Assessing the role of habitat, climate, and anthropization gradients on terrestrial mammal diversity in the western Mediterranean basin

Ignasi FERNÁNDEZ-CABELLO , Marc FRANCH , Marc VILELLA , Nerea FERNANDEZ-ARRIETA , Marc ROTA , Ariadna SANGLAS , Eric BAQUÉ-DÍAZ , Marc GALLARDET , Pau FEDERICO , Albert PERIS , Eric SERRATOSA , Joan REAL , Ferran SAYOL , Roger PUIG-GIRONÈS

Integrative Zoology ›› 2025, Vol. 20 ›› Issue (3) : 485 -503.

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Integrative Zoology ›› 2025, Vol. 20 ›› Issue (3) : 485 -503. DOI: 10.1111/1749-4877.12866
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Assessing the role of habitat, climate, and anthropization gradients on terrestrial mammal diversity in the western Mediterranean basin

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Abstract

Mammal species globally exhibit distribution patterns conditioned by environmental conditions and human impact. The Mediterranean basin provides an ideal system to study these effects due to its diverse climate, and habitat conditions. In this work, we aim to assess the impact of landscape heterogeneity and anthropization degree on terrestrial mammal diversity in this region. Accordingly, we deployed over 300 camera traps across 28 sites for 3 months. Detected mammal species (weighing more than 1kg) were classified as domestic carnivores, domestic ungulates, wild carnivores, wild ungulates, lagomorphs, and large rodents. Alpha and beta diversity were calculated for each group and all wild mammals. Simple linear regressions and multimodal analysis were conducted between mammal diversities and climate, environmental conditions, landscape heterogeneity, and anthropization degree variables. Redundancy analyses were performed to identify variables and species determining the mammalian community composition. Indexes measuring landscape heterogeneity, anthropization degree, and its 30-year change did not correlate with mammal diversity. However, the difference in elevation within sites and domestic carnivore abundance showed a significant positive correlation with some of the diversity indexes. Nonetheless, rainfall and mean elevation factors generally showed the highest correlation with mammal diversity. Instead, a few influential species, including generalists and open-habitat specialists, highlighted the importance of conserving open areas, as well as the importance of the Pyrenees region as a key habitat for certain species. Therefore, climatic variables emerged as the key determinants of mammal diversity, highlighting climate change as a potential threat to mammal diversity in this area.

Keywords

alpha diversity / beta diversity / biodiversity / camera trap / landscape heterogeneity / Pyrenees

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Ignasi FERNÁNDEZ-CABELLO, Marc FRANCH, Marc VILELLA, Nerea FERNANDEZ-ARRIETA, Marc ROTA, Ariadna SANGLAS, Eric BAQUÉ-DÍAZ, Marc GALLARDET, Pau FEDERICO, Albert PERIS, Eric SERRATOSA, Joan REAL, Ferran SAYOL, Roger PUIG-GIRONÈS. Assessing the role of habitat, climate, and anthropization gradients on terrestrial mammal diversity in the western Mediterranean basin. Integrative Zoology, 2025, 20(3): 485-503 DOI:10.1111/1749-4877.12866

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References

[1]

Alexandre M, Hipólito D, Ferreira E, Fonseca C, Rosalino LM (2019). Humans do matter: Determinants of red fox (Vulpes vulpes) presence in a western Mediterranean landscape. Mammal Research 65, 203-214.

[2]

Ameztegui A, Morán-Ordóñez A, Márquez A et al. (2021). Forest expansion in mountain protected areas: Trends and consequences for the landscape. Landscape and Urban Planning 216, 104240.

[3]

Andermann T, Faurby S, Turvey ST, Antonelli A, Silvestro D (2020). The past and future human impact on mammalian diversity. Science Advances 6, eabb2313.

[4]

Andrews P, O'Brien EM (2000). Climate, vegetation, and predictable gradients in mammal species richness in southern Africa. Journal of Zoology 251, 205-231.

[5]

August PV (1983). The role of habitat complexity and heterogeneity in structuring tropical mammal communities. Ecology 64, 1495-1507.

[6]

Azevedo FC, Lemos FG, Freitas-Junior MC, Rocha DG, Azevedo FCC (2018). Puma activity patterns and temporal overlap with prey in a human-modified landscape at Southeastern Brazil. Journal of Zoology 305, 246-255.

[7]

Bartoń K (2016). Multi-model inference (MuMIn), R Package Version 1.15.6. Vienna, Austria. Available from URL: https://cran.r-project.org/web/packages/MuMIn/MuMIn.pdf

[8]

Bates D, Mächler M, Bolker B, Walker S (2014). Fitting linear mixed-effects models using lme4. arXiv, 1406.5823. https://doi.org/10.48550/arXiv.1406.5823

[9]

Blaum N, Tietjen B, Rossmanith E (2010). Impact of livestock husbandry on small-and medium-sized carnivores in Kalahari savannah rangelands. The Journal of Wildlife Management 73, 60-67.

[10]

Blondel J, Aronson J, Bodiou J-Y, Boeuf G (2010). The Mediterranean Region: Biological Diversity in Space and Time, 2nd edn. Oxford University Press, New York.

[11]

Bonnot N, Morellet N, Verheyden H et al. (2012). Habitat use under predation risk: hunting, roads and human dwellings influence the spatial behaviour of roe deer. European Journal of Wildlife Research 59, 185-193.

[12]

Burnham KP, Anderson DR (2002). Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach, 2nd edn. Springer, New York.

[13]

Burton AC, Neilson E, Moreira D et al. (2015). Wildlife camera trapping: A review and recommendations for linking surveys to ecological processes. Journal of Applied Ecology 52, 675-685.

[14]

Ceballos G, Brown JH (1995). Global patterns of mammalian diversity, endemism, and endangerment. Conservation Biology 9, 559-568.

[15]

Chiaradia A, Ramírez F, Forero MG, Hobson KA (2016). Stable isotopes (δ13C, δ15N) combined with conventional dietary approaches reveal plasticity in central-place foraging behavior of little penguins Eudyptula minor. Frontiers in Ecology and Evolution 3, 154.

[16]

Cuyckens GAE, Trasci NVGB, Perovic PG, Malizia LR (2022). Effect of free-ranging cattle on mammalian diversity: An Austral Yungas case study. Oryx 56, 877-887.

[17]

Delibes-Mateos M, Delibes M, Ferreras P, Villafuerte R (2008). Key role of European rabbits in the conservation of the Western Mediterranean basin hotspot. Conservation Biology 22, 1106-1117.

[18]

Dell'Arte GL, Laaksonen T, Norrdahl K, Korpimäki E (2007). Variation in the diet composition of a generalist predator, the red fox, in relation to season and density of main prey. Acta Oecologica 31, 276-281.

[19]

Donald PF, Green RE, Heath MF (2001). Agricultural intensification and the collapse of Europe's farmland bird populations. Proceedings of the Royal Society of London B: Biological Sciences 268, 25-29.

[20]

Dorph A, Swan M, Rochelmeyer E, Di Stefano J (2020). Complex habitat drives mammal communities in a flammable landscape. Forest Ecology and Management 462, 117979.

[21]

European Union (2018). Copernicus Land Monitoring Service. European Environment Agency (EEA). Available from URL: https://land.copernicus.eu/

[22]

Eurostat (2017). Glossary: Hemeroby Index. Available from URL: https://ec.europa.eu/eurostat/statistics-explained/index.php?title=Glossary:Hemeroby_index

[23]

Faurby S, Svenning JC (2015). Historic and prehistoric human-driven extinctions have reshaped global mammal diversity patterns. Diversity and Distributions 21, 1155-1166.

[24]

Fernández-de-Simón J, Díaz-Ruiz F, Rodríguez-de la Cruz M, Delibes-Mateos M, Villafuerte R, Ferreras P (2015). Can widespread generalist predators affect keystone prey? A case study with red foxes and European rabbits in their native range. Population ecology 57, 591-599.

[25]

Ferrer-Castán D, Morales-Barbero J, Vetaas OR (2016). Water-energy dynamics, habitat heterogeneity, history, and broad-scale patterns of mammal diversity. Acta Oecologica 77, 176-186.

[26]

Fløjgaard C, Normand S, Skov F, Svenning JC (2010). Deconstructing the mammal species richness pattern in Europe-towards an understanding of the relative importance of climate, biogeographic history, habitat heterogeneity and humans. Global Ecology and Biogeography 20, 218-230.

[27]

Fox J, Weisberg S (2019). An R Companion to Applied Regression, 3rd edn. Thousand Oaks, CA. Available from URL: https://www.john-fox.ca/Companion/index.html

[28]

Gálvez L, López-Pintor A, De Miguel JM et al. (2008). Ecosystem engineering effects of European rabbits in a Mediterranean habitat. In: Alves PC, Ferrand N, Hackländer K, eds. Lagomorph Biology: Evolution, Ecology, and Conservation. Springer, Berlin, Heidelberg, pp. 125-139.

[29]

Generalitat de Catalunya, Departament d'Acció Climàtica, Alimentació i Agenda Rural (2022). Dades de Medi Ambient a Catalunya. Available from URL: https://mediambient.gencat.cat/web/.content/home/dades-documentacio/estadistica/publicacions-estadistiques/dades_ma_cat/cat_es/2022-ca.pdf

[30]

Generalitat de Catalunya, Departament de Territori (2023). Hipermapa. Available from URL: https://sig.gencat.cat/visors/hipermapa.html

[31]

Herrero J, García-Serrano A, Reiné R et al. (2021). Challenges for recovery of large carnivores in humanized countries: Attitudes and knowledge of sheep farmers towards brown bear in Western Pyrenees, Spain. European Journal of Wildlife Research 67, 105.

[32]

Hibert F, Calenge C, Fritz H et al. (2010). Spatial avoidance of invading pastoral cattle by wild ungulates: Insights from using point process statistics. Biodiversity and conservation 19, 2003-2024.

[33]

Institut Cartogràfic i Geològic de Catalunya (2018). Model d'Elevacions del Terreny de 5×5 m. Available from URL: https://www.icgc.cat/Administracio-i-empresa/Descarregues/Elevacions/Model-d-elevacions-del-terreny-de-5X5-m

[34]

Institut d'Estadística de Catalunya (2022). Indicadors Anuals. Utilització del sòl. Available from URL: https://www.idescat.cat/indicadors/?id=anuals&n=10547&tema=TERRI&col=1

[35]

IUCN (2022). The IUCN Red List of Threatened Species. Version 2022-2. Available from URL: https://www.iucnredlist.org/

[36]

Jung M (2016). LecoS—A python plugin for automated landscape ecology analysis. Ecological informatics 31, 18-21.

[37]

Keenan RJ, Reams GA, Achard F, de Freitas JV, Grainger A, Lindquist E (2015). Dynamics of global forest area: Results from the FAO Global Forest Resources Assessment 2015. Forest Ecology and Management 352, 9-20.

[38]

Kennedy CM, Lonsdorf E, Neel MC et al. (2013). A global quantitative synthesis of local and landscape effects on wild bee pollinators in agroecosystems. Ecology Letters 16, 584-599.

[39]

Kerr JT, Packer L (1997). Habitat heterogeneity as a determinant of mammal species richness in high-energy regions. Nature 385, 252-254.

[40]

López P, Martín J (2022). Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales-CSIC. Available from URL: http://www.vertebradosibericos.org/

[41]

López-López P, Maiorano L, Falcucci A, Barba E, Boitani L (2011). Hotspots of species richness, threat and endemism for terrestrial vertebrates in SW Europe. Acta Oecologica 37, 399-412.

[42]

Lowry H, Lill A, Wong BB (2013). Behavioural responses of wildlife to urban environments. Biological Reviews 88, 537-549.

[43]

Lozano J, Olszańska A, Morales-Reyes Z et al. (2019). Human-carnivore relations: A systematic review. Biological Conservation 237, 480-492.

[44]

MacKenzie DI, Royle JA, Brown JA, Nichols JD (2004). Occupancy estimation and modeling for rare and elusive populations. In: Thompson WL, ed. Sampling Rare or Elusive Species: Concepts, Designs, and Techniques for Estimating Population Parameters. Island Press, Washington, DC, pp. 149-171.

[45]

Maiorano L, Amori G, Capula M et al. (2013). Threats from climate change to terrestrial vertebrate hotspots in Europe. PLoS ONE 8, e74989.

[46]

Maiorano L, Falcucci A, Zimmermann NE et al. (2011). The future of terrestrial mammals in the Mediterranean basin under climate change. Philosophical Transactions of the Royal Society B: Biological Sciences 366, 2681-2692.

[47]

Martínez-Jauregui M, Linares O, Carranza J, Soliño M (2017). Dealing with conflicts between people and colonizing native predator species. Biological Conservation 209, 239-244.

[48]

Martín-Vide J, Raso Nadal J, Morera Palacios A (2008). Atles Climàtic de Catalunya, període 1961-1990. Institut Cartogràfic de Catalunya i Servei Meteorològic de Catalunya, Generalitat de Catalunya, Barcelona, Spain.

[49]

Melo AS, Rangel TFL, Diniz-Filho JAF (2009). Environmental drivers of beta-diversity patterns in New-World birds and mammals. Ecography 32, 226-236.

[50]

Montalvo AE, Lopez RR, Parker ID, Silvy NJ, Cooper SM, Feagin RA (2017). Quantifying meso-mammal cave use in central Texas. Wildlife Biology 2017, 1-7.

[51]

Monterroso P, Brito JC, Ferreras P, Alves PC (2009). Spatial ecology of the European wildcat in a Mediterranean ecosystem: Dealing with small radio-tracking datasets in species conservation. Journal of Zoology 279, 27-35.

[52]

Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GA, Kent J (2000). Biodiversity hotspots for conservation priorities. Nature 403, 853-858.

[53]

O'Connell AF, Nichols JD, Karanth KU (2011). Camera Traps in Animal Ecology: Methods and Analyses. Springer, New York. Available from URL: https://doi.org/10.1007/978-4-431-99495-4

[54]

Oksanen J, Simpson G, Blanchet F et al. (2022). vegan: community ecology package, R Package Version 2.6-4. Available from URL: https://cran.r-project.org/web/packages/vegan/index.html

[55]

Oliveira BF, Machac A, Costa GC et al. (2016). Species and functional diversity accumulate differently in mammals. Global Ecology and Biogeography 25, 1119-1130.

[56]

Owen JG (1990). Patterns of mammalian species richness in relation to temperature, productivity, and variance in elevation. Journal of mammalogy 71, 1-13.

[57]

Paracchini ML, Capitani C (2011). Implementation of a EU wide indicator for the rural-agrarian landscape. Joint Research Centre Technical Report EUR: 25114. Available from URL: https://core.ac.uk/download/pdf/38626712.pdf

[58]

Pita R, Mira A, Moreira F, Morgado R, Beja P (2009). Influence of landscape characteristics on carnivore diversity and abundance in Mediterranean farmland. Agriculture, Ecosystems & Environment 132, 57-65.

[59]

Pörtner HO, Roberts DC, Adams H et al. (2022). Climate Change 2022: Impacts, Adaptation and Vulnerability. IPCC, Geneva, Switzerland. https://doi.org/10.1017/9781009325844

[60]

Puig-Gironès R, Brotons L, Pons P (2017). Aridity influences the recovery of vegetation and shrubland birds after wildfire. PLoS ONE 12, e0173599.

[61]

Puig-Gironès R, Brotons L, Pons P, Franch M (2023). Examining the temporal effects of wildfires on forest birds: Should I stay or should I go? Forest Ecology and Management 549, 121439.

[62]

Puig-Gironès R, Real J (2022). A comprehensive but practical methodology for selecting biological indicators for long-term monitoring. PLoS ONE 17, e0265246.

[63]

Pushkina D, Raia P (2008). Human influence on distribution and extinctions of the late Pleistocene Eurasian megafauna. Journal of Human Evolution 54, 769-782.

[64]

R Development Core Team (2022). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.

[65]

Real R, Márcia Barbosa A, Porras D et al. (2003). Relative importance of environment, human activity and spatial situation in determining the distribution of terrestrial mammal diversity in Argentina. Journal of Biogeography 30, 939-947.

[66]

Reif J, Hanzelka J (2020). Continent-wide gradients in open-habitat insectivorous bird declines track spatial patterns in agricultural intensity across Europe. Global Ecology and Biogeography 29, 1988-2013.

[67]

Remmers JJ, Nielsen CK, Lesmeister DB (2023). Anthropogenic and environmental influences on mammalian alpha and beta diversity in a hardwood forest landscape. Global Ecology and Conservation 41, e02369.

[68]

Rey Benayas JM, Martins A, Nicolau JM, Schulz JJ (2007). Abandonment of agricultural land: An overview of drivers and consequences. CABI Reviews 14. https://doi.org/10.1079/PAVSNNR20072057

[69]

Rogala JK, Hebblewhite M, Whittington J, White CA, Coleshill J, Musiani M (2011). Human activity differentially redistributes large mammals in the Canadian Rockies National Parks. Ecology and Society 16, https://doi.org/10.5751/ES-04251-160316

[70]

Rosalino LM, Macdonald DW, Santos-Reis M (2004). Spatial structure and land-cover use in a low-density Mediterranean population of Eurasian badgers. Canadian Journal of Zoology 82, 1493-1502.

[71]

Rowcliffe JM, Field J, Turvey ST, Carbone C (2008). Estimating animal density using camera traps without the need for individual recognition. Journal of Applied Ecology 45, 1228-1236.

[72]

RStudio Team (2022). RStudio: integrated development for R. RStudio. Inc., Boston,MA. http://www.rstudio.com/

[73]

Santini L, González-Suárez M, Russo D, Gonzalez-Voyer A, von Hardenberg A, Ancillotto L (2019). One strategy does not fit all: Determinants of urban adaptation in mammals. Ecology Letters 22, 365-376.

[74]

Santos AM, Cianciaruso MV, Barbosa AM et al. (2020). Current climate, but also long-term climate changes and human impacts, determine the geographic distribution of European mammal diversity. Global Ecology and Biogeography 29, 1758-1769.

[75]

Santos-Reis M, Santos MJ, Lourenço S, Marques JT, Pereira I, Pinto B (2004). Relationships between stone martens, genets and cork oak woodlands in Portugal. In: Harrison DJ, Fuller AK, Proulx G, eds. Martens and Fishers (Martes) in Human-Altered Environments. Springer-Verlag, New York. pp. 147-172.

[76]

Stevens RD, Rowe RJ, Badgley C (2019). Gradients of mammalian biodiversity through space and time. Journal of Mammalogy 100, 1069-1086.

[77]

Stillfried M, Gras P, Börner K et al. (2017). Secrets of success in a landscape of fear: Urban wild boar adjust risk perception and tolerate disturbance. Frontiers in Ecology and Evolution 5, 157.

[78]

Stoate C, Baldi A, Beja P et al. (2009). Ecological impacts of early 21st century agricultural change in Europe-A review. Journal of Environmental Management 91, 22-46.

[79]

Suárez-Tangil BD, Rodríguez A (2023). Environmental filtering drives the assembly of mammal communities in a heterogeneous Mediterranean region. Ecological Applications 33, e2801.

[80]

Suraci JP, Gaynor KM, Allen ML et al. (2021). Disturbance type and species life history predict mammal responses to humans. Global Change Biology 27, 3718-3731.

[81]

Swan M, Christie F, Steel E, Sitters H, York A, Di Stefano J (2020). Ground-dwelling mammal diversity responds positively to productivity and habitat heterogeneity in a fire-prone region. Ecosphere 11, e03248.

[82]

Szilassi P, Bata T, Szabó S, Czúcz B, Molnár Z, Mezősi G (2017). The link between landscape pattern and vegetation naturalness on a regional scale. Ecological Indicators 81, 252-259.

[83]

Tack J (2018). Wild Boar (Sus scrofa) Populations in Europe: A Scientific Review of Population Trends and Implications for Management. European Landowners’ Organization, Brussels, Belgium.

[84]

Teacher AG, Thomas JA, Barnes I (2011). Modern and ancient red fox (Vulpes vulpes) in Europe show an unusual lack of geographical and temporal structuring, and differing responses within the carnivores to historical climatic change. BMC Evolutionary Biology 11, 214.

[85]

Teixeira DF, Ares-Pereira G, Camarinha C et al. (2023). Effect of anthropic disturbances on the activity pattern of two generalist mesocarnivores inhabiting Mediterranean forestry plantations. Biodiversity and Conservation 32, 1251-1270.

[86]

Tews J, Brose U, Grimm V et al. (2004). Animal species diversity driven by habitat heterogeneity/diversity: The importance of keystone structures. Journal of Biogeography 31, 79-92.

[87]

Tixier H, Duncan P, Scehovic J, Yant A, Gleizes M, Lila M (1997). Food selection by European roe deer (Capreolus capreolus): Effects of plant chemistry, and consequences for the nutritional value of their diets. Journal of Zoology 242, 229-245.

[88]

Vallecillo S, Hermoso V, Possingham HP, Brotons L (2013). Conservation planning in a fire-prone Mediterranean region: Threats and opportunities for bird species. Landscape Ecology 28, 1517-1528.

[89]

Varga D, Roigé M, Pintó J, Saez M (2019). Assessing the spatial distribution of biodiversity in a changing temperature pattern: The case of Catalonia, Spain. International Journal of Environmental Research and Public Health 16, 4026.

[90]

Wagenmakers EJ, Farrell S (2004). AIC model selection using Akaike weights. Psychonomic Bulletin & Review 11, 192-196.

[91]

Walz U, Stein C (2014). Indicators of hemeroby for the monitoring of landscapes in Germany. Journal for Nature Conservation 22, 279-289.

[92]

Whittaker RH (1972). Evolution and measurement of species diversity. Taxon 21, 213-251.

[93]

Wickham H, Bryan J (2022). readx1: Read Excel files, R Package Version 1.4.1. Available from URL: https://cran.r-project.org/web/packages/readxl/index.html

[94]

Wolff M, Haase D, Haase A (2018). Compact or spread? A quantitative spatial model of urban areas in Europe since 1990. PLoS ONE 13, e0192326.

[95]

Zeileis A, Hothorn T (2002). Diagnostic checking in regression relationships. R News 2, 7-10.

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