Colonial seabird's paralytic perfume slows lice down: an opportunity for parasite-mediated selection?

Selection for chemical signals in birds could be influenced by parasitism as has been previously suggested for visual and acoustic displays. Crested auklets (Aethia cristatella), colonial seabirds from Alaska and Siberia, offer an example of how this might occur. Crested auklets secrete lipids in plumage, possibly as an indicator of status and attractiveness. Prominent among these secretions are aldehydes, which are noticeable as a pungent citrus-like odour. Octanal and hexanal, the most abundant aldehydes in the plumage of crested auklets, are potent invertebrate repellents, reported from the chemical defenses of heteropteran insects. These aldehydes occur at high concentrations within specialized secretory structures. Experiments presented here show that these compounds can paralyse lice. Lice obtained from auklets were paralysed or killed within seconds after exposure to volatiles from nicks in the integument of a crested auklet. Chemical analysis demonstrated the presence of aldehydes in the area of integument used for this experiment. Lice exposed to control tissues in the same manner were not affected. A synthetic blend of crested auklet odourant constituents caused a sequence of impaired behaviours in auklet lice comparable to the effects of neuroactive insecticides. The time until onset of effects was dependent on dose, suggesting that the rate of molecular diffusion into louse spiracles was the explanatory factor. Impairment was evident even at very low concentrations that can occur in crested auklet plumage during winter. The same aqueous emulsions were present in both experimental and control treatments but lice in controls experiments were not affected. Crested auklets inhabit crowded social neighbourhoods with larger social groups, closer interindividual spacing and higher rates of contact than sympatric least auklets (Aethia pusilla). This could help to explain why crested auklets can have higher louse abundances. Lice are spread through direct contact between hosts and louse-infected mates could transmit lice to offspring. Large differences in the louse loads on crested auklet fledglings suggest differences in the parental transmission of lice to offspring.

Size of ornament is negatively correlated with baseline corticosterone in males of a socially monogamous colonial seabird.

The Goymann-Wingfield model predicts that glucocorticoid levels in social animals reflect the costs of acquiring and maintaining social status. The crested auklet is one of the few avian colonial species where a mutual ornament in males and females is used in both sexual and aggressive displays. Previous studies of the crested auklet support the notion that the crest ornament is a badge of status in this species. Here, we examined the relationship between the crest ornament size and the adrenocortical function in breeding crested auklets. Crest length was negatively correlated with corticosterone at baseline in males, but not in females. Baseline corticosterone in females (but not in males) was negatively correlated with body condition index. Although male and female crested auklets are monomorphic in their ornamental traits, our results suggest that the socially mediated physiological costs associated with status signaling may differ between the sexes.

Seasonal covariation in progesterone and odorant emissions among breeding crested auklets (Aethia cristatella).

Crested auklets emit a citrus-like odorant that is seasonally modulated, suggesting that it is a secondary sexual trait. We hypothesized that expression of the chemical odorant is facilitated by steroid hormones, similar other secondary sexual traits in birds. Therefore we examined variation in concentrations of hormones in blood plasma and odor production during incubation and early chick rearing. A novel method was used to obtain and measure chemical emissions of crested auklets. Blood plasma samples were analyzed by radioimmunoassay. Progesterone was detected in all birds, and it varied during the breeding season. Octanal emissions covaried with progesterone levels in males but not in females. No seasonal patterns were detected in testosterone, estrogen or DHT, and these hormones were not detected in all breeding adults. Covariance of progesterone and octanal emissions in males suggests there could be at least an indirect relationship between odor emissions and steroid hormones in this species. Thus expression of the citrus-like odorant of crested auklets, like other secondary sexual traits in birds, could be regulated by steroid hormones.

Prenuptial perfume: alloanointing in the social rituals of the crested auklet (Aethia cristatella) and the transfer of arthropod deterrents.

Alloanointing, the transfer of chemicals between conspecifics, is known among mammals, but hitherto, the behavior has not been documented for birds. The crested auklet (Aethia cristatella), a colonial seabird of Alaskan and Siberian waters, alloanoints during courtship with fragrant aldehydes that are released from specialized wick-like feathers located in the interscapular region. Crested auklets solicit anointment at the colony, and prospective mates rub bill, breast, head, and neck over wick feathers of their partners. This distributes aldehydes over the head, neck, and face where the birds cannot self-preen. The resulting chemical concentrations are sufficient to deter ectoparasites. Auklets that emit more odorant can transfer more defensive chemicals to mates and are thus more sexually attractive. Behavioral studies showed that crested auklets are attracted to their scent. Wild birds searched for dispensers that emitted their scent and rubbed their bills on the dispensers and engaged in vigorous anointment behaviors. In captive experiments, naïve crested auklets responded more strongly to synthetic auklet scent than controls, and the greatest behavioral response occurred during early courtship. This study extends scientific knowledge regarding functions of alloanointing. Alloanointing had previously been attributed to scent marking and individual recognition in vertebrates. Alloanointing is described here in the context of an adaptive social cue--the transfer of arthropod deterrents between prospective mates.

Measurement of chemical emissions in crested auklets (Aethia cristatella).

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 micro l/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.

Interspecific differences in Aethia spp. auklet odorants and evidence for chemical defense against ectoparasites.

The true auklets (Genus Aethia) are small planktivorous seabirds of the Bering Sea and North Pacific. Two species, the crested and whiskered auklets produce volatile citrus-like odorants. We here show that the whiskered auklet odorant is composed predominantly of two odd-numbered aldehydes (heptanal and nonanal) with no detectable unsaturated aldehydes. By comparison the crested auklet odorant is dominated by even-numbered aldehydes, both saturated and monounsaturated, ranging in size from 6 to 12 carbons. This is evidence of species-specific acquisition or biosynthetic pathways. We clarify the chemistry of the crested auklet odorant. We cite evidence that the C-12:1 aldehyde in crested auklets is actually two isomers, (Z)-4-dodecenal and (Z)-6-dodecenal. We also report on experimental evidence that aldehyde constituents kill and repel ectoparasites. Efficacy of the aldehydes may increase when they are combined in a mixture. The repellency of the mixture increases with chemical concentration. This suggests that individuals with higher chemical production are likely to repel ectoparasites more effectively.