First record of leucism in puma from Serra dos Órgãos National Park, Brazil

Abstract

Although polymorphic phenotypes are common in wild felids, leucism is a rather rare characteristic and consists in the general cleaning of the animal's coat, assigning a white coloration pattern. This characteristic is genetically controlled, with reces-sive inheritance. We present the first record ever of leucism in pumas Puma concolor recorded in wild populations, from Serra dos Órgãos National Park, Atlantic Forest of southeastern Brazil. This record was documented with a great sampling effort, with camera traps from 2010 to 2016, being registered only in two of the twenty-four sampling stations in 2013. The record of this rare phenotype will be the baseline for later studies on the genetic basis of leucism and the adaptive relevance of this phenotypic characteristic in wild cat populations.

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N° 68 | Autumn 2018

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CECÍLIA CRONEMBERGER1,2, FABIANE DE AGUIAR PEREIRA1, ANA ELISA DE FARIA BACELLAR1
AND LUCAS GONÇALVES DA SILVA3
First record of leucism in
puma from Serra dos Órgãos
National Park, Brazil
Although polymorphic phenotypes are common in wild felids, leucism is a rather rare
characteristic and consists in the general cleaning of the animal's coat, assigning a
white colouration pattern. This characteristic is genetically controlled, with reces-
sive inheritance. We present the first record ever of leucism in pumas Puma concolor
recorded in wild populations, from Serra dos Órgãos National Park, Atlantic Forest of
southeastern Brazil. This record was documented with a great sampling effort, with
camera traps from 2010 to 2016, being registered only in two of the twenty-four sam-
pling stations in 2013. The record of this rare phenotype will be the baseline for later
studies on the genetic basis of leucism and the adaptive relevance of this phenotypic
characteristic in wild cat populations.
Polymorphic phenotypes are common in wild
cats. There are records of iconic cases such
as melanism in leopards and jaguars called
‘black panthers’ (Eizirik et al. 2003, Schnei-
der et al. 2012, Silva 2017, Silva et al. 2017)
and leucism in white tigers and lions (War-
rick 2010, Cho et al. 2013, Xu et al. 2013).
Leucism can be defined as the total lack of
pigmented cells in the fur in some areas
or all the body, which rarely affects hair-
less body parts such as the nose, feet, and
exposed skin but never affects the iris, while
albinism is the impairment of the bioche-
mical pathway of melanin production that
affects all body parts, including hair, eyes
and skin (Arriaga-Flores et al. 2016, Utzeri
2017). The main distinctive feature of albino
animals is pink eyes, because without me-
lanin in the body, it is the colour that comes
from blood vessels behind the eye (Sokos
et al. 2018). These polymorphic phenotypes
are genetically controlled by several genes,
dominant in some cases, and recessive in
others (Eizirik et al. 2003, Utzeri 2017) and
can play adaptive roles in certain ecological
conditions (Caro 2005, Silva et al. 2017).
The main adaptive functions of colouration in
mammals, as a general rule, are concealment,
communication, and regulation of physiologi-
cal processes, but these mechanisms are still
poorly understood in felids (Caro 2005). Albi-
nism and leucism are commonly considered
a disadvantage for wild animals for various
reasons, such as their higher visibility to pre-
dators, visual pathologies and immunological
defects (Abreu et al. 2013, Sokos et al. 2018).
However, some authors argue that survival
of albinos does not differ from that of non-
albinos of cryptic or nocturnal species and of
those that have few predators (Abreu et al.
2013). Albino or leucistic specimens may not
be so attractive for breeding or be treated as
foreigners by their co-specifics (Sokos et al.
2018). Because such colour abnormalities
are rare and poorly studied, their effect in
the fitness and survival of the affected indi-
viduals is not yet known (Caro 2005, Abreu et
al. 2013, Sokos et al. 2018). Monitoring this
polymorphism may contribute to the identifi-
cation of the populations exposed to stress or
inbreeding (Bensch et al. 2000).
Only for two species of wild cat leucism is
presently described and already genetic ba-
sis defined: in tigers Panthera tigris the white
colouration pattern is associated with the
A477V gene that causes a dysfunction in the
transporter protein SLC45A2, promoting the
loss of function for pheomelanin (Xu et al.
2013); and in lions Panthera leo it is caused
by a mutation in the TYR260G>A gene, in the
same way inducing the white background
colour phenotype (Cho et al. 2013). This trait
has a recessive inheritance pattern, with very
low frequency and appears to be a neutral
character in wild populations (Xu et al. 2013).
The puma is the most widely distributed wild
cat in the Neotropics, occurring from northern
Canada to the southern tip of South Ame-
rica, from sea level to 5,800 m (Sunquist &
Sunquist 2002). This large felid is found in a
broad range of habitats, in all forest types,
shrublands, grasslands and savannas, as well
as lowlands and montane deserts (Sunquist
& Sunquist 2002). Throughout its distribution
this species is categorised by the IUCN as
Least Concern (Nielsen et al. 2015), but in
Brazil it is considered as Vulnerable (Azevedo
et al. 2013). Pumas are threatened by habitat
loss and fragmentation, and poaching of their
wild prey base (Novack et al. 2005). They are
persecuted across their range by retaliatory
hunting due to livestock depredation and the
fear that they pose a threat to human life
(Treves & Karanth 2003).
Adult pumas are uniformly coloured with no
body marks (Werdelin & Olsson 1997). Adult
dorsal pelage is usually tan but may appear
greyish, reddish, or brownish, and ventral
Fig. 1. Map of the study area, Serra dos Órgãos National Park (PARNASO) in Rio de Janei-
ro State, southeastern Brazil, depicting the locations of each camera trap sampling station
(orange circles) and the locations where the leucistic phenotype was registered (red circles).
original contribution

CATnews 68 Autumn 2018
39
pelage ranges from creamy to white (Trani &
Chapman 2007). The tail tip and the back of
the ears are brown to black, and the white
muzzle is bordered by a black line. According
to Sunquist & Sunquist (2002), temperate
pumas tend to have paler, light greyish co-
louration, while tropical pumas tend to have
brighter, reddish tones. There is no record of
any melanistic or leucistic phenotype for this
species in wild populations, although albi-
nism has been rarely recorded (Sunquist &
Sunquist 2002).
Serra dos Órgãos National Park (PARNA-
SO) is located in the mountainous area of
Rio de Janeiro State, southeastern Bra-
zil, about 100 km from Rio de Janeiro city
(-22°23’36.96’’ – -22°34’57.72’’ N and
-43°10’57.72’’ – -42°58’43.68’’ E). The park
protects 200.24 km² of Atlantic Forest, one the
most threatened biodiversity hotspots of the
world (Rezende et al. 2018), in a very complex
scenery, surround-ed by rapidly growing cities
and various sources of pressure, such as pol-
luting industries and agrochemical-based ag-
riculture (Cronemberger & Viveiros de Castro
2009).
According to Thorntwaite’s classification, cli-
mate in PARNASO is mesothermic and super
humid, with little or no water deficit (FIDERJ
1978). Rainfall presents a seasonal distribu-
tion, with concentration in summer (Decem-
ber to March) and dry season in winter (June
to August). This area has the highest rainfall
of Rio de Janeiro state, which varies from
1,500 to 3,000 mm annually, due to orograph-
ic rainfall (Davis & Naghettini 2000).
The park shows a very steep relief that
ranges from 80 to 2,275 m. The considerable
variation in altitude contributes to maintain a
high variety of micro habitats that favours the
occurrence of great biological diversity. The
vegetation is mainly dense ombrophilous for-
est (Veloso et al. 1991), which can be divided
into four phytophysionomies, according to al-
titude (Rizzini 1959). Over 2000 plant species
have been found in the area (Rizzini 1959).
The fauna is similarly diverse, and the most
species-rich vertebrate groups are birds, with
over 460 species, and amphibians, with over
100 species (Cronemberger & Viveiros de
Castro 2009). A recent study listed 99 mam-
mal species for the area, including five wild
cats with recent records (Puma concolor, Her-
pailurus yagouaroundi, Leopardus pardalis,
L. wiedii and L. gutullus; Cronemberger et al.
in prep). The jaguar Panthera onca was once
present but is considered locally extinct in
this area, along with three other large-sized
mammals (Cunha 2007).
Park staff conducted an extensive mammal
monitoring project using camera traps from
2010 to 2016, with a total effort of 18,252
camera trap days, which has recorded 24
species of medium and large sized mammals
(Pereira 2017). Puma was the second most
registered species in the sampling period,
being the opossum Didelphis aurita the first
one (Pereira 2017).
In 2013, we used 48 camera traps (Tigrinus®
and Bushnell® models) in 24 sampling
stations each consisting of 2 camera traps
facing each other, in an attempt to record
both left and right sides of the animals to
be able to identify individuals. Sampling
stations were located about 3 km apart from
each other (Fig. 1). The total sampling effort
was of 4,792 camera trap days (from April to
December 2013).
We obtained 33 independent records (at least
one hour apart from each other) of puma
from 11 different sampling stations. In this
dataset, we found four records of an indivi-
dual showing leucistic characteristics: its fur
was greyish white and it did not show typical
puma colouring on the tip of the tail, behind
the ears or around the mouth. This individual
was identified as a male and a young speci-
men (Fig. 2). This same specimen was cap-
tured by two different camera trap stations
located about 4.5 km apart (Fig. 2). Both sites
were located in dense ombrophylous forest;
MAE was located in 1,054 m of elevation and
CX was located in 1,259 m (Fig. 1). Because
Fig. 2. Leucistic male puma recorded in two different sampling stations of PARNASO: (A) MAE July 5th 2013, (B) MAE in August 13th
2013, (C) CX in July 21st 2013 and (D) CX in September 7th 2013 (Photos ICMBio).
first record of leucism in puma, Brazil
A B
C D

CATnews 68 Autumn 2018
40
of the proximity of the sites, and considering
the rarity of leucism in this species, assuming
it was a single individual seems more parsi-
monious than considering that two leucistic
individuals would appear in the study area at
the same time.
The animal visited both sites repeatedly: re-
cords show him on MAE on 5. July; then in CX
on 21. July; then back to MAE on 13. August
and back to CX in 7. September. In MAE, the
leucistic individual was the only puma record-
ed. In CX, there were other three records of pu-
mas (on 7. and 15. July and 2. September), but
different from the previous mentioned records,
these were made at night, using infrared light,
and resulted in poorer quality pictures which
do not allow to check the animal's fur colour-
ation. Nevertheless, considering the animal’s
size and structure, it does seem like the same
individual, but, being conservative, we have
not considered these records. Moreover, it is
noteworthy that between the two sites where
the leucistic individual was recorded lies a
third sampling station (CA2) where a female
and another male were recorded during the
same period, showing that the leucistic indi-
vidual may have crossed their territory mul-
tiple times to move between MAE and CX.
Unfortunately, the leucistic animal was not
seen in the following years, despite the effort
of 5,531 camera trap days in 2014, 2,023 in
2015 and 1,561 in 2016, including the same
sites where this phenotype was recorded in
2013. The two sites where it was recorded
were occupied by ancestral coloured pumas
between 2014 and 2016.
Despite the species’ wide distribution, this
is the first record ever of leucism for puma in
wild populations. We did not find any records
of leucism in this species, either in wild or
captive populations, described in the scienti-
fic literature. The next step of this study will
be to locate this individual, live capture it and
obtain a biological sample, aiming to identify
the leucism mutation in this species. Addi-
tionally, we hope to compare this genetic data
with the identified mutation for white tigers
(Xu et al. 2013) and lions (Cho et al. 2013) to
test if these different mutations have arisen
independently. As this record is very rare
and uncommon, this animal can be treated
as a treasure and opens up new avenues to
investigate this colouration polymorphic phe-
notype in wild cats and its ecological implica-
tions. Considering the recessive nature of leu-
cism (Utzeri 2017), the decreasing population
trend of pumas (Azevedo et al. 2013, Nilsen
et al. 2015) and the fragmented landscape of
the Atlantic Forest (Rezende et al. 2018), the
appearance of this leucistic specimen may be
an indicator of inbreeding or environmental
stress (Bensch et al. 2000) in the local popula-
tion, which is of conservation concern.
Acknowledgements
Authors would like to thank PARNASO’s staff for par-
ticipation in field expeditions and logistic support;
CENAP/ICMBio and LabVert/UFRJ for camera-trap
loans; Ernesto Viveiros de Castro, Vitor Pimentel,
Jorge Luiz do Nascimento, Eduardo Eizirik, Martín
Alejandro Montes, Felipe Pessoa, Ronaldo Morato,
Rogério de Paula and Beatriz Beisiegel for helpful
discussions;and ICMBio for research authorization
(number 24613). We thank PIBIC/ICMBio and PI-
BIC/UFRJ for undergraduate scholarships. We also
thank Maria de las Mercedes Guerisoli and Laura
Bertola for helpful comments in the editorial pro-
cess. This research was funded by ICMBio, CNPq,
PPBio/CNPq – Rede BioM.A., FAPERJ and FACEPE.
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1 Instituto Chico Mendes de Conservação da Bio-
diversidade, Parque Nacional da Serra dos Ór-
gãos, Av. Rotariana s/n, Teresópolis, RJ, Brazil,
25960-602
2 Universidade do Estado do Rio de Janeiro, Pro-
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3 Universidade Federal Rural de Pernambuco, De-
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<ceciliacronemberger@gmail.com>
<lucas_gonc@yahoo.com.br>
ROLAND BÜRKI1 AND URS BREITENMOSER1
Inaugural Range State meet-
ing for the joint CMS–CITES
African Carnivores Initiative,
5–8 November 2018 in Bonn,
Germany
In 2014, the Convention on the Conservation
of Migratory Species of Wild Animals CMS
and the Convention on International Trade in
Endangered Species of Wild Fauna and Flo-
ra CITES developed a joint work programme
for the period 2015–20201. It aims to perform
“joint activities addressing shared species
and issues of common interest”. Subse-
quently, the Secretariats of both Conventions
proposed the establishment of a Joint CMS
– CITES African Carnivores Initiative (ACI;
CMS & CITES 2017), covering the African lion
Panthera leo, leopard Panthera pardus and
cheetah Acinonyx jubatus, which are listed
under both Conventions, and the African wild
dog Lycaon pictus listed under CMS (CITES
2017, CMS 2018). The proposal was en-
dorsed by the 12th Conference of the Parties
to CMS and the task of establishing the ACI
was formally given to the Secretariat in Deci-
sion 12.60 (CMS 2017). The CITES Secretariat
does not yet have a mandate beyond the joint
working programme, as there has not been a
CoP since the development of the proposal.
However, it is expected that at the upcoming
18th CITES CoP in May 2019 in Colombo, Sri
Lanka, the ACI will be discussed.
The 1st Meeting of Range States for the Joint
CMS – CITES African Carnivore Initiative
ACI1 took place at the UN Campus in Bonn,
Germany from 5 to 8 November 2018. Repre-
sentatives of 31 Range States attended the
conference (Fig. 1 & 2; CMS & CITES 2018);
Fig. 1. Attendants of the 1st Meeting of Range States for the Joint CMS – CITES African Carnivores Initiative (Photo UNEP–CMS).