MECHANISMS AFFECTING REPRODUCTION AND ORNAMENT EXPRESSION IN MALE TETRAONIDAE BIRDS

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1 REVIEWS Bioproduction Environment Life Science OPEN ACCESS MECHANISMS AFFECTING REPRODUCTION AND ORNAMENT EXPRESSION IN MALE TETRAONIDAE BIRDS Saori Yamamoto Laboratory of Animal Reproduction, The United Graduate School of Agricultural Science, Gifu University, 1-1 Yanagido, Gifu , Japan ABSTRACT Most avian species have breeding seasons that are appropriate for their survival. The hypothalamic pituitary testicular axis controls the endocrine system and the onset of breeding. The Tetraonidae (a family of birds in the order Galliformes) live in extreme environments where their breeding season is restricted by ambient factors, particularly day length. In the breeding season, male Tetraonidae birds prominently express combs over their eyes (supraorbital combs), the expression of which is controlled by testosterone, a well-known androgen. Testosterone also regulates immunocompetence and there is a trade-off between the cost for condition and the benefit for reproduction in the expression of sexual traits like the comb. Thus, the comb may be the specific indicator projecting male quality. This article reviews the effects of the endocrine system on reproduction and expression of the comb in male Tetraonidae. Keywords: Comb, Conservation, Lagopus species, Male grouse, Testosterone Introduction The family Tetraonidae in the order Galliformes consists of 8 genera and 20 species of birds (del Hoyo and Collar, 2014). These species, commonly called grouse or ptarmigan depending on whether or not they have white plumage in winter, are distributed throughout the northern hemisphere (Nakamura, 2007). Phylogeny of Tetraonidae birds have been studied by Dimcheff et al. (2002), using mitochondrial 12S and ND2 genes. Some species have evolved to adjust to extreme and unusual environment conditions, such as extremely low ambient temperature, short day length or continuous darkness in winter, and midnight sun in summer. These extreme environmental factors control fat deposition (Grammeltvedt and Steen, 1978), body mass (Lindgard and Stokkan, 1989; Stokkan et al., 1995), metabolic cost (Mortensen and Blix, 1986; Lees et al., 2010), and reproduction (Stokkan et al., 1986; Wilson and Martin, 2010) in these birds. For instance, despite sufficient day length for reproduction to occur, ambient temperatures below zero degrees suppress egg laying owing to the birds being unable to nest in deep snow and judging the environment being inadequate for chicks survival (Stokkan et al., 1986). The Japanese rock ptarmigan (Lagopus muta japonicus), which is the southern-most living subspecies in the world (Figures 1 and 2), inhabits mountain ranges in Japan at an altitude of 2,400 m above sea level. This bird was designated as a Special Natural Treasure of Japan in Studies on the habitat, population census (Haneda et al., 1985; Hotta et al., 2008), seasonality of foraging (Kobayashi and Nakamura, 2011), genetic diversity (Baba et al., 2001), infection status (Hagihara et al., 2004; Ishihara et al., 2006; Murata et al., 2007) and life history (Nakamura, 2006) have been conducted for this species. The breeding season of Japanese rock ptarmigan begins with a fight among males to settle territory, which occur simultaneously with the melting of the snow. Male birds settle into their territories by late April, and monogamous pairs form by May (Nakamura, 2007). Females lay approximately six eggs in June and then incubate them while their mates stand sentry over their territory guarding them (Nakamura, 2006). The eggs hatch on day 21 of incubation, and chicks are reared by the female (Nakamura, 2006). A recent study by Nakamura (2006) revealed the population of the Japanese rock ptarmigan has decreased compared to 1980s. This population decline has been caused by an increase in the number of predators, habitat loss, and climate change. Global warming, specifically, causes the tree line to shift upward subsequently decreasing ptarmigan habitat. Recently, certain Received: May 4, Revised: October 14, Accepted: December 25, Published on line: April 9, 2016 Correspondence to S.Y.: saori_3002_0974@yahoo.co.jp

2 Bioproduction Environment Life Science Please cite this article as: Fig.1. Winter plumage of male Japanese rock ptarmigan at Otari-mura, Tsugaike Kogen, Kitaazumi-gun, Nagano, Japan. (Feb 26, 2014) Fig.2. Summer plumage of Japanese rock ptarmigan at Norikura highland between Matsumoto, Nagano to Takayama, Gifu, Japan; male (left) and female (right). (Jul 20, 2012). mammals, such as the Japanese monkey (Macaca fuscata) and sika deer (Cervus nippon), have invaded the alpine region, and their overabundance has caused the destruction of Alpine vegetation (Nakamura, 2006). To protect these birds from facing probable extinction in the coming decades, serious conservation efforts are currently being undertaken both in situ and ex situ. Continuous in situ efforts include monitoring populations and studying ptarmigan ecology. A

3 Bioproduction Environment Life Science recent analysis revealed the time series variation of chick survival (Kobayashi and Nakamura, 2013), and a new approach using cages to protect chicks from predation and bad weather during the rainy season has improved their survival. Furthermore, institutions like zoos have been keeping Svalbard ptarmigan (L. m. hyperboreus), another subspecies of rock ptarmigan, and conducting ex situ efforts such as collecting biological data in order to establish captive breeding techniques for this species (Takahashi et al., 2012). The Ex Situ Conservation Project Team was established by the Japanese Association of Zoos and Aquariums in 2014 (Ministry of the Environment, 2014), and they have since initiated a Japanese rock ptarmigan captive breeding program as well. Understanding the underlying endocrinology of these birds will help in promoting reproduction, and hormonal monitoring is one step toward understanding the endocrine activity of ptarmigans. Several studies of Tetraonidae have elucidated the endocrinological parameters, which relate to reproductive physiology with their special survival factors, both in wild and in captivity (Table 1). Some of the endocrinological studies of various Tetraonidae species since 1980 are shown in Table 1. This review considers studies on male Tetraonidae species reproduction, endocrinological factors, and the expression of male secondary sexual traits, especially the supraorbital comb. Reproduction in male Tetraonidae birds Breeding in male birds is controlled by the hypothalamic pituitary testicular hormone axis. Gonadotropin releasing hormone (GnRH), secreted by the hypothalamus, acts on the anterior lobe of the pituitary gland, causing secretion of follicle stimulating hormone (FSH) and luteinizing hormone (LH) (Asa, 2010). FSH promotes Sertoli cell differentiation and is related to spermatogenesis, and LH stimulates differentiation of Leydigs interstitial cells (Brown et al., 1975) and promotes androgen (e.g., testosterone) production. For avian species, including some Tetraonidae, there have been many studies that link photoperiod and gonadal activity, particularly gonadal development that occurs when the photoperiod is longer than a certain level (e.g. Rowan, 1925; Follett et al., 1974; Dawson et al., 2001; Gupta, 2014). The relationship between day length and gonadal hormone is also reported for Tetraonidae birds. According to a study on captive male willow ptarmigan (L. lagopus lagopus) by Stokkan and Sharp (1980), stimulation of the pituitary testicular hormone axis depends entirely on long day length, and long periods of light induce increases in plasma LH levels and subsequent increases in testosterone levels in willow ptarmigan. At some point, however, long days induce testicular regression associated with photorefractoriness. Immediately after onset of the photorefractory period, plasma testosterone concentrations started to decline prior to plasma LH concentrations (Stokkan and Sharp, 1980). This may be because LH levels during the photorefractory period are suppressed by a negative feedback mechanism caused by testicular steroid hormones (Sharp and Moss, 1977). In some birds, hormonal changes in the blood during the breeding season have been documented (Table 1). In captive capercaillie (Tetrao urogallus), blood LH and FSH concentrations increased in April and May, with mating observed in May (Hissa et al., 1983). Hannon and Wingfield (1990) monitored plasma LH and testosterone concentrations of free-living willow ptarmigan. In both cases, the concentrations changed throughout the breeding season, being higher earlier when birds were settling territories and significantly declining during the laying period (Hannon and Wingfield, 1990), indicating that hormonal dynamism is strongly linked to reproductive activity. Testis activity and secondary sexual traits, including the comb, are strongly controlled by the pituitary testicular axis (Ottinger and Bakst, 1995). In Svalbard ptarmigan, Stokkan et al. (1986) showed Table 1: Endocrinological studies in various Tetraonidae species Species Study location Endocrinological studies; studies (captive-wild status) Reference Svalbard ptarmigan (Lagopus Svalbard, Norway Testes weight, spermatogenesis, LH level, comb Stokkan et al., 1986 lagopus hyperboreus) height (wild population) Willow ptarmigan (L. l. Tromso, Norway Seasonal changes in testosterone and LH levels, Stokkan and Sharp, 1980 lagopus) comb size, plumage (captive population) Red grouse (L. l. scoticus) Northeast Scotland Testosterone manipulation on comb size, Mougeot et al., 2004 condition, parasite burden (wild population) Red grouse (L. l. scoticus) Northeast Scotland, England Testosterone implant on comb size, comb Martínez-Padilla et al., 2014 coloration (wild population) Black grouse (Tetrao tetrix) Central regions in Sweden/Finland Testosterone level, comb size, sexual selection (wild population in leks) Rintamäki et al., 2000 Capercaillie (T. urogallus) Northern Finland Seasonal variation in the levels of LH, FSH, Hissa et al., 1983 prolactin, corticosterone, thyroxine (captive population)

4 Bioproduction Environment Life Science Please cite this article as: anatomically that plasma LH concentration varied with testicular mass and the presence of sperm. In quail (Coturnix japonica), the median eminence of the mediobasal hypothalamus (MBH) releases GnRH, which induces development of the gonad (Yamamura et al., 2006; Dickens et al., 2014 and literature cited therein). This occurs when long daylight stimulates expression of type 2 iodothyronine deiodinase, which catalyzes the conversion of thyroxin to triiodothyronine in the MBH, leading to the secretion of GnRH (Yoshimura et al., 2003). These details have not been revealed in Tetraonidae birds, but such detailed studies of the mechanisms controlling endocrinological regulation have been revealed in quail. Combs, a prominent secondary sexual trait in males Generally, combs of male birds become larger during the breeding season. Tetraonidae species have brightly colored supraorbital combs, and these combs are usually more conspicuous in males than in females (Owens and Short, 1995). Comb growth of a male willow ptarmigan is directly dependent on testicular hormones and indirectly related to day length (Stokkan, 1979a) with comb size increasing with long day length for uncastrated but not castrated males (Stokkan et al., 1979b). Likewise, red grouse (L.l. scoticus) with testosterone implanted in the chest can be induced to increase comb size (Mougeot et al., 2004). Furthermore, a study on red jungle fowl (Gallus gallus) showed that the onset of male male competition is also controlled by gonadal activity (Ligon et al., 1990). In male red grouse, the relationship between testosterone and comb growth was altered by intrasexual competition levels, becoming weaker as intrasexual competition increased (Martinez- Padilla et al., 2014). In addition, young (or weaker) individuals behave subordinately, and they have suppressed testosterone levels (Tudge, 2012), and it may for avoiding fighting. The comb plays an important role in sexual selection as a reliable indicator for females of male quality. This can be explained with the handicap principle of Zahavi (1975), the parasite hypothesis of Hamilton and Zuk (1982), and the immunocompetence handicap hypothesis of Folstad and Karter (1992). Zahavi (1975) proposed the idea of a handicap in sexual selection, i.e., developing and maintaining exaggerated secondary sexual characters may impose a cost (handicap) on individuals, but it may also be an indicator for a prospective mate to discern something about the individuals quality. Hamilton and Zuk (1982) expanded on this by stating that the indicator of quality (exaggerated sexual trait) relates to condition in terms of parasite resistance and these traits may be heritable. Folstad and Karter (1992) took this idea a step further, relating parasite resistance, immunocompetence, testosterone levels, and the expression of sexual traits to female preferences. It is known that while testosterone regulates the expression of sexual traits, which in turn affects an individuals fitness, it simultaneously suppresses immune function (Folstad and Karter, 1992). Reduction in immunocompetence has been demonstrated in red jungle fowl, wherein testosterone-treated males exhibited a negative correlation between plasma testosterone concentration and lymphocyte count (Zuk et al., 1995). Folstad and Karter (1992) postulated that the tradeoff between the cost (parasite-induced pathogenicity) and benefit (higher fitness due to a more developed sexual trait) of testosterone levels is plastic and set by the feedback of these effects. Thus, superior-quality males should be able to afford the cost of parasites and have a reproductive advantage over lower quality males that cannot bear the cost to the immune system, thus, producing less testosterone and not fully expressing the sexual trait. The result is that female birds prefer males with exaggerated sexual traits because such males possess genes that resist parasite infections. Thus, the comb of male birds may be an indicator to females of both the males reproductive ability and immunocompetence. Several studies support a relationship between comb and sexual selection in Tetraonidae birds. In the breeding season, male black grouse (T. tetrix) gather in leks (i.e., sites where many males congregate for social courtship displays and fight for access to females), Rintamäki et al. (2000) demonstrated a positive and significant relationship between male comb size and copulatory success in not all males but in males achieved copulations; these facts suggesting that combs are a cue for females to assess male quality. Additionally, testosterone-treated red grouse have been shown to result in individuals with large combs (Mougeot et al., 2004; Mougeot et al., 2006; Martinez-Padilla et al., 2014), high competitive ability, and breeding success (Mougeot et al., 2006), all potential boosts to reproduction. Nevertheless, they also had high parasitic loads (Mougeot et al., 2004; Mougeot et al., 2006) and decreased immunocompetence and physical condition (Mougeot et al., 2004; Mougeot et al., 2006; Martinez-Padilla et al., 2014). Peters (2007) proposed a mechanism for how testosterone, carotenoids, and lipoproteins may interplay in the trade-off among immunity, sexual signals, and oxidative stress. In this scenario, testosterone mediates immunosuppression by inducing oxidative stress in immune cells while concurrently up-regulating circulating levels of carotenoids via increased production of carotenoidtransporting lipoproteins. Carotenoids enhance immune functions by buffering testosterone-mediated immunosuppression with their antioxidant properties and directly stimulating immune cells. They also improve sexual signaling via enhancement of comb ornamentation (Peters, 2007). Studies of birds such as the American kestrel (Falco sparverius), house finch (Carpodacus mexicanus), and North American passerines indicate that carotenoids do play a role as a key factor in enhancing immunity and sexual signaling (Olson and Owens, 1998). Likewise, a study

5 Bioproduction Environment Life Science on wild red grouse indicated that the allocation of carotenoids for comb coloration or self-maintenance depended on physiological constraints (Martínez-Padilla et al., 2010). These examples suggest that the comb is a reliable indicator of male condition. Hormonal monitoring problems and countermeasures The comb is an index of testis development (with a highly developed comb relating to a more developed testis) and is regulated by the pituitary testicular axis. This axis is also the main regulator of the reproductive strategy of Tetraonidae birds. However, ambient factors also exert influence on reproductive hormones; of these, day length is most influential. Monitoring hormonal dynamics is the most effective way to understand reproductive physiology. Because blood transports hormones from endocrine organs to target tissues, circulating blood levels provide immediate information on endocrine status. In earlier hormonal studies of Tetraonidae, blood was collected from living or dead birds, but repetitious blood collection of wild birds is a more difficult task. Practicability of hormone studies is often limited by the frequency and volume of blood samples that can be obtained (Goymann, 2005), limiting the effectiveness of this strategy. A review by Schewarzenberger and Brown (2013) discusses the benefits of non-invasive monitoring of hormones from feces for mammals and suggests that this method is preferable for captive management of these animals and for wildlife research. Empirical evidence provides support for the non-invasive collection method. In Japanese quail, concomitant increase in plasma concentration and fecal content of testosterone was confirmed (Ishii et al., 1994). Feces, therefore, may be considered as an alternative source of testosterone. With this testosterone source come various benefits, including the ability to conduct repetitive collections from individuals, lower invasiveness of the technique, and the ability to use it in long-term studies. Feces contain several hormonal metabolites. Even in closely related species, speciesspecific differences of steroid metabolism may exist and it is necessary for accurate results to validate the assay methods carefully (Schwarzenberger, 2007). Adopting a viable method of monitoring sexual hormones via feces in Tetraonidae birds will facilitate data collection on changes in endocrine status, and the knowledge gained from this, in combination with other factors such as behavior and molting characteristics, will result in improved captive management strategies. We have been studying the gonadal activity of captive female Svalbard rock ptarmigans by analyzing their feces and have previously reported on the concentrations and dynamics of testosterone, progesterone and estradiol-17in both rectal and cecal feces (Yamamoto et al., 2014; 2015). Currently, we are focusing on sex steroid hormone concentrations in wild Japanese rock ptarmigans as well. Some priorities for continued research include, deciphering the mechanisms driving hormonal fluctuations in response to external light between wild and captive ptarmigan subspecies. Investigating the multiple interactions of the immune system and comb traits with testosterone levels and parasitic infections in terms of the immunocompetence handicap hypothesis proposed by Folstad and Karter (1992) is another area of curiosity. Several researchers have reported parasitic loads of wild Japanese rock ptarmigans (Hagihara et al., 2004; Ishihara et al., 2006; Murata et al., 2007). Next, the relationship of these loads needs to be measured in concordance with reproductive fitness, immunocompetence, and testosterone levels. We may be able to estimate the influence on fitness and reproduction offered by combs because their expression is regulated by the testosterone and parasite infection trade-off. Particularly in ex situ breeding, variations in comb size and color status may be a vital indicator in understanding individual breeding ability and/or health (Yamamoto et al., 2016). With the advent of the non-invasive fecal hormonal assays making these types of studies more practical, increased understanding of the effects of testosterone on reproduction of Japanese rock ptarmigans should progress and aid field and laboratory ornithologists in better understanding the biology of these birds. Acknowledgement I acknowledge the advice and critical comments of Associate Professors Sachi Sri Kantha and Satoshi Kusuda in preparing this manuscript. References Asa CS (2010) Reproductive physiology. In: Wild mammals in captivity Principles and techniques for Zoo Management, 2nd edition. (Kleman DG, Thompson KV, Baer CK, eds.). pp University of Chicago Press, Chicago. Baba Y, Fujimaki Y, Yoshii R and Koike H (2001) Genetic variability in the mitochondrial control region of the Japanese rock ptarmigan Lagopus mutus japonicus. Jpn. J. Ornithol., 50: Brown NL, Bayle JD, Scanes CG and Follet BK (1975) Chicken gonadotropins: their effects on the testes of immature and hypophysectomized Japanese quail. Cell Tissue Res., 156: Dawson A, King VM, Bentley GE, Ball GF (2001) Photoperiodic control of seasonality in birds. J. Biol. Rhythm, 16: del Hoyo J, Collar NJ (2014) Order GALLIFORMES. In: HBW and Bird Life International Illustrated Checklist of the Birds of the World Volume 1 Non-passerines. pp Lynx Edicions, Barcelona. Dickens MJ, de Bournonville C, Balthazart J and Cornil CA (2014)

6 Bioproduction Environment Life Science Please cite this article as: Relationship between rapid changes in local aromatase activity and estradiol concentrations in male and female quail brain. Horm. Behav., 65: Dimcheff DE, Drovetski SV and Mindell DP (2002) Phylogeny of Tetraoninae and other galliform birds using mitochondrial 12S and ND2 genes. Mol. Phylogenet. Evol., 24: Follett BK, Mattocks PW and Farner DS (1974) Circadian function in the photoperiodic induction of gonadotropin secretion in the white-crowned sparrow, Zonotrichia leucophyrys gambelii. Proc. Natl. Acad. Sci. USA, 71: Folstad I and Karter AJ (1992) Parasites, bright males and the immunocompetence handicap. Am. Nat., 139: Goymann W (2005) Noninvasive monitoring of hormones in birds droppings: Physiological validation, sampling, extraction, sex differences, and the influence of diet on hormone metabolite levels. Ann. New York Acad. Sci., 1046: Grammeltvedt R and Steen JB (1978) Fat deposition in Spitzbergen ptarmigan (Lagopus mutus hyperboreus). Arctic, 31: Gupta NJ (2014) Role of day length in the regulation of annual testicular cycle in male black-headed munia. Biol. Rhythm Res., 45: Hagihara M, Yamaguchi T, Kitahara M, Hirai K and Murata K (2004) Leucocytozoon lovati infections in wild rock ptarmigan (Lagopus mutus) in Japan. J. Wildlife Dis., 40: Hamilton WD and Zuk M (1982) Heritable true fitness and bright birds: a role for parasites? Science, 218: Haneda K, Nakamura H, Koiwai A, Iizawa T and Tajima K (1985) Distribution and density of the rock ptarmigan Lagopus mutus in the southern Japan alps. Tori, 34: (in Japanese with English summary). Hannon SJ and Wingfield JC (1990) Endocrine correlates of territoriality, breeding stage, and body molt in free-living willow ptarmigan of both sexes. Can. J. Zool., 68: Hissa R, Sasrela S, Balthazart J and Etches RJ (1983) Annual variation in the concentrations of circulating hormones in capercaillie (Tetrao urogallus). Gen. Comp. Endocr., 51: Hotta M, Miyano N and Ozeki M (2008) Breeding status of ptarmigan Lagopus mutus in Mt. Jigatake to Mt. Iwagoyazawadake. Bull. Nagano Environ. Conserv. Res. Inst., 4: (in Japanese with English summary). Ishihara S, Shibashi T, Sato Y, Murata K and Nogami S (2006) Two Eimeria species isolated from wile Japanese rock ptarmigans (Lagopus mutus japonicus) in Japan. J. Vet. Med. Sci., 68: Ishii S, Wada M, Wakabayashi S, Sakai H, Kubodera Y, Yamaguchi N and Kikuchi M (1994) Endocrinological studies for artificial breeding of the Japanese ibis, Nipponia nippon, an endangered avian species in Asia. J. Biosciences, 19: Kobayashi A and Nakamura H (2011) Seasonal change of food items of the Japanese rock ptarmigan Lagopus mutus japonicas. Jpn. J. Ornithol., 60: Kobayashi A and Nakamura H (2013) Chick and juvenile survival of Japanese rock ptarmigan Lagopus muta japonica. Wildlife Biol., 19: Lees J, Nudds R, Stokkan KA, Folkow L and Codd J (2010) Reduced metabolic cost of locomotion in Svalbard rock ptarmigan (Lagopus muta hyperborea) during winter. PLoS ONE 11: e Lindgård K and Stokakan KA (1989) Daylength control of food intake and body weight in Svalbard ptarmigan Lagopus mutus hyperboreus. Ornis Scand., 20: Ligon JD Thornhill R Zuk M and Johnson K (1990) Male-male competition, ornamentation and the role of testosterone in sexual selection in red jungle fowl. Anim. Behav., 40: Martínez-Padilla J, Mougeot F, Webster LMI and Pérez-Rodríguez L (2010) Testing the interactive effects of testosterone and parasites on carotenoid-bases ornamentation in a wild bird. J. Evol. Biol., 23: Martínez-Padilla J, Perez-Rodriguez L, Mougeot F, Ludwig S and Redpath SM (2014) Intra-sexual competition alters the relationship between testosterone and ornament expression in a wild territorial bird. Horm. Behav., 65: Ministry of the Environment (2014) Document 3: About Japanese Association of Zoos and Aquariums. ( press/18936.html) (in Japanese) Mortensen A and Blix AS (1986) Seasonal changes in resting metabolic rate and mass-specific conductance in Svalbard ptarmigan, Norwegian rock ptarmigan and Norwegian willow ptarmigan. Ornis Scand., 17: Mougeot F, Irvine JR, Seivwright L, Redpath SM and Piertney S (2004) Testosterone, immunocompetence, and honest sexual signaling in male red grouse. Behav. Ecol., 15: Mougeot F, Redpath SM and Piertney SB (2006) Elevated spring testosterone increases parasite intensity in male red grouse. Behav. Ecol., 17: Murata K, Tamada A, Ichikawa Y, Hagihara M, Sato Y, Nakamura H, Nakamura M, Sakanakura T and Asakawa M (2007) Geographical distribution and seasonality of the prevalence of Leucocytozoon lovati in Japanese rock ptarmigans (Lagopus mutus japonicus) found in the Alpine regions of Japan. J. Vet. Med. Sci., 69: Nakamura H (2006) Life history of ptarmigan. In: What Japanese Rock Ptermigan Tells Us. pp YAMA-KEI Publishers Co., Ltd., Tokyo (in Japanese). Nakamura H (2007) Japanese rock ptarmigan Lagopus mutus

7 Bioproduction Environment Life Science japonicas. Jpn. J. Ornithol., 56: (in Japanese with English abstract). Olson VA and Owens IPF (1998) Costly sexual signals: are carotenoids rare, risky or required? Trends Ecol. Evol., 13: Ottinger MA and Bakst MR (1995) Endocrinology of the avian reproductive system. J. Avian Med. Surg., 9: Owens IPF and Short RV (1995) Hormonal basis of sexual dimorphism in birds: implications for new theories of sexual selection. Trends Ecol. Evol., 10: Peters A (2007) Testosterone and carotenoids: an integrated view of trade-offs between immunity and signalling. BioEssays 29: Rintamäki PT, Hoglund J, Karvonen E, Alatalo V, Bjorklund N, Lundberg A, Ratti O and Vouti J (2000) Combs and sexual selection in black grouse (Tetrao tetrix). Behav. Ecol., 11: Rowan W (1925) Relation of light to bird migration and developmental changes. Nature, 115: Schwarzenberger F (2007) The many uses of non-invasive faecal steroid monitoring in zoo and wildlife species. Int. Zoo. Year Bk., 41: Schewarzenberger F and Brown JL (2013) Hormone monitoring: an important tool for the breeding management of wildlife species. Wien. Tierarztl. Monat., 100: Sharp PJ, Moss R (1977) The effects of castration on concentrations of luteinizing hormone in the plasma of photorefractory red grouse (Lagopus lagopus scoticus). Gen. Comp. Endocr., 32: Stokkan KA (1979a) The effect of permanent short days and castration on plumage and comb growth in male willow ptarmigan (Lagopus lagopus lagopus). Auk, 96: Stokkan KA (1979b) Testosterone and daylength-dependent development of comb size and breeding plumage of male willow ptarmigan (Lagopus lagopus lagopus). Auk, 96: Stokkan KA and Sharp PJ (1980) Seasonal changes in the concentrations of plasma lutenizing hormone and testosterone in willow ptarmigan (Lagopus lagopus lagopus) with observations on the effects of permanent short days. Gen. Comp. Endocr., 40: Stokkan KA, Sharp PJ and Unander S (1986) The annual breeding cycle of the high-arctic Svalbard ptarmigan (Lagopus mutus hyperboreus). Gen. Comp. Endocr., 61: Stokkan KA, Lindgård K and Reierth E (1995) Photoperiodic and ambient temperature control of the annual body mass cycle in Svalbard ptarmigan. J. Comp. Physiol. B, 165: Takahashi Y, Ishida J, Maeda M (2012) Artificial hatching and brooding of Svalbard rock Ptarmigan. Animals and Zoos, 64 : (in Japanese). Tudge C (2012) Chapter 7 Breeding biology. In: The Secret Life of Birds: Who they are and what they do. translated by Kurosawa R pp CMC Press. Tokyo (in Japanese). Wilson S amd Martin K (2010) Variable reproductive effort for two ptarmigan species in response to spring weather in northern alpine ecosystem. J. Avian Biol., 41: Yamamoto S, Kusuda S, Hori H, Takahashi Y, Horiguchi M, Murai H and Doi O (2014) Changes in gonadal activity associated with rearing condition, egg lying and molting in captive Svalbard rock ptarmigan (Lagopus muta hyperboreus). 26th International Ornithological Congress. Tokyo, Japan. Poster presentation Abstract. P Yamamoto S, Kusuda S, Takahashi Y, Hori H, Horiguchi M, Ishihara Y and Doi O (2015) Differences of hormone concentrations and dynamics in rectal and cecal feces of captive Svalbard rock ptarmigan (Lagopus muta hyperboreus). Jpn. J. Zoo Wildl. Med., 20: (in Japanese with English summary). Yamamoto S, Kusuda S, Horiguchi M. Ishihara Y and Doi O (2016) Seasonal changes in supraorbital comb characteristics and fecal testosterone levels in captive male Svalbard rok ptarmigans (Lagopus muta hyperboreus). Jpn.J.Zoo Wildl.Med (submitted). Yamamura T, Yasuo S, Hirunagi K, Ebihara S and Yoshimura T (2006) T 3 implantation mimics photoperiodically reduced encasement of nerve terminals by glial processes in the median eminence of Japanese quail. Cell Tissue Res., 324: Yoshimura T, Yasuo S, Watanabe M, Iigo M, Yamamura T, Hirunagi K and Ebihara S (2003) Light-induced hormone conversion of T 4 to T 3 regulates photoperiodic response of gonads in birds. Nature, 426: Zahavi A (1975) Mate selection a selection for a handicap. J. Theor. Biol., 53: Zuk M, Johnsen TS and Maclarty T (1995) Endocrine-immune interactions, ornaments and mate choice in red jungle fowl. Proc. Roy. Soc. Lond. B., 260: