O U R C E A L L O C A T I O N AT T H E I N D I V I D U A L P L A N T LEVEL
77
sected leaves are once more favored through reduced drag, hence less tearing and battering of leaf structure (Madsen, 1986). Using these model predictions, the composition of over 200 submersed macrophyte communities were examined for the percentage of entire-leaved and dissected-leaved species. As was expected from the models, streams and marine systems, with moderate, laminar flows dominating, had significantly higher percentages of species with entire leaves (98% and 100% median, respectively) than lake systems (median, 79%; Chi-square P = 0.0007; Fig. 5 ). In stream communities with areas of higher flow rates and turbulent flows, species with dissected leaves dominated. In contrast, marine systems are dominated by species with entire leaves, in part owing to the exclusive taxonomic grouping of seagrasses as monocotyledons, which do not have any species with dissected leaves. However, significant variation in leaf width occurs both within and between seagrass species and is an ecologically significant feature (Phillips and Lewis, 1983 ). Among lake communities, a trend was also noted (Fig. 5) of a high composition of species with entire leaves in oligotrophic systems (median, 94%), intermediate in mesotrophic communities (median, 80%), and lowest in eutrophic communities (median, 70%). The differences in the observed patterns were highly significant (Chi square P--0.0083). This pattern may be 20 15
7 ~
20 z 0
0 10 20 30 40 50 60 70 80 90100 PERCENTCLASSENTIRE 15
i1
80 10 20 ~0 40 50 6b io eo 90100 PERCENT CLASS ENTIRE
SOT
10 5 00102030405060708090100 PERCENTCLASSENTIRE 2025 I15,
EUTROPHIC LAKES
10 0
0 10 20 30 40 50 60 70 80 90100 PERCENTCLASSENTIRE
s'm~a~s
N
20211151
~INE
2O 10 0
0102030405060708090100
PERCENTCLASSENTIRE
O6 1o. :io . ~o. 40. go go 7o so do16o PERCENTCLASSENTIRE
Fig. 5. Percent classes of the macrophyte species composition composed of entire-leaved species vs. the number of cases observed for each percent class, for all lakes, oligotrophic lakes, mesotrophic lakes, eutrophic lakes, streams and marine communities. Data from Madsen, 1986.
78
J.D. MADSEN
interpreted as a gradient of reduced water m o v e m e n t from the low-growing communities in oligotrophic lakes, to the open heterogeneous canopies of mesotrophic lakes, and finally the extremely low current velocities of dense closed canopies, which are often monospecific, in eutrophic lakes. With decreased currents and increasingly dense canopies, diffusion-related processes become more limiting and enhance the adaptive value of dissected leaves (Madsen, 1986). Leaf shape is a significant adaptive feature for aquatic macrophytes, and should be studied further. Dissected leaves appear to be well suited to both stagnant water situations in being able to counteract diffusive resistance, and high flow situations, in being able to counteract the deleterious effects of drag. On the other hand, entire leaves are well suited to areas of moderate water movement, whether in open lake communities, marine communities, or moderate flow situations in streams, by inducing the formation of a turbulent boundary layer and thus greatly reducing diffusive resistance.
Growth form and environment One exceptionally interesting group of submersed macrophytes in terms of resource allocation patterns, is the isoetids. This group of morphologically similar but taxonomically unrelated plants shares the c o m m o n characteristics of evergreen leaves: low stature, a high root:shoot ratio, and low growth rates. Collectively, these characteristics have been interpreted to be adaptations to low-nutrient, low-productivity environments (Boston, 1986; Farmer and Spence, 1986 ), typical of a stress-tolerant species (Grime, 1977 ). Generally, isoetids predominate in waters low in nutrients and dissolved inorganic carbon (DIC). As is typical of terrestrial evergreen species in stressful environments, the isoetids have a low turnover rate which helps to conserve nutrients and carbon invested in leaf material (Table 5). For the most part, isoetid turnover rates are less than l, indicating that an individual leaf lasts more than a single year. Turnover rates for other species listed exceed one, demonstrating individual leaf lives of less than 6 months. Erect caulescent species, such as Potamogeton species forming a canopy, typically have higher turnover rates, in part due to self-shading of lower leaves during canopy development. Nonisoetid rosette species, such as Vallisneria species which have multiple elongated leaves arising from an underground stem, exhibit a range of turnover rates, in part from inhabiting high exposure sites, such as seagrass meadows, active wave zones, or streams. Isoetids in low-productivity environments maintain a low turnover rate to minimize the loss of limiting nutrients (Moeller, 1978 ) and carbon (Boston, 1986 ). Fertilization ofisoetids does not increase growth rates, compared with
RESOURCEALLOCATIONAT THE INDIVIDUALPLANTLEVEL
79
TABLE 5 Growth form, turnover rate (P/Bmax) and leaf weight (rag dry weight) for several macrophyte species Species
Growth form'
P/Bmax
Leaf wt. (mg DW)
Ref?
Myriophyllum spicatum L. Potamogeton pectinatus L. Ruppia cirrhosa (Petagna) Grande Isoetes macrospora Durieu Lobelia dortmanna L. Sparganium emersum Rehm. Zostera marina L.
C C C I I R R
3.8 2.01 2.5 0.85 0.69 2.3 2.5
2.32 52.1 1.56 5.8 2.5 60 140
1 4 3 2 5 6 7
~C, caulescent; I, isoetid; R, rosette. 21, Adams and McCracken, 1974; 2, Boston and Adams, 1986, 1987; 3, Kiorboe, 1980; 4, Madsen and Adams, 1988; 5, Moeller, 1978; 6, Nielsen et al., 1985; 7, Sand-Jensen, 1975.
other macrophyte species (Farmer and Spence, 1986), as is typical of all stresstolerators from low nutrient environments (Grime, 1977 ). In contrast, some macrophyte species from high productivity environments exhibit turnover rates of 2.5 or more, indicating a substantial loss of carbon and nutrients. Even with large leaves being lost, the productivity of the site enables higher turnover rates without stressing the availability of nutrients. Another interesting morphological adaptation of isoetids is the high root:shoot ratio. Although known to be important in the acquisition of nutrients, recent research also indicates that high allocation to roots relative to shoots is an important mode of DIC acquisition in low-productivity waters. The DIC levels of sediments in lakes where isoetids occur are 5-100 times higher than the overlying water column (Boston et al., 1987a,b). Therefore, these sediments supply a vastly superior source of DIC than the water column. Isoetids have developed the means to take up DIC from the sediments via the roots, and utilize the carbon in photosynthesis in the shoots. Isoetids acquire 60-99% of photosynthetic carbon from the sediment (Boston et ah, 1987a,b), in contrast to the less than _'.5% observed in non-isoetid species (Loczy et al., 1983 ). Some morphological adaptations that assist this process include a large root surface, internal lacunae for gas transport, and a thick cuticle over the leaves in some species (Boston et al., 1987a,b). Additionally, many isoetids have metabolic adaptations for nighttime carbon acquisition and reduced respiratory carbon loss (Boston and Adams, 1985, 1986). The root: shoot ratio of isoetids is substantially above that of both caulescent species and non-isoetid rosette species (Table 6). As substantial root uptake of DIC requires a high root:shoot ratio, this adaptation is unnecessary and counterproductive for a species not growing in low DIC waters. If suffi-
80
J.D. MADSEN
TABLE 6 Growth form, root:shoot ratio for dry weight ( R : S ) , and percentage of total carbon uptake from the
sediment via roots Species
Growth form ~
R: S
Percent C uptake (sediment)
Ref. 2
Lobelia dortmanna L. Littorella uniflora (L.)
I I
0.53 0.73
76-96 65-96
1 1
I I I C
0.79 1.03 1.29 0.05
60-96 85-98 89-99 0.3
1 1 1 2
C R
0.09 0.2
Aschers.
lsoetes macrospora Durieu Gratiola aurea Muhl. Eriocaulon septangulare With. Heteranthera dubia (Jacq.) MacMill.
Myriophyllum spicatum L. Vallisne?ia americana Michx.
0.1-1.0 1.4
2 2
]C, caulescent; I, isoetid; R, rosette. Zl, Boston et al., 1987a,b; 2, Loczy et al., 1983.
cient DIC is available in the water column, increased allocation to shoot material in non-isoetids allows increased photosynthesis and carbon uptake for enhanced productivity. C O S T / B E N E F I T ANALYSIS
With the application of optimization theory to ecology, many ecologists have examined the adaptiveness of costly plant structures or responses. One example of this investigation examines optimal leaf size using theoretical calculations of leaf functions under a variety of conditions (Parkhurst and
I .c
D
\
<>
0
0
E ,.n
0
o
~J~o o
-
o
0 0.0
I 0.5 RESPIRATION ( m g C
ISOETtO_ <> ROSETTE
I 1.0
1.5
g-1 h-l)
Fig. 6. Dark respiration vs. net photosynthetic rate ( b o t h in mg C g - L h - t ) for 22 species of submersed macrophytes.
RESOURCE ALLOCATION AT T H E I N D I V I D U A L PLANT LEVEL
8|
0 ISOET1D FLEXUOUS O CAULESCENT 0 ROSETTE []
zk
zx
E
0
en
Ix.
[]
O
O []
o
O o
[]
I~3 O
Az~
6)
D
[]
0 I
0.1
1.0
I
I
10.0 LEAF WEIGHT (rag)
100.0
Fig. 7. Leaf weight (rag) on a log scale vs. biomass turnover rate, P/Bm,~.
60 t, [] 0
ISOErlD FLEXUOUS CAULESCENT ROSETTE
4-
rlA
E ,.n 0.
°[3
O El
20
O
[] O
zx
O
D DD B
z~
%0
I I 10 100 ANNUAL PRODUCTIVITY ( g m - 2 y - l )
I 1000
Fig. 8. Annual productivity ( g m -2 y e a r - ~) on a log scale vs. turnover rate, P/Bma x.
"~ o
3025-
z
0 zx " [] '0'
ISOETID FLEXUOUS CAULESCENT ROSETTE
20.
z o
15.
~
10
~
5
rl
/k
o
/
I 2
I I I I 4 6 8 10 LEAF LIFE COST / UNIT WT. * DAY
12
Fig. 9. The costs of leaves of different submersed macrophyte species per unit weight per day of expected leaf life, vs. potential production per unit weight per day averaged over the life of the leaf.
82
J.D. MADSEN
Loucks, 1972 ). An examination based on costs and benefits (or income) was performed for plant leaves under arid and semi-arid conditions examining predicted performance and costs of construction (Orians and Solbrig, 1977 ). Some examples of costs and benefits involved in leaf construction and function will be examined using data for 24 species collected from a variety of literature sources. An annotated bibliography of species examined, data collected, and literature sources is available from the author. Data on leaf size, photosynthetic and respiratory rates, plant turnover rates (P/nmax), and annual productivity were collected, with species categorized based on plant form: isoetid, flexuous species, in which the stem grows recumbent and the plants are generally poorly rooted, if at all (e.g. Ceratophyllum ); caulescent, in which the stem grows erect and rooted in the sediment (e.g. Potamogeton); nonisoetid rosettes (e.g. Fallisneria). The most basic of resource allocations to be made is to the photosynthetic enzymatic complex. The most abundant protein by weight in plant tissue is ribulose diphosphate carboxylase, the enzyme required to reduce carbon dioxide to organic carbon. However, allocation to a large photosynthetic apparatus with a large amount of photosynthetic enzymes requires an increase in basal metabolic respiration. In Fig. 6, the relationship between maximum net photosynthetic rate and dark respiration for each species is presented. This line indicates a threshold of a factor of three more than reported dark respiration. All points fall near this line or above, not below. Although the factor of three is empirical and arbitrary, net photosynthesis must of necessity be substantially higher than respiration. Net photosynthesis must accrue stored energy for dark-period respiration, non-photosynthetic tissue respiration, and future periods of low or no photosynthesis. High respiratory rates dictate the need for high net photosynthetic rates to support it, yet high metabolic rates are required for high productivity. Note that the group with low productivity, the isoetids, have both low respiratory rates and low photosynthetic rates, while the higher productivity rosettes display a much higher level of photosynthesis and respiration. Another important component of examining the costs and benefits of allocation to leaves is the longevity and size of the leaf. Leaf sizes range widely in submersed macrophytes, and broadly cover a range of life expectancies (the inverse of the turnover rate, P/Bmax). Low productivity plants, such as the isoetids, have leaves of an intermediate size with a low turnover rate (Fig. 7 ). The bimodal distribution of turnover rates with leaf size is related to annual productivity: the largest leaves are found on high productivity rosettes, with intermediate turnover rates, while the highest turnover rates are exhibited by high productivity plants with very small leaves. These small leaves, with low investment in carbon, are rapidly lost with the growth of the plant's canopy and resultant self-shading. Examples of these plants include Myriophyllum spicatum and Hydrilla verticillata (L.f.) Royle.
RESOURCEALLOCATIONATTHE INDIVIDUALPLANTLEVEL
83
Allocation patterns are also dictated by expected productivity. If plants have higher productivity rates, they can afford to allocate carbon to higher turnover leaves, while plants on a strict carbon budget cannot afford to waste any energy on leaves of short life (Fig. 8 ). Higher productivity allows the potential of higher turnover rates, but relatively moderate turnover rates may still be observed in plants of relatively high productivity. Note again that isoetids are among the lowest in both turnover rates and productivity. Utilizing data on leaf size, net photosynthetic and respiratory rates, percent carbon in leaf tissue, and turnover rates, the cost of construction and maintenance of leaves over their lifetime (per unit weight) and the expected productivity can be calculated for each species (Fig. 9). The values presented are standardized over the expected life of the leaf. The line indicates the hypothetical break-even point where production equals costs. Isoetids rank lowest for both productivity and costs. This is expected in low-productivity environments, resulting from long-lived leaves of moderate size, which have low overhead. Some other plants minimize associated costs by producing many small leaves with a high turnover rate. The small investment offsets the short life of the leaf itself. In this cost/income analysis of submersed macrophyte leaves, I have shown some preliminary indications of how different types of submersed macrophyte species adapt to varying demands from the environment. Low productivity species, such as the isoetids, have a low-overhead, low-gain strategy. The leaves produced are of intermediate size, but are long lived and metabolically inexpensive. High-productivity species fall into two types: some produce many small leaves with a very high turnover (such as some caulescent species), while others produce large leaves of intermediate turnover rates (e.g. rosette species). In general, turnover rate increases with productivity rate. Also, the expected production of a leaf over its lifetime equals or exceeds the expected cost of the leaf. The study of resource allocation in submersed macrophytes has been tangential, at best. The potential exists for expanding our understanding of submersed macrophyte ecology, especially when combined with studies of limiting factors and methods of plant propagation.
REFERENCES Adams, M.S. and McCracken, M.D., 1974. Seasonal production of the Myriophyllum component of the littoral of Lake Wingra, Wisconsin. J. Ecol., 62: 457-467. Agami, M. and Waisel, Y., 1988. The role offish in distribution and germination of seeds of the submerged macrophytes Najas marina L. and Ruppia maritima L. Oecologia, 76: 83-88. Bartley, M.R. and Spence, D.H.N., 1987. Dormancy and propagation in helophytes and hydrophytes. Arch. Hydrobiol. Beih., 27:139-155. Best, E.P.H. and Visser, H.W.C., 1987. Seasonal growth of the submerged macrophyte Cerato.
84
J.D. MADSEN
phyllum demersum L. in mesotrophic Lake Vechten in relation to insolation, temperature and reserve carbohydrates. Hydrobiologia, 148: 231-243. Boston, H.L.,1986. A discussion of the adaptations for carbon acquisition in relation to the growth strategy of aquatic isoetids. Aquat. Bot., 26: 259-270. Boston, H.L. and Adams, M.S., 1985. Seasonal diurnal acid rhythms in two aquatic crassulacean acid metabolism plants. Oecologia, 65: 573-579. Boston, H.L. and Adams, M.S., 1986. The contribution of crassulacean acid metabolism to the annual productivity of two aquatic vascular plants. Oecologia, 68:615-622. Boston, H.L. and Adams, M.S., 1987. Productivity, growth, and photosynthesis of two small "isoetid" plants, Littorella uniflora and Isoetes macrospora. J. Ecol., 75: 333-350. Boston, H.L., Adams, M.S. and Pienkowski, T.P., 1987a. Models of the use of root-zone CO2 by selected North American isoetids. Ann. Bot., 60: 495-503. Boston, H.L., Adams, M.S. and Pienkowski, T.P., 1987b. Utilization of sediment CO2 by selected North American isoetids. Ann. Bot., 60: 485-494. Bowes, G., Holaday, A.S. and Haller, W.T., 1979. Seasonal variation in the biomass, tuber density, and photosynthetic metabolism of Hydrilla in three Florida lakes. J. Aquat. Plant Manage., 17: 61-65. Brock, M.A., 1982. Biology of the salinity tolerant genus Ruppia L. in saline lakes in south Australia II. Population ecology and reproductive biology. Aquat. Bot., 13: 249-268. Brock, M.A., 1983. Reproductive allocation in annual and perennial species of the submersed aquatic halophyte Ruppia. J. Ecol., 71: 811-818. Denny, P., 1980. Solute movement in submerged angiosperms. Biol Rev., 55: 65-92. Donnermeyer, G.N. and Smart, M.M., 1985. The biomass and nutritive potential of Vallisneria americana Michx. in navigation pool 9 of the upper Mississippi River. Aquat. Bot., 22: 3344. Duarte, C.M. and Kalff, J., 1987. Weight-density relationships in submerged macrophytes: the importance of light and plant geometry. Oecologia, 72:612-617. Farmer, A.M. and Spence, D.H.N., 1986. The growth strategies and distribution of isoetids in Scottish freshwater lochs. Aquat. Bot., 26: 247-258. Fitter, A.H., 1986. Acquisition and utilization of resources. In: M.J. Crawley (Editor), Plant Ecology, Chap. 12, Blackwell Scientific Publications, Oxford, pp. 375-405. Grime, J.P., 1977. Plant Strategies and Vegetation Processes. Wiley, New York, 222 pp. Hunt, G.S. and Lutz, R.W., 1959. Seed production by curly-leaved pondweed and its significance to waterfowl. J. Wildl. Manage., 23: 405-408. Husband, B.C. and Hickman, M., 1985. Growth and biomass allocation ofRuppia occidentalis in three lakes, differing in salinity. Can. J. Bot., 63: 2004-2014. Kautsky, L., 1987. Life-cycles of three populations of Potamogeton pectinatus L. at different degrees of wave exposure in the Asko area, northern Baltic proper. Aquat. Bot., 27:177-186. Keddy, C.J., 1987. Reproduction of annual eelgrass: variation among habitats and comparison with perennial eelgrass (Zostera marina L.). Aquat. Bot., 27: 243-256. Kiorboe, T., 1980. Production of Ruppia cirrhosa (Petagna) Grande in mixed beds in Ringkobing Fjord (Denmark). Aquat. Bot., 9:135-143. Koehl, M.A.R., 1986. Seaweeds in moving water: form and mechanical function. In: T. Givnish (Editor), On Plant Form and Function, Chap. 18. Cambridge University Press, London, pp. 603-634. Kunii, H., 1982. Life cycle and growth of Potamogeton crispus L. in a shallow pond, Ojaga-ike. Bot. Mag. Tokyo, 95: 109-124. Kunii, H., 1989. Continuous growth and clump maintenance ofPotamogeton crispus L. in Narutoh River, Japan. Aquat. Bot., 33:13-26. Loczy, S., Carignan, R. and Planas, D., 1983. The role of roots in carbon uptake by the sub-
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEE
85
mersed macrophytes Myriophyllum spicatum, Vallisneria americana, and Heteranthera dubia. Hydrobiologia, 98: 3-7. Madsen, J.D., 1986. The production and physiological ecology of the submersed aquatic macrophyte community in Badfish Creek, Wisconsin. Ph.D. Dissertation, University of Wisconsin-Madison, 445 pp. Madsen, J.D. and Adams, M.S., 1988. The seasonal biomass and productivity of the submerged macrophytes in a polluted Wisconsin stream. Freshwater Biol., 20:41-50. Madsen, J.D. and Boylen, C.W., 1988. Seed ecology of Eurasian Watermilfoil (Myriophyllum spicatum L.). Rensselaer Fresh Water Institute Rep. 88-7, Rensselaer Polytechnic Institute, Troy, NY, 26 pp. Madsen, J.D., Sutherland, J.W., Bloomfield, J.A., Roy, K.M., Eichler, L.W. and Boylen, C.W., 1989. Lake George Aquatic Plant Survey Final Report. New York State Department of Environmental Conservation, Albany, New York, 219 pp. Moeller, R.E., 1978. Seasonal changes in biomass, tissue chemistry, and net production of the evergreen hydrophyte, Lobelia dortmanna. Can. J. Bot., 56:1425-1433. Nielsen, L.W., Nielsen, K. and Sand-Jensen, K., 1985. High rates of production and mortality of submerged Sparganium emersum Rehman during its short growth season in a eutrophic Danish stream. Aquat. Bot., 22: 325-334. Orians, G.H. and Solbrig, O.T., 1977. A cost-income model of leaves and roots with special reference to arid and semiarid areas. Am. Nat., 111: 677-690. Parkhurst, D.F. and Loucks, O.L., 1972. Optimal leaf size in relation to environment. J. Ecol., 60: 505-537. Phillips, R.C. and Lewis, IIl, R.L., 1983. Influence of environmental gradients on variations in leaf widths and transplant success in North American seagrasses. Mar. Tech. Sci. J., 17 (2): 59-68. Rogers, K.H. and Breen, C.M., 1980. Growth and reproduction of Potamogeton crispus in a South African lake. J. Ecol., 68: 561-571. Sand-Jensen, K., 1975. Biomass, net production and growth dynamics in an eelgrass (Zostera marina L. ) population in Vellerup Vig, Denmark. Ophelia, 14:185-201. Sastroutomo, S.S., 1981. Germination of turions in Potamogeton berchtoldii. Bot. Gaz., 142: 454-460. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular Plants. Edward Arnold, London, 610 PP. Spence, D.H.N., Campbell, R.M. and Crystal, J., 1973. Specific leaf areas and zonation of freshwater macrophytes. J. Ecol., 61: 317-328. Spencer, D.F., 1986. Tuber demography and its consequences for Potamogeton pectinatus L. Proc. EWRS/AAB Symp. Aquat. Weeds, 7: 321-325. Spencer, D.F. and Anderson, L.W.J., 1987. Influence of photoperiod on growth, pigment composition and vegetative propagule formation for Potamogeton nodosus Poir. and Potamogeton pectinatus L. Aquat. Bot., 28:103-112. Steward, K.K. and Van, T.K., 1987. Comparative studies of monoecious and dioecious ttydrilla (Hydrilla verticillata) biotypes. Weed Sci., 35: 204-210. Szmeja, J., 1987a. The seasonal development of Lobelia dortmanna L. and annual balance of its population size in an oligotrophic lake. Aquat. Bot., 28:15-24. Szmeja, J., 1987b. The structure of a population of Lobelia dortmanna L. along a gradient of increasing depth in an oligotrophic lake. Aquat. Bot., 28:1-13. Titus, J.E. and Adams, M.S., 1979. Comparative carbohydrate storage and utilization patterns in the submersed macrophytes, Myriophyllum spicatum and Vallisneria americana. Am. Midl. Nat., 102: 263-272. Titus, J.E. and Stephens, M.D., 1983. Neighbor influences and seasonal growth patterns for Vallisneria americana in a mesotrophic lake. Oecologia, 56: 23-29.
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Van Vierssen, W., 1982. The ecology of communities dominated by Zannichellia taxa in western Europe. I. Characterization and autecology of the Zannichellia taxa. Aquat. Bot., 12: 103-155. Van Wijk, R.J., 1983. Life-cycles and reproductive strategies of Potamogeton pectinatus L. in the Netherlands and the Camargue (France). Proceedings of an International Symposium on Aquatic Macrophytes, 18-23 September 1983, Nijmegen, Netherlands. Faculty of Science, Catholic University, Nijmegen, pp. 317-32 I. Vollebergh, P.J. and Congdon, R.A., 1986. Germination and growth of Ruppia polycarpa and Lepilaena cylindrocarpa in ephemeral saltmarsh pool, Westernport Bay, Victoria. Aquat. Bot., 26: 165-179. Yeo, R.R., 1966. Yields ofpropagules of certain aquatic plants I. Weeds, 14:110-113.
67
Elsevier Science Publishers B.V., Amsterdam
Resource allocation at the individual plant level* John D.
Madsen
1
Rensselaer Fresh Water Institute, MRC 203, Rensselaer Polytechnic Institute, Troy, N Y 12180-3590, USA (Accepted for publication 20 December 1990)
ABSTRACT Madsen, J.D., 1991. Resource allocation at the individual plant level. Aquat. Bot., 41: 67-86. Although resource allocation studies are well represented in terrestrial plant ecological literature, such studies have been tangential, at best, for submersed aquatic macrophytes. Utilizing data from published studies, trends in the allocation of resources are examined for sexual and asexual propagation of both annual and perennial macrophytes, seasonal patterns in allocation and storage, specialization of structures for storing carbohydrates, and tissue nutrient allocation. The effect of environmental conditions on allocation patterns, leaf shape, and growth form are also discussed. Finally, a cost/benefit model of leaf construction and maintenance costs vs. lifetime yield is presented as an explanation of high leaf turnover rates in productive species.
INTRODUCTION
Resource allocation consists of difficult 'choices' between what are often competing demands. Generous capital investments into leaves and stems for increased photosynthesis may exceed the ability of the root apparatus to both support shoot mass and acquire necessary mineral building blocks. Too great an investment in root material may create an unacceptable overhead of maintenance respiration. Either excess neglects the importance of perpetuating the species by means of successfully pollinating ovules, or by creating propagules of an adequate size to survive the cruel realities of natural selection. The result of poor investment is not merely bankruptcy, but the extinction of a plant's genome, if not its species. The resources plants allocate to various organs and functions are molecules, the building blocks of matter, and energy, the power to build, converted from light into chemical reserves through plant metabolism. Building blocks include carbon, reduced from the atmosphere or dissolved CO2, and many *Rensselaer Fresh Water Institute Contribution No. 566. JPresent address: AScI Corporation, USAE WES, Lewisville Aquatic Ecosystem Research Facility, RR3 Box 446, Lewisville, T X 75056, USA.
0304-3770/91/$03.50
© 1991 - - Elsevier Science Publishers B.V.
68
J.D. MADSEN
mineral nutrients acquired from the sediment or water column. These resources are necessary to form structures and acquire additional energy, minerals, and carbon, as well as for reproduction (both sexual and asexual). Plant resource allocation studies have examined total energy (calories), dry weight, carbon, nitrogen and phosphorus allocation patterns. Allocation patterns have been shown to vary with the size and age of the plant, season, and environmental conditions. Submersed aquatic macrophytes are particularly interesting in that highly plastic responses may be exhibited within a single population. Cost/benefit analyses applied to resource allocation permit the testing of hypotheses regarding allocation patterns and strategies for plant survival. Analyses of the costs of construction and materials as related to leaf size and longevity are typical of this approach (Orians and Solbrig, 1977 ). In this review, the available data on resource allocation in reproduction and growth of submersed macrophytes are summarized. The role of differing environments is examined, indicating the extent of plastic responses in plant resource allocation. Lastly, the concept of cost/benefit analyses is applied to growth forms of submersed aquatic macrophytes. LIFE CYCLE STRATEGIES
Even though reproductive allocation is strongly affected by environmental conditions, certain trends can be identified among the basic reproductive strategies exhibited by submersed aquatic macrophytes. In this section, I will classify these basic strategies as either annual (A), overwintering strictly by seeds, or perennial, in which vegetative parts overwinter. The perennial strategies can be separated into those using a vegetative propagule for overwintering, such as a turion, tuber, or winter bud, designated as perennial herbaceous (Ph), and those which overwinter using vegetative, non-reproductive biomass designated as perennial overwintering (Po), or evergreen species. The relative advantages of sexual and asexual propagation are quite different. The associated costs of sexual propagation are generally higher than for asexual propagation, and require more specialized structures. Seeds are generally smaller than vegetative propagules, with a more resistant coating. Two obvious advantages of sexual propagation are that the propagules are more resistant to environmental stress than vegetative propagules, and sexual propagation allows for the recombination of genetic traits. Asexual propagules are less differentiated; in some instances they are merely stem fragments and require no specialized allocation. Vegetative propagules have larger reserves, allowing a more rapid initial growth phase. As the aquatic environment is buffered from extremes of the environment, vegetative propagules are generally sufficient to ensure overwintering. Data on the production of seeds and asexual propagules (e.g. tubers or tur-
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
69
ions) per unit area are presented in Table 1. Annual plants produce more seeds per unit area than either of the perennial types, apparently because seed production for annuals is the only means of overwintering. This higher production by annuals may be a function of higher seed production per stalk or a higher number of stalks per unit area. Perennial submersed macrophytes often produce few, if any, seeds. An interesting example of this within a single species is the marine macrophyte, Zostera marina L. Zostera marina may adopt the strategy of either an annual or a perennial, often in adjacent localities. Annual Z. marina produces seven times more seeds per unit area than perennial Z. marina (Keddy, 1987). Annual Z. marina optimizes biomass growth by allocation to structures associated with flowering, at the expense of vegetative structures, in comparison with perennial Z. marina. Although perennial species may produce some seeds, they produce as many as twice the number of vegetative propagules as seeds (Table 1 ). Overall, however, the number of seeds produced by annual species exceeds the number of asexual propagules produced by perennials by as much as two orders of magnitude. In Table 2, data on propagule dry weight and percent germination are presented. In general, the percentage of vegetative propagules achieving reproTABLE l
Propagule production as density (number per square meter) of seeds and asexual propagules for annual ( A ) , perennial herbaceous (Ph), and overwintering perennial (Po) submersed aquatic macrophytes Species
Lepilaena cylindrocarpa
Seed density
Asexual propagule density
(nm -2)
(nm -2)
A
99400
-
6
A
10696
-
7
A A Ph Ph Ph Ph Ph
799630 78000 1445 7000 1985 330 491
1129 544 358 75 322
7 3 4 7 7 2 7
Ph Ph Po Po Po
61 890 14200 11000
109 1963 510 -
7 6 1 5 3
A, Ph or Po
Ref.
(Koern. ex Walp. ) Benth.
Najas guadalupensis (Spreng.) Magn.
Zannichellia palustris L. Zostera marina L. Potamogeton crispus L. Potamogetonfoliosus Raf. Potamogeton nodosus Poir. Potamogeton pectinatus L. Potamogeton richardsonii (A. Benn. ) Rydb.
Potamogeton vaginatus Turcz. Ruppia polycarpa R. M a s o n Hydrilla verticillata (L.f.) Royle Lobelia dortmanna L. Zostera marina L.
~1, Bowes et al., 1979; 2, Kautsky, 1987; 3, Keddy, 1987; 4, Rogers and Breen, 1980; 5, Szmeja, 1987a,b; 6, Vollebergh and C o n g d o n , 1986; 7, Yeo, 1966.
70
J.D. MADSEN
TABLE 2
Propagule type, percentage germination, and weight (mg dry weight) for annual, herbaceous perennial and overwintering perennial submersed macrophytes Species
A, Ph or Po
Propagule type Percent Weight germination (mg DW)
Ref,
Lepilaena cylindrocarpa
A
Seed
12
(Koern. ex Walp.) Benth. Ruppia maritima L. Zannichellia major Boenn. Zannichellia palustris L. Hydrillaverticillata (L.f,) Royle 2 Hydrilla verticillata (L.f.) Royle 3 Potamogeton berchtoldii Fieber Potamogeton crispus L. Potamogeton crispus L. Potamogeton pectinatus L. Potamogeton pectinatus L. Ruppiapolycarpa R. Mason Ruppiapolycarpa R. Mason Lobelia dortmanna L. Myriophyllum spicatum L. Ruppia megacarpa R. Mason
A A A Ph Ph Ph Ph Ph Ph Ph Ph Ph Po Po Po
Seed Seed Seed Tuber Tuber Turion Turion Seed Tuber Seed Seed Turion Seed Seed Seed
85 12 56 100 88 100 45 60 0.001 100 8 35 65 80 69 27.8
0.120 66.66 35.55 11 5.045 0.011 56.2 0.510 1.225 0.6 -
1 10 10 8 8 6 5 3,5 7,11 11 12 12 9 4 2
t l, Agami and Waisel, 1988; 2, Brock, 1982; 3, Hunt and Lutz, 1959; 4, Madsen and Boylen, 1988; 5, Rogers and Breen, 1980; 6, Sastroutomo, 1981; 7, Spencer, 1986; 8, Steward and Van, 1987; 9, Szmeja, 1987a; 10, van Vierssen, 1982; 11, van Wijk, 1983; 12, Vollebergh and Congdon, 1986. 2Dioecious strain. 3Monoecious strain.
ductive success is higher than that of seeds. These observations could result from two different conditions: (i) although most vegetative propagules lack true dormancy (Bartley and Spence, 1987), seeds may have strong dormancy patterns (Agami and Waisel, 1988 ); ( ii ) vegetative propagules are one to two orders of magnitude larger than seeds, as measured by dry weight (Table 2), which confers higher possible propagule viability (Spencer, 1986). To compensate for these differences, seed production may be substantially greater than asexual propagule production, as noted in Table 1. The ecological functions of differing types of propagules must be considered to better understand the relative trade-off between sexual and asexual reproduction. For the perennial herbaceous macrophytes (Ph), seeds allow long-distance dispersal or long periods of dormancy, while asexual propagules are more suited to short-term dormancy (e.g. overwintering) or short-distance dispersal (van Wijk, 1983). Perennial species may then have a small, hardy seed for long-distance dispersal, and a large vegetative propagule for short-distance dispersal and overwintering. Annual macrophytes must utilize seeds for both purposes. For some species, such as Trapa natans L., the pro-
RESOURCEALLOCATIONAT THE INDIVIDUALPLANT LEVEL
71
TABLE 3
Biomass allocation (as a percentage of total dry weight) to sexual and asexual propagation and vegetative growth structures for submersed aquatic macrophytes of annual (A), perennial herbaceous (Ph), and perennial overwintering (Po) forms Species
Hydrilla verticillata
A, Ph or Po
Propagation
Vegetative
Sexual
Asexual Total
Shoot Root
Total
Ref.
Ph
-
40
40
60
-
60
8
A Po Ph Ph
29 7 < 1 -
42 27
29 7 42 27
51 41 52 54
20 52 6 19
71 93 58 73
10 6 5 7
Ph Ph Po
38 22 20
38 26 25
56 74 45
6
4 5
30
62 74 75
7 4 1
Ph Ph Ph Ph
2 21 13 4
66 3 21 34
68 24 34 38
26 54 51 20
6 22 15 42
32 76 66 62
3 1 10 1
Ph
< 1
25
26
61
13
74
9
Ph
10
22
32
61
7
68
2
(L.f.) Royle
Lepilaena cylindrocarpa (Koern. ex Walp.) Benth. Lobelia dortmanna L. Potamogeton crispus L. Potamogeton nodosus Poir. Potamogeton pectinatus L. Potamogeton pectinatus L.
Ruppia megacarpa R. Mason
Ruppia occidentalis Watson Ruppia polycarpa R. Mason Ruppia polycarpa R. Mason Ruppia tuberosa Davis & Tomlinson
Vallisneria americana Michx.
Vallisneria americana Michx.
~1, Brock, 1983; 2, Donnermeyer and Smart, 1985; 3, Husband and Hickman, 1985; Kautsky, 1987; 5, Kunii, 1982; 6, Moeller, 1978; 7, Spencer and Anderson, 1987; 8, Steward and Van, 1987; 9, Titus and Stephens, 1983; 10, Vollebergh and Congdon, 1986.
duction of a small number of large seeds may be adaptive by creating a large, highly viable propagule with large reserves for rapid spring growth. On the other hand, large numbers of small seeds (e.g. Zannichellia palustris L., Table 1) saturate the environment with propagules. The hardiness of seeds increases the probability of survival, particularly for long-term dormancy or long-distance dispersal. Overwintering perennials (Po) are also capable of perennation through their standing biomass, thus either negating the need for asexual propagules, or diminishing the need for specialized structures. For instance, Myriophyllum spicatum L. successfully utilizes stem fragments as an asexual means of short-distance dispersal. Allocation to reproduction varies greatly with extremes in environmental conditions, e.g. ranging from 5 to 42% of the total biomass for Potamogeton pectinatus L. depending on whether it is found in sheltered or partially exposed habitats (Kautsky, 1987). Under typical environmental conditions,
72
J.D. MADSEN
biomass allocation to propagation is quite consistent for annual and perennial submersed macrophytes (Table 3). Generally, 30% of total biomass is allocated to propagation of some form by annuals and herbaceous perennials (A, Ph), a figure consistent with observations made for both annual and perennial terrestrial plants (Fitter, 1986). The allocation between sexual and asexual forms of propagation varies between groups of submersed macrophytes. The one example in Table 3 of allocation to seed production in a true annual (A) indicates 29% of biomass allocated to sexual propagation. Both herbaceous and overwintering perennials allocated only 5%, on average, of total biomass to sexual propagation, with 25% or more of biomass allocated to asexual propagules. SEASONALITY OF ALLOCATION PATTERNS
For most perennial macrophytes, distinct seasonal cycles of carbon and nutrients are characteristic of overwintering strategies. Carbohydrate reserves are important to the overwintering and competitive ability of many macrophytes (Titus and Adams, 1979). A typical seasonal pattern for carbohydrate storage indicates high levels in spring, before intensive plant growth, followed by consumption and dilution of reserves through the early and mid growing season (Fig. 1 ). After active growth has ceased, the plant allocates fixed carbon to storage for overwintering. Although this pattern is from the simplest case in which the plant (Ceratophyllum demersum L. ) has neither roots nor specialized storage organs (Best and Visser, 1987 ), similar patterns are demonstrated for other species (Titus and Adams, 1979). Carbohydrate reserves are often laid down in overwintering stems; however, there is a greater storage efficiency in roots or modified stem tissue (such as tubers), where morphological and anatomical alterations increase the concentrations of carbohydrate reserves (Table 4). Although the production of .~.12 10"
o
86I
~
0
I
I
I
I
F
M
A
M J J A S MONTH OF THE YEAR
I
I
I
I
I
I
I
O
N
D
Fig. 1. Total reserved carbohydrates (as a percentage of dry weight) vs. month of the year for Ceratophyllum demersum (data from Best and Visser, 1987).
73
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
TABLE 4
Total non-structural carbohydrate (TNC) concentrations (as a percentage of dry weight) in tissues of submersed aquatic vascular plant species Species
Tissue
TNC (% DW cone. )
Ref. ~
Ceratophyllum demersum L. Myriophyllum spicatum L. Myriophyllum spicatum L. Potamogeton crispus L. Potamogeton crispus L. Vallisneria americana Michx. Vallisneria americana Michx. Vallisneria americana Michx.
Shoot Shoot Root Stem Turion Shoot Root Tuber
I1 20 20 17 40 15 28 46
1 3 3 2 2 3 3 3
]l, Best and Visser, 1987; 2, Kunii, 1989; 3, Titus and Adams, 1979. 300-
- 5O
0--0
SHOOT BIOMASS
E ] - - ' m BUD BIOMASS
I
I
-40 E
E
o 200. -30 o
-20 r~
N 100-
ffl 0.-..~~ 0
0 M
/
z
0
I
I
!
I
J
J
A S MONTH
I
I
0
N
0
Fig. 2. Shoot biomass and winter bud (tuber) biomass of Vallisneria americana for one growing season (data from Donnermeyer and Smart, 1985).
specialized structures allows for greater concentrations of stored carbohydrates, the lower biomass of these propagules relative to overwintering stems and roots may not compensate for this specialization if only total storage capacity is considered (Titus and Adams, 1979). However, the hardiness and dispersability of specialized propagules may confer other selective advantages. Production of propagules, as with production of reserve carbohydrates, follows a seasonal cycle. In general, propagule development follows the period of active biomass development (Fig. 2 ), and coincides with flower development and seed formation (Kunii, 1982; Donnermeyer and Smart, 1985 ). In many species, the propagule is the only overwintering portion of the plant. Active growth initiates from this propagule, until maximum biomass is approached. Either through environmental or physiological cues, the plant diverts energy and fixed carbon from biomass production to flower and seed production, and the formation of asexual propagules. Senescence follows,
74
J.D. M A D S E N
~-~ 6
0.4
TISSUE NUTRIENT CONCENTRATION o--o N
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P
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5
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o z
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NUTRIENT STANDING CROP N
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E
,0.1 o
0
I
I
I
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d
d
A MONTH OF 1988
S
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Fig. 3. Tissue concentration of nitrogen and phosphorus (as a percentage of dry weight), biomass (g dry weight m-2), and standing crop of nitrogen and phosphorus (g m-2) in the biomass of Myriophyllum spicatum (data from Madsen et al., 1989). 6 .~
'-,FLOWERING PLANTS 17-71 STERILE PLANTS
r" 0.5
FLOWERING PLANTS STERILE PLANTS
.0.4 3
~=4. .0.3
E3
.0.2
b_2" 0 Z
.0.1 o.
,0.0
LV
ST FL PLANTORGAN
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ST FL PLANTORGAN
R
Fig. 4. Nitrogen and phosphorus tissue concentrations in Lobelia dortmanna organs: LV, leaves; ST, stems; FL, floweringstalks; FR, fruits (data from Moeller, 1978). leaving only the seeds and asexual propagules to overwinter until the next growing season. Tissue concentrations of essential nutrients (e.g. phosphorus and nitrogen) follow similar patterns to those of reserve carbohydrates. Concentrations o f nutrients are typically high in the spring, before active growth. Plants often
RESOURCE ALLOCATION AT THE INDIVIDUAL PLANT LEVEL
75
contain high, 'luxury' levels of nutrients before active growth periods, either through continuous uptake or translocation to overwintering tissues. As growth initiates in the spring, uptake rates of nutrients typically lag behind growth rates of tissue, resulting in 'growth-dilution' of these nutrients (Fig. 3 ). Continued growth necessitates increased uptake rates of nutrients once critical tissue concentrations are approached. At this point, the total standing crop of nutrients within the tissue of the plants must increase to maintain critical concentrations in the plant. After maximum biomass is achieved and senescence of tissue begins, some nutrients may be translocated to overwintering tissues, resulting in higher concentrations in these tissues (Denny, 1980). However, the bulk of these nutrients usually is lost upon decomposition of senescing biomass. The distribution of nutrients within plant tissue is also a significant factor in the allocation of these resources. Photosynthetic tissues require higher levels of nitrogen, for the synthesis of photosynthetic enzymes, than root tissues. Reproductive tissues, seeds and asexual propagules, typically have higher concentrations of nutrients than most other tissues. For example, both sterile (non-flowering) and flowering plants of Lobelia dortmanna L. have been reported to have similar concentrations of nitrogen in leaf and stem material, with lower levels of nitrogen in the flowers (Moeller, 1978; Fig. 4). Fruits were higher in both nitrogen and phosphorus than leaf or stem material. The allocation of increased phosphorus to fruits may cause reduced availability of phosphorus to the vegetative tissues of flowering plants, as compared with sterile plants. It is clear that seasonal allocation patterns of both critical nutrients and carbohydrate reserves follow distinct patterns relative to the growth phases of aquatic plants, responding to environmental or physiological cues that create whole-plant changes. Allocation patterns vary seasonally both for the entire plant, and for individual organs throughout the year. ENVIRONMENT
Changing environmental factors may favor one species over another, or even cause the differential allocation of resources within a single species. For terrestrial plants, this has been observed for the effects of both shading and high winds, and for alterations in water supply or mineral nutrition (Fitter, 1986). For submersed macrophytes, incident light, stand density and selfshading influence allocation to stems and leaves (Duarte and Kalff, 1987). Leaf shape, size, and specific leaf area are influenced by plant depth and shading (Spence et al., 1973 ). Sediment chemistry, wave action, and other factors may also influence allocation patterns in submersed macrophytes.
76
J.D. MADSEN
Leaf shape and the environment Leaf form has often been cited as an adaptive feature in terrestrial plant ecology literature, such as the variation between sun and shade leaves (Fitter, 1986 ). However, little has been done to quantitatively examine leaf form in submersed macrophytes, though some work has been done on macroalgae (Koehl, 1986). The size, shape and number of leaves relate to resource allocation through the expenditure of energy and materials devoted to construct a more or less costly leaf, and their relative expected lifetime. For instance, the production of expensive, large leaves in environments where leaves may have a low life expectancy is a useless expenditure of necessary material. Leaf construction is a trade-off between maximizing photosynthetic area, and avoiding herbivory, stress (e.g. light or nutrient limitation) and disturbance (e.g. wave damage or drag) of these costly structures. Leaf size and shape may vary with environment within a given species. Leaves of Potamogeton pectinatus in still waters are short and fine, while those growing in streams are long and robust in appearance. Tubers ofP. pectinatus from stream populations, grown in still water cultures, will develop the fine leaves characteristic of lake populations (J.D. Madsen, personal observation, 1984). Genetically identical plants will exhibit differing phenotypes in response to water velocity with leaf shapes that are better adapted to the given flow conditions. Leaves of submersed macrophytes can be characterized as one of three groups: entire, dissected, and fenestrate (Sculthorpe, 1967 ). Although of various shapes, entire leaves are typically flattened and not broken into subcomponent leaflets. These leaves are typical of most monocotyledons, and some dicotyledons. Dissected leaves are usually composed of many fine, cylindrical leaflets. Dissected leaves are found only in dicotyledons. Fenestrate leaves have holes or 'windows' in an entire leaf blade, and are found only in some species within the Aponogetonaceae, a monocotyledonous family. A preliminary study of leaf shape and ecological adaptation involved examining data from herbarium specimens, literature sources, and photomicrographs (Madsen, 1986). Leaf type was differentiated into dissected, entire and fenestrate. As the latter form is rare, only dissected and entire leaves were analyzed in depth. By modeling leaf shapes based on simple hydrodynamic models, it was determined that in stagnant waters, dissected-leaved species had greatly reduced boundary-layer resistances, and might be favored under conditions of low flow where the acquisition of carbon and nutrients by diffusion would limit growth rates. However, under moderate flow rates with laminar flows, entire-leaved species were favored through inducing a turbulent boundary layer, thus greatly reducing diffusive barriers. Lastly, under high flows near the point at which turbulent flows would be expected, dis-
R E S O U R C E A L L O C A T I O N AT T H E I N D I V I D U A L P L A N T LEVEL
77
sected leaves are once more favored through reduced drag, hence less tearing and battering of leaf structure (Madsen, 1986). Using these model predictions, the composition of over 200 submersed macrophyte communities were examined for the percentage of entire-leaved and dissected-leaved species. As was expected from the models, streams and marine systems, with moderate, laminar flows dominating, had significantly higher percentages of species with entire leaves (98% and 100% median, respectively) than lake systems (median, 79%; Chi-square P = 0.0007; Fig. 5 ). In stream communities with areas of higher flow rates and turbulent flows, species with dissected leaves dominated. In contrast, marine systems are dominated by species with entire leaves, in part owing to the exclusive taxonomic grouping of seagrasses as monocotyledons, which do not have any species with dissected leaves. However, significant variation in leaf width occurs both within and between seagrass species and is an ecologically significant feature (Phillips and Lewis, 1983 ). Among lake communities, a trend was also noted (Fig. 5) of a high composition of species with entire leaves in oligotrophic systems (median, 94%), intermediate in mesotrophic communities (median, 80%), and lowest in eutrophic communities (median, 70%). The differences in the observed patterns were highly significant (Chi square P--0.0083). This pattern may be 20 15
7 ~
20 z 0
0 10 20 30 40 50 60 70 80 90100 PERCENTCLASSENTIRE 15
i1
80 10 20 ~0 40 50 6b io eo 90100 PERCENT CLASS ENTIRE
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EUTROPHIC LAKES
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0102030405060708090100
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Fig. 5. Percent classes of the macrophyte species composition composed of entire-leaved species vs. the number of cases observed for each percent class, for all lakes, oligotrophic lakes, mesotrophic lakes, eutrophic lakes, streams and marine communities. Data from Madsen, 1986.
78
J.D. MADSEN
interpreted as a gradient of reduced water m o v e m e n t from the low-growing communities in oligotrophic lakes, to the open heterogeneous canopies of mesotrophic lakes, and finally the extremely low current velocities of dense closed canopies, which are often monospecific, in eutrophic lakes. With decreased currents and increasingly dense canopies, diffusion-related processes become more limiting and enhance the adaptive value of dissected leaves (Madsen, 1986). Leaf shape is a significant adaptive feature for aquatic macrophytes, and should be studied further. Dissected leaves appear to be well suited to both stagnant water situations in being able to counteract diffusive resistance, and high flow situations, in being able to counteract the deleterious effects of drag. On the other hand, entire leaves are well suited to areas of moderate water movement, whether in open lake communities, marine communities, or moderate flow situations in streams, by inducing the formation of a turbulent boundary layer and thus greatly reducing diffusive resistance.
Growth form and environment One exceptionally interesting group of submersed macrophytes in terms of resource allocation patterns, is the isoetids. This group of morphologically similar but taxonomically unrelated plants shares the c o m m o n characteristics of evergreen leaves: low stature, a high root:shoot ratio, and low growth rates. Collectively, these characteristics have been interpreted to be adaptations to low-nutrient, low-productivity environments (Boston, 1986; Farmer and Spence, 1986 ), typical of a stress-tolerant species (Grime, 1977 ). Generally, isoetids predominate in waters low in nutrients and dissolved inorganic carbon (DIC). As is typical of terrestrial evergreen species in stressful environments, the isoetids have a low turnover rate which helps to conserve nutrients and carbon invested in leaf material (Table 5). For the most part, isoetid turnover rates are less than l, indicating that an individual leaf lasts more than a single year. Turnover rates for other species listed exceed one, demonstrating individual leaf lives of less than 6 months. Erect caulescent species, such as Potamogeton species forming a canopy, typically have higher turnover rates, in part due to self-shading of lower leaves during canopy development. Nonisoetid rosette species, such as Vallisneria species which have multiple elongated leaves arising from an underground stem, exhibit a range of turnover rates, in part from inhabiting high exposure sites, such as seagrass meadows, active wave zones, or streams. Isoetids in low-productivity environments maintain a low turnover rate to minimize the loss of limiting nutrients (Moeller, 1978 ) and carbon (Boston, 1986 ). Fertilization ofisoetids does not increase growth rates, compared with
RESOURCEALLOCATIONAT THE INDIVIDUALPLANTLEVEL
79
TABLE 5 Growth form, turnover rate (P/Bmax) and leaf weight (rag dry weight) for several macrophyte species Species
Growth form'
P/Bmax
Leaf wt. (mg DW)
Ref?
Myriophyllum spicatum L. Potamogeton pectinatus L. Ruppia cirrhosa (Petagna) Grande Isoetes macrospora Durieu Lobelia dortmanna L. Sparganium emersum Rehm. Zostera marina L.
C C C I I R R
3.8 2.01 2.5 0.85 0.69 2.3 2.5
2.32 52.1 1.56 5.8 2.5 60 140
1 4 3 2 5 6 7
~C, caulescent; I, isoetid; R, rosette. 21, Adams and McCracken, 1974; 2, Boston and Adams, 1986, 1987; 3, Kiorboe, 1980; 4, Madsen and Adams, 1988; 5, Moeller, 1978; 6, Nielsen et al., 1985; 7, Sand-Jensen, 1975.
other macrophyte species (Farmer and Spence, 1986), as is typical of all stresstolerators from low nutrient environments (Grime, 1977 ). In contrast, some macrophyte species from high productivity environments exhibit turnover rates of 2.5 or more, indicating a substantial loss of carbon and nutrients. Even with large leaves being lost, the productivity of the site enables higher turnover rates without stressing the availability of nutrients. Another interesting morphological adaptation of isoetids is the high root:shoot ratio. Although known to be important in the acquisition of nutrients, recent research also indicates that high allocation to roots relative to shoots is an important mode of DIC acquisition in low-productivity waters. The DIC levels of sediments in lakes where isoetids occur are 5-100 times higher than the overlying water column (Boston et al., 1987a,b). Therefore, these sediments supply a vastly superior source of DIC than the water column. Isoetids have developed the means to take up DIC from the sediments via the roots, and utilize the carbon in photosynthesis in the shoots. Isoetids acquire 60-99% of photosynthetic carbon from the sediment (Boston et ah, 1987a,b), in contrast to the less than _'.5% observed in non-isoetid species (Loczy et al., 1983 ). Some morphological adaptations that assist this process include a large root surface, internal lacunae for gas transport, and a thick cuticle over the leaves in some species (Boston et al., 1987a,b). Additionally, many isoetids have metabolic adaptations for nighttime carbon acquisition and reduced respiratory carbon loss (Boston and Adams, 1985, 1986). The root: shoot ratio of isoetids is substantially above that of both caulescent species and non-isoetid rosette species (Table 6). As substantial root uptake of DIC requires a high root:shoot ratio, this adaptation is unnecessary and counterproductive for a species not growing in low DIC waters. If suffi-
80
J.D. MADSEN
TABLE 6 Growth form, root:shoot ratio for dry weight ( R : S ) , and percentage of total carbon uptake from the
sediment via roots Species
Growth form ~
R: S
Percent C uptake (sediment)
Ref. 2
Lobelia dortmanna L. Littorella uniflora (L.)
I I
0.53 0.73
76-96 65-96
1 1
I I I C
0.79 1.03 1.29 0.05
60-96 85-98 89-99 0.3
1 1 1 2
C R
0.09 0.2
Aschers.
lsoetes macrospora Durieu Gratiola aurea Muhl. Eriocaulon septangulare With. Heteranthera dubia (Jacq.) MacMill.
Myriophyllum spicatum L. Vallisne?ia americana Michx.
0.1-1.0 1.4
2 2
]C, caulescent; I, isoetid; R, rosette. Zl, Boston et al., 1987a,b; 2, Loczy et al., 1983.
cient DIC is available in the water column, increased allocation to shoot material in non-isoetids allows increased photosynthesis and carbon uptake for enhanced productivity. C O S T / B E N E F I T ANALYSIS
With the application of optimization theory to ecology, many ecologists have examined the adaptiveness of costly plant structures or responses. One example of this investigation examines optimal leaf size using theoretical calculations of leaf functions under a variety of conditions (Parkhurst and
I .c
D
\
<>
0
0
E ,.n
0
o
~J~o o
-
o
0 0.0
I 0.5 RESPIRATION ( m g C
ISOETtO_ <> ROSETTE
I 1.0
1.5
g-1 h-l)
Fig. 6. Dark respiration vs. net photosynthetic rate ( b o t h in mg C g - L h - t ) for 22 species of submersed macrophytes.
RESOURCE ALLOCATION AT T H E I N D I V I D U A L PLANT LEVEL
8|
0 ISOET1D FLEXUOUS O CAULESCENT 0 ROSETTE []
zk
zx
E
0
en
Ix.
[]
O
O []
o
O o
[]
I~3 O
Az~
6)
D
[]
0 I
0.1
1.0
I
I
10.0 LEAF WEIGHT (rag)
100.0
Fig. 7. Leaf weight (rag) on a log scale vs. biomass turnover rate, P/Bm,~.
60 t, [] 0
ISOErlD FLEXUOUS CAULESCENT ROSETTE
4-
rlA
E ,.n 0.
°[3
O El
20
O
[] O
zx
O
D DD B
z~
%0
I I 10 100 ANNUAL PRODUCTIVITY ( g m - 2 y - l )
I 1000
Fig. 8. Annual productivity ( g m -2 y e a r - ~) on a log scale vs. turnover rate, P/Bma x.
"~ o
3025-
z
0 zx " [] '0'
ISOETID FLEXUOUS CAULESCENT ROSETTE
20.
z o
15.
~
10
~
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o
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I I I I 4 6 8 10 LEAF LIFE COST / UNIT WT. * DAY
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Fig. 9. The costs of leaves of different submersed macrophyte species per unit weight per day of expected leaf life, vs. potential production per unit weight per day averaged over the life of the leaf.
82
J.D. MADSEN
Loucks, 1972 ). An examination based on costs and benefits (or income) was performed for plant leaves under arid and semi-arid conditions examining predicted performance and costs of construction (Orians and Solbrig, 1977 ). Some examples of costs and benefits involved in leaf construction and function will be examined using data for 24 species collected from a variety of literature sources. An annotated bibliography of species examined, data collected, and literature sources is available from the author. Data on leaf size, photosynthetic and respiratory rates, plant turnover rates (P/nmax), and annual productivity were collected, with species categorized based on plant form: isoetid, flexuous species, in which the stem grows recumbent and the plants are generally poorly rooted, if at all (e.g. Ceratophyllum ); caulescent, in which the stem grows erect and rooted in the sediment (e.g. Potamogeton); nonisoetid rosettes (e.g. Fallisneria). The most basic of resource allocations to be made is to the photosynthetic enzymatic complex. The most abundant protein by weight in plant tissue is ribulose diphosphate carboxylase, the enzyme required to reduce carbon dioxide to organic carbon. However, allocation to a large photosynthetic apparatus with a large amount of photosynthetic enzymes requires an increase in basal metabolic respiration. In Fig. 6, the relationship between maximum net photosynthetic rate and dark respiration for each species is presented. This line indicates a threshold of a factor of three more than reported dark respiration. All points fall near this line or above, not below. Although the factor of three is empirical and arbitrary, net photosynthesis must of necessity be substantially higher than respiration. Net photosynthesis must accrue stored energy for dark-period respiration, non-photosynthetic tissue respiration, and future periods of low or no photosynthesis. High respiratory rates dictate the need for high net photosynthetic rates to support it, yet high metabolic rates are required for high productivity. Note that the group with low productivity, the isoetids, have both low respiratory rates and low photosynthetic rates, while the higher productivity rosettes display a much higher level of photosynthesis and respiration. Another important component of examining the costs and benefits of allocation to leaves is the longevity and size of the leaf. Leaf sizes range widely in submersed macrophytes, and broadly cover a range of life expectancies (the inverse of the turnover rate, P/Bmax). Low productivity plants, such as the isoetids, have leaves of an intermediate size with a low turnover rate (Fig. 7 ). The bimodal distribution of turnover rates with leaf size is related to annual productivity: the largest leaves are found on high productivity rosettes, with intermediate turnover rates, while the highest turnover rates are exhibited by high productivity plants with very small leaves. These small leaves, with low investment in carbon, are rapidly lost with the growth of the plant's canopy and resultant self-shading. Examples of these plants include Myriophyllum spicatum and Hydrilla verticillata (L.f.) Royle.
RESOURCEALLOCATIONATTHE INDIVIDUALPLANTLEVEL
83
Allocation patterns are also dictated by expected productivity. If plants have higher productivity rates, they can afford to allocate carbon to higher turnover leaves, while plants on a strict carbon budget cannot afford to waste any energy on leaves of short life (Fig. 8 ). Higher productivity allows the potential of higher turnover rates, but relatively moderate turnover rates may still be observed in plants of relatively high productivity. Note again that isoetids are among the lowest in both turnover rates and productivity. Utilizing data on leaf size, net photosynthetic and respiratory rates, percent carbon in leaf tissue, and turnover rates, the cost of construction and maintenance of leaves over their lifetime (per unit weight) and the expected productivity can be calculated for each species (Fig. 9). The values presented are standardized over the expected life of the leaf. The line indicates the hypothetical break-even point where production equals costs. Isoetids rank lowest for both productivity and costs. This is expected in low-productivity environments, resulting from long-lived leaves of moderate size, which have low overhead. Some other plants minimize associated costs by producing many small leaves with a high turnover rate. The small investment offsets the short life of the leaf itself. In this cost/income analysis of submersed macrophyte leaves, I have shown some preliminary indications of how different types of submersed macrophyte species adapt to varying demands from the environment. Low productivity species, such as the isoetids, have a low-overhead, low-gain strategy. The leaves produced are of intermediate size, but are long lived and metabolically inexpensive. High-productivity species fall into two types: some produce many small leaves with a very high turnover (such as some caulescent species), while others produce large leaves of intermediate turnover rates (e.g. rosette species). In general, turnover rate increases with productivity rate. Also, the expected production of a leaf over its lifetime equals or exceeds the expected cost of the leaf. The study of resource allocation in submersed macrophytes has been tangential, at best. The potential exists for expanding our understanding of submersed macrophyte ecology, especially when combined with studies of limiting factors and methods of plant propagation.
REFERENCES Adams, M.S. and McCracken, M.D., 1974. Seasonal production of the Myriophyllum component of the littoral of Lake Wingra, Wisconsin. J. Ecol., 62: 457-467. Agami, M. and Waisel, Y., 1988. The role offish in distribution and germination of seeds of the submerged macrophytes Najas marina L. and Ruppia maritima L. Oecologia, 76: 83-88. Bartley, M.R. and Spence, D.H.N., 1987. Dormancy and propagation in helophytes and hydrophytes. Arch. Hydrobiol. Beih., 27:139-155. Best, E.P.H. and Visser, H.W.C., 1987. Seasonal growth of the submerged macrophyte Cerato.
84
J.D. MADSEN
phyllum demersum L. in mesotrophic Lake Vechten in relation to insolation, temperature and reserve carbohydrates. Hydrobiologia, 148: 231-243. Boston, H.L.,1986. A discussion of the adaptations for carbon acquisition in relation to the growth strategy of aquatic isoetids. Aquat. Bot., 26: 259-270. Boston, H.L. and Adams, M.S., 1985. Seasonal diurnal acid rhythms in two aquatic crassulacean acid metabolism plants. Oecologia, 65: 573-579. Boston, H.L. and Adams, M.S., 1986. The contribution of crassulacean acid metabolism to the annual productivity of two aquatic vascular plants. Oecologia, 68:615-622. Boston, H.L. and Adams, M.S., 1987. Productivity, growth, and photosynthesis of two small "isoetid" plants, Littorella uniflora and Isoetes macrospora. J. Ecol., 75: 333-350. Boston, H.L., Adams, M.S. and Pienkowski, T.P., 1987a. Models of the use of root-zone CO2 by selected North American isoetids. Ann. Bot., 60: 495-503. Boston, H.L., Adams, M.S. and Pienkowski, T.P., 1987b. Utilization of sediment CO2 by selected North American isoetids. Ann. Bot., 60: 485-494. Bowes, G., Holaday, A.S. and Haller, W.T., 1979. Seasonal variation in the biomass, tuber density, and photosynthetic metabolism of Hydrilla in three Florida lakes. J. Aquat. Plant Manage., 17: 61-65. Brock, M.A., 1982. Biology of the salinity tolerant genus Ruppia L. in saline lakes in south Australia II. Population ecology and reproductive biology. Aquat. Bot., 13: 249-268. Brock, M.A., 1983. Reproductive allocation in annual and perennial species of the submersed aquatic halophyte Ruppia. J. Ecol., 71: 811-818. Denny, P., 1980. Solute movement in submerged angiosperms. Biol Rev., 55: 65-92. Donnermeyer, G.N. and Smart, M.M., 1985. The biomass and nutritive potential of Vallisneria americana Michx. in navigation pool 9 of the upper Mississippi River. Aquat. Bot., 22: 3344. Duarte, C.M. and Kalff, J., 1987. Weight-density relationships in submerged macrophytes: the importance of light and plant geometry. Oecologia, 72:612-617. Farmer, A.M. and Spence, D.H.N., 1986. The growth strategies and distribution of isoetids in Scottish freshwater lochs. Aquat. Bot., 26: 247-258. Fitter, A.H., 1986. Acquisition and utilization of resources. In: M.J. Crawley (Editor), Plant Ecology, Chap. 12, Blackwell Scientific Publications, Oxford, pp. 375-405. Grime, J.P., 1977. Plant Strategies and Vegetation Processes. Wiley, New York, 222 pp. Hunt, G.S. and Lutz, R.W., 1959. Seed production by curly-leaved pondweed and its significance to waterfowl. J. Wildl. Manage., 23: 405-408. Husband, B.C. and Hickman, M., 1985. Growth and biomass allocation ofRuppia occidentalis in three lakes, differing in salinity. Can. J. Bot., 63: 2004-2014. Kautsky, L., 1987. Life-cycles of three populations of Potamogeton pectinatus L. at different degrees of wave exposure in the Asko area, northern Baltic proper. Aquat. Bot., 27:177-186. Keddy, C.J., 1987. Reproduction of annual eelgrass: variation among habitats and comparison with perennial eelgrass (Zostera marina L.). Aquat. Bot., 27: 243-256. Kiorboe, T., 1980. Production of Ruppia cirrhosa (Petagna) Grande in mixed beds in Ringkobing Fjord (Denmark). Aquat. Bot., 9:135-143. Koehl, M.A.R., 1986. Seaweeds in moving water: form and mechanical function. In: T. Givnish (Editor), On Plant Form and Function, Chap. 18. Cambridge University Press, London, pp. 603-634. Kunii, H., 1982. Life cycle and growth of Potamogeton crispus L. in a shallow pond, Ojaga-ike. Bot. Mag. Tokyo, 95: 109-124. Kunii, H., 1989. Continuous growth and clump maintenance ofPotamogeton crispus L. in Narutoh River, Japan. Aquat. Bot., 33:13-26. Loczy, S., Carignan, R. and Planas, D., 1983. The role of roots in carbon uptake by the sub-
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