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Harpy eagle kill sample provides insights into the mandibular ontogenetic patterns of two-toed sloths (Xenarthra: Choloepus)

  • Lucas C. Pasin , Daniel M. Casali ORCID logo , Thiago B. F. Semedo ORCID logo and Guilherme S. T. Garbino ORCID logo EMAIL logo
Published/Copyright: May 22, 2024
Mammalia
From the journal Mammalia Volume 88 Issue 5

Abstract

Skeletal ontogeny of xenarthrans is poorly known, especially because of the paucity of study specimens from distinct developmental stages. Here, we investigate morphometric aspects of the mandible ontogeny in the two-toed sloths, Choloepus spp. We examined mandibles of infant, juveniles and subadult sloths that were present in kill assemblages of harpy eagles, Harpia harpyja, and complemented our study with adult museum specimens. We carried out uni- and multivariate linear morphometric analyzes to assess the growth pattern of the mandible. Harpy eagles did not prey on adult two-toed sloths, preferring younger individuals. We found an overall strong correlation between the total length of the mandible and other mandibular measurements across age classes, with some of them scaling isometrically, and others presenting allometric growth. Also, morphometric data correlated with patterns of symphysial fusion across ontogenetic stages, rendering the latter a reliable indicator of the animal’s age category. Although it was necessary to complement our sample with museum material, individuals obtained from the harpy eagle kill assemblage proved to be a valuable complementary source of specimens to be studied.

Keywords: allometry; dentary; isometry; morphometrics; pilosa
Corresponding author: Guilherme S. T. Garbino, Departamento de Biologia Animal, Laboratório de Mastozoologia, Museu de Zoologia João Moojen, Universidade Federal de Viçosa, 36570-900 Viçosa, Minas Gerais, Brazil; and Pós-graduação em Biologia Animal, Universidade Federal de Viçosa, Viçosa, Minas Gerais, Brazil, E-mail:

Funding source: Fundação para a Ciência e a Tecnologia

Award Identifier / Grant number: 202210212BD

Award Identifier / Grant number: UIDP/50027/2020

Funding source: Fundação de Amparo à Pesquisa do Estado de São Paulo

Award Identifier / Grant number: #2022/00044-7

Acknowledgments

Everton B. P. Miranda kindly provided the osteological material collected in the harpy eagle nests and gave important advice on the interpretation of the predation patterns. We are thankful to Joyce R. Prado, Juliana Gualda Barros, Fabio O. Nascimento, and José Eduardo Serrano Villavicencio, Museu de Zoologia da USP (MZUSP), for the privilege of studying the collections in their care. Fabiana Cristina S. A. de Melo gave very useful advice on an earlier version of this manuscript. We are also grateful to Juliano A. S. V. Paes for taking some of the mandible photos used here. We are indebted to the editor and two anonymous reviewers for their suggestions and corrections, which helped us to improve the manuscript.

  1. Research ethics: Licenses and permits to collect the osteological material and install the camera traps in the nests were provided by the Instituto Chico Mendes de Conservação da Biodiversidade (ICMBio), Brazilian Ministry of the Environment (SISBIO process No. 58533). The study was also approved by the Ethics Committee on Animal Use (CEUA) of the Universidade Federal de Viçosa (UFV) – process no. 1106/2021. No live animal was handled and/or injured.

  2. Author contributions: L.C.P. contributed to data collection and analyzes. D.M.C. contributed to data analyzes, data visualization, interpretation, and manuscript writing. T.B.F.S. contributed to data collection and funding acquisition. G.S.T.G. contributed to the project design, data collection, analyzes, interpretation, and manuscript writing. All authors read and approved the final version of this manuscript.

  3. Competing interests: The authors declare no conflict of interest.

  4. Research funding: Bone collection in the field was supported by SouthWild.com Conservation Travel System, Rainforest Biodiversity Group, Idea Wild, The Mamont Scholars Program of the Explorer’s Club Exploration Fund, Cleveland Metroparks Zoo, and the Rufford Small Grants Foundation (18743-1, 23022-2, and 31091 B). Daniel M. Casali is currently being funded by grant #2022/00044-7, São Paulo Research Foundation (FAPESP), Brazil. Thiago B. F. Semedo is supported by a fellowship from the Portuguese Foundation for Science and Technology under scholarship number (202210212BD).

  5. Data availability: The raw data can be obtained on request from the corresponding author.

Appendix 1

Specimens of Choloepus from Brazil used in this study are deposited in the Museu de Zoologia João Moojen (MZUFV), and Museu de Zoologia da Universidade de São Paulo (MZUSP) collections. Localities are arranged by the Brazilian federal state (in bold) and municipality or specific locality. Decimal geographic coordinates (latitude and longitude, respectively) are between parentheses, when available. Disarticulated dentaries were counted as separate specimens.

C. didactylus – Adult specimens in MZUSP (N = 5): Amazonas, Rio Juruá: 781; Maranhão, Miritiba: 2899; Pará, Cachoeira do Espelo, Altamira: 21328; Cametá: 19925; Óbidos: 3651.

C. hoffmanni – Adult specimens in MZUSP (N = 4): Amazonas, Eirunepé: 19926; Igarapé Grande, Rio Juruá: 5446, Santa Cruz, Rio Eiru: 5461; Rondônia: 32340.

Choloepus sp. – Infant, juvenile, and subadult specimens in MZUFV (N = 37): Mato Grosso, Apiacás 1 (−9.383853; −57.64427): ED0116, ED0117, ED0118, ED0119, ED0201; Berneck 1 (−9.78344; −58.302317): B0111, B0401, B0750; Berneck 2 (−9.687318; −58.280317): B20101; Cotriguaçu 2 (−9.85620; −58.38038): AW0111, AW0212, AW0213; Cotriguaçu 3 (−9.990286; −58.362616): EL0219/0220, EL0528, EL0725; Cotriguaçu 4 (−9.993833; −58.280667): CE01101, CE01109, CE0196/01324, CE0197, CE0201, CE0202, CE0203, CE0204, CE0323; FSN 1 (−9.850086; −58.306281): FS0202, FS0216, FS0223, FS0224, FS0225, FS0306, FS0414; NB1 (−10.20675; −58.307479): JB0301, JB0302, JB0303; NB2 (−10.043259; −57.911096): VA0203.

References

Aguiar-Silva, F.H., Sanaiotti, T.M., and Luz, B.B. (2014). Food habits of the Harpy Eagle, a top predator from the Amazonian rainforest canopy. J. Raptor Res. 48: 24–35, https://doi.org/10.3356/jrr-13-00017.1.Search in Google Scholar

Anderson, M.J. (2001). A new method for non‐parametric multivariate analysis of variance. Austral. Ecol. 26: 32–46, https://doi.org/10.1111/j.1442-9993.2001.tb00081.x.Search in Google Scholar

Bargo, M.S., Toledo, N., and Vizcaíno, S.F. (2006). Muzzle of South American pleistocene ground sloths (Xenarthra, Tardigrada). J. Morphol. 267: 248–263, https://doi.org/10.1002/jmor.10399.Search in Google Scholar PubMed

Bastidas-Domínguez, M.C., Link, A., Di Fiore, A., and Mosquera, D. (2023). Sloths strike back: predation attempt by an ocelot (Leopardus pardalis) on a Linnaeus’s two-toed sloth (Choloepus didactylus) at a mineral lick in Western Amazonia, Ecuador. Food Webs 36: e00291, https://doi.org/10.1016/j.fooweb.2023.e00291.Search in Google Scholar

Boscaini, A., Gaudin, T.J., Mamani Quispe, B., Münch, P., Antoine, P.O., and Pujos, F. (2019). New well-preserved craniodental remains of Simomylodon uccasamamensis (Xenarthra: Mylodontidae) from the Pliocene of the Bolivian Altiplano: phylogenetic, chronostratigraphic and palaeobiogeographical implications. Zool. J. Linn. Soc. Lond. 185: 459–486, https://doi.org/10.1093/zoolinnean/zly075.Search in Google Scholar

Cartelle, C. and De Iuliis, G. (2006). Eremotherium laurillardi (Lund)(Xenarthra, Megatheriidae), the Panamerican giant ground sloth: taxonomic aspects of the ontogeny of skull and dentition. J. Syst. Palaeontol. 4: 199–209, https://doi.org/10.1017/s1477201905001781.Search in Google Scholar

Cartelle, C., De Iuliis, G., Boscaini, A., and Pujos, F. (2019). Anatomy, possible sexual dimorphism, and phylogenetic affinities of a new mylodontine sloth from the late Pleistocene of intertropical Brazil. J. Syst. Palaeontol. 17: 1957–1988, https://doi.org/10.1080/14772019.2019.1574406.Search in Google Scholar

Cartelle, C., De Iuliis, G., and Pujos, F. (2015). Eremotherium laurillardi (Lund, 1842) (Xenarthra, Megatheriinae) is the only valid megatheriine sloth species in the Pleistocene of intertropical Brazil: a response to Faure et al., 2014. C. R. Palevol 14: 15–23, https://doi.org/10.1016/j.crpv.2014.09.002.Search in Google Scholar

De Iuliis, G., Boscaini, A., Pujos, F., McAfee, R.K., Cartelle, C., Tsuji, L.J., and Rook, L. (2020). On the status of the giant mylodontine sloth Glossotherium wegneri (Spillmann, 1931) (Xenarthra, Folivora) from the late Pleistocene of Ecuador. C. R. Palevol 19: 215–232.10.5852/cr-palevol2020v19a12Search in Google Scholar

De Iuliis, G., Cartelle, C., McDonald, H.G., and Pujos, F. (2017). The mylodontine ground sloth Glossotherium tropicorum from the late Pleistocene of Ecuador and Peru. Pap. Palaeontol. 3: 613–636, https://doi.org/10.1002/spp2.1088.Search in Google Scholar

Delsett, L.L. (2024). Collecting whales: processes and biases in Nordic museum collections. PeerJ 12: e16794, https://doi.org/10.7717/peerj.16794.Search in Google Scholar PubMed PubMed Central

Garbino, G.S.T., Semedo, T.B.F., and Miranda, E.B.P. (2024). Taphonomy of harpy eagle predation on primates and other mammals. Am. J. Primatol. 86: e23567, https://doi.org/10.1002/ajp.23567.Search in Google Scholar PubMed

Gaudin, T.J. and Scaife, T. (2023). Cranial osteology of a juvenile specimen of Acratocnus ye (Mammalia, Xenarthra, Folivora) and its ontogenetic and phylogenetic implications. Anat. Rec. 306: 607–637, https://doi.org/10.1002/ar.25062.Search in Google Scholar PubMed

Hautier, L., Billet, G., Eastwood, B., and Lane, J. (2014). Patterns of morphological variation of extant sloth skulls and their implication for future conservation efforts. Anat. Rec. 297: 979–1008, https://doi.org/10.1002/ar.22916.Search in Google Scholar PubMed

Hautier, L., Gomes Rodrigues, H., Billet, G., and Asher, R.J. (2016). The hidden teeth of sloths: evolutionary vestiges and the development of a simplified dentition. Sci. Rep. 6: 27763, https://doi.org/10.1038/srep27763.Search in Google Scholar PubMed PubMed Central

Hautier, L., Oliver, J.D., and Pierce, S.E. (2018). An overview of xenarthran developmental studies with a focus on the development of the xenarthrous vertebrae. J. Mamm. Evol. 25: 507–523, https://doi.org/10.1007/s10914-017-9412-y.Search in Google Scholar

Holm, S. (1979). A simple sequentially rejective multiple test procedure. Scand. J. Stat. 6: 65–70.Search in Google Scholar

Kassambara, A. (2023a). rstatix: Pipe-friendly framework for basic statistical tests, R package version 0.7.2, https://cran.r-project.org/web/packages/rstatix/index.html.Search in Google Scholar

Kassambara, A. (2023b). ggpubr: ’ggplot2’ based publication ready plots, R package version 0.6.0, <https://cran.r-project.org/web/packages/ggpubr/index.html>.Search in Google Scholar

Martinez Arbizu, P. (2017). pairwiseAdonis: pairwise multilevel comparison using Adonis, R package version 0.4.1, <https://github.com/pmartinezarbizu/pairwiseAdonis>.Search in Google Scholar

Miranda, E.B.P. (2018). Prey composition of harpy eagles (Harpia harpyja) in raleighvallen, Suriname. Trop. Conserv. Sci. 11: 194008291880078, https://doi.org/10.1177/1940082918800789.Search in Google Scholar

Miranda, E.B.P., Peres, C.A., Carvalho-Rocha, V., Miguel, B.V., Lormand, N., Huizinga, N., Munn, C.A., Semedo, T.B.F., Ferreira, T.V., Pinho, J.B., et al.. (2021). Tropical deforestation induces thresholds of reproductive viability and habitat suitability in Earth’s largest eagles. Sci. Rep. 11: 13048, https://doi.org/10.1038/s41598-021-92372-z.Search in Google Scholar PubMed PubMed Central

Oksanen, J., Simpson, G., Blanchet, F., Kindt, R., Legendre, P., Minchin, P., and Weedon, J. (2022). Vegan: community ecology package, R package version 2.6-4, <https://cran.r-project.org/web/packages/vegan/index.html>.Search in Google Scholar

Peres, C. (1999) The structure of nonvolant mammal communities in different Amazonian forest types. In: Eisenberg, J.F., and Redford, K.H. (Eds.). Mammals of the neotropics. Volume 3. The central neotropics: Ecuador, Peru, Bolivia Brazil. The University of Chicago Press, Chicago, pp. 564–581.Search in Google Scholar

Pujos, F., De Iuliis, G., Vilaboim Santos, L., and Cartelle, C. (2023). Description of a fetal skeleton of the extinct sloth Nothrotherium maquinense (Xenarthra, Folivora): ontogenetic and palaeoecological interpretations. J. Mamm. Evol. 30: 577–595, https://doi.org/10.1007/s10914-023-09665-5.Search in Google Scholar

Pujos, F., Gaudin, T.J., De Iuliis, G., and Cartelle, C. (2012). Recent advances on variability, morpho-functional adaptations, dental terminology, and evolution of sloths. J. Mamm. Evol. 19: 159–169, https://doi.org/10.1007/s10914-012-9189-y.Search in Google Scholar

Pyke, G.H. and Ehrlich, P.R. (2010). Biological collections and ecological/environmental research: a review, some observations and a look to the future. Biol. Rev. 85: 247–266, https://doi.org/10.1111/j.1469-185x.2009.00098.x.Search in Google Scholar

R Core Team (2023). R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, <https://www.R-project.org/>.Search in Google Scholar

Rocha, L.A., Aleixo, A., Allen, G., Almeda, F., Baldwin, C.C., Barclay, M.V., Bates, J.M., Bauer, A.M., Benzoni, F., Berns, C.M., et al.. (2014). Specimen collection: an essential tool. Science 344: 814–815, https://doi.org/10.1126/science.344.6186.814.Search in Google Scholar PubMed

Santos, P.M., Bocchiglieri, A., Chiarello, A.G., Paglia, A.P., Moreira, A., de Souza, A.C., Abba, A.M., Paviolo, A., Gatica, A., Medeiro, A.Z., et al.. (2019). Neotropical xenarthrans: a data set of occurrence of xenarthran species in the Neotropics. Ecology 100: e02663, https://doi.org/10.1002/ecy.2663.Search in Google Scholar PubMed

Schauberger, P. and Walker, A. (2023). Openxlsx: read, write and edit xlsx files, R package version 4.2.5.2, <https://cran.r-project.org/web/packages/openxlsx/openxlsx.pdf>.Search in Google Scholar

Smith, K.J., Mead, J.G., and Peterson, M.J. (2021). Specimens of opportunity provide vital information for research and conservation regarding elusive whale species. Environ. Conserv. 48: 84–92, https://doi.org/10.1017/s0376892920000521.Search in Google Scholar

Tang, Y., Horikoshi, M., and Li, W. (2016). ggfortify: unified interface to visualize statistical result of popular R packages. R Journal 8: 478–489.10.32614/RJ-2016-060Search in Google Scholar

Tejada, J.V., Flynn, J.J., MacPhee, R., O’Connell, T.C., Cerling, T.E., Bermudez, L., Capuñay, C., Wallsgrove, N., and Popp, B.N. (2021). Isotope data from amino acids indicate Darwin’s ground sloth was not an herbivore. Sci. Rep. 11: 18944, https://doi.org/10.1038/s41598-021-97996-9.Search in Google Scholar PubMed PubMed Central

Wickham, H. (2016). ggplot2: elegant graphics for data analysis. Springer-Verlag, New York, <https://cran.r-project.org/web/packages/ggplot2/index.html>.10.1007/978-3-319-24277-4Search in Google Scholar

Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/mammalia-2024-0037).

Received: 2024-03-11
Accepted: 2024-05-02
Published Online: 2024-05-22
Published in Print: 2024-09-25

© 2024 Walter de Gruyter GmbH, Berlin/Boston

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https://doi.org/10.1515/mammalia-2024-0037
Keywords for this article
allometry; dentary; isometry; morphometrics; pilosa

Articles in the same Issue

  1. Frontmatter
  2. Ecology
  3. Occurrence and temporal activity pattern of Burmese Red Serow (Capricornis rubidus, Bovidae) in Baraiyadhala National Park, Bangladesh: insights from a camera trapping study
  4. Understanding habitat suitability and road mortality for the conservation of the striped hyaena (Hyaena hyaena) in Batna (East Algeria)
  5. Striped hyena Hyaena hyaena (Linnaeus 1758): feeding ecology based on den prey remains in a pastoralist landscape, southern Kenya
  6. Harpy eagle kill sample provides insights into the mandibular ontogenetic patterns of two-toed sloths (Xenarthra: Choloepus)
  7. Drivers of Indian pangolin (Manis crassicaudata) mortality in Central and Western Pakistan
  8. Food habits of invasive masked palm civets (Paguma larvata) in northern Japan
  9. First predation event of an anuran by Holochilus chacarius in the Pantanal wetland, central portion of South America
  10. Potential seed dispersal of cumbaru (Dipteryx alata) by fruit-eating bats (Artibeus sp.) in a Brazilian urban context
  11. Biogeography
  12. New and unusual records of Glironia venusta (Didelphimorphia, Didelphidae) in Brazil
  13. Bats (Mammalia: Chiroptera) from two priority areas for biodiversity conservation in the Brazilian Amazon and range extension for Carollia benkeithi (Phyllostomidae)
  14. A multidisciplinary approach unveils the distribution of the Alpine long-eared bat Plecotus macrobullaris (Vespertilionidae) in Italy
  15. First record of Great Himalayan leaf-nosed bat, Hipposideros armiger (Hipposideridae) from Bangladesh
  16. Ethology
  17. Insights into marking behavior of giant anteaters: a camera trap study in the Rupununi savannahs, Guyana
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