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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

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Abstract

One of the main aims of protected areas is to be effective in the conservation of target species, i.e. those of the highest conservation concern. The Natura 2000 network (N2000) of protected areas is the main pillar of European action to halt biodiversity loss. Within N2000, special areas of conservation (SACs) are designated to protect habitats and species of the highest conservation interest, i.e. habitats from Annex I and species (other than birds) listed in Annex II of the Habitat Directive. Thus, a critical and urgent task is to assess the effectiveness of N2000 in the protection of these species. Here, we used distribution data for Spanish bats to test whether the species included in Annex II are better represented in N2000 than the remaining bats found in Spain, since SAC sites were specifically designated to protect the former species. In general, we found significantly high overlapping values between species distribution and N2000 sites (both groups of species are in general over-represented in N2000). However, contrary to our expectations, N2000 (even when only SACs were considered) did not offer higher representation values for the species listed in Annex II than for other species. We found that N2000 performed well even for non-target species, and that species from Annex II could have acted as effective umbrella species for the remaining bat species. Finally, the usefulness of including a species in Annex II is discussed, and guidelines to improve the efficiency of the N2000 for bat conservation are offered.

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References

  • Abellán P, Sánchez-Fernández D (2015) A gap analysis comparing the effectiveness of Natura 2000 and national protected area networks in representing European amphibians and reptiles. Biodivers Conserv. doi:10.1007/s10531-015-0862-3

    Google Scholar 

  • Abellán P, Sánchez-Fernández D, Velasco J, Millán A (2007) Effectiveness of protected area networks in representing freshwater biodiversity: the case of a Mediterranean river basin (south-eastern Spain). Aquat Conserv 17:361–374. doi:10.1002/aqc.778

    Article  Google Scholar 

  • Akasaka T, Akasaka M, Nakamura F (2012) Scale-independent significance of river and riparian zones on three sympatric Myotis species in an agricultural landscape. Biol Conserv 145:15–23. doi:10.1016/j.biocon.2011.08.017

    Article  Google Scholar 

  • Alagador D, Triviño M, Cerdeira JO, Brás R, Cabeza M, Araújo MB (2012) Linking like with like: optimising connectivity between environmentally-similar habitats. Landsc Ecol 27:291–301. doi:10.1007/s10980-012-9704-9

    Article  Google Scholar 

  • Almenar D, Aihartza JR, Goiti U, Salsamendi E, Garín I (2006) Habitat selection and spatial use by the trawling bat Myotis capaccinii (Bonaparte, 1837). Acta Chiropterol 8:157–167

    Article  Google Scholar 

  • Almenar D, Monsalve MA, Alcocer A, Castelló AJ (2007) Rhinolophus mehelyi Matschie, 1901. In: Palomo LJ, Gisbert J, Blanco JC (eds) Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General para la Biodiversidad-SECEM-SECEMU, Madrid, pp 151–152

    Google Scholar 

  • Almenar D, Aihartza JR, Goiti U, Salsamendi E, Garín I (2009) Foraging behaviour of the long-fingered bat Myotis capaccinii: implications for conservation and management. Endanger Species Res 8:60–78. doi:10.3354/esr00183

    Article  Google Scholar 

  • Amorim F, Carvalho SB, Honrado J, Rebelo H (2014) Designing optimized multi-species monitoring networks to detect range shifts driven by climate change: a case study with bats in the North of Portugal. PLoS One 9:e87291. doi:10.1371/journal.pone.0087291

    Article  PubMed Central  PubMed  Google Scholar 

  • Araújo MB (2004) Matching species with reserves: uncertainities from using data at different resolutions. Biol Conserv 118:533–538. doi:10.1016/j.biocon.2003.10.006

    Article  Google Scholar 

  • 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 

  • Araújo MB, Alagador D, Cabeza M, Nogués-Bravo D, Thuiller W (2011) Climate change threatens European conservation areas. Ecol Lett 14:484–492. doi:10.1111/j.1461-0248.2011.01610.x

    Article  PubMed Central  PubMed  Google Scholar 

  • Biscardi S, Russo D, Casciani V, Cesarini D, Mei M, Boitani L (2007) Foraging requirements of the endangered long-fingered bat: the influence of micro-habitat structure, water quality and prey type. J Zool 273:372–381. doi:10.1111/j.1469-7998.2007.00337.x

    Article  Google Scholar 

  • Bosso L, Rebelo H, Garonna AP, Russo D (2012) Modelling geographic distribution and detecting conservation gaps in Italy for the threatened beetle Rosalia alpina. J Nat Conserv 21:72–80. doi:10.1016/j.jnc.2012.10.003

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Bruno D, Belmar O, Sánchez-Fernández D, Guareschi S, Millán A, Velasco J (2014) Responses of Mediterranean aquatic and riparian communities to human pressures at different spatial scales. Ecol Indic 45:456–464. doi:10.1016/j.ecolind.2014.05.051

    Article  Google Scholar 

  • Butchart SHM, Walpole M, Collen B, van Strien A, Scharlemann JPW, Almond REA, Baillie JEM, Bomhard B, Brown C, Bruno J, Carpenter KE, Carr GM, Chanson J, Chenery AM, Csirke J, Davidson NC, Dentener F, Foster M, Galli A, Galloway JN, Genove P, Gregory RD, Hockings M, Kapos V, Lamarque JF, Leverington F, Loh J, McGeoch MA, McRae L, Minasyan A, Hernández-Morcillo M, Oldfield TEE, Pauly D, Quader S, Revenga C, Sauer JR, Skolnik B, Spear D, Stanwell-Smith D, Suart SN, Symes A, Tierney M, Tyrrell TD, Vié JC, Watson R (2010) Global biodiversity: indicators of recent declines. Science 328:1164–1168. doi:10.1126/science.1187512

    Article  CAS  PubMed  Google Scholar 

  • Civantos E, Thuiller W, Maiorano L, Guisan A, Araújo MB (2012) Potential impacts of climate change on ecosystem services in Europe: the case of pest control by vertebrates. Bioscience 62:658–666. doi:10.1525/bio.2012.62.7.8

    Article  Google Scholar 

  • Cox RL, Underwood EC (2011) The importance of conserving biodiversity outside of protected areas in Mediterranean ecosystems. PLoS One doi:10.1371/journal.pone.0014508

    Google Scholar 

  • Crouzeilles R, Lorini ML, Viveiros-Grelle CE (2013) The importance of using sustainable use protected areas for functional connectivity. Biol Conserv 159:450–457. doi:10.1016/j.biocon.2012.10.023

    Article  Google Scholar 

  • D’Amen M, Bombi P, Campanaro A, Zapponi L, Bologna MA, Mason F (2013) Protected areas and insect conservation: questioning the effectiveness of Natura 2000 network for saproxylic beetles in Italy. Anim Conserv 16:370–378. doi:10.1111/acv.12016

    Article  Google Scholar 

  • Daniel S, Korine C, Pinshow B (2008) Central-place foraging in nursing, arthropod-gleaning bats. Can J Zool 86:623–626. doi:10.1139/Z08-041

    Article  Google Scholar 

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

    Google Scholar 

  • Dimitrakopoulos PG, Memtsas D, Troumbis AY (2004) Questioning the effectiveness of the Natura 2000 special areas of conservation strategy: the case of Crete. Glob Ecol Biogeogr 13:199–207. doi:10.1111/j.1466-822X.2004.00086.x

    Article  Google Scholar 

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

    Google Scholar 

  • Gaston KJ, Jackson SF, Nagy A, Cantú-Salazar A, Johnson M (2008) Protected areas in Europe: principle and practice. Ann NY Acad Sci 1134:97–119. doi:10.1196/annals.1439.006

    Article  PubMed  Google Scholar 

  • Grodzinska-Jurczak M, Cent J (2011) Expansion of nature conservation areas: problems with Natura 2000 implementation in Poland? Environ Manag 47:11–27. doi:10.1007/s00267-010-9583-2

    Article  Google Scholar 

  • Gruber B, Evans D, Henle K, Bauch B, Schmeller D, Dziock F, Henry PY, Lengyel S, Margules C, Dormann C (2012) Mind the gap!: How well does Natura 2000 cover species of European interest? Nat Conserv 3:45–62. doi:10.3897/natureconservation.3.3732

    Article  Google Scholar 

  • Haysom K, Dekker J, Russ J, van der Meij T, van Strien A (2013) European bat population trends: a prototype biodiversity indicator. EEA Technical report 19/2013. Brussels. http://www.eea.europa.eu/publications/european-bat-population-trends-2013

  • Hochkirch A, Schmitt T, Beninde J, Hiery M, Kinitz T, Kirschey J, Matenaar D, Rohde K, Stoefen A, Wagner N, Zink A, Lötters S, Veith M, Proelss A (2013) Europe needs a new vision for a Natura 2000 network. Conserv Lett 6:462–467. doi:10.1111/conl.12006

    Article  Google Scholar 

  • Ibáñez C, García-Mudarra JL, Ruedi M, Stadelmann B, Juste J (2006) The Iberian contribution to cryptic diversity in European bats. Acta Chiropterol 8:277–297. doi:10.3161/1733-5329(2006)8[277:TICTCD]2.0.CO;2

    Article  Google Scholar 

  • Jones G, Jacobs DS, Kunz TH, Willig MR, Racey PA (2009) Carpe noctem: the importance of bats as bioindicators. Endanger Species Res 8:93–115. doi:10.3354/esr00182

    Article  Google Scholar 

  • Juste J, Benda P, García-Mudarra JL, Ibáñez C (2013) Phylogeny and systematics of Old World serotine bats (genus Eptesicus, Vespertilionidae, Chiroptera): an integrative approach. Zool Scr 42:441–457. doi:10.1111/zsc.12020

    Article  Google Scholar 

  • Kati V, Hovardas T, Dieterich M, Ibisch PL, Mihok M, 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 

  • Knight T, Jones G (2009) Importance of night roosts for bat conservation: roosting behaviour of the lesser horseshoe bat Rhinolophus hipposideros. Endanger Species Res 8:79–86. doi:10.3354/esr00194

    Article  Google Scholar 

  • Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats. Ann NY Acad Sci 1223:1–38. doi:10.1111/j.1749-6632.2011.06004.x

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • 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 

  • 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 

  • Lisón F, Haz A, Calvo JF (2014) Preferencia de hábitat del murciélago hortelano meridional Eptesicus isabellinus (Temminck, 1840) en ambientes mediterráneos semiáridos. Anim Biodivers Conserv 37:59–67

    Google Scholar 

  • Loucks C, Ricketts TH, Naidoo R, Lamoreux J, Hoekstra J (2008) Explaining the global pattern of protected area coverage: relative importance of vertebrate biodiversity, human activities and agricultural suitability. J Biogeogr 35:1337–1348. doi:10.1111/j.1365.2699.2008.01899.x

    Article  Google Scholar 

  • Lundy M, Montgomery I (2010) Summer habitat associations of bats between riparian landscapes and within riparian areas. Eur J Wildlife Res 56:385–394. doi:10.1007/s10344-009-0330-z

    Article  Google Scholar 

  • Maes J, Paracchini ML, Zulian G, Dunbar MB, Alkemade R (2012) Synergies and trade-offs between ecosystem service supply, biodiversity, and habitat conservation status in Europe. Biol Conserv 155:1–12. doi:10.1016/j.biocon.2012.06.016

    Article  Google Scholar 

  • Maiorano L, Falcucci A, Garton AEO, Boitani L (2007) Contribution of the Natura 2000 Network to biodiversity conservation in Italy. Conserv Biol 21:1433–1444. doi:10.1111/j.1523-1739.2007.00831.x

    Article  PubMed  Google Scholar 

  • Maiorano L, Falcucci A, Zimmermann NE, Psomas A, Pottier J, Baisero D, Rondinini C, Guisan A, Boitani L (2011) The future of terrestrial mammals in the Mediterranean basin under climate change. Philos Trans Roy Soc B 366:2681–2692. doi:10.1098/rstb.2011.0121

    Article  Google Scholar 

  • Martínez-Fernández J, Esteve MA, Calvo JF (2000) Environmental and socioeconomic interactions in the evolution of traditional irrigated lands: a dynamics system model. Hum Ecol 28:279–299. doi:10.1023/A:1007024204961

    Article  Google Scholar 

  • Martínez-Fernández J, Esteve MA, Baños-González I, Carreño F, Moreno A (2013) Sustainability of Mediterranean irrigated agro-landscapes. Ecol Model 248:11–19

    Article  Google Scholar 

  • McDonald RI, Boucher TM (2010) Global development and the future of the protected area strategy. Biol Conserv 144:383–392. doi:10.1016/j.biocon.2010.09.016

    Article  Google Scholar 

  • Monadjem A, Reside A (2008) The influence of riparian on the distribution and abundance of bat in an African savanna. Acta Chiropterol 10:339–348. doi:10.3161/150811008X414917

    Article  Google Scholar 

  • O’Keefe JM, Loeb SC, Gerard PD, Lanham JD (2013) Effects of riparian buffer width on activity and detection of common bats in the southern Appalachian Mountains. Wildlife Soc Bul 37:319–326. doi:10.1002/wsb.267

    Article  Google Scholar 

  • Ormerod SJ (2014) Rebalancing the philosophy of river conservation. Aquat Conserv 24:147–152. doi:10.1002/aqc.2452

    Article  Google Scholar 

  • Palomo LJ, Gisbert J, Blanco JC (2007) Atlas y Libro Rojo de los Mamíferos Terrestres de España. Dirección General de la Biodiversidad-SECEM-SECEMU, Madrid

    Google Scholar 

  • Pellissier V, Touroult J, Julliard R, Siblet JP, Jiguet F (2013) Assessing the Natura 2000 network with a common breeding birds survey. Anim Conserv 16:566–574. doi:10.1111/acv.12030

    Article  Google Scholar 

  • Piquer-Rodríguez M, Kuemmerle T, Alcaraz-Segura D, Zurita-Milla R, Cabello J (2012) Future land use effects on the connectivity of protected area networks in southeastern Spain. J Nat Conserv 20:326–336. doi:10.1016/j.jnc.2012.07.001

    Article  Google Scholar 

  • R Core Team. (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing. Vienna, Austria. URL http://www.R-project.org/

  • Rainho A, Palmeirim JM (2011) The importance of distance to resources in the spatial modeling of bat foraging habitat. PLoS One 6:e19227. doi:10.1371/journal.pone.0019227

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rainho A, Palmeirim JM (2013) Prioritizing conservation areas around multispecies bat colonies using spatial modeling. Anim Conserv 16:438–448. doi:10.1111/acv.12013

    Article  Google Scholar 

  • Rodríguez-Rodríguez D, Martínez-Vega J (2012) Proposal of a system for the integrated and comparative assessment of protected areas. Ecol Indic 23:566–572. doi:10.1016/j.ecolind.2012.05.009

    Article  Google Scholar 

  • Rosati L, Marignani M, Blasi C (2008) A gap analysis comparing Natura 2000 versus National protected area network with potential natural vegetation. Commun Ecol 9:147–154

    Article  Google Scholar 

  • Russo D, Jones G (2003) Use of foraging habitats by bats in a Mediterranean area determined by acoustic surveys: conservation implications. Ecography 26:197–209

    Article  Google Scholar 

  • Sánchez-Fernández D, Abellán P (2015) Using null models to identify under-represented species by protected areas: an example with European amphibians and reptiles. Biol Conserv 184:290–299. doi:10.1016/j.biocon.2015.02.006

    Article  Google Scholar 

  • Sánchez-Fernández D, Bilton DT, Abellán P, Ribera I, Velasco J, Millán A (2008) Are the endemic water beetles of the Iberian Peninsula and the Balearic Islands effectively protected? Biol Conserv 141:1612–1627. doi:10.1016/j.biocon.2008.04.005

    Article  Google Scholar 

  • Sánchez-Fernández D, Abellán P, Picazo F, Millán A, Ribera I, Lobo JM (2013) Do protected areas represent species optimal climatic conditions? Divers Distrib 19:1407–1417. doi:10.1111/ddi.12104

    Article  Google Scholar 

  • Santos H, Juste J, Ibáñez C, Palmeirim JM, Godinho R, Amorim F, Alves P, Costa H, de Paz O, Pérez-Suarez G, Martínez-Alos S, Jones G, Rebelo H (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 

  • Scott JM, Davis F, Csuti B, Noss R, Butterfield B, Groves C, Anderson H, Caicco S, D’Erchia F, Edwards TC, Ulliman J, Wright RG (1993) Gap analysis: a geographic approach to protection of biological diversity. Wildlife Monograph 123:1–41

    Google Scholar 

  • Skokanová H, Eremiášová R (2013) Landscape functionality in protected and unprotected area: case studies from the Czech Republic. Ecol Inform 14:71–74. doi:10.1016/j.ecoinf.2012.11.007

    Article  Google Scholar 

  • Trochet A, Schmeller DS (2013) Effectiveness of the Natura 2000 network to cover threatened species. Nat Conserv 4:35–53. doi:10.3897/natureconservation.4.3626

    Article  Google Scholar 

  • Venter O, Fuller RA, Segan DB, Carwardine J, Brooks T, Butchart SHM, Di Marco M, Iwamura T, Joseph L, O’Grady D, Possingham HP, Rondinini C, Smith RJ, Venter M, Watson JEM (2014) Targeting global protected areas expansion for imperiled biodiversity. PLoS Biol 12:e1001891. doi:10.1371/journal.pbio.1001891

    Article  PubMed Central  PubMed  Google Scholar 

  • Verboom B, Huitema H (1997) The importance of linear landscape elements for the pipistrelle Pipistrellus pipistrellus and serotine Eptesicus serotinus. Landscape Ecol 277:494–499

    Google Scholar 

  • Vimal R, Rodrigues ASL, Mathevet R, Thompson JD (2011) The sensitivity of gap analysis to conservation targets. Biodivers Conserv 20:531–543. doi:10.1007/s10531-010-9963-1

    Article  Google Scholar 

  • Zehetmair T, Müller J, Runkel V, Stahlschmidt P, Winter S, Zharov A, Gruppe A (2014) Poor effectiveness of Natura 2000 beech forests in protecting forest-dwelling bats. J Nat Conserv 23:53–60

    Article  Google Scholar 

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Acknowledgements

We are grateful for the important contributions of bat workers and SECEMU members to the development of the distribution of bat fauna of Spain. We are also grateful for the support and the comments of the people of “Ecosistemas Mediterráneos” and “Ecología Acuática” research groups (University of Murcia), especially Félix Picazo. We thank Philip Thomas and Ángeles Haz for correcting the English. The first version of the manuscript was considerably improved by the comments of anonymous reviewers and the editors. D. S.-F. was supported by a postdoctoral Grant (Juan de La Cierva programme) from Spanish Ministry of Economy and Competitiveness.

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  1. Departamento de Ecología e Hidrología, Universidad de Murcia, Campus de Espinardo, 30100, Murcia, Spain

    Fulgencio Lisón & José F. Calvo

  2. Institut de Biologia Evolutiva (UPF-CSIC), Passeig Maritim de la Barceloneta 37-49, 08003, Barcelona, Spain

    David Sánchez-Fernández

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  1. Fulgencio Lisón
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  2. David Sánchez-Fernández
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Communicated by Danna J. Leaman.

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Lisón, F., Sánchez-Fernández, D. & Calvo, J.F. 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 (2015). https://doi.org/10.1007/s10531-015-0937-1

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