The Distribution, Habitat Use, and Conservation ...

Int J Primatol DOI 10.1007/s10764-015-9884-7

The Distribution, Habitat Use, and Conservation Status of Three Atlantic Forest Monkeys (Sapajus xanthosternos, Callicebus melanochir, Callithrix sp.) in an Agroforestry/Forest Mosaic in Southern Bahia, Brazil Kevin Michael Flesher 1

Received: 9 June 2015 / Accepted: 27 October 2015 # Springer Science+Business Media New York 2015

Abstract If we are to develop effective conservation strategies for primates in heavily disturbed biomes, we must understand why they persist or perish in human-dominated landscapes. I investigated the potential of an agroforestry/forest mosaic in the Atlantic forest of Bahia, Brazil to sustain populations of three monkey species —capuchins (Sapajus xanthosternos), titi monkeys (Callicebus melanochir), and marmosets (Callithrix sp.)— sampling the primates in three forest and four agroforestry landscapes across a 1000 km2 landscape during a 17-yr study. I used 754 km of transects, reconnaissance walks, semistructured interviews, and key informant reports to collect information on the monkeys. Capuchins and titi monkeys are mostly restricted to the largest forests, with titi monkeys widely distributed and capuchins nearly extinct. Both species are absent from the Attalea funifera forests, but a few capuchins persist in the Brodiguesia santosii forests. Marmosets live throughout the landscape and are the only species inhabiting the agroforestry lands. The abundance data indicate that the disturbed forests characteristic of the landscape provide adequate habitat for all three species, but chronic hunting suppresses titi and capuchin populations and limits their distributions. Data from the Reserva Ecológica Michelin show that protected monkey populations can reach abundances equal to those at other protected sites, and that capuchins and titi monkeys enter agroforestry lands when protected. Long-term data indicate that deforestation rates are low and that illegal logging and hunting pressure are declining. The creation of reserves and the relatively large amount of forest left make the regional landscape a vital part of the strategy to conserve these species. This study demonstrates that agroforestry/forest landscapes can play an important role in primate * Kevin Michael Flesher [email protected] 1

Centro de Estudos da Biodiversidade, Reserva Ecológica Michelin, Igrapiúna, BA 45443-000, Brasil

K.M. Flesher

conservation when large blocks of contiguous forest with adequate escape space for hunted primates remain, but that the potential conservation value of agroforestry habitats and small forest fragments for hunted species will be realized only if hunting is controlled. Keywords Agroforestry . Atlantic forest . Hunting . Monkeys . Secondary forest

Introduction With ongoing human population growth and widespread poverty in most primate range countries, people continue to clear, degrade, and fragment natural habitats, and 48% of all primate species are in danger of extinction (Estrada 2013; Isabirye-Basuta and Lwanga 2008; Rylands et al. 2008). Although the number of protected areas has increased over the past decades, reserves will never encompass all, or even the majority, of primate populations (Estrada et al. 2012). Because of this, many primates will survive only if they are able to adapt to human-dominated landscapes (IsabiryeBasuta and Lwanga 2008). One of our handicaps in trying to initiate effective conservation actions is that we know little about the natural history of most species, which impedes us from predicting how alterations of the original forest ecosystem will affect them. Understanding how forest disturbance, the conversion of primary to secondary forest, fragmentation, matrix habitats, and hunting affect the capacity of primates to adapt to transformed forest landscapes is essential for devising conservation strategies (Isabirye-Basuta and Lwanga 2008). Although scientists are beginning to make progress in understanding how primates adapt to diverse human-dominated landscapes (Anderson et al. 2007; Arroyo-Rodríguez and Mandujano 2009; Estrada and CoatesEstrada 1996; Pozo- Montuy et al. 2011), we still know little about how most primates fare in most of them. The plight of the South American Atlantic forest primates is characteristic of that of monkeys in other devastated tropical biomes (Chapman et al. 2006; Corlett 2007). Centuries of widespread deforestation, degradation, fragmentation, and hunting have radically modified monkey habitats, and many species have disappeared from large parts of their former ranges (Canale et al. 2012; Santos et al. 1987). Much of the forest was converted to particularly hostile habitats for arboreal species, such as sugarcane, soy, and pasture (Dean 1995; Galindo-Leal and de Gusmão Camara 2003), isolating primates in small degraded fragments where they have little chance of long-term persistence (Canale et al. 2012). However, in some parts of the biome agroforestry systems replaced the native habitat, and although overwhelmingly planted with exotic trees, they are nonetheless trees, and therefore provide potential habitat for monkeys. Most of these agroforestry systems are pulpwood plantations with monocultures of Eucalyptus or Pinus covering hundreds to thousands of hectares (Galindo-Leal and de Gusmão Camara 2003), but there are also other agroforestry systems such as the cabruca cacao groves (native forests trees left to shade the cacao) of southern Bahia that cover an area >6000 km2 (Saatchi et al. 2001). Whereas primate use of cabruca cacao is fairly well studied (Cassano et al. 2012; Estrada et al. 2012; Mikich and Liebsch 2014), primate use of other agroforestry systems such as mixed tree crop groves, rubber monocultures, cacao/rubber plantations, and native palm fiber extraction

Distribution and Conservation of Three Atlantic Forest Monkeys

forests remains largely unexplored. As these habitats cover extensive areas in the range of several monkey species, it is important to understand their potential role for primate conservation. The forests of coastal Bahia are one of the richest centers of primate diversity in the Atlantic forest, with 11 species historically found along the 700-km coast and as many as 6 species occurring sympatrically (Mittermeier et al. 1982). However, with the exception of the Callithrix species, the Bahian monkeys have suffered drastic population declines over the past 70 yr following widespread deforestation, fragmentation, forest degradation, and hunting (Santos et al. 1987). In 2011 only 12.7% (24,6086 km2) of the forest remained (SOS Mata Atlântica 2012), and six species (Alouatta guariba, Brachyteles hypoxanthus, Leontopithecus chrysomelas, Sapajus xanthosternos, Sapajus robustus, and Callicebus coimbrai) are Endangered or Critically Endangered in the state and one (Callicebus melanochir) is Vulnerable (IUCN 2014). This situation makes Bahia a high-priority conservation area within the Atlantic forest, yet the lack of detailed studies outside of the Ilhéus/Una region makes conservation initiatives difficult. Despite decades of primate research in the state, we know little about how monkeys are faring in most of Bahia’s landscapes and why they are adapting or failing to adapt to particular landscape mosaics. One region of particular interest is the coastal strip between the Rio de Contas and the Rio Jequiriça, where forest still accounts for up to 40% of the landscape and agroforestry is one of the dominant agricultural practices (Flesher 2006). This agroforestry/forest mosaic encompasses an area of several thousand square kilometers in the heart of the ranges of three species (Sapajus xanthosternos, Callicebus melanochir, and Callithrix sp.), making it an important region for primate conservation. People have intensively logged, gathered forest products, and hunted these forests for centuries, but the high percentage of forest cover remaining and the dominance of agroforestry systems as the matrix habitats create conditions favorable for these monkeys. Given this, the region between the Rio de Contas and Rio Jequiriça should be a promising site for primate conservation in the largely devastated Atlantic forest of Bahia. If monkeys thrive there, understanding how they use the landscape will provide insights for designing landscapes that are both agriculturally productive and beneficial for the monkeys. If, however, they have difficulty surviving there, understanding why this is will help address the causes of monkey declines. I designed this 17-yr study to investigate the potential of agroforestry/forest landscapes between the Rio de Contas and Rio Jequiriça in southern Bahia to serve as habitat for the three monkey species, focusing my efforts on a 1000-km2 landscape in the municipalities of Ituberá, Igrapiúna, Nilo Peçanha, and Camamu. I sampled monkeys in the three forest types (lowland evergreen rainforest, piaçava resting, and jataipeba restinga) and four agroforestry systems (mixed tree crops/ manioc/forest, mixed tree crops, rubber monocultures, and cacao/rubber plantations) representative of the regional landscape, mapping their distribution, identifying the habitats they use, and measuring their relative abundance across four of the landscape types. I analyzed the effects of forest degradation, forest fragmentation, matrix habitats, and hunting on their distributions and abundances. I investigated trends in deforestation, logging, agricultural practices, the creation of protected areas, and hunting pressure to discuss the long-term outlook for primate conservation in the region.

K.M. Flesher

Methods Study Area The research landscape encompasses an area of 1000 km2, radiating 20–30 km out from the town of Ituberá (13°43.9′S; 39°09′′W) in a region of the southern Bahian coast (Baixo Sul) known as the Costa do Dendê (Oil Palm Coast). The mean annual precipitation is 2000 mm, with rainfall throughout the year and daily temperatures between 18° and 30°C [Reserva Ecológica Michelin (REM) unpub. data]. The topography is hilly with elevations of 40–586 m. The regional ecosystems include lowland Atlantic broadleaf evergreen rain forest, piaçava (Attalea funifera) restinga (forests growing on sandy soils) forests, jataipeba (Brodriguesia santosii) restinga forests, mangrove-lined estuaries, and diverse agroforestry systems with 200 cultivars planted, including 60 tree crops (Flesher 2006). Before the 1950s the region was largely forested with subsistence agriculturalists scattered throughout the hills, but by the middle of the 1970s farmers cleared most of the forest to establish large cacao and rubber plantations and smallholder farms (Devore 2014; Flesher 2006). The landscape today supports 42,640 ha of forest (ca. 40% of the study area), and although no pristine forests remain (Flesher 2006), the flora is rich (Rocha Santos and Talora 2012). The human population density is 64/km2, with people living throughout the landscape and no place in the forest is >2 km from a road. The rural economy is depressed and most people live on less than twice the minimum wage per month (ca. US$600) (Devore 2014; Flesher 2006). Landscape Characterization To characterize the regional landscape, I first conducted reconnaissance surveys using a 1:100,000 scale topographical map (SUDENE 1976). I hiked throughout the study area and made five over-flights, taking >1000 photographs to serve as a visual memory to help classify the landscape, and noting the agricultural habitats, forest cover and state of conservation, and house distribution. I used a 1999 Landsat image with a 30 × 30 m resolution to classify the forest cover using an ERDAS program (version 1), transferring the classified map to an ArcMap program (version 9.2) to calculate fragment sizes, interfragment distances, and total forest cover. I ground-truthed the forest map by hiking throughout the landscape (Flesher 2006). Based on this analysis, I mapped seven landscape types in the region: large forests, jataipeba (Brodiguesia santosii) restinga forests, piaçava (Attalea funifera) restinga forests, mixed tree crops/manioc/ forest, mixed tree crops, rubber monocultures, and cacao/rubber plantations (Appendix 1). Forest Characterization I used six categories to classify the forest according to the history of human use: pioneer forest, early secondary forest, late secondary forest, heavily logged forest, medium-impact logged forest, and lightly logged forest (Appendix 2). I gathered this information by interviewing farmers and men who previously worked on timber crews (Flesher 2006). In the case of the REM, I used aerial photographs (1964 and 1974) and


a SPOT image (1989) to determine the age of manioc fallows and forest clearing. I used the species lists and forest structure parameters of Rocha Santos and Talora (2012), who sampled the REM forests using the same classification system. Study Species Three monkey species inhabit the study landscape: the yellow-breasted capuchin (Sapajus xanthosternos), the Bahian masked titi monkey (Callicebus melanochir), and the black tuft-eared marmoset (Callithrix penicillata and/or hybrids with Callithrix penicillata × C. kuhlii) (Appendix 3). Hunters killed the last howlers (Alouatta guariba) in the 1950/60s, and there are no records of golden-headed lion tamarin (Leontopithecus chrysomelas) or northern muriqui (Brachyteles hypoxanthus), supporting biogeographic surveys that mark the Rio de Contas as the northern limit of their distributions (Santos et al. 1987). Census Methods I conducted the study between May 1997 and July 2013, sampling in every year except 2005, with a total of 1194 days and >5000 h in the field. I used line transects, reconnaissance hikes, semistructured interviews, key informant reports, and sighting reports to collect the data. I worked throughout the landscape between 1997 and 2004, but concentrated my efforts in the REM (forest fragments in the rubber monoculture landscape) from 2006 onward. I continued to collect data in the greater landscape after 2006 through periodic visits and key informant reports. I include several primate observations between August 2013 and April 2015 to discuss changes in ranging behavior and habitat use in the REM after the termination of the study. Transect Site Selection I established transects at 13 census sites to collect quantitative data on relative abundance and habitat use, sampling forest fragments of various sizes and the agricultural landscapes typical of the region (Fig. 1 and Table I). Owing to logistical constraints I did not have fixed transects in the piaçava or jataipeba restinga forests and relied exclusively on reconnaissance censuses, interviews, and key informant reports to collect data there. Because people regularly use the forests for hunting and wood gathering, I was unable to design a trail network free of human use. Instead I chose the least used trails available at each site (used once a week or less), opening new trails at only six of the forest sites. All trails were loops that passed through a representative sample of the site habitats. Census walks To census monkeys I walked quietly along the trails at ca. 1.2 km/h, scanning the surrounding vegetation with 7 × 35 binoculars and stopping every 50 m to listen for animal sounds (Emmons 1984). I began morning walks within the first hour of sunrise, ending no later than 11:00 h and afternoon walks between 14:00 h and dusk. I

K.M. Flesher

Fig. 1 Distribution of marmosets (Callithrix) in the municipality of Ituberá, Bahia, Brazil, 1997–2013. Closed circles = encounters; open circles = interviews. Census sites as listed in Table I.

conducted most census walks in the agricultural lands in the afternoon to minimize encounters with farm workers. I decided on sampling effort based on the census area and logistic constraints, with a minimum sample effort of 24 km and a maximum of 138.3 km (Table I). For each encounter I recorded the species, group size, time, location, strata used, and habitat. I was able to collect these data for all marmoset and capuchin encounters, but for 40.5% of the titi monkey encounters I was able to collect only location data because the groups were far from the trail. I plotted all encounters on individual species maps (Figs. 1, 2 and 3). Apart from the census walks, I spent thousands of hours in the landscape conducting other fieldwork. Each time I encountered a primate, either by sight or sound, I recorded the same information as I did for the census walks. Interview Census Design I conducted 177 interviews to plot species distributions and habitat use in areas without fixed transects. I attempted to interview at least one person in each 4-km2 grid of agricultural

Distribution and Conservation of Three Atlantic Forest Monkeys Table I Abundances of three species of primates (encounters/10 km–1), from transect walks, Ituberá, Bahia, Brazil, 1997–2013 Census site

Census area

Census Sapajus Callicebus km

100 ha in a 400-ha forest

24

Forest F1 Piauí

Callithrix

N = 13

N = 130

N = 51

0

1.25

1.67

F2 Karin/Guadalupe

500 ha in a 13,000-ha forest

43

0.23

0.23

0.47

F3 Ondulada


25

0

*

0.40

F4 Pacangê


138.26 0.83

0.76 1.81 (1.97; 1.50)a (0.49; 0.37)a

F5 Vila 5


116.1

*

5.00 1.89 (3.17; 5.74)a (2.67; 0.61)a

F6 Pancada Grande


50.25

**

5.17 0.80 (1.54; 6.49)a (1.54; 0.43)a

F7 Luis Inácio

60 ha in a140-ha forest

52.35

0.19

3.44 0.76 (1.94; 3.53)a (1.29; 0.59)a

F8 Novo Milenio


27

**

Total 10 km–1

475.96 0.27

Rubber R1 Michelin Club Loop

320 ha of a 7500-ha landscape 62

*

1.48

2.73

1.07

N=0

N=0

N=5

0

0

0.65

R2 Michelin Rubber Ridge 240 ha of a 7500-ha landscape 34.2

0

0

*

R3 Michelin West Rubber

0

0

0.25

360 ha of a 7500-ha landscape 39.5

Total 10 km–1

135.7

Cacao/rubber

—

—

0.37

N=0

N=0

N=1

C1 Fazenda Juliana

200 ha of a >3000-ha property 20

0

0

0

C2 Fazenda Ondulada

180 ha of a >3000-ha property 31

0

0

0.32

—

—

0.20

N=0

N=0

N = 16

Total 10 km–1

51

Mixed tree crops S1 Cavaloc Farm

30 ha in a smallholder mosaic

30.5

0

0

1.64

S2 Brito Lima Farm


29.5

0

0

2.03

S3 Oliveira Farm


31

0

0

1.61

Total 10 km–1

91

—

—

1.76

Total: Regional landscape

753.66 0.17

Total: Agricultural lands

277.7

*

—

1.72

0.97

—

0.79

Observed at site by author, but not during census walks

**

Observed at site by informants, but not by the author

a

Relative abundances from monitoring census: first estimate = 1997–2004 before protection; second estimate = 2011–2013, 6–8 yr after protection.

land on the SUDENE map. I chose a 4-km2 area as the minimum unit of interview density because most people were unfamiliar with areas beyond 2 km from their farms. I chose interviewees by visiting each section of the landscape and speaking with as many people as possible, revisiting areas until I had interviewed at least one person in most or all of the 4-km2 pixels. I interviewed any man who was willing to converse, determining his willingness based on his reaction to my presence. When I approached

K.M. Flesher

Fig. 2 Distribution of titi monkeys (Callicebus melanochir) in the municipality of Ituberá, Bahia, Brazil, 1997–2013. Closed circles = encounters; open circles = interviews; crosses = groups extirpated during the study period. Census sites as listed in Table I.

an individual and he showed an interest in my presence, I began the conversation by explaining my interest and asking if he would like to participate in an interview. If he was willing, I would proceed to ask questions. If he actively ignored me or said hello but showed no interest in conversation, I moved on. I did not interview women because they did not have answers to my questions. All interviews started as open-ended conversations during which I asked about the monkeys present, the habitats used by monkeys, and when the person last saw them. If I doubted a claim that a particular species was present, I asked specific details about the life history and physical characteristics of the species and accepted the information only if, through his explanation, the person convinced me of his knowledge. Owing to the illegality of hunting, I restricted questions on this subject to the 50 interviewees (28.2%) who knew me well enough to know that the interview was confidential. Starting in 2006 I collected detailed information on hunting in the REM, using hunting incident data (encounters with hunters, gunshots, dogs, traps, and hides) gathered daily by the forest guards while making their rounds. Seventeen key informants participated in the study, providing regular updates of wildlife sightings and hunting incidents. These men were acquaintances who were born


Fig. 3 Distribution of capuchins (Sapajus xanthosternos) in the municipality of Ituberá, Bahia, Brazil, 1997– 2013. Closed circles = encounters; open circles = interviews. Census sites as listed in Table I.

in the region and who I knew had an active interest in wildlife. I also collected sighting reports from people I knew or spoke with who told me about monkeys they had seen recently. Analysis I plotted all interview and sighting records directly on the regional map (Figs. 1–3) to determine which of the landscape types each species inhabited and their distributions within each landscape type. I used relative abundances, calculated as the number of encounters per 10 km walked, as the measure for analyzing the relative value of each landscape type for each species. I chose to use relative abundances instead of calculating densities because low encounter rates and probable violation of assumption that monkeys act independently of the observer precluded the calculation of species-specific densities (Peres 1999). Owing to the low number of replicates for some of the landscape types I was unable to use inferential statistical tests and used descriptive statistics instead. As primates in heavily hunted forests frequently adopt cryptic behavior, this may have affected abundance estimates (Remis and Jost Robinson 2012), and

K.M. Flesher

all relative abundance estimates presented in this study should be considered as minimums. This is especially true for the capuchins, which appear to learn to avoid trail areas and cease calling, but is also the case of titi monkeys, which are in the best of circumstances cryptic monkeys difficult to observe (Price et al. 2002), and marmosets that move quietly. I analyzed the REM data to test for habitat selection, using a chi-square test (I set the α at 0.05 for all statistical tests). To do so I classified each 50 m segment of 27,050 m of trails according to the history of human land use as described in the preceding text, assigning a habitat category for each monkey record according to the location on the trail. I kept a record of each trail walked and summed the habitat sampled along all the trails to calculate the total of each habitat type sampled during the study. I excluded pioneer forest encounters because these were 1500 (using Müller's (1995) Table II Results of interview censuses for three monkey species by landscape type, Ituberá, Bahia, Brazil, 1997–2013 Landscape type

No. of interviews No. of key informants Sapajus Callicebus Callithrix (%) (%) (%)

Large forest

30

11

30

70

73.3

Piaçava restinga forest

10

1

0

0

60

Jataipeba restinga forest

6

0

83.3

0

83.3

Mixed tree crops/manioc/forest 17

2

17.6

52.9

82.4

Mixed tree crops

62

6

0

6.5

82.3

Rubber monocultures

32

8

6.3

0

68.75

Cacao/rubber

20

6

0

5

80

Total

177

17a

10.7

20.3

76.8

Data are expressed as the percentage of interviewees who had seen the species in each landscape type. a

Some key informants provided information on more than one landscape type.

K.M. Flesher

estimation of 24-ha home ranges and an average group size of 3), with perhaps as many as 1000 monkeys in the largest subpopulation. Though I never encountered titi monkeys in the mixed tree crop landscape, interviews indicate that they persisted in four fragments, inhabiting three 40–100-ha and one 16-ha fragment, but it appears that at least two of these groups were extinguished during the study period. None of the interviewees remember titi monkeys inhabiting either the piaçava or jataipeba restinga forests. Capuchins occupy 70–100 monkeys. The largest subpopulation is that of the Pacangê, Luis Inácio, and Itapema I forests, where at least three groups, and perhaps as many as five, have contiguous home ranges. The remaining groups are mostly isolated from one another by distances of several to >10 km and the subpopulations are unlikely to have contact. None of the informants remember capuchins inhabiting the piaçava restinga forests and few animals remain in the jataipeba restinga landscape. Use of Forest Habitats Each of the species used all of the forest types found in the main forest block (Table III), but each used them differently (Table IV). Marmosets selected strongly for agricultural fallows in all stages of development and against the other forest habitats . Titi monkeys showed a significant preference for mature fallows and heavily logged forests, using the other forest types less than expected. Use of Agricultural Habitats Informants reported marmosets as present in all of the agroforestry habitats. I encountered marmosets 284 times in agricultural lands (51.5% of the records), seeing them in rubber, cacao, oil palm, and piaçava groves and in orchard trees, but 56.3% of these records were in narrow pioneer forests along the waterways (Table III). Marmosets used the mixed tree crop groves and REM rubber groves with pioneer forest in the inter-rows extensively, but the low number of records in the rubber with cleared interrows and cacao/rubber groves indicates that these are not productive habitats for marmosets. Though informants occasionally see marmosets foraging in the rubber groves, they appear to use this habitat mostly to move between riparian forests. They enter the cacao/rubber groves along the forest edge but spend little time there. There are several groups that live on the outskirts of town that move between hillside forests and people’s gardens to feed in the orchards. One group had a home range completely within town, living in the orchard and oil palm groves of a rubber factory. I did not encounter titi monkeys in the agricultural lands during the study, and know of only two cases in which they entered agricultural land. The first was of a group of


Table III Total number of records of three species of monkey by habitat type, Ituberá, Bahia, Brazil, 1997–2013

Habitat type

Forest

Callithrix

Callicebus

Sapajus

N = 552

N = 413

N = 57

28

1

1

Pioneer forest Early secondary

79

61

6

Late secondary

39

59

6

Heavily logged

54

125

11

Medium-impact logging

46

131

24

Lightly logged

6

36

5

Jataipeba restingas

7

—

3

Riparian pioneer forest

160

—

—

Rubber monocultures

41

—

—

Mixed tree crops

37

—

—

Gardens

19

—

—

Piaçava restingas

18

—

—

Beach/coconut

4

—

—

Cacao/rubber

2

—

—

Agricultural

protected titi monkeys that regularly entered a mixed tree crop smallholder farm adjacent to a large forest, occasionally sleeping in remnant forest trees and feeding on bananas. The other case was of a group that an informant saw in a banana tree along the forest edge on a cacao/rubber plantation. Table IV Observed and expected forest habitat selection for three species of monkey, Ituberá, Bahia, Brazil, 1997–2013, with results of chi-square tests demonstrating whether or not each species selected forest habitats according to their availability Callithrix N = 161

Callicebus N = 390

Sapajus N = 42

Forest habitat type

Expected Observed Expected Observed Expected Observed

Early secondary

26

49

62

58

12

5

Late secondary

20

34

49

59

6

6

Heavily logged

40

36

96

119

7

9

Medium-impact logged

60

36

146

122

—

—

Lightly logged

15

6

37

35

—

—

—

—

—

17

22

Medium-impact logged + lightly loggeda — df

4

4

3

χ2

46.32

11.28

6.00

P