Conservation status and natural history of Ctenomys, tuco-tucos in Bolivia

Scott Lyell Gardner, Sebastian Botero-Cañola, Enzo Aliaga- Rossel, Altangerel Tsogtsaikhan Dursahinhan, Jorge Salazar-Bravo

Resumen


The genus Ctenomys consists of about 70 species and in addition to the Geomyidae of the Nearctic, Neotropical tuco-tucos represent a well-documented case of diversification in the subterranean biotype. Here we will: i) Provide an updated summary of the natural history of the 12 species of extant tuco-tucos from Bolivia; ii) Update information on distributions of each species; and iii) Using ecological niche modeling, evaluate recent and projected habitat transformation or habitat degradation within the known range of each species to provide a preliminary assessment of the preservation or conservation status of ctenomyids within Bolivia.  We follow Gardner et al. (2014) and combine species summaries with both updated published and new data to compile a complete list of known extant species of tuco-tucos from Bolivia.  Occurrence data for Ctenomys in Bolivia and surrounding areas were extracted from the database Arctos and GBIF.  All individual specimen-based locality records were checked and georeferenced by referring to original museum collection records. We created species distribution models for the species with enough locality records using climate and soil data, while for the rest of the species we estimated the ranges based on the known occurrence localities. Finally, we quantified the amount of large-scale habitat conversion occurring within each species range, as well as the potential effect of climatic change on species distribution.  Here we present information regarding the biology of tuco-tuco (Ctenomys) species known to occur in Bolivia, including unpublished natural history data such as habitat association, interactions and activity patterns gathered by the authors through extensive field work. Besides this, we estimated the current distribution of Ctenomys species, quantified large-scale habitat transformation within each species range and assessed the potential effect of climatic change on five tuco-tuco species. We found that the habitats within the ranges of C. boliviensis and C. steinbachi have experienced significant land-cover conversions in recent years.  We also show that C. opimus, as well as the above mentioned species are expected to undergo range contractions resulting from climatic change by 2070.  Our review shows that there is a dearth of information regarding natural history, taxonomy and distribution for many Bolivian tuco-tuco species. Nonetheless, the information presented here can be a tool for directing and focusing field studies of these species. This is of great importance if we take into account that most of the Bolivian tuco-tucos are subject to one or several conservation/preservation threats.  These include: Habitat destruction via land use or climatic changes in conjunction with geographic ranges of Ctenomys that are small in areal extent and which in many cases are not adequately covered by protected areas.


Palabras clave


Bolivia; Caviomorpha; climate change; Ctenomyidae; Ctenomys; Hystricomorpha; land use change; natural history; species distribution model; subterranean rodents.

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Referencias


AIELLO-LAMMENS, M. E., R. A. BORIA, A. RADOSAVLJEVIC, B. VILELA, AND R.P. ANDERSON. 2015. spThin: an R package for spatial thinning of species occurrence records for use in ecological niche models. Ecography 38: 541–545.

ANDERSON, S., T. L. YATES, AND J. A. COOK. 1987. Notes on Bolivian mammals 4: the genus Ctenomys (Rodentia: Ctenomyidae) in the eastern lowlands. American Museum Novitates 2891:1-20.

ANDERSON, S. 1997. Mammals of Bolivia: taxonomy and distribution. Bulletin of the AMNH 231 pp.

ASHE, J. S., R. M. TIMM, AND M. H. GALLARDO. 1996. Systematics, distribution, and host specificity of Edrabius fauvel (Insecta: Coleoptera: Staphylinidae). Proceedings of the Biological Society of Washington 109:731-743.

BARVE, N., V. BARVE, A. JIMÉNEZ-VALVERDE, A. LIRA-NORIEGA, S.P. MAHER, A.T. PETERSON, J. SOBERÓN, AND F. VILLALOBOS. 2011. The crucial role of the accessible area in ecological niche modeling and species distribution modeling. Ecological Modelling 222:1810–1819.

BIDAU, C. J. 2006. Familia Ctenomyidae. Pp. 212 -231, in Mamíferos de Argentina. Sistemática y distribución (Bárquez,R. J., M. M. Díaz, and R. A. Ojeda, eds.). Sociedad Argentina para el Estudio de los Mamíferos. Tucumán, Argentina.

BIDAU, C. J. 2015. Family Ctenomyidae Lesson, 1842. In: Mammals of South America 2:818-877.

BRANT, S. V., AND S .L. GARDNER. 1997. Two new species of Litomosoides (Nemata: Onchocercidae) from Ctenomys opimus (Rodentia: Ctenomyidae) on the Altiplano of Bolivia. Journal of Parasitology 83:700-705.

BREINER, F. T., A. GUISAN, A. BERGAMINI, AND M. P. NOBIS. 2015. Overcoming limitations of modelling rare species by using ensembles of small models. Methods in Ecology and Evolution 6:1210– 1218.

BREINER, F. T., M. P. NOBIS, A. BERGAMINI, AND A. GUISAN. 2018. Optimizing ensembles of small models for predicting the distribution of species with few occurrences. Methods in Ecology and Evolution 9:802-808.

BUSCH, C., C. D. ANTINUCHI, J. C. DEL VALLE, M. J. KITTLEIN, A. I. MALIZIA, A. I. VASSALLO, AND R. R. ZENUTO. 2000. Population ecology of subterranean rodents. Pp 183–226, in Life Underground: The Biology of Subterranean Rodents (Lacey E. A., J. L. Patton, and G. N. Cameron, eds). University of Chicago Press. Chicago, Illinois.

CALDAS, M. M., D. GOODIN, S. SHERWOOD, J. M. CAMPOS KRAUER, AND S. M. WISELY. 2015. Land-cover change in the Paraguayan Chaco: 2000–2011. Journal of Land Use Science 10: 1-8.

CAMPBELL, L.P., C. LUTHER, D. MOO-LLANES, J. M. RAMSEY, R. DANIS-LOZANO, AND A. T. PETERSON. 2015. Climate change influences on global distributions of dengue and chikungunya virus vectors. Philosophical Transactions of the Royal Society B: Biological Sciences 370:20140135

CARABALLO, D. A., S. L. LÓPEZ, A. A. CARMARÁN, AND M. S. ROSSI. 2020. Conservation status, protected area coverage of Ctenomys (Rodentia, Ctenomyidae) species and molecular identification of a population in a national park. Mammalian Biology 100:33-47.

CASTILLO, A., M. CORTINAS, AND E. P. LESSA. 2005. Rapid diversification of South American tuco-tucos (Ctenomys: Rodentia: Ctenomyidae): Contrasting mitochondrial and nuclear intron sequences. Journal of Mammalogy 86:170–179.

CEBALLOS, G., P. R. EHRLICH, AND P. H. RAVEN. 2020. Vertebrates on the brink as indicators of biological annihilation and the sixth mass extinction. Proceedings of the National Academies of Sciences of the United States 117:13596-13602.

COBOS, M. E., A. T. PETERSON, N. BARVE, AND L. OSORIO-OLVERA. 2019. kuenm: an R package for detailed development of ecological niche models using Maxent. PeerJ 7:e6281.

COOK, J. A., S. ANDERSON, AND T. L. YATES. 1990. Notes on Bolivian mammals 6: the genus Ctenomys (Rodentia: Ctenomyidae) in the highlands. American Museum Novitates 2980:1–27.

COOK, J. A., AND T. L. YATES. 1994. Systematic relationships of the tuco-tucos, genus Ctenomys (Rodentia: Octodontidae). Journal of Mammalogy 75: 583–599.

COOK, J. A., AND E. P. LESSA. 1998. Are rates of diversification in subterranean South American tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) unusually high? Evolution 52:1521–1527.

DARWIN, C. R. 1860. Journal of researches into the natural history & geology of the countries visited during the voyage round the world of H.M.S. ‘Beagle’ under the command of captain Fitz Roy, R. N. John Murray. Albemarle St., London.

DI COLA, V., O. BROENNIMANN, B. PETITPIERRE, F.T. BREINER, M. D’AMEN, C. RANDIN, R. ENGLER, J. POTTIER, D. PIO, A. DUBUIS, L. PELLISSIER, R. G. MATEO, W. HORDIJK, N. SALAMIN, AND A. GUISAN. 2017. Ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography 40:774–787.

DRABIK, G. O., AND S. L. GARDNER. 2019. A new species Ancylostoma (Nemata: Strongylida: Ancylostomatidae) from two species of Ctenomys in lowland Bolivia. Journal of Parasitology 105:904-912.

DUNNUM, J., AND N. BERNAL. 2016. Ctenomys boliviensis (errata version published in 2017). The IUCN Red List of Threatened Species 2016: e.T5798A115079917. https://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T5798A22192171.en. Downloaded on 03 May 2020.

DUNNUM, J., J. VARGAS, N. BERNAL, N. ZEBALLOS, AND E. VIVAR. 2016. Ctenomys opimus. The IUCN Red List of Threatened Species 2016: e.T5818A22194246. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T5818A22194246.en. Downloaded on 06 June 2020.

EISENBERG, J. F. 1963. The behavior of heteromyid rodents. University of California Publications in Zoology 69: 1-114.

ELITH, J., AND J. R. LEATHWICK. 2009. Species distribution models: Ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics 40:677–697.

FICK, S. E., AND R. J. HIJMANS. 2017. WorldClim 2: new 1km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37:4302-4315.

FOURCADE, Y., J. O. ENGLER, D. RÖDDER, AND J. SECONDI. 2014. Mapping species distributions with MAXENT using a geographically biased sample of presence data: A performance assessment of methods for correcting sampling bias. PLoS One 9: e97122.

FREITAS, T. R. O. 2006. Cytogenetics status of four Ctenomys species in the south of Brazil. Genetica 126:227–235.

GARDNER, S. L. 1991. Phyletic coevolution between subterranean rodents of the genus Ctenomys (Rodentia: Hystricognathi) and nematodes of the genus Paraspidodera (Heterakoidea: Aspidoderidae) in the Neotropics: temporal and evolutionary implications. Zoological Journal of the Linnean Society 102:169-201.

GARDNER, S. L, AND D.W. DUSZYNSKI. 1990. Polymorphism of Eimerian Oocysts can be a problem in naturally infected hosts: An example from subterranean Rodents in Bolivia. Journal of Parasitology 76:805-811.

GARDNER, S. L. AND L. RUEDAS. 2019. Origin and development of the South American montane mammal fauna by the Andean speciation engine. Abstract 197: 81. http://www.mammalsociety.org/uploads/2019%20ASM%20Abstracts-2019.06.18.pdf

GARDNER, S. L. 1991. Phyletic coevolution between subterranean rodents of the genus Ctenomys (Rodentia: Hystricognathi) and nematodes of the genus Paraspidodera (Heterakoidea: Aspidoderidae) in the Neotropics: temporal and evolutionary implications. Zoological Journal of the Linnean Society 102:169-201.

GARDNER, S. L., AND S. ANDERSON. 2001. Persistent fontanelles in rodent skulls. American Museum Novitates 3327:1–15.

GARDNER, S. L., J. SALAZAR-BRAVO, AND J. A. COOK. 2014. New Species of Ctenomys Blainville 1826 (Rodentia: Ctenomyidae) from the lowlands and central valleys of Bolivia. Special Publications, Museum of Texas Tech University 62:1-34.

HENGL, T., G. B. MENDES DE JESUS, M. HEUVELINK, M. R. GONZALEZ, M. KILIBARDA, A. BLAGOTIĆ, W. SHANGGUAN, M. N. WRIGHT, X. GENG, B. BAUER-MARSCHALLINGER, M. A. GUEVARA, R. VARGAS, R. A. MACMILLAN, N. H. BATJES, J. G. B. LEENAARS, E. RIBEIRO, I. WHEELER, S.MANTEL, AND B. KEMPEN. 2017. SoilGrids250m: Global gridded soil information based on machine learning. Plos One 12:e0169748.

IBISCH, P., S. BECK, B. GERKMANN, AND Y.A. CARRETERO. 2003. Ecoregiones y ecosistemas. Pp. 47–88, in Biodiversidad: La Riqueza de Bolivia (Ibisch, P., and G. Mérida, eds.). FAN. Santa Cruz, Bolivia.

IUCN. 2020. The IUCN Red List of Threatened Species. Version 2020-1. https://www.iucnredlist.org. Downloaded on 20 May 2020.

LACEY, E. A., J. L. PATTON, AND G. N. CAMERON. 2000. Life underground: the biology of subterranean rodents. University of Chicago Press. Chicago, Illinois.

LAMBERT, C. R., S. L. GARDNER, AND D. W. DUSZYNSKI. 1988. Coccidia (Apicomplexa: Eimeriidae) from the subterranean rodent Ctenomys opimus Wagner (Ctenomyidae) from Bolivia, South America. Journal of Parasitology 74:1018-1022.

LESSA, E. P., AND J. A. COOK. 1998. The molecular phylogenetics of tuco-tucos (genus Ctenomys, Rodentia: Octodontidae) suggests an early burst of speciation. Molecular Phylogenetics and Evolution 9:88–99.

LÓPEZ, R. P. 2003. Phytogeographical relations of the Andean dry valleys of Bolivia. Journal of Biogeography 30:1659–1668.

MASCHERETTI, S., P. MIROL, M. GIMÉNEZ, C. BIDAU, J. CONTRERAS, AND J. SEARLE. 2000. Phylogenetics of the speciose and chromosomally variable genus Ctenomys (Ctenomyidae: Octodontoidea), based on mitochondrial cytochrome-b sequences. Biological Journal of the Linnean Society 70: 361–376.

MCQUARRIE, N., B. K. HORTON, G. ZANDT, S. BECK, AND P. G. DECELLES. 2005. Lithospheric evolution of the Andean fold-thrust belt, Bolivia, and the origin of the central Andean plateau. Tectonophysics 399:15–37.

MINISTERIO DE MEDIO AMBIENTE Y AGUA. 2009. Libro rojo de la fauna silvestre de vertebrados de Bolivia. Ministerio de Medio Ambiente y Agua. La Paz, Bolivia.

MUSCARELLA, R., P. J. GALANTE, M. SOLEY‐GUARDIA, R. A. BORIA, J. M. KASS, M. URIARTE, AND R. P. ANDERSON. 2014. ENM eval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5:1198-1205.

OLROG, C. C., AND M. M. LUCERO. 1981. Guía de los mamíferos argentinos. Ministerio de Cultura y Educación, Tucumán: Fundación Miguel Lillo.

PARADA, A. S., G. D’ELÍA, C. J. BIDAU, AND E. P. LESSA. 2011. Species groups and the evolutionary diversification of tuco-tucos, genus Ctenomys (Rodentia: Ctenomyidae). Journal of Mammalogy 92:671–682.

PEARSON, O. P. 1959. Biology of the subterranean rodents, Ctenomys, in Peru. Memorias del Museo de Historia Natural Javier Prado 9:3-56.

PHILLIPS, S. J., AND M. DUDÍK. 2008. Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175.

PUCU, E., M. LARESCHI, AND S. L. GARDNER. 2014. Bolivian ectoparasites: a survey of the fleas of Ctenomys (Rodentia: Ctenomyidae). Comparative Parasitology 81:114-118.

RAXWORTHY, C. J., E. MARTINEZ-MEYER, N. HORNING, R. A. NUSSBAUM, G. E. SCHNEIDER, M. A. ORTEGA-HUERTA, AND A. T. PETERSON. 2003. Predicting distributions of known and unknown reptile species in Madagascar. Nature 426:837-841.

RIDGWAY, R. 1912. Color standards and color nomenclature. Published by the author, A. Hoen (printer). Baltimore, Maryland. 53 colored plates.

ROACH, N., AND L. NAYLOR. 2016a. Ctenomys lewisi. The IUCN Red List of Threatened Species 2016: e.T5811A22193810. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T5811A22193810.en. Downloaded on 06 June 2020.

ROACH, N., AND L. NAYLOR. 2016b. Ctenomys steinbachi. The IUCN Red List of Threatened Species 2016: e.T5827A22194994. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T5827A22194994.en. Downloaded on 12 June 2020.

TETA, P., AND G. D’ELÍA. 2020. Uncovering the species diversity of subterranean rodents at the end of the World: Three new species of Patagonian tuco-tucos (Rodentia, Hystricomorpha, Ctenomys). PeerJ. 2020;8:e9259. Published 2020 May 29. doi:10.7717/peerj.9259

THOMAS, O. 1919. Two new rodents from Tartagal, Salta, N. Argentina. Annals and Magazine of Natural History, ser. 9, 4: 154-156.

THOMAS, O. 1921. A new tuco-tuco from Bolivia. Annals and Magazine of Natural History, ser. 9, 7:136–137.

THOMAS, O. 1926. The Spedan Lewis South American exploration, II: On mammals collected in the Tarija Department, southern Bolivia. Annals and Magazine of Natural History, ser. 9, 17:318–328.

UNZUETA, Q. O. 1975. Mapa ecológico de Bolivia. 1:1,000,000. Ministerio de Asuntos Campesinos y Agropecuarios, Memoria explicativa by Unzueta, 11 pp. Color pl., 312 pp.

VIVAR, E. 2017. Ctenomys frater (errata version published in 2018). The IUCN Red List of Threatened Species 2017: e.T115553730A123796865. https://dx.doi.org/10.2305/IUCN.UK.2017-3.RLTS.T115553730A115553734.en. Downloaded on 04 June 2020.

WALLACE, A. R. 1876. The geographical distribution of animals. With a study of the relations of living and extinct faunas as elucidating the past changes of the earth's surface. Volumes 1 and 2. Macmillan and Co. London, U.K.

WILSON, D. E., AND D. M. REEDER (EDS.). 2005. Mammal Species of the World, a Taxonomic and Geographic Reference, 3rd ed. Johns Hopkins Press, Baltimore, Maryland.

WILSON, D. E., T. E. LACHER JR., AND R. A. MITTERMEIER (EDS.). 2017. The Mammals of the World-Vol. 7, Rodents II. Lynx Edicions. Barcelona, España.

ZEBALLOS, H., AND E. VIVAR . 2016. Ctenomys leucodon. The IUCN Red List of Threatened Species 2016: e.T5810A22193526. https://dx.doi.org/10.2305/IUCN.UK.2016-2.RLTS.T5810A22193526.en. Downloaded on 05 June 2020.

ZURELL, D., J. FRANKLIN, C. KÖNIG, P. J. BOUCHET, C. F. DORMANN, J. ELITH, G. FANDOS, X. FENg, G. Guillera‐Arroita, A. Guisan, and J. J. Lahoz‐Monfort. 2020. A standard protocol for reporting species distribution models. Ecography 43:1261-1277.


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