Mapping vocal interactions in space and time differentiates signal broadcast versus signal exchange in meerkat groups.

Animal vocal communication research traditionally focuses on acoustic and contextual features of calls, yet substantial information is also contained in response selectivity and timing during vocalization events. By examining the spatiotemporal structure of vocal interactions, we can distinguish between 'broadcast' and 'exchange' signalling modes, with the former potentially serving to transmit signallers' general state and the latter reflecting more interactive signalling behaviour. Here, we tracked the movements and vocalizations of wild meerkat (Suricata suricatta) groups simultaneously using collars to explore this distinction. We found evidence that close calls (used for maintaining group cohesion) are given as signal exchanges. They are typically given in temporally structured call-response sequences and are also strongly affected by the social environment, with individuals calling more when they have more neighbours and juveniles responding more to adults than the reverse. In contrast, short note calls appear mainly in sequences produced by single individuals and show little dependence on social surroundings, suggesting a broadcast signalling mode. Despite these differences, both call categories show similar clustering in space and time at a group level. Our results highlight how the fine-scale structure of vocal interactions can give important insights into the usage and function of signals in social groups. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics.'

Meerkat manners: Endocrine mediation of female dominance and reproductive control in a cooperative breeder.

This article is part of a Special Issue (Hormones and Hierarchies). To gain more balanced understanding of sexual selection and mammalian sexual differentiation processes, this review addresses behavioral sex differences and hormonal mediators of intrasexual competition in the meerkat (Suricata suricatta) - a cooperative breeder unusual among vertebrates in its female aggression, degree of reproductive skew, and phenotypic divergence. Focused on the evolution, function, mechanism, and development of female dominance, the male remains a key reference point throughout. Integrated review of endocrine function does not support routine physiological suppression in subordinates of either sex, but instead a ramp up of weight, reproduction, aggression, and sex steroids, particularly androgens, in dominant females. Important and timely questions about female competition are thus addressed by shifting emphasis from mediators of reproductive suppression to mediators of reproductive control, and from organizational and activational roles of androgens in males to their roles in females. Unusually, we ask not only how inequity is maintained, but how dominance is acquired within a lifetime and across generations. Antiandrogens administered in the field to males and pregnant dominant females confirm the importance of androgen-mediated food competition. Moreover, effects of maternal endocrine milieu on offspring development reveal a heritable, androgenic route to female aggression, likely promoting reproductive priority along dominant matrilines. Integrating endocrine measures with long-term behavioral, ecological, morphological, and life-history data on normative and experimental individuals, across life stages and generations, provides better appreciation of the role of naturally circulating androgens in regulating the female phenotype, and sheds new light on the evolution of female dominance, reproductive inequity, and cooperative breeding.

An intergenerational androgenic mechanism of female intrasexual competition in the cooperatively breeding meerkat.

Female intrasexual competition can be intense in cooperatively breeding species, with some dominant breeders (matriarchs) limiting reproduction in subordinates via aggression, eviction or infanticide. In males, such tendencies bidirectionally link to testosterone, but in females, there has been little systematic investigation of androgen-mediated behaviour within and across generations. In 22 clans of wild meerkats (Suricata suricatta), we show that matriarchs 1) express peak androgen concentrations during late gestation, 2) when displaying peak feeding competition, dominance behaviour, and evictions, and 3) relative to subordinates, produce offspring that are more aggressive in early development. Late-gestation antiandrogen treatment of matriarchs 4) specifically reduces dominance behaviour, is associated with infrequent evictions, decreases social centrality within the clan, 5) increases aggression in cohabiting subordinate dams, and 6) reduces offspring aggression. These effects implicate androgen-mediated aggression in the operation of female sexual selection, and intergenerational transmission of masculinised phenotypes in the evolution of meerkat cooperative breeding.

Mongooses (Urva auropunctata) as reservoir hosts of Leptospira species in the United States Virgin Islands, 2019-2020.

During 2019-2020, the Virgin Islands Department of Health investigated potential animal reservoirs of Leptospira spp., the bacteria that cause leptospirosis. In this cross-sectional study, we investigated Leptospira spp. exposure and carriage in the small Indian mongoose (Urva auropunctata, syn: Herpestes auropunctatus), an invasive animal species. This study was conducted across the three main islands of the U.S. Virgin Islands (USVI), which are St. Croix, St. Thomas, and St. John. We used the microscopic agglutination test (MAT), fluorescent antibody test (FAT), real-time polymerase chain reaction (lipl32 rt-PCR), and bacterial culture to evaluate serum and kidney specimens and compared the sensitivity, specificity, positive predictive value, and negative predictive value of these laboratory methods. Mongooses (n = 274) were live-trapped at 31 field sites in ten regions across USVI and humanely euthanized for Leptospira spp. testing. Bacterial isolates were sequenced and evaluated for species and phylogenetic analysis using the ppk gene. Anti-Leptospira spp. antibodies were detected in 34% (87/256) of mongooses. Reactions were observed with the following serogroups: Sejroe, Icterohaemorrhagiae, Pyrogenes, Mini, Cynopteri, Australis, Hebdomadis, Autumnalis, Mankarso, Pomona, and Ballum. Of the kidney specimens examined, 5.8% (16/270) were FAT-positive, 10% (27/274) were culture-positive, and 12.4% (34/274) were positive by rt-PCR. Of the Leptospira spp. isolated from mongooses, 25 were L. borgpetersenii, one was L. interrogans, and one was L. kirschneri. Positive predictive values of FAT and rt-PCR testing for predicting successful isolation of Leptospira by culture were 88% and 65%, respectively. The isolation and identification of Leptospira spp. in mongooses highlights the potential role of mongooses as a wildlife reservoir of leptospirosis; mongooses could be a source of Leptospira spp. infections for other wildlife, domestic animals, and humans.

A veil of ignorance can promote fairness in a mammal society.

Rawls argued that fairness in human societies can be achieved if decisions about the distribution of societal rewards are made from behind a veil of ignorance, which obscures the personal gains that result. Whether ignorance promotes fairness in animal societies, that is, the distribution of resources to reduce inequality, is unknown. Here we show experimentally that cooperatively breeding banded mongooses, acting from behind a veil of ignorance over kinship, allocate postnatal care in a way that reduces inequality among offspring, in the manner predicted by a Rawlsian model of cooperation. In this society synchronized reproduction leaves adults in a group ignorant of the individual parentage of their communal young. We provisioned half of the mothers in each mongoose group during pregnancy, leaving the other half as matched controls, thus increasing inequality among mothers and increasing the amount of variation in offspring birth weight in communal litters. After birth, fed mothers provided extra care to the offspring of unfed mothers, not their own young, which levelled up initial size inequalities among the offspring and equalized their survival to adulthood. Our findings suggest that a classic idea of moral philosophy also applies to the evolution of cooperation in biological systems.

Modeling Mongoose Rabies in the Caribbean: A Model-Guided Fieldwork Approach to Identify Research Priorities.

We applied the model-guided fieldwork framework to the Caribbean mongoose rabies system by parametrizing a spatially-explicit, individual-based model, and by performing an uncertainty analysis designed to identify parameters for which additional empirical data are most needed. Our analysis revealed important variation in output variables characterizing rabies dynamics, namely rabies persistence, exposure level, spatiotemporal distribution, and prevalence. Among epidemiological parameters, rabies transmission rate was the most influential, followed by rabies mortality and location, and size of the initial infection. The most influential landscape parameters included habitat-specific carrying capacities, landscape heterogeneity, and the level of resistance to dispersal associated with topography. Movement variables, including juvenile dispersal, adult fine-scale movement distances, and home range size, as well as life history traits such as age of independence, birth seasonality, and age- and sex-specific mortality were other important drivers of rabies dynamics. We discuss results in the context of mongoose ecology and its influence on disease transmission dynamics. Finally, we suggest empirical approaches and study design specificities that would provide optimal contributing data addressing the knowledge gaps identified by our approach, and would increase our potential to use epidemiological models to guide mongoose rabies control and management in the Caribbean.

Call order within vocal sequences of meerkats contains temporary contextual and individual information.

BACKGROUND: The ability to recombine smaller units to produce infinite structures of higher-order phrases is unique to human language, yet evidence of animals to combine multiple acoustic units into meaningful combinations increases constantly. Despite increasing evidence for meaningful call combinations across contexts, little attention has been paid to the potential role of temporal variation of call type composition in longer vocal sequences in conveying information about subtle changes in the environment or individual differences. Here, we investigated the composition and information content of sentinel call sequences in meerkats (Suricata suricatta). While being on sentinel guard, a coordinated vigilance behaviour, meerkats produce long sequences composed of six distinct sentinel call types and alarm calls. We analysed recordings of sentinels to test if the order of the call types is graded and whether they contain additional group-, individual-, age- or sex-specific vocal signatures. RESULTS: Our results confirmed that the six distinct types of sentinel calls in addition to alarm calls were produced in a highly graded way, likely referring to changes in the perceived predation risk. Transitions between call types one step up or down the a priory assumed gradation were over-represented, while transitions over two or three steps were significantly under-represented. Analysing sequence similarity within and between groups and individuals demonstrated that sequences composed of the most commonly emitted sentinel call types showed high within-individual consistency whereby adults and females had higher consistency scores than subadults and males respectively. CONCLUSIONS: We present a novel type of combinatoriality where the order of the call types contains temporary contextual information, and also relates to the identity of the caller. By combining different call types in a graded way over long periods, meerkats constantly convey meaningful information about subtle changes in the external environment, while at the same time the temporal pattern of the distinct call types contains stable information about caller identity. Our study demonstrates how complex animal call sequences can be described by simple rules, in this case gradation across acoustically distinct, but functionally related call types, combined with individual-specific call patterns.

Sperm evaluation and morphological description of male genitalia of meerkats (Suricata suricatta).

In ex situ conditions, little is known about the reproductive biology of meerkats. The aim of present study was to describe the morphological aspects of male genital organs and accessory glands using macroscopic evaluation, ultrasonography, and radiography, as well as describing semen characteristics post-electroejaculation. The results indicated anatomical characteristics of meerkats are very similar to those of cats, having a prostate, accessory bulbourethral glands, and an elongated and radiopaque structure in the penis, which is indicative of there being a baculum. The testicular volume was 0.81 cm³ (± 0.10) and the relative testis weight was 1.37 cm³/kg (± 0.15). Both testicles are present in the scrotum, which has an ellipsoidal shape, homogeneous texture, hypoechoic parenchyma and are encased in a hyperechoic tunica albuginea. Electroejaculation was effectively induced in all animals for semen collection with utilization of medetomidine and ketamine. The values semen samples variables were as follows for volume - 0.125 ±â€¯0.193 mL, motility - 19.8 ±â€¯18.6 %, vigor - 1.9 ±â€¯1.0, concentration - 40.5 ±â€¯25.2 × 106 sperm/mL and morphologically normal sperm - 10.8 ±â€¯6.6 %. This is the first study in which there is a description of morphological and imaging aspects of the male reproductive tracts of meerkats, as well as the seminal characteristics after using electroejaculation for semen collection. Knowledge of anatomical and seminal characteristics is essential for implementation of assisted reproduction programs, as well as reproductive management in the species.

Signalling adjustments to direct and indirect environmental effects on signal perception in meerkats.

The efficiency of communication between animals is determined by the perception range of signals. With changes in the environment, signal transmission between a sender and a receiver can be influenced both directly, where the signal's propagation quality itself is affected, and indirectly where the senders or receivers' behaviour is impaired, impacting for example the distance between them. Here we investigated how meerkats (Suricata suricatta) in the Kalahari Desert adjust to these challenges in the context of maintaining group cohesion through contact calls. We found that meerkats changed their calling rate when signal transmission was affected indirectly due to increased dispersion of group members as during a drought, but not under typical wet conditions, when signal transmission was directly affected due to higher vegetation density. Instead under these wetter conditions, meerkats remained within proximity to each other. Overall, both direct and indirect environmental effects on signal perception resulted in an increased probability of groups splitting. In conclusion, we provide evidence that social animals can flexibly adjust their vocal coordination behaviour to cope with direct and indirect effects of the environment on signal perception, but these adjustments have limitations.

Rapid evolution of the primate larynx?

Tissue vibrations in the larynx produce most sounds that comprise vocal communication in mammals. Larynx morphology is thus predicted to be a key target for selection, particularly in species with highly developed vocal communication systems. Here, we present a novel database of digitally modeled scanned larynges from 55 different mammalian species, representing a wide range of body sizes in the primate and carnivoran orders. Using phylogenetic comparative methods, we demonstrate that the primate larynx has evolved more rapidly than the carnivoran larynx, resulting in a pattern of larger size and increased deviation from expected allometry with body size. These results imply fundamental differences between primates and carnivorans in the balance of selective forces that constrain larynx size and highlight an evolutionary flexibility in primates that may help explain why we have developed complex and diverse uses of the vocal organ for communication.

Evaluating toxicity impacts of environmental exposed chromium on small Indian mongoose (Urva auropunctatus) hematological, biochemical and histopathological functioning.

Sub-lethal toxic impacts of chromium on hematological, biochemical and histological parameters were analyzed in the female small Indian mongoose (Urva auropuctatus) residing contaminated environment of tannery industry. Chromium bioaccumulation in the blood, liver and kidney tissue of the exposed mongooses was found elevated compared to the control mongooses' tissues. Total body weight (75.7%), liver weight (83.6%) as well as HSI (68.1%), RSI (86.2%) and the platelets counts (59.7%) were found significantly elevated, with significantly reduced RBCs (59.6%), and WBCs (64%). LFT and RFT were also found abnormal, moreover, the histopathological injuries had been distinct inside the kidney (>75%) and hepatic (>75%) tissues of exposed animals. Shrinkage and vacuolization (>75%) inside the hepatocyte expanded sinusoidal spaces and nuclear pyknosis (>75%) was evident within the hepatic tissue. Hypertrophy of epithelial cells of renal tubules and inter-renal cells of the head kidney with a reduction in tubular lumens (>75%) and vacuolization of tubules were witnessed within the kidney section. Atrophy inside the kidney inter-renal cells, glomeruli compression within the Bowman's capsules (>75%) following the necrosis in hematopoietic tissues were found in exposed animals. The present findings indicate that chronic exposure to chromium induces severe anemia, decreased serum protein concentration, hepatic and renal tissue histopathology, impairing the vital capabilities of liver, metabolic regulation, excretion, and stress homeostasis maintenance of which within the long-run may posture a severe risk to animal well-being then distress their inhabitants.

The globally invasive small Indian mongoose Urva auropunctata is likely to spread with climate change.

Invasive alien species represent one of the major factors of global loss of biodiversity and disruption of natural ecosystems. The small Indian mongoose, Urva auropunctata, is considered one of the wild carnivore species with the greatest negative impact on global biodiversity. Understanding of the factors underpinning the species' distribution and potential dispersion in a context of climate change thus appears crucial in the conservation of native ecosystems. Here we modelled the current and future climatically favourable areas for the small Indian mongoose using Ecological Niche Modelling based on data sets filtrated in environmental spaces. Projections from these models show extensive current favourable geographical areas, covering continental and insular regions within tropical and sub-tropical latitudes. Moreover, predictions for 2050 reveal that climate change is likely to expand current favourable areas north of the current favourable spaces, particularly in Eastern Europe. This climate-induced expansion is particularly worrisome given that the species is already spreading in the Balkan region. Our projections suggest that it is very likely that the small Indian mongoose will have an increasing influence on ecosystems and biodiversity in Europe by 2050.

Rapid evolution by sexual selection in a wild, invasive mammal.

Sexual selection theory provides a framework for investigating the evolution of traits involved in attracting and competing for mates. Given the sexual function of such traits, studies generally focus on individual interactions (i.e., displays and contests) in explaining trait origin and persistence. We show that ecological factors can strongly influence the adaptive value of these traits, and changes to these factors can lead to rapid evolutionary change. We compared sexually selected traits in the small Indian mongoose (Urva auropunctata) between their sparsely populated native range and four tropical islands to which they were introduced within the last 150 years and where, due to a lack of interspecific competition and predation, they have become invasive and densely populated. Because of a likely increase in encounter rate, we predicted that selection on long-distance chemical advertisement by males would relax in the introduced range. Accordingly, male, but not female, anal pads (used in scent marking) decreased in size in relation to both time since introduction and population density, and their relationship to body size and condition weakened. Concurrently, as predicted by intensified sperm competition, testis size increased following introduction. The small Indian mongoose thus experienced an inversion in the relative contributions to fitness of two sexual traits, followed by their rapid evolution in line with ecological changes.

Cost of dispersal in a social mammal: body mass loss and increased stress.

Dispersal is a key process influencing the dynamics of socially and spatially structured populations. Dispersal success is determined by the state of individuals at emigration and the costs incurred after emigration. However, quantification of such costs is often difficult, due to logistical constraints of following wide-ranging individuals. We investigated the effects of dispersal on individual body mass and stress hormone levels in a cooperative breeder, the meerkat ( Suricata suricatta). We measured body mass and faecal glucocorticoid metabolite (fGCM) concentrations from 95 dispersing females in 65 coalitions through the entire dispersal process. Females that successfully settled lost body mass, while females that did not settle but returned to their natal group after a short period of time did not. Furthermore, dispersing females had higher fGCM levels than resident females, and this was especially pronounced during the later stages of dispersal. By adding information on the transient stage of dispersal and by comparing dispersers that successfully settled to dispersers that returned to their natal group, we expand on previous studies focusing on the earlier stages of dispersal. We propose that body mass and stress hormone levels are good indicators to investigate dispersal costs, as these traits often play an important role in mediating the effects of the environment on other life-history events and individual fitness.

The development of individual differences in cooperative behaviour: maternal glucocorticoid hormones alter helping behaviour of offspring in wild meerkats.

The phenotype of parents can have long-lasting effects on the development of offspring as well as on their behaviour, physiology and morphology as adults. In some cases, these changes may increase offspring fitness but, in others, they can elevate parental fitness at a cost to the fitness of their offspring. We show that in Kalahari meerkats ( Suricata suricatta), the circulating glucocorticoid (GC) hormones of pregnant females affect the growth and cooperative behaviour of their offspring. We performed a 3-year experiment in wild meerkats to test the hypothesis that GC-mediated maternal effects reduce the potential for offspring to reproduce directly and therefore cause them to exhibit more cooperative behaviour. Daughters (but not sons) born to mothers treated with cortisol during pregnancy grew more slowly early in life and exhibited significantly more of two types of cooperative behaviour (pup rearing and feeding) once they were adults compared to offspring from control mothers. They also had lower measures of GCs as they aged, which could explain the observed increases in cooperative behaviour. Because early life growth is a crucial determinant of fitness in female meerkats, our results indicate that GC-mediated maternal effects may reduce the fitness of offspring, but may elevate parental fitness as a consequence of increasing the cooperative behaviour of their daughters. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Live long and prosper: durable benefits of early-life care in banded mongooses.

Kin selection theory defines the conditions for which altruism or 'helping' can be favoured by natural selection. Tests of this theory in cooperatively breeding animals have focused on the short-term benefits to the recipients of help, such as improved growth or survival to adulthood. However, research on early-life effects suggests that there may be more durable, lifelong fitness impacts to the recipients of help, which in theory should strengthen selection for helping. Here, we show in cooperatively breeding banded mongooses ( Mungos mungo) that care received in the first 3 months of life has lifelong fitness benefits for both male and female recipients. In this species, adult helpers called 'escorts' form exclusive one-to-one caring relationships with specific pups (not their own offspring), allowing us to isolate the effects of being escorted on later reproduction and survival. Pups that were more closely escorted were heavier at sexual maturity, which was associated with higher lifetime reproductive success for both sexes. Moreover, for female offspring, lifetime reproductive success increased with the level of escorting received per se, over and above any effect on body mass. Our results suggest that early-life social care has durable benefits to offspring of both sexes in this species. Given the well-established developmental effects of early-life care in laboratory animals and humans, we suggest that similar effects are likely to be widespread in social animals more generally. We discuss some of the implications of durable fitness benefits for the evolution of intergenerational helping in cooperative animal societies, including humans. This article is part of the theme issue 'Developing differences: early-life effects and evolutionary medicine'.

Meerkats (Suricata suricatta) are able to detect hidden food using olfactory cues alone.

Meerkats (Suricata suricatta) are known to strongly rely on chemical signals for social communication. However, little is known about their use of the sense of smell in foraging and food detection. The aim of the present study was therefore to assess whether captive meerkats are able to (1) detect hidden food using olfactory cues alone, (2) discriminate between the odor of real food and a single food odor component, and (3) build an association between the odor of real food and a novel odor. We employed the buried food test, widely used with rodents to assess basic olfactory abilities and designed to take advantage of the propensity of certain species to dig. We found that the meerkats were clearly able to find all four food types tested (mouse, chicken, mealworm, banana) using olfactory cues alone and that they successfully discriminated between the odor of real food (banana) and a food odor component (iso-pentyl acetate). In both tasks, the animals dug in the food-bearing corner of the test arena as the first one significantly more often than in the other three corners. No significant association-building between a food odor and a novel odor was found within the 60 trials performed per animal. We conclude that meerkats are able to use olfactory cues when foraging for hidden food. Further, we conclude that the buried food test, employed for the first time with a non-rodent species, is a useful means of assessing basic olfactory capabilities in meerkats.

Life history responses of meerkats to seasonal changes in extreme environments.

Species in extreme habitats increasingly face changes in seasonal climate, but the demographic mechanisms through which these changes affect population persistence remain unknown. We investigated how changes in seasonal rainfall and temperature influence vital rates and viability of an arid environment specialist, the Kalahari meerkat, through effects on body mass. We show that climate change-induced reduction in adult mass in the prebreeding season would decrease fecundity during the breeding season and increase extinction risk, particularly at low population densities. In contrast, a warmer nonbreeding season resulting in increased mass and survival would buffer negative effects of reduced rainfall during the breeding season, ensuring persistence. Because most ecosystems undergo seasonal climate variations, a full understanding of species vulnerability to global change relies on linking seasonal trait and population dynamics.

Environmental chromium from the tannery industry induces altered reproductive endpoints in the wild female small Indian mongoose ( Urva auropunctatus).

The populations of wild animals are declining in many parts of the world in response to man-made alterations in the environment. Environmental contamination due to heavy metals discharge from industry may contribute to the decline of wild animal populations by impacting their reproduction, growth, and development. In the leather tanning industry, chromium (Cr) is used as a basic component, but it is a potent toxicant that can affect many of the physiological functions of animals. In the current study, we investigated the reproductive toxicity of industrial Cr in female small Indian mongooses inhabiting a tannery area. Adult female specimens were live trapped from February 2015 to January 2016. Blood and other body tissues (ovaries, kidneys and liver) of the captured specimens were collected along with soil and water samples from the environment for analysis. The Cr concentrations were found significantly ( p < 0.0001) increased compared to control in the environment, blood, and all body tissues of the animals. Estradiol and progesterone levels were found to be significantly decreased in comparison with control ( p < 0.0001), along with reduced ovarian weights, while follicle stimulating hormone (FSH) and luteinizing hormone levels were found significantly ( p < 0.0001) elevated. Light microscopy revealed significantly decreased in comparison with control ovarian follicle numbers ( p < 0.0001) and diameters, vacuolization of the oocytes, and a significantly higher percentage of atretic follicles inside the ovary. We conclude that Cr discharged from the tanneries is absorbed by the exposed female small Indian mongoose, leading to ovarian dysfunction with potential impairment of reproductive function.

Vocal Turn-Taking in Meerkat Group Calling Sessions.

Coordination is a fundamental aspect of social living, underlying processes ranging from the maintenance of group cohesion to the avoidance of competition. Coordination can manifest as synchronization, where individuals perform the same action at the same time but can also take the form of anti-synchronization or turn-taking. Turn-taking has mainly been studied in the context of the development of language [1] due to the fact that it is a universal feature in all languages and has been found to appear early in infancy [2, 3]. Recently, turn-taking has received attention in animal communication research [4-7] as a potential foundation on which social communication was formed [1, 3]. In this study, we describe turn-taking in group-wide vocal interactions of meerkats (Suricata suricatta) during low-conflict sunning behavior, which is accompanied by the production of specific "sunning calls." We show that sunning-call production is socially stimulated and that at the group level, meerkats avoid overlap, thus fulfilling a key principle of turn-taking [8]. Through observational data and playback experiments, we show that these group-level patterns arise from two individual-level rules: call inhibition over short timescales, which prevents mutual interference, and call excitation over longer timescales, which stimulates further group calling. These simple rules suggest that hierarchy formation and turn allocation are not required for achieving group-wide coordination of communication. We also suggest that the potential bonding function of turn-taking shown in humans might have similar effects in animal interactions. VIDEO ABSTRACT.