Networks provide an ideal tool to link social behaviour and infection in animal societies (White et al. 2017). A major focus of previous research has been on the links between social centrality and infection (Briard & Ezenwa 2021). But what happens when conclusions are drawn from sampled networks in which some individuals are not observed, or when studies focus on some individuals at the expense of others (e.g. adults versus juveniles or females versus males)? Xu et al. (2022) examine how focusing on different samples of individuals in a network analysis relating centrality to parasite load in Japanese macaques Macaca fuscata influence the conclusions drawn.

Xu et al. (2022) use faecal egg counts to estimate parasite loads of three environmentally transmitted parasites Oesophagostomum aculeatum, Strongyloides fuelleborni and Trichuris trichiura in a group of macaques on Koshima Island, Japan. After showing positive associations between parasite load and strength (the sum of an individual’s connections) and eigenvector centrality (accounting for second-order connections) in a 1-metre proximity network, the authors explore how this result is impacted by focusing on only adult females, only juveniles or random sub-samples of the population. Their results indicate that the positive association persists more strongly in the adult female networks albeit with reduced statistical power to detect it. It is largely absent in juveniles (either based on their centrality in the full network or centrality in the juvenile-only network). Random removal of individuals from the network led to a rapid reduction in the ability to detect the same positive association between centrality and parasite load due to a combination of changes in individual centrality in re-sampled networks and reduced statistical power. 

The timescale of network data collection and proximity networks studied are (likely) not fully relevant for the transmission of these parasites and social transmission of the parasites studied here is likely to be limited, there remain other reasons that we may expect correlations between sociality and infection (Ezenwa et al. 2016). Nevertheless, this is a useful contribution to the literature on sampling effects in animal networks, complementing existing work (Franks et al. 2010, Silk et al. 2015, Davis et al. 2018, Silk 2018). The results from considering different sub-samples of the group show the potential importance of carefully considering whether social network effects will be equivalently important for the whole population and which interactions will contribute either to promoting health or increasing the risk of infection. The results of random sub-sampling show how in small (within-group) networks such as these even small numbers of missing individuals could have substantial impacts on testing how traits are associated with the social network position of individuals.

The findings set up some interesting questions about how best to develop effective sampling designs in single-group studies such as these, or in how best to extend these types of projects across multiple groups (see also Silk 2018). Testing the generality of these findings across taxa with different social systems and infection prevalences or loads will also be a valuable next step for behavioural disease ecology.

References

Briard L, Ezenwa VO. 2021. Parasitism and host social behaviour: a meta-analysis of insights derived from social network analysis. Anim. Behav. 172, 171-182. https://doi.org/10.1016/j.anbehav.2020.11.010

Davis GH, Crofoot MC, Farine DR. 2018. Estimating the robustness and uncertainty of animal social networks using different observational methods. Anim. Behav. 141, 29-44. https://doi.org/10.1016/j.anbehav.2018.04.012

Ezenwa VO, Ghai RR, McKay AF, Williams AE. 2016. Group living and pathogen infection revisited. Curr. Opin. Behav. Sci. 12, 66-72. https://doi.org/10.1016/j.cobeha.2016.09.006 

Franks DW, Ruxton GD, James R. 2010. Sampling animal association networks with the gambit of the group. Behav. Ecol. Sociobiol. 64, 493-503. https://doi.org/10.1007/s00265-009-0865-8

Silk MJ, Jackson AL, Croft DP, Colhoun K, Bearhop S. 2015. The consequences of unidentifiable individuals for the analysis of an animal social network. Anim. Behav. 104, 1-11. https://doi.org/10.1016/j.anbehav.2015.03.005

Silk MJ. 2018. The next steps in the study of missing individuals in networks: a comment on Smith et al. (2017). Soc. Net. 52, 37-41. https://doi.org/10.1016/j.socnet.2017.05.002

White LA, Forester JD, Craft ME. 2017. Using contact networks to explore mechanisms of parasite transmission in wildlife. Biol. Rev. 92, 389-409. https://doi.org/10.1111/brv.12236

Xu Z, MacIntosh AJJ, Castellano-Navarro A, Macanás-Martinez E, Suzumura T, Dubosq J. 2022. Linking parasitism to network centrality and the impact of sampling bias in its interpretation. bioRxiv 2021.06.07.447302, ver. 6 peer-reviewed and recommended by Peer Community in Network Science. https://doi.org/10.1101/2021.06.07.447302 

In their article “Behavioural synchronization in a multilevel society of feral horses”, Maeda and colleagues (2021) use stochastic multi-agent based modeling to explore the degree to which feral horses synchronize their behavior across multiple levels of organization. The authors compare a drone-derived empirical data set on a feral population of horses with simulated data from multi-agent-based models to determine whether behavioral synchronization of resting and movement states in a multilevel society can be described by one of three models: A) independent model in which horses do not synchronize, B) anonymous model in which horses synchronize with any individual in any unit, C) unit-level social model in which horses synchronize only within units and D) herd-level social model in which horses synchronize across and within units, but internal synchronization is stronger. In a series of 100 simulations for each of seven different models, the authors conclude that evidence for the herd-level model had the strongest support in relation to the empirical data. This finding suggests that connections among individuals in such multi-level societies are rather complex in that local connections are not the only interactions driving social behavior, and specifically synchronization. This approach could be successfully applied to a number of different species that exhibit multi-level organization and possibly fission-fusion dynamics.

This study is especially innovative and interesting for three major reasons. First, the use of drone technology to successfully identify individual animals and generate social networks is highly novel and permits the study of large multi-level social groups of animals that previously have been challenging to study due to limitations in collecting data at an appropriate scale. Second, the comparison of multi-agent-based models with actual empirical data is highly applauded. Most agent-based studies design their parameters from previous empirical studies, (sometimes with questionably simple assumptions) but rarely do they actually compare model outputs to their own empirical data. This is an important next step in the burgeoning field of agent-based modeling. Finally, this study sheds light on the utility of using relatively simple mathematical models to explain highly complex behavior. It also highlights that feral horses can synchronize their behavior beyond clustered local connections which suggests that they possess the cognitive ability to track the behavior of individuals at higher social orders. As the authors state, in a multilevel society, inter-unit distance should be moderate, that is “not too close but not too far” because this strategy simultaneously avoids inter-unit competition while also providing the benefits of social buffering that comes with large group living, such as protection from bachelors or predators.

As the authors dutifully note, there were also some limitations to the study: (1) the relatively sparse empirical dataset that made it difficult to resolve the relative fitness of the two herd-level models (absolute versus proportional social models), (2) the lack of a temporal component that would provide a better understanding on how synchronization flows through the social/spatial network, and (3) the limited variation in the parameters tested which constrained identification of their true function in the model. Such limitations, however, provide fruitful avenues for further development of the model in future studies.

Overall then, this study provides new insights into the processes underlying the behavioral synchronization process and thus nicely contributes to the understanding of collective behaviors in complex animal societies as well as the evolution and functional significance of multi-level animal societies. This study is a fine addition to both the fields of agent-based modeling and the evolution of collective behavior in complex societies. I thus highly endorse its publication.

References

Maeda T, Sueur C, Hirata S, Yamamoto S (2021) Behavioural synchronization in a multilevel society of feral horses. bioRxiv, 2021.02.21.432190,  ver. 3 peer-reviewed and recommended by Peer community in Network Science. https://doi.org/10.1101/2021.02.21.432190