Urinary oxytocin and social bonding in related and unrelated wild chimpanzees

Oxytocin concentration of urine samples was measured using an established method to sample specific events.

“We conducted focal animal sampling (23) for 20 adult male and female chimpanzees of two neighboring groups, and measured the oxytocin concentration of urine samples from all individuals using an established method to sample specific events (19, 20).”

All samples relating to a target context were collected within the time window of oxytocin excretion into urine at least 15 min after the start and up to 60 min after the end of interactions.

“All samples relating to a target context were collected within the time window of oxytocin excretion into urine at least 15 min after the start and up to 60 min after the end of interactions (19, 20).”

The oxytocinergic system in chimpanzees is involved in prosocial and cooperative behavior between both kin and nonkin group members, such as grooming and food sharing.

“Also similar to humans, the oxytocinergic system in chimpanzees is involved in prosocial and cooperative behavior between both kin and nonkin group members, such as grooming (19) and food sharing (20), suggesting parallels in oxytocinergic system involvement between humans and chimpanzees.”

Oxytocin validations of parallelism and accuracy were conducted and appeared satisfactory.

“Oxytocin validations of parallelism and accuracy were conducted and appeared satisfactory (19).”

Urinary oxytocin measures show biobehaviorally relevant levels following target behaviors or social interactions that occur within the 15 to 60 min time window.

“Urinary oxytocin measures show biobehaviorally relevant levels following target behaviors or social interactions that occur within this time window (19, 20).”

The clearance of oxytocin into urine in chimpanzees was taken to be 15 to 60 min after secretion, adapted from a human clearance study.

“We took the clearance of oxytocin into urine in chimpanzees to be 15 to 60 min after secretion (19, 20), adapted from a human clearance study (43).”

In chimpanzees, grooming among bonding partners is associated with higher urinary oxytocin concentration than grooming between non-bonding partners.

“Such a link is also evident in chimpanzees, where grooming among bonding partners is associated with higher urinary oxytocin concentration than grooming between non-bonding partners [15].”

The measurement of urinary chimpanzee oxytocin levels was validated through parallelism and accuracy tests.

“We validated the measurement of urinary chimpanzee oxytocin levels through parallelism and accuracy tests, as described in a previous paper [15].”

Sharers may experience a mutual increase in positive attitude, resulting in the promotion of stronger social bonds and longer-term benefits of more frequent cooperation.

“Also, as oxytocin is thought to act on positive feedback circuits [16,17,21], sharers may experience a mutual increase in positive attitude [15,79,80], resulting in the promotion of stronger social bonds and longer-term benefits of more frequent cooperation [23,26,80].”

Food sharing in chimpanzees is non-random, being more likely within dyads that engage in high rates of other cooperative behaviours.

“Its occurrence is non-random, given that food sharing is more likely within dyads that engage in high rates of other cooperative behaviours [7,15,52,78].”

Food sharing in chimpanzees occurs between kin, in sexual contexts, and also between non-kin adults in non-sexual contexts, which is unusual in the animal kingdom.

“What makes food sharing in chimpanzees unusual in the animal kingdom is that, as well as occurring between kin [52] and in sexual contexts [50], food sharing also occurs between non-kin adults in non-sexual contexts [13,15,52,53].”

There is some evidence that oxytocin release is more likely during interactions with certain individuals, such as bond partners.

“There is some evidence that oxytocin release is more likely during interactions with certain individuals, such as bond partners (Seltzer et al., 2010; Crockford et al., 2013).”

Urinary oxytocin levels in chimpanzees were not different from resting controls when grooming occurred with a non-bonded partner.

“However, urinary oxytocin levels were not different from resting controls when grooming occurred with a non-bonded partner (Crockford et al., 2013).”

Free-ranging male and female chimpanzees had higher urinary oxytocin levels following at least 10 min of grooming with a bond partner compared with resting controls.

“Free-ranging male and female chimpanzees had higher urinary oxytocin levels following at least 10 min of grooming with a bond partner compared with resting controls.”

In wild chimpanzees, allo-grooming and food sharing were associated with significantly higher urinary oxytocin levels than non-cooperative behaviors, feeding in the presence of others without sharing, or resting.

“Two cooperative behaviors, allo-grooming and food sharing, were associated with significantly higher urinary oxytocin levels than non-cooperative behaviors, feeding in the presence of others without sharing, or resting.”

In the food sharing context, urinary oxytocin levels were high irrespective of the valence of the relationship between sharing partners.

“In the food sharing context, however, urinary oxytocin levels were high irrespective of the valence of the relationship between sharing partners.”

The effects of cooperative acts on urinary oxytocin were similar whether subjects were donors or recipients of grooming or food sharing, and whether donors and receivers were male or female.

“The effects were similar whether subjects were donors or recipients of grooming or food sharing, and whether donors and receivers were male or female.”

In the grooming context, only subjects who groomed with bond partners, as opposed to known but neutral others, had higher urinary oxytocin levels than in the resting condition.

“In the grooming context, only subjects who groomed with bond partners, as opposed to known but neutral others, had higher urinary oxytocin levels than in the resting condition.”

Non-invasive sampling allows repeated measures to be examined in relation to particular social interactions or individuals within the subjects' normal social and physical environment.

“non-invasive sampling allows repeated measures to be examined in relation to particular social interactions or individuals within the subjects' normal social and physical environment (Holt-Lunstad et al., 2008; Crockford et al., 2013; Wittig et al., 2014).”

The action of OT in social processing seems to critically depend on the history of social interactions between two individuals.

“Therefore, the action of OT in social processing seems to critically depend on the history of social interactions between two individuals.”

Urinary OT levels after grooming behaviors predicted the strength of social bonds among partners in wild chimpanzees, and this effect was not explained by genetic relatedness.

“A recent study in wild chimpanzees (Pan troglodytes) measured urinary OT levels after grooming bouts with different partners (Crockford et al., 2013). urinary OT levels after grooming behaviors predicted the strength of social bonds among the partners, and, surprisingly, this effect was not explained by genetic relatedness.”

In chimpanzees, excreted OT levels were higher following grooming bouts with a bonded partner (regardless of genetic relatedness) than a non-bonded partner.

“In chimpanzees, excreted OT levels were higher following grooming bouts with a bonded partner (regardless of genetic relatedness) than a non-bonded partner (Crockford et al., 2013).”