Reassessing protocarnivory – how hungry are triggerplants?
Francis J. Nge A B C and Hans Lambers AA School of Biological Sciences, University of Western Australia, 35 Stirling Highway, Crawley (Perth), WA 6009, Australia.
B School of Biological Sciences, Faculty of Science, The University of Adelaide, Adelaide, SA 5005, Australia.
C Corresponding author. Email: francis.nge@adelaide.edu.au
Australian Journal of Botany 66(4) 325-330 https://doi.org/10.1071/BT18059
Submitted: 20 March 2018 Accepted: 7 June 2018 Published: 9 July 2018
Abstract
Stylidium species (triggerplants) are claimed to be protocarnivorous based on the presence of glandular hairs, observations of trapped small organisms, and induction of proteinase activity. However, these traits might serve alternative functions. We aimed to re-assess and quantify the degree of carnivory for Stylidium species in an ecological context, by comparing the natural abundance (δ15N) of Stylidium species with co-occurring carnivorous (Drosera species) and non-carnivorous plants in their natural habitats. We hypothesised that the δ15N signature of Stylidium species would more closely match co-occurring carnivorous plant species than their non-carnivorous counterparts if they rely on captured organisms as a nutrient source, since there is an increase in fractionation by 3–5 ‰ per trophic level. Our results show that the Stylidium species sampled had δ15N signatures that matched more closely with co-occurring non-carnivorous plants than with carnivorous Drosera species. This does not support the claim that they rely on captured organisms as a nitrogen source, or the source is negligible. Other studies have shown that protocarnivorous species have a δ15N signature that is more similar to that of co-occurring carnivorous than that of non-carnivorous species. Therefore, our findings question the protocarnivory status of Stylidium species.
Additional keywords: carnivorous plants, Drosera, insectivorous plants, protocarnivorous plants, stable nitrogen isotopes, Stylidium, Stylidiaceae.
References
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 |
Anderson B, Midgley J (2003) Digestive mutualism, an alternate pathway in plant carnivory. Oikos 102, 221–224.
| Digestive mutualism, an alternate pathway in plant carnivory.Crossref | GoogleScholarGoogle Scholar |
Brearley F (2011) Natural abundance of stable isotopes reveals the diversity of carnivorous plant diets. Carnivorous Plant Newsletter 40, 84–87.
Darnowski DW (2017) Further evidence of carnivory in triggerplants (Stylidium spp.; Stylidiaceae). Carnivorous Plant Newsletter 46, 28–29.
Darnowski DW, Carroll DM, Płachno B, Kabanoff E, Cinnamon E (2006) Evidence of protocarnivory in triggerplants (Stylidium spp.; Stylidiaceae). Plant Biology 8, 805–812.
| Evidence of protocarnivory in triggerplants (Stylidium spp.; Stylidiaceae).Crossref | GoogleScholarGoogle Scholar |
Ellison AM, Gotelli NJ (2001) Evolutionary ecology of carnivorous plants. Trends in Ecology & Evolution 16, 623–629.
| Evolutionary ecology of carnivorous plants.Crossref | GoogleScholarGoogle Scholar |
Fahn A (1979) ‘Secretory tissues in plants.’ (Academic Press: London)
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. American Naturalist 124, 479–497.
| Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats.Crossref | GoogleScholarGoogle Scholar |
Högberg P (1990) 15N natural abundance as a possible marker of the ectomycorrhizal habit of trees in mixed African woodlands. New Phytologist 115, 483–486.
| 15N natural abundance as a possible marker of the ectomycorrhizal habit of trees in mixed African woodlands.Crossref | GoogleScholarGoogle Scholar |
Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biometrical Journal. Biometrische Zeitschrift 50, 346–363.
| Simultaneous inference in general parametric models.Crossref | GoogleScholarGoogle Scholar |
Lamont BB (1994) Triangular trophic relationships in Mediterranean-climate Western Australia. In ‘Plant-animal interactions in Mediterranean-type ecosystems. Vol. 31’. (Eds M Arianoutsou, RH Groves) pp. 83–89. (Springer: Dordrecht, The Netherlands)
Levin DA (1973) The role of trichomes in plant defense. Quarterly Review of Biology 48, 3–15.
| The role of trichomes in plant defense.Crossref | GoogleScholarGoogle Scholar |
Lloyd FE (1934) Is Roridula a carnivorous plant? Canadian Journal of Research 10, 780–786.
| Is Roridula a carnivorous plant?Crossref | GoogleScholarGoogle Scholar |
Midgley J, Stock W (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 |
Mithöfer A (2011) Carnivorous pitcher plants: insights in an old topic. Phytochemistry 72, 1678–1682.
| Carnivorous pitcher plants: insights in an old topic.Crossref | GoogleScholarGoogle Scholar |
Nishi AH, Vasconcellos-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 |
Pinheiro J, Bates D, DebRoy S, Sarkar D, R Core Team (2014) nlme: linear and nonlinear mixed effects models. R package ver. 3.1–117. Available at https://CRAN.R-project.org/package=nlme [Verified 23 June 2018]
Płachno BJ, Adamec L, Huet H (2009) Mineral nutrient uptake from prey and glandular phosphatase activity as a dual test of carnivory in semi-desert plants with glandular leaves suspected of carnivory. Annals of Botany 104, 649–654.
| Mineral nutrient uptake from prey and glandular phosphatase activity as a dual test of carnivory in semi-desert plants with glandular leaves suspected of carnivory.Crossref | GoogleScholarGoogle Scholar |
R Core Team (2016) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria) Available at http://www.R-project.org/ [Verified 6 May 2017]
Schmidt S, Stewart G (1997) Waterlogging and fire impacts on nitrogen availability and utilization in a subtropical wet heathland (wallum). Plant, Cell & Environment 20, 1231–1241.
| Waterlogging and fire impacts on nitrogen availability and utilization in a subtropical wet heathland (wallum).Crossref | GoogleScholarGoogle Scholar |
Schulze E-D, Gebauer G, Schulze W, Pate J (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 |
Spomer GG (1999) Evidence of protocarnivorous capabilities in Geranium viscosissimum and Potentilla arguta and other sticky plants. International Journal of Plant Sciences 160, 98–101.
| Evidence of protocarnivorous capabilities in Geranium viscosissimum and Potentilla arguta and other sticky plants.Crossref | GoogleScholarGoogle Scholar |
Tingey WM, Laubengayer JE (1981) Defense against the green peach aphid and potato leafhopper by glandular trichomes of Solanum berthaultii. Journal of Economic Entomology 74, 721–725.
| Defense against the green peach aphid and potato leafhopper by glandular trichomes of Solanum berthaultii.Crossref | GoogleScholarGoogle Scholar |
Voigt D, Gorb S (2010) Desiccation resistance of adhesive secretion in the protocarnivorous plant Roridula gorgonias as an adaptation to periodically dry environment. Planta 232, 1511–1515.
| Desiccation resistance of adhesive secretion in the protocarnivorous plant Roridula gorgonias as an adaptation to periodically dry environment.Crossref | GoogleScholarGoogle Scholar |