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Example of C. aurita hybrids with “koala bear” appearance. Whole genome analysis suggests that individuals in (a) and (b) are likely triple C. aurita × C. penicillata × C. jacchus hybrids (J. Malukiewicz unpubl. data). These are captive hybrids were photographed at the Guarulhos Zoo, state of São Paulo. Photo: J. Malukiewicz.
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Natural and anthropogenic hybridization both occur in primates, but the effects of these distinct processes on primate evolution and population dynamics can be difficult to disentangle from one another. With most primate species being endangered, conservation prioritizes natural over anthropogenic hybrids. However, anthropogenic hybridization can g...
Citations
... It was considered Endangered for over 30 years (Hannibal et al., 2019) until it was classified as Critically Endangered since 2020 (de Melo, Hilário, et al., 2021). Its presence on the list of threatened species is due to (1) intensive deforestation across the states of Minas Gerais (MG) and Espírito Santo (ES) (Hirsch et al., 1999), (2) climate change, resulting in dryer and warmer climate within the species range (Carlucci et al., 2021;Townsend, 2008), (3) yellow fever outbreaks, which have highly affected Callithrix populations across the states of ES andMG in 2017 (Mares-Guia et al., 2020;Possamai et al., 2022) and (4) invasive species (especially C. jacchus and C. penicillata) leading to hybridisation between Callithrix species (Braz et al., 2019;Malukiewicz, 2019;Moraes et al., 2019). ...
Endemic to the Atlantic Forest in Southeastern Brazil, the critically endangered Buffy-Headed marmoset (Callithrix flaviceps) is lacking the required attention for effective conservation. We modelled its ecological niche with the main objectives of (1) defining suitable habitat and (2) prioritising areas for conservation and/or restoration. The current geographical range of Callithrix flaviceps in the Atlantic Forest of Southeast Brazil. We used Ensemble Species Distribution Modelling to define current habitat suitability considering four climate and two landscape variables. To identify areas to prioritise for conservation and/or restoration, we predicted future habitat suitability considering the intermediate (RCP4.5) and extreme (RCP8.5) climate change scenarios for the years 2050 and 2070. Among the variables included to predict current species distribution, tree canopy cover, precipitation seasonality and temperature seasonality were the most important whereas digital elevation model and precipitation during the wettest month were the least important. Callithrix flaviceps was most likely to occur in areas with tree canopy cover >80%, high precipitation seasonality and temperature seasonality between 21 and 23°C. From the future suitability prediction maps, the Caparaó National Park stands out as a likely key area for the preservation of the species. Furthermore, high climatic suitability but low landscape suitability suggests that habitat restoration in 'Serra das Torres' (South of the current distribution area) might be a useful strategy. However, creating ecological corridors on the west side of Caparaó would be necessary to improve connectivity. More surveys within and beyond the current geographical range are required to define more precisely the distribution of the species. Our results support the notion that seasonality is important for Callithrix flaviceps and that as a montane species, it prefers colder environments and higher altitudes. Within both climate change scenarios, Caparaó National Park was predicted to be highly suitable, with a high probability of presence.
... The marmosets in this region are hybrids of two species (Callithrix jacchus and C. penicillata) introduced as a consequence of the illegal wildlife trade (Malukiewicz, 2018;Malukiewicz et al., 2020;Ruiz-Miranda et al., 2000). They are considered a threat to the population of golden lion tamarins because of the potential for disease transmission and competition for resources (Kierulff et al., 2012;Malukiewicz et al., 2020;Ruiz-Miranda et al., 2006, 2019. ...
The conservation of endangered primates often relies on data on population dynamics and health obtained from individuals captured with baited traps. This could increase the risk of injury or predation by attracting competitors and predators to the baited locations. It also can lead to unforeseen interactions of ecological significance among nontarget species. We evaluated these hypotheses by monitoring visits by multiple species to capture platforms for endangered golden lion tamarins (Leontopithecus rosalia). We placed camera traps on ten platforms baited with bananas resulting in more than 1500 species records. We calculated species richness and temporal patterns of visitation overlap among lion tamarins, predators, and competitor species. We also fitted a lion tamarin group with a GPS telemetry transmitter to assess whether movements toward and visits to the platform occurred more than expected by chance. Thirteen mammals and 12 bird species visited the platforms. There was high temporal overlap, albeit with peaks at different times, with the tayra (Eira barbara)—a main predator. Introduced hybrid marmosets (Callithrix spp.) were present on the platforms in 42% of visits by lion tamarins, and we recorded fights between the two species. There was significant temporal overlap between lion tamarins and capuchin monkeys. The lion tamarin visitation rate to platforms did not differ from random locations, nor did they show significant recursive behavior. Lion tamarins were vigilant in 90% of platform visits and emitted mild alarm calls, mobbing calls, and food calls. Their vocal output increased when marmosets were on the platforms. We suggest that lion tamarins consider the platforms an attractive, albeit risky, food resource. Baited platforms attract species beyond the target species and create conditions for unintended potentially negative effects on multiple species.
... The reintroduction of trafficked individuals from non-native primate species could lead to hybridization and threaten the conservation of other primate species native to the release site. An example of hybridization related to the illegal pet trade is the case of marmosets (Callithrix sp.) in Brazil (Beck, 2018;Malukiewicz, 2019). Some marmosets are native to the Atlantic rainforest in southeastern Brazil, such as the buffy-tufted-ear marmoset (Callithrix aurita) and the buffy-headed marmoset (Callithrix flaviceps). ...
... Other marmoset species, namely black-tufted marmosets (Callithrix penicillata) and common marmosets (Callithrix jacchus) are native to the northeast of Brazil and are frequently traded illegally. Hybridization has resulted after escape during transport and abandonment of trafficked individuals (i.e., individuals kept as pets and abandoned by their "owners" in local areas) from these northeastern species in southeastern Brazil and subsequent mixing with Callithrix species native to this area or between nonnative Callithrix species (Beck, 2018;Malukiewicz, 2019). This has led to the establishment of hybrid populations who are phenotypically and genetically different from their parental species (Malukiewicz, 2019). ...
... The effects of hybridization are not clear, and it can lead to positive or negative consequences for reproduction and survival (Palmer, 2020;Palmer et al., 2021). Marmoset hybrids, potentially, could have increased fitness because of genetic adaptation and novelty, but hybridization also could lead to further endangerment of already threatened marmoset species if hybrid offspring are less viable or fit than their parental species (Malukiewicz, 2019). ...
The illegal primate trade is one of the major drivers of the decline of nonhuman primate populations and a threat to their wellbeing. Thousands of trafficked primates enter rescue centers every year, and their destiny (release back into the wild, long-term captivity, or euthanasia) involves controversial decisions and complex ethical considerations. To navigate these issues, we developed an ethical matrix, an ethical framework previously used to address conservation-related issues. We gathered information from studies on the reintroduction of trafficked platyrrhines in Latin America from 1990 to 2022 to develop the matrix. We found 22 studies performed in eight Latin American countries, which included howler monkeys, spider monkeys, woolly monkeys, capuchin monkeys, squirrel monkeys, marmosets, and tamarins. We found that the reintroduction of trafficked platyrrhines may yield positive results for the welfare of individuals and for the conservation of their taxa and some of the potential negative effects, such as spillover of infectious agents to free-ranging populations or to human populations, or competition for resources between reintroduced monkeys and resident conspecifics have not yet been documented in the scientific literature, although this does not mean that they do not occur. We conclude that the ethical matrix is a useful method to consider the interests of all potential stakeholders and that the reintroduction of trafficked primates may be a viable management option if the individual welfare of the animals is considered, programs comply with the IUCN and government guidelines, and the objective and justification of the reintroduction are clear.
... Compared to other primates, marmosets are more generalist in their behavior, which can lead to ecological impacts when they are introduced or relocated. These impacts may include competition with native species (Ruiz-Miranda et al., 2006), predation on small vertebrates and eggs (Alexandrino et al., 2012;Begotti and Landesmann, 2008;Galetti et al., 2009), and hybridization with other species of the genus Callithrix (Malukiewicz, 2019). The black-tufted marmoset (C. ...
The introduction of species in areas with no top-down control is a recipe for ecosystem catastrophe. Theory predicts that introduced species in areas that lack predators may experience rapid growth and subsequently crash or stabilize around the carrying capacity. Impressively, there are very few studies on the population trend of tropical forest-dwelling mammals. In 1983, 100 individuals from 15 species of generalist mammals were introduced on an 828-ha tropical island in Southeast Brazil (Anchieta Island). Here, we present the status and population dynamics of the introduced species after 19, 21, 35, 38, and 39 years based on 611 km of line transects split into diurnal and nocturnal surveys. Among the introduced species, five were extinct and two species became super-abundant. The population of agouti has been fluctuating around 900 individuals and black-tufted marmoset around 600 individuals which may reflect the carrying capacity of the island. Our results showed that a tropical island, without top predators, resulted in a massive population explosion of 2 of the 15 introduced mammals, demonstrating that colonization and invasion processes are not straightforward to predict.
... Hybridization is most important when it results from the spread of an invasive species, usually caused by human activity, such as animal trade or habitat disturbance, leading to non-sympatric species being in contact with each other. Among the primates of the Callithrix genus, besides causing habitat displacement and engaging in competition for resources (Melo et al. 2020), invasive species threaten native ones due to the possibility of hybridization that produces fertile descendants (Malukiewicz 2019), possibly resulting in the loss of the pure gene pool of the native species. Using the mtDNA control region, Malukiewicz et al. (2014) found different patterns of hybrid formation between anthropogenic and natural zones. ...
Molecular techniques have emerged as powerful tools to study ecological aspects of biodiversity. As a result, the interdisciplinary field of Molecular Ecology was created, combining a wide range of strategies in order to address ecological questions, which may involve molecular species confirmation, species occurrence and distribution, demography estimates, relatedness among individuals, intra and interspecific interactions, dispersal patterns, sex ratio, as well as other ecological information. In this chapter, we provide an overview of how molecular techniques have been contributing to answering ecological questions about neotropical mammals, using various sources of biological samples (including non-invasive sampling) and the most appropriate molecular markers to achieve each objective. Mammals constitute one of the most threatened taxa due to the direct and indirect environmental effects of human activity, and therefore ecological information must be obtained about this group for the proposal of conservation strategies.KeywordsSpecies monitoringMitochondrial DNAMicrosatellitesSex identificationPhilopatry
... Callithrix aurita is an endemic species from the Atlantic Forest and occurs in inland and altitudinal forests (up to 1300 m) in the southernmost limit of the natural range distribution of the genus (Ferrari et al. 1996;Melo et al. 2021). Nowadays, C. aurita co-occurs with two other (invasive) Callithrix species: Callithrix penicillata, a parapatric species with C. aurita, which was introduced in allochthonous areas, but that has also expanded its natural distribution to new adjacent areas along with anthropogenic landscape changes (Vale et al. 2020;Carvalho et al. 2018;Malukiewicz 2019); and Callithrix jacchus, which was brought by humans from the northeastern region of Brazil . The main cause for the introduction of C. jacchus in allochthonous areas is the illegal pet trade Silva et al. 2018;Malukiewicz 2019). ...
... Nowadays, C. aurita co-occurs with two other (invasive) Callithrix species: Callithrix penicillata, a parapatric species with C. aurita, which was introduced in allochthonous areas, but that has also expanded its natural distribution to new adjacent areas along with anthropogenic landscape changes (Vale et al. 2020;Carvalho et al. 2018;Malukiewicz 2019); and Callithrix jacchus, which was brought by humans from the northeastern region of Brazil . The main cause for the introduction of C. jacchus in allochthonous areas is the illegal pet trade Silva et al. 2018;Malukiewicz 2019). Such trade seems to be facilitated by the presence of roads that allow the access to the areas where animals can be captured and also their transport (Malukiewicz et al. 2020). ...
Habitat loss, fragmentation and invasive species are the major causes of biodiversity loss. In the Atlantic Forest, Callithrix aurita is threatened by habitat modification and the invasion of Callithrix jacchus. We evaluated how landscape variables and a local one, the distance to the roads, influence the presence of the native and invasive species within the distribution range of the native. For that, we retrieved data on the presence of C. aurita and C. jacchus from published papers. Comparing species, C. aurita occurs in higher altitudes and lesser urbanized areas than C. jacchus. In presence modeling, the probability of presence of the native C. aurita was higher within deforested landscapes with intense road traffic, while the presence of the invasive species, C. jacchus, was increased in urbanized areas, mostly in non-mountainous terrain, confirming its generalist habits. If such results are not related to biased detectability, C. aurita are living in suboptimal areas, and probably should be more affected by the presence of invasive species. These opposite characteristics of the species highlighted some regions in which conservation measures should be guided, where C. aurita is probably more present and the negative influence of C. jacchus is still limited.
... Callithrix jacchus is native to Northeast Brazil ( Figure S1), occurring mainly in the Caatinga ecoregion, whereas C. penicillata is native to Central Brazil, occurring mainly in the Cerrado ecoregion (Rylands et al., 2009). C. jacchus and C. penicillata are the most trafficked Brazilian marmosets (Malukiewicz, 2019). They are commonly kept as pets and are often released into urban forest patches, with successful habitat invasion in many states of South and Southern Brazil, facilitated by long-term Atlantic Forest disturbance (Malukiewicz, 2019;Pinto and Voivodic, 2021). ...
... C. jacchus and C. penicillata are the most trafficked Brazilian marmosets (Malukiewicz, 2019). They are commonly kept as pets and are often released into urban forest patches, with successful habitat invasion in many states of South and Southern Brazil, facilitated by long-term Atlantic Forest disturbance (Malukiewicz, 2019;Pinto and Voivodic, 2021). In these regions, C. jacchus and C. penicillata have become sympatric to other marmoset species, such as the buffy-tufted-ear marmoset, C. aurita, an endangered species facing habitat destruction and population declines (Malukiewicz 2019;Nogueira et al., 2022;Malukiewicz et al., 2014Malukiewicz et al., , 2015Silva et al., 2018). ...
... They are commonly kept as pets and are often released into urban forest patches, with successful habitat invasion in many states of South and Southern Brazil, facilitated by long-term Atlantic Forest disturbance (Malukiewicz, 2019;Pinto and Voivodic, 2021). In these regions, C. jacchus and C. penicillata have become sympatric to other marmoset species, such as the buffy-tufted-ear marmoset, C. aurita, an endangered species facing habitat destruction and population declines (Malukiewicz 2019;Nogueira et al., 2022;Malukiewicz et al., 2014Malukiewicz et al., , 2015Silva et al., 2018). Because reproductive isolation is not complete in Callithrix, C. jacchus, C. penicillata and C. aurita can successfully produce fertile hybrids, which represent a challenge to C. aurita conservation (Nogueira et al., 2022;Malukiewicz, 2019). ...
Callithrix jacchus and C. penicillata have successfully established anthropogenic introduced populations throughout Rio de Janeiro state, where the endangered buffy-tufted-ear marmoset, Callithrix aurita, naturally occurs. These three species can produce fertile hybrids, which represent a challenge to C. aurita conservation. Callithrix anthropogenic hybrids show an overall increase in phenotypic variation and in genetic diversity in relation to parental populations and can also form hybrid swarms. Here, we examined ear tuft variation, cranial morphometrics and mitochondrial DNA sequences in three marmoset species (C. jacchus, C. penicillata and C. aurita) and their hybrids from anthropogenic environments in several localities of Rio de Janeiro state. Our data suggest that the sample evaluated is mostly composed of hybrids of C. jacchus and C. penicillata, excepted by one individual which has C. aurita ancestry. The phenotypes of hybrids were highly variable, with six external morphotypes varying from intermediate to parental-like. Cranial morphometric analyses revealed a mosaic of parental traits in hybrids, although there were some transgressive traits, while molecular analyses indicate higher genetic diversity among hybrids relative to parental species. No clear geographical association was found in relation to hybrid distribution, with the hybrid haplotypes occurring randomly throughout Rio de Janeiro state.
... In this context, this work aimed to evaluate whether landscape elements, such as patch attributes and the occurrence of allochthonous congeneric species, influence the occurrence of C. aurita within its distribution. We hypothesized that the probability of occurrence of C. aurita would be: (1) positively influenced by forest fragment altitude, area, connectivity, and distance to allochthonous species (Arroyo-Rodríguez & Mandujano, 2009;Carvalho et al., 2018;Corrêa et al., 2000;Malukiewicz, 2019;Palacios, 2018;Rylands & Faria, 1993); ...
... The Callithrix genus speciation is relatively recent, which enables hybridization and some natural hybrid zones (Malukiewicz, 2019). ...
... Furthermore, there is a major knowledge gap about C. aurita's ability to disperse in different types of matrices. In addition, management, for the control, removal, or another type of strategy specific to each location, of allochthonous species in protected areas is essential for the successful conservation of the genetic integrity of C. aurita in situ(Carvalho et al., 2018;ICMBio/MMA, 2018;Malukiewicz, 2019;Moraes et al., 2019). Finally, it is worth noting that for some variables, such as those associated with large estimates of confidence intervals (e.g., nonvegetated areas matrix and savanna formation matrix), more data collection (i.e., species registers) is necessary to increase their strength of inference on whether or not they influence the species occurrence.Based on the results, we suggest actions that could be integrated into the PAN PPMA, such as monitoring C. aurita populations, in order to expand knowledge and update data on the occurrence and environmental predictors of the species (ICMBio/MMA, 2018). ...
The buffy-tufted-ear marmoset (Callithrix aurita) is a small primate endemic to the Brazilian Atlantic Forest biome, and one of the 25 most endangered primates in the world, due to fragmentation, loss of habitat, and invasion by allochthonous Callithrix species. Using occurrence data for C. aurita from published data papers, we employed model selection using Akaike Information Criterion corrected for small samples and cumulative AICc weight (w +) to evaluate whether fragment size, distance to fragments with allochthonous species, altitude, connectivity, and surrounding matrices influence the occurrence of C. aurita within its distributional range. Distance to fragments with C. jacchus (w + = 0.94) and nonvegetated areas (w + = 0.59) correlated negatively with C. aurita occurrence. Conversely, the percentage of agriculture and pasture mosaic (w + = 0.61) and the percentage of savanna formation (w + = 0.59) in the surrounding matrix correlated positively with C. aurita occurrence. The findings indicate that C. aurita is isolated in forest fragments surrounded by potentially inhospitable matrices, along with proximity of a more generalist and invasive species, thereby increasing the possibility of introgressive hybridization. The findings also highlighted the importance of landscape elements and allochthonous congeneric species for C. aurita conservation, besides indicating urgency for allochthonous species management. Finally, the approach used here can be applied to improve conservation studies of other endangered species, such as C. flaviceps, which is also endemic to the Brazilian Atlantic Forest and faces the same challenges.
... exudivory), facial and overall body pelage patterns and coloration, and peri-auricular ear-tuft shape and color [24]. While natural hybridization occurs between certain pairs of Callithrix species under secondary contact at species range boundaries, anthropogenic hybridization has dramatically increased between several species over the last few years as a result of the illegal pet trade [23,24,25]. ...
... Using the approach developed in Fuzessy et al. [32], marmoset facial markings and pelage characteristics were used to phenotypically differentiate between species and hybrids. Defining facial and pelage characteristics from each species and hybrid type were based on published descriptions [27,32,31,34,25] and personal observations by JM and CSI. Facial landmarks used to assign sampled individuals to species are shown in Supplementary Figure S1. ...
... Facial landmarks used to assign sampled individuals to species are shown in Supplementary Figure S1. Phenotypes of hybrids classified as C. aurita hybrids suggest that these individuals possess ancestry from C. aurita and at least one species from the jacchus group [25,34]. Previous phylogenetic analysis of mitogenomic haplotypes assigned to a subset of C. aurita hybrids used in our sample also support C. aurita x jacchus group ancestry in these individuals (BJT024/C. ...
Background
Hybrids are expected to show greater phenotypic variation than their parental species, yet how hybrid phenotype expression varies with genetic distances in closely-related parental species remains surprisingly understudied. Here we study pelage and morphometric trait variation in anthropogenic hybrids between four species of Brazilian Callithrix marmosets, a relatively recent primate radiation. Marmoset species are distinguishable by pelage phenotype and level of morphological specialization for eating tree exudates. Here, we (1) describe qualitative phenotypic pelage differences between parental species and hybrids; (2) test whether significant quantitative differences exist between parental and hybrid morphometric phenotypes; and (3) determine which hybrid morphometic traits show heterosis, dysgenesis, trangression, or intermediacy relative to the parental trait. For morphometric traits, we investigated both cranial and post-cranial traits, particularly as most hybrid morphological studies focus on the former instead of the latter. Finally, we estimate mitogenomic distances between marmoset species from previously published data.
Results
Hybrid facial and overall body pelage variation reflected coloration and patterns seen in parental species. In morphometric traits, C. jacchus and C. penicillata were the most similar to each other, while C. aurita was the most distinct, and C. geoffroyi trait measures fell between these other species. Most traits in C. jacchus x C. penicillata hybrids showed either heterosis or were intermediate relative to the parental trait values. We observed heterosis and dygenesis in traits of C. penicillata x C. geoffroyi hybrids. Trangressive segregation was observed in hybrids of C. aurita and the other species. These hybrids were also C. aurita -like for a number of traits. Genetic distance was closest between C. jacchus and C. penicillata and farthest between C. aurita and the other species.
Conclusion
We attributed significant phenotypic differences between marmoset species to differences in morphological exudivory specialization in these species. Our results suggest that intermediate hybrid traits relative to the parental trait values are more likely in crosses between species with relatively lesser genetic distance. More extreme phenotypic variation is more likely in parental species with greater genetic distance, with transgressive traits appearing in hybrids of the most genetically distant parental species. We further suggest that that less developmental disturbances can be expected in hybrids of more recently diverged parental species.
... In Brazil, common marmosets occur within three major Brazilian biomes: the scrub-brush and semi-arid Caatinga, the semiarid savanna-like Cerrado, and the humid-coastal Atlantic Forest [1,3]. Marmosets are also known to hybridize, both under free-ranging and captive conditions, with the majority of cases involving C. jacchus as one of the parental species [1,[4][5][6]. Brazilian free-ranging populations of common marmosets are declining [7], and marmosets for biomedical use are difficult to import under international wildlife trade regulations [2]. Given the limited marmoset supply outside of Brazil, uncovering the phylogeny, ancestral biogeographic origins, and hybrid status of captive marmosets is critical for their biomedical use. ...
... This facility is located at the natural border between the natural geographic ranges of C. jacchus and C. penicillata where a natural hybrid zone exists [4]. However, the two species are also frequently captured illegally, interbred, and kept as pets in Brazil [1,5]. ...
... However, there is phenotypic evidence of possible Callithrix jacchus x C. penicillata hybrids present among marmosets kept in US biomedical facilities (personal observation, Malukiewicz). Additionally, previous mtDNA genetic studies show that cryptic hybridization in the wild does seem to occur regularly within the Callithrix genus [4][5][6]9]. ...
Marmosets, especially Callithrix jacchus, are becoming valuable, high-demand biomed-ical models but their supply outside of their native Brazil is limited. Thus, uncovering the ancestry and biogeographic origins of captive marmosets is an essential task to optimize their biomedical use. Such information facilitates assessing standing levels of captive marmoset genetic diversity, identifying hybrids, and maintaining genetic diversity of captive marmoset populations. Here, we present 16 newly sequenced mitochondrial genomes from marmosets with C. jacchus phenotypes from international biomedical and animal supply facilities. We combine these new data with publicly available sequences * Corresponding author. 1 Marmoset mtDNA 2 to compare usage of mitogenome and the mtDNA control region for determining the ancestry and diversity of captive marmosets. MtDNA control region and mitogenome haplotypes from all 16 newly sequenced marmosets grouped within C. jacchus phylo-genetic clades. Overall, phylogenies based on mitogenomes rather than the control region showed better resolved branching patterns with stronger statistical support within C. jacchus clades. However, both mtDNA markers show that C. jacchus is the sister clade to the phylogenetic C. penicillata Caatinga biome clade. Callithrix jacchus mtDNA control region haplotypes showed the highest haplotype and nucleotide diversity, and were intermediate in terms of per sequence theta and polymorphic sites. The larger number of available Callithrix mtDNA control region sequences relative to mitogenomes was used to determine ancestral mtDNA haplotype biogeographic origins. However, biogeographic origins for many C. jacchus haplotypes including those from international captive facilities could not be determined, which we attributed to unknown provenance information from natural C. jacchus populations. Given our results, we encourage increased sampling and genomic sequencing efforts for natural C. jacchus populations in Brazil, and utilizing the mitogenome over other mtDNA markers for phylogenetic-based analyses. Further, combining marmoset mitogenomic data with phenotypic and nuclear genomic data will greatly enhance the biomedical use of marmosets.
