The scent of wolves: pyrazine analogs induce avoidance and vigilance behaviors in prey

Abstract

The common gray wolf (Canis lupus) is an apex predator located at the top of the food chain in the Northern Hemisphere. It preys on rodents, rabbits, ungulates, and many other kinds of mammal. However, the behavioral evidence for, and the chemical basis of, the fear-inducing impact of wolf urine on prey are unclear. Recently, the pyrazine analogs 2, 6-dimethylpyrazine, 2, 3, 5-trimethylpyrazine and 3-ethyl-2, 5-dimethyl pyrazine were identified as kairomones in the urine of wolves. When mice were confronted with a mixture of purified pyrazine analogs, vigilance behaviors, including freezing and excitation of neurons at the accessory olfactory bulb, were markedly increased. Additionally, the odor of the pyrazine cocktail effectively suppressed the approach of deer to a feeding area, and for those close to the feeding area elicited fear-related behaviors such as the “tail-flag,” “flight,” and “jump” actions. In this review, we discuss the transfer of chemical information from wolf to prey through the novel kairomones identified in wolf urine and also compare the characteristics of wolf kairomones with other predator-produced kairomones that affect rodents.

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

“…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, ). The compound benzaldehyde has already been found in gland secretions released by marmosets (Smith et al, ), and functions as sex pheromone in other mammals (reviewed in El‐Sayed, ) and also as cue to genetic quality (reviewed in Wyatt, ) in other vertebrates (e.g., in the crested auklet, a seabird with citrus scent based on decanal and octanal produced by both sexes during the breeding season, concentration correlates with rank in males).…”

Symbiotic skin bacteria as a source for sex-specific scents in frogs

“…Pyrazines are widely distributed in nature, possess intense odors, and are some of the major volatile compounds produced by bacteria (29,30). They likewise mediate communication in different organisms such as bacteria (31), insects (32,33), and mammals (34,35). Particularly, MOPs have been described as mate attractants and aposematic signals in insects (32,36).…”

Pyrazine analogues from wolf urine induced unlearned fear in rats

“…In fact, exposure to the urine of wolves induces avoidance and the flat-back approach in rats ( Fendt, 2006 ). Previously, we identified pyrazine derivatives in wolf urine that induced fear-related responses in mice and Hokkaido deer ( Cervus nippon yesoensis ), a species native to Japan (Osada et al, 2013 ; 2014 ; 2015 ).…”

“…Cat odor but not TMT caused pronounced activation of Fos, a marker of neuronal excitation, in the AOB, a primary brain region that receives information of pheromones and kairomones from the VSNs, of rats, suggesting that cat odor induces fear-related responses via the vomeronasal system ( McGregor et al, 2004 ; Staples et al, 2008a ; b ). Wolf urine or a mixture of three pyrazine derivatives (P-mix) induced an increase in Fos-immunoreactive (Fos-ir) cells in the AOB in mice (Osada et al, 2013 ; 2015 ). The amygdala is an important brain region for threat detection and the elicitation of fear-related behavior ( Asok et al, 2013 ).…”