Temporal changes of taxonomic and functional diversity in dung beetles inhabiting forest fragments and pastures in Los Tuxtlas Biosphere Reserve, Mexico
DOI:
https://doi.org/10.22201/ib.20078706e.2023.94.5059Keywords:
Anthropogenic landscape, Bioindicators, Habitat modification, Scarabaeinae, Temporal patternsAbstract
We evaluated short- (among months within-years) and long-term (between 1999-2000 and 2016-2017) temporal patterns of taxonomic and functional β- diversity (and its components of substitution and gain/loss) of dung beetle assemblages in forest fragments and pastures in the Los Tuxtlas Biosphere Reserve (LTBR). Habitat type affected the taxonomic dissimilarity and the richness difference component, with average values being respectively 1.42 and 1.56 times higher in pastures than in forest fragments. Only habitat type was important for functional richness, being 1.93 and 1.69 higher in forest fragments than pastures in 1999-2000 and 2016-2017, respectively. Pastures were taxonomically and functionally poorer but were also more temporally dynamic than forest fragments both within-year and between-years. Habitat type is a determining factor for temporal dynamics, with forest fragments presenting more stable dung beetle assemblages than cattle pastures.
References
Alvarado, F., Escobar, F., Williams, D. R., Arroyo-Rodríguez, V., & Escobar-Hernández, F. (2018). The role of livestock intensification and landscape structure in maintaining tropical biodiversity. Journal of Applied Ecology, 55, 185–194. https://doi.org/10.1111/1365-2664.12957
Andresen, E. (2003). Effect of forest fragmentation on dung beetle communities and functional consequences for plant regeneration. Ecography, 26, 87–97. https://doi.org/10.1034/j.1600-0587.2003.03362.x
Andresen, E., & Feer, F. (2005). The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests. In P. M. Forget, J. E. Lambert, P. E. Hulme, & S. B. Vander-Walls (Eds.), Seed fate: predation, dispersal, and seedling establishment (pp. 331–349). CAB International: Wallingford.
Audino, L. D., Louzada, J., & Comita, L. (2014). Dung beetles as indicators of tropical forest restoration success: Is it possible to recover species and functional diversity? Biological Conservation, 169, 248–257. https://doi.org/10.1016/j.biocon.2013.11.023
Barlow, J., Gardner, T. A., Louzada, J., & Peres, C. A. (2010). Measuring the conservation value of tropical primary forests: the effect of occasional species on estimates of biodiversity uniqueness. Plos One, 5, e9609. https://doi.org/10.1371/journal.pone.0009609
Barlow, J., Lennox, G. D., Ferreira, J., Berenguer, E., Lees, A. C., Mac Nally, R. et al. (2016). Anthropogenic disturbance in tropical forests can double biodiversity loss from deforestation. Nature, 535, 144–147. https://doi.org/10.1038/nature18326
Barragan, F., Moreno, C. E., Escobar, F., Halffter, G., & Navarrete, D. (2011). Negative impacts of human land use on dung beetle functional diversity. Plos One, 6, e17976. https://doi.org/10.1371/journal.pone.0017976
Baselga, A., & Orme, C. D. L. (2012). betapart: an R package for the study of beta diversity. Methods in Ecology and Evolution, 3, 808–812. https://doi.org/10.1111/j.204114210X.2012.00224.x
Baselga, A., Orme, D., Villéger, S., De Bortoli, J., & Leprieur, F. (2018). betapart: Partitioning beta diversity into turnover and nestedness components. R package version 1.5.0. https://CRAN.R-project.org/package=betapart.
Biggs, C. R., Yeager, L. A., Bolser, D. G., Bonsell, C., Dichiera, A. M., Hou, Z. et al. (2020). Does functional redundancy affect ecological stability and resilience? A review and meta-analysis. Ecosphere, 11, e03184. https://doi.org/10.1002/ecs2.3184
Bourg, A., Escobar, F., MacGregor-Fors, I., & Moreno, C. E. (2016). Got dung? Resource selection by dung beetles in neotropical forest fragments and cattle pastures. Neotropical Entomology, 45, 490–498. https://doi.org/10.1007/s13744-016-0397-7
Braga, R. F., 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, 8, e57786. https://doi.org/10.1371/journal.pone.0057786.g001
Cardoso, P., Mammola, S., Rigal, F., & Carvalho, J. C. (2020). Package 'BAT': Biodiversity Assessment Tools. R package version 2.1.0. https://CRAN.R-project.org/package=BAT.
Castillo-Escrivà, A., Mesquita-Joanes, F., & Rueda, J. (2020). Effects of the temporal scale of observation on the analysis of aquatic invertebrate metacommunities. Frontiers in Ecology and Evolution, 8, 561838. https://doi.org/10.3389/fevo.2020.561838
Castro, D. M. P., da Silva, P. G., Solar, R., & Callisto, M. (2020). Unveiling patterns of taxonomic and functional diversities of stream insects across four spatial scales in the neotropical savanna. Ecological Indicators, 118, 106769. https://doi.org/10.1016/j.ecolind.2020.106769
Chao, A., & Lin, S. Y. (2011). Program CLAM (Classification method). Program and user’s guide. http://purl.oclc.org/clam. Assessed on: 20 October 2018.
Chazdon, R. L., Chao, A., Colwell, R. K., Lin, S.-Y., Norden, N., Letcher, S. G. et al. (2011). A novel statistical method for classifying habitat generalists and specialists. Ecology, 92, 1332–1343. https://doi.org/10.1890/10-1345.1
Conanp (Comisión Nacional de Áreas Naturales Protegidas). (2019). Áreas Naturales Protegidas decretadas. Gobierno de México. Recuperado el 16 noviembre, 2020 de: https://www.gob.mx/conanp/acciones-y-programas/areas-naturales-protegidas-decretadas
Correa, C. M. A., Ferreira, K. R., Abot, A. R., Louzada, J., & Vaz-de-Mello, F. Z. (2022). Ivermectin impacts on dung beetle diversity and their ecological functions in two distinct Brazilian ecosystems. Ecological Entomology, 47, 736–748. https://doi.org/10.1111/een.13158
Crawley, M. J. (2013). The R Book. Chichester: John Wiley.
Cuesta, E., & Lobo, J. M. (2019). A comparison of dung beetle assemblages (Coleoptera, Scarabaeoidea) collected 34 years apart in an Iberian mountain locality. Journal of Insect Conservation, 23, 101–110. https://doi.org/10.1007/s10841-018-00119-5
da Silva, P. G., Hernández, M. I. M., & Heino, J. (2018). Disentangling the correlates of species and site contributions to beta diversity in dung beetle assemblages. Diversity and Distributions, 24, 1674–1686. https://doi.org/10.1111/ddi.12785
da Silva, P. G., Lobo, J. M., & Hernández, M. I. M. (2019). The role of habitat and daily activity patterns in explaining the diversity of mountain Neotropical dung beetle assemblages. Austral Ecology, 44, 300–312. https://doi.org/10.1111/aec.12675
Díaz, A., & Favila, M. E. (2009). Escarabajos coprófagos y necrofagos (Scarabaeidae, Trogidae y Silphidae) de al Reserva de la Biosfera Los Tuxtlas, México. In V. Hernández-Ortiz, C. Deloya, & P. Reyes-Castillos (Eds.), Memorias VIII Reunión Latinoamericana de Scarabaeoidología (pp. 1–4). Los Tuxtlas, Veracruz: Instituto de Ecología, A.C.
Dirzo, R., Young, H. S., Galetti, M., Ceballos, G., Isaac, N. J. B., & Collen, B. (2014). Defaunation in the Anthropocene. Science, 345, 401–406. https://doi.org/10.1126/science.1251817
Dornelas, M., Gotelli, N. J., McGill, B., Shimadzu, H., Moyes, F., Sievers, C. et al. (2014). Assemblage time series reveal biodiversity change but not systematic loss. Science, 344, 296–299. https://doi.org/10.1126/science.1248484
Edwards, D. P., Gilroy, J. J., Thomas, G. H., Uribe, C. A. M., & Haugaasen, T. (2015). Land-sparing agriculture best protects avian phylogenetic diversity. Current Biology, 25, 2384–2391. https://doi.org/10.1016/j.cub.2015.07.063
Escobar, F., Halffter, G., & Arellano, L. (2007). From forest to pasture: an evaluation of the influence of environment and biogeography on the structure of beetle (Scarabaeinae) assemblages along three altitudinal gradients in the Neotropical region. Ecography, 30, 193–208. https://doi.org/10.1111/j.2007.0906-7590.04818.x
Escobar, F., Halffter, G., Solís, Á., Halffter, V., & Navarrete, D. (2008). Temporal shifts in dung beetle community structure within a protected area of tropical wet forest: a 35-year study and its implications for long-term conservation. Journal of Applied Ecology, 45, 1584–1592. https://doi.org/10.1111/j.1365-2664.2008.01551.x
Estrada, A., Coates-Estrada, R., Dadda, A. A., & Cammarano, P. (1998). Dung and carrion beetles in tropical rain forest fragments and agricultural habitats at Los Tuxtlas, Mexico. Journal of Tropical Ecology, 14, 577–593. https://doi.org/10.1017/S0266467498000418
Favila, M. E. (2004). Los escarabajos y la fragmentación. In S. Guevara, J. Laborde, & G. Sánchez-Ríoss (Eds.), Los Tuxtlas, el paisaje de la sierra (pp. 135–157). Xalapa: Instituto de Ecología A.C.
Favila, M. E. (2005). Diversidad alfa y beta de los escarabajos del estiércol (Scarabaeinae) en Los Tuxtlas, México. In G. Halffter, J. Soberón, P. Koleff, & A. Melics (Eds.), Sobre diversidad biológica: el significado de las diversidades alfa, beta y gamma (pp. 209–219). Zaragoza: Sociedad Entomológica Aragonesa.
Ferreira, S. C., da Silva, P. G., Paladini, A., & Di Mare, R. A. (2019). Climatic variables drive temporal patterns of α and β diversities of dung beetles. Bulletin of Entomological Research, 109, 390–397. https://doi.org/10.1017/S0007485318000676
Filgueiras, B. K. C., Melo, D. H. A., Andersen, A. N., Tabarelli, M., & Leal, I. R. (2019). Cross-taxon congruence in insect responses to fragmentation of Brazilian Atlantic forest. Ecological Indicators, 98, 523–530. https://doi.org/10.1016/j.ecolind.2018.11.036
Flynn, D. F., Gogol-Prokurat, M., Nogeire, T., Molinari, N., Richers, B. T., Lin, B. B. et al. (2009). Loss of functional diversity under land use intensification across multiple taxa. Ecology Letters, 12, 22–33. https://doi.org/10.1111/j.1461-0248.2008.01255.x
Frank, K., Brückner, A., Blüthgen, N., & Schmitt, T. (2018). In search of cues: dung beetle attraction and the significance of volatile composition of dung. Chemoecology, 28, 145–152. https://doi.org/10.1007/s00049-018-0266-4
Frank, K., Bruckner, A., Hilpert, A., Heethoff, M., & Bluthgen, N. (2017). Nutrient quality of vertebrate dung as a diet for dung beetles. Scientific Reports, 7, 12141. https://doi.org/10.1038/s41598-017-12265-y
Gardner, T. A., Barlow, J., Chazdon, R., Ewers, R. M., Harvey, C. A., Peres, C. A. et al. (2009). Prospects for tropical forest biodiversity in a human-modified world. Ecology Letters, 12, 561–582. https://doi.org/10.1111/j.1461-0248.2009.01294.x
Gibbs, H. K., Ruesch, A. S., Achard, F., Clayton, M. K., Holmgren, P., Ramankutty, N. et al. (2010). Tropical forests were the primary sources of new agricultural land in the 1980s and 1990s. Proceedings of the National Academy of Sciences, 107, 16732–16737. https://doi.org/10.1073/pnas.0910275107
Gill, B. (1991). Dung beetles in tropical American forests. In I. Hanski, & Y. Cambeforts (Eds.), Dung beetle ecology (pp. 211–229). Princeton University Press: Princeton.
Giménez Gómez, V. C., Verdú, J. R., & Zurita, G. A. (2020). Thermal niche helps to explain the ability of dung beetles to exploit disturbed habitats. Scientific Reports, 10, 13364. https://doi.org/10.1038/s41598-020-70284-8
Guevara, S., Laborde-Dovalí, J., & Sánchez-Ríos, G. (2000). La Reserva de la Biosfera Los Tuxtlas. Paris: UNESCO.
Guevara, S., Laborde, J., & Sánchez, G. (2004). Los Tuxtlas: el paisaje de la sierra. Mexico D.F.: Instituto de Ecología.
Gutiérrez-García, G., & Ricker, M. (2011). Climate and climate change in the region of Los Tuxtlas (Veracruz, Mexico): a statistical analysis. Atmósfera, 24, 347–373.
Halffter, G. (2005). Towards a culture of biodiversity conservation. Acta Zoológica Mexicana Nueva Serie, 21, 133–153. https://doi.org/10.21829/azm.2005.2121991
Halffter, G., & Arellano, L. (2002). Response of dung beetle diversity to human-induced changes in a tropical landscape. Biotropica, 34, 144–154. https://doi.org/10.1111/j.1744-7429.2002.tb00250.x
Halffter, G., & Edmonds, W. D. (1982). Nesting behavior of dung beetles (Scarabaeinae). Mexico D.F.: Man and Biosphere Program - UNESCO.
Hansen, M. C., Wang, L., Song, X. P., Tyukavina, A., Turubanova, S., Potapov, P. V. et al. (2020). The fate of tropical forest fragments. Science Advances, 6, eaax8574. https://doi.org/10.1126/sciadv.aax8574
Hanski, I. (1991). The dung insect community. In I. Hanski, & Y. Cambeforts (Eds.), Dung beetle ecology (pp. 5–21). Princeton: Princeton University Press.
Hernández, M. I. M., & Vaz-de Mello, F. Z. (2009). Seasonal and spatial species richness variation of dung beetle (Coleoptera, Scarabaeidae s. str.) in the Atlantic Forest of southeastern Brazil. Revista Brasileira de Entomologia, 53, 607–613. https://doi.org/10.1590/S0085-56262009000400010
Herrick, J. E., & Lal, R. (1996). Dung decomposition and pedoturbation in a seasonally dry tropical pasture. Biology and Fertility of Soils, 23, 177–181. https://doi.org/10.1007/BF00336060
Horgan, F. G. (2005). Effects of deforestation on diversity, biomass and function of dung beetles on the eastern slopes of the Peruvian Andes. Forest Ecology and Management, 216, 117–133. https://doi.org/10.1016/j.foreco.2005.05.049
Horgan, F. G. (2008). Dung beetle assemblages in forests and pastures of El Salvador: a functional comparison. Biodiversity and Conservation, 17, 2961–2978. https://doi.org/10.1007/s10531-008-9408-2
Howden, H., & Gill, B. (1993). Mesoamerican Onthophagus Latreille in the dicranius and mirabilis species groups (Coleoptera: Scarabaeidae). The Canadian Entomologist, 125, 1091–1114. https://doi.org/10.4039/Ent1251091-6
Howden, H. F., & Young, O. P. (1981). Panamanian Scarabaeinae: Taxonomy, distribution, and habits (Coleoptera, Scarabaeidae). Contributions American Entomological Institute, 18, 1–204.
Laliberté, E., Legendre, P., & Shipley, B. (2014). FD: measuring functional diversity from multiple traits, and other tools for functional ecology. R package version 1.0-12. https://cran.r-project.org/web/packages/FD/index.html.
Larsen, T., Lopera, A., & Forsyth, A. (2006). Extreme trophic and habitat specialization by Peruvian dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The Coleopterists Bulletin, 60, 315–324.
https://doi.org/10.1649/0010-065X(2006)60[315:ETAHSB]2.0.CO;2
Laurance, W. F. (2007). Have we overstated the tropical biodiversity crisis? Trends in Ecology & Evolution, 22, 65–70. https://doi.org/10.1016/j.tree.2006.09.014
Laurance, W. F., Sayer, J., & Cassman, K. G. (2014). Agricultural expansion and its impacts on tropical nature. Trends in Ecology & Evolution, 29, 107–116. https://doi.org/10.1016/j.tree.2013.12.001
Legendre, P. (2014). Interpreting the replacement and richness difference components of beta diversity. Global Ecology and Biogeography, 23, 1324–1334. https://doi.org/10.1111/geb.12207
Legendre, P. (2019). A temporal beta‐diversity index to identify sites that have changed in exceptional ways in space–time surveys. Ecology and Evolution, 9, 3500–3514. https://doi.org/10.1002/ece3.4984
Lindholm, M., Alahuhta, J., Heino, J., & Toivonen, H. (2020). No biotic homogenisation across decades but consistent effects of landscape position and pH on macrophyte communities in boreal lakes. Ecography, 43, 294–305. https://doi.org/10.1111/ecog.04757
Loiseau, N., Legras, G., Gaertner, J.-C., Verley, P., Chabanet, P., & Mérigot, B. (2017). Performance of partitioning functional beta-diversity indices: Influence of functional representation and partitioning methods. Global Ecology and Biogeography, 26, 753–762. https://doi.org/10.1111/geb.12581
Magurran, A. E., Dornelas, M., Moyes, F., Henderson, P. A., & Storch, D. (2019). Temporal β diversity —a macroecological perspective. Global Ecology and Biogeography, 28, 1949–1960. https://doi.org/10.1111/geb.13026
Maire, E., Grenouillet, G., Brosse, S., & Villéger, S. (2015). How many dimensions are needed to accurately assess functional diversity? A pragmatic approach for assessing the quality of functional spaces. Global Ecology and Biogeography, 24, 728–740. https://doi.org/10.1111/geb.12299
Monjardín-Armenta, S. A., Pacheco-Angulo, C. E., Plata-Roch, W., & Corrales-Barraza, G. (2017). La deforestación y sus factores causales en el estado de Sinaloa, México. Madera y Bosques, 23, 7–22. https://doi.org/10.21829/myb.2017.2311482
Myers, N., Mittermeier, R. A., Mittermeier, C. G., Fonseca, G. A. B., & Kent, J. (2000). Biodiversity hotspots for conservation priorities. Nature, 403, 853–845. https://doi.org/10.1038/35002501
Navarrete, D., & Halffter, G. (2008). Dung beetle (Coleoptera: Scarabaeidae: Scarabaeinae) diversity in continuous forest, forest fragments and cattle pastures in a landscape of Chiapas, Mexico: the effects of anthropogenic changes. Biodiversity and Conservation, 17, 2869–2898. https://doi.org/10.1007/s10531-008-9402-8
Neves, F. d. S., Oliveira, V. H. F., Espírito-Santo, M. M., Vaz-de-Mello, F. Z., Louzada, J., Sanchez-Azofeifa, A. et al. (2010). Successional and seasonal changes in a community of dung beetles (Coleoptera: Scarabaeinae) in a Brazilian tropical dry forest. Natureza & Conservacao, 8, 160–164. https://doi.org/10.4322/natcon.00802009
Newbold, T., Bentley, L. F., Hill, S. L. L., Edgar, M. J., Horton, M., Su, G. et al. (2020). Global effects of land use on biodiversity differ among functional groups. Functional Ecology, 34, 684–693. https://doi.org/10.1111/1365-2435.13500
Newbold, T., Hudson, L. N., Hill, S. L., Contu, S., Lysenko, I., Senior, R. A. et al. (2015). Global effects of land use on local terrestrial biodiversity. Nature, 520, 45–50. https://doi.org/10.1038/nature14324
Nichols, E., Spector, S., Louzada, J., Larsen, T., Amezquita, S., Favila, M. E. et al. (2008). Ecological functions and ecosystem services provided by Scarabaeinae dung beetles. Biological Conservation, 141, 1461–1474. https://doi.org/10.1016/j.biocon.2008.04.011
Nichols, E., Uriarte, M., Bunker, D. E., Favila, M. E., Slade, E. M., Vulinec, K. et al. (2013). Trait-dependent response of dung beetle populations to tropical forest conversion at local and regional scales. Ecology, 94, 180–189. https://doi.org/10.1890/12-0251.1
Noriega, J. A., Santos, A. M. C., Calatayud, J., Chozas, S., & Hortal, J. (2021). Short- and long-term temporal changes in the assemblage structure of Amazonian dung beetles. Oecologia, 195, 719–736. https://doi.org/10.1007/s00442-020-04831-5
R Core Team. (2021). R: A language and environment for statistical computing. R Foundation for Statistical Computing: Austria, Vienna.
Ribeiro, M. C., Metzger, J. P., Martensen, A. C., Ponzoni, F. J., & Hirota, M. M. (2009). The Brazilian Atlantic Forest: How much is left, and how is the remaining forest distributed? Implications for conservation. Biological Conservation, 142, 1141–1153. https://doi.org/10.1016/j.biocon.2009.02.021
Rivera, J. D., da Silva, P. G., & Favila, M. E. (2021). Landscape effects on taxonomic and functional diversity of dung beetle assemblages in a highly fragmented tropical forest. Forest Ecology and Management, 496, 119390. https://doi.org/10.1016/j.foreco.2021.119390
Rivera, J. D., Espinosa-de los Monteros, A., da Silva, P. G., & Favila, M. E. (2022). Dung beetles maintain phylogenetic divergence but functional convergence across a highly fragmented tropical landscape. Journal of Applied Ecology, 59, 1781–1791. https://doi.org/10.1111/1365-2664.14185
Rosenfeld, J. S. (2002). Functional redundancy in ecology and conservation. Oikos, 98, 156–162. https://doi.org/10.1034/j.1600-0706.2002.980116.x
Rosete-Vergés, F. A., Pérez-Damián, J. L., Villalobos-Delgado, M., Navarro-Salas, E. N., Salinas-Chávez, E., & Remond-Noa, R. (2014). El avance de la deforestación en México 1976-2007. Madera y Bosques, 20, 21–35. https://doi.org/10.21829/myb.2014.201173
Salomão, R. P., Favila, M. E., & González-Tokman, D. (2020). Spatial and temporal changes in the dung beetle diversity of a protected, but fragmented, landscape of the northernmost Neotropical rainforest. Ecological Indicators, 111, 105968. https://doi.org/10.1016/j.ecolind.2019.105968
Sands, B., & Wall, R. (2017). Dung beetles reduce livestock gastrointestinal parasite availability on pasture. Journal of Applied Ecology, 54, 1180–1189. https://doi.org/10.1111/1365-2664.12821
Schmera, D., Podani, J., & Legendre, P. (2020). What do beta diversity components reveal from presence-absence community data? Let us connect every indicator to an indicandum! Ecological Indicators, 117, 106540. https://doi.org/10.1016/j.ecolind.2020.106540
Scholtz, C. H., Davis, A. L. V., & Kryger, U. (2009). Evolutionary biology and conservation of dung beetles. Sofia, Bulgary: Pensoft Publishers.
Slade, E. M., Mann, D. J., Villanueva, J. F., & Lewis, O. T. (2007). Experimental evidence for the effects of dung beetle functional group richness and composition on ecosystem function in a tropical forest. Journal of Animal Ecology, 76, 1094–1104. https://doi.org/10.1111/j.1365-2656.2007.01296.x
Slade, E. M., Riutta, T., Roslin, T., & Tuomisto, H. L. (2016). The role of dung beetles in reducing greenhouse gas emissions from cattle farming. Scientific Reports, 6, 18140. https://doi.org/10.1038/srep18140
Solar, R. R., Barlow, J., Ferreira, J., Berenguer, E., Lees, A. C., Thomson, J. R. et al. (2015). How pervasive is biotic homogenization in human-modified tropical forest landscapes? Ecology Letters, 18, 1108–1118. https://doi.org/10.1111/ele.12494
Suggitt, A. J., Gillingham, P. K., Hill, J. K., Huntley, B., Kunin, W. E., Roy, D. B. et al. (2011). Habitat microclimates drive fine-scale variation in extreme temperatures. Oikos, 120, 1–8. https://doi.org/10.1111/j.1600-0706.2010.18270.x
Tatsumi, S., Iritani, R., & Cadotte, M. W. (2021). Temporal changes in spatial variation: partitioning the extinction and colonisation components of beta diversity. Ecology Letters, 24, 1063–1072. https://doi.org/10.1111/ele.13720
Tonkin, J. D., Bogan, M. T., Bonada, N., Rios-Touma, B., & Lytle, D. A. (2017). Seasonality and predictability shape temporal species diversity. Ecology, 98, 1201–1216. https://doi.org/10.1002/ecy.1761
UNESCO (United Nations Educational, Scientific and Cultural Organization). (2020). Los Tuxtlas Biosphere Reserve, Mexico. Retrieved on August 17, 2020. Available at: https://en.unesco.org/biosphere/lac/los-tuxtlas
Vega-Vela, V., Muñoz-Robles, C. A., Rodríguez-Luna, E., López-Acosta, J. C., & Serna-Lagunes, R. (2018). Analysis of landscape fragmentation in the Los Tuxtlas Biosphere Reserve, Veracruz, Mexico. Ecosistemas y Recursos Agropecuarios, 5, 227–238. https://doi.org/10.19136/era.a5n14.1442
Verdú, J. R., Lobo, J. M., Sánchez-Piñero, F., Gallego, B., Numa, C., Lumaret, J. P. et al. (2018). Ivermectin residues disrupt dung beetle diversity, soil properties and ecosystem functioning: An interdisciplinary field study. Science of the Total Environment, 618, 219–228. https://doi.org/10.1016/j.scitotenv.2017.10.331
Villéger, S., Mason, N. W. H., & Mouillot, D. (2008). New multidimensional functional diversity indices for a multifaceted framework in functional ecology. Ecology, 89, 2290–2301. https://doi.org/10.1890/07-1206.1
Villéger, S., Miranda, J. R., Hernandez, D. F., & Mouillot, D. (2012). Low functional β-diversity despite high taxonomic β-diversity among tropical estuarine fish communities. Plos One, 7, e40679. https://doi.org/10.1371/journal.pone.0040679
Zunino, M., & Halffter, G. (1997). Sobre Onthophagus Latreille, 1802 americanos (Coleoptera: Scarabaeidae: Scarabaeinae). Elytron, 11, 157–178.