Microbes and animal olfactory communication: Where do we go from here?

We know that microbes contribute to the production of odors that some animals use to communicate, but how common is this phenomenon? Recent studies capitalizing on new molecular technologies are uncovering fascinating associations between microbes and odors of wild animals, but causality is difficult to ascertain. Fundamental questions about the nature of these unique host-microbe interactions also remain unanswered. For instance, do microbes benefit from signaling associations with hosts? How does microbial community structure influence signal production? How do hosts regulate microbes in order to generate appropriate signals? Here, we review the current state of knowledge on microbially produced signals in animals and discuss key research foci that can advance our understanding of microbial-based signaling in the animal world.

Odour dialects among wild mammals.

Across multiple taxa, population structure and dynamics depend on effective signalling between individuals. Among mammals, chemical communication is arguably the most important sense, underpinning mate choice, parental care, territoriality and even disease transmission. There is a growing body of evidence that odours signal genetic information that may confer considerable benefits including inbreeding avoidance and nepotism. To date, however, there has been no clear evidence that odours encode population-level information in wild mammals. Here we demonstrate for the first time the existence of 'odour dialects' in genetically distinct mammalian subpopulations across a large geographical scale. We found that otters, Lutra lutra, from across the United Kingdom possess sex and biogeography-specific odours. Subpopulations with the most distinctive odour profiles are also the most genetically diverse but not the most genetically differentiated. Furthermore, geographic distance between individuals does not explain regional odour differences, refuting other potential explanations such as group odour sharing behaviour. Differences in the language of odours between subpopulations have the potential to affect individual interactions, which could impact reproduction and gene-flow.

[Unknown hepatoid glands of some species of cats and deer]. / Neizvestnye gepatoidnye zhelezy nekotorykh koshach'ikh i olen'ikh.

Our histological description of the fourth type of mammalian skin glands--hepatiod glands--allowed us to revise the obtained and published data mistaking the alveolar glands of the anal sacs in cats and the limb glands in deers as sebaceous. Large clusters of hepatiod glands were discovered in the anal sacs of the cat, lynx, and tiger, interdigital gland of elk, and the tarsal gland of reindeer. These glands secrete considerable amounts of protein to the clearance of the intercellular canaliculi and contain hydrophobic lipids. The available data substantiate revision of the data on the structure of many skin glandular organs with atypical sebaceous glands.

Behavioral, ultrastructural and chemical studies on the honeydew and waxy secretions by nymphs and adults of the Asian citrus psyllid Diaphorina citri (Hemiptera: Psyllidae).

The Asian citrus psyllid (ACP), Diaphorina citri (Hemiptera: Psyllidae) is the primary vector of the bacterium causing citrus huanglongbing (citrus greening), the most serious disease of citrus worldwide. Psyllids and other hemipterans produce large amounts of honeydew, which has been used previously as an indicator of phloem sap composition and insect feeding or metabolism. Behavioral, ultrastructural and chemical studies on ACP, its honeydew and waxy secretions showed important differences between nymphs, males and females, and suggested some mechanisms by which the psyllids, especially nymphs and adult females, can minimize their contamination with honeydew excretions. The anal opening in ACP, near the posterior end of the abdomen, is on the ventral side in nymphs and on the dorsal side in adult males and females. Video recordings showed that adult males produce clear sticky droplets of honeydew gently deposited behind their body on the leaf surface, whereas adult females produce whitish honeydew pellets powerfully propelled away from the female body, probably to get their excretions away from eggs and newly hatched nymphs. ACP nymphs produce long ribbons or tubes of honeydew that frequently stay attached to the exuviae after molting, or drop when feeding on the lower side of citrus leaves. Furthermore, honeydew excretions of both nymphs and adult females are covered with a thin layer of whitish waxy material ultrastructurally composed of a convoluted network of long fine filaments or ribbons. This material is extruded from intricate arrays of wax pores in the circumanal ring (around the anus) that is found in nymphs and females but not in males of ACP or other psyllid species. Infrared microscopy and mass spectroscopy revealed that, in addition to various sugars, honeydew excretions of ACP nymphs and females are covered with a thin layer of wax similar in profile to ester waxes.

Histochemical characteristics of the anal sacs of the cat.

The histochemistry of polysaccharides and proteins and the distribution of RNA were investigated in the glands and mature secretion of the anal sacs of the cat. Glycogen was extremely abundant in the epithelial lining of the lumen and efferent duct of the anal sac and also in ducts of sebaceous glands of the sacs constantly formed in the place of degenerating acini. Little glycogen was found in the unchanged sebaceous acini. The apocrine glands of the anal sacs were substantially richer in glycogen than the apocrine sweat glands of the skin and were in an active state. A high concentration of acid mucopolysaccharides was present in the mature secretion, and their source was the apocrine glands. The phases of the secretory cycle alternated in different cells and secretory portions of the apocrine glands highly asynchronously. Carboxylated acid mucopolysaccharides were more abundant than sulfated. Sialomucin, hyaluronic acid, and chondroitin sulfate could be identified in the secretion. Neutral and acid mucopolysaccharides were present in the mature secretion in the form of complexes with one another in approximately equal proportions; neutral polysaccharides consisted chiefly of glycogen. Besides polysaccharides, the apocrine glands produce large quantities of protein, in which the mature secretion was rich. This protein was predominantly basic, and the secretion contained very little acid protein. Maturing cells of the sebaceous acini, and also other specific sebaceous glands, were characterized by a much higher protein concentration than in ordinary sebaceous glands.

Differential activation of glomeruli in the ferret's main olfactory bulb by anal scent gland odours from males and females: an early step in mate identification.

Peripheral anosmia was previously found to disrupt sex discrimination and partner preference in male and female ferrets. Here we show directly that volatile anal scent gland odourants from male and female ferrets activated overlapping but distinguishable clusters of glomeruli located in the ventral-caudal portion of the main olfactory bulb (MOB) of breeding ferrets of both sexes. No glomerular activation was seen in the accessory olfactory bulb (AOB). The profile of MOB glomerular activation induced in oestrous females by male anal scents was very similar to that induced by direct contact with a male during mating, and oestrogen treatment failed to alter the profile of glomerular activation induced in ovo-hysterectomized females by male anal scents. In rodents, 'atypical' MOB glomeruli, which have dense acetylcholinesterase (AChE) activity in the neuropil, may be activated by body odours from conspecifics. No such AChE-staining 'atypical' glomeruli were found in the ferret's MOB, suggesting that in this carnivore they do not constitute a subset of MOB glomeruli that respond to body odourants. In ferrets of both sexes, volatile body odourants that are detected by the main as opposed to the vomeronasal-AOB accessory olfactory system may play a critical role in mate identification.

Possible coding for recognition of sexes, individuals and species in anal gland volatiles of Mustela eversmanni and M. sibirica.

With a combination of solvent extraction and gas chromatography-mass spectrometry, we found eight new compounds in the two sympatric Mustela species, M. eversmanni and M. sibirica. These compounds had not been detected by headspace sampling with solvent desorption. Two of the newly detected compounds are nitrogen-containing compounds, indole and o-aminoacetophenone and the remaining are sulfur-containing volatiles. By comparing same and opposite sexes between the two Mustela species, we found that qualitative differences in the anal gland secretion are most likely to be used to code for information about species, corresponding to the idea of digital coding. In the Siberian weasel (M. sibirica), both presence or absence of sex-specific compounds (Z-2-ethyl-3-methylthietane only in females) and relative abundance of some compounds between males and females could be used to code for information about sex, corresponding to the idea of digital and analog coding, respectively. In the steppe polecat (M. eversmanni), only quantitative differences provided the possibility for inter-sexual communication. Thus coding for information about sex appeared to be digital. Coding for individual information could also be either digital or analog or both through the presence or absence of certain compounds and/or the difference in the relative abundances of certain compounds among individuals. Comparing with other Mustela spp., we failed to find a congruence between the chemical composition of anal gland secretions and the phylogenetic relationship among the species in this genus.

Differences among antimicrobial properties of carrion beetle secretions reflect phylogeny and ecology.

Carrion beetles (Coleoptera: Silphidae) consist of two subfamilies in North America. Members of the Silphinae arrive at carcasses during the mid-stage of decay and their larvae feed on developing maggots, while members of the Nicrophorinae bury and tend carcasses upon which their developing larvae feed. The Nicrophorinae maintain the condition of the carcass by applying oral and anal secretions that reduce carcass decay apparently through bacterial inhibition, although quantification has not been made. We hypothesized that enzymes in the oral and anal secretions of the subfamily Nicrophorinae would inhibit bacterial growth, while secretions from the subfamily Silphinae would not. The secretions were assayed for inhibitory effects with a Microtox Analyzer that monitors the decrease in bioluminescence from the bacterium Vibrio fischerii. We found a significant difference of bioluminescence in the control compared to secretions of 8 out of 10 tested Nicrophorinae (with oral secretions being most active), while only anal secretions from Necrodes surinimensis of the Siphinae significantly reduced bacterial survival. These data follow the known phylogenic relationship in which Necrodes is the closest genus to the Nicrophorinae. The two species of Nicrophorinae, which did not show significant reductions in bacterial growth, differ ecologically from the others. Thus, the presence of antimicrobial compounds in most Nicrophorinae secretions, but not in most other Silphinae, represents an adaptation to preserve the buried carcass.