Do glucocorticoids or carotenoids mediate plumage coloration in parrots? An experiment in Platycercus elegans

https://doi.org/10.1016/j.ygcen.2019.04.014Get rights and content

Highlights

  • We experimentally studied relationships between diet, stress physiology and coloration in a parrot.

  • Stress-induced CORT predicted change in pigment- and structural-based coloration after molting.

  • CORT did not differ between diet treatments, but stress induced CORT declined during the experiment.

  • Heterophil/lymphocyte ratio differed between diet treatments.

  • Our results suggest no effect of carotenoid intake on coloration in parrots.

Abstract

Conspicuous coloration can indicate phenotypic quality, and may reflect exposure or vulnerability to stress, or access to essential nutrients such as pigments. Although the production of pigmented colours is well understood, much less is known about how structural colours are affected by physiological state. In this study, we tested whether glucocorticoids (corticosterone) predicted expression of plumage coloration in an Australian parrot, the crimson rosella (Platycercus elegans). Parrots provide an interesting and unique test, as they possess conspicuous coloration produced by distinctive pigments known as psittacofulvins, in addition to structural coloration. We have previously documented that coloration in P. elegans is condition-dependent and responds to dietary manipulation. Here, n = 21 P. elegans underwent a dietary manipulation (including food restriction or carotenoid supplementation) during which they moulted, and the change in reflectance was measured for three structural and three pigmentary plumage patches. Stress-induced corticosterone (10 min after handling) measured at the start of the experiment predicted change in coloration in two pigmentary patches (crown and front). We also found that change in stress-induced corticosterone during the experiment was associated with the change in coloration of the crown and two structural patches (cheek and epaulette). Baseline corticosterone (<3 min after handling) was not associated with any measure of coloration. We found no effects of dietary manipulation on baseline or stress-induced corticosterone, but carotenoid supplementation was associated with an increase in a measure of chronic stress (heterophil/lymphocyte ratio), and the corticosterone response to handling decreased over the course of the study. Our results suggest that corticosterone may be linked to colour expression more broadly than previously recognised, including psittacofulvin and structural coloration in parrots, and they confirm the independence of plumage pigmentation in parrots from carotenoid accumulation. Moreover, our study provides new insight into the stress responses of Psittaciformes, one of the most highly threatened avian orders.

Introduction

Conspicuous, condition-dependent signals such as elaborate coloration can reflect various aspects of phenotypic quality (Hill, 2006, Hill, 2006, Hill and Hill, 2002). For example, colour traits may convey information about the condition or physiological state of the bearer, access to essential nutrients such as pigments and antioxidants (e.g. carotenoids), or reflect exposure or vulnerability to stress (Lendvai et al., 2013, McGraw and Ardia, 2003, McGraw et al., 2002). Many mechanisms are involved in the production of animal coloration, but the two main types are pigments (such as carotenoids and melanins) and variation in integument structure (Mcgraw, 2006). Both carotenoid pigments and structural coloration (though the latter has been studied less) have been widely implicated in condition-dependence signalling (e.g. Dale et al., 2001, Hamilton and Zuk, 1982, Hill, 2006, Hill, 2006), but the role of physiological response to stress is less clear.

Biologically meaningful stressors may come in many forms, such as nutritional deficits, immune challenges, oxidative, and behavioural challenges, and most of these have been linked to signal expression in animals (e.g. Mougeot et al., 2010, Romero and Wingfield, 2015, Roulin et al., 2011, Roulin et al., 2008). One of the primary means of assessing stress is by quantifying circulating levels of the glucocorticoids which mediate the endocrine response to environmental stress in vertebrates (e.g. Sapolsky et al., 2000). Corticosterone (CORT) is the primary glucocorticoid in birds and may negatively affect an individual’s condition during chronic stress and can induce immunosuppression (Buchanan, 2000, Cote et al., 2010a, Cote et al., 2010b,b; Moore and Miller, 1984, Sapolsky et al., 2000, Tokarz, 1987).

CORT may be associated with the production or deposition of the pigments such as melanins or carotenoids (e.g. Almasi et al., 2010, Loiseau et al., 2008, Martínez-Padilla et al., 2013, Roulin et al., 2008), which form the basis of many well-studied colour signals (Hill, 2006, Hill, 2006, Hill, 2011). CORT also inhibits protein deposition (Romero et al., 2005, Sapolsky et al., 2000), and in birds higher CORT has been linked to reduced feather structural quality (DesRochers et al., 2009, Grunst et al., 2015, Jenni-Eiermann et al., 2014, Lattin et al., 2011). As such, there is a plausible link between CORT and feather barb nanostructure, and thus structural coloration in birds (Kennedy et al., 2013). CORT is also known to be directly affected by dietary restriction (e.g. Lendvai et al., 2014). Therefore, CORT is a plausible candidate in mediating links between diet, stress and at least pigment- or structural-based coloration, and thus the information content of many condition-dependent colour signals. However, the relationships between CORT and colour traits seem to vary, even within the same colour mechanism. Recent research provides support for negative, positive, or no relationships between CORT levels and carotenoid or melanin coloration (e.g. Fairhurst et al., 2014, Grunst et al., 2015, Jenkins et al., 2013, Kennedy et al., 2013, San-Jose and Fitze, 2013). Compared to pigmentary coloration, the relationships between CORT and structural coloration have been much less studied, but current evidence for any such associations is similarly mixed (Grindstaff et al., 2012, Henderson et al., 2013).

In this study, we extend tests of the associations between CORT and plumage coloration to both structural coloration and utilize the unique, little studied pigmentary colour system, based on psittacofulvins, afforded by parrots (order Psittaciformes). Parrots are a large, phylogenetically distinct lineage of birds, which feature some of the most striking coloration found in nature and an extremely high proportion of threatened species (Berg and Bennett, 2010, Delhey, 2015, Hastad and Odeen, 2008, IUCN, 2016, Juniper and Parr, 1998, Mcgraw, 2006, Nemesio, 2001). Although the unusual mechanism of parrot coloration has been recognised for over a century (Krukenberg, 1882), only relatively recently have the pigments involved in their colour production been elucidated (Cooke et al., 2017, Mcgraw, 2006, McGraw and Nogare, 2005, Stradi et al., 2001). This work has revealed that much parrot coloration is based on a unique class of polyenal lipochrome pigments called psittacofulvins. In contrast to the carotenoid pigments of most other bird species, it is thought that psittacofulvins are synthesized endogenously during feather growth, most likely within the follicular tissue at the site of growing feathers (McGraw and Nogare, 2004). Parrots also produce coloration rich in short wavelengths (UV and blue) produced by feather nanostructure (Berg and Bennett, 2010, Dyck, 1971, Mullen and Pohland, 2008, Prum, 2006, Prum et al., 1999).

Despite their remarkable coloration, popularity and perilous conservation status, little is known about the stress responses of parrots, their utilisation of carotenoids, or the functional significance of their coloration (Berg and Bennett, 2010, Cooke et al., 2017, Knott et al., 2010, Mcgraw, 2006, McGraw and Nogare, 2004, Ribot et al., 2019). However, there are several reasons to hypothesize that either form of parrot coloration (pigment or structural) could function as condition-dependent signals. Firstly, psittacofulvins act as powerful antioxidants (McGraw, 2005, Morelli et al., 2003), and the metabolic processes and enzymatic pathways involved in psittacofulvin synthesis may be sensitive to limitation in intake of energy or particular nutrients. This suggests that psittacofulvins may provide signals of quality in a similar way to other forms of pigmentary coloration (Masello et al., 2008, Masello et al., 2004, Masello and Quillfeldt, 2003). Further, evidence suggests that the mechanism of non-iridescent structural coloration used by parrots can provide sexually selected signals of quality in passerine birds (e.g. Amundsen et al., 1997, Andersson et al., 1998, Keyser and Hill, 1999, Peters et al., 2007, Siefferman and Hill, 2005). In burrowing parrots (Cyanoliseus patagonus), the size of a psittacofulvin-based plumage patch covaried with a measure of body condition in adult males; the size and luminance (achromatic reflectance) of the same patch, as well as luminance of a structural patch, varied between years with different levels of precipitation (indirectly suggesting a possible link with food availability); and luminance of a structural patch in nestlings was related to body weight (Masello et al., 2008, Masello and Quillfeldt, 2003).

As parrots use psittacofulvin pigments rather than carotenoids directly in their feathers, the prevailing, yet hitherto untested, assumption is that dietary carotenoid intake will have no effect on their coloration, as it does many other taxa. However, parrots do accumulate high levels of circulating carotenoids (McGraw and Nogare, 2004), which are sensitive to dietary intake (Knott et al., 2010). As such, this hypothesis warrants testing to eliminate the possibility that carotenoids indirectly affect psittacofulvin-based coloration via general condition effects, physiological trade-offs between the deposition of psittacofulvins in feathers and the intake and utilisation of carotenoids, or through a role as pigment precursors. To date the relationships between CORT, carotenoids, diet, and immune function or condition remain untested in parrots, and whether stress or dietary intake is associated with the expression of parrot plumage coloration is unknown.

Here, we studied crimson rosellas (Platycercus elegans), a parrot native to south-eastern Australia which possesses multiple patches of both pigment- and structurally-based plumage coloration (Berg and Bennett, 2010, Ribot et al., 2019). Birds were assigned to one of three diet treatments (food restriction to lower energy intake; carotenoid supplementation; and controls), and we considered multiple plumage patches comprising two forms of colour production (psittacifulvin- or structural-based plumage). We have previously shown that food restriction resulted in a decrease in body weight and carotenoid supplementation resulted in higher levels of circulating carotenoids (Knott et al., 2010). Moreover, we have found that plumage coloration following moulting during this experiment was affected by the dietary treatment, particularly for structural coloration (unpublished results). Our aim in the study reported here, was to test whether physiological indices of stress were associated with the diet manipulation, and whether circulating CORT or carotenoids measured prior to or after the experiment predicted the change in plumage coloration of birds that underwent the manipulation. Specifically, we tested: (i) how baseline (collected within 3 min of disturbance) and stress-induced (collected after 10 min handling/restraint) CORT responded to dietary manipulation; (ii) whether CORT, or the change in CORT over the course of the experiment, predicted the change in plumage reflectance following moult during the experiment; (iii) whether circulating carotenoids were related to parrot coloration; and (iv) whether additional measures of chronic stress (heterophyl/lymphocyte ratio) or immunocompetence (phytohemagglutinin-induced response) were affected by the dietary manipulation or covaried with CORT in parrots.

Section snippets

Experimental design

We carried out the experiment using 21 captive P. e. elegans, from early spring (20 March 2007) to late autumn (12 November 2007) to ensure that the experiment encompassed the putative moulting period for P. elegans. In Australia, wild P. elegans populations exhibit signs of moult over a period of up to six months, from late spring (November) to mid autumn (April); outside these months Higgins (1999) found no birds with signs of tail or primary moult and only 4.1% of birds with signs of active

Dietary and temporal changes in CORT

Diet treatment (LMM: F2, 13 = 1.844, P = 0.197) and sampling round (F2, 80 = 0.805, P = 0.451; treatment × bleed round interaction F4,701 = 70.332, P < 0.704) did not predict CORT levels overall (Fig. 1). As expected, stress-induced CORT levels were significantly higher than baseline CORT levels (F1, 81 = 23.561, P < 0.001), with no influence of diet treatment (interaction P = 0.309). However, stress-induced CORT levels were significantly higher than baseline CORT levels only at the start of

Discussion

In this study, we tested, for the first time in a parrot species, whether physiological stress levels resulting from dietary restriction and/or carotenoid supplementation were related to the change in coloration during plumage moult. In doing so we sought to test the mechanisms determining the expression of plumage coloration in parrots, a little studied group. We studied crimson rosellas, a species for which we have found that structural coloration is more strongly associated with body

Acknowledgements

We thank Sadie Illes-Ryan, Rob Massie and Di Flower for care of the birds at Bristol, Jen Hoyal Cuthill for assistance with collecting data, and Jonathon Blount, Jarrod Hadfield, and Patrick Fitze for advice about carotenoids. We are also grateful to Ian Stewart and the staff of the NERC-funded Sheffield Molecular Genetics Facility for sexing birds, Jennie Evans and Shai Markman for assistance with the corticosterone assays, Ian D. Bull and James M. Williams for assistance with the HPLC, and

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