Recent Submissions

  • Journal Article

    Lactation and menstruation shift the vaginal microbiota in captive rhesus monkeys to be more similar to the male urethral microbiota 

    Hallmaier-Wacker, L. K.; Lüert, S.; Roos, C.; Knauf, S.
    Scientific Reports 2019; 9(1)
    The vaginal microbiota of nonhuman primates differs substantially from humans in terms of Lactobacillus abundance, overall taxonomic diversity, and vaginal pH. Given these differences, it remains unclear in what way the nonhuman primate genital microbiota protects against pathogens, in particular sexually transmitted infections. Considering the effect that microbiota variations can have on disease acquisition and outcome, we examined endogenous and exogenous factors that influence the urogenital microbiota of male and female captive rhesus monkeys. The male urethral (n = 37) and vaginal (n = 194) microbiota of 11 breeding groups were examined in a cross-sectional study. During lactation and menstruation, the vaginal microbiota becomes significantly more diverse and more similar to the microbes observed in the male urethra. Group association and cage-mate (sexual partners) relationships were additionally associated with significant differences in the urogenital microbiota. Our results demonstrate that microbiota considerations are necessary in order to make informed selection of nonhuman primates as translational animal models.
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  • Journal Article

    Temporal stability of fMRI in medetomidine-anesthetized rats 

    Sirmpilatze, Nikoloz; Baudewig, Jürgen; Boretius, Susann
    Scientific Reports 2019; 9(1)
    Medetomidine has become a popular choice for anesthetizing rats during long-lasting sessions of blood-oxygen-level dependent (BOLD) functional magnetic resonance imaging (fMRI). Despite this, it has not yet been thoroughly established how commonly reported fMRI readouts evolve over several hours of medetomidine anesthesia and how they are affected by the precise timing, dose, and route of administration. We used four different protocols of medetomidine administration to anesthetize rats for up to six hours and repeatedly evaluated somatosensory stimulus-evoked BOLD responses and resting state functional connectivity. We found that the temporal evolution of fMRI readouts strongly depended on the method of administration. Intravenous administration of a medetomidine bolus (0.05 mg/kg), combined with a subsequent continuous infusion (0.1 mg/kg/h), led to temporally stable measures of stimulus-evoked activity and functional connectivity throughout the anesthesia. Deviating from the above protocol-by omitting the bolus, lowering the medetomidine dose, or using the subcutaneous route-compromised the stability of these measures in the initial two-hour period. We conclude that both an appropriate protocol of medetomidine administration and a suitable timing of fMRI experiments are crucial for obtaining consistent results. These factors should be considered for the design and interpretation of future rat fMRI studies.
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  • Journal Article

    An Exploration of the Relationships Among Facial Dimensions, Age, Sex, Dominance Status, and Personality in Rhesus Macaques (Macaca mulatta) 

    Altschul, D. M.; Robinson, L. M.; Coleman, K.; Capitanio, J. P.; Wilson, V. A. D.
    International Journal of Primatology 2019; 40(4-5) p.532-552
    Aspects of personality in nonhuman primates have been linked to health, social relationships, and life history outcomes. In humans as well as nonhuman primates, facial morphology is associated with assertiveness, aggression, and measures of dominance status. In this study we aimed to examine the relationship among facial morphology, age, sex, dominance status, and ratings on the personality dimensions Confidence, Openness, Assertiveness, Friendliness, Activity, and Anxiety in rhesus macaques (Macaca mulatta). We measured facial width-to-height ratio (fWHR) and lower-height/full-height ratio (fLHFH) using photographs from 109 captive rhesus macaques, which observers also assessed for dominance status and personality, and explored the associations among facial morphology, age, sex, dominance status, and personality. fWHR and fLHFH personality associations depended on age category: Assertiveness was associated with higher fWHR and fLHFH, and Confidence was associated with lower fWHR and fLHFH, but all these associations were consistent only in individuals <8 yr. of age. We found fWHR and fLHFH to not be consistently associated with sex or dominance status; compared to younger individuals, we found few associations with fWHR and fLHFH for individuals older than 8 yr., which may be due to limited sample size. Our results indicate that in macaques <8 yr. old, facial morphology is associated with the Assertiveness and Confidence personality dimensions, which is consistent with results suggesting a relationship between fWHR and trait aggression in humans and assertiveness in brown capuchins, all of which implies that fWHR might be a cue to assertive and aggressive traits.
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  • Journal Article

    Comparing mitogenomic timetrees for two African savannah primate genera (Chlorocebus and Papio) 

    Dolotovskaya, Sofya; Torroba Bordallo, Juan; Haus, Tanja; Noll, Angela; Hofreiter, Michael; Zinner, Dietmar; Roos, Christian
    Zoological Journal of the Linnean Society(181) p.471-483
    Complete mitochondrial (mtDNA) genomes have proved to be useful in reconstructing primate phylogenies with higher resolution and confidence compared to reconstructions based on partial mtDNA sequences. Here, we analyse complete mtDNA genomes of African green monkeys (genus Chlorocebus), a widely distributed primate genus in Africa representing an interesting phylogeographical model for the evolution of savannah species. Previous studies on partial mtDNA sequences revealed nine major clades, suggesting several cases of para- and polyphyly among Chlorocebus species. However, in these studies, phylogenetic relationships among several clades were not resolved, and divergence times were not estimated. We analysed complete mtDNA genomes for ten Chlorocebus samples representing major mtDNA clades to find stronger statistical support in the phylogenetic reconstruction than in the previous studies and to estimate divergence times. Our results confirmed para- and polyphyletic relationships of most Chlorocebus species, while the support for the phylogenetic relationships between the mtDNA clades increased compared to the previous studies. Our results indicate an initial west–east division in the northern part of the Chlorocebus range with subsequent divergence into north-eastern and southern clades. This phylogeographic scenario contrasts with that for another widespread African savannah primate genus, the baboons (Papio), for which a dispersal from southern Africa into East and West Africa was suggested.
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  • Journal Article

    Trunk rotation and handedness modulate cortical activation in neglect-associated regions during temporal order judgments 

    Paschke, Kerstin; Bähr, Mathias; Wüstenberg, Torsten; Wilke, Melanie
    NeuroImage: Clinical 2019; 23: Art. 101898
    The rotation of the trunk around its vertical midline could be shown to bias visuospatial temporal judgments towards targets in the hemifield ipsilateral to the trunk orientation and to improve visuospatial performance in patients with visual neglect. However, the underlying brain mechanisms are not well understood. Therefore, the goal of the present study was to investigate the neural effects associated with egocentric midplane shifts under consideration of individual handedness. We employed a visuospatial temporal order judgment (TOJ) task in healthy right- and left-handed subjects while their trunk rotation was varied. Participants responded by a saccade towards the stimulus perceived first out of two stimuli presented with different stimulus onset asynchronies (SOA). Apart from gaze behavior, BOLD-fMRI responses were measured using functional magnetic resonance imaging (fMRI). Based on findings from spatial neglect research, analyses of fMRI-BOLD responses were focused on a bilateral fronto-temporo-parietal network comprising Brodmann areas 22, 39, 40, and 44, as well as the basal ganglia core nuclei (caudate, putamen, pallidum). We observed an acceleration of saccadic speed towards stimuli ipsilateral to the trunk orientation modulated by individual handedness. Left-handed participants showed the strongest behavioral and neural effects, suggesting greater susceptibility to manipulations of trunk orientation. With respect to the dominant hand, a rotation around the vertical trunk midline modulated the activation of an ipsilateral network comprising fronto-temporo-parietal regions and the putamen with the strongest effects for saccades towards the hemifield opposite to the dominant hand. Within the investigated network, the temporo-parietal junction (TPJ) appears to serve as a region integrating sensory, motor, and trunk position information. Our results are discussed in the context of gain modulatory and laterality effects.
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  • Journal Article

    Analysis of IFITM-IFITM Interactions by a Flow Cytometry-Based FRET Assay 

    Winkler, Michael; Wrensch, Florian; Bosch, Pascale; Knoth, Maike; Schindler, Michael; Gärtner, Sabine; Pöhlmann, Stefan
    International Journal of Molecular Sciences 2019; 20(16): Art. 3859
    The interferon-induced transmembrane proteins 1-3 (IFITM1-3) inhibit host cell entry of several viruses. However, it is incompletely understood how IFITM1-3 exert antiviral activity. Two phenylalanine residues, F75 and F78, within the intramembrane domain 1 (IM1) were previously shown to be required for IFITM3/IFITM3 interactions and for inhibition of viral entry, suggesting that IFITM/IFITM interactions might be pivotal to antiviral activity. Here, we employed a fluorescence resonance energy transfer (FRET) assay to analyze IFITM/IFITM interactions. For assay calibration, we equipped two cytosolic, non-interacting proteins, super yellow fluorescent protein (SYFP) and super cyan fluorescent protein (SCFP), with signals that target proteins to membrane rafts and also analyzed a SCFP-SYFP fusion protein. This strategy allowed us to discriminate background signals resulting from colocalization of proteins at membrane subdomains from signals elicited by protein-protein interactions. Coexpression of IFITM1-3 and IFITM5 fused to fluorescent proteins elicited strong FRET signals, and mutation of F75 and F78 in IFITM3 (mutant IFITM3-FF) abrogated antiviral activity, as expected, but did not alter cellular localization and FRET signals. Moreover, IFITM3-FF co-immunoprecipitated efficiently with wild type (wt) IFITM3, lending further support to the finding that lack of antiviral activity of IFITM3-FF was not due to altered membrane targeting or abrogated IFITM3-IFITM3 interactions. Collectively, we report an assay that allows quantifying IFITM/IFITM interactions. Moreover, we confirm residues F75 and F78 as critical for antiviral activity but also show that these residues are dispensable for IFITM3 membrane localization and IFITM3/IFITM3 interactions.
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  • Journal Article

    A Metataxonomic Tool to Investigate the Diversity of Treponema 

    Hallmaier-Wacker, Luisa K.; Lüert, Simone; Gronow, Sabine; Spröer, Cathrin; Overmann, Jörg; Buller, Nicky; Vaughan-Higgins, Rebecca J.; Knauf, Sascha
    Frontiers in Microbiology 2019; 10: Art. 2094
    The genus Treponema contains a number of human and animal pathogenic as well as symbiotic bacteria that are found in vastly different anatomical and environmental habitats. Our understanding of the species range, evolution, and biology of these important bacteria is still limited. To explore the diversity of treponemes, we established, validated, and tested a novel metataxonomic approach. As the informative nature of the hypervariable regions of the 16S rRNA gene differ, we first analyzed each variable region independently. Considering the in silico results obtained, we established and validated the sequencing of the V4-region of the 16S rRNA gene using known mixtures of Treponema species as well as a selected number of clinical samples. The metataxonomic approach was able to identify Treponema to a near-species level. We demonstrate that using a spirochete-specific enrichment, our method is applicable to complex microbial communities and large variety of biological samples. The metataxonomic approach described provides a useful method to unravel the full diversity and range of Treponema in various ecosystems.
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  • Journal Article

    6-Sulfo LacNAc (Slan) as a Marker for Non-classical Monocytes 

    Hofer, Thomas P.; van de Loosdrecht, Arjan A.; Stahl-Hennig, Christiane; Cassatella, Marco A.; Ziegler-Heitbrock, Loems
    Frontiers in Immunology 2019; 10: Art. 2052
    Monocytes are subdivided into three subsets, which have different phenotypic and functional characteristics and different roles in inflammation and malignancy. When in man CD14 and CD16 monoclonal antibodies are used to define these subsets, then the distinction of non-classical CD14low and intermediate CD14high monocytes requires setting a gate in what is a gradually changing level of CD14 expression. In the search for an additional marker to better dissect the two subsets we have explored the marker 6-sulfo LacNAc (slan). Slan is a carbohydrate residue originally described to be expressed on the cell surface of a type of dendritic cell in human blood. We elaborate herein that the features of slan+ cells are congruent with the features of CD16+ non-classical monocytes and that slan is a candidate marker for definition of non-classical monocytes. The use of this marker may help in studying the role of non-classical monocytes in health and in diagnosis and monitoring of disease.
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  • Journal Article

    Fluctuating asymmetry and feather growth bars as biomarkers to assess the habitat quality of shade coffee farming for avian diversity conservation 

    Gebremichael, Gelaye; Tsegaye, Diress; Bunnefeld, Nils; Zinner, Dietmar; Atickem, Anagaw
    Royal Society Open Science 2019; 6(8): Art. 190013
    Shade coffee farming has been promoted as a means of combining sustainable coffee production and biodiversity conservation. Supporting this idea, similar levels of diversity and abundance of birds have been found in shade coffee and natural forests. However, diversity and abundance are not always good indicators of habitat quality because there may be a lag before population effects are observed following habitat conversion. Therefore, other indicators of habitat quality should be tested. In this paper, we investigate the use of two biomarkers: fluctuating asymmetry (FA) of tarsus length and rectrix mass, and feather growth bars (average growth bar width) to characterize the habitat quality of shade coffee and natural forests. We predicted higher FA and narrower feather growth bars in shade coffee forest versus natural forest, indicating higher quality in the latter. We measured and compared FA in tarsus length and rectrix mass and average growth bar width in more than 200 individuals of five bird species. The extent of FA in both tarsus length and rectrix mass was not different between the two forest types in any of the five species. Similarly, we found no difference in feather growth between shade coffee and natural forests for any species. Therefore, we conclude our comparison of biomarkers suggests that shade coffee farms and natural forests provide similar habitat quality for the five species we examined.
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  • Journal Article

    Aberrant functional connectivity of resting state networks related to misperceptions and intra-individual variability in Parkinson‘s disease 

    Miloserdov, Kristina; Schmidt-Samoa, Carsten; Williams, Kathleen; Weinrich, Christiane Anne; Kagan, Igor; Bürk, Katrin; Trenkwalder, Claudia; Bähr, Mathias; Wilke, Melanie
    NeuroImage: Clinical: Art. 102076
    Patients with Parkinson's disease (PD) frequently suffer from visual misperceptions and hallucinations, which are difficult to objectify and quantify. We aimed to develop an image recognition task to objectify misperceptions and to assess performance fluctuations in PD patients with and without self-reported hallucinations. Thirty-two non-demented patients with Parkinson's disease (16 with and 16 without self-reported visual hallucinations) and 25 age-matched healthy controls (HC) were tested. Participants performed a dynamic image recognition task with real and scrambled images. We assessed misperception scores and intra-individual variability in recognition times. To gain insight into possible neural mechanisms related to misperceptions and performance fluctuations we correlated resting state network connectivity to the behavioral outcomes in a subsample of Parkinson's disease patients (N = 16). We found that PD patients with self-reported hallucinations (PD-VH) exhibited higher perceptual error rates, due to decreased perceptual sensitivity and not due to changed decision criteria. In addition, PD-VH patients exhibited higher intra-individual variability in recognition times than HC or PD-nonVH patients. Both, misperceptions and intra-individual variability were negatively correlated with resting state functional connectivity involving frontal and parietal brain regions, albeit in partly different subregions. Consistent with previous research suggesting that hallucinations arise from dysfunction in attentional networks, misperception scores correlated with reduced functional connectivity between the dorsal attention and salience network. Intra-individual variability correlated with decreased connectivity between somatomotor and right fronto-parietal networks. We conclude that our task can detect visual misperceptions that are more prevalent in PD-VH patients. In addition, fluctuating visual performance appear to be a signature of PD-VH patients, which might assist further studies of the underlying pathophysiological mechanisms and cognitive processes.
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  • Journal Article

    Dynamic Quantitative Iodine Myocardial Perfusion Imaging with Dual-Layer CT using a Porcine Model 

    Scherer, Kai; Hammel, Johannes; Sellerer, Thorsten; Mechlem, Korbinian; Renger, Bernhard; Bähr, Andrea; Kupatt, Christian; Hinkel, Rabea; Herzen, Julia; Pfeiffer, Franz; et al.
    Rummeny, ErnstPfeiffer, Daniela
    Scientific Reports 2019; 9(1)
    Ischemic heart disease is the globally leading cause of death. When using coronary CT angiography, the functional hemodynamics within the myocardium remain uncertain. In this study myocardial CT perfusion imaging using iodine contrast agent demonstrated to strongly improve the assessment of myocardial disorders. However, a retrieval of such dynamics using Hounsfield units from conventional CT poses concerns with respect to beam-hardening effects and low contrast-to-noise ratio (CNR). Dual-energy CT offers novel approaches to overcome aforementioned limitations. Quantitative peak enhancement, perfusion, time to peak and iodine volume measurements inside the myocardium were determined resulting in 0.92 mg/ml, 0.085 mg/ml/s 17.12 s and 29.89 mg/ml*s, respectively. We report on the first extensive quantitative and iodine-based analysis of myocardial dynamics in a healthy porcine model using a dual-layer spectral CT. We further elucidate on the potential of reducing the radiation dose from 135 to 18 mGy and the contrast agent volume from 60 to 30 mL by presenting a two-shot acquisition approach and measuring iodine concentrations in the myocardium in-vivo down to 1 mg/ml, respectively. We believe that dynamic quantitative iodine perfusion imaging may
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  • Journal Article

    Comparing Open-Source Toolboxes for Processing and Analysis of Spike and Local Field Potentials Data 

    Unakafova, Valentina A.; Gail, Alexander
    Frontiers in Neuroinformatics 2019; 13: Art. 57
    Analysis of spike and local field potential (LFP) data is an essential part of neuroscientific research. Today there exist many open-source toolboxes for spike and LFP data analysis implementing various functionality. Here we aim to provide a practical guidance for neuroscientists in the choice of an open-source toolbox best satisfying their needs. We overview major open-source toolboxes for spike and LFP data analysis as well as toolboxes with tools for connectivity analysis, dimensionality reduction and generalized linear modeling. We focus on comparing toolboxes functionality, statistical and visualization tools, documentation and support quality. To give a better insight, we compare and illustrate functionality of the toolboxes on open-access dataset or simulated data and make corresponding MATLAB scripts publicly available.
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  • Journal Article

    Local field potentials are induced by visually evoked spiking activity in macaque cortical area MT 

    Esghaei, Moein; Daliri, Mohammad Reza; Treue, Stefan
    Scientific Reports 2017; 7(1)
    Local field potentials (LFP) have been the focus of many recent studies in systems neuroscience. However, the exact neural basis of these signals remains unclear. To address this question, we determined the relationship between LFP signals and another, much better understood, signature of neural activity: action potentials. Specifically, we focused on the relationship between the amplitude of stimulus-induced LFPs and the magnitude of spiking activity in visual cortex of non-human primates. Our trial-by-trial correlation analyses between these two components of extracellular signals in macaque visual cortex show that the spike rate is coupled to the LFP amplitude with a surprisingly long latency, typically 50 ms. Our analysis shows that the neural spike rate is a significant predictor of the LFP amplitude. This limits the functional interpretation of LFP signals beyond that based on spiking activities.
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  • Journal Article

    Dissecting Multivalent Lectin–Carbohydrate Recognition Using Polyvalent Multifunctional Glycan-Quantum Dots 

    Guo, Yuan; Nehlmeier, Inga; Poole, Emma; Sakonsinsiri, Chadamas; Hondow, Nicole; Brown, Andy; Li, Qing; Li, Shuang; Whitworth, Jessie; Li, Zhongjun; et al.
    Yu, AnchiBrydson, RikTurnbull, W. BrucePöhlmann, StefanZhou, Dejian
    Journal of the American Chemical Society 2017; 139(34) p.11833-11844
    Multivalent protein-carbohydrate interactions initiate the first contacts between virus/bacteria and target cells, which ultimately lead to infection. Understanding the structures and binding modes involved is vital to the design of specific, potent multivalent inhibitors. However, the lack of structural information on such flexible, complex, and multimeric cell surface membrane proteins has often hampered such endeavors. Herein, we report that quantum dots (QDs) displayed with a dense array of mono-/disaccharides are powerful probes for multivalent protein-glycan interactions. Using a pair of closely related tetrameric lectins, DC-SIGN and DC-SIGNR, which bind to the HIV and Ebola virus glycoproteins (EBOV-GP) to augment viral entry and infect target cells, we show that such QDs efficiently dissect the different DC-SIGN/R-glycan binding modes (tetra-/di-/monovalent) through a combination of multimodal readouts: Förster resonance energy transfer (FRET), hydrodynamic size measurement, and transmission electron microscopy imaging. We also report a new QD-FRET method for quantifying QD-DC-SIGN/R binding affinity, revealing that DC-SIGN binds to the QD >100-fold tighter than does DC-SIGNR. This result is consistent with DC-SIGN's higher trans-infection efficiency of some HIV strains over DC-SIGNR. Finally, we show that the QDs potently inhibit DC-SIGN-mediated enhancement of EBOV-GP-driven transduction of target cells with IC50 values down to 0.7 nM, matching well to their DC-SIGN binding constant (apparent Kd = 0.6 nM) measured by FRET. These results suggest that the glycan-QDs are powerful multifunctional probes for dissecting multivalent protein-ligand recognition and predicting glyconanoparticle inhibition of virus infection at the cellular level.
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  • Journal Article

    Experimental evidence for heterospecific alarm signal recognition via associative learning in wild capuchin monkeys 

    Wheeler, Brandon C.; Fahy, Martin; Tiddi, Barbara
    Animal Cognition 2019; 22(5) p.687-695
    Many vertebrate taxa respond to heterospecific alarm calls with anti-predator behaviours. While it is unclear how apparent recognition is achieved, learned associations between the occurrence of the call and the presence of a predator are considered the most likely explanation. Conclusive evidence that this behaviour is indeed underpinned by learning, however, is scarce. This study tested whether wild black capuchin monkeys (Sapajus nigritus) learn to associate novel sounds with predators through a two-phase field experiment. During an initial training phase, three study groups were each presented with a playback of one of the three novel sounds together with a simulated felid predator on four occasions over an 8- to 12-week period. This was followed by a test phase, wherein each of the three sounds was played back to individuals in all three groups, allowing each sound to serve as both a test stimulus for individuals trained with that sound, and a control stimulus for individuals trained with another sound. Antipredator responses were significantly stronger in response to test sounds than to controls. Limited observations suggest that antipredator responses persisted for at least 2 years without reinforcement of the predator-sound link. Additionally, responses to noisier sounds were typically stronger than were those to more tonal sounds, although the effect of sound type cannot be disentangled from potential effects of group. This study provides the strongest evidence to date that learning affects the responses of primates to sounds such as heterospecific alarm calls, and supports the contention that signals provide receivers with information.
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  • Journal Article

    Foraging ecology of African wolves (Canis lupaster) and its implications for the conservation of Ethiopian wolves (Canis simensis) 

    Gutema, Tariku Mekonnen; Atickem, Anagaw; Tsegaye, Diress; Bekele, Afework; Sillero-Zubiri, Claudio; Marino, Jorgelina; Kasso, Mohammed; Venkataraman, Vivek V.; Fashing, Peter J.; Stenseth, Nils C.
    Royal Society Open Science 2019; 6(9)
    African wolves (AWs) are sympatric with endangered Ethiopian wolves (EWs) in parts of their range. Scat analyses have suggested a dietary overlap between AWs and EWs, raising the potential for exploitative competition, and a possible conservation threat to EWs. However, in contrast to that of the well-studied EW, the foraging ecology of AWs remains poorly characterized. Accordingly, we studied the foraging ecology of radio-collared AWs (n = 11 individuals) at two localities with varying levels of anthropogenic disturbance in the Ethiopian Highlands, the Guassa-Menz Community Conservation Area (GMCCA) and Borena-Saynt National Park (BSNP), accumulating 845 h of focal observation across 2952 feeding events. We also monitored rodent abundance and rodent trapping activity by local farmers who experience conflict with AWs. The AW diet consisted largely of rodents (22.0%), insects (24.8%), and goats and sheep (24.3%). Of the total rodents captured by farmers using local traps during peak barley production (July to November) in GMCCA, averaging 24.7 ± 8.5 rodents/hectare/day, 81% (N = 3009) were scavenged by AWs. Further, of all the rodents consumed by AWs, most (74%) were carcasses. These results reveal complex interactions between AWs and local farmers, and highlight the scavenging niche occupied by AWs in anthropogenically altered landscapes in contrast to the active hunting exhibited by EWs in more intact habitats. While AWs cause economic damage to local farmers through livestock predation, they appear to play an important role in scavenging pest rodents among farmlands, a pattern of behaviour which likely mitigates direct and indirect competition with EWs. We suggest two routes to promote the coexistence of AWs and EWs in the Ethiopian highlands: local education efforts highlighting the complex role AWs play in highland ecosystems to reduce their persecution, and enforced protection of intact habitats to preserve habitat preferred by EWs.
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  • Journal Article

    Complementary encoding of priors in monkey frontoparietal network supports a dual process of decision-making 

    Suriya-Arunroj, Lalitta; Gail, Alexander
    eLife 2019; 8: Art. e47581
    Prior expectations of movement instructions can promote preliminary action planning and influence choices. We investigated how action priors affect action-goal encoding in premotor and parietal cortices and if they bias subsequent free choice. Monkeys planned reaches according to visual cues that indicated relative probabilities of two possible goals. On instructed trials, the reach goal was determined by a secondary cue respecting these probabilities. On rarely interspersed free-choice trials without instruction, both goals offered equal reward. Action priors induced graded free-choice biases and graded frontoparietal motor-goal activity, complementarily in two subclasses of neurons. Down-regulating neurons co-encoded both possible goals and decreased opposite-to-preferred responses with decreasing prior, possibly supporting a process of choice by elimination. Up-regulating neurons showed increased preferred-direction responses with increasing prior, likely supporting a process of computing net likelihood. Action-selection signals emerged earliest in down-regulating neurons of premotor cortex, arguing for an initiation of selection in the frontal lobe.
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  • Journal Article

    Establishing an infrastructure for collaboration in primate cognition research 

    Altschul, Drew M.; Beran, Michael J.; Bohn, Manuel; Call, Josep; DeTroy, Sarah; Duguid, Shona J.; Egelkamp, Crystal L.; Fichtel, Claudia; Fischer, Julia; Flessert, Molly; et al.
    Hanus, DanielHaun, Daniel B. M.Haux, Lou M.Hernandez-Aguilar, R. AdrianaHerrmann, EstherHopper, Lydia M.Joly, MarineKano, FumihiroKeupp, StefanieMelis, Alicia P.Motes Rodrigo, AlbaRoss, Stephen R.Sánchez-Amaro, AlejandroSato, YutaroSchmitt, VanessaSchweinfurth, Manon K.Seed, Amanda M.Taylor, DerryVölter, Christoph J.Warren, ElizabethWatzek, Julia
    PLOS ONE 2019; 14(10): Art. e0223675
    Inferring the evolutionary history of cognitive abilities requires large and diverse samples. However, such samples are often beyond the reach of individual researchers or institutions, and studies are often limited to small numbers of species. Consequently, methodological and site-specific-differences across studies can limit comparisons between species. Here we introduce the ManyPrimates project, which addresses these challenges by providing a large-scale collaborative framework for comparative studies in primate cognition. To demonstrate the viability of the project we conducted a case study of short-term memory. In this initial study, we were able to include 176 individuals from 12 primate species housed at 11 sites across Africa, Asia, North America and Europe. All subjects were tested in a delayed-response task using consistent methodology across sites. Individuals could access food rewards by remembering the position of the hidden reward after a 0, 15, or 30-second delay. Overall, individuals performed better with shorter delays, as predicted by previous studies. Phylogenetic analysis revealed a strong phylogenetic signal for short-term memory. Although, with only 12 species, the validity of this analysis is limited, our initial results demonstrate the feasibility of a large, collaborative open-science project. We present the ManyPrimates project as an exciting opportunity to address open questions in primate cognition and behaviour with large, diverse datasets.
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  • Journal Article

    Role of rhesus macaque IFITM3(2) in simian immunodeficiency virus infection of macaques 

    Winkler, Michael; Gärtner, Sabine; Markus, Lara; Hoffmann, Markus; Nehlmeier, Inga; Krawczak, Michael; Sauermann, Ulrike; Pöhlmann, Stefan
    PLOS ONE 2019; 14(11): Art. e0224082
    The experimental infection of rhesus macaques (rh) with simian immunodeficiency virus (SIV) is an important model for human immunodeficiency virus (HIV) infection of humans. The interferon-induced transmembrane protein 3 (IFITM3) inhibits HIV and SIV infection at the stage of host cell entry. However, it is still unclear to what extent the antiviral activity of IFITM3 observed in cell culture translates into inhibition of HIV/SIV spread in the infected host. We have shown previously that although rhIFITM3 inhibits SIV entry into cultured cells, polymorphisms in the rhIFITM3 gene are not strongly associated with viral load or disease progression in SIV infected macaques. Here, we examined whether rhIFITM3(2), which is closely related to rhIFITM3 at the sequence level, exerts antiviral activity and whether polymorphisms in the rhIFITM3(2) gene impact the course of SIV infection. We show that expression of rhIFITM3(2) is interferon-inducible and inhibits SIV entry into cells, although with reduced efficiency as compared to rhIFITM3. We further report the identification of 19 polymorphisms in the rhIFITM3(2) gene. However, analysis of a well characterized cohort of SIV infected macaques revealed that none of the polymorphisms had a significant impact upon the course of SIV infection. These results and our previous work suggest that polymorphisms in the rhIFITM3 and rhIFITM3(2) genes do not strongly modulate the course of SIV infection in macaques.
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  • Journal Article

    Estimating seed dispersal distance: A comparison of methods using animal movement and plant genetic data on two primate‐dispersed Neotropical plant species 

    Gelmi‐Candusso, Tiziana A.; Bialozyt, Ronald; Slana, Darja; Zárate Gómez, Ricardo; Heymann, Eckhard W.; Heer, Katrin
    Ecology and Evolution 2019; 9(16) p.8965-8977
    Seed dispersal distance (SDD) critically influences the survival of seedlings, spatial patterns of genetic diversity within plant populations, and gene flow among plant populations. In animal-dispersed species, foraging behavior and movement patterns determine SDD. Direct observations of seed dispersal events by animals in natural plant populations are mostly constrained by the high mobility and low visibility of seed dispersers. Therefore, diverse alternative methods are used to estimate seed dispersal distance, but direct comparisons of these approaches within the same seed dispersal system are mostly missing.We investigated two plant species with different life history traits, Leonia cymosa and Parkia panurensis, exclusively dispersed by two tamarin species, Saguinus mystax and Leontocebus nigrifrons. We compared SDD estimates obtained from direct observations, genetic identification of mother plants from seed coats, parentage analysis of seedlings/saplings, and phenomenological and mechanistic modeling approaches.SDD derived from the different methods ranged between 158 and 201 m for P. panurensis and between 178 and 318 m for L. cymosa. In P. panurensis, the modeling approaches resulted in moderately higher estimates than observations and genotyping of seed coats. In L. cymosa, parentage analysis resulted in a lower estimate than all other methods. Overall, SDD estimates for P. panurensis (179 ± 16 m; mean ± SD) were significantly lower than for L. cymosa (266 ± 59 m; mean ± SD).Differences among methods were related to processes of the seed dispersal loop integrated by the respective methods (e.g., seed deposition or seedling distribution). We discuss the merits and limitations of each method and highlight the aspects to be considered when comparing SDD derived from different methodologies. Differences among plant species were related to differences in reproductive traits influencing gut passage time and feeding behavior, highlighting the importance of plant traits on animal-mediated seed dispersal distance.
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