The mara (Dolichotis patagonum; Caviidae family) is the second largest rodent in the world with an average body length of 70 cm and ≃ 8kg (Campos et al., 2001). The mara is endemic to Argentina (Campos et al., 2001; Torres, 2018; Alonso Roldán et al., 2019), and is widespread across the country, inhabiting the Dry Chaco, Espinal, Patagonian Steppe and Monte Desert ecoregions (Baldi, 2007; Sombra and Mangione, 2005). The maras exhibit a unique reproductive system; they combine monogamy, a reproductive strategy present only in 5% of studied mammals, with communal breeding, a strategy exhibited in 30% of mammals (Lukas and Clutton-Brock, 2012; Johnson and Young, 2015; Drickamer, 2019; Bales et al., 2021). During the breeding season (from August to January in the Argentine Patagonian), an average of two pups from a single litter per year have been observed in the wild (Taber, 1987; Taber and Macdonald, 1992b; Adrian and Sachser, 2011; Maher and Burger, 2016; Gatica et al., 2019) and in semi-controlled conditions (e.g. zoological institutions; Baechli et al., 2021).

Monogamy may have evolved in adult maras due to females exhibiting a short period of estrus (shorter than 1 hour for every 3 to 4 months). Since the pair bond involves sharing space and time, it has been suggested that the area around the female acts as a mobile territory (the average distance between maras is 2–4 meters). Typically, the female initiates activities and the male follows her to keep proximity (Taber, 1987). Behavioral studies have revealed that monogamy persists all year long and is an essential part of this species’ lifestyle, both in the wild (Taber, 1987; Campos et al., 2001) and in captivity (Genest and Dubost, 1974). This could also reveal the species’ needs and/or preferences in this context. Monogamy is also characterized by a high degree of behavioral synchronization or coordination during typical activities, which is frequently observed in the wild during feeding and locomotion. This synchronization enables pair members to stay close to each other, thereby preventing extra-pair copulation (Genest and Dubost, 1974; Taber and Macdonald, 1992a). This behavioral synchronization has been suggested as a strategy to strengthen the bond between pairs in several species (Duranton and Gaunet, 2016).

Communal breeding in maras could be linked to the distribution of food resources, depending on the productivity of an area or the transition from dry to wet seasons and vice versa. Therefore, it is not surprising to observe flexibility in the expression of this social strategy among mara pairs; as has been observed in long-term studies of other rodent species in the wild (Hayes et al., 2017). In the Argentinian Patagonia, wild maras were found living in 1 burrow shared by 1 or 2 pairs, or in 1 to 5 burrows shared by 8 to 20 pairs, with the latter being the most frequent case (Taber and Macdonald, 1992a; 1992b; Campos et al., 2001). Conversely, solitary mara pairs have also been observed in the Monte-Chaco ecotone of Argentina (Gatica et al., 2019). Communal breeding has been linked to feeding, survival and reproductive benefits in the wild (Taber and Macdonald, 1992b), which could mean that this strategy has a high biological value for males and females of the mara pair. Examples of the benefits of communal breeding have been observed in members of the Caviidae family (Ebensperger and Hayes, 2016a); particularly for wild maras, Taber and Macdonald (1992b) revealed the following benefits: a) increased access to food: with some pups being fed from non-parent females; b) energy and hydration savings: with mara adults and pups of the community achieving better thermoregulation through huddling; c) decreased predation risk: by increasing the number of maras in the breeding site, the group devotes more time to vigilance, presumably enhancing predator detection. Taber (1987) observed in Patagonia that proportionally fewer adults should be vigilant while a greater proportion should feed, rest and nurse pups as the number of adults at the den increases.

Currently, the species faces serious conservation problems: habitat fragmentation and/or loss, hunting (Alonso Roldán et al., 2019; Beninato et al., 2021) and interspecific competition with exotic European hares and domestic livestock (e.g. sheep) due to trophic overlap (Barrios Garcia Moar et al., 2023). These factors have led to a reduction in the species’ distribution area. The mara is categorized as near threatened internationally by the IUCN (2025), as vulnerable in Argentina (Alonso Roldán et al., 2019), and as threatened in the Dry Chaco (Córdoba province), where it is experiencing significant population decline (Cabrera, 1953; Rosacher, 2004; Periago et al., 2015; Alonso Roldán et al., 2019; Beninato et al., 2021). Since this species is quickly disappearing across its distribution area, its conservation may require human intervention. The literature shows that the most common approaches to dealing with the conservation status of maras focus on in situ actions, such as habitat conservation and protected zones (Campos et al., 2001; Alonso Roldán et al., 2019; Chillo et al., 2010; Beninato et al., 2021). However, ex situ studies are proportionally scarce and could provide valuable information about breeding programs and increased societal commitment (Abba et al., 2018). For example, in zoological institutions or primary care rescue centers, maras can recover from several conservation problems and could be reintroduced and/or subjected to a breeding conservation program. Success has occurred by spurring on controlled, natural breeding or, in some cases, in combination with assisted reproductive technologies (ART); although, ART is usually an expensive challenge for most zoos (Wildt et al., 2010). Among different topics, behavior is an important subject (and perhaps less expensive and complicated than ART) within many international breeding programs managed by Species Survival Plans (e.g. Martin-Wintle et al., 2018; Martin-Wintle and Shepherdson, 2012). Thus, to overcome different conservation threats, maras could benefit from conservation actions both in situ (e.g., protected zones) and ex situ (e.g., breeding programs) (Holt and Pickard, 1999).

In order to perform ex situ conservation for a species, it is essential to consider certain aspects such as habits, diet, social needs and activity budgets to satisfy their behavioral needs and individual welfare (Kelly et al., 2025), and also to guarantee positive results for animals under human care. For example, individuals of the species Airulopoda melanoleuca (panda) were allowed to choose their mates, resulting in higher copulation and birth rates than couples formed without this choice (Martin-Wintle et al., 2015). Regarding maras, Genest and Dubost (1974) demonstrated that both males and females could adjust their behavior to an artificial environment while maintaining their natural behaviors and reproductive success (Campos et al., 2001; Kessler et al., 2009; Alonso Roldán et al., 2019; Gatica et al., 2019). According to Kelly et al.’s (2025) review, the behavioral flexibility exhibited by maras in ex situ conditions indicates a high level of welfare. Baechli et al. (2021) observed strongly bonded mara pairs in captivity that exhibited an activity budget similar to those in the wild. However, there were some differences in the time spent on certain behaviors, such as an increase in resting and a decrease in feeding. Similar changes have been reported in other mammals under similar conditions (Höhn et al., 2000; Melfiv and Feinstner, 2002; Kerridge, 2005). Particularly in maras, Baechli et al. (2021) detected a behavioral synchronization value of 48% in zoo-housed monogamous pairs, while Taber and Macdonald (1992b) detected a value of 57% in the wild.

Nevertheless, some management challenges in ex situ conditions can exceed the maras’ capabilities to cope with them; as an example, Busso et al. (2022) demonstrated that the level of monogamous activity, behavioral synchronization, and reproductive success decreased in zoo-housed mara pairs when the pair bond was disrupted. Conversely, the impact of social bond disturbances within mara groups due to typical zoo management has yet to be explored. To the best of our knowledge, there is no specific data on the impact of social factors on behavior and reproduction in maras. Thus, the question arises as to whether disturbances in communal breeding could be considered a social stressor. This idea is supported by a framework in mammals that explains how environmental influences impact reproduction, particularly in rodents, although there is limited species-specific evidence (Bronson, 1985; Beery and Kaufer, 2015).

Among models that allow interpretation of stress responses, such as at a behavioral level, Romero et al. (2009) proposed a reactive homeostasis model, which integrates homeostasis, allostasis and stress. The Reactive Scope model establishes ranges of values for various physiological mediators that reflect an individual’s “normality.” For instance, in the context of behavioral physiological systems, foraging, feeding, locomotion and aggression are mediators of stress-related behaviors. Thus, animal response to a specific stressor (real and/or perceived) would exhibit changes in these measurements. In the present study, the experimental treatment can be considered as an environmental change at the social level that could cause a behavioral stress response.

We hypothesized that shifting from communal to solitary breeding disrupts the behavior and seasonal reproduction of zoo-housed mara pairs that express strong bonds. We predicted that solitary breeding maras would increase their time spent sitting in alert, while decreasing the time they spend resting and feeding, as well as decreasing their level of synchronization. Additionally, we predicted that the number of offspring would diminish over the reproductive season (spring-summer). The objective was to assess the impact of zoo management impact on some of the maras´ preferences, considering their life history strategies. Experimental manipulation in controlled or semi-controlled environments contributes to our understanding of cause and effect regarding certain factors, such as the influence of group size over behaviors related to social organization and reproduction in caviomorph rodents (Maher and Burger, 2011). Furthermore, the current evidence has implications for animal welfare and management because social aspects fall within the domain of one of the most widely accepted models of animal welfare (Kappel et al., 2017; Mellor et al., 2020; Kelly et al., 2025).

The members of a pair occasionally showed the same behavioral activity; however, the observed values were not statistically different from the randomly expected values. There were no two-way differences between the control and treatment groups throughout the experimental period (F_4.36 = 0.94; p=0.4530), nor was there an effect of treatment on this variable. However, significant differences were detected for the time factor between months, with October and December higher than November, January and February (F_4.36 = 4.93; p=0.0028; Figure 2).

Tables 2, 3 show examples of the social matrices obtained in Month 1 for control and treatment, respectively. Table 2 shows that Feeding and Resting were the most frequent synchronized behaviors in the control group during October, while Resting and Sitting in Alert were the most frequent for the treatment group in Table 3. The remaining social matrices are shown in Supplementary Appendix.

The activity/inactivity ratio was similar between maras from the control and treatment groups throughout the months in which this study took place: the values were 0.57 ± 0.03 and 0.55 ± 0.03, respectively (F_4.36 = 1.23; p=0.3155). The behavioral pattern was evaluated, and the two-way analysis revealed differences between the control and treatment group. Subsequent analysis (p < 0.05) revealed that mara pairs in the treatment group exhibited more sitting in alert records than those in the control group (F = 25.02; p = 0.0007). Conversely, the treatment group displayed fewer feeding records than the control group (F1.9 = 33.77; p = 0.0003). Figure 3 shows the behavioral proportion by sex, revealing mean values for males and females in the same experimental groups.

In particular, the analysis of the sitting in alert behavior was deepened at the individual level according to sex (Figure 4: males; Figure 5: females). This revealed more individuals in the sitting in alert state in the treatment group than in the control group.

Finally, all mara pairs were capable of digging their burrow in both the control and treatment pens. The control group pairs had 5 litters (2 pups per pair), while the treatment group had 4 litters (3 pairs with 2 pups each and 1 pair with 1 pup). Two pairs in the treatment group did not have any litters during the experimental period. A Chi-square test revealed no significant differences between experimental groups (X² = 2.01; gl=1; p=0.1535).

Our results showed the first evidence that the change from communal to solitary breeding can disrupt behavioral pattern in maras, suggesting an overload of some behavioral stress indicators in captivity; however, their reproductive capacity was not affected over one season. This is particularly relevant in the wild, considering that mara populations are declining with an estimated decreasing population trend of >30% in the last 10 years (Beninato et al., 2021) along their distribution area.

In the treatment context or solitary breeding space, each mara pair was housed alone during the spring-summer months without demands from factors that motivate behavioral synchronization to ensure monogamy, such as the competition between unfamiliar males for the mated female. Besides, there were neither intraspecific demands like non-related pups that required feeding and/or thermoregulation through huddling nor interspecific like predation. However, solitary breeding pairs from the beginning of the study (springtime) exhibited synchronization levels similar to communal breeding pairs. The average synchronization levels were around 50% in both experimental groups, comparable to previous studies in the same environmental conditions (Baechli et al., 2021) and in the wild (Taber and Macdonald, 1992b). As the breeding season progressed in the present study, independently from the experimental groups, mara pairs exhibited a lack of behavioral synchronization. This response appeared earlier in solitary breeding pairs (in November) than in communal breeding pairs (in January). Thus, considering that the female is the passive leader of the pair because she initiates action and the male follows closely, the male would always keep the female in close proximity under the treatment pen’s conditions. This may have been especially true in the treatment pen because it was smaller than the control pen. Particularly in the treatment pen context, this suggests that behavioral synchronization is unnecessary to maintain proximity and safeguard the pair bond. In a context of low intersexual competition, such as the one set up in the present study, Henry et al. (2021) proposed that animals in the wild or in the laboratory will not act without motivation. This observation seems obvious but is often overlooked when studies do not yield the desired/expected results, such as the treatment not having much of an effect in this particular case. Whenever motivation is considered, it implies a state influenced by intrinsic and extrinsic factors. Henry et al. (2021) suggest that motivations in a mating context are unlikely to remain consistent over time and may only manifest during the breeding season. In the present study, the combination of the time scale (analysis factor) and environmental context (e.g., food, weather, social relationships, and the absence of predators) may explain why synchronization diminished throughout the breeding season, although the behavioral dynamics of this trait differed among the experimental groups.

Furthermore, demographic changes within each pair’s family could be another influential factor in behavioral synchronization, especially for the control group. The birth of one or more pups in the pen could be one such factor. Taber and Macdonald (1992b) demonstrated that male and female maras exhibit different behavioral patterns during the breeding season in the wild. These patterns reduce the level of behavioral synchronization due to typical activities that occur as the breeding season progresses, such as the birth of offspring and its effect on behavioral interactions (particularly the bond between mother and pup). The presence of offspring at the end of the study in the maras’ families (each pair with its pup) in both the control and treatment groups may also explain changes in behavioral synchronization dynamics. Additionally, synergistic effects from other environmental factors, such as climatic and physical aspects, cannot be ruled out as possible influences on this trait. Photoperiod is recognized as an influential factor in reproduction and behavior in rodents. Many rodent species inhibit breeding when daylength (number of hours of light per day) falls below a critical minimum during the late summer/early autumn. For example, short daylengths typically induce changes in brain synthesis and storage of peptides that regulate reproductive state (e.g., gonadotropin-releasing hormone, GnRH), declines in circulating concentrations of reproductive hormones, and decreases in gonadal steroid production and reproductive behaviors (e.g., partner preference, sex behaviors) (Prendergast et al., 2001). In the summer (the last days of February in this region) photoperiod indicates unfavorable conditions for breeding purposes for the oncoming months, such as a shorter light phase and the reduced temperatures of Autumn. Perhaps the behavioral synchronization of maras decreased due to changes in the natural photoperiod. Therefore, solitary breeding, as well as seasonal changes (climatic-physical factor), would cause variation in maras’ behavioral synchronization. This synchronization may be attributed to the behavioral stress response rather than the monogamous strategy. Our experimental design does not allow us to rule out other sources of variation, such as available space. Perhaps solitary pair maras housed in larger enclosures would exhibit a different stress response in terms of synchronization, since their territory would be larger, the female could move across wider areas, challenging males’ monitoring capacity. Further investigation is required to compare solitary pairs in spaces of different sizes.

Behavioral synchronization has been linked to data revealed by Taber (1987), who detected the proportionate hierarchy of simultaneously expressed or synchronized behaviors: feeding > sitting in alert > locomotion > resting (Taber and Macdonald, 1992b). In the present study, the control group exhibited a behavioral hierarchy apparently adapted to their local context: feeding > resting > sitting in alert. The communal breeding behavior of the control group could primarily be explained by intrinsic, species-related factors. For example, they are herbivores that feed frequently throughout the day, which allows them to spend most of their time feeding. This behavioral hierarchy could also be explained by extrinsic factors typical of low environmental complexity spaces, such as the absence of predators, which explains the low expression of sitting –in alert behavior, and the restriction of limited space, which explains why locomotion behavior was unnecessary. On the other hand, solitary breeding maras (treatment group) exhibited the following hierarchy of synchronized behaviors: resting > sitting in alert > feeding. Considering the size of the pen, perhaps the maras did not need to move too much to access their food. Without the locomotion behavior, their behavioral pattern changed, reinforcing energy conservation processes, which are always vital in homeothermic species. Unexpectedly, sitting in alert behavior remains as an important component of synchronized behaviors in the Cordoba Zoo. This may happen because the maras perceive visitors (unknown humans) as a possible threat, either because of their quantity or due to them exhibiting scents and high vocalizations different to the zookeepers´, particularly the maras in the treatment group that were not supported by conspecific neighbors and/or did not have the chance to escape, if needed. Thus, this situation reinforces that maras should have enough enclosure space to avoid visitors, in comparison to the present experimental pens where the visitors walked close by. Wild maras studied in areas associated to tourism in the Monte Desert Argentina region seemed to prefer places near touristic activities, probably as a safe zone from predators (Beninato et al., 2021). This may indicate that maras did not perceive humans as a threat in a natural protected area. Solitary breeding maras spent more time in the sitting in alert state while reducing the feeding behavior. Sitting in alert usually refers to the environment’s vigilance for the purposes of: a) detecting stressors (e.g. predators), b) observing group members and/or c) locating food resources (Quenette, 1990; Beauchamp, 2015). Solitary breeding maras might not have been motivated by these 3 purposes (a, b and c). Within the conceptual framework of fear as a homeostatic mechanism and as a source of alertness or vigilance, fear could explain the high proportion of time dedicated to the sitting in alert behavior. However, the factor or factors that induce a fear response remain unknown. Perhaps, since only 2 individuals were in the treatment pens and they could easily satisfy their energetic needs, they prioritized a behavior with high biological value, such as sitting in alert, even though this activity might overload their homeostatic state.

Among the studied species that behave synchronously, it is inferred that synchronization reduces predation risk and strengthens social cohesion (Duranton and Gaunet, 2016). In this regard, the mara resembles some ungulates that have been studied for their synchronized activities. In the wild, monogamous pairs of the species Oreotragus oreotragus have been observed with 51, 6% behavioral synchronization (standing > resting > locomotion > feeding). Regarding territorial defense, the detection of same-species intruders and/or predators and the consistent proximity of pair members would explain their high degree of synchronization (Dunbar and Dunbar, 1980). In contrast, in environmental conditions similar to the present study, a high level of monogamy was observed in Madoqua kirki specimens, though with a moderate degree of real behavioral synchronization. This is because a significant portion (67%) of simultaneous activities were coincidental, as observed in maras in January and February (summer). This lack of true synchronization exhibited by M. kirki individuals could be explained by the dispersed food in their living area and/or long-distance monitoring by the male (Kranz, 1991). However, these factors do not explain the behavior of maras, since their food was not dispersed and distances among pair members were short. Kranz (1991) suggested that the absence of synchronicity, compared to what is typically observed in this species, indicates that monogamy may be viewed as a continuous phenomenon rather than as mutually exclusive extremes (facultative or forced). Perhaps, the environmental context is decisive in expressing behavioral synchronization, even in maras. It is possible that the degree of monogamy in terms of synchronization is minimized (reaching null values) when individuals find themselves in an environment with low social challenges regarding sexual resource competition.

Behavioral pattern analysis confirmed observations made regarding the hierarchy of synchronized behaviors. This analysis revealed that solitary breeding caused a decrease in feeding and an increase in sitting in alert behaviors. Breed and Moore (2022) indicate that the time animals dedicate to vigilance is inversely proportional to group size; this behavior is more effective in social species than in solitary ones. Observations on maras seem to support this hypothesis. However, it is interesting to consider what threat, or perceived threat, could stimulate this behavior in males within the territory of the pen, and whether this level of vigilance reflects their predictive or basal activity budget within the normal range of an individual. In the control group, cohabiting males could be an incentive for maintaining vigilance because any male would be considered an intruder, even if they already have an established stable bond. However, sitting in alert behavior values were higher in solitary breeding than in communal breeding. From a reactive homeostasis viewpoint, perhaps this response is correlated with higher catecholamine concentrations, which have already been identified as key factors in decreasing feeding behavior (Breed and Moore, 2022). This correlation should be studied at a physiological level in maras. Nevertheless, several factors may affect vigilance responses in wild animals. Beauchamp (2017) studied the connection between vigilance and stress, providing a clear example: an increase in stress hormone concentrations in European fallow deer (Dama dama) after hearing gunshots during hunting season. Figures 4 and 5 reveal two things at an individual level: first, more individuals in the treatment pens were observed in an alert sitting position than in the control pen; second, the sitting in alert state may have reflected the circadian rhythm, initially observing that both experimental groups exhibited individuals in a sitting in alert state, but communal breeding maras exhibited lower values as the day progressed. More human presence is normally detected in the morning at the Córdoba Zoo; this may explain the treatment group’s response compared to the control group. This behavioral pattern has been observed previously, particularly in the early morning, in another group of maras in the same breeding space, probably due to routine activities in the institution (Baechli et al., 2021). We dismissed the idea that the observed increase in sitting –in alert behavior was due to the animals being moved to the experimental pens because all maras experienced novelty during the acclimatization period; thus, the increase should have been evident both in the treatment and control groups.

In conclusion, the transition from communal breeding to solitary breeding: a) it did not affect behavioral synchronization; b) it showed a clear difference in activity patterns, with resting and sitting alert being the main behaviors observed (compared to feeding and resting in the control group); c) it caused a change in the proportion of time that pair members dedicated to sitting in alert (higher) and feeding (lower), while resting, locomotion, exploration, and other behaviors remained unchanged; and d) it did not prevent pair members from digging their own burrows and producing offspring during the breeding season, resulting in productivity similar to that of communal breeding mara pairs. Thus, ex situ management of social factors at group level affects behavior of zoo-housed maras with strong monogamy bonds, but does not affect reproduction over one season.