Behavioral and endocrine consequences of placentophagia in male California mice (Peromyscus californicus)

Abstract

Ingestion of placenta by mammalian mothers can lead to changes in pain sensitivity, hormone levels, and behavioral responses to newborns. In some biparental mammals, males, in addition to females, ingest placenta when their offspring are born. In the monogamous, biparental California mouse (Peromyscus californicus), males first become attracted to placenta when cohabitating with their pregnant mate, and virgin males administered placenta are less neophobic than males given oil vehicle. In this study, we investigated the effects of placentophagia on pain sensitivity, anxiety-like behavior, behavioral responses to pups, and circulating corticosterone levels of both breeding and nonbreeding male California mice. We orally administered either a conspecific placenta or oil vehicle to male mice from three reproductive conditions (first-time fathers, first-time expectant fathers, and virgin males) and tested their pain sensitivity 1 h later, as well as their exploratory behavior and paternal responsiveness in an open field 4 h post-treatment. We measured plasma corticosterone immediately after the open-field test. We found that placenta-treated males, independent of reproductive condition, traveled significantly longer distances in the open field than males treated with oil, indicative of lower anxiety. Additionally, fathers had shorter latencies to approach and to care for pups (i.e., huddling and licking pups), and spent more time engaging in these behaviors, than did age-matched expectant fathers and virgin males, independent of treatment. We found no effect on plasma corticosterone levels or pain sensitivity as a result of either treatment or reproductive condition. These findings indicate that placenta ingestion decreases anxiety-related behaviors in male California mice, but might not influence pain sensitivity, paternal responsiveness, or plasma corticosterone concentrations.

Consequences of placentophagia by adult virgin male California mice (Peromyscus californicus)

“…Placenta administration did, however, transiently reduce males' latencies to approach an unfamiliar pup or a novel object, and reduced Fosimmunoreactivity in the dorsal region of the bed nucleus of the stria terminalis after exposure to each of these stimuli. Thus, our results are consistent with findings from a previous study (Perea-Rodriguez et al, 2018) suggesting that ingestion of placenta may reduce neophobia and anxietyrelated behavior in males, but not paternal behavior per se. or 24 after treatment with oil or placenta.…”

“…First, we evaluated effects of placentophagia only in virgin males, rather than in fathers, because fathers typically show maximum paternal care. In our recent study, however, behavioral effects of oral treatment with placenta did not differ among California mouse fathers, first-time expectant fathers, and virgin males (Perea-Rodriguez et al, 2018). Second, although Fos expression has been linked to changes in neuronal activity, this is not always the case; Fos may or may not be expressed when neurons undergo changes in electrical activity or gene expression (Hoffman & Lyo, 2002).…”

“…In the case of males, a study on rats, which are uniparental, showed that virgin males experience hypoalgesia after ingesting placenta (Abbott et al, 1991). Recently, we showed that oral administration of placenta to male California mice, irrespective of reproductive experience, increased exploration of a novel space (an openfield arena) but had no effect on paternal behaviors (Perea-Rodriguez et al, 2018). Similarly, in the present study, placentophagia did not enhance pup-directed care, but it decreased latencies to approach novel stimuli (pups and marbles) and led to changes in neural activity in a brain nucleus heavily involved in regulating responses to a variety of environmental stimuli, including pup-related and other social stimuli.…”

“…7 2c. Placenta Collection As previously described (Perea-Rodriguez & Saltzman, 2014;Perea-Rodriguez et al, 2018), placentas were collected from multiparous (2-7 previous litters) females 1-3 days prior to their estimated parturition date, determined by the date of their previous parturition and assessment of changes in female body mass based on measurements taken every 3-4 days.…”

Consumption of Maternal Placenta in Humans and Nonhuman Mammals: Beneficial and Adverse Effects

“…Placentophagia has been thoroughly studied, primarily in mice (Peromyscus californicus) [9], hamsters (Phodopus campbelli) [10], rats (Mus musculus) [11], rabbits (Oryctolagus cuniculus) [12,13], ungulates [14,15], and carnivores [16], and regularly occurs in all nonhuman primate species [17][18][19]. In contrast, it is assumed that traditionally, women did not carry out this practice for socio-cultural reasons.…”