A comparison of growth responses between two species of Potamogeton with contrasting canopy architecture

Aquatic Botany 70 (2001) 53–66

A comparison of growth responses between two species of Potamogeton with contrasting canopy architecture David Cenzato∗ , George Ganf CRC for Freshwater Ecology and the Department of Environmental Biology, The University of Adelaide, South Australia, 5005 Received 10 December 1999; received in revised form 21 August 2000; accepted 13 September 2000

Abstract This study examines the response of two species of Potamogeton (Family: Potamogetonaceae), with differing canopy architectures, to an artificial light gradient. Potamogeton ochreatus Raoul and P. tricarinatus F. Meull. and A. Bennett were grown in water with an attenuation coefficient of 8.8 m−1 at various depths (10–81 cm) to give initial instantaneous irradiances between 0.4 and 460 ␮mol m−2 s−1 . The average daily water column irradiances (I¯ave ) between the planting depth and the water surface, over 15 daylight hours, ranged from 3.8 to 18.4 mol m−2 . After about 80 days all P. tricarinatus plantings, except those at 81 cm, formed dense surface canopies which could access atmospheric CO2 and had a maximum relative growth rate (70 ± 4 mg g−1 per day) and net assimilation rates (0.1–0.9 mg cm−2 day−1 ) significantly above those of P. ochreatus (57 ± 3 mg g−1 day−1 and , 0.1–0.5 mg cm−2 day−1 , respectively). P. ochreatus, which had a more diffuse and fully submersed habit, had a lower specific absorption coefficient (0.1 m−2 g−1 ) and average daily light compensation point (37 ␮mol m−2 s−1 ) than P. tricarinatus (0.9–1.2 m−2 g−1 and 57 ␮mol m−2 s−1 , respectively), but had a relative growth rate of approximately 25 mg g−1 per day even at an initial instantaneous irradiance of 0.4 ␮mol m−2 s−1 . In addition, P. ochreatus allocated about 80% of its biomass to leaves and stems irrespective of the light climate, whereas only small P. tricarinatus plants preferentially allocated biomass above ground. As energy levels increased, P. tricarinatus allocated a greater proportion of biomass to tissues capturing the limiting resource, light. As the light climate became more favourable, P. tricarinatus allocated more biomass to the rhizome. However, when compared to a wider range of submerged macrophytes, the two species optimised their respective growth rates by reacting to varying I¯ave in a similar way. Both

∗ Corresponding author. Present address: The Department of Environmental Biology, The University of Adelaide, Adelaide, SA 5005, Australia. Tel.: +61-88303-4560; fax: +61-88303-6222. E-mail address: [email protected] (D. Cenzato).

0304-3770/01/$ – see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 0 0 ) 0 0 1 4 3 - 1

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responded to lower than optimal I¯ave by increasing photosynthetic area and to above optimal values of I¯ave by decreasing photosynthetic area. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Macrophyte; Light; Turbidity; RGR; NAR; LAR

1. Introduction Numerous studies have shown that the depth distribution of submerged macrophytes is related to irradiance through the process of photosynthesis (Madsen and Sand-Jensen, 1991; Middelboe and Markager, 1997). However, for submerged macrophytes, the capture of light energy and access to an inorganic carbon source are dependent upon leaf morphology and canopy architecture, the efficiencies of which may alter as the plant grows upwards through a water column. Species such as Villarsia reniformis R. Br. (Family: Menyanthaceae), Aponogeton distachyon L.f. (Family: Aponogetonaceae) and members of the genera Nelumbo and Nymphaea (Family: Nymphaeaceae) have leaves which float on the surface, thereby optimising access to light and atmospheric CO2 but the depth to which they grow is restrained by maximum petiole length (Cooling, 1996). In contrast, species such as Lepilaena australis Drumm. ex Harvey (Family: Zannichelliaceae) and Ruppia polycarpa R. Mason (Family: Potamogetonaceae) have fully submerged leaves and are reliant upon dissolved inorganic carbon (DIC; dissolved CO2 and HCO3 − ) as a carbon source. Hence, their depth distribution is not influenced by petiole length and is more likely to be restricted by the underwater light climate. These differences suggest that species with fully submersed, sessile leaves and a diffuse canopy may be better suited to deeper, more turbid water, whereas species with petiolate, floating or emergent leaves forming a predominantly surface canopy may be more suited to shallow less turbid water. To test this hypothesis we chose two species of Potamogeton (Family: Potamogetonaceae). The South Australian species of Potamogeton (Jessop and Toelken, 1986) are distinguished by either having wholly submerged sessile leaves without petioles (P. pectinatus L., P. crispus L. and P. ochreatus Raoul) or with the upper leaves emergent or floating with petioles (P. tepperi A. Bennett, P. tricarinatus F. Meull. and A. Bennett, P. australiensis A. Bennett). P. ochreatus and P. tricarinatus represent two species from the same genus with two distinct leaf types and canopy architectures which may influence plant performance across a depth gradient via access to light and either atmospheric CO2 or DIC. These differences may also reflect a habitat preference: P. ochreatus may be better suited to deeper, more turbid water, whereas P. tricarinatus may be more suited to shallow, less turbid water. P. ochreatus has green to brown translucent, sessile linear leaves, up to 10 cm long and 6 mm wide which are distributed throughout the water column, whereas the petiolate leaves of P. tricarinatus congregate at the surface and are relatively thick and leathery, up to 15 cm long and 1 cm wide, broadly elliptic or ovate. The presence of emergent or floating leaves in P. tricarinatus suggests it is more resistant to desiccation and is able to utilise atmospheric CO2 . In contrast, the wholly submerged leaf canopy of P. ochreatus suggests it is less resistant to desiccation and dependent upon DIC. Furthermore, if P. tricarinatus is able to form an emergent or floating leaved canopy with access to atmospheric CO2 , it should have an enhanced growth rate compared with

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P. ochreatus, which is restricted to the use of DIC. To test these hypotheses we grew juvenile (ca. 10 cm high with 8–12 leaves) P. ochreatus and P. tricarinatus at depths between 10 and 81 cm with a vertical attenuation coefficient of ca. 9 m−1 and an euphotic depth of ca. 0.5 m. Initially individuals at 81 cm received <0.1% of surface irradiance, as the plants grew upwards they would encounter a more favourable light climate. We therefore calculated the average irradiance I¯ave that was potentially available between the water surface and the potting depth and related this to the response of the two species in terms of their relative growth rates (RGR), net assimilation rates (NAR) and leaf area ratios (LAR).

2. Materials and methods P. ochreatus was propagated from material collected from Barker Inlet Wetland (34◦ 490 S, 138◦ 340 E). P. tricarinatus was propagated from plants collected from Bool Lagoon, South Australia (37◦ 080 S, 140◦ 410 E). The propagative unit consisted of a length of stem (ca. 3 cm) containing a node and the associated leaf. Plants were propagated in 30 cm of water in pots (85 mm dia. × 145 mm) containing a mixture of 90% clay and 10% sand and fertilised with 3 g of Osmocote® (9-month release) per litre of soil mixture, providing a nitrogen loading of 100 g m−2 per year. The establishment period was 6 weeks. After establishment, 45 plants of each species were chosen on the basis of similar height (6–8 cm high), similar number of leaves (8–12) and dry weight (30–31 mg). Ten individuals from each species were destructively harvested and separated into leaf, stem, root and rhizome to provide initial values for plant dry weight and leaf area. Leaf area was measured using a DeltaT-Leaf area meter. Dry weight was recorded after drying to constant weight at 80◦ C. Six replicate individuals of each species were randomly allocated to five groups and placed on submerged fibreglass platforms in outdoor ponds (3 m × 4 m × 1.2 m) at depths of 10, 21, 41, 59 and 81 cm. A suspension of Bentonite clay (Blanch et al., 1998) was used to obtain a downwelling extinction coefficient (Kd ) of approximately 9 m−1 . Two submersible pumps (Ebara Best-Zero, 33 mm outlet, pond turnover time 0.75 h) constantly stirred the pond to prevent rapid settling of the suspension. Damage to the plants was prevented by directing flow underneath the platforms and around the pond walls. To estimate the depths at which the pots should be placed prior to filling the ponds, the values for light saturated photosynthesis (387 ␮mol m−2 s−1 ) and the light compensation point (50 ␮mol m−2 s−1 ) for Potamogeton perfoliatus L. (Harley and Findlay, 1994) were used in conjunction with an assumed vertical attenuation coefficient (Kd ) of 10 m−1 and a mid-day subsurface irradiance of 1250 ␮mol m−2 s−1 . From the Beer–Lambert Law, the instantaneous irradiances at the sediment surfaces at depths of 10, 21, 41, 50 and 81 cm were calculated to be 460, 153, 21, 3.4 and 0.4 ␮mol m−2 s−1 . After filling the ponds and the addition of bentonite, the downwelling attenuation coefficient was measured weekly using a LiCor underwater quantum sensor and turbidity was measured every 2–3 days using a Hach 2100a turbidimeter. The linear relationship between the two variables

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(Kd = 0.93 + 0.057 Turbidity, r 2 = 0.97, n = 27) was used to predict Kd from turbidity readings and additional bentonite was added as required. Turbidity readings at different positions within the pond confirmed a homogeneous distribution of bentonite. Solar irradiance (400–700 nm) was logged every minute and averaged over each hour (LiCor quantum sensor coupled to a LiCor Li1000 data logger). Surface reflection was measured over a range of incident irradiances on three consecutive cloudless days and used to estimate the immediate subsurface irradiance (I00 ). The mean daily subsurface irradiance (I¯o ) was calculated as the mean value from 0600 to 2100 h. The average daily irradiance (I¯ave ) in the water column, between the water and sediment surfaces, was calculated from the equation of Riley (1957) as modified by Blanch et al. (1998). The specific absorption coefficients (Ks ) of P. ochreatus and P. tricarinatus (with and without a floating canopy) were measured following the technique of Westlake (1964) as modified by Blanch et al. (1998). The specific absorption coefficient was estimated as the incremental increase in the vertical attenuation coefficient per unit increase in the leaf biomass (g DW m−3 over the depth of the canopy, ca. 0.4 m). Six replicate readings were taken for each increase in leaf density. The difference between the average irradiance with and without leaves present was used to estimate the absorption profiles for each species grown at each depth. Water temperature, pH and salinity were measured weekly. Plants were harvested at a rate of one species per treatment, per day, from January 12 to January 22 1998 after 78–88 days growth. The above ground tissue from each replicate, at each depth, was divided into portions representing the biomass present in sequential 10 cm vertical zones. This material was further sub-divided as follows: P. ochreatus leaf and stem, P. tricarinatus floating leaves, submerged leaf and stem. Calculations assumed that the green stems of P. ochreatus were photosynthetic, whereas the yellow stems of P. tricarinatus were not. A sub-sample of ca. 25% of the leaf types from each species, from each depth zone and each planting depth was used to estimate leaf surface area (DeltaT-Leaf area meter). Total leaf area was estimated from relationships between leaf dry weight and double sided leaf area. Below ground material was washed free of sediment and divided into root and rhizome. Dry weight was determined after drying at 80◦ C to constant weight. The RGR, NAR and LAR were calculated from the equations of Harper (1977). Extrapolation of the linear portion of the relationship between RGR and the average irradiance was used to calculate the average column irradiance at which RGR = 0 and the intensity which signified the onset of light saturated growth (I¯k ). The slope of this linear portion was also used to estimate growth efficiency, α. Statistical analysis was performed using JMP (version, 3.2 SAS Institute, 1989–1997) software package. Normality was determined with a Shapiro–Wilk test and homogeneity with the O’Brian and Brown–Forsythe tests. 3. Results 3.1. Temperature, pH, salinity and irradiance Temperature ranged from a minimum of 21◦ C to a maximum of 30.5◦ C, pH from 7.5 to 7.9 and salinity from 418 to 565 ppm.

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Table 1 Average daily subsurface irradiance (I¯o0 ) and the average daily irradiance between the sediment and water surface I¯ave throughout the experiment and the daily light intensities (Iz ) at the start of the experiment for P. ochreatus and P. tricarinatus relative to the planting depths (Z) and duration Species

I¯o0 a (mol m−2 )

I¯ave b (mol m−2 )

Iz b (mol m−2 )

Z

Duration (days)

P. ochreatus

27.2 27.1 27.2 27.1 27.1

18.0 12.3 7.3 5.2 3.8

27.9 10.5 1.8 0.4 0.1

10 21 41 59 81

79 80 82 81 78

P. tricarinatus

27.7 27.5 27.7 27.8 27.1

18.4 12.5 7.4 5.3 3.8

27.9 10.5 1.8 0.4 0.05

10 21 41 59 81

87 85 86 88 78

a b

Calculated using 39% surface reflectance. Calculated using mean Kd (8.84 m−1 ).

Surface reflection was 39%, similar to that recorded by Blanch et al. (1998). The mean Kd for the duration of the experiment was 8.8 ± 2.1 m−1 . The variation was due to the persistent settling of Bentonite even though particles were manually resuspended every 2 days. Mean daily I¯o0 , calculated as the mean integral I¯o0 over 15 h per day over 78–88 days, ranged from 27.1 to 27.8 mol m−2 and the I¯ave between water and sediment surfaces between 18.4 and 3.8 mol m−2 (Table 1). The initial daily light irradiance at each depth ranged from 0.05 to 27.9 mol m−2 (Table 1). 3.2. Survivorship and growth Survivorship was 100% across all treatments irrespective of species and planting depth. However, the growth characteristics of the two species differed. For P. ochreatus, the relationship between I¯ave and the whole plant RGR resembled the typical relationship between instantaneous irradiance and photosynthesis (Fig. 1a). At the low irradiances growth was light-limited. RGR was maximal at 7.3 mol m−2 (57 ± 2.9 mg g−1 per day) and declined as the I¯ave in the water column increased. As I¯ave increased, LAR reached an optimum of 281 ± 41 cm2 g−1 at 7.3 mol m−2 (Fig. 1b), the plant became more leafy as less biomass was invested per unit leaf surface area. At intensities above the optimum, LAR declined to a minimum of 109 ± 6.9 cm2 g−1 at 18 mol m−2 as the biomass allocated to unit leaf surface area increased. In contrast to RGR and LAR, the net production per unit leaf area (NAR) increased from a minimum of 0.12 ± 0.01 mg cm−2 per day at 3.8 mol m−2 to a maximum of 0.5 ± 0.2 mg cm−2 per day at 12.3 mol m−2 and remained constant as I¯ave increased to 18 mol m−2 (Fig. 1c). These data suggest that NAR became light saturated at an I¯ave greater than 12.3 mol m−2 .

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Fig. 1. The RGR (a), LAR (b) and the NAR (c) of P. ochreatus (diamond) and P. tricarinatus (square) grown for 78–88 days at five depths with an attenuation coefficient of 8.84 m−1 to give a range of average daily column irradiances.

RGR is a product of NAR and LAR and the small decrease in RGR observed from 7.3 to 18 mol m−2 was a result of LAR decreasing more rapidly than NAR increased. Nonetheless, in response to higher than optimal I¯ave , P. ochreatus still maintained a near optimal RGR, despite the decline in LAR from 281 to 109 cm2 g−1 . This suggests that at these values of I¯ave , growth was light saturated and plants did not require as large a photosynthetic area in comparison to plants at 7.3–3.8 mol m−2 . However, reductions in RGR as I¯ave decreased

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below the optimum were a result of both decreasing allocation to photosynthetic tissue and a decreased photosynthetic capacity. The relationship between I¯ave and RGR for P. tricarinatus also resembled the typical photosynthesis–irradiance curve (Fig. 1a). Growth was light limited at low irradiances and rose to a maximum of 70.4 ± 4.3 mg g−1 per day at 12.5 mol m−2 but unlike P. ochreatus, did not diminish as I¯ave increased. The leafiness of the plants rose to a maximum (LAR, 232 ± 35 cm2 g−1 ) at 5.3 mol m−2 as intensity increased but declined to a minimum of 87 ± 24 cm2 g−1 as I¯ave increased further (Fig. 1b). Unlike P. ochreatus, the NAR of P. tricarinatus rose in a linear manner as the average daily instantaneous column irradiance increased (Fig. 1c) which suggests that net assimilation did not become light saturated. The ability of this species to maintain optimal growth rates across a broad spectrum of intensities was due to the increase in NAR which off-set the reduction in LAR. However, at the lowest I¯ave growth rates reflected a decline in both these characteristics. 3.3. Comparative RGR, NAR and LAR Although the response patterns of RGR, LAR and NAR to I¯ave appeared similar for both species (Fig. 1), analysis demonstrated that there was a significant interaction between irradiance and species (RGR, p < 0.0001; LAR, p = 0.04; NAR, p = 0.01). The source of the growth rate interaction was found in the higher RGR of P. ochreatus compared with that of P. tricarinatus at the lowest I¯ave , whereas at all other intensities the RGR of P. tricarinatus was greater than P. ochreatus (Fig. 1a). The interaction detected for LAR reflected the observation that the LAR of P. tricarinatus began to decline before the LAR of P. ochreatus at higher irradiances, and at the two highest irradiances LARs were similar. The positive interaction between species and I¯ave intensity reflected the similar NARs for both species at the lowest irradiances and the higher rate for P. tricarinatus at all other intensities. 3.4. Growth curve analysis Even at the lowest irradiance both species showed positive growth rates. In order to estimate the I¯ave at which RGR would approximate to zero it was assumed that the growth rate declined linearly as intensity decreased. With this assumption the average irradiance compensation points, I¯c , were calculated to be ca. 37 and 57 ␮mol m−2 s−1 (2 and 3.1 mol m−2 per 15 h day) for P. ochreatus and P. tricarinatus, respectively. The I¯ave intensities which indicated the onset of light saturated growth, I¯k , were 113 and 99 ␮mol m−2 s−1 (6.1 and 5.4 mol m−2 per 15 h day) and the maximum growth efficiencies, α, were 0.5 and 0.71 mg g−1 per day (␮mol m−2 s−1 )−1 for P. ochreatus and P. tricarinatus, respectively (Table 2). 3.5. Biomass allocation The weight of P. ochreatus individuals was greatest at an I¯ave of 7.3 mol m−2 , where ca. 80% was allocated to stems and leaves (Fig. 2a). Above and below this optimal intensity

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Table 2 Calculated average column irradiance compensation point (I¯c ), average irradiance at onset of light saturated RGR (I¯k ), RGR efficiency (α) and maximum relative growth rate (RGRmax ) for P. tricarinatus and P. ochreatus Species

I¯c (␮mol m−2 s−1 )

I¯k (␮mol m−2 s−1 )

α (mg g−1 per day (␮mol m−2 s−1 )−1 )

RGRmax (mg g−1 per day)

P. tricarinatus P. ochreatus

57 37

99 113

0.71 0.5

74 60.4

Fig. 2. Biomass allocation to various tissues of P. ochreatus (a) and P. tricarinatus (b) grown for 78–88 days at five depths with an attenuation coefficient of 8.84 m−1 to give a range of average daily column irradiances.

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weight decreased, principally as a result of a decline in the allocation to rhizome, although at the lowest I¯ave the percentage allocation to roots also declined. In general, the allocation to leaves and stems was approximately five times that allocated to roots and rhizomes irrespective of I¯ave . In contrast to P. ochreatus, the maximum total weight of P. tricarinatus occurred at 18.4 and 12.5 mol m−2 but was differentially allocated (Fig. 2b). At the shallowest depth 80% was allocated to root and rhizome. As the I¯ave decreased, the allocation to rhizomes decreased and biomass was preferentially allocated to stems and submerged leaves. In the deeper water, many of the stems were devoid of leaves. Root biomass showed relatively little change. 3.6. Specific absorption coefficients There were linear relationships between the vertical attenuation coefficient and increasing canopy biomass of P. tricarinatus with submerged leaves (Kd = 1.22 g DW + 2.264, r 2 = 0.91, n = 36), P. tricarinatus with a floating canopy (Kd = 0.867 g DW + 0.55, r 2 = 0.99, n = 36) and P. ochreatus (Kd = 0.074 g DW + 1.645, r 2 = 0.76, n = 36). From the incremental increase in Kd the highest specific absorption coefficients (Ks ) was for P. tricarinatus with submerged leaves (1.2 m2 g−1 ) followed in turn by P. tricarinatus with a mature floating canopy (0.9 m2 g−1 ) and P. ochreatus with its submerged canopy (0.1 m2 g−1 ). This is consistent with canopy structure and leaf morphology of both species. Submerged leaves of P. tricarinatus are thinner and more numerous in comparison to aerial leaves and therefore, cover a larger surface area. Thus, for a given weight, the submerged canopy of P. tricarinatus is able to intercept more light than the floating canopy. In addition, the high Ks values of P. tricarinatus may result in a high level of self-shading. Hence, the formation of a canopy by concentrating leaf material at the surface may be a growth response to optimise the positioning of leaves, such that leaves on a mature stem are only present close to the surface, thereby minimising self-shading. In contrast, the canopy of P. ochreatus was more diffuse with much smaller leaves than either type of P. tricarinatus canopy, resulting in a reduced light intercepting ability and a much lower Ks value. However, this canopy structure allows the penetration of light to the lower leaves, representing a passive strategy to optimise light capture. 3.7. Light absorbance profiles The biomass of photosynthetic tissue present within the water column for each species at each planting depth was used in conjunction with the appropriate Ks to calculate the percentage of available light absorbed by the two species (Fig. 3). P. tricarinatus, which had developed a floating canopy of leaves by the end of the experiment, absorbed between 89 and 98% of the available irradiance. However, at the lowest I¯ave where a canopy had not formed, only 10% was absorbed. P. ochreatus absorbed much less of the available light, only 3.8% was absorbed by individuals planted at 81 cm and this increased to only 40% for those planted at 41 cm, before falling to 20% for those planted at 10 cm.

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Fig. 3. The percentage of average daily water column irradiance absorbed by P. ochreatus (circle) and P. tricarinatus (square) after 78–88 days growth. Individuals were planted at five depths with an attenuation coefficient of 8.84 m−1 which gave five average water column irradiances.

4. Discussion P. ochreatus and P. tricarinatus display contrasting canopy structures. P. ochreatus had an erect, entirely submerged, diffuse canopy, which allowed light to illuminate the lower leaves. P. tricarinatus had a more concentrated surface canopy which captured light at, or close to, the surface. These canopy architectures resulted in differing efficiencies of light capture in the two species with P. tricarinatus having the higher specific absorption coefficient. However, both P. tricarinatus and P. ochreatus represent shade adapted morphologies which saturate at about 5% of full sun. Nevertheless, the growth rate of P. tricarinatus was greater than P. ochreatus except at the lowest average irradiance where the final plant weights were 205 and 169 mg for P. tricarinatus and P. ochreatus, respectively. This result suggests that even though the submerged leaves of P. tricarinatus are shade tolerant, the surface canopy is able to tolerate the much higher irradiances at the water surface by the use of emergent leaves. P. ochreatus uses changes in photosynthetic area to optimise its growth without altering allocation of biomass between the above and below ground plant components. It is therefore capable of persisting under low light conditions and represents a truly shade tolerant species. P. tricarinatus with a higher I¯c requires either a lower Kd or establishment at shallower depths. It also responds morphologically by allocating a larger proportion of biomass to the surface canopy. The production of aerial leaves also has consequences in terms of accessibility to inorganic carbon through exploiting atmospheric CO2 . Given that plants receive adequate nutrients, optimal plant growth will be achieved when there is a balance between the level of irradiance and the supply rate of inorganic carbon. Hence, for a plant with a submerged canopy, the inorganic carbon supply is restricted to

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dissolve inorganic carbon (DIC) (Bowes and Salvucci, 1989; Madsen and Sand-Jensen, 1991). Since the rate of diffusion for DIC through water is approximately 10,000 times slower than that of CO2 through air, and boundary layer resistance is between 100 and 500 times greater in water than in air, photosynthesis may become carbon limited at higher irradiances (Madsen and Sand-Jensen, 1991). Conversely, if a plant is able to access atmospheric CO2 maximum photosynthesis can be maintained at a higher irradiance due to the increased availability of inorganic carbon which leads to a higher RGR (Bowes and Salvucci, 1989; Madsen and Sand-Jensen, 1991). Moreover, the availability of oxygen for night-time respiration is also increased in plants with aerial leaves (Bowes and Salvucci, 1989). Consequently, the differences observed between P. ochreatus and P. tricarinatus may be a result of canopy contact with the atmosphere by the latter. At the other extreme, species such as Chara sp. (Family: Characeae), which are well adapted to shade conditions and the use of DIC, may change morphology in response to changes in the amount of light they receive in order to optimise growth (Chambers, 1987). The use of this strategy indicates that light is the limiting resource for bottom dwelling species and not the availability of DIC. The species used in this study have features that place them between these two extremes. P. tricarinatus, in particular, uses both CO2 and DIC as inorganic carbon sources. The production of aerial leaves at the four shallowest planting depths indicate the use of CO2 and high irradiance, while growth of the species at 81 cm, where the canopy was always submerged provides evidence for DIC utilisation under sub-optimal light conditions. Thus, P. tricarinatus utilises both changes in canopy structure and efficiency in order to optimise growth. As P. ochreatus has a submerged canopy, it uses changes in leaf area to optimise growth, given that DIC is the only source of inorganic carbon available. Hence, in this study, P. ochreatus grew optimally at a lower I¯ave than P. tricarinatus. 4.1. Comparison with other submerged aquatic macrophytes A direct comparison of the species used in this study is only possible with a similar study on Vallisneria americana Michx. (Family: Hydrocharitaceae) by Blanch et al. (1998). This is primarily due to the many and varied procedures used by the researchers in the past with the major differences being the use of short-term photosynthetic rates to infer plant growth and the use of instantaneous irradiances. Nonetheless, for species other than V. americana, instantaneous growth rates can be estimated from photosynthetic rates of carbon fixation (mg C g−1 DW h−1 ), assuming that plant biomass (g DW) is approximately 40% carbon. However, irradiance values for growth compensation points (Ic ) cannot be converted. Thus, values of Ic are most likely to be underestimates of I¯c values which incorporate the irradiance of the whole water column. Conversely, calculated instantaneous growth rates are over estimates as there is no consideration of night-time respiration or seasonal senescence. The least shade tolerant of the species compared is Myriophyllum spicatum L. (Family: Haloragaceae), which has the highest Ic value (Table 3). This is indicative of its canopy morphology, where up to 68% of the photosynthetic area is concentrated within the upper

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Table 3 Comparison of RGR and irradiance compensation point between various aquatic macrophytes Species

RGR (mg g−1 per day)

Irradiance compensation point (␮mol m−2 s−1 )

Source

M. spicatum P. tricarinatus P. ochreatus V. americana Potamogeton robbinsii E. canadensis P. obtusifolius P. perfoliatus

27.8a 74 60.4 19.1 8.6a 30–70a 86.4a 43a

37–83b 57 37 26 20b 12b 10–13b 25–57b

Madsen et al. (1991) This study This study Blanch et al. (1998) Madsen et al. (1991) Madsen et al. (1991) Maberly (1993) Madsen et al. (1991), Goldsborough and Kemp (1988), and Harley and Findlay (1994)

a b

Calculated from photosynthetic rates (mg C g−1 DW h−1 ), assuming plant dry weight is 40% carbon. Instantaneous irradiance values.

30 cm of the water column (Titus and Adams, 1979). Thus, M. spicatum has adapted to higher irradiances in terms of both morphology and the efficiency of light capture (Titus and Adams, 1979; Madsen et al., 1991; Harley and Findlay, 1994). The calculated growth rate of M. spicatum is lower than that of P. tricarinatus and P. ochreatus. This may be attributed to a lower Ks value (0.006 m2 g−1 DW) in comparison to the study species. Hence, M. spicatum has a reduced light harvesting capability that manifests itself as a reduced growth rate. In addition, the canopy of M. spicatum remains submerged unlike M. brasiliense Cambess. which has aerial leaves to exploit atmospheric CO2 . The amphibious habit of M. brasiliense results in a higher growth rate than M. spicatum (Salvucci and Bowes, 1982). Similarly, the high growth rate of P. tricarinatus in comparison to P. ochreatus is likely to be largely a result of increased availability of inorganic carbon (via atmospheric CO2 ) and tolerance to high irradiances. These factors combined, result in P. tricarinatus also having a higher I¯c value (Table 3). P. perfoliatus L. is a similar species to P. ochreatus having a moderate growth rate and a range of Ic values (Table 3). At low irradiances, P. perfoliatus produces an erect canopy which becomes more diffuse as light availability increases (Goldsborough and Kemp, 1988). Similarly, Elodea canadensis Michx. (Family: Hydrocharitaceae) also exhibits changes in canopy structure with varying irradiance resulting in maximum growth rates similar to those of the study species (Table 3). At low irradiances, E. canadensis forms an erect canopy, exploiting a more favourable light climate closer to the surface. However, at high irradiances the canopy becomes prostrate in order to avoid excessive light (Barko et al., 1981). This avoidance of high light and a low Ic value indicate E. canadensis is a well suited shade species. The remaining species of Potamogeton in Table 3 are also shade tolerant, displaying low Ic values. In addition, the canopies of these species are erect and diffuse and, as with other shade species, the canopies of these species become more diffuse as available light increases (Madsen et al., 1991; Maberly, 1993). However, the high growth rate of Potamogeton obtusifolius Mert. and Koch is indicative of a species capable of exploiting a wider range of irradiances.

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Thus far, the species compared in Table 3 all possess branching, leafy canopies produced from apical meristems. In contrast, V. americana produces long strap-like leaves from basal meristems which form a shallow submerged canopy suited for turbulent environments (Blanch, 1997). By exploiting a lotic environment, V. americana benefits from an increased DIC availability through reduced boundary layer thickness and can therefore maintain maximum photosynthesis at higher irradiances. This is reflected by a moderate growth rate and I¯c value (Table 3). In response to decreasing I¯ave , V. americana responds in a similar manner to a plant with a branching, leafy habit and apical meristems. The strap-like leaves of V. americana become thinner and longer for the same weight, thereby, increasing the photosynthetic area exposed to incoming irradiance at the canopy surface (Blanch, 1997). However, the strap-like canopy of V. americana has a low Ks value (0.005 m2 g−1 ) when compared with either P. ochreatus or P. tricarinatus. Yet, V. americana maintains a moderate growth rate due to a much higher α value of 0.33 mg g−1 per day (␮mol m−2 s−1 )−1 (Blanch et al., 1998) (Table 3). It is apparent from the comparison between the study species and a wider range of submerged macrophytes, that P. ochreatus and P. tricarinatus optimised their respective growth rates by reacting to varying I¯ave in a similar way. Both responded to lower than optimal I¯ave by increasing photosynthetic area and to above optimal values of I¯ave by decreasing photosynthetic area. However, the differences observed in RGR, Ks , I¯c and I¯k between the two study species are a reflection upon their differing canopy architecture and morphology. References Barko, J.W., Hardin, D.G., Matthews, M.S., 1981. Growth and morphology of submersed freshwater macrophytes in relation to light and temperature. Can. J. Bot. 60, 877–887. Blanch, S.J., 1997. Influence of water regime on growth and resource allocation in aquatic macrophytes of the Lower River Murray, Australia. Unpublished Ph.D. Thesis. Department of Botany, The University of Adelaide, Adelaide, SA. Blanch, S.J., Ganf, G.G., Walker, K.F., 1998. Growth and recruitment in Vallisneria americana as related to average irradiance in the water column. Aquat. Bot. 1242, 1–25. Bowes, G., Salvucci, M.E., 1989. Plasticity in the photosynthetic carbon metabolism of submersed aquatic macrophytes. Aquat. Bot. 34, 233–266. Chambers, P.A., 1987. Light and nutrients in the control of aquatic plant community structure. II. In situ observations. J. Ecol. 75, 621–628. Cooling, M.P., 1996. Adaptations of aquatic macrophytes to seasonally fluctuating water levels. Unpublished Ph.D. thesis, Department of Botany, The University of Adelaide, South Australia. Goldsborough, W.J., Kemp, W.M., 1988. Light responses of a submersed macrophyte: implications for survival in turbid tidal waters. Ecology 69, 1775–1786. Harley, M.T., Findlay, S., 1994. Photosynthesis–irradiance relationships for three submersed macrophytes in the tidal freshwater Hudson River. Estuaries 17, 200–205. Harper, J.L., 1977. Population Biology of Plants. Academic Press, London. Jessop, J.P., Toelken, N.R. (Eds.) 1986. Flora of South Australia Part IV, 4th Edition. South Australian Government Printing Division, Adelaide, SA. Maberly, S.C., 1993. Morphological and photosynthetic characteristics of Potamogeton obtusifolius from different depths. J. Aquat. Plant Mgmt. 31, 34–39. Madsen, T.V., Sand-Jensen, K., 1991. Photosynthetic carbon assimilation in aquatic macrophytes. Aquat. Bot. 41, 5–40.

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