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8/13/2019 Sexual Dichromatism in the Blue Fornted Amazon (Amazona Aestiva) Revealed by Multiple Angel Spectrometry

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Sexual Dichromatism in the Blue-fronted Amazon Parrot ( Amazona aestiva )Revealed by Multiple-angle SpectrometryAuthor(s): Susana I. C O. SantosPhD, Brian Elward, Johannes T. LumeijDVM, PhD, Dipl ECAMSSource: Journal of Avian Medicine and Surgery, 20(1):8-14. 2006.Published By: Association of Avian VeterinariansDOI: http://dx.doi.org/10.1647/1082-6742(2006)20[8:SDITBA]2.0.CO;2URL: http://www.bioone.org/doi/full/10.1647/1082-6742%282006%2920%5B8%3ASDITBA%5D2.0.CO%3B2

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Journal of Avian Medicine and Surgery 20(1):814, 2006 2006 by the Association of Avian Veterinarians

Sexual Dichromatism in the Blue-frontedAmazon Parrot ( Amazona aestiva ) Revealed by

Multiple-angle SpectrometrySusana I. C. O. Santos, PhD, Brian Elward, and Johannes T. Lumeij, DVM, PhD,

Dipl ECAMS

Abstract: Seventy-ve percent of psittacine species, including the blue-fronted Amazon parrot( Amazona aestiva ), are classied as sexually monomorphic. However, this classication is based onthe inability of the trichromatic human eye to perceive light in the near-ultraviolet spectrum. Spec-

trometry is a technique that enables humans to recognize the increased range of color perceived bythe tetrachromatic avian eye. By using this technique, researchers have reclassied many avianspecies as sexually dimorphic. In this exploratory study, several body regions of 30 blue-frontedAmazon parrots (males and females) were investigated by multiple-angle spectrometry. A modelwas developed that enabled gender prediction with 100% accuracy based on plumage color char-acteristics. However, the areas that were most promising in our model (forehead and wing tip) needto be conrmed independently to exclude the possibility of type I error attributed to multiple testing.

Key words: sexual dimorphism, spectrometry, ultraviolet reectance, plumage color, avian, blue-fronted Amazon parrot, Amazona aestiva

Introduction

Birds have traditionally been categorized as sex-ually monomorphic or dimorphic based on theiranatomy and plumage color as judged by the humaneye. 1,2 Approximately 70%80% of birds are sexu-ally dimorphic by this system, but the males andfemales of many species of birds, including 75% of parrot species, remain indistinguishable to the hu-man eye. 3,4 Knowledge of a birds gender is impor-tant for the veterinary practitioner, the owner, andthe breeder. Accurate gender determination is es-sential for proper pairing of birds, and knowing thegender of a bird will allow the veterinarian to rulein or out gender-specic diseases.

Several means of gender determination have beendeveloped for sexually monomorphic avian species.In poultry, cloacal sexing of day-old chicks is wide-ly used, but this method of sexing birds is limited

From the Zoology Museum of Barcelona, P picasso s/n, ParcCiutadella, 08003 Barcelona, Spain (Santos); and the Division of Avian and Exotic Animal Medicine, Department of Clinical Sci-ences of Companion Animals, Faculty of Veterinary Medicine,Utrecht University, Yalelaan 8, 3584 CM Utrecht, The Nether-lands.

to only a few species. Gonad visualization by lap-aroscopy is a direct and accurate method for sexinga bird. 5 Laparoscopic sexing, however, requirestraining and expensive instruments and carries withit the risk of anesthesia and injury from an invasiveprocedure. It is also not 100% accurate, especiallywhen immature birds are examined. 6,7 More recent-ly, laboratory-based assays for gender determinationhave been developed, including hormone assays of feces; examination of cells in metaphase for Z andW chromosomes; and molecular techniques such asrestriction fragment length polymorphism, analysisof polymerase chain reaction amplication prod-ucts, and random amplied polymorphic DNA

markers.5,814

Although laboratory-based tests, par-ticularly molecular assays, have proven to be af-fordable and accurate for many avian species, eachhas its limitations, and none can be applied to allspecies of birds.

Recently, it has been shown that birds have theability to see the near-ultraviolet (UV) spectrum andthat most birds have plumage that reects UV light.Some psittacine species also have uorescent plum-age, which absorbs short wavelengths and re-emitsthem at longer wavelengths, resulting in a color that


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9SANTOS ET ALMULTIPLE-ANGLE SPECTROMETRY REVEALS SEXUAL DICHROMATISM

Figure 1. Multiple-angle spectrometric measuring tech-nique showing the angle ber holder (A) and positioningof the holder on the plumage of a blue-fronted Amazonparrot (B). The angle ber holder is a mechanical device

with 15 -angle steps that holds illumination and obser-vation ber-optic probes in position at a xed distance (2mm) from the measuring surface, preventing exposure toany external reectance and illumination. The holder waspressed lightly on the birds plumage surface while ori-ented perpendicular to the birds longitudinal axis (B) forevery measurement. The incident illumination beam isshown 90 to the plumage surface, and the 2 arrows(black and white) represent 2 examples of observationpositions ( 45 ).

is a combination of UV reectance and uores-cence. Ultraviolet reectance may play a role insexual communication, mate choice, and courtshipdisplays. 1521

Reectance spectrometry in the avian visiblerange (320700 nm) has been shown to be an im-

portant tool for plumage color assessment in variousstudies. 2,1727 Many studies have shown that birds,initially classied as sexually monochromatic, areactually dichromatic when the UV part of the spec-trum is considered. 18,2832 Most of these studies usedonly 1 illumination and 1 observation angle. Morerecent work shows that by varying these angles, ad-ditional information can be obtained, resulting inthe detection of gender-specic plumage differenc-es. 33 In the study reported here, multiple-angle re-ectance spectrometry was used to investigate gen-der differences in plumage color in the blue-frontedAmazon parrot ( Amazona aestiva ).

Materials and Methods

Spectroscopy

A total of 30 adult blue-fronted Amazon parrots(17 live, 13 dead) were used in the study. All pro-cedures were performed with permission from theanimal experimentation committee from the Facultyof Veterinary Medicine, Utrecht University,Utrecht, The Netherlands (DEC 0404.0703).

Five body regions were examined in each birdbased on their importance in sexual displays, UVphotography, and previous ndings from other spe-cies of birds 33 : the frons (blue forehead), the occiput(green nape), the tetriceces alulae dorsales (yellowalula), the pars pennacea of the rst remiges pri-mariae (dark-blue wing tip), and the tectrices cau-dales (green tail, middle portion). Live birds wereanesthetized with isourane for all measurements,and each carcass was examined within 2 days of abirds death. Ten reectance measurements weretaken from each body region. After each measure-ment, the probe was removed from and reapplied tothe same area. Feathers were illuminated with aDH-2000 deuterium-halogen light source (AvantesBV, Eerbeek, The Netherlands), and measurementswere made with an AVS-USB2000 spectrometer(Avantes BV) connected to a computer notebook with software (Avasoft-basic, Avantes BV, Eerbeek,The Netherlands) that stored data and calculated allcolor parameters.

Five different illumination/observation angleswere used for spectra measurements: 45 /45 , 45 / 90 , 45 /135 , 90 /75 , and 90 /90 . The illumina-tion/observation angles of 45 /45 and 90 /90 weremade with a bifurcated ber-optic probe (FCR-

7UV4002, Avantes BV) that had a black plasticsheath xed to the ber end. The sheath kept theprobe the same distance from the feathers for allbody regions measured. All other illumination/ob-servation angles were achieved with an AFH-15 an-gled ber holder (Avantes BV) (Fig 1A). The berholder was lightly pressed on the feathers perpen-dicular to the long axis of the birds body (Fig 1B).Reectance spectra with wavelengths of 320700nm were measured over an approximately 2-mmarea. Reectance was dened as the percentage of reected light compared with the reective lightfrom a polytetrauorethylene white standard tile(WS-2, Avantes BV, Eerbeek, The Netherlands) anda dark standard (light source off). White and dark references were taken before each different illumi-nation/observation angle was investigated and at thebeginning of each measurement session. The genderof each bird was unknown at the time spectra mea-surements were recorded. After measurements wereobtained, each birds gender was determined byDNA analysis 13 or, in the cases of deceased birds,by dissection.

To determine if uorescence was present in thebody regions examined and to prevent inuence of


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10 JOURNAL OF AVIAN MEDICINE AND SURGERY

Figure 2. Examples of angle geometries demonstratingsexual dichromatism in 3 body regions of male and fe-male blue-fronted Amazon parrots. (A) Forehead mea-sured with 90 /75 illumination/observation angles. (B)Wing tip measured with 90 /90 illumination/observation

angles. (C) Alula measured with 90 /75 illumination/ob-servation angles. Males (n 12) are represented withsolid lines and females (n 18) are represented withdotted lines. Each line represents the average of the me-dians of 10 measurements.

this trait on reectance results, an additional surveywas made in the plumage of 6 birds with a UV light.

Data analysis

Each reectance spectrum contained 1206 datapoints taken at 0.31-nm intervals. The original spec-tra were compressed to 102 data points to facilitatecalculations. Reectance data were summarized inseveral parameters, both in the UV spectrum (wave-length 320400 nm) and in the total spectrum(wavelength 320700 nm). Denition of param-eters was as follows: lightness (L), the light reect-ed by the plumage surface, was calculated as thesum of percent reectance values from the consid-ered range; color intensity (R max ) was the maximumreectance reached in the considered range; hue (H)was the wavelength at peak reectance in the con-sidered range ( R max ); contrast (C) was the differ-ence between the maximum and minimum reec-tance in the considered range (R max R min ); and UVChroma (UV Ch) was the reectance sum over theUV range divided by the total reectance (R 320400 / R 320700 ). 35 Medians of the values of the 10 param-eters (for each bird and each body region) were usedin a logistic regression analysis to test for sexualplumage color dichromatism in each body regionand each angle geometry, and signicance was test-ed with the Likelihood ratio test. 35 To establish evenmore accurate models to predict the gender of blue-fronted Amazon parrots, new logistic regressionmodels were established by a combination of pa-

rameters from different angle geometries and bodyregions. These parameters were the selected vari-ables (relevant for the model) for the rst logisticregression. Results were evaluated for P values of .05 and .001. The latter value was used to reducethe possibility of type I error attributed to multipletesting. Statistical analysis was conducted by SPSS11.0 (SPSS Inc, Chicago, IL, USA).

Results

According to DNA analysis or direct visualiza-tion of the gonads at necropsy, 18 of the blue-front-

ed Amazon parrots were identied as females and12 were identied as males. Fluorescence was notfound in any body region of the birds; therefore, all


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Table 1. Results from logistic regression analysis for each angle geometry and body region of the blue-fronted Amazonparrot. a

Anglegeometry

(illumination/ observation)

Bodyregion

Modelvariables

Mean SD

Females (n 18) Males (n 12) OR b POverall %

correct gender

45 /45

45 /90

45 /135

Forehead

ForeheadWing tip

Forehead

C uv

C uvH uv

UV ChC uv

18.65 6.69

10.64 3.00389.01 16.90

0.20 0.036.99 2.29

13.33 2.86

7.42 3.10372.56 19.20

0.23 0.014.82 1.91

0.82

0.690.96

6.10E 260.54

.0151

.0098

.0435

.0091

.0122

65.4

76.971.4

84.6

90 /90

90 /75

ForeheadWing tip

Forehead

AlulaWing tip

H uvH tot

UV ChH uvC totH tot

380.63 12.14433.91 38.49

0.21 0.02386.55 13.7

76.78 10.13414.77 37.64

370.24 7.01396.28 48.47

0.23 0.01371.17 11.11

63.40 14.21360.50 44.05

0.090.98

2.98E 700.880.910.97

.0135

.0265

.0008

.0112

.0067

.0023

69.271.4

84.6

74.178.6

a OR indicates odds ratio; C, contrast (R max R min ); uv, ultraviolet range (320400 nm); H, hue ( R max ); UV Ch, UV Chroma (R 320400 /R 320700 ); and tot, total range (320700 nm).

b Condence intervals of the OR were omitted because of inaccurate standard errors.

Figure 3. Example of different angle geometries show-ing or not showing gender differences in the wing tips of blue-fronted Amazon parrots. Solid lines correspond tomales (n 12) and dotted lines correspond to females (n

18). Gray lines correspond to 45 /45 illumination/ob-servation angles and black lines correspond to 90 /90illumination/observation angles. Each line is the averageof the medians of 10 measurements.

reectance captured by the spectrometer was attri-buted to light reectance. Reectance spectra fromall body regions were characterized by 2 spectralpeaks, 1 in the UV and 1 in the visible portionof the spectrum. These 2 peaks were less clearlydened in the wing tips. Reectance spectra reacheda maximum of 102.5% in the alula; the next highestvalue was 84.2% in the forehead. The forehead was

the body region that showed highest brightness inboth the UV and visible spectra.

Signicantly different (.001 P .05) meanvalues for brightness, color, or hue were demon-strated on the forehead, wing tip, and alula betweenthe male and female groups (Table 1; Fig 2). Dif-ferences in the means for the males and femaleswere seen in all angle geometries of the forehead.Logistic regression analysis showed that malescould be separated from females with 84.6% cer-tainty in 2 angle geometries, 45 /135 and 90 /75 ,each based on the calculation of 2 parameters in theUV part of the spectrum, that is, UV Ch and C uv orUV Ch and H uv , respectively (Table 1). The 90 /75angle geometry appeared to show gender differenc-es most clearly. In all body regions, the reectancespectra, and consequently most calculated parame-ters, changed signicantly when the angle geometrywas changed (Fig 3). The H uv was an exception tothis in the forehead, alula, and nape.

Several models combining different parameters,body regions, and angle geometries resulted in a100% accurate gender determination of all the birds.Table 2 illustrates some of the possible combina-tions.

Discussion

The results of this study demonstrate that meanvalues of several spectra parameters measured weresignicantly different ( P .05) between male andfemale blue-fronted Amazon parrots. These data


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Table 2. Examples of combined multiple logistic regression models for gender prediction in the blue-fronted Amazonparrot. a

Body regions(parameters)

Angle geometry(illumination/ observation) OR b P

Overall %correct gender

Wing tip (Htot

)Forehead (UV Ch)Alula (L tot )

90 /7590 /7590 /75

0.56

0.99

.0058

.0005

.0146100

Wing tip (H tot )Wing tip (L tot )Wing tip (C tot )Wing tip (UV Ch)

90 /7590 /9090 /9045 /135

0.021.11

7.12E 135

.0000

.0081

.0000

.0000

100

Wing tip (H tot )Forehead (UV Ch)

90 /7590 /75

0.861.52E 219

.0006

.0002 96

Forehead (UV Ch)Alula (H tot )

45 /4545 /45

1.96E 781.10

.0021

.0015 82.6

a OR indicates odds ratio; H, hue ( R max ); tot, total range (320700 nm); UV Ch, ultraviolet Chroma; L, lightness; C, contrast (R max Rmin ).b

Condence intervals of the OR, and some OR values (indicated by empty cells), were omitted because of inaccurate standard errors.

suggest that there is sexual dimorphism in this spe-cies that cannot be recognized by the human eye.The use of a single measurement in an individualbird, however, did not provide sufcient accuracyfor applied use of this technique. When groups of 3 variables were used in the logistic regression, 2combinations of variables were found that coulddistinguish gender in 100% of the birds examined.Additional studies are needed to determine whetherthese values will be equally predictive in other pop-ulations of blue-fronted Amazon parrots. Examina-tion of other areas of feathering may also revealgender-linked variations.

Psittaciforms are some of the most colorful birds;however, few studies have been performed on parrotcoloration, 22,3640 and even fewer have been per-formed on the ecological and evolutionary signi-cance of their plumage color. 37,40 Recent studieshave suggested that avian plumage colors have thepotential to indicate male quality, 30,37,4144 immuno-competence, 44,45 body condition, 34,47,48 health, 46,4953

and the ability to provide parental care. 32,54,55 Therange of values observed in the population of birdsexamined with the overlap of male and female val-ues may reect the variations in the underlyinghealth of the birds. Therefore, it is possible that thistechnique may have some value as a diagnostic toolin addition to its potential use for gender determi-nation.

This exploratory study suggests that multiple-an-gle spectroscopy may provide a quick, readily ap-plied, and noninvasive method for gender determi-nation in the blue-fronted Amazon parrot. The use

of multiple-angle geometries in the forehead andcalculation of contrast in the UV range seems themost promising model for gender determination inthis species. However, further independent work isneeded to conrm the usefulness of this model.

Acknowledgments: We thank the staff from the Sectionof Avian and Exotic Animal Pathology, Department of Pathobiology, Veterinary Faculty, Utrecht University, fortheir assistance. We are grateful to Sander van der Waland Carolijn Herenius for their assistance with the mea-surements and to all the technicians of the Division of Avian and Exotic Animal Medicine, Department of Clin-ical Sciences of Companion Animals, Utrecht University.We also thank Sandra Imholz for assistance with DNAsexing of the birds. Furthermore, we would like to thank all the persons willing to volunteer their animals for thisresearch: Dennis Jansen, Bert Deiman, Stichting Pape-gaaienhulp, and Mark Jansen. This research was fundedby an investigation grant provided by Fundacao para aCiencia e Tecnologia (FCT), SFRH/BD/3405/2000, Por-tugal.

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