Use of early and late successional forest patches by the endangered Lowland tapir Tapirus terrestris (Perissodactyla: Tapiridae)

Large herbivores play crucial ecological roles, affecting the structure and function of terrestrial ecosystems. Their effect, however, depend on how they select plants and vegetation patches for foraging. At the landscape scale, succession is one of the processes that should generate vegetation patches with different nutritional quality, affecting selection by herbivores. Earlier successional stages should be preferred as they are dominated by plants with nutritious and palatable leaves. Here, we investigate if the Lowland tapir prefers early compared to late successional forest patches, aiming at contributing to the understanding of the ecological role of the largest terrestrial South American herbivore, and to conservation strategies for this endangered species. We sampled 12 vegetation patches varying in successional stages across a 20.000-ha continuously-forested landscape in the Brazilian Atlantic Forest, recording tapirs through standardized camera trap and track surveys, and quantifying vegetation structure and treefall gaps. Whereas the number of individuals using each patch was not influenced by successional stage, intensity of use was higher in patches in earlier successional stages, in particular patches with higher density of smaller trees and higher cover of treefall gaps. Although inferences on the effects of tapir on plant community depends on future, smaller-scale studies, our results suggest herbivory by tapirs affects forest regeneration, potentially contributing to the maintenance of plant diversity. Results also point out to the potential of mosaics encompassing old-growth and secondary forests for the conservation of the Lowland tapir.     

Ungulate biomass in relation to feeding strategy within Amazonian forests

Summary The relationship between diet and biomass was examined in the Amazonian ungulates (red brocket deer, grey brocket deer, collared peccary, white-lipped peccary, and lowland tapir) of Northeastern Peru. Tropical forest ungulates have lower biomasses than savanna or grassland ungulates, because in tropical forests the majority of primary production occurs in the canopy, well out of reach from terrestrial herbivores. Within the Amazonian ungulates, species that supplement their diet with animal material, namely the peccaries, obtain a greater crude and metabolic biomass, and higher reproductive rates than the purely herbivorous species. Omnivory appears to help terrestrial herbivores inhabiting closed canopy forests overcome some effects of food limitation.     

Frugivory and Seed Dispersal by the Lowland Tapir Tapirus terrestris in the Peruvian Amazon

The lowland tapir Tapirus terrestris is the largest herbivore in the Neotropics and feeds on a large quantity of fruits, often ingesting the seeds and defecating them intact. Seed dispersal by the lowland tapir in the southwestern Amazon was studied by examining seeds from 135 dung samples collected between 2005 and 2007. Seeds of a total of 122 plant species were identified, representing 68 genera and 33 families. The species accumulation curve showed that more species can be expected with further sampling. Many species (45%) were only encountered once, and only 10 percent of all species were found in >10 samples, indicating that the lowland tapir is an opportunistic forager. Seed diversity showed a clear seasonal pattern and was highly correlated with fruit availability. Seed diameter ranged from <1 to 25 mm with 81 percent <10 mm diam. The size distribution of seeds found in lowland tapir dung generally followed that of seeds found in the forest, but had a lower proportion of seeds in the smallest size class (<2.5 mm) and a larger proportion found in the largest size class (20–25 mm). The diversity of seeds encountered in dung of the lowland tapir in this study was much higher than in previous studies. We conclude that the lowland tapir is a potential disperser for a large number of plant species, including many that previously have been thought to be dispersed only by large primates.     

Complete plastome sequences of Equisetum arvense and Isoetes flaccida: implications for phylogeny and plastid genome evolution of early land plant lineages

Background

Understanding the forces that shaped Neotropical diversity is central issue to explain tropical biodiversity and inform conservation action; yet few studies have examined large, widespread species. Lowland tapir (Tapirus terrrestris, Perissodactyla, Tapiridae) is the largest Neotropical herbivore whose ancestors arrived in South America during the Great American Biotic Interchange. A Pleistocene diversification is inferred for the genus Tapirus from the fossil record, but only two species survived the Pleistocene megafauna extinction. Here, we investigate the history of lowland tapir as revealed by variation at the mitochondrial gene Cytochrome b, compare it to the fossil data, and explore mechanisms that could have shaped the observed structure of current populations.

Results

Separate methodological approaches found mutually exclusive divergence times for lowland tapir, either in the late or in the early Pleistocene, although a late Pleistocene divergence is more in tune with the fossil record. Bayesian analysis favored mountain tapir (T. pinchaque) paraphyly in relation to lowland tapir over reciprocal monophyly, corroborating the inferences from the fossil data these species are sister taxa. A coalescent-based analysis rejected a null hypothesis of allopatric divergence, suggesting a complex history. Based on the geographic distribution of haplotypes we propose (i) a central role for western Amazonia in tapir diversification, with a key role of the ecological gradient along the transition between Andean subcloud forests and Amazon lowland forest, and (ii) that the Amazon river acted as an barrier to gene flow. Finally, the branching patterns and estimates based on nucleotide diversity indicate a population expansion after the Last Glacial Maximum.

Conclusions

This study is the first examining lowland tapir phylogeography. Climatic events at the end of the Pleistocene, parapatric speciation, divergence along the Andean foothill, and role of the Amazon river, have similarly shaped the history of other taxa. Nevertheless further work with additional samples and loci is needed to improve our initial assessment. From a conservation perspective, we did not find a correspondence between genetic structure in lowland tapir and ecogeographic regions proposed to define conservation priorities in the Neotropics. This discrepancy sheds doubt into this scheme's ability to generate effective conservation planning for vagile species.     

Effects of palm heart harvesting on avian frugivores in the Atlantic rain forest of Brazil

1. It has been suggested that palm fruits are keystone resources for frugivores in tropical rain forests, but no study has addressed this hypothesis. The effects of the harvesting of a dominant palm tree Euterpe edulis were studied over 2 years in the Atlantic forest of Brazil.
2. The abundance of 15 large frugivorous birds from five families (Ramphastidae, Cracidae, Cotingidae, Trogonidae and Psittacidae) was estimated using unlimited distance point counts (IPA) and encounter rate.
3. Although all species studied are known to eat Euterpe fruits, only one Cotingidae ( Carpornis melanocephalus ) and one Ramphastidae ( Ramphastos vitellinus ) were negatively affected by the removal of this palm from the forest.
4. This result indicates that Euterpe palms in the lowland forests do not fulfil the role of keystone species, because they bear ripe fruits during the period of peak overall fruit availability and because birds may switch their diets to other food sources when palms are removed.
5. Palm-heart exploitation is not recommended in small forest areas, nor in areas where E. edulis bears fruit during the period of overall fruit scarcity. Only long-term monitoring can evaluate the responses of the bird and mammal communities to the harvesting process.     

Seed Dispersal of the Palm Syagrus romanzoffiana by Tapirs in the Semi-deciduous Atlantic Forest of Argentina

Vertebrates play a fundamental role in the dispersal of Neotropical trees, generating different seed shadows according to their physical and behavioral features. Tapirs are capable of consuming great quantities of large fruits, and they defecate seeds far from parent trees. For instance, intact seeds of the palm Syagrus romanzoffiana have been found in tapir dung piles in the Atlantic Forest of southeastern Brazil, suggesting that tapirs effectively disperse this species. However, recruitment was not examined therein. We studied tapir endozoochory of large and medium seeds in the semi-deciduous Atlantic Forest of Argentina by examining dung piles found within Iguazu National Park. We recorded dung-pile positions to evaluate the spatial distribution. We also counted the number of juveniles in 2 × 2 m quadrats placed on old dung piles in latrines, beneath adults and in random sites to estimate recruitment levels. Syagrus romanzoffiana seeds were present in 98 percent of dung piles, averaging >200 seeds/dung pile, indicating that this species constitutes the main fruit component in the tapir's diet. Dung piles showed a clumped deposition pattern reflecting the use of latrines. Juvenile recruitment in latrines was 21 times higher than that of under-adult sites and 500 times greater than in random sites, and correlated with the frequency of use of the areas. We concluded that the lowland tapir is a major disperser of S. romanzoffiana . Given that this palm can be considered a keystone species, a disruption of this interaction might affect the entire community of frugivores in the long term.     

Frugivory in Amazonian Artiodactyla: evidence for the evolution of the ruminant stomach

Red and grey brocket deer and collared and white-lipped peccary of the Peruvian Amazon are frugivores and consume many types of seeds. The ruminant stomach of brocket deer functions as a mechanism to digest the abundant hard palm seeds of Iriartea sp., Euterpe sp. and Mauritia flexuosa . The sympatric peccaries also consume hard palm seeds; however, peccaries crack these palms by using their strong jaws, thick skull bones and interlocking canines. The ruminant stomach might have evolved as a means to digest structural components of seeds, similar to that employed by extant brocket deer, since ancestral ruminants appear to have evolved as smallbodied, forest-dwelling frugivores.     

Unveiling the Diet of Elusive Rainforest Herbivores in Next Generation Sequencing Era? The Tapir as a Case Study

Characterizing the trophic relationships between large herbivores and the outstanding plant diversity in rainforest is a major challenge because of their elusiveness. This is crucial to understand the role of these herbivores in the functioning of the rainforest ecosystems. We tested a non-invasive approach based on the high-throughput sequencing of environmental samples using small plant plastid sequences (the trnL P6 loop) and ribosomal ITS1 primers, referred to as DNA metabarcoding, to investigate the diet of the largest neotropical herbivore, the lowland tapir. Sequencing was performed on plant DNA extracted from tapir faeces collected at the Nouragues station, a protected area of French Guiana. In spite of a limited sampling, our approach reliably provided information about the lowland tapir''s diet at this site. Indeed, 95.1% and 74.4% of the plant families and genera identified thanks to the trnL P6 loop, respectively, matched with taxa already known to be consumed by tapirs. With this approach we were able to show that two families and eight new genera are also consumed by the lowland tapir. The taxonomic resolution of this method is limited to the plant family and genera. Complementary barcodes, such as a small portion of ITS1, can be used to efficiently narrow identifications down to the species in some problematic families. We will discuss the remaining limitations of this approach and how useful it is at this stage to unravel the diet of elusive rainforest herbivores and better understand their role as engineers of the ecosystem.     

The potential for harvesting fruits in tropical rainforests: new data from Amazonian Peru

New data shows that edible fruit and nut production in Amazonian forests is substantially lower than most conservationists assume. Direct measures of production in Amazonian Peru show that two terra firma forest types produced significantly less edible fruit than an alluvial soil forest. Swamp forest produced more edible fruit than any other forest type measured. Palms produce 60% of edible fruit productivity, averaged over three forest types, but the most preferred palm fruits are difficult to harvest because they are borne too high for easy access by collectors. Forest fruit collection in Amazonia is less productive in the short-term than all other food-producing activities except for hunting and cattle ranching. Technological, social and political changes are essential so that sustainable but intrinsically low-yielding extractive activities like fruit collecting become more attractive to Amazonians.     

Within Flood Season Variation in Fruit Consumption and Seed Dispersal by Two Characin Fishes of the Amazon

Many Amazon River fishes consume fruits and seeds from floodplain forests during the annual flood season, potentially serving as important seed dispersers and predators. Using a participatory approach, this study investigated how within-season variation in flood level relates to fruit consumption and seed dispersal by two important frugivorous fish, Colossoma macropomum and Piaractus brachypomus , in two Lower Amazon River fishing communities in Brazil. Diets of both fish species were comprised of 78–98 percent fruits, largely dominated by a few species. Diets included fruits of 27 woody angiosperms and four herbaceous species from 26 families, indicating the importance of forest and Montrichardia arborescens habitat during peak flood. A correspondence between peak fruit species richness and peak flood level was observed in one of two communities, which may reflect higher forest diversity and/or differences in selection of fishing habitat. Both fishes are seed dispersers and predators, the relative role of which did not vary by flood level, seed size, or fish size, but may vary with seed hardness. Interspecific differences in diet volume and intact seeds suggest P. brachypomus are more effective seed dispersers than C. macropomum . Overall, the spatial and temporal variation in fruit species composition and richness demonstrate plasticity in fruit consumption in relation to flood level and locally available fruits. While such diets are adaptive to the dynamic changes of Amazon floodplain habitats, the high consumption of forest fruits and seeds from mid- and late-successional species suggests that floodplain forest degradation could disrupt seed dispersal and threaten local and regional fisheries.     

Apes in space: saving an imperilled orangutan population in Sumatra

Deforestation rates in Sumatra are amongst the highest in the tropics. Lowland forests, which support the highest densities of orangutans, are particularly vulnerable to clearance and fragmentation because they are highly accessible. Consequently, many orangutans will, in the future, live in strictly or partially isolated populations. Whilst orangutans have been extensively studied in primary forests, their response to living in human-dominated landscapes remains poorly known, despite it being essential for their future management. Here, we focus on an isolated group of critically endangered Sumatran orangutans (Pongo abelii) that co-exist with farmers in a mixed agroforest system consisting of degraded natural forest, smallholder (predominantly rubber) farms and oil palm plantations. Over 24 months we conducted the first ever spatial assessment of orangutan habitat use in the human-transformed landscape of Batang Serangan, North Sumatra. From 1,204 independent crop-raiding incidents recorded, orangutans showed strong foraging preference for mixed farmland/degraded forest habitat over oil palm patches. The core home range areas of the eight adult orangutans encompassed only 14% of the available study area. Monthly home range sizes averaged 423 ha (±139, SD) for males, and 131 ± 46 ha for females, and were positively influenced by wild and cultivated fruit presence, and by crop consumption. The average daily distance travelled was similar for both adult males (868 m ± 350, SD) and females (866 m ± 195), but increased when orangutans raided crops. These findings show that orangutans can survive, demographically, in certain types of degraded landscapes, foraging on a mixture of crops and wild fruits. However, the poor quality habitat offered to orangutans by oil palm plantations, in terms of low food availability and as a barrier to female movements, is cause for concern since this is the land use type that is most rapidly replacing the preferred forest habitat across both Sumatran and Bornean orangutan ranges.     

Preferences and Food Quality of Fruit‐Feeding Butterflies in Kibale Forest,Uganda1

Many butterflies in tropical forests feed on fruits that have fallen to the forest floor. This substrate differs in many ways from floral nectar, and therefore fruit‐feeding butterflies are expected to possess adaptations for efficient foraging, choice, and ingestion of their food. Differences in food quality and in spatial and temporal availability are also likely to have led to life history evolution. Here we describe the sugar and nitrogen content of fruits that butterflies feed on in a tropical forest in Uganda, and measure the attractiveness of these fruits to the local butterfly fauna together with the role that decay plays in the attraction. These data are supplemented with feeding observations at fruit falls in the forest. Our results show that (1) fruits contain significant and variable concentrations of sugar and nitrogen, and constitute a nutritious food source for butterflies in tropical forests; (2) fruit‐feeding butterflies use cues from the fruits and fermentation products to locate their food; (3) different classes of fruit‐feeding butterflies may vary in their preferences for certain fruits, and differ in their ability to find preferred food; and (4) fruit choice is not strongly correlated with attractiveness or nutrient content. The results are discussed in the light of the evolution of food searching and life history strategies.     

Parrots consume sodium‐rich palms in the sodium‐deprived landscape of the Western Amazon Basin

Herbivorous animals face shortages of different minerals in different geographic areas. In the Amazon Basin, sodium is often limiting, driving herbivores to seek supplemental sources. In the lowlands of the western Amazon Basin, parrots commonly consume sodium‐rich soils at clay licks but lick use varies widely among species, and to date, parrots in the region have not been reported consuming other supplemental sodium sources. We document 11 species of psittacines consuming sodium‐rich leaves and trunks of Attalea butyracea palms growing on sodium‐rich soils in lowland Peru. Consumed palms had more sodium and less potassium than uneaten A. butyracea palms and other palm species in the area. Among A. butyracea palm parts, sodium and Na:K ratios were highest in trunks (consumed by parrots in 94% of the 387 foraging bouts recorded) and lowest in leaves (consumed in only 14% of foraging bouts). The low potassium and high Na:K ratio suggest that birds may be seeking not just any sodium sources, but those low in potassium, as potassium is known to exacerbate dietary sodium shortages. Use of the palms and species’ abundance in the study area were not correlated. Instead, parrot species that consumed palms the most were those that use relatively few traditional soil clay licks. This finding suggests that parrot species in the region have fundamental differences in preferred strategies for obtaining supplemental sodium and may help explain documented interspecific differences in geophagy.     

Day-journey length and daily diet of solitary male gorillas in lowland and highland habitats

We compared day-journey length and daily diets of solitary male gorillas in lowland versus highland habitats. Solitary males in tropical forests of Zaire tend to travel longer distances, to visit more types of vegetation, and to consume more kinds of food than a solitary male mountain gorilla in the Virunga Volcanoes did. The number of feeding sites per day is larger and the mean distance between feeding sites is far longer for the former than the latter. These observations may reflect differences in food breadth and availability between highland and lowland habitats. The herbaceous plants that are eaten by mountain gorillas are densely and evenly distributed in the higher montane forest of the Virungas, where gorillas need not cover long distances to search for food. In contrast, herbaceous plants are scarce in primary and ancient secondary forests of lowland habitats, where gorillas travel long distances and eat various fruits and insects. The patchy and unpredictable distribution of foods may extend the distances over which gorillas search for food in the lowland habitat. However, solitary males showed a prominent reduction in day-journey length and changed their choices of food during the nonfruiting season (the long rainy and dry seasons) in the lowland habitats. This strategy may have developed during the Pleistocene and may have enabled them to enlarge their ranges to the higher montane forests, where fruits are sparse throughout the year.     

Unpaved roads disrupt the effect of herbivores and pollinators on the reproduction of a dominant shrub

Anthropogenic linear developments, such as trails and firebreaks, also called soft linear developments (SLD), can influence animal behavior, altering the ecological interactions in which animals are involved. For example, SLD can affect the behavior of pollinators and herbivores, but little is known about the combined effect of these three elements on plant reproduction.We evaluated the combined effect of SLD, insect pollinators and herbivores (ungulates) on three reproductive output variables (fruit set, seed set, and seed mass) of a Mediterranean shrub (Halimium halimifolium). We considered two different habitats (SLD verges vs. adjacent scrublands), two scenarios of herbivory (with and without ungulates), and three scenarios of pollinator activity (without pollinators, with manual pollination and with natural pollination).SLD had contrasting effects on H. halimifolium reproduction. In the absence of herbivores, overall fruit set was lower in the verges of SLD than in adjacent scrublands, probably due to lower flower pollination rates. Where herbivores were present, overall fruit set was similar between habitats, because ungulate browsing was lower in SLD verges than in adjacent scrublands. The quantity and weight of seeds per fruit was similar in both habitats, probably because all fertilized flowers received similar amounts of pollen.SLD can alter the interaction among pollinators, herbivores and plants, leading to changes in the reproductive performance of the latter. These changes can have strong negative impacts on endangered plants that rely on fruit and seed production to persist. However, SLD verges could be safe places for plants particularly sensitive to herbivory by ungulates.     

Fruit production of the Ungurahua Palm (Oenocarpus bataua subsp.Bataua, Arecaceae) in an Indigenous Managed Reserve

The ungurahua palm (Oenocarpus bataua subsp.bataua) is widely used throughout the Amazon Basin for its thatch, fibers, wood, and edible fruits. The fruits of this species are especially important to indigenous peoples and yield a high quality oil. This study examines the use of this species by the Siona people of the Ecuadorian Amazon in the Cuyabeno Faunistic Reserve. The reproductive phenology, fruit production, and relationship between vegetative characteristics and fruit production is explored here. Fruit production varies greatly from palm to palm with a range of approximately 500–7000 fruits biennially. This amounts to approximately 700 kg/ha every two years. Height, diameter breast height (dbh), and number of leaves on an individual are poor predictors of tree productivity. Reproductive histories of individual palms are examined. The economic potential of this species and the implications of overharvesting are discussed.     

Western lowland gorilla diet and resource availability: new evidence,cross-site comparisons,and reflections on indirect sampling methods

We describe the resource availability and diet of western lowland gorillas (Gorilla gorilla gorilla) from a new study site in the Central African Republic and Republic of Congo based on 3 years of study. The results, based on 715 fecal samples and 617 days of feeding trails, were similar to those reported from three other sites, in spite of differences in herb and fruit availability. Staple foods (consumed year-round) included high-quality herbs (Haumania), swamp herbs (when present), and a minimal diversity of fruit. A variety of fruits (average of 3.5 species per day and 10 per month) were selectively consumed; gorillas ignored some common fruits and incorporated rare fruits to a degree higher than predicted based on availability. During periods of fruit abundance, fruit constituted most of the diet. When succulent fruits were unavailable, gorillas used low-quality herbs (i.e., low-protein), bark, and more fibrous fruits as fallback foods. Fibrous fruit species, such as Duboscia macrocarpa and Klainedoxa gabonensis, were particularly important to gorillas at Mondika and other sites as fallbacks. The densities of these two species are similar across sites for which data are available, in spite of major differences in forest structure, suggesting they may be key species in determining gorilla density. No sex difference in diet was detected. Such little variation in western lowland gorilla diet across sites and between sexes was unexpected and may partly reflect limitations of indirect sampling.     

Nutritional Aspects of Western Lowland Gorilla (Gorilla gorilla gorilla) Diet During Seasons of Fruit Scarcity at Bai Hokou,Central African Republic

Traditionally, gorillas were classified as folivores, yet 15 years of data on western lowland gorillas (Gorilla gorilla gorilla) show their diet to contain large quantities of foliage and fruit, and to vary both seasonally and annually. The consumption of fruit by gorillas at Bai Hokou, Central African Republic, is correlated with rainfall and ripe fruit availability (Remis, 1997a). We investigated the nutritional and chemical content of gorilla foods consumed at Bai Hokou during two seasons of fruit scarcity as measured by phenological observations and compared our findings with the nutrient content of gorilla foods at other African sites. We conclude that during lean times, Bai Hokou gorillas consumed fruits with higher levels of fiber and secondary compounds than those of other populations of western lowland or mountain gorillas. Conversely, leaves consumed by Bai Hokou gorillas were relatively low in fiber and tannins. Bai Hokou gorillas appeared to meet their nutritional needs by eating a combination of fruit and foliage. They ate fruits comparatively high in secondary compounds and fiber when necessary. While gorillas are selective feeders, wherever and whenever preferred foods are scarce, their large body size and digestive anatomy enable them to consume and process a broader repertoire of foods than smaller bodied-apes.     

Ecological Responses of Frugivorous Bats to Seasonal Fluctuation in Fruit Availability in Amazonian Forests

Lowland Amazon is climatically one of the least seasonal regions on the planet, but little is known about how this is reflected in ecological seasonality. The central objective of this study was to determine whether seasonal fluctuations in the availability of fruit resources in Neotropical forests are sufficiently marked to affect the ecology and physiology of frugivorous bats. Seasonal variations in the overall bat abundance and in the captures, body condition, and reproductive activity of the two most abundant species, Carollia perspicillata and Artibeus planirostris, were studied within a region of central Brazilian Amazonia dominated by a mosaic of nonflooded (terra firme) and seasonally flooded forests (várzea and igapó). Concurrent seasonal changes in fruit availability were measured. The abundance of fruits was markedly seasonal, with far fewer resources available during the low-water season. There was a positive correlation between fruit and bat abundance. Overall, bats did not increase the consumption of arthropods during the period of fruit shortage. In A. planirostris, the body condition declined when fruits were scarcer. In both C. perspicillata and A. planirostris, foraging and reproductive activity were positively correlated with fruit availability. Consequently, the results suggest that resource seasonality is sufficiently marked to affect frugivorous bats and force them to make important eco-physiological adjustments.