Saliva of the graminivorous Theropithecus gelada lacks proline‐rich proteins and tannin‐binding capacity

Abstract

Gelada baboons are the sole survivors of the genus Theropithecus and the only known graminivorous primates. They developed special adaptations to their diet such as high-crowned teeth for processing hard and abrasive feed. The fine-tuning of salivary protein composition might be another key mechanism that is used by species for adapting to the environment and competing with rivals for exploiting new ecological niches. In order to test whether gelada (graminivorous) and hamadryas baboons (omnivorous) differ in their salivary protein composition, we compared whole saliva samples of captive Theropithecus gelada and Papio hamadryas using gel electrophoresis and tannin-binding assay. We hypothesized that the amount of proline-rich salivary proteins with tannin-binding capacity is higher in baboons consuming a feed with high dicot/monocot rations. Dicots produce tannins as a chemical defense system, discouraging animals from eating them. In contrast to dicots, monocots do not synthesize tannins. The presence of tannin-binding proteins in saliva should effectively inactivate the dicot tannin-based defense mechanism and increase the dietary breadth and/or the capability to switch between monocots and dicot leaves. The lack of such tannin-binding proteins in saliva would indicate a narrow dietary spectrum more restricted to monocots. We found T. gelada to completely lack proline-rich proteins (PRPs) and tannin-binding capacity similar to a great variety of other grazing mammals. In contrast, P. hamadryas does possess PRPs with tannin-binding activity. The findings support a growing body of evidence suggesting a high-level specialization of T. gelada to grass diets. However, it remains unclear, whether loss of salivary tannin-binding capacity drove the gelada into its narrow feeding niche, or whether this loss is the result of a long process of increased specialization. Thus, from an ecological point of view, T. gelada appears to be more vulnerable to environmental changes than other baboon species owing to its narrow dietary traits.

First identification of tannin‐binding proteins in saliva of Papio hamadryas using MS/MS mass spectrometry

“…However, although the exact tannin content of the diet is unknown, it is likely that hamadryas baboons, especially in the wild, consume considerable amounts of tannic acid with fruits and leaves. Therefore, it may be inferred that hamadryas baboons possess a significant ability to bind and precipitate tannic acid with the help of tannin‐binding proteins, as previously demonstrated [Mau et al, 2009]. In fact, in recent tannin‐binding assays using the saliva of captive P. hamadryas , we detected for the first time a number of yet unidentified proteins together with the characteristic pink staining of a PRP with a molecular mass of approximately 23 kDa [Mau et al, 2009].…”

“…Therefore, it may be inferred that hamadryas baboons possess a significant ability to bind and precipitate tannic acid with the help of tannin‐binding proteins, as previously demonstrated [Mau et al, 2009]. In fact, in recent tannin‐binding assays using the saliva of captive P. hamadryas , we detected for the first time a number of yet unidentified proteins together with the characteristic pink staining of a PRP with a molecular mass of approximately 23 kDa [Mau et al, 2009]. This specific staining method uses Coomassie Brilliant Blue R250 to stain PRP [Beeley et al, 1991].…”

Abrasive, Silica Phytoliths and the Evolution of Thick Molar Enamel in Primates, with Implications for the Diet of Paranthropus boisei

“…It has “intermediate/thick” enamel on the occlusal surface of its molars, as classified by the enamel thickness scoring system of Martin [2], [102], with a 2-D RET value of 15.51, slightly higher than that of Pongo pygmaeus at 15.33 [13]. In addition, T. gelada has tall-crowned teeth [103], [104]. Hypsodont or tall-crowned teeth are an adaptation found in grazing herbivores, in which greater enamel volume is added by raising the height of the crown.…”

Physical Properties of Fruit and Seeds Ingested by Primate Seed Predators with Emphasis on Sakis and Bearded Sakis

“…Less is known about chemical feeding deterrents beyond the apparent ubiquity of secondary compounds in wild foods (but see Milton,1979; Rosenthal and Berenbaum,1992; Lambert,1998). Tannins, phenolics, alkaloids, and many other compounds affect the digestibility of plant products (e.g., trypsin inhibitors in legume seeds, Altmann,2009) and while there is some information on proteins in human and nonhuman primate saliva that bind with secondary compounds and reverse their effects (Milton,1999; Mau et al,2009), there are few studies of wild primates that have studied this topic (e.g., cyanide tolerance by Hapalemur : Glander et al,1989). Altmann (2009) refers to the mixed nutrient/digestion inhibitor or toxic constituents of primate foods as the “package problem.”…”