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The greater bamboo lemur is Madagascar’s ecological equivalent of the giant panda
Dental remains diagnostic of a bamboo diet are found across Madagascar
Mechanically demanding bamboo trunk is consumed only during the dry season
Longer dry seasons caused by climate change will cause further range contraction
Animals with dietary specializations can be used to link climate to specific ecological drivers of endangerment. Only two mammals, the giant panda (Ailuropoda melanoleuca) in Asia and the greater bamboo lemur (Prolemur simus) in Madagascar, consume the nutritionally poor and mechanically challenging culm or trunk of woody bamboos [
]. Here, integrating morphological, paleontological, and ecological evidence, we project the effects of climate change on greater bamboo lemurs. Both the giant panda and the greater bamboo lemur are shown to share diagnostic dental features indicative of a bamboo diet, thereby providing an ecometric indicator [
] of diet preserved in the fossil record. Analyses of bamboo feeding in living populations show that bamboo culm is consumed only during the dry season and that the greater bamboo lemur is currently found in regions with the shortest dry season. In contrast, paleontological localities of the greater bamboo lemurs have the longest dry seasons. Future projections show that many present-day greater bamboo lemur populations will experience prolonged dry seasons similar to those of the localities where only fossils of the greater bamboo lemur are found. Whereas abundant foods such as bamboo allow feeding specialists to thrive, even a moderate change in seasonality may outstrip the capacity of greater bamboo lemurs to persist on their mechanically demanding food source. Coupling known changes in species distribution with high-resolution ecological and historical data helps to identify extinction risks.
]. 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.
Here we focus on P. simus (Figure 1A) 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 [
] (Figure 1B). To measure fine-scale complexity using orientation patch count rotated (OPCR; see STAR Methods and Figure 1B; Figures S1A 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 1B).
With increasing resolution, the OPCR values of bamboo specialists show progressively higher values compared to the non-bamboo feeders (Figure S1C 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 S1C) [
]. 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) [
]. 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.
Linking Precipitation to Patterns of Bamboo Feeding
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 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 [
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 [
The results show that culm feeding is restricted to the months of August to November (Figure 2A 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 2B). 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 2A and 2B).
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).
] in 10-min degree grid cell resolution (approximately 18 × 18 km at the equator, mean precipitation from 1950 to 2000), we first determined both the wet-season and dry-season precipitation thresholds for the grid cell containing RNP. The wet-season feeding threshold was set at >250 mm monthly precipitation, encompassing the months of December to March. We consider this a reasonable threshold because it covers the four peak months of feeding on shoots in our feeding data at RNP (Figures 2A and 3A ). For dry-season feeding, we used two grid cell thresholds. To account for the strict culm-feeding season, we used a <50 mm monthly precipitation threshold that encompasses the months August to October, only excluding November when the transition from culm to shoot feeding happens as the rainy season begins (Figures 2A and 3A). To cover the whole dry-season feeding period, which includes bamboo culm and a mixture of leaves and shoots (Figure 2A), we used a <80 mm monthly precipitation threshold, encompassing the months of May to October (Figure 3A). Similarly, the precipitation reanalysis data (ERA-Interim) from the RNP region spanning 2005 to 2015 show that the months December to March and May to October are the periods of the highest and the lowest precipitation, respectively (see STAR Methods and Figure S2).
The island-wide maps show the projected wet-season and dry-season feeding durations in months (Figure 3B), 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 3B 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 3B 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 [
]. Our data suggest that rapidly changing climate may also endanger bamboo feeders in a subtle way by affecting seasonal availability of preferred bamboo parts, and the giant panda may be similarly vulnerable [
]. Southwestern Madagascar is devoid of P. simus fossil localities, and it also has the longest and the shortest projected durations of dry-season and wet-season feeding, respectively (Figure 3B). We note that the present P. simus localities with exceptionally long projected dry-season feeding even at the threshold <50 mm are the westernmost sites at the edge of the high plateau (for example, Andringitra; Figure S4A). These exceptionally long dry-season feeding estimates are likely to be artifacts of grid cells spanning beyond the relatively small patches of forest, but they may also signify the precarious nature of these sites (a close up of the localities is shown in Figure S4A).
Future Changes in Bamboo-Feeding Seasons
To examine the potential effect of climate change on P. simus, we used representative concentration pathway (RCP; see STAR Methods and [
]) scenarios for the future. The climate model data were downscaled to the same resolution as the present-day data and were bias-corrected using the present-day as a baseline (see http://worldclim.org/downscaling for details). We calculated a model ensemble mean value, using all available climate model data for each RCP to obtain a more robust estimate of the future conditions than using individual climate model runs.
For the grid cells in which P. simus is currently present, our future projections predict a relatively small drop in the duration of wet-season feeding by 2070, with the median duration shortening from 4 to 3 months (Figures 4B and 4C ; randomization test between recent and 2070 sites is p = 0.1942). However, the <50 mm threshold dry seasons in particular are predicted to be prolonged for many of the present-day P. simus sites (Figure 4A, 4B, and S4; randomization tests between recent and 2070 means are p = 0.0261 for <50 mm threshold and p = 0.1438 for <80 mm threshold). This projection is not restricted to the high-greenhouse-gas-concentration scenario (RCP 8.5), as all of the RCPs show that the dry-season durations become longer (Table S4 and Figure S3). These analyses indicate that regions in which P. simus is currently found are projected to experience precipitation patterns more comparable to those in the regions in which P. simus has gone extinct.
Overall, the projected lengthening of the dry-season feeding period would cause prolonged usage of bamboo culm and other mechanically demanding and drier plants, which in addition to nutritional challenges can be predicted to increase the rate of tooth wear, leading to loss in dental function and premature dental senescence [
]. In comparison to human-induced habitat loss directly driving populations to extinction, climate change drives prolongation of the dry season. Hence, P. simus populations in both protected and unprotected areas would be affected, suggesting that protecting the existing habitats might not be enough to guarantee the continued existence at the face of ongoing climate change (see also [
]). An additional factor in Madagascar is the frequent occurrence of tropical cyclones that can defoliate large swathes of forest. Whereas cyclone damage may benefit fast-growing bamboo, and thus open new areas for P. simus to persist, the toughness of plants during the dry season would still remain a challenge. Increasing dryness of bamboo would most likely threaten all bamboo specialists, despite their physiological adaptations to have low daily energy expenditure and to cope with chemical defenses of bamboo [
In general, linking morphology, resource use, and precipitation data with distribution data allows new ways to make specific predictions about the response of biodiversity to future climate change and also to interpret paleontological data [
]. Our analyses suggest that the combination of low-crowned teeth with high dental complexity indicates mechanically demanding diets but with limited duration and severity of dry seasons (Figure 3). Taxa with complex but low-crowned teeth are known from the fossil record [
], this study indicates that climate change has become an additional threat to the lemurs and has most likely contributed to the critical endangerment of P. simus. Considering bamboo lemurs and other bamboo specialists, the price of their specialization to an abundant but demanding food source appears to be their undoing in a changing climate.
Further information and requests for resources should be directed to and will be fulfilled by the Lead Contact, Jukka Jernvall ([email protected]).
Experimental Model and Subject Details
Dental specimens studied were BMNH 22.214.171.124 (Prolemur), USNM 259400 (Ailuropoda), MZH 1.537 (Ailurus), MZH U86 (Eulemur), SMNH A585456 (Ursus), MZH 885/1960 (Procyon). BMNH, Natural History Museum London, UK; MZH, Finnish Museum of Natural History, Finland; SMNH, Swedish Museum of Natural History, Sweden; USNM, National Museum of Natural History, Smithsonian Institution, USA. Unworn dentitions were digitized using a Nextec Hawk 3-D laser scanner [
P. simus observations were recorded from a wild population that had been habituated to human presence in the southeastern rainforest of Madagascar at Ranomafana National Park (RNP) (47° 18’ - 47° 37’ E and 21° 02’ - 21° 25’ S) [
]. During the study period this population comprised three females and two to three males, together with one lemur that was born during the study. Adult lemurs were marked with collars to facilitate the identification of individuals from a distance. All international, national and institutional guidelines for the care and use of animals were followed.
We used the orientation patch count rotated method (OPCR, a geographic information systems-derived method to analyze tooth topography) to measure surface complexity of teeth [
]. We measured the complexity of cheek tooth rows dedicated for mastication of foods using dental specimens listed above. Because of the variable number of cheek teeth present in different taxa, the teeth measured were p4-m3 (upper) and m1-m3 (lower) for P. simus and E. macacao, p4-m2 (upper) and m1-m3 (lower) for A. melanoleuca and U. arctos, and p4-m2 (upper) and m1-m2 (lower) for A. fulgens and P. lotor (Figure S1). The evolutionary comparative species were chosen based on them having broad, generalized diets [
], and our results on OPCR should be considered minimum estimates for the P. simus. The digitized tooth rows were then resampled to 50, 75, 100, 150, 200, 250, and 300 anterior-posterior data rows to measure the effect of surface resolution (Figure S1 and Table S1). This resampling scheme brackets a previous analysis, showing that P. simus has the highest OPCR among lemurs, using a 50 row resolution to measure individual lower second molars (roughly equalling 150 rows for a tooth row) [
Feeding behavior observations were recorded from a population of P. simus living in RNP for 18 contiguous months, from 2006-2008 by trained technicians employed by the Centre ValBio research station. Behavioral data were collected at 5-minute intervals and mean daily feeding for each month was tabulated (Table S2). Although data were collected from randomly selected focal individuals, all the members of the group tend to share the same activity, especially during feeding (this study).
We compiled the present-day occurrence data for P. simus (Table S3). In addition to the present occurrences, we also included historic occurrences (where a population had been seen in the last 50 years), and known subfossil sites (Table S3).
Climate and precipitation analysis
For RNP precipitation conditions, we used the Centre ValBio weather station data between 2006-2008. We combined the daily precipitation data with the feeding data at a monthly resolution for the 2006-2008 period, for which we have the feeding observation data.
To determine climatically the wet-season and dry-season precipitation thresholds for the grid cell containing RNP we downloaded the present-day climate (1950-2000) from worldclim.org [
] in 10-minute degree cell resolution (roughly 18 × 18 km at the equator), and located the closest grid cell for each of the P. simus localities in our dataset. To estimate future conditions, we downloaded the future Representative Concentration Pathways (RCPs) scenarios from the worldclim.org site (RCP8.5, RCP6, RCP4.5 and RCP2.6 projections depending on how much greenhouse gases are emitted in the years to come [
]). The RCP scenarios are downscaled and bias-corrected by worldclim.org so that they can be compared to present conditions (Table S4). For visual mapping we plotted the dry- and wet-season duration in months using worldclim.org grid cells for the whole of Madagascar. We also used the Paleoclimate data from WorldClim to characterize the last glacial maximum (LGM, approximately 22,000 years ago). The data come originally from CMIP5, but are downscaled and biascorrected by WorldClim.
To examine how representative the precipitation data from RNP are, we also used ERA-interim climate reanalysis data [
]. We downloaded the ERA-interim data from European Centre for Medium-Range Weather Forecasts at 1-degree grid cell resolution (roughly 111 km at the equator) for the time interval 2005-2015. We pre-processed the data to daily sum of precipitation, and located the closest grid cell for RNP. We created a time-series for RNP site using both the Centre ValBio and ERA-interim precipitation datasets for 2005-2015 (Figure S2).
Quantification and Statistical Analysis
Surfer Manipulator was used to calculate dental complexity values [
]. Eight equal orientation directions of 45° were used and patches smaller than 3 pixels were excluded from the OPC count. The calculation of OPC was repeated eight times by rotating the center of the first orientation direction from 0° at increments of 5.625° to account for variation in rotation in the x and y planes to give OPCR [
]. For comparisons between localities, all p values were obtained after the locality identity assignments were randomized 10,000 times (with and without combining nearby localities).
J.T.E., S.Z., P.C.W., and J.J. designed the project; A.R.E., J.J., and S.Z. contributed to the dental data and analyses; S.R.T, S.Z, P.C.W., and J.J. contributed to the field data and analyses; J.T.E contributed to the climate data and analyses; and J.T.E, S.Z., and J.J. took the lead in writing the paper with contributions from all co-authors.
We would like to especially thank B. Rabaoarivola, R. Rafaliarison Rabetokotany, J. Rakotonjatovo, A. Feistner, J. Carag, and T. Sefczek for their contributions to the RNP dataset and G. Wilson and I. Corfe with help on the dental data. We thank Jan Schnitzler and Hui Tang for help with the climate and time-series data processing and two anonymous reviewers for their suggestions that improved the manuscript. For logistical support, we thank Madagascar National Parks, Madagascar Institute pour la Conservation des Ecosystemes Tropicaux, and the staff of the Centre ValBio Research Station. Field research was authorized by Madagascar Ministry of Environment. This study was supported by the Academy of Finland (J.J.), Stony Brook University (P.C.W., S.R.T.), Marie Curie Actions of the European Union (J.J., S.Z.), and Kone Foundation (J.T.E.). This article is a contribution to the Integrative Climate Change Biology (iCCB) program.