A synthesized pheromone induces upstream movement in female sea lamprey and summons them into traps

Abstract

Female insect pheromone blends induce robust tracking responses in males and direct them into traps. In vertebrates, pheromones that induce strong and precise tracking responses in natural habitats have rarely been described. Here, we show in the sea lamprey (Petromyzon marinus), a vertebrate invader of the Laurential Great Lakes, that a synthesized component of the male mating pheromone, 7␣, 12␣, 24-trihydroxy-5␣-cholan-3-one 24-sulfate (3kPZS), when released into a stream to reach concentrations of 10 ؊14 , 10 ؊13 , 10 ؊12 ,10 ؊11 , or 10 ؊10 M, triggers robust upstream movement in ovulated females drawing Ϸ50% into baited traps. Experiments conducted in diverse stream segments demonstrate the level of behavioral response was not affected by habitat conditions and is effective over hundreds of meters. 3kPZS is equally effective at luring ovulated females as the whole pheromone blend released by males between 10 ؊14 and 10 ؊11 M. 3kPZS diverts ovulated females away from and disrupts orientation to male washings when applied at concentrations higher than washings. Indeed, a single pheromone compound is able to redirect female sea lampreys away from a natural pheromone source and lure them into traps, which should be more effective than targeting males when applied in population control. Our findings may spur the discovery of other potent and environmentally benign agents to combat biological invasion, a process accelerated by globalization, exacerbated by climate change, and costing the global economy US$ 1.4 trillion of damage annually.invasive species ͉ odorant tracking ͉ pest control ͉ odorant disruption ͉ jawless vertebrate

Evidence for partial overlap of male olfactory cues in lampreys

“…Components of complex signals can have different underlying functions and be shaped by different selective pressures (Candolin, 2003). In P. marinus, the major pheromone component 3kPZS elicits long-distance mate search (Siefkes et al, 2005;Johnson et al, 2009), while minor components probably facilitate close-proximity courtship behaviours (Johnson et al, 2012). Most pheromones identified in fish are released at relatively low rates, are likely to guide close-proximity spawning synchronization rather than mate search, and are hypothesized to represent receiver adaptations (Stacey, 2015).…”

“…Upon reaching the final stages of sexual maturation, males construct nests and signal with an odour that elicits upstream movement and nesting behaviours in females (Li et al, 2002;Siefkes et al, 2005;Johnson et al, 2012). The major component 7α, 12α, 24-trihydroxy-5α-cholan-3-one-24-sulfate (3-keto petromyzonol sulfate, 3kPZS) guides female movement over long distances to the nest (Li et al, 2002;Siefkes et al, 2005;Johnson et al, 2009). Additional minor components that retain females in the area of the nest and elicit nesting behaviours remain unidentified (Johnson et al, 2012), but may include 3,12-diketo-4,6-petromyzonene-24-sulfate (DkPES; Li et al, 2013;Brant et al, 2016a) and petromyzestrosterol .…”

Odorant organization in the olfactory bulb of the sea lamprey

“…The ex vivo preparation described in the 'Tissue preparation' section (above) was utilized. Amino acids, a bile acid (taurocholic acid) and bile acid steroid pheromones previously shown to be stimulatory to the main olfactory epithelium (Li et al, 1995(Li et al, , 2002Bjerselius et al, 2000;Siefkes et al, 2003;Siefkes and Li, 2004;Sorensen et al, 2005;Johnson et al, 2005Johnson et al, , 2009 were tested. The pheromone test solution included the migratory pheromones petromyzonol sulphate (PZS), and two disulphated aminosterol derivatives known as petromyzonamine disulphate (PADS) and petromyzonolsterol disulphate (PSDS) (Li et al, 1995;Bjerselius et al, 2000;Sorensen et al, 2005), as well as the reproductive pheromones 3-keto petromyzonol sulphate (3KPZS) and 3-keto allocholic acid (3KACA).…”

“…During spawning migration, sea lampreys encounter a mixture of bile acid steroids released from larval sea lamprey in the streambed, and these larval odours have an important role in identifying a suitable river for spawning and larval rearing (Li et al, 1995;Sorensen and Vrieze, 2003). Once a spawning location is found, spermiated male sea lampreys release steroid pheromones, which induce movement/searching and spawning behaviours in ovulated female sea lamprey (Li et al, 2002;Siefkes et al, 2003;Siefkes and Li, 2004;Johnson et al, 2005Johnson et al, , 2009. Physiological studies have also investigated olfactory function in the sea lamprey.…”

“…Basic amino acids and a variety of steroid bile acids (including the lamprey pheromones) stimulate olfactory sensory responses from the main olfactory epithelium (e.g. Li et al, 1995Li et al, , 2002Li and Sorensen, 1997;Siefkes and Li, 2004;Sorensen et al, 2005;Johnson et al, 2009). However, the peripheral olfactory organ also houses abundant tubular diverticula known as the accessory olfactory organ (Hagelin and Johnels, 1955).…”