Skip to main content

Advertisement

SpringerLink
Log in

Invasive conifers reduce seed set of a native Andean cedar through heterospecific pollination competition

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

The invasion of natural forest communities by introduced woody species may threat processes that are critical for ecosystem integrity, including plant pollination and reproduction. In particular, invasive conifers (e.g., Pseudotsuga menziesii, Pinus spp.) escaped from forest plantations may impair seed production of anemophilous native conifers by altering the dynamics of wind-borne pollen flow among trees. In this study, we analyzed the effects of invasive conifers on the pollination and sexual reproduction of Andean cedar (Austrocedrus chilensis), a dioecious conifer native to the temperate forests of southern South America. Wind-dispersed pollen captured in pollen traps revealed that the timing of pollen release between the invasive and native conifers overlapped extensively, and the pollen cloud surrounding female cedar trees in invaded forest was heavily contaminated with pollen from the invasive conifers. Increasing abundance of invasive conifers in the proximity of female cedars decreased the local density of air-borne cedar pollen and increased contamination of the pollen cloud with pollen from the invasive conifers. This increased the chance of finding heterospecific pollen from these invaders in the micropyles of the native cedar. In turn, the presence of pollen grains from invasive conifers, particularly of P. menziesii, in the cedar’s micropyles was associated with a strong increase in the percentage of seed abortion. Our results clearly support the hypothesis that invasive conifers can interfere with the pollination and sexual reproduction of native wind-pollinated conifers. Thus, plantations of introduced and highly invasive conifers should not occur in the proximity of stands of native conifers in order to guarantee their reproduction and long-term population viability.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aizen MA, Harder LD (2007) Expanding the limits of the pollen-limitation concept: effects of pollen quantity and quality. Ecology 88:271–281

    Article  PubMed  Google Scholar 

  • Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122

    CAS  PubMed  Google Scholar 

  • Arbuckle JL (2003) AMOS 5.0 uppdate to the AMOS user’s guide. Chicago, Illinois, USA

  • Augspurger CK (1983) Phenology, flowering synchrony, and fruit set of six neotropical shrubs. Biotropica 15:257–267

    Article  Google Scholar 

  • Bacles CFE, Ennos RA (2008) Paternity analysis of pollen-mediated gene flow for Fraxinus excelsior L. in a chronically fragmented landscape. Heredity 101:368–380

    Article  CAS  PubMed  Google Scholar 

  • Bell JM, Karron JD, Mitchell RJ (2005) Interspecific competition for pollination lowers seed production and outcrossing in Mimulus ringens. Ecology 86:762–771

    Article  Google Scholar 

  • Bjerknes AL, Totland Ø, Hegland SJ et al (2007) Do alien plant invasions really affect pollination success in native plant species? Biol Conserv 138:1–12

    Article  Google Scholar 

  • Bloom AJ, Chapin Iii FS, Mooney HA (1985) Resource limitation in plants—an economic analogy. Annu Rev Ecol Syst 16:363–392

    Google Scholar 

  • Bran D, Pérez A, Barrios D et al (2002) Eco-región Valdiviana: distribución actual de los bosques de “Ciprés de la Cordillera” (Austrocedrus chilensis) – Escala 1:250.000. INTA – Administración de Parques Nacionales – Fundación Vida Silvestre Argentina Bariloche

  • Brion C, Grigera D, Rosso P (1993) The reproduction of Austrocedrus chilensis (D. Don) Florin etBoutleje. Comp R Acad Sci Paris 316:721–724

  • Brown BJ, Mitchell RJ (2001) Competition for pollination: effects of pollen of an invasive plant on seed set of a native congener. Oecologia 129:43–49

    Article  Google Scholar 

  • Buonaccorsi JP, Elkinton J, Koenig W et al (2003) Measuring mast seeding behavior: relationships among population variation, individual variation and synchrony. J Theor Biol 224:107–114

    Article  PubMed  Google Scholar 

  • Burgess KS, Morgan M, Husband BC (2008) Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytol 177:276–283

    PubMed  Google Scholar 

  • Burkle LA, Alarcon R (2011) The future of plant-pollinator diversity: understanding interaction networks across time, space, and global change. Am J Bot 98:528–538

    Article  PubMed  Google Scholar 

  • Campoe OC, Stape JL, Nouvellon Y et al (2013) Stem production, light absorption and light use efficiency between dominant and non-dominant trees of Eucalyptus grandis across a productivity gradient in Brazil. For Ecol Manag 288:14–20

    Article  Google Scholar 

  • Castor C, Cuevas JG, Kalin Arroyo MT et al (1996) Austrocedrus chilensis (D. Don) Pic.- Ser. Et. Bizz (Cupressaceae) from Chile and Argentina: monoecious or dioecious? Rev Chil Hist Nat 69:89–95

    Google Scholar 

  • CONAF (1999) Catastro y evaluación de recursos vegetacionales nativos de Chile. Informe regional IX Región. CONAF-CONAMA-BIRF, Santiago

    Google Scholar 

  • Currier HB, Strugger S (1956) Aniline blue and fluorescence microscopy of callose in bulb scales of Allium cepa L. Protoplasma 45:552–559

    Article  Google Scholar 

  • Daniels RF, Burkhart HE, Clason TR (1986) A comparison of competition measures for predicting growth of loblolly pine trees. Can J For Res 16:1230–1237

    Article  Google Scholar 

  • Dietzsch AC, Stanley DA, Stout JC (2011) Relative abundance of an invasive alien plant affects native pollination processes. Oecologia 167:469–479

    Article  PubMed  Google Scholar 

  • Friedman J, Barrett SC (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann Bot 103:1515–1527

    Article  PubMed Central  PubMed  Google Scholar 

  • Gonzalez-Varo JP, Biesmeijer JC, Bommarco R et al (2013) Combined effects of global change pressures on animal-mediated pollination. Trends Ecol Evol 28:524–530

    Article  PubMed  Google Scholar 

  • Gray AN, Spies TA, Pabst RJ (2012) Canopy gaps affect long-term patterns of tree growth and mortality in mature and old-growth forests in the Pacific Northwest. For Ecol Manag 281:111–120

    Article  Google Scholar 

  • Greene DF, Messier C, Asselin H et al (2002) The effect of light availability and basal area on cone production in Abies balsamea and Picea glauca. Can J Bot 80:370–377

    Article  Google Scholar 

  • Hu LT, Bentler PM (1999) Cutoff criteria for fit indexes in covariance structure analysis: conventional criteria versus new alternatives. Struct Equ Model 6:1–55

    Article  Google Scholar 

  • Kelly D, Sork VL (2002) Mast seeding in perennial plants: why, how, where? Annu Rev Ecol Syst 33:427–447

    Article  Google Scholar 

  • Koenig WD, Ashley MV (2003) Is pollen limited? The answer is blowin’ in the wind. Trends Ecol Evol 18:157–159

    Article  Google Scholar 

  • Matsumoto T, Takakura KI, Nishida T (2010) Alien pollen grains interfere with the reproductive success of native congener. Biol Invasions 12:1617–1626

    Article  Google Scholar 

  • McKinney AM, Goodell K (2010) Shading by invasive shrub reduces seed production and pollinator services in a native herb. Biol Invasions 12:2751–2763

    Article  Google Scholar 

  • Millerón M, López de Heredia U, Lorenzo Z et al (2012) Effect of canopy closure on pollen dispersal in a wind-pollinated species (Fagus sylvatica L.). Plant Ecol 213:1715–1728

    Article  Google Scholar 

  • Mitchell RJ, Flanagan RJ, Brown BJ et al (2009) New frontiers in competition for pollination. Ann Bot (Lond) 103:1403–1413

    Article  Google Scholar 

  • Morales CL, Traveset A (2008) Interspecific pollen transfer: magnitude, prevalence and consequences for plant fitness. Crit Rev Plant Sci 27:221–238

    Article  CAS  Google Scholar 

  • Morales CL, Traveset A (2009) A meta-analysis of impacts of alien vs. native plants on pollinator visitation and reproductive success of co-flowering native plants. Ecol Lett 12:716–728

    Article  PubMed  Google Scholar 

  • Niesenbaum RA (1993) Light or pollen—seasonal limitations on female reproductive success in the understory shrub Lindera benzoin. J Ecol 81:315–323

    Article  Google Scholar 

  • Nishida S, Takakura KI, Nishida T et al (2012) Differential effects of reproductive interference by an alien congener on native Taraxacum species. Biol Invasions 14:439–447

    Article  Google Scholar 

  • Oostermeijer JGB, De Knegt B (2004) Genetic population structure of the wind-pollinated, dioecious shrub Juniperus communis in fragmented Dutch heathlands. Plant Species Biol 19:175–184

    Article  Google Scholar 

  • Pastorino MJ, Gallo LA (2002) Quaternary evolutionary history of Austrocedrus chilensis, a cypress native to the Andean-Patagonian forest. J Biogeogr 29:1167–1178

    Article  Google Scholar 

  • Pastorino MJ, Gallo LA (2009) Preliminary operational genetic management units of a highly fragmented forest tree species of southern South America. For Ecol Manag 257:2350–2358

    Article  Google Scholar 

  • Piotti A, Leonardi S, Buiteveld J et al (2012) Comparison of pollen gene flow among four European beech (Fagus sylvatica L.) populations characterized by different management regimes. Heredity 108:322–331

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rangel TFLVB, Diniz-Filho JAF, Bini LM (2010) SAM: a comprehensive application for spatial analysis in macroecology. Ecography 33:46–50

    Article  Google Scholar 

  • Richardson DM, Pyšek P (2012) Naturalization of introduced plants: ecological drivers of biogeographical patterns. New Phytol 196:383–396

    Article  PubMed  Google Scholar 

  • Rovere A (1991) Estudio experimental de germinación y desarrollo temprano del ciprés de la cordillera (Austrocedrus chilensis). Universidad Nacional del Comahue, pp 79

  • Sarasola MM, Rusch VE, Schlichter TM et al (2006) Tree conifers invasion in steppe areas and Austrocedus chilensis forests in NW Patagonia. Ecol Austral 16:143–156

    Google Scholar 

  • Schumacker R, Lomax R (2004) A beginner’s guide to structural equation modeling. Lawrence Erlbaum Associates, Mahwah

    Google Scholar 

  • Shipley B (1997) Exploratory path analysis with applications in ecology and evolution. Am Nat 149:1113–1138

    Article  CAS  PubMed  Google Scholar 

  • Simberloff D, Nuñez MA, Ledgard NJ et al (2010) Spread and impact of introduced conifers in South America: lessons from other southern hemisphere regions. Austral Ecol 35:489–504

    Article  Google Scholar 

  • Souto C, Gardner M (2013) Austrocedrus chilensis. IUCN Red List Threatened Species. Version 2013.2

  • Suhr DD (2006) Exploratory or confirmatory factor analysis? Thirty-first annual SAS® users group international conference. SAS Institute Inc., Cary, NC, San Francisco, CA, USA

  • Sullivan JJ, Timmins SM, Williams PA (2005) Movement of exotic plants into coastal native forests from gardens in northern New Zealand. N Z J Ecol 29:1–10

    Google Scholar 

  • Tercero-Bucardo N, Kitzberger T, Veblen TT et al (2007) A field experiment on climatic and herbivore impacts on post-fire tree regeneration in north-western Patagonia. J Ecol 95:771–779

    Article  Google Scholar 

  • Tomé M, Burkhart HE (1989) Distance dependent competition measures for predicting growth of individual trees. Forensic Sci Int 35:816–831

    Google Scholar 

  • Traveset A, Richardson DM (2006) Biological invasions as disruptors of plant reproductive mutualisms. Trends Ecol Evol 21:208–216

    Article  PubMed  Google Scholar 

  • Van Wilgen BW, Richardson DM (2012) Three centuries of managing introduced conifers in South Africa: benefits, impacts, changing perceptions and conflict resolution. J Environ Manag 106:56–68

    Article  Google Scholar 

  • Vilà M, Basnou C, Pyšek P et al (2010) How well do we understand the impacts of alien species on ecosystem services? A pan-European, cross-taxa assessment. Front Ecol Environ 8:135–144

    Article  Google Scholar 

  • Vitousek PM, D’Antonio CM, Loope LL et al (1996) Biological invasions as global environmental change. Am Sci 84:468–478

    Google Scholar 

  • Waser NM (1978) Interspecific pollen transfer and competition between co-occuring plant species. Oecologia 36:223–236

    Article  Google Scholar 

  • Zenkteler M, Relska-Roszak D (2003) Bidirectional pollination of angiosperm and gymnosperm ovules. Acta Biol Crac Ser Bot 45:77–81

    Google Scholar 

Download references

Acknowledgments

We thank Alejandro Martyniuk for his assistance with the field experiments and companionship during sampling. Also we thank to Martin Nuñez and two anonymous reviewers for valuable comments and thoughtful input on a previous version of the MS, and the Delegación Regional Patagonia of the Administración Parques Nacionales (APN) for granting permission to collect material for this study. This study was partially funded by a grant to N.M. provided under the agreement for technical and scientific cooperation between the Universidad Nacional del Comahue and APN, the Universidad Nacional de la Patagonia San Juan Bosco (PI No. 560), the Centro de Investigación y Extensión Forestal Andino Patagónico, and the Agencia Nacional de Promoción Científica y Tecnológica (PICTO Forestal No. 36879).

Author information

Authors and Affiliations

  1. Laboratorio ECOTONO - Centro Regional Universitario Bariloche (CRUB), Universidad Nacional del Comahue and Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), Quintral 1250, 8400, San Carlos de Bariloche, Río Negro, Argentina

    Nicolás A. Martyniuk, Carolina L. Morales & Marcelo A. Aizen

Authors
  1. Nicolás A. Martyniuk
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carolina L. Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Marcelo A. Aizen
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nicolás A. Martyniuk.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 2101 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martyniuk, N.A., Morales, C.L. & Aizen, M.A. Invasive conifers reduce seed set of a native Andean cedar through heterospecific pollination competition. Biol Invasions 17, 1055–1067 (2015). https://doi.org/10.1007/s10530-014-0775-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-014-0775-1

Keywords

Search

Navigation