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The Extended
Specimen: Emerging
Frontiers in
Collections-based
Ornithological
Research
 STUDIES IN AVIAN BIOLOGY

A Publication of The American Ornithological Society

www.crcpress.com/browse/series/crcstdavibio

Studies in Avian Biology is a series of works founded and published by the Cooper Ornithological
Society in 1978, and published by The American Ornithological Society since 2017. Volumes in the
series address current topics in ornithology and can be organized as monographs or multi-authored
collections of chapters. Authors are invited to contact the Series Editor to discuss project proposals and
guidelines for preparation of manuscripts.

Series Editor
Kathryn P. Huyvaert, Colorado State University

Editorial Board
Lauryn Benedict, University of Northern Colorado
Bonnie Bowen, Iowa State University
Scott Loss, Oklahoma State University
Michael Patten, University of Oklahoma
Morgan Tingley, University of Connecticut

Science Publisher
Charles R. Crumly, CRC Press/Taylor & Francis Group
 Volume 50
Studies in Avian Biology
American Ornithological Society

The Extended
Specimen: Emerging
Frontiers in
Collections-based
Ornithological
Research
EDITED BY

Michael S. Webster
Cornell Lab of Ornithology
Cornell Universit y
Ithaca, NY
Cover photo by Mike McDowell: Magnolia Warbler (Setophaga magnolia). Pheasant Branch, Wisconsin, May 17, 2014 (spring
migration).

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Library of Congress Cataloging‑in‑Publication Data

Names: Webster, Michael S., (Ornithologist) editor.

Title: The extended specimen : emerging frontiers in collections-based ornithological research / editor,
Michael S. Webster.
Description: Boca Raton : Taylor & Francis, 2017. | Series: Studies in avian biology | Includes bibliographical
references.
Identifiers: LCCN 2016059788 | ISBN 9781498729154 (hardback : alk. paper)
Subjects: LCSH: Birds--Collection and preservation. | Birds--Research.
Classification: LCC QL677.7 .R65 2017 | DDC 598.072/3--dc23
LC record available at https://lccn.loc.gov/2016059788

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 CONTENTS

Contributors / vii 7 • W
 HAT BIRD SPECIMENS CAN REVEAL
ABOUT SPECIES-LEVEL DISTRIBUTIONAL
Preface / xi ECOLOGY / 111
A. Townsend Peterson and
1 • T HE EXTENDED SPECIMEN / 1 Adolfo G. Navarro-Sigüenza
Michael S. Webster 8 • U
 SING MUSEUM SPECIMENS TO STUDY
FLIGHT AND DISPERSAL / 127
2 • G
 ETTING UNDER THE SKIN: A CALL FOR
SPECIMEN-BASED RESEARCH ON THE Santiago Claramunt and Natalie A. Wright
INTERNAL ANATOMY OF BIRDS / 11
9 • T
 RANSFORMING MUSEUM SPECIMENS
Helen F. James INTO GENOMIC RESOURCES / 143
3 • A
 DVANCED METHODS FOR STUDYING John E. McCormack,
PIGMENTS AND COLORATION USING Flor Rodríguez-Gómez,
AVIAN SPECIMENS / 23 Whitney L. E. Tsai, and Brant C. Faircloth
Kevin J. Burns, Kevin J. McGraw,
Allison J. Shultz, Mary C. Stoddard, and 10 • M
 ETHODS FOR SPECIMEN-BASED
STUDIES OF AVIAN SYMBIONTS / 157
Daniel B. Thomas
Holly L. Lutz, Vasyl V. Tkach, and
4 • I NTEGRATING MUSEUM AND MEDIA Jason D. Weckstein
COLLECTIONS TO STUDY VOCAL
ECOLOGY AND EVOLUTION / 57 11 • S
 TUDENT-LED EXPEDITIONS AS AN
Nicholas A. Mason, EDUCATIONAL AND COLLECTIONS-
BUILDING ENTERPRISE / 185
Bret Pasch, Kevin J. Burns,
David W. Winkler, Teresa M. Pegan,
and Elizabeth P. Derryberry
Eric R. Gulson-Castillo,
5 • L
 EVERAGING DIVERSE SPECIMEN Joseph I. Byington, Jack P. Hruska,
TYPES TO INTEGRATE BEHAVIOR AND Sophia C. Orzechowski,
MORPHOLOGY / 75
Benjamin M. Van Doren, Emma I. Greig,
Kimberly S. Bostwick, Todd Alan Harvey,
and Eric M. Wood
and Edwin Scholes III
6 • E
 MERGING TECHNIQUES FOR ISOTOPE
STUDIES OF AVIAN ECOLOGY / 89
Anne E. Wiley, Helen F. James, and
Peggy H. Ostrom

v
12 • B
 IODIVERSITY INFORMATICS AND DATA 13 • O
 RNITHOLOGICAL COLLECTIONS
QUALITY ON A GLOBAL SCALE / 201 IN THE 21st CENTURY / 219
Carla Cicero, Carol L. Spencer, Michael S. Webster, Carla Cicero,
David A. Bloom, Robert P. Guralnick, John Bates, Shannon Hackett, and
Michelle S. Koo, Javier Otegui, Leo Joseph
Laura A. Russell, and John R. Wieczorek
Index / 233
Complete Series List / 239

vi Studies in Avian Biology NO. 50 Webster

 CONTRIBUTORS

JOHN BATES JOSEPH I. BYINGTON

Life Sciences Cornell University Museum of Vertebrates
Field Museum of Natural History Department of Ecology and Evolutionary Biology
1400 S. Lake Shore Drive Cornell University
Chicago, IL 60605 Ithaca, NY 14853
[email protected] [email protected]

DAVID A. BLOOM CARLA CICERO

Museum of Vertebrate Zoology Museum of Vertebrate Zoology
3101 Valley Life Sciences Building 3101 Valley Life Sciences Building
University of California University of California
Berkeley, CA 94720-3160 Berkeley, CA 94720-3160
[email protected] [email protected]

KIMBERLY S. BOSTWICK SANTIAGO CLARAMUNT

Cornell University Museum of Vertebrates Department of Natural History
Department of Ecology and Evolutionary Biology Royal Ontario Museum
Cornell University Toronto, Canada
Sapsucker Woods Road
Ithaca, NY 14850 ELIZABETH P. DERRYBERRY
[email protected] Department of Ecology and Evolutionary Biology
Tulane University
KEVIN J. BURNS 400 Lindy Bogs
Department of Biology New Orleans, LA 70118
San Diego State University [email protected]
5500 Campanile Drive
San Diego, CA 92182-4614
[email protected]

vii
BRANT C. FAIRCLOTH HELEN F. JAMES
Department of Biological Sciences Department of Vertebrate Zoology
Museum of Natural Science National Museum of Natural History
202 Life Sciences Building Smithsonian Institution
Louisiana State University P.O. Box 37012, MRC 116
Baton Rouge, LA 70808 Washington, DC 20013-7012
[email protected] [email protected]

EMMA I. GREIG LEO JOSEPH

Cornell Laboratory of Ornithology Australian National Wildlife Collection
Cornell University CSIRO National Facilities and Collections
Ithaca, NY 14853 GPO Box 1700
[email protected] Canberra, ACT 2601 Australia
[email protected]
ERIC R. GULSON-CASTILLO
Cornell University Museum of Vertebrates MICHELLE S. KOO
Department of Ecology and Evolutionary Biology Museum of Vertebrate Zoology
Cornell University 3101 Valley Life Sciences Building
Ithaca, NY 14853 University of California
[email protected] Berkeley, CA 94720-3160
[email protected]
ROBERT P. GURALNICK
Department of Natural History HOLLY L. LUTZ
Florida Museum of Natural History Department of Surgery
358 Dickinson Hall University of Chicago
University of Florida 5841 S. Maryland Avenue
Gainesville, FL 32611 Chicago, IL 60637
[email protected] [email protected]

SHANNON HACKETT and

Life Sciences
Field Museum of Natural History Department of Population Medicine and
1400 S. Lake Shore Drive Diagnostic Sciences College of Veterinary
Chicago, IL 60605 Medicine
[email protected] Cornell University
Ithaca, NY 14853
TODD ALAN HARVEY
Peabody Museum and
Yale University
New Haven, CT Lab of Ornithology
[email protected] Cornell University
159 Sapsucker Woods Road
JACK P. HRUSKA
Ithaca, NY 14850
Department of Ecology and Evolutionary Biology
University of Kansas NICHOLAS A. MASON
Lawrence, KS 66045 Department of Ecology and Evolutionary Biology
[email protected] Cornell University
Corson Hall, 215 Tower Road
Ithaca, NY 14853
[email protected]

viii Studies in Avian Biology NO. 50 Webster

JOHN E. MCCORMACK TERESA M. PEGAN
Moore Laboratory of Zoology Cornell University Museum of Vertebrates
Occidental College Department of Ecology and Evolutionary Biology
1600 Campus Rd Cornell University
Los Angeles, CA 90041 Ithaca, NY 14853
[email protected] [email protected]

KEVIN J. MCGRAW A. TOWNSEND PETERSON

School of Life Sciences Biodiversity Institute
Arizona State University University of Kansas
Tempe, AZ 85287-4501 Lawrence, Kansas 66045
[email protected] [email protected]

ADOLFO G. NAVARRO-SIGÜENZA FLOR RODRÍGUEZ-GÓMEZ

Museo de Zoología Moore Laboratory of Zoology
Facultad de Ciencias Occidental College
Universidad Nacional Autónoma de México 1600 Campus Rd
Circuito Exterior Los Angeles, CA 90041
Ciudad Universitaria [email protected]
Mexico City 04510, Mexico
[email protected] LAURA A. RUSSELL
Biodiversity Institute
SOPHIA C. ORZECHOWSKI and Natural History Museum
Department of Wildlife Ecology and Conservation 1345 Jayhawk Boulevard
University of Florida University of Kansas
Gainesville, FL 32611 Lawrence, KS 66045
[email protected] [email protected]

PEGGY H. OSTROM EDWIN SCHOLES III

Department of Integrative Biology Macaulay Library
Ecology, Evolutionary Biology, and Behavior Johnson Center for Birds and Biodiversity
Program Sapsucker Woods Road
Michigan State University Museum Ithaca, NY 14850
203 Natural Science Building [email protected]
Michigan State University
East Lansing, MI 48824 ALLISON J. SHULTZ
[email protected] Department of Organismic and Evolutionary
Biology
JAVIER OTEGUI Museum of Comparative Zoology
Department of Natural History Harvard University
Florida Museum of Natural History 26 Oxford Street
358 Dickinson Hall Cambridge, MA 02138
University of Florida [email protected]
Gainesville, FL 32611
[email protected] CAROL L. SPENCER
Museum of Vertebrate Zoology
BRET PASCH 3101 Valley Life Sciences Building
Department of Biological Sciences University of California
Northern Arizona University Berkeley, CA 94720-3160
617 S. Beaver Street [email protected]
Flagstaff, AZ 86011
[email protected]

Contributors ix
MARY C. STODDARD JASON D. WECKSTEIN
Department of Ecology and Evolutionary Biology Academy of Natural Sciences of Drexel University
Princeton University Ornithology Department
Princeton, NJ, 08544 Department of Biodiversity, Earth, and
[email protected] Environmental Sciences
Drexel University
DANIEL B. THOMAS 1900 Benjamin Franklin Parkway
Institute of Natural and Mathematical Sciences Philadelphia, PA 19103
Massey University [email protected]
Auckland 0632, New Zealand
[email protected] JOHN R. WIECZOREK
Museum of Vertebrate Zoology
VASYL V. TKACH 3101 Valley Life Sciences Building
Department of Biology University of California
University of North Dakota Berkeley, CA 94720-3160
10 Cornell Street STOP [email protected]
Grand Forks, ND 58202
[email protected] ANNE E. WILEY
Department of Biology
WHITNEY L. E. TSAI University of Akron
Moore Laboratory of Zoology 185 East Mill Street
Occidental College Akron, OH 44325-3908
1600 Campus Rd [email protected]
Los Angeles, CA 90041
[email protected] DAVID W. WINKLER
Cornell University Museum of Vertebrates
BENJAMIN M. VAN DOREN Department of Ecology and Evolutionary Biology
Edward Grey Institute of Field Ornithology Cornell University
Department of Zoology Ithaca, NY 14853
University of Oxford [email protected]
South Parks Road
Oxford OX1 3PS UK ERIC M. WOOD
[email protected] Department of Biological Sciences
California State University
MICHAEL S. WEBSTER Los Angeles, CA 90032
Cornell Lab of Ornithology [email protected]
Cornell University
159 Sapsucker Woods Road NATALIE A. WRIGHT
Ithaca, NY 14850 Division of Biological Sciences
[email protected] University of Montana
32 Campus Dr., HS104
Missoula, MT 59812
[email protected]

x Studies in Avian Biology NO. 50 Webster

 PREFACE

The dawn of the 21st century has seen a broad- were to survey the many uses of traditional orni-
ening gap between views of ornithological and thological specimens, to illustrate new technolo-
other biological collections. On the one hand, gies for using them in modern-day research,
these collections and the specimens they contain and to introduce the concept of the “extended
are recognized by many as central to modern-day specimen”—a constellation of specimen and
research ranging from ecology through functional data types that jointly add research value to each
anatomy to genomics. Indeed, dramatic new tech- other. At the conclusion of that symposium, I was
nical advancements have diversified the types of approached by Brett Sandercock, who at that time
specimens that we can collect and preserve, and was Series Editor for the Studies in Avian Biology
have opened new doors to the types of questions series. Brett suggested that the symposium might
that can be answered with both traditional and make a useful contribution to that series, and so
new specimen types. Accordingly, to many, this the concept for this volume was hatched.
century heralds expanding potential for collections-­ The intent of this volume is very much in line
based ornithological research. On the other hand, with the original AOU/COS symposium: to intro-
the broader public, and even many in the scien- duce both professional and amateur ornithologists
tific research community, appear to view biologi- to the many modern-day uses of ornithological
cal collections as something of a holdover from a research collections, and thereby bridge the per-
bygone age of discovery. Many picture museum ception gap regarding their scientific value. The
collections as arcane repositories of dusty old authors of the various chapters hope to inspire
specimens, and this view has fueled opposition creative young minds to use specimens and asso-
from some to modern specimen collecting. This ciated data in exciting new ways to address ever
opposition, in turn, has led to increasing chal- more challenging research questions. At the same
lenges for modern collections, and a seismic shift time, we hope to encourage and support those in
away from research for many. charge of ornithological collections to embrace
The growing disconnect between the perceived the concept of the extended specimen, thereby
and actual research value of ornithological col- further broadening the research impact of those
lections led to a symposium, held at the Joint collections. Happily, many in the collections com-
Meeting of the American Ornithologists’ Union munity have been thinking in this way for years,
(AOU) and Cooper Ornithological Society (COS) and have been growing their own collections and/
in August 2013, which was hosted—appropriately or building strategic partnerships to include new
enough—by the Field Museum of Natural History specimen and data types that have historically
in Chicago, Illinois. The goals of that symposium fallen somewhat outside of most ornithological

xi
collections. This volume celebrates those efforts authors of chapters in this volume. The Local
and encourages more. Finally, we aim to help the Committee, particularly John Bates, was instru-
broader public understand that, rather than being mental in making that symposium a reality. Brett
dusty old drawers filled with specimens of ques- Sandercock encouraged us to publish the sympo-
tionable research value, ornithological collections sium as a volume in the Studies in Avian Biology
are dynamic centers of modern-day research, uti- series, and Kate Huyvaert picked up the baton to
lizing cutting-edge methods drawn from across help make that happen when she took over as
the scientific spectrum to help us understand and Series Editor. Thanks to Chuck Crumly at CRC Press
preserve the diversity of life on our planet. for pushing this project along with appropriate
This volume would not have been possible with- carrots and sticks. Most of all, thanks to the many
out the help and input of many. I wish to thank my researchers and staff working hard to expand our
co-organizers of the AOU/COS symposium—​Kim ornithological collections to meet the opportuni-
Bostwick, Edwin Scholes III, and David Winkler—for ties and challenges of research in the 21st century.
pulling together that original collection of presen-
tations. Thanks also, of course, to the participants MICHAEL S. WEBSTER
in that original symposium, many of whom are Ithaca, New York

xii Studies in Avian Biology NO. 50 Webster

 Chapter ONE

The Extended Specimen*

Michael S. Webster

Abstract. The purpose of biological research col- specimens (study skins), as well as new speci-
lections is to preserve and make accessible speci- men and data types, now make this possible. The
mens that capture the individual phenotype for “extended specimen” is a constellation of speci-
research on the patterns of biodiversity across men preparations and data types that, together,
taxa, time, and space. In ornithology, the most capture the broader multidimensional pheno-
common specimen type is the “study skin,” type of an individual, as well as the underly-
which primarily captures the outward appear- ing genotype and biological community context
ance of the individual. That outward appear- from which they were sampled. Ornithological
ance, though, is just one aspect of a complex collections are now growing to embrace these
multidimensional phenotype. The research specimen and data types, which creates enor-
value of ornithological collections is enhanced mous potential for specimen-based research in
when they include specimen types and data the 21st century.
that capture other aspects of the phenotype and
its underlying genotype. Fortunately, recent Key Words: biodiversity media, ornithology, research
advances that make new use of traditional collections, specimens.

O
rnithological collections preserve and that preserves the outward appearance of the bird
make accessible specimens that capture while discarding most other “skin-in” parts of the
the phenotypic variation of birds: varia- bird’s anatomy. Numerous studies in the past have
tion across taxonomic boundaries (species and used study skins to examine and explore variation
subspecies), across space (geographic locations in features such as plumage coloration, molt pat-
and populations), and across time (collecting terns, and size/shape of external anatomical fea-
events). As such, these specimens have been used tures (e.g., tarsus, wing, or bill). Such studies are
to explore a host of questions central to under- sometimes used to define species/subspecies lim-
standing the ecology, evolution, and conservation its (i.e., alpha taxonomy), to explore clinal varia-
of birds (Chapter 13, this volume). The most typi- tion associated with ecology or other factors, to
cal type of specimen in these ornithological col- understand the selective factors that have shaped
lections is, by far, the “study skin” (Chapter 2, this the external anatomy of birds, and to address a
volume), which is essentially a cotton-stuffed skin broad range of other questions. Accordingly,

* Webster, M. S. 2017. The extended specimen. Pp. 1–9 in M. S. Webster (editor), The Extended Specimen: Emerging Frontiers
in Collections-based Ornithological Research. Studies in Avian Biology (no. 50), CRC Press, Boca Raton, FL.

1
study skins have been—and continue to be—an tissue-specific gene expression, molecular
invaluable source of data for ornithological stud- microstructure of feathers, internal anatomy,
ies (Bates et al. 2004, Joseph 2011, Clemann et al. and physiological processes are all aspects of
2014, Rocha et al. 2014). the phenotype that cannot be easily discerned
Yet these traditional ornithological specimens with the naked eye. Moreover, these pheno-
also are somewhat limited because they do not typic attributes of the individual organism can
capture all aspects of the phenotype, which also affect the phenotype of other organisms, as
is complex and multidimensional. Over three when Sociable Weaver (Philetairus socius) nesting
decades ago, Dawkins (1982) introduced the con- colonies become the nesting substrate for other
cept of the extended phenotype, his main idea being birds (Maclean 1973), or when young exhibit
that genes have phenotypic effects that stretch traits that increase feeding rates from the par-
beyond the body of the individual organism. ents (e.g., Lyon et al. 1994, Wright and Leonard
As Dawkins argued, defining the phenotype as 2002), even when those parents are a different
merely the anatomical features of the individual species (e.g., Kilner et al. 1999).
(external or otherwise) is arbitrary and limiting, If the central mission of ornithological col-
as that definition excludes other important fea- lections is to preserve specimens that capture
tures of the phenotype. Take, for example, bird the phenotypic diversity of birds across space
nests. These structures all serve essentially the and time, then a broader concept is needed with
same purpose across birds—to protect the eggs regard to what those specimens are. We need to
from environmental conditions such as weather think more broadly about the multidimensional
and predators—yet the diversity of these struc- individual phenotype, and to preserve in our
tures is stunning (Collias and Collias 1984). ornithological collections those specimen types,
Moreover, the nest is a physical manifestation of associated assets, and data that capture that phe-
the parent bird’s behavior (Clutton-Brock 1991), notype. We need specimen types that preserve
is shaped by the interaction of genes and envi- phenotypic traits that are not easily discernable
ronment (Muth and Healy 2011; Hoi et al. 2012; from the outward appearance of a bird. We need
Hall et al. 2013, 2014), is adapted to local envi- an extended specimen that captures the extended phenotype
ronmental conditions (Crossman et al. 2011, (Figure 1.1).
Mainwaring et al. 2014), and evolves over time in Fortunately, recent technological and analytical
response to selective pressures (e.g., Collias 1997, developments now make it possible to collect, cat-
Winkler and Sheldon 1993, Irestedt et al. 2006, alog, and use the information that comprises the
Hall et al. 2015). Yet the nest itself lies well outside extended specimen. We currently are witnessing
of the organism’s actual body, and hence would a renaissance in collections-based ornithological
be excluded from overly restrictive definitions of research that embraces a broader concept for the
the phenotype. types of specimens and data that can be preserved
Dawkins’s (1982) concept proved highly influ- in our collections (Chapter 13, this volume). These
ential, but also highly controversial, particularly new technological and analytical approaches have
with respect to its strong advocacy for a gene- opened the gates to a broad diversity of questions
centric view of evolution that ignores polygenic that lay somewhat outside traditional concepts
and gene-by-environment interactions (e.g., see of collections-based research. In some cases, the
Dawkins 2004, Jablonka 2004, Turner 2004). “new” developments began decades ago and are
But the starting premise of Dawkins’s assertion now accumulating a track record of research suc-
remains intact and relevant: the phenotype of an cesses. In other cases, the new developments are
organism, whether it be the product of gene(s) just now getting their start, but hold enormous
or environment or a combination of the two, is potential for future research. The various chapters
more than just that organism’s outward appear- in this volume detail several different areas where
ance. For example, behavioral attributes such as ornithological specimens—both traditional and
nest structure, male courtship displays, foraging new—are being used in exciting new ways to
strategies, and parental care are all manifesta- broaden and deepen our understanding of birds
tions of the individual phenotype, produced and biodiversity, and to conserve that biodiversity
by the interaction of genotype and environ- in the face of ever-increasing anthropogenic pres-
ment, and yet are not anatomical. Similarly, sure. This chapter provides a brief introduction to

2 STUDIES IN AVIAN BIOLOGY NO. 50 Webster

 e

P 2
n 1H

5
4
3
kHz

2
1
0
1 2
Time (sec)

Figure 1.1. The “extended specimen” is a constellation of specimen and data types that, in combination, capture the
multidimensional phenotype (and genotype) of an individual. At the center is a traditional “study skin” that captures
the external morphology. Across the top are images depicting specimens and extracts that capture other dimensions of
the phenotype (left to right): a spread wing, DNA extracted from the study skin or a separately preserved subsample,
chemical isotopes (e.g., deuterium) also extracted from the specimen tissue, a malarial parasite among healthy red blood
cells, and an ectoparasitic louse collected from a specimen during preparation. Across the bottom are other specimen
and data types that capture still other dimensions of the phenotype (left to right): a CT scan of the internal morphology
(made from a fluid-preserved specimen), iridescent feathers that can be used for photospecrometric analyses of reflectance,
a range map developed from specimen metadata, an acoustic spectrogram of a vocalization, and a frame from a video
depicting a courtship display. In principle, most or all of these various specimen and data types could be collected from a
single individual (e.g., audio and video recordings could be taken before the bird is collected, and parasites can be collected
during specimen preparation), and so would be tied together by their association with the physical study skin and with
each other. It is also possible that some specimen/data types would be collected from individuals that are not prepared as
physical specimens; for example, audio and video recordings or DNA samples might be collected from individuals from
the same population/location but that were not sacrificed. This figure illustrates the conceptual connections between
specimen types, rather than actual connections, as in this case the specimens/data depicted were not collected from the
same individual. Actual images shown are as follows: the center study skin is a Spectacled Weaver (Ploceus ocularis suahelicus
FMNH441159; photo by Holly Lutz); the spread wing is from a Striped Wren-Babbler (Kenopia striata; photo by Reid Rumelt);
the endoparasite is a malarial parasite (Haemoproteus zosteropis ex. African Yellow White-eye, Zosterops senegalensis; photo by
Holly Lutz); the ectoparasite is an avian louse (Cotingacola lutzae ex. Cinereous Mourner, Laniocera hypopyrra; photo by Michel
Valim); the iridescent feathers are from a specimen of a Wahnes’s Parotia (Parotia wahnesi; photo by Edwin Scholes); the
CT scan is from a Black-and-yellow Broadbill (Eurylaimus ochromalus; CUMV44530; image courtesy of Eric Gulson); the map
depicts avifaunal species turnover in Mexico based on analyses of museum specimen records (reprinted with permission
from Peterson et al. 2015); the audio spectrogram is from a recording of a Northern Cardinal (Cardinalis cardinalis; Macaulay
catalogue #191165, recorded by Wilbur Hershberger in 2012); and the video frame is from a video of a Wahnes’s Parotia
(Macaulay catalogue #469255; filmed by Edwin Scholes and Tim Laman).

The Extended Specimen 3

the central concept of this volume: the extended Advanced methods for studying plumage col-
specimen (Figure 1.1). oration are only the tip of the iceberg, as other
developing technologies are similarly creating
new research uses for traditional study skins. A
EXTENDING THE TRADITIONAL SPECIMEN
prime example is extraction of chemicals from
Recent developments are broadening the utility small subsamples of a physical specimen, which
of ornithological specimens in two key ways. The can be used for isotopic studies that reveal hid-
first is by creating new uses for traditional physical den dimensions of the extended phenotype, such
specimens (i.e., study skins). Consider, for example, as movement patterns and diet (Chapter 6, this
studies of plumage coloration. Although museum volume). Similarly, traditional physical specimens
skins have long been used for studies of external such as study skins can also yield “ancient DNA”
morphology and coloration (e.g., West 1962, Rising for sophisticated population genetic and genomic
1970, Greenberg and Droege 1990), new technolog- studies, allowing us to explore phylogenetic rela-
ical advances have created unprecedented opportu- tionships and the genotypes that underlie pheno-
nities for addressing exciting new questions in this typic diversity at unprecedented levels of detail
area (Chapter 3, this volume). These techniques (Chapter 9, this volume). Finally, advances in the
include sophisticated and objective approaches to analysis of distributional data, as can be gleaned
measuring coloration (reflectance) of feathers that from the metadata associated with specimens
are pigmented or have non-iridescent structural col- (e.g., on the specimen tag), have transformed our
oration (e.g., Eaton and Lanyon 2003; Stoddard and ability to explore animal distributions and how
Prum 2008, 2011) as well as those that are iridescent these change over time (Chapter 7, this volume).
(Meadows et al. 2011), methods for measuring and The second way that we are now broadening
decomposing the patterns on birds’ eggs (Stoddard the utility and scope of specimen-based research is
and Stevens 2010), and methods for directly exam- through expansion of the types of specimen prep-
ining the pigments found in feathers (e.g., McGraw arations and other materials that are collected and
et al. 2005). A complementary but somewhat dif- preserved in ornithological collections. Although
ferent approach is the use of scanning and trans- specimen types such as skeletons and anatomical
mission electron microscopy (SEM and TEM, (fluid-preserved) specimens have been collected
respectively) to examine melanosomes and color- for many decades, the number of these specimens
producing nanostructures in feathers, the morphol- in our collections is dwarfed by the number of tra-
ogy and density of which affect the color produced ditional study skins (Chapter 2, this volume). New
(Prum 2006, Vinther et al. 2008). Remarkably, some techniques that allow for sophisticated 3D imag-
of these methods can be applied to fossil specimens ing and analysis of anatomy from micro- to mac-
as well as to specimens of extant species, leading roscales promise to revolutionize the analysis of
to discoveries about the coloration of long extinct internal anatomy and portend a dramatic increase
animals, such as dinosaurs and early birds (e.g., Li in the utility and collection of such specimens
et al. 2010, Vinther et al. 2016). Moreover, studies of (Chapter 2, this volume). Similarly, spread wing
integument of both extant and extinct species from preparations are currently rare in research collec-
museum specimens have shown that the physiolog- tions, yet these preparation types are extremely
ical mechanisms producing diverse melanin-based useful for analyses that can reveal, among other
coloration in modern birds arose abruptly with the things, important phenotypic traits such as flight
evolution of feathers themselves (Li et al. 2014). In behavior and dispersal ability (Chapter 8, this vol-
addition to shedding light on the mechanisms and ume). These various specimen types are rare com-
evolution of bird coloration, these methods have pared to traditional study skins, yet their value to
allowed researchers to address broader interdisci- exploring key patterns of avian biodiversity, now
plinary questions. For example, integrative stud- being unlocked by developing new methodolo-
ies of study skins from museum collections have gies, cannot be overemphasized.
recently shed light on the processes of coevolution,
the degree to which underlying mechanisms affect
EXTENDING THE SPECIMEN CONCEPT
evolutionary patterns, and the general rules govern-
ing the design of signals of individuality (see Maia The preceding discussion centers on new uses for
et al. 2013, Stoddard et al. 2014, Eliason et al. 2015). physical specimen types that have long had a home

4 STUDIES IN AVIAN BIOLOGY NO. 50 Webster

in ornithological collections, albeit only in small handling such media requires specialized infra-
numbers for some specimen types. Just as impact- structure and expertise that differs substantially
ful are other assets and data types that are mostly from that needed to handle physical specimens
just now finding their way into ornithological col- (Gaunt et al. 2005, Webster and Budney 2016).
lections as those collections expand the scope of As a result, most biodiversity media tend to be
the materials they curate and preserve. Although preserved and curated in collections that spe-
not “specimens” by the traditional meaning of cialize on such material, such as the Macaulay
the word, these assets capture key aspects of the Library at the Cornell Lab of Ornithology and the
extended phenotype that physical specimens sim- Borror Laboratory at Ohio State University (see
ply cannot. Accordingly, many ornithological col- Alström and Ranft 2003, Ranft 2004, Webster
lections are now becoming repositories for these and Budney 2016). Nonetheless, such media are
materials or are partnering with institutions that valuable to research on the extended phenotype,
have the expertise to handle them. and the institutions that house them are part of a
One prime example is “biodiversity media”: global network of ornithological collections that
audio recordings, video recordings, and still pho- is expanding in the 21st century.
tographs of living animals. Audiovisual recordings In addition to standard physical specimens,
of this sort can capture the behavioral phenotype some ornithological collections also preserve
of an individual, including its voice, courtship assets that are associated with, but not really a
displays, foraging techniques, and other behav- part of, an individual bird. Excellent examples
iors that cannot be discerned easily, if at all, from of this are nest and egg collections, such as those
examination of a physical specimen (Figure 1.2). found at the Museum of Vertebrate Zoology,
Accordingly, these media can be used for a mul- the Field Museum in Chicago, and the Peabody
titude of studies, such as those on the evolution Museum of Natural History at Yale University.
of acoustic (Chapter 4, this volume) and physi- Nests and eggs are not a part of a bird taken as
cal (Chapter 5, this volume) courtship displays. a specimen, but rather are things that birds pro-
Yet, with a few key exceptions (e.g., the Museum duce, and as such they serve as prime examples
of Vertebrate Zoology, University of California, of the extended phenotype. Eggs and nests also
Berkeley), few traditional ornithological collec- show staggering diversity across space and time,
tions currently preserve or curate biodiversity and the collections that house them allow for
media of this sort. In large part this is because detailed analyses of that diversity (e.g., Chapter 3,

Ptiloris magnificus
179.008.003

Figure 1.2. Physical specimen (study skin) of a Magnificent Riflebird (Ptiloris magnificus) from the Naturalis Biodiversity
Center, Leiden, Netherlands. A specimen such as this can yield data on phenotypic traits such as external morphology,
coloration, and molt, as well as DNA and chemicals for genetic and isotopic analysis. For “media specimens” that can be
used to study the behavioral phenotype of this same species, see http://macaulaylibrary.org/video/455444 and http://
macaulaylibrary.org/audio/173711.

The Extended Specimen 5

this volume). Similarly, some researchers are now temporal scales. Citizen science approaches side-
beginning to collect endo- and ectoparasites from step this constraint, and can be used for powerful
birds, including from birds collected as speci- and fine-grained analyses of distributions, includ-
mens, and these invertebrate specimens tell us a ing detailed analyses of contemporary change as
good deal about the birds from which they were populations adjust to anthropogenic pressures
collected (Chapter 10, this volume). Such samples (Pimm et al. 2014). Ornithological and other bio-
are typically deposited in appropriate invertebrate logical collections should embrace and work with
or entomological collections, and can be used to these “specimen-free” data, as these collections
study epidemiology, population health, coevolu- already have expertise in organizing and curating
tion, and a host of other questions focused on the large amounts of data. Indeed, incorporation of
biology of the avian hosts (as well as the parasites specimen-free data into traditional collections is
themselves) if linked to the physical specimen already beginning to happen. Many citizen sci-
with which they are associated. ence projects have originated from and/or are
Another category of “nontraditional” ornitho- housed at research collections that handle physi-
logical materials is data and other assets associated cal specimens: eBird, along with the Macaulay
with a specific collecting event. These materials Library and the Cornell Museum of Vertebrates,
can include information and photographs describ- is housed at the Cornell Lab of Ornithology;
ing the collecting locale, field notes about the col- and iNaturalist finds its home at the California
lecting event itself, or data about organisms in the Academy of Sciences in San Francisco. This trend
area that were not actually collected (e.g., count is likely to expand in the future, as ornithological
data and lists of bird species present in the area and other natural history collections expand their
but not collected). Such data can tell us a good own citizen science efforts, harnessing the power
deal about the populations and communities of of the crowd and blurring the distinction between
birds sampled. Although some larger collections specimens and data (Chapter 13, this volume).
have routinely preserved and maintained this
information for decades (e.g., collections of field
CONCLUSION: JUST WHAT IS THE
notebooks), the practice is now becoming more
routine as scanning and databasing technologies “EXTENDED SPECIMEN?”
have made the process simpler and more robust. These are exciting times for specimen-based orni-
Importantly, the collection and archiving of col- thological research. In recent years, other authors
lecting event data is being facilitated by the recent have written about the value of ornithological
explosion in observational databases such as eBird specimens and the important research oppor-
(Wood et al. 2011, Sullivan et al. 2014), which tunities that they bring (e.g., Suarez and Tsutsui
allows bird census data to be easily uploaded and 2004, Bates et al. 2004, Joseph 2011, Clemann
archived online, including observational data et al. 2014, Rocha et al. 2014). But the purpose of
gathered during a collecting event (Chapter 11, this brief essay—and the rest of this book—is to
this volume). illustrate the value of new approaches using spec-
Mechanisms like eBird are also lowering barri- imens to examine the broader extended pheno-
ers to participation in biodiversity data collection, type of birds and other organisms. New specimen
and have spurred an explosion in “citizen science” and data types, as well as new uses for traditional
projects (Bonney et al. 2014). Just as ornithologi- specimens, are now being harnessed to explore
cal specimens can provide important insights into variation in previously hidden aspects of the
bird distributions (Chapter 7, this volume) and avian phenotype. These approaches allow for
how they change over short periods of time (e.g., studies examining the causes and consequences
Peterson et al. 2015), eBird observations can be of phenotypic variation in both space and time,
used to explore the dynamics of bird distribu- including dynamic responses to anthropogenic
tions at contemporary timescales (Sullivan et al. pressures. The extended specimen is the sum of these
2009, Wood et al. 2011). Moreover, traditional various specimen and data types, which, together,
specimen-based approaches to such studies are by reveal key aspects of the extended phenotype of
their very nature coarse-grained, because collect- the individual (Figure 1.1).
ing expeditions are complicated and expensive, An important goal for the collections commu-
and so sampling occurs only at broad spatial and nity, then, is to embrace these diverse specimen

6 STUDIES IN AVIAN BIOLOGY NO. 50 Webster

and data types to make our research collections M. Shawkey, and D. Winkler for stimulating dis-
maximally useful for a broad array of future anal- cussions and comments (although they may not
yses, all aimed at a better understanding and con- agree with all of the opinions expressed here).
servation of birds. To do so, though, will require Brett Sandercock originally encouraged us to pub-
not just application of new methodologies and lish the symposium as a volume in the Studies in
collection of new specimen types, but also main- Avian Biology series, and Kate Huyvaert picked up
taining strong connections across associated spec- the baton to help make that happen. Holly Lutz
imens and data assets. Case studies given by Mason kindly created Figure 1.1. Thanks most of all to the
et al. (Chapter 4, this volume) and Bostwick et al. many researchers and staff working to expand our
(Chapter 5, this volume) illustrate well the power ornithological collections to meet the opportuni-
that comes from simultaneous analysis of physi- ties and challenges of research in the 21st century.
cal specimens and other assets collected from
the same populations or individuals. Similarly,
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icry of host eggs by the common cuckoo, as seen Wood, C., B. Sullivan, M. Iliff, D. Fink, and S. Kelling.
through a bird’s eye. Proceedings of the Royal 2011. eBird: engaging birders in science and con-
Society B 277:1387–1393. servation. PLoS Biology 9:e1001220.
Suarez, A. V., and N. D. Tsutsui. 2004. The value Wright, J., and M. L. Leonard. 2002. The evolution of
of museum collections for research and society. begging: competition, cooperation and communi-
BioScience 54:66–74. cation. Springer, New York, NY.

The Extended Specimen 9

http://taylorandfrancis.com
 Chapter TWO

Getting under the Skin

A CALL FOR SPECIMEN-BASED RESEARCH

ON THE INTERNAL ANATOMY OF BIRDS*

Helen F. James

Abstract. Study of the comparative internal anatomy scans enable the production of detailed computer
of birds is undergoing a renaissance, spurred by models of the bones for biometric and biome-
technological and methodological advances. Our chanical studies. Online repositories of morpho-
ability to image the soft anatomy and bones in 3D logical image files can make internal anatomy
using x-ray computed tomography (CT), magnetic widely accessible. Avian skeletal and anatomical
resonance imaging (MRI), and optical surface collections are far less comprehensive than tradi-
imaging has opened the door to a wide range of tional study skin collections, yet they represent a
analyses using avian skeletal and anatomical spec- wealth of relatively unexplored phenotypic varia-
imens. For anatomical specimens, simple staining tion in birds. The purpose of this chapter is to
techniques that enhance the contrast between dif- review and encourage the use of these techniques
ferent soft tissues, and at the same time raise the in the study of avian phenotypes, emphasizing the
opacity of soft tissues to x-rays, enable the simul- various specimen types that can be used as well
taneous 3D visualization of skeletal and soft tis- as the deeper understanding of the ecological and
sue anatomy. Image processing software further behavioral context of the phenotype that emerges
allows anatomical features such as individual from such studies.
muscles to be segregated and measured on a com-
puter monitor, without necessitating dissection of Key Words: anatomical specimens, avian paleontol-
the anatomical specimen. Perfusion techniques ogy, computed tomography, functional anatomy,
can allow the vascular or respiratory system to be geometric morphometrics, skeletons, spirit col-
similarly imaged. For the skeleton, CT and optical lections, 3D imaging.

* James, H. F. 2017. Getting under the skin: a call for specimen-based research on the internal anatomy of birds. Pp. 11–22 in
M. S. Webster (editor), The Extended Specimen: Emerging Frontiers in Collections-based Ornithological Research. Studies
in Avian Biology (no. 50), CRC Press, Boca Raton, FL.

11
A
dvances in instrumentation and meth- In consonance with the theme of this volume,
ods for studying vertebrate morphology I omit discussion of several important research
offer exciting new ways to reveal and areas that admittedly make good use of skeletal
analyze internal phenotypic variation in birds. and anatomical collections, but that do not aim
Emblematic of these advances are the captivat- specifically to understand the phenotype in an
ing 3D visualizations of internal anatomy that evolutionary or ecological context. Thus, I d­ iscuss
have recently appeared in a diversity of journals avian paleontology but not zooarchaeology, and I
(e.g., Figure 2.1). The primary tools employed to omit ancient biomolecules such as the gene frag-
create those images are computed tomography ments and proteins that are often preserved in skel-
(CT), magnetic resonance imaging (MRI), and etal and sometimes anatomical specimens. Good
laser or other optical surface scanning technolo- reviews are available on these topics, such as Wiley
gies, combined with software programs for cre- et al. (Chapter 6, this volume) for stable isotope
ating 3D images from the scans (Chatham and analysis of avian museum specimens, Wood and
Blackband 2001, Rosset et al. 2004, Goldman De Pietri (2015) for emerging ­paleo-ornithological
2007, Marshall and Stutz 2012). These approaches, techniques including the study of ancient bio-
together with a suite of other techniques, some molecules, and McCormack et al. (Chapter 9,
old and some new, have opened a frontier in our this volume) for genomic approaches that utilize
ability to see and study the insides of birds. specimens.
My objective in this chapter is to spur orni-
thologists to adopt these techniques, to incorpo-
AVIAN ANATOMICAL AND
rate internal anatomical traits more frequently
SKELETAL COLLECTIONS
in their study designs, and to collect the ana-
tomical specimens that make these stud- Traditional museum study skin collections lie at
ies possible. The chapter touches on topics in the heart of our knowledge about the species and
avian biology to which studies of skeletal and taxonomy of birds, their geographic distributions,
anatomical specimens principally contribute, plumages, and other external traits. The major sci-
and highlights emerging techniques in imag- entific collections of birds were built up primarily
ing, data gathering, and data analysis that can from the 1880s through the 1960s (Winker 1996,
facilitate research using those collections. I also Livezey 2003), a period when much ornithological
offer brief comments on the readiness of avian research effort was devoted to establishing basic
skeletal and anatomical collections to fulfill this information about the systematics and biogeogra-
research mission. phy of the world’s birds. The avian study skin was

Figure 2.1. Visualization of the cranial vasculature of an American Flamingo (Phoenicopterus ruber), created by injecting a
latex/barium medium into the vasculature and producing a CT scan. (From Holliday et al. 2006.)

12 Studies in Avian Biology  NO. 50 Webster

adopted early on as a common unit of comparison which are anything other than a study skin. It
for this research, a unit that was also conveniently almost goes without saying that the phenotypic
fungible for curators engaged in trades with other variation that lies beneath the skin of birds has not
institutions. When, in the 1960s and 1970s, the been studied to nearly the same extent as has the
attention of ornithologists turned increasingly to variation observable in study skins, particularly
ecology, the study skin was still the specimen of when it comes to intrageneric and intraspecific
choice because it preserved external traits of birds ­patterns. Thus, specimens that capture the inter-
that could be compared with those of birds stud- nal anatomy of birds can be considered as part of
ied in the field. the “extended specimen” that is the focus of this
A consequence of this love for the beautiful book (see Chapter 1, this volume).
study skin is that collectors of birds have preserved
far fewer skeletal and anatomical specimens than
COMPARATIVE ANATOMY
skins. As an example, at the National Museum of
Natural History (NMNH; Washington, DC), the The comparative study of avian anatomy, tra-
avian holdings fall out as roughly 84% study skins ditionally based on dissection and histology,
representing 75% of the world’s species, but only has fallen into a relatively quiet period in recent
11% skeletons representing 54% of the species and decades (Livezey 2003), although certainly some
5% anatomical specimens representing 44% of the notable work has continued to appear (e.g., Moreno
species; eggs and nests are excluded from these and Carrascal 1993, Patak and Baldwin 1998,
calculations. The skeletal and anatomical holdings Maxwell and Larsson 2007). The rise in interest in
at NMNH are the most comprehensive anywhere, avian ecology and behavior, and the supplanting
yet they continue to lag far behind the study skin of comparative anatomy with molecular genetics
collection, even though, in recent decades, the in the field of systematics, must partly account for
curators at NMNH have placed a priority on clos- this. The result has been that fluid-preserved avian
ing those gaps (Figure 2.2). The emphasis on study specimens have by and large been languishing in
skins for alpha taxonomy is further highlighted their jars, and curators have received very few
by the composition of avian type collections. requests for their use. Yet this situation is begin-
Again using the NMNH as an example, 3,971 type ning to reverse itself, and anatomical specimens
specimens are in the bird collection, only five of are coming back in demand thanks to exciting

70

60
Thousands of specimens

50

40

30

20

10

0
18 0
18 0
18 0
18 0
18 0
18 0
18 0
19 0
19 0
19 0
19 0
19 0
19 0
19 0
19 0
19 0
19 0
20 0
20 0
10
2
3
4
5
6
7
8
9
0
1
2
3
4
5
6
7
8
9
0
18

Decade

Skins Eggs Nests Skeletons Anatomicals

Figure 2.2. Bird specimens added to the scientific collection of the National Museum of Natural History, Smithsonian
Institution, by decade and specimen type. The 2010 time bin represents the first half of the decade.

Getting under the Skin 13

developments in imaging and computer-based fluid-preserved anatomical specimens of small
analytical methods. animals with iodine or iodine potassium iodide
Some recent examples of this trend include (I2KI) to enhance the contrast between soft tis-
studies of the vascular system of the head of sues, such as individual muscles and organs, in
­flamingoes that revealed a previously unknown CT scans. A mineral stain like iodine also raises
paralingual sinus that may be part of the fi ­ lter the opacity of soft tissues to x-rays, making them
feeding mechanism (Holliday et al. 2006), a study similar enough to bone in opacity that bones and
of the anatomy of the knee joint of ostriches soft anatomy can be visualized in a single CT scan.
that detailed the skeletomuscular system associ- This simple but exciting insight about the advan-
ated with their unusual second patella (Chadwick tages of iodine-based staining facilitates simul-
et al. 2014), and a study of the tongue apparatus taneous visualization and precise measurements
of waterfowl that characterized anatomical dif- of the soft anatomy and skeleton in 3D. It opens
ferences between grazers and filter-feeders and the door to detailed anatomical and biomechani-
used them to interpret key fossil anatids (Li cal investigations of fluid-preserved specimens,
and Clarke 2015). Each of these studies used CT with traditional dissection and histology needed
scanning to create 3D anatomical models. In
­ only to confirm the computer-based interpreta-
the flamingo study, a barium/latex medium was tions. Further experiments on iodine-based stain-
injected into the carotid artery and jugular vein to ing of anatomical specimens for CT scanning have
produce spectacular scans of the vascular s­ystem refined the methods and adapted them for use
(Figure 2.1). In the ostrich study, MRI was used to with larger animals (e.g., Gignac and Kley 2014,
visualize the muscular system and CT to image the Li et al. 2015).
bones of the knee joint. Finally, the study of the
tongue apparatus in waterfowl imaged both bones
SYSTEMATICS OF EXTANT SPECIES
and muscles simultaneously, using CT scanning
enhanced with iodine-based perfusion staining Skeletons and anatomical specimens have long
of the whole specimen. It was then possible to played a strong role in avian systematics. In clas-
segment the individual muscles using computer sic taxonomies, higher categories of birds were
models and create a 3D, in situ, virtual dissec- arranged in part based on a small number of
tion (Figure 2.3). This technique is part of a important anatomical traits, drawn, for example,
revolution sparked by Metscher (2009), who from the hind-limb myology and configuration of
highlighted the advantages of staining whole palatal bones (e.g., Fürbringer 1888, Gadow 1892).

Pg
Mha Mha

Bh Miv Mho
Mid Miv Mid
Uh Mst
Mic Msp Msp
Mcg
Cb
Mss Mss

Ep Mbm
Mbm
(a) (b) (c) (d)

Figure 2.3. Virtual dissection of the tongue apparatus in a Canada Goose (Branta canadensis), created by segmenting individual
muscles in enhanced-contrast CT scans. Dorsal (a, b) and ventral (c, d) views. Abbreviations: Bh, basihyal; Cb, ceratobran-
chial; Ep, epibranchial Pg, paraglossal; Uh, urohyal; Mbm, M. branchiomandibularis; Mcg, M. ceratoglossus; Mha, M. hyo-
glossus anterior; Mho, M. hyoglossus obliquus; Mic, M. interceratobranchialis; Mid, M. intermandibularis dorsalis; Miv, M.
intermandibularis ventralis; Msp, M. serpihyoideus; Mss, M. stylohyoideus; Mst, M. stylohyoideus. (From Li and Clarke 2015.)

14 Studies in Avian Biology  NO. 50 Webster

Other authors took a fine-scale approach, using selection (see Chapter 5, this volume). Riede et al.
comparative myology and osteology to inform the (2015) examined the myology and histology of
classification of all taxa within a group or clade, the syrinx in male Pectoral Sandpipers (Calidris
such as in Raikow’s (1993) study of woodcreep- melanotos), detailing the anatomical specializations
ers and Bertelli and Giannini’s (2005) study of in the inflatable esophagus that allow them to
penguins. Despite this deep history of anatomi- produce hooting calls during courtship display.
cal investigation, the internal anatomy of many Prince et al. (2011) showed that sexual dimor-
groups of birds, for example, in the Passeriformes, phism in morphology of the syrinx and upper
has yet to receive very much attention at all. As vocal tract underlies the larger vocal repertoires
one example, the notarium—a series of fused tho- and more frequent vocalizations of male versus
racic vertebrae independent of the synsacrum— female European Starlings. As a final example,
was thought to be absent in Passeriformes until a Krilow and Iwaniuk (2015) identified seasonal
relatively recent osteological survey revealed these changes in the volumes of two specific brain
structures to be widespread in the order, includ- regions, the striatopallidal complex and acropal-
ing in such familiar taxa as the European Starling lium, that occur in association with drumming
(Sturnus vulgaris) and the crossbills (Loxia spp.; Storer behavior in male Ruffed Grouse (Bonasa umbellus).
1982, James 2009). Establishing the systematic
distribution of a trait that has evolved repeatedly,
PALEONTOLOGY
like the notarium, can open the door to studies of
the trait’s function and evolutionary development. The portion of an avian phenotype that is most
Beginning in the 1970s for anatomical speci- likely to fossilize is the skeleton, which, as a con-
mens (e.g., Raikow 1977) and somewhat later for sequence, has not experienced the same slow rate
skeletons (e.g., Livezey 1986), internal anatomy of use in research as have anatomical specimens.
has been used to build character state matrices for Indeed, avian paleontology—including consider-
phylogenetic analysis, primarily using the par- able work with skeleton specimens—has a bur-
simony criterion. The ambitious morphological geoning literature that is bringing forth new
analysis of higher-level classification of birds by findings for every major geological period in the
Livezey and Zusi (2006, 2007) is a prime exam- history of birds. Some recent highlights include
ple. However, by now, molecular systematics has a greatly improved and still expanding Mesozoic
understandably supplanted morphology as the fossil record of birds (e.g., Carvalho et al. 2015,
main source of data for phylogenetics of mod- Hu et al. 2015), Paleogene fossils from several
ern birds (see Jarvis et al. 2014, Prum et al. 2015). continents that are particularly informative about
Yet anatomical characters remain relevant in sys- the biogeographic and temporal origins of mod-
tematics because they are a valuable data parti- ern bird orders (Mayr 2009), a diverse Neogene
tion often used in tandem with molecular data record that encompasses extinct avian giants as
(Fleischer et al. 2001, James et al. 2003), because well as fossils that are clearly relevant to modern
they enable interpretation of the fossil record (dis- genera and species (e.g., Olson and Rasmussen
cussed later), and because they reveal evolutionary 2001, Tambussi et al. 2012), and rich Quaternary
patterns in the phenotype. island records that are informative about the his-
tory of interactions between birds and people
(e.g., James 1995, Worthy and Holdaway 2002,
MORPHOLOGY AND BEHAVIOR
Steadman 2006, Meijer et al. 2013).
Research that extends beyond the boundaries of Phylogenetic placement of fossils relies on com-
traditional systematics to place morphology in an parative osteology, and consequently many osteo-
ecological or behavioral context can be particu- logical character state matrices have been developed
larly satisfying because it provides a more holis- primarily to analyze fossils (e.g., Mayr and Clarke
tic explanation of morphological diversity. For 2003, James 2004, Worthy 2009, Smith 2010).
example, Bostwick et al. (2012) used CT scanning There is also great interest in how best to make use
to document the unique construction of forelimb of the fossil record to reliably calibrate molecular
bones in the Club-winged Manakin (Machaeropterus phylogenetic trees to a timescale (e.g., Ksepka and
deliciosus), and then related the bony morphology Clarke 2015, Smith and Ksepka 2015). Figure 2.4
to the evolution of unusual feathers via sexual shows the type specimen of Limnofregata azygosternon,

Getting under the Skin 15

Figure 2.4. Holotype of Limnofregata azygosternon, USNM 22753, an Eocene relative of frigatebirds from Wyoming that
constrains the minimum age of the split between Fregatidae and Suloidea (including Sulidae, Phalacrocoracidae, and
Anhingidae; see Smith and Ksepka 2015).

a fossil relative of frigatebirds that is a minimum guilds. If the same study were performed today,
of 51.8 million years old, and illustrates the quality we could characterize skull geometry using 3D
of preservation in older fossils that is particularly landmark-based geometric morphometrics, as
helpful for calibrating the molecular phylogeny of Kulemeyer et al. (2009) did in their analysis of
modern birds. morphological integration of the neurocranium
Once the systematic position and time frame and bony beak of corvids. Kulemeyer et al.’s study
of a fossil have been worked out, its morphology generated several hypotheses about the adapta-
can be further studied to answer diverse ques- tion of beak shapes and binocular visual fields
tions about the history of avian phenotypes. CT in corvids, as they relate to pecking compared
and optical scanning are excellent tools to visu- to probing foraging modes, and raised a possible
alize and model fossils, and are good compan- relationship among skull shape, head posture, and
ions to more traditional techniques like caliper their propensity to take lengthy flights (as indi-
morphometrics and histology. To give just one of cated by wing tip shape; see Chapter 8, this vol-
many possible examples, the ability to create vir- ume). This is just one example of how the ability
tual endocasts of the braincase from CT scans has to take precise measurements, including geomet-
facilitated comparisons of fossil and modern neu- ric measurements based on landmarks and mea-
roanatomy (Ksepka et al. 2012, Smith and Clarke surements of surface areas and volumes, is leading
2012, Tambussi et al. 2015). to a deeper understanding of avian morphology
and stimulating new hypotheses to explain the
ecological, functional, and developmental context
MORPHOMETRICS
of morphologies.
Morphometrics, or the measurement and analy- Geometric morphometric analysis is an umbrella term
sis of linear dimensions, shapes, and volumes, that encompasses a variety of specific analytical
is employed in research on all topics surround- approaches based on landmarks, but it has some
ing the internal anatomy of birds. For instance, general limitations when it comes to birds. Because
caliper measurements of the skeleton have long birds lack teeth and have many fused bones with
been used to characterize the diversity of avian few open sutures in adulthood, they provide fewer
phenotypes in relation to ecology and evolution- good skeletal landmarks than is typical of other ver-
ary diversity. A classic example is Hertel’s (1994) tebrate groups. It may thus be necessary to resort
discriminant function analysis of cranial mor- to interpolated or “semi-landmarks” in birds, as
phometrics in vultures, in relationship to feeding Kulemeyer et al. (2009) did to characterize skull

16 Studies in Avian Biology  NO. 50 Webster

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