Olfactory sensory input increases gill ventilation in male round gobies (Neogobius melanostomus) during exposure to steroids Rachelle M. Belanger a,c , Lynda D. Corkum a , Weiming Li b , Barbara S. Zielinski a, ⁎ a Department of Biological Sciences, University of Windsor, Windsor, ON, Canada N9B 3P4 b Department of Fisheries and Wildlife, Michigan State University, East Lansing, MI 48824, USA c Department of Biological Sciences, Bowling Green State University, Bowling Green, OH 43403, USA Received 30 May 2005; received in revised form 18 February 2006; accepted 21 February 2006 Available online 28 February 2006 Abstract In teleostean fish, ventilation increases have been observed in response to low dissolved oxygen levels, visual stimuli, and gustatory cues. However, olfactory sensory input may also stimulate gill ventilation rate. We investigated whether olfactory sensory input mediates gill ventilation responses, as suggested by the observation that steroidal compounds detected by the olfactory system elicited increases in opercular activity in the perciform teleost, the round goby (Neogobius melanostomus). Close parallels between gill ventilation and olfactory responses, led us to conduct an empirical study that used two different olfactory sensory deprivation techniques to seek a causal relationship between olfactory epithelial activity and hyperventilation. Chemical lesion of olfactory sensory neurons or mechanical occlusion of the nasal cavities inhibited gill ventilation responses of reproductive male round gobies to estrone (1,3,5(10)-estratrien-3-ol-17-one) and to ovarian extracts. This direct evidence demonstrates the role of olfactory sensory input for the gill ventilation response to putative reproductive pheromones and may represent an important regulatory mechanism for odorant sampling during pheromone communication. © 2006 Elsevier Inc. All rights reserved. Keywords: Copper sulfate; Estrone; Fish; Gill ventilation; Nasal occlusion; Olfactory sensory neurons; Ovarian extract; Round goby 1. Introduction In teleostean fish, opercular movement allows for the flow of water over the gill arches where gas exchange takes place. Oxygen receptors on the gills serve to modulate gill ventilation (Smatresk, 1990; Burleson and Milsom, 1993) such that the rate of gill ventilation increases as oxygen levels decrease (Gee and Gee, 1991). Gill ventilation responses may be driven by alternate sensory modalities. For example, the visual effects of predators override gill chemoreceptors in the flathead gray mullet, Mugil cephalus, and gill ventilation rates increase following this visual stimulation (Shingles et al., 2005). This hyperventilation allows the fish to acquire adequate oxygen as it descends in the water to avoid predators. In channel catfish, Ictalurus punctatus, the taste of amino acids stimulates gill hyperventilation during feeding (Valentinčič and Caprio, 1994). Finally, a “sniffing” mecha- nism, driven by opercular movement may facilitate odor detection in flounder species, Lepidopsetta bilineata and Platichthys stellatus (Nevitt, 1991). Accessory nasal sacs, caudal to the olfactory chamber in many Acanthoptergii fish (including gobies and flounder; Burne, 1909; Sinha and Sinha, 1990; Belanger et al., 2003; Hansen and Zielinski, in press) undergo a pumping action that coincides with the opening and closing of the mouth (Nevitt, 1991). When the mouth opens, muscles that regulate gill motion contract and water is drawn into the anterior nostril. When the mouth closes and the gill muscles relax, water is expelled from the posterior nostril (Johnson and Brown, 1962). Recent studies of the round goby have demonstrated increased gill ventilation frequency during exposure to synthetic steroids (putative reproductive pheromones), with threshold values closely matched between olfactory epithelial (electro-olfactogram) and gill ventilation responses (Murphy Comparative Biochemistry and Physiology, Part A 144 (2006) 196 – 202 www.elsevier.com/locate/cbpa ⁎ Corresponding author. Tel.: +1 519 253 3000x2726; fax: +1 519 971 3609. E-mail address: zielin1@uwindsor.ca (B.S. Zielinski). 1095-6433/$ - see front matter © 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.cbpa.2006.02.027