Bile Salts as Semiochemicals in Fish

Chem. Senses 39: 647–654, 2014 doi:10.1093/chemse/bju039 Advance Access publication August 23, 2014 Bile Salts as Semiochemicals in Fish Tyler J. Buchinger1, Weiming Li1 and Nicholas S. Johnson2 Department of Fisheries and Wildlife, Room 13 Natural Resources Building, Michigan State University, East Lansing, MI 48824, USA and 2United States Geological Survey, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI 49759, USA 1 Correspondence to be sent to: Nicholas S. Johnson, United States Geological Survey, Great Lakes Science Center, Hammond Bay Biological Station, 11188 Ray Road, Millersburg, MI 49759, USA. e-mail: Accepted July 7, 2014 Abstract Bile salts are potent olfactory stimuli in fishes; however the biological functions driving such sensitivity remain poorly understood. We provide an integrative review of bile salts as semiochemicals in fish. First, we present characteristics of bile salt structure, metabolism, and function that are particularly relevant to chemical communication. Bile salts display a systematic pattern of structural variation across taxa, are efficiently synthesized, and are stable in the environment. Bile salts are released into the water via the intestine, urinary tract, or gills, and are highly water soluble. Second, we consider the potential role of bile salts as semiochemicals in the contexts of detecting nearby fish, foraging, assessing risk, migrating, and spawning. Lastly, we suggest future studies on bile salts as semiochemicals further characterize release into the environment, behavioral responses by receivers, and directly test the biological contexts underlying olfactory sensitivity. Key words: chemical cue, communication, electro-olfactogram, olfaction, pheromone Introduction Bile salts are functionally diverse metabolites of cholesterol in vertebrates (Hofmann 1999). The primary function of bile salts is the solubilization of dietary fats in the intestine. However, additional functions include cholesterol homeostasis, antimicrobial effects, and endocrine signaling (Houten et al. 2006; Hofmann and Hagey 2008). Interest in bile salts spans a diverse range of disciplines, including medicine (Hofmann and Hagey 2008), evolution (Hagey et al. 2010), physiology (Cai et al. 2012; Yeh et al. 2012), and environmental chemistry (Li et al. 2011). Hypotheses pertaining to the role of bile salts as olfactory cues have garnered the interest of chemical ecologists (Døving et al. 1980). Bile salts are potent olfactory stimuli in fish (Table 1). Døving et al. (1980) first proposed that bile salts excreted by stream resident conspecifics guide migrating Arctic char (Salvelinus alpinus) to spawning streams. A widespread sensitivity of fish to bile salts has now become apparent. Olfactory detection of bile salts appears throughout the phylogeny of fish, including early vertebrates (Li et al. 1995) and more recently diverged fishes (Michel and Lubomudrov 1995). Species residing in marine (Velez et al. 2009) and freshwater (Zhang et al. 2001) habitats, and those migrating between the Published by Oxford University Press on behalf of US Government 2014. 2 (Sola and Tosi 1993; Li et al. 1995; Baker et al. 2006) detect bile salts with high sensitivity. While olfactory detection of bile salts is well-supported by electrophysiological evidence (Table 1), the biological function of fish sensitivity to bile salts is understood only in the sea lamprey (Petromyzon marinus; Li et al. 1995, 2002; Bjerselius et al. 2000). Here, we review evidence for the role of bile salts as semiochemicals (molecules which carry information to individuals) in fishes. We begin by highlighting characteristics of bile salt chemistry and physiology that are particularly relevant to olfaction. Second, we consider the information fishes receive when bile salts are detected in several contexts. We conclude by suggesting research to further characterize bile salts as semiochemicals. Bile salt chemistry and physiology Structure Bile salts display many minor structural variations (Hofmann et al. 2010) and have high potential to function as specific olfactory cues. Minor structural differences between bile 648 T.J. Buchinger et al. salts can have major consequences for their affinity for a given olfactory receptor (Li et al. 1995; Siefkes and Li 2004; Johnson et al. 2012). The steroid nucleus of bile salts varies in ring stereochemistry, hydroxyl and oxo groups, and conjugation, and the side chain varies in length, hydroxyl and carboxyl groups, saturation, stereochemistry, and conjugation (Figure 1; Hofmann et al. 2010). Variation in bile salt structure follows a systematic pattern (Hofmann et al. 2010) and may contribute to taxon-specific odor profiles (Huertas et al. 2010). Hofmann et al. (2010) proposed a progression from C27 bile alcohols to C27 bile acid intermediates to C24 bile acids throughout the evolution of vertebrates (Figure 1). The pattern generally holds in fishes; hagfish primarily produce 5α C27 bile alcohols, lampreys use 5α C27 and C24 bile alcohols, cartilaginous fishes use 5β C27 bile alcohols, and ray-finned fish use 5β C24 bile acids (Figure 2; Hagey et al. 2010). Lobe-finned Table 1 Evidence for bile salt olfactory cues in fish, including physiological detection as determined by electroolfactograms (EOG), release of bile salts into the water, and behavioral responses in the laboratory and in the field Species Common name Detection Release Response Reference laboratory field Petromyzon marinus Sea lamprey x x x x Li et al. (1995, 2002); Polkinghorne et al. (2001); Yun et al. (2003a) Ichthyomyzon unicuspis Silver lamprey x x x x Fine et al. (2004); Buchinger et al. (2013) Entosphenus tridentatus Pacific lamprey x x — — Yun et al. (2003b, 2011); Robinson et al. (2009); Fine et al. (2004) Petromyzontiforme sp. Various lampreys — x — — Fine et al. (2004); Stewart et al. (2011) Sphyrna tiburo Bonnethead shark x — — — Meredith et al. (2012) Dasyatis Sabina Atlantic stingray x — — — Meredith et al. (2012) Anguilla Anguilla European eel x — x — Sola and Tosi (1993); Huertas et al. (2007) Danio rerio Zebrafish x — — — Michel and Lubomudrov (1995); Friedrich and Korsching (1997) Carassius auratus Goldfish x — — — Sorensen et al. (1987); Huertas et al. (2010) Catostomus catostomus Longnose sucker x — — — Cardwell et al. (1992) Catostomus commersoni White sucker x — — — Cardwell et al. (1992) Ictalurus punctatus Channel catfish x — — — Erickson and Caprio (1984) Oncorhynchus mykiss Rainbow trout x — x — Hara et al. (1984); Giaquinto and Hara (2008); Vermeirssen and Scott (2001) Salvelinus namaycush Lake trout x x — — Zhang et al. (2001); Zhang and Hara (2009) Salvelinus alpinus Arctic char x x x — Døving et al. (1980); Selset and Døving (1980) Solea senegalensis Senegalese sole x x — — Velez et al. (2009) (...truncated)