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We investigated the spatial distribution of native and invasive marmoset species (Callithrix), as well as their hybrids, in the Serra dos Órgãos National Park (PARNASO) and surrounding area in Rio de Janeiro state, Brazil. To estimate occupancy and the detection probability, we surveyed 56 sites within the park and 52 sites outside its limits using...
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The common marmoset (Callithrix jacchus) is a small New World primate species that has been recently targeted as a potentially powerful preclinical model of human prefrontal cortex dysfunction. Although the structural boundaries of frontal cortex were described in marmosets at the start of the 20th century (Brodmann, 1909) and refined more recently...
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Citations
... and locations closer to forest edges, and secondary forest with denser understory, with tangles of lianas and epiphytes, which are associated with greater availability of natural food resources for marmosets (Rylands and Faria 1993; Norris et al. 2011). We also expected greater abundance of Callithrix spp. in locations closer to roads and tourist and urban areas, as these species have greater exibility to survive in places with higher levels of human interference, which have greater anthropogenic food offered by humans (Stevenson and Rylands 1988;Secco et al. 2018;Detogne et al. 2017). Finally, we expected that detection probability of Callithrix spp. ...
Biological invasions can interfere decisively with the dynamics of important ecological processes.For primates of the genus Callithrix (marmosets), congener introductions and hybridization represent one of the greatest threats to native species. The Rio Doce State Park (RDSP), in southeastern Brazil, has records of three species of Callithrix , the endangered native species C. aurita , and two species of introduced marmosets, C. geoffroyi and C. penicillata .We used the playback method combined with adapted N-mixture models to estimate abundance and detection probability for Callithrix spp. in relation to biological variables. We estimated a total of 139 individuals, equivalent to 0.12 ind./ha, all being hybrids, except for one individual of C. aurita observed in a group of hybrids.The abundance of Callithrix spp. was higher in locations close to the forest edge, possibly due to the high availability of insects and greater availability of shelters in these areas.The detection probability of Callithrix spp. correlated positively with precipitation, indicating that greater humidity, as well as greater availability of arthropods, may favor the detection of individuals due to their high foraging activity during these periods. The results of this study show the critical scenario of biological invasions in RDSP, with serious threats to the native species.We suggest urgent and integrated measures to contribute to the conservation of C. aurita , such as a management plan for the few individuals of the native species. The unprecedented adaptation of the N-mixture model showed effectiveness for estimate abundance and detection probability of acoustically-responsive primates such as species of the genus Callithrix .
... Serra dos Ó rgãos National Park location, Rio de Janeiro, Brazil(Detogne et al., 2017). ...
Purpose
In this study, we describe the impact of the Environmental Education (EE) projects for environmental regeneration conducted by the Group of Research and Studies in Environmental Education and Sustainability (GEPEASA) in Brazil.
Methods
EE programs have been conducted in National Parks and public schools in urban cities with the objective to include EE in the school curriculum, with school farms, classes of sustainability, food security and environmental health, and recover local green areas.
Results
In the areas where EE programs have been applied, there are increases of green areas, ecological consciousness and social engagement, and well-being of students and communities.
Conclusions
Lack of ‘nature’ contact is critical in urban areas, where reduced green areas and outdoor activities have created an artificial lifestyle and a false perception of natural reality, increasing the risk of chronic diseases and mental disorders. EE carries the main responsibility to reestablish the connection between nature and children and communities, re-educating them to be the future's conscious Earth's citizens.
... The distribution range of C. aurita is within the most human-populated region of Brazil (southeast) and, differently from C. jacchus and C. penicillata, the buffy-tufted-ear marmoset seems to be less frequent in forest edges and near urban areas (e.g., Serra dos Órgãos National Park, Detogne et al., 2017). This habitat restriction makes C. aurita even more threatened by habitat reduction, landscape fragmentation, and presence of closely related invasive Callithrix species . ...
... One of us (JMGJ) walked slowly (almost 2 km/h constant) along the transects stopping for playback sessions every 200 m to enhance marmoset detectability (e.g., Dacier et al., 2011;Detogne et al., 2017). During the playback session, a 2-minute recording of C. aurita "long phee call" was played directing the loudspeaker to the four cardinal directions for 30 s each. ...
... Notably, the lowest density estimate reported was also recorded in a large (about 200 km 2 ) and protected area of montane semideciduous forest (Pereira, 2010). In this same study area, Detogne et al. (2017) reported the presence of a small population of C. aurita and the presence of two invasive species, C. jacchus and C. penicillata. It appears that primates' co-occurrence and forest remnant size alone might not explain the density range of C. aurita observed in the previous studied areas and in Serra do Japi (table 1). ...
Forest-dependent species are among the most threatened species due to landscape changes, and this is the case of the buffy-tufted-ear marmoset (Callithrix aurita), an Atlantic Forest endemic primate. Besides its extensive habitat reduction across Atlantic Forest, the species suffers from the negative impact of the presence of non-native congeners that threatens its local populations due to competition and hybridization events. Knowing the population status of this endangered species is important to guide conservation efforts. Thus, we estimated the population density of C. aurita and recorded the presence of invasive Callithrix species and Callithrix hybrids in Serra do Japi, a large forest remnant with mountainous terrain within the most human-populated region of the State of São Paulo, Brazil. We surveyed a 14.8 km 2 area with 387.2 km of survey effort. We estimated a sighting rate of 4.4 groups/10 km walked. The maximum number of individuals recorded per group ranged from 7 to 12. We identified 15 groups throughout the sampled area, totalling 1.01 groups/km 2. Two individuals from two distinct groups presented body pelage characteristic of hybrids between C. aurita and other Callithrix species. No individuals of other Callithrix species were recorded within the surveyed area. Considering the total size of this remnant and the potential population size of C. aurita inhabiting this area, this local population may be an important source of individuals for helping the conservation and long-term persistence of the species. However, the presence of Callithrix hybrids in the area is worrying and may threaten the local native population. Our study reinforces the concern with C. aurita conservation and the need for studies focused on the management of hybrids and invasive Callithrix species. Mitigation measures should be directed to readily control hybridization to keep this large population of Serra do Japi safe.
... The color of the body was lighter with eventual grooves (Fig. 2). These features confer to the individuals sampled a mixed pelage pattern of the tufts and the back, suggesting that they are hybrids between C. aurita and C. penicillata or C. jacchus 29,32,41 (since both alien species are observed at the sampling locations). SRY analysis. ...
The native marmoset of the Southeastern Atlantic Forest in Brazil is among the 25 most endangered primates of the world. Hybridization with alien species is one of its main threats registered since the early 2000s based on phenotype, so far, without genetic confirmation. Using uniparental molecular markers, we analyzed 18 putative hybrids, captured from 2004 to 2013 in different localities of the Atlantic Forest. A nine base pair deletion in the SRY gene of C. aurita was used to investigate paternal ancestry. Maternal ancestry was assessed by DNA sequencing of ca. 455 bp from the COX2 gene. Hybridization was confirmed for 16 out of the 18 marmosets since they inherited COX2 haplotypes of the alien C. penicillata or C. jacchus and the SRY deletion specific to C. aurita. Two individuals inherited both parental lineages of C. aurita, which is probably related to backcrossing or hybrid interbreeding. The direction of hybridization of females with the matrilineal lineage of invasive species with males descending from the native lineage was predominant in our sampling. This is the first time that hybridization between C. aurita and invasive species has been confirmed through genetic analysis.
... 2,4,21,[152][153][154] Contemporary allochthonous Callithrix species are usually found in urban or peri-urban areas of the southeastern Atlantic forest. 17,21,150,151,[154][155][156] Within these contexts, allochthonous Callithrix have frequent human contact and exposure and receive anthropogenic food supplementation. 17,54,157 These allochthonous marmosets can also be found within or around natural reserves, 13,17,150,151,154,156 and in some areas, such marmoset populations are larger than those of native, endangered callitrichids (eg, 150 ). ...
... 17,21,150,151,[154][155][156] Within these contexts, allochthonous Callithrix have frequent human contact and exposure and receive anthropogenic food supplementation. 17,54,157 These allochthonous marmosets can also be found within or around natural reserves, 13,17,150,151,154,156 and in some areas, such marmoset populations are larger than those of native, endangered callitrichids (eg, 150 ). Such introductions could alter the ecological relationships among taxa, 13,158 because the main threats posed by allochthonous marmosets are competition for food resources, increased predation of native fauna, the introduction and maintenance of disease, and hybridization. ...
We provide here a current overview of marmoset (Callithrix) evolution, hybridization, species biology, basic/biomedical research, and conservation initiatives. Composed of 2 subgroups, the aurita group (C aurita and C f laviceps) and the jacchus Downloaded from https://academic.oup.com/ilarjournal/advance-article/doi/10.1093/ilar/ilab027/6474502 by Houston Academy of Medicine-Texas Medical Center Library user on 22 December 2021 2 Malukiewicz et al. group (C geoffroyi, C jacchus, C kuhlii, and C penicillata), this relatively young primate radiation is endemic to the Brazilian Cerrado, Caatinga, and Atlantic Forest biomes. Significant impacts on Callithrix within these biomes resulting from anthropogenic activity include (1) population declines, particularly for the aurita group; (2) widespread geographic displacement, biological invasions, and range expansions of C jacchus and C penicillata; (3) anthropogenic hybridization; and (4) epizootic Yellow Fever and Zika viral outbreaks. A number of Brazilian legal and conservation initiatives are now in place to protect the threatened aurita group and increase research about them. Due to their small size and rapid life history, marmosets are prized biomedical models. As a result, there are increasingly sophisticated genomic Callithrix resources available and burgeoning marmoset functional, immuno-, and epigenomic research. In both the laboratory and the wild, marmosets have given us insight into cognition, social group dynamics, human disease, and pregnancy. Callithrix jacchus and C penicillata are emerging neotropical primate models for arbovirus disease, including Dengue and Zika. Wild marmoset populations are helping us understand sylvatic transmission and human spillover of Zika and Yellow Fever viruses. All of these factors are positioning marmosets as preeminent models to facilitate understanding of facets of evolution, hybridization, conservation, human disease, and emerging infectious diseases.
... O tamanho total da população de C. aurita é estimado entre 10.000 a 11.000 indivíduos maduros, apresentando tendência ao declínio e uma redução de 50% ao longo das últimas três gerações, estando listada como "em perigo" tanto pela Lista Vermelha da IUCN quanto pelo Livro Vermelho da Fauna Brasileira Ameaçada de Extinção (CARVALHO et al., 2018;MELO et al., 2018;MELO et al., 2021). A maior parte da população remanescente da espécie encontra-se isolada (DETOGNE et al., 2017). A perda e fragmentação dos habitats, a competição e hibridação com congêneres alóctones (principalmente C. jacchus e C. penicillata) (NORRIS et al., 2011;CARVALHO et al., 2018;MALUKIEWICZ, 2018) As metodologias de levantamento variaram entre os trabalhos. ...
... E em um dos locais ondeVital et al. (2020) registraram o sagui-da-serra-escuro no município em 2017, observamos apenas es-pécimes híbridos. Este curto espaço de tempo para a suplantação de grupos aparentemente puros ou indivíduos de C. aurita em mais de uma localidade demonstra a já mencionada grande capacidade invasiva das espécies alóctones ou formas híbridas.Em toda a distribuição de C. aurita, saguis invasores e híbridos já são amplamente encontrados em áreas de mata contínua, conservadas ou perturbadas, e até mesmo em unidades de conservação de proteção integral(NOGUEIRA et al., 2011;CARVALHO;XAVIER; ESBÉRARD, 2015;AXIMOFF et al., 2016;DETOGNE et al., 2017;MALUKIEWICZ, 2018). Isso sugere que embora C. aurita sejatipicamente florestal (JERUSALINSKY; MELO, 2018), a conservação da espécie não depende apenas da criação de áreas de floresta protegidas, mas carece, adicionalmente, de um trabalho de manejo integrado, com ações in situ e ex situ visando o incremento de populações nativas, o controle de populações invasoras, como também a educação ambiental em detrimento do tráfico de animais e da proliferação de saguis invasores e híbridos (MENDES; BRANDÃO; IGAYARA, 2016). ...
Callithrix aurita, endemic to the Atlantic Forest, is one of the most endangered primates in the world, due to habitat fragmentation, deforestation, hybridization and competition with other species of the genus. Through new records of the species and its congeners in the Zona da Mata, Minas Gerais, we can contribute to the conservation of C. aurita, informing about the expansion of invasive marmosets and hybridization in its area of occurrence. In fragments inspected through active search and with use of playback, between 2017 and 2021, a total of 137 groups of marmosets were identified in 18 municipalities, among which 13 were groups of C. aurita, four of C. penicillata and 110 groups of hybrid forms. The sampled points alert to the need to define priority areas for the conservation of C. aurita, in addition to the urgency of its management and of its allochthonous species and hybrid forms, preventing the continuity of hybridization and consequent extinction of the species
... Em contrapartida, as espécies C. penicillata e C. jacchus apresentam adaptações morfológicas que as tornam mais aptas à gomivoria do que seus congêneres de Mata Atlântica, utilizando de forma majoritária um recurso alimentar que se mantém disponível durante todo o ano (PONTES; MONTEIRO DA CRUZ, 1995;DUARTE;YOUNG, 2014;TEIXEIRA et al., 2015). Como resultado, presume-se uma disparidade competitiva entre autóctone e alóctones em fragmentos de vegetação mais atropizados, potencializando a sobreposição da área de ocorrência do sagui-da-serra-escuro por seus congêneres MITTERMEIER, 1976aMITTERMEIER, , 1976bDE MIRANDA;DE FARIA, 2001;VILELA;DEL-CLARO, 2011;FRANCISCO et al., 2014;DETOGNE et al., 2017). O histórico de levantamentos realizados nas proximidades da área de estudo do presente estudo apontam para este processo (FUZESSY et al., 2014;MASSARDI, 2021;PEREIRA, 2012;SANTANA et al., 2008;VITAL, 2017VITAL, , 2020. ...
... Este panorama configura não somente a situação do município em que o referente estudo foi realizado, como também de diversas áreas do sudeste brasileiro(SILVA, 2014;DETOGNE et al., 2017;SILVA et al., 2018;CARVALHO, et al., 2018).Os fenótipos observados durante a coleta de dados, ilustrados pelas Figuras 7,8, 9 e 10 evidenciam e reforçam diagnósticos anteriores sobre a ocupação do município por Callithrix sp. e espécies alóctones, dada a constatação da presença de fenótipos híbridos na totalidade dos indivíduos avistados.Fuzessy et al (2014) compara coloração, pelagem e morfometria de saguis híbridos de C. penicillata x C. geoffroyi capturados em um fragmento florestal da UFV. A prevalência de características do fenótipo facial de C. penicillata observada no referido estudo se confirmou, assim como notável variação fenotípica em termos de pelagens e padrões faciais. ...
... A presença de Callithrix sp. também já foi atrelada à proximidade com seres humanos, de forma que abundância e densidade desses animais pode ser acentuada devido ao suprimento alimentar ofertado por pessoas(DETOGNE et al., 2017).Os resultados alcançados pelo presente levantamento evidenciam maior número mínimo de indivíduos estimados, abundância relativa e 2ª maior inferência de densidade absoluta na Mata da Biologia, único fragmento amostrado utilizado pela população como área de lazer. Embora seja o segundo maior fragmento dentre os amostrados, é provável que este resultado esteja também relacionado à interações antrópicas, nas quais alimentos podem ser providos por transeuntes ou mesmo por funcionários de departamentos localizados no entorno da vagetação. ...
Atualmente, observa-se uma série de ações antrópicas que promovem graves consequências à biodiversidade. A introdução de espécies alóctones, por exemplo, é uma intervenção capaz de desencadear a hibridação entre congêneres, panorama observado em diversas localidades do território brasileiro entre espécies de primatas do gênero Callithrix. O município de Viçosa, em Minas Gerais, experimenta esta situação por décadas, na qual sua única espécie nativa e ameaçada de extinção, Callithrix aurita, tem registros cada vez mais escassos. Em contrapartida, a ocupação da região por espécies alóctones e indivíduos híbridos invasores vem sendo continuamente notificada por estudos pretéritos. No presente estudo, foi realizado um levantamento e diagnóstico populacional de saguis híbridos (Callithrix sp.), por meio de busca ativa e utilização de playback, em cinco fragmentos florestais pertencentes ao bioma Mata Atlântica e localizados dentro da Universidade Federal de Viçosa, campus Viçosa (20º75‟72‟‟ S , 42º 87‟ 51‟‟ W): Mata do Paraíso, Mata da Biologia, Mata da Divisão de Água e Esgoto, Mata da Silvicultura e Mata do Ginásio. Os dados foram coletados durante o final da estação seca de 2021, prevista para o município; 23,06km de trilhas e estradas foram percorridos, nos quais 90 pontos de playback foram distribuídos. Estimou-se o total de 215,64 indivíduos nos 5 fragmentos amostrados, levando em conta não somente os espécimes avistados, como também uma inferência média a partir dos registros vocais obtidos, diante da ocasional impossibilidade de efetiva visualização e contagem dos indivíduos. Foi calculada abundância relativa (indivíduos/ponto amostral) e inferida densidade absoluta (indivíduos/hectare) para cada fragmento. Assim, os resultados apontam que tamanho do fragmento e a presença antrópica são fatores relevantes para as maiores cifras de abundância relativa e densidade absoluta aqui averiguadas. 97,64% dos indivíduos avistados foram diferenciados quanto às classes etárias, enquanto 29,13% foram diferidos quanto ao sexo, contribuindo para a construção de um conhecimento sistemático sobre a caracterização demográfica de Callithrix sp., ainda inédita para o município. Tal contribuição pode ser útil como linha de base para o monitoramento de saguis híbridos invasores na região, subsidiando ações que visam o manejo populacional de invasores e a futura reintrodução de C. aurita em Viçosa. O presente estudo também aponta para a necessidade do desenvolvimento de ações informativas para a população sobre impactos envolvidos no contato entre humanos e primatas não-humanos.
... The study area (PNMMT) is the largest municipal PA for the Atlantic Forest biome, protecting 4.397 hectares (SOS Mata Atlântica, 2017). Studies on C. aurita have been taken only in PARNASO and PETP, indicating the presence of the species and its allochthonous congeners (Pereira et al., 2008;Detogne et al., 2017;Culot et al., 2019;Cronemberger et al., 2019). ...
Callithrix aurita, an Atlantic Forest endemic primate, is a threatened species due to habitat loss, deforestation, interspecific competition and hybridization. In 2018, it entered the list of the world's 25-most threatened primate species, therefore, new occurrence sites must help in its conservation. Transects in the Montanhas de Teresópolis Municipal Natural Park and occasional sampling on the surrounding roads, using playback, have been carried out between March 2020 and January 2021. Eleven new records were made of the occurrence of the species in and around the PNMMT, in secondary forest sites with altitudes between 711 and 1000m. These records reinforce the importance of the Park for the conservation of this primate. The presence of this species can help the planning and management of this protected area, indicating areas for preservation.
... Contemporary allochthonous Callithrix species are usually found in urban or peri-urban areas of the southeastern Atlantic Forest [21,58,151,152,[155][156][157]. Within these contexts, allochthonous ...
... Callithrix have frequent human contact and exposure, and receive anthropogenic food supplementation [54,58,158]. These allochthonous marmosets can also be found within or around natural reserves [13,58,151,152,155,157], and in some areas, such marmoset populations are larger than those of native, endangered callitrichids [e.g.,151]. Such introductions could alter the ecological relationships among taxa [13,159], as the main threats posed by allochthonous marmosets are competition for food resources, increased predation of native fauna, the introduction and maintenance of disease, and hybridization [160][161][162]. ...
We provide here a current overview of marmoset (Callithrix) evolution, hybridization, species biology, basic/biomedical research, and conservation initiatives. Composed of two subgroups, the aurita group (C. aurita and C. flaviceps) and the jacchus group (C. geoffroyi, C. jacchus, C. kuhlii and C. penicillata), this relatively young primate radiation is endemic to the Brazilian Cerrado, Caatinga, and Atlantic Forest biomes. Significant impacts on Callithrix within these biomes resulting from anthropogenic activity include: (1) population declines, particularly for the aurita group; (2) widespread geographic displacement, biological invasions, and range expansions of C. jacchus and C. penicillata; (3) anthropogenic hybridization; and (4) epizootic Yellow Fever and Zika viral outbreaks. A number of Brazilian legal and conservation initiatives are now in place to protect the threatened aurita group and increase research about them. Due to their small size and rapid life history, marmosets are prized biomedical models. As a result, there are increasingly sophisticated genomic Callithrix resources available and burgeoning marmoset functional, immuno-, and epi- genomic research. In both the laboratory and the wild, marmosets have given us insight into cognition, social group dynamics, human disease, and pregnancy. Callithrix jacchus and C. penicillata are emerging Neotropical primate models for arbovirus disease, including Dengue and Zika. Wild marmoset populations are helping us understand sylvatic transmission and human spillover of Zika and Yellow Fever viruses. All of these factors are positioning marmosets as preeminent models to facilitate understanding of facets of evolution, hybridization, conservation, human disease, and emerging infectious diseases.
... In our study area, predators of the 16 nests of the two thamnophilids were two mammal and two bird species, although invasive marmosets of the genus Callithrix caused most damage. In the Atlantic Forest, these marmosets are found typically in edge habitats (Detogne et al. 2017), but are also able to colonize novel and disturbed environments. Some of the marmosets encountered in the study area were hybrids of the two species occupying habitats that are exotic to both (Reis et al. 2011). ...
Invasive predators contributed to recent extinctions worldwide, including endemic birds. We monitored nests of two endemic birds in the Atlantic Forest, the serra antwren (Formicivora serrana littoralis) and the sooretama slaty antshrike (Thamnophilus ambiguus) during two consecutive breeding seasons, to estimate predation rates and identify the predators. As invasive marmosets apparently became locally common, we hypothesized that they would prey upon natural nests at a higher rate than native predators. We found 13 nests of the antwren and 15 of the antshrike, of which 100% and 73%, respectively, were preyed upon. Invasive marmosets preyed upon 13 of 16 nests (81%) with identified predators, affecting 90% and 67% of the antwren and the antshrike nests. This study documented that invasive primates negatively affect the breeding success of native birds in Brazil. We highlight the need for urgent measures to manage invasive marmosets to avoid the local extirpation of the endemic birds.
