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Mineral nutrition of carnivorous plants: a review.

II. Introduction

More than 600 species of carnivorous plants occur throughout the world, out of a total of about 300,000 species of vascular plants. All plants considered carnivorous fulfill 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 carnivorous plants (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 unfavorable conditions (for a discussion of this, see Juniper et al., 1989: 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, German physiologist K. Goebel summarized the importance of carnivory as early as 1893: "Carnivory is useful for plants but it is not indispensable."

The basic questions raised by biologists over the past 120 years involve the relative importance of foliar and root nutrition of CPs, the identification of the nutrients (elements) from prey bodies which are of principal importance for growth, the relationship between organic and mineral nutrition of CPs, and the importance of carnivory under natural conditions. In the past 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 (Luttge, 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, this review emphasizes recapitulation of original data and conclusions of results from a variety of studies that approach CPs from an ecophysiological perspective.

III. Ecological Factors in Habitats of Carnivorous Plants

The majority of terrestrial CPs grows in bog and fen soils, in which they encounter persistent unfavorable conditions. The soils are usually wet or waterlogged, at least over the growing period. Soils are mostly acid (pH 3-6; e.g., Roberts & Oosting, 1958; Chandler & Anderson, 1976a; Juniper et al., 1989: 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 or entirely deprived of oxygen (hypoxic and anoxic, respectively). Moreover, changing of anaerobic and aerobic conditions is also harmful (post-anoxic injury; Crawford, 1989: 105-129). In wet soils, decomposition of organic matter may lead to a high concentration of toxic [H.sub.2]S (or [S.sup.2-]) 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 unfavorable ecological factor in these soils; this factor is overcome by carnivory (Luttge, 1983; Juniper et al., 1989: 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.sup.-1] DW [dry weight]): [N[H.sub.4].sup.+], 2; P[O.sub.4], [less than]2; K, 2; Mg, 1; Fe, 1. There was a complete lack of detectable [N[O.sub.3].sup.-], 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 four Australian and New Zealand Drosera species (in g [kg.sup.-1] DW): N, 0.46-2.5; P, 0.09-1.9 (data summarized in Chandler & Anderson, 1976a).

Normal functioning of CP roots (uptake of nutrients and water) is inhibited 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 of 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 unfavorable factors by growing slowly. They do not require a high supply rate of mineral nutrients from soils, for 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 (Luttge, 1983; Juniper et al., 1989: 21-22). The root:total biomass ratio ranges from only 3.4% to 23% in various CPs (Karlsson & Carlsson, 1984; Karlsson & Pate, 1992b; Adamec et al., 1992). Roots are usually short, weakly branched, and able to tolerate, in an unknown way, anoxia and related phenomena ([H.sub.2]S) 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 in plant metabolism and physiological functions, and release from primary physiological functions and of entry secondary ones. Our knowledge of CP mineral nutrition can be considered 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 C[O.sub.2] by leaves. All CPs are green and able to fix C[O.sub.2] (autotrophy), although the growth of some species (mainly aquatic) is partly dependent on organic carbon uptake from prey (facultative heterotrophy; see Luttge, 1983). Many CPs of all taxonomic groups fix C[O.sub.2] according to the [C.sub.3] scheme of the Calvin cycle (Luttge, 1983), but anatomical evidence in favor of the [C.sub.4] type has been given in six Mexican succulent Pinguicula species (Studnicka, 1991). The relationship between CP photosynthetic performance and carnivory is complex and ambiguous (Juniper et al., 1989: 144-146). Although photosynthetic rate of traps is lower than that of leaves (Knight, 1992; Adamec, 1997), 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. Dykyjova, 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.sup.-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) that 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 that 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 dry weight. Thus, P vulgaris, via its roots, is able to take up all nutrients required for its vigorous growth from nutrient-rich soil. Moreover, insect feeding stimulated the effective nutrient uptake by roots and resulted in approximately 1.6x higher accumulation of N in plants than could have been absorbed from the prey. The similar growth pattern was also found in aseptically grown P. lusitanica, [TABULAR DATA FOR TABLE I OMITTED] where the effect of insect feeding correlated positively with increasing nutrient content of the soil (Harder & Zemlin, 1967).

The positive growth effect of insect feeding in CPs can also be achieved when only minemi nutrient solution is dropped on the trapping part of leaves instead of prey (Karlsson & Carlsson, 1984; Adamec et al., 1992). Pinguicula vulgaris, grown in a fen soil supplied with a diluted nutrient solution, was able to enhance its growth and accumulate N and P in its biomass to a similar or even greater extent than it does through insect feeding when leaves were supplied with either mineral N, P, or microelements or mixtures of these nutrients (Karlsson & 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. Nitrogen 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 markedly promote the root uptake of other nutrients and thus lead 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 & 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) was there support for the hypothesis that plant response to feeding was higher in nutrient-poor soils. In contrast, the hypothesis was rejected in only 1 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.
Table II

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 N[H.sub.4]N[O.sub.3] (variant N) or 0.1% P (P) or
micronutrients (M) or mixture of N + P (NP) or N + P + M (N-PM);
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 percent of the controls, for all
variants. (After Karlsson & 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[[micro]gram] 169 176 151 142 177 146
Total P 58.9[[micro]gram] 109 143 90 115 192 132


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 18x 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 the three species, the highest growth enhancement (12-18x) 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 seedling 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 & Oosting, 1958). Soil alkalization by NaHC[O.sub.3] 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 [TABULAR DATA FOR TABLE III OMITTED] 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, 12-47x; P, 4 - 16x; K, 29-114x; Ca, 2-8x; Mg, 15-59x; Fe, 43-169x. These numbers are rough estimates ([+ or -]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, ca. 1.4x; K, 3.4x; Mg, 1.8x) 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 fully explain 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 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 attained in complete Knop solution. Thus, Ca or Mg deficiency in nutrient solution had the same growth-retarding 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. Drosera 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 [N[H.sub.4].sup.+] and [N[O.sub.3].sup.-] by roots as a N source for its growth. Rychnovska-Soudkova (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 [NH.sub.4].sup.+] at pH [greater than]5.0 but was inhibited by [N[O.sub.3].sup.-]. In contrast, [N[O.sub.3].sup.-] was used efficiently at a low pH (3.0) and [N[H.sub.4].sup.+] use was weak. The low pH protected the plants from a high [Ca.sup.2+] concentration in the solution, whereas high [Ca.sup.2+] inhibited growth at higher pH ([greater than]5.0; Rychnovska-Soudkova, 1953). A similar pH effect on D. aliciae growth in [N[O.sub.3].sup.-]- and [N[H.sub.4].sup.+]nutrient solutions was also found by Small et al. (1977). Aseptically grown D. rotundifolia tolerated high concentrations of both N[H.sub.4]Cl and N[H.sub.4]N[O.sub.3] in nutrient solution, with growth saturated at 2.5 mM N[H.sub.4]N[O.sub.3] (Simola, 1978).

Krafft and Handel (1991) tested the effect of insect feeding rate on Drosera 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 markedly enhanced in D. rotundifolia both flowering and the production of reproductive biomass (4.2-8.8x), 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 vigor 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 in this species the majority of N and P, but the minority of K, Ca, and Mg, 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; Ca[Cl.sub.2], 1; Mg[Cl.sub.2], 1; NaCl, 1; Na[H.sub.2]P[O.sub.4], 0.5; N[H.sub.4]Cl, 18.7) poured into their pitcher leaves (Jaffe et al., 1992). During a period of 24 hours, leaves took up 92-98% of the added P, 66-67% of K, 28-54% of Na, 9-30% of Ca, and 18-32% of Mg. Heliamphora tatei took up all ions more efficiently than H. heterodoxa. The results show that the former species is able to take up P and K more efficiently from prey than it can 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 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 & 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 [N[O.sub.3].sup.-]- or [S[O.sub.4].sup.2-]-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 [N[O.sub.3].sup.-] concentration within 0-1.1 mM. The negative interactions between foliar and root nutrient uptake, together with total root unresponsiveness to [N[O.sub.3].sup.-], indicate clearly a rather limited absorption capacity of roots in this species. In parallel experiments, insect feeding of D. binata growing in N[O.sub.[3.sup.-]]-free nutrient solution increased its biomass by 3 x, while increasing the N[[O.sub.3].sup.-] concentration (0.1-1 mM) gradually declined the effect of feeding (by 6-30%). Unfed D. binata reacted positively to increasing N[[O.sub.3].sup.-] concentration in the solution.

In Drosera whittakeri growing in complete solution, the activity of shoot nitrate reductase (NR) was ca. 30-50% lower in insect-fed plants than that in unfed ones (Chandler & Anderson, 1976a). NR was distinctly inducible by N[[O.sub.3].sup.-] in unfed plants. Thus, N-containing organic substances from insects are more effective in promoting growth than N[[O.sub.3].sup.-], 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 N[[O.sub.3].sup.-] (and S[[O.sub4].sup.2-]) 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 N[[O.sub.3].sup.-] (Small et al., 1977). The activity of both enzymes was 2-4.5x higher in roots than in shoots. The enzymes incorporating N[[H.sub.4].sup.+] into metabolism (GS, GDH, GOGAT) were present in roots and shoots in all variants.

Chandler and Anderson (1976b) demonstrated the uptake of labeled S[[O.sub.4].sup.2-] from S[[O.sub.4].sup.2-] solution that was dropped onto the leaves of Drosera whittakeri and D. binata grown in a greenhouse or aseptically. The label was incorporated mostly to cystein. Both species absorbed S[[O.sub.4].sup.2-], cysteic acid, and cystein from insects. P-labeling patterns in shoots were the same after leaf supply of labeled phosphate or insects (Chandler & 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 & 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% more P, 80-100% more K, and 15-25% more Ca in their tubers. Insect-fed plants contained 60% more N, 40% more P, and 25% more 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 (2.2x), P (4.7x), K (2.0x), Ca (3.9x), Mg (1.6x), and Zn (3.5x) 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 Drosera 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, whereas 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% in stem, 18% in developing daughter tubers and rhizomes, and 29% in new replacement tuber; no N was present 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, whereas 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. Drosera erythrorhiza uptake of N from insects was enormously efficiently, with most being stored in tubers. Moreover, its leaf and stem N and P are perfectly re-utilized and translocated to tubers so that the plant loses only 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 & Komiya, 1972, 1973).

A total lack of response to soil nutrient supply was found in the perennial pygmy sundew Drosera closterostigma (Karlsson & 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 5x. The total N content increased 6-7x, and that of P, 14x. In contrast to stimulation of root nutrient uptake in Pinguicula (Karlsson & 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 59-67% 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 N[[O.sub.3].sup.-] (see Karlsson & Pate, 1992a).

A. CONCLUSIONS

It may be inferred from the above literature data that all terrestrial CPs may be loosely 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 Pinguicula vulgaris, P. alpina, P. lusitanica, Drosera 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 [ILLUSTRATION FOR FIGURE 1A OMITTED]. A partial saturation effect may occur in other cases ([ILLUSTRATION FOR FIGURE 1B OMITTED]; 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 Drosera whittakeri, D. binata, Pinguicula villosa, and probably also Drosera 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 that in the first plant group [ILLUSTRATION FOR FIGURE 1C OMITTED]. 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 Drosera closterostigma and perhaps also Dionaea muscipula [ILLUSTRATION FOR FIGURE 1D OMITTED]. 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 potentially in competition with non-CPs (e.g., Wilson, 1985), are subject to mortality (Thum, 1989b), and are sometimes robbed of their prey by opportunistic predators (Thum, 1989a; Zamora, 1990). The nutrients released from insect carcasses may be washed out by rain, or even whole prey may be 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., [TABULAR DATA FOR TABLE IV OMITTED] 1987; Karlsson, 1988; see Table V). The nutrient losses in senescent leaves and roots (estimated as total summer nutrient content - nutrient content of winter buds - nutrient content of reproductive organs), expressed in percent of the total summer nutrient content, ranged between 11% and 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 nonflowering specimens. On the basis of measured seasonal rate of catering 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 (Table 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; of. Karlsson et al., 1994; Table 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 Pinguicula alpine 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 10x) 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 & Handel, 1991), the seasonal growth of Drosera intermedia and D. rotundifolia in a peat bog was greatly dependent on the quantity of supplied prey (Thum, 1988). As shown in Table VI, the fed plants of both species produced 3.5-5x 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 that were fed (Table VI). In adult D. intermedia plants, flowering and seed set increased proportionally [TABULAR DATA FOR TABLE V OMITTED] with vegetative growth, whereas they were highly stimulated (68-192x) 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 to leaf trapping area, which further allows the catching of more prey (positive feedback).
Table VI

Effect of supplementary insect feeding of naturally growing
Drosera intermedia and D. rotundifolia (Bavaria, FRG) on
seasonal growth and developmental parameters (after Thum,
1988). Unfed controls were able to catch natural prey; the variant
was supplementarily fed on Drosophila flies throughout the
season. DW of supplementary prey was ca. 2.6 x higher than that
of natural prey in D. intermedia and 9x higher in D. rotundifolia.
The ratio of parameters between fed and unfed plants is shown.

Parameter D. intermedia D. rotundifolia

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


Thum (1988) also found that 1 mg DW of the supplied prey led to a summer biomass increase of 6.5 mg in Drosera 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 mg 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 & Schulze, 1990), 99-100% of the increased N can be taken up from prey. Natural seasonal catch of digested prey (0.2 mg DW per 1 [mg.sup.-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 content, 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 of 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 Drosera rotundifolia growing outdoors in big cubes of natural peat for 15 weeks and watered by rain water (Schulze & 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 1.73x and 2.98x 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 Schulze and Schulze (1990), ca. 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 Drosera 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 that 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 (N[H.sub.4]N[O.sub.3]; 4 g N [m.sup.-2] [year.sup.-1]) of D. rotundifolia led to a moderate increase in stem height, leaf thickness, leaf number, and leaf dry weight per plant, but leaf area per plant was unchanged (Svensson, 1995). Stem enlargement helped the plants avoid being overgrown with the Sphagnum moss.

The importance of the natural catch of prey, in field experiments in southeastern United States, 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 more flowers and seeds. Furthermore, when these plants (except Dionaea) were fed insects at ca. 3x 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 Rychnovska-Soudkova (1954), evidence was also given which implies a negative influence of insect feeding and soil nutrient supply on Drosera rotundifolia growth (Stewart & Nilsen, 1992). Plants growing in a nutrient-rich peat bog (in mg [kg.sup.-1] soil DW: N[H.sub.3], 20-150; P, 2-3) in Virginia were treated by supplemental insect feeding (one fly per month), prey deprival, urea (170 g N [m.sup.-2]), phosphate (195 g P [m.sup.-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 5-15x. 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 2.8x compared to the controls, and P supply increased the P tissue content by 3.57x. Insect feeding had no significant effect on N and P tissue content. Fertilized plants (and also, to a lesser extent, 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," 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. Table I).

The effect of leaf nutrient and insect supply was tested on growth of Sarracenia purpurea in a fen in Minnesota (Chapin & Pastor, 1995). Over the course of 16 weeks and in 2-week intervals, workers applied to each pitcher leaf a total of either 4 ml of 157.6 mM N[H.sub.4]Cl, 35.5 mM K[H.sub.2]P[O.sub.4]/[K.sub.2]HP[O.sub.4], 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. The leaves were prevented from catching natural prey. The total amount of N and P applied was 10x 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 10x 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 & Pastor, 1995). However, all applications of N and insect feeding led to an increase in N content per leaf DW that was significant in comparison 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 5.5-7x 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. 271), could supply the roots with up to 1.05 g N[H.sub.3]-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 per [g.sup.-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 Sarracenia purpurea growth.

Naturally growing Drosera erythrorhiza was found as compensating ca. 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 Southwestern Australia. Rosette species (Drosera 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), ca. 47% in Cephalotus follicularis, and ca. 21% in semi-terrestrial Polypompholyx multifida. Obviously, these numbers indicate relative trapping efficiencies of CPs with different growth forms.

A perennial pygmy sundew Drosera closterostigma grown in a greenhouse was totally inert to soil nutrient supply, and the same held for natural habitats in Western Australia (Karlsson & 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 that 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 the naturally growing non-gemmiferous pygmy annual D. glanduligera was able to moderately increase 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 & 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 & 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 & Dixon, 1978).

A. CONCLUSIONS

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; Thum, 1988; Krafft & Handel, 1991; Karlsson & Pate, 1992a). Therefore, the quantity of caught prey is a major factor mostly for the vigor of CP populations. Catching of prey is evidently much more important for seedlings and small juvenile specimens with shorter roots than it is for big adult plants (Thum, 1988; Karlsson, 1988; Karlsson & Pate, 1992a; Adamec et al., 1992). In juvenile specimens, catching prey is limited [TABULAR DATA FOR TABLE VII OMITTED] 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 it promotes vegetative growth, but it accelerates the rate at which minimum plant size necessary for flowering is reached (Thum, 1988; Karlsson et al., 1991; Karlsson & Pate, 1992a). On the contrary, small naturally growing specimens of Drosera rotundifolia are even supposed to die when permanently deprived of prey (Schulze & 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; Karlsson, 1988; Thum, 1988, 1989b). However, the efficiency of absorption 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 absorption 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 reutilization from aged leaves and stems. As opposed to the very efficient N and P re-utilization from D. erythrorhiza shoots (Pate & 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; Thum, 1988; Schulze & Schulze, 1990; Karlsson & Pate, 1992b). 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 & Schulze, 1990) than in D. erythrorhiza (Pate & 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: 134). Dionaea muscipula grew very poorly in a conventional clay-loam garden soil (Roberts & 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 ca. 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.sup.-2] and 5.9 g P [m.sup.-2]; cf. Stewart & Nilsen, 1992; section VI, above). Possible negative effects of nutrient-rich soils on the growth of Nepenthes were discussed by Juniper et al. (1989: 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 & Anderson, 1976a) or of an unsuitable pH (cf. Rychnovska-Soudkova, 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, D. capillaris grown in vitro 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 a certain concentration of humic acids and tannins (i.e., dystrophic waters). The waters are usually nutrient poor, and the concentration of inorganic N (N[[H.sub.4].sup.+], N[[O.sub.3].sup.-]) may be [less than] 150 [[micro]gram] [l.sup.-1], of inorganic P [less than] 50 [[micro]gram] [l.sup.-1], and of inorganic K [less than] 1 mg [l.sup.-1] (Komiya, 1966; Kaminski, 1987a, 1987b; Kosiba, 1992a, 1993; Akeret, 1993). In waters not impacted by human activity, the concentrations may be as low as 1-2 [[micro]gram] N [l.sup.-1], 2 [[micro]gram] P [l.sup.1], and 0.01 mg K [l.sup.-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 & Leuven, 1988; Hough & Fornwall, 1988; Kosiba & Sarosiek, 1989; Kosiba, 1992a, 1993; Akeret, 1993; Adamec, 1995a, 1997). 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 C[O.sub.2]. A very high C[O.sub.2] concentration between 0.1 mM and 0.6 mM occurs commonly in aquatic habitats of CPs (Komiya, 1966; Akeret, 1993; Adamec, 1995b, 1997).

All aquatic CP species are rootless and either float freely below the water surface or are loosely 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. Unlike 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 to be essential for normal growth and development in Aldrovanda vesiculosa (Ashida, 1937; Kaminski, 1987b) and Utricularia vulgaris (Kosiba, 1992b) but facultative in other species (Pringsheim & Pringsheim, 1967; see Luttge, 1983). All aquatic CPs tested so far can use only free C[O.sub.2] (not HC[[O.sub.3].sup.-]) for photosynthesis. Their photosynthetic C[O.sub.2] compensation points fall within the range of 1.5-7.2 [[micro]molar] (Moeller, 1978; Adamec, 1995a, 1997). Similar values of 1.5-10 [[micro]molar] C[O.sub.2] are reported generally in aquatic non-CPs (cf. Maberly & 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 & Pringsheim, 1967; see below). In U. gibba, grown aseptically in a concentrated mineral medium for 8 weeks with neither Mg nor K, feeding on protozoa promoted its growth and overcame fully the deficiency of K but only partly that of Mg (Sorenson & 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 Utricularia 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 4-8x. 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, 1992b). 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 C[O.sub.2] 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 HC[[O.sub.3].sup.-] and [Ca.sup.2+]). 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-labeled 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, ca. 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 ca. 83% of the total 15N in the prey had been still present in the plants 14 days after feeding, and ca. 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 labeled 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 5-7.5x diluted solution and at 5 mg [1.sup.-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 C[O.sub.2] 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 Aldrovanda vesiculosa shoots was studied in 6-8-hour experiments (Adamec, unpubl.). The light uptake of N[[H.sub.4].sup.+] from 15 or 30 [[micro]molar] N[H.sub.4]N[O.sub.3] was the same in both apical and basal parts and ca. 6x higher than N[[O.sub.3].sup.-] uptake. N[[H.sub.4].sup.+] uptake was observed overnight, but N[[O.sub.3].sup.-] was not. Phosphate was taken up by apical parts ca. 2x as fast as it was by basal parts. However, [K.sup.+] was taken up only by basal parts, and its uptake rate by intact plants was ca. 1/2 of that by basal parts. Thus, A. vesiculosa prefers N[[H.sub.4].sup.+] to N[[O.sub.3].sup.-], and [K.sup.+] is taken up only 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 ca. 13x higher than that in the last living whorls and 4.8x 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 lose a majority of K, Ca, Mg, and Na. Utricularia 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 C[O.sub.2] (Luttge, 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 C[O.sub.2] 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 labeled organic substances or 14C from labeled prey by traps, b) promotion of CPs' growth by catching prey at C[O.sub.2] 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 Luttge, 1983; Juniper et al., 1989: 207-226). Traps of CPs were found to absorb all amino acids, some dipeptides, and urea (e.g., Plummer & Kethley, 1964; Luttge, 1965; Chandler & Anderson, 1976b). Both the uptake affinity and capacity for amino acids 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 (Luttge, 1965). High capacity for uptake of amino acids was found in Sarracenia flava traps (Plummet & Kethley, 1964). Nearly all amino acids added to the traps were absorbed completely within 2 days and found in other organs. In pitcher leaves of Heliamphora tatei and H. heterodoxa, ca. 50% of added alanine and valine was absorbed within 1 day (Jaffe et al., 1992). The absorbed amino acids are metabolized readily to a variety of compounds (Luttge, 1964).
Table VIII

Effect of zooplankton feeding, addition of Carex rhizomes, or a
combination of the two on the growth of Aldrovanda vesiculosa in
a greenhouse. Apical shoot segments 3 cm long were grown in a
diluted mineral nutrient solution in aquaria for 27 days. (After
Kaminski, 1987b.)

Treatment Plant length (cm) Dry weight (mg)

Controls 4.3 3.2
Zooplankton 7.9 8.6
Carex rhizomes 8.4 8.0
Zoopl. + rhizomes 11.0 10.7


Drosera capensis and Aldrovanda vesiculosa absorbed organic substances from 14C-labeled Daphnia prey (Fabian-Galan & 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 labeled flies was stored in daughter and replacement tubers of D. erythrorhiza 2 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 absorption 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), who found that intact plants of Drosera sp. had absorbed 80% of 14C from labeled 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 C[O.sub.2] or light limitation. Aldrovanda 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 C[O.sub.2] concentration of which was evidently lower than their C[O.sub.2] compensation point (Adamec, 1995b). Similarly, the growth of Utricularia vulgaris fed on Daphnia was promoted when there was a C[O.sub.2] shortage in water (Kosiba, 1992a, 1992b). However, insect-fed Drosera whittakeri was not able to grow at a very reduced irradiance (1.5 W [m.sup.-2]; Chandler & Anderson, 1976a). It is obvious that any estimates of an ecological role of absorption 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 mg in D. rotundifolia due to feeding on 1 mg of insects. Assuming a 50% absorption 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% 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 ca. 10% of the plants' organic carbon.

Some aquatic CPs strictly require humic acids for normal growth and development, while other species (Utricularia minor, U. ochroleuca) grow only in a mineral medium with traces of peptone, beef extract, glucose, or acetate (Pringsheim & 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 of 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 been demonstrated only 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 been observed only 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 absorption 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 and 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 absorption capacity of mots 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 vigor 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 uptake and organic carbon uptake from prey is ecologically very important for growth. Traps of terrestrial CPs efficiently absorb amino acids from prey, but absorption of organic carbon from prey may be of only 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.

XII. Acknowledgments

This paper is dedicated to Dr. Miroslav Dvorak (Charles University, Prague). 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. Leos Klimes (Trebon, Czech Rep.), Jana Cernohorska, and Miroslav Dvorak (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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Title Annotation:Interpreting Botanical Progress
Author:Adamec, Lubomir
Publication:The Botanical Review
Date:Jul 1, 1997
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