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- LITERATURE CITED
The populations of the Mexican mantled howler monkey (Alouatta palliata mexicana) in the Los Tuxtlas region, Mexico, have declined drastically due to habitat loss and fragmentation. Nevertheless, several troops still inhabit very small and isolated rain forest fragments. We identified the main vegetation attributes that can favor the presence of howlers within 18 small (< 10-ha) fragments that did not differ significantly in size, shape, and isolation (nine occupied and nine unoccupied by howlers). We found that habitat quality (i.e., food resources and vegetation structure) affected howler incidence in small fragments. Particularly, the occupied fragments showed greater density of big trees (dbh > 60 cm), greater total basal area, greater basal area of persistent tree species, and greater basal area of top food species than the unoccupied fragments; suggesting that even for small fragments the loss of big trees and particularly the decrease in size class of the top food species can negatively affect howler distribution in highly fragmented landscapes. These findings could be used to establish foreground conservation areas for this critically endangered subspecies in fragmented landscapes of Los Tuxtlas.
Accelerated deforestation of tropical rain forests around the world has led to the destruction of suitable habitat for primates (Marsh 2003, Estrada et al. 2006). As deforestation increases, there is a reduction in fragment size and an increase in fragment isolation (Fahrig 2003). As fragments become smaller, more irregularly shaped, and more isolated, their floristic composition, plant species diversity, and vegetation structure are increasingly modified (Benítez-Malvido 1998; Laurance et al. 1998, 2000; Hill & Curran 2003; Arroyo-Rodríguez & Mandujano 2006a), potentially decreasing the quality and quantity of food resources for primates (Arroyo-Rodríguez & Mandujano 2006b). Furthermore, the magnitude of the negative fragmentation effects on the surviving fauna increases in small forest fragments due to anthropogenic activities, such as logging and hunting (Peres 1997, 2001; Chapman et al. 2000; Chiarello & de Melo 2001). Therefore, populations living in small fragments have higher probability of extinction (Hanski 1999).
Evidence from several primate species, including howler monkeys, suggests that < 10-ha fragments have little probability of being occupied (Cowlishaw & Dunbar 2000, Gilbert 2003, Mandujano & Estrada 2005, Mandujano et al. 2006). For instance, Cowlishaw and Dunbar (2000) reported that extinction rates of three primate species increased sharply when primates inhabited < 10-ha forest fragments in the Tana River, Kenya, whereas in Manaus, Brazil, Gilbert (2003) found higher number of primate species and groups in 10-ha and 100-ha fragments than in 1-ha fragments. Nevertheless, in some tropical regions the remaining forests are mainly represented by small habitat fragments scattered in human-dominated landscapes that can, however, support many native animal and plant species (Chiarello 2003, Daily et al. 2003, Mayfield & Daily 2005, Arroyo-Rodríguez & Mandujano 2006a). It is important to determine the key factors influencing the presence of particular species in these very small fragments as in some cases these fragments may represent the only remaining habitat for several species. Therefore, this information may help in designing management and conservation strategies.
Numerous studies have shown that fragment size and isolation are important spatial attributes in determining the presence (Chapman et al. 2003, Gilbert 2003, Wieczkowski 2004, Anzures-Dadda & Manson 2006) and abundance (Chiarello & de Melo 2001, Wieczkowski 2004, Martins 2005) of primates. However, evidence shows that, apart from fragment size and isolation, other habitat attributes, such as food resources play an important role in the occupation of fragments by several animal species including primates (Fleishman et al. 2002, Mbora & Meikle 2004, Anzures-Dadda & Manson 2006, Rode et al. 2006, Worman & Chapman 2006). Some studies have shown that the presence and abundance of primates are related to vegetation attributes, such as the diversity, abundance, and basal area of top food resources (Estrada & Coates-Estrada 1996, Balcomb et al. 2000, Cristóbal-Azkarate et al. 2005). In addition, for many primates, the number and size of trees correlate positively with primate abundance (Medley 1993, Mbora & Meikle 2004, Wieczkowski 2004, Anzures-Dadda & Manson 2006, Worman & Chapman 2006).
Due mainly to habitat loss and fragmentation, populations of the Mexican mantled howler monkey (Alouatta palliata mexicana) have declined drastically by 73–84 percent (Cuarón 1997), and this subspecies has been recently classified as critically endangered by the International Union for Conservation of Nature and Natural Resources (IUCN) (Cuarón et al. 2003). The populations of the Los Tuxtlas region, southeast Mexico, are the northernmost of the Neotropics (Estrada & Coates-Estrada 1996). This region has been severely fragmented during the last 60 yr (Dirzo & García 1992), and the remaining howler populations are isolated, inhabiting archipelagos of forest fragments that vary in size, degree of isolation, and habitat quality (Estrada & Coates-Estrada 1996, Cristóbal-Azkarate et al. 2005, Mandujano et al. 2006). To understand how the remaining howler populations can persist in small rain forest fragments, it is critical to identify which are the key habitat attributes favoring the distribution of howlers in this highly diverse but vanishing tropical system.
Within the genus Alouatta, A. palliata has the largest home ranges (Bicca-Marques 2003) and howler troops at Los Tuxtlas have been shown to occupy an average home range of 28 ha (Cristóbal-Azkarate & Arroyo-Rodríguez 2007). Therefore, < 10-ha fragments could be considered unsuitable habitat, and it is highly relevant for the conservation of this endangered subspecies to study the factors favoring the occurrence of primates in these small fragments. In this study, we analyzed 18 very small (< 10-ha) fragments of Los Tuxtlas region to: (1) identify differences in vegetation structure and composition that could explain the distribution of howlers in these fragments; and (2) discuss some management implications for the conservation of this subspecies.
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We recorded a total of 1351 plants, from 194 species, within 51 families in a sampled area of 18,000 m2, distributed in the 18 selected fragments. We identified 99.3 percent of plants to species. The families with the highest number of individuals were Euphorbiaceae (11.8% of all plants recorded), Moraceae (7.3%), Lauraceae (4.4%), Anacardiaceae (4.1%), and Annonaceae (4.1%). We found that certain pioneer species were notably abundant, representing 13 percent of all plants recorded (Table 4): Croton schiedeanus (Euphorbiaceae), Siparuna andina (Monimiaceae), Myriocarpa longipes (Urticaceae), Hampea nutricia (Malvaceae), Cecropia obtusifolia (Cecropiaceae).
Table 4. The ten plant species with the highest importance value indices (IVI) within occupied and unoccupied small forest fragments by howler monkeys at Los Tuxtlas, Mexico.a
|Species||Family||EG||Abundance||Basal area (m2)||IVI||Top food|
|Occupied fragments (N= 9)|
|Dendropanax arboreus||Araliaceae||Pers||25||3.14||11.43|| |
|Myriocarpa longipes||Urticaceae||Pion||35||0.89||10.61|| |
|Cecropia obtusifolia||Cecropiaceae||Pion||26||1.15|| 9.52||Yes|
|Orthion oblanceolatum||Violaceae||Pers||18||0.98|| 7.34|| |
|Cordia alliodora||Boraginaceae||Pers|| 8||2.75|| 7.55|| |
|Pseudolmedia oxyphyllaria||Moraceae||Pers||20||1.42|| 6.39||Yes|
|Hampea nutricia||Malvaceae||Pion||25||0.96|| 8.34|| |
|Terminalia amazonia||Combretaceae||Pers|| 3||2.19|| 6.42||Yes|
|Siparuna andina||Monimiaceae||Pion||26||0.64|| 5.43|| |
|Unoccupied fragments (N= 9)|
|Vochysia guatemalensis||Vochysiaceae||Pers||48||3.94||20.97|| |
|Croton schiedeanus||Euphorbiaceae||Pion||47||1.55||16.32|| |
|Dendropanax arboreus||Araliaceae||Pers||21||1.59||10.63|| |
|Rollinia mucosa||Annonaceae||Pers||15||1.91|| 9.58||Yes|
|Spondias radlkoferi||Anacardiaceae||Pers||14||1.57|| 8.20||Yes|
|Alchornea latifolia||Euphorbiaceae||Pers||17||1.30|| 8.01|| |
|Poulsenia armata||Moraceae||Pers||10||1.37|| 6.37||Yes|
|Cymbopetalum baillonii||Annonaceae||Pers||17||0.61|| 6.30|| |
|Siparuna andina||Monimiaceae||Pion||17||0.31|| 6.14|| |
|Bursera simaruba||Burseraceae||Pers|| 9||1.25|| 6.10||Yes|
Both occupied and unoccupied fragments presented top food species for howlers (Table 4). However, the IVI of top food species was greater in the occupied (IVI = 85.5) than in the unoccupied (IVI = 69.6) fragments (Table 3). It was interesting that both Brosimum alicastrum (Moraceae) and C. obtusifolia (Cecropiaceae) were found among the four most important plant species of the occupied fragments (Tables 3 and 4).
Considering the 15 vegetation attributes analyzed, only four attributes significantly differed between occupied and unoccupied fragments (Table 2). Occupied fragments presented greater total basal area (Wald χ2= 7.6, df = 1, P= 0.006), greater basal area of top food species (Wald χ2= 5.6, df = 1, P= 0.02), greater basal area of persistent species (Wald χ2= 5.0, df = 1, P= 0.03), and greater density of large trees (dbh > 60 cm) (Wald χ2= 4.4, df = 1, P= 0.04) than unoccupied ones (Table 2).
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- LITERATURE CITED
As the occupied and unoccupied fragments showed no significant differences in size, shape, and degree of isolation (Table 1), we expected few differences in vegetation attributes between the two types of fragments (Benítez-Malvido 1998; Laurance et al. 1998, 2000; Hill & Curran 2003; Arroyo-Rodríguez & Mandujano 2006a). However, we found that some important vegetation attributes differed significantly between occupied and unoccupied fragments, which could explain the presence of howlers in some of the small fragments. Occupied fragments showed greater density of large trees (dbh > 60 cm) and greater basal area than unoccupied fragments. In particular, basal area in occupied fragments was greater for persistent species characteristic of old-growth forests and for the top food tree species. These findings suggest that, even for small fragments, the presence of large trees and trees of the top food species influence howler distribution in the strongly fragmented landscapes of Los Tuxtlas.
Evidence suggests that howlers feed from a wide variety of plant species but generally, they spend most of their time feeding on a small, selected number of species (Milton 1980, Bicca-Marques 2003, Cristóbal-Azkarate & Arroyo-Rodríguez 2007). The IVI values of the top food species in our study were greater in occupied fragments. In the Yucatán Peninsula, howlers (Alouatta pigra) are more abundant in forests dominated by B. alicastrum, an important food species, than in other vegetation types (J. Cristóbal-Azkarate, pers. comm). Worman and Chapman (2006) demonstrated that forest areas used by blue monkeys (Cercopithecus mitis) and gray-cheeked mangabeys (Lophocebus albigena) in Kibale National Park, Uganda, had higher basal area and densities of food resources than unused areas of the forest. Similarly, we found that important food species, such as B. alicastrum, C. obtusifolia, Pseudolmedia oxyphyllaria, Lonchocarpus cruentus, Pterocarpus rohrii, and Dussia mexicana were larger and much more abundant within occupied fragments, suggesting that the loss of these species can influence the distribution of howlers in very small fragments of Los Tuxtlas.
Edge effects are stronger in small fragments than in larger ones (Laurance & Yensen 1991, Malcolm 1994), resulting in increased mortality of big trees (Laurance et al. 1998, 2000) that could decrease the quality and quantity of food resources for howlers in the long term (Arroyo-Rodríguez & Mandujano 2006b). Furthermore, hunting pressure could be more intense in the smallest fragments, where primates are easily found and targeted (Peres 1997, 2001; Chiarello & de Melo 2001). In our study, all fragments selected were of a similar size and distance from human settlements, therefore hunting pressure is unlikely to be the principal factor explaining howler distribution within these fragments.
The strong relationships between occupancy, the density of large trees (dbh > 60 cm), the total basal area, the basal area of persistent species, and the basal area of top food plant species are useful management tools to be considered in conservation efforts. We support the idea that even forest fragments of a few hectares are unquestionably valuable for primate conservation in tropical regions, such as Los Tuxtlas, where small fragments are the only remaining habitat for numerous plant and animal species, some of which are unique to this region (Castillo-Campos & Laborde 2004, Arroyo-Rodríguez & Mandujano 2006a). In Los Tuxtlas, the largest forest fragments are located above 700-m asl (Mendoza et al. 2005) falling outside the distribution range of howler monkeys (Estrada & Coates-Estrada 1996). Therefore, it is necessary to restore the small- and medium-sized fragments on the lowlands of the Biosphere Reserve. Such action could diminish numerous edge effects that contribute to the death of big trees (Malcolm 1994; Laurance et al. 1998, 2000).