Austral Ecology (2022) 47, 954–970

Population decline and demography of the world’s largest

breeding population of huemul deer (Hippocamelus bisulcus)
in Bernardo O’Higgins National Park, Chile
SHALYNN M. PACK,1,2* DIANA BERTUOL-GARCIA,1,3 MATTHEW POMILIA,1
1 4
ADAM SPENCER AND DENNIS ALDRIDGE
1
Round River Conservation Studies, 925 E 900 S, Ste 210, Salt Lake City, Utah, 84105, USA
(Email: shalynnpack@gmail.com); 2Department of Fisheries, Wildlife, and Conservation Sciences,
Oregon State University, 104E Nash Hall, Corvallis, Oregon, 97331, USA (Email:
shalynnpack@gmail.com); 3School of Environmental Studies, University of Victoria, Victoria, British
Columbia, Canada; and 4Corporaci
on Nacional Forestal, Regi
on de Ays
en, Chile

Abstract The largest remaining populations of the endangered huemul deer (Hippocamelus bisulcus) are believed to be
concentrated in the remote, rugged and largely uninhabited glacial valleys and fjords surrounding the Southern Pata-
gonian Ice Field that lie within Chile’s Bernardo O’Higgins National Park. On the Park’s northwestern edge is Bernardo
Fjord, an area home to the world’s largest known breeding population of huemul. We present a demographic study of this
population and examine its population trends since 2004. We conducted huemul transect surveys on-foot during 16 expe-
ditions to Bernardo Fjord from October 2014 to March 2020, during which we spent a total of 254 days in the field and
documented 284 observations of huemul. This coastal population of huemul exhibited higher female proportions (mean
0.64  SD 0.05), lower fawn:female ratios (mean 0.18  SD 0.23 in March and mean 0.22  SD 0.07 in November),
and similar group sizes (mean 1.77  1.06 SD individuals) to previous studies. Huemul densities in Bernardo Valley
encountered from 2016 to 2019 were 60% lower than densities observed in a previous study from 2004 to 2008. We pro-
duce a 2019 huemul population estimate for Bernardo Fjord of 84 (SD 7) individuals including 44 observed individuals
and 40 (SD 10) individuals estimated to be undetected by our surveys, which comprises 6–8% of the IUCN global
population estimate. Two of the surveyed sectors – Bernardo Valley and Pampa – are of critical conservation importance,
given that the 5 km2 Pampa is home to 42% of the total huemul population and 41% of the fawn population of Bernardo
Fjord. We examine potential drivers of this population decline, which may include poor recruitment, predation and high
incidences of foot disease exacerbated by climatic conditions, and we offer recommendations for the conservation,
monitoring and management of this and other coastal huemul populations.
Las mayores poblaciones remanentes del amenazado Huemul (Hippocamelus bisulcus) se cree que est
an concentra-
das en los remotos, accidentados y mayoritariamente inahabitados valles glaciares y fiordos que rodean el Campo de
Hielo Patag
onico Sur, la mayor parte del cual est
a contenido en el Parque Nacional Bernardo O’Higgins en Chile.
En el borde noroeste est
a el Fiordo Bernardo, un
area que alberga la poblaci
on reproductiva m
as grande conocida.
Presentamos un estudio demogr
afico de esta poblaci
on y analizamos su tendencia poblacional desde 2004. Recorri-
mos a pie transectos de huemul durante 16 expediciones en el Fiordo Bernardo, desde Octubre de 2014 hasta Marzo
de 2020, durante las cuales permanecimos un total de 254 d
ıas en terreno y registramos 284 observaciones de hue-
mules. Esta poblaci
on costera de huemul mostr
o una proporci
on mayor de hembras (media 0.64  SD 0.05), una
relaci
on cr
ıa:hembra menor (media 0.18  SD 0.23 en Marzo y media 0.22  SD 0.07 en Noviembre), y tama~ nos
de grupo similares (media 1.77  SD 1.06 individuos), que en estudios previos. Las densidades de huemules que se
encontraron para el Fiordo Bernardo en el periodo 2016–2019 fueron 60% menores que las densidades observadas
en un estudio previo de 2004–2008. Concluimos para el a~ no 2019 en el Fiordo Bernardo una poblaci
on estimada de
huemules de 84 (SD 7) individuos, considerando 44 individuos observados y 40 (SD 10) individuos que se esti-
man no detectados en los muestreos, lo que representa 6–8% de la estimaci
on poblacional global de acuerdo con
UICN. Dos de los sectores muestreados – Valle Bernardo y Pampa – poseen una importancia cr
ıtica de conser-
vaci
on, ya que los 5 km2 de Pampa albergan el 42% de la poblaci
on total de huemules y el 41% de la poblaci
on de
cr
ıas del Fiordo Bernardo. Analizamos las causas potenciales de la declinaci
on poblacional, las que pueden incluir
bajo reclutamiento, depredaci
on y alta incidencia de enfermedades podales exacerbadas por las condiciones

*Corresponding author.
Accepted for publication April 2022.
[Correction added on 30 May 2022, after first online
publication: The paragraph spacing was inserted to differenti-
ate the Spanish language in the Abstract]

© 2022 Ecological Society of Australia. doi:10.1111/aec.13178

 CRITICAL HUEMUL POPULATION IN DECLINE
clim
aticas. Finalmente, entregamos recomendaciones para la conservaci

poblaciones costeras de huemules.
Key words: Chile, conservation, endangered species, Hippocamelus bisulcus, huemul.
INTRODUCTION
The huemul (Hippocamelus bisulcus) is an endangered
deer species endemic to the south of Chile and
Argentina (Black-Decima et al. 2016). Huemul are
important both culturally as a symbol of Patagonia
and ecologically as one of the few remaining mega-
fauna species in the ecoregion. Due to hunting and
habitat loss during the 19th and 20th centuries, today
its population has been reduced to just 1% of histori-
cal levels, with estimates ranging from 1048 to 2500
individuals (Redford & Eisenberg 1992; Vila
et al. 2006; Black-Decima et al. 2016). Remaining
populations occupy 50% of the species’ historical dis-
tribution, and survive in isolated and fragmented
populations mostly in mountainous and uninhabited
terrain, habitat which is marginal relative to the valley
floors from which they have largely been extirpated
(Vila et al. 2006). Despite its conservation status and
cultural relevance, there is a profound lack of formal
information on the huemul in Chile, particularly out-
side of protected areas, which makes it impossible to
determine its global population trend (Wittmer
et al. 2010). Moreover, the majority of what has been
published on huemul ecology has been generated in
inland areas (Povilitis 1998, 2002; Corti et al. 2010),
which are considered to be of a different ecotype with
significantly different genetics than coastal popula-
tions. It is suggested that coastal and inland huemul
should be managed separately to preserve their
genetic diversity (Mar
ın et al. 2013).
The largest remaining populations of huemul are
believed to survive near the southern Patagonian Ice
Field, most of which lies within Chile’s Bernardo
O’Higgins National Park (Povilitis 1986; Frid 1994;
Vila et al. 2006; Black-Decima et al. 2016). Near the
northern limit of the park lies Bernardo Fjord, an
area believed to have the highest density of huemul
anywhere in the world (Frid 2001; CONAF 2015).
The huemul population in Bernardo Fjord has been
studied sporadically for decades, starting with the
first expedition by Chile’s National Forestry service
(Corporaci
on Nacional Forestal or CONAF) in
1985, during which they sighted 11 individuals
(CONAF 2015), and continuing with an in situ
research project on huemul habitat use, social
dynamics and interactions with introduced cattle
(Frid 1994, 1999, 2001). The cattle were mostly
removed by 2005 (Vila et al. 2019) and the last indi-
vidual was removed in 2014 (F. Paredes, pers.
© 2022 Ecological Society of Australia.
955
on, monitoreo y manejo de esta y otras
comm., 2016). Today, huemul in Bernardo Fjord
continue to live in a habitat nearly unaltered by
humans. The only natural predator of adult huemul,
the puma (Puma concolor) is likely absent from Ber-
nardo Fjord (although Wensing (2005) sighted puma
tracks, no other study including our 5 years of in situ
and camera trap research has documented any sign).
Huemul fawns, however, are frequently predated by
culpeo foxes (Lycalopex culpaeus), which are the most
important causes of mortality in this age class in
inland populations (Smith-Flueck 2003; Corti
et al. 2010).
The most recent demographic study of huemul at
Bernardo – the only such study of a coastal huemul
population to date – summarized an annual popula-
tion census from 2004 to 2008 and estimated 71
individual huemul inhabiting the 500-ha survey area
of Bernardo Valley as of 2008 (Brice~ no et al. 2013).
When we, however, began monitoring the Bernardo
Fjord sector in 2014, the park guards claimed that
the huemul population had been in steep decline
since the 2008 survey. Our initial surveys also indi-
cated this population was significantly smaller than
previously documented. Given the global importance
of this population of endangered huemul deer – both
for its density and for being characteristic of a popu-
lation relatively undisturbed by human impacts and
influence – it is crucial to understand how the hue-
mul population is changing at Bernardo Fjord and
surrounding areas.
We aimed to fill this knowledge gap by using inno-
vative methods to provide updated estimates of hue-
mul population size and demographic rates in
Bernardo Fjord, offering a point of reference for
managers and researchers to better understand the
huemul populations of the southern Patagonian
fjords and Ice Field. From 2016 to 2020, in collabo-
ration with CONAF, we conducted bi-annual, stan-
dardized surveys of the huemul population in this
remote and rugged area. We conducted surveys in
November during the peak birthing period (F. Pare-
des, pers. comm., 2016), and in March to determine
the survival of fawns and generate population esti-
mates outside of the breeding season. In this paper,
our goals are to: (i) assess population trends of this
critical population, comparing with estimates from
Brice~ no et al. (2013); (ii) provide demographic rates
for huemul in the fjords ecoregion to compare with
rates from inland habitats; and (iii) estimate the cur-
rent population size by integrating detection
doi:10.1111/aec.13178
956 S. M. PACK ET AL.
Fig. 1. Location of the region studied in the Bernardo O’Higgins National Park (left) in Chile and the sectors included in
the biannual census (right). Sectors in the Bernardo Valley Region are in green, the Huemules region in orange and the Ofhi-
dro region in blue. Contour lines represent 100 m of elevation.
probability. Based on our results, we then examine
potential causes for population trends; and offer
management recommendations for huemul in this
and other coastal areas.
METHODS
Study area
In Bernardo Fjord (Fig. 1), the climate is cold and wet
throughout the year due to a strong oceanic influence, pre-
senting an annual mean precipitation of 4000 mm, annual
temperatures averaging 7–8°C, and snowfall at any time of
year (although mainly from June to August) (Carrasco
et al. 1998). Soils are rocky, nutrient-poor, and water-
saturated, due to high rainfall and poor drainage from post-
glacial depressions on the landscape. The topography is
dominated by steep-walled glacial valleys and retreating gla-
ciers, with ecosystem types including periglacial grasslands,
dense thickets of low-lying shrubs including calafate (Ber-
beris microphylla) and chaura (Gaultheria mucronata), old-
growth forests of Nothofagus spp., and moorlands of red
doi:10.1111/aec.13178
crowberry (Empetrum rubrum) and Gunnera magellanica
(Frid 1994, 2001; Brice~ no et al. 2013).
For this study, we divided the Bernardo Fjord area into
three regions comprising a total of eight sectors, all of
which lack permanent human colonization and were
selected based on the presence of huemul and a topogra-
phy that allowed field surveys: Bernardo Valley region
(sectors Pampa, GLOF, Valle Bajo, and Refugio), Hue-
mules region (sectors Valle Huemules, Valle Toros, and
Terrazas) and Ofhidro region (Ofhidro sector; Fig. 1). Of
these sectors, four (Pampa, Valle Bajo, Refugio and Valle
Huemules) were surveyed in 2004–2008 by Brice~ no
et al. (2013).
In the Bernardo Valley region, the Pampa sector (5 km2)
is a low, flat peninsula covered with scrub that transitions
into a wooded hill on its southwest and northeast slopes;
this sector has long been known to have a breeding popula-
tion of huemul (Frid 1999). The Valle Bajo sector
(4.6 km2) is a flooded grassland bordered by the fjord and
dense forest. The GLOF sector (2.95 km2) includes a steep
hillside that transitions from fjord edge into a small grass-
land plateau overlooking Bernardo Glacier and its glacial
lake, which has an annual outburst flood into the fjord (F.
Paredes, pers. comm., 2016). On the west side of the fjord,
© 2022 Ecological Society of Australia.
 CRITICAL HUEMUL POPULATION IN DECLINE
the Refugio sector (4.14 km2) contains a long, narrow area
of flat topography that is densely covered in shrubs, and is
home to the CONAF-Ays
en guard station which is occu-
pied sporadically through the year. In the Huemules region,
the Terrazas sector (6.93 km2) includes a hillside that
climbs out of the Refugio sector, spilling into the wide, flat
grassland valley of the Valle Toros (5.85 km2), aptly named
for its previous presence of domestic cattle. To its west is
the Valle Huemules sector (4.83 km2), a wide grassland
valley connecting to the T
empano Fjord. Lastly, the Ofhi-
dro region and sector (15.29 km2) lies within a small fjord
18 km north of the Bernardo Fjord, and contains narrow
valleys with steep hillsides around the Ofhidro Glacier.
Although these sectors represent biogeographical distinc-
tions, there is certainly some genetic flow of huemul
between them; for example, we have observed a huemul
swim across the narrow section of Bernardo Fjord from the
Pampa to the Refugio sector. However, given the philopatry
of female huemul, that the area of most sectors is approxi-
mately one huemul home range of 3.5–6.5 km2, and that
average daily movements of huemul are <1 km, for this
study we assume that huemul populations in the sectors are
closed with no emigration or immigration (Fig. 1; D
ıaz &
Smith-Flueck 2000; Gill et al. 2008).
METHODS
Field surveys
From October 2014 to March 2020, huemul deer were sur-
veyed biannually in the Bernardo Fjord through a collabo-
rative effort between Round River Conservation Studies
(RRCS) and CONAF, either in the austral spring (October
or November) or the austral summer (February or March).
Initial surveys in 2014–2016 aimed to determine areas of
huemul habitat and select the study sectors. In August
2016, CONAF visited the Pampa to capture, ear-tag, and
treat nine individuals with health issues, including three
adult males, five adult females and one juvenile; they trea-
ted seven of these for a foot ailment and one for an abdom-
inal tumour. In August 2018 they treated and ear-tagged
one additional adult male with a foot ailment
(CONAF 2016). By November 2016, we began surveying
routes using the standardized methodology detailed here.
For all sectors except the Pampa, we surveyed on foot in a
single-file line, one person behind the other, generally in a
group of 10 people led by a CONAF park guard or RRCS
biologist; all surveyors received at least 1 month of previous
training in the observation and field detection of huemul.
We elected for this single-line survey method to ensure sur-
veyor safety while maximizing the total area we could sur-
vey during the multi-day survey expedition; this method
still afforded high visual coverage of huemul due to the
open terrain. For the Pampa sector, however, we deviated
from this methodology and instead surveyed in a sweeping
line, with each surveyor walking 250–500 m from the next
observer, following an azimuth of 330°; we elected the
sweep method on the Pampa because its location, accessi-
bility by boat and small size allowed us to survey it during
a half-day outing from base camp. Total survey effort var-
ied across expeditions and sectors and was measured by the
© 2022 Ecological Society of Australia.
957
total distance walked by the surveying group and by the
number of people in the group. The association between
both measures of survey effort and the number of individ-
ual huemul seen across sectors and expeditions was tested
using a non-parametric Spearman rank correlation, with
P-values lower than 0.05 considered to be significant.
Each time a huemul was sighted, we recorded the num-
ber, age, sex and condition of individuals, and the presence
or absence of an ear tag, date, time, observer UTM coordi-
nates, distance and angle between observers and individuals
(calculated with a Nikon Laser 1200 Monarch Gold laser
rangefinder and compass, respectively), and photo num-
bers. We categorized huemul age classes following Corti
et al. (2010) as follows: adults (individuals older than
3 years), juveniles (2–3 years), yearlings (1–2 years), and
fawns (<1 year old, usually born in November). In all sur-
veys, we reduced the possibility of double-counting by not
counting individuals in an area already surveyed during that
expedition, by using photo-identification, and by analysing
the location and time of each sighting. When mapping our
sightings, we used the distance and angle from the individ-
ual or group sighted to observers to calculate and map the
true location of the animal.
We created a database with individuals observed during
surveys in each of the 8 sectors, linked to photo(s) of the
individuals when able. We categorized sightings observed
outside of our standardized survey methodology – for
example, from a boat-based sighting during travel, or from
CONAF data taken prior to 2016 – as “opportunistic” data,
which we used to document the presence of huemul but
excluded from analyses. We tracked all re-sightings of the
10 ear-tagged individuals and also documented any huemul
carcasses, skeletons, or other remains observed during
expeditions. All statistical analyses described were done in
the R environment (R Core Team 2021), using the tidy-
verse package (Wickham et al. 2019).
Assessing long-term population trends
To assess huemul population trends over a longer time
scale, we compared our results from 2016 to 2020 with
those from the only previous survey in the region con-
ducted from 2004 to 2008 (Brice~ no et al. 2013). We used
the densities estimated as an indicator of changes in abun-
dance, and we compared our data set to that of Brice~ no
et al. (2013) by using a matching subset of our larger data
set. Their study was conducted in three valleys, two of
which overlap with our study: the Bernardo Valley and the
Huemules Valley (the same as our sector Valle Huemules).
We assumed that their survey in Bernardo Valley included
our sectors Pampa, Valle Bajo, and Refugio, and so we
summed our observations from these sectors to compare
with their survey results from Bernardo Valley. We repeated
their methodology to calculate the area surveyed: a fixed
width transect of 300 m (150 m on each side of the lines
walked) in Bernardo Valley and full coverage of 3.2 km2 in
Huemules Valley. We excluded from this analysis several of
our surveys in which field conditions prevented a full sur-
vey, including Valle Huemules in November 2019 and Ber-
nardo Valley in February 2016 and March 2020. We then
calculated the density of huemul in the region in the same
doi:10.1111/aec.13178
958 S. M. PACK ET AL.
way as Brice~ no et al. (2013), by dividing the total number
of individuals seen of all age classes by the area surveyed.
To ensure comparability between our studies, we recalcu-
lated their density values based on their reported number
of observed individuals and distance surveyed for Bernardo
Valley. Finally, we compared our densities with those
reported by Brice~ no et al. (2013) by performing a one-
tailed Wilcoxon Rank Sum test with the hypothesis that
their densities were higher than the ones we encountered;
before performing the test, we checked for independence of
observations by calculating the temporal autocorrelation
using the Spearman correlation index between lagged
observations, and we considered P-values lower than 0.05
to be significant in both steps. To ensure that our assump-
tion about the area Brice~ no et al. (2013) included in their
surveys of the Bernardo Valley did not affect our results,
we also generated different combinations of the sectors
included as part of the Bernardo Valley and repeated the
above analysis.
Calculating demographic indices for the region
Pooling every sector and expedition, we calculated key
demographic variables from our entire data set to provide a
point of comparison with studies of huemul in other
regions. For these analyses, we calculated the area surveyed
using different distances than the ones employed in Brice~no
et al. (2013), because we felt this more accurately repre-
sented our survey conditions. For this, we estimated the
total area surveyed in QGIS by using a buffer around the
line surveyed and eliminating any overlap; buffers differed
for each sector (Table 1) and were determined based on
our experience of average visibility for each sector. To
ensure that our estimates of average visibility were reason-
able and thus our estimates of survey area were accurate,
we also compared our estimates to the average sighting dis-
tance of all surveys in each sector (Table 1). In the sectors
La Pampa and Valle Bajo, due to their flat terrain and low
vegetation, we assumed our surveys covered the totality of
the area and, therefore, used a fixed area covered for every
survey in these sectors (5 km2 for La Pampa and 0.46 km2
for Valle Bajo), independent of the route surveyed.
Then, we calculated huemul density by dividing the total
number of individuals older than 1 year by the area
Table 1. Estimated visibility range (i.e. buffer) for huemul surveyed in each sector, compared with the observed average,
maximum and minimum sighting distance of huemul individuals and/or groups in that sector (surveys between 2014 and
2020)
Buffer
Region Sector used (m)
Bernardo GLOF 50
Valley Pampa No buffer, see text
Valle Bajo No buffer, see text
Refugio 100
Huemules Terrazas 200
Valle Huemules 100
Valle Toros 200
Ofhidro Ofhidro 200
doi:10.1111/aec.13178
surveyed for each sector and expedition; we restricted our
estimate of density to yearlings, juveniles and adults
because variation in these age classes is a more meaningful
indicator of long-term trends in populations of species with
high variability in fawn survival (Gaillard et al. 2000; Corti
et al. 2010; Wittmer et al. 2010). The proportion of females
was calculated for every sector and expedition by dividing
the number of females by the total number of individuals
from both sexes. For the female proportion calculation, we
excluded individuals whose sex was not identified and indi-
viduals younger than 2 years (Corti et al. 2010; Brice~ no
et al. 2013). The fawn:female ratio was calculated for every
sector and expedition by dividing the observed number of
fawns by the observed number of adult females. However,
for November expeditions, this value closely represents the
fertility rate, for March expeditions – which occur at least
3 months after the birthing period – this value represents a
combination of fertility and fawn survival in the initial
months.
To investigate differences in density, female proportion
and fawn:female ratio across regions and sectors, we used
each survey in each sector (e.g. Pampa survey of November
2019) as an observation and performed a Kruskal–Wallis
Rank Sum Test. When significant differences across regions
or sectors were encountered, we then performed pairwise
Wilcoxon Rank Sum tests with Bonferroni correction for
the P-value (two-sided) to identify which regions or sectors
were different from the others. Before performing these
tests, we checked for independence of observations within
each sector by calculating the temporal autocorrelation
using the Spearman correlation index between lagged
observations (Appendix S3). Additionally, we tested
whether the proportion of huemul in each age class was dif-
ferent across regions and sectors by performing Chi-Square
tests with each individual huemul as an observation.
Finally, we examined patterns in average group size of
huemul when females, males and fawns were present, as
well as by sector, region and season for our standardized
survey data from November 2016 to November 2019, using
each group sighting as an observation. We performed
Kruskal–Wallis Rank Sum tests to investigate differences
across regions and sectors, followed by pairwise Wilcoxon
Rank Sum tests with Bonferroni correction for the P-value
(two-sided) if needed to identify which regions or sectors
were different from the others. To investigate differences
Average sighting Minimum sighting Maximal sighting
distance (m) distance (m) distance (m)
47.71 (n = 7) 4 120
82.26 (n = 46) 0 500
40 (n = 2) 20 60
75.81 (n = 22) 0 400
213.38 (n = 8) 46 700
40.67 (n = 3) 20 52
163.5 (n = 4) 50 353
166.14 (n = 14) 2 500
© 2022 Ecological Society of Australia.
 CRITICAL HUEMUL POPULATION IN DECLINE 959

between groups with and without fawns, we performed a
Wilcoxon Rank Sum test (two-sided). P-values lower than
0.05 were considered to be significant in all tests.
Estimating the current population size by
including undetected individuals
To estimate the population size of huemul in the region
based on the number of sighted individuals, we needed to
account for imperfect detection during our surveys. Avail-
able methods to calculate detection probabilities are dis-
tance sampling (Buckland et al. 2015) or following marked
individuals to retroactively estimate detection probability
(Wittmer et al. 2010). Both of these methods were not fea-
sible in Bernardo Fjord. The number of observations in
each survey was too small to be able to successfully esti-
mate detection probability as a function of sighting distance
for each sector and survey (Buckland et al. 2015), and visi-
bility across sectors was too heterogenous to allow pooling
of all observations and calculate a single detection probabil-
ity (Appendix S1). Moreover, the remoteness and terrain
made following marked individuals nearly impossible.
Therefore, we estimated the number of undetected individ-
uals by combining our database of sighted individuals with
survival and fertility rates from the literature. To our
knowledge, this is an innovative method that can be applied
in situations in which species ecology, terrain characteristics
and logistical difficulties prevent the use of more estab-
lished methods to account for undetected individuals, as
long as survival and fertility rates are available from another
population.
We estimated the number of undetected individuals for
every austral summer survey as this provided a larger sam-
ple size. We used survival and fertility rates from the
literature (Table 2, Appendix S1) to calculate the expected
contribution of each individual in 1 year to the population
in the next year (Caswell 2001). This generated a number
of expected individuals in the next year, which was com-
pared with the number of observed individuals to arrive at
an estimate of undetected individuals for that year. The
estimated population size for that year was then calculated
as the sum of observed and undetected individuals, and this
estimate was used as the base number to calculate the
expected contribution of each individual for the next year.
Those steps were done first within each sector and then
summarized across sectors for a total population estimate
for each year; we started with data from the austral summer
of 2017 and finished with an estimated population size for
the austral summer of 2019. To account for possible varia-
tion in vital rates and incorporate uncertainty in our esti-
mate, we conducted 1000 simulations, each time using a
different set of fertility and survival rates. These vital rates
were randomly sampled from a normal distribution with a
mean set to the calculated vital rate average and standard
deviation set to a value that took into account the average
variability in ungulate vital rates from the literature (Gail-
lard et al. 2000; Wittmer et al. 2010) (Table 2). Then, we
used the mean and standard deviation of the 1000 repli-
cates of population size calculated for the austral summer
of 2019 to arrive at our final estimate of the huemul popu-
lation size in the Bernardo Fjord region.
Culpeo fox diet & presence
During selected expeditions (November 2016, March 2017,
March 2018, November 2018, and March 2019), we col-
lected scat piles of culpeo fox encountered during huemul
surveys, to analyse fox diet and spatial distribution in

Table 2. Rates used in the estimation of undetected individuals

Values used
Rate (mean  SD) Source

Fertility 0.72  0.11 Mean value from Corti et al. (2010) and standard deviation
considering an average variability of 15% from Wittmer
et al. (2010)
Fawn survival (November–March) 0.50  0.10 Estimated using an exponential decay function fitted with mean values
from Corti et al. (2010) and considering an average variability of
40% from Wittmer et al. (2010)
Fawn survival (March–March) 0.65  0.15 Estimated using an exponential decay function fitted with mean values
from Corti et al. (2010) and considering an average variability of
40% for fawns and 15% for yearlings from Wittmer et al. (2010)
Yearling survival (March–March) 0.89  0.13 Estimated assuming constant survival throughout the year with data
from Corti et al. (2010) and an average variability rate of 15%
from Wittmer et al. (2010)
Juvenile survival (March–March) 0.91  0.09 Estimated assuming constant survival throughout the year with data
Females 0.93  0.09 from Corti et al. (2010) and an average variability rate of 10%
Males 0.86  0.09 from Wittmer et al. (2010)
Adult survival (March–March) 0.91  0.09 Average adult survival from Wittmer et al. (2010), sex-specific adult
Females 0.94  0.09 survival from Corti et al. (2010) and average variability rates of
Males 0.83  0.08 10% from Wittmer et al. (2010)
Female proportion 0.64  0.05 This study

Details of how these rates were calculated, their differences, and how they were used to estimate the expected number of
individuals from 1 year to the next, can be found in Appendix S1.

© 2022 Ecological Society of Australia. doi:10.1111/aec.13178

960 S. M. PACK ET AL.

Bernardo Fjord. For each collected sample, we recorded
the date, UTM coordinates and sector, and later processed
unique sample piles by placing into a fine sieve and rinsing
to remove digested material, drying over low heat (200°F)
and examining the remaining contents under a microscope.
In each scat pile, we noted the presence or absence of hue-
mul hair, rodent hair or bones, insects, birds, berries and
fish. We referenced Cheh
ebar and Mart
ın (1989) to differ-
entiate huemul from fox and rodent hairs by their length,
colour and shape. We calculated the frequency of occur-
rence of each dietary component by dividing the number of
scat samples containing each component by the total num-
ber of scat samples, and mapped the spatial distribution of
huemul remains and collected fox scat, noting which scat
piles contained huemul hair. We tested whether the propor-
tion of fox scat containing huemul hair was different across
survey sectors and seasons by performing Chi-square tests
using each scat sample as an observation, with P-values
below 0.05 considered to be significant, and repeated this
test for berries.
RESULTS
Field surveys
not correlated with the total number of individuals
seen, both when considering the total distance
walked (r = 0.21, P = 0.07) and the number of peo-
ple in the group (r = 0.14, P = 0.15).
From October 2014 to March 2020, we docu-
mented a total of 284 observations involving 548
individual huemul including 70 fawns
(Appendix S2); these initial figures include double
counts between seasons and are not a population
estimate. Of fawns, 87.1% (n = 61) were observed in
the Bernardo Valley region, the majority of these
(n = 42) in the Pampa sector, and the remaining
8.6% (n = 6) in Ofhidro and 4.3% (n = 3) in Hue-
mules Valley regions. We generated photo records
for 76 observations and compiled 158 photographs
into a photo-database (Appendix S2). We observed
huemul in all sectors surveyed and our opportunistic
sightings demonstrated huemul presence in addi-
tional locations (Fig. 2).
Excluding any potential double counts of individu-
als within the same expedition, the Pampa sector
consistently held the most individuals, reaching 35
individuals observed in one expedition compared to a
maximum of 12 in other sectors (Fig. 3).

We compiled huemul sightings data from 16 expedi-

tions to Bernardo Fjord from 9 October 2014 to 14
March 2020, during which we spent a total of
254 days in the field. Of these, we utilized standard-
ized survey methodologies in seven expeditions from
11 November 2016 to 14 March 2020, which totalled
to 69 days spent surveying for huemul. Each expedi-
tion lasted an average of 9 days and involved an aver-
age of nine observers (Table 3). Survey effort was
Assessing long-term population trends
Huemul densities (including all age classes) in Ber-
nardo Fjord encountered from 2016 to 2019 were
smaller than those estimated for the period 2004–
2008 by Brice~ no et al. (2013) (W6,6 = 32.5,
P = 0.01), and the same trend was found for the
Huemules Valley (W6,4 = 21, P = 0.03; Fig. 4).

Table 3. Expeditions for huemul surveys conducted by Round River Conservation Studies and CONAF from 2014–2020

Expedition dates Expedition lead # Of surveyors† Km surveyed

November 27–30, 2014 CONAF 2 NR

October 8–29, 2014 RRCS 13 24.5
January 18–26, 2015 CONAF 2 NR
February 2–19, 2015 RRCS 16 24.2
July 15–October 25, 2015 CONAF 2 NR
January 29–February 23, 2016 RRCS 12 29.9
December 12, 2016 CONAF 2 NR
November 11–22, 2016‡ RRCS 12 70.5
March 8–21, 2017‡ RRCS 14 61.6
July 4, 2018 CONAF 2 NR
March 9–19, 2018‡ RRCS 15 112.2
October 23, 2018 CONAF 2 NR
November 12–21, 2018‡ RRCS 11 55.8
March 22–April 1, 2019‡ RRCS 15 114.4
November 10–17, 2019‡ RRCS 10 97.9
March 12–14, 2020‡ RRCS 6 9.3

NR, not recorded.

†
Of these surveyors, on average two were from CONAF and the remainder were from RRCS.
‡
These are standardized surveys used in the demography analysis of this paper.

doi:10.1111/aec.13178 © 2022 Ecological Society of Australia.

 CRITICAL HUEMUL POPULATION IN DECLINE
(a)
Fig. 2. Location of huemul sightings from opportunistic and survey expeditions from 2014 to 2020 in the surroundings of
Bernardo Fjord (a) and Ofhidro Fjord (b).
Considering the Refugio, Valle Bajo and Pampa sec-
tors as part of the Bernardo Valley, the average hue-
mul density in Bernardo Valley was 60% lower in
2016–2019, at 3.48 (SD 1.66) ind km 2 than in
2004–2008, at 8.47 (SD 3.45) ind km 2. In Hue-
mules valley, the density was 68% lower in 2016–
2019 at 0.52 (SD 0.61) ind km 2 than in 2004–
2008, at 1.62 (SD 0.73) ind km 2. These trends
were the same regardless of the sectors considered as
part of Bernardo Valley (Appendix S3).
Estimating demographic indices
From November 2016 to November 2019, we docu-
mented 108 observations of huemul in our standard-
ized survey routes, totalling between 17 and 50
unique individuals observed per seasonal expedition
(Table 4). Across all areas surveyed in each expedi-
tion, we documented an average density of individu-
als older than 1 year of 2.06 ind km 2 (SD 1.2)
(Table 4). There were marked variations in the num-
ber of sighted individuals and huemul density across
expeditions; for example, density in March 2017 was
© 2022 Ecological Society of Australia.
961
(b)
more than double the density of most other expedi-
tions (Table 4).
Densities were different across regions (H = 10.6,
d.f. = 2, P = 0.005) and sectors (H = 25.8, d.f. = 7,
P < 0.001), with Valley Bernardo and Ofhidro
regions presenting higher densities than the Hue-
mules region (Huemules vs. Bernardo: W = 268,
Nhuemules = 23, Nbernardo = 16, P = 0.04, two-sided;
Huemules vs. Ofhidro: W = 0, Nhuemules = 16,
Nofhidro = 4, P = 0.007, two-sided). Although pair-
wise Wilcoxon Rank Sum tests did not indicate
which sectors presented statistically different densi-
ties, we can note that the highest densities of huemul
were encountered in the Pampa, Refugio and Ofhi-
dro sectors (Table 5).
Adult individuals comprised the majority of the
observed population, which also had on average
more females than males. The overall mean female
proportion, including adults and juveniles, was
skewed towards females (mean 0.64  SD 0.05)
(Table 4), and this trend was slightly more marked
when considering just adults (mean 0.66  SD
0.05). The female proportion did not differ signifi-
cantly across survey regions (H = 5.27, d.f. = 2,
doi:10.1111/aec.13178
962 S. M. PACK ET AL.

Fig. 3. Number of huemul individuals observed within all RRCS survey sectors from 2014 to 2020. Double counts have
been eliminated so these data represent unique individuals within each expedition. Note that the y-axis scale is different for
the sector Pampa. NS, not surveyed; V, Valle.

doi:10.1111/aec.13178 © 2022 Ecological Society of Australia.

 CRITICAL HUEMUL POPULATION IN DECLINE
Fig. 4. Density of huemul of all age classes encountered
in standardized surveys conducted in a previous study
(Brice~
no et al. 2013) and in this study in the Bernardo and
Huemules Valley of the Bernardo Fjord. Black lines repre-
sent mean density for each study and grey shadings repre-
sent standard deviations.
P = 0.07) or sectors (H = 8.11, d.f. = 6, P = 0.23)
(Table 5). The average fawn:female ratio for Novem-
ber expeditions was 0.22  SD 0.07 and 0.18  SD
0.23 for March expeditions (Table 4), and did not
differ significantly across regions (H = 0.48, d.f. = 2,
P = 0.78) or sectors (H = 7.03, d.f. = 6, P = 0.32)
(Table 5). The highest number of fawns were
observed in the Pampa, Refugio and Ofhidro sectors
(Fig. 3), although age structure did not vary signifi-
cantly across survey regions (v2 = 8.43, d.f. = 6,
P = 0.21) or sectors (v2 = 19.01, d.f. = 18,
P = 0.39).
Of our 108 observations during standardized sur-
veys, group size varied from 1 to 6 individuals, with a
mean of 1.77 (SD 1.06) individuals. The majority
of observations were of a solitary huemul (51.4%) or
a group of two individuals (31.2%). The average
group size remained around 2 individuals, regardless
of whether a male (adult or juvenile;
mean = 2.01  SD 1.21) or a female (adult or juve-
nile; mean = 1.97  SD 1.12) was present in the
group. However, when a fawn was present in the
group, the mean group size was 2.83 (SD 1.25),
significantly larger than when fawns were absent
(W = 288, Nfawn = 18, Nnofawn = 90, P < 0.001, two-
sided). Group size did not vary across sectors
(H = 11.7, d.f. = 6, P = 0.07) but significantly dif-
fered between survey regions (H = 6.64, d.f. = 2,
© 2022 Ecological Society of Australia.
963
P = 0.04). Although pairwise Wilcoxon Rank Sum
tests did not indicate which regions presented statisti-
cally different group sizes, larger groups of huemul
were encountered in the Ofhidro region, with average
group size of 2.23 (SD 0.93) compared to 1.74
(SD 1.09) in Bernardo Valley and 1.53 (SD 0.92)
in Valle Huemules (Table 6).
During all expeditions, we tracked the survival of
the 10 adult individuals that were marked by
CONAF with coloured ear tags in August 2016 and
2018. The number of days since capture that a
tagged individual was last observed averaged
432 days, ranging from a minimum of 94 days to a
maximum of 1190 days or 3.3 years. The foot injury
treatment that CONAF applied during capture
appears to have been largely successful: of the eight
individuals that were treated for a foot ailment upon
their capture in 2016 or 2018, seven did not present
a limp or foot injury at their last sighting. Tagged
individuals were not seen on most surveys of their
tagging site: although we conducted six surveys of
the Pampa, on average each tagged individual was
only seen on two of the six surveys. When re-sighted,
however, individuals were always located in the same
sector where they were captured.
Estimating the current population size by
including undetected individuals
We estimate the huemul population size for the Ber-
nardo Fjord region in the austral summer of 2019 to
be 84 (SD 8) individuals. Because we directly
observed 44 individuals during this 2019 survey, we
estimate that 40 (SD 7) individuals were unde-
tected by our surveys, arriving at a detection proba-
bility of 52%. We estimate 69% of all individuals to
be located in the Bernardo Valley, especially in the
Pampa sector which holds an estimated 50% of the
Bernardo Fjord huemul population. The Pampa was
also the sector with the highest proportion of fawns
with 46.7% of the total estimated fawns, followed by
the Ofhidro sector with 26.7% (Table 7).
Culpeo fox diet & presence
We collected and identified the contents of 101 piles
of culpeo fox scat over five expeditions, huemul hair
in 15% of scats, rodent in 88%, berries/fruits (B. mi-
crophylla, E. rubrum, G. mucronata) in 62%, birds in
41%, insects in 32% and fish scats in 0.9%. The pro-
portion of scats containing huemul hair differed by
sector (v2 = 20.9, d.f. = 5, P < 0.001), with the high-
est rates in GLOF (60%, N = 10), Pampa (20%,
N = 15), Refugio (12.5%, N = 40) and Valle Toros
(4%, N = 24). Some of the samples containing
doi:10.1111/aec.13178
 964

Table 4. Observed number of huemul individuals by sex and age class and demographic variables for each survey expedition in the Bernardo Fjord (M = male, F = female,

doi:10.1111/aec.13178
U = unknown sex; V=Valle)

Observed
S. M. PACK ET AL.

Adults Juveniles Yearlings

Area surveyed Female Fawn: female Density
Year Month Sectors surveyed (km2) F M U F M U F M U Fawns Total proportion ratio (ind km 2)

2016 Nov Pampa, V Bajo, Refugio, 18.04 16 8 0 0 0 0 1 0 0 4 29 0.67 0.25 1.39

Terrazas, V Huemules
and V Toros
2017 Mar GLOF, Pampa, V Bajo, 14.32 31 13 0 2 0 0 0 0 3 1 50 0.72 0.03 3.42
Refugio, Terrazas, V
Huemules and V Toros
2018 Mar GLOF, Pampa, V Bajo, 20.03 18 7 0 0 2 0 0 0 0 3 30 0.67 0.17 1.35
Refugio, Terrazas, V
Huemules, V Toros and
Ofhidro
2018 Nov GLOF, Pampa, V Bajo, 11.68 11 6 0 0 1 0 0 0 0 3 21 0.61 0.27 1.54
Refugio, Terrazas and
Ofhidro
2019 Mar GLOF, Pampa, V Bajo, 19.54 20 10 0 1 1 0 1 1 0 10 44 0.66 0.50 1.74
Refugio, Terrazas, V
Huemules, V Toros and
Ofhidro
2019 Nov Pampa, V Bajo, Refugio, 17.61 7 5 1 1 1 0 1 0 0 1 17 0.57 0.14 0.91
Terrazas, V Huemules, V
Toros and Ofhidro
2020 Mar Refugio 1.22 3 2 0 0 0 0 0 0 0 0 5 0.60 0.00 4.10
Mean  SD 0.64  0.05 Nov: 0.22  0.07 2.06  1.20
Mar: 0.18  0.23

© 2022 Ecological Society of Australia.

 CRITICAL HUEMUL POPULATION IN DECLINE 965

Table 5. Demographic variables of huemul by region and sector in the Bernardo Fjord

Expeditions Density
to the Female proportion Fawn:female ratio (ind. km 2,
Region and sector Dates surveyed sector (mean  SD) (mean  SD) mean  SD)

Bernardo Valley 0.61  0.12 0.20  0.30 2.44  2.46

region
† †
GLOF Mar 2017, Mar 2018, Nov 4 00
2018, and Mar 2019
Pampa Nov 2016, Mar 2017, Mar 6 0.66  0.06 0.25  0.23 3.13  1.88
2018, Nov 2018, Mar
2019, and Nov 2019,
Valle Bajo Nov 2016, Mar 2017, Mar 6 0.58  0.12 00 1.81  2.89
2018, Nov 2018, Mar
2019, and Nov 2019
Refugio Nov 2016, Mar 2017, Mar 7 0.57  0.15 0.21  0.39 3.78  2.3
2018, Nov 2018, Mar
2019, Nov 2019, and
Mar 2020
Huemules region 0.82  0.22 0.26  0.43 0.4  0.42
Terrazas Nov 2016, Mar 2017, Mar 6 0.79  0.25 00 0.42  0.39
2018, Nov 2018, Mar
2019, and Nov 2019,
Valle Huemules Nov 2016, Mar 2017, Mar 5 10 0.50  0.71 0.3  0.42
2018, Mar 2019, and
Nov 2019,
Valle Toros Nov 2016, Mar 2017, Mar 5 0.75  0.25 0.44  0.51 0.47  0.53
2018, Mar 2019, and
Nov 2019
Ofhidro region 0.60  0.08 0.46  0.63 3.22  1.1
Ofhidro Mar 2018, Nov 2018, Mar 4 0.60  0.08 0.46  0.63 3.22  1.1
2019, and Nov 2019
†
No huemul was seen during a standardized survey in the GLOF sector, so female proportion and fawn:female ratio do not
apply.

Table 6. Huemul group size by region and sector in the containing huemul hair did not vary across survey
Bernardo Fjord
seasons (v2 = 0.0712, d.f. = 1, P = 0.79), whereas
Region and sector N Group size (mean  SD) the proportion of scats containing berries did differ
significantly by season (v2 = 20.7, d.f. = 1,
Bernardo Valley region 80 1.74  1.09 P < 0.001) with scats found in the austral summer
†
GLOF 0 containing a higher proportion of berries. Addition-
Pampa 57 1.84  1.21 ally, we observed many culpeo foxes during each
V Bajo 4 1.25  0.50
expedition, and the individuals showed signs of
Refugio 19 1.53  0.70
Huemules region 15 1.53  0.92 excellent health in their size, body mass and coat
Terrazas 7 1.29  0.50 sheen (Appendix S2).
V Huemules 3 1  0 Additionally, we documented the presence of 18
V Toros 5 2.2  1.30 unique huemul remains, including four fresh car-
Ofhidro region 13 2.23  0.93 casses, seven older skeletons and seven craniums
Ofhidro 13 2.23  0.93 (Fig. 5). Six of the 18 remains were of fawns, 11
†
No huemul was seen during a standardized survey in the
were of adults, and 1 was of unknown age. Two of
GLOF sector, so female proportion and fawn:female ratio the remains indicated a possible cause of death,
do not apply. including one adult male carcass with a dislocated
back leg joint and one fawn that likely drowned in
the rising tide. At least five remains – two adults and
huemul hair also included huemul skin, large pieces three fawns – showed signs of fox scavenging, includ-
of fatty tissue (1 9 1 cm) and a strong smell of car- ing body and joint distortion, torn flesh and the pres-
rion after washing, which was not present in other ence of nearby fox scat and hair. The remains were
scat samples. The proportion of scat samples concentrated on the Pampa sector (n = 9), followed

© 2022 Ecological Society of Australia. doi:10.1111/aec.13178

 966 S. M. PACK ET AL.

by GLOF (n = 4), Refugio (n = 3), Terrazas (n = 1)

Table 7. Number (mean  SD) of estimated huemul individuals present in the study regions and sectors of Bernardo Fjord in the austral summer of 2019, divided by sex

13  1 (15.5%)

13  1 (15.5%)
58  6 (69%)
and Ofhidro (n = 1) (Fig. 5).

Total

42  5

11  0

13  1
84  8
00

51

50
20
61
DISCUSSION

Using the same methodology as previous studies, we

observed significantly lower huemul densities in
1 (100%)
Unknown sex

2016–2019 than those reported in 2004–2008 by

0 (0%)

0 (0%)
Brice~no et al. (2013) or by Wensing (2005), pointing
to a decline in the huemul population in the Ber-
0
1
0
0

0
0
0

0
1












nardo region over the past 15 years. This is in con-
3
0
3
0
0
0
0
0
0
0
0
3
trast to previous studies that indicated an increasing
population (Frid 1999; Wensing 2005; Brice~ no
et al. 2013). Despite the decline, huemul densities in
12  1 (70.6%)

3  0 (17.6%)

2  0 (11.8%)

Bernardo Valley (3.48 huemul km 2) are almost

Male
Adults

twice as large as those observed in inland locations

(1.79  0.33 huemul km 2) (Corti et al. 2010). Our
17  1
00
71
10
40

20
00
10

20

estimate of 84  8 individuals inhabiting the region

accounts for 6 to 8% of the estimated global popula-
tion of huemul, a disproportionately high number
considering that 101 subpopulations are thought to
26  3 (72.2%)

6  0 (16.7%)

4  0 (11.1%)

exist (Vila et al. 2006; Black-Decima et al. 2016).

Female

While the cause of the apparent decline is unclear,

we have identified potential factors that could be
19  3

36  3
00

20
50

20
10
30

40

driving higher mortality and or lower recruitment

among the Bernardo population.
0 (33.3%)

0 (66.6%)

Possible drivers of the population decline

Numbers in parenthesis are the percentage of the total for each sex and age class.
Juveniles

0 (0%)

One factor that could explain a decline in the huemul

0
0
0
0

0
0
0

0
0

population is poor recruitment. We reported lower














fawn:female ratios (0.22  SD 0.07 for November

1
0
1
0
0
0
0
0
0
2
2
3

and 0.18  SD 0.23 for March) than those reported

in inland habitats (0.72  0.20; Corti et al. 2010).
7  2 (70%)

2  0 (20%)

1  0 (10%)

However, this comparison should be made with cau-

Yearlings

tion as the latter estimate is from a study where all

10  2

huemul individuals were radio-collared and moni-

00
52
10
10

00
10
10

10

tored to assess reproduction and survival (Corti

et al. 2010), a method that certainly resulted in a
higher fawn detection rate than our methods and
study site allowed. Nonetheless, taking into account
2  0 (13.3%)

4  0 (26.7%)
9  2 (60%)

Corti’s fertility rate of 0.72 and 50% survival over

Fawns

summer, the numbers we encountered in March,

15  2

when fawns are more visible, are still lower than

00
72
10
10

10
00
10

40

those observed in inland populations.

Although predation by culpeo is the leading cause
of huemul fawn mortality in many populations (Corti
et al. 2010), our data did not present decisive evi-
Bernardo Valley region

dence pointing to fox as a main cause of huemul

Valle Huemules

population decline since 2008. Although we docu-

Huemules region
and age classes

Ofhidro region

mented that huemul are being consumed by culpeo

Valle Toros
Valle Bajo

fox, with 15% of scat piles containing huemul hair,

Terrazas

Ofhidro
Refugio
Pampa
GLOF

culpeo are long-time residents (Frid 1999) and there

Sector

Total

is limited evidence to support the theory that huemul

possess inadequate predator responses due to
doi:10.1111/aec.13178 © 2022 Ecological Society of Australia.
 CRITICAL HUEMUL POPULATION IN DECLINE
(a)
Fig. 5. Spatial distribution of collected culpeo fox scat and encountered huemul remains from 2014 to 2020 in the sur-
roundings of Bernardo Fjord (a) and Ofhidro Fjord (b).
evolutionary absence of predators (Flueck & Smith-
Flueck 2012). Rather, if Bernardo culpeo are heavily
reliant on huemul prey, we would expect the fox
population to eventually decline in response to a
decline in huemul, allowing the population to
recover. That is, unless there are additional, and nov-
el, species interactions influencing the system. A the-
ory held by a long-term park guard (Paredes, F.,
pers. comm., 11/21/19) is that since the previous
study occurred, the abundance of non-native salmon
in Bernardo Fjord has increased, providing a winter
food source for foxes that reduces winter mortality,
thus increasing predation pressure on huemul fawns.
Although this theory was not directly supported by
our data as we only found fish scales in one fox scat,
ecosystem impacts of non-native salmonids have
been noted at other sites (Novaro et al. 2000; Zava-
leta et al. 2001) and could warrant further research
as a potential ecosystem change influencing huemul
in Bernardo.
Alternatively, another compelling explanation of the
apparent decrease in population size is that putative
parapoxvirus (Chordopoxvirinae subfamily)-associated
© 2022 Ecological Society of Australia.
967
(b)
foot disease, which would have been introduced to
Bernardo by domestic cattle, is leading to elevated
huemul mortality. In a study of foot lesions in 24 hue-
mul from Bernardo O’Higgins National Park between
2005 and 2010, Vila et al. (2019) found that males
were 2.59 more likely to be infected with parapoxvirus
and 2.49 more likely to display lesions. Animals with
foot disease show signs of intense pain and reduced
mobility followed by loss of body condition and
recumbency, which often precedes death. Morbidity
and mortality in that study reached 80% and 40%
respectively (Vila et al. 2019).
The higher male mortality due to parapoxvirus
could also potentially explain the skewed female pro-
portion encountered in this study (0.64  SD 0.05),
which is outside the range of 0.44–0.63 (mean of
0.51) estimated for the inland huemul population at
Lago Cochrane National Reserve (Wittmer
et al. 2010) and higher than ratios reported previ-
ously for the same population (0.48 for Huemules
Valley and 0.50 for Bernardo Valley; Brice~ no
et al. 2013). This statement needs to be made with
caution, because it is common for dimorphic species
doi:10.1111/aec.13178
968 S. M. PACK ET AL.
with opportunistically polygynous mating systems,
such as deer, to exhibit a female-biased sex ratio
(Mysterud et al. 2000). However, the differences in
female proportions when compared to inland popula-
tions and from surveys of this population from previ-
ous years suggest additional factors might be playing
a role in driving the current higher proportion of
females in Bernardo Fjord region.
Moreover, habitat and weather at Bernardo,
including extremely wet conditions and rugged, rocky
terrain, may create additional complications for hue-
mul affected with foot disease (Vila et al. 2006;
CONAF 2015), and nutritional deficiencies linked to
marginal habitat conditions may confer additional
disease susceptibility (CONAF 2015). Huemul con-
fined to mountainous areas are known to have diets
deficient in trace minerals like Selenium, impairing
bone metabolism and resulting in hoof ailments,
lameness, and bone deformities, especially in males
(Flueck et al. 2014; Flueck 2015, 2020; Flueck &
Smith-Flueck 2017). Our experience and those of
local park guards and managers indeed indicates that
small, deformed antler are the norm at Bernardo
(CONAF 2015), as well as are foot problems result-
ing in limping, swollen joints and mortality. If para-
poxvirus is indeed driving the decline of this
population, directly or indirectly through changes in
adult sex ratio, it would dispel the claim that “no evi-
dence supports. . .disease from livestock as having
caused declines” in huemul (Flueck & Smith-
Flueck 2012).
Management implications
The Bernardo Fjord region is currently zoned as an
“Untouchable Zone” – a zoning similar to that of a
“wilderness” category – under the 2018 Bernardo
O’Higgins National Park Public Use Plan for the
Ays
en region (CONAF 2018). This zoning prohibits
development and tourism and allows only visitation
and use related to scientific study and management.
However, in our years at the site, we witnessed
groups ranging from tourists, adventure groups and
fishermen visiting the Pampa and Refugio sectors.
Given that it contains the world’s largest breeding
population of endangered huemul deer, one that
appears to be declining due to unclear causes, we
support a precautionary approach that maintains this
zoning and its active enforcement.
We have observed that this population, within a
habitat that has experienced relatively little human
impact, has shown variation in density and demo-
graphic rates in recent years. Given its conservation
relevance, increased monitoring efforts are needed to
better understand the possible causes of these trends.
Threats to huemul in the fjords likely differ from
doi:10.1111/aec.13178
inland habitats where domestic dogs and habitat loss
present the main risks (Black-Decima et al. 2016);
however, based on our findings, both inland and
coastal populations may share the impacts of diseases
transmitted from domestic cattle. Active management
may improve conservation outcomes in these remote
areas. For example, during our study, seven of the
eight huemul treated for their foot injury by CONAF
in 2016 did not present with an injury when last re-
sighted over a year later. Therefore, periodic sanitary
interventions could be an effective strategy for reduc-
ing huemul mortality from parapoxvirus-associated
foot injuries in the future. In order to determine
whether parapoxvirus is indeed driving the observed
population decline, future studies might generate
comparative demographic data, specifically female
proportion and fawn:female ratios, in coastal popula-
tions of Bernardo O’Higgins National Park without
historic presence of cattle. Alternatively, should more
research capacity become available in the Park, an
experimental approach to management could be
explored, which would test the efficacy of various
treatments addressing different hypothesized causes
of the decline. These treatments, each applied to dif-
ferent sectors, could involve treating parapoxvirus
lesions, providing mineral supplements and control-
ling fox populations.
Beyond reporting on the population trend of hue-
mul in Bernardo Fjord, we have used an innovative
method to account for undetected individuals that
can be applied in other studies that aim to estimate
population size of low-density, difficult-to-observe
species, especially those that display strong trends of
philopatry. However, this method requires detailed
data on fertility and survival rates, which in our case
were only available for inland areas. Hence, the accu-
racy of our population estimates is dependent on the
similarity between demographic rates of fjords and
inland areas. This is an important topic for huemul
research and conservation, as our results suggest that
population dynamics differ between inland and
coastal regions. For example, lower survival rates for
huemul in the fjords might explain some of the
encountered differences in female proportion or
fawn:female ratio. If this is the case, our estimates
might be overestimating the size of the huemul popu-
lation in the Bernardo Fjord.
Nonetheless, in the absence of local demographic
parameters, estimating undetected individuals with
the best available information is a step forward from
previous surveys in the region in which population
estimates were based only on detected individuals
(Brice~no et al. 2013). To avoid overestimating the
huemul population, we were conservative in our
methods by considering individuals of same sex and
age observed in different years in the same sector as
the same individual. Overall, despite its limitations,
© 2022 Ecological Society of Australia.
 CRITICAL HUEMUL POPULATION IN DECLINE
we believe this to be a promising approach in the
cases were traditional methods such as distance sam-
pling are not viable. For future improvement, we rec-
ommend repeated surveys of the same area or the
permanent presence of park rangers to be able to
compare and verify the number of estimated and
observed individuals each year. Despite the time and
effort associated with this approach, we believe the
conservation importance of the huemul population in
the Bernardo Region, together with evidence pointing
towards a recent decline, warrant continued monitor-
ing and active management of this population,
enhanced conservation protections and zoning
enforcement, and investigation of possible drivers of
huemul population dynamics in the Chilean fjords.
ACKNOWLEDGEMENTS
This project would not have been possible without sup-
port from CONAF, especially the guardaparques Feli-
dor Paredes, Raul Pereda, Orlando Beltr
an, Fabio
Paredes, and Luis Paredes, who have accompanied us
with expertise and great ability in all our years working
in Bernardo O’Higgins National Park. We thank Piero
Caviglia of CONAF Ays
en for his leadership and sup-
port of our expeditions, and Carolina Panichine Faun-
des for her support in photo identification and ageing.
Last but not least, we thank the leaders of Round River
Conservation Studies including Fernando Iglesias
Letelier, Elizabeth Brunner, Scott Braddock, Valeria
Briones, Samara Moreira, Kyla Zaret, Gabriel Kayano,
Violeta Martinez Amigo and Jessica Hightower, and all
of the students who engaged in fieldwork through even
the most challenging weather from the Southern Patag-
onia Icefield. The authors declare that they have no rel-
evant or material financial interests that relate to the
research described in this paper, that they have no
industrial links or affiliations that could create a conflict
of interest with this research, and that they received no
financial support for the authorship or publication of
this article. The author(s) received no financial support
for the research, authorship, and/or publication of this
article.
AUTHOR CONTRIBUTIONS
Shalynn McKenzie Pack: Conceptualization (lead);
data curation (lead); formal analysis (supporting);
investigation (equal); methodology (equal); project
administration (lead); resources (equal); supervision
(equal); writing – original draft (lead); writing –
review and editing (lead). Diana Bertuol Garcia:
Conceptualization (supporting); data curation (sup-
porting); formal analysis (lead); investigation (equal);
methodology (equal); project administration (equal);
© 2022 Ecological Society of Australia.
969
resources (equal); software (lead); supervision
(equal); validation (lead); visualization (lead); writing
– original draft (equal); writing – review and editing
(equal). Matthew Pomilia: Conceptualization
(equal); data curation (supporting); formal analysis
(supporting); funding acquisition (lead); investigation
(supporting); methodology (lead); project administra-
tion (lead); resources (lead); supervision (lead); vali-
dation (supporting); visualization (supporting);
writing – review and editing (supporting). Adam
Spencer: Conceptualization (supporting); data cura-
tion (equal); investigation (lead); methodology (lead);
project administration (equal); resources
(supporting); writing – original draft (supporting);
writing – review and editing (supporting). Dennis
Aldridge: Conceptualization (equal); data curation
(supporting); formal analysis (supporting); funding
acquisition (equal); investigation (supporting);
methodology (equal); project administration (equal);
resources (equal); supervision (supporting); writing –
review and editing (equal).
CONFLICT OF INTEREST
The authors declare that they have no relevant or
material financial interests that relate to the research
described in this paper, and that they have no indus-
trial links or affiliations that could create a conflict of
interest with this research.
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SUPPORTING INFORMATION
Additional supporting information may/can be found
online in the supporting information tab for this article.
Appendix S1. Additional methods.
Appendix S2. Dataset and photo database online
repository.
Appendix S3. Additional results.
© 2022 Ecological Society of Australia.