Conservation planning with spatially explicit models: a case for horseshoe bats in complex mountain landscapes

Abstract

Context

Context Bats are considered as an ecological indicator of habitat quality due to their sensitivity to human-induced ecosystem changes. Hence, we will focus the study on two indicator species of bats as a proxy to evaluate structure and composition of the landscape to analyze anthropic pressures driving changes in patterns.

Objectives

This study develops a spatially-explicit model to highlight key habitat nodes and corridors which are integral for maintaining functional landscape connectivity for bat movement. We focus on a complex mountain landscape and two bat species: greater (Rhinolophus ferrumequinum) and lesser (Rhinolophus hipposideros) horseshoe bats which are known to be sensitive to landscape composition and configuration.

Methods

Species distribution models are used to delineate high-quality foraging habitat for each species using opportunistic ultrasonic bat data. We then performed connectivity analysis combining (modelled) suitable foraging habitat and (known) roost sites. We use graph-theory and the deviation in the probability of connectivity to quantify resilience of the landscape connectivity to perturbations.

Results

Both species were confined to lowlands (<1000 m elevation) and avoided areas with high road densities. Greater horseshoe bats were more generalist than lesser horseshoe bats which tended to be associated with broadleaved and mixed forests.

Conclusions

The spatially-explicit models obtained were proven crucial for prioritizing foraging habitats, roost sites and key corridors for conservation. Hence, our results are being used by key stakeholders to help integrate conservation measures into forest management and conservation planning at the regional level. The approach used can be integrated into conservation initiatives elsewhere.

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References

  1. Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232

    Article  Google Scholar 

  2. Archaux F, Tillon L, Fauvel B, Martin H (2013) Foraging habitat use by bats in a large temperate oak forest: importance of mature and regeneration stands. Le Rhinolophe 19:47–58

    Google Scholar 

  3. Arthur L, Lemaire M (2009) Les chauves-souris de France, Belgique, Luxembourg et Suisse (Biotope Eds)

  4. Baldwin RA (2009) Use of maximum entropy modeling in wildlife research. Entropy 11:854–866

    Article  Google Scholar 

  5. Barataud M (2012) Ecologie acoustique des chiroptères d’Europe. Identification des espèces, études de leurs habitats et comportements de chasse (BIOTOPE ÉDITIONS)

  6. Bellamy C, Altringham J (2015) Predicting species distributions using record centre data: multi-scale modelling of habitat suitability for bat roosts. PLoS ONE 10(6):e0128440

    Article  PubMed  PubMed Central  Google Scholar 

  7. Bellamy CC, Scott CD, Altringham JD (2013) Multiscale, presence-only habitat suitability models: fine resolution models for eight bat species. J Appl Ecol 50:892–901

    Article  Google Scholar 

  8. Bennett VJ, Sparks DW, Zollner PA (2013) Modeling the indirect effects of road networks on the foraging activities of bats. Landsc Ecol 28:979–991

    Article  Google Scholar 

  9. Berthinussen A, Altringham J (2012a) Do bat gantries and underpasses help bats cross roads safely? PLoS ONE 7:e38775

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  10. Berthinussen A, Altringham J (2012b) The effect of a major road on bat activity and diversity. J Appl Ecol 49:82–89

    Article  Google Scholar 

  11. Blanchard R (1918) Le contraste climatique entre Vercors et Diois. Recl Trav Inst Géographie Alp 6:427–446

    Article  Google Scholar 

  12. Bontadina F, Schofield H, Naef-Daenzer B (2002) Radio-tracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland. J Zool 258:281–290

    Article  Google Scholar 

  13. Breiman L, Friedman J, Olshen R, Stone C (1984) Classification and regression trees. Chapman & Hall, London

    Google Scholar 

  14. Chaverri G, Kunz TH (2011) Response of a specialist bat to the loss of a critical resource. PLoS ONE 6:e28821

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  15. Correa CA, Mendoza ME, Etter A, Perez Salicrup DR (2016) Habitat connectivity in biodiversity conservation: a review of recent studies and applications. Prog Phys Geogr 40(1):7–37

    Article  Google Scholar 

  16. Decout S, Manel S, Miaud C, Luque S (2012) Integrative approach for landscape-based graph connectivity analysis: a case study with the common frog (Rana temporaria) in human-dominated landscapes. Landsc Ecol 27:267–279

    Article  Google Scholar 

  17. Dixon MD, Heist K, Tinsley K (2013) The state of bats in conservation planning for the national wildlife refuge system with recommendations. J Fish Wildl Manag 4:406–422

    Article  Google Scholar 

  18. Downs NC, Cresswell Warren J, Reason P, Sutton G, Wells D, Wray S (2016) Sex-specific habitat preferences of foraging and commuting lesser horseshoe bats Rhinolophus hipposideros (Borkhausen, 1797) in Lowland England. Acta Chiropter 18:451–465

    Article  Google Scholar 

  19. Elith J, Leathwick JR, Hastie T (2008) A working guide to boosted regression trees. J Anim Ecol 77:802–813

    CAS  Article  PubMed  Google Scholar 

  20. Elith J, Philips SJ, Hastie T, Dudik M, En Chee Y, Yates CJ (2011) A statistical explanation of MaxEnt for ecologists. Divers Distrib 17:43–57

    Article  Google Scholar 

  21. Entwistle A (2001) Habitat management for bats: a guide for land managers, land owners and their advisors (Peterborough: Joint Nature Conservation Committee (Great Britain))

  22. Fall A, Fortin M-J, Manseau M, O’Brien D (2007) Spatial graphs: principles and applications for habitat connectivity. Ecosystems 10:448–461

    Article  Google Scholar 

  23. Flanders J, Jones G (2009) Roost use, ranging behavior, and diet of greater horseshoe bats (Rhinolophus Ferrumequinum) using a transitional roost. J Mammal 90:888–896

    Article  Google Scholar 

  24. Friedman JH (1991) Multivariate adaptive regression splines. Ann Os Stat 19:1–141

    Article  Google Scholar 

  25. Gonzalez-Redin J, Luque S, Poggio L, Smith R, Gimona A (2016) Spatial Bayesian belief networks as a planning decision tool for mapping ecosystem services trade-offs on forested landscapes. Environ Res 144:15–26

    CAS  Article  PubMed  Google Scholar 

  26. Guisan A, Edwards TC, Hastie T (2002) Generalized linear and generalized additive models in studies of species distributions: setting the scene. Ecol Model 157:89–100

    Article  Google Scholar 

  27. Guisan A, Thuiller W (2005) Predicting species distribution: offering more than simple habitat models. Ecol Lett 8:993–1009

    Article  Google Scholar 

  28. Hastie T, Tibshirani R, Buja A (1994) Flexible discriminant analysis by optimal scoring. J Am Stat Assoc 89:1255–1270

    Article  Google Scholar 

  29. Holzhaider J, Kriner E, Rudolph B-U, Zahn A (2002) Radio-tracking a Lesser horseshoe bat (Rhinolophus hipposideros) in Bavaria: an experiment to locate roosts and foraging sites. Myotis 40:47–54

    Google Scholar 

  30. Ingersoll TE, Sewall BJ, Amelon SK (2013) Improved analysis of long-term monitoring data demonstrates marked regional declines of bat populations in the eastern United States. PLoS ONE 8:e65907

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  31. Jaberg C, Guisan A (2001) Modelling the distribution of bats in relation to landscape structure in a temperate mountain environment. J Appl Ecol 38:1169–1181

    Article  Google Scholar 

  32. Kaňuch P, Danko Š, Celuch M, Krištín A, Pjenčák P, Matis š, Šmídt J (2008) Relating bat species presence to habitat features in natural forests of Slovakia (Central Europe). Mamm Biol Z. Für Säugetierkd 73:147–155

    Article  Google Scholar 

  33. Kokurewicz T (1990) The decrease in abundance of the lesser horseshoe bat Rhinolophus Hipposideros Bechstein, 1800 (Chiroptera: Rhinolophidae) in Winter Quarters in Poland. Myotis 109–118

  34. Kunz TH, Braun de Torrez E, Bauer D, Lobova T, Fleming TH (2011) Ecosystem services provided by bats: ecosystem services provided by bats. Ann N Y Acad Sci 1223:1–38

    Article  PubMed  Google Scholar 

  35. Le Roux M, Luque S, Vincent S, Planckaert O (2014) Integration de la connectivite dans la gestion et la conservation des habitats. Sciences Eaux et Territoires, 14: 20–25 https://hal.archives-ouvertes.fr/hal-01071937

  36. Le Roux M, Redon M, Vincent S, Tillon L, Bouix T, Archaux F, Luque S (2016) La modélisation spatiale des habitats et des corridors: un outil pour la conservation et la gestion des chauves-souris Symbioses, nouvelle série, n° 34:28–34

  37. Lebrun F, Coudène M (2011) Vercors: un développement à deux vitesses (INSEE)

  38. Luque S, Saura S, Fortin M-J (2012) Landscape connectivity analysis for conservation: insights from combining new methods with ecological and genetic data. Landsc Ecol 27:153–157

    Article  Google Scholar 

  39. Manel S, Dias JM, Buckton ST, Ormerod SJ (1999) Alternative methods for predicting species distribution: an illustration with Himalayan river birds. J Appl Ecol 36:734–747

    Article  Google Scholar 

  40. McRae BH, Dickson BG, Keitt TH, Shah VB (2008) Using circuit theory to model connectivity in ecology, evolution, and conservation. Ecology 89:2712–2724

    Article  PubMed  Google Scholar 

  41. Medinas D, Marques JT, Mira A (2012) Assessing road effects on bats: the role of landscape, road features, and bat activity on road-kills. Ecol Res 28:227–237

    Article  Google Scholar 

  42. Mickleburgh SP, Hutson AM, Racey PA (2002) A review of the global conservation status of bats. Oryx 36:18–34

    Article  Google Scholar 

  43. Monserud RA, Leemans R (1992) Comparing global vegetation maps with the kappa statistic. Ecol Model 62:275–293

    Article  Google Scholar 

  44. Motte G, Libois R (2002) Conservation of the lesser horseshoe bat (Rhinolophus hipposideros Bechstein, 1800)(Mammalia: Chiroptera) in BelgiumA case study of feeding habitat requirements. Belg J Zool 132:49

    Google Scholar 

  45. Nelson E, Mendoza G, Regetz J, Polasky S, Tallis H, Cameron D, Chan K, Daily GC, Goldstein J, Kareiva PM, Lonsdorf E (2009) Modelling multiple ecosystem services, biodiversity conservation, commodity production, and tradeoffs at landscape scales. Front Ecol Environ 7(1):4–11

    Article  Google Scholar 

  46. O’Shea TJ, Bogan MA, Ellison LE (2003) Monitoring trends in bat populations of the United States and territories: status of the science and recommendations for the future. Wildl Soc Bull 31:16–29

    Google Scholar 

  47. Pearce J, Ferrier S (2000) Evaluating the predictive performance of habitat models developed using logistic regression. Ecol Model 133:225–245

    Article  Google Scholar 

  48. Racey PA (2009) Bats: status, threats and conservation successes Introduction. Endanger Species Res 8:1–3

    Article  Google Scholar 

  49. Ransome RD, Hutson AM (2000) Action plan for conservation of the greater horseshoe bat (Rhinolophus ferrumequinum) in Europe (Council of Europe)

  50. Razgour O Rebelo H, Di Febbraro M, Russo D (2016) Painting maps with bats: species distribution modelling in bat research and conservation Hystrix, the Italian Journal of Mammalogy 27(1) ISSN 1825-5272

  51. Razgour O, Rebelo H, Puechmaille SJ, Juste J, Ibáñez C, Kiefer A, Burke T, Dawson DA, Jones G (2014) Scale-dependent effects of landscape variables on gene flow and population structure in bats. Divers Distrib 20:1173–1185.

    Article  Google Scholar 

  52. Rebelo H, Jones G (2010) Ground validation of presence-only modelling with rare species: a case study on barbastelles Barbastella barbastellus (Chiroptera: Vespertilionidae). J Appl Ecol 47:410–420

    Article  Google Scholar 

  53. Reiter G (2004) The importance of woodland for Rhinolophus hipposideros (Chiroptera, Rhinolophidae) in Austria. Mamm Mamm 68:403–410

    Google Scholar 

  54. Reiter G, Pölzer E, Mixanig H, Bontadina F, Hüttmeir U (2013) Impact of landscape fragmentation on a specialised woodland bat, Rhinolophus hipposideros. Mamm Biol Z Für Säugetierkd 78:283–289

    Article  Google Scholar 

  55. Rossiter S, Jones G, Ransome R, Barratt E (2002) Relatedness structure and kin-biased foraging in the greater horseshoe bat (Rhinolophus ferrumequinum). Behav Ecol Sociobiol 51:510–518

    Article  Google Scholar 

  56. Roy HE, Pocock MJO, Preston CD, Roy DB, Savage J, Tweddle JC, Robinson LD (2012) Understanding Citizen Science & Environmental Monitoring. Final Report on behalf of UK-EOF. NERC Centre for Ecology & Hydrology and Natural History Museum

  57. Russell A, Butchkoski C, Saidak L, McCracken G (2009) Road-killed bats, highway design, and the commuting ecology of bats. Endanger Species Res 8:49–60

    Article  Google Scholar 

  58. Saura S, Pascual-Hortal L (2007) A new habitat availability index to integrate connectivity in landscape conservation planning: comparison with existing indices and application to a case study. Landsc Urban Plan 83(2–3):91–103

    Article  Google Scholar 

  59. Saura S, Rubio L (2010) A common currency for the different way in which patches and links can contribute to habitat availability and connectivity in the landscape. Ecography 33:523–537

    Google Scholar 

  60. Saura S, Torné J (2009) Conefor Sensinode 2.2: a sofware package for quantifying the importance of habitat patches for landscape connectivity. Environ Model Sofware 24:135–139

    Article  Google Scholar 

  61. Siemers BM, Schaub A (2011) Hunting at the highway: traffic noise reduces foraging efficiency in acoustic predators. Proc R Soc B-Biol Sci 278:1646–1652

    Article  Google Scholar 

  62. Tenerelli P, Demšar U, Luque S (2016) Crowdsourcing indicators for cultural ecosystem services: a geographically weighted approach for mountain landscapes. Ecol Indic 64:237–248

    Article  Google Scholar 

  63. Thuiller W, Georges D, Engler R, Breiner F (2016) biomod2: Ensemble platform for species distribution modeling. R package version 3.3–7. http://CRAN.R-project.org/package=biomod2

  64. Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD–a platform for ensemble forecasting of species distributions. 369–373

  65. Tournant P, Afonso E, Roué S, Giraudoux P, Foltête J-C (2013) Evaluating the effect of habitat connectivity on the distribution of lesser horseshoe bat maternity roosts using landscape graphs. Biol Conserv 164:39–49

    Article  Google Scholar 

  66. UICN (2003) Lignes directrices pour l’application, au niveau régional, des critères de l’UICN pour la liste rouge (Gland [etc.]; Cambridge: UICN, Union mondiale pour la nature; disponible auprès du: Service des publications de l’UICN)

  67. Urban D, Keitt T (2001) Landscape connectivity: a graph-theoretic perspective. Ecology 82:1205–1218

    Article  Google Scholar 

  68. Vincent PJ, Haworth JM (1983) Poisson regression models of species abundance. J Biogeogr 10:153

    Article  Google Scholar 

  69. Warren RD, Witter MS (2002) Monitoring trends in bat populations through roost surveys: methods and data from Rhinolophus hipposideros. Biol Conserv 105:255–261

    Article  Google Scholar 

  70. Willis CKR, Brigham RM (2004) Roost switching, roost sharing and social cohesion: forest-dwelling big brown bats, Eptesicus fuscus, conform to the fission–fusion model. Anim Behav 68:495–505

    Article  Google Scholar 

  71. Wordley CFR, Sankaran M, Mudappa D, Altringham JD (2015) Landscape scale habitat suitability modelling of bats in the Western Ghats of India: bats like something in their tea. Biol Cons 191(2015):529–536.

    Article  Google Scholar 

  72. Zahn A, Holzhaider J, Kriner E, Maier A, Kayikcioglu A (2008) Foraging activity of Rhinolophus hipposideros on the Island of Herrenchiemsee, Upper Bavaria. Mamm Biol Z Für Säugetierkd 73:222–229

    Article  Google Scholar 

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Acknowledgements

This work was partly Funded by the French Ministry of Ecology, Sustainable Development and Energy, France in support of the development of the DEB-MOCHAB project (2013–2015) (Species distribution modelling: a tool for evaluation the conservation of species’ habitats and ecological continuities). We thank the LPO (League for the Protection of Birds), the Departments of Drôme and Isère, France and the National Forest Office for their interest, support, expertise of species ecology and time invested in this project. In particular, we would like to thank Tillon, L., Planckaert, O, Bouix, T and everyone who contributed in the data collection efforts and expertise. Santiago Saura for advice on landscape connectivity analysis. Damien Gorges for his work on Biomod2 package improvement and support. We would like to thank the Editor and the two anonymous reviewers for their valuable and very constructive comments and suggestions that helped improve the manuscript.

This work was also partially supported by the OpenNESS project funded from the European Union’s Seventh Programme for research, technological development and demonstration under grant agreement n° 308428. The authors are solely responsible for the content of this publication. It does not represent the opinion of the European Union, nor is the European Union responsible for any use that might be made of information appearing herein.

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Correspondence to Sandra Luque.

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Le Roux, M., Redon, M., Archaux, F. et al. Conservation planning with spatially explicit models: a case for horseshoe bats in complex mountain landscapes. Landscape Ecol 32, 1005–1021 (2017). https://doi.org/10.1007/s10980-017-0505-z

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Keywords

  • Species distribution modelling
  • Ensemble modelling
  • Expert based knowledge
  • Landscape connectivity
  • Landscape structure
  • Complex mountain landscapes
  • Greater horseshoe bat
  • Lesser horseshoe bat