Environmental Pollution 317 (2023) 120742

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

High incidence of plastic debris in Andean condors from remote areas:

Evidence for marine-terrestrial trophic transfer
Víctor Gamarra-Toledo a, b, *, Pablo I. Plaza b, Yuri A. Peña a, Pierina A. Bermejo c, Juan López d,
Gonzalo L. Cano a, Santiago Barreto a, Sandra Cáceres-Medina a, Sergio A. Lambertucci b
a
Área de Ornitología, Colección Científica, Museo de Historia Natural (MUSA), Universidad Nacional de San Agustín de Arequipa, Av. Alcides Carrión s/n, Arequipa,
Peru
b
Grupo de Investigaciones en Biología de la Conservación, Laboratorio Ecotono, INIBIOMA, Universidad Nacional del Comahue - CONICET, Quintral 1250, R8400FRF,
San Carlos de Bariloche, Argentina
c
Asociación de Guías Oficiales y Profesionales de Turismo de la Región Arequipa (ADEGOPA), Calle Palacio Viejo Nº 216, interior 301, Arequipa, Peru
d
Reserva Nacional Pampa Galeras Bárbara D’Achille, Servicio Nacional de Áreas Naturales Protegidas por el Estado (SERNANP), Av. Circunvalación s/n - Pasaje
Bisambra, Interior 15, Ica, Nazca, Peru

A R T I C L E I N F O A B S T R A C T

Keywords: Plastic pollution is an alarming environmental problem affecting diverse species worldwide. Scavenging birds are
Diet currently exposed to plastic due to contamination of their food sources. Here, we evaluated the ingestion of
Pellets plastic by a threatened top scavenger, the Andean condor (Vultur gryphus), and the potential origin of the plastic.
Plastic pollution
We analyzed the biotic (organic items from the diet) and abiotic (synthetic material) composition of regurgitated
Peru
Scavenger
pellets in two remote areas of Peru associated with protected areas: a marine-coastal region and an Andean
Threatened species region. Condors consume mainly Pinnipeds and South American camelids in the marine-coastal region, and
camelids and livestock in the Andean region. We found different sizes and varieties of plastic debris, with a very
high frequency of occurrence (85–100%) of microplastics in pellets of both areas studied. The occurrence of
microplastics differed between sites; although very high in general, the rate of occurrence and density were
higher in the marine-coastal region. We also confirmed that carcasses consumed by condors in both study areas
were contaminated with plastic. Therefore, plastic in Andean condors is most probably acquired through the food
web in both the marine and terrestrial environments. Andean condors from Peru are highly contaminated with
plastic, which may affect their health, population dynamics, and conservation. Moreover, as condors are apex
scavengers, our results highlight the fact that plastic pollution in remote areas of Peru is present at different
levels of the food web and in the environment. Urgent Action should be taken to reduce environmental
contamination with this hazardous pollutant.

1. Introduction 2018). Therefore, plastic pollution is cumulative, and persistent

(MacLeod et al., 2021). Plastic pieces remain in the environment for
Plastic pollution is currently one of the most serious environmental thousands of years, and cannot be removed without difficulty, especially
problems worldwide (Rhodes, 2018). Plastic production has increased when some factors (e.g., animal digestive processes or environmental
from 1950 (when mass production of plastic products started) to the factors) cause fragmentation of macroplastics into micro and
present, reaching a peak of 460 million tons in 2019, and this tendency nano-plastics, which are not even visible to the human eye (Barnes et al.,
will continue even in the most optimistic scenarios (MacLeod et al., 2009; MacLeod et al., 2021; So et al., 2022). Worryingly, small plastic
2021; Ritchie and Roser, 2018). A matter of great concern is that global fragments can enter the food web, leading to bioaccumulation of this
plastic waste per year exceeds annual production. This is because of synthetic material in living organisms (Provencher et al., 2022).
discarded items of the accumulated production of previous years; for Diverse wildlife species, both in marine and terrestrial environments,
instance, in 2010 global primary plastic production was 270 million are currently affected by plastic pollution around the world (Santos
tons, while global plastic waste was 275 million tons (Ritchie and Roser, et al., 2021). For instance, plastic pollution in oceans is harmful for sea

* Corresponding author.
E-mail addresses: vgamarrat@unsa.edu.pe, victor.gamarrat@gmail.com (V. Gamarra-Toledo).

https://doi.org/10.1016/j.envpol.2022.120742
Received 28 September 2022; Received in revised form 6 November 2022; Accepted 23 November 2022
Available online 24 November 2022
0269-7491/© 2022 Elsevier Ltd. All rights reserved.
V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

birds, sea turtles, marine mammals and even cetaceans, because of Given that Andean condors in Peru forage in natural and semi-natural
entanglement or ingestion (Ayala et al., 2022; Sigler, 2014). The number areas and have not been reported using rubbish dumps, we expect a
of marine species reported to be affected by plastic debris has increased low occurrence of plastic debris in regurgitated pellets, particularly
over recent years, reaching almost 1300 (Santos et al., 2021). While considering that we surveyed remote and pristine areas with a low level
plastic pollution in terrestrial and freshwaters environments has been of anthropization.
less studied than in marine environments, it currently affects many
reptile, mammal and especially bird species worldwide (Malizia and 2. Material and methods
Monmany-Garzia, 2019; Puskic et al., 2020; Santos et al., 2021): at least
277 terrestrial and freshwater species are currently affected by plastic 2.1. Study species
pollution (Santos et al., 2021). The differences between marine and
terrestrial environments in the number of species affected by plastic The Andean condor is the largest New World vulture (it can weigh up
could be biased by the fact that terrestrial environments are less studied, to 16 kg, wingspan 3 m), and occurs from the north of Venezuela and
but also because plastic debris tends to accumulate near marine envi­ Colombia to the south of Argentina and Chile (Alarcón et al., 2017; Hoyo
ronments (Barnes et al., 2009; Dris et al., 2015; Santos et al., 2021). et al., 1994). It is considered Vulnerable by the IUCN because it is
Evaluating the consumption of plastic debris in species of conser­ negatively affected by several human disturbances, such as intentional
vation concern is important because this synthetic and hazardous ma­ poisoning and lead contamination (Birdlife International, 2022; Plaza
terial could represent a hidden threat to their health and conservation. and Lambertucci, 2020). Condors are highly mobile (they can travel up
Among the diverse terrestrial bird species, obligate scavenging birds to 350 km per day; Lambertucci et al., 2014), but they have
(hereafter, vultures) can be particularly affected by plastic pollution due well-established foraging territories. They roost communally in variable
to contamination of their food sources, and also due to their habit of numbers on large cliffs with ledges, generally far from anthropized areas
consuming indigestible non-food items (e.g., glass, plastic, metal, etc.) (Lambertucci, 2013; Lambertucci et al., 2008). Particularly in Peru,
(e.g., Ballejo et al., 2021; Houston et al., 2007). Some other obligate Andean condors are affected by threats such as intentional poisoning,
scavenging birds also use anthropogenic sites such as rubbish dumps to trading of body parts, collision with power lines, and their use in
obtain food resources (Gangoso et al., 2013; Houston et al., 2007; Plaza traditional ceremonies (Piana, 2014, 2019; Plaza and Lambertucci,
and Lambertucci, 2018; Plaza et al., 2018; Pomeroy, 1975), resulting in 2020; Williams et al., 2011). Population numbers for this species in Peru
plastic ingestion (Ballejo et al., 2021; Duclos et al., 2020; Houston et al., are not well known, but a recent census found that there are at least 300
2007). individuals (SERFOR, unpublished data). While this species has been
The Andean condor (Vultur gryphus), an emblematic and vulnerable reported to take advantage of rubbish dumps in some parts of their
vulture species of South America, is experiencing population decline distribution, such as Chile and Argentina (Duclos et al., 2020; Plaza and
because of diverse human disturbances (Plaza and Lambertucci, 2020). Lambertucci, 2020), there are no reports of this feeding behavior in
In recent years, some populations of this species have been exposed to Peru. Moreover, information about the dietary habits of condors in this
plastic debris in Chile, especially when foraging in rubbish dumps country is still lacking (but see McGahan, 1972).
(Duclos et al., 2020). In contrast, when Andean condors forage in natural
and semi natural areas in Argentina, within or close to protected areas, 2.2. Study area
the occurrence of plastic is less common (Ballejo et al., 2021). To
improve conservation policies for this species and its environment, it is We conducted this study in two contrasting geographical areas of
important to know whether Andean condors are exposed to plastic Peru: i) Reserva Nacional San Fernando (RNSF), a marine-coastal region
pollution in different parts of their distribution range, as with other of the Peruvian Pacific coast, and ii) the buffer area of Reserva Nacional
threats such as intentional poisoning and lead contamination (Plaza and Pampas Galeras Barbara D′ Achille (RNPGBA), an Andean region of
Lambertucci, 2020; Wiemeyer et al., 2016). Moreover, given that An­ central Peru (Fig. 1). The area between these two regions represents a
dean condors are apex scavengers at the top of the trophic chain, this biological corridor between the Andean mountains and the coast (Meza
species can serve as an indicator of plastic pollution in the environment et al., 2021). The RNSF protected area (154,000 ha) is located in the
and for other species. Finally, given the long distances condors travel per department of Ica-Peru (Vásquez, 2015) (Fig. 1). The human population
day – from breeding or roosting areas to feeding areas, and through is very low in this protected area: approximately 60 people (mainly
diverse landscapes (Lambertucci et al., 2014; Williams et al., 2020) – fishermen) live in sites far from where condors feed or roost. The closest
they may transport plastic to pristine, inaccessible areas, promoting the town (San Juan de Marcona) to the protected area lies 30 km away from
generation of plastic islands in these sites, as has been reported for other condor sites and has 15,900 inhabitants (INEI, 2018). In this area, the
vultures (Ballejo et al., 2021). condor population presents low abundance and seems to be associated
Here, we evaluate plastic ingestion in Andean condors in two con­ mainly with the pinniped breeding season. The RNPGBA is a protected
trasting environments of Peru: a marine-coastal and an Andean region. area (6500 ha) lying 3800–5000 above sea level, and the buffer area
Assessing the level of plastic ingestion by condors in these remote and belongs to the Lucanas province, in the department of Ayacucho-Peru
contrasting environments will help us to detect plastic pollution in the (Fig. 1). The closest town to the protected area is 20 km away and has
study areas and determine whether there are differences between ma­ 326 inhabitants (INEI, 2018). The human population in this area is very
rine and terrestrial environments in terms of exposure to this synthetic low: only 10 livestock farmers and 5 rangers live there. An inter-oceanic
material. To this end, we analyze plastic debris in regurgitated pellets in highway crosses this protected area, so there is constant waste accu­
i) a marine-coastal region: “Reserva Nacional San Fernando” (RNSF) and mulation along the road (Fig. 2A). In this area, Andean condors are
ii) an Andean region: buffer zone of the “Reserva Nacional Pampas present in higher abundances than in RNSF: during our surveys we
Galeras Barbara D′ Achille” (RNPGBA). In addition, we determine the counted up to 50 condors roosting in the area at the same time (although
main food items present in Andean condor pellets collected in these there are records of at least 90 condors in this area).
areas to infer the possible origin of the plastic and evaluate the likeli­ Diverse colonies of Otaria flavescens and Arctocephalus australis (Goya
hood of trophic transfer. To look for potential trophic transfer of plastic, et al., 2020; Vásquez, 2015) inhabit the marine-coastal region; these
we also consulted published literature on the presence of plastic (mega, species are used as food sources by condors on the Pacific coasts of Peru
macro, meso and microplastics) in the animals condors may consume. In (Stucchi, 2013; Wallace and Temple, 1987). In fact, in our
addition, we interviewed livestock producers to ask whether they had marine-coastal study area condors are regularly seen feeding on
seen animals (that could later be consumed by condors) ingesting plastic pinniped colonies (authors’ personal observations). In the Andean re­
or found plastic in internal organs when the livestock were slaughtered. gion there are terrestrial species such as Lama guanicoe, Vicugna vicugna

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

Fig. 1. Map of Peru showing the study area and sampling sites.

(Vásquez, 2015) and livestock (sheep, cows and goats) (Alvarado, 2.4. Plastic origin
2019), and in this study area condors are regularly seen foraging in areas
with a high abundance of herbivores (camelids, livestock, etc.; authors’ To infer the possible trophic origin of the plastic debris and to learn
personal observations). more about the condors’ main diet in the study areas, we performed diet
analysis using the pellets. Moreover, we assessed the possibility of tro­
2.3. Field work phic transfer of plastic by reviewing the literature on plastic pollution in
animal carcasses consumed by condors in the study areas. This biblio­
To analyze plastic debris and diet composition in each study area, we graphic research was performed in Google Scholar and Scopus using key
collected fresh pellets from the ground under Andean condor communal terms such as “plastic” and “microplastic” combined with “Pinniped”,
roosts between April and July 2021. This methodology is widely used to “Otariid”, “Livestock”, “Animal”, “Camelid” and “Peru”. In addition, we
evaluate both diet composition and plastic contamination in this and interviewed all the farmers and park rangers living in the Andean region,
other vulture species (Ballejo et al., 2021, 2018; Duclos et al., 2020; asking whether they had seen livestock ingesting plastic or had found
Torres-Mura et al., 2015). The pellets were collected when no condors mega, macro or mesoplastic in internal organs when slaughtering live­
were roosting (between 10 h and 14 h). In the marine-coastal region, we stock. We did not perform interviews in the marine-coastal region, since
sampled the only known large roost site (Punta San Fernando, Fig. 1). In no livestock or people are present in the area frequented by condors; we
the Andean region, we sampled three roost sites (Ilacata 1, Ilacata 2 and used the review of published information to find out whether the car­
Huaraya, Fig. 1). Punta San Fernando roost site is located inside the casses of animals consumed by condors in this site may contain plastic.
protected area (RNSF), while Illacata 1 and 2 lie in the buffer zone of
RNPGBA; Huaraya is located outside this protected area, but nearby 2.5. Laboratory work
(Fig. 1). The distance between the coastal roost site and the three An­
dean sites averages approximately 120 km. The distance between Pellets collected from the roosts were stored in paper bags. Each
Huaraya and Ilacata 1 and 2 is 16 km and the distance between Ilacata 1 pellet was placed in an individual bag, sealed and coded. They were then
and 2 is 1 km. In both marine and Andean regions, roost sites are cliff taken to the laboratory to be dried at room temperature for a minimum
ledges that provide refuge, as in other parts of the condor’s geographical of 48 h. In the laboratory, each pellet was mechanically separated (using
distribution (Lambertucci and Ruggiero, 2013). We collected only fresh metal forceps and scissors) and divided into five parts following Lam­
or dry structurally intact pellets because the probability of finding bertucci et al. (2009). Each pellet was then placed immediately in glass
plastic debris, or recognizing the entire pellet, decreases with the Petri dishes, and the most representative elements such as hair, bone,
degradation process of a pellet once it lies on the ground (Ballejo et al., and synthetic material were removed and stored in hermetically sealed
2021; Provencher et al., 2019). bags following Ballejo et al. (2018, 2021). This first step enabled us to

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

Fig. 2. Images showing A) Image of inter-oceanic highway (the arrow shows the waste accumulation). B) Andean condor pellet with plastic of different sizes and
colors. C, D) Grid of 56 cm2 used to compute microplastic density. E) South American camelid ingesting plastic (plastic bag) in the Andean region (the arrow shows
the plastic bag). F) Ancestral celebration with South American camelids involving the use of plastic (photo credit: Milton Huarancca). (For interpretation of the
references to color in this figure legend, the reader is referred to the Web version of this article.)

make a visual identification of synthetic and organic material (Fig. 2B). the Natural History Museum of the Universidad Nacional de San Agustín
We then used microscopic analysis of fragmented pellets to detect syn­ de Arequipa, Peru. We also used reference catalogues or guides to hair
thetic materials in more detail, to evaluate the range of sizes, and to from species consumed by these birds (Medina, 2017; Medina et al.,
examine the organic material to determine the main food items 2019). We performed this classification with a microscope (Zeiss, Pri­
consumed by condors. mostar 1, 10–40X), following the procedure of Medina (2017) for
We classified plastic items following Provencher et al. (2017), mounting and identification of organic samples. To determine the main
separating them by size as microplastics (<5 mm), mesoplastics (5–20 food items consumed by condors we used a subsample of 132 pellets (27
mm), macroplastics (>20–100 mm), or megaplastics (>100 mm), and from the marine-coastal region and 105 random samples from the An­
also by type: plastic fibers, sheet (e.g., plastic bags), threadlike (e.g., dean region).
rope or netting), foamed synthetics (e.g., polystyrene), hard fragments
(unidentifiable objects) and other plastics (e.g., uncommon items such
as pieces of balloon rubber). To quantify the amount of microplastic 2.6. Statistical analysis
debris present per pellet (i.e., microplastic density) and its color, we
used a grid with 56 quadrants of 1 cm2. On this grid, we counted the To evaluate the presence of plastic debris in Andean Condor pellets
number of quadrants occupied by microplastic debris per pellet and we estimated the frequency of occurrence of plastic debris, following
classified the colors with the aid of a magnifying stereo microscope Provencher et al. (2017). We divided the number of pellets with plastic
(Nikon, SMZ745/745 T, 3.35 X – 300 X) (Fig. 2C and D). For this plastic debris by the total pellets examined, and multiplied the result by 100.
classification we used 573 pellets (27 from the marine-coastal region For each study site, we computed the frequency of occurrence of the
and 546 from the Andean region). different sizes of plastic debris (i.e., mega, macro, meso and micro­
To evaluate the main diet items present in the pellets, we used plastic). To evaluate differences in the frequency of occurrence of plastic
reference samples (e.g., hair and bone) from the scientific collection of between sites we used the Fisher Exact Test.
For each plastic size, we determined the frequency of occurrence of

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

the different types (i.e., plastic fibers, sheet plastic, threadlike plastic, following Ballejo et al. (2018). Diet was classified into the main groups
foamed synthetics, hard fragments and other plastics) in each study of species: marine mammals (Otaria flavescens and Arctocephalus aus­
area. For microplastics, for instance, we first divided the number of tralis), South American camelids (Lama glama, Lama guanicoe, Vicugna
pellets containing a particular type of microplastic (e.g., plastic fibers) vicugna, Vicugna pacos), livestock (cows, sheep), and others (e.g., Lyca­
by the number of pellets with microplastics, and multiplied the result by lopex spp, Lontra spp.). All statistical analyses were performed with R
100. We repeated the same procedure for mega, macro and mesoplastic. core team (2015), and we considered p-values < 0.05 as significant.
We then computed the frequency of occurrence of microplastic colors by
dividing the number of microplastic debris with a certain color (e.g., 3. Results
blue) by the total number of pellets with microplastics, multiplying this
value by 100. We used the Fisher Exact Test to evaluate whether dif­ 3.1. Plastic presence in condor pellets
ferences in color between the study sites were statistically significant. To
compute the density of microplastic present per pellet, we summed up Most of the synthetic materials present in Andean condor pellets
all the quadrants of 1 cm2 on the grid of 56 cm2 occupied by micro­ were plastic debris (N = 613), except for some pieces of paper (N = 6),
plastics (Fig. 2C and D). We used microplastic density instead of total raffia (N = 2), cloth (N = 1) and wool (N = 1). We did not find synthetic
number of microplastics per pellet because these two variables are materials such as glass, wire, washers, electrical wiring, or metals. In the
highly correlated (r = 0.85, P < 0.001) and would give very similar marine-coastal region, the frequency of occurrence of macroplastic was
results. To evaluate potential differences in microplastic density be­ 7.4%, and microplastic was 100%; we found no mega or mesoplastic (N
tween study sites, we performed non-parametric statistics (Kruskal- = 27 pellets; Fig. 3A). In contrast, in the Andean region we found all
Wallis Test), because this variable was not normally distributed (Sha­ sizes of plastic in the pellets: the frequency of occurrence of megaplastic,
piro-Wilk Test< 0.05). macroplastic, mesoplastic and microplastic was 4.6%, 4.6%, 7.2%, and
Finally, to evaluate the composition of the main diet of Andean 84.9%, respectively (N = 546 pellets; Fig. 3A). Differences between sites
Condors for each study area we computed the relative frequency of were statistically significant only for microplastic (Fisher exact test, P =
occurrence of food items (i.e., the number of occurrences of a particular 0.022), which presented a higher frequency of occurrence in the marine-
food item divided by the total number of items, multiplied by 100) coastal region than the Andean region.

Fig. 3. A) Frequency of occurrence (%) of mega, macro, meso and microplastic in Andean Condor pellets according to study area (marine-coastal and Andean
region). B) Frequency of occurrence of different plastic types according to particle size (mega, macro, meso and microplastic) and study area. Mg = megaplastic, Ma
= macroplastic, Me = mesoplastic, Mi = microplastic.

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

In the marine-coastal region, macroplastics and mesoplastics were and other indeterminate plastics (2.5%, 1/39) (Fig. 3B). Finally,
represented entirely by sheet plastics (i.e., plastic bags) (Fig. 3B; Fig. 4A, microplastics were represented by plastic fibers (90%, 416/464), plastic
C, D). Microplastics in this region were represented predominately by bags (11%, 53/464), hard fragments (9.2%, 43/464) and foamed syn­
plastic fibers (100%, 27/27) and by hard fragments (7%, 2/27) (Figs. 3B thetics (0.64%, 3/464) (Fig. 3B; Fig. 4E and F).
and 4E, F). In the Andean region (Fig. 4B), megaplastics were repre­ The mean (±SD) microplastic density per pellet in the marine-coastal
sented entirely by plastic bags (Fig.3B; Fig. 4C and D). Macroplastics in region was 5.4 ± 4.2 fragments per quadrant of 56 cm2, with a median
this region were represented by plastic bags (80%, 20/25), plastic fibers of 5.0. In the Andean region, the mean (±SD) density was 3.46 ± 3.19
(4%, 1/25), hard fragments (4%, 1/25) and other indeterminate plastics fragments per quadrant of 56 cm2, with a median of 3.0. Plastic density
(4%, 1/25) (Fig. 3B). Mesoplastics were represented by plastic bags differed statistically between areas (Kruskal-Wallis Test, Chi-squared =
(71%, 28/39), plastic fibers (12%, 5/39), hard fragments (12%, 5/39) 20.123, P < 0.001). The predominant microplastic colors from the

Fig. 4. Images showing the study areas and plastic debris: A) Marine-costal region. B) Andean region. C-D) Different sizes of plastic debris found in Andean condor
pellets (macro and mesoplastics). E-F) Yellow and blue microplastic fibers found in Andean condor pellets; G) Plastic debris found in the gastrointestinal tract of a
cow slaughtered in the Andean region; H) Dead condor found near the Andean region with plastic in its stomach; I) Plastic debris found in the digestive tract of the
dead Andean condor found. (For interpretation of the references to color in this figure legend, the reader is referred to the Web version of this article.)

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

marine-coastal region were blue (n = 23) and black (n = 17), followed embedded in body) (Table S1). For the Andean region we did not find
by red (n = 6), green (n = 5), and yellow (n = 1) (Fig. 4E and F; Fig. 5), any publications on the presence of plastic in wildlife or livestock, but all
whereas the predominant colors in the Andean region were blue (n = farmers and park rangers interviewed (N = 15; the entire human pop­
363) and black (n = 203), followed by red (n = 54), green (n = 39), ulation of this site) reported having seen their livestock ingest plastic,
white (n = 26), transparent (n = 19), yellow (n = 8) and violet (n = 2) and they had also found plastic debris in livestock when it was slaugh­
(Fig. 4E and F; Fig. 5). There were no statistical differences between sites tered (mega, macro and mesoplastic) (Figs. 2E and 4G, Table S1).
in terms of the most abundant colors (Fisher exact test, P > 0.05).
4. Discussion
3.2. Condor diet
4.1. Occurrence of mega, macro and mesoplastic in condor pellets
The main food items consumed by Andean condors in the marine-
costal region were marine mammals, such as pinnipeds (Otaria fla­ We found that Andean condors from remote areas of Peru are highly
vescens and Arctocephalus australis), but they also consumed terrestrial contaminated with plastic debris of different sizes and types. Most mega,
items, mainly South American camelids (Lama glama, Lama guanicoe, macro and mesoplastics detected in pellets consisted of sheet plastic
Vicugna vicugna and Vicugna pacos; Fig. 6). In 11% of the pellets from the (plastic bags) (Fig. 4C and D). The high incidence of mega, macro and
marine-costal region (all with plastic present), we found only marine meso plastic debris we found in Andean condor pellets from both study
mammals, while in the remainder we found a combination of marine areas was unexpected; these results are of great concern considering that
and terrestrial mammals. The main food items consumed by Andean these condors forage in natural and semi-natural remote environments,
condors in the Andean region were terrestrial South American camelids, within or very close to protected areas. A previous study in Argentine
but they also fed on livestock (Equus caballus and Bos taurus, Fig. 6). One Patagonia found that vultures feeding close to anthropized areas were
pellet from this Andean area contained marine mammal hair. more exposed to plastic than others (Ballejo et al., 2021). However,
Andean condors from the same area that foraged close to or inside
3.3. Plastic origin protected areas registered very low levels of meso to mega plastic debris
(1.1%) (microplastics were not studied) (Ballejo et al., 2021). This
Our review found three articles that evaluated the presence of plastic contrasts with our results of 7.4% and 16.3% plastic occurrence
in species consumed by condors in the marine-coastal study area and its (considering mega, macro and mesoplastic together) in the remote
surroundings. These papers found that both Otaria flavescens and Arc­ marine-coastal and Andean regions, respectively.
tocephalus australis – which are much consumed by condors – are Unfortunately, we do not have information on the pattern of move­
exposed to and contaminated with plastic debris of different sizes both ment of the studied population, and of course condors can travel hun­
internally (presence of plastic in scats) and externally (collars, hooks dreds of kilometers in search of food, even crossing the Andes mountains

Fig. 5. Color of microplastics found in condors according to study area (Marine-coastal and Andean region). The size of the rectangles is proportional to the fre­
quency of occurrence of microplastic colors. B = blue, Bl = black, R = red, G = green, Y = yellow, W = white, T = transparent, V = violet. (For interpretation of the
references to color in this figure legend, the reader is referred to the Web version of this article.)

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

Fig. 6. Relative frequency of occurrence (%) of items consumed by Andean condors according to study area: Marine-coastal or Andean region. The size of the
silhouettes is proportional to the relative frequency of occurrence.

(Lambertucci et al., 2018). They might therefore be consuming plastic 4.2. Microplastic in condor pellets
from other, more anthropic areas far from the study sites. However,
condors from our study areas have not been seen foraging in rubbish Most microplastic found was in the form of plastic fibers (Fig. 4E and
dumps or in anthropized areas in this region. Moreover, we did not find F). We found a very high frequency of occurrence of microplastic debris
items like glass or wire which are commonly present in pellets when in both study areas, with higher density in the marine-costal area than in
individuals forage in these sites (Duclos et al., 2020; Pavez et al., 2019). the Andean region. This may be because plastic pollution is ubiquitous
However, the occurrence of plastic in the Andean region (mega, macro and tends to accumulate in coastal-marine environments (Barnes et al.,
and meso, 16,3%) resembles the results from central Chile where An­ 2009; Santos et al., 2021). Microplastics found in Andean condor pellets
dean condors routinely use rubbish dumps (Duclos et al., 2020). from both study areas may have two possible sources. On the one hand,
Therefore, these results for Andean condors, as apex scavengers, are a it could be from consumption of mega, macro, or meso plastic present in
sign of worrying levels of plastic environmental pollution in marine and the environment (e.g., consumption of entangled animals, soil contam­
terrestrial ecosystems, even within or in the surroundings of wild pro­ ination), which is then fragmented by the condor’s digestive process
tected areas. (see, So et al., 2022 for a detailed explanation of the general process)
While vultures can directly ingest synthetic material such as plastic, (Fig. 7). On the other hand, microplastics could enter by trophic transfer;
confusing it with food items, especially in rubbish dumps (Houston i.e., microplastics present in the digestive tract or tissues of items
et al., 2007), the origin of the mega, macro and mesoplastic we found consumed by condors (Fig. 7) (Carbery et al., 2018; Huerta Lwanga
seems to be related to the presence of plastic debris in carcasses they et al., 2017; Provencher et al., 2022).
consume (i.e., trophic transfer). Our results suggest that the plastic Plastic fragmentation by condor digestive processes could be the
present in condor pellets comes mainly from marine mammals and reason for the high levels of microplastic we detected in pellets. In both
camelids in the marine-coastal region and South American camelids and sites studied, people tend to discard dead animals such as livestock and
livestock in the Andean region. Our bibliographic search showed that even dogs in plastic bags. Moreover, in the Andean region, people use
pinnipeds near the study area are contaminated internally (e.g., plastic in ancestral celebrations involving Vicugna vicugna (Fig. 2F), so
gastrointestinal tract) and externally (e.g., hooks, collars) by plastic condors may get contaminated when consuming these carcasses. Addi­
(Ayala et al., 2022, 2021; Table S1). Moreover, interviews and evalua­ tionally, as mentioned above, the food items most consumed by condors,
tions of slaughtered livestock in the Andean study site showed that such as Otariids (e.g., Arctocephalus australis or Otaria flavescens) or
livestock from this region do ingest plastic, and their carcasses have this herbivores (e.g., livestock, camelids), may present mega, macro and
synthetic material in their gastrointestinal tract (Figs. 2E and 4G). In any meso plastic in their bodies (e.g., entangled animals, animals with
case, plastic debris is entering condors’ bodies, exposing them to this plastic in their digestive tracts or other body parts). Therefore, Andean
pollution. condors could be ingesting plastic and fragmenting it through digestive
Our results are therefore worrying for a vulnerable species such as processes (Fig. 7), similar to other animal species (Provencher et al.,
the Andean condor; it is well known that in diverse animal species 2022; So et al., 2022).
(including Neotropical vultures) plastic can cause health problems such Ingestion of microplastic by trophic transfer could be another po­
as oxidative stress, toxicological problems or inflammatory responses tential reason for the high values of microplastic we found (Fig. 7). In­
(Biamis et al., 2021; Cunha et al., 2022; Waring et al., 2018). In fact, formation provided by other scientific articles supports the fact that
recent studies with the closely related black vulture (Coragyps atratus) plastic pollution by food transfer is plausible in the study area. Marine
and other bird species show that plastic ingestion leads to alterations in environments (e.g., sandy beaches) in Peru, and specifically in the study
health, such as high production of ROS (reactive oxygen species), he­ area, are highly contaminated with microplastic (De-la-Torre et al.,
patic stress, and tissue damage (Cunha et al., 2022; Rivers-Auty et al., 2020). In fact, on the marine coast associated with the study area,
2022). Moreover, an Andean condor that was found dead in the Andean Otarids (both Arctocephalus australis and Otaria flavescens) that represent
region (department of Arequipa, Yura district), presented plastic debris one of the main food sources for condors in the marine-coastal region
in its digestive tract (Fig. 4H and I; Mariana Peralta personal commu­ present microplastic debris in their fecal material which is compatible
nication). This suggests we should pay attention to, and evaluate, the with its presence in their digestive tract (Ayala et al., 2021; Per­
possibility that plastic may already be affecting the health of these birds, ez-Venegas et al., 2020). Microplastic present in these marine mammals
even to the extent of producing lethal alterations. is acquired both by direct ingestion and by consuming food items
contaminated with this synthetic material (e.g., fishes, Perez-Venegas

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

Fig. 7. Scheme showing the potential origin of microplastics in Andean Condor pellets. On the left, potential terrestrial and marine trophic transfer. On the right, the
generation of micro plastic through digestion of mega, macro and mesoplastic.

et al., 2020). Our results highlight that Otariids constitute an important particle/fiber, ii) if the particle was a fiber it should be consistently
part of the Andean condor diet in the marine-coastal regions, and that all thick, not taper towards the ends and have three-dimensional bending
the pellets with only Otariids as food items had plastic debris. This (not entirely straight fibers, which indicates a biological origin), iii) the
suggests that microplastic may reach these birds through trophic fiber was clear and homogeneous in color (Noren, 2007; Perez-Venegas
transfer when consuming contaminated carcasses. et al., 2020, 2018).
Similarly, terrestrial animals such as livestock or South American
camelids which are consumed by condors also present microplastic in 5. Conclusions
their bodies, associated with contaminated soils or food sources (e.g.,
plastic waste dispersed from the interoceanic highway), as reported in Plastic pollution is widely present in Andean condor pellets from
other geographical areas of the world (Beriot et al., 2021; Pironti et al., wild marine-coastal and Andean remote ecosystems of Peru. In coastal
2021; Uwamungu et al., 2022; Wu et al., 2021). In fact, interviewed areas, condors consume a large number of marine mammal carcasses,
livestock producers from the Andean region reported plastic (mega, but also some terrestrial species. Andean condors from the Andean re­
macro and mesoplastic) in internal organs of their livestock and other gion consume mostly camelids, but also livestock. Given the high inci­
herbivores consumed by condors (see Fig. 4G). However, information on dence of plastic in Andean condor pellets, it is difficult to link any
microplastic in terrestrial environments is lacking in southern Peru particular food item with plastic ingestion by these birds. What seems
(De-la-Torre et al., 2020). Plastic pollution is therefore of concern in this clear is that plastic comes from both marine and terrestrial environ­
region, but further studies are necessary to determine the dynamics of ments. The ingestion of Otariid species, which present high plastic
this pollutant in these environments. contamination, is probably largely responsible for the plastic we found
We found that the predominant colors of microplastics detected in in condors from the marine-coastal region (Perez-Venegas et al., 2020).
Andean condor pellets in both study sites were blue, followed by black; Our results show that livestock species present in the Andean region also
there was no difference in the main colors between study sites. This have plastic in their bodies and internal organs, thus condors become
suggests that these plastic colors are commonly used and discarded by contaminated when consuming these food items. This article is the first
humans in these areas, or where condors aggregate to feed, and are thus to report microplastic presence in Andean condor pellets. We emphasize
ingested by these birds and other animals. Condors may just be eating that the high level of plastic contamination we found has not been re­
more plastic of the type most used and discarded in the region; however, ported before in any terrestrial bird species in Peru and, to our knowl­
it would be interesting to determine whether condors or their prey have edge, in any Andean region of the Neotropics. It would therefore be
any preference for specific plastic colors. This has already been reported interesting to investigate further, through simultaneous sampling of
in fish, for instance: some species ingest blue plastic particles because diverse prey items and the environment, whether the plastic present in
they confuse them with natural food (Ory et al., 2017; Thiel et al., 2018), these birds is a consequence of both bioaccumulation and trophic
then the fish can be consumed by Otariids (Perez-Venegas et al., 2020) transfer. Finally, it is important to consider that condors are apex
whose carcasses are consumed by condors. In fact, the blue fibers we scavengers; our results with these birds testify to the high level of plastic
found in Andean color pellets are the most predominant microplastics in pollution in the environment in southern Peru, which could have a
Otariids from the Peruvian coast (Perez-Venegas et al., 2020). On the negative impact on the biodiversity of two important ecosystems in the
other hand, the presence of black microplastic fibers merits further study country (Andean and coastal). This is of particular concern because our
in order to establish their origin and their association with condor food study sites lie within or in the buffer zone of protected areas, and also
items, since diverse marine organisms and water courses register high because this synthetic material is present at different levels of the food
levels of black microplastics (Ding et al., 2019; Gray et al., 2018; Susanti web. Importantly, the dispersal of plastic debris by Andean condors
et al., 2022). contributes to the formation of plastic islands (Ballejo et al., 2021) in
While our results confirmed a high occurrence of plastic in Andean remote and inaccessible sites like the communal roosts they used in our
condor pellets, we were not able to perform complementary analyses to study area. Therefore, there is an urgent need for action to reduce plastic
determine the nature of each synthetic material detected, particularly use and pollution in this region, especially in areas inhabited by
microplastics (e.g., micro-Fourier Transform Infrared Spectroscopy, threatened species such as the Andean condor, so as to diminish the
μFTIR). However, we have full confidence in our methodology and re­ impact of this pollutant on these species and on the entire ecosystem.
sults because before classifying a synthetic material as plastic debris we
ensured that: i) no cellular or organic structures were visible in the

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V. Gamarra-Toledo et al. Environmental Pollution 317 (2023) 120742

Author statement Ayala, F., Cardeña, M., Cárdenas-Alayza, S., 2021. Registro preliminar de microplásticos
en fecas del león marino sudamericano (Otaria byronia [de Blainville 1820])
recolectadas en punta San Juan. Perú. Rev. Int. Contam. Ambient. 37, 273–279.
Victor Gamarra-Toledo: Conceptualization; Data curation; Formal Ayala, F., Castillo-Morales, K., Cárdenas-Alayza, S., 2022. Impact of marine debris
analysis; Investigation; Methodology; Project administration; Resources; recorded in a sympatric colony of otariids in the south coast of Peru. Mar. Pollut.
Validation; Visualization; Roles/Writing - original draft; Writing - re­ Bull. 174, 113281.
Ballejo, F., Lambertucci, S.A., Trejo, A., De Santis, L.J., 2018. Trophic niche overlap
view & editing; Pablo Plaza: Conceptualization; Data curation; Formal among scavengers in Patagonia supports the condor-vulture competition hypothesis.
analysis; Investigation; Resources; Validation; Visualization; Roles/ Bird. Conserv. Int. 1–13.
Writing - original draft; Writing - review & editing.; Sergio Lamber­ Ballejo, F., Plaza, P., Speziale, K.L., Lambertucci, A.P., Lambertucci, S.A., 2021. Plastic
ingestion and dispersion by vultures may produce plastic islands in natural areas.
tucci: Conceptualization; Data curation; Formal analysis; Funding Sci. Total Environ. 755, 142421.
acquisition; Investigation; Methodology; Project administration; Re­ Barnes, D.K., Galgani, F., Thompson, R.C., Barlaz, M., 2009. Accumulation and
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draft; Writing - review & editing; Yuri A. Peña: Data curation; Inves­ Beriot, N., Peek, J., Zornoza, R., Geissen, V., Huerta Lwanga, E., 2021. Low density-
tigation; Methodology; Pierina A. Bermejo: Data curation; Investiga­ microplastics detected in sheep faeces and soil: a case study from the intensive
tion; Methodology; Juan López: Data curation; Investigation; vegetable farming in Southeast Spain. Sci. Total Environ. 755, 142653 https://doi.
org/10.1016/j.scitotenv.2020.142653.
Methodology; Gonzalo L. Cano: Data curation; Investigation; Method­ Biamis, C., O’Driscoll, K., Hardiman, G., 2021. Microplastic toxicity: a review of the role
ology; Santiago Barreto: Data curation; Methodology; Sandra Cáceres- of marine sentinel species in assessing the environmental and public health impacts.
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