Tree Genetics & Genomes

, 13:17 | Cite as

Effects of habitat fragmentation on parental correlations in the seed rain of a bird-dispersed species

  • Clara Parejo-Farnés
  • Juan J. Robledo-Arnuncio
  • Rafael G. Albaladejo
  • Encarnación Rubio-Pérez
  • Abelardo Aparicio
Original Article
Part of the following topical collections:
  1. Population structure


Seed dispersal plays a crucial role in natural forest regeneration. Changes in the seed rain due to anthropogenic habitat alteration can influence seedling recruitment patterns and affect the evolutionary dynamics of populations. Using a combined endocarp-embryo microsatellite assay of naturally dispersed seeds, we concomitantly quantify the contribution of contemporary pollen and seed dispersal to the genetic structure of the seed rain of the shrub species Pistacia lentiscus L. The study was conducted in two consecutive seasons at four forest fragments embedded in contrasting (connected vs. isolated) landscapes. Interseasonal variation in the parental genetic structure of the seed rain was assessed through analysis of molecular variance, and paternal and maternal correlations and effective parental numbers were computed for different fragments and microhabitats (within fragments) using genetic kinship analysis. Temporal variation in the genetic structure of the dispersed seeds was higher for maternal gametes, reflecting a more temporally variable contribution of individual mother plants to the seed rain, as a potential consequence of masting and/or natural heterogeneity. Higher effective numbers of fathers than mothers were consistently observed in all studied forest fragments and microhabitats, the difference being more pronounced for connected than for isolated fragments. The effective number of mothers, directly influenced by disperser birds’ behavior, was apparently insensitive to fragmentation. Despite potentially high mobility of pollen by wind and seeds by birds, habitat fragmentation could influence the parental structure of dispersed seeds, with potential consequences for the genetic structure of the adult generation.


Gene flow Pistacia lentiscus Pollen and seed dispersal Kinship Parental structure analysis 



The authors thank to the local landowners for permission to work at the study sites, S. Nora for field and laboratory assistance, and E. Villalobo, three anonymous reviewers, and the editor for helpful comments on the manuscript. This study was supported by a grant from the Spanish Ministry of Economy and Competitiveness (CGL2011-23721). JJRA was partly supported by CGL2015-64164-R project from the Spanish Ministry of Economy and Competitiveness. CPF is supported by a predoctoral fellowship from Ministry of Economy and Competitiveness (BES-2012-055103).

Data Archiving Statement

Microsatellite data is already uploaded to the dryad database with the accession number doi: 10.5061/dryad.45t51

Supplementary material

11295_2017_1100_MOESM1_ESM.docx (83 kb)
ESM 1 (DOCX 83 kb).


  1. Aguilar R, Galetto L (2004) Effects of forest fragmentation on male and female reproductive success in Cestrum parqui (Solanaceae). Oecol 138:513–520. doi: 10.1007/s00442-003-1451-9 CrossRefGoogle Scholar
  2. Aguilar R, Ashworth L, Galetto L, Aizen MA (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 CrossRefPubMedGoogle Scholar
  3. Aguilar R, Quesada M, Ashworth L, Herrerias-Diego Y, Lobo J (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. doi: 10.1111/j.1365-294X.2008.03971.x CrossRefPubMedGoogle Scholar
  4. Albaladejo RG, Sebastiani F, Aparicio A, Buinamici A, González-Martínez GC, Vendramin GG (2008) Development and characterization of eight polymorphic microsatellite loci from Pistacia lentiscus L. (Anacardiaceae). Mol Ecol Resour 8:904–906. doi: 10.1111/j.1755-0998.2008.02110.x CrossRefPubMedGoogle Scholar
  5. Albaladejo RG, González-Martínez SC, Heuertz M, Vendramin GG, Aparicio A (2009) Spatiotemporal mating pattern variation in a wind-pollinated Mediterranean shrub. Mol Ecol 18:5195–5206. doi: 10.1111/j.1365-294X.2009.04415.x CrossRefPubMedGoogle Scholar
  6. Albaladejo RG, Guzmán B, González-Martínez SC, Aparicio A (2012) Extensive pollen flow but few pollen donors and high reproductive variance in an extremely fragmented landscape. PLoS One 7:e49012. doi: 10.1371/journal.pone.0049012 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Aparicio A (2008) Descriptive analysis of the ‘relictual’ Mediterranean landscape in the Guadalquivir River valley (southern Spain): a baseline for scientific research and the development of conservation action plans. Biodivers Conserv 17:2219–2232. doi: 10.1007/s10531-007-9295-y CrossRefGoogle Scholar
  8. Broadhurst L (2015) Pollen dispersal in fragmented populations of the dioecious wind-pollinated tree, Allocasuarina verticillata (drooping sheoak, drooping she-oak; Allocasuarinaceae). PLoS One 10:e0119498. doi: 10.1371/journal.pone.0119498 CrossRefPubMedPubMedCentralGoogle Scholar
  9. Caves EM, Jennings SB, Hillerislambers J, Tewsbury JJ, Rogers HS (2013) Natural experiment demonstrates that bird loss leads to cessation of dispersal of native seeds from intact to degraded forests. PLoS One 8:e65618. doi: 10.1371/journal.pone.0065618 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chibicky IJ, Burczyk J (2009) Simultaneous estimation of null alleles and inbreeding coefficients. J Hered 100:106–113. doi: 10.1093/jhered/esn088 CrossRefGoogle Scholar
  11. Chung MG, Chung MY, Oh GS, Epperson BK (2000) Spatial genetic structure in a Neolitsea sericea population (Lauraceae). Heredity 85:490–497. doi: 10.1046/j.1365-2540.2000.00781.x CrossRefPubMedGoogle Scholar
  12. Cordeiro NJ, Howe HF (2003) Forest fragmentation severs mutualism between seed dispersers and an endemic African tree. Proc Natl Acad Sci U S A 100:14052–14056. doi: 10.1073/pnas.2331023100 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Crawford TJ (1984) The estimation of neighbourhood parameters for plant populations. Heredity 52:273–283. doi: 10.1038/hdy.1984.29 CrossRefGoogle Scholar
  14. de Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, Martins da Silva P, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. doi: 10.1007/s10531-010-9850-9 CrossRefGoogle Scholar
  15. Dick CW (2008) New interpretations of fine-scale spatial. Mol Ecol 17:1873–1874. doi: 10.1007/s12042-007-9006-6 CrossRefPubMedGoogle Scholar
  16. Ennos RA (1994) Estimating the relative rates of pollen and seed migration among plant populations. Heredity 72:250–259. doi: 10.1038/hdy.1994.35 CrossRefGoogle Scholar
  17. Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 10:564–567. doi: 10.1111/j.1755-0998.2010.02847.x CrossRefPubMedGoogle Scholar
  18. Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application. Genetics 131:479–491PubMedPubMedCentralGoogle Scholar
  19. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi: 10.1146/132419 CrossRefGoogle Scholar
  20. García C, Grivet D (2011) Molecular insights into seed dispersal mutualisms driving plant population recruitment. Acta Oecol 37:632–640. doi: 10.1016/j.actao.2011.04.009 CrossRefGoogle Scholar
  21. García D, Martínez D (2012) Species richness matters for the quality of ecosystem services: a test using seed dispersal by frugivorous birds. Proc R Soc Biol Sci 279:3106–3113. doi: 10.1098/rspb.2012.0175 CrossRefGoogle Scholar
  22. Godoy JA, Jordano P (2001) Seed dispersal by animals: exact identification of source trees with endocarp DNA microsatellites. Mol Ecol 10:2275–2283. doi: 10.1046/j.0962-1083.2001.01342.x CrossRefPubMedGoogle Scholar
  23. González-Varo JP, Albaladejo RG, Aparicio A (2008) Mating patterns and spatial distribution of conspecific neighbours in the Mediterranean shrub Myrtus communis (Myrtaceae). Plant Ecol 203:207–215. doi: 10.1007/s11258-008-9534-7 CrossRefGoogle Scholar
  24. Grivet D, Robledo-Arnuncio JJ, Smouse PE, Sork VL (2009) Relative contribution of contemporary pollen and seed dispersal to the effective parental size of seedling population of California valley oak (Quercus lobata, Née). Mol Ecol 18:3967–3979. doi: 10.1111/j.1365-294X.2009.04326.x CrossRefPubMedGoogle Scholar
  25. Hamilton MB (1999) Tropical tree gene flow and seed dispersal. Nature 401:8–9. doi: 10.1038/43597 CrossRefGoogle Scholar
  26. Hamrick J (2004) Response of forest trees to global environmental changes. For Ecol Manag 197:323–335. doi: 10.1016/j.foreco.2004.05.023 CrossRefGoogle Scholar
  27. Herrera CM (1984) A study of avian frugivores, bird-dispersed plants, and their interaction in Mediterranean scrublands. Ecol Monogr 54:1–23CrossRefGoogle Scholar
  28. Herrera CM (1995) Plant-vertebrate seed dispersal systems in the Mediterranean: ecological, evolutionary, and historical determinants. Annu Rev Ecol Syst 26:705–727CrossRefGoogle Scholar
  29. Herrera CM (1998) Population-level estimates of interannual variability in seed production: what do they actually tell us? Oikos 82:612–616. doi: 10.2307/3546384 CrossRefGoogle Scholar
  30. Irwin A, Hamrick JL, Godt MJW, Smouse PE (2003) A multiyear estimate of the effective pollen donor pool for Albizia julibrissin. Heredity 90:187–194. doi: 10.1038/sj.hdy.6800215 CrossRefPubMedGoogle Scholar
  31. Iwaizumi MG, TakahashI M, Isoda K, AusterlItz F (2013) Consecutive five-year analysis of paternal and maternal gene flow and contributions of gametic heterogeneities to overall genetic composition of dispersed seeds of Pinus densiflora (Pinaceae). Am J Bot 100:1896–1904. doi: 10.3732/ajb.1200563 CrossRefPubMedGoogle Scholar
  32. Jordano P (1988) Polinizacion y variabilidad de la produccion de semillas en Pistacia lentiscus L. Anales Jard Bot Madrid 45:2123–2231Google Scholar
  33. Jordano P (2007) Frugivores, seeds and genes: analysing the key elements of seed shadows. In Dennis AJ, Green RJ, Schupp EW (eds.) Seed Dispersal: Theory and its Application in a Chagings World 229–251.CABIGoogle Scholar
  34. Jordano P (2010) Pollen, seeds and genes: the movement ecology of plants. Heredity 105:329–330. doi: 10.1038/hdy.2010.28 CrossRefPubMedGoogle Scholar
  35. Karubian J, Durães R (2009) Effects of seed disperser social behavior on patterns of seed movement and deposition. Oecol Bras 13:45–57Google Scholar
  36. Koenig WD, Ashley MV (2003) Is pollen limited? The answer is blowin’ in the wind. Trends Ecol Evol 18:157–159. doi: 10.1016/S0169-5347(03)00034-X CrossRefGoogle Scholar
  37. Lowe AJ, Boshier D, Ward M, Bacles CFE, Navarro C (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273. doi: 10.1038/sj.hdy.6800725 CrossRefPubMedGoogle Scholar
  38. Lowe AJ, Cavers S, Boshier D, Breed MF, Hollingsworth PM (2015) The resilience of forest fragmentation genetics—no longer a paradox—we were just looking in the wrong place. Heredity 115:97–99. doi: 10.1038/hdy.2015.40 CrossRefPubMedPubMedCentralGoogle Scholar
  39. Lyles D, Rosenstock TS, Hastings A, Brown PH (2009) The role of large environmental noise in masting: general model and example from pistachio trees. J Theor Biol 259:701–713. doi: 10.1016/j.jtbi.2009.04.015 CrossRefPubMedGoogle Scholar
  40. Mezquida ET, Olano JM (2013) What makes a good neighborhood? Interaction of spatial scale and fruit density in the predator satiation dynamics of a masting juniper tree. Oecol 173:483–492. doi: 10.1007/s00442-013-2631-x CrossRefGoogle Scholar
  41. Nora S, Albaladejo RG, Aparicio A (2015) Genetic variation and structure in the Mediterranean shrubs Myrtus communis and Pistacia lentiscus in different landscape contexts. Plant Biol 17:311–319. doi: 10.1111/plb.12242 CrossRefPubMedGoogle Scholar
  42. Petit RJ, Hampe A (2006) Some evolutionary consequences of being a tree. Annu Rev Ecol Evol Syst 37:187–214CrossRefGoogle Scholar
  43. Rey PJ, Alcantara JM (2000) Recruitment dynamics of a fleshy-fruited plant (Olea europaea): connecting patterns of seed dispersal to seedling establishment. J Ecol 88:622–633. doi: 10.1046/j.1365-2745.2000.00472.x CrossRefGoogle Scholar
  44. Rey PJ, Alcantara JM (2013) Effects of habitat alteration on the effectiveness of plant-avian seed dispersal mutualisms: consequences for plant regeneration. Perspect Plant Ecol Evol Syst 16:21–31. doi: 10.1016/j.ppees.2013.11.001 CrossRefGoogle Scholar
  45. Robledo-Arnuncio JJ, Grivet D, Smouse PE, Sork VL (2012) PSA: software for parental structure analysis of seed or seedling patches. Mol Ecol Resour 12:1180–1189. doi: 10.1111/1755-0998.12005 CrossRefPubMedGoogle Scholar
  46. Robledo-Arnuncio JJ, Klein EK, Muller-Landau HC, Santamaría L (2014) Space, time and complexity in plant dispersal ecology. Mov Ecol 2:16. doi: 10.1186/s40462-014-0016-3 CrossRefPubMedPubMedCentralGoogle Scholar
  47. Saura S, Torné J (2009) Conefor Sensinode 2.2: a software package for quantifying the importance of habitat patches for landscape connectivity. Environ Model Softw 24:135–139. doi: 10.1016/j.envsoft.2008.05.005 CrossRefGoogle Scholar
  48. Schupp EW, Milleron T, Russo SE (2002) Dissemination limitation and the origin and maintenance of species-rich tropical forest. In: Levey DJ, Silva WR, Galetti M (eds) Seed dispersal and frugivory: ecology, evolution and conservation. CAB International, Wallingford, pp 19–23Google Scholar
  49. Sork VL, Smouse PE, Grivet D, Scofield DG (2015) Impact of asymmetric male and female gamete dispersal on allelic diversity and spatial genetic structure in valley oak (Quercus lobata Née). Evol Ecol 29:927–945. doi: 10.1007/s10682-015-9769-4 CrossRefGoogle Scholar
  50. Torimaru T, Tani N, Tsumura Y, Nishimura N, Tomaru N (2007) Effects of kin-structured seed dispersal on the genetics structure of the clonal dioecious shrub Ilex leucoclada. Evolution 61:1289–1300. doi: 10.1111/j.1558-5646.2007.00108.x CrossRefPubMedGoogle Scholar
  51. Uriarte M, Anciães M, Da Silva MT, Rubim P, Johnson E, Bruna EM (2011) Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape. Ecology 92:924–937. doi: 10.1890/10-0709.1 CrossRefPubMedGoogle Scholar
  52. Verdú M, García-Fayos P (1996) Nucleation process in a Mediterranean bird-dispersed plant. Funct Ecol 10:275–280. doi: 10.2307/2389853 CrossRefGoogle Scholar
  53. Verdú M, García-Fayos P (1998a) Ecological causes, function, and evolution of abortion and parthenocarpy in Pistacia lentiscus (Anacardiaceae). Can J Bot 76:134–141. doi: 10.1139/cjb-76-1-134 Google Scholar
  54. Verdú M, García-Fayos P (1998b) Female biased sex ratios in Pistacia lentiscus L. (Anacardiaceae). Plant Ecol 135:95–101. doi: 10.1023/A:1009764613803 CrossRefGoogle Scholar
  55. Young A, 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 CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Clara Parejo-Farnés
    • 1
  • Juan J. Robledo-Arnuncio
    • 2
  • Rafael G. Albaladejo
    • 1
  • Encarnación Rubio-Pérez
    • 1
  • Abelardo Aparicio
    • 1
  1. 1.Department of Biología Vegetal y EcologíaUniversidad de SevillaSevillaSpain
  2. 2.Department of Ecología y Genética Forestal, INIA-CIFORMadridSpain

Personalised recommendations