Invasive male round gobies (Neogobius melanostomus) release pheromones in their urine to attract females

Abstract

The round goby (Neogobius melanostomus) is an invasive fish in the Laurentian Great Lakes and beyond. Pheromones appear to be important for their reproductive success, as females are attracted to water in which reproductive males have resided ("conditioned water"). Previous investigation has shown conjugated and unconjugated forms of 3␣-hydroxy- are released in the urine of these males. The goal of this study was to determine if the urine of reproductive males and fractionated extracts attract females. We found that reproductively active females were attracted to male urine and to isolates of male-conditioned water that contained conjugated 11-O-ETIO. The fractionated preparation that corresponded to unconjugated 11-O-ETIO (i.e., "free" steroid released via the gills of males) was not attractive to reproductive females, but curiously, it was attractive to nonreproductive females. Olfactory sensory deprivation confirmed that the behavioural responses were mediated by olfaction. These findings take us closer towards identifying the pheromone(s) that attract female gobies and, therefore, closer to having a method to limit this species' damaging invasion.Résumé : Le gobie à taches noires (Neogobius melanostomus) est un poisson envahissant dans les Grands Lacs laurentiens et au-delà . Les phérormones semblent être un facteur important en ce qui concerne leur succès de reproduction, les femelles étant attirées par l'eau dans laquelle ont résidé des mâles reproducteurs (« eau conditionnée »). Une étude précédente a démontré que des formes conjuguées et non conjuguées de la 3␣-hydroxy-5␤-androstane-11,17-dione (11-oxo-étiocholanolone; 11-O-ETIO) sont libérées dans l'urine de ces mâles. Le but de l'étude était de déterminer si l'urine de mâles reproducteurs et des extraits fractionnés attiraient les femelles. Nous avons constaté que les femelles reproductrices étaient attirées par l'urine des mâles et des isolats d'eau conditionnée par ces derniers contenant de la 11-O-ETIO conjuguée. La préparation fractionnée qui correspondait à la 11-O-ETIO non conjuguée (c.-à -d. stéroïde « libre » libéré par les branchies des mâles) n'attirait pas les femelles reproductrices bien que, fait surprenant, elle ait attiré les femelles non reproductrices. La privation olfactive a confirmé que les réponses comportementales étaient modulées par l'olfaction. Ces résultats sont un pas de plus vers l'identification de la ou des phéror-mones qui attirent les gobies et ainsi, vers la mise au point d'une méthode permettant de limiter l'invasion de cette espèce dommageable. [Traduit par la Rédaction]

Olfactory sensitivity to steroid glucuronates in Mozambique tilapia suggests two distinct and specific receptors for pheromone detection

“…A similar observation was made of African catfish (Clarias gariepinus) males, where the most potent testicular odorant was found to be 20one-P-3-G (Lambert and Resink, 1991). Androstanes and pregnanes with a 5β,3α configuration are also potent odorants for the round goby (Neogobius melanostomus, Pallas 1814) (Murphy et al, 2001), and recent studies have demonstrated that round goby males release several conjugated forms of these steroids via their urine (Katare et al, 2011), eventually to attract females (Tierney et al, 2013). However, in the round goby, the olfactory receptors detecting ETIO-3-G appear to be less specific than those in tilapia; several unconjugated androstanes, pregnanes and even androsten, are detected by the same (ETIO-3-G) receptor site (Murphy et al, 2001).…”

“…Within the Perciformes, the largest teleost order (Order Summary for Perciformes, www.fishbase.org), studies on olfactory sensitivity to, and pheromonal function of, hormonal steroids are scarce and derive from a few representatives of the Gobiidae (Colombo et al, 1980;Corkum et al, 2008;Murphy et al, 2001;Tierney et al, 2013) and Cichlidae (Cole and Stacey, 2006;Hubbard et al, 2014;KellerCosta et al, 2014). Cichlids are an extremely diverse taxon with currently 1670 described species ('List of Nominal Species of Cichlidae', www.fishbase.org), mostly native to Africa, and adaptation of the sensory and signalling systems to different environmental conditions has been suggested as an important driver in African cichlid radiation (Seehausen et al, 2008).…”

The round goby genome provides insights into mechanisms that may facilitate biological invasions

“…In addition, the observed cases of gene expansions in receptors warrant investigations into the evolution of ligand binding repertoires. For example, olfactory receptor 7tm1 subfamily members are expanded in Gobiidae, and we hypothesize that they may be involved in the detection of distinctive types of odors relevant for Gobiidae ecology and/or reproduction [31][32][33]. Which types of odorants are detected by parallel expanded ORs, and whether these expansions serve to detect similar or different types of odorant molecules in different species, remain to be studied.…”

“…Similarly, olfaction is an essential chemoreception sense for fish, allowing for fast responses to predators and alarm cues, as well as for intra-species communication. Pheromones play an important role in the round goby [31][32][33], and males attract females into their nests by releasing them [34]. A particularly specialized sense of smell therefore may provide an advantage during initial population establishment in novel environments, when population densities are still low.…”