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Threatened birds, climate change, and human footprint: protected areas network in Neotropical grassland hotspot

Abstract

Climate change (CC) and human footprint (HF) shape species spatial patterns and may affect the effectiveness of Protected Areas (PAs) network. Spatial patterns of threatened bird species of Subtropical–temperate hotspots in Southeastern South American grasslands are relevant biodiversity features to guide conservation policies. However, the PAs network covers less than 1% of grassland areas and does not overlap areas with the most suitable environmental conditions for threatened birds. Our aim was to find the most environmentally suitable areas for both current and future threatened birds (2050 and 2070) in Entre Ríos. We applied Systematic Conservation Planning protocols with Ecological Niche Models (ENMs) and ZONATION using distribution interaction function and HF as a cost. Then we overlapped binary maps to find priority areas among time periods. HF showed a more fragmented spatial configuration. The PAs network may include environmentally suitable conditions for threatened birds in CC scenarios and HF. We found areas that showed more connectivity in landscape prioritization over time and ensure high-quality environmental conditions for birds. We concluded that the effectiveness of the PAs network could be improved by overlapping priority areas. Our approach provides a knowledge base as a contribution to conservation-related decisions by considering HF and CC.

Key words
climate change; human footprint; overlapped areas; protected area network; threatened birds

INTRODUCTION

Biodiversity loss is one of the main topics of global concern (Ceballos et al. 2015CEBALLOS G, EHRLICH, PR, BARNOSKY AD, GARCÍA A, PRINGLE RM & PALMER TM. 2015. Accelerated modern human-induced species losses: Entering the sixth mass extinction. Sci Adv 1(5). https://doi.org/10.1126/sciadv.1400253.
https://doi.org/10.1126/sciadv.1400253...
). Climate change (CC) and human footprint (HF) produce a synergistic effect on biodiversity loss and these effects will continue in the future (Borges & Loyola 2020BORGES FJA & LOYOLA R. 2020. Climate and land-use change refugia for Brazilian Cerrado birds. Perspec Ecol Conserv 18(2): 109-115. https://doi.org/10.1016/j.pecon.2020.04.002.
https://doi.org/10.1016/j.pecon.2020.04....
). Bird species often respond to climate change according to niche conservatism: when environmental conditions no longer match current species environmental tolerance, species need to change their spatial patterns (Triviño et al. 2018TRIVIÑO M, KUJALA H, ARAÚJO MB & CABEZA M. 2018. Planning for the future: identifying conservation priority areas for Iberian birds under climate change. Landscape Ecol 33: 659-673. https://doi.org/10.1007/s10980-018-0626-z.
https://doi.org/10.1007/s10980-018-0626-...
) and this may lead to modifications in the representativeness and effectiveness of the Protected Areas (PAs) network (Thomas & Gillingham 2015THOMAS CD & GILLINGHAM PK. 2015. The performance of protected areas for biodiversity under climate change. Biol J Linn Soc 115: 718-730. https://doi.org/10.1111/bij.12510.
https://doi.org/10.1111/bij.12510...
). Geographical distribution of species is one of the main biodiversity features that may enhance the representativeness of a PAs network (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
). Moreover, PAs do not often overlap with current biodiversity hotspots, especially in South America (Soutullo & Gudynas 2006SOUTULLO A & GUDYNAS E. 2006. How effective is the MERCOSUR’s network of protected areas in representing South America’s ecoregions? Oryx 40: 112-116.). Currently, they are established in pristine habitats generally surrounded by highly modified landscape matrices (Thomas & Gillingham 2015THOMAS CD & GILLINGHAM PK. 2015. The performance of protected areas for biodiversity under climate change. Biol J Linn Soc 115: 718-730. https://doi.org/10.1111/bij.12510.
https://doi.org/10.1111/bij.12510...
). However, these areas may not overlap with those spatial patterns of endangered species (Cristaldi et al. 2019CRISTALDI MA, SARQUIS A, ARZAMENDIA V, BELLINI P & GIRAUDO AR. 2019. Human activity and climate change as determinants of spatial prioritization for the conservation of globally threatened birds in the southern Neotropic (Santa Fe, Argentina). Biodivers conserv 28(10): 2531-2553.). The attributes of PAs networks may be enhanced by introducing scientific criteria into their planning and management (Giraudo et al. 2003GIRAUDO AR, KRAUCZUK E, ARZAMENDIA V & POVEDANO H. 2003. Chapter 3 - Critical Analysis of Protected Areas in the Atlantic Forest of Argentina, En: Atlantic Forest of the South America (Eds), Washington D. C., Biodiversity status, threats and outlook CABS y Island Press, p. 160-180.).

Spatial conservation prioritization allows analyzing distributions of various classes of biodiversity features and HF, such as threats, land cost, and opportunity costs for stakeholders (Moilanen et al. 2005MOILANEN A, FRANCO AMA, EARLY RI, FOX R, WINTLE B & THOMAS CD. 2005. Prioritizing multiple-use landscapes for conservation: methods for large multi-species planning problems. P R Soc London B Bio 272: 1885-1891. https://doi.org/10.1098/rspb.2005.3164.
https://doi.org/10.1098/rspb.2005.3164...
). Ecological Niche Modelling (ENM) allows finding association patterns among environmental variables and species occurrence and can provide useful ecological insights about species distribution dynamics over time (Soberón & Peterson 2005SOBERÓN J & PETERSON AT. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Inform 2: 1-10. https://doi.org/10.17161/bi.v2i0.4.
https://doi.org/10.17161/bi.v2i0.4...
).

Subtropical temperate hotspots of Southeastern South American grasslands (SESA Grasslands) in the province of Entre Ríos encompasses important bird areas (IBAs) that are threatened and overlap with the spatial distribution of endemic grassland birds (Azpiroz et al. 2012AZPIROZ AB, ISACCH JP, DIAS RA, DI GIACOMO A, SUERTEGARAY FONTANA C & MORALES PALAREA C. 2012. Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83: 217-246. http://doi.org/10.1111/j.1557-9263.2012.00372.x.
https://doi.org/10.1111/j.1557-9263.2012...
). SESA Grasslands are subject to some activities that cause habitat transformation and bird population decline, such as hunting, intensive agriculture and livestock (Giraudo et al. 2003GIRAUDO AR, KRAUCZUK E, ARZAMENDIA V & POVEDANO H. 2003. Chapter 3 - Critical Analysis of Protected Areas in the Atlantic Forest of Argentina, En: Atlantic Forest of the South America (Eds), Washington D. C., Biodiversity status, threats and outlook CABS y Island Press, p. 160-180.). In this context, the establishment of PAs can provide for threatened species, thus playing a significant role in the conservation of regional biodiversity (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
). However, the PAs network in SESA grasslands was established for opportunistic reasons (e.g. nonproductive areas, landscape beauties, availability of fiscal lands, flood lands) and covers less than 17% of grassland surface, which is the minimal threshold suggested by Aichi Biodiversity Target 11 (Juffe-Bignoli et al. 2014JUFFE-BIGNOLI D ET AL. 2014. Protected Planet Report 2014. UNEP-WCMC: Cambridge, UK., Azpiroz et al. 2012AZPIROZ AB, ISACCH JP, DIAS RA, DI GIACOMO A, SUERTEGARAY FONTANA C & MORALES PALAREA C. 2012. Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83: 217-246. http://doi.org/10.1111/j.1557-9263.2012.00372.x.
https://doi.org/10.1111/j.1557-9263.2012...
further revision). Also, most remnants of large grasslands are devoted to livestock and native grasslands are threatened by inappropriate management (Bilenca & Miñarro 2004BILENCA D & MIÑARRO F. 2004. Identificación de Áreas Valiosas de Pastizal (AVPs) en las Pampas y Campos de Argentina, Uruguay y sur de Brasil. Fundación Vida Silvestre, Buenos Aires, Argentina, 353 p.). Since the province of Entre Ríos still present natural patches with threatened bird populations that should be protected, spatial conservation prioritization might contribute to enhance the current PAs network.

Therefore, our aims were: (1) to model the ecological niche of 17 threatened bird species that inhabit SESA grasslands; (2) to assess the current PAs network in the province of Entre Ríos in relation to the current and future coverage of the most environmentally suitable areas for grassland bird species; and (3) to identify priority areas for PAs network expansion in order to enhance its representativeness and effectiveness for threatened birds over time.

MATERIALS AND METHODS

Study area

The province of Entre Ríos (Argentina) has a surface of 78,781 km2, bordered by the Guayquiraró River to the north and Basualdo Stream, Mocoretá River, and Las Tunas Stream to the South, by the Paraná River to the West, and by the Uruguay River to the East (Di Giacomo & Krapovickas 2005DI GIACOMO AS & KRAPOVICKAS S. 2005. Conserving the grassland Important Bird Areas (IBAs) of southern South America: Argentina, Uruguay, Paraguay, and Brazil, 1243-1249 in Ralph CJ and Rich TD (Eds), Bird conservation implementation and integration in the Americas: Proceedings of the Third International Partners in Flight Conference. 2005 March 20-24; Asilomar, California; Volume 2. Gen. Tech. Rep. PSW-GTR-191. Albany, CA: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture.). Entre Ríos encompasses four phytogeographical regions: Paranaense by the Uruguay River; Delta and Islands of Paraná River; Humid Chaco (all dominated by subtropical and riparian forests and wetlands); and Mesopotamic and Pampas grasslands, all being part of SESA grassland hotspot, which occupies most provincial surface (savannas, grasslands, and temperate open dry forests and shrublands called ‘Espinal’) (Di Giaccomo & Krapovickas 2005, Azpiroz et al. 2012AZPIROZ AB, ISACCH JP, DIAS RA, DI GIACOMO A, SUERTEGARAY FONTANA C & MORALES PALAREA C. 2012. Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83: 217-246. http://doi.org/10.1111/j.1557-9263.2012.00372.x.
https://doi.org/10.1111/j.1557-9263.2012...
) (Fig. 1).

Figure 1
Map of Argentina and the province of Entre Ríos. The background being used is shown on the left upper corner of the map of Argentina (gray area). Black dots represent the records of threatened birds that inhabit Entre Ríos. Numbers (1 and 2) represent the Protected Area Network.

Records of species occurrence

We found 17 threatened bird species according to the criteria established by the International Union for Conservation of Nature (IUCN 2020IUCN. 2020. The IUCN Red List of Threatened Species. Version 2020-2. www.iucnredlist.org. Downloaded on 09 July 2020.
www.iucnredlist.org...
). We obtained 1494 records (range of sample size: min=24 and max=200, see Supplementary Material – Table SI Figures S1, S2. Table SI. ). Occurrence data were obtained from: (1) museum collections; (2) scientific literature published from 1868 to 2020; (3) online data bases: (I) Sistema Nacional de Datos Biológicos (Argentine Biological Data System) (www.sndb.mincyt.gob.ar); (II) eBird (http://ebird/content/Argentina); (III) GBIF (www.gbif.org); (IV) Xenocanto (http://www.xeno-canto.org); (V) Ecoregistros (www.ecoregistros.org); and (4) 392 field work carried out between 1989 and 2018 throughout the country (Table SI). We only used georeferenced records with evidence (vouchers, photos, and bird singing records). We selected a background beyond the boundaries of the province of Entre Ríos including most of the distribution range of species for the following reasons: (1) scattering plays a crucial role in species distribution (Barve et al. 2011BARVE N, BARVE V, JIMÉNEZ-VALVERDE A, LIRA-NORIEGA A, MAHER SP, PETERSON AT, SOBERÓN J & VILLALOBOS F. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecol Modelling 222(11): 1810-1819. https://doi.org/10.1016/j.ecolmodel.2011.02.011.
https://doi.org/10.1016/j.ecolmodel.2011...
); (2) large backgrounds reduces the likelihood of biases due to historical events in the parametrization of ENM (explained below) (Owens et al. 2013OWENS HL, CAMPBELL LP, DORNAK LL, SAUPE EE, BARVE N, SOBERÓN J, INGENLOFF K, LIRA-NORIEGA A, HENSZ CM, MYERS CE & TOWNSEND PETERSON A. 2013. Constraints on interpretation of ecological niche models by limited environmental ranges on calibration areas. Ecol Modell 263: 10-18. https://doi.org/10.1016/j.ecolmodel.2013.04.011.
https://doi.org/10.1016/j.ecolmodel.2013...
); (3) we have a representative database at this spatial scale with 350,000 records (Zeng et al. 2016ZENG Y, LOW BW & YEO DCJ. 2016. Novel methods to select environmental variables in MaxEnt: a case study using invasive crayfish. Ecol Model 341: 5-13. https://doi.org/10.1016/J.ECOLMODEL.2016.09.019.
https://doi.org/10.1016/J.ECOLMODEL.2016...
); (4) this background includes accessibility areas of the studied species (part “M” of BAM diagram in Soberón & Peterson 2005SOBERÓN J & PETERSON AT. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Inform 2: 1-10. https://doi.org/10.17161/bi.v2i0.4.
https://doi.org/10.17161/bi.v2i0.4...
); and (5) the area is bounded by the Paraná and Uruguay Rivers and overlapped with the SESA grasslands and savannas inhabited by the studied species (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
, Azpiroz et al. 2012AZPIROZ AB, ISACCH JP, DIAS RA, DI GIACOMO A, SUERTEGARAY FONTANA C & MORALES PALAREA C. 2012. Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83: 217-246. http://doi.org/10.1111/j.1557-9263.2012.00372.x.
https://doi.org/10.1111/j.1557-9263.2012...
). We obtained a digital map of the current PAs network of Entre Ríos from UNEP-WCMC & IUCN (2021)UNEP-WCMC & IUCN. 2021. Protected Planet: The World Database on Protected Areas (WDPA) and World Database on Other Effective Area-based Conservation Measures (WD-OECM) [Online], May 2021, Cambridge, UK: UNEP-WCMC and IUCN. Available at: www.protectedplanet.net.
www.protectedplanet.net...
. We only considered those PAs included in categories I-IV of the IUCN (Dudley, 2008DUDLEY N. 2008. Directrices para la aplicación de las categorías de gestión de áreas protegidas. UICN, Gland, Suiza, 96 p.). Under this requirement, the PAs network currently covers 0.14% of the province (Fig. 1).

Environmental data

We used 19 climatic variables from WorldClim (http://www.worldclim.org/bioclim) for current and future conditions (2050 and 2070) and one topographical variable (altitude) obtained with R-package raster, with 2.5 x 2.5 arc-minute spatial resolution for South America (Hijmans et al. 2005HIJMANS RJ, CAMERON SE, PARRA JL, JONES PG & JARVIS A. 2005. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25: 1965-1978. https://doi.org/10.1002/joc.1276.
https://doi.org/10.1002/joc.1276...
). We assessed the effect of climate change on threatened bird species distribution using the Representative Concentration Pathways (RCP) 6 (van Vuuren et al. 2011VAN VUUREN ET AL. 2011. The Representative Concentration Pathways: An Overview. Clim Change 109(1): 5-31. https://doi.org/10.1007/s10584-011-0148-z.
https://doi.org/10.1007/s10584-011-0148-...
). The RCP 6 simulate climate system responses to increasing levels of green-house gases based on projected human population size, technological advances, and socio-economic trends with moderate changes in climate (Ferretti et al. 2018FERRETTI NE, ARNEDO M & GONZÁLEZ A. 2018. Impact of Climate Change on Spider Species Distribution Along the La Plata River Basin, Southern South America: Projecting Future Range Shifts for the Genus Stenoterommata (Araneae, Mygalomorphae, Nemesiidae). Ann Zool Fenn 55(1–3): 123-133. https://doi.org/10.5735/086.055.0112.
https://doi.org/10.5735/086.055.0112...
). A projection of climate change for 2050 and 2070 was used according to three Global Circulation Models (GCMs): The Community Climate System Model 4 (CCSM), the Hadley Centre Global Environmental Model 2 (HCGE), and the Coupled Model version 4.0 of Pierre Simon Laplace Institute (IPSL). Such models describe the atmospheric physics and dynamics and are used to simulate the global atmospheric circulation and provide weather forecasting (Krechemer & Marchioro, 2020KRECHEMER F & MARCHIORO CA. 2020. Past, Present and Future Distributions of Bumblebees in South America: Identifying Priority Species and Areas for Conservation.”JAppl Ecol 57(9): 1829-1839.39. https://doi.org/10.1111/1365-2664.13650.
https://doi.org/10.1111/1365-2664.13650...
). Also, these GCMs have been widely used in previous studies conducted in regions that overlap our study area (Maenza et al. 2017MAENZA RA, AGOSTA EA & BETTOLLI ML. 2017. “Climate Change and Precipitation Variability over the Western ‘Pampas’ in Argentina.” Int JClimatol 37: 445-463. https://doi.org/10.1002/joc.5014.
https://doi.org/10.1002/joc.5014...
, Velazco et al. 2021VELAZCO SJE, SVENNING JC, RIBEIRO BR & LAURETO LMO. 2021. “On Opportunities and Threats to Conserve the Phylogenetic Diversity of Neotropical Palms.” Divers Distrib 27(3): 512523. https://doi.org/10.1111/ddi.13215.
https://doi.org/10.1111/ddi.13215...
). Besides, they have been used to assess the spatial distributions of many species according to CC, ecosystems, and other long timescale components of the earth, including the simulations of the currently available RCPs (Santana et al. 2019SANTANA PA JR, KUMAR L, DA SILVA RS, PEREIRA JL & PICANÇO MC. 2019. Assessing the impact of climate change on the worldwide distribution of Dalbulus maidis (DeLong) using MaxEnt. Pest Manage Sci 75(10): 2706-2715. https://doi.org/10.1002/ps.5379.
https://doi.org/10.1002/ps.5379...
).

To avoid overfitting, we reduced the total set of determinants by dropping collinear variables as follows (Zuur et al. 2010ZUUR AF, IENO EN & ELPHICK CS. 2010. A protocol for data exploration to avoid common statistical problems. Methods Ecol Evol (1): 3-14. https://doi.org/10.1111/j.2041210X.
https://doi.org/10.1111/j.2041210X...
): (1) we carried out a Principal Component Analysis for both temperature and precipitation variables; (2) we selected the variables with the highest loads in the first and second main components; (3) we used the Variance Inflation factor (VIF) to detect collinearity between the retained variables in (2) and altitude. The five selected variables were: Mean Diurnal Range (Bio 2), Mean Temperature of Coldest Quarter (Bio 11), Annual Precipitation (Bio12), Precipitation of Warmest Quarter (Bio 18), and Altitude. We considered all variables in the final set for further analysis since they were not correlated (VIF < 5) (Dormann et al. 2013DORMANN CF ET AL. 2013. Collinearity: A review of methods to deal with it and a simulation study evaluating their performance. Ecography 36: 027-046. https://doi.org/10.1111/j.1600-0587.2012.07348.x.
https://doi.org/10.1111/j.1600-0587.2012...
). We fitted ENMs using all possible subsets of three, four, and five environmental predictors.

Environmental Niche Models

We conducted species-specific tuning of Maxent settings since it proved to be a simpler and substantially more realistic model than those built using default settings (Radosavljevic & Anderson, 2014). Since auto feature in MaxEnt may capture local idiosyncratic effects rather than broad physiological responses of species (Syfert et al. 2013SYFERT MM, SMITH MJ & COOMES DA. 2013. The Effects of Sampling Bias and Model Complexity on the Predictive Performance of MaxEnt Species Distribution Models. PLoS ONE 8(2). https://doi.org/10.1371/journal.pone.0055158.
https://doi.org/10.1371/journal.pone.005...
), we used linear and quadratic feature classes. Quadratic responses are suitable for unimodal curves, as expected for fundamental niches (Austin 2007AUSTIN M. 2007. Species distribution models and ecological theory: A critical assessment and some possible new approaches. Ecol Modelling 200(1-2): 1-19. https://doi.org/10.1016/j.ecolmodel.2006.07.005.
https://doi.org/.https://doi.org/10.1016...
). Finally, we tested 8 values for the regularization multiplier (0.5–4.0 at intervals of 0.5) and different combinations of the previously stated set of environmental variables. We randomly selected 70% of the data (both presence and background) to fit the models and held the remaining 30% for testing purposes, running one replicate per model. We evaluated the candidate model performance based on partial ROC (significance test), omission rates, and model complexity (AICc) (Galante et al. 2018GALANTE PJ, ALADE B, MUSCARELLA R, JANSA SA, GOODMAN SM & ANDERSON RP. 2018. The challenge of modeling niches and distributions for data-poor species: a comprehensive approach to model complexity. Ecography 41(5): 726-736. https://doi.org/10.1111/ecog.02909.
https://doi.org/10.1111/ecog.02909...
). The best models were selected according to Cobos et al. (2019)COBOS ME, TOWNSEND PETERSON A, BARVE N & OSORIO-OLVERA L. 2019. Kuenm: An R package for detailed development of ecological niche models using Maxent. PeerJ 2019(2): 1-15. https://doi.org/10.7717/peerj.6281.
https://doi.org/10.7717/peerj.6281...
using Rstudio (2015)RSTUDIO TEAM. 2015. RStudio: Integrated Development Environment for R. Boston, MA. Retrieved from http://www.rstudio.com/.
http://www.rstudio.com/...
: (1) significant models with (2) omission rates ≤5%. From this set, then, we selected those models with delta AICc values ≤2 as final models (Cobos et al. 2019COBOS ME, TOWNSEND PETERSON A, BARVE N & OSORIO-OLVERA L. 2019. Kuenm: An R package for detailed development of ecological niche models using Maxent. PeerJ 2019(2): 1-15. https://doi.org/10.7717/peerj.6281.
https://doi.org/10.7717/peerj.6281...
). We fitted MaxEnt models that met all previous criteria for all species except for Culicivora cuadacuta and Sporophila cinnamomea. The omission rate of the best models for these species were 5.3% and 5.9%, respectively. These values are lower than the 10th percentile presence threshold widely applied in the scientific literature (Radosavljevic & Anderson 2014RADOSAVLJEVIC A & ANDERSON RP. 2014. Making better Maxent models of species distributions: Complexity, overfitting and evaluation. J Biogeogr 41: 629-643. https://doi.org/10.1111/jbi.12227.
https://doi.org/10.1111/jbi.12227...
). Moreover, all models presented high values of partial ROC, and thus they were considered in further analysis.

Then we projected model predictions under future climate scenarios by 2050 and 2070. After that, we transformed ENM predictions into binary outputs using the Minimum Training Presence (MTP) value as a threshold. The MTP included all training presences with a zero-omission rate, a desired result when trying to define suitable areas for threatened species (Marcer et al. 2013MARCER A, SÁEZ L, MOLOWNY-HORAS R, PONS X & PINO J. 2013. Using species distribution modelling to disentangle realised versus potential distributions for rare species conservation. Biol Conserv 166: 221-230. https://doi.org/10.1016/j.biocon.2013.07.001.
https://doi.org/10.1016/j.biocon.2013.07...
). These binary maps were used to determine areas that each species may lose (become unsuitable), gain (suitable), and keep (remain unchanged) in the future with respect to current suitable conditions. Binary maps were drawn using Map Comparison Kit (MCK) 3.2.3 software (Visser & Nijs 2006VISSER H & NIJS T. 2006. The Map Comparison Kit. Environ Modell Soft 21(3): 346-358. https://doi.org/10.1016/j.envsoft.2004.11.013.
https://doi.org/10.1016/j.envsoft.2004.1...
http://www.riks.nl/mck). We overlapped binary predictions and we identified agreement/disagreement areas (Visser & Nijs 2006VISSER H & NIJS T. 2006. The Map Comparison Kit. Environ Modell Soft 21(3): 346-358. https://doi.org/10.1016/j.envsoft.2004.11.013.
https://doi.org/10.1016/j.envsoft.2004.1...
).

Landscape prioritization

We used ZONATION algorithm to identify priority areas for threatened birds in Entre Ríos for current and future conditions (Moilanen et al. 2005MOILANEN A, FRANCO AMA, EARLY RI, FOX R, WINTLE B & THOMAS CD. 2005. Prioritizing multiple-use landscapes for conservation: methods for large multi-species planning problems. P R Soc London B Bio 272: 1885-1891. https://doi.org/10.1098/rspb.2005.3164.
https://doi.org/10.1098/rspb.2005.3164...
). ZONATION generates a hierarchical and nested prioritization of a landscape by removing the least valuable cells from the landscape while minimizing marginal loss of the conservation value (Moilanen et al. 2005MOILANEN A, FRANCO AMA, EARLY RI, FOX R, WINTLE B & THOMAS CD. 2005. Prioritizing multiple-use landscapes for conservation: methods for large multi-species planning problems. P R Soc London B Bio 272: 1885-1891. https://doi.org/10.1098/rspb.2005.3164.
https://doi.org/10.1098/rspb.2005.3164...
). We did not use the background to identify priority areas since the management of natural resources in Argentina are managed by each province. We considered two alternative prioritization criteria that complement each other (Moilanen et al. 2014MOILANEN A, POUZOLS FM, MELLER L, VEACH V, ARPONEN A, LEPPÄNEN J & KUJALA H. 2014. Spatial conservation planning methods and software Zonation. User Manual. https://doi.org/10.1017/CBO9781107415324.004.
https://doi.org/10.1017/CBO9781107415324...
): (1) core-area ZONATION (CAZ), which emphasizes areas with the highest suitability scores for each species; and (2) the additive-benefit function (ABF), to favor species-rich areas over areas with a high occurrence value for just one or a few species (Moilanen et al. 2005MOILANEN A, FRANCO AMA, EARLY RI, FOX R, WINTLE B & THOMAS CD. 2005. Prioritizing multiple-use landscapes for conservation: methods for large multi-species planning problems. P R Soc London B Bio 272: 1885-1891. https://doi.org/10.1098/rspb.2005.3164.
https://doi.org/10.1098/rspb.2005.3164...
). When compared to CAZ, the ABF method considers all (weighted) feature proportions in each cell instead of only one feature that has the highest value (Moilanen et al. 2014MOILANEN A, POUZOLS FM, MELLER L, VEACH V, ARPONEN A, LEPPÄNEN J & KUJALA H. 2014. Spatial conservation planning methods and software Zonation. User Manual. https://doi.org/10.1017/CBO9781107415324.004.
https://doi.org/10.1017/CBO9781107415324...
). As a result, we may have a more connected landscape prioritization but this does not necessarily mean that those areas are better for each target species (Moilanen et al. 2014MOILANEN A, POUZOLS FM, MELLER L, VEACH V, ARPONEN A, LEPPÄNEN J & KUJALA H. 2014. Spatial conservation planning methods and software Zonation. User Manual. https://doi.org/10.1017/CBO9781107415324.004.
https://doi.org/10.1017/CBO9781107415324...
). Furthermore, we used the distribution interactions component of ZONATION to find areas that overlap with current and projected future conditions (Rayfield et al. 2009RAYFIELD B, MOILANEN A & FORTIN MJ. 2009. Incorporating consumer-resource spatial interactions in reserve design. Ecol Model 220: 725-733. https://doi.org/10.1016/j.ecolmodel.2008.11.016.
https://doi.org/10.1016/j.ecolmodel.2008...
). This component transforms the distribution of one conservation target (current distribution) according to its proximity to the distribution of another conservation target (future distribution) and provides high values where both distributions overlap (Carroll et al. 2010CARROLL C, DUNK JR & MOILANEN A. 2010. Optimizing resiliency of reserve networks to climate change: Multispecies conservation planning in the Pacific Northwest, USA. Global Change Biol 16(3): 891-904. https://doi.org/10.1111/j.1365-2486.2009.01965.x.
https://doi.org/10.1111/j.1365-2486.2009...
). We parameterized the interaction between current and future distribution as a positive value because it is possible to identify priority areas that are currently valuable and may coincide with the expected future distribution areas for bird species (Carroll et al. 2010CARROLL C, DUNK JR & MOILANEN A. 2010. Optimizing resiliency of reserve networks to climate change: Multispecies conservation planning in the Pacific Northwest, USA. Global Change Biol 16(3): 891-904. https://doi.org/10.1111/j.1365-2486.2009.01965.x.
https://doi.org/10.1111/j.1365-2486.2009...
). We considered the Human Footprint (HF) as ‘cost’ because threatened birds in Entre Ríos are affected by HF (Wildlife Conservation Society 2005WILDLIFE CONSERVATION SOCIETY - WCS. 2005. Center for International Earth Science Information Network - CIESIN - Columbia University. Last of the Wild Project, Version 2, 2005 (LWP-2): Global Human Influence Index (HII) Dataset (Geographic). Palisades, NY: NASA Socioeconomic Data and Applications Center http://dx./10.7927/H4BP00QC. Accessed: 9/2/2018.
http://dx./10.7927/H4BP00QC...
). We performed the analysis with CAZ and ABF considering two different scenarios: (1) one included all ENM predictions for all threatened bird species and the current PAs network (CAZ 1 and ABF 1, respectively), and (2) the other one consisted of scenario 1 including HF (CAZ 2 and ABF 2, respectively).

To show consensus areas among priority areas for the GCMs, we reclassified each ZONATION landscape prioritization on a binary map, using the first 17% as a threshold (from 0 to 82.99% and 83% to 100%) and we overlapped them using Map Comparison Kit (MCK). The purpose was to find out if the province could still meet the Aichi Biodiversity Target 11 for threatened bird species and to identify the representativeness and effectiveness of the PAs system of the province over time.

RESULTS

Environmental data and predictors

The analysis selected 16 subsets with combinations among three and five of 19 environmental predictors and the altitude to model environmentally suitable areas for species. Bio 18 (Precipitation of Warmest Quarter), Bio 2 (Mean Diurnal Range), Bio 11 and 12 (Mean Temperature of Coldest Quarter and Annual Precipitation respectively), and altitude are among the main environmental predictors for most species. All significant ENMs presented a low omission rate since it was lower than the 10th percentile for all species and lower than the 5th percentile for most of them. Therefore, we included all species in the spatial prioritization (Table SI).

Species distribution models

Results showed that some of the current environmentally suitable areas for all species will remain. On the other hand, we observed substantial changes in spatial patterns of environmental suitability for all species in the different GCMs. All of them, however, will keep areas with their current environmentally suitable space within the province. Asthenes hudsoni, Limnoctites rectirostris, Spartonoica maluroices, and Sporophila ruficollis might lose more than 25% of their current environmentally suitable areas according to some GCMs. Alectrurus risora, Calidris subruficollis, L. rectirostris, S. maluroides, S. hypochroma, and S. ruficollis might keep less than 50% of their current environmentally suitable conditions; the remaining species will maintain more than 50%. Finally, A. risora, C. subruficollis, Eleothreptus anomalus and Sporophila palustris might gain 40% of their current environmentally suitable conditions in new areas. All species showed highest values of environmentally suitable conditions in riverside areas. Specifically, A. risora, A. hudsoni, C. subruficollis, E. anomalus, Polystictus pectoralis, Rhea. americana, S. maluroides, S. cinnamomea, S. hypochroma, S. palustris, S. ruficollis, and Xanthopsar flavus showed the highest values of environmentally suitable conditions in both Paraná River and its Delta and Uruguay River by 2070 (Fig. 2 and Figure S1). Culicivora caudacuta, Gubernatrix cristata, Sturnella defilippii and Xolmis dominicanus showed highest values of environmentally suitable conditions only in the Uruguay River, and L. rectirostris did so in the Delta of the Paraná River (Figure S1).

Figure 2
Bar plot showing the average percentage of environmental suitability that each species wins, lose, and keep between current predictions and the average of future predictions.

Spatial conservation prioritization

The PAs network of Entre Ríos does not overlap with the most environmentally suitable areas for threatened bird species for present and future. Also, no differences were found in the spatial prioritization when including the current PAs network in the analysis. The Delta of the Paraná River and the Lower Uruguay River always reached the first 17% of the landscape prioritization, showing high conservation scores (Fig. 3 red areas and Figure S2). North areas reached the highest conservation scores only in CAZ 1. The center region never reached priority scores. Priority areas are mainly concentrated in the south of the province. Overall, priority areas might change their position from the northwest to the southeast by 2050 and 2070 even though Paraná and Uruguay Rivers always reached the first 17%. Priority areas overlapping shows landscape connections between the Delta of the Paraná and Uruguay Rivers, and both might maintain suitable conditions for birds in future. Unfortunately, no priority areas connect the northern with the southern region (Fig. 3).

Figure 3
Spatial prioritization areas for the threatened bird species that inhabit Entre Ríos province considering years 2050-2070 and Global Circulation Models. PAs are represented in black dotted circles. Areas with more overlapped spatial prioritizations are shown in red; those with less overlapped spatial prioritizations are shown in blue and those with intermediate scores are depicted in green and yellow. CAZ 1: it includes the overlapped spatial prioritizations obtained with Core Area Zonation and Protected Areas Networks. CAZ 2: it includes CAZ 1 but obtained with Human Footprint. ABF 1 and ABF 2 are like CAZ 1 and CAZ 2 respectively but with Additive Benefit Function (ABF).

Human Footprint substantially affected those priority areas selected in CAZ 2 and ABF 2 with a more fragmented spatial configuration, i.e. there was a larger number of patches with different sizes and shapes and a larger perimeter mainly located in the Delta of the Paraná River and in the north (Fig. 3 and Figure S2).

Priority areas present a wider variation across removal rules (CAZ and ABF) than GCMs and the different periods. CAZ 1 showed important areas in the north and south along the boundaries of rivers. CAZ 2 showed a shift to the north/center, excluding the Paraná and Uruguay Rivers in the north as priority areas. ABF 1 selected the southwest corner and areas along the Uruguay River. CAZ 2 showed a thinning of priority areas in the north over time: it will almost disappear as a priority area in ABF 2 (Figure S2) but it will remain being a priority area in CAZ 2 even though with a substantial surface reduction.

DISCUSSION

Our results show that Climate Change turns some areas environmentally unsuitable and causes some others to become suitable for threatened birds in Entre Ríos. As a pattern, suitable areas will switch from the north to the south and from the west to the east. Also, environmental suitability in some areas will remain almost unchanged in the future and, consequently, the province will be able to offer shelter for threatened bird species in the future. These refuges offered by priority areas present a balance between CC, HF, and threatened bird species persistence over time. We found priority areas using both removal rules (CAZ and ABF), which are necessary to improve the current PAs network. Furthermore, the distribution interactions component of ZONATION shows more aggregated priority areas with local habitat quality for all bird species. On the other hand, overlapped maps display potentially important areas even in 2050 and 2070. These two methods expose a simplified way to understand a possible pattern among suitable areas for species, CC, and HF, which helps stakeholders to make decisions on which areas must be protected.

Species distribution models

Climate change may affect the spatial patterns of environmentally suitable areas for threatened bird species and, consequently, the latter may respond by changing their distribution in their search for new sheltering places (Triviño et al. 2018TRIVIÑO M, KUJALA H, ARAÚJO MB & CABEZA M. 2018. Planning for the future: identifying conservation priority areas for Iberian birds under climate change. Landscape Ecol 33: 659-673. https://doi.org/10.1007/s10980-018-0626-z.
https://doi.org/10.1007/s10980-018-0626-...
). Although our models predicted suitable environmental conditions for species by 2050 and 2070, we found differences in bird responses. For instance, A. risora and L. defilippi may gain suitable areas in Entre Ríos where they used to inhabit in the past and disappeared because of agricultural expansion (Di Giacomo & Krapovickas 2005DI GIACOMO AS & KRAPOVICKAS S. 2005. Conserving the grassland Important Bird Areas (IBAs) of southern South America: Argentina, Uruguay, Paraguay, and Brazil, 1243-1249 in Ralph CJ and Rich TD (Eds), Bird conservation implementation and integration in the Americas: Proceedings of the Third International Partners in Flight Conference. 2005 March 20-24; Asilomar, California; Volume 2. Gen. Tech. Rep. PSW-GTR-191. Albany, CA: Pacific Southwest Research Station, Forest Service, U.S. Department of Agriculture.). Both species show marked niche conservatism, so they will change their spatial patterns (almost 50%) when trying to find shelter (Borges & Loyola 2020BORGES FJA & LOYOLA R. 2020. Climate and land-use change refugia for Brazilian Cerrado birds. Perspec Ecol Conserv 18(2): 109-115. https://doi.org/10.1016/j.pecon.2020.04.002.
https://doi.org/10.1016/j.pecon.2020.04....
). Entre Ríos still presents natural grassland patches in the north and in the east; therefore, both species may still find sheltering areas to inhabit. The Uruguay River and its intersection with the Delta of the Paraná River presented high suitability scores for Sporophila cinnamomea, S. hypochroma, S. palustris, X. flavus and X. dominicanus (Fig. 3, Figure S1, S2 for a revision). The Uruguay River covers a variety of habitats that can be used by these species, such as wetlands with humid grasslands, savannas, and forests. In Entre Ríos, species of the genus Sporophila inhabit grasslands and wetlands mainly affected by agricultural expansion over their habitats (Thompson et al. 2013THOMPSON JJ, GOIJMAN AP & BERNARDOS JN. 2013. Influencia de la agriculturización sobre aves de pastizal en la región central de Argentina, in: Marino GD, Miñarro F, Zaccagnini ME and López-Lanús B (Eds), Pastizales y sabanas del cono sur de Sudamérica: iniciativas para su conservación en la Argentina. Temas de naturaleza y conservación, Monografía de Aves Argentinas Nº 9. Buenos Aires: Aves Argentinas/AOP, Fundación Vida Silvestre Argentina e Instituto Nacional de Tecnología Agropecuaria. Buenos Aires, Argentina, 574 p.). Entre Ríos present priority areas that overlap with SESA grasslands in the south (Delta of the Paraná River) and in the north (Selva de Montiel) for all threatened species of the genus Sporophila; thus, they should be considered in future management decisions (Fig. 1 and 3). Predictions for X. flavus and X. dominicanus showed highly suitable areas in the southern areas of SESA grasslands (as stated by Azpiroz et al. 2012AZPIROZ AB, ISACCH JP, DIAS RA, DI GIACOMO A, SUERTEGARAY FONTANA C & MORALES PALAREA C. 2012. Ecology and conservation of grassland birds in southeastern South America: a review. J Field Ornithol 83: 217-246. http://doi.org/10.1111/j.1557-9263.2012.00372.x.
https://doi.org/10.1111/j.1557-9263.2012...
, Di Giacomo & Kaprovickas 2005). Moreover, SESA grasslands are affected by CC, especially in relation to seasonal precipitations. More extreme precipitation events change the natural variability of seasonal precipitation (Grimm 2011GRIMM AM. 2011. Interannual climate variability in South America: Impacts on seasonal precipitation, extreme events, and possible effects of climate change. Stochastic Environ Res Risk Assess 25(4): 537-554. https://doi.org/10.1007/s00477-010-0420-1.
https://doi.org/10.1007/s00477-010-0420-...
) and, therefore, can further affectthreatened bird species. This could be the reason why four in five climatic variables used to construct model predictions were related to precipitation even though there is a wide variety of predictors that must be consider to model species distribution (see BAM diagram in Soberón & Peterson 2005SOBERÓN J & PETERSON AT. 2005. Interpretation of models of fundamental ecological niches and species’ distributional areas. Biodiversity Inform 2: 1-10. https://doi.org/10.17161/bi.v2i0.4.
https://doi.org/10.17161/bi.v2i0.4...
). However, our priority areas coincide with those obtained with alternative criteria in other studies (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
, Di Giacomo & Kaprovickas 2005, Giraudo et al. 2003GIRAUDO AR, KRAUCZUK E, ARZAMENDIA V & POVEDANO H. 2003. Chapter 3 - Critical Analysis of Protected Areas in the Atlantic Forest of Argentina, En: Atlantic Forest of the South America (Eds), Washington D. C., Biodiversity status, threats and outlook CABS y Island Press, p. 160-180., Giraudo & Arzamendia 2018GIRAUDO AR & ARZAMENDIA V. 2018. Descriptive bioregionalisation and conservation biogeography: What is the true bioregional representativeness of protected areas? Aust Syst Bot 30: 403-413. https://doi.org/10.1071/SB16056.
https://doi.org/10.1071/SB16056...
).

Spatial prioritization for conservation

We obtained priority areas for threatened birds with the aim of ensuring current and future conservation. We found that the obtained priority areas with high species richness may underrepresent the spatial distribution of some species such as A. risora and A. hudsoni. C. caudacuta, G. cristata, R. americana and S. ruficollis. Some species lose environmentally suitable areas in Entre Ríos but gain areas in other provinces or countries. It is important to consider ecological and biogeographical processes rather than political boundaries when making decisions and conducting studies on conservation strategies (Leach et al. 2013LEACH K, ZALAT S & GILBERT F. 2013. Egypt’s Protected Area network under future climate change. Biol Conserv 159: 490-500. https://doi.org/10.1016/j.biocon.2012.11.025.
https://doi.org/10.1016/j.biocon.2012.11...
). In Argentina, however, each province supervises the management of natural resources within its boundaries, so that conservation policies and strategies in Entre Ríos should be coordinated with those proposed and implemented by neighboring provinces.

The current PAs network of Entre Ríos does not comprise the best environmentally suitable areas for threatened birds and SESA grasslands, which is a common situation in Argentina, where PAs were established for opportunistic reasons, without scientific criteria and planning (Giraudo et al. 2003GIRAUDO AR, KRAUCZUK E, ARZAMENDIA V & POVEDANO H. 2003. Chapter 3 - Critical Analysis of Protected Areas in the Atlantic Forest of Argentina, En: Atlantic Forest of the South America (Eds), Washington D. C., Biodiversity status, threats and outlook CABS y Island Press, p. 160-180.). In fact, only 5% of grassland regions in South America is protected under IUCN categories I–IV with scientific criteria (Soutullo & Gudynas 2006SOUTULLO A & GUDYNAS E. 2006. How effective is the MERCOSUR’s network of protected areas in representing South America’s ecoregions? Oryx 40: 112-116.).

Trade-offs between spatial patterns of species and HF must be considered to improve the current PAs network and minimize conflicts with anthropogenic uses (Dorning et al. 2015DORNING MA, KOCH J, SHOEMAKER DA & MEENTEMEYER RK. 2015. Simulating urbanization scenarios reveals tradeoffs between conservation planning strategies. Landsc Urban Plann 136: 28-39. https://doi.org/10.1016/j.landurbplan.2014.11.011.
https://doi.org/10.1016/j.landurbplan.20...
). Spatial patterns of HF affected the spatial prioritization process and thus we obtained a priority area network with a more fragmented spatial configuration (Suri et al. 2017SURI J, ANDERSON PM, CHARLES-DOMINIQUE T, HELLARD E & CUMMING GS. 2017. More than just a corridor: a suburban river catchment enhances bird functional diversity. Landsc Urban Plann 157: 331-342. https://doi.org/10.1016/J.LANDURBPLAN.2016.07.013.
https://doi.org/10.1016/J.LANDURBPLAN.20...
). Even though HF pushes priority areas to other sites, it is important to account for human activities to solve human–nature conflicts (Dickman 2010DICKMAN AJ. 2010. Complexities of conflict: the importance of considering social factors for effectively resolving human–wildlife conflict. Anim Conserv 13: 458-466. https://doi.org/10.1111/j.1469-1795.2010.00368.x.
https://doi.org/10.1111/j.1469-1795.2010...
). However, the biggest selected patches overlapped ‘Selva de Montiel’ -the only IBA of the north- in both time periods. Although this region did not present the most environmentally suitable areas for birds, it might offer shelter and food for threatened birds, which turns it a key region to be conserved (Dardanelli et al. 2018DARDANELLI S, REALES CF & SARQUIS JA. 2018. Avifaunal inventory of northern Entre Ríos, Argentina: noteworthy records and conservation prospects. Rev Mus Argentino Cienc Nat 20(2): 217-227. https://doi.org/10.22179/REVMACN.20.577.
https://doi.org/10.22179/REVMACN.20.577...
). The selection of the Delta of the Paraná River and the Lower Uruguay River as priority areas may offer great conservation opportunities for threatened birds. Moreover, other findings in the region showed important areas for snakes and proposed these rivers as corridors (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
, Giraudo & Arzamendia 2018GIRAUDO AR & ARZAMENDIA V. 2018. Descriptive bioregionalisation and conservation biogeography: What is the true bioregional representativeness of protected areas? Aust Syst Bot 30: 403-413. https://doi.org/10.1071/SB16056.
https://doi.org/10.1071/SB16056...
).

We observed that the distribution interactions component of ZONATION provides results considering niche conservatism, since it shows high values on overlapped areas with present and future conditions. This is mostly expected in birds that tend to conserve their niches (Triviño et al. 2018TRIVIÑO M, KUJALA H, ARAÚJO MB & CABEZA M. 2018. Planning for the future: identifying conservation priority areas for Iberian birds under climate change. Landscape Ecol 33: 659-673. https://doi.org/10.1007/s10980-018-0626-z.
https://doi.org/10.1007/s10980-018-0626-...
). Also, the province of Entre Ríos do not present geographical barriers that could affect the bird species under study. The Paraná and Uruguay Rivers favor accessibility and displacement for birds and other species acting as biological corridors (Arzamendia & Giraudo 2012ARZAMENDIA V & GIRAUDO AR. 2012. A panbiogeographical model to prioritize areas for conservation along large rivers. Divers Distrib 18(1): 168-179. https://doi.org/10.1111/j.1472-4642.2011.00829.x.
https://doi.org/10.1111/j.1472-4642.2011...
). Hence, considering the distribution interactions component function of ZONATION allows for a more reliable reflection of the possible effect of CC on threatened bird species of Entre Ríos. We found that map overlapping using Map Comparison Kit is a useful tool that provides reliable results and shows more connected landscapes. It provides the possibility of understanding slipping patterns of CC and HF. This allows the scientific community and stakeholders to identify important areas that remain ‘unalterable’ and/or fixed like APs, or the Delta and islands of the Paraná River.

On the other hand, there are other predictors affecting population distribution, and thus stakeholders and decision makers must consider this biological approach and all social parties should be involved in the conservation process. Therefore, depending on the area and species, it would be necessary to (1) consider reintroduction programs for A. risora and S. defilippi (Smeraldoa et al. 2017SMERALDOA S, DI FEBBRARO M, CIROVIÓC C, BOSSO J, TRBOJEVIÓC I & RUSSO D. 2017. Species distribution models as a tool to predict range expansion after reintroduction: A case study on Eurasian beavers (Castor fiber). J Nat Conserv 37: 12-20. https://doi.org/10.1016/J.JNC.2017.02.008.
https://doi.org/10.1016/J.JNC.2017.02.00...
); (2) mitigate antropogenic systems and agricultural land use for all species but especially for Sporophila groups, X. flavus and X. dominicanus; (3) select corridors for species such as example Calidris subruficollis, L. rectirostris, Polystictus pectoralis, and Spartonoica maluroides (Suri et al. 2017SURI J, ANDERSON PM, CHARLES-DOMINIQUE T, HELLARD E & CUMMING GS. 2017. More than just a corridor: a suburban river catchment enhances bird functional diversity. Landsc Urban Plann 157: 331-342. https://doi.org/10.1016/J.LANDURBPLAN.2016.07.013.
https://doi.org/10.1016/J.LANDURBPLAN.20...
); and (4) include social factors and education in order to effectively solve human-wildlife conflicts (Dickman 2010DICKMAN AJ. 2010. Complexities of conflict: the importance of considering social factors for effectively resolving human–wildlife conflict. Anim Conserv 13: 458-466. https://doi.org/10.1111/j.1469-1795.2010.00368.x.
https://doi.org/10.1111/j.1469-1795.2010...
) and mitigate the effects of CC on threatened species distribution.

ACKNOWLEDGMENTS

This work was supported by: CONICET (PIP 2014-700), Universidad Nacional del Litoral (CAID-2016-UNL, CAID-UNL-2020), and ANPCYT (PICT 2017-3610). We thank Lorena Sovrano, Evelina León, Rodrigo Lorenzón, Ignacio Berón, María Eugenia Rodriguez, Romina Pavé, and the Instituto Nacional de Limnología (INALI-CONICET-UNL) for collaborating with our work.

SUPPLEMENTARY MATERIAL

Figures S1, S2.

Table SI.

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Publication Dates

  • Publication in this collection
    05 Sept 2022
  • Date of issue
    2022

History

  • Received
    12 Nov 2020
  • Accepted
    11 Oct 2021
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