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provided by Frontiers - Publisher Connector OPINION ARTICLE published: 31 January 2013 doi: 10.3389/fpls.2013.00010 Foliar mineral nutrient uptake in carnivorous : what do we know and what should we know?

Lubomír Adamec*

Department of Functional Ecology, Section of Ecology, Institute of Botany of the Academy of Sciences of the Czech Republic, Treboˇ n,ˇ Czech Republic *Correspondence: [email protected] Edited by: Yanbo Hu, Northeast Forestry University, China Reviewed by: Simon Poppinga, Plant Biomechanics Group, Germany

CARNIVOROUS PLANTS AS STIMULATION OF ROOT MINERAL the stimulatory effect was of a quanti- ECOLOGICAL GROUP NUTRIENT UPTAKE BY FOLIAR tative nature, dependent on the amount Carnivorous plants (CPs) usually grow NUTRIENT UPTAKE of prey (Hanslin and Karlsson, 1996). In in nutrient-poor, wet or aquatic environ- The four principal processes that deter- three species, slightly greater root ments and possess foliar traps which cap- mine the mineral nutrient budget in ter- lengths could only explain about 17% of ture animal prey ( et al., 1989). restrial CPs are: foliar nutrient uptake the uptake stimulation, the higher theo- There are about 600 terrestrial and 50 from prey, root nutrient uptake from retical uptake rate of roots per unit root aquatic or amphibious species of CPs the soil, mineral nutrient reutilization biomass being only about 15–30%, but which supplement the conventional min- from senescing shoots and stimulation the greater root biomass could explain eral nutrient uptake by roots or shoots of root nutrient uptake by foliar nutri- up to 70–85% of the effect (Adamec, from their environment by the absorp- ent uptake. This stimulated uptake was 2002). Root aerobic respiration, however, tion of nutrients (mainly N, P, K, Mg) repeatedly confirmed in about 10 terres- was unchanged. Moreover, the stimulatory from prey carcasses captured by their trial species under greenhouse or field con- effect on the roots did not correlate with traps (for the review, see Adamec, 1997, ditions (e.g., Hanslin and Karlsson, 1996; tissue mineral nutrient content in the roots 2002, 2011a). Among vascular plants, they Adamec, 1997, 2002, 2011a)andthispre- or shoots and the root: shoot biomass probably have the greatest capacity of sumably represents one of the most impor- ratio of fed plants slightly decreased. foliar mineral nutrient uptake which can tant ecophysiological adaptations of CPs. Phosphate alone could cause the stimula- cover 5–100% of their seasonal N and P Generally, CPs fed on insects or min- tion (Karlsson and Carlsson, 1984)butthe gain (consumption) but only 1–16% for eral nutrient solutions grew rapidly and role of other nutrients (especially N) is as K from captured prey (Adamec, 1997, accumulated far more mineral nutrients yet unknown. 2011a). The main ecophysiological strat- in their total produced biomass (about The explanation of the stimulatory egy of terrestrial species as S-strategists 1.6-27 × moreforN,P,K,Ca,andMg effect on the roots should be a pri- is slow growth and very effective min- compared to unfed control plants) than ority challenge for CP ecophysiologists. eral nutrient economy. Due to new dis- they could theoretically take up from the As shown by Adamec (2002), the effect coveries (e.g., Spomer, 1999; Anderson limited foliar nutrient supply. Thus, min- could not be caused by an increased root and Midgley, 2003; Pavlovic,ˇ 2012), the eral substances taken up by leaves from mineral nutrient content. Evidently, one boundary between carnivory and non- preystimulated,inanunknownway,the of the possible mechanisms of the root carnivory remains slightly blurred. In activity of the roots which then took up the uptake stimulation could be based on an line with recent findings, the concept of quantity of nutrients needed for increased increased photosynthetic rate in leaves and plant carnivory should be defined with growth from the mineral-poor soil. It is subsequent allocation of photosynthates an emphasis on the main benefit of fascinating that the stimulated uptake is to to roots. Nevertheless, stimulation of CP carnivory—the uptake of mineral nutri- a much greater physiological extent than photosynthesis by feeding on prey is still ents from prey (directly or indirectly) cap- the direct uptake of nutrients from prey a great issue. While an increased pho- tured by traps. Moreover, as all plants with itself. It is possible to assume that the tosynthetic rate due to prey feeding has glandular hairs are potentially carnivorous extent of this stimulation will be several recently been proven only in (Spomer, 1999), a defining statement that times greater for K, Ca, and Mg uptake and species with pitcher traps foliar nutrient uptake from prey must be than that for N and P under natural con- (Farnsworth and Ellison, 2008; Pavlovicˇ “ecologically significant” for CPs seems ditions as prey are a rather poor source et al., 2009), no increase occurred in reasonable (Płachno et al., 2009)whereas of these metallic cations. The essence of Drosera or species (Méndez criteria such as producing their own diges- the stimulation of root uptake in CPs has and Karlsson, 1999) though commonly tive enzymes or prey attraction are only not yet been explained. A stepwise feed- these latter two genera exhibit marked marginal. ing on prey in the field revealed that root uptake stimulation (Adamec, 1997,

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2002, 2011a). It is thus possible that Friday and Quarmby (1994)estimated digestion by producing their own enzymes the photosynthetic response to prey feed- an 83% efficiency of N uptake from (Adamec, 2011a). However, the major- ing is genus specific. Another direction model mosquito larvae in vul- ity of traps are known to capture no of the stimulation study could be hor- garis traps which is higher than that in prey during their life-span though their monal: to investigate the distribution of terrestrial species (cf. Adamec, 2011a). commensal communities are very pro- cytokinins and the strength of the sinks Although prey feeding markedly enhanced lific and dense. To support the communi- within CP roots. Finally, modern tran- the growth of aquatic CPs in many growth ties, traps even exude organic substances scriptomic research should reveal gene experiments (Adamec, 1997, 2011a), the intothetrapfluid(Sirová et al., 2010). families which are switched on or off uptake efficiency from prey is unknown. Nevertheless, in barren waters, commen- in stimulated and control roots, respec- Moreover, the available results do not sal communities in traps seemed to be tively (sensu Ibarra-Laclette et al., 2011). In allow one to determine whether captured more beneficial for the plants than the any case, direct measurements of mineral prey leads to a stimulation of nutrient trapping of prey alone (Richards, 2001). + nutrient (ammonium, phosphate, K ) uptake by shoots. However, it is possible In prey-free traps, which can suck in uptake by intact or excised CP roots are to deduce from the growth in very olig- much detritus or phytoplankton from the essential for quantifying the root uptake otrophic waters with zero prey availabil- ambient water during incidental firings, affinity and achieving any progress in ity that aquatic Utricularia species have a a miniature microbial food web may run this field. On the other hand, following very high shoot uptake affinity for min- (Sirová et al., 2009)andmanyUtricularia µ + from numerous data (Adamec, 1997, 2002, eral nutrients: at least 0.4 MforNH4 species may rather be considered “bac- 2011a; Moran et al., 2010), the affinity of and 0.1 µM for phosphate (see Adamec, terivorous” or “detritivorous” than car- mineral nutrient uptake from prey by traps 2009). Again, the affinity has never been nivorous.However,unlikethepostulated is rather high. measured. hypothesis on the nutritive role of trap One of the challenges for study is K+ commensals for N and P uptake by traps FOLIAR NUTRIENT UPTAKE IN economy in aquatic CPs. Rapidly growing (Richards, 2001), very high concentrations AQUATIC CARNIVOROUS PLANTS aquatic species exhibit a high shoot K+ of total soluble N and P were found in the Aquatic carnivorous plants (ACPs) com- content of 1.5–5% of dry weight but always Utricularia trap fluid; the concentrations + prise the species vesiculosa lose all K in their senescent shoots (but increased with the trap age and correlated (Droseraceae) and about 50 species of very effectively re-utilize N and P) which with commensal biomass (Sirová et al., + the genus Utricularia (Lentibulariaceae). greatly contrasts with very efficient K 2009). They usually grow in shallow, standing reutilization in terrestrial CPs (Adamec, To reveal whether Utricularia traps can humic waters which are usually poor in 1997, 2011a). As prey is a relatively poor gain N and P from the accumulated + NandP(Adamec, 1997, 2011a). ACPs K source, aquatic CPs must rely mainly organic material inside traps or whether + are ecophysiologically quite dissimilar to on permanent rapid K uptake from the traps rather exude these nutrients for their terrestrial counterparts; they take up ambient water by shoots. In A. vesicu- the microbial community, an ecological + all necessary nutrients either directly from losa, surprisingly, K was taken up only model based on literature data was devised the water by their shoots or from animal by basal shoot segments, but not apical (Adamec, 2011b). Simply, a theoretical + prey by traps. Their entirely rootless shoots ones which permanently need much K N and P input rate from the natural ambi- are mostly linear and, under favourable for their rapid apical growth (Adamec, ent water into the trap was compared with + conditions even in barren habitats, they 2000). Presumably, K is allocated from the estimated total N and P content inside exhibit very rapid apical shoot growth of basal shoot segments to the apical ones. the trap. The model shows that the total 3–4 leaf nodes d−1 while their shoot bases Repeated experiments both in Aldrovanda N and P content inside the traps is too high decay at this same high rate. The very and U. australis failed to estimate any posi- to be accumulated from only the ambi- + rapid growth requires a combination of tive K uptake from diluted media in light ent water (Adamec, 2011b). Thus, such a several ecophysiological processes includ- (Adamec, unpublished) and indicated that low N and P gain cannot be ecologically + ing the capture of animal prey, very high K uptake could occur only at high photo- important for the plant mineral nutri- photosynthetic rates, very efficient mineral synthetic rate or rapid apical shoot growth. tion. Moreover, the prey-free traps do not nutrient uptake from water and efficient Utricularia suction traps are hermet- take up any N and P from the trap fluid mineral nutrient reutilization (except K+) ically closed bladders filled by a fluid but rather exude an amount of N and P from senescent shoots (Adamec, 1997, and function on the basis of negative to the fluid to support the microbial 2011a). pressure (Juniper et al., 1989; Adamec, community. This implies that the uptake Foliar nutrient uptake in ACPs is still 2011a,b). In addition to their trapping affinity of prey-free traps for mineral veiled in mystery caused by methodi- animal prey, commensal microorganisms and organic nutrients is surprisingly very cal difficulties. Unlike terrestrial CPs, in (bacteria, algae, ciliates, and rotifers) prop- low—unlike the above very high nutrient which the efficiency of foliar mineral agate in the traps of aquatic Utricularia uptake affinity of shoots—although traps uptake from prey has been quantified for species. The question of their role in trap are nutrient absorbing organs. Therefore, several nutrients (Adamec, 2002, 2011a; functioning and plant nutrition is often the trap microorganisms behave more Płachno et al., 2009), such information is discussed. In traps with captured prey, as parasites than commensals and repre- almost entirely lacking for aquatic CPs. commensals evidently participate in prey sent an additional ecological cost for trap

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maintenance. It is a question, however, (Lentibulariaceae) and its investment in carnivory. species: flux rates and gland distribution patterns whether the nutrient uptake affinity is dif- Ecol. Res. 24, 327–333. reflect nitrogen sequestration strategies. J. Exp. ferent in prey-free traps and in those with Adamec, L. (2011a). “Ecophysiological look at plant Bot. 61, 1365–1374. carnivory: why are plants carnivorous?” in All Pavlovic,ˇ A. (2012). Adaptive radiation with regard to captured prey. Utricularia traps are the Flesh is Grass. Plant-Animal Interrelationships. nutrient sequestration strategies in the carnivorous most sophisticated ones among all CPs. Cellular Origin, Life in Extreme Habitats and plants of the genus Nepenthes. Plant Signal. Behav. In spite of their demanding physiologi- Astrobiology, Vol. 16, eds J. Seckbach and Z. 7, 1–3. cal functions, including mineral nutrient Dubinski (Dordrecht, Heidelberg, London, New Pavlovic,ˇ A., Singerová, L., Demko, V., and uptake from prey, their nutrient absorp- York: Springer Science + Business Media, B. V.), Hudák, J. (2009). Feeding enhances photo- 455–489. synthetic efficiency in the carnivorous pitcher tion affinity is paradoxically very low Adamec, L. (2011b). Functional characteristics of plant Nepenthes talangensis. Ann. Bot. 104, though the uptake rate in traps with cap- traps of aquatic carnivorous Utricularia species. 307–314. tured prey may be very high. On the con- Aquat. Bot. 95, 226–233. Płachno, B. J., Adamec, L., and Huet, H. (2009). trary, mineral nutrient uptake (N, P, and Anderson, B., and Midgley, J. J. (2003). Digestive Mineral nutrient uptake from prey and glan- K)byshootsofaquaticCPsrunswithvery mutualism, an alternate pathway in plant car- dular phosphatase activity as a dual test of nivory. Oikos 102, 221–224. carnivory in semi-desert plants with glandular high affinity but the uptake rate per unit Farnsworth, E. J., and Ellison, A. M. (2008). Prey avail- leaves suspected of carnivory. Ann. Bot. 104, biomassispresumablyverylow. ability directly affects physiology, growth, nutrient 649–654. In conclusion, thanks to the dynami- allocation and scaling relationships among leaf Richards, J. H. (2001). Bladder function in Utricularia cally growing knowledge of CPs, we are traits in ten species. J. Ecol. 96, purpurea (Lentibulariaceae): is carnivory impor- 213–221. tant? Am.J.Bot.88, 170–176. increasingly more able to discuss to what Friday, L. E., and Quarmby, C. (1994). Uptake and Sirová, D., Borovec, J., Cerná,ˇ B., Rejmánková, E., extent CPs are different from or similar to translocation of prey-derived 15Nand32Pin Adamec, L., and Vrba, J. (2009). Microbial com- “normal” non-CPs. Utricularia vulgaris L. New Phytol. 126, 273–281. munity development in the traps of aquatic Hanslin, H. M., and Karlsson, P. S. (1996). Nitrogen Utricularia species. Aquat. Bot. 90, 129–136. uptake from prey and substrate as affected by Sirová, D., Borovec, J., Šantr˚ucková,ˇ H., Šantr˚ucek,ˇ ACKNOWLEDGMENTS prey capture level and plant reproductive status J., Vrba, J., and Adamec, L. (2010). Utricularia Sincere thanks are due to Dr. Brian G. in four carnivorous plant species. Oecologia 106, carnivory revisited: plants supply photosynthetic 370–375. carbon to traps. J. Exp. Bot. 61, 99–103. McMillan for correction of the language. Ibarra-Laclette, E., Albert, V. A., Perez-Torres, C. A., Spomer, G. G. (1999). Evidence of protocarnivo- This study was partly supported by the Zamudio-Hernandez, F., Ortega-Estrada, M. de. J., rous capabilities in viscosissimum and Czech Research Project CSF P504/11/0783 Herrera-Estrella, A., et al. (2011). Transcriptomics Potentilla arguta and other sticky plants. Int. 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Ion fluxes across the pitcher authors and source are credited and subject to any copy- the aquatic carnivorous plant Utricularia australis walls of three Bornean Nepenthes right notices concerning any third-party graphics etc.

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