Measuring mantled howler monkey (Alouatta palliata) testes via parallel laser photogrammetry: Expanding the use of noninvasive methods.

Parallel laser photogrammetry (PLP), which consists of attaching two or three parallel laser beams at a known inter-beam distance to a camera, can be used to collect morphological measurements of organisms noninvasively. The lasers project onto the photo being taken, and because the inter-beam distance is known, they act as a scale for image analysis programs like ImageJ. Traditionally, this method has been used to measure larger morphological traits (e.g., limb length, crown-rump length) to serve as proxies for overall body size, whereas applications to smaller anatomical features remain limited. To that end, we used PLP to measure the testes of 18 free-living mantled howler monkeys (Alouatta palliata) at La Selva Biological Station, Costa Rica. We tested whether this method could reliably measure this relatively small and globular morphology, and whether it could detect differences among individuals. We tested reliability in three ways: within-photo (coefficient of variation [CV] = 4.7%), between-photo (CV = 5.5%), and interobserver (intraclass correlation = 0.92). We found an average volume of 36.2 cm3 and a range of 16.4-54.4 cm3, indicating variation in testes size between individuals. Furthermore, these sizes are consistent with a previous study that collected measurements by hand, suggesting that PLP is a useful method for making noninvasive measurements of testes.

Chimpanzee (Pan troglodytes schweinfurthii) Population Spans Multiple Protected Areas in the Albertine Rift.

We used mitochondrial DNA to examine gene flow in a region of western Uganda that has received little attention regarding chimpanzee population dynamics. The area is critical to gene flow between isolated Democratic Republic of Congo populations and the rest of East Africa. None of the chimpanzees in each of the 4 protected areas under consideration (Toro-Semliki Wildlife Reserve, Semuliki National Park, Rwenzori Mountains National Park and Itwara Central Forest Reserve) are fully habituated. Therefore, it is not clear whether one or more populations have historically used this fragmented landscape for (1) regular ranging and/or (2) infrequent dispersal. We incorporated the published sequences of the first hypervariable region of the D-loop of the mitochondrial genome from 3 previously sampled sites (n = 39) while also contributing the first extensive genetic sampling of chimpanzees in Toro-Semliki (n = 80). Our goal was to generate a historical baseline model of metapopulation dynamics in this region and determine which, if any, of these protected areas forms a fragmented landscape for a single chimpanzee population. According to a discriminant analysis of principal components, the haplotypes at Toro-Semliki form a central cluster, and Itwara is its nearest genetic neighbor. Rwenzori Mountains National Park is the most distant neighbor of all protected areas. We performed an analysis of molecular variance for 14 different population models that divided the samples from the 4 protected areas into 2, 3 or 4 populations. The best fit model included 3 populations: Toro-Semliki Wildlife Reserve and Itwara Forest Reserve comprised a single population; Semuliki National Park and Rwenzori Mountains National Park formed 2 additional separate populations (variance among = 9%, p = 0.014). The results indicated that some protected areas comprised distinctive populations, while others formed a fragmented landscape for a population's ranging for foraging purposes. Therefore, the edges of a protected area do not always define a chimpanzee population. We propose a closer examination of those dynamics through renewed sampling. Advances in DNA extraction and next-generation sequencing will allow us to compare thousands of single nucleotide polymorphisms in the genomes of unhabituated chimpanzees living in each of these protected areas.

Detecting riparian habitat preferences in "savanna" chimpanzees and associated Fauna with strontium isotope ratios: Implications for reconstructing habitat use by the chimpanzee-human last common ancestor.

OBJECTIVES: Riparian or gallery forests are critical habitats for numerous plants and animals today. Paleoanthropologically, reliance on such habitats informs behavioral and ecological reconstructions; for example, gallery forest habitats likely played a critical role in the transition from ape to hominin in the early Pliocene and may represent a preferred habitat for the last common ancestor of chimpanzees and humans. Direct indicators for gallery forest habitats preference are lacking. The objective of this article is to assess whether strontium isotope ratios are a reliable indicator of habitat preference for fauna living in and around gallery forests. MATERIALS AND METHODS: We report bioavailable strontium isotope ratios from the Mugiri River, its tributaries, and its gallery forest (Toro-Semliki Wildlife Reserve, southwestern Uganda), and compare them to surrounding savanna-grassland values. We compare these environmental values to strontium isotopes ratios in faunal tooth enamel to determine if habitat preferences are accurately reflected. RESULTS: Gallery forest and savanna-grassland vegetations have significantly different strontium isotope ratio profiles. We trace these isotopic differences to the influence of the Mugiri tributaries, which originate on Paleoproterozoic gneiss deposits on top of the surrounding escarpments. These isotopic differences in vegetation are mirrored in the tissues of fauna with habitat preferences for either the gallery forest or the surrounding grasslands. DISCUSSION: This research demonstrates the potential of strontium isotope ratios to identify habitat preferences in modern or fossil fauna under proper geologic variability. It provides a methodological model for future studies seeking to reconstruct habitat preferences in early hominins.

Is genetic drift to blame for testicular dysgenesis syndrome in Semliki chimpanzees (Pan troglodytes schweinfurthii)?

BACKGROUND: We present 3 likely cases of testicular dysgenesis syndrome (TDS) within a community of chimpanzees (Pan troglodytes schweinfurthii). We tested whether genetic drift may be the culprit, as a genetic cause has been suspected to account for TDS among other wildlife. METHODS: We successfully sequenced a 367-bp segment spanning the first hypervariable region within the D-loop of the mitochondrial genome for 78 DNA samples. RESULTS: We found 24 polymorphic sequence sites consisting of 7 singletons and 17 parsimony informative sites. This sample contained 9 haplotypes with a diversity index of 0.78 (SD = 0.03). All tests against the null hypothesis of neutral polymorphisms were non-significant (P > .10). The mismatch distribution of pairwise differences does not fit a Poisson's curve (raggedness index = 0.166; SSD = 0.12; P = 1). CONCLUSIONS: Thus, we found no significant signs of genetic isolation, population expansion, or genetic bottleneck. Alternative causes of TDS and how they might pertain to this population are discussed.

Why are there apes? Evidence for the co-evolution of ape and monkey ecomorphology.

Apes, members of the superfamily Hominoidea, possess a distinctive suite of anatomical and behavioral characters which appear to have evolved relatively late and relatively independently. The timing of paleontological events, extant cercopithecine and hominoid ecomorphology and other evidence suggests that many distinctive ape features evolved to facilitate harvesting ripe fruits among compliant terminal branches in tree edges. Precarious, unpredictably oriented, compliant supports in the canopy periphery require apes to maneuver using suspensory and non-sterotypical postures (i.e. postures with eccentric limb orientations or extreme joint excursions). Diet differences among extant species, extant species numbers and evidence of cercopithecoid diversification and expansion, in concert with a reciprocal decrease in hominoid species, suggest intense competition between monkeys and apes over the last 20 Ma. It may be that larger body masses allow great apes to succeed in contest competitions for highly desired food items, while the ability of monkeys to digest antifeedant-rich unripe fruits allows them to win scramble competitions. Evolutionary trends in morphology and inferred ecology suggest that as monkeys evolved to harvest fruit ever earlier in the fruiting cycle they broadened their niche to encompass first more fibrous, tannin- and toxin-rich unripe fruits and later, for some lineages, mature leaves. Early depletion of unripe fruit in the central core of the tree canopy by monkeys leaves a hollow sphere of ripening fruits, displacing antifeedant-intolerant, later-arriving apes to small-diameter, compliant terminal branches. Hylobatids, orangutans, Pan species, gorillas and the New World atelines may have each evolved suspensory behavior independently in response to local competition from an expanding population of monkeys. Genetic evidence of rapid evolution among chimpanzees suggests that adaptations to suspensory behavior, vertical climbing, knuckle-walking, consumption of terrestrial piths and intercommunity violence had not yet evolved or were still being refined when panins (chimpanzees and bonobos) and hominins diverged.

Selective insectivory at Toro-Semliki, Uganda: comparative analyses suggest no 'savanna' chimpanzee pattern.

Chimpanzee (Pan troglodytes) insectivory across Africa is ubiquitous. Insects provide a significant nutritional payoff and may be important for chimpanzees in dry, open habitats with narrow diets. We tested this hypothesis at Semliki, Uganda, a long-term dry study site. We evaluated prospects for insectivory by measuring insect abundance along de novo transects and trails, monitoring social insect colonies, and surveying available raw materials for elementary technology. We determined the frequency and nature of insectivory through behavioral observation and fecal analysis. We then compared our results with those from 15 other long-term chimpanzee study sites using a cluster analysis. We found that Semliki chimpanzees are one of the most insectivorous populations studied to date in terms of frequency of consumption, but they are very selective in their insectivory, regularly consuming only weaver ants (Oecophylla longinoda) and honey and bees from hives of Apis mellifera. This selectivity obtains despite having a full range of typical prey species available in harvestable quantities. We suggest that Semliki chimpanzees may face ecological time constraints and therefore bias their predation toward prey taxa that can be quickly consumed. Geographical proximity correlated with the results of the cluster analysis, while rainfall, a relatively gross measure of environment, did not. Because broad taxonomic groups of insects were used in analyses, prey availability was unlikely to have a strong effect on this pattern. Instead, we suggest that transmission of cultural knowledge may play a role in determining chimpanzee prey selection across Africa. Further study is needed to test these hypotheses.

Chimpanzees preferentially select sleeping platform construction tree species with biomechanical properties that yield stable, firm, but compliant nests.

The daily construction of a sleeping platform or "nest" is a universal behavior among large-bodied hominoids. Among chimpanzees, most populations consistently select particular tree species for nesting, yet the principles that guide species preferences are poorly understood. At Semliki, Cynometra alexandri constitutes only 9.6% of all trees in the gallery forest in which the study populations ranges, but it was selected for 73.6% of the 1,844 chimpanzee night beds we sampled. To determine whether physical properties influence nesting site selection, we measured the physical characteristics of seven common tree species at the Toro-Semliki Wildlife Reserve, Uganda. We determined stiffness and bending strength for a sample of 326 branches from the seven most commonly used tree species. We selected test-branches with diameters typically used for nest construction. We measured internode distance, calculated mean leaf surface area (cm2) and assigned a tree architecture category to each of the seven species. C. alexandri fell at the extreme of the sample for all four variables and shared a tree architecture with only one other of the most commonly selected species. C. alexandri was the stiffest and had the greatest bending strength; it had the smallest internode distance and the smallest leaf surface area. C. alexandri and the second most commonly selected species, Cola gigantea, share a 'Model of Koriba' tree architecture. We conclude that chimpanzees are aware of the structural properties of C. alexandri branches and choose it because its properties afford chimpanzees sleeping platforms that are firm, stable and resilient.

Do chimpanzees (Pan troglodytes schweinfurthii) exhibit sleep related behaviors that minimize exposure to parasitic arthropods? A preliminary report on the possible anti-vector function of chimpanzee sleeping platforms.

Great apes spend half of their lives in a nightly "nest" or sleeping platform (SP), a complex object created by modifying foliage, which functions as a stable substrate on which to sleep. Of the several purported functions of SPs, one hypothesis is that they protect against parasitic infection. Here we investigate the role of SP site choice in avoiding molestation by arthropods. This study presents preliminary data on the insect-repellent properties of preferred sleeping tree species Cynometra alexandri. Insect traps were deployed in gallery forest habitats in which chimpanzees typically "nest." We compared traps placed adjacent to SPs artificially manufactured with C. alexandri trees to an open area within the same habitat. Multiple measures of arthropod counts indicate that simulated C. alexandri SP sites have fewer arthropods than similar non-SP sites. Volatile compounds secreted by C. alexandri foliage are hypothesized to repel annoying arthropods and/or mask chimpanzee olfactory signals. Of the total insects captured (n = 6,318), n = 145 were mosquitoes. Of the total mosquitoes captured, n = 47 were identified as Anopheles (female, n = 12). The prominent malarial vector Anopheles gambiae was identified among the captured mosquito sample. These results suggest that the presence of broken branches of the tree species C. alexandri reduce the amount of insects a chimpanzee is exposed to throughout a night's sleep. This great ape behavioral and socio-technological adaptation may have evolved, in part, to increase quality of sleep as well as decrease exposure to vectors of disease.

A thermodynamic comparison of arboreal and terrestrial sleeping sites for dry-habitat chimpanzees (Pan troglodytes schweinfurthii) at the Toro-Semliki Wildlife Reserve, Uganda.

The nightly construction of an arboreal sleeping platform (SP) has been observed among every chimpanzee's population studied to date. Here, we report on bioclimatic aspects of SP site choice among dry-habitat chimpanzees (Pan troglodytes schweinfurthii) at the Toro-Semliki Wildlife Reserve, Uganda. We placed a portable weather monitor within 1 m of chimpanzee SPs and compared the microenvironment of this site with terrestrial monitors placed 10 cm above the ground directly underneath the simultaneously studied SP. We calculated physical "comfort levels" of monitored sites using the RayMan thermophysiological model that we modified to take ape body proportions into account. The RayMan tool gauges energy balance using wind speed, temperature, relative humidity, and heat index in conjunction with the study subject's mass and stature to determine whether the individual is in energy balance or homeostasis. We found that (1) terrestrial microclimates have greater homeostatic potential than arboreal microclimates, and (2) there is a significant positive linear relationship between wind speed and height of SP in the forest canopy. Advantages of terrestrial sites are that they require lesser energetic expenditure to stabilize the body when the SP is under construction and perhaps during use as well. We found that terrestrial sites also had better homeostatic potentials. This combination of advantages explains why SPs are so often sited terrestrially in habitats where predation risk is low. Early hominins must have had technological or social measures to avoid or deter predators that were significantly advanced over those found among chimpanzees before they began sleeping on the ground.

Locomotor behavior and long bone morphology in individual free-ranging chimpanzees.

We combine structural limb data and behavioral data for free-ranging chimpanzees from Taï (Ivory Coast) and Mahale National Parks (Tanzania) to begin to consider the relationship between individual variation in locomotor activity and morphology. Femoral and humeral cross sections of ten individuals were acquired via computed tomography. Locomotor profiles of seven individuals were constructed from 3387 instantaneous time-point observations (87.4 hours). Within the limited number of suitable chimpanzees, individual variation in locomotor profiles displayed neither clear nor consistent trends with diaphyseal cross-sectional shapes. The percentages of specific locomotor modes did not relate well to diaphyseal shapes since neither infrequent nor frequent locomotor modes varied consistently with shapes. The percentage of arboreal locomotion, rather than estimated body mass, apparently had comparatively greater biological relevance to variation in diaphyseal shape. The mechanical consequences of locomotor modes on femoral and humeral diaphyseal shapes (e.g., orientation of bending strains) may overlap between naturalistic modes more than currently is recognized. Alternatively, diaphyseal shape may be unresponsive to mechanical demands of these specific locomotor modes. More data are needed in order to discern between these possibilities. Increasing the sample to include additional free-ranging chimpanzees, or primates in general, as well as devoting more attention to the mechanics of a greater variety of naturalistic locomotor modes would be fruitful to understanding the behavioral basis of diaphyseal shapes.

The single species hypothesis: truly dead and pushing up bushes, or still twitching and ripe for resuscitation?

Frank Livingstone proclaims himself to be the last living proponent of the single species hypothesis. In sharp contrast, a species-rich, bushy phylogeny is favored by most human paleontologists. Is Livingstone's proclamation merely contrarian posturing, or does closer inspection warrant reconsideration of just how speciose the hominin lineage is? The high-speciation perspective draws on evidence of speciosity in the Cercopithecoidea and punctuated equilibria theory for support. If blue monkeys and redtail monkeys are indistinguishable skeletally, this reasoning goes, or if red colobus and black and white colobus are likewise indistinguishable, should we not expect that there are more species of hominin than is apparent from skeletal evidence alone? A contrarian perspective notes that not all monkey taxa are speciose. Importantly, two broadly distributed, partly terrestrial monkeys have not speciated at all: vervets and baboons. Nor are monkeys the first choice as a hominin speciation model. If expectations of species numbers are based on the Hominoidea, a taxon more closely related to hominins, more similar in body size, and found in more hominin-like habitats than monkeys, a single-species perspective is more appealing. No great ape genus has even two sympatric species. Moreover, despite a separation of 1.6 Ma, West African chimpanzees have not speciated from Pt. troglodytes nor Pt. schweinfurthii. It is notable that no two contemporaneous species of hominin were separated by significantly more than this interval. A biological--as opposed to an ecological or geographical--species definition would place all hominins in a single, phenotypically diverse species. Since divergence from the chimpanzee, "species" distinctness in hominins may have been maintained by temporary allopatry and centripetal niche separation. The hominin lineage may have evolved as a single, phenotypically diverse, reticulately evolving species.

Demography, female life history, and reproductive profiles among the chimpanzees of Mahale.

Demography provides critical data to increase our understanding of the evolution, ecology, and conservation of primate populations. The chimpanzees of the Mahale Mountains National Park, Tanzania, have been studied for more than 34 yr on the basis of individual identification and standardized attendance records. From this long-term study, we derived the following demographic data: The major cause of death was disease (48%), followed by senescence (24%) and within-species aggression (16%). Fifty percent of Mahale chimpanzees died before weaning. The median ages of female life history variables were: first maximal swelling, 10.0 yr (n = 5); emigration, 11.0 yr (n = 11); and first birth, 13.1 yr (n = 5). The median period of adolescent infertility was 2.8 yr (n = 4) when calculated from the age at immigration to that at first birth. Female fecundity was highest between 20 and 35 yr of age, with an annual birth rate of 0.2. Twenty-six females that were observed from a young age (10-13 yr) to death at various ages (15-40 yr) gave birth to an average of 3.9 and weaned an average of 1.4 offspring. Twenty-five females that were observed from middle age (18-33 yr) to death in older age (31-48) gave birth to an average of 2.7 and weaned an average of 2.0 offspring. The post-reproductive lifespan for female chimpanzees was defined as the number of years that passed from the year when the last offspring was born to the year when the female died, minus 5. Twenty-five percent of old females had a post-reproductive lifespan. The interbirth interval after the birth of a son (x = 72 mo) tended to be longer than that after the birth of a daughter (x = 66 mo). The extent of female transfer, which is a rule in chimpanzees, is influenced by the size and composition of the unit group and size of the overall local community.

GRADUAL CHANGE IN HUMAN TOOTH SIZE IN THE LATE PLEISTOCENE AND POST-PLEISTOCENE.

Starting with the onset of the last glaciation approximately 100,000 years ago and continuing to the end of the Late Pleistocene approximately 10,000 years ago, human tooth size began to reduce at a rate of 1% every 2,000 years. Both the mesial-distal and the buccal-lingual dimensions of mandibular and maxillary teeth were undergoing the same rate of reduction. From the beginning of the Post-Pleistocene until the present, the overall rate of dental reduction doubled, becoming approximately 1% per thousand years. Buccal-lingual dimensions are now reducing twice as fast as mesial-distal dimensions, and maxillary teeth are reducing at an even more rapid rate than mandibular teeth. Late Pleistocene rates are comparable in Europe and the Middle East. The Post-Pleistocene rates are also the same for Europe, the Middle East, China, Japan, and Southeast Asia. It is suggested that the cookery at the beginning of the Late Pleistocene allowed the earlier changes to occur. The use of pottery within the last 10,000 years further reduced the amount of selection that had previously maintained usable tooth substance. Reduction then occurred as a consequence of the Probable Mutation Effect (Brace, 1963; McKee, 1984).