Environmental enrichment on the behavior and welfare of cockatiels (Nymphicus hollandicus)

Abstract

This study evaluated the influence of physical environmental enrichment on the behavior of cockatiels (Nymphicus hollandicus). Eighteen birds, nine males and nine females, were monitored in environments enriched with wooden sticks and bead rings and in non-enriched environments, in a completely randomized design. Behavioral categories were grouped into locomotion, maintenance, rest, feed, undesirable activities, and interaction with environmental enrichment. Data were analyzed using descriptive analysis of behaviors to produce the ethogram and percentage comparison of frequency values for behavior analysis. Environmental enrichment positively influenced behavioral categories and some behavioral activities of birds.

Full text

Arq. Bras. Med. Vet. Zootec., v.68, n.3, p.562-570, 2016
Environmental enrichment on the behavior and welfare
of cockatiels (Nymphicus hollandicus)
Enriquecimento ambiental no comportamento e no bem-estar de calopsitas
(Nymphicus hollandicus)]
V.D.L. Assis1, T.S.G. Carvalho2, V.M. Pereira3, R.T.F. Freitas2, C.E.P. Saad2,
A.C. Costa2, A.A.A. Silva4
1Universidade Federal de Goiás ˗ Goiânia, GO
2Universidade Federal de Lavras ˗ Lavras, MG
3Universidade Federal de Minas Gerais ˗ Belo Horizonte, MG
4Centro Universitário de Lavras ˗ Lavras, MG
ABSTRACT
This study evaluated the influence of physical environmental enrichment on the behavior of cockatiels
(Nymphicus hollandicus). Eighteen birds, nine males and nine females, were monitored in environments
enriched with wooden sticks and bead rings and in non-enriched environments, in a completely
randomized design. Behavioral categories were grouped into locomotion, maintenance, rest, feed,
undesirable activities, and interaction with environmental enrichment. Data were analyzed using
descriptive analysis of behaviors to produce the ethogram and percentage comparison of frequency values
for behavior analysis. Environmental enrichment positively influenced behavioral categories and some
behavioral activities of birds.
Keywords: ethogram, parrot, stress, wild animal
RESUMO
Objetivou-se, com o presente trabalho, avaliar a influência do enriquecimento ambiental físico sobre o
comportamento de calopsitas (Nymphicus hollandicus). Foram monitoradas 18 aves, sendo nove machos
e nove fêmeas, em ambientes enriquecidos com tocos de madeira e argola de miçangas e sem
enriquecimento ambiental. O delineamento foi inteiramente ao acaso. As categorias comportamentais
foram agrupadas em locomoção, manutenção, repouso, alimentação, atividades indesejáveis e interação
com o enriquecimento ambiental. Os dados foram examinados por meio da análise descritiva dos
comportamentos para elaboração do etograma e comparação percentual das frequências observadas
para análise dos comportamentos. Foi observada influência positiva do enriquecimento ambiental sobre
as categorias comportamentais e algumas atividades comportamentais das aves.
Palavras-chave: animal selvagem, etograma, estresse, psitacídeos
INTRODUCTION

Characteristic features of parrots (Psittaciformes)
include a strong, curved bill and thick fleshy
tongue with the upper jaw curved over the lower
one, adapted for a seed and fruit-based diet.
Members of this order include macaws, parrots,
parakeets, cockatoos, and cockatiels (Nymphicus
hollandicus). The Cockatiel was described by
Recebido em 11 de setembro de 2015
Aceito em 7 de janeiro de 2016
E-mail: nessinhadany@yahoo.com.br
Scottish writer and naturalist Robert Kerr in
1793 as Psittacus Hollandicus and was
subsequently moved to its own genus,
Nymphicus, by Wagler in 1832. The bird became
well known in England in 1864, and around 1884
there were several European breeders.
Cockatiel breeding requires no special
authorization, as the Ordinance No. 93
of the Brazilian Institute of Environment and

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Renewable Natural Resources of June 7 1998
considers these birds as pets (Ibama, 1998), thus
enabling captive breeding.
A captive environment is mostly a structure
where animals rarely face challenges when
compared to the natural environment, which can
cause them problems. Environmental enrichment
techniques have been used as an alternative to
reduce such concerns. Cubas et al. (2006)
described environmental enrichment as an
example of promoting captive animal welfare, as
it provides opportunities to maintain motor skills
and exploratory, predatory, and other near-
natural behaviors, thus improving psychological
and physiological welfare and health conditions.
However, introducing any form of environmental
enrichment requires knowing animal behavior.
To expand knowledge beyond practice, we can
use ethograms for each species. Del-Claro (2004)
defined ethograms as tabular representations to
classify and quantify a species’ behaviors,
composing a properly quantified list of
behavioral acts which may be described when
necessary.
This study evaluated the influence of
environmental enrichment on the behavior of
captive cockatiels (Nymphicus hollandicus) by
comparing the frequency of behavioral
categories and bird activities.
MATERIAL AND METHODS
The experiment was conducted at the Division of
Wildlife, Department of Animal Science (DZO),
Federal University of Lavras (UFLA), located in
southern Minas Gerais at a 900m altitude. This
study had the approval of the ethics committee in
the use of animals, under protocol 013/13.
The study observed eighteen cockatiels, nine
females and nine males at an average age of ten
months. Birds were identified by open bands
around the left paw in females and right paw in
males for easy differentiation.
Each bird was housed in a wire cage of
85x40x45cm (length, depth, height) comprising
three wood perches, two feeding bowls (plastic
and ceramic), and a ceramic water bowl placed
on the bottom. Cages were placed side by side in
two shelves of 10m each in a 12-meter masonry
shed covered with asbestos roof tiles.
Temperature and humidity were measured by a
thermo hygrometer.
Birds received 12 hours of artificial light (40 W
lamps) controlled by timer Elcon TE 30. The
behavioral analysis took place during the day,
from 6am to 6pm. Feed and water were provided
ad libitum, and feed comprised a seed mixture of
50% millet, 30% birdseed, 15% oat, 5%
sunflower, and commercial parrot feed. Cage
management was performed once a day from
8am to 10am, and afterwards the birds remained
alone.
The trial took place from March - May 2013. In
March the birds were observed to produce the
ethogram. In April and May the experiment
began by introducing environmental enrichment.
After a seven-day adjustment, we began the
observation phase.
Environmental enrichment tools were:
- Wood sticks 3cm long and 2cm wide with a
hole, so that birds could easily catch them with
their beaks;
- Iron rings with 14cm circumference partially
covered with beads, so that birds could move
them around the ring.
Cockatiels (Nymphicus hollandicus) were
observed in the experimental area using the ad
libitum technique. According to Castro (2010),
this method consists of non-systematic records in
which the observer tries to note all visible and
relevant activities.
Observations lasted seven days from 8am - 11am
and 12:30pm - 4:30pm, amounting to 49 hours.
The ethogram for evaluating bird behavior was
based on both previous bird observations and
adapted ethograms by Prestes (2000), Pimenta et
al. (2009), Sgarbiero (2009), Silva et al. (2010),
and Andrade and Azevedo (2011). Activities
were grouped into behavioral categories defined
as locomotion, maintenance, rest, feeding,
undesirable activities, and interaction with
enrichment tools.
We found 15 types of behavior in the species
under study, listed on Table 1.

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Table 1. Behavioral acts recorded on observation of cockatiels (Nymphicus hollandicus) with
abbreviations and description of each behavior
Behavioral Categories Abbreviation Description
Locomotion
DP Moving laterally on the perch
AT Walking on the cage screen
A Walking on the cage floor
Maintenance LP Preening
SP Shaking the plumage
Rest
R Resting over the belly, head backwards rested on the
back or under the wing, or eyes closed
RP Resting on the perch
PT Standing still on the cage screen
PCH Standing still on the cage floor
Feeding BA Drinking water
C Climbing food bowls or eating
Undesirable Activities
RPO Biting the perch
RPA Biting food bowls
RG Biting the cage screen
Interaction with
enrichment tools BR Playing with enrichment tools.
Based on previous observations and adapted from Prestes (2000), Soares et al. (2009); Sgarbiero (2009), Silva
(2010), and Andrade (2011).
Data was collected by recording each cage for 12
uninterrupted hours from 6am - 6pm during three
consecutive days, totaling 36-hours of footage
per period.
We used the all-occurrence sampling technique,
which according to Roll (2006) allows for
observing an animal group by recording all
occurrences of a given category in a previously
determined behavior. Images were recorded by
three video cameras (Camera Color 8mm CCD
1/3 Infrared ST1230) placed on tripods 1.20cm
distant from the cages and connected to a Dvr
Stand Alone 4 Channels 120 Frames Lux Vision
Vga 3g. Images were transmitted to an LG
monitor c17lc-0 for analysis. Footage material
was monitored every ten minutes while recording
for collecting data series for behavioral
analysis: 6xz observations/hour/cage, 72
observations/day/cage, 216 observations/cage/
period, 648 observations/cage during the
experimental time. The total 11,664 observations
were recorded on spreadsheets (Attachments)
based on the behavioral categories as indicated in
the ethogram.
The experiment used a completely random
design in treatment rotation, so that each bird
received all three treatments. At each enrichment
change, the birds underwent a 7-day adaption
period. Data were subjected to descriptive
analysis of behaviors for making the ethogram
and to percentage comparison of frequency
values for behavioral analysis.
RESULTS AND DISCUSSION
Figure 1 shows the percentages of behavioral
categories shown by the animals during the
evaluation period. Observation frequency of
behavioral categories differed between
treatments.
Birds in cages without environmental enrichment
moved around more frequently than the ones in
the enriched environment. No abnormal behavior
was recorded in this study. Locomotion is very
important for assessing bird activity and
excessive behavioral activities, as excess and
repeatability of certain behaviors may indicate
stereotyped or abnormal behavior.

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Figure 1. Percentage of behavioral categories in adult cockatiels (Nymphicus hollandicus) in three
conditions of environmental enrichment
1L - Locomotion; M - Maintenance; A - Feeding; R - Rest; AI - Undesirable activities; IE- Interaction
with enrichment tools.2 SE- No enrichment; AM- Bead rings; TO - Wood sticks.
Cockatiels spent more time preening feathers
when cages were not enriched. However, this
increased frequency did not lead to any
exaggerated behavior. This result corroborates
with Santos et al. (2011), who reported reduced
preening in macaws housed in enriched
environment.
Parrots spend most of their time preening
feathers, lubricating and protecting them with
uropygial gland oil. However, this behavior
increases when the captive environment becomes
boring, and exaggerated care can cause self-
mutilation. Abnormal behaviors, such as
stereotypies, self-mutilation, feather pecking, or
excessively aggressive behavior indicate that the
animal is under low welfare conditions (Broom
and Molento, 2004).
We found a higher frequency of feeding in birds
housed in cages without environmental
enrichment. However, it is not possible to affirm
that environmental enrichment negatively or
positively affected the birds, as feed
consumption was not measured during the
evaluation period.
Birds in cages with environmental enrichment
had decreased idleness in relation with birds
without enrichment. This result corroborates with
Soares et al. (2009) and Santos et al. (2011), who
evaluated the influence of environmental
enrichment on macaw behavior and found
decreased bird idleness in cages with physical
and feeding enrichment.
Environmental enrichment had a positive effect
on the behavior of cockatiels, reducing the
frequency of undesirable activities when bead
rings and wooden sticks enriched the cages. In
this study, birds interacted with both types of
tools. These activities are good examples of
promoting captive animal welfare, as they
provide opportunities to maintain motor skills
and exploratory, predatory, and other near-
natural behaviors, thus improving psychological
and physiological welfare and health conditions
(Cubas et al., 2006).
Frequency of birds moving laterally on the perch
was higher with ring beads (AM) (35.15%) and
wooden sticks (TO) (37.75%) in the cages
(Figure 2).

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Figure 2. Mean frequency of behavioral activities in the category "locomotion" of adult cockatiels
(Nymphicus hollandicus) in three conditions of environmental enrichment
1DP- Moving on the perch, AT- Walking on the cage screen, A- Walking on the cage floor.2SE - No
enrichment, AM - Bead rings, TO - Wooden sticks.
Walking on the cage screen (AT) was more
frequent in environments enriched with ring
beads (AM) (39.89%) than with wooden sticks
(TO) (33.08%). Walking on the floor was more
frequent in cages with wooden sticks (29.17%)
than with ring beads (24.96%). According to
Andrade and Azevedo (2011), the behaviors
"moving on the perch" and "moving on
the cage screen" decreased with environmental
enrichment.
Birds preened feathers (LP) more frequently
(91.84%) and shook the plumage (SP) less
frequently (8.16%) when there was no
environmental enrichment available (Figure 3).
Figure 3. Mean frequency of behavioral activities in the category "maintenance" of adult cockatiels
(Nymphicus hollandicus) under three conditions of environmental enrichment.
1LP – Preening feathers, SP - Shaking the plumage, 2SE - No enrichment. AM - Bead rings, TO - Wooden
sticks.

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According to Andrade and Azevedo (2011),
frequency of shaking the plumage is very high
during the enrichment phase, as bird interaction
is intense. Prestes (2000) suggests that the
species (Amazona pretrei) of parrot family
(Psittaciformes) such as cockatiels, scratches its
own body mostly for relaxation and tranquility.
However, the behavior "preening feathers" was
lower during the enrichment phase.
Environmental enrichment did not reduce the
mean frequency of idleness in the evaluation of
the behavioral activities "lying on belly" (R) and
"resting on the perch" (RP) (Figure 4).
Figure 4. Mean frequency of behavioral activities in the category "rest" of adult cockatiels (Nymphicus
hollandicus) in three conditions of environmental enrichment.
1R- Lying on belly; RP - Resting on the perch, PCH - Standing on the cage floor, PT- Standing on the
cage screen. 2SE - No enrichment AM - Bead rings, TO - Wooden sticks.
However, birds stood still on the screen (PT) less
in cages with wooden sticks (TO) (22.92%) than
in cages with bead rings (AM) or no enrichment
(SE). The mean frequency of "standing on the
cage floor" (PCH) reduced with bead rings (AM)
(14.06%) and wooden sticks (14.84%).
Parrots in general are very active, curious birds
(Gorman, 2010), thus captive ones need stimuli
to prevent them from becoming too idle and
bored. However, information on most species of
parrots is limited, and captivity management can
be challenging. Thus, daily observation of birds
is very important to understand their behavior.
(Allgayer and Cziulik, 2007). In the behavioral
category "rest", it is clear that environmental
enrichment can reduce idleness in some
activities.
Bead rings (AM) and wooden sticks (TO)
increased the frequency of behavioral activity
"drinking water" (BA), (4.53%) and (3.30%)
respectively (Figure 5).
Figure 5. Mean frequency of behavioral activities in category "feeding" of adult cockatiels (Nymphicus
hollandicus) in three conditions of environmental enrichment.
1BA-Drinking water, C- Climbing food bowls or eating. 2SE - No enrichment, AM - Bead rings; TO -
Wooden sticks.

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568 Arq. Bras. Med. Vet. Zootec., v.68, n.3, p.562-570, 2016
Frequency of feeding was higher in birds
in cages without environmental enrichment
(97.72%) than with enrichment.
Andrade and Azevedo (2011) reported that birds
in cages without environmental enrichment
increased water consumption and reduced dietary
intake. Reduced consumption was explained by
the greater interest of birds for enrichment items
than for the feed available.
Undesirable activities "biting the perch" (RPO)
and "biting the cage" (RG) were more frequent in
birds in cages without environmental enrichment,
(1.74%) (RPO) and (64.34%) (RG), showing that
environmental enrichment could reduce such
behaviors (Figure 6).
Figure 6. Mean frequency of behavioral category "undesirable activities" of adult cockatiels (Nymphicus
hollandicus) in three conditions of environmental enrichment.
1RPO - Biting the perch, RPA - Biting food bowls, RG - Biting the cage. 2SE - No enrichment, AM- Bead
rings, TO - Wooden sticks.
Biting the cage (RG) was reduced by introducing
environmental enrichment (bead rings - AM and
wooden sticks - TO), and this behavior was less
frequent when birds received bead rings (AM)
(25.43%). Bead rings (AM) and wooden sticks
(TO) did not positively affected reduction in
"biting food bowls" (RPA), showing that birds
did not interact with enrichment tools enough to
reduce this behavior (Figure 6).
When the environment is not enriched, captive
parrots tend to bite everything around, which is a
common habit in both nature and captivity.
Biting is their way to wear the beak down to
avoid abnormal growth, apart from being an
activity to occupy time and reduce boredom.
Typical behavioral mismatches are common in
these species when observed in captive
environments (Meehan et al., 2004). In this study
we characterized undesirable behaviors as those
that lead to nursery losses, as parrots cause
destruction in facilities. The behaviors "pecking
the perch" (BP), "pecking the screen" (BT),
"walking from one side to the other" (PAC) and
"pecking the wire" (BAR) are deemed abnormal
behaviors (Young 2003).
Mean frequency showed that birds had greater
interaction with bead rings than with wooden
sticks (Figure 7).
This preference may have been due to wide color
variation in bead rings in relation to wooden
sticks. Turek (1963) cited by Kim et al. (2009)
reported the preference of European birds for
more colorful plants. Arruda et al. (2008)
evaluated the influence of fruit color on bird
preference and found they prefer bright-colored
fruits to white ones.

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Figure 7. Mean frequency of behavioral category "interaction with environmental enrichment" in adult
cockatiels (Nymphicus hollandicus).
*AM- Bead rings, TO - Wooden sticks.
Environmental enrichment should be creative
and animal-safe. According to Milatão (2008),
enrichment tools must be nontoxic and must not
facilitate escape or cause animal harm. Tools
should be suitable for each cage and not remain
there for long; otherwise they will lose the
novelty characteristics. Although the types of
enrichment used in the study had not been
previously tested, we observed bird interaction
with both tools.
When animal behavior is assessed in categories
and activity, analyses show different frequencies.
The reason is that birds have different behaviors
in relation to frequency of activities, despite
belonging to the same species. In addition, there
is individuality among individuals. Most
available indicators of high degree of welfare are
found in studies reporting positive animal
preferences (Broom et al., 2004).
CONCLUSIONS
Environmental enrichment showed positive
results in some behavioral activities, confirming
that birds need an environment that provides
more ways to spend their time, thus enhancing
welfare. In other activities, it was not possible to
observe changes in the behavior of cockatiels in
enriched cages. Thus, more research is needed to
test other parameters and types of environmental
enrichment.
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