Variation in fruit and seed dimensions is better explained by dispersal system than by leaf size in a tropical rainforest.

PREMISE: Variation in fruit and seed traits could originate from selection pressures exerted by frugivores or other ecological factors (adaptive hypotheses) and developmental constraints (by-product hypotheses) or chance. METHODS: We evaluated fruit and leaf traits for nearly 850 plant species from a rainforest in Tinigua Park, Colombia. Through a series of linear regressions controlling for the phylogenetic signal of the traits (minimum N = 542), we tested (1) whether the allometry between seed width and length depends on seed dispersal system (Mazer and Wheelwright's adaptive hypothesis of allometry for species dispersed in the guts of animals = endozoochory) and (2) whether fruit length is associated with leaf length (i.e., Herrera's by-product hypothesis derived from the assumption that both organs develop from homologous structures). RESULTS: We found a strong negative allometric association between seed width and length for seeds of endozoochorous species, as expected; but also, for anemochorous species. We found a positive relationship between fruit and leaf length, but this relationship was not evident for zoochorous species. Fruit size was highly correlated with seed size. CONCLUSIONS: The allometry between seed length and width varied among dispersal systems, supporting that fruit and seed morphology has been modified by interactions with frugivores and by the possibility to rotate for some wind dispersed species. We found some support for the hypothesis on developmental constraints because fruit and leaf size were positively correlated, but the predictive power of the relationship was low (10-15%).

PREMISA: La variación en los rasgos de frutos y semillas de las plantas podría tener su origen en las presiones de selección ejercidas por los frugívoros u otros factores ecológicos (hipótesis adaptativas), así como en limitaciones del desarrollo (hipótesis de subproductos) o en el azar. MÉTODOS: Nosotros evaluamos rasgos de frutos y hojas en cerca de 850 especies de plantas de un bosque húmedo tropical en el Parque Nacional Natural Tinigua, Colombia. Usando una serie de regresiones lineales que controlan por la señal filogenética de dichos rasgos (mínimo N = 542), nosotros probamos (1) si la alometría entre el ancho y largo de la semilla depende del sistema de dispersión de la semilla (i.e., hipótesis adaptativa de Mazer y Wheelwright; en la que se espera una alometría negativa para especies dispersadas por endozoocoria) y (2) si el largo del fruto está asociado con el largo de la hoja (i.e., la hipótesis del subproducto de Herrera derivada de la suposición de que ambos órganos se desarrollan a partir de estructuras homólogas). RESULTADOS: Nosotros encontramos una fuerte asociación alométrica negativa entre el ancho y el largo de las semillas para las semillas de las especies endozoócoras, como era de esperar; pero también, para las especies anemócoras. Nosotros también hallamos una relación positiva entre el largo del fruto y de la hoja, pero esta relación no fue evidente para las especies endozoócoras. Detectamos que el tamaño del fruto esta altamente correlacionado con el tamaño de la semilla. CONCLUSIONES: La alometría entre el largo y el ancho de la semilla varió entre sistemas de dispersión, lo que sugiere que la morfología de frutos y semillas ha sido moldeada por interacciones con frugívoros en el caso de las semillas endozoócoras y por la posibilidad de rotar para algunas especies dispersadas por el viento. Aunque el poder predictivo de la relación entre el tamaño del fruto y de la hoja fue bajo (10-15%), nosotros encontramos un apoyo moderado a la hipótesis sobre las limitaciones del desarrollo, ya que el tamaño del fruto y de la hoja estaban correlacionados positivamente.

Influence of Arthropod and Fruit Abundance on the Dietary Composition of Highland Colombian Woolly Monkeys (Lagothrix lagotricha lugens).

The woolly monkey's (Lagothrix lagotricha) diet consists primarily of fruits, and for some populations fruit availability predicts its frequency in the diet. Woolly monkeys also eat new leaves, flowers, seeds and arthropods, but it is unclear whether arthropods are consumed in proportion to their environmental availability. We tested the hypothesis that arthropod consumption by woolly monkeys depends on availability. We studied a group of woolly monkeys for 10 months in 2013-2014, in Cueva de los Guácharos National Park, Colombia, in order to test the hypothesis that arthropod consumption by woolly monkeys depends on availability. We carried out surveys of plant phenology each month for 10 months to estimate fruit productivity, and every 2 months we also surveyed 3 canopy substrates (leaves, mosses and bromeliads) to quantify variation in arthropod biomass. During this time, we also quantified the diet of a woolly monkey group. The items most consumed were fruits (60%), followed by arthropods (24%), leaves (13%) and miscellaneous other items (3%). Arthropod biomass in the canopy did not vary considerably over the 10 months (0.014-0.037 g/g substrate) but was lower at the end of the second rainy season. A positive correlation was found between availability and entomophagy, but only when arthropods were relatively abundant. We did not find a relationship between arthropod and fruit feeding frequencies. Our results indicate that arthropods are prevalent in the diet of the woolly monkeys due to their abundance in Andean forest canopies.

Thermophilization of adult and juvenile tree communities in the northern tropical Andes.

Climate change is expected to cause shifts in the composition of tropical montane forests towards increased relative abundances of species whose ranges were previously centered at lower, hotter elevations. To investigate this process of "thermophilization," we analyzed patterns of compositional change over the last decade using recensus data from a network of 16 adult and juvenile tree plots in the tropical forests of northern Andes Mountains and adjacent lowlands in northwestern Colombia. Analyses show evidence that tree species composition is strongly linked to temperature and that composition is changing directionally through time, potentially in response to climate change and increasing temperatures. Mean rates of thermophilization [thermal migration rate (TMR), °C ⋅ y(-1)] across all censuses were 0.011 °C ⋅ y(-1) (95% confidence interval = 0.002-0.022 °C ⋅ y(-1)) for adult trees and 0.027 °C ⋅ y(-1) (95% confidence interval = 0.009-0.050 °C ⋅ y(-1)) for juvenile trees. The fact that thermophilization is occurring in both the adult and juvenile trees and at rates consistent with concurrent warming supports the hypothesis that the observed compositional changes are part of a long-term process, such as global warming, and are not a response to any single episodic event. The observed changes in composition were driven primarily by patterns of tree mortality, indicating that the changes in composition are mostly via range retractions, rather than range shifts or expansions. These results all indicate that tropical forests are being strongly affected by climate change and suggest that many species will be at elevated risk for extinction as warming continues.

Specific gravity of woody tissue from lowland Neotropical plants: differences among forest types.

Wood density, or more precisely, wood specific gravity, is an important parameter when estimating aboveground biomass, which has become a central tool for the management and conservation of forests around the world. When using biomass allometric equations for tropical forests, researchers are often required to assume phylogenetic trait conservatism, which allows us to assign genus- and family-level wood specific gravity mean values, to many woody species. The lack of information on this trait for many Neotropical plant species has led to an imprecise estimation of the biomass stored in Neotropical forests. The data presented here has information of woody tissue specific gravity from 2,602 individual stems for 386 species, including trees, lianas, and hemi-epiphytes of lowland tropical forests in Colombia. This data set was produced by us collecting wood cores from woody species in five localities in the Orinoco and Magdalena Basins in Colombia. We found lower mean specific gravity values in várzea than in terra firme and igapó.

Environmental filtering of eudicot lineages underlies phylogenetic clustering in tropical South American flooded forests.

The phylogenetic community assembly approach has been used to elucidate the role of ecological and historical processes in shaping tropical tree communities. Recent studies have shown that stressful environments, such as seasonally dry, white-sand and flooded forests tend to be phylogenetically clustered, arguing for niche conservatism as the main driver for this pattern. Very few studies have attempted to identify the lineages that contribute to such assembly patterns. We aimed to improve our understanding of the assembly of flooded forest tree communities in Northern South America by asking the following questions: are seasonally flooded forests phylogenetically clustered? If so, which angiosperm lineages are over-represented in seasonally flooded forests? To assess our hypotheses, we investigated seasonally flooded and terra firme forests from the Magdalena, Orinoco and Amazon Basins, in Colombia. Our results show that, regardless of the river basin in which they are located, seasonally flooded forests of Northern South America tend to be phylogenetically clustered, which means that the more abundant taxa in these forests are more closely related to each other than expected by chance. Based on our alpha and beta phylodiversity analyses we interpret that eudicots are more likely to adapt to extreme environments such as seasonally flooded forests, which indicates the importance of environmental filtering in the assembly of the Neotropical flora.

Neotropical primate communities: Effects of disturbance, resource production and forest type heterogeneity.

Undisturbed primate communities in the Neotropics are bottom-up structured as their biomass and species richness can be predicted from fruit production. However, the effects of fruit scarcity and the availability of forest types have not been fully analyzed, and seasonality is expected to differently affect small and large monkeys. The first aim of this study was to examine the effect of contrasting forest types within a location on the temporal variation in fruit production. The second was to assess the relative roles of disturbance, climate, patterns of fruit and leaf production, and plant composition on determining Neotropical primate communities. I compiled population density data for diurnal primate species from 154 sites to calculate species richness and assemblage biomass. Fruit abundance in the study sites was estimated from fruit trap data and phenology transects, and fruit variability was calculated as the monthly coefficient of variation (CV) and the length of the fruit scarcity period (LFSP). The results indicate that fruit production in floodplain forests is generally more variable than in terra firme forests, and this variation decreases in habitats with mixed forest types. Endozoochorous fruit production (based on fruit traps) and litter productivity were good predictors of the biomass of Neotropical primates (R2 = 0.83 and R2 = 0.59, respectively), but neither CV nor LFSP were good predictors. The biomass of large primates was independent of rainfall variation, but the biomass of small and medium sized monkeys was negatively correlated with temporal rainfall variability. Varzea forests tended to show higher biomass than those from terra firme and igapó. These results suggest that the production of fleshy fruits is the best predictor of the structure of primate assemblages in the Neotropics, but the effect of leaf quality and productivity remains to be investigated. Am. J. Primatol. 78:391-401, 2016. © 2015 Wiley Periodicals, Inc.

A primer on the phylogeography of Lagothrix lagotricha (sensu Fooden) in northern South America.

The taxonomic history of the genus Lagothrix is complex, with molecular and morphological assessments giving conflicting results for the separation between its taxa. Phylogeographic studies of the most widely distributed species, Lagothrix lagotricha, have only been attempted recently and are limited to few individuals per collection site, many of which were captive making their geographical origin dubious. There is debate regarding the possibility of raising subspecies of Lagothrix lagotricha to the species level, therefore the geographical origin of samples is particularly relevant. In the present work we revisit the intraspecific phylogeography of L. lagotricha from northwestern South America, including the subspecies L. l. poeppiggi, L. l. lagotricha and L. l. lugens (sensu Fooden, 1963), using DNA sequence data from hypervariable region I of the mitochondrial control region (D-loop HVI). Our results suggest a complex picture in which there are well delimited evolutionary units that, nonetheless, do not correlate well with the morphological variation used to support the current delimitation of taxa. Additionally, we corroborate previous results showing a lack of reciprocal monophyly between the putative subspecies of Lagothrix lagotricha, and we propose that this may be due to ancestral polymorphism that has been maintained following the recent spread of woolly monkeys throughout the western Amazonian lowlands and into the inter-Andean region of Colombia.

Animal seed dispersal recovery during passive restoration in a forested landscape.

Seed dispersal by animals is key for restoration of tropical forests because it maintains plant diversity and accelerates community turnover. Therefore, changes in seed dispersal during forest restoration can indicate the recovery of species interactions, and yet these changes are rarely considered in forest restoration planning. In this study, we examined shifts in the importance of different seed dispersal modes during passive restoration in a tropical chronosequence spanning more than 100 years, by modelling the proportion of trees dispersed by bats, small birds, large birds, flightless mammals and abiotic means as a function of forest age. Contrary to expectations, tree species dispersed by flightless mammals dominated after 20 years of regeneration, and tree richness and abundance dispersed by each mode mostly recovered to old growth levels between 40 and 70 years post-abandonment. Seed dispersal by small birds declined over time during regeneration, while bat dispersal played a minor role throughout all stages of succession. Results suggest that proximity to old growth forests, coupled with low hunting, explained the prevalence of seed dispersal by animals, especially by flightless mammals at this site. We suggest that aspects of seed dispersal should be monitored when restoring forest ecosystems to evaluate the reestablishment of species interactions. This article is part of the theme issue 'Understanding forest landscape restoration: reinforcing scientific foundations for the UN Decade on Ecosystem Restoration'.

Diet of the critically endangered brown spider monkey (Ateles hybridus) in an inter-Andean lowland rainforest in Colombia.

Brown spider monkeys (Ateles hybridus) are one of the least known and more threatened primates in the Neotropics. Recognized as a species about a decade ago, field studies on these endangered primates have mainly focused on estimating local population densities. Since 2006, we habituated a group of wild brown spider monkeys at Serranía de Las Quinchas, Colombia, and studied their feeding ecology during 2.5 years using focal "subgroup" sampling, and conducted phenological surveys in order to estimate habitat-wide fruit availability. Based on 847 hr of behavioral follows, brown spider monkeys spent approximately 25% of their time in feeding activities, and fed from fruits and leaves on at least 123 plant species. Ripe fruits were the most important item in the diet of A. hybridus at Las Quinchas comprising 92% of their feeding time. Probably due to the minor variation in the monthly proportion of fruits in brown spider monkey's diet throughout this study, there was no relation between habitat-wide fruit availability and the proportion of fruit included in their monthly diet. The diet of brown spider monkeys at Las Quinchas is toward the high end of fruit intake, even within other wild spider monkeys' populations, suggesting that these endangered primates might also be facing the challenges of being a large bodied fruit specialist under a regional scenario of habitat loss and fragmentation.

Dietary preferences and feeding strategies of Colombian highland woolly monkeys.

Primates are very selective in the foods they include in their diets with foraging strategies that respond to spatial and temporal changes in resource availability, distribution and quality. Colombian woolly monkeys (Lagothrix lagotricha lugens), one of the largest primate species in the Americas, feed mainly on fruits, but they also eat a high percentage of arthropods. This differs from closely related Atelid species that supplement their diet with leaves. In an 11 month study, we investigated the foraging strategies of this endemic monkey and assessed how resource availability affects dietary selection. Using behavioural, phenological, arthropod sampling and metabarcoding methods, we recorded respectively foraging time, forest productivity, arthropod availability in the forest and arthropod consumption. Scat samples and capturing canopy substrates (i.e. moss, bromeliads, aerial insects) were used for assigning arthropod taxonomy. The most important resource in the diet was fruits (54%), followed by arthropods (28%). Resource availability predicted feeding time for arthropods but not for fruits. Further, there was a positive relationship between feeding time on fruits and arthropods, suggesting that eating both resources during the same periods might work as an optimal strategy to maximize nutrient intake. Woolly monkeys preferred and avoided some fruit and arthropod items available in their home range, choosing a wide variety of arthropods. Geometrid moths (Lepidoptera) were the most important and consistent insects eaten over time. We found no differences in the type of arthropods adults and juveniles ate, but adults invested more time foraging for this resource, especially in moss. Although woolly monkeys are generalist foragers, they do not select their food items randomly or opportunistically.

Continental-scale patterns of Cecropia reproductive phenology: evidence from herbarium specimens.

Plant phenology is concerned with the timing of recurring biological events. Though phenology has traditionally been studied using intensive surveys of a local flora, results from such surveys are difficult to generalize to broader spatial scales. In this study, contrastingly, we assembled a continental-scale dataset of herbarium specimens for the emblematic genus of Neotropical pioneer trees, Cecropia, and applied Fourier spectral and cospectral analyses to investigate the reproductive phenology of 35 species. We detected significant annual, sub-annual and continuous patterns, and discuss the variation in patterns within and among climatic regions. Although previous studies have suggested that pioneer species generally produce flowers continually throughout the year, we found that at least one third of Cecropia species are characterized by clear annual flowering behaviour. We further investigated the relationships between phenology and climate seasonality, showing strong associations between phenology and seasonal variations in precipitation and temperature. We also verified our results against field survey data gathered from the literature. Our findings indicate that herbarium material is a reliable resource for use in the investigation of large-scale patterns in plant phenology, offering a promising complement to local intensive field studies.

Pulp-seed attachment is a dominant variable explaining legitimate seed dispersal: a case study on woolly monkeys.

Seed dispersal is a mutualistic interaction in which frugivores gain nutrients and plants gain when seeds are transported to adequate places for establishment. However, this relationship is prone to deceit, for example, when frugivores spit-out seeds in the proximity of parental trees. Still, few hypotheses have offered explanations on why deceiving strategies are not widespread. In this study, I explore the importance of how difficult it is to mechanically separate the nutritious pulp from the seeds, as a factor that can explain the chance a seed has of being dispersed by woolly monkeys (Lagothrix lagothricha). I completed 1,440 h of focal animal follows during 2 years in order to quantify the chances plant species have of being dispersed. To do so, I evaluated the residuals from the relationship between the number of seeds manipulated and seeds dispersed by a population of woolly monkeys in Tinigua Park (Colombia). For 74 fruit species, I estimated how difficult it is to separate pulp from seeds as the time needed to separate the parts. An exponential model showed that this variable was able to predict 38% of the variation on dispersal probability, demonstrating that, when it is difficult to separate the pulp from the seeds, the probability of legitimate dispersal increases. However, when fruit parts were easy to separate, there was more variation in the outcome. My results suggest that many plants have evolved mechanisms (e.g., small seeds embedded in pulp, strong attachment, irregular seed surface, and thin pulp layer) that preclude deceit by frugivores.

Use of space, activity patterns, and foraging behavior of red howler monkeys (Alouatta seniculus) in an Andean forest fragment in Colombia.

Howler monkeys are among the most studied primates in the Neotropics, however, behavioral studies including estimation of food availability in Andean forests are scarce. During 12 months we studied habitat use, behavior, and feeding ecology of two groups of red howler monkeys (Alouatta seniculus) in an isolated fragment in the Colombian Andes. We used a combination of focal animal and instantaneous sampling. We estimated fruit production (FP) using phenology transects, and calculated young leaf abundance by observing marked trees. The home range area used by each group was 10.5 and 16.7 ha and daily distances traveled were 431 ± 228 and 458 ± 259 m, respectively. We found that both groups spent most of their time resting (62-64%). Resting time did not increase with leaf consumption as expected using a strategy of energy minimization. We did not find a relationship between daily distances traveled and leaf consumption. However, howlers consumed fruits according to their availability, and the production of young leaves did not predict feeding time on this resource. Overall, our results are similar to those found on other forest types. We found that despite limited FP in Andean forests, this did not lead to a higher intake of leaves, longer resting periods, or shorter traveling distances for red howlers.

A new hypothesis for the importance of seed dispersal in time.

Most studies on seed dispersal in time have focused on seed dormancy and the physiological triggers for germination. However, seed dispersed by animals with low metabolic and moving rates, and long gut-passage times such as terrestrial turtles, could be considered another type of dispersal in time. This study tests the hypothesis that seeds dispersed in time may lower predation rates. We predicted that seeds deposited below parent trees after fruiting fall has finished is advantageous to minimize seed predators and should show higher survival rates. Four Amazonian plant species, Dicranostyles ampla, Oenocarpus bataua, Guatteria atabapensis and Ocotea floribunda, were tested for seed survival probabilities in two periods: during fruiting and 10-21 days after fruiting. Experiments were carried out in two biological stations located in the Colombian Amazon (Caparú and Zafire Biological Stations). Seed predation was high and mainly caused by non-vertebrates. Out of the four plant species tested, only Guatteria atabapensis supported the time escape hypothesis. For this species, seed predation by vertebrates after the fruiting period increased (from 4.1% to 9.2%) while seed predation by non-vertebrates decreased (from 54.0% to 40.2%). In contrast, seed predation by vertebrates and by non-vertebrates after the fruiting period in D. ampla increased (from 7.9% to 22.8% and from 40.4% to 50.6%, respectively), suggesting predator satiation. Results suggest that for some species dispersal in time could be advantageous to avoid some type of seed predators. Escape in time could be an additional dimension in which seeds may reach adequate sites for recruitment. Thus, future studies should be address to better understand the survival advantages given by an endozoochory time-dispersal process.

Phenology, seed dispersal and difficulties in natural recruitment of the canopy tree Pachira quinata (Malvaceae).

Life history and recruitment information of tropical trees in natural populations is scarce even for important commercial species. This study focused on a widely exploited Neotropical canopy species, Pachira quinata (Malvaceae), at the southernmost, wettest limit of its natural distribution, in the Colombian Amazonia. We studied phenological patterns, seed production and natural densities; assessed the importance of seed dispersal and density-dependent effects on recruitment, using field experiments. At this seasonal forest P. quinata was overrepresented by large adult trees and had very low recruitment caused by the combination of low fruit production, high seed predation and very high seedling mortality under continuous canopies mostly due to damping off pathogens. There was no evidence of negative distance or density effects on recruitment, but a clear requirement of canopy gaps for seedling survival and growth, where pathogen incidence was drastically reduced. In spite of the strong dependence on light for survival of seedlings, seeds germinated readily in the dark. At the study site, the population of P. quinata appeared to be declining, likely because recruitment depended on the rare combination of large gap formation with the presence of reproductive trees nearby. The recruitment biology of this species makes it very vulnerable to any type of logging in natural populations.

Oilbirds disperse large seeds at longer distance than extinct megafauna.

The extinction of megafauna in the Neotropics is thought to have reduced the potential of large seeds to be dispersed over long distances by endozoochory (ingestion by animals), but some seed dispersal systems have not been considered. We describe the role of oilbirds (Steatornis caripensis) as seed dispersers, in terms of seed width and dispersal distance (using GPS tracking devices), and we compare with data reported for other animals. Oilbirds dispersed seeds up to 29 mm wide, with a mean dispersal distance of 10.1 km (range 0-47.6 km). Some components of seed dispersal by oilbirds are outliers compared to that of other frugivores, such as the relationship between maximum seed width and body weight (however, few other extant specialized frugivores are also outliers). Estimates of mean dispersal distance by oilbirds are the largest reported, and we confirm that some living frugivores currently fulfil roles of seed dispersers and ecosystem services previously assumed to be only performed by extinct species.

Monitoring the variation in the gut microbiota of captive woolly monkeys related to changes in diet during a reintroduction process.

Microbiome is known to play an important role in the health of organisms and different factors such as diet have been associated with modifications in microbial communities. Differences in the microbiota composition of wild and captive animals has been evaluated; however, variation during a reintroduction process in primates has never been reported. Our aim was to identify changes in the bacterial composition of three individuals of reintroduced woolly monkeys (Lagothrix lagothricha) and the variables associated with such changes. Fecal samples were collected and the V4 region of the 16S rRNA gene was sequenced to determine gut microbial composition and functionality. Individual samples from released individuals showed a higher microbial diversity after being released compared to before liberation, associated with changes in their diet. Beta diversity and functionality analysis showed separation of samples from released and captive conditions and the major factor of variation was the moment of liberation. This study shows that intestinal microbiota varies depending on site conditions and is mainly associated with diet diversity. The intake of food from wild origin by released primates may promote a positive effect on gut microbiota, improving health, and potentially increasing success in reintroduction processes.

Nutrient transport within and between habitats through seed dispersal processes by woolly monkeys in north-western Amazonia.

The contribution of vertebrate animals to nutrient cycling has proven to be important in various ecosystems. However, the role of large bodied primates in nutrient transport in neotropical forests is not well documented. Here, we assess the role of a population of woolly monkeys (Lagothrix lagothricha lugens) as vectors of nutrient movement through seed dispersal. We estimated total seed biomass transported by the population within and between two habitats (terra firme and flooded forests) at Tinigua Park, Colombia, and quantified potassium (K), phosphorus (P) and nitrogen (N) content in seeds of 20 plant species from both forests. Overall, the population transported an estimated minimum of 11.5 (±1.2 SD) g of potassium, 13.2 (±0.7) g of phosphorus and 34.3 (±0.1) g nitrogen, within 22.4 (±2.0) kg of seeds ha(-1) y(-1). Approximately 84% of all nutrients were deposited in the terra firme forest mostly through recycling processes, and also through translocation from the flooded forest. This type of translocation represents an important and high-quality route of transport since abiotic mechanisms do not usually move nutrients upwards, and since chemical tests show that seeds from flooded forests have comparatively higher nutrient contents. The overall contribution to nutrient movement by the population of woolly monkeys is significant because of the large amount of biomass transported, and the high phosphorus content of seeds. As a result, the phosphorus input generated by these monkeys is of the same order of magnitude as other abiotic mechanisms of nutrient transport such as atmospheric deposition and some weathering processes. Our results suggest that via seed dispersal processes, woolly monkey populations can contribute to nutrient movement in tropical forests, and may act as important nutrient input vectors in terra firme forests.

How many species of woolly monkeys inhabit Colombian forests?

There is a controversy regarding how many species the genus Lagothrix contains, since the Lagothrix lagothricha subspecies have been recently proposed to be actual species. Clarification of species status is of particular importance in the case of L. l. lugens, because it is the most endangered and its distribution is restricted to the Colombian Andes, a highly deforested region. Using cytogenetic and molecular markers, we obtained evidence indicating that the subspecies status is appropriate for the two taxa occurring in this country. We also report high levels of intraspecific variability in the karyotype. We find evidence for a late Pleistocene separation of the subspecies, and we propose it is the limited area of contact between the taxa that allowed for them to partially differentiate.

Correction to: Review of GPS collar deployments and performance on nonhuman primates.

In the original publication of the article, figure 1 was wrongly published as a duplication.