Olfactory discrimination of anal sac secretions in the domestic cat and the chemical profiles of the volatile compounds

Scent emitted from anal sac secretions provides important signals for most Carnivora. Their secretions emit a variety of volatile compounds, some of which function as chemical signals with information about the scent owners. The domestic cat has a pair of anal sac glands to secrete a pungent liquid. Their anal sac secretions may give information about sex, reproductive state, and recognition of individuals. However, little is known about the volatile compounds emitted from anal sac secretions and their biological functions in cats. In this study, we examined the volatile chemical profiles of anal sac secretions in cats and their olfactory ability to discriminate intraspecific anal sac secretions. Analysis with gas chromatography–mass spectrometry showed that the major volatile compounds were short-chain free fatty acids, whose contents varied among individuals, as well as other carnivores. There was no sex difference in the volatile profiles. In temporal analyses of individual anal sac secretions performed 2 months apart, the profiles were highly conserved within individuals. Habituation–dishabituation tests showed that cats can distinguish individual differences in the odor of anal sac secretions. These results suggest that cats utilize short-chain free fatty acids emitted from anal sac secretions to obtain scent information for individual recognition rather than species or sex recognition.     

Molecular phylogeny of the Herpestidae (Mammalia, Carnivora) with a special emphasis on the Asian Herpestes

Until now, phylogenetic studies of the mongooses (Carnivora, Herpestidae) have not included an exhaustive sampling of the Asian members of this family. In this study, we used mitochondrial (Cytochrome b and ND2), nuclear (β-fibrinogen intron 7 and Transthyretin intron 1) sequences from almost all of the recognized mongoose species to produce a well-resolved phylogeny of the Herpestidae. We also performed molecular dating analyses to infer divergence dates of the different lineages within the Herpestidae. Our results confirmed the paraphyly of the Herpestes genus and other phylogenetic relationships, which previously had only been moderately supported. The Asian herpestid species were found to form a monophyletic group within the Herpestidae. Within the Asian species, a cyto-nuclear conflict was discovered between the small Indian mongoose (Herpestes auropunctatus), the Indian gray mongoose (Herpestes edwardsii) and the Javan mongoose (Herpestes javanicus), which may have occurred through interspecific hybridization. This study inferred an Early Miocene origin for the Herpestidae and a Middle Miocene origin for the Asian mongooses.     

Systematic status and biogeography of the Javan and small Indian mongooses (Herpestidae, Carnivora)

The Javan and small Indian mongooses, ranging from the Middle East to South-east Asia, are considered as two species or as a single species, varying in size and colour from west to east. In order to clarify their systematic status and to define the limits of their ranges, Cytochrome b sequences were obtained from 27 specimens, and localities of 392 specimens from museum collections were determined. The phylogenetic analyses revealed that the Javan and Small Indian mongooses grouped in two separate clades with their range limits located in Myanmar. The Javan mongoose is in fact closer to the grey mongoose than to the small Indian mongoose.     

Spatial ecology of white-tailed mongoose in farmland in the Ethiopian Highlands

The spatial ecology of the white‐tailed mongoose Ichneumia albicauda was studied during November 1998 to February 2000 on farmland adjacent to the Bale Mountains National Park in southern Ethiopia. Four male and one female white‐tailed mongooses were captured and radiotagged. The average range size was 3.2 km² for three adult males and 2.6 km² for the female which is larger than previously recorded in savannah habitat. Asymptotic range size was reached at approximately 50 locations for the males and twenty locations for the female. The ranges of the three adult male mongooses overlapped on average only 2% whereas the single female range overlapped with two adjacent males by 81 and 25%, respectively. Twenty per cent of mongoose sightings were of groups that consisted of a male and female. Diurnal resting sites were found amongst rocks or in empty buildings. The mongooses foraged on grassy areas within woodland and bush during nocturnal activity periods. We conclude that white‐tailed mongoose social organization in this agricultural landscape was similar to other solitary mongooses and was characterized by a mosaic of exclusive male ranges overlapping a separate mosaic of smaller female ranges.     

Relationships between capture-site characteristics and capture levels of the invasive mongoose on Amami-Oshima Island,Japan

We used a generalized linear model (GLM) to investigate environmental characteristics of capture sites of the invasive small Indian mongoose (Herpestes auropunctatus) on Amami Island, Japan. Data were collected from 2002 to 2011, from an area with the lowest mongoose density. Data on capture levels and environmental factors were obtained within 1 × 1 km grid cells. In addition, we developed an evaluation map that predicts the occurrence of mongooses throughout the island by extrapolating the 2011 results, in which the last mongoose appearance was confirmed. We found that environmental characteristics of capture sites drastically changed during the final stage of the eradication project. From 2002 to 2010, mongooses were captured in grid cells with many gentle ridges. In 2011, when mongoose density became exceedingly low, mongooses seem to have survived in the grid cells with abundant steep ridges, where it was difficult to establish traps. Therefore, environmental factors affected capture levels and the density of the mongoose population. The evaluation map predicts that mongooses could survive on the southwest and southeast island peninsulas. This evaluation map will be helpful in allocating limited labor and financial resources toward the most effective capture strategies. This study suggests that an analysis of pest management data is an important step in the eradication of mongooses. Our results can contribute to long-term projects in invasive pest management not only for the mongoose population on Amami Island, but also for other invasive species globally.     

Systematics of the Southeast Asian mongooses (Herpestidae,Carnivora): solving the mystery of the elusive collared mongoose and Palawan mongoose

Although recent molecular studies have clarified the phylogeny of mongooses, the systematics of the Southeast Asian species was incomplete as the collared mongoose Urva semitorquata and some debatable taxa (Hose's mongoose, Palawan mongoose) were missing in the analyses. We sequenced three mitochondrial (cytochrome b, ND2, control region) and one nuclear (beta‐fibrinogen intron 7) fragments of the Southeast Asian mongooses to clarify the systematic position of the different species and populations occurring in this region. Our results showed that the collared mongoose is closely related to the crab‐eating mongoose Urva urva, these two species forming a sister‐group to the short‐tailed mongoose Urva brachyura. Despite Sumatran collared mongooses having a peculiar orange phenotype, we showed that they exhibited very little genetic divergence to individuals from Borneo. In contrast, the populations of the short‐tailed mongoose from Borneo were strongly divergent to those from Peninsular Malaysia and Sumatra, and these might represent separate species. Within the crab‐eating mongoose, we observed little geographical genetic structure. Our study suggests that Hose's mongoose is not a valid species. The Palawan mongooses did not cluster with the other populations of the short‐tailed mongoose; they were closer to the collared mongoose and should be included in this species. © 2014 The Linnean Society of London     

Highly variable microsatellite loci for studies of introduced populations of the small Indian mongoose (Herpestes javanicus)

During their introduction, non‐native species typically undergo founder events that reduce genetic variation. To allow a high‐resolution genetic investigation of introduced populations of the small Indian mongoose (Herpestes javanicus), we developed primers for nine variable microsatellite loci. Their applicability was assessed in 10 mongooses from the large Fijian population, which originated from a single pair from Calcutta, India. The number of alleles ranged from two to five per locus, possibly as a result of preservation of initial variability and in situ mutations during the rapid population expansion after introduction.     

The Asian grass lizard (Takydromus sexlineatus) does not respond to the scent of a native mammalian predator

Lacertid lizards use chemical cues emitted by saurophagous snakes to evade predation. Whether these lizards can detect and respond to the chemical cues of predatory mammals has not been studied. As many mammals carry distinct body odours and/or use chemical cues for intraspecific communication, lizards can be expected to use these chemicals as early warning cues. To test this idea, we observed the behaviour of Asian grass lizards (Takydromus sexlineatus) that had been transferred to an unfamiliar test arena containing one of four scent treatments. No particular scent was applied to the arena in the control situation. Diluted aftershave served as a pungency control. In the snake treatment, scent of the Oriental whip snake (Ahaetulla prasina) was applied. We included this treatment to learn how Asian grass lizards react to predator chemical cues. Finally, in the mongoose treatment, the lizards were confronted with scent cues of several small Indian mongooses (Herpestes auropunctatus). Snake scent elicited foot shakes, startles and tail vibrations. These are behaviours that in lacertid lizards are associated with stressful situations such as predatory encounters. Surprisingly, lizards confronted with mongoose scent exhibited none of these stress-indicating behaviours. In fact, their behaviour did not differ from that of lizards subjected to an odourless control treatment. These results raise concern. Mongooses are rapidly invading ecosystems worldwide. If lizards that have co-evolved with mongooses are unable to detect these predators’ presence through chemical cues, it seems highly unlikely that evolutionary naïve lizards will develop this ability rapidly.     

Conservation implications of small Indian mongoose (<Emphasis Type="Italic">Herpestes auropunctatus</Emphasis>) predation in a hotspot within a hotspot: the Hellshire Hills,Jamaica

This study documents impacts of the small Indian mongoose (Herpestes auropunctatus) on a threatened endemic fauna occurring in a biodiversity hotspot within a hotspot, the Hellshire Hills, Jamaica. We analyzed the stomach contents of 217 mongooses and supplemented this information with behavioural observations. The mongoose’s diet consists primarily of invertebrates and lizards, but bird feathers, mammal hair, and a small number of seeds were also recorded. Invertebrates and lizards accounted for 93% of identified prey items. Of special concern were the remains of threatened species such as the recently re-discovered blue-tailed galliwasp (Celestus duquesneyi), indicating that the mongoose may represent a considerable threat to this poorly known taxon. Dietary analyses did not reveal remains of the Critically Endangered Jamaican iguana (Cyclura collei), yet field observations confirmed that the mongoose is a potent predator of hatchling iguanas. Ignoring issues of sample size, this suggests that the analysis of stomach contents alone may mask important demographic impacts attributable to the mongoose (or other predator species). In other words, rare and endangered species may not be detected in diet samples, but the impact of predation may be of demographic significance for effected prey taxa. This study supports previous arguments concerning the negative impact of the mongoose on endemic insular species, and underscores the utility of employing field observations of mongoose foraging behaviour to provide important insights into the conservation implications of predation by non-native predators.     

Eradication of the mongoose is crucial for the conservation of three endemic bird species in Yambaru,Okinawa Island,Japan

Okinawa Island, Japan, is a globally important biodiversity hotspot. Three endemic bird species, Okinawa rail (Hypotaenidia okinawae), Okinawa woodpecker (Dendrocopos noguchii), and Okinawa robin (Larvivora namiyei), are found only in the Yambaru region of the northern part of Okinawa Island. In order to conserve endemic species, it is important to determine the effect of alien species on endemic species. We conducted playback surveys four times every three years from 2007 to 2016 to evaluate the recent distribution of these three forest-dwelling bird species during the breeding season. Then, the association between the numbers of detections of these three species with the invasive mongoose density and the hardwood forest area was evaluated with a generalized additive mixed model (GAMM). The results showed that the distribution areas of these bird species have been recovering since the 2007 within the small Indian mongoose (Urva auropunctata) controlled area. The GAMM results showed that these bird species were abundant in areas with fewer small Indian mongooses and larger areas of hardwood forests. Thus, the mongoose had a negative impact not only on the flightless rails but also on the woodpeckers and the robins. In recent years, most of the old-growth forests have been designated as protected forests, and large-scale logging is no longer taking place in Yambaru. Eradication of the mongoose is particularly important for the conservation of these three endemic bird species.

     

Evaluation of the palatability and toxicity of candidate baits and toxicants for mongooses (<Emphasis Type="Italic">Herpestes auropunctatus</Emphasis>)

The small Indian mongoose (Herpestes auropunctatus) is an invasive pest species responsible for damage to native avian, reptile, and amphibian species on Hawaii, Croatia, Mauritius, and several Caribbean Islands, among other regions. Mongoose control has been pursued through a variety of means, with varying success. One toxicant, diphacinone, has been shown to be effective in mongooses and is co-labeled in a rodenticide bait for mongoose control in Hawaii; however, preliminary observations indicate low performance as a mongoose toxicant due likely to poor consumption. We evaluated the efficacy and palatability of 10 commercial rodenticide baits, technical diphacinone powder, and two alternative acute toxicants against mongooses in laboratory feeding trials. We observed poor acceptance and subsequent low overall mortality, of the hard grain-based pellets or block formulations typical of most of the commercial rodenticide baits. The exception was Tomcat® bait blocks containing 0.1% bromethalin, an acute neurotoxin, which achieved up to 100% mortality. Mortality among all other commercial rodenticide formulations ranged from 10 to 50%. Three-day feedings of 0.005% technical diphacinone formulated in fresh minced chicken achieved 100% mortality. One-day feedings of para-aminopropiophenone (PAPP), a chemical that reduces the oxygen-carrying capacity of the blood, achieved 100% mortality at concentrations of 0.10 to 0.15%. Bait acceptance of two sodium nitrite formulations (similar toxic mode of action as PAPP) was relatively poor, and mortality averaged 20%. In general, commercially produced rodenticide baits were not preferred by mongooses and had lower mortality rates compared to freshly prepared meat bait formulations. More palatable baits had higher consumption and achieved higher mortality rates. The diphacinone bait registered for rat and mongoose control in Hawaii achieved 20% mortality and was less effective than some of the other commercial or candidate fresh bait products evaluated in this study.     

The Phylogeography of Rabies in Grenada,West Indies,and Implications for Control

In Grenada, West Indies, rabies is endemic, and is thought to be maintained in a wildlife host, the small Indian mongoose (Herpestes auropunctatus) with occasional spillover into other hosts. Therefore, the present study was undertaken to improve understanding of rabies epidemiology in Grenada and to inform rabies control policy. Mongooses were trapped island-wide between April 2011 and March 2013 and examined for the presence of Rabies virus (RABV) antigen using the direct fluorescent antibody test (dFAT) and PCR, and for serum neutralizing antibodies (SNA) using the fluorescent antibody virus neutralization test (FAVN). An additional cohort of brain samples from clinical rabies suspects submitted between April 2011 and March 2014 were also investigated for the presence of virus. Two of the 171 (1.7%) live-trapped mongooses were RABV positive by FAT and PCR, and 20 (11.7%) had SNAs. Rabies was diagnosed in 31 of the submitted animals with suspicious clinical signs: 16 mongooses, 12 dogs, 2 cats and 1 goat. Our investigation has revealed that rabies infection spread from the northeast to the southwest of Grenada within the study period. Phylogenetic analysis revealed that the viruses from Grenada formed a monophyletic clade within the cosmopolitan lineage with a common ancestor predicted to have occurred recently (6–23 years ago), and are distinct from those found in Cuba and Puerto Rico, where mongoose rabies is also endemic. These data suggest that it is likely that this specific strain of RABV was imported from European regions rather than the Americas. These data contribute essential information for any potential rabies control program in Grenada and demonstrate the importance of a sound evidence base for planning interventions.     

A computational investigation of sulfur-containing heterocyclic components from the anal sac secretions of Mustela species

A computational investigation of the sulfur-containing heterocyclic components (substituted thietanes and 1,2-dithiolanes) of Mustela anal sac secretions has been carried out. A cluster analysis of the chemical compositions of Mustela anal sac volatiles reveals little similarity with established phylogenetic relationships between members of the genus. Ab initio calculations [MP2/6–311++G(2df,2p)//B3LYP/6–311++G**] show the lowest-energy C₅H₁₀S isomeric thietane to be 2,2-dimethylthietane, which is also the most abundant of the Mustela thietanes. Similarly, 3,3-dimethyl-1,2-dithiolane is the lowest-energy C₅H₁₀S₂ compound. 2-n-Propylthietane is the highest-energy C₆H₁₂S compound, but the most abundant Mustela C₆H₁₂S compound produced, whereas cis-2-ethyl-4-methylthietane, the lowest-energy C₆H₁₂S thietane, has never been observed in Mustela anal sac secretions. A molecular docking analysis of the Mustela sulfur-containing heterocycles into both porcine and bovine odorant binding proteins reveals the interactions of the docked ligands with the proteins to be largely hydrophobic, and have binding energies generally lower than typical odorant molecules such as linalool or eugenol. Figure Mustela anal sac volatile components, 2,2-dimethylthietane and cis-3,4-dimethyl–1,2-dithiolane.     

An olfactory recognition system in the ferret Mustela furo L. (Carnivora: Mustelidae)

This study demonstrates that ferrets can use variations in odours from anal sac secretions as a communication system. Odour preference tests showed that ferrets can discriminate between male and female ferret anal sac odours, between strange and familiar, familiar and their own, and fresh and 1-day-old odours. They did not discriminate between fresh and 2-h-old odours, nor did male ferrets discriminate between the odours of oestrous and anoestrous females. Ferrets were more attracted to the odours of the opposite sex than to those of their own sex. When faced by an opponent, male ferrets were more aggressive in the presence of their own rather than their opponent's odour, and less aggressive with their opponent's odour than with that of a known, dominant animal's odour. These results are consistent with both a sex attraction role and a territorial defence role for anal sac odours. A scent-matching mechanism for territorial defence is supported, although a neighbour-neighbour recognition/avoidance mechanism cannot be rejected. Gas chromatography revealed sexually and individually distinct profiles of volatile compounds in anal sac extracts, but no consistent seasonal trends. Females had high concentrations of 2,3-dimethylthietane and/or 3,4-dimethyl-1,2-dithiolane. Males usually had high concentrations of indole. 2-Propylthietane was an important constituent in most individuals. These differences in concentration were significant and could provide an olfactory recognition system of sex and individual identity.     

Putative chemosignals of the ferret (Mustela furo) associated with individual and gender recognition

Quantitative stir bar sorptive extraction methods, both in the aqueous and headspace modes, followed by thermal desorption gas chromatography-mass spectrometry were used to investigate individual variations in the volatile components of male and female ferret (Mustela furo) urine. The urinary profiles were further compared with volatile profiles of anal gland secretions of breeding male and female ferrets. Thirty volatile compounds were quantified in male and female urine. Among them, 2-methylquinoline was unique to male urine. Four ketones (4-heptanone, 2-heptanone, o-aminoacetophenone, and a dimethoxyacetophenone) and several nitrogen compounds (e.g., 2,5-dimethylpyrazine, quinoline, 4-methylquinazoline) and low levels of three unidentified nonsulfur compounds were significantly more abundant in males than in females. Quantitative comparison of 30 volatile urinary compounds showed several statistically significant differences between the sexes and individuals of the same sex. These findings suggest that ferrets may use urine marking for sex and individual recognitions. Ten of the 26 compounds identified in anal gland secretions from females and males were also found in urine. However, most of the major compounds (thietanes, dithiolanes, and indole) in anal glands were not present in urine. This suggests that urine may convey specific signals that differ from those of anal glands. Additionally, 10 volatiles (two aldehydes, five ketones, benzothiazole, 2-methylquinoline, and 4-methylquinazoline), not previously identified, were found in ferret anal gland secretions. Among the new compounds, o-aminoacetophenone was found only in males, while only traces of this compound were found in females. Similar results were previously obtained in anal glands of three other Mustela species. These findings provide new information about the constituents of urine and volatile components of anal gland secretions in ferrets.     

Identification of volatile compounds from fungus-infected date fruit that stimulate upwind flight in femaleEctomyelois ceratoniae

Four volatile compounds emitted from fungus-infected date fruit,Phoenix dactylifera L., were identified using coupled gas chromatographic-electroantennographic recordings, coupled gas chromatographic-mass spectrometric analysis, electroantennographic assays of synthetic standards, and wind tunnel bioassays. These compounds were ethyl hexanoate, ethanol, acetaldehyde, and 2-phenylethanol. Wind tunnel bioassays showed that ethyl hexanoate was capable of stimulating upwind flight and landing on the source by mated female carob moths,Ectomyelois ceratoniae (Zeller). Addition of both ethanol and acetaldehyde to ethyl hexanoate resulted in an increase in attraction to a level similar to that found for date fruits. No such effect was noted for additions of 2-phenylethanol at the dosages tested. In this study, it appears that ethyl hexanoate is a dominant olfactory stimulant and attractant for mated female carob moths, and represents a novel compound with regard to previously identified lepidopteran host odor attractants.     

Do not feed the wildlife: associations between garbage use,aggression, and disease in banded mongooses (Mungos mungo)

Urbanization and other human modifications of the landscape may indirectly affect disease dynamics by altering host behavior in ways that influence pathogen transmission. Few opportunities arise to investigate behaviorally mediated effects of human habitat modification in natural host–pathogen systems, but we provide a potential example of this phenomenon in banded mongooses (Mungos mungo), a social mammal. Our banded mongoose study population in Botswana is endemically infected with a novel Mycobacterium tuberculosis complex pathogen, M. mungi, that primarily invades the mongoose host through the nasal planum and breaks in the skin. In this system, several study troops have access to human garbage sites and other modified landscapes for foraging. Banded mongooses in our study site (N = 4 troops, ~130 individuals) had significantly higher within‐troop aggression levels when foraging in garbage compared to other foraging habitats. Second, monthly rates of aggression were a significant predictor of monthly number of injuries in troops. Finally, injured individuals had a 75% incidence of clinical tuberculosis (TB) compared to a 0% incidence in visibly uninjured mongooses during the study period. Our data suggest that mongoose troops that forage in garbage may be at greater risk of acquiring TB by incurring injuries that may allow for pathogen invasion. Our study suggests the need to consider the indirect effects of garbage on behavior and wildlife health when developing waste management approaches in human‐modified areas.     

Banded mongooses avoid inbreeding when mating with members of the same natal group

Inbreeding and inbreeding avoidance are key factors in the evolution of animal societies, influencing dispersal and reproductive strategies which can affect relatedness structure and helping behaviours. In cooperative breeding systems, individuals typically avoid inbreeding through reproductive restraint and/or dispersing to breed outside their natal group. However, where groups contain multiple potential mates of varying relatedness, strategies of kin recognition and mate choice may be favoured. Here, we investigate male mate choice and female control of paternity in the banded mongoose (Mungos mungo), a cooperatively breeding mammal where both sexes are often philopatric and mating between relatives is known to occur. We find evidence suggestive of inbreeding depression in banded mongooses, indicating a benefit to avoiding breeding with relatives. Successfully breeding pairs were less related than expected under random mating, which appeared to be driven by both male choice and female control of paternity. Male banded mongooses actively guard females to gain access to mating opportunities, and this guarding behaviour is preferentially directed towards less closely related females. Guard–female relatedness did not affect the guard's probability of gaining reproductive success. However, where mate‐guards are unsuccessful, they lose paternity to males that are less related to the females than themselves. Together, our results suggest that both sexes of banded mongoose use kin discrimination to avoid inbreeding. Although this strategy appears to be rare among cooperative breeders, it may be more prominent in species where relatedness to potential mates is variable, and/or where opportunities for dispersal and mating outside of the group are limited.     

黄鼬肛腺分泌物的挥发性成分

利用顶空取样、溶剂解吸附和气质联用技术分析了黄鼬（Mustela sibirica)肛腺分泌物的挥发性成分。鉴定出的六种化合物均为含硫的环状有机物：（1）2,2－二甲基硫代环丁烷;（2）顺或反2,4－二甲基硫代环丁烷;（3）反－2,3－二甲基硫代环丁烷;（4）2－乙基硫代环丁烷;（5）2－丙基硫代环丁烷;（6）3,3－二甲基－1,2－二硫代环戊烷。尽管黄鼬肛腺成分的组成和鼬鼠其它种存在很大的相似性,但是成分组成的种间差异很明显。另外,2－乙基硫代环丁烷仅存在于雌性黄鼬中。很多研究已经证明对鼠类有驱赶作用的2,2－二甲基硫代环丁烷和2－丙基硫代环丁烷在黄鼬肛腺分泌物同时存在,说明黄鼬肛腺分泌物对鼠类可能有很强的驱避作用。     

Molecular systematics and origin of sociality in mongooses (Herpestidae, Carnivora)

The Herpestidae are small terrestrial carnivores comprising 18 African and Asian genera, currently split into two subfamilies, the Herpestinae and the Galidiinae. The aim of this work was to resolve intra-familial relationships and to test the origin of sociality in the group. For this purpose we analysed sequences of the complete cytochrome b gene for 18 species of Herpestidae. The results showed that the mongooses were split into three clades: (1) the Malagasy taxa (Galidiinae and Cryptoprocta), (2) the true social mongooses and (3) the solitary mongooses, each group being also supported by morphological and chromosomal data. Our results suggested unexpected phylogenetic relationships: (1) the genus Cynictis is included in the solitary mongoose clade, (2) the genera Liberiictis and Mungos are sister-group, and (3) the genus Herpestes is polyphyletic. We examined the evolution of the sociality in mongooses by combining behavioural traits with the cytochrome b data. Some of the behavioural traits provided good synapomorphies for characterizing the social species clade, showing the potential benefit of using such characters in phylogeny. The mapping of ecological and behavioural features resulted in hypothesizing solitary behavior and life in forest as the conditions at the base of the mongoose clade.