Abstract
Glossy privet (Ligustrum lucidum) is an aggressive invasive plant that replaces native forests and forms dense stands without understory in central Argentina. However, the consequences of these changes in terms of vegetation structure and composition in bird communities are unknown. Our goal was to understand how the effects of glossy privet invasion-induced habitat changes vary among bird species that differ in resource requirements (e.g., fruit supply, vegetation structure) and how these responses may in turn interact with the invasion process. We compared the avian–habitat relationships among forest patches with different invasion conditions (Serrano native forest, mixed forest and glossy privet forest) using a landscape approach. We found that bird richness was substantially lower in glossy privet forests, with up to 37% loss of bird species. Bird assemblages in invaded habitats changed, with an increase in the prevalence of bird species that feed on glossy privet, particularly during the cold season, when Serrano forest plants do not fruit. Our findings show that the loss of bird diversity and structural assemblage simplification were directly related to the loss of structural complexity caused by the invasion of glossy privet. The increased abundance of birds feeding on glossy privet contributed to the spread of this plant. Given the probable continued expansion of glossy privet and its resistance to control, the persistence of diverse native bird and plant communities in areas subject to invasion by this plant species is at risk.
Similar content being viewed by others
References
Agudelo-Henríquez WJ (2015) Escenarios futuros de deforestación como herramienta para evaluar políticas de manejo en un sector de las Sierras Chicas de Córdoba, Argentina. Tesis de Maestría, Centro de Zoología Aplicada, Córdoba, Argentina
Aguirre-Acosta N, Kowaljow E, Aguilar R (2014) Reproductive performance of the invasive tree Ligustrum lucidum in a subtropical dry forest: does habitat fragmentation boost or limit invasion? Biol Invasions 16:1397–1410
Albanesi S, Dardanelli S, Bellis LM (2014) Effects of fire disturbance on bird communities and species of mountain Serrano forest in central Argentina. J For Res 19:105–114
Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46
Argañaraz JP, Gavier-Pizarro GG, ZakM BellisLM (2015) Fireregime, climate, and vegetation in the Sierras de Córdoba. Argent Fire Ecol 11(1):55–73
Aslan CE (2011) Implications of newly-formed seed-dispersal mutualisms between birds and introduced plants in northern California, USA. Biol Invasions 13:2829–2845
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 Oecol 54:72–81
Baraldi A, Parmiggiani F (1995) An investigation of textural characteristics associated with gray level co-occurrence matrix statistical parameters. IEEE Trans Geosci Rem Sens 33:293–304
Beissinger SR, Steadman EC, Wohlgenant T, Blake JG, Zack S (1996) Null models for assessing ecosystem conservation priorities: threatened birds as titers of threatened ecosystems in South America. Conserv Biol 10:1343–2135
Bellis LM, Pidgeon AM, Radeloff VC, St-Louis V, Navarro JL, Martella MB (2008) Modeling habitat suitability for Greater Rheas based on satellite image texture. Ecol Appl 18:1956–1966
Bellis LM, Pidgeon A, Alcántara PC, Dardanelli S, Radeloff V (2015) Influences of succession and erosion on bird communities in a South American highland wooded landscape. For Ecol Manag 349:85–93
Bibby CJ, Burgess ND, Hill DA, Mustoe SH (2000) Bird census techniques. Academic Press, London
Brooks ML, D’Antonio CM, Richardson DM, Grace JB, Keeley JE, Di Tomaso JM, Hobbs RJ, Pellant M, Pyke D (2004) Effects of invasive alien plants on fire regimes. Bioscience 54:677–688
Cabido MR, Zak M (1999) Vegetación del Norte de Córdoba. Instituto Multidisciplinario de Biología Vegetal, Universidad Nacional de Córdoba y CONICET, Córdoba
Capllonch P, Soria C, Ortiz D (2011) Un ejemplo de migración altitudinal: el arañero corona rojiza Myioborus brunniceps (aves:Parulidae) en las Yungas australes. Kempffiana 7:3–18
Clarke KR (1993) Non-parametric multivariate analysis of changes in community structure. Aust J Ecol 18:117–143
Cueto VR, Lopez de Casenave J (1999) Determinants of bird species richness: role of climate and vegetation structure at a regional scale. J Biogeogr 26:487–492
Culbert PD, Radeloff VC, St-Louis V, Flather CH, Rittenhouse CD, Albright TP, Pidgeon AM (2013) Modeling broad-scale patterns of avian species richness across the Midwestern United States with measures of satellite image texture. Remote Sens Environ 118:140–150
Da Silva Nunes A, Higuchi P, Da Silva AC, De Vargas Kilca R, Da Silva MAF, Larsen JG (2018) Ligustrum lucidum como uma espécie invasora oportunista em uma Floresta com Araucária no sul do Brasil. Rodriguésia 69:351–362
Dardanelli S, Nores ML, Nores M (2006) Minimum area requirements of breeding birds in fragmented woodland of Central Argentina. Divers Distrib 12:687–693
De la Peña MR, Pensiero JF (2017) Las plantas como recurso alimenticio de las aves. Ediciones UNL. 1a ed. Santa Fe
Dong-Chen H, Wang L (1990) Texture unit, texture spectrum, and texture analysis. IEEE Trans Geosci Remote Sens 28:509–512
Dufrene M, Legendre P (1997) Species assemblages and indicator species: the need for a flexible asymmetrical approach. Ecol Monogr 67:345–366
Ekert PA, Bucher DJ (1999) Winter use of large-leaved privet Ligustrum lucidum (family Oleaceae) by birds in suburban Lismore, New South Wales. Proc Linn Soc NSW 121:29–38
Fandiño B, Berduc AJ, Beltzer AH (2010) Ensambles de aves de bosques nativos y exóticos en la estación reproductiva de un área protegida en el Espinal de Entre Ríos, Argentina. Ornitol Neotrop 21:1–16
Ferreras AE, Torres C, Galetto L (2008) Fruit removal of an invasive exotic species (Ligustrum lucidum) in a fragmented landscape. J Arid Environ 72:1573–1580
Gamon J, Field CB, Gulden ML, Griffin KL, Hartley AE, Joel G, Peñuelas J, Valentini R (1995) Relationships between NDVI, canopy structure, and photosynthesis in three Californian vegetation types. Ecol Appl 5:28–41
Gavier GI, Bucher EH (2004) Deforestación de las Sierras Chicas de Córdoba (Argentina) en el período 1970–1997, vol 101. Academia Nacional de Ciencias, Córdoba
Gavier-Pizarro GI, Kuemmerle T, Hoyos LE, Stewart SI, Huebner CD, Keuler NS, Radeloff VC (2012) Monitoring the invasion of an exotic tree (Ligustrumlucidum) from 1983 to 2006 with Landsat TM/ETM+ satellite data and Support Vector Machines in Córdoba, Argentina. Remote Sens Environ 122:134–145
Ge S, Carruthers R, Gong P, Herrera A (2006) Texture analysis for mapping Tamarix parviflora using aerial photographs along the Cache creek, California. Environ Monit Assess 114:65–83
Giorgis MA, Cingolani AM, Chiarini F, Chiapella J, Barboza G, Ariza Espinar L, Morero R, Gurvich D, Tecco PA, Subils R, Cabido M (2011) Composición florística del Bosque Chaqueño Serrano de la provincia de Córdoba, Argentina. Kurtziana 36:9–43
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
Gurvich DE, Tecco PA, Diaz S (2005) Plant invasions in undisturbed ecosystems: the triggering attribute approach. J Veg Sci 16:723–728
Hammer O (2019) PAST: paleontological statistics. Version 3.25. Natural History Museum University of Oslo, Oslo
Hansen MC, Potapov PV, Moore HM, Turubanova SA, Tyukavina A, Thau D, Stehman SV, Goetz SJ, Loveland TR, Kommareddy A, Egorov A, Chini L, Justice CO, Townshend JRC (2013) High-resolution global maps of 21st-century forest cover change. Science 342:850–853
Hepinstall JA, Sader SA (1997) Using Bayesian statistics, Thematic Mapper satellite imagery, and breeding bird data to model bird species probability of occurrence in Maine. Photogramm Eng Remote Sens 63:1231–1237
Heredia J, Salvador S (2014) Comportamiento ecológico y primer descripción del nido del arañero corona rojiza (Myioborus brunniceps) en el centro de Argentina. Hist Nat 4:55–62
Hoyos LE, Gavier-Pizarro GI, Kuemmerle T, Bucher EH, Radeloff VC, Tecco PA (2010) Invasion of glossy privet (Ligustrum lucidum) and native forest loss in the Sierras Chicas of Córdoba, Argentina. Biol Invasions 12:3261–3275
Hudak A, Wessman CA (1998) Textural analysis of historical aerial photography to characterize woody plant encroachment in South African Savanna. Remote Sens Environ 66:317–330
Lichstein JW, Grau HR, Aragón R (2004) Recruitment limitation in secondary forests dominated by an exotic tree. J Veg Sci 15:721–728
Lindenmayer DB, Cunningham RB, Donnelly CF, Nix H, Lindenmayer BD (2002) Effects of forest fragmentation in bird assemblages in a novel landscape context. Ecol Manag 72:1–18
Mac Arthur RH, Mac Arthur JW (1961) On bird species diversity. Ecology 42:594–598
Mack RN, Simberloff D, Lonsdale WM, Evans H, Clout M, Bazzaz FA (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710
MacNally R, Parkinson A, Horrocks G, Conole L, Tzaros C (2001) Relationships between terrestrial vertebrate diversity abundance and availability of coarse woody debris on south-eastern Australian floodplains. Biol Conserv 99:191–205
Magurran AE (2004) Measuring biological diversity. Blackwell Publishing, Oxford
Malizia A, Osinaga-Acosta O, Powell PA, Aragon R (2017) Invasion of Ligustrum lucidum (Oleaceae) in subtropical secondary forests of NW Argentina: declining growth rates of abundant native tree species. J Veg Sci. https://doi.org/10.1111/jvs.12572
Mangla S, Sheley RL, Radosevich SR (2011) Intra and interspecific competition among invasive and native species during early stages of plant growth. Plant Ecol 212:531–542
Montaldo NH (1993) Dispersión por aves y éxito reproductivo de dos especies de Ligustrum (Oleaceae) en un relicto de selva subtropical en la Argentina. Rev Chil Hist Nat 66:75–85
Montaldo NH (2000) Éxito reproductivo de plantas ornitócoras en un relicto de selva subtropical en Argentina. Rev Chil Hist Nat 73:511–524
Montaldo NH (2005) Aves frugívoras de un relicto de selva subtropical ribereña en Argentina: manipulación de frutos y destino de las semillas. Hornero 20:163–172
Montti L, Piriz Carrillo V, Gutierrez-Angonese J, Gasparri I, Aragon R (2017) The role of bioclimatic features, landscape configuration and historical land use in the invasion of an Asian tree in subtropical Argentina. Landsc Ecol. https://doi.org/10.1007/s10980-017-0563-2
Nelson SB, Coon JJ, Duchardt CJ et al (2017) Patterns and mechanisms of invasive plant impacts on North American birds: a systematic review. Biol Invasions 19:1547–1563
Paritsis J, Aizen M (2008) Effects of exotic conifer plantations on the biodiversity of understory plants, epigeal beetles and birds in Nothofagus dombeyi forests. For Ecol Manag 255:1575–1583
Paruelo JM, Epstein HE, Lauenroth WK, Burke IC (1997) ANPP estimates from NDVI for the central grassland region of the U.S. Ecology 78:953–958
Powell P, Aráoz E (2018) Biological and environmental effects on fine-scale seed dispersal of an invasive tree in a secondary subtropicalforest. Biol Invasions 20:461–473
Quinn G, Keough M (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Ralph CJ, Droege, Sauer JR (1995) Managing and monitoring birds using point counts: standards and applications. USDA Forest Service Gen. Tech. Rep. PSW-GTR-149
Ralph CJ, Geupel GR, Pyle P, Martin TE, Desante DF (1993) Handbook of field methods for monitoring land birds. USDA Forest Service General Technical Report PSW-144. Albany, CA
Remsen JV, Cadena JR, Jaramillo CD, Nores M, Pacheco JF, Robbins MB, Schulenberg, TS, Stiles FG, Stotz DF, Zimmer KJ (2019) A classification of the bird species of South America. American Ornithologists’ Union. http://www.museum.lsu.edu/*Remsen/SACCBaseline.htm
Richardson DM, Pysek P, Rejmánek M, Barbour MG, Panetta FD, West CJ (2000) Naturalization and invasion of alien plants: concepts and definitions. Divers Distrib 6:93–107
Río ME, Achaval L (1904) Geografía de la Provincia de Córdoba: Atlas. (vol 1). Compañía sud-americana de billetes de banco
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. Glob Change Biol 22:594–603
Shahabuddin G, Kumar R (2007) Effects of extractive disturbance on bird assemblages, vegetation structure and floristics in tropical scrub forest, Sariska Tiger Reserve, India. For Ecol Manag 246:175–185
Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176
Simberloff D, Rejmanek M (2011) Encyclopedia of biological invasions. University of California Press, Berkeley
St-Louis V, Pidgeon AM, Clayton MK, Locke BA, Bash D, Radeloff VC (2009) Satelliteimage texture and vegetation index predict avian biodiversity in the Chihuahuan Desert of New Mexico. Ecography 32:468–480
TNC (2005) Gran Chaco americano ecoregional assessment. FundaciónVida Silvestre Argentina, Fundación para el Desarrollo Sustentable del Chaco (DeSdel Chaco) and Wildife Conservation Society Bolivia (WCS), 1st edn. The Nature Conservancy, Buenos Aires
Theoharides KA, Dukes JS (2007) Plant invasion across space and time: factors affecting non indigenous species success during four stages of invasion. New Phytol 176:256–273
Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371(6492):65–66
Tuttle EM, Jensen RR, Formica VA, Gonser RA (2006) Using remote sensing image texture to study habitat use patterns: a case study using the polymorphic white-throated sparrow (Zonotrichia albicolis). Glob Ecol Biogeogr 15:349–357
Verga E, Galetto L, Peluc SI (2020) Avian responses to forest fragmentation during the breeding and non-breeding seasons. IBIS. https://doi.org/10.1111/ibi.12828
Vergara-Tabares DL, Badini J, Peluc SI (2016) Fruiting phenology as a ‘“triggering attribute”’ of invasion process: do invasive species take advantage of seed dispersal service provided by native birds? Biol Invasions 18:677–687
Wang R, Gamon J, Montgomery RA, Townsend PA, Zygielbaum AI, Bitan K, Tilman D, Cavender-Bares J (2016) Seasonal variation in the NDVI-species richness relationship in a prairie Grassland experiment (cedar creek). Remote Sens. https://doi.org/10.3390/rs8020128
Weidenhamer JD, Callaway RM (2010) Direct and indirect effects of invasive plants on soil chemistry and ecosystem function. J Chem Ecol 36:59–69
White E, Vivian-Smith G (2011) Contagious dispersal of seeds of synchronously fruiting species beneath invasive and native fleshy-fruited trees. Austral Ecol 36:195–202
Wiens JA, Rotenberry JT (1981) Habitat associations and community structure of birds in shrub steppe environments. Ecol Monogr 51:21–41
Wiens J, Sutter R, Anderson M, Blanchard J, Barnett A, Aguilar-Amuchastegui N, Avery C, Laine S (2009) Selecting and conserving lands for biodiversity: the role of remote sensing. Remote Sens Environ 113:1370–1381
Wilcox J, Beck CW (2007) Effects of Ligustrum sinense Lour. (Chinese privet) on abundance and diversity of songbirds and native plants in a southeastern nature preserve. Southeast Nat 6:535–550
Woltmann S (2003) Bird community responses to disturbance in a forestry concession in lowland Bolivia. Biodivers Conserv 12:1921–1936
Wood EM, Pidgeon AM, Radeloff VC, Keuler NS (2013) Image texture predicts avian density and species richness. PLoS ONE 8:e63211
Zak MR, Cabido M (2002) Spatial patterns of the Chaco vegetation of central Argentina: integration of remote sensing and phytosociology. Appl Veg Sci 5:213–226
Zamora Nasca NL, Montti L, Grau R, Paolini L (2014) Efectos de la invasión del ligustro, Ligustrum lucidum, en la dinámica hídrica de las Yungas del noroeste Argentino. Bosque 35:195–205
Zeballos SR, Tecco PA, Cabido M, Gurvich D (2014) Woody species composition in invaded communities from mountains of central Argentina: their relations with local environmental factors. Rev Biol Trop 62:1549–1563
Zurita GA, Rey N, Varela DM, Villagra M, Bellocq MI (2006) Conversion of the Atlantic Forest into native and exotic tree plantations: effects on bird communities from the local and regional perspectives. For Ecol Manag 235:164–173
Acknowledgements
We are very grateful to field assistants for their help with fieldwork. This research was supported by Secyt—UNC and FONCyT (PICT 2016 #1338). L.M.B. is a researcher at CONICET and professor at the Universidad Nacional de Córdoba. G.G.P is a researcher at CONICET and INTA; S. D. is a researcher at INTA and M.A.L is a technician at CONICET. Part of this study was the subject of the final undergraduate thesis of A. Astudillo.
Author information
Authors and Affiliations
Corresponding author
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.
Rights and permissions
About this article
Cite this article
Bellis, L.M., Astudillo, A., Gavier-Pizarro, G. et al. Glossy privet (Ligustrum lucidum) invasion decreases Chaco Serrano forest bird diversity but favors its seed dispersers. Biol Invasions 23, 723–739 (2021). https://doi.org/10.1007/s10530-020-02399-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-020-02399-y