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This study aimed to report an interspecific association between brown-nosed coatis (Nasua nasua) and capybaras (Hydrochoerus hydrochaeris) in an urban area of Brazil. We recorded N. nasua feeding on ectoparasites (ticks) attached to H. hydrochaeris, which in turns, did not show any reaction of discomfort with the situation. Thus, we report an unprecedented case of protocooperation between apparently unrelated species. Moreover, the interspecies interaction reveals other interesting scenarios as the inclusion of ticks in the diet of N. Nasua and the possibility of parasite transmission and adaptation to a new host species, a phenomenon known as ‘host switching’. We associate these new records as adaptations of wildlife to urbanization, and their effects should be further investigated from both wildlife conservation and ‘One Health’ approach.
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Bol. Mus. Para. Emílio Goeldi. Cienc. Nat., Belém, v. 15, n. 3, p. 843-848, set.-dez. 2020
843
Interspecific association between brown-nosed coatis and
capybaras in an urban area of Brazil
Associação interespecífica entre quatis e capivaras em uma
área urbana do Brasil
Andreza Castro RuccoI | Heitor Miraglia HerreraI, II |
Filipe Martins SantosI | Grasiela Edith de Oliveira PorfirioIII
IUniversidade Católica Dom Bosco. Programa de Pós-Graduação em Ciências Ambientais e
Sustentabilidade Agropecuária. Campo Grande, Mato Grosso do Sul, Brasil
IIUniversidade Federal de Mato Grosso do Sul. Programa de Pós-Graduação em Ecologia e Conservação.
Campo Grande, Mato Grosso do Sul, Brasil
IIIUniversidade Federal de Mato Grosso do Sul. Pós-Graduação em Recursos Naturais. Campo Grande, Mato Grosso do Sul, Brasil
Abstract: This study aimed to report an interspecific association between brown-nosed coatis (Nasua nasua) and capybaras
(Hydrochoerus hydrochaeris) in an urban area of Brazil. We recorded N. nasua feeding on ectoparasites (ticks) attached
to H. hydrochaeris, which in turns, did not show any reaction of discomfort with the situation. Thus, we report an
unprecedented case of protocooperation between apparently unrelated species. Moreover, the interspecies interaction
reveals other interesting scenarios as the inclusion of ticks in the diet of N. Nasua and the possibility of parasite transmission
and adaptation to a new host species, a phenomenon known as ‘host switching’. We associate these new records as
adaptations of wildlife to urbanization, and their effects should be further investigated from both wildlife conservation
and ‘One Health’ approach.
Keywords: Carnivora. Protocooperation. Rodentia. Urban ecology.
Resumo: O objetivo deste estudo foi relatar uma associação interespecífica entre quatis (Nasua nasua) e capivaras (Hydrochoerus
hydrochaeris) em uma área urbana do Brasil. Registramos N. nasua se alimentando de ectoparasitas (carrapatos) aderidos
em H. hydrochaeris, que, por sua vez, não mostrou nenhuma reação de desconforto com a situação. Logo, relatamos
um caso de protocooperação entre espécies aparentemente não relacionadas. Além disso, a interação interespecífica
revela outros cenários interessantes, como a inclusão de carrapatos na dieta de N. nasua e a possibilidade de transmissão
e adaptação de parasitas a uma nova espécie hospedeira, fenômeno conhecido como ‘troca de hospedeiro’. Associamos
esses novos registros como adaptações da vida selvagem à urbanização, e seus efeitos devem ser investigados a partir
da perspectiva da conservação da vida selvagem e da abordagem de Saúde Única.
Palavras-chave: Carnívora. Protocooperação. Rodentia. Ecologia urbana.
RUCCO, A. C., H. M. HERRERA, F. M. SANTOS & G. E. O. PORFIRIO, 2020. Interspecific association between brown-nosed coatis
and capybaras in an urban area of Brazil. Boletim do Museu Paraense Emílio Goeldi. Ciências Naturais 15(3): 843-848. DOI: http://
doi.org/10.46357/bcnaturais.v15i3.284.
Autora para correspondência: Grasiela Edith de Oliveira Porfirio. Universidade Federal de Mato Grosso do Sul. Programa de Pós-Graduação
em Recursos Naturais. Avenida Costa e Silva, s/n – Cidade Universitária. Campo Grande, MS, Brasil. CEP 79070-900 (grasi_porfirio@
hotmail.com).
Recebido em 20/02/2020
Aprovado em 10/11/2020
Responsabilidade editorial: Alexandra Maria Ramos Bezerra
BY
Interspecific association between brown-nosed coatis and capybaras in an urban area of Brazil
844
It is well documented that some wild animals inhabit, and
therefore benefit from, remnant forest fragments found in
urban and peri-urban areas worldwide. In South America,
a widely distributed mesocarnivore, the brown-nosed coati
Nasua nasua (Linnaeus, 1766), and the largest extant rodent
species, the capybara Hydrochoerus hydrochaeris (Linnaeus,
1766), are both known to inhabit several urban areas of
Brazil (Costa et al., 2009; Ferreira, G. et al., 2013; Tonin
et al., 2016). Notably, the city of Campo Grande, Mato
Grosso do Sul state, in the western Brazilian Cerrado, has
a diverse array of wild fauna utilizing the urban environment
(Ferreira, C. et al., 2010). From the human perspective,
interacting with wildlife is positive for the wellbeing of
people, and has the added benefit of attracting tourism to
the area, particularly if wildlife has become used to human
presence (Mamede & Benites, 2018; Calderan et al.,
2019). However, wild animals in urban areas can provide
other scenarios as they can pose risk of traffic accidents,
invade residences, and even maintain zoonotic parasites
(Soulsbury & White, 2016). Hydrochoerus hydrochaeris, for
example, play a primary role in the transmission cycle of
Rickettsia rickettsii (Ricketts, 1909), which is the etiological
agent of Brazilian spotted fever, considered the most deadly
rickettsiosis worldwide (Labruna, 2013). Furthermore,
from an ecological viewpoint, urbanization can change
population parameters and the behavioral dynamics
of animal species in these areas, revealing previously
undescribed, or seemingly unlikely, relationships among
species (Soulsbury & White, 2016).
Here we report on an interspecific association
between N. nasua and H. hydrochaeris at Parque das
Nações Indígenas (PNI), regarded as one of the most
important urban parks of Campo Grande city, Mato
Grosso do Sul state, Brazil (Figure 1). The PNI is an
urban secondary forest fragment with an area of 119
hectares; the forest formations and wildlife species
assemblages of the park are typical of the Cerrado biome.
The connectivity of PNI with other forest fragments
allows several species of wild animals to use the park,
for example Didelphis albiventris Lund, 1840, Dasyprocta
azarae Lichtenstein, 1823, Ara ararauna (Linnaeus, 1758),
Dasypus novemcinctus Linnaeus, 1758, and Ramphastos
toco Müller, 1776, besides N. nasua and H. hydrochaeris
(G. Porfirio, personal observation, 2017).
Figure 1. A) Mato Grosso do Sul state in Brazil (pale gray); B) location of the municipality of Campo Grande in Mato Grosso do Sul state
(pale gray); and C) location of Parque das Nações Indígenas in the city of Campo Grande (pale gray), and its land use in the enlarged image.
Map: Filipe Martins Santos (2020).
Bol. Mus. Para. Emílio Goeldi. Cienc. Nat., Belém, v. 15, n. 3, p. 843-848, set.-dez. 2020
845
Interspecific associations between N. nasua and H.
hydrochaeris in the PNI were recorded on two occasions,
in January (rainy season) and August (dry season) 2019,
respectively. Individuals of N. nasua were observed feeding
on ectoparasites (ticks) attached to H. hydrochaeris (Figures
2A and 2B). Nasua nasua group composition consisted of
adult females and their cubs, and juveniles. Animals were
classified according to their age and sex, based on Barros &
Frenedozo (2010): (i) adult males: animals with large body
and head size, in addition to the presence of the scrotal
sac; (ii) adult females: smaller than adult males, rarely seen
alone; (iii) youngs: smaller than adult females or of similar
proportions; (iv) cubs: smaller than the youngs, with similar
head/body proportions.
Cubs were the first individuals of the group to be
observed foraging on ticks attached to H. hydrochaeris, just
prior to sunset (approximately 17:00 pm in both occasions).
Initially, adult females foraged on fruit in the surrounding
area; adult females and the rest of the group were later
observed alternating between foraging on ticks attached
to H. hydrochaeris. Interactions were interrupted when
casual human observers approached the site resulting in the
dispersal of both wildlife species involved in the interaction.
During both observation periods, H. hydrochaeris did not
show any avoidance behavior toward N. nasua, instead
individuals remained immobile, in the ventral position,
while N. nasua foraged for ticks.
Although there are other reported cases of
mammalian interspecies associations (McClearn, 1992;
Haugaasen & Peres, 2008; Desbiez et al., 2010), this is
the first time an interspecies association between N. nasua
and H. hydrochaeris has been described. Moreover, we
consider this species interaction particularly interesting
because, although N. nasua and H. hydrochaeris coexist
in several tropical ecosystems (see Paglia et al., 2012),
they are thought to rarely interact in natural areas due
to their contrasting habits (H. Herrara and G. Porfirio,
personal observations, 2020). While, H. hydrochaeris is
a herbivorous and semi-aquatic species (Mones & Ojasti,
1986; Desbiez et al., 2011), N. nasua (although classified
as a carnivore taxonomically) is ecologically classified as
an omnivore (Gompper & Decker, 1998; Desbiez et al.,
2010), consuming mainly fruits and invertebrates (insects
and other arthropods) (Bianchi et al., 2013).
Accordingly, we report here on three interesting
ecological scenarios associated with the described interspecies
interaction. The first is protocooperation between N.
nasua and H. hydrochaeris in an urban forest fragment.
Figure 2. Groups of brown-nosed coatis (Nasua nasua) foraging on capybara (Hydrochoerus hydrochaeris) (A and B) in the Parque das Nações
Indígenas, urban area of Campo Grande, Mato Grosso do Sul state, Brazil. Photos: Andreza Castro Rucco (2019) (A) and Gabriel Tirintan
de Lima (2019) (B).
Interspecific association between brown-nosed coatis and capybaras in an urban area of Brazil
846
Protocooperation is defined as a harmonic interspecific
relationship whereby both species benefit from the
interaction but neither species require the interaction
to survive (Odum & Barrett, 2011). Nasua nasua gained
a novel food source, while the H. hydrochaeris had its
ectoparasite load reduced. Interestingly, this type of
association has been described on multiple occasions
for herbivorous African mammals and birds (Mikula et
al., 2018). For H. hydrochaeris, association with birds is
commonly reported in Brazil, especially involving two
bird species, the cattle tyrant Machetornis rixosa (Vieillot,
1819) and the yellow-headed caracara Milvago chimachima
(Vieillot, 1816) (Sazima et al., 2012; D’Angelo et al., 2016).
However, this is the first record of H. hydrochaeris in a
harmonic interspecific relationship with N. nasua. For
N. nasua, in turns, interspecific association with other
mammals is not a novelty. Nasua nasua is known to
associate with squirrel monkeys Saimiri ustus I. Geoffroy,
1843 in Amazonian dry forest, but the association was
limited to foraging in the same place, in different strata
(Haugaasen & Peres, 2008). According to the Haugaasen
& Peres (2008), no interspecific interference or aggression
was observed in any occasion of such observations. In
the same study site, these authors reported two events
of associations between N. nasua and brown-capuchins
Cebus (Sapajus) apella (Linnaeus, 1758), but unlike the
previous association described, N. nasua and C. (S.) apella
foraged side by side. Again, no interspecific interference or
aggression was recorded (Haugaasen & Peres, 2008). In the
Brazilian Pantanal, N. nasua was observed associating with
Dicotyles tajacu (Linnaeus, 1758), also to forage together
on fruits (Desbiez et al., 2010).
The second point of interest is the inclusion of ticks as
a food item in the diet of N. nasua. Although invertebrates
are a known part of the species’ diet (Gompper & Decker,
1998; Bianchi et al., 2013; Ferreira, G. et al., 2013), the
consumption of ticks has not been observed before. On
the other hand, Nasua narica (Linnaeus, 1766), another
procyonid species occurring from south United States,
Central America up to northern South America (Cuarón
et al., 2016), was recorded grooming and ingesting ticks
attached to Tapirus bairdii (Gill, 1865) in Barro Colorado
Island, Panamá (McClearn, 1992). On these occasions,
both individuals were habituated to humans, and McClearn
(1992) suggested that the association was probably a
learned phenomenon occurring in a small subset of both
populations. According to McClearn (1992) humans and
their behavior favor this kind of association.
Finally, we highlight the possibility of parasite
transmission and adaptation to a new host species, in
this case Nasua nasua, in a phenomenon known as ‘host
switching’ (Araujo et al., 2015). This scenario can happen
because some parasites have arthropods as intermediate
hosts (Avancini & Ueta, 1990; Bennett et al., 1992; Labruna
et al., 2004), and it may be that certain parasite species that
co-evolved with ticks attached to H. hydrochaeris (the host
species), such as Rickettsia spp. (Queirogas et al., 2012) and
Mycoplasma spp. (Cubilla et al., 2017) could be transmitted
to a new mammalian host, in this case, N. nasua.
Additionally, as some of the same microorganisms infect
animals and humans, possible transmission of parasites to
urban inhabiting N. nasua could potentially impact human
populations occupying the same environment. Therefore,
tick consumption by N. nasua in urban areas should be
investigated further from both wildlife conservation and
human health perspectives (i.e., ‘One Health’ approach)
(Dantas-Torres et al., 2012).
In conclusion, urban parks in Campo Grande city,
appear to provide an environment that can support
interspecific interactions between apparently disparate
wildlife species. Nasua nasua and H. hydrochaeris were
found to have a previously undescribed, interspecific
association. Based on our observations, we propose that
ticks (from H. hydrochaeris) appear to be a new food
item in the diet of urban inhabiting N. nasua. Additionally,
we consider the possibility of a new parasitic adaptation
associated with tick consumption by N. nasua, and possible
concerns for the conservation of N. nasua in urban forest
Bol. Mus. Para. Emílio Goeldi. Cienc. Nat., Belém, v. 15, n. 3, p. 843-848, set.-dez. 2020
847
fragments associated with this. Accordingly, research into
this interspecies association warrants further investigation.
ACKNOWLEDGMENTS
Authors thanks Coordenação de Aperfeiçoamento de Pessoal
de Nível Superior (CAPES, Brazil) for the grants received
(88882.315124/2019-01; 88887.369261/2019-00),
and Conselho Nacional de Desenvolvimento Científico e
Tecnológico (CNPq) (308768/2017-5). We are grateful to
two anonym reviewers for their valuable suggestions and
comments in a previous version of this manuscript. This
study was financed in part by the Fundação Universidade
Federal de Mato Grosso do Sul (UFMS/MEC) and CAPES
(Finance Code 001).
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Article
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Understanding the diversity and ecology of ectoparasites in wild animals is essential for surveillance of vector-borne diseases. Coatis (Nasua nasua) easily adapt to anthropized areas, favoring close contact with domestic animals and humans, with the possibility of exchange of ectoparasites and pathogens. The present study aimed to identify the diversity of ticks parasitizing coatis from forest urban areas of midwestern Brazil, to evaluate the seasonal dynamics of ticks during the seasons of the year, and to assess the correlation between tick species and gender and age of the sampled coatis. For this purpose, 103 coatis were captured in two Conservation areas, both located in Campo Grande city, Mato Grosso do Sul state, Midwestern Brazil. The animals’ entire body was inspected for the presence of ectoparasites, and ticks were removed for taxonomic identification. In total, 168 captures were performed in both areas during the observational study considering the first capture and recaptures. In total, 2242 ticks were collected: 838 Amblyomma larvae, 1241 A. sculptum nymphs, and 150 A. dubitatum nymphs. Thirteen adult ticks were identified as three males and five females of A. sculptum and two males and three females of A. ovale. While a quantity of Amblyomma larvae was observed in the first months of the year (January, April and May), Amblyomma nymphs showed a higher quantity during the months of July, August, October and November. No statistical difference was observed when comparing mean intensity and prevalence of Amblyomma larvae, nymphs of A. sculptum and A. dubitatum between the two sampled areas, males vs. females and immature vs. mature animals. In conclusion, three tick species were identified parasitizing coatis from forested urban fragments in midwestern Brazil, namely A. dubitatum nymphs, A. sculptum adults and nymphs, and A. ovale adults. Coatis from anthropized areas seem to present tick species diversity lower than those from natural areas. The lack of statistical difference regarding mean intensity and prevalence of Amblyomma larvae and nymphs between males vs. females and immature vs. mature animals might have reflected the gregarious behavior of coatis, since adult males live together with females and offspring outside and inside the mating season, forming large groups of individuals.
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Fundamentos de Ecologia: 1-612. Cengage Learning
  • E P G W Odum
  • Barrett
ODUM, E. P. & G. W. BARRETT, 2011. Fundamentos de Ecologia: 1-612. Cengage Learning, São Paulo.