A mammalian blood odor component serves as an approach-avoidance cue across phylum border - from flies to humans

Abstract

Chemosignals are used by predators to localize prey and by prey to avoid predators. These cues vary between species, but the odor of blood seems to be an exception and suggests the presence of an evolutionarily conserved chemosensory cue within the blood odor mixture. A blood odor component, E2D, has been shown to trigger approach responses identical to those triggered by the full blood odor in mammalian carnivores and as such, is a key candidate as a food/alarm cue in blood. Using a multidisciplinary approach, we demonstrate that E2D holds the dual function of affecting both approach and avoidance behavior in a predator-prey predicted manner. E2D evokes approach responses in two taxonomically distant blood-seeking predators, Stable fly and Wolf, while evoking avoidance responses in the prey species Mouse. We extend this by demonstrating that this chemical cue is preserved in humans as well; E2D induces postural avoidance, increases physiological arousal, and enhances visual perception of affective stimuli. This is the first demonstration of a single chemical cue with the dual function of guiding both approach and avoidance in a predator-prey predicted manner across taxonomically distant species, as well as the first known chemosignal that affects both human and non-human animals alike.

Attractant or Repellent? Behavioral Responses to Mammalian Blood Odor and to a Blood Odor Component in a Mesopredator, the Meerkat (Suricata suricatta)

“…A comparison of the behavioral responses of the meerkats in the present study to those of several species of top predators tested previously with the same method and odor stimuli ( Nilsson et al, 2014 ; Arshamian et al, 2017 ) shows that the meerkats displayed the highest number of interactions per animal with the odorized wooden logs ( Table 4 ). This was true both when considering all four odor stimuli combined and separately.…”

“…Thus, it should not have been surprising if the meerkats in our study would have behaved like mice and rats, that is, like a prey species and accordingly would have avoided the odor of blood ( Hornbuckle and Beal, 1974 ; Lahger and Laska, 2018 ). If we further consider that the diet of meerkats is not exclusively based on smaller vertebrates but also includes a variety of non-vertebrate food items such as arthropods and plant material ( van Staaden, 1994 ), it is actually somewhat unexpected that the meerkats behaved like top predators such as tigers and wolves ( Nilsson et al, 2014 ; Arshamian et al, 2017 ) and were attracted to blood odor. This, in turn, suggests that the attraction to blood odor displayed by carnivorous mammals of the feline and canine families may be an evolutionarily old trait as the mongoose family (Herpestidae) to which the meerkats belong split from the other carnivore families about 25 million years ago ( Nyakatura and Bininda-Emonds, 2012 ).…”

“…Unfortunately, the olfactory detection threshold for TED is not known for any of the predator species that are attracted by this blood odor component. However, human subjects and mice which are both repelled by the odor of TED ( Arshamian et al, 2017 ; Lahger and Laska, 2018 ) have been shown to be extraordinarily sensitive to this compound with threshold values in the ppt (parts per trillion) range ( Buettner and Schieberle, 2001 ; Sarrafchi and Laska, 2017 ). Thus, there is at least circumstantial evidence that TED may fulfill the prerequisite of a “key” or “character impact” compound of being detectable at low concentrations.…”

“…The rationale for using these two odor stimuli was that horse blood and trans -4,5-epoxy-(E)-2-decenal had also been used in previous studies assessing behavioral responses of top predators ( Nilsson et al, 2014 ; Arshamian et al, 2017 ) and a prey species ( Lahger and Laska, 2018 ) to blood odor.…”

“…The odor of blood has been shown to be attractive to mammalian top predators such as tigers ( Nilsson et al, 2014 ) and wolves ( Arshamian et al, 2017 ) and to be aversive to mammalian prey species such as the mouse ( Sandnabba, 1997 ; Lahger and Laska, 2018 ) and the rat ( Stevens and Saplikoski, 1973 ; Hornbuckle and Beal, 1974 ; Mackay-Sim and Laing, 1981 ). Interestingly, the tigers and wolves were equally attracted to and the mice were equally repelled by trans -4,5-epoxy-(E)-2-decenal (TED), a single component of mammalian blood odor which has been described by humans as having a typical “metallic, blood-like” odor quality ( Buettner and Schieberle, 2001 ).…”