Velocity of the Falling Dispersal Units in Zelkova Abelicea: Remarkable Evolutionary Conservation Within the Relict Tree Genus
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ORIGINAL ARTICLE Velocity of the falling dispersal units in Zelkova abelicea: remarkable evolutionary conservation within the relict tree genus Daniele Certini1 , Laurence Fazan2, Naomi Nakayama3 , Ignazio Maria Viola1 , and Gregor Kozlowski2,4,5,6 Manuscript received 13 May 2020; revision accepted 14 September PREMISE: Seed dispersal is extremely important for the recovery and restoration of forest 2020. communities. Relict tree genus Zelkova possesses a unique dispersal mechanism: mature 1 School of Engineering, Institute of Energy Systems, University of fruits fall with the entire twig, and the dried leaves that are still attached function as a Edinburgh, Sanderson Building, Robert Stevenson Road, Edinburgh drag-enhancing appendage, carrying the fruits away from the parent tree. This singular EH9 3FB, United Kingdom adaptation has never been investigated in Z. abelicea. 2 Department of Biology and Botanic Garden, Ecology and Evolution, University of Fribourg, Chemin du Musée 10, CH-1700, METHODS: Drop tests with dispersal units and individual fruits of Z. abelicea were Fribourg, Switzerland performed in controlled conditions to measure their dispersal velocity and to define their 3 Department of Bioengineering, Imperial College London, Bessemer flight mode. Building, South Kensington, London SW7 2AZ, United Kingdom 4 Natural History Museum Fribourg, Chemin du Musée 6, CH-1700, RESULTS: Zelkova abelicea uses both slowly falling dispersal units with chaotic motion, as Fribourg, Switzerland well as fast falling individual fruits using a straight path. The falling velocity of Z. abelicea 5 Shanghai Chenshan Plant Science Research Center, Chinese dispersal units is 1.53 m s-1, which is virtually identical to that of the East Asiatic Z. serrata Academy of Sciences, Shanghai Chenshan Botanical Garden, 3888 (1.51 m s-1). In contrast, the falling velocity of individual fruits was 2.74 m s-1 (Z. serrata: 5.36 Chenhua Road, Songjiang, Shanghai 201602, China m s-1). 6Author for correspondence (e-mail: [email protected]) Citation: Certini, D., L. Fazan, N. Nakayama, I. Viola, and G. CONCLUSIONS: Members of the genus Zelkova, growing today in distant regions, show Kozlowski. 2020. Velocity of the falling dispersal units in Zelkova remarkable evolutionary conservation of the velocity and flight mechanics of their abelicea: remarkable evolutionary conservation within the relict tree dispersal units. This is surprising because the Mediterranean and East Asiatic Zelkova genus. American Journal of Botany. 107(12): 1–8. species have been separated at least 15–20 mya. Zelkova abelicea, although growing in the doi:10.1002/ajb2.1581 Mediterranean with completely different forest structure and composition, still uses the same dispersal mechanism. The dispersal capacity of the genus Zelkova is less efficient than that of other wind dispersed trees, and it presumably evolved for short-distance ecological spread and not for long-distance biogeographical dispersal. KEY WORDS Crete; diaspore flight dynamics; relict tree; seed dispersal; terminal velocity; threatened species; Ulmaceae; wind dispersal. Seed dispersal is universally considered extremely important for Oyama et al., 2018b), and it has never been investigated in Z. abeli- metapopulation dynamics and for the recovery and restoration cea (Kozlowski et al., 2018). of Mediterranean forest communities (Trakhtenbrot et al., 2005). Relict tree species of Zelkova were important elements of the Members of the relict tree genus Zelkova (Ulmaceae) possess a vast forests that prevailed throughout the Northern Hemisphere unique dispersal mechanism (referred sometimes as “decurtation”): during much of the Cenozoic Period (Mai, 1995; Fineschi et al., mature fruits fall with the entire twig, and the dried leaves that 2002, 2004). Relicts are remnants of past populations that have are still attached function as a wing-like drag-enhancing append- become fragmented by climate-driven changes and habitat loss age, carrying the fruits away from the parent tree (Kozlowski and (Hampe and Jump, 2011). They were left behind during past range Gratzfeld, 2013). The detachment of the fruiting shoot is not in- shifts and can persist today only in enclaves of benign environmen- cidental but is related to the abscission process, similar to that of tal conditions within an inhospitable regional climate (Woolbright the autumnal shedding of leaves. However, nothing is known about et al., 2014). Currently, the Zelkova genus comprises six extant spe- the anatomy of the abscission zone. Generally, this singular adapta- cies with disjunct distribution patterns (Wu and Raven, 2003; Denk tion of the genus Zelkova has been poorly studied (Hoshino, 1990; and Grimm, 2005; Kozlowski et al., 2018): three in eastern Asia (Z. American Journal of Botany 107(12): 1–8, 2020; http://www.wileyonlinelibrary.com/journal/AJB © 2020 Botanical Society of America • 1 2 • American Journal of Botany serrata, Z. schneideriana and Z. sinica), one in southwestern Asia Mountains (Søndergaard and Egli, 2006). It is currently found in (Z. carpinifolia) and two on the Mediterranean islands of Sicily (Z. scattered and isolated stands within the five main mountain ranges sicula) and Crete (Z. abelicea). of Crete (Lefka Ori, Psiloritis, Kedros, Dikti, and Thripti) distrib- Zelkova abelicea (Lam.) Boiss. is a broadleaved endemic tree of uted from 900 m a.s.l. to the upper tree limit at approximately Crete (Fazan et al., 2012) (Fig. 1). This species was supposedly wide- 1800 m a.s.l. (Egli, 1997; Kozlowski et al., 2014). In some areas, Z. spread in the past and may have formed a forest belt in the Cretan abelicea may form mixed stands with Acer sempervirens, Quercus A B C FIGURE 1. Dispersal units of Zelkova abelicea. (A) Population composed of large and fruiting trees (Dikti Mountains, Crete); (B–C) Closeup showing the morphology and variability of dispersal units used in this study. Scale bars = 10 mm. 2020, Volume 107 • Certini et al.—Dispersal in relict trees • 3 coccifera, and occasionally Cupressus sempervirens. Most fre- We considered the wing loading of the dispersal unit, defined as quently, however, the species has a scattered distribution with few the ratio between its weight (W = mg, where g = 9.81 m s-2) and the to no arborescent individuals in a more or less degraded phrygana leaf surface area S. For the calculation of S, the dispersal units were with numerous dwarfed individuals. placed over a flat surface, and the projected area on the horizontal The species does not tolerate very xeric conditions and is there- plane was measured with a camera and the image processing soft- fore preferentially found on north-facing slopes in and around do- ware Fiji (Schindelin et al., 2012) (Fig. 1, Appendix S1). The length lines where the soil moisture and water supply are most adequate of leaves l was also measured as the maximum Euclidean distance (Egli, 1997; Søndergaard and Egli, 2006). Zelkova abelicea is also between two points of the leaf. The leaf thicknesst was evaluated found growing on scree slopes and around riverbeds that are active with an RS PRO Micrometer External (RS Components Ltd., Corby, only during extreme precipitation events as well as at high eleva- Northants, United Kingdom), with an accuracy of 1 μm. tions on south-facing slopes. It is most frequent in the Lefka Ori and Dikti Mountains, with only one known population in the Psiloritis Drop tests and Thripti Mountains and a very scattered but widespread popula- tion on Mt. Kedros (Egli, 1997; Kozlowski et al., 2018). The species The flight path and terminal velocityw of dispersal units and fruits is listed as endangered in the International Union for Conservation alone were studied by performing drop tests. We used a similar ex- of Nature (IUCN) Red List of Threatened Species (Kozlowski et al., perimental setup in the so-called “dead air space” as described in 2012), is protected under Greek law, and is included in the Bern Oyama et al. (2018b) to avoid the influence of any air movement Convention and in Annexes II and IV of the European Habitats and to better compare both studies. This drop test took place in a Directive (Fournaraki and Thanos, 2006). Pastoral activities pose closed room without windows and minimizing the movements, to the most important threats to the species, as not only browsing by reduce air motion. Testo 405 (Testo Ltd., Alton Hampshire, United goats, but also trampling by numerous sheep or goats prevent seed- Kingdom), a thermal anemometer, was used to ensure the presence lings from establishing and dwarfed shrubs from growing tall and of still air in the region of the experiment, according to Cummins fructifying. et al. (2018) and Murren and Ellison (1998). Testo 405 was placed The aim of our work was to understand the underlying fluid me- on a rod, more than 0.2 m from the vertical axis where the fruit chanics of Z. abelicea dispersal units. More specifically, we aimed was falling and far from the ground. Dispersal units (n = 32) and to answer the following questions: (1) What is the falling velocity fruits removed from the dispersal units (n = 27) were dropped three of the dispersal units in comparison with solitary fruits of Z. abeli- times, with zero initial velocity from a height of 1.8 m in quiescent cea? (2) What is the velocity of the dispersal units of Z. abelicea in air, to record a complete fall over 1 m, at a distance of 1 m from comparison with other Zelkova species and other wind dispersed the camera. The 95% confidence intervals were calculated using bi- plants? (3) What is the flight mode of the dispersal units? Finally, we as-corrected and accelerated bootstrapping. discuss the implications of our findings to understand the ecology The fall occurred in the focal plane of the camera at a distance of Z. abelicea and the implications for conservation of this endan- greater than 200 mm from every solid boundary to avoid wall ef- gered relict tree.