No evidence of sex-related differences in the diet of giant anteater in the Brazilian savanna.

Author(s): Tainara Galvao Santana [sup.1], Nina Attias [sup.2], Natalia Teixeira Nascimento [sup.1], Mariáh Tibcherani [sup.3], Mauricio Martins Rocha [sup.4], Arnaud Léonard Jean Desbiez [sup.2] [sup.5] [sup.6]

Author Affiliations:

(1) https://ror.org/0366d2847, grid.412352.3, 0000 0001 2163 5978, Animal Biology Graduate Program, Federal University of Mato Grosso Do Sul (UFMS), , CEP 79070-900, Campo Grande, Mato Grosso Do Sul, Brazil

(2) grid.508412.a, Institute for the Conservation of Wild Animals (ICAS), , Campo Grande, Mato Grosso Do Sul, Brazil

(3) https://ror.org/0366d2847, grid.412352.3, 0000 0001 2163 5978, Ecology Graduate Program, Federal University of Mato Grosso Do Sul (UFMS), , Campo Grande, Mato Grosso Do Sul, Brazil

(4) https://ror.org/036rp1748, grid.11899.38, 0000 0004 1937 0722, Museu de Zoologia, Universidade de São Paulo (USP), , São Paulo, Brazil

(5) https://ror.org/05rw53r38, grid.452921.9, 0000 0001 0725 5733, Royal Zoological Society of Scotland (RZSS), , Murrayfield, Edinburgh, UK

(6) Institute for Ecological Research (IPÊ), , Nazaré Paulista, São Paulo, Brazil

Introduction

The study of animal feeding behaviors allows us to understand the different forms of life, their interactions with other species and their ecological role, which includes regulating ecosystem functions (Redford 1992). Feeding habits are one of the major factors defining the relationships of a species with other organisms and its habitat, hence the importance of dietary studies (Dunlop et al. 2017; Slauson and Zielinski 2017). Specifically, dietary information can provide insights into the resource constraints and requirements of a species, which can directly influence population dynamics, habitat use (McNab 1963), its response to environmental changes, and the measures managers can adopt to promote its conservation (Young et al. 2016; Dunlop et al. 2017).

Feeding habits can be associated with species and individual traits, but also with resource availability, its energetic value and nutritional composition (Lindstedt et al. 1986; Kohl et al. 2015; Bertassoni and Ribeiro 2019). In general, the more specialized the diet, the greater the chance that an animal can be affected by resource availability (Hockey and Curtis 2009). Therefore, research on diet composition and level of specialization can help in the assessment of species extinction risk and provide essential data for planning conservation strategies (Young et al. 2016). Determining the extinction risk of a species must also consider other behavioral factors, such as home range and foraging strategies, which are directly linked to the energy provided by the diet (Futuyma and Moreno 1988; Slauson and Zielinski 2017).

According to optimal foraging theory, there must be balance between energetic cost and intake during foraging activities (Hughes 1979; Futuyma and Moreno 1988). This favors the consumption of prey with the highest energy value possible whenever encountered (Hughes 1979). Therefore, insectivorous mammals, such as the giant anteater (Myrmecophaga tridactyla), the lesser anteater (Tamandua tetradactyla), and the giant armadillo (Priodontes maximus) that feed on prey that generally provides low energy individually, require prey abundance to fulfill their energetic needs (Silva et al. 2019). Termites and ants compose only 2% of insect species but represent at least half of the biomass of terrestrial invertebrates (Rosenberg et al. 2023). Nevertheless, insect prey abundance tends to be associated with resource-rich habitats and is impacted by habitat degradation (Constantino 2002; Carrijo et al. 2009). Hence, insectivorous mammals need to forage in habitats rich in resources to access the volume of prey necessary to provide energy for the endothermic regulation of its temperature and nutritional balance (McNab 1974). This means that insectivorous mammals could be especially affected by habitat degradation and the potential disturbances in resource availability.

Mammalian behavior can also be influenced by intrinsic factors (e.g., gender and life-stage; Di Blanco et al. 2016; Bertassoni and Ribeiro 2019), which can be reflected in feeding habit differences (Lindstedt et al. 1986). For example, sex-related differences in feeding habits have been recorded for several mammalian species, from insectivorous bats to large carnivores such as leopards (Voigt et al. 2018; Haarsma et al. 2023). There are at least three evolutionary theories to explain that. The first is related to morphological sexual dimorphism, which could produce different dietary requirements or enable individuals to explore different resources (Rose 1994). The second is related to differences in reproductive strategies of males and females. For example, the reproductive success of males and females in promiscuous or polygynous reproductive systems is influenced by different factors: females require habitats and food resources that favor offspring survival, and males need resources that offer competitive advantages for reproductive partners (Clutton-Brock 1989; Lazenby-Cohen and Cockburn 1991; Main et al. 1996). Furthermore, females have greater energy demands during gestation, offspring care and lactation (Lindstedt et al. 1986; Rose 1994). Males on the other hand, may be more linked to the availability and distribution of females of the same species (Powell 2000). Thus, the variation in the availability and distribution of resources can influence mammalian mating systems (Clutton-Brock 1989). Finally, habitat and diet are related niche dimensions, which means that the habitat occupied defines the food resources available for individuals (Magioli et al. 2022). Hence, the third theory would be related to the fact that sex-related differences in resource selection favors behavioral differentiation among individuals occupying the same habitat reducing inter-sexual competition for the same resources with potential mates (Rose 1994; Shibuya et al. 2018; Zanni et al. 2021).

Anteaters belong to the Xenarthra superorder, together with armadillos and sloths. The giant anteater Myrmecophaga tridactyla Linnaeus 1758 (Mammalia: Pilosa) weighs up to 39 kg and has a Neotropical distribution, occupying mainly savanna and forested areas (McNab 1985; Di Blanco et al. 2017). They are classified as a myrmecophagous species, specializing in ants (Hymenoptera) and termites (Blattodea; Redford 1986). M. tridactyla, has morphological characteristics that increase its myrmecophagy efficiency, such as an elongated snout, a keen sense of smell, an elongated and protractile tongue, long and strong claws for digging termite mounds, and well-developed mucus salivary glands (McAdam and Way 1967; McNab 1984; Naples 1999). Their specialized diet, low metabolic rates, and low reproductive rate are factors that increase their risk of extinction (Rodrigues et al. 2008).

M. tridactyla presents a promiscuous mating system where the female is solely responsible for parental care. Females have an average of one pup per year, provide long-term maternal care, and carry the cub on their back for 6-12 months after birth, when it reaches about 30% of the mother's body mass (Bertassoni and Desbiez 2021). Hence, females of this species present significantly higher energetic demands related to pregnancy and cub hearing, when compared to males, which could generate differences in dietary behavior. M. tridactyla can be found at high densities in savanna environments, where home ranges of both sexes and age groups highly overlap (Medri and Mourão 2005; Macedo et al. 2010; Bertassoni and Ribeiro 2019; Giroux et al. 2021; Chhen et al. 2023). Therefore, intra-population variation in feeding habits could also be an efficient coexistence mechanism for this myrmecophagous species. Although solitary and asocial, M. tridactyla commonly shares space with conspecifics. However, pairs of females tend to have less encounters than pairs of males or male-female pairs (Chhen et al. 2023). Furthermore, even though the species does not present morphological dimorphism, males present larger home ranges than females (Bertassoni and Desbiez 2021; Chhen et al. 2023), which could generate differences in resource availability and consumption between sexes. These facts evidence the different space use and energy allocation strategies between sexes, which could be reflected in male and female foraging strategies.

Many gaps remain regarding M. tridactyla ecology in the wild, being one of them the effects of habitat degradation on its diet (Montgomery 1985; Redford 1985, 1986; Shaw et al. 1985; Miranda et al. 2014). Unfortunately, savannas suffer with high rates of conversion and degradation (Strassburg et al. 2017). Despite being a biodiversity hotspot, the Brazilian Cerrado savanna has very low levels of protection and 46% of its original cover have already been converted into crops and pasturelands (Rodrigues et al. 2022). The giant anteater is classified as vulnerable by the International Union for Conservation of Nature (IUCN) due to habitat degradation and deforestation, fire, predatory hunting, and roadkill (Miranda et al. 2014).

Given this scenario, the aim of this study was to describe the food items that make up the diet of M. tridactyla in a degraded savanna region, the Cerrado of Mato Grosso do Sul state, Brazil. Population level processes play a key role in species persistence and chances of recovery or survival in face of environmental changes. Hence, understanding sex-related variability in feeding habits can aid in understanding if different demographic groups might be affected differently and how this may influence population survival. Therefore, besides describing population patterns, we aim to understand if the species presents sex differences in their feeding habits.

Methods

Study area

The study, was conducted from October 2018 to April 2020 in the plateau region of Cerrado biome (21° 05' 59" S, 53° 51' 14" W), in the state of Mato Grosso do Sul, Brazil (Fig. 1). The region's climate is classified as tropical with a dry winter according to Koppen's classification system (Aw; Alvares et al. 2013). The Cerrado is a biodiversity hotspot that performs a vital role in sustaining biological diversity, ecosystem services, and fresh water supply in Brazil. The biome's native vegetation cover is composed of grasslands, shrubby grasslands, dense forest and or dry shrublands (Overbeck et al. 2015). However, 88 Mha (46%) of the Cerrado's native vegetation cover have been converted, mostly to enable agricultural and livestock activities, and only 19.8% of the biome remains undisturbed (Silva 2011; Strassburg et al. 2017; Guerra et al. 2020).Fig. 1

Collection sites of fecal samples from 29 individuals of giant anteater (Myrmecophaga tridactyla) in the Mato Grosso do Sul state, Brazil. Map colors indicate native and degraded areas within the Cerrado savanna biome. Samples were collected from October 2018 to April 2020

Sample collection

We collected samples in collaboration with the Anteaters and Highways Project a multidisciplinary conservation initiative led by ICAS, the Wild Animal Conservation Institute ( www.icasconservation.org.br ). Living specimens of M. tridactyla were captured and chemically immobilized with the main objective of placing, adjusting, or removing GPS telemetry harnesses (Telonics Inc, Mesa, USA) for ecological studies. The animals were captured using two long-handled dip nets and anesthetized with a protocol of butorphanol tartrate (Zoetis Indústria de Produtos Veterinários Ltda, São Paulo, Brazil; 0.1 mg/kg), detomidine hydrochloride (Agener-União, Apucarana, Brazil; 0.1 mg/kg), and midazolam hydrochloride (Cristália, Itapira, Brazil; 0.2 mg/kg) described in detail by Kluyber et al. (2021). The physical restraint of the animal during captures frequently causes the animal to defecate, which facilitates the collection of fecal material. Fecal samples were placed in plastic containers with 70% alcohol for storage. Once under anesthesia, animals were sexed and had their weight and biometric information collected (Kluyber et al. 2021). After these procedures, the animals were kept in a ventilated wooden box until complete recovery from sedation and posterior release at their capture site (Kluyber et al. 2021). In addition to the collection of fecal material from live animals, we also collected fecal samples from M. tridactyla roadkills found adjacent to highways (BR-267, BR-262 and MS-040). At the time, samples were collected by the 'Anteater & Highways Project' that were evaluating the impact of roads on wildlife in the state of Mato Grosso do Sul (Fig. 1). These samples were also stored in plastic containers with 70% alcohol.

Sample processing

Fecal samples were oven dried for 20-40 min at 60 â and weighed. We used a point-frame sampling method (Ciucci et al. 2004) to define random subsamples from each sample. The point sampling method consists of homogenizing and spreading the total sample on a metal tray with distance measurements (Ciucci et al. 2004). At the top of the tray with the 0.5 cm marked distances, we placed a sliding device, the point sampling frame, which contains two vertical rods at a 45° inclination in relation to the tray, connected by a horizontal rod. On the horizontal rod, there are five movable metal pins equally spaced (Fig. A, Suppl. Material 1). The method assumes a random distribution of the food items in the sample (Ciucci et al. 2004). Therefore, when sliding the equipment and letting the pins touch an item every 0.5 cm, the item is randomly sampled for analysis. In order to collect material from 50 points of each sample, we dropped the five pins in 10 fixed positions for each sample (Ciucci et al. 2004).

The subsamples were subsequently washed using 0.297 mm and 0.150 mm mesh sieves under running water. We analyzed the processed material with the use of a stereoscopic microscope and separated the items according to identified morphotypes. With the help of expert entomologists and identification keys (e.g., Mathews 1977; Baccaro et al. 2015), we classified items to the lowest possible taxonomic level based on anatomical features such as the mandible and head (Mathews 1977; Baccaro et al. 2015). We used a precision balance (Shimadzu Analytical Balance AUW220) to weigh the biomass of each identified genus or species to the nearest 0.1 mg.

Data analysis

We describe and quantify the items that make up M. tridactyla diet in the Cerrado of Mato Grosso do Sul state and assessed sex related differences in diet. To characterize the individuals' diet, we estimated the relative frequency (RF) and frequency of occurrence (FO) of each food item consumed. We defined the RF of each prey item as the proportion of the total mass of the sample represented by the mass of the given item. We calculated the FO of each food item as the proportion of the total samples analyzed in which that prey was detected (Klare et al. 2011).

We used the prey species accumulation curves to determine if the sampling effort was sufficient to characterize M. tridactyla diet diversity using the function 'specaccum' from vegan R package (Oksanen et al. 2019). We used the "random" method, with 1000 permutations to generate the species accumulation curve and its standard deviation (Fig. 2; Gotelli and Colwell 2001). We also applied the "collector" method to generate the observed species accumulation curve according to our sampling history. Then we fitted an Arrhenius model to the "collector" method to allow the comparison between the observed and expected patterns of prey species richness in relation to the sampling effort (Fig. 2b). Finally, we estimated an extrapolated species richness using a first order Jackknife through using the function "specpool" from the same R package to identify the potential number of undetected prey items. This is an incidence-based estimate that uses the frequency of occurrence of the detected prey items, especially the rare items, to estimate an extrapolated species richness (i.e., how many species might not have been detected through our sampling).Fig. 2

Species accumulation curve according to sample size. (a) Prey species accumulation curve according to the number of individual samples processed. (b) Collector curve (black) and fitted Arrhenius model of estimated species accumulation (red). The models are based on data from 29 giant anteaters (Myrmecophaga tridactyla) fecal samples collected from 2018 to 2020 in the Cerrado of Mato Grosso do Sul state. Prey items were identified to the species level whenever possible. The curves showed an asymptotically stable trend but did not reach a plateau, indicating that new food items could be identified if more samples were examined

Diet similarity between sexes was tested using a Permutation Multivariate Analysis of Variance (PERMANOVA) with 999 permutations using Bray Curtis similarity index (Oksanen et al. 2019). This analysis was performed considering the relative frequency of invertebrate dietary items. To reduce the number of variables, items were grouped by genus and items consumed by only one or two individuals were excluded, resulting in 10 prey types. A graphical representation of the dietary differences between sexes was facilitated by using a non-metric multidimensional scaling (nMDS) with the Bray Curtis similarity index (Dexter et al. 2018) and the data set described above. All analysis were performed within the vegan package (Oksanen et al. 2019) in the R environment (v. 4.2.2.; R Core Team 2022).

Results

We analyzed 29 fecal samples, belonging to 29 adult M. tridactyla (13 M; 16F).

Diet characterization

We found 28 ant morphotypes (Formicidae), belonging to 15 genera, and 14 termite morphotypes (Blattodea), belonging to seven genera (Suppl. Material 2) in the fecal samples analyzed. In addition to these groups, unidentifiable plant and insect fragments, grass seeds (Poaceae) and soil particles also composed the samples (Table 1). Table 1

Frequency of occurrence (FO) and relative frequency (RF) of the prey items identified in the diet of the giant anteater (Myrmecophaga tridactyla; N = 29) based on fecal samples, collected from October 2018 to April 2020, in the Cerrado savanna of Mato Grosso do Sul, Brazil

Family	Genus	Species	FO(%) all	RF(%) all	FO(%) female	FO(%) male	RF(%) female	RF(%) male
Termitidae			89.65	75.85	87.5	92.30	83.61	67.54
	Syntermes		86.20	75.55	81.25	92.31	83.24	67.33
		Syntermes grandis	37.93	27.18	25	53.85	28.43	25.86
		Syntermes molestus	44.83	1.00	37.5	53.85	0.89	1.11
		Syntermes sp.1	48.28	1.69	50	46.15	1.76	1.61
		Syntermes sp.3	75.86	44.39	75	76.92	51.76	36.62
		Syntermes sp.4	51.72	0.62	50	53.85	0.39	0.86
		Syntermes sp.5	3.45	0.11	0	7.69	0	0.22
	Silvestritermes	Silvestritermes euamignathus	3.45	< 0.01	0	7.69	0	< 0.01
	Cornitermes		10.34	0.20	12.5	7.69	0.24	0.16
		Cornitermes cumulans	3.45	0.11	6.25	0	0.21	0
		Cornitermes sp.1	10.34	0.10	12.5	7.69	0.03	0.16
	Rhynchotermes		27.59	< 0.01	31.25	23.08	< 0.01	< 0.01
		Rhynchotermes diphyes	27.59	0.05	31.25	23.08	0.07	0.03
		Rhynchotermes sp.2	6.90	6.34	12.5	0	< 0.01	0
	Diversitermes	Diversitermes sp.	3.45	< 0.01	0	7.69	0	< 0.01
	Velocitermes	Velocitermes sp.	3.45	0.03	6.25	0	0.06	0
	Nasutitermes	Nasutitermes sp.	3.45	< 0.01	0	7.69	0	< 0.01
Formicidae			100	23.08	100	100	15.10	31.62
	Odontomachus		3.45	0.66	6.25	0	1.28	0
		Odontomachus meinerti	3.45	0.65	6.25	0	1.26	0
		Odontomachus sp.1	3.45	< 0.01	6.25	0	0.01	0
	Neivamyrmex	Neivamyrmex swainsonii	13.79	0.02	25	0	0.03	0
	Eciton	Eciton burchelli	3.45	0.01	6.25	0	0.02	0
	Nomamyrmex		6.90	0.1	6.25	7.70	0.12	0.07
		Nomamyrmex esenbeckii	3.45	0.04	0	7.70	0	0.07
		Nomamyrmex hartigii	3.45	0.06	6.25	0	0.12	0
	Dorymyrmex	Dorymyrmex brunnem	17.24	0.05	12.5	23.08	0.06	0.04
	Pseudomyrmex		6.90	0.02	6.25	7.70	0.02	0.02
		Pseudomyrmex gracilis	3.45	0.01	0	7.70	0	0.02
		Pseudomyrmex sp.1	3.45	0.01	6.25	0	0.02	0
	Ectatomma		44.83	3.57	37.5	53.85	3.49	3.65
		Ectatomma brunneum	17.24	1.01	12.5	23.08	1.51	0.47
		Ectatomma opaciventre	31.03	2.53	31.25	30.77	1.98	3.12
	Gnamptogenys	Gnamptogenys sulcata	3.45	0.01	6.25	0	0.01	0
	Camponotus		75.86	4.26	62.5	92.31	2.24	6.43
		Camponotus balzani	58.62	1.19	43.75	76.92	0.53	1.89
		Camponotus crassus	58.62	3.04	43.75	76.92	1.71	4.44
	Crematogaster	Crematogaster sp.1	3.45	< 0.01	0	7.70	0	< 0.01
	Cephalotes	Cephalotes pusillus	3.45	0.03	6.25	0	0.05	0
	Acromyrmex	Acromyrmex sp.1	27.59	0.84	25	30.77	0.46	1.25
	Atta		17.24	6.70	12.5	23.08	2.03	11.70
		Atta sexdens	13.79	5.63	12.5	15.38	2.03	9.43
		Atta sp.1	3.45	1.01	0	7.69	0	2.08
	Mycocepurus	Mycocepurus goeldii	3.45	< 0.01	0	7.70	0	< 0.01
	Pheidole		96.55	6.82	93.75	100	5.29	8.47
		Pheidole fimbriata	6.90	0.14	6.25	7.69	< 0.01	0.28
		Pheidole oxyops	65.52	2.35	68.75	61.54	2.66	2.02
		Pheidole radoszkowskii	17.24	0.01	12.5	23.08	0.01	< 0.01
		Pheidole sp.1	41.38	0.13	31.25	69.23	0.14	0.12
		Pheidole sp.2	44.83	1.49	43.75	46.15	1.39	1.59
		Pheidole sp.3	6.90	0.01	12.5	0	0.02	0
		Pheidole sp.4	62.07	2.64	56.25	69.23	1.06	4.31
		Pheidole sp.5	3.45	0.01	0	7.69	0	0.02
Poaceae			31.03	1.02	37.5	23.08	1.29	0.74

Data for all sampled individuals and according to sex (13 M; 16F)

M. tridactyla fed primarily on termites (FO = 89.65%; RF = 75.85%) and ants (FO = 100%; RF = 23.08%; Fig. 3). Considering all identified prey items from all samples, most of the prey biomass was composed of termites of the genus Syntermes (RF = 75.55%). Most termite specimens were represented by soldiers, although a few workers were found in samples and identified. Although common in samples, ants represented a small portion of the consumed biomass. The genus of ants that composed most of the prey biomass were Pheidole (RF = 6.82%, FO = 96.55%), Atta (RF = 6.70%, FO = 17.24%), and Camponotus (RF = 4.26%, FO = 75.86%). Nevertheless, the RF of Atta could be biased by the high consumption rate of this genus observed in one individual (Suppl. Material 2). Furthermore, it is noteworthy that leaf-cutter ants of the genus Acromyrmex were also consumed (RF = 0.84%; FO = 27.59%; Table 1).Fig. 3

Relative Frequency (RF) of the three main classes of food items found in giant anteater's (Myrmecophaga tridactyla) diet in the Cerrado of Mato Grosso do Sul: termites (Termitidae; green), ants (Formicidae; blue) and grass seeds (Poaceae; black). Observed patterns for all sampled individuals and according to sex. Data based on fecal samples of 29 M. tridactyla individuals (13 M; 16F) collected from October 2018 to April 2020

Only a few prey items were common in the diet of M. tridactyla individuals (e.g., FO of ants of the genus Pheidole = 96.55%; FO of termites of the genus Syntermes = 86.20%; FO of ants of the genus Ectatomma = 44.83%). Most food items were rare, being found only in a few of the individual's diet (e.g., FO of termites of the genera Velocitermes, Nasutitermes and Diversitermes = 3.45%; and of ants of the genera Odontomachus, Crematogaster, Cephalotes, Eciton, Mycocepurus and Gnamptogenys = 3.45%; Table 1). The presence of several rare prey items in the samples may explain why although the species accumulation curve showed a trend to reach a stable asymptote, it indicated that new prey species would probably be detected in the diet of the species if we increased our sampling effort (Fig. 2). The first order Jackknife estimated an extrapolated prey richness of 60 species (SE = 5.75), in contrast to the 42 morphotypes we encountered.

Sex differences in diet

The main dietary difference between the sexes occurred through the variation in the proportion of ant and termite consumption (Fig. 3). On average, more than half of the mass of the prey items of male anteaters was composed of termites (RF = 67.54%, SD = 27.21; Termitidae), followed by ants (RF = 31.62%, SD = 26.96; Formicidae), and less than 1% of seeds. Meanwhile, female's diet was primarily composed by termites (RF = 83.61%), while the average RF of ants was 15.10% and that of seeds was 1.29%. It was possible to observe higher dietary variation in the relative frequency of consumption of ants and termites among females, when compared to males (Fig. 4). Nevertheless, there was not a statistically significant difference in the dietary habits between males and females of M. tridactyla (F[sub.1,28] = 0.58; R[sup.2] = 0.02; p = 0.68; Fig. 4). The termite genus Syntermes represented most of the biomass found in samples from both males and females, RF = 67.33%, and 83.24%, respectively (Suppl. Material 2). Syntermes was present in 81.25% of female samples and in 92.31% of male samples. Ants of the genus Pheidole were found in 93.75% of the female samples and in 100% of the male samples (Table 1).Fig. 4

Level of similarity in diet composition of male and female giant anteaters Myrmecophaga tridactyla. The distance between the dietary pattern of each sampled individual is represented by dimensions 1 and 2 of the multidimensional non-metric scaling analysis (NMDS with Bray Curtis similarity index. Food items found in fecal samples collected from 29 individuals in the Cerrado of Mato Grosso do Sul state from October 2018 to April 2020

Discussion

M. tridactyla feeding habits

In this study we confirmed M. tridactyla's highly specialized myrmecophagous diet consuming almost exclusively termites and ants (Redford 1985; Shaw et al. 1985; Medri et al. 2003; Gallo et al. 2017). We found that, at our study region, M. tridactyla fed more on termites, although ants were present in all samples at lower relative frequencies. This higher proportion of termites, in relation to ants, in the species' diet corroborates previous studies performed in the Cerrado (e.g., Redford 1985). However, it contrasts with studies conducted in the Cerrado and other regions of Brazil (e.g., Shaw et al. 1985; Medri et al. 2003; Braga et al. 2014) and Argentina (Gallo et al. 2017; Jiménez et al. 2018), which found a higher consumption of ants in relation to termites. These differences may be due to variations among sampling methods and/or study site landscapes. For example, some of these studies (Medri et al. 2003) were based on samples collected on only one season of the year. However, insect abundance is highly seasonal and can influence resource availability and dietary patterns in M. tridactyla (Redford 1986; Medri et al. 2003). Deloss et al. (2023) also found ants in all samples (FO = 100%) of lesser anteaters' (T. tetradactyla) stomachs, but termites were found in less than 70% of the samples.

It should be noted that Jiménez et al. (2018) suggest that 200 samples are necessary to fully understand the diet of M. tridactyla. In our study, the species accumulation curve showed that, despite this being the study with the largest number of M. tridactyla individuals sampled in the same area (N = 29), we could not detect all items of the species diet (Fig. 2). The species accumulation curve indicates an asymptotic trend but did not reach a plateau. In other words, more food items could be found in the species' diet if new samples were collected (Jiménez et al. 2018). This could be because most items of the species diet were rare, being consumed at low quantities and/or by few individuals (Suppl. Material 2), making their detection in the species diet harder. Nevertheless, it was clear that the species diet was dominated by few dietary items, although a rich composition of invertebrates was identified in their diet.

More than half of the dietary samples' mass was composed of termites of the genus Syntermes (RF = 75.55%, FO = 86.20%), especially soldiers. Syntermes sp. are relatively large termites that feed on leaf and grass litter foraging mostly in open vegetation areas. Their nests are primarily subterranean with epigeal mound structures with varying degrees of compactness (Constantino 2002, 2012). This termite genus has a wide distribution throughout South American, occurring both in forests and savannas (Constantino 2002). Syntermes sp. is commonly found in dietary studies of M. tridactyla (e.g., Redford 1985) and are known for their great nutritional value being high in proteins, amino acids, and minerals such as iron and calcium (Paoletti et al. 2003). In addition to Syntermes sp. termites, ants were consumed at low rates by all sampled individuals of M. tridactyla and were represented by a diversity of species (N = 29). The most consumed ants are those that nest in the ground, in trunks, or at tree bases, such as those belonging to the genera Atta, Pheidole and Camponotus (Mathews 1977; Melo et al. 2012; Baccaro et al. 2015). Atta nests can have several underground chambers, distributed at a depth of up to eight meters. The excavation and cleaning of their nests generates a conspicuous accumulation of dirt around the colony up to two meters high (Baccaro et al. 2015), which could facilitate their detection by predators such as M. tridactyla. In the neighboring floodable savanna of the Pantanal, Pheidole ants were the most detected ants, being associated mostly with secondary native vegetation (Martins et al. 2021). This indicates they are likely abundant at our savanna study area as well, although their mass represented only a small fraction of the prey items detected, indicating this is not a preferred prey for the studied species.

Our results corroborate the findings of Drumond (1992), who has shown that M. tridactyla presents a selective feeding behavior, ingesting prey at different proportions to their availability in the landscape. Hence, the frequency of consumption of prey items could be the result of prey preference, but also of the interaction between variations in prey abundance (Medri et al. 2003; Sandoval-Gómez et al. 2012) and prey adaptations and defense mechanisms against specialized predators, e.g., nest structure with a location or composition that facilitates access by anteaters. The T. tetradactyla, on the other hand, has a diet in which the consumption is more related to the insects' availability (Silva et al. 2019).

Prey use different defense techniques against their predators (Cunha et al. 2015). McNab (1984) suggested that predators such as M. tridactyla would avoid consuming ants and termites with aggressive behavior such as leaf-cutter ants or termites of the genus Syntermes, which bite and use chemical defenses against attackers (McNab 1984; Redford 1985). However, termites of the genus Syntermes, both soldiers and workers, were found in large proportions in our samples. Furthermore, other aggressive insects, such as ants of the genus Odontomachus (RF = 0.66%; FO = 3.45%), leaf-cutter ants of the genus Atta (RF = 6.70%; FO = 17.24%) and Acromyrmex (RF = 0.84%; FO = 27.59%) were also found in the diet of anteaters in our study. These insects, despite being aggressive, were found in our study and in the studies by Braga et al. (2014) and Sandoval-Gómez et al. (2012). This observation contradicts McNab's (1984) hypothesis, demonstrating that the defense mechanisms of these insects do not seem to inhibit predation by this large myrmecophagous mammal. The coevolution of predators and their prey can lead to an evolutionary "arms-race", where adaptations by a predator are countered by adaptation by their prey (Dawkins and Krebs 1979). In the studied system, it seems that the highly specialized morphological adaptations to myrmecophagy (McAdam and Way 1967; McNab 1984; Naples 1999) and the behavioral adaptations of M. tridactyla, which only feeds on insect colonies for short periods of time before moving to the next colony (Bertassoni and Desbiez 2021), allows this predator to feed even on the most aggressive termites and ants, but not for long enough to eat a substantial number of individuals in the inner parts of the colony (i.e., workers).

Most prey items identified in this study were found at small proportions in the species diet. This may be related to the colonial lifestyle of many insects and the investment of anteaters to open their nests and colonies. Many termite and ant colonies in underground or epigeal (above ground) nests can be occupied by one or numerous species of colonial insects. M. tridactyla consume their prey using specialized morphological adaptations, such as their large muscular front claws and large protractile tongue (McAdam and Way 1967; McNab 1984; Naples 1999). Thus, when tearing open a nest, M. tridactyla will feed on any insect species living within the colony collected by their sticky mucous tongue, which can generate the consumption of non-targeted prey at lower proportions (Drumond 1992).

Sex differences

Free-ranging males and females from our study area did not show significantly different eating habits. This pattern is similar to that found by Jiménez et al. (2018), who observed similar diets for individuals of both sexes reintroduced in the Iberá National Park in Argentina, in a protected area with a landscape mosaic composed of open fields, savannas and floodplains. However, despite being studied in the wild, not all reintroduced animals were born in the wild and their eating habits may have been influenced by management and pre-release learning. The lack of significant differences in the diet between the sexes could be explained by the absence of sexual dimorphism and overlapping territories between sex and age groups (Shaw et al. 1987; Bertassoni and Ribeiro 2019). Also, resources available in our study area could not have been diverse enough to enable intraspecific foraging differences (Kernaléguen et al. 2015). Nevertheless, females at our study site presented a broader variation in the relative frequency with which they consumed their main dietary items. Although this difference was not statistically significant, this could be related to varying energetic needs of females during different reproductive phases (e.g., lactation and cub hearing) in comparison to the stable energetic needs of promiscuous males that are not involved in parental care and continuously seek for receptive females with no reproductive seasonality (Bertassoni and Desbiez 2021).

Conservation implications

The Cerrado savanna is a biodiversity hotspot and is located at the core of M. tridactyla's distribution (Miranda et al. 2014; Strassburg et al. 2017). This biome has lost 46% of its native vegetation and still suffers with fast rates of land conversion, being converted mostly into cash crop plantations and agropastoral lands (Strassburg et al. 2017; Rodrigues et al. 2022). Environmental integrity can influence prey presence, abundance, and richness. For example, areas covered by native vegetation tend to have greater ant richness when compared to degraded areas, such as those converted into pasture (de Queiroz et al. 2020). The conversion of Cerrado savannas into pasture has also been shown to alter the composition and reduce the richness of termite communities (Carrijo et al. 2009). Some termite genera that composed M. tridactyla's diet in our study are mostly found in native Cerrado areas and habitat degradation could affect their availability as prey (Carrijo et al. 2009). Nevertheless, termites of the genus Syntermes, the termite most frequently consumed in our study, can be found both in native areas and modified pastures (Carrijo et al. 2009).

The tolerance of prey species to habitat degradation could be viewed as advantageous for the persistence of M. tridactyla's individuals and populations however, the consumption of prey that feeds on modified landscapes, such as pasture and croplands, can also have negative consequences for the species. In Minas Gerais, two giant anteaters have died due to intoxication by organophosphates, an agrochemical insecticide commonly applied in pastures and croplands in Brazil (Silva et al. 2022). One of the intoxication-induced deaths happened after a juvenile individual that was being rehabilitated for release was fed with termites taken from a peri urban pasture area, showing how insect prey contamination can affect the species survival. The assessment of the impact of agrochemicals on the health and survival of M. tridactyla has been appointed as a priority action for the conservation of giant anteaters by the Brazilian National Action Plan coordinated by ICMBio (ICMBio 2019). This highlights the relevance of this topic for the species' conservation and the need for further studies to understand the direct and indirect impact of the use agrochemicals on the species' health and survival. Finally, in the Mato Grosso do Sul (Brazil), where this research was conducted, only 16% of native Cerrado remains, but is pulverized in small ~ 9 ha fragments surrounded by agricultural matrix (Reynolds et al. 2016). This landscape configuration puts wildlife in close contact with human activities, increasing challenges for species conservation and human-wildlife coexistence.

M. tridactyla is a specialized insectivorous mammal that feeds exclusively on ants and termites. However, the species presents a somewhat opportunistic behavior, being able to predate on different prey species according to their local and seasonal availability (e.g., Medri et al. 2003). This might be one of the reasons why individuals can persist in modified and degraded landscapes (Zimbres et al. 2012). Furthermore, behavioral plasticity can allow insectivorous mammals to maintain the same isotopic diet in preserved and human modified landscapes (Magioli et al. 2019). Nevertheless, all species have a tolerance threshold to disturbance, and species behavioral plasticity can only go so far in allowing their persistence in the increasingly impacted Cerrado biome.

Conclusions

This study investigated the diet of M. tridactyla inhabiting the Cerrado region of Brazil. Although challenging to obtain, information on diet is useful for future conservation measures for this species vulnerable to extinction. It is evident that, despite being a myrmecophagous specialist, anteaters can consume a great diversity of prey species, but only a few taxa were common in the diet. Although common in samples, ants represented a small portion of the consumed biomass, and the giant anteater fed primarily on termites. Their prey is associated with different habitats that are characteristic to the natural heterogeneity of Cerrado. Therefore, to guarantee the availability of food resources and the conservation of the species, it is necessary to maintain areas that preserve the natural heterogeneity of the Cerrado landscapes while implementing more biodiversity-friendly management practices in areas under human use.

Author contributions

Nina Attias and Arnaud Léonard Jean Desbiez were responsible for study conception and design. Data collection and material preparation were performed by Tainara Galvao Santana, Natália Teixeira Nascimento, Mariáh Tibcherani and Mauricio Martins Rocha. Data analysis was performed by Nina Attias and Tainara Galvao Santana. Funding acquisition was performed by Arnaud Léonard Jean Desbiez. Tainara Galvao Santana and Nina Attias led the writing and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.

Funding

Financial support for this study has been received in the form of multiple small grants from American and European Zoos and NGOs listed at icasconservation.org.br. Financial support has also been given in the form of a grant stipend to TSGS by the Coordination for the Improvement of Higher Education-CAPES.

Data availability

The datasets generated and/or analyzed during the current study are available from the corresponding author upon reasonable request.

Declarations

Conflict of interest

The authors do not have financial or proprietary interests in the material presented in this manuscript.

Ethical approval

This study was performed in line with the guidelines of the American Society of Mammalogists (ASM) concerning the use of wildlife in research (Sikes et al. <xref ref-type="bibr" rid="CR71">2016</xref>) and was conducted under license #53798-10 granted by Chico Mendes Institute for Biodiversity Conservation (ICMBio).

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Title Annotation:	Original Article
Author:	Santana, Tainara Galvao; Attias, Nina; Nascimento, Natalia Teixeira; Tibcherani, Mariáh; Rocha, Maur
Publication:	Mammalian Biology
Date:	Jul 28, 2024
Words:	8971
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