The role of food odor in invertebrate foraging

Abstract

Foraging for food is an integral part of animal survival. In small insects and invertebrates, multisensory information and optimized locomotion strategies are used to effectively forage in patchy and complex environments. Here, the importance of olfactory cues for effective invertebrate foraging is discussed in detail. We review how odors are used by foragers to move toward a likely food source and the recent models that describe this sensory-driven behavior. We argue that smell serves a second function by priming an organism for the efficient exploitation of food. By appraising food odors, invertebrates can establish preferences and better adapt to their ecological niches, thereby promoting survival. The smell of food pre-prepares the gastrointestinal system and primes feeding motor programs for more effective ingestion as well. Optimizing resource utilization affects longevity and reproduction as a result, leading to drastic changes in survival. We propose that models of foraging behavior should include odor priming, and illustrate this with a simple toy model based on the marginal value theorem. Lastly, we discuss the novel techniques and assays in invertebrate research that could investigate the interactions between odor sensing and food intake. Overall, the sense of smell is indispensable for efficient foraging and influences not only locomotion, but also organismal physiology, which should be reflected in behavioral modeling.

Keywords: C. elegans; D. melanogaster; foraging; invertebrate; navigation; odor sensing.

FIGURE 1

Typical odor plumes and navigational strategies for invertebrates. (A) Typical plumes and odor‐guided foraging lengths encountered by roundworms (a),, copepods (b), blue crabs (c) or green crabs (d), desert ants (e),, gypsy or hawk moths (f, g) and bumble bees (h)., Odors transition from smooth gradients to turbulent odor plumes with increasing travel distances. (B) Navigational strategies of three species encountering odor plumes of different types. C. elegans,, , blue crabs and walking D. melanogaster. Irrespective of the strategy followed, navigation can be divided in runs (light blue) and turns (pink). Odor concentration is shown in dark green

FIGURE 2

Advantages of odor sensation during exploitation. (A) Besides determining distance to food, odor plumes allow for distinctions between food type, quality and size and allow animals to navigate based on nutritional needs and other internal drivers. (B) Anticipatory feeding behaviors induced by food odor, including the motor‐ and digestive priming, allow for improved animal survival, fitness and reproduction through efficient food capture and ingestion

FIGURE 3

Foraging decisions are altered when a forager is primed by odor sensation. (A) Foraging encompasses multiple sub‐behaviors of which a forager can perform all or a subset. The animal starts with a random search pattern, and once an odor is encountered, odor navigation begins. Upon food encounter, feeding begins. Eventually, the forager leaves the current food patch. There are many decisions involved (black arrowheads): choice of a patch, taste and choice of leaving. (B) Anticipatory behaviors can alter energy intake, for example by shortening ingestion and digestion delays or by allowing a higher metabolic efficiency. (C) Possible effects of odor priming on a marginal value theory forager: The forager leaves a patch when the food intake drops below the average expected rate (top, dashed line is the average expected rate, gray is time in a patch). Given the same time spent in a food patch, both efficient digestion (middle) and motor priming (bottom) lead to more energy intake compared with an unprimed classical forager, either by faster metabolism or reducing ingestion delays, respectively