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Size matters: penis size, sexual maturity and their consequences for giant armadillo conservation planning

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Abstract

The giant armadillo (Priodontes maximus) is the largest living armadillo and is classified as Vulnerable by the International Union for Conservation of Nature. Little is known about the species biology and especially its reproduction. However, data such as the age at sexual maturity are employed for estimation of a species generation length, which is an important parameter for extinction risk assessment. Thus, the aim of this study is to estimate the age at sexual maturity for male P. maximus in the wild and to predict generation length for this species. During a long-term in situ study, eight male P. maximus were captured for reproductive evaluation considering both morphometric characteristics (e.g. body, penis and testes dimensions), and data on sperm production (assessed by electroejaculation). Based on observations of this study, it is estimated that male P. maximus reach sexual maturity at an age of 6.5–8 years. This is at least 5.5–7 years later than previously published. Consequently, generation length for P. maximus results in 11 years when applying standard formula including age at sexual maturity in males and an estimate of age at last reproduction of 20 years. However, the generation length is probably underestimated here as sexual maturity in females and age at last reproduction could be later than estimates used. Even these conservative estimates result in noticeable change for the timeframe used in extinction risk assessments for this species as it is 33 instead of 21 years. Thus, results from this study might affect the classification status of P. maximus particularly for regional assessments.

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References

  • Anacleto TCS, Miranda F, Medri I, Cuéllar E, Abba AM, Superina M (2014) Priodontes maximus. International Union for Conservation and Nature, Red List of Threatened Species, Version 2014.3. Accessed 7 July 2019

  • Banhos A, Fontes BL, Yogui D, Alves MH, Ardente NC, Valls R, Mendes Barreto L, Damásio L, Colombo Ferreguetti Á, Siqueira Carvalho A, Schettino VR, Rosa dos Santos A, Godoy Bergallo H, Srbek-Araujo AC, Medici P, Canena A, Desbiez ALJ (2020) Highways are a threat for giant armadillos that underpasses can mitigate. Biotropica (in press)

  • Brito LFC, Barth AD, Wilde RE, Kastelic JP (2012) Testicular ultrasonogram pixel intensity during sexual development and its relationship with semen quality, sperm production, and quantitative testicular histology in beef bulls. Theriogenology 78:69–76

    CAS  PubMed  Google Scholar 

  • Carter TS, Superina M, Leslie DM (2016) Priodontes maximus (Cingulata: Chlamyphoridae). Mammal Species 48(932):21–34

    Google Scholar 

  • Cetica PD, Merani MS (2008) Sperm evolution in Dasypodids. In: Vizcaino SF, Loughry WJ (eds) Biology of the Xenarthra. University Press of Florida, Gainesville, pp 143–150

    Google Scholar 

  • Charpentier MJE, Tung J, Altmann J, Alberts SC (2008) Age at maturity in wild baboons: genetic, environmental and demographic influences. Mol Ecol 17:2026–2040

    CAS  PubMed  Google Scholar 

  • Chen LM, Hou R, Zhang ZH, Wang JS, An XR, Chen YF, Zheng HP, Xia GL, Zhang MJ (2007) Electroejaculation and semen characteristics of Asiatic Black bears (Ursus thibetanus). Anim Reprod Sci 101:358–364

    CAS  PubMed  Google Scholar 

  • Chiarello AG, Röhe F, Miranda FR, Mourão GDM, Silva KD, Vaz SM, Anacleto TDS (2015) Avaliação do risco de extinção de Priodontes maximus (Kerr, 1792) no Brasil. Série Estado de Conservação da Fauna Brasileira 2:209–222

    Google Scholar 

  • Cooke RSC, Gilbert TC, Riordan P, Mallon D (2018) Improving generation length estimates for the IUCN Red List. PLoS One 13(1):e0191770. https://doi.org/10.1371/journal.pone.019177

    Article  PubMed  PubMed Central  Google Scholar 

  • Desbiez ALJ, Massocato GF, Kluyber D, Luba CN, Attias N (2019a) How giant are giant armadillos? The morphometry of giant armadillos (Priodontes maximus Kerr, 1792) in the Pantanal of Brazil. Mamm Biol 95:9–14

    Google Scholar 

  • Desbiez ALJ, Massocato GF, Kluyber D (2019b) Insights in Giant Armadillo (Priodontes maximus Kerr, 1792) reproduction. Mammalia (in press)

  • Desbiez ALJ, Massocato GF, Kluyber D, Oliveira-Santos LGR, Attias N (2020) Spatial ecology of the giant armadillo (Priodontes maximus) in Midwestern Brazil. J Mammal 101:151–163

    Google Scholar 

  • Eaton MJ, Link WA (2011) Estimating age from recapture data: integrating incremental growth measures with ancillary data to infer age-at-length. Ecol Appl 21:2487–2497

    PubMed  Google Scholar 

  • Emmons LH, Feer F (1997) Neotropical rainforest mammals: a field guide. The University of Chicago Press, Chicago

    Google Scholar 

  • Fickel J, Wagener A, Ludwig A (2007) Semen cryopreservation and the conservation of endangered species. Eur J Wildl Res 53:81–89

    Google Scholar 

  • Fonseca GAB, Aguiar JM (2004) The 2004 edentate species assessment workshop. Edentata 6:1–26

    Google Scholar 

  • Ford JJ, Wise TH (2011) Assessment of pubertal development of boars derived from ultrasonographic determination of testicular diameter. Theriogenology 75:241–247

    CAS  PubMed  Google Scholar 

  • Fung HC, Waples RS (2017) Performance of IUCN proxies for generation length. Conserv Biol 31:883–893

    PubMed  Google Scholar 

  • Gaillard JM, Yoccoz NG, Lebreton JD, Bonenfant C, Devillard S, Loison A, Pontier D, Allaine D (2005) Generation time: a reliable metric to measure life-history variation among mammalian populations. Am Nat 166:119–123

    PubMed  Google Scholar 

  • Grandi MF, Dans SL, García NA, Crespo EA (2010) Growth and age at sexual maturity of South American sea lions. Mamm Biol 75(5):427–436

    Google Scholar 

  • Hayward MW, Child MF, Kerley GIH, Lindsey PA, Somers MJ, Burns B (2015) Ambiguity in guideline definitions introduces assessor bias and influences consistency in IUCN Red List status assessments. Front Ecol Evol 3:87

    Google Scholar 

  • Hernandez SM, Gammons DJ, Gottdenker N, Mengak MT, Conner LM, Divers SJ (2010) Technique, safety and efficacy of intra-abdominal transmitters in nine-banded armadillos. J Wildl Manag 74:174–180

    Google Scholar 

  • Hildebrandt TB, Saragusty J (2015) Use of ultrasonography in wildlife species. In: Miller RE, Fowler ME (eds) Fowler´s zoo and wild animal medicine, 8th edn. Saunders Ltd, London, pp 714–723

    Google Scholar 

  • Hildebrandt TB, Hermes R, Pratt NC, Fritsch G, Blottner S, Schmitt DL, Ratanakorn P, Brown JL, Rietschel W, Göritz F (2000) Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing male reproductive function. Zoo Biol Publ Affil Am Zoo Aquar Assoc 19(5):333–345

    Google Scholar 

  • Hiort O (2002) Androgens and puberty. Best Pract Res Cl En 16(1):31–41

    CAS  Google Scholar 

  • IUCN Standards and Petitions Committee (2019) Guidelines for Using the IUCN Red List Categories and Criteria. Version 14. Prepared by the Standards and Petitions Committee. http://www.iucnredlist.org/documents/RedListGuidelines.pdf. Accessed 30 Mar 2020

  • Jones TH (2008) Diagnosis of hypogonadism: symptoms, signs, tests, and guidelines. In: Jones TH (ed) Testosterone deficiency in men. University Press, Oxford, pp 23–37

    Google Scholar 

  • Kemper CM, Trentin E, Tomo I (2014) Sexual maturity in male Indo-Pacific bottlenose dolphins (Tursiops aduncus): evidence for regressed/pathological adults. J Mamm 95(2):357–368

    Google Scholar 

  • Kluyber D, Lopez RPG, Massocato G, Attias N, esbiez ALJ (2020) Anesthesia and surgery protocols for intra-abdominal transmitter placement in four species of wild Armadillo. J Zoo Wildl Med (in press)

  • Lambert B (1951) The frequency of mumps and of mumps orchitis and the consequences of sexuality and fertility. Acta Genet Stat Med 2:1–166

    CAS  PubMed  Google Scholar 

  • Liu Y, Jin L-R, Metzner W, Feng J (2009) Postnatal growth and age estimation in big-footed myotis, Myotis macrodactylus. Acta Chiropterol 11:105–111

    Google Scholar 

  • Luaces JP, Rossi LF, Merico V, Zuccotti M, Redi CA, Solari AJ, Merani MS, Garagna S (2013) Spermatogenesis is seasonal in the large hairy armadillo, Chaetophractus villosus (Dasypodidae, Xenarthra, Mammalia). Reprod Fertil Dev 25(3):547–557

    PubMed  Google Scholar 

  • Luba CN, Boakari YL, Lopes AMC, Gomes MS, Miranda FR, Papa FO, Ferreira JCP (2015) Semen characteristics and refrigeration in free-ranging giant anteaters (Myrmecophaga tridactyla). Theriogenology 84(9):1572–1580

    Google Scholar 

  • Massocato GF, Desbiez ALJ (2019) Guidelines to identify individual giant armadillos, Priodontes maximus (Kerr, 1792), through camera traps. Edentata 20:1–16

    Google Scholar 

  • Meritt DA Jr (2006) Research questions on the behavior and ecology of the giantarmadillo (Priodontes maximus). Edentata 7:30–33

    Google Scholar 

  • Merrett PK (1983) Edentates: project for city and guilds animal management course. Zoological Trust of Guernsy, Guernsy

    Google Scholar 

  • Noakes DE (2009) Endogenous and exogenous control of ovarian cyclicity. In: Noakes DE, Parkinson TJ, England GCW (eds) Veterinary reproduction and obstetrics, 9th edn. Saunders Ltd, London, pp 3–58

    Google Scholar 

  • Pacifici M, Santini L, Di Marco M, Baisero D, Francucci L, Marasini GG, Visconti P, Rondinini C (2013) Generation length for mammals. Nat Conserv 5:87–94

    Google Scholar 

  • Peppler RD (2008) Reproductive biology of the nine-banded armadillo. In: Vizcaíno SF, Loughry WJ (eds) The biology of Xenarthra. University Press of Florida, Gainesville, pp 151–159

    Google Scholar 

  • Peppler RD, Stone SC (1981) Annual pattern in plasma testosterone in the male armadillo, Dasypus novemcinctus. Anim Reprod Sci 4:49–53

    CAS  Google Scholar 

  • Platz CC, Seager SWJ (1978) Semen collection by electroejaculation in the domestic cat. J Am Vet Med Assoc 173:1353–1355

    PubMed  Google Scholar 

  • Pollard RE, Herrgesell EJ (2009) Abdominal Ultrasonography. In: Ettinger SJ, Feldman EC (eds) Textbook of veterinary internal medicine, 7th edn. Elsevier Health Science, St. Louis, pp 373–374

    Google Scholar 

  • Richard JT, Schmitt T, Haulena M, Vezzi N, Dunn JL, Romano TA, Sartini BL (2017) Seasonal variation in testes size and density detected in belugas (Delphinapterus leucas) using ultrasonography. J Mamm 98(3):874–884

    Google Scholar 

  • Ritz C, Baty F, Streibig JC, Gerhard D (2015) Dose-response analysis using R. PLoS One 10:e0146021

    PubMed  PubMed Central  Google Scholar 

  • Sadleir R (1973) Puberty and frequency of breeding by individuals. In: Sadleir R (ed) The reproduction of vertebrates. Academic Press, London, pp 156–158

    Google Scholar 

  • Sakamoto H, Saito K, Oohta M, Inoue K, Ogawa Y, Yoshida H (2007) Testicular volume measurement: comparison of ultrasonography, orchidometry, and water displacement. Urology 69(1):152–157

    PubMed  Google Scholar 

  • Sikes RS, the Animal Care and Use Committee of the American Society of Mammalogists (2016) 2016 Guidelines of the American Society of Mammalogists for the use of wild mammals in research and education. J Mamml 97(3):663–688

    Google Scholar 

  • Silveira L, Jácomo ATA, Furtado MM, Torres NM, Sollmann R, Vynne C (2009) Ecology of the giant armadillo (Priodontes maximus) in the grasslands of Central Brazil. Edentata 8–10:25–34

    Google Scholar 

  • Soriano BMA (2000) Boletim agrometeorológico: Fazenda Nhumirim. Embrapa Pantanal Boletim Agrometeorol 4:1–81

    Google Scholar 

  • Strauss A, Mascher E, Palme R, Millesi E (2007) Sexually mature and immature yearling male European ground squirrels: a comparison of behavioral and physiological parameters. Horm Behav 52(5):646–652

    PubMed  Google Scholar 

  • Superina M (2008) The natural history of the pichi, Zaedyus pichiy, in western Argentina. In: Vizcaíno SF, Loughry WJ (eds) The biology of Xenarthra. University Press of Florida, Gainesville, pp 313–318

    Google Scholar 

  • Superina M, Jahn GA (2009) Seasonal reproduction in male pichis Zaedyus pichiy (Xenarthra:Dasypodidae) estimated by fecal androgen metabolites and testicular histology. Anim Reprod Sci 112:283–292

    CAS  PubMed  Google Scholar 

  • Superina M, Carreno N, Jahn GA (2009) Characterization of seasonal reproduction patterns in female pichis Zaedyus pichiy (Xenarthra:Dasypodidae) estimated by fecal sex steroid metabolites and ovarian histology. Anim Reprod Sci 116(3–4):358–369

    CAS  PubMed  Google Scholar 

  • Superina M, Pagnutti N, Abba AM (2014) What do we know about armadillos? An analysis of four centuries of knowledge about a group of South American mammals, with emphasis on their conservation. Mamm Rev 44:69–80

    Google Scholar 

  • Tanner JM (1981) Growth and maturation during adolescence. Nut Rev 39(2):43–55

    CAS  Google Scholar 

  • Tarsi K, Tuff T (2012) Introduction to population demographics. Nat Ed Know 3(11):3

    Google Scholar 

  • ZIMS (2020) Giant armadillo (Priodontes maximus) species historical holdings. Zoological Information Management System, Species360, Bloomington

    Google Scholar 

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Acknowledgements

We are grateful to the owners of the Fazenda Baía das Pedras for their hospitality, generous support, and permission to work on their land. This study is part of the Giant Armadillo Conservation Program, which benefited from multiple grants, mostly from Zoos in North America and Europe, listed at www.giantarmadillo.org. This study was performed under License No. 27587 (Chico Mendes Institute for Biodiversity Conservation) that granted permission to capture, immobilize, and manipulate armadillos and collect/store biological samples. We would like to thank two anonymous reviewers for their useful comments that help improve the manuscript. All procedures followed the Guidelines of the American Society of Mammalogists for the use of wild mammals in research (Sikes et al. 2016).

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Correspondence to Arnaud Leonard Jean Desbiez.

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Luba, C.N., Kluyber, D., Massocato, G.F. et al. Size matters: penis size, sexual maturity and their consequences for giant armadillo conservation planning. Mamm Biol 100, 621–630 (2020). https://doi.org/10.1007/s42991-020-00065-3

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