Seed Dispersal and Ingestion of Insect-Infested Seeds by Black Howler Monkeys in Flooded Forests of the Parana River, Argentina

All howler monkey species ( Alouatta spp.) have a folivorous–frugivorous diet. Howler monkeys are reported to be seed dispersers in several areas, including black howlers ( Alouatta caraya ), which are important seed dispersers in northern Argentinean forests. The goal of this work was to study the three-way interaction between insects, seeds, and black howlers, and assess the functional significance of this tri-trophic interaction for seed dispersal. I determined through direct observation that fruits of species with a high proportion of insect infestation were important components of howler monkey diet. Ocotea diospyrifolia seeds from fresh faeces of black howlers contained dead larvae, but seeds were still able to germinate. Seeds in which larvae had reached an advanced stage of development did not germinate. Larvae of infested Eugenia punicifolia fruits were killed by digestion when they occurred in the pulp early in the fruiting season, but were dispersed alive with seeds later in the season. Banara arguta fruits contained both healthy and infested seeds; infested seeds were destroyed during digestion, while healthy seeds were dispersed. Black howlers' ingestion of infested fruits could result in the: (1) killing of larvae and dispersion of healthy seeds; (2) spread of larvae; or (3) destruction of infested seeds. This will depend on the relationship between the time at which fruit is consumed by black howlers, the time at which insect infestation occurs, and also probably on the hardness of the seed coat and the seed–insect size ratio.     

Primary Seed Dispersal by Red Howler Monkeys and the Effect of Defecation Patterns on the Fate of Dispersed Seeds1

The effectiveness of a seed disperser depends on the quantity and quality of dispersal. The quality of dispersal depends in large part on factors that affect the post–dispersal fate of seeds, and yet this aspect of dispersal quality is rarely assessed. In the particular case of seed dispersal through endozoochory, the defecation pattern produced has the potential of affecting the fate of dispersed seeds and consequently, dispersal quality and effectiveness. In this study, I assessed the effects of dung presence and dung/seed densities on seed predation by rodents and secondary dispersal by dung beetles. In particular, I compared seed fates in clumped defecation patterns, as those produced by howler monkeys, with seed fates in scattered defecation patterns, as those produced by other frugivores. I also determined the prevalence of red howler monkeys (Alouatta seniculus) as seed dispersers at the plant community level in Central Amazonia by determining the number of species they dispersed in a 25–month period. I found that dung presence and amount affected rodent and dung beetle behavior. Seed predation rates were higher when dung was present, and when it was in higher densities. The same number of seeds was buried by dung beedes, in dumped versus scattered defecation patterns, but more seeds were buried when they were inside large dung–piles versus small piles. Seed density had no effect on rodent or dung beetle behavior. Results indicate that caution should be taken when categorizing an animal as a high or low quality seed disperser before carefully examining the factors that affect the fate of dispersed seeds. Red howler monkeys dispersed the seeds of 137 species during the study period, which is the highest yet reported number for an Alouatta species, and should thus be considered highly prevalent seed dispersers at the plant community level in Central Amazonian terra firme rain forests.     

Seed Dispersal by Monkeys and the Fate of Dispersed Seeds in a Peruvian Rain Forest1

Primary seed dispersal by two species of monkeys and the effects of rodents and dung beetles on the fate of dispersed seeds are described for a rain forest in southeastern Perú. During the six-month study period (June–November 1992) spider monkeys (Ateles paniscus) dispersed the seeds of 71 plant species, whereas howler monkeys (Alouatta seniculus) dispersed seeds of 14 species. Spider and howler monkeys also differed greatly in their ranging behavior and defecation patterns, and as a consequence, produced different seed rain patterns. Monkey defecations were visited by 27 species of dung beetles (Scarabaeidae). Dung beetles buried 41 percent of the seeds in the dung, but the number of seeds buried varied greatly, according to seed size. Removal rates of unburied seeds by rodents varied between 63–97 percent after 30 d for 8 plant species. The presence of fecal material increased the percentage of seeds removed by seed predators, but this effect became insignificant with time. Although seed predators found some seeds buried in dung balls (mimicking burial by dung beetles), depth of burial significantly affected the fate of these seeds. Less than 35 percent of Brosimum lactescens seeds buried inside dung balls at a depth of 1 cm remained undiscovered by rodents, whereas at least 75 percent of the seeds escaped rodent detection at a depth of 3 cm and 96 percent escaped at 5 cm. Both dung beetles and rodents greatly affected the fate of seeds dispersed by monkeys. It is thus important to consider postdispersal factors affecting the fate of seeds when assessing the effectiveness of frugivores as seed dispersers.     

Genetic Structure and Kinship Patterns in a Population of Black Howler Monkeys, Alouatta pigra, at Palenque National Park, Mexico

We investigated the genetic structure and kinship patterns of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. Fecal samples from 49 individuals residing in eight social groups were successfully genotyped for 19 polymorphic microsatellite markers known to be variable in other ateline primates. Overall, genetic diversity was low (H_o = 0.588) with an average of 4.2 alleles per loci (range = 2–8). We found that intergroup genetic variation among adults was relatively high (mean between‐group F_ST = 0.119), largely due to the genetic divergence of one study group from the others. Intragroup kinship patterns showed that in most social groups, either adult males, adult females, or individuals of both sexes resided with same‐sexed adult kin, suggesting that some black howler males and females may not disperse from their natal group or may disperse with related individuals. Of the six sampled immigrant males, two males joined established groups by themselves, and four males formed two pairs that each took over the social group they joined after evicting the resident males. Males in both these coalitions were genetically closely related, while the two solitary immigrants were not closely related to any of the resident males present in the group they joined. Am. J. Primatol. 74:948‐957, 2012. © 2012 Wiley Periodicals, Inc.     

Seed Dispersal of a High Quality Fruit by Specialized Frugivores: High Quality Dispersal?1

Dispersal quality, as estimated by the cumulative effects of dispersal, germination, seed predation, and seedling survival, was examined for Beilschmiedia pendula (Lauraceae) in Monteverde, Costa Rica. I determined the pattern of dispersal by finding seeds deposited by birds, protected the seeds from seed predators with cages to assess germination and seedling survival, and examined seed predation rates with marked seeds. Seed predation, germination, and seedling survival were compared between seeds naturally dispersed by birds and seeds placed at randomly located sites. Approximately 70 percent of seeds dispersed by birds (N= 244) were deposited <10 m from crown edges of fruiting B. pendula trees, although some seeds were dispersed at least 70 m away. Larger seeds were more likely to be dispersed under or close to the parent trees, and larger seeds produced larger seedlings. Seed size was not correlated directly with seedling survival, but larger seedlings at three months were most likely to survive one year. Seed predation by mammals and insects and seedling mortality due to fungal pathogens were concentrated beneath the crowns of parent trees. Seedlings and saplings were more abundant beneath fruiting B. pendula trees, but individuals farther away were taller on average. Thus, dispersal is beneficial for B. pendula, but such benefits appear most pronounced at a small spatial scale; seeds dispersed >30 m from the crown edges actually had a lower probability of survival than those dispersed 10–20 m. Only 10 percent of B. pendula. seeds received high‐quality dispersal in terms of landing in the zone with the highest per seed probability of seedling survival 10–20 m from parental crowns.     

Comparative Seed Dispersal Effectiveness of Sympatric Alouatta guariba and Brachyteles arachnoides in Southeastern Brazil1

I compared the effectiveness of sympatric brown howlers (Alouatta guariba) and muriquis (Brachyteles arachnoides) as seed dispersers in terms of quantitative and qualitative attributes. I hypothesized that differences in feeding and behavioral patterns between these large‐bodied folivorous/frugivorous primates would lead to dissimilarities in their effectiveness as endozoochoric seed dispersal agents. The study was carried out in a semideciduous forest fragment of Fazenda Barreiro Rico, southeastern Brazil. Through behavioral sampling of frugivory and defecation events as well as analyses of fecal samples, I determined that A. guariba dispersed fewer species and produced a lower proportion of dung with intact seeds than B. arachnoides. There was no difference between the number of seeds in fecal samples of A. guariba and B. arachnoides. These primates affected to a similar degree both germination percentage and latency to germination of seeds they ingested or removed the pulp from. Howlers and muriquis were also similar in carrying seeds away from the parent trees. Contrary to muriquis, howlers defecated seeds under the canopy of conspecific lianas, where seeds are expected to suffer high mortality rates, and voided seeds predominantly in a clumped pattern. B. arachnoides was a more effective seed disperser when compared to A. guariba in some attributes evaluated, but not in others. Given the interspecific variation in recruitment patterns of tropical plants and the loss of frugivorous bird species at the study site, the differences between howlers and muriquis in their abilities as seed dispersers may crucially influence the composition and maintenance of seedling diversity.     

Seed Dispersal and Demography of Pioneer Trees: The Case of Hortia arborea

Abstract: This study investigates the relationships among seed dispersal, patterns of seedling recruitment and the spatial distribution of a pioneer tree (Hortia arborea, Rutaceae) in the Brazilian Atlantic forest. The study was carried out at Dois Irmãos Reserve, a 387.4 ha reserve in northeastern Brazil. Fruit shadow concentrated beneath parental trees (74.6 % < 6 m distant) and fruit removal averaged 5.6 % (0 ‐ 25.5 %). Agoutis (Dasyprocta prymnolopha, Rodentia) ate fruits in the forest and in captivity and were the only vertebrates recorded feeding on Hortia fruits. Agoutis, however, destroyed 86.7 % of the seeds they ingested. In addition, only one seed from an expected number of 1980 germinated in a treefall gap after it passed through the digestive tract of agoutis. Both seed germination and seedling recruitment were restricted to gaps, and occurred among seeds manually released from the pulp or among those from fruits that naturally rotted in gaps. Moreover, exposed seedlings were taller than those covered by plants in a gap. H. arborea appears to self‐maintain populations in the same patches of forest, which are delimited by a pool of old and newly created gaps. More specifically, there is successful recruitment in patches occupied by parents, resulting in dense clumps of H. arborea.     

Seed Dispersal Phenology and Germination Characteristics of a Drought-Prone Vegetation in Southeastern Brazil

Seed germination is determined by the environmental conditions typical of a habitat and also by the geographical origin of the source species pool. During the Quaternary, Brazilian Atlantic Rain Forest species expanded their distribution into the sandy coastal plains (restingas). Periods of water shortage, however, are frequent in the sandy substrate of the restinga. We investigated whether the germination characteristics of restinga species are more related to their biogeographical origin in the humid forest or to water shortage on sandy substrates. We characterized the seed dispersal phenology of a restinga community and conducted experiments to determine the water requirements for seed germination and the short-term seed dehydration sensitivity of different species. Species shed seeds throughout the year in the restinga. When subjected to Ψ=−0.37 MPa, seed germination percentage decreased and germination time increased in six of ten species when compared with Ψ=0 MPa. Most species showed high seed moisture content (MC>40 %) at seed dispersal. Seeds took 3–17 d to dehydrate when subjected to relative humidity≤76 percent and only two of eight species had seeds sensitive to short-term dehydration. Thus, rather than a specific set of germination characteristics related to humid or dry habitats, we gathered evidence to show that the germination characteristics of restinga species represent a multiplicity of responses that may be found in both kinds of habitat.     

The Bonobo–Dialium Positive Interactions: Seed Dispersal Mutualism

A positive interaction is any interaction between individuals of the same or different species (mutualism) that provides a benefit to both partners such as increased fitness. Here we focus on seed dispersal mutualism between an animal (bonobo, Pan paniscus) and a plant (velvet tamarind trees, Dialium spp.). In the LuiKotale rainforest southwest of Salonga National Park, Democratic Republic of Congo, seven species of the genus Dialium account for 29.3% of all trees. Dialium is thus the dominant genus in this forest. Dialium fruits make up a large proportion of the diet of a habituated bonobo community in this forest. During the 6 months of the fruiting season, more than half of the bonobos’ feeding time is devoted to Dialium fruits. Furthermore, Dialium fruits contribute a considerable proportion of sugar and protein to bonobos’ dietary intake, being among the richest fruits for these nutrients. Bonobos in turn ingest fruits with seeds that are disseminated in their feces (endozoochory) at considerable distances (average: 1.25 km after 24 hr of average transit time). Endozoochory through the gut causes loss of the cuticle protection and tegumentary dormancy, as well as an increase in size by water uptake. Thus, after gut passage, seeds are better able to germinate. We consider other primate species as a potential seed disperser and conclude that Dialium germination is dependent on passage through bonobo guts. This plant–animal interaction highlights positive effects between two major organisms of the Congo basin rainforest, and establishes the role of the bonobo as an efficient disperser of Dialium seeds. Am. J. Primatol. 75:394‐403, 2013. © 2013 Wiley Periodicals, Inc.     

The capuchin, the howler, and the Caatinga: seed dispersal by monkeys in a threatened Brazilian forest

Regeneration of the Brazilian Caatinga forest may be restricted by the naturally low diversity and density of fruit-eating animals, which has been aggravated by local faunal extinction induced by human activities. We made a preliminary evaluation of the potential seed-dispersal role of capuchin (Cebus apella libidinosus) and howler monkeys (Alouatta caraya) in Serra da Capivara National Park. The monkeys dispersed at least 26 species. Alouatta dispersed larger seeds than Cebus, and the two species apparently dispersed seeds in different local habitats. Seed dispersal by monkeys potentially makes a significant contribution to Caatinga regeneration.     

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.     

The Shape of the Female Fitness Curve for Cynoglossum officinale: Quantifying Seed Dispersal and Seedling Survival in the Field

Abstract: When hermaphroditic plants shift their sex allocation to produce more seeds and less pollen, it is frequently assumed that the female component of fitness is strictly proportional to the number of seeds produced. However, if producing more seeds results in more competition between seedlings, the female fitness gain curve levels off with high investments in seeds. The shape of this curve is relevant for sex allocation theory, but rarely have data been collected. For Cynoglossum officinale we described the relationship between the number of seeds produced on the mother plant and the number and weight of seedlings in September of the following year. As expected, around large plants of C. officinale more seedlings were retrieved after the germination period in March. The seedlings of large plants were dispersed over an area similar to that of small plants. As a result, seedlings around large plants had a significantly higher chance to have a neighbouring sibling within one dm². Survival and growth of single or grouped (density > 2) seedlings did not differ significantly. As a result, total dry weight of seedlings in September was a linear function of the number of seeds on the parent plant. Our data indicate a linear female fitness gain curve.     

Sleeping Sites and Latrines of Spider Monkeys in Continuous and Fragmented Rainforests: Implications for Seed Dispersal and Forest Regeneration

Spider monkeys (Ateles geoffroyi) use sites composed of one or more trees for sleeping (sleeping sites and sleeping trees, respectively). Beneath these sites/trees they deposit copious amounts of dung in latrines. This behavior results in a clumped deposition pattern of seeds and nutrients that directly impacts the regeneration of tropical forests. Therefore, information on the density and spatial distribution of sleeping sites and latrines, and the characteristics (i.e., composition and structure) of sleeping trees are needed to improve our understanding of the ecological significance of spider monkeys in influencing forest composition. Moreover, since primate populations are increasingly forced to inhabit fragmented landscapes, it is important to assess if these characteristics differ between continuous and fragmented forests. We assessed this novel information from eight independent spider monkey communities in the Lacandona rainforest, Mexico: four continuous forest sites and four forest fragments. Both the density of sleeping sites and latrines did not differ between forest conditions. Latrines were uniformly distributed across sleeping sites, but the spatial distribution of sleeping sites within the areas was highly variable, being particularly clumped in forest fragments. In fact, the average inter-latrine distances were almost double in continuous forest than in fragments. Latrines were located beneath only a few tree species, and these trees were larger in diameter in continuous than fragmented forests. Because latrines may represent hotspots of seedling recruitment, our results have important ecological and conservation implications. The variation in the spatial distribution of sleeping sites across the forest indicates that spider monkeys likely create a complex seed deposition pattern in space and time. However, the use of a very few tree species for sleeping could contribute to the establishment of specific vegetation associations typical of the southeastern Mexican rainforest, such as Terminalia-Dialium, and Brosimum-Dialium.     

Effects of Seed Dispersal by Three Ateline Monkey Species on Seed Germination at Tinigua National Park, Colombia

We examined the effect of seed ingestion by three ateline primates: woolly monkeys, Lagothrix lagothricha; spider monkeys, Ateles belzebuth; and, red howler, Alouatta seniculus on germination rates and latency periods of seeds of several plant species in Tinigua National Park, Colombia. We collected dispersed seeds from feces and control seeds from the parental trees and washed them for germination trials. For the majority of plants, dispersed seeds germinated as well or better than control seeds did. Although spider monkeys depend more heavily on fruits than the other monkey species do, they were not more efficient than howlers or woolly monkeys at improving germination rates. A considerable proportion of the seeds dispersed by howlers and woolly monkeys showed reduced latency periods to germination, but spider monkeys showed less effect on reducing germination time. This result may be related to longer gut retention times, but such a trend has not been observed in other primate species. We conclude that, like many other primates, ateline monkeys are effective seed dispersers in terms of their effects on the seeds they swallow because they rarely decrease their germination rates. We discuss problems that make interspecific comparisons difficult, such as inappropriate control seeds and differences associated with germination substrates, and we stress the importance of studying other components of seed dispersal effectiveness.     

Feeding Behavior of Purple‐throated Fruitcrow (Querula purpurata: Cotingidae) in the Colombian Amazon and Its Implications for Seed Dispersal1

We studied some feeding behaviors of the purple‐throated fruitcrow (Querula purpurata) in two Colombian Amazonian forests, which affect the primary seed dispersal of the plants on which it feeds. Visit length, number of fruits removed and dispersed, feeding rates, and fruit‐handling times were compared to those obtained for two other cotingas feeding on the same fruiting trees. Querula purpurata exhibited shorter visits (98 sec) and fruit‐handling times (4 sec), and higher mean feeding rates (1.6 fruits/min) than Phoenicircus nigricollis and Cotinga cayana. In contrast, P. nigricollis dispersed the highest number of seeds of four of the five tree species studied. Although Q. purpurata and P. nigricollis exhibited feeding behaviors that increase seed dispersal, Q. purpurata may be more important in the transport of seeds between habitats, while P. nigricollis may be a major seed disperser within the primary forest.     

The Ecology and Evolution of Fruit Odor: Implications for Primate Seed Dispersal

Primates are now known to possess a keen sense of smell that serves them in various contexts, including feeding. Many primate species are frugivorous and provide essential seed dispersal services to a variety of plants. Studies of pollination ecology, and recently seed dispersal ecology, indicate that animal mutualist behavior exerts selection pressures that drive changes in flower and fruit traits. As a result, the use of olfaction in in primate feeding ecology may have affected the evolution of fruit odor in species that rely on primate seed dispersal. However, this hypothesis is seldom tested. Here, we summarize the available information on how primates may have affected the evolution of fruit odor. We ask what the chemistry of primate fruit odor may look like, what information fruit odor may convey, whether there are geographical differences in fruit odor, and what other factors may affect the odor of fruits consumed by primates. We identify many gaps in the available data and offer research questions, hypotheses, and predictions for future studies. Finally, to facilitate standardization in the field, we discuss methodological issues in the process of odor sampling and analysis.     

Primate and Dung Beetle Communities in Secondary Growth Rain Forests: Implications for Conservation of Seed Dispersal Systems

Conservation efforts are often aimed at one or a few species. However, habitat sustainability relies on ecological interactions among species, such as seed dispersal. Thus, a community-scale conservation strategy may be more valuable in some settings. We describe communities of primary (primates) and secondary (dung beetles) seed dispersers from 5 sites in the Brazilian Amazon. We estimate community biomass of these taxa and, using multivariate ordination, examine the potential for natural reforestation at each site, given the communities of seed dispersers present. Since disturbed habitat is increasingly common and increasingly the focus of conservation efforts, we also examine differences among seed disperser communities between primary forest and secondary growth at each site. Analyses of faunal biomass in different localities and habitats indicate that secondary growth receives nearly as much use by primates as primary forest; given the dominant groups of dung beetles in secondary growth, disturbed habitat should show a pattern of seed burial that is clumped and deep. Areas with high biomass of Alouatta spp. and the large nocturnal dung beetle species may have the greatest potential for natural reforestation of secondary growth particularly for large seeded species. The data suggest that knowledge of the biomass of primary and secondary dispersing fauna facilitates predictions for the likelihood of disturbed habitat to regenerate and comparisons of sites in broader geographical areas e.g., Neotropical vs. Paleotropical forests.     

Frugivory and Seed Dispersal by Four Species of Primates in Madagascar's Eastern Rain Forest1

In the unique faunal assemblage of the Malagasy rain forest, lemurs appear to play particularly important roles as seed-dispersing frugivores. A three-month study of feeding ecology and seed dispersal by four species of lemurs in Madagascar's eastern rain forest found that three species, Eulemur rubriventer, Eulemur fulvus, and Varecia variegata were seed dispersers, and the fourth, Propithecus diadema, was a seed predator. In germination trials, seeds passed by lemurs sprouted significantly faster and in greater numbers than those not passed by lemurs. Analysis of fruit morphologies of 69 local plant taxa producing fleshy fruits during the study period found that these fruits fell into two well-defined color categories that correlated significantly with fruit size. Seventy seven percent of fleshy fruits greater than 10 mm in diameter were colored green, brown, tan, purplish, or black, while all fruits less than 10 mm in diameter were colored red, yellow, orange, pink, blue, or white. Three introduced exotic plant species provided exceptions to this pattern, producing fruits which were larger than 10 mm and pink or orange. Fruits chosen by the primates in this study were usually larger than 10 mm in diameter and were in nearly all cases colored green, brown, tan, purplish, red, or some combination of these colors. Morphological traits shared by fruits of multiple plant taxa in the diets of seed-dispersing lemurs suggest possible coevolved relationships between Malagasy rain forest plants and lemurs.     

Seed Treatment Optimizes Benefits of Seed Bank Storage for Restoration‐Ready Seeds: The Feasibility of Prestorage Dormancy Alleviation for Mine‐Site Revegetation

Dormant seeds of 18 species from 9 families covering a diverse range of seed dormancy syndromes and life histories from the southwest Australian biodiversity hotspot were assessed for germinability following storage at 15–25°C for 36 months. A total of 10 species with physical dormancy (PY) and 8 with either physiological dormancy (PD) or morphophysiological dormancy (MPD) were assessed as part of the study. Prior to storage, germination from dormant seeds was 1–27%, rising to 41–100% following specific dormancy‐breaking treatments. When seed dormancy was removed prior to storage for 36 months seeds from all species were found to maintain a nondormant state and germinate to a similar level to that observed at the beginning of the experiment (44–100%). Likewise, seeds that did not receive a prestorage dormancy‐breaking treatment maintained a dormant state (0–50% germination) and subsequently responded well to a dormancy‐breaking treatment immediately prior to germination assessment (49–99%). There were minimal differences in response to dormancy‐breaking treatments before and after 36 months storage (average 4–6% difference) and in the germination responses observed between both storage environments assessed (15°C/15% eRH or 15–25°C air dried). Based on these findings, storing seeds in a nondormant state does not alter germinability and this approach provides significant benefits to current seed‐based restoration programs through reduction of double handling and improved seed use efficiency.