Skip to main content

Combined effects of area, connectivity, history and structural heterogeneity of woodlands on the species richness of hoverflies (Diptera: Syrphidae)

Abstract

Context

Hoverflies are often used as bio-indicators for ecosystem conservation, but only few studies have actually investigated the key factors explaining their richness in woodlands.

Objectives

In a fragmented landscape in southwest France, we investigated the joint effects of woodland area, structural heterogeneity, connectivity and history on the species richness of forest-specialist hoverflies, and whether there was a time lag in the response of hoverflies to habitat changes, and tested the effect of spatiotemporal changes.

Methods

Current species richness was sampled in 48 woodlands using 99 Malaise traps. Structural variables were derived from a rapid habitat assessment protocol. Old maps and aerial photographs were used to extract past and present spatial patterns of the woodlands since 1850. Relationships between species richness and explanatory variables were explored using generalized linear models.

Results

We show that current habitat area, connectivity, historical continuity and the average density of tree-microhabitats explained 35 % of variation in species richness. Species richness was affected differently by changes in patch area between 1979 and 2010, depending on woodland connectivity. In isolated woodlands, extinction debt and colonization credit were revealed, showing that even several decades are not sufficient for hoverflies to adapt to landscape-scale habitat conditions.

Conclusions

These findings emphasise the importance of maintaining connectedness between woodlands, which facilitates the dispersion in a changing landscape. Our results also highlight the benefits of using a change-oriented approach to explain the current distribution patterns of species, especially when several spatial processes act jointly.

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

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

References

  • Andren H (1994) Effects of habitat fragmentation on birds and mammals in landscapes with different proportions of suitable habitat: a review. Oikos 71:355–366

    Article  Google Scholar 

  • Andrieu E, De Warnaffe GDB, Ladet S, Heintz W, Sourdril A, Deconchat M (2008) Cartographier l’historique des coupes forestières dans les petits bois. Rev For Fr 60:667–676

    Google Scholar 

  • Baily B, Riley M, Aucott P, Southall H (2011) Extracting digital data from the First Land Utilisation Survey of Great Britain-Methods, issues and potential. Appl Geogr 31:959–968

    Article  Google Scholar 

  • Bommarco R, Lindborg R, Marini L, Öckinger E (2014) Extinction debt for plants and flower-visiting insects in landscapes with contrasting land use history. Divers Distrib 20:591–599

    Article  Google Scholar 

  • Bouget C, Larrieu L, Nusillard B, Parmain G (2013) In search of the best local habitat drivers for saproxylic beetle diversity in temperate deciduous forests. Biodivers Conserv 22:2111–2130

    Article  Google Scholar 

  • Bouget C, Larrieu L, Brin A (2014a) Key features for saproxylic beetle diversity derived from rapid habitat assessment in temperate forests. Ecol Ind 36:656–664

    Article  Google Scholar 

  • Bouget C, Parmain G, Gilg O, Noblecourt T, Nusillard B, Paillet Y, Pernot C, Larrieu L, Gosselin F (2014b) Does a set aside conservation strategy help restore old-growth attributes and conserve saproxylic beetles in temperate forests? Anim Conserv 17:342–353

    Article  Google Scholar 

  • Brooks TM, Pimm SL, Oyugi JO (1999) Time lag between deforestation and bird extinction in tropical forest fragments. Conserv Biol 13:1140–1150

    Article  Google Scholar 

  • Brotons L, Mönkkönen M, Martin JL (2003) Are fragments islands? landscape context and density-area relationships in boreal forest birds. Am Nat 162:343–357

    Article  PubMed  Google Scholar 

  • Burnham KP, Anderson DR (2004) Model selection and inference: a practical information-theoretic approach. Soc Methods Res 33:261–304

    Article  Google Scholar 

  • Cateau E, Larrieu L, Vallauri D, Savoie JM, Touroult J, Brustel H (2015) Ancienneté et maturité: deux qualités complémentaires d’un écosystème forestier. C R Biol 338:58–73

    Article  PubMed  Google Scholar 

  • Connor EF, McCoy ED (1979) The statistics and biology of the species-area relationship. Am Nat 113:791–833

    Article  Google Scholar 

  • Cousins SA (2009) Extinction debt in fragmented grasslands: paid or not? J Veg Sci 20:3–7

    Article  Google Scholar 

  • Cousins SA, Vanhoenacker D (2011) Detection of extinction debt depends on scale and specialisation. Biol Conserv 144:782–787

    Article  Google Scholar 

  • Cristofoli S, Mahy G (2010) Colonisation credit in recent wet heathland butterfly communities. Insect Cons Div 3:83–91

    Article  Google Scholar 

  • Cristofoli S, Piqueray J, Dufrêne M, Bizoux JP, Mahy G (2010) Colonization credit in restored wet heathlands. Restor Ecol 18:645–655

    Article  Google Scholar 

  • De Warnaffe GDB, Deconchat M, Ladet S, Balent G (2006) Variability of cutting regimes in small private woodlots of south-western France. Ann For Sci 63:915–927

    Article  Google Scholar 

  • Development Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Garcia Marquéz JR, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, 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 36:027–046

    Article  Google Scholar 

  • Ewers RM, Didham RK, Pearse WD, Lefebvre V, Rosa I, Carreiras J, Lucas RM, Reuman DC (2013) Using landscape history to predict biodiversity patterns in fragmented landscapes. Ecol Lett 16:1221–1233

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Favre C, Granier E, Cosserat-Mangeot R, Bachacou J, Dupouey JL (2012) La digitalisation des cartes anciennes. Manuel pour la vectorisation de l’usage des sols et le géoréférencement de la Carte d’Etat-Major-INRA

  • Fayt P, Dufrêne M, Branquart E, Hastir P, Pontégnie C, Hénin JM, Versteirt V (2006) Contrasting responses of saproxylic insects to focal habitat resources: the example of longhorn beetles and hoverflies in Belgian deciduous forests. J Insect Conserv 10:129–150

    Article  Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK, Helkowski JH, Holloway T, Howard EA, Kucharik CJ, Monfreda C, Patz JA, Prentice IC, Ramankutty N, Snyder PK (2005) Global consequences of land use. Science 309:570–574

    CAS  Article  PubMed  Google Scholar 

  • Ford HA, Walters JR, Cooper CB, Debus S, Doerr V (2009) Extinction debt or habitat change? Ongoing losses of woodland birds in north-eastern New South Wales, Australia. Biol Conserv 142:3182–3190

    Article  Google Scholar 

  • Good JA, Speight MCD (1996) Saproxylic invertebrates and their conservation throughout Europe. Council of Europe, Strasbourg

    Google Scholar 

  • Gosselin M, Laroussinie O (2004) Biodiversité et gestion forestière: connaître pour préserver, synthèse bibliographique. Cemagref

  • Gotelli NJ, Colwell RK (2001) Quantifying biodiversity: procedures and pitfalls in the measurement and comparison of species richness. Ecol Lett 4:379–391

    Article  Google Scholar 

  • Groot M, Bevk D (2012) Ecosystem services and phenology of hoverflies (Diptera: Syrphidae) in a slovenian forest stand. Les (Ljubljana) 64:123–128

    Google Scholar 

  • Guardiola M, Pino J, Rodà F (2013) Patch history and spatial scale modulate local plant extinction and extinction debt in habitat patches. Divers Distrib 19:825–833

    Article  Google Scholar 

  • Guisan A, Zimmermann NE (2000) Predictive habitat distribution models in ecology. Ecol Model 135:147–186

    Article  Google Scholar 

  • Hanski I (2005) Landscape fragmentation, biodiversity loss and the societal response. EMBO Rep 6:388–392

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  • Hanski I, Ovaskainen O (2002) Extinction debt at extinction threshold. Conserv Biol 16:666–673

    Article  Google Scholar 

  • Hanski I, Thomas CD (1994) Metapopulation dynamics and conservation: a spatially explicit model applied to butterflies. Biol Conserv 68:167–180

    Article  Google Scholar 

  • Helm A, Hanski I, Pärtel M (2006) Slow response of plant species richness to habitat loss and fragmentation. Ecol Lett 9:72–77

    PubMed  Google Scholar 

  • Herrault P-A, Sheeren D, Fauvel M, Paegelow M (2013) Automatic extraction of forests from historical maps based on unsupervised classification in the CIELab color space. In: Geographic information science at the heart of Europe Springer, pp 95–112

  • Huston MA (1994) Biological diversity: the coexistence of species. Cambridge University Press, Cambridge  

    Google Scholar 

  • IGN (2011) Scan Etat-major® 40 K—descriptif de contenu, version 1. IGN, Saint-Mandé

    Google Scholar 

  • Inventaire Forestier National (IFN) (2000) Les arbres hors-forêt en France. FAO, Rome

    Google Scholar 

  • Keil P, Konvicka M (2005) Local species richness of Central European hoverflies (Diptera: Syrphidae): a lesson taught by local faunal lists. Divers Distrib 11:417–426

    Article  Google Scholar 

  • Krauss J, Bommarco R, Guardiola M, Heikkinen RK, Helm A, Kuussari M, Lindborg R, Öckinger E, Pärtel M, Pino J, Pöyry J, Raatikainen KM, Sang A, Stefanescu C, Teder T, Zober M, Steffan-Dewenter I (2010) Habitat fragmentation causes immediate and time-delayed biodiversity loss at different trophic levels. Ecol Lett 13:597–605

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuussaari M, Bommarco R, Heikkinen RK, Helm A, Krauss J, Lindborg R, Öckinger E, Pärtel, Pino J, Roda F, Stefanecu C, Teder T, Zobel M, Steffan-Dewenter I (2009) Extinction debt: a challenge for biodiversity conservation. Trends Ecol Evol 24:564–571

    Article  PubMed  Google Scholar 

  • Larrieu L, Gonin P (2008) L’Indice de Biodiversité Potentielle (IBP): une méthode simple et rapide pour évaluer la biodiversité potentielle des peuplements forestiers. Rev For Fr 60:727–748

    Google Scholar 

  • Larsson TB (2001) Biodiversity evaluation tools for European forests. Criteria and indicators for sustainable management unit level 75

  • Leyk S, Boesch R, Weibel R (2006) Saliency and semantic processing: Extracting forest cover from historical topographic maps. Pattern Recogn 39:953–968

    Article  Google Scholar 

  • Lin D (2009) VIF package (R package) http://cran.r-project.org/web/packages/VIF/index.html

  • Lindborg R, Eriksson O (2004) Historical landscape connectivity affects present plant species diversity. Ecology 85:1840–1845

    Article  Google Scholar 

  • MacArthur RH (1967) The theory of island biogeography. Princeton University Press, Princeton

    Google Scholar 

  • Magle SB, Theobald DM, Crooks KR (2009) A comparison of metrics predicting landscape connectivity for a highly interactive species along an urban gradient in Colorado, USA. Landscape Ecol 24:267–280

    Article  Google Scholar 

  • Metzger JP, Martensen AC, Dixo M, Bernacci LC, Ribeiro MC, Godoy Teixeira AM, Pardini R (2009) Time-lag in biological responses to landscape changes in a highly dynamic Atlantic forest region. Biol Conserv 142:1166–1177

    Article  Google Scholar 

  • Meyer B, Jauker F, Steffan-Dewenter I (2009) Contrasting resource-dependent responses of hoverfly richness and density to landscape structure. Basic Appl Ecol 10:178–186

    Article  Google Scholar 

  • Münzbergová Z, Mildén M, Ehrlén J, Herben T (2005) Population viability and reintroduction strategies: a spatially explicit landscape-level approach. Ecol Appl 15:1377–1386

    Article  Google Scholar 

  • Nadal F (2011) La cartographie militaire des Pyrénées françaises et la guerre civile espagnole. Sud-Ouest Européen 31:169–182

    Article  Google Scholar 

  • Nagelkerke CJ, Verboom J, van den Bosc F, van de wolfshaar KE (2002) Time lags in metapopulation responses to landscape change. In: Gutzwiller KJ (ed) Applying landscape ecology in biological conservation. Springer, New York, pp 330–354

    Chapter  Google Scholar 

  • Oksanen J, Kindt R, Legendre P, Solymos P (2007) The vegan package. Community Ecol. R Package 2.2-0. http://vegan.r-forge.r-project.org/

  • Ouin A, Sarthou J-P, Bouyjou B, Deconchat M, Lacombe JP, Monteil C (2006) The species-area relationship in the hoverfly (Diptera, Syrphidae) communities of forest fragments in southern France. Ecography 29:183–190

    Article  Google Scholar 

  • Piqueray J, Cristofoli S, Bisteau E, Palm R, Mahy G (2011) Testing coexistence of extinction debt and colonization credit in fragmented calcareous grasslands with complex historical dynamics. Landscape Ecol 26:823–836

    Article  Google Scholar 

  • Ricklefs RE (1987) Community diversity: relative roles of local and regional processes. Science 235:167–171

    CAS  Article  PubMed  Google Scholar 

  • Root RB (1973) Organization of a plant-arthropod association in simple and diverse habitats: the fauna of collards (Brassica oleracea). Ecol Monogr 43:95–124

  • Rösch V, Tscharntke T, Scherber C, Batary P (2013) Landscape composition, connectivity and fragment size drive effects of grassland fragmentation on insect communities. J Appl Ecol 50:387–394

    Article  Google Scholar 

  • Sarthou V, Sarthou J-P (2007) Evaluation écologique d’écosystèmes forestiers de Réserves Naturelles de Haute Savoie à l’aide des Diptères Syrphidés. Zone Natura 2000 Arve-Giffre, Réserve Naturelle des Contamines-Montjoie, Réserve Naturelle des Aiguilles Rouges. Rapport d’études pour ASTERS, février 2007

  • Sarthou J-P, Speight M (2005) Les Diptères Syrphidés, peuple de tous les espaces. Insectes 137:3–8

    Google Scholar 

  • Smith GF, Gittings T, Wilson M, French L, Oxbrough A, O' Donoghue S, O' Halloran J, Kelly DL, Mitchell F, Kelly T, Iremonger S, Mc Kee AM, Giller P (2008) Identifying practical indicators of biodiversity for stand-level management of plantation forests. Biodivers Conserv 17:991–1015

    Article  Google Scholar 

  • Sommaggio D (1999) Syrphidae: can they be used as environmental bioindicators? Agric Ecosyst Environ 74:343–356

    Article  Google Scholar 

  • Speight MCD (1989) Saproxylic invertrebrates and their conservation. 42, 1–79. Concil of Europe. Nature and Environment Series

  • Speight MCD, Good JA (2003) Development of eco-friendly forestry practices in Europe and the maintenance of saproxylic biodiversity. In: Proceedings of international symposium “Dead Wood Key Biodiversity” Mantova, pp 73–77

  • Speight MCD, Castella E, Obrdlik P (2000) Use of the Syrph the Net database 2000. Syrph Net Database Eur Syrphidae 25:99

    Google Scholar 

  • Speight MCD, Castella E, Sarthou JP (2013) Species accounts of European Syrphidae (Diptera) 2010. Syrph Net Database Eur Syrphidae 72:316

    Google Scholar 

  • Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  • Tischendorf L, Bender DJ, Fahrig L (2003) Evaluation of wood isolation metrics in mosaic landscapes for specialist vs. generalist dispersers. Landscape Ecol 18:41–50

    Article  Google Scholar 

Download references

Acknowledgments

We are very grateful to the handling editor O. Schweiger and to two anonymous reviewers for their constructive comments on the previous version of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to P.-A. Herrault.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 29 kb)

Supplementary material 2 (DOCX 120 kb)

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Herrault, PA., Larrieu, L., Cordier, S. et al. Combined effects of area, connectivity, history and structural heterogeneity of woodlands on the species richness of hoverflies (Diptera: Syrphidae). Landscape Ecol 31, 877–893 (2016). https://doi.org/10.1007/s10980-015-0304-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-015-0304-3

Keywords

  • Hoverflies
  • Woodlands
  • Heterogeneity
  • Connectivity
  • History
  • Extinction debt
  • Colonization credit