ABSTRACT
Influence of Quaternary climate change on the potencial distribution of Atlantic Forest dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). The role of Cenozoic paleoclimatic changes in the distribution of dung beetles species from the Atlantic Forest (AF) remains poorly understood. We used ecological niche modeling under different scenarios (present, 6 ka, 21 ka, and 120 ka) to investigate how climatic oscillations during the Quaternary might have influenced the distribution of species endemic to this region. Models were built for five of the nine dung beetle species of the Dichotomius sericeus group: D. iannuzziae, D. irinus, D. laevicollis, D. schiffleri, and D. sericeus. The models of climatic suitability for D. irinus and D. laevicollis show a similar historical pattern in response to climate change but were divergent from D. iannuzziae, D. schiffleri, and D. sericeus. Dichotomius schiffleri is the species with the smallest area of potencial occurrence. Over time, the species probably remained limited to lowland AF areas on the Brazilian coast and, it is currently found preferentially in Restinga ecosystems along the coast. Regarding the potential distribution models at the present, D. iannuzziae, D. schiffleri, and D. sericeus have potential distributions similar to their realized distribution. This study shows that the historical distribution of the D. sericeus species group has been influenced by paleoclimatic changes that occurred in the AF over the last 120 ka.
Keywords:
Biogeography; Conservation; Distribution patterns; Insects; Quaternary climatic; scillations
Introduction
The Atlantic Forest (AF) domain is dated to approximately 60 million years ago, when there was an area climatically suitable for the formation and expansion of a tropical forest (Por, 1992Por, F.D., 1992. Sooretama: the Atlantic Rain Forest of Brazil. SPB Academic Publishing, Texas, 130 pp.). In the last thousands of years, oscillations in global climate and sea levels resulted in drastic changes in biodiversity distribution (Vanzolini and Williams, 1981Vanzolini, P.E., Williams, E.E., 1981. The vanishing refuge: a mechanism for ecogeographic speciation. Pap. Avulsos Zool. 34 (23), 251–255. http://doi.org/10.11606/0031-1049.1980.34.p251-255.
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Climate changes along the Last Glacial Maximum (LGM, around 21 thousand years ago) have been reflected in the evolutionary history of many taxa (Mustrangi and Patton, 1997Mustrangi, M.A., Patton, J.L., 1997. Phylogeography and Systematics of the Slender Mouse Opossum Marmosops (Marsupialia: Didelphidae). University of California Press, California, 70 pp.; Costa et al., 2003Costa, M.H., Botta, A., Cardille, J.A., 2003. Effects of large-scale changes in land cover on the discharge of the Tocantins River, Southeastern Amazonia. J. Hydrol. (Amst.) 283 (1–4), 206–217. http://doi.org/10.1016/S0022-1694(03)00267-1.
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The effects of different paleoclimatic events on AF-endemic invertebrate taxa are still poorly explored, especially concerning megadiverse groups such as insects of the order Coleoptera (Erwin, 1985Erwin, T.L., 1985. The taxon pulse: a general pattern of lineage radiation and extinction among carabid beetles. In: Ball, G.E. (Eds.), Taxonomy, Phylogeny, and Zoogeography of Beetles and Ants. Junk Publishers, Dordrecht, pp. 437–472.; Lü et al., 2020Lü, L., Cai, C.Y., Zhang, X., Newton, A.F., Thayer, M.K., Zhou, H.Z., 2020. Linking evolutionary mode to palaeoclimate change reveals rapid radiations of staphylinoid beetles in low-energy conditions. Curr. Zool. 66 (4), 435–444. http://doi.org/10.1093/cz/zoz053.
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). Understanding the space-time dynamics of the ecological niche occupied by these groups can provide valuable insights into the drivers of diversification along habitat transitions in the AF, and about the future of species under global climate change scenarios (Hoffmann and Sgrò, 2011Hoffmann, A.A., Sgrò, C.M., 2011. Climate change and evolutionary adaptation. Nature 470 (7335), 479–485. http://doi.org/10.1038/nature09670.
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Ecological niche modeling (ENM) is a technique used to predict environmental suitability for the occurrence of a particular species in a spatial area. For this purpose, data from the current distribution of the species and a set of environmental variables are used. This routine is widely employed as a way of predicting the potential distribution of species with diverse goals, including biological invasions (Peterson, 2011Peterson, A.T., 2011. Ecological niche conservatism: a time‐structured review of evidence. J. Biogeogr. 38 (5), 817–827. http://doi.org/10.1111/j.1365-2699.2010.02456.x.
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In a nutshell, species niche reconstruction has as main objectives: (i) to reconstruct the potential historical distribution (Yesson and Culham, 2006Yesson, C., Culham, A., 2006. Phyloclimatic modeling: combining phylogenetics and bioclimatic modeling. Syst. Biol. 55 (5), 785–802. http://doi.org/10.1080/1063515060081570.
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The dung beetles of the subfamily Scarabaeinae comprise 6.891 valid species grouped into 282 genera (Schoolmeesters, 2024Schoolmeesters, P., 2024. World Scarabaeidae Database. In: Bánki, O., Roskov, Y., Döring, M., Ower, G., Hernández Robles, D.R., Plata Corredor, C.A., Stjernegaard Jeppesen, T., Örn, A., Vandepitte, L., Hobern, D., Schalk, P., DeWalt, R.E., Ma, K., Miller, J., Orrell, T., Aalbu, R., Abbott, J., Adlard, R., Aedo, C.. (Eds.), Catalogue of Life Checklist (Version 2024-03-05). The Catalogue of Life Partnership, Amsterdam. http://doi.org/10.48580/dfz6w-38g.). In Brazil, 786 species have been recorded in 69 genera (Vaz-de-Mello, 2024Vaz-de-Mello, F.Z., 2024. Scarabaeidae. In: PNUD. Catálogo taxonômico da fauna do Brasil. PNUD. Available in: http://fauna.jbrj.gov.br/fauna/faunadobrasil/127498 (acessed 23 April 2024).
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). The restricted ecological niches of many species enable the use of dung beetles as environmental bioindicators or in ecological biogeographic studies. Cupello et al. (2023)Cupello, M., Silva, F.A.B., Vaz-de-Mello, F.Z., 2023. The Taxonomic Revolution of New World dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae). Front. Ecol. Evol. 11, 1168754. http://doi.org/10.3389/fevo.2023.1168754.
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stated that dung beetles have been one of the major taxa used as bioindicators during the past decades by ecologists. Despite being considered one of the major taxa for ecological studies in tropical biomes, only a couple of recent studies have been performed using ecological niche modeling to investigate how environmental and climatic suitability influence the distribution of Neotropical species (Moctezuma et al., 2021Moctezuma, V., Halffter, G., Lizardo, V., 2021. The Phanaeus tridens species group (Coleoptera: Scarabaeoidea): a dung beetle group with genital morphological stasis but a changing ecological niche. Acta Entomol. Mus. Natl. Pragae 61 (2), 447–482. http://doi.org/10.37520/aemnp.2021.025.
http://doi.org/10.37520/aemnp.2021.025...
; Cupello et al., 2022Cupello, M., Ribeiro-Costa, C.S., Vaz-de-Mello, F.Z., 2022. The evolution of Bolbites onitoides (Coleoptera: Scarabaeidae: Phanaeini): its phylogenetic significance, geographical polychromatism and the subspecies problem. Zool. J. Linn. Soc. 194 (3), 973–1034. http://doi.org/10.1093/zoolinnean/zlab015.
http://doi.org/10.1093/zoolinnean/zlab01...
; Lizardo et al., 2022Lizardo, V., Moctezuma, V., Escobar, F., 2022. Distribution, Regionalization, and Diversity of the dung beetle genus Phanaeus MacLeay (Coleoptera: Scarabaeidae) using Species Distribution Models. Zootaxa 5213 (5), 546–568. http://doi.org/10.11646/zootaxa.5213.5.4.
http://doi.org/10.11646/zootaxa.5213.5.4...
; Vieira et al., 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
; Moctezuma et al., 2024Moctezuma, V., de los Monteros, A.E., Halffter, G., 2024. Phylogenetic analyses of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) provide new insights into the Mexican Transition Zone theory. Zootaxa 5415 (4), 501–528. http://doi.org/10.11646/zootaxa.5415.4.1.
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).
The Dichotomius sericeus species group comprises nine known species distributed in Brazil, Paraguay, and Argentina (Vaz-de-Mello et al., 2001Vaz-de-Mello, F.Z., Louzada, J.N.C., Gavino, M., 2001. Nova espécie de Dichotomius Hope, 1838 (Coleoptera, Scarabaeidae) do Espírito Santo, Brasil. Rev. Bras. Entomol. 45 (2), 99–102.; Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
http://doi.org/10.11646/zootaxa.4277.4.3...
; Silva et al., 2020Silva, F.A.B., Moura, A.B.G., Araújo, J.F., Moura, R.C., 2020. Brazilian Atlantic rainforest endangered biodiversity: a new species of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4834 (3), 434–442. http://doi.org/10.11646/zootaxa.4834.3.6.
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). Its species live in AF and associated ecosystems such as Caatinga and Restinga (Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
; Vieira et al., 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
; Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
http://doi.org/10.11646/zootaxa.4277.4.3...
; Silva et al., 2020Silva, F.A.B., Moura, A.B.G., Araújo, J.F., Moura, R.C., 2020. Brazilian Atlantic rainforest endangered biodiversity: a new species of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4834 (3), 434–442. http://doi.org/10.11646/zootaxa.4834.3.6.
http://doi.org/10.11646/zootaxa.4834.3.6...
). Many of these ecosystems are threatened by fragmentation, defaunation, logging, and agricultural expansion (Halffter and Favila, 1993Halffter, G., Favila, M.E., 1993. The Scarabaeinae (Insecta: Coleoptera) an animal group for analysing, inventorying and monitoring biodeiversity in tropical rainforest and modified landscapes. Biol. Int. 27, 15–21.; Audino et al., 2014Audino, L.D., Louzada, J., Comita, L.S., 2014. Dung beetles as indicators of tropical forest restoration success: is it possible to recover species and functional diversity? Biol. Conserv. 169, 248–257. http://doi.org/10.1016/j.biocon.2013.11.023.
http://doi.org/10.1016/j.biocon.2013.11....
; Dirzo et al., 2014Dirzo, R., Young, H.S., Galetti, M., Ceballos, G., Isaac, N.J.B., Collen, B., 2014. Defaunation in the Anthropocene. Science 345 (6195), 401–406. http://doi.org/10.1126/science.1251817.
http://doi.org/10.1126/science.1251817...
; Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
, 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
, 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
). Some species of the D. sericeus group are, therefore, at imminent risk of extinction. For example, Dichotomius schiffleri Vaz-de-Mello, Gavino & Louzada, 2001 has its current geographic distribution limited to a narrow strip of Restinga on the Brazilian coast between the states of Pernambuco and Espírito Santo (Vieira et al., 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
) and, recently, D. valoisae Silva et al., 2020 was described from a small area of AF (Silva et al., 2020Silva, F.A.B., Moura, A.B.G., Araújo, J.F., Moura, R.C., 2020. Brazilian Atlantic rainforest endangered biodiversity: a new species of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4834 (3), 434–442. http://doi.org/10.11646/zootaxa.4834.3.6.
http://doi.org/10.11646/zootaxa.4834.3.6...
).
The species of these group are a dominant component in their communities, in addition, they are susceptible to being delimited by geographic or ecological barriers (Vieira et al., 2022bVieira, L., Costa, C., Vaz-de-Mello, F.Z., Louzada, J., 2022b. Riverine barrier hypothesis explains the structure of dung beetle communities in sand-dune forests. Acta Oecol. 115, 103835. http://doi.org/10.1016/j.actao.2022.103835.
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), rendering them a good model to test biogeographic hypotheses.
In this study, we built ecological niche models for species of the Dichotomius sericeus group in different climate periods of the present and past to verify how the climatic oscillations in the AF domain during the Quaternary influenced the species distribution. In addition, these ecological niche models can be used to verify sampling gaps along regions with high climatic suitability, something useful not only for basic sciences like biogeography and systematics but also applied ones such as conservation (Chefaoui et al., 2005Chefaoui, R.M., Hortal, J., Lobo, J.M., 2005. Potential distribution modelling, niche characterization and conservation status assessment using GIS tools: a case study of Iberian Copris species. Biol. Conserv. 122 (2), 327–338. http://doi.org/10.1016/j.biocon.2004.08.005.
http://doi.org/10.1016/j.biocon.2004.08....
; Lawler et al., 2011Lawler, J.J., Wiersma, Y.F., Huettmann, F., 2011. Using species distribution models for conservation planning and ecological forecasting. In: Drew, C.A., Wiersma, Y.F., Huettmann, F. (Eds.), Predictive Species and Habitat Modeling in Landscape Ecology. Springer, New York, pp. 271–290. http://doi.org/10.1007/978-1-4419-7390-0_14.
http://doi.org/10.1007/978-1-4419-7390-0...
).
Material and methods
Study area
All species studied here are limited to areas of the AF domain. This biogeographical unit encompasses different vegetation types, namely ombrophilous, deciduous, semi-deciduous, and Araucaria forests, as well as the Restinga and the high altitude fields. The AF domain extends from the eastern coast of South America to portions further inland, following the main courses of rivers and tributaries, and mountainous regions. Morrone et al. (2022)Morrone, J.J., Escalante, T., Rodríguez-Tapia, G., Carmona, A., Arana, M., Mercado-Gómez, J.D., 2022. Biogeographic regionalization of the Neotropical region: new map and shapefile. An. Acad. Bras. Cienc. 94 (1), e20211167. http://doi.org/10.1590/0001-3765202220211167.
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named this biogeographic unit “Parana dominion”.
Occurrence records
The records for each species analyzed were obtained from Valois et al. (2017)Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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(Figs. 1a-e). Each occurrence was obtained through label data from individuals examined during the taxonomic revision of the D. sericeus species group. The occurrence data were included individually (not transformed into presence cells). We built individual models only for species with more than ten known occurrence records: D. iannuzziae Valois, Vaz-de-Mello & Silva, 2017 (23 records), D. schiffleri (34), D. laevicollis (Felsche, 1901Felsche, C., 1901. Beschreibungen coprophager Scarabaeiden. Dtsch. Entomol. Z. 2, 135–155.) (11), D. sericeus (Harold, 1867Harold, E., 1867. Diagnosen neuer Coprophagen. Coleopterologische (2), 94–100.) (62), and D. irinus (Harold, 1867Harold, E., 1867. Diagnosen neuer Coprophagen. Coleopterologische (2), 94–100.) (29).
Known distribution of five species of the D. sericeus group: (a) Dichotomius iannuzziae Valois, Vaz-de-Mello & Silva, 2017. (b) Dichotomius irinus (Harold, 1867Harold, E., 1867. Diagnosen neuer Coprophagen. Coleopterologische (2), 94–100.). (c) Dichotomius laevicollis (Felsche, 1901Felsche, C., 1901. Beschreibungen coprophager Scarabaeiden. Dtsch. Entomol. Z. 2, 135–155.). (d) Dichotomius schiffleri Vaz-de-Mello, Gavino & Louzada, 2001. (e) Dichotomius sericeus (Harold, 1867Harold, E., 1867. Diagnosen neuer Coprophagen. Coleopterologische (2), 94–100.).
Setting the current and paleoclimatic variables
For the prediction of the historical distribution of the species, 19 current and paleobioclimatic variables available at the WorldClim website (Fick and Hijmans, 2017Fick, S.E., Hijmans, R.J., 2017. WorldClim 2: new 1km spatial resolution climate surfaces for global land areas. Int. J. Climatol. 37 (12), 4302–4315. http://doi.org/10.1002/joc.5086.
http://doi.org/10.1002/joc.5086...
) were selected. The selected historical clipping corresponds to four climate scenarios: present, mid-Holocene (6 ka), last glacial maximum ‒ LGM (21 ka), and last interglacial maximum ‒ LIG (120 ka). Paleoclimatic data were based on Atmosphere-Ocean-Global-Circulation-Models (AOGCM) Community Climate System Model v.3 (CCSM3) simulations. Paleoclimatic data from the LIG were based on Otto-Bliesner et al. (2006)Otto-Bliesner, B.L., Tomas, R., Brady, E.C., Ammann, C., Kothavala, Z., Clauzet, G., 2006. Climate sensitivity of moderate-and low-resolution versions of CCSM3 to preindustrial forcings. J. Clim. 19 (11), 2567–2583. http://doi.org/10.1175/JCLI3754.1.
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. All variables were in the WGS84 datum and were cut to the extent of Chacoan and Parana dominions (Morrone et al., 2022Morrone, J.J., Escalante, T., Rodríguez-Tapia, G., Carmona, A., Arana, M., Mercado-Gómez, J.D., 2022. Biogeographic regionalization of the Neotropical region: new map and shapefile. An. Acad. Bras. Cienc. 94 (1), e20211167. http://doi.org/10.1590/0001-3765202220211167.
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), with 2.5' Arc-resolution (~5 x 5 Km, in the Equator region). This extension was chosen as the background as it encompasses all known occurrences of the species and this is considered a potential area for the historical dispersal of the species, two background selection criteria discussed by Barve et al. (2011)Barve, N., Barve, V., Jiménez-Valverde, A., Lira-Noriega, A., Maher, S.P., Peterson, A.T., Soberón, J., Vilalobos, F., 2011. The crucial role of the accessible area in ecological niche modelling and species distribution modelling. Ecol. Modell. 222 (11), 1810–1819. http://doi.org/10.1016/j.ecolmodel.2011.02.011.
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.
The 19 bioclimatic (current climate scenario) and paleoclimatic (past climate scenario) variables available in WorldClim are correlated with each other. Therefore, a variable selection process becomes necessary as a way to reduce the collinearity of environmental data (Peterson et al., 2011Peterson, A.T., Soberón, J., Pearson, R.G., Anderson, R.P., Martínez-Meyer, E., Nakamura, M., Araújo, M.B., 2011. Ecological Niches and Geographic Distributions (MPB-49). Princeton University Press, Princeton, 314 pp. http://doi.org/10.23943/princeton/9780691136868.001.0001.
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; Varela et al., 2015Varela, S., Lima-Ribeiro, M.S., Terribile, L.C., 2015. A short guide to the climatic variables of the last glacial maximum for biogeographers. PLoS One 10 (6), e0129037. http://doi.org/10.1371/journal.pone.0129037.
http://doi.org/10.1371/journal.pone.0129...
). For that, we performed factor analysis using current bioclimatic variables through VariMax Rotation of the orthogonal axes (details in Sobral-Souza et al., 2015Sobral-Souza, T., Lima-Ribeiro, M.S., Solferini, V.N., 2015. Biogeography of Neotropical Rainforests: past connections between Amazon and Atlantic Forest detected by ecological niche modeling. Evol. Ecol. 29 (5), 643–655. http://doi.org/10.1007/s10682-015-9780-9.
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). In sequence, the following variables were selected: Mean Temperature of Warmest Quarter (BIO 10), Temperature Seasonality (BIO 04), Precipitation of Driest Quarter (BIO 17), and Mean Diurnal Range (BIO 02), which explain 87% of the climate variance in the spatial area of the study.
Modeling techniques
Currently, there are several algorithms available in the literature (Qiao et al., 2019Qiao, H., Feng, X., Escobar, L.E., Peterson, A.T., Soberón, J., Zhu, G., Papeş, M., 2019. An evaluation of transferability of ecological niche models. Ecography 42 (3), 521–534. http://doi.org/10.1111/ecog.03986.
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), such as presence-only, presence and background, and presence and absence algorithms. Each tends to estimate a different distribution based on different niche assumptions (Jiménez-Valverde et al., 2008Jiménez-Valverde, A., Lobo, J.M., Hortal, J., 2008. Not as good as they seem: the importance of concepts in species distribution modelling. Divers. Distrib. 14 (6), 885–890. http://doi.org/10.1111/j.1472-4642.2008.00496.x.
http://doi.org/10.1111/j.1472-4642.2008....
). Therefore, there is no 100% efficient algorithm (Qiao et al., 2015Qiao, H., Lin, C., Jiang, Z., Ji, L., 2015. Marble algorithm: a solution to estimating ecological niches from presence-only records. Sci. Rep. 5 (1), 1–10. http://doi.org/10.1038/srep14232.
http://doi.org/10.1038/srep14232...
) and it becomes necessary to use several algorithms simultaneously.
Four algorithms were selected to construct the models: two that deal only with presence data, Bioclim (Nix, 1986Nix, H.A., 1986. A biogeographic analysis of Australian elapid snakes. In: Longmore, R. (Eds.), Atlas of Elapid Snakes of Australia: Australian Flora and Fauna. CSIRO Publishing, Canberra, pp. 4–15. (series 7).) and Gower (Carpenter et al., 1993Carpenter, G., Gillison, A.N., Winter, J., 1993. DOMAIN: a flexible modelling procedure for mapping potential distributions of plants and animals. Biodivers. Conserv. 2 (6), 667–680. http://doi.org/10.1007/BF00051966.
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), and two of pseudoabsence, Maximum Entropy ‒ Maxent (Phillips and Dudík, 2008Phillips, S.J., Dudík, M., 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31 (2), 161–175. http://doi.org/10.1111/j.0906-7590.2008.5203.x.
http://doi.org/10.1111/j.0906-7590.2008....
) and Support Vector Machines – SVM (Tax and Duin, 2004Tax, D.M., Duin, R.P., 2004. Support vector data description. Mach. Learn. 54 (1), 45–66. http://doi.org/10.1023/B:MACH.0000008084.60811.49.
http://doi.org/10.1023/B:MACH.0000008084...
). We did not use presence-absence algorithms as true absence points are not known for the studied species. Species occurrence data were randomly divided into 70% for training and 30% for testing. The bootstrap technique was used to reduce the autocorrelation between these data (Peterson et al., 2011Peterson, A.T., Soberón, J., Pearson, R.G., Anderson, R.P., Martínez-Meyer, E., Nakamura, M., Araújo, M.B., 2011. Ecological Niches and Geographic Distributions (MPB-49). Princeton University Press, Princeton, 314 pp. http://doi.org/10.23943/princeton/9780691136868.001.0001.
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), opting for 10 sets of data randomization for each species within each climate scenario. The models were built for four climate scenarios: present, 6 ka, 21 ka, and 120 ka. In total, 160 models were generated (10 randomizations; 4 algorithms; 4 climate scenarios) for each species. In sequence, we established cut-off thresholds for each model to transform them into presence-absence data. The models were evaluated using True Skill Statistic (TSS, Allouche et al., 2006Allouche, O., Tsoar, A., Kadmon, R., 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43 (6), 1223–1232. http://doi.org/10.1111/j.1365-2664.2006.01214.x.
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). The TSS values vary from -1 to 1, where negative values or close to 0 correspond to models with low accuracy, indicating that they do not differ statistically from randomly generated models. Values close to 1 correspond to excellent models. However, values above 0.5 are still considered suitable (Allouche et al., 2006Allouche, O., Tsoar, A., Kadmon, R., 2006. Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J. Appl. Ecol. 43 (6), 1223–1232. http://doi.org/10.1111/j.1365-2664.2006.01214.x.
http://doi.org/10.1111/j.1365-2664.2006....
).
The suitability maps of each species were obtained using the ensembles forecasting technique (Araújo and New, 2007Araújo, M.B., New, M., 2007. Ensemble forecasting of species distributions. Trends Ecol. Evol. 22 (1), 42–47. http://doi.org/10.1016/j.tree.2006.09.010.
http://doi.org/10.1016/j.tree.2006.09.01...
). This technique enabled the concatenation of the 10 maps produced by each of the 4 algorithms. In sequence, it gathered the 4 maps produced by each algorithm. The 40 maps resulting from this procedure have suitability values ranging from 0‒40. These values demonstrate the frequency with which the species was predicted for each cell.
Results
The niche models provided reliable predictions in all used algorithms (Table 1), except for the mean TSS value for the models generated in Bioclim for D. laevicollis (0.33 ± 0.22). All other models generated for each species reached mean values above 0.5 for all algorithms.
Mean and Standart deviation (SD) values of True Skill Statistic (TSS) for all combinations of algorithms for each generated model.
The models generated for D. iannuzziae in the LIG (120 ka) indicate continuous areas of climate suitability along the northeastern coast of Brazil (Fig. 2a). This species had the potential distribution areas retracted and fragmented during the LGM (21 ka). The climate suitability areas were restricted to small and isolated portions along the northeastern coastline that would have behaved as refuges (Fig. 2b). In the Holocene (6 ka), the climate suitability areas for the species would expand again, potentially reconnecting disjunct populations (Fig. 2c). At present, the species has a broad potential distribution (Fig. 2d). These supposed recently colonized areas and the areas that would have been permanently inhabited can be validated in future molecular studies. However, the climate suitability areas for D. iannuzziae were always restricted to northeastern Brazil within the entire time frame analyzed (Figs. 2a-d).
Ensembles Forecasting Models for Dichotomius iannuzziae in four historical climate scenarios: (a) 120ka. (b) 21ka. (c) 6ka. (d) Present. Colors represent different degrees of climatic suitability (red: high suitability, blue: low suitability).
In general, D. irinus presents a historical pattern of climate suitability areas different from D. iannuzziae. At 120 ka, the species had disjunct climate suitability areas (i - one in northeastern Brazil, from the coast to inland portions; ii - one on the southeastern coast; iii - four disjunct areas inland along a northeastern/southwestern axis) (Fig. 3a). During the LGM, the potential climate areas were concentrated in northeastern Brazil, both on the coast and inland (Fig. 3b). Since then, the potential areas have expanded along the southeastern coast and inland areas of AF (Figs. 3c-d).
Ensembles Forecasting Models for Dichotomius irinus in four historical climate scenarios: (a) 120ka. (b) 21ka. (c) 6ka. (d) Present. Colors represent different degrees of climatic suitability (red: high suitability, blue: low suitability).
The historical patterns of the potential areas of D. laevicollis are similar to those of D. irinus. These two species presented a higher climate suitability in isolated refuges in the northeastern, southeastern coast, and inland AF in 120 ka (Figs. 3a, 4a). Dichotomius laevicollis also showed the same pattern of displacement to the northeastern during the LGM, and had its potential climatically favorable areas expanded into the AF from 6 ka to the present (Figs. 4c-d). However, concerning the previous species, D. laevicollis presents more extensive and continuous areas, besides a few changes in its climate suitability areas over time, showing greater tolerance to historical climate changes (Figs. 4a-d).
Ensembles Forecasting Models for Dichotomius laevicollis in four historical climate scenarios: (a) 120ka. (b) 21ka. (c) 6ka. (d) Present. Colors represent different degrees of climatic suitability (red: high suitability, blue: low suitability).
Dichotomius schiffleri has the smallest area of climate suitability (Figs. 5a-d). Over time, the species probably remained limited to lowland AF areas on the Brazilian coast. It is currently found preferentially in Restinga ecosystems along the coast. At 21 ka, the climate suitability areas became greatly reduced (Fig. 5b).
Ensembles Forecasting Models for Dichotomius schiffleri in four historical climate scenarios: (a) 120ka. (b) 21ka. (c) 6ka. (d) Present. Colors represent different degrees of climatic suitability (red: high suitability, blue: low suitability).
Dichotomius sericeus has the most extensive areas of climatic suitability (Figs. 6a-d). The species is currently recorded in the southeastern portion of the continent, from the interior highland forests to the coastal areas (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Fig. 1e). Climate changes during the LGM would have reduced its areas of climatic suitability and at the same time promoted an expansion along a narrow strip across the Atlantic coast towards the northeastern region of Brazil (Fig. 6b). Over the last 6 ka, suitable areas became mainly concentrated in southern and southeastern Brazilian AF, reaching Argentina, Paraguay, and portions of the Bolivian Chaco through AF incursions (Figs. 6c-d).
Ensembles Forecasting Models for Dichotomius sericeus in four historical climate scenarios: (a) 120ka. (b) 21ka. (c) 6ka. (d) Present. Colors represent different degrees of climatic suitability (red: high suitability, blue: low suitability).
Discussion
Herein, we studied how climatic oscillations throughout the Quaternary have influenced the potential distribution based on climate for dung beetles endemic to the AF. The Dichotomius sericeus species group currently has a wide occurrence in areas of the AF Domain (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Figs. 1a-e). However, the historical distribution models built for the analyzed species indicate that climatic oscillations during the Quaternary influenced the distribution patterns differently over time, with some retractions and/or expansions in areas of climatic suitability (Figs. 2-6).
The disjunct climatically suitable areas observed in some models, mainly in the 120 ka (Figs. 3a, 4a) and 21 ka models (Figs. 2b, 5b), suggests that climate oscillations may have contributed to diversification processes within the group through geographic isolation of lineages. According to the refugia hypothesis (Haffer, 1969Haffer, J., 1969. Speciation in Amazonian Forest Birds. Science 165 (3889), 131–137. http://doi.org/10.1126/science.165.3889.131.
http://doi.org/10.1126/science.165.3889....
; Haffer and Prance, 2002Haffer, J., Prance, G.T., 2002. Impulsos climáticos da evolução na Amazônia durante o Cenozóico: sobre a teoria dos Refúgios da diferenciação biótica. Estud. Av. 16 (46), 175–206. https://doi.org/10.1590/S0103-40142002000300014.
https://doi.org/10.1590/S0103-4014200200...
, cyclical climate changes in the Pleistocene drove speciation processes by promoting contraction, fragmentation, expansion, and reconnection of tropical forests.
The combination of distribution data and phylogenetic information can provide robust hypotheses to understand diversification processes and biogeographic patterns in tropical forests (Batalha-Filho et al., 2013Batalha-Filho, H., Fjeldså, J., Pierre-Henri, F., Miyaki, C.Y., 2013. Connections between the Atlantic and the Amazonian forest avifaunas represent distinct historical events. J. Ornithol. 154 (1), 41–50. http://doi.org/10.1007/s10336-012-0866-7.
http://doi.org/10.1007/s10336-012-0866-7...
; Mascarenhas et al., 2019Mascarenhas, R., Miyaki, C.Y., Dobrovolski, R., Batalha-Filho, H., 2019. Late Pleistocene climate change shapes population divergence of an Atlantic Forest passerine: a model-based phylogeographic hypothesis test. J. Ornithol. 160 (3), 733–748. http://doi.org/10.1007/s10336-019-01650-1.
http://doi.org/10.1007/s10336-019-01650-...
; Silveira et al., 2019Silveira, M.H.B., Mascarenhas, R., Cardoso, D., Batalha-Filho, H., 2019. Pleistocene climatic instability drove the historical distribution of forest islands in the northeastern Brazilian Atlantic Forest. Palaeogeogr. Palaeoclimatol. Palaeoecol. 527, 67–76. http://doi.org/10.1016/j.palaeo.2019.04.028.
http://doi.org/10.1016/j.palaeo.2019.04....
; Sheu et al., 2020Sheu, Y., Zurano, J.P., Ribeiro‐Junior, M.A., Ávila‐Pires, T.C., Rodrigues, M.T., Colli, G.R., Werneck, F.P., 2020. The combined role of dispersal and niche evolution in the diversification of Neotropical lizards. Ecol. Evol. 10 (5), 2608–2625. http://doi.org/10.1002/ece3.6091.
http://doi.org/10.1002/ece3.6091...
). Unfortunately, there are still no molecular dating or phylogenetic analysis published for the D. sericeus species group. These information may be helpful to understand whether the Quaternary climate changes had influenced the species ranges and their respective populational sizes, or if were also responsible for speciation processes within the group.
During the Quaternary period, some species exhibited distinct responses to climate changes. Dichotomius irinus and D. laevicollis had a similar historical pattern (Figs. 3a-d, 4a-d). At the same time, they were distinct from D. iannuzziae, D. schiffleri, and D. sericeus (Figs. 2a-d, 5a-d, 6a-d). In 120 ka, the climatically suitable areas of those two species were quite fragmented, with a high suitability in isolated refuges in northeastern Brazil, the southeastern coast, and inland AF (Figs. 3a, 4a). Meanwhile, the other three species had a more continuous suitable areas in this period (Figs. 2a, 5a, 6a). During the LGM, the areas of climate suitability of D. irinus and D. laevicolis also exhibited the same pattern of displacement into northeastern Brazil, and expansion to inland AF from 6 ka to the present (Figs. 3b, 4b). On the other hand, other species showed retraction and fragmentation into their range (Figs. 2b, 5b, 6b) instead of changing their areas of climatic suitability as mentioned for D. irinus and D. laevicollis.
The regional response to climate change among the studied species may be associated with differences in their altitudinal ranges. According to Batalha-Filho et al. (2014)Batalha-Filho, H., Pessoa, R.O., Pierre-Henri, F., Fjeldså, J., Irestedt, M., Ericson, P.G.P., Silveira, L.F., Miyaki, C.Y., 2014. Phylogeny and historical biogeography of gnateaters (Passeriformes, Conopophagidae) in the South America forests. Mol. Phylogenet. Evol. 79, 422–432. http://doi.org/10.1016/j.ympev.2014.06.025.
http://doi.org/10.1016/j.ympev.2014.06.0...
, the lowlands and upland regions of the AF seem to have been differently affected by the Quaternary climate change. In general, species from lowland forests were strongly influenced by the effect of the Last Glacial Maximum (Carnaval et al., 2009Carnaval, A.C., Hickerson, M.J., Haddad, C.F.B., Rodrigues, M.T., Moritz, C., 2009. Stability predicts genetic diversity in the Brazilian Atlantic Forest hotspot. Science 323 (5915), 785–789. http://doi.org/10.1126/science.1166955.
http://doi.org/10.1126/science.1166955...
), while some highland species were not (Amaro et al., 2012Amaro, R.C., Rodrigues, M.T., Yonenaga-Yassuda, Y., Carnaval, A.C., 2012. Demographic processes in the montane Atlantic rainforest: molecular and cytogenetic evidence from the endemic frog Proceratophrys boiei. Mol. Phylogenet. Evol. 62 (3), 880–888. http://doi.org/10.1016/j.ympev.2011.11.004.
http://doi.org/10.1016/j.ympev.2011.11.0...
; Batalha-Filho et al., 2012Batalha-Filho, H., Cabanne, G.S., Miyaki, C.Y., 2012. Phylogeography of an Atlantic Forest passerine reveals demographic stability through the last glacial maximum. Mol. Phylogenet. Evol. 65 (3), 892–902. http://doi.org/10.1016/j.ympev.2012.08.010.
http://doi.org/10.1016/j.ympev.2012.08.0...
). Individuals of D. irinus and D. laevicollis are generally found in moderate elevations and inland plateau regions, while D. schiffleri, for instance, is currently found at low elevations close to sea level (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Figs. 1b-d). This latter species might have suffered a drastic reduction in areas of climatic suitability during the LGM (Fig. 5b).
Except for D. sericeus, which exhibits climatically suitable areas in the southern and southeastern AF (Figs. 6a-d), all other species have climatically suitable areas along lower latitudes. D. sericeus is a habitat generalist species, and its geographic distribution comprises intermediate latitudes of AF from Argentina and Paraguay to southern and southeastern Brazil (Fig. 1e) (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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). The species may have expanded its distribution northwards in the LGM through a narrow strip along the coast of Brazil to the northeastern region (Fig. 6b). The climate during this period would have provided milder temperatures and favorable conditions for its establishment in that region.
The potential distribution models at the present exhibits similar potential distributions for D. iannuzziae, D. schiffleri, and D. sericeus (Figs. 2d, 5d, 6d) compared to their current known ranges (Figs. 1a, d, e). D. iannuzziae occurrence goes from northern Pernambuco to eastern Minas Gerais (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
http://doi.org/10.11646/zootaxa.4277.4.3...
; Araújo et al., 2020Araújo, J.F., Silva, F.A.B., de Moura, R.D.C., 2020. New records of relictual populations of dung beetle species (Coleoptera, Scarabaeidae) in the Atlantic Forest of the Brazilian Northeast. Check List 16 (5), 1289–1303. http://doi.org/10.15560/16.5.1289.
http://doi.org/10.15560/16.5.1289...
) (Fig. 1a); in D. schiffleri it goes from the southern coast of Pernambuco to the north coast of Espírito Santo (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Fig. 1d); and in D. sericeus it stretches along wide portions in southern and southeastern Brazil, reaching Argentina and Paraguay by the AF incursions through main rivers and tributaries (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Fig. 1e).
The models for D. irinus and D. laevicollis indicate that the inland AF in northeastern Brazil has favorable climatic conditions for these species maintenance, as well as some isolated parts of the Brazilian central plateau (Figs. 3d, 4d). However, these species have known distributions more restricted. Dichotomius irinus was only recorded from northern Bahia to Rio de Janeiro (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Fig. 1b), and D. laevicollis from southern Bahia to Rio de Janeiro, through Espírito Santo and the central and eastern portions of Minas Gerais (Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
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) (Fig. 1c). Although the models have indicated climatically suitable areas in inland northeastern Brazil, we believe the absence of records for these two species in northern Bahia is not due to sampling gaps. Several collections of dung beetles have already been carried out in different ecosystems of the northeastern region (Costa et al., 2009Costa, C.M.Q.D., Silva, F.A.B., Farias, Â.I.D., de Moura, R.C., 2009. Diversidade de Scarabaeinae (Coleoptera, Scarabaeidae) coletados com armadilha de interceptação de vôo no refúgio ecológico Charles Darwin, Igarassu-PE, Brasil. Rev. Bras. Entomol. 53 (1), 88–94. http://doi.org/10.1590/S0085-56262009000100021.
http://doi.org/10.1590/S0085-56262009000...
; Silva et al., 2010Silva, F.A.B., Costa, C.M.Q., Moura, R.C., Farias, A.I., 2010. Study of the dung beetle (Coleoptera: Scarabaeidae) community at two sites: Atlantic forest and clear-cut, Pernambuco, Brazil. Environ. Entomol. 39 (2), 359–367. http://doi.org/10.1603/EN09180.
http://doi.org/10.1603/EN09180...
; Barretto et al., 2021Barretto, J., da Cunha, J.C.S., Silva, F., Moura, R.C., 2021. Dung beetle communities of altitudinal Atlantic forest remnants: diversity and composition. Int. J. Trop. Insect Sci. 41 (4), 2873–2881. http://doi.org/10.1007/s42690-021-00471-1.
http://doi.org/10.1007/s42690-021-00471-...
). Therefore, we believe that historical and/or ecological aspects of biogeography, such as geographic or ecological barriers, can better explain these distribution patterns. For example, the greatest species richness of the group is found in northeastern Brazil; such diversity may mean that all available niches for medium-sized borrowers have already been filled there. Competitive exclusion from these native, locally adapted species might, in turn, have prevented both D. irinus and D. laevicollis from dispersing and occupying the region.
As mentioned, the current distribution of species richness is not homogeneous along the AF. The northeastern region has several regional endemics and different phytophysiognomies, such as dense ombrophylous forest, open ombrophylous forest, submontane semideciduous seasonal forest, montane semideciduous seasonal forest, and associated ecosystems, such as mangroves and restingas, which provide varied ecological niches for these species. Eight out of the nine known species of the group currently occupy the AF domain in northeastern Brazil (Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
; Vieira et al., 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
; Valois et al., 2017Valois, M.C., Vaz-de-Mello, F.Z., Silva, F.A., 2017. Taxonomic revision of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4277 (4), 503–530. http://doi.org/10.11646/zootaxa.4277.4.3.
http://doi.org/10.11646/zootaxa.4277.4.3...
; Araújo et al., 2020Araújo, J.F., Silva, F.A.B., de Moura, R.D.C., 2020. New records of relictual populations of dung beetle species (Coleoptera, Scarabaeidae) in the Atlantic Forest of the Brazilian Northeast. Check List 16 (5), 1289–1303. http://doi.org/10.15560/16.5.1289.
http://doi.org/10.15560/16.5.1289...
; Silva et al., 2020Silva, F.A.B., Moura, A.B.G., Araújo, J.F., Moura, R.C., 2020. Brazilian Atlantic rainforest endangered biodiversity: a new species of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4834 (3), 434–442. http://doi.org/10.11646/zootaxa.4834.3.6.
http://doi.org/10.11646/zootaxa.4834.3.6...
). Two of those species, D. schiffleri and D. valoisae, are already recognized as threatened (Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
; Vieira et al., 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
; Silva et al., 2020Silva, F.A.B., Moura, A.B.G., Araújo, J.F., Moura, R.C., 2020. Brazilian Atlantic rainforest endangered biodiversity: a new species of the Dichotomius sericeus (Harold, 1867) species group (Coleoptera: Scarabaeidae: Scarabaeinae). Zootaxa 4834 (3), 434–442. http://doi.org/10.11646/zootaxa.4834.3.6.
http://doi.org/10.11646/zootaxa.4834.3.6...
). In addition, northeastern Brazil has the most endangered AF remnants in the country. This region has only about 2.21% of its original coverage reduced to small and isolated fragments, some smaller than 10 ha (Tabarelli et al., 2006Tabarelli, M., Melo, M.D.V.C., Lira, O.C., 2006. A Mata Atlântica do Nordeste. In: Campanili, M., Prochnow, M. (Eds.), Mata Atlântica - uma rede pela floresta. RMA, Brasília, pp. 1–17.).
Dichotomius schiffleri probably experienced populational bottlenecks that may have reduced genetic variability since at 21 ka the climate suitability areas became greatly reduced (Fig. 5b). It has its current geographic distribution limited to a narrow strip of the Brazilian coast (Vieira et al., 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
; Vieira et al., 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
) (Fig. 1d). Individuals are found usually inhabiting restinga ecosystems between the states of Pernambuco and Espírito Santo. Restinga refers to a mosaic of different coastal vegetation types, ranging from open scrubs to forests. These ecosystems have undergone an intense transformation since European colonization (Lacerda et al., 1984Lacerda, L.D., Araujo, D.S.D., Cerqueira, R., Turcq, B., 1984. Restingas: origem e estrutura no Brasil. Universidade Federal Fluminense, Rio de Janeiro.). Most of restinga areas are threatened by residential development, fire, and wood exploitation (Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
, 2011Vieira, L., Louzada, J.N.C., Vaz-de-Mello, F.Z., Lopes, P.P., Silva, F.A.B., 2011. New records, threatens and conservation status for Dichotomius schiffleri Vaz-de-Mello, Louzada & Gavino (Coleoptera: Scarabaeidae): an endangered dung beetle species from Brazilian atlantic forest ecosystems. Neotrop. Entomol. 40 (2), 282–284. http://doi.org/10.1590/S1519-566X2011000200020.
http://doi.org/10.1590/S1519-566X2011000...
, 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
). Even in the face of this ongoing habitat loss, it has not been adequately prioritized in most conservation strategies due to its low levels of faunal and flora endemism (Vieira et al., 2008Vieira, L., Louzada, J.N.C., Spector, S., 2008. Effects of degradation and replacement of southern Brazilian coastal sandy vegetation on the dung beetles (Coleoptera: scarabaeidae). Biotropica 40 (6), 719–727. http://doi.org/10.1111/j.1744-7429.2008.00432.x.
http://doi.org/10.1111/j.1744-7429.2008....
). The few protected areas that have been created were established in disturbed fragments after habitat loss had already occurred. The extirpation of restinga patches brings on colonization by cerrado-adapted and generalist species of dung beetles from other ecoregions, which may lead to local species extinctions (Vieira et al., 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
). Historical climate changes need to be investigated to better understand why forest dung beetle species are sensitive to microclimate changes and habitat modification.
The present study highlights the influence of the historical climate scenarios on forest dung beetle species in tropical forests. Climate suitability of dung beetle species is an issue not frequently addressed in research, despite the urgent need for species distribution data under a scenario of ongoing climate change (Lobo and Davis, 1999Lobo, J.M., Davis, A.L.V., 1999. An intercontinental comparison of dung beetle diversity between two Mediterranean-climatic regions: local versus regional and historical influences. Divers. Distrib. 5 (3), 91–103. http://doi.org/10.1046/j.1472-4642.1999.00039.x.
http://doi.org/10.1046/j.1472-4642.1999....
; Martín-Piera, 2001Martín-Piera, F., 2001. Area networks for conserving Iberian insects: a case study of dung beetles (Col., Scarabaeoidea). J. Insect Conserv. 5 (4), 233–252. http://doi.org/10.1023/A:1013306929014.
http://doi.org/10.1023/A:1013306929014...
; Lobo and Martín-Piera, 2002Lobo, J.M., Martín-Piera, F., 2002. Searching for a predictive model for species richness of Iberian dung beetle based on spatial and environmental variables. Conserv. Biol. 16 (1), 158–173. http://doi.org/10.1046/j.1523-1739.2002.00211.x.
http://doi.org/10.1046/j.1523-1739.2002....
; Chefaoui et al., 2005Chefaoui, R.M., Hortal, J., Lobo, J.M., 2005. Potential distribution modelling, niche characterization and conservation status assessment using GIS tools: a case study of Iberian Copris species. Biol. Conserv. 122 (2), 327–338. http://doi.org/10.1016/j.biocon.2004.08.005.
http://doi.org/10.1016/j.biocon.2004.08....
; Dortel et al., 2013Dortel, E., Thuiller, W., Lobo, J.M., Bohbot, H., Lumaret, J.P., Jay-Robert, P., 2013. Potential effects of climate change on the distribution of Scarabaeidae dung beetles in Western Europe. J. Insect Conserv. 17 (5), 1059–1070. http://doi.org/10.1007/s10841-013-9590-8.
http://doi.org/10.1007/s10841-013-9590-8...
; Vieira et al., 2022bVieira, L., Costa, C., Vaz-de-Mello, F.Z., Louzada, J., 2022b. Riverine barrier hypothesis explains the structure of dung beetle communities in sand-dune forests. Acta Oecol. 115, 103835. http://doi.org/10.1016/j.actao.2022.103835.
http://doi.org/10.1016/j.actao.2022.1038...
). Some recent studies that have addressed climate suitability in Neotropical fauna of dung beetles provided new insights into the Mexican Transition Zone theory (Moctezuma et al., 2024Moctezuma, V., de los Monteros, A.E., Halffter, G., 2024. Phylogenetic analyses of the subfamily Scarabaeinae (Coleoptera: Scarabaeidae) provide new insights into the Mexican Transition Zone theory. Zootaxa 5415 (4), 501–528. http://doi.org/10.11646/zootaxa.5415.4.1.
http://doi.org/10.11646/zootaxa.5415.4.1...
), the effects of climate changes on the spatial distribution of endangered dung beetles (Vieira et al., 2022aVieira, L., Sobral-Souza, T., Spector, S., Vaz-de-Mello, F.Z., Costa, C.M.Q., Louzada, J., 2022a. Synergistic effects of climate and human-induced landscape changes on the spatial distribution of an endangered dung beetle. J. Insect Conserv. 26 (2), 315–326. http://doi.org/10.1007/s10841-022-00388-1.
http://doi.org/10.1007/s10841-022-00388-...
), and the use of species distribution models to describe dung beetle species richness or to test their diversification patterns (Moctezuma et al., 2021Moctezuma, V., Halffter, G., Lizardo, V., 2021. The Phanaeus tridens species group (Coleoptera: Scarabaeoidea): a dung beetle group with genital morphological stasis but a changing ecological niche. Acta Entomol. Mus. Natl. Pragae 61 (2), 447–482. http://doi.org/10.37520/aemnp.2021.025.
http://doi.org/10.37520/aemnp.2021.025...
; Cupello et al., 2022Cupello, M., Ribeiro-Costa, C.S., Vaz-de-Mello, F.Z., 2022. The evolution of Bolbites onitoides (Coleoptera: Scarabaeidae: Phanaeini): its phylogenetic significance, geographical polychromatism and the subspecies problem. Zool. J. Linn. Soc. 194 (3), 973–1034. http://doi.org/10.1093/zoolinnean/zlab015.
http://doi.org/10.1093/zoolinnean/zlab01...
; Lizardo et al., 2022Lizardo, V., Moctezuma, V., Escobar, F., 2022. Distribution, Regionalization, and Diversity of the dung beetle genus Phanaeus MacLeay (Coleoptera: Scarabaeidae) using Species Distribution Models. Zootaxa 5213 (5), 546–568. http://doi.org/10.11646/zootaxa.5213.5.4.
http://doi.org/10.11646/zootaxa.5213.5.4...
). Hence, we reinforce that past climate patterns must be addressed to understand the present and predict the future patterns of dung beetle species distributions to provide reliable data for conservation purposes.
The historical distribution of the D. sericeus dung beetles species group has been influenced by paleoclimatic changes that occurred in the AF over the last 120 ka. These species are sensitive to climate change and, due to the strong habitat restrictions of some species such as D. schiffleri, they may be considered endangered. The paleoclimatic models might be integrated with models of ancestral area reconstruction to test diversification hypotheses in the AF. This approach connects hypotheses of historical and ecological biogeography, providing subsidies to understanding patterns of diversification and species richness by considering the biogeographic history of species and clades that give rise to these patterns.
Acknowledgments
Our special thanks are due to Mario Cupello for his valuable suggestions on the text of the manuscript. We also thank CNPq for providing research grants to Fernando Silva (444020/2014-4). Fernando Silva is a CNPq PQ2 fellow.
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Publication Dates
-
Publication in this collection
16 Aug 2024 -
Date of issue
2024
History
-
Received
24 Feb 2024 -
Accepted
09 June 2024