Visual and acoustic exploratory behaviors toward novel stimuli in Antillean manatees (Trichechus manatus manatus) under human care.

Exploratory behaviors describe the actions performed by an animal to obtain information on an object, environment, or individual by using its different senses. Exploration is described in some marine mammals, but not yet in manatees. Our study investigated behavioral and acoustic responses of two groups of Antillean manatees (N = 12 and N = 4) housed in zoological parks toward various stimuli involving three sensory modalities: visual, tactile, and auditory. Simultaneous audio and video recordings were collected during three periods of time (i.e., before, during, and after the presentation of all stimuli). Behaviors related to interest, social behaviors, the number and type of calls produced, and their frequency and duration were recorded and analyzed. Manatees reacted more to submerged stimuli than to out-of-water and sound stimuli, with an increase in approach, social contacts, and number of vocalizations. The proportion of squeaks and squeals call types also varied according to stimuli, and call entropy and F0 range varied according to periods. Our results suggest that manatees display sensory preferences when exploring stimuli, with more interest in manipulable stimuli, supporting the importance of their somatic perception. We highlight the need for particular enrichment programs (i.e., involving submerged objects) in zoological facilities. By displaying social contacts and by producing vocalizations, manatees communicate information such as their motivational state. The increase in call rate, harsh calls, and entropy values could be valid indicators of heightened arousal. We encourage further studies to associate acoustic recordings with ethological data collection to increase the understanding of manatees' behaviors andperception. (PsycInfo Database Record (c) 2023 APA, all rights reserved).

Ranking parameters driving siring success during sperm competition in the North African houbara bustard.

Sperm competition is a powerful force driving the evolution of ejaculate and sperm traits. However, the outcome of sperm competition depends on many traits that extend beyond ejaculate quality. Here, we study male North African houbara bustards (Chlamydotis undulata undulata) competing for egg fertilization, after artificial insemination, with the aim to rank the importance of 14 parameters as drivers of siring success. Using a machine learning approach, we show that traits independent of male quality (i.e., insemination order, delay between insemination and egg laying) are the most important predictors of siring success. Traits describing intrinsic male quality (i.e., number of sperm in the ejaculate, mass motility index) are also positively associated with siring success, but their contribution to explaining the outcome of sperm competition is much lower than for insemination order. Overall, this analysis shows that males mating at the last position in the mating sequence have the best chance to win the competition for egg fertilization. This raises the question of the importance of female behavior as determinant of mating order.

Enforced monoandry over generations induces a reduction of female investment into reproduction in a promiscuous bird.

While uncovering the costs and benefits of polyandry has attracted considerable attention, assessing the net effect of sexual selection on population fitness requires the experimental manipulation of female mating over generations, which is usually only achievable in laboratory populations of arthropods. However, knowing if sexual selection improves or impairs the expression of life-history traits is key for the management of captive populations of endangered species, which are mostly long-lived birds and mammals. It might therefore be questionable to extrapolate the results gathered on laboratory populations of insects to infer the net effect of sexual selection on populations of endangered species. Here, we used a longitudinal dataset that has been collected on a long-lived bird, the houbara bustard, kept in a conservation breeding program, to investigate the effect of enforced monoandry on female investment into reproduction. In captivity, female houbara bustards are artificially inseminated with sperm collected from a single male (enforced monoandry), or sequentially inseminated with semen of different males (polyandry), allowing postcopulatory sexual selection to operate. We identified female lines that were produced either by monoandrous or polyandrous inseminations over three generations, and we compared reproductive investment of females from the two mating system groups. We found that females in the polyandrous lines had higher investment into reproduction as they laid more eggs per season and produced heavier hatchlings. Higher reproductive investment into reproduction in the polyandrous lines did not result from inherited differences from females initially included in the two mating system groups. These results show that removal of sexual selection can alter reproductive investment after only few generations, potentially hindering population fitness and the success of conservation breeding programs.

Prosociality and reciprocity in capybaras (Hydrochoerus hydrochaeris) in a non-reproductive context.

Prosocial behaviours (providing benefits to a recipient with or without cost for the donor) have been found to be highly influenced by sex and by hierarchy. Rodents, in particular, are good model for studying prosocial responses, as they were found to exhibit intentional prosocial behaviours to reward a conspecific, and are very sensitive to reciprocity. In our study, we conducted a Prosocial Choice Test (PCT) in which four capybaras (Hydrochoerus hydrochaeris) living in a social group could choose between three tokens: choosing the prosocial token rewarded simultaneously the subject and a recipient, while choosing the selfish token only rewarded the subject; and choosing the null token provided no reward to anyone. Dominance within each dyad was also studied, both before and during the PCT experiment. Our results showed an influence of hierarchy: subjects were more prosocial towards the recipient when it was a subordinate than when it was a dominant individual. These results could be interpreted as a desire of strengthening a hierarchical rank regarding the subordinate, of punishing aggressive conspecifics (usually the subject's direct dominant), and of weakening dominant individuals in order to modify the pre-existing hierarchy. Additionally, our results highlighted a direct reciprocity phenomenon, a subject being more likely to be prosocial towards a prosocial recipient. All these findings suggest that prosociality could be well developed in other taxa than Primates and that, in long enough PCT experiments, subtle rules could influence individual prosocial strategies.

Paternal age negatively affects sperm production of the progeny.

Parental age has profound consequences for offspring's phenotype. However, whether patrilineal age affects offspring sperm production remains unknown, despite the importance of sperm production for male reproductive success in species facing post-copulatory sexual selection. Using a longitudinal dataset on ejaculate attributes of the houbara bustard, we showed that offspring sired by old fathers had different age-dependent trajectories of sperm production compared to offspring sired by young fathers. Specifically, they produced less sperm (-48%) in their first year of life, and 14% less during their lifetime. Paternal age had the strongest effect, with weak evidence for grandpaternal or great grandpaternal age effects. These results show that paternal age can affect offspring reproductive success by reducing sperm production, establishing an intergenerational link between ageing and sexual selection.

No evidence for prezygotic postcopulatory avoidance of kin despite high inbreeding depression.

Offspring resulting from mating among close relatives can suffer from impaired fitness through the expression of recessive alleles with deleterious effects. Postcopulatory sperm selection (a prezygotic mechanism of cryptic female choice) has been suggested to be an effective way to avoid inbreeding. To investigate whether postcopulatory female choice allows the avoidance of fertilization by close kin, we performed artificial inseminations in a promiscuous bird, the houbara bustard (Chlamydotis undulata undulata). Females were inseminated with a mix of sperm from triads of males, each constituted of a male genetically unrelated to the female, a first cousin and a half-sibling. When counting the number of eggs sired by unrelated males, cousins or half-siblings, we found a significant deviation from the expected random distribution, with more eggs sired by unrelated males. However, offspring sired by cousins, and especially by half-siblings suffered from high prehatching mortality, suggesting that the observed paternity skew towards unrelated males might reflect differential offspring mortality rather than sperm selection. In agreement with this hypothesis, within-triad siring success was similar for the three parental relatedness categories, but the relationship between siring and hatching success differed across categories. In clutches with high hatching success, unrelated males had the highest success while in clutches with high failure rate, half-siblings had the highest success. Offspring sired by half-siblings also suffered from reduced growth rate during the first three months and higher posthatching mortality. Hence, despite substantial fitness costs associated with fertilization by close relatives, females do not seem to select sperm of unrelated males.

Reading wild minds: A computational assay of Theory of Mind sophistication across seven primate species.

Theory of Mind (ToM), i.e. the ability to understand others' mental states, endows humans with highly adaptive social skills such as teaching or deceiving. Candidate evolutionary explanations have been proposed for the unique sophistication of human ToM among primates. For example, the Machiavellian intelligence hypothesis states that the increasing complexity of social networks may have induced a demand for sophisticated ToM. This type of scenario ignores neurocognitive constraints that may eventually be crucial limiting factors for ToM evolution. In contradistinction, the cognitive scaffolding hypothesis asserts that a species' opportunity to develop sophisticated ToM is mostly determined by its general cognitive capacity (on which ToM is scaffolded). However, the actual relationships between ToM sophistication and either brain volume (a proxy for general cognitive capacity) or social group size (a proxy for social network complexity) are unclear. Here, we let 39 individuals sampled from seven non-human primate species (lemurs, macaques, mangabeys, orangutans, gorillas and chimpanzees) engage in simple dyadic games against artificial ToM players (via a familiar human caregiver). Using computational analyses of primates' choice sequences, we found that the probability of exhibiting a ToM-compatible learning style is mainly driven by species' brain volume (rather than by social group size). Moreover, primates' social cognitive sophistication culminates in a precursor form of ToM, which still falls short of human fully-developed ToM abilities.

The sperm of aging male bustards retards their offspring's development.

Understanding whether the sperm of older males has a diminished capacity to produce successful offspring is a key challenge in evolutionary biology. We investigate this issue using 10 years of reproductive data on captive long-lived houbara bustards (Chlamydotis undulata), where the use of artificial insemination techniques means parents can only influence offspring quality via their gametes. Here we show that paternal aging reduces both the likelihood that eggs hatch and the rate at which chicks grow, with older males producing the lightest offspring after the first month. Surprisingly, this cost of paternal aging on offspring development is of a similar scale to that associated with maternal aging. Fitting with predictions on germline aging, the sperm of immature males produce the fastest growing offspring. Our findings thus indicate that any good genes benefit that might be offered by older 'proven' males will be eroded by aging of their germline DNA.

Does recognized genetic management in supportive breeding prevent genetic changes in life-history traits?

Supportive breeding is one of the last resort conservation strategies to avoid species extinction. Management of captive populations is challenging because several harmful genetic processes need to be avoided. Several recommendations have been proposed to limit these deleterious effects, but empirical assessments of these strategies remain scarce. We investigated the outcome of a genetic management in a supportive breeding for the Houbara Bustard. At the phenotypic level, we found an increase over generations in the mean values of gamete production, body mass and courtship display rate. Using an animal model, we found that phenotypic changes reflected genetic changes as evidenced by an increase in breeding values for all traits. These changes resulted from selection acting on gamete production and to a lesser extent on courtship display. Selection decreased over years for female gametes, emphasizing the effort of managers to increase the contribution of poor breeders to offspring recruited in the captive breeding. Our results shed light on very fast genetic changes in an exemplary captive programme that follows worldwide used recommendations and emphasizes the need of more empirical evidence of the effects of genetic guidelines on the prevention of genetic changes in supportive breeding.

Plasma protein electrophoresis in birds: comparison of a semiautomated agarose gel system with an automated capillary system.

Plasma agarose gel electrophoresis (AGE) is recognized as a very reliable diagnostic tool in avian medicine. Within the last 10 years, new electrophoresis techniques such as capillary zone electrophoresis (CZE) have emerged in human laboratory medicine but have never been investigated in birds. To investigate the use of CZE in birds and to compare it with AGE, plasma samples from 30 roosters (Gallus gallus), 20 black kites (Milvus migrans), and 10 racing pigeons (Columba livia) were analyzed by both AGE and CZE. For the 3 species studied, values determined by AGE and CZE were well correlated for albumin and beta and gamma fractions whereas other values differed significantly. Values for alpha-3 fraction in the rooster, alpha-1 fraction in the black kite, and alpha fractions in the pigeon obtained by AGE were very well correlated with the prealbumin fraction values obtained by CZE. Repeatability and reproducibility appeared higher with CZE than with AGE. Although the interpretation of CZE electrophoresis patterns seems to produce results similar to those obtained with AGE, some proteins present in the alpha fraction measured with AGE migrated to the prealbumin fraction found with CZE. Although CZE requires the use of specific reference intervals and a much higher sample volume, this method has many advantages when compared with AGE, including better repeatability and reproducibility and higher analysis output.

Response to bitter substances in primates: roles of diet tendency and weaning age.

In primates, the perception of bitter taste may be an essential mechanism for avoiding the ingestion of bitter, and often toxic, substances. Bitterness sensitivity varies across the different primate species and, for bitter thioure substances (e.g., phenylthiocarbamide-PTC), within species. Primates respond to bitterness by displaying aversive affective reactions, and whether these serve for conspecifics as information on the taste of food is still unclear. The aim of this study was to investigate the response to two bitter substances (quinine and PTC) in 11 primate species (N = 29 individuals) hosted at the Ménagerie du Jardin des Plantes, in relation to their main diet tendency and weaning age. We tested primate reactions to bitterness with a two-bottle method. The study individuals showed a strong aversion to bitter taste, minimizing consumption of both bitter solutions. All of the individuals were PTC-taster phenotypes, but the degrees of sensitivity to PTC varied among the individuals. Across-species comparisons revealed that whereas the degree of frugivory of the species had a negative effect on the consumption of bitter solutions by the individuals, a later weaning age seems to be a better predictor for the occurrence of aversive affective reactions. Although the low sample size does not allow for excluding interindividual variability, our results support the hypothesis that affective reactions to bitterness may be trustworthy information for conspecifics during the learning process. Thus, the evolution of the appropriate perceiver systems to convert affective displays into true affective signals could be a shared trait among human and nonhuman primates.

Quantitative genetics of sexual display, ejaculate quality and size in a lekking species.

The investment into extravagant sexual display and competitive sperm are two essential components of pre- and post-copulatory sexual selection. Even though the selective forces acting on sexual display and sperm characteristics have been extensively studied in recent years, the genetic architecture underlying the expression of these traits has been rarely explored. Here, we estimated the genetic variances and covariances of traits linked with ejaculate size and quality, and sexual display in the houbara bustard (Chlamydotis undulata undulata, Jacquin 1784). Using a very large pedigree-based data set, we show that sexual signalling and ejaculate size (but not ejaculate quality) are heritable and genetically positively correlated. The matrix of genetic covariances also provided support for some across-sex correlations: male and female gamete numbers are positively correlated, and more surprisingly, male display and female gamete numbers are also positively correlated. These results can have important implications for the understanding of the evolution of sperm traits and sexual display in animals.

Unusual feeding behavior in wild great apes, a window to understand origins of self-medication in humans: role of sociality and physiology on learning process.

Certain toxic plants are beneficial for health if small amounts are ingested infrequently and in a specific context of illness. Among our closest living relatives, chimpanzees are found to consume plants with pharmacological properties. Providing insight on the origins of human self-medication, this study investigates the role social systems and physiology (namely gut specialization) play on learning mechanisms involved in the consumption of unusual and potentially bioactive foods by two great ape species. We collected data from a community of 41-44 wild chimpanzees in Uganda (11 months, 2008), and a group of 11-13 wild western gorillas in Central African Republic (10 months, 2008-2009). During feeding, we recorded food consumed, its availability, and social interactions (including observers watching conspecifics and the observers' subsequent activity). Unusual food consumption in chimpanzees was twice higher than in gorillas. Additionally chimpanzees relied more on social information with vertical knowledge transmission on unusual foods by continually acquiring information during their life through mostly observing the fittest (pre-senescent) adults. In contrast, in gorillas observational learning primarily occurred between related immatures, showing instead the importance of horizontal knowledge transmission. As chimpanzees' guts are physiologically less specialized than gorillas (more capable of detoxifying harmful compounds), unusual-food consumption may be more risky for chimpanzees and linked to reasons other than nutrition (like self-medication). Our results show that differences in sociality and physiology between the two species may influence mechanisms that discriminate between plants for nutrition and plants with potential therapeutic dietary components. We conclude that self-medication may have appeared in our ancestors in association with high social tolerance and lack of herbivorous gut specialization.

Training large macaws for artificial insemination procedures.

For some endangered parrot species, captive breeding may be the only insurance for their survival. However, many individuals in captivity do not reproduce. Artificial insemination (AI) may help overcome reproductive failures or geographic distance. For semen collection in birds, massage is the most commonly used method. However, this process, which usually requires capture and restraint, involves risk of stress and injuries. The aim of this experiment was to train large macaws to accept the physical manipulations of their body parts needed for the artificial insemination process. Within 15 weeks, a male and a female Buffon's macaw (Ara ambiguus) learned to accept handling without apparent stress. A pair of green-winged macaws (Ara chloropterus) progressed more slowly and displayed some signs of stress. This stress highlights the need to monitor the birds' possible signs of discomfort during the training in order to adapt the working protocol. These results demonstrate that it is possible to train the AI behaviors, thus avoiding the capture, restraint, and anesthesia. An added benefit to this is the potential for the training to provide a form of behavioral enrichment.

Immune-mediated change in the expression of a sexual trait predicts offspring survival in the wild.

BACKGROUND: The "good genes" theory of sexual selection postulates that females choose mates that will improve their offspring's fitness through the inheritance of paternal genes. In spite of the attention that this hypothesis has given rise to, the empirical evidence remains sparse, mostly because of the difficulties of controlling for the many environmental factors that may covary with both the paternal phenotype and offspring fitness. Here, we tested the hypothesis that offspring sired by males of a preferred phenotype should have better survival in an endangered bird, the houbara bustard (Chlamydotis undulata undulata). METHODOLOGY/PRINCIPAL FINDINGS: We tested if natural and experimentally-induced variation in courtship display (following an inflammatory challenge) predicts the survival of offspring. Chicks were produced by artificial insemination of females, ensuring that any effect on survival could only arise from the transfer of paternal genes. One hundred and twenty offspring were equipped with radio transmitters, and their survival monitored in the wild for a year. This allowed assessment of the potential benefits of paternal genes in a natural setting, where birds experience the whole range of environmental hazards. Although natural variation in sire courtship display did not predict offspring survival, sires that withstood the inflammatory insult and maintained their courtship activity sired offspring with the best survival upon release. CONCLUSIONS: This finding is relevant both to enlighten the debate on "good genes" sexual selection and the management of supportive breeding programs.

Pigeons discriminate between human feeders.

Considered as plague in many cities, pigeons in urban areas live close to human activities and exploit this proximity to find food which is often directly delivered by people. In this study, we explored the capacity of feral pigeons to take advantage of this human-based food resource and discriminate between friendly and hostile people. Our study was conducted in an urban park. Pigeons were fed by two experimenters of approximately the same age and skin colour but wearing coats of different colours. During the training sessions, the two human feeders displayed different attitudes: one of the feeders was neutral and the second was hostile and chased away the pigeons. During the two test phases subsequent to the training phase, both feeders became neutral. Two experiments were conducted, one with one male and one female feeder and the second with two female feeders. In both experiments, the pigeons learned to quickly (six to nine sessions) discriminate between the feeders and maintained this discrimination during the test phases. The pigeons avoided the hostile feeder even when the two feeders exchanged their coats, suggesting that they used stable individual characteristics to differentiate between the experimenter feeders. Thus, pigeons are able to learn quickly from their interactions with human feeders and use this knowledge to maximize the profitability of the urban environment. This study provides the first experimental evidence in feral pigeons for this level of human discrimination.

Neophobia and learning mechanisms: how captive orangutans discover medicinal plants.

Great apes sometimes feed on items of low nutritional value with bioactive secondary compounds. These molecules may be toxic and neophobia is presumed to be an essential factor in avoiding the ingestion of noxious items. The aim of this study is to investigate, in captive orangutans, individual and social learning involved in the discovery and ingestion of new items. We presented novel aromatic plants - 11 fresh plants and 4 infused plants - to 4 captive weaned Bornean orangutans, both under isolated and group conditions, and recorded their behaviour and interactions between group members. All animals tasted by nibbling or ingested most of the plants presented. Regardless of the experimental condition, individual responses did not vary visibly across the sessions, despite numerous close observations, and food transfers between individuals were observed. Our results suggest that a low level of neophobia and a strong propensity to look to conspecifics for information allow Bornean orangutans to expand their diet after weaning. Our results also provide some evidence that olfaction is a key sense in determining food edibility based on previous experience.

Male health status, signalled by courtship display, reveals ejaculate quality and hatching success in a lekking species.

1. The information content of secondary sexual traits and the benefits gathered by choosy females are at the heart of sexual selection theory. Indicator models of sexual selection assume that secondary sexual traits reflect the phenotypic/genetic quality of their bearers and that females gather benefits from choosing these high-quality males. 2. Here, we tested the idea that courtship display reflects the health status in a bird species with a lek-based mating system, the houbara bustard (Chlamydotis undulata undulata). A group of males was treated with the lipopolysaccharide (LPS) of the cell wall of the bacterium Escherichia coli during the seasonal peak of courtship display, while another group of males was injected with a phosphate-buffered saline solution (PBS) as a control. We then monitored the effect of the treatment on both courtship display and ejaculate quality. Finally, females were artificially inseminated with semen from LPS and PBS males, which allowed us to assess the effect of the immunological treatment on reproduction. 3. We found that the inflammatory challenge reduced courtship display and semen quality compared to controls. Interestingly, males that better resisted to the immune challenge in terms of courtship display also better resisted in terms of ejaculate quality. Early reproductive failure was increased when females were artificially inseminated with semen from immune-activated males. Failure of eggs laid by females inseminated with LPS semen was due to a reduced fertilization power of sperm of LPS males or to increased embryo mortality in the very early stage of embryo development. As a consequence, hatching rate was reduced for females inseminated with semen collected from LPS males. 4. These results show that by assessing male courtship display, females may gain insight into the current phenotypic/genetic quality of mates and gather fitness benefits in terms of reproductive success.