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DNA Metabarcoding Reveals Changes in the Contents of Carnivorous Plants Along an Elevation Gradient

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DNA Metabarcoding Reveals Changes in the Contents of Carnivorous Plants Along an Elevation Gradient Published in "Molecular Ecology 28(2): 281–292, 2019" which should be cited to refer to this work. DNA metabarcoding reveals changes in the contents of carnivorous plants along an elevation gradient Joanne E. Littlefair1,2 | Axel Zander3 | Clara de Sena Costa2 | Elizabeth L. Clare2 1Department of Biology, McGill University, Montréal, Québec, Canada Abstract 2School of Biological and Chemical Resource variation along abiotic gradients influences subsequent trophic interac- Sciences, Queen Mary University of tions and these effects can be transmitted through entire food webs. Interactions London, London, UK 3Department of Biology, Unit of Ecology along abiotic gradients can provide clues as to how organisms will face changing and Evolution, University of Fribourg, environmental conditions, such as future range shifts. However, it is challenging to Fribourg, Switzerland find replicated systems to study these effects. Phytotelmata, such as those found in Correspondence carnivorous plants, are isolated aquatic communities and thus form a good model Joanne E. Littlefair, Department of Biology, McGill University, Montréal, Québec, for the study of replicated food webs. Due to the degraded nature of the prey, Canada. molecular techniques provide a useful tool to study these communities. We studied Email: [email protected] the pitcher plant Sarracenia purpurea L. in allochthonous populations along an eleva- Funding information tional gradient in the Alps and Jura. We predicted that invertebrate richness in the Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen contents of the pitcher plants would decrease with increasing elevation, reflecting Forschung, Grant/Award Number: harsher environmental conditions. Using metabarcoding of the COI gene, we 31003A_138489 sequenced the invertebrate contents of these pitcher plants. We assigned Molecu- lar Operational Taxonomic Units at ordinal level as well as recovering species‐level data. We found small but significant changes in community composition with eleva- tion. These recovered sequences could belong to invertebrate prey, rotifer inquili- nes, pollinators and other animals possibly living inside the pitchers. However, we found no directional trend or site‐based differences in MOTU richness with eleva- tional gradient. Use of molecular techniques for dietary or contents analysis is a powerful way to examine numerous degraded samples, although factors such as DNA persistence and the relationship with species presence still have to be com- http://doc.rero.ch pletely determined. KEYWORDS carnivory, DNA metabarcoding, food web, invasive, molecular dietary analysis, plant–insect interactions, Sarracenia purpurea 1 | INTRODUCTION Baltz, & Allen, 2002; O'Gorman et al., 2012). Studies of how resource use varies along environmental gradients are likely to be Spatial and temporal variation in resource distribution is present important for understanding species invasions (Gallien et al., 2015), throughout an organism's environment. Environmental resources and and responses to climate change scenarios as species undergo range stressors may be organized in a spatial hierarchy or along a gradient, shifts (Colwell, Brehm, Cardelus, Gilman, & Longino, 2008; Parme- as is the case for heat stress and elevation, or pressure and ocean san, 2006). Gradients can also serve as natural experiments to depth (Desmarais & Tessier, 1999; Flesch & Steidl, 2010; Jones, extrapolate the temporal variability of communities and ecosystems | 1 (Fukami & Wardle, 2005; Lester, Close, Barton, Pope, & Brown, technologies such as metabarcoding, the massively parallel sequenc- 2014). ing of targeted gene fragments from all components of an environ- Elevation is one source of variation in resource distribution. mental sample, are now commonly used to analyse the partially Resources alter either as a direct result of abiotic factors or from the digested elements of diet. Metabarcoding is fast becoming the tool effects of abiotic factors on biotic components. Abiotic conditions of choice in dietary analyses, including work on a wide range of diet vary with elevation: higher altitudes are strongly associated with types such as liquids (sap, blood, nectar, etc.), prey which do not exposure to colder temperatures (known as the lapse rate), more leave hard remains or where destructive sampling is not ethical, or extreme weather patterns, greater exposure to UV, lower atmo- the material highly degraded (Clare, 2014; Pompanon et al., 2012). spheric pressure and lower oxygen availability (Blumthaler, 2012; Clustering sequences into Molecular Operational Taxonomic Units Hodkinson, 2005). Common biotic responses include shifts in species (MOTU) (Floyd, Abebe, Papert, & Blaxter, 2002) can be used to quan- distribution, or complete species replacement, as organisms differ in tify diversity for subsequent ecological analyses (Clare, Chain, Little- their environmental tolerances (e.g., thermal limits Sundqvist, San- fair, & Cristescu, 2016). ders, & Wardle, 2013). Although it was initially thought that biodi- In this study, we examine how the invertebrate contents of a versity decreases with increasing elevation, Rahbek (2005) carnivorous pitcher plant (Sarracenia purpurea) alter over an eleva- demonstrated a peak in diversity at midelevation, which holds true tional gradient. The natural range of S. purpurea extends from Florida for 75% of elevational gradients examined (Rahbek, 2005; Sundqvist to subarctic Canada, in nutrient‐limited areas (Kneitel & Miller, et al., 2013), although different functional groups will vary in their 2002). However, S. purpurea has been frequently introduced in Bri- response (Sundqvist et al., 2013). tain, Ireland and central Europe from escaped ornamentals and delib- When gradients influence species distributions, we expect varia- erate planting in bog areas, and displays invasive characteristics in tion in trophic relationships within ecosystems. For example, the certain areas of central Europe due to its frost‐hardy nature change in biodiversity with elevation will influence predator–prey (Adlassnig, Mayer, Peroutka, Pois, & Lichtsheidl, 2010; Walker, 2014; and host–parasite interactions (Case, Holt, Mcpeek, & Keitt, 2005). Zander, Gravel, Bersier, & Gray, 2016). Sarracenia purpurea is a par- This is difficult to study on a spatially replicated scale in the field, ticularly interesting case for the study of elevation gradients as the although attempts have been made experimentally (Greig, Wissinger, plant is allochthonous in the Alps, and thus, it has not undergone & Mcintosh, 2013). Phytotelmata are isolated aquatic communities long‐term adaptation to the environment. As such, we can assess that form natural mesocosms in living terrestrial plants, such as resource variation induced by elevational gradients against a back- bromeliads, tree holes and certain types of carnivorous plant (Kitch- ground of species invasion. ing, 2000), and can be studied as small replicated ecosystems located In this study, we use DNA metabarcoding techniques to investi- within a larger landscape (Kitching, 2000). gate the contents of Sarracenia purpurea across sites in France and The leaves of pitcher plants form phytotelmata, connecting the Switzerland over an elevation gradient of 850 m. We assess how external environment to an enclosed aquatic food web of inquilines MOTU richness and community composition of invertebrate con- that aid in the decomposition of invertebrate prey. Prey are sources tents of pitcher plants changes with elevation, and test for linear of nitrogen and phosphorus, which compensate for the nutrient‐poor and other relationships between elevation gradient and MOTU rich- environments which the pitcher plants inhabit. Prey capture has ness. Finally, we predict that community dissimilarity will vary in been shown to increase plant fitness (Zamora, Gomez, & Hodar, such a way that the most similar communities are closer in elevation 1997), and the inquiline food web is limited by prey capture (Heard, to each other. http://doc.rero.ch 1994). Unlike bromeliads or tree holes, which are primarily contain- ers, pitcher plants are an active part of the phytotelmata ecosystem. 2 | MATERIALS AND METHODS While obtaining nutrients is crucial for both plant and inquiline biol- ogy, it is not known to what extent the invertebrate contents of 2.1 | Sample collection pitcher plants are shaped by gradients such as elevation which can structure resources. Here, we test the ecological hypothesis that We collected samples of pitcher contents from Sarracenia purpurea pitcher plant phytotelmata contents are influenced by elevational pitchers in five locations in the Alps, Jura Mountains and the Swiss gradients. Plateau (Switzerland and France), between October 29 and Novem- The morphological identification of prey is often complicated by ber 28, 2014. Our sampling locations comprised of raised bogs, fens digestion and degradation. This problem has been encountered both and alpine wetlands at Champ Buet (46°36′41″N 6°34′41″E, ca. generally (Pompanon et al., 2012; Valentini et al., 2009), and specifi- 600 m a.s.l), Frasne (46°49′35″N 6°10′25″E, ca. 800 m a.s.l), Les cally in pitcher plants, where studies refer to an unidentified mass of Embreux (47°15′44″N 7°6′57″E, ca. 1000 m a.s.l), Les Tenasses insect exoskeletons (Cresswell, 1991; Horner, Steele, Underwood, & (46°29′28.37″N 6°55′15.00″E, ca. 1200 m a.s.l) and Les Mosses Lingamfelter, 2012). Additionally, the characterization of food webs (46°23′47.10″N,
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