Abstract
High mountain ecosystems are subjected to frequent freeze–thaw events all-year round, consequently plants have developed freezing resistance mechanisms to cope with extreme low temperatures. Additionally, these events have also been correlated with the risk of cavitation so that plants need to adapt their water transport system. Information on freezing resistance and xylem vessel characteristics along elevation gradients is scarce for neotropical high elevation species. In this study we aboard two specific questions: 1. Are there intraspecific differences in freezing resistance between low and high elevation populations of Senecio formosus Kunth? 2. Could an increase in freeze–thaw cycle frequency and lower freezing temperatures at higher elevations determine differences in xylem conduit traits between low and high elevation S. formosus populations? We expect greater freezing resistance and a safer water transport system, mainly shaped by narrower tracheary elements in higher elevation populations compared to lower ones. Freezing resistance (avoidance and tolerance) and tracheary elements were studied in S. formosus at its lower (3100 m) and upper (4200 m) distributional limits in the Venezuelan paramo. Freezing resistance was determined through injury and freezing temperature determinations; whereas xylem conduit characteristics dealt with were: vessel element and tracheid diameters, % conducting area and vessel element density. S. formosus increased freezing resistance and presented narrower vessel element diameters under more extreme thermal conditions (4200 m). Increasing evidence of intraspecific plant trait variations under different environmental gradients will aid to determine the outcome of individual species and their effects on ecosystem functioning under a changing climate.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
All data are available if required.
References
Ataroff M (2004) Las unidades ecológicas de los Andes de Venezuela. Reptiles de los Andes de Venezuela. Fundación Polar, Conservation Internacional, CODEPRE-ULA, Fundación Merida. Merida.
Auld J, Everingham SE, Hemmings FA, Moles AT (2022) Alpine plants are on the move: quantifying distribution shifts of Australian alpine plants through time. Divers Distrib 28(5):943–955. https://doi.org/10.1111/ddi.13494
Azócar A, Rada F (2006) Ecofisiología de plantas de páramo. Universidad de Los Andes, Merida, Ediciones ICAE
Briceño B, Morillo G (2002) Catálogo abreviado de las plantas con flores de los páramos de Venezuela. Parte I. Dicotiledóneas (Magnoliopsida). Acta Bot Venez 25(1):1–46
Briceño B, Azócar A, Fariñas M, Rada F (2000) Características anatómicas de dos especies de Lupinus L. de los Andes venezolanos. Pittieria 1(29–30):21–35
Bucher SF, Rosbakh S (2021) Foliar summer frost resistance measured via electrolyte leakage approach as related to plant distribution, community composition and plant traits. Funct Ecol 35:590–600. https://doi.org/10.1111/1365-2435.13740
Carlquist S (1966) Wood anatomy of compositae: a summary, with comments on factors controlling wood evolution. Aliso: J Syst Floristic Bot 6:25–44
Carlquist S (1988) Near-vessellessness in Ephedra and its significance. Am J Bot 75:598–601. https://doi.org/10.1002/j.1537-2197.1988.tb13480.x
Choat B, Medek DE, Stuart SA, Pasquet-Kok J, Egerton JJG, Salari H, Lawren S, Ball MC (2011) Xylem traits mediate a trade-off between resistance to freeze–thaw-induced embolism and photosynthetic capacity in overwintering evergreens. New Phytol 191:996–1005. https://doi.org/10.1111/j.1469-8137.2011.03772.x
Cochard H, Tyree MT (1990) Xylem dysfunction in Quercus: vessel sizes, tyloses, cavitation and seasonal changes in embolism. Tree Physiol 6:393–407. https://doi.org/10.1093/treephys/6.4.393
Davis SD, Sperry JS, Hacke UG (1999) The relationship between xylem conduit diameter and cavitation caused by freezing. Am J Bot 86:1367–1372. https://doi.org/10.2307/2656919
Dória LC, Meijs C, Podadera DS, Del Arco M, Smets E, Delzon S, Lens F (2019) Embolism resistance in stems of herbaceous Brassicaceae and Asteraceae is linked to differences in woodiness and precipitation. Ann Bot 124(1):1–14. https://doi.org/10.1093/aob/mcy233
Fajardo A, Martínez-Pérez C, Cervantes-Alcayde MA, Olson ME (2019) Stem length, not climate, controls vessel diameter in two tree species across a sharp precipitation gradient. New Phytol 225:2347–2355. https://doi.org/10.1111/nph.16287
Fisher JB, Goldstein G, Jones TJ, Cordell S (2007) Wood vessel diameter is related to elevation and genotype in the Hawaiian tree Metrosideros polymorpha (Myrtaceae). Am J Bot 94:709–715. https://doi.org/10.3732/ajb.94.5.709
García-Cervigón AI, Fajardo A, Caetano-Sánchez C, Camarero JJ, Olano JM (2020) Xylem anatomy needs to change, so that conductivity can stay the same: xylem adjustments across elevation and latitude in Nothofagus pumilio. Ann Bot 125:1101–1112. https://doi.org/10.1093/aob/mcaa042
García-Cervigón AI, García-López MA, Pistón N, Pugnaire FI, Olano JM (2021) Co-ordination between xylem anatomy, plant architecture and leaf functional traits in response to abiotic and biotic drivers in a nurse cushion plant. Ann Bot 127(7):919–929. https://doi.org/10.1093/aob/mcab036
Goldstein G, Rada F, Azocar A (1985) Cold hardiness and supercooling along an altitudinal gradient in Andean giant rosette species. Oecologia 68:147–152. https://doi.org/10.1007/BF00379487
Hacke UG, Sperry JS (2001) Functional and ecological xylem anatomy. Perspect Plant Ecol Evol Syst 4(2):97–115. https://doi.org/10.1078/1433-8319-00017
Hacke UG, Sperry JS, Wheeler JK, Castro L (2006) Scaling of angiosperm xylem structure with safety and efficiency. Tree Physiol 26:689–701. https://doi.org/10.1093/treephys/26.6.689
Hacke UG, Spicer R, Schreiber SG, Plavcová L (2017) An ecophysiological and developmental perspective on variation in vessel diameter. Plant Cell Environ 40:831–845. https://doi.org/10.1111/pce.12777
Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol 126:695–705. https://doi.org/10.1111/j.1469-8137.1994.tb02964.x
Hernández-Fuentes C, Bravo LA, Cavieres LA (2015) Conductancia hidráulica foliar y vulnerabilidad a la cavitación disminuyen con la altitud en Phacelia secunda JF Gmel. (Boraginaceae). Gayana Bot 72:84–93
Koide D, Yoshida K, Daehler CC, Mueller-Dombois D (2017) An upward elevation shift of native and non-native vascular plants over 40 years on the island of Hawai’i. J Veg Sci 28(5):939–950. https://doi.org/10.1111/jvs.12549
Körner C (2021) Alpine plant life: functional plant ecology of high mountain ecosystems. Springer Nature, Switzerland. https://doi.org/10.1007/978-3-3030-59538-8
Ladinig U, Hacker J, Neuner G, Wagner J (2013) How endangered is sexual reproduction of high-mountain plants by summer frosts? Frost resistance, frequency of frost events and risk assessment. Oecologia 171:743–760. https://doi.org/10.1007/s00442-012-2581-8
Larcher W, Kainmüller C, Wagner J (2010) Survival types of high mountain plants under extreme temperatures. Flora 205:3–18. https://doi.org/10.1016/j.flora.2008.12.005
Lens F, Tixier A, Cochard H, Sperry JS, Jansen S, Herbette S (2013) Embolism resistance as a key mechanism to understand adaptive plant strategies. Curr Opin Plant Biol 16:287–292. https://doi.org/10.1016/j.pbi.2013.02.005
León-Hernández WJ, Gámez LE (2018) Aspectos ecoanatómicos de ocho especies de Pentacalia Cass.(Asteraceae) de los Andes venezolanos. Pittieria 42:8–21. http://bdigital2.ula.ve:8080/xmlui/654321/1332
Liang Q, Mao X, Wang M, Wang K, ** Z, Liu J (2018) Shifts in plant distributions in response to climate warming in a biodiversity hotspot, the Hengduan Mountains. J Biogeogr 45:1334–1344. https://doi.org/10.1111/jbi.13229
Lindén L (2002) Measuring cold hardiness in woody plants. Dissertation. University of Helsinki, Publication nº 10.
Márquez EJ, Rada F, Fariñas MR (2006) Freezing tolerance in grasses along an altitudinal gradient in the Venezuelan Andes. Oecologia 150:393–397. https://doi.org/10.1007/s00442-006-0556-3
Medeiros JS, Pockman WT (2014) Freezing regime and trade-offs with water transport efficiency generate variation in xylem structure across diploid populations of Larrea sp. (Zygophyllaceae). Am J Bot 101(4):598–607. https://doi.org/10.3732/ajb.1400046
Michaletz ST, Weiser MD, Zhou J, Kaspari M, Helliker BR, Enquist BJ (2015) Plant thermoregulation: energetics, trait–environment interactions, and carbon economics. Trends Ecol Evol 30:714–724. https://doi.org/10.1016/j.tree.2015.09.006
Morales LV, Alvear C, Sanfuentes C, Saldaña A, Sierra-Almeida A (2020) Annual and perennial high-Andes species have a contrasting freezing-resistance mechanism to cope with summer frosts. Alp Bot 130:169–178. https://doi.org/10.1007/s00035-020-00239-2
Morris H, Gillingham MA, Plavcova L, Gleason SM, Olson ME, Coomes DA, Jansen S (2018) Vessel diameter is related to amount and spatial arrangement of axial parenchyma in woody angiosperms. Plant Cell Environ 41:245–260. https://doi.org/10.1111/pce.13091
Morueta-Holme N, Engemann K, Sandoval-Acuña P, Jonas JD, Segnitz RM, Svenning JC (2015) Strong upslope shifts in Chimborazo’s vegetation over two centuries sinceHumboldt. Proc Nat Acad Sci USA 112:12741–12745. https://doi.org/10.1073/pnas.1509938112
Motomura H, Noshiro S, Mikage M (2007) Variable wood formation and adaptation to the alpine environment of ephedra pachyclada (Gnetales: Ephedraceae) in the Mustang District, Western Nepal. Ann Bot 100:315–324. https://doi.org/10.1093/aob/mcm111
Neuner G, Huber B, Plangger A, Pohlin JM, Walde J (2020) Low temperatures at higher elevations require plants to exhibit increased freezing resistance throughout the summer months. Environ Exp Bot 169:103882. https://doi.org/10.1016/j.envexpbot.2019.103882
Noshiro S, Suzuki M (2001) Ontogenetic wood anatomy of tree and subtree species of Nepalese Rhododendron (Ericaceae) and characterization of shrub species. Am J Bot 88:560–569. https://doi.org/10.2307/2657054
Olano JM, Almería I, Eugenio M, von Arx G (2013) Under pressure: how a Mediterranean high-mountain forb coordinates growth and hydraulic xylem anatomy in response to temperature and water constraints. Funct Ecol 27:1295–1303. https://doi.org/10.1111/1365-2435.12144
Olson ME, Rosell JA (2013) Vessel diameter–stem diameter scaling across woody angiosperms and the ecological causes of xylem vessel diameter variation. New Phytol 197:1204–1213. https://doi.org/10.1111/nph.12097
Olson ME, Soriano D, Rosell JA et al (2018) Plant height and hydraulic vulnerability to drought and cold. Proc Natl Acad Sci USA 115:7551–7556. https://doi.org/10.1073/pnas.1721728115
Pandey M, Pathak ML, Shrestha BB (2021) Morphological and wood anatomical traits of Rhododendron lepidotum Wall ex G. Don along the elevation gradients in Nepal Himalayas. Arct Antarct Alp Res 53(1):35–47. https://doi.org/10.1080/15230430.2020.1859719
Percolla MI, Fickle JC, Rodríguez-Zaccaro FD, Pratt RB, Jacobsen AL (2021) Hydraulic function and conduit structure in the xylem of five oak species. IAWA J 42:279–298. https://doi.org/10.1163/22941932-bja10059
Pescador DS, Siera-Almeida Á, Torres PJ, Escudero A (2016) Summer freezing resistance: a critical filter for plant community assemblies in Mediterranean high mountains. Front Plant Sci 7:194. https://doi.org/10.3389/fpls.2016.00194
Pittermann J, Sperry J (2003) Tracheid diameter is the key trait determining the extent of freezing-induced embolism in conifers. Tree Physiol 23:907–914. https://doi.org/10.1093/treephys/23.13.907
Pouchon C, Fernández A, Nassar JM, Boyer F, Aubert S, Lavergne S, Mavárez J (2018) Phylogenomic analysis of the explosive adaptive radiation of the espeletia complex (Asteraceae) in the Tropical Andes. Syst Biol 67:1041–1060. https://doi.org/10.1093/sysbio/syy022
Rada F, Goldstein G, Azócar A, Torres F (1987) Supercooling along an altitudinal gradient in Espeletia schultzii, a caulescent giant rosette species. J Exp Bot 38:491–497. https://doi.org/10.1093/jxb/38.3.491
Rada F, Briceño B, Azócar A (2008) How do two Lupinus species respond to temperature along an altitudinal gradient in the Venezuelan Andes? Rev Chil Hist Nat 81:335–343
Rada F, Azócar A, García-Núñez C (2019) Plant functional diversity in tropical Andean páramos. Plant Ecol Divers 12:539–553. https://doi.org/10.1080/17550874.2019.1674396
Rixen C, Wipf S, Rumpf SB, Giejsztowt J, Millen J, Morgan JW et al (2022) Intraspecific trait variation in alpine plants relates to their elevational distribution. J Ecol 110(4):860–875. https://doi.org/10.1111/1365-2745.13848
Rosbakh S, Margreiter V, Jelcic B (2020) Seedlings of alpine species do not have better frost-tolerance than their lowland counterparts. Alp Bot 130:179–185. https://doi.org/10.1007/s00035-020-00237-4
RStudio Team (2020) RStudio: integrated development for R. RStudio, PBC, Boston
Sakai A, Larcher W (1987) Low temperature and frost as environmental factors In Frost Survival of Plants. Springer, Berlin
Schulze ED, Beck E, Buchmann N, Clemens S, Müller-Hohenstein K, Scherer-Lorenzen M (2019) Plant Ecology. Springer Nature, Berlin. https://doi.org/10.1007/978-3662-56233-8
Sierra-Almeida A, Cavieres LA, Bravo LA (2009) Freezing resistance varies within the growing season and with elevation in high-Andean species of central Chile. New Phytol 182:461–469. https://doi.org/10.1111/j.1469-8137.2008.02756.x
Sklenář P, Kucêrová A, Macek P, Macková J (2012) The frost resistance mechanism in neotropical alpine plants is related to geographic origin. N Zeal J Bot 50:391–400. https://doi.org/10.1080/0028825X.2012.706225
Sklenář P, Hedberg I, Cleef AM (2014) Island biogeography of tropical alpine floras. J Biogeogr 41:287–297. https://doi.org/10.1111/jbi.12212
Sklenář P, Kucêrová A, Macková J, Romoleroux K (2016) Temperature microclimates of plants in tropical alpine environment: how much does growth-form matter? Arct Antarct Alp Res 48:61–78. https://doi.org/10.1657/AAAR0014-084
Soukup A, Pecková E, Ježková B, Sklenář P (2021) Structural adaptations in plants from the humid equatorial Andes indicate a trade-off between hydraulic transport efficiency and safety. Am J Bot 108:2127–2142. https://doi.org/10.1002/ajb2.1799
Spehn, EM, Rudmann-Maurer K, Körner C, Maselli D (2010) Mountain biodiveristy and global change. GMBA-DIVERSITAS. Basel.
Sperry JS, Hacke UG, Pittermann J (2006) Size and function in conifer tracheids and angiosperm vessels. Am J Bot 93:1490–1500. https://doi.org/10.3732/ajb.93.10.1490
Sperry JS, Meinzer FC, McCulloh KA (2008) Safety and efficiency conflicts in hydraulic architecture: scaling from tissues to trees. Plant Cell Environ 31:632–645. https://doi.org/10.1111/j.1365-3040.2007.01765.x
Squeo FA, Rada F, García C, Ponce M, Rojas A, Azócar A (1996) Cold resistance mechanisms in high desert Andean plants. Oecologia 105:552–555. https://doi.org/10.1007/BF00330019
Trew BT, Maclean IM (2021) Vulnerability of global biodiversity hotspots to climate change. Glob Ecol Biogeogr 30(4):768–783. https://doi.org/10.1111/geb.13272
Tyree MT, Ewers FW (1991) The hydraulic architecture of trees and other woody-plants. New Phytol 119:345–360. https://doi.org/10.1111/j.1469-8137.1991.tb00035.x
Vivas Y, Ubiergo P (2010) Asteraceae del valle morrénico de Mucubají, estado Mérida, Venezuela. Rev Fac Agron (LUZ) 27:39–60
von Arx G, Archer SR, Hughes MK (2012) Long-term functional plasticity in plant hydraulic architecture in response to supplemental moisture. Ann Bot 109:1091–1100. https://doi.org/10.1093/aob/mcs030
Zhang SB, Cao KF, Fan ZX, Zhang JL (2013) Potential hydraulic efficiency in angiosperm trees increases with growth-site temperature but has no trade-off with mechanical strength. Glob Ecol Biogeogr 22:971–981. https://doi.org/10.1111/geb.12056
Acknowledgements
This project was funded by the Consejo de Desarrollo Científico, Humanístico, Tecnológico y Arte of the Universidad de Los Andes (ULA, Merida-Venezuela) (Project Nº C-1731-11-01-F). F. Rada is grateful to the Open Society University Network (OSUN) and the Universidad de Los Andes (UniAndes, Bogota-Colombia) for their sponsorship and essential support.
Funding
This work was suported by the Consejo de Desarrollo Científico, Humanístico, Tecnológico y Arte of the Universidad de Los Andes (ULA, Merida-Venezuela) (Project No. C-1731–11-01-F). FR received funding through an Open Society University Network (OSUN) fellowship.
Author information
Authors and Affiliations
Contributions
All authors planned the research and designed the experiments. MA and FR conducted freezing resistance measurements, MA and FE conducted anatomical studies. All authors analyzed the data. FR wrote the original draft, MA and FE reviewed and edited the manuscript.
Corresponding author
Ethics declarations
Competing interest
The authors declare that they have no conflict of interest. Authors have no relevant financial or non-financial interests to disclose.
Additional information
Communicated by Paul Ramsay.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Araujo, M., Rada, F. & Ely, F. Freezing resistance and xylem anatomy in low and high elevation populations of Senecio formosus Kunth in the tropical Andes. Plant Ecol 224, 157–171 (2023). https://doi.org/10.1007/s11258-022-01286-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11258-022-01286-x