Mix it and fix it: functions of composite olfactory signals in ring-tailed lemurs

Abstract

Animals communicating via scent often deposit composite signals that incorporate odorants from multiple sources; however, the function of mixing chemical signals remains understudied. We tested both a ‘multiple-messages’ and a ‘fixative’ hypothesis of composite olfactory signalling, which, respectively, posit that mixing scents functions to increase information content or prolong signal longevity. Our subjects—adult, male ring-tailed lemurs (Lemur catta)—have a complex scent-marking repertoire, involving volatile antebrachial (A) secretions, deposited pure or after being mixed with a squalene-rich paste exuded from brachial (B) glands. Using behavioural bioassays, we examined recipient responses to odorants collected from conspecific strangers. We concurrently presented pure A, pure B and mixed A + B secretions, in fresh or decayed conditions. Lemurs preferentially responded to mixed over pure secretions, their interest increasing and shifting over time, from sniffing and countermarking fresh mixtures, to licking and countermarking decayed mixtures. Substituting synthetic squalene (S)—a well-known fixative—for B secretions did not replicate prior results: B secretions, which contain additional chemicals that probably encode salient information, were preferred over pure S. Whereas support for the ‘multiple-messages’ hypothesis underscores the unique contribution from each of an animal's various secretions, support for the ‘fixative’ hypothesis highlights the synergistic benefits of composite signals.

Sex differences in scent‐marking in captive red‐ruffed lemurs

“…Volatile hydrocarbons have previously been identified in odorants deriving from ring‐tailed lemurs and sifakas (Hayes et al, ; Scordato et al, ) as well as from Old World monkeys such as mandrills (Setchell et al, ; Vaglio et al, ) and olive baboons (Vaglio et al, in preparation). In particular, high‐molecular weight volatile hydrocarbons might act as a fixative which slows the release of more volatile compounds, as suggested for major urinary proteins in mice (Greene et al, ; Hurst et al, ). The compounds benzaldehyde, p‐cresol (also known as p‐methylphenol), hexanal, and geranylacetone are commonly encountered in mammal scent markings (e.g., lions, wild dogs, wolves, mice, red foxes) (Osada, Miyazono, & Kashiwayanagi, ; Roberts et al, ; Soso & Koziel, ).…”

Multimodal pair‐bond maintenance: A review of signaling across modalities in pair‐bonded nonhuman primates

“…One example is complex unimodal chemical signals in which individuals are more responsive when exposed to the combination of two secretions than to either pure secretion on its own. In this case, the unimodal components may not only contain multiple messages, but they may also work together to increase the longevity of the message (Greene et al, 2016).…”

“…Importantly, message diversity (encoded nonredundant or novel information) may be constrained by intense selection for signal robustness (Ay et al, 2007). Determining if each component is redundant or nonredundant requires careful behavioral study, and experimental methods when possible (e.g., Greene et al, 2016;Partan, 2013). For example, an experimenter can present just F I G U R E 1 Overview of species included in this review by exemplified modality part of the signal versus the whole signal and gauge the responses.…”

Ontogeny and Microanatomy of the Nasal Turbinals in Lemuriformes

“…This is not to say there is a lesser importance of olfaction in these species. Diurnal/cathemeral strepsirrhines are generally larger and easier to study compared to nocturnal species, and a growing body of literature suggests that olfaction (via both main and accessory olfactory systems) is also an essential modality for their foraging and sociosexual interactions (Kappeler, ; Gould and Overdorff, ; Palagi et al, ; Scordato and Drea, ; Drea and Scordato, ; Smith et al, ; Greene et al, ). Although the repertoire of olfactory behavioral correlates has been extensively investigated in diurnal/cathemeral strepsirrhines such as Lemur catta , our knowledge of pertinent anatomy is greatly limited, except to say that ample potential surface area for olfactory mucosa exists.…”