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Ecology |
Department of Biological Sciences, Binghamton University, Binghamton, New York 13902 USA
Received for publication November 14, 2000. Accepted for publication March 22, 2001.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: amphibious plants • aquatic plants • floating leaves • heterophylly • Nuphar • Nymphaeaceae • plasticity • submersed leaves
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), may result from a rigid developmental program in which juvenile leaves are distinct from adult leaves (heteroblastic development; Briggs and Walters, 1984
; Kerstetter and Poethig, 1998
) or, at the other extreme, from plastic plant responses to sharply varying environmental regimes prevailing at different times and/or for different regions of the same plant. Amphibious plants, those with both submersed and floating or aerial leaves, have long been subjects of investigations on heterophylly (Arber, 1920
; Sculthorpe, 1967
; Hutchinson, 1975
). These plants typically are confronted with abruptly different microenvironments—air and water—that contrast strikingly as media for plant life (Maberly and Spence, 1989
; Denny, 1993
), and heterophylly in amphibious plants is thought to be a means of contending with this environmental variation. For example, the cuticle of floating or aerial leaves affords a regulation of water loss that is unnecessary for submersed leaves, which typically have poor cuticle development. Also, floating leaves are likely to have greater access to CO2 for photosynthesis than are submersed leaves because the diffusivity of CO2 is several orders of magnitude greater in air than water, and because near-leaf fluid depleted in CO2 (i.e., due to CO2 uptake) is more readily replaced in air due to its much lower dynamic viscosity (Denny, 1993
). Submersed leaves in heterophyllous plants are typically thinner or more dissected, traits that help counter the lower availability of CO2 in water (Sculthorpe, 1967
).
Among aquatic plants with plastic developmental responses to environmental variation, some produce different leaf types from meristems exposed to underwater vs. aerial environments (e.g., Ranunculus aquatilis, at least within some photoperiodic constraints; Cook, 1969
). Similarly, others first develop floating or aerial leaves while still underwater, as the plant grows up through the water column and is exposed to conditions typically indicating the proximity of the surface, such as low red : far red ratios (e.g., Bodkin, Spence, and Weeks, 1980
) and high flux densities of blue light (e.g., Lin and Yang, 1999
). Abscisic and giberellic acids may mediate morphogenic responses to external environmental conditions (Anderson, 1978, 1982
; Kane and Albert, 1983
; but see Lin and Yang, 1999
). Still other plants, for example the water fern Marsilea (Allsopp, 1965
), appear to develop aerial leaves in response to internal nutrient status: those plants that garner more resources develop larger meristems, along with a greater potential to produce floating or aerial leaves (Allsopp, 1965, 1967
).
The primary goal of this research was to test the effect of essentially natural variations in environmental conditions on leaf types developed by Nuphar variegata Durand (the yellow waterlily). This inquiry was driven by our field observations of a population of this Nuphar species with abundant submersed leaves—quite atypical in our experience. The site, Otselic Pond, is naturally acidic (pH 
4.7), with high CO2 concentrations (
70–100 µmol/L) and highly organic, loosely consolidated sediment. While we are most interested in identifying conditions favoring submersed leaf development, we frame our hypotheses below in terms of floating leaf development. This is because floating leaf production represents a developmental switch, both in the normal ontogeny of these plants, which begin life with submersed leaves, and for our experimental plants, which also initially had only submersed leaves.
Our first hypothesis is that more fertile natural sediments, i.e., those with greater availability of ammonium and/or phosphate, promote greater development of floating leaves than less fertile sediments. The premise is that greater resource availability promotes growth and development, including that of the potentially costlier floating leaves. The few reports on the effects of mineral nutrition on morphogenesis in heterophyllous plants that have appeared are conflicting. For example, Edwards and Allsopp (1956)
found that lower nutrient levels favored juvenile leaves in Marsilea, whereas Njoku (1957)
determined that nutrient excess favored more juvenile leaf traits in Ipomoea. Our hypothesis is more consistent with Edwards and Allsopp (1956)
.
Our second hypothesis is that relatively low [CO2] favors the development of floating leaves over submersed leaves. This is consistent with our field observations of abundant submersed leaves in a high CO2 pond, and perhaps with Bristow and Looi (1968)
and Bristow (1969)
, who reported that high [CO2] favored the development of water leaf traits in three amphibious species. The following alternative hypothesis, however, also seems reasonable: CO2 enrichment promotes the development of floating leaves, much as hypothesized for mineral resources in more fertile sediments, i.e., simply because it represents greater resource availability and thus accelerates growth and development.
Our third primary hypothesis is that shallower water favors the development of floating leaves. Depth is a complex gradient (Spence, 1982
), but a key component of it is that light availability decreases with increasing depth. Past literature has reported that low light favors submersed leaves in several taxa (Sculthorpe, 1967
). This is consistent with our secondary hypothesis that the cost of producing floating leaves, as indicated by mean leaf biomass, should be greater for plants at greater depth, if for no other reason than that petioles must be longer to reach the surface. A corollary is that the cost of producing floating leaves in shallow water, which we expect to be greater than the cost of producing the thinner, shorter-petioled submersed leaves at the same depth, can more readily be met by the benefit of the ensuing greater CO2 availability to floating leaves. For a potentially heterophyllous plant such as Nuphar variegata, then, depth influences access to atmospheric CO2 as well as light availability.
The effects of sediment type, [CO2], and depth on floating vs. submersed leaf production are the primary foci of this study. In addition, our experiments afforded us the opportunity to test secondary hypotheses on mean leaf mass and to characterize the seasonal timing of leaf development under controlled conditions.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). It is typically considered a floating-leaved macrophyte with few or no submersed leaves (e.g., Gleason and Cronquist, 1991
), but underwater seedlings produce submersed leaves before any floating leaves appear (in this paper, we use "underwater" to refer to microhabitat and "submersed" to refer to leaf type). There is thus a strong ontogenetic component over the plant's lifetime to heterophylly in this species. There also appears to be a strong seasonal component: in the source population for these experiments, most if not all plants have only submersed leaves prior to floating-leaf development in spring and after floating-leaf senescence in fall.
Submersed leaves in Nuphar are flaccid, appreciably thinner than floating leaves, and translucent with wavy margins, little cuticle development, and no stomata (Sculthorpe, 1967
), all in contrast to the more rigid floating leaves with well-developed cuticle and stomata on adaxial surfaces. Floating leaves may have greater rates of CO2 fixation due to the presumed greater availability of CO2 in air cited above, although free CO2 concentrations well above saturation in Otselic Pond, the site for the source population used in this study, may serve to counter this pattern (Frost-Christensen and Sand-Jensen, 1995
). A second potential benefit of floating leaves is increased light availability, perhaps especially in Otselic Pond, where submersed leaves are often densely covered by filamentous algae by midsummer (J. E. Titus, personal observations). A third benefit in this species is pressurized ventilation (Dacey, 1980
), a mechanism by which O2 is transported from floating leaves into rhizomes lying in anaerobic sediments. A possible detriment of floating leaves, in addition to the expected greater costs of leaf construction, is that they may be subject to greater herbivory in some Nuphar populations (Kouki, 1993
). Herbivory on submersed leaves, however, as well as on floating leaves before they reach the surface, is just as evident in Otselic Pond as is herbivory on floating leaves (J. E. Titus, personal observations). Further, Cronin, Wissing, and Lodge (1998)
reported greater herbivory on submersed than floating leaves in another Nuphar variegata population.
Only natural lake sediments were used. In experiment 1 (see Experimental Design below), we used sediment collected from alkaline Otsego Lake (Otsego County, New York, USA) and anthropogenically acidified (Charles, 1984
) Big Moose Lake (Hamilton County, New York, USA) because we knew the former had significantly higher bulk density and lower organic content (Table 1), both indirect indicators of greater fertility in nonsandy sediments (Barko and Smart, 1986
). In confirmation, porewater [NH4+] and soluble reactive phosphate (SRP) concentrations were fivefold and 3.5-fold higher, respectively, in Otsego sediment (Table 1). We measured NH4+ because little if any nitrate is expected in typically anaerobic lake sediments. All differences between these two sediments were statistically significant (Titus, 1992
).
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), was far lower (P < 0.0001). Porewater SRP concentrations were far greater (Table 1; P < 0.001), but [NH4+] values did not differ significantly in Chenango vs. Otselic sediment. Thus, the first pair of sediments differed significantly in both [NH4+] and [SRP], while the second pair differed significantly only in [SRP].
Experimental design
Experiment 1
To test the hypothesis that greater sediment fertility promotes the development of floating leaves, 24 field-collected Nuphar plants with only submersed leaves were sorted into six size classes to control for possible size effects on floating leaf development (subsequent analysis showed that size class had no significant effect on floating leaf production). For each size class, the four similar plants were blindly assigned to the two sediment types (less fertile Big Moose and more fertile Otsego), with one per sediment type in each of two replicate greenhouse tanks. We treated this as a randomized complete block design, with sediment type as the treatment of interest and tank as the block. All of these plants were grown at the same [CO2] and at the same depth.
Experiment 2
To evaluate the effects of free [CO2] and to retest the effect of sediment type on submersed leaf development, 40 field-collected Nuphar plants with only submersed leaves were separated into five size classes based on initial fresh mass. The eight plants in each class were randomly assigned to native (Otselic) vs. alkaline lake (Chenango) sediment and to low vs. high [CO2] treatments. Each of the two tanks randomly assigned to each CO2 level contained a representative of each initial size class on each sediment type, for a total of ten pots per tank in a nested (tank within [CO2]), split-plot (sediment type within each tank) design. All of these plants were grown at the same depth.
Experiment 3
To test the hypothesis that greater depth favors submersed leaf development and increases the cost of leaf construction (and to retest free [CO2] influences on submersed leaf development), the same nested, split-plot design as used in experiment 2 was followed, except that water depth rather than sediment type was varied within each tank. All of these plants were grown on the same alkaline lake (Chenango) sediment.
Experiments 2 and 3 were run simultaneously and had in common the set of plants on alkaline lake sediment in "deep" water, so that each tank contained a total of 15 plants: five were placed deep after planting in native acidic pond sediment, five deep on alkaline lake sediment, and five shallow on alkaline lake sediment.
Planting, environmental control, data collection, and harvesting
For all three experiments, small Nuphar plants with roots and rhizomes intact and with only submersed leaves were collected from Otselic Pond and transplanted 2–3 cm deep into sediment 15 cm deep in 16-cm (top diameter) plastic pots. They were immersed in a culture solution containing 0.315 mmol/L CaCl2, 0.075 mmol/L KHCO3, and 0.14 mmol/L MgSO4, modified from Smart and Barko (1985)
, within 1200-L fiberglass tanks in the Binghamton University Research Greenhouse. Horizon 5997 pH controllers (Cole Parmer Instruments, Vernon Hills, Illinois, USA) maintained pH at 5.0 ± 0.2 units by automatic dropwise addition of 0.4 mol/L HCl when pH rose above 5.2; 0.4 mol/L NaOH was added manually if pH declined below 4.8. At pH 5 and 23°C, 96% of the inorganic carbon present is in the form of free CO2, with the remainder present as HCO3–. Remcor CFF-500 refrigerated circulators (Remcor Products, Franklin Park, Illinois, USA) controlled water temperature at 23 ± 2°C and, along with bubbling compressed air streams, provided continuous mixing. Monitoring included daily temperature and pH measures as a check on circulators and pH controllers and occasional specific conductance measures with a Radiometer CDM 80 conductivity meter (Radiometer America, Westlake, Ohio, USA). Specific conductance remained below 400 µS/cm in all experiments.
Experiment 1
Plants were collected on 6 June 1994 and transplanted later that day into either Big Moose or Otsego (more fertile) sediment. Tank water depth, initially 45 cm above plant bases, was raised to 70 cm above plant bases on day 16 of the experiment—before any floating leaf development was evident—to more closely approximate the depth from which plants were collected. Tanks were covered with a layer of neutral density shadecloth (Lumite 25; Chicopee, Cornelia, Georgia, USA), which reduced incident quantum flux density by about one-third. Counts of submersed and floating leaves for each plant were made on days 3, 18, 22, 49, 67, and 94.
Experiments 2 and 3
Plants were collected on 1 June 1995. Initial leaf counts were made on 2 June (day 0), and plants were transplanted on 3 June. Each intact plant was gently shaken, but not blotted, prior to fresh mass measurement. The five initial fresh mass classes were 1.8–2.2 g, 2.3–2.7 g, 2.8–3.3 g, 3.5–4.3 g, and 4.3–6.3 g. Tank water depth was 70 cm above the sediment for the 20 plants in Otselic sediment and for half of the 40 plants in Chenango sediment. The remaining 20 Chenango sediment plants were raised on plastic crates to a depth of 35 cm. The plants grown at 70 cm on Chenango sediment were shared between the two experiments. Tanks were randomly assigned to CO2 levels, with two at low [CO2] (in equilibrium with an unenriched, bubbling airstream) and two at high [CO2] (enriched due to higher [CO2] in the bubbling airstream as controlled by a Tylan FC-280 mass flow controller with an RO-28 control unit [Tylan, Carson, California, USA]). Mean CO2 level, as determined by regular monitoring of tank water samples for total dissolved inorganic carbon with infrared gas analysis (Model 225 Mk II gas analyzer, Analytical Development, Hertfordshire, UK; Hewlett-Packard 3390A Integrator, Hewlett-Packard, Avondale, Pennsylvania, USA), was 20 µmol/L CO2 for low CO2 tanks and 125 µmol/L CO2 for high CO2 tanks.
On days 8, 23, 37, 51, 66, 81, 94, and 110 of the experiment, all new submersed and floating leaves produced since the previous sampling were distinguished, tagged with a short section of clear vinyl tubing around the petiole, and tallied. With correction for the length of the prior interval between leaf censuses, these tallies were converted to rates of new leaf production per week. Plants were harvested on day 110 (20 September), rinsed carefully, and shaken before final fresh mass and leaf lengths were measured, and dry mass was determined separately for roots, rhizomes, submersed leaves, and floating leaves after drying at 85°C. For each plant, the mean dry mass per leaf was determined for each leaf type present at harvest. The mean of these means was compared statistically.
Statistical analysis
For some of the leaf count data in all three experiments (especially number of floating leaves and the ratio of floating leaves to total leaf number), marked nonnormality occurred (P < 0.001 for the Shapiro-Wilk statistic determined using SAS PROC UNIVARIATE; SAS Institute, 1990
) and could not be remedied with data transformations. We therefore used Friedman's nonparametric test (Zar, 1984
) for the two-way, randomized complete block design of experiment 1, and Zar's (1984)
extension of Kruskal-Wallis nonparametric ANOVA (analysis of variance) for the nested, split-plot design of experiments 2 and 3. In both cases, analyses were based on midsummer leaf census data because the maximum development of floating leaves occurred then (see below).
To gauge differences in the time passing before floating leaves were first produced in low- vs. high-[CO2] grown plants, the number of intervals between leaf censuses without floating leaves for all plants in experiments 2 and 3 combined were compared (via a 
2 test). Mean leaf dry mass for submersed vs. floating leaves grown in low vs. high [CO2] was compared via parametric two-way analysis of variance. These two-way (leaf type x [CO2]) leaf mass data were first log-transformed (without first adding 1) because we wished to test the a posteriori interaction hypothesis that the effect of [CO2] on mean leaf mass was proportionally the same for submersed and floating leaves. This null hypothesis is supported if the differences between the mean of log-transformed leaf mass are the same at both CO2 levels.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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6 at the maximum on day 49 (25 July) in both treatments (Fig. 1), then declined. Floating leaves, absent on day 18, were first tallied on day 22 (28 June) for plants on both sediments, were most abundant in midsummer, and were clearly much more abundant on plants grown on the richer Otsego Lake sediment (Fig. 1b vs. 1a). The total number of leaves present increased by means of 2.8 and 5.4 leaves/plant on Big Moose and Otsego sediment, respectively, before declining after midsummer.
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The time elapsed before the production of the first floating leaf was significantly less in low CO2-grown plants (2.2 vs. 3.8 census intervals; 2 = 25.6; P < 0.001 for 7 df): 57% of low CO2-grown plants produced their first floating leaf before any high CO2-grown plants produced a floating leaf. This lag is evident in Fig. 6d, e, and f.
Experiments 2 and 3: mean leaf mass
The cost of producing a leaf, as measured by mean leaf biomass, is several-fold greater for floating leaves than for submersed leaves regardless of [CO2] and at high [CO2] increases 88% for submersed leaves, but only 13% for floating leaves (Fig. 7a). Parametric ANOVA results from testing log-transformed leaf mass data were as follows: F1,70 for main effects of leaf type = 92.1 (P < 0.001); F1,70 for main effects of [CO2] = 8.51 (P < 0.01); and F1,70 for the leaf type x [CO2] interaction = 6.36 (P < 0.05). That is, the proportional effect of CO2 enrichment on mean leaf mass is significantly greater for submersed leaves. Indeed, according to Tukey's means comparison test, the [CO2] effect is significant (P < 0.05) for submersed leaves, but not for floating leaves (Fig. 7a).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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It is possible that nitrogen availability is of particular importance to the development of floating leaves. This could account for the significant sediment effect in experiment 1, in which porewater [NH4+] was fivefold greater in the sediment yielding more floating leaves, and the lack thereof in experiment 2 (Fig. 3), in which porewater [NH4+] did not differ significantly between the two sediments. More direct manipulation of NH4+ availability would be needed to test this hypothesis. Phosphate availability, at least as measured by porewater [SRP], is not so clearly correlated with floating leaf production in this study. We conclude that sediment type may have a pronounced effect on floating leaf production, as it did in experiment 1, but also that even very different sediments may yield similar patterns (experiment 2).
There is a hint of a different sediment effect in experiment 2, namely the lag between the early season peak of new submersed leaf production on native acidic pond sediment vs. alkaline lake sediment (Fig. 6c vs. 6a and b). This may reflect time required for acclimation to a foreign sediment. Overall, however, the transplanted Nuphar plants and their roots appear to have made a ready adjustment to a very different sediment type in this experiment.
Heterophylly and [CO2]
Our most consistent effect on leaf type arose from the two CO2 enrichment tests (experiments 2 and 3). High [CO2] stimulated submersed leaf development and disfavored floating leaf development, in both absolute and relative terms (Figs. 3, 4, 6). Further, low CO2-grown plants showed a strong tendency to produce floating leaves sooner. Our data favor the argument that morphogenesis in Nuphar variegata is sensitive to the vertical distribution of CO2 availability in its natural habitat. This is in a sense analogous to the "foraging" of root systems with local proliferation in zones of high resource availability (Hutchings and de Kroon, 1994
). Aside from its effects on morphogenesis, CO2 enrichment appears to favor greater allocation to individual submersed leaves, although not to individual floating leaves (Fig. 7a). This, too, could effect a greater exploitation of high dissolved free CO2 and helps account for the greater growth rate of CO2-enriched plants (J. E. Titus, unpublished data) despite insignificant (Fig. 3c; Table 3a) or slight (Fig. 4c; Table 3b) changes in total new leaf production.
Our findings are consistent to a degree with those of Bristow and Looi (1968)
and Bristow (1969)
. They reported that high [CO2] favored the development of submersed-type leaves in three species, but their plants were grown in air with far higher levels of CO2—their lowest level of CO2 enrichment was 0.65%, or >20 times ambient levels used in their experiment, and their highest was 50%. They believed, however, that the source stream for one of their experimental plant populations had a free [CO2] as high as 280 µM, or 20 times the level expected for water in equilibrium with the atmosphere, so that morphogenesis in that stream could be influenced by the relatively high [CO2]. It is difficult to compare the availabilities of CO2 in air and water when at essentially the same volumetric concentration because of the great differences in gas diffusivity and mass flow regimes, but we reach the same conclusion: natural systems exist with high enough free [CO2] (see also Titus, Feldman, and Grisé, 1990
; Cole et al., 1994
) to influence the determination of leaf type.
Heterophylly and depth
Testing the effect of depth yielded mixed results: there was no significant effect of depth on midsummer leaf count data (Fig. 4; Table 3b), but later in the season, the percentage of plants with floating leaves was significantly greater for plants grown in shallower water (Fig. 5). The corollary that deeper water favors submersed leaves is an intuitively comfortable notion because floating leaves are more costly to produce in deeper water than in shallower water (Fig. 7b), and floating leaves are more costly to produce than submersed leaves (Fig. 7a). This is consistent with the classic pattern of zonation among species, with floating-leaved plants typically dominant in shallower water and submersed macrophytes in deeper water (Sculthorpe, 1967
; Spence, 1982
), presumably because the benefits of floating leaves are outweighed by increasing costs as depth increases.
In any factorial experiment, the levels chosen for each factor may influence the outcome. A depth difference >35 cm (35 vs. 70 cm) might have had a greater impact on plant developmental pattern, but our experimental options were restricted by tank dimensions. These depths, however, represent an ecologically meaningful range for Otselic Pond, much of which is 70–80 cm deep, but drops 20–30 cm in a drought year such as 1999 (J. E. Titus, personal observations).
We note that the prevailing conditions in Otselic Pond in nondrought years, i.e., Otselic Pond sediment as the substrate, relatively great depth, and high free [CO2], all tend to favor submersed leaf development, albeit not strongly so in the case of sediment and depth effects.
Rates and seasonal patterns of leaf production
The seasonal patterns of submersed vs. floating leaf production are not markedly different among the three sediment x depth combinations (Fig. 6). They are a rough match to the pattern described for floating leaves of Nuphar lutea in Finland by Kouki (1991)
: there, floating leaf development began soon after ice thaw in midspring, remained near 1.5 new floating leaves·plant–1·wk–1 until early July, then gradually declined to zero by late August. We observed substantially lower rates of new floating leaf production, with a maximum rate of only 0.4 new floating leaves·plant–1·wk–1 and 0.7 total new leaves·plant–1·wk–1. Perhaps our relatively small plants (1.8–6.3 g initial fresh mass) with a history of growth in a relatively infertile acidic bog pond did not have the resources to support greater rates of leaf production.
Photoperiod, which was essentially natural for our experimental plants in the greenhouse, may have been a trigger for the seasonal shift from producing floating leaves in midsummer to submersed leaves in late summer. Wallenstein and Albert (1963)
, Cook (1969)
, and Kane and Albert (1983)
showed that short days tend to favor submersed leaf development and long days tend to favor aerial leaf development in two heterophyllous species. For our data, however, the wide variation in the date by which this "reversion" occurred (from 23 July to 20 September) suggests a weak control by photoperiod, or perhaps an alternative mechanism such as energy limitation when daylength shortens and photosynthetically active radiation is reduced. The more costly floating leaves are produced when light is most available. Whatever the mechanism, floating leaves are eventually frozen as ice forms on the water surface in late fall, if they do not decay first, so that continued development of floating leaves into the fall at northern latitudes is unlikely to realize a net gain for the plant.
How might the type of heterophylly exhibited by this Nuphar population be characterized? Hutchinson (1975, p. 159) credited internal factors for the switch from submersed to floating leaves in the "very simple kind of heterophylly" that exists in Nuphar. There is an element of heteroblastic development, but there is clearly not a rigid pattern from juvenile, submersed leaves to adult, floating leaves. First, many of the submersed leaves observed in situ, whether before or after floating leaves on a seasonal basis, are sizable and cannot be considered to be juvenile leaves. Second, the great majority of plants that produced floating leaves in this study reverted to submersed leaf production by late summer, paralleling the apparent pattern for Otselic Pond plants. Contrary to Sculthorpe's (1967, p. 223) assertion, heterophylly is not confined to seedling stages or early season growth. Third, there is clearly an element of plasticity as shown by the environmental sensitivity of leaf developmental patterns in this study and as shown for the closely related Nuphar lutea by Kouki (1993)
. While some of the conditions that favor submersed leaves (less fertile sediment, greater depth) might be thought to reflect a depletion of internal plant resources available to meristems, and thus limit the development of costlier floating leaves, the effects of CO2 enrichment cannot be regarded in this way; in this case, greater rather than lesser resource availability promotes submersed leaf development. However typified, the flexible pattern of leaf development exemplified by this Nuphar variegata population appears to facilitate effective exploitation of the vertical distribution of CO2 in aqueous vs. aerial microenvironments.
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FOOTNOTES |
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2 Author for reprint requests (tel: 607-777-2445, FAX: 607-777-6521, jtitus{at}binghamton.edu
).
3 Current address: The Wetlands Initiative, Suite 1015, 53 West Jackson Boulevard, Chicago, Illinois 60604 USA.
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Allsopp A. 1965 Land and water forms: physiological aspects. In W. Ruhland [ed.], Handbuch der Pflanzenphysiologie, vol. XV, 1, 1236–1255. Springer-Verlag, Berlin, Germany
———. 1967 Heteroblastic development in vascular plants. Advances in Morphogenesis 6: 127-171[Medline]
Anderson L. W. J. 1978 Abscisic acid induces formation of floating leaves in the heterophyllous aquatic angiosperm Potamogeton nodosus. Science 201: 1135-1138
———. 1982 Effects of abscisic acid on growth and leaf development in American pondweed (Potamogeton nodosus Poir.). Aquatic Botany 13: 29-44
Arber A. 1920 Water plants: a study of aquatic angiosperms. Cambridge University Press, Cambridge, England
Barko J. W. R. M. Smart 1986 Sediment-related mechanisms of growth limitation in submersed macrophytes. Ecology 67: 1328-1340[CrossRef][ISI]
Bodkin P. C. D. H. N. Spence D. C. Weeks 1980 Photoreversible control of heterophylly in Hippuris vulgaris L. New Phytologist 84: 533-542[CrossRef][ISI]
Briggs D. S. M. Walters 1984 Plant variation and evolution, 2nd ed. Cambridge University Press, Cambridge, UK
Bristow J. M. 1969 The effects of carbon dioxide on the growth and development of amphibious plants. Canadian Journal of Botany 47: 1803-1807
———, and A-S. Looi 1968 Effects of carbon dioxide on the growth and morphogenesis of Marsilea. American Journal of Botany 55: 884-889[CrossRef][ISI]
Charles D. F. 1984 Recent pH history of Big Moose Lake (Adirondack Mountains, New York, USA) inferred from sediment diatom assemblages. Verheimnis Internationale Vereinigung Limnologie 22: 559-566
Cole J. J. N. F. Caraco G. W. Kling T. K. Kratz 1994 Carbon dioxide supersaturation in the surface waters of lakes. Science 265: 1568-1570
Cook C. D. K. 1969 On the determination of leaf form in Ranunculus aquatilis. New Phytologist 68: 469-480[CrossRef][ISI]
Cronin G. K. D. Wissing D. M. Lodge 1998 Comparative feeding selectivity of herbivorous insects on water lilies: aquatic vs. semi-terrestrial insects and submersed vs. floating leaves. Freshwater Biology 39: 243-257
Dacey J. W. H. 1980 Internal winds in water lilies: an adaptation for life in anaerobic sediments. Science 210: 1017-1019
———. 1981 Pressurized ventilation in the yellow waterlily. Ecology 62: 1137-1147[CrossRef][ISI]
Denny M. 1993 Air and water: life's media. Princeton University Press, Princeton, New Jersey, USA
Edwards P. St. J. A. Allsopp 1956 The effects of changes in the inorganic nitrogen supply on the growth and development of Marsilea in aseptic culture. Journal of Experimental Botany 7: 194-202
Frost-Christensen H. K. Sand-Jensen 1995 Comparative kinetics of photosynthesis in floating and submerged Potamogeton leaves. Aquatic Botany 51: 121-134
Gleason H. A. A. Cronquist 1991 Manual of vascular plants of northeastern United States and adjacent Canada, 2nd ed. New York Botanical Garden, Bronx, New York, USA
Hellquist C. B. G. E. Crow 1984 Aquatic vascular plants of New England: Part 7. Cabombaceae, Nymphaeaceae, Nelumbonaceae, and Ceratophyllaceae. New Hampshire Agriculture Experiment Station Bulletin 527
Hutchings M. J. H. de Kroon 1994 Foraging in plants: the role of morphological plasticity in resource acquisition. Advances in Ecological Research 25: 159-238[ISI]
Hutchinson G. E. 1975 A treatise on limnology. 3. Limnological botany. Wiley, New York, New York, USA
Kane M. E. L. S. Albert 1983 Environmental and growth regulator effects on heterophylly and growth of Proserpinaca intermedia (Haloragaceae). Aquatic Botany 13: 73-85
Kerstetter R. A. R. S. Poethig 1998 The specification of leaf identity during shoot development. Annual Review of Cell and Developmental Biology 14: 373-398[CrossRef][ISI][Medline]
Kouki J. 1991 The effect of the water-lily beetle, Galerucella nymphaeae, on leaf production and leaf longevity of the yellow water-lily, Nuphar lutea. Freshwater Biology 26: 347-353[CrossRef][ISI]
———. 1993 Herbivory modifies the production of different leaf types in the yellow water-lily, Nuphar lutea (Nymphaeaceae). Functional Ecology 7: 21-26[CrossRef][ISI]
Lin B-L. W-J. Yang 1999 Blue light and abscisic acid independently induce heterophyllous switch in Marsilea quadrifolia. Plant Physiology 119: 429-434
Maberly S. C. D. H. N. Spence 1989 Photosynthesis and photorespiration in freshwater organisms: amphibious plants. Aquatic Botany 34: 267-286[CrossRef]
Njoku E. 1957 The effect of mneral nutrition and temperature on leaf shape in Ipomoea caerulea. New Phytologist 56: 154-171[CrossRef]
SAS Institute. 1990 SAS/STAT user's guide, version 6, fourth edition, volume 2. SAS Institute, Cary, North Carolina, USA
Sculthorpe C. D. 1967 The biology of aquatic vascular plants. Edward Arnold, London, England
Smart R. M. J. W. Barko 1985 Laboratory culture of submersed freshwater macrophytes on natural sediments. Aquatic Botany 21: 251-263[CrossRef]
Spence D. H. N. 1982 The zonation of plants in freshwater lakes. Advances in Ecological Research 12: 37-126
Titus J. E. 1992 Submersed macrophyte growth at low pH. II. CO2 x sediment interactions. Oecologia 92: 391-398[CrossRef][ISI]
———,R. S. Feldman D. Grisé 1990 Submersed macrophyte growth at low pH. I. CO2 enrichment effects with fertile sediment. Oecologia 84: 307-313[ISI]
Wallenstein A. L. S. Albert 1963 Plant morphology: its control in Proserpinaca by photoperiod, temperature and giberellic acid. Science 140: 998-1000
Zar J. H. 1984 Biostatistical analysis, 2nd ed. Prentice-Hall, Englewood Cliffs, New Jersey, USA
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