Insights Into Giant Armadillo (Priodontes Maximus Kerr, 1792
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Mammalia 2019; aop Arnaud Leonard Jean Desbiez*, Gabriel Favero Massocato and Danilo Kluyber Insights into giant armadillo (Priodontes maximus Kerr, 1792) reproduction https://doi.org/10.1515/mammalia-2019-0018 Received February 21, 2019; accepted August 20, 2019 Introduction Abstract: This paper presents unique data on the repro- The giant armadillo [Priodontes maximus (Kerr, 1792)], ductive behavior of the rare giant armadillo (Priodontes the largest of living cingulates (Mammalia: Cingulata), maximus), including gestation, inter-birth intervals, can reach up to 150 cm (head to tail) and weigh up to 50 number of offspring and parental care. It also describes kg (Emmons and Feer 1997, Eisenberg and Redford 1999, a potential non-parental infanticide. The study used Desbiez et al. 2019). One of the most striking features of telemetry, camera traps and track observations for over the species is the large scimitar-shaped fore-claws, the 7 years in a 300-km2 area in the central Brazilian Panta- third of which is greatly enlarged and can be as long as nal. Females with young were recorded 5 times. Repro- 20.3 cm (Carter et al. 2016). Giant armadillos are found ductive events did not appear to be seasonal. A 5-month over much of South America – in 11 different countries – gestation period was estimated. Parental care is long, as in habitats ranging from tropical forest to open savanna the offspring is completely dependent on its mother’s milk (Abba and Superina 2010). Although widespread, giant until 6–8 months of age. Weaning was estimated to occur armadillos are rare (Meritt 2006), and are currently clas- at 11–12 months, but the offspring continued to be depend- sified as “Vulnerable” (A2cd) on the International Union ent on its mother’s burrows until 18 months old. Three for Conservation of Nature (IUCN) Red List of Threatened births were recorded over a 6-year period for one individ- Species (Anacleto et al. 2014). ual. The offspring from the first birth recorded was killed Giant armadillos are nocturnal and fossorial, and at 4 weeks of age in a potential infanticide, but 7 months rarely seen, even by local people. All studies confirm after the first birth, a second offspring was born. A third the rarity of the species (Walsh and Gannon 1967, Noss birth was recorded 3 years after the second birth. Results et al. 2004, Silveira et al. 2009, Srbek-Araujo et al. 2009). from this study suggest that the population growth rate of Their large burrows are often the only evidence of their giant armadillos is very low and the species can therefore presence and the focus of several studies (Carter 1983, easily be locally extirpated. Carter and Encarnação 1983, Anacleto 1997, Ceresoli and Fernandez-Duque 2012, Porfirio et al. 2012). The role they Keywords: Cingulata; gestation period; infanticide; inter- play in the ecological community as ecosystem engineers birth interval; parental care. has been described for various biomes (Leite Pitman et al. 2004, Desbiez and Kluyber 2013, Aya-Cuero et al. 2017, Massocato and Desbiez 2017). Despite being the object of quite a number of publications (Superina et al. 2014), the *Corresponding author: Arnaud Leonard Jean Desbiez, Instituto de Conservação de Animais Silvestres (ICAS), Rua Licuala 622, overall life-history data for giant armadillos are lacking, 79046150, Campo Grande, Mato Grosso do Sul, Brazil; Instituto de and reports on the basic reproductive characteristics Pesquisas Ecológicas (IPÊ), Rodovia Dom Pedro I, km 47, 12960-000, (Merrett 1983) are probably inaccurate (Aya-Cuero et al. Nazaré Paulista, São Paulo, Brazil; and Royal Zoological Society 2015, Carter et al. 2016). Despite a misleading picture in of Scotland (RZSS), Murrayfield, Edinburgh, EH12 6TS, UK, e-mail: Gijzen (1965), the species has never bred in captivity (ZIMS [email protected] 2017). The only information on reproduction comes from Gabriel Favero Massocato: Instituto de Conservação de Animais Silvestres (ICAS), Rua Licuala 622, 79046150, Campo Grande, Aya-Cuero et al. (2015), who, using camera traps, obtained Mato Grosso do Sul, Brazil; Instituto de Pesquisas Ecológicas (IPÊ), three records of giant armadillo females with single off- Rodovia Dom Pedro I, km 47, 12960-000, Nazaré Paulista, São spring in Colombia. Paulo, Brazil; and Houston Zoo, 6200 Hermann Park Drive, Houston, Conservation strategies for giant armadillos must be TX 77030, USA based on the characteristics of their ecology and biology Danilo Kluyber: Instituto de Conservação de Animais Silvestres (ICAS), Rua Licuala 622, 79046150, Campo Grande, Mato Grosso do that impact their population dynamics the most. Analy- Sul, Brazil; and Naples Zoo and Caribbean Gardens, 1590 Goodlette- sis of the population growth rate and its determinants is Frank Rd, Naples, FL 34102, USA key to understanding population dynamics, as population Unauthenticated Download Date | 9/14/19 9:15 PM 2 A.L.J. Desbiez et al.: Giant armadillo reproduction growth rate is the key unifying variable that links the that could allow visual identification of the individual in various aspects of a species’ population ecology (Sibly and the future were collected. Skin biopsies were performed to Hone 2002). A basic understanding of a species’ reproduc- allow genetic kinship studies in the future. tive rate is necessary for the assessment of population Armadillos were implanted with intra-abdominal growth rates. This paper presents some of the first data very-high-frequency (VHF) radio transmitters (IMP 310, on the reproductive behavior of giant armadillos, includ- Telonics, Inc., Mesa, AZ, USA – weight = 38.5 g, i.e. 1.28% ing reproductive seasonality, gestation period, inter-birth of armadillo’s body mass) following the surgical proce- intervals, number of offspring and parental care. It also dures proposed by Hernandez et al. (2010). Once all proce- discusses a possible non-parental infanticide. dures were terminated, anesthesia was reversed through an intravenous injection of naloxone (0.04 mg/kg), yohimbine (0.125 mg/kg) and flumazenil (0.025 mg/kg). Animals were released in the same burrow they were cap- Materials and methods tured from. Study area Animal monitoring This study was carried out between July 2010 and July 2017, in a 300-km2 area that includes seven traditionally Animals were monitored for an average of 15 days per managed cattle ranches (19° 16′ 60″ S, 55° 42′ 60″ W) in month. Monitoring was accomplished through VHF telem- the Nhecolândia sub-region of the Brazilian Pantanal. The etry, to find the burrow using the homing-in to the animal landscape is a mosaic of different habitats that include technique (Samuel and Fuller 1994). Once encountered, open grassland, scrub grassland, scrub forest and semi- the burrow location was recorded using a handheld global deciduous forest. The historical mean temperature is positioning system (GPS) device. To allow the identifica- 25.4°C, climate is classified as semi-humid tropical (Aw), tion and the comparison between “regular” burrows and with a hot, rainy season (October to March) and a warm “nesting” burrows (i.e. burrows used to shelter infants), drier season (April to September) during which tempera- the burrow entrance height and width were measured fol- tures may drop due to cold fronts from the South (Soriano lowing the protocol used by Desbiez and Kluyber (2013). 2000). The area lacks permanent watercourses, and there In addition, the amount of sand in front of a burrow was is widespread flooding during the rainy season. Tradi- measured and characterized by the height of the sand tional extensive cattle ranching is practiced in the area, mound (from the soil level to the top of the mound). and there are no paved roads. Hunting and habitat loss Animals were captured and anesthetized under the license is limited, and the overall anthropogenic threats are low. number 27587-8 from the Brazilian Federal Environmental Protection Agency (ICMBIO), which regulates and protects wildlife in the country. Capture and handling We performed active searches by foot or pickup trucks Camera trapping looking for signs (tracks, feces and burrows) of giant arma- dillos that could lead to a burrow in use. Animals were We used camera traps to record the different types of captured using iron funnel traps that were placed in the behavior performed by individuals with and without off- entrance of burrows with evidence of recent activity. We spring near burrow entrances and eventual visits of other captured 26 giant armadillos in the study area, 14 females individuals to those burrows. When burrows in use were (10 adults and four subadults) and 12 males (seven adults, encountered, either through telemetry or active searches, four subadults and one juvenile). Once captured, animals camera traps were placed in front of its entrances and set were temporarily placed in ventilated wooden boxes and to take a succession of pictures (Reconyx® HC-500, Holmen, then anesthetized through an intramuscular injection in WI, USA) or set to video mode (Bushnell® Trophy Camera the hind limbs. The anesthetic protocol was composed of Brown Model, Overland Park, Kansas, USA and Reconyx® butorphanol 10 mg/ml (0.1 mg/kg), detomidine 10 mg/ml XP9, Holmen, WI, USA) as described in Desbiez and Kluyber (0.1 mg/kg) and midazolam 5 mg/ml (0.2 mg/kg) (Kluyber (2013). Camera traps remained set in front of burrows for 2016). While immobilized, information on age, sex, any at least 40 days after the monitored individuals left it (5769 evidences of reproductive activity and any natural marks camera traps/night). Through this method, we were able to Unauthenticated Download Date | 9/14/19 9:15 PM A.L.J. Desbiez et al.: Giant armadillo reproduction 3 record the time an individual entered and exited the burrow of known age. The patterns of coloring and behavioral and estimate the time spent inside and outside the burrow change chronicled were used in an attempt to estimate the in each outing.