Optimal foraging on the roof of the world: Himalayan langurs and the classical prey model

Optimal foraging theory has only been sporadically applied to nonhuman primates. The classical prey model, modified for patch choice, predicts a sliding “profitability threshold” for dropping patch types from the diet, preference for profitable foods, dietary niche breadth reduction as encounter rates increase, and that exploitation of a patch type is unrelated to its own abundance. We present results from a 1‐year study testing these predictions with Himalayan langurs (Semnopithecus entellus) at Langtang National Park, Nepal. Behavioral data included continuous recording of feeding bouts and between‐patch travel times. Encounter rates were estimated for 55 food types, which were analyzed for crude protein, lipid, free simple sugar, and fibers. Patch types were entered into the prey model algorithm for eight seasonal time periods and differing age‐sex classes and nutritional currencies. Although the model consistently underestimated diet breadth, the majority of nonpredicted patch types represented rare foods. Profitability was positively related to annual/seasonal dietary contribution by organic matter estimates, whereas time estimates provided weaker relationships. Patch types utilized did not decrease with increasing encounter rates involving profitable foods, although low‐ranking foods available year‐round were taken predominantly when high‐ranking foods were scarce. High‐ranking foods were taken in close relation to encounter rates, while low‐ranking foods were not. The utilization of an energetic currency generally resulted in closest conformation to model predictions, and it performed best when assumptions were most closely approximated. These results suggest that even simple models from foraging theory can provide a useful framework for the study of primate feeding behavior. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Use of local North Carolina browse species to supplement the diet of a captive colony of folivorous primates (Propithecus sp.)

The nutrient content and intake of locally available North Carolina browse was evaluated for use as a supplement to a herbivorous primate diet of commercial biscuit and produce. Twice weekly from May to October 1997, total dietary intakes were determined for two groups of folivorous lemurs. Group I consisted of Propithecus diadema diadema (n = 1) and P. tattersalli (n = 1) and group II consisted of P. verreauxi coquereli (n = 3). Six pooled samples of the diet and weekly samples of three browse species, Rhus copallina, Albizia julibrissin, and Liquidamber styrachiflua were analyzed for dry matter, energy, fiber, and nitrogen content. Browse species were also analyzed for nonprotein nitrogen and acid‐insoluble nitrogen. Group average dry matter intakes were 37.1 ± 2.2% (mean ± SEM) and 49.7 ± 3.0% of amount offered for groups I and II, respectively. Browse contributed 40.7 ± 2.9% and 29.6 ± 2.4% of the total daily intake for groups I and II, respectively. Browse species differed (P < 0.05) for dry matter, energy, neutral detergent fiber, acid detergent fiber, cellulose, lignin, total nitrogen, nonprotein nitrogen, available nitrogen, and available protein. R. copallina and L. styrachiflua were similar in total nitrogen, available nitrogen, and nonprotein nitrogen; A. julibrissin was higher. L. styrachiflua was highest in lignin. Dry matter, acid detergent fiber, and lignin in browse samples increased seasonally (P < 0.05), whereas available protein decreased (P < 0.01). Animals were offered and consumed R. copallina most often, followed by A. julibrisson and L. styrachiflua. With the exception of R. copallina, animals generally consumed only the immature leaves, flowers, or seeds of species offered. Daily dry matter intake varied because of both browse offered and consumed and biscuit and produce diet consumed. Thus, increased fiber density can be a major benefit of browse use only when incorporated into the total diet with respect to species use, quantity of other diet ingredients offered, and targeted nutrient intakes. Zoo Biol 20:447–461, 2001. © 2002 Wiley‐Liss, Inc.     

Cafeteria-style feeding trials provide new insights into the diet and nutritional strategies of the black snub-nosed monkey (Rhinopithecus strykeri): Implications for conservation

Anthropogenic changes and fragmentation of natural habitats often exert a negative effect on resource availability and distribution, and the nutritional ecology and feeding behavior of nonhuman primates. The goals of this study are to examine food choice and to identify the nutritional profile of foods consumed by the Critically Endangered black snub-nosed monkey (Rhinopithecus strykeri). To accomplish our study goals, we presented cafeteria-style feeding trials of fresh food items collected in the home range of wild black snub-nosed monkeys to the only two captive R. strykeri, and compared the nutritional profiles of the leafy foods (buds, young, and mature leaves, 100 items from 70 plant species) selected with those avoided (54 items from 48 plant species). Overall, the results indicate that captive R. strykeri selected foods that were higher in moisture (Mo; 77.7%), crude protein (CP; 21.2%), total nonstructural carbohydrates (TNC; 34.9%), and phosphorus (P; 0.37%) while tending to avoid foods with a neutral detergent fiber (NDF) content of greater than 46.8%. Leaves collected in autumn and selected by the monkeys were characterized by a slightly higher amount of metabolizable energy (ME) than those rejected (1,350 kJ/100 g vs. 1,268 kJ/100 g). In contrast, the protein content of foods collected and consumed during the spring was greater (22.9%) than in autumn (16.4%). Random Forests modeling, an ensemble learning method, indicated that the proportion of Mo, NDF, ME, CP, P, and TNC were among the most important factors in predicting which items were consumed by the captive R. strykeri during spring and autumn. On the basis of the nutritional profile of foods consumed across the two seasons, we identified 18 nutrient-rich native plant species that we recommend for use in ex- and in-situ conservation management and reforestation programs to provide long-term access to a nutritionally adequate diet.     

The challenge of interpreting primate diets: mangabey foraging on Blighia unijugata fruit in relation to changing nutrient content

Primates often make foraging selections that are not apparent. For example, they may eagerly consume a particular plant part and species in some instances, but reject it at other times. Blighia unijugata (Baker) fruit is one of the most frequently eaten foods of mangabeys (Lophocebus albigena) in Lwamunda Forest Reserve, Uganda; however, its use varies strikingly depending on the fruit's developmental stage. We conducted feeding observations to investigate the nutritional criteria that mangabeys may have used for the consumption of specific fruit parts by conducting analysis of fruit parts eaten and rejected at different developmental stages. When seeds had low condensed tannins, mangabeys ate them, but seeds were rejected when tannin levels increased. In the first five stages of fruit development, tannin levels in arils declined and the frequency of consumption of the aril increased. Although fat content in seeds increased with maturity, it did not appear to influence seed consumption, but fat content was related to frequency of consumption of the aril. Considering that primates are often making food selections among many species/part combinations, our results illustrate the value of using nutritional analyses to understand foraging decisions. Furthermore, they demonstrate how very specific trade‐offs between consumption of critical nutrients and antifeedants can drive which foods and parts are eaten.     

Cautious climbing and folivory: a model of hominoid differentation

Despite the large and growing number of Miocene fossil catarrhine taxa, suitable common ancestors of great apes and humans have yet to be agreed upon. Considering a) the conservative and primitive nature of the hominoid molar cusp pattern, and b) the variability of secondary dental features, it is difficult to discern whether a hominoid dentition is primitive, secondarily simplified to the primitive condition or too far derived to be ancestral to any of the living forms. Nonetheless, the inability to recognize a common ancestor is primarly due to the absence of a model of hominoid differentiation that provides a basis for its recognition. Vertical climbing as the limiting component of cautious climbing, explains all of the locomotor anatomy shared by living hominoids. Comparison of the shared derived characters of hominoids to those of forms which have converged on hominoidsi.e colobines, atelines, lorisines, paleopropithecines and sloths suggest that early hominoids were probably folivores. In arboreal forms there is a strong link between a large body size, folivory and cautious climbing. Comparison of craniodental characters of committed folivores to committed frugivores from among each of the compared groups with the exception of lorisines, indicates that many of the distinguishing craniodental characters of humans and great apes are adaptations to folivory. Many of these characters, however, are also present in Jolly's seed eating complex. As such folivory may be the heritage factor which Jolly hypothesized to account for differential reduction of canines in fossilTheropithecus and hominids.     

Diet ofColobus polykomos on Tiwai Island: Selection of food in relation to its seasonal abundance and nutritional quality

A group of Colobus polykomosat Tiwai, Sierra Leone, demonstrated seasonal flexibility in its diet, with seeds, young leaves, and mature leaves each dominating the diet at different times. Comparison of food consumption with phenological data indicates that seeds are eaten whenever available and are preferred to other foods, while young leaves are preferred to mature leaves. Colobus polykomosalso prefer liane to tree leaves, despite the relatively high quality of mature tree foliage at the Tiwai site. Analysis of protein, fiber, and energy values of foods selected and items available, but not eaten, suggests that preference is related to protein and energy maximization. Leguminous plants, especially Papilionaceae and Mimosaceae, are highlighted as important food sources for C. polykomos;seeds and leaves from these families have a high nitrogen content, and the protein content of leguminous seeds often equals or exceeds that found in leaves. It is predicted, therefore, that colobines living in habitats with a high density of legumes will feed heavily on seeds, subject to constraints such as seasonal availability. Where suitable leguminous species are less common, a mixture of fruits, seeds, and young or mature leaves or both is likely to be selected. The results of this and other recent studies of colobines do not support the notion that colobines are specialist folivores.     

Variation in the Nutritional Value of Primate Foods: Among Trees, Time Periods, and Areas

The study of nutritional ecology has proven to be useful for understanding many aspects of primate behavior and ecology and is a valuable tool in primate conservation. However, to date this approach has had limited application since chemical analyses of food items is very time-consuming and collections of perishable food material are often made in remote field locations. Such logistic difficulties have led to plant material being collected in a variety of fashions, and it is not known how variation in collection method might influence our understanding of the chemical basis of dietary selection. A standardization of collection methods is greatly needed to allow for direct comparison among studies. To develop an appropriate standardized method and to evaluate past research, it is necessary to understand along what dimensions plant chemistry varies. We evaluated variation in nutritional value—protein, fiber, digestibility, alkaloids, saponins, cyanogenic glycocides, and minerals—of leaf material from species eaten by red colobus (Piliocolobus tephrosceles) and black-and-white colobus (Colobus guereza) of Kibale National Park, Uganda. We consider variation at 3-levels: among trees, time periods, and areas. While there was considerable variation among species with respect to protein, digestibility, and saponins, there was also variation among individuals of the same species; in fact, individuals may vary by as much as 20%. The average coefficients of variation (CV) among individuals of the same species are 13.4 for protein, 12 for digestibility, and 43 for saponins, while the average CV among species are 35, 31.3, and 82.4, respectively. No species showed a variable response with respect to testing for the presence or absence of cyanogenic glycocides, while 2 of 11 species tested for alkaloids showed a variable response. Over 2 years there was evidence of variation among time periods in the chemical composition of the same food items. The protein-to-fiber ratio of mature leaves of the same species collected from 4 sites separated by 12 km within Kibale was also variable and in some cases the variation among sites was greater than the differences among species. For example, while Funtumia latifolia had little variation in protein-to-fiber ratio at 3 sites (0.44 at all sites), the remaining site was 28% greater. Because temporal variation is less than variation among individuals, it is likely more important to sample from multiple trees at a single point in time than to sample across time. However, the most accurate assessment of nutrient intake is obtained by collecting plant material from the specific trees selected for consumption.     

Towards a synthesis of frameworks in nutritional ecology: interacting effects of protein,carbohydrate and phosphorus on field cricket fitness

Phosphorus has been identified as an important determinant of nutrition-related biological variation. The macronutrients protein (P) and carbohydrates (C), both alone and interactively, are known to affect animal performance. No study, however, has investigated the importance of phosphorus relative to dietary protein or carbohydrates, or the interactive effects of phosphorus with these macronutrients, on fitness-related traits in animals. We used a nutritional geometry framework to address this question in adult field crickets (Gryllus veletis). Our results showed that lifespan, weight gain, acoustic mate signalling and egg production were maximized on diets with different P : C ratios, that phosphorus did not positively affect any of these fitness traits, and that males and females had different optimal macronutrient intake ratios for reproductive performance. When given a choice, crickets selected diets that maximized both lifespan and reproductive performance by preferentially eating diets with low P : C ratios, and females selected diets with a higher P : C ratio than males. Conversely, phosphorus intake was not regulated. Overall, our findings highlight the importance of disentangling the influences of different nutrients, and of quantifying both their individual and interactive effects, on animal fitness traits, so as to gain a more integrative understanding of their nutritional ecology.     

Dietary generalists and nutritional specialists: Feeding strategies of adult female blue monkeys (Cercopithecus mitis) in the Kakamega Forest,Kenya

Generalist primates eat many food types and shift their diet with changes in food availability. Variation in foods eaten may not, however, match variation in nutrient intake. We examined dietary variation in a generalist‐feeder, the blue monkey (Cercopithecus mitis), to see how dietary food intake related to variation in available food and nutrient intake. We used 371 all‐day focal follows from 24 adult females (three groups) in a wild rainforest population to quantify daily diet over 9 months. We measured food availability using vegetation surveys and phenology monitoring. We analyzed >700 food and fecal samples for macronutrient content. Subjects included 445 food items (species‐specific plant parts and insect morphotypes) in their diet. Variation in fruit consumption (percentage of diet and total kcal) tracked variation in availability, suggesting fruit was a preferred food type. Fruits also constituted the majority of the diet (by calories) and some fruit species were eaten more than expected based on relative availability. In contrast, few species of young leaves were eaten more than expected. Also, subjects ate fewer young leaves (based on calories consumed) when fruit or young leaves were more available, suggesting that young leaves served as fallback foods. Despite the broad range of foods in the diet, group differences in fiber digestibility, and variation that reflected food availability, subjects and groups converged on similar nutrient intakes (grand mean ± SD: 637.1 ± 104.7 kcal overall energy intake, 293.3 ± 46.9 kcal nonstructural carbohydrate, 147.8 ± 72.4 kcal lipid, 107.8 ± 12.9 kcal available protein, and 88.1 ± 17.5 kcal structural carbohydrate; N = 24 subjects). Thus, blue monkeys appear to be food composition generalists and nutrient intake specialists, using flexible feeding strategies to regulate nutrient intake. Findings highlight the importance of simultaneously examining dietary composition at both levels of foods and nutrients to understand primate feeding ecology.     

Assessment of nutritional subsidies to freshwater mussels using a multiple natural abundance isotope approach

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Predicting changes in the abundance of African wetland birds by incorporating abundance–occupancy relationships into habitat association models

Aim To map changes in the abundance of African wetland birds using remotely derived habitat data. We show that abundance–occupancy relationships can be coupled with habitat association models to map changes in abundance. As conservation resources are more easily allocated when spatial and temporal patterns of abundance are known, our method provides guidance for conservation planning. Location Papyrus, Cyperus papyrus, swamps in east central Africa. Methods Presence/absence surveys of six bird species in 93 wetlands were used to construct models predicting probability of occurrence from habitat characteristics. Densities were then determined from surveys in 23 additional wetlands and modelled as functions of occurrence probability. We then used satellite imagery to derive habitat characteristics remotely in two time periods (1984–87 and 2000–03) and used the modelled relationships between (1) habitat and occupancy and (2) occupancy and density, to infer changes in abundance in all c. 30,000 wetlands within the study area. Results Wetlands within the region declined by 8.6% between the two time periods, but by > 75% in regions of high human population density. Bird densities were also highest in these regions, which comprised wetlands subject to high levels of disturbance. The geographical coincidence of high densities and habitat loss and the existence of positive associations between bird density and occurrence meant that birds declined by much more than the average rate of their habitat. Main conclusions Targeting conservation efforts in areas with high drainage would protect a high proportion of the bird populations. Encouraging people to derive income from disturbance to which the birds are tolerant, rather than drainage, is likely to be an effective strategy. Because habitat characteristics are a key driver of abundance–occupancy relationships, we conclude that there is wide‐scale scope to couple abundance–occupancy relationships with remote habitat mapping to efficiently inform conservation planning.     

Hierarchy theory reveals multiscale predictors of Arkansas darter (Etheostoma cragini) abundance in a Great Plains riverscape

1. Landscape ecology and its emphasis on relationships between spatial heterogeneity, scale, and ecological processes can be applied to manage stream ecosystems as riverscapes. Hierarchy theory, a central tenet of riverscape ecology, allows for investigating ecological relationships between aquatic organisms and habitat by exploring the nested interactions inherent in reaches, segments, and basins. Arkansas darter Etheostoma cragini is a Great Plains fish endemic to the Arkansas River basin and is listed as in need of conservation in all five states within its range in North America. The aim of this study was to develop empirical models describing relationships between Arkansas darter abundance and local habitats, and identify the appropriate scale(s) for assessing and managing populations.
2. We used Arkansas darter abundance data collected from stream sample units as a fixed grain size (10² m) and compiled datasets at three hierarchical spatial extents, including reach (10³ m), nested within segment (10⁴ m), nested within basin (10⁵ m) in southcentral Kansas. We fit generalised linear mixed models (GLMMs) to assess scale‐specific relationships between Arkansas darter abundance and local habitat dimensions (stream depth and width) and heterogeneity (canopy cover, overhanging vegetation, and woody structure).
3. Habitat parameters included in best‐supported GLMMs differed among extents. Variation in Arkansas darter abundance was explained by canopy cover and channel depth at the reach (54% explained) and segment (56%) extents, and stream width and depth at the basin extent (37%). Partial dependence plots from multiple regression GLMMs revealed that Arkansas darter abundance was negatively correlated with increasing channel depth across all extents, increasing canopy cover at reach and segment extents, and increasing channel width at the basin extent.
4. Our results highlight scale‐specific relationships between Arkansas darter abundance and local habitats across multiple spatial extents. These findings provide direction for assessing stream fish ecology pattern‐process relationships at the appropriate spatial scales and benefit native fish conservation by highlighting the application of hierarchy theory to address management challenges.