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Bird Conservation International (2012)0:1–8. © BirdLife International, 2012
doi:10.1017/S0959270912000160
Habitat occupancy of the Dusky-legged Guan in
the lower delta of the Paraná River, Argentina
SILVINA L. MALZOF, MARIA L. BOLKOVIC, JEFFREY J. THOMPSON
and RUBEN D. QUINTANA
Summary
The Dusky-legged Guan Penelope obscura is the southernmost species of the family Cracidae,
reaching its southern distributional limit in the delta of the Paraná River. Habitat loss, together
with uncontrolled harvest, has led to local-scale decreases or extirpation of the species, but no
quantitative evaluation of habitat preferences has been made. We surveyed Dusky-legged Guans
in the Delta del Paraná Biosphere Reserve, Argentina, by motorboat along 543.9km of nine
waterways during both January and July 2009 and used occupancy modelling to estimate habitat
and seasonal effects on occupancy. Detectability was 21–22% on average and occupancy estimates
were highly variable within habitats, but highest in secondary forest, followed by mature
plantation, and lowest in occupied residences. There were no significant differences in occupancy
or detectability among habitats or seasonally. There was a strong positive effect of length of
riparian habitat segments on occupancy and detectability. Habitat management efforts should
address increasing the suitability of mature plantation forest for guans by increasing their
similarity to native forest in structure and composition. Furthermore, we illustrate that surveys
by boat can be logistically effective for surveying cracids associated with riverine habitats and that
it is important to account for incomplete detectability since in our case failing to do so would have
underestimated occupancy by 78–79% on average. Given this, the use of commonly accepted
methodologies for surveying cracids that do not account for incomplete detectability should be
reconsidered and methodologies that can produce robust, reliable estimates applied.
Resumen
La Pava de Monte Común Penelope obscura es la especie con distribución más austral de toda las
especies de la familia Cracidae y vive en el Delta del Rio Paraná. La perdida de habitat, combinada
con la falta de control de caza, ha provocado una disminución a escala local de la especie, además
que nunca fue realizada una evaluación cuantitativa de la preferencia de hábitat. Muestreamos a la
Pava de Monte en la Reserva de Biosfera Delta del Paraná, en Argentina a lo largo de 543.9km
correspondientes a nuevo cursos de agua en una embarcación con motor fuera de borda durante
los meses de enero y julio de 2009 y se usó el modelado de ocupación para estimar los efectos
de hábitat y estación sobre la ocupación de sitios. La detección de las pavas estuvo en un rango de
21–22% y las estimaciones de la ocupación fueron altamente variables dentro de los hábitats, pero
mucho mayor en bosques secundarios, seguido por las plantaciones maduras, y menores en las
residencias ocupadas. No hubo diferencias significativasenlaocupaciónyenladetecciónentrelos
hábitats y las estaciones del año. Hubo un fuerte efecto positivo del largo del segmento de hábitat
ribereño sobre ocupación y detección. Los esfuerzos de manejo del hábitat debería abordar el
aumento de la idoneidad de las plantaciones forestales maduras para la pava al aumentar su similitud
con el bosque nativo en la estructura y composición. Además, ponen de manifiesto que los muestreos
desde una embarcación pueden ser logísticamente efectivos para la asociación de los crácidos con los
hábitats ribereños y la importancia de los conteos de detección incompleta, ya que en nuestro caso de
no hacerlo habríamos subestimado la ocupación en un 78–79% en promedio. El uso de metodologías
comúnmente aceptadas para los muestreos de crácidos debería tomarse en cuenta ya que la detección
incompleta se debe reconsiderar para aplicar metodologías que pueden producir estimaciones
robustas y fiables.
Introduction
The order Galliformes is one of the most endangered avian orders both globally and in the
Neotropics, while the family Cracidae is the most endangered avian family with 37% of species
listed as ‘Vulnerable’or higher (IUCN 2011). Although non-threatened species may be of lesser
conservation concern, some populations of these species are at risk or have been locally extirpated.
Understanding how threats that affect many species, such as habitat loss, affect the more common
cracid species is not only important for the conservation of those species but is also potentially an
important tool for inferring how these factors affect species of greater conservation concern
(Brooks and Strahl, 2000).
The Dusky-legged Guan Penelope obscura is the southernmost species of the family Cracidae,
principally inhabiting riparian forests in southern Brazil, Paraguay and Argentina that reaches its
southern distributional limit in the delta of the Paraná River, Argentina. Its global status is listed
as ‘Least Concern’(IUCN 2011) but at the local scale, the species has been greatly reduced in
numbers or extirpated in many areas due to habitat loss and degradation and uncontrolled hunting.
Based on these facts, at national level it has been considered as ‘Vulnerable’(Lopez Lanús et al.
2008). In the lower delta of the Paraná River, riparian forest, the primary habitat of Dusky-legged
Guan, has been largely converted or modified since the mid-19
th
century so that the landscape is now
a mosaic of secondary forest, plantation forest, deforested land and occupied and unoccupied
residences. Although Dusky-legged Guan appears to exhibit varying preferences among habitat
types these preferences have not been quantified.
We surveyed Dusky-legged Guan in the lower delta of the Paraná River, Argentina during winter
and summer, using occupancy modelling to estimate habitat preferences and seasonal effects on
occupancy. Surveys were conducted by boat and we illustrate that this is an effective method for
surveying guan species associated with riparian habitats. Moreover, our results indicate that
although Dusky-legged Guans utilisea diversity of anthropogenic habitats, they exhibit a preference
for habitats most similar to mature riparian forest, which has important implications for the
protection of these habitats and the species in the region.
Study area
The study was conducted in the Paraná River Delta Biosphere Reserve (34°159009S, 58°589339W),
located in the lower delta of the Paraná River at the southern end of the Rio de la Plata basin. The
islands of the lower delta are generally saucer-shaped with natural levees around their perimeters
which were originally covered with native riparian forest while lowland areas are occupied by
freshwater marshes and flooded forests of Erythrina crista-galli (Kandus et al. 2006). Riparian
forest in the region has been highly modified so that forested areas are now dominated by poplars
Populus spp. and willows Salix spp., interspersed with remnants of native forest, secondary
forests dominated by exotic vegetation, and occupied or abandoned homesteads.
Methods
We surveyed 543.9km of nine waterways (Largo, Cruz del Sauce, Inatonta, Carpincho, Dominguito,
Herrera, Pantanoso, Arroyo Las Cubiertas streams and Barquita river) from a motorboat moving
S. L. Malzof et al. 2
at approximately 20 km/hr using two observers. Each waterway was surveyed five times during
January (austral summer) and July (austral winter) 2009 between 08h00 and 11h00 and 16h00-
19h00 in January and 08h00-11h00 to 15h00-18h00 in June. We characterised both sides of each
waterway by habitat type (secondary forest, mature plantation forest, young plantation forest,
deforested area, and occupied residence) with each length of a specific habitat considered a sampling
site, resulting in 158 sites. Mean segment length varied from 154 m(SE517.5m) for young
plantation forest to 518 m(SE590.7m) for secondary forest (Figure 1). Since Dusky-legged
Guans are confined to riparian forest in our study area, this was the most efficient method for
sampling a large area of potentially suitable habitat.
During each survey, the detection or non-detection of Dusky-legged Guans was recorded for
each site and these data were used to construct detection histories for each of the sampling periods.
Since naive estimates of occupancy from raw counts, uncorrected for incomplete detection, are
potentially biased, we used occupancy modelling (MacKenzie et al. 2006) to model habitat
occupancy (w) and detection probabilities (p). We used the program PRESENCE 3.1(Hines 2006)
to test 22 models developed a priori which included habitat type and length of habitat as
co-variables. Covariates were ztransformed so that the mean was equal to zero. All models
included the effect of sampling period on occupancy since the data from both seasons were analysed
together and we utilised categorical variables to represent sampling periods so that the assumption
of population closure was met, which is akin to a robust design model (Pollock 1982)althoughwe
did not estimate colonisation or extinction parameters.
Models were ranked using Akaike’s Information Criterion (AIC) adjusted for small sample size
and overdispersion using quasi-AIC (QAICc) and models averaged for those models with
a weight of at least 10% of the highest ranked model within the candidate set (Burnham and
Anderson 2002). Differences in estimates of occupancy and detection probability were determined
using 95%confidence intervals of the beta coefficients from the composite model were utilised to
determine the magnitude of the effect of covariates. Where the 95% CIs did not include zero, the
effect of the covariate was considered to be strong.
Figure 1. Mean length and 95% confidence limits of riparian habitat surveyed. OR 5occupied
residence, SF 5secondary forest, YPF 5young plantation forest, MPF 5mature plantation
forest, D 5deforested area.
Dusky-legged Guan in the Paraná River delta 3
Results
We detected Dusky-legged Guans at 40 sites during January 2009 and 25 sites during June 2009
(observed w50.25 and 0.16 respectively) (Table 1). Of the 22 models tested, eight had weights
with at least 10% of the weight of the highest ranked model, which also accounted for 94% of all
model weights (Table 2). Model fit was good with ^
c51.08 for the global model.
The composite model from model averaging estimated a mean wacross all sites for the winter
sampling period of 0.26 with a 95% confidence interval of 0.11–0.40, while for the summer
sampling period a mean w50.36 with a 95% confidence interval of 0.20–0.52 (Table 1). These
estimates are 61% and 69% greater than the observed occupancy for the winter and summer
sampling periods, respectively (Table 1). Mean detection probability was nearly equal during both
sampling periods and highly variable (summer p50.21,95%CI50.07–0.36; winter p50.22,
95%CI50.07–0.37; Table 1).
Figure 2. Estimated detection probability (a) and occupancy (b) by habitat type and season from
the composite occupancy model. Error bars represent 95% confidence limits. OR 5occupied
residence, SF 5secondary forest, YPF 5young plantation forest, MPF 5mature plantation
forest, D 5deforested area.
S. L. Malzof et al. 4
Estimated detectability was nearly constant among habitat types and season (Figure 2a). During
winter and summer, detection was highest in secondary forest (winter p50.23,summerp50.24),
followed by deforested land (winter p50.22,summerp50.23), mature plantation forest (winter
p50.22, summer p50.22), young plantation forest (winter p50.19, summer p50.19), and
occupied residence (winter p50.18,summerp50.18). Estimates of occupancy varied among
habitat types and season but not significantly (Figure 2b). Occupancy estimates during both winter
and summer were highest in secondary forest (winter w50.39,summerw50.51), followed by
mature plantation forest (winter w50.3,summerw50.42), deforested land (winter w50.19,
summer w50.29), young plantation forest (winter w50.14,summerw50.23), and occupied
residence (winter w50.12, summer w50.19).
Beta coefficients and their 95% confidence intervals from the composite model indicated
a strong positive effect of length of riparian habitat segments on occupancy of Dusky-legged
Guans, the 95% CI interval did not span zero. Occupied residences appeared to have a weak to
moderate negative effect since zero was included in the lower limit of the confidence interval
(Table 3). Additionally, there was a moderate positive effect of habitat length on detection
probability since the lower limit of the 95% confidence interval included zero (Table 3).
Discussion
Mean estimated occupancy was higher during summer than winter although highly variable and
not significantly different. If higher occupancy is indicative of greater abundance (MacKenzie and
Nichols 2004) then the difference between the two seasons is likely due to increased population
from post-breeding recruitment. Although estimates of occupancy were highly variable, guans
exhibited a preference for secondary forest followed by mature plantation forest. Given the lack of
mature native forest within our study area, this suggests that secondary forest and mature
plantation forest are preferred since they have a well developed understorey and offer resources
Table 1. Observed (W
(obs)
) and estimated occupancy (W
(estimated)
) and estimated detection (p
(estimated)
)
probabilities by season with their respective 95% confidence intervals (95% CI) from the composite models.
Season W
(obs)
W
(estimated)
W
(estimated)
95%CI p
(estimated)
p
(estimated)
95%CI
Winter 0.16 0.26 0.11–0.40 0.21 0.07–0.36
Summer 0.25 0.36 0.20–0.52 0.22 0.07–0.37
Table 2. Models with model weights (w) within 10% of the top ranked model which were used for model
averaging. W5probability of occupancy, QAICc5Quasi-Akaike’s Information Criteria corrected for small
sample size, and -2*LogL 5-2times the Log likelihood. All models include the effect of survey season on W.
Model
1
QAICcw Number of
parameters
-2*LogL
w(habitat1length),p(length) 00.2874 10 653.69
w(length),p(length) 0.43 0.2087 6 665.14
w(habitat1length),p(.) 1.75 0.1111 9 657.89
w(length),p(.) 1.84 0.1036 4 668.79
w(length),p(habitat1length) 2.68 0.0734 10 656.63
w(length),p(habitat) 2.85 0.0657 9 659.02
w(habitat1length),p(season1length) 3.25 0.0572 12 652.86
w(length),p(season1length) 4.07 0.0325 7 664.83
1
Occupancy and detection were modeled as constant (.) or as a function of habitat type (habitat), season
(summer or winter) and length of habitat segment (length) which constituted each site.
Dusky-legged Guan in the Paraná River delta 5
and shelter most similar to what would be provided by mature native forest (Malzof et al. 2006).
For example, secondary forests provide important fruit resources throughout the year (S. Malzof
unpubl. data), such as Ligustrum lucidum and L. sinense, whose fruits are staple food items for
guans (Merler et al. 2001).
Young plantation forest, deforested areas, and occupied residences were least occupied, consistent
with the negative effect of occupied residences and young plantation forest on occupancy exhibited
by the bvalues of the process model. Insufficient resources and habitat structure are likely causes of
lower occupancy in these habitats, although in occupied residences and young plantation forest,
anthropogenic disturbance, both direct and indirect, also contributes to lower occupancy. Human
activity around occupied residences is high and young plantations require considerable management
during the first five years of establishment which likely presents a significant amount of human
disturbance. Moreover, an increased human presence likely equates to increased hunting pressure.
As with occupancy, detection by habitat type was highly variable, although similar across
habitats and seasons. Detectability by habitat type, excluding deforested areas was highly
correlated with occupancy (r
2
50.98), suggesting that abundance in these habitats affects
detectability. The greater detectability in relation to occupancy in deforested areas is likely to be
due to increased visibility. As with seasonal differences, if higher occupancy is related to greater
abundance, then the moderate positive effect of secondary forest on detectability can be attributed
to higher abundance of guans in this habitat.
Habitat length was the only factor that had a strong effect on occupancy and appeared to
positively influence detection rates. Increased detectability in longer habitat sections is attributable
to greater probability of detecting an individual as function of survey effort. After correcting for
the effect of habitat length on detectability, the length of habitat positively affects occupancy
which suggests that regardless of habitat type, larger habitat fragments have a greater probability
of being occupied.
The relatively low detectability highlights the importance of accounting for incomplete detection,
since on average 78–79% of individuals are not detected, depending upon the season. Additionally,
although we found a strong correlation between occupancy and detection in four of the five habitat
types, the greater detectability in deforested areas and the positive effect of habitat length on
detectability further highlights the importance of accounting for incomplete detection when
evaluating habitat preferences. If not accounted for, the higher detectability in deforested habitats
relative to occupancy would erroneously place greater importance on deforested areas, while greater
detectability in longer habitat segments would overestimate the importance of secondary forest and
mature plantation forest, since on average these habitats represented the longest habitat segments.
Accounting for incomplete detectability is fundamental to estimating population parameters
(Anderson 2001, Williams et al. 2002), which is evident by our results. In our case, a failure to
account for incomplete detectability would underestimate occupancy in general and would
produce biased estimates of habitat preference. Cracids generally occur at low densities, even in
pristine habitats, which often makes surveying these species difficult, but we believe that we
developed a sound methodology for large-scale surveys of cracids associated with riparian forest
Table 3. Beta coefficients and their standard errors for the habitat covariates used in the analysis from the
composite occupancy (b
w
) and detection (b
p
,) models.
Habitat covariate b
w
b
w
SE b
p
b
p
SE
Occupied residence -0.7385 0.6946 -0.0859 0.1882
Secondary forest 0.1606 0.5972 0.1316 0.1662
Young plantation forest -0.4465 0.6349 -0.0357 0.1799
Mature plantation forest -0.0098 0.5970 0.0791 0.1668
Deforested area -0.3399 0.6193 0.1536 0.1757
Habitat length 0.9305 0.1283 0.1283 0.0990
S. L. Malzof et al. 6
that produces robust estimates of site occupancy. Based upon our results, the use of the common
methodology for cracid surveys (Strahl and Silva 1997) should be reconsidered and we urge
researchers to adopt methods that account for incomplete detection to produce reliable and robust
estimates of cracid population parameters.
The pattern in habitat occupancy that we observed is consistent with the ecology of cracids in
general, preferring more mature forests and exhibiting a high level of sensitivity to anthropogenic
disturbance (Strahl et al. 1997, Brooks and Strahl 2000, Brooks 2006). Even though the Dusky-
legged Guan utilised a diversity of habitats, including highly modified habitats, it still illustrated
the relative avoidance of such habitats, preferring those most analogous to mature riverine forest.
A similar response was observed in the congeneric Penelope perspicax which preferred forest
patches over exotic tree plantations (Ríos et al. 2008). Therefore, the abundance and distribution
of Dusky-legged Guan in the lower delta of the Paraná River is likely to be highly dependent
upon the availability of native forest remnants and secondary forest.
Although the Dusky-legged Guan is still relatively common in the lower delta of the Paraná
River, its distribution is dependent upon the availability of preferred habitat. In our study area,
the habitats with the highest estimated occupancy, secondary forest and mature plantation forest,
represented 43% and 30% of the habitat area respectively and in part explains the relative
commonness of guans in the area. The maintenance of these habitats in the landscape is critical
for the conservation of Dusky-legged Guan in the lower delta of the Paraná River and suggests
that management to increase habitat quality, particularly mature plantation forest, may have
particular positive effects on guan populations.
Acknowledgements
We thank Carlos Zoppi and family for logistic support, BEX (Birders Exchange) and Idea Wild for
equipment support and Interisleña for providing us free passes to motorboats.
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SILVINA L. MALZOF*, RUBEN D. QUINTANA
1
Departamento de Ecología Genética y Evolución, Facultad de Ciencias Naturales, Universidad de
Buenos Aires, Buenos Aires, Argentina.
1
Instituto de Investigación e Ingeniería Ambiental (3iA), Universidad Nacional de San Martín,
Buenos Aires, Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas
(CONICET).
MARIA L. BOLKOVIC
Dirección de Fauna, Secretaría de Ambiente y Desarrollo Sustentable de la Nación.
JEFFREY J. THOMPSON
Instituto Nacional de Tecnología Agropecuaria (INTA), Centro de Investigación en Recursos
Naturales (CIRN-IRB), De los Reseros y Las Cabañas S/N, HB1712WAA Hurlingham,
Buenos Aires, Argentina.
*Author for correspondence; email: silvinamalzof@ege.fcen.uba.ar
Received 21 September 2011; revision accepted 20 February 2012
S. L. Malzof et al. 8
