Carnivorous plants: the role of 15N in tracing nitrogen dynamics in the prey–plant–soil–aquatic continuum
Phillip M. Chalk
A * and Hang-Wei Hu A
+ Author Affiliations
- Author Affiliations
A Faculty of Veterinary and Agricultural Sciences, The University of Melbourne, Parkville, Vic. 3010, Australia.
Australian Journal of Botany 70(2) 103-113 https://doi.org/10.1071/BT21128
Submitted: 28 October 2021 Accepted: 6 December 2021 Published: 25 January 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Carnivorous plants have access to several potential sources of nitrogen, including root uptake, predation, litterfall, atmospheric deposition and defecation by mutualistic animals. Our aim was to assess the relative importance of different N sources so as to better understand the ecology of these physiologically diverse plants that include many genera and species inhabiting terrestrial and aquatic environments worldwide. Plant physiology and habitat were the major determinants of the relative importance of N source. Our secondary aim was to examine protocarnivorous plants that do not fit the exact definition for carnivory. Several protocarnivorous plants were classified as carnivorous based on specialised trapping mechanisms, isotopic data and mixing models. Several carnivorous plants can transfer their functions of prey capture and digestion to mutualistic animal partners, which is termed ecological outsourcing. Outsourcing arthropod prey capture and digestion to mutualistic bats is a beneficial strategy for the carnivorous plant Nepenthes hemsleyana.
Keywords: Bromeliaceace, carnivorous plant species, Droseraceae, ecological outsourcing, insectivores, Nepenthes spp, nitrogen, protocarnivory.
References
Adamec L (1997) Mineral nutrition of carnivorous plants: a review. The Botanical Review 63, 273–299.| Mineral nutrition of carnivorous plants: a review.Crossref | GoogleScholarGoogle Scholar |
Adlassnig W, Peroutka M, Lambers H, Lichtscheidl IK (2005) The roots of carnivorous plants. Plant and Soil 274, 127–140.
| The roots of carnivorous plants.Crossref | GoogleScholarGoogle Scholar |
Anderson B, Midgley J (2002) It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant Roridula. Oecologia 132, 369–373.
| It takes two to tango but three is a tangle: mutualists and cheaters on the carnivorous plant Roridula.Crossref | GoogleScholarGoogle Scholar | 28547414PubMed |
Anderson B, Midgley JJ (2003) Digestive mutualism, an alternate pathway in plant carnivory. Oikos 102, 221–224.
| Digestive mutualism, an alternate pathway in plant carnivory.Crossref | GoogleScholarGoogle Scholar |
Anderson B, Kawakita A, Tayasu I (2012) Sticky plant captures prey for symbiotic bug: is this digestive mutualism? Plant Biology 14, 888–893.
| Sticky plant captures prey for symbiotic bug: is this digestive mutualism?Crossref | GoogleScholarGoogle Scholar | 22449033PubMed |
Bazile V, Moran JA, Le Moguédec G, Marshall DJ, Gaume L (2012) A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism. PLoS ONE 7, e36179
| A carnivorous plant fed by its ant symbiont: a unique multi-faceted nutritional mutualism.Crossref | GoogleScholarGoogle Scholar | 22590524PubMed |
Brearley FQ (2011) Natural abundance of stable isotopes reveals the diversity of carnivorous plant diets. Carnivorous Plant Newsletter 40, 84–87.
Butler JL, Ellison AM (2007) Nitrogen cycling dynamics in the carnivorous northern pitcher plant, Sarracenia purpurea. Functional Ecology 21, 835–843.
| Nitrogen cycling dynamics in the carnivorous northern pitcher plant, Sarracenia purpurea.Crossref | GoogleScholarGoogle Scholar |
Chalk PM (2016) The strategic role of 15N in quantifying the contribution of endophytic N2 fixation to the N nutrition of non-legumes. Symbiosis 69, 63–80.
| The strategic role of 15N in quantifying the contribution of endophytic N2 fixation to the N nutrition of non-legumes.Crossref | GoogleScholarGoogle Scholar |
Chalk PM, Ladha JK (1999) Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution. Soil Biology and Biochemistry 31, 1901–1917.
| Estimation of legume symbiotic dependence: an evaluation of techniques based on 15N dilution.Crossref | GoogleScholarGoogle Scholar |
Chalk P, Smith C (2021) On inorganic N uptake by vascular plants: can 15N tracer techniques resolve the NH4+ vs. NO3− ‘preference’ conundrum? European Journal of Soil Science 72, 1762–1779.
| On inorganic N uptake by vascular plants: can 15N tracer techniques resolve the NH4+ vs. NO3− ‘preference’ conundrum?Crossref | GoogleScholarGoogle Scholar |
Chalk PM, He J-Z, Peoples MB, Chen D (2017) 15N2 as a tracer of biological N2 fixation: a 75-year retrospective. Soil Biology and Biochemistry 106, 36–50.
| 15N2 as a tracer of biological N2 fixation: a 75-year retrospective.Crossref | GoogleScholarGoogle Scholar |
Clarke CM, Bauer U, Lee CIC, Tuen AA, Rembold K, Moran JA (2009) Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant. Biology Letters 5, 632–635.
| Tree shrew lavatories: a novel nitrogen sequestration strategy in a tropical pitcher plant.Crossref | GoogleScholarGoogle Scholar | 19515656PubMed |
Cook JL, Newton J, Millett J (2018) Environmental differences between sites control the diet and nutrition of the carnivorous plant Drosera rotundifolia. Plant and Soil 423, 41–58.
| Environmental differences between sites control the diet and nutrition of the carnivorous plant Drosera rotundifolia.Crossref | GoogleScholarGoogle Scholar | 31402798PubMed |
DeNiro MJ, Epstein S (1981) Influence of diet on the distribution of nitrogen isotopes in animals. Geochimica et Cosmochimica Acta 45, 341–351.
Dixon KW, Pate JS, Bailey WJ (1980) Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves. Australian Journal of Botany 28, 283–297.
| Nitrogen nutrition of the tuberous sundew Drosera erythrorhiza Lindl. with special reference to catch of arthropod fauna by its glandular leaves.Crossref | GoogleScholarGoogle Scholar |
Ellis AG, Midgley JJ (1996) A new plant–animal mutualism involving a plant with sticky leaves and a resident hemipteran insect. Oecologia 106, 478–481.
| A new plant–animal mutualism involving a plant with sticky leaves and a resident hemipteran insect.Crossref | GoogleScholarGoogle Scholar | 28307447PubMed |
Fasbender L, Maurer D, Kreuzwieser J, Kreuzer I, Schulze WX, Kruse J, Becker D, Alfarraj S, Hedrich R, Werner C, Rennenberg H (2017) The carnivorous Venus flytrap uses prey-derived amino acid carbon to fuel respiration. New Phytologist 214, 597–606.
| The carnivorous Venus flytrap uses prey-derived amino acid carbon to fuel respiration.Crossref | GoogleScholarGoogle Scholar |
Friday L, Quarmby C (1994) Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L. New Phytologist 126, 273–281.
| Uptake and translocation of prey-derived 15N and 32P in Utricularia vulgaris L.Crossref | GoogleScholarGoogle Scholar |
Gannes LZ, O’Brien DM, del Rio CM (1997) Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments. Ecology 78, 1271–1276.
| Stable isotopes in animal ecology: assumptions, caveats, and a call for more laboratory experiments.Crossref | GoogleScholarGoogle Scholar |
Gao P, Loeffler TS, Honsel A, Kruse J, Krol E, Scherzer S, Kreuzer I, Bemm F, Buegger F, Burzlaff T, Hedrich R (2015) Integration of trap- and root-derived nitrogen nutrition of carnivorous Dionaea muscipula. New Phytologist 205, 1320–1329.
| Integration of trap- and root-derived nitrogen nutrition of carnivorous Dionaea muscipula.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromelaid Brocchinia reducta, with a cost-benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. The American Naturalist 124, 479–497.
Gonçalves AZ, Mercier H, Mazzafera P, Romero GQ (2011) Spider-fed bromeliads: seasonal and interspecific variation in plant performance. Annals of Botany 107, 1047–1055.
| Spider-fed bromeliads: seasonal and interspecific variation in plant performance.Crossref | GoogleScholarGoogle Scholar | 21385776PubMed |
Gonçalves AZ, Oliveira RS, Oliveira PS, Romero GQ (2016) Species-specific effects of ant inhabitants on bromeliad nutrition. PLoS ONE 11, e0152113
| Species-specific effects of ant inhabitants on bromeliad nutrition.Crossref | GoogleScholarGoogle Scholar | 27002980PubMed |
Grafe TU, Schöner CR, Kerth G, Junaidi A, Schöner MG (2011) A novel resource–service mutualism between bats and pitcher plants. Biology Letters 7, 436–439.
| A novel resource–service mutualism between bats and pitcher plants.Crossref | GoogleScholarGoogle Scholar | 21270023PubMed |
Greenaway W, May J, English S, Whatley FR (1990) Metabolism of [15N] glycine and [13C] glycine by Dionaea muscipula studied by gas chromatography−mass spectrometry. New Phytologist 114, 581–588.
| Metabolism of [15N] glycine and [13C] glycine by Dionaea muscipula studied by gas chromatography−mass spectrometry.Crossref | GoogleScholarGoogle Scholar |
Hanslin HM, Karlsson PS (1996) Nitrogen uptake from prey and substrate as affected by prey capture level and plant reproductive status in four carnivorous plant species. Oecologia 106, 370–375.
| Nitrogen uptake from prey and substrate as affected by prey capture level and plant reproductive status in four carnivorous plant species.Crossref | GoogleScholarGoogle Scholar | 28307324PubMed |
Karagatzides JD, Butler JL, Ellison AM (2009) The pitcher plant Sarracenia purpurea can directly acquire organic nitrogen and short-circuit the inorganic nitrogen cycle. PLoS ONE 4, e6164
| The pitcher plant Sarracenia purpurea can directly acquire organic nitrogen and short-circuit the inorganic nitrogen cycle.Crossref | GoogleScholarGoogle Scholar | 19582167PubMed |
Klink S, Giesemann P, Gebauer G (2019) Picky carnivorous plants? Investigating preferences for preys’ trophic levels – a stable isotope natural abundance approach with two terrestrial and two aquatic Lentibulariaceae tested in Central Europe. Annals of Botany 123, 1167–1177.
| Picky carnivorous plants? Investigating preferences for preys’ trophic levels – a stable isotope natural abundance approach with two terrestrial and two aquatic Lentibulariaceae tested in Central Europe.Crossref | GoogleScholarGoogle Scholar | 30865264PubMed |
Kruse J, Gao P, Honsel A, Kreuzwieser J, Burzlaff T, Alfarraj S, Hedrich R, Rennenberg H (2014) Strategy of nitrogen acquisition and utilization by carnivorous Dionaea muscipula. Oecologia 174, 839–851.
| Strategy of nitrogen acquisition and utilization by carnivorous Dionaea muscipula.Crossref | GoogleScholarGoogle Scholar | 24141381PubMed |
Kruse J, Gao P, Eibelmeier M, Alfarraj S, Rennenberg H (2017) Dynamics of amino acid redistribution in the carnivorous Venus flytrap (Dionaea muscipula) after digestion of 13C/15N-labelled prey. Plant Biology 19, 886–895.
| Dynamics of amino acid redistribution in the carnivorous Venus flytrap (Dionaea muscipula) after digestion of 13C/15N-labelled prey.Crossref | GoogleScholarGoogle Scholar | 28727249PubMed |
Lambers H, Shane MW, Laliberté E, Swarts ND, Teste FP, Zemunik G (2014) Plant mineral nutrition. In ‘Plant life on the sandplains in southwest Australia, a global biodiversity hotspot’. (Ed. H Lambers) pp. 101–127. (UWA Publishing: Perth, WA, Australia)
Lin Q, Ané C, Givnish TJ, Graham SW (2021) A new carnivorous plant lineage (Triantha) with a unique sticky-inflorescence trap. Proceedings of the National Academy of Sciences of the United States of America 118, e2022724118
| A new carnivorous plant lineage (Triantha) with a unique sticky-inflorescence trap.Crossref | GoogleScholarGoogle Scholar | 34373325PubMed |
McPherson S (2007) The carnivorous bromeliads. Journal of the Bromeliad Society 57, 80–88.
Midgley JJ, Stock WD (1998) Natural abundance of δ15N confirms insectivorous habit of Roridula gorgonias, despite it having no proteolytic enzymes. Annals of Botany 82, 387–388.
| Natural abundance of δ15N confirms insectivorous habit of Roridula gorgonias, despite it having no proteolytic enzymes.Crossref | GoogleScholarGoogle Scholar |
Millett J, Jones RI, Waldron S (2003) The contribution of insect prey to the total nitrogen content of sundews (Drosera spp.) determined in situ by stable isotope analysis. New Phytologist 158, 527–534.
| The contribution of insect prey to the total nitrogen content of sundews (Drosera spp.) determined in situ by stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Millett J, Leith ID, Sheppard LJ, Newton J (2012a) Response of Sphagnum papillosum and Drosera rotundifolia to reduced and oxidized wet nitrogen deposition. Folia Geobotanica 47, 179–191.
| Response of Sphagnum papillosum and Drosera rotundifolia to reduced and oxidized wet nitrogen deposition.Crossref | GoogleScholarGoogle Scholar |
Millett J, Svensson BM, Newton J, Rydin H (2012b) Reliance on prey-derived nitrogen by the carnivorous plant Drosera rotundifolia decreases with increasing nitrogen deposition. New Phytologist 195, 182–188.
| Reliance on prey-derived nitrogen by the carnivorous plant Drosera rotundifolia decreases with increasing nitrogen deposition.Crossref | GoogleScholarGoogle Scholar |
Millett J, Foot GW, Svensson BM (2015) Nitrogen deposition and prey nitrogen uptake control the nutrition of the carnivorous plant Drosera rotundifolia. Science of the Total Environment 512–513, 631–636.
| Nitrogen deposition and prey nitrogen uptake control the nutrition of the carnivorous plant Drosera rotundifolia.Crossref | GoogleScholarGoogle Scholar |
Moran JA, Clarke CM (2010) The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions. Plant Signaling & Behavior 5, 644–648.
| The carnivorous syndrome in Nepenthes pitcher plants: current state of knowledge and potential future directions.Crossref | GoogleScholarGoogle Scholar |
Moran JA, Merbach MA, Livingston NJ, Clarke CM, Booth WE (2001) Termite prey specialization in the pitcher plant Nepenthes albomarginata – evidence from stable isotope analysis. Annals of Botany 88, 307–311.
| Termite prey specialization in the pitcher plant Nepenthes albomarginata – evidence from stable isotope analysis.Crossref | GoogleScholarGoogle Scholar |
Moran JA, Clarke CM, Hawkins BJ (2003) From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria. International Journal of Plant Sciences 164, 635–639.
| From carnivore to detritivore? Isotopic evidence for leaf litter utilization by the tropical pitcher plant Nepenthes ampullaria.Crossref | GoogleScholarGoogle Scholar |
Nge FJ, Lambers H (2018) Reassessing protocarnivory – how hungry are triggerplants? Australian Journal of Botany 66, 325–330.
| Reassessing protocarnivory – how hungry are triggerplants?Crossref | GoogleScholarGoogle Scholar |
Nishi AH, Nasconcellos-Neto J, Romero GQ (2013) The role of multiple partners in a digestive mutualism with a protocarnivorous plant. Annals of Botany 111, 143–150.
| The role of multiple partners in a digestive mutualism with a protocarnivorous plant.Crossref | GoogleScholarGoogle Scholar | 23131297PubMed |
Ogle K, Tucker C, Cable JM (2014) Beyond simple linear mixing models: process-based isotope partitioning of ecological processes. Ecological Applications 24, 181–195.
| Beyond simple linear mixing models: process-based isotope partitioning of ecological processes.Crossref | GoogleScholarGoogle Scholar | 24640543PubMed |
Pavlovič A, Slovakova Ľ, Šantrůček J (2011) Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria. Plant, Cell & Environment 34, 1865–1873.
| Nutritional benefit from leaf litter utilization in the pitcher plant Nepenthes ampullaria.Crossref | GoogleScholarGoogle Scholar |
Pavlovič A, Krausko M, Adamec L (2016) A carnivorous sundew plant prefers protein over chitin as a source of nitrogen from its traps. Plant Physiology and Biochemistry 104, 11–16.
| A carnivorous sundew plant prefers protein over chitin as a source of nitrogen from its traps.Crossref | GoogleScholarGoogle Scholar | 26998942PubMed |
Pereira CG, Almenara DP, Winter CE, Fritsch PW, Lambers H, Oliveira RS (2012) Underground leaves of Philcoxia trap and digest nematodes. Proceedings of the National Academy of Sciences of the United States of America 109, 1154–1158.
| Underground leaves of Philcoxia trap and digest nematodes.Crossref | GoogleScholarGoogle Scholar | 22232687PubMed |
Post DM (2002) Using stable isotopes to estimate trophic position: models, methods, and assumptions. Ecology 83, 703–718.
| Using stable isotopes to estimate trophic position: models, methods, and assumptions.Crossref | GoogleScholarGoogle Scholar |
Romero GQ, Mazzafera P, Vasconcellos-Neto J, Trivelin PCO (2006) Bromeliad-living spiders improve host plant nutrition and growth. Ecology 87, 803–808.
| Bromeliad-living spiders improve host plant nutrition and growth.Crossref | GoogleScholarGoogle Scholar | 16676522PubMed |
Romero GQ, Vasconcellos-Neto J, Trivelin PCO (2008) Spatial variation in the strength of mutualism between a jumping spider and a terrestrial bromeliad: evidence from the stable isotope 15N. Acta Oecologica 33, 380–386.
| Spatial variation in the strength of mutualism between a jumping spider and a terrestrial bromeliad: evidence from the stable isotope 15N.Crossref | GoogleScholarGoogle Scholar |
Romero GQ, Nomura F, Gonçalves AZ, Dias NYN, Mercier H, Conforto EDC, Rossa-Feres DDC (2010) Nitrogen fluxes from treefrogs to tank epiphytic bromeliads: an isotopic and physiological approach. Oecologia 162, 941–949.
| Nitrogen fluxes from treefrogs to tank epiphytic bromeliads: an isotopic and physiological approach.Crossref | GoogleScholarGoogle Scholar | 20024585PubMed |
Rowland K (2012) Hungry plant traps worms underground. Nature 55, 9757
| Hungry plant traps worms underground.Crossref | GoogleScholarGoogle Scholar |
Scharmann M, Thornham DG, Grafe TU, Federle W (2013) A novel type of nutritional ant–plant interaction: ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna. PLoS ONE 8, e63556
| A novel type of nutritional ant–plant interaction: ant partners of carnivorous pitcher plants prevent nutrient export by dipteran pitcher infauna.Crossref | GoogleScholarGoogle Scholar | 23717446PubMed |
Schöner CR, Schöner MG, Grafe TU, Clarke CM, Dombrowski L, Tan MC, Kerth G (2017) Ecological outsourcing: a pitcher plant benefits from transferring pre-digestion of prey to a bat mutualist. Journal of Ecology 105, 400–411.
| Ecological outsourcing: a pitcher plant benefits from transferring pre-digestion of prey to a bat mutualist.Crossref | GoogleScholarGoogle Scholar |
Schulze E-D, Gebauer G, Schulze W, Pate JS (1991) The utilization of nitrogen from insect capture by different growth forms of Drosera from Southwest Australia. Oecologia 87, 240–246.
| The utilization of nitrogen from insect capture by different growth forms of Drosera from Southwest Australia.Crossref | GoogleScholarGoogle Scholar |
Schulze W, Schulze ED, Pate JS, Gillison AN (1997) The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica. Oecologia 112, 464–471.
| The nitrogen supply from soils and insects during growth of the pitcher plants Nepenthes mirabilis, Cephalotus follicularis and Darlingtonia californica.Crossref | GoogleScholarGoogle Scholar | 28307622PubMed |
Schulze W, Schulze ED, Schulze I, Oren R (2001) Quantification of insect nitrogen utilization by the venus fly trap Dionaea muscipula catching prey with highly variable isotope signatures. Journal of Experimental Botany 52, 1041–1049.
| Quantification of insect nitrogen utilization by the venus fly trap Dionaea muscipula catching prey with highly variable isotope signatures.Crossref | GoogleScholarGoogle Scholar | 11432920PubMed |
Sirová D, Šantrůček J, Adamec L, Bárta J, Borovec J, Pech J, Owens SM, Šantrůčková H, Schäufele R, Štorchová H, Vrba J (2014) Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important? Annals of Botany 114, 125–133.
| Dinitrogen fixation associated with shoots of aquatic carnivorous plants: is it ecologically important?Crossref | GoogleScholarGoogle Scholar | 24817095PubMed |
Skates LM, Paniw M, Cross AT, Ojeda F, Dixon KW, Stevens JC, Gebauer G (2019) An ecological perspective on ‘plant carnivory beyond bogs’: nutritional benefits of prey capture for the Mediterranean carnivorous plant Drosophyllum lusitanicum. Annals of Botany 124, 65–76.
| An ecological perspective on ‘plant carnivory beyond bogs’: nutritional benefits of prey capture for the Mediterranean carnivorous plant Drosophyllum lusitanicum.Crossref | GoogleScholarGoogle Scholar | 31329814PubMed |
Smith CJ, Chalk PM (2021) Organic N compounds in plant nutrition: have methodologies based on stable isotopes provided unequivocal evidence of direct N uptake? Isotopes in Environmental and Health Studies 57, 333–349.
| Organic N compounds in plant nutrition: have methodologies based on stable isotopes provided unequivocal evidence of direct N uptake?Crossref | GoogleScholarGoogle Scholar | 34074191PubMed |
Tiunov AV (2007) Stable isotopes of carbon and nitrogen in soil ecological studies. Biology Bulletin 34, 395–407.
| Stable isotopes of carbon and nitrogen in soil ecological studies.Crossref | GoogleScholarGoogle Scholar |
