Reprinted from the Journal Trifid No. 3/2005:
ANDREJ PAVLOVIČ*1), ELENA MASAROVIČOVÁ, JÁN HUDÁK
Department of Plant Physiology, Faculty of Natural Sciences, Comenius University in Bratislava, Mlynská dolina, SK-842 15, Bratislava, the Slovak Republic.
*author for correspondence (anpa@pobox.sk)
According to Givnish’s cost/benefit model of carnivory, carnivorous plants are restricted to environments with abundant supply of water and light but poor in nutrients. In other environments, the cost of producing traps would exceed the benefits gained from prey. From photosynthetic point of view, cost represents extra energy requirement for respiration of carnivorous organs. Benefit is increased supply of nutrients, mainly nitrogen. If water and light are in a short supply or nutrients are abundand, carnivorous plants give up carnivory temporarily. Nepenthes is Asian pitcher plants which leaves are composed of assimilation part and trapping pitcher. This allow us to make a direct comparison between assimilation part and carnivorous trapping pitcher and to understand which features are involved in carnivorous syndrome. This was not able in former studies in Drosera, Pinguicula and Darlingtonia in which the entire shoot is photosynthetic and captured organs.
Nepenthes alata and Nepentes mirabilis were grown under greenhouse conditions in moss without fertilizer. We measured the rate of photosynthesis (PN) and respiration (RD) gasometrically in assimilation leaves and pitchers. Assimilation pigment concentration was determined spectrophotometrically, N, C and H concentration using CHN-method. Samples for light and electron microscopy were fixed in glutaraldehyde and OsO4 and were embadded in Durcupan and double stained with toulidine blue and basic fuchsin (light microscopy) and uranyl acetate and lead citrate (transmission electron microscopy). Stomata density was determined using microrelief method. To evaluate the significance of obtained data Student’s t-test was used.
PN of assimilation leaves (PNleaf) ranged 34.8–53.0 in N. alata and 16.3–40.6 nmol CO2 g-1 d.w. s-1 in N. mirabilis and pitcher (PNpitcher) ranged -6.2–0.0 (CO2 was emitted) in N. alata and -3.2–(+)4.4 nmol CO2 g-1 d.w. s-1 in N. mirabilis at 300 μmol.m-2.s-1 PAR, 25°C and 660 mg CO2 m-3. The RDleaf of N. alata was significantly higher than RDpitcher. On the contrary, N. mirabilis had higher RDpitcher. Lower PNleaf in N. mirabilis is probably due to lower nitrogen concentration in the leaf. In comparison with non-carnivorous plants we can conclude that PN is lower and the pitchers represent the cost for plant. PN at different irradiance revealed, that at low light intensity (60 μmol.m-2.s-1 PAR) more CO2 is emitted through RDpitcher + RDleaf – PNpitcher than assimilate by PNleaf and carnivory does not pay. PNleaf increased with leaf possition number such that youngest leaves carrying the pitcher had PNleaf once that of older leaf without pitcher.
We found a set of characteristics that are involved in low assimilation capacity of traps. First, five times lower assimilation pigment concentration (chla, chlb, carotenoids) as well as lower nitrogen concentration in the pitcher, although H and C concentration do not differ significantly. Abaxial side of assimilation leaf has app. 10 times (N. alata) and 200 times (N. mirabilis) higher stomata density than the pitcher. This result in lower stomatal conductance for CO2 in the pitcher. Similarly, we can predict lower mesophyll conductance in the pitcher, because mesophyll is compact and has a very low proportion of intercellular spaces without palisade and spongious parenchyma in the mesophyll. On the contrary, mesophyll of assimilation leaf is composed of palisade layer with numerous chloroplasts and spongious parenchyma with a well developed intercellular spaces. Chloroplasts in both tissue has well developed grana with numerous plastoglobuli and differences in mesophyll chloroplasts between pitcher and assimilation leaf are rather quantitative than qualitative character.
We predict, that some of the characteristics, that make photosynthesis inefficient, may be responsible for carnivorous function in nutrient poor habitat. Compact mesophyll may provide better symplastic transport for water with enzymes into the pitcher as well as better transport for nutrients obtained from prey. Apoplastic barriers were found beneath digestive glands – analogy of Casparian strip in root endodermis (using flourescencemicroscopy). Very low stomata density is probably consequence of low assimilation capacity of pitcher, because respiration delivers sufficiency CO2 for PN and thus pitcher is less dependent on atmosferic CO2 concentration as well as transpiration is not favoured in traps, because water is secreted into the pitcher as a digestive fluid.