Abstract
Introduction
Land-use change has tremendous negative impacts on ecosystems that often assessed by using indicator taxa, such as dung beetles. Commonly, changes in dung beetle community attributes are used to evaluate habitat disturbance. Within species, changes in functional traits could also be informative, but are rarely used.
Aims/methods
Our goal was to evaluate whether intraspecific variation in beetle morphology could indicate habitat disturbance, and whether changes in morphology could be a better indicator than changes in abundance.
Beetles were collected in four major land uses: cerrado, eucalypt tree plantations, introduced cattle pastures, and soybean plantations. We focused on nine abundant paracoprid species. For each species in each land use, we estimated mean abundance and five morphological traits.
Results
Seven of the nine species showed intraspecific morphological differences due to land use, while five showed differences in abundance. All morphological traits showed effects of land-use change, but there was much variability in responses depending on species and land uses being compared.
Discussion
In dung beetles, intraspecific changes in phenotypically plastic morphological traits can be a more sensitive indicator of habitat disturbance than changes in abundance.
Implications for insect conservation
When using dung beetles as an indicator taxon, monitoring protocols could use morphological changes of a few focal species, thus avoiding massive lethal sampling which may oppose conservation goals. Also, because morphology is affected by land use, to obtain accurate results, studies using morphological traits to calculate functional community metrics, ought to use separate mean trait values for each habitat condition.
Similar content being viewed by others
References
Albert CH, de Bello F, Boulangeat I, Pellet G, Lavorel S, Thuiller W (2012) On the importance of intraspecific variability for the quantification of functional diversity. Oikos 121:116–126. https://doi.org/10.1111/j.1600-0706.2011.19672.x
Bolnick DI, Amarasekare P, Araújo MS, Reinhard B, Levine JM, Novak M, Rudolf VHW, Schreiber SJ, Urban M, Vasseur DA (2011) Why intraspecific trait variation matters in community ecology. Trends Ecol Evol 26:183–192. https://doi.org/10.1016/j.tree.2011.01.009
Bui VB, Ziegler T, Bonkowski M (2020) Morphological traits reflect dung beetle response to land use changes in tropical karst ecosystems of Vietnam. Ecol Indic 108:105697. https://doi.org/10.1016/j.ecolind.2019.105697
Carvalho RL, Frazão F, Ferreira-Châline RS, Louzada J, Cordeiro L, França F (2018) Dung burial by roller dung beetles (Coleoptera: Scarabaeinae): an individual and specific-level study. Int J Trop Insect Sci 38(4):373–380. https://doi.org/10.1017/S1742758418000206
Carvalho RL, Andersen AN, Anjos DV, Pacheco R, Chagas L, Vasconcelos HL (2020) Understanding what bioindicators are actually indicating: linking disturbance responses to ecological traits of dung beetles and ants. Ecol Indic 108:105764. https://doi.org/10.1016/j.ecolind.2019.105764
Carvalho RL, Vieira J, Melo C, Silva AM, Tolentino VC, Neves K, Vaz de Mello F, Andersen AN, Vasconcelos HL (2022) Interactions between land use, taxonomic group and aspects and levels of diversity in a brazilian savanna: implications for the use of bioindicators. J Appl Ecol 59(10):2642–2653. https://doi.org/10.1111/1365-2664.14270
deCastro-Arrazola I, Andrew N, Berg MP, Curtsdotter A, Lumaret JP, Menéndez R, Moretti M, Nervo B, Nichols ES, Sánchez-Piñero F, Santos AMC, Sheldon KS, Slade E, Horta J (2022) A trait-based framework for dung beetle functional ecology. J Anim Ecol in press. https://doi.org/10.1111/1365-2656.13829
Des Roches S, Post DM, Turley NE, Bailey JK, Hendry AP, Kinnison M, Schweitzer JA, Palkovacs EP (2018) The ecological importance of intraspecific variation. Nat Ecol Evol 2:57–64. https://doi.org/10.1038/s41559-017-0402-5
Fox J, Weisberg S (2011) Multivariate linear models in R. An R Companion to Applied Regression. Thousand Oaks, Los Angeles
França F, Barlow J, Araújo B, Louzada J (2016) Does selective logging stress tropical forest invertebrates? using fat stores to examine sublethal responses in dung beetles. Ecol Evol 6(23):8526–8533
Fuzessy LF, Benítez-López A, Slade EM, Bufalo FS, Magro-de-Souza GC, Pereira LA, Culot L (2021) Identifying the anthropogenic drivers of declines in tropical dung beetle communities and functions. Biol Conserv 256:109063. https://doi.org/10.1016/j.biocon.2021.109063
Gatica-Saavedra P, Echeverría C, Nelson CR (2017) Ecological indicators for assessing ecological success of forest restoration: a world review. Restor Ecol 25(6):850–857. https://doi.org/10.1111/rec.12586
Giménez Gómez VC, Verdú JR, Casanoves F, Zurita GA (2022) Functional responses to anthropogenic disturbance and the importance of selected traits: a study case using dung beetles. Ecol Entomol 47:503–514. https://doi.org/10.1111/een.13135
Gollan JR, de Bruyn LL, Reid N, Wilkie L (2013) Monitoring the ecosystem service provided by dung beetles offers benefits over commonly used biodiversity metrics and a traditional trapping method. J Nat Conserv 21:183–188. https://doi.org/10.1016/j.jnc.2012.12.004
Griffiths HM, Louzada J, Bardgett RD, Barlow J (2016) Assessing the importance of intraspecific variability in dung beetle functional traits. PLoS ONE 11:1–14. https://doi.org/10.1371/journal.pone.0145598
Griffiths HM, Louzada J, Bardgett RD, Barlow J (2016) Assessing the importance of intraspecific variability in dung beetle functional traits. PLoS ONE 11(3):e0145598. https://doi.org/10.1371/journal.pone.0145598
Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S, Hothorn MT (2016) Package ‘multcomp’. Simultaneous inference in general parametric models. Project for Statistical Computing, Vienna
Ibanez CA, Erthal RP, Ogo FM, Peres MN, Vieira HR, Conejo C, Tófolo LP, Francisco FA, Silveira SS, Malta A, Pavanello A, Martins IP, da Silva PHO, Saavedra LPJ, Gonçalves GD, Moreira VM, Alves VS, Silva Franco CC, Previate C, Gomes RM, Venci RO, Dias FRS, Armitage JA, Zambrano E, Mathias PCF, Fernandes GSA, Palma-Rigo K (2017) A high fat diet during adolescence in male rats negatively programs reproductive and metabolic function which is partially ameliorated by exercise. Front Physiol 8:807. https://doi.org/10.3389/fphys.2017.00807
Klink CA, Machado RB (2005) Conservation of the brazilian Cerrado. Conserv Biol 19:707–713. https://doi.org/10.1111/j.1523-1739.2005.00702.x
Larsen TH, Williams NM, Kremen C (2005) Extinction order and altered community structure rapidly disrupt ecosystem functioning. Ecol Lett 8:538–547. https://doi.org/10.1111/j.1461-0248.2005.00749.x
Linz DM, Hu AW, Sitvarin MI, Tomoyasu Y (2016) Functional value of elytra under various stresses in the red flour beetle, Tribolium castaneum. Sci Rep 6:34813. https://doi.org/10.1038/srep34813
López-Bedoya PA, Bohada‐Murillo M, Ángel‐Vallejo MC, Audino LD, Davis ALV, Gurr G, Noriega JA (2022) Primary forest loss and degradation reduces biodiversity and ecosystem functioning: a global meta‐analysis using dung beetles as an indicator taxon. J Appl Ecol 59:1572–1585. https://doi.org/10.1111/1365-2664.14167
Macagno AL, Moczek AP, Pizzo A (2016) Rapid divergence of nesting depth and digging appendages among tunneling dung beetle populations and species. Am Nat 187:E143–E151. https://doi.org/10.1086/685776
Macedo R, Audino LD, Korasaki V, Louzada J (2020) Conversion of Cerrado savannas into exotic pastures: the relative importance of vegetation and food resources for dung beetle assemblages. Agric Ecosyst Environ 288:106709. https://doi.org/10.1016/j.agee.2019.106709
MapBiomas Observatório do Clima, São Paulo, Brazil; www.mapbiomas.org. Acessed in 20/01/2020
Marsh CJ, Louzada J, Beiroz W, Ewers RM (2013) Optimising bait for Pitfall trapping of Amazonian dung beetles (Coleoptera: Scarabaeinae). PLoS ONE 8(8):e73147. https://doi.org/10.1371/journal.pone.0073147
Negro M, Rolando A, Palestrini C (2011) The impact of overgrazing on dung beetle diversity in the Italian Maritime. Alps Environ Entomol 40:1081–1092. https://doi.org/10.1603/EN11105
Nichols E, Gardner TA (2011) Dung beetles as a candidate study taxon in applied biodiversity conservation research. In: Simmons LW, Ridsdill-Smith TJ (eds) Ecology and Evolution of Dung Beetles Chichester. Wiley, West Sussex, pp 267–291
Nichols E, Spector S, Louzada J, Larsen T, Amezquita S, Favila ME, The Scarabaeinae Research Network (2008) Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biol Conserv 141:1461–1474. https://doi.org/10.1016/j.biocon.2008.04.011
Oliveira YF, Oliveira CM, Frizzas MR (2021) Changes in land use affect dung beetle communities but do not affect ecosystem services in the Cerrado of Central Brazil. Ecol Entomol 46:973–987. https://doi.org/10.1111/een.13034
Oliveira-Filho T, Ratter JA (2002) Vegetation physiognomies and woody flora of the savana biome. In: Oliveira OS, Marquis RJ (eds) Cerrados Brazil. Columbia University Press, New York, pp 91–120
Perrin W, Fontana S, Coq S, Berlioz, Jay-Robert P, Moretti M (2021) The influence of fine-scale grazing heterogeneity on dung beetle assemblages: what trait analysis teaches us. Environ Entomol 50:1332–1343. https://doi.org/10.1093/ee/nvab091
Pessôa MB, Izzo TJ, Vaz-de-Mello FZ (2017) Assemblage and functional categorization of dung beetles (Coleoptera: Scarabaeinae) from the Pantanal. PeerJ 5:e3978. https://doi.org/10.7717/peerj.3978
Quintero I, Halffter G (2009) Temporal changes in a comunity of dung beetles (Insecta: Coleoptera: Scarabaeinae) resulting from the modification and fragmentation of tropical rain forest. Acta Zool Mex 25:625–649
Raine EH, Gray CL, Mann DJ, Slade EM (2018) Tropical dung beetle morphological traits predict functional traits and show intraspecific differences across land uses. Ecol Evol 8:8686–8696. https://doi.org/10.1002/ece3.4218
Zuur AF, Ieno EN (2016) A protocol for conducting and presenting results of regression-type analyses. Methods Ecol Evol 7:636–645. https://doi.org/10.1111/2041-210X.12577
R Development Core Team (2022) R: A language and environment for statistical 4 computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07- 5 0, Available: http://www.R-project.org/. Access: Set 2020
Rosa R, Lima SC, Assunção WL (1991) Abordagem preliminar das condições climáticas de Uberlândia (MG). Sociedade Natureza. https://doi.org/10.14393/SN-v3-1991-60693
Salomão RP, González-Tokman D, Dáttilo W, López-Acosta JC, Favila ME (2018) Landscape structure and composition define the body condition of dung beetles (Coleoptera: Scarabaeinae) in a fragmented tropical rainforest. Ecol Indic 88:144–151. https://doi.org/10.1016/j.ecolind.2018.01.033
Salomão RP, Alvarado F, Baena-Díaz F, Favila ME, Iannuzzi L, Liberal CN, Santos BA, Villegas-Guzmán GA, González-Tokman D (2020) Negative effects of urbanisation on the physical condition of an endemic dung beetle from a neotropical hotspot. Ecol Entomol 45(4):886–895. https://doi.org/10.1111/een.12865
Sano EE, Rodrigues AA, Martins ES, Bettiol GM, Bustamante MMC, Bezerra AS, Vasconcelos V, Schuler J, Bolfe E (2019) Cerrado ecoregions: a spatial framework to assess and prioritize brazilian savanna environmental diversity for conservation. J Environ Manag 232:818–828. https://doi.org/10.1016/j.jenvman.2018.11.108
Schulze CH, Waltert M, Kessler PJA, Pitopang R, Shahabuddin, Veddeler D, Mühlenberg M, Gradstein R, Leuschner C, Steffan-Dewenter I, Tscharntke T (2004) Biodiversity indicator groups of tropical land-use systems: comparing plants, birds, and insects. Ecol Applic 14:1321–1333. https://doi.org/10.1890/02-5409
Simmons LW, Ridsdill-Smith TJ (2011) Ecology and evolution of dung beetles. Wiley-Blackwell, West Sussex
Tonelli M, Verdú JR, Zunino ME (2017) Effects of grazing intensity and the use of veterinary medical products on dung beetle biodiversity in the sub-mountainous landscape of central Italy. PeerJ 5:e2780. https://doi.org/10.7717/peerj.2780
Tonelli M, Verdú JR, Zunino M (2018) Effects of the progressive abandonment of grazing on dung beetle biodiversity: body size matters. Biodivers Conserv 27:189–204. https://doi.org/10.1007/s10531-017-1428-3
Tonelli M, Verdú JR, Morelli F, Zunino M (2020) Dung beetles: functional identity, not functional diversity, accounts for ecological process disruption caused by the use of veterinary medical products. J Insect Conserv 24:643–654. https://doi.org/10.1007/s10841-020-00240-4
Turner BL, Lambin EF, Reenberg A (2007) The emergence of land change science for global environmental change and sustainability. Proc Natl Acad Sci USA 104:20666–20671. https://doi.org/10.1073/pnas.0704119104
Vandewalle M, de Bello F, Berg MP, Bolger T, Doledec S, Dubs F, Feld CK, Harrington R, Harrison PA, Lavorel S, Silva PM, Moretti M, Niemela J, Santos P, Sattler T, Souza P, Sykes M, Vanbergen AJ, Woodcock BA (2010) Functional traits as indicators of biodiversity response to land use changes across ecosystems and organisms. Biodiver Conserv 19:2921–2947. https://doi.org/10.1007/s10531-010-9798-9
Violle C, Enquist BJ, McGill BJ et al (2012) The return of the variance: intraspecific variability in community ecology. Trends Ecol Evol 27:244–252. https://doi.org/10.1016/j.tree.2011.11.014
Wang Y, Naumann U, Wright ST, Warton DI (2012) Mvabund- an R package for model-based analysis of multivariate abundance data. Methods Ecol Evol 3:471–474. https://doi.org/10.1111/j.2041-210X.2012.00190.x
Winkler K, Fuchs R, Rounsevell M, Herold M (2021) Global land use changes are four times greater than previously estimated. Nat Commun 12:2501. https://doi.org/10.1038/s41467-021-22702-2
Acknowledgements
RLC is supported by the researcher fellowship FAPESP (2022/07381-9). ALF thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – Brasil (CAPES) – Financing code 001. We also thank CNPq-PELD (441225/2016-0 and 441142/2020-6) and FAPEMIG (APQ-04815-17 and APQ-03372-21) for funding this research.
Author information
Authors and Affiliations
Contributions
ALF, RLC and EA led the writing of the manuscript. RLC collected data in the field. ALF measured the morphological data. FM analyzed the data. All authors made contributions to the intellectual content, interpretation and editing of the manuscript.
Corresponding authors
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Franco, A.L., Carvalho, R.L., Andresen, E. et al. Dung beetle morphological traits show intraspecific differences among four land uses in the Cerrado biome. J Insect Conserv 27, 97–106 (2023). https://doi.org/10.1007/s10841-022-00452-w
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10841-022-00452-w