Morphology and Function of the Drinking Apparatus in Hummingbirds

241 Pages·2016·17.36 MB·English

University of Connecticut
OpenCommons@UConn
Doctoral Dissertations University of Connecticut Graduate School
8-15-2014
Morphology and Function of the Drinking
Apparatus in Hummingbirds
Alejandro Rico-Guevara
University of Connecticut - Storrs, [email protected]
Follow this and additional works at:https://opencommons.uconn.edu/dissertations
Recommended Citation
Rico-Guevara, Alejandro, "Morphology and Function of the Drinking Apparatus in Hummingbirds" (2014).Doctoral Dissertations.
490.
https://opencommons.uconn.edu/dissertations/490
Morphology and Function of the Drinking Apparatus in Hummingbirds

Alejandro Rico-Guevara
University of Connecticut, 2014

My research aims to answer the questions: How do hummingbirds feed? And, how do the
mechanics of feeding define the limits and adaptive values of feeding behaviors? I meticulously
study every step of nectar capture and ingestion. My dissertation chapters are organized
following a morpho-functional and feeding sequence approach: 1) Feeding Apparatus
Morphology; with emphasis on the understudied morphology of the tongue grooves and bill
tongue coupling. 2) Tongue Tip Dynamics; how hummingbird tongues entrap nectar. 3) Tongue
Grooves Functioning: how the tongue acts as an elastic micropump while collecting nectar. 4)
Bill Tip Mechanics; internal bill structures that aid in offloading nectar from the tongue. 5)
Intraoral Transport: how the nectar flows inside the bill to the throat where it can finally be
swallowed.
My results demonstrate that capillarity equations are unsuitable to calculate energy
intake rate, which is the building unit of foraging theories; therefore a development of a new
theoretical framework to study hummingbird energetics and foraging ecology is needed. I
describe previously unknown methods of tongue-based nectar collection, report undocumented
tongue and bill structures, and offer the first test of intraoral transport hypotheses.
Alejandro Rico-Guevara – University of Connecticut, 2014

I followed the scientific
method cycle of deduction and
induction. To understand the
determinants of hummingbird
feeding mechanics in an
ecological context, I tested
biophysical model predictions
using data from wild birds.

Elucidating the drinking mechanism of hummingbirds will facilitate downstream
calculations of the rates at which birds can obtain nectar along several environmental axes (e.g.
altitudinal and latitudinal ranges, migrations, corolla morphology, etc.). This will in turn inform
how and where the limits of nectar uptake have shaped the distribution, ecology and evolution of
hummingbirds.

With their enchanting appeal and unique physical capabilities, hummingbirds captivate
people of all ages. As such, they serve as ambassadors to the natural world, fostering public
appreciation for scientific and conservation efforts aimed at preserving these fascinating birds,
and the biodiversity upon which they depend.
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Morphology and Function of the Drinking Apparatus in Hummingbirds

Alejandro Rico-Guevara
B.S. Biology, Universidad Nacional de Colombia, 2005

A Dissertation
Submitted in Partial Fulfillment of the
Requirements for the Degree of
Doctor of Philosophy
at the
University of Connecticut
2014
iii
Copyright by

Alejandro Rico-Guevara

2014
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ACKNOWLEDGEMENTS

To my wife, Kristiina Hurme, for unconditional support and insightful contributions to
this dissertation. I am deeply indebted to my parents, Lorenzo Rico and Magdalena Guevara for
all their assistance, as well as to my extensive and fabulous family. This work would not have
been possible without the guidance of my advisor, Margaret Rubega, and committee, Rob
Colwell, Kurt Schwenk, Tai-Hsi Fan and Carl Schlichting. Special thanks to Diego Sustaita for
being a role model and for all his invaluable help on my projects. To Gary Stiles for having
infected me with his passion for hummingbirds and for his constant encouragement. I thank Jesse
Joy, Briana Lechkun, Sebastian Aragon, Catalina Peña, Miguel Ángel Muñoz, Andrea Morales,
Laura Cárdenas, Orlando Acevedo and Edward Hurme for assistance in the field, as well as
Kelsey O’Connor and Jessica Attalah for help organizing data and measuring videos. Thanks to
Jon Velotta, James Mickley, Daniel Field, Chris Elphick, Chris Field, Holly Brown, Kevin
Burgio, Maude Baldwin, Bill Ryerson, the Ornithological Research Group and the Vertebrate
Biology Seminar at UConn for helpful discussions and feedback. I am grateful to Chris Clark,
Doug Altshuler, and Rick Prum for the loan of high-speed cameras and logistic support. Thank
you to Marie Cantino and Steve Daniels for their help with histological sectioning and electron
microscopy. Infinite thanks to all the curators of the bird collections I visited during the last five
years, and the EEB offices Staff for their kindness and willingness to help. And to the reader of
this dissertation since it is one of my utmost gratifications to share science with others avid for it.
My work was supported by the UConn EEB Department, Fulbright, Colciencias,
Colfuturo, Center for Environmental Sciences and Engineering, American Ornithologists’ Union,
Sigma Xi, and NSF, Division of Integrative Organismal Systems, DDIG 1311443.
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TABLE OF CONTENTS

Chapter 1: Ultrastructure and three-dimensional microanatomy of hummingbird tongues

Abstract………………………………………………………………………………… 1
Introduction……………………………………………………………………………… 2
Methods………………………………………………………………………………… 4
Results………………………………………………………………………………… 11
Discussion……………………………………………………………………………… 23
Literature Cited………………………………………………………………………… 36
Supplementary Figures………………………………………………………………… 46
Supplementary Movies………………………………………………………………… 58
Supplementary Tables………………………………………………………………… 60

Chapter 2: The hummingbird tongue is a fluid trap, not a capillary tube

Abstract………………………………………………………………………………… 62
Introduction…………………………………………………………………………… 63
Methods………………………………………………………………………………… 66
Results………………………………………………………………………………… 67
Discussion……………………………………………………………………………… 71
Literature Cited………………………………………………………………………… 80
Supplementary Movies………………………………………………………………… 84
Supplementary Tables………………………………………………………………… 88
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Chapter 3: Hummingbird tongues are elastic micropumps

Abstract………………………………………………………………………………… 89
Introduction…………………………………………………………………………… 90
Methods………………………………………………………………………………… 99
Results………………………………………………………………………………… 101
Discussion…………………………………………………………………………… 107
Literature Cited……………………………………………………………………… 113
Supplementary Figures……………………………………………………………… 117
Supplementary Movies……………………………………………………………… 126
Supplementary Tables………………………………………………………………… 130

Chapter 4: Hummingbird bill tips function as tongue wringers

Abstract……………………………………………………………………………… 131
Introduction…………………………………………………………………………… 132
Methods……………………………………………………………………………… 136
Results………………………………………………………………………………… 140
Discussion…………………………………………………………………………… 150
Literature Cited……………………………………………………………………… 160
Supplementary Figures……………………………………………………………… 164
Supplementary Movies……………………………………………………………… 178
Supplementary Tables………………………………………………………………… 179
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Chapter 5: Intraoral transport of nectar in hummingbird bills

Abstract……………………………………………………………………………… 184
Introduction…………………………………………………………………………… 185
Methods……………………………………………………………………………… 193
Results………………………………………………………………………………… 201
Discussion…………………………………………………………………………… 211
Literature Cited……………………………………………………………………… 220
Supplementary Figures……………………………………………………………… 225
Supplementary Movies……………………………………………………………… 229
Supplementary Tables………………………………………………………………… 231

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