25/01/2023
Abstract
In despotically driven animal societies, one or a few individuals tend to have a disproportionate influence on group decision-making and actions. However, global communication allows each group member to assess the relative strength of preferences for different options among their group-mates. Here, we investigate collective decisions by free-ranging African wild dog packs in Botswana. African wild dogs exhibit dominant-directed group living and take part in stereotyped social rallies: high energy greeting ceremonies that occur before collective movements. Not all rallies result in collective movements, for reasons that are not well understood. We show that the probability of rally success (i.e. group departure) is predicted by a minimum number of audible rapid nasal exhalations (sneezes), within the rally. Moreover, the number of sneezes needed for the group to depart (i.e. the quorum) was reduced whenever dominant individuals initiated rallies, suggesting that dominant participation increases the likelihood of a rally's success, but is not a prerequisite. As such, the ‘will of the group’ may override dominant preferences when the consensus of subordinates is sufficiently great. Our findings illustrate how specific behavioural mechanisms (here, sneezing) allow for negotiation (in effect, voting) that shapes decision-making in a wild, socially complex animal society.
1. Background
Group consensus is ubiquitous in social invertebrate and vertebrate animals [1] and is necessary for individuals to reap the benefits of group living—including added protection from predators, greater information sharing and better defence of resources [2]. One of the most obvious instances of group coordination in social animals is the decision to move off from a resting spot [3]. Signals used by individuals in the pre-departure and foraging stage of group movement have been described across taxa [4] and often operate in a type of quorum, where a specific signal has to reach a certain threshold before the group changes activity [4,5]. This ensures that a minimum number of individuals (the actual quorum number) are ready to move off [4]. Past research in meerkats, Suricata suricatta, for example, has found that a quorum of at least two and usually three meerkats emitting ‘moving calls’ are necessary for the whole group to move to a new foraging patch, and ‘piping signals’ in honeybees, Apis mellifera [6], and ‘trills’ in white faced capuchin monkeys, Cebus capucinus, [7] are required for collective departures to occur.
Certain individuals can also have a disproportionate influence on collective behaviour decisions within social systems that exhibit variation in inter-individual relationships (e.g. kinship and dominance structures, see [8,9]). For example, dominance rank and/or an individual's social role (measured as social affiliation strength to others) are often found to correlate with leadership roles, a phenomenon observed pervasively in primates [10]. In social canids, research on group living has focused largely on the role of dominants in directing and repressing subdominant behaviour in group decision-making [11].
Here, we investigate the collective decisions of African wild dog (Lycaon pictus) packs in Botswana during the transition from a sedentary resting state to an active moving state. African wild dogs are the ‘most social canid’ and exhibit uniquely non-aggressive, dominant directed group living, exemplified by stereotyped social rallies [12–14]: high energy, socially intricate pre-departure greeting ceremonies that are ‘conspicuous’, ‘highly ritualized’, and are ‘of high adaptive value…and serve to hold the pack together’ [13]. Dominant breeding pairs in an African wild dog pack affect the behaviour of the pack as a whole; the dominant-directed social system facilitates feeding by pups at kill sites [15], suppresses sub-dominant pregnancies [16], and ensures collective care for a denning female and pups [17]. However, little is known about the extent to which dominants, or single individuals, drive behaviour outside the reproductive realm. Sueur & Petit [3], assert that African wild dogs (Lycaon pictus) likely use ‘shared consensus’, in which all group members participate in the decision-making process, because their ‘open social system’ is defined by pervasive cooperation. However, no study has systematically investigated how these social carnivores make collective decisions.
Given that African wild dog packs are characterized by pervasive cooperation [12,14] and show intricate pre-departure greeting ceremonies [12–14], we expected a majority or all group members to participate in group consensus about departures. However, because dominant individuals are known to steer many types of group activities [16–18], we expected dominants to have a disproportionate influence in this process. We therefore tested the overall hypothesis that African wild dogs exhibit ‘partially shared consensus’ decisions [3,18].
It is known in several other animal species that the number and identity of individuals participating in the decision process can influence the outcome of collective decisions, and that valuable experience may be correlated with age or dominance [9,19,20]. Moreover, specific recruitment cues or signals may help guide conspecifics [9] or even be used as a type of voting mechanism [4]. Therefore, to understand the mechanisms by which packs reach a consensus [15] we gathered data relating to the proportion of the pack engaged in social behaviour, individual participation, and the role of potential communication mechanisms to negotiate timing of departure. Since African wild dogs display dominant-directed group living [20,21] we examined to what extent individual participation in rallies, and specifically the dominants' participation, affected the likelihood of a successful group movement. Preliminary observations during rallies indicated that audible, abrupt exhalations of air through the nose, ‘sneezes’ (figure 1; see electronic supplementary material video), appeared to be frequent during rallies and may serve as a pre-departure cue or signal [15]. Therefore we investigated the potential for the occurrence of sneezes to serve as a voting mechanism that determines whether the pack should depart [4,22] while also considering the relative importance of other factors: the dominance status of the initiator [9], the level of social participation [10], and the number of other departure events that day [11].
Figure 1.
Figure 1. Spectrogram of dominant male African wild dog ‘sneeze’ recorded prior to a group departure event. This example spectrogram was prepared in CoolEdit Pro 2002 (v. 2.0, Syntrillium Software Corporation, Phoenix, AZ), with 44 100 sampling rate visualized in Hamming window, resolution 1024 bands, and linear energy plot at 20% scaling. The spectrogram shows linear bars (likely an intake of breath), followed by atonal high-frequency bandwidth rapid exhalation, or ‘sneeze’. Energy is shown from light (low) to dark (high).
Download figureOpen in new tabDownload PowerPoint
2. Methods
Data were collected from five packs (Inline Formula adult group size = 8.80 ± 3.63) of African wild dogs in and around the Moremi Game Reserve in the Okavango Delta from June 2014 to May 2015. At least one individual in each pack was fitted with a VHF radio collar (ca. 180 g; Sirtrack, Havelock West, New Zealand) using darting and immobilization procedures described previously [23]. Collars allowed packs to be located and were replaced when they failed. Some individuals remained collared following the completion of this study as they formed part of a long-term study conducted by the Botswana Predator Conservation Trust (BPCT) spanning the past 25 years [20]. All individuals (N = 49) were identified by their unique pelage patterns, and ages and life histories were known for all individuals except some immigrants (N = 10). We estimated the age classes (adult, yearling, or pup) of these 10 individuals using a combination of body size, pelage development, testicular development, and tooth and ear wear. All work was conducted in accordance with the guidelines for the treatment of animals in behavioural research and teaching [24].
To explore the dynamics of collective movement decisions, packs were observed from a vehicle (N = 52 days; Inline Formula days/pack/month = 2.03 ± 0.50), and their behaviours were recorded during rally periods via direct observation (scan and continuous sampling) and video recordings (Nikon, COOLPIX S7000). Rallies were initiated when an individual rose from rest in the distinctive initiation posture: head lowered, mouth open, and ears folded back [13]. These initiators were identified. Not all rallies resulted in collective movements, and rallies were considered to have ended when all individuals either returned to rest or departed the resting site. We observed 1.92 ± 0.54 (Inline Formula) rallies per observation session (N = 68 rallies; Inline Formula per pack = 14.2 ± 6.75).
From video data, we performed behavioural scans every 5 s from initiation until the end of the rally. We used critical incident sampling to record the number of audible, abrupt exhalation of air through the nose, or ‘sneezes’, during rally attempts and calculated the aggregated frequency of sneeze events per minute before and after the end of rallies. ‘Sneezes’ are atonal high-frequency bandwidth rapid exhalations that are stereotyped and obvious in rallies (figure 1). We observed sneezes while individuals were walking with their heads hanging or standing with their ears alert and tail relaxed (electronic supplementary material video). Other dogs did not startle in response to these vocalizations, or look toward the sneezer, as might be expected if the sounds were associated with a threat display or a sign of alarm. While it was clear from video data how many sneezes occurred during a rally, the thick habitat prevented us from being able to routinely identify which individuals sneezed, and so we only measure frequency, and not identity, of sneezers. For each behavioural scan, we recorded which individuals participated in one or more of three stereotypical social interactions: ‘Greet’, when individuals touched heads or approached within 1 m of one another; ‘Parallel Run’, when individuals ran flank to flank; and ‘Mob’, when three or more individuals gathered within 1 m of one another [12,13]. The proportion of adults participating in these interactions ranged from 0 (rallies in which there was no social behaviour or only yearlings and pups interacted) to 1 (rallies in which all adults were actively engaged at one point, though not necessarily simultaneously).
In a variety of animal systems, the identity, social status, or age–sex class of the individual initiating a collective movement (i.e. moving away from the resting group) can be critical to the likelihood of a collective departure [9,18,19]. Because relative rank beneath the dominant pair is not readily decipherable within African wild dog packs, we used priority of access to carcasses (POA) as a proxy for dominance: the dominant pair and their pups (less than 1 year) have first access to kills (POA1), followed by yearlings, (POA2), and subdominant adults (more than 2 years) (POA3) [20,21].
We used simple bivariate tests, such as chi-square and the binomial test for equality of proportions conducted in the package R with significance level 0.05, to initially explore relationships between rally success (departure/no departure) and recorded observations of order of rally attempt, proportion of adults participating in social behaviour, dominants' participation in rallies, number of sneezes, and initiator demographic [25]. To further investigate the factors affecting whether a social rally resulted in the pack departing (1) or not (0) from their current rest site, we ran a series of binomial generalized linear mixed effects models (GLMMs) in the package ‘lme4’ [26] in R [25]. Eleven out of 68 rallies were excluded from these specific analyses as their ultimate success or failure and/or the identity of the initiator was not determined. Terms included in the model set were: total number of sneezes in a rally, the initiator's priority of access to kills (1, 2, 3), consecutive attempt number per observation session, and the proportion of adults participating in social behaviours. Pack identity was included as a random term in the models to control for repeated measures. We used Akaike's information criterion to select the most plausible model from a set of credible options. All terms and their two-way interactions were sequentially added to the basic model, with each retained only if it reduced the AIC by two or more as lower AIC values correspond to better relative support for each model [27]. To validate that there was no improvement to the minimal model, each term was then removed sequentially from the minimal model. Terms were retained only if their removal inflated AIC by more than two [28] As the Akaike weight of the best model was less than 0.9 and several models had deviance in the AIC lower than seven units [29,30], we conducted model averaging using the MuMIn package [31]. We selected the top models whose cumulative AIC weights were more than 0.95 to construct model-averaged estimates of the parameters [28] Model diagnostics were performed by inspection using the DHARMa package, which uses a simulation-based approach to create readily interpretable scaled residuals from fitted GLMMs [32] Data from all top models included in model averaging met model assumptions.
