Morphology of the adrenal glands of giant anteater (Myrmecophaga tridactyla, Linnaeus, 1758) of wild life

Abstract

The Myrmecophaga tridactyla (family Pilosa), popularly known in Brazil as the giant anteater is classified as an endangered species by the main survey agencies of biodiversity preservation around the world. The adrenal glands are important organs, which are related to homeostasis of the animal. This study aimed to describe the morphology of the adrenal glands of M. tridactyla, providing data for future studies related to the production of steroid hormones in specimens exposed to different stress factors. The adrenal glands of 14 specimens were used. The glands were measured, photodocumented and described by light microscopy. The adrenals were positioned in the cranial extremity of the kidneys (left and right) and related medially to the caudal vena cava. The right adrenal gland had an elongated shape while the left adrenal gland had pyramidal or triangular shape. The weight was 4.765±0.129g for the right adrenal and 3.975±0.213g for the left adrenal. The length was 4.50±0.14cm for the right adrenal and 4.28±0.11cm for the left adrenal. The width was 2.60±0.13cm for the right adrenal and 2.37±0.12cm for the left adrenal. The thickness was 0.45±0.11cm for the right adrenal and 0.68±0.14cm for the left adrenal. Statistical differences (p

Full text

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Original Article
Biosci. J., Uberlândia, v. 32, n. 6, p. 1559-1566, Nov./Dec. 2016
MORPHOLOGY OF THE ADRENAL GLANDS OF GIANT ANTEATER
(Myrmecophaga tridactyla, LINNAEUS, 1758) OF WILD LIFE
MORFOLOGIA DAS GLÂNDULAS ADRENAIS DE TAMANDUÁ-BANDEIRA
(Myrmecophaga tridactyla, LINNAEUS, 1758) DE VIDA LIVRE
Amilton Cesar dos SANTOS
1
; Diego Carvalho VIANA
1
; Rafael Magdanelo LEANDRO
2
;
Rosângela Felipe RODRIGUES
3
; Antônio Chaves de ASSIS-NETO
2
;
Alan Peres Ferraz de MELO
3
1. Doutorando, Faculdade de Medicina Veterinária e Zootecnia- FMVZ, Universidade de São Paulo-USP, São Paulo, SP, Brasil.
amiltonsantoss@usp.br; 2. Professores Doutores, Faculdade de Medicina Veterinária e Zootecnia – FMVZ, Universidade de São Paulo-
USP, São Paulo, SP, Brasil; 3. Professores Doutores. Faculdade de Engenharia, Universidade Estadual Paulista-UNESP, Campus de Ilha
Solteira, SP, Brasil.
ABSTRACT:
The Myrmecophaga tridactyla (family Pilosa), popularly known in Brazil as the giant anteater is
classified as an endangered species by the main survey agencies of biodiversity preservation around the world. The adrenal
glands are important organs, which are related to homeostasis of the animal. This study aimed to describe the morphology
of the adrenal glands of M. tridactyla, providing data for future studies related to the production of steroid hormones in
specimens exposed to different stress factors. The adrenal glands of 14 specimens were used. The glands were measured,
photodocumented and described by light microscopy. The adrenals were positioned in the cranial extremity of the kidneys
(left and right) and related medially to the caudal vena cava. The right adrenal gland had an elongated shape while the left
adrenal gland had pyramidal or triangular shape. The weight was 4.765±0.129g for the right adrenal and 3.975±0.213g for
the left adrenal. The length was 4.50±0.14cm for the right adrenal and 4.28±0.11cm for the left adrenal. The width was
2.60±0.13cm for the right adrenal and 2.37±0.12cm for the left adrenal. The thickness was 0.45±0.11cm for the right
adrenal and 0.68±0.14cm for the left adrenal. Statistical differences (p<0.05) between right and left adrenals for all values
analyzed were observed. Microscopically it was observed a capsule composed by modeled dense connective tissue lining
the organ. Below this capsule, from the outermost to the innermost layer, it was observed a cortical region divided into
glomerular, fasciculata and reticular zones with a medullar region occupying the center of the organ. Further studies
related to steroidogenesis with specimens collected at different periods of the year are necessary, aiming to observe if there
are morphological or hormonal variations in the adrenal glands due to seasonal periods. This information would be of great
importance because it could reflect the behavioral habits of this species.
KEYWORDS:
Endangered species. Fasciculata zone. Glomerular zone. Reticular zone.
INTRODUCTION
The Myrmecophaga tridactyla are mammals
that live at the Cerrado biome (CUNHA et al., 2015)
and are popularly known in Brazil as the Giant
Anteater (ROSA et al., 2012). They are members of
Superorder Xenarthra belonging to family Pilosa
(SANCHEZ et al., 2013), previously described as
family Mymercophagidae (SHAW; MCDONALD,
1987; ROSSI et al., 2012). This family of mammals
constitute an important conservation group, because
is highly vulnerable, according to Brazilian Official
List of Species Threatened with Extinction (CRUZ
et al., 2013; IBAMA, 2016) and “near threatened”
in Red List of the International Union for
Conservation of Nature (ROSSI et al., 2012; CRUZ
et al., 2013; IUCN, 2015) and since 2003 is included
in the Appendix II of the Convention on
International Trade in Endangered Species
(SANCHES et al., 2013). Although in recent years,
M. tridactyla is threatened with extinction, it had a
much wider geographical distribution in past times,
inhabiting even other sub-continents, such as North
America according to the discovery of fossil records
(SHAW; MCDONALD, 1987).
The adrenal glands can undergo adjustment
due to various stress factors (PARKER et al., 2011).
In mammals, each adrenal gland is composed of two
structures: the cortex, which is originated from
embryonic mesoderm and the medulla, which is
originated from embryonic neurectoderm. Each part
of the adrenal gland has different cell types: the
cortex cells produce mineralocorticoid,
glucocorticoids and sexual steroid hormones
(SANTOS et al., 2016) while in the medulla,
chromaffin cells produce catecholamine and
neuropeptides (KEMPNÁ; FLÜCK, 2008; QIU et
al., 2012).
Due to the importance of the adrenal glands
to the homeostasis of animals, especially those
exposed to large amounts of stress factors, this study
aimed to describe for the first time, the macroscopic
Received: 17/05/16
Accepted: 05/10/16

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Biosci. J., Uberlândia, v. 32, n. 6, p. 1559-1566, Nov./Dec. 2016
and microscopic anatomy of the adrenal glands in
M. tridactyla, providing data for future studies
related to the production of steroid hormones in
these glands.
MATERIAL AND METHODS
In the present study, adrenal glands from 14
specimens of M. tridactyla were studied. All
specimens were collected at the SACCAS (Sector of
Clinical and Surgical Attendance of Wild Animals)
of the Veterinary Hospital “Dr. Halim Atique”,
responsible for providing support for Environmental
Military Police of São Paulo and IBAMA -
Brazilian Institute of Environment and Renewable
Natural Resources. The research was duly approved
by the Bioethics Committee of the School of
Veterinary Medicine and Animal Science of the
University of São Paulo with the protocol number
3016/2013.
The adrenal glands were photodocumented
in situ for topographical description of the organ.
Then, adrenals were weighted using a precision
scale (Slim
®
high precision) and measured by
Mitotuyo
®
precision calipers to perform comparison
between the glands of the right and left antimeres.
The analysis of variance using the GraphPad InStat
program to obtain the mean and standard deviation
was performed. Cramer-von Mises test for
normality checked homoscedasticity between the
variables; Tukey comparison average test provided
morphometric rates. Biometrics variables are
unstable (CV≤15%) at significance p<0.05.
Adrenal glands were sectioned in the
sagittal plane, and the hemi-adrenal glands were
fixed in 10% formaldehyde solution for microscopic
analysis, looking for morphological differences
between left and right adrenals and distinct regions
of the gland. Subsequently, the glands were
dehydrated in increasing concentrations (from 50%
to 100%) of ethanol and cleared in xylene for later
inclusion in paraffin. Paraffin blocks were sectioned
and samples with 5µm of thickness were stained
with H/E (hematoxylin/eosin). The microscopic
photodocumentation was performed using
photomicroscope Olympus BX61VS. The
nomenclature of the anatomical structures was based
on Nomina Anatomica Veterinaria (2012).
RESULTS
Macroscopic analysis
Pairs of the adrenal glands (left and right) of
all specimens were positioned in the cranial
extremity of the kidneys and presented syntopy.
They were medially related to the caudal vena cava;
with the pancreas, liver and rectum on the left
antimere; and, with the duodenum and jejunum on
the right antimere (Figure 1).
Figure 1. Image of the adrenal gland in the abdominal cavity of M. tridactyla. The left kidney evolved by renal
capsule (r) in proximity to the left adrenal gland (g) and the jejunum (j). Bar: 1cm.
The right adrenal had an elongated shape
while the left adrenal had a triangular shape.
Different results regarding morphology of the right
and left adrenal gland were also found for weight
and all dimensions analyzed (length, width and
thickness).
After the sagittal section, it was found a
thick yellowish color capsule lining the organ and
cortical and medullar regions with evident blood
vessels in the medullar tissue. The cortex divisions
were not observed macroscopically (Figure 2).

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Biosci. J., Uberlândia, v. 32, n. 6, p. 1559-1566, Nov./Dec. 2016
Figure 2. Image of the adrenal glands of the M. tridactyla. A: anatomical conformation of the right (R) and left
(L) adrenal. Bar: 1cm. B: cortical region (c), medullar region (m) and capsule (arrows) of the
sectioned adrenal. Bar: 0.5cm.
The weight was 4.765±0.129g for the right
adrenal and 3.975±0.213g for the left adrenal. The
length was 4.50±0.14cm for the right adrenal and
4.28±0.11cm for the left adrenal. The width was
2.60±0.13cm for the right adrenal and 2.37±0.12cm
for the left adrenal. The thickness was 0.45±0.11cm
for the right adrenal and 0.68±0.14cm for the left
adrenal. Statistical differences (p<0.05) between
right and left adrenals for all values analyzed were
observed.
H/E stained images showed a dense capsule
composed by modeled dense connective tissue
lining the organ. Below this capsule, from the
outermost region to the innermost region, it was
possible to observe a cortical region, divided into
glomerular, fasciculata and reticular zones and a
medullar region occupying the center of the organ.
The glomerular zone presented cellular
clusters arranged in oval shape, while the fasciculata
zone had cells arranged in cords. The reticular zone
was composed of cells spread across the large
amount of non-modeled dense connective tissue
with presence of blood vessels. The medullary
region was rich in blood vessels and chromaffin
cells (Figure 3).
The tissue slices stained with Trichrome of
Gomori revealed the presence of collagen fibers in
the dense capsule of the organ and within the
medullar region. The glomerular zone had little
amount of collagen fibers and more clustered cells
compared to other zones in the adrenal cortex. The
fasciculata zone showed little collagen fibers. On
the other hand the reticular zone showed large
amount of collagen fibers (blue) and blood vessels,
while the medullar region had more evident cellular
nucleus when compared to cells of the fasciculata
and reticular zones. At the center of the medullar
region it was possible to observe a large area with
collagen fibers and large blood vessels. Surrounding
this area, it was possible to note an area with less
collagenous fibers and an area with higher amount
of these fibers (Figure 4).

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Figure 3. Photomicrograph of the adrenal gland of M. tridactyla stained with H/E. A: capsule (arrow); zones:
glomerular (arrowhead), fasciculata (f) and reticular (r) in the cortical region; medullar region (m).
Bar: 500µm. B: capsule (c); zones: glomerular (g) and fasciculata (f). Bar: 50µm. C: fasciculata zone
(f). Bar: 50µm. D: reticular zone (r) with blood vessel (*). Bar: 50µm. E: medullar region (arrow)
with blood vessel (V). Bar: 50µm.
Figure 4. Photomicrograph of the adrenal gland of M. tridactyla stained with Trichrome of Gomori. A:
reticular (r) and fasciculata (f) zones. Bar: 100µm. B: capsule (c) glomerular (g) and fasciculata (f)
zones. Bar: 100µm. C: reticular zone (r) of the cortical region and medulla (m). Bar: 100µm. D:
medullar region with a region rich in modeled dense connective tissue (mdct) and blood vessels with
large-diameter (arrows). It was possible to observe an area with non-modeled dense connective
tissue (nmdct). Bar: 100µm.
DISCUSSION
The adrenal glands found in M. tridactyla
are positioned in the cranial extremity of the kidney
and related medially to the caudal vena cava. These
characteristics follow the topographic location
described in other wild mammals such as rodents
Lagostomus maximus (RIBES, 1999), Myocastor
coypus (MACHADO et al., 2002; CULAU et al.,
2008), Dasyprocta agouti (NEVES et al., 2007),
Cavia porcellus (COOPER; SCHILLER, 1975) and
Galea spixii (SANTOS et al., 2016), and domestic
animals such as dogs, cats and horses (REECE et
al., 2005).

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In current study, the adrenal glands of M.
tridactyla with different formats and sizes when
comparing right and left glands were found. The
right gland had elongated shape while the left gland
had triangular shape. Additionally, measurements
were statistically higher (p<0.05) in the right glands,
except for thickness. These results differ from
studies by Machado et al. (2002) in Myocastor
coypus and Santos et al. (2016) in Galea spixii. In
this study, the authors observed asymmetry between
the right and left glands. The right adrenal had
triangular shape and smaller volume compared with
the left gland, which had elongated shape in Galea
spixii (SANTOS et al., 2016).
In this regard, with respect to morphology,
anatomy and secretion products, it is known that the
adrenal glands may differ between the different
classes and animal species. In fishes, the chromaffin
tissue and adrenocortical may be separated; in birds,
these tissues are fused; the adrenal cortex of
mammals is divided into zones, but the glomerulosa
zone is not perceived in some of them, such as
lemurs, monkeys and mice; in dogs and guinea pigs
adrenocortical tissue is more abundant than
chromaffin tissue (BENTLEY, 1982).
In relation to the different zones of the
adrenal cortex in M. tridactyla, it was found that the
first and outermost layer is the glomerular zone,
located just under the capsule (consisting of
connective tissue), which surrounds the organ. It has
as main characteristic, the presence of cells arranged
in oval groups very attached and with reduced
intracellular spaces, similarly to rats (CHANG et al.,
2011), Galea spixii (SANTOS et al., 2016) and
Gerbilus tarabuli (SAADI; LEBAILI, 2012); the
second layer is the fasciculata, characterized by
columns of vacuolated cells as in rats (CHANG et
al., 2011.) and Galea spixii (SANTOS et al., 2016.);
and the third and last zone is the reticular,
containing in its parenchyma irregular cell cords,
anastomosis and randomly arrangement, similar to
that found in Lagostamus maximus (RIBES et al.,
1999) and Galea spixii (SANTOS et al., 2016).
Below the reticular zone of the cortical region is the
medullar region, which is composed of large
chromaffin cells and numerous blood vessels,
similar to that described in Cavia porcellus
(KACZMARCZYK; KMIEC, 2004) and Galea
spixii (SANTOS et al., 2016).
Regarding the division of regions of the
adrenal cortex of M. tridactyla, it was found less
evident glomerular zone in relation to fasciculata
and reticular zones. Then, stereological studies in
order to confirm these findings were required
because the dimensions of the cortical zones could
be related to different demands in the production of
different steroid hormones. Hîncu et al. (2006),
described that in Cavia porcellus exposed to stress,
structural changes occur in the cortex due to the
adaptive capacity of adrenal gland to stress factors,
because initially an adaptive process is characterized
by morphological and functional changes in order to
life maintenance.
The adrenal glands have an important role
due enzymatic mechanisms able to synthesize
cholesterol and convert it into different steroid
hormones, including sexual hormones (DI RIO et
al., 1994; SANTOS et al., 2016); however,
corticosteroids are the most important adrenal
steroid hormones, both physiologically and
quantitatively (Whitley et al., 1994).
Several studies have attempted to
demonstrate the differentiation of the synthesis of
steroid hormones in the different zones of the
adrenal cortex in mammals. As example, glomerular
zone synthesizes mineralocorticoid (aldosterone),
the fasciculata zones produces glucocorticoids and
the reticular zone produces sexual steroid hormones
C19 (androgens) in humans and primates (CHANG
et al., 2011), but not in rats and mice (VAN
WEERDEN et al., 1992; PIGNATELLI et al., 1998;
KEMPNÁ; FLÜCK, 2008). However, Shinzawa et
al. (1988) in Cavia porcellus and Santos et al.
(2016) in Galea spixii demonstrated that androgen
production site is mainly the fasciculata zone.
Already Pignatelli et al. (1998) demonstrated that in
rats, the androgen production is more present in the
glomerular zona than in the fasciculata zone.
Considering the difficulty to find relevant
quantity of specimens for morphological studies due
to vulnerability in conservation of the species as M.
tridactyla, future studies related to steroidogenesis
with specimens at different periods of the year will
elucidate if the adrenal glands have seasonal
variations in its morphological conformation or
production of adrenal hormones resulting from these
changes, and these data would be of great
importance because it could reflect the behavioral
habits in this species.
In conclusion, the right adrenal glands had
larger measurements of weight, length and width
than the left gland, however, the thickness of the
right gland was lower than the left. By microscopic
analysis, a modeled dense connective tissue capsule
lining the organ was observed. Below this capsule,
from the outermost to the innermost layer, it was
possible to evidence, a cortical region, divided into
glomerular, fasciculata and reticular zones and a
medullar region rich in blood vessels occupying the
center of the organ.

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ACKNOWLEDGEMENTS
The authors thank the Sector for Clinical
Surgical Attendance (SACCAS) of the Veterinary
Hospital "Dr. Halim Atique "for the donation of
animals and to Fundação de Amparo à Pesquisa do
Estado de São Paulo for financial Support.
RESUMO:
O Myrmecophaga tridactyla (família Pilosa), conhecido popularmente no Brasil como Tamanduá-
Bandeira, é uma espécie classificada como ameaçada de extinção pelos principais órgãos de levantamento e preservação
da biodiversidade no mundo. As glândulas adrenais são importantes órgãos, relacionados com a homeostasia dos animais.
Neste estudo, objetivou-se descrever a morfologia das glândulas adrenais de M. tridactyla, fornecendo dados para futuros
estudos relacionados à produção de hormônios esteroides em espécimes expostos a diferentes fatores de stress. Esta
pesquisa traz a análise das glândulas adrenais em 14 espécimes de M. tridactyla, as quais foram mensuradas,
fotodocumentadas, processadas e analisadas por microscopia de luz. Encontrou-se que as glândulas adrenais pares estavam
posicionadas na extremidade cranial dos rins e relacionadas medialmente com a veia cava caudal. Sendo que, a glândula
adrenal direita possuía formato mais alongado que a glândula adrenal esquerda, a qual apresentou formato piramidal ou
triangular. A massa da glândula adrenal direita foi de 4,765±0,129g, enquanto a esquerda pesou 3,975±0,213g. O
comprimento foi de 4,50±0,14cm para a glândula direita e 4,28±0,11cm para a esquerda. A largura foi de 2,60±0,13cm
para a glândula direita e 2,37±0,12cm para a esquerda. A espessura da glândula direita foi de 0,45±0,11cm e da esquerda
foi 0,68±0,14. Foram observadas diferenças estatísticas (p<0,05) entre as glândulas direitas e esquerdas em todas as
dimensões analisadas. Com auxílio de microscopia de luz observou-se uma cápsula de tecido conjuntivo denso modelado,
revestindo o órgão. Abaixo dessa cápsula, foi possível evidenciar, da camada mais externa para a mais interna, uma região
cortical, dividida em zonas glomerular, fasciculada e reticular, com uma região medular ocupando o centro do órgão.
Futuros estudos relacionados à esteroidogênese adrenal com espécimes em diferentes épocas do ano poderiam demonstrar
se as glândulas adrenais apresentam variações sazonais em sua conformação morfológica ou na produção de hormônios
adrenais decorrentes dessas variações, sendo que, estes dados seriam de grande importância, pois poderiam refletir os
hábitos comportamentais nesta espécie.
PALAVRAS CHAVE:
Animais em risco de extinção. Tamanduá-Bandeira. Zona fasciculada. Zona
glomerular. Zona reticular.
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