Nature Blog Network

Saturday, October 9, 2010

Cranes may sniff aphrodisiacs

 Do cranes emit and perceive sex pheromones?

Personal perspective
In 1958, one of the Blogauthors (George) chose Cornell University for graduate study in bird behavior and animal communication. I was intrigued by three kinds of signals:
  • Sounds - Birds and insects have rich repertoires of chirps, songs, and buzzes.
  • Visual displays  - Birds present feathery dynamic postures and insects flash markings on their wings.
  • Scents  - In 1958, clever chemists used new technologies like gas chromatography to isolate pheromones1 and defensive secretions2 . Scientists were astonished to discover that a single substance could trigger a whole chain of behaviors in insects. 
Chemical signaling was the emerging field, but searching for avian pheromones appeared to hold little promise.  Pierre Grassé's Traité de Zoologie3, the zoologist's Bible of that era, stated that most birds are anosmic, without a robust sense of smell.

Thus I opted to do my doctoral thesis on insects when I changed advisers in 1959. 

What a difference a half-century makes! 

           ============================

What data argue that birds use pheromones?

In 1959, we knew:

1. Birds have well-developed exocrine glands, including uropygial glands at the base of the tail, anal glands, salt glands, and ear glands, most of which produce greasy odorous mixtures. 

2. Birds spread these secretions upon their feathers when they preen.

In 2010, we also know:

 3. Exocrine secretions, especially those from the uropygial glands, vary according to age, species, season of the year, and hormonal state4-10.

 4. Birds are far from anosmic. Bird brains "have the right stuff" to distinguish odors.
  • Birds have nostrils, olfactory cavities, and olfactory neurons that are anatomically like those of mammals. Olfactory information flows to well-developed brain centers that include the piriform cortex, amygdala, and entorhinal cortex32,33, parts of the brain that are associated with emotion. As theropod dinosaur descendants gave rise to birds (see How birds think blog, 9-Feb-2011), the olfactory bulb became larger31, suggesting  increasing importance of the sense of smell to the life styles of birds. 
  • Olfactory receptor (OR) genes encode proteins that are embedded in the surfaces of olfactory neurons and can discriminate among odorous molecules. Silke Steiger in Starnberg Germany10-12 showed that birds have hundreds of OR genes, comparable in diversity to mammal ORs.  The fact that one large gene clade, termed γ-c, is expanded across the class Aves, argues for the importance of olfaction for many birds.
  • In the last decade, there has been wholesale rethinking about bird brain architecture13. The superficial appearance of the brain differs between birds and mammals, but the contrasts are mostly due to topological shuffling of neuron clusters and centers. Birds have sophisticated information processing capacity. 
5.  Birds use their sense of smell, for example: to find food, to distinguish individuals from one another, to recognize nest sites (petrels), and for many other purposes5. Three notable examples involve mating.
  • Since 1979, Jacques Balthazart and others at the University of Leige in Belgium have been convincingly pleading the case for duck sex pheromones from the uropygial glands, starting with their classic paper demonstrating hormonal control of secretion14. 
  • Male chickens (roosters) court with a sequence of behaviors: first waltzing, then mounting, and finally copulating. Hirao and colleagues (2009) surgically excised uropygial glands of female chickens and then placed roosters with either intact or "glandectomized" females. Roosters waltzed equally with both groups of hens, but they mounted and copulated significantly more often with intact hens.  Surgically anosmic roosters couldn't tell the difference15.
  • Tobias Krause and his colleagues at Bielefeld University in Germany recently reported that a songbird can recognize kin by smell. The experimental data clearly demonstrate that zebra finch chicks fostered at 2 days of age into unrelated broods prefer the odor of their hatch-nest over that of the foster-nest34. 
6.  In 2010, the molecular components of sex-specific odorants were identified in the oils from uropygial glands.
  • Jerome Mardon and colleagues showed that, during the breeding season, there is a sex-biased chemosignal (more C23-C28 esters) in uropygial secretions of female petrels. It has not yet been possible to demonstrate that the "Sex signal" affected male behavior under field conditions16.
  • Jian-Xu Zhang and others from the Chinese Academy of Sciences (Beijing) report that a blend of 18-, 19-, and 20-carbon alcohols, found in uropygial secretions of both male and female budgerigars, are strongly enriched in males.  With a classic Y-maze bioassay, they showed that the alkanol blend, reconstituted from pure chemicals, was attractive to female budgerigars17. 
7. Recent papers document individual recognition by scent in humboldt penguins35 , petrels36 and zebra finches37 .
8.  A 2013 paper38 strongly suggests that male satin bowerbirds paint their spectacular bowers with chemical signals.  The paint is attractive females who taste it.
Why haven't more ornithologists seen birds use pheromones? 

Birders have logged millions of hours watching birds. How could pheromones escaped their attention for so long?

We think that the answer is threefold:

  = First, because birds don't wave mobile pendulous snouts as they walk about.
In a seminal article, Samuel Caro and Jacques Balthazart argue persuasively for the existence of bird pheromones. These authors suggest that birds aren't obvious when they use chemical signals:
 "Mammals extend their neck, move their head, sniff, and track the source of the odor.....Birds, in contrast, have developed a wide array of alternative communication signals and do not show behaviors typically associated with olfactory sampling..." 5 (italics added).
  = Second, because most of the accumulating evidence1has been published in biochemical publications rather than the birder journals that are read by most ornithologists.

   = Third, because it takes a lot of expensive scientific slogging to get from observation and experiment in the field and laboratory, to purification of the molecules, to behavioral assay, and finally to manipulating physiological context, all of which must come together to definitively prove pheromone function.

The roles of pheromones can be obvious or subtle.
  • Pheromones (including blends of several substances) can be classical releasers that trigger a quick behavioral response or primers that cause a specific but sustained change in physiological state. 
  • Pheromones could mediate general arousal, like a perfume that is "chemical mood music".  
  • A given pheromone signal could be emitted by both sexes and/or could impact both sexes. 
Pheromone research starts with observations of behavior. Let me digress by presenting a personal example:

In 1969 after several years of behavioral experiments, George and his students concluded that mealworm beetles use multiple sex pheromones18, 19 (diagram left): A) an attractant produced by male beetles for females; B) a substance from females that excites males; C) an antiaphrodisiac produced by males that inhibits other male competitors, and  D) primer pheromones that accelerate oocyte maturation in females.

Next, the behavior needed validation by chemistry. But my laboratory and other colleagues failed in attempts to chemically purify even one of these four putative pheromones. So instead, after 1970, we pursued research themes in cell and developmental biology.

In ensuing last 40 years, our conclusions, based on behavior, have been validated by the work of chemists. In 1986, a Japanese group identified B, the female beetle's attractant20. Recently (2005), an English group isolated A, the male's attractant21. Since the existence of antiaphrodisiac C and primer D have not been definitively confirmed by isolation and bioassay of a pure substance, the case for each of these is yet incomplete.
 
The case for pheromones in Sandhill Cranes

Three lines of evidence strongly suggest that cranes use pheromones:
   =First - Cranes have capacious uropygial glands that secrete a melange of oils and waxes. The drawing to the right is the uropygial gland of a Sandhill Crane22.  In his classic inventory of uropygial secretions23,24, Jürgen Jacob found that crane uropygial secretions contain unusually large proportions of sesquiterpenes and diterpenes, substances built up from isoprene building blocks like those used to make steroids. Isoprenoids are auspicious pheromone candidates.

    =Second - Every crane repeatedly harvests secretions of its uropygial gland (left, below) and wipes the greasy gue over their wing and body feathers (right, below) as it preens.


   =Third - In nature, both crane sexes exhibit a fascinating exploratory behavior (photo to the right) as they pace forward just before copulation. It has been sketched for Eurasian Cranes by Paul Johnsgard25 (who called it 'parade march'). It has been named 'bill-raising' in Red-crowned Cranes by Masatomi and Kitagawa26, and included in most accounts of crane precopulatory rituals25-28.

In our Crane Display Dictionary29, we suggest that the 'Parade-march' can facilitate olfaction.

We agree with Caro and Balthazart that most species of birds "... do not show behaviors typically associated with olfactory sampling".5 However, there are exceptions where sniffing seems evident. We believe that two of the notable  exceptions are the Parade-march posture of cranes and the Ruff-Sniff behavior of Crested Auklets (seen to the right in a drawing from Hunter and Jones).30

Given these lines of evidence, we conclude that it is quite plausible that cranes emit and perceive reproductive pheromones. This idea deserves serious further investigation:
  • Uropygial glands of captive cranes could be milked and analyzed. Are the secretions sex specific? age specific? seasonally changing? species specific? affected by changes in hormones? 
  • A quantitative bioassay needs to be developed for cranes. With a behavioral or physiological bioassay, one could ask whether responsiveness to crude uropygial secretions, purified components, or defined mixtures varies with sex, season, endocrine background, etc.
  • Can purified pheromones or mixtures be tools for improved crane husbandry and thus assist in conservation of endangered species of cranes?  

References:
1. Karlson P. Lusher M 1959. 'Pheromones': A new class of biologically active substances. Nature 183:55-56.
2. Roth LM, Eisner T 1962. Chemical defenses of arthropods. Ann Rev Ent 7:107-136.
3. Grassé P-P 1950. Traité de Zoologie, Tome XV. Oiseaux.
4. Hagelin JC, Jones IL 2007. Bird odors and other chemical substances: a defense mechanism or overlooked mode of intraspecific communication? Auk 125:741-761.
5. Caro SP, Balthazart J 2010. Pheromones in birds: myth or reality? J Comp Physiol A 196:751-66.
6. Kolattukudy PE, Rogers L 1987. Biosynthesis of 3-hydroxy fatty acids, the pheromone component of female mallard ducts, by cell-free preparations from the uropygial gland. Archiv Biochem Biophys 252:121-129.
7. Bhatttacharyya SP, Chowdhury M 1987. The effect of androgen on the composition of lipid material of the preen gland of pigeons. Folia Biologica 26: 15-32.
8. Bohnet SI, Rogers G, Sasaki G, Kolattukudy PE, 1991. Estradiol induces proliferation of peroxisome-like microbodies and the production of 3-hydroxy fatty acid diesters, the female pheromones, in the urogygial glands of male and female mallards. J Biol Chem 266:9795-9804.
9. Bhatttacharyya SP, Chowdhury M 1995. Seasonal variation in the secretory lipids of the uropygial gland of a subtropical wild passerine bird, Pycnonotus cafer, in relation to the testicular cycle. Biol Rhythm Res 26:79-87.
10. Steiger SS, Fidler AE, Valcu M, Kempenaers B 2008. Avian olfactory receptor gene repertoires: evidence for a well-developed sense of smell in birds? Proc Roy Soc B 275:2309-2317.
11. Steiger SS, Kuryshev VY, Stensmyr MC, Kempenaers B, Mueller JC 2009. A comparison of reptilian and avain olfactory gene repertoires: Species-specific expansion of group γ genes in birds. BMC Genomics 10:446-456.
12 Steiger SS, Fidler AE, Mueller JC, Kempenaers B 2010. Evidence for adaptive radiation of olfactory receptor genes in 9 bird species. J Heredity 101:325-333. 
13. Jarvis ED, Gunturkun O (25 colleagues), Reiner A, Butler AB, 2005. Avian brains and a new understanding of vertebrate brain evolution. Nature Reviews Neuroscience 6:151-159.
14. Balthazart, J, Schoffeniels E 1979. Pheromones are involved in the control of sexual behaviour in birds. Naturwiss 66:55-56.
15. Hirao A, Aoyama M, Sugita S 2009. The role of uropygial gland on sexual behavior in domestic chicken Gallus gallus domesticus. Behav Process 80:115-120. 
16. Mardon J, Saunders SM, Anderson SM, Chouchoux C, Bonadonna F 2010. Species, gender, and identity: Cracking the petrel's sociochemical code. Chem Senses 35:309-321.
17. Zhang J-X, Wei W, Zhang J-H, Yang, W-H. 2010. Uropygial gland-secreted alcohols contribute to olfactory sex signals in budgerigars. Chem Senses 35:375-382.
18. Happ GM 1969. Multiple sex pheromones of the mealworm beetle, Tenebrio molitor L. Nature 222:180-181.
19. Happ GM, Schroeder ME, Wang JCH 1970. Effects of male and female scent on reproductive maturation in young female Tenebrio molitor. J. Insect Physiol 16: 1543-1548.
20. Tanaka Y, Osawa K, Honda H, Yamamoro I 1986. A sex attractant of the yellow mealworm beetle, Tenebrio molitor, and its role in mating behaviour. J Pest. Sci 11:49-55.
21. Bryning GP, Chambers J, Wakefield ME 2005. Identification of a sex attractant from male yellow mealworm beetles, Tenebrio molitor. J Chem Ecol. 31: 2721-2730.
22. Johnston DW 1988. A morphological atlas of the uropygial gland.  Bulletin of the British Museum (Natural History). Zoology series. 54(55):199-258.
23. Jacob J, Plawer J, Rosenfeldt P 1979. Gefiederwachskompositionen von Kranichen und Rallen. Beitrag zur Systematik der Gruiformes. J Ornithol 120:54-63.
24. Jacob, J. 1982. Uropygial gland secretions and feather waxes. Avian Biology, Vol VI, edited by Farner DS, King JR, Parkes KC , Academic Press, New York, pp199-324.
25.Johnsgard P 1983. Cranes of the World. 2. Individualistic and social behavior. Papers in Biological Sciences, University of Nebraska, Lincoln, pp. 11-24.
26. Masatomi H, Kitagawa T 1975. Bionomics and sociology of the Japanese Crane, Grus japoniensis, II. Ethogram. Jour. Fac. Sci. Hokkaido Univ. Ser. VI, Zool. 19:834-878. 
27. Ellis DH, Swengel SR, Archibald GE, Kepler CB 1998. A sociogram for cranes of the world. Behav Process 43:125-151. 
28. Masatomi H 1983. Some observations on mating behaviour of several cranes in captivity. J. Ethol. 1:62-69.
29. Happ, CY,  Happ GM 2011. Sandhill Crane Display Dictionary. What cranes say with their body language. Waterford Press.
30. Hunter FM. Jones IL 1999. The frequency and function of aquatic courtship and copulation in least, crested, whiskered, and parakeet auklets. The Condor 101:518-528. 
31.  Zelenitsky DK, Therrien F, Ridgley RC, McGee AR, Witmer LM. 2011. Evolution of olfaction in non-avian theropod dinosaurs and birds. Proc Roy Soc B doi:10.1098/rspb.2011.0238. 
32. Reiner A, karten HJ 1985. Comparison of olfactory bulb projections in pigeons and turtkes. Brain Behav Evol 27:11-27.
33. Abellan A, Legaz I, Vernier B, Retaux S, Medina L 2009. Olfactory and amygdalar structures of the chicken ventral pallium based on the combinational expression patterns of LIM and other developmental regulatory genes. J Comp Neurol 516:166-186. 
34. Krause ET, Kruger O, Kohlmeir P, Caspers BA, 2012. Olfactory kin recognition in a songbird. Biology Letters, published online   doi:10:198/rsbl.2011.1093.
35. Coffin HR, Watters JV, Mateo JM 2011 Odor-Based Recognition of Familiar and Related Conspecifics: A First Test Conducted on Captive Humboldt Penguins (Spheniscus humboldti) PloS ONE 6:e25002
36. Mardon J, Saunders SM, Anderson MJ, Couchoux C, Bonadonna F 2010. Species, Gender, and Identity: Cracking Petrels' Sociochemical Code, Chem Senses 35:309-321.
37. Caspers BA, Krause ET 2011 Odour-based natal nest recognition in the zebra finch (Taeniopygia guttata), a colony-breeding songbird. Bio Lettr 7:184-186
38. Hicks RE, Larned A, Borgia G 2013  Bower paint removal leads to reduced female visits, suggesting bower paint as a chemical signal. Anim Behav online http://dx.doi.org/10.1016/j.anbehav.2013.03.007.

Updated: April 17, 2011 & January 5, 2012 & April 17, 2013
Posted by Christy Yuncker and George Happ at 6:15 PM

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