The xeric side of the Brazilian Atlantic Forest: The forces shaping phylogeographic structure of cacti

In order to investigate biogeographic influences on xeric biota in the Brazilian Atlantic Forest (BAF), a biodiversity hotspot, we used a monophyletic group including three cactus taxa as a model to perform a phylogeographic study: Cereus fernambucensis subsp. fernambucensis, C. fernambucensis subsp. sericifer, and C. insularis. These cacti are allopatric and grow in xeric habitats along BAF, including isolated granite and gneiss rock outcrops (Inselbergs), sand dune vegetation (Restinga forest), and the rocky shore of an oceanic archipelago (islands of Fernando de Noronha). The nucleotide information from nuclear gene phytochrome C and plastid intergenic spacer trnS‐trnG was used to perform different approaches and statistical analyses, comprising population structure, demographic changes, phylogenetic relationships, and biogeographic reconstruction in both spatial and temporal scales. We recovered four allopatric population groups with highly supported branches in the phylogenetic tree with divergence initiated in the middle Pleistocene: southern distribution of C. fernambucensis subsp. fernambucensis, northern distribution of C. fernambucensis subsp. fernambucensis together with C. insularis, southern distribution of C. fernambucensis subsp. sericifer, and northern distribution of C. fernambucensis subsp. sericifer. Further, the results suggest that genetic diversity of population groups was strongly shaped by an initial colonization event from south to north followed by fragmentation. The phylogenetic pattern found for C. insularis is plausible with peripatric speciation in the archipelago of Fernando de Noronha. To explain the phylogeographic patterns, the putative effects of both climatic and sea level changes as well as neotectonic activity during the Pleistocene are discussed.     

Enhanced resistance in Theobroma cacao against oomycete and fungal pathogens by secretion of phosphatidylinositol‐3‐phosphate‐binding proteins

The internalization of some oomycete and fungal pathogen effectors into host plant cells has been reported to be blocked by proteins that bind to the effectors' cell entry receptor, phosphatidylinositol‐3‐phosphate (PI3P). This finding suggested a novel strategy for disease control by engineering plants to secrete PI3P‐binding proteins. In this study, we tested this strategy using the chocolate tree Theobroma cacao. Transient expression and secretion of four different PI3P‐binding proteins in detached leaves of T. cacao greatly reduced infection by two oomycete pathogens, Phytophthora tropicalis and Phytophthora palmivora, which cause black pod disease. Lesion size and pathogen growth were reduced by up to 85%. Resistance was not conferred by proteins lacking a secretory leader, by proteins with mutations in their PI3P‐binding site, or by a secreted PI4P‐binding protein. Stably transformed, transgenic T. cacao plants expressing two different PI3P‐binding proteins showed substantially enhanced resistance to both P. tropicalis and P. palmivora, as well as to the fungal pathogen Colletotrichum theobromicola. These results demonstrate that secretion of PI3P‐binding proteins is an effective way to increase disease resistance in T. cacao, and potentially in other plants, against a broad spectrum of pathogens.     

Carbon dynamics,net primary productivity and human‐appropriated net primary productivity across a forest–cocoa farm landscape in West Africa

Terrestrial net primary productivity (NPP) is an important metric of ecosystem functioning; however, there are little empirical data on the NPP of human‐modified ecosystems, particularly smallholder, perennial crops like cocoa (Theobroma cacao), which are extensive across the tropics. Human‐appropriated NPP (HANPP) is a measure of the proportion of a natural system's NPP that has either been reduced through land‐use change or harvested directly and, previously, has been calculated to estimate the scale of the human impact on the biosphere. Additionally, human modification can create shifts in NPP allocation and decomposition, with concomitant impacts on the carbon cycle. This study presents the results of 3 years of intensive monitoring of forest and smallholder cocoa farms across disturbance, management intensity, distance from forest and farm age gradients. We measured among the highest reported NPP values in tropical forest, 17.57 ± 2.1 and 17.7 ± 1.6 Mg C ha^?1 year^?1 for intact and logged forest, respectively; however, the average NPP of cocoa farms was still higher, 18.8 ± 2.5 Mg C ha^?1 year^?1, which we found was driven by cocoa pod production. We found a dramatic shift in litterfall residence times, where cocoa leaves decomposed more slowly than forest leaves and shade tree litterfall decomposed considerably faster, indicating significant changes in rates of nutrient cycling. The average HANPP value for all cocoa farms was 2.1 ± 1.1 Mg C ha^?1 year^?1; however, depending on the density of shade trees, it ranged from ?4.6 to 5.2 Mg C ha^?1 year^?1. Therefore, rather than being related to cocoa yield, HANPP was reduced by maintaining higher shade levels. Across our monitored farms, 18.9% of farm NPP was harvested (i.e., whole cocoa pods) and only 1.1% (i.e., cocoa beans) was removed from the system, suggesting that the scale of HANPP in smallholder cocoa agroforestry systems is relatively small.     

Comparative phylogeography and demographic history of two marsupials of the Atlantic Forest in eastern Brazil

The Atlantic Forest biodiversity hotspot in eastern South America has been the focus of several phylogeographic studies concerning relationships between populations and areas and how taxa respond to environmental changes. We infer and compare the demographic and biogeographic histories of two didelphid marsupial species, Gracilinanus microtarsus and Marmosops incanus, from the Atlantic Forest of eastern Brazil to determine how these species responded to environmental changes over time, using mitochondrial and nuclear DNA sequences. We found great intraspecific genetic divergence in both species and a strong geographic structure related to similar and spatially cohesive groups within each species. These groups are consistent with the same topographical barriers, such as mountains and river valleys. Intraspecific clades are very old, dating back to a period of tectonic activities in the Neogene (5.39–8.57 Mya). Changes in the environment over the last 7 million years lead to fairly concordant demographic changes in both marsupial species, including population expansion during the last glacial maximum (ca. 21,000 years ago) or last interglacial (ca. 120,000 years ago) or both. These results do not fit the Pleistocene refuge hypothesis as an explanation of the historical biogeography and diversification of both species in the Atlantic Forest, but are compatible with the Atlantis Forest hypothesis.     

Microhabitat Selection of three Forest Understory Birds in the Brazilian Atlantic Rainforest

When assessing fragmentation effects on species, not only habitat preferences on the landscape scale, but also microhabitat selection is an important factor to consider, as microhabitat is also affected by habitat disturbance, but nevertheless essential for species for foraging, nesting and sheltering. In the Atlantic Rainforest of Brazil we examined microhabitat selection of six Pyriglena leucoptera (white-shouldered fire-eye), 10 Sclerurus scansor (rufous-breasted leaftosser), and 30 Chiroxiphia caudata (blue manakin). We radio-tracked the individuals between May 2004 and February 2005 to gain home ranges based on individual fixed kernels. Vegetation structures in core plots and fringe plots were compared. In C. caudata, we additionally assessed the influence of behavioural traits on microhabitat selection. Further, we compared microhabitat structures in the fragmented forest with those in the contiguous, and contrasted the results with the birds' preferences. Pyriglena leucoptera preferred liana tangles that were more common in the fragmented forest, whereas S. scansor preferred woody debris, open forest floor (up to 0.5 m), and a thin closed leaf litter cover which all occurred significantly more often in the contiguous forest. Significant differences were detected in C. caudata for vegetation densities in the different strata; the distance of core plots to the nearest lek site was significantly influenced by sex and age. However, core sites of C. caudata in fragmented and contiguous forests showed no significant differences in structure. Exploring microhabitat selection and behavior may greatly support the understanding of habitat selection of species and their susceptibility to fragmentation on the landscape scale.     

Queen palm fruit selection and foraging techniques of squirrels in the Atlantic Forest

Queen palm seeds (Syagrus romanzoffiana) are a vital source of nutrients for Ingram's squirrel (Guerlinguetus ingrami), a common inhabitant of the Atlantic forest biome of Brazil. G. ingrami acts as both a seed predator and disperser of this important palm; however, little is known about how G. ingrami selects or efficiently opens queen palm seeds. The objectives of this study were to: (1) investigate the squirrel's capacity to determine the germinal orifice among the fruit's three pores, which permits more efficient opening of the fruit; (2) assess whether the thickness and size of the fruit endocarp influence the squirrel's palm selection during foraging; and (3) evaluate whether the rodents preferentially select fruits with invertebrate infestations. To answer these questions, we used a series of behavioral experiments measuring patterns of squirrel feeding behavior (fruit opening, fruit selection, and patch selection), controlling for environmental variables. We found that (1) squirrels identify the queen palm germinal pore by its greater relative depth to the other pores; (2) the average size and thickness of fruit does not influence the squirrel's choice of palm for foraging; and (3) squirrels preferentially consume fruits infested by invertebrates. The development of methods for more efficient processing of queen palm fruit highlights the importance of this resource for G. ingrami. In addition, due to its preferential selection of infested fruits, G. ingrami may benefit palms by reducing parasite population loads.     

The conservation value of cacao agroforestry for bird functional diversity in tropical agricultural landscapes

Cacao agroforestry have been considered as biodiversity‐friendly farming practices by maintaining habitats for a high diversity of species in tropical landscapes. However, little information is available to evaluate whether this agrosystem can maintain functional diversity, given that agricultural changes can affect the functional components, but not the taxonomic one (e.g., species richness). Thus, considering functional traits improve the understanding of the agricultural impacts on biodiversity. Here, we measured functional diversity (functional richness‐FD, functional evenness‐FEve, and functional divergence‐Rao) and taxonomic diversity (species richness and Simpson index) to evaluate changes of bird diversity in cacao agroforestry in comparison with nearby mature forests (old‐growth forests) in the Brazilian Atlantic Forest. We used data from two landscapes with constraining areas of mature forest (49% Una and 4.8% Ilhéus) and cacao agroforestry cover (6% and 82%, respectively). To remove any bias of species richness and to evaluate assembly processes (functional overdispersion or clustering), all functional indices were adjusted using null models. Our analyses considered the entire community, as well as separately for forest specialists, habitat generalists, and birds that contribute to seed dispersal (frugivores/granivores) or invertebrate removal (insectivores). Our findings showed that small cacao agroforestry in the forested landscape sustains functional diversity (FD and FEve) as diverse as nearby forests when considering the entire community, forest specialist, and habitat generalists. However, we observed declines for frugivores/granivores and insectivores (FD and Rao). These responses of bird communities differed from those observed by taxonomic diversity, suggesting that even species‐rich communities in agroforestry may capture lower functional diversity. Furthermore, communities in both landscapes showed either functional clustering or neutral processes as the main driver of functional assembly. Functional clustering may indicate that local conditions and resources were changed or lost, while neutral assemblies may reveal high functional redundancy at the landscape scale. In Ilhéus, the neutral assembly predominance suggests an effect of functional homogenization between habitats. Thus, the conservation value of cacao agroforestry to harbor species‐rich communities and ecosystem functions relies on smallholder production with reduced farm management in a forested landscape. Finally, we emphasize that seed dispersers and insectivores should be the priority conservation targets in cacao systems.     

Evidence for Seed Dispersal by Rodents in Tropical Montane Forest in Africa

Seed dispersal by rodents has been understudied in Africa. Based on seed‐removal experiments, the presence of seeds in burrows and caches, cotyledon burial of seedlings, and images from camera traps, we provide evidence that rodents (Cricetomys kivuensis) remove and hoard large seeds of Carapa grandiflora in Nyungwe National Park, Rwanda.     

An in situ approach to detect tree root ecology: linking ground‐penetrating radar imaging to isotope‐derived water acquisition zones

Tree root distribution and activity are determinants of belowground competition. However, studying root response to environmental and management conditions remains logistically challenging. Methodologically, nondestructive in situ tree root ecology analysis has lagged. In this study, we tested a nondestructive approach to determine tree coarse root architecture and function of a perennial tree crop, Theobroma cacao L., at two edaphically contrasting sites (sandstone and phyllite–granite derived soils) in Ghana, West Africa. We detected coarse root vertical distribution using ground‐penetrating radar and root activity via soil water acquisition using isotopic matching of δ¹⁸O plant and soil signatures. Coarse roots were detected to a depth of 50 cm, however, intraspecifc coarse root vertical distribution was modified by edaphic conditions. Soil δ¹⁸O isotopic signature declined with depth, providing conditions for plant–soil δ¹⁸O isotopic matching. This pattern held only under sandstone conditions where water acquisition zones were identifiably narrow in the 10–20 cm depth but broader under phyllite–granite conditions, presumably due to resource patchiness. Detected coarse root count by depth and measured fine root density were strongly correlated as were detected coarse root count and identified water acquisition zones, thus validating root detection capability of ground‐penetrating radar, but exclusively on sandstone soils. This approach was able to characterize trends between intraspecific root architecture and edaphic‐dependent resource availability, however, limited by site conditions. This study successfully demonstrates a new approach for in situ root studies that moves beyond invasive point sampling to nondestructive detection of root architecture and function. We discuss the transfer of such an approach to answer root ecology questions in various tree‐based landscapes.     

Bats and birds increase crop yield in tropical agroforestry landscapes

Human welfare is significantly linked to ecosystem services such as the suppression of pest insects by birds and bats. However, effects of biocontrol services on tropical cash crop yield are still largely unknown. For the first time, we manipulated the access of birds and bats in an exclosure experiment (day, night and full exclosures compared to open controls in Indonesian cacao agroforestry) and quantified the arthropod communities, the fruit development and the final yield over a long time period (15 months). We found that bat and bird exclusion increased insect herbivore abundance, despite the concurrent release of mesopredators such as ants and spiders, and negatively affected fruit development, with final crop yield decreasing by 31% across local (shade cover) and landscape (distance to primary forest) gradients. Our results highlight the tremendous economic impact of common insectivorous birds and bats, which need to become an essential part of sustainable landscape management.     

Optimizing Diversity Assessment Protocols for High Canopy Ants in Tropical Rain Forest

The canopies of tropical rain forests support highly diverse, yet poorly known, animal and plant communities. It is vital that researchers who invest the time needed to gain access to the high canopy are able efficiently to survey the animals and plants that they find there. Here, we develop diversity assessment protocols for one of the most ecologically important canopy animal groups, the ants, in lowland dipterocarp rain forest in Sabah, Malaysia. We design and test a novel trap (the purse‐string trap) that can be remotely collected, thus avoiding disturbance to ants. We compare this modified trap with two other methods for surveying canopy ants: precision insecticide fogging and baited pitfall trapping. In total, we collected 39,351 ants belonging to 173 species in 38 genera. Fogging collected the most individuals and species, followed by purse‐string trapping with baited pitfall trapping catching the fewest. Fogging also resulted in samples with a different species composition to purse‐string trapping and baited pitfall trapping, which were not different from one another. Using a ‘greedy algorithm’, which guides the selection of inventory methods in order to maximize new species discovered per researcher‐hour, we show that projects allocating fewer than 132 researcher‐hours to canopy ant collection and identification should sample exclusively using fogging. Those with more time should use a combination of methods. This prioritization technique could be used to accelerate species discovery in future rapid biodiversity assessments. Abstract in Malay is available in the online version of this article.     

Abundance,density and activity of Salvator merianae (Reptilia: Teiidae) and the effect of poaching on the site occupancy by the lizard in an Atlantic Forest Reserve,Brazil

We aimed to estimate the density, occupancy and detectability of Salvator merianae (Tegu) in one of the largest Atlantic rainforest remnants in Espírito Santo, Brazil, the VNR. Species patch occupancy was modelled and used to predict the response direction of six covariates based on prior knowledge of the Tegu's ecology. A priori, we expected that the covariates measured should represent key habitat features for the species (i.e. temperature, forest edge, open habitats) or elements possibly avoided by the species, based on the hypothesis that poaching would have a negative effect on patch occupancy. We used line‐transect surveys to estimate density and abundance. Camera‐traps were used to estimate patch occupancy by the Tegu. Estimated density for S. merianae was 0.21 ± 0.02 Tegus/ha and estimated population size was 4990 ± 521 individuals. Patch occupancy was best described by two covariates: poaching intensity and distance to the forest edge. Detectability was affected by three covariates: poaching intensity, tree density and temperature. Our study presents robust information on abundance and density, habitat use, and activity of S. merianae in the VNR and is the first study providing data on the effects that poaching has on patch occupancy of this lizard. The data indicated that the occupancy and detectability of this species were influenced by a set of factors, providing information that can be useful in management plans in areas where this species can potentially decline and in areas where it may be introduced.     

Forest edge orientation influences leaf‐cutting ant abundance and plant drought stress in the Brazilian Atlantic forest

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RAD sequencing reveals genomewide divergence between independent invasions of the European green crab (Carcinus maenas) in the Northwest Atlantic

Genomic studies of invasive species can reveal both invasive pathways and functional differences underpinning patterns of colonization success. The European green crab (Carcinus maenas) was initially introduced to eastern North America nearly 200 years ago where it expanded northwards to eastern Nova Scotia. A subsequent invasion to Nova Scotia from a northern European source allowed further range expansion, providing a unique opportunity to study the invasion genomics of a species with multiple invasions. Here, we use restriction‐site‐associated DNA sequencing‐derived SNPs to explore fine‐scale genomewide differentiation between these two invasions. We identified 9137 loci from green crab sampled from 11 locations along eastern North America and compared spatial variation to mitochondrial COI sequence variation used previously to characterize these invasions. Overall spatial divergence among invasions was high (pairwise F_ST ~0.001 to 0.15) and spread across many loci, with a mean F_ST ~0.052 and 52% of loci examined characterized by F_ST values >0.05. The majority of the most divergent loci (i.e., outliers, ~1.2%) displayed latitudinal clines in allele frequency highlighting extensive genomic divergence among the invasions. Discriminant analysis of principal components (both neutral and outlier loci) clearly resolved the two invasions spatially and was highly correlated with mitochondrial divergence. Our results reveal extensive cryptic intraspecific genomic diversity associated with differing patterns of colonization success and demonstrates clear utility for genomic approaches to delineating the distribution and colonization success of aquatic invasive species.     

Evolutionary dynamics of the leaf phenological cycle in an oak metapopulation along an elevation gradient

It has been predicted that environmental changes will radically alter the selective pressures on phenological traits. Long‐lived species, such as trees, will be particularly affected, as they may need to undergo major adaptive change over only one or a few generations. The traits describing the annual life cycle of trees are generally highly evolvable, but nothing is known about the strength of their genetic correlations. Tight correlations can impose strong evolutionary constraints, potentially hampering the adaptation of multivariate phenological phenotypes. In this study, we investigated the evolutionary, genetic and environmental components of the timing of leaf unfolding and senescence within an oak metapopulation along an elevation gradient. Population divergence, estimated from in situ and common‐garden data, was compared to expectations under neutral evolution, based on microsatellite markers. This approach made it possible (1) to evaluate the influence of genetic correlation on multivariate local adaptation to elevation and (2) to identify traits probably exposed to past selective pressures due to the colder climate at high elevation. The genetic correlation was positive but very weak, indicating that genetic constraints did not shape the local adaptation pattern for leaf phenology. Both spring and fall (leaf unfolding and senescence, respectively) phenology timings were involved in local adaptation, but leaf unfolding was probably the trait most exposed to climate change‐induced selection. Our data indicated that genetic variation makes a much smaller contribution to adaptation than the considerable plastic variation displayed by a tree during its lifetime. The evolutionary potential of leaf phenology is, therefore, probably not the most critical aspect for short‐term population survival in a changing climate.     

Jaguar and Puma Activity Patterns and Predator‐Prey Interactions in Four Brazilian Biomes

Jaguars (Panthera onca) and pumas (Puma concolor) coexist throughout the Neotropics. Using camera trapping in four Brazilian biomes, we compare the daily activity patterns of the jaguar and puma, and their relationships with their main prey species. We used a kernel density method to quantify daily activity patterns and to investigate overlap between these predators and their main prey. Both cats showed intensive nocturnal and crepuscular activity (0.69 and 0.14 kernel density, respectively, for jaguars; 0.68 and 0.19 kernel density, respectively, for pumas). Only in the Pantanal did we observe a pattern of concentrated diurnal activity for both species. We found little temporal segregation between jaguars and pumas, as they showed similar activity patterns with high coefficients of overlapping (average ?₁ = 0.86; SE = 0.15). We also observed a significant overlap between the activity patterns of the predators and their main prey species, suggesting that both predators adjust their activity to reduce their foraging energy expenditure. Our findings suggest that temporal partitioning is probably not a generalized mechanism of coexistence between jaguars and pumas; instead, the partitioning of habitat/space use and food resources may play a larger role in mediating top predator coexistence. Knowledge about these behavior aspects is crucial to elucidating the factors that enable coexistence of jaguars and pumas. Furthermore, an understanding of their respective activity periods is relevant to management and associated research efforts.     

Differences in seed rain composition in small and large fragments in the northeast Brazilian Atlantic Forest

Tropical forests are seriously threatened by fragmentation and habitat loss. The impact of fragment size and forest configuration on the composition of seed rain is insufficiently studied. For the present study, seed rain composition of small and large forest fragments (8–388 ha) was assessed in order to identify variations in seed abundance, species richness, seed size and dispersal mode. Seed rain was documented during a 1‐year period in three large and four small Atlantic Forest fragments that are isolated by a sugarcane matrix. Total seed rain included 20,518 seeds of 149 species of trees, shrubs, palms, lianas and herbs. Most species and seeds were animal‐dispersed. A significant difference in the proportion of seeds and species within different categories of seed size was found between small and large fragments. Small fragments received significantly more very small‐sized seeds (<0.3 cm) and less large‐seeded species (>1.5 cm) that were generally very rare, with only one species in small and eight in large fragments. We found a negative correlation between the inflow of small‐sized seeds and the percentage of forest cover. Species richness was lower in small than in large fragments, but the difference was not very pronounced. Given our results, we propose changing plant species pools through logging, tree mortality and a high inflow of pioneer species and lianas, especially in small forest fragments and areas with low forest cover. Connecting forest fragments through corridors and reforestation with local large‐seeded tree species may facilitate the maintenance of species diversity.     

How to deal with neglected tropical diseases in the light of an African ethic

Many countries in Africa, and more generally those in the Global South with tropical areas, are plagued by illnesses that the wealthier parts of the world (mainly ‘the West’) neither suffer from nor put systematic effort into preventing, treating or curing. What does an ethic with a recognizably African pedigree entail for the ways various agents ought to respond to such neglected diseases? As many readers will know, a characteristically African ethic prescribes weighty duties to aid on the part of those in a position to do so, and it therefore entails that there should have been much more contribution from the Western, ‘developed’ world. However, what else does it prescribe, say, on the part of sub‐Saharan governments and the African Union, and are they in fact doing it? I particularly seek to answer these questions here, by using the 2013‐16 Ebola crisis in West Africa to illustrate what should have happened but what by and large did not.