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Palm snorkelling: leaf bases as aeration structures in the mangrove palm (Nypa fruticans) G. Chomicki, Luc Bidel, William. J. Baker, Christian Jay-Allemand To cite this version: G. Chomicki, Luc Bidel, William. J. Baker, Christian Jay-Allemand. Palm snorkelling: leaf bases as aeration structures in the mangrove palm (Nypa fruticans). Botanical Journal of the Linnean Society, Linnean Society of London, 2014, 174 (2), pp.257-270. 10.1111/boj.12133. hal-01189916 HAL Id: hal-01189916 https://hal.archives-ouvertes.fr/hal-01189916 Submitted on 27 May 2020 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. Botanical Journal of the Linnean Society, 2013, ••, ••–••. With 8 figures Palm snorkelling: leaf bases as aeration structures in the mangrove palm (Nypa fruticans) GUILLAUME CHOMICKI FLS1*, LUC P. R. BIDEL2, WILLIAM J. BAKER FLS3 and CHRISTIAN JAY-ALLEMAND4 1Systematic Botany and Mycology, Department of Biology, University of Munich (LMU), Munich 80638, Germany 1 2INRA Montpellier, UMR AGAP, Montpellier, France bs_bs_query 3Royal Botanic Gardens, Kew, Richmond, Surrey, TW9 3AB, UK 2 4University of Montpellier 2, UMR DIADE, Place Eugène Bataillon, F-34 095, Montpellier, France bs_bs_query Received 31 July 2013; revised 28 October 2013; accepted for publication 29 October 2013 Mangrove species have evolved specialized structures, such as pneumatophores, to supply oxygen to the roots, but, in Nypa fruticans, the only mangrove palm, no such structure has been reported. This study aimed to determine the adaptations of N. fruticans to the mangal habitat with special reference to the air-supplying structure. Following senescence, the rachis is abscised at the zone of junction with the leaf base. Simultaneously, lenticels develop so that, when abscission is completed, a network of mature lenticels covers the leaf base. Expansigenous aerenchyma with increasing porosity towards the stem junction occurs in the leaf base. The first two root branching orders present a subero-lignified rhizodermis and exodermis, and the cortex consists of schizo-lysigenous aerenchyma with wide lacuna, limiting radial oxygen loss and facilitating longitudinal oxygen transport to living tissues. Lifespan estimation suggests that leaf bases can live for up to 4 years following abscission, ensuring the persistence of aeration structures. This study provides structural evidence indicating that N. fruticans has evolved a unique type of air-supplying structure in the mangal habitat. © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, 00, 000–000. Version preprint ADDITIONAL KEYWORDS: aerenchyma – Arecaceae – expansigeny – hypertrophic lenticel – leaf lifespan – Palmae – rachis abscission – root oxygen supply – schizo-lysigeny – tannins. INTRODUCTION known as stilt roots, such as in Rhizophora stylosa Griff, knee roots [e.g. Bruguiera gymnorrhiza (L.) The success of mangrove species in waterlogged, and Lamk.], buttress roots, such as those of Heritiera therefore anoxic and highly reduced, environments is littoralis Aiton, or sinuous buttresses, so-called plank classically attributed to the remarkable morphologi- roots, of Xylocarpus granatum Ridl. (Saenger, 1982; cal adaptations of their root systems (Scholander, Van Tomlinson, 1995). All of these structures possess high Dam & Scholander, 1955; Tomlinson, 1995). These densities of lenticels, which enable gas transfer whilst typically aerial root adaptations include pneumato- preventing water entry (Tomlinson, 1995). In man- phores [e.g. Avicennia marina (Forsk.) Vierh.], adven- grove species, it has long been assumed that such titious aerial roots that can emerge ectopically from adaptive root systems enable oxygen transport to high branches, such as in the red mangle (Rhizophora drowned tissues, hence ensuring aerobic metabolism mangle L.), or form a cluster at the base of the trunk, in an anaerobic environment (Scholander et al., 1955; Saenger, 1982; Tomlinson, 1995). Beyond the morphological adaptations of man- 1bs_bs_query grove root systems, the key anatomical trait that 2bs_bs_query *Corresponding author. E-mail: enables tolerance to inundation and soil anoxia is the 3bs_bs_query [email protected]; 4bs_bs_query [email protected] formation of aerenchyma with interconnected air © 2013 The Linnean Society of London, Botanical Journal of the Linnean Society, 2013, ••, ••–•• 1 Comment citer ce document : Chomicki, G. (Auteur de correspondance), Bidel, L., Baker, W. J., Jay-Allemand, C. (2014). Palm snorkelling: leaf bases as aeration structures in the mangrove palm (Nypa fruticans). Botanical Journal of the Linnean Society, 174 (2), 257-270. DOI : 10.1111/boj.12133 2 G. CHOMICKI ET AL. 1bs_bs_query channel systems throughout the plant. Consistently, in turn, allows vegetative colonization (Tomlinson, 57bs_bs_query 2bs_bs_query an increase in tissue porosity and the formation of air 1971, 1995; Fig. 1). One remarkable adaptation of 58bs_bs_query 3bs_bs_query channels are pivotal to increase the rate of oxygen Nypa to the mangal habitat is the viviparous seed- 59bs_bs_query 4bs_bs_query diffusion in plant tissues (Arber, 1920; Armstrong, lings which germinate following seed maturation, 60bs_bs_query 5bs_bs_query 1979). Aerenchyma types fall into three main catego- before being shed from the fruiting head that termi- 61bs_bs_query 6bs_bs_query ries according to the mode of development: lysigeny, nates the inflorescence (Tomlinson, 1971, Fig. 1C). As 62bs_bs_query 7bs_bs_query schizogeny and expansigeny (Seago et al., 2005). In a result of the plagiotropic habit of Nypa and tides, its 63bs_bs_query 8bs_bs_query lysigenous aerenchyma, the air lacunae arise from stem is often immersed, the leaves being the only 64bs_bs_query 9bs_bs_query cell lysis and collapse, whereas, in schizogenous aer- emergent part of the plant (Fig. 1). Nypa does not 65bs_bs_query 10bs_bs_query enchyma, cell separation of adjacent cell layers produce breathing roots like many other mangrove 66bs_bs_query 11 bs_bs_query occurs, resulting in the joining of intercellular spaces species, including some palm species living as mangal 67bs_bs_query 12bs_bs_query into lacunae. Expansigeny is somewhat different from associates in wet habitats, which develop thin 68bs_bs_query 13bs_bs_query these two processes in that it involves the enlarge- pneumatophores (Tomlinson, 1995). Thus, the air- 69bs_bs_query 14bs_bs_query ment of intercellular spaces by cell division and supplying structures should be the leaves, as they are 70bs_bs_query 15bs_bs_query expansion, but not by cell death, collapse or separa- the only emergent part of the plant. Tomlinson (1995: 71bs_bs_query 16bs_bs_query tion (Seago et al., 2005). 105) hypothesized that Nypa leaves play the role of a 72bs_bs_query 17bs_bs_query Aerenchyma structure and development have been ‘giant pneumatophore’, based on their spongy texture 73bs_bs_query 18bs_bs_query described in detail for several mangrove species, and that of the rhizome ground tissue, and further 74bs_bs_query 19bs_bs_query 3 including Rhizophora mangle (Gill and Tomlinson, suggested that this role may continue in the leaf 75bs_bs_query bs_bs_query 20bs_bs_query 4 1977) and Avicennia marina (Purnobasuki and base, noting that they break at an apparently similar 76bs_bs_query bs_bs_query 21bs_bs_query Suzuki, 2005). Moreover, in mangrove species, the position. 77bs_bs_query 22bs_bs_query pattern of oxygenation of the root system is depend- In this study, we explore the role of the Nypa leaf in 78bs_bs_query 23bs_bs_query ent upon tides, with oxygen concentration peaking at the mangrove habit. We show that leaves of N. fruti- 79bs_bs_query 24bs_bs_query low tides (Scholander et al., 1955; Allaway et al., cans follow a distinctive developmental path, whereby 80bs_bs_query 25bs_bs_query 2001). the distal part of older leaves abscises, leaving 81bs_bs_query 26bs_bs_query Nypa fruticans Wurmb. is the only extant mangrove behind persistent leaf bases that have attributes of 82bs_bs_query 27bs_bs_query palm, and is distributed from India and Sri Lanka in pneumatophore-like aeration structures. This indi- 83bs_bs_query 28bs_bs_query the west through South-East Asia to Australia and cates that N. fruticans has evolved an air-supplying 84bs_bs_query 29bs_bs_query the Solomon Islands (Dransfield et al., 2008). Nypa structure that is unique among mangrove species. 85bs_bs_query 30bs_bs_query Steck is a monotypic genus that arose as an early 86bs_bs_query 31bs_bs_query diverging lineage near the base of the palm phylogeny MATERIAL AND METHODS 87bs_bs_query 32bs_bs_query (Asmussen et al., 2006; Baker et al., 2009), dated at bs_bs_query 33bs_bs_query 93.5 Mya (Baker & Couvreur, 2013). PLANT MATERIAL 88 Version preprint 34bs_bs_query Nypa has an extensive fossil record dating back to Plant material was collected from a mature specimen 89bs_bs_query 35bs_bs_query the upper Cretaceous (Maastrichtian) (Tralau, 1964; of N. fruticans growing at the Montgomery Botanical 90bs_bs_query 36bs_bs_query Morley, 2000; Gee,

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