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Partial regressions of the number of terrestrial records in titi monkeys against (a) study duration (controlled for rainfall level and vegetation height) and (b) rainfall level (controlled for study duration and vegetation height).
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For arboreal primates, ground use may increase dispersal opportunities, tolerance to habitat change, access to ground-based resources, and resilience to human disturbances, and so has conservation implications. We collated published and unpublished data from 86 studies across 65 localities to assess titi monkey (Callicebinae) terrestriality. We exa...
Citations
... So far, terrestrial foraging but not terrestrial travelling has been observed in P. oenanthe (DeLuycker, 2007). However, other Plecturocebus species regularly forage and travel on the ground, including travelling between forest fragments (Martıńez and Wallace, 2011;Souza-Alves et al., 2019). Travelling between forest fragments, both above and on the ground, has been reported in different species of howler monkeys, genus Alouatta (e.g (Asensio et al., 2009;Arroyo-Rodrıǵuez and Dias, 2010;Serio-Silva et al., 2019). ...
This study describes the characteristics of forest fragments occupied by a Critically Endangered endemic Peruvian primate, the San Martín titi monkey, Plecturocebus oenanthe (Pitheciidae; Platyrrhini). We selected 45 fragments; 20 had already been surveyed in 2015 by the Proyecto Mono Tocón (six of these had been further split, resulting in 27 fragments); an additional 18 fragments were randomly selected from satellite images. We surveyed these fragments for the presence of P. oenanthe and determined characteristics of the fragments (size, shape, tree density, canopy height) and of the landscape (distance to nearest fragment and road). We also examined changes in the number of fragments and in forest cover between 2015 and 2019. We encountered P. oenanthe in all surveyed fragments except for the smallest one (0.2 ha). Our findings suggest that P. oenanthe can persist in fragments with a wide range of characteristics, particularly with regard to size and tree density. Unless fragmentation continues and overall forest cover in the area diminishes further, the species may be able to persist even in a fragmented landscape, provided that the matrix allows for movements between fragments. However, persistence might not be long-term if groups are not reproductive, populations become too small, and reduced gene flow results in inbreeding.
... Traditional methods of collecting primate locomotor behavior data consist of direct in situ observations, which may influence the frequency and duration of terrestrial behaviors of primates, even those that are accustomed to human presence (e.g., Souza-Alves et al. 89 ). Camera trap surveying is an ideal approach to observe terrestrial behaviors in primates, providing researchers with the means to capture rare behaviors without the risk of disrupting their natural expressions, and should be deployed whenever possible for this purpose. ...
Terrestriality is relatively rare in the predominantly arboreal primate order. How frequently, and when, terrestriality appears in primate evolution, and the factors that influence this behavior, are not well understood. To investigate this, we compiled data describing terrestriality in 515 extant nonhuman primate taxa. We describe the geographic and phylogenetic distribution of terrestriality, including an ancestral state reconstruction estimating the frequency and timing of evolutionary transitions to terrestriality. We review hypotheses concerning the evolution of primate terrestriality and test these using data we collected pertaining to characteristics including body mass and diet, and ecological factors including forest structure, food availability, weather, and predation pressure. Using Bayesian analyses, we find body mass and normalized difference vegetation index are the most reliable predictors of terrestriality. When considering subsets of taxa, we find ecological factors such as forest height and rainfall, and not body mass, are the most reliable predictors of terrestriality for platyrrhines and lemurs.
... These encounters sometimes lead to interspecies aggression (Aldrich 2006;DeLuycker 2006DeLuycker , 2007b. Young individuals of these species have been seen playing together for extended periods (DeLuycker 2007b;Souza-Alves et al. 2019). DeLuycker (2007b reported that C. oenanthe would react to alarm calls of the Common Andean Saddle-back Tamarin, retreating to less exposed places, and that it would only enter more exposed or higher risk areas after the tamarins left. ...
Callicebus oenanthe Thomas, 1924, commonly known as the San Martín Titi Monkey, is endemic to the northern portion of the department of San Martin, in the Alto Mayo and Huallaga river valleys. It lives in family groups, consisting of a monogamous pair and their offspring. It occurs at elevations between 200 and 1,000 m. Callicebus oenanthe feeds primarily on fruit, but includes other foods like leaves, flowers, and invertebrates in its diet. Although locally common, the species is listed as “Critically Endangered” (CR) both by the International Union for Conservation of Nature and under Peruvian legislation.
... The group size varies between two and seven individuals; as in other titi monkeys, they usually produce one offspring per year, but a single case of twin birth has been recorded (Santana et al. 2014). Also, Coimbra-Filho's titi monkeys follow an income breeding strategy, where the lactation period coincides with the period of high fruit availability (Souza-Alves et al. 2019a, 2019b. They explore primarily the low-medium forest strata (5-10 m) (Chagas and Ferrari 2010) and use tall and large trees as sleeping sites (Souza-Alves et al. 2011b). ...
Many primatological studies do not assess direct indexes of food availability to make inferences about behavioral strategies. We related the diet and behavior of a group of Callicebus coimbrai in northeastern Brazil to fruit availability indexes and compared this pattern between seasons (direct and indirect assessment of food availability) to assess whether direct and indirect approaches detect similar ecological patterns. We monitored the study group for 33 months (5 days/month) via scan sampling. Monthly availability of fruits and new leaves was recorded in phenological transects. Fruit availability varied across years based on fruit prevalence, and timing and duration of the abundant seasons. We did not find evidence of a time-minimizing strategy, since C. coimbrai did not change its activity levels according to food availability. However, the negative relationship between foraging and fruit availability indicates that C. coimbrai can compensate for the lower fruit availability by increasing the search for alternative food sources. Monthly fruit consumption was positively correlated to fruit availability and negatively related to the consumption of other food items. However, the behavioral and feeding profiles did not vary between seasons and were not related to rainfall levels. Primate studies should directly relate behavioral and feeding profiles to fruit availability indices, thus avoiding using seasons as proxies of food availability.
... Throughout the Amazon, they commonly live in seasonally flooded lowland forests, as well as terra firme and highland forests that do not flood. In these forests, they occupy every forest stratum from 3 to 35 m above the ground (Moynihan 1964;Wright 1978;Aquino and Encarnacion 1986;González-Hernández et al. 2020) and can use terrestrial stratum to cross natural and anthropogenic canopy gaps Souza-Alves et al. 2019). ...
The owl monkeys, genus Aotus, are among the most widely distributed of all platyrrhine genera. The 13 currently recognized taxa are found in Argentina, Bolivia, Brazil, Colombia, Ecuador, Panama, Paraguay, Peru, and Venezuela. They range from lowland tropical moist and dry forests to over 3000 m.a.sl. in the cloud forests of the Andes. Owl monkeys appear to be sufficiently flexible to persist in anthropogenically altered habitats and fragmented forest patches. Here we gathered 1,703 owl monkey localities from a wide range of published and unpublished sources, making the most comprehensive database to date. These records were used to map the distributions of all owl monkey taxa based on our current understanding of the genus. Our knowledge is still limited in many areas where records are lacking, and we caution that all species IDs and maps be treated as tentative until the wide-ranging employment of genetic testing is available.
... For example, golden-backed uakari (Cacajao melanocephalus ouakary) only foraged on the ground at patches closer to arboreal refuges and further from dense ground-based vegetation, presumably to avoid ambush (Barnett et al., 2012a). Despite the danger of terrestrial predators, arboreal primates use the ground to avoid predation by flying/arboreal predators (Barnett et al., 2012b), to forage (Souza-Alves et al., 2019, to reduce energy expenditure when sleeping (Samson & Hunt, 2012) or foraging (Eppley et al., 2016a), and to avoid intraspecific competition and hostility (Campbell et al., 2005;Williamson et al., 2021). As habitat degradation and climate change continues, arboreal primates might increase using the ground for resource acquisition and thermoregulation needs (Eppley et al., 2022;Souza-Alves et al., 2019), increasing their likelihood that terrestrial predators kill them at higher rates and add pressure to already threatened populations. ...
... Despite the danger of terrestrial predators, arboreal primates use the ground to avoid predation by flying/arboreal predators (Barnett et al., 2012b), to forage (Souza-Alves et al., 2019, to reduce energy expenditure when sleeping (Samson & Hunt, 2012) or foraging (Eppley et al., 2016a), and to avoid intraspecific competition and hostility (Campbell et al., 2005;Williamson et al., 2021). As habitat degradation and climate change continues, arboreal primates might increase using the ground for resource acquisition and thermoregulation needs (Eppley et al., 2022;Souza-Alves et al., 2019), increasing their likelihood that terrestrial predators kill them at higher rates and add pressure to already threatened populations. Understanding how arboreal primate ground use is influenced by their perception of predation risk is therefore important in this changing world. ...
It is thought arboreal species avoid foraging on the ground due to perceived predation risk, making the study of when and where arboreal species use the ground key in understanding foraging versus safety tradeoffs. We used publicly available, opportunistic, camera-trap observations from surveys across Madagascar to examine whether arboreal lemur ground use was spatially and temporally related to fosa (Cryptoprocta ferox), a native predator, and human presence. We observed 14 species of diurnal lemur (n = 287 individual observations) and six species of nocturnal lemur (n = 105 individual observations). With static two-species occupancy models and kernel density estimation, we found diurnal and nocturnal lemur ground use was spatially and temporally related to fosa presence. Diurnal lemurs used the ground less at camera locations where fosa were present compared to camera locations where they were absent, particularly if those camera locations lacked other native carnivores. Nocturnal lemurs used the ground more at camera locations fosa were observed at within the past 5 days compared with camera locations where fosa were not observed at within the past 5 days. Despite humans and diurnal lemurs being active at the same time 80% of the diel cycle (temporal overlap Δ = 0.80; 95% confidence interval [CI]: 0.75–0.85), diurnal lemur spatial or temporal use of the ground and human presence were unrelated. Diurnal lemur temporal overlap with humans at camera locations where fosa were uncommon was higher (Δ = 0.79; 95% CI: 0.71–0.86) compared with where fosa were common (Δ = 0.57; 95% CI: 0.46–0.66). Future research on how arboreal lemurs navigate ground use in a multipredator landscape should include behavioral observations to better understand animal decision-making.
... For example, a restoration project initiated between 1994 and 1996 regenerated a forest fragment (23.5 ha) from an area of pasture and croplands in Peru; P. oenanthe was initially absent from the fragment, but, in 2010, a group of P. oenanthe was recorded there and, some years later, a total of 27 individuals were recorded with the density estimated at 35 groups/ km 2 and 124 individuals/km 2 (Allgas et al., 2017). Such results demonstrate the importance of ecological restoration projects for increasing the long-term viability of titi species and illustrate the capacity of titi monkeys to use ground-based access to colonize isolated forest areas (Souza-Alves et al., 2019b). Furthermore, long-term studies that document the effects of habitat loss and fragmentation on titi monkeys (Hutchinsonian and Raunkiaeran shortfalls) would enable us to understand how some populations are surviving in these heavily impacted areas. ...
Titi monkeys (Callicebus, Cheracebus, and Plecturocebus) comprise the most species-rich group of primates in South America. Thirty-six currently recognized species composing this group inhabit a multitude of habitats across most of South America. While field-based and laboratory research has provided insights into the behavior, ecology, and physiology of some titis, multiple knowledge gaps regarding their biodiversity patterns persist. Here, we provide an overview of titi research and identify their biodiversity knowledge shortfalls. Using online databases, we collated the literature of all titi studies published up to December 31, 2021. We compiled 521 publications, with 48% representing in situ field studies of the monkeys. The majority of field-based publications focused on studies conducted in Brazil and Peru. We found that research efforts have increased in recent decades, as indicated by the increased number of publications on titis. However, given the large number of species and their wide distribution across South America, there is limited information about most of these species and their geographic ranges. By highlighting the focal points where conservation-related data are still required, our findings demonstrate the importance of expanding research efforts and investment on the full extent of titi species and their entire geographic regions; doing so will help fill the knowledge shortfalls rather than solely advancing the study of a restricted range of topics in one or two habitats or countries. These advances will contribute to fill knowledge gaps through the creation/expansion of data repositories, citizen science programs, and increased financial support to maintain long-term data collection.
... First, as forest layers are expressed as percentage of canopy cover, we binarized these layers into forest and non-forest layers. Although some neotropical primates can perform specific activities at the ground level (Mourthé et al. 2007;Souza-Alves et al. 2019;Eppley et al. 2022), all Plathrrine monkeys are strictly arboreal, thus we followed previous studies and considered only areas where the tree cover was > 75% (Aleman et al. 2018;Vieilledent et al. 2018;Eppley et al. 2020). Then, we overlaid the geographic range areas with the binary forest maps to calculate the amount of forest habitat for each species. ...
Habitat fragmentation and overexploitation of natural resources are the most prevalent and severe threats to biodiversity in tropical forests. Several studies have estimated the effect of these threats on species extinction risk, however the effect resulting from their interaction remains poorly understood. Here, we assess whether and how habitat area, fragmentation, and hunting can synergistically affect the extinction risk of neotropical primates (Platyrrhine). We use a Random Forest model to estimate the Red List extinction risk category of 147 primate species based on their biological traits and the environmental predictors they are exposed to. We find that environmental variables are better predictors of extinction risk than biological traits, and that hunting and fragmentation interact creating synergistic feedback that lead to higher extinction risk than when considered in isolation. We also show that the effect of environmental predictors is mediated by biological traits, with large species being sensitive to habitat area and fragmentation, and frugivorous species more threatened by hunting. Our results increase the understanding of potentially interactive effects between different threats, habitat area and species traits, supporting the idea that multiple threats can reinforce each other and should be thus addressed simultaneously in conservation agendas.
... The phylogenetic and divergence time analyses of Byrne et al. (2016) resulted in the recommendation placing the titi monkeys into three genera, of which two were new, as follows: (1) Cheracebus Byrne et al. 2016 for the collared titi monkeys from the Amazon and Orinoco basins (the torquatus group of Hershkovitz 1990); (2) Plecturocebus Byrne et al. 2016, for the remaining species of the Amazon basin and the Chaco (the modestus, donacophilus and moloch groups, excepting C. personatus, of Hershkovitz 1990); and (3) Callicebus Thomas 1903, for the titis of the Atlantic forest and Caatinga of Brazil (the personatus group). This division has been largely accepted (e.g., Carneiro et al. 2018;Souza-Alves et al. 2019;Mammal Diversity Database 2022), although some authors have argued the use of subgenera rather than genera (e.g., Gutiérrez and Marinho-Filho 2017;Teta 2018). ...
The subfamily Callicebinae is composed of 35 recognized living species that are grouped into the genera, Callicebus, Plecturocebus, and Cheracebus. In this study we assess the taxonomic sta- tus of the population of Cheracebus from the Nanay-Tigre inter uvium in Peruvian Amazonia, based on morphological (cranial and pelage) and molecular (mitochondrial DNA) evidence. Following the integrated assessment of the evidence, we conclude that specimens from the Nanay-Tigre inter uvium comprise a distinct lineage at the species level. It is easily distinguished from the other species of the genus, including C. lucifer to which the new species was considered to belong so far, by, among other characters, overall Reddish-brown pelage; crown intense reddish brown; Cream-colored collar, like a bow tie, with a band that does not extend laterally. The description of a new species of Cheracebus is not unexpected since other new species of titi monkeys have been described in recent years and there are several candidate species awaiting validation of their distinction. As such, we anticipate that in the next few years several taxonomic changes will be proposed in order to reveal a classi cation that mirrors the real species diversity of the subfamily Callicebinae.
... Conversely, adaptations for predominantly terrestrial lifestyles are notably absent among living Platyrrhini of the Americas and Strepsirrhini of Africa (including Madagascar) and Asia (7,(12)(13)(14). However, some of these arboreal, diurnal primates periodically use the ground (15)(16)(17)(18)(19)(20)(21). ...
... Denser canopy cover was associated with spending less time on the ground within species, but was not associated with ground use in the between-species model. The former is in line with our expectation that terrestrial activity tends to be higher in habitats with sparser canopies, such as those disturbed by anthropogenic activities (19,38). Arboreal species in more open habitats (i.e., sparser canopies) may need to descend to the ground to forage and drink (19,34,38,73,74), although their ability to do so may be guided by species-specific characteristics acting as a predisposition (i.e., behavioral and anatomical exaptations) (75,76). ...
... The former is in line with our expectation that terrestrial activity tends to be higher in habitats with sparser canopies, such as those disturbed by anthropogenic activities (19,38). Arboreal species in more open habitats (i.e., sparser canopies) may need to descend to the ground to forage and drink (19,34,38,73,74), although their ability to do so may be guided by species-specific characteristics acting as a predisposition (i.e., behavioral and anatomical exaptations) (75,76). Primate species richness had contrasting results, with a negative effect on terrestriality in the interspecific model and positive effect in the intraspecific model. ...
Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestrial-ity is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arbo-real, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of fru-givory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Amer-icas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.
