Translator Disclaimer
1 December 2004 Movements of Alouatta Palliata Among Forest Fragments in Los Tuxtlas, Mexico
Author Affiliations +

Introduction

Individual dispersal is part of a reproductive strategy that balances the costs and benefits for an individual as it chooses to stay with or leave its natal group (Jones, 1995). Dispersal in Alouatta has been documented in a number of studies (Agoramoorthy and Rudran, 1993; Clarke and Glander, 2004; Glander, 1992; Moore, 1992). However, habitat fragmentation may significantly limit the options available for an individual to move between social groups (Swart and Lawes, 1996). In many cases, this interference with the ability to disperse forces primates to live in small and isolated fragments, which in turn may cause changes in foraging and activity patterns, social organization, and physiological conditions, leading to inbreeding that can diminish genetic variability (Clarke et al., 2002; Gonçalves et al., 2003). The ability to disperse across fragmented landscapes will depend on the characteristics of each species (Bicca-Marques, 2003; Jones, 1999) as well as the spatial configuration of the landscape in question (Fahrig, 2003). Tischendorf et al. (2003) defined a specialist disperser as having a low probability of crossing boundaries from habitat to matrix, a high risk of mortality while in the matrix, and fast movement and high inter-step movement correlation (i.e., small turning angles between consecutive movement steps, in matrix). In contrast, generalist dispersers have a higher probability of leaving habitat, lower dispersal mortality and less directed movement paths while traveling through the matrix (i.e., larger turning angles between consecutive movement steps).

Howler monkeys are arboreal quadrupeds and are observed only occasionally to leave the trees and walk along the ground (Glander, 1992). For example, A. pigra individuals walk among the naturally patchy vegetation in the Petenes of Yucatán (A. Estrada, pers. comm.) and Tabascan swamps (J. C. Serio-Silva, pers. comm.). The same is true for red howlers, A. seniculus, travelling among clumps of trees in the Venezuelan llanos. Data on travel patterns in continuous forest suggest that A. palliata uses routes that minimize travel times from feeding to resting trees (Garber and Jelink, 2004). Fedigan et al. (1998) mention that the formation of new A. palliata groups in Santa Rosa, Costa Rica, occurred as a result of large groups splitting, and the dispersal of lone individuals in search of females. Glander (1992) reported an average travel distance of 700 m for A. palliata at Hacienda La Pacifica, Costa Rica. Individuals had to cross open areas to reach a new group; in some cases, these movements occurred in several stages between “stepping stone” fragments. In particular, dispersal success declines with a decrease in habitat and increased fragmentation of the landscape, but the rate of this decline accelerates once the amount of remaining habitat falls below 10–20% (King and With, 2002). Therefore, one might expect that howler monkeys do not travel among fragments randomly, and that the spatial configuration of habitat patches and the nature of the surrounding matrix is critical to successful dispersal.

The tropical rainforest in Los Tuxtlas in the Mexican state of Veracruz has been largely deforested: 75% of native habitat has been lost, 20% now survives only in isolated fragments, and barely 5% is comprised of widespread contiguous rainforest at high elevations (>800 m) (Estrada and Coates-Estrada, 1996). Alouatta palliata, the mantled howler monkey native to Veracruz, now survives in archipelagos of forest fragments that vary in size, age, and degree of isolation. Their existence in these scattered forest remnants is precarious both ecologically and demographically, which compounds the dilemma of dispersal (Estrada and Coates-Estrada, 1996; Mandujano et al., in press). Here we present data on the movements of howler monkeys in this region's highly altered landscape and develop a preliminary model of the probability of interchange between fragments.

Methods

Fieldwork

This research was conducted in the Sierra Santa Marta in the south of Los Tuxtlas, Veracruz, Mexico (18°22′N, 94°45′W). We defined the study area as the landscape between the Ríos Tecuanapa and Pilapa, covering 4,960 ha, of which only 11% is suitable primate habitat (Fig. 1). Elevation ranges from sea level to 900 m. Corn crops and livestock pasture make up the matrix that surrounds the 92 remaining fragments, most of which are located in riparian zones along rivers and streams, often on slopes steeper than 30°. Some fragments are on hilltops, while others lie in permanently flooded areas. Of these fragments, 81% are smaller than 5 ha, and only five (8%) are between 10 and 75 ha. The mean distance between fragments and the higher elevation continuous forest was 3,625 m, while the mean distance from one fragment to the next was 111 m. The mean distance from any fragment to the nearest town was 880 m.

Figure 1.

The landscape of the study area in Los Tuxtlas showing the fragments (numbered) occupied by Alouatta palliata (in black) and those that were empty (in white). See Table 1 for information on each of the occupied fragments.

i1413-4705-12-3-126-f01.gif

Table 1.

Characteristics of the study area. Annual numbers and group composition of howler monkeys and of forest fragments characteristics in the study area. Fragments are labeled in Figure 1.

i1413-4705-12-3-126-t01.gif

We carried out fieldwork from January 2001 to July 2003. Three times a year we conducted a census of all fragments identified in the study area noting the presence or absence of Alouatta groups in each. Two to five people spent 4–5 hours sampling in small fragments (<10 ha) and 1–2 days in larger fragments (>10 ha). We compiled a catalog of individuals according to their identifying features and facial shapes, plus scars and coloration patterns of the back and tail. Although animal dispersal is broadly defined (see Clobert et al., 2004), for the purpose of this study we consider it be movement between fragments by individuals of any age or sex class. To quantify dispersal, we observed the movement of individuals into adjacent fragments and noted whether or not they later returned to their group of origin. We also recorded the number of solitary individuals inhabiting fragments at the time, plus the number of individuals entering empty fragments. Although we report here all the movements we observed, we recognize that there were other arrivals and departures that we were unable to observe.

Modeling

We divided up all observations of the movements of individuals between adjacent fragments into the following distance classes: 0–100 m, 101–200 m, 201–400 m, and 401–800 m. and then calculated the proportion of the movements in each. We observed no movements greater than 800 m (see Results). We then fitted these data to negative exponential, half-normal, and linear inverse models through the least squares method using the STATISTICA Program (StatSoft, Inc., 1998). These and other dispersal models have been theoretically and empirically used for investigating patterns in a number of animal and plant species (e.g., Urban and Keitt, 2001; Mennechez et al., 2003; Skalski and Gilliam, 2003).

In these three models, the dispersal probability decreased as isolation distance increased between fragments; however, the probability varied among models. For the negative exponential model, the dispersal probability pij was estimated as

i1413-4705-12-3-126-eq01.gif
for the half-normal model, the dispersal probability was
i1413-4705-12-3-126-eq02.gif
while for the linear inverse model, the dispersal probability was
i1413-4705-12-3-126-eq03.gif

In all cases, θ is a distance-decay coefficient (θ<0.0) that determines the slope of the relationship (Urban and Keitt, 2001). To fit the observed data, we made two assumptions. First, if two different primate groups inhabit the same fragment, the probability of dispersal between them is equal to 1.0 because there is no isolation. Second, if two groups inhabit different fragments with an isolation distance equal or greater than 1000 m, the probability of dispersal was equal to 0.0. The 1000 m limit was chosen considering the very few observations of howler monkeys traveling between groups inhabiting fragments at distances of this magnitude (see Glander, 1992).

Results

Overall counts ranged from 71 to 76 howler monkeys inhabiting 19 fragments — 17.5% of the 92 fragments in the study area. Three groups of howlers (of 6, 5 and 3 individuals, respectively) lived in fragment F19 (Fig. 1 and Table 1), while, at the other extreme, one group used four fragments. Eight fragments were each inhabited by a separate group, while five fragments were each inhabited by a separate solitary male. The mean isolation distance of any one occupied fragment to any other was 2.71 ±0.75 km. The mean distance of any one group to the closest fragment was 0.33 ±0.39 km, while the mean distance of the howler groups to continuous forest was 6.18 ±2.31 km.

The following are some examples of movements that we recorded:

  1. A male moved from his group in fragment F6 into fragment F8, 78 m away; he remained for almost a year, then returned to F6.

  2. Another adult male left fragment F6 to inhabit fragment F7, 79 m away. He remained in this fragment for less than six months before returning to F6.

  3. The entire group inhabiting F6 moved to F5, 120 m away, and stayed there for less than one month before returning to their original fragment.

  4. At the beginning of the study, a solitary male was found inhabiting F48. According to the field assistant and local landowners, this individual had moved from F19, 656 m away.

  5. There were no howlers in F37 when it was first surveyed, but one male who had not been recorded in the next nearest groups, F41 and F17, subsequently took up residence. We suspect that he moved from an unstudied group located 80 m away.

  6. Another male appeared in F37, probably from the nearest fragment 80 m away as well.

  7. An older male arrived in F37 and then moved on to F38. Again, we suspect that this individual was from an unstudied group located 80 m away. Local people supported this supposition.

  8. One group of six individuals initially occupied F32. This group later divided into two, each with three individuals; one group moved out and took up residence in the nearest fragment, F33, 47 m away.

  9. Fragment F4 was empty at the beginning of the study; six to eight months later, individuals were continuously observed there. It is probable that they moved from fragments F2 or F3, located 41 m and 92 m away, respectively.

  10. An adult male moved 171 m from F5 to F102.

Distance of movement ranged from 15 to 656 m, but 70% were under 100 m (Fig. 2). Data fit the negative exponential (r2 = 0.90, F = 28.6, df = 1, 3, P = 0.01) and half-normal (r2 = 0.89, F = 24.6, df = 1, 3, P = 0.02) models (Fig. 2). In contrast, data did not fit the linear inverse model (r2 = 0.47, F = 2.7, df = 1, 3, P = 0.20). The θ coefficients were –0.007 and –0.000035 for the negative exponential and half-normal models, respectively.

Figure 2.

Relationship between dispersal probability and isolation distance. The points represent the proportion of Alouatta palliata movements at different isolation distances. Note our assumptions (see methods) that at 0 m the dispersal probability is 1.00; and at 1000 m the probability is 0.00. Lines represent, from left to right, the expected probability of movements in the exponential negative, half-normal, and linear inverse models. Note the field data fit better to the negative exponential and half-normal models.

i1413-4705-12-3-126-f02.gif

Discussion

The landscape of our study area is characterized by considerable destruction and fragmentation of the natural habitats; the remaining forest occurs predominantly in small fragments with a lack of corridors between the fragments (e.g., riparian vegetation, live fences), and a homogeneous matrix consisting mainly of pastures and seasonal agriculture. As a result, Alouatta palliata is scarce, and the remaining individuals inhabit only a few fragments (19 of the 92 fragments we investigated), which are isolated from one another and from continuous forest (Rodriguez-Toledo et al., 2003; Mandujano et al., in press). As such, the probability that animals will disperse from one group to another is sharply limited by isolation distances. Considering Tischendorf et al.'s (2003) definition of specialist and generalist dispersers, we initially expected that each of the three dispersal models in this study (negative exponential, half-normal, and linear inverse) would represent the hypothetical facility with which the monkeys could disperse from one fragment to another. If a generalist species, the howler monkey would have a greater capacity to move along the ground in the matrix as it disperses from one fragment to other; in this case, the data should be adjusted to a linear inverse model. But if the howler monkey is a habitat specialist and more limited in its dispersal ability, then field data should be adjusted to a negative exponential or half-normal model. The difference between negative exponential and half-normal models is that in the first, the probability of dispersal decreases exponentially with a small increase in isolation distance; in the second model, there is an isolation distance where the dispersal probability is high, and then the probability decreases slowly. The few data obtained during field work showed that the most frequent movements were towards fragments located a very short distance away (<100 m); beyond this distance the frequency of movements dropped. Thus, data fit better into the negative exponential or halfnormal models, indicating, therefore, that A. palliata may be classified as a specialist disperser.

Our analysis suggests that the degree of structural heterogeneity in the landscape may be an important factor determining the possibility of dispersal by primates across it. In heterogeneous landscapes, primates may use forest fragments as well as tree plantations (for example, shade coffee and cacao agroecoystems) as stepping stones or corridors when moving from one forest patch to another (Estrada et al., in press). In highly homogeneous landscapes (i.e., dominated by pasture or other monocultures, with scant tree cover) exchange of individuals among fragments is more difficult. Using percolation models, it has been found that dispersal success declines with increasing fragmentation of the landscape, with this decline accelerating once the amount of suitable habitat falls below 10–20% (King and With, 2002). The connectivity of habitat patches in a landscape, therefore, depends on the dispersal capacity of the individuals. In the study landscape, connectivity is currently low (<30%) given the high rate of habitat destruction and loss, with only 11% of the original vegetation remaining, and the relatively low dispersal capacity of howler monkeys through the matrix (Palacios-Silva and Mandujano, in press).

Habitat connectivity is a central theme in both metapopulation ecology and conservation biology (Bennett, 2004). As the number of occupied fragments decreases, so too does the probability of persistence on a regional level decline, due to a possible imbalance between the extinction rate of local populations and the colonization rate (Ovaskainen and Hanski, 2004). Therefore, if the dispersal rate proves lower than the deforestation rate, the only conservation alternative on a regional level would involve habitat rehabilitation in an effort to create corridors and stepping stones, plus the translocation of individuals and/or groups to other fragments offering better survival conditions. In particular, the creation of stepping stone fragments could be an alternative management action that increases connectivity and could allow movement among primate groups (Mandujano et al., in press). Basically, a stepping stone can be any landscape element that the animal perceives as a transitional step leading toward a habitat patch (Bennett, 2004). For primates, a stepping stone can be a group of isolated trees, live fences that separate strips of land, riparian zones, corridors, remnants of arboreal vegetation and/or habitat patches that are substantially smaller than an animal's home range. Studies showed that for species with limited dispersal ability and a landscape with isolated habitat, stepping stone habitat patches greatly increase a species' ability to disperse (Bennett, 2004; King and With, 2002).

Evidently, more factors than isolation distance contribute to an individual's dispersal between habitat fragments (Clobert et al., 2004). For example, in a 30-year study of A. palliata at La Pacifica, Clarke and Glander (2004) found that female migration patterns were primarily associated with environmental variables (habitat, rainfall) and secondarily with social variables (number of females in the group, sex ratio); while male migration patterns were only associated with social variables (i.e., male-female ratio and male age). In contrast, from a census of 333 howlers in a recent study in the northern part of Los Tuxtlas, Cristobal-Azkarate et al. (2004) found 16 solitary males and only one solitary female. These authors suggest that females remain in their natal groups, probably reinforced by habitat fragmentation. Thus, the relationships between intrinsic factors (social, demographic, and genetic), habitat factors (quantity, quality, and spatial configuration), and human factors (deforestation, hunting, and others) that influence the decision of an individual monkey to stay or leave its natal group are complex. In consequence, the dispersal models presented here, based only on isolation distance between fragments, are preliminary, and field and experimental data will be required to test their accuracy and general application.

Acknowledgments

The authors thank the Mateo-Gutierrez family for their hospitality and invaluable help during the fieldwork, and also E. M. Rodriguez-Toledo and A. Gonzalez-Zamora for their assistance in the field. A. Estrada and G. Echaverria-Lozano reviewed an early version of this manuscript. The Department of Biodiversity and Animal Ecology of the Instituto de Ecologia A. C. provided the support necessary for the completion of this research. The American Society of Primatologists (ASP) and Primate Conservation, Inc. provided additional support for some aspects of this study through their respective small-grants programs.

References

  1. G. Agoramoorthy and R. Rudran . 1993. Male dispersal among free-ranging red howler monkeys (Alouatta seniculus) in Venezuela. Folia Primatol 61:92–96. Google Scholar

  2. A. F. Bennett 2004. Enlazando el Paisaje: El Papel de los Corredores y la Conectividad en la Conservación de la Vida Silvestre. UICN-Unión Mundial para la Naturaleza. San José, Costa Rica. pp. Google Scholar

  3. J. C. Bicca-Marques 2003. How do howler monkeys cope with habitat fragmentation. In Primates in Fragments: Ecology and Conservation. L. K. Marsh , editor. (ed.), pp. 283–303.Kluwer Academic/Plenum Publishers. New York. Google Scholar

  4. M. R. Clarke and K. E. Glander . 2004. Adult migration patterns of the mantled howlers of La Pacifica. Am. J. Primatol 62:Suppl. 187. Google Scholar

  5. M. R. Clarke, D. A. Collins, and E. L. Zucker . 2002. Responses to deforestation in a group of mantled howlers (Alouatta palliata) in Costa Rica. Int. J. Primatol 23:365–381. Google Scholar

  6. J. Clobert, R. A. Ims, and F. Rousset . 2004. Causes, mechanisms and consequences of dispersal. In Ecology, Genetics and Evolution of Metapopulations. I. Hanski and O. E. Gaggiotti , editors. (eds.), pp. 307–335.Elsevier Academic Press. Burlington, MA. Google Scholar

  7. J. M. Dietz, A. J. Baker, and J. D. Ballou . 2000. Demographic evidence of inbreeding depression in wild golden lion tamarins. In Genetics, Demography and Viability of Fragmented Populations. A. G. Young and G. M. Clarke , editors. (eds.), pp. 203–211.Cambridge University Press. Cambridge, UK. Google Scholar

  8. A. Estrada and R. Coates-Estrada . 1996. Tropical rain forest fragmentation and wild populations of primates at Los Tuxtlas. Int. J. Primatol 5:759–783. Google Scholar

  9. A. Estrada, J. Saenz, C. Harvey, E. Naranjo, D. Muñoz, and M. Rosales-Meda . In press Primates in agroecosystems: Conservation value of some agricultural practices in Mesoamerican landscapes. In New Perspectives in Mesoamerican Primatology: Demography and Conservation. A. Estrada, P. Garber, M. Pavelka, and L. Luecke , editors. (eds.). Kluwer Academic/Plenum Publishers. New York. Google Scholar

  10. L. Fahrig 2003. Effects of habitat fragmentation on biodiversity. Ann. Rev. Ecol. Syst 34:487–515. Google Scholar

  11. L. M. Fedigan, L. M. Rose, and R. Morera-Avila . 1998. Growth of mantled howler groups in a regenerating Costa Rican dry forest. Int. J. Primatol 19:405–432. Google Scholar

  12. P. A. Garber and P. E. Jelink . 2004. Travel patterns and spatial mapping in Nicaraguan mantled howler monkeys (Alouatta palliata). Am. J. Primatol 62:Suppl. 189–90. Google Scholar

  13. K. E. Glander 1992. Dispersal patterns in Costa Rica mantled howling monkeys. Int. J. Primatol 13:415–436. Google Scholar

  14. E. C. Gonçalves, S. F. Ferrari, A. Silva, P. E G. Coutinho, E. V. Menezes, and M. P C. Schneider . 2003. Effects of habitat fragmentation on the genetic variability of silvery marmosets, Mico argentatus. In Primates in Fragments: Ecology and Conservation. L. K. Marsh , editor. (ed.), pp. 17–28.Kluwer Academic/Plenum Publishers. New York. Google Scholar

  15. C. B. Jones 1995. Dispersal in mantled howler monkeys: A threshold model. Mastozool. Neotropical 2:207–211. Google Scholar

  16. C. B. Jones 1999. Why both sexes leave: Effects of habitat fragmentation on dispersal behavior. Endangered Species UPDATE 16:70–73. Google Scholar

  17. A. W. King and K. A. With . 2002. Dispersal success on spatially structured landscapes: When do spatial pattern and dispersal behavior really matter. Ecol. Modelling 147:23–39. Google Scholar

  18. S. Mandujano, L. A. Escobedo-Morales, R. Palacios-Silva, V. Arroyo, and E. M. Rodriguez-Toledo . In press A metapopulation approach to conservation of howler monkeys in highly altered landscape in Mexico. In New Perspectives in Mesoamerican Primatology: Demography and Conservation. A. Estrada, P. Garber, M. Pavelka, and L. Luecke , editors. (eds.). Kluwer Academic/Plenum Publishers. New York. Google Scholar

  19. G. Mennechez, N. Schtickzelle, and M. Baguette . 2003. Metapopulation dynamics of the bog fritillary butterfly: comparison of demographic parameters and dispersal between a continuous and a highly fragmented landscape. Landscape Ecol 18:279–291. Google Scholar

  20. J. Moore 1992. Dispersal, nepotism, and primate social behavior. Int. J. Primatol 13:361–378. Google Scholar

  21. O. Ovaskainen and I. Hanski . 2004. Metapopulation dynamics in highly fragmented landscapes. In Ecology, Genetics, and Evolution of Metapopulations. I. Hanski and O. E. Gaggiotti , editors. (eds.), pp. 23–44.Elsevier Academic Press. Burlington, MA. Google Scholar

  22. R. Palacios and S. Mandujano . In press Conectividad de parches de hábitat para los primates en un paisaje altamente fragmentado en el sureste de México. In Evaluación y Conservación de la Biodiversidad en Paisajes Fragmentados en Mesoamérica. J. Saénz and C. Harvey , editors. (eds.). Universidad Nacional. Costa Rica. Google Scholar

  23. E. M. Rodriguez-Toledo, S. Mandujano, and F. Garcia-Orduña . 2003. Relationships between characteristics of forest fragments and howler monkeys (Alouatta palliata mexicana) in southern Veracruz, México. In Primates in Fragments: Ecology and Conservation. L. K. Marsh , editor. (ed.), pp. 79–97.Kluwer Academic/Plenum Publishers. New York. Google Scholar

  24. G. T. Skalski and J. F. Gilliam . 2003. A diffusion-based theory of organism dispersal in heterogeneous populations. Am. Nat 161:441–458. Google Scholar

  25. J. Swart and M. J. Lawes . 1996. The effect of habitat patch connectivity on samango monkey (Cercopithecus mitis) metapopulation persistence. Ecol. Model 93:57–74. Google Scholar

  26. L. Tischendorf, D. J. Bender, and L. Fahrig . 2003. Evaluation of patch isolation metrics in mosaic landscapes for specialist vs. generalist dispersers. Landscape Ecol 18:41–50. Google Scholar

  27. D. Urban and T. Keitt . 2001. Landscape connectivity: a graph-theoretic perspective. Ecology 82:1205–1218. Google Scholar

Notes

[1] Salvador Mandujano, Luis Arturo Escobedo-Morales, and Rodolfo Palacios-Silva, Instituto de Ecología A. C., km 2.5 Carret. Ant. Coatepec No. 351, Congregación del Haya, Xalapa 91070, Veracruz, México. E-mail: <mandujan@ecologia.edu.mx>.

Salvador Mandujano, Luis Arturo Escobedo-Morales, and Rodolfo Palacios-Silva "Movements of Alouatta Palliata Among Forest Fragments in Los Tuxtlas, Mexico," Neotropical Primates 12(3), (1 December 2004). https://doi.org/10.1896/1413-4705.12.3.126
Published: 1 December 2004
JOURNAL ARTICLE
6 PAGES


SHARE
ARTICLE IMPACT
Back to Top