Conservation Biology of the Genus - Springer Link

International Journal of Primatology, Vol. 19, No. 3, 1998

Conservation Biology of the Genus Alouatta Carolyn M. Crockett1,2 Received November 11, 1996; accepted May 23, 1997

As assessed by the IUCN Mace–Lande system, seven (35%) of the 20 Alouatta species and subspecies with adequate data are classified as "threatened," i.e., critically endangered, endangered, or vulnerable (Rylands et al., 1995). This percentage is much lower than the 75 to 100% threatened taxa for the other large-bodied genera: Ateles, Lagothrix, and Brachyteles. Only 5 of the 16 Neotropical genera have lower percentages of threatened taxa than that of Alouatta: Cebuella, Pithecia, Saguinus, Saimiri, and Cebus. The threatened howler taxa occupy small distributions in areas of forest fragmentation. In general, populations are most affected by major habitat disturbance, such as total deforestation and flooding from dam construction, and by human hunters. Facilitated by their ability to exploit folivorous diets in small home ranges, howlers can tolerate considerable habitat fragmentation but not the increased exposure to hunting that may accompany it. Howlers seem particularly vulnerable to yellow fever and bot fly parasitism. Although the former threat may decrease by increasing fragmentation of the habitat, other sorts of parasitism may increase in disturbed habitats. The low genetic variability of the Central American howlers suggests a resistance to inbreeding depression potentially experienced during population bottlenecks. Greater between-population variability may still exist. Although howlers are not readily bred in captivity, they respond well to translocation. Translocation has been successfully achieved for >4 howler species and is a viable option for introducing new genetic variability into population fragments and repopulating areas from which howlers are extinct. Their pattern of bisexual dispersal

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Regional Primate Research Center, University of Washington, Seattle, Washington 98195, and National Zoological Park, Smithsonian Institution, Washington, DC 20008. To whom correspondence should be addressed at Regional Primate Research Center, Box 357330, University of Washington, Seattle, Washington 98195-7330. e-mail: [email protected].

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549 0164-0291/98/0600-0549$ 15.00/0 C 1998 Plenum Publishing Corporation

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facilitates colonization of regenerating habitats, and in suitable, protected habitats they have shown the capacity for strong population recovery. KEY WORDS: Alouatta; howler monkey; population assessment; habitat fragmentation.

INTRODUCTION

As a scientific discipline, conservation biology has expanded rapidly over the past decade. So too has information on the distribution and status of the howlers (Alouatta). This is due partially to the creation of Neotropical Primates, the multilingual newsletter of the Neotropical Section of the IUCN/SSC Primate Specialist Group. I summarize the conservation status of howlers, as presented in the recent special supplement issue of Neotropical Primates, which categorizes all Neotropical primate species according to the IUCN Mace-Lande system (Rylands et al, 1995). The summary also serves to introduce the taxa and geographical distribution of the recognized howler species. Secondly, I review the major factors contributing to conservation status, examining data from howlers with respect to these factors and identifying which ones may have led to the threatened categories identified by the Mace-Lande system. Thirdly, I describe conservation strategies that are most effective in improving the conservation outlook for these species.

HOWLER SPECIES, STATUS, AND GEOGRAPHIC DISTRIBUTION

The Mace-Lande system for categorizing threatened species and subspecies on the basis of specific criteria pertaining to population size and composition, population changes, fragmentation, and extent of occurrence was adopted by the World Conservation Union (IUCN) in 1994, after review and modification (IUCN Species Survival Commission, 1994; Mace and Lande, 1991; Rylands et al, 1995). This system includes 3 classifications, which together comprise the assessment threatened: critically endangered, endangered, and vulnerable. Taxa classified as lower risk may be subdivided into conservation dependent, near-threatened, and least concern. A distinction is made between taxa classified as extinct vs. extinct in the wild. When appropriate information on abundance or distribution is inadequate to make an assessment, the taxon is listed as data deficient, which makes no judgment regarding threatened vs. lower risk status. A final category, not evaluated, is applied when a taxon has not yet been assessed

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against the criteria. No modern neotropical taxon is classified as extinct or extinct in the wild. The Mace-Lande classification system relies upon a complete listing of taxa. Table I lists the species and subspecies of Alouatta, the countries in which they are reported to occur, and their conservation status rating (Rylands et al, 1995). It should be noted that the taxonomy of Alouatta is still in some dispute. Hill classified howlers as representing at least 5 welldefined species—(A. palliata, A. seniculus, A. belzebul, A. fusca=guariba, and A. caraya)—and a questionable sixth species: A. villosa (Hill, 1962). Subsequently, Alouatta villosa and a subspecies of A. palliata were confirmed as the sixth species: A. pigra (Horwich and Johnson, 1986; James and Horwich, 1993; Smith, 1970). Ten years ago yet another taxon formerly classified as a subspecies of Alouatta palliata was elevated to specific status on the basis of dermatoglyphic evidence: A. coibensis (Froehlich and Froehlich, 1987). Two taxa generally considered to be subspecies of Alouatta seniculus have been elevated to species level—A. sara and A. arctoides—on the basis of genetic evidence; the subspecies A. belzebul nigerrima may also warrant specific status [Rylands et al. (1995), provide details]. Chromosomal studies indicate that Alouatta belzebul nigerrima is more closely related to A. seniculus than to other A. belzebul spp. (Correa de Oliveira, 1996). Bonvicino et al. (1995) considered 2 subspecies of Alouatta seniculus, to warrant specific status—A. macconelli and A. stramineus though questions remain (Rylands, 1998). I continue to classify them as subspecies. Most people, however, would agree that there are 6 distinct species groups: mantled howlers (Alouatta palliata), Central American black howlers (A. pigra), red howlers (A. seniculus), South American black howlers (A. caraya), brown howlers (A. fused), and red-handed howlers (A. belzebul) (Emmons and Feer, 1990). Figure 1 depicts the approximate distributions of these species groups. Genetic studies suggest a close relationship between Alouatta fusca and A. belzebul, except A. b. nigerrima (Sampaio et al., 1996); and Correa de Oliveira (1996) placed them as a single group. Apart from variation in color and howling vocalizations, the various howler taxa are superficially similar (Rowe, 1996). The distinction of taxa as species versus subspecies does not affect my analysis. Of the 23 howler taxa recognized in the listing, 3 are critically endangered, one is endangered, 3 are vulnerable, 13 are lower risk, and 3 are data deficient (Rylands et al, 1995). Thus, of the taxa for which data are sufficient for evaluation, 35% are threatened (Table II). The three taxa considered as data deficient are of questionable validity, having been identified only in old museum collections and do not contribute to the percentagethreatened calculation. To put the howler status in perspective, in Table II I present the number of taxa and percentage classified as threatened for all

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Table I. Howler Species and Subspecies (After Rylands et al, 1995) and Corresponding Species Listed by Crockett and Eisenberg (1987) Current species/ subspecies

Species (C & E)

Statusa

Approximate distribution (primarily after Hill, 1962; also see text)

Alouatta palliata palliata

A. palliata

LR

A. p. mexicana A. p. aequatorialis

A. palliata A. palliata

VU LR

Alouatta coibensis coibensis A. c. trabeata Alouatta pigra

A. palliata

EN

A. palliata A. pigra

Panama (Azuero Peninsula) Mexico (S. Yucatan), Belize, Guatemala E. Colombia, W. Venezuela, E. LR Ecuador, E. Peru, N.W. Bolivia Trinidad VU N.W. Brazil (north of Amazon); LR possibly extending to Venezuela (S. of Orinoco) Brazil (north of mouth of AmaLR zon); possibly extending to Guianas and N.E. Venezuela DD* Brazil (Codajaz, north of Rio Solimoes, Amazonas) DD* W. Brazil, along Rio Jurua, Amazonas DD* W. Brazil, along Rio Purus, Amazonas Venezuela, north of Orinoco (see LR Bodini and Perez-Hernandez, 1987) Venezuela, north of Rio Orinoco LR LR Bolivia, N.W. of Rio Beni LR Brazil, S. of Amazon, near mouth, and isolated populations in easternmost Brazil Brazil, S. of Amazon; S.E. of Rio LR Madeira Brazil, S. of Amazon; between A. LR b. nigerrima and A. b. belzebul CR Northeast coast of Brazil, state of Maranhao CR E. Brazil, S. of Rio San Francisco VU S.E. Brazil; N.E. Argentina LR N. Argentina, S.E. Brazil, Paraguay, Bolivia; possibly Uruguay

Alouatta seniculus seniculus A. s. insulanus A. s. stramineus

A. seniculus

A. s. macconelli

A. seniculus

A. s. amazonica

A. seniculus

A. s. juara

A. seniculus

A. s. puruensis

A. seniculus

A. s. ssp.

A. seniculus

Alouatta arctoidea Alouatta sara Alouatta belzebul belzebul

A. seniculus A. seniculus A. belzebul

A. b. nigerrima

A. belzebul

A. b. discolor

A. belzebul

A. b. ululata

A. belzebul

Alouatta fusca fusca A. f. clamitans Alouatta caraya

A. fusca A. fusca A. caraya

a

A. seniculus A. seniculus

Honduras, Nicaragua, Costa Rica, Panama (but now extinct from El Salvador) S. Mexico, Guatemala S. Panama, W. Colombia, W. Ecuador, N.W. Peru Panama (Coiba Island)

CR LR

LR, lower risk; VU, vulnerable; EN, endangered; CR, critically endangered. DD*, data deficient. Not used to calculate percentages in Table II. These taxa known from old collections; may not be distinct from typical Alouatta s. seniculus (Hill, 1962; Rylands et al., 1995; Bonvicino et al, 1995).

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Fig. 1. Approximate limits of distribution of 6 species groups of Alouatta (A. b. nigerrima may belong to the A. seniculus group; see text). Actual distributions are considerably smaller because unsuitable, fragmented, and degraded habitat areas are not distinguished. General locations of subspecies and recently elevated species are indicated; no demarkation of possible boundaries of their distributions is attempted.

16 Neotropical primate genera (Rylands et al., 1995). In contrast to the other large-bodied genera—Ateles, Lagothrix, and Brachyteles—a far lower percentage of howler taxa are threatened. Only five Neotropical genera have fewer threatened taxa than Alouatta: Cebuella, Pithecia, Saguinus, Saimiri, and Cebus. Three other genera have slightly more percentages of taxa threatened. In this review, I identify subspecies or species as reported by the individual investigators. Many authors do not identify the subspecies studied. Unless specified, references to Alouatta seniculus include A. sara and A. arctoides.

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Table II. Neotropical Genera and Number of Countries Occupied, Number of Genera, and Percentage Threatened (After Data of Rylands et al., 1995)a

No. % threatened threatened

No. countries

Genus

No. taxa

No. DD

Cebuella Callithrix Saguinus

1 17 32

0 1 2

0 6 5

38 17

5 3 10

4 1

0 0

4 1

100 100

1 4

Aotus

12

1

4

36

10

Callicebus

26

1

9

36

7

Saimiri

12

0

3

25

11

Cebus

33

10

6

26

17

Pithecia

8

0

1

13

9

Chiropotes Cacajao

4 6

0 0

2 4

50 67

5 4

23

3

7

35

19

Leontopithecus Callimico

Alouatta

Ateles

Lagothrix Brachyteles a

0

17

1

12

75

17

5 2

0 0

4 2

80 100

5 1

Countries

BO, BO, BO, FG, BR BO,

BR, CO, E, PAR BR, PE BR, CO, CR, E, GY, PAN, PE, S BR, CO, PE

A, BO, BR, CO, CR, E, PAN, PAR, PE, V BO, BR, CO, E, PAR, PE, V BO, BR, CO, CR, E, FG, GY, PAN, PE, S, V A, BO, BR, BZ, CO, CR, E, FG, GY, H, N, PAN, PAR, PE, S, T, V BO, BR, CO, E, FG, G, PE, S, V BR, FG, GY, S, V BR, CO, PE, V A, BO, BR, BZ, CO,

CR, E, FG, GU, GY, H, M, N, PAN, PAR, PE, S, T, V; U? excluded; apparently extinct in ES BO, BR, BZ, CO, CR, E, ES, FG, GU, GY, H, M, N, PAN, PE, S, V BR, CO, E, PE, V BR

A, Argentina; BO, Bolivia; BR, Brazil; BZ, Belize; CO, Colombia; CR, Costa Rica; E, Ecuador; ES, El Salvador; FG, French Guiana; GU, Guatemala; GY, Guyana; H, Honduras; M, Mexico; N, Nicaragua; PAN, Panama; PAR, Paraguay; PE, Peru; S, Suriname; T, Trinidad; U, Uruguay; V, Venezuela. DD, data deficient.

FACTORS CONTRIBUTING TO CONSERVATION STATUS Size of the Geographical Distribution

As the geographical range of a species or subspecies increases, the taxon's chances of total extinction decreases. For example, the threatened


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Alouatta seniculus insulanus is confined to Trinidad, whereas the lower-risk monotypic A. caraya has a large distribution. Furthermore, the number of different countries occupied is likely to be positively correlated with specific survival, since the probability of one or more having an active environmental policy or lower human population density increases. Howlers are distributed widely, from about 21°N to 30°S (Crockett and Eisenberg, 1987; Emmons and Feer, 1990; Hill, 1962; Wolfheim, 1983). Alouatta is present in 19 countries, more than any other Neotropical genus (Table II). They live on Trinidad and in all the continental nations of Latin America except Chile and Uruguay, where their presence has still to be confirmed (Villalba et al, 1995). In El Salvador, they are either extremely endangered (Daugherty, 1972) or extinct (Rodriguez-Luna et al., 1996b; Rylands et al., 1995). Given this broad distribution, we might expect howlers to be less threatened than members of some other Neotropical genera. On the basis of the percentage of taxa threatened, Alouatta is the sixth least threatened of 16 genera (Table II). Across genera, there is a significant negative correlation between number of countries occupied and percentage of taxa threatened (rs = -.58, df = 14, p < .05). The 6 howler species groups occupy essentially allopatric distributions. Small areas of sympatry between Alouatta pigra and A. palliata may still exist (Curdts, 1993; Horwich and Johnson, 1986). Hernandez-Camacho and Cooper (1976) reported a small zone of sympatry for Alouatta palliata and A. seniculus in northwestern Colombia. Both species apparently live in the same national park (Defler, 1994; Hernandez-Camacho and Defler, 1985). A third possible area of howler specific sympatry, between Alouatta caraya and A. fusca in Iguazu National Park, Misiones, Argentina (Crespo, 1954), has not been verified; the distribution of A. fusca comes near to but may not overlap that of A. caraya in Misiones (di Bitetti et al, 1994). Approximate broad distributions of howler species were mapped by Wolfheim (1983), Emmons and Feer (1990), Kinzey (1997), and Rowe (1996) and are summarized in Fig. 1. The ranges of subspecies, some of which are now considered full species, are presented in Hill (1962). Distributions are often assessed largely from collection locations of museum specimens (Bodini and Perez-Hernandez, 1987; Hirsch et al., 1991). Although important for understanding biogeography, they may have little bearing on actual present distribution and conservation status. Of the approximate distributions of howler species, Alouatta seniculus has by far the largest distribution even if A. sara and A. arctoides are considered distinct species, encompassing parts of 10 countries, from Venezuela and the Guianas to Bolivia (Table I). The next largest distribution is that of Alouatta caraya, which occupy four countries, primarily Brazil and Paraguay, but extending into Bolivia (Garcia Yuste, 1986) and northern

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Argentina (Brown, 1984) and perhaps Uruguay (Villalba et al, 1995). Alouatta belzebul has a moderate distribution, entirely in Brazil, south of the Amazon River (Coimbra-Filho et al., 1995; Langguth et al., 1987). The distribution of Alouatta fusca was formerly relatively large but is reduced to a few remnant populations, due to extensive habitat destruction and high human population density in southeastern Brazil (Chiarello and Galetti, 1994; Mittermeier et al., 1982; Santos et al., 1987). Its distribution in northeastern Argentina is small and of unknown status (Brown, 1984; di Bitetti et al., 1994). Alouatta palliata is distributed in 10 countries, but most of them are small. Its distribution in Colombia and Ecuador is a narrow coastal strip, extending into a tiny portion of Peru (Aquino and Encarnacion, 1994; Hernandez-Camacho and Cooper, 1976). Its range in Mexico and Guatemala is fragmented and endangered (Estrada and Coates-Estrada, 1988). Alouatta pigra has a small distribution in Belize, Guatemala, and the Yucatan, Mexico (Horwich and Johnson, 1986). Alouatta coibensis has a tiny distribution in Panama (Froehlich and Froehlich, 1987). The distribution sizes of Alouatta sara and A. arctoides are similar to that of A. pigra (Hill, 1962). If Alouatta b. nigerrima is elevated to specific status, its distribution is larger than those of A. sara and A. arctoides (Hill, 1962). The actual area of howler specific distribution is much less than the broad range illustrated in Fig. 1 since preferred microhabitats may be patchily distributed and many areas have experienced extensive habitat destruction and human hunting. For example, Alouatta fusca fusca, the northern subspecies, had not actually been seen in the state of Bahia by scientists in over 40 years, and more recent reports are few (Santos et al, 1987). Alouatta b. belzebul has a distribution that is very fragmented in northeastern Brazil, where scientists verified the existence of small, highly endangered populations in five previously unknown areas (Langguth et al., 1987). Alouatta pigra appears to be locally common, and even increasing, in many forested areas of Belize but not in others. They also seem to be secure in Tikal, Guatemala, but uncommon elsewhere. They are threatened with extinction in Mexico (Dahl, 1987; Estrada and Coates-Estrada, 1988; Horwich, 1989; Hubrecht, 1986; Watts et al, 1986). The distribution of Alouatta seniculus in Venezuela, based on collection locations, is broad (Bodini and Perez-Hernandez, 1987). The species is still widely distributed in Venezuela, despite some areas of habitat destruction (Robinson and Ramirez C, 1982; Rudran and Eisenberg, 1982). Alouatta are sometimes absent from areas where suitable habitat occurs: human hunting and disease are possible reasons (Brooks, 1996; de Oliveira and Oliveira, 1993; Encarnacion et al, 1993; Ferrari et al, 1996; Hubrecht, 1986).


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Habitat Types Occupied Within the geographical range, the greater number of habitat types occupied increases the probability of specific survival. Furthermore, the more tolerant a species is of degraded, disturbed habitats, and proximity to humans, the better the conservation status is likely to be, in the absence of severe hunting pressures that correlate with these factors. Range of Habitat Types As a genus, howlers occupy the widest range of habitats of any Neotropical species (Crockett and Eisenberg, 1987). Howlers are found from sea level to >3200 m and occupy diverse habitat types, from closed-canopy wet evergreen forests, including terra firma and inundated swamp forests, to open, highly seasonal deciduous and semideciduous woodlands and gallery forests (Crockett and Eisenberg, 1987; Hernandez-Camacho and Defler, 1985; Wolfheim, 1983). Since howlers do not need to drink water, they are not restricted to its proximity. There is interspecific variation in howler habitats, due partly to availability within the specific distributions. Alouatta seniculus and A. palliata occur in the widest range of habitats. Rudran and Eisenberg (1982) reported that Alouatta seniculus occurs in >5 and perhaps all 7 biogeographical zones that they identified for Venezuela. HernandezCamacho and Defler (1985) divided Colombia into 7 humidity provinces. Alouatta seniculus occurs in as many as any of the Colombian primate species, 5 (tied with Cebus capucinus), and A. palliata occurs in 4. Alouatta seniculus live up to 3200 m (Hernandez-Camacho and Cooper, 1976). In the Amazon region of Colombia, Alouatta seniculus prefer habitats along rivers and are at low densities elsewhere in the region (Defler, 1994). Alouatta palliata is absent from mangrove forest in Colombia (HernandezCamacho and Cooper, 1976) but occupies such habitats in northwestern Peru (R. Valega R., personal communication, 1987), northwestern Costa Rica (K. Stoner, personal communication, 1997), and Panama (Baldwin and Baldwin, 1976), as does A. coibensis in Panama (Milton and Mittermeier, 1977). Alouatta seniculus occurs in mangrove habitats in Colombia (Hernandez-Camacho and Defler, 1985), as does A. belzebul ululata in Brazil (Fernandes and Aguiar, 1993). The highest densities for Alouatta seniculus are in semideciduous woodland and gallery forest habitats in the llanos or plains of Venezuela, where I studied them (Crockett, 1985, 1996; Crockett and Eisenberg, 1987). Alouatta palliata also occur at high densities in similar tropical dry forest habitats in Costa Rica (Clarke and Zucker, 1994; Clarke

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et al., 1986) and the moister semievergreen forests of Barro Colorado Island (Milton, 1982). Alouatta pigra was originally considered to be a habitat specialist, confined to undisturbed tropical rain forest (Smith, 1970). More recent researchers found the species in various types of evergreen and semievergreen forests, including disturbed and riverine forests. Horwich and Johnson (1986) reported that all habitats containing Alouatta pigra are 2000 m in Guatemala. Alouatta belzebul is basically an Amazonian forest species, though remnant populations live in the eastern corner of Brazil, in the northernmost extent of the Atlantic forest region where it was widespread in the past (Coimbra-Filho et al., 1995; Hirsch et al., 1991; Langguth et al, 1987). They seem to be absent from the dry Caatinga (thorn scrub) region of northeastern Brazil, which has a low annual rainfall of 300-1000 mm (Eiten, 1974). This vegetation type has expanded due to the destruction of the Atlantic forest—evergreen and semideciduous—and gallery forest in northeast Brazil since the 1500s (Coimbra-Filho and Camara, 1996). Alouatta caraya is also a lowland form, but they primarily inhabit seasonally dry semideciduous and deciduous forests, including the seasonally flooded Pantanal. For example, at a Brazilian ranch on the edge of the Pantanal, Schaller (1983) observed Alouatta caraya in deciduous forest, gallery forest, and inundated flood plain but not in cerrado habitat—savanna with narrow-crowned small trees. In Paraguay, Alouatta caraya live in the eastern semideciduous and semievergreen forests and, in the west, in gallery forests of the chaco, in areas usually with >900 mm annual rainfall (Stallings, 1985). In Argentina, Alouatta caraya also live in the chaco but not in the semievergreen forests of Misiones. The distribution of Alouatta fusca is predominantly in hilly uplands. Its habitat types are primarily remnant Atlantic Forest patches and the Araucaria Brazilian pine forests. In the areas where the distributions of Alouatta caraya and A. fusca approach sympatry—Misiones, Argentina, and southernmost Brazil—habitat preference may separate the species: A. fusca seems more bound to moister, continuous Araucaria forest, whereas A. caraya is more likely to survive in secondary and disturbed habitats (di Bitetti et al., 1994). Although various authors have suggested that howler densities may vary directly as a function of habitat type, Chapman and Balcomb (1998) report that little variation is clearly explained by habitat differences. They suggest that much of the variation in population characteristics is related


559

to recent events such as food crop failure, disease, habitat alteration, and hunting pressure. Existence in Forest Fragments and Disturbed Habitats

In the absence of severe hunting pressure, howler species can exist in forest fragments, disturbed habitats, and close proximity to human populations. Alouatta caraya, A. seniculus, A. palliata, A. pigra, and A. belzebul all inhabit forest patches on cattle ranches (Bonvicino, 1989; Clarke and Zucker, 1994; Clarke et al, 1986; Crockett, 1985, 1996; Schaller, 1983; Watts et al., 1986). Alouatta caraya, A. seniculus, A. pigra, and A. fusca also can live in forest fragments in agricultural areas (Chiarello, 1994; Estrada and Coates-Estrada, 1988; Galetti et al., 1987; Johns, 1985; Rumiz, 1990; Zunino and Rumiz, 1986). However, the survival of howlers in forest fragments may be compromised. Alouatta pigra occupies all successional stages of riverine forest including second growth in an agricultural area of Belize (Horwich and Lyon, 1987a), and low seasonally inundated riverine forest patches on cattle ranches in Mexico (Watts et al., 1986). In the Cantareira Reserve, at the edge of Sao Paulo city, Alouatta fusca lives at high densities (da Silva, 1981). One troop regularly ranged into trees in an adjacent middle-class neighborhood (C. T. Carvahlo, personal communication, personal observations, 1988). At Hato Masaguaral, Venezuela, the home range of one troop of A. seniculus included the trees in a building compound, which they visited when certain species, such as mangos, were fruiting (personal observation). Lovejoy et al. (1986) found that Alouatta seniculus was the only primate species to persist in all 5 isolated reserves created in a forest-cutting experiment—the Biological Dynamics of Forest Fragments project: 1 was 100 ha and 4 were only 10 ha each. A second howler group formed in one of the 10-ha plots, apparently through the immigration of an outside male. Further studies suggested that howlers in the smallest fragments experienced dietary stress (Neves and Rylands, 1991), indicating that although howlers may be able to survive in fragmented areas, the populations are not healthy. DeLuycker (1995) compared population characteristics of a population of Alouatta caraya in forest fragments in northern Argentina with similar data collected there a decade before (Rumiz, 1990). The overall density— individuals and groups per km 2 —had not changed much. However, the ratio of immatures to adults had declined substantially, suggesting lower rates of successful reproduction or reduced opportunities for dispersal of

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maturing individuals or both. Selective logging and clear-cutting had altered the specific composition of the patches. Rodriguez-Luna et al. (1987) found that only 21% of fragmented natural forest area in the Mexican region still had primates. In 14 patches in which they saw primates, 7 contained Alouatta palliata (patch size range = 4 to 20 ha) and 10 had Ateles geoffroyi (range = 2 to 20 ha); overall, the spider monkeys outnumbered the howlers 67 to 40. However, in a nearby area in Mexico, Estrada and Coates-Estrada (1988) noted that Alouatta palliata considerably outnumbered Ateles geoffroyi in forest fragments. They also found that mean troop size and density were larger in protected fragments compared with unprotected fragments. Howler ecological density in protected fragments was 23 individuals per km2, compared to 3.6 individuals/km2 in unprotected fragments. In a follow-up study Estrada and Coates-Estrada (1994) censused 120 forest fragments in Los Tuxtlas, Mexico, ranging from 1 to 2000 ha, isolated for 1-20 years, and located at a 0.2- to 8-km straight-line distance to the nearest forest. They saw howlers in only 40% of the fragments. The number of howlers was positively correlated with the size of the fragment and negatively correlated with the number of years since the forest fragment was isolated and the distance to the nearest forest. The undisturbed patches had higher densities of howlers than disturbed ones. Spider monkeys were in only 10% of the Los Tuxtlas forest fragments. In another area, where hunting was common, Alouatta pigra was rarely found in the remaining forest (Watts et al., 1986). Hunting can exterminate howlers in forest patches (Chiarello and Galetti, 1994). This may partially account for Alouatta fusca being absent in 7 of 8 fragments censused by Pereira et al. (1995). Parasitic infestation is greater in smaller fragments (Gilbert, 1994) or within troops that have restricted ranges (Stoner, 1996). Unless howlers can effectively disperse from one forest fragment to another, survival in them is transitory, as suggested by the findings of Estrada and Coates-Estrada (1994). The existence of howlers in small forest patches should not give us undue optimism. Gilpin and Soule (1986, p. 27) note that "such [isolated] groups are not likely to persist for more than a few generations, according to population biology theory." Robinson and Ramirez (1982) estimated the minimum area required to support an effective primate population size of 500 individuals, which is recommended to maintain sufficient genetic variability and heterozygosity in the long term. The minimum size for Cebus nigrivittatus (olivaceus) is 550 km2 and for Callicebus moloch it is 105 km2. These calculations are based on the assumption that the species occur at relatively high densities under optimal ecological conditions.


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In howlers, dispersal rates are likely to be mediated by population density and intrasexual competition such that changes in population structure caused by habitat degradation can increase inbreeding (Pope, 1995). Central American Alouatta spp. have a very low genetic diversity, apparently related to repeated population bottlenecks from yellow fever epidemics and hurricanes, compared with the high allozymic diversity of South American A. seniculus and A. belzebul, which have large distributions (Pope, 1995). Fragmentation of Central American forests may actually offer protection from disease transmission. Although heterozygosity within fragments may be very low, it may be preserved to some extent between them (Pope, 1995). If so, management programs could increase genetic diversity within forest fragments through reintroductions or translocations. Typical Home Range Size

Smaller home ranges will increase the chances of a species surviving in forest fragments. The persistence of howlers in forest fragments is facilitated by the fact that their home ranges are typically 1 in Bolivia (Garcia and Braza, 1987), and 3 in Trinidad (Neville, 1976). However, they have declined seriously in the Trinidadian reserves (Agoramoorthy and Hsu, 1995). Alouatta fusca clamitans live in >6 reserves, but are already extinct in perhaps 3 others (Mittermeier et al, 1982). In the 1980s, Alouatta belzebul lived in 6 protected areas in Argentina and 1 in Brazil (Brown, 1984; Prates et al, 1993).

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CONSERVATION STRATEGIES FOR HOWLERS

Among the conservation strategies especially relevant to howlers, 3 are particularly noteworthy: 1. Increasing the number, size, and monitoring of protected areas, especially to safeguard threatened populations. Estrada and Coates-Estrada (1988) and Chapman and Balcomb (1998) report that protection is associated with higher population densities. Monitoring new and existing reserves is of utmost importance. There is considerable evidence that hunting has exterminated howlers from many areas, including reserves. 2. Expanding local education programs to encourage attitudes and land management schemes that will allow coexistence of people and monkeys. Successful sanctuaries involve the support of local people (Steinberg, 1993). In areas where absolute protection of forests is not feasible, programs that would protect at least some of the monkeys could include planned deforestation and other multiple-use approaches such as pioneered for Alouatta pigra in Belize by Horwich and colleagues (Horwich and Lyon, 1987a, b; Lyon and Horwich, 1996). In areas where selective timber extraction occurs, management schemes should protect tree species that provide important primate foods during seasonal shortages (Terborgh, 1986). Tourism may provide alternative income to other uses of the forest and its wildlife, but unless properly managed, it may have few local monetary benefits and may have negative effects on some wildlife species (Groom et al, 1991; Kinnaird and O'Brien, 1996). Multiple-use schemes which allow continued hunting by indigenous peoples are controversial given the evidence that such hunting can occur at non-sustainable levels, eventually resulting in prey extinctions (Redford and Robinson, 1985). 3. Translocating and reintroducing howlers. The first documented reintroduction—a group of captive-born Alouatta caraya to Brasilia National Park—was unsuccessful, though wild A. caraya were successfully translocated to the same park (Lindbergh, 1987). A group of Alouatta caraya held captive at the Centro Argentino de Primates (Colillas and Coppo, 1978) was eventually released into an area across a river from its original range (G. E. Zunino, personal communication). Troops of Alouatta palliata have been successfully translocated (Estrada and Coates-Estrada, 1988; Rodriguez-Luna and Cortes-Ortiz, 1994; Rodriguez-Luna et al., 1993), but some translocations have been less successful (de Vries, 1991). Individual Alouatta seniculus were translocated from several areas flooded by dam construction in Venezuela and Surinam; they were not monitored and their success is unknown (Konstant and Mittermeier, 1982; T. Blohm, personal communication). A recent translocation of >100


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Alouatta seniculus after dam flooding in French Guiana was monitored, including the use of radio telemetry (Vie and Richard-Hansen, 1997). Success rate, though not yet fully presented, is promising. The most successful and carefully monitored translocation to date is the reintroduction of Alouatta pigra into Cockscomb Basin, Belize, an area where they had become extinct due to yellow fever, hurricane devastation, and overhunting; >86% survived the first 10 mo (Horwich et al, 1993; Koontz et al., 1994). Translocation of healthy howlers doomed by dam construction and other habitat destruction into forests from which they have been exterminated seems to be a viable conservation strategy. Translocations also may be used to introduce genetic diversity into population fragments. For successful translocation the new area should (a) contain food and other habitat characteristics similar to the source population's home range, (b) be close to the capture area to reduce transportation time, (c) be devoid of the species, or have a resident population too small for long-term viability, (d) have experienced prior human disturbance, such as hunting (intact, pristine habitats should be avoided), and (e) be protected from hunting, logging, and excessive tourism at the time of release; and (f) the subjects should be given a health exam under sedation, and unhealthy individuals should not be released, (g) entire social groups should be released if possible, (h) subjects should be maintained in a holding enclosure at the site for about 2 days before release to promote group cohesion, and (i) different groups should be released some distance apart (Horwich et al., 1993; Koontz et al., 1994; Vie and Richard-Hansen, 1997). Captive propagation of howlers has been rarely successful and is unlikely to be an effective conservation strategy. In general, zoo propagation of threatened and endangered primates is less successful than for less vulnerable species (Lindburg et al, 1986). In 1987, there were 81 howlers in US zoos, 60% of them being Alouatta caraya (ISIS Species Distribution Report, July 1987; A. Shoemaker, personal communication). Of all howlers in captivity, Alouatta caraya have reproduced most successfully (ThomasBaker, 1987). Alouatta palliata and A. pigra have been bred in a Mexican zoo (Estrada and Coates-Estrada, 1988). The first captive reproduction of Alouatta belzebul occurred at the Brazilian Primate Center, Belem, where individuals threatened by dam flooding had been moved (Kingston, 1987). As a last resort, highly endangered populations of rare species or subspecies might be moved to captivity, at least until a suitable reintroduction site is found, e.g., Alouatta fusca fusca (Santos et al., 1987).

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CONCLUSION

Howlers are still a major part of the mammalian biomass in the Neotropics, though in comparison to today their former numbers must have been enormous. By virtue of widespread howler distribution geographically and ecologically, some species will persist after many other Neotropical primates have become extinct. However, as assessed by the IUCN Mace-Lande system, 7 (35%) of the 20 species and subspecies with adequate data are classified as threatened. Howler populations are most affected by major habitat disturbance, such as total deforestation and flooding from dam construction, and by hunting. However, facilitated by their ability to exploit folivorous diets in small home ranges, howlers can tolerate considerable habitat fragmentation, although not the increased exposure to hunting that may accompany it. Howlers seem particularly vulnerable to yellow fever and bot fly parasitism. The former threat may decrease by increasing fragmentation of the habitat. Some sorts of parasitism may increase in disturbed habitats. The low genetic variability of Central American howlers suggests a resistance to inbreeding depression potentially experienced during population bottlenecks. Greater interpopulation variability may still exist. Although howlers are not readily bred in captivity, they respond well to translocation. Translocation has been successful for >4 howler species and is a viable option to introduce new genetic variability into population fragments and to repopulate areas from which howlers are extinct. The pattern of bisexual dispersal facilitates colonization of regenerating habitats. Howlers in suitable, protected habitats have the capacity for strong population recovery. On balance, the assessment for Alouatta is guarded optimism. The conservation strategies suggested for many other Neotropical primate and nonprimate taxa will usually benefit howlers. Reductions in deforestation and in hunting of wild fauna, increasing reforestation and reliance on tropical forest crops rather than ranching or farming, alternative uses of forests such as managed tourism, and promoting widespread family planning among nearby human settlements are measures that will help sustain howler populations indefinitely. ACKNOWLEDGMENTS

I revised this paper from a presentation originally prepared for the symposium Howling Monkeys: Past and Future, organized by Ken Glander for the 1988 Congress of the International Primatological Society. I am


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very grateful to Margie Clarke for bringing this collection of articles to publication. Valuable bibliographic information was obtained from the Primate Information Center. I appreciate the many articles relevant to primate conservation provided by Russ Mittermeier. My thanks go to A. Rylands, K. Stoner, and anonymous reviewers for constructive comments. Preparation of the manuscript was supported in part by the Washington Regional Primate Research Center (NIH Grant RR00166). My husband Bob Brooks has contributed moral and financial support to my perpetual interest in howlers for many years. My field research on red howlers was funded by the Smithsonian Institution International Sciences Program, Friends of the National Zoo, National Geographic Society, and Harry Frank Guggenheim Foundation. I thank the T. Blohm family for providing Hato Masaguaral as a research site over the years and John Eisenberg for giving me the opportunity to go there.

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