Foliar mineral nutrient uptake in carnivorous plants: what do we know and what should we know?

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