In most species of seasonally breeding songbirds studied to date, the brain areas that control singing (i.e. the song control system, SCS) are larger during the breeding season than at other times of the year. In the family of titmice and chickadees (Paridae), one species, the blue tit (Cyanistes caeruleus), shows the typical pattern of seasonal changes, while another species, the black-capped chickadee (Poecile atricapillus), shows, at best, very reduced seasonal changes in the SCS. To test whether this pattern holds up in the two Parid lineages to which these two species belong, and to rule out that the differences in seasonal patterns observed were due to differences in geography or laboratory, we compared the seasonal patterns in two song system nuclei volumes (HVC and Area X) in willow tits (Poecile montanus), closely related to black-capped chickadees, and in great tits (Parus major), more closely related to blue tits, from the same area around Oulu, Finland. Both species had larger gonads in spring than during the rest of the year. Great tit males had a larger HVC in spring than at other times of the year, but their Area X did not change in size. Willow tits showed no seasonal change in HVC or Area X size, despite having much larger gonads in spring than the great tits. Our findings suggest that the song system of willow tits and their relatives may be involved in learning and producing nonsong social vocalizations. Since these vocalizations are used year-round, there may be a year-round demand on the song system. The great tit and blue tit HVC may change seasonally because the demand is only placed on the song system during the breeding season, since they only produce learned vocalizations during this time. We suggest that changes were not observed in Area X because its main role is in song learning, and there is evidence that great tits do not learn new songs after their first year of life. Further study is required to determine whether our hypothesis about the role of the song system in the learned, nonsong vocalizations of the willow tit and chickadee is correct, and to test our hypothesis about the role of Area X in the great tit song system.

1.
Avey MT, Quince AF, Sturdy CB (2008): Seasonal and diurnal patterns of black-capped chickadee (Poecile atricapillus) vocal production. Behav Process 77:149-155.
[PubMed]
2.
Avey MT, Rodriguez A, Sturdy CB (2011): Seasonal variation of vocal behaviour in a temperate songbird: assessing the effects of laboratory housing on wild-caught, seasonally breeding birds. Behav Process 88:177-183.
[PubMed]
3.
Baker MC, Howard TM, Sweet PW (2000): Microgeographic variation and sharing of the gargle vocalization and its component syllables in black-capped chickadee (Aves, Paridae, Poecile atricapillus) populations. Ethology 106:819-838.
4.
Ball GF, Auger CJ, Bernard DJ, Charlier TD, Sartor JJ, Riters LV, Balthazart J (2004): Seasonal plasticity in the song control system: multiple brain sites of steroid hormone action and the importance of variation in song behavior. Ann NY Acad Sci 1016:586-610.
[PubMed]
5.
Ball GF, Balthazart J (2010): Seasonal and hormonal modulation of neurotransmitter systems in the song control circuit. J Chem Neuroanat 39:82-95.
[PubMed]
6.
Bijnens L, Dhondt AA (1984): Vocalizations in a Belgian blue tit, Parus c. caeruleus, population. De Giervalk 74:243-269.
7.
Brenowitz EA, Lent K (2002): Act locally and think globally: intracerebral testosterone implants induce seasonal-like growth of adult avian song control circuits. Proc Natl Acad Sci 99:12421-12426.
[PubMed]
8.
Brenowitz EA, Lent K, Rubel EW (2007): Auditory feedback and song production do not regulate seasonal growth of song control circuits in adult white-crowned sparrows. J Neurosci 27:6810-6814.
[PubMed]
9.
Calisi RM, Bentley GE (2009): Lab and field experiments: are they the same animal? Horm Behav 56:1-10.
[PubMed]
10.
Caro SP, Lambrechts MA, Balthazart JB (2005): Early seasonal development of brain song control nuclei in male blue tits. Neurosci Lett 386:139-144.
[PubMed]
11.
De Groof G, Verhoye M, Van Meir V, Balthazart J, Van Der Linden A (2008): Seasonal rewiring of the songbird brain: an in vivo MRI study. Eur J Neurosci 28:2475-2485.
[PubMed]
12.
Ekman J (1989): Ecology of non-breeding social systems of Parus. Wilson Bull 101:263-288.
13.
Ficken MS, Ficken RW, Apel KM (1985): Dialects in a call associated with pair interactions in the black-capped chickadee. Auk 102:145-151.
14.
Ficken MS, Ficken RW, Witkin SR (1978): Vocal repertoire of the black-capped chickadee. Auk 95:34-48.
15.
Ficken MS, Weise CM (1984): A complex call of the black-capped chickadee (Parus atricapillus). I. Microgeographic variation. Auk 101:349-360.
16.
Ficken MS, Weise CM, Reinartz JA (1987): A complex vocalization of the black-capped chickadee. II. Repertoires, dominance and dialects. Condor 89:500-509.
17.
Franco P, Slabbekoorn H (2009): Repertoire size and composition in great tits: a flexibility test using playbacks. Anim Behav 77:261-269.
18.
Haftorn S (1993): Ontogeny of the vocal repertoire in the willow tit Parus montanus. Ornis Scand 24:267-289.
19.
Hughes M, Nowicki S, Lohr B (1998): Call learning in black-capped chickadees (Parus atricapillus): the role of experience in the development of ‘chick-a-dee' calls. Ethology 104:232-249.
20.
Johansson US, Ekman J, Bowie RC, Halvarsson P, Ohlson JI, Price TD, Ericson PG (2013): A complete multilocus species phylogeny of the tits and chickadees (Aves: Paridae). Mol Phylogenet Evol 69:852-860.
[PubMed]
21.
Koivula K, Orell M (1988): Social rank and winter survival in the willow tit Parus montanus. Ornis Fennica 65:114-120.
22.
Kroodsma DE, Albano DJ, Houlihan PW, Wells JA (1995): Song development by black-capped chickadees (Parus atricapillus) and Carolina chickadees (P. carolinensis). Auk 112:29-43.
23.
LaDage LD, Roth TC II, Fox RA, Pravosudov VV (2009): Effects of captivity and memory-based experiences on the hippocampus in mountain chickadees. Behav Neurosci 123:284.
[PubMed]
24.
Laverghetta AV, Shimizu T (1999). Visual discrimination in the pigeon (Columba livia): effects of selective lesions of the nucleus rotundus. Neuroreport 10:981-985.
[PubMed]
25.
Leitner S, Voigt C, Gahr M (2001): Seasonal changes in the song pattern of the non-domesticated island canary (Serinus canaria) a field study. Behaviour 138:885-904.
26.
Leitner S, Voigt C, Garcia-Segura LM, Van't Hof T, Gahr M (2001): Seasonal activation and inactivation of song motor memories in wild canaries is not reflected in neuroanatomical changes of forebrain song areas. Horm Behav 40:160-168.
[PubMed]
27.
MacDougall-Shackleton SA, Hernandez AM, Valyear KF, Clark AP (2003): Photostimulation induces rapid growth of song-control brain regions in male and female chickadees (Poecile atricapilla). Neurosci Lett 340:165-168.
[PubMed]
28.
Madison FN, Rouse ML, Balthazart J, Ball GF (2015): Reversing song behavior phenotype: testosterone driven induction of singing and measures of song quality in adult male and female canaries (Serinus canaria). Gen Comp Endocrinol 215:61-75.
[PubMed]
29.
Mammen DL, Nowicki S (1981): Individual differences and within-flock convergence in chickadee calls. Behav Ecol Sociobiol 9:179-186.
30.
Marler P (1970): A comparative approach to vocal learning: song development in white-crowned sparrows. J Comp Physiol Psychol 71(2p2):1.
31.
Martens J, Nazarenko AA (1993): Microevolution of eastern palaearctic grey tits as indicated by their vocalizations [Parus (Poecile) Paridae, Aves]. I. Parus montanus: contributions to the fauna of the far east, No. 2. J Zool System Evol Res 31:127-143.
32.
McGregor PK, Avery MI (1986): The unsung songs of great tits (Parus major): learning neighbours' songs for discrimination. Behav Ecol Sociobiol 18:311-316.
33.
McGregor PK, Krebs JR (1982): Song types in a population of great tits (Parus major): their distribution, abundance and acquisition by individuals. Behaviour 79:126-152.
34.
Meitzen J, Moore IT, Lent K, Brenowitz EA, Perkel DJ (2007): Steroid hormones act transsynaptically within the forebrain to regulate neuronal phenotype and song stereotypy. J Neurosci 27:12045-12057.
[PubMed]
35.
Meitzen J, Thompson CK (2008): Seasonal-like growth and regression of the avian song control system: neural and behavioral plasticity in adult male Gambel's white-crowned sparrows. Gen Comp Endocrinol 157:259-265.
[PubMed]
36.
Meitzen J, Weaver AL, Brenowitz EA, Perkel DJ (2009): Plastic and stable electrophysiological properties of adult avian forebrain song-control neurons across changing breeding conditions. J Neurosci 29:6558-6567.
[PubMed]
37.
Miyasato LE, Baker MC (1999): Black-capped chickadee call dialects along a continuous habitat corridor. Anim Behav 57:1311-1318.
[PubMed]
38.
Moore IT, Wingfield JC, Brenowitz EA (2004): Plasticity of the avian song control system in response to localized environmental cues in an equatorial songbird. J Neurosci 24:10182-10185.
[PubMed]
39.
Nottebohm F (1981): A brain for all seasons: cyclical anatomical changes in song control nuclei of the canary brain. Science 214:1368-1370.
[PubMed]
40.
Nottebohm F, Nottebohm ME, Crane L (1986): Developmental and seasonal changes in canary song and their relation to changes in the anatomy of song-control nuclei. Behav Neural Biol 46:445-471.
[PubMed]
41.
Nowicki S (1989): Vocal plasticity in captive black-capped chickadees: the acoustic basis and rate of call convergence. Anim Behav 37:64-73.
42.
Orell M, Ojanen M (1980): Overlap between breeding and moulting in the great tit Parus major and the willow tit P. montanus in northern Finland. Ornis Scand 11:43-49.
43.
Orell M, Ojanen M (1983): Timing and length of the breeding season of the great tit (Parus major) and the willow tit (P. montanus) near Oulu, northern Finland. Ardea 71:183-198.
44.
Phillmore LS, Hoshooley JS, Hahn TP, MacDougall-Shackleton SA (2005): A test of absolute photorefractoriness and photo-induced neural plasticity of song-control regions in black-capped chickadees (Poecile atricapillus). Can J Zool 83:747-753.
45.
Phillmore LS, Hoshooley JS, Sherry DF, MacDougall-Shackleton SA (2006): Annual cycle of the black-capped chickadee: seasonality of singing rates and vocal-control brain regions. J Neurobiol 66:1002-1010.
[PubMed]
46.
Phillmore LS, MacGillivray HL, Wilson KR, Martin S (2015): Effects of sex and seasonality on the song control system and Foxp2 protein expression in black-capped chickadees (Poecile atricapillus). Dev Neurobiol 75:203-216.
[PubMed]
47.
Rivera-Gutierrez HF, Pinxten R, Eens M (2011): Difficulties when assessing birdsong learning programmes under field conditions: a re-evaluation of song repertoire flexibility in the great tit. PLoS One 6:e16003.
[PubMed]
48.
Rost R (1990): Hormones and behaviour. A joint examination of studies on seasonal variation in song production and plasma levels of testosterone in the great tit Parus major. J Ornithol 131:403-412.
49.
Sartor JJ, Ball GF (2005): Social suppression of song is associated with a reduction in volume of a song-control nucleus in European starlings (Sturnus vulgaris). Behav Neurosci 119:233.
[PubMed]
50.
Sartor JJ, Balthazart J, Ball GF (2005): Coordinated and dissociated effects of testosterone on singing behavior and song control nuclei in canaries (Serinus canaria). Horm Behav 47:467-476.
[PubMed]
51.
Schwabl H, Dowling J, Baldassarre DT, Gahr M, Lindsay WR, Webster MS (2015): Variation in song system anatomy and androgen levels does not correspond to song characteristics in a tropical songbird. Anim Behav 104:39-50.
52.
Shackleton SA, Ratcliffe L, Weary DM (1992): Relative frequency parameters and song recognition in black-capped chickadees. Condor 94:782-785.
53.
Silverin B (1984): Annual gonadotropin and testosterone cycles in free-living male birds. J Exp Zool 232:581-587.
[PubMed]
54.
Silverin B, Deviche P (1991): Biochemical characterization and seasonal changes in the concentration of testosterone-metabolizing enzymes in the European great tit (Parus major) brain. Gen Comp Endocrinol 81:146-159.
[PubMed]
55.
Silverin B, Viebke PA, Westin J (1986): Seasonal changes in plasma levels of LH and gonadal steroids in free-living willow tits Parus montanus. Ornis Scand 230-236.
56.
Simpson HB, Vicario DS (1990): Brain pathways for learned and unlearned vocalizations differ in zebra finches. J Neurosci 10:1541-1556.
[PubMed]
57.
Small TW, Brenowitz EA, Wojtenek W, Moore IT (2015): Testosterone mediates seasonal growth of the song control nuclei in a tropical bird. Brain Behav Evol 86:110-121.
[PubMed]
58.
Smith GT, Brenowitz EA, Beecher MD, Wingfield JC (1997): Seasonal changes in testosterone, neural attributes of song control nuclei, and song structure in wild songbirds. J Neurosci 17:6001-6010.
[PubMed]
59.
Smith GT, Brenowitz EA, Wingfield JC, Baptista LF (1995): Seasonal changes in song nuclei and song behavior in Gambel's white-crowned sparrows. J Neurobiol 28:114-125.
[PubMed]
60.
Smulders TV (2002): Natural breeding conditions and artificial increases in testosterone have opposite effects on the brains of adult male songbirds: a meta-analysis. Horm Behav 41:156-169.
[PubMed]
61.
Smulders TV, Casto JM, Nolan V, Ketterson ED, DeVoogd TJ (2000): Effects of captivity and testosterone on the volumes of four brain regions in the dark-eyed junco (Junco hyemalis). J Neurobiol 43:244-253.
[PubMed]
62.
Smulders TV, Lisi MD, Tricomi E, Otter KA, Chruszcz B, Ratcliffe LM, DeVoogd TJ (2006): Failure to detect seasonal changes in the song system nuclei of the black-capped chickadee (Poecile atricapillus). J Neurobiol 66:991-1001.
[PubMed]
63.
Svensson L (1992): Identification Guide to European Passerines. British Trust for Ornithology.
64.
Tarr BA, Rabinowitz JS, Imtiaz MA, DeVoogd TJ (2009): Captivity reduces hippocampal volume but not survival of new cells in a food-storing bird. Dev Neurobiol 69:972-981.
[PubMed]
65.
Thompson CK, Brenowitz EA (2005): Seasonal change in neuron size and spacing but not neuronal recruitment in a basal ganglia nucleus in the avian song control system. J Comp Neurol 481:276-283.
[PubMed]
66.
Tramontin AD, Brenowitz EA (2000): Seasonal plasticity in the adult brain. Trends Neurosci 23:251-258.
[PubMed]
67.
Tramontin AD, Hartman VN, Brenowitz EA (2000): Breeding conditions induce rapid and sequential growth in adult avian song control circuits: a model of seasonal plasticity in the brain. J Neurosci 20:854-861.
[PubMed]
68.
Van Duyse E, Pinxten R, Eens M (2003): Seasonal fluctuations in plasma testosterone levels and diurnal song activity in free-living male great tits. Gen Comp Endocrinol 134:1-9.
[PubMed]
69.
Vatka E, Orell M, Rytkönen S (2011): Warming climate advances breeding and improves synchrony of food demand and food availability in a boreal passerine. Glob Change Biol 17:3002-3009.
70.
Vatka E, Rytkönen S, Orell M (2014): Does the temporal mismatch hypothesis match in boreal populations? Oecologia 176:595-605.
[PubMed]
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