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Revista
Chilena
de
Historia
Natural
69:
113-123,
1996
Niche-complementarity
of
South American foxes:
reanalysis
and
test
of
a hypothesis
Complementariedad de nicho en zorros sudamericanos:
reamilisis y puesta a prueba de una hip6tesis
JAIME
E.
JIMENEZ1• 5, JOSE L.
YAfEZ2,
ELIER L.
TABIL0
3
and FABIAN
M.
JAKSIC4
1
Department
of
Wildlife Ecology and Conservation, University
of
Florida, Gainesville, Florida 32611, USA.
"secciyn
Zoologia, Museo Nacional de Historia Natural, Casilla 787, Santiago, Chile.
3Corporacion Nacional Forestal,
Vicuxa
Mackenna 93, Illapel. Chile .
.JDepartamento de Ecologia, Pontificia Universidad Catolica de Chile, Casilla I 14-D, Santiago, Chile
E-mail: fjaksic@genes.bio.puc.cl
5Present address: Department
of
Fisheries and Wildlife, Utah State University, Logan, Utah
84322-5210,
USA
ABSTRACT
The
niche-complementarity hypothesis states that for coexistence to occur. high overlap in one dimension
of
the niche must be
compensated by low overlap in another. Fuentes & Jaksic (1979) noted that two fox species (Pseudalopex cu/paeus and
P.
Jriseus)
along the western coast
of
South America displayed this phenomenon, compensating low habitat overlap (allopatry)
with high dietary overlap, and high habitat overlap (sympatry) with low dietary overlap and character displacement in body
size. Fuentes & Jaksic offered scant quantitative evidence for their proposed hypothesis
of
fox coexistence patterns, and the
habitat scale used was rather coarse: lowlands versus highlands (Andean Ranges). With the benefit
of
hindsight and a much
better database that included one site (Auco) where the two foxes are sympatric when they should not be according to the
Fuentes & Jaksic hypothesis, we reanalyze the sources used by these authors as well as reports accumulated
over
the
subsequent years. We also report an in-depth study
of
resource partitioning (food, habitat, and activity time) and coexistence
of
sympatric foxes at
Aucy.
At this site, the two foxes coexist by partitioning habitat at a fine-scale, maintaining interspersed
non-overlapping species-specific home ranges in the patchy environment. Through interference, the larger
P.
culpaeus
excludes the
smaller
P.
griseus from high-quality (abundant prey) habitat patches. Though sympatric they are not syntopic: the
two foxes overlap little at the habitat-type scale, have intermediate food overlap and complete overlap in activity time, thus
supporting the niche-complementarity hypothesis but at a finer scale.
In
conclusion, the Fuentes & Jaksic hypothesis is still
valid. but requires consideration
of
two factors previously ignored: the spatial scale at which coexistence occurs, and the
availability
of
high-quality (large) prey.
Key
words:
Niche-complementarity hypothesis, Pseudalopex spp., spatial scale, resource partitioning, Chile.
RESUMEN
La
hip6tesis de complementaricdad de nicho establece que
para
que ocurra coexistencia, alta sobreposicion
en
una dimension
de be ser
compensada
por baja sobreposicion en otra. Fuentes & Jaksic ( 1979) notaron que dos especies de zorros (Pseuda/opex
culpaeus y
P.
griseus) distribuidas a lo largo de la costa occidental de
Sudamprica
exhibian este fenomeno, compensando baja
sobreposici6n de habitat (alopatria) con alta sobreposici6n en dieta y alta sobreposici6n espacial (simpatrfa) con baja
sobreposicion dietaria y desplazamiento del caracter en tamaiio corporal. Fuentes & Jaksic ofrecieron escasa evidencia cuanti-
tativa para su modelo de coexistencia de zorros y la
escalade
habitat con que trabajaron era bastante gruesa: llanuras costeras
y del Valle Central versus montaiias (Cordillera de Ios Andes). Con beneficia de
la
retrospectiva y de una
mejor
base de datos
que incluye
un
sitio (Auc6)
en
que Ios dos zorros son simpatridos cuando ello no debiera ocurrir de acuerdo a la hipotesis de
Fuentes & Jaksic, nosotros reanalizamos !as fuentes usadas por dichos autores
asi
como datos que se han acumulado
en
aiios
recientes. Tambien documentamos un estudio
en
profundidad de la particion de recursos (alimento, habitat y tiempo de
actividad) y de
la
coexistencia de zorros
simpitridos
en
Aucy.
En este sitio, !as dos especies coexisten a traves de repartirse
el
habitat a una
escala
fina, manteniendo ambitos de hogar inter-dispersos, no sobrepuestos, y especie-especfficos
en
un ambiente
naturalmcnte heterogeneo. Mediante interferencia, el zorro
PiV
grande
(P.
culpaeus) excluye al
PiV
pequeiio (P. griseus) de
Ios
parches de habitat de mayor calidad (con abundantes presas). Aunque son simpatridos, estos zorros no son sint6picos:
!as dos especies se sobreponen poco
en
la escala del tipo de
hibitat,
tienen sobreposici6n dietaria intermedia, y sobreposicion
completa en tiempo de actividad, corroborando asi la hipotesis de complementariedad de nicho a una escala
mis
fina.
En
conclusion.
la
hipotesis de Fuentes & Jaksic
a~n
es valida, pero requiere consideracion de dos factores previamente ignorados:
la
escala
espacial en que ocurre la coexistencia y la disponibilidad de presas de alta calidad (grandes).
Palabras
clave: Hipotesis de complementariedad de nicho, Pseudalopex spp., escala espacial, particion de recursos, Chile.
(Received 7 December 1994; accepted
11
January 1996; managed by Javier
A.
Simonetti)
114 JIMENEZ ET AL.
INTRODUCTION
Culpeos (Pseudalopex culpaeus) and chillas
(P. griseus) are among the most widespread
South American foxes (Ginsberg & Mac-
Donald 1990, Sheldon 1992). However, their
distributions do not completely overlap, thus
creating different biogeographical contexts
of
sympatry and allopatry
of
their popula-
tions. In the northern part
of
the culpeo' s
range (Ecuador and Peru), chillas are absent.
The opposite happens in southeastern Argen-
tina, where chillas are abundant and culpeos
are not found. Across Chile and western Ar-
gentina, the two species are allopatric in the
north (Mares et al. 1989) and sympatric in
the south (Osgood 1943,
Medel
& Jaksic
1988). Throughout their ranges, these foxes
face varying landscapes and environmental
conditions (habitat types, temperature and
precipitation
regimes,
etc.),
as
well
as
varying biotic networks (different arrays
of
prey types, sizes, and abundances).
Based on the distribution patterns
of
chi-
llas and culpeos between 33° and 53° S in
Chile, Fuentes & Jaksic (1979) hypothesized
that
niche-complementarity
of
diet
and
habitat
accounted
for
their
distributions
and body sizes.
The
niche-complementarity
hypothesis states that in order for two species
with high habitat overlap to coexist, they
must differ in diet, and vice-versa (Schoener
1974). Fuentes & Jaksic (1979) examined
body-length data
of
chillas and culpeos, and
body
length
of
prey
over
20
degrees
of
latitude in Chile. They found that chillas and
culpeos were similar in size in central Chile,
where they were reported to be allopatric.
In
southernmost
Chile,
these
foxes
were
sympatric
and
differed
in
body
size (the
culpeo always being larger). According to
Fuentes & Jaksic (1979), where the foxes did
not overlap in space, body sizes were similar
supposedly because
of
relaxed competition
for prey
of
similar sizes.
Further,
Fuentes
&
Jaksic
(1979) sug-
gested
that
because
of
the profile
of
the
Andean Ranges (which in Chile decrease in
altitude toward the south), habitat partition-
ing by altitudinal segregation would only
be possible in the central part
of
the country.
Here, chillas would use lowlands and culpeos
use the mountains. In the south, both foxes
would
use
the
lowlands.
These
authors
interpreted
the
foxes'
size
differences
in
terms
of
character divergence related to use
of
differently-sized prey when in sympatry
(e.g.,
Rosenzweig
1966,
Gittleman
1985,
Vezina 1985).
Several
subsequent
studies
conducted
throughout Chile support Fuentes & J aksic' s
hypothesis. In a
north-south
sequence
in
Chile, where the culpeo is present the chilla
is absent: in parts
of
Tarapaci.,
I Region
(Marquet
et
al. 1992); at Parque Nacional
Fray Jorge, IV Region (Meserve et al. 1987,
Jaksic et al. 1993); at Fundo San Carlos de
Apoquindo, Metropolitan Region (Jaksic
et
al. 1980, Simonetti 1986, Iriarte
et
al. 1989);
and at Fundo El Pangue, V Region (Eben-
sperger et al. 1991, Bustamante et al. 1992).
The reverse is true for the culpeo where the
chilla
is present: in
parts
of
Tarapaca,
I
Region (Marquet et al. 1992); at Chafiaral,
Ill
Region (Simonetti et al. 1984); at Fundo
Santa Laura, V Region (Jaksic et al. 1980); at
Parque
Nacional
Nahuelbuta,
IX
Region
(Medel
et al. 1990);
at
Parque
Nacional
Puyehue, X Region (Rau et al. 1995); and at
Bosque Experimental San Martfn, X Region
(Martfnez et al. 1993). In southernmost Chi-
le, Johnson (1992) found chillas and culpeos
in sympatry at Parque Nacional Torres del
Paine
(XII
Region),
as
predicted
by
the
hypothesis.
Dietary analyses
of
chillas and culpeos
support
the
niche-complementarity
hypo-
thesis. Although with a small sample size,
Fuentes & J aksic (1979) found that allopatric
central
Chilean
foxes
showed
high
diet
similarity and that southern Chilean chillas
ate prey
of
smaller sizes than northern ones
(they did not have data on southern culpeo
diets).
Later,
Jaksic
et
al.
(1980,
1983)
provided
a much
larger
sample
size that
corroborated the initial findings.
However, contrary to expectations
of
the
Fuentes & Jaksic hypothesis,
De
La
Maza
(
1981)
reported
chill
as
and
culpeos
in
sympatry in a north-central Chilean site: in
the
Reserva
Nacional Las
Chinchillas,
at
Auc6, IV Region. The sympatry
of
chillas
and
culpeos
at
Auc6
was
subsequently
confirmed by Duran et al. (1987) and Jaksic
et al. (1992). How do these two foxes coexist
at Auc6? This site, which lies roughly
1.5
NICHE-COMPLEMENTARITY
OF
SOUTH AMERICAN FOXES 115
degrees
to the
north
of
the
northernmost
populations
analyzed
by Fuentes & Jaksic
(
1979),
seems
ideal
for
examining
their
proposed hypothesis in greater detail.
We
will
show
that
although
niche-
complementarity
and
resource
partitioning
indeed
occur
between
foxes at Auc6, they
are substantiated at a much smaller spatial
scale than the one originally proposed.
We
will not focus on the character displacement
expressed as
change
in body size
of
chillas
and
culpeos
along their ranges, because we
have
already
reported
on
that
elsewhere
(Jimenez
et
al. 1995).
The
new
data
here
reported
enable
us
to
revise
the
original
hypothesis
of
Fuentes & Jaksic (1979), and
thus explain
"anomalous"
situations
of
fox
sympatry.
MATERIAL AND METHODS
Literature review
We
reviewed
and
analyzed
the
published
information on chillas and culpeos
under
the
light
of
Fuentes &
Jaksic's
(1979) approach.
This
time,
we
paid
special
attention
to
exactly where the information was collected
and its implications for the spatial distribu-
tion
of
foxes.
Field study
The
Reserva
Nacional
Las
Chinchillas
at Auc6
(31
°30' S,
71
°06' W), IV Region, is
a
4,570-ha
(corrected by slope) fenced area
about
300
km
north
of
Santiago. It has a
mediterranean-arid
climate
with rain con-
centrated during the cold winter. Interannual
rain variability is high with a mean
of
about
175
mm.
The
rugged
topography
(400
-
1,700 m elevation) determines a landscape
dominated
by ridges,
interspersed
ravines
and slopes, with scarce flatlands in the lower
areas.
The
vegetation is dominated by thorn
scrub, with species composition varying with
slope exposure.
On
the drier, north-facing
slopes, cacti and bromeliads constitute the
dominant
vegetation. South-facing slopes are
more
mesic, with
more
evergreen shrubs and
the ground covered by abundant grasses.
The
remainder
of
the
area
is physiognomically
intermediate between north- and south-facing
slopes. A more detailed description
of
the
site is found in Jimenez (1993).
In order to test the niche-complementarity
hypothesis, we
evaluated
the
evidence
for
resource-partitioning
by
foxes
at
Auc6
during the entire year
of
1992.
We
evaluated
the resources
used
by chillas and
culpeos
along what have been considered the three
most
important
niche
dimensions
for
vertebrates: food, habitat, and activity
time
(Schoener 1974).
Food
We
studied
fox
diets
by
examining
the
contents
of
feces.
Because
the
bile
acid
technique
failed to
distinguished
between
feces
of
the two foxes (Jimenez
et
al., ms.
accepted),
we
used
two
other
criteria
combined: (1)
The
diameter
of
the scat had
to be within the 95% confidence interval
of
the feces
of
known foxes (Jimenez 1993); (2)
the feces had to be collected within a
known
fox territory (see below).
About
one
third
(31.4%)
of
the
seats
did
not
meet
both
criteria simultaneously and
were
therefore
discarded
from
the
analyses.
Feces
were
collected every
other
week
throughout the
area, especially along established transects
(see below).
For
comparative purposes, we
computed
three
food-niche
metrics:
(a)
Geometric mean weight
of
prey; (b)
Levins'
food-niche breadth
or
diet diversity index;
(c) Pianka' s symmetrical food-niche overlap
or
diet similarity index (see Jaksic
et
al. 1983
for computations
of
these indices).
Habitat
We
studied
the
spatial
dimension
of
the
niche using three different methods:
(1)
Scent stations (Linhart & Knowlton
1975), lured with fox
No
1 urine
(Crank's
Outdoor Supplies, Wiscasset, Maine), were
run once a month during a 24-h period. Six
scent stations, set
400
m apart, were distri-
buted along a
2,000-m
transect.
Transects
were established in: (a) flatlands, (b) ravines,
(c) north-facing, and (d) south-facing slopes,
which were the most extensive habitat types
recognized.
We
replicated each habitat type
116 JIMENEZ ET AL.
four times
in
each
of
four sectors within the
Reserve.
We
checked
transects
during
mornings and measured tracks with a 1-mm
precision calipers. Tracks were assigned to
either chilla
or
culpeo by comparing them to
those from radio-tracked foxes (see Jimenez
1993 for details).
We
computed an index
of
visitation rate for each transect and species.
(2) Foxes were captured along transects
in flatlands and ravines after checking the
scent stations (Andelt et al. 1983).
We
used
13
Victor 1.5 padded leg-hold traps baited
with
canned
fish, set apart every 300 m.
Traps were checked every 12 h and trapped
every month for 2-10 days in a row.
We
tranquilized captured foxes with ketamine
(Ramsden et al. 1976), and they were sexed,
aged,
measured,
weighed,
and
released
within two hours.
(3)
Four
chillas and five culpeos were
fitted with radiocollars. Two individuals
of
each species were fit with motion-sensitive
transmitters.
We
estimated fox locations by
triangulation
from
several
places
scatter-
ed within the Reserve, as well as by direct
sightings. Fixes were obtained for varying
periods at random times.
We
drew locations
on maps and assigned them to one
of
the four
habitat
types
already
described,
but
in
addition we considered east- and west-facing
slopes. The 50-m contour lines for the Reser-
ve as well as for the fox radio-locations were
digitized in a
PC
geographical information
system
(GIS)
in
ARC/INFO
format.
We
computed
habitat
availability
as the pro-
portion
of
the total area covered by each
habitat type (see Jimenez 1993 for details).
Activity time
We
estimated the activity status
of
foxes as
the percent
of
the radio fixes that indicated
movement within 3-hour periods.
We
also
estimated activity by comparing the number
of
foxes caught in traps at night versus those
caught during daylight.
RESULTS
Literature review
Qualitative reports typically describe culpeos
as inhabitants
of
rugged, arid or semiarid
mountain ranges,
either
open or forested,
usually associated with the Andean Ranges
up to 4,500 m elevation (Alien 1905, Osgood
1943, Mann 1945, Housse 1953, Crespo &
De
Carlo
1963,
Greer
1965).
Chillas
are
described as occurring in lowland and coastal
habitats, grass lands with rolling topography,
and other relatively flat habitats with short,
open vegetation (Housse 1953, Greer 1965).
However, some authors indicate that both
foxes sometimes occupy
open
habitats in
plains and low mountains
(Osgood
1943,
Housse
1953,
Novaro
1991,
Redford
&
Eisenberg 1992). Although culpeos in high-
lands and chillas in lowlands appears to be
the most recurrent pattern, there are several
geographical areas where their sympatry
or
allopatry is
not
clear,
and
these
warrant
further
analysis.
These
cases
have
been
overlooked, ignored,
or
not given sufficient
importance. Here, we will focus mainly on
those places where Fuentes & J aksic ( 1979)
as
well
as
Jaksic et al. (1980, 1983) studied
the foxes' diet quantitatively (i.e., central and
southernmost Chile).
Fuentes &
Jaksic'
s
hypothesis
predicts
that in central Chile, chilla and culpeo should
be allopatric.
This
prediction
was
corro-
borated by Jaksic et al. (1980) when studying
foxes in Fundo Santa Laura
(a
coastal hilly
area in the V Region) and in four neigh-
boring sites in the Andean foothills near San-
tiago (Metropolitan Region).
The
first site,
where only chillas were seen, is only 68
km
across the Central Valley from the closest
of
the four
pre-Andean
sites,
where
only
culpeos
were
observed.
More
recently,
Ebensperger et al. (1991) studied the diet
of
culpeos at
Fundo
El
Pangue
(V Region),
which lies approximately 18 km west
of
Fun-
do Santa Laura. Apparently, these two fox
populations
are
parapatric
(i.e.,
have
adjoining
geographic
distributions)
rather
than allopatric (i.e., separated by a broad
hiatus). Indeed, there are historical records
of
parapatric distribution
of
these two foxes in
central Chile. Osgood (1943: 64) observed
" ... it [culpeo] appears to be fairly common
in the coast hills near Valparaiso ... " and "
..
.
chilla is very abundant in central Chile
..
.
even persists within the city
of
Santiago as
I
discovered
by
seeing
several
. . . in the
parklike
surroundings
of
the
Cerro
San
NICHE-COMPLEMENT ARITY
OF
SOUTH AMERICAN FOXES 117
Cristobal
... " (1943: 69-70).
Osgood
(1943:
64, 70) stated
that
he
also
examined
chillas
and
culpeos
from
Papudo
and
Limache
(V
Region).
Thus,
both
recent
and
past
information
on
fox
distribution
in
central
Chile
indicates that chillas
and
culpeos
are
sympatric
(see below).
On
the
other
hand,
Fuentes
& 1
aksic
( 1979:
45)
predicted
that
in
southernmost
Chile
foxes
should
be
sympatric. However,
they
studied
chillas from
Onaistn
(on
Tierra
del
Fuego
Island,
XII
Region),
where
they
were
introduced
in 1951 (Jaksic & y
ixez
1983: 370).
Further,
these chillas introduced
in
the
flat
northern
part
of
Tierra
del
Fuego
were
considered
as
sympatric
with
native
culpeos
that
occur
only in
the
forested and
more
rugged
southern
part
of
the
island
(Jaksic et al. 1983).
The
closest
record
of
a
culpeo
was
at
least
70
km
away
(see
Fuentes
& 1aksic 1979). Atalah et al. (1980) studied
insular
chillas
(only
3/69
came
from
potential
culpeo
ranges)
without
reporting
the
presence
of
culpeos
at
any
of
their study
sites. In fact, in three different trips to
Tierra
del
Fuego
1E1
saw
chillas
but
no
culpeos
on
the
northern
half
of
the island.
Across
from
Tierra
del
Fuego,
on
mainland
Magallanes,
1 aksic
et
al. (1983) did
not
mention
the
presence
of
chillas at
Parque
Nacional
Torres
del Paine.
Further,
1aksic
et al. (1983:
693)
reported only chillas from
Monte
Aymond,
253
km
northeast
of
Par-
que
Nacional
Torres
del Paine.
Durin
et
al.
( 1985)
surveyed
foxes
on
six different areas
on
flatlands
and
rolling hills
along
a
767-km
transect
between
Torres
del
Paine
and
Punta
Arenas
(XII
Region)
and
saw
nothing
but
chillas.
They
stated that
culpeo
" ... inhabits
the
forest
area
and
more
closed
vegetation
sites
throughout
the
region ... these species
are allopatric ... " (1985: 142)
and
that " ...
grey
fox
habitat
was
characterized
by
the
'coir6n'
steppe
chaparral
... " (1985: 146).
Alien (1905: 161) had already implied that
most
fox
populations
in
Patagonia
were
allopatric
or
parapatric, stating that " ... In my
experience
the
range
of
the
grey
fox [his
Cerdocyon griseus]
seems
to
cease
at
the
foothills
of
the
Cordillera,
where
the
Magellan
wolf
(Canis
magellanicus)
[ culpeo] is to
be
found
... " However, John son
(1992)
conducted
an
intensive study
of
foxes
at
Parque
Nacional
Torres
del
Paine
and
found
that
chillas
and
culpeos
were
in
sympatry, as predicted by
Fuentes
&
Jaksic
(1979).
It
is
unlikely
that
the
presence
of
chillas
at
this
site
was
due
solely
to
the
expansion
of
their
ranges
during
the
last
decade
(Abello 1979 in
1ohnson
1992)
and
perhaps
their
presence
was
overlooked
during the
earlier
studies.
Therefore,
the
biogeography
of
foxes
in
the
XII
Region
is
more
complex
than
originally
thought.
It
appears
that
chillas
and
culpeos
are
not
sympatric,
but
rather
allopatric in
southernmost
Chile.
Thus
far,
the only truly sympatric chillas
and
culpeos
have been found in
Parque
Nacional
Torres
del Paine. All the
other
records indicate that
chillas
use
flatlands
(even
in
areas
where
they
were
introduced)
and
culpeos
use
rugged and forested landscape.
In summary, chillas
and
culpeos
in cen-
tral
Chile
are not strictly allopatric,
but
rather
parapatric
or
even
sympatric
(see
below),
whereas
in
southernmost
Chile
they
are
mostly allopatric
except
for
Parque
Nacional
Torres del Paine.
Food
The
feces
of
chilla
and
culpeo
that
we
analyzed
contained
vertebrates,
inverte-
brates,
and
fruits
throughout
the
year.
Although the ordinal
ranking
of
prey
classes
is
similar
between
fox
species,
their
pro-
portional
occurrences
are
different.
By
number,
culpeos
consume
about
twice
as
many
mammals,
birds,
and
reptiles
than
do
chillas
(Table
1).
Chillas
eat
more
insects
and
fruits than culpeos.
On a
biomass
basis,
the
differences
be-
tween
chillas
and
culpeos
become
less
obvious and proportions
of
vertebrates
more
even
(indeed,
there
were
no
significant
differences
between
the
two
fox
species,
Table
1
).
The
only significant difference is
for insects,
which
contributed
seven
times
more
biomass
to
chilla
than to
culpeo
diets
(Table 1
).
By
far,
most
of
the
biomass
in
the
two
foxes'
diets
was
made
up
of
mammals
(>
80%,
Jimenez
1993).
On
average,
chillas
consume
more
than
twice
the
small
mammal
(rodents
and
marsupials)
biomass
taken by
culpeos (38.9 vs. 16.9%).
Conversely,
chillas
118
JJMENEZ ET AL.
TABLE I
Percent representation
of
prey by numbers
and by biomass
in
the diet
of
chill as (
131
feces)
and culpeos (285) at Auc6, north-central Chile.
Values are means
of
four calendar seasons.
Kruskal-Wallis tests with Chi-square
approximation were used to compare
biomass figures between foxes
Representaci6n porcentual por numero
y biornasa de presas en las dietas de chillas (131 fecas) y
culpeos (285) en Auc6, centro-norte de Chile. Los valores
son medias de cuatro estaciones calendario. Pruebas de
Kruskal-Wallis con aproximaci6n de Chi-cuadrado se usaron
para comparar Ios valores de biomasa entre Ios zorros
Prey
%Number
% Biomass 1 x2
Chilla Culpeo Chilla Culpeo
Mammals 14.4 37.6 80.7 92.2
Birds 2.2 5.4 5.8 3.2
Reptiles
2.1
4.9 6.8 3.6
lnsects2 81.4 52.1 4.1 0.6
Fruits
21.9_1
5.93 2.6 0.4
See Jirnenez ( 1993) for computations
Includes a few arachnids
3.00
3.00
0.76
5.33
2.19
p
0.083
0.083
0.384
0.021
0.139
These values correspond to percentage
of
occurrence
among feces.
consume lower biomass
of
lagomorphs than
do culpeos (41.8 vs. 68.0%, Jimenez 1993).
The yearly average
of
the geometric mean
weight
of
culpeo
prey
was
almost
four
times that
of
chillas (Table 2). This certainly
resulted from the
higher
consumption
of
insects by chillas, given that there was no
significant difference
in
the geometric mean
weight
of
vertebrate prey taken by the two
foxes (Table 2). Food-niche breadth was
almost
twice
as high in culpeos than in
chillas, but when standardized
by
the number
of
taxa taken
(Bsta),
the two foxes did not
differ significantly in this regard (Table 2).
Diet similarity ranged from 0.431 to 0.865
throughout the year (Jimenez 1993).
Habitat
Both fox species combined had four times
more visits to scent stations on flatlands
(20.6% stations visited) and ravines (20.1%)
than on north- or south-facing slopes (both
with 4.7% stations visited; F = 7.68; d.f. = 3,
105; P = 0.0001
).
Visitation rates showed
strong
interaction
between
species
and
habitat (F = 4.00; d.f. = 3, 105; P = 0.0094),
which indicates differential use
of
habitat
types by chillas and culpeos. On average,
over the four
calendar
seasons, the rank
order
of
culpeo visitation rates to habitat
types was: ravines > flatlands > north-facing
slopes = south-facing slopes. For chillas the
sequence was: flatlands > ravines > north-
facing slopes = south-facing slopes.
Fox trapping results were similar. More
chillas
than
culpeos
were
captured
in
flatlands (G = 12.20, d.f. =
1,
P < 0.001). The
opposite was true for ravines (G = 4.86, d.f.
=
1,
p < 0.05).
Radiotelemetry also indicates that chillas
and cu1peos differed in their habitat use (G =
117.65, d.f. =
5,
P < 0.0001). Based on the
use and availability
of
different habitat types
(using Z Bonferroni confidence intervals
and a = 0.05), the four radio-tracked culpeos
appeared to prefer ravines and to avoid both
south- and west-facing slopes. The remaining
three habitat types (north- and east-facing
slopes and flat areas) were used according to
their respective availability. The five radio-
tracked chillas also showed clear differences
in habitat use. Overall, they appeared to
prefer flat areas and to avoid north- and
south-facing slopes. The remaining three
habitat types were used by chillas in pro-
portion to their respective availability.
The three methods used to estimate habitat
use lead to the conclusion that chillas use flat
areas more than culpeos and that the latter
use ravines more than the former.
TABLE 2
Comparison
of
food-niche metrics between
chillas and culpeos at Auc6, north central Chile.
Values are means
of
four calendar seasons.
Kruskal-Wallis tests with Chi-square
approximation were used to compare
metrics between foxes
Comparaci6n de estadfgrafos de nicho alimentario
entre chillas y culpeos en Auc6, centro-norte de Chile. Los
valores son medias de cuatro estaciones calendario. Pruebas
de Kruskal-Wallis con aproximaci6n de Chi-cuadrado se
usaron para comparar Ios estadfgrafos entre Ios zorros
Food-niche metrics Chi !la Culpeo
x2
p
Geometric mean weight 2.2 8.4 5.33 0.021
of
total prey (g)
Geometric mean weight 71.2 71.9 0.00 0.999
of
vertebrate prey (g)
Food-niche breadth 4.8 8.4 5.33 0.021
(44 prey categories)
Standardized food-niche breadth 0.2 0.3 3.00 0.083
NICHE-COMPLEMENTARITY
OF
SOUTH AMERICAN FOXES 119
Activity time
Sufficient radio-tracking data were obtained
from two individuals
of
each species. One
culpeo (G = 9.6, d.f. =
1,
P < 0.005) and one
chilla (G = 13.6, d.f. =
1,
P < 0.001) were
more active during the afternoon and nightly
periods. The other chilla (G = 0.061, d.f. =
1,
P > 0.50) and the other culpeo (G = 0.067,
d.f. =
1,
P > 0.50) were active throughout
day and night.
The
frequency distribution
of
active
radio
locations
for the two chillas
was not different from those
of
three culpeos
(Smirnov large sample two-tailed test, x2 =
0.6697, four time periods, m = 59, n = 78,
P >
0.1
0), thus indicating that chillas and
culpeos overall do not differ in their activity
time. Activity as assessed by fox trappings
shows that chillas were more active during
the night than during daylight (G = 11.25,
d.
f.
=
1,
P < 0.001). Although more culpeos
were captured at night, the difference with
daylight captures was not significant (G =
2.61' d.f. = 1' p >
0.1
0).
DISCUSSION
The niche complementarity hypothesis
of
coexistence
Fuentes & Jaksic ( 1979) hypothesized that
the biogeographical pattern
of
chillas and
culpeos south
of
33° in Chile is the conse-
quence
of
partitioning
prey
resources
to
lessen
interspecific
competition.
This
in
turn results in body size differences, i.e.,
character displacement
of
sympatric foxes.
When
habitat can be partitioned, the hypo-
thesis predicts that foxes become allopatric
by habitat segregation and converge to sim-
ilar body sizes. In this allopatric situation,
competition
for
food
relaxes
and
diet
similarity
between
the
species
increases.
When
habitat
cannot
be
partitioned,
the
foxes
diverge
in
body
size and
hence
in
prey
size
consumed,
thus
resulting
in
decreased
diet
similarity.
This
hypothesis
is
supported
by
most
studies
of
chillas
and culpeos (e.g., Jaksic et al. 1980, 1983,
Johnson 1992) and has been considered
as
a
neat
example
of
character
displacement
(Wayne et al. 1989).
Unfortunately
there
are
not
too
many
instances wherein diet similarity has been
calculated for allopatric versus
sympatric
foxes. Jaksic et al. (1983) calculated that
food-niche overlap between allopatric chillas
and culpeos was 90% in central Chile (Me-
tropolitan Region) and 63% in southernmost
Chile (XII Region). Jimenez (1993) reported
that yearly diet overlap between sympatric
chillas and culpeos was 64% in Auc6 (IV
Region), and Johnson (1992, and Johnson &
Franklin 1994) that it was only 14% in Par-
que Nacional Torres del Paine (XII Region).
Therefore, the prediction that foxes should
have higher diet similarity in allopatry than
in sympatry is sustained (90 vs. 64% in cen-
tral Chile, 63 vs. 14% in southernmost Chile,
respectively).
In
Fuentes
&
Jaksic's
hypothesis,
the
expected partitioning
of
habitat between chi-
llas and culpeos was by altitude, the former
in the lowlands, the latter in the highlands.
However, elevation per se seems not be the
adequate spatial dimension to be partitioned
by foxes. In fact, Fuentes & J aksic (1979)
reported on culpeo feces collected at a site in
central Chile at an elevation similar to a
collection site for chilla feces (784 m at Los
Dominicos
=
Fundo
San
Carlos
de Apo-
quindo, and 600 m at Tiltil = Fundo Santa
Laura). Parenthetically, Jaksic et al. (1980:
255)
report
that
the
same
samples
were
collected
at
950
and 1,000 m
elevation,
respectively. Culpeos from Fundo El Pangue
(Ebensperger et al. 1991) may even be at
lower
elevation
than
chillas
from
Fundo
Santa
Laura.
Something
similar has
been
documented
in
southern
Chile,
wherein
culpeos from Collipulli and Angol and chi-
llas from Nahuelbuta are found at roughly
the same elevation (Greer 1965: 136, Medel
et al. 1990). There, at the IX Region, the ac-
tual distribution
of
foxes seems the opposite
of
that
predicted:
culpeos
are
frequently
found in the Central Valley lowlands and
chillas
in
both the Andes and Nahuelbuta
ranges (JE Jimenez saw only chillas in the
Andes at Conguillfo, 1 ,600 m elevation, and
WE
Johnson, pers. comm., captured chillas
in Conguillfo at
1,
100 m elevation and in
Nahuelbuta at about 1,000 m elevation). It
does
appear
that the two foxes
have
in-
terspersed altitudina1 ranges in the IX Region
120 JIMENEZ ET AL.
( culpeos have been collected
in
Curacautfn,
Cunco, Collipulli, Angol, and Nacimiento,
and chillas
in
Curacautfn, Los Sauces, An-
go!,
Mulchpn,
and
Cabrero;
see
Osgood
1943, Greer 1965, B Guiiiez, pers. comm.).
Further, L Pincheira (pers. comm.) observed
an event
of
predation
of
culpeo upon chilla
on
the
outskirts
of
Nahuelbuta
Range.
Therefore, elevation
is
too coarse and indirect
a measure
of
habitat segregation for foxes.
Below we discuss what may be a more wide-
spread mode
of
habitat partitioning between
chiOOas
and culpeos.
Resource partitioning
The Fuentes & Jaksic hypothesis predicts
that at the latitude
of
Auc6, chillas should
be found
in
lowlands and culpeos in the
mountains (i.e., they should be allopatric), be
of
similar size and have high diet similarities.
We found (Jimenez et al. 1995) that foxes
at Auc6 are sympatric, differ somewhat
in
total body length (culpeo:
chiOOa
= 1.22, the
same ratio as at Parque Nacional Torres
del Paine), differ markedly in body mass
(culpeo: chilla = 1.73), and have intermediate
diet overlap (mean = 0.643, range = 0.43 I -
0.865).
Foxes
at
Auc6
are
sympatric
but
not
syntopic. Although chillas and culpeos do
not partition habitat altitudinally, despite
the rugged topography and different eleva-
tions available at the site, they do segregate
spatially by selecting different habitat types.
Chillas
were
consistently
found
in flat
areas whereas culpeos primarily occupied
ravines. Therefore their fine-scale habitat
overlap was low. This pattern
is
unlikely
to be a methodological artifact, because three
different
methods
gave the same result.
Habitat use appears to be a dynamic process
as revealed by radio-telemetry. At Auc6, as
well as
in
Parque Nacional Torres del Paine,
chillas and culpeos maintain interspersed and
almost
non-overlapping
species-specific
home ranges throughout the year (Johnson
1992, Jimenez 1993). In Auc6, we detected
twice as many agonistic incidents at in-
terspecific home-range boundaries than at
intraspecific ones. When a culpeo moved
into a chilla home range, the
chilla
retreated
to the farthest extreme
of
its home range.
When the culpeo left the area, the chilla mo-
ved back again.
These observations concur with Johnson's
(1992) findings
in
Parque Nacional Torres
del Paine, and support his hypothesis that
interference between chillas and culpeos may
be the mechanism by which they partition
habitat. Predation, an extreme form
of
in-
terference, may also be involved.
Durán
et
al. (1987) reported 5.6%
of
fox vertebrate
prey at Auc6 was made up
of
unidentified
carnivores
(see also L
Pincheira's
pers.
comm. above). The ultimate factor for this
pattern
of
habitat partitioning may be related
to energy requirements (Johnson et al., ms.
submitted).
The
larger
culpeo
seems
to
exclude chilla from better-quality habitats
(i.e., ravines), which on average had almost
seven times more small mammals than flat
areas
in
Auc6 (Jimenez 1993). As a result
of
the culpeo's dominance, chillas occupy
the less-productive and more risk-exposed
flat areas where most human activities are
concentrated.
Following
J
ohnson
et
al.'s
arguments (ms. submitted), unlike chillas,
culpeos would be unable to meet their energy
demands
in
low-quality habitats such as flat
areas
in
Auc6. Nonetheless, the partitioning
of
habitat found at Auc6, reveals that foxes
do not select their activity ranges based
solely on food abundance, because south-
and north-facing slopes have more small
mammals than ravines or flat areas (Jimenez
1993). But prey abundance
is
not the same as
prey availability. Perhaps foxes hunt less
efficiently
in
the steep slopes
of
Auc6 and
thus avoid those habitats and prefer more
level terrain.
The pattern
of
habitat partitioning at a
finer-scale and the interspersion
of
home
ranges displayed by foxes at Auc6, also
found by Johnson (1992) in Parque Nacional
Torres del Paine, may be more common than
previously thought. Apart from the Chilean
studies cited above, there is a report
of
sympatric chillas and culpeos
in
Neuquen,
Argentina (Novaro 1991).
Foxes at
Auc6
also partition prey re-
sources. Mean diet overlap for chillas and
culpeos was relatively low (64.3%), although
not as low to that reported for sympatric
foxes at Parque Nacional Torres del Paine
(14.0%, J ohnson 1992, J ohnson & Franklin
NICHE-COMPLEMENT ARITY
OF
SOUTH AMERICAN FOXES
121
1994). Culpeos at Auc6 have a broader diet
than chillas, although the reverse was found
in Parque Nacional Torres del Paine, at least
for vertebrate prey. These differences are
difficult to explain in light
of
the information
available.
The
fact that southern foxes have a
three-fold higher mean weight
of
vertebrate
prey (2, 170 -2,590 g) than northern foxes
(71
-72 g) may be a reflection
of
the dif-
ferent availability
of
prey sizes in the en-
vironment. In particular, European hares are
abundant, large, and preyed upon by both
foxes
in
Parque Nacional Torres del Paine.
Auc6
foxes do not
segregate
their
ac-
tivities throughout the 24 h daily cycle. Chi-
11as
and culpeos were active at any time.
Similarly, Johnson (1992) did not find dif-
ferent patterns
of
activity between chillas and
culpeos in Parque Nacional Torres del Paine,
although they both were more active at night.
In summary, sympatric chillas and culpeos
at Auc6 present low spatial overlap, inter-
mediate diet overlap, and complete temporal
overlap. It is remarkable that sympatric foxes
at Parque Nacional Torres del Paine, under
quite
different
environmental
conditions,
partition resources in the same way as foxes
in
Auc6.
A revised hypothesis
Habitat selection is scale dependent. Without
definition
of
scale, this concept is too broad
and vague. Fuentes & Jaksic's (1979) use
of
habitat partitioning was applied to a large
geographical scale,
or
first-order selection
(sensu Johnson 1980). This may be the first
step for understanding coexistence
of
wide
ranging, mobile, and opportunistic mammals
such
as foxes.
However,
the
information
analyzed here shows that chillas and culpeos
also
respond
to
second-
and
third-order
selection (individual home ranges and habitat
components,
respectively).
These
smaller
spatial scales, were not considered in Fuentes
&
Jaksic's
hypothesis.
Therefore,
the
hypothesis
needs to be
modified to render it more realistic in light
of
the new evidence and detailed reanalysis
of
previous evidence. Current information
indicates
that
fox
distributions
are much
more complicated than previously believed.
Throughout
Chile
chillas and culpeos are
found in both allopatric (or parapatric) and
sympatric
contexts,
independent
of
their
body sizes (Jimenez et al. 1995). Although
not all combinations
of
species occurrences
and habitat types are found, culpeos appear
more
frequently
associated
with
higher
elevations
and
more
rugged
landscapes
than chillas. The latter occur more often in
lowlands and level landscapes. These foxes
are sympatric at intermediate elevations and
in areas where the landscape appears more
complex at an
intermediate
spatial scale,
and habitat patches are interspersed. Patchy
prey productivity compounded with habitat
heterogeneity may be important features
of
intermediate-elevation sites. Therein, foxes
may partition space at a fine scale, so that
they coexist in sympatry but not in syntopy
(Johnson
1992,
Jimenez
1993).
The
proximate mechanism appears to be inter-
ference, a process driven by the dominant
culpeo,
which
monopolizes
high-quality
patches and excludes chilla to low-quality
ones (Johnson et al., ms. submitted).
Mountains
where
culpeos
occur
allopatrically
may
not
be
heterogeneous
enough to enable the presence
of
chillas.
Conversely,
lowland
and
coastal
habitats
may not have the larger prey species needed
by the more energetically demanding culpeo.
Evidence
of
food-limitation for culpeo, as
well as
intolerance
of
chillas
and
other
culpeos, is provided by Crespo &
De
Carlo
(1963) and Abello (1979, as cited in Johnson
1992). In the first case, culpeos expanded
their
range
and
became
more
abundant
owing to an increase
of
food supply (sheep
ranching) in
Neuquen,
Argentina.
In the
second
case,
the
removal
of
livestock
(potential food for culpeos, Crespo &
De
Carlo 1963, Novaro 1991 ), resulting from
the establishment
of
a National Park
at
To-
rres del Paine, correlated with the invasion
of
chillas, presumably as a result
of
culpeo
decrease in abundance.
However, under the scenario described, it
is still not clear why Parque Nacional Fray
Jorge, at a latitude, altitude, and with an en-
vironmental heterogeneity similar to Auc6,
supports
culpeos
but
not
chillas.
There,
culpeos are also larger than those at Auc6
(Jimenez et al. 1995). Competitive release
(i.e.,
absence
of
chillas)
does
not
fully
122 JIMENEZ ET AL.
explain the pattern at Fray Jorge. Prey size
distribution (Meserve et al. 1987) does not
account for the larger body size
of
Fray Jorge
culpeos.
Indeed,
Chinchillas
(Chinchilla
lanigera) and hares (Lepus capensis) which
are the largest mammalian prey at Auc6, are
absent from the otherwise similar prey base
at Fray Jorge (where the largest prey is
approximately 200 g, Meserve et al. 1987).
The fact that nowadays chinchilla abundance
at Auc6
is
very low (Jimenez 1993) goes
counter the prey-size availability hypothesis
to explain fox coexistence. However, the
increase in
rabbit
populations
may
have
compensated for the loss
of
chinchillas (e.g.,
Simonetti 1986), thus supporting the co-
existence
of
chillas and culpeos.
In
conclusion,
Fuentes
&
Jaksic's
hypothesis is partially valid (see Jimenez et
al. 1995),
but
requires
consideration
of
two factors previously ignored: the spatial
scale at which coexistence occurs, and the
availability
of
high-quality
(large) prey.
Where large prey such as rabbits
or
hares
(Lepus capensis) are present, the two fox
species may eo-occur in sympatry provided
that the habitat is sufficiently complex to
offer shelter for the smaller fox from the
aggressively dominant culpeo. Where only
small prey is present, only one fox species
will survive, most often (but not necessarily)
the smaller chilla.
ACKNOWLEDGMENTS
The Corporaci6n Nacional Forestal provided
logistics and permitted work at the Reserva
Nacional Las Chinchillas. Boris Saavedra
and
Christian
Muiioz helped in the field
and Enrique Silva in the laboratory. Warren
Johnson
assisted
with
radio-tracking
expertise. Jimenez thanks his former advisor
Kent
Redford
for
support
and
encoura-
gement, and Warren Johnson, Wes Stone and
Fred W agner for comments on an earlier
draft. Jimenez also thanks Patricio Jimenez
and Irene Davila for hospitality in Santiago,
and Marfa Ines for understanding his lengthy
absences from home. This study was sup-
ported by grants from FONDECYT 92-0038,
Scott Neotropic Fund (Lincoln Park Zoo),
and Tropical Conservation and Development
Program (University
of
Florida).
Jimenez
was
initially
supported
by
a
Fullbright-
LASPAU fellowship and eo-wrote this paper
under a Quinney Fellowship from Utah State
University.
LITERATURE CITED
ALLEN JA (1905) Reports
of
the Princeton Expedition to
Patagonia, 1896-1899. Zoology. Part I. Mammalia
of
southern Patagonia. Schweitzerbartsche Verlagshand-
lung, Stuttgart.
ANDELT WF, CE HARRIS &
FF
KNOWLTON (1983)
Prior trap experience might bias coyote responses to
scent stations. Southwestern Naturalist 30: 317-318.
ATALAH AG, W SIELFELD & C VENEGAS (1980) Ante-
cedentes sobre el nicho tr6fico de Canis griseus Gray
1836, en Tierra del Fuego. Anales del lnstituto de
La
Patagonia (Chile) 11: 259-271.
BUSTAMANTE RO, JA SIMONETTI & JE MELLA (1992)
Are foxes legitimate and efficient seed dispersers? A
field test. Acta Oecologica
13:
203-208.
CRESPO JA, & JM DE CARLO (1963) Estudio ecol6gico
de una
poblaci6n
de zorros
colorados
Dusicyon
culpaeus culpaeus (Molina) en el oeste de la provin-
cia
de
Neuquen. Revista del Museo Argentina de
Ciencias Naturales "Bernardino Rivadavia", Ecologfa
I:
1-55 + 9 plates.
DE LA MAZA AG ( 1981) Dieta
alimentaria
de zorros
(Dusicyon) en zonas de distribuci6n de Chinchilla
/anigera, Auc6 (lllapel-JV Region). DVM Thesis,
University
of
Chile, Santiago.
DU
RAN JC, CA TT AN PE & JL Y
AÑEZ
(1985) The grey
fox Canis griseus (Gray) in Chilean Patagonia (south-
ern Chile). Biological Conservation 34: 141-148.
DURAN JC, PE CATTAN & JL
YAÑEZ
(1987) Food habits
of
foxes (Canis sp.) in the Chilean National Chinchi-
lla Reserve. Journal
of
Mammalogy 68: I 79-181.
EBENSPERGER
LA.
JE
MELLA
&
JA
SIMONETTI
( 199 I) Trophic-niche relationships among Galictis
cuja, Dusicyon culpaeus, and
Tyro
alba in central
Chile. Journal
of
Mammalogy 72: 820-823.
FUENTES
ER
& FM
JAKSIC
(1979)
Latitudinal
size
variation
of
Chilean
foxes:
tests
of
alternative
hypotheses. Ecology 60: 43-47.
GINSBERG JR, DW
MACDONALD,
compilers
(1990)
Foxes. wolves, jackals, and dogs: An action plan
for the conservation
of
canids. IUCN/SSC Canid
Specialist Group and IUCN/SSC
Wolf
Specialist
Group. International Union for Conservation
of
Nature
and Natural Resources, Gland, Switzerland. 116 pp.
G !TTLEMAN JL (1985) Carnivore body size: ecological
and taxonomic correlates. Oecologia 67: 540-554.
GREER JK ( 1965) Mammals
of
Malleco Province, Chile.
Publications
of
the
Museum,
Michigan
State
University, Biological Series
3:
49-152.
HOUSSE R (1953) Animales salvajes de Chile en su clasifi-
caci6n moderna: su vida y sus costumbres. Ediciones
Universidad
de
Chile, Santiago. 189 pp.
IRIARTE
JA,
JE
JIMENEZ,
LC
CONTRERAS
& FM
JAKSIC
(1989)
Small-mammal
availability
and
consumption by the fox, Dusicyon culpaeus, in cen-
tral Chilean scrublands. Journal
of
Mammalogy 70:
641-645.
JAKSIC
FM
&
JL
Y
ANEZ
(1983)
Rabbit
and
fox
introductions
in
Tierra
del
Fuego:
history
and
assessment
of
the attempts at biological control
of
NICHE-COMPLEMENT ARITY
OF
SOUTH AMERICAN FOXES
123
the rabbit infestation. Biological Conservation 26:
367-374.
JAKSIC
FM.
RP
SCHLATTER
& JL
YANEZ
(1980)
Feeding ecology
of
central Chilean foxes Dusicyon
culpaeus
and
Dusicyon
griseus.
Journal
of
Mam-
malogy 61: 254-260.
JAKSIC FM, JL Y ANEZ & JR RAU (1983) Trophic relations
of
the southernmost populations
of
Dusicymz in Chile.
Journal
of
Mammalogy 64: 693-697.
JAKSIC
FM,
JE
JIMENEZ,
SA
CASTRO
& P
FEINSINGER
(
1992)
Numerical
and
functional
response
of
predators to a long-term decline
in
mam-
malian prey at a semi-arid Neotropical site. Oeco-
logia 89: 90-101.
JAKSJC FM, PL MESERVE, JR GUTIERREZ &
EL
TA-
B ILO (199 3) The components
of
predation on small
mammals in semiarid Chile: preliminary results. Re-
vista Chilena de Historia Natural 66: 305-321.
JIMENEZ
JE ( 1993)
Comparative
ecology
of
Dusicyon
foxes at the Chinchilla National Reserve in north-
central Chile. Master
of
Science Thesis, University
of
Florida, Gainesville, Florida. viii + 163 pp.
JIMENEZ
JE. JL Y
AÑEZ,
EL TABILO & FM JAKSIC
( 1995) Body size
of
Chilean foxes: a new pattern in
light
of
new data. Acta Theriologica 40: 321-326.
JIMENEZ
JE, JL Y
ANEZ
&
FM
JAKSIC
(Accepted)
Inability
of
thin-layer-chromatography
to
distinguish
feces
from
congeneric
foxes
by
their
bile
acid
contents. Acta Theriologica.
JOHN
SON
DE
(
1980)
The
comparison
of
usage
and
availability
measurements
for evaluating resource
preference. Ecology 61: 65-71.
JOHN
SON
WE
( 1992) Comparative ecology
of
the two
sympatric South American foxes. Dusicyon culpaeus
and
D.
griseus. PhD Thesis, Iowa State University,
Ames, Iowa. 142 pp.
JOHNSON WE & WL FRANKLIN ( 1994) Role
of
body
size in the diets
of
sympatric gray and culpeo foxes.
Journal
of
Mammalogy 75: 163-174.
JOHNSON
WE.
JE
JIMENEZ
&
WL
FRANKLIN
(submitted) Energy requirements and local distribu-
tions
of
sympatric
Dusicyon
griseus and
D.
cu/paeus
in South America. Mastozoologia Neotropical (Ar-
gentina).
LINHART
SB &
FF
KNOWLTON (1975) Determining the
relative abundance
of
coyotes by scent station lines.
Wildlife Society Bulletin
3:
119-124.
MANN G ( 1945) Mamfferos de Tarapaca: observaciones
realizadas durante una expedici6n al alto norte de
Chile. Biol6gica (Chile)
2:
23-134.
MARES MA, RA OJEDA & RM BARQUEZ (1989) Guide
to
the
mammals
of
Salta
province,
Argentina.
University
of
Oklahoma Press, Norman, Oklahoma.
MARQUET
PA. LC CONTRERAS, JC TORRES-MURA,
SI SILV A & FM
JAKSIC
(1992) Food habits
of
Pseudalopex
foxes
in the
Atacama
desert,
pre-
Andean
ranges, and the
high
Andean
plateau
of
northernmost Chile. Mammalia 56: 77-82.
MARTINEZ DR, JR RAU, R MURUA & MS TILLERIA
( 1993) Depredaci6n selectiva de roedores por zorros
chillas (Pseudalopex griseus) en la pluviselva valdi-
viana, Chile. Revista Chilena de Historia Natural 66:
419-426.
MEDEL RG & FM JAKSIC (1988) Ecologfa de Ios canidos
sudamericanos: una revision. Revista Chilena de His-
toria Natural 61: 67-79.
MED EL RG, JE JIMENEZ, FM JAKSIC, JL Y ANEZ & JJ
ARMESTO ( 1990) Discovery
of
a continental pop-
ulation
of
the rare
Darwin's
fox,
Dusicyon
fulvipes
(Martin, 1837) in Chile. Biological
Conservation
51: 71-77.
MESERVE PL. EJ SHADRICK & DA KELT (1987) Diets
and
selectivity
of
two
Chilean
predators
in
the
northern semi-arid zone. Revista Chilena de Historia
Natural 60: 93-99.
NOV ARO
AJ
(1991) Feeding ecology and abundance
of
a
harvested population
of
culpeo fox (Dusicyon cul-
paeus)
in Patagonia. Master
of
Science Thesis, Uni-
versity
of
Florida, Gainesville, Florida. vii + I 03 pp.
OS
GOOD
WH
(1943)
The
mammals
of
Chile.
Field
Museum
of
Natural History,
Zoological
Series
30:
1-268.
RAMSDEN RO.
PF
COPPIN &
DH
JOHNSTON (1976)
Clinical
observations
on
the
use
of
ketamine
hydrochloride in wild carnivores. Journal
of
Wildlife
Diseases
12:
221-225.
RAU JR, DR MARTINEZ, JR
LOW
& MS
TILLERIA
( 1995) Depredaci6n por zorros chillas
(Pseuda/opex
griseus) sobre micromamiferos cursoriales, escanso-
riales y arborfcolas en un
área
silvestre protegida del
sur de Chile. Revista Chilena de Historia Natural 68:
333-340.
REDFORD KH &
JF
EISENBERG (1992) Mammals
of
the
Neotropics. Volume
2.
the southern cone: Chile, Ar-
gentina, Uruguay, Paraguay. University
of
Chicago
Press, Chicago, Illinois. ix + 430 pp.
ROSENZWEIG
ML
(
1966)
Community
structure
in
sympatric Carnivora. Journal
of
Mammalogy
47:
602-612.
SCHOENER TW (1974) Resource partitioning in ecological
communities. Science 185: 27-39.
SHELDON JW (1992) Wild dogs: the natural history
of
the
nondomestic Canidae. Academic Press, New York.
248 pp.
SIMONETTI JA ( 1986) Human-induced dietary
shift
in
Dusicyon cu/paeus. Mammalia 50: 406-408.
SIMONETTI JA. A POIANI & KJ RAEDEKE (1984) Food
habits
of
Dusicyon griseus in northern Chile. Journal
ofMammalogy
65:515-517.
VEZINA
AF
(
1985)
Empirical
relationships
between
predator and prey size among terrestrial vertebrate
predators. Oecologia 67: 555-565.
WAYNE RK, B VAN VALKENBURGH, PW KAT, TK
FULLER,
WE
JOHNSON & SJ
O'BRIEN
(1989)
Genetic
and
morphological
divergence
among
sympatric canids. Journal
of
Heredity 80: 447-454.
