Skip to main content

Advertisement

Log in

Native anurans threatened by the alien tree Ligustrum lucidum in a seasonal subtropical forest

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

Abstract

Amphibians are declining globally from diverse and complex causes, with one of the most prevalent being alien species invasion. Alien woody invaders, such as the evergreen Ligustrum lucidum, are deeply transforming native ecosystems worldwide. Our aim was to evaluate the effect of Ligustrum lucidum invasion on native anurans in a seasonal semiarid subtropical forest. Sampling was conducted in streams dominated by L. lucidum forest and streams dominated by native forest. Amphibian species richness and diversity, and community and species abundance were recorded. We characterized invaded and non-invaded streams by measuring biotic and abiotic variables. Invaded streams support only three of the seven species present in non-invaded streams. Species richness in non-invaded streams was twice as high as in invaded streams and community abundance was almost five times greater in the former than in the latter. Invasion by L. lucidum triggers profound changes in vegetation physiognomy and composition of this xerophytic seasonal forest, resulting in dark, unsuitable habitats for several native anurans. In agreement with the few studies focused on the effect of alien woody invaders on amphibians, this study supports that woody alien invasion results in a reduction of native anuran richness and the dominance of a generalist anuran species. This is the first report on the disruptive role of L. lucidum invasion in local anurans diversity and community dynamics.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Acosta R (2009) Plasticidad fenotípica en la metamorfosis de larvas de Rhinella arenarum del Valle de Lerma, Salta (Doctoral dissertation, Facultad de Ciencias Naturales y Museo). Universidad Nacional de La Plata.

  • Angilleta MJ (2009) Thermal adaptation A theoretical and empirical synthesis. Oxford University Press, New York, p 291

    Book  Google Scholar 

  • Ayup MM, Montti L, Aragón R, Grau HR (2014) Invasion of Ligustrum lucidum (Oleaceae) in the southern Yungas: Changes in habitat properties and decline in bird diversity. Acta Oecologica 54:72–81. https://doi.org/10.1016/j.actao.2013.03.006

    Article  Google Scholar 

  • Babini MS, Salas NE, Bionda CL et al (2015) Implicaciones de la urbanización en la presencia, distribución y ecología reproductiva de la fauna de anuros de una ciudad del área central de Argentina. Revista Mexicana De Biodiversidad 86:188–195. https://doi.org/10.7550/rmb.43684

    Article  Google Scholar 

  • Bellard C, Cassey P, Blackburn TM (2016) Alien species as a driver of recent extinctions. Biol Lett 12(2):20150623

  • Bellis LM, Astudillo A, Gavier-Pizarro G, Dardanelli S, Landi M, Hoyos L (2021) Glossy privet (Ligustrum lucidum) invasion decreases Chaco Serrano forest bird diversity but favors its seed dispersers. Biol Invasions 23(3):723–739. https://doi.org/10.1007/s10530-020-02399-y

    Article  Google Scholar 

  • Boyce RL, Durtsche RD, Fugal SL (2012) Impact of the invasive shrub Lonicera maackii on stand transpiration and ecosystem hydrology in a wetland forest. Biol Invasions 14:671–680. https://doi.org/10.1007/s10530-011-0108-6

    Article  Google Scholar 

  • Bucciarelli GM, Blaustein AR, Garcia TS, Kats LB (2014) Invasion complexities: The diverse impacts of nonnative species on amphibians. Copeia 4:611–632. https://doi.org/10.1643/OT-14-014

    Article  Google Scholar 

  • Cabrera A (1976) Regiones fitogeográficas argentinas. Enciclopedia Argentina de Agricultura y Jardinería. Tomo 2. 2a edición. ACME Buenos Aires Argentina Fascículo 1:1–85

    Google Scholar 

  • Catenazzi A (2015) State of the world’s amphibians. Ann Rev Environ Res 40:91–119

  • Cei JM (1980) Amphibians of Argentina. Monitore Zoologico Italiano New Series. Taylor & Francis, Monographs, Milan

    Google Scholar 

  • Cohen JS, Rainford SD, Blossey B (2014) Community-weighted mean functional effect traits determine larval amphibian responses to litter mixtures. Oecologia 174(4):1359–1366. https://doi.org/10.1007/s00442-013-2856-8

    Article  CAS  PubMed  Google Scholar 

  • Colwell RK (2013) EstimateS: statistical estimation of species richness and shared species from samples. Version 9. Persistent. purl.oclc.org/estimates

  • Cotton TB, Kwiatkowski MA, Saenz D, Collyer M (2012) Effects of an invasive plant, Chinese Tallow (Triadica sebifera), on development and survival of anuran larvae. J Herpetol 46:186–193. https://doi.org/10.1670/10-311

    Article  Google Scholar 

  • Crooks JA (2002) Characterizing ecosystem-level consequences of biological invasions: the role of ecosystem engineers. Oikos 97:153–166. https://doi.org/10.1034/j.1600-0706.2002.970201.x

    Article  Google Scholar 

  • Crump ML, Scott NJ (2001) Relevamientos por encuentros visuales. Medición y monitoreo de la diversidad biológica. Métodos estandarizados para anfibios. Comodoro Rivadavia (Argentina): Editorial Universitaria de la Patagonia, pp. 80–87

  • De Fina AL (1992) Aptitud agroclimática de la República Argentina. Academia Nacional de Agronomía y Veterinaria, pp. 1–402

  • Díaz D, Settele J, Brondízio ES et al (2019) Pervasive human-driven decline of life on Earth points to the need for profound change. Science 366:3100. https://doi.org/10.1126/science.aax3100

    Article  CAS  Google Scholar 

  • Dreyer JBB, Higuchi P, Silva AC (2019) Ligustrum lucidum WT Aiton (broad-leaf privet) demonstrates climatic niche shifts during global-scale invasion. Sci Reports 9(1):1–6. https://doi.org/10.1038/s41598-019-40531-8

    Article  CAS  Google Scholar 

  • Earl JE, Cohagen KE, Semlitsch RD (2012) Effects of leachate from tree leaves and grass litter on tadpoles. Environ Toxicol Chem 31:1511–1517. https://doi.org/10.1002/etc.1829

    Article  CAS  PubMed  Google Scholar 

  • Earl JE, Semlitsch RD (2015) Effects of tannin source and concentration from tree leaves on two species of tadpoles. Environ Toxicol Chem 34(1):120–126. https://doi.org/10.1002/etc.2767

    Article  CAS  PubMed  Google Scholar 

  • Fabrezi M (2011) Heterochrony in growth and development in Anurans from the Chaco of South America. Evol Biol 38(4):390–411. https://doi.org/10.1007/s11692-011-9128-5

    Article  Google Scholar 

  • Falaschi M, Melotto A, Manenti R, Ficetola GF (2020) Invasive species and amphibian conserrvation. Herpetologica 76(2):216–227

    Article  Google Scholar 

  • Fernandez RD, Ceballos SJ, Aragón R et al (2020) A global review of Ligustrum lucidum (OLEACEAE) invasion. Bot Rev 86(2):93–118. https://doi.org/10.1007/s12229-020-09228-w

    Article  Google Scholar 

  • Ferreras AE, Giorgis MA, Tecco PA et al (2015) Impact of Ligustrum lucidum on the soil seed bank in invaded subtropical seasonally dry woodlands (Cordoba, Argentina). Biol Invasions 217:3547–3561. https://doi.org/10.1007/s10530-015-0977-1

    Article  Google Scholar 

  • Ferreras AE, Whitworth-Hulse JI, Tecco PA, Marcora PI, Funes G (2019) Environmental constraints to native woody species recruitment in invaded mountain woodlands of central Argentina. Forest Ecol Manag 440:189–201

    Article  Google Scholar 

  • Fonovich TM, Perez-Coll CS, Fridman O et al (2016) Phospholipid changes in Rhinella arenarum embryos under different acclimation conditions to copper. Comp Biochem Physiol c: Toxicol Pharmacol 189:10–16. https://doi.org/10.1016/j.cbpc.2016.06.007

    Article  CAS  Google Scholar 

  • Furey C, TeccoPerez–Harguindeguy PAN et al (2014) The importance of native and exotic plant identity and dominance on decomposition patterns in mountain woodlands of central Argentina. Acta Oecol 54:13–20. https://doi.org/10.1016/j.actao.2012.12.005

    Article  Google Scholar 

  • Garcia RA, Clusella-Trullas S (2019) Thermal landscape change as a driver of ectotherm responses to plant invasions. Proc R Soc B 286:2019–1020. https://doi.org/10.1098/rspb.2019.1020

    Article  Google Scholar 

  • Gavier G, Kufner MB, Giraudo L, Sironi M, Altrichter M, Tamburini D (2003) Comunidades herpetológicas de la reserva la quebrada, Río Ceballos, Córdoba (Argentina). Cuadernos de Herpetología 17(1–2):51–64. http://sedici.unlp.edu.ar/handle/10915/6382

  • Gavier GI, Bucher EH (2004) Deforestación de las Sierras Chicas de Córdoba (Argentina) en el período 1970–1997. Córdoba Academia Nacional De Ciencias 101:1–27

    Google Scholar 

  • Gavier-Pizarro GI, Kuemmerle T, Hoyos LE et al (2012) Monitoring the invasion of an exotic tree (Ligustrum lucidum) from 1983 to 2006 with 1 Landsat TM/ETM+ satellite data and support vector machines in Córdoba, Argentina. Remote Sens Environ 122:134–145. https://doi.org/10.1016/j.rse.2011.09.023

    Article  Google Scholar 

  • Giorgis MA, Cingolani AM, Gurvich DE et al (2017) Changes in floristic composition and physiognomy are decoupled along elevation gradients in central Argentina. Appl Veg Sci 20:558–571. https://doi.org/10.1111/avsc.12324

    Article  Google Scholar 

  • Giorgis MA, Cingolani AM, Tecco PA et al (2016) Testing alien plant distribution and habitat invasibility in mountain ecosystems: growth form matters. Biol Invasions 18:2017–2028. https://doi.org/10.1007/s10530-016-1148-8

    Article  Google Scholar 

  • Halverson MA, Skelly D, Kiesecker JM, Freidenburg LK (2003) Forest mediated light regime linked to amphibian distribution and performance. Oecologia 134:360–364. https://doi.org/10.1007/s00442-002-1136-9

    Article  CAS  PubMed  Google Scholar 

  • Hickman CR, Watling JI (2014) Leachates from an invasive shrub causes risk-prone behavior in a larval amphibian. Behav Ecol 25(2):300–305. https://doi.org/10.1093/beheco/art121

    Article  Google Scholar 

  • Hill WR, Ryon MG, Schilling EM (1995) Light Limitation in a Stream Ecosystem: responses by Primary Producers and Consumers. Ecology, 76 (4): 1297–1309 Houlahan JE, Findlay CS, Schmidt BR, Meyer AH, Kuzmin, SL, (2000) Quantitative evidence for global amphibian population declines. Nature 404:752–755. https://doi.org/10.1038/35008052

    Article  Google Scholar 

  • Hoyos LE, Gavier-Pizarro GI, Kuemmerle T et al (2010) Invasion of glossy privet (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Córdoba, Argentina. Biol Invasions 12:3261–3275. https://doi.org/10.1007/s10530-010-9720-0

    Article  Google Scholar 

  • IUCN (2020) The IUCN Red List of Threatened Species. Version 2020–2. https://www.iucnredlist.org

  • Kiffney PM, Richardson JS, Bull JP (2004) Establishing light as a causal mechanism structuring stream communities in response to experimental manipulation of riparian buffer width. J N Am Benthol Soc 23(3):542–555

    Article  Google Scholar 

  • Lane S, Hamer A, Mahony M (2007) Habitat correlates of five amphibian species and of sepecies-richnes in a wetland system in New South Wales, Australia. Appl Herpetol 4:65–82

  • Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam, pp. 1–969

  • Lemckert F, Haywood A, Brassil T, Mahony M (2005) Correlations between frogs and pond attributes in central New South Wales, Australia: what makes a good pond?. Appl Herpetol 3(1):67

  • Lescano JN, Nori J, Verga E et al (2015) Anfibios de las Sierras Pampeanas Centrales: Diversidad y Distribución altitudinal. Cuadernos de Herpetología 29:103–115. http://sedici.unlp.edu.ar/handle/10915/56638

  • Loyola RD, Lemes P, Brum FT et al (2014) Clade-specific consequences of climate change to amphibians in Atlantic Forest protected areas. Ecography 37:65–72. https://doi.org/10.1111/j.1600-0587.2013.00396.x

    Article  Google Scholar 

  • Maerz JC, Brown CJ, Chapin CT, Blossey B (2005) Can secondary compounds of an invasive plant affect larval amphibians? Funct Ecol 19:970–975. https://doi.org/10.1111/j.1365-2435.2005.01054.x

    Article  Google Scholar 

  • Maerz JC, Cohen JS, Blossey B (2010) Does detritus quality predict the effect of native and non-native plants on the performance of larval amphibians? Freshwater Biol 55:1694–1704. https://doi.org/10.1111/j.1365-2427.2010.02404.x

    Article  Google Scholar 

  • Mallory MA, Richardson JS (2004) Complex interactions of light, nutrients and consumer density in a stream periphyton–grazer (tailed frog tadpoles) system. J Anim Ecol 74:1020–1028. https://doi.org/10.1111/j.1365-2656.2005.01000.x

    Article  Google Scholar 

  • Marano AV, Saparrat MCN, Steciow MM, Cabello MN, Gleason FH, Pireszottarelli CLA, Barrera MD (2013) Comparative analysis of leaf-litter decomposition from the native Pouteria salicifolia and the exotic invasive Ligustrum lucidum in a lowland stream (Buenos Aires, Argentina). Fund Appl Limnol 183:297–307

    Article  CAS  Google Scholar 

  • Martin LJ, Blossey B (2013) Intraspecific variation overrides origin effects in impacts of litter-derived secondary compounds on larval amphibians. Oecologia 173(2):449–459

    Article  Google Scholar 

  • Martin LJ, Murray BR (2011) A predictive framework and review of the ecological impacts of exotic plant invasions on reptiles and amphibians. Biol Rev 86:407–419. https://doi.org/10.1111/j.1469-185X.2010.00152.x

    Article  PubMed  Google Scholar 

  • McCary MA, Mores R, Farfan MA, Wise DH (2016) Invasive plants have different effects on trophic structure of green and brown food webs in terrestrial ecosystems: A meta-analysis. Ecol Letters 19(3):328–335. https://doi.org/10.1111/ele.12562

    Article  Google Scholar 

  • McCune B, Mefford MJ (2011). Multivariate Analysis of Ecological Data, Version 6, MjM Software. PC-ORD, Gleneden Beach, Oregon, USA, pp 1–232

  • Medina RG, Ponssa ML, Aráoz E (2016) Environmental, land cover and land use constraints on the distributional patterns of anurans: Leptodacylus species (Anura, Leptodactylidae) from Dry Chaco. PeerJ 4:e2605. https://doi.org/10.7717/peerj.2605

    Article  PubMed  PubMed Central  Google Scholar 

  • Miloch D, Bonino A, Leynaud GC, Lescano JN (2020) Endemic amphibians cornered in headwaters by trout invasion in a mountain range in Argentina. Aquat Conserv. https://doi.org/10.1002/aqc.3441

    Article  Google Scholar 

  • Nunes AL, Fill JM, Davies SJ et al (2019) A global meta-analysis of the ecological impacts of alien species on native amphibians. Proc R Soc 286:2018–2528. https://doi.org/10.1098/rspb.2018.2528

    Article  Google Scholar 

  • Olden JD (2008) Biotic Homogenization. In: Encyclopedia of Life Sciences (ELS). John Wiley & Sons, Ltd., Chichester. https://doi.org/10.1002/9780470015902.a0020471

  • Pearson DE (2010) Trait-and density-mediated indirect interactions initiated by an exotic invasive plant autogenic ecosystem engineer. Am Nat 176(4):394–403

    Article  Google Scholar 

  • Perez A, Mazerolle MJ, Brisson J (2013) Effects of exotic common reed (Phragmites australis) on wood frog (Lithobates sylvaticus) tadpole development and food availability. J Freshwater Ecol 28(2):165–177

    Article  CAS  Google Scholar 

  • Pyšek P, Jarošík V, Pergl J, Moravcova L, Chytrý M, Kuehn I (2014) Temperate trees and shrubs as global invaders: the relationship between invasiveness and native distribution depends on biological traits. Biol Invasions 16(3):577–589. https://doi.org/10.1007/s10530-013-0600-2

    Article  Google Scholar 

  • R Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/

  • Rejmánek M, Richardson DM (2013) Trees and shrubs as invasive alien species—2013 update of the global database. Divers Distrib 19:1–2

    Article  Google Scholar 

  • Sacerdote AB, King RB (2014) Direct effects of an invasive European Buckthorn metabolite on embryo survival and development in Xenopus laevis and Pseudacris triseriata. J Herpetol 48:51–58. https://doi.org/10.1670/12-066

    Article  Google Scholar 

  • Saenz D, Adams CK (2017) Effects of Chinese tallow leaf litter on water chemistry and surfacing behaviour of anuran larvae. Herpetol J 27(4):326–332

    Google Scholar 

  • Saenz D, Fucik EM, Kwiatkowski MA (2013) Synergistic effects of the invasive Chinese tallow (Triadica sebifera) and climate change on aquatic amphibian survival. Ecol Evol 3(14):4828–4840

    Article  Google Scholar 

  • Sanabria EA, Quiroga LB, Martino AL (2011) Seasonal changes in the thermoregulatory strategies of Rhinella arenarum in the Monte desert, Argentina. J Therm Biol 36:23–28. https://doi.org/10.1016/j.jtherbio.2010.10.002

    Article  Google Scholar 

  • Schalk CM, Saenz D (2016) Environmental drivers of anuran calling phenology in a seasonal Neotropical ecosystem. Austral Ecol 41:16–27. https://doi.org/10.1111/aec.12281

    Article  Google Scholar 

  • Schiesari L (2006) Pond canopy cover: a resource gradient for anuran larvae. Freshwater Biol 51:412–423. https://doi.org/10.1111/j.1365-2427.2005.01497.x

    Article  CAS  Google Scholar 

  • Schirmel J, Bundschuh M, Entling MH, Kowarik I, Buchholz S (2016) Impacts of invasive plants on resident animals across ecosystems, taxa, and feeding types: a global assessment. Global Change Biol 22(2):594–603. https://doi.org/10.1111/gcb.13093

    Article  Google Scholar 

  • Skelly DK, Freidenburg LK, Kiesecker JM (2002) Forest canopy and the performance of larval amphibians. Ecology 83(4):983–992. https://doi.org/10.1890/0012-9658(2002)083[0983:FCATPO]2.0.CO;2

    Article  Google Scholar 

  • Skelly DK, Bolden SR, Freidenburg LK (2014) Experimental canopy removal enhances diversity of vernal pond amphibians. Ecol Appl 24(2):340–345

  • Stephens JP, Berven KA, Tiegs SD (2013) Anthropogenic changes to leaf litter input affect the fitness of a larval amphibian. Freshwater Biol 58(8):1631–1646

    Article  CAS  Google Scholar 

  • Stewart PS, Hill RA, Stephens PA, Whittingham MJ, Dawson W (2021) Impacts of invasive plants on animal behaviour. Ecol Letters 24(4):891–907. https://doi.org/10.1111/ele.13687

    Article  Google Scholar 

  • Stuart SN, Chanson JS, Cox NA et al (2004) Status and trends of amphibian declines and extinctions worldwide. Science 307:1783–1786. https://doi.org/10.1126/science.1103538

    Article  Google Scholar 

  • Tecco PA, Pais Bosch AI, Funes G, Marcora P, Zeballos SR, Cabido M, Urcelay C (2016) Mountain invasions on the way: are there climatic constraints for the expansion of alien woody species along an elevation gradient in Argentina? J Plant Ecol 9:380–392

    Article  Google Scholar 

  • Verga EG, Leynaud GC, Lescano JN, Bellis LM (2012) Is livestock grazing compatible with amphibian diversity in the High Mountains of Córdoba, Argentina? Eur J Wildlife Res 58(6):823–832. https://doi.org/10.1007/s10344-012-0630-6

    Article  Google Scholar 

  • Watling JI, Hickman CR, Lee E, Wang K, Orrock JL (2011a) Extracts of the invasive shrub Lonicera maackii increase mortality and alter behavior of amphibian larvae. Oecologia 165:153–159. https://doi.org/10.1007/s00442-010-1777-z

    Article  CAS  PubMed  Google Scholar 

  • Watling JI, Hickman CR, Orrock JL (2011b) Invasive shrub alters native forest amphibian communities. Bioll Conserv 144:2597–2601. https://doi.org/10.1016/j.biocon.2011.07.005

    Article  Google Scholar 

  • Whitworth-Hulse JI (2018) Efectos de la invasion de Ligustrum lucidum sobre la dinámica hidrica en bosques nativos del Chaco Serrano: la interaccion entre precipitacion, vegetacion y suelo. Doctoral dissertation, Universidad Nacional de Cordoba, Cordoba, Argentina

  • Zeballos SR, Tecco PA, Cabido M, Gurvich DE (2014) Composición de especies leñosas en comunidades invadidas en montañas del centro de Argentina: su relación con factores ambientales locales. Rev Biol Trop 62:1549–1563

    Article  Google Scholar 

  • Zimmerman BL (2001) Transectas de bandas auditivas. In: Heyer WR, Donnelly MA, McDiarmid MR, Hayek LC, Foster MS (eds) Medición y monitoreo de la diversidad biológica: métodos estandarizados para anfibios. Smithsonian Institution Press & Editorial Universitaria de la Patagonia, Chubut, pp 87–93

    Google Scholar 

Download references

Acknowledgements

This study was supported by SeCyT, National University of Córdoba. Project code 33620180101120CB 2018/2021. We thank Gustavo Castillo and Mario Martín for their help in data collection, as well as all those who accompanied us in different ways in the sampling campaigns. We also thank Jeremias Dutto, Emiliano Giorgis and Jorgelina Brasca for improving the English style. We thank Paula Tecco, Gerardo Leynaud, and Javier Nori for their important suggestions on our preliminary manuscript and to anonymous reviewers and editor for their valuable comments. M.A.G. and J.L. are researchers from CONICET and professor at the National University of Córdoba.

Funding

(Information that explains whether and by whom the research was supported) SeCyT, Universidad Nacional de Córdoba. Project code 33620180101120CB 2018/2021, support fuel cost.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed equally to the design of the survey and the writing of the manuscript.

Corresponding author

Correspondence to M. A. Giorgis.

Ethics declarations

Conflicts of interest

The authors declare that they have no Conflicts of interest.

Consent to participate

All the authors consent to participate.

Consent for publication

All the authors consent to publication.

Additional information

Publisher's Note

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

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Segura, E.M., Giorgis, M.A. & Lescano, J.N. Native anurans threatened by the alien tree Ligustrum lucidum in a seasonal subtropical forest. Biol Invasions 23, 3859–3869 (2021). https://doi.org/10.1007/s10530-021-02617-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-021-02617-1

Keywords

Navigation