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Genetic Guidelines for Captive Breeding and Reintroductions of the Endangered Black-Fronted Piping Guan, Aburria jacutinga (Galliformes, Cracidae), an Atlantic Forest Endemic

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  • Universidade Federal de São Carlos, campus de Sorocaba

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The survival of a number of birds rely on captive breeding and reintroduction into the wild, but captive populations are often small and can be exposed to the negative effects of inbreeding and genetic drift. Then, managers are concerned not only with producing as much offspring as possible, but also with the retention of the maximum genetic variability within and between populations. The Black-fronted Piping Guan, Aburria jacutinga, is an endangered cracid endemic to the Atlantic Forest of southeastern South America. Because of its conservation status and functional importance, a captive breeding program started independently, mainly in three aviaries, in the decade of 1980. Although they have supplied animals for reintroductions, genetic variability aspects have never been considered. Here we addressed levels of genetic variability within and between these aviaries. Bayesian clustering analyses revealed two lineages. Inbreeding was not detected, although we found evidences for a recent bottleneck in one of the aviaries. Then, our main management recommendations are: i) reintroducing the species in areas where it has been extinct is more prudent than supplementing natural populations, as it could involve risks of disrupting local adaptive complexes; ii) as far as inbreeding can be avoided, the captive groups should be managed separately to minimize adaptation to captivity; iii) crossbreedings in pre-release generations could improve reintroduction success; and iv) a studbook should be implemented. As populations of Black-fronted Piping Guan from conservation units are progressively declining, these captive genetic repositories may gain importance in a near future. Zoo Biol. XX:XX-XX, 2016. © 2016 Wiley Periodicals, Inc.
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RESEARCH ARTICLE
Genetic Guidelines for Captive Breeding and
Reintroductions of the Endangered Black-Fronted
Piping Guan, Aburria jacutinga (Galliformes,
Cracidae), an Atlantic Forest Endemic
Paulo R.R. Oliveira-Jr.,
1
Mariellen C. Costa,
2
Luis F. Silveira,
3
and Mercival R. Francisco
4
*
1
Programa de P
os-GraduaSc~
ao em Diversidade Biol
ogica e ConservaSc~
ao, Universidade Federal de S~
ao Carlos,
Campus de Sorocaba, Sorocaba, S~
ao Paulo, Brazil
2
Programa de P
os-GraduaSc~
ao em Ecologia e Recursos Naturais, Universidade Federal de S~
ao Carlos, S~
ao
Carlos, S~
ao Paulo, Brazil
3
SeSc~
ao de Aves, Museu de Zoologia da Universidade de S~
ao Paulo, S~
ao Paulo, Brazil
4
Departamento de Ci^
encias Ambientais, Universidade Federal de S~
ao Carlos, Campus de Sorocaba, Sorocaba,
S~
ao Paulo, Brazil
The survival of a number of birds rely on captive breeding and reintroduction into the wild, but captive populations are often
small and can be exposed to the negative effects of inbreeding and genetic drift. Then, managers are concerned not only with
producing as much offspring as possible, but also with the retention of the maximum genetic variability within and between
populations. The Black-fronted Piping Guan, Aburria jacutinga, is an endangered cracid endemic to the Atlantic Forest of
southeastern South America. Because of its conservation status and functional importance, a captive breeding program started
independently, mainly in three aviaries, in the decade of 1980. Although they have supplied animals for reintroductions,
genetic variability aspects have never been considered. Here we addressed levels of genetic variability within and between
these aviaries. Bayesian clustering analyses revealed two lineages. Inbreeding was not detected, although we found evidences
for a recent bottleneck in one of the aviaries. Then, our main management recommendations are: i) reintroducing the species in
areas where it has been extinct is more prudent than supplementing natural populations, as it could involve risks of disrupting
local adaptive complexes; ii) as far as inbreeding can be avoided, the captive groups should be managed separately to
minimize adaptation to captivity; iii) crossbreedings in pre-release generations could improve reintroduction success; and iv)
a studbook should be implemented. As populations of Black-fronted Piping Guan from conservation units are progressively
declining, these captive genetic repositories may gain importance in a near future. Zoo Biol. XX:XXXX, 2016. © 2016
Wiley Periodicals, Inc.
Keywords: endangered species; Aves; conservation; management; genetic variability
INTRODUCTION
The survival of a growing number of bird species rely
on captive breeding and reintroduction into the wild, and
this conservation strategy applies not only to species that
have become extinct in the wild [Jones et al., 1995; Ralls
and Ballou, 2004; Silveira et al., 2004; Sven and Ryan,
2012], but also to those facing imminent risks of extinction
on nature [Jones et al., 2002; Earnhardt et al., 2014;
VanderWerf et al., 2014; Mounce et al., 2015]. The nal
goal of any ex situ breeding program is to found new
populations or to genetically and demographically reinforce
the populations that still exist in the wild [Conway, 1980;
Grant sponsor: FAPESP; grant numbers: 2008/51197-0, 2010/08586-6,
2010/01251-9, 2011/06210-1; grant sponsor: Brazilian Council of
Research (CNPq); grant sponsor: SAVE Brasil.
Conicts of interest: None.
Correspondence to: Mercival Roberto Francisco, Depto. de Ci^
encias
Ambientais, Universidade Federal de S~
ao Carlos, Campus de Sorocaba,
Rod. Jo~
ao Leme dos Santos, km 110, CEP 18052-780, Sorocaba, SP,
Brazil
E-mail: mercival@ufscar.br
Received 23 October 2015; Revised 13 April 2016; Accepted 11 May 2016
DOI: 10.1002/zoo.21296
Published online XX Month Year in Wiley Online Library
(wileyonlinelibrary.com).
© 2016 Wiley Periodicals, Inc.
Zoo Biology 9999 : 16 (2016)
Frankham et al., 2004; Witzenberger and Hochkirch, 2011].
Because captive populations are often small and founded by
a limited number of individuals, the major concerns of
managers are not only to produce as much offspring as
possible, but also to maintain the genetic integrity of the
populations [Frankham et al., 2004; Frankham, 2010;
Witzenberger and Hochkirch, 2011). Small populations are
more exposed to the negative impacts of inbreeding and
genetic drift, which may translate into reduced survival,
reduced fertility, and limited capability of the populations to
adapt to changing environments [Shaffer, 1987; Frankham
et al., 2004], threatening the success of both captive
breeding and reintroductions [Witzenberger and Hochkirch,
2011]. To tackle this problem, the maximum genetic
variability should be preserved within and between
populations during the captive stage of conservation
programs [Frankham et al., 2004; Witzenberger and
Hochkirch, 2011]. When founders are sampled from various
natural populations, reproduction should be achieved in as
many genetic lineages as possible, and when genetic
variability is low within each lineage, the exchange of
individuals between them generally leads to increased
heterozigosity levels, augmenting the chances of survival of
endangered taxa [Witzenberger and Hochkirch, 2011].
Therefore, understanding the levels of population structur-
ing and levels of genetic variability within the different
lineages provide important guidelines for management
strategies [Nielsen et al., 2007; Nsubuga et al., 2010;
Mukesh et al., 2013].
The Black-fronted Piping Guan, Aburria jacutinga,isa
medium-sized (1.11.4 kg) representative of the family
Cracidae (Galliformes), endemic to the Atlantic Forest from
the Brazilian state of Bahia south to northeastern Argentina and
eastern Paraguay [Sick, 1997; Bernardo and Clay, 2006]. Over
the past 500 years, this biome has been extensively exploited
andonly11.416% of the original 150 million ha has been left.
Of the remaining forested areas, 97% are isolated fragments
smaller than 250 ha, that still experience strong anthropogenic
pressures [Ribeiro et al., 2009]. Furthermore, the remaining
continuums are embedded within the Neotropicsmost
densely-populated region, and recent studies have revealed
that even some of the largest conservation units may not sustain
viable populations of Atlantic Forest medium-sized to large-
bodied vertebrates, especially due to overhunting [Marsden
et al., 2005; Galetti et al., 2009].
In this scenario, large-gape seed disperser birds
like the Black-fronted Piping Guan are especially
vulnerable and their local extinctions often imply in
cascading effects to Atlantic Forest ecosystem functions
[Bernardo et al., 2011; Galetti et al., 2013]. This once
abundant species has been a remarkable game bird for
centuries, which has resulted in its extinction in most of
its original distribution [Sick, 1997; Bernardo and Clay,
2006; Bernardo et al., 2011]. Due to past and ongoing
threats, the species is currently classied as endangered
in the IUCN Red List.
Because of the conservation status and functional
importance of the Black-fronted Piping Guan, a captive
breeding program started in the decade of 1980 mainly in
three Brazilian aviaries: Tropicus, in the state of Rio de
Janeiro; CESP/Paraibuna, in the state of S~
ao Paulo, and
Guaratuba, in the state of Paran
a, all in southeastern Brazil.
These breeding groups were founded independently from an
uncertain number of animals that were conscated by the
police from illegal bird keepers, and by animals being raised
by rural people living nearby Atlantic Forest areas that were
pursued by the aviary owners. These breeding facilities are
collaborators of the Brazilian Action Plan for the Conserva-
tion of Endangered Galliformes [Silveira et al., 2008],
regulated by the Brazilian Federal Government, and over the
last two decades they have supplied animals for the
foundation of a number of small (one to three pairs) or
large (more than 10 breeding pairs) breeding groups in other
aviaries. A small number of animals (34) were exchanged
between Tropicus and Guaratuba more than one decade ago,
and although we cannot assert that individuals with different
origins are not present in other aviaries, to our knowledge
these are the three main genetic repositories of Black-fronted
Piping Guans in captivity. Reintroduction plans have been
conducted in Fazenda Maced^
onia, in the state of Minas
Gerais, and in Reserva Ecol
ogica de GuapiaSc
u, in the state of
Rio de Janeiro (where the species was extinct), using animals
from a breeding group maintained by Crax Foundation, in the
state of Minas Gerais; and in Paraibuna, S~
ao Paulo, using
animals from CESP [Silveira et al., 2008; Bernardo et al.,
2011], and further reintroductions have been planned for a
near future in at least three more areas in which the species
has been locally or ecologically extinct. However, genetic
variability issues have not been considered so far. As the
captive populations were founded decades ago, we predict
that genetic drift could have led to reduced genetic variability
within aviaries. However, if they retain signals of indepen-
dent foundation, crossbreedings could be considered for
rescuing genetic variability within both captive and
reintroduced populations.
The objective of this work was to investigate levels of
genetic structuring between and levels of genetic variability
within the three main genetic repositories of captive Black-
fronted Piping Guans. Specically, we used nine microsatellite
loci and Bayesian clustering analysis to address the following
questions: 1) is there population genetic structuring between the
breeding groups? 2) are there evidences of inbreeding within
these lineages? 3) are there evidences of recent genetic
bottlenecks? These data will provide valuable information for
conservation planning in this endangered species.
METHODS
Blood Sampling and DNA Extraction
At variable times we have sampled all the breeding
pairs and young animals present in the three aviaries that
compose the main original genetic repositories of the
2Oliveira-Jr. et al.
Zoo Biology
Black-fronted Piping Guan in captivity: CESP/Paraibuna
(from 2007 to 2012) (n¼27), Tropicus (from 2010 to 2012)
(n¼31), and Criadouro de Aves Silvestres Guaratuba
(20112012) (n¼40). From each animal we obtained
approximately 20 ml of blood by venipuncture of the brachial
vein, and blood was preserved in 100% ethanol at 20°C.
DNA was extracted using a standard phenol:chloroform:
isoamilic alcohol protocol [Sambrook et al., 1989].
Genotyping
DNA samples were amplied at ve unlinked
microsatellite loci isolated for Black-fronted Piping Guan
(Aburria 21, Aburria 22, Aburria 44, Aburria 48, Aburria
105) [Costa et al., 2014], and four heterologous loci
developed for Razor-billed Curassow, Pauxi tuberosa (Pauxi
14, Pauxi 22, Pauxi 230, and Pauxi 34) [Sousa et al.,
2013]. Details on loci isolation, PCR conditions, linkage
disequilibrium, and tests for null alleles are described in
Costa et al. [2014]. Forward primers were uorescently
labeled, amplication products were analyzed on an ABI
3730 automated sequencer (Applied Biosystems), and alleles
were scored based on an internal size standard (500 ROX)
using GeneMarker 2.6.0 (SoftGenetics, State College, PA).
Population Structure Analyses
Population structuring and assignment of individuals
to their population of origin were obtained using the
Bayesian clustering method implemented in the software
STRUCTURE 2.3.4 [Pritchard et al., 2000], which assumes
that there are Kdistinct populations, or genetic clusters, each
with a different set of allele frequencies per locus. We used
an admixture model with correlated allele frequencies,
without prior information. We ran 1000,000 MCMC
iterations (discarding 10,000 as burn-in) for each K(16).
Each Kvalue was obtained in ten replicates, and the most
appropriate Kwas dened using the method proposed by
Evanno et al. [2005], implemented in the software
STRUCTURE HARVESTER [Earl and VonHoldt, 2012],
where the true Kis the greatest delta K(DK) averaged across
runs. To assign individuals probabilistically to a certain
cluster, those with membership (q) thresholds of q0.8
were assigned to one cluster, while those with q<0.8 were
considered as admixted [Lecis et al., 2006; Nsubuga et al.,
2010; Mukesh et al., 2013]. Levels of genetic differentiation
between clusters were estimated using the F
ST
of Weir and
Cockerham [1984], implemented in the software FSTAT
2.9.3.2 [Goudet, 1995].
Genetic Variability Within Aviaries
For each aviary, we obtained expected (H
E
) and
observed (H
O
) levels of heterozygosity, and number of
observed alleles (N
A
), using GENEPOP 4.2 [Raymond and
Rousset, 1995]. We inferred occurrence of inbreeding by
assessing levels of hetorizygosity decit using the inbreeding
coefcient (F
IS
) of Weir and Cockerham [1984] implemented
in FSTAT 2.9.3.2 [Goudet, 1995]. The critical levels of
signicance were also obtained with this software, and were
adjusted with the sequential Bonferroni correction for
multiple comparisons [Rice, 1989].
Contemporary Effective Population Sizes and
Recent Bottlenecks
Effective population sizes were estimated for each
aviary using the linkage disequilibrium method implemented
by software NeEstimator, Ver. 2, using the Monogamy
mating option, with a critical value of 0.02 to discard rare
alleles. This method has been demonstrated to perform
satisfactorily when a moderate number of microsatellite loci
is used [Do et al., 2014]. Potential recent bottlenecks were
assessed using the software BOTTLENECK [Piry et al.,
1999], with the two-phase microsatellite mutation model
(TPM), as it is suggested as the most appropriate model for
detecting recent bottlenecks using microsatellites [Piry et al.,
1999]. The statistical signicance of the results were
obtained using Wilcoxon sign-rank tests.
RESULTS
Population Structuring
The Bayesian clustering analyses of STRUCTURE
revealed genetic structuring between the aviaries (Fig. 1),
and STRUCTURE HARVESTER indicated two as the best
Kfor the sample, suggesting two distinct lineages. Cluster 1
(dark gray color) was composed mainly by the individuals
from CESP, and cluster 2 (light gray color) contained mostly
the animals from Tropicus and Guaratuba (Fig. 1). The
Fig. 1. Graphic representation of the two lineages of captive Black-fronted Piping Guan identied using Structure (K¼2). Colors in each
bar represent the proportional membership (q) of each individual.
Managing Black-Fronted Piping Guan 3
Zoo Biology
number of admixted individuals were: two in CESP and
Guaratuba, and six in Tropicus. One individual from
Tropicus and two from Guaratuba were assigned to CESP.
The level of structuring between these two lineages was
highly signicant (F
ST
¼0.18, P<0.0001).
Genetic Variability
Across the three aviaries we found a total of 34 alleles
for the nine microsatellite loci, with the number of alleles per
loci averaging 3.78 (210, 1.7). Mean number of alleles
within aviaries were 2.9, 3.0, and, 3.2 for CESP, Tropicus,
and Guaratuba, respectively. None of the aviaries presented
signicant overall decit of heterozigosity after Sequential
Bonferroni correction (Table 1). All of the aviaries presented
private alleles, being three for CESP, and one for each of
Tropicus and Guaratuba.
Software BOTTLENECK revealed a signicant excess
of heterozygosity only for Tropicus (P¼0.019), suggesting a
recent bottleneck in this aviary. Contemporary effective
population sizes and condence intervals obtained with
NeEstimator were 24.8 (11.470) for CESP, 37.1 (18104.7)
for Tropicus, and 33.2 (19.163.1) for Guaratuba.
DISCUSSION
The three main geneticrepositories of the Black-fronted
Piping Guan in captivity are signicantly structured into two
lineages, each preserving a few private alleles, and these
groups of birds are not inbred. Practical applications of these
ndings involve answering if these groups should still be
managed separately, and if animals to be used in reintroduc-
tions should derive from only one lineage, from a combination
of lineages, or if they should have admixted ancestry.
Captive populations may be structured because they
have derived from populations that were structured in the
wild [Nsubuga et al., 2010; McGreevy et al., 2011; Simons
et al., 2013], or because of founding effects or bottlenecks
that led to random loss of alleles in different captive groups,
even when they are derived from a unique wild population
[Forstmeier et al., 2007]. When structuring in captivity
reects the structuring of natural populations the captive
groups should be managed separately to preserve adaptive
complexes of each region, and only captive groups derived
from each specic population should be used in reintro-
ductions or supplementation plans to avoid disrupting
potential local adaptations [Frankham et al., 2004;
Champagnon et al., 2012]. Presently, it is impossible to
know what is the genetic diversity of the Black-fronted
Piping Guan in the wild because the remaining populations
are scatteredly distributed and capture to get samples enough
for any genetic analysis is not plausible. The evidence for a
recent bottleneck in at least one of the aviaries (Tropicus)
may suggest that genetic stochasticity occurred in captivity
could explain part of the observed levels of structuring, but
the potential inuence of groups that were structured in the
wild also should not be ignored. It has important implications
for releasing planning because when genetic parameters of
native populations are not known, the most prudent
management strategy is avoiding the supplementation of
pre-existing native populations with captive-born animals as
it could incur in disruption of potential local adaptive
complexes [for a review, see Champagnon et al., 2012].
Therefore, we recommend that reintroduction programs
should be differentiated from those of supplementation, and
conducted only after the identication and elimination of the
causes of disappearing of the target species. Deforestation
can be considered as a minor threaten for the Black-fronted
Piping Guan, while hunting is the main threat for the survival
of this species [Bernardo et al., 2011]. This means that in
areas where the species still occurs, other conservation
strategies, such as improving surveillance, would be more
appropriate.
In the face of the lack of information on structuring
of natural populations, we suggest that releasing programs
TABLE 1. Number of alleles (N
A
), observed (H
O
) and expected (H
E
) heterozygosities, inbreeding coefcient (F
IS
), and probability
that F
IS
has differed signicantly from zero (P) for each of the three aviaries that hold the main genetic repositories of the Black-
fronted Piping Guan in captivity
CESP TROPICUS GUARATUBA
Locus N
A
H
O
H
E
F
IS
PN
A
H
O
H
E
F
IS
PN
A
H
O
H
E
F
IS
P
Aburria21 4 0.89 0.70 0.279 0.993 4 0.45 0.43 0.057 0.778 4 0.77 0.74 0.045 0.754
Aburria22 2 0.52 0.50 0.031 0.704 2 0.52 0.46 0.111 0.839 2 0.37 0.37 0.023 0.711
Aburria44 3 0.07 0.07 0.010 1.000 3 0.26 0.54 0.529 0.002 3 0.25 0.55 0.550 0.002
Aburria48 4 0.67 0.55 0.209 0.981 2 0.32 0.27 0.176 1.000 3 0.12 0.14 0.129 0.167
Aburria105 2 0.37 0.45 0.185 0.291 2 0.35 0.50 0.293 0.093 2 0.47 0.48 0.012 0.580
Pauxi1-4 2 0.18 0.17 0.083 1.000 3 0.55 0.66 0.171 0.146 3 0.72 0.67 0.084 0.806
Pauxi2-2 5 0.78 0.68 0.154 0.909 6 0.93 0.82 0.147 0.989 7 0.80 0.72 0.107 0.944
Pauxi2-30 2 0.18 0.17 0.083 1.000 3 0.35 0.31 0.142 1.000 3 0.62 0.57 0.098 0.817
Pauxi3-4 2 0.11 0.48 0.774 0.002 2 0.00 0.32 1.000 0.002 2 0.10 0.49 0.796 0.002
Average 2.89 0.42 0.42 0.002 0.493 3.00 0.41 0.48 0.135 0.009 3.22 0.47 0.53 0.103 0.011
SD 0.99 0.19 0.21 ––0.89 0.18 0.13 ––1.01 0.23 0.14
Critical value after Sequential Bonferroni correction ¼0.002.
4Oliveira-Jr. et al.
Zoo Biology
should give priority to areas where the species has been
locally extinct beyond any reasonable doubt. In these sites,
however, as local adaptations are not known, and often the
habitat has changed e.g. due to deterioration or fragmenta-
tion, a combination of individuals from various captive
lineages, or admixtured animals with high levels of
heterozigosity can increase reintroduction success, as it
improves the chances that at least some of the genetic
complexes are adaptive [Frankham et al., 2004; Frankham,
2008; Robert, 2009; Zeisset and Beebee, 2013]. This seems
to be the case of the three areas in which releasing has
already occurred: Paraibuna and Fazenda Maced^
onia are
forest fragments largely isolated by eucalyptus plantations
[personal observation]. Although GuapiaSc
u is very close to
the forest continuums of Serra do Mar, the species vanished
from this region decades ago. However, animals used in
reintroductions in Paraibuna were exclusively from CESP,
and those reintroduced in Fazenda Maced^
onia and
GuapiaSc
u were all derived from Crax Foundation, whose
lineage was founded mainly by animals from Tropicus and
Guaratuba [R. Azeredo, pers. comm.]. As a consequence,
these reintroduced populations are certainly not represen-
tative of all the genetic variability existing in captivity.
Although the presence of second generation animals
(unmarked animals) at least in Fazenda Maced^
onia
[personal observation] is an indicative of success,
thoroughly monitoring programs have never been con-
ducted, and we suggest that mixing the captive lineages
could increase the long term viability of these and future
reintroduced populations.
Despite population structuring issues, when the differ-
ent captive lineages are inbred crossbreedings are indicated to
rescue the genetic variability and to avoid inbreeding
depression within each lineage [Frankham et al., 2004;
Witzenberger and Hochkirch, 2011]. As we did not nd
evidences for inbreeding, crossbreedings between aviaries do
not seem to be an urgent need. Indeed, maintaining these
lineages separately may contribute to avoiding genetic
adaptations to captivity [Margan et al., 1998; Frankham,
2008). After a number of generations, captive populations
adapt to captive environment, which implies in reduced
reintroduction success [Williams and Hoffman, 2009].
Limiting the number of generations in captivity, e.g. up to
three generations, can minimize genetic adaptation [Araki
et al., 2007; Frankham, 2008], but like the Black-fronted
Piping Guan, many captive breeding programs have
accumulated a greater number of generations. We estimate
that younger Black-fronted Piping Guans have been through
at least six generations of captive breeding, indicating that
adaptation to captivity may have occurred. Then, a plausible
alternative strategy for minimizing this problem involves
maintaining a number of populations separately, so that each
small group retains less genetic variability than the whole
captive population, limiting the capability of each group to
adapt to captivity [Margan et al., 1998; Frankham, 2008]. As
far as levels of inbreeding can be constantly monitored
[Frankham, 2008], this strategy seems to be adequate for the
groups of Black-fronted Piping Guans analyzed here. It is
important to note that the theoretical loss of heterozygosity in
nite populations, assuming constant population size and
random mating, is (1/2N
e
)
t
,wheretis the number of
generations [Wright, 1931; Frankham et al., 2004]. Then,
with a generation time of 3 years for the Black-fronted Piping
Guan, the studied populations might lose from 37 to 50% of
their heterozygosity in 100 years, which is above the
acceptable level of 10% proposed by Frankham et al.
[2004]. It suggests that the implementation of relatedness
analyses and of genealogical recordings to guide pairing
would be essential to minimize future losses of
heterozygosity.
Then, in summary, we propose four main management
guidelines:
Reintroducing the species in areas where it has been extinct is
more prudent than supplementing natural populations;
As far as inbreeding can be avoided within these three captive
groups, they should be managed separately to minimize
adaptation to captivity;
Crossbreedings, however, are indicated for pre-release
generations. Then, pre-release pairs should be formed and
managed separately, e.g. in other aviaries, to avoid
homogenizing the original lineages;
Relatedness analyses and a studbook should be implemented
to avoid future losses of genetic variability.
The lack of inbreeding is surprising after so many
generations in captivity. Because of the limited nancial
support, these private aviaries have tended to reduce the
number of breedingpairs, and in the more dramatic cases, they
can be closed, which may imply in more bottlenecks. The
creation of governmental mechanisms of nancial support for
breeding facilities involved in the conservation of endangered
species is urgently needed in Brazil, as captive breeding has
become the last reduct for a growing number of species
[Silveira et al., 2008]. Today, the management of Brazilian
endangered species has relied mostly on researchers, private
institutions, and non-governmental organizations, with lim-
ited governmental participation. While the populations from
the large Atlantic Forests conservation units are declining
progressively [Bernardo et al., 2011], the genetic repositories
of Black-fronted Piping Guans maintained in captivity can
become very important in a near future.
ACKNOWLEDGMENTS
To Instituto Chico Mendes para a ConservaSc~
ao da
Biodiversidade (ICMBio) for authorizing sample collec-
tions and to the owners/keepers of Criadouro Tropicus,
Criadouro Guaratuba, and CESP/Paraibuna for providing
the samples and logistical support. This research is part of
the recommendations of the Brazilian Action Plan for the
Conservation of Endangered Galliformes, ruled by the
Brazilian Federal government.
Managing Black-Fronted Piping Guan 5
Zoo Biology
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6Oliveira-Jr. et al.
Zoo Biology
... Here we used the Brazilian avifauna to evaluate potential parameters accounting for the existence of ex situ breeding plans for certain threatened birds, and not for others. We considered that the Brazilian avifauna is an ideal study model for addressing the challenges of ex situ conservation because: (i) information on bird conservation status is relatively good compared, for instance, to invertebrates and other groups of vertebrates (Verdade et al., 2012); (ii) Brazil is the richest country on earth in the number of bird species, and at the same time it is the country with the greatest number of threatened avian taxa (BirdLife International, 2021;Pacheco et al., 2021), and (iii) some of the threatened taxa are known to be a target to ex situ breeding plans, while many others are not (Hammer and Watson, 2012;Oliveira-Jr et al., 2016;Francisco et al., 2021). First, we addressed whether levels of threat, diet, body size, and phylogeny could influence in the choice of the endangered taxa by illegal and legal bird keepers not involved in conservation actions. ...
Article
Full-text available
Species have been lost at unprecedented rates. Because only a small fraction of the threatened taxa have been managed under human care, contrasting the characteristics of taxa that have, and have not been targeted to ex situ conservation can reveal the reach of this conservation strategy, and can indicate its main challenges. Here we investigated whether the level of threat, diet, body mass, phylogeny, and previous presence in captivity due to non-conservation purposes could be potential parameters accounting for the occurrence of Brazilian threatened avian species and subspecies in ex situ conservation facilities and for their eligibility to organized ex situ conservation plans. Using Bayesian phylogenetic comparative models we found positive effects of body mass and phylogeny, and a negative effect of insectivorous diet in the occurrence of the taxa in non-conservation facilities. The previous presence in non-conservation facilities, together with phylogeny, diet, and body mass were the main parameters accounting for the occurrence of the threatened taxa in ex situ conservation facilities, and the previous presence in non-conservation facilities and phylogeny explained the existence of organized ex situ conservation plans. This is evidence that conservation breeding facilities have mostly harbored threatened confiscated birds than choosing them based on scientific criteria. We suggest that investing in the development of husbandry techniques, especially for insectivorous passerines, and choosing taxa based on scientific criteria are important challenges that should be on the agenda of conservation managers.
... The expected heterozygosity H e was significantly higher than H o in the captive population of Hume's pheasant. Similar cases were also observed in the captive populations of cracids [60] and Black-fronted piping guan (Aburria jacutinga, Spix, 1825) [61], which is suggestive of possible inbreeding owing to the small population size. This result is consistent with the positive F IS value (mean = 0.153 ± 0.179) and the mean r values in the captive population. ...
Article
Full-text available
Captive breeding programs are crucial to ensure the survival of endangered species and ultimately to reintroduce individuals into the wild. However, captive-bred populations can also deteriorate due to inbreeding depression and reduction of genetic variability. We geno-typed a captive population of 82 individuals of the endangered Hume's pheasant (Syrmati-cus humiae, Hume 1881) at the Doi Tung Wildlife Breeding Center to assess the genetic consequences associated with captive breeding. Analysis of microsatellite loci and mito-chondrial D-loop sequences reveal significantly reduced genetic differentiation and a shallow population structure. Despite the low genetic variability, no bottleneck was observed but 12 microsatellite loci were informative in reflecting probable inbreeding. These findings provide a valuable source of knowledge to maximize genetic variability and enhance the success of future conservation plans for captive and wild populations of Hume's pheasant.
... The expected heterozygosity H e was significantly higher than H o in the captive population of Hume's pheasant. Similar cases were also observed in the captive populations of cracids [60] and Black-fronted piping guan (Aburria jacutinga, Spix, 1825) [61], which is suggestive of possible inbreeding owing to the small population size. This result is consistent with the positive F IS value (mean = 0.153 ± 0.179) and the mean r values in the captive population. ...
Article
Full-text available
Captive breeding programs are crucial to ensure the survival of endangered species and ultimately to reintroduce individuals into the wild. However, captive-bred populations can also deteriorate due to inbreeding depression and reduction of genetic variability. We genotyped a captive population of 82 individuals of the endangered Hume’s pheasant ( Syrmaticus humiae , Hume 1881) at the Doi Tung Wildlife Breeding Center to assess the genetic consequences associated with captive breeding. Analysis of microsatellite loci and mitochondrial D-loop sequences reveal significantly reduced genetic differentiation and a shallow population structure. Despite the low genetic variability, no bottleneck was observed but 12 microsatellite loci were informative in reflecting probable inbreeding. These findings provide a valuable source of knowledge to maximize genetic variability and enhance the success of future conservation plans for captive and wild populations of Hume’s pheasant.
... Discerning between drift and selection is essential to understanding functional consequences of the variants and the effects of environmental pressures. Accurately modeling the bottleneck, genetic drift, and selection has many important applications for humans and other organisms, such as studying the results of natural disasters [30][31][32] , captive breeding [33][34][35] and re-introduction [36][37][38] of animals, especially endangered species 36; 39; 40 , understanding host-pathogen relationships [41][42][43] , and identifying disease patterns 19; 44-48 . ...
Thesis
The increasing number of large-scale sequencing studies has provided unprecedented access to rare genetic variation. Rare variants are often population specific and arose recently, giving unique insight into recent population history. We require innovative population genetics methods to leverage this new information. In Chapter 2, we present a method for estimating changing migration using the distribution of rare variants among populations. We develop a likelihood function based on this distribution to obtain one estimate of the migration rate for variants with a given minor allele count. As the distribution depends only on the migration rate after the mutation-generating event, we compare migration estimates in variants with different minor allele counts to obtain evidence of changing migration. Evaluating our method on simulated data and applying the method to exome sequence data of drug target genes, we identify migration changes as recent as 20 generations in the past and estimate migration rate parameters. In Chapter 3, we develop a flexible mathematical model for population bottlenecks and genetic drift. Using binomial sampling and a stochastic process, we construct a discrete Markov chain with two transition matrices. We apply this approach to sequencing of mitochondrial DNA (mtDNA) of mother-child pairs and estimate the bottleneck size during mtDNA transmission. In a second application, we adapt this model for cell growth experiments. We determine the probability of drift, without selection, producing extreme shifts in allele frequencies during cell replication. At low probabilities, we find evidence of selection and adapt the model to incorporate and estimate a selection coefficient. In Chapter 4, we explore signals of selection in autoimmune disease genes by adapting site frequency spectrum (SFS) tests to whole genome sequencing (WGS) data. We hypothesize loci associated with multiple autoimmune diseases were once selected for protection from pathogens. We calculate these SFS tests across the genome, generating an empirical distribution and applying a rank-based testing procedure for our genes. Our novel approach eliminates ascertainment bias found in genome-wide association studies data, while accounting for population growth and dependency across the genome. We assess the power of this approach and discuss optimal parameters for its application.
... In Australia, between 30 and 34 mammalian taxa have become extinct since European settlement in 1788 (Legge et al. 2018;Woinarski et al. 2015Woinarski et al. , 2019. Conservation biologists utilise a range of methods to manage species, including captive breeding programs that aim to preserve a species in the safety of a managed captive environment (Courtney Jones et al. 2017), often with a view to supplementing or re-establishing wild populations (Frankham 2008;Oliveira et al. 2016). For programs that intend to conduct wild releases, it is vital that animals maintain their natural, wild behaviours in captivity to improve their chance of survival and reproduction upon release (Håkansson and Jensen 2008). ...
Article
Full-text available
The increased availability of genomic resources for many species has expanded perspectives on problems in conservation by helping to design management strategies for threatened species. Tasmanian devils (Sarcophilus harrisii) are an iconic and endangered marsupial with an intensively managed breeding program aimed at preventing extinction in the wild caused by devil facial tumour disease. Between 2015 and 2017, 85 devils from this program were released to three sites in Tasmania to support wild populations. Of these, 26 were known to have been killed by vehicles shortly after release. A previous analysis indicated that increased generations in captivity was a positive predictor of vehicle strike, with possible behavioural change hypothesised. Here we use 39 resequenced devil genomes to characterise diversity at 35 behaviour-associated genes, which contained 826 single nucleotide polymorphisms (24 were non-synonymous). We tested for a predictor of survival by examining three genes (AVPR1B, OXT and SLC6A4) in 62 released devils with known fates (survived, N = 39; died, N = 23), and genome-wide associations via reduced-representation sequencing (1727 single nucleotide polymorphisms [SNPs]), in 55 devils with known fates (survived, N = 38; died, N = 17). Overall, there was little evidence of an association between genetic profile and probability of being struck by a vehicle. Despite previous evidence of low genetic diversity in devils, the 35 behaviour-associated genes contained variation that may influence their functions. Our dataset can be used for future research into devil behavioural ecology, and adds to the increasing body of research applying genomics to conservation problems.
... the most important seed dispersers from the Atlantic rainforest (Galetti et al., 2013), playing a crucial role in this highly endangered biodiversity hotspot (Myers et al., 2000). Currently, five conservation centrers breed this species for reintroduction under the Brazilian Action Plan for the Conservation of Endangered Galliformes (ICMBio, 2008;Oliveira-Jr. et al., 2016). ...
Article
Haemosporidian parasites of the genus Haemoproteus are widespread and can cause disease and even mortality in birds under natural and captive conditions. The Black-fronted Piping-guan (Aburria jacutinga) is an endangered Neotropical bird of the Cracidae (Galliformes) going through a reintroduction program to avoid extinction. We used microscopic examination and partial cytochrome b DNA sequencing to describe a new Haemoproteus species infecting Black-fronted Piping-guans bred and raised in captivity that were reintroduced into the Atlantic rainforest. Haemoproteus (Parahaemoproteus) paraortalidum n. sp. was detected in the blood of 19 out of 29 examined birds. The new species is distinguished from other haemoproteids due to the shape of gametocytes, which have pointed ends in young stages, and due to the presence of vacuole-like unstained spaces in macrogametocytes and numerous volutin granules both in macro- and microgametocytes. Illustrations of the new species are provided. Phylogenetic inference positioned this parasite in the Parahaemoproteus subgenus clade together with the other two Haemoproteus genetic lineages detected in cracids up to date. We discuss possible implications of the reintroduction of birds infected with haemosporidian parasites into the wild. Treatment of Haemoproteus infections remains insufficiently studied, but should be considered for infected birds before reintroduction to improve host reproductive and survival rates after release.
... Ecotourism as well as the creation and maintenance of protected areas could play a key role in socioeconomic development in the local communities, which would enable both species conservation and the generation of local culture for conservation. Cracid reintroductions have been used as a conservation tool for the restoration of threatened species, as was the case with Crax blumenbachii (São Bernardo 2012), Pipile albipennis (Angulo and Barrio 2004), and Aburria jacutinga (Oliveira et al. 2016). Reintroduction and ecotourism are being carried out effectively in some parts of the Argentinean Chaco, as happens in Iberá -Corrientes province (Caruso and Jiménez Pérez 2013, Di Blanco et al. 2015, Zamboni et al. 2017, where local hunters started working as provincial park rangers or local guides, which created a socioeconomic change in the region. ...
Article
Full-text available
Identifying factors that determine the spatial distribution of threatened species is key to ensuring their conservation. TheBare-faced Curassow (Crax fasciolata) is a globally threatened bird that is categorized as Vulnerable, and its populations are declining in the gallery forests of the Humid Chaco. To evaluate the effect of human activities and environmental characteristics on the occupancy of Bare-faced Curassows, we sampled 48 sites along two rivers in northern Argentina. Bare-faced Curassows were recorded in 46% of the sites visited. The anthropic activities were identified as hunting pressure, selective logging of timber, and livestock production. Hunting and logging were positively associated with each other, and in turn, negatively related to village distance. We evaluated 17occupancy models using six predictive variables. Occupancy by the Bare-faced Curassow was positively influenced by the distance to the nearest village and by forest cover. To a lesser extent, occupancy was also positively associated with an increase in availability of trees with fleshy fruits and with river course length. Our results indicate that hunting pressure and selective logging are limited by the cost of access from populated areas. Thus, distance to the villages was a good indicator of these human activities along the gallery forests and could be used to determine the spatial distribution of the Bare-faced Curassow in its southern range. Our study highlights the value of using presence/absence surveys and occupancy models for assessing threats of threatened and elusive species such as cracids.
... the most important seed dispersers from the Atlantic rainforest (Galetti et al., 2013), playing a crucial role in this highly endangered biodiversity hotspot (Myers et al., 2000). Currently, five conservation centrers breed this species for reintroduction under the Brazilian Action Plan for the Conservation of Endangered Galliformes (ICMBio, 2008;Oliveira-Jr. et al., 2016). Reintroduction of captive-bred animals is essential to avoid threatened birds from being extinct (Costa et al., 2017;Earnhardt et al., 2014;Hammer and Watson, 2012) and is successful for the Red-billed Curassow (Crax blumenbachii), for example, a Brazilian cracid that has been reintroduced in the Atlantic rainforest for almost 30 years ...
Preprint
Full-text available
Haemosporidian parasites of the genus Haemoproteus are widespread and can cause disease and even mortality in birds under natural and captive conditions. The Black-fronted Piping-guan (Aburria jacutinga) is an endangered Neotropical bird of the Cracidae (Galliformes) going through a reintroduction program to avoid extinction. We used microscopic examination and partial cytochrome b DNA sequencing to describe a new Haemoproteus species infecting Black-fronted Piping-guans bred and raised in captivity that were reintroduced into the Atlantic rainforest. Haemoproteus (Parahaemoproteus) paraortalidum n. sp. was detected in the blood of 19 out of 29 examined birds. The new species is distinguished from other haemoproteids due to the shape of gametocytes, which have pointed ends in young stages, and due to the presence of vacuole-like unstained spaces in macrogametocytes and numerous volutin granules both in macro-and microgametocytes. Illustrations of the new species are provided. Phylogenetic inference positioned this parasite in the Parahaemoproteus subgenus clade together with the other two Haemoproteus genetic lineages detected in cracids up to date. We discuss possible implications of the reintroduction of birds infected with haemosporidian parasites into de wild. Treatment of Haemoproteus infections remains insufficiently studied, but should be considered for infected birds before reintroduction to improve host reproductive and survival rates after release.
Chapter
As the loss of biodiversity accelerates, there is general recognition that managing species outside of their native range (ex situ) will become increasingly important as populations continue to decline. Well-grounded in population genetic theory, ex situ conservation strategies, such as captive breeding, have largely relied on pedigree-based management out of both necessity and preference, despite known violations of important assumptions. Since the advent of molecular markers, many studies have successfully used empirical genetic data for informing ex situ conservation, yet their utility has been questioned due to competing priorities and resources as well as concerns related to potential biases associated with estimating individual- and population-level parameters based on traditional suites of loci. Paired with modern genotyping-by-sequencing approaches, population genomics holds great promise for overcoming past limitations associated with the use of empirical genetic data in ex situ conservation, allowing for highly precise estimates of population genetic parameters and identification of specific loci underlying traits of interest. Here, we review available literature and discuss the clear advantages and ultimate potential of using genome-wide data when managing species outside of their native range, from refining breeding decisions and assessing lineage integrity to minimizing adaptation to the captive environment and informing interactive in situ/ex situ conservation strategies. With resource-driven and capacity-related barriers to adoption falling away, our ability to harness leading-edge technologies to mine the genomes of wildlife species will enable more effective and efficient planning, implementation and monitoring of ex situ conservation strategies moving forward.
Article
Full-text available
Estimating and monitoring adult and juvenile survival are vital to understanding population status, informing recovery planning for endangered species, and quantifying the success of management. We used mark–recapture models to estimate apparent annual survival of the Puaiohi (Myadestes palmeri), an endangered thrush endemic to the Hawaiian island of Kauai, from 2005 to 2011. Our sample included 87 wild birds and 123 captive-bred birds that were released at various ages. Survival was higher for wild adult males (0.71 ± 0.09) than for wild adult females (0.46 ± 0.12). Survival of wild juveniles (0.23 ± 0.06) was lower than that of wild adults of both sexes, indicating that recruitment may limit population growth. Captive-bred birds released when <1 yr old had survival (0.26 ± 0.21) comparable with that of wild juveniles, but captive-bred birds released at 1–3 yr old had very low survival (0.05 ± 0.06). Only 8 of 123 (7%) captive birds were seen again after release. Two wild birds resighted five years after marking are the oldest known individuals, being at least six years of age. Malarial infection did not affect survival of wild Puaiohi, unlike many Hawaiian forest birds. The difference between adult male and adult female survival is consistent with rat (Rattus spp.) predation of females on the nest as a major source of mortality. As such, attempting to reduce nest predation by controlling rats may be the best available management option. Releasing captive-bred birds has had little effect on the wild population in recent years.
Chapter
What is the minimum viable population (MVP) of a particular species? Besides the obvious implications for conservation, especially of endangered species, this question raises important issues in population biology. MVP obviously varies with demographic, life history and environmental factors, but also depends upon genetic load and genetic variability. This book addresses the most recent research in the rapidly developing integration of conservation biology with population biology. Chapters consider the roles of demographic and environmental variability; the effects of latitude, body size, patchiness and metapopulation structure; the implications of catastrophes; and the relevance of effective population size on inbreeding and natural selection. Other topics addressed include the role of decision theory in clarifying management alternatives for endangered species, and the opportunities for improved co-operation between agencies responsible for management. The book concludes with a forward-looking and plain-speaking summary on future research and its application for conservation practice.
Article
We describe a model-based clustering method for using multilocus genotype data to infer population structure and assign individuals to populations. We assume a model in which there are K populations (where K may be unknown), each of which is characterized by a set of allele frequencies at each locus. Individuals in the sample are assigned (probabilistically) to populations, or jointly to two or more populations if their genotypes indicate that they are admixed. Our model does not assume a particular mutation process, and it can be applied to most of the commonly used genetic markers, provided that they are not closely linked. Applications of our method include demonstrating the presence of population structure, assigning individuals to populations, studying hybrid zones, and identifying migrants and admixed individuals. We show that the method can produce highly accurate assignments using modest numbers of loci—e.g., seven microsatellite loci in an example using genotype data from an endangered bird species. The software used for this article is available from http://www.stats.ox.ac.uk/~pritch/home.html.