Abstract
Tropical forests worldwide have succumbed to rapid conversion into agricultural landscapes, but the local- and landscape-scale drivers of functional diversity and consequently ecosystem functioning remain poorly known, which limits management and conservation strategies. Here, we quantitatively assess how biofuel croplands affect taxonomic and functional diversity as well as trait-composition of dung beetle assemblages in a hyper-fragmented landscape of the Brazilian Atlantic forest dominated by sugarcane plantations. We also examine to what extent changes in patch attributes (patch scale forest loss), landscape composition (landscape scale forest loss) and landscape configuration (degree of fragmentation and forest edge density), induced by the establishment of sugarcane plantations, affect the functional reorganization of dung beetle assemblages. We estimated taxonomic and functional diversity (functional richness, evenness and redundancy) of dung beetle assemblages at 50 sampling sites across a sugarcane dominated hyper-fragmented landscape. In general, sugarcane plantations showed lower functional diversity than forest sites. Large-bodied coprophagous tunnelers were dominant across all forest sites, while small-bodied generalist-rollers were more abundant in sugarcane plantations. Functional evenness and dispersion were negatively affected by landscape composition, while landscape configuration and forest loss played a minor role. Our findings indicate that changes at both the patch and landscape scales induced by the establishment of sugarcane plantations exert strong impacts on the taxonomic and functional diversity of dung beetles.
Implications for insect conservation
These shifts in functional diversity can disrupt ecological functions served by these insects which, in turn, can accelerate the collapse of ecosystem functioning across tropical landscapes immersed in sugarcane plantations.
Similar content being viewed by others
References
Alvarado F, Escobar F, Williams DR, Arroyo-Rodríguez V, Escobar-Hernández F (2017) The role of livestock intensification and landscape structure in maintaining tropical biodiversity. J App Ecol 55:185–194
Andresen E (2002) Dung beeltes in Central Amazonian rainforest and their ecological role as secondary seed dispersers. Ecol Entomol 27:257–270
Anduaga S (2004) Impact of the activity of dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae) inhabiting pasture land in Durango, Mexico. Environ Entomol 33:1306–1312
Arellano L, León-Cortés JL, Ovaskainen O (2008) Patterns of abundance and movement in relation to landscape structure: a study of a common scarab (Canthon cyanellus cyanellus) in Southern Mexico. Landsc Ecol 23:69–78
Arroyo-Rodríguez V, Rojas C, Saldaña-Vázquez RA, Stoner KE (2016) Landscape composition is more important than landscape configuration for Phyllostomid bat assemblages in a fragmented biodiversity hotspot. Biol Conserv 198:84–92
Banks-Leite C, Ewers RM, Metzger JP (2010) Edge effects as the principal cause of area effects on birds in fragmented secondary forest. Oikos 119:918–926
Barlow J, Louzada J, Parry L, Hernandez MIM, Hawes J, Peres CA, Vaz-de-Mello F, Gardner TA (2010) Improving the design and management of forest strips in human-dominated tropical landscapes: a field test on Amazonian dung beetles. J App Ecol 47:779–788
Barragán F, Moreno CE, Escobar F, Halffter G, Navarrete D (2011) Negative impacts of human land use on dung beetle functional diversity. PLoS ONE 6:e17976
Beca G, Vancine MH, Carvalho CS, Pedrosa F, Alves RSC, Buscariol D, Peres CA, Ribeiro MC, Galetti M (2017) High mammal species turnover in forest patches immersed in biofuel plantations. Biol Conserv 210:352–359
Braga RF, Korasaki V, Andresen E, Louzada J (2013) Dung beetle community and functions along a habitat-disturbance gradient in the Amazon: a rapid assessment of ecological functions associated to biodiversity. PLoS ONE. https://doi.org/10.1371/journal.pone.005786
Bruno D, Gutiérrez-Cánovas C, Sánchez-Fernández D, Velasco J, Nilsson C (2016) Impacts of environmental filters on functional redundancy in riparian vegetation. J Appl Ecol 53:846–855
Burnham K, Anderson D (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Cadotte MW, Carscadden K, Mirotchnick N (2011) Beyond species: functional diversity and the maintenance of ecological processes and services. J App Ecol 48:1079–1087
Calcagno V, Mazancourt C (2010) Glmulti: an R package for easy automated model selection with (generalized) linear models. J Stat Softw 34:1–29
Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P et al (2012) Biodiversity loss and its impacts on humanity. Nature 486:59–67
Chao A, Jost L (2012) Coverage-based rarefaction and extrapolation: standardizing samples by completeness rather than size. Ecology 93:2533–2547
Chatterjee S, Hadi AS, Price B (2000) Regression analysis by example. Wiley, New York
Choo J, Gill BD, Zuur AF, Zent F, Economo EP (2020) Impacts of an Indigenous settlement on the taxonomic and functional structure of dung beetle communities in the Venezuelan Amazon. Biodivers Conserv 29:207–228
Clarke KR, Gorley RN (2006) PRIMER v6: User Manual/Tutorial. In PRIMER-E. Plymouth.
Crawley MJ (2013) The R Book (2nd edn). Wiley, New York
Debastiani VJ, Pillar VD (2012) SYNCSA-R tool for analysis of metacommunities based on functional traits and phylogeny of the community components. Bioinformatics 28:2067–2068
Eigenbrod F, Hecnar SJ, Fahrig L (2011) Sub-optimal study design has major impacts on landscape-scale inference. Biol Conserv 144:298–305
Elmqvist T, Folke C, Nystrom M, Peterson G, Bengtsson J, Walker B, Norberg J (2003) Response diversity, ecosystem change, and resilience. Front Ecol Environ 1:488–494
ESRI (2016) ArcGIS desktop: Release 10.2. Redlands, CA: Environmental Systems Research Institute.
Estrada A, Anzures A, Coates-Estrada R (1999) Tropical rain forest fragmentation, howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas, Mexico. Am J Primatol 48:253–262
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol S 34:487–515
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
Fahrig L, Arroyo-Rodríguez V, Bennett JR, Boucher-LalondeV CE et al (2019) Is habitat fragmentation bad for biodiversity? Biol Conserv 230:179–186
Filgueiras BKC, Iannuzzi L, Leal IR (2011) Habitat fragmentation alters the structure of dung beetle communities in the Atlantic Forest. Biol Conserv 144:362–369
Filgueiras BKC, Tabarelli M, Leal IR, Vaz-de-Mello F, Iannuzzi L (2015) Dung beetle persistence in human-modified landscapes: combining species indicators with anthropogenic land use and fragmentation-related effects. Ecol Indic 55:65–73
Fincher GT (1973) Dung beetles as biological control agents for gastrointestinal parasites of livestock. J Parasitol 59:396–399
Fletcher RJ, Ries L, Batin J, Chalfoun AD (2007) The role of habitat area and edge in fragmented landscapes: definitively distinct or inevitably intertwined? Can J Zool 8:1017–1030
Fox J, Weisberg S (2011) An {R} Companion to Applied Regression, Second Edition. Thousand Oaks CA: Sage. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion
Gardner TA, Hernández MIM, Barlow J, Peres CA (2008) Understanding the biodiversity consequences of habitat change: the value of secondary and plantation forests for neotropical dung beetles. J App Ecol 45:883–893
Gascon C, Lovejoy TE, JrRO B, Malcolm JR, Stouffer PC, Vasconcelos HL, Laurance WF, Zimmerman B, Tocher M, Borges S (1999) Matrix habitat and species richness in tropical forest remnants. Biol Conserv 91:223–229
Gotelli NJ, Graves GR (1996) Null models in ecology. Smithsonian Institution Press, Washington, DC
Guillemot N, Kulbicki M, Chabanet P, Vigliola L (2011) Functional redundancy patterns reveal non-random assembly rules in a species-rich marine assemblage. PLoS ONE 6:e26735
Halffter G, Matthews EG (1966) The natural history of dung beetles of the subfamily Scarabaeinae (Coleoptera, Scarabaeidae). Folia Entomol Mex 12:1–312
Harper KA, Macdonald SE, Burton PJ, Chen J, Brosofske KD, Saunders SC, Euskirchen ES, Roberts DAR, Jaiteh MS, Pers-Anders E (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv Biol 19:768–782
Hooper DU, Chapin FSIII, Ewel JJ, Hector A, Inchausti P, Lavorel S et al (2005) Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35
Hsieh TC, Ma KH, Chao A, McInerny G (2016) iNEXT: an R package for rarefaction and extrapolation of species diversity (Hill numbers). Methods Ecol Evol 7:1451–1456
Jaeger JAG (2000) Landscape division, splitting index, and effective mesh size: new measures of landscape fragmentation. Landsc Ecol 15:115–130
Jaiswal D, De Souza A, Larsen S et al (2017) Brazilian sugarcane ethanol as an expandable green alternative to crude oil use. Nat Clim Change 7:788–792
Jost L (2006) Entropy and diversity. Oikos 113:363–375
Jost L (2007) Partitioning diversity into independent alpha and beta components. Ecology 88:2427–2439
Klingbeil BT, Willig MR (2016) Matrix composition and landscape heterogeneity structure multiple dimensions of biodiversity in temperate forest birds. Biodivers Conserv 25:2687–2708
Korasaki V, Braga RF, Zanetti R, Moreira FMS, Vaz-de-Mello FZ, Louzada J (2013) Conservation value of land-use systems for dung beetles in Amazon: valuing traditional farming practices. Biodivers Conserv 22:1485–1499
Laliberté E, Legendre P, Shipley B (2015) Measuring functional diversity (FD) from multiple traits, and other tools for functional ecology. Package ‘‘FD’’ for version 1.0–12
Laurance WF (2001) Fragmentation and plant communities: synthesis and implications for landscape management. In: Bierregaard Jr RO, Gascon C, Lovejoy TE, Mesquita RCG (eds) Lessons from Amazonia: the ecology and conservation of a fragmented forest. Yale University Press, New Haven, pp 158–168
Laurance WF, Ferreira LV, Rankin-de-Merona JM, Laurance SG (1998) Rain forest fragmentation and the dynamics of Amazonian tree communities. Ecology 79:2032–2040
Lee JSH, Lee IQW, Lee-Hong S, Lim Huijbregts J, Navjot S (2009) Changes in dung beetle communities along a gradient of tropical forest disturbance in south-east Asia. J Trop Ecol 25:677–680
Liu Y, Xu Y, Zhang F, Yun J, Shen Z (2014) The impact of biofuel plantation on biodiversity: a review. Chinese Sci Bull 59:4639–4651
Lopes AV, Girão LC, Santos BA, Peres CA, Tabarelli M (2009) Long-term erosion of tree reproductive trait diversity in edge-dominated Atlantic Forest fragments. Biol Conserv 142:1154–1165
Louzada J, Lima AP, Matavelli R, Zambaldi L, Barlow J (2010) Community structure of dung beetles in Amazonian savannas: role of fire disturbance, vegetation and landscape structure. Landsc Ecol 25:631–641
Martinelli LA, Filoso S (2008) Expansion of sugarcane ethanol production in Brazil: environmental and social challenges. Ecol Appl 18:855–898
McGarigal K, Cushman SA (2002) Comparative evaluation of experimental approaches to the study of habitat fragmentation effects. Ecol Appl 12:335–345
Melo FPL, Arroyo-Rodríguez V, Fahrig L, Martínez-Ramos M, Tabarelli M (2013) On the hope for biodiversity-friendly tropical landscapes. Trends Ecol Evol 28:462–468
Mendes G, Arroyo-Rodríguez V, Almeida VR, Pinto SRR, Pillar VD, Tabarelli M (2016) Plant trait distribution and the spatial reorganization of tree assemblages in a fragmented tropical forest landscape. Plant Ecol 217:31–42
Mouillot D, Graham NAJ, Villéger S, Mason NWH, Bellwood DR (2013) A functional approach reveals community responses to disturbances. Trends Ecol Evol 28:167–177
Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62
Nichols E, Larsen T, Spector S, Davis AL, Escobar F, Favila M, Vulinec K, Scarabaeinae Research Network (2007) Global dung beetle response to tropical forest modification and fragmentation: a quantitative literature review and meta-analysis. Biol Conserv 137:1–19
Nichols E, Uriarte M, Bunker DE, Favila ME, Slade EM, Vulinec K, Larsen T, Vaz-de-Mello FZM, Louzada J, Naeem S, Spector SH (2013) Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales. Ecology 94:180–189
Oliveira MA, Grillo AS, Tabarelli M (2004) Forest edge in the Brazilian Atlantic forest: drastic changes in tree species assemblages. Oryx 38:389–394
Peck SB, Forsyth A (1982) Composition, structure and competitive behavior in a guild of Ecuadorian rain forest dung beetles (Coleoptera, Scarabaeidae). Can J Zool 60:1624–1634
Pfeifer M, Lefebvre V, Peres CA, Banks-Leite C, Wearn OR, Marsh CJ, Butchart SHM, Arroyo-Rodríguez V, Barlow J, Cerezo A et al (2017) Creation of forest edges has a global impact on forest vertebrates. Nature 551:187–191
Pimentel DS, Tabarelli M (2004) Seed dispersal of the palm Attalea oleifera in a remnant of the Brazilian Atlantic Forest. Biotropica 36:74–84
Püttker T, Crouzeilles R, Almeida-Gomes M, Schmoeller M, Maurenza D et al (2020) Indirect effects of habitat loss via habitat fragmentation: a cross-taxa analysis of forest-dependent species. Biol Conserv 241:18368
R Core Team (2017) R: a language and environment for statistical computing. R Core Team, Vienna
Ribeiro MC, Metzger JP, Martensen AC, Ponzoni FJ, Hirota MM (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153
Sajjad A, Ahmad F, Makhdoom AH, Imran A (2012) Does trash burning harm arthropods biodiversity in sugarcane? Int J Agric Biol 14:1021–1023
Sánchez-de-Jésus H, Arroyo-Rodríguez V, Andresen E, Escobar F (2016) Forest loss and matrix composition are the major drivers shaping dung beetle assemblages in a fragmented rainforest. Landsc Ecol 31:843–854
Santos BA, Peres CA, Oliveira MA, Grillo A, Alves-Costa CP, Tabarelli M (2008) Drastic erosion in functional attributes of tree assemblages in Atlantic Forest fragments of northeastern Brazil. Biol Conserv 141:249–260
Santos LAO, Guevara NN, Fernandes OA (2017) Diversity and abundance of edaphic arthropods associated with conventional and organic sugarcane crops in Brazil. Flo Entomol 100:134–144
Silva JMC, Casteleti CHM (2003) Status of the biodiversity of the Atlantic forest of Brazil. In: Galindo-Leal C, Câmara IG (eds) The Atlantic Forest of South America: biodiversity status, threats and outlook. Island Press and CABS, Washington, DC, pp 43–59
Silva PG, Hernández M (2015) Scale-dependence of processes structuring dung beetle metacommunities using functional diversity and community deconstruction approaches. PLoS ONE 10(3):1–29
Silva JMC, Tabarelli M (2000) Tree species impoverishment and the future flora of the Atlantic forest of northeast Brazil. Nature 404:2–73
Slade EM, Mann DJ, Villanueva JF, Lewis OT (2007) Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical Forest. J Anim Ecol 76:1094–1104
Tabarelli M, Lopes AV, Peres CA (2008) Edge-effects drive tropical forest fragments towards an early-successional system. Biotropica 40:657–661
Yamada D, Imura O, Shi K, Shibuya T (2007) Effect of tunneler dung beetles on cattle dung decomposition, soil nutrients and herbage growth. Grassland Sci 53:121–129
Acknowledgements
We thank Conservação Internacional do Brasil for provide aerial photographs of the Usina Serra Grande; Luis Antônio Bezerra and José Clodoaldo Bakker for authorizing our fieldwork at the Usina Serra Grande. Conservação Internacional do Brasil, Centro de Estudos Ambientais do Nordeste and Usina Serra Grande provided infrastructure and logistic support during the field work. We thank Fernando Z. Vaz-de-Mello (UFMT) for help with the taxonomic identifications. We are also grateful to “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior” (CAPES) for financial support (PNPD # 02488/09-4).
Funding
No funding was received for conducting this study.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The author declares that they have no conflict of interest.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Filgueiras, B.K.C., Peres, C.A., Iannuzzi, L. et al. Functional reorganization of dung beetle assemblages in forest-replacing sugarcane plantations. J Insect Conserv 26, 683–695 (2022). https://doi.org/10.1007/s10841-022-00412-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-022-00412-4