Skip to main content

Low effectiveness of the Natura 2000 network in preventing land-use change in bat hotspots

Abstract

One of the most important issues in biodiversity conservation is an exploration of the relationships among protected areas, land-use changes and biodiversity, so we aimed to assess the performance of the Natura 2000 network (N2000) in representing the bat conservation hotspots in peninsular Spain and the Balearic Islands and to compare the rates of land-use changes within these hotspots with those observed throughout the rest of the study area. First, we applied a Combined Index that integrates various biodiversity metrics (species richness, rarity and vulnerability) to identify hotspots, and once they were identified, we used null models to assess the performance of N2000 in representing them. Finally, also using null models, we tested whether the changes in land use (“anthropization” or “naturalization”) within the hotspots occurred at a significantly higher or lower frequency than in the rest of the study area; for this, we considered two temporal windows (1980–2006 and 2006–2012) corresponding with periods before and after the official designation of the N2000 sites. Our results show that bat hotspots are effectively represented in the Iberian N2000, but although land-use changes were generally higher in Spain before 2006, hotspots have not experienced lower rates of change compared to the remainder of the territory (regardless of the period under consideration). This suggests low effectiveness of the Iberian N2000 in preventing land-use change in bat hotspots, so to preserve the Iberian bat fauna, we encourage the urgent implementation of management plans to avoid intensive changes in land use both inside and around bat hotspots.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3

References

  1. Alberdi A, Aihartza JR, Albero JC, Aizpurua O, López-Baucells A, Freixas L, Puig X, Flaquer C, Garín I (2012) First records of the parti-coloured bat Vespertilio murinus (Chiroptera: Vespertilionidae) in the Pyrenees. Mammalia 76:109–111. doi:10.1515/MAMM.2011.106

    Article  Google Scholar 

  2. Alcalde JT (2009) Myotis alcathoe Helversen & Heller, 2001 y Pipistrellus pygmaeus (Leach, 1825), nuevas especies de quirópteros para Navarra. Munibe 57: 225–236

  3. Alcalde JT, Trujillo D, Artázcoz A, Agirre-Mendi PT (2008) Distribución y estado de conservación de los quirópteros en Aragón. Graellsia 64:3–16

    Article  Google Scholar 

  4. Altringham J, Kerth G (2016) Bats and roads. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: Conservation of Bats in a Changing World. SpringerOpen, Berlin, pp 35–62

    Chapter  Google Scholar 

  5. Araújo MB, Lobo JM, Moreno JC (2007) The effectiveness of Iberian protected areas in conserving terrestrial biodiversity. Conserv Biol 21:1423–1432. doi:10.1111/j.1523-1739.2007.00827.x

    Article  PubMed  Google Scholar 

  6. Arnett EB, Baerwald EF, Mathews F, Rodrigues L, Rodríguez-Durán A, Rydell J, Villegas-Patraca R, Voigt CC (2016) Impacts of wind energy development on bats: A global perspective. In: Voigt CC, Kingston T (eds) Bats in the Anthropocene: Conservation of Bats in a Changing World. SpringerOpen, Berlin, pp 295–324

    Chapter  Google Scholar 

  7. Bader E, Jung K, Kalko EKV et al (2015) Mobility explains the response of aerial insectivorous bats to anthropogenic habitat change in the Neotropics. Biol Conserv 186:97–106. doi:10.1016/j.biocon.2015.02.028

    Article  Google Scholar 

  8. Bailey KM, McCleery RA, Binford MW, Zweig C (2016) Land-cover change within and around protected areas in a biodiversity hotspot. J Land Use Sci 11:154–176. doi:10.1080/1747423X.2015.1086905

    Article  Google Scholar 

  9. Beresford AE, Buchanan GM, Sanderson FJ et al (2016) The Contributions of the EU Nature Directives to the CBD and Other Multilateral Environmental Agreements. Conserv Lett. doi:10.1111/conl.12259

    Google Scholar 

  10. Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press, Oxford

    Google Scholar 

  11. Boyles JG, Cryan PM, McCracken GF, Kunz TK (2011) Economic importance of bats in agriculture. Science 332:41–42. doi:10.1126/science.1201366

    Article  PubMed  Google Scholar 

  12. Buchmann CM, Schurr FM, Nathan R, Jeltsch F (2013) Habitat loss and fragmentation affecting mammal and bird communities-The role of interspecific competition and individual space use. Ecol Inform 14:90–98. doi:10.1016/j.ecoinf.2012.11.015

    Article  Google Scholar 

  13. Charbonnier Y, Gaüzère P, van Halder I et al (2016) Deciduous trees increase bat diversity at stand and landscape scales in mosaic pine plantations. Landsc Ecol 31:291–300. doi:10.1007/s10980-015-0242-0

    Article  Google Scholar 

  14. Cisneros LM, Fagan ME, Willig MR (2015) Season-specific and guild-specific effects of anthropogenic landscape modification on metacommunity structure of tropical bats. J Anim Ecol 84:373–385. doi:10.1111/1365-2656.12299

    Article  PubMed  Google Scholar 

  15. De la Montaña E, Rey Benayas JM, Vasques A et al (2011) Conservation planning of vertebrate diversity in a Mediterranean agricultural-dominant landscape. Biol Conserv 144:2468–2478. doi:10.1016/j.biocon.2011.07.001

    Article  Google Scholar 

  16. Dietz C, von Helversen O, Nill D (2009) Bats of Britain. Europe and northwest Africa. A&C Black Publishers Ltd., London

    Google Scholar 

  17. Dirzo R, Young HS, Galetti M et al (2014) Defaunation in the Anthropocene. Science 345:401–406. doi:10.1126/science.1251817

    CAS  Article  PubMed  Google Scholar 

  18. Duarte J, Farfán MA (2009) Nuevos datos sobre factores de riesgo y presencia del murciélago rabudo Tadarida teniotis (Rafinesque, 1814) en Andalucia. Galemys 21:76–77

    Google Scholar 

  19. Encabo I, Barba E, Belda EJ, Monrós JS (2007) Área de campeo de quirópteros en el término municipal de Carcaixent (Valencia): Nuevas citas para el Atlas de los Mamíferos Terrestres. Galemys 19:37–44

    Google Scholar 

  20. Estrada-Villegas S, Meyer CFJ, Kalko EKV (2010) Effects of tropical forest fragmentation on aerial insectivorous bats in a land-bridge island system. Biol Conserv 143:597–608. doi:10.1016/j.biocon.2009.11.009

    Article  Google Scholar 

  21. Ethier K, Fahrig L (2011) Positive effects of forest fragmentation, independent of forest amount, on bat abundance in eastern Ontario, Canada. Landsc Ecol 26:865–876. doi:10.1007/s10980-011-9614-2

    Article  Google Scholar 

  22. European Commission (2010) Natura 2000 Database and GIS. http://ec.europa.eu/environment/nature/natura2000/db_gis/index_en.htm#area_calc

  23. European Commission (2015) Communication from the commission to the European Parliament, the council, the European economic and social committee and the committee of the regions. Regulatory Fitness and Performance Programme (REFIT): State of Play and Outlook. COM/2014/368

  24. Falcucci A, Maiorano L, Boitani L (2007) Changes in land-use/land-cover patterns in Italy and their implications for biodiversity conservation. Landsc Ecol 22:617–631. doi:10.1007/s10980-006-9056-4

    Article  Google Scholar 

  25. Fischer J, Lindenmayer DB (2007) Landscape modification and habitat fragmentation: a synthesis. Glob Ecol Biogeogr 16:265–280. doi:10.1111/j.1466-8238.2007.00287.x

    Article  Google Scholar 

  26. Flaquer C, Torre I, Arrizabalaga A, Torre I (2007) Comparison of sampling methods for inventory of bat communities. J Mammal 88:526–533. doi:10.1644/06-MAMM-A-135R1.1

    Article  Google Scholar 

  27. Flaquer C, Puig X, Fàbregas E, Guixe D, Torre I, Ràfols RG, Páramo F, Camprodon J, Cumplido JM, Ruíz-Jarillo R, Baucells AL, Freixas L, Arrizabalaga A (2010) Revisión y aportación de datos sobre quirópteros de Catalunya: Propuesta de Lista Roja. Galemys 22:29–61

    Google Scholar 

  28. Flynn DFB, Gogol-Prokurat M, Nogeire T et al (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33. doi:10.1111/j.1461-0248.2008.01255.x

    Article  PubMed  Google Scholar 

  29. García D, Arbona P (2009) Presencia del murciélago ratonero pardo Myotis emarginatus (Geoffroy, 1806) (Chiroptera: Vespertilionidae) en Mallorca (Islas Baleares). Endins 33:121–124

    Google Scholar 

  30. Gaston KJ, Pressey RL, Margules CR (2002) Persistence and vulnerability: retaining biodiversity in the landscape and in protected areas. J Biosci 27:361–384. doi:10.1007/BF02704966

    CAS  Article  PubMed  Google Scholar 

  31. Hermida RJ, Lamas FJ, Graña DA, Rial S, Cerqueira F, Arzúa M, Seage R (2012) Contribución al conocimiento de la distribución de los Murciélagos (O. Chiroptera) en Galicia. Galemys 24:13–23

    Article  Google Scholar 

  32. Hernández-Manrique OL, Sanchez-Fernández D, Numa C et al (2013) Extinction trends of threatened invertebrates in peninsular Spain. J Insect Conserv 17:235–244. doi:10.1007/s10841-012-9502-3

    Article  Google Scholar 

  33. Hovick TJ, Elmore RD, Dahlgren DK et al (2014) Evidence of negative effects of anthropogenic structures on wildlife: a review of grouse survival and behaviour. J Appl Ecol 51:1680–1689. doi:10.1111/1365-2664.12331

    Article  Google Scholar 

  34. Ibisch PL, Hoffmann MT, Kreft S, Pe’er G, Kati V, Biber-Freudenberger L, DellaSala DA, Vale MM, Hobson PR, Selva N (2016) A global map of roadless areas and their conservation status. Science 354:1423–1427. doi:10.1126/science.aah7393

    CAS  Article  PubMed  Google Scholar 

  35. Jantz SM, Barker B, Brooks TM et al (2015) Future habitat loss and extinctions driven by land-use change in biodiversity hotspots under four scenarios of climate-change mitigation. Conserv Biol 29:1122–1131. doi:10.1111/cobi.12549

    Article  PubMed  Google Scholar 

  36. Jones G, Jacobs DS, Kunz TH et al (2009) Carpe noctem: the importance of bats as bioindicators. Endanger Species Res 8:93–115. doi:10.3354/esr00182

    Article  Google Scholar 

  37. Jung K, Kalko EKV (2010) Where forest meets urbanization: foraging plasticity of aerial insectivorous bats in an anthropogenically altered environment. J Mammal 91:144–153. doi:10.1644/08-MAMM-A-313R.1

    Article  Google Scholar 

  38. Kati V, Hovardas T, Dieterich M, Ibisch PL, Mihok B, Selva N (2015) The challenge of implementing the European network of protected areas Natura 2000. Conserv Biol 29:260–270. doi:10.1111/cobi.12366

    Article  PubMed  Google Scholar 

  39. Kunz TH, de Torrez EB, Bauer D et al (2011) Ecosystem services provided by bats. Ann N Y Acad Sci 1223:1–38. doi:10.1111/j.1749-6632.2011.06004.x

    Article  PubMed  Google Scholar 

  40. Lisón F (2012) Murciélago de cueva – Miniopterus schreibersii. In: Salvador A, Cassinello J (eds) Enciclopedia Virtual de los Vertebrados Españoles. Museo Nacional de Ciencias Naturales, Madrid. http://www.vertebradosibericos.org/

  41. Lisón F (2015) Murciélago hortelano meridional—Eptesicus isabellinus. In Salvador A, Barja I (eds) Enciclopedia virtual de los vertebrados españoles. Madrid. Museo Nacional de Ciencias Naturales. http://www.vertebradosibericos.org

  42. Lisón F, Calvo JF (2011) The significance of water infrastructures for the conservation of bats in a semiarid Mediterranean landscape. Anim Conserv 14:533–541. doi:10.1111/j.1469-1795.2011.00460.x

    Article  Google Scholar 

  43. Lisón F, Calvo JF (2013) Ecological niche modelling of three pipistrelle bat species in semiarid Mediterranean landscapes. Acta Oecologica 47:68–73. doi:10.1016/j.actao.2013.01.002

    Article  Google Scholar 

  44. Lisón F, Yelo ND, Haz Á, Calvo JF (2010) Contribución al conocimiento de la distribución de la fauna quiropterológica de la Región de Murcia. Galemys 22:11–28

    Google Scholar 

  45. Lisón F, Aledo E, Calvo JF (2011) Los murciélagos (Mammalia: Chiroptera) de la Región de Murcia (SE España): distribución y estado de conservación. Anales de Biología 33:79–92

    Google Scholar 

  46. Lisón F, Picazo J, López M (2012) Primera cita del murciélago ratonero patudo Myotis capaccinii (Bonaparte, 1837) en el Parque Natural Lagunas de Ruidera (Castilla-La Mancha). Galemys 24:65–66

    Article  Google Scholar 

  47. Lisón F, Palazón JA, Calvo JF (2013) Effectiveness of the Natura 2000 network for the conservation of cave-dwelling bats in a Mediterranean region. Anim Conserv 16:528–537. doi:10.1111/acv.12025

    Article  Google Scholar 

  48. Lisón F, Sánchez-Fernández D, Calvo JF (2015) Are species listed in the Annex II of the Habitats Directive better represented in Natura 2000 network than the remaining species? A test using Spanish bats. Biodivers Conserv 24:2459–2473

    Article  Google Scholar 

  49. Lisón F, Altamirano A, Field R, Jones G (2017) Conservation on the blink: deficient technical reports threaten conservation in the Natura 2000 network. Biol Conserv 209:11–16. doi:10.1016/j.biocon.2017.02.003

    Article  Google Scholar 

  50. López-López P, Maiorano L, Falcucci A et al (2011) Hotspots of species richness, threat and endemism for terrestrial vertebrates in SW Europe. Acta Oecologica 37:399–412. doi:10.1016/j.actao.2011.05.004

    Article  Google Scholar 

  51. López-Roig M, Serra-Cobo J (2014) Impact of human disturbance, density, and environmental conditions on the survival probabilities of pipistrelle bat (Pipistrellus pipistrellus). Popul Ecol 56:471–480. doi:10.1007/s10144-014-0437-2

    Article  Google Scholar 

  52. Maas B, Karp DS, Bumrungsri S et al (2015) Bird and bat predation services in tropical forests and agroforestry landscapes. Biol Rev. doi:10.1111/brv.12211

    PubMed  Google Scholar 

  53. Martínez-Abraín A, Crespo J, Berdugo M et al (2013) Causes of human impact to protected vertebrate wildlife parallel long-term socio-economical changes in Spain. Anim Conserv 16:286–294. doi:10.1111/j.1469-1795.2012.00599.x

    Article  Google Scholar 

  54. Medail F, Quezel P (1997) Hot-spots analysis for conservation of plant biodiversity in the Mediterranean Basin. Ann Missouri Bot Gard 84:112–127. doi:10.2307/2399957

    Article  Google Scholar 

  55. Newbold T, Hudson LN, Hill SLL et al (2015) Global effects of land use on local terrestrial biodiversity. Nature 520:45–50. doi:10.1038/nature14324

    CAS  Article  PubMed  Google Scholar 

  56. Newbold T, Hudson LN, Arnell AP et al (2016a) Has land use pushed terrestrial biodiversity beyond the planetary boundary? A global assessment. Science 353:288–291. doi:10.1126/science.aaf2201

    CAS  Article  PubMed  Google Scholar 

  57. Newbold T, Hudson LN, Hill SLL et al (2016b) Global patterns of terrestrial assemblage turnover within and among land uses. Ecography 39:1151–1163. doi:10.1111/ecog.01932

    Article  Google Scholar 

  58. Palomo LJ, Gisbert J, Blanco JC (2007) Altas y Libro Rojo de los mamíferos terrestres de España. Dirección General de la Biodiversidad-SECEM-SECEMU, Madrid

  59. Picazo F, Lisón F (2013) Fauna quiropterológica del término municipal de Villalgordo del Júcar y sus alrededores (Castilla-La Mancha). Anales de Biología 35:1–8

    Google Scholar 

  60. Psaralexi MK, Votsi N-EP, Selva N, Mazaris AD, Pantis JD (2017) Importance of roadless areas for the European Conservation Network. Front Ecol Evol 5:2. doi:10.3389/fevo.2017.00002

    Article  Google Scholar 

  61. Purvis A, Hector A (2000) Getting the measure of biodiversity. Nature 405:47. doi:10.1038/35012221

    Article  Google Scholar 

  62. R Core Team (2014) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria

  63. Rey Benayas JM, De La Montaña E (2003) Identifying areas of high-value vertebrate diversity for strengthening conservation. Biol Conserv 114:357–370. doi:10.1016/S0006-3207(03)00064-8

    Article  Google Scholar 

  64. Reyjol Y, Hugueny B, Pont D et al (2007) Patterns in species richness and endemism of European freshwater fish. Glob Ecol Biogeogr 16:65–75. doi:10.1111/j.1466-8238.2006.00264.x

    Article  Google Scholar 

  65. Rodriguez-San Pedro A, Simonetti JA (2015) The relative influence of forest loss and fragmentation on insectivorous bats: does the type of matrix matter? Landsc Ecol 30:1561–1572. doi:10.1007/s10980-015-0213-5

    Article  Google Scholar 

  66. Romo H, García-Barros E, Lobo JM (2006) Identifying recorder-induced geographic bias in an Iberian butterfly database. Ecography (Cop) 29:873–885. doi:10.1111/j.2006.0906-7590.04680.x

    Article  Google Scholar 

  67. Rösch V, Tscharntke T, Scherber C, Batáry P (2013) Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. J Appl Ecol 50:387–394. doi:10.1111/1365-2664.12056

    Article  Google Scholar 

  68. Russo D, Ancillotto L (2014) Sensitivity of bats to urbanization: a review. Mamm Biol - Zeitschrift für Säugetierkd 80:205–212. doi:10.1016/j.mambio.2014.10.003

    Article  Google Scholar 

  69. Sala OE, Chapin FS, Armesto JJ et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774. doi:10.1126/science.287.5459.1770

    CAS  Article  PubMed  Google Scholar 

  70. Sánchez-Fernández D, Abellán P (2015) Using null models to identify under-represented species in protected areas: a case study using European amphibians and reptiles. Biol Conserv 184:290–299. doi:10.1016/j.biocon.2015.02.006

    Article  Google Scholar 

  71. Sánchez-Fernández D, Lobo JM, Abellán P et al (2008) Bias in freshwater biodiversity sampling: the case of Iberian water beetles. Divers Distrib 14:754–762. doi:10.1111/j.1472-4642.2008.00474.x

    Article  Google Scholar 

  72. Santos H, Juste J, Ibáñez C et al (2014) Influences of ecology and biogeography on shaping the distributions of cryptic species: three bat tales in Iberia. Biol J Linn Soc 112:150–162. doi:10.1111/bij.12247

    Article  Google Scholar 

  73. Serra-Cobo J, Amengual B, López-Roig M, Márquez J, Bayer X, Guasch C, Sánchez A, Oliver JA (2007) Quinze anys d’estudis quiropterlògics a les Illes Balears (1993-2007). Endins 31:125–140

    Google Scholar 

  74. Sirami C, Jacobs DS, Cumming GS (2013) Artificial wetlands and surrounding habitats provide important foraging habitat for bats in agricultural landscapes in the Western Cape, South Africa. Biol Conserv 164:30–38. doi:10.1016/j.biocon.2013.04.017

    Article  Google Scholar 

  75. Spanish Government (2013) Lugares de Importancia Comunitaria (LIC). http://www.magrama.gob.es/es/biodiversidad/temas/espacios-protegidos/rednatura-2000/lic.aspx

  76. Trujillo D, García D (2009) Primera cita del murciélago de Nathusius Pipistrellus nathusii (Keyserling y Blasius, 1839) para las Islas Baleares. Galemys 21:39–46

    Google Scholar 

  77. Turner BL, Lambin EF, Reenberg A (2007) The emergence of land change science for global environmental change and sustainability. Proc Natl Acad Sci USA 104:20666–20671. doi:10.1073/pnas.0704119104

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  78. Voigt CC, Kingston T (2016) Bats in the Anthropocene: conservation of bats in a changing world. SpringerOpen, New York

    Book  Google Scholar 

Download references

Acknowledgements

We are grateful for the important contribution of bat workers and SECEMU members to understanding the distributions of the bat fauna of Spain. We thank Ángeles Haz and Ana María Soria for correcting the English in the manuscript. FL was supported by a fellowship (Programa MECE Educación Superior, Project FRO 1555) from Ministerio de Educación of Gobierno de Chile and a postdoctoral fellowship (Programa de Formación de Investigadores Postdoctorales, Ord. N°001/VRIP) from Universidad de La Frontera, Chile. DS-F was supported by a post-doctoral contract funded by the Universidad de Castilla-La Mancha and the European Social Fund (ESF). This project has been partially funded by project CGL2016-76995-P from Ministerio de Economía, Industria y Competitividad of Gobierno de España.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Fulgencio Lisón.

Additional information

This article belongs to the Topical Collection: Biodiversity protection and reserves.

Communicated by Stephen Garnett.

Appendices

Appendix 1

List of bibliographic references used to complete the database of bats distribution in Spain (Alberdi et al. 2012; Alcalde et al. 2008; Alcalde 2009; Duarte and Farfán 2009; Encabo et al. 2007; Flaquer et al. 2010; García and Arbona 2009; Hermida et al. 2012; Lisón et al. 2010, 2011, 2012; Lisón 2012; Picazo and Lisón 2013; Serra-Cobo et al. 2007; Trujillo and García 2009).

Appendix 2

See Table 5.

Table 5 Number of cells recorded for each species (n) and its percentage for the 5429 cells of the study area

Appendix 3

See Fig. 4.

Fig. 4
figure4

Hotspots for bat diversity outside of protected areas of Natura 2000 network

Appendix 4

See Fig. 5.

Fig. 5
figure5

Maps with distribution of the cells from anthropization (a, b) and naturalization (c, d) rates in both periods (1986–2006 and 2006–2012). The colours represent the different quartiles and black lines delimit Spanish provinces. (Color figure online)

Appendix 5

See Fig. 6.

Fig. 6
figure6

Hotspots and Roadless areas (>100 km2). (Color figure online)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Lisón, F., Sánchez-Fernández, D. Low effectiveness of the Natura 2000 network in preventing land-use change in bat hotspots. Biodivers Conserv 26, 1989–2006 (2017). https://doi.org/10.1007/s10531-017-1342-8

Download citation

Keywords

  • Chiroptera
  • Conservation
  • CORINE
  • Management police
  • Protected areas
  • Roadless areas