Feeding behavior of Geoffroy's marmoset - Springer Link

PRIMATES,41 (1): 27-38, January 2000

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Feeding Behavior of Geoffroy's Marmoset (Callithrix geoffroyi) in an Atlantic Forest Fragment of South-eastern Brazil MARCELOPASSAMANI Universidade Federal de Minas Gerais, Brazil

and Museu de Biologia Prof Mello Leit6o, Brazil and ANTHONY B. RYLANDS Universidade Federal de Minas Gerais, Brazil and Conservation International do Brasil

ABSTRACT. We report on the diet and feeding behaviour of a group of Geoffroy's marmosets (Callithrix geoffroyi) in an Atlantic forest fragment in south-eastern Brazil, studied during the period February 1993 to January 1994. Major food categories were gums (68.6 %), fruits (15%), and small animal prey (invertebrates 14.6% and vertebrates 0.8%). Dietary changes were observed between the wet and dry seasons, although they were not statistically significant. Insects and gums were consumed throughout the year but fruits were more prevalent in the diet in the wet season. Plant species exploited for their gums included lnga stipularis, followed by Acacia paniculata, Paulinia carpopodia, and Bauhinia angulosa. Chemical analysis of the gum of the four species most used all presented high values for carbohydrates and crude proteins. Fruits of an unidentified species of Myrtaceae (sp. 2) were consumed the most. Animal prey consisted mainly of insects, arachnids, snails, and in three cases, lizards and frogs, with orthopterans being the most prevalent insect prey. This study demonstrates that C. geoffroyi efficiently exploits resources typically available in secondary and disturbed forest habitat. The main threat to the species is forest destruction, degradation, and fragmentation, but the management of small forest fragments may be an effective conservation strategy. Key Words: Callithrix geoffroyi; Geoffroy's marmoset; Diet; Feeding ecology; Atlantic forest.

INTRODUCTION Callitrichid diets include principally fruits, gums, and insects and small vertebrates, and occasionally or seasonally, nectar and fungi (GARBER, 1980, 1984; RYLANDS, 1982; SUSSMAN & KINZEY, 1984; FERRARI, 1988; SNOWDON t~ SOINI, 1988; STEVENSON• RYLANDS, 1988; PERES, 1993; RYLANDS t~Z FARIA, 1993; CORRI~A, 1995). Marmosets, Callithrix and Cebuella, have anatomical and behavioural adaptations for tree-gouging, which sets them apart from the tamarins, Saguinus, and lion tamarins, Leontopithecus, which eat gums opportunistically (COIMBRA-FILHO, 1972; COIMBRA-FILHO ~Z MITI'ERMEIER, 1976, 1977; COIMBRA-FILHO et al., 1980; ROSENBERGER, 1992; RYLANDS & FARIA, 1993). The contribution of gum to the diet has been observed to be seasonal and related to the availability of fruits; some marmoset species reduce gum intake when fruits are more abundant (RYLANDS, 1984, 1986; ALONSO & LANGGUTH,1989). Invertebrates, mainly insects, are another important item in the marmosets' diet, and foraging for small animal prey takes up a large part of the day of all callitrichid species studied to date (RYLANDS,1982; SUSSMAN t~ KINZEY, 1984; FERRARI, 1988; STEVENSON& RYLANDS, 1988; CORREA, 1995; PASSAMANI, 1998).

28

M. PASSAMANI& A. B. RYLANDS

Geoffroy's marmoset (Callithrix geoffroyi), one of the six species comprising the marmoset radiation in the Atlantic forest of Brazil (RYLANDS et al., 1996), occurs throughout the lowland forests (below about 500 m altitude) north of the Rio Doce in the state of Espfrito Santo, extending into southern Bahia and adjacent parts of the state of Minas Gerais (RYLANDS et al., 1993). Preliminary information on C. geoffroyi was provided by RYLANDS and COSTA (1988) and PRICE (1993), but little is known on their feeding behaviour. In this paper, we report on the diet of a single group of these marmosets, presenting a quantitative analysis of the items and species consumed, and their seasonality. We also examine the nutritional composition of some of the gum species they eat.

METHODS THE STUDY SITE This study was carried out in an Atlantic forest patch of approximately 110 ha belonging to Aracruz Celulose S.A., a privately-owned company in the state of Espfrito Santo, south-eastern Brazil (19~ 40~ It is isolated by Eucalyptus plantations, and was selectively logged in the past, resulting in the proliferation of lianas and secondary vegetation up to 10 m of height (MEIRA-NETO, 1992). The climate of the region is characterized by a dry season, with less than 70 mm rainfall each month, from July to November, and a wet season from December to June. Average annual rainfall is around 1050 mm (unpublished records from February 1993 to January 1994; Aracruz Celulose S.A.). The average temperature is 23~ but it is slightly cooler from May to October (including most of the dry season) with monthly means ranging from 20.9~ to 23.8~ than from November to April (early to middle of the wet season), with monthly mean temperatures ranging from 25.9~ to 27.8~ (unpublished records from February 1993 to January 1994; Aracruz Celulose S.A.). THE STUDY GROUP In February 1993, at the beginning of systematic observation, the study group was composed of one adult female, two adult males, and two juveniles (estimated born in November 1992). One of the adult males had been trapped (November 1992), sedated with Ketamine, and fitted with a radio-collar (Wildlife Materials, Inc.). In September 1993, the female produced twins, which however disappeared in October 1993. In this same month, one adult male and one juvenile emigrated. From October 1993 to January 1994, therefore, the group was comprised of one adult female, an adult male, and a subadult male. DATA COLLECTION Following two months of habituation, data was collected systematically from February 1993 to January 1994. In January 1994, the group was observed during three complete days, four days each in October and December 1993, and five days in each of the remaining months; a total of 56 complete days and 464.1 hr of direct observation. Instantaneous scan sampling during one minute, with a 4-min interval between scans (ALTMANN,1974) was used to record the feeding of all individuals except for dependent infants. Feeding was recorded when the animals were biting, chewing, swallowing, or manipulating any kind of food. Whenever possible, the food item was noted, and classified as gums, fruits, inver-

Diet and Feeding Behavior of Geoffroy's Marmoset

29

tebrates, or small vertebrates. When the food eaten could not be discerned, it was scored as unidentified. Food trees and lianas used were marked with coloured flagging tape whenever the species was not identified in situ. Voucher specimens were subsequently collected and deposited at the herbarium of the Museu de Biologia Professor Mello Leitao, Santa Teresa, Espffito Santo. Fresh samples of gums of the species most used by the group were collected and sent to the Department of Microbiology of the Universidade Federal de Minas Gerais for analysis of the nutritional composition. The proportion of feeding time the group devoted to different food types was calculated by dividing the number of feeding records for a particular food type by the total number of feeding records. The data for each were combined to compare months, and months were combined to compare seasons; July to November (dry season) and December to June (wet season). The Mann-Whitney 'U' test (SIEGEL, 1956) was used to examine differences in the percentage of records for each type of food between seasons. The Spearman rank correlation coefficient (r 2) was used to test for a relation between the contribution of different species of trees or lianas in the diet and the number of individuals used (SIEGEL, 1956).

RESULTS MONTHLY AND SEASONAL VARIATION IN THE DIET

Of the 9,013 records obtained over 464.1 contact hours with the study group, 1,848 were of feeding. The marmosets were observed to feed on gums in 68.6 % of these records, on fruits in 15%, invertebrates in 14.6%, and on small vertebrates in 0.8%. The food type was not identified for 1% of the records. Gums were the most frequently recorded food resource in the majority of the months and only in December and January were fruits predominant, representing 42.3% and 43% of the diet, respectively. In other months, the percentage contribution of fruits to the diet was lower, reaching only 1% in May (Fig. 1). Invertebrates were consumed in all months, representing between 5% (in February) and 25%

Fig. 1. Monthly variation in consumption of the main food categories by the C. geoffroyi study group during the period February 1993 to January 1994. T: Total consumption of the year.

30


(in November) of the total feeding records. Small vertebrates were eaten rarely, observed only in September and October (Fig. 1). There was a tendency for the marmosets to eat more fruits in the wet season, due mainly to the months of December and January, when fruits of an unidentified species of Myrtaceae were important. The difference in diet between the wet season and the dry season, however, was not statistically significant (Table 1). In July and August (dry season), the group eat fruits of a single Acanthinophylum ilicifolia tree and some Miconia trees. Gums comprised 66% of the feeding records in the dry season and 70.4% in the wet season, and the proportion of records for invertebrate prey also showed no significant difference between the seasons (19.3% in the dry season and 11% in the wet). GUM-FEEDING Gums were an important component of the diet of C. geoffroyi throughout the year, and were only eaten less frequently during the months of December and January, when fruit feeding was more prevalent (Fig. 1). All of the species of trees and lianas providing gum were actively gouged by the marmosets, except for Dyctioloma incanescens, on which the animals spent a large amount of time searching for gums exuded, apparently, in response to insect damage. After a variable period of use, the natural healing process caused the gouge-holes to close, and the trees were subsequently abandoned. The animals gouged trees in a rotational manner, although some individual trees were used daily over several months. The majority was abandoned at some stage. Twelve species of trees and lianas were identified which were used as sources of gums during this study; eight of them (64.5%) were from the family Leguminosae (Table 2). The other species belonged to the families Sapindaceae, Rutaceae, and Anacardiaceae. Gum of lnga stipularis was the most consumed, representing 28.5% of the feeding records for this food type, followed by Acacia paniculata (22.3%), Paulinia carpopodia (19.2%), and Bauhinia angulosa (8.3%). The remaining species, including those unidentified, represented 21.7% of the time spent feeding on gums. The study group used 216 individual trees and lianas, and the contribution of each species to the gum portion of the diet was correlated with the number of individual trees or lianas the study group used (r2=0.574, n = 12, p=0.004). The monthly variation in the top four species used as gum sources, which represented 78.3% of the total gum-feeding records, is shown in Figure 2. lnga stipularis was mostly used from February until June, decreasing by the end of study period. Paulinia carpopodia was most used between July and October, and A. paniculata was first used intensively in September, reaching its peak in December.

Table 1. Percentage of records for different food items consumed by the C. geoffroyi study group for each season. Items consumed Season Gums Fruits Insects Vertebrates Unidentified Dry 66.0 12.5 19.3 0.5 1.7 Wet 70.4 17.0 11.14 0 1.4 U 491.0 424.5 321.5 * N 58 58 58 * p 0.218 0.849 0.153 * U: Mann-Whitneytest; N: sample size; p: probabilities associated with the test; .: insufficient data for the test.


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Table 2. Monthly and total percentage of records of each species providing gums in the diet of the C. geoffroyi study group. Species (life forms) N Total Leguminosae Inga stipularis (T) 361 28.5 lnga thibaudiana (T) 20 1.6 Inga sp. (T) 23 1.8 Acacia paniculata (L) 282 22.3 Mimosa sp. (L) 9 0.7 Bauhinia angulosa (L) 105 8.3 Bauhinia sp. (L) 8 0.6 Hymenaea courbaril (T) 9 0.7 Sapindaceae

Paulinia carpopodia (L)

164

!9.2

26

2.2

86 6

6.8 0.5

86

6.8

Anacardiaceae

Tapirira guianensis (T) Rutaceae

Dictyoloma incanescens (T) Zanthoxylon sp. (T) Others unidentified T: Tree; L: liana; N: total numberof feedingrecords.

CHEMICAL ANALYSISOF GUMS The data obtained from the chemical analysis of the top four species used as gum sources are shown in Table 3. All species presented high values for carbohydrates, ranging from 73.5% in P. carpopodia to 81.4% in B. angulosa. For P carpopodia and A. paniculata crude protein content was also quite high; 15.2% and 10.8%, respectively. Ash values were a little less than 2%.

Fig. 2. Monthly variation in the percentage of records for four species providing gums in the diet of the C. geoffroyi study group.

32

M. PASSAMANI& A. B, RYLANDS

Table 3. Nutritional composition of the top four species providing gums in the diet of the C, geoffroyi study group. Composition (%) Moisture Crude protein Ether extract Carbohydrates Ash Total (%)

Acacia paniculata

Paulinia carpopodia Bauhinia angulosa

5.3 10.8 2.3 79.7 1.9

6.6 15.2 2.8 73.5 1.9

100

Dyctioloma incanensis

7.6 6.3 2.8 81,4 1.9

100

6.5 7.1 3.4 81.1 1,9

100

100

Table 4. Monthly and total percentage of records for each species providing fruits in the diet of the C. geoffroyi study group from February 1993 to January 1994. Species (life forms)

1993 F M

A

M

J

J

A

S

O

N

D

1994 J

N

Total

Euphorbiaceae

Pera leandri (T)

1.5

4

1.5

2

0.7

23

8.5

4

1.6

I 44

0.4 16.1

Annonaceae

Annona longifolia (T)

0.7

Sapindaceae

Allophyllus edulis (T)

8.5

Menispermaceae Abuta sp. (L)

0.4

0.4

0.4 0.4

Moraceae

Cecropia sp. (T) Acanthinophylum iliclfolia (T)

0.4 14.3 1.8

Leguminosae (Mimosoideae) Inga stipularis (T)

2,6

7

2.6

Sapotaceae Unidentified (T)

1.5

4

1.5

Myrtaceae

Campomanesia sp. (T) Unidentified spl. (T) Unidentified sp2. (T) Unidentified sp3. (T)

1. I 1.1 26.1 18.3 3.3 1.1

Melastomataceae Miconia sp. (T)

4.8 2.9

Chrysobalanaceae Unidentified(T)

2.2 0.4 0.4

3 1.1 3 IA 121 44.4 12 4.4

21

7.7

8

3.0

Boraginaceae

Tournefortia sp. (L) Unidentified (L)

3.7 0.7

10 2

3.7 0.7

Solanaceae Unidentified (T)

0.4

I

0.4

0.4

2

0.8

Unidentified (L)

0.4

T: Tree; L: liana; N: total number of feeding records.


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FRUITS The study group was observed eating fruits of 18 plant species from 13 families, although in most cases, the number of feeding records for any particular species was very small (Table 4), indicating that fruit consumption is opportunistic. All of the fruits eaten were small and easily accessible to the marmosets. With the exception of L stipularis, where the animals bite open the pod to extract the seeds and hold them to eat the aril, for all other species the marmosets detach the fruits directly from the plant with their mouth, or bring them to the mouth with their hands. They swallowed the seeds of the fruits of Miconia sp., Cecropia sp., and Tormefortia sp. Fruits of one species of Myrtaceae (unidentified sp.2) contributed most to the fruit part of the diet, representing 44.4% of the total fruit consumption (Table 4). The fruiting periods the two most consumed species of Myrtaceae (unidentified sp.2 and sp.3) coincided. The high consumption of these Myrtaceae species can be attributed to the proximity of the individual trees, forming groves frequently visited by the study group. It was only during the fruiting period of these two species (December and January) that the consumption of fruits was higher than that of gums (see Fig. 1). Acanthinophylum ilicifolia was the second most important species (16.1%). The other 16 species included in the fruit part of the diet contributed relatively little, and for 12 of them feeding was recorded on only eight occasions (3%) or less. ANIMAL PREY Prey captured by the marmosets included insects, arachnids, gastropods, lizards (Anolis), and frogs (Hyla). Orthopterans were the most frequently ingested prey, comprising 71.3% of the species identified (Table 5). Gryllidae predominated, representing 19.4% of the identified prey captured. They were caught especially when the marmosets were foraging above ant swarms. Other orthopterans captured included stick-insects (Phasmidae), katydids (Tettigoniidae), prey-

Table 5. Invertebrates and small vertebrates consumed by the C. geoffroyi study group during the study. Prey item N % of total identified Invertebrates Orthoptera 144 71.3 Gryllidae 28 19.4 Phasmidae 19 13.2 Tettigoniidae 16 11.1 Mantidae 7 4.9 Blattidae 2 1.4 Acrididae 1 0.7 Undetermined 71 49.3 Coleoptera 8 4.0 Lepidoptera 3 1.5 Homoptera 2 1.0 Immature forms 4 2.0 Arachnida 9 4.5 Gastropods 27 13.3 Vertebrates Frog (Hyla sp.) Lizard (Anolis sp.) Total N: Total number of feeding records.

3 2

1.5 1.0

202

100.0

34

M. PASSAMANI8Z A. B. RYLANDS

ing-mantis (Mantidae), cockroaches (Blattidae), and short-horned grasshoppers (Acrididae), respectively (Table 5). To capture prey, the animals moved quickly on horizontal and vertical substrates searching attentively along branches and vines, and below leaves. This foraging was typically an individual behaviour, occurring at any time of the day, and often when other group members were involved in other behaviours. The entire group foraged together, however, when following army ant swarms, Eciton burchelli. This was seen on three occasions, each lasting approximately 2 hr, when the marmosets would place themselves within a meter of the ground, above and in front of the swarm, frequently going down to capture prey disturbed by the ants, mainly crickets (Gryllidae), and spiders (Arachnidae). Snails (Gastropods) were an important item in the diet (13.4% of animal prey feeding records), breaking the shell at the apex with their teeth. Small vertebrates were eaten on only five occasions during the period of systematic observations (Table 5).

DISCUSSION Some information on the diet of C. geoffroyi was obtained by RYLANDSand COSTA (1988) at the Peti Station, Minas Gerais and by PmCE (1993) at the Linhares Reserve of the Companhia Vale do Rio Doce, Espfrito Santo. However, those studies were of short duration, and the importance of each food item in the diet and its seasonal variation were not quantified. Contributions of the main food categories to the diet of the study group were very similar to those observed for other species of marmosets, especially with regard to gums which are consumed throughout the year (RYLANDS, 1982; FONSECA & LACHER, 1984; FERRARI, 1988; ALONSO& LANGGUTH, 1989). As in other species of marmoset, C. geoffroyi reduce their gum intake in favour of fruit when they are plentiful. Insects and gums were consumed regularly throughout the study period, whereas fruits were more seasonal, consumption depending on their availability and abundance. Similar behaviour has been observed in Callithrixflaviceps and Callithrix aurita (FERRARI, 1988; CORRI~A, 1995), both of which that increased their fruit consumption during the wet season. The study group eat gums of 12 species of trees and lianas, and, as has been observed for other marmosets (RYLANDS, 1982, 1984; STEVENSON & RYLANDS, 1988; FERRARI, 1988), Leguminosae was the most important source family. Although L stipularis was the most important species providing gum in the first months of the study, gums of liana species were used more heavily by the group overall. The high abundance of lianas in this fragment, especially Bauhinia spp. (Leguminosae) and Paulinia (Sapindaceae) (MEIRA-NETO, 1992), may have influenced directly their use by the study group, indicating a flexibility in the diet of these animals, with the most abundant plants being also the main food sources. Gums of the A. paniculata and P. carpopodia were one of the most used by the marmosets, and contained high percentages of crude protein; possibly an important factor determining their consumption, although further studies are required to verify if these species of gum sources are also those occurring in the highest densities in the area. Other studies, such as those of LACHER et al. (1984), FONSECA and LACHER (1984), and PASSAMANI(1996b), have demonstrated that C. penicillata, at least, uses gum trees according to their abundance. SILVA (1993) observed that genera such as Bauhinia and lnga occur at high densities in secondary forests, a fact that may contribute to their preference for this type of habitat. The large number of trees and lianas used as gum sources demonstrates that C. geoffroyi can monitor their resources in a manner to assure its continuous supply during certain times in the year. FERRAR! (1988) observed a similar pattern in C. flaviceps. Groups of C. geoffroyi were observed at the Peti Station, Minas Gera]s, feeding


35

on gums ofAnadenanthra macrocarpa (RYLANDS & COSTA, 1988), and at the Linhares Reserve, Espffito Santo, they fed on gums of Sterculia speciosa and Spondias macrocarpa (PRICE, 1993). These species did not occur in the range of our study group, demonstrating again the varied and opportunistic diet of these marmosets. Gums are composed of complex polysaccharides, crude proteins, and minerals (ANDERSON et al., 1972; ANDERSON 8,: GILL, 1975; BEARDER & MARTIN, 1980; POWER, 1996). These authors have reported low levels of crude proteins in gums, much lower than that found by us for A. paniculata and P. carpopodia gums, much used by the marmosets in this study. Because of the low levels in gums, SUSSMAN and KINZEY (1984) argued that the small marmosets depend on insects for their crude protein needs, but for C. geoffroyi, at least, it would seem that gums can also act as an important source. Besides A. ilicifolia, another important fruit source in the dry season was Miconia (Melastomataceae); trees typical of secondary forests in the region, and with the various species producing small quantities of fruits for extended periods throughout the year (OPLER et al., 1980). Some of these species provide a continuous and relatively stable supply of food to small primate species, even during the dry season when fruits are usually scarce (SuSSMAN & KINZEY, 1984; RYLANDS, 1989). Species with these characteristics were also the main source of fruits eaten by Callithrix intermedia, C. flaviceps, and C. aurita (RYLANDS, 1986; FERRARI, 1988; CORR~A, 1995). In this study, the synchronous fruiting of several Myrtaceae trees contributed significantly to the increase of fruit consumption during the wet season. Although insect populations tend to increase when rainfall is higher (JANZEN, 1973; JANZEN & SCHOENER, 1968; FERRARL 1988), we did not observe differences in the consumption of insects by the marmosets in the different seasons throughout the year. It may be that the decrease of the number of insects during the dry season is compensated by an increase in the area used for foraging by this group (PASSAMANI,1996a). In this case, it seems that the use of this resource is directly related to habitat quality. The group concentrated its foraging along the edges of the forest and in areas with secondary growth, where insects tend to be more abundant (LovEJOY et al., 1986). FERRAR1 (1993) concluded that marmosets prefer dense vegetation in the lower strata of disturbed forests to prey on a greater variety of insects there, mainly Orthoptera. As in several other Callithrix species (C. flaviceps: see FERRARI, 1988; C. aurita: see CORR~A, 1995; C. intermedia and C. kuhli: see STEVENSON& RVLANDS, 1988), Orthoptera comprised the main prey eaten by C. geoffroyi. Foraging above army ant swarms, where large numbers of prey, especially spiders and crickets, are disturbed and exposed by the swarm, has also been observed in C. geoffroyi in Minas Gerais (see RYLANDS & COSTA, 1988), as well other marmosets (FERRARI, 1988; RYLANDSet al., 1989). In general, this study demonstrates that C. geoffroyi are adapted to the exploitation of resources typically available in secondary and disturbed forest habitats (RYLANDS et al., 1996). The contribution of gums in the diet of C. geoffroyi seems to be greater than in other species except for C. jacchus, and is undoubtedly a key factor in allowing for their permanence in small and highly seasonal forest patches. Although the main threat to this species, and other marmosets, is the fragmentation of their habitats (MENDES, 1995; PASSAMANI, 1996a), the management of available forest fragments, guaranteeing key food sources, could be a most effective conservation strategy for this and other Atlantic forest primates (MENDES & CHIARELLO, 1993; CHIARELLO& GALLETI, 1994; FERRARI & DIEGO, 1995).

Acknowledgements. The field study reported here formed part of the requirements for the Master's course in Ecology, Conservation and Wildlife Management of the Institute of Biological Sciences, Federal University of Minas Gerais, Belo Horizonte. It was kindly financed by Aracruz Celulose S.A. and sup-

36

M. PASSAMANIt~ A. B. RYLANDS

ported by the Museu de Biologia Mello Leit~o. The research was also supported by a grant from the Brazil Science Council (CNPq), and the United States Fish and Wildlife Service (USFWS) through the Funda~:~o Biodiversitas, Belo Horizonte. 1 am grateful to A. G. CH1ARELLOfor their critical comments, and S. G. PACCAGNELLA,ARACRUZCELULOSES.A., kindly provided essential logistical support. L. E L. FERNANDES reviewed the English version of the text. I am grateful to J. NIcou for chemical analysis of gums, and S. L. MENDESand J. A. PASSAMANIassisted with the fieldwork.

REFERENCES

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Received: December 9, 1998; Accepted: August 27, 1999

Authors" Names and Addresses: MARCELOPASSAMAN1,Museu de Biologia Prof. Mello Leit6o, Av. Josg Ruschi 04, 29650000, Santa Teresa, Espfrito Santo, Brazil and Department of Zoology, lnstituto de Ci~ncias Bioldgicas, Universidade Federal de Minas Gerais, 31270-901 Belo Horizonte, Minas Gerais, Brazil. e-mail: [email protected]; ANTHONY B. RYLANDS,Department of Zoology, Instituto de Ci~ncias Bioldgicas, Universidade Federal de Minas Gerais, 31270901 Belo Horizonte, Minas Gerais, Brazil and Conservation International do Brasil, Av. Anti)nio Abrah6o Caram 820/302, 31275-000, Belo Horizonte, Minas Gerais, Brazil.