Tolypeutes Research Articles

Local Ecological Knowledge on the Natural History and Human–Fauna Relationships of the Brazilian Three-banded Armadillo (Tolypeutes tricinctus) in Northeast Brazil

Local ecological knowledge (LEK) can be a valuable source of information about species’ biology and their conservation, especially for threatened and poorly known species, such as the Brazilian three-banded armadillo ( Tolypeutes tricinctus). Here, we gathered information about the natural history and human–fauna relationships of T. tricinctus based on the LEK of residents from a rural community in northeast Brazil, where a population of T. tricinctus has been recently discovered. To understand LEK, we used participatory transect walks, semi-structured interviews, and a member-checking workshop. T. tricinctus was considered a locally abundant and widespread species, primarily nocturnal, highly popular, and not among the most hunted species. Our findings have important implications for the understanding of T. tricinctus biology and conservation. First, they show that, although T. tricinctus is highly threatened by hunting, there are still localities where it is not among the most hunted species, where it may still be common. Second, as T. tricinctus is a locally common and popular species, research and participatory science projects may be feasible in the area. Moreover, to increase sampling effectiveness, research projects can consider aspects of T. tricinctus biology identified in this study. In conclusion, our findings reinforce the importance of ethnobiology assessments to improve knowledge about species’ biology and inform local research and conservation efforts.

Structural abnormalities in Paraguayan southern three-banded armadillos Tolypeutes matacus (Chlamyphoridae)

Two structural abnormalities are reported in southern three-banded armadillos Tolypeutes matacus (Chlamyphoridae) from Paraguay. Additional reports of individuals with amputated legs are noted, and a potential explanation for the frequency of such occurrences associated with predation and their defensive behaviour is hypothesized. This is the first documented report of a band anomaly for adults of this species.

Effects of Quaternary climatic oscillations over the Chacoan fauna: phylogeographic patterns in the southern three-banded armadillo Tolypeutes matacus (Cingulata: Chlamyphoridae)

Abstract The southern three-banded armadillo, Tolypeutes matacus, is one of the most representative species of the South American Chaco region. The susceptibility of this species to climatic changes and its good number of paleontological records has led to the study of their range dynamics for untangling the effects of Quaternary oscillations. These studies yielded contradictory results, suggesting expansion processes under opposite conditions: some during glacial periods and others during interglacial periods. Here, we assess the population structure of T. matacus in Argentina based on mitochondrial genes, and estimate demographic and spatial dynamics that contribute to unveiling the evolutionary process that moulded its biogeography. We found no clear phylogeographical breaks, although there were differences in the composition and frequency of haplotypes between the northern and southern localities studied. Demographic inferences indicate that the species has undergone population and range expansion processes. The higher diversity found in the north and the spatial diffusion analysis allow us to infer a north–south direction of this expansive process. Our results yield essential evidence for disentangling the evolution of this Chacoan species linked with Quaternary climates and provide genetic information about its populations that should be taken into account for the conservation of this threatened mammal.

Integrating Measures of Fecal Glucocorticoid Metabolites and Giving-Up Densities to Assess Adrenocortical Activity and Well-Being in Zoo-Housed Three-Banded Armadillos (Tolypeutes matacus).

To monitor adrenocortical activity in zoo-housed species, we propose using physiological and behavioral indicators that are non-invasive and practical to implement. We explore this model in the southern three-banded armadillo (Tolypeutes matacus; armadillo), which is a near-threatened species commonly found in zoos. We aimed to (1) deploy food patches to quantify foraging behavior (via giving-up densities, GUDs); (2) determine the effects of food patch and environmental modifications on individuals' GUDs and adrenocortical activity (via fecal glucocorticoid metabolites, FGMs); and (3) examine the relationship between GUDs and FGMs. Three males and four females received food patches under varying experimental conditions at the Lincoln Park Zoo (Chicago, IL, USA). Fecal samples were collected before, during, and after foraging experiments to examine FGMs. Armadillos did not respond to patch modifications but did forage more when given increased cover. Individual mean FGMs and GUDs were highly variable, and individuals had consistent FGM and GUD ranks across experiments. FGMs and GUDs did not vary across the experiments nor did they relate to each other. Armadillos and species with a limited behavioral repertoire (i.e., constant movement) can benefit from this multi-trait model to determine the effect of environmental modifications on individuals and provide meaningful information about adrenocortical activity.

Fleas and lesions in armadillo osteoderms.

Armadillos are bitten by several species of flea. Females of the genus Tunga penetrate the epidermis and when in place are fertilised by males, after which the abdomen swells enormously to form a 'neosome'. Within the penetrans group, T. perforans, makes lesions that perforate the osteoderms within the integument to form ~3 mm diameter cavities occupied by a discoid neosome. We examined these lesions in carapace material from animals which had died in the wild to see whether we could recruit evidence as to how they may be generated, either by the insect or by the host. We studied one species without such lesions, the nine-banded armadillo Dasypus novemcinctus, and two species with, the greater hairy armadillo Chaetophractus villosus and the southern three-banded armadillo Tolypeutes matacus, both showing the characteristic 'flea bite' holes in the external surfaces of the osteoderms. Samples were studied by three-dimensional backscattered electron mode scanning electron microscopy and X-ray microtomography. Both methods showed resorption pit complexes in the external surfaces of the osteoderms characteristic of those made by osteoclasts in active bone resorption. Lesions involved both the syndesmoses (sutures) between adjacent bones and the central regions of the osteoderms. Many lesions showed extensive repair by infilling with new bone. We conclude that the T. perforans neosome creates a local host response which causes bone resorption, creating the space in which it can grow.

From Fairies to Giants: Untangling the Effect of Body Size, Phylogeny, and Ecology on Vertebral Bone Microstructure of Xenarthran Mammals.

Trabecular bone is a spongy bone tissue that serves as a scaffolding-like support inside many skeletal elements. Previous research found allometric variation in some aspects of trabecular bone architecture (TBA) and bone microstructure, whereas others scale isometrically. However, most of these studies examined very wide size and phylogenetic ranges or focused exclusively on primates or lab mice. We examined the impact of body size on TBA across a smaller size range in the mammalian clade Xenarthra (sloths, armadillos, and anteaters). We µCT-scanned the last six presacral vertebrae of 23 xenarthran specimens (body mass 120 g-35 kg). We collected ten gross-morphology measurements and seven TBA metrics and analyzed them using phylogenetic and nonphylogenetic methods. Most metrics had similar allometries to previous work. However, because ecology and phylogeny align closely in Xenarthra, the phylogenetic methods likely removed some covariance due to ecology; clarifying the impact of ecology on TBA in xenarthrans requires further work. Regressions for Folivora had high P-values and low R-squared values, indicating that the extant sloth sample either is too limited to determine patterns or that the unique way sloths load their vertebral columns causes unusually high TBA variation. The southern three-banded armadillo sits far below the regression lines, which may be related to its ability to roll into a ball. Body size, phylogeny, and ecology impact xenarthran TBA, but parsing these effects is highly complex.

Defining priority areas for conservation of poorly known species: A case study of the endemic Brazilian three-banded armadillo

Abstract Conservation of poorly known species is challenging as lack of knowledge on their specific requirements may hamper effective strategies. Here, by integrating biogeographical and landscape analyses, we show that informed actions can be delineated for species with limited presence-only data available. We combine species distribution and connectivity models with temporal land cover changes to define priority areas for conservation of the endemic Brazilian three-banded armadillo, one of the most threatened xenarthrans that was once considered extinct in the wild. We revealed that areas of savanna and grassland are the most suitable habitats for the species and that uplands in the Caatinga ecoregion have a greater likelihood for dispersal. The few remnant armadillo populations are spatially associated with core areas of natural vegetation remnants. Worrisomely, 76% of natural core areas were lost in the past 30 years, mirroring the species’ severe population decline. Preserving the remnant core natural areas should be a high priority to ensure the species’ survival. We highlight key areas for proactive and reactive conservation actions for the three-banded armadillo that will benefit other threatened sympatric species. Our integrative framework provides a set of valuable information for guided conservation management that can be replicated for other poorly known species.

The Brazilian three-banded armadillo is widely distributed in a human-modified landscape in northeastern Brazil

The Brazilian three-banded armadillo is widely distributed in a human-modified landscape in northeastern Brazil

Reconstructing the distribution of Chacoan biota from current and past evidence: the case of the southern three-banded armadillo Tolypeutes matacus (Desmarest, 1804)

Reconstructing the distribution of Chacoan biota from current and past evidence: the case of the southern three-banded armadillo Tolypeutes matacus (Desmarest, 1804)

Aroma-dillo or Area-dillo? An examination of armadillos’ sensory modality bias

Many species of armadillo demonstrate impressive navigation abilities and may compensate for poor eyesight with a strong sense of smell. We examined which modality four three-banded armadillos and one hairy armadillo prioritized when two cues (olfactory or spatial) previously associated with reward were put in conflict. The armadillos learned to approach one of two locations - each paired with a distinctive scent - for reward. When the scent cues were reversed, the armadillos demonstrated a strong bias for attending to the location cue over the scent cue. Therefore, a follow-up test presented them with the same scents and assessed their spontaneous preferences. Although the armadillos did not show an immediate preference for the previously rewarded scent, they did learn to discriminate two novel scents when they were placed in a circular arena containing two tins - each scented with a unique scent. They learned to selectively open the tins containing reward based on scent. This result indicates that their bias towards location cues was not due to an inability to discriminate between scents. Armadillos may attend to either location or scent but may prioritize location when both cues are equally predictive.

Cephalic shield morphology as species diagnostic trait and individual natural mark in three-banded armadillos (Tolypeutes; Cingulata: Chlamyphoridae)

Abstract Previous studies have suggested species- and individual-specific morphologies of cephalic shields of three-banded armadillos (Tolypeutes spp.). Central cephalic scutes would form discrete lines; the first two posterior lines being composed of one scute (1-1) in Tolypeutes matacus and one followed by two scutes (1-2) in Tolypeutes tricinctus. However, conclusions were limited to a few specimens and the T. tricinctus pattern was later observed in T. matacus. Here, we assessed the potential use of the morphology of the cephalic shield as a species diagnostic trait and individual natural mark in three-banded armadillos by quantifying their patterns in museum (n = 71) and field (n = 82) specimens. In total, 93% of T. matacus and 88% of T. tricinctus specimens presented the respective species’ character states. All specimens could be individualized based on a visual comparison of their cephalic shields. Our findings show that the morphology of cephalic shields is a species diagnostic trait and an individual natural mark in three-banded armadillos. Therefore, we add an accessible character for species diagnosis in Tolypeutes and provide an alternative to artificial marks that presents virtually no associated cost and damage to animal welfare and can be reliably applied in ecological and participatory science projects.

Distress vocalizations in five species of armadillos (Xenarthra, Cingulata)

Abstract Distress vocalizations are emitted by animals experiencing extreme physical distress, such as when caught by a predator. These signals are emitted by numerous and phylogenetically distant vertebrate species and are composed of sequences of broadband and high-amplitude notes. In this study, we provide the first acoustic characterization of distress vocalizations in four armadillo species: pink fairy armadillo (Chlamyphorus truncatus), greater fairy armadillo (Calyptophractus retusus), Southern three-banded armadillo (Tolypeutes matacus), and Chacoan naked-tailed armadillo (Cabassous chacoensis). We also recharacterized the weeping call of the screaming hairy armadillo (Chaetophractus vellerosus) to compare vocalizations, discuss potential homologies, and examine possible causes of structural and acoustic similarities among these species. In three species the vocalizations were sequences of exhaled notes that differed in their fine spectral structure (exhaled harmonic notes in C. retusus, and exhaled harsh notes in C. truncatus and T. matacus). The vocalization of C. chacoensis was composed of exhaled harsh and inhaled harsh notes that occurred alternately and continuously in a quick sequence. Based on the mode of production and acoustic similarity, we propose that the notes of C. retusus and C. truncatus would be homologous to the conspicuous crying notes of C. vellerosus. The exhaled harsh notes of T. matacus and C. chacoensis may also be homologous to the crying notes of C. vellerosus, but the notes of T. matacus are quite different in various acoustic parameters. Furthermore, the inhaled and exhaled harsh notes of C. chacoensis are similar to the inhaled and exhaled sobbing notes of C. vellerosus, making assessments of homologies uncertain in these species. Because a common motivational state (physical distress) underlies these vocalizations, we propose that the notable differences in body size and habitat preferences of the armadillos could represent potential drivers of the acoustic divergence among their vocalizations.

First records of Brazilian three-banded armadillo (Tolypeutes tricinctus, Mammalia, Cingulata, Chlamyphoridae) predation by jaguar (Panthera onca, Mammalia, Carnivora, Felidae)

The jaguar Panthera onca and the Brazilian three-banded armadillo Tolypeutes tricinctus are two threatened mammals that coexist in the Caatinga dry forests and the Cerrado savannas of Brazil. Yet, to the best of our knowledge, interactions between these species have not been reported in the literature. Here, we present the first records of P. onca predation on T. tricinctus from two different areas in the Caatinga in northeastern Brazil. We showed that P. onca can pierce the hard carapace of T. tricinctus, which may be possible due to its distinctly strong bite and associated predation behavior. We argue that P. onca may be the most adapted non-human predator to feed on T. tricinctus, and that the smaller body sizes of P. onca individuals in the Caatinga may increase their likelihood to feed on smaller prey, including T. tricinctus. Thus, the originality of our records is probably more related to insufficient research in the areas where these species coexist than to the rarity of this interaction.

Ecology and social biology of the southern three-banded armadillo (Tolypeutes matacus; Cingulata: Chlamyphoridae)

Abstract Basic knowledge of species biology and ecology is essential for the assessment of species conservation status and planning for efficient conservation strategies; however, this information is not always readily available. Here we use movement behavior to understand the ecology and social biology of the poorly known southern three-banded armadillo (Tolypeutes matacus). We used VHF and GPS telemetry to monitor 26 individuals from two sites in the Pantanal wetlands of Brazil. We characterized armadillo activity patterns, evaluated the relationship between sex and body mass with home range size and mean daily distance traveled, and examined home and core range overlap. Three-banded armadillos were active on average for 5.5 ± 2.8 h/day, with most of their activity concentrated in the first half of the night. Adult males were heavier and had larger home ranges than adult females. Home range size scaled positively with body mass for males, but not for females. Core ranges for females overlapped little (< 1%) regardless of age, but home ranges for males overlapped both with other males (12%) and females (18%). Our data suggest that three-banded armadillos are mainly a nocturnal species. Home range and spacing patterns point to a generally asocial behavior and a polygynous or promiscuous mating system. We hope that the data generated as a result of this project will contribute to this species’ conservation in Brazil and elsewhere by guiding future management and research efforts.

Effects of air temperature on habitat selection and activity patterns of two tropical imperfect homeotherms

In this study, we aimed to evaluate how air temperature is related to variation in activity patterns and habitat selection by two species of tropical armadillos, which are imperfect homeotherms. Although their behaviour is little studied, armadillos provide valuable models for understanding how physiology affects mammalian behaviour in response to environmental changes. We used GPS devices to track yellow armadillos, Euphractus sexcinctus, and southern three-banded armadillos, Tolypeutes matacus, at three sites of the Pantanal wetlands, Brazil. We used linear mixed-effects models to evaluate the variation in the timing and duration of activity patterns according to changes in air temperature. We fitted step selection functions to evaluate the effects of cover type, diel cycle and air temperature on armadillo habitat selection. Our models suggest that E. sexcinctus activity during the daytime decreases as air temperature increases. In contrast, T. matacus shows less variation, maintaining a predominantly nocturnal activity pattern. However, as air temperature decreases, activity periods of T. matacus are of shorter duration and peak earlier in the day. Both species should select forested areas when experiencing air temperatures outside their thermoneutral zones, as these areas act as thermal shelters. This study provides specific examples of the dynamic nature of activity patterns and habitat selection, and illustrates how thermal constraints, which vary dynamically over the daily cycle and among days, can alter behaviour. Our results highlight the importance of habitat heterogeneity for the long-term conservation of animal species that rely on behaviour to achieve adequate thermoregulation.

Intestinal parasites of Tolypeutes matacus, the most frequently consumed armadillo in the Chaco region.

The southern three-banded armadillo Tolypeutes matacus (Desmarest, 1804) is distributed from eastern Bolivia, south-west Brazil, the Gran Chaco of Paraguay and Argentina, and lives in areas with dry vegetation. This armadillo is one of the most frequently consumed species by people in this area. The objective of this work was test for zoonotic species among helminths in 12 intestinal tracts of T. matacus in a locality from the Argentinean Chaco (Chamical, La Rioja province). The parasites were studied with conventional parasite morphology and morphometrics, and prevalence, mean intensity and mean abundance were calculated for each species encountered. In the small intestine, seven species of nematodes and two species of cestodes were identified. In the large intestine, two species of nematodes were recorded. We did not find zoonotic species but have added new host records. This study in the Chaco region thus contributes to growing knowledge of the parasite fauna associated with armadillo species in this region.

Yes, they can! Three-banded armadillos Tolypeutes sp. (Cingulata: Dasypodidae) dig their own burrows

It is believed that the two species of Tolypeutes Illiger, 1811are the only armadillos that do not dig their own burrows, and that these species simply re-use burrows dug by other species. Here, we show that Tolypeutes matacus (Desmarest, 1804) and Tolypeutes tricinctus (Linnaeus, 1758) dig their own burrows. We describe the burrows and three other types of shelters used by them, and provide measurements and frequency of use of the different types of shelter. We have studied free-ranging individuals of T. matacus in two locations in Central Brazil and individuals of T. tricinctus in semi-captivity in the Northeast of Brazil. Individuals of T. matacus were found primarily in small burrows (76%), straw nests (13%), shallow depressions covered with leaf-litter (7%) or in straw nests made on shallow depressions (4%). Adult males and females of T. matacus did not differ in frequency of use of different types of shelter. Sub-adults T. matacus used shallow depressions and nests more often (40%) than adults (22%) and nurslings (10%). Nurslings of T. matacus reused the shelters more frequently (66%), than sub-adults (46%) and adults (35%). Adult females reused burrows and other types of shelter more frequently than adult males. Tolypeutes tricinctus rested mainly in burrows and under leaf-litter, but did not dig depressions or build nests. Tolypeutes tricinctus occasionally used burrows dug by Euphractus sexcinctus (Linnaeus, 1758), but T. matacus never used burrows dug by other species. Nursling T. matacus always shared shelter with an adult female therefore, both used shelters with similar frequency. Adult females and nurslings of T. matacus reused shelters in higher frequency. That can be explained by the fact that adult females with offspring tend to remain for consecutive nights in the same burrow when cubs are recently born. Due to their smaller body size, subadult T. matacus used shelter strategies that require less energetic effort more frequently than adults and nurslings. The habit of covering the burrow entrance with foliage and the burrow?s reduced depth, indicates that Tolypeutes use of burrows is more likely to be related to parental care behavior and thermoregulation strategies than to defense mechanisms. We are confident that the burrows used for resting were indeed dug by Tolypeutes because, besides the direct observation of armadillos digging burrows, the measures of the burrows are very distinctive from those presented as characteristic for the co-occurring burrowing species and are congruent with Tolypeutes size and carapace shape. The newly acquired knowledge that species of Tolypeutes dig burrows can be used to increase the well-being of individuals kept in captivity by adapting enclosures to enable their digging behavior. In addition, this information contributes not only to the study of the ecology and natural history of the species, but can shed new light on the study of the anatomy of specialized diggers. Tolypeutes spp. can comprise the least fossorial of all living armadillo species, but they can no longer be classified as non-diggers.

Distribution of tolypeutes illiger, 1811 (xenarthra: cingulata) with comments on its biogeography and conservation.

This study reviews the data available on the distribution of three-banded armadillos of the genus Tolypeutes, identifying potential geographic barriers and evaluating possible biogeographic processes that may account for the present-day distribution of the species and its conservation status. The database was derived from published records, interviews, and voucher specimens, over a timescale ranging from the fossil record to specimens collected in 2013. A total of 236 localities were recorded, with 68 attributed to Tolypeutes matacus and 168 to Tolypeutes tricinctus. The vegetation within the range of the genus is predominantly a xerophytic mosaic of grassland, savannas, open woodland, and xeric thorn forest. The marine transgressions of the Miocene and the uplifting of the Brazilian Shield may have contributed to the vicariant separation of the ancestral populations of T. matacus, to the west and south, and T. tricinctus, to the north and east. The three-banded armadillo is possibly one of the most threatened of Brazilian mammals, considering the low number of recent records and the fact that it is hunted intensively throughout its range.

Football and Biodiversity Conservation: FIFA and Brazil Can Still Hit a Green Goal

ResumoA seleção do tatu‐bola (Tolypeutes tricinctus), uma espécie endêmica e ameaçada do Brasil como o mascote oficial da Copa do Mundo FIFA 2014 é significativa e representa uma grande oportunidade para engajar os parceiros do maior evento esportivo do mundo emu ma agenda efetiva de conservação. Frente ao mal estado de conservação da espécie escolhida e de seu habitat principal, a Caatinga do nordeste do Brasil, nós encorajamos a FIFA e o Governo Brasileiro a incorporarem três ações conservacionistas concretas no legado prometido para a Copa. Ainda há tempo para um grande gol ambiental e provocamos a FIFA e o Brasil a estabelecerem uma meta ambiciosa: para cada gol marcado na Copa, ao menos 1000 hectares de Caatinga devem ser protegidos como parques e reservas.

UTERINE ADENOMYOSIS IN SOUTHERN THREE-BANDED ARMADILLOS (TOLYPEUTES MATACUS)

Uterine adenomyosis was diagnosed in five southern three-banded armadillos (Tolypeutes matacus) from four different zoological collections in North America between 1995 and 2012. Two cases were diagnosed after ovariohysterectomy and histopathologic evaluation of the uteri, and the remaining cases were identified incidentally at the time of postmortem examination. Animals ranged from 5 to 14 yr of age at the time of diagnosis. Of armadillos diagnosed before postmortem examination, clinical signs included weakness, collapse, anemia, and vulvar discharge. Histopathologic evaluation of the uteri revealed well-developed, irregular endometrial glands extending into the myometrium and occasional hemorrhage within these glands. The two cases diagnosed antemortem were successfully treated with ovariohysterectomy. To the authors' knowledge, this condition has not been previously reported in Xenarthra, including armadillos.