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Different Pitcher Shapes and Trapping Syndromes Explain Resource Partitioning in Nepenthes Species Laurence Gaume, Vincent Bazile, Maïlis Huguin, Vincent Bonhomme

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Different Pitcher Shapes and Trapping Syndromes Explain Resource Partitioning in Nepenthes Species Laurence Gaume, Vincent Bazile, Maïlis Huguin, Vincent Bonhomme Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species Laurence Gaume, Vincent Bazile, Maïlis Huguin, Vincent Bonhomme To cite this version: Laurence Gaume, Vincent Bazile, Maïlis Huguin, Vincent Bonhomme. Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species. Ecology and Evolution, Wiley Open Access, 2016, 6 (5), pp.1378-1392. 10.1002/ece3.1920. hal-01289725 HAL Id: hal-01289725 https://hal-sde.archives-ouvertes.fr/hal-01289725 Submitted on 20 Nov 2019 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Different pitcher shapes and trapping syndromes explain resource partitioning in Nepenthes species Laurence Gaume1,2, Vincent Bazile1,Ma€ılis Huguin2,3 & Vincent Bonhomme1,4 1Universite de Montpellier, UMR AMAP: botAnique et Modelisation de l’Architecture des Plantes et des veg etations, CIRAD – TA A51/PS2, Boulevard de la Lironde, F-34398 Montpellier, France 2CNRS, UMR AMAP: botAnique et Modelisation de l’Architecture des Plantes et des veg etations, CIRAD – TA A51/PS2, Boulevard de la Lironde, F-34398 Montpellier, France 3Universite Francßois Rabelais, 60 rue du Plat D’Etain, F-37020 Tours, France 4Universite de Montpellier, UMR 5554 Institut des Sciences de l’Evolution, Place Eugene Bataillon, F-34095 Montpellier, France Keywords Abstract Adaptation, carnivorous plant, niche segregation, pitcher morphology, prey Nepenthes pitcher plants display interspecific diversity in pitcher form and diets. composition. This species-rich genus might be a conspicuous candidate for an adaptive radia- tion. However, the pitcher traits of different species have never been quantified Correspondence in a comparative study, nor have their possible adaptations to the resources Laurence Gaume, AMAP: botAnique et they exploit been tested. In this study, we compare the pitcher features and Modelisation de l’Architecture des Plantes et prey composition of the seven Nepenthes taxa that grow in the heath forest of des veg etations, CIRAD – TA A51 / PS2, Boulevard de la Lironde, F-34398 Montpellier Brunei (Borneo) and investigate whether these species display different trapping Cedex 5, France. syndromes that target different prey. The Nepenthes species are shown to dis- Tel: 33 4 67 61 71 66; play species-specific combinations of pitcher shapes, volumes, rewards, attrac- Fax: 33 4 67 61 56 68; tion and capture traits, and different degrees of ontogenetic pitcher E-mail: [email protected] dimorphism. The prey spectra also differ among plant species and between ontogenetic morphotypes in their combinations of ants, flying insects, termites, Funding Information and noninsect guilds. According to a discriminant analysis, the Nepenthes spe- Centre National de la Recherche Scientifique. cies collected at the same site differ significantly in prey abundance and compo- Received: 24 September 2015; Revised: 30 sition at the level of order, showing niche segregation but with varying degrees November 2015; Accepted: 1 December of niche overlap according to pairwise species comparisons. Weakly carnivorous 2015 species are first characterized by an absence of attractive traits. Generalist car- nivorous species have a sweet odor, a wide pitcher aperture, and an acidic pitcher fluid. Guild specializations are explained by different combinations of morpho-functional traits. Ant captures increase with extrafloral nectar, fluid doi: 10.1002/ece3.1920 acidity, and slippery waxy walls. Termite captures increase with narrowness of pitchers, presence of a rim of edible trichomes, and symbiotic association with ants. The abundance of flying insects is primarily correlated with pitcher conic- ity, pitcher aperture diameter, and odor presence. Such species-specific syn- dromes favoring resource partitioning may result from local character displacement by competition and/or previous adaptations to geographically distinct environments. Introduction exploit a variety of different resources (Schluter 2000). Archipelagos often favor adaptive radiations because the One of the fundamental aims of research in ecology and different islands represent different opportunities for colo- evolution is to understand the origin and cause of species nization and habitats characterized by specific climatic diversity. Adaptive radiations are a major feature of spe- and ecological conditions (Jorgensen and Olesen 2001). cies diversification. An adaptive radiation is defined as The best known adaptive radiation is certainly that the rapid diversification of a lineage into species display- of Darwin’s finches in the Galapagos Islands. This exam- ing different morphological or physiological traits used to ple presents the evolution of different species of the ª 2016 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 1 This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Pitcher Traits Condition Nepenthes Diet L. Gaume et al. Geospizinae with specific morphological adaptations of juvenile stage to a mature, flower-producing stage (Lee their beak to different diets reflecting the resources of and Richards 1991). The genus Nepenthes also displays a their habitat (Darwin 1859; Grant and Grant 2002). great diversity of mechanisms of insect attraction and Similarly, the carnivorous plants of the genus Nepenthes capture (Moran et al. 1999, 2013; Bonhomme et al. (Caryophyllales: Nepenthaceae) may be good candidates 2011b; Bazile et al. 2015). To attract insect prey, for an adaptive radiation with respect to trap morphology Nepenthes species display different attracting signals rang- and nutrient sequestration strategy (Pavlovic 2012). The ing from nectar rewards (Bauer et al. 2009), emission of genus Nepenthes is distributed from Madagascar to New volatile compounds (Di Giusto et al. 2010) to visual cues Caledonia and comprises 164 species, with hotspots of (Moran et al. 1999). To capture insects, the genus deploys diversity in the islands of Borneo (Clarke 1997), Sumatra different combinations of mechanisms as diverse as a wet- (Clarke 2001), and the Philippines (McPherson 2009). table peristome (Bohn and Federle 2004), trap walls cov- The islands of Southeastern Asia have undergone an ered by a slippery waxy layer (Gaume et al. 2002), traps eventful geological and climatic history during the most filled with a viscoelastic digestive fluid (Gaume and recent glaciations with numerous episodes of sea-level Forterre 2007), or light traps (Moran et al. 2012). changes, creating refuge zones for species and block settle- Additionally, there is also an increasing body of evi- ments (Woodruff 2010). Some studies based on fossil dence that Nepenthes pitcher plants differ in their diet, data give an estimate of the first diversification of with certain species displaying nutrition strategies, which Nepenthes at 65 million years, with a diversification in are sometimes more detritivorous (Moran et al. 2003; South-Eastern Asia dating from the Pliocene/Pleistocene, Pavlovic et al. 2011) or partially coprophagous (Clarke that is, 1.5–3 million years (Meimberg et al. 2001). The et al. 2009; Grafe et al. 2011) than purely carnivorous genus Nepenthes, with such a relatively recent diversifica- strategies. Among insectivorous plants, although ants and tion and with its numerous species, most of which are flies are the two main prey items, the prey assemblages endemic species with restricted geographical distributions, appear to differ among Nepenthes species (Kato et al. could thus represent a conspicuous case of rapid and pro- 1993; Adam 1997; Chin et al. 2014). fuse speciation. However, neither the interspecific diver- However, there is still little evidence in the genus sity in trap morphology nor its possible adaptive Nepenthes for any adaptive significance of trap character- significance has so far been investigated based on quanti- istics in terms of species’ diet. The possible correspon- tative approaches. dence between trap geometry and type of nitrogen source The Nepenthes species are tropical vines that grow has only been investigated in the noncarnivorous species solely or coexist in different habitats such as heath forest, bearing large traps, such as Nepenthes rajah, N. lowii, and peat swamp forest, mangroves, and cloudy montane for- N. macrophylla. For those species, the trap geometry per- ests on diverse infertile substrates including white sands, fectly matches the body size of the tree shrew that defe- peat, cliffs, ultramafic soils, or epiphytic substrates. All cates into the trap (Chin et al. 2010). In carnivorous these substrates are characterized by a scarcity of nutri- species, some studies have shown that specific traits can ents, especially nitrogen, or their nonavailability in a form favor the capture of a specific guild of insects. In this easily assimilated (Vitousek and Howarth 1991; Yule way, the capture of flies is favored by viscoelastic fluids 2010). These vines have evolved, at
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