Adamec L., 1997. Mineral nutrition of carnivorous plants: A review. Bot. Rev. 63: 273-299.
Institute of Botany of the Academy of Sciences of the Czech Republic, Section of Plant Ecology, Dukelská 145, CZ-379 82 Tøeboò, Czech Republic; fax 0042-333-721136
Table of Contents
III. Ecological Factors in Habitats of carnivorous Plants
IV. Mineral Nutrition of carnivorous Plants - General Principles
V. Mineral Nutrition of terrestrial carnivorous Plants under Greenhouse Conditions
VI. Mineral Nutrition of terrestrial carnivorous Plants in natural Habitats
VII. High-nutrient Conditions
VIII. Mineral Nutrition of aquatic carnivorous Plants
IX. Organic Nutrition of carnivorous Plants
X. Inspiration for further Research
XI. General Conclusions
XIII. Literature cited
Plant carnivory is one of many possible adaptation strategies to unfavourable conditions, mostly low nutrient availability in wet, acid soils. The following questions concerning the mineral nutrition of carnivorous plants are reviewed: the relative importance of carnivory and root nutrition for growth; which nutrients (elements) from prey are of principal importance for growth; what is the relationship between mineral and organic nutrition based on carnivory; what are the interactions between carnivory and root mineral nutrition; and what is the importance of carnivory under natural conditions. Special attention is paid to aquatic carnivorous plants. Studies on mineral nutrition carried out under laboratory and/or greenhouse conditions are discussed separately from those under field conditions. In this review, emphasis is placed on recapitulation of original data and conclusions of results from a variety of studies which approach carnivorous plants from an ecophysiological point of view.
Die Karnivorie der Pflanzen ist eine von mehreren Adaptationsstrategien zu ungünstigen Bedingungen, meist zu niedrigem Nährstoffangebot in feuchten, sauren Böden. Es wird eine Übersicht präsentiert über folgende Fragen der Mineralernährung von karnivoren Pflanzen: die entsprechende Bedeutung der Karnivorie und der Wurzelernährung für das Wachstum; welche Nährstoffe (Elemente) von der Beute prinzipielle Bedeutung für das Wachstum haben; welche Beziehung ist zwischen der anorganischen und organischen Ernährung, die auf der Karnivorie beruht; welche Zwischenbeziehung besteht zwischen der Karnivorie und der Mineralernährung durch Wurzeln; und welche Bedeutung hat die Karnivorie unter natürlichen Bedingungen. Eine besondere Aufmerksamkeit ist den aquatischen karnivoren Pflanzen gewidmet. Untersuchungen über Mineralernährung in Labor- und/oder Gewächshausbedingungen werden gesondert von Ergebnissen diskutiert, die unter Feldbedingungen gewonnen wurden. In dieser Übersicht werden nachdrücklich Originaldaten und Schlussfolgerungen aus Ergebnissen verschiedener Studien rekapituliert, die sich mit karnivoren Pflanzen vom ökophysiologischen Standpunkt befassen.
Over 600 species of carnivorous plants (CPs), from a total of about 300,000 species of vascular plants, grow over the world. All plants considered carnivorous fulfil the following three criteria: they a) catch or trap prey, b) absorb metabolites from prey and c) utilize these metabolites in their growth and development (Lloyd, 1942). As CPs grow together with non-carnivorous plants in their natural habitats, both plant groups are subjected to the same ecological conditions. Carnivory, which developed several times during plant evolution, is only one of many possible adaptation strategies to unfavourable conditions (for the discussion see Juniper et al., 1989, p. 3-11).
Charles Darwin (1875) was the first to reveal that CPs showed enhanced growth if fed on insects and/or animal proteins. His successors showed that Drosera plants fed on insects had a higher rate of plant reproduction than vegetative growth (see Oosterhuis, 1927; Lloyd, 1942). It was also demonstrated in Drosera that, alone, foliar uptake of nutrients from prey was not sufficient for normal growth of CPs. However, root mineral nutrition, alone, without feeding on insects was sufficient for normal growth. On the basis of laboratory growth experiments, a German physiologist K. Goebel summarized the importance of carnivory as early as 1893, as: 'Carnivory is useful for plants but it is not indispensable.'
The basic questions raised by biologists over about the last 120 years involve: the relative importance of foliar and root nutrition of CPs; which nutrients (elements) from prey bodies are of principal importance for growth?; what is the relationship between organic and mineral nutrition of CPs?; and what is the importance of carnivory under natural conditions? In the last 20 years, the question about the interaction between foliar and root mineral nutrition in CPs has also become topical. In this review, all these questions are discussed in the light of recent literature. Special attention is paid to aquatic CPs. This review follows on from previous publications in this field (Lüttge, 1983; Juniper et al., 1989). Since different CP species react to similar ecological conditions of mineral nutrition in a rather different way and because experimental conditions are greatly variable in different studies, it is hardly possible to create a united generalized concept of mineral nutrition that is valid for all CP species. Therefore, in this review, emphasis is placed on recapitulation of original data and conclusions of results from a variety of studies which approach CPs from an ecophysiological point of view.
III. Ecological Factors in Habitats of carnivorous Plants
The majority of terrestrial CPs grow in bog and fen soils in which they encounter persistent unfavourable conditions. The soils are usually wet or waterlogged, at least over the growing period. They are mostly acid (pH 3-6; e.g. Roberts and Oosting, 1958; Chandler and Anderson, 1976a; Juniper et al., 1989, p. 21-22) but some are neutral or slightly basic (e.g. Schwintzer, 1978). They usually contain a high proportion of slowly decomposing organic matter (plant remnants). Due to waterlogging, the soils are partly (hypoxia) or entirely (anoxia) deprived of oxygen. Moreover, changing of anaerobic and aerobic conditions is also harmful (post-anoxic injury; Crawford, 1989, p. 105-129). In wet soils, decomposition of organic matter may lead to a high concentration of toxic H2S (or S2-) and a low redox potential. When redox potentials are low, iron and manganese may solubilize and become toxic to plant roots, while some other microelements may become unavailable to plants (Crawford, 1989).
It is presumably the very low level of macronutrients available to plants which is the primary unfavourable ecological factor in these soils, that is overcome by carnivory (Lüttge, 1983; Juniper et al., 1989, p. 129-135). However, there is a tremendous difference between the available and total macronutrient content in most bog and fen soils. For example, Roberts and Oosting (1958) reported very low available nutrient content in bog soils with Dionaea in North Carolina (in mg.kg-1 dry weight, DW): NH4+, 2; PO4, less than 2; K, 2; Mg, 1; Fe, 1. There was a complete lack of detectable NO3-, Ca, and Mn. However, the available nutrient content in fen soils can be one to two orders of magnitude higher (e.g. Schwintzer, 1978; Aldenius et al., 1983). In contrast, the following total N and P contents were found in bog soils inhabited by 4 Australian and New Zealand Drosera species (in g.kg-1 DW): N, 0.46-2.5; P, 0.09-1.9 (data summarized by Chandler and Anderson, 1976a).
Normal functionning of CP roots' (uptake of nutrients and water) is dampened by low nutrient availability in soils, and this stress factor is greatly amplified by waterlogged and anoxic soils. Therefore, carnivory of most terrestrial CPs can be explained as an adaptation to all these stress factors. However, the extent of adaptation of CP roots' to waterlogging alone has not yet been studied.
Terrestrial CPs have adapted to these unfavourable factors by growing slowly. They do not require a high supply rate of mineral nutrients from soils, as they are able to store nutrients in their organs and re-utilize them efficiently (Dixon et al., 1980). A weakly developed root system is a common characteristic of most CPs (Lüttge, 1983; Juniper et al., 1989, p. 21-22). The root:total biomass ratio ranges from only 3.4 to 23 % in various CPs (Karlsson and Carlsson, 1984; Karlsson and Pate, 1992b; Adamec et al., 1992). Roots are usually short, weakly branched, and able to tolerate, in an unknown way, anoxia and related phenomena (H2S) in wet soils. They are able to regenerate easily. Generally, the capacity of CP roots for mineral nutrient uptake is limited, and compensated by nutrient uptake from prey.
IV. Mineral Nutrition of carnivorous Plants - general Principles
The term mineral nutrition of plants includes processes of mineral nutrient uptake by plants from the ambient medium, nutrient translocation within the plant, incorporation of mineral nutrients to plant metabolism and physiological functions, release from primary physiological functions and of entry secondary ones. Our knowledge of CP mineral nutrition can be considered to be fragmented, as it is confined to about 40 species and less than 45 studies since the 1950s.
The most extensive process of CP mineral nutrition is photosynthetic fixation of CO2 by leaves. All CPs are green and able to fix CO2 (autotrophy) although the growth of some species (mainly aquatic) is partly dependent on organic carbon uptake from prey (facultative heterotrophy; see Lüttge, 1983). Many CPs of all taxonomic groups fix CO2 according to the C3 scheme of the Calvin cycle (Lüttge, 1983), but anatomical evidence in favour of the C4 type has been given in 6 Mexican succulent Pinguicula species (Studnièka, 1991). The relationship between CP photosynthetic performance and carnivory is complex and ambiguous (Juniper et al., 1989, p. 144-146). Although photosynthetic rate of traps is lower than that of leaves (Knight, 1992; Adamec, 1996), carnivory may increase the plant's total photosynthetic rate due to higher leaf biomass and also to increased rates per leaf area unit (Givnish et al., 1984).
Although growing in mineral-poor habitats, both terrestrial and aquatic CPs have nearly the same composition of macroelements as non-carnivorous wetland and aquatic plants (Table I; cf. Dykyjová, 1979). However, terrestrial CPs have considerably lower content of macroelements per DW unit than aquatic CPs. The surprisingly high P content in Aldrovanda could be caused by prey left in its traps. Nutrient uptake from prey is advantageous because animal prey is relatively rich in mineral nutrients. The following total nutrient content was found in insects (g.kg-1 DW): N, 99-121; P, 6-14.7; K, 1.5-31.8; Ca, 22.5; Mg, 0.94 (Reichle et al., 1969; Watson et al., 1982). However, a part of insect nutrients is not available to CPs (Dixon et al., 1980).
V. Mineral Nutrition of terrestrial carnivorous Plants under Greenhouse Conditions
In all studies, in which CPs were fed or fertilized, results have been greatly dependent on variables such as length of growing period, initial size of plants, nutrient content in rooting medium, quantity of added prey, and species identity. As greenhouse studies represent a considerable simplification of the ecological factors (e.g. lack of competition) which CPs face in natural habitats, results reflect the potential abilities of CPs to take up nutrients through roots or leaves and to regulate these processes, rather than plant responses in natural habitats or the ecological importance of carnivory.
The effect on growth of insect feeding versus mineral fertilization of fen soil was compared in Pinguicula vulgaris (Aldenius et al., 1983), a species which usually grows in mineral richer soils. The supply of concentrated mineral nutrient solution to fen soil led to a 100 % increase in total biomass, whereas insect feeding alone led to only a 24-48 % increase. However, feeding combined with fertilization led to a 200 % increase in DW. Thus, P. vulgaris is able to take up all nutrients required for its vigorous growth from nutrient rich soil by roots. Moreover, insect feeding stimulated the effective nutrient uptake by roots and resulted in approx. 1.6 times higher accumulation of N in plants than it could have been absorbed from the prey. The similar growth pattern was also found in aseptically grown P. lusitanica where the effect of insect feeding correlated positively with increasing nutrient content of the soil (Harder and Zemlin, 1967).
The positive growth effect of insect feeding in CPs can also be achieved when only mineral nutrient solution is dropped on the trapping part of leaves instead of prey (Karlsson and Carlsson, 1984; Adamec et al., 1992). P. vulgaris, grown in a fen soil supplied with a diluted nutrient solution, was able to enhance its growth and accumulation of N and P in its biomass to a similar or even greater extent than due to insect feeding when leaves were supplied with either mineral N, P or microelements or mixtures of these nutrients (Karlsson and Carlsson, 1984; see Table II). It indicates that utilization of mineral nutrients (N, P, microelements) is of a primary importance in this species. It was mainly phosphate that enhanced significantly plant growth and also led to a high increase of total content of both P and N in plants. N and microelements were less efficient and increased the total N but not P content. Mild negative interactions usually occurred between the effects of N, P and microelements when these nutrients were combined but microelements with N+P increased the total N and P content (Table II). Thus, the foliar uptake of certain nutrient(s) in P. vulgaris may promote markedly the root uptake of other nutrients, leading to higher plant biomass. This is a well-known response in non-CPs. It should be added that nutrient content per unit of biomass, can remain unaffected or be even lower after nutrient supply, as a result of fast growth (see Tables II and VII; Christensen, 1976). It is therefore an unreliable measure of nutrient uptake by CPs.
Harder and Zemlin (1968) demonstrated in axenic cultures of Pinguicula lusitanica, grown on agar without N and P for 8 weeks, nutrient utilization from supplied Pinus pollen. The pollen-fed plants grew faster, contained more chlorophyll, and aged more slowly. In contrast to unfed plants, they initiated flower buds very early and flowered richly. Since the pollen grains germinated on glands of Pinguicula leaves (Joel, unpubl.) the digestion of germinated pollen grains was easy. Thus, the Pinguicula species with broad leaves (and possibly also Drosera) may benefit from aerial rain of pollen and probably also of spores, seeds and leaf fragments under natural conditions.
The hypothesis that CPs respond less to prey at high soil nutrient levels than at lower levels (Givnish et al., 1984) was tested on P. vulgaris, P. alpina, P. villosa and Drosera rotundifolia from subarctic habitats (Karlsson et al., 1991). The plants were grown in pots in natural soils in a greenhouse for 4 months. Some variants were supplied by a concentrated nutrient solution to the soil, while other variants were insect fed. Insect feeding led to a higher biomass of winter buds and a higher N and P accumulation in the buds of all four species. The same effect was attained also by soil nutrient supply in D. rotundifolia and P. vulgaris, whereas the effects on seed set and related parameters were ambiguous. On the other hand, the roots of P. villosa were found to have a low capacity for nutrient uptake. There was also a weak negative interaction between root and leaf nutrient uptake. However, only in 5 cases (out of 26), the hypothesis that plant response to feeding was higher in nutrient poor soils was supported. In contrast, the hypothesis was rejected in only one case. The other 20 cases were not significant and, thus, the hypothesis could not be supported. It may be concluded that growth of CPs can be covered by nutrients coming from only one source.
CPs differ greatly in their ability to enhance growth after nutrient supply to roots or leaves. In Drosera adelae, D. aliciae, and D. capillaris grown in a fen soil in aquaria, the shoot and root growth was markedly promoted and the total biomass rose to about 2.4 to 18 times more than that in controls. This was the result of weak nutrient supply either to the soil or on the leaves (Adamec et al., 1992; see Table III). The growth enhancement in D. capillaris was similar to that in D. adelae. Of these species, the highest growth enhancement (12-18 times) occurred in tiny seedlings of D. aliciae (initial rosette diam. 4-5 mm). It is not clear whether this growth effect was caused by very short seedlings' roots or by a high-nutrient requirement in this species, as can be deduced from the results of Small et al. (1977). Dionaea muscipula, however, was quite insensitive to leaf nutrient supply and the effect of soil nutrient supply was slightly negative (cf. Roberts and Oosting, 1958). Soil alkalization by NaHCO3 from pH 3.9 to about 5.2 was slightly positive in D. aliciae and D. capillaris but negative in D. adelae and Dionaea.
In the three Drosera species, a remarkably high efficiency of utilization of leaf-supplied nutrients for nutrient accumulation was estimated. The efficiency of utilization of single leaf-supplied nutrients accumulated in plant biomass ([total nutrient content in the leaf-fertilized plants - total nutrient content in controls] / total nutrient content supplied onto the leaves) was as follows: N, 12-47 times; P, 4-16; K, 29-114; Ca, 2-8; Mg, 15-59; Fe, 43-169 times. These numbers are only rough estimates (+50 %) as only 10 plants were in variants and literature data on nutrient content were used. Similarly, accumulation of nutrients in the biomass of the soil-supplied variant was theoretically higher (for N about 1.4 times; K, 3.4; Mg 1.8 times) than would be expected from the soil nutrient supply. In the three Drosera species, both nutrient-supplied variants had appreciably longer roots (Table III). They may therefore be capable of absorbing more nutrients from the poor fen soil, supporting more shoot growth. However, the changed root geometry cannot explain fully the effect. Obviously, the leaf (and/or soil) nutrient supply might lead to stimulation of nutrient uptake by roots.
The stimulation effect of insect feeding in CPs was proved first by Oosterhuis (1927) who found that insect-fed Drosera intermedia had contained more ash matter in its biomass than it could have absorbed from the prey. Its growth in N-, P-, K-, Ca-, or Mg-free Knop nutrient solutions or distilled water was reduced to 51-67 % of that in complete Knop solution. Thus, Ca or Mg deficiency in nutrient solution had the same retarding growth effect as that of N, P or K. However, the feeding of insects to deficient plants enabled them to recover vigorous growth in deficient solutions (160-200 % of that in complete Knop). As follows D. intermedia can absorb physiologically significant amounts of N, P, K, Ca and Mg from prey. D. capensis grown in a fen soil in a greenhouse also increased appreciably its growth due to insect feeding or soil nutrient supply (Oosterhuis, 1927).
Drosera rotundifolia can utilize both NH4+ and NO3- by roots as a N source for its growth. Rychnovská-Soudková (1954) found that when this species was grown in 1/4 strength Knop solution, the utilization of N source was greatly dependent on pH. Growth was significantly promoted by NH4+ at pH > 5.0, but inhibited by NO3-. In contrast, NO3- was used efficiently at a low pH (3.0) and NH4+ use was weak. The low pH protected the plants from a high Ca2+ concentration in the solution, whereas high Ca2+ inhibited growth at higher pH (>5.0; Rychnovská-Soudková, 1953). A similar pH effect on D. aliciae growth in NO3-- and NH4+-nutrient solutions was also found by Small et al. (1977). Aseptically grown D. rotundifolia tolerated high concentrations of both NH4Cl and NH4NO3 in nutrient solution, with growth saturated at 2.5 mM NH4NO3 (Simola, 1978).
Krafft and Handel (1991) tested the effect of insect feeding rate on D. rotundifolia and D. filiformis growth. The plants, growing outdoors and in pots containing nutrient-poor peat, were fed 0, 5, 10, or 20 flies per week for 8 weeks before the end of the first growing season. Catch of prey was excluded from the plants during the second season. In D. rotundifolia, feeding led to the increased growth rate of leaves (by 72-93 % compared to the unfed controls) in the first season, while similar results were seen during the second season (leaf DW increased by 148-198 %). Growth enhancement was fully saturated at the lowest feeding rate. In D. filiformis, however, feeding had only a weak and non-significant effect on leaf biomass during both seasons. In the second season, feeding enhanced flowering markedly, as well as production of reproductive biomass in D. rotundifolia (4.2-8.8 times), but feeding only weakly enhanced reproduction biomass in D. filiformis (34-56 %). These results confirm those of Thum (1988, 1989b) and Schulze and Schulze (1990) who demonstrated the great importance of prey in the growth and vigour of D. rotundifolia under natural conditions. In this species, a large amount of nutrients coming from carnivory is stored in winter buds and utilized for vigorous growth throughout the following season.
Sarracenia flava grown outdoors in pots in nutrient-free vermiculite for 4.5 months, increased its growth when allowed to catch prey or when its substrate was fertilized (Christensen, 1976). The plants fertilized or catching natural prey appeared to be considerably larger and robust than the controls, but numerical data are lacking. Catch of prey led to a considerable increase in leaf tissue N and P content per DW unit but K, Ca, and Mg contents were unchanged. In contrast, substrate fertilization significantly increased the content of all 5 nutrients in leaf tissue. This shows that the majority of N and P but the minority of K, Ca, and Mg, in this species, can be taken up from prey.
Uptake of some mineral ions was estimated in Heliamphora tatei and H. heterodoxa, by measuring the disappearance of ions from a solution (in mM: KCl, 1; CaCl2, 1; MgCl2, 1; NaCl, 1; NaH2PO4, 0.5; NH4Cl, 18.7) poured into their pitcher leaves (Jaffe et al., 1992). During 24 hours, 92-98 % of added P, 66-67 % of K, 28-54 % of Na, 9-30 % of Ca, and 18-32 % of Mg was taken up by the leaves. The former species took up all ions more efficiently than the latter. The results show that the species is able to take up P and K more efficiently from prey, than Na, Ca, and Mg.
Not only positive interactions exist between insect feeding and root nutrient supply in CPs. Negative interactions were shown in Drosera whittakeri, D. binata, and in pygmy sundews D. closterostigma and D. glanduligera. The growth of tuberous D. whittakeri in a nutrient-free sand culture in a greenhouse was promoted significantly by either insect feeding (by 27-51 % of controls) or root supply of a diluted nutrient solution (by ca 50 %; Chandler and Anderson, 1976a). However, omitting N or S in the solution led to a growth decrease, compared with controls, of 6-38 % and 16 %, respectively. Insect feeding did not affect the plants growing in P-free solution and promoted the growth in only NO3-- or SO42--free variants whereas it inhibited (by 20 %) plant growth in the complete solution. Thus, nitrate and sulphate in the soil solution, which are taken up by roots, interfere with nutrient uptake from insects in this species. Moreover, the growth of unfed plants in nutrient solution was quite independent of NO3- concentration within 0-1.1 mM. The negative interactions between foliar and root nutrient uptake together with total root unresponsiveness to NO3-, indicate clearly a rather limited absorbtion capacity of roots in this species. In parallel experiments, insect feeding of D. binata growing in NO3--free nutrient solution increased its biomass 3 times, while increasing the NO3- concentration (0.1-1 mM) gradually declined the effect of feeding (by 6-30 %). Unfed D. binata reacted positively on increasing NO3- concentration in the solution.
In D. whittakeri growing in complete solution, the activity of shoot nitrate reductase (NR) was about 30-50 % lower in insect-fed plants than that in unfed ones (Chandler and Anderson, 1976a). NR was distinctly inducible by NO3- in unfed plants. Thus, N-containing organic substances from insects are more effective in promoting growth than NO3-, with competition existing between these principal N sources in plants and leading to a decrease in NR activity. However, competition obviously does not occur in natural habitats where NO3- (and SO42-) is nearly lacking. In aseptically grown D. aliciae, activity of nitrate and nitrite reductase was found in both roots and shoots only when plants were supplied with NO3- (Small et al, 1977). The activity of both enzymes was 2-4.5 times higher in roots than shoots. The enzymes incorporating NH4+ into metabolism (GS, GDH, GOGAT) were present in roots and shoots in all variants.
Chandler and Anderson (1976b) demonstrated the uptake of labelled SO42- from SO42- solution that was dropped onto the leaves of D. whittakeri and D. binata grown in a greenhouse or aseptically. The label was incorporated mostly to cystein. Both species absorbed SO42-, cysteic acid and cystein from insects. P-labelling patterns in shoots were the same after leaf supply of labelled phosphate or insects (Chandler and Anderson, 1976b). It may indicate that the P form taken up from insects is mineral phosphate.
The tuberous Drosera erythrorhiza when grown in a sand culture in a greenhouse, produced the same biomass of aestivating dormant tubers even under different conditions of root nutrient supply or insect feeding. However, the nutrient content in tubers was different (Pate and Dixon, 1978). As compared to unfed plants grown in distilled water, the plants grown in a concentrated nutrient solution or eluate of litter ash, contained 25-90 % more N, 0-15 % P, 80-100 % K, and 15-25 % more Ca in their tubers. Insect-fed plants contained 60 % more N, 40 % P, and 25 % K. Simultaneous insect feeding stimulated partly N, P, and Zn uptake by roots. When grown in pots with natural calcareous soil with ash supply, unfed plant tubers' contained more N (2.2 times), P (4.7), K (2.0), Ca (3.9), Mg (l.6), and Zn (3.5 times) than those in distilled water. Thus, the species can obtain more nutrients from an ash-fertilized natural soil than from insects. Re-utilization of nutrients from senescent shoots was very efficient for P (88 %) and N (79 %), but less efficient for Mg (63 %), K (56 %), Zn (39 %), Na (37 %), and especially Ca (25 %).
The efficiency of N absorbtion (i.e. the availability of N) from Drosophila flies and its distribution in plant organs was studied in greenhouse-grown D. erythrorhiza by Dixon et al. (1980). Four weeks after feeding period ended, 24 % of the total insect N remained unused in spent insect carcasses on the leaves while the remaining part (76 %) had been absorbed by the leaves. In this way, the plants increased their total N by 44.5 %. Of the total insect N, 27 % was present in leaf rosette, 2.0 % in stem, 18 % in developing daughter tubers and rhizomes, and 29 % in new replacement tuber while no N was in old parent tuber. In senescent plants, 22 % of the total insect N was stored in daughter tubers and 48 % in the replacement one. Thus, 70 % of the total insect N (i.e. 92 % of the total absorbed N) was carried over by tubers to the next growing season. The dead leaf rosette contained only 5.6 % of N that was present in the leaf rosette in the peak summer, while the dead stem contained only 0.8 %. From 60 to 70 % of total N stored in dormant tubers was present as arginine. Obviously, a good deal of N in the spent insects was present in unavailable chitinous skeletons. D. erythrorhiza uptake of N from insects was enormously efficiently with most being stored in tubers. Moreover, its leaf and stem N and P is perfectly re-utilized and translocated to tubers so that the plant only loses a small part of N and P in senescent organs. In contrast, D. rotundifolia leaves did not absorb more than 10 % of N from a protein (Shibata and Komiya, 1972; 1973).
A total lack of response to soil nutrient supply was found in the perennial pygmy sundew D. closterostigma (Karlsson and Pate, 1992a). Its germlings raised from gemmae grew very slowly in diluted nutrient solutions, with their total N and P content about the same as in the gemmae (Table IV). Insect feeding increased the growth of all variants by about 5 times. The total N content increased 6 to 7 times, and that of P, 14 times. In contrast to stimulation of root nutrient uptake in Pinguicula (Karlsson and Carlsson, 1984), all increases of N and P in plants was the result of uptake from insects. From 56 to 65 % of the total insect N and 59 to 67 % of P was absorbed by the plants. Weak competition was found between root nutrient supply and insect feeding. Unresponsiveness of this species to soil nutrients is supported by barely detectable NR activity in plants growing in 5 mM NO3- (see Karlsson and Pate, 1992a).
It may be drawn from the above literature data that all terrestrial CPs may be loosly subdivided into three groups according to their ability to produce new biomass and accumulate mineral nutrients on the account of nutrients taken up by roots and leaves. The first group, named "nutrient-requiring species", comprises P. vulgaris, P. alpina, P. lusitanica, D. adelae, D. aliciae, D. capillaris, D. capensis, D. rotundifolia, D. intermedia and Sarracenia flava. These species increase markedly their growth due to both soil and leaf nutrient supply and their root nutrient uptake may be partly stimulated by foliar uptake (see Fig. 1A). A partial saturation effect may occur in other cases (Fig. 1B; cf. the slopes of soil-fertilized variants). Re-utilization of N and P from senescent organs is relatively inefficient. It is probable that these species grow in natural habitats with relatively higher soil nutrient content.
The second group of CPs, named "root-leaf nutrient competitors", comprises D. whittakeri, D. binata, P. villosa and probably also D. erythrorhiza. These species grow better and accumulate more nutrients thanks to both root and leaf nutrient uptake. However, their growth enhancement is usually lower than in the first plant group (Fig. 1C). Root nutrient uptake is limited. Competition occurs between root and leaf nutrient uptake. The plants efficiently re-utilize N and P.
The third group, named "nutrient-modest species", comprises D. closterostigma and perhaps also Dionaea muscipula (Fig. 1D). The roots of these species have a very low nutrient uptake capacity and rely on leaf nutrient uptake. These species live in very infertile soils.
VI. Mineral Nutrition of terrestrial carnivorous Plants in natural Habitats
Investigations of mineral nutrition of CPs under natural conditions are much less detailed than those performed in greenhouses, but they show clearly the ecological importance of carnivory, including the benefit, cost, and limitations, for natural growth and development. CPs growing in natural habitats are subjected to competition with non-CPs (e.g. Wilson, 1985), mortality (Thum, 1989b), and their prey can be robbed by opportunistic predators (Thum, 1989a; Zamora, 1990). The nutrients released from insect carcasses may be washed out by rain or even whole prey completely washed away by heavy rains (Karlsson et al., 1987).
The importance of carnivory for seasonal gain of N, P, and K and nutrient economy were thoroughly studied in three Pinguicula species growing in northern Sweden (Karlsson et al., 1987; Karlsson, 1988; see Table V). The nutrient losses in senescent leaves and roots (estimated as the total summer nutrient content minus that of winter buds, minus that in reproductive organs) expressed in % of the total summer nutrient content, ranged between 11-44 % for N, 19-59 % for P, and 29-75 % for K (Karlsson, 1988). Greater losses of N and P usually occurred in non-flowering specimens. Of the total summer nutrient content, 56-63 % N, 41-47 % P, and 26-66 % K were re-utilized and stored in winter buds in non-flowering specimens. On the basis of measured seasonal rate of catching prey, plant nutrient content, literature data on prey nutrient content, and assuming a 75 % efficiency of nutrient uptake from prey, Karlsson et al. (1987) were able to estimate the proportion of the total summer nutrient content derived from catching prey (Tab. V). The proportion is high for N (17-63 %) and P (31-91 %) but low for K (4-29 %). However, the three species' uptake from prey can be as high as 32-100 % N, 43-100 % P, but only 5-82 % K of the estimated seasonal nutrient gain (i.e. nutrient consumption; Karlsson, 1988; cf. Karlsson et al., 1994; Tab. V). As follows a higher seasonal nutrient consumption in flowering specimens is less compensated by the nutrient uptake from prey than in non-flowering CPs. The relatively low values in P. alpina were due to its lower catch of prey (Karlsson et al., 1987). Since the catch of prey was highly variable among individuals or populations (up to 10 times) the contribution of carnivory to the seasonal nutrient gain was also highly variable among individuals. This might lead to size differentiation within a CP population.
In accordance with greenhouse-grown plants (Oosterhuis, 1927; Krafft and Handel, 1991), the seasonal growth of D. intermedia and D. rotundifolia in a peat bog was greatly dependent on the quantity of supplied prey (Thum, 1988). As shown in Tab. VI the fed plants of both species produced 3.5-5 times more summer biomass than the plants with natural catch of prey. At the same time, there was a proportional increase in the biomass of winter buds (21-38 % of the summer DW increase). Though vegetative growth was promoted to the same extent in both species, flowering and seed set differed greatly between species which were fed (Tab. VI). In adult D. intermedia plants, flowering and seed set increased proportionally with vegetative growth, whereas they were highly stimulated (68-192 times) in fed D. rotundifolia. However, these findings do not prove an extraordinary feeding role for flowering of D. rotundifolia because of the small size of tested unfed plants (rosette diam. 2.6 cm) which rarely flowered. Due to feeding, they exceeded the minimum size necessary for flowering and then flowered abundantly. Thus, the use of prey in D. intermedia and D. rotundifolia leads to greater plant size, and therefore leaf trapping area, which further allows the catching of more prey (positive feed-back).
Thum (1988) also found that 1 mg DW of the supplied prey, led to a summer biomass increase of 6.5 mg in D. intermedia and 2.9 mg in D. rotundifolia. Since 5 % of freshly supplied preys were robbed by opportunistic predators in the former species and 71 % in the latter within the first 24 hours, 1 mg DW of digested prey led to an increase in summer biomass by 6.8 mg and DW of winter buds by 2.6 mg in D. intermedia and by 10.0 and 2.1 mg in D. rotundifolia, respectively. Taking into account the data on nutrient content of prey (Watson et al., 1982) and D. rotundifolia plants (see Table I) and assuming a 76 % nutrient availability from prey (sensu Dixon et al., 1980), the increased summer biomass can contain 92 % N, 100 % P, and only 1.6 % K from the prey in D. intermedia and 63 % N, 95 % P, and 1.1 % K in D. rotundifolia. In winter buds in both species (N, 2.92 % of DW; Schulze and Schulze, 1990), 99-100 % of the increased N can be taken up from prey. Natural seasonal catch of digested prey (0.20 mg DW per 1 mg-1 of plant DW) was estimated in both species in a southern German bog (Thum, 1989b). Based on the above assumptions, 100 % of the total summer plant N and P, but only 2.2 % of K content could be taken up from prey. Thus, both Drosera species can take up theoretically 100 % of the seasonal N and P gain and only a negligible fraction of K from prey. These results are comparable with those for D. erythrorhiza (Watson et al., 1982) and for three Pinguicula species (Karlsson, 1988; Table V). All these results show clearly that uptake of N and P from seasonally caught prey is of principal importance for nutrient economy in natural CP populations of various taxa and that catch of prey by CPs markedly stimulates K uptake by roots. Thus, K may be the most limiting nutrient for the vigorous growth of CPs under natural conditions of abundant prey.
A strict dependence of plant size on quantity of supplied Drosophila flies was found in D. rotundifolia growing outdoors in big cubes of natural peat for 15 weeks and watered by rain water (Schulze and Schulze, 1990). Big plants totally deprived of prey reduced their leaf area to 26 % of their initial size. The plants fed on one and two flies per new leaf attained 1.73 and 2.98 times higher leaf area, respectively, than that of unfed ones. Similarly, the plants of different size groups attained the same size after having been fed on one fly per new leaf. The faster growth of fed plants was connected with a faster production of new leaves, but this process was counterbalanced by accelerated leaf ageing and decay. The faster turnover of leaves of fed plants represented one of the physiological costs of carnivory. Since the efficiency of nutrient re-utilization from aged leaves was obviously low in D. rotundifolia, the unfed plants markedly reduced their size. Feeding of plants also resulted in larger winter buds (184 % of unfed controls) and increased N content per DW unit. As estimated by these authors about 24-30 % of the total N in winter buds originated from insects.
As opposed to the results of Oosterhuis (1927) and Thum (1988), the seasonal growth of D. intermedia in natural nutrient-rich fen in southern Canada, was quite independent of natural prey catch only when grown in isolation (Wilson, 1985). The plants deprived of prey and grown in contact with a potential competitor (Lysimachia terrestris) produced 41 % less biomass than the controls which caught prey. These results suggest that insectivory may be important for reducing the effect of interspecific competition. A shading effect of the competitor might be overcome by the uptake of organic substances from prey. In a three-year growth experiment in a Sphagnum fuscum-dominated subarctic bog, soil fertilization (NH4NO3; 4 g N.m-2.year-1) of D. rotundifolia led to a moderate increase in stem height, leaf thickness, leaf number and leaf DW per plant, but leaf area per plant was unchanged (Svensson, 1995). Stem enlargement helped the plants to avoid being overgrown with the Sphagnum moss.
The importance of the natural catch of prey, in field experiments in southeastern USA, was confirmed by Gibson (1983). When CPs from several species (Dionaea muscipula, Drosera intermedia, D. filiformis var. tracyi, Sarracenia leucophylla, S. flava, Pinguicula spp.) caught more prey, they produced more total biomass, as well as flowers and seeds. Moreover, when these plants (except Dionaea) were fed insects at about three times the rate of normal prey capture, they grew faster, flowered more richly, and survived longer than control plants and plants without prey. As well, both Drosera species reproduced more asexually.
In contrast with the findings of the above authors and Rychnovská-Soudková (1954), evidence was also given which implies a negative influence of insect feeding and soil nutrient supply on D. rotundifolia growth (Stewart and Nilsen, 1992). Plants growing in a nutrient-rich peat bog (in mg.kg-1 soil DW: NH3, 20-150; P, 2-3) in Virginia, USA, were treated by supplemental insect feeding (one fly.month-1), prey deprival, urea (170 g N.m-2), phosphate (195 g P.m-2) soil supply, or by combination of N and P. The doses of fertilizers were excessive, highly extending those applied by Eleuterius and Jones (1969) and Svensson (1995). The soil N and P concentrations extended those in control soil by 5-15 times. Insect feeding increased flowering moderately, but the total plant biomass was 19 % lower than the controls which were naturally catching prey. Similarly, prey deprival led to a 20 % increase in total plant biomass. Soil supply of N strongly inhibited flowering and led to a 26 % reduction of total plant DW and to a 60 % reduction in the case of P supply. The reduction of winter bud DW, due to different treatments, was about proportional to that in summer plant biomass. Soil N supply increased the N tissue content in summer plants by 2.8 times compared to the controls, while P supply increased the P tissue content by 3.57 times. Insect feeding had no significant effect on N and P tissue content. Fertilized plants (and to a lesser extent also insect-fed ones) retained N and P from summer biomass less efficiently in their winter buds. This study confirms that D. rotundifolia is very plastic as to the source of macronutrients it requires for growth. Uptake by roots from nutrient-rich soils can fully saturate the plant with nutrients so that catch of prey has no or even negative effects on plant growth. Although the species was classed to "nutrient-requiring species" (see chapter V.), high-nutrient conditions may reduce its growth. This is most probably due to excessive accumulation of N (to 7.5 % of DW) and P (to 2.4 %) in plants (cf. Tab. I).
The effect of leaf nutrient and insect supply was tested on growth of Sarracenia purpurea in a Minnesota fen, USA (Chapin and Pastor, 1995). Over the course of 16 weeks and in 2-week intervals, a total of either 4 ml of 157.6 mM NH4Cl, 35.5 mM KH2PO4/K2HPO4, both N and P, 20 ml of microelement solution (either alone or with N or P), or up to 1.0 g of dried insects was applied to each pitcher leaf. The leaves were prevented from catching natural prey. The total amount of N and P applied was 10 times greater than the maximum N and P amount received from the seasonal catch of prey. The amount of insects applied to each leaf was also 10 times greater than the maximum amount of caught insects (see Wolfe, 1981). Aboveground plant DW, number of leaves produced per season, and mean leaf DW did not differ significantly among treatments (Chapin and Pastor, 1995). However, all applications of N and insect feeding led to a significant increase in N content per leaf DW, when compared to the unfed controls. N application also promoted a significant P accumulation in the leaves, however, P application did not enhance N accumulation, in contrast with the results of Karlsson and Carlsson (1984). P content per leaf DW and the total P content were 5.5-7 times higher in all P treatments than in the controls but insect feeding had no effect. Microelements alone, in combination with N, P or natural catch of prey, did not significantly increase N and P accumulation.
The authors also found that the fen soil, with the rhizome and roots of one plant (ca 27 l), could supply the roots with up to 1.05 g NH3-N per season, while the total rainwater N input into the pitchers was negligible. In summary, the plants can take up only about 5 % of their total N and P content from natural prey per season, due to low seasonal catch of prey (ca 80 mg prey DW.g-1 aboveground plant DW). Furthermore,, catch of prey does not lead to a significant increase in plant growth or N and P content (cf. Karlsson et al., 1987; Thum, 1988, 1989b). Soil N is the main N source for S. purpurea growth.
Naturally growing D. erythrorhiza was found as compensating about 11-17 % of the seasonal N gain by prey in one case (Dixon et al, 1980) but 100 % N and P and only 2-3 % K in another (Watson et al., 1982). Tentacle-free phenotypic variant of this species appeared as vigorous and as high in N as did the normal plants (Dixon et al., 1980). It is possible that root uptake of N became more active in this variant.
Using natural 15N distribution, Schulze et al. (1991) investigated the proportion of prey-derived N in summer biomass of CP species of different growth forms, growing naturally in SW Australia. Rosette species (D. erythrorhiza, D. macrophylla, D. zonaria, D. bulbosa, D. glanduligera, D. dichrosepala, D. pulchella) were found not to take up N from prey. This presumably results from the low sensitivity of this method and shows that the real N proportion from prey would be low in this growth form. However, when a tentacle-free phenotypic variant of D. erythrorhiza was used as a reference plant, 12-32 % of prey-derived N was found in the normal D. erythrorhiza. Unlike rosette species, the proportion of prey-derived N was 37-57 % in erect low species (D. huegellii, D. menziesii, D. stolonifera), 49-65 % in erect high species (D. gigantea, D. heterophylla, D. marchantii), 35-87 % in vine species (D. macrantha, D. modesta, D. pallida, D. subhirtella), about 47 % in Cephalotus follicularis, and about 21 % in semi-terrestrial Polypompholyx multifida. Obviously, these numbers indicate relative trapping efficiencies of CPs with different growth forms.
A perennial pygmy sundew D. closterostigma grown in a greenhouse was totally inert to soil nutrient supply and the same also held for natural habitats in W Australia (Karlsson and Pate, 1992a; cf. Table IV). Over the season, the insect-fed plants attained 52-57 % higher biomass, 21-272 % higher total N and 95-107 % higher total P content than the unfed plants which caught only natural prey. The higher values held for small first-season germlings from gemmae, whereas adult plants were less dependent on feeding. The proportion of flowering plants was also 50 % higher in fed plants. Although a naturally growing non-gemmiferous pygmy annual D. glanduligera was able to increase moderately its biomass, as well as its total N and P content due to soil nutrient supply, the effect of feeding had the most effect (Karlsson and Pate, 1992a; see Table VII). Competition between soil nutrient supply and feeding took place. In this annual species, 59 % of total N and 65 % of total P was stored in seeds (Karlsson and Pate, 1992b). The authors found that in the gemmiferous perennial pygmy Drosera species, 60 % of total N and 38 % of P was on average allocated to gemmae in rosette form species and only 20 % N and 23 % P in micro-stilt form species. In all perennial pygmy species, only 1-6 % of the total N and 1-8 % of P was stored in seeds but 9-40 % of the total N and 7-32 % of P content was lost in dead inflorescences. Thus, N and P re-utilization in pygmy Drosera species was less efficient than in rhizomatous D. erythrorhiza (cf. Pate and Dixon, 1978).
It is difficult to compare growth effects of soil nutrient supply and/or insect feeding (catching) in CP species under greenhouse and natural conditions, primarily because of different nutrient levels in substrates and different insect-feeding (catching) rates in various studies. As with experiments on terrestrial CPs, their growth in natural habitats showed that they could utilize more prey to promote growth than they really catch (Dixon et al., 1980; Gibson, 1983; Karlsson et al., 1987; Karlsson, 1988; Karlsson and Pate, 1992a; Thum, 1988; Krafft and Handel, 1991). Therefore, the quantity of caught prey is mostly a major factor for the vigour of CP populations. Catching of prey is evidently much more important for seedlings and small juvenile specimens with shorter roots than for big adult plants (Thum, 1988; Karlsson, 1988; Karlsson and Pate, 1992a; Adamec et al., 1992). In juvenile specimens, catching prey is limited but leads to faster growth, earlier maturity, and abundant flowering and seed set. Catching prey probably promotes flowering in adult specimens to the same extent as vegetative growth, but it accelerates the rate at which minimum plant size necessary for flowering is reached (Thum, 1988; Karlsson et al., 1991; Karlsson and Pate, 1992a). On the contrary, small naturally growing specimens of D. rotundifolia are even supposed to die when permanently deprived of prey (Schulze and Schulze, 1990).
It was estimated for several naturally growing terrestrial CPs, that they were able to take up their (almost) total seasonal gain (consumption) of N and P from carnivory, but only a small proportion of their K, and perhaps also Ca and Mg (Christensen, 1976; Watson et al., 1982; Thum 1988, 1989b; Karlsson, 1988). However, the efficiency of absorbtion of P, K, Ca, Mg, and other nutrients from prey carcasses in laboratory is still unknown and the same holds for the efficiency under natural conditions. Due to many factors (robbing of prey, washing away of preys and nutrients by rain), it is obvious that the natural efficiency of nutrient absorbtion from prey is much lower than that in greenhouses (e.g. Thum, 1988). The role of microelements in carnivory is still unclear.
A typical feature of CPs is relatively high efficiency of N and P re-utilization from aged plant organs. This is also higher than that in other accompanying non-CPs (Karlsson, 1988). Yet, considerable differences exist between CP species in their efficiency of N and P re-utilization from aged leaves and stems. As opposed to the very efficient N and P re-utilization from D. erythrorhiza shoots (Pate and Dixon, 1978; Dixon et al., 1980), European Pinguicula and Drosera species as well as Australian pygmy Drosera species lose a good deal of the total N and P content in their senescent biomass (Karlsson, 1988; Karlsson and Pate, 1992b; Thum, 1988; Schulze and Schulze, 1990). It is apparent that these differences in nutrient economy among CPs are caused partly by different leaf turnover rates which are higher in D. rotundifolia (Schulze and Schulze, 1990) than in D. erythrorhiza (Pate and Dixon, 1978; Dixon et al., 1980).
VII. High-nutrient conditions
Some CPs may reduce their growth and even die when grown in nutrient enriched soils (see Juniper et al., 1989, p. 134). Dionaea muscipula grew very poorly in a conventional clay-loam garden soil (Roberts and Oosting, 1958). The leathery leaves did not develop traps and flowering was greatly reduced. After 5 months, most plants were dead. Similarly, when grown in a fertilized greenhouse potting soil, roots of Dionaea were atrophied, no new roots formed, and plants died within 70 days. In another experiment, the growth of Dionaea in a sand culture with mineral nutrient solution was poor; plants declined in weight, and died after about 3 months, while the controls watered with distilled water grew much better. The insect- or protein-fed plants showed more vigorous growth than the controls. As follows Dionaea is very susceptible to higher soil nutrient level and its root growth is suppressed in heavier soils (cf. Adamec et al., 1992). Eleuterius and Jones (1969) studied the growth of Sarracenia alata in a southern Mississippi bog and found a growth decrease in fertilized bog soil (seasonal supply of 37.1 g N.m-2 and 5.9 g P.m-2; cf. Stewart and Nilsen, 1992; chapter VI.). Possible negative effects of nutrient-rich soils on the growth of Nepenthes were discussed by Juniper et al. (1989, p. 134).
These findings demonstrate that higher nutrient levels in soils may inhibit growth of some CPs (mainly root growth). Due to shortage of data, it is not clear whether this effect is confined only to some species or whether it is an extreme consequence of the above stated competition between root and leaf nutrient conditions (sensu Chandler and Anderson, 1976a) or of an unsuitable pH (cf. Rychnovská-Soudková, 1953, 1954). However, many CP species including Dionaea may grow vigorously in rather concentrated nutrient solutions (e.g. Small et al., 1977; Simola, 1978; Aldenius et al., 1983) and are generally able to tolerate these conditions. On the other hand, CPs growing in nutrient solutions in vitro lose some features of carnivory. For example, in-vitro grown D. capillaris formed non-functional tentacles, while Dionaea formed immobile leaf lobes (Adamec, unpubl.). Thus, the development of carnivory is partly blocked under high-nutrient conditions.
VIII. Mineral Nutrition of aquatic carnivorous Plants
Aquatic CPs of the genera Utricularia and Aldrovanda usually grow in shallow standing waters with certain concentration of humic acids and tannins (i.e. dystrophic waters). The waters are usually nutrient poor and the concentration of inorganic N (NH4+, NO3-) may be <150 µg.l-1, inorganic P <50 µg.l-1, and K <1 mg.l-1 (Komiya, 1966; Kaminski, 1987a,b; Kosiba, 1992a, 1993; Akeret, 1993). In waters not impacted by human activity, the concentrations may be as low as 1-2 µg N.l-1, 2 µg P.l-1, and 0.01 mg K.l-1 (Friday, 1989; Akeret, 1993; Kosiba, 1993). The majority of aquatic CPs usually grow in soft or medium-hard, acid or neutral, waters, but some temperate-zone species may grow in hard and slightly alkaline waters (Komiya, 1966; Moeller, 1978; Kadono, 1982; Fraser et al., 1986; Kaminski, 1987a; Arts and Leuven, 1988; Hough and Fornwall, 1988; Kosiba and Sarosiek, 1989; Kosiba, 1992a, 1993; Akeret, 1993; Adamec, 1995a, 1996). The accumulation of partly decomposed nutrient-poor plant litter is common in aquatic habitats of CPs (e.g. Kaminski, 1987a). The litter releases humic acids and CO2. A very high CO2 concentration between 0.1-0.6 mM occurs commonly in aquatic habitats of CPs (Komiya, 1966; Akeret, 1993; Adamec, 1995b, 1996).
All aquatic CP species are rootless and either float freely below the water surface or are loosly anchored by their trapping shoots in sediments; some species are amphibious. They take up all necessary nutrients through their shoots, either from the water or from prey. As opposed to all terrestrial CPs, aquatic CP species show a very fast apical growth and produce as much as 1-2.8 new leaf whorls per day (Lloyd, 1942; Friday, 1989). The basal end is permanently subjected to senescence and decomposition. They seem to tolerate high concentrations of humic acids and tannins in water. Humic acids were found as being essential for normal growth and development in A. vesiculosa (Ashida, 1937; Kaminski, 1987b) and U. vulgaris (Kosiba, 1992b) but facultative in other species (Pringsheim and Pringsheim, 1967; see Lüttge, 1983). All aquatic CPs tested so far, can only use free CO2 (not HCO3-) for photosynthesis. Their photosynthetic CO2 compensation points range within 1.5-7.2 µM (Moeller, 1978; Adamec, 1995a, 1996). Similar values of 1.5-10 µM CO2 are reported generally in aquatic non-CPs (cf. Maberly and Spence, 1983).
The growth of some aquatic Utricularia species in aseptic cultures was promoted considerably by organic substances with or without N (Harder, 1963, 1970; Pringsheim and Pringsheim, 1967; see below). In U. gibba, grown aseptically in a concentrated mineral medium without either Mg or K for 8 weeks, feeding on protozoa promoted its growth and overcame fully the deficiency of K but only partly that of Mg (Sorenson and Jackson, 1968). Moreover, feeding also markedly promoted the production of new bladders. However, the growth effect of feeding was only slightly positive in complete medium.
Kosiba (1992a) cultivated apical shoot segments of U. vulgaris in aquaria in a greenhouse in various mineral nutrient solutions for 3 weeks and found that the plants grew best in Knop nutrient solution diluted 4-8 times. In similar aquaria experiments with pond water at different pH, the growth of Daphnia-fed plants was higher than that of unfed plants at only higher pH values of 7.6-9.1 (cf. Kosiba, 1992a,b). Moreover, the fed plants produced more and longer lateral shoots at higher pH than did unfed plants. The positive growth effect of feeding at higher pH shows a partial substitution of a limited CO2 source by organic carbon from Daphnia. When grown in diluted Knop nutrient solution the fed plants were larger and more branched than the controls (Kosiba, 1992b). Knight and Frost (1991) found in plants of U. vulgaris (syn. U. macrorhiza) growing in lakes in Wisconsin that the number of bladders per leaf was very plastic and correlated positively with electrical conductivity of lake water (caused mainly by HCO3- and Ca2+). A slight mineral enrichment of lake water doubled the number of bladders per leaf whereas with feeding on zooplankton there was an insignificant reduction.
Friday and Quarmby (1994) fed 15N- and 32P-labelled mosquito larvae to leaves of known age in U. vulgaris under near-natural conditions. Prey-derived 15N was rapidly taken up and translocated. In plants, where prey was fed to 3-day old leaves, about 30 % of the prey 15N appeared in the immature parts of the plants within 2 days. Almost all parts of the plants which were immature at the time of feeding received prey 15N and stored it during the next 20 days. Calculations for the 3-day plants suggested that about 83 % of the total 15N in the prey had been still present in the plants 14 days after feeding and about 75 % after 20 days. 32P was also taken up and translocated rapidly, but it was not stored in young tissues after their maturation. Backward translocation of 32P was observed into lateral shoot apices and flowers arising on parts of the plants older than the fed leaves. Thus, P was better re-utilized in the plants than N. Knight (1988) estimated that this species could compensate up to 75 % of its seasonal N gain by carnivory. The plants deprived of prey grew poorly. Rapid uptake of 32P from zooplankton was demonstrated in U. inflata shoot segments (Lollar et al., 1971). Two days after feeding on labelled prey, high radioactivity was found in leaves and stems. Thus, aquatic Utricularia species can take up a considerable proportion of both N and P from prey.
Aldrovanda vesiculosa is an aquatic CP with the steepest growth polarity between the apex and senescent basal end. Kaminski (1987a) cultivated apical segments of A. vesiculosa in aquaria in a greenhouse in a diluted mineral nutrient solution and found that the plants had grown best in 5-7.5 times diluted solution and at 5 mg.l-1 of humic acids. Feeding plants on zooplankton promoted plant growth by 170 %. The same effect was also found after addition of Carex rhizomes to aquaria (Kaminski, 1987b; see Table VIII). The positive effect of Carex rhizomes on A. vesiculosa growth was probably caused by a release of CO2 and some organic substances. A synergistic growth effect was found when feeding was combined with the addition of rhizomes. Addition of other wetland plants also promoted its growth.
Ion uptake by A. vesiculosa shoots was studied in 6-8-hour experiments (Adamec, unpubl.). The light uptake of NH4+ from 15 or 30 µM NH4NO3 was the same in both apical and basal parts and about 6 times higher than NO3- uptake. NH4+ uptake was observed overnight, but NO3- was not. Phosphate was taken up by apical parts about twice faster than basal parts. However, K+ was only taken up by basal parts and its uptake rate by intact plants was about a half of that by basal parts. Thus, A. vesiculosa prefers NH4+ to NO3-, while K+ is only taken up by shoot bases and then translocated to apices. N, P, and Ca content per DW unit in shoot segments of different age shows a distinct polarity in A. vesiculosa (Adamec, unpubl.). N content per DW unit in apices was about 13 times higher than that in the last living whorls and 4.8 times higher in the case of P; the polarity of Ca content was the reverse whereas K and Mg contents were constant along the shoots. Presumably, the plants permanently lose a small part of N and P in their senescent biomass, but a majority of K, Ca, Mg, and Na. U. purpurea, however, lost as much as 63 % of the original content of N and only 29 % of P in senescent shoot segments (Moeller, 1980).
It therefore seems that aquatic CPs are considerably (or even strictly) dependent on organic substances in water. Catching of prey significantly promotes their growth and it may be concluded that carnivory is ecologically very important in these plants. To ensure their fast apical growth, loss of nutrients in senescent organs must be compensated by a permanent nutrient uptake from water or prey.
IX. Organic Nutrition of carnivorous Plants
As stated above, all CPs are green and able to fix CO2 (Lüttge, 1983). Givnish et al. (1984) assume that mineral nutrient uptake due to carnivory should achieve positive photosynthetic benefits, as compared to the costs of carnivory, only in nutrient-poor, sunny, and moist habitats whereas negative photosynthetic benefits would occur in shady habitats. However, under shade conditions or at low CO2 availability, the resultant negative photosynthetic benefits in CPs are counterbalanced by organic carbon uptake from prey. This point has partly been underestimated (Givnish et al., 1984). Obviously, the release of mineral nutrients (N, P, S, K, Ca, Mg) from prey carcasses in traps concurs with enzymatic disintegration of organic macromolecules in prey. If the organic substances released from prey were not absorbed by traps, the traps with prey could putrefy. Three types of evidence for direct utilization of organic substances from prey carcasses or aquatic medium have been presented in CPs so far: a) uptake of labelled organic substances or 14C from labelled prey by traps, b) promotion of CPs' growth by catching prey at CO2 shortage, and c) strict requirement for organic substances in water in some aquatic CP species for growth and development.
Uptake of many organic substances by traps and spreading of the absorbed substances within plants was observed in many CP species (for the review see Lüttge, 1983; Juniper et al., 1989, p. 207-226). Traps of CPs were found to absorb all aminoacids, some dipeptides, and urea (e.g. Plummer and Kethley, 1964; Lüttge, 1965; Chandler and Anderson, 1976b). Both the uptake affinity and capacity for aminoacids are high. The uptake of alanine by Nepenthes pitchers was faster than that of phosphate and sulphate at the same concentrations, and within 1-10 mM (Lüttge, 1965). High capacity for uptake of aminoacids was found in S. flava traps (Plummer and Kethley, 1964). Nearly all aminoacids added to the traps were absorbed completely within two days and found in other organs. In pitcher leaves of Heliamphora tatei and H. heterodoxa, about 50 % of added alanine and valine was absorbed within one day (Jaffe et al., 1992). The absorbed aminoacids are metabolized readily to a variety of compounds (Lüttge, 1964).
D. capensis and A. vesiculosa absorbed organic substances from 14C-labelled Daphnia prey (Fabian-Galan and Salageanu, 1968). In D. capensis, the absorbed substances were spread within the whole plant whereas in A. vesiculosa they were translocated almost entirely from mature traps to the growing apex. Yet, this species loses a substantial amount of sugars (starch, sucrose, glucose, fructose; ca 14 % of DW) in senescent shoot segments (Adamec, unpubl.). About 47 % of the total 14C from labelled flies was stored in daughter and replacement tubers of D. erythrorhiza two months after feeding (Dixon et al., 1980). Since at least a part of 14C absorbed from flies could be released by respiration or remain in senescent shoots, the real efficiency could be higher. Thus, the efficiency of N absorbtion from prey (76 %) may not differ distinctly from that of organic carbon in this species. This view is supported further by Ashley and Gennaro (1971). They found that intact plants of Drosera sp. had absorbed 80 % of 14C from labelled flies within 24 hours, but only 12 % in excised leaves.
In aquatic CPs, the role of organic carbon absorbed from prey may be ecologically important, mainly under the conditions of CO2 or light limitation. A. vesiculosa is able to take up a substantial amount of organic substances from its prey. Plants with prey were able to grow slowly also in alkaline fen pool water (pH 9.1-9.3), the CO2 concentration of which was evidently lower than their CO2 compensation point. (Adamec, 1995b). Similarly, the growth of U. vulgaris fed on Daphnia was promoted when there was a CO2 shortage in water (Kosiba, 1992a,b). However, insect-fed D. whittakeri was not able to grow at a very reduced irradiance (1.5 W.m-2; Chandler and Anderson, 1976a). It is obvious that any estimates of an ecological role of absorbtion of organic carbon from prey in CPs should be based on the relative amount of prey caught. Thum (1988) found a net biomass increase of 6.8 mg in D. intermedia and 10.0 mg in D. rotundifolia due to feeding on 1 mg of insects. Assuming a 50 % absorbtion of organic carbon from insect carcasses and about the same C content in both CPs and insects, only 7.4 % of C in plant biomass might be compensated by insects in the former species and 5.0 % in the latter one. A natural seasonal catch of 0.2 mg prey per mg of plant biomass in these two species (Thum, 1989b) might gain about 10 % of the plants' organic carbon.
Some aquatic CPs strictly require humic acids for normal growth and development (see above), while other species (U. minor, U. ochroleuca) only grow in a mineral medium with traces of peptone, beef extract, glucose or acetate (Pringsheim and Pringsheim, 1967). It is not clear whether humic acids act in these species as a supplementary source of N (or C), or facilitate uptake of other mineral nutrients, or act as exogenous growth regulators (see Kaminski, 1987b). Because N-containing peptone or beef extract always promoted CP growth most efficiently, it is possible to assume that some aquatic CPs are not able to obtain their total N gain from mineral forms alone. Moreover, when grown in the presence of humic acids and tannins in water, they are adapted to absorbing a variety of organic substances by their shoots. Some species may also grow heterotrophically in darkness (Harder, 1970).
X. Inspiration for further Research
To fill the gaps in our understanding the processes of mineral nutrition of CPs, it is recommended to consider the following directions of research.
1) Nutrient uptake by roots of CPs has only been demonstrated in growth experiments as an increase in total nutrient content in plants. Basic properties of ion uptake need to be studied in isolated roots (root segments): e.g., uptake affinity for different mineral ions; uptake capacity; active and passive transport processes; effect of different soil nutrient level.
2) The interactions between root and leaf nutrient supply have only been observed at the level of intact CP growth. Ion uptake properties of intact and excised roots of CPs need to be studied in plants being fed on insects or fertilized by particular nutrients on the leaves. It is expected that uptake rates of K, Ca, and Mg in roots might be stimulated by feeding.
3) Generally, radial transport of ions in roots and long-distance translocation of ions in xylem of roots and shoots are correlated closely with water flow in plants. Basic properties of water relations should be studied in CPs: e.g., water uptake by roots; transpiration stream; and transpiration coefficient.
4) Roots of most CP species grow in hypoxic or anoxic soils at low redox potential but adaptation to these factors has not yet been studied.
5) The efficiency of absorbtion of mineral nutrients (N, P, S, K, Ca, Mg, microelements) and organic carbon from prey carcasses by CPs should be studied under natural conditions.
6) The extent of re-utilization of mineral nutrients and organic carbon from senescent leaves and stems of CPs should be studied under both greenhouse and natural conditions.
XI. General Conclusions
Plant carnivory developed as an adaptation to growth in nutrient-poor and wet or waterlogged soils, in which normal root functions are endangered. As shown in greenhouse growth experiments, all CP species respond positively to insect feeding. Uptake of N, P, S, K, Ca, and Mg from insect carcasses has been shown. Positive as well as negative interactions occur between root and leaf nutrient uptake in CPs. According to these interactions and CPs' ability to respond to soil or leaf nutrient supply, CP species may be subdivided into three ecophysiological groups which reflect partly an adaptation of species to different soil nutrient availability, plant growth strategy, and degree of nutrient re-utilization from senescent organs. Positive interactions between root and leaf nutrient uptake are caused presumably by stimulating absorbtion capacity of roots by nutrients derived from prey (mainly phosphate).
The growth of CPs in greenhouse experiments is not comparable with that occurring under natural conditions (robbing of prey, washing away of prey, plant competition, etc.). Catching of prey is the most important factor influencing the vigour of CPs in natural habitats. Terrestrial CPs can usually take up over 50 % of their seasonal N and P gain from prey but most K, Ca, and Mg must be taken up from soils by roots. Thus, these cations may be limiting for vigorous growth of CPs. Obviously, the root uptake of K, Ca, and Mg is greatly stimulated by nutrient(s) coming from prey. Under high-nutrient conditions, the growth of some CP species is poor and plants lose their features of carnivory. A typical feature of both terrestrial and aquatic CPs is relatively efficient re-utilization of N and P from aged organs.
Aquatic CPs are adapted mainly to low concentration of mineral nutrients (N, P, K) but relatively high concentrations of humic acids and tannins in waters. They require facultatively or strictly organic substances in water and their mineral nutrient as well as organic carbon uptake from prey is ecologically very important for growth. Traps of terrestrial CPs efficiently absorb aminoacids from prey, but absorbtion of organic carbon from prey may only be of minor ecological importance.
CPs are ecologically rather variable and lie along a gradient from almost total dependence on, to relative independence of, prey diet for their growth, natural occurrence and spread. This holds for utilization of both mineral and organic nutrients from prey. The Goebel's conclusion on carnivory, based on laboratory studies on D. rotundifolia, may be generalized as follows: carnivory is not indispensable for greenhouse growing CPs, but it is almost indispensable for CPs in natural habitats.
This paper is dedicated to Dr. Miroslav Dvoøák (Charles University, Prague, Czech Rep.). This study was supported in part by the Grant Agency of the Academy of Sciences of the Czech Republic (project No. 605401). Thanks are due to Drs. Leo Klime (Tøeboò, Czech Rep.), Jana Èernohorská, and Miroslav Dvoøák (Prague, Czech Rep.) for critically reading the manuscript. Sincere thanks are due to Dr. Naomi Rea (CSIRO, Darwin, Australia) for language correction.
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Figure 1. The schematic comparison of responses of CPs to insect feeding or catching prey alone (solid line) or soil nutrient supply (dashed line) with or without feeding. The responses are expressed in relative units either as a change in biomass or as total nutrient content in biomass. x-axis, relative units of prey quantity; 0, no feeding; 1, feeding or catching prey. A and B, "nutrient-requiring species" (A, stimulation effect; B, saturation effect); C, "root-leaf nutrient competitors"; D, "nutrient-modest species".
Macronutrient composition of some CPs. Mean values in g.kg-1 (DW). A, terrestrial species; B, aquatic species.
Species Organ N P K Ca Mg Ref.
A. Drosera rotundifolia whole pl. 12
0.8 10 1 2.8 1
Pinguicula vulgaris -"-
7 0.7 2.5 -- -- 2
Sarracenia flava leaf 9 0.6 8 1.4 1.9 3
B. Aldrovanda vesiculosa shoot 28
10.8 15.0 16.8 8.0 4
Utricularia vulgaris shoot
25 1.9 17.3 15.2 5.3 5
References: 1, Slater (1981); 2, Karlsson (1988); 3, Christensen (1976); 4, Kaminski (1987a); 5, Kosiba (1992a)
Effects of mineral nutrients applied on the leaves of Pinguicula vulgaris and insect feeding (IF) of the plants grown in fen soil in a greenhouse for 47 days. Little blocks of agar gel impregnated with mineral solution were applied on the leaves weekly. They contained 0.5 % N as NH4NO3 (variant N) or 0.1 % P (P) or micronutrients (M) or mixture of N+P (NP) or N+P+M (NPM); control, agar with distilled water. Reproduction DW is the sum of DW of flower stems and flowers. Mean values are given only for the controls and relative values as a % of the controls, for all variants. Modified after Karlsson and Carlsson (1984).
Treatment (% of the control)
Parameter Controls N P M NP NPM IF
Total DW 37.3 mg 110 145 113 131 134 133
Root DW 2.2 mg 128 157 114 148 133 141
Leaf DW 18.0 mg 134 211 159 180 180 182
Reprod. DW 12.3 mg 108 114 84 141 111 112
N content 0.48 % DW 124 86 107 83 134 75
P content 0.13 % DW 106 105 77 88 153 104
Total N 103 µg 169 176 151 142 177 146
Total P 58.9 µg 109 143 90 115 192 132
Effect of mineral nutrient solution supplied to fen soil (NS-S) and/or dropped onto the leaves (NS-L) on longest root length and biomass production in Drosera adelae (A) and D. aliciae (B) after 217 days of growing in aquaria. C, controls. Modified after Adamec et al. (1992).
Root length DW (mg)
Variants +SEM (cm) Shoots Roots
A. C 4.1+0.6 15.1 4.5
NS-S 10.6+1.6 43.0 13.0
NS-L 8.1+1.0 38.4 8.9
B. C 0.52+0.06 0.24 0.04
NS-S 3.6+0.3 4.3 0.62
NS-L 1.3+0.3 3.1 0.14
Effect of feeding and/or soil nutrient supply on the growth of Drosera closterostigma germlings in a greenhouse after 121 days. Certain germlings were grown in a nutrient-free sand culture with distilled water (denoted as DW). Low-nutrient variants (LN) were supplied with 1/200 strength Hoagland nutrient solution to the rooting medium while high-nutrient variants (HN) were supplied with 1/20 strength solution. Eight collembolans were supplied on each plant in insect-fed variants (+I) during the growth period (unfed variants, -I). Total N and P content per plant, gemma, and that in the 8 insects (in brackets) are shown. All values are expressed in % of the low-nutrient unfed variant (LN-I) which was chosen as the control. Modified after Karlsson and Pate (1992a).
Parameter Insects Gemma LN-I HN-I DW+I LN+I HN+I
Total biomass -- 15 100 89 559 523 455
Total root length -- -- 100 87 175 173 168
Total N per plant (943) 67 100 76 682 646 592
Total P per plant (1980) 96 100 108 1352 1256 1432
The estimated seasonal nutrient uptake from carnivory in three Pinguicula species in natural habitats expressed (A) as % of the total summer nutrient content and (B) as % of the seasonal nutrient gain in non-flowering and flowering specimens. Values greater than 100 %, indicate that the supply of insect-derived nutrients was theoretically higher than the plants could take up. Modified after Karlsson et al. (1987) and Karlsson (1988).
% of total content % of seasonal nutrient gain
Flowering specimens Non-flowering Flowering
Species N P K N P K N P K
P. alpina 17-21 31-38 4-5 51 43 7 32 70 5
P. villosa 33 34 14 105 72 82 48 43 20
P. vulgaris 35-63 55-91 16-29 219 >100 61 100 135 28
Effect of supplementary insect feeding of naturally growing D. intermedia and D. rotundifolia (Bavaria, FRG) on seasonal growth and developmental parameters (modified after Thum, 1988). Unfed controls were able to catch natural prey while the variant was supplementarily fed on Drosophila flies throughout the season. DW of supplementary prey was ca 2.6 times higher than that of natural prey in D. intermedia and 9.0 times higher in D. rotundifolia. The ratio of parameters between fed and unfed plants is shown.
Parameter D. int. D. rot.
Number of active leaves 1.5 1.5
Leaf trapping area 2.7 2.9
DW of summer plants 3.5 5.0
DW of winter buds 3.6 4.5
% of flowering plants 1.6 68
Fruits per plant 2.4 98
Seeds per plant 3.5 192
Effect of supplementary feeding (16 Drosophila flies per plant) and/or soil fertilization with 1/20 strength Hoagland nutrient solution (NS) on the growth and N and P content in the annual Drosera glanduligera grown in a natural habitat for 77 days. All plants were able to catch natural prey. Modified after Karlsson and Pate (1992a).
No feeding Feeding
Parameter -NS +NS -NS +NS
Biomass (mg DW) 4.4 7.1 13.3 11.0
(SEM) (0.8) (1.5) (2.1) (2.1)
N content (% DW) 1.5 1.1 2.1 1.8
Total N (µg.plant-1) 69 80 279 199
P content (% DW) 0.08 0.05 0.07 0.10
Total P (µg.plant-1) 3.5 3.8 9.3 11.4
Effect of zooplankton feeding or addition of Carex rhizomes on the growth of A. vesiculosa in a greenhouse. Apical shoot segments 3 cm long were grown in a diluted mineral nutrient solution in aquaria for 27 days. Modified after Kaminski (1987b).
Plant length Dry weight
Treatment (cm) (mg)
Controls 4.3 3.2
Zooplankton 7.9 8.6
Carex rhizomes 8.4 8.0
Zoopl. + rhizomes 11.0 10.7
Copyright (c) Lubomír Adamec, 1997