OPEN ACCESS JZAR Research arcle
Journal of Zoo and Aquarium Research 5(4) 2017 1
Provision of ultraviolet basking lights to indoor housed tropical birds
and their eect on suspected vitamin D3 deciency
Gabby J. Drake1*, Robyn L. Shea2, Andrea Fidge3, Javier Lopez1 and Robert M. Christley4
1North of England Zoological Society, Caughall road, Upton, Chester, CH2 1LH, U.K.
2Sandwell and West Birmingham Hospital NHS Trust, Vitamin Laboratory, Sandwell General Hospital, Lyndon, West Bromwich, B71 4HJ, U.K.
3San Diego Zoo Global, PO BOX 120551, San Diego, CA 92112-0551, United States
4Instute of Infec on and Global Health, University of Liverpool, Leahurst Campus, CH64 7TE, U.K.
*Correspondence: Dr. Gabby Drake; email@example.com
Keywords: avian, MBD, osteodystrophy,
tropical birds, ultraviolet light, UVB,
Received: 16 Dec 2016
Accepted: 9 Aug 2017
Published online: 31 Oct 2017
Vitamin D deciency (measured as 25(OH)D3) can occur if birds are fed a vitamin D decient diet and
do not have access to ultraviolet B light (UVB). This can result in eggs with decient yolks and ulmately
to metabolic bone disease (MBD) in chicks. In this study, hypovitaminosis D was suspected in 31 adult
birds, from ve orders, housed indoors long-term without prior access to UVB light. The study aimed
to assess the eect of providing UVB basking lights on vitamin D status and the incidence of MBD
in chicks. It also aimed to assess whether the birds would access the UVB provided. Breeding and
pathology records were analysed, and birds were blood tested for 25(OH)D3 before, and 12 months
aer, being provided with access to UVB basking lights. The area of perching with UVB irradiance was
lmed before and aer the UVB basking lights were switched on. There was a signicant increase
in 25(OH)D3 aer 12 months of UVB provision from a mean of 9.3 nmol/L to 14.2 nmol/L (P=0.001,
CI=2.35 to 9.47). Annual incidence of metabolic bone disease in chicks dropped from an average of
14.3% over the three years prior to UVB provision to 3.2% in the two years aerwards. Birds appeared
to acvely seek the basking spots and signicantly increased the proporon of me spent in the area of
UVB irradiance (P=0.02). No correlaon was found between the total amount, or change, in me spent
in the UVB area and the nal, or change, in number of individual birds with circulang 25(OH)D3 levels.
These results show that indoor-housed birds will bask in UVB light if provided and that this radiaon
can increase vitamin D levels of the birds, which may prevent MBD in their ospring.
Vitamin D is a steroid hormone essenal for calcium and bone
metabolism in most vertebrates, including birds (Bauck, 1995,
Watson, 2014). Adequate vitamin D, calcium and phosphorus
are required for normal growth. Vitamin D deciency can
cause metabolic bone disease (MBD), characterised by low
bone density, bowing of long bones and pathological fractures
(Adkesson and Langan 2007; Cousquer et al. 2007; Stanford
2006; Tangredi and Krook 1999; Van Wyk 1993).
Vitamin D precursors are either obtained through the diet
or endogenously produced in the skin or uropygial gland
secreons through photo-conversion by ultraviolet B (UVB)
light found in sunlight, wavelengths 290–315 nm. The major
circulang vitamin D metabolite is 25-hydroxycholecalciferol
(25(OH)D3) which represents the sum of dietary and sunlight/
UVB sources (Lupu and Robins 2013; Watson 2014). 25(OH)
D3 has the longest half-life of the metabolites, and serum or
plasma levels provide the most stable indicator of vitamin
D status (Bar 2008); thus, it is the most commonly used
metabolite for measuring vitamin D. 25(OH)D3 is converted
to calcitriol (1,25-dihydroxyvitamin D), the acve vitamin D
metabolite, in the kidneys.
Diet is a signicant source of cholecalciferol (vitamin D3)
in carnivorous or piscivorous birds. Ergocalciferol (vitamin
D2), an alternave pre-cursor of calcitriol, found in plant
material, may be ulised by some omnivore or herbivore
species. However, it is unknown which bird species, if any, have
the metabolic pathways required to process this pre-cursor
(Watson 2014). Birds generally have high renal clearance and
a poor metabolism of dietary vitamin D2 so it is unlikely to
constute a substanal source of vitamin D (Stanford 2006;
Bar 2008; Watson 2014). Furthermore, the diet of granivorous
and frugivorous species (Lupu and Robins, 2013) is commonly
decient in vitamin D3. In such cases, therefore, if there is a
prolonged lack of exposure to UVB light, vitamin D deciency
can result. Parental deciency of calcium or vitamin D3
can cause poor quality yolk with lile or no reserves for the
developing chick (Coto et al. 2010a; Mala et al. 2004). UVB
dependent vitamin D deciency and MBD is well documented
in callitrichid monkeys (Thornton 2002), reples (Calvert 2004)
and birds, such as African grey parrots (Psiacus e. erithacus)
Journal of Zoo and Aquarium Research 5(4) 20172
Drake et al.
(Stanford 2005). No published data could be found relang to the
species invesgated in this study.
Producon of 25(OH)D3 via the UVB pathway is self-regulang
due to build-up of inert metabolites in the cus (Lupu and Robins
2013). However, oral supplementaon of 25(OH)D3 is poorly
regulated via negave feedback (Bar 2008), and can result in an
excess, which could be harmful to the bird (Watson 2014; Sco
Echols 2006). For this reason, exposure to UVB light is a safer
alternave to dietary supplementaon (Stanford 2006; Lupu and
Robins 2013), especially if species requirements are unknown.
Domesc poultry given UVB via natural sunlight signicantly
increased the 25(OH)D3 content of their egg yolks (Kuhn 2014),
suggesng that the provision of UVB light in sucient quanes
to the hens in this study should be a way to increase yolk vitamin
D3 to provide for the chick in the rst three weeks of life.
At Chester Zoo, osteodystrophy and pathological fractures
consistent with metabolic bone disease were idened in the
chicks of mulple tropical bird species breeding in an indoor aviary.
The aected chicks and their parents had no access to either
sunlight or UVB radiaon in the wavelengths 290–315 nm. Since
dietary calcium and calcium to phosphorus raos were known to
be adequate, vitamin D deciency in parents was hypothesised
to be the cause of the MBD in chicks. This study was designed
in response to these clinical issues and addressed the following
objecves: to invesgate whether this populaon of birds would
ulise arcial UVB basking spots; and to assess the eect of this
method of UVB light supplementaon on the circulang vitamin
D levels (measured as 25(OH)D3) of the adult birds and on the
incidence of MBD in chicks.
Materials and methods
This study was opportunisc as UVB lighng was being installed
in the study aviaries as part of ongoing husbandry improvements.
Study design was longitudinal, each bird was its own control, thus
ensuring no bird was denied UVB light. The study was approved
by the Ethical Commiee of both Chester Zoo and the University
of Liverpool. Samples were taken during clinical invesgaon and
followed up by a qualied veterinary surgeon.
Animals and husbandry
Birds were housed in ve large aviaries (minimum 15 m2 to
maximum 25 m2) within a tropical house. Thirty-one adult birds
of ve orders (Table 1) had been living in these aviaries for more
than one year at the start of the study in January 2012, and were
thus eligible for inclusion. A calculaon using Altman’s nomogram
revealed a sample size of 25 birds should be sucient to idenfy
biologically signicant changes in vitamin D (Sabin and Petrie
2011). Aviary groups remained stable, with the excepon of
birds added through breeding (n=25), or removed by death (n=3
adults) or removed as young stock (fully grown) once independent
from their parents (n=16). A singe male was briey moved to
the neighbouring study aviary due to aggression. Pathology
and breeding records for all birds housed in these aviaries were
reviewed for breeding acvity and cases of metabolic bone
disease between 2009 and 2014 inclusive.
Birds were fed species-appropriate diets formulated by a
nutrionist, comprising a combinaon of commercial pellets, fresh
chopped fruit and live invertebrates, and blends made with pellets,
crushed egg shell, vegetables and cooked egg as appropriate. Diets
had a mean calcium content of 1.36% dry maer. Diets contained
suitable calcium to phosphorus raos (mean 5.7:1) and remained
unchanged throughout the study period.
Two UVB spot-lights (Arcadia 160W Basking lamps, Arcadia
Products plc, Redhill, U.K.), producing light in the wave lengths
290–315 nm, were installed in each aviary. In each aviary, one light
was posioned high, above the branches used for perching, to
give tree dwelling birds UVB access—subsequently referred to as
the high resource area; and the second was located at a height to
provide ground dwelling birds with an area of UVB, subsequently
referred to as the low resource area. Lights were situated a mean
distance of 66.3 cm (range 60–90 cm) from the perch or ground.
Lights and perches were ed for at least three weeks prior to light
illuminaon, to allow the birds to acclimase to the new aviary
furniture. Basking lights were then switched on (Day 0 for study
mings) from 10:00 to 14:00 every day from Day 0 to Month 4,
then from 06:00 to 14:00 for the rest of the study (Months 5–12).
The output of the lights was monitored throughout the
Order Species (Common name) Scienc name Number in study MBD seen
Galliformes Congo peafowl Afropavo congensis 1Yes
Cuculiformes White crested turaco Tauraco leucolophus 3Yes
Passeriformes Snowy headed robin chat Cossypha niveicapilla 2Ye s
White-rumped shama Copsychus malabaricus 2Yes
Chestnut-backed thrush Zoothera dohertyi 1
Montserrat oriole Icterus oberi 2Yes
Fairy bluebird Irena puella 2
Brazilian tanager Ramphocelus bresilius 2
Columbiformes Mindanao bleeding heart dove Gallicolumba criniger 4Yes
Luzon bleeding heart dove Gallicolumba luzonica 1Yes
Socorro dove Zenaida macroura graysoni 4
Green naped pheasant pigeon Odiphaps nobilis nobilis 2Yes
White naped pheasant pigeon Odiphaps nobilis aruensis 3Ye s
Piciformes Brown-breasted barbet Lybius melanopterus 2
Table 1. Species, number and history of metabolic bone disease (MBD) in birds
Journal of Zoo and Aquarium Research 5(4) 2017 3
Vitamin D and ultraviolet light in indoor birds
study using a UVB meter (Solarmeter® Model 6.2, SOLAR LIGHT
COMPANY INC. Glenside, PA, USA, measuring µw/cm2 UVB light).
Bulbs were tested at 30 cm and gave readings between 90 and 134
µw/cm2 when new. They were replaced if their output dropped
by more than 50% from the inial reading. There was no other
source of UVB in the study aviaries.
Health assessment and vitamin D3 sampling
All birds were examined prior to the main breeding season
in 2012, which was prior to Day 0. The birds were weighed,
clinically examined, radiographed and blood sampled. Where
sucient sample was obtained, blood biochemistry was checked
as well as vitamin D (measured as 25(OH)D3). The birds were re-
examined and blood sampled again 12 months aer illuminaon
of the basking lights. At the inial examinaon, radiographic bone
density and conformaon was considered normal for all birds
and plasma ionised calcium, where measured, was within normal
avian limits (>1.00 mmol/L) (data not shown), so these tests were
Blood samples for 25(OH)D3 analysis were taken from the
jugular, ulnar or metatarsal vein (as appropriate) and placed in
heparinised blood tubes (Microvee 500 lithium heparin, Sarstedt,
Numbrecht, Germany). Sample volume never exceeded 1% of body
weight as per avian guidelines (Best 2008). Heparinised samples
were centrifuged at 11,800 rpm for three minutes and separated
plasma samples were placed in Eppendorf tubes and either sent
directly to the laboratory or frozen at –20°C unl batches could
be sent for analysis. The drops remaining in the syringe hub were
placed on lter paper (Whatman 903 lter paper, GE Healthcare,
Whatman Plc, Maidstone, UK) and air-dried for blood spot analysis.
In some birds, small sample volume allowed only one technique to
be used (blood spot, n=4; plasma, n=5).
At Sandwell & West Birmingham Hospitals NHS Trust Vitamin
Laboratory, UK, blood spots were analysed for 25(OH)D3 as three
millimetre punches from the lter paper on a Waters TQS Tandem
Mass spectrometer using an electro-spray ionisaon interface
with a Water’s i-Class UPLC, following liquid/liquid extracon with
a derivasaon step enhancing small volume analysis.
Plasma 25(OH)D3 was assayed using a Waters ACQUITY
UPLC and Quaro Premier XE MS/MS mass spectrometer
(Herordshire, England) with an electro-spray ionisaon interface
following liquid/liquid extracon of the sample. Both methods are
linear to 1,100 nmol/L with a limit of quantaon of 7.5 nmol/L
for 25(OH)D3. The plasma assay is accredited by the Vitamin D
External Quality Assessment Scheme (DEQAS) and the laboratory
is accredited by the Clinical Pathology Accreditaon (CPA) UK Ltd.
Using human samples, the blood spot assay had been aligned
with the plasma assay so that blood spot and plasma results were
UVB resource use
UVB meter readings were used to map out the area of UVB
radiaon produced by each bulb (high and low) and the intensity
of radiaon at bird level. In each aviary, a “UVB resource area” was
dened as the basking areas at bird level where >10 µw/cm2 UVB
irradiance was detected. This constuted a radius of between 60
and 80 cm in each case. The peak UVB reading at bird level was
also recorded, with an average of 31 µW/cm2 (24–65 µW/cm2).
A webcam (Logitech Webcam HD C270, Logitech Europe S.A.,
Lausanne, CH) was used to lm the UVB resource areas in each
aviary, as the presence of an observer could alter bird behaviour.
Footage was recorded on a laptop outside the aviary using
movement recognion soware (iSpy freeware, hp://www.
iSpyconnect.com). Each resource area was lmed in each aviary
(n=6) for ve to seven consecuve days between 06:00 and
14:00 during the six-week period prior to UVB light illuminaon
(baseline data). Filming was repeated at least four weeks aer
light illuminaon (UVB data).
Mpeg video clips were reviewed by a single observer using
QuickTime Player (QuickTime 7.0, Apple Inc., Cuperno, CA) and
the me stamp was used to record the me and duraon of a visit
by any bird accessing the UVB resource during the observaons.
Birds were idened to species level in all cases and individually
where possible. Where two indisnguishable birds were present
in an aviary their UVB resource use was recorded as the average of
the total me one or both birds were visible in the UVB resource.
Aviaries were not lmed if birds were breeding, as brooding could
restrict access to the UVB resource.
All data analyses were performed using Microso Excel (2010,
Microso Corporaon, Redmond, WA) and R (R core team, 2013).
Annual incidence of MBD in chicks before and aer provision
of UVB supplementaon was compared using Fisher’s exact
test due to small sample size in the post treatment group. This
test was performed excluding the rst treatment year (2012)
as iniaon of supplementaon coincided with the start of the
breeding season, thus there would have been insucient me for
circulang 25(OH)D3 levels in the hen birds to change.
25(OH)D3 levels obtained by each method (blood spot and
plasma) were averaged between the methods for each sampling
point to minimise missing data, as some samples only provided
enough volume for one method. The lower limit of the assay was
7.5 nmol/L; thus, values reported as <7.5 nmol/L were given a
nominal value of 7.5 nmol/L for stascal analysis. A Wilcoxon-
signed ranks test for non-parametric paired data was used to
compare values from pre-supplementaon and 12 months aer
Behavioural data were only available from three of the six
aviaries holding a total of 15 birds due to issues with the video
footage. Data were analysed for me spent in the resource area
for baseline and UVB access. For each bird, the total me, in
seconds, spent in the resource area was calculated. Total me
observed was calculated. As not all observaon periods were the
same length, the proporon of me spent in the resource area
during observaon was used for comparison.
Year Number chicks
Annual incidence of MBD
in chicks at risk (%)
No UVB provision
2009 23 4 17.4
2010 27 3 11.1
2011 41 614.6
Total 91 13 14.3
Paral UVB provision
2012 25 4 16.0
2013 13 0 0.0
2014 18 15.6
Total 31 1 3.2
Table 2. Number of birds bred and cases of metabolic bone disease (MBD)
idened per year.
UVB, ultraviolet B light. Paral UVB provision refers to supplementaon
being for insucient duraon prior to the breeding season for data to be
Journal of Zoo and Aquarium Research 5(4) 20174
Drake et al.
UVB radiaon doses (mJ/cm2) were calculated from the
irradiance received by each bird (mW/cm2) mulplied by the
exposure me (seconds) (Lupu and Robins 2013).
It was noted during video analysis that some birds roosted
overnight on the UVB resource perches. As light intensity is the
trigger for birds to rise in the mornings, birds were frequently
sll roosng during the rst hour of data collecon during the
baseline data collecon period, but roused immediately once
the UVB basking lights came on during the UVB data collecon
period. In order to allow a comparison of baseline and UVB data,
only acvity between 10:00 and 14:00 was compared to avoid
this “roosng eect”. A Wilcoxon-signed ranks test was used to
compare the proporon of me spent in the UVB resource pre-
and post-UVB supplementaon.
Spearman’s rank correlaon tests were used for all correlaon
assessments. The full data set from 06:00 to 14:00 was used to
compare me spent accessing the UVB basking light with nal
25(OH)D3 concentraon and changes in 25(OH)D3, as baseline
observaon data were not required. The data from 10:00 to
14:00 were used to assess for correlaon between change in UVB
resource use and the nal 25(OH)D3 and changes in 25(OH)D3
Annual incidence of MBD appeared to decrease from a range of
11.1–17.4% before UVB supplementaon to a range of 0–5.6%
in the years aer UVB supplementaon was iniated (Table 2).
However, this dierence was not stascally signicant (P=0.19).
There was a signicant increase in circulang 25(OH)D3 levels aer
12 months of UVB supplementaon (P=0.001, CI=2.35 to 9.47;
Figure 1, full data set Appendix 1). However, there was individual
variaon with some birds showing a marked increase, while lile
change was observed in others. The mean pre-supplementaon
circulang 25(OH)D3 was 9.3 nmol/L and the mean aer 12
months was 14.2 nmol/L, thus exhibing a mean increase of 4.9
nmol/L across all birds. The pre-supplementaon range was 7.5 to
27.7 nmol/L, interquarle range (IQR) 7.5 to 8.25 nmol/L. Twelve
months aer UVB supplementaon the range was 7.5 to 48.1
nmol/L, IQR 7.5 to 15.2 nmol/L.
25(OH)D3 levels were reported as <7.5 nmol/L in a number of
birds since this was the lower limit of quantaon of the assay.
As a result, actual levels in these birds may have been anywhere
between 0 and 7.4 nmol/L. Therefore, actual increases could be
larger than idened for 12 of the birds whose baseline values
were at 7.5 nmol/L and increased above this threshold aer 12
months, which could mean a biologically signicant increase for
the individual. Six of the birds remained below 7.5 nmol/L, so it is
unknown whether their levels increased or decreased between 0
and 7.4 nmol/L. The measures of three out of four birds with levels
that dropped, went below 7.5 nmol/L, so there may actually have
been larger decreases than could be detected by the assay.
Seven hens bred in 2012, and three of these were birds with
circulang 25(OH)D3 levels which dropped aer supplementaon.
Table 3 shows the mean dierence between blood spot and
plasma methods, range and standard deviaons for these results
Use of UVB resource area
Baseline observaons compared to UVB provision
The proporon of me spent in the UVB resource area increased
signicantly aer the basking lights were illuminated (P=0.02;
point esmate of mean 0.0272 ± 0.0204; Figure 2, full data set
Appendix 1). This corresponds to an average increase of 6 min 32
sec per bird, per four hour observed window per day (CI 1 min 39
sec to 11 min 25 sec) in the UVB resource area.
The pre-supplementaon minimum proporon was 0.000360,
corresponding to 5 seconds, median 0.005008 (1 min 12 sec),
IQR 0.002644 to 0.017090 (38 sec to 4 min 6 sec) and maximum
Species (common name) Average dierence between blood
spot and plasma D3 (nmol/L)
Range (nmol/L) Standard deviaon (nmol/L)
Congo peafowl -2.4 -2.7–2.0 0.5
White crested turaco -0.1 -2.1–1.8 1.4
Snowy headed robin chat 1.6 0–5.5 2.6
White-rumped shama -5.7 -13.8–0.1 7.3
Chestnut-backed thrush n/a n/a n/a
Montserrat oriole 0.2 0–0.3 0.2
Fairy bluebird -0.4 -2.8–1.1 1.7
Brazilian tanager 0 0–0 0
Mindanao bleeding heart dove 0.4 -6.6–4.9 3.5
Luzon bleeding heart dove 0.2 -0.2–0.6 0.6
Socorro dove -1.4 -7.2–0 3.2
Green naped pheasant pigeon 0.3 -1.2–2.6 1.6
White naped pheasant pigeon 0 0–0 0
Brown-breasted barbet n/a n/a n/a
Table 3. Comparison of blood spot and plasma 25(OH)D3 results grouped by species.
Journal of Zoo and Aquarium Research 5(4) 2017 5
Vitamin D and ultraviolet light in indoor birds
light to adults and increased 25(OH)D3 in adults to be consistent
with other more-studied avian species. Sub-clinical vitamin D
deciency in chickens can result in deciency in their egg yolks and
in the developing chicks, leading to MBD, which can be resolved by
addressing the vitamin D3 levels of the adults (Coto et al. 2010b).
No clinical issues were found in the adult birds in this study,
despite hypothesised vitamin D deciency. This is consistent with
work on domesc poultry where hens with vitamin D deciency,
but ample calcium, show no clinical signs of hypovitaminosis D
(Nascimento et al. 2014). The diet provided was adequate for
calcium. Although oered zoo diets are formulated complete, it
is well documented from intake studies there may be dierences
in nutrional balance compared to the actual diet eaten (Fidge
and Robert 1993). Therefore, we cannot be certain of nutrient
bioavailability from the data available and cannot rule out a
dietary component of the MBD seen in chicks. However, the diets
oered did not change during the study and we have no reason to
suspect the birds altered their intake during this me, therefore
diet is unlikely to be the cause of the reducon in MBD.
Arcial provision of UVB basking lights had a posive eect
on vitamin D3 levels in the birds in this study, with a stascally
signicant increase in circulang 25(OH)D3 following 12 months
of eight hours per day ad libitum UVB basking light access. As
there is believed to be eecve feedback to prevent excess levels
of vitamin D3 accumulang from UVB exposure (Lupu and Robins
2013), this suggests that some of the birds could have been sub-
clinically decient at the start of the study, as their levels were
physiologically able to rise.
Average pre-supplementaon circulang 25(OH)D3
concentraon was 9.3 nmol/L in this study, which appears low
when compared to some other avian taxa. In experimental work
with African grey parrots (Psiacus e. erithacus), Stanford (2005)
reported a mean pre-UVB plasma 25(OH)D3 concentraon of
23.1 nmol/L in capve birds. In budgerigars (Melopsiacus
undulatus) given no UVB access, 25(OH)D3 levels of 7.93–16.03
nmol/L have been reported (Lupu and Robins 2013). In other avian
orders, cases of metabolic bone disease have been reported in
growing wild birds with vitamin D3 levels this low. In American
crows (Corvus b. brachyrhynchos), plasma 25(OH)D3 values of
8.0 (± 2.65) nmol/L were found in young wild birds with MBD
compared to 20.0 (± 6.04) nmol/L in unaected birds (Tangredi
and Krook 1999). In Columbiformes, values of 3.90 nmol/L were
reported for three clinical MBD cases in young wild collared doves
0.043700 (10 min 29 sec) per bird per four hour observed window
per day. Aer 12 months of UVB supplementaon this had
increased to a minimum proporon of 0.01010 (2 min 25 sec),
median 0.03360 (8 min 4 sec), IQR 0.01360 to 0.05805 (3 min 15
sec to 13 min 56 sec) and maximum 0.11950 (28 min 41 sec) per
bird per four hour observed window per day. However, within
each of the aviaries, some birds dramacally increased their usage
of the UVB resource area while others reduced their usage.
Esmated UVB doses
When the lamp was in use, the daily average me spent in the
UVB resource area (>10 uW/cm2) was 18 min 35 sec (range 2 min
46 sec to 40 min 17 sec). Minimum average daily UVB doses were
therefore 11.15 mJ/cm2 (range 1.66 to 24.17 mJ/cm2). Maximum
average calculated daily doses based on the average maximum
irradiance of 31 µW/cm2 were 34.57 mJ/cm2 (5.15 to 74.93 mJ/
cm2) if the birds remained in the peak area of UVB emied by the
Correlaons between UVB resource use and average 25(OH)D3
Final, and change in, circulang 25(OH)D3 concentraon aer
12 months was not associated with the proporon of me spent
in the UVB resource (rho=0.08, P=0.8 and rho=0.17, P=0.59,
respecvely). The nal, and change in, circulang 25(OH)D3
concentraon was not associated with the change in proporon
of me spent in the UVB resource before and aer the basking
lights were illuminated (rho=0.12, P=0.7 and rho=0.23, P=0.47,
The incidence of MBD in chicks appeared to reduce following
UVB basking light provision to the adults from 14.3 % to 3.2 %
subsequently. However, the small numbers involved, combined
with the limited number of years of follow up, may have contributed
to the lack of stascal signicance. Fewer chicks were bred in
2013 and 2014, compared to previous years. However, three of
four birds which bred in 2013, and four of ve birds which bred
in 2014, had previously produced chicks with MBD, supporng
the possibility of a true reducon following UVB provision. The
annual incidence of 5.6% in 2014 represents a single case of MBD
from the snowy headed robin chats. Physiologically, we nd the
reducon in MBD in ospring following provision of UVB basking
Figure 1. Box and whisker plot of vitamin D (25(OH)D3) concentraons
before and aer 12 months of UVB basking light provision.
Figure 2. Box and whisker plot of the proporon of me spent in the UVB
basking spot between 10:00 and 14:00 before and aer UVB basking lights
Journal of Zoo and Aquarium Research 5(4) 20176
Drake et al.
(Streptopelia decaocto) and a range of 10.0–25.0 nmol/L is quoted
as normal, although this is unreferenced (Cousquer et al. 2007).
If this ‘normal’ range is accurate, then 83% (25/30) of the birds in
this study were decient in vitamin D3 at the start, falling to 44%
(12/27) by the end of the study.
Average 25(OH)D3 concentraon aer 12 months of UVB
supplementaon in this study was 14.2 nmol/L; an average
increase of 4.9 nmol/L. These are considerably lower levels and
smaller changes than those idened in African grey parrots by
Stanford (2005) who reported a mean increase in plasma 25(OH)
D3 concentraon of 77.9 nmol/L aer one year of 12 hours per
day of direct UVB light. However, the same study also found
mean concentraons of 33.68 nmol/L (95% CI 8.00–59.63) in
19 wild African grey parrots, suggesng such high 25(OH)D3
concentraons, although not detrimental to the birds, may not
be physiologically required. In budgerigars, increases in 25(OH)
D3 of 1.61–11.31 nmol/L, to 9.54–27.34 nmol/L, occurred aer
short duraon UVB exposure experiments (Lupu and Robins
2013); changes which are comparable with those observed in
the present study. Despite there being considerable variability in
response to UVB provision in this study, the overall tendency was
for circulang 25(OH)D3 levels to increase with UVB basking light
provision. This is especially signicant as birds were not forced to
remain under the UVB basking lights, unlike in the experimental
work discussed, but were free to access the resource, suggesng
provision of UVB basking lights for indoor housed birds does not
have to be ubiquitous to have an eect. In addion, the spectrum
of the lights used in this study is more akin to natural sunlight
than those used by Lupu and Robins (2013), which contained
proporonally higher levels of very short wavelength UVB light
which can cause damage to the skin and eyes of birds.
Blood spot and plasma results were averaged to minimise
missing data where only one method was possible in this study.
The blood spot assay was aligned with the plasma assay using
human samples, not avian samples. There is evidence that
these two methods may not be comparable in reples, likely
due to issues with lower haematocrits signicantly altering the
spreading characteriscs of replian blood compared to mammals
(Whitehead and Fogge 2016); however, bird haematocrits are
more similar to those of mammals and our data suggest that the
two methods are acceptably similar. This is concurred by Michaels
(2015) who states that results for these two methods should be
comparable within the same study, as applies here.
Mulple species were used in this study, and despite the
mechanism for producon of vitamin D3 appearing to be well
conserved throughout the taxonomic groups (Dacke 2000; Bar
2008), species variaon, both physiologically and in feeding and
basking behaviours, may have aected conversion eciency and
therefore inuenced these results. In a zoological collecon, it
is rare to have large numbers of the same species to study, and
therefore when an opportunity arises to perform a study such as
this, even with mulple species, the generated data are valuable.
Some of the birds’ circulang 25(OH)D3 levels did not change
detectably post-supplementaon (n=6) and some actually
reduced (n=4). Some birds may not have received adequate
doses because in a mixed aviary, there may be compeon for
the UVB resource. In addion, birds were given the freedom to
voluntarily access the resource, and the UVB provided by a bulb
is weak compared to sunlight. Doses of 180 mJ/cm2 (0.012 mW/
cm2 over 6 hr for 5 d) have been reported to produce a signicant
increase in plasma 25(OH)D3 in budgerigars, while doses of 65 mJ/
cm2 (0.012 mW/cm2 for 2 hr) resulted in no signicant increase
(Lupu and Robins 2013). These are considerably larger doses and
of shorter wavelengths—due to dierences in the lamps used—
than the birds in this study received, but this perhaps suggests
that the UVB dose could have been inadequate for some study
birds. However, the experiments of Lupu and Robins (2013)
lasted only ve days, unlike the present study in which long-term
exposure was provided. This may be why, in the majority of birds,
circulang 25(OH)D3 increased through bioaccumulaon, despite
the low doses. In chickens, circulang 25(OH)D3 has a half-life
of approximately 21 days (Coto et al. 2010a) and changes in
circulang 25(OH)D3 may occur more slowly than accounted for
by Lupu and Robins (2013).
Three of the four birds whose circulang 25(OH)D3 levels
decreased aer 12 months of UVB provision were breeding
hens, raising the possibility that their starng levels were either
arcially elevated as serum stores transferred to yolk at the
me of rst sampling, or were depleted by egg laying by the
me of the second sample. One of these hens was the snowy
headed robin chat hen, which produced a MBD-aected chick
following provision of UVB light. In domesc poultry, increases
and decreases in yolk vitamin D have been shown to occur in line
with both circulang vitamin D levels and UVB access (Narbaitz et
al. 1987; Kuhn 2014). Values from wild birds would also aid in the
understanding of normal ranges for each species, to truly dene
deciency in these hens.
The dierences in eect may also be due to interspecic
variaon in the eciency of conversion of 7-dehydrocholesterol
to pre-vitamin D3 in the skin. For example, canopy-dwelling
species, where UVB exposure should be high in the wild, might
have received insucient doses compared to naturally-reclusive
species which may be beer adapted to photoconvert at lower
light levels. This hypothesis is consistent with the poor responses
seen in this study in the Brazilian tanagers, fairy bluebirds and
white crested turacos, all of which are canopy species; this eect
warrants further invesgaon.
The indoor housed tropical birds in this study chose to access
UVB basking lights when given the opportunity, with a stascally
signicant increase in the proporon, and amount, of me spent in
the UVB resource area observed aer the lights were illuminated.
This nding is consistent with another study in which various birds
showed a preference for an area of ultraviolet spectrum lighng
(Ross 2013). Not all birds showed increased usage in each aviary.
The variaon in use could represent compeon from dominant
species prevenng access by the shyer ones. For instance, the
snowy headed robin chats were observed compeng with the
white crested turacos (which are much larger and more aggressive
birds) for access, and the proporon of me spent in the resource
by the robin chats decreased as that of the turacos increased. This
compeon eect would be worth invesgang further, as it could
have a signicant impact on the eecveness of UVB basking light
provision in mixed species exhibits.
It is unclear why the birds chose to spend more me under
the lights. They may be insncvely basking in the “sunlight”;
indeed, many birds were observed preening while sing under
the lights. Equally, the birds may be seeking the heat produced
by the lights, or the UVA light emied by the bulbs, as birds can
see into this spectrum (Rajchard 2009). Addional experiments
substung the UVB bulbs with basking lamps which produce
dierent combinaons of heat, UVA and UVB would be required
to disentabgle these possible inuences and determine the best
condions to aract birds to a therapeuc source of UVB.
There was no signicant correlaon between the nal, or
change in, circulang 25(OH)D3 levels in the birds and the total
or change in proporon of me spent in the UVB resource
area. However, data for both circulang 25(OH)D3 levels and
behavioural observaons were only available from 13 birds for this
comparison. Hence, the sample size is small in these analyses, and
a weak correlaon may have been missed. The results could also
have been inuenced by interspecies variaon, the species mixes
and the necessity to average data between birds which could
Journal of Zoo and Aquarium Research 5(4) 2017 7
Vitamin D and ultraviolet light in indoor birds
not be individually idened. Some females in this comparison
bred in the 2012 season and depleon to yolk may have aected
circulang 25(OH)D3 levels. Finally, the behavioural data collecon
period constuted one week, which equates to only a fracon of
the study me, and so may not truly represent the birds’ acvity.
In conclusion, provision of UVB basking light in the wavelengths
290–315 nm to indoor housed tropical birds on an ad libitum basis
can result in increases in circulang vitamin D3, levels which may
be biologically signicant. Therefore, UVB basking light access
could be used to reduce vitamin D3 deciency in a variety of
species without restricng aviary sizes. Importantly, the incidence
of metabolic bone disease in chicks appeared to be reduced
following UVB provision for the adult birds. Birds appeared to
acvely choose to access the ultraviolet basking spots and showed
a signicant increase in the proporon of me spent in an area
where this resource was provided. Whether this preference was
due to the UVB, UVA or increased heat from the lamps could not
be determined from the data available. Parcular care should be
taken when providing UV to mixed species aviaries, as interspecies
compeon may prevent some species from accessing the
The authors would like to thank the Bird Team of Chester Zoo, with
special acknowledgment to Andrew Owen, Wayne Mcleod and
Clare Wylie for their support of this work and the veterinary team,
with special thanks to Alison Kelsall and Tanya Grubb for help with
the diagnosc sampling.
Adkesson M.J., Langan J.N. (2007) Metabolic bone disease in juvenile
Humboldt penguins (Spheniscus humbold): Invesgaon of
ionized calcium, parathyroid hormone, and vitamin D3 as diagnosc
parameters. Journal of Zoo and Wildlife Medicine 38(1): 85–92.
Bar A. (2008) Review: ‘Calcium homeostasis and vitamin D metabolism
and expression in strongly calcifying laying birds. Comparave
Biochemistry and Physiology Part A 151: 477–490.
Bauck L. (1995) Nutrional Problems in Pet Birds. Seminars in Avian and
Exoc Pet Medicine 4(1): 3–8.
Best J.R. (2008) Passerine birds: approach to the sick individual. In: Chiy, J.
and Liertz, M. (eds). BSAVA Manual of Raptors, Pigeons and Passerine
birds, Gloucester, UK: Brish Small Animal Veterinary Associaon,
Calvert I. (2004) Nutrional problems. In: Girling, S.J. and Rai, P. (eds).
BSAVA Manual of Reples (2nd Edion), Gloucester, UK: Brish Small
Animal Veterinary Associaon, 289–308.
Coto C., Cerate S., Wang Z., Yan F., Min Y., Costa F.P., Waldroup P.W. (2010a)
Eect of source and level of vitamin D on the performance of breeder
hens and the carryover to the progeny. Internaonal Journal of Poultry
Science 9: 623–633.
Coto C., Cerate S., Wang Z., Yan F., Waldroup P.W. (2010b) Eect of source
and level of maternal vitamin D on carryover to newly hatched chicks.
Internaonal Journal of Poultry Science 9: 613–622.
Cousquer G.O., Dankoski E.J., Paerson-Kane J.C. (2007) Metabolic bone
disease in wild collared doves (Streptopelia decaocto). Veterinary
Record 160: 78–84.
Dacke C.G. (2000) Chapter 18 – The Parathyroids, Calcitonin, and Vitamin
D In: Causey Whiow G. (ed). Sturkie’s Avian Physiology (5th Edion),
Cambridge, Massachuses: Academic Press, 473–488.
Fidge, A.L. and Robert, J.N. (1993) An invesgaon into nutrion and
mortality in capve St. Lucia parrots (Amazona versicolor). Dodo,
Journal of the Wildlife Preservaon Trusts 29: 103–125.
Lupu C. and Robins S. (2013) Determinaon of a safe and eecve
ultraviolet B radiant dose in budgerigars (Melopsiacus undulatus):
A pilot study. Journal of Avian Medicine and Surgery 27(4): 269–279.
Mala P., Valaja J., Rossow L., Venalainen E., Tupasela T. (2004) Eect
of vitamin D2- and D3-enriched diets on egg vitamin D content,
producon, and bird condion during an enre producon period.
Poultry Science 83(3): 433–440.
Michaels C.J., Antwis R.E., Preziosi R.F. (2015) Impacts of UVB provision
and dietary calcium content on serum vitamin D3, growth rates,
skeletal structure and coloraon in capve oriental re-bellied
toads (Bombina orientalis). Journal of Animal Physiology and Animal
Nutrion 99: 391–403.
Narbaitz R., Tsang C.P.W., Grunder A.A. (1987) Eects of vitamin D
deciency in the chicken embryo. Calcied Tissue Internaonal 40:
Nascimento G.R., Murakami A.E.I., Guerra A.F.Q.M.I., Ospinas-Rojas I.C.I,
Ferreira M.F.Z.I., Fanhani J.C.I. (2014) Eect of dierent vitamin D
sources and calcium levels in the diet of layers in the second laying
cycle. Brazilian Journal of Poultry Science 16(2): 37–42.
R Core Team (2013). R: A language and environment for stascal
compung. R Foundaon for Stascal Compung, Vienna, Austria.
[online] ISBN 3-900051-07-0. Available from hp://www.R-project.
Ross M.R., Gillespie K.L., Hopper L.M., Bloomsmith M.A., Maple T.L. (2013)
Dierenal preference for ultraviolet light among capve birds from
three ecological habitats. Applied Animal Behaviour Science 147:
Sabin A., Petrie C. (eds) (2011) Medical Stascs at a Glance (3rd Edion),
Hoboken, NJ: Wiley Blackwell.
Sco Echols, M. (2006) Evaluang and treang the kidneys. In: Harrison
G.J. and Lighoot T.L. (eds). Clinical Avian Medicine: Volume 2. Palm
Beach, Florida: Spix Publishing Inc., 451–492.
Stanford M.D. (2005) Calcium metabolism in grey parrots: the eects of
husbandry. Fellowship Thesis London, UK: Royal College of Veterinary
Stanford M.D. (2006) Calcium Metabolism. In: Harrison G.J. and Lighoot
T.L. (eds). Clinical Avian Medicine: Volume 1. Palm Beach, Florida: Spix
Publishing Inc., 141–151.
Tangredi B.P and Krook L.P. (1999) Nutrional secondary
hyperparathyroidism in free-living edgling American crows (Corvus
brachyrhynchos brachyrhynchos) Journal of Zoo and Wildlife Medicine
Thornton S.M. (2002) Primates. In: Meredith A. and Johnson Delaney C.
BSAVA Manual of Exoc Pets (4th Edion), Gloucester, UK: Brish
Small Animal Veterinary Associaon, 127–137.
Van Wyk E., Van der Bank F.H., Verdoorn G.H. (1993) Blood plasma calcium
concentraons in capve and wild individuals of the cape grion
vulture (Gyps coprotheres). Comparave Biochemistry and Physiology
Part A 104(3): 555–559.
Whitehead M.L. and Fogge S. (2016) UV lighng, dietary vitamin D3, and
serum 25(OH)D in crocodilians and iguanas. Proceedings of the Brish
Veterinary Zoological Society, September 2016, Oxford: 20.
Journal of Zoo and Aquarium Research 5(4) 20178
Drake et al.
Journal of Zoo and Aquarium Research 5(4) 2017 9
Vitamin D and ultraviolet light in indoor birds
Journal of Zoo and Aquarium Research 5(4) 201710
Drake et al.
Journal of Zoo and Aquarium Research 5(4) 2017 11
Vitamin D and ultraviolet light in indoor birds
Journal of Zoo and Aquarium Research 5(4) 201712
Drake et al.