Landscape attributes affecting patch occupancy by howler monkeys (Alouatta palliata mexicana) at Los Tuxtlas, Mexico

Understanding how forest cover is related to patch attributes such as size, shape, and isolation, and how this influences the occurrence of a species in fragmented landscapes is an important question in landscape ecology and conservation biology. To study the effects of fragmentation on patch occupancy by the critically endangered Mexican mantled howler monkey (Alouatta palliata mexicana) in the Los Tuxtlas region of Mexico, we selected three landscapes of ca. 5,000 ha, which differed in their remaining forest cover (24, 11, and 4%). For each landscape, we related patch occupancy to forest cover, patch size and shape, and four isolation parameters. Landscape attributes varied according to forest cover, and the percentage of occupation was greater in landscapes with more forest cover. The attributes affecting the probability of occupancy differed among landscapes. Occupancy was positively related to patch size in all landscapes, but in the northernmost landscape, shape irregularity had a negative effect on occupancy, whereas in the southernmost landscape, occupancy was favored by greater distances to the nearest village. The results show that not only the total amount of forest cover but also patch configuration need to be taken into consideration when designing management strategies for the conservation of the Mexican mantled howler monkey.     

Genetic Variation of Mantled Howler Monkeys (Alouatta palliata) from Costa Rica1

We examined genetic diversity of howler monkeys (Alouatta palliata) from Costa Rica. Blood samples of howler monkeys were collected at various locations in Costa Rica, and electrophoresis of total plasma proteins yielded no variation. We also conducted starch gel electrophoresis of red cell isozymes and did not find variation for any of the 14 loci analyzed (i.e., ACP, ADA, CA2, EST, GPI, IDH, LDH‐1, LDH‐2, MDH, PGD, PGM‐1, PGM‐2, SOD, and TPI). These findings were compared with the levels of genetic variation for A. seniculus and A. belzebul from one Brazilian population. Four of the 14 isozymes (ADA, GPI, PGD, and SOD) showed more than one allele for these species. Both A. seniculus and A. belzebul from Brazil showed similar levels of genetic variation. The potential causes of the low genetic variation in A. palliata from Costa Rica are discussed.     

Forest Fragmentation Modifies Habitat Quality for Alouatta palliata

Fragmentation reduces habitat area, increases the number of habitat patches, decreases their size, and increases patch isolation. For arboreal mammals such as howlers (Alouatta palliata), canopy modifications from fragmentation processes could also negatively affect habitat quality. We analyzed changes in the composition and plant structure of 15 fragments (1–76 ha) and compared them with vegetation from a continuous tropical rain forest reserve (700 ha) in Los Tuxtlas, Mexico. At each site, we sampled 1000 m² of all trees, shrubs, and lianas with a diameter at breast height (DBH) ≥10 cm. We obtained estimates of species richness, density, and basal area for different ecological groups, DBH ranges, and top food resources for howlers. We used a stepwise multiple regression analysis to determine relationships between fragment characteristics (size, shape index, and isolation) and plant variables. Compared to continuous forest, fragments have altered composition and plant structure, with large trees absent from the canopy. The basal area of top food resources is higher in continuous forest. Fragment size is the best explanation for the differences in composition and plant structure. The largest fragments had greater basal area of top food resources and more large primary trees in the canopy. Overall, our results suggest that fragmentation altered the habitat quality for howlers.     

The Role of Minerals in Food Selection in a Black Howler Monkey (Alouatta Pigra) Population in Belize Following a Major Hurricane

As plants may contain low levels of some minerals including sodium, copper, and phosphorous, herbivores may become deficient in these nutrients. In 2001, Hurricane Iris hit the Monkey River Forest in Belize causing substantial damage to the food supply of the black howler monkey population (Alouatta pigra) living there. This included an 18‐month absence in fruit production and a complete loss of figs that are high in calcium. In this article, we describe the post‐hurricane diet of this monkey population and compare the mineral content of food items to each other and to recommendations for non‐human primates [NRC 2003]. We also investigate food selection in relation to potentially limiting minerals. Behavioral data from four groups of howlers (2002–2006) and samples of all ingested food items were collected and a sample of 99 plant from 18 food species was analyzed for mineral content. Unexpectedly, the post‐hurricane diet contained more mature leaves than new leaves despite the availability of new leaves. Leaves contained higher amounts of minerals than reproductive parts and with the exception of Cecropia peltata stems, plant parts were low in sodium. Cecropia peltata is a pioneer species that grows following habitat disturbance thus the ingestion of these stems may be a potential mechanism to avoid sodium deficiency in this damaged forest. Calcium and zinc were found above recommended values in most food items; however, both positively predicted food selection, which may reflect a difference between their abundance and their bioavailability. However, as mature leaves contained more calcium than other plant parts, their high post‐hurricane consumption may also be a response to the absence of figs and the need to find an alternate calcium source. This study highlights how habitat disturbance may affect mineral abundance and the dietary choices of primates. Am. J. Primatol. 74:1054‐1063, 2012. © 2012 Wiley Periodicals, Inc.     

Gastrointestinal parasites of Howler monkeys (Alouatta palliata) inhabiting the fragmented landscape of the Santa Marta mountain range,Veracruz, Mexico

In recent years populations of howler monkeys (Alouatta palliata) in southeastern Mexico have decreased substantially due to the transformation and loss of natural habitats. This is especially evident in the Santa Marta mountain range, Veracruz, Mexico where several studies have evaluated the impact of fragmentation on howler monkey populations in order to propose management programs for their conservation. The conditions generated by fragmentation likely change the rates of parasitic infection and could decrease howler survival. In this study, gastrointestinal parasite species richness, prevalence, and egg density of infection were determined in howler groups inhabiting five forest fragments at the Santa Marta mountain range. Two hundred and seventy‐eight fresh fecal samples were collected between October 2002 and April 2003. Three parasite species were found during the dry and the wet season in all forest fragments sampled: one unidentified species of Eimeriidae; Trypanoxyuris minutus (Oxyuridae); and Controrchis biliophilus (Dicrocoeliidae). Both the prevalence of T. minutus and infection density for all parasites differed between seasons and fragments (the largest fragment consistently differed from other fragments). Host density, distance to the nearest town, fragment size, fragment shape, and total basal area of food trees explained parasite prevalence, but each species had a different pattern. Although parasite richness was lower, prevalence and density were higher than values reported for howlers in conserved forests. These results suggest that the establishment of biological corridors and animal translocation programs must take into account the parasite ecology of each fragment to avoid higher infection rates and preclude potential consequent mortality. Am. J. Primatol. 72:539–548, 2010. © 2010 Wiley‐Liss, Inc.     

The Importance of Tropical Rain Forest Fragments to the Conservation of Plant Species Diversity in Los Tuxtlas, Mexico

Of what value are forest fragments to the conservation of the tropical rain forest diversity for a landscape? We compared the changes in composition, diversity, and plant structure of 15 small (1–76 ha) relatively unprotected forest fragments with those of a large (700 ha) well protected fragment (LWPF) in Los Tuxtlas, Mexico. The trees, shrubs, lianas, palms, and herbs with dbh?≥?2.5 cm were sampled in 1000 m² at each site. For each ecological group (based on light requirements for germination: primary, secondary, and non-secondary light demanding, NSLD, species) and life form, estimates of species diversity, density, and basal area were analyzed using a stepwise multiple regression to determine whether there were any relationships between these variables and fragment characteristics (size, shape index, and isolation). The composition and plant structure of LWPF were different from those of the small fragments and large trees are absent from the canopy of the latter. Fragment size best explained the differences in composition and plant structure. Species composition in the largest fragments was similar to that of LWPF, but there was no significant difference in total richness between LWPF and the fragments, even though both the richness and abundance of secondary and NSLD species did differ. LWPF had more large primary trees in the canopy, and a greater abundance and basal area of palms and herbs. For tropical rain forest conservation, it is important to maintain the greatest possible number of large fragments and establish policies that prevent forest remnants from being further reduced in size and increasingly isolated from each other.     

Feeding and general activity patterns of a howler monkey (Alouatta palliata) troop living in a forest fragment at Los Tuxtlas,Mexico

The feeding behavior and general activity patterns of a howler monkey troop living in a 3.6 ha forest fragment were studied at Los Tuxtlas, Mexico, for an annual cycle. Monthly samples of their feeding behavior indicated that they used 52 species of 24 plant families as sources of food. Of these, 67% were trees, which accounted for 96% of total feeding time recorded. Ten species of Moraceae, Cecropiaceae, Anacrdiaceae. and Sapotaceae contributed to 70% of the trees used and to almost 90% of feeding time. The number of plant species used per monthly record varied from 7 to 31 with an average of 19.9 species. Young leaves and ripe fruit were the principal items in the monthly diet of howlers and average percent of time spent consuming these plant parts was 46.7% and 34.8%, respectively. The use of tree species was found to be associated to their importance value and to their pattern of spatial dispersal in the study site. Availability of young leaves was fairly constant from month to month, but it presented a seasonal pattern, and there was a significantly lower number of tree species bearing ripe fruit through the year with brief pulses of production. The monthly activity pattern was found to be related to variations in the availability of young leaves and ripe fruit as well as to the values of the intermonthly overlap in plant species used. Resting and feeding presented a bimodal pattern of occurrence throughout the day that seemed to be related to variations in maximum ambient temperatures. Results are discussed in light of the small size and shape of the forest fragment inhabited by the howler troop. Am. J. Primatol. 48:167–183, 1999. © 1999 Wiley‐Liss, Inc.     

Causes of Intraspecific Aggression in Alouatta palliata mexicana: Evidence from Injuries,Demography, and Habitat

Although howlers have been traditionally considered to be pacific, showing one of the lowest rates of aggression among primates, new evidence is emerging to question this image. We present data on injuries in Mexican mantled howlers (Alouatta palliata mexicana) in relation to different sociecological parameters. We censused howler populations in 19 forest fragments over a 17-mo period in the Los Tuxtlas Region, southern Veracruz, Mexico. We conducted detailed observations of scars, torn lips, broken fingers, mutilated tails and other visible injuries. We also collected data on the demography, biogeography and vegetation of each fragment in order to relate injury data to them. We censused 333 howlers, of which we exhaustively observed 254 for injuries. Four resident adult females (n = 108) and 29 adult resident males (n = 76) had injuries, while none of the solitary males (n=16), solitary females (n=1), juveniles (n=23) and infants (n=30) had them. We discuss possible interpretative scenarios for the distribution of injuries. Although some results suggest that food resource concentration may determine intergroup agonistic encounters, we propose that physical injury is primarily associated with male-male agonistic encounters during takeovers, and consequently it could indicate migration among troops.     

Differences in diet and activity pattern between two groups of Alouatta palliata associated with the availability of big trees and fruit of top food taxa

The threat that forest fragmentation and habitat loss presents for several Alouatta taxa requires us to determine the key elements that may promote the persistence of howler monkeys in forest fragments and to evaluate how changes in the availability of these elements may affect their future conservation prospects. In this study we analyzed the relationship between the availability of both big trees of top food taxa (BTTFT) (diameter at breast height>60) and fruit of top food taxa (FrTFT) in the home ranges of two groups of Alouatta palliata mexicana occupying different forest fragments in Los Tuxtlas, Mexico, and their diet and activity pattern. Both study groups preferred big trees for feeding and the group with lower availability of BTTFT in their home range fed from more, smaller food sources. Furthermore, both study groups also increased the number of food sources when their consumption of fruit decreased, and the group with lower availability of FrTFT in their home range fed from more food sources. The increase in the number of food sources used under such conditions, in turn, set up a process of higher foraging effort and lower rest. In summary, our results support other studies that suggest that the availability of big trees and fruit may be two important elements influencing the persistence of howler monkeys in forest fragments. Am. J. Primatol. 71:654–662, 2009. © 2009 Wiley‐Liss, Inc.     

Habitat fragmentation and population size of the black and gold howler monkey (Alouatta caraya) in a semideciduous forest in Northern Argentina

A population of black and gold howler monkeys (Alouatta caraya) living near the southern limit of its distribution in a semideciduous forest located in northern Argentina was studied in 2003 to evaluate the possible effects of habitat fragmentation - owing to logging - on its density and social organization within it. Aerial photographs taken in 1982, 1992, and 2001 were used to compare maps of vegetation. These maps were used to evaluate changes in the area covered by forest fragments. From March to June 2003, 10-day monthly surveys of howlers were made in each fragment. A total of 232 individual howlers were counted, belonging to 34 groups plus a solitary adult female. Groups ranged from 2 to 19 individuals (mean = 6.82, SD = 4.23), and 21% of the groups contained more than one adult male. Adults accounted for 55% of the individuals, immatures for 45%, and infants represented 13% of the total. Data obtained were compared with information available for the same population for 1982 and 1995. Results revealed no significant changes in the area of fragments, the crude and ecological density of howlers, and group composition. Group sizes and group composition of howlers suggest that the population remained stable over the past 22 years. The density, number of groups, and individuals appears not to be affected by fragmentation and logging, but crude density was low compared with other less-disturbed habitats. The status of the population remains uncertain owing to isolation, and because there are no protected areas to ensure its stability for the future.     

Biogeographical and floristic predictors of the presence and abundance of mantled howlers (Alouatta palliata mexicana) in rainforest fragments at Los Tuxtlas, Mexico

This research focuses on identifying the principal habitat characteristics that influence the presence and abundance of mantled howlers in forest fragments. We provide information on the demography of several fragmented Alouatta palliata mexicana subpopulations at Los Tuxtlas, Mexico, and relate this to the biogeographical and floristic characteristics of the forest fragments inhabited. The most important habitat characteristics related to the presence and abundance of howlers in the fragments were fragment size and floristic diversity. On the other hand, some evidence suggests that given the conditions under which howlers in our study area live (i.e., small and degraded fragments with high densities), secondary vegetation may be beneficial for the survival of the howlers. Finally, we discuss the possibility that the very low immature-to-female ratio (IFR) in the groups, and the lack of juveniles found in many of the study groups may be due to high mortality rates in immatures. A reduction in food availability because of the high population densities of these groups may be responsible for this process.     

Brief report: Infant-killing and infant disappearance following male takeovers in a group of free-ranging howling monkeys (Alouatta palliata) in Costa Rica

Events surrounding an infant-killing following a male takeover are described for a group of free-ranging howling monkeys in Costa Rica, and additional evidence is presented for infant disappearances following three previous male takeovers. Infant-killing is best interpreted in this context as a male reproductive strategy, as infant-killing did effectively shorten the interbirth interval, and only infants of high-ranking females died or disappeared following a male takeover. Due to the exclusive access of the dominant male to high-ranking estrous females, an incoming male who had lived as a peripheral male before taking over the group would run little risk of eliminating his own offspring in the course of killing the offspring of high-ranking females.     

Nutritional status of free‐ranging Mexican howler monkeys (Alouatta palliata mexicana) in Veracruz,Mexico: Serum chemistry; lipoprotein profile; vitamins D,A, and E; carotenoids; and minerals

The purpose of this work was to measure important nutritional status parameters for a group of free‐ranging Mexican mantled howler monkeys (A. palliata mexicana) and compare those data to published data for primates. The nutritional status of six free‐ranging Mexican mantled howler monkeys was examined using biochemical analysis. Blood samples were analyzed for serum chemistry; lipids; vitamins D, A, and E; carotenoids; and minerals. Serum chemistries were somewhat different from published values, but did not indicate clear abnormalities. Circulating lipids were not different from those in captive primates. Circulating vitamin D metabolites (83±16.3 for 25(OH)D ng/mL; 563±53.8 for 1,25(OH)₂D pg/mL) were similar to those in wild‐caught tamarins (Saguinus oedipus), lower than some published data for captive Cebidae and Callitrichidae, and higher than for Old World primates. Serum concentrations of retinol (16.5±1.64 μg/dl) were similar to those in captive spider monkeys (Ateles geoffroyi). Retinyl palmitate and retinyl stearate was present in howler samples and may have reflected recent dietary intake. Circulating α‐tocopherol (997±97.6 μg/dl) was similar to published values for other primates. Carotenoid levels in howlers were within the ranges reported for many primates. A significant finding was the presence of cadmium in samples that should be further studied. The number of individuals sampled was limited, and further investigation into the effects of seasonality is needed. However, this information provides new data for howler monkeys and for free‐ranging primates in general. Zoo Biol 22:239–251, 2003. © 2003 Wiley‐Liss, Inc.     

The Conservation Value of Small Fragments For Atlantic Forest Reptiles

Loss and fragmentation of natural habitats are key contributors to the decline of populations and impoverishment of biological communities. The response to these disturbances can vary substantially among taxa and depends on spatial metrics of habitat fragments and the surrounding landscape. Herein we test how fragment area, shape, isolation, and matrix quality affect reptile richness, abundance, and occurrence in Brazilian Atlantic Forest fragments, a biodiversity hotspot with a poorly studied reptile fauna. We used 23 forest fragments, ranging from 2 to 30 hectares, surrounded by different matrix types, including sugarcane crop fields, cattle ranching, subsistence farmlands and rural communities. Species richness, total reptile abundance, population abundance, and occurrence probability of many species decreased with fragment area. Model selection suggested that fragment area is the main predictor of both richness and abundance, but matrix quality as well as fragment shape are also important predictors. For population abundance and occurrence probability, fragment area and proximity were the most important predictors followed by fragment shape and matrix quality, but the strength and even the sign of predictors varied substantially among species. We highlight that the value of small fragments should not be neglected for the conservation of Atlantic Forest reptiles.     

The Ranging Costs of a Fallback Food: Liana Consumption Supplements Diet but Increases Foraging Effort in Howler Monkeys

Lianas are important components in the dynamics of tropical forests and represent fallback foods for some primates, yet little is known about their impact on primate ecology, behavior or fitness. Using 2 yr of field data, we investigated liana consumption and foraging effort in four groups of howler monkeys (two in bigger, more conserved forest fragments and two in smaller, less conserved fragments) to assess whether howler monkeys use lianas when and where food availability is scarce, and how liana consumption is related to foraging effort. Howler monkeys in smaller fragments spent more time consuming lianas and liana consumption was negatively related to the consumption of preferred food resources (fruit and Ficus spp.). Further, travel time was positively related to liana feeding time, but not to tree feeding time, and howler monkeys visited a greater number of food patches when feeding from liana leaves than when feeding from tree leaves. Our results suggest that these increases in foraging effort were related to the fact that lianas are mainly a source of leaves, and that liana patch size was probably smaller than tree patch size. While these results were clear when analyzing all four groups combined, however, they were not always significant in each of the groups individually. We suggest that this may be related to the differences in group size, patch size and the availability of resources among groups. Further studies are necessary to assess whether these dietary and behavioral adjustments negatively impact on the fitness and conservation of primates in fragments.     

Population of the black howler monkey (Alouatta pigra) in a fragmented landscape in Palenque,Chiapas, Mexico

Little is known about the population characteristics of Alouatta pigra under conditions of forest fragmentation-information that is important to understanding its tolerance to habitat loss. In this work we present data on forest loss and on troop size, age, and sex composition for a population of black howler monkeys existing in the fragmented landscape surrounding the Mayan site of Palenque, Chiapas, Mexico. Two aerial photos (1:70,000) of the study area (261 km(2)) taken in 1984 and 2001 were examined to assess forest loss. Between June and December 2001 and January and March 2002 we surveyed 44 forest fragments for the presence of howler monkeys. Examination of aerial photos showed that 33% of the forest present in 1984 had disappeared by 2001, and detected an increment in the number of forest fragments present in the landscape. We discovered a total of 115 howler monkeys living in 22 of the 44 forest fragments studied, of which 107 were members of 18 troops. The rest were solitary males or small groups of males living in isolated forest fragments. Troop size ranged from two to 15 individuals (mean 5.9+3.0 ind). 31% and 15% of individuals in the troops were juveniles and infants, respectively, suggesting continued reproductive activity. Howler monkey troops in the forest fragments were on average smaller (5.9+/-3.0 ind) than troops in the nearby protected forest of the Mayan site (7.0+/-2.8 ind). The mean density of howlers in the forest fragments was 119+/-82.9 ind/km(2). The establishment of corridors is suggested as a possible conservation scenario for the fragmented howler population investigated, and as a conservation measure to connect this population with the howler population found in the protected forest of the Mayan site.     

Fruit eating and seed dispersal by howling monkeys (Alouatta palliata) in the tropical rain forest of Los Tuxtlas,Mexico

The frugivory and ranging habits of howling monkeys living in the rain forest of Los Tuxtlas, Veracruz, Mexico, were studied for 5 consecutive years with the aim of investigating the role of seed dispersal agents played by the howling monkeys. The howling monkeys' consumption of fruit occupied half of their feeding time, and 80% of this time was spent feeding on mature fruit. Observations confirmed use of 19 tree species and a preference for a few species of Moraceae and Lauraceae. Fruit exploitation was very seasonal; only two species provided fruit year-round. Home range size was about 60 ha, and animals in the troop (N = 16) showed a day range of 10–893 m. Monthly collection of fecal samples during 2 years indicated that 90% of the seeds (N = 7,928) in the samples belonged to eight tree species and to one liana; the rest belonged to 15 unidentified species of vines. Germination success for the seeds in the feces was about 60% and for control seeds was 35%. Howling monkeys created diverse seed shadows in the vicinity of their leaf and fruit sources, and while they dispersed the seeds of some plant species, they also produced a great deal of fruit and seed waste for others.