Skip to main content

Advertisement

SpringerLink
Log in

Are introduced plants a threat to native pollinator services in montane–alpine environments?

  • Original Article
  • Published:
Alpine Botany Aims and scope Submit manuscript

A Correction to this article was published on 28 June 2018

This article has been updated

Abstract

While introduced plants often have restricted distributions at high elevations, their impacts may be more extensive if they compete for native pollinators, potentially reducing pollinator services to native biotically pollinated plants. Conversely, introduced biotically pollinated plants might facilitate improved pollinator services to native plants by supporting higher pollinator densities and extending the flowering season. We examined weekly pollinator visitation to native and introduced plants, at five elevations over two flowering seasons on The Remarkables range, south-central South Island, New Zealand. In this area, introduced plants dominate the vegetation at lower elevations but are restricted to disturbed areas above treeline. We tested whether pollinator visitation rates and quantities of introduced pollen on insects or transferred to native flowers differed with elevation and community context, or with the local abundance of introduced flowers regardless of elevation. Introduced biotically pollinated plants produced more flowers and flowered later than most native species and were extensively utilised by native solitary bees. Weekly visitation rates to native flowers were higher in the first half of the flowering season than the second half, and were positively correlated with visitation rates to co-occurring introduced flowers. Introduced flower abundance did not affect visitation to native flowers but did significantly predict the occurrence of introduced pollen on native insects and stigmas of native flowers. Pollen contamination was also higher in the latter part of the flowering season. While an increase in introduced flowers at high elevations may benefit native pollinators by increasing the quantity and duration of floral resources available, the heavy use of introduced flowers by native bees will lead to at least localised stigma contamination, particularly for late flowering species. However, more information is required on foraging ranges of native pollinators and pollen limitation in native species to understand the consequences of introduced species expansion into alpine areas.

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

Similar content being viewed by others

Change history

  • 28 June 2018

    The Editor-in-Chief has retracted this article [1] because the three studies included in the meta-analysis [2,3 and 4] (cited as references 16, 17 and 18) have been retracted due to concerns regarding the data, which has rendered the results of this meta-analysis invalid.

References

  • Aizen MA, Morales CL, Morales JM (2008) Invasive mutualists erode native pollination webs. PLoS Biol 6:e31

    Article  CAS  Google Scholar 

  • Albrecht M, Schmid B, Hautier Y, Müller CB (2012) Diverse pollinator communities enhance plant reproductive success. Proc R Soc Lond B Biol 279:4845–4852

    Article  Google Scholar 

  • Albrecht M, Padrón B, Bartomeus I, Traveset A (2014) Consequences of plant invasions on compartmentalization and species’ roles in plant–pollinator networks. Proc R Soc B 281:20140773

    Article  Google Scholar 

  • Alexander JM, Lembrechts JJ, Cavieres LA, Dachler C, Haider S, Kueffer C, Liu G, McDougall K, Milbau A, Pauchard A, Rew LJ, Seipel T (2016) Plant invasions into mountains and alpine ecosystems: current status and future challenges. Alpine Bot 126:89–103

    Article  Google Scholar 

  • Arroyo MTK, Armesto JJ, Primack RB (1985) Community studies in pollination ecology in the high temperate Andes of central Chile II. Effect of temperature on visitation rates and pollination possibilities. Plant Syst Evol 149:187–203

    Article  Google Scholar 

  • Bartomeus I, Vilà M, Santamaría L (2008) Contrasting effects of invasive plants in plant–pollinator networks. Oecologia 155:761–770

    Article  Google Scholar 

  • Bergman P, Molau U, Holmgren B (1996) Micrometerological impacts on insect activity and plant reproductive success in an alpine environment, Swedish Lapland. Arct Alp Res 28:196–202

    Article  Google Scholar 

  • Bingham RA, Orthner AR (1998) Efficient pollination of alpine plants. Nature 391:238–239

    Article  Google Scholar 

  • Bischoff M (2008) Pollination ecology of the New Zealand alpine flora. Unpublished doctoral dissertation. University of Heidelberg, Heidelberg, Germany

  • Bischoff M, Campbell DR, Lord JM, Robertson AW (2013a) The relative importance of solitary bees and syrphid flies as pollinators of two outcrossing plant species in the New Zealand alpine. Austral Ecol 38: 169–176

    Article  Google Scholar 

  • Bischoff M, Lord JM, Robertson AW, Dyer AG (2013b) Hymenopteran pollinators as agents of selection on flower colour in the New Zealand alpine region: salient chromatic signals enhance flower discrimination. N Z J Bot 51:181–193

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Brown BJ, Mitchell RJ, Graham SA (2002) Competition for pollination between an invasive species (Purple Loosestrife) and a native congener. Ecology 83:2328–2336

    Article  Google Scholar 

  • Bruckman D, Campbell DR (2014) Floral neighborhood influences pollinator assemblages and effective pollination in a native plant. Oecologia 176:465–476

    Article  Google Scholar 

  • Buxton MN, Anderson BJ, Lord JM (2018) The secret service: analysis of the available knowledge on moths as pollinators in New Zealand. N Z J Ecol 42:1–9

    Google Scholar 

  • Campbell DR, Bischoff M, Lord JM, Robertson AW (2010) Flower colour influences insect visitation in alpine New Zealand. Ecology 91:2638–2649

    Article  Google Scholar 

  • Campbell DR, Bischoff M, Lord JM, Robertson AW (2012) Where have all the blue flowers gone? Pollinator responses and selection on flower colour in New Zealand Wahlenbergia albomarginata. J Evol Biol 25: 352–364

    Article  CAS  Google Scholar 

  • Chittka L, Schürkens S (2001) Successful invasion of a floral market. Nature 411:653

    Article  CAS  Google Scholar 

  • Dafni A (1992) Pollination ecology: a practical approach. Oxford University Press, Oxford

    Google Scholar 

  • Donovan BJ (2007) Fauna of New Zealand, Number 57: Apoidea (Insecta:Hymenoptera). Manaaki Whenua Press, Landcare Research, Lincoln

    Google Scholar 

  • Dorado J, Vázquez DP (2014) The diversity–stability relationship in floral production. Oikos 123:1137–1143

    Article  Google Scholar 

  • Esler AE, Astridge SJ (1986) The naturalisation of plants in urban Auckland, New Zealand 2. Records of introduction and naturalisation. NZ J Botany 25:523–537

    Article  Google Scholar 

  • Fontaine C, Collin CL, Dajoz I (2008) Generalist foraging of pollinators: diet expansion at high density. J Ecol 96:1002–1010

    Article  Google Scholar 

  • García-Camacho R, Totland Ø (2009) Pollen limitation in the alpine: a meta-analysis. Arct Antarct Alp Res 41(1):103–111

    Article  Google Scholar 

  • Ghazoul J (2006) Floral diversity and the facilitation of pollination. J Ecol 94:295–304

    Article  Google Scholar 

  • Gómez JM, Abdelaziz M, Lorite J, Muñoz-Pajares AJ, Perfectti F (2010) Changes in pollinator fauna cause spatial variation in pollen limitation. J Ecol 98:1243–1252

    Article  Google Scholar 

  • Goodell K, Parker IM (2017) Invasion of a dominant floral resource: effects on the floral community and pollination of native plants. Ecology 98:57–69

    Article  Google Scholar 

  • Graves SD, Shapiro AM (2003) Exotics as host plants for the Californian butterfly fauna. Biol Conserv 110:413–433

    Article  Google Scholar 

  • Halloy SRP, Mark AF (2003) Climate-change effects on alpine plant biodiversity: a New Zealand perspective on quantifying threats. Arct Antarct Alp Res 35:248–254

    Article  Google Scholar 

  • Hirao AS, Kameyama Y, Ohara Y, Isagi Y, Kudo G (2006) Seasonal changes in pollinator activity influence pollen dispersal and seed production of the alpine shrub Rhododendron aureum (Ericaceae). Mol Ecol 15:1165–1173

    Article  CAS  Google Scholar 

  • Iler AM, Goodell K (2014) Relative floral density of an invasive plant affects pollinator foraging behaviour on a native plant. J Poll Ecol 13: 174–183

    Google Scholar 

  • Iwasaki JM, Dickinson KJM, Barratt BIP, Mercer AR, Jowett TWD, Lord JM (2018) Floral usage partitioning and competition between social (Apis mellifera, Bombus terrestris) and solitary bees in New Zealand: niche partitioning via floral preferences? Austral Ecol Rev (in review)

  • Jakobsson A, Padrón B, Traveset A (2008) Pollen transfer from invasive Carpobrotus spp. to natives—a study of pollinator behaviour and reproduction success. Biol Conserv 141: 136–145

    Article  Google Scholar 

  • Johnston F, Pickering C (2001) Alien plants in the Australian Alps. Mt Res Devel 21:284–291

    Article  Google Scholar 

  • Körner C (2003) Alpine plant life. Springer, Berlin

    Book  Google Scholar 

  • Lázaro A, Lundgren R, Totland Ø (2009) Co-flowering neighbors influence the diversity and identity of pollinator groups visiting plant species. Oikos 118:691–702

    Article  Google Scholar 

  • Lembrechts JJ, Pauchard A, Lenoir J, Nuñez MA, Geron C, Ven A, Bravo-Monasterio P, Teneb E, Nijs I, Milbau A (2016) Disturbance is the key to plant invasions in cold environments. Proc Nat Acad Sci USA 113:14061–14066

    Article  CAS  Google Scholar 

  • Lloyd DG (1985) Progress in understanding the natural history of New Zealand plants. N Z J Bot 23:707–722

    Article  Google Scholar 

  • Lopezaraiza-Mikel ME, Hayes RB, Whalley MR, Memmott J (2007) The impact of an alien plant on a native plant–pollinator network: an experimental approach. Ecol Lett 10:539–550

    Article  Google Scholar 

  • Mark AF (2012) Above the treeline. Craig Potton Publishing, Nelson

    Google Scholar 

  • Mark AF, Dickindon KJM, Hofstede RGM (2000) Alpine vegetation, plant distribution, life forms, and environments in a perhumid New Zealand region: oceanic and tropical high mountain affinities. Arct Antarct Alp Res 32:240–254

    Article  Google Scholar 

  • Masters JA, Emery SM (2015) The showy invasive plant Ranunculus ficaria facilitates pollinator activity, pollen deposition, but not always seed production for two native spring ephemeral plants. Biol Invasions 17:2329–2337

    Article  Google Scholar 

  • McDougall KL, Morgan JW, Walsh NG, Williams RJ (2005) Plant invasions in treeless vegetation of the Australian Alps. Perspect Plant Ecol Evol Syst 7:159–171

    Article  Google Scholar 

  • McGimpsey V, Lord JM (2015) In a world of white, flower colour matters: a white-purple transition signals lack of reward in an alpine Euphrasia Austral Ecol 40:701–708

    Article  Google Scholar 

  • Memmott J, Waser NM (2002) Integration of alien plants into a native flower-pollinator visitation web. Proc R Soc B Biol Sci 269(1508):2395–2399

    Article  Google Scholar 

  • Miller CM (2015) The impact of introduced flowering species on alpine plant–pollinator networks in southern New Zealand. Unpublished Ph.D. dissertation, University of Otago, New Zealand

  • Mitchell RJ, Flanagan RJ, Brown BJ, Waser NM, Karron JD (2009) New frontiers in competition for pollination. Ann Bot 103:1403–1413

    Article  Google Scholar 

  • Moar NT (1993) Pollen grains of New Zealand dicotyledonous plants. Manaaki Whenua Press, Lincoln

    Google Scholar 

  • Montero-Castaño A, Vilá M (2012) Impact of landscape alteration and invasions on pollinators: a meta-analysis. J Ecol 100:884–893

    Article  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  Google Scholar 

  • Muñoz AA, Cavieres LA (2008) The presence of a showy invasive plant disrupts pollinator service and reproductive output in native alpine species only at high densities. J Ecol 96: 459–467

    Article  Google Scholar 

  • Newstrom L, Robertson A (2005) Progress in understanding pollination systems in New Zealand. N Z J Bot 43:1–59

    Article  Google Scholar 

  • Olesen JM, Jordano P (2002) Geographic patterns in plant–pollinator mutualistic networks. Ecology 83:2416–2424

    Google Scholar 

  • Ollerton J, Winfree R, Tarrant S (2011) How many flowering plants are pollinated by animals? Oikos 120:321–326

    Article  Google Scholar 

  • Patrick B, Patrick H (2012) Butterflies of the South Pacific. Otago University Press, Dunedin

    Google Scholar 

  • Pauchard A, Kueffer C, Dietz H, Daehler CC, Alexander J, Edwards PJ, Arévalo JR, Cavieres LA, Guisan A, Haider S, Jakobs G, McDougall K, Millar CI, Naylor BJ, Parks CG, Rew LJ, Seipel T (2009) Ain’t no mountain high enough: plant invasions reaching high elevations. Front Ecol Environ 7:479–486

    Article  Google Scholar 

  • Petitpierre B, McDougall K, Siepel T, Broennimann O, Guisan A, Kueffer C (2016) Will climate change increase the risk of plant invasions into mountains? Ecol Appl 26:530–544

    Article  Google Scholar 

  • Pleasants JM (1983) Structure of plant and pollinator communities. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold Company, New York, pp 375–393

    Google Scholar 

  • Primack RB (1978) Variability in New Zealand montane and alpine pollinator assemblages. N Z J Ecol 1:66–73

    Google Scholar 

  • Primack RB (1983) Insect pollination in New Zealand mountain flora. N Z J Bot 21: 317–333

    Article  Google Scholar 

  • Pyšek P, Jarošik V, Chytrý Danihelka J, Kühn I, Pergl J, Tichý L, Biesmeijer JC, Ellis WN, Kunin WE, Settele J (2011) Successful invaders co-opt pollinators of native flora and accumulate insect pollinators with increasing residence time. Ecol Monogr 81:277–293

    Article  Google Scholar 

  • Sawrey O (2013) Effect of altitude and co-occurring species on sequential reproductive stages in a grassland harebell. New Zealand. Unpublished M.Sc. Dissertation, University of Otago, New Zealand

  • Sullivan JJ, Williams PA, Timmins SM, Smale MC (2009) Distribution and spread of environmental weeds along New Zealand roadsides. N Z J Ecol 33:190–204

    Google Scholar 

  • Tiedeken EJ, Stout JC (2015) Insect–flower interaction network structure is resilient to a temporary pulse of floral resources from invasive Rhododendron ponticum. PLOS ONE 10(3):e0119733

    Article  CAS  Google Scholar 

  • Tomb AS (1975) Pollen morphology in Tribe Lactuceae (Compositae). Grana 15:79–89

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Trunschke J, Stöcklin J (2017) Plasticity of flower longevity in alpine plants is increased in populations from high elevation compared to low elevation populations. Alpine Bot 127:41–51

    Article  Google Scholar 

  • Vilà M, Bartomeus I, Dietzsch AC, Petanidou T, Steffan-Dewenter I, Stout JC, Tscheulin T (2009) Invasive plant integration into native plant–pollinator networks across Europe. Proc R Soc B 276:3887–3893

    Article  Google Scholar 

  • Waters SM, Fisher SE, Hille Ris Lambers J (2014) Neighborhood-contingent indirect interactions between native and exotic plants: multiple shared pollinators mediate reproductive success during invasions. Oikos 123: 433–440

    Article  Google Scholar 

  • Wilton AD, Brietwiesser I (2000) Composition of the New Zealand seed plant flora. N Z J Bot 38: 537–549

    Article  Google Scholar 

  • Wratten SD, White AJ, Bowie MH, Berry NA, Weigmann U (1995) Phenology and ecology of hoverflies (Diptera, Syrphidae) in New-Zealand. Environ Entomol 24:595–600

    Article  Google Scholar 

  • Zefferman E, Stevens JT, Charles GK, Dunbar-Irwin M, Emam T, Fick S, Morales LV, Wolf KM, Young DJ, Young TP (2015) Plant communities in harsh sites are less invaded: a summary of observations and proposed explanations. AoB Plants 22:7

    Google Scholar 

Download references

Acknowledgements

Thanks to Vickey Tomlinson for assistance with equipment, Jeanne Hutchinson, Olivia Sawrey and Dana Dudle for assistance in the field and Barry Donovan, John Dugdale, Brian Patrick and Dave Voice for insect identifications. We also appreciate the valuable contributions of two anonymous reviewers.

Funding

CM was supported by a University of Otago PhD scholarship and a Brenda Shore Award (New Zealand Federation of Graduate Women), with additional funding from the Miss E. L. Hellaby Indigenous Grasslands Research Trust.

Author information

Authors and Affiliations

  1. Department of Botany, University of Otago, Dunedin, New Zealand

    Christa M. Miller, Barbara I. P. Barratt, Katharine J. M. Dickinson & Janice M. Lord

  2. AgResearch, Invermay Agricultural Centre, Mosgiel, New Zealand

    Barbara I. P. Barratt

Authors
  1. Christa M. Miller
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Barbara I. P. Barratt
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Katharine J. M. Dickinson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Janice M. Lord
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

All authors contributed to study design, CM conducted experiments and wrote the first draft, JML led subsequent writing and analysis, all authors commented on final manuscript.

Corresponding author

Correspondence to Janice M. Lord.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Work in the Rastus Burn Recreational Reserve was conducted under a Department of Conservation research permit. Ngāi Tahu (traditional land owners) were consulted prior to the commencement of the study through the University of Otago Ngāi Tahu Research Consultation committee.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 47 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Miller, C.M., Barratt, B.I.P., Dickinson, K.J.M. et al. Are introduced plants a threat to native pollinator services in montane–alpine environments?. Alp Botany 128, 179–189 (2018). https://doi.org/10.1007/s00035-018-0206-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00035-018-0206-5

Keywords

Search

Navigation