Citreoline Trogon: a bird endemic to western Mexico

Citreoline Trogon
1 February 2025, El Jorullo, Jalisco, Mexico

We saw this Citreoline Trogon after walking across the 470 metre long suspension bridge at El Jorullo a few miles inland from Puerto Vallarta on the Pacific Coast of Mexico. We had to wait for a while because Canopy River park is used for all sorts of outdoor activities and several convoys of all-terrain vehicles were heading in the opposite direction. The suitability for such vehicles makes it, so it is claimed, the longest vehicular suspension bridge in the world. The whole area has been owned and operated since 1940 by an association of local foresters; the vehicles and zip wire etc came later, after 2005. The Sierra Madre mountains provide a backdrop to the protected area of forest while the Cuale River runs way below the bridge.

Jorullo Suspension Bridge

The Citreoline Trogon (Trogon citreolus) is endemic to the woods and forests of western Mexico. They nest by digging into the nests of tree termites. This one was eating berries and at various times of year eat either or both fruit and insects.

From the photograph at high magnification it can be seen that the trogon has two toes visible at the front. Does that make it a zygodactyl like parrots and woodpeckers? Well, no. It does have two toes at the front and two at the back but in trogons digits 3 and 4 face forward while 1 and 2 face back. In zygodactyly, 2 and 3 face forward and 1 and 4 back. Trogons are thus described as heterodactylous.

There were mammalian delights too along the trail through the forest beyond the suspension bridge but they are for later.

Comparative Endocrinology Revisited: Hellbenders, Giant Salamanders and their hormones

Hellbender from the Appalachian Mountains
Brian Gratwicke Creative Commons Attribution 2.0 Generic

In a recent article I mentioned that there is still discussion on why the adrenal glands of different groups and species of vertebrates produce either or both of the two steroid hormones, cortisol and corticosterone. Both are these hormones are glucocorticoids, originally named for their effect on glucose metabolism and both have wide-ranging effects on the body. Both have a little mineralocorticoid action, i.e. acting to retain sodium, the role of the other major adrenal steroid hormone, aldosterone. In different tissues of different animals corticosterone and cortisol have been found to have slight differences in their mineralocorticoid action.

The difference between corticosterone and cortisol is the absence or presence of a hydroxyl moiety at the 17 carbon position of the steroid molecule. Corticosterone does not have it; cortisol does. In some mammals, rats and mice for example, the adrenal cortex does not have the enzyme 17α-hydroxylase* An earlier chemical precursor of cortisol is therefore not produced, leaving corticosterone as the only glucocorticoid produced by the rat adrenal. Since aldosterone has been found in all vertebrates, corticosterone must also be produced since it is a precursor in aldosterone synthesis. In some animals that produce both corticosterone and cortisol, one or the other may predominate. In primates it is cortisol.

The structural difference between corticosterone and cortisol (ringed in red)
Adapted from the classic textbook by Aubrey Gorbman and Howard Bern,
A Textbook of Comparative Endocrinology, New York: John Wiley. 1962

A paper published in 2020 raised an interesting question and demolished the generally accepted view that corticosterone is the major and perhaps the only major glucocorticoid produced by the adrenal cortex of amphibians. Hellbenders (Cryptobranchus alleganiensis) are the American relatives of the Giant Salamanders of East Asia. They too are large, but not so large, up to 70 cm in length, long-lived and fully aquatic. As part of an extensive study of an amphibian in decline in the wild, the concentration of cortisol was found to be five times that of corticosterone in blood taken from a tail vein. The difference was even greater—up to ten times—after the injection of mammalian adrenocorticotrophic hormone (ACTH). The authors suggested that cortisol may predominate, as it does in fish, in these aquatic salamanders since in other vertebrates cortisol has a somewhat greater mineralocorticoid activity than corticosterone thereby preserving salt and water balance. However, that inference, at first sight, does not seem to hold. In work done in Hong Kong by my old fellow postgraduate student Samuel Chan, Tom Sandor (1924-2003) (a doyen of steroid biosynthesis in vertebrates) and Brian Lofts (1929-2015) only corticosterone was found after adrenal tissue from similarly aquatic Chinese giant salamanders (Andrias) was incubated with radiolabelled precursors in the steroidogenic pathway.

The authors of the papers on the Hellbender drew up a table showing previous studies on the occurrence of corticosterone and cortisol in amphibians and emphasised the difficulties of interpreting studies in which blood concentrations were recorded and experiments on adrenal tissue in vitro. They also noted that a number of studies were done before reliable methods had been established for identifying and quantifying corticosterone in the presence of cortisol and vice versa. They made sure that they established the chemical identity of the hormones using mass spectroscopy—something not possible in the early studies with the low but biologically active concentrations found in blood plasma. However, there is another difference that may be significant: the site from which blood was taken. Because the analytical methods did not exist at the time to study hormones in peripheral blood, John Phillips (1933-1987) made his name in the late 1950s by devising techniques to sample blood from the veins draining the adrenal gland or from those that carried a high proportion of adrenal venous effluent. The distinction is important because, as I suggest below, any production of adrenocortical-like hormones from elsewhere in the body would not have been at detectable concentrations.

What could be the explanation of the findings in the Hellbender and indeed in those amphibians in which both corticosterone and cortisol have been found to be present in the blood (albeit with the caveats on methodology outlined above)? I suggest there are two hypotheses which are not mutually exclusive:

1. The adrenal tissue expresses the gene CYP17A1 that produces 17α-hydroxylase during the breeding season but not at other times. The Hellbenders sampled were, as the authors note, caught in late summer ‘prior to nesting because at this time adult male and female hellbenders can be distinguished by the swollen cloaca of males’. There is evidence gathered in the first half of the twentieth century that the adrenal of many amphibians varies in appearance, both macroscopic and microscopic, according to season. In newts and salamanders the adrenals are multi-segmented strands of tissue on the ventral side of the kidneys. In the California Newt (Taricha torosa), as one example, during the two-month breeding season the adrenal is bright orange in colour and expanded compared wit the non-breeding season when the gland is dull, smaller and flatter. In other words, the gland waxes and wanes and it is easy to imagine that the production of 17α-hydroxylase follows a similar pattern. An adrenal with 17α-hydroxylase is also capable of producing androgens that might play a role in reproduction.
2. The adrenal is not the site of cortisol synthesis or secretion. The gonads in a number of vertebrates are known to be capable of synthesis and secretion of adrenocorticosteroids. Of necessity in being able to sythesise androgens and oestrogens they must express CYP17A1. The adrenal, testis and ovary are all of similar embryonic origin and complete separation of steroid synthesis and secretion   is far from complete with overt clumps of cells characteristic of the adrenal cortex being present in the ovary.

A possible clue as to the cellular origins of of the two adrenal steroids is that while in the Hellbender both corticosterone and cortisol concentrations increased in response to ACTH the time course was different and there was no correlation between concentrations of the two hormones in blood at any time point. Thus corticosterone reached a peak at one hour after ACTH; cortisol at three hours. Does this finding suggest a different cellular origin of the two steroids? I suspect that it does with either two cell populations in the adrenal itself (one only seasonally present producing cortisol and probably androgens, the ‘permanent’ cells producing corticosterone) or of the adrenal producing corticosterone and the ovary and testis producing cortisol as well as androgens and oestrogens.

Assuming that the other members of the cryptobranchid family have a similar endocrine system, both of these possibilities are compatible with the finding of cortisol and corticosterone in the blood of Hellbenders but the finding of only corticosterone  being produced in vitro by the adrenal of Chinese giant salamanders, assuming of course the latter were not in the breeding season or breeding condition.

Chinese Giant Salamander (Andrias sp)
On the roof of the now demolished Northcote Science Building
Univewrsity of Hong Kong ca 1966

I would argue that the next step in solving this problem lies in China where farm-bred Giant Salamanders are readily available in the restaurant trade. The question is a simple one: what are the concentrations of corticosterone and cortisol in the blood at different stages of the reproductive cycle? Modern students may prefer the question in molecular biological terms: where are the sites of expression of the gene CYP17A1?

...And surely the Axolotl is just asking to be looked at!

Comparative endocrinology may no longer be fashionable but there are still important areas where new knowledge and a look at unsolved old problems are needed if we are to understand how signalling systems that operate between organs and tissues work. The science of intercellular signalling is now being neglected. 

*I have seen the odd paper showing cortisol as present in mice (at least in a particular strain of lab mouse) but without comment as to the significance of the finding.

The paper on the Hellbender:

Hopkins WA, DuRant SE, Beck ML, Ray WK, Helm RF, Romero LM. 2020. Cortisol is the predominant glucocorticoid in the giant paedomorphic hellbender salamander (Cryptobranchus alleganiensis). General and Comparative Endocrinology 285, 113267 doi: 10.1016/j.ygcen.2019.113267

The paper on the Chinese Giant Salamander:

Chan STH, Sandor T, Lofts B, 1975. A histological, histochemical, and biochemical study of the adrenal tissue of the Chinese giant salamander (Andrias davidianus Blanchard). General and Comparative Endocrinology 25, 509–516 doi: 10.1016/0016-6480(75)90161-6

For the older literature on the adrenal gland of amphibians:

Chester Jones I. 1957. The Adrenal Cortex. Cambridge: Cambridge University Press.

UPDATED 17 JUNE 2025