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On the way to systematize habituation: a protocol to minimize the effects of observer presence on wild groups of Leontocebus lagonotus
Abstract
Habituation is used in most field research with primates to minimize observer effects on their behavior. Despite its importance, there is little published on the methods used to habituate different taxa of primates or how these methods vary in different habitat types. We assessed changes in behavior and space use of two groups of Leontocebus lagonotus in the Ecuadorian Amazon in order to document this process. Although the subjects had not been studied before, visitors and researchers were more frequently in the home range of Group 1 than of Group 2. We followed both groups for 2 months, collecting behavioral data through scan sampling and recording the use of space (ground, understory, subcanopy, and canopy) and the routes along which we followed the groups. We then divided our data into two equivalent stages, randomized the data for each stage and looked for significant differences using Wilcoxon tests. Our results show a significant decrease in submissive behaviors toward the observer for both groups and a significant increase in resting and foraging for Group 1. In addition, Group 2 used the subcanopy significantly less and the understory more during the second stage. The routes the animals used were significantly longer in the second stage for Group 1, but not for Group 2. We conclude that our methodology is adequate to advance in the habituation of L. lagonotus in less than 2 months and that a group will habituate more quickly if it has had some previous neutral exposure to humans.
... Wild primates usually react to the presence of humans and flee from them (Gazagne et al., 2020;Williamson & Feistner, 2003). Therefore, habituation to human presence is a critical first step for primate behavioral ecology studies to reduce the impact of observer presence on the behavior of study subjects and enable detailed data collection on the biotic and abiotic factors that affect primate behavior (Aguiar & Moro-Rios, 2009;Crofoot et al., 2010;Goldsmith, 2005;Hanson & Riley, 2018;Souza-Alves & Ferrari, 2010;Vicente-Alonso et al., 2021;Williamson & Feistner, 2003). Habituation generally refers to the reduction in individuals' response to repetitive stimuli (Gazagne et al., 2020;Mackintosh, 1987;Stein, 1966;Williamson & Feistner, 2003). ...
Habituation is crucial for studying the behavioral ecology of wild nonhuman primates, but the process can vary between species and sites. Few studies have described habituation in lemurs. We initiated a long-term study of black-and-white ruffed lemurs (Varecia variegata) in Vohibe Forest, eastern Madagascar, by habituating 15 individuals from three subgroups over 12 weeks (January–April 2022). We characterize their habituation by assessing changes over time in subgroup behavior (all adults and juveniles) in the presence of observers using: 1) instantaneous sampling (5-min intervals) to quantify daily activity budgets (nine behavioral categories) and 2) all-occurrence sampling to quantify daily rates of six behaviors. Over 33 days, spanning 10 observation weeks and including 171.8 observation hours, we collected 297 activity budget data points and 198 all-occurrence data points. As habituation progressed, the proportion of time that we lost the groups and the proportion of time that they spent traveling decreased while the proportion of time spent feeding, self-grooming, resting, and being vigilant increased. The lemurs also significantly reduced the frequency of their alarm vocalizations and increased the frequency of fission–fusion events. Together, these changes suggest that the lemurs resumed more typical behavior as they became habituated to observers. We conclude that traveling, alarm vocalizations, and feeding are key indicators of habituation for the black-and-white ruffed lemurs. Habituation requires careful balancing of benefits and risks by taking precautions to mitigate negative effects. Our methods for habituating black-and-white ruffed lemurs can provide guidance for future studies.
... Whereas some African apes may take several years to habituate (Goldsmith, 2005;Green & Gabriel, 2020), urban monkeys already living among humans may be easier to habituate, although the risk of monkey-human conflict remains high (Chauhan & Pirta, 2010;Priston & McLennan, 2013;Sha et al., 2009). Indeed, previous neutral exposure to humans is associated with faster habituation among some primates (Vicente-Alonso et al., 2021). As such, the impacts of habituation on some species, or individuals, are likely to be greater than those for others (Allan et al., 2020). ...
Researchers have studied non-human primate cognition along different paths, including social cognition, planning and causal knowledge, spatial cognition and memory, and gestural communication, as well as comparative studies with humans. This volume describes how primate cognition is studied in labs, zoos, sanctuaries, and in the field, bringing together researchers examining similar issues in all of these settings and showing how each benefits from the others. Readers will discover how lab-based concepts play out in the real world of free primates. This book tackles pressing issues such as replicability, research ethics, and open science. With contributors from a broad range of comparative, cognitive, neuroscience, developmental, ecological, and ethological perspectives, the volume provides a state-of-the-art review pointing to new avenues for integrative research.
... A global pandemic has forced us to rethink our approach to fieldwork to address the human-nonhuman primate (hereafter primate) interface and the risk of zoonotic disease transfer. Currently, most field projects begin with a habituation process where primates are desensitized to the presence of researchers (Souza-Alves and Ferrari 2010; Vicente-Alonso et al. 2021). ...
Keystone species are organisms, usually animals of higher trophic levels, that have large ecological impacts relative to their abundance. A recent extension of this concept recognizes hyperkeystone species, such as humans, which affect other keystone species and often play a key role in multiple ecosystem dynamics. Following a systematic review, we propose that the Neotropical palm species Mauritia flexuosa, though abundant locally, plays a role resembling that of a hyperkeystone species. First, it provides multiple types of key plant resources (food, nest sites, habitat) to a wide variety of species (at least 940 vertebrate species). Of vertebrates that directly use this palm as a food or nest resource (at least 74), at least 8 highly dependent on it for survival, 28 are threatened species, and at least 19 are keystone species themselves. This implies that a change in the abundance or distribution of Mauritia flexuosa is likely to have multiple cascading effects on Neotropical ecosystems. In addition, we highlight that this palm is also important for many invertebrates and other organisms and provides multiple ecosystem services, such as carbon sequestration. This vast ecological role of M. flexuosa, combined with its provision of a host of products to people, makes the species unique and worth prioritizing in conservation and plans for sustainable management across the Neotropics.
En este artículo se proporciona información sobre la diversidad, tamaño de grupo y densidad poblacional de primates para cada hábitat diferenciado en el área de estudio. En 556 km de transectos recorridos de setiembre a octubre del 2011 y luego de febrero a mayo y julio a octubre del 2012, se registró 200 grupos de nueve especies de primates y otras dos fueron observadas fuera de los censos, alcanzando el registro a 11 especies. Grupos más pequeños correspondieron a Pithecia aequatorialis, Callicebus torquatus y Callicebus discolor, cuyo tamaño de acuerdo al tipo de hábitat varió entre 2 y 6 individuos y la más grande fue para Saimiri sciureus (12 a 42 individuos). Las densidades poblacionales fueron más altas para Saguinus lagonotus (55,8 individuos/km2) y S. sciureus (52 individuos/km2) y la más baja para C. torquatus (0,4 individuos/km2). Grupos de S. sciureus, S. lagonotus y P. aequatorialis fueron los más frecuentemente observados (78% de los avistamientos) en los tres tipos de hábitats diferenciados. Entre las especies, Lagothrix poeppigii, Alouatta seniculus y C. torquatus estuvieron ausentes en el lado oriental de la carretera Iquitos-Nauta; la extinción local de estas especies estarían relacionadas con la alta presión de caza y deforestación.
After World War II, primate studies began on Japanese macaques and artificial provisioning facilitated short-distance observation. During these early stages of primate field research, this method allowed for individual recognition and long-term studies whereby individual and social behaviors could be described in detail and, ultimately, social structure. Owing primarily to provisioning, monkeys and apes were able to innovate some cultural behaviors. However, provisioning influences the behavior of animals. Artificially fed primate populations in Japan grew rapidly and social relationships among individuals changed. After the 1980s, scientific reports tended to not mention the incidence of provisioning in descriptions of the environment. Such omissions could inadvertently lead to misleading interpretations of the data. Therefore, authors must describe the provisioning situation as an important element of the environment. Even in the early stages of the primate studies, it should have been noted that provisioning was an experimental method and was partly an artificial living condition applied to wild populations of animals, which could have both positive and negative outcomes. In this paper I defined the terms wild, provisioning, free-ranging and habituation in appropriate words.
Habituation is the term used to describe acceptance by wild animals of a human observer as a neutral element in their environment. Among primates, the process takes from a few days for Galago spp. to several years for African apes. There are also intraspecies differences reflecting differences in habitat, home range, and ape-human relationship history. Here, we present the first study of the process of bonobo habituation in a fragmented habitat, a forest-savanna mosaic in the community-based conservation area led by the Congolese nongovernmental organization Mbou-Mon-Tour, Democratic Republic of the Congo. In this area, local people use the forest almost every day for traditional activities but avoid bonobos because of a traditional taboo. Because very few flight reactions were observed during habituation, we focused on quantitative parameters to assess the development of ape tolerance and of the tracking efficiency of observer teams. During the 18-month study period (May 2012-October 2013), 4043 h (319 days) were spent in the forest and bonobos were observed for a total of 405 h (196 contacts on 134 days). The average contact duration was stable over time (124 min), but the minimal distance during a contact decreased with habituation effort. Moreover, bonobo location and tracking efficiency, daily ratio of contact time to habituation effort, and the number of observations at ground level were positively correlated with habituation effort. Our observations suggest that bonobos become habituated relatively rapidly. These results are discussed in relation to the habitat type, ape species, and the local sociocultural context of villagers. The habituation process involves changes in ape behavior toward observers and also more complex interactions concerning the ecosystem, including the building of an efficient local team. Before starting a habituation process, knowledge of the human sociocultural context is essential to assess the balance between risks and benefits.
Field biologists adopted the term habituation from physiology, as the relatively persistent waning of a response as a result of repeated stimulation that is not followed by any kind of reinforcement (Thorpe, 1963). Repeated neutral contacts between primates and humans can lead to a reduction in fear, and ultimately to the ignoring of an observer. Historically, the techniques and processes involved were rarely described, as habituation was generally viewed as a means to an end (Tutin & Fernandez, 1991). As we become increasingly aware of the potential effects of observer presence on primate behaviour, and especially the potential risks of close proximity with humans, it behoves us to measure as much about the habituation process as possible. However, most recent studies that have quantified primate behaviour in relation to habituators have focussed on great apes (see, for example, Ando et al., 2008; Bertolani & Boesch, 2008; Blom et al., 2004; Cipolletta, 2003; Doran-Sheehy et al., 2007; Sommer et al., 2004; Werdenich et al., 2003), with little information available for other primate taxa (but see Jack et al., 2008).
A new species of titi monkey, Catticebus, is described based on five specimens obtained from the state of Sergipe, north-eastern Brazil. It is a member of the Personatus group, but is easily distinguished from the other forms. The most noticeable differences are in the pelage coloration, the forehead, crown, and ear being black, and having a zebra-like, striped pattern on the anterior half of the back. Distinct features of its dental morphology and craniometry are also described.
Play is a complex behavior that is widespread among vertebrates. Despite the potential benefits for the development of social, cognitive and motor skills, play behavior has costs: energy expenditure, and the risks of injury and predation. As the fitness benefits of play are presumably to be gained as adults, we expect young animals to minimize its immediate costs. Here, we describe play behavior in golden lion tamarins (GLTs) (Leontopithecus rosalia) and test cost-minimizing hypotheses. We collected data on play behavior and adult vigilance in nine groups (four wild and five supplemented, the latter deriving from a reintroduction) of wild-living lion tamarins (16 infants) in Brazil. Results showed that play occupied 3.8% of the activity budget, occurred during the hottest times of the day, and was characterized by being mainly social, involving partners of different ages, and sometimes different species. We found no differences in playing time between wild and supplemented groups. The lion tamarins played less in ‘dangerous’ substrates (canopy branches and forest floor), and more in ‘safe’ substrates (large branches and vine tangles), and favored playing in the center of the group over the periphery. The reproductive animals were vigilant during 78% of the time the infants were playing, and were mostly oriented away from the playing animals. The observed organization of play behavior suggests that juvenile GLTs minimize the risk of predation and accidental injuries, but do not seem to minimize energy expenditure and the risks of social injuries. The social-cognitive benefits acquired from experience of older partners during play may overcome the costs of the latter behavior, and because little time was spent in play, the energetic costs may be inconsequential.
We monitored the impact of habituation for tourism through changes in gorillas' behavior during the habituation process at Bai Hokou (Dzanga-Ndoki National Park, Central African Republic) from August 1996 to December 1999. From August 1998 onwards we focused on one gorilla group: the Munye. During the habituation process, it became increasingly easier to locate and to remain with the gorillas. Their initial reactions of aggression, fear and vocalization upon contact were replaced increasingly by ignoring us. Curiosity appeared to be an intermediate stage in the process. The way in which contacts with the Munye ended became more subdued over time. Regular daily contact is important in promoting habituation. Likewise, contacting gorillas while they are in a tree or in dense forest provides positive results compared to open habitat. Contacts within 10 m and contacts without forewarning the gorillas of observer presence, e.g., via tongue clacking, should be avoided. As of December 1999, habituation had progressed well; habituation of western gorillas is feasible. However, the gorillas experience negative effects during the habituation process, showing, for example, an increase in daily path length, and reactions of aggression, fear and vocalization upon contact. Impacts diminish over time. Given these and other potentially negative effects, the decision to begin habituation should not be taken lightly.
In the Serengeti National Park, Tanzania, large fluctuations of prey abundance alters the frequency at which spotted hyena
(Crocuta crocuta) cubs are nursed and thus the total level of maternal input available to them. Maternal input is high when mothers feed on
high densities of locally available migratory herbivores and low when mothers travel up to 70km to forage. Using data from
19 cub cohorts on the incidence of siblicide (from monitoring the survival of 609 cubs in twin litters) and cub growth rates
(from 195 cubs in twin litters) as a measure of maternal input, we demonstrate that the incidence of siblicide increased as
average cohort growth rate declined. In total, there were 37 siblicides in 384 litters (9% of litters). When both cubs were
alive, total maternal input in siblicidal litters was significantly lower than in non-siblicidal litters and the mean share
of the dominant sib of 64.6% was significantly higher than the mean of 52.1% for dominant sibs of non-siblicidal litters.
After siblicide, growth rates of siblicide victors substantially increased, demonstrating that mothers did not reduce maternal
input after litter reduction. As a result, siblicide victors achieved a long-term growth rate similar to that of singletons
and thus significantly increased their expected survival. We conclude that in spotted hyenas, high maternal input in lactation
has favoured the evolution of facultative siblicide in populations inhabiting areas with low or fluctuating food resources.
Animal populations are increasingly challenged by anthropogenic environmental changes. Species, populations and individuals vary in their ability to cope with exposure to human proximity. However, little is known about what drives habituation or sensitization in wild populations. Via behavioural observations and heart rate telemetry during experimental disturbance, we determined the habituation potential of yellow-eyed penguins, Megadyptes antipodes, a key species for nature-based tourism in southern New Zealand. Individual birds differed significantly in both their initial stress response and habituation potential. While some birds did not habituate, or even appeared to be sensitized by frequent disturbance, others habituated. Individual variation in habituation potential depended on previous experience with humans, sex and character (i.e. timid, calm or aggressive). Birds that were exposed to research that involved frequent interactions at the nest site, including blood sampling, several years prior to our experiments were less likely to habituate. Overall, females were more flexible than males in their stress response pattern, and calm individuals appeared to adapt more readily than aggressive birds. Character, classified during penguin–researcher interactions at the nest site, was independent of sex, age or previous experience, and was consistent over two seasons. Initial heart rate response to human approach, also similar between seasons, varied with sex and character of an individual. Yellow-eyed penguins may habituate to short and consistent approaches, but appear unsuitable for unregulated tourist visits at nest sites. Individual differences in habituation potential to human disturbance can have fitness consequences and may lead to contemporary evolutionary change in the composition of breeding populations.
Adequate habituation of free-ranging subjects is essential for any field study, but is generally unsystematic. Here, attempts to habituate three titi monkey (Callicebus coimbrai Kobayashi & Langguth, 1999) groups are described, and factors determining the effectiveness of the process are discussed. The "relentless pursuit" approach was aided by playback recordings of vocalizations but only one group was habituated adequately. Average contact in 13 encounters with group 1 was just over one minute, whereas in 32 encounters with group 2, it averaged 3,5 minutes (maximum = 22 minutes). Group 3 was more tolerant of observers, and was considered fully habituated by the seventh encounter. The factors determining this disparity remain unclear, although vegetation density seems important. Whereas group 3 occupied an area of relatively undisturbed forest, with a sparse understory, the other groups occupied a habitat with dense undergrowth and an irregular canopy. The subjects' tolerance may have been affected by reduced visibility and less discreet behavior of the observers. On 10 occasions, the members of group 2 leapt to the ground and fled through the undergrowth. The results indicate the need for a careful evaluation of habitat characteristics prior to the selection of groups for habituation.
The callitrichines are a specialized radiation of primates that are characterized in part by variable social systems and cooperative infant care. Callimico goeldii, unlike the other callitrichines, have single rather than twin offspring, reducing the need for allocare and permitting synchronous breeding within groups. Low mortality rates among offspring and unstable social groups are suggested to be possible factors that have led to single births among C. goeldii. Single offspring may benefit from greater maternal investment and more frequent food sharing than twin offspring, factors that may help to explain why C. goeldii reaches sexual maturity more rapidly than other callitrichines. In addition, increased breeding opportunities for young C. goeldii females may have selected for rapid maturation rates among this species. Postpartum ovulation and aseasonal resource availability appear to permit females to have biannual birth seasons, further increasing the potential reproductive output.
This study demonstrates that ocelots (Leopardus pardalis) extensively use primates as a food resource at the Caratinga Biological Station (CBS) in Southeast Brazil. Analysis of 60 fecal samples collected over 4 years revealed predation upon the brown howler monkey (Alouatta guariba), the muriqui (Brachyteles hypoxanthus), and the brown capuchin monkey (Cebus apella). The most frequent items found in the fecal samples analyzed were Calomys (n=16) and non-identified Aves (n=15), followed by A. guariba (n=12). Although Rodentia was the most common group consumed (n=52) Primates were found in 27% of total fecal samples and were the third most consumed group in relation to the total items. Particularly, predation of A. guariba by ocelots (20% of the total fecal samples) was not an isolated event; our results showed that this species was preyed on across several months. Predation on primates was far higher at CBS than at other sites where comparable studies have been carried out.
The last part of the chimpanzee (Pan troglodytes) habituation process of the Taï South Group was monitored over 2 years (1994-1996), during which all males and most of the females became habituated to observation by humans. The time needed (5-7 years) to habituate the community was similar to that recorded for the Taï North Group and is comparable to other populations studied in Africa. Variation emerged in habituation rate: males were habituated earlier than females, and among females, sexually cycling individuals were habituated faster than non-cycling females. Such differences may be a function of both the methods used to find the chimpanzees and the sex of the individual. Reproductive status and individuality may also have influenced habituation rates by affecting the number of contacts required to habituate a chimpanzee to neutral humans.
Like other animals, primates respond to predation using behavioural adaptations. Hence, they should optimise their escape strategy under the risk of predation, and flee at a distance, referred to as flight initiation distance (FID), when the fitness-related benefits of staying are balanced against the costs of escape. However, there is an absence of FID studies in primates. In this study, we used vervet monkeys Chlorocebus pygerythrus, a medium-sized African cercopithecoid, as a model species to investigate the influence of environment type (urban and rural), group size (defined as the number of visible neighbours), sex and age on FID when approached by a human. We found significantly shorter FID among urban than rural monkeys; urban individuals delayed their escape compared to rural individuals. We found no relationship between FID and sex and age class, but FID was positively correlated with group size in both settings; urban monkeys live in smaller groups than monkeys in rural areas. As FID and group size are important predictors of predation risk perception in primates, results suggest that, despite probable effects of habituation, vervet monkeys in Uganda adjust their antipredator behaviour when coping with novel environments within human settlements. Our findings are consistent with some previous studies of risk perception in animals, and indicate that FID could be used as an alternative measure for predation risk in primates.
Wild primates show a variety of responses when primatologists arrive to study them. Some are very shy and flee rapidly, while others lack fear and are easy to approach and observe. Habituation is the term used to describe the acceptance by wild animals of a human observer as a neutral element in their environment. The process is rarely described, as it is commonly regarded as a means to an end; namely, the progression to a state that allows the natural behaviour of a species to be observed and documented.
Primatology, as a field of study within biological anthropology, is the science of understanding nonhuman primates with the goal of gaining insight into the human condition. To better examine and understand the behavioral intricacies of their study animals, primatologists usually rely on habituating their subjects to their presence. As defined by Tutin and Fernandez (1991), habituation is the acceptance by wild animals of a human observer as a neutral element in their environment. This is the progression to a state that allows the natural behavior of a species to be observed and documented. Although information from habituated primates has been instrumental in providing a wealth of information for both research and conservation, little attention has been given to the costs these animals bear when their fear of humans is removed.
Twelve generic names have been ascribed to the New World tamarins but all are currently placed in just one: Saguinus Hoffmannsegg, 1807. Based on geographical distributions, morphology, and pelage patterns and coloration, they have been divided into six species groups: (1) nigricollis, (2) mystax, (3) midas, (4) inustus, (5) bicolor and (6) oedipus. Molecular phylogenetic studies have validated five of these groups; each are distinct clades. Saguinus inustus is embedded in the mystax group. Genetic studies show that tamarins are sister to all other callitrichids, diverging 15 to 13 Ma. The small-bodied nigricollis group diverged from the remaining, larger tamarins 11 to 8 Ma, and the mystax group diverged 7 to 6 Ma; these radiations are older than those of the marmosets (Callithrix, Cebuella, Mico), which began to diversify 6 to 5 Ma. The oedipus group diverged from the midas and bicolor groups 5 to 4 Ma. We review recent taxonomic changes and summarize the history of the generic names. Taking into account the Late Miocene divergence time (11 to 8 Ma) between the large- and small- bodied tamarin lineages, the small size of the nigricollis group species when compared with other tamarins, and the sympatry of the nigricollis group species with the larger mystax group species, we argue that the nigricollis group be recognized as a distinct genus: Leontocebus Wagner, 1839.
The monthly daytime and night-time diet, activity and feeding height of an habituated black lemur group were compared by ‘auditory group sampling’ for a total of 561 daytime hours and 472 night-time hours in Lokobe Forest, Madagascar. Both the daytime and night-time diets were dominated by fruit, but the former was more diverse than the latter and included more leaves. Some food items were eaten mainly or solely at night or during the day. The proportion of total time spent feeding was variable and was lowest between March and June, coinciding with a dearth of ripe fruit. The proportion of night-time spent feeding exceeded the proportion of daytime spent feeding during August, September, October and December. The group fed more frequently in the undercanopy during the day and the canopy during the night. The ratio of time spent feeding to time spent travelling was significantly smaller during the day compared to the night. These differences can be best explained by the group preferring to feed in the undercanopy during the day and the canopy at night.
A free-ranging troop of 108 to 130 yellow baboons (Papio cynocephalus) was sampled systematically for 1596 h. Seasonal variations in the area of the range of the troop, and the degree to which the patterns of range use of the troop were clumped in space are found to be correlated with (1) diversity of use of sleeping sites, (2) time of departure from sleeping trees, (3) number of impregnable females in the troop, and (4) number of emigrations from, and immigrations into the troop by adult males. The reproductive strategies of troop members, especially those of impregnable females, are suggested to influence patterns of range use. Some effects of the presence of observers on the troop are measured and discussed.
Seven major types of sampling for observational studies of social behavior have been found in the literature. These methods differ considerably in their suitability for providing unbiased data of various kinds. Below is a summary of the major recommended uses of each technique: In this paper, I have tried to point out the major strengths and weaknesses of each sampling method. Some methods are intrinsically biased with respect to many variables, others to fewer. In choosing a sampling method the main question is whether the procedure results in a biased sample of the variables under study. A method can produce a biased sample directly, as a result of intrinsic bias with respect to a study variable, or secondarily due to some degree of dependence (correlation) between the study variable and a directly-biased variable. In order to choose a sampling technique, the observer needs to consider carefully the characteristics of behavior and social interactions that are relevant to the study population and the research questions at hand. In most studies one will not have adequate empirical knowledge of the dependencies between relevant variables. Under the circumstances, the observer should avoid intrinsic biases to whatever extent possible, in particular those that direcly affect the variables under study. Finally, it will often be possible to use more than one sampling method in a study. Such samples can be taken successively or, under favorable conditions, even concurrently. For example, we have found it possible to take Instantaneous Samples of the identities and distances of nearest neighbors of a focal individual at five or ten minute intervals during Focal-Animal (behavior) Samples on that individual. Often during Focal-Animal Sampling one can also record All Occurrences of Some Behaviors, for the whole social group, for categories of conspicuous behavior, such as predation, intergroup contact, drinking, and so on. The extent to which concurrent multiple sampling is feasible will depend very much on the behavior categories and rate of occurrence, the observational conditions, etc. Where feasible, such multiple sampling can greatly aid in the efficient use of research time.
Resumen. Los anfibios y reptiles que se encuentran en un área pequeña dentro de una reserva fragmentada de bosque lluvioso en la Amazonía ecuatoriana han sido intensivamente investigados en un período inicial de dos años mediante la recolección de muestras (1986–88). Esta actividad coincidió con la construcción de un camino a través del área y la subsiguiente oleada de conversión y fragmentación del bosque en las áreas circundantes. Se empleó una técnica de muestreo de transectos de tiempo restringido para facilitar luego el monitoreo de encuentro visual post-fragmentación y reunir datos de largo plazo sobre la riqueza y composición de las especies (en una escala cronológica desigual). Entre 1998 y 2005 se acumuló un esfuerzo de investigación y muestreo equivalente en la misma área reducida para compararla con la información de 1986 a 1988, en un intento por evaluar la eficiencia de esta reserva en la conservación de la fauna herpetológica documentada más de 10 años atrás. Basada en un total de 6,722 registros individuales obtenidos durante 1,117 horas de recolección de muestras divididas en dos períodos principales y cinco períodos secundarios de muestreo, la diversidad herpetofaunística estuvo entre las más altas reportadas hasta el momento en una única ubicación en la Amazonía, con 84 especies de anfibios y 82 especies de reptiles registrados de 1986 a 2007. Se provee una lista completa de especies, con comentarios en los registros más significativos. De las 73 especies de anfibios y 46 especies de reptiles registradas de 1986 a 1988, 68 anfibios (93%) y 40 reptiles (87%) fueron registrados nuevamente en el muestreo de 1998 a 2007; 11 especies de anfibios y 33 especies de reptiles no registrados entre 1986 y 1988 fueron añadidos en 1998 a 2007. Mediante un análisis de composición de pareja entre todos los períodos de muestreo usando un indice de similitud revelaron un > 50% de similitud para ambos grupos taxonómicos entre períodos; la similitud de estos dos períodos principales (1986–88 vs. 1998–2005) fue 0.90 por anfibios y 0.70 por reptiles. El presente estudio provee otro punto de referencia de sitio único para la herpetofauna megadiversa de la zona alta de la cuenca amazónica, pero es diferente ya que ofrece datos de largo plazo en la persistencia de especies; los resultados de un lapso de muestreo de 20 años sugieren que esta pequena reserva, desde 1986 ha conservado exitosamente esta fauna. Estos resultados coinciden con estudios previos de largo plaza de la cuenca central de la Amazonía en sugerir que las reservas relativamente pequeñas y otros remanentes de bosque con suficiente diversidad de hábitat pueden contribuir sustancialmente a la continua supervivencia de la alta diversidad de comunidades herpetofaunísticas de los bosques lluviosos amazónicos en medio de la extendida deforestación regional.
The ranging behaviour of a group of marmosets (Callithrix humeralifer) in seasonal Amazonian rain forest was studied during one year. Range sizes (monthly and daily), day range lengths and patterns of range use are examined for correlations with feeding behaviour and the distribution of three forest types within the marmoset's range. Seasonal differences in ranging are associated with changes in the abundance and distribution of plant food sources. The marmosets ranged more widely and used more sources of a greater diversity of plant food species, which were distributed over a wider area, in the wet season than in the dry season. In the dry season, they ranged over a smaller area and, although they used fewer sources of a reduced diversity of plant species overall, they exploited a larger number of sources of the five highest ranked plant species in the diet. Throughout the year, they showed a preference for disturbed primary forest, characterized by dense understoreys and abundant second growth patches. Reasons for this preference are discussed, taking into account their use of fruits of typical pioneer species (particularly in the dry season), insect prey abundance, sleeping site availability and defence against predators.
The first extensive butterfly survey of the upper Río Napo ba-sin in eastern Ecuador was conducted from 1990 to 1993. A total of 811 species was recorded at Jatun Sacha Biological Reserve. Based on species richness comparisons with a similar site in southern Peru and extrapola-tions from ithomiine diversity, Jatun Sacha is estimated to have approxi-mately 1300 species of butterflies. Species richness is compared with two other Amazonian sites (Pakitza, Peru, 1300 species and Cacaulandia, Bra-zil, 843 species). Species and generic compositions are more similar be-tween Pakitza and Jatun Sacha than Cacaulandia. This similarity may be due to environmental factors. A greater percentage of Nymphalidae and a lower percentage of Hesperiidae and Lycaenidae occur at the two some-what disturbed sites (Jatun Sacha and Cacaulandia) than the less disturbed site (Pakitza). Of the 228 species common to all three sites, more nympha-lid butterfly species were found than expected based on observed spe-cies in each family.
Chimpanzees in Gombe National Park, Tanzania have been given bananas since 1962. Attendance rates at the feeding area, aggregation sizes and the frequency of aggresson of chimpanzees and baboons were closely affected by the manner of feeding. Reduced access to food appeared most responsible for the increase in aggression. The advantages and disadvantages of artificial feeding are discussed.
Mycophagy has been documented in a number of species of marmosets and lion tamarins (Callitrichinae) but its effect on ranging behavior is not known. We present the results of 10 years of research on five groups of Goeldi's monkey (Callimico goeldii) at a field site in northwestern Bolivia. We studied the diet and ranging behavior of two of the groups. On average, groups contained 4.5 individuals (range 2.0-9.0), but they gradually decreased in size until only the breeding female remained in the home range. The annual diet was composed of fungi (31.1-34.9%), fruits (34.0-40.6%), prey (17.4-30.1%), and exudates (1.0-10.9%). They had large home ranges (114-150 ha) and over time individuals tended to shift their core areas of use. They used secondary and bamboo forest and forest with dense understories more than expected based on availability. We suggest that the large home ranges and shifting core areas used by C. goeldii are components of a foraging strategy to track patchy, low density, and ephemeral fungal fruiting bodies. Our results, along with data published on other callitrichines, indicate that groups of Leontopithecus, Callithrix, and Callimico that eat fungi have larger home ranges than those that do not. Mycophagy is one of the several factors that evidently affect home range size in callitrichines. Fungi are clearly an important food source for a number of populations, but additional studies are needed to determine why some eat fungi frequently while others do not.
INTRODUCTION
Field biologists adopted the term habituation from physiology, as the relatively persistent waning of a response as a result of repeated stimulation that is not followed by any kind of reinforcement (Thorpe, 1963). Repeated neutral contacts between non-human primates (hereafter called primates in this chapter) and humans can lead to a reduction in fear, and ultimately to the ignoring of an observer. The techniques and processes involved have only rarely been described (e.g. Schaller, 1963; Kummer, 1995), as habituation has generally been viewed as a means to an end (Tutin & Fernandez, 1991). The few studies that have quantified primate behaviour in relation to habituators describe the process with African great apes (Grieser Johns, 1996; van Krunkelsven et al., 1999; Blom et al., 2001). As we become increasingly aware of the potential effects of observer presence on primate behaviour, and especially the potential risks of close proximity with humans, it behoves us to measure as much as possible about the habituation process.
Many behavioural responses are taxon specific, and these should be taken into account when one is trying to habituate human-naïve wild primates. Between us we have had experience with a wide range of wild primates, ranging in size from marmosets (Callithrix spp.) to gorillas (Gorilla spp.), from South America, Africa, Madagascar and Asia, which, together with discussions with colleagues, we have used to make this chapter as broadly applicable as possible.
Data on the activity pattern of a group of red colobus monkeys (Colobus badius rufomitratus) living along the Tana river, Kenya, were collected during monthly 5-day observation periods between October 1973 and December 1974. The two most important activities were feeding and resting which occupy about one-third and one-half of daytime, respectively. These proportions vary considerably, however, according to age-sex class, time of day and month of year. Compared to a group studied at a rain-forest site in Uganda, the Tana animals spend substantially less time feeding and more time resting. Possible reasons for this difference are discussed.
Habituation of nonhuman primates to observer presence is a necessary and often arduous prologue to collection of data on individuals. Subjects are habituated so their behavior will be as close as is possible to their behavior if the observer were not present [1]. In an initial field study conducted on a new study group, habituation may account for a major proportion of the observers’ time [2-5].
This report describes the activity budget of a group of Callithrix geoffroyi in a patch of Atlantic forest on the Brazilian coast, between February 1993 and January 1994, using the scan sampling methods. On average, the group rested for 29% of the daylight hours, fed for 21%, moved for 20%, and foraging and gouging occupied 14% and 13% of this period, respectively. A greater proportion of time was spent resting during the wet seasons (32.1%) than the dry seasons (17.8%), but the reverse observed for time spent foraging (9.7% and 20.6% of the group's daylight hours during wet and dry seasons, respectively). The time allocated to feeding was greater in the first hours of the day. Gum consumption showed two peaks, a larger one in the early morning and a minor one in the afternoon. Animal prey foraging occurred throughout the day, but was more intense during the hottest hours. The increase in foraging and decrease in resting during the dry season was related to a decrease in the availability of insects.
Habituation of western gorillas to human presence is generally an expensive, lengthy and difficult process. Here we describe the habituation process for two groups of western gorillas at the Mondika Research Center, with the hope that the lessons we learned will facilitate future gorilla studies. We expand upon earlier studies by describing the process through complete habituation for both males and females, and for more than one group. The major obstacle to habituation was developing sufficient tracking skills to follow gorilla trail on a daily basis. Once this was achieved, the silverback became semi-habituated (i.e. ignoring human presence during half of contacts) within a year, although the majority of group females continued to avoid humans. As female presence at contacts increased, a period of male recidivism followed, requiring an additional year before his complete habituation was reached. Habituating the females took longer than the male, but we found, contrary to earlier studies, that it consisted of the same stages, including avoidance, aggression, and curiosity before habituation. We compare results between groups and across sites and discuss how factors such as tracking abilities, group size and cohesion, population density and home range overlap, and the manner of approaching gorillas during contacts influence the habituation process.
We report on the responses of Cebus capucinus in the Santa Rosa Sector of the Area de Conservación Guanacaste, Costa Rica, to the presence of observers over a 4-week period. Study groups were habituated to different degrees: (1) Cerco de Piedra (CP): continuous observations began in 1984; (2) Exclosure (EX): focus of an 18-month study on males from 1998 to 1999; and (3) NBH: never studied/followed but the group frequently encounters researchers. We collected three types of data: group scans (group state was coded as calm or agitated at observer presence), focal animal data (observer-directed behaviors were recorded), and fecal cortisol levels. The two less-habituated groups (NBH and EX) differed significantly from the habituated group (CP) in their behavioral and cortisol responses, and they showed an increase in habituation over the study period (agitation and cortisol levels both dropped). Individuals in NBH also decreased their responses to observers during focal follows; however, at the end of the study the responses of the two less-habituated groups (NBH and EX) remained elevated in comparison to the habituated group (CP), suggesting the need for further habituation. Unlike capuchin groups that rarely encounter humans, NBH and EX never fled from observers and they rarely emitted observer-directed alarm calls. We suggest that the permanence of habituation and the ability to habituate animals passively through a neutral human presence are both important considerations for researchers conducting studies in areas where animal safety from poachers, etc. cannot be guaranteed.
Distribution and demography of Leontocebus spp. in Amazonian Ecuador, are they influenced by human activities
- Torre De La
- S De la Torre
De la Torre S (2017) Distribution and demography of Leontocebus spp.
in Amazonian Ecuador, are they influenced by human activities?
BioBrasil 7:133-144
Species diversity in vertical, horizontal, and temporal dimensions of a fruit-feeding butterfly community in an Ecuadorian rainforest
- P J Devries
- D Murray
- R Lande
- PJ Devries