The Secret Perfume of Birds: Uncovering the Science of Avian Scent. Danielle J. Whittaker. 2022. John Hopkins University Press, Baltimore, MD, USA. 296 pages. ISBN-10: 1421443473 (Hardcover) $23.97.
The COVID19 pandemic presented an enormous scientific challenge almost unparalleled in its urgency. Among the myriad of questions laid at the feet of virologists and epidemiologists by the emergence of SARS-CoV2 was the question of transmission. We all recall the first months of the pandemic in early 2020 and the guidelines calling for frequent handwashing and distancing of two meters. This guidance grew from a convention regarding respiratory diseases that distinguished between airborne transmission and infection via droplets. Airborne transmission with viruses carried by aerosols disseminating across comparatively long distances was thought of as the exception – reserved for a few highly contagious respiratory infections such as measles and tuberculosis. Most respiratory illnesses were thought to spread by either direct contact with droplets expelled from an infected individual at close range through coughing or sneezing or by indirect contact with surfaces contaminated by droplets, known as fomites. SARS-CoV2 was expected to behave according to convention and spread as typical coronaviruses, like those involved in common colds, by droplets across relatively short distances and through contact with fomites and this expectation influenced the guidelines.
A critical question is imbedded in this narrative. What is the distinction between an airborne aerosol and a less volatile droplet? The convention among infectious disease scientists was that 5 microns demarcated heavy droplets from lighter, airborne aerosols. According to this convention, airborne diseases, like measles and tuberculosis, could spread widely through aerosols drifting through the environment and diseases like COVID19 and other coronaviruses spread across short distances and surfaces via droplets.
Along come aerosol scientists, including Lindsey Marr of Virginia Tech, Jose-Luiz Jimenez of the University of Colorado Boulder, Yuguo Li of the University of Hong Kong, and others with data demonstrating that, depending on the environmental conditions, particles larger than five microns may behave like aerosols. However, data from aerosol scientists often fell on deaf ears at the World Health Organization and US Centers for Disease Control where public health officials clung to the five-micron convention.
The urgent need to understand transmission of COVID19 led Marr, Jimenez, Li, and others to seek to uncover the evidentiary basis for the five-micron rule in infectious disease. They came up short. The supporting evidence for the five-micron rule seemed absent from the literature. However, with help from a historian of science, Tom Ewing, and graduate student whose prior thesis research was interrupted by the pandemic, Katie Randall, it was discovered that this convention was borne out of research specific to tuberculosis from the 1950’s and 60’s that was uncritically adopted as a general rule for all respiratory diseases. This once unchallenged convention has been reversed and empirical studies have demonstrated that many respiratory illnesses may spread in aerosols – changing how we think about infectious respiratory diseases in general (Molteni, 2021, Tang et al., 2021).
I have two reasons to begin a review of a book in ornithology with a discussion of transmission of respiratory diseases. First and foremost, both Danielle Whittaker’s book The Secret Perfume of Birds (Whittaker, 2022) and the question posed by aerosol scientists regarding the airborne transmission of COVID19 are stories of convention versus consensus in science. Just as the five-micron rule in infectious disease science was one adopted based on educated hunches, appeals to authority, overgeneralization, and intuition, but little data, the idea that olfaction was not a readily available sensory channel in birds was for much of the history of ornithology a convention. Conventions are difficult to avoid entirely in science. They often form the basis for many of our underlying assumptions about how nature works and shape our methodologies. The 0.05 cut-off for statistical significance for example may be among the most ubiquitous of our methodological conventions. Conventions may in some cases be necessary as temporary, short-hand assumptions that allow us to move on and tackle other questions. However, eventually our assumptions and conventions need to be examined critically and often those conventions fail to live up to empirical scrutiny.
Second, in many popular science books written during the past two years there is very often a mention of the COVID19 pandemic. Mention of how scientific careers have been stalled and the stress of uncertainty on the personal and professional lives of individual scientists shares narrative space alongside the scientific story. The pandemic is an even more salient theme in Whittaker’s book as both deal with invisible airborne agents wafting between individuals and affecting their biology and behavior.
For many ornithologists, save perhaps for those new to the field, the idea that birds possess a comparatively weak sense of smell (microsmatic) or are virtually without a sense of smell (anosmic) was the convention. Whittaker examines the origins of this convention from anatomical observations of the relatively small olfactory bulbs in birds to behavioral experiments dating back to John James Audubon. Like many conventions the idea of anosmic birds was not one based on much empirical evidence and would eventually not survive the test of time as researchers like Bernice Wenzel, Kenneth Stager, Larry Hutchison, Betsy Bang, Julie Hagelin, and eventually Whittaker herself designed experiments to rigorously deal with the question of avian olfaction (Bang, 1960, Hagelin et al., 2003, Hagelin, 2007, Jones et al., 2004, Wenzel, 1968, Stager, 1964, Hutchison and Wenzel, 1980).
Some avian species seemed to be ideal candidates to challenge the general convention that birds were anosmic. Tube-nosed seabirds, vultures, alcids, and the Brown Kiwi (Apteryx australis) were the subjects of some of the first modern studies to overturn the notion that birds have little capacity for olfaction. The ecology of these species strongly suggested olfaction would be important. Hutchison and Wenzel demonstrated that shearwaters, fulmars, albatross, and other pelagic seabirds were attracted by food related odors over those not directly associated with food (i.e. motor or mineral oils, Hutchison and Wenzel, 1980). Stager found that Turkey Vultures (Cathartes aura) were readily attracted to an open container of ethyl mercaptan, a volatile compound associated with carrion (Stager, 1964). Wenzel found that Brown Kiwi could distinguish concealed caches of food by scent (Wenzel, 1968). Hagelin’s pioneering studies of the tangerine-scented, colony-nesting Crested Auklet (Aethia cristatella) showed they could detect and preferred conspecific odors (Hagelin et al., 2003, Hagelin, 2007, Jones et al., 2004). These and other studies from the 1960’s through the 2000’s seemed to put to rest the idea of birds in general as an olfactory deprived taxon. The data over these decades reversed the convention and established an evidence-based consensus that chemical odors were in fact a sensory channel available to birds.
Many of the studies overturning the anosmia convention for birds were performed on non-passerines, most with either foraging or colony-nesting ecologies suggestive of a reliance on olfaction. Fewer studies focused on passerine birds. Determining whether or not over half of the avian class relied on scent was a critical task in determining the ubiquity of olfaction in the sensory world of birds. Whittaker draws heavily on the work she began in Ellen Ketterson’s laboratory on the role of olfaction in the breeding biology of the Dark-eyed Junco (Junco hyemalis). The olfactory world of the once assumed anosmic, or at best microsmatic, passerine birds Whittaker reveals to be far more complex than convention suggested.
Compared to the gland-rich skin of mammals, birds have little in the way of secreting integumentary structures. They really are left with only one – the uropygial gland. Whittaker and her colleagues have found that the uropygial gland is the source of a number of volatile compounds, mostly fatty acids, that may be used as either chemical cues or signals in Dark-eyed Juncos (Whittaker et al., 2010) and Whittaker takes the time to draw a clear distinction between a cue and a signal. Juncos also vary the abundance of these compounds in relation to the breeding season producing more potential odorants during the breeding season (Whittaker et al., 2011b) and while there is no evidence of sex-specific odorants, junco sexes vary in the proportions of these compounds with each sex producing a particular sex-specific blend during the breeding season (Whittaker et al., 2010). What’s more, Whittaker found that juncos may detect certain odors and alter their behavior accordingly. Preen oil from another species or unfamiliar conspecific applied to a junco nest resulted in a shorter incubation bout compared to preen oil from the incubating female herself or an acetone control (Whittaker et al., 2009). Juncos can also distinguish between the scents associated with males versus females and appear to prefer associating with smells aligned with their sex, perhaps a behavior related to intrasexual territoriality (Whittaker et al., 2011a).
A significant portion of the book covers what I refer to as olfactory adjacent topics – broad topics clearly intersecting with olfaction, or those topics related to the biological production of odorants themselves. Major histocompatibility complex (MHC) alleles as they relate to mate choice and heterozygosity has been a major focus of research. MHC alleles have been shown in many taxa, including mice, humans, and fishes, to be associated with disassortative mate preferences (Milinski and Wedekind, 2001, Wedekind et al., 1995, Wedekind and Furi, 1997, Milinski, 2003, Milinski, 2006). The evidence for genetic dissimilarity and mate choice in birds however is mixed (Mays et al., 2008). Whittaker found a correlation between the similarity among social pairs and the frequency of extra-pair offspring in juncos but this only held true for some populations as opposed to others (Whittaker, 2022, pg. 197). For mammals and fish olfaction has been posed as the mechanism of mate discrimination on the basis of MHC. Human MHC genes and the largest cluster of olfactory receptors are found on chromosome six and this linkage may be the basis for certain olfactory preferences (Younger et al., 2001). Whittaker and others propose that the microbiome may serve as a proxy for MHC based discrimination in birds given that some early evidence suggests that high MHC diversity is correlated with less diverse microbial communities and microbial communities are implicated in the diversity of odorants (Leclaire et al., 2019). However, the evidence for these claims for now is comparatively scant, and selection for MHC diverse genotypes in offspring may be favored through mechanisms other than olfaction.
The topic of avian microbiomes looms large in Whittaker’s book. So prominent is this topic that it arguably could have been expanded to be the subject of its own book. The reason for the emphasis on microbiomes is the link between bacteria and odorants. Many odors in humans for example are associated with the breakdown of otherwise odorless compounds by microbes (Gower et al., 1994). Whittaker’s work on the microbial communities of the avian uropygial gland is a key part of the story on avian scents. Whittaker and her colleagues found that the uropygial gland of juncos is host to a diversity of bacteria and treating the gland with antibiotics not only changed the diversity of the microbiome but reduced the prevalence of certain volatile compounds (Whittaker et al., 2019). Whittaker however describes these results as revealing but “statistically speaking” not “super impressive” (Whittaker, 2022, pg. 135). This is a repeated occurrence throughout the book. Interesting results are presented but are linked to certain caveats, including small sample sizes and preliminary analyses. One almost gets the feel that the book is a bit premature and in another five or ten years a less speculative book on avian olfaction could be authored, at least in reference to passerines.
Throughout the book Whittaker discusses various hypotheses related to the adaptive significance of olfaction in intraspecific communication either as a mechanism involved in mate choice, parental care, or intrasexual aggression. However, very little of the book touches on the heritability of odors in birds. If odors have evolved through natural selection as signals in interactions of parental care, dominance, or mate choice then they must have at least in part a heritable component. Whittaker devotes a great deal to the environmental components of variation in avian odors, specifically the influence of the microbiome, but comparatively little to genetic sources of variation in avian odors. She does mention evidence of this in other species. For example, Whittaker briefly mentions the influence of mutations at the ATP-binding cassette transporter sub-family C member 11 (ABCC11) gene that interrupts the production of compounds that provide a substrate for bacteria to make human body odor (Martin et al., 2010). Whittaker reports her finding in juncos that nestmates are more similar microbiomes to each other than to non-nestmates, and this is equally true for full and half-sibs, and that mothers have more similar microbiomes to the nestlings they incubate than do non-incubating fathers (Whittaker et al., 2016). She concludes that, “…an organism’s bacterial community is shaped by its social behavior, rather than one’s own genome” which would lead one to wonder how readily olfaction-based recognition may evolve if olfaction relies on microbiomes and genes have little influence on variation in microbiomes (Whittaker, 2022, pgs. 155-156). Future researchers may want to examine the heritability of those odors in passerine birds suspected to play a role in social behavior.
A value of a popular science book is that in addition to covering the conceptual and evidentiary basis for a scientific subject they provide the reader with a feel for doing science in that field. This aspect is especially valuable for students but also important for more senior researchers especially if the author’s background differs from their own. I for one was pleased to hear that Whittaker’s time in graduate school was as long as my own! Whittaker does an excellent job conveying to the reader the arc of her career and its challenges including everything from switching to a completely different model organism to finding permanent employment to dodging Black Bears (Ursus americanus) at Mountain Lake Biological Station in Virginia. Whittaker’s frank descriptions of her career path and work-life balance are a welcome affirmation and will undoubtedly serve as encouragement for students and junior faculty – especially for women in the field. Most of the chapters begin with these personal anecdotes culminating in Whittaker’s 2019 visit to the Natural History Museum in Los Angeles where she encounters exhibits that now describe an olfactory-rich aves as the consensus position – bringing the study of avian olfaction from ill-conceived convention to data-based consensus.
Clearly the consensus position is now that most birds do in fact use olfaction as a sensory channel. My own work over a decade ago underappreciated this fact (Mays et al., 2008). Whittaker’s book lays to rest the old convention of an anosmic aves. However, while their ability to access odors and use those odors in their behavioral decisions was wildly underestimated, many birds, with notable exceptions, may not have olfactory abilities on par with say mammals or fishes. I’m not sure that your county sheriff’s bloodhound or the airport beagle will be replaced by trained fowl anytime soon. However, Whittaker (2022) has convincingly countered the notion that birds are anosmic, or even microsmatic, and that birds do not incorporate chemical signals in their behavioral decisions.
I would highly recommend Whittaker’s book to anyone interested in not just avian olfaction and sensory ecology but microbiomes and behavioral ecology in general. This book is entertainingly written, rigorous in its scholarship, and well well-conceived. Despite my feeling that the book comes at a time when this topic in ornithology is still being explored, it still has enormous value in prompting other researchers to think about avian olfaction and take the field in novel directions.
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Herman L Mays Jr.
Marshall University Department of Biological Sciences
Header photo: Dark-eyed Junco (Junco hyemalis), USFWS/Zak Pohlen
Mays Jr., H. 2022. Review of the book The Secret Perfume of Birds: Uncovering the Science of Avian Scent, by Danielle J. Whittaker. Association of Field Ornithologists Book Review, https://afonet.org/2022/06/the-secret-perfume-of-birds-uncovering-the-science-of-avian-scent/.