23 Articles from The Auk: Ornithological Advances and The Condor: Ornithological Applications. ALL ARTICLES ARE OPEN ACCESS

Highlighting the Use of Museum Collections in Avian Research

Nadje Najar,^1* Lauryn Benedict,¹ Andrew Doll,² and Garth Spellman²

¹School of Biological Sciences, University of Northern Colorado, Greeley, Colorado, USA
²Denver Museum of Nature and Science, Denver, Colorado, USA
*Corresponding author: [email protected]

Natural history collections began as taxonomic repositories for the preservation of specimens, some serving as types and others serving to document diversity around the type for comparative study. These collections have matured into invaluable repositories of biodiversity over time. Modern museum preparation now involves the preservation of many sources of biological information including ecto-parasites and endo-parasites, stomach and gut contents, partial or full skeletons, blood smears, blood stored in RNA stable solutions, fecal samples, and frozen tissue samples. The continuous collection of avian specimens and associated documentation of live birds and their behaviors have enabled ornithologists to start asking and answering questions that involve wide-ranging temporal, geographic, and systematic coverage.

For this Special Collection on Museum Collections, we provide a brief overview of studies published in 2015, 2016, and 2017 issues of The Condor: Ornithological Applications and The Auk: Ornithological Advances that made use of museum collections to advance the field of ornithology. The selected papers cover a range of subjects, including new species descriptions, systematics and taxonomy, phylogeography, population genetics, migratory connectivity, plumology, and ancestral state reconstruction. We have given special emphasis to publications that use archived materials in interesting and novel ways, thus highlighting the wide variety of data that collections can provide.

Perhaps the most common use of natural history museums is as the primary source for revisions and updates of taxonomy, which often requires the use of some combination of genetic material, locality information, morphology, field notes, archived recordings, and other museum data.

Fernando et al. (2016) assessed hybridization in two forms of the Red-backed Woodpecker (Dinopium benghalense) by sequencing DNA from woodpeckers collected along a transect spanning their putative hybrid zone (Figure 1). A small hybrid zone with limited haplotype introgression warrants elevation of each to species status. 

Figure 1. Series of Red-backed woodpeckers from Sri Lanka illustrating variation in plumage color. See Fernando et al. (2016) for details.

Another study of a woodpecker, the Helmeted Woodpecker (Celeus galeatus), revealed that although it is morphologically very similar to the larger Lineated Woodpecker (Drycopus lineatus), genetic analysis places this species firmly in the genus Celeus (Benz et al. 2015). The authors suggest that this morphological convergence represents a form of interspecific mimicry, a hypothesis tentatively supported by submissive behaviors observed in the smaller Helmeted Woodpecker. Avendaño et al. (2015) documented a new species of tapaculo, the Perijá Tapaculo (Scytalopus perijanus), a species that had been collected as early as 1941 but had not been recognized as a separate taxon. Comparison with specimens in the genus Scytalopus and observations of the behaviors of live birds yielded diagnosable traits to support the designation of this taxon as a species. Feo et al. (2015) used study skins and audio–video recordings to demonstrate the morphological, acoustic, and genetic distinctiveness of a subspecies of the Bahama Woodstar (Calliphlox evelynae lyrura), a bird that occurs on just two islands, potentially warranting species-level status.

Museum collections are particularly valuable for studies of population genetics and phylogeography because they facilitate access to specimens spanning a broad range of space and time. DNA from Virginia's Warbler (Oreothlypis virginiae) skins collected throughout the species' range exhibited little overall population structure, provided support for a post-glacial range expansion, and offered evidence that a newly established population in the Black Hills of South Dakota is connected via gene flow with populations in the heart of the species distribution (Bubac and Spellman 2016). A similar pattern of relatively high diversity but low population structure was found in California Condors (Gymnogyps californianus), in which haplotype diversity dropped dramatically after the 19th century, supporting the hypothesis that humans contributed to the decline of this species (D'Elia et al. 2016). This study estimated the genetic structure of condors through time using specimens collected over a period of 159 years, a feat that only archived specimens make possible. Pruett et al. (2017) examined the effect of island isolation on genetic variation in a widespread species, the Pacific Wren (Troglodytes pacificus), in which they found the lowest amounts of genetic diversity and highest divergence in island populations farthest from possible mainland sources. Each of these population genetic studies provides conclusions that will facilitate management decisions and highlight the value of museum collections to conservation science.

Specimen collections have recently been used to investigate the phylogeography of many groups, including ground-doves (Sweet and Johnson 2015), grebes (Ogawa et al. 2015), and swamphens (Garcia and Trewick 2015). Barker et al. (2015) built a massive phylogeny of nearly all members of the Emberizoidea, and found support for a north temperate origin of many groups, in line with Ernst Mayr's early predictions. This study is exemplary in its scope and would not have been possible without access to nearly 800 species from museum collections.

In addition to providing genetic samples, museum specimens hold a wealth of data about the evolution of avian morphology, distribution, breeding phenology, and trait diversification. Recent publications have investigated the evolution of superorbital ossification in Charadriiforms (Hughes 2015), body size and shape in members within the genus Cinclodes (Rader et al. 2015), and the evolution of song complexity among warblers in the genus Geothlypis (Byers 2015) by using archived skins and/or recordings. Oswald and Steadman (2015) made use of archived skeletons to identify Late Pleistocene fossils in Peru to compare historical species distributions and assemblages with modern ones. Egg collections helped Duursma et al. (2017) determine the phenology of egg laying in more than 300 Australian species. Their study demonstrated that a single observation, such as that represented by a collected egg, is nearly as accurate as intensive nest visits at assessing the initiation of egg laying. Danner et al. (2017) used CT scans of dry and fluid-preserved Song Sparrows (Melospiza melodia) to determine whether the size and shape of the nasal concha, a structure important for moisture capture and conditioning of inhaled air, was associated with habitat type. A subspecies inhabiting coastal dunes (M. m. atlantica) had larger conchae than a neighboring subspecies (M. m. melodia), potentially facilitating moisture recapture in the drier dune environment (Figure 2).

Figure 2. Cross sections of the middle and rostral nasal conchae of preserved Song Sparrows from each subspecies, (A) M. m. atlantica and (B) M. m. melodia, obtained from CT scans. See Danner et al. (2017) for details.

Feathers can contribute a wealth of information about bird biology. Study skins preserve the structure, arrangement, replacement pattern, appearance, and chemical composition of feathers at the time of death. Luttrell et al. (2015) investigated the effects of salinity on melanism in Song Sparrows using digital photography of specimens representing three saline-dwelling subspecies and one freshwater-dwelling subspecies. Song Sparrows living in more saline environments were darker than their freshwater conspecifics, adding another example to the pattern of salt marsh melanism seen in other groups. In an impressive use of archived specimens, Roulin and Randin (2015) investigated environmental effects on melanism in Barn Owls (Tyto alba) by characterizing the plumage of 1,369 study skins collected across nearly all of North America. Overall patterns of melanism were consistent with Gloger's rule, with variation in melanin deposition correlating with ambient temperature and precipitation.

Several publications use spectroscopy to study feather reflectance and composition. Barreira et al. (2016) used study skins to investigate how viewing geometry affects feather color perception in Swallow Tanagers (Tersina viridis). Although not iridiscent, Swallow Tanager feathers appear to change color with viewing angle; but the feathers are much more conspicuous to an avian visual system than a non-avian one and result in high male conspicuousness and female crypsis. Thomas and James (2016) used a single specimen to study the composition of the uniquely colored (and possibly extinct) Pink-headed Duck (Rhodonessa caryophyllacea). Raman spectroscopy supported their hypothesis that the bright pink head is the result of carotenoid deposition, a rare pigment in waterfowl.

Similar to the revelations of taxonomic and population structure provided by DNA, tissues obtained from museum specimens contain additional intrinsic markers that can indicate certain behavioral traits. For example, the composition of stable isotope ratios in animal tissue can provide information on movement patterns and dietary habits. For most migratory species, tracking their migrations is still time-consuming and expensive. Using a few feathers from living and preserved Golden Eagles (Aquila chrysaetos), Nelson et al. (2015) were able to estimate the locations of the breeding grounds and infer moderate amounts of connectivity between populations. Exploiting a presumed switch from marine to terrestrial diet items upon completion of spring migration, Doll et al. (2015) used muscle and blood tissues of collected and live-captured Dunlin (Calidris alpina arcticola) to estimate arrival dates at their Arctic breeding grounds. The authors demonstrated that blood isotope analyses of wild birds provided more accurate arrival estimates than lab-generated parameters did (as validated by geolocator data).

Conclusion

Specimens archived in museums have been used in a variety of ways to answer diverse questions about the biology of birds. Many of the publications highlighted here were conducted, in their entirety, using collected specimens and metadata associated with those specimens, while others used museum resources to help make sense of newly collected field data. The humble study skin and associated specimens may yet yield more information as new techniques are developed, making this material even more valuable. Museums serve as time capsules, transporting the researcher to a time and place otherwise unreachable in order to ask a multitude of questions. Scientists embarking on collecting expeditions centuries ago did not anticipate the discovery of DNA or the advent of isotope analysis, but their efforts are proving invaluable today. This special function of museums can only be maintained through the continued conscientious collection, curation, and storage of bird specimens.

Museum Collections Articles – All Open Access

Selections on Museum Collections

Phenotypic and genetic analysis support distinct species status of the Red-backed Woodpecker (Lesser Sri Lanka Flameback: Dinopium psarodes) of Sri Lanka by S. P. Fernando, D. E. Irwin, and S. S. Seneviratne. The Auk 133(3):497–511. Published June 22, 2016.

Phylogenetic relationships of the Helmeted Woodpecker (Dryocopus galeatus): A case of interspecific mimicry? by B. W. Benz, M. B. Robbins, and K. J. Zimmer. The Auk 132(4):938–950. Published September 30, 2015.

A new species of tapaculo (Rhinocryptidae: Scytalopus) from the Serranía de Perijá of Colombia and Venezuela by J. E. Avendaño, A. M. Cuervo, J. P. López-O., N. Gutiérrez-Pinto, A. Cortés-Diago, and C. D. Cadena. The Auk 132(2):450–466. Published March 11, 2015.

Divergence in morphology, calls, song, mechanical sounds, and genetics supports species status for the Inaguan hummingbird (Trochilidae: Calliphlox “evelynae” lyrura) by T. J. Feo, J. M. Musser, J. Berv, and C. J. Clark. The Auk 132(1):248–264. Published December 17, 2014.

How connectivity shapes genetic structure during range expansion: Insights from the Virginia's Warbler by C. M. Bubac and G. M. Spellman. The Auk 133(2):213–230. Published February 24, 2016.

Ancient DNA reveals substantial genetic diversity in the California Condor (Gymnogyps californianus) prior to a population bottleneck by J. D'Elia, S. M. Haig, T. D. Mullins, and M. P. Miller. The Condor 118(4):703–714. Published September 21, 2016.

Island life and isolation: The population genetics of Pacific Wrens on the North Pacific Rim by C. L. Pruett, A. Ricono, C. Spem, and K. Winker. The Condor 119(1):131–142. Published February 8, 2017.

Patterns of diversification in small New World ground doves are consistent with major geologic events by A. D. Sweet and K. P. Johnson. The Auk 132(1):300–312. Published December 31, 2014.

Opposing demographic histories reveal rapid evolution in grebes (Aves: Podicipedidae) by L. M. Ogawa, P. C. Pulgarin, D. A. Vance, J. Fjeldså, and M. van Tuinen. The Auk 132(4):771–786. Published July 22, 2015.

Dispersal and speciation in purple swamphens (Rallidae: Porphyrio) by J. C. Garcia-R. and S. A. Trewick. The Auk 132(1):140–155. Published November 19, 2014.

New insights into New World biogeography: An integrated view from the phylogeny of blackbirds, cardinals, sparrows, tanagers, warblers, and allies by F. K. Barker, K. J. Burns, S. M. Lanyon, and I. J. Lovette. The Auk 132(2):333–348. Published January 7, 2015.

Evolution of supraorbital ossification in Charadriiformes by A. L. Hughes. The Auk 132(3):685–696. Published June 10, 2015.

Morphological divergence in a continental adaptive radiation: South American ovenbirds of the genus Cinclodes by J. A. Rader, M. E. Dillon, R. T. Chesser, P. Sabat, and C. Martínez del Rio. The Auk 132(1):180–190. Published December 3, 2014.

Migration and song elaboration in wood-warblers (Geothlypis) by B. E. Byers. The Auk 132(1):167–179. Published December 3, 2014.

The changing diversity and distribution of dry forest passerine birds in northwestern Peru since the last ice age by J. A. Oswald and D. W. Steadman. The Auk 132(4):836–862. Published September 9, 2015.

Characterizing opportunistic breeding at a continental scale using all available sources of phenological data: An assessment of 337 species across the Australian continent by D. E. Duursma, R. V. Gallagher, and S. C. Griffith. The Auk 134(3):509–519. Published April 19, 2017.

Habitat-specific divergence of air conditioning structures in bird bills by R. M. Danner, E. R. Gulson-Castillo, H. F. James, S. A. Dzielski, D. C. Frank III, E. T. Sibbald, and D. W. Winkler. The Auk 134(1):65–75. Published November 9, 2016.

Digital photography quantifies plumage variation and salt marsh melanism among Song Sparrow (Melospiza melodia) subspecies of the San Francisco Bay by S. A. M. Luttrell, S. T. Gonzalez, B. Lohr, and R. Greenberg. The Auk 132(1):277–287. Published December 17, 2014.

Gloger's rule in North American Barn Owls by A. Roulin and C. Randin. The Auk 132(2):321–332. Published January 7, 2015.

Viewing geometry affects sexual dichromatism and conspicuousness of noniridescent plumage of Swallow Tanagers (Tersina viridis) by A. S. Barreira, N. C. García, S. C. Lougheed, and P. L. Tubaro. The Auk 133(3):530–543. Published July 6, 2016.

Nondestructive Raman spectroscopy confirms carotenoid-pigmented plumage in the Pink-headed Duck by D. B. Thomas and H. F. James. The Auk 133(2):147–154. Published January 27, 2016.

Stable hydrogen isotopes identify leapfrog migration, degree of connectivity, and summer distribution of Golden Eagles in eastern North America by D. M. Nelson, M. Braham, T. A. Miller, A. E. Duerr, J. Cooper, M. Lanzone, J. Lemaître, and T. Katzner. The Condor 117(3):414–429 Published August 12, 2015.

Improved arrival-date estimates of Arctic-breeding Dunlin (Calidris alpina arcticola) by A. C. Doll, R. B. Lanctot, C. A. Stricker, S. M. Yezerinac, and M. B. Wunder. The Auk 132(2):408–421. Published February 25, 2015.