Chapter 2 – Proximate and Ultimate Causes of Bird Song Biology 484 – Ethology Chapter 2 – Proximate and Ultimate Causes of Bird Song

White-crowned Sparrow (Zonotrichia leucophrys) Chapter 2 Studies of bird song have relied heavily on male white-crowned sparrows White-crowned Sparrow (Zonotrichia leucophrys) forage on the ground or in low vegetation mainly eat seeds, other plant parts and insects. The White-crowned Sparrow is known for its “alertness mechanism” which allows it to remain awake for as long as two weeks (typically during migration) This “alertness mechanism” effect has been studied for possible human applications. C:\Figures\Chapter02\high-res\Alcock8e-ChOpener-02.jpg

Peter Marler University of California – Davis Primary author of the studies about the dialects of song sparrows described. Note: Sometimes people wonder about the use of the terms “dialect” and “accent”. In the case of these bird songs, the term “dialect” is a better one because there appear to be the equivalent of distinctly different “vocabulary” and “grammar” in the bird calls. An accent difference would show only pronunciation variations.

2.1 Song dialects in white-crowned sparrows from Marin, Berkeley, and Sunset Beach, California In each of the three locations shown, we see the bird song sung by multiple members of the local population display the SAME “vocabulary” and “grammar” whereas there are significant differences between members of different regions. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-01-0.jpg

(Taeniopygia guttata) 2.2 Hearing is critically important for song learning in the zebra finch Zebra Finch (Taeniopygia guttata) In this species, it was often wondered how its song developed? Was the song innate or was it learned in some fashion? In this species, it was determined in an elaborate experiement that learning is required and occurs when a son hears his father’s song and models his own after it as it matures. In the sonogram of the experiment show, the son that was deafened prior to learning the song, shows an atypical song, and demonstrates the need for learning in this species. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-02-0.jpg

2.3 Song learning hypothesis based on laboratory experiments with white-crowned sparrows The hypothesis suggests that young W-C Sparrows have only a critical period where they can acquire exposure to their species specific song in order to reproduce it successfully. The critical period was experimentally shown to be a brief window only between days 10 – 50 (after hatching from the egg). Exposure to the song ONLY before OR after this time period resulted in failure of the normal adult song. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-03-0.jpg

2.6 Sonograms of contact calls of galahs and pink cockatoos reared under different conditions The Galah’s and Pink Cockatoos appear similar, and can cross foster each other. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-06-0.jpg The top graph shows the normal Galah song in birds raised by Galah. The middle graph shows the normal Cockatoo song in birds raised by Cockatoos. The bottom graph shows the disrupted song that develops in a Galah raised by Cockatoos.

2.7 Changes in the song system of young male and female zebra finches The neuroendocrinology of the brain development is sexually dimorphic in zebra finches roughly after day 15. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-07-0.jpg

Between 15 – 40 days after hatching, the number of neurons in the Higher Vocal Center (HVC) declines in the female, but increases in the male. This shows how the brain, which at birth was bipotential in regards to the HVC, became sexually dimorphic, which leads to the differences in behavior. These developmental changes to the brain are due to both genetic and environmental differences: The genetic difference leads to hormonal differences (environmental) which lead to differences in activity levels of brain cells. In these finches, the gonads are not the only nor the most important source for chemical signals (predicted due to suspected role of Testosterone) It is actually ESTROGEN that is the key signal for differentiation of the brain… which is produced in certain brain cells of the male. Research by Gurney & Konishi in 1980 has shown this in females… estrogen implants in young fledgling females leads to the development of male song in zebra finches.

Aromatase Hypothesis for Mammalian Brain Development In mammals, the in-utero exposure to massive levels of estrogen via the mother is blocked by a compound called alpha-fetoprotein. In mammals (like birds) the role of key aspects of brain differentiation is a result of estrogen. However, mammals use the aromatase enzyme to convert testostrone into estrogen in specific undifferentiated brain cells to foster this development.

2.8 The timing of gene activity in different components of the avian song control system in males In the vast majority of species of birds, song production is much more highly developed in males than in females. The neural pathway shown represents the typical pattern shown for an adult male. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-08-0.jpg This image shows gene activity (as measured via protein production) in the given brain region. In the graph, the first term is the brain region, the second term (after the colon) is the protein produced.

Brain regions associated with song learning include: HVC – (higher vocal center) – a nucleus in the brain of the songbirds needed for both the learning and the production of bird song Area X – a homolog to mammalian basal ganglia (used in motor control and in procedural learning of frequent behaviors) lMAN – (lateral (lower case “L”) magnocellular nucleus of the anterior neostriatum) - part of the pathway for circuitry NCM – (caudomedial neostriatum) (see paper by Bolhuis and Eda-Fujiwara) - a region of the brain involved with auditory perception RA – (robust nucleus of the arcopallium) – roughly homologous to the amygdala of mammals and it functions in a similar way as a site of emotions and emotional response pathways nXIIts - hypoglossal nucleus (nXIIts) (dark blue areas in the previous diagram of the spinal cord) that project to vocal muscles

Bird song learning pathway… the intensity of color indicates the activity (as a measure of protein production). Nucleus HVC feeds information into two pathways that ultimately lead to the neurons in the tracheosyringeal half of the hypoglossal nucleus (nXIIts). HVC projects: to nucleus RA directly indirectly via Area X Indirectly to the dorsolateral anterior thalamic nucleus (DLM) d. and indirectly to the LMAN in a manner that shares similarities with the mammalian pathway

2.9 Gene expression in a component of the zebra finch song system In this example of a ZEBRA FINCH brain, we see Area X expressing for the gene/protein called ZENK. This was active in the NCM at a different time frame for the same species. Question to contemplate: How do you explain the different gene activities at different times in the same brain region? Of what value is this difference? C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-09-0.jpg High level of activity in Area X in the ZENK gene…. This leased to production of the ZENK protein Note in previous graph how the brain levels for zenk will rise then fall to indicate the period where learning is possible. Human similarities?

2.12 Differences in the size of one nucleus of the song system C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-12-0.jpg Male is on the left, the female on the right.

2.13 Single cells and song learning in the swamp sparrow Different components of songs are learned by single cells and song learning… response of action potentials to certain song components. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-13-0.jpg The most interesting idea from this image is how it shows that different individual neurons of the same nucleus (in this case, the HVC) can be used to different behavioral responses. Thought Question: Imagine how this specificity could guide different behavioral responses to different sounds. Applications?

2.15 The song of a vocal non-learner, the eastern phoebe There are vocal non-learner species of birds as well. In this case, the species has ONLY an innate song. In this data, 12 & 13 were experimentally deafened and yet produce same song. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-15-0.jpg

2.16 The song control systems of parrots, hummingbirds, and oscine songbirds (Part 1) Song learning is actually considered fairly specialized and appears to have arisen three separate times when viewed through our current understanding of phylogeny. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-16-1.jpg

The song control systems of parrots, hummingbirds, and oscine songbirds (Part 2) C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-16-2.jpg Even though three separate origins phylogenically….. Note the incredible similarity of the brain development for song learning in these groups.

Does bird song repel territorial intruders? In this species….. YES! The researchers compared the number of intruders to a territory that had lost the presence of a W-T Sparrow to that of a territory that had also lost a W-T Sparrow , but the researchers played back the song of a typical W-T Sparrow within the boundary of that territory. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-17-0.jpg

White-crowned sparrow females are attracted to the songs of male white-crowned sparrows Higher trill rate by the female is associated greater interest in the singer. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-18-0.jpg Greater distance kept by the female to the singer is associated lowered interest .

Why have dialects within a species? Songs match habitats Why have dialects within a species? This is only seen in birds that LEARN songs. Innate songs do not show the propensity towards being dialectic. The prevailing theory as to why dialects arise are associated with the ability to fine-tune a song for specialized needs. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-19-0.jpg In these data, the forest area is an area denser with vegetation whereas the woodland is considerably more open. It is thought that the higher pitch sounds shown as part of a woodland member’s song cannot penetrate as well in the forest environment.

2.20 Dialect selection by male white-crowned sparrows C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-20-2.jpg

2.23 Evidence that male Cassin’s finches direct their songs at females In this interesting species, the male uses its song when he finds a female that was present in his territory leaves. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-23-0.jpg

2.24 Nutritional stress early in life has large effects This shows how environmental stressors can greatly impact health and well being. Birds in the experimental group received only 70% of the caloric content the ad.lib. fed control group ate for a two week period early in life during active brain development. The term “ad.lib.” Is an abbreviation for “ad libitum” which is Latin for "at one's pleasure“. Therefore when we use the term in science, we are saying the animal eats as much food as it wants. C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-24-0.jpg

2.25 Mean number of precopulatory displays given by female song sparrows (Part 1) C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-25-1.jpg

2.25 Mean number of precopulatory displays given by female song sparrows (Part 2) C:\Figures\Chapter02\high-res\Alcock8e-Fig-02-25-2.jpg