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Water Relations of Bromeliaceae in Their Evolutionary Context

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Water Relations of Bromeliaceae in Their Evolutionary Context View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Apollo Botanical Journal of the Linnean Society, 2016, 181, 415–440. With 2 figures Think tank: water relations of Bromeliaceae in their evolutionary context JAMIE MALES* Department of Plant Sciences, University of Cambridge, Downing Street, Cambridge CB2 3EA, UK Received 31 July 2015; revised 28 February 2016; accepted for publication 1 March 2016 Water relations represent a pivotal nexus in plant biology due to the multiplicity of functions affected by water status. Hydraulic properties of plant parts are therefore likely to be relevant to evolutionary trends in many taxa. Bromeliaceae encompass a wealth of morphological, physiological and ecological variations and the geographical and bioclimatic range of the family is also extensive. The diversification of bromeliad lineages is known to be correlated with the origins of a suite of key innovations, many of which relate directly or indirectly to water relations. However, little information is known regarding the role of change in morphoanatomical and hydraulic traits in the evolutionary origins of the classical ecophysiological functional types in Bromeliaceae or how this role relates to the diversification of specific lineages. In this paper, I present a synthesis of the current knowledge on bromeliad water relations and a qualitative model of the evolution of relevant traits in the context of the functional types. I use this model to introduce a manifesto for a new research programme on the integrative biology and evolution of bromeliad water-use strategies. The need for a wide-ranging survey of morphoanatomical and hydraulic traits across Bromeliaceae is stressed, as this would provide extensive insight into structure– function relationships of relevance to the evolutionary history of bromeliads and, more generally, to the evolutionary physiology of flowering plants. © 2016 The Author. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean Society of London., Botanical Journal of the Linnean Society, 2016, 181, 415–440 ADDITIONAL KEYWORDS: adaptive radiation – crassulacean acid metabolism – ecophysiology – epiphytism – functional anatomy – succulence. INTRODUCTION It would be another hundred years before research- ers began exploring in earnest the functional biology When French botanist Antoine de Jussieu in his of bromeliads, but many of them were then drawn to Genera plantarum of 1789 first established the pay special attention to these tanks and other adap- bromeliads as a taxonomic group, he was laying the tations in bromeliad water relations, physiology and modest foundations for over two centuries and ecology (Schimper, 1884, 1888; Mez, 1904; Tietze, recording of research on this fascinating family of 1906; Picado, 1913). monocotyledons. Admittedly, de Jussieu did include Although a few phylogenetic quandaries await reso- among his ‘ordine naturale’ such interlopers as Bur- lution, our understanding of the diversity and phy- mannia L. (Burmanniaceae), Xerophyta Juss. (Vel- logeny of Bromeliaceae is considerably more advanced loziaceae) and Agave L. (Asparagaceae). He also fell than that of de Jussieu. New bromeliad species con- into the popular trap of describing the epiphytic spe- tinue to be discovered (Aguirre-Santoro, Betancur & cies as ‘parasiticæ’. However, one seemingly minor Holst, 2015; Aguirre-Santoro & Michelangeli, 2015; but important observation recorded in de Jussieu’s Buneker€ et al., 2015; Espejo & Lopez-Ferrari, 2015; brief commentary on bromeliads is the presence of Forzza & Leme, 2015; Gonzalez-Rocha et al., 2015; leaves described as ‘vaginantia’ and ‘canaliculata’. Leme, 2015; Monteiro & Forzza, 2015; Ramırez et al., This commentary represents one of the earliest refer- 2015; de Sousa & Wanderley, 2015), but with >3300 ences, albeit oblique, to the water-impounding tanks species already described (Luther, 2012; Govaerts, (phytotelmata) characteristic of so many bromeliads. Luther & Grant, 2013), the discovery of an explana- tion of the drivers and mechanisms of bromeliad diver- *E-mail: [email protected] sification has become one of the overarching aims of © 2016 The Author. Botanical Journal of the Linnean Society published by John Wiley & Sons Ltd on behalf of Linnean 415 Society of London., 2016, 181, 415–440 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. 416 J. MALES research into the family. To this end, well resolved, data would shed light on the coherence and origins time-calibrated multi-locus molecular phylogenetic of the ecophysiological syndromes or functional types trees have been reconstructed, recognizing eight sub- recognized by Pittendrigh (1948), which are closely families: (Brocchinioideae, (Lindmanioideae, (Tilland- connected with water-use strategies. In classifying sioideae, (Hechtioideae, (Navioideae, (Pitcairnioideae, the bromeliad flora of Trinidad, Pittendrigh identi- (Bromelioideae, Puyoideae))))))) (Givnish et al., 2011). fied a series of characteristic functional types: Type I Informative analyses have been conducted to assess Soil-Root; Type II Tank-Root; Type III Tank-Absorb- the impact of putative key innovations on net diversi- ing Trichome; and Type IV Atmosphere-Absorbing fication rates, demonstrating links between the accu- Trichome. Benzing (2000) modified Pittendrigh’s clas- mulation of species richness in specific lineages and sification to separate Tank-Absorbing Trichome characters such as epiphytism, crassulacean acid Bromelioideae and Tillandsioideae into Types III and metabolism (CAM), impounding tanks, entangling IV, respectively, leaving the atmospheric species as seeds and occurrence in moist, fertile habitats in Type V. The splitting of Pittendrigh’s Type III group South American cordilleras (Givnish et al., 2014; Sil- along phylogenetic lines should be subjected to fur- vestro, Zizka & Schulte, 2014). It is important to note ther scrutiny. Analysis of larger comparative eco- that extreme care should be taken when performing physiological datasets will indicate whether the such analyses to use best practice in terms of model phylogenetic distinction is mirrored by a clear diver- calibration and sampling methodology. Quezada & gence in functional type. However, the prevalence of Gianoli (2011) ostensibly recovered CAM as a driver of CAM photosynthesis in Type III species and of C3 diversification in Bromeliaceae, but there were two photosynthesis in Type IV is expected to have impor- fundamental problems with their analysis rendering tant implications for water relations and therefore this result highly questionable. First, the putative Benzing’s scheme is provisionally maintained in this phylogenetic relationships used in this analysis are work. not consistent with those supported by the most com- These functional types represent an evolutionary prehensive molecular phylogenetic analyses. For progression involving decreasing physiological depen- example, the weight of evidence does not support a sis- dence on the substrate, providing access to epiphytic ter-group relationship between Puya Molina and a and lithophytic niche space with reduced interspeci- clade comprising Fascicularia Mez, Ochagavia Phil. fic competition (Pittendrigh, 1948; Givnish et al., and Greigia Regel (Schulte, Barfuss & Zizka, 2009; 1997; Benzing, 2000). Epiphytes account for 56% of Givnish et al., 2011, 2014; Escobedo-Sarti et al., all bromeliad species, such that the family ranks sec- 2013). Second, the character coding fails to capture ond only to Orchidaceae for epiphytic species rich- the complexity of variation in CAM within and ness (Zotz, 2013). The atmospheric Type V species, between lineages. Both Puya and Tillandsia L. are which obtain moisture and nutrients only from direct coded as CAM genera, whereas both are known to or occult precipitation, represent the ultimate include many C3 species and in Puya there are several expression of extreme epiphytism (Schimper, 1888; intermediates (e.g. Herrera et al., 2010; Quezada, Zotz Benzing, 1978; Benzing & Ott, 1981). Characteristic & Gianoli, 2014). A more rigorous analysis by Silve- combinations of innovating traits provide the defini- stro et al. (2014) identified CAM as a driver of diversi- tion of each functional type and its overall water-use fication in Bromelioideae, but it is too facile to assume strategy, but Pittendrigh’s framework could also be this conclusion should apply across the whole family, used to explore the evolution of structure and func- in which 50% of extant species use C3 photosynthesis tion in finer detail. As different lineages have inde- only (Crayn et al., 2015). pendently undergone transitions along the functional A critical dimension of bromeliad biology that has type series, it is interesting to ask whether conver- remained absent from these investigations is the gence in functional type has been achieved through suite of underlying traits pertaining to organismal parallel or alternative changes at the anatomical and and leaf-level anatomical and hydraulic specializa- hydraulic level. tion. These traits undoubtedly make an adaptive con- An improved understanding of the controls on tribution to bromeliad survival in mesic and stressful water fluxes through bromeliads would also be of terrestrial and epiphytic habitats ranging from moist broader relevance and utility, as
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