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Are Ontogenetic Shifts in Foliar Structure and Resource Acquisition Are ontogenetic shifts in foliar structure and resource acquisition spatially conditioned in tank-bromeliads? Matthis Petit, Régis Céréghino, Jean-François Carrias, Bruno Corbara, Olivier Dezerald, Fréderic Petitclerc, Alain Dejean, Céline Leroy To cite this version: Matthis Petit, Régis Céréghino, Jean-François Carrias, Bruno Corbara, Olivier Dezerald, et al.. Are ontogenetic shifts in foliar structure and resource acquisition spatially conditioned in tank-bromeliads?. Botanical Journal of the Linnean Society, Linnean Society of London, 2014, 175 (2), pp.299-312. 10.1111/boj.12171. hal-02181065 HAL Id: hal-02181065 https://hal.archives-ouvertes.fr/hal-02181065 Submitted on 11 Jul 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. bs_bs_banner Botanical Journal of the Linnean Society, 2014, 175, 299–312. With 4 figures Are ontogenetic shifts in foliar structure and resource acquisition spatially conditioned in tank-bromeliads? MATTHIS PETIT1,2, RÉGIS CÉRÉGHINO3,4, JEAN-FRANÇOIS CARRIAS5,6, BRUNO CORBARA5,6, OLIVIER DÉZERALD2, FRÉDERIC PETITCLERC2, ALAIN DEJEAN2,3 and CÉLINE LEROY7* 1AgroParisTech’, UMR EcoFoG (Ecologie des Forêts de Guyane), Campus Agronomique, F-97379 Kourou Cedex, France 2CNRS, UMR EcoFoG, Campus Agronomique, F-97379 Kourou Cedex, France 3INP, UPS EcoLab (Laboratoire Ecologie Fonctionnelle et Environnement), Université de Toulouse, F-31062 Toulouse, France 4CNRS, EcoLab, 118 Route de Narbonne, F-31062 Toulouse, France 5Clermont Université, Université Blaise Pascal, BP 10448, F-63000 Clermont-Ferrand, France 6CNRS, UMR 6023, Laboratoire Microorganismes: Génome et Environnement, BP 80026, F-63171 Aubière cedex, France 7IRD, UMR AMAP (botAnique et bioinforMatique de l’Architecture des Plantes), Boulevard de la Lironde, TA A-51/PS2, F-34398 Montpellier Cedex 5, France Received 22 October 2013; revised 17 January 2014; accepted for publication 27 March 2014 The phenotypic plasticity of plants has been explored as a function of either ontogeny (apparent plasticity) or environment (adaptive plasticity), although few studies have analyzed these factors together. In the present study, we take advantage of the dispersal of Aechmea mertensii bromeliads by Camponotus femoratus or Pachycondyla goeldii ants in shaded and sunny environments, respectively, to quantify ontogenetic changes in morphological, foliar, and functional traits, and to analyze ontogenetic and ant species effects on 14 traits. Most of the morphological (plant height, number of leaves), foliar (leaf thickness, leaf mass area, total water content, trichome density), and functional (leaf δ13C) traits differed as a function of ontogeny. Conversely, only leaf δ15N showed an adaptive phenotypic plasticity. On the other hand, plant width, tank width, longest leaf length, stomatal density, and leaf C concentration showed an adaptation to local environment with ontogeny. The exception was leaf N concentration, which showed no trend at all. Aechmea mertensii did not show an abrupt morphological modification such as in heteroblastic bromeliads, although it was characterized by strong, size-related functional modifications for CO2 acquisition. The adaptive phenotypic variation found between the two ant species indicates the spatially conditioned plasticity of A. mertensii in the context of insect-assisted dispersal. However, ant-mediated effects on phenotypic plasticity in A. mertensii are not obvious because ant species and light environment are confounding variables. © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175, 299–312. ADDITIONAL KEYWORDS: Aechmea mertensii – Camponotus femoratus – French Guiana – leaf traits – mutualistic ants – natural stable isotopes – ontogeny – Pachycondyla goeldii – phenotypic plasticity – plant morphology. INTRODUCTION adult vegetative, and adult reproductive), each char- acterized by morphological, anatomical, and physi- Plant development may be viewed as a succession of ological changes (Poethig, 2003; Barthélémy & different ontogenetic phases (e.g. embryonic, juvenile, Caraglio, 2007). These changes, which are the result of a developmentally programmed growth trajectory, *Corresponding author. E-mail: [email protected] have been referred to as ‘apparent plasticity’ (Weiner, © 2014 The Linnean Society of London, Botanical Journal of the Linnean Society, 2014, 175, 299–312 299 300 M. PETIT ET AL. 2004). For most species, this apparent plasticity is bromeliad, C. femoratus and P. goeldii directly and/or relatively subtle and gradual (‘homoblastic’ species), indirectly influence its vegetative (Leroy et al., 2009a) although there are also species with an abrupt change and reproductive (Leroy et al., 2012) traits by deter- (‘heteroblastic’ species; Leroy & Heuret, 2008; Fadzly mining the location of the seedling, from sun-exposed et al., 2009; Zotz, Wilhelm & Becker, 2011). In Bro- to partially shaded areas, respectively. These studies meliaceae, many epiphytic C3 photosynthetic pathway dealing with mature A. mertensii showed that the tillandsioids are characterized by a conspicuous shift variation in some traits (i.e. the size and shape of the between two (Benzing, 2000; Schmidt & Zotz, 2001; bromeliad) was related to abiotic environmental accli- Zotz et al., 2004) or even three (Meisner & Zotz, 2011) mation processes, whereas others (i.e. leaf thickness, ontogenetic phases. Small juveniles have morphologi- leaf mass area, number of flowers and fruits) were cal characteristics typical of atmospheric tillandsioids related to nutrient-stressed environments linked to (i.e. non-impounding rosettes with small, linear the species of the associated ant. leaves, densely covered by the shields of absorbent Earlier studies conducted on ontogenetic (i.e. plant trichomes), whereas larger bromeliads form tanks or size) or environmental factors (Laube & Zotz, 2003; phytotelmata (i.e. interlocking leaves forming water- Cavallero, Lopez & Barberis, 2009) showed that the filled chambers). This change in life form implies morphological and physiological plasticity of bromeli- morphological, anatomical, and physiological differ- ads can be seen as a result of both ontogeny and ences (Adams & Martin, 1986a, 1986b; Reinert & adaptive plasticity. In the present study, we took Meirelles, 1993; Schmidt & Zotz, 2001). However, advantage of the dispersal of A. mertensii bromeliads recent studies have shown that most of these changes by C. femoratus or P. goeldii in shaded and sunny are more pronounced within a life form than between environments, respectively, to carry out a joint analy- life forms (Schmidt, Stuntz & Zotz, 2001; Schmidt & sis of ontogenetic and habitat effects on phenotypic Zotz, 2001; Zotz et al., 2004; Meisner, Winkler & Zotz, traits in bromeliads. Specifically, we predicted that 2013). the apparent and adaptive plasticity of bromeliads is As a result of a sessile life-style, plants respond to spatially conditioned related to the spatial distribu- different environmental conditions through changes in tion (i.e. shaded or sunny environments) of the plants their phenotypes. Subsequently, plants may show con- by the two ant species. To test this hypothesis, we siderable morphological and physiological variations quantified ontogenetic changes by measuring a set of during their life cycle. Such an ‘adaptive phenotypic key morphological, foliar, and functional traits plasticity’ is rather frequent in tank-bromeliads, which (Table 1) of the tank-bromeliad A. mertensii associ- grow in a broad range of environmental conditions, ated either with C. femoratus or P. goeldii in habitats especially in terms of light environments and flooding ranging from shaded understories to fairly sun- regimes (Lee et al., 1989; Scarano et al., 2002; Freitas, exposed areas. Scarano & Biesboer, 2003), as well as nutrient avail- First, we quantified the effect of ant species and ability (Zotz & Asshoff, 2010; Gonzalez et al., 2011). ontogeny on plant growth and architecture by meas- Besides abiotic factors, biological interactions with uring plant height, plant and tank width, number of other organisms may also play a significant role in leaves, and the longest leaf length. Because mature plant plasticity. For example, herbivory can modify the plants are significantly larger when associated with morphological traits of plants (Agrawal, 1998; C. femoratus-AGs than when associated with P. Ohgushi, 2005; Heil, 2010) and insect-assisted seed goeldii-AGs (Leroy et al., 2009a), we hypothesized dispersal can influence the shape and size of the that growth is higher when A. mertensii is associated associated plants through the distribution of the seed- with the former ant (Table 1). Next, we used foliar ling along gradients of incident light (Leroy et al., traits such as leaf thickness, leaf mass area, total 2009a, 2012). Hence, associations of plants with other water content, and the density of the stomata and organisms that result in predictable spatial distribu- trichomes to quantify the resource-use strategy. Here, tion gradients form particularly
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