ArticlePDF Available

Diet of a Free-Ranging Group of Squirrel Monkeys (Saimiri sciureus) in Eastern Brazilian Amazonia

Authors:

Abstract and Figures

The feeding behaviour of free-ranging Saimiri sciureus was monitored over a 6-month period in eastern Brazilian Amazonia. Behavioural data were collected in scan samples (7-9 days per month), and fruit and arthropod availability were recorded monthly. A total of 3,546 feeding records were collected, divided between reproductive plant parts (55.1%) and arthropods (44.9%). The majority of identified prey were orthopterans and lepidopterans, and 10 of the 23 plant species exploited were Leguminosae and Sapotaceae. The diet varied progressively between August (20.0% plant, 80.0% animal) and January (79.7% plant, 20.3% animal). This shift accompanied an increase in the number of fruiting trees and evidence of declining arthropod availability. This included a marked reduction in foraging success and increasing consumption of immature prey. Overall, the data indicate that Amazonian squirrel monkeys may be relatively frugivorous during periods when prey is scarce.
Content may be subject to copyright.
Fax +
41 61 306 12 34
E-Mail karger@karger.ch
www.karger.com
Ó2003 S. Karger AG, Basel
0015–5713/03/0743–0150$19.50/0
Accessible online at:
www.karger.com/fpr
Eldianne M. Lima, DEGEN/UFPa
Ciaxa Postal 8607
66.075-900 Belém, PA (Brazil)
Tel. +55 91 916 17293, Fax +55 91 211 1662
E-Mail eldianne@bol.com.br
Reviewed Article
Folia Primatol 2003;74:150–158 Received: June 18, 2002
DOI: 10.1159/000070648 Accepted after revision: February 7, 2003
Diet of a Free-Ranging Group of
Squirrel Monkeys
(Saimiri sciureus)
in Eastern Brazilian Amazonia
Eldianne M. Lima
a
Stephen F. Ferrari
a
,
b
Departamentos de
a
Psicologia Experimental e
b
Genética, Universidade Federal do
Pará, Belém, Brasil
Key Words
Squirrel monkeys `
Saimiri sciureus
` Diet ` Frugivory ` Insectivory ` Eastern
Amazonia
Abstract
The feeding behaviour of free-ranging
Saimiri sciureus
was monitored over
a 6-month period in eastern Brazilian Amazonia. Behavioural data were collected
in scan samples (7–9 days per month), and fruit and arthropod availability were
recorded monthly. A total of 3,546 feeding records were collected, divided be-
tween reproductive plant parts (55.1%) and arthropods (44.9%). The majority
of identified prey were orthopterans and lepidopterans, and 10 of the 23 plant
species exploited were Leguminosae and Sapotaceae. The diet varied progres-
sively between August (20.0% plant, 80.0% animal) and January (79.7% plant,
20.3% animal). This shift accompanied an increase in the number of fruiting
trees and evidence of declining arthropod availability. This included a marked
reduction in foraging success and increasing consumption of immature prey.
Overall, the data indicate that Amazonian squirrel monkeys may be relatively
frugivorous during periods when prey is scarce.
Introduction
Amazonian squirrel monkeys, Saimiri sciureus [Silva et al., 1993; Costello et
al., 1993], are small, insectivorous platyrrhines amply distributed in northern South
America. Ecological studies are rare, however [Terborgh, 1983; Mitchell, 1994;
Copyright © 2003 S. Karger AG, Basel
Diet of Free-Ranging Saimiri sciureus 151 Folia Primatol 2003;74:150–158
Souza et al., 1997; Lima et al., 2000], although the second species, Saimiri
oerstedi, has been well studied in Costa Rica [Boinski, 1987, 1988, 1989]. Squirrel
monkeys are active animals, spending much of their daily activity period foraging
for arthropods, which they complement with reproductive plant parts. Despite
broad similarities, interspecific differences may exist in characteristics such as so-
cial organisation and foraging patterns [Mitchell et al., 1991]. However, as S. sci-
ureus is widespread in the Amazon and Orinoco basins, it seems reasonable to as-
sume that the full variation in behaviour has yet to be understood. Here, data on the
feeding behaviour of free-ranging squirrel monkeys from eastern Amazonia provide
new insights into the ecology of the species and in particular its variability in rela-
tion to environmental factors.
Methods
The study site was the Gunma Ecological Park, a privately owned reserve in
Santa Bárbara do Pará (01°13’36” S, 48°17’42” W), which encompasses 400 ha of
mainly primary lowland ‘terra firme’ forest [Lima, 2000], contiguous with forest on
neighbouring properties. The mean annual precipitation (from 1968 to 1997) is
3,266.1 ± 492.8 mm. At 3,026 mm, precipitation in 1998 was slightly below aver-
age. The study encompassed most of the dry season, which begins in July, and the
onset of the wet season (fig. 1).
Behavioural data were collected between August 1998 and January 1999. The
study group contained 60 members in August, but divided at the end of October,
leaving only 21 individuals at the beginning of November. The study group was
easily identified because it returned to the same site to sleep every night. The num-
ber of trees bearing fruit was recorded monthly in 4 phenology quadrats (total
area = 7,750 m
2
), and arthropod availability was estimated using sixty 25-cm di-
ameter water traps [Ferrari, 1988; Basset et al., 1996] set at monthly intervals, be-
Fig. 1. Monthly precipitation at the study site (data from the DENPASA meteorological
station [Lima, 2000] between January 1998 and January 1999. The study period is shaded.
152
Folia Primatol 2003;74:150–158
Lima/Ferrari
ginning in May 1998, within the study group’s home range. Trees and arthropods
were identified to at least family or order, respectively [Lima, 2000].
Behavioural data were collected in scan samples, with a 1-min scan being con-
ducted at 5-min intervals, following Ferrari and Rylands [1994]. During scans, the
activity state of each visible subject was recorded at the moment of sighting. Only
feeding records are presented here. This category was recorded whenever the sub-
ject was observed ingesting a food item. The forage category, used for the calcula-
tion of the foraging index (see below) refers to any behaviour related to the local-
isation or capture of prey. Whenever possible, the type of resource and its taxon
were identified. Plants were marked and identified at the herbarium of the Goeldi
Museum in Belém. Scans were conducted continuously throughout the diurnal ac-
tivity period. Monthly samples consisted of 7 days in August and January, 8 in De-
cember and 9 in September, October and November. Estimates of the composition
of the diet were based on the proportions of feeding records collected during a
given period. An index of foraging success – (number of records of prey feeding/
number of records of foraging) × 100 – was calculated for each month of the study
to evaluate seasonal variation in the efficiency of foraging for arthropods [Boinski,
1988; Ferrari, 1988].
Results
The number of trees bearing fruit increased progressively during the study (fig.
2), from 86.0 per hectare in August to 181.3 in January. By contrast, the only pat-
tern in arthropod abundance was a contrast between the study period and the pre-
ceding 3 months (fig. 3). Increased arthropod abundance during the wet season is a
typical pattern at most tropical sites [Wolda, 1978; Tanaka and Tanaka, 1982; Fer-
Fig. 2. Number of trees bearing fruit each month in the phenology plots at Gunma
Ecological Park, showing trees with dbh <10 cm (shaded) and those with dbh ³10 cm
(unshaded).
Diet of Free-Ranging Saimiri sciureus 153 Folia Primatol 2003;74:150–158
rari, 1988], including eastern Amazonia [Oliveira, 1996], although here, the period
of least arthropod abundance was later than that of least precipitation.
A total of 3,546 feeding records were collected, 1,954 (55.1%) involving re-
productive plant parts and 1,592 (44.9%) arthropod prey. However, the diet varied
significantly and progressively during the study (fig. 4). In the first month, 80.0%
of feeding records (n = 413) involved prey and only 20.0% plant material, whereas
Fig. 3. Arthropods captured at Gunma, from May 1998 to January 1999 (the study period
is shaded). As the number of traps recovered each month varied, values are the mean
number of animals captured per standard sample of 10 traps. Standard sample = (total
number of arthropods captured/total number of traps recovered) × 10.
Fig. 4. Monthly variation in the composition of the diet of S. sciureus at Gunma. Values
are percentages of feeding records collected each month, according to item: arthropods
(unshaded) and reproductive plant parts (shaded).
154
Folia Primatol 2003;74:150–158
Lima/Ferrari
Fig. 5. The number of plant species exploited by S. sciureus each month at Gunma. Values
are daily rates (number of species exploited during the month/number of observation days).
Table 1. Plant taxa exploited by S. sciureus in the Gunma Ecological Park
Taxon Part ingested Period
Annonaceae Duguetia surinamensis fruit Aug., Nov., Dec., Jan.
Cecropiaceae Cecropia sp. inflorescence Aug., Sep., Oct.
Dileniaceae
Darle rugoso fruit Jan.
Euphorbiaceae
Drypetes variabilis fruit Dec.
Guttiferae
Symphonia globulifera nectar Aug., Sep.
Lacistemaceae
Lacistema pubescensis fruit Jan.
Leguminosae
Inga alba fruit Sep., Oct., Nov., Dec.
Inga thibaudiana fruit Sep., Oct., Nov., Dec.
Inga paraensis fruit Nov., Dec.
Abarema jupunba fruit Nov.
Pitecelobium conchelotum fruit Nov.
Malpighiaceae Byrsonima stipulacea fruit Jan.
Melastomataceae Belucia dichotoma fruit Aug., Nov., Dec.
Belucia sp. fruit Aug.
Myristicaceae Virola surinamensis aril Dec., Jan.
Moraceae Ficus nymphaeaefolia fruit Oct.
Porouma paraense fruit Dec.
Sapotaceae Sisiziporus sp. fruit Oct.
Pouteria laurifolia fruit Oct.
Nemaluma engleri fruit Oct., Nov.
Saroculo brasiliensis fruit Oct.
Pouteria sp fruit Nov.
Simarubaceae Simarouba amara fruit Dec., Jan.
Diet of Free-Ranging Saimiri sciureus 155 Folia Primatol 2003;74:150–158
by the final month, these proportions were reversed (20.3% animal, 79.7% plant,
n = 479).
The relative consumption of plant material each month correlated significantly
with the number of trees bearing fruit (Spearman rank, r
s
= 0.886, p = 0.019, n = 6).
Twenty-three plant species from 13 families were exploited (table 1), almost half of
which belonged to the Leguminosae and Sapotaceae. There was also a strong corre-
lation (r
s
= 0.771, p = 0.072, n = 6) between the number of species used each month
(fig. 5) and the plant proportion of the diet.
Orthopterans and lepidopterans accounted for almost three quarters of identi-
fied prey (table 2), although there was a pronounced seasonal change in their ma-
turity. Only adult arthropods were captured in August and September (fig. 6), but
Table 2. Arthropod taxa exploited by S. sciureus at Gunma (prey was not identified in 794
records)
Taxon Records of All records
immatures adults
Araneae 69 (8.65) 69 (8.65)
Coleoptera 100 (12.53) 100 (12.53)
Lepidoptera 82 (10.27) 188 (23.56) 270 (33.83)
Orthoptera 23 (2.88) 301 (37.72) 324 (40.60)
Hymenoptera 11 (1.38) 15 (1.88) 26 (3.26)
Homoptera 9 (1.13) 9 (1.13)
All 116 (14.54) 682 (85.46) 798 (100.00)
Figures in parentheses indicate percentages of total in the case of immatures and adults.
Fig. 6. Monthly contribution of adult and immature arthropods to the diet of S. sciureus at
Gunma. Values are percentages of identified items (adults unshaded, immatures shaded)
captured each month.
156
Folia Primatol 2003;74:150–158
Lima/Ferrari
by December, the majority of prey were immature, mainly caterpillars (Lepidopte-
ra). This trend coincides with a progressive decline in the index of foraging success
(fig. 7), from 19.5 in August to 6.4 in January, indicating that prey was at least 3
times as difficult to capture by the end of the study. Taken together, the evidence
suggests that the capture of arthropod prey, in particular adult insects, became in-
creasingly difficult during the study period.
Discussion
Overall, the study group’s diet was slightly more frugivorous than insectivo-
rous, contrasting with previous squirrel monkey studies [Terborgh, 1983; Boinski,
1987; Souza et al., 1997; Lima et al., 2000]. While the study was relatively short, it
was clear that fruit predominated in the diet during a number of months. It should
perhaps be noted that the only long-term study of S. sciureus [Terborgh, 1983] was
based on quarterly samples rather than continuous monitoring, so, despite encom-
passing a longer period overall, it may have sampled seasonal variation less effec-
tively [Souza et al., in press].
The recorded preference for orthopteran and lepidopteran prey appears to be
characteristic of the genus throughout its range [Thorington Jr., 1968; Baldwin and
Baldwin, 1972; Terborgh, 1983; Boinski, 1987; Souza et al., 1997]. Here, this ap-
plied to both mature and immature prey. Overall, the evidence indicates that the
monkeys faced a progressive decline in prey availability and a concomitant in-
crease in an alternative resource (fruit). It is difficult to evaluate, however, to what
extent variation in the diet was related to the availability of prey or a preference for
fruit. S. oerstedi sustained the animal proportion of its diet by increasing foraging
time when arthropods were scarce [Boinski, 1987], although there was little varia-
tion in the availability of fruit.
The patterns encountered in this study appear to be more similar to those re-
corded for central American S. oerstedi [Boinski, 1987, 1988, 1989] than for S.
Fig. 7. Monthly variation in the foraging success of S. sciureus at Gunma. IFS = Index o
f
foraging success.
Diet of Free-Ranging Saimiri sciureus 157 Folia Primatol 2003;74:150–158
sciureus [Terborgh, 1983]. This contrast may be related to the more pronounced
seasonality at the former two sites in comparison with the latter, in Peru, although
other factors may be involved, such as the composition of the flora. For example,
while Ficus fruit was a key resource for S. sciureus in Peru [Terborgh, 1983], it is
only a minor item in the diet of eastern Amazonian squirrel monkeys [Lima et al,
2000; this study]. This may have additional implications for foraging and ranging
patterns. Overall, this study emphasises the ecological and behavioural flexibility
of squirrel monkeys, and the need for new studies from different, representative
sites within their considerable geographic range.
Acknowledgements
This study was supported by the Postgraduate Training Council (CAPES) and the Na-
tional Research Council (CNPq) of the Brazilian government as well as the Gunma Kenjin-
Kai of northern Brazil. Special thanks go to Hiroshi Okajima, Rogério Okajima, Roberta
Andrade, Suleima Bastos, Luciano Nascimento, Fábio Diamantino, Iris Possas, Raimundo
Orlando and all other Gunma personnel. We thank two anonymous reviewers for their help-
ful comments on the manuscript.
References
Baldwin JD, Baldwin JI (1972). The ecology and behavior of squirrel monkeys (Saimiri oerstedii) in a
natural forest in western Panama. Folia Primatologica 18: 161–184.
Basset Y, Spingate ND, Aberlinc HP, Delvane G (1996). A review of methods for sampling arthropods
in tree canopies. In Canopy Arthropods (Stork NE, Adis JC, Didham RK, eds.), pp 27–52. Lon-
don, Chapman & Hall.
Boinski S (1987). Habitat use by squirrel monkeys (Saimiri oerstedii) in Costa Rica. Folia Prima-
tologica 49: 151–167.
Boinski S (1988). Sex differences in the foraging behaviour and substrate use of squirrel monkeys in a
seasonal habitat. Behavioural Ecology and Sociobiology 23: 177–186.
Boinski S (1989). The positional behaviour and substrate use of squirrel monkeys: Ecological implica-
tions. Animal Behaviour 41: 89–102.
Costello RK, Dickinson C, Rosenberger AL, Boinski S, Szalay FS (1993). A multi-disciplinary ap-
proach to squirrel monkey (genus Saimiri) species taxonomy. In Species, Species Concepts, and
Primate Evolution (Kimbel W, Martin L, eds.), pp 177–237. New York, Plenum Press.
Ferrari SF (1988). Behaviour and Ecology of the Buffy-Headed Marmoset, Callithrix flavicepts (O.
Thomas, 1903). PhD thesis, University of London, London.
Ferrari SF, Rylands AB (1994). Activity budgets and differential visibility in field studies of three
marmosets (Callithrix spp.). Folia Primatologica 63: 78–83.
Lima EM (2000). Ecologia Comportamental de um Grupo Silvestre de Macaco-de-Cheiro (Saimiri
sciureus) no Parque Ecológico de Gunma, Santa Bárbara do Pará, PA. Masters dissertation,
Universidade Federal do Pará, Belém.
Lima EM, Pina ALCB, Ferrari SF (2000). Behaviour of free-ranging squirrel monkeys (Saimiri sci-
ureus, Platyrrhini, Cebidae) at the Fazenda Monte Verde, Peixe-Boi, Pará. In A Primatologia no
Brasil (Alonso C, ed.), vol 7, pp 171–180. João Pessoa, Sociedade Brasileira de Primatologia.
Mitchell CL (1994). Migration alliances and coalitions among adult male south American squirrel
monkeys (Saimiri sciureus). Behaviour 130: 169–190.
Mitchell CL, Boinski S, Schaik CP (1991). Comparative regimes and female bonding in two species of
squirrel monkeys (Saimiri oerstedii and Saimiri sciureus). Behavioural Ecology and Sociobiology
28: 55–60.
Oliveira ACM (1996). Ecologia e Comportamento Alimentar, Padrões de Atividade e Uso de Espaço de
um Grupo de Saguinus midas niger (Callitrichidae, Primates) na Amazônia Oriental. Masters
dissertation, Universidade Federal do Pará, Belém.
Silva BTF, Sampaio MIC, Schneider H, Schneider MPC, Montoya E, Encarnación F, Callegari-Jacques
SM, Salzano FM (1993). Protein electrophoretic variability in Saimiri and the question of its
species status. American Journal of Primatology 29: 183–193.
158
Folia Primatol 2003;74:150–158
Lima/Ferrari
Souza LL, Pina ALCB, Ferrari SF (1997). Feeding behaviour and predation of a bat by Saimiri sciureus
in a semi-natural Amazonian environment. Folia Primatologica 68: 194–198.
Souza LL, Pina ALCB, Ferrari SF (in press). Diet of the red-handed howler monkey, Alouatta belzebul
(Primates, Atelidae), at the Ferreira Penna Scientific Station. In Caxiuanã, Biodiversidade e Sus-
tentabilidade (Lisboa PLB, ed.). Belém, CNPq/MCT.
Tanaka LK, Tanaka SK (1982). Rainfall and seasonal changes in arthropod abundance on a tropical
oceanic island. Biotropica 14: 114–123.
Terborgh J (1983). Five New World Primates: A Study in Comparative Ecology. Princeton, Princeton
University Press.
Thorington RW Jr (1968). Observations of squirrel monkeys in a Colombian forest. In The Squirrel
Monkey (Rosenblum LA, Cooper RW, eds.), pp 69–85. New York, Academic Press.
Wolda H (1978). Seasonal fluctuations in rainfall, food and abundance of tropical insects. Journal of
Animal Ecology 47: 369–381.
... Frugivorousfaunivorous primates often consume nectar and other flower parts more frequently than whole flowers (Heymann, 2011). Several neotropical primate species have been documented feeding specifically on the nectar of S. globulifera including spider monkeys (Ateles geoffroyi) (Riba-Hernández and Stoner, 2005), brown capuchins (Cebus apella), woolly monkeys (Lagothrix lagotricha) (Peres, 1994), tamarins (Saguinus fuscicollis, Saguinus mystax) (Garber, 1988), and squirrel monkeys (Saimiri sciureus) (Lima and Ferrari, 2003). S. globulifera flowers and nectar are also consumed by red-tailed monkeys (Cercopithecus ascanius) (Struhsaker, 2017;Bryer, 2020), red colobus (Piliocolobus badius) (Dominy and Lucas, 2001), grey-cheeked mangabeys (Lophocebus albigena) (Rothman, unpubl. ...
Article
Full-text available
Flowers are ubiquitous in primate environments, yet their nutritional advantages are underexamined. Symphonia globulifera is a widely distributed tree exploited by a variety of animals in Africa and the Americas. We collected S. globulifera flower samples consumed by red-tailed monkeys ( Cercopithecus ascanius ) and compared them nutritionally to flower samples from other plant species in Kibale National Park, Uganda. Flowers were assayed for three fiber fractions (NDF, ADF, lignin), fat, crude protein, acid detergent insoluble nitrogen (ADIN), ash, and soluble sugars. We estimated available protein, total nonstructural carbohydrates (TNC), and metabolizable energy (ME). We calculated the mean and standard deviation for all nutrient categories and applied nutritional geometry to illustrate the balance among the energetic gains from available protein, fat, fiber, and TNC across flower species. Our results suggest that S. globulifera flowers provide an unusually high fat resource (14.82% ± 1.41%) relative to other flowers (1.38% ± 5.79%) and other foods exploited in the same habitat.
... For this, the number of records of a given food group was divided by the total number of feeding records in the study period. To assess whether there was a difference in the use of food items between the dry season (June-November) and the rainy season (December-May), we used the statistical test Z binomial (Rimolí et al. 2008), with an α = 0.01, to prevent type I errors (Lima and Ferrari 2003). We used the same test to assess if there was a difference in the time spent feeding between seasons. ...
Article
Full-text available
Little is known of the ecology of Saguinus martinsi martinsi (Callitrichidae), native to the Brazilian Amazon. In this study, we present information on its diet, and investigate seasonal changes in the feeding ecology of a group at the core of its restricted range in the Saracá-Taquera National Forest in the municipality of Oriximiná, state of Pará, Brazil. We followed the group between May 2013 and April 2014 and collected data using scan sampling, with one-minute scans every 10 minutes. This resulted in 3,230 scans equivalent to 518 hours of observation. The group's diet was composed mainly of fruits (84.5%). Those of Byrsonima crispa were the most exploited in terms of time spent feeding (20%). An average of 10 trees in fruit were visited per day in the rainy season and eight per day in the dry season. The average time spent in any tree where they were feeding was seven minutes and 32 seconds (range 1-43 minutes) overall but was shorter in the dry season than in the rainy season. More plant species were included in the diet in the wet season (41) than in the dry season (24). The scarcity of fruit in the dry season affected the dietetic diversity of the group; they exploited fewer species for fruit (and principally Byrsonima crispa and Cecropia sp.) and turned to Parkia gum as a fallback.
... However, studies from other parts of their range show that both the weeper capuchin (Cebus olivaceus) and the brown capuchin (Sapajus apella) are omnivorous, groups present a home ranges between 270 and 320 ha (Zhang 1995;Miller 1996), and population densities range between 6 and 55 individuals/km 2 (Freese and Oppenheimer 1981). The squirrel monkey (Saimiri sciureus) is mainly insectivorous-frugivorous, groups have a home range varying from 65 to 280 ha Lima and Ferrari 2003;Defler 2010), and population densities range between 16 and 528 individuals/km 2 (Baldwin and Baldwin 1981). The red-handed tamarin (Saguinus midas) is the smallest primate in the SOA, is mainly insectivorous, group home range size is 31-42 ha Day and Elwood 1999), and population densities range between 2 and 30 individuals/km 2 (Snowdon and Soini 1988). ...
Article
Full-text available
We assessed the spatial extent at which the species-landscape relationship is strongest (i.e. the scale of effect—SE) on primate occurrence (Alouatta belzebul, Saguinus midas, Saimiri sciureus, and Sapajus apella and Cebus olivaceus, the last two considered together in the analysis) and species richness and evaluated which landscape, patch, and human variables influence primate distribution in a savanna ecosystem in Brazil. We used nested buffers to measure the landscape attributes, and used these data to assess the SE of the species-landscape relationships. We explored the relative contributions of landscape, patch, and human variables to species richness and occurrences by using Generalized Linear Mixed Models and logistic regression. We found that the SE did not differ between primates, but did between two regions with different matrix composition. At the landscape level, occurrence of all species was higher as the distance to the nearest block of continuous forest decreased, but was lower as the amount of water bodies and anthropogenic cover in the matrix increased. The occurrence of S. apella, C. olivaceus and A. belzebul was positively related to forest cover, and all species but A. belzebul had higher occurrence in taller forest. The occurrence of S. apella, C. olivaceus and A. belzebul decreased closer to the city, and S. apella and C. olivaceus presence increased with the number of residents. Richness was negatively related to the number of residents and anthropogenic cover, but positively to forest height. We concluded that conservation planning for primates should follow a “functional landscape” perspective, by maintaining higher forest cover and minimizing the anthropogenic alterations in the matrix.
... Members of the genus Saimiri in their native habitat have been considered as predominantly insectivorous (Janson & Boinski 1992;Stone 2007b;Zimbler-Delorenzo & Stone 2011), insectivorous-frugivorous (Lima & Ferrari 2003) or frugivorous (Pinheiro et al. 2013;Paim et al. 2017). Our results indicate an essentially frugivorous diet for the squirrel monkeys living in the Atlantic forest, with the predominance of fruits from three exotic plant species (exotic to both Atlantic and Amazon forests). ...
Article
Inadvertent or intentional introductions of species in non-native habitats are forcing them to adapt quickly, resulting in evolutionarily-significant changes in their ecology and social organization. Understanding how these species are adapting in non-native areas will elucidate evolutionary aspects of migration and adaptation skills of exotic species in general. Thus, we investigated how Amazonian squirrel monkeys (Saimiri sciureus) have adjusted their behavioural ecology and call propagation in an Atlantic Forest fragment in North-eastern Brazil. Behavioural ecology data were obtained via instantaneous scan and ad libitum sampling methods. Call propagation data were obtained through playback experiments conducted in the Atlantic and Amazon forests. Atlantic forest squirrel monkey diet was found to be composed, primarily, of fruits considered “exotic” to the region. There was no variation between dry and wet months in food resource exploitation except for flowers. Squirrel monkeys spent most of their time engaged in locomotion and foraging activities and had a preference for the Atlantic forest mid-strata. Nevertheless, resting, locomotion and social activities were most frequently demonstrated in the dry months, whereas foraging behaviours were mostly performed in the wet months. We found no seasonal variation in the vertical use of the stratum, daily path length or home range size. The propagation of squirrel monkey isolation calls was more efficient in the Amazon compared to the Atlantic forest, with call acoustic parameters degrading faster in the Atlantic forest. Our results indicate that exotic squirrel monkeys have adjusted their activity pattern and diet in the Atlantic forest, resulting in behavioural variations consistent with the existing resources. Vocalisations, however, despite not being fully adapted for propagation in the Atlantic forest, do not appear to interfere in the occupation success of the species in the Atlantic forest
... Saimiri oesterdii tem sua ocorrência restrita à Costa Rica, América Central. A maioria das pesquisas com macacos-de-cheiro estão voltadas principalmente a questões biomédicas e, no Brasil, tópicos com ênfase em ecologia e comportamento de apenas poucas espécies (S. vanzolinii, S. macrodon, S. cassiquiarensis e S. coliinsi) foram investigados (Lima & Ferrari 2003, Paim 2008, Paim & Queiroz 2009, Pinheiro et al. 2011Ruivo & Stone 2014;Stone 2006Stone , 2007aStone , 2007bStone , 2008. Estudos de campo envolvendo S. ustus, S. sciureus e S. boliviensis (consideram-se para as duas últimas espécies apenas as populações restritas ao Brasil) nunca foram realizados e pouco se sabe sobre fatores de ameaça. ...
Article
Full-text available
The Mamirauá Sustainable Development Reserve (MSDR) is the largest protected area dedicated to the conservation of biodiversity in floodplain forests. Primate richness there is one of the highest in an Amazonian protected area, but primatological studies are still incipient. The black-headed squirrel monkey (Saimiri vanzolinii) was described in 1985, but the first studies on the species only began more than two decades later. This ‘Vulnerable’ species is endemic to the area, and its geographic distribution is only 870km². Two other squirrel monkeys (S. cassiquiarensis and S. macrodon) occur in the area, and have peripatric distributions with S. vanzolinii, including contact zones on the bordering regions. These peripatric species have large geographic distributions and their conservation status is “Least Concern”. Phylogenetic studies have determined that the three Saimiri taxa are considered valid species. Bioacoustic and morphological analyses corroborated the previous study, demonstrating differentiation between the species. The main incentive for starting a long-term research was program was interest in investigating the reasons for S. vanzolinii’s limited range. Aspects related to ecology, behavior, taxonomy, and phylogenetic and historical biogeography are essential to understand the current pattern of geographic distribution of the squirrel monkeys in Mamirauá. These aspects are also important in the planning of conservation strategies, especially for S. vanzolinii. Studies being conducted in the MSDR are focusing on the floristic communities comprising the ranges of these species, and availability of food sources and their presence in the diet. These questions will help us understand whether evolutionary processes, such as competitive exclusion, might be affecting S. vanzolinii and consequently contributing to its natural extinction process. The major concern about the species relates to climate change, with models indicating an increase in the intensity and frequency of flooding in the region of the middle Rio Solimões. Logging in the region may also be contributing to environmental changes. The association between these two factors could result in habitat loss for S. vanzolinii, increasing its risk of extinction. Management of ex situ breeding colonies of S. vanzolinii should be considered as an additional conservation strategy.
Article
Many mammals coincide their reproductive activities with factors such as ambient temperature, rainfall, and food availability. In primates that invest immediate food intake into reproduction, the periods of maximum fruit production often coincide with the peak of lactation (to maximize maternal survival) or the occurrence of weaning (to maximize infant survival). This study investigates the relationship between reproductive periods and the availability of ripe fruit in the habitat of a population of wild squirrel monkeys (Saimiri collinsi) in Amazonian Brazil. We combine data from several years (2002–2003; 2011–2015) during which we followed the monkeys and quantified the occurrence of matings, gestations, births, and the number of lactating females. We also collected rainfall and plant phenological data for 24 months. Our results confirm that reproductive events are highly seasonal in S. collinsi. The period of weaning corresponded to the peak in the abundance of ripe fruits consumed by the monkeys. This indicates that the period of infant nutritional independence is optimally timed to coincide with periods of greater food production in this habitat. We suggest that seasonal breeding in these primates does not necessarily reduce maternal energetic stress, but likely improves infant survivorship. Research Highlights • Squirrel monkeys in Eastern Amazonia are seasonal breeders, with the weaning period, rather than the birth peak/early lactation, matching the peak of fruit availability in the environment. • This species of squirrel monkey are income‐I breeders, where seasonal breeding maximizes weanling survival.
Article
A dieta do gênero Saimiri ainda é pouca relatada na literatura. Devido ao reduzido número de investigações realizadas sobre o assunto, este estudo teve como objetivo realizar um registro dos frutos que integram a dieta de Saimiri sciureus collinsi em ambiente natural em dois fragmentos de florestas distintas em uma unidade de conservação localizada em Soure, Ilha do Marajó, Amazônia Oriental. O estudo foi realizado durante 9 meses e dividido em 3 etapas: a) habituação (fevereiro a abril de 2014), b) observações na mata da Betânia (maio a julho de 2014) e c) observações no sítio Vila Nova (agosto a outubro de 2014). As incursões a campo ocorreram em média 3 vezes por semana, entre 5 horas e 30 minutos e 8 horas da manhã e entre 15 horas e 17 horas da tarde. Foram registrados um total de 15 espécies de frutos consumidos pelos Saimiri sciureus collinsi pertencentes as seguintes famílias: Arecaceae (n=2), Anacardiaceae (n=2), Sapotaceae (n=2), Humiriaceae (n=2), Myrtaceae (n=1), Passifloraceae (n=1), Rubiaceae (n=1), Chrysobalanaceae (n=1), Mimosoideae (n=1), Siparunaceae (n=1) e Malpighiaceae (n=1). Por existir uma indisponibilidade de dados científicos sobre a ecologia alimentar, principalmente relacionadas aos itens vegetais (frutos), de Saimiri sciureus collinsi, este estudo acrescentou novas informações acerca dos frutos consumidos por estes animais, principalmente para a região da Ilha de Marajó, Amazônia Oriental.
Article
China's Belt and Road Initiative (BRI) is an unprecedented global development program that involves nearly half of the world's countries [1]. It not only will have economic and political influences, but also may generate multiple environmental challenges and is a focus of considerable academic and public concerns [2–6]. The Chinese government expects BRI to be a sustainable development, paying equal attention to economic development and environmental conservation [7]. However, BRI's high expenditure on infrastructure construction, by accelerating trade and transportation, is likely to promote alien species invasions [5], one of the primary anthropogenic threats to global biodiversity [8]. BRI countries may have different susceptibilities to invasive species due to different financial and response capacities [9]. Moreover, these countries overlap 27 of 35 recognized global biodiversity hotspots [10]. Identifying those areas with high-invasion risks, and species with high invasive potentials within BRI countries, is therefore of vital importance for the sustainable implementation of the BRI, and the development of early, economical, and effective biosecurity strategies [11]. In response, we present here a comprehensive study to evaluate invasion risks by alien vertebrates within BRI. We identified a total of 14 invasion hotspots, the majority of which fall along the six proposed BRI economic corridors, with the proportion of grid cells in invasion hotspots 1.6 times higher than other regions. Based on our results, we recommend the initiation of a project targeting early prevention, strict surveillance, rapid response, and effective control of alien species in BRI countries to ensure that this development is sustainable.
Thesis
This thesis presents the results of the first long-term field study of the buffy-headed marmoset, Callirhrix flaviceps, a rare primate species with a small natural range in southeastern Brazil. The introductory discussion presents the species in the context of a review of the available literature on the taxonomy, evolution, behaviour and ecology of the primates of the family Callitrichidae. The study animals, study site and methodology are then described. A detailed description of seasonal fluctuations in the abundance and distribution of dietary resources at the site provides a frame of reference for the analysis of the study group's behaviour. General patterns in the group's use of time and space are outlined in the context of these variables and comparisons are made with other callitrichid species. A number of behavioural strategies are identified. A more detailed analysis of seasonal patterns in the group's foraging and feeding behaviour emphasizes the systematic nature of its exploitation of resources. The gum-feeding adaptation of the marmosets is seen as having far-reaching implications for many aspects of their behaviour and ecology. Behavioural specialisations for the capture of certain types of prey and the exploitation of secondary and disturbed forest habitats are also proposed. It is concluded that most features of the group's foraging behaviour support predictions drawn from optimality models, in the context of an overall 'time-minimising' strategy in particular. As much of the behavioural repertoire of this species appears to be broadly similar to that of other callitrichids, these findings offer a number of important insights into their ecological adaptations.
Article
The findings are presented from a 10-week field study on Saimiri oerstedi during mating season in southwestern Panama. The main study troop consisted of 23 monkeys. It used a home range of 0.175 km2 (43.5 ac) which was not a defended territory. Food was apparently scarce and the monkeys spent 95 % of each hour of their 14-hour day engaged in travel and foraging. Adult females, infants, juveniles and sub-adult males traveled as a cohesive, integrated unit. The troop’s 2 adult males usually traveled at the edge of the troop. A young adult male traveled further at the periphery of the troop. All overt social interactions were infrequent.
Article
Weekly sweeps for arthropods were taken and compared for an entire year (1977) on Grenada, West Indies, where there is a marked wet and dry season. The average wet-season abundance of arthropods was 2.3 times greater, and the wet-season biomass (grams) was 3.1 times greater, than that for the dry season. A significant correlation between biomass and abundance existed for the entire year. There was no change in arthropod size between wet and dry season. Intra-seasonal variations in arthropod abundance occurred, and were significantly correlated with seven-day accumulated rainfall following a three-week interval. Abundance of seven of 10 taxa showed the same three-week response to rain-fall. Coleoptera were identified to species, so that species diversity, species overlap, and feeding guilds for the entire year could be compared to Central American Coleoptera. The results indicate the Coleoptera fauna on Grenada are more generalized compared to the tropical mainland, and composed of the same species whose abundance fluctuates seasonally throughout the year.
Article
1. Male South American squirrel monkeys form groups whose composition remains stable over migrations between troops. These groups are called 'migration alliances'. 2. Members of migration alliances support one another against other males through coalitions in genital display bouts both during immigration and throughout the year. Male alliances do not function to overcome female dominance. 3. Seasonal reproduction in squirrel monkeys may influence male alliances by a) intensification of within-group competition during the mating season, and b) production of temporally and spatially fluctuating mating opportunities between groups.
Article
An electrophoretic survey of 15 protein systems (22 loci) was employed to determine the genetic relationships among 9 populations (441 individuals) of South American squirrel monkeys (Saimiri sciureus sciureus, S. sciureus boliviensis, and S. sciureus ustus). Genetic markers capable of differentiating the second from the two other taxa were observed mainly in the ADA and GPI systems. Heterogeneity for ADA and CA2 between populations from opposite banks of the Jamari river was verified in S. sciureus ustus. The average heterozygosities ranged from 3% to 5%, the lowest being in S. sciureus sciureus and the highest in S. sciureus boliviensis. Low genetic distances (D = 0.001−0.057) were observed between populations within taxa or between S. sciureus sciureus and S. sciureus ustus. But both differed to a larger extent from S. sciureus boliviensis (D = 0.11 in both comparisons). There is a positive correlation between the genetic and geographic distance matrices. The three taxa are more clearly separated (D = 0.76–0.77) from the outgroup used for comparison (Cebus apella). Our data suggest that there is only one large, polytypic species of squirrel monkeys in South America, S. sciureus, forming a contiguous ring of geographical races or subspecies. Two of the most differentiated forms meet at the Peruvian Amazonia where natural hybrids and secondary intergradation have been reported. © 1993 Wiley-Liss, Inc.
Article
The effects of sex and seasonal changes in food abundance on foraging behavior was studied in squirrel monkeys (Saimiri oerstedi) in Costa Rica over an eleven-month period. Females searched for and ate food at significantly greater frequencies than did males throughout the study. The frequency of the specific foraging techniques used occasionally differed significantly within seasons, but not across the study period. Few differences were found in the foraging behaviors of nonreproductive sexually mature females compared to females that were pregnant or lactating. The major exception was that during the month following parturition reproductive females foraged for flowers and fruits more frequently than did non-reproductive females. The reduction of time spent by males in foraging activities gives them more time for other activities, especially anti-predator vigilance. Foraging techniques and the proportions of different food types in the diet changed seasonally. Foraging for arthropods was most frequent in the season when arthropod abundance was lowest, resulting in the amount of time spent eating arthropods to vary less across the seasons. Fruits and flowers were not eaten in a direct relationship to availability, but were used more than expected relative to availability when arthropod abundance was reduced. Individuals were more dispersed when foraging compared to other activities. Overall, there was little evidence of any direct foraging benefits for a squirrel monkey from being social.
Article
Continuous focal recordings were collected of the vocalizations of 21 marked adult female squirrel monkeys, Saimiri oerstedi, in their natural Costa Rican habitat. Concurrent data were also obtained for each focal female on her foraging activity, distance from the nearest neighbouring adult female, spatial position within the troop, and ongoing troop activities and movements. A cumulative 18·6 h of continuous samples and 3080 sonagrams were analysed. Consistent with earlier studies, four major call types were identified: smooth chuck, bent mast chuck, peep and twitter. As the distance from the nearest adult female increased, the rate of vocalizations increased dramatically, the peep call disproportionately so. A rapid rate of vocalization, with an increased proportion of twitters and a decreased proportion of bent mast chucks, was strongly associated with the initiation of troop movement and with females in the vanguard of a moving troop. No direct relationship was found between foraging and vocal behaviour. Even the most narrowly defined call types were likely to be uttered in sequences. There was no evidence that sequential patterns of calls (syntax) differed across contexts.