Love is in the air - aerial courtship displays in the bird world.

Aerial courtship displays are fairly common throughout the avian world, however relatively little is known about the complexities and functions of these displays (Arroyo et al. 2013). Just as morphological characteristics can be used by females to assess the quality of a prospective male, so too can behavioural displays (Clark 2009). Some behavioural displays may serve as an honest indication of overall condition and may become elaborate and exaggerated due to directional selection caused by female preference (Arroyo et al. 2013, Clark 2009). 

The Golden Eagle (Aquila chrysaetos) is just one of many species of birds that perform aerial courtship displays, https://www.youtube.com/watch?v=koWpTZ8Jo-s. Viewed on 30th April 2017.

Male Anna's Hummingbirds (Calypte anna) perform spectacular aerial dives as a component of their courtship behaviour, in which they can reach speeds of up to 385 body lengths per second - achieving the highest known length-specific velocity of any vertebrate (Clark 2009). Males ascend to a height of approximately 30m before diving head first and swooping over a watching female (Clark & Feo 2008). As they perform this incredibly fast dive they emit a brief, loud squeak or chirp produced by air passing over their tail feathers (Clark & Feo 2008). It is a puzzling display as the males go to great lengths to produce this sound that requires extremely high velocities, but are capable of singing at the same frequency (Clark & Feo 2008). So why do they go to this effort to produce an accoustically similar sound mechanically when they can produce it vocally??? Another unanswered question!!!

The male Anna's Hummingbird (Calypte anna) achieves the highest known length-specific velocity of any vertebrate. Image sourced from http://animalia-life.club/birds/annas-hummingbird.html. Viewed on 28th April 2017.

The male Anna's Hummingbird (Calypte anna) performing his incredible aerial display. Listen and watch closely or you just might miss it! https://www.youtube.com/watch?v=7Rm5RfuexGU. Viewed on 29th April 2017.

Raptors are well known for their spectacular aerial displays (Arroyo et al. 2013). In one species of raptor, the Montagu's Harrier (Circus pygargus), males perform frequent "sky-dancing" displays  leading up to the breeding season, in which they ascend before rapidly plunging downward while performing twists, undulations, loops and display calls (Simmons 1988). The timing of these displays suggests that they may well be used in the process of mate appraisal and selection (Arroyo et al. 2013, Simmons 1988). The "aerial display hypothesis" in which aerial agility and hence small size is favoured by sexual selection, is also supported by this species in which males are lighter and more agile than females (Arroyo et al. 2013, Simmons 1988).

The striking looking male Montagu's Harrier (Circus pygargus) perform frequent "sky-dancing" displays  leading up to the breeding season. Photo by Saptagirish Oleti, http://www.girisholeti.com/show_photo.php?album_id=1&photo_id=47. Viewed on 29th April 217.

These are just two examples of the many species of birds that perform aerial courtship displays. I have been lucky enough to witness some of these incredible aerial courtship displays first-hand, the most impressive of which would have to be that of the Red-tailed Tropicbird, although I found it difficult to learn anything about this in the scientific literature. The birds gracefully circle each other over the ocean in the period leading up to the breeding season - a beautiful display by a beautiful bird!!!

Red-tailed Tropicbirds (Phaethon rubricauda) performing an aerial courtship display. Photo by Paul Mckenzie, http://www.wildencounters.net/2012/06/midway-atoll-april-2012/. Viewed on 29th April 2017.

References

Arroyo, B., Mougeot, F. & Bretagnolle, V. 2013, "Characteristics and sexual functions of sky-dancing displays in a semi-colonial raptor, the montagu's harrier (Circus pygargus)", Journal of Raptor Research, vol. 47, no. 2, pp. 185-196

 

Clark, C.J. 2009, "Courtship dives of Anna's hummingbird offer insights into flight performance limits", Proceedings of the Royal Society B: Biological Sciences, vol. 276, no. 1670, pp. 3047-3052.

Clark, C.J. & Feo, T.J. 2008, "The Anna's hummingbird chirps with its tail: a new mechanism of sonation in birds", Proceedings of the Royal Society B: Biological Sciences, vol. 275, no. 1637, pp. 955-962.

Simmons, R. 1988, "Honest advertising, sexual selection, courtship displays, and body condition of polygynous male harriers", The Auk, vol. 105, no. 2, pp. 303-307.

Olfactory cues in seabirds as a driver of sexual selection.

When we think of sexual selection in birds we usually think of colour, song and their associated displays, but what about scent? A functional sense of smell has been exhibited by every bird that has been tested, yet the study of chemical signalling in birds has been historically neglected (Hagelin et al. 2003, Roper 1999). It has now been shown that some species of seabirds display olfactory discrimination capabilities, suggesting that scent may provide valuable information as to the quality of prospective mates and also be used as an inbreeding avoidance mechanism (Mardon & Bonadonna 2009). 

The Blue Petrel (Halobaena caerulea) has been shown to prefer the odour of its mate and other conspecifics than that of itself (Mardon & Bonadonna 2009). This odour recognition and preference could serve many functions but it has been suggested that it may be used to facilitate genetically based mate choice (Mardon & Bonadonna 2009, Zelano & Edwards 2002). Olfactory signals from urine or body odours have been associated with certain genotypes in many species of vertebrates, meaning that chemical signalling may be also playing a role in mediating mate choice in birds (Mardon & Bonadonna 2009, Singh 2001).

The Blue Petrel (Halobaena caerulea) may be using olfactory cues to facilitate genetically based mate choice. Image sourced from https://oceanwide-expeditions.com/to-do/wildlife/blue-petrel. Viewed on 18th April 2017.

The Crested Auklet (Aethia cristatella) emits a tangerine-scented odour during the breeding season that is thought to be used as a method of chemical communication (Hagelin et al. 2003). Throughout the courtship period both sexes emit this odour and frequently engage in 'ruff sniff' displays where individuals rub their beaks in the nape feathers of display partners, the region where the tangerine odour is the strongest (Jones & Hunter 1993). The fact that this scent is only produced, and 'ruff sniff' display only occurs in the breeding season, provides strong evidence that birds are using  olfactory cues in the process of sexual selection (Hagelin et al. 2003).

Crested Auklets (Aethia cristatella) engaged in a 'ruff sniff' display where individuals rub their beaks in the nape feathers of display partners, the region where the tangerine odour emitted is the strongest. Photo by Lars Petersson http://www.hbw.com/ibc/species/54074/photos. Viewed on 18th April 2017.

So next time you admire the striking colouration of a bird, or listen to a beautiful melody of birdsong, consider that there is often more to birds than meets the eye or ear. I have shown you throughout the blog so far how more well known and studied visual and accoustic-based cues can often be associated with sexual selection. These alone result in a huge variety of intriguing and incredible morphological and behavioural traits, but with olfactory cues thrown into the mix, yet another layer of complexity is added to the wonderful world of birds!

References

Hagelin, J.C., Jones, I.L. & Rasmussen L.E.L. 2003, "A tangerine-scented social odour in a monogamous seabird", Proceedings of the Royal Society of London. Series B: Biological Sciences, vol. 270, no. 1522, pp. 1323-1329.

Jones, I.L. & Hunter, F.M. 1993, "Mutual sexual selection in a monogamous seabird", Nature, vol. 362, no. 6417, pp. 238-239.

Mardon, J. & Bonadonna, F. 2009, "Atypical homing or self-odour avoidance? Blue Petrels (Halobaena caerulea) are attracted to their mate's odour but avoid their own", Behavioral Ecology and Sociobiology, vol. 63, no. 4, pp. 537-542.

Roper, T.J. 1999. "Olfaction in birds", Advances in the Study of Behavior, vol. 28, pp. 247-247.

Singh, P. 2001, "Chemosensation and genetic individuality", Reproduction, vol. 121, no. 4, pp. 529-539.

Zelano, B. & Edwards, S.V. 2002, "An MHC component to kin recognition and mate choice in birds: predictions, progress, and prospects", The American naturalist, vol. 160 Suppl 6, no. 6, pp. S225. 

Vocal mimicry: a result of sexual selection???

One of the earliest memories I have of developing a love of birds was when I saw and heard a Superb Lyrebird (Menura novaehollandiae) for the first time. Growing up on the South Coast of NSW I was lucky enough to be able to venture into their habitat and witness first hand their incredible antics. Watching a lyrebird perfectly mimic the sound of a Laughing Kookaburra (Dacelo novaeguineae) blew my mind and I have since heard them while camping mimic the sound of campers banging in tent pegs. I have also been fooled and amazed when I heard what I thought was the unmistakable call of a Whistling Kite (Haliastur sphenurus) coming from a mango tree in Kakadu National Park, only to discover it was emanating from a Great Bowerbird (Chlamydera nuchalis). It is not just lyrebirds and bowerbirds that mimic other birds and environmental noises, it is suggested that 15-20% of passerines incorporate heterospecific elements into their songs (Zann & Dunstan 2008).

The male Superb Lyrebird (Menura novaehollandiae) has possibly the greatest song repertoire in the world. His ability to to accurately mimic up to 20 different species of birds along with many other environmental noises is truly amazing https://www.youtube.com/watch?v=VjE0Kdfos4Y. Viewed on 12th April 2017.

So why do birds vocally mimic other bird species? The short answer is that we still don't really know. There have been many theories put forward that have tried to answer this complex question, one of which is that female preference for song complexity has resulted in mimicry to enlarge the male's song repertoire (Zann & Dunstan 2008). Research has since shown that in some species of birds, accuracy of vocal mimicry and size of repertoire in males can predict mating success better than other display traits that have been determined as important for male mating success (Coleman et al. 2007). The fact that mimicry is a learned behaviour requiring the modification of vocal motor patterns (Zollinger & Suthers 2004) has prompted the idea that mimicry accuracy may provide females with information as to the male's past (Nowicki et al. 2002) and present (Garamszegi 2005) condition and serve as an honest indicator of physiological performance (Coleman et al. 2007).

The Great Bowerbird (Chlamydera nuchalis) is also an excellent mimic and has certainly fooled me more than once! It has been suggested that Great Bowerbirds mimic predators to protect their nest, however field evidence does not support this hypothesis. Image sourced from https://www.flickr.com/photos/21342600@N03/5024267447.  Viewed on 13th April 2017.

Researching vocal mimicry in birds has once again highlighted the many complexities embedded within the avian world we do not, and may never, fully understand. It seems to me that researchers are often at risk of trying to prove each other wrong when in fact given the sheer diversity and vastly different characteristics of birds, in some cases there may be as many answers to the same question as there are species of birds.

References


Coleman, S.W., Patricelli, G.L., Coyle, B., Siani, J. & Borgia, G. 2007, "Female preferences drive the evolution of mimetic accuracy in male sexual displays", Biology Letters, vol. 3, no. 5, pp. 463-466.

Garamszegi, L.Z. 2005, "Age-dependent health status and song characteristics in the barn swallow", Behavioral Ecology, vol. 16, no. 3, pp. 580-591.

Nowicki, S., Searcy, W. & Peters, S. 2002, "Brain development, song learning and mate choice in birds: a review and experimental test of the "nutritional stress hypothesis"", Journal of Comparative Physiology A, vol. 188, no. 11, pp. 1003-1014.

Zann, R. & Dunstan, E. 2008, "Mimetic song in superb lyrebirds: species mimicked and mimetic accuracy in different populations and age classes", Animal Behaviour, vol. 76, no. 3, pp. 1043-1054.

Zollinger, S.A. & Suthers, R.A. 2004, "Motor mechanisms of a vocal mimic: implications for birdsong production", Proceedings of the Royal Society of London. Series B: Biological Sciences, vol. 271, no. 1538, pp. 483-491.

The great frigatebird: a puzzling case of inbreeding and sexual selection.

Inbreeding, or the mating of more genetically similar individuals than the average relatedness of individuals in a population, has been shown to reduce fitness through the increase in frequency of  deleterious recessive alleles being expressed in offspring (Cohen & Dearborn 2004). Throughout the animal and plant world, strategies have been developed that decrease the likelihood of inbreeding and the negative effects it can produce (Darwin 1876, Charlesworth & Charlesworth 1987, Pusey & Wolf 1996). However, in certain populations of organisms including birds, it does occur due to limited dispersal ability, random mating processes with respect to relatedness and natal breeding site fidelity (Bohonak 1999, Cohen & Dearborn 2004). But is this the ONLY reason we see inbreeding occurring in bird populations?

The male great frigatebird (Fregata minor) shows off his inflated red gular pouch to attract a female, but is this really what the female is inspecting? Could this be used by the female as an indicator of genetic similarity? Image sourced from http://www.pelagicodyssey.ca/styled-3/page37/. Viewed on 3rd April, 2017.

The great frigatebird (Fregata minor) population of Tern Island in Hawaii has been shown to display high levels of inbreeding, but not due to any of the reasons mentioned above (Cohen & Dearborn 2004). Great frigatebird breeding ecology would make it improbable that inbreeding would occur, as the species does not suffer from any of the constraints that would "force"  genetically similar individuals to breed with each other - females aerially assess the displays of up to several hundred males, males can travel hundreds of kilometers to display to females on other islands and interisland genetic diversity is reasonably high (Dearborn & Ryan 2002, Dearborn et al. 2003). While great frigatebirds do show a degree of natal site fidelity, females have a broad range of males to choose from as the operational sex ratio is male biased at the time the sexes are pairing-up to breed (Dearborn et al. 2001). 

Great frigatebirds (Fregata minor) (foreground), and red-footed boobies (Sula sula) (background) both breed on Tern Island in Hawaii. Photo by P.D. Tillmam https://commons.wikimedia.org/wiki/File:Great_frigatebirds_and_red-footed_boobies_at_Tern_Island.jpg. Viewed on 3rd April, 2017.

Despite these breeding behaviours and opportunities for females to pick genetically dissimilar males, inbreeding is widespread throughout the population (Cohen & Dearborn 2004). This would suggest that females are actively picking genetically similar males to breed with (Cohen & Dearborn 2004). Sexual imprinting, descibed by Irwin & Price (1999) as "the means by which a young bird learns species-specific characteristics that enables it to find a conspecific mate when adult", has been suggested as a possible mechanism for inbreeding in the great frigatebird, but there is still much uncertainty about the resulting fitness consequences and whether they are beneficial or detrimental (Cohen & Dearborn 2004). There would have to be an advantage associated with inbreeding in this case if the postulates of sexual selection apply wouldn't there??? A very interesting but still unanswered question!

References 

Bohonak, A.J. 1999, "Dispersal, gene flow, and population structure", The Quarterly Review of Biology, vol. 74, no. 1, pp. 21-45.

Charlesworth, D. & Charlesworth, B. 1987, "Inbreeding depression and its evolutionary consequences", Annual Review of Ecology and Systematics, vol. 18, no. 1, pp. 237-268.

Cohen, L.B. & Dearborn, D.C. 2004, "Great frigatebirds, Fregata minor, choose mates that are genetically similar", Animal Behaviour, vol. 68, no. 5, pp. 1229-1236.

Darwin, C. 1876, The effects of cross and self fertilisation in the vegetable kingdom. J. Murray.

Dearborn, D.C., Anders, A. D. & Parker, P. G. 2001, "Sexual dimorphism, extrapair fertilizations, and operational sex ratio in great frigatebirds (Fregata minor)", Behavioral Ecology, vol. 12, no. 6, pp. 746-752.

Dearborn, D.C., Anders, A.D., Schreiber, E.A., Adams, R.M.M. & Mueller, U.G. 2003, "Inter‐island movements and population differentiation in a pelagic seabird", Molecular Ecology, vol. 12, no. 10, pp. 2835-2843. 

Dearborn, D. C. & Ryan, M. J. 2002, "A test of the Darwin–Fisher theory for the evolution of male secondary sexual traits in monogamous birds", Journal of Evolutionary Biology, vol. 15, pp. 307–313.

Irwin, D.E. & Price, T. 1999, "Sexual imprinting, learning and speciation", Heredity, vol. 82, no. 4, pp. 347-354.

Pusey, A. & Wolf, M. 1996, "Inbreeding avoidance in animals", Trends in Ecology & Evolution, vol. 11, no. 5, pp. 201-206.