Skip to main content

Advertisement

SpringerLink
Log in

Plant origin and fruit traits shape fruit removal patterns by native birds in invaded plant communities

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

Abstract

Biotic interactions and mutualisms in particular have an important role in ecosystem structure and functioning as well as in the maintenance of biodiversity. Understanding how communities respond to the introduction of non-native species and what determines the establishment of novel interactions between native and introduced species will help in determining the potential impacts of biological invasions. The aims of this work were to assess patterns of frugivory and fruit removal in environments with invasion of non-native fleshy-fruited plants and to evaluate whether novel associations between native frugivores and non-native plants are determined by fruit traits. For this we selected eight study sites in areas with different degrees of invasion of non-native fleshy-fruited plants. In each site, we measured fruit availability and fruit traits of native and non-native plants. In addition, we conducted direct frugivory observations. We found that native and non-native fruits differed based on morphological trait variables, such as fruit weight and dimensions. Only two birds, Elaenia albiceps (smaller and migrant) and Turdus falcklandii (bigger and resident), are the main frugivorous present in the area. At the scale of the community of frugivores, neither visit nor fruit removal rates differ between natives and non-natives. However, at the species scale, while E. albiceps preferentially foraged on native plants, T. falcklandii preferred non-natives. Thus, some generalist frugivorous species like T. falcklandii can play a key role in promoting the invasion of non-native plants.

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, Ezcurra C (1998) High incidence of plant–animal mutualisms in the woody flora of the temperate forest of southern South America: biogeographical origin and present ecological significance. Ecol Austral 8:217–236

    Google Scholar 

  • Aizen MA, Vázquez DP, Smith-Ramírez C (2002) Historia natural y conservación de los mutualismos planta-animal del bosque templado de Sudamerica austral. Rev Chil Hist Nat 75:79–97

    Google Scholar 

  • Amico GC, Aizen MA (2005) Dispersión de semillas por aves en un bosque templado de Sudamérica austral: ¿quién dispersa a quién? Ecol Austral 15:89–100

    Google Scholar 

  • Amico GC, Rodríguez-Cabal MA, Aizen MA (2009) The potential key seed-dispersing role of the arboreal marsupial Dromiciops gliroides. Acta Oecol 35:8–13

    Google Scholar 

  • Amodeo MR, Zalba SM (2013) Wild cherries invading natural grasslands: unraveling colonization history from population structure and spatial patterns. Plant Ecol 214:1299–1307

    Google Scholar 

  • Armesto JJ, Rozzi R (1989) Seed dispersal syndromes in the rain forest of Chiloé: evidence for the importance of biotic dispersal in a temperate rain forest. J Biogeogr 16:219–226

    Google Scholar 

  • Aslan C, Rejmanek M (2012) Native fruit traits may mediate dispersal competition between native and non-native plants. NeoBiota 12:1–24

    Google Scholar 

  • Baret S, Maurice S, Le Bourgeois T, Strasberg D (2004) Altitudinal variation in fertility and vegetative growth in the invasive plant Rubus alceifolius Poiret (Rosaceae), on Réunion island. Plant Ecol 172:265–273

    Google Scholar 

  • Bartuszevige AM, Gorchov DL (2006) Avian seed dispersal of an invasive shrub. Biol Invasions 8:1013–1022

    Google Scholar 

  • Bascompte J, Jordano P (2014) Mutualistic networks. Princeton University Press, Princeton

    Google Scholar 

  • Bascompte J, Jordano P, Melian CJ, Olesen JM (2003) The nested assembly of plant–animal mutualistic networks. Proc Natl Acad Sci 100:9383–9387

    CAS  PubMed  Google Scholar 

  • Bascompte J, Jordano P, Olesen JM (2006) Asymmetric coevolutionary networks facilitate biodiversity maintenance. Science 312:431–433

    CAS  PubMed  Google Scholar 

  • Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Google Scholar 

  • Bitani N, Ehlers Smith DA, Ehlers Smith YC, Downs CT (2020) Functional traits vary among fleshy-fruited invasive plant species and their potential avian dispersers. Acta Oecol 108:103651

    Google Scholar 

  • Blendinger PG, Martín E, Osinaga Acosta O et al (2016) Fruit selection by Andean forest birds: influence of fruit functional traits and their temporal variation. Biotropica 48:677–686

    Google Scholar 

  • Bravo SP, Berrondo MO, Cueto VR (2019) Are small abandoned plantations a threat for protected areas in Andean forests? The potential invasion of non-native cultivated species. Acta Oecol 95:128–134

    Google Scholar 

  • Buckley YM, Anderson S, Catterall CP et al (2006) Management of plant invasions mediated by frugivore interactions. J Appl Ecol 43:848–857

    Google Scholar 

  • Burns KC (2012) Are introduced birds unimportant mutualists? A case study of frugivory in European blackbirds (Turdus merula). N Z J Ecol 36:171–176

    Google Scholar 

  • Burns KC (2013) What causes size coupling in fruit-frugivore interaction webs? Ecology 94:295–300

    CAS  PubMed  Google Scholar 

  • Deckers B, Verheyen K, Vanhellemont M et al (2008) Impact of avian frugivores on dispersal and recruitment of the invasive Prunus serotina in an agricultural landscape. Biol Invasions 10:717–727

    Google Scholar 

  • Díaz Vélez MC, Sérsic AN, Traveset A, Paiaro V (2018) The role of frugivorous birds in fruit removal and seed germination of the invasive alien Cotoneaster franchetii in central Argentina. Austral Ecol 43:558–566

    Google Scholar 

  • Donatti CI, Guimarães PR, Galetti M et al (2011) Analysis of a hyper-diverse seed dispersal network: modularity and underlying mechanisms. Ecol Lett 14:773–781

    PubMed  Google Scholar 

  • Dormann CF, Gruber B, Fründ J (2008) Introducing the bipartite package: analysing ecological networks. R News 8:8–11

    Google Scholar 

  • García D, Zamora R, Amico GC (2010) Birds as suppliers of seed dispersal in temperate ecosystems: conservation guidelines from real-world landscapes. Conserv Biol 24:1070–1079

    PubMed  Google Scholar 

  • García D, Martínez D, Stouffer DB, Tylianakis JM (2014) Exotic birds increase generalization and compensate for native bird decline in plant–frugivore assemblages. J Anim Ecol 83: 1441–1450

    PubMed  Google Scholar 

  • Gleditsch JM, Carlo TA (2014) Living with aliens: effects of invasive shrub honeysuckles on avian nesting. PLoS One 9:e107120

    PubMed  PubMed Central  Google Scholar 

  • González-Castro A, Yang S, Nogales M, Carlo TA (2015) Relative importance of phenotypic trait matching and species’ abundances in determining plant—avian seed dispersal interactions in a small insular community. AoB Plants 7:017

    PubMed  PubMed Central  Google Scholar 

  • Gosper CR, Vivian-Smith G (2010) Fruit traits of vertebrate-dispersed alien plants: smaller seeds and more pulp sugar than indigenous species. Biol Invasions 12:2153–2163

    Google Scholar 

  • Gosper CR, Stansbury CD, Vivian-Smith G (2005) Seed dispersal of fleshy-fruited invasive plants by birds: contributing factors and management options. Divers Distrib 11:549–558

    Google Scholar 

  • Heleno RH, Olesen JM, Nogales M, Vargas P, Traveset A (2013) Seed dispersal networks in the Galápagos and the consequences of alien plant invasions. Proc R Soc B 280: 20122112

    PubMed  Google Scholar 

  • Hervé M (2018) RVAideMemoire: testing and plotting procedures for biostatistics

  • Iglesias A (2015) Dinámica de invasión de plantas con frutos carnosos dispersadas por aves en el noroeste de la Patagonia. Dissertation, Universidad Nacional del Comahue

  • Jordaan LA, Johnson SD, Downs CT (2011) The role of avian frugivores in germination of seeds of fleshy-fruited invasive alien plants. Biol Invasions 13:1917–1930

    Google Scholar 

  • Jordano P (1995) Angiosperm fleshy fruits and seed dispersers: a comparative analysis of adaptation and constraints in plant–animal interactions. Am Nat 145:163

    Google Scholar 

  • Kassambara A, Mundt F (2017) Package factoextra: extract and visualize the results of multivariate data analyses

  • Kitamura S, Yumoto T, Poonswad P et al (2002) Interactions between fleshy fruits and frugivores in a tropical seasonal forest in Thailand. Oecologia 133:559–572

    PubMed  Google Scholar 

  • Kueffer C, Kronauer L, Edwards PJ (2009) Wider spectrum of fruit traits in invasive than native floras may increase the vulnerability of oceanic islands to plant invasions. Oikos 118:1327–1133

    CAS  Google Scholar 

  • Lediuk K, Damascos MA, Puntieri JJ, Svriz M (2014) Differences in phenology and fruit characteristic between invasive and native woody species favor exotic species invasiveness. Plant Ecol 215:1455–1467

    Google Scholar 

  • Lediuk K, Damascos MA, Puntieri JJ, de Torres Curth MI (2016) Population dynamics of an invasive tree, Sorbus aucuparia, in the understory of a Patagonian forest. Plant Ecol 217:899–911

    Google Scholar 

  • Martin-Albarracin VL, Amico GC, Nuñez MA (2017) The introduced silver pheasant Lophura nycthemera (Phasianidae) in Isla Victoria, Patagonia Argentina: abundance, group structure, activity patterns and association to anthropic disturbance. El Hornero 32:227–236

    Google Scholar 

  • Martin-Albarracin VL, Nuñez MA, Amico GC (2018) Non-redundancy in seed dispersal by native and introduced frugivorous birds: implications for invasive bird impact on native plant communities. Biodivers Conserv 27:3793–3806

    Google Scholar 

  • Mermoz M, Martin C (1987) Mapa de vegetacion del Parque y Reserva Nacional Nahuel Huapi. Administración de Parques Nacionales

  • Millennium Ecosystem Assessment (2003) Ecosystems and human well-being: a framework for assessment. Island Press, Washington

    Google Scholar 

  • Mokotjomela TM, Musil CF, Esler KJ (2013) Frugivorous birds visit fruits of emerging alien shrub species more frequently than those of native shrub species in the South African Mediterranean climate region. South Afr J Bot 86:73–78

    Google Scholar 

  • Morán-López T, Carlo TA, Amico GC, Morales JM (2018) Diet complementation as a frequency-dependent mechanism conferring advantages to rare plants via dispersal. Funct Ecol 32:2310–2320

    Google Scholar 

  • Palacio FX, Ordano M (2018) The strength and drivers of bird-mediated selection on fruit crop size: a meta-analysis. Front Ecol Evol 6:18

    Google Scholar 

  • Peralta G, Perry GLW, Vázquez DP, Dehling M, Tylianakis JM (2020) Strength of niche processes for species interactions is lower for generalists and exotic species. J Anim Ecol 89:2145–2155

    PubMed  Google Scholar 

  • Pizo M (2002) The seed-dispersers and fruit syndromes of Myrtaceae in the Brazilian Atlantic Forest

  • R Development Core Team (2017) R: a language and environment for statistical computing. R Development Core Team, Vienna

    Google Scholar 

  • Reid S, Armesto JJ (2011) Interaction dynamics of avian frugivores and plants in a Chilean Mediterranean shrubland. J Arid Environ 75:221–230

    Google Scholar 

  • Rentería JL, Gardener MR, Panetta FD et al (2012) Possible impacts of the invasive plant Rubus niveus on the native vegetation of the Scalesia forest in the Galapagos islands. PLoS One 7:e48106

    PubMed  PubMed Central  Google Scholar 

  • Riádigos E, Martínez E (1994) Producción de frambuesa en los valles patagónicos. Presencia 32:20–21

    Google Scholar 

  • Rojas TN, Gallo MCF, Vergara-Tabares DL, Nazaro MG (2019) Being popular or freak: how alien plants integrate into native plant–frugivore networks. Biol Invasions 21:2589–2598

    Google Scholar 

  • Rovere AE, Molares S, Ladio AH (2013) Plantas utilizadas en cercos vivos de ciudades patagónicas: Aportes de la etnobotánica para la conservación. Ecol Austral 23:165–173

    Google Scholar 

  • Schaefer HM, Schmidt V, Bairlein F (2003) Discrimination abilities for nutrients: which difference matters for choosy birds and why? Anim Behav 65:531–541

    Google Scholar 

  • Schupp EW, Jordano P, Gómez JM (2010) Seed dispersal effectiveness revisited: a conceptual review. New Phytologyst 188:333–353

    Google Scholar 

  • Sebastián-González E (2017) Drivers of species’ role in avian seed-dispersal mutualistic networks. J Anim Ecol 86:878–887

    PubMed  Google Scholar 

  • Smith SB, DeSando SA, Pagano T (2013) The value of native and invasive fruit-bearing shrubs for migrating songbirds. Northeast Nat 20:171–184

    Google Scholar 

  • Smith-Ramírez C, Arellano G, Hagen E et al (2013) The role of Turdus falcklandii (Aves: Passeriforme) as disperser of invasive plants in the Juan Fernández Archipelago. Rev Chil Hist Nat 86:33–48

    Google Scholar 

  • Spotswood EN, Meyer JY, Bartolome JW (2012) An invasive tree alters the structure of seed dispersal networks between birds and plants in French Polynesia. J Biogeogr 39:2007–2020

    Google Scholar 

  • Stachowicz JJ (2001) Mutalism, facilitation, and the structure of ecological communities. Bioscience 51:235–246

    Google Scholar 

  • Stacklies W, Redestig H, Scholz M et al (2007) pcaMethods—a bioconductor package providing PCA methods for incomplete data. Bioinformatics 23:1164–1167

    CAS  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  • Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45:89–113

    Google Scholar 

  • Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363

    PubMed  Google Scholar 

  • Valiente-Banuet A, Aizen MA, Alcántara JM et al (2015) Beyond species loss: the extinction of ecological interactions in a changing world. Funct Ecol 29:299–307

    Google Scholar 

  • Vargas R, Gärtner S, Alvarez M et al (2013a) Does restoration help the conservation of the threatened forest of Robinson Crusoe Island? The impact of forest gap attributes on endemic plant species richness and exotic invasions. Biodivers Conserv 22:1283–1300

    Google Scholar 

  • Vargas R, Gärtner S, Hagen E, Reif A (2013b) Tree regeneration in the threatened forest of Robinson Crusoe Island, Chile: the role of small-scale disturbances on microsite conditions and invasive species. For Ecol Manag 307:255–265

    Google Scholar 

  • Vergara-Tabares DL, Toledo M, García E, Peluc SI (2018) Aliens will provide: avian responses to a new temporal resource offered by ornithocorous exotic shrubs. Oecologia 188:173–182

    PubMed  Google Scholar 

  • Viana DS, Santamaría L, Figuerola J (2016) Migratory birds as global dispersal vectors. Trends Ecol Evol 31:763–775

    PubMed  Google Scholar 

  • Vizentin-Bugoni J, Tarwater CE, Foster JT, Drake DR, Gleditsch JM, Hruska AM, Kelley JP, Sperry JH (2019) Structure, spatial dynamics, and stability of novel seed dispersal mutualistic networks in Hawai’i. Science 364:78–82

    CAS  PubMed  Google Scholar 

  • Vollstädt MGR, Ferger SW, Hemp A et al (2017) Direct and indirect effects of climate, human disturbance and plant traits on avian functional diversity. Glob Ecol Biogeogr 26:963–972

    Google Scholar 

  • Wheelwright NT (1985) Fruit-size, gape width, and the diets of fruit‐eating birds. Ecology 66:808–818

    Google Scholar 

  • Williams PA (2006) The role of blackbirds (Turdus merula) in weed invasion in New Zealand. N Z J Ecol 30:285–291

    Google Scholar 

Download references

Acknowledgements

We thank Agustín Vitali, Mariano Rodríguez-Cabal, Teresa Morán-López and two anonymous reviewers for their comments and suggestions on previous drafts of the manuscript. We also thank the Municipal Park Llao Llao, the Environment and Sustainable Development Secretariat from Río Negro Province and the National Parks Administration (APN) for granting permits to work in the area. VMA was supported by a postdoctoral fellowship from the National Scientific and Technical Research Council (CONICET). GCA was supported by the CONICET.

Funding

Funding was provided by FONCyT (Grant No. 2017-2328) and Universidad Nacional del Comahue (Grant No. PIN 04/B229).

Author information

Authors and Affiliations

  1. Laboratorio Ecotono, INIBIOMA, CONICET-Universidad Nacional del Comahue, Dirección Postal: Quintral 1250, 8400, Bariloche, Río Negro, Argentina

    Valeria L. Martin-Albarracin & Guillermo C. Amico

Authors
  1. Valeria L. Martin-Albarracin
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Guillermo C. Amico
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Valeria L. Martin-Albarracin.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Material 1

Supplementary Material 2

Supplementary Material 3

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Martin-Albarracin, V.L., Amico, G.C. Plant origin and fruit traits shape fruit removal patterns by native birds in invaded plant communities. Biol Invasions 23, 857–870 (2021). https://doi.org/10.1007/s10530-020-02407-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-020-02407-1

Keywords

Search

Navigation