Salivary tannin‐binding proteins are a pervasive strategy used by the folivorous/frugivorous black howler monkey

Abstract

Dietary tannins can affect protein digestion and absorption, be toxic, and influence food selection by being astringent and bitter tasting. Animals that usually ingest tannins may regularly secrete tannin-binding salivary proteins (TBSPs) to counteract the negative effects of tannins or TBSPs production can be induced by a tannin-rich diet. In the wild, many primates regularly eat a diet that contains tannin-rich leaves and unripe fruit and it has been speculated that they have the physiological ability to cope with dietary tannins; however, details of their strategy remains unclear. Our research details the salivary protein composition of wild and zoo-living black howler monkeys (Alouatta pigra) feeding on natural versus manufactured low-tannin diets, and examines differences in TBSPs, mainly proline-rich proteins (PRPs), to determine whether production of these proteins is dependent on the tannin content of their food. We measured the pH, flow rate, and concentration of total protein and trichloroacetic acid soluble proteins (an index of PRPs) in saliva. Howler monkeys produced slightly alkaline saliva that may aid in the binding interaction between tannin and salivary proteins. We used gel electrophoresis to describe the salivary protein profile and this analysis along with a tannin-binding assay allowed us to detect several TBSPs in all individuals. We found no differences in the characteristics of saliva between wild and zoo-living monkeys. Our results suggest that black howler monkeys always secrete TBSPs even when fed on foods low in tannins. This strategy of constantly using this salivary anti-tannin defense enables them to obtain nutrients from plants that sometimes contain high levels of tannins and may help immediately to overcome the astringent sensation of their food allowing howler monkeys to eat tanniferous plants.

Peer Review #1 of "Salivary proteome of a Neotropical primate: potential roles in host defense and oral food perception (v0.1)"

“…Corresponding to howler monkeys' ability to feed on tannin-rich diet (Espinosa-Gómez et al, 2015;Espinosa-Gómez et al 2018), we identified several salivary proteins that have been related with the capacity to accept astringent and bitter foods e.g., cystatins (Dsamou et al, 2012;Dinella et al, 2010;Quintana et al, 2009), glyceraldehyde-3-phosphate (Quintana et al, 2009), lactoperoxidase (Morzel et al, 2014), histidine-rich glycoproteins (Dinella et al, 2010), and albumin (Dsamou et al, 2012) (Table 2). PRPs, histatins, statherins, cystatins, and amylase are salivary proteins with considerable affinity for tannins and are involved in astringency and bitter taste (Lamy et al, 2016;Torregrosa et al, 2014)).…”

“…Their ability to eat fibrous (Espinosa-Gómez et al, 2013) tannin-rich leaves and toxic unripe fruits contribute to their adaptability (Garber, Righini & Kowalewski 2015;Milton 1979). Black howler monkeys (Alouatta pigra) can consume plants with high concentration of tannins (Espinosa-Gómez et al, 2018;Righini, Garber & Rothman, 2017) and these monkeys continuously secrete salivary proteins with tannin-binding affinity (Espinosa-…”

Salivary proteome of a Neotropical primate: potential roles in host defense and oral food perception

“…Monkeys were darted and anaesthetized by a veterinarian with ketamine hydrochloride (8 mg/kg estimated body mass, Ketaset, Fort Dodge Animal Health, Iowa USA). Once monkeys were stabilized following sedation, the body weight was determined and the saliva flow was stimulated by an intra-muscular administration of the parasympathomimetic compound pilocarpine-hydrochloride (0.5 mg/ body mass) ( Espinosa-Gómez et al, 2018 ; Da Costa et al., 2008 ). The whole saliva was collected from the mouth of each monkey using a micropipette, placed in a tube, and immediately frozen in liquid nitrogen.…”

“…Their ability to eat fibrous ( Espinosa-Gómez et al, 2013 ) tannin-rich leaves and toxic unripe fruits contribute to their adaptability ( Garber, Righini & Kowalewski, 2015 ; Milton, 1979 ). Black howler monkeys ( Alouatta pigra ) can consume plants with high concentration of tannins ( Espinosa-Gómez et al, 2018 ; Righini, Garber & Rothman, 2017 ) and these monkeys continuously secrete salivary proteins with tannin-binding affinity ( Espinosa-Gómez et al, 2018 ). Their tannin-binding salivary proteins (TBSPs) might be PRPs, but this remains to be confirmed ( Espinosa-Gómez et al, 2018 ).…”

What Is (Not) a Baboon?

“…However, many popular sources now go out of their way to correct the misunderstanding that mandrills are baboons (e.g., http://www.monkeyworlds.com/mandrill/). The application of Bbaboonĉ urrently extends beyond the genus Papio mainly to the genus Theropithecus, as the gelada continues to be called the Bgelada baboon^in scientific publications, including in primatology journals (e.g., Abie et al 2017;Espinosa-Gómez et al 2018;Reyes-Velasco et al 2018;Thompson and Georgiev 2014).…”