Abstract
Riparian habitats are key landscape elements promoting regional biodiversity, particularly in areas where water availability is scarce. In Mediterranean Iberia, the microclimatic conditions that occur near rivers support the development of humid riparian woodlands, which differ markedly from those growing in equivalent upland areas but share structural and compositional similarities with higher-latitude (Atlantic) formations. However, the effects of this variation on the animal species assemblages inhabiting each woodland type have not been well-documented. We characterized the vegetation of riparian and upland woodlands (general structure and composition) and their avian breeding communities (diversity, climatic and habitat preferences) in 38 sites across mainland Spain to explore how these characteristics changed across a climatic gradient of increasing summer drought. Our results revealed that the prevalence of deciduous woody plants decreased with increasing summer drought. However, this reduction was less steep in riparian than in upland woodlands, reinforcing the idea that Mediterranean riparian areas act as microclimatic refugia where more Atlantic (deciduous) woody species can persist. We also found a lower similarity between riparian and upland bird assemblages in areas with higher indices of summer drought, making riparian woodlands comparatively more diverse than upland woodlands in the Mediterranean. This pattern was partly attributed to the presence of deciduous-tree-related bird species that could not persist in equivalent upland woodlands. These findings suggest that restoring habitat of riparian woodlands would provide refuges with suitable conditions for many woodland species whose persistence on the limit of their distribution range in southern Iberia is threatened by global warming.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data available at the Supplementary Information section (Appendix 1) and at the figshare repository: 10.6084/m9.figshare.25425913.
References
Alena H, Jan D, Jana D (2022) Threats, biodiversity drivers and restoration in temperate floodplain forests related to spatial scales. Sci Total Environ 854:158743. https://doi.org/10.1016/j.scitotenv.2022.158743
Baldocchi DD, Ma S, Rambal S, Misson L, Ourcival J, Limousin J, Pereiraç J, Papale D (2010) On the differential advantages of evergreenness and deciduousness in mediterranean oak woodlands: a flux perspective. Ecol Appl 20:1583–1597. https://doi.org/10.1890/08-2047.1
Barnagaud J-Y, Devictor V, Jiguet F, Barbet-Massin M, Le Viol I, Archaux F (2012) Relating habitat and climatic niches in birds. PLoS ONE 7(3):e32819. https://doi.org/10.1371/journal.pone.0032819
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48
Bennett S, Wernberg T, Arackal Joy B, De Bettignies T, Campbell AH (2015) Central and rear-edge populations can be equally vulnerable to warming. Nat Commun 6(1):10280. https://doi.org/10.1038/ncomms10280
Biurrun I, Campos JA, García-Mijangos I, Herrera M, Loidi J (2016) Floodplain forests of the Iberian Peninsula: vegetation classification and climatic features. Appl Veg Sci 19(2):336–354. https://doi.org/10.1111/avsc.12219
Blondel J, Farré H (1988) The convergent trajectories of bird communities along ecological successions in European forests. Oecologia 75:83–93. https://doi.org/10.1007/BF00378818
Blondel J, Aronson J, Bodiou JY, Boeuf G (2010) The Mediterranean region: biological diversity in space and time. Oxford University Press
Brinson M (1990) Riverine forests. In: Lugo AE, Brinson M, Brown S (eds) Forested wetlands. Ecosystems of the world 15. Elsevier, Amsterdam, pp 87–143
Bub BR, Flaspohler DJ, Huckins CJF (2004) Riparian and upland breeding-bird assemblages along headwater streams in Michigan’s Upper Peninsula. J Wildl Manage 68(2):383–392. https://www.jstor.org/stable/3803314
Camprodon J, Plana E (2001) Conservación De La Biodiversidad Y Gestión Forestal. Su Aplicación en la Fauna Vertebrada. Edicions Universitat de Barcelona, Barcelona
Clerici N, Weissteiner CJ, Paracchini LM, Strobl P (2011) Riparian zones: where green and blue networks meet: pan-European zonation modelling based on remote sensing and GIS. JRC Scientific and Technical Reports
Cooper SD, Lake PS, Sabater S, Melack JM, Sabo JL (2013) The effects of land use changes on streams and rivers in mediterranean climates. Hydrobiologia 719:383–425. https://doi.org/10.1007/s10750-012-1333-4
R Core Team (2022) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Costa-Tenorio M, Morla Juaristi C, Sainz-Ollero H (2005) Los Bosques Ibéricos. Una interpretación geobotánica. Editorial Planeta, Barcelona
Sánchez de Dios R, Benito-Garzón M, Sáinz-Ollero H (2009) Present and future extension of the Iberian submediterranean territories as determined from the distribution of marcescent oaks. Plant Ecol 204:189–205. https://www.jstor.org/stable/40305759
De Meester L, Stoks R, Brans KI (2018) Genetic adaptation as a biological buffer against climate change: potential and limitations. Integr Zool 13(4):372–391
Devictor V, Julliard R, Couvet D, Jiguet F (2008) Birds are tracking climate warming, but not fast enough. Proc Royal Soc B 275:2743–2748. https://doi.org/10.1098/rspb.2008.0878
Dudgeon D, Arthington AH, Gessner MO, Kawabata ZI, Knowler DJ et al (2006) Freshwater biodiversity: importance, threats, status and conservation challenges. Biol Rev 81(2):163–182. https://doi.org/10.1017/S1464793105006950
EU Habitats Directive (1992) [online] Available at: https://ec.europa.eu/environment/nature/legislation/habitatsdirective/index_en.htm [Accessed 13 March 2023]
EU Water Framework Directive (2000) [online] Available at: https://environment.ec.europa.eu/topics/water/water-framework-directive_en [Accessed 13 March 2023]
Font I (1983) Climatología De España Y Portugal. Instituto Nacional de Meteorología, Madrid
Gaget E, Devictor V, Frochot B, Desbrosses R, Eybert MC, Faivre B (2021) Disentangling the latitudinal and altitudinal shifts in community composition induced by climate change: the case of riparian birds. J Biogeogr 48(3):526–536. https://doi.org/10.1111/jbi.14016
Gasith A, Resh VH (1999) Streams in Mediterranean climate regions: abiotic influences and biotic responses to predictable seasonal events. Annu Rev Ecol Evol Syst 30(1):51–81. https://doi.org/10.1146/annurev.ecolsys.30.1.51
Gaussen H, Bagnouls F (1953) Saison sèche et indice xérothermique. Toulouse. Université de Toulouse, Facultei dês Sciences, França
Gil-Tena A, Saura S, Brotons L (2007) Effects of forest composition and structure on bird species richness in a Mediterranean context: implications for forest ecosystem management. Ecol Manag 242:470–476. https://doi.org/10.1016/j.foreco.2007.01.080
González E, González-Sanchis M, Cabezas A, Comín FA, Muller E (2010) Recent changes in the riparian forest of a large regulated Mediterranean river: implications for management. Environ Manage 45:669–681
Habibzadeh N, Ghoddousi A, Bleyhl B, Kuemmerle T (2021) Rear-edge populations are important for understanding climate change risk and adaptation potential of threatened species. Conserv Sci Pract 3(5):e375. https://doi.org/10.1111/csp2.375
Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8(5):461–467. https://doi.org/10.1111/j.1461-0248.2005.00739.x
Helle P, Mönkkönen M (1990) Forest successions and bird communities: theoretical aspects and practical implications. In: Keast A (ed) Biogeography and ecology of forest bird communities, The Hague, SPB Academic Publishing, pp 299–318
Herrero A, Zavala MA (2015) Los Bosques Y La Biodiversidad Frente Al Cambio Climático: Impactos, Vulnerabilidad Y Adaptación en España. Documento De Síntesis. Ministerio de Agricultura, Alimentación y Medio Ambiente, Madrid
Jiguet F, Gadot AS, Julliard R, Newson SE, Couvet D (2007) Climate envelope, life history traits and the resilience of birds facing global change. Glob Chang Biol 13(8):1672–1684. https://doi.org/10.1111/j.1365-2486.2007.01386.x
Jost L (2006) Entropy and diversity. Oikos 113:363–375. https://doi.org/10.1111/j.2006.0030-1299.14714.x
Kim H, McComb BC, Frey SJ, Bell DM, Betts MG (2022) Forest microclimate and composition mediate long-term trends of breeding bird populations. Glob Chang Biol 28(21):6180–6193. https://doi.org/10.1111/gcb.16353
Kuznetsova A, Brockhoff P, Christensen R (2017) lmerTest Package: tests in Linear mixed effects models. J Stat Softw 82:1–26
Martí R, Del Moral JC (2004) Atlas de las Aves reproductoras de España. Dirección General de la Conservación de la Naturaleza-Sociedad Española de Ornitología, Madrid
Mingarro M, Lobo JM (2021) Connecting protected areas in the Iberian peninsula to facilitate climate change tracking. Environ Conserv 48(3):182–191. https://doi.org/10.1017/S037689292100014X
Molina B, Nebreda A, Muñoz AR, Seoane J, Real R, Bustamante J, Moral JD (2022) III Atlas de las aves en época de reproducción en España. SEO/BirdLife, Madrid
Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Oksanen J, Blanchet FG, Kindt R, Legendre P, O’Hara RB et al (2018) vegan: Community Ecology Package. R package versión 2.5-7
Peñuelas J, Sardans J, Filella I, Estiarte M, Llusià J, Ogaya R et al (2017) Impacts of global change on Mediterranean forests and their services. Forests 8:463. https://doi.org/10.3390/f8120463
Pereira P, Godinho C, Gomes M, Rabaça JE (2014) The importance of the surroundings: are bird communities of riparian galleries influenced by agroforestry matrices in SW Iberian Peninsula? Ann Sci 71(1):33–41. https://doi.org/10.1007/s13595-012-0228-x
Poblador-Ibáñez S (2018) Responses of Mediterranean riparian forests to water availability: Insights of present and future conditions. A case study in La Tordera catchment. Phd dissertation, Universidad de Barcelona
Reid AJ, Carlson AK, Creed IF, Eliason EJ, Gell PA, Johnson PT et al (2019) Emerging threats and persistent conservation challenges for freshwater biodiversity. Biol Rev 94(3):849–873. https://doi.org/10.1111/brv.12480
Resco de Dios V, Fischer C, Colinas C (2007) Climate change effects on Mediterranean forests and preventive measures. New for 33(1):29–40. https://doi.org/10.1007/s11056-006-9011-x
Richardson DM, Holmes PM, Esler KJ, Galatowitsch SM, Stromberg JC et al (2007) Riparian vegetation: degradation, alien plant invasions, and restoration prospects. Divers Distrib 13(1):126–139. https://doi.org/10.1111/j.1366-9516.2006.00314.x
Rundel PW, Arroyo MT, Cowling RM, Keeley JE, Lamont BB, Pausas JG, Vargas P (2018) Fire and plant diversification in Mediterranean-climate regions. Front Plant Sci 9:851. https://doi.org/10.3389/fpls.2018.00851
Sabater S, Elosegi A, Ludwig R (2018) Multiple stressors in river ecosystems: status, impacts and prospects for the future. Elsevier
Sabo JL, Sponseller R, Dixon M, Gade K, Harms T, Heffernan J, Jani A, Katz G, Soykan C, Watts J, Welter J (2005) Riparian zones increase regional species richness by harboring different, not more, species. Ecology 86:56–62. https://doi.org/10.1890/04-0668
Santos MJ (2010) Encroachment of upland Mediterranean plant species in riparian ecosystems of southern Portugal. Biodivers Conserv 19:2667–2684. https://doi.org/10.1007/s10531-010-9866-1
Santos T, Tellería JL, Díaz M, Carbonell R (2006) Evaluating the benefits of CAP reforms: can afforestations restore bird diversity in Mediterranean Spain? Basic Appl Ecol 7(6):483–495. https://doi.org/10.1016/j.baae.2005.11.001
Seavy NE, Gardali T, Golet GH, Griggs FT, Howell CA, Kelsey R et al (2009) Why climate change makes riparian restoration more important than ever: recommendations for practice and research. Ecol Restor 27(3):330–338
Shirley SM (2005) Habitat use by riparian and upland birds in old-growth coastal british Columbia rainforest. Willson Bull 117(3):245–257
Suggitt AJ, Wilson RJ, Isaac NJB et al (2018) Extinction risk from climate change is reduced by microclimatic buffering. Nat Clim Change 8:713–717. https://doi.org/10.1038/s41558-018-0231-9
Tellería JL (2020) Altitudinal shifts in forest birds in a Mediterranean mountain range: causes and conservation prospects. Bird Conserv Int 30(4):495–505. https://doi.org/10.1017/S0959270919000455
Tellería JL, Hernández-Tellez I, de la Hera I, Aguirre JI, Onrubia A (2022) Altitudinal seasonality as a potential driver of morphological diversification in rear-edge bird populations. Avian Res 13:100039. https://doi.org/10.1016/j.avrs.2022.100039
Tockner K, Stanford JA (2002) Riverine flood plains: present state and future trends. Environ Conserv 29(3):308–330. https://doi.org/10.1017/S037689290200022X
Toscano S, Ferrante A, Romano D (2019) Response of Mediterranean ornamental plants to drought stress. Horticulturae 5(1):6. https://doi.org/10.3390/horticulturae5010006
Vidal-Abarca Gutierrez MR, Suarez Alonso ML (2013) Which are, what is their status and what can we expect from ecosystem services provided by Spanish rivers and riparian areas? Biodivers Conserv 22:2469–2503 (2013). https://doi.org/10.1007/s10531-013-0532-2
Virkkala R, Lehikoinen A, Rajasärkkä A (2020) Can protected areas buffer short-term population changes of resident bird species in a period of intensified forest. Harvesting? Biol Conserv 244:108526. https://doi.org/10.1016/j.biocon.2020.108526
Vogel J, Paton E, Aich V, Bronstert A (2021) Increasing compound warm spells and droughts in the Mediterranean Basin. Weather Clim Extremes 32:100312. https://doi.org/10.1016/j.wace.2021.100312
Weigelhofer G, Feldbacher E, Trauner D, Pölz E, Hein T, Funk A (2020) Integrating conflicting goals of the EC water framework directive and the EC habitats directives into floodplain restoration schemes. Front Environ Sci 8:538139. https://doi.org/10.3389/fenvs.2020.538139
Whittaker RH (1972) Evolution and measurement of species diversity. Taxon 21:213–251. https://doi.org/10.2307/1218190
Yadav RKP, Bosabalidis AM, Vokou D (2004) Leaf structural features of Mediterranean perennial species: plasticity and life form specificity. J Biol Res 2:21–34
Zhang X, Ci X, Hu J, Bai Y, Thornhill AH, Conran JG, Li J (2023) Riparian areas as a conservation priority under climate change. Sci Total Environ 858:159879. https://doi.org/10.1016/j.scitotenv.2022.159879
Acknowledgements
We first want to thank the support of the staff of the Spanish Ministry for the Ecological Transition and the Demographic Challenge (MITERD)-DG Water, particularly to Belén Calleja and Fernando Magdaleno, who promoted this project. We are also very grateful to José Luis Tellería, María Torres-Sánchez, Javier Fernández-López and Guillermo Fandos for enriching discussion on the field sampling design. Two anonymous reviewers provided insightful comments that improved an early version of the manuscript.
Funding
This study was funded by the Spanish Ministry for the Ecological Transition and the Demographic Challenge (MITERD)-DG Water through the project entitled “Monitoring the effect of the ecological regime of flows established by the river basin management plans on the water bodies” (Project 21.834-060/0411).
Author information
Authors and Affiliations
Contributions
All authors contributed to the conception, design and logistic implementation of the study. Field data collection was performed by IdH. JAA extracted the climatic data for bird species and study sites. IdH performed the statistical analyses and wrote a first draft of the manuscript on which all authors made comments for improvement. All authors read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Communicated by Daniel Sanchez Mata.
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Supplementary Material 1: Appendix 1.
Database for the 152 semicircular sampling units analysed in this study
Supplementary Material 2: Appendix 2.
Analyses of PC2 and PC3 without potential outliers
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
de la Hera, I., Alcaraz-Hernández, J.D., Mezger, G. et al. Breeding bird communities of riparian and upland woodlands respond differently to an Atlantic-Mediterranean climatic gradient in Mainland Spain. Biodivers Conserv 33, 1729–1749 (2024). https://doi.org/10.1007/s10531-024-02828-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10531-024-02828-7