Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

The role of neophobia in a pioneer olfactory enrichment

for amazons, macaws, and toucans

Mª Carmen Hernández1,2*; https://orcid.org/0000-0001-6918-6761

Isabel Barja1,3; https://orcid.org/0000-0002-8354-5342

1. Unidad Zoología, Departamento de Biología, Universidad Autónoma de Madrid, C/ Darwin 2, Campus Universitario

de Cantoblanco, 28049, Madrid, Spain; carmen.hdez.glez@gmail.com (*Correspondence)

2. Instituto de Investigación en Recursos Cinegéticos (IREC), CSIC-UCLM-JCCM, Ronda de Toledo 12, 13005, Ciudad

Real, Spain.

3. Centro de Investigación en Biodiversidad y Cambio Global (CIBC-UAM) Universidad Autónoma de Madrid, C.

Darwin 2, E-28049, Madrid, Spain; isabel.barja@uam.es

Received 17-IV-2023. Corrected 10-X-2023. Accepted 16-I-2024.

ABSTRACT

Introduction: Despite sensory enrichment being critical for ensuring the well–being of captive wild animals,

smells are not being included in enrichment protocols for birds. For this group, neophobia can be a problem

when it comes to implementing new enrichment devices.

Objective: To explore how participation in an olfactory enrichment and latency times varies between bird taxo-

nomic groups (Amazona spp. / Ara spp. / Ramphastos spp.).

Methods: We exposed 257 birds to a scent enrichment, and we recorded which individuals engaged with it and

the time they took to interact with it.

Results: We discovered that participation by toucans in the enrichment was higher compared to amazons and

macaws. Furthermore, latency time to interact with the enrichment was higher in amazons that in the other spe-

cies. Our findings could suggest that toucans are neophilic species which could benefit from higher exploration

rates. Amazons on the contrary seem to be particularly neophobic, possibly because of their less opportunistic

feeding habits compared to toucans and their higher vulnerability to predation compared to macaws.

Conclusion: These results point out that toucans would be more inclined to engage in environmental enrich-

ments, while a more natural design using smells inside familiar objects could be a more successful enrichment

for psittacids.

Key words: psittacine; ramphastids; captivity; animal welfare; rescue center; Costa Rica.

RESUMEN

El papel de la neofobia en un enriquecimiento olfativo pionero para guacamayos, loros y tucanes

Introducción: A pesar de que el enriquecimiento sensorial es fundamental para garantizar el bienestar de los ani-

males silvestres en cautiverio, los olores no son incluidos de forma rutinaria en los protocolos de enriquecimiento

para aves. Además, en el caso de estos animales, la neofobia puede ser un problema a la hora de implementar

nuevos dispositivos de enriquecimiento.

Objetivo: Explorar cómo varía la participación y la latencia en la interacción con un enriquecimiento olfativo

entre grupos taxonómicos de aves (Amazona spp. / Ara spp. / Ramphastos spp.).

Métodos: Expusimos a 257 aves a un enriquecimiento olfativo y registramos qué individuos participaron y el

tiempo que tardaron en interactuar con él.

https://doi.org/10.15517/rev.biol.trop..v72i1.54616

VERTEBRATE BIOLOGY

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

INTRODUCTION

Environmental enrichment can be defined

as any modification in the environment of

captive animals which improves their biologi-

cal functioning (Newberry, 1995). Enrichment

provides the opportunity to display a wider

range of adaptive behaviours and reduces the

frequency of abnormal ones, enhancing animal

welfare (Newberry, 1995; Young, 2013). There

exist a diverse variety of enrichment types:

nutritional, sensory, cognitive, social, physi-

cal features in their environment and so forth

(Newberry, 1995; Young, 2013). Particularly,

olfactory enrichment has been extensively used

in mammals (Wells, 2009), especially for felids

(Clark & King, 2008), but the importance of

the olfactory dimension for other taxa such

as reptiles and birds has been systematically

overlooked (Nielsen et al., 2015). Birds kept in

captivity often develop maladaptive conducts

such as spot picking, route tracing and feather

damaging behaviour (i.e. repetitive self-groom-

ing including picking, plucking or chewing on

feathers) (Brilot et al., 2009; Colton & Fraley,

2014; de Haas & van der Eijk, 2018; Jenkins,

2001; Mellor et al., 2018; Samson, 1996; van

Hoek & Ten-Cate, 1998), this last one being

particularly common in captive Psittaciformes

(Jenkins, 2001; Mellor et al., 2021). Psitta-

cine intellectual capacity appears to be similar

to great apes and marine mammals (Kalmar

et al., 2007; Krasheninnikova et al., 2019),

hence, captive Psittaciformes require high levels

of cognitive stimulation to prevent abnormal

behaviours (Kalmar et al., 2010; Mellor et al.,

2021; Rodriguez-Lopez, 2016). Although the

benefits of implementing enrichment for par-

rots has been extensively described in the litera-

ture (Kalmar et al., 2007; Lumeij & Hommers,

2008; Rodriguez-Lopez, 2016; Young, 2013), it

seems like routine enrichment for psittacines

is constrained to only two types: foraging and

physical modifications of their environment,

whereas sensory-based enrichment has been

neglected (Rodriguez-Lopez, 2016).

In the case of Ramphastids, there is a

concerning lack of research regarding which

types of enrichment they would benefit from,

with only one study evaluating the effects of

conspecific playbacks on a pair of Toco toucans

Ramphastos toco (O’Brien, 2006). Psittacines

and toucans are among the most common bird

groups kept in rescue and rehabilitation cen-

tres across Central America (Hernández pers.

obsv.). Thus, developing and implementing

new enrichments to ensure high quality welfare

standards must be a priority.

One challenge when it comes to design-

ing new enrichment techniques is neophobia

(Clark & King, 2008). Neophobia is described

as the innate aversion to novel stimuli (Green-

berg, 1990; Greenberg & Mettke-Hofmann,

2001). It is considered as an adaptive response

because engaging an unknown object, food or

location may entail being harmed or even killed

by a predator, competitor, or poisonous food

(Greenberg, 1990; Greenberg, 2003; Greenberg

& Mettke-Hofmann, 2001). However, neopho-

bia also carries disadvantages, as it prevents

individuals from interacting with potentially

new fitness-enhancing resources, obtaining less

Resultados: La participación en el enriquecimiento fue mayor en los tucanes en comparación con las amazonas

y los guacamayos. Además, el tiempo de latencia para interactuar con el enriquecimiento fue mayor en las ama-

zonas que en las otras especies. Nuestros hallazgos sugieren que los tucanes son especies neofílicas que podrían

beneficiarse de tasas de exploración más altas. Por otro lado, las amazonas parecen ser particularmente neofóbi-

cas, posiblemente debido a sus hábitos alimenticios menos oportunistas en comparación con los tucanes y a su

mayor vulnerabilidad a la depredación en comparación con los guacamayos.

Conclusión: Estos resultados señalan que los tucanes serían más proclives a participar en enriquecimientos

ambientales, mientras que un diseño que utilice olores dentro de objetos más naturales o familiares podría ser

más exitoso para las psitácidas.

Palabras clave: psitácidas; ranfástidos; cautiverio; bienestar animal; centro de rescate; Costa Rica.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

information, and losing the opportunity to

exploit new food sources or microhabitats.

Moreover, displaying a vigilant state can also

divert energy and time from other vital activi-

ties such as foraging or mating (Crane & Fer-

rari, 2017). Hence, there exists a clear trade-off

between the costs of displaying neophobia

and its benefits (Greenberg, 2003; Greenberg

& Mettke-Hofmann, 2001), and it is expected

that this behavioural trait varies across species

depending on their ecological particularities.

Neophobia may be advantageous in species

that inhabit high risk habitats or that exhibit

a narrow or specialised trophic niche, while it

could be detrimental for more generalist spe-

cies which could benefit from exploring unpre-

dictable and variable new resources (Brown

et al., 2013; Greenberg, 2003; Greenberg &

Mettke-Hofmann, 2001; Mettke-Hofmann et

al., 2002). Furthermore, for species living in

complex habitats, decreased neophobia would

entail higher exploratory rates, providing a sig-

nificant increase in acquired information which

can impact the individual fitness (Biondi et al.,

2010; Greenberg, 2003; Greenberg & Mettke-

Hofmann, 2001; Mettke-Hofmann et al., 2002).

However, it is also true that differences in neo-

phobia can also be found within individuals of

the same species, caused by previous experienc-

es or personality types (Ensminger & Westneat,

2012; Fox & Millam, 2004; Herborn et al., 2010;

Medina-García et al., 2017).

Therefore, the aim of this study was to eval-

uate differences in participation in an olfactory

enrichment depending on the taxonomic group

(Amazons Amazona / Macaws Ara / Toucans

Ramphastos), as well as comparing neopho-

bia response between them. Since neophobia

seems to be particularly pronounced for at least

some psittacine species (Mettke-Hofmann et

al., 2002; Van Horik, 2014; Wilson & Luescher,

2006), we predicted that toucans would show

a higher participation in the enrichment. In

parallel, we also expected that the mean latency

time to interact with the enrichment would be

lower in toucans due to psittacine tendency

towards neophobia.

MATERIALS AND METHODS

Study location and animals tested:

Research was conducted in five Costa Rica

wildlife rescue centers: The Toucan Rescue

Ranch, Centro de Rescate Las Pumas, Parque

Zoológico y Jardín Botánico Nacional Simón

Bolívar, Rescue Center Costa Rica, and Res-

cate Wildlife Rescue Center. The study was

performed with 73 red-lored amazons (Ama-

zona autumnalis), 101 yellow-naped amazons

(Amazona auropalliata), 52 scarlet macaws

(Ara macao), 11 great green macaws (Ara

ambiguus), 10 keel-billed toucans (Ramphas-

tos sulfuratus) and 10 yellow-throated toucans

(Ramphastos ambiguus) (Table 1). All indi-

viduals were adults, but sexes were unknown.

Most of the tested birds were non–releasable

animals because they were confiscated pets,

lacking key behaviours to survive in the wild.

Birds were held in communal aviaries, except

for the toucans that were kept individually or

in pairs. Enclosures were provided with natural

vegetation and perches. Environmental enrich-

ment was frequently provided by these centres,

for example wooden toys, wrapped food, for-

aging devices with berries and so forth. The

diet mainly consisted of fruits (banana, apple,

papaya, pineapple, watermelon, cantaloupe),

vegetables (carrot, broccoli, squash, celery, zuc-

chini), beans, corn, and sunflower seeds. Also

boiled eggs, pellets and worms were part of the

diet for the toucans.

All experiments were non-invasive and

based exclusively on behavioural tests in which

animals could decide whether to participate or

not. All applicable international, national, and/

or institutional guidelines for the care and use

of animals were followed. The experiments

were performed in accordance with the ethical

standards of each institution at which the stud-

ies were conducted, with Costa Rica animal

welfare law (Ley No. 7451. Ley del bienestar

de los animales, 1994) and with the Spanish

Government animal research legislation (Real

Decreto 53/2013, 2013).

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

Table 1

Detailed description of the enclosures in each centre and the number of individuals of each species held in each facility.

Center Size of the enclosure

(L × W × H, m)

Ara

macao

Ara

ambiguu

Amazona

autumnalis

Amazona

auropalliata

Ramphastos

sulfuratus

Ramphastos

ambiguus

Toucan Rescue Ranch 10 × 3 × 4 6

Toucan Rescue Ranch 10 × 4 × 4 10 13

Toucan Rescue Ranch 3 × 2 × 3 2

Toucan Rescue Ranch 5 × 3 × 3 2 3

Toucan Rescue Ranch 2 × 2 × 2 2 2

Toucan Rescue Ranch 2 × 2 × 2 4 2

Toucan Rescue Ranch 10 × 4 × 6 2 2

Toucan Rescue Ranch 10 × 4 × 6 2

Toucan Rescue Ranch 4 × 2 × 4 1

Toucan Rescue Ranch 5 × 3 × 4 1

Toucan Rescue Ranch 4 × 2 × 4 1

Toucan Rescue Ranch Release Site 10 × 4 × 4 11 4

Toucan Rescue Ranch Release Site 10 × 4 × 4 10 4

Toucan Rescue Ranch Release Site 4 × 2 × 4 2

Toucan Rescue Ranch Release Site 10 × 4 × 8 6

Las pumas 18 × 4 × 6 10 30

Las pumas 10 × 8 × 4 3 5 10

Las pumas 8 × 6 × 4 5 15

Las pumas 8 × 6 × 4 3

Simón Bolivar Zoo 4.5 × 3.5 × 2.5 3

Simón Bolivar Zoo 6 × 3 × 2.5 2

Simón Bolivar Zoo 3 × 3 × 2.5 4

Simón Bolivar Zoo 3 × 3 × 2.5 2

Simón Bolivar Zoo 3 × 3 × 2.5 1

“Rescate” Wildlife Rescue Center 8 × 6 × 6 10

“Rescate” Wildlife Rescue Center 6 × 3 × 4 1

“Rescate” Wildlife Rescue Center 8 × 6 × 6 7

Rescue Center Costa Rica 10 × 3 × 3 4 10 16

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

Experimental design and behavioral data

collection: Animals were exposed to an olfac-

tory enrichment consisting of closed plastic

containers (12 × 12 × 7 cm, all were opaque

yellow) with small holes to allow the odours to

come out following the Hernández et al., (2022)

protocol which confirmed that at least toucans

and macaws can discriminate between odours.

Three different odour choices were simultane-

ously presented to the birds: a) water, b) apple

vinegar, c) banana and papaya juice. Prelimi-

nary analyses showed that bird willingness to

participate in the enrichment and latency times

were not determined by the odour type, so

we analyse them together. We kept the three-

choice scent design because we demonstrated

that it was interesting for the birds. Once they

decide to engage with the enrichment, they

alternate interest in the containers depending

on what’s inside. Therefore, the neophobia/

neophilia tendency analysed in this study was

in response to the novel odour containers

rather than to the odour itself, whereas previ-

ous studies revealed that the odour is the deter-

minant of the total time they spend with each

container (Hernández et al., 2022). Treatments

consisted in eight cotton balls impregnated in

60 ml of one of each. The three plastic contain-

ers were placed in a random order inside the

enclosures separated by 50 cm (Fig. 1). After

installing the enrichment, the researcher left

the enclosure and initiated the video recording

of bird responses for 10 min. To establish com-

parable conditions, data collection was always

performed before bird breakfast (between 6:00-

8:00 h). Each enclosure was tested only once, to

avoid pseudoreplication due to the inability to

discriminate between individuals between vid-

eos (but we could discriminate between indi-

viduals within a video by following each bird

movements throughout the entire video record-

ing). Later, we analysed the video recordings to

Fig. 1. Schematic illustration of the experimental design: Three scents (water, vinegar, papaya and banana juice) were

simultaneously presented to the birds in separate plastic boxes. (Author: modified from Hernández et al., 2022).

6Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

the experiment and the latency. We considered

participation in the study as the physical con-

tact of the bird (touching any plastic container

with the beak or foot to explore it) with the

containers and we define latency as the delay

between the exposure to the enrichment and

bird physically interacting with it.

Statistical analysis: To evaluate differ-

ences in bird participation between taxonomic

groups (Amazona / Ara / Ramphastos), we

performed a contingency table analysis using

χ2 and Cramer’s V tests. Bird latency to interact

with the olfactory enrichment was analysed

using a Generalized Linear Mixed effect model

(GLMM), fitting normal distribution and iden-

tity link function. The response variable consid-

ered for the model was bird latency (s) (i.e. the

delay between putting the olfactory enrichment

in the enclosure and bird touching it) and we

included the taxonomic group (Genus) as fixed

factor (Amazona spp. / Ara spp. / Ramphastos

spp.). We also set the individual as random fac-

tor to control for possible differences in animal

personality traits. Preliminary analysis showed

that there were no differences in the participa-

tion and latency of the birds between centers, so

we did not include this variable in the models in

order to have greater statistical power.

Results were considered significant at α <

0.05. Data are represented as mean (s) ± stan-

dard error (SE). The software used to perform

the statistical analysis was SPSS 23.0 for Win-

dows (IBM Corp, 2015).

RESULTS

Bird participation: 257 birds were exposed

to the olfactory enrichment: 175 amazons Ama-

zona spp., 63 macaws Ara spp. and 19 toucans

Ramphastos spp. Of them, only 28 (16.00 %)

amazons Amazona spp., 12 macaws (19.04 %)

Ara spp. and 10 toucans (52.63 %) Ramphas-

tos spp. engaged in physical contact with the

enrichment. Data analyses showed that there

were differences in bird participation depend-

ing on the taxonomic group, with amazons and

macaws being much less inclined to interact

with the olfactory enrichment compared to

toucans (χ2 = 14.686, d.f. = 2, P = 0.001; Cra-

mer’s V = 0.239, P = 0.001, Fig. 2).

Bird latency time to interact with the

enrichment: for birds participating in the

enrichment, according to GLMM, the mean

latency time was higher (73.11 ± 17.88 s) in

amazons, Amazona spp., than for Ara spp.

(16.08 ± 5.60 s) or Ramphastos spp. (15.30 ±

Fig 2. Relationship between the number of individuals of each taxonomic group (Amazons Amazona spp. / Macaws Ara spp.

/ Toucans Ramphastos spp.) exposed to the olfactory enrichment and the number of individuals which participated in it: A.

Absolute numbers and B. Percentages.

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

6.85 s) (Table 2, Fig. 3). Furthermore, the indi-

vidual identity has influence as random factor

over the variance of latency response of the

birds (Table 2).

Table 2

Results of the GLMM analysing latency time (s) exhibited

by the birds which interacted with the olfactory enrichment

depending on the taxonomic group (Amazons Amazona

spp. / Macaws Ara spp. / Toucans Ramphastos spp.) and the

individual as random factor.

Factors F df P

Corrected model 3.814 47 0.029

Genus 3.814 47 0.029*

Individuala

aRandom factor. (Estimate = 2 657.30, SE = 1 097.14, Z–test

= 2.424, P = 0.015). *Genus Amazona (SE= 26.86; t = 2.152;

P = 0.037).

DISCUSSION

The results of this study showed that bird

participation in the olfactory enrichment was

determined by the taxonomic group. As we

expected, toucans engaged with the smell con-

tainers more frequently than amazons and

macaws. This finding indicates that toucans

are more prone towards neophilia compared

to psittacines. Keel-billed and yellow-throated

toucans have been traditionally considered gen-

eralist frugivores (Remsen et al., 1993), but they

are also opportunistic foragers which consume

invertebrate and vertebrate preys, eggs and even

carrion (Cove et al., 2016; Davlantes & Howe,

2018; Romero et al., 2022; Zúñiga-Ortiz, 2014).

Our results may suggest that keel-billed and

yellow-throated toucans are neophilic species,

since neophobia would be disadvantageous

for opportunistic species, as they would lose

chances to exploit unpredictable and unknown

resources. On the contrary, red-lored amazons,

yellow-naped amazons, scarlet macaws, and

great green macaws, are not omnivorous spe-

cies and only feed on seeds, fruits, flowers,

leaves and bark (Benavidez et al., 2018; Berg

et al., 2007; Vaughan et al., 2006; Volpe et

al., 2022), which may explain their tendency

towards neophobia. The main limitation of

this study was the fact that birds were kept in

different housing conditions and that we could

not control the possible influence of social

competition in the willingness of the birds

and the latency times showed to approach the

enrichment. Amazons and macaws are highly

social species which benefit from being kept in

communal aviaries (Seibert, 2006; van Zeeland

et al., 2009) while toucans are usually held

alone or in pairs because they are territorial,

Fig. 3. Mean latency time (s) exhibited by the birds which interacted with the olfactory enrichment depending on the

taxonomic group (Amazons Amazona spp. / Macaws Ara spp. / Toucans Ramphastos spp.).

8Revista de Biología Tropical, ISSN: 2215-2075 Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

especially during breeding season (Bor-Mikich

et al., 2008). It is probable that the hierarchy

among parrots could delay the interaction of

lower rank individuals with the scent contain-

ers. Consequently, further research is warrant-

ed to gain insight into how hierarchy influences

participation in this type of enrichment. In

large groups, we recommend including as many

enrichment containers as possible, to guarantee

that all individuals have access to it. In this

regard, further research would be needed, test-

ing animal responses individually to further

verify our results.

Regarding the differences found in mean

latency time, we found the delay to interacting

with the olfactory enrichment was significantly

higher in amazons than in macaws and toucans.

These results suggest that amazons are particu-

larly cautious when it comes to exploring new

objects in comparison to macaws and toucans.

This finding can be also linked to a neophobic

tendency in red-lored amazons and yellow-

naped amazons, explained by their life-history

traits. As we mentioned above, amazons do not

prey on other animals nor opportunistically

consume eggs or carrion as toucans do. More-

over, amazons are much smaller psittacines

than macaws so they may be easier to prey

upon, whereas macaws’ predators mainly affect

the nest (Fraixedas et al., 2014; Schruhl et al.,

2012). This could entail that unknown settings

are riskier for amazons than for macaws, so

they would benefit from a neophobic approach.

Moreover, it is also important to highlight

that there were individual differences in the

latency time. As previously described in the

literature, personality and previous experiences

can affect neophobia responses (Ensminger &

Westneat, 2012; Fox & Millam, 2004; Herborn

et al., 2010; Medina-García et al., 2017). There-

fore, each bird response to the enrichment was

not only determined by the taxonomic group,

but probably also by personality types and

the reason why they came to the rescue cen-

tres. Many birds were confiscated because they

were pets while others were born and raised

in the wild but suffered from injuries or other

health problems. Future studies could focus on

evaluating differences in personality traits and

neophobic behaviour depending on the animal

background history.

We found that participation success was

higher in toucans than in amazons and macaws

possibly because of a lesser neophobic reac-

tion to the containers. Red-lored amazons and

yellow-naped amazons seemed to be particu-

larly neophobic species, showing higher latency

times to interact with the enrichment, prob-

ably due to their life-history attributes. Our

results indicate that the container determined

the neophobic/neophilic response, whereas the

odour inside would determine the time spend

which each container (Hernández et al., 2022).

We also highlight that keel-billed and yellow-

throated toucans are highly participative in

environmental enrichments, so it would be

of relevance to routinely include this kind of

enrichment in captivity welfare plans. In the

case of amazons and macaws, they seem to

be more cautious so it may be more success-

ful to present odours in natural containers or

to apply them on features in their enclosure.

Finally, the next step would be to evaluate if

this kind of enrichment produces differences

in bird conduct (more desirable behaviours

and less stereotypies) and in the physiological

stress response, to properly assess its impact on

animal welfare.

Ethical statement: the authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict 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 acknowledgments sec-

tion. A signed document has been filed in the

journal archives.

ACKOWLEDGMENTS

We wish to thank all the centres that have

kindly allowed us to conduct the experiments

in their facilities: The Toucan Rescue Ranch,

Centro Rescate Las Pumas, Parque Zoológico

y Jardín Botánico Nacional Simón Bolívar,

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 72: e54616, enero-diciembre 2024 (Publicado Ene. 23, 2024)

Rescue Center Costa Rica and Rescate Wildlife

Rescue Center.

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