Use of traps to capture black and gold howlers (Alouatta caraya) on the Islands of the upper Paraná River, Southern Brazil

Howlers (genus Alouatta) are widely captured with the use of anesthetic projectiles; however, no capture protocol involving the use of traps has been described to date. In the present study we describe the first efficient capture program for black and gold howlers (Alouatta caraya) using traps, which was implemented on the islands of the upper Paraná River in southern Brazil. We constructed two trap models with either manual or automatic activation (trap A with two entrances and guillotine-type doors; trap B with one entrance and a guillotine-type door). The traps were suspended in the canopy by means of vertical climbing techniques, and were baited regularly and abundantly with bananas and mangoes. We captured 70 howlers (86% using manual activation and 14% using automatic activation) on four different islands. We restrained 41 of these animals and measured their body mass, which averaged 5.30 kg+/-1.79. Given our results, we suggest that the system described in the present study represents an alternative capture program for howlers in areas that have low food diversity and no other mammal species that will compete for the bait, as has been observed in riparian environments, islands, and forest fragments.     

Ecological opportunity and diversification in a continental radiation of birds: climbing adaptations and cladogenesis in the Furnariidae

Ecological theories of adaptive radiation predict that ecological opportunity stimulates cladogenesis through its effects on competitive release and niche expansion. Given that key innovations may confer ecological opportunity, we investigated the effect of the acquisition of climbing adaptations on rates of cladogenesis in a major avian radiation, the Neotropical bird family Furnariidae, using a species-level phylogeny. Morphological specializations for vertical climbing originated in the woodcreepers ～23 million years ago, well before that adaptation occurred in woodpeckers (Picidae) or in other potential competitors in South America. This suggests that the acquisition of climbing adaptations conferred ample ecological opportunity to early woodcreepers. Nonetheless, we found that increases in speciation rates in Furnariidae did not coincide with the acquisition of climbing adaptations and that the relationship between the accumulation of climbing adaptations and rates of speciation was negative. In addition, we did not detect a diversity-dependent decline in woodcreeper diversification rates consistent with saturation of the trunk-climbing niche. These findings do not support the hypothesis that ecological opportunity related to trunk foraging stimulated cladogenesis in this radiation. The negative effect of climbing on diversification may be mediated by an indirect positive effect of climbing on dispersal ability, which may reduce speciation rates over evolutionary timescales.     

Mechanical implications of chimpanzee positional behavior.

Mechanical hypotheses concerning the function of chimpanzee anatomical specializations are examined in light of recent positional behavior data. Arm-hanging was the only common chimpanzee positional behavior that required full abduction of the humerus, and vertical climbing was the only distinctive chimpanzee positional behavior that required forceful retraction of the humerus and flexion of the elbow. Some elements of the chimpanzee anatomy, including an abductible humerus, a broad thorax, a cone-shaped torso, and a long, narrow scapula, are hypothesized to be a coadapted functional complex that reduces muscle action and structural fatigue during arm-hanging. Large muscles that retract the humerus (latissimus dorsi and probably sternocostal pectoralis major and posterior deltoid) and flex the elbow (biceps brachii, probably brachialis and brachioradialis) are argued to be adaptations to vertical climbing alone. A large ulnar excursion of the manus and long, curved metacarpals and phalanges are interpreted as adaptations to gripping vertical weight-bearing structures during vertical climbing and arm-hanging. A short torso, an iliac origin of the latissimus dorsi, and large muscles for arm-raising (caudal serratus, teres minor, cranial trapezius, and probably anterior deltoid and clavicular pectoralis major) are interpreted as adaptations to both climbing and unimanual suspension.     

Foraging habits of Alouatta palliata mexicana in three forest fragments

The activity patterns and diet of howler monkeys (Alouatta palliata mexicana) were studied in 3 forest fragments in south-eastern Mexico: Playa Escondida (PLA), Agaltepec Island (AGA) and Arroyo Liza (LIZ). Intersite differences offered the opportunity to investigate the foraging adaptations of howler monkeys in response to population and habitat size. In the largest fragment (PLA), the howlers' diet was based on high-quality items (fruit and young leaves). In AGA, where the density of howlers was the highest, their diet was mostly folivorous with a marked exploitation of uncommon food items such as vines, lianas, shrubs and herbs. The dietary differences in AGA were accompanied by more time spent travelling and less time spent resting. Although LIZ was the smallest fragment and had a high howler density, the small group size and the use of energy-minimizing strategies (less time spent travelling and more time spent resting) probably allowed howlers to maintain a frugivorous diet.     

Climbing and the daily energy cost of locomotion in wild chimpanzees: implications for hominoid locomotor evolution

As noted by previous researchers, the chimpanzee postcranial anatomy reflects a compromise between the competing demands of arboreal and terrestrial locomotion. In this study, we measured the distance climbed and walked per day in a population of wild chimpanzees and used published equations to calculate the relative daily energy costs. Results were used to test hypotheses regarding the arboreal-terrestrial tradeoff in chimpanzee anatomy, specifically whether arboreal adaptations serve to minimize daily locomotor energy costs by decreasing the energy spent climbing. Our results show that chimpanzees spend approximately ten-times more energy per day on terrestrial travel than on vertical climbing, a figure inconsistent with minimizing energy costs in our model. This suggests non-energetic factors, such as avoiding falls from the canopy, may be the primary forces maintaining energetically costly climbing adaptations. These analyses are relevant to anatomical comparisons with living and extinct hominoids.     

Goal-driven behavioral adaptations in gap-climbing Drosophila

Tasks such as reaching out toward a distant target require adaptive and goal-oriented muscle-activity patterns. The CNS likely composes such patterns from behavioral subunits. How this coordination is done is a central issue in neural motor control. Here, we present a novel paradigm, which allows us to address this question in Drosophila with neurogenetic tools. Freely walking flies are faced with a chasm in their way. Whether they initiate gap-crossing behavior at all and how vigorously they try to reach the other side of the gap depend on a visual estimate of the gap width. By interfering with various putative distance-measuring mechanisms, we found that flies chiefly use the vertical edges on the targeted side to distill the gap width from the parallax motion generated during the approach. At gaps of surmountable width, flies combine and successively improve three behavioral adaptations to maximize the front-leg reach. Each leg pair contributes in a different manner. A screen for climbing mutants yielded lines with defects in the control of climbing initiation and others with specific impairments of particular behavioral adaptations while climbing. The fact that the adaptations can be impaired separately unveils them as distinct subunits.     

Diets of some French guianan primates: Food composition and food choices

We studied food choices of black spider monkeys (Ateles paniscus) and red howlers (Alouatta seniculus) in an undisturbed tropical forest of French Guiana for 6 months in the rainy season. We made additional observations on tufted capuchins (Cebus apella) and examined the differences and similarities in feeding behavior with respect to the plant specific composition of the habitat and the biochemical characteristics of their food. Capuchins and spider monkeys mainly fed on ripe fruit pulp, to which they added invertebrates (capuchins) or young leaves (spider monkeys); their plant diet was more varied than that of howlers, which contained approximately equal proportions of ripe fruits and young leaves of many species, with large monthly variations in these food categories. BothAteles andAlouatta tended to feed preferentially on abundant plant species, with a large overlap in their fruit choices. The former species included a high proportion of soluble sugars and a low proportion of protein in its diet compared, to howlers. Leaves of several species selected byAlouatta reacted positively when screened for alkaloids and phenolic compounds. Besides specific metabolic requirements and adaptations to deriving nutrients from distinct food types, we hypothesize that the ability to taste sugars, which varies among primates, affects the range of foods appearing to be palatable and, consequently, contributes to the differentiation of feeding niches.     

Scapular position in primates

Scapular position affects shoulder mobility, which plays an important role in the upper limb adaptations in primates. However, currently available data on scapular position are unsatisfactory because of the failure to simultaneously consider the relative dimensions of all the three skeletal elements of the shoulder girdle, i.e. the clavicle, the scapula and the thorax. In the present study, the clavicular length and the scapular spine length were measured on preserved cadavers, and the dorsoventral thoracic diameter was measured on scaled radiographs of a wide range of primates, permitting a quantitative comparison of scapular position among primates. It was found that arboreal monkeys have a more dorsally situated scapula than terrestrial ones, but the same difference was not found between terrestrial and arboreal prosimians. Hominoids were found to have the most dorsally situated scapula. Contrary to the slow climbing theory of hominoid evolution, which tries to explain most postcranial specializations of hominoids as adaptations for slow climbing, the scapulae of slow-climbing lorines and Alouatta are much less dorsal than those of the hominoids.     

Glenohumeral mobility in primates

This study refutes the traditional idea that the glenohumeral joint of hominoids is more mobile than that of other primates, a belief that forms a basis for the two prominent theories of hominoid evolution. According to the brachiation theory, many anatomical features of the hominoid shoulder (including those of the glenohumeral joint) increase shoulder mobility and are interpreted as adaptations for brachiation. The slow climbing theory explains the same set of features as adaptations for slow climbing. The slow-climbing primates should therefore also possess these features, and their glenohumeral mobility should be the same as that of hominoids and be higher than that of other primates. This study presents three-dimensional glenohumeral mobility data, measured using a single video camera method on fresh specimens. The results show that the hominoid glenohumeral joint is actually less mobile than those of non-hominoid primates, including the habitually slow-climbing lorines, but it is characterized by a smooth excursion in the scapulocranial direction.     

Serum Nutritional Profiles of Free-Ranging <Emphasis Type="Italic">Alouatta Caraya</Emphasis> in Northern Argentina: Lipoproteins; Amino Acids; Vitamins A,D, and E; Carotenoids; and Minerals

Quantifying circulating nutrient concentrations in sera of free-ranging subjects will help to establish a basis from which we can evaluate the nutritional status and needs of the captive population. We collected serum samples from 26 free-ranging black-and-gold howlers (Alouatta caraya) in San Cayetano forest in northern Argentina. We analyzed them for concentrations of lipoproteins; amino acids; vitamins A, D, and E; carotenoids; and minerals. There are a few significant differences between sexes in concentrations of high-density lipoprotein cholesterol, certain amino acids, vitamin E, lutein + zeaxanthin, and copper. Most nutritional parameters are similar to the ones measured in free-ranging Mexican mantled howlers (Alouatta palliata mexicana) and in captive New World primates (NWPs). Carotenoid, vitamin D, and phosphorus concentrations are the exceptions. Carotenoid concentrations are higher in free-ranging Alouatta caraya than reported for other free-ranging and captive species. Vitamin D concentrations are 14 times greater in the free-ranging black-and-gold howlers than in captive NWPs. Phosphorus concentrations are also higher than expected and higher than typically occur in captive primates, leading to a 1:1.6 calcium:phosphorus ratio. Because we based our study on a small number of free-ranging howlers, additional samples from different regions and throughout the year would better define desirable nutritional parameters for captive howlers.     

The functional anatomy of the forelimb of some African viverridae (Carnivora)

The functional morphology of the forelimbs of the following African Viverridae was studied, Atilax paludinosus, Bdeogale crassicauda, Civettictis civetta, Genetta genetta, G. tigrina, Helogale parvula, Herpestes ichneumon, H. sanguineus, Ichneumia albicauda, Mungos mungo, Nandinia binotata. Their locomotory behaviour has been previously studied and described and is related to morphological differences. The osteology of all the species and the myology of three species is described. The species have been assigned to primary locomotor categories on the basis of their locomotion. These are 1, climbing, arboreal walking; 2, arboreal and terrestrial walking and jumping; 3, general terrestrial walking and scrambling; and 4, trotting. In the climbing arboreal walking category the most distinctive morphological adaptations are powerful flexors and extensors as well as a flexible plantigrade manus with retractile claws. In the arboreal and terrestrial walking category the shoulder, elbow and carpal joints are flexible and the manus has retractile claws, though the flexor and extensor musculature is insufficiently developed for controlled climbing. The trotting category is characterised by a high humero-radial index and a rigid antibrachium. The foot is digitigrade with the claws short and stout. Species in the general walking and scrambling category show many differences in the morphology of their feet, even though the proximal parts of the forelimb appear similar. Due to the restricted nature of the adaptations, these species have been assigned to secondary locomotor categories. Morphological characters typical of the locomotor categories are summarized in the discussion.     

Mechanical analysis of the external forces on climbing mammals

Summary Analysis of external forces acting on a climbing mammal under static conditions can be made with the method of free-body diagrams which requires the minimum number of measurements. The analysis must satisfy simultaneously equilibria for both linear translational and rotational effects of the external forces. Solution of the equations generated from the free-body diagram will give the vector direction and magnitude of the contact forces acting on the animal at the supports. Determination of these external forces cannot solve all aspects of climbing adaptations; it provides only the first essential step.     

Kinematics of vertical climbing in lorises and Cheirogaleus medius

The type of climbing exhibited by apes and atelines is argued to have been important in the evolution of specialized locomotion, such as suspensory locomotion and bipedalism. However, little is known about the mechanics of climbing in primates. Previous work shows that Asian apes and atelines use larger joint excursions and longer strides than African apes and the Japanese macaque, respectively. This study expands knowledge of climbing mechanics by providing the first quantitative kinematic data for vertical climbing in four prosimian species: three lorisid species (Loris tardigradus, Nycticebus coucang, and Nycticebus pygmaeus) that share with apes and atelines morphological traits arguably related to climbing, and a more generalized quadruped, Cheirogaleus medius. Subjects were videotaped as they climbed up a wooden pole. Kinematic values, such as step length and limb excursions, were calculated and compared between species. The results of this study show that lorises, like Asian apes and spider monkeys, use relatively larger joint excursions and longer steps than does C. medius during climbing. These data lend further support to the idea that some primate species (e.g., lorises, atelines, and apes) are more specialized kinematically and morphologically for climbing than others. Pilot data suggest that such kinematic differences in climbing style across broad phylogenetic groups may relate to the energetics of climbing. Such data may be important for understanding the morphological and kinematic adaptations to climbing exhibited by some primates.     

Health evaluation of translocated free-ranging primates in French Guiana

Among over 40 mammal species threatened by the filling of a hydroelectric dam reservoir in French Guiana, three species of primates have been translocated, comprising 124 red howler monkeys, six white-faced sakis, and 95 golden-handed tamarins. Health status of the animals was evaluated by direct physical examination and by hematological, biochemical, virological, and parasitological surveys of collected blood. The physical condition of the howlers was slightly worse toward the end of the capture period, but that of sakis and tamarins remained satisfactory. Several ectoparasites (ticks, larvae of dipterous insects, fleas, and lice) were collected, and various wounds, apparently nondebilitating, were recorded in howlers. Hematological and biochemical profiles determined for the three species revealed a slight anemia in howlers. Entamoeba, Strongyloides, and Trypanoxyurus were common in fecal samples of howlers. A survey of blood smears from the three species revealed infection by several types of microfilaria, Trypanosoma rangeli-like and Plasmodium brasilianum in all three, and Trypanosoma cruzi-like in howlers. These infections had no significant impact on the health status or the hematological profiles. Serologic investigations revealed occasional reactions against Toxoplasma gondii, a strong anti-Plasmodium response in the two Cebidae species, and a weaker one in tamarins. Attempts to isolate arbovirus failed, but antibody responses to Mayaro and yellow fever viruses were strong, especially in the howlers. A strong correlation between age and serological status led to a better understanding of the epidemic cycles. Our survey indicates French Guianan primates are reservoirs for several anthropozoonoses, including malaria, Chagas disease, and arboviruses.     

The systematic position of Hemicircus and the stepwise evolution of adaptations for drilling,tapping and climbing up in true woodpeckers (Picinae,Picidae)

The cladistic analysis of 69 morphological and behavioural characters supports the recent DNA sequence–based hypothesis that Hemicircus forms the sister group of all the remaining true woodpeckers (Picinae), but also indicates a sister‐group relationship between Dendropicini and Malarpicini, which challenges the results of previous analyses. The present phylogeny further allows a more detailed reconstruction of the stepwise evolution of adaptations for drilling, tapping and climbing up head first on vertical surfaces. The last common ancestor of woodpeckers (Picidae) was neither capable of excavating nest cavities by drilling with its beak nor of climbing up tree trunks. First adaptations for drilling such as reinforced rhamphotheca, frontal overhang and proc. dorsalis pterygoidei evolved in the ancestral lineage of piculets (Picumninae) and true woodpeckers (Picinae s.l.). Further adaptations for drilling and tapping are an enlarged condylus lateralis of the quadrate and fused cotylae mediales and laterales of the lower jaw, but these characters evolved in the ancestral lineage of Picinae s. str. and are primarily lacking in Hemicircus. The inner rectrix pairs became stiffened, and the lamina pygostyli was enlarged in the ancestral lineage of true woodpeckers (Hemicircus + Picinae s. str.). These features can be regarded as first adaptations for climbing up head first and were retained by Hemicircus. In the ancestral lineage of Picinae s. str., however, the tail feathers became further transformed into a specialized support tail, the discus pygostyli became greatly enlarged, and the ectropodactyl toe arrangement evolved. The last mentioned characters might have been the prerequisites for the enormous increase in body size in different lineages of Picinae s. str., namely Megapicini such as Campephilus and Malarpicini such as Dryocopus and Mulleripicus.     

Effects of habitat fragmentation and disturbance on howler monkeys: a review

We examined the literature on the effects of habitat fragmentation and disturbance on howler monkeys (genus Alouatta) to (1) identify different threats that may affect howlers in fragmented landscapes; (2) review specific predictions developed in fragmentation theory and (3) identify the empirical evidence supporting these predictions. Although howlers are known for their ability to persist in both conserved and disturbed conditions, we found evidence that they are negatively affected by high levels of habitat loss, fragmentation and degradation. Patch size appears to be the main factor constraining populations in fragmented habitats, probably because patch size is positively related to food availability, and negatively related to anthropogenic pressures, physiological stress and parasite loads. Patch isolation is not a strong predictor of either patch occupancy or population size in howlers, a result that may be related to the ability of howlers to move among forest patches. Thus, we propose that it is probable that habitat loss has larger consistent negative effects on howler populations than habitat fragmentation per se. In general, food availability decreases with patch size, not only due to habitat loss, but also because the density of big trees, plant species richness and howlers' home range size are lower in smaller patches, where howlers' population densities are commonly higher. However, it is unclear which vegetation attributes have the biggest influence on howler populations. Similarly, our knowledge is still limited concerning the effects of postfragmentation threats (e.g. hunting and logging) on howlers living in forest patches, and how several endogenous threats (e.g. genetic diversity, physiological stress, and parasitism) affect the distribution, population structure and persistence of howlers. More long‐term studies with comparable methods are necessary to quantify some of the patterns discussed in this review, and determine through meta‐analyses whether there are significant inter‐specific differences in species' responses to habitat loss and fragmentation. Am. J. Primatol. 72:1–16, 2010. © 2009 Wiley‐Liss, Inc.     

Foraging ecology of howler monkeys in a cacao (Theobroma cacao) plantation in Comalcalco, Mexico

Recent evidence indicates that primate populations may persist in neotropical fragmented landscapes by using arboreal agroecosystems, which may provide temporary habitats, increased areas of vegetation, and connectivity, among other benefits. However, limited data are available on how primates are able to sustain themselves in such manmade habitats. We report the results of a 9-month-long investigation of the feeding ecology of a troop of howler monkeys (n = 24) that have lived for the past 25 years in a 12-ha cacao plantation in the lowlands of Tabasco, Mexico. A vegetation census indicated the presence of 630 trees (> or =20 cm diameter at breast height (DBH)) of 32 shade species in the plantation. The howlers used 16 plant species (13 of which were trees) as sources of leaves, fruits, and flowers. Five shade tree species (Ficus cotinifolia, Pithecellobium saman, Gliricidia sepium, F. obtusifolia, and Ficus sp.) accounted for slightly over 80% of the total feeding time and 78% of the total number trees (n = 139) used by the howlers, and were consistently used by the howlers from month to month. The howlers spent an average of 51% of their monthly feeding time exploiting young leaves, 29% exploiting mature fruit, and 20% exploiting flowers and other plant items. Monthly consumption of young leaves varied from 23% to 67%, and monthly consumption of ripe fruit varied from 12% to 64%. Differences in the protein-to-fiber ratio of young vs. mature leaves influenced diet selection by the monkeys. The howlers used 8.3 ha of the plantation area, and on average traveled 388 m per day in each month. The howlers preferred tree species whose contribution to the total tree biomass and density was above average for the shade-tree population in the plantation. Given the right conditions of management and protection, shaded arboreal plantations in fragmented landscapes can sustain segments of howler monkey populations for many decades.     

Effective Solutions for Howler Conservation

All species of howlers are at risk due to habitat destruction. I review the three most serious threats to howler survival—agricultural disturbance, logging disturbance, and hunting—both in a general context and in species accounts. Withal, the adaptability of howlers has allowed them to be a widespread genus throughout Central and South America. Alouatta is especially adaptable due to its generalized folivorous diet. I discuss how this adaptability relates to survival in situations of habitat destruction. In addition, I examine howler preference for riverine habitats and their ability to capitalize on secondary forests and secondary growth. I take a practical approach, suggesting some solutions for species survival, which include habitat management and reintroductions. Successful conservation models highlighted are the Community Baboon Sanctuary in Belize, in which villagers manage their lands for the benefit of the black howler and for their own economic benefit from ecotourism, and a village-sustainable logging system in Quintana Roo, Mexico, which has reduced levels of deforestation while benefiting both villagers and howlers, as well as other wildlife. A successful translocation of black howlers in Belize in order to reestablish a viable population is also described. The paper concludes with further suggestions to encourage howler conservation.     

Recruitment of Black Howler Fruit Trees in Fragmented Forests of Northern Belize

We examined recruitment of trees whose seeds are dispersed by black howler monkeys (Alouatta pigra) in forest fragments within the Community Baboon Sanctuary in north-central Belize. In the fragments, most other large frugivores are absent and howlers dominate the large frugivore community. Consequently, we expected to observe an increased representation of howler fruit trees among the sapling community. To test this prediction preliminarily we observed howler feeding behavior for one year and conducted adult tree and sapling transects in 6 locations where howlers were present. We sampled a seventh site where howlers were absent for vegetation only. We found that in 4 of 6 sites there were proportionately fewer howler fruit saplings when compared to adult tree samples. However, when recruitment of howler fruit trees in the 6 sites was compared to a site where howlers were absent, 11 of 12 species had relatively higher recruitment. The lack of recruitment among howler fruit trees in general likely reflects differences in responses of individual species, as well as disruptions from human activities to natural processes within the forests. The observed lower recruitment patterns of howler trees suggest that over time, the abundance of the trees will likely decline and thus affect the foraging behavior and possibly survival of howlers in the fragmented forests.