Separating the effects of habitat amount and fragmentation on invertebrate abundance using a multi-scale framework

Abstract

Context

Herbicide treatments in viticulture can generate highly contrasting mosaics of vegetated and bare vineyards, of which vegetated fields often provide better conditions for biodiversity. In southern Switzerland, where herbicides are applied at large scales, vegetated vineyards are limited in extent and isolated from one another, potentially limiting the distribution and dispersal ability of organisms.

Objectives

We tested the separate and interactive effects of habitat amount and fragmentation on invertebrate abundance using a multi-scale framework, along with additional environmental factors. We identified which variables at which scales were most important in predicting patterns of invertebrate abundance.

Methods

We used a factorial design to sample across a gradient of habitat amount (area of vegetated vineyards, measured as percentage of landscape PLAND) and fragmentation (number of vegetated patches, measured as patch density PD). Using 10 different spatial scales, we identified the factors and scales that most strongly predicted invertebrate abundance and tested potential interactions between habitat amount and fragmentation.

Results

Habitat amount (PLAND index) was most important in predicting invertebrate numbers at a field scale (50 m radius). In contrast, we found a negative effect of fragmentation (PD) at a broad scale of 450 m radius, but no interactive effect between the two.

Conclusions

The spatial scales at which habitat amount and fragmentation affect invertebrates differ, underpinning the importance of spatially explicit study designs in disentangling the effects between habitat amount and configuration. We showed that the amount of vegetated vineyards has more influence on invertebrate abundance, but that fragmentation also contributed substantially. This suggests that efforts for augmenting the area of vegetated vineyards is more beneficial for invertebrate numbers than attempts to connect them.

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References

  1. Arlettaz R, Maurer ML, Mosimann-Kampe P, Nusslé S, Abadi F, Braunisch V, Schaub M (2012) New vineyard cultivation practices create patchy ground vegetation, favouring woodlarks. J Ornithol 153:229–238

    Article  Google Scholar 

  2. Bartón K (2016) Mumin: Multi-model inference. R package version 1.10.6. https://cran.R-project.Org/package=mumin

  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48

    Article  Google Scholar 

  4. Bivand R, Piras G (2015) Comparing implementations of estimation methods for spatial econometrics. J Stat Softw 63:1–36

    Google Scholar 

  5. Bolker BM, Brooks ME, Clark CJ, Geange SW, Poulsen JR, Stevens MHH, White JSS (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–135

    Article  PubMed  Google Scholar 

  6. Bowman J, Jaeger JAG, Fahrig L (2002) Dispersal distance of mammals is proportional to home range size. Ecology 83:2049–2055

    Article  Google Scholar 

  7. Braaker S, Ghazoul J, Obrist M, Moretti M (2014) Habitat connectivity shapes urban arthropod communities: the key role of green roofs. Ecology 95:1010–1021

    Article  CAS  PubMed  Google Scholar 

  8. Burnham KP, Anderson DR (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York

    Google Scholar 

  9. Chambers CL, Cushman SA, Medina-Fitoria A, Martínez-Fonseca J, Chávez-Velásquez M (2016) Influences of scale on bat habitat relationships in a forested landscape in Nicaragua. Landscape Ecol 31:299–1318

    Article  Google Scholar 

  10. Coxwell CC, Bock CE (1995) Spatial variation in diurnal surface temperatures and the distribution and abundance of an alpine grasshopper. Oecologia 104:433–439

    Article  CAS  PubMed  Google Scholar 

  11. Cushman SA, Gutzweiler K, Evans JS, McGarigal K (2010) The gradient paradigm: a conceptual and analytical framework for landscape ecology. Spatial complexity, informatics, and wildlife conservation. Springer, New York, pp 83–108

    Google Scholar 

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

    Article  Google Scholar 

  13. Cushman SA, Shirk AJ, Landguth EL (2013) Landscape genetics and limiting factors. Conserv Genet 14:263–274

    Article  Google Scholar 

  14. Debinski DM, Holt RD (2000) A survey and overview of habitat fragmentation experiments. Conserv Biol 14:342–355

    Article  Google Scholar 

  15. Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Diekötter T, García Márquez J, Gruber B, Lafourcade B, Leitão P, Münkemüller T, McClean C, Osborne P, Reineking B, Schröder B, Skidmore A, Zurell D, Lautenbach S (2012) Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46

    Article  Google Scholar 

  16. Eigenbrod F, Hecnar SJ, Fahrig L (2008) Accessible habitat: an improved measure of the effects of habitat loss and roads on wildlife populations. Landscape Ecol 23:159–168

    Article  Google Scholar 

  17. ESRI (2015) Arcgis 10.3.1 for desktop. In: Institute E. S. R. (ed). Redlands, California

  18. Evans JS, Oakleaf J, Cushman SA, Theobald D (2014) An arcgis toolbox for surface gradient and geomorphometric modeling, version 2.0–0

  19. Ewers RM, Didham RK (2008) Pervasive impact of large-scale edge effects on a beetle community. Proc Natl Acad Sci USA 105:5426–5429

    Article  PubMed  Google Scholar 

  20. Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Ann Rev Ecol Evol Syst 34:487–515

    Article  Google Scholar 

  21. Fahrig L (2013) Rethinking patch size and isolation effects: the habitat amount hypothesis. J Biogeogr 40:1649–1663

    Article  Google Scholar 

  22. Fahrig L, Rytwinski T (2009) Effects of roads on animal abundance: An empirical review and synthesis. Ecol and Soc 14: 21. http://www.ecologyandsociety.org/vol14/iss1/art21/

  23. Flather CH, Bevers M (2002) Patchy reaction-diffusion and population abundance: the relative importance of habitat amount and arrangement. Am Nat 159:40–56

    Article  PubMed  Google Scholar 

  24. Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockstrom J, Sheehan J, Siebert S, Tilman D, Zaks DPM (2011) Solutions for a cultivated planet. Nature 478:337–342

    Article  CAS  PubMed  Google Scholar 

  25. Gelman A, Su Y-S (2015) Arm: data analysis using regression and multilevel/hierarchical models. http://CRAN.R-project.org/package=arm

  26. Grand J, Buonaccorsi J, Cushman SA, Griffin CR, Neel MC (2004) A multiscale landscape approach to predicting bird and moth rarity hotspots in a threatened pitch pine–scrub oak community. Conserv Biol 18:1063–1077

    Article  Google Scholar 

  27. Haddad NM, Gonzalez A, Brudvig LA, Burt MA, Levey DJ, Damschen EI (2017) Experimental evidence does not support the habitat amount hypothesis. Ecography 40:48–55

    Article  Google Scholar 

  28. Hanski I (2015) Habitat fragmentation and species richness. J Biogeogr 42:989–993

    Article  Google Scholar 

  29. Holland J, Fahrig L (2000) Effect of woody borders on insect density and diversity in crop fields: a landscape-scale analysis. Agric Ecosyst Environ 78:115–122

    Article  Google Scholar 

  30. Holland JD, Fahrig L, Cappuccino N (2005) Body size affects the spatial scale of habitat–beetle interactions. Oikos 110:101–108

    Article  Google Scholar 

  31. Jaeger JA (2000) Landscape division, splitting index, and effective mesh size: new measures of landscape fragmentation. Landscape Ecol 15:115–130

    Article  Google Scholar 

  32. Korner-Nievergelt F (2015) Bayesian data analysis in ecology using linear models with R, Bugs, and Stan. Academic Press, Amsterdam

    Google Scholar 

  33. Krebs JR, Wilson JD, Bradbury RB, Siriwardena GM (1999) The second silent spring? Nature 400:611–612

    Article  CAS  Google Scholar 

  34. Laforge MP, Vander Wal E, Brook RK, Bayne EM, McLoughlin PD (2015) Process-focussed, multi-grain resource selection functions. Ecol Modell 305:10–21

    Article  Google Scholar 

  35. Lawton JH (1995) Extinction risks. In: Lawton JH, May RM (eds) Population dynamics principles. Oxford University Press, Oxford, pp 147–163

    Google Scholar 

  36. Legendre P, Legendre L (1998) Numerical ecology. Elsevier, Amsterdam

    Google Scholar 

  37. Levin SA (1992) The problem of pattern and scale in ecology. Ecology 73:1943–1967

    Article  Google Scholar 

  38. Martin AE, Fahrig L (2012) Measuring and selecting scales of effect for landscape predictors in species-habitat models. Ecol Appl 22:2277–2292

    Article  PubMed  Google Scholar 

  39. McGarigal K, Cushman SA (2002) Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecol Appl 12:335–345

    Article  Google Scholar 

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

  41. McGarigal K, Wan HY, Zeller KA, Timm BC, Cushman SA (2016) Multi-scale habitat selection modeling: a review and outlook. Landsc Ecol 31:1161–1175

    Article  Google Scholar 

  42. Melo GL, Sponchiado J, Caceres NC, Fahrig L (2017) Testing the habitat amount hypothesis for south American small mammals. Biol Conserv 209:304–314

    Article  Google Scholar 

  43. Mendenhall CD, Karp DS, Meyer CFJ, Hadly EA, Daily GC (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509:213–217

    Article  CAS  PubMed  Google Scholar 

  44. Miguet P, Jackson HB, Jackson ND, Martin AE, Fahrig L (2016) What determines the spatial extent of landscape effects on species? Landscape Ecol 31:1177–1194

    Article  Google Scholar 

  45. Mortelliti A, Amori G, Capizzi D, Cervone C, Fagiani S, Pollini B, Boitani L (2011) Independent effects of habitat loss, habitat fragmentation and structural connectivity on the distribution of two arboreal rodents. J Appl Ecol 48:153–162

    Article  Google Scholar 

  46. Neel MC, McGarigal K, Cushman SA (2004) Behavior of class-level landscape metrics across gradients of class aggregation and area. Landscape Ecol 19:435–455

    Article  Google Scholar 

  47. Pedro ARS, Simonetti JA (2015) The relative influence of forest loss and fragmentation on insectivorous bats: does the type of matrix matter? Landscape Ecol 30:1561–1572

    Article  Google Scholar 

  48. R Development Core Team (2018) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/

  49. Radford JQ, Bennett AF (2007) The relative importance of landscape properties for woodland birds in agricultural environments. J Appl Ecol 44:737–747

    Article  Google Scholar 

  50. Rybicki J, Hanski I (2013) Species-area relationships and extinctions caused by habitat loss and fragmentation. Ecol Lett 16(Suppl 1):27–38

    Article  PubMed  Google Scholar 

  51. Schüepp C, Herzog F, Entling MH (2014) Disentangling multiple drivers of pollination in a landscape-scale experiment. Proc R Soc B 281:20132667. https://doi.org/10.1098/rspb.2013.2667

    Article  PubMed  Google Scholar 

  52. Seibold S, Bässler C, Brandl R, Fahrig L, Förster B, Heurich M, Hothorn T, Scheipl F, Thorn S, Müller J (2017) An experimental test of the habitat-amount hypothesis for saproxylic beetles in a forested region. Ecology 98:1613–1622

    Article  PubMed  Google Scholar 

  53. Trzcinski MK, Fahrig L, Merriam G (1999) Independent effects of forest cover and fragmentation on the distribution of forest breeding birds. Ecol Appl 9:586–593

    Article  Google Scholar 

  54. Wan HY, McGarigal K, Ganey JL, Lauret V, Timm BC, Cushman SA (2017) Meta-replication reveals non-stationarity in multi-scale habitat selection of Mexican spotted owl. Condor 119:641–658

    Article  Google Scholar 

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

    Article  Google Scholar 

  56. Winter S, Bauer T, Strauss P et al (2018) Effects of vegetation management intensity on biodiversity and ecosystem services in vineyards: a meta-analysis. J Appl Ecol 55:2484–2495

    Article  PubMed  PubMed Central  Google Scholar 

  57. Wu J, David JL (2002) A spatially explicit hierarchical approach to modeling complex ecological systems: theory and applications. Ecol Model 153:7–26

    Article  Google Scholar 

  58. Zeller KA, McGarigal K, Beier P, Cushman SA, Vickers TW, Boyce WM (2014) Sensitivity of landscape resistance estimates based on point selection functions to scale and behavioral state: Pumas as a case study. Landscape Ecol 29:541–557

    Article  Google Scholar 

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Acknowledgements

We thank all farmers and the VITIVAL (Valais association for viticulture) groups for their collaboration and allowing us to do this study on their vineyards. We are grateful to Valentin Moser for field and lab assistance and Luca Chiaverini for help with GIS analyses. We further thank both reviewers for their valuable comments and inputs which improved the quality of this paper substantially. This study was supported by the Swiss National Science Foundation, grant 31003A_149780 to Alain Jacot.

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Correspondence to Laura Bosco.

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Bosco, L., Wan, H.Y., Cushman, S.A. et al. Separating the effects of habitat amount and fragmentation on invertebrate abundance using a multi-scale framework. Landscape Ecol 34, 105–117 (2019). https://doi.org/10.1007/s10980-018-0748-3

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Keywords

  • Agriculture
  • Conservation
  • Habitat amount hypothesis
  • Patch density
  • Vineyard