Skip to main content

Advertisement

Log in

Different bat guilds perceive their habitat in different ways: a multiscale landscape approach for variable selection in species distribution modelling

  • Research Article
  • Published:
Landscape Ecology Aims and scope Submit manuscript

Abstract

Context

Unveiling the scale at which organisms respond to habitat features is crucial to understand how they are influenced by anthropogenic environmental changes. We implemented species distribution models (SDMs) based on multiple-scale landscape pattern analysis for four bat species representative of different foraging guilds: Nyctalus leisleri, Rhinolophus hipposideros, Myotis emarginatus and Pipistrellus pipistrellus.

Objectives

(a) to assess the environmental factors and the influence of scale on the habitat suitability of bats; (b) to develop an objective methodology to select the best performing variables from a large variable dataset.

Methods

We performed the study in central Italy (Tuscany): 381 variables were derived from topographical and habitat maps using a moving windows analysis set at three spatial scales (1, 5 and 10 km) that are ecologically meaningful for bats. For each species, we ran 381 univariate models to select the variables for multivariate SDMs.

Results

All the variables retained in the SDMs described spatial pattern indices underlining the importance of landscape structure for species distribution. Species reacted differently in terms of both scale and landscape pattern. P. pipistrellus only responded to variables at 10 km; N. leisleri and M. emarginatus did so at two scales (5 and 10 km); whereas R. hipposideros also responded to variables at 1 km.

Conclusions

Our findings make it possible to tailor SDMs according to species-specific landscape pattern requirements at appropriate scales. Our approach, which can be easily extended to other taxa and different spatial scales, represents a significant step towards more effective land management planning.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agnelli P, Castelli C, Ducci L, Foggi B, Frizzi F, Giunti M, Guidi T, Puglisi L, Santini G, Vanni S, (2014) Elaborazioni analitiche a supporto della Rete Ecologica Toscana. In Reti ecologiche e paesaggio per il governo del territorio in Toscana (a cura di Falqui e Paolinelli). Collana Paesaggio, ISPRA, ETS Pisa

  • 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(6):1223–1232

    Article  Google Scholar 

  • Araújo MB, Pearson RG, Thuiller W, Erhard M (2005) Validation of species–climate impact models under climate change. Glob Chang Biol 11(9):1504–1513

    Article  Google Scholar 

  • Baddeley A, Turner R (2012). Package ‘spatstat’. http://www.spatstat.org

  • Battersby J (2010) Guidelines for surveillance, monitoring of European bats. EUROBATS Publication series No. 5. UNEP/EUROBATS Secretariat, Bonn, p 95

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

    Article  Google Scholar 

  • Bontadina F, Schofield H, Naef-Daenzer B (2002) Radio-tracking reveals that lesser horseshoe bats (Rhinolophus hipposideros) forage in woodland. J Zool 258(03):281–290

    Article  Google Scholar 

  • Booth GD, Niccolucci MJ, Schuster EG (1994) Identifying proxy sets in multiple linear regression: an aid to better coefficient interpretation Research Paper INT-470n. United States Department of Agriculture, Forest Service), Ogden

    Google Scholar 

  • Bosso L, Rebelo H, Garonna AP, Russo D (2013) Modelling geographic distribution, detecting conservation gaps in Italy for the threatened beetle Rosalia alpine. J Nat Conserv 21:72–80

    Article  Google Scholar 

  • Boughey KL, Lake IR, Haysom KA, Dolman PM (2011) Improving the biodiversity benefits of hedgerows: how physical characteristics and the proximity of foraging habitat affect the use of linear features by bats. Biol Conserv 144(6):1790–1798

    Article  Google Scholar 

  • Clark PJ, Evans FC (1954) Distance to nearest neighbour as a measure of spatial relationships in populations. Ecology 34:445–453

    Article  Google Scholar 

  • Cushman SA, McGarigal K, Neel MC (2008) Parsimony in landscape metrics: strength, universality, and consistency. Ecol Ind 8:691–703

    Article  Google Scholar 

  • Di Febbraro M, Lurz PW, Genovesi P, Maiorano L, Girardello M, Bertolino S (2013) The use of climatic niches in screening procedures for introduced species to evaluate risk of spread: a case with the American eastern grey squirrel. PLoS One 8(7):e66559

    Article  PubMed Central  PubMed  Google Scholar 

  • Dietz C, Von Helversen O (2004) Illustrated identification key to the bats of Europe. Eur Bat Res Symp 1:11–157

    Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, García Marquéz J, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne P, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S (2013) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Article  Google Scholar 

  • Ehrenbold AF, Bontadina F, Arlettaz R, Obrist MK (2013) Landscape connectivity, habitat structure and activity of bat guilds in farmland-dominated matrices. J Appl Ecol 50(1):252–261

    Article  Google Scholar 

  • Elith J, Graham CH, Person RP, Dudík M, Ferrier S, Guisan A, Hijmans RJ, Huettmann F, Leathwick JR, Lehmann A, Li J, Lohmann LG, Loiselle BA, Manion G, Moritz C, Nakamura M, Nakazawa Y, McC Overton J, Peterson AT, Phillips SJ, Karen Richardson K, Scachetti-Pereira R, Schapire RE, Soberón J, Williams S, Wisz MS, Zimmermann NE (2006) Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29:129–151

    Article  Google Scholar 

  • Flaquer C, Puig-Montserrat X, Burgas A, Russo D (2008) Habitat selection by Geoffroy’s bats (Myotis emarginatus) in a rural Mediterranean landscape: implications for conservation. Acta Chiropterol 10(1):61–67

    Article  Google Scholar 

  • Forman RT (1995) Some general principles of landscape and regional ecology. Landscape Ecol 10(3):133–142

    Article  Google Scholar 

  • Gehrt SD, Chelsvig JE (2003) Bat activity in an urban landscape: patterns at the landscape and microhabitat scale. Ecol Appl 13(4):939–950

    Article  Google Scholar 

  • Goiti U, Aihartza J, Guiu M, Salsamendi E, Almenar D, Napal M, Garin I (2011) Geoffroy’s bat, Myotis emarginatus, preys preferentially on spiders in multistratified dense habitats: a study of foraging bats in the Mediterranean. Folia Zool 60(1):17–24

    Google Scholar 

  • Gorresen PM, Willig MR, Strauss RE (2005) Multivariate analysis of scaledependent associations between bats and landscape structure. Ecol Appl 15:2126–2136

    Article  Google Scholar 

  • Grantham HS, Wilson KA, Moilanen A, Rebelo T, Possingham HT (2009) Delaying conservation actions for improved knowledge: how long should we wait? Ecol Lett 12:293–301

    Article  PubMed  Google Scholar 

  • Hale JD, Fairbrass AJ, Matthews TJ, Sadler JP (2012) Habitat compo sition and connecti vity predicts bat prese nce and activity at foraging sites in a large UK conurbation. PLoS One 7(3):e33300

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hanley JA, McNeil BJ (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143:29–36

    Article  CAS  PubMed  Google Scholar 

  • Hanspach J, Fischer J, Ikin K, Stott J, Law BS (2012) Using trait-based filtering as a predictive framework for conservation: a case study of bats on farms in southeastern Australia. J Appl Ecol 49(4):842–850

    Article  Google Scholar 

  • Hargis CD, Bissonette JA, Turner DL (1999) The influence of forest fragmentation and landscape pattern on American martens. J Appl Ecol 36:157–172

    Article  Google Scholar 

  • Hirzel AH, Helfer V, Metral F (2001) Assessing habitat-suitability models with a virtual species. Ecol Model 145:111–121

    Article  Google Scholar 

  • Holling CS (1992) Cross-scale morphology, geometry, and dynamics of ecosystems. Ecol Monog 62:447–502

    Article  Google Scholar 

  • Hostetler M, Holling CS (2000) Detecting the scales at which birds respond to structure in urban landscapes. Urban Ecosyst 4(1):25–54

    Article  Google Scholar 

  • Jiguet F, Barbet-Massin M, Henry PY (2010) Predicting potential distributions of two rare allopatric sister species, the globally threatened Doliornis cotingas in the Andes. J Field Ornithol 81(4):325–339

    Article  Google Scholar 

  • Johnson DH (1980) The comparison of usage and availability measurements for evaluating resource preference. Ecology 61:65–71

    Article  Google Scholar 

  • Jones G, Rayner JM (1989) Foraging behavior and echolocation of wild horseshoe bats Rhinolophus ferrumequinum and R. hipposideros (Chiroptera, Rhinolophidae). Behav Ecol Sociobiol 25(3):183–191

    Article  Google Scholar 

  • Jones G, Jacobs DS, Thomas HK, Willing MR, Racey PA (2009) Carpe Noctem: the importance of bats as bioindicators. Endanger Species Res 8:93–115

    Article  Google Scholar 

  • Krull D, Schumm A, Metzner W, Neuweiler G (1991) Foraging areas and foraging behavior in the notch-eared bat, Myotis emarginatus (Vespertilionidae). Behav Ecol Sociobiol 28(4):247–253

    Article  Google Scholar 

  • Le Coeur D, Baudry J, Burel F, Thenail C (2002) Why and how we should study field boundary biodiversity in an agrarian landscape context. Agric Ecosyst Environ 89(1):23–40

    Article  Google Scholar 

  • Li H, Wilkins T (2014) Patch or mosaic: bat activity responds to fine-scale urban heterogeneity in a medium-sized city in the United States. Urban Ecosyst 17:1013–1031

    Article  Google Scholar 

  • Mander Ü, Uuemaa E (2010) Landscape assessment for sustainable planning. Ecol Ind 10(1):1–3

    Article  Google Scholar 

  • Marmion M, Parviainen M, Luoto M, Heikkinen RK, Thuiller W (2009) Evaluation of consensus methods in predictive species distribution modelling. Divers Distrib 15:59–69

    Article  Google Scholar 

  • McGarigal K, McComb WC (1995) Relationships be- tween landscape structure and breeding birds in the Oregon coast range. Ecol Monogr 65:235–260

    Article  Google Scholar 

  • McGarigal K, Cushman S, Reagan C (2005) Quantifying terrestrial habitat loss and fragmentation: a protocol; USDA general technical report. Golden, USDA, Rocky Mountain Region

    Google Scholar 

  • McGarigal K, Cushman SA, Ene E (2012) “FRAGSTATS v4: spatial pattern analysis program for categorical and continuous maps.”. Computer software program produced by the authors at the University of Massachusetts, Amherst. http://www.umass.edu/landeco/research/fragstats/fragstats.html

  • Merckx B, Steyaert M, Vanreusel A, Vincx M, Vanaverbeke J (2011) Null models reveal preferential sampling, spatial autocorrelation and overfitting in habitat suitability modelling. Ecol Model 222:588–597

    Article  CAS  Google Scholar 

  • Mills M, Pressey RL, Weeks R, Foale S, Ban NC (2010) A mismatch of scales: challenges in planning for implementation of marine protected areas in the Coral Triangle. Conserv Lett 3:291–303

    Article  Google Scholar 

  • Moudrý V, Šímová P (2012) Influence of positional accuracy, sample size and scale on modelling species distributions: a review. Int J Geogr Inf Syst 26:2083–2095

    Article  Google Scholar 

  • Nicholls B, Racey PA (2006a) Contrasting home-range size and spatial partitioning in cryptic and sympatric pipistrelle bats. Behav Ecol Sociobiol 61(1):131–142

    Article  Google Scholar 

  • Nicholls B, Racey PA (2006b) Habitat selection as a mechanism of resource partitioning in two cryptic bat species Pipistrellus pipistrellus and Pipistrellus pygmaeus. Ecography 29(5):697–708

    Article  Google Scholar 

  • Norberg UM, Rayner JM (1987) Ecological morphology and flight in bats (Mammalia: Chiroptera): wing adaptations, flight performance, foraging strategy and echolocation. Philos Trans R Soc B 316(1179):335–427

    Article  Google Scholar 

  • Numa C, Verdú JR, Sánchez-Palomino P (2005) Phyllostomid bat diversity in a variegated coffee landscape. Biol Conserv 122(1):151–158

    Article  Google Scholar 

  • Pearce JL, Boyce MS (2006) Modelling distribution and abundance with presence-only data. J Appl Ecol 43:405–412

    Article  Google Scholar 

  • Phillips SJ, Dudík M, Elith J, Graham CH, Lehmann A, Leathwick JR, Ferrier S (2009) Sample selection bias, presence-only distribution models: implications for background, pseudo-absence data. Ecol Appl 19:181–197

    Article  PubMed  Google Scholar 

  • Razgour O, Hanmer J, Jones G (2011) Using multi-scale modeling to predict habitat suitability for species of conservation concern: the grey log-eared bat. Biol Conserv 144:2922–2930

    Article  Google Scholar 

  • 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 

  • Rettie WJ, Messier F (2000) Hierarchical habitat selection by woodland caribou: its relationship to limiting factors. Ecography 23:466–478

    Article  Google Scholar 

  • Riitters KH, Wickham JD, O’Neill R, Jones KB, Smith ER, Coulston JW, Wade TG and Smith JH (2002) Fragmentation of continental United States forests. Ecosystems 5:815–822

  • Rodrigues L, Bach L, Duborg-Savage MJ, Goodwin J and Harbusch C (2008) Guidelines for consideration of bats in wind farm projects. EUROBATS Publication Series No. 3 (English version). UNEP/EUROBATS Secretariat, Bonn

  • Roscioni F, Russo D, Di Febbraro M, Frate L, Carranza ML, Loy A (2013) Regional-scale modelling of the cumulative impact of wind farms on bats. Biodivers Conserv 22:1821–1835

    Article  Google Scholar 

  • Roscioni F, Rebelo H, Russo D, Carranza ML, Di Febbraro M, Loy A (2014) A modelling approach to infer the effects of wind farms on landscape connectivity for bats. Landscape Ecol 29(5):891–903

  • Russ J (1999) The Bats of Britain, Ireland. Echolocation calls, sound analysis, species identification. Alana Books, Alana Ecology LTD, Quezon

    Google Scholar 

  • Russ JM, Briffa M, Montgomery WI (2003) Seasonal patterns in activity and habitat use by bats (Pipistrellus spp. and Nyctalus leisleri) in Northern Ireland, determined using a driven transect. J Zool 259:289–299

    Article  Google Scholar 

  • Russo D (2007) Effects of land abandonment on animal species in Europe: conservation and management implications. Integrated Assessment of vulnerable ecosystems under global change in the European Union. European commission, directorate–general for research environment. Luxembourg: Office for Official Publications of the European Communities, p 53

  • Russo D, Jones G (2000) The two cryptic species of Pipistrellus pipistrellus (Chiroptera: Vespertilionidae) occur in Italy: evidence from echolocation, social calls. Mammalia 64:187–197

    Article  Google Scholar 

  • Russo D, Jones G (2002) Identification of twenty-two bat species (Mammalia: Chiroptera) from Italy by analysis of time-expanded recordings of echolocation calls. J Zool Lond 258:91–103

    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 MC, Cushman SA, Saura S (2013) Scale dependence in habitat selection: the case of the endangered brown bear (Ursus arctos) in the Cantabrian Range (NW Spain). Int J Geogr Inf Sci 28(8):1–16

    Google Scholar 

  • Schaefer JA, Messier F (1995) Habitat selection as a hierarchy: the spatial scales of winter foraging by muskoxen. Ecography 18:333–344

    Article  Google Scholar 

  • Shirk AJ (2012) Scale dependency of American marten (Martes americana) habitat relationships. Biology and conservation of martens, sables, and fishers: a new synthesis. Cornell University Press, Ithaca

    Google Scholar 

  • Suárez-Seoane S, Baudry J (2002) Scale dependence of spatial patterns and cartography on the detection of landscape change: relationships with species’ perception. Ecography 25(4):499–511

    Article  Google Scholar 

  • Swets JA (1988) Measuring the accuracy of diagnostic systems. Science 240:1285–1293

    Article  CAS  PubMed  Google Scholar 

  • Thompson CM, McGarigal K (2002) The influence of research scale on bald eagle habitat selection along the lower Hudson River, New York (USA). Landscape Ecol 17:569–586

    Article  Google Scholar 

  • Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD—a platform for ensemble forecasting of species distributions. Ecography 32(3):369–373

    Article  Google Scholar 

  • Veloz SD (2009) Spatially autocorrelated sampling falsely inflates measures of accuracy for presence-only niche models. J Biogeogr 36:2290–2299

    Article  Google Scholar 

  • Vicente JR, Fernandes RF, Randin CF, Broennimann O, Gonçalves J, Marcos B, Pôças I, Alves P, Guisan A, Honrado JP (2013) Will climate change drive alien invasive plants into areas of high protection value? An improved model-based regional assessment to prioritise the management of invasions. J Environ Manag 131:185–195

    Article  CAS  Google Scholar 

  • Villard MA, Trzcinski MK, Merriam G (1999) Fragmentation effects on forest birds: relative influence of woodland cover and configuration on landscape occupancy. Conserv Biol 13(4):774–783

    Article  Google Scholar 

  • Voigt CC, Popa-Lisseanu AG, Niermann I, Kramer-Schadt S (2012) The catchment area of wind farms for European bats: a plea for international regulations. Biol Conserv 153:80–86

    Article  Google Scholar 

  • Wasserman TN, Cushman SA, Do W, Hayden J (2012) Multi scale habitat relationships of Martes americana in northern Idaho, USA. Research Paper RMRS-RP-94. Fort Collins, CO: U.S. Department of Agriculture, Forest Service, Rocky Mountain Research Station, p 21

  • Waters DA, Jones G, Furlong M (1999) Foraging ecology of Leisler’s bat Nyctalus leisleri at two sites in southern Britain. J Zool Lond 249:173–180

    Article  Google Scholar 

  • Wickham JD, Riitters KH, Wade TG, Homer C (2008) Temporal change in fragmentation of continental US forests. Landscape Ecol 23(8):891–898

    Google Scholar 

  • Wiens JA (1989) Spatial scaling in ecology. Funct Ecol 3:385–397

    Article  Google Scholar 

  • Wiens JA (1990) On the use of `grain’ and `grain size’ in ecology. Funct Ecol 3:385–397

    Article  Google Scholar 

Download references

Acknowledgments

We thank NEMO s.r.l. for providing the CLC map. We also acknowledge Filippo Frizzi for his support in providing the topographic maps. Thanks also go to Stefano Vanni for his support in georeferencing the presence data.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Danilo Russo.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ducci, L., Agnelli, P., Di Febbraro, M. et al. Different bat guilds perceive their habitat in different ways: a multiscale landscape approach for variable selection in species distribution modelling. Landscape Ecol 30, 2147–2159 (2015). https://doi.org/10.1007/s10980-015-0237-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-015-0237-x

Keywords

Navigation