Ecological Modelling xxx (xxxx) xxx–xxx

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Ecological Modelling
journal homepage: www.elsevier.com/locate/ecolmodel

Letter to the editor

Deterministic population growth models and conservation translocation as a management strategy for the critically
endangered Blue-throated Macaw (Ara glaucogularis): A critique of Maestri et al.

to an exponential growth model, although this was not stated explicitly

The Blue-throated Macaw (Ara glaucogularis) is one of the most
by the authors. No justification was given for the use of an exponential
highly threatened species in the parrot family Psittacidae (BirdLife
model, which is characterized by constant population growth rates re-
International, 2018a). Endemic to the Beni savannas or Llanos de
gardless of population size (Renshaw, 1991), assuming that resource
Moxos of Bolivia, the species is considered critically endangered as a
availability will not be limited even at large population sizes. The lo-
consequence of the cage-bird trade and habitat loss due to large-scale
gistic population growth model, which is more realistic and con-
cattle ranching, which are thought to have resulted in a substantial
servative because growth rates decrease as the population approaches
reduction and spatial subdivision of its global population (Hesse and
its carrying capacity imposed by environmental pressures such as lim-
Duffield, 2000; BirdLife International, 2018b). The wild population has
ited resources (Renshaw, 1991), was not considered by Maestri et al.
been subject to intensive conservation and management actions for
(2017). Certainly, at small population sizes growth is similarly ex-
over 15 years, ranging from awareness campaigns to nest box programs
ponential for both models (Renshaw, 1991). However, several cir-
to the direct protection of important breeding and roosting sites
cumstances caution against the appropriateness of an exponential
(BirdLife International, 2018b).
growth model: 1) the authors’ model projection times of up to 215 years
To evaluate the effectiveness of releasing captive-reared individuals
(over such a long period a recovering population, aided by conservation
for the recovery of the wild Blue-throated Macaw population, Maestri
management, may approach its carrying capacity); 2) uncertainty about
et al. (2017) used a deterministic model that assumes exponential po-
the size of the global wild population, both current (see below) and past
pulation growth to assess population dynamics based on a birth pulse,
(prior to poaching activities; see BirdLife International, 2018b); 3)
post-breeding census, stage-structured projection matrix. Population
corresponding uncertainty about the relative size of the current wild
dynamics were assessed under three different levels (low, medium,
population with respect to the species’ carrying capacity; and 4) the fact
high) of both hatching success and nestling survival. Four out of the
that the reproductive data presented in table 1 of Maestri et al. (2017)
nine possible combinations predicted a population increase (medium
show no indication that the subpopulation under study exhibits ex-
hatching success combined with high nestling survival; high hatching
ponential population growth even though it is subject to intensive
success combined with each low, medium, and high nestling survival).
conservation management.
For those four scenarios of population increase, the authors then esti-
The lack of model validation based on the authors’ empirical data is
mated the number of years required to double the current wild popu-
a shortcoming that extends beyond the choice of an appropriate po-
lation of the macaw under three different types of management actions:
pulation growth model. Their use of a simple deterministic model was
(1) no release of captive-reared birds; (2) release of 50 captive-reared
based on Caswell (2001) and Otway et al. (2004). However, large in-
adult macaws in groups of ten individuals per year during five con-
terannual variation existed in maternity (m; range: 0.0204–0.2286) and
secutive years; and (3) release of 50 captive-reared adult macaws in a
nestling survival (l; range: 0.0000–1.0000) parameters (table 2 in
single group. The time required for a 100% population increase was
Maestri et al., 2017) and in the number of breeding pairs (1–10), hat-
estimated at 33–215 years without releasing captive-reared birds and
ched eggs (1–16), and fledglings (0–10) (table 1 in Maestri et al., 2017).
7–46 years with the release of 50 captive-reared adults (i.e. population
This strongly indicates that stochastic processes (which were also ex-
reinforcement; Corlett, 2016). The authors concluded that releasing 50
amined by Caswell, 2001) have a significant influence on Blue-throated
adult macaws will lead to a doubling of the wild population 4–5 times
Macaw population dynamics, rendering deterministic models, which
faster than current management actions.
ignore stochastic effects, inappropriate for elucidating growth dynamics
While such a modeling approach per se certainly has the potential to
in this critically endangered species. Fauvergue et al. (2012) presented
provide important, urgently needed insights into the effectiveness of
an overview of demographic and environmental stochasticity and,
population reinforcement and other management actions for the con-
based on numerical simulations, argued that especially demographic
servation of the Blue-throated Macaw, we consider that the authors’
stochasticity can lead to the extinction of small (meta) populations even
choice of a deterministic model combined with static input parameters
when subpopulations exhibit a positive growth rate.
are overly simplistic, and that several parameter values are based on
To demonstrate the substantially different results that a non-de-
unrealistic or flawed assumptions, leading to biased, unreliable results
terministic approach can produce, we used the authors’ exponential
and conclusions. We further find it worrisome that the authors make no
growth model (for the sake of comparability) based on the time-de-
attempt to discuss potential shortcomings of their deterministic model,
pendent population size vector n and the projection matrix A (Eq. (1)).
levels of uncertainty associated with input parameter values, and the
We then introduced stochasticity for maternity and nestling survival,
effects that such uncertainties, knowledge gaps, or pitfalls may have on
which determine the fertility parameter F3 of the projection matrix (Eq.
model projections and the corresponding management recommenda-
(2)). We calculated the mean and standard deviation for the annual
tions.
maternity (m) and nestling survival (l) data presented in table 2 of
The model equation employed by Maestri et al. (2017) corresponds

https://doi.org/10.1016/j.ecolmodel.2018.06.007
Received 9 April 2018
0304-3800/ © 2018 Elsevier B.V. All rights reserved.
Letter to the editor
Maestri et al. (2017). For each simulated year we then randomly drew
values for m and l from their respective normal distribution to calculate
F3 (while recognizing that a normal distribution represents a first ap-
proximation as eight years of data with large variation are insufficient
to determine a precise distribution type).
⎛ 0 0 F3 ⎞
n (t + 1) = An (t ) where: A = ⎜G1 P2 0 ⎟
⎜ ⎟
⎝ 0 G2 P3 ⎠
F3 = m*l where: m ∼ N (μm , σm2 ) and l ∼ N (μl , σl2)
All other parameter values of the projection matrix (G1, G2, P2, P3)
were kept constant and were taken from table 4 of Maestri et al. (2017).
Based on the mean value for F3, as used by the authors, the projection
matrix exhibits an eigenvalue of 1, which leads us to expect a stable
population size. We then computed 100 Monte Carlo simulations over a
100-year period with initial values of 7, 19, and 99 for the number of
fledglings, juveniles, and adults, respectively. These values were based
on the assumed global population size of 115–125 individuals
(Berkunsky et al., 2014; Maestri et al., 2017) and the demographic
distribution enforced by the deterministic projection matrix. The source
code of our model is available at https://github.com/ici-bolivia/exp_
population_growth.
Fig. 1 shows changes in adult population size for each of the 100
simulations and the overall mean. As expected from the projection
matrix’ eigenvalue of 1, the mean represents a stable population.
However, stochastic variation (uncertainty) in annual maternity and
nestling survival (fertility), as documented by Maestri et al. (2017, table
2), leads to drastically different scenarios of population dynamics, ap-
proximately ranging from a doubling to a halving of the population
over a 100-year period (Fig. 1). This confirms our concern that a de-
terministic exponential growth model is overly simplistic and does not
allow for a proper assessment of Blue-throated Macaw population dy-
namics, nor does it provide reliable support for management actions
such as population reinforcement.
In addition to these shortcomings of the modeling approach per se,
values used by Maestri et al. (2017) for three of the input parameters
are debatable. First, the authors used an adult sex ratio of 1:1 based on
the species’ largest captive population, arguing that data on sex ratios in
the wild are scarce. While this is true for the Blue-throated Macaw, sex
ratios in other wild parrot populations were reported by several studies
not cited by Maestri et al. (2017). The majority reported nestling sex
ratios only, which were close to unity for two species of Ara macaws in
Brazil (Caparroz et al., 2001), Yellow-naped Amazons (Amazona aur-
opalliata) in Costa Rica (South and Wright, 2002), and Green-rumped
Parrotlets in Venezuela (Budden and Beissinger, 2004). In a global
Fig. 1. Monte Carlo simulations (100) of Blue-throated Macaw (Ara glaucogularis) population dynamics using the exponential growth model and projection matrix
parameter values of Maestri et al. (2017) except for fertility (F3), where stochasticity was taken into account annually based on the authors’ empirically derived
variation in maternity (m) and nestling survival (l). The thick red line represents the mean (For interpretation of the references to colour in this figure legend, the
reader is referred to the web version of this article).
Ecological Modelling xxx (xxxx) xxx–xxx
literature review, Donald (2007) found only seven studies of adult sex
ratios in Psittaciformes (e.g., Greene and Fraser, 1998; Heinsohn and
Legge, 2003), five of which reported a significant skew towards males
and two a balanced sex ratio. Sandercock et al. (2000), a study not cited
by Donald (2007), also reported a male-biased adult sex ratio for Green-
rumped Parrotlets in Venezuela. Across taxonomic groups (orders),
adult males outnumbered adult females by on average 33%, and this
bias was significantly more severe in populations of globally threatened
(1) bird species than in non-threatened species (Donald, 2007). Donald
(2007) concluded that higher female mortality, rather than skewed
(2) offspring sex ratio, is the main driver of male-skewed adult sex ratios in
birds. Thus, extrapolating balanced sex ratios of captive populations to
wild populations as done by Maestri et al. (2017) is likely to be flawed,
especially for globally threatened species. Unlike wild populations,
captive populations are not exposed to predators, competitors, or most
natural parasites, are cared for by veterinarians, supplied with suffi-
cient high-quality food, and largely sheltered from climatic extremes. A
naturally balanced sex ratio in fledglings can therefore be expected to
be retained over time in an adult captive population.
Second, Maestri et al. (2017) stated that the current wild population
unlikely exceeds 115–125 individuals, erroneously citing BirdLife
International (2016) as the source while ignoring Waugh's (2007)
higher estimate of 250–300 birds actually cited by BirdLife
International (2016, 2018b). To our knowledge, the original sources for
the population estimate of 115–125 individuals were Milpacher (2013)
and Berkunsky et al. (2014), neither of whom justified this estimate or
presented any indications on the methods used to obtain this estimate,
rendering it mere conjecture. An objective, rigorous analysis of Blue-
throated Macaw population growth dynamics should therefore in-
corporate both lower and upper bound estimates of the Blue-throated
Macaw’s current wild population size.
Third, Maestri et al. (2017) assumed identical survival rates for
juvenile and adult Blue-throated Macaws. Again, this assumption was
based on observations of captive populations, and as for adult sex ratio,
this assumption is likely to be incorrect for the same reasons detailed
above. In a Blue-throated Macaw population viability analysis, Strem
and Bouzat (2012) applied different mortality rates for nestlings, ju-
veniles, and adults. Although Maestri et al. (2017) incorporated Strem
and Bouzat's (2012) nestling mortality rate of 30% into their model,
they ignored the corresponding juvenile and adult mortality rates
without justification. As for wild population size estimates, in the ab-
sence of better data, an objective analysis of population growth dy-
namics should consider mortality or survival rates used by prior studies
on the same species, or at the very least justify why those values were
not taken into account.
A further concern of ours is related to the accuracy of the raw
2
Letter to the editor
reproductive data presented in Table 1 of Maestri et al. (2017). The
source for data from 2007 to 2011 (five breeding seasons) was given as
Berkunsky et al. (2014). This latter study reported 31 nesting attempts
(defined as the laying of at least one egg in a nest), whereas values for
the same five breeding seasons in Table 1 of Maestri et al. (2017) add
up to only 27 pairs laying eggs. Likewise, Berkunsky et al. (2014) re-
ported that 26 nestlings fledged successfully, whereas values for the
same time period in Table 1 of Maestri et al. (2017) add up to only 24
fledglings. These inconsistencies call into question the data manage-
ment and quality of both studies.
In summary, neither the deterministic modeling approach, nor
several of the input parameter values used by Maestri et al. (2017) are
sufficiently solid, rigorous, and void of pitfalls to provide a reliable
assessment of Blue-throated Macaw population dynamics. Conse-
quently, the authors’ decisive conclusion that the release of 50 captive-
reared adult macaws will lead to a doubling of the wild population 4–5
times faster than current management actions is not supported by the
simplistic, partly flawed modeling approach or by the available em-
pirical data. As pointed out by Beissinger and Westphal (1998), de-
mographic models should be used with much caution in endangered
species management, especially when diagnosing potential for popu-
lation recovery. A much more thorough and carefully designed sto-
chastic modeling approach, combined with more reliable, rigorous
empirical data, will be required to objectively and realistically assess
the effectiveness of population reinforcement for the recovery of the
wild population of the Blue-throated Macaw.
Regardless of these issues, this potentially misleading conclusion
about the effectiveness of population reinforcement is based on several
additional assumptions that may not be met and which the authors
completely failed to address in their Discussion section. One major as-
sumption is the almost immediate, successful establishment of a sub-
stantial number of released birds as breeding pairs. Of 71 hand-raised
Scarlet Macaws (Ara macao) released in Peru and Costa Rica, only 27
(38%) formed pairs and even fewer reproduced successfully
(Brightsmith et al., 2005). Brightsmith et al. (2005) concluded that “it is
unclear if reproduction will be sufficient to allow the populations to
grow and expand as hoped.” Another major assumption is that the
survival and reproductive success of released individuals are similar to
those of adult birds born and raised in the wild that are adapted to local
environmental pressures. Will captive-reared birds really be able to
immediately adapt to the presence of predators (see White et al., 2012),
parasites, competitors, or occasional adverse climatic conditions? White
et al. (2005) reported an estimated first-year survival of only 41% for
captive-reared Puerto Rican Parrots (Amazona vittata) that were sub-
jected to extensive prerelease training and acclamation. For the Scarlet
Macaw in Peru and Costa Rica, first-year survival was 74% (Brightsmith
et al., 2005). Thus, the failure of Maestri et al. (2017) to take into ac-
count low reproductive success and considerable first-year mortality
rates of released birds that were raised in captivity further undermines
their conclusion about the effectiveness of population reinforcement in
doubling the wild Blue-throated Macaw population.
Furthermore, the authors indicated that during their 8-year field
studies no new adult pairs were recruited into local breeding popula-
tions, even though these populations contained 16 breeding pairs that
produced a total of 33 successful fledglings over the same period, and
even though Blue-throated Macaws are considered to reach sexual
maturity at the age of five years (Maestri et al., 2017, and references
cited therein). How can this be explained? The authors failed to address
this paradox. Dispersal and high post-fledging mortality rates are two
possible reasons, among other potential factors that may directly or
indirectly limit recruitment into the breeding population.
Finally, in accordance with Corlett (2016), the release of new in-
dividuals into existing populations is referred to as reinforcement. Re-
introduction (i.e. the term used by the authors), on the other hand, is
the release of new individuals into previous native range (Corlett,
2016). It is widely acknowledged that reinforcement and reintroduction
3
Ecological Modelling xxx (xxxx) xxx–xxx
bear the risk of genetic swamping of the native population by the
translocated individuals (i.e. it can constrain local adaptation and
thereby lower short-term population fitness), if most of the re-
productive output comes from the less well-adapted translocated stock
(IUCN/SSC, 2013). Therefore, reinforcement and reintroduction are
still controversial subjects in conservation genetics (Amato et al., 2009;
Dresser et al., 2017). The absence of urgently needed studies on the
genetic diversity within and across subpopulations of the Blue-throated
Macaw and a corresponding lack of insights on gene flow (connectivity)
levels across the landscape make reinforcement a highly debatable
management action that can pose a serious additional threat to an al-
ready critically endangered species (e.g. Storfer, 1999).
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2012. Psittacine reintroductions: common denominators of success. Biol. Conserv. Coquimbo, Chile
148 (1), 106–115. b
Instituto de Filosofía y Ciencias de la Complejidad, IFICC, Los Alerces
⁎
3425, Santiago, Chile
Sebastian K. Herzog
Asociación Armonía, Av. Lomas de Arena 400, Casilla 3566, Santa Cruz de Renzo R. Vargasa,b
a
la Sierra, Bolivia Universidad de San Francisco Xavier de Chuquisaca, Aniceto Arce 46,
E-mail address: skherzog@armonia-bo.org Sucre, Bolivia
b
Department of Biology, Universidad de La Serena, Raul Britrán 1305,
Jens Bürger Coquimbo, Chile
Centro de Investigaciones en Nuevas Tecnologías Informáticas, Universidad
Privada Boliviana, Av. Juan Pablo II, Colcapirhua, Bolivia Tjalle Boorsma, Rodrigo W. Soria-Auza
Asociación Armonía, Av. Lomas de Arena 400, Casilla 3566, Santa Cruz de
Alejandra J. Troncosoa,b la Sierra, Bolivia
a
Department of Biology, Universidad de La Serena, Raul Britrán 1305,

⁎
Corresponding author.