Morphological Indicators of Olfactory Capability in Wobbegong Sharks (Orectolobidae, Elasmobranchii)

Abstract

Elasmobranchs are thought to possess an acute sense of smell, but the relationship between the anatomy of their olfactory organs and their sensory ecology is poorly understood. Moreover, the ecological diversity of elasmobranchs as a group indicates that there might be considerable interspecific variation in the importance of the olfactory sense. Wobbegong sharks, with their sedentary lifestyle and ambush predatory technique, probably utilize their senses differently than other shark species, making it difficult to generalize about their olfactory capabilities and olfaction-dependent behaviors. In this study, the number of olfactory lamellae and the surface area of the olfactory epithelium were measured as a means of assessing relative olfactory sensitivity in four species of wobbegong shark (the Western wobbegong, Orectolobus hutchinsi; the spotted wobbegong, O. maculatus; the ornate wobbegong, O. ornatus; and the dwarf spotted wobbegong, O. parvimaculatus). We also present a phylogenetic comparative analysis between wobbegongs and other elasmobranchs for which published data on olfactory morphology are available. There is a significant difference in the total number of olfactory lamellae between most species, but not between O. hutchinsi and O. maculatus, although the olfactory sensory surface area is comparable between these two species and O. ornatus. Orectolobus parvimaculatus has a significantly larger olfactory sensory surface area than the other three species, and there is a positive relationship between total body length and olfactory sensory surface area for all four species. Assuming that these morphological measures are true indications of olfactory capability, the olfactory abilities of wobbegongs are as good as, or better than, other benthic elasmobranchs. Interspecific differences in olfactory ability within this group of benthic ambush predators could indicate relative differences in prey detection, intraspecific recognition and mate detection.

Olfactory morphology and physiology of elasmobranchs

“…Whereas lamellar surface area increases with body size of an elasmobranch, the number of lamellae does not; therefore, body size was not included as a covariate during analyses (Fishelson and Baranes, 1997;Schluessel et al, 2010). Our results corroborate those of previous studies, which found interspecific differences in the number of lamellae and surface area for elasmobranchs (Kajiura et al, 2005;Schluessel et al, 2008;Theiss et al, 2009). A recent study (Schluessel et al, 2008) quantified the number of lamellae and epithelial surface area for 21 elasmobranch species and concluded that those factors did not correlate with phylogeny but did with habitat (i.e.…”

“…in only five elasmobranch species (Nikonov et al, 1990;Silver, 1979;Tricas et al, 2009;Zeiske et al, 1986). Also, several recent morphological studies assumed that interspecific differences in the size of elasmobranch olfactory structures confer differences in olfactory sensitivity (Kajiura et al, 2005;Schluessel et al, 2008;Theiss et al, 2009). This study is the first to address these assumptions by comparing the olfactory morphology and physiology of five phylogenetically diverse elasmobranch species.…”

“…Studies on elasmobranch olfactory morphology have attempted to correlate differences in lamellar surface area with olfactory threshold (Kajiura et al, 2005;Schluessel et al, 2008;Theiss et al, 2009) even though the lack of correlation was previously demonstrated in teleost species (Hara, 1994). The rationale behind this proposed correlation is that a species with a greater lamellar surface area should possess a greater number of ORNs and molecular olfactory receptors, which would increase the probability of odorant binding, and thus the ability to detect odorants at a lower concentration than species with less lamellar surface area.…”

“…This reputation is partly based on anecdotal observations, but is also due to their particularly large olfactory structures, including olfactory epithelial surface area (Schluessel et al, 2008) and olfactory bulb volume Lisney and Collin, 2006). Several studies related the size of their olfactory structures to species ecology, invoking the assumption that differences in the size of olfactory structures correlate with olfactory sensitivity Lisney and Collin, 2006;Northcutt, 1977;Northcutt, 1978;Schluessel et al, 2008;Theisen et al, 1986;Theiss et al, 2009;Yopak et al, 2007). This assumption has been refuted for teleost fishes (Hansen and Zielinski, 2005;Hara, 1994;Yamamoto, 1982) and has yet to be tested for elasmobranchs.…”

“…Comparative morphological studies demonstrated that elasmobranchs, like teleost fishes, exhibit interspecific differences in the number and surface area of olfactory lamellae (Hansen and Zielinski, 2005;Kajiura et al, 2005;Schluessel et al, 2008;Theiss et al, 2009;Yamamoto, 1982). Whereas the gross morphology and ultrastructure of the elasmobranch olfactory system are well described (Bell, 1993;Bronshtein, 1976;Meng and Yin, 1981;Schluessel et al, 2008;Tester, 1963;Theisen et al, 1986;Zeiske et al, 1986), olfactory thresholds have been assessed for only five elasmobranch species: the nurse shark (Hodgson and Mathewson, 1978); the Atlantic stingray, Dasyatis sabina (Silver, 1979); the lemon shark, Negaprion brevirostris ; the black sea skate, Raja clavata (Nikonov et al, 1990); and the scalloped hammerhead shark, Sphyrna lewini (Tricas et al, 2009).…”