Plant Ecology

, Volume 216, Issue 2, pp 343–355 | Cite as

Do climatic and habitat conditions affect the reproductive success of an invasive tree species? An assessment of the phenology of Acacia longifolia in Portugal

  • Patrícia Fernandes
  • Cristina Antunes
  • Otília Correia
  • Cristina Máguas


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.


Plant phenology Invasive plants Maritime pine forest Dunes 



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.


  1. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  2. 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 CrossRefGoogle Scholar
  3. 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 CrossRefGoogle Scholar
  4. 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 PubMedCrossRefGoogle Scholar
  5. Di Castri F, Goodall DW, Specht RL (1981) Mediterranean-type shrublands. In: Goodall DW (ed) Ecosystems of the World 11. Elsevier, Amsterdam, p 643Google Scholar
  6. 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 PubMedCrossRefGoogle Scholar
  7. Fitter AH (1995) Relationships between first flowering date and temperature in the flora of a locality in central England. Funct Ecol 9:55–60CrossRefGoogle Scholar
  8. Fitter AH, Fitter RSR (2002) Rapid changes in flowering time in British plants. Science 296(5573):1689–1691. doi: 10.1126/science.1071617 PubMedCrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. Fox GA (1990) Drought and the evolution of flowering time in desert annuals. Am J Bot 77:1508–1518. Retrieved from
  11. 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 CrossRefGoogle Scholar
  12. 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 PubMedCrossRefGoogle Scholar
  13. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  14. Groves RH, di Castri KJ (1991) Biogeography of Mediterranean invasions. Cambridge University Press, Cambridge. Retrieved from
  15. 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 CrossRefGoogle Scholar
  16. Herrera CM (1997) Thermal biology and foraging responses of insect pollinators to the forest floor irradiance mosaic. Oikos 78:601–611. Retrieved from
  17. Jackson MT (1966) Effects of microclimate on spring flowering phenology. Ecology 47(3):407. doi: 10.2307/1932980 CrossRefGoogle Scholar
  18. 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 PubMedCrossRefGoogle Scholar
  19. 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 CrossRefGoogle Scholar
  20. 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 CrossRefGoogle Scholar
  21. Lieth H (Ed) (1974) Phenology and seasonality modeling (vol 8). Springer, Berlin. doi: 10.1007/978-3-642-51863-8
  22. 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 CrossRefGoogle Scholar
  23. Marchante H (2011) Invasion of Portuguese dunes by Acacia longifolia: present status and perspectives for the future. Universidade de Coimbra. Retrieved from
  24. 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 75–85Google Scholar
  25. Marquis RJ (1988) Phenological variation in the neotropical understory shrub piper arielanum: causes and consequences. Ecology 69(5):1552. doi: 10.2307/1941653 CrossRefGoogle Scholar
  26. 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 PubMedCrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. 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 CrossRefGoogle Scholar
  30. 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 CrossRefGoogle Scholar
  31. 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 CrossRefGoogle Scholar
  32. 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 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. Post E, Stenseth NC (1999) Climatic variability, plant phenology, and northern ungulates. Ecology 80:1322–1339CrossRefGoogle Scholar
  35. 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 PubMedCentralPubMedCrossRefGoogle Scholar
  36. 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 97–125CrossRefGoogle Scholar
  37. 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 CrossRefGoogle Scholar
  38. 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  CrossRefGoogle Scholar
  39. 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
  40. Rathcke B, Lacey EP (1985) Phenological patterns of terrestrial plants. Annu Rev Ecol Syst 16(1):179–214. doi: 10.1146/ CrossRefGoogle Scholar
  41. 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
  42. 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 
  43. Schwartz MD (1999) Advancing to full bloom: planning phenological research for 21st century. Int J Biometeorol 42:113–118CrossRefGoogle Scholar
  44. 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  
  45. 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 CrossRefGoogle Scholar
  46. 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
  47. 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
  48. 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 CrossRefGoogle Scholar
  49. 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
  50. 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 PubMedCrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. Zar J (1999) Biostatistical analysis. Prentice-Hall International, New JerseyGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • Patrícia Fernandes
    • 1
  • Cristina Antunes
    • 1
  • Otília Correia
    • 1
  • Cristina Máguas
    • 1
  1. 1.Centro de Biologia Ambiental, Faculdade de CiênciasUniversidade de LisboaLisbonPortugal

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