Presence and monitoring of albino giant anteaters ( Myrmecophaga tridactyla ) in the Cerrado savanna Presença e monitoramento de tamanduás-bandeira ( Myrmecophaga tridactyla ) albinos no Cerrado

: Here we present two cases of albinism in giant anteaters from the same area in Central Brazil. The two juvenile individuals presented light-colored fur, unpigmented eyes, and pinkish skin around the eyes, ears, and snout tip. One of the individuals died before achieving adulthood. Given that albinism might affect individual behavior, survival, and fitness, we have started the GPS monitoring of one of the albino individuals. We present the results of our initial health assessment of the individual, showing that its parameters are generally within normality. We also present opportunistic observations showing that its atypical coloration did not affect intraspecific interactions, i


INTRODUCTION
Atypical coloration in animals is caused by genetic conditions that cause abnormal production of pigmentation and can have fitness consequences for individuals. The three most observed patterns are albinism, leucism, and melanism. Albinism is the total absence of skin and retina pigmentation (Hiller, 1983). Partial albinism occurs when there is a reduction in pigmentation in the skin, fur, or eyes. Leucism is a form of partial albinism where the animal presents typical coloration in their eyes, but their skin or hair contains no color pigment (Forrest & Naveen, 2000). In contrast, melanism is characterized by an excessive deposition of pigmentation. These are rare genetic conditions generally related to recessive alleles (McCardle, 2012;Summers, 2009) and can become more frequent in small populations with higher inbreeding rates (Cuxim-Koyoc et al., 2020;Kuras et al., 2001).
Animal coloration can have an important role in intraspecific behavior and is one of the main factors responsible for crypsis, i.e., an animal's ability to blend with their surroundings and be unnoticed by their predators and prey. Hence, atypical coloration tends to have negative effects on animal survival and fitness (Cuxim-Koyoc et al., 2020;Uieda, 2000). However, when presented in the species with cryptic or nocturnal habits, or those with efficient defense mechanisms, individuals have higher chances of survival (Sazima & Di-Bernardo, 1991). Coat color also plays a key role in filtering solar radiation. Hence, coat color abnormalities could increase skin cancer propensity (Marçon & Maia, 2019) and also affect heat gain, which, in turn, could affect behavioral and metabolic thermoregulation mechanisms (Stuart-Fox et al., 2017;Walsberg, 1983). Furthermore, because pigment cells are essential for the proper functioning of sensory organs such as eyes and ears, color mutations can also negatively affect sensory organs and nerves (Reissmann & Ludwig, 2013). Unfortunately, most records of color abnormalities are presented as opportunistic photographic or video records (e.g., LaPergola, 2019; Uieda, 2000), and few studies have been able to monitor these individuals in the wild to understand how this condition affects their behavior and survival rates (e.g., Tavares et al., 2020).
The giant anteater (Myrmecophaga tridactyla Linnaeus, 1758) is a large sized insectivorous mammal (22-45 kg) that can reach up to 2 m in length . The species is broadly distributed throughout the Neotropics and inhabits a variety of habitats, from grasslands to forests . They are mostly nocturnal but increase diurnal activity when experiencing lower temperatures (Camilo- Alves & Mourão, 2005;Giroux et al., 2021). Due to their size and defense mechanisms, the only animals known to predate on adult giant anteaters are jaguars (Panthera onca Linnaeus, 1758) and pumas (Puma concolor Linnaeus, 1771). Although there is high phenotypic variation in fur coloration along the distribution of lesser anteaters of the genus Tamandua Rafinesque, 1815 (Hayssen, 2011), coat color of giant anteaters presents a consistent pattern with small intraspecific variation along its distribution (Möcklinghoff et al., 2018).
In this study, we present two cases of albinism in giant anteaters from the same area in Midwestern Brazil and discuss the potential relationship between the cases. Given that albinism might affect individual behavior, survival, and fitness, we present the initial conditions and preliminary results of a monitoring program for one of these albino individuals.

STUDY AREA
This study is being conducted at Barra Bonita Ranch, Arapuá district, Três Lagoas municipality, Mato Grosso do Sul state, Brazil ( Figure 1). The ranch is dedicated to cattle ranching activity, being covered mainly by pasturelands, and is inserted in a region of Cerrado savanna that has undergone severe degradation, through the conversion of native vegetation into pastureland and Eucalyptus plantations, with only a few remnant native savanna fragments (Reynolds et al., 2016).
The Cerrado is one of the world's largest Biodiversity Hotspots (Myers et al., 2000), but it has one of the lowest levels of protection (1.6% strictly protected). In Mato Grosso do Sul state, only 16% (58,459 km 2 ) of native Cerrado remains pulverized in small fragments (average ~9 ha) within an agricultural matrix (Reynolds et al., 2016).

FIRST RECORD
In August 2021, an individual giant anteater with atypical coloration was recorded walking alone in a pasture area (photographed and filmed; Figures 2A and 2C 1 ) by two ranch workers (Valdemar da Silva and Elias Menossi). Based on video and photo records, it is possible to state that the individual of unknown sex presented hypopigmentation in its fur, skin, and eyes, which are characteristic of albinism. The record was publicly shared by a local news website (Arapuá News, 2021 After three days of active search, we encountered the carcass of an albino juvenile individual near the location of the first sighting by ranch workers (approx. 200 m; 20° 51' 5.5" S, 52° 02' 6.7" W; Figure 3), which makes us assume this is the same albino individual that had last been seen alive on August 2 nd , 2021.

SECOND RECORD
One year later (August 22 nd , 2022), a second juvenile albino individual was seen by the same ranch workers in the same area and reported directly to our team. This individual seemed younger than the first one, as it was still on its mother's back ( Figure 2B), a behavior observed in individuals under 6 months of age (Jerez & Halloy, 2003). Our team visited Barra Bonita Ranch (September 5 th 2022) and captured both mother and cub using longhandled dip nets. Individuals were anesthetized through intramuscular injection and had samples of tissue, blood, hair, feces, and swabs (nasal, oral, ear, and rectal) collected. Capture and handling procedures followed . Finally, to enable periodic health assessments and behavioral monitoring, during anesthesia the albino juvenile was equipped with a GPS harness (TGW4570-4 Iridium GPS; Bertassoni et al., 2022). This will allow us to understand the potential consequences of albinism for individual behavior, physical conditions, and survival. To ensure that the harness does not harm the individual and is fit to the body, periodic recaptures of the individual are being performed for adjustment of the harness' size and health assessments.
To assess the potential relatedness between the albino individuals recorded in the same area, tissue and  hair samples from both albino individuals and from the female that was nursing the second one, were sent to the Molecular Biodiversity and Conservation Lab at the University of São Carlos for genetic kinship analysis. Blood samples were subjected to hematology and biochemistry analysis to assess the health conditions of the albino individual and its mother.

ETHICAL GUIDELINES
This study was performed under License No. 53798-16 from the Chico Mendes Institute for Biodiversity Conservation, granting permission for individual capture and handling, and biological sample collection and storaging. All procedures followed the Guidelines of the American Society of Mammalogists for the use of wild mammals in research (Sikes & ACUC, 2016).

RESULTS AND DISCUSSION
In this study, we actively recorded two juvenile individuals with light-colored fur and unpigmented (red) eyes, characteristic of albinism, in the field. The skin around the eyes, ears, and tip of the snout were light and pinkish

FIRST RECORD
We encountered the albino anteater's carcass in an advanced stage of decomposition, with no internal tissues or organs, and only bones and pieces of skin that could be detected (Figure 3). Based on our previous studies with carcass degradation along highways (Ascensão et al., 2021), this level of degradation indicates that the death of the individual is most likely to have occurred more than two weeks before we encountered it. In addition, the condition of the carcass, with scattered pieces of skin and fur, and fractured bones, could be a sign of predation. Finally, the examination of the carcass with atypically light-colored fur allowed us to confirm that it was a young giant anteater (confirmed by epiphyseal plates on bones; Figure 3C

SECOND RECORD
The second individual was recorded in the same area as the first one, one year later (20° 51' 40" S, 52° 01' 49" W). Based on its size and behavior (riding on its mother's back; Figure 2B), the albino individual #2 seemed younger than #1 and was estimated to be 4-5 months old (ZIMS, 2023).
The albino individual and its mother, which presented typical fur and skin coloration ( Figure 2B), were captured on September 5 th 2022, for the collection of biological material (blood and skin), a health assessment, and the fitting of the juvenile with a GPS harness. Upon close inspection, it was possible to record that individual #2 presented a complete absence of pigmentation, with red eyes, a pinkish tongue (the usual coloration is blackish or brown), and unpigmented claws (Figures 2D and 4). Skin tissue was stored at the aforementioned biological collection under the ids #MAM_1043 (albino juvenile) and #MAM_1044 (the albino's mother). Both the mother (body mass = 28 kg) and the albino cub (body mass = 5.6 kg) showed good body condition and blood parameters generally within normality (Table 1; Alves et al., 2023). The alkaline phosphatase of the juvenile was over the normal range, but that is a common pattern among juvenile individuals (Alves et al., 2023). Serum alkaline phosphatase (ALP) activity is used primarily as an indicator of hepatic disease. However, there are numerous non-hepatic factors that can increase serum ALP activity (Fernandez & Kidney, 2007), such as bone mineralization (Vimalraj, 2020), which can explain higher ALP values in growing animals. Both individuals showed blood platelet numbers that indicate thrombocytosis. Thrombocytosis is a multifactorial condition, and some of its causes can be associated with an inflammatory response (Neel et al., 2012). In the present study, the animals did not show signs of inflammatory disease, however, we will repeat these exams to confirm a potential diagnosis, as the other leucogram results do not show any indication of inflammation.
Atypical coloration can affect fitness and survival in mammals (Cuxim-Koyoc et al., 2020;Uieda, 2000), and albinos of most species tend to be rapidly removed from populations through predation (Espinal et al., 2016). Albino individuals lack pigmentation in their eyes which can result in poor eyesight (Summers, 2009) and could hinder the detection of resources and predators by visually oriented species, reducing their fitness (Espinal et al., 2016). However, due to the opportunistic nature of most records of albinism, there is little evidence of its ecological consequences in the wild, and most discussions regarding its fitness consequences are speculative (Espinal et al., 2016). Giant anteaters are primarily smell-oriented species that feed on colonial insects .Hence, albinism is unlikely to affect the individual's ability to feed, but it could potentially make it more prone to predation. Much like other mammals, the natural coloration of giant anteaters is key to their camouflage in forests and savannas (Nedyalkov et al., 2014). The lighter coloration of albino and leucistic animals can make individuals more conspicuous in the landscape and more prone to predation (Sandoval-Castillo, 2006). In general, the survival of albino individuals until adulthood is low (McCardle, 2012). Nevertheless, this disadvantage can be offset in highquality habitat (Kehas et al., 2005), with more vegetation cover and high-quality food resources (Peles et al., 1995). Unfortunately, this is not the case in our study region, and one of the juvenile albino individuals here reported was encountered dead in a degraded savanna landscape, which could be the result of a predation event. Hence, albinism in giant anteaters could be considered a maladaptive trait leading to premature death, however, further observations would be needed to confirm this. Color abnormalities can also affect intraspecific relationships, e.g., parental care and mate choice (McCardle, 2012). However, we did not observe any abnormalities in the parental care behavior of the adult female with normal coloration patterns towards her albino young. During the first two and a half months of GPS monitoring of the albino individual captured in 2022, the female cared for her young as expected according to his life stage, carrying him on her back, nursing him and sleeping together . Afterwards, the albino juvenile started foraging by himself, as expected according to his estimated age. The last time it was seen on its mother's back was on November 21 st 2022.
In the future, the movement tracking of the albino giant anteater will also allow us to understand the consequences of this color abnormality in the species thermoregulatory mechanisms. Like other xenarthrans, giant anteaters have low basal metabolic rates when compared to other placental mammals of similar size, limiting their physiological capacity for thermoregulation (McNab, 1985). Hence, giant anteaters often rely on behavioral mechanisms for thermoregulation (Camilo-Alves & Mourão, 2005;Giroux et al., 2021). Because hair coat pigmentation plays a key role in filtering solar radiation, we expect albino giant anteaters to have different dynamics of heat gain, which could affect their thermoregulation mechanisms (Stuart-Fox et al., 2017;Walsberg, 1983) and could be reflected in their activity and habitat selection patterns (Camilo- Alves & Mourão, 2005;Giroux et al., 2021). Hence, the GPS-monitoring of this albino individual could provide key insights on the role of coat color in the thermoregulation strategies of this iconic tick-furred mammal in tropical savannas.
In this study, we recorded two albino individuals in the same area (1.2 km apart) over the course of a year. Giant anteaters occur at low densities (< 1 individual/ km 2 ;  and, in general, the female is responsible for hearing one pup per year . Hence, it is possible that both albino individuals share the same mother or some other close relationship. Kinship analysis based on the collected tissue samples will be performed by the Laboratory of Molecular Biodiversity and Conservation (UFSCar), which will allow us to test this hypothesis. Furthermore, the occurrence of two albino individuals in the same area raises concerns regarding the population's genetic diversity. That is because the frequency of albinism in a population can be associated with population size, with smaller populations leading to higher rates of inbreeding, which increases the chances of the manifestation of recessive alleles (Kuras et al., 2001;Nedyalkov et al., 2014).
Large mammal species with highly specialized feeding behaviors and solitary habits, such as giant anteaters, are expected to suffer genetic consequences from habitat loss and fragmentation (Lino et al., 2019). The Cerrado biome is highly degraded due to human activities, and very little native vegetation remains within its landscape, which suffers from increasing urbanization and is dominated by agricultural lands and transected by an extensive road network (Reynolds et al., 2016). Giant anteaters have been experiencing population declines throughout their distribution due to habitat loss, roadkill, fire, humanwildlife conflicts, and sometimes hunting, and are classified as Vulnerable by the Species Survival Committee of the International Union for Conservation of Nature (Miranda et al., 2014). In Mato Grosso do Sul state, road kills have been shown to significantly reduce population growth rates, being a real threat to the persistence of giant anteater species in the region (Ascensão & Desbiez, 2022). In addition, recent genetic demographic analysis has shown that the current population of giant anteaters in this region presents a significant inbreeding coefficient value and a moderate level of genetic diversity that are likely related to a recent bottleneck (i.e., decrease) in the population (Barragán-Ruiz et al., 2021). Hence, the cases of albinism reported in this study might be additional evidence of the population decline and loss of genetic diversity in this highly degraded part of the Cerrado. This highlights the urgency of the implementation of conservation measures to cease further population declines of giant anteaters in the Cerrado of Mato Grosso do Sul state.