Nitrogen deposition and prey nitrogen uptake control the nutrition of the carnivorous plant Drosera rotundifolia

Abstract

2 AbstractNitrogen (N) deposition has important negative impacts on natural and semi-natural ecosystems, impacting on biotic interactions across trophic levels. Low-nutrient systems are particularly sensitive to changes in N inputs and are therefore more vulnerable to N deposition. Carnivorous plants are often part of these ecosystems partly because of the additional nutrients obtained from prey. We studied the impact of N deposition on the nutrition of the carnivorous plant Drosera rotundifolia growing on 16 ombrotrophic bogs across Europe. We measured tissue N, phosphorus (P) and potassium (K) concentrations and prey and root N uptake using a natural abundance stable isotope approach. Our aim was to test the impact of N deposition on D.rotundifolia prey and root N uptake, and nutrient stoichiometry. Drosera rotundifolia root N uptake was strongly affected by N deposition, possibly resulting in reduced N limitation. The contribution of prey N to the N contained in D. rotundifolia ranged from 20 to 60%. N deposition reduced the maximum amount of N derived from prey, but this varied below this maximum. Drosera rotundifolia tissue N concentrations were a product of both root N availability and prey N uptake. Increased prey N uptake was correlated with increased tissue P concentrations indicating uptake of P from prey. N deposition therefore reduced the strength of a carnivorous plant-prey interaction, resulting in a reduction in nutrient transfer between trophic levels. We suggest that N deposition has a negative impact on D. rotundifolia and that responses to N deposition might be strongly site specific.Key words: atmospheric nitrogen deposition; carnivorous plants; Drosera rotundifolia; plantinsect interactions; round-leaved sundew; stable isotopes 3 IntroductionAtmospheric nitrogen (N) deposition is a globally important pollutant (Galloway et al. 2008;Bobbink et al. 2010), which has significant local and regional impacts on ecosystems (Bobbink et al. 2010). N deposition increases N availability which can have direct impacts on individual plants (Tomassen et al. 2003;van Heerwaarden et al. 2003) and can also impact species interactions across trophic levels (Tylianakis et al. 2008). Understanding these impacts is crucial because they can result in altered species abundance, plant community composition Carnivorous plants supplement nutrients obtained through root uptake by capturing, digesting and assimilating the nutrients in animal prey, usually arthropods (Juniper et al. 1989).The uptake of prey nutrients uncouples growth and reproduction from root nutrient availability and enables carnivorous plants to successfully compete with non-carnivorous plants ( Karlsson et al. 1996) when N availability is low. The value of the captured prey is dependent on root nutrient availability; responses to prey addition are normally reduced or absent in more nutrient replete plants (Ellison 2006). Carnivorous plants can also forage for prey, reducing investment in prey capture when the value of that prey is reduced Thorén et a...

Occurrence of myo-inositol and alkyl-substituted polysaccharide in the prey-trapping mucilage of Drosera capensis

“…Indeed, putative diazotrophic bacteria have been reported to be enriched in the rhizosphere and in the root tissues of a related species Drosera villosa , despite the presumably hostile acidic environment for the bacteria (Albino et al 2006 ). Access to inorganic N through root is advantageous, since the N is immediately useable to incorporate into metabolic grids without further digestion (Kraiser et al 2011 ; Millett et al 2015 ). Potentially, N-fixing bacteria have also been found on the pitcher of Sarracenia minor (Sarraceniaceae) and in the acidic fluids (Siragusa et al 2007 ).…”

“…The presence of NFB has also been confirmed inside the traps of the aquatic carnivorous plants of Utricularia (Lentibulariaceae) (Sirová et al 2014 ), although those NFB may be bycatch in the same way inanimate microalgae and pollens are sucked into the traps (Koller-Peroutka et al 2015 ). Overall, the bacterial associates may be underappreciated source of N beside animal preys, their predators at higher trophic levels, and atmospheric deposition (Millett et al 2015 ; Pavlovič et al 2016 ).…”

The Effect of Fertilizers on Biomass and Biodiversity on a Semi-Arid Grassland of Northern China

“…It has been proven that aboveground biomass increases with N input across various ecosystems [9,10]. However, some studies have illustrated that irrational fertilization would cause atmospheric N deposition and pollution, and that low-nutrient systems, such as natural ecosystems, are especially sensitive to N inputs and are therefore more susceptible to N deposition [11]. Specifically, N deposition has been shown to affect species interaction at the trophic level [12] and then change species abundance, plant community composition [13], and even decrease biodiversity [14].…”

Geographic variation in Sundew (Drosera) leaf colour: plant–plant interactions counteract expected effects of abiotic factors

“…The equation for each line is presented in Appendix S7, site codes are explained in Appendix S1. Individual leaf colour and vegetation influence measures are shown in Table 2 (Millett et al, 2012(Millett et al, , 2015 and might warrant further investigation of the potential for local adaptation. Our data also raise a number of further questions.…”

“…Understanding the patterns and causes of this within-species geographic variability in traits can, therefore, provide insight into the links between plant function, biotic and abiotic interactions (Gaston, Chown, & Evans, 2008). It can also help us to understand the impacts on ecosystems of anthropogenic drivers such as altered precipitation patterns and increased temperature (Millien et al, 2006;Zeuss, Brandl, Br€ andle, Rahbek, & Brunzel, 2014), and deposition of atmospheric pollutants such as nitrogen and sulphur (Ellison & Gotelli, 2002;Millett, Foot, & Svensson, 2015). For example, phenotypic variability along latitudinal gradients reflects the combination of adaptive and plastic effects, which can inform understanding of the effects of warming on plant distributions (De Frenne et al, 2013); latitudinal gradients in nitrogen deposition have also been used to better understand species responses to atmospheric nitrogen deposition (e.g.…”