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Measurement of Chemical Emissions in Crested Auklets (Aethia cristatella)

DOI:10.1007/s10886-006-9164-2
Authors:
Hector D. Douglas III at Grambling State University
Hector D. Douglas III
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Abstract and Figures

This report presents the first quantitative estimates of emission rates for chemical signals in a bird—the crested auklet (Aethia cristatella). Volatile emissions from live birds were captured in a purified airstream onto polymer traps. Traps were eluted with methanol and analyzed with gas chromatography-mass spectrometry. The volatile collection chamber was field-calibrated with an in-line bubbler and synthetic octanal, the dominant constituent of the crested auklet’s citruslike odor. The result is an index of volatile chemical emissions within a small population of wild crested auklets at Big Koniuji Island, AK, USA. The average emission rate for octanal was 5.7 μl/50 min. Males and females did not differ in their emission rates (t (0.05)two-tailed = 0.44, P = 0.66). There was a sevenfold difference between minimum and maximum emission rates. Prevalence of tick infection (2%) was low despite the high abundance of ticks in the colony. The crested auklet with the lowest chemical emission rate was heavily parasitized by ticks.
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AUTHOR'S PROOF
Metadata of the article that will be visualized in OnlineFirst
1
Article Title
Measurement of Chemical Emissions in Crested Auklets (
Aethia
cristatella
)
2
Journal Name
Journal of Chemical Ecology
3
Corresponding
Author
Family Name
Douglas
4
Particle
5
Given Name
Hector D.
6
Suffix
III
7
Organization
University of Alaska Fairbanks
8
Division
Institute of Marine Science
9
Address
Fairbanks 9970, Alaska, USA
10
e-mail
hddouglas@gmail.com
11
Schedule
Received
27 March 2006
12
Revised
2 June 2006
13
Accepted
21 June 2006
14
Abstract
This report presents the first quantitative estimates of emission rates for
chemical signals in a bird—the crested auklet (Aethia cristatella). Volatile
emissions from live birds were captured in a purified airstream onto polymer
traps. Traps were eluted with methanol and analyzed with gas chromatography-
mass spectrometry. The volatile collection chamber was field-calibrated with an
in-line bubbler and synthetic octanal, the dominant constituent of the crested
auklet’s citruslike odor. The result is an index of volatile chemical emissions
within a small population of wild crested auklets at Big Koniuji Island, AK, USA.
The average emission rate for octanal was 5.7 µl/50 min. Males and females
did not differ in their emission rates (t
(0.05)two-tailed
= 0.44, P = 0.66). There was
a sevenfold difference between minimum and maximum emission rates.
Prevalence of tick infection (2.1%) was low despite the high abundance of ticks
in the colony. The crested auklet with the lowest chemical emission rate had 14
ticks attached to the face, whereas nearly all other crested auklets had no ticks.
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Keywords
separated by ' - '
Crested auklet - Chemical emissions - Chemical signal - Octanal -
Ectoparasites - Repellents - Chemical defense
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Foot note
information
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Testsite
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file://D:\Programs\Metadata\temp\jec69164.htm
... Aside from studies of the uropygial gland, intraspecifi c patt erns of avian compounds are rarely noted in the literature. Important exceptions include adult Crested Auklets, pitohuis, and Antarctic Prions (Pachyptila desolata), which exhibit individual variation in the chemical substances they produce-in the rate of odor emissions (Douglas 2006a), concentration of feather toxins (Dumbacher et al. 2000), and volatile compounds extracted from plumage (Bonadonna et al. 2007), respectively. No striking chemical diff erences are evident between the sexes (Dumbacher et al. 2000, Hagelin et al. 2003, Bonadonna et al. 2007. ...
... L. Jones pers. obs.; see also Douglas 2006a). The tick transmits disease, including the spirochete Borrelia and viruses (Muzaff ar and Jones 2004). ...
... If the compounds in Crested Auklet scent defend against ectoparasites, the result is not as toxic, nor is the aversion as marked as in Pitohui (Dumbacher 1999). Sublethal or physiological eff ects on auklet ectoparasites (e.g., impaired development) have been implied (Douglas et al. 2005b, Douglas 2006a), but currently require supporting data. Natural vertebrate predators (foxes, gulls) have not been tested, though Crested Auklets are traditionally hunted and eaten by local residents (Sealy 2006). ...
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... Predictably, chemical sampling methods that directly capture compounds released into the environment immediately surrounding the animal (its 'headspace') reveal fewer analytes compared to liquid extraction techniques. By selectively trapping volatile chemicals, systems such as solid phase microextraction (SPME), thermal desorption (TD), or other polymer trapping techniques (e.g., SuperQ or Tenax) deliver a more discerning representation of the natural volatilome profile [51][52][53]. For example, Gabiriot et al. compared traditional solvent extraction with SPME and TD methods to explore the musky odour of the blue petrel (Halobaena caerulea) [51]. ...
... Similarly, solvent-free gas-phase sampling techniques were used to capture the short-chain saturated and mono-unsaturated aldehydes that give rise to the distinctive citrus-like aroma of crested auklets (Aethia cristatella) and whiskered auklets (A. pygmaea) [52][53][54]. ...
Volatile Cues Influence Host-Choice in Arthropod Pests
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  • Oct 2020
Many arthropod pests of humans and other animals select their preferred hosts by recognising volatile odour compounds contained in the hosts’ ‘volatilome’. Although there is prolific literature on chemical emissions from humans, published data on volatiles and vector attraction in other species are more sporadic. Despite several decades since the identification of a small number of critical volatiles underpinning specific host–vector relationships, synthetic chemicals or mixtures still largely fail to reproduce the attractiveness of natural hosts to their disease vectors. This review documents allelochemicals from non-human terrestrial animals and considers where challenges in collection and analysis have left shortfalls in animal volatilome research. A total of 1287 volatile organic compounds were identified from 141 species. Despite comparable diversity of entities in each compound class, no specific chemical is ubiquitous in all species reviewed, and over half are reported as unique to a single species. This review provides a rationale for future enquiries by highlighting research gaps, such as disregard for the contribution of breath volatiles to the whole animal volatilome and evaluating the role of allomones as vector deterrents. New opportunities to improve vector surveillance and disrupt disease transmission may be unveiled by understanding the host-associated stimuli that drive vector-host interactions.
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... Finally, we note that many studies to date have focused on uropygial secretions only (e.g., Grieves et al. 2018;Mardon et al. 2010;Whittaker et al. 2010), while behavioral assays typically use whole-body odor as a stimulus (e.g., Amo et al. 2012b;Bonadonna and Nevitt 2004;Caspers et al. 2015). Currently surprisingly little is known about how secretions might differ from body odor (e.g., oxidation or bacterial processes), and thus precisely what chemical information the receiver perceives (but see Douglas III 2006). ...
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Article
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Much of the growing interest in avian chemical signals has focused on the role of kin recognition or mate attraction, often with an emphasis on males, with uropygial gland secretions perhaps providing information about an individual’s identity and quality. Yet, data collected to date suggest sexual dimorphism in uropygial glands and secretions are often emphasized in female, rather than in male birds. That is, when a sexual difference occurs (often during the breeding season only), it is the female that typically exhibits one of three patterns: (1) a larger uropygial gland, (2) a greater abundance of volatile or semi-volatile preen oil compounds and/or (3) greater diversity of preen oil compounds or associated microbes. These patterns fit a majority of birds studied to date (23 of 30 chemically dimorphic species exhibit a female emphasis). Multiple species that do not fit are confounded by a lack of data for seasonal effects or proper quantitative measures of chemical compounds. We propose several social functions for these secretions in female-based patterns, similar to those reported in mammals, but which are largely unstudied in birds. These include: (1) intersexual advertisement of female receptivity or quality, including priming effects on male physiology, (2) intrasexual competition, including scent marking and reproductive suppression or (3) parental behaviors, such as parent-offspring recognition and chemical protection of eggs and nestlings. Revisiting the gaps of chemical studies to quantify the existence of female social chemosignals and any fitness benefit(s) during breeding are potentially fruitful but overlooked areas of future research.
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... Except for very few studies (Douglas, 2006), the present work presents a rare odour analysis in birds performed using the entire bird and the first exhaustive and reliable VOC database from hens (Supplementary material S1). Most of the previous studies on bird odours, and particularly those conducted in hens (Williams et al., 2003;Bernier et al., 2008), relied on dipping some feathers in solvent or analysing uropygial gland secretions (see Campagna et al., 2012). ...
Modulation of feed composition is able to make hens less attractive to the poultry red mite Dermanyssus gallinae
Article
  • Sep 2019
The poultry red mite (PRM) is an obligatory hematophagous pest that causes substantial economic losses in poultry worldwide. PRM does not live on the host but in the bird’s environment and must find its host remotely. Hence, manipulating chicken odors is of interest. Several crude plant-originating volatile organic compounds (VOCs) have already been shown as repellent to D. gallinae. We aimed to test whether these VOCs can interfere with PRM host-seeking behavior by their oral administration to the poultry. The objectives were to determine (1) if hen odors are modified by supplemented feed ingestion and (2) if such treatment makes hens less attractive to PRM. Chemical characterization by GC-MS of the hen odor was conducted before and after the hens ingested the supplemented feed. The chromatograms obtained show that hen odor was substantially modified after the hens consumed it. Among the molecules recurrently detected from the supplemented hens, 26% were nearly absent in the unsupplemented hens. Behavioral choice tests to compare the effect of the modified and unmodified host odors on PRM show that some of the plant-originating emitted VOCs and the modified whole-hen odors were repellent to PRM.
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... Except for very few studies (Douglas, 2006), the present work presents a rare odour analysis in birds performed using the entire bird and the first exhaustive and reliable VOC database from hens (Supplementary material S1). Most of the previous studies on bird odours, and particularly those conducted in hens (Williams et al., 2003;Bernier et al., 2008), relied on dipping some feathers in solvent or analysing uropygial gland secretions (see Campagna et al., 2012). ...
Attractiveness of volatile organic compounds on Dermanyssus gallinae (Mesostigmata: Dermanyssidae)
Presentation
  • Jul 2018
The Poultry Red Mite (PRM), Dermanyssus gallinae, is an obligate blood-sucking ectoparasite of economic importance in layer farms. Increasing acaricide resistance and strengthening of environmental policies make PRM control challenging and require alternative control tools. Whilst the general life cycle and habits of PRM are well established, determinants of its interaction with environment keep poorly understood. The role of general host-related stimuli on the behavioral response of the PRM, like CO2 and temperature, was well investigated. However, the role of volatile organic compounds (VOCs) other than CO2 found in the chemical landscape constituted by the henhouse environment on PRM behaviour received little attention. The aim of the study was to explore the attractiveness of some of the VOCs present in farm buildings and their interaction with temperature. We evaluated the attractive response of starved PRM female adults to 8 volatiles compounds commonly found in the farm context, either alone or associated in a blend, in two choice test bioassays (one performed in a Y-tube olfactometer, another one in a field-mimicking lab design). The impact of temperature on the attractiveness of VOCs was studied using a heated substrate. Our results showed that a single VOC (ammonia) and one VOC blend were significantly attractant to PRM in our laboratory conditions. The interaction between VOCs and temperature had a significant impact on PRM attraction. Our work brings fundamental information on chemical interactions between PRM and its environment in farm buildings. This study demonstrates the potential of using volatile substances to manipulate the behavior of PRM, combined or not to different stimuli, to elaborate an attract-and-kill control strategy. The authors would like to thank the European Cooperation in Science and Technology (COST Action (FA1404 - COREMI) “Improving current understanding and research for sustainable control of the poultry red mite Dermanyssus gallinae”).
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... Yet to date no published study has focused on the actual airborne volatiles emitted by birds. There are only a small number of studies on chemical signals emitted from whole birds, with most studies focusing on insects and rodents (Moritz & Crewe 1988, Card e & Millar 2004, Douglas 2006, R€ ock et al. 2006. Sampling odours (and VOCs) from a relatively large vertebrate in a remote field location is a logistical challenge. ...
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Smell is a sensory modality that is rarely considered in birds, but evidence is mounting that olfaction is an important aspect of avian behaviour and ecology. The uropygial gland produces an odoriferous secretion (preen oil) that can differ seasonally and between the sexes. These differences are hypothesized to function in olfactory camouflage, i.e. minimizing detection by nest predators (olfactory crypsis hypothesis), and/or intraspecific olfactory communication, particularly during breeding (sex semiochemical hypothesis). However, evidence for seasonal and sex differences in preen oil is mixed, with some studies finding differences and others not, and direct evidence for the putative function(s) of seasonal variation and sex differences in preen oil remains limited. We conducted a systematic review of the evidence for such changes in preen oil chemical composition, finding seasonal differences in 95% of species (57/60 species in 35 studies) and sex differences in 47% of species (28/59 species in 46 studies). We then conducted phylogenetic comparative analyses using data from 59 bird species to evaluate evidence for both the olfactory crypsis and sex semiochemical hypotheses. Seasonal differences were more likely in the incubating than non‐incubating sex in ground‐nesting species, but were equally likely regardless of incubation strategy in non‐ground‐nesting species. This result supports the olfactory crypsis hypothesis, if ground nesters are more vulnerable to olfactorily searching predators than non‐ground nesters. Sex differences were more likely in species with uniparental than biparental incubation and during breeding than non‐breeding, consistent with both the olfactory crypsis and sex semiochemical hypotheses. At present, the data do not allow us to disentangle these two hypotheses, but we provide recommendations that will enable researchers to do so.
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Individual Chemical Profiles in the Leach’s Storm-Petrel
Article
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Odor is linked to adrenocortical function and male ornament size in a colonial seabird
Article
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Crested auklets (Aethia cristatella), colonial seabirds of Alaska and Siberia, emit a citrus-like odorant from wick-like feathers. We examined whether the odorant emission is linked to adrenocortical function and correlated with size of the crest feather ornament. Conventional signals like the size of crest ornament are inexpensive to produce and thus may be prone to deception. However, assessment signals such as the odorant could be more reliable if they impose costs and more proximate since they are continually produced. This may be the case for the crested auklet’s volatile aldehyde odorant. The signal is composed of highly volatile chemicals that appear to be products of fatty acid metabolism. Adrenocortical function helps to mobilize endogenous resources for metabolism. Elevation of corticosterone may be needed to sustain a reliable chemical signal, but there are physiological costs for prolonged elevation of circulating corticosterone. We predicted that higher odorant emissions would be correlated with larger crest ornaments. Furthermore, we predicted that odorant emissions would be linked to adrenocortical response. Octanal, the most abundant compound in the citrus-like odorant, was positively correlated with crest size (r = 0.37) in males, and adrenocortical response explained 42% of the variation in octanal emissions, after controlling for stage of the breeding period. Adrenocortical response was positively correlated with octanal emissions (rs = 0.57) in females. We conclude that dominant individuals with greater capacity to mount a more robust stress response may have greater capacity to sustain odorant secretions.
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Odors and ornaments in crested auklets (Aethia cristatella) signals of mate quality?
Thesis
Full-text available
  • Aug 2006
Crested auklets (Aethia cristatella) are small colonial seabirds that display an ornamental feather crest and emit a citrus-like odorant during the breeding season. In this study odors and ornaments were investigated as possible signals of mate quality. Crest size was negatively correlated with the stress hormone corticosterone in males, but this was not the case in females. Body condition was negatively correlated with corticosterone in females, but this was not the case in males. Corticosterone levels were interpreted as an index of physiological condition, and it was concluded that males with longer crests were more competent at meeting the social and energetic costs of reproduction. I hypothesized that the crested auklet odorant: 1) functions as a chemical defense against ectoparasites, 2) is assessed as a basis for mate selection, 3) is facilitated by steroid sex hormones. Laboratory and field experiments showed that synthetic replicas of the crested auklet odorant repelled, impaired, and killed ectoparasites in a dose-dependent fashion. Chemical concentrations in plumage were at least sufficient to repel and impair ectoparasites. Chemical emissions from breeding adult crested auklets peaked at the time of egg hatching when young are most vulnerable to tick parasitism. In males, chemical emissions were correlated with crest size, a basis for mate selection. Presentation of synthetic aldehydes elicited behaviors similar to those that occur during courtship. Captive crested auklets responded preferentially to synthetic replicas of their odor, and the highest frequency of response occurred during early courtship. These results show that the chemical odor could be a basis for mutual mate selection. Production of the chemical odorant may be facilitated by steroid sex hormones since octanal emission rates were correlated with progesterone in males. Finally it was determined that the chemical composition of odorants in crested auklets and whiskered auklets (A. pygmaea) differed in three key respects. This suggests that an evolutionary divergence occurred in the odorants of the two species similar to what has been suggested for ornamental traits. In conclusion, crested auklets appear to communicate with odors and ornaments, and these signals may convey multiple messages regarding condition, quality, and resistance to parasites.
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Odors and ornaments in crested auklets (Aethia cristatella) signals of mate quality?
Thesis
Full-text available
  • Aug 2006
Crested auklets (Aethia cristatella) are small colonial seabirds that display an ornamental feather crest and emit a citrus-like odorant during the breeding season. In this study odors and ornaments were investigated as possible signals of mate quality. Crest size was negatively correlated with the stress hormone corticosterone in males, but this was not the case in females. Body condition was negatively correlated with corticosterone in females, but this was not the case in males. Corticosterone levels were interpreted as an index of physiological condition, and it was concluded that males with longer crests were more competent at meeting the social and energetic costs of reproduction. I hypothesized that the crested auklet odorant: 1) functions as a chemical defense against ectoparasites, 2) is assessed as a basis for mate selection, 3) is facilitated by steroid sex hormones. Laboratory and field experiments showed that synthetic replicas of the crested auklet odorant repelled, impaired, and killed ectoparasites in a dose-dependent fashion. Chemical concentrations in plumage were at least sufficient to repel and impair ectoparasites. Chemical emissions from breeding adult crested auklets peaked at the time of egg hatching when young are most vulnerable to tick parasitism. In males, chemical emissions were correlated with crest size, a basis for mate selection. Presentation of synthetic aldehydes elicited behaviors similar to those that occur during courtship. Captive crested auklets responded preferentially to synthetic replicas of their odor, and the highest frequency of response occurred during early courtship. These results show that the chemical odor could be a basis for mutual mate selection. Production of the chemical odorant may be facilitated by steroid sex hormones since octanal emission rates were correlated with progesterone in males. Finally it was determined that the chemical composition of odorants in crested auklets and whiskered auklets (A. pygmaea) differed in three key respects. This suggests that an evolutionary divergence occurred in the odorants of the two species similar to what has been suggested for ornamental traits. In conclusion, crested auklets appear to communicate with odors and ornaments, and these signals may convey multiple messages regarding condition, quality, and resistance to parasites.
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Heteropteran chemical repellents identified in the citrus odor of a seabird (crested auklet: Aethia cristatella): Evolutionary convergence in chemical ecology
Article
Full-text available
  • Aug 2001
The exogenous application of chemical repellents is widespread in birds, but endogenous production is exceedingly rare. We herein report a new class of avian defensive compounds isolated from the feathers and volatile odor of the crested auklet (Aethia cristatella). Mass spectra indicate that n-hexanal, n-octanal, n-decanal, Z-4-decenal and a 12-carbon unsaturated aldehyde comprise the auklet odorant. Octanal and hexanal are also secreted in the repugnant metasternal gland emissions of heteropteran insects and are known to be potent invertebrate repellents. We suggest that the auklet odorant functions as an ectoparasite repellent and a signal of mate quality. This would represent a rare and direct link between vigor, quality and parasite resistance, one of several putative bases for mate selection. This is the first report of defensive compounds produced by a seabird or colonial bird and one of the few examples of chemical defense in a polar or subpolar marine vertebrate.
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An Experimental Field Study of the Function of Crested Auklet Feather Odor
Article
  • Feb 2004
During the breeding season, female and male Crested Auklets (Aethia cristatella; Alcidae) emit a pungent citruslike odor from their plumage. Previous experiments showed that captive birds oriented toward sources of the natural odor and toward isolates of its major constituents, cis-4 decenal and octanal, and avoided a noxious odor. In a blind experiment we manipulated odor on 12 life-sized, realistic Crested Auklet models (6 males, 6 females) to test for a social or sexual preference for the odor isolates in a natural setting. Based on the quantified behavior of 555 males and 280 females that approached the models at a breeding colony, we found no evidence for a sexual preference for models with added odor. Female auklets that approached male models with artificially added odor were no more likely to perform sexual displays than females that approached control models with less odor. Fewer males approached female models but the effect was the same: males that approached female models with artificially added odor were no more likely to perform sexual displays. However, males approached scented male models more closely and for longer duration than they approached control male models, and females approached scented male models more closely. Our findings confirm previous experiments with captive birds and further suggest that Crested Auklets' plumage odor serves at least a general social function. Estudio Experimental de Campo de la Función del Olor de las Plumas en Aethia cristatella Resumen. Durante la estación reproductiva, el plumaje del macho y la hembra de Aethia cristatella (Alcidae) emite un olor picante-cítrico. Experimentos previos han demostrado que las aves en cautiverio se orientan hacia fuentes de olor natural y hacia extractos de sus principales constituyentes, cis-4 decano y octano, y evitan un olor nocivo. En un experimento a ciegas, manipulamos el olor en 12 modelos de tamaño real de A. cristatella (6 machos y 6 hembras) para probar la preferencia sexual o social por los extractos en un ambiente natural. Basados en el comportamiento cuantitativo de 555 machos y 280 hembras que se acercaron a los modelos en la colonia reproductiva, no encontramos ninguna evidencia por una preferencia sexual por los modelos con el olor añadido. Las hembras de A. cristatella que se aproximaron a los modelos con el olor artificial añadido no presentaron una probabilidad mayor de realizar despliegues sexuales que las hembras que se acercaron a modelos con poco olor (control). Sin embargo, los machos se acercaron más y por más tiempo a los modelos de macho con olor que a los modelos de macho control, y las hembras se acercaron más a los modelos de macho con olor. Nuestros resultados confirman experimentos previos en aves en cautiverio y sugieren que el olor del plumaje de A. cristatella tiene por lo menos una función social general.
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Hyperinfestation by Ticks Ixodes uriae: A Possible Cause of Death in Adult King Penguins, a Long-Lived Seabird
Article
  • Jan 1998
We report cases of death in adult King Penguins (Aptenodytes patagonicus) hyperinfested by the tick Ixodes uriae. The distribution and level of infestation by ticks were assessed by skin samples of body parts. The preferred feeding sites on the host were the head and the neck for adult and nymph ticks, and the lower parts for larvae. King Penguins carried up to 263 adults, 548 nymphs, or 3,500 larvae. We have been able to estimate the amount of blood loss in King Penguins during the incubation shift. These results are discussed in relation to the breeding behavior of this colonial waterbird.
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