Olfactory navigation during spawning migrations: a review and introduction of the Hierarchical Navigation Hypothesis

Abstract

Migrations are characterized by periods of movement that typically rely on orientation towards directional cues. Anadromous fish undergo several different forms of oriented movement during their spawning migration and provide some of the most well-studied examples of migratory behaviour. During the freshwater phase of the migration, fish locate their spawning grounds via olfactory cues. In this review, we synthesize research that explores the role of olfaction during the spawning migration of anadromous fish, most of which focuses on two families: Salmonidae (salmonids) and Petromyzontidae (lampreys). We draw attention to limitations in this research, and highlight potential areas of investigation that will help fill in current knowledge gaps. We also use the information assembled from our review to formulate a new hypothesis for natal homing in salmonids. Our hypothesis posits that migrating adults rely on three types of cues in a hierarchical fashion: imprinted cues (primary), conspecific cues (secondary), and non-olfactory environmental cues (tertiary). We provide evidence from previous studies that support this hypothesis. We also discuss future directions of research that can test the hypothesis and further our understanding of the spawning migration.

Evidence of Olfactory Imprinting at an Early Life Stage in Pink Salmon (Oncorhynchus gorbuscha)

“…Natal site fidelity appears to be lower in pink salmon than the other species as well24, which could result from an imprinting period that is contracted or occurs at an earlier developmental stage, as necessitated by their unique life history. Aside from the research of Tilson et al 21, though, direct evidence of imprinting during larval stages is limited25, and olfactory imprinting prior to emergence from the gravel has not been demonstrated in pink salmon.…”

Ectopic expression of olfactory receptors and associated G‐protein subunits in the head integument of the amphihaline migratory fish hilsa Tenualosa ilisha

“…They proposed that such organization of structures might help the fish to receive chemical signals from its breeding habitats to initiate upstream migration. Other than olfaction, which has received attention as the main biological mechanism involved in sensory reception during fish migration (Bett & Hinch ), the involvement of integumentary tissues for sensory reception in fish is not known. After Malick et al .…”

Physiological Mechanisms of Imprinting and Homing Migration of Pacific Salmon

“…The second is the pheromone hypothesis developed by Nordeng (1977) using Arctic char and Atlantic salmon that juvenile salmon in a stream release population-specific odors that guide homing adults. And, the third is the hierarchical navigation hypothesis proposed by Bett and Hinch (2015), that migrating adult salmon relied on primary directional cue, is imprinted odors. Secondary directional cue is conspecific odors, and tertiary cue is non-olfactory environmental indicators.…”

“…L-kynurenine, an amino acid was identified as a sex pheromone in the urine of ovulated female masu salmon (Yambe et al 2006). Recently, the hierarchical navigation hypothesis was proposed by Bett and Hinch (2015) that migrating adult salmon relied on primary imprinting cues, secondary conspecific cues, and tertiary non-olfactory environmental cues.…”