Graduation Year

2012

Document Type

Dissertation

Degree

Ph.D.

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Philip J. Motta, Ph.D.

Co-Major Professor

Robert E. Hueter, Ph.D.

Committee Member

Jelle Atema, Ph.D.

Committee Member

Stephen M. Deban, Ph.D.

Committee Member

Lynn B. Martin, Ph.D.

Keywords

electroreception, lateral line, olfaction, vision

Abstract

Multimodal sensory input directs simple and complex behaviors in animals. Most research to date has been limited to studies of individual senses rather than multiple senses working together, leading to important advances in our comprehension of the sensory systems in isolation, but not their complementary and alternative roles in difficult behavioral tasks, such as feeding. In the marine environment, a prey item might emit an odor, create a hydrodynamic disturbance, such as from gill movements or swimming, be visible to the predator, produce a sound, and/or produce a weak electrical field. Therefore, the goal of this study was to investigate the integration of olfaction, mechanoreception by the lateral line system, vision, and electroreception in a marine animal. Sharks were chosen as a model organism in which to investigate multisensory integration because of their sensitivity and acuity, the presence of the same suite of sensory modalities in all species, the availability of experimental animals from different species, habitats and ecologies, and the rich literature on sharks' prey capture behavior. Two approaches were used: controlled artificial stimuli, delivered to the animals, were used to determine the spatial and concentration characteristics of odor encounters that guide the initial orientation to an odor plume in the far field in a model elasmobranch, the smooth dogfish, Mustelus canis; and sensory deprivation was used to restrict the availability of natural cues emanating from live prey items in order to elucidate the complementary and alternating roles of the senses in detecting, tracking, orienting to, striking at, and ultimately capturing prey. In the latter experiments, three species of sharks from different ecological niches were investigated: benthic, suction-feeding nurse sharks (Ginglymostoma cirratum) that hunt nocturnally for fish; ram-biting bonnetheads (Sphyrna tiburo) that scoop crustaceans off the bottom of seagrass beds; and ram-feeding blacktip sharks (Carcharhinus limbatus) that rapidly chase down midwater teleost prey. In orienting to odor patches, bilateral time differences between the nares are more important than concentration differences, such that animals turn toward the side stimulated first, even with delayed pulses of higher concentration. This response would steer the shark into each oncoming odor patch, helping the animal maintain contact with an odor plume. Sensory deprivation experiments revealed similarities and differences among species in terms of which senses they choose to focus on for particular behaviors, likely as a result of differences in the environments that they hunt in, type of prey consumed, and foraging strategies used, as well as anatomical differences in the central nervous system and the sensory organs. In most cases, multiple senses can be used for the same behavioral task. Thus, sharks are capable of successfully capturing prey, even when the optimal sensory cues are unavailable, by switching to alternative sensory modalities, which indicates that feeding behavior is plastic. Nurse sharks rely primarily on olfaction for detection. Olfaction in combination with vision, the lateral line, or touch is required for tracking. Nurse sharks orient to prey using the lateral line, vision, or electroreception, but will not ingest food if olfaction is blocked. Capture is mediated by the electrosensory system or tactile cues. Bonnetheads normally detect prey using olfaction, rely on olfactory-based tracking until they are close to the prey, then vision to line up a strike, and finally electroreception to time the jaw movements for capture. They can detect, orient, and strike visually in the absence of olfactory cues. Blacktip sharks also detect prey using olfaction or vision. Olfaction is used in combination with vision or the lateral line system for tracking. Long-distance orientation and striking is visually mediated, but strike precision relies on lateral line cues and an increase in misses occurs when this system is blocked. In the absence of vision, short-range orientation and striking can occur using lateral line cues. Capture is mediated by electroreception or tactile cues. Collectively, these results were used to develop species-specific sensory hierarchies for shark feeding behavior in a captive environment, the first such hierarchies to cover a complete behavioral sequence in a vertebrate.

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