Graduation Year

2017

Document Type

Dissertation

Degree

Ph.D.

Degree Name

Doctor of Philosophy (Ph.D.)

Degree Granting Department

Biology (Integrative Biology)

Major Professor

Stephen Deban, Ph.D.

Committee Member

Daniel Huber, Ph.D.

Committee Member

Philip Motta, Ph.D.

Committee Member

Henry Mushinsky, Ph.D.

Keywords

feeding performance, morphology, prey capture, salamanders, trade-off

Abstract

Performance is an organism’s ability to accomplish a particular task or behavior, and morphology can have a major impact on the performance of an organism. Salamanders are ecologically diverse and can feed using a variety of behaviors depending on the environment in which feeding occurs. Feeding is accomplished through the use of the hyobranchial apparatus, which lies along the oropharynx, and this structure can have competing roles; in aquatic environments the apparatus is used for suction feeding and works to depress the floor of the mouth, but during terrestrial feeding this structure projects the tongue forward out of the mouth. Diverse morphologies of the hyobranchial apparatus enable varying degrees of feeding performance, both in aquatic and terrestrial environments. For my dissertation I have investigated the interactions, and possible functional trade-offs, of feeding morphology and performance in salamanders of Family Salamandridae. These salamanders are an ideal system for studying the interactions of morphology and performance across different environments because they have diverse ecology, being either fully aquatic, semi-aquatic, or terrestrial as adults, as well as differences in hyobranchial apparatus morphology. In these studies I have quantified the morphology and performance of seven salamandrid species feeding in aquatic (Chapter 2) and terrestrial (Chapter 3) environments to assess the links between these two parameters, as well as investigated the evolutionary patterns of feeding morphology, performance, and behavior across the Salamandridae (Chapter 4) to better understand the co-evolution of these traits across water-land transitions.

During aquatic feeding salamanders use rapid mouth opening and hyobranchial depression to expand the oropharynx and generate negative pressure, and fluid flow, into the mouth. I hypothesized that more robust hyobranchial apparatus would yield increased aquatic feeding performance in salamandrids. When compared to semi-aquatic newts, the fully aquatic species, Paramesotriton labiatus, had greater mineralization of the hyobranchial apparatus, as well as relatively narrower basibranchial and wider ceratobranchial I + II complexes. These morphological differences coincide with greater aquatic feeding performance. Kinematics from high-speed videography revealed that maximum mouth opening velocities and accelerations were approximately two and five times greater, respectively, in Paramesotriton, and hyobranchial depression acceleration was found to be approximately three times greater than in the semi-aquatic species Pleurodeles, Notophthalmus, Triturus, and Cynops. Using digital particle image velocimetry, peak and average fluid velocities generated in Paramesotriton during suction feeding events were found to be 0.5 m s-1 and 0.2 m s-1, respectively, doubling that of all semi-aquatic species. These findings reveal that specialized morphology increases aquatic feeding performance in a fully aquatic newt.

Salamanders use the hyobranchial apparatus and its associated musculature for tongue projection during terrestrial feeding. Hyobranchial apparatus composition and morphology vary across species and different morphologies are better suited for feeding in aquatic versus terrestrial environments. I hypothesized that differences in hyobranchial apparatus morphology and function result in functional trade-offs in feeding performance. Specifically I predicted that semi-aquatic and aquatic salamandrids with hyobranchial morphology suited for aquatic feeding would have lower performance, in terms of tongue-projection distance, velocity, acceleration and power, compared to terrestrial salamandrids when feeding in a terrestrial environment. I found that semi-aquatic and aquatic newts had lower tongue projection performance when compared to the terrestrial salamanders Chioglossa lusitanica and Salamandra salamandra. The fully aquatic newt, Paramesotriton labiatus, has a robust, heavily mineralized hyobranchial apparatus and was unable to project its tongue during terrestrial feeding, and instead exhibited suction-feeding movements better suited for aquatic feeding. Conversely, terrestrial species have gracile, cartilaginous hyobranchial apparatus and enlarged tongue pads that coincided with greater tongue-projection distance, velocity, acceleration, and power. Chioglossa exhibited extreme tongue-projection performance, similar to that seen in elastically projecting plethodontid salamanders; muscle-mass-specific power of tongue projection exceeded 2200 W kg-1, more than 350 times that of the next highest performer, Salamandra, which reached 6.3 W kg-1. These findings reveal that two fully terrestrial salamandrids have morphological specializations that yield greater tongue-projection performance compared to species that naturally feed in both aquatic and terrestrial environments.

Salamanders of the Salamandridae that feed in both aquatic and terrestrial environments employ different behaviors depending on the environment. Using phylogenetic comparative methods, I assessed the relationships between feeding morphology, kinematics, and performance, and the ecology and feeding behavior of salamandrids. I also examined the co-evolution of feeding morphology and performance within Family Salamandridae. Behavior appears to co-evolve with feeding musculature, velocity of feeding movements, and fluid velocity produced during aquatic feeding. Flow velocity produced during aquatic feeding was related to the cross-sectional area of the rectus cervicis muscles, which rapidly depress the hyobranchial apparatus during suction feeding. Salamandrids with greater cross-sectional area of these depressor muscles generate faster flow velocity in aquatic feeding. Conversely, the evolution of hyobranchial apparatus morphology is more closely linked to ecology than to behavior. These findings indicate that both behavior and ecology are important for understanding the evolution of morphology and feeding performance across Family Salamandridae.

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