Journal of Threatened Taxa |
www.threatenedtaxa.org | 17 February 2020 | 12(2): 15229–15237
ISSN 0974-7907 (Online) | ISSN 0974-7893
(Print)
doi: https://doi.org/10.11609/jott.5506.12.2.15229-15237
#5506 | Received 28 October 2019 | Final
received 25 January 2020 | Finally accepted 10 February 2020
Iberian Lynx Lynx
pardinus Temminck, 1827
(Mammalia: Carnivora: Felidae) in central Spain: trophic niche of an isolated
population
Pedro Alfaya
1, Ariadna Invernón
2 & Germán Alonso 3
1,2,3 Department of Biodiversity,
Ecology and Evolution, Complutense University of
Madrid. Avda. José Antonio Nováis
12, 28040 Madrid, Spain.
1 palfaya@ucm.es (correspondence
author), 2 arinvern@ucm.es, 3 galonso@ucm.es
Editor: Angie Appel, Wild Cat Network,
Bad Marienberg, Germany. Date
of publication: 17 January 2020 (online & print)
Citation: Alfaya,
P., A. Invernon & G. Alonso (2020). Iberian Lynx Lynx
pardinus Temminck 1827
(Carnivora: Felidae) in central Spain: trophic niche of an isolated population.
Journal of Threatened Taxa 12(2): 15229–15237. https://doi.org/10.11609/jott.5506.12.2.15229-15237
Copyright: © Alfaya
et al. 2020. Creative Commons Attribution
4.0 International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: Spanish Ministry
of Agriculture, Food and
Environment.
Competing interests: The authors
declare no competing interests.
Author details: Pedro Alfaya is a honorary research fellow in the Ecology Department of the
Universidad Complutense de Madrid. He is interested
in species conservation, landscape ecology and statistical modelling, but
currently he is working on environmental impact consulting. Ariadna Invernón: she is a Msc in ecology and collaborator of the Ecology Department
of the Universidad Complutense de Madrid. Germán Alonso is a lecturer of Ecology
in the Universidad Complutense Madrid. He has
alternated his research activity with public positions, being always linked to
environmental conservation, landscape ecology and land management.
Author contribution: PA made the bibliographic review,
statistical analysis, wrote the manuscript and participated in scat
collection. AI designed and carried out the identification of scat
samples content. GA provides support and experience in field work,
identification of scat content and also reviewed the manuscript.
Acknowledgements: We thank the Spanish Ministry of
Agriculture, Food and Environment (16MNSV002) for funding our study. We also appreciate the effort of Pilar,
Beatriz, and Alejandra for their hard work in the laboratory, and also to
Javier and Jorge for their assistance in the fieldwork.
Abstract: Understanding predator-prey
relationships is fundamental to develop effective conservation plans. Between 2015 and 2018, we combed 21
transects, each 7km long, searching for Iberian Lynx Lynx
pardinus scat within the province of Madrid in
central Spain. In order to minimise inherent subjectivity of visual identification as
much as possible, we performed a double specific nested polymerase chain
reaction (PCR) followed by a primer extension assay addressed to two Iberian
Lynx diagnostic single nucleotide polymorphisms. Forty-six scat samples were positively
identified as belonging to Iberian Lynx through genetic analysis. From these, we extracted remains of consumed
prey, which we determined to the lowest possible taxonomic level, mainly
through hair identification. Identified
prey was divided into four types: lagomorphs, small mammals, birds, and
ungulates. The species’ diet composition
was described based on the frequency of occurrence (FO) of each prey and niche
breadth, and also compared with prior knowledge of the species using four prior
studies as a comparative reference through the calculation of the niche overlap
value. The FO of lagomorphs (39%) was the
lowest, while the FO of small mammals (54%) was the highest recorded to
date. The niche breath (0.36) was higher
than recorded in prior studies, but still showing the specialist character of
the Iberian Lynx. Niche overlap was low
(C = 0.49), showing differences in trophic niche between the population
in our study area and the one studied in southern Spain. This indicates that the Iberian Lynx is adept
at switching its main prey, an ability that has previously been firmly
rejected. It is, however, capable of
adapting to alternative prey more often than recorded to date, which could be a
behavioural response to the patchy distribution of
European Rabbit Oryctolagus cuniculus
in the study area.
Keywords: Diet, lagomorphs, niche
breadth, niche overlap, single nucleotide polymorphism.
Introduction
The Iberian Lynx Lynx
pardinus is endemic to the Iberian peninsula
(Rodríguez & Delibes 1992), and is regarded as a trophic super specialist
(Ferrer & Negro 2004). Since the
1950s, the Iberian Lynx population has declined continuously (Valverde 1963; Cabezas-Díaz et al. 2009).
Only 93 individuals were recorded in 2002 (Guzmán et al. 2004). Following conservation measures such as
reintroductions of captive-bred Iberian Lynxes in southern Spain, this
population experienced a constant growth (Simón et al. 2011; Rodríguez & Calzada 2015), reaching 589 individuals in 2017 (Simón
2018). Furthermore, Cruz et al. (2019)
confirmed the presence of Iberian Lynxes outside the currently known range of
the species in the southern Iberian peninsula, suggesting the continued
existence of a stable population in central Spain within the province of
Madrid.
The diet of a species is a fundamental aspect
of its ecology that depends mainly on the abundance and availability of prey
types (Terraube & Arroyo 2011), but also on
learning and experience of individuals (Shipley et al. 2009). A widespread phenomenon in many vertebrate
and invertebrate taxa (Bolnick et al. 2003) is the
so- called ‘niche variation hypothesis’.
This occurs when some co-occurring individuals of a species actively
select different prey types in their shared environment (Araujo et al.
2011). The niche variation could be a
response to two main factors: (i) change in
environmental conditions that affects prey availability and prompts all
individuals of a population to use a larger spectrum of resources, or (ii) each
individual continues to use a narrow range of resources that diverges from
conspecifics, thus minimizing the interspecific competition (Costa et al.
2008).
Understanding predator-prey relationships is
fundamental to identify conservation priorities, prior to the design of
conservation programmes for vulnerable or endangered
species (Popp et al. 2018). Lacking
information on these relationships could result in ill-informed conservation
strategies that lead to a failure of reaching conservation goals and at the
same time to a gross waste of resources, as occurred in the Doñana
National Park with the restocking of European Rabbits Oryctolagus
cuniculus (Carro et al. 2019).
The knowledge about diet plasticity of a
species is a keystone to assess the transferability of results obtained in a
certain area to another, and for assessing whether an alternative management
will provide similar results (Terraube & Arroyo
2011). A relevant descriptor of niche is
breadth, which is a function of the proportion of each resource used with
regard to total consumed resources (Smith 1982). Therefore, a species that uses a wide range
of trophic resources in a similar proportion will show a high niche breadth and,
consequently, will be regarded as a generalist for studied resources (Symondson
et al. 2002). On the contrary, a species
that uses a high proportion of a narrow range of resources will be regarded as
a specialist (Shipley et al. 2009).
Rodríguez & Delibes (1992) were the last
authors who reported an Iberian Lynx population in the province of Madrid
before Cruz et al. (2019). The
territorial and solitary behaviour of the Iberian
Lynx (San Miguel 2006; Calzada et al. 2007; Martín et
al. 2007) results in a low-density spatial organization that makes it extremely
difficult to find and track (Alfaya et al.
2019). The central Spanish population
was already small in the early 1990s (Rodríguez & Delibes 1992), remained
elusive and was not considered in conservation programs initiated in 2002 (Rodríguez
& Calzada 2015) that lead to the recovery of the
population in southern Spain (Simón 2018).
Different studies carried out in Doñana National Park and in Sierra Morena showed that the
European Rabbit is its main prey, being present in 70–99% of analysed samples (Delibes 1980; Beltrán
& Delibes 1991; Palomares et al. 2001;
Gil-Sánchez et al. 2006). The Iberian
Lynx, however, also consumes other prey species in lower proportions, but their
relative importance increases when the availability of Rabbits decreases (Beltrán et al. 1985; Beltrán
& Delibes 1991). Therefore, Iberian
Lynxes also prey on small mammals, e.g., Wood Mouse Apodemus
sylvaticus and Garden Dormouse Eliomys quercinus (Aymerich 1982; Gil-Sánchez et al. 2006), wild ungulates
like Red Deer Cervus elaphus,
Fallow Deer Dama dama
(Delibes 1980; Beltrán et al. 1985; Beltrán & Delibes 1991; Gil-Sánchez et al. 2006), European
Mouflon Ovis orientalis
musimon (Gil-Sánchez et al. 2006), and birds such
as Red-legged Partridge Alectoris rufa, Mallard Anas platyrhynchos and Eurasian
Magpie Pica pica (Delibes 1980; Aymerich 1982; Beltrán &
Delibes 1991; Gil-Sánchez et al. 2006).
In this article, we report the diet
composition of Iberian Lynx, based on analysis of scat collected in a study
area in central Spain. We discuss the
trophic niche breadth of this population in the light of research conducted on
the species’ diet in southern Spain.
Study area
The research was performed in the western
region of the province of Madrid (Figure 1), which is delimited by boundaries
with the community of Castilla–León in the north and northwest, the community
of Castilla–La Mancha in the south, and the Manzanares River basin in the
east. The study area ranges in elevation
from 440 to 2,320 m. It represents three
main landscape regions: (i) the Guadarrama
Mountains, a mountainous granitic zone, (ii) the foothills with a gradient of
siliceous sand and soft slopes, and (iii) the depression, a terrain characterised by interfluvial hills (Rivas-Martínez 1982; Zabía & del Olmo 2007).
The meso-Mediterranean
zone is the dominant bioclimatic belt within the study area, but the oro- and supra-Mediterranean zones are also present in the Guadarrama Mountains (Rivas-Martínez 1982). The main climatic features of the study area
are the seasonal variation in temperature between -8°C and 44°C, summer drought
and irregular precipitation ranging from 400 to 2,000 mm per year (Zabía & del Olmo 2007).
The landscape in the study area is a mosaic
of pastures with scrub and Holm Oak Quercus ilex groves interspersed
with villages and patches of agricultural land (Schmitz et al. 2007; Image
1). Local people use pastures
traditionally during the summer for grazing transhumant cattle, periodically
perform selective logging in the forests and clean the understorey
(Arnaiz-Schmitz et al. 2018).
Material and Methods
Sample collection
Evidence of the presence of Iberian Lynxes
within the study area was collected between January 2015 and May 2018. We designed 21 transects of 7km each that
were combed by at least two researchers.
We searched for scat on foot along pathways and firebreaks, since both
Iberian Lynx and European Wildcat Felis silvestris usually move along such linear structures
(Lozano et al. 2013; Garrote et al. 2014).
Sometimes, we also combed other less regular landscape features such as
the bases of large rocks, around Rabbit holes and near rivers, where scat was
more likely to be found (Martín et al. 2007).
Along these transects, we searched for scat that is morphologically
compatible with scat of the Iberian Lynx.
This ranges in length from 5cm to 9cm and in width from 1.5cm to 2cm,
and is divided into several fragments (Rodríguez 1993). It ranges in colour
from ash-grey to dark-brown, and is entirely covered by a mucous patina when
fresh (Iglesias & España 2010).
The probability of an erroneous
identification of the scat of Iberian Lynx, however, is high (Boshoff &
Kerley 2010, Molinari-Jobin et al. 2012; Garrote & de Ayala 2015). It has been often misidentified due to its
similarity with the scat of European Wildcat and Red Fox Vulpes vulpes (Palomares et al.
2002). To reduce this probability as
much as possible, we performed a specific genetic identification analysis
designed by Cruz et al. (2019). This
genetic analysis consists of a double specific nested PCR followed by a primer
extension assay addressed to two Iberian Lynx diagnostic single nucleotide
polymorphisms (SNPs). The product of the
double nested PCR is already specific for the Iberian Lynx since we used the
primer DL7F [5’-CTT AAT CGT GCA TTA TAC CTTGT-3’] developed by Palomares et al. (2002), which was aligned to sequences of
orthologue carnivores including Eurasian Lynx Lynx
lynx, Canada Lynx L. canadensis, European
Wildcat, and Domestic Cat Felis catus in order to select diagnostic positions. Then we identified two SNPs specific of the
Iberian Lynx. These SNPs were marked
with fluorescence and detected through a capillary electrophoresis. This method of analysis provides an increase
of sensitivity and straightforward verification of the belonging species
through the diagnostic SNPs, being strongly protected against false positive
results. For further details see Cruz et
al. (2019).
Content analysis
Subsequent to positive genetic identification
of scat samples as belonging to the Iberian Lynx, we analysed
the contents of these samples. We used a
stereomicroscope to identify and remove remains of consumed prey like broken
bones, teeth, feathers, and hair. Teeth
and bone remains were identified with a stereomicroscope, while feathers and
hair required the use of a 40x microscope.
We washed hairs, first with distilled water and detergent, and then with
70% alcohol as described in Teerink (1991). After drying hairs, we poured a thin layer of
transparent nail varnish over a slide and let it dry for 30 seconds. Then we put each hair on the slide for 30
minutes and covered it with a cover glass.
That way, we obtained a hair cuticle mould
with a scale pattern showing a certain, although limited, taxonomic value
(Short 1978).
Removed remains were identified up to the
family level, except those belonging to Wild Boar Sus
scrofa, because of their easy
identification. We identified hair using
Teerink (1991) and Valente et al. (2015), teeth using
Dueñas et al. (1985), and feathers using Dove &
Koch (2011).
Diet composition
Hutchinson (1957) defined the niche as an
n-dimensional hypervolume where distribution of environmental variables and/or
factors would allow a certain species to exist indefinitely. This approach provides a quantitative
perspective of the niche concept and, therefore, established the conceptual
basis for the performance of studies in many different fields of ecology (Smith
1982). We defined the trophic niche as
the n-dimensional hypervolume, n being the number of prey types consumed
by the target species, constrained by used trophic resources that would allow
the species to exist indefinitely.
For diet description we grouped consumed prey
into four categories: birds, lagomorphs, small mammals and ungulates. We calculated the frequency of occurrence
(FO) for each category regarding total analysed scat
samples, and also the niche breadth using Levins
Index (Levins 1968):
B = 1/(∑ [pi2])
where pi is the proportion of
occurrence of the prey category i, regarding the
total consumed prey. To compare this
with other populations, we used the standardisation
suggested by Colwell & Futuyma (1971),
Bstand= (B-1)/ (n-1)
where n is the number of prey categories
consumed. This index shows the degree of
specialisation of a certain species; a value close to
0 is indicative of a specialist predator, while a generalist predator shows
values close to 1 (Colwell & Futuyma 1971).
Both FO and Bstand
calculated from analysed scat samples were
compared with prior knowledge of the trophic ecology of the Iberian Lynx. For that, we selected four relevant studies
as a comparative reference (Table 1), and regrouped their results to our four prey
types. This was not possible in regard
to the study by Fedriani et al. (1999) who used a
broad classification of prey items, e.g., other vertebrates, referring to all
non-lagomorph vertebrates. Therefore, we
calculated the FO of each prey category and Bstand
for all four reference studies, and compared results with those obtained in our
study area.
We compared the trophic niche of the Iberian
Lynx population in the province of Madrid (M) with that described in prior
studies (A). For the latter, we
calculated the average FO of each prey category in the reference studies. Then
we used the index formulated by Schoener (1970) for
calculating the niche overlap between both populations, M and A:
C = 1- ½ ∑|piM
– piA|
where piM
is the proportion of occurrence of the category i
within population M, and piA is the same
but within population A. C takes a
minimum value of 0 when there is no overlap, and a maximum of 1 when the
proportions of consumed resources are the same in both populations.
Lastly, we compared FO and Bstand obtained in the
province of Madrid between the two periods when samples were collected, i.e.,
spring–summer and autumn–winter. We used
Fisher’s exact test, which is suitable for small sampling sizes.
Results
Between January 2015 and May 2018, we
collected 98 scat samples along 21 transects that were each combed twice, once
in spring–summer from May to July and once in autumn–winter from October to
February. Through genetic analysis we
identified 46 of these samples positively as belonging to Iberian Lynx, with 31
collected in the spring–summer season and 15 collected in the autumn–winter
season. As our genetic method allows
only for identifying scat of Iberian Lynx, we did not attempt to identify the
remaining 52 scat samples to other species.
The content analysis of the 46 scat samples
revealed an overall niche breadth Bstand
of 0.36, with small mammals constituting the majority of prey categories. Fisher’s exact test shows the existence of
marginally non-significant (p = 0.07) differences in diet composition between
both seasons of the year considered (Figure 2).
Details are provided in Table 2.
Discussion
The Bstand
(0.36) calculated for the population in our study area shows the
specialist character of the Iberian Lynx. However, this value is higher
than those obtained for comparative reference studies in Table 1. Furthermore, the obtained C value of 0.49
shows the trophic niche shift of this
population, with regard to that known so far. Figure 3 shows that the trophic niche of the
Iberian Lynxes within the study area is directed towards predation on small
mammals.
The Iberian Lynx is
regarded as a trophic specialist, strictly dependent of the European Rabbit
(Delibes 1980; Aymerich 1982; Beltrán
et al. 1985; Beltrán & Delibes 1991; Calzada & Palomares 1996; Palomares et al. 2001; Ferrer & Negro 2004; Gil-Sánchez
et al. 2006). There are such strong
links between these two species that the collapse of Rabbit populations can
even inhibit the reproductive capability of the Iberian Lynx which has been
interpreted as its ‘inability’ to switch its main prey (Ferreras
et al. 2011). In this research, we
compared niche breadth and overlap between a potential population in the
central Iberian peninsula and prior knowledge obtained from southern
populations. Our results show
differences in comparison with those obtained from the four studies used as a
comparative reference (Fig. 3).
Therefore, our study is the first record in which lagomorphs are not the
main prey, showing a 30% lower FO than in the lowest record so far (70%, Beltrán & Delibes 1991). On the contrary, the FO of small mammals is
clearly over-represented (47.5% higher) in comparison with prior studies.
A similar pattern than
the one observed here was already recorded in Delibes et al. (1975). In this study carried out in the provinces of
Cáceres and Salamanca (closer to our study area than
to southern populations), the recorded FO for Rabbits was 56.5% while the small
mammals and birds occur in the 27% and 12% of samples, respectively. These results, although still different to
ours, show a pattern of Iberian Lynxes farther inland feeding on alternative
prey other than Rabbits more frequently.
Rabbit distribution
within our study area shows clear differences between main landscape
regions. The population in the north is
naturally fragmented, most likely because of the patchy distribution of
suitable habitat (Virgós et al. 2003). In the south, Rabbits are widespread (Blanco
& Villafuerte 1993) due to the existence of a
high density of boundaries between croplands and scrublands (Calvete et al. 2004) where they find a suitable combination
of trophic resources and shelter (Tapia et al. 2014). As far as we know there is no more actualized
information about new population trends, but the described spatial arrangement
coincides with our field observations throughout the sampling period.
The observed pattern in our study area could
be a response to: (i) Iberian Lynx adaptation that
shows a different trophic behaviour in different
environments. Note that 65% of the
Iberian Lynx scat samples analysed were collected in
the landscape region of the Guadarrama Mountains,
where Rabbit distribution is patchy.
This could lead to the exploration of different trophic niches in areas
where Rabbit abundance is lower. A similar
pattern was obtained by Sáez-Gómez et al. (2018) and Nájera et al. (2019), who recorded Iberian Lynxes preying
on Red-necked Nightjar Caprimulgus ruficollis eggs and Domestic Cats, respectively,
as a response to the decline of Rabbit abundance; (ii) an uncertain proportion
of our Iberian Lynx scat samples could come from juvenile individuals, whose
habitat requirements are less restrictive than those of resident individuals
(Gastón et al. 2016). Therefore, trophic
plasticity could be wider too, which would add some noise to our results; and
(iii) overestimations of the FO of small species might have been obtained
(Torres et al. 2015). These have more
hair and other indigestible matter per unit of body mass, which can cause their
occurrence in a higher number of scat samples per unit of consumed mass (Floyd
et al. 1978). Despite this, earlier
studies on the trophic ecology of the Iberian Lynx did not suggest evidence of
overrepresentation of small prey (Delibes 1980; Aymerich
1982; Beltrán et al. 1985; Beltrán
& Delibes 1991; Calzada & Palomares
1996; Palomares et al. 2001; Ferrer & Negro 2004;
Gil-Sánchez et al. 2006). Therefore
results are still comparable.
The observed seasonal variation in the diet
of the Iberian Lynx in our study area corroborates results of previous studies
on the species (Delibes 1977; Beltrán & Delibes
1991; Gil-Sánchez et al. 2006) as well as on the Eurasian Lynx (Krofel et al. 2011).
Lagomorph predation resulted in a 27% lower value during the
spring–summer period, while small mammals consumed showed a 10% increase in
comparison with the autumn–winter period.
Bird predation was only recorded in spring–summer (FO =
21%). Bstand
also shows differences between both seasons, being higher in spring–summer
(0.58) than in autumn–winter (0.41).
Therefore, during the cold season of the year, the Iberian Lynx consumes
a lower variety of trophic resources, whilst this pattern changes in the warm
season.
This could be motivated by two facts that are
likely to produce a synergic effect: (i) during
autumn–winter, when high precipitation and low temperature occur, the daily
activity of prey is reduced, being less available for Iberian Lynxes (Beltrán & Delibes 1994). On the other hand, during the spring–summer
season, climatic conditions are less adverse, which allows for an increase in
daily activity and, therefore, higher availability of different prey species;
(ii) the Rabbit reproduction period begins in October–November and can last
until June–July, depending on environmental conditions. This produces a maximum peak of abundance
just before summer. Then Rabbits become
the most abundant prey and, as a consequence, predators apply the highest
pressure to a single trophic resource.
Moreover, Rabbits do not reproduce during summer (Soriguer
& Palacios 1994). Therefore, a quick
and deep decrease of Rabbits occurs, forcing Iberian Lynxes to prey on
alternative trophic resources (Delibes 1980) for the rest of the summer.
Our results reinforce the key role that
lagomorphs play in the diet of the Iberian Lynx. This category is the most frequent prey when
diversity of available prey is lower.
Here, however, we provide evidence for a lower trophic dependence of the
Iberian Lynx on lagomorphs than in the areas of Doñana-Aljarafe
and Andújar-Cardeña.
In our study area, the Iberian Lynx shows its adaptive capacity,
adopting a relatively generalist strategy when trophic diversity is high, and a
more specialist strategy when diversity is low.
Despite this, the low number of samples collected in autumn–winter
season (n=15) must be taken into account and, therefore, the pattern showed
here may change with a larger dataset.
Knowledge of predator-prey relationships is
fundamental for the adequate design and implementation of species conservation
plans (Popp et al. 2018). Therefore, the
results of our research provides base line information for designing
conservation actions for the Iberian Lynx in central Spain. We show that the Iberian Lynx is capable to
adapt to a wider prey spectrum than previously assumed by Ferrer & Negro
(2004) and Ferreras et al. (2011). Based on the described pattern, we think that
Iberian Lynxes can profit from an increase in prey diversity provided in enrichment
programmes carried out at captive breeding centres (Rivas et al. 2016). Familiarising them
with a broader prey diversity may enhance the ability of reintroduced
individuals to colonise and survive in new
territories.
Future research efforts on the trophic
ecology of the Iberian Lynx should focus on increasing the number of scat
samples for analysis of diet composition, but also on prey availability and the
estimation of ‘real’ proportion each prey species contributes to the diet by
means of correction factors, as suggested by Wachter et al. (2012) and Klare et al. (2011).
This will provide more reliable information about the trophic needs of
the Iberian Lynx.
Table 1. Previous studies used as
comparative references, with authors, sample size (n), sample periods (years),
studied population and niche breadth (Bstand)
of respective populations.
Authors |
n |
Years |
Population |
Bstand |
Delibes 1980 |
1573 |
1973–1976 |
Doñana-Aljarafe |
0.060 |
Beltrán & Delibes 1991 |
209 |
1983–1984 |
Doñana-Aljarafe |
0.279 |
Palomares 2001 |
1171 |
1993–1996 |
Doñana-Aljarafe |
0.005 |
Gil-Sánchez et al. 2006 |
360 |
2001–2002 |
Andújar-Cardeña |
0.035 |
Table 2. Frequency of occurrence (FO)
of prey categories in scat samples of Iberian Lynx (n=46) collected in the
study area between January 2015 and May 2018.
Prey category |
FO in spring–summer |
FO in autumn–winter |
Total FO |
Small mammals |
50% |
40% |
54% |
Lagomorphs |
26.31% |
53.33% |
39% |
Birds |
21.05% |
0% |
17% |
Ungulates |
2.63% |
6.67% |
4% |
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