Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

Reintroduction and monitoring of the bird Amazona aestiva

(Psittaciformes: Psittacidae) in Brazil

Ricardo Evangelista Fraga1, 2; https://orcid.org/0000-0001-9345-4869

Caio Márcio Rodrigues Santos2; https://orcid.org/0009-0005-0074-1858

Ramona Soares Silva2; http://orcid.org/0000-0002-1176-1986

Rayana Emanuelle Rocha Teixeira1; https://orcid.org/0000-0001-5287-2853

Laize Tomazi1; https://orcid.org/0000-0003-0977-8508

Márcio Borba da Silva1; https://orcid.org/0000-0002-6497-7924

Cleverson Zapelini2; https://orcid.org/0000-0002-0796-1563

Alexandre Schiavetti2*; https://orcid.org/0000-0001-8429-7646

1. Multidisciplinary Institute in Health, Federal University of Bahia, Vitória da Conquista, Bahia, Brazil;

ricardoefraga@hotmail.com, rayemanuelle27@gmail.com, laizetomazi@yahoo.com.br,

biologomarcioborba@gmail.com

2. Laboratory of Ethnoconservation and Protected Areas (LECAP), State University of Santa Cruz, Ilhéus,

Brazil; caiorodrigues.s@hotmail.com, ramonacte@hotmail.com, czapelini@yahoo.com.br, aleschi@uesc.br

(Correspondencia*)

Received 14-XI-2022. Corrected 20-III-2023. Accepted 16-V-2023.

ABSTRACT

Introduction: Reintroduction is a procedure used to reestablish wild animal populations.

Objective: To evaluate the success of reintroducing Amazona aestiva and investigate whether abiotic factors

(temperature, humidity, and luminosity) interfere with the search for food supplementation in feeders installed

in the release area.

Methods: Pre-release evaluations were initiated with 59 Amazonas spp. Tests were run to stool parasitological

tests, leukocytes, flight capacity, and level of animal-human interaction. In all, 33 animals were selected and

sent to the release area, which is an ecotone between the Atlantic Forest and the Caatinga biomes. After release,

visits to the feeders and survival in the area were monitored for a year. Abiotic factors were also recorded in

these periods.

Results: The stool parasitological tests revealed the presence of Heterakis spp. and Eimeira spp. The leukocyte

parameters were within the reference values for the species. At least 50 % of the released animals survived after

one year, with recordings of reproductive events. Abiotic factors did not interfere with the animal visits to the

feeder. However, the variable humidity best explained visits in the morning, while the variables temperature and

luminosity most influenced visits in the afternoon.

Conclusion: The reintroduction observed and presented here is on the threshold of being classified as success-

ful. The installed feeders and artificial nests caused the animals to stay in the area for monitoring. Abiotic factors

may influence daily behavioral decision-making related to the use of supplementary feeding in reintroduced

parrots.

Key words: turquoise-fronted parrot; CETAS; monitoring post-release; food supplementation; seasonal

variation.

https://doi.org/ 10.15517/rev.biol.trop..v71i1.53145

CONSERVACIÓN

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

INTRODUCTION

Amazona aestiva (Linneaus, 1758), known

as the turquoise-fronted parrot, is a species of

Neotropical parrot widely distributed in eco-

systems in Brazil such as humid forests, caat-

inga, and cerrado (Sick, 2001). Although the

species is considered of “Near Threatened “ for

the risk of extinction (IUCN, 2018), the popula-

tion has been gradually decreasing due to habi-

tat loss and, mainly, by illegal trade (Schunck

et al., 2011). In Brazil, Amazon aestiva is one

of the psittacids that most often enter wildlife

screening centers (Destro et al., 2012; Schunck

et al., 2011). Therefore, decisions on how these

rescued animals are handled must be judicious,

while also ensuring their safe return to nature

(White Jr. et al., 2012).

Wildlife reintroductions are common con-

servation tools aimed at reestablishing popula-

tions of species within their historic geographic

range (Armstrong & Seddon, 2008; Fischer

& Lindenmeyer, 2000; Griffith et al., 1989;

White Jr. et al., 2012). Reintroduction proj-

ects of Amazona aestiva help determine the

destination of animals rescued from traffick-

ing and provide more accurate information on

procedures on this methodology, which can be

applied to the conservation of other threatened

species (de Azevedo et al., 2017; Silva et al.,

2021; White Jr. et al., 2012).

According to a systematic review that

evaluated 75 scientific studies on bird rein-

troductions and the threats to restoring these

populations, 13 factors had a negative impact

on these activities. The main factors were pre-

dation and unexpected dispersion of animals

(Destro et al., 2018).

A strategy used to ensure the fidelity of

reintroduced animals is supplementary feed-

ing with feeders and artificial nests placed

in the release areas (Tollington et al., 2013;

White Jr. et al., 2012). Long-term food sup-

plementation can help increase social inter-

actions and improve the integration of new

RESUMEN

Reintroducción y seguimiento del ave Amazona aestiva (Psittaciformes: Psittacidae) en Brasil.

Introducción: La reintroducción es un procedimiento utilizado para restablecer las poblaciones de animales

silvestres.

Objetivo: Evaluar el éxito de la reintroducción de Amazona aestiva e investigar si los factores abióticos (tempe-

ratura, humedad y luminosidad) interfieren en la búsqueda de la complementación alimenticia en los comederos

instalados en el área de liberación.

Métodos: Se iniciaron evaluaciones previas a la liberación con 59 Amazonas spp. Se realizaron pruebas de para-

sitología en heces, leucocitos, capacidad de vuelo y nivel de interacción animal-humano. En total, 33 animales

fueron seleccionados y enviados al área de liberación, que es una región de ecotono entre los biomas de la Mata

Atlántica y la Caatinga. Después de la liberación, se monitorearon durante un año las visitas a los comederos y

la supervivencia en el área. En estos períodos también se registraron factores abióticos.

Resultados: Las pruebas parasitológicas de huevos y parásitos en heces revelaron la presencia de Heterakis spp.

y Eimeira spp. Los parámetros leucocitarios estuvieron dentro de los valores de referencia para la especie. Al

menos el 50 % de los animales liberados sobrevivieron después de un año, con registros de eventos reproducti-

vos. Los factores abióticos no interfirieron con las visitas de los animales al comedero. Sin embargo, la variable

humedad explicó mejor las visitas por la mañana, mientras que las variables temperatura y luminosidad influye-

ron en la mayoría de las visitas por la tarde.

Conclusión: La reintroducción está en el umbral de ser clasificada como exitosa. Los comederos y nidos artifi-

ciales instalados provocaron que los animales permanecieran en el área para ser monitoreados. Los factores abió-

ticos pueden influir en la toma de decisiones de comportamiento diario relacionadas con el uso de alimentación

complementaria en loros reintroducidos.

Palabras clave: loro de frente turquesa; CETAS; seguimiento posterior a la liberación; complemento alimenticio;

variación estacional.

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birds reintroduced into previously established

flocks (Brightsmith et al., 2005; Elliott, 2006;

Lima et al., 2014; Paranhos et al., 2007;

Plair et al., 2008).

The characteristics and state of conserva-

tion of the environment, as well as climatic

conditions, can also influence the fidelity of

reintroduced animals. Physical environmental

factors define microclimates occupied by birds

and these microclimates affect energy balance

and water consumption and influence behaviors

(Bakken et al., 1991; Petit et al., 1985; Ryder,

1977; Wolf & Walsberg, 1996). Moreover,

the combination of these factors may affect

how reintroduced birds search for supplemen-

tary feeding and may influence the fidelity

of animals to the area. Therefore, it is critical

to understand how environmental factors can

interfere with the search for supplementary

feeding in feeders when managing areas des-

tined for reintroduction. This information can

help managers decide the best way to imple-

ment, maintain, and monitor feeders (Ewen et

al., 2015).

Supplementary feeding is associated with

many positive effects in various bird reintro-

duction projects (Brightsmith et al., 2005;

Vilarta et al., 2021). However, further research

is needed on the broader impacts of food supply

and factors such as climate, pathogen disper-

sal, and predation (Robb et al., 2008). Thus,

this study aimed to evaluate the reintroduction

success of a group of Amazona aestiva and

whether abiotic factors (temperature, humidity,

and luminosity) interfere in the daily search

dynamics for food supplementation in feeders.

The hypothesis is that animals may seek more

food supplementation in more unfavorable abi-

otic conditions for more distant foraging, such

as low light, temperature, and high humidity.

MATERIALS AND METHODS

Animal: At the beginning of this study

(January 2015), the Wildlife Screening Center

(Centro de Triagem de Animais Silvestres –

CETAS, in Portuguese) in Vitória da Conquis-

ta, housed 59 Amazonas spp. These animals

came mainly from illegal trade confiscations.

This study was submitted to and approved by

the Animal Ethics Committee of the Multidisci-

plinary Institute of Health of the Universidade

Federal da Bahia, under number 034/2015.

All 59 animals were initially tested to

detect gastrointestinal parasites. For this test,

fecal samples were randomly collected from

the floor of the enclosures according to the

number of birds. Stool parasitological tests

were performed using the direct method, the

Willis method, and the spontaneous sedimen-

tation method (Matos & Matos, 1988). Once

the endoparasites were identified, all birds

were subjected to therapeutic interventions

with piperazine citrate tetrahydrate, diluted

in water, for three consecutive days (Miranda

et al., 2014). New fecal samples were col-

lected to evaluate the effectiveness of treatment

after 20 days.

Soon after completing the first dose of

antiparasitic treatment, flight capacity was

evaluated only for animals of the species Ama-

zona aestiva, the focus of this study. This evalu-

ation was carried out using the methodology

proposed by Pedroso (2013), in which the flight

capacity of each animal is related to a score

ranging from 1-4, from animals that did not

fly to those that flew with constant rhythm and

height. Only animals with a score of three or

four had the flight capacity required to continue

in the reintroduction project.

The animals selected in the flight capacity

test were transferred to a single enclosure 4.15

m in length, 3.70 m in width, and 4.00 m in

height outside the CETAS building, near denser

vegetation, used to prepare animals for reintro-

duction. After three days of acclimatization,

the test of socialization/aversion to humans

was performed. Animals that showed aversion

to the approach of an unknown human offering

food were subsequently selected. The animals

that accepted the food were removed from the

enclosure and returned to the initial enclosures

(Pedroso, 2013; Ramos et al., 2021).

From the selected group, feces were col-

lected again from the enclosure to evaluate the

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

effectiveness of the treatment, as previously

described. Blood samples were also collected

to analyze hematological parameters (leuko-

gram) and for molecular sexing. The blood was

collected by cutting the claw to obtain a small

volume of blood (around 10 µl), according to

Echols (1999), Murray (1997), and Silva et

al. (2021). Blood smears were immediately

prepared by the sliding technique and Panoptic

fast staining to assess the leukocyte profile of

the animals (Guzman et al., 2008).

A drop of blood from each bird was

transferred to a filter paper for molecular sex-

ing using an optimized protocol described by

Griffiths (1998) and published by Barros et al.

(2017) to determine the ratio between released

males and females and support the reproduc-

tive monitoring of the established pairs. At

the time of blood collection, all animals were

individually clinically evaluated by a veterinar-

ian to detect clinical signs of any infectious

disease that was suggestive of further research

(Miranda et al., 2014).

Environmental physical and food enrich-

ment was used to support the social interaction

between individuals seeking group cohesion,

flight training, stimulation for the formation of

pairings, and to stimulate post-release foraging.

The enrichment was carried out in the CETAS

facilities for four months using tree branches,

hanging toys made with colored wood and

sisal rope, and whole fruits hanging or hidden

in boxes. Enrichment elements were changed

twice a week (Rupley & Simone-Freilicher,

2015; Simone-Freilicher & Rupley, 2015).

Each animal was identified with a num-

bered metal ring placed on the tarsus (Rings-

CETAS/UFBA + numbering) and by microchip

(electronic microchip, microchip-electronic tag

in the 12 mm mark) with individual numbers

inserted into the pectoral muscle of the animal

without impairing its flight capacity. In addi-

tion to these markings, the ventral region of

the animals was painted with non-toxic red

paint for easier identification in the wild, after

reintroduction (Raigoza-Figueras, 2014). To

facilitate distance identification, photographs

of the animals, specifically the phenotypic

characteristics of the head region, were taken

of each individual and included in a portfolio.

Study area: The area selected to receive

the animals is in the rural area of the munici-

pality of Condeuba, Bahia, Brazil, at an alti-

tude of approximately 634 m (14°53’43” S &

41°48’11” W). Condeuba has approximately

17 000 inhabitants and an area of 1 285.9 km²,

with a population density of 13.1 inhabitants

per km², according to the regional census

(Cidade-Brasil, 2016).

The area is characterized by vegetation

typically found in the transitional environment

of two biomes, that is, medium and large trees

such as Copaifera langsdorffii Desf. (Caesal-

pinioideae) in the Atlantic Forest and vegeta-

tion such as Anadenanthera macrocarpa in the

Caatinga (Benth.) (IBGE, 2016). According

to the European Centre for Medium-Range

Weather Forecasts (ECMWF), the highest

humidity (68.02 %) and rainfall (average of

132 mm) in the region is recorded in December.

In contrast, the lowest humidity, with 54.30

%, is recorded in September. November has

the highest number of rainy days (12.10 days),

while August is the dried month, with 1.63 days

and 6 mm. The average annual temperature in

Condeuba is 22.9 °C. The warmest month of

the year is February, with an average tempera-

ture of 24.5 °C. The lowest temperature of the

year is in July, with an average temperature of

20.2 °C. January has the most daily hours of

sunshine with an average of 8.17 hours. Aver-

age annual rainfall is 630 mm (climate-data.

org, 2022).

The release site includes a permanent pres-

ervation area of native forest with three sources

of a permanent river. One of the main criteria

used for choosing this area was its location,

as it is of difficult access and with few signs

of human activity, composed predominantly

of small farmers, and the state of forest pres-

ervation. Another important criterion was the

reports of older residents on the occurrence of

native populations of Amazona aestiva and the

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

identification by the CETAS team of other psit-

tacine species in the area, such as Eupsittula

cactorum and Eupsittula aurea.

To ensure the reintroduced animals remain

close to the chosen release area, they were

kept in installed nurseries for 10 days (Mitch-

ell et al., 2011). During this period, the par-

rots received fruits and seeds collected in the

locality, as well as sunflower seeds that were

routinely used for food during their captivity

in CETAS. The parrots received prophylactic

treatment to eliminate the risk of contamina-

tion by gastrointestinal parasites during their

transport to the reintroduction site. For this

treatment, mebendazole (Avitrin®, Coveli) was

used, in the dilution of 2.4 ml (containing 0.12

g of the active ingredient) in 1 l of water. The

dilution was left in the enclosure in a single col-

lective drinker freely accessed by the animals

for three consecutive days and changed daily.

The dilution was administered according to the

manufacturer’s guidelines.

Reintroduction: The animals were rein-

troduced using the soft-release method (Macias

et al., 2010). During release, the nurseries were

opened in the morning and the spontaneous exit

of the animals was monitored and recorded. At

the end of the day, the nurseries were closed

to prevent predators from entering at night. In

the morning in the following days, the animals

that had remained in the avian nursery were

identified and the doors were opened again (de

Oliveira et al., 2014; Silva et al., 2021). This

procedure was repeated for one month (the

period in which the enclosures remained in the

area), and animals that did not leave during the

period in which the doors remained open were

always identified.

After the nurseries were opened, the sup-

plementary diet of regional fruits and spo-

radic sunflower seeds (the same seeds offered

during the acclimatization period) was pro-

vided twice a day inside the nurseries and in

a feeder installed 5 m from the avian nursery.

In the study area, 12 artificial nests were also

installed to encourage reproduction, as per-

formed by White Jr. et al. (2005).

Monitoring: Monitoring was divided into

two stages, from May 2015 to May 2016. In

the first stage, the animals were evaluated for

18 consecutive days immediately after release,

while in the second stage, they were evalu-

ated for three to seven days at intervals of two

months, during a year, totaling six monitor-

ing campaigns. Monitoring was carried out at

dawn and in the late afternoon (for 2 hours

per period) to identify the animals around the

release site (in trees) and the animals feed-

ing in the feeders. When an animal was seen

feeding on native fruits scattered in the study

area, the plant species were also identified

(Silva et al., 2021).

The animals were identified through the

microchip reader or by detecting the ring

or phenotypic characteristics recorded in the

portfolio (Silva et al., 2021). Binoculars and

cameras were used to record the sightings (de

Almeida & de Almeida, 1998). In addition to

these monitoring stages, between the two daily

observations, the neighbors of the release site

were visited and questioned about the possible

presence of the reintroduced birds on their

properties.

To identify the paired animals, mutual

care behaviors such as beak to beak, cleaning

care, sleeping, and feeding close, and mov-

ing together in the departures and arrivals in

the monitored area were observed (Trillmich,

1976a; Trillmich, 1976b). Pairing was con-

sidered when the animals formed a pair for at

least two monitoring campaigns. Each installed

artificial nest was inspected during the cam-

paigns to identify possible occupations. Nests

that showed signs of occupation were identified

and photographed.

Abiotic factors were evaluated according

to the procedures established by Moura (2007)

in previous monitoring campaigns. The climatic

factors of temperature, humidity, and luminos-

ity were measured using a thermohygrometer

(EQUITHERM-TH-439) and luxmeter (UV-A

MAGNAFLUX). These factors were measured

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

on all animal monitoring days in all campaigns,

at two different times (8:00 h and 16:00 h). The

measurements were always carried out at the

same point, next to the feeder, from May 2015

to May 2016.

The success of reintroduction was evalu-

ated according to the recommendations of

White Jr. et al. (2012), where the survival of

reintroduced animals is evaluated after one

year and should be greater than 50 %, with the

reproduction of the reintroduced animals.

Some data related to abiotic factors were

not collected on the morning of the first day

of each monitoring campaign due to the arrival

time at the field. Thus, the missing values were

imputed with plausible data values using the

mice package. This package provides a method

for handling missing data, as the function cre-

ates multiple imputations (substitute values) for

multivariate missing data. The algorithm can

impute combinations of continuous categori-

cal, binary, unordered categorical, and ordered

categorical data (Van Buuren et al., 2019).

Data analysis: The values of each evalu-

ated health parameter, the ratio between males

and females, and the number of animals sighted

by monitoring campaign were tabulated and

analyzed through descriptive statistics (mean

± standard deviation) using GraphPad Prism®

version 5 software. The completed data table

(through the data imputation described above)

was used to perform principal component anal-

ysis (PCA) and verify how the abiotic data

relate to the frequency of visits to the feeder.

The paired t-test was used to verify pos-

sible differences between the periods (morning/

afternoon) considering the variables ‘frequency

of visits’, ‘temperature’, ‘humidity’, and ‘lumi-

nosity’. The data were distributed normally

only for temperature (afternoon) and humidity

(morning and afternoon). However, the t-test is

robust for non-normality, considering that there

are no outliers. The analyses were performed in

R software (R Core Team, 2020).

RESULTS

For the preparation of the animals selected

for the reintroduction project, fecal samples of

all 59 Amazonas spp., which were in the same

enclosure at CETAS, were evaluated for the

presence of gastrointestinal parasites.

To prepare the animals that were selected

for the reintroduction project, fecal samples

from all 59 Amazonas spp. in CETAS were

evaluated for the presence of gastrointestinal

parasites. Heterakis spp. and Eimeira spp. were

identified (Table 1). After treatment, a new

evaluation was carried out and no parasites

were found in the collected samples.

The species of Amazonas spp. in the

CETAS at the start of the study were (I) 48

Amazona aestiva, (II) 08 Amazona amazo-

nica, (III) 02 Amazona vinacea, and (VI) 01

Amazona rhodocorytha. Only animals of the

species Amazona aestiva (81.3 %) continued

to be evaluated and prepared for a group to

be reintroduced. This species was selected

because there were enough specimens to form

a more robust group and because it has already

been reported in the previously selected rein-

troduction area.

In the flight capacity evaluation of speci-

mens of A. aestiva, 72.9 % scored three or

four, which is compatible with reintroduction.

The rest of the animals (27.1 %) exhibited

some alteration that compromised their flight

capacity, mainly cut wing feathers, and were,

Table 1

Percentage of samples contaminated by the direct, Willis, and sedimented methods in fecal samples of Amazonas spp. from

CETAS - Vitória da Conquista, Bahia, before treatment.

Endoparasites Direct method (%) Willis method (%) Sedimented method (%)

Heterakis spp. 25.29 29.86 40.23

Eimeira spp. 9.20 14.94 17.79

Eimeira spp. / Heterakis spp 0 0 1.15

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

therefore, not prepared for reintroduction. Of

the 35 remaining animals, two were removed

for exhibiting high animal-human interaction.

Therefore, 33 animals had compatible flight

capacity for release and low interaction with

unknown humans since they did not allow the

approach of people.

Molecular sexing revealed a proportion of

69.69 % (23/33) of males and 30.30 % (10/33)

of females. For the leukocyte evaluation, all

animals had values within the expected param-

eters for the species (Table 2). The clinical eval-

uation did not identify any signs that indicated

the need to run complementary tests. Thus, all

33 animals previously selected continued in the

enclosure with environmental and food enrich-

ment to later be sent to the release area.

The avian nursery was opened at 11:30 h

and the first animal left at 13:32 h, soon after

which other animals accompanied the first

animal to perch and vocalize on nearby trees.

On the first day, 78.78 % of the animals left

the avian nursery, however, 18.18 % of those

that left returned to spend the night inside the

avian nursery. The doors of the avian nursery

were opened in the morning and closed in the

evening every day, for a month. In this period,

only one female animal did not leave the avian

nursery at any time and was returned to CETAS

with the withdrawal of the avian nursery. Thus,

32 animals remained in the release area and

were monitored for one year in campaigns

comprising 340 h of sampling effort and 204 h

of bird watching (Fig. 1).

The fidelity of the animals in the area,

using the feeder or the areas surrounding the

release site, allowed the identification of 50 %

(16/32) of the animals after one year of release

(Fig. 2). During monitoring, the reintroduced

animals fed on 10 native plant species in the

area (Table 3).

During the monitoring visits to the rural

owners near the release site, the team was

informed that a resident had trapped a project

animal in his home. This animal was rescued

and exhibited cut wing feathers, so it was

returned to CETAS, and environmental edu-

cation during the visits was intensified. In

addition, community members reported the

presence of wildlife hunters in the area (mainly

deer and armadillo hunters) and stated that with

the constant presence of the monitoring team,

the sounds coming from firearms used by these

people had decreased, suggesting that they

were hunting less frequently.

The formation of five pairs and two trios

of animals was identified. From these pairs, we

identified the occupation of two artificial nests

and one natural nest (occupied by a trio). Three

eggs were recorded in only one artificial nest.

However, the contents of the nest were predated

by a toucan. An individual of Ramphastos toco,

Table 2

Leukocyte values obtained for all samples of male and female individuals of the species Amazona aestiva pre-selected for

participation in the reintroduction project.

Hematological parameters

Mean and

standard deviation

(x 109 /l)

Minimum-

Maximum

(x 109 /l)

Mean and

standard deviation

(x 109 /l)

Minimum-

Maximum

(x 109 /l)

Males Females

Total Value of Leukocytes 8.843 ± 2.486 2.800-14.200 8.363 ± 3.625 0.196-12.000

Heterophil 4.690 ± 1.476 1.876-7.154 4.201 ± 2.072 0.196-7.068

Lymphocyte 3.486 ± 1.444 0.728-6.390 3.386 ± 1.794 0.196-6.000

Monocyte 0.466 ± 1.122 0.094-5.600 0.414 ± 0.374 0.120-1.298

Eosinophil 0.220 ± 147.73 0.062-0.612 0.234 ± 0.173 0.072-0.570

Basophil 0.207 ± 0.187 0.056-0.612 0.236 ± 0.197 0.084-0.570

Total Value of thrombocytes 1.0733 ± 2.600 5.600-14.700 10.659 ± 4.960 0.196-16.100

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

Statius Muller, 1776 (toco-toucan), a species

native to the area, was seen entering the nest,

which indicates that it fed on the parrot eggs

(Fig. 3). Two other artificial nests were occu-

pied by pairs of passerines Troglodytes muscu-

lus (Naumann, 1823).

The PCA results indicate that the two

main axes explained 74.17 % of the data varia-

tion. Axis one explained 54.91 % of the data

variation. Humidity was more associated with

the morning period, while temperature and

luminosity most influenced the frequency of

afternoon visits (Fig. 4).

There was a difference between the morn-

ing/afternoon periods for the variables: temper-

ature (t = -12.452, df = 33, P < 0.05), humidity

(t = 4.626, df = 33, P < 0.05), and luminosity (t

= -2.0803, df = 33, P < 0.05). However, this did

Fig. 1. Map of the State of Bahia. Highlighted in red for the municipality of Condeúba, the site selected to receive individuals

of the Amazona aestiva species. Individual of the species foraging in a feeder at the release site.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

not influence the frequency of visits between

the two periods (t = -1.8686, df = 33, P = 0.07)

(Fig. 5).

DISCUSSION

Reintroduction enables the reestablishment

of populations of different parrot species bred

for this purpose (Brightsmith et al., 2005;

Earnhardt et al., 2014; Smales et al., 2000)

or confiscated from illegal trafficking (Sanz

& Grajal, 1998; Silva et al., 2021). Therefore,

it is an important procedure to enable the

destination of psittacines rescued from illegal

wildlife trafficking.

Amazona aestiva was the most common

parrot species in the CETAS of Vitória da

Conquista, Bahia, with 81.3 %. This species is

the tenth most frequent among the birds that

entered the CETAS of Bahia between 2009

to 2019, with a total of 1 429 specimens (dos

Santos, 2021). These figures reveal the com-

plexity of the management and destination of

these animals. The most frequently observed

problem was the inability to fly due to cut

wing feathers that prevent the animals from

escaping illegal captivity. Cut wing feathers

have also been identified in other rehabilita-

tion centers for wild birds in Brazil (Fitorra et

al., 2021). Moreover, poor feather quality was

one of the physical abnormalities observed

in 36 % of 122 illegally trafficked parrots

in Costa Rica (Mora-Chavarría et al., 2017)

demonstrating the impact of this problem on

reintroduction projects.

In our study, after selecting the group of

animals suitable for reintroduction, a bias was

observed in the sex ratio of the animals, with a

higher number of males (69.69 %). Efforts to

Fig. 2. Demographic census of released parrots that

were visiting the feeder or present in the remediations

by monitoring campaign. The campaigns occurred as

follows: Campaign 1-May 2015 (18 monitoring days),

Campaign 2-June 2015 (seven monitoring days), Campaign

3-September 2015 (seven monitoring days), Campaign

4-December 2015 (five monitoring days), Campaign

5-March 2016 (three monitoring days) and Campaign

6-May 2016 (three monitoring days).

Table 3

Record of supplementary food offered at the feeder or by active search of the 32 individuals of Amazona aestiva after

reintroduction in Condeuba, Bahia

Supplemented foods Active search foods

Scientific name Popular name Scientific name Popular name

Musa sapientum Banana Plinia cauliflora Jabuticaba

Citrullus lanatus Melancia Citrullus lanatus Melancia

Carica papaya Mamão Eugenia uniflora Pitanga

Mangifera indica Manga Spondias purpurea Seriguela

Uncaria sp Unha-de-gato Morus sp. Amora

Helianthus annuus sunflower Copaifera langsdorffii Copaiba

Mangifera indica Manga

Uncaria sp. Unha-de-gato

Passiflora cincinnata Maracujá do mato

Psidium guajava Goiaba

10 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

Fig. 3. Photographic records of mating monitoring. A. pair of parrots (Ring-CETAS/UFBA 031 and CETAS/UFBA 024)

mating; B. eggs in the artificial nest; C. eggs predated by Ramphastos toco.

Fig. 4. Principal component analysis (PCA) to evaluate the influence of abiotic factors (temperature, humidity, and

luminosity) on animal visits to the feeder in Condeuba, Bahia.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

maintain a reintroduced bird population should

consider the sex ratio of the released animals

since the release of both sexes improves long-

term population consolidation (Lambertucci

et al., 2013). In contrast, the presence of more

males tends to increase the probability of

extinction of a group (Donald, 2007). There-

fore, the release of females should be a priority

in future reintroductions in this group.

Health assessments greatly minimize the

risks of releasing infected animals (Deem et al.,

2008; Jacobson et al., 1999). However, there is

no uniformity in the types of tests performed

in the different animal preparation protocols.

Efforts are needed to determine minimum

suggested procedures for the health screening

of candidates for reintroduction projects, espe-

cially when the high costs of testing hinder the

achievement of these projects (Saidenberg et

al., 2015). Hematological blood and parasito-

logical of feces parameters are complementary,

low-cost tests used in the routine monitoring

of animal health (del Pilar-Lanzarot et al.,

2001; Karesh et al., 1997; Melo et al., 2019).

In the present study, these analyses deter-

mined the necessary therapeutic interventions

to be performed in the group before they

were reintroduced.

The return to the natural habitat after a

period of captivity can sometimes be a stress-

or and reveal new challenges for individuals

(Parker et al., 2012). Thus, more attentive care

is required in the first stages of reintroduc-

tion for the adaptation period in the selected

environment. This stage consisted of a period

of recognition of the new environment while

still in captivity, as recommended by Jones

& Merton (2012) and tested for A. aestiva by

Silva et al. (2021). The next stage was to open

the nurseries using the soft release method

(Scott & Carpenter, 1987). Maintaining access

to the aviaries even after the animals left proved

Fig. 5. Evaluation between morning/afternoon periods. In A. frequency of visits to the feeder, in B. temperature differences,

in C. humidity, and in D. luminosity. The red dots are the raw data, the horizontal black line represents the mean, bean is the

density, and the rectangle is the confidence interval.

12 Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

critical for the parrots to gain confidence in the

new area, as it was observed that the parrots

returned to spend the night inside the nurseries

during the first days of freedom or some parrots

did not leave the aviary at any time of the day,

despite having gone through all the stages of

preparation. The return of the released animals

to the aviary was also monitored and identified

in other reintroduction projects of psittacids

(Silva et al., 2021; Vilarta et al., 2021).

To evaluate reintroduction success in par-

rots, White Jr. et al. (2012) proposed the

criterion of more than 50 % survival of ani-

mals released after one year. In the present

study, at least 50 % of the released animals

that remained in the monitored area survived.

Although one bird was captured by humans, no

deaths or predation of adults by other animals

was recorded. We believe that the other animals

dispersed beyond the monitored areas. Given

the uncertain fate of some individuals that leave

the monitored areas, it is impossible to attest

to the level of success of some reintroductions

of psittacids (Snyder et al., 1994; Vilarta et al.,

2021). Despite the impossibility of evaluating

success, dispersal can reveal a positive effect

since the population may have occupied new

areas (Vilarta et al., 2021).

Prolonged periods of feeder use with sup-

plementary feeding encourage the animals to

remain loyal to the release area (Brightsmith

et al., 2005; Vilarta, 2021) and facilitates post-

release data collection (Tollington et al., 2013).

The feeders used in the present study contrib-

uted to monitoring by providing the sighting

of at least half of the reintroduced animals

visiting the feeders or adjacent areas after one

year. Supplementary feeding, when not prop-

erly monitored, can be counterproductive and

cause unwanted effects such as the spread of

diseases, nutritional imbalances, or behavioral

changes, as in the case of increased fighting

and increased predation pressure (Robb et al.,

2008; White Jr., 2012), facts not observed in

the present study.

Supplementary feeding improves the

reproductive performance of birds (Pearson &

Husby, 2021) and reproduction is the second

criterion presented by White Jr. et al. (2012) to

evaluate the success of reintroduction. The fre-

quent monitoring of the reintroduced animals

allowed the observation and identification of

breeding pairs, mating, and egg-laying in the

first year of the study. The provision of arti-

ficial nests in reintroduction areas also favors

reproduction since it offers immediate nesting

opportunities (Tollington et al., 2013; Vilarta et

al., 2021; White Jr. et al., 2005). However, the

recorded eggs were predated by an individual

of Ramphastos toco, which is already known

as a potential predator of psittacine nests (Oren

& Novaes, 1986; Vilarta et al., 2021). Although

the nests used in this study were used by pairs

of A. aestiva, some nests were occupied by

non-target species. Therefore, the effectiveness

of artificial nests should be evaluated regularly

to ensure and adapt the conditions to favor the

target species (Gautschi et al., 2022).

The evaluation of the impact of abiotic fac-

tors on the visits to feeders in the morning and

afternoon showed that, despite the difference

between the periods for the variables: tempera-

ture, humidity, and luminosity, these factors did

not influence the animals in this regard. How-

ever, the variable humidity best explains morn-

ing visits, while the variables temperature and

luminosity had the greatest influence on visits

in the afternoon. Changes in local climatic

conditions lead to physiological adjustments in

the metabolism of these animals. Birds exhibit

adaptive physiological responses when faced

with climate change (Noakes et al., 2016).

Environmental temperature and humidity were

correlated with duration of daily activity in

Amazona amazonica and herons (Hirundo flu-

vicola and Ardea insignis), where the duration

of daily activity was positively correlated with

morning and evening temperatures and nega-

tively correlated with sunrise time and morning

and evening humidity (Khandu et al., 2022;

Moura et al., 2012; Singh et al., 2015).

The results of these past studies may help

to understand the pattern observed in the pres-

ent study, where on wetter days the animals

start their activities later, which may influence

more visits to feeders in the morning. On

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: e53145, enero-diciembre 2023 (Publicado May. 30, 2023)

warmer days, and with more light, the birds

start their foraging activities in more distant

areas earlier and only in the afternoon visit the

feeders when returning to maintenance areas.

This study confirms the reintroduction of

A. aestiva as a viable possibility for the destina-

tion of animals seized from wildlife trafficking

and the importance of monitoring for at least

one year to evaluate and ensure successful rein-

troduction. Furthermore, food supplementation

and the installation of artificial nests in the

release area favor monitoring and enable repro-

duction. We consider that these activities are

necessary to achieve the objective of reintro-

duction projects, which is the establishment of

viable populations and the consequent increase

in overall chances of survival and conservation

of the studied species.

Moreover, we consider that the reintroduc-

tion presented here is on the threshold of clas-

sification as successful since it was possible to

identify the survival of at least 50 % of the ani-

mals after one year of release and record repro-

duction events. In addition, the study presents

environmental clues as to how abiotic factors

may influence daily behavioral decision-mak-

ing related to the use of supplementary feeding

in reintroduced parrots. We suggest the evalu-

ation of the release of new groups of animals,

preferably formed by females, for population

reinvigoration. Moreover, further studies can

shed valuable light on how abiotic factors can

influence the behavioral dynamics of animals

reintroduced during climatic seasons.

Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We thank the veterinarians Aderbal Aze-

vedo Alves and Rosana Ferreira, the biologist

Giselle Góes, and the entire team of handlers at

CETAS Vitória da Conquista. We also thank the

students who assisted in the monitoring in the

field (Maíla Brandão Couto and Barbara Alves)

and the owner of the area. We thank CAPES

for the grant awarded to the second author and

CNPq for the productivity grant awarded to the

last author. To the State University of Santa

Cruz for the post-doctorate offered to Ricardo

Fraga and the postdoctoral fellowship offered

to Cleverson Zapelini.

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