Plant Ecology

, 200:241 | Cite as

Temporal variation in the effects of habitat fragmentation on reproduction of the Mediterranean shrub Colutea hispanica

  • Sonia G. RabasaEmail author
  • David Gutiérrez
  • Adrián Escudero


Habitat fragmentation poses a major threat to the viability of plant populations. However, the intensity of fragmentation effects may vary among years. We studied two possible effects of habitat fragmentation (patch size and isolation) on the reproduction and proportion of damaged fruits in 24 patches of the self-compatible shrub Colutea hispanica for three consecutive years with different climate conditions. We also studied the effect of fragmentation on the incidence of two main pre-dispersal seed predators, the butterflies Iolana iolas and Lampides boeticus. High between-year variability was found in number of viable seeds per fruit, number of fruits per plant, total number of viable seeds per plant and proportion of damaged fruits. In 2003, small, isolated patches had a higher fruit set and number of fruits per plant. The proportion of damaged fruits was significantly lower in isolated populations in 2003, while it was very high in all patches in 2004 and 2005. High between-year variability was also found in the proportion of fruits per plant with I. iolas eggs. In 2003 isolated patches had a lower proportion of fruits with I. iolas eggs, but no significant effect of patch size and isolation was found in 2004 or 2005. The proportion of fruits with L. boeticus eggs was similar in the three years of study, although it was slightly higher in large, non-isolated patches in 2003. Thus, the effects of fragmentation on plant reproduction cannot be generalized from one single-year survey. In contrast to the generally accepted idea that fragmentation reduces plant reproduction, plant fitness may increase in isolated patches in years with high fruit production and low seed predation.


Habitat fragmentation Isolation Patch size Plant–animal interaction 



We thank C. F. Aragón, M. J. Albert, L. Giménez-Benavides and A. López de Luzuriaga for their help with field work, C. M. Herrera for statistical advice, M. Méndez for discussion and J. Ehrlén for interesting comments on the manuscript. We also thank the Regional Government of Madrid for providing 1:5,000 digital maps and permission to work with C. hispanica and I. iolas, and the Spanish National Meteorological Institute for thermopluviometric data. This study was supported by the research projects BOS2002-00742 and CGL2006-09431 from the Spanish Ministry of Education and Science, the REMEDINAL program (ref. S-0505/AMB-0335), and a FPU predoctoral fellowship to SG Rabasa.


  1. Aguilar R, Ashworth L, Galetto L et al (2006) Plant reproductive susceptibility to habitat fragmentation: review and synthesis through a meta-analysis. Ecol Lett 9:968–980. doi: 10.1111/j.1461-0248.2006.00927.x PubMedCrossRefGoogle Scholar
  2. Ågren J (1996) Population size, pollinator limitation, and seed set in the self-incompatible herb Lythrum salicaria. Ecology 77:1779–1790. doi: 10.2307/2265783 CrossRefGoogle Scholar
  3. Aizen MA, Feinsinger P (1994) Forest fragmentation, pollination, and plant reproduction in a Chaco dry forest, Argentina. Ecology 75:330–351. doi: 10.2307/1939538 CrossRefGoogle Scholar
  4. Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15:257–267. doi: 10.2307/2387650 CrossRefGoogle Scholar
  5. Barrett SCH, Kohn JR (1991) Genetic and evolutionary consequences of small population size in plants: implications for conservation. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. University Press, Oxford, pp 31–61Google Scholar
  6. Bosch M, Simon J, Rovira AM et al (2002) Pollination ecology of the pre-Pyrenean endemic Petrocoptis montsicciana (Caryophyllaceae): effects of population size. Biol J Linn Soc 76:79–90CrossRefGoogle Scholar
  7. Breslow NE, Clayton DG (1993) Approximate inference in generalized linear mixed models. J Am Stat Assoc 88:9–25. doi: 10.2307/2290687 CrossRefGoogle Scholar
  8. Bruna EM (2003) Are plant populations in fragmented habitats recruitment limited? Tests with an amazonian herb. Ecology 84:932–947. doi: 10.1890/0012-9658(2003)084[0932:APPIFH]2.0.CO;2 CrossRefGoogle Scholar
  9. Brys R, Jacquemyn H, Endels P et al (2004) Reduced reproductive success in small populations of the self-compatible Primula vulgaris. J Ecol 92:5–14. doi: 10.1046/j.0022-0477.2004.00840.x CrossRefGoogle Scholar
  10. Chacoff NP, Morales JM, Vaquera MP (2004) Efectos de la fragmentación sobre la aborción y depredación de semillas en el Chaco Serrano. Biotropica 36:109–117Google Scholar
  11. Costin BJ, Morgan JW, Young AD (2001) Reproductive success does not decline in fragmented populations of Leucochrysum albicans subsp. albicans var. tricolor (Asteraceaea). Biol Conserv 98:273–284. doi: 10.1016/S0006-3207(00)00165-8 CrossRefGoogle Scholar
  12. Cunningham SA (2000) Effects of habitat fragmentation on the reproductive ecology of four plant species in Mallee Woodland. Conserv Biol 14:758–768. doi: 10.1046/j.1523-1739.2000.98609.x CrossRefGoogle Scholar
  13. Donaldson J, Näni I, Zachariades C et al (2001) Effects of habitat fragmentation on pollinator diversity and plant reproductive success in Renosterveld shrublands of South Africa. Conserv Ecol 16:1267–1276Google Scholar
  14. Duncan HD, Nicotra AB, Wood JF et al (2004) Plant isolation reduces outcross pollen receipt in a partially self-compatible herb. J Ecol 92:977–985. doi: 10.1111/j.1365-2745.2004.00933.x CrossRefGoogle Scholar
  15. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242. doi: 10.1146/ CrossRefGoogle Scholar
  16. Fischer M, Matthies D (1998) Effects of population size on performance in the rare plant Gentianella germanica. J Ecol 86:195–204. doi: 10.1046/j.1365-2745.1998.00246.x CrossRefGoogle Scholar
  17. García D, Chacoff NP (2007) Scale-dependent effects of habitat fragmentation on hawthorn pollination, frugivory, and seed predation. Conserv Biol 21:400–411. doi: 10.1111/j.1523-1739.2006.00593.x PubMedCrossRefGoogle Scholar
  18. García D, Zamora R (2003) Persistence, multiple demographic strategies and conservation in long-lived Mediterranean plants. J Veg Sci 14:921–926. doi: 10.1658/1100-9233(2003)014[0921:PMDSAC]2.0.CO;2 CrossRefGoogle Scholar
  19. Gil-T F (2001) Estudio sobre la influencia de parasitoides (Hymenoptera: Ichneumonoidea) en poblaciones del raro lepidóptero Iolana iolas Oschsenheimer, 1816 (Lepidoptera: Lycaenidae). Bol Soc Entomol Aragon 29:85–88Google Scholar
  20. Glémin S (2003) How are deleterious mutations purged? Drift versus nonrandom mating. Evolution Int J Org Evolution 57:2678–2687Google Scholar
  21. Goverde M, Schweizer K, Baur B et al (2002) Small-scale habitat fragmentation effects on pollinator behaviour: experimental evidence from the bumblebee Bombus veteranus on calcareous grasslands. Biol Conserv 104:293–299. doi: 10.1016/S0006-3207(01)00194-X CrossRefGoogle Scholar
  22. Groom MJ (2001) Consequences of subpopulation isolation for pollination, herbivory, and population growth in Clarkia concinna concinna (Onagraceae). Biol Conserv 100:55–63. doi: 10.1016/S0006-3207(00)00207-X CrossRefGoogle Scholar
  23. Hackney EE, McGraw JB (2001) Experimental demonstration of an Allee effect in American Ginseng. Conserv Biol 15:129–136. doi: 10.1046/j.1523-1739.2001.98546.x CrossRefGoogle Scholar
  24. Hanski I, Kuussaari M, Nieminen M (1994) Metapopulation structure and migration in the butterfly Melitea cinxia. Ecology 75:747–762. doi: 10.2307/1941732 CrossRefGoogle Scholar
  25. Hobbs RJ, Yates CJ (2003) Impacts of ecosystem fragmentation on plant populations: generalizing the idiosyncratic. Aust J Bot 51:471–488. doi: 10.1071/BT03037 CrossRefGoogle Scholar
  26. Jacquemyn H, Brys R, Hermy M (2002) Patch occupancy, population size and reproductive success of a forest herb (Primula elatior) in a fragmented landscape. Oecologia 130:617–625. doi: 10.1007/s00442-001-0833-0 CrossRefGoogle Scholar
  27. Janzen DH (1971) Seed predation by animals. Annu Rev Ecol Syst 2:465–492. doi: 10.1146/ CrossRefGoogle Scholar
  28. Jennersten O (1988) Pollination of Dianthus deltoides (Caryophyllaceae): effects of habitat fragmentation on visitation and seed set. Conserv Biol 2:225–366. doi: 10.1111/j.1523-1739.1988.tb00200.x CrossRefGoogle Scholar
  29. Johnson SD, Collin CL (2004) Factors contributing to variation in seed production among remnant populations of the endangered daisy Gerbera aurantiaca. Biotropica 36:148–155Google Scholar
  30. Kareiva P (1987) Habitat fragmentation and the stability of predator-prey interactions. Nature 326:388–390. doi: 10.1038/326388a0 CrossRefGoogle Scholar
  31. Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112. doi: 10.1146/annurev.ecolsys.29.1.83 CrossRefGoogle Scholar
  32. Kéry M, Matthies D, Fischer M (2001) The effect of plant population size on the interactions between the rare plant Gentiana cruciata and its specialized herbivore Maculinea rebeli. J Ecol 89:418–427. doi: 10.1046/j.1365-2745.2001.00550.x CrossRefGoogle Scholar
  33. Kruess A, Tscharntke T (1994) Habitat fragmentation, species loss, and biological control. Science 264:1581–1584. doi: 10.1126/science.264.5165.1581 PubMedCrossRefGoogle Scholar
  34. Lienert J (2004) Habitat fragmentation effects on fitness of plant populations—a review. J Nat Conserv 12:53–72. doi: 10.1016/j.jnc.2003.07.002 CrossRefGoogle Scholar
  35. Lienert J, Fischer M (2003) Habitat fragmentation affects the common wetland specialist Primula farinosa in north-east Switzerland. J Ecol 91:587–599. doi: 10.1046/j.1365-2745.2003.00793.x CrossRefGoogle Scholar
  36. Littell RC, Milliken GA, Stroup WW et al (1996) SAS system for mixed models. SAS Institute, CaryGoogle Scholar
  37. McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman and Hall, LondonGoogle Scholar
  38. Menges ES (1992) Stochastic modeling of extinction in plant populations. In: Fiedler PL, Jain SK (eds) Conservation biology: the theory and practice of nature conservation, preservation, and management. Chapman and Hall, New York, pp 253–275Google Scholar
  39. Molano-Flores B, Hendrix SD, Heard SB (1999) The effect of population size on stigma pollen load, fruit set, and seed set in Allium stellatum Ker. (Liliaceae). Int J Plant Sci 160:753–757. doi: 10.1086/314160 CrossRefGoogle Scholar
  40. Molitor A (1937) Zur vergleichenden psychobiologie der akuleatuen hymenopteren auf experimenteller grundlage. Biol Gen 13:295–333Google Scholar
  41. Moody-Weis JM, Heywood JS (2001) Pollination limitation to reproductive success in the Missouri evening primrose Oenothera macrocarpa (Onagraceae). Am J Bot 88:1615–1622. doi: 10.2307/3558406 CrossRefGoogle Scholar
  42. Morgan JW (1999) Effects of population size on seed production and germinability in a endangered, fragmented grassland plant. Conserv Biol 13:266–273. doi: 10.1046/j.1523-1739.1999.013002266.x CrossRefGoogle Scholar
  43. Munguira ML (1989) Biología y Biogeografía de los Licénidos Ibéricos en peligro de extinción (Lepidoptera: Lycaenidae). PhD Thesis, Servicio de Publicaciones de la Universidad Autónoma de MadridGoogle Scholar
  44. Murren CJ (2002) Effects of habitat fragmentation on pollination: pollinators, pollinia viability and reproductive success. J Ecol 90:100–107. doi: 10.1046/j.0022-0477.2001.00638.x CrossRefGoogle Scholar
  45. Navarro L (1997) Is the dichogamy of Salvia verbenaca (Lamiaceae) an effective barrier to self-pollination? Plant Syst Evol 207:111–117. doi: 10.1007/BF00985212 CrossRefGoogle Scholar
  46. Navarro L, Guitián J (2002) The role of floral biology and breeding system on the reproductive success of the narrow endemic Petrocoptis viscosa rothm (Caryophyllaceae). Biol Conserv 103:125–132. doi: 10.1016/S0006-3207(01)00108-2 CrossRefGoogle Scholar
  47. Patterson HD, Thompson R (1971) Recovery of interblock information when block sizes are unequal. Biometrika 58:545–554. doi: 10.1093/biomet/58.3.545 CrossRefGoogle Scholar
  48. Rabasa SG, Gutiérrez D, Escudero A (2005) Egg laying by a butterfly on a fragmented host plant: a multi-level approach. Ecography 28:629–639. doi: 10.1111/j.2005.0906-7590.04229.x CrossRefGoogle Scholar
  49. Schemske DW, Husband BC, Ruckelshaus MH et al (1994) Evaluating approaches to the conservation of rare and endangered plants. Ecology 75:584–606. doi: 10.2307/1941718 CrossRefGoogle Scholar
  50. Schulke B, Waser NW (2001) Long-distance pollinator flights and pollen dispersal between populations of Delphinium nuttallianum. Oecologia 127:239–245. doi: 10.1007/s004420000586 CrossRefGoogle Scholar
  51. Sih A, Baltus MS (1987) Patch size, pollinator behaviour, and pollinator limitation in catnip. Ecology 68:1679–1690. doi: 10.2307/1939860 CrossRefGoogle Scholar
  52. Steffan-Dewenter I, Tscharntke T (1999) Effects of habitat isolation on pollinator communities and seed set. Oecologia 121:432–440. doi: 10.1007/s004420050949 CrossRefGoogle Scholar
  53. Steffan-Dewenter I, Münzenberg U, Tscharntke T (2001) Pollination, seed set and seed predation on a landscape scale. Proc R Soc Lond B Biol Sci 268:1685–1690. doi: 10.1098/rspb.2001.1737 CrossRefGoogle Scholar
  54. Talavera S, Arista M (1998) Notas sobre el género Colutea (Leguminosae) en España. An Jardin Botanico Madr 56:410–416Google Scholar
  55. Tolman T, Lewington R (1997) Collins field guide. Butterflies of Britain and Europe. Harper Collins Publishers, LondonGoogle Scholar
  56. Tomimatsu H, Ohara M (2002) Effects of forest fragmentation on seed production of the understory herb Trillium camschatcense. Conserv Biol 16:1277–1285. doi: 10.1046/j.1523-1739.2002.00412.x CrossRefGoogle Scholar
  57. Verbeke G, Molenberghs G (1997) Linear mixed models in practice. A SAS-oriented approach. Springer, New YorkGoogle Scholar
  58. Wang J, Hill WG, Charlesworthn D, Charlesworth B (1999) Dynamics of inbreeding depression due to deleterious mutations in small populations: mutation parameters and inbreeding rate. Genet Res 74:165–178. doi: 10.1017/S0016672399003900 PubMedCrossRefGoogle Scholar
  59. Ward M, Johnson SD (2005) Pollen limitation and demographic structure in small fragmented populations of Brunsvigia radulosa (Amaryllidaceae). Oikos 108:253–262. doi: 10.1111/j.0030-1299.2005.13468.x CrossRefGoogle Scholar
  60. Young AG, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418. doi: 10.1016/0169-5347(96)10045-8 CrossRefGoogle Scholar
  61. Zabel J, Tscharntke T (1999) Does fragmentation of Urtica habitats affect phytophagous and predatory insects differentially? Oecologia 116:419–425. doi: 10.1007/s004420050605 CrossRefGoogle Scholar
  62. Zar JH (1999) Biostatistical analyses, 4th edn. Prentice Hall, New JerseyGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Sonia G. Rabasa
    • 1
    Email author
  • David Gutiérrez
    • 1
  • Adrián Escudero
    • 1
  1. 1.Área de Biodiversidad y Conservación, Escuela Superior de Ciencias Experimentales y TecnologíaUniversidad Rey Juan CarlosMadridSpain

Personalised recommendations