Abstract
Phenology expresses strategies related to resource use and can play an important role in the success of invasive plants. Araucaria forests are highly fragmented ecosystems that are increasingly impacted by invasive plants, such as Ligustrum lucidum (Oleaceae). The present study aimed to describe the phenological events of L. lucidum; identify the influence climate has on its phenophases; and compare reproductive phenophases between L. lucidum and that of Araucaria forest. The phenological study was conducted over the course of 24 months, with the intensity of each phenophase being evaluated by the Fournier Index. Ligustrum lucidum exhibited phenophases throughout the entire year in Araucaria forest, all of which exhibited a seasonal pattern except for leaf fall. The same pattern was observed for the species in its native area. Day length was the best predictor of the phenology of L. lucidum. The reproductive phenology of L. lucidum differed from that of Araucaria forest, especially with regard to fruiting. The influence of day length on the phenophases of L. lucidum seems to be part of a strategy for efficient resource acquisition and allocation. The competitive advantage of L. lucidum in Araucaria forest may be due to the maintenance of its climatic niche, which gives it a different reproductive phenology in comparison to native species. The present study shows how phenology can play an important role in the invasion process and highlights the importance of creating management strategies to avoid the spread of L. lucidum in the already threatened Araucaria forest ecosystem.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aguirre-Acosta N, Kowaljow E, Aguilar R (2014) Reproductive performance of the invasive tree Ligustrum lucidum in a subtropical dry forest: does habitat fragmentation boost or limit invasion? Biol Invasions 16:1397–1410. https://doi.org/10.1007/s10530-013-0577-x
Aragón R, Groom M (2003) Invasion by Ligustrum lucidum in NW Argentina: plant characteristics in different habitats. Rev Biol Trop 51:59–70
Aslan CE (2011) Implications of newly-formed seed-dispersal mutualisms between birds and introduced plants in northern California, USA. Biol Invasions 13:2829–2845. https://doi.org/10.1007/s10530-011-9966-1
Aslan CE, Rejmánek M, Klinger R (2012) Combining efficient methods to detect spread of woody invaders in urban-rural matrix landscapes: An exploration using two species of Oleaceae. J Appl Ecol 49:331–338. https://doi.org/10.1111/j.1365-2664.2011.02097.x
Au AYY, Corlett RT, Hau BCH (2006) Seed rain into upland plant communities in Hong Kong, China. Plant Ecol 186:13–22. https://doi.org/10.1007/s11258-006-9108-5
Ayup MM, Montti L, Aragón R, Grau HR (2014) Invasion of Ligustrum lucidum (Oleaceae) in the southern Yungas: Changes in habitat properties and decline in bird diversity. Acta Oecol 54:72–81. https://doi.org/10.1016/j.actao.2013.03.006
Backes P, Irgang B (2004) Árvores cultivadas no sul do Brasil: guia de identificação e interesse paisagístico das principais espécies exóticas, Palotti, Porto Alegre
Basler D, Körner C (2012) Photoperiod sensitivity of bud burst in 14 temperate forest tree species. Agric For Meteorol 165:73–81. https://doi.org/10.1016/j.agrformet.2012.06.001
Benson D, McDougall L (1999) Ecology of Sydney plant species Part 7a Dicotyledon families Nyctaginaceae to Primulaceae. Cunninghamia 6:402–509
Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (purple loosestrife) and a native congener. Ecology 83:2328–2336. https://doi.org/10.1890/0012-9658(2002)083[2328:CFPBAI]2.0.CO;2
Burnham K, Anderson D (2002) Model selection and multi-model inference: a practical information-theoretic model, 2nd edn. Spring-Verlag, New York
Castro-Díez P, Montserrat-Martí G, Cornelissen JHC (2003) Trade-offs between phenology, relative growth rate, life form and seed mass among 22 Mediterranean woody species. Plant Ecol 166:117–129. https://doi.org/10.1023/A:1023209230303
Chang-Yang CH, Lu CL, Sun IF, Hsieh CF (2012) Flowering and fruiting patterns in a subtropical rain forest. Taiwan Biotropica 45:165–174. https://doi.org/10.1111/j.1744-7429.2012.00911.x
Cordeiro J, Rodrigues WA, Albrecht LP, Krenchenski FH (2014) Contaminação biológica vegetal em fragmento de floresta ombrófila mista. Rev em Agronegócios e Meio Ambient 7:455–473
Corlett RT (1993) Reproductive phenology of Hong Kong shrubland. J Trop Ecol 9:501–510
Corlett RT (2011) Seed dispersal in Hong Kong, China: past, present and possible futures. Integr Zool 6:97–109. https://doi.org/10.1111/j.1749-4877.2011.00235.x
Daehler CC (2003) Performance comparisons of co-occurring native and alien invasive plants: implications for conservation and restoration. Annu Rev Ecol Evol Syst 34:183–211. https://doi.org/10.1146/132403
Dawson W, Rohr RP, van Kleunen M, Fischer M (2012) Alien plant species with a wider global distribution are better able to capitalize on increased resource availability. New Phytol 194:859–867. https://doi.org/10.1111/j.1469-8137.2012.04104.x
Dreyer JBB, Higuchi P, Silva AC (2019) Ligustrum lucidum W. T. Aiton climatic niche shifts during global- scale invasion. Nature 9:1–6. https://doi.org/10.1038/s41598-019-40531-8
Du Y, Mi X, Liu X et al (2009) Seed dispersal phenology and dispersal syndromes in a subtropical broad-leaved forest of China. For Ecol Manage 258:1147–1152. https://doi.org/10.1016/j.foreco.2009.06.004
Ekert PA, Bucher DJ (1999) Winter use of large-leafed privet Ligustrum lucidum (Family: Oleaceae) by birds in suburban Lismore, New South Wales. Proc Linn Soc New South Wales 1999:29–38
Fenner M (1998) The phenology of growth and reproduction in plants. Perspect Plant Ecol Evol Syst 1:78–91. https://doi.org/10.1078/1433-8319-00053
Fernandes P, Antunes C, Correia O, Máguas C (2015) Do climatic and habitat conditions affect the reproductive success of an invasive tree species? An assessment of the phenology of Acacia longifolia in Portugal. Plant Ecol 216:343–355. https://doi.org/10.1007/s11258-014-0441-9
Forrest J, Miller-Rushing AJ (2010) Toward a synthetic understanding of the role of phenology in ecology and evolution. Philos Trans R Soc B Biol Sci 365:3101–3112. https://doi.org/10.1098/rstb.2010.0145
Fournier L (1974) Un método cuantitativo para la medición de características fenológicas en árboles. Turrialba 24:422–423
Gibson MR, Richardson DM, Marchante E et al (2011) Reproductive biology of Australian acacias: important mediator of invasiveness? Divers. Distrib 17:911–933
Godoy O, Castro-Díez P, Valladares F, Costa-Tenorio M (2009) Different flowering phenology of alien invasive species in Spain: evidence for the use of an empty temporal niche? Plant Biol 11:803–811. https://doi.org/10.1111/j.1438-8677.2008.00185.x
Godoy O, Richardson DM, Valladares F, Castro-Díez P (2009) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103:485–494. https://doi.org/10.1093/aob/mcn232
Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11:549–558. https://doi.org/10.1111/j.1366-9516.2005.00195.x
Guidini AL, Silva AC, Higuchi P et al (2014) Invasão por espécies arbóreas exóticas em remanescentes florestais no planalto sul catarinense. Rev Árvore 38:469–478. https://doi.org/10.1590/S0100-67622014000300009
Guilhermetti PGC, Vogel GF, Martinkoski L, Mokochinski FM (2013) Aspectos da distribuição de Ligustrum lucidum W. T. Ainton em diferentes ecossistemas: revisão bibliográfica. Rev Verde Agroecol e Desenvolv Sustentável 8:171–176
Gurvich DE, Tecco PA, Díaz S (2005) Plant invasions in undisturbed ecosystems: the triggering attribute approach. J Veg Sci. https://doi.org/10.1111/j.1654-1103.2005.tb02415.x
Hartz SM, Pinheiro GC, de Mendonça-Lima A, da Duarte L (2012) The potential role of migratory birds in the expansion of Araucaria forest. Nat Conserv 10:52–56. https://doi.org/10.4322/natcon.2012.009
Higuchi P, da Silva AC, Ferreira TS et al (2012) Floristic composition and phytogeography of the tree component of Araucaria Forest fragments in southern Brazil. Braz J Bot 35:145–157. https://doi.org/10.1590/S1806-99592012000200004
Hoyos LE, Gavier-Pizarro GI, Kuemmerle T et al (2010) Invasion of glossy privet (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Córdoba, Argentina. Biol Invasions 12:3261–3275. https://doi.org/10.1007/s10530-010-9720-0
Huang J, Huang J, Lu X, Ma K (2016) Diversity distribution patterns of Chinese endemic seed plant species and their implications for conservation planning. Sci Rep 6:1–12. https://doi.org/10.1038/srep33913
Ishii HT, Iwasaki A (2008) Ecological restoration of a fragmented urban shrine forest in southeastern Hyogo Prefecture, Japan: initial effects of the removal of invasive Trachycarpus fortunei. Urban Ecosyst 11:309–316. https://doi.org/10.1007/s11252-008-0067-6
Kikuzawa K (1995) Leaf phenology as an optimal strategy for carbon gain in plants. Can J Bot 73:158–163. https://doi.org/10.1139/b95-019
Kraft NJB, Godoy O, Levine JM (2015) Plant functional traits and the multidimensional nature of species coexistence. Proc Natl Acad Sci 112:797–802. https://doi.org/10.1073/pnas.1413650112
Kwok HK, Corlett RT (1999) Seasonality of a forest bird community in Hong Kong, South China. Ibis (Lond 1859) 141:70–79. https://doi.org/10.1111/j.1474-919X.1999.tb04264.x
Leal-Zanchet AM, Baptista V, Campos LM, Raffo JF (2011) Spatial and temporal patterns of land flatworm assemblages in Brazilian Araucaria forests. Invertebr Biol 130:25–33. https://doi.org/10.1111/j.1744-7410.2010.00215.x
Lediuk KD, Damascos MA, Puntieri JG, Svriz M (2014) Differences in phenology and fruit characteristic between invasive and native woody species favor exotic species invasiveness. Plant Ecol 215:1455–1467. https://doi.org/10.1007/s11258-014-0402-3
Li B, Hao Z, Bin Y et al (2012) Seed rain dynamics reveals strong dispersal limitation, different reproductive strategies and responses to climate in a temperate forest in northeast China. J Veg Sci 23:271–279. https://doi.org/10.1111/j.1654-1103.2011.01344.x
Liebsch D, Mikich SB (2009) Fenologia reprodutiva de espécies vegetais da Floresta Ombrófila Mista do Paraná, Brasil. Rev Bras Botânica 32:375–391. https://doi.org/10.1590/S0100-84042009000200016
MacDougall AS, Gilbert B, Levine JM (2009) Plant invasions and the niche. J Ecol 97:609–615. https://doi.org/10.1111/j.1365-2745.2009.01514.x
Marques MCM, Roper JJ, Salvalaggio AP (2004) Phenological patterns among plant life-forms in a subtropical forest in southern Brazil. Plant Ecol 173:203–213. https://doi.org/10.1023/B:VEGE.0000029325.85031.90
Montaldo NH (1993) Dispersión por aves y éxito reproductivo de dos especies de Ligustrum (Oleaceae) en un relicto de selva subtropical en la Argentina. Rev Chil Hist Nat 66:75–85
Montaldo NH (2000) Exito reproductivo de plantas ornitócoras en un relicto de selva subtropical en Argentina. Rev Chil Hist Nat 73:511–524
Morais MC, Freitas H (2015) Phenological dynamics of the invasive plant Acacia longifolia in Portugal. Weed Res 55:555–564. https://doi.org/10.1111/wre.12177
Murray BR, Phillips ML (2010) Investment in seed dispersal structures is linked to invasiveness in exotic plant species of south-eastern Australia. Biol Invasions 12:2265–2275. https://doi.org/10.1007/s10530-009-9637-7
Noma N, Yumoto T (1997) Fruiting phenology of animal-dispersed plants in response to winter migration of frugivores in a warm temperate forest on Yakushima Island, Japan. Ecol Res 12:119–129
Oliveira TWG, Milani JEF, Blum CT (2016) Comportamento fenológico da espécie invasora Ligustrum lucidum em um fragmento florestal urbano em Curitiba, Paraná, Brasil. FLORESTA 46:371–378. https://doi.org/10.5380/rf.v46i3.43386
Panetta FD (2000) Fates of fruits and seeds of Ligustrum lucidum W.T.Ait. and L. sinense Lour. maintained under natural rainfall or irrigation. Aust J Bot 48:701–705. https://doi.org/10.1071/BT00005
Peterson AT (2011) Ecological niche conservatism: a time-structured review of evidence. J Biogeogr 38:817–827. https://doi.org/10.1111/j.1365-2699.2010.02456.x
Petitpierre B, Kueffer C, Broennimann O et al (2012) Climatic niche shifts are rare among terrestrial plant invaders. Science 335:1344–1348. https://doi.org/10.1126/science.1215933
Powell PA, Aráoz E (2018) Biological and environmental effects on fine-scale seed dispersal of an invasive tree in a secondary subtropical forest. Biol Invasions 20:461–473. https://doi.org/10.1007/s10530-017-1548-4
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16:179–214
Reginato M, Matos FB, Lindoso GDS et al (2008) A vegetação na Reserva Mata Viva, Curitiba, Paraná, Brasil. Acta Biol Parana 37:229–252
Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661
Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species—2013 update of the global database. Divers Distrib 19:1093–1094. https://doi.org/10.1111/ddi.12075
Richardson DM, Pysek P, Rejmanek M et al (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107. https://doi.org/10.1046/j.1472-4642.2000.00083.x
Rivera G, Elliott S, Caldas LS et al (2002) Increasing day-length induces spring flushing of tropical dry forest trees in the absence of rain. Trees - Struct Funct 16:445–456. https://doi.org/10.1007/s00468-002-0185-3
Scheibler DR, Melo-Júnior TA de (2003) Frugivory by birds on two exotic Ligustrum species (Oleaceae) in Brazil. Ararajuba 11:89–91
Tang J, Chen Z, Fang J (2017) Study on the growth adaptability of Ligustrum L. plants in southeast Tibet. Asian Agric Res 9:38–39
Tang C, Huang L, Huang Z, Krzton A (2016) Forest seasonality shapes diet of limestone-living rhesus macaques at Nonggang, China. Primates 57:83–92. https://doi.org/10.1007/s10329-015-0498-7
Tecco PA, Díaz S, Cabido M, Urcelay C (2010) Functional traits of alien plants across contrasting climatic and land-use regimes: do aliens join the locals or try harder than them? J Ecol 98:17–27. https://doi.org/10.1111/j.1365-2745.2009.01592.x
Tecco P, Pais-Bosch A, Funes G et al (2015) Mountain invasions on the way: are there climatic constraints for the expansion of alien woody species along an elevation gradient in Argentina? J Plant Ecol. https://doi.org/10.1093/jpe/rtv064
Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting nonindigenous species success during four stages of invasion. New Phytol 176:256–273. https://doi.org/10.1111/j.1469-8137.2007.02207.x
Vergara-Tabares DL, Badini J, Peluc SI (2016) Fruiting phenology as a “triggering attribute” of invasion process: do invasive species take advantage of seed dispersal service provided by native birds? Biol Invasions 18:677–687. https://doi.org/10.1007/s10530-015-1039-4
Vitasse Y, Basler D (2013) What role for photoperiod in the bud burst phenology of European beech. Eur J For Res 132:1–8. https://doi.org/10.1007/s10342-012-0661-2
Vogel HF, Metri R, Zawadzki CH, Moura MO (2011) Avifauna from a campus of Universidade Estadual do Centro-Oeste, Guarapuava, Paraná State, Brazil. Acta Sci Biol Sci 33:197–207. https://doi.org/10.4025/actascibiolsci.v33i2.7710
Walther GR, Roques A, Hulme PE et al (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24:686–693. https://doi.org/10.1016/j.tree.2009.06.008
Way DA, Montgomery RA (2015) Photoperiod constraints on tree phenology, performance and migration in a warming world. Plant Cell Environ 38:1725–1736. https://doi.org/10.1111/pce.12431
Wilcox M (2000) Tree privet (Ligustrum lucidum) a controversial plant. Auckl Bot Soc 55:72–74
Wilczek AM, Burghardt LT, Cobb AR et al (2010) Genetic and physiological bases for phenological responses to current and predicted climates. Philos Trans R Soc B Biol Sci 365:3129–3147. https://doi.org/10.1098/rstb.2010.0128
Williams PA, Karl BJ (1996) Fleshy fruits of indigenous and adventive plants in the diet of birds in forest remnants, Nelson, New Zealand. N Z J Ecol 20:127–145
Wilson SB, Knox GW, Deng Z et al (2014) Landscape performance and fruiting of twelve privet selections grown in northern and southern Florida. HortScience 49:706–713
Wolkovich EM, Cleland EE (2011) The phenology of plant invasions: a community ecology perspective. Front Ecol Environ 9:287–294. https://doi.org/10.1890/100033
Zanini L, Ganade G (2005) Restoration of Araucaria forest: the role of perches, pioneer vegetation, and soil fertility. Restor Ecol 13:507–514. https://doi.org/10.1111/j.1526-100X.2005.00063.x
Zar JH (2010) Bioestatistical analysis, 5th edn. Prentice Hall, Upper Saddle River
Zhang S, Fan D, Wu Q et al (2013) Eco-physiological adaptation of dominant tree species at two contrasting karst habitats in southwestern China. F1000Research. https://doi.org/10.12688/f1000research.2-122.v1
Zotz G, Franke M, Woitke M (2000) Leaf phenology and seasonal carbon gain in the invasive plant, Bunias orientalis L. Plant Biol 2:653–658. https://doi.org/10.1055/s-2000-16639
Acknowledgements
The authors are grateful to Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) for the scholarship to the first author.
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic Supplementary Material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Nogueira, G.S., Seger, G.D.S., Boeger, M.R.T. et al. The phenology of Ligustrum lucidum (Oleaceae): climatic niche conservatism as an important driver of species invasion in Araucaria forest. Biol Invasions 22, 2975–2987 (2020). https://doi.org/10.1007/s10530-020-02302-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02302-9