Spot the odd one out: do snake pictures capture macaques' attention more than other predators?

Detecting and identifying predators quickly is key to survival. According to the Snake Detection Theory (SDT), snakes have been a substantive threat to primates for millions of years, so that dedicated visual skills were tuned to detect snakes in early primates. Past experiments confronted the SDT by measuring how fast primate subjects detected snake pictures among non-dangerous distractors (e.g., flowers), but did not include pictures of primates' other predators, such as carnivorans, raptors, and crocodilians. Here, we examined the detection abilities of N = 19 Tonkean macaques (Macaca tonkeana) and N = 6 rhesus macaques (Macaca mulatta) to spot different predators. By implementing an oddity task protocol, we recorded success rates and reaction times to locate a deviant picture among four pictures over more than 400,000 test trials. Pictures depicted a predator, a non-predator animal, or a simple geometric shape. The first task consisted of detecting a deviant picture among identical distractor pictures (discrimination) and the second task was designed to evaluate detection abilities of a deviant picture among different distractor pictures (categorization). The macaques detected pictures of geometric shapes better and faster than pictures of animals, and were better and faster at discriminating than categorizing. The macaques did not detect snakes better or faster than other animal categories. Overall, these results suggest that pictures of snakes do not capture visual attention more than other predators, questioning previous findings in favor of the SDT.

Chemical cues of identity and reproductive status in Japanese macaques.

Olfactory communication plays an important role in the regulation of socio-sexual interactions in mammals. There is growing evidence that both human and nonhuman primates rely on odors to inform their mating decisions. Nevertheless, studies of primate chemical ecology remain scarce due to the difficulty of obtaining and analyzing samples. We analyzed 67 urine samples from five captive female Japanese macaques (Macaca fuscata) and 30 vaginal swabs from three of these females using gas chromatography-mass spectrometry and examined the relationship between odor (compounds identified, richness, intensity, and diversity) and female identity as well as cycle phase. We found a total of 36 urine compounds of which we identified 31, and 68 vaginal compounds of which we identified 37. Our results suggest that urine and vaginal odor varied more between individuals than within cycle phases. However, we found that within a female cycle, urine samples from similar phases may cluster more than samples from different phases. Our results suggest that female odor may encode information about identity (vaginal and urine odor) and reproductive status (urine odor). The question of how conspecifics use female urine and vaginal odor remains open and could be tested using bioassays. Our results and their interpretation are constrained by our limited sample size and our study design. Nonetheless, our study provides insight into the potential signaling role of female odor in sexual communication in Japanese macaques and contributes to our understanding of how odors may influence mating strategies in primates.

Effect of Popcorn (Zea mays var. everta) Popping Mode (Microwave, Hot Oil, and Hot Air) on Fumonisins and Deoxynivalenol Contamination Levels.

Mycotoxins are secondary metabolites that are produced by molds during their development. According to fungal physiological particularities, mycotoxins can contaminate crops before harvest or during storage. Among toxins that represent a real public health issue, those produced by Fusarium genus in cereals before harvest are of great importance since they are the most frequent in European productions. Among them, deoxynivalenol (DON) and fumonisins (FUM) frequently contaminate maize. In recent years, numerous studies have investigated whether food processing techniques can be exploited to reduce the levels of these two mycotoxins, which would allow the identification and quantification of parameters affecting mycotoxin stability. The particularity of the popcorn process is that it associates heat treatment with a particular physical phenomenon (i.e., expansion). Three methods exist to implement the popcorn transformation process: hot air, hot oil, and microwaves, all of which are tested in this study. The results show that all popping modes significantly reduce FUM contents in both Mushroom and Butterfly types of popcorn. The mean initial contamination of 1351 µg/kg was reduced by 91% on average after popping. For DON, the reduction was less important despite a lower initial contamination than for FUM (560 µg/kg). Only the hot oil popping for the Mushroom type significantly reduced the contamination up to 78% compared to unpopped controls. Hot oil popping appears to provide the most important reduction for the two considered mycotoxins for both types of popcorn (-98% and -58% average reduction for FUM and DON, respectively).

The energy allocation trade-offs underlying life history traits in hypometabolic strepsirhines and other primates.

Life history, brain size and energy expenditure scale with body mass in mammals but there is little conclusive evidence for a correlated evolution between life history and energy expenditure (either basal/resting or daily) independent of body mass. We addressed this question by examining the relationship between primate free-living daily energy expenditure (DEE) measured by doubly labeled water method (n = 18 species), life history variables (maximum lifespan, gestation and lactation duration, interbirth interval, litter mass, age at first reproduction), resting metabolic rate (RMR) and brain size. We also analyzed whether the hypometabolic primates of Madagascar (lemurs) make distinct energy allocation tradeoffs compared to other primates (monkeys and apes) with different life history traits and ecological constraints. None of the life-history traits correlated with DEE after controlling for body mass and phylogeny. In contrast, a regression model showed that DEE increased with increasing RMR and decreasing reproductive output (i.e., litter mass/interbirth interval) independent of body mass. Despite their low RMR and smaller brains, lemurs had an average DEE remarkably similar to that of haplorhines. The data suggest that lemurs have evolved energy strategies that maximize energy investment to survive in the unusually harsh and unpredictable environments of Madagascar at the expense of reproduction.

Study of the relationship between red wine colloidal fraction and astringency by asymmetrical flow field-flow fractionation coupled with multi-detection.

Macromolecules including condensed tannins and polysaccharides impact wine taste and especially astringency. Asymmetrical Flow-Field-Flow-Fractionation (AF4) coupled to UV detection (UV), multi-angle light scattering (MALS) and refractive index detection (dRI) has been proposed to separate red wine colloids. The present work aimed at relating AF4-mutidetection profiles with red wine astringency. Fifty commercial red wines characterized by a trained sensory panel were analysed by AF4-UV-MALS-dRI and UV-visible spectroscopy. The analytical data set was built by selecting the three variables most predictive of the astringency score from each table (UV, dRI, MALS, Mw distribution, and UV-visible spectra of whole wine, permeate and retentate A4F fractions) and analysed by principal component analysis. Red wine astringency was more related to variables extracted from the AF4 data than to UV- absorbance of the wine or permeate, confirming the relevance of AF4-multidetection for analysis of the colloidal fraction involved in this perception.

New insights in Cercopithecinae spermatozoa.

Sperm morphometric and morphologic data have been shown to represent useful tools for monitoring fertility, improving assisted reproduction techniques and conservation of genetic material as well as detecting inbreeding of endangered primates. We provide here for the first time sperm morphologic and morphometric data from Cercopithecus neglectus, Cercopithecus cephus, Papio papio and critically endangered Cercopithecus roloway, as well as comparative data from other Cercopithecinae species, i.e. Allochrocebus lhoesti, Mandrillus sphinx and Papio anubis. Following collection from the epididymis, spermatozoa were measured for each species for the following parameters: head length, head width, head perimeter, head area, midpiece length and total flagellum length, and the head volume, ellipticity, elongation, roughness and regularity were then calculated. Our data are consistent with both the general morphology and the morphometric proportions of Cercopithecinae sperm. Some specificities were observed, with C. cephus displaying a narrow head (width = 2.76 ± 0.26 µM) and C. roloway displaying a short midpiece (6.65 ± 0.61 µM). This data set represents an important contribution, especially for Cercopithecus roloway, one of the most endangered monkeys in the world, and further data on additional specimens coupled to data on mating systems and reproductive ecology should allow a better understanding of the mechanisms underlying these morphological differences across primate species.

Balancing costs and benefits in primates: ecological and palaeoanthropological views.

Maintaining the balance between costs and benefits is challenging for species living in complex and dynamic socio-ecological environments, such as primates, but also crucial for shaping life history, reproductive and feeding strategies. Indeed, individuals must decide to invest time and energy to obtain food, services and partners, with little direct feedback on the success of their investments. Whereas decision-making relies heavily upon cognition in humans, the extent to which it also involves cognition in other species, based on their environmental constraints, has remained a challenging question. Building mental representations relating behaviours and their long-term outcome could be critical for other primates, but there are actually very little data relating cognition to real socio-ecological challenges in extant and extinct primates. Here, we review available data illustrating how specific cognitive processes enable(d) modern primates and extinct hominins to manage multiple resources (e.g. food, partners) and to organize their behaviour in space and time, both at the individual and at the group level. We particularly focus on how they overcome fluctuating and competing demands, and select courses of action corresponding to the best possible packages of potential costs and benefits in reproductive and foraging contexts. This article is part of the theme issue 'Existence and prevalence of economic behaviours among non-human primates'.

Prediction and detection of human epileptic seizures based on SIFT-MS chemometric data.

Although epilepsy is considered a public health issue, the burden imposed by the unpredictability of seizures is mainly borne by the patients. Predicting seizures based on electroencephalography has had mixed success, and the idiosyncratic character of epilepsy makes a single method of detection or prediction for all patients almost impossible. To address this problem, we demonstrate herein that epileptic seizures can not only be detected by global chemometric analysis of data from selected ion flow tube mass spectrometry but also that a simple mathematical model makes it possible to predict these seizures (by up to 4 h 37 min in advance with 92% and 75% of samples correctly classified in training and leave-one-out-cross-validation, respectively). These findings should stimulate the development of non-invasive applications (e.g., electronic nose) for different types of epilepsy and thereby decrease of the unpredictability of epileptic seizures.

Sexual selection and sperm diversity in primates.

Many aspects of primate sperm physiology and reproductive behavior have been influenced by sexual selection, especially in taxa exposed to sperm competition where females mate with multiple partners. Primate sperm diversity reflects therefore the evolutionary divergences of the different primate species and the impact of a combination of variables exerting selection pressures on sperm form, function, and competition. Thereby, mating systems, life cycle or ecological variables are some of the important factors driving sperm diversity and explaining variation in terms of sperm morphology, parameters or male sexual characters. Here, we address primate sperm diversity through a compilation of all data available in the literature concerning primate sperm parameters and relationships between them. We also review the factors that can influence primate sperm diversity (e.g. mating systems, trade-off between investments in precopulatory and postcopulatory sexual traits, male and female sexual behaviors, seasonality, social constraints, testosterone levels), and discuss also their relevance to our understanding of human reproduction.

Identification of lactic acid bacteria Enterococcus and Lactococcus by near-infrared spectroscopy and multivariate classification.

Lactic acid bacteria are important in numerous biological processes. The fabrication of cheese, for example, uses the lactic acid bacteria found in raw milk such as Lactococcus lactis as starters to improve the organoleptic properties of milk. Conventional methods to determine the genus and species of lactic acid bacteria isolated from raw milk involve genotyping and phenotyping, which require specific preparation and sample destruction. To improve on this situation, we present herein a simple and non-destructive screening method to discriminate between the Lactococcus and Enterococcus species most commonly found in raw milk (L. lactis, E. durans, E. faecalis, and E. faecium). The bacteria are grown on agar plates and assessed by using near-infrared spectroscopy in a spectral range from 800 to 2777 nm. Principle component analysis loading line plots highlight the inter-genus and inter-species differences at various wavelengths, which are mostly assigned to cell-wall compounds such as polysaccharides. The best artificial neural network identification models give 98.8% and 86.3% classification rates at the genus and species level, respectively, for an external validation set made of 80 samples. These results suggest that near-infrared spectroscopy may be used to identify lactic acid bacteria on agar medium.

Refining the ecological brain: Strong relation between the ventromedial prefrontal cortex and feeding ecology in five primate species.

To survive in complex and seasonal environments, primates are thought to rely upon cognitive capacities such as decision-making and episodic memory, which enable them to plan their daily foraging path. According to the Ecological Brain hypothesis, feeding ecology has driven the expansion of the brain to support the corresponding development of cognitive skills. Recent works in cognitive neurosciences indicate that cognitive operations such as decision-making or subjective evaluation (which are contextual and dependent upon episodic memory), relied critically upon a small part of the frontal lobe, often referred to as the ventromedial prefrontal cortex (VMPFC). Several authors suggested that this area might be important for foraging, but this has never been tested. In the present study, we quantified the relation between the size of the VMPFC (along with other cerebral measures: the whole brain, the gyrus rectus and the somatosensory cortex) and key socio-ecological variables in five primate species (Macaca mulatta, Macaca fuscata, Gorilla gorilla, Pan troglodytes and Homo sapiens). We hypothesized that the size of the VMPFC would be greater in primates with a large dietary spectrum and complex foraging strategies. We also hypothesized that the impact of feeding ecology would be stronger on this specific region than on other regions (somatosensory cortex) or on more global cerebral measures (e.g., whole brain). In line with these hypotheses, we found that all cerebral measures were more strongly related to feeding ecology than group size, a proxy for social complexity. As expected, the VMPFC volume is more precisely related to feeding ecology than the whole brain, and appears to be critically related to dietary quality. Thus, combining a comparative approach with predictions coming both from behavioral ecology and cognitive neurosciences, our study provides evidence that feeding ecology played a key role in the development of specific cognitive skills, which rely upon the expansion of a specific cortical area.

Physicochemical characterization and study of molar mass of industrial gelatins by AsFlFFF-UV/MALS and chemometric approach.

Industrial gelatins have different physicochemical properties that mainly depend of the raw materials origin and the extraction conditions. These properties are closely related to the molar mass distribution of these gelatins. Several methods exist to characterize molar mass distribution of polymer, including the Asymmetrical Flow Field Flow Fractionation method. The goal of this study is to analyze the relationship between physicochemical properties and the gelatins molar mass distribution obtained by Asymmetrical Flow Field Flow Fractionation. In this study, 49 gelatins samples extracted from pig skin are characterized in terms of gel strength and viscosity and their molar mass distribution are analyzed by Asymmetrical Flow Field Flow Fractionation coupled to an Ultraviolet and Multi Angle Light Scattering detector. This analytical method is an interesting tool for studying, simultaneously, the primary chains and the high-molar-mass fraction corresponding to the polymer chains. Correlation analysis between molar mass distribution data from the different fractions highlights the importance of high molar mass polymer chains to explain the gel strength and viscosity of gelatins. These results are confirmed by an additional chemometric approach based on the UV absorbance of gelatin fractograms to predict gel strength (r2Cal = 0.85) and viscosity (r2Cal = 0.79).

Updated Overview of Infrared Spectroscopy Methods for Detecting Mycotoxins on Cereals (Corn, Wheat, and Barley).

Each year, mycotoxins cause economic losses of several billion US dollars worldwide. Consequently, methods must be developed, for producers and cereal manufacturers, to detect these toxins and to comply with regulations. Chromatographic reference methods are time consuming and costly. Thus, alternative methods such as infrared spectroscopy are being increasingly developed to provide simple, rapid, and nondestructive methods to detect mycotoxins. This article reviews research conducted over the last eight years into the use of near-infrared and mid-infrared spectroscopy to monitor mycotoxins in corn, wheat, and barley. More specifically, we focus on the Fusarium species and on the main fusariotoxins of deoxynivalenol, zearalenone, and fumonisin B1 and B2. Quantification models are insufficiently precise to satisfy the legal requirements. Sorting models with cutoff levels are the most promising applications.

Testing for links between face color and age, dominance status, parity, weight, and intestinal nematode infection in a sample of female Japanese macaques.

Studies of the role of secondary sexual ornaments in mate choice tend to focus on colorful traits in males, but females of many animal species express colorful ornamentation too. Among non-human primates, investigations into the role of female secondary sexual traits as indicators of life history characteristics, reproductive success, and health status have mostly focused on sexual swellings, whereas only few studies have been conducted on the role of facial color. Recent studies on rhesus macaques and mandrills suggested that female ornamentation might provide information about female life history characteristics, but not on disease resistance factors and parasite infection, which have been shown to affect male ornamentation in some non-primate species. In Japanese macaques (Macaca fuscata), females have brightly colored faces that are indicative of their reproductive status. Here, we aimed to determine whether female facial color might also convey information about age, dominance rank, parity, weight, and intestinal nematode infection in free-ranging individuals. We analyzed whether female facial parameters (luminance and redness) were linked to these individual characteristics, using digital photography and data on intestinal parasite infection collected systematically during 1 month for each of seven free-ranging females. We found no evidence to suggest that female facial color is an indicator of any of these measures in Japanese macaques. Considering our small data set, it is still preliminary to draft any clear conclusions. Future studies combining digital, hormonal, parasitological and behavioral data are needed to assess the possible role of female face color on male preferences and mating choice in Japanese macaques.

An infrared diagnostic system to detect causal agents of grapevine trunk diseases.

In most vineyards worldwide, agents of grapevine trunk diseases represent a real threat for viticulture and are responsible for significant economic loss to the wine industry. The conventional microbiological isolation technique used to diagnose this disease is tedious and frequently leads to false negatives. Thus, a dire need exists for an alternative method to detect this disease. One possible way involves infrared spectroscopy, which is a rapid, nondestructive analytical tool that is commonly used for quality control of feed stuffs. In the present work, a midinfrared spectrometer was tested as a fast tool for detecting agents of grapevine trunk disease. Midinfrared spectra were collected from 70 Vitis vinifera L. cv. Cabernet-Sauvignon one year old trunk-wood samples that were infected naturally in one viticulture nursery of the south of France. The samples underwent polymerase chain reaction and morphological identification, and the results were correlated to the midinfrared spectra by using multivariate analysis to discriminate between noninfected and infected samples. Based on comparison with some control samples, the highest percentage of correct identification of fungal contamination when using the midinfrared spectroscopy method is 80%.

Multimodal Advertisement of Pregnancy in Free-Ranging Female Japanese Macaques (Macaca fuscata).

The role of multiple sexual signals in indicating the timing of female ovulation, and discrimination of this timing by males, has been particularly well studied among primates. However the exhibition of pregnancy signals, and how such signals might modulate male post-conception mating decisions, is still poorly understood. Here we aimed to determine if Japanese macaque males use changes in female sexual signals (behavioral, visual and auditory) to discriminate pregnancy and adjust their socio-sexual behaviors. We combined behavioral observations, digital photography and endocrinological (progestogen and estrogen) data, collected systematically during three one-month periods: the pre-conceptive period, the 1st month of pregnancy and the 2nd month of pregnancy. We analyzed variation in the probability of detecting male and female socio-sexual behaviors and estrus calls, as well as changes in female face color parameters, in relation to female reproductive state. Based on our focal observations, we found that males did not copulate during the pregnancy period, and that female socio-sexual behaviors generally decreased from the pre-conceptive to post-conceptive periods. Female face luminance decreased from the pre-conceptive month to the pregnancy period whereas face color only varied between the 1st and 2nd month of gestation. Our results suggest that Japanese macaque females display sexual cues of pregnancy that males might use to reduce energy wasted on non-reproductive copulations with pregnant females. We hypothesize that females advertize their pregnancy through changes in behavioral, visual and potential auditory signals that males can use to adjust their mating behaviors. We finish by discussing implications for male and female post-conception strategies.

Environmental, biological, and social factors influencing fecal adrenal steroid concentrations in female Japanese macaques (Macaca fuscata).

The ability to determine hormonal profiles of primate populations using non-invasive techniques can help to monitor physical fitness, stress, and physiological responses to environmental changes. We investigated fecal glucocorticoids (fGC) and DHEAS concentrations in captive Japanese macaques (Macaca fuscata) in relation to environmental, biological, and social factors. The subjects were female Japanese monkeys from 4 months to 31 years old housed in captivity (27 in social groups and 12 in single cages). Fecal samples were collected from all females, and behavioral data from the social groups during the mating season and the following birth season. Hormonal concentrations were analyzed by enzyme immunoassay. Our results revealed that both fGC and fecal DHEAS concentrations are higher in females housed indoors in single cages than in those living outdoors in social groups. We also found that fGC concentrations were higher in the cycling females during the mating (winter) season than the lactating females in the birth (spring) season. Age was negatively associated to both fGC and fecal DHEAS levels, but the relationship between age and fecal DHEAS was more evident in females housed indoors in single cages than in females housed in outdoor social groups. We did not observe any association of dominance rank with either fecal DHEAS or fGC. This study showed that measurement of fecal DHEAS and fGC can be a good method to assess stress in Japanese macaques. These findings provide insights about the physiology of these two adrenal hormones in female Japanese macaques, which can be applied to wild populations and is fundamental for captive management and conservation biology.

Multimodal sexual signaling and mating behavior in olive baboons (Papio anubis).

In primate species, mating decisions seem to be based on multiple signal elements with different roles in the signaling of female reproductive status. Whereas some primate signals are relatively well described (e.g., sexual swellings and copulation calls), studies that simultaneously assess visual, auditory, behavioral, and olfactory cues as signals of reproductive state are rarely undertaken. We used data on variation in sexual behaviors and sexual swellings in relation to the fertile period (estimated from the date of swelling detumescence) from a troop of semi-free ranging olive baboons (Papio anubis) to assess how different signals influence patterns of mate choice. Using an objective and quantitative measure of swelling size and color, along with detailed data on sexual behaviors from 13 cycles of nine adult females, we found that fine-scale variation in sexual swelling size, female behavior and copulation call rates could advertise the beginning of the fertile phase whereas swelling color did not. Rates of olfactory inspections by males also increased during the fertile phase, suggesting that olfactory signals were of interest to males and may contain information about ovulation. There was no relationship between female characteristics (age and rank) and the expression of sexual signals, except for proceptive behaviors which increased with female rank. Males displayed more sexual behaviors such as approaches and holding and tended to direct more ejaculatory mounts during the fertile phase. All together, we suggest that whereas all males could have information concerning the timing of ovulation through female proceptive behaviors and swelling size, consorting males may have access to additional signals (olfactory cues). Sexual communication in olive baboons is consistent with a multimodal framework for fertility signaling, potentially allowing males and females to establish different mating strategies. The possible selective pressures leading to multi-modal signaling are discussed.

Monkeys in the middle: parasite transmission through the social network of a wild primate.

In wildlife populations, group-living is thought to increase the probability of parasite transmission because contact rates increase at high host densities. Physical contact, such as social grooming, is an important component of group structure, but it can also increase the risk of exposure to infection for individuals because it provides a mechanism for transmission of potentially pathogenic organisms. Living in groups can also create variation in susceptibility to infection among individuals because circulating levels of immunosuppressive hormones like glucocorticoids often depend on an individual's position within the group's social structure. Yet, little is known about the relative roles of socially mediated exposure versus susceptibility in parasite transmission among free-living animal groups. To address this issue, we investigate the relationship between host dominance hierarchy and nematode parasite transmission among females in a wild group of Japanese macaques (Macaca fuscata yakui). We use social network analysis to describe each individual female's position within the grooming network in relation to dominance rank and relative levels of infection. Our results suggest that the number of directly-transmitted parasite species infecting each female, and the relative amount of transmission stages that one of these species sheds in faeces, both increase with dominance rank. Female centrality within the network, which shows positive associations with dominance hierarchy, is also positively associated with infection by certain parasite species, suggesting that the measured rank-bias in transmission may reflect variation in exposure rather than susceptibility. This is supported by the lack of a clear relationship between rank and faecal cortisol, as an indicator of stress, in a subset of these females. Thus, socially mediated exposure appears to be important for direct transmission of nematode parasites, lending support to the idea that a classical fitness trade-off inherent to living in groups can exist.