With increasing resolution, the OPCR values of bamboo specialists show progressively higher values compared to the non-bamboo feeders ( Figure S1 C and Table S1 ). Both upper and lower dentitions of P. simus and A. melanoleuca show high fine-grained complexity, whereas the relatively low OPCR values of A. fulgens lower dentition are likely to reflect the highly selective foraging of different bamboo parts by red pandas ( Figure S1 C) []. The average cheek tooth complexities of A. melanoleuca (108.8) and P. simus (84.0) are comparable to the values reported previously for the horse (109.5) and the early equid Eohippus (88.6), respectively (calculated for upper teeth at 50-row resolution) []. Moreover, similar to equids, but exceptional for primates, P. simus has a high degree of molarization of the premolars []. All of these dental features indicate that P. simus has a dentition that is at least as diagnostic of bamboo feeding as that of A. melanoleuca. Because advancing wear removes surface features from low-crowned teeth, bamboo-feeding taxa should be especially sensitive to, and informative about, changes in precipitation patterns.

Here we focus on P. simus ( Figure 1 A) because of abundant paleontological and neontological evidence. First, we evaluated whether feeding on woody bamboos, which are grasses belonging to the subfamily Bambusoideae, can be diagnosed from the P. simus dentition. Mammalian dentitions are especially informative about the diet of extinct and taxonomically distant taxa. Relevant to a bamboo diet, feeding on fibrous vegetation in seasonally variable environments is linked in recent and past mammal communities to high-crowned molars [], and grass specialists also tend to have complex molar surfaces []. For example, horses, which are specialized grazers, have high-crowned molars with high fine-scale dental complexity resulting from complex folding of enamel bands []. Although bamboo specialists lack high-crowned molars, they appear to have high dental complexity [] ( Figure 1 B). To measure fine-scale complexity using orientation patch count rotated (OPCR; see STAR Methods and Figure 1 B; Figures S1 A and S1B), here we contrasted the complexity of the bamboo specialists P. simus, A. melanoleuca, and A. fulgens with the dental complexity of the brown bear (Ursus arctos), the raccoon (Procyon lotor), and the black lemur (Eulemur macacao). These latter taxa, which represent the phylogenetic contrasts to the bamboo specialists, have generalized diets ( STAR Methods and Figure 1 B).

(B) Orientation patch count (OPC) maps of the dentitions of bamboo specialists show high surface complexity compared to species with generalized diets (tooth rows scaled to 150-row resolution). Anterior is toward left, and buccal is toward the top.

A characteristic of bamboo-feeding mammals is that most, if not all, of them are considered threatened by extinction []. In Asia, both giant (Ailuropoda melanoleuca) and red (Ailurus fulgens) pandas have much diminished geographical ranges when compared with their historical and paleontological records []. Similarly, in Madagascar, the two larger bamboo lemurs, the greater bamboo lemur (Prolemur simus) and the golden bamboo lemur (Hapalemur aureus), have highly restricted distributions within the island and are listed as critically endangered []. Both the endangerment and the dietary specializations of bamboo-feeding taxa suggest that they may be especially sensitive to changes in climate.

The results show that culm feeding is restricted to the months of August to November ( Figure 2 A and Table S2 ). Shoot feeding begins abruptly with the full onset of the rainy season, and shoots are the primary diet when rainfall exceeds 250 mm/month ( Figure 2 B). The distinct pattern of feeding either on shoots or culm ( Figure 2 ) was reported for the same locality 10 years previously [], suggesting robust feeding patterns. Feeding on shoots continues in the austral winter when an increasing amount of time is spent feeding on leaves ( Figures 2 A and 2B).

(B) Monthly rainfall, monitored in proximity to the P. simus study group during 2006 to 2008 shows that shoot feeding occurs during the rainy season and leaf and culm feeding during the dry season. Numbers in parentheses denote the number of months. Boxes enclose 50% of observations; the median and mean are indicated with a horizontal bar and circle, respectively, and whiskers denote range.

(A) A monitored P. simus group in RNP shows highly monotonous feeding on bamboo, with the diet consisting almost solely of bamboo shoots in December to April. Culm feeding is restricted to August to November, and bamboo leaves are eaten between peak shoot and culm feeding. Data are from 2006 to 2008. 2007 was a cyclone year that may have prolonged the availability of shoots beyond March. The mean number of monthly observation days is 10.3 (ranging from 3 to 20), with observed mean daily feeding of 64.5 min (ranging from 40 to 115). Error bars indicate the SEM.

An 18-month focal-animal follow of a P. simus group was carried out during 2006–2008 in Ranomafana National Park (RNP), Madagascar, a location in which P. simus was first found in 1987 and the first site at which P. simus was habituated []. From 2,387 feeding observations, we tabulated the proportion of feeding time spent on eating bamboo culms, leaves, and shoots (see STAR Methods ). In RNP, 95% of feeding time was spent on a single species of woody bamboo (Cathariostachys madagascariensis), and individual members of P. simus groups typically had synchronous activities. One exception is that juvenile P. simus cannot break the bamboo culm and rely on adults in obtaining the softer inner parts of the culm [].

Next, we used data on living P. simus feeding behavior to link the details of bamboo feeding to precipitation. The durations of rainy and dry seasons have been proposed to have especially strong effects on P. simus communities [], and although they feed on most parts of bamboo, the preferred parts are new ground shoots ( Figure 1 A). The availability of shoots, however, is seasonally restricted to the rainy season [], and feeding on mechanically demanding [] and nutritionally poor culm can be considered a regular fallback food for P. simus. This preference for shoots, which are the nutritionally high-quality parts of bamboo, appears to be shared by all bamboo specialists []. Furthermore, the birth and weaning seasons of P. simus are during peak bamboo shoot availability [].

Linking Past and Present P. simus Distributions

Because the dental morphology ( Figure 1 ) of P. simus appears ecologically highly diagnostic and because RNP has distinct seasonal and precipitation patterns of bamboo feeding ( Figure 2 ), we next estimated the durations of wet-season and dry-season feeding for the whole of Madagascar. This allows us to integrate data on precipitation in present-day localities with the paleontological localities of P. simus, which are scattered throughout Madagascar (except for the southwest) and which are relatively rich in dental material ( Table S3 ).

21 King T.

Randrianarimanana H.L.L.

Rakotonirina L.H.F.

Mihaminekena T.H.

Andrianandrasana Z.A.

Ratolojanahary M.

Randriahaingo H.N.T.

Ratolojanahary T.

Rafalimandimby J.

Bonaventure A.

et al. Large-culmed bamboos in Madagascar: distribution and field identification of the primary food sources of the critically endangered greater bamboo lemur Prolemur simus. 22 Rakotoarinivo M.

Blach-Overgaard A.

Baker W.J.

Dransfield J.

Moat J.

Svenning J.-C. Palaeo-precipitation is a major determinant of palm species richness patterns across Madagascar: a tropical biodiversity hotspot. 4 Godfrey L.R.

Simons E.L.

Jungers W.L.

DeBlieux D.D.

Chatrath P.S. New discovery of subfossil Hapalemur simus, the greater bamboo lemur, in western Madagascar. The island-wide maps show the projected wet-season and dry-season feeding durations in months ( Figure 3 B), revealing that grid cells containing only paleontological P. simus finds are consistently in regions where dry-season feeding would be required for at least five consecutive months in the present-day climate ( Figures 3 B and 3C; randomization tests between fossil and recent means are p = 0.0025 for <50 mm threshold and p = 0.0174 for <80 mm threshold). In contrast, there is no marked difference in the number of potential wet-season months between the sites ( Figures 3 B and 3C; randomization test between fossil and recent means is p = 0.2394). These patterns indicate that if P. simus were still living in the areas of P. simus paleontological localities, they would have to persist either on bamboo leaves and culm for the extended dry season or on alternative diets. Woody bamboos have been reported to have present-day distribution in the regions that contain at least some of the P. simus paleontological localities []. Furthermore, relatively high present-day palm species richness in northeastern Madagascar has been reconstructed to be a relict pattern influenced by high precipitation in that region during the Last Glacial Maximum (LGM) []. Our combined analyses ( Figures 2 3 , and S3 ) support wetter conditions for the northern half of Madagascar in the past, and some P. simus populations may have persisted even beyond the LGM in the north [].