The Ecological Significance of Aphid Cornicles and Their Secretions

Aphid cornicles are abdominal appendages that secrete an array of volatile and nonvolatile compounds with diverse ecological functions. The emission of alarm pheromones yields altruistic benefits for clone-mates in the aphid colony, which is essentially a superorganism with a collective fate. Secreted droplets also contain unsaturated triglycerides, fast-drying adhesives that can be lethal when smeared on natural enemies but more often impede their foraging efficiency. The longest cornicles have evolved in aphids that feed in exposed locations and are likely used to scent-mark colony intruders. Reduced cornicles are associated with reliance on alternative defenses, such as the secretion of protective waxes or myrmecophily. Root-feeding and gall-forming lifestyles provide protected feeding sites and are associated with an absence of cornicles. In some eusocial gall-formers, soldier morphs become repositories of cornicle secretion used to defend the gall, either as menopausal apterae that defend dispersing alatae or as sterile first instars that dispatch predators with their stylets and use cornicle secretions as a construction material for gall repair. Collectively, the evidence is consistent with an adaptive radiation of derived cornicle functions molded by the ecological lifestyle of the aphid lineage.

Meadow voles differentiate between scents of different sources

Scent marks are an important means of transmitting information between rodents, and they can be produced from several body sources. Previous studies have shown that scents from multiple sources can convey the same information; female meadow voles, for example, have three scent sources that communicate sex. However, possessing three separate sources that convey the same information is likely costly due to the metabolic energy required to produce these signals and the increased chance that eavesdropping individuals may intercept information present in these signals. In this study, we investigated if these scent sources could communicate other information, in addition to scent donor sex, by determining if male meadow voles could distinguish scent marks taken from different sources of a single female scent donor. This was accomplished with a habituation-test method, that allowed us to compare how male meadow voles differently investigate scent from a familiar and novel source of a female scent donor. Male meadow voles could distinguish between faeces and urine scent marks of a female, but could only distinguish mouth from urine and faeces scent marks when first familiarized with mouth scent marks. Our findings suggest that mouth, urine, and faeces scent marks of female meadow voles produce both redundant and distinct information. The overlap in information between scent marks produced from separate sources may be needed to provide social context, which allows receiving individuals to accurately weigh the tradeoffs associated with responding to an olfactory cue. While this overlap in information remains costly, this cost may be minimized by the different fade-out times of scent marks from distinct body sources, which may limit the amount of time information in a scent mark is available to a time period where this information is socially relevant.

Ontogeny of scent marking behaviours in an apex carnivore

Puma (Puma concolor) communication with conspecifics is via indirect scent marking behaviours that are important for individuals to advertise their territory and reproductive status, but little is known about how the behaviours develop with age. To examine the development of scent marking behaviours, we monitored the behaviours of adult pumas and dependent kittens. Based on video recordings, we found that the frequency of puma communication behaviours significantly changed over time. Kittens exhibited olfactory investigation more frequently as they aged, but kittens generally did not exhibit scent marking behaviours. Kittens travel with their mothers until they disperse, so there is no need to establish territories or advertise availability to mate, but kittens are at risk of injury or mortality from other pumas. It is possible that there is no functional need for dependent kittens to scent mark until they mature, but there is a need for frequent use of investigative behaviours.

Modelling the effects of the repellent scent marks of pollinators on their foraging efficiency and the plant-pollinator community

Pollinator insects forage in complex and unpredictable resource landscapes, often using social information from congeneric individuals to acquire knowledge about their environment. It has long been recognized that this process allows them to exploit floral resources more efficiently and thus increase individual fitness. However, by creating correlations between the behaviors of pollinators within a population, this could also indirectly influence the entire plant-pollinator community. One type of social information used by pollinators is the scent mark left on the corolla of flowers by previous visitors, which can be used as a cue to avoid recently depleted resources. We developed a spatially explicit agent-based model to examine the effects, at both individual and community levels, of pollinators using these scent marks. The model simulates a population of pollinators foraging on flowers in a continuous 2D space in which we can vary the density of pollinators. We showed that the use of scent marks as a source of information significantly increased the foraging efficiency of pollinators except when competition between pollinators was very low. At the community level, this also resulted in a marked homogenization between floral resources within the landscape: in the absence of scent marks, the coefficient of variation of the remaining nectar quantity per flower strongly increased with greater pollinator competition, but it remained low at all levels of competition when scent marks were used by the pollinators. Finally, the use of scent marks markedly decreased the number of pollinator flower visits, especially at high levels of pollinator competition, which can potentially reduce the pollination service.

Sociality and signaling activity modulate information flow in river otter communication networks

Animal communication networks are built from interactions between senders and receivers of signals. The drivers of signaling decisions, which are the building blocks of such networks, are not well understood. Theory predicts that conditions which ensure information spread to the largest possible number of receivers should be favored. Several carnivores use latrine sites for visual, olfactory, and auditory signaling. We tested the hypotheses that signaling behavior at latrine sites is influenced by social structure and locally acquired information on the presence of conspecifics, using coastal river otters (Lontra canadensis), in Alaska. River otters exhibit a flexible social system of mostly males that communicate through scent marking at latrines. During scent marking, river otters also perform feet stomping, which may add a visual component to their signal. Using trail camera footage, we found that solitary otters were more likely to perform both sniffing and scent marking compared with otters in groups. Feet stomping was more intense for solitary otters but less pronounced during overmarking. Signalers demonstrated a greater tendency to scent mark when in smaller groups at highly active latrines, whereas feet stomping was more intense in recently visited sites. When in groups, scent-marking frequency increased when other individuals were signaling, suggesting a positive feedback, possibly driven by feet stomping. In concert, our results suggest that in river otters, scent-marking decisions minimize signal dilution by being performed in small groups and maximize the receivers through preferential signaling at latrines with higher, more recent activity. Because signaling decisions in social animals are linked to key life-history events such as mating and group membership shifts, understanding their individual and population-level drivers can be crucial.

The scent world of cats: where to place a urine scent mark to increase signal persistence?

Scent-marking is a predominant form of communication among felids, with urine spraying having a key role. Detectability and longevity of scent marks are recognized as crucial for efficiency of scent-marking, but there is limited research that has tested scent persistence with respect to various environmental factors. We used an experimental framework to measure human-perceived strength of felid urine smell and determine the effects of substrate, tilt and aspect of marked surfaces on persistence of the simulated scent marks. We used area under the curve (AUC), calculated for the scent strength of each scent-marked surface over time, as a proxy for urine scent preservation. Thereafter, we used ANOVA, followed by analysis of differences of interest between the marking sites, to assess the effect of environmental factors on human-perceived scent mark persistence. Odour persisted significantly better on rough surfaces, surfaces covered with moss and on surfaces with overhanging tilts, while there was no significant difference between the northerly- and southerly-oriented surfaces. The results are generally in accordance with the use and selection of marking sites previously reported for wild felids throughout the world, confirming that in their marking behaviour felids strive to prolong the persistence of scent marks. This knowledge will help researchers in interpretation of data on scent-marking and to evaluate the adaptive significance of this behaviour.

Design, delivery and perception of condition-dependent chemical signals in strepsirrhine primates: implications for human olfactory communication

The study of human chemical communication benefits from comparative perspectives that relate humans, conceptually and empirically, to other primates. All major primate groups rely on intraspecific chemosignals, but strepsirrhines present the greatest diversity and specialization, providing a rich framework for examining design, delivery and perception. Strepsirrhines actively scent mark, possess a functional vomeronasal organ, investigate scents via olfactory and gustatory means, and are exquisitely sensitive to chemically encoded messages. Variation in delivery, scent mixing and multimodality alters signal detection, longevity and intended audience. Based on an integrative, 19-species review, the main scent source used (excretory versus glandular) differentiates nocturnal from diurnal or cathemeral species, reflecting differing socioecological demands and evolutionary trajectories. Condition-dependent signals reflect immutable (species, sex, identity, genetic diversity, immunity and kinship) and transient (health, social status, reproductive state and breeding history) traits, consistent with socio-reproductive functions. Sex reversals in glandular elaboration, marking rates or chemical richness in female-dominant species implicate sexual selection of olfactory ornaments in both sexes. Whereas some compounds may be endogenously produced and modified (e.g. via hormones), microbial analyses of different odorants support the fermentation hypothesis of bacterial contribution. The intimate contexts of information transfer and varied functions provide important parallels applicable to olfactory communication in humans. This article is part of the Theo Murphy meeting issue ‘Olfactory communication in humans’.

Scent anointing in mammals: functional and motivational insights from giant pandas

Although several mammals impregnate their fur with environmental odors, a phenomenon termed scent anointing or rubbing, the functional relevance of this behavior often is unclear. One theory is that scent anointing could be a form of scent matching with environmental odors to signal competitiveness and home range occupation. In this study we presented giant pandas with a range of odors to determine whether scent matching could provide a functional explanation for scent anointing in this species. We found that only a musk-based perfume elicited significantly more scent-anointing and scent-marking behavior than control. Males were also significantly more likely to scent-anoint and scent-mark than females. A preference for anointing, but not scent marking, when presented with peppermint (an insecticide) also was revealed. Our results suggest that giant pandas differentially scent-anoint with foreign odors to signal home range occupation, and possibly to repel ectoparasites. We also highlight how chemical signaling of resource-holding potential is likely to play an important role in determining competitive interactions between adult male giant pandas.

Patterns of urine scent mark pheromone evolution in house mice and relatives (Muridae:Mus)

ABSTRACTScent marks are important mediators of territorial behavior and sexual selection in many species, especially among mammals. As such, the evolution of compounds used in scent marks has the potential to inform our understanding of signal evolution in relation to social and sexual selection. A major challenge in studies of chemical communication is that the link between semiochemical compounds and genetic changes is often unclear. The major urinary proteins (MUPs) of house mice are elaborated pheromone blends that provide information on sex, status and individual identity. Importantly, MUPs are a direct protein product of genes, providing a clear link between genotype and phenotype. Here we examine the evolution of urinary pheromone signals among house mice and relatives by examining the sequences and patterns of expression of MUPs in the liver, where urine excreted MUPs are produced. MUP patterns have evolved among mouse species both by gene duplication and variation in expression. Notably, the sex-specificity of pheromone expression that has previously been assumed to be male-specific varies considerably across species. Our data reveal that individual identity signals in MUPs evolved prior to 0.35 million years ago and have rapidly diversified through recombining a modest number of perceptually salient amino acid variants. Amino acid variants are much more common on the exterior of the protein where they could interact with vomeronasal receptors, suggesting that perception have played a major role in shaping MUP diversity. Collectively, these data provide new insights into the diverse processes and pressures shaping pheromone signals, and suggest new avenues for using house mice and their wild relatives to probe the evolution of signals and signal processing.

Hierarchical social networks shape gut microbial composition in wild Verreaux's sifaka

In wild primates, social behaviour influences exposure to environmentally acquired and directly transmitted microorganisms. Prior studies indicate that gut microbiota reflect pairwise social interactions among chimpanzee and baboon hosts. Here, we demonstrate that higher-order social network structure—beyond just pairwise interactions—drives gut bacterial composition in wild lemurs, which live in smaller and more cohesive groups than previously studied anthropoid species. Using 16S rRNA gene sequencing and social network analysis of grooming contacts, we estimate the relative impacts of hierarchical (i.e. multilevel) social structure, individual demographic traits, diet, scent-marking, and habitat overlap on bacteria acquisition in a wild population of Verreaux's sifaka ( Propithecus verreauxi ) consisting of seven social groups. We show that social group membership is clearly reflected in the microbiomes of individual sifaka, and that social groups with denser grooming networks have more homogeneous gut microbial compositions. Within social groups, adults, more gregarious individuals, and individuals that scent-mark frequently harbour the greatest microbial diversity. Thus, the community structure of wild lemurs governs symbiotic relationships by constraining transmission between hosts and partitioning environmental exposure to microorganisms. This social cultivation of mutualistic gut flora may be an evolutionary benefit of tight-knit group living.