ISSN 2477-9458
BOLETÍN DEL
CENTRO DE
INVESTIGACIONES
BIOLÓGICAS
TASAS DE FAGOCITOSIS EN LAS ESPECIES DE ACANTHAMOEBA PROVENIENTES
DE AGUAS SUBTERRÁNEAS. PARTE I.
Silvana B. Pertuz Belloso, Deyamira Matuz Mares, Emelia Campoy,
Miroslav Macek y Elizabeth Ramírez Flores................................................
CLASIFICACIÓN DE NUEVOS MICROHÁBITATS DE AGUA SALOBRE EN VENEZUELA.
CONSIDERACIONES BIOECOLÓGICAS SOBRE LAS ESPECIES DE INSECTOS
ACUÁTICOS EN LA PENÍNSULA DE ARAYA.
Erickxander Jiménez-Ramos, Mauricio García y Vanessa Acosta.................
EATING THE FORBIDDEN FRUIT? AVOCADO CONSUMPTION BY NEOTROPICALES
AT AN URBAN GARDEN.
Andrés E. Seijas...............................................................................................
MICROMOLUSCOS DEL CONTENIDO ESTOMACAL DE ASTEROIDEOS DEL GÉNERO
ASTROPECTEN: ORIGEN DE UNA COLECCIÓN DE REFERENCIA.
Ricardo Bitter-Soto y Ronald Rivas-Suarez................................................
INSTRUCCIONES A LOS AUTORES............................................................................
INSTRUCTIONS FOR AUTHORS..................................................................................
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UNA REVISTA INTERNACIONAL DE BIOLOGÍA
PUBLICADA POR LA
UNIVERSIDAD DEL ZULIA, MARACAIBO,
VENEZUELA
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57
70
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Boletín del Centro de Investigaciones Biológicas
Vol. 55. Nº 1, Enero- Junio 2021, Pp. 57-69
57
EATING THE FORBIDDEN FRUIT? AVOCADO CONSUMPTION BY NEOTROPICAL
BIRDS AT AN URBAN GARDEN.
ANDRÉS E. SEIJAS
Universidad Nacional Experimental de los Llanos Occidentales “Ezequiel Zamora”,
Guanare, Venezuela. aeseijas@gmail.com
ABSTRACT
The consumption of fruits by birds that visited a feeder in an urban garden in
Guanare, Venezuela, was evaluated. There was an emphasis in the analysis of the
consumption of avocado (Persea americana) whose fruit, leaves and seed have been
found to be toxic for some animals. The number of visits to the feeder of each species
was counted. The time spent in the consumption of each fruit type was calculated
prorating the duration of every visit according to the number of pecks in each one of
them. In a first trial, avocado, papaya, plantain, banana, and mango were offered
simultaneously. Birds of the Turdidae family (Turdus leucomelas and T. nudigenis)
consumed exclusively avocado, while Sicalis flaveola and Thraupis episcopus
preferred mango and plantain, respectively. In a second trial, Musaceae fruits
(plantain or banana) and avocado were offered. Of the total time devoted to the
consumption of avocado, 80% belonged to only three species: the two thrushes and
the Red-crowned Woodpecker (Melanerpes rubricapillus). The other species either
did not consume avocado or consumed Musaceae fruits during a high percentage of
their time at the feeder, as was the case of T. episcopus (92.2%), Mimus gilvus
(87.8%), Cacicus cela (97.9%), Psarocolius decumanus (92.9%) and Euphonia
laniirostris (83.1%) It is the first time that the consumption of the P. americana fruit
has been evaluated in Neotropical birds. The non-preference (or rejection) of some
birds for avocado deserves to be investigated in more detail.
Key words: Avocado; Persea americana; birds; fruit selection; feeder; urban.
Avocado consumption by Neotropical birds.
Andrés Seijas.
58
¿COMIENDO LA FRUTA PROHIBIDA? CONSUMO DE AGUACATE POR AVES
NEOTROPICALES EN UN COMEDERO DE UN JARDÍN URBANO.
RESUMEN
Se evaluó el consumo de frutas por parte de animales silvestres que visitaron un
comedero en un jardín urbano de Guanare, Venezuela, con énfasis en el análisis del
consumo de aguacate (Persea americana) cuya fruta, hojas y semilla han sido
señaladas como tóxicas para algunos animales.
Para cada especie se cuantificó el
número de visitas al comedero. Se calculó el tiempo empleado en el consumo de
cada fruta prorrateando el tiempo total de la visita de acuerdo al número de
picoteos en cada una de ellas. En una primera prueba se ofreció simultáneamente
aguacate, papaya, plátano, y mango. Las aves de la familia Turdidae (Turdus
leucomelas y T. nudigenis) consumieron exclusivamente aguacate, mientras que
Sicalis flaveola y Thraupis episcopus prefirieron mango y musáceas (plátano o
banana), respectivamente. En una segunda prueba se ofreció solo musáceas y
aguacate. Del total del tiempo dedicado por todas las especies al consumo del
aguacate, 80% correspondió a solo tres especies: los dos Turdidae y Melanerpes
rubricapillus. Las otras especies o bien no consumieron aguacate o consumieron
frutos de Musaceae en un alto porcentaje de sus tiempos en el comedero, como
fue el caso de T. episcopus (92.2%), Mimus gilvus (87.8%), Cacicus cela
(97.9%), Psarocolius decumanus (92,9%) y Euphonia laniirostris (83.1%). Es la
primera vez que se evalúa el consumo del fruto P. americana en aves
neotropicales. La no preferencia (o rechazo) de algunas aves por el aguacate
merece ser investigado con más detalle.
Palabras clave
: Aguacate; Persea americana; aves; selección de frutas;
comedero; urbano.
Recibido / Received: 0
2-02-2021 ~
Aceptado / Accepted:
05-04-2021.
INTRODUCTION
The investigations carried out in Latin American countries on the fauna that
visit feeders are scarce. The main goals of the few papers that have been found
were to test some ecological theories about behavior, such as neophobia (aversive
responses no novel stimuli) by some birds (Echeverria et al. 2006, Echeverría and
Boletín del Centro de Investigaciones Biológicas
Vol. 55. Nº 1, Enero- Junio 2021, Pp. 57-69
59
Vasallo 2008), the interactions and hierarchies established among birds that access to
the feeder (Levín et al. 2000; Sainz-Borgo 2017), or the possible anti-predatory
function of the grouping of certain species when accessing to the feeder (Sainz-Borgo
and Levín 2012). The food offered in all these studies has been very varied and in no
case has food preference been the object of analysis.
Since 2005, informal notes began to be taken on the preferences of animals for the
fruits or fruit remains offered in feeders placed in the same garden where the present
investigation took place. Preliminary analyzes of these observations have already
been published (Seijas and Seijas-Falkenhagen 2020a). It should be noted that
whenever pieces of avocado (Persea americana) were placed in the feeder, only birds
of the Turdidae family (Turdus leucomelas and T. nudigenis) seemed to be interested
in that fruit.
In the search for bibliographical references on avocado consumption by
wildlife, it was found that the scarce available literature accounts mostly on the
toxicity of the leaves, bark, seeds and even the ripe fruit of P. americana for
various domestic or captive animals, as will be discussed later. A few references
were found on the consumption of avocado by wild animals. Hardy (1973), for
example, mentioned having received information that the Canary-winged
parakeet Brotogeris versicolurus (a species native to South America) feeds on the
fruits of this tree and Clark (1976) indicated that the House finch (Carpodacus
mexicanus) has been identified as causing damage to immature fruits of P.
americana. Verea et al. (2016) reported that the thrushes Turdus leucomelas and
T. nudigenis consume avocado fruits in orchards of that plant.
The objective of this study is to evaluate the consumption of fruits by birds that
visit a feeder. Even though in the trials carried out various types of fruits were
offered, the study focuses on avocado consumption, considering that given the
toxicity demonstrated by different parts of this plant in some animals, feeding on
its fruit constitutes a novelty that deserves to be highlighted.
MATERIALS AND METHODS.
The study was carried out in the garden of a house on the outer edge of the city of
Guanare, Portuguesa state, Venezuela. Details on the characteristics of this garden
Avocado consumption by Neotropical birds.
Andrés Seijas.
60
and the feeder are found in Seijas and Seijas-Falkenhagen (2020a, b). The feeder used
to attract the animals consisted of a square cement block (40cmx40cm and 5 cm
thick) placed at ground level. On the surface of this block, pieces of selected fruits
were placed and covered with a mesh (5x5) of plastic-covered wires. The mesh
prevented the animals from taking away or turning around the food, and also served
as a perch for the birds when accessing the food. The activities of the animals were
recorded on video with a cell phone placed on a tripod at a height of 30 cm and 70 cm
away from the feeder. The storage capacity on the phone card (3.6 MB) limited the
duration of the recorded videos. For each sampling day, the first recording started at
sunrise. Before every new recording, if necessary, the pieces of fruits were
replenished to ensure the offer of each type of fruit was ad libitum. For each species,
the number of visits per recording hour (v/h) and the time at the feeder (in minutes)
per recording hour (min/h) were calculated. The time spent consuming each fruit
piece was estimated prorating the total time of the visit according to the number of
pecks in each one of them.
Two trials were carried out. In the first one, on May 20, 2020, pieces of four
fruits were offered simultaneously: mango (Mangifera indica), papaya (Carica
papaya), plantain (Musa paradisiaca) and avocado (Persea americana). Pieces of
each of them were placed in a different corner of the feeder. Six recordings of 9 ±
0.68 minutes were made with approximately 15 minutes in between, so the time
elapsed between the beginning of the first recording and the end of the last one
was just over two hours. Preliminary analysis of this first trial seemed to indicate
a rejection by some bird species to feed on avocado. Thus, a second trial was
performed where pieces of a Musaceae (most frequently plantain, but
occasionally Musa sapientum) and avocado were offered to the animals. Plantain
was selected to contrast with avocado, since in previous studies this fruit always
turned out to be preferred by birds. During five consecutive days (December 21
to 25, 2020), four or five video-recordings were made with an average duration
of
10.3 minutes, for a mean duration of daily recordings of 47.3 minutes. A piece
of Musaceae was placed in one corner of the feeder, in another corner a piece of
avocado and, in a third one, pieces of these two fruits were placed close to each
other, although not in contact. Each day of recording, the arrangement of the
fruits was varied, to reduce a possible bias in the selection of the animals due to
the location of the pieces in the feeder. With this second trial, it was expected to
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determine not only that some animals did not consume avocado, but that they visited
less the piece of Musaceae that was next to the avocado, which would be taken as an
indication of rejection of that fruit.
Two-sample paired tests (Wilcoxon) were performed to determine the significance
of the differences in times used by each species in the consumption of pairs of fruit
offered simultaneously. Statistical analyzes were carried out with the open access
program Past 4.02 (Hammer et al. 2001, Hammer 2020).
RESULTS
Sixteen species of birds visited the feeder during the two trials; only nine of them
in the first trial and thirteen in the second (Table 1).
Table 1. Number of visits to the feeder and total time spend consuming fruits (in
seconds) by the different bird species. Total recording time of each trial, in hours, is
indicated within brackets. Only visits in which birds pecked any of the fruit pieces
at least once were used for calculations of Time (min/hour).
Four fruits [0.90h]
Avocado & plantain [3.94h]
Families and species
Visits(*)
Time
(s)
min/hour
Visits(*)
Time (s)
min/hour
Fringillidae
Euphonia laniirostris
-
-
-
42(29)
525
2.2
Icteridae
Cacicus cela
-
-
-
17(16)
580
2.5
Psarocolius decumanus
-
-
-
17(13)
386
1.6
Mimidae
Mimus gilvus
-
-
-
46(38)
1948
8.2
Picidae
Melanerpes
rubricapillus
-
-
-
17(15)
968
4.1
Thraupidae
Ramphocelus carbo
4(4)
140
2.6
-
-
-
Avocado consumption by Neotropical birds.
62 Andrés Seijas.
Continuación Tabla 1.
Saltator coerulescens
-
-
-
8(5)
81
0.3
Sicalis flaveola
20(19)
609
11.3
-
-
-
Sporophila intermedia
8(6)
217
4.0
-
-
-
Stilpnia cayana
5(3)
55
1.0
23(17)
137
0.6
Thraupis episcopus
18(16)
375
6.9
613(398)
4519
19.1
Thraupis palmarum
3(3)
109
2
17(10)
71
0.3
Troglodytidae
Campylorhynchus
nuchalis
2(2)
56
1
1(0)
-
-
Turdidae
Turdus leucomelas
18(17)
511
9.5
318(243)
5081
21.5
Turdus nudigenis
6(4)
48
0.9
22(15)
336
1.4
*Visits in which birds pecked any of the fruit pieces at least once.
In the first trial, the mango pieces were the ones where birds spent most of
their consuming time (37%), followed, in decreasing order, by papaya (23.9%),
avocado (20.1%) and plantain (19.1%). The preeminence of mango over other
fruits was due to the time spent by the Saffron Finch (Sicalis flaveola) and, to a
lesser extent, by the Gray Seedeater (Sporophila intermedia) on its consumption.
These two birds were also the ones that spent the most time consuming papaya.
Given the short duration of the trial, the number of visits by some birds was too
low for statistical analysis. Most of the species consumed at least two fruits, but
the Turdidae (Turdus leucomelas and T. nudigenis) were the only ones to
consume avocado (Fig. 1). These two thrushes spent 76.0% of the time in their 21
visits to the feeder consuming that fruit. The Saffron Finch, in 19 visits to the
feeder, consumed mainly mango (73.2%) instead of papaya. Finally, the Blue-
gray Tanager (Thraupis episcopus, n = 16) spent 72.8% of its time to the
consumption of plantain.
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Vol. 55. Nº 1, Enero- Junio 2021, Pp. 57-69
63
Figure 1
. Cumulative time at the feeder of each species feeding on the
fruits offered. The species included in “Others” are Ramphocelus carbo,
Thraupis palmarum; Stilpnia cayana and Campylorhynchus nuchalis.
The second trial, in which pieces of plantain (or occasionally banana) and
avocado were offered, was carried out seven months after the first one, and with a
recording effort 4.4 times greater. The location and arrangement of the fruit
pieces was not found to influence the frequency of visits by the animals, and
would not be considered from here on. In this trial, even though there was a
preference for the consumption of Musaceae, animals other than the thrushes feed
also on the avocado. The Blue-gray Tanager (92.2%), the Tropical Mockingbird
(Mimus gilvus, 87.7%), the Yellow-rumped Cacique (Cacicus cela, 97.9%), the
Crested Oropendola (Psarocolius decumanus, 92.6%) and the Thick-billed
Euphonia (Euphonia laniirostris, 83.1%) showed a clear preference for Musaceae
(Fig. 2). To this group favoring Musaceae we can add species that visited the
feeder with relative low frequency and were not included in Fig. 2. That was the
case of the Grayish Saltator (Saltator coerulescens), the Burnished-buff Tanager
(Stilpnia cayana) and the Palm Tanager (Thraupis palmarum). The first one
never ate avocado in its eight visits, while S. cayana only pecked that fruit once
(in 23 visits) and T. palmarum pecked it twice (in 17 visits).
Avocado consumption by Neotropical birds.
64 Andrés Seijas.
Figure 2
. Time spent consuming plantain or avocado by the different bird
species.
The thrushes and the Red-crowned Woodpecker (Melanerpes rubricapillus)
accounted for 80% of the total time dedicated to the consumption of avocado by
all visitors. However, with the exception of T. nudigenis, these species consumed
plantain in a higher proportion than avocado, although in any case the differences
were statistically significant (Wilcoxon paired tests, P> 0.17
or greater). A
species not included in this study that also visited the feeder was the Red-tailed
Squirrel (Sciurus granatensis) which consumed mainly plantain (55% of the time
at the feeder).
DISCUSSION
To highlight the courage and bravery of someone, there is a saying in
Venezuela that expresses: “he [or she] is braver than the person who ate the first
avocado” which refers to how risky it seems to be to consume a fruit that never
loses its color green (in the most common varieties in Venezuela) and that,
Boletín del Centro de Investigaciones Biológicas
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65
supposedly, wild animals do not eat. The fear that the avocado fruit could be
poisonous, as the aforementioned saying implies, seems to have some basis,
although there is no evidence that humans are in danger after its consumption. On
the contrary, its high content in calories, proteins, fatty acids and vitamins
(Burger 1994; Borchert et al. 2008; Gouegni and Abubakar 2013) has made it a
highly appreciated fruit whose cultivation has spread throughout the world.
However, the leaves, bark, immature fruits, and seed of P. americana have been
identified as toxic for various animals, such as laboratory mice, rabbits, cattle,
goats, horses, and ostriches (McKenzie and Brown 1991, Buoro et al. 1994,
Burguer et al. 1994, Padilla-Camberos et al. 2013). The toxicity of ripe fruit has
also been demonstrated for cage birds such as Australian parakeets (Budgerigar,
Melopsittacus undulatus; Cockatiel, Nymphicus hollandicus) and canaries
(Serinus canaria) (Hargis et al. 1989). These cases of poisoning have turned
avocado into a kind of “forbidden fruit” that, in the opinion of Kovalkovicova et
al. (2009) “Feeding avocados to any non-human animal should be completely
avoided”.
Not all varieties of avocados have been shown to be toxic to wildlife and one
native to Guatemala seems to have the strongest effects (Burger et al. 1994,
Hargis et al. 1989). The variety of avocado used in the present research is not
known, but it was probably a local variety, or a hybrid between the many varieties
that have been developed over the years.
Isolated avocado trees planted in family gardens offer few opportunities for
birds and other animals to consume its fruits. Fruits remain green on the tree and
ripen only after they have been harvested. It is a highly valued and expensive
fruit, and it is not usually offered to animals. Even in commercial plantations of
P. americana, at least in Venezuela, the consumption by animals of fruits that
ripen as they fall from trees has gone unnoticed, if we take into account that
Verea et al. (2011) did not mention in their research in an avocado orchard,
whether or not any of the birds
they observed ate the fruits of that tree. However,
Borchert et al. (2008) showed that in orchards of P. Americana in California
(USA), avocado fruits is consumed by various species of mammals (bears,
domestic dogs, coyotes, squirrels and other wild animals) but not by birds.
The consumption of avocado by Neotropical wild birds is for the first time
evaluated
in the present study. Birds of the family Turdidae (thrushes) were the
Avocado consumption by Neotropical birds.
66 Andrés Seijas.
ones that showed the highest consumption of avocado, which confirms
preliminary observations in Seijas and Seijas- Falkenhagen (2020a). It was rather
surprising to observe the consumption of avocado by Red- crowned woodpeckers
and by Red-tailed squirrels, animals that had never been observed eating this
fruit. Some other species of birds also pecked the pieces of avocado supplied, but
seemingly, consumption was always low (if there was any) since in many
occasions birds (especially T. episcopus) were observed to shake their beaks as if
to get rid of the collected portion. A case that is worth highlighting is that of the
Burnished-buff Tanager, a species that only pecked on the avocado once in its 28
visits to the feeder (taking the two trials together). This species, in a previous
study (Seijas and Seijas-Falkenhagen 2020b), was regarded as the most generalist
of all the birds visiting the feeder, since it never showed a preference for any of
the pairs of fruits that were offered, which included papaya, plantain, banana and
mango, so avoiding avocado consumption may be interpreted as a rejection of
that fruit.
The Saffron Finch and the Gray Seedeater only went down to the feeder when
mangoes were offered, as had happened in previous trials carried out in mid-May
2020 (Seijas and Seijas- Falkenhagen 2020b) even though these species are
observed in the garden throughout the year. The Blue-gray Tanager, for its part,
confirmed its preference for Musaceae fruits, as had been shown in the cited
article.
No strange behavior was observed in the animals that ate avocado repeatedly
(thrushes, woodpeckers and squirrels) during the five days that the videos of the
second trial were recorded. The negative effects described for some species that
have consumed this fruit manifest themselves in a matter of a few hours (Hargis
et al. 1989, Kovalkovicova et al. 2009). The animals that came to the feeder were
not marked, but a few birds had physical features that allowed them to be
individualized. This is the case of a Blue-gray Tanager with only one leg, another
with a deformed neck; a Tropical Mockingbird with a partially broken beak, and a
Thickbilled Euphonia with a scar on its chest. All of them pecked the avocado at
least once and were still observed in the feeder weeks after the samplings.
The animals that consume avocado without ostensible consequences, including
those in the present study, are original from the American continents, while those
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Vol. 55. Nº 1, Enero- Junio 2021, Pp. 57-69
67
that have been mentioned in the literature (horses, goats, mice, rabbits, ostriches,
Australian Psittacines and others) as affected by the consumption of some part of
the P. americana tree, are original from other continents. It is beyond the scope of
this study to investigate whether this is merely a coincidence. The apparent
rejection or non-preference of some birds to avocado deserves to be investigated
in more detail. Many chemical compounds have been found in the avocado fruit
(Bhuyan et al. 2019) and the role they play in defining preferences for
consumption by birds and other animals is worth investigating.
The present investigation is based on samplings carried out in two short
periods with a separation of several months between them. One could speculate
on the effect that this fact may have had on the results. Although it is necessary to
carry out more samplings, the results in previous publications (Seijas and Seijas-
Falkenhagen 2020a,b) and data that are still being processed for the rainy season,
seem to indicate that even though the frequency of visits to the feeder by each
bird species may vary over time, their preferences per fruit type do not change.
It must be mentioned that this research is part of a project with samplings
carried out over a whole year. In the published works, the preferences of the birds
for the different fruits offered in the feeder and the interactions established among
them have been analyzed. New publications could complement the findings of
those already published. The information collected throughout the articles that
emerge will allow planning new studies aimed at laying the foundations for the
management of these feeders, in such a way that they better fulfill the objective of
conserving and enhancing the wildlife of urban environments.
ACKNOWLEDGEMENTS
Jorge Seijas-Méndez helped with the search for some of the articles cited in the
bibliography. Lemnie Falkenhagen, Sara and Andrés Seijas-Falkenhagen made
valuable observations on an early version of the manuscript. Three anonymous
reviewers made significant observations and recommendations that helped to
improve this paper.
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