Sickness effects on social interactions depend on the type of behaviour and relationship

Abstract

Infections can change social behaviour in multiple ways, with profound impacts on pathogen transmission. However, these impacts might depend on the type of behaviour, how sociality as a biological trait is defined (e.g. network degree vs. mean edge strength) and the type of social relationship between the interacting individuals. We used the highly social common vampire bat Desmodus rotundus to test how an immune challenge by lipopolysaccharide (LPS) injections affects two different social behaviours and three alternate measures of sociality, and whether the LPS effect differs by kinship relationship. Effects of sickness should be lower for social behaviours that bestow greater benefits to inclusive fitness, such as food sharing. As predicted, immune‐challenged bats experienced a greater reduction in allogrooming received than food sharing received. Sickness effects might also depend on how a social interaction is defined (e.g. the number of grooming partners vs. the duration of grooming events). We predicted that sickness would impact both the number and duration of social encounters, but we only detected a decrease in the number of grooming partners. Finally, sickness effects might vary with social relationship type. We predicted that sickness effects should be smaller for interactions among close kin. As expected, the immune challenge had smaller effects on mother–offspring interactions. In conclusion, our results highlight the need to explicitly consider how the effects of sickness on social network structure can differ depending on the ‘who, what, and how’ of social interactions, because these factors are likely to influence how sickness behaviour alters pathogen transmission.

Sickness behaviour reduces network centrality in wild vampire bats

“…They also produce fewer contact calls [12], which attract bonded partners [13]. When tested in a flight cage, ‘sick’ vampire bats engaged in social grooming with fewer partners [6], but we observed dramatic reductions in social grooming even when captive pairs were forced into close association [7]. LPS-induced sickness behaviours therefore reduce both associations and behaviours, like social grooming, which can further enhance pathogen transmission between associated bats.…”

“…We randomly assigned the females to the test or control treatment by flipping a coin, then adjusted to ensure more balanced samples. We injected the individuals in the test group under the dorsal skin with 70-100 μl of LPS (lipopolysaccharide in phosphate-buffered saline, L2630 Sigma-Aldrich, St Louis, MO, U.S.A.) at a dosage of 5 mg/kg, following previous studies with this species [6, 7]. Bats in the control group received an injection of the same volume per body mass of phosphate-buffered saline.…”

“…We released them back into their wild colony and tracked changes in their association rates. Based on the effects of LPS on the physiology and behaviour of captive vampire bats [6, 7], we predicted reduced association rates between ‘sick’ bats and control bats in the wild.…”

Immune-challenged vampire bats produce fewer contact calls

“…Besides courtship vocalizations, a broader range of vocal interactions could be influenced by 60 sickness, but these other call types have received less attention. In many group-living animals that live in 61 conditions of low visibility, or that must maintain cohesion while on the move, individuals produce 62 contact calls to maintain contact with groupmates or particular affiliated individuals (Arnold and 63 bats are groomed by fewer bats and have lower social connectedness in the wild, an effect that could be 82 driven in part by a reduction in contact calling (Ripperger et al, 2020;Stockmaier et al, 2020). We show 83 that LPS-induced sickness behavior decreases the number of contact calls produced by isolated vampire 84 bats.…”

“…In LPS trials, we induced sickness behavior in subjects 99 by injecting them subcutaneously with lipopolysaccharide (LPS, L2630 Sigma-Aldrich, USA, dose: 5 100 mg/kg body mass of bat) in phosphate-buffered saline (PBS) before the recording period. We chose this 101 dose based initially on observed effects in another bat species (Stockmaier et al, 2015), and on later 102 studies in vampire bats, which showed that this dose increases white blood cell count and neutrophil to 103 lymphocyte ratio (Stockmaier et al, 2018) and decreases in physical activity, social encounters, and social 104 grooming (Ripperger et al, 2020;Stockmaier et al, 2020Stockmaier et al, , 2018. In control trials, the same bats were 105 injected with an equivalent volume of only PBS as a control treatment.…”