Skip to main content

Advertisement

Log in

Correlations and variance among species traits explain contrasting impacts of fragmentation and habitat loss on functional diversity

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

Abstract

Context

Understanding how landscape fragmentation affects functional diversity, defined as the distribution of functional traits in an assemblage, is critical for managing landscapes for biodiversity and ecosystem functions. Despite some scattered evidence, we lack a clear understanding of how patterns of fragmentation drive changes in functional diversity, and its relationship with species richness as habitat is lost from a landscape.

Objectives

To develop testable predictions about how landscape fragmentation, relative to the effects of habitat loss, impacts functional diversity and its relationship with species richness.

Methods

We used a spatially explicit metacommunity model that evaluates communities that vary in the distribution of response traits (traits involved in species responses to environmental change) and the correlation between response and effect traits (traits associated with species’ effects on ecosystem functioning).

Results

Compared to effects of habitat loss, relative effects of fragmentation on functional diversity increased as the variance in the distribution of response traits was high and the correlation among traits was high. Functional richness decreased faster than species richness in highly fragmented landscapes as habitat was lost. However, functional diversity remained unchanged or even increased in fragmented landscapes when either response and effect traits were not correlated (or weakly correlated), or when the proportion of generalist species with high dispersal capacities was high.

Conclusions

Compared to effects of habitat loss, the relative effects of fragmentation on functional diversity and species richness are more dependent on the type of community evaluated. A careful evaluation of the variance in the distribution of response traits within a community, as well as the correlation among response and effect traits, can help to determine when it is important to manage landscape fragmentation to protect functional diversity.

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
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Aguilar R, Cristóbal-Pérez EJ, Balvino-Olvera FJ, de Jesús Aguilar-Aguilar M, Aguirre-Acosta N, Ashworth L, Lobo JA, Martén-Rodríguez S, Fuchs EJ, Sanchez-Montoya G, Bernardello G, Quesada M (2019) Habitat fragmentation reduces plant progeny quality: a global synthesis. Ecol Lett 22:1163–1173. https://doi.org/10.1111/ele.13272

    Article  PubMed  Google Scholar 

  • Barbaro L, Giffard B, Charbonnier Y, van Halder I, Brockerhoff EG (2014) Bird functional diversity enhances insectivory at forest edges: a transcontinental experiment. Divers Distrib 20:149–159

    Google Scholar 

  • Bartomeus I, Cariveau DP, Harrison T, Winfree R (2018) On the inconsistency of pollinator species traits for predicting either response to land-use change or functional contribution. Oikos 127:306–315 https://doi.org/10.1111/oik.04507

    Article  Google Scholar 

  • Bartlett LJ, Newbold T, Purves DW, Tittensor DP, Harfoot MBJ (2016). Synergistic impacts of habitat loss and fragmentation on model ecosystems Proc R Soc B. https://doi.org/10.1098/rspb.2016.1027

    Article  PubMed  Google Scholar 

  • Batáry P, Kurucz K, Suarez-Rubio M, Chamberlain DE (2017) Non-linearities in bird responses across urbanization gradients: a meta-analysis. Global Change Biol. https://doi.org/10.1111/gcb.13964

    Article  Google Scholar 

  • Benchimol M, Peres CA (2015) Edge-mediated compositional and functional decay of tree assemblages in Amazonian forest islands after 26 years of isolation. J Ecol 103:408–420

    Google Scholar 

  • Biswas SR, Mallik AU, Braithwaite NT, Wagner HH (2016) A conceptual framework for the spatial analysis of functional trait diversity. Oikos 125:192–200

    Google Scholar 

  • Bovo AAA, Ferraz KMPMB, Magioli M, Alexandrino ER, Hasui É, Ribeiro MC, Tobias JA (2018) Habitat fragmentation narrows the distribution of avian functional traits associated with seed dispersal in tropical forest. Perspect Ecol Conserv. https://doi.org/10.1016/j.pecon.2018.03.004

    Article  Google Scholar 

  • Bregman TP, Sekercioglu CH, Tobias JA (2014) Global patterns and predictors of bird species responses to forest fragmentation: Implications for ecosystem function and conservation. Biol Conserv 169:372–383

    Google Scholar 

  • Bu W, Huang J, Xu H, Zang R, Ding Y, Li Y, Lin M, Wang J, Zhang C (2019) Plant functional traits are the mediators in regulating effects of abiotic site conditions on aboveground carbon stock-evidence from a 30 ha tropical forest . Front Plant Sci. https://doi.org/10.3389/fpls.2018.01958

    Article  PubMed  PubMed Central  Google Scholar 

  • Büchi L, Vuilleumier S (2012) Dispersal strategies, few dominating or many coexisting: the effect of environmental spatial structure and multiple sources of mortality (dispersal strategies in a metacommunity). PLoS ONE 7:e34733

    PubMed  PubMed Central  Google Scholar 

  • Büchi L, Vuilleumier S (2014) Coexistence of specialist and generalist species is shaped by dispersal and environmental factors. Am Nat 183:612–624

    PubMed  Google Scholar 

  • Büchi L, Vuilleumier S (2016) Ecological strategies in stable and disturbed environments depend on species specialisation. Oikos 125:1408–1420

    Google Scholar 

  • Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J Appl Ecol 48:1079–1087

    Google Scholar 

  • Carmona CP, Azcárate FM, Bello F, Ollero HS, Lepš J, Peco B (2012) Taxonomical and functional diversity turnover in Mediterranean grasslands: interactions between grazing, habitat type and rainfall. J Appl Ecol 49:1084–1093

    Google Scholar 

  • Carmona CP, Francesco de B, Norman WHM, Jan L (2016) Traits without borders: integrating functional diversity across scales traits without borders: integrating functional diversity across scales. Trends Ecol Evol 31:382–394

    PubMed  Google Scholar 

  • Carrié R, Andrieu E, Cunningham SA, Lentini PE, Loreau M, Ouin A (2017) Relationships among ecological traits of wild bee communities along gradients of habitat amount and fragmentation. Ecography 40:85–97

    Google Scholar 

  • Cattarino L, McAlpine CA, Rhodes JRJ (2013) The consequences of interactions between dispersal distance and resolution of habitat clustering for dispersal success. Landsc Ecol 28:1321–1334

    Google Scholar 

  • Cattarino L, McAlpine CA, Rhodes JR (2016) Spatial scale and movement behaviour traits control the impacts of habitat fragmentation on individual fitness. J Anim Ecol 85:168–177

    PubMed  Google Scholar 

  • Cernansky R (2017) Biodiversity moves beyond counting species. Nature 646:22–24

    Google Scholar 

  • Concepcion ED, Moretti M, Altermatt F, Nobis MP, Obrist MK (2015) Impacts of urbanisation on biodiversity: the role of species mobility degree of specialisation spatial scale. Oikos 124:1571–1582

    Google Scholar 

  • de Bello F, Lavorel S, Díaz S, Harrington R, Cornelissen JHC, Bardgett RD, Berg MP, Cipriotti P, Feld CK, Hering D, Martins da Silva P, Potts SG, Sandin L, Sousa JP, Storkey J, Wardle DA, Harrison PA, Sveriges l (2010) Towards an assessment of multiple ecosystem processes and services via functional traits. Biodivers Conserv 19:2873–2893. https://doi.org/10.1007/s10531-010-9850-9

    Article  Google Scholar 

  • Devictor V, Julliard R, Couvet D, Lee A, Jiguet F (2007) Functional homogenization effect of urbanization on bird. Communities Conserv Biol 21:741–751

    PubMed  Google Scholar 

  • Dias CTDS, Samaranayaka A, Manly B (2008) On the use of correlated beta random variables with animal population modelling. Ecol Model 215:293–300

    Google Scholar 

  • Díaz S, Hodgson JG, Thompson K, Cabido M, Cornelissen JHC, Jalili A, Montserrat-Martí G, Grime JP, Zarrinkamar F, Asri Y, Band SR, Basconcelo S, Castro-Díez P, Funes G, Hamzehee B, Khoshnevi M, Pérez-Harguindeguy N, Pérez- Rontomé MC, Shirvany A, Vendramini F, Yazdani S, Abbas-Azimi R, Bogaard A, Boustani S, Charles M, Dehghan M, Torres-Espuny Ld, Falczuk V, Guerrero-Campo J, Hynd A, Jones G, Kowsary E, Kazemi-Saeed F, Maestro- Martínez M, Romo-Díez A, Shaw S, Siavash B, Villar-Salvador P, Zak MR (2004) The plant traits that drive ecosystems: Evidence from three continents. J Veg Sci 15:295–304. https://doi.org/10.1658/1100-9233(2004)015[0295:TPTTDE]2.0.CO;2

    Article  Google Scholar 

  • Didham RK, Leather SR, Basset Y (2016) Circle the bandwagons – challenges mount against the theoretical foundations of applied functional trait and ecosystem service research Insect Conservation and Diversity 9:1–3 https://doi.org/10.1111/icad.12150

    Article  Google Scholar 

  • Ding Z, Feeley KJ, Wang Y, Pakeman RJ, Ding P (2013) Patterns of bird functional diversity on land-bridge island fragments. J Anim Ecol 82:781–790

    PubMed  Google Scholar 

  • Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494. https://doi.org/10.1890/1540-9295(2003)001[0488:Rdecar]2.0.Co;2

    Article  Google Scholar 

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

    Google Scholar 

  • Fahrig L (2017) Ecological responses to habitat fragmentation per se . Annu Rev Ecol Evol Syst 48:1–23

    Google Scholar 

  • Fahrig L, Baudry J, Brotons L, Burel FG, Crist TO, Fuller RJ, Sirami C, Siriwardena GM, Martin JL (2011) Functional landscape heterogeneity and animal biodiversity in agricultural landscapes. Ecol Lett 14:101–112. https://doi.org/10.1111/j.1461-0248.2010.01559.x

    Article  PubMed  Google Scholar 

  • Farwig N, Schabo DG, Albrecht J (2017) Trait-associated loss of frugivores in fragmented forest does not affect seed removal rates. J Ecol 105:20–28

    Google Scholar 

  • Filgueiras BKC, Tabarelli M, Leal IR, Vaz-de-Mello FZ, Peres CA, Iannuzzi L (2016) Spatial replacement of dung beetles in edge-affected habitats: biotic homogenization or divergence in fragmented tropical forest landscapes? Divers Distrib 22:400–409

    Google Scholar 

  • Fletcher RJ, Didham RK, Banks-Leite C, Barlow J, Ewers RM, Rosindell J, Holt RD, Gonzalez A, Pardini R, Damschen EI, Melo FPL, Ries L, Prevedello JA, Tscharntke T, Laurance WF, Lovejoy T, Haddad NM (2018) Is habitat fragmentation good for biodiversity? Biol Conserv 226:9–15. https://doi.org/10.1016/j.biocon.2018.07.022

    Article  Google Scholar 

  • Flynn DFB, Gogol-Prokurat M, Nogeire T, Molinari N, Richers BT, Lin BB, Simpson N, Mayfield MM, DeClerck F (2009) Loss of functional diversity under land use intensification across multiple taxa. Ecol Lett 12:22–33. https://doi.org/10.1111/j.1461-0248.2008.01255.x

    Article  PubMed  Google Scholar 

  • Galetti MG, Côrtes R, Fadini M, Von Matter R, Leite S, Labecca A, Ribeiro F, Carvalho T, Collevatt C, Pires R, Guimarães M, Brancalion P Jr, Ribeiro P, Jordano M (2013) Functional extinction of birds drives rapid evolutionary changes seed size. Science 340:6

    Google Scholar 

  • Garibaldi Lucas A, Bartomeus I, Bommarco R, Klein Alexandra M, Cunningham Saul A, Aizen Marcelo A, Boreux V, Garratt Michael PD, Carvalheiro Luísa G, Kremen C, Morales Carolina L, Schüepp C, Chacoff Natacha P, Freitas Breno M, Gagic V, Holzschuh A, Klatt Björn K, Krewenka Kristin M, Krishnan S, Mayfield Margaret M, Motzke I, Otieno M, Petersen J, Potts Simon G, Ricketts Taylor H, Rundlöf M, Sciligo A, Sinu Palatty A, Steffan-Dewenter I, Taki H, Tscharntke T, Vergara Carlos H, Viana Blandina F, Woyciechowski M, Devictor V (2015) Editor's choice: review: Trait matching of flower visitors and crops predicts fruit set better than trait diversity. J Appl Ecol 52:1436–1444. https://doi.org/10.1111/1365-2664.12530

    Article  Google Scholar 

  • González E, Buffa L, Defagó MT, Molina SI, Salvo A, Valladares G (2018) Something is lost and something is gained: loss and replacement of species and functional groups in ant communities at fragmented forests. Landsc Ecol 33:2089–2102

    Google Scholar 

  • Grace JB (2006) Structural equation modeling and natural systems. Cambridge University Press, Cambridge/New York

    Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J, Davies KF, Gonzalez A, Holt RD, Lovejoy TE, Sexton JO, Austin MP, Collins CD, Cook WM, Damschen EI, Ewers RM, Foster BL, Jenkins CN, King AJ, Laurance WF, Levey DJ, Margules CR, Melbourne BA, Nicholls AO, Orrock JL, Song D-X, Townshend JR (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv. https://doi.org/10.1126/sciadv.1500052

    Article  PubMed  PubMed Central  Google Scholar 

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

    Google Scholar 

  • Hatfield JH, Harrison MLK, Banks-Leite C (2018) Functional diversity metrics: how they are affected by landscape change and how they represent ecosystem functioning in the tropics current. Landscc Ecol Rep 3:35–42

    Google Scholar 

  • Henle K, Davies KF, Kleyer M, Margules C, Settele J (2004) Predictors of species sensitivity to fragmentation. Biodivers Conserv 13:207–251

    Google Scholar 

  • Hooper DU, Chapin Iii FS, Ewel JJ, Hector A, Inchausti P, Lavorel S, Lawton JH, Lodge DM, Loreau M, Naeem S, Schmid B, Setälä H, Symstad AJ, Vandermeer J, Wardle DA (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge Ecol Monogr 75:3–35. https://doi.org/10.1890/04-0922

    Article  Google Scholar 

  • Jackson HB, Fahrig L (2015) Are ecologists conducting research at the optimal scale? Global Ecol Biogeogr 24:52–63

    Google Scholar 

  • Keinath DA, Doak DF, Hodges KE, Prugh LR, Fagan W, Sekercioglu CH, Buchart SHM, Kauffman M (2017) A global analysis of traits predicting species sensitivity to habitat fragmentation. Global Ecol Biogeogr 26:115–127. https://doi.org/10.1111/geb.12509

    Article  Google Scholar 

  • Laliberté E, Wells JA, DeClerck F, Metcalfe DJ, Catterall CP, Queiroz C, Aubin I, Bonser SP, Ding Y, Fraterrigo JM, McNamara S, Morgan JW, Merlos DS, Vesk PA, Mayfield MM (2010) Land-use intensification reduces functional redundancy and response diversity in plant communities Ecol Lett 13:76–86. https://doi.org/10.1111/j.1461-0248.2009.01403.x

    Article  PubMed  Google Scholar 

  • Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8:538–547

    PubMed  Google Scholar 

  • Laughlin DC, Messier J (2015) Fitness of multidimensional phenotypes in dynamic adaptive landscapes. Trends Ecol Evol 30:487–496

    PubMed  Google Scholar 

  • Loreau M, Mouquet N, Gonzalez A (2003) Biodiversity as spatial insurance in heterogeneous landscapes. Proc Natl Acad Sci 100:12765

    CAS  PubMed  Google Scholar 

  • Luck GW, Carter A, Smallbone L (2013) Changes in bird functional diversity across multiple land uses: interpretations of functional redundancy depend on functional group. Identity PLoS Biol. https://doi.org/10.1371/journal.pone.0063671

    Article  Google Scholar 

  • Luck GW, Lavorel S, McIntyre S, Lumb K (2012) Improving the application of vertebrate trait-based frameworks to the study of ecosystem services. J Anim Ecol 81:1065–1076

    PubMed  Google Scholar 

  • Magnago LFS, Edwards DP, Edwards FA, Magrach A, Martins SV, Laurance WF (2014) Functional attributes change but functional richness is unchanged after fragmentation of Brazilian Atlantic forests. J Ecol 102:475–485

    Google Scholar 

  • Mayfield MM, Bonser SP, Morgan JW, Aubin I, McNamara S, Vesk PA (2010) What does species richness tell us about functional trait diversity? Predictions and evidence for responses of species and functional trait diversity to land-use change. Global Ecol Biogeogr 19:423–431

    Google Scholar 

  • Mori AS, Furukawa T, Sasaki T (2013) Response diversity determines the resilience of ecosystems to environmental change. Biol Rev Camb Philos Soc 88:349–364

    PubMed  Google Scholar 

  • Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 503:853

    Google Scholar 

  • R Core Team (2015) R: a language and environment for statistical computing, Vienna, Austria. Available at: https://www.R-project.org/

  • Rocha-Santos L, Mayfield MM, Lopes AV, Pessoa MS, Talora DC, Faria D, Cazetta E (2020) The loss of functional diversity: a detrimental influence of landscape-scale deforestation on tree reproductive traits. J Ecol 108:212–223

    Google Scholar 

  • Rosseel Y (2012) lavaan: an R package for structural equation modeling. J Stat Softw. https://doi.org/10.18637/jss.v048.i02

  • Rybicki J, Abrego N, Ovaskainen O (2019) Habitat fragmentation and species diversity in competitive communities. Ecol Lett. https://doi.org/10.1111/ele.13450

    Article  PubMed  PubMed Central  Google Scholar 

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

    PubMed  Google Scholar 

  • Saupe D (1988) Algorithms for random fractals. In: Peitgen H, Saupe D (eds) The science of fractal images. Springer, New York, pp 71–113

    Google Scholar 

  • Sfair JC, Arroyo-Rodríguez V, Santos BA, Tabarelli M (2016) Taxonomic and functional divergence of tree assemblages in a fragmented tropical forest. Ecol Appl 26:1816–1826

    PubMed  Google Scholar 

  • Shipley B (2000) A new inferential test for path models based on directed acyclic graphs. Struct Equ Model 7:206–218

    Google Scholar 

  • Smith TJ, Mayfield MM (2018) The effect of habitat fragmentation on the bee visitor assemblages of three Australian tropical rainforest tree species. Ecol Evol 8:8204–8216

    PubMed  PubMed Central  Google Scholar 

  • Sonnier G, Jamoneau A, Decocq G (2014) Evidence for a direct negative effect of habitat fragmentation on forest herb functional diversity. Landsc Ecol 29:857–866

    Google Scholar 

  • Staddon P, Lindo Z, Crittenden PD, Gilbert F, Gonzalez A (2010) Connectivity, non-random extinction and ecosystem function in experimental metacommunities. Ecol Lett 13:543–552

    PubMed  Google Scholar 

  • Suárez-Castro AF, Simmonds JS, Mitchell MGE, Maron MM, Rhodes J (2018) The scale-dependent role of biological traits in landscape ecology: a review. Curr Landsc Ecol Rep 3:12–22

    Google Scholar 

  • Suding KN, Lavorel S, Chapin Iii FS, Cornelissen JHC, Diaz S, Garnier E, Goldberg D, Hooper DU, Jackson ST, Navas ML (2008) Scaling environmental change through the community-level: a trait-based response-and-effect framework for plants. Global Change Biol 14:1125–1140. https://doi.org/10.1111/j.1365-2486.2008.01557.x

    Article  Google Scholar 

  • Thompson PL, Rayfield B, Gonzalez A (2017) Loss of habitat and connectivity erodes species diversity, ecosystem functioning, and stability in metacommunity networks. Ecography 40:98–108

    Google Scholar 

  • Villard MA, Metzger JP (2014) Beyond the fragmentation debate: a conceptual model to predict when habitat configuration really matters. J Appl Ecol 51:309–318

    Google Scholar 

  • Villéger S, Mason NWH, Mouillot D (2008) New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology 89:2290–2301

    PubMed  Google Scholar 

  • Woodcock BA, Garratt MPD, Powney GD et al (2019) Meta-analysis reveals that pollinator functional diversity and abundance enhance crop pollination and yield. Nat Commun 10:1481

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zambrano J, Garzon-Lopez CX, Yeager L, Fortunel C, Cordeiro NJ, Beckman NG (2019) The effects of habitat loss and fragmentation on plant functional traits and functional diversity: what do we know so far? Oecologia 191:505–518

    PubMed  Google Scholar 

Download references

Acknowledgements

We would like to thank Raphael Didham, Natalie Jones and William Goulding for comments that greatly improved the manuscript. This work was supported by an Australian Research Council (ARC) Discovery Project (DP130100218) and a Colombian Ministry of Education (COLCIENCIAS 529) scholarship to AF Suárez Castro. M Maron was supported by ARC Future Fellowship 140100516.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Andrés Felipe Suárez-Castro.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Suárez-Castro, A.F., Mayfield, M.M., Mitchell, M.G.E. et al. Correlations and variance among species traits explain contrasting impacts of fragmentation and habitat loss on functional diversity. Landscape Ecol 35, 2239–2253 (2020). https://doi.org/10.1007/s10980-020-01098-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10980-020-01098-2

Keywords

Navigation