Journal of Ecology and Environment

The Ecological Society of Korea (한국생태학회)
권호 표지
DOI QR코드

DOI QR Code

Comparison of ecophysiological and leaf anatomical traits of native and invasive plant species

  • Rindyastuti, Ridesti (Purwodadi Botanic Garden, Research Center for Plant Conservation and Botanic Gardens, Indonesian Institute of Sciences) ;
  • Hapsari, Lia (Purwodadi Botanic Garden, Research Center for Plant Conservation and Botanic Gardens, Indonesian Institute of Sciences) ;
  • Byun, Chaeho (Department of Biological Sciences and Biotechnology, College of Life Sciences & Biotechnology, Andong National University)
  • Received : 2020.09.07
  • Accepted : 2020.11.26
  • Published : 2021.03.31
Download PDF
⟨ Previous Next ⟩

Abstract

Background: To address the lack of evidence supporting invasion by three invasive plant species (Imperata cylindrica, Lantana camara, and Chromolaena odorata) in tropical ecosystems, we compared the ecophysiological and leaf anatomical traits of these three invasive alien species with those of species native to Sempu Island, Indonesia. Data on four plant traits were obtained from the TRY Plant Trait Database, and leaf anatomical traits were measured using transverse leaf sections. Results: Two ecophysiological traits including specific leaf area (SLA) and seed dry weight showed significant association with plant invasion in the Sempu Island Nature Reserve. Invasive species showed higher SLA and lower seed dry weight than non-invasive species. Moreover, invasive species showed superior leaf anatomical traits including sclerenchymatous tissue thickness, vascular bundle area, chlorophyll content, and bundle sheath area. Principal component analysis (PCA) showed that leaf anatomical traits strongly influenced with cumulative variances (100% in grass and 88.92% in shrubs), where I. cylindrica and C. odorata outperformed non-invasive species in these traits. Conclusions: These data suggest that the traits studied are important for plant invasiveness since ecophysiological traits influence of light capture, plant growth, and reproduction while leaf anatomical traits affect herbivory, photosynthetic assimilate transport, and photosynthetic activity.

Keywords

References

  1. Bajwa AA, Chauhan BS, Farooq M, Shabbir A, Adkins SW. What do we really know about alien plant invasion? A review of the invasion mechanism of one of the world's worst weeds. Planta. 2016;244:39-57. https://doi.org/10.1007/s00425-016-2510-x
  2. Banovetz SJ, Scheiner SM. The effect of seed mass on the seed ecology of Coreopsis lanceolata. Am Midl Nat. 1994;131(1):65-74. https://doi.org/10.2307/2426609
  3. Baruch Z, Goldstein G. Leaf construction cost, nutrient concentration, and net CO2 assimilation of native and invasive species in Hawaii. Oecologia. 1999;121:183-92. https://doi.org/10.1007/s004420050920
  4. Brantley ST, Young DR. Linking light attenuation, sunflecks, and canopy architecture in mesic shrub thickets. Plant Ecol. 2009;206:225-36. https://doi.org/10.1007/s11258-009-9637-9
  5. Brym ZT, Lake JK, Allen D, Ostling A. Plant functional traits suggest novel ecological strategy for an invasive shrub in an understory woody plant community. J Appl Ecol. 2011;48:1098-106. https://doi.org/10.1111/j.1365-2664.2011.02049.x
  6. Burns JH, Winn AA. A comparison of plastic responses to competition by invasive and non-invasive congeners in the Commelinaceae. Biol Invasions. 2006;8:797-807. https://doi.org/10.1007/s10530-005-3838-5
  7. Calado H, Fonseca C, Vergilio M, Costa A, Moniz F, Gil A, Dias JA. Small islands conservation and protected areas. J Integr Coast Zone Manag. 2014;14(2):167-74.
  8. CBD (Convention on Biological Diversity). Invasive alien species. www.cbd.int/invasive. 2010. Accessed 2 May 2018.
  9. Daehler CC. Performance comparison of co-occuring native and alien invasive plants: implications for conservation and restoration. Ann Rev Ecol Evol Syst. 2003;34:183-211. https://doi.org/10.1146/annurev.ecolsys.34.011802.132403
  10. Dozier H, Gaffney JF, McDonald SK, Johnson ERRL, Shilling DG. Cogongrass in the United States: History, ecology, impacts, and management. Weed Technol. 1998;12:737-43. https://doi.org/10.1017/S0890037X0004464X
  11. Drenovsky RE, Grewell BJ, D'Antonio CM, Funk JL, James JJ, Molinari N, Parker IM, Richards CL. A functional trait perspective on plant invasion. Ann Bot. 2012;110:141-53. https://doi.org/10.1093/aob/mcs100
  12. Fahn A. Plant anatomy. 3rd ed. Oxford: Pergamon Press; 1982.
  13. Farnsworth EJ, Meyerson LA. Comparative ecophysiology of four wetland plant species along a continuum of invasiveness. Wetlands. 2003;23(4):750-62. https://doi.org/10.1672/0277-5212(2003)023[0750:CEOFWP]2.0.CO;2
  14. Fenner M. Seed ecology: Chapman and Hall Ltd.; 1985. p. 2-10.
  15. Foloruso AE, Awosode OD. Comparative anatomy of invasive and non-invasive species in the family Asteraceae in Nigeria. Int J Biol Chem Sci. 2013;7(5):1804-19. https://doi.org/10.4314/ijbcs.v7i5.2
  16. Gallagher RV, Randall RP, Leishman MR. Trait differences between naturalized and invasive plant species independent of residence time and phylogeny. Conserv Biol. 2014;29(2):360-9. https://doi.org/10.1111/cobi.12399
  17. Global Invasive Species Database (GISD). Species profile Chromolaena odorata. 2015. Available from: http://www.iucngisd.org/gisd/species.php?sc=47. Accessed 2 Dec 2019.
  18. Graebner RC, Callaway RM, Montesinos D. Invasive species grows faster, competes better, and shows greater evolution toward increased seed size and growth than exotic non-invasive congeners. Plant Ecol. 2012;213:545-53. https://doi.org/10.1007/s11258-012-0020-x
  19. Greene DF, Johnson EA. Seed mass and dispersal capacity in wind-dispersed diaspores. Oikos. 1993;67:69-74. https://doi.org/10.2307/3545096
  20. Grime JP. The C-S-R model of primary plant strategies-origins, implications and tests. In: Gottlieb LD, Jain SK, editors. Plant Evolutionary Biology. Dordrecht: Springer; 1988; https://doi.org/10.1007/978-94-009-1207-6_14.
  21. Grotkopp E, Rejmánek M. High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot. 2007;94(4):526-32. https://doi.org/10.3732/ajb.94.4.526
  22. Grotkopp E, Rejmanek M, Rost TL. Toward a causal explanation of plant invasiveness: seedling growth and life‐history strategies of 29 Pine (Pinus) Species. Am Nat. 2002;159(4):396-419. https://doi.org/10.2307/3079249
  23. Hakim L, Leksono AS, Purwaningtyas D, Nakagoshi N. Invasive plant species and the competitiveness of wildlife tourist destination: a case of Sadengan Feeding Area at Alas Purwo National Park, Indonesia. J Intl Dev Coop. 2005;12(1):35-45.
  24. Hameed M, Ashraf M. Anatomical adaptation to salinity in cogon grass (Imperata cylindrica (L). Raeuschel) from the Salt Range, Pakistan. Plant Soil. 2009;322:229-38. https://doi.org/10.1007/s11104-009-9911-6
  25. Hamilton MA, Murray BR, Cadotte MW, Hose GC, Baker AC, Harris CJ, Licari D. Life-history correlates of plant invasiveness at regional and continental scales. Ecol Lett. 2005;8:1066-74. https://doi.org/10.1111/j.1461-0248.2005.00809.x
  26. Hammer O, Harper DAT, Ryan PD. Past: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4(1):9.
  27. Hapsari L, Abywijaya IK, Nurfadilah S, Rindyastuti R. Diversity and ecology of understory plant in Sempu Island, East Java, Indonesia. Biotropia 2020;27(3):222-37.
  28. Hapsari L, Basith A, Novitasiah HR. Inventory of invasive plant species along the corridor of Kawah Ijen Nature Tourism Park, Banyuwangi, East Java. J. Indones Tour Dev Stud. 2014;2(1):1-9. https://doi.org/10.21776/ub.jitode.2014.002.01.01
  29. Hodkinson DJ, Askew AP, Thompson K, Hodgson JG, Bakker JP, Bakker RM. Ecological correlates of seed size in the British flora. Funct Ecol. 2002;12(5):762-6. https://doi.org/10.1046/j.1365-2435.1998.00256.x
  30. Holzmueller EJ, Jose S. Invasion success of cogon grass, an alien C4 perennial grass, in the southeastern United States: exploration of the ecological basis. Biol Invasion. 2010;13(2):435-42. https://doi.org/10.1007/s10530-010-9837-1
  31. James JJ, Drenovsky RE. A basis for relative growth rate differences between native and invasive forb seedlings. Rangel Ecol Manag. 2007;60(4):395-400. https://doi.org/10.2111/1551-5028(2007)60[395:ABFRGR]2.0.CO;2
  32. Junaedi DI, Dodo. Exotic plants in Halimun Salak corridor: micro-environment, detection and risk analysis of invasive plants. Biotropia. 2014;21(1):38-52.
  33. Kattge J, Diaz S, Lavorel S, Prentice IC, et al. TRY-a global database of plant traits. Glob Change Biol. 2011;17(9):2905-35. https://doi.org/10.1111/j.1365-2486.2011.02451.x
  34. Kudo Y, Mutaqien Z, Simbolon H, Suzuki E. Spread of invasive plants along trails in two national parks in West Java, Indonesia. Tropics. 2014;23(3):99-110. https://doi.org/10.3759/tropics.23.99
  35. Lack AJ, Evans DE. Instant notes of plant biology. Oxford: BIOS Scientific Publishers Limited; 2001.
  36. Lambers H, Poorter H. Inherent variation in growth rate between higher plants: a search for physiological causes and ecological consequenses. Adv Ecol Res. 1992;23:187-261. https://doi.org/10.1016/S0065-2504(08)60148-8
  37. Lambers H, Chapin FS, Pons TL. Plant physiological ecology. New York: Spinger-Verlag; 1998. p. 299-322.
  38. Leishman MR, Haslehurst T, Ares A, Baruch Z. Leaf trait relationships of native and invasive plants: community- and global-scale comparisons. New Phytol. 2007;176:635-43. https://doi.org/10.1111/j.1469-8137.2007.02189.x
  39. Liao Z-Y, Scheepens JF, W-Tao L, Fang WR, Y-Long Z, Y-Long F. Biomass reallocation and increased plasticity might contribute to successful invasion of Chromolaena odorata, Flora; 2019. https://doi.org/10.1016/j.flora.2019.05.004.
  40. Lowe S, Browne M, Boudjelas S, De Poorter M. 100 of the world's worst invasive alien species. A selection from the global invasive species database. Published by The Invasive Species Specialist Group (ISSG) a specialist group of the Species Survival Commission (SSC) of the World Conservation Union (IUCN); 2000. p. 12. First published as special lift-out in Aliens 12, December 2000. Updated and reprinted version: November 2004.
  41. MacDonald GE. Cogongrass (Imperata cylindrica)-biology, ecology, and management. Critical Rev Plant Sci. 2004;23(5):367-80. https://doi.org/10.1080/07352680490505114
  42. Marchante H, Freitas H, Hoffmann J. Seed ecology of an invasive alien species, Acacia Longifolia (Fabaceae), in Portuguese dune ecosystems. Am J Bot. 2010;97(11):1780-90. https://doi.org/10.3732/ajb.1000091
  43. Maschinski J. Impacts of ungulate herbivores on a rare willow at the southern edge of its range. Biol Conserv. 2001;101:119-30. https://doi.org/10.1016/S0006-3207(01)00029-5
  44. Mcalpine KG, Jesson LK, Kubien DS. Photosynthesis and water-use efficiency: a comparison between invasive (exotic) and non-invasive (native) species. Austral Ecol. 2008;33:10-9. https://doi.org/10.1111/j.1442-9993.2007.01784.x
  45. McDowell SCL. Photosynthetic characteristics of invasive and noninvasive species of Rubus (Rosaceae). Am J Bot. 2002;89:1431-8. https://doi.org/10.3732/ajb.89.9.1431
  46. Moles AT, Warton DI, Warman L, Swenson NG, Laffan SW, Zanne AE, Pitman A, Hemmings FA, Leishman MR. Global patterns in plant height. J Ecol. 2009;97:923-32. https://doi.org/10.1111/j.1365-2745.2009.01526.x
  47. Moodley D, Geerts S, Richardson DM, Wilson JRU. Different traits determine introduction, naturalization and invasion success in woody plants: Proteaceae as a test case. PLoS One. 2013;8(9):e75078. https://doi.org/10.1371/journal.pone.0075078
  48. Moravcova L, Pysek P, Jarosik V, Pergl J. Getting the right traits: reproductive and dispersal characteristics predict the invasiveness of herbaceous plant species. PLoS One. 2015;10(4):e0123634. https://doi.org/10.1371/journal.pone.0123634
  49. Morris TL, Esler KJ, Barger NN, Jacobs SM, Cramer MD. Ecophysiological traits associated with the competitive ability of invasive Australians Acacia. Divers Distrib. 2011;17:898-910. https://doi.org/10.1111/j.1472-4642.2011.00802.x
  50. Muniappan R, Reddy GVP, Raman A. Biological control of tropical weeds using arthropods. USA: Cambridge University press; 2009. p. 130-40.
  51. Nagaraj N, Reese JC, Kirkham MB, Kofoid K, Campbell LR, Loughin TM. Relationship between chlorophyll loss and photosynthetic rate in Greenbug (Homoptera) damaged sorghum. J Kansas Entomol Soc. 2002;75(2):101-9.
  52. Namagada M, Krekling T, Lye KA. Leaf anatomical characteristics of Ugandan species of Festuca L. (Poaceae). S Afr J Bot. 2009;75:52-9. https://doi.org/10.1016/j.sajb.2008.07.004
  53. Nurse LA, Sem G, Hay JE, Suarez AG, Wong PP, Briguglio L, Ragoonaden S. Small island states. Climate change 2001: impacts, adaptation, and vulnerability. Cambridge: Cambridge University Press; 2001.
  54. Pattinson RR, Goldstein G, Ares A. Growth, biomass allocation and photosynthesis of invasive and native Hawaian rainforest species. Oecologia. 1998;117(4):449-59. https://doi.org/10.1007/s004420050680
  55. Perez-Harguindeguy N, et al. New handbook for standardize measurement of plant functional traits worldwide. Aust J Bot. 2013;61:167-234. https://doi.org/10.1071/BT12225
  56. Poorter H, Remkes C. Leaf area ratio and net assimilation rate of 24 wild species differing in relative growth rate. Oecologia. 1990;83:553-9. https://doi.org/10.1007/BF00317209
  57. Priyanka N, Joshi PK. A review of Lantana camara studies in India. Int J Sci Res Publ. 2013;3(10):1-11.
  58. Pugnaire IF, Valladares F. Handbook of functional plant ecology. New York: Marcel Dekker, Inc.; 1999. p. 81-121.
  59. Quan GM, Mao DJ, Zhang JE, Xie JF, Xu HQ, An M. Response of invasive Chromolaena odorata and two coexisting weeds to contrasting irradiance and nitrogen. Photosynthetica. 2015;53:419-29. https://doi.org/10.1007/s11099-015-0137-y
  60. Rejmanek M. What makes species invasive. In: Pysek, Prach K, Rejmanek M, Wade M, editors. Plant invasions-general aspects and special problems. Amsterdam: Academic Publishing; 1995.
  61. Rejmanek M. A theory of seed plant invasiveness: the first sketch. Biol Conserv. 1996;78:171-81. https://doi.org/10.1016/0006-3207(96)00026-2
  62. Rejmanek M, Richardson DM. What attributes make some plant species more invasive? Ecology. 1996;77:1655-166. https://doi.org/10.2307/2265768
  63. Rindyastuti R, Sancayaningsih RP. The growth strategies analysis of ten woody plant species for effective revegetation. Biotropia. 2018;25(1):43-55.
  64. Rindyastuti R, Abywijaya IK, Rahadiantoro A, Irawanto R, et al. Keanekaragaman Tumbuhan Pulau Sempu dan Ekosistemnya. Jakarta: LIPI Press. [Indonesian]; 2018a.
  65. Rindyastuti R, Rachmawati D, Sancayaningsih RP, Yulistyarini T. Ecophysiological and growth characters of ten woody plant species in determining their carbon sequestration. Biodiversitas. 2018b;19(2):610-9. https://doi.org/10.13057/biodiv/d190238
  66. Riveron-Giro FB, Damon AD, Garcia-Gonzalez A, Solis-Montero L, Aguilar-Romero O, Ramirez-Marcial N, Nieto G. Anatomy of the invasive orchid Oeceoclades maculata: ecological implications. Bot J Linnean Soc. 2017;184:94-112. https://doi.org/10.1093/botlinnean/box014
  67. Roger D. Invasive alien species: global perspectives. In: Proceedings of the national workshop on invasive alien species, 20 October 2003, Kuala Lumpur: Organized by the Department of Agriculture, Ministry of Agriculture, Malaysia in collaboration with ASEANET and CAB International - SEA Regional Office; 2003.
  68. Sarijeva G, Knapp M, Lichtenthaler HK. Differences in photosynthetic activity, chlorophyll and carotenoid levels, and in chlorophyll fluorescence parameters in green sun and shade leaves in Ginkgo and Fagus. J Plant Physiol. 2007;164:950-5. https://doi.org/10.1016/j.jplph.2006.09.002
  69. Shipley B. Trade-offs between net assimilation rate and specific leaf area and determining relative growth rate: relationship with daily irradiance. Funct Ecol. 2002;16:682-98. https://doi.org/10.1046/j.1365-2435.2002.00672.x
  70. Sukistyanawati A, Pramono H, Suseno B, Cahyono H, Andriyono S. Wild animals inventarisation in Sempu Island Nature Reserve. Jurnal Ilmiah Perikanan dan Kelautan. 2016;8(1):26-35 [Indonesian]. https://doi.org/10.20473/jipk.v8i1.11188
  71. Sutomo E, van Etten, Wahab L. Proof of Acacia nilotica stand expansion in Bekol Savanna, Baluran National Park, East Java, Indonesia through remote sensing and field observations. Biodiversitas. 2016;17(1):96-101.
  72. Thompson K, Band SR, Hodgson JG. Seed size and shape predict persistence in soil. Funct Ecol. 1993;7:236. https://doi.org/10.2307/2389893
  73. Thomson FJ, Moles AT, Auld TD, Kingsford RT. Seed dispersal distance is more strongly correlated with plant height than with seed mass. J Ecol. 2011;99:1299-307. https://doi.org/10.1111/j.1365-2745.2011.01867.x
  74. Tjitrosoedirdjo SS. Inventory of the invasive alien plant species in Indonesia. Biotropia. 2005;25:60-73.
  75. Tjitrosoedirdjo SS, Mawardi I, Tjitrosoedirdjo S. 75 important invasive plant species in Indonesia: SEAMEO BIOTROP Southeast Asian Regional Centre for Tropical Biology; 2016. p. 115. https://biotrop.org/publication/show/75-important-invasive-alien-plant-species-in-indonesia.
  76. Trimanto, Hapsari L. Botanical survey in thirteen montane forests of Bawean Island Nature Reserve, East Java Indonesia: Flora diversity, conservation status, and bioprospecting. Biodiversitas. 2016;17(2):832-46.
  77. USDA National Resource Conservation Service: Plant Database. http://plants.usda.gov/java/. Accessed 12 Oct 2012.
  78. Van Kleunen M, Weber E, Fischer M. A meta-analysis of trait differences between invasive and non-invasive plant species. Ecol Lett. 2010;13:235-45. https://doi.org/10.1111/j.1461-0248.2009.01418.x
  79. Vanderwoude C, Scanlan JC, Davis B, Funkhouser S. Plan for national delimiting survey for Siam weed. Queensland Government: Natural Resources and Mines Land Protection Services; 2005.
  80. Wang C, Liu J, Xiao H, Zhou J. Differences in leaf functional traits between Rhus typhina and native species. Clean Soil Air Water. 2016;44(11):1591-7. https://doi.org/10.1002/clen.201600144
  81. Weber E. Invasive plant species of the world. A reference guide to environmental weeds. Wallingford: CABI Publishing; 2003.
  82. Westoby M. A leaf-height-seed (lhs) plant ecology strategy scheme. Plant Soil. 1998;199:213-27. https://doi.org/10.1023/A:1004327224729
  83. Westoby M, Jurado E, Leishman M. Comparative evolutionary ecology of seed size. Trends Ecol Evol. 1992;7:368-72. https://doi.org/10.1016/0169-5347(92)90006-W
  84. Witkowski ETF, Wilson M. Changes in density, biomass, seed production and soil seed banks of the non-native invasive plant, Chromolaena odorata, along a 15 year chronosequence. Plant Ecol. 2001;152:13-27. https://doi.org/10.1023/A:1011409004004