Behavioral responses to odors from other species: introducing a complementary model of allelochemics involving vertebrates

Abstract

It has long been known that the behavior of an animal can be affected by odors from another species. Such interspecific effects of odorous compounds (allelochemics) are usually characterized according to who benefits (emitter, receiver, or both) and the odors categorized accordingly (allomones, kairomones, and synomones, respectively), which has its origin in the definition of pheromones, i.e., intraspecific communication via volatile compounds. When considering vertebrates, however, interspecific odor-based effects exist which do not fit well in this paradigm. Three aspects in particular do not encompass all interspecific semiochemical effects: one relates to the innateness of the behavioral response, another to the origin of the odor, and the third to the intent of the message. In this review we focus on vertebrates, and present examples of behavioral responses of animals to odors from other species with specific reference to these three aspects. Searching for a more useful classification of allelochemical effects we examine the relationship between the valence of odors (attractive through to aversive), and the relative contributions of learned and unconditioned (innate) behavioral responses to odors from other species. We propose that these two factors (odor valence and learning) may offer an alternative way to describe the nature of interspecific olfactory effects involving vertebrates compared to the current focus on who benefits.

Keywords: allomones; innateness; interspecific interactions; kairomones; learning; odor valence; olfaction; semiochemicals.

Figure 1

Number of publications per year containing the terms allomone, kairomone, or synomone in their topic. The narrow, black line shows their use overall since their coinage in the 1970's (N = 2635 publications) found in a search made in January 2015 in Topic (which includes words in title, keywords, and abstract) in Web of Science™ (ver. 5.16.1; Thomson Reuters © 2015). The bold, red line shows the number of publications among these, which includes vertebrate species (N = 184). Of these, 98 were concerned with kairomones emitted by vertebrates (mainly humans, as well as dogs, ruminants, hedgehogs, poultry, snakes, and penguins) attracting biting or stinging insects (mainly mosquitoes, as well as midges, mites, bed bugs, ticks, tsetse flies, and wasps). Only 32 publications concerning odor-based behavioral responses in vertebrate species were found when searching on any of these three terms.

Figure 2

Conceptual framework to describe interspecific olfactory effects for a given animal at a given time. (A) The simplest categorization of odor-based behavioral responses is a binomial split into either innate or learned responses. Likewise, odor valence can be positive (+ve; attractive odors) or negative (−ve; aversive odors). These combine into four groupings, as depicted here by rectangles. However, odors can be more or less aversive, and odor-based behavioral responses may change with learning, even when the initial response is innate. We have therefore superimposed the four groupings onto a continual representation of learning and valence, expressing odor valence (y-axis) as a function of learning (x-axis), where positive and negative parts of the y-axis indicate degree of attraction and aversion, respectively. It is important to note that odors, which do not elicit an innate behavioral response, have no valence, i.e., are neutral to the animal and thus placed at the origin; Innate responses require no learning, but may be hard to determine and to differentiate from those arising from odors experienced in utero via amniotic fluid; (B) Examples of how different odors may be categorized relative to each other within the conceptual framework, and how odor valence may change with learning. Odor Y could be the natural smell of a predator, whereas molecule A is TMT or 2-phenylethylamine. Both evoke innate responses, but the natural odor is more fear-inducing. Molecule B is an initially neutral odor, which the animal first learns to find aversive, and subsequently associate with a positive experience. Finally, odor X may be the smell of estrus to a male before and after he gains sexual experience.