Abstract
How social and ecological factors are associated with variation in dominance style across species of animals has been studied frequently, but the underlying processes are often not addressed. Theoretical research indicates that stronger spatial cohesion among individuals in a group causes a higher frequency of fighting and, thus, through the self-reinforcing effects of winning and losing fights, a stronger differentiation of the dominance hierarchy and dominance of females over more males. Our aim in the present paper is to study whether the same interrelationship among processes may underlie differences in dominance style among three species of lemur that differ in their degree of despotism: Lemur catta, Propithecus verreauxi and Eulemur rufifrons. We investigated their agonistic interactions and spatial cohesion based on 2752 h of observational data of 20 wild groups of these three species. We determined dominance style using the proportion of counter-aggression, with a lower proportion indicating a more despotic dominance style. We found that stronger spatial cohesion among individuals is associated with a higher rate of aggression, stronger despotism and dominance of females over more males. The results of our study emphasise the general importance of spatial cohesion in determining dominance style.
Significance statement
Theoretical studies have shown that the spatial configuration of individuals in a group influences the dominance style. In an agent-based model, DomWorld, individuals are guided by simple rules of grouping and fighting and emergent patterns of behaviour switch between resembling those of despotic or egalitarian primates depending on the degree of cohesion in groups. Yet this link has seldom been studied empirically. We, therefore, examine the relevance of spatial cohesion on patterns of behaviour of individuals in groups of three species of lemur. We confirm the predictions from the model and show that stronger spatial cohesion results in more frequent aggression, a more despotic dominance style and stronger female dominance over males. In light of this, we urge future research of animal dominance to include measures of cohesion.
Similar content being viewed by others
Avoid common mistakes on your manuscript.
Introduction
Group living in animals is associated with advantages such as enhanced detection of predators, defence of resources and transmission of information (Krause and Ruxton 2002). However, as the number of individuals in a group increases, so does competition over access to limited resources. Dominance relationships formed through repeated agonistic interactions among individuals represent a widespread adaptation to prevent costly conflicts because individuals are unlikely to attack if they think they will lose (Jackson 1991; Hemelrijk 1999a). The dominance style in a particular hierarchy can be classified on a continuum from despotic to egalitarian (Vehrencamp 1983), reflecting the degree of power asymmetry between individuals (Flack and de Waal 2004). In despotic societies, some individuals are much more socially powerful than others and can exclude others from resources, whereas in more egalitarian societies, group members have similar agonistic power and seldom exclude others from resources (Vehrencamp 1983). The drivers of this interspecific variation remain poorly known, however.
The identity of the winner of a fight is thought to result from prior attributes, self-organisation or both. The prior attribute hypothesis relates dominance to biological traits such as body size, where larger individuals are more likely to win than smaller ones (Chase and Seitz 2011). Yet, sometimes, smaller females are dominant over larger males in sexually dimorphic species, leading to variable patterns of intersexual dominance (Hemelrijk et al. 2008, 2020; Izar et al. 2021; Kappeler et al. 2022). The self-organisation hypothesis attributes this outcome to the winner-loser effect, which implies that following a conflict, winners are more likely to win their subsequent fight and vice versa for losers (Hsu et al. 2006; Chase and Seitz 2011). This effect has been demonstrated throughout the animal kingdom, including insects, crustaceans, fishes, amphibians, reptiles and primates (Hsu et al. 2006; Franz et al. 2015), and has also been shown to influence intersexual dominance (Hemelrijk et al. 2008, 2020; Izar et al. 2021).
Variation in dominance styles among groups and species has also been related to variation in the distribution and abundance of food and the resulting type of competition individuals experience for it (e.g. scramble vs contest). The underlying socioecological model was originally developed for non-human primates (Wrangham 1980), and subsequently extended to include risks of predation and infanticide (van Schaik 1989; Sterck et al. 1997). More recently, the extended model has also been tested in non-primates, such as coatis and ungulates (de la O et al. 2019; Szemán et al. 2021). Yet critiques of this model have suggested that a one-size-fits-all approach may not be suitable (Thierry 2008, 2021).
Indeed, in macaques, ecological differences cannot so far explain the interspecific variation in dominance style (Thierry 2021). Rather, selection may have only acted on one or two ‘pacemaker’ traits (e.g. intensity of aggression and degree of nepotism), which cause a shift in a suite of behavioural traits concerning agonism and affiliation that co-vary with one another (Thierry et al. 2004). For instance, more despotic (intolerant) species of macaque exhibit higher intensity of aggression, stronger nepotism, more uni-directionality of aggression and less reconciliation than more egalitarian species (Thierry 2000; but see Balasubramaniam et al. 2012, 2018). Moreover, since those macaque species that are more similar in their dominance style are also sometimes more strongly related, phylogenetic distances may influence interspecific variation in aspects of dominance style as well (e.g. Balasubramaniam et al. 2018).
An agent-based model, DomWorld (Hemelrijk et al. 2017), demonstrated a causal relationship among agonistic and affiliative traits. In this model, each individual is guided to group with others and fight nearby individuals. After losing a fight, the loser is more likely to lose again, and after winning, the victorious individual is more likely to win again, representing the winner-loser effect (Hsu et al. 2006). Even though all individuals of one sex start with the same fighting capacity, represented by their Dom-Value, over time a hierarchy differentiates due to these self-reinforcing effects (Chase et al. 1994). Emergent patterns of behaviour switch from resembling despotic species to egalitarian ones by changing a single trait: the intensity of aggression. When intensity of aggression is high rather than low, outcomes of fights have a strong impact on the hierarchy, causing it to differentiate strongly, which leads to aggression being more uni-directional, reconciliation and consolation occurring less often and grooming being mainly directed up the hierarchy (Puga-Gonzalez et al. 2009, 2014).
In the primate radiation of lemurs, group living evolved twice independently (Kappeler and Pozzi 2019) and species range from clearly despotic to much more egalitarian. It remains unknown what underlies differences in dominance styles and whether patterns of behaviour co-vary in species of lemur. Unlike macaques, lemurs supposedly do not differ in their intensity of aggression (Kappeler 1993). Moreover, phylogenetic closeness seemingly cannot explain differences in dominance style among species either, as more distantly related species are more similar in dominance style than more closely related species (e.g. Eulemur macaco and Lemur catta are more despotic than Eulemur fulvus (Kappeler 1993; Roeder et al. 2002)).
An alternative mechanism that may underlie differences in dominance style in lemurs is again suggested by DomWorld, which relates dominance style also to the degree of group cohesion (Hemelrijk et al. 2017). Specifically, the model shows that when individuals in a group are closer together, they have higher rates of aggression because they are more often close to potential interaction partners. This higher rate of aggression causes the hierarchy to differentiate more through the winner-loser effect, causing a more despotic hierarchy and the associated patterns of behaviour (Hemelrijk 1999b, 2003). However, empirical studies on the association between the frequency of aggression and dominance style are missing.
In DomWorld, a further side effect of stronger group cohesion is an increase of dominance of females over males. This occurs because individuals interact more often, which results in a more differentiated dominance hierarchy of males and females, and as a consequence, some females become dominant over some males. Yet, this effect has only been demonstrated when males are larger than females and, thus, are equipped with a higher initial dominance and intensity of aggression. In the present study, we examine how cohesion, and thus frequency of aggression, influences intersexual dominance in lemurs, where males and females do not differ in body size, and female dominance over males is common but differs in its degree among species (Eichmueller et al. 2013; Rina Evasoa et al. 2019; Kappeler et al. 2022).
In this study, we want to unravel whether, as predicted by DomWorld, the degree of spatial cohesion underlies variation in dominance style and the degree of intersexual dominance in three species of lemur. These are, ranging from most to least despotic, as follows: ring-tailed lemurs (Lemur catta), Verreaux’s sifakas (Propithecus verreauxi) and red-fronted lemurs (Eulemur rufifrons) (Kappeler 1999; Norscia and Palagi 2015). We studied several groups of each species to determine in particular whether individuals in groups with stronger cohesion fight more often (prediction 1), whether a more despotic dominance style is associated with a higher rate of aggression initiated (prediction 2) and whether stronger cohesion underlies a higher degree of female dominance over males in lemurs (prediction 3).
Methods
Study species, site and groups
Ring-tailed lemurs (RTLs), Verreaux’s sifakas (VS) and red-fronted lemurs (RFLs) live in multi-male multi-female groups and are endemic to Madagascar. Adult ring-tailed lemurs weigh around 2 kg and form groups of individuals ranging from 9 to 16 individuals. We studied them at Berenty Reserve, where they feed mostly on Tamarindus indica (Simmen et al. 2006). We studied Verreaux’s sifakas, who have a body size of 3.6 kg and an average group size of six individuals in Kirindy Forest (Kappeler and Fichtel 2012). They are highly folivorous and feed mostly on mature leaves and flowers (Koch et al. 2017). Red-fronted lemurs weigh 2.2 kg and occur in dry-deciduous forests in western Madagascar but also in rain forests in south-eastern Madagascar. Their group sizes vary between 4 and 18 individuals, with an average of nine individuals. The diet of red-fronted lemurs is diverse, including different plant items and insects, with leaves making 52% of their diet in the dry season in Kirindy Forest (de Winter et al. 2013).
Five groups of ring-tailed lemur (C1, C12, C2A, T2, YF) were studied in Berenty Reserve in southern Madagascar (Jolly 2012). Individuals were identified by natural markings on their face and fur. Nine groups of Verreaux’s sifakas (C, E, F, F1, G, G1, H, J, L) and six groups of red-fronted lemurs (A, A1, B, B1, F, J) were studied in Kirindy Forest in western Madagascar, (Kappeler and Fichtel 2012). Groups of Verreaux’s sifakas and red-fronted lemurs were tracked by radio collars that were worn by a single individual in each group. Individual group members were identified by collars of different colour combinations (Kappeler and Fichtel 2012).
Data collection and analyses
Data collected before 2018 were collected by conducting continuous focal observations of adult individuals. In 2018, we performed all-occurrence observations of agonism of adults in groups, as well as scan-sampling every 10 min to record the location of individuals (Table 1). Here, a focal individual was selected to follow and the location of all individuals relative to it was recorded to quantify group cohesion. An effort was made to ensure each individual in a group was observed for a similar amount of time by pre-selecting the observation of individuals via a rotation system. Three hours of focal observation of individuals from a group were recorded in the morning and in the afternoon. Focal observations per individual per day lasted 30 min, except for some groups of sifaka (C, E, F, F1, G, H, J, L) which lasted 1 h. During observations, all agonistic interactions were recorded, including the identity and behaviour of the interaction partner. Some data had already been collected as part of previous projects (e.g. Koch et al. 2017; Fichtel et al. 2018). It was not possible to record data blind because our study involved focal animals in the field.
Agonistic interactions were defined by the exchange of either aggression or submission or both. Aggressive behaviours included chase, grab, lunge, bite and displace while submissive behaviours included submissive vocalisations (‘spat call’ in ring-tailed lemurs and ‘chatter’ in Verreaux’s sifakas) or fleeing in all three species. Agonistic interactions were classified as ‘decided’ (AS) if only one of the opponents exhibited submissive behaviour to the other. Spontaneous submission (OS) was characterised by submissive behaviour that was not prompted by an aggressive act, with the loser being the individual that submitted. Following other studies in lemurs, we considered spontaneous submission as a decided agonistic interaction (Pereira and Kappeler 1997). Interactions were classified as undecided when there was no clear winner, meaning that submission from either opponent was absent. In these cases, aggression was either met with counter-aggression (AA) or a neutral behaviour (AO), such as doing nothing or turning but remaining on the same location. For a full ethogram and definitions, see Pereira and Kappeler (1997) and Kraus et al. (1999).
To be included in our analyses, individuals had to have been engaged in at least one agonistic interaction (decided or undecided). Therefore, two males from group B1 and one female as well as one male from group B of red-fronted lemurs were omitted. We also excluded one male from group T2 of ring-tailed lemurs because he was in the process of immigrating into the group and was not yet socially integrated.
Dominance hierarchy
We derived the dominance hierarchy among adults of each group from decided agonistic interactions (AS + OS). For this, we used the Average Dominance Index (ADI). The average dominance index is the average proportion of winning by an individual from all of its opponents, excluding opponents with whom it did not interact. The degree of female dominance over males was measured by the Female Dominance Index (FDI; Hemelrijk et al. 2008). This is the average proportion of males in the group over which females are dominant. If males and females are equal in their dominance (ADI), we use the common procedure of ties (the tie counts for each of the pair members as 0.5).
To assess the dominance style in a group, we used the proportion of fights with counter-aggression, which has been suggested to be an appropriate measure of dominance style in macaques (Balasubramaniam et al. 2012; Thierry 2021). A higher proportion of counter-aggression indicates species to be more egalitarian. We use this over the common measure of steepness (Gammell et al. 2003; de Vries et al. 2006) since steepness is known to be highly influenced by a high proportion of unknown relationships and small group sizes (Klass and Cords 2011), which were common in our data. We calculated the proportion of counter-aggression as the number of counter-attacks (conflicts in which the receiver of aggression immediately aggresses back to an aggressor) divided by the total number of interactions per group (all agonistic interactions). The proportion of counter-aggression per group was strongly correlated with the average proportion of counter-aggression per interacting dyad, and per individual per group, and thus, it was little influenced by a single individual or dyad (R = 0.99, p < 0.001, Fig. S6). To understand how the proportion of counter-aggression relates to differences in fighting capability among individuals in a group, we tested per species whether interactions involving counter-aggression occurred more often between individuals of closer dominance rank than decided interactions did. We did this by comparing per species the rank difference (ADI of actor – ADI of receiver) when agonistic interactions were decided or involved counter-aggression.
Agonistic interactions
The rate of aggression per individual was calculated as the sum of the number of decided and undecided agonistic interactions (not including spontaneous submissions) it initiated per hour. We combine rates of aggression calculated by focal and all-occurrence collection methods since these did not significantly differ within the same species (Table S9, S10). Intensity of aggression was recorded on a scale from 1 to 5 according to Kappeler (1993), with level 1 for displacements; level 2 for aggression without physical contact, such as using signals or threatening another individual; level 3 for physical contact, such as wrestling or hitting; level 4 for intense physical aggression such as biting; and level 5 for chasing. Agonistic interactions with aggression were scored based on the most intense aggression displayed by the initiator, meaning that for example if an interaction included a chase as well as a signal, it would be scored as 5. The intensity of aggression was averaged over all fights initiated per individual. Spontaneous submissions were not included in the rate of aggression or intensity of aggression because in this case neither partner performed an aggressive act.
Cohesion
Data regarding cohesion were measured for fewer groups than for agonism (5 groups vs 20 groups, respectively). This is because focal observations collected during previous projects did not collect data on group cohesion. Data on cohesion were collected specifically for the present study between March and July 2018. Data were collected using Animal Observer App for iPad (Caillaud 2018). Here, an individual was chosen and followed for 30 min. Every 10 min, a scan of the group was taken, and the location of all other individuals relative to the focal individual was recorded on a map. Scans were conducted in 2D. Per scan, the heading of the front of the group was taken as the direction of movement of the whole group (and considered ‘north’ in the map interface). As a proxy of cohesion, we calculated per individual per scan the number of individuals within 3 m.
Statistical analyses
Data processing and statistical tests were conducted in R (version 4.0.3) (R Core Team 2020) and RStudio (RStudio Team 2020). Graphs were created in RStudio with ggplot2 (Wickham 2016) and ggpubr (Kassambara 2020). General and linear models were fitted using stats package from R (R Core Team 2020), glmmTMB package (Brooks et al. 2017) and lme4 (Bates et al. 2015). Goodness of fit was measured through statistics based on simulated residuals from the package DHARMa (Hartig 2022) and dfbetas and variation inflation factor using the car package (Fox and Weisberg 2019). For some models, significant outliers were found and they were removed from the dataset and the model was conducted again. If the results were qualitatively the same (same direction and similar magnitude of the estimate and degree of significance), we report results from the full dataset (see supplementary material for details).
We confirmed whether species differed in their intensity of aggression or not using a linear mixed model (LMM) with average intensity per individual as the response variable and species as the predictor variable with group as a random effect.
We investigated whether individuals that had more neighbours within 3 m also had a higher rate of aggression (prediction 1). We conducted a negative binomial regression with a log link to examine whether the rate of aggression (number of aggressive acts initiated per individual) was predicted by the average number group members within 3 m. We include group size and species as control factors, group identity as a random factor and the number of observational hours as an offset.
To investigate whether a higher rate of aggression is related to a more despotic dominance style (prediction 2), we performed a binomial GLM with a logit link. We used the proportion of counter-aggression per group as the response variable (inputted as the number of interactions involving counter-aggression per group as ‘successes’ and the number of decided fights per group as ‘failures’ using the cbind function), and the average rate of aggression per group as predictor. We included species and group size as control factors.
Finally, to study whether in more cohesive groups, females were dominant over relatively more males (prediction 3); we compared whether species that had stronger female dominance over males also had a stronger group cohesion. Variation in female dominance was compared across species by fitting a binomial regression with group size as a control factor. Due to the complete separation in the logistic regression of the Female Dominance Index (all FDI of Verreaux’s sifaka = 1), we applied the brglm fitting method (Kosmidis and Firth 2021). Differences in the average degree of cohesion (number of individuals within 3 m) per individual were compared among species using an LMM with group as a random effect. We did not directly correlate group cohesion and FDI because of the low number of data-points for group cohesion (n = 5).
We tested per species whether the rate of aggression initiated differed between the sexes using negative binomial GLMM with log link, using group as random effect and the number of observation hours as an offset.
For comparisons among species, we report likelihood ratio tests (LRTs) between full and null models (just control factors and random effects). If significant, we conducted post hoc pairwise comparisons using the emmeans package (Lenth 2021) to compare the estimate marginal means. We corrected p-values for multiple comparisons using the Tukey method.
Results
In line with previous findings, intensity of aggression of fights was on average intermediate and did not differ significantly among species (mean ± SE RTL: 2.26 ± 0.20; VS: 2.40 ± 0.27; RFL: 2.48 ± 0.23; LRT: X2 = 0.86; df = 2; p = 0.65; Table S1, S2, Fig. S1). We also demonstrate that counter-aggression occurred more often between individuals of a similar dominance rank (ADI) than decided fights, especially in ring-tailed lemurs and red-fronted lemurs (RTL: W = 29,601.5, n1 = 3118, n2 = 12, p < 0.001; VS: W = 338, n1 = 368, n2 = 1, p = 0.15; RFL: W = 1318.5, n1 = 86, n2 = 23, p < 0.01, Table S8, Fig. S7).
In line with prediction 1 (stronger cohesion results in a higher rate of aggression), individuals in groups aggressed others at a higher rate when they had more neighbours (β = 1.17, se = 0.42, z = 2.80, p = 0.005, n = 34 individuals, Fig. 1A, S4, Table S3, S4). This result was robust even when cohesion was measured as the number of individuals within different distances around the focal individual (Fig. S5, Table S7). In support of prediction 2 (higher rate of aggression, more despotic dominance style), groups with a higher average rate of aggression had a lower proportion of counter-aggression (β = − 1.45, se = 0.51, z = − 2.84, p = 0.0045, n = 20 groups, Fig. 1B, Fig. S10).
Regarding prediction 3 (stronger cohesion is associated with stronger female dominance), we show that groups of species that exhibited a stronger group cohesion also had a higher female dominance index (Fig. 2A, B, Table 2, S15–18). Note also that in groups of species where the Female Dominance Index was higher, females initiated a higher rate of aggression than males (Fig. 2C, ring-tailed lemur β = − 1.71, SE = 0.23, z = − 7.57, p < 0.001; Verreaux’s sifaka β = − 1.46, SE = 0.29, z = − 5.02, p < 0.001; red-fronted lemur β = 0.54, SE = 0.31, z = 1.74, p = 0.08).
Discussion
In this study, we provide evidence indicating that the dominance style of three species of lemur depended on the degree of cohesion, but not on the intensity of aggression. Firstly, we confirmed that individuals that had more group members nearby initiated more fights (prediction 1). Secondly, we demonstrated that a higher rate of aggression correlated with a more despotic dominance style in lemurs (prediction 2). Thirdly, we showed that stronger cohesion may underlie a stronger degree of female dominance over males (prediction 3). We discuss these points in detail below.
Cohesion, rate of aggression and dominance style
In groups of lemurs where individuals were surrounded by more neighbours, they initiated more aggression (prediction 1), particularly in ring-tailed lemurs and red-fronted lemurs. This higher rate of aggression was associated with a lower frequency of counter-aggression, and, thus, a more despotic dominance style (prediction 2). Hence, we offer support with our data in three species of lemurs for predictions made by the DomWorld model, suggesting that a higher rate of aggression from individuals resulting from their closer proximity causes stronger hierarchical differentiation through the winner-loser effect (Hemelrijk 2003; Hsu et al. 2006).
Despite our small dataset for group cohesion, our results are in line to those reported in other studies of wild lemurs (e.g. Hood and Jolly 1995; Cavigelli et al. 2003; Norscia and Palagi 2015). However, the underlying factors driving variation in group cohesion (and thus rate of aggression and dominance style) in lemurs are unclear. Here, we address three possible explanations according to the socio-ecological model (Wrangham 1980; van Schaik 1989; Sterck et al. 1997): (1) the distribution of food, (2) predation pressure and (3) group size. We limit ourselves to these three possible explanations that may underlie variation in cohesion, yet there may be other contributing factors; for instance, intergroup competition (Samuni et al. 2020), habitat fragmentation and seasonality (Irwin 2007) are also known to influence intragroup cohesion.
Firstly, we hypothesise that stronger cohesion may be related to a patchier distribution of food. In support of this, ring-tailed lemurs, which exhibited the strongest group cohesion, have previously been reported to experience contest competition and to feed often within 3 m of their nearest group member (Sauther 1993; Gemmill and Gould 2008). In contrast, the less cohesive red-fronted lemurs are capable of switching their diet from fruit to other items during periods of scarcity (Erhart et al. 2018). Thus, they may group more sparsely at a food source and thus have fewer conflicts. In a controlled feeding experiment, red-fronted lemurs also exhibited more social tolerance towards conspecifics than ring-tailed lemurs (Fichtel et al. 2018). Indeed, nearest neighbour distance in primates has been shown to be larger when individuals are feeding on leaves than on fruits (Bryer et al. 2013; Le Flohic et al. 2015). Also, in other species of lemurs, the rate of aggression was lower in the folivorous Hapalemur griseus, than in the frugivorous Eulemur macaco (Digby and Stevens 2007), which may be a consequence of cohesion.
Because Verreaux’s sifakas are highly folivorous (Koch et al. 2017), we expected individuals to be more spread out and to exhibit fewer conflicts. Instead, individuals had a relatively high number of neighbours nearby, but fought infrequently. Originally, it has been suggested that folivorous species do not fight over food because leaves are abundant (Isbell 1991). However, more recent studies revealed that this concept may be outdated because intense feeding competition has also been observed in folivorous species (Koenig 2002; Snaith and Chapman 2007). Unexpectedly, Verreaux’s sifaka’s dominance style appeared to be highly despotic (almost no counter-aggression) despite their rate of aggression being low. In general, the dominance style of Verreaux’s sifaka was difficult to assess because of their low interaction rates. Note that dominance style in Verreaux’s sifaka has been reported to be variable and difficult to determine elsewhere too, even when aggression matrices were more complete (Palagi et al. 2008; Norscia and Palagi 2015).
Secondly, cohesion may relate to risk of predation. Groups that experience stronger predation have stronger cohesion, because cohesion increases protection against predators (Sogard and Olla 1997; Schreier and Swedell 2012). However, this does not explain the differences in cohesion among our three study species. Ring-tailed lemurs were highly cohesive, but were studied in Berenty where they suffer less predation pressure than Verreaux’s sifaka and red-fronted lemurs in Kirindy Forest (Fichtel and Kappeler 2011). Moreover in Kirindy Forest, red-fronted lemurs are more terrestrial than Verreaux’s sifaka and therefore experience stronger predation risk from the largest Malagasy carnivore (fosa, Cryptoprocta ferox; Schnoell and Fichtel 2012), but their groups were not more cohesive than those of Verreaux’s sifaka. Hence, the variation in group cohesion across the three species of lemurs is unlikely to be due to variation in predation risk.
Thirdly, group size may also influence cohesion in groups. In our study, ring-tailed lemurs had a larger group size and were more cohesive than red-fronted lemurs, mirroring a similar pattern between group size and cohesion in some fish (Partridge 1980; Hemelrijk et al. 2010). However, among primates, a larger group size is usually associated with weaker cohesion (e.g. Zárate and Stevenson 2014). Stronger cohesion within groups may also arise from stronger competition between groups, for which larger group size is advantageous (LaBarge et al. 2020; Samuni et al. 2020). However, in Verreaux’s sifakas at our study site, larger groups are not more likely to win in intergroup conflicts (Koch et al. 2016), suggesting that larger group sizes might be counteracted by the disadvantage of increased competition over food (Koch et al. 2016) or other costs (Rudolph et al. 2020).
Female dominance and cohesion
In our data, female dominance over males was stronger in groups from species that were more cohesive (prediction 3), and in these species, females initiated more aggression than males. In general, hypotheses regarding female dominance over males in lemurs focus on the similar body size of the sexes as well as the greater effort that females invest in conflicts because of their higher energetic demand during reproduction (cost-asymmetry hypothesis, Dunham 2008). Until recently, variation among lemur species in the degree of female dominance over males has largely been ignored but recent results show that it is more variable than previously thought (Kappeler et al. 2022). We propose here that the degree of female dominance over males may relate to differences in cohesion due to differences in the distribution of food and thus intensity of feeding competition. When food is more clumped, individuals are closer together and more likely to engage in competition for food, with females competing more strongly over food than males due to their greater energetic demands. When food is more spread out, females, however, may not need to engage that strongly in competition over food, resulting in weaker female dominance over males.
Counter-aggression and measures of dominance style
In the present study, we determined dominance style using the proportion of counter-aggression, which reflects the degree of symmetry in dyadic contests (Balasubramaniam et al. 2012; Thierry 2021). When interaction rates are low, this measure is preferable over the measure of steepness by de Vries and co-authors (2006) because steepness is biased by the proportion of unknown relationships (Klass and Cords 2011). In macaques, counter-aggression occurs relatively more often in egalitarian than despotic species supposedly because aggression in egalitarian species is milder and thus the risk of injury is lower (Thierry 2000). However, among the species of lemur in the present study, the proportion of counter-aggression differed among species even though their intensity of aggression was similar. Instead, we found that counter-aggression occurred more between individuals of a similar rank, which is an alternative explanation of why more frequent counter-aggression implies a more egalitarian dominance style. What is still unknown and requires further study is which circumstances (outside of rank differences) lead to counter-aggression and whether certain types of interactions are more likely to illicit counter-aggression as a response.
Fights that do not have a clear outcome may not induce a hormone response associated with a winner-loser effect (e.g. mirror fights in fish Teles et al. 2013; Oliveira et al. 2016)), and therefore may not affect hierarchical differentiation. Thus, a high proportion of counter-aggression may be both a cause and a consequence of an egalitarian hierarchy, because an undifferentiated hierarchy will result in frequent counter-aggression and frequent counter-aggression may prevent the hierarchy from differentiating. This is important for understanding the mechanisms underlying hierarchy formation and suggests that undecided fights should not be included in the analysis when deriving a dominance hierarchy (e.g. Elo-rating (Neumann et al. 2011)).
Future work
The relationship between spatial structure and social behaviour is often ignored in empirical studies, despite models of animal behaviour highlighting its importance (e.g. Hemelrijk et al. 2017; Tyutyunov and Titova 2017). We demonstrate here in three species of lemurs that spatial proximity among group members was associated with differences in rates of aggression, dominance style and degree of female dominance over males. Studies in captivity support our finding for the association between stronger cohesion and higher rates of aggression in other species of lemur (Digby and Stevens 2007; Cherevko 2020), as well as in other taxa such as gazelles (Cassinello and Pieters 2000), horses (Flauger and Krueger 2013), apes (Sannen et al. 2004, but see de Waal 1989), chickens (Estevez et al. 2002), cows (DeVries et al. 2004), pigs (Remience et al. 2008) and kangaroos (Höhn et al. 2000)). Yet, in our study in the wild, how and why strong cohesion in ring-tailed lemurs is maintained despite a high rate of aggression is unclear since individuals could flee or spread out to avoid costly fights. This paradox requires further study.
The generality of the relationship between cohesion, rate of aggression and dominance should be studied in more groups of lemurs and in other animals. Currently, our study offers only correlational support for this relationship based on a small dataset of three species observed at different times of year. To test this prediction more extensively, data should be collected on more groups and species of group-living animals, preferably over multiple seasons. Moreover, alternative explanations for difference in cohesion, rates of aggression and dominance style should be studied because DomWorld does not take into account many relevant biological factors such as feeding ecology, reproductive seasonality, presence of offspring and intergroup competition, all of which could influence patterns of spatial configuration and social interaction. Which factor may underlie the differences in cohesion is uncertain. We indicate three potential causes (e.g. distribution of food, predation pressure and group size) to be studied, as well as the possible interplay between cohesion, group competition and group size.
Why groups of Verreaux’s sifaka did not fit the expected pattern predicted by DomWorld though they were matched in red-fronted and ring-tailed lemurs is unclear. Whether this is related to our limited data on cohesion, their strongly folivorous diet or because they evolved from a lineage separate from the other two species (Kappeler and Pozzi 2019) should be investigated further.
Conclusions
We show that among three species of lemur, spatial cohesion, rate of aggression, dominance style and female dominance over males co-vary in groups as we predicted based on the computational model DomWorld: stronger spatial cohesion among group members contributes to a more despotic dominance style (and greater female dominance over males) via higher rates of aggression and the winner-loser effect. We highlight that studies on dominance style should include the proportion of counter-aggression as a measure of dominance style and relate it to measures of spatial cohesion in groups.
Data availability
The datasets that were analysed for this study are deposited under the link https://doi.org/10.34894/OC4V2A.
Code availability
The computer code that was used to analyse the data is available from the following link: https://doi.org/10.34894/OC4V2A.
References
Balasubramaniam KN, Beisner BA, Berman CM et al (2018) The influence of phylogeny, social style, and sociodemographic factors on macaque social network structure. Am J Primatol 80:e22727. https://doi.org/10.1002/ajp.22727
Balasubramaniam KN, Dittmar K, Berman CM, Butovskaya M, Cooper MA, Majolo B, Ogawa H, Schino G, Thierry B, De Waal FBM (2012) Hierarchical steepness, counter-aggression, and macaque social style scale. Am J Primatol 74:915–925. https://doi.org/10.1002/ajp.22044
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. https://doi.org/10.18637/jss.v067.i01
Brooks ME, Kristensen K, van Benthem KJ, Magnusson A, Berg CW, Nielsen A, Skaug HJ, Mächler M, Bolker BM (2017) glmmTMB balances speed and flexibility among packages for zero-inflated generalized linear mixed modeling. R J 9:378–400. https://doi.org/10.32614/RJ-2017-066
Bryer MAH, Chapman CA, Rothman JM (2013) Diet and polyspecific associations affect spatial patterns among redtail monkeys (Cercopithecus ascanius). Behaviour 150:277–293. https://doi.org/10.1163/1568539X-00003049
Caillaud D (2018) Animal Observer (version 1.0) (Apple iPad Software). https://apps.apple.com/app/animal-observer/id991802313. Accessed 3 March 2018
Cassinello J, Pieters I (2000) Multi-male captive groups of endangered dama gazelle: social rank, aggression, and enclosure effects. Zoo Biol 19:121–129. https://doi.org/10.1002/1098-2361(2000)19:2%3c121::AID-ZOO3%3e3.0.CO;2-1
Cavigelli SA, Dubovick T, Levash W, Jolly A, Pitts A (2003) Female dominance status and fecal corticoids in a cooperative breeder with low reproductive skew: ring-tailed lemurs (Lemur catta). Horm Behav 43:166–179. https://doi.org/10.1016/S0018-506X(02)00031-4
Chase ID, Bartolomeo C, Dugatkin LA (1994) Aggressive interactions and inter-contest interval: how long do winners keep winning? Anim Behav 48:393–400. https://doi.org/10.1006/anbe.1994.1253
Chase ID, Seitz K (2011) Self-structuring properties of dominance hierarchies. Adv Genet 75:51–81
Cherevko LS (2020) Aggressive behavior of black-and-white ruffed (Varecia variegata variegata) and red ruffed (Varecia variegata rubra) lemurs (primates, Lemuridae). Biol Bull 47:1032–1042. https://doi.org/10.1134/S106235902008004X
de la O C, Fürtbauer I, King AJ, Valenzuela-Galván D (2019) A resident-nepotistic-tolerant dominance style in wild white-nosed coatis (Nasua narica)? Behaviour 156:927–968. https://doi.org/10.1163/1568539X-00003547
de Vries H, Stevens JMG, Vervaecke H (2006) Measuring and testing the steepness of dominance hierarchies. Anim Behav 71:585–592. https://doi.org/10.1016/j.anbehav.2005.05.015
de Waal FBM (1989) The myth of a simple relation between space and aggression in captive primates. Zoo Biol 8:141–148. https://doi.org/10.1002/zoo.1430080514
de Winter II, Gollner A, Akom E (2013) Diet overlap of Propithecus verreauxi and Eulemur rufifrons during the late dry season in Kirindy Forest. Lemur News 17:18–21
DeVries TJ, von Keyserlingk MAG, Weary DM (2004) Effect of feeding space on the inter-cow distance, aggression, and feeding behavior of free-stall housed lactating dairy cows. J Dairy Sci 87:1432–1438. https://doi.org/10.3168/jds.S0022-0302(04)73293-2
Digby L, Stevens AM (2007) Maintenance of female dominance in blue-eyed black lemurs (Eulemur macaco flavifrons) and gray bamboo lemurs (Hapalemur griseus griseus) under semi-free-ranging and captive conditions. Zoo Biol 26:345–361. https://doi.org/10.1002/zoo.20140
Dunham AE (2008) Battle of the sexes: Cost asymmetry explains female dominance in lemurs. Anim Behav 76:1435–1439. https://doi.org/10.1016/j.anbehav.2008.06.018
Eichmueller P, Thorén S, Radespiel U (2013) The lack of female dominance in golden-brown mouse lemurs suggests alternative routes in lemur social evolution. Am J Phys Anthropol 150:158–164. https://doi.org/10.1002/ajpa.22189
Erhart EM, Tecot SR, Grassi C (2018) Interannual variation in diet, dietary diversity, and dietary overlap in three sympatric strepsirrhine species in southeastern Madagascar. Int J Primatol 39:289–311. https://doi.org/10.1007/s10764-018-0040-z
Estevez I, Newberry RC, Keeling LJ (2002) Dynamics of aggression in the domestic fowl. Appl Anim Behav Sci 76:307–325. https://doi.org/10.1016/S0168-1591(02)00013-8
Fichtel C, Kappeler PM (2011) Variation in the meaning of alarm calls in Verreaux’s and coquerel’s sifakas (Propithecus verreauxi, P. coquereli). Int J Primatol 32:346–361. https://doi.org/10.1007/s10764-010-9472-9
Fichtel C, Schnoell AV, Kappeler PM (2018) Measuring social tolerance: an experimental approach in two lemurid primates. Ethology 124:65–73. https://doi.org/10.1111/eth.12706
Flack JC, de Waal FBM (2004) Dominance style, social power and conflict. In: Thierry B, Singh M, Kaumanns W (eds) Macaque Societies: A Model for the Study of Social Organization. Cambridge University Press, Cambridge, pp 157–185
Flauger B, Krueger K (2013) Aggression level and enclosure size in horses (Equuscaballus). Pferdeheilkunde 29:495–504. https://doi.org/10.21836/PEM20130404
Fox J, Weisberg S (2019) An R companion to applied regression. Sage Publications, Thousand Oaks, CA
Franz M, McLean E, Tung J, Altmann J, Alberts SC (2015) Self-organizing dominance hierarchies in a wild primate population. Proc R Soc B 282:20151512. https://doi.org/10.1098/rspb.2015.1512
Gammell MP, de Vries H, Jennings DJ, Carlin CM, Hayden TJ (2003) David’s score: a more appropriate dominance ranking method than Clutton-Brock et al’.s index. Anim Behav 66:601–605. https://doi.org/10.1006/anbe.2003.2226
Gemmill A, Gould L (2008) Microhabitat variation and its effects on dietary composition and intragroup feeding interactions between adult female Lemur catta during the dry season at Beza Mahafaly Special Reserve, southwestern Madagascar. Int J Primatol 29:1511–1533. https://doi.org/10.1007/s10764-008-9316-z
Hartig F (2022) DHARMa: residual diagnostics for hierarchical (multi-level / mixed) regression models. https://CRAN.R-project.org/package=DHARMa. Accessed 18 Aug 2022
Hemelrijk CK (1999a) An individual-orientated model of the emergence of despotic and egalitarian societies. Proc R Soc Lond B 266:361–369. https://doi.org/10.1098/rspb.1999.0646
Hemelrijk CK (1999b) Effects of cohesiveness on intersexual dominance relationships and spatial structure among group-living virtual entities. In: Floreano D, Nicoud J-D, Mondada F (eds) Advances in artificial life. Fifth European Conference on Artificial Life, vol 1674. Springer Verlag, Berlin, pp 524–534. https://doi.org/10.1007/3-540-48304-7_71
Hemelrijk CK (2003) Self-organizing properties of primate social behavior: a hypothesis for intersexual rank overlap in chimpanzees and bonobos. Evol Anthropol 11:91–94. https://doi.org/10.1002/evan.10066
Hemelrijk CK, Hildenbrandt H, Reinders J, Stamhuis EJ (2010) Emergence of oblong school shape: models and empirical data of fish. Ethology 116:1099–1112
Hemelrijk CK, Kappeler PM, Puga-Gonzalez I (2017) The self-organization of social complexity in group-living animals: lessons from the DomWorld model. Adv Stud Behav 49:361–405. https://doi.org/10.1016/bs.asb.2017.02.005
Hemelrijk CK, Wantia J, Isler K (2008) Female dominance over males in primates: self-organisation and sexual dimorphism. PLoS One 3:e2678. https://doi.org/10.1371/journal.pone.0002678
Hemelrijk CK, Wubs M, Gort G, Botting J, van de Waal E (2020) Dynamics of intersexual dominance and adult sex- ratio in wild vervet monkeys. Front Psychol 11:839. https://doi.org/10.3389/fpsyg.2020.00839
Höhn M, Kronschnabl M, Gansloßer U (2000) Similarities and differences in activities and agonistic behavior of male Eastern grey kangaroos (Macropus giganteus) in captivity and the wild. Zoo Biol 19:529–539. https://doi.org/10.1002/1098-2361(2000)19:6%3c529::AID-ZOO5%3e3.0.CO;2-L
Hood LC, Jolly A (1995) Troop fission in female Lemur catta at Berenty Reserve, Madagascar. Int J Primatol 16:997–1015. https://doi.org/10.1007/BF02696113
Hsu Y, Earley RL, Wolf LL (2006) Modulation of aggressive behaviour by fighting experience: Mechanisms and contest outcomes. Biol Rev 81:33–74
Irwin MT (2007) Living in forest fragments reduces group cohesion in diademed sifakas (Propithecus diadema) in eastern Madagascar by reducing food patch size. Am J Primatol 69:434–447. https://doi.org/10.1002/ajp.20360
Isbell LA (1991) Contest and scramble competition: patterns of female aggression and ranging behavior among primates. Behav Ecol 2:143–155. https://doi.org/10.1093/beheco/2.2.143
Izar P, Fernández-Bolaños M, Seex L, Gort G, Suscke P, Tokuda M, Mendonça-Furtado O, Verderane MP, Hemelrijk CK (2021) Female emancipation in a male dominant, sexually dimorphic primate under natural conditions. PLoS One 16:e0249039. https://doi.org/10.1371/journal.pone.0249039
Jackson WM (1991) Why do winners keep winning? Behav Ecol Sociobiol 28:271–276. https://doi.org/10.1007/BF00175100
Jolly A (2012) Berenty reserve, Madagascar: a long time in a small space. In: Kappeler PM, Watts DP (eds) Long-Term Field Studies of Primates. Springer, Berlin, pp 21–44
Kappeler PM (1993) Reconciliation and post-conflict behaviour in ringtailed lemurs, Lemur catta and redfronted lemurs, Eulemur fulvus rufus. Anim Behav 45:901–915. https://doi.org/10.1006/anbe.1993.1110
Kappeler PM (1999) Lemur social structure and convergence in primate socioecology. In: Lee PC (ed) Comparative Primate Socioecology. Cambridge University Press, Cambridge, pp 273–299
Kappeler PM, Fichtel C (2012) A 15-year perspective on the social organization and life history of sifaka in Kirindy Forest. In: Kappeler PM, Watts DP (eds) Long-Term Field Studies of Primates. Springer, Berlin, pp 101–121
Kappeler PM, Fichtel C, Radespiel U (2022) The island of female power? Intersexual dominance relationships in the lemurs of Madagascar. Front Ecol Evol 10:858859. https://doi.org/10.3389/fevo.2022.858859
Kappeler PM, Pozzi L (2019) Evolutionary transitions toward pair living in nonhuman primates as stepping stones toward more complex societies. Sci Adv 5:eaay1276. https://doi.org/10.1126/sciadv.aay1276
Kassambara A (2020) ggpubr: “ggplot2” based publication ready plots. R package version 0.4.0. https://rpkgs.datanovia.com/ggpubr/. Accessed 20 June 2022
Klass K, Cords M (2011) Effect of unknown relationships on linearity, steepness and rank ordering of dominance hierarchies: simulation studies based on data from wild monkeys. Behav Process 88:168–176. https://doi.org/10.1016/j.beproc.2011.09.003
Koch F, Ganzhorn JU, Rothman JM, Chapman CA, Fichtel C (2017) Sex and seasonal differences in diet and nutrient intake in Verreaux’s sifakas (Propithecus verreauxi). Am J Primatol 79:e22595. https://doi.org/10.1002/ajp.22595
Koch F, Signer J, Kappeler PM, Fichtel C (2016) The role of the residence-effect on the outcome of intergroup encounters in Verreaux’s sifakas. Sci Rep 6:28457. https://doi.org/10.1038/srep28457
Koenig A (2002) Competition for resources and its behavioural consequences among female primates. Int J Primatol 23:759–783. https://doi.org/10.1023/A:1015524931226
Kosmidis I, Firth D (2021) Jeffreys-prior penalty, finiteness and shrinkage in binomial-response generalized linear models. Biometrika 108:71–82. https://doi.org/10.1093/biomet/asaa052
Kraus C, Heistermann M, Kappeler PM (1999) Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)? Physiol Behav 66:855–861. https://doi.org/10.1016/s0031-9384(99)00024-4
Krause J, Ruxton GD (2002) Living in groups. Oxford University Press, Oxford
LaBarge LR, Allan ATL, Berman CM, Margulis SW, Hill RA (2020) Reactive and pre-emptive spatial cohesion in a social primate. Anim Behav 163:115–126. https://doi.org/10.1016/j.anbehav.2020.03.005
Le Flohic G, Motsch P, DeNys H, Childs S, Courage A, King T (2015) Behavioural ecology and group cohesion of juvenile western lowland gorillas (Gorilla g. gorilla) during rehabilitation in the Batéké Plateaux national park. Gabon. PLoS One 10:e0119609. https://doi.org/10.1371/journal.pone.0119609
Lenth RV (2021) Emmeans: estimated marginal means, aka least-squares means. https://CRAN.R-project.org/package=emmeans. Accessed 27 Jan 2020
Neumann C, Duboscq J, Dubuc C, Ginting A, Irwan AM, Agil M, Widdig A, Engelhardt A (2011) Assessing dominance hierarchies: validation and advantages of progressive evaluation with Elo-rating. Anim Behav 82:911–921. https://doi.org/10.1016/j.anbehav.2011.07.016
Norscia I, Palagi E (2015) The socio-matrix reloaded: from hierarchy to dominance profile in wild lemurs. PeerJ 2015:e729. https://doi.org/10.7717/peerj.729
Oliveira RF, Simes JM, Teles MC, Oliveira CR, Becker JD, Lopes JS (2016) Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain. P Natl Acad Sci USA 113:E654–E661. https://doi.org/10.1073/pnas.1514292113
Palagi E, Antonacci D, Norscia I (2008) Peacemaking on treetops: first evidence of reconciliation from a wild prosimian (Propithecus verreauxi). Anim Behav 76:737–747. https://doi.org/10.1016/j.anbehav.2008.04.016
Partridge BL (1980) Effect of school size on the structure and dynamics of minnow schools. Anim Behav 28:68–77. https://doi.org/10.1016/S0003-3472(80)80009-1
Pereira ME, Kappeler PM (1997) Divergent systems of agonistic behaviour in lemurid primates. Behaviour 134:225–274. https://doi.org/10.1163/156853997x00467
Puga-Gonzalez I, Butovskaya M, Thierry B, Hemelrijk CK (2014) Empathy versus parsimony in understanding post-conflict affiliation in monkeys: model and empirical data. PLoS One 9:e91262. https://doi.org/10.1371/journal.pone.0091262
Puga-Gonzalez I, Hildenbrandt H, Hemelrijk CK (2009) Emergent patterns of social affiliation in primates, a model. PLoS Comput Biol 5:e1000630. https://doi.org/10.1371/journal.pcbi.1000630
R Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org. Accessed 31 Aug 2021
Remience V, Wavreille J, Canart B, Meunier-Salaün MC, Prunier A, Bartiaux-Thill N, Nicks B, Vandenheede M (2008) Effects of space allowance on the welfare of dry sows kept in dynamic groups and fed with an electronic sow feeder. Appl Anim Behav Sci 112:284–296. https://doi.org/10.1016/j.applanim.2007.07.006
Rina Evasoa M, Zimmermann E, Hasiniaina AF, Rasoloharijaona S, Randrianambinina B, Radespiel U (2019) Sources of variation in social tolerance in mouse lemurs (Microcebus spp.). BMC Ecol 19:20. https://doi.org/10.1186/s12898-019-0236-x
Roeder JJ, Fornasieri I, Gosset D (2002) Conflict and postconflict behaviour in two lemur species with different social organizations (Eulemur fulvus and Eulemur macaco): a study on captive groups. Aggressive Behav 28:62–74. https://doi.org/10.1002/ab.90006
RStudio Team (2020) Rstudio: integrated development environment for R. RStudio PBC., Boston, MA. https://www.rstudio.com/. Accessed 31 Aug 2021
Rudolph K, Fichtel C, Heistermann M, Kappeler PM (2020) Dynamics and determinants of glucocorticoid metabolite concentrations in wild Verreaux’s sifakas. Horm Behav 124:104760. https://doi.org/10.1016/j.yhbeh.2020.104760
Samuni L, Mielke A, Preis A, Crockford C, Wittig RM (2020) Intergroup competition enhances chimpanzee (Pan troglodytes verus) in-group cohesion. Int J Primatol 41:342–362. https://doi.org/10.1007/s10764-019-00112-y
Sannen A, van Elsacker L, Eens M (2004) Effect of spatial crowding on aggressive behaviour in a bonobo colony. Zoo Biol 23:383–395. https://doi.org/10.1002/zoo.20024
Sauther ML (1993) Resource competition in wild populations of ringtailed lemurs (Lemur catta): Implications for female dominance. In: Kappeler PM, Ganzhorn JU (eds) Lemur Social Systems and Their Ecological Basis. Springer, US, Boston, MA, pp 135–152
Schnoell A, Fichtel C (2012) Predation on redfronted lemurs (Eulemur rufifrons) by fossas (Cryptoprocta ferox). Lemur News 16:30–32
Schreier AL, Swedell L (2012) Ecology and sociality in a multilevel society: ecological determinants of spatial cohesion in hamadryas baboons. Am J Phys Anthropol 148:580–588. https://doi.org/10.1002/ajpa.22076
Simmen B, Sauther ML, Soma T, Rasamimanana H, Sussman RW, Jolly A, Tarnaud L, Hladik A (2006) Plant species fed on by Lemur catta in gallery forests of the southern domain of Madagascar. In: Jolly A, Sussman RW, Koyama N, Rasamimanana H (eds) Ringtailed lemur biology. Developments in primatology: progress and prospect. Springer, Boston, pp 55–68. https://doi.org/10.1007/978-0-387-34126-2_5
Snaith TV, Chapman CA (2007) Primate group size and interpreting sociolecological models: do folivores really play by different rules? Evol Anthropol 16:94–106. https://doi.org/10.1002/evan.20132
Sogard SM, Olla BL (1997) The influence of hunger and predation risk on group cohesion in a pelagic fish, walleye pollock Theragra chalcogramma. Environ Biol Fish 50:405–413. https://doi.org/10.1023/A:1007393307007
Sterck EHM, Watts DP, van Schaik CP (1997) The evolution of female social relationships in nonhuman primates. Behav Ecol Sociobiol 41:291. https://doi.org/10.1007/s002650050390
Szemán K, Liker A, Székely T (2021) Social organization in ungulates: revisiting Jarman’s hypotheses. J Evol Biol 34:604–613. https://doi.org/10.1111/jeb.13782
Teles MC, Dahlbom SJ, Winberg S, Oliveira RF (2013) Social modulation of brain monoamine levels in zebrafish. Behav Brain Res 253:17–24. https://doi.org/10.1016/j.bbr.2013.07.012
Thierry B (2008) Primate socioecology, the lost dream of ecological determinism. Evol Anthropol 17:93–96. https://doi.org/10.1002/evan.20168
Thierry B (2021) Where do we stand with the covariation framework in primate societies? Am J Biol Anthropol 178:5–25. https://doi.org/10.1002/ajpa.24441
Thierry B (2000) Covaration of conflict management patterns across macaque species. In: Aureli F, de Waal FBM (eds) Natural Conflict Resolution. University of California Press, Berkeley, pp 106–128
Thierry B, Singh M, Kaumanns W (eds) (2004) Macaque Societies. Cambridge University Press, Cambridge
Tyutyunov YV, Titova LI (2017) Simple models for studying complex spatiotemporal patterns of animal behavior. Deep-Sea Res Pt II 140:193–202. https://doi.org/10.1016/j.dsr2.2016.08.010
van Schaik CP (1989) The ecology of social relationships amongst female primates. In: Standen V, Foley GRA (eds) Comparative Socioecology. Blackwell, Oxford, pp 195–218
Vehrencamp SL (1983) A model for the evolution of despotic versus egalitarian societies. Anim Behav 31:667–682
Wickham H (2016) ggplot2: elegant graphics for data analysis. Springer, New York
Wrangham RW (1980) An ecological model of female-bonded primate groups. Behaviour 75:262–300. https://doi.org/10.1163/156853980X00447
Zárate DA, Stevenson PR (2014) Behavioral ecology and interindividual distance of woolly monkeys (Lagothrix lagothricha) in a rainforest fragment in Colombia. In: Defler TR, Stevenson PR (eds) The Woolly Monkey. Springer, New York, pp 227–245
Acknowledgements
We thank the Commission Tripartite de Direction des Eaux et Forêts and the CNFEREF Morondava for their authorization and support for this study. We are grateful to Ms. Claire Foulon, Ms. Bénédicte de Heaulme and their family members for their kind permission to carry out our studies and their hospitality at Berenty Reserve. We thank the Kirindy and Berenty field assistants for help with data collection and logistical support. We thank Maria van Noordwijk and Christof Neumann as well as one anonymous reviewer for helpful comments and discussion that improved the manuscript.
Funding
This work was financially supported by the Dobberke Foundation, the Leverhulme Foundation Study Abroad Studentship awarded to LS and the Lucie Burgers foundation for Comparative Behaviour Research and Westerdijk talent impuls premie awarded to CKH, and the Deutsche Forschungsgemeinschaft (DFG Fi 929/5–1) awarded to CF.
Author information
Authors and Affiliations
Contributions
CKH and LS conceived the study. LS conducted the data analysis. LS performed data collection for data collected in 2018, other data were provided from previous projects by CF and PMK. LS drafted the manuscript and all authors contributed to writing and revising of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
All research adhered to the legal requirements of Madagascar. Research in Kirindy Forest and Berenty Reserve was approved by a committee of the Ministry for the Environment, Water and Forests of Madagascar (MINEEF) (Permit number: 394–10/MEF/SG/DGF/SVRN/SGFF). The use of animals adheres to the guidelines set forth by the Animal Behavior Society/Association for the Study of Animal Behaviour. Further ethics approval was not required.
Consent for publication
The authors consent to the publication of this manuscript in Behavioral Ecology and Sociobiology.
Conflict of interest
The authors declare no competing interests.
Additional information
Communicated by M. A van Noordwijk
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
About this article
Cite this article
Seex, L., Fichtel, C., Kappeler, P.M. et al. Interrelationship among spatial cohesion, aggression rate, counter-aggression and female dominance in three lemur species. Behav Ecol Sociobiol 76, 133 (2022). https://doi.org/10.1007/s00265-022-03241-2
Received:
Revised:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00265-022-03241-2