The broad pattern of the endocrine system is the same throughout the verte- brates. However, with the exception of reproductive endocrinology, which has been studied in ostriches and emus, and thyroid endocrinology, which has been studied in ostriches, the ratite endocrine system has received little attention. There is little reason to think that ratites differ in any significant way in this respect from other birds. The following brief description therefore represents a broad avian perspective, but refers to specific information on ostriches or other ratites where this exists. Harvey and Etches (1997) provide a more detailed description of avian endocrinology.
Endocrine control of metabolism
As with most other aspects of endocrinology, little is known relating specifically to ostriches: this description is based almost entirely on work done on the domes- tic fowl. A wide variety of hormones are involved in the control of carbohydrate and lipid metabolism. The adipose tissue of birds only has a limited capacity for
de novo fatty acid synthesis, and most of the fatty acids that accumulate there are
derived directly from the diet or are synthesized in the liver. Metabolism of fatty acids in the liver is controlled by insulin, glucagon, prolactin, growth hormone, thyroid hormones and corticosteroids. In mammals, insulin is a potent stimulator of hepatic lipogenesis, but birds appear to be much less responsive. On the other hand, glucagon is a potent inhibitor of lipogenesis in birds. Glucagon may be a much more significant partner in the insulin/glucagon relationship in birds than it is in mammals. Growth hormone inhibits lipogenesis and corticosteroids pro- mote lipogenesis.
Homeostasis of carbohydrate metabolism is maintained by insulin and glucagon. Although birds are relatively insensitive to insulin, it has metabolic effects similar to those in mammals, promoting uptake of glucose from the circu- lation. Glucagon has the reverse role and stimulates glycogen breakdown from tis- sues to increase blood glucose. There are several other related polypeptide hormones which are important in avian metabolism. Pancreatic polypeptide, pro- duced in the pancreas, is antilypolitic and suppresses glucose-induced insulin release. Similarly, polypeptide YY, which is mainly produced in the lower gut, also suppresses glucose-induced insulin release. A third member of the family, neu- ropeptide Y, is found mainly in the brain and may also regulate insulin secretion. It is involved in modifying behaviour to regulate food intake. Growth hormone is important in regulating carbohydrate metabolism in favour of growth. Corticosteroids and adrenaline have the opposite effect: they stimulate the mobi- lization of energy reserves so that an animal is better prepared to respond to stress.
A recently discovered hormone, leptin, is also involved in metabolism in mammals (O’Rahilly, 1998). Leptin is produced by adipocytes in adipose tissue. The more adipose tissue there is, the higher the levels of leptin, thereby
providing a measure of fatness. Its role is to reduce appetite and so the fatter an animal is, the more its appetite is suppressed. Several laboratories have tried to clone the gene for leptin in birds, including emus, but as yet none has produced a convincing product. It remains possible that leptin does not occur in birds.
All of these metabolic effects act in harmony as a result of complex interre- lated control mechanisms. Thyroid hormones have a direct effect on metabolic rate and increase oxygen consumption. The thyroid hormone active in increasing metabolic rate is tri-iodothyronine (T3) which is produced by de-iodination of
thyroxine, the main secretory product of the thyroid glands, and this occurs mainly in the liver. The amount of T3in the circulation depends on the amount
of thyroxine released from the thyroid glands, the rate of conversion of thyroxine to T3, and the rate of breakdown of T3. The release of thyroxine from the pitu-
itary glands is comparatively straightforward, being determined by the amount of the pituitary peptide hormone, thyrotrophin-releasing hormone (TSH). However, de-iodination to T3and the breakdown of T3is affected by corticos-
terone, adrenocorticotrophic hormone (ACTH), growth hormone and prolactin, all of which have their own independent effects on metabolism.
Hormones and osmoregulation
The antidiuretic hormone of birds is arginine vasotocin (AVT) (Skadhauge, 1981) which has been isolated from the ostrich neurohypophysis (Saayman et al., 1986). Gray et al. (1988) developed an accurate radio-immunoassay for AVT and for angiotensin II (ANG II) and followed the plasma concentration of both hor- mones for 5 days of dehydration. Water deprivation elevated the average plasma AVT from 10.2 to 32.3 pg ml–1 on average, and ANG II from 44.3 to 143.1
pg ml–1. These AVT data established the relationship between plasma osmolality
and AVT concentrations, and indicated a sensitivity of 0.54 pg ml–1mOsm–1with
a threshold for release of 271 mOsm. Plasma concentrations of both AVT and ANG II are similar to the concentrations found in other birds. The ostrich did not show a greater sensitivity for AVT release, whereas the osmotic threshold was relatively low. In a subsequent study Gray and Brown (1995) exposed ostriches on a low and a high salt intake to a hyperosmotic intravenous salt load. This resulted in increased plasma concentrations of AVT and permitted calculation of the relationship between plasma osmolality and plasma AVT concentrations. The osmotic sensitivity for AVT release was 0.25 and 0.21 pg ml–1mOsm–1in the
low- and high-salt birds, respectively. Although lower than previously encoun- tered in association with dehydration, these values are similar to those found in other avian species, confirming that enhanced sensitivity for AVT release is not a part of an ostrich’s adaptation to osmotic stress.
The major part of plasma osmolality is due to, and therefore proportional to, the concentrations of sodium and chlorine (Table 3.2 and Fig. 3.1). Normal val- ues in the ostrich of these and other plasma or serum chemistry parameters have been published by van Heerden et al. (1985); Levy et al. (1989); Palomeque et al.
(1991) and Angel (1996). The sodium balance is expected to be influenced by aldosterone produced by the adrenals; the plasma concentration of this hormone was augmented after 2 days of dehydration (Levy et al., 1990), and it was higher in non-laying than in laying ostriches (Levy et al., 1996). Average values of plasma and electrolyte concentrations from normally fed and watered ostriches (i.e. not exposed to osmotic stress) are summarized in Table 3.3.
The hypothalamus and pituitary
Central control of the endocrine system resides within the hypothalamus, a region of the brain posterior to the optic chiasma (where the optic nerves cross). The hypothalamus is the focus for a wide variety of external environmental infor- mation (e.g. day length), stressors, behavioural cues and internal information (e.g. temperature, osmolality and nutritional status). In response to these cues, neurosecretory neurones within the hypothalamus synthesize a variety of releas- ing hormones (specific small peptide hormones). In mammals, these pass down nerve fibres directly to the anterior pituitary or the posterior pituitary gland, but in birds the situation is slightly different.
The posterior pituitary is connected to the hypothalamus, as in mammals, and it releases neurohormones such as mesotocin, vasotocin, oxytocin and vaso- pressin. These hormones have been identified in ostriches (Rouillé et al., 1986); they affect the contractility of smooth muscle and have roles in osmoregulation.
The anterior pituitary of birds is not directly connected to the hypothalamus. Instead of passing directly to the anterior pituitary as in mammals, the releasing hormones are secreted from the ends of the neurosecretory neurones, at the median eminence (the base of the hypothalamus), and pass via a blood capillary
Table 3.3. Average values for plasma osmolality and selected electrolyte
concentrations.
Osmolality Sodium Chlorine Potassium
Study (mOsm) (mM l–1) (mM l–1) (mM l–1)
Skadhauge et al. (1984a) 300 143 106 3.5
van Heerden et al. (1985) – 151 104 3.5
Gray et al. (1988) 293 148 99 4.3
Levy et al. (1989) 286 148 100 3.3
Gray and Brown (1995) 303 149 – 4.4
portal system to the anterior pituitary gland. Within the anterior pituitary gland, each of these releasing hormones stimulates specific cells to synthesize and secrete much larger amounts of specific large peptide hormones which then pass into the general circulation. These ‘trophic’ hormones act in one of two ways. They may act directly on their target tissue(s), e.g. growth hormone stimulating the bones to grow; or they may stimulate a target endocrine gland to produce its particular hormone products, e.g. the thyroid gland to produce thyroid hormones, which are in turn released into the circulation and have their effects on their tar- get tissues. In most cases hormone levels are in part controlled by negative feed- back mechanisms, where one or more of the products of an endocrine gland inhibits release of its trophic hormone, e.g. thyroid hormones inhibit release of TSH from the pituitary.
Adrenal
The avian adrenal consists of the cortex and the medulla, which have different origins and functions. In response to a perceived stress, neurosecretory neurones within the hypothalamus synthesize and secrete the peptide corticotrophin- releasing hormone (CRH). In the pituitary, CRH stimulates cells to synthesize and secrete larger amounts of another peptide hormone, ACTH, and this passes in the circulation to the adrenals. ACTH stimulates cells within the adrenal cor- tex to synthesize corticosteroids. The major corticosteroid in birds, and presum- ably ostriches, is corticosterone. The corticosteroids are important in mobilization of energy reserves and in immune responses. Another product of the adrenal cortex is the steroid aldosterone which is important in osmoregulation.
Within the medulla of the adrenal glands are cells which, unlike the cortical cells, are not controlled by a pituitary trophic hormone. Instead, they are inner- vated directly. In response to a perceived stress, they secrete the catecholamine hormone, adrenaline which, like corticosterone, is important in preparing an ani- mal for ‘flight or fight’.
Reproductive endocrine system
The hypothalamic releasing hormone responsible for the control of reproduction is gonadotrophin-releasing hormone (GnRH), a decapeptide consisting of 10 amino-acid residues. In mammals there is only one GnRH; in birds there are two, designated GnRH-I and GnRH-II. Avian GnRH-I is identical to mammalian GnRH except that glutamine is substituted for arginine at position 8 (and so is designated as [Gln8]–GnRH). Avian GnRH-II has three substitutions and is des-
ignated as [His5, Trp7, Tyr8]–GnRH. Both avian GnRH-I and GnRH-II have been
found in ostriches (Powell et al., 1987). GnRH-I cell bodies are located in the sep- tal and pre-optic regions of the hypothalamus, and project to the median emi- nence, whereas GnRH-II is more widely distributed. Only GnRH-I is secreted from the median eminence and is thought to play the major endocrine role in
reproduction. GnRH-I secretion is stimulated by the catecholamines adrenaline and noradrenaline, and is inhibited by opioid peptides.
The release rate of GnRH-I presumably increases at the beginning of the breeding season, although this has not been measured directly. In response, the pituitary synthesizes and secretes larger amounts of the two gonadotrophic pep- tide hormones, luteinizing hormone (LH) and follicle-stimulating hormone (FSH). The complete amino-acid sequences for these two hormones in ostriches have been determined (Koide et al., 1996). Both LH and FSH consist of two sub- units, a common
a
subunit and a hormone-specific ß subunit. Thea
subunit comprises 96 amino-acid residues and has 70–80% sequence identity with thea
subunit of most vertebrates. The ostrich FSH ß subunit consists of 106 amino- acid residues and shows 70–74% sequence identity with mammalian FSH ß sub- unit. The ostrich LH ß subunit consists of 128 amino-acid residues and shows 76–78% sequence identity with other avian LH ß subunits. Purified ostrich FSH is effective in a mammalian bioassay system, confirming its similarity to the mam- malian hormone (Yu et al., 1996).Annual changes in circulating LH concentrations have been measured in ostriches (Degen et al., 1994). In both males and females, LH reaches a peak which coincided with the beginning of egg-laying. However, the amplitude of the seasonal cycle is small compared with that of other birds. Similarly, in emus LH shows a subdued annual cycle (Malecki et al., 1997). LH and FSH together stim- ulate growth and maturation of the gonads, the testes of the male and the left ovary of the female. FSH specifically stimulates maturation of the follicles in the ovary and the Sertoli cells in the testes. Feedback inhibition of FSH in females is mediated by inhibin, another peptide consisting of alpha and beta subunits, pro- duced by the granulosa of the ovarian follicles. Inhibin may also have a direct role within the ovary.
LH stimulates the interstitial cells of the ovary and the Leydig cells of the testes to synthesize the gonadal steroid hormones, of which the most important is oestradiol in females and testosterone in males. These have a variety of effects, including sexual differentiation, development of secondary sexual characters, behaviour, metabolism, gamete production, moult and feedback inhibition of LH secretion. In addition, oestradiol stimulates the liver to synthesize vitellogenin, which passes in the blood to the ovary where it is taken up by ovarian follicles to form the yolk. The largest ovarian follicle, when nearing maturation, begins to secrete another steroid hormone, progesterone, which has a positive feedback effect on the pituitary causing it to secrete a surge of LH and resulting in ovula- tion. Levels of both oestradiol and testosterone have been measured in ostriches (Degen et al., 1994). As with LH, peak levels coincide with egg laying, but the seasonal amplitude is small compared with other seasonally breeding birds.
Prolactin
Prolactin is a pituitary peptide hormone with a wide range of functions amongst vertebrates. In birds it induces broodiness and other parental behaviours, gonadal
regression and moult. In pigeons it stimulates crop sac development, and the secretion of crop milk on which the young are fed. In mammals, release of pro- lactin from the pituitary occurs autonomously in the absence of hypothalamic control. Unlike most other hormones, whose secretion is stimulated by hormones from the hypothalamus, release of prolactin is inhibited by the hormone dopamine. By contrast, in birds synthesis and secretion of prolactin from the anterior pituitary is stimulated by a hypothalamic hormone, vasoactive intestinal polypeptide (VIP – a 28 amino-acid-residue peptide). Avian VIP differs from mammalian VIP by just one residue ([Glu16]–VIP).
In most birds studied, there are marked seasonal changes in circulating con- centrations of prolactin. Typically, prolactin levels increase during late spring and this is in response to increasing day length. Peak levels occur in late spring or summer, often coinciding with the end of the breeding season. This is associated with two of the functions of prolactin, namely inducing gonadal regression and incubation. Seasonal changes in prolactin have not been measured in ostriches, but they have been measured in emus (Malecki et al., 1997). The emu is unusual in that it breeds during winter. Prolactin levels in non-breeding males increased from mid-winter until mid-spring and highest levels coincided with a rapid decrease in testosterone levels, marking the end of the breeding season. This may reflect the anti-gonadal role of prolactin. In many birds, breeding behaviour has an effect on prolactin which is superimposed on the seasonal cycle (Sharp et al., 1997). The presence of a nest and eggs further stimulates prolactin secretion, pos- sibly as a direct tactile response. In breeding male emus (as in ostriches, it is the males which incubate the eggs), prolactin levels in incubating birds were higher than in non-incubating birds at the same time (Malecki et al., 1997). Testosterone levels in these incubating birds were much lower than in non-incubating birds, i.e. testosterone levels decreased in incubating birds in advance of the seasonal decrease in non-incubating birds. Again, this probably reflects the anti-gonadal role of prolactin. There have been a few measurements of prolactin in incubating ostriches, but levels in one incubating male were higher than in non-incubating birds (P.J. Sharp, personal communication, 1997).
Growth hormone
Growth hormone is related to prolactin and has a range of effects which result in somatic growth, maintenance of metabolic homeostasis and maintenance of the immune system. It may also have a role in the control of appetite. Its effects are diverse and include alteration of lipid, nitrogen and carbohydrate metabolism, activation of thyroid hormones and cellular differentiation. Growth hormone stimulates synthesis of insulin-like growth factor (IGF–1) which mediates many of the functions of growth hormone.
Growth hormone is synthesized and secreted by the anterior pituitary, but control of the rate of secretion is complex and not fully understood. Release is stimulated and inhibited by a variety of hypothalamic factors. Release may be stimulated by growth hormone-releasing hormone (GHRH), as it is in mammals,
and inhibited by somatostatin. However, the major stimulus to release in birds appears to be thyrotrophin-releasing hormone (TRH). In adult birds, TRH is more important in stimulating the release of growth hormone than of thyroid- stimulating hormone.
Growth rates amongst young ostriches vary considerably more than between young of other avian species. To investigate whether this could be related to growth hormone, blood samples were taken from 23 5-month-old ostriches whose body mass varied from 11 to 52 kg (Dawson et al., 1996). Plasma growth hormone concentrations ranged from 0.7 to 45.6 µg l–1, but there was no correlation
between growth hormone and body mass. However, this does not preclude an effect of growth hormone. Release of growth hormone from the pituitary occurs as a series of pulses rather than a steady release, and so concentrations in blood will vary with time, which could account for the variation between individuals. A detailed time-series analysis would probably be necessary to establish any associ- ation. However, it was clear from the data that slow growth in some birds was not simply due to an absence of growth hormone: the distribution of high and low growth hormone values was similar amongst small and large birds.
Pineal
The pineal gland produces the hormone melatonin but only during darkness; cir- culating levels are high at night and low during the day. Consequently, the daily pattern of melatonin changes seasonally as day length changes. In mammals, this photoperiodic signal is important in timing seasonal events such as breeding. In birds, it is not used to time seasonal events, but is important as a circadian clock to time daily activities. Whether melatonin is present in ostriches has yet to be investigated.
Thyroid
The avian thyroid comprises two dark red ovoid lobes located low in the neck, internal to the jugular vein and external to the carotid (at its junction with the subclavian artery). It is composed of roughly spherical follicles, each consisting of a colloid-containing lumen surrounded by a single layer of epithelial cells. These follicles contain thyroglobulin, a large molecular-weight protein. The major hor- mone secreted by the thyroid is thyroxine (tetra-iodothyronine), which is an iod- inated derivative of the amino acid tyrosine with each molecule of thyroxine containing four iodine atoms. The thyroid gland extracts and accumulates iodide ions from the blood which are used to iodinate tyrosine residues within thy- roglobulin, which is inactive but releases thyroxine when it undergoes proteoly- sis.
In mammals, the activity of the thyroid gland is controlled by TRH, which is a tripeptide (Glu–His–Pro) synthesized in the hypothalamus. TRH stimulates the pituitary to synthesize and release TSH. This mammalian mechanism is also true
for embryonic birds, but in adult birds the pituitary appears to function more autonomously. TRH does not stimulate release of TSH but appears to be more