Abstract
Plant phenological events are some of the most sensitive indicators of how plant species respond to favourable or stressful conditions. The evaluation of the flowering phenology of invasive plant species is particularly relevant, mainly due to its crucial importance in determining plant reproductive success and the outcome of invasion. We studied the phenology of Acacia longifolia, an aggressive, invasive plant species in the Mediterranean basin. We measured its vegetative growth and reproductive traits, specifically flowering phenophases and fruit production, under different climatic conditions (mesic and xeric Mediterranean climates), and in two different habitats (pine forest and open area). All the measured phenological phases began earlier at the xeric site than at the mesic site; this was particularly evident when comparing reproductive phenophases. Flowering dates were significantly associated with air temperature, with early peak flowering dates linked to increases in air temperature. The number of fruiting flowers per inflorescence in A. longifolia trees was higher at the mesic site, mainly in the pine forest plot, and the number of aborted fruits was notably lower than in the xeric plots. The presence of a pine forest at the mesic site strongly influenced the flowering phenology of A. longifolia and resulted in the highest reproductive success and the lowest branch growth rate. Our results demonstrate that a combination of climate and forest structure can cause pronounced differences in phenology and reproductive success of A. longifolia. These data can help to understand the variations in invasive rates of A. longifolia across the Mediterranean basin.
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References
Bustamante E, Búrquez A (2008) Effects of plant size and weather on the flowering phenology of the organ pipe cactus (Stenocereus thurberi). Ann Bot 102(6):1019–1030. doi:10.1093/aob/mcn194
Castro-Díez P, Montserrat-Martí G (1998) Phenological pattern of fifteen Mediterranean phanaerophytes from shape Quercus ilex communities of NE-Spain. Plant Ecol 139(1):103–112. doi:10.1023/A:1009759318927
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(1):117–129. doi:10.1023/A:1023209230303
Dahlgren JP, von Zeipel H, Ehrlén J (2007) Variation in vegetative and flowering phenology in a forest herb caused by environmental heterogeneity. Am J Bot 94(9):1570–1576. doi:10.3732/ajb.94.9.1570
Di Castri F, Goodall DW, Specht RL (1981) Mediterranean-type shrublands. In: Goodall DW (ed) Ecosystems of the World 11. Elsevier, Amsterdam, p 643
Elzinga JA, Atlan A, Biere A, Gigord L, Weis AE, Bernasconi G (2007) Time after time: flowering phenology and biotic interactions. Trends Ecol Evol 22(8):432–439. doi:10.1016/j.tree.2007.05.006
Fitter AH (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 9:55–60
Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296(5573):1689–1691. doi:10.1126/science.1071617
Fleming PA, Hofmeyr SD, Nicolson SW (2007) Role of insects in the pollination of Acacia nigrescens (Fabaceae). South Afr J Bot 73(1):49–55. doi:10.1016/j.sajb.2006.06.010
Fox GA (1990) Drought and the evolution of flowering time in desert annuals. Am J Bot 77:1508–1518. Retrieved from https://foxlab.files.wordpress.com/2011/06/droughtfltime_amjbot1990.pdf
Gibson MR, Richardson DM, Marchante E, Marchante H, Rodger JG, Stone GN, Wilson JRU (2011) Reproductive biology of Australian acacias: important mediator of invasiveness? Divers Distrib 17(5):911–933. doi:10.1111/j.1472-4642.2011.00808.x
Godoy O, Castro-Díez P, Valladares F, Costa-Tenorio M (2009a) Different flowering phenology of alien invasive species in Spain: evidence for the use of an empty temporal niche? Plant Biol 11(6):803–811. doi:10.1111/j.1438-8677.2008.00185.x
Godoy O, Richardson DM, Valladares F, Castro-Díez P (2009b) Flowering phenology of invasive alien plant species compared with native species in three Mediterranean-type ecosystems. Ann Bot 103(3):485–494. doi:10.1093/aob/mcn232
Groves RH, di Castri KJ (1991) Biogeography of Mediterranean invasions. Cambridge University Press, Cambridge. Retrieved from http://www.cambridge.org/ar/academic/subjects/life-sciences/ecology-and-conservation/biogeography-mediterranean-invasions
Hellmann C, Sutter R, Rascher KG, Máguas C, Correia O, Werner C (2011) Impact of an exotic N2-fixing Acacia on composition and N status of a native Mediterranean community. Acta Oecol 37(1):43–50. doi:10.1016/j.actao.2010.11.005
Herrera CM (1997) Thermal biology and foraging responses of insect pollinators to the forest floor irradiance mosaic. Oikos 78:601–611. Retrieved from http://digital.csic.es/handle/10261/42296
Jackson MT (1966) Effects of microclimate on spring flowering phenology. Ecology 47(3):407. doi:10.2307/1932980
Kilkenny FF, Galloway LF (2008) Reproductive success in varying light environments: direct and indirect effects of light on plants and pollinators. Oecologia 155(2):247–255. doi:10.1007/s00442-007-0903-z
Lake JC, Leishman M (2004) Invasion success of exotic plants in natural ecosystems: the role of disturbance, plant attributes and freedom from herbivores. Biol Conserv 117(2):215–226. doi:10.1016/S0006-3207(03)00294-5
Lesica P, Kittelson PM (2010) Precipitation and temperature are associated with advanced flowering phenology in a semi-arid grassland. J Arid Environ 74(9):1013–1017. doi:10.1016/j.jaridenv.2010.02.002
Lieth H (Ed) (1974) Phenology and seasonality modeling (vol 8). Springer, Berlin. doi:10.1007/978-3-642-51863-8
Máguas C, Rascher KG, Martins-Loução A, Carvalho P, Pinho P, Ramos M, Werner C (2011) Responses of woody species to spatial and temporal ground water changes in coastal sand dune systems. Biogeosciences 8(12):3823–3832. doi:10.5194/bg-8-3823-2011
Marchante H (2011) Invasion of Portuguese dunes by Acacia longifolia: present status and perspectives for the future. Universidade de Coimbra. Retrieved from https://estudogeral.sib.uc.pt/bitstream/10316/18181/1/HeliaMarchantePhDthesis.pdf
Marchante H, Marchante E, Freitas H (2003) Invasion of the Portuguese dune ecosystems by the exotic species Acacia longifolia (Andrews) Willd.: effects at the community level. In: Child L, Brock JH, Brundu G, Prach K, Pyšek P, Wade P, Williamson M (eds) Plant invasions: ecological threats and management solutions. Backhuys Publishers, Leiden, pp 75–85
Marquis RJ (1988) Phenological variation in the neotropical understory shrub piper arielanum: causes and consequences. Ecology 69(5):1552. doi:10.2307/1941653
Matesanz S, Gianoli E, Valladares F (2010) Global change and the evolution of phenotypic plasticity in plants. Ann N Y Acad Sci 1206:35–55. doi:10.1111/j.1749-6632.2010.05704.x
Menzel A, Sparks TH, Estrella N, Koch E, Aasa A, Ahas R, Zust A (2006) European phenological response to climate change matches the warming pattern. Glob Change Biol 12(10):1969–1976. doi:10.1111/j.1365-2486.2006.01193.x
Milla R, Castro-Díez P, Montserrat-Martí G (2010) Phenology of Mediterranean woody plants from NE Spain: synchrony, seasonality, and relationships among phenophases. Flora-Morphol Distrib Funct Ecol Plants 205(3):190–199. doi:10.1016/j.flora.2009.01.006
Miller-Rushing AJ, Inouye DW, Primack RB (2008) How well do first flowering dates measure plant responses to climate change? The effects of population size and sampling frequency. J Ecol 96(6):1289–1296. doi:10.1111/j.1365-2745.2008.01436.x
Milton SJ, Moll EJ (1982) Phenology of Australian acacias in the S.W. Cape, South Africa, and its implications for management. Bot J Linn Soc 84(4):295–327. doi:10.1111/j.1095-8339.1982.tb00367.x
Montserrat-Martí G, Pérez-Rontomé C (2002) Fruit growth dynamics and their effects on the phenological pattern of native Pistacia populations in NE Spain. Flora-Morphol Distrib Funct Ecol Plants 197(3):161–174. doi:10.1078/0367-2530-00027
Newmark W (2005) Diel variation in the difference in air temperature between the forest edge and interior in the Usambara Mountains, Tanzania. Afr J Ecol 43(3):177–180. doi:10.1111/j.1365-2028.2005.00557.x
Orlandi F, Sgromo C, Bonofiglio T, Ruga L, Romano B, Fornaciari M (2010) Yield modelling in a Mediterranean species utilizing cause–effect relationships between temperature forcing and biological processes. Sci Hortic 123(3):412–417. doi:10.1016/j.scienta.2009.09.015
Post E, Stenseth NC (1999) Climatic variability, plant phenology, and northern ungulates. Ecology 80:1322–1339
Prieto P, Peñuelas J, Ogaya R, Estiarte M (2008) Precipitation-dependent flowering of Globularia alypum and Erica multiflora in Mediterranean shrubland under experimental drought and warming, and its inter-annual variability. Ann Bot 102(2):275–285. doi:10.1093/aob/mcn090
Pysek P, Richardson DM (2007) Traits associated with invasiveness in alien plants: where do we stand? In: Nentwig W (ed) Biological invasions. Springer, Berlin, pp 97–125
Raine NE, Pierson AS, Stone GN (2007) Plant–pollinator interactions in a Mexican Acacia community. Arthropod-Plant Interact 1(2):101–117. doi:10.1007/s11829-007-9010-7
Rascher KG, Große-Stoltenberg A, Máguas C, Meira-Neto JAA, Werner C (2011) Acacia longifolia invasion impacts vegetation structure and regeneration dynamics in open dunes and pine forests. Biol Invasions 13(5):1099–1113. doi:10.1007/s10530-011-9949-2
Rascher KG, Hellmann C, Máguas C, Werner C (2012) Community scale 15N isoscapes: tracing the spatial impact of an exotic N2-fixing invader. Ecol Lett 15(5):484–491. doi:10.1111/j.1461-0248.2012.01761.x
Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16(1):179–214. doi:10.1146/annurev.es.16.110185.001143
Roberts EH, Summerfield RJ (1987) Measurement and prediction of flowering in annual crops. In: Atherton JG (Ed) Manipulation of flowering, Butterworths, London, pp 17–50. Retrieved from http://agris.fao.org/agris-search/search.do?recordID=US201302074042
Schröder W, Schmidt G, Schönrock S (2014) Modelling and mapping of plant phenological stages as bio-meteorological indicators for climate change. Environ Sci Eur 26:5. doi:10.1186/2190-4715-26-5
Schwartz MD (1999) Advancing to full bloom: planning phenological research for 21st century. Int J Biometeorol 42:113–118
Seghieri J, Carreau J, Boulain N, De Rosnay P, Arjounin M, Timouk F (2012) Is water availability really the main environmental factor controlling the phenology of woody vegetation in the central Sahel?. Plant Ecol 213:861–870. doi:10.1007/s11258-012-0048-y
Sekhwela MBM, Yates DJ (2007) A phenological study of dominant acacia tree species in areas with different rainfall regimes in the Kalahari of Botswana. J Arid Environ 70(1):1–17. doi:10.1016/j.jaridenv.2006.12.006
Sparks TH, Carey PD (1995) The responses of species to climate over two centuries: an analysis of the Marsham phenological record. 1736-1947. J Ecol 83:321–329. Retrieved from http://books.google.pt/books/about/The_responses_of_species_to_climate_over.html?id=n_4CaAEACAAJ&pgis=1
Sparks TH, Jeffree EP, Jeffree CE (2000) An examination of the relationship between flowering times and temperature at the national scale using long-term phenological records from the UK. Int J Biometeorol 44(2):82–87. Retrieved from http://www.ncbi.nlm.nih.gov/pubmed/10993562
Stone GN, Raine NE, Prescott M, Willmer PG (2003) Pollination ecology of acacias (Fabaceae, Mimosoideae). Aust Syst Bot 16(1):103. doi:10.1071/SB02024
US/IBP Phenology Committee Report (1972) French NR (ed) Chairman. Austin, Texas: US/IBP Environmental Coordinating Office. In: Lieth H (ed) Phenology and seasonality modeling, Ecological Studies, Vol 8. Springer, Berlin, pp 23–24. doi:10.1007/978-3-642-51863-8_2
Walther G-R, Roques A, Hulme PE, Sykes MT, Pysek P, Kühn I, Settele J (2009) Alien species in a warmer world: risks and opportunities. Trends Ecol Evol 24(12):686–693. doi:10.1016/j.tree.2009.06.008
Werner C, Zumkier U, Beyschlag W, Máguas C (2009) High competitiveness of a resource demanding invasive acacia under low resource supply. Plant Ecol 206(1):83–96. doi:10.1007/s11258-009-9625-0
Yates CJ, Broadhurst LM (2002) Assessing limitations on population growth in two critically endangered Acacia taxa. Biol Conserv 108(1):13–26. doi:10.1016/S0006-3207(02)00084-8
Zar J (1999) Biostatistical analysis. Prentice-Hall International, New Jersey
Acknowledgments
The authors are grateful to REN-Armazenagem, SA (former TransGas, SA) and Estabelecimento Prisional de Pinheiro da Cruz for logistical support and allowing the establishment of our field sites, and to all the colleagues who performed field work.
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Communicated by Lesley Rigg.
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Fernandes, P., Antunes, C., Correia, O. et al. 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 (2015). https://doi.org/10.1007/s11258-014-0441-9
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DOI: https://doi.org/10.1007/s11258-014-0441-9