Why are wobbegongs such good predators?

By Morgan Halley (Scripps College) and Kendall Kritzik (Scripps College) [edited by Lars Schmitz, as part of BIOL 167 “Sensory Evolution”, an upper division class at the Claremont Colleges]

There are a number of different sensory receptors found in animals. They range from photoreceptors, chemoreceptors, mechanoreceptors, electroreceptors and magnetoreceptors. The mechanosensory lateral line (MLL) is a common feature that is found in all species of fish and most aquatic amphibians (Figure 1).

Figure 2. The lateral line system.

Figure 2. The lateral line system.

The MLL is a line of mechanoreceptors located very close to the skin surface, and can detect water movements in relation to the skin surface; however it can only detect movements that are within a few centimeters from the skin. It is thought that the MLL is responsible for many behaviors seen in fish and amphibians, including prey detection.

The Elasmobranchii are a subgroup of Chondrichthyes, the cartilaginous fish that includes rays and sharks (Palmer, ed., 1999). The MLL of elasmobranchs are composed of four organs: the vesicles of Savi, spiracular organs, canal neuromasts, and pit organs. Studies of the MLL in elasmobranchs have focused on the canal morphology and topography for rays with very few studies that look at the canal systems in sharks. Because of the large variation between sharks and rays, it is not known if findings of ray MLL systems can be applied to sharks. There have also been very few studies that look at pit organ morphology and distribution.

The wobbegong sharks (Orectolobidae) are part of a unique group of Elasmobranchii that differ from other sharks in terms of shape and ecology. They have a compressed body and live on the seafloor, which is often seen in rays (Figure 2). Wobbegongs also employ sit-and-wait ambush feeding that is very rare, not only among sharks, but among elasmobranchs in general. Taking all these differences into account one should expect fundamentally different sensory adaptations in wobbegongs, and that’s what Theiss and her colleagues went after in their study on the MLL.

Figure 2. The Spotted Wobbegong Shark, Orectolobus maculatus.

Figure 2. The Spotted Wobbegong Shark, Orectolobus maculatus.

Theiss et al. examined the morphology and spatial arrangement of the MLL system in two species of wobbegong shark, the spotted wobbegong Orectolobus maculatus and the ornate wobbegong Orectolobus ornatus.  These two species spend the majority of their time on the sea floor, ready to ambush fish and cephalopods both during the day and at night. The MLL morphology and distribution was hypothesized to be specialized in wobbegong sharks due to their unusual feeding strategy. The morphology of canal neuromasts was described along with the location of the lateral line canals and the distribution and number of canal pores in both species (Figure 3). The pit organ distribution and numbers were only reported for O. ornatus, because they have been previously reported for O. maculatus (Peach 2003). The MLL topography was then paired with biological and ecological functions.

Figure 3. Schematic drawing of the fine structure of the lateral line system.

Figure 3. Schematic drawing of the fine structure of the lateral line system.

In order to study the MLL, four members of O. maculatus and O. ornatus were examined for lateral line pore and canal distribution, neuromast and pit organ morphology, and pit organ distribution (O. orectus). The animals were euthanized, and the heads removed. The skin was removed from the dorsal and ventral sides of the head, and the MLL canals were stained using 0.05% Methylene Blue. In order to see the smaller pores, a dissecting microscope was used.

Pit organs could be identified by the two enlarged denticles (tiny scales) on either side of the organ. The head outline and locations of the canals, pores, and pit organs (O. orectus) were traced onto transparencies and scanned into a computer. The canal pores and pit organs were counted for each individual, and averaged based on pore type. These numbers were analyzed using two-tailed t tests. Pore and canal maps were made using Adobe Illustrator CS3 (Adobe) and a digital drawing tablet.

Skin samples from each individual were dissected from each lateral line system with the exception of the nasal and prenasal canals. The samples were bisected through the middle and examined with a scanning electron microscope in order to view the canal neuromasts. Samples containing dorsolateral, spiracular, and mandibular pit organs were also removed from three individuals of each species. The samples were decalcified and the denticles removed. The samples were mounted and examined for width, length, hair cell kinocilia and stereovilli length, and microvilli length using a scanning electron microscope (Figure 3).

It is known that, in elasmobranchs, pored MLL canals detect information on external water acceleration, as neuromasts are directly in contact with the external water environment (Figure 3). Theiss and her colleagues found that, in both species of wobbegong sharks, the pored MLL canals were located predominantly on the top of the head. This distribution is nearly identical to that of the Japanese wobbegong shark Orectolobus japonicas. Behaviorally, they speculated that this arrangement facilitates ambush predation; wobbegongs feed on fish and cephalopods at night, and so the dorsal (top) arrangement of mechanosensory canals and pores would allow them to easily detect and accurately strike at prey swimming in front and above them. Because of this mechanosensory system, the sharks would not have to rely on limited vision during the night.

Interestingly, non-pored canals do not detect external water acceleration directly; neuromasts respond instead to internal fluid velocity that is caused by skin movement. Theiss and her team found that the canals behind the eye and just before the nose of both wobbegong species are non-pored canals. This canal type is known to exist ventrally in stingrays and aid them in capturing benthic (bottom-dwelling) prey (Wueringer and Tibbetts 2008). Although wobbegongs are themselves a benthic species and feed on non-benthic prey, the authors proposed that the dorsal position of their non-pored canals optimizes their tactile sensation while feeding in a similar manner; if the shark bumps into prey on these surfaces while swimming or while striking (perhaps they identified the prey item via small water currents which they would register with dorsal pored canals), the receptors will immediately recognize the prey’s location and enable more accurate striking.

The discovery of non-pored canals in the two wobbegong species studied contradicted findings in a study of the Japanese wobbegong, in which the same canals are pored. This shows that even among species of the same clade, there are structural differences. It is therefore important to sample across a broad phylogenetic spectrum. Additionally, the hyomandibular canal (running parallel to the jaw) in the two species studied was located dorsally on the head, rather than ventrally (as commonly seen in sharks) or ventral-dorsally (as seen in batoids; Wueringer and Tibbetts 2008). This change may be a result of the sharks’ compressed head morphology. Another notable difference in the wobbegong sharks is the non-continuous distribution of canals with neuromast sensory tissue; in other elasmobranch species, sensory tissue is either continuous or near-continuous. The authors speculated that this may indicate a decrease in sensitivity in the wobbegong sharks, although it may be possible that neuromast tissue was damaged or hard to visualize in the prepared specimens. As such, further examination is needed to confirm this observation.

Some problems that arose during this study had to do with the technical difficulty of finding the pores of the lateral line canals. The authors noted that the pores have extremely small diameters and could be easily missed – particularly in the nasal region which has dense connective tissue. Additionally, the fixation process in this study damaged the fragile neuromast structures and prevented a thorough examination of their morphology; no remnants of the cupula (Figure 3) were present for analysis. It would be advantageous to fine-tune the fixation procedures so that these structures are not damaged, as characteristics of the neuromast (such as hair cell orientation) could provide useful information on directional detection of water flow. Most importantly, Theiss et. al speculated that the MLL of wobbegongs is an adaption to benthic lifestyle; however, the study design examined only two species, both of which were wobbegong sharks. It would be beneficial to confirm this speculation with studies examining the MLL of a wide variety of sharks and rays (Garland and Adolph 1994). Finally, further behavioral studies should be done to confirm the specific advantages of pored and non-pored canals in these two species.

References:

Garland, T., Jr., and Adolph, S.C. (1994). Why not to do two-species comparative studies: limitations on inferring adaptation. Physiological Zoology 67:797-828.

Palmer, D., ed. (1999). The Marshall Illustrated Encyclopedia of Dinosaurs and Prehistoric Animals. London: Marshall Editions. p. 26. ISBN 1-84028-152-9.

Peach, M.B. (2003). Inter- and intraspecific variation in the distribution and number of pit organs (free neuromasts) of sharks and rays. Journal of Morphology, 256: 89-102.

Wueringer, B.E. and Tibbetts, I.R. (2008). Comparison of the lateral line and ampullary systems   of two species of shovelnose ray. Rev Fish Biol Fisheries, 18:47-64.

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