Mechanical food properties and dental topography differentiate three populations of Lemur catta in southwest Madagascar.

Determining the proximate causes of tooth wear remains a major focus of dental study. Here we compare the diets of three ring-tailed lemur (Lemur catta) populations and examine how different dietary components may contribute to patterns of wear-related tooth shape. Casts were made from dental impressions collected between 2003 and 2010 from lemurs in the gallery and spiny/mixed forests of the Bezá Mahafaly Special Reserve (BMSR; Parcels 1 and 2) and the spiny/mixed forests of Tsimanampesotse National Park (TNP), Madagascar. Tooth shape variables (occlusal relief and slope, angularity) were analyzed using dental topographic analysis. Focal observations and food mechanical properties (FMPs: toughness, hardness, elastic modulus) were conducted and tested, respectively, during wet and dry seasons from 2008 to 2012. We found that FMPs correlate with patterns of dental topography in these three populations. Specifically, food toughness and elastic modulus correlate with the dental variables, but hardness does not. Average food toughness and elastic modulus, but not hardness, are highest in BMSR Parcel 2, followed by BMSR Parcel 1 and TNP. Occlusal relief and slope, which serve as proxies for tooth wear, show the greatest wear in Parcel 2 and the least in TNP. Angularity is also more pronounced in TNP. Further, dental topographic patterns correspond to reliance on Tamarindus indica (tamarind) fruit. Both BMSR populations consume tamarind at high frequencies in the dry season, but the fruits are rare at TNP and only occasionally consumed. Thus, high seasonal tamarind consumption and its mechanical values help explain the low dental relief and slope among BMSR lemurs. By investigating the ecology of a single widespread species across a variety of habitats, we have been able to link specific components of diet to patterns of dental topography in this species. This provides a context for interpreting wear-related tooth shape changes more generally, illustrating that populations can develop different dental wear patterns resulting from a mix of intrinsic factors (thin enamel) and local conditions (food properties, frequency of consumption).

Primate dietary ecology in the context of food mechanical properties.

Substantial variation exists in the mechanical properties of foods consumed by primate species. This variation is known to influence food selection and ingestion among non-human primates, yet no large-scale comparative study has examined the relationships between food mechanical properties and feeding strategies. Here, we present comparative data on the Young's modulus and fracture toughness of natural foods in the diets of 31 primate species. We use these data to examine the relationships between food mechanical properties and dietary quality, body mass, and feeding time. We also examine the relationship between food mechanical properties and categorical concepts of diet that are often used to infer food mechanical properties. We found that traditional dietary categories, such as folivory and frugivory, did not faithfully track food mechanical properties. Additionally, our estimate of dietary quality was not significantly correlated with either toughness or Young's modulus. We found a complex relationship among food mechanical properties, body mass, and feeding time, with a potential interaction between median toughness and body mass. The relationship between mean toughness and feeding time is straightforward: feeding time increases as toughness increases. However, when considering median toughness, the relationship with feeding time may depend upon body mass, such that smaller primates increase their feeding time in response to an increase in median dietary toughness, whereas larger primates may feed for shorter periods of time as toughness increases. Our results emphasize the need for additional studies quantifying the mechanical and chemical properties of primate diets so that they may be meaningfully compared to research on feeding behavior and jaw morphology.

Beyond the Gallery Forest: Contrasting Habitat and Diet in Lemur catta Troops at Bezà Mahafaly Special Reserve.

Ring-tailed lemurs have been studied intensively in the Parcel 1 gallery forest of Bezà Mahafaly Special Reserve. Here, we report on lemur groups in a mixture of deciduous dry forest and spiny forest just 5 km to the west. Compared to Parcel 1, Parcel 2 (P2) has a lower density of Tamarindus indica, a major dietary plant species for gallery forest lemurs. Recent studies in drier habitats have called into question the association of lemur density and tamarind presence. In order to address this question, we measured forest structure and composition of plant plots between parcels and conducted lemur feeding observations. The trees and shrubs within the parcels did not differ in height or diameter at breast height, but the frequencies of plant species that were common between parcels were significantly different. Numbers of feeding observations on foods common to both parcels did not differ, but their relative rankings within parcels did. Frequencies of food plants corresponded to earlier reports of lemur population densities. However, we found that the ring-tailed lemur diet is a mixture of plants that are eaten in abundance regardless of frequency and those that are locally available. In terms of their reliance on Tamarindus, P2 animals appear intermediate between those in gallery forests and nontamarind sites.

The effects of feeding frequency on jaw loading in two lemur species.

OBJECTIVES: Studies on oral processing are often snapshots of behaviors that examine feeding through individual bouts. In this study, we expand on our previous work comparing bite/chew variables per feeding bout to summed daily biting, chewing, and food intake to interpret loading that could have potential morphological effects. MATERIALS AND METHODS: We observed sympatric Lemur catta and Propithecus verreauxi over two field seasons in the dry forest of Bezà Mahafaly Special Reserve in southwestern Madagascar. Bite and chew rates determined from videos filmed during observations were multiplied with time spent feeding on specific foods during focal follows to calculate daily values for each feeding bout. Food mechanical properties (FMPs) were tested on dietary items with a portable tester. We contrasted daily bite/chew numbers and intake with FMPs, species, season, and food shape. RESULTS: Daily bite and chew numbers increased with maximum, but not average, food toughness. Daily intake decreased with average and maximum toughness. Season had a strong effect on daily bites and chews, but not on intake. Food shape influenced intake and total bite and chew numbers. The lemur species did not differ in our models. DISCUSSION: Maximum food toughness impacted feeding behaviors and intake, which is consistent with higher loads having a greater effect on morphology. In contrast to feeding per bout, cumulative biting and chewing did not differ between species; taking feeding frequency into consideration affects interpretation of jaw loading. Finally, biting, as much as chewing, may generate strains that impact morphology.

Comparing effects of food mechanical properties on oral processing behaviors in two sympatric lemur species.

OBJECTIVES: The link between diet and the masticatory apparatus in primates is complex. We investigated how food mechanical properties (FMPs) and food geometry affect feeding behaviors and subsequent jaw loading. We compared oral processing in two sympatric lemur species with distinct diets and mandibular morphologies. MATERIALS AND METHODS: All-day focal follows of Lemur catta (Lc) and Propithecus verreauxi (Pv) were conducted in both the dry and wet seasons at Beza Mahafaly Special Reserve. We collected activity budget data, filmed feeding bouts, and collected food items to measure their mechanical properties with an FLS-1 portable tester. Feeding videos for the top food items they spent the most time consuming were analyzed frame-by-frame to assess bite and chew numbers and rates. RESULTS: Lc bite more and at a slower rate on tougher (maximum) foods, chew more for tougher (average) foods, and chew less for stiffer leaves. Pv initially increase chew number for tougher (average) foods, but their behavior is less affected as food toughness increases. Pv chew less and more slowly but spend more of the day feeding than Lc. Additionally, they have a tougher (maximum) diet than Lc. DISCUSSION: Lc adjust their feeding behaviors depending on the FMPs of their top food items, while Pv feed more consistently. The more robust masticatory apparatus of Pv may not require them to adjust their feeding behaviors for more mechanically challenging foods. Furthermore, the two species show distinct differences in chewing. Exploring chewing on a daily scale could aid in understanding its impact on the loading of the masticatory apparatus.

Interpreting food processing through dietary mechanical properties: a Lemur catta case study.

Knowledge of dietary mechanical properties can be informative about physical consequences to consumers during ingestion and mastication. In this article, we examine how Tamarindus indica fruits can affect dental morphology in a population of ring-tailed lemurs (Lemur catta) at Beza Mahafaly special reserve in southwestern Madagascar. Ring-tailed lemurs in tamarind dominated gallery forests exhibit extreme wear and tooth loss on their postcanine dentition that has been related to processing T. indica fruits. We measured and compared mechanical properties of individual food parts in the diet of ring-tailed lemurs in different seasons in 1999-2000, 2008, and 2010. Fracture toughness, hardness, and modulus of foods were measured with a portable mechanical tester. The ripe fruits of T. indica are indeed the toughest and hardest foods ingested by the lemurs. In addition, they are among the largest foods consumed, require high numbers of ingestive bites to process, and are the most frequently eaten by volume. During controlled cutting tests of the ripe fruit shell, multiple runaway side cracks form alongside the cut. Similarly, the lemurs repeatedly bite the ripe shell during feeding and thereby introduce multiple cracks that eventually fragment the shell. Studies of enamel microstructure (e.g., Lucas et al.: BioEssays 30 (2008) 374-385; Campbell et al., 2011) advance the idea that the thin enamel of ring-tailed lemur teeth is susceptible to substantial micro-cracking that rapidly erodes the teeth. We conclude that micro-cracking from repeated loads, in combination with the mechanical and physical properties of the fruit, is primarily responsible for the observed dental damage.

Global patterns of leaf mechanical properties.

Leaf mechanical properties strongly influence leaf lifespan, plant-herbivore interactions, litter decomposition and nutrient cycling, but global patterns in their interspecific variation and underlying mechanisms remain poorly understood. We synthesize data across the three major measurement methods, permitting the first global analyses of leaf mechanics and associated traits, for 2819 species from 90 sites worldwide. Key measures of leaf mechanical resistance varied c. 500-800-fold among species. Contrary to a long-standing hypothesis, tropical leaves were not mechanically more resistant than temperate leaves. Leaf mechanical resistance was modestly related to rainfall and local light environment. By partitioning leaf mechanical resistance into three different components we discovered that toughness per density contributed a surprisingly large fraction to variation in mechanical resistance, larger than the fractions contributed by lamina thickness and tissue density. Higher toughness per density was associated with long leaf lifespan especially in forest understory. Seldom appreciated in the past, toughness per density is a key factor in leaf mechanical resistance, which itself influences plant-animal interactions and ecosystem functions across the globe.

Semi-quantitative tests of cyanide in foods and excreta of Three Hapalemur species in Madagascar.

Three sympatric Hapalemur species (H. g. griseus, H. aureus, and H. (Prolemur) simus) in Ranomafana National Park, Madagascar are known to eat bamboo food parts that contain cyanide. How these lemurs avoid cyanide poisoning remains unknown. In this study, we tested for the presence/absence of cyanide in bamboo lemur foods and excreta to (1) document patterns of cyanide consumption among species with respect to diet, (2) identify routes of elimination of cyanide from the gastrointestinal tract, and (3) determine whether cyanide is absorbed from the diet. We tested 102 food, urine, and fecal samples for hydrogen cyanide (HCN) during two "pre-dry" seasons (April 2006, May 2007) using commercially available Cyantesmo test strips. The test strips changed color in the presence of HCN, and we recorded color change on a scale of 0 (no change) to 5 (cobalt) at preset intervals with a final score taken at 24 hr. We detected cyanide in bamboo food parts and urine of all three Hapalemur species. Time to color change of the test strips ranged from almost instantaneous to >12 hr incubation. Of the foods tested, only bamboo contained cyanide, but results differed among bamboo species and plant parts of the same species. Specifically, branch shoot and culm pith of the giant bamboo produced strong, immediate reactions to the test paper, whereas parts of liana bamboos produced either weak or no color change. Cyanide was present in almost all urine samples but rarely in fecal samples. This suggests that dietary cyanide is absorbed in the gastrointestinal tract of the Hapalemur species and excreted, at least in part, by the kidneys. Samples from H. griseus exhibited lower, though still detectable, cyanide levels compared with H. simus and H. aureus. Differences among lemur species appear to be related to the specific bamboo parts consumed.

Food mechanical properties in three sympatric species of Hapalemur in Ranomafana National Park, Madagascar.

We investigated mechanical dietary properties of sympatric bamboo lemurs, Hapalemur g. griseus, H. aureus, and H. (Prolemur) simus, in Ranomafana National Park, Madagascar. Each lemur species relies on bamboo, though previous behavioral observations found that they specialize on different parts of a common resource (Tan: Int J Primatol 20 1999 547-566; Tan: PhD dissertation 2000 State University of New York, Stony Brook). On the basis of these earlier behavioral ecology studies, we hypothesized that specialization on bamboo is related to differences in mechanical properties of specific parts. We quantified mechanical properties of individual plant parts from the diets of the bamboo lemur species using a portable tester. The diets of the Hapalemur spp. exhibited high levels of mechanical heterogeneity. The lemurs, however, could be segregated based on the most challenging (i.e., mechanically demanding) foods. Giant bamboo culm pith was the toughest and stiffest food eaten, and its sole lemur consumer, H. simus, had the most challenging diet. However, the mechanical dietary properties of H. simus and H. aureus overlapped considerably. In the cases where lemur species converged on the same bamboo part, the size of the part eaten increased with body size. Plant parts that were harvested orally but not necessarily masticated were the most demanding, indicating that food preparation may place significant loads on the masticatory apparatus. Finally, we describe how mechanical properties can influence feeding behavior. The elaborate procurement processes of H. simus feeding on culm pith and H. griseus and H. aureus feeding on young leaf bases are related to the toughnesses of protective coverings and the lemurs' exploitation of mechanical vulnerabilities in these plants.

Evolution and function of routine trichromatic vision in primates.

Evolution of the red-green visual subsystem in trichromatic primates has been linked to foraging advantages, namely the detection of either ripe fruits or young leaves amid mature foliage. We tested competing hypotheses globally for eight primate taxa: five with routine trichromatic vision, three without. Routinely trichromatic species ingested leaves that were "red shifted" compared to background foliage more frequently than species lacking this trait. Observed choices were not the reddest possible, suggesting a preference for optimal nutritive gain. There were no similar differences for fruits although red-greenness may sometimes be important in close-range fruit selection. These results suggest that routine trichromacy evolved in a context in which leaf consumption was critical.

Cathemerality in wild ring-tailed lemurs (Lemur catta) in the spiny forest of Tsimanampetsotsa National Park: camera trap data and preliminary behavioral observations.

Cathemerality consists of discrete periods of activity during both the day and night. Though uncommon within Primates, cathemerality is prevalent in some lemur genera, such as Eulemur, Hapalemur, and Prolemur. Several researchers have also reported nighttime activity in Lemur catta, yet these lemurs are generally considered "strictly diurnal". We used behavioral observations and camera traps to examine cathemerality of L. catta at the Tsimanampetsotsa National Park, Madagascar. Nighttime activity occurred throughout the study period (September 2010-April 2011), and correlated with warm overnight temperatures but not daytime temperatures. Animals spent 25% of their daytime active behaviors on the ground, but appeared to avoid the ground at night, with only 5% of their time on the ground. Furthermore, at night, animals spent the majority of their active time feeding (53% nighttime, 43% daytime). These findings imply that both thermoregulation and diet play a role in the adaptive significance of cathemerality. Additionally, predator avoidance may have influenced cathemerality here, in that L. catta may limit nighttime activity as a result of predation threat by forest cats (Felis sp.) or fossa (Cryptoprocta ferox). Further data are needed on cathemeral lemurs generally, but particularly in L. catta if we are to fully understand the evolutionary mechanisms of cathemerality in the Lemuridae.

A comparison of salivary pH in sympatric wild lemurs (Lemur catta and Propithecus verreauxi) at Beza Mahafaly Special Reserve, Madagascar.

Chemical deterioration of teeth is common among modern humans, and has been suggested for some extinct primates. Dental erosion caused by acidic foods may also obscure microwear signals of mechanical food properties. Ring-tailed lemurs at the Beza Mahafaly Special Reserve (BMSR), Madagascar, display frequent severe tooth wear and subsequent tooth loss. In contrast, sympatric Verreaux's sifaka display far less tooth wear and infrequent tooth loss, despite both species regularly consuming acidic tamarind fruit. We investigated the potential impact of dietary acidity on tooth wear, collecting data on salivary pH from both species, as well as salivary pH from ring-tailed lemurs at Tsimanampesotse National Park, Madagascar. We also collected salivary pH data from ring-tailed lemurs at the Indianapolis Zoo, none of which had eaten for at least 12 hr before data collection. Mean salivary pH for the BMSR ring-tailed lemurs (8.098, n=41, SD=0.550) was significantly more alkaline than Verreaux's sifaka (7.481, n=26, SD=0.458). The mean salivary pH of BMSR (8.098) and Tsimanampesotse (8.080, n=25, SD=0.746) ring-tailed lemurs did not differ significantly. Salivary pH for the Indianapolis Zoo sample (8.125, n=16, SD=0.289) did not differ significantly from either the BMSR or Tsimanampesotse ring-tailed lemurs, but was significantly more alkaline than the BMSR Verreaux's sifaka sample. Regardless of the time between feeding and collection of pH data (from several minutes to nearly 1 hr), salivary pH for each wild lemur was above the "critical" pH of 5.5, below which enamel demineralization occurs. Thus, the high pH of lemur saliva suggests a strong buffering capacity, indicating the impact of acidic foods on dental wear is short-lived, likely having a limited effect. However, tannins in tamarind fruit may increase friction between teeth, thereby increasing attrition and wear in lemurs. These data also suggest that salivary pH varies between lemur species, corresponding to broad dietary categories.

Evidence from opsin genes rejects nocturnality in ancestral primates.

It is firmly believed that ancestral primates were nocturnal, with nocturnality having been maintained in most prosimian lineages. Under this traditional view, the opsin genes in all nocturnal prosimians should have undergone similar degrees of functional relaxation and accumulated similar extents of deleterious mutations. This expectation is rejected by the short-wavelength (S) opsin gene sequences from 14 representative prosimians. We found severe defects of the S opsin gene only in lorisiforms, but no defect in five nocturnal and two diurnal lemur species and only minor defects in two tarsiers and two nocturnal lemurs. Further, the nonsynonymous-to-synonymous rate ratio of the S opsin gene is highest in the lorisiforms and varies among the other prosimian branches, indicating different time periods of functional relaxation among lineages. These observations suggest that the ancestral primates were diurnal or cathemeral and that nocturnality has evolved several times in the prosimians, first in the lorisiforms but much later in other lineages. This view is further supported by the distribution pattern of the middle-wavelength (M) and long-wavelength (L) opsin genes among prosimians.

Food procurement and tooth use in two sympatric lemur species.

This study of two lemur species (Lemur catta and Propithecus v. verreauxi) in Madagascar combines observations of food procurement and initial food placement in the mouth with comparisons to food toughness and external properties. Food toughness was hypothesized to play a decisive role in determining food placement during ingestion. It was found that tougher foods are generally ingested on the postcanines for all foods eaten. However, when leaves and fruits are analyzed separately, food size and shape, represented here by mass and food type, are more reliable predictors of initial food placement. Larger leaves and bulkier fruits and stalks are ingested posteriorly. Leaf toughness is not related to leaf size, though the toughness and size of the most commonly eaten fruits are correlated. Furthermore, ingestive food toughness, which is the maximum toughness, and "average" food toughness may make different mechanical demands on the masticatory apparatus that have consequences for jaw morphology.