Leaf-cutting ant nests support less dense and impoverished seed assemblages in a human-modified Caatinga dry forest

Regenerating forests make up an increasingly large portion of tropical landscapes worldwide and regeneration dynamics may be influenced by leaf-cutting ants (LCA), which proliferate in disturbed areas and collect seeds for fungus culturing. Here, we investigate how LCA influences seed fate in human-modified areas of Caatinga dry forest. We evaluate the seed deposition and predation on Atta opaciceps nests, foraging habitat surrounding nest and control habitat away of nest influence of 15 colonies located along a forest cover gradient during the rainy and dry seasons. For each habitat, four 50-cm² plots were established and all seeds on the soil surface were collected along 1 year. We recorded 13,628 seeds distributed among 47 species and 36.57% of the total seeds did not show any sign of predation. Nest mound habitats supported low-density and species-poor seed assemblages, which were taxonomically distinct from the control habitats. These effects only occurred in the rainy season. The proportion of undamaged seeds were similar across the habitats. While forest cover did not influence seed assemblage in terms of species richness or seed predation, it did interact with habitat type via increments in seed abundance as forest cover increased across the nests. Forest cover also affected seed composition, but only in the rainy season. These results indicate that LCA decrease seed deposition in areas under their influence, particularly on the nest mounds. As LCA profit from human disturbance in the Caatinga, their role as seed ‘sinks’ should be enhanced in disturbed Caatinga patches, particularly during the rainy season, when most of the plant recruitment occurs. Our findings reinforce the importance of LCA as drivers of forest dynamics and resilience in human-modified landscapes.     

Tropical rain forest fragmentation,howler monkeys (Alouatta palliata), and dung beetles at Los Tuxtlas,Mexico

In Neotropical rain forests, fresh mammal dung, especially that of howler monkeys, constitutes an important resource used by dung beetles as food and for oviposition and further feeding by their larvae. Tropical rain forest destruction, fragmentation, and subsequent isolation causing reductions in numbers of and the disappearance of howler moneys may result in decreasing numbers of dung beetles, but this has not been documented. In this study, we present information on the presence of howlers and dung beetles in 38 isolated forest fragments and 15 agricultural habitats. Howler monkeys were censused by visual means, while dung beetles were sampled with traps baited with a mixture of howler, cow, horse, and dog dung. Results indicated that loss of area and isolation of forest fragments result in significant decrements in howlers and dung beetles. However, dung beetle abundance was found to be closely related to the presence of howler monkeys at the sites and habitats investigated. Scenarios of land management designed to reduce isolation among forest fragments may help sustain populations of howler monkeys and dung beetles, which may have positive consequences for rain forest regeneration. Am. J. Primatol. 48:253–262, 1999. © 1999 Wiley‐Liss, Inc.     

Seed dispersal by ants in the semi-arid Caatinga of North-East Brazil

BACKGROUND AND AIMS: Myrmecochory is a conspicuous feature of several sclerophyll ecosystems around the world but it has received little attention in the semi-arid areas of South America. This study addresses the importance of seed dispersal by ants in a 2500-km(2) area of the Caatinga ecosystem (north-east Brazil) and investigates ant-derived benefits to the plant through myrmecochory. METHODS: Seed manipulation and dispersal by ants was investigated during a 3-year period in the Xingó region. Both plant and ant assemblages involved in seed dispersal were described and ant behaviour was characterized. True myrmecochorous seeds of seven Euphorbiaceae species (i.e. elaiosome-bearing seeds) were used in experiments designed to: (1) quantify the rates of seed cleaning/removal and the influence of both seed size and elaiosome presence on seed removal; (2) identify the fate of seeds dispersed by ants; and (3) document the benefits of seed dispersal by ants in terms of seed germination and seedling growth. KEY RESULTS: Seed dispersal by ants involved one-quarter of the woody flora inhabiting the Xingó region, but true myrmecochory was restricted to 12.8 % of the woody plant species. Myrmecochorous seeds manipulated by ants faced high levels of seed removal (38-84 %) and 83 % of removed seeds were discarded on ant nests. Moreover, seed removal positively correlated with the presence of elaiosome, and elaiosome removal increased germination success by at least 30 %. Finally, some Euphorbiaceae species presented both increased germination and seedling growth on ant-nest soils. CONCLUSIONS: Myrmecochory is a relevant seed dispersal mode in the Caatinga ecosystem, and is particularly frequent among Euphorbiaceae trees and shrubs. The fact that seeds reach micro-sites suitable for establishment (ant nests) supports the directed dispersal hypothesis as a possible force favouring myrmecochory in this ecosystem. Ecosystems with a high frequency of myrmecochorous plants appear not to be restricted to regions of nutrient-impoverished soil or to fire-prone regions.     

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.     

Floral traits and pollination systems in the Caatinga, a Brazilian tropical dry forest

BACKGROUND AND AIMS: Pollination is a critical stage in plant reproduction and thus in the maintenance and evolution of species and communities. The Caatinga is the fourth largest ecosystem in Brazil, but despite its great extent and its importance few studies providing ecological information are available, with a notable lack of work focusing on pollination biology. Here, general data are presented regarding the frequency of pollination systems within Caatinga communities, with the aim of characterizing patterns related to floral attributes in order to make possible comparisons with data for plant communities in other tropical areas, and to test ideas about the utility of syndromes. This paper also intends to provide a reference point for further studies on pollination ecology in this threatened ecosystem. METHODS: The floral traits and the pollination systems of 147 species were analysed in three areas of Caatinga vegetation in northeastern Brazil, and compared with world-wide studies focusing on the same subject. For each species, floral attributes were recorded as form, size, colour, rewards and pollination units. The species were grouped into 12 guilds according to the main pollinator vector. Analyses of the frequencies of the floral traits and pollination systems were undertaken. KEY RESULTS: Nectar and pollen were the most common floral resources and insect pollination was the most frequent, occurring in 69.9 % of the studied species. Of the entomophilous species, 61.7 % were considered to be melittophilous (43.1 % of the total). Vertebrate pollination occurred in 28.1 % of the species (ornithophily in 15.0 % and chiropterophily in 13.1 %), and anemophily was recorded in only 2.0 %. CONCLUSIONS: The results indicated that the pollination systems in Caatinga, despite climatic restrictions, are diversified, with a low percentage of generalist flowers, and similar to other tropical dry and wet forest communities, including those with high rainfall levels.     

Plant sexual systems and a review of the breeding system studies in the Caatinga, a Brazilian tropical dry forest

BACKGROUNDS AND AIMS: The reproductive biology of a community can provide answers to questions related to the maintenance of the intraspecific pollen flow and reproductive success of populations, sharing and competition for pollinators and also questions on conservation of natural habitats affected by fragmentation processes. This work presents, for the first time, data on the occurrence and frequency of plant sexual systems for Caatinga communities, and a review of the breeding system studies of Caatinga species. METHODS: The sexual systems of 147 species from 34 families and 91 genera occurring in three Caatinga areas in north-eastern Brazil were analysed and compared with worldwide studies focusing on reproductive biology of different tropical communities. KEY RESULTS: The frequency of hermaphrodite species was 83.0 % (122 species), seven of these (or 4.8 % of the total) being heterostylous. Monoecy occurred in 9.5 % (14) of the species, and andromonoecy in 4.8 % (seven). Only 2.7 % (four) of the species were dioecious. A high percentage of hermaphrodite species was expected and has been reported for other tropical ecosystems. With respect to the breeding system studies with species of the Caatinga, the authors' data for 21 species and an additional 18 species studied by others (n = 39) revealed a high percentage (61.5 %) of obligatory self-incompatibility. Agamospermy was not recorded among the Caatinga studied species. CONCLUSIONS: The plant sexual systems in the Caatinga, despite the semi-arid climate, are similar to other tropical dry and wet forest communities, including those with high rainfall levels, except for the much lower percentage of dioecious species. The high frequency of self-incompatible species is similar to that reported for Savanna areas in Brazil, and also for dry (deciduous and semideciduous) and humid tropical forest communities.     

The enhanced tool‐kit of two groups of wild bearded capuchin monkeys in the Caatinga: tool making,associative use,and secondary tools

The use of stones to crack open encapsulated fruit is widespread among wild bearded capuchin monkeys (Cebus libidinosus) inhabiting savanna‐like environments. Some populations in Serra da Capivara National Park (Piauí, Brazil), though, exhibit a seemingly broader toolkit, using wooden sticks as probes, and employing stone tools for a variety of purposes. Over the course of 701.5 hr of visual contact of two wild capuchin groups we recorded 677 tool use episodes. Five hundred and seventeen of these involved the use of stones, and 160 involved the use of sticks (or other plant parts) as probes to access water, arthropods, or the contents of insects' nests. Stones were mostly used as “hammers”—not only to open fruit or seeds, or smash other food items, but also to break dead wood, conglomerate rock, or cement in search of arthropods, to dislodge bigger stones, and to pulverize embedded quartz pebbles (licking, sniffing, or rubbing the body with the powder produced). Stones also were used in a “hammer‐like” fashion to loosen the soil for digging out roots and arthropods, and sometimes as “hoes” to pull the loosened soil. In a few cases, we observed the re‐utilization of stone tools for different purposes (N=3), or the combined use of two tools—stones and sticks (N=4) or two stones (N=5), as sequential or associative tools. On three occasions, the monkeys used smaller stones to loosen bigger quartz pebbles embedded in conglomerate rock, which were subsequently used as tools. These could be considered the first reports of secondary tool use by wild capuchin monkeys. Am. J. Primatol. 71:242–251, 2009. © 2008 Wiley‐Liss, Inc.     

Seed dispersal by red howling monkeys (Alouatta seniculus) in the tropical rain forest of French Guiana

A 2-year field study of the frugivorous diet of a howling monkey troop, in a tropical rain forest in French Guiana, shows that they disperse by endozoochory ≥95% of plant species from which they eat ripe fruit. Passage through the digestive tract of howlers does not significantly modify the germination success of most plant species samples. Their low digestion rate (X = 20 hr 40 min) is the ultimate cause of a bimodal defecation rhythm that results in the concentration of 60% of defecations being deposited under sleeping sites. The distance of seed dispersal can reach more than 550 m from parent trees,with a mean of 260 m. Although howling monkeys consume fruits differing in morphological characteristics, they are particularly able to disseminate seeds of species whose fruits have a hard and indehiscent external coat or large seeds or both. In French Guiana, they may be especially important dispersers of the Sapotaceae with fruits that simultaneously present both characteristics.     

The role of tropical dry forest as a long-term barrier to dispersal: a comparative phylogeographical analysis of dry forest tolerant and intolerant frogs

We used a comparative phylogeographical approach to investigate the origins of the disjunct wet forest biota of the Golfo Dulce region along the Pacific slope of Costa Rica. This region is isolated by Pacific dry forests north and south and isolated from Caribbean wet forests by mountains. We studied three sympatric lowland frog species in the Craugastor fitzingeri species group that prefer wet forest but differ in their response to dry habitats. In dry forest, C. fitzingeri can survive along streams while C. crassidigitus and C. talamancae are entirely absent. We collected samples from across the ranges of all three species, and obtained mitochondrial DNA sequence data from the COI and cytochrome b genes. We observed significant phylogeographical structure in C. crassidigitus and C. talamancae, but much less in C. fitzingeri, demonstrating that mountain barriers and dry forest habitat have reduced mitochondrial gene flow in the strictly wet-forest species. Additionally, we discovered that the Golfo Dulce and Central Panama populations of C. crassidigitus appear to have diverged in the Pliocene or earlier, suggesting that the dry forest separating these populations is old. Our phylogenetic analysis of 12 of approximately 16 species of the C. fitzingeri species group suggests that the three lowland species are each other's closest relatives. Because of this shared phylogenetic history, we attribute the striking differences in phylogeographical structure to the different ecologies of the frogs. In summary, we find that what appear to be minor differences in the natural history of these three closely related species may profoundly impact the potential for dispersal, range size, and cladogenesis.     

Land use,fallow period and the recovery of a Caatinga forest

Caatinga vegetation continues to be converted into mosaics of secondary forest stands, but the affect of this process on biodiversity has not yet been examined. We used 35 regenerating and old‐growth stands of Caatinga to examine the recovery of plant assemblages subsequent to slash‐and‐burn agriculture and cattle ranching/pasture in northeastern Brazil. Plant assemblages were contrasted in terms of community structure (stem density/basal area/species richness/diversity), functional (leaf habit/reproductive traits) and taxonomic composition. Soil attributes were also examined to infer potential drivers for cross‐habitat differences. As expected, plant assemblages clearly differed across a large set of community‐level attributes, including all trait categories relative to leaf habit and reproduction (pollination syndrome/floral color, size, type). Overall, old‐growth forest stands supported distinct and more diverse assemblages at the plot and habitat level; e.g., long‐lived tree species were almost exclusively found in old‐growth forest stands. For most attributes, plant assemblages subsequent to pasture exhibited intermediate values between those exhibited by old‐growth forest and those of agriculture‐related stands. Surprisingly, soils exhibited similar fertility‐related scores across habitats. Our results indicate that: (1) sprouting/resprouting represents an important mechanism of forest regeneration; (2) assemblage‐level attributes suggest recovery at distinct rates; (3) forest regeneration implies community‐level changes in both vegetative and reproductive functional attributes, including directional changes; (4) Caatinga is not able to completely recover in a period of 15‐yr following land abandonment; and (5) historical land use affects recovery rates and successional pathways/taxonomic trajectories. Seasonally dry tropical forests may intrinsically cover a wide range of patterns relative to successional model, recovery rates and successional pathways.     

Fruit choice by red howler monkeys (Alouatta seniculus) in a tropical rain forest

This paper presents and discusses aspects of fruit selectivity by red howler monkeys (Alouatta seniculus) in relation with morphological characteristics of fruits. These data are used to provide an answer to the following questions: which are the fruit characteristics that lead fruit choice of howler monkeys and to what extent fruit characteristics play a role in seed dispersal by monkeys? The frugivorous diet of a troop of red howler monkeys was determined during a 2-year field study in French Guiana. The selection of fruit by howler monkeys was analyzed in relation to the fruit availability. Results showed that, although consumption followed availability, fruit species could be classified in three categories according to their selection ratio (percentage of consumption/percentage of abundance) as “high ranking,” “middle ranking,” and “low ranking” species. Also, the 97 species of fruit eaten by the monkeys were grouped according to the morphological characteristics thought to influence the monkeys' choice. This showed that howler monkeys consumed essentially fruits with juicy pulp, bright color, and a small number of well-protected seeds. Most of high ranking species had medium-sized fruits with yellow color, and low ranking species often had small fruits. However, howler monkeys are associated with the dispersal of seeds from fruit with a hard and indehiscent pericarp and/or large seeds, like those of the Sapotaceae family. Consequently, they can be considered as “specialized” frugivores for this fruit syndrome. © l996 Wiley-Liss, Inc.     

Down by the riverside: Riparian edge effects on three monkey species in a fragmented Costa Rican forest

Rivers represent natural edges in forests, serving as transition zones between landscapes. Natural edge effects are important to study to understand how intrinsic habitat variations affect wildlife as well as the impact of human-induced forest fragmentation. We examined the influence of riparian and anthropogenic edge on mantled howler, white-faced capuchin, Central American spider monkeys, and vegetation structure at La Suerte Biological Research Station (abbreviated as LSBRS), Costa Rica. We predicted lower monkey encounter rate, tree species richness, and median dbh at both edge types compared to interior and that monkeys would show species-specific responses to edge based on size and diet. We expected large, folivorous–frugivorous howler monkeys and small, generalist capuchins would be found at increased density in forest edge, while large, frugivorous spider monkeys would be found at decreased density in forest edge. We conducted population and vegetation surveys along interior, riparian, and anthropogenic edge transects at LSBRS and used GLMM to compare vegetation and monkey encounter rate. Tree species richness and median dbh were higher in forest interior than anthropogenic edge zones. Although spider monkey encounter rate did not vary between forest edges and interior, howler monkeys were encountered at highest density in riparian edge, while capuchins were encountered at highest density in anthropogenic edge. Our results indicate that diverse forest edges have varying effects on biota. Vegetation was negatively affected by forest edges, while monkey species showed species-specific edge preferences. Our findings suggest that riparian zones should be prioritized for conservation in Neotropical forests.     

Estimation of the retention times and distances of seed dispersed by two monkey species, Alouatta seniculus and Lagothrix lagotricha, in a Colombian forest

Isolated-bout method to estimate the retention times and dispersal distances was applied to the seed dispersal by red howler monkeys (Alouatta seniculus) and Humboldts woolly monkeys (Lagothrix lagotricha) in a lowland tropical forest at La Macarena, on the border of the Macarena and Tinigua National Parks, the Department of Meta, Colombia. Continuous observations were made on the feeding and ranging behavior of well-habituated troops of howler monkeys and woolly monkeys as well as continuous collection of monkeys feces. We selected out the isolated-bout as a feeding bout on the specific species that was only once recorded within 48 h before the seeds of that species appeared in the feces of monkeys. In that case, the seeds were strongly suggested to come from that isolated bout. Then retention times, route seed dispersal distances and direct seed dispersal distances were estimated. Howler monkeys, which are regarded as generalist herbivores, showed longer retention times and dispersal distances along monkeys route than did woolly monkeys, which are specialist frugivores. However, the direct distances that seeds were carried from the mother tree were not significantly greater for howler monkeys than for woolly monkeys. This shows that both retention time and movement patterns by the monkeys, especially the total ranging area, influence the direct distance that seeds are carried from the mother tree.     

High diversity of arbuscular mycorrhizal fungi in natural and anthropized sites of a Brazilian tropical dry forest (Caatinga)

Arbuscular mycorrhizal fungi (AMF) establish symbiotic associations with higher plants, which support the establishment and maintenance of plant communities across a range of environments, including those adversely affected by anthropogenic activity as well as natural sites. This study aimed at determining the diversity and distribution of AMF in areas of the tropical semi-arid region of Caatinga, Brazil, and compare areas in a naturally preserved state with anthropized sites. We characterized AMF communities in soil samples (n = 108), based on morphological taxonomy, at three sampling occasions and from six areas (typical Caatinga, extremely sandy Caatinga, stony Caatinga, rocky Caatinga, and two typical Caatinga areas that had been modified by human activities), at the National Park of Catimbau, Northeast Brazil. Eighty AMF species were recorded, with Glomus and Acaulospora predominating at all sites. There were significant differences in the composition of AMF communities between natural and anthropized sites, and among sampling occasions. Habitat-types also influenced AMF communities in Caatinga. Extensive tropical dry forest areas, such as the Catimbau National Park possess distinct niches, which maintain diverse AMF communities that are determined by anthropogenic activities, as well as vegetation types and environmental conditions.     

Ant seed removal in a non-myrmecochorous Neotropical shrub: Implications for seed dispersal

This study investigated ant seed removal of Piper sancti-felicis, an early successional Neotropical shrub. Neotropical Piper are a classic example of bat-dispersed plants, but we suggest that ants are underappreciated dispersal agents. We identified eleven ant species from the genera Aphaenogaster, Ectatomma, Paratrechina, Pheidole, Trachymyrmex, and Wasmannia recruiting to and harvesting P. sancti-felicis seeds in forest edge and secondary forest sites at La Selva, Costa Rica. We also tested for differences in ant recruitment to five states in which ants can commonly encounter seeds: unripe fruit, ripe fruit, overripe fruit, bat feces, and cleaned seeds. Overall, ants harvested more seeds from ripe and overripe fruits than other states, but this varied among species. To better understand the mechanisms behind ant preferences for ripe/overripe fruit, we also studied how alkenylphenols, secondary metabolites found in high concentrations in P. sancti-felicis fruits, affected foraging behavior in one genus of potential ant dispersers, Ectatomma. We found no effects of alkenylphenols on recruitment of Ectatomma to fruits, and thus, these compounds are unlikely to explain differences in ant recruitment among fruits of different maturity. Considering that P. sancti-felicis seeds have no apparent adaptations for ant dispersal, and few ants removed seeds that were cleaned of pulp, we hypothesize that most ants are harvesting its seeds for the nutritional rewards in the attached pulp. This study emphasizes the importance of ants as important additional dispersers of P. sancti-felicis and suggests that other non-myrmecochorous, vertebrate-dispersed plants may similarly benefit from the recruitment to fruit by ants.     

Diet of the brown howler monkeyAlouatta fusca in a semi-deciduous forest fragment of southeastern Brazil

The diet of a group of six brown howlers was studied weekly during 12 months in a reserve of 250 ha of secondary, mesophytic, semi-deciduous forest. The phenology of 186 trees of 72 species and 29 families was monitored simultaneously. Scan sampling was used to record the diet from dawn until dusk on a total of 60 days of observation, yielding 718 hr of animal-observer contact and 2,943 feeding scans. The diet was composed of leaves (73%), flowers (12%), and fruits (5%), from 68 identified plant species.Celtis iguanae, Cassia ferruginea, andInga spp. were the main food sources, accounting for approximately 50% of the diet. Young leaves (59%) were preferred to mature leaves (31%), trees contributing 56% and lianas 41% of the leaf diet. The ingestion of young leaves was correlated to the availability of these items, however, the correlations were not significant for flowers and fruits. The diet was poorer in fruits and richer in young leaves of lianas in comparison to other howler monkey species studies, probably as a consequence of the liana abundance in this forest fragment.     

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.