ARTÍCULO

Notes on the western black-handed tamarin, Saguinus niger (É. Geoffroy, 1803) (PRIMATES) from an amazonia-cerrado ecotone in central-western Brazil: new data on its southern limits

 

Guilherme S. T. Garbino¹, Thiago B. F. Semedo², and André Pansonato³

¹ IPÊ – Instituto de Pesquisas Ecológicas, C. Postal 47, 12960-000, Nazaré Paulista, São Paulo, Brazil. [Correspondência: Guilherme S. T. Garbino <gstgarbino@hotmail.com>]
² Pós-graduação em Zoologia, Universidade Federal de Mato Grosso (UFMT), Instituto de Biociências, Cuiabá, Mato Grosso, Brazil.
³ Faculdade de Ciências Biológicas, Universidade de Cuiabá (UNIC), Av. Manoel José de Arruda, 3100, Jardim Europa, 78065–900, Cuiabá, Mato Grosso, Brazil

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ABSTRACT.

The western black tamarin, Saguinus niger, is an endemic Brazilian primate currently classified as Vulnerable by the Brazilian environmental authorities. In this paper, we report two new records from an Amazonia-Cerrado ecotone that extend the range of the species further south to the Brazilian state of Mato Grosso. Additionally, we obtained an ecological niche model (ENM) for S. nigerusing eight climatic variables. The results of the ENM analysis suggest that the species is strongly associated with lowland areas where the temperature does not vary significantly among seasons. We also point out that the Araguaia, Tapirapé, and Comandante Fontoura rivers may act, along with open Cerrado formations and more seasonal climate, as southern barriers. The absence of protected areas in the southern part of its range, in combination with the intense deforestation that southeastern Amazonia faces, casts doubts on the continued presence of this and other forest-dependent species in the region.

RESUMO.

Notas sobre o sauim-preto, Saguinus niger (É. Geoffroy, 1803) (Primates), em uma área de ecótono Amazônia-Cerrado no centro-oeste do Brasil: novos dados sobre seus limites austrais.

O sauim amazônico Saguinus niger é um primata endêmico do Brasil, atualmente classificado como vulnerável na lista brasileira de espécies ameaçadas. Neste estudo, reportamos dois novos registros para uma área ecotonal entre Amazônia e Cerrado estendendo a distribuição da espécie ao sul para o estado de Mato Grosso. Adicionalmente, utilizamos modelagem de nicho ecológico (MNE) utilizando oito variáveis climáticas. O resultado da MNE sugere que a espécie está fortemente associada às áreas baixas onde temperaturas não variam significantemente ao longo das estações do ano. Sugerimos que os rios Araguaia, Tapirapé e Comandante Fontoura juntamente com a formação aberta do Cerrado e um clima mais sazonal podem ser barreiras de dispersão ao sul para espécie. Além disso, a inexistência de áreas protegidas ao sul da distribuição em combinação com intenso desflorestamento põe em dúvida a presença da espécie nesta região no longo prazo.

Key words: Amazon Forest; Cerrado; Large-bodied tamarin; Mato Grosso.

Palavras chave: Cerrado; Floresta Amazônica; Mato Grosso; Sagui amazônico.

Recibido 26 mayo 2015.
Aceptado 13 octubre 2015.

Editor asociado: R Gregorin

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INTRODUCTION

Tamarins, genus Saguinus (sensu Hershkovitz, 1977), are one of the most species-rich genera of Neotropical monkeys, with 22 recognized species distributed throughout Amazonia, the rainforests of southern Central America and northern South America (Rylands and Mit­termeier, 2013; Sampaio et al., 2015).

The midas species group of Saguinus, part of the large-bodied clade of tamarins (Buckner et al., 2015), is composed of three species: Saguinus midas (Linnaeus, 1758); S. ursulus Hoffmannsegg, 1807, and S. niger(É. Geoffroy, 1803) (Vallinoto et al., 2006; Gregorin and de Vivo, 2013).

The range of Saguinus niger, as redefined by Gregorin and De Vivo (2013), is limited by the Rio Tocantins to the east, by the Rio Xingu to the west and by the Rio Amazonas to the north. The southern limits of the species, however, are unknown, and the southernmost confirmed records are from a latitude of about 8° S (Gregorin and De Vivo, 2013; Carvalho et al., 2014). In this study, we present two new records that extend the range of S. niger southwards, into the central-western region of Brazil in the northeastern portion of Mato Grosso state. Additionally, we perform an ecological niche model (ENM) analysis for the species and comment on the biogeographical relevance of our records.

MATERIALS AND METHODS

Data

We obtained species occurrence data from published records (see Table 1). One of the two new records is based on an observed animal and the other on a museum specimen, collected by L. F. Silveira (IC­MBio permit number 28198-4), that is preserved as a skin at the Museu de Zoologia da Universidade de São Paulo (MZUSP), São Paulo, Brazil.

Table 1 Summary of the known localities for Saguinus niger

Ecological niche modeling

To estimate the habitat suitability and infer the potential distribution of S. niger, we produced an ENM for the species. We chose the algorithm MaxEnt v. 3.2.3k (Phillips et al., 2006; Phillips and Dudík, 2008), due to the fact that it performs well for a small amount of locality data and because we assume that there are not broad unsampled areas for the species, which could bias the results (Elith et al., 2006; Pearson et al., 2007; Peterson et al., 2007).

We downloaded climatic data at 5 arc-minute (~0.08° or 10 km) resolution, from Worldclim database (Hijmans et al., 2005; http://www.worldclim.org/bioclim). Eight climatic variables were selected, all of which derive from topography, precipitation or temperature (Table 2). We chose these from a total of 20 available variables based on the low correlation values between them (Pearson correlation coefficient < 0.4) (Table 3). A few variables, even though strongly correlated, were kept because we believe they are biologically meaningful for the species. Precipitation of the driest month (BIO 14), for example, is relevant for the Amazonia-Cerrado ecotone, which is an area strongly influenced by rainfall seasonality (Ivanauskas et al., 2008).

Table 2 Environmental variables used to infer habitat suitability of Saguinus niger

Table 3 Pearson’s correlation coefficients between the eight climatic variables used in this study (acronyms explained in Table 2). Values with medium to high correlation (> 0.4) are in bold.

We ran the program with the default settings, except for “maximum iterations” which was set to 5000 and “do clamping”, which was disabled. We used random seed to generate 10 replicate analyses based on bootstrap subsampling.

We ran the model for the entire Neotropical region and clipped the area of interest. This should not be a problem, since callitrichines that occur in the Amazonia south of Madeira and Amazonas rivers have relatively restricted, river-bound, ranges (see Rylands and Mittermeier, 2013). The selected output was the median of the 10 output grids.

We used a jackknife test to estimate the relative importance of each variable. This test calculates how much each variable individually contributes to the overall gain and the effect of its absence in the model (Phillips et al., 2006; Phillips and Dudík, 2008). To determine whether the observed probabilities differed from a random result; we used the values of the area under the receiver operating characteristic curve (AUC) (Elith et al., 2006).

RESULTS

Geographic distribution

The present records, in an Amazonia-Cerrado transition zone, extend the geographic distribution of S. niger approximately 280 km southwards, to the central-western region of Brazil (Fig. 1A, localities 1 and 2). They also represent the southernmost available records for the species and for any large-bodied Saguinus (sensu Matauschek et al., 2011).

Fig. 1. a) Known localities for Saguinus niger. Dashed lines are Brazilian state boundaries and solid lines represent rivers. Major biomes are: I- Amazonia; II- Cerrado; III- Mato Grosso tropical dry forest; IV- Seasonal semideciduous forest. For locality data see Table 1. b) Potential geographic distribution of S. nigerbased on environmental suitability model.

The first record (Fig. 1A, locality 1) is based on an observed individual from the municipality of Confresa, state of Mato Grosso (10° 08’ 53’’ S - 51° 54’ 18’’ W, ca. 290 m a.s.l.) (Fig. 2A). The record was made in July 30, 2014 at around 10:00 h in a site with a high degree of anthropogenic disturbance and habitat fragmentation (Fig. 2B). The area where the species was recorded consists of Cerrado forest surrounded by pasture and extensive corn and soy bean plantation. The second record is from Fazenda Fartura (Fig. 1A, locality 2), a farm with the headquarters in the municipality of Santana do Araguaia, state of Pará. The farm has an area of 53 078 ha of which 35 108 ha are protected areas, including forested formations (Somenzari et al., 2011) where the specimen MZUSP 35403 (female, skin only) was collected, in November 12, 2010 (09° 38’ S - 50° 26’ W, 201 m a.s.l.). The area is transitional between the Cerrado and Amazonia, presenting sea­sonally flooded forests and terra firme moist broadleaf forests, which are the predominant formation (Somenzari et al., 2011). Both individuals could be identified as S. nigerbased on the following characters given by Gregorin and De Vivo (2013): shorter dorsal hairs, dark and opaque ochraceous bands of the rump and saddle hairs and notably haired face, hands and fingers (Fig. 3).

Fig. 2. a) Live specimen of Saguinus niger (unknown sex) observed in Confresa, Mato Grosso, Brazil. b) Area where the species was recorded (note the Pecari tajacu on the background).

Fig. 3. a) Saguinus niger, adult female (MZUSP 35403, Fazenda Fartura, Santana do Ara­guaia, Pará); b) Saguinus niger, adult female (MZUSP 4937, Cametá, Pará); c) Saguinus ursulus, adult female (MZUSP 8932, BR-010 highway, Km 93, Pará).

Ecological niche modeling

The AUC had a high average value, over 10 replications (AUC = 0.953 S.D. 0.022), meaning that the model performed better than random, i.e. 0.5 < AUC < 1 (Elith et al., 2006).

From the jackknife results, the variable with the highest gain in the model was temperature seasonality (BIO 4). Altitude (ALT) and mini­mum temperature of coldest month (BIO 6) were the second and third most important predictors, respectively. Precipitation of driest month (BIO 14) and precipitation seasonality (BIO 15) also were relevant to explain the observed model.

According to our results, S. nigeris strongly associated with lowland areas with little changes in temperature along the year. Most of the records of the species were made in areas that are highly suitable for the species, according to the model. The area east of the Rio Tocantins, where the closely related S. ursulus occurs (see Gregorin and De Vivo, 2013), also showed high habitat suitability. Despite the high suitability in the Araguaia-Tocantins interfluvium, there is no record of tamarins in that region.

The record from Confresa is in an area with medium-low suitability for the species (Fig. 1B), which is expected, since this area is more seasonal than the central and northern range of the species. A low suitability also reinforces the hypothesis that the new records may indeed represent the southern limit of the distribution of the western black tamarin.

DISCUSSION

There are some species of Amazonian primates that occur in similar habitats as S. nigerbut are found further south than the southernmost localities presented for the black tamarin in this study. Snethlage’s marmoset, Mico emiliae, occurs at latitudes of 8° S between the Xingu and Teles Pires rivers (Pimenta and Silva-Júnior, 2005; Fialho, 2010) and has been recorded much southwards, at the ecotonal areas of the Rio Xingu headwaters (approx. 11° S) (Garbino, 2011; Miranda et al., 2014). Likewise, Vieira’s titi, Callicebus vieirai, is known from Largo do Souza, right margin of Rio Iriri (4°S) and its type locality is at the Xingu headwaters (11° S) (Gualda-Barros et al., 2012).

The two records of S. niger herein reported for the Mato Grosso and Pará states are within the Xingu center of en­demism (sensu Silva et al., 2005) situated in a transitional zone between the Amazonia and Cerrado biomes, and conform to the distribution range of the species proposed by Gregorin and De Vivo (2013). In this sense, it appears that the distribution of the black tamarin is delimited to the south by the large rivers and also the open vegetation and more seasonal climate of the Cerrado (Fig. 1). The western barrier may be the Rio Comandante Fontoura, a right-bank tributary of Rio Xingu. To the east, three rivers may act as barriers: the expansive Rio Araguaia, its left-bank tributary Rio Ta­pirapé, and Rio das Mortes. Our hypothesis is consistent with our environmental niche modeling results, indicating that the climate and vegetation present in the area represent the southernmost suitable habitat for the species (see Fig. 1b). Additionally, another monkey, Uta Hick’s bearded saki, Chiropotes utahicki, also has its southern limit in the Rio Tapirapé, corroborating our hypothesis related to habitat suitability (Silva-Júnior et al., 2013).

Areas where tamarins were recorded are currently subject to an accelerated deforestation process for agriculture, selective logging, and cattle ranching developments (Gascon et al., 2001; Yoshikawa and Sanga-Ngoie, 2011). The Xingu center of endemism is considered the second most deforested of the Amazonian centers, having only 27.11% of its total area protected (Silva et al., 2005). For that reason, conservation policies must be applied urgently for the species as its habitat is being lost rapidly. It is important to note that, while S. niger is already classified at the national (ICMBio) and international (IUCN) levels as Vulnerable, pri­marily due to habitat loss (Rylands and Mitter­meier, 2008; ICMBio, 2014), both assessments (IUCN and ICMBio) considered S. nigerand S. ursulus to conform a single species. Thus it is possible that, now that they are treated as distinct taxa, the situation of both species is worse than previously assumed.

Some parts of the range of S. niger, such as Caxiuanã National Forest, Tapirapé-Aquiri National Forest and Carajás National Forest, are within protected areas of sustainable use. However, on the southernmost tip of the species range, a portion where its presence is relevant, both biogeographically (it is the only record of a large-bodied Saguinus for an ecotonal area) and politically (it is the only place where the species occur in the state of Mato Grosso), the species depends on forest remnants in private properties to survive. Some of them, such as Fazenda Fartura, still provide a habitat of considerable size, but its protection there can only be guaranteed in the long term by the establishments of new protected areas, either private or public.

ACKNOWLEDGEMENTS

We thank Mario de Vivo and Juliana Barros (MZUSP) for allowing us to examine specimens under their care, Victor Fonseca for discussion on the taxonomy of the species and the Associate Editor, Renato Gregorin, whose com­ments and suggestions were very helpful. We also thank Paula Prist for providing fundamental advice on the ENM analysis and Rafael Marcondes for reviewing the English. TBFS was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior – CAPES.

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