Analysis of trophic structure of two carnivore assemblages
by means of guild identification
Sonia Cristina Zapata & Alejandro Travaini &
Pablo Ferreras & Miguel Delibes
Abstract We evaluated the existence of trophic guild structure, considering seasonal and annual variation, in two
terrestrial carnivore assemblages: one from Santa Cruz
province (Argentinean Patagonia, composed by six carnivore species), and the other from Doñana National Park (SW
Spain, composed by five carnivore species). To identify
trophic guilds, we first studied seasonal and annual diets of
predators, calculated trophic overlap among species pairs,
and then constructed overlap matrices (similarity matrices).
We determined guild membership objectively by entering
the similarity matrices into the clustering technique unweighted pair-group method with arithmetic averaging.
Carnivores from both assemblages were grouped, respectively, into four feeding guilds. Lagomorphs and rodents
C ommunicated by C. Gortazár
S. C. Zapata (*) : A. Travaini
Centro de Investigaciones de Puerto Deseado (UNPA-UACO),
Av. de la Prefectura Naval s/n,
9050 Puerto Deseado, Santa Cruz, Argentina
e-mail: titinazapata@yahoo.com.ar
A. Travaini
CONICET,
Puerto Deseado, Santa Cruz, Argentina
P. Ferreras
Instituto de Investigación en Recursos Cinegéticos (IREC),
CSIC-UCLM-JCCM,
Ronda Toledo s/n,
13005 Ciudad Real, España
M. Delibes
Estación Biológica de Doñana (CSIC),
Av. de María Luisa s/n,
41013 Sevilla, España
.
Keywords Diet overlap . Community structure .
Resource use . Patagonia . Doñana National Park
Introduction
A current practice both in empirical and theoretical studies
of ecological communities consists in simplifying the
analysis of food webs by grouping species into groups,
namely, guilds (Root 1967; Terborgh and Robinson 1986;
Hawkins and MacMahon 1989; Jaksic 1981; Jaksic and
Medel 1990; Simberloff and Dayan 1991; Wilson 1999;
Blondel 2003). This concept was first introduced by Root
(1967) who defined them as “groups of species that exploit
the same class of resources in a similar way.” This
definition is immersed in the conceptual framework of
competition theory: exploitative competition will usually
occur among guild members (Pianka 1980), especially
when guilds include a moderate to small number of species
(MacNally 1983).
Nevertheless, Jaksic et al. (1993) and Wiens (1989,
1993) pointed out that interspecific competition is not necessarily a prerequisite for the emergence of guild structure.
Opportunistic capacity of some species to take advantage of
temporarily superabundant resources (Erlinge et al. 1982;
Jiménez et al. 1992; Meserve et al. 1995) may originate the
same emergent phenomenon especially when guilds include
species with trophic plasticity and opportunistic feeding
behavior (Travaini et al. 1996; Fedriani and Travaini 2000).
Accordingly, Jaksic et al. (1996) and Farias and Jaksic
(2004) suggested the hypothesis that guilds are originated
by opportunistic convergence of species on abundant and
energetically rewarding resources.
The guild approach has sometimes been considered as a
starting point for understanding the role of species associates
(Jaksic 1981), representing the ecological structure of
communities (Keddy 1990; Southwood 1996). Nevertheless,
it is unclear whether species of the same guild are more
similar in functional effects than are species of different
guilds (Chalcraft and Resetarits 2003). After decay some
years ago (Simberloff and Dayan 1991), the interest in the
concept of guilds has increased in recent years, and guilds
have been advocated as the key to a number of issues in
ecology and conservation, including ecosystem functioning
and communities dynamics (Wilson 1999).
Analyses of trophic structure of carnivore communities based on the study of guilds are scarce. These
focused in a subset of the community (Jaksic and
Delibes 1987; Jaksic et al. 1993, 1996, but see Travaini
et al. 1996) or established guild membership among
samples of species dispersed in time and space (Travaini
1995; Fedriani and Travaini 2000). Although guild
structure was detected in these studies, the repeatability
of guilds in time should be demonstrable if guilds are
fundamental units or basic “building blocks” of communities (Blondel 2003). But this approach was rarely
performed on carnivore communities.
In this work, we use a guild approach to study the
trophic structure of two carnivore assemblages: one from
southern Patagonia Argentina and one from the Doñana
National Park (DNP), in Spain. The assemblage from
Patagonia was constituted by six species: the puma (Puma
concolor), the pampas cat (Oncifelis colocolo), the culpeo
fox (Pseudalopex culpaeus), the Patagonian gray fox
(Pseudalopex griseus), the Patagonian hog-nosed skunk
(Conepatus humboldtii), and the lesser grison (Galictis
cuja). Those from Doñana were five carnivore species: the
Iberian lynx (Lynx pardinus), the red fox (Vulpes vulpes),
the badger (Meles meles), the Egyptian mongoose (Herpestes
ichneumon), and the common genet (Genetta genetta). We
did not include the European wildcat (Felis silvestris) in our
study because its occurrence in the Park was very rare at the
time of the study (Fernández-Requena 1997).
Our specific goals were: (1) To identify trophic guild
structure in both assemblages, based on similar resource
utilization by species, by means of objective methods to
establish guild membership (Jaksic and Medel 1990; Pillar
1999). These methods consist in determining cut-off
points in cluster analysis from computer algorithms based
on bootstrap procedures. (2) To evaluate the existence of
seasonal and/or annual changes in trophic guild structure
in both assemblages, or lack of them, which would
indicate some constancy of guild structure in time. (3) To
compare results obtained for both assemblages as a
function of the use of prey resource base, to explore
whether these different assemblages are constructed with
similar kinds of guilds, and if those guilds are constituted
by similar species.
Materials and methods
Study areas
One of the areas was located in the northeastern portion of
Santa Cruz Province, southern Argentina Patagonia, and
belongs to the Deseado Department. It is a region of
11,000 km2 which includes a protected area: the Monumento Natural Bosques Petrificados (approximately 47°66′
S, 67°99′W) and the surroundings of Puerto Deseado city
(47°47′S; 65°49′W). This region is typically a flat steppe
covered by tussock grasses and dome shaped spindly
shrubs, with low cover (20 to 30%) interrupted by ravines
and rocky outcrops (Soriano 1983). The weather corresponds to that of a desert biome, with rainfall and snowfall
fluctuating between 110 and 150 mm, and concentrated
during the winter time (Oliva et al. 2001). We distinguished
two climatic seasons: (1) a relative warm and dry season,
between October and March, corresponding to spring and
summer. In this period, highest temperatures are reached,
no rainfalls are registered, and winds get a great frequency
and intensity. (2) A relative cold season, from April to
September, corresponding to autumn, winter, and the start
of spring. This season concentrates precipitation and
achieves the lowest temperatures, with frequent frosts
(León et al. 1998).
The other study area was the Biologic Reserve of
Doñana (BRD, 6,794 Ha, 37°00′N, 06°30′W), and
surrounding estates (La Algaida, to the North and El Puntal
to the South), constituting the core area of DNP located in
SW Spain. The area is occupied mainly by Mediterranean
scrubland, and the ecotone between the scrubland and the
adjacent marshlands locally called Vera, where high rabbit
densities and highest diversity of vertebrate predators are
found (Valverde 1958; Kufner 1986; Villafuerte et al.
1997). Climate is Mediterranean subhumid, with hot and
dry summers (mean temperature between 23.4 and 23.6°C
and rainfall less than 5 mm) and mild and rainy winters
(600 mm), and temperatures rarely below freezing (mean
temperature 9.3°C).
European rabbit (Oryctolagus cuniculus) populations
from DNP decreased drastically after the arrival of the
rabbit hemorrhagic disease (RHD) in 1990, remaining
about one third the former densities (Villafuerte et al.
1994, 1995). The rapid decrease in the number of rabbits
affected predators in different ways, but as a general rule,
there was a reduction in the consumption of rabbits among
the different species (Ferreras et al., unpublished data). We
then considered two periods for our study: one before and
one after the arrival of the RHD at Doñana.
Dietary analysis
We used diet information of carnivores from Patagonia
from previous works (Zapata 2005 and Zapata et al. 2001,
2005a, b). The diets of these species were estimated from
fresh feces collected between July 1998 and August 2000
and corresponded to the two climatic seasons mentioned
above. Diet information of carnivores from Doñana were
taken from studies conducted at the Park between 1973 and
1986, long time before the decline of rabbit populations
(Delibes 1980; Rau 1987; Palomares and Delibes 1991a, b;
Martín et al. 1995). From January 1990 to January 1992,
after the arrival of the RHD, we collected a sample of feces
from the five carnivores species. To analyze the diet of
these species during this period, we followed the same
procedure as in our previous works (see above).
The importance of each prey type in the diet of each
predator from Patagonia was quantified calculating the
dry mass of each food type in the feces ×100/total dry
mass of feces because we were not able to transform the
dry weight of scats to consumed biomass. For the
assemblage from Doñana, the importance of different
prey in the carnivores diet was estimated by using the
percentage of ingested biomass, estimated by transforming the dry weight of scats to consumed biomass. For
this purpose, we used correction factors for each species
in the area when available (Lockie 1959, 1961; Palomares
and Delibes 1990; Martín et al. 1995; Aldama 1993).
Methods of diet quantification that take into account
the biomass of prey are more adequate to estimate
trophic relationships among vertebrate predators when
prey sizes are variable (Fedriani and Travaini 2000).
Seasonal differences in the diets of species from Patagonia
were tested through a contingency-table analysis (G test,
Sokal and Rohlf 1981).
Trophic guilds identification
With diet results, we first calculated diet overlap between
species pairs by using a symmetrical overlap index (Pianka
1973); for this purpose, we utilized percent of dry weight
for Patagonian carnivores and percent of consumed
biomass for Doñana carnivores:
X
O¼
X
p i qi
p2i
X
q 2i
1=2
where pi = percent of dry weight or consumed biomass of a
prey type in one predator’s diet and qi = percent of dry
weight or consumed biomass of the same prey type in a
second predator’s diet.
With diet overlap values, we then constructed overlap
matrices called “similarity matrices.” We obtained four
similarity matrices: two for Patagonia, which corresponded
to each climatic season (spring–summer and autumn–
winter), and two for Doñana, which corresponded to
carnivores diet overlaps before and after the arrival of
RHD.
We determined guild membership by entering the
similarity matrices into the clustering technique unweighted
pair-group method with arithmetic averaging (UPGMA;
Sneath and Sokal 1973; Jaksic and Delibes 1987). Average
linkage is a space-conserving strategy and is the most
frequently used technique, the algorithm is unique in that it
appears to maximize the correlation between the input
dissimilarities (in the entities-by-entities dissimilarity matrix) and the output dissimilarities implied by the resulting
dendrogram termed the cophenetic correlation (McGarigal
et al. 2000). To determine the level of similarity that defines
the groups in the dendrogram (i.e., guilds), we used an
objective method that allowed us to identify guilds with
statistical significance. The method, developed by Strauss
(1982) and modified by Jaksic and Medel (1990), is based
on bootstrap procedures to generate overlap pseudovalues
between all pairs of predators. We used one of the
randomization algorithms proposed by Lawlor (1980) to
resample the predator by prey matrix (dietary matrix). This
algorithm retained zero values (where they were found) of
frequencies of biomass of prey (rows), independently and
simultaneously for each and every predator (columns) in
the matrix. The dietary overlap (overlap pseudovalues)
between all pairs of predators was computed in every
iteration. We repeated this procedure 1,000 times to obtain
a frequency distribution of pseudovalues, and that overlap
pseudovalue that exceeded the 95% percentile was chosen
as the cut point in the dendrogram (Jaksic and Medel 1990).
Statistical analyses were performed with STATISTICA 6.0
and Microsoft Office Excel for PC.
Results
Guild structure of carnivore assemblage: seasonal variation
in guilds composition
(1) Patagonia
The dendrogram obtained from applying the UPGMA
technique to the similarity matrix from the autumn–winter
period is shown in Fig. 1. The 95% of the pseudovalues
obtained from randomization of the original similarity
matrix was achieved at a similarity level of 54%. This
value was used as the cut off point to identify groups in the
dendrogram with statistical significance (p < 0.05, Fig. 1). In
this way, the species from Patagonia were separated into
four groups which we considered trophic guilds because
they contained species that exploit resources in a similar
way. The guilds were named according the dominant prey
consumed by their members. Three guilds were composed
by only one species and one guild was composed by three
species, they were:
(1.1) Guild I: composed by the puma. A large felid that
ate mainly edentates (Patagonian pichi, Zaedyus
pichii), big rodents (the mara, Dolichotis patagonum), and is capable of subduing ungulates
larger than itself, like the guanaco (Lama
guanicoe). In addition, the introduced European
hare (Lepus europaeus) was abundant in the diet
of this felid (Table 1). We named this guild as
the “edentates–ungulates” feeding guild.
(1.2) Guild II: composed by the pampas cat. A
small cat that consumed mainly rodent species
over the year: rabbit rats (Reithrodon auritus)
Fig. 1 Trophic guild structure
of carnivore assemblage from
NE Santa Cruz, Argentine Patagonia during autumn–winter.
Dotted line at 54% of similarity
indicates the existence of four
guilds (in brackets) with statistical significance (p < 0.05).
Cophenetic correlation = 0.90
and Magellan’s tucos (Ctenomys magellanicus;
Table 1). Therefore, we named this guild as the
“rodents” feeding guild.
(1.3) Guild III: composed by the lesser grison and the
two canids (culpeo and gray foxes). The grison
behaved as a specialist in the consumption of
mammals, its diet was dominated by rodents
(lesser cavies, Microcavia australis, and rabbit
rats were the more abundant species; Table 1),
but also consumed European hare in a great
proportion. Mammals were the most important
prey in the diet of the culpeo fox during this
season. European hare was the most important
item together with large rodents (mainly lesser
cavies and rabbit rats), but culpeo foxes also
consumed edentates and carrion (Table 2). Birds,
arthropods, and fruits were less important in its
diet (Tables 1 and 2). A great variety of foods
were included in the diet of the gray fox during
this period (Table 2), but rodents, European
hares, and edentates were the more important
items. Among rodents, large species like the
lesser cavy were the more frequent species.
Birds, arthropods, and plant materials were also
present in its diet. The three species converged
in the consumption of European hares and lesser
cavies during this period. Note that the lesser
grison and the culpeo fox constituted a subunit
inside the group (Fig. 1) because they consumed
hares in a greater proportion than the gray fox.
Although lesser cavies, a rodent species, were an
important item in the diet of these predators, we
named this guild as the “lagomorphs” feeding
guild to make a difference with the previous
guild.
(1.4) Guild IV: composed by the Patagonian skunk.
This species ate a great proportion of arthropods
during this season, although rodents, carrion,
birds, and fruits were also present in its diet
(Tables 1 and 2). We named this guild as the
“arthropods” feeding guild.
During the spring–summer, the same guilds were
present, but with some variation in species composition.
In the dendrogram obtained for this period (Fig. 2), the 95%
of the pseudovalues derived from randomization of the
original similarity matrix was achieved at a similarity level
of 63%. This value, used as the cut off point to identified
groups in the dendrogram, allowed us to identified four
groups (p < 0.05, Fig. 2). The puma, the pampas cat, the
culpeo fox and the Patagonian skunk stayed in the same
guilds, but the lesser grison overlapped with the pampas cat
because this species increased the consumption of rodents
and decreased the consumption of lagomorphs, although
these seasonal differences in grison diet were not statistically significant. On the other hand, the gray fox increased
the consumption of arthropods, overlapping its diet with
that of the skunk (Tables 1 and 2).
2) Doñana
In the period previous to the arrival of the RHD, we
identified four guilds. The 95% of the pseudovalues obtained
from randomization of the original similarity matrix was
achieved at a similarity level of 70% (p < 0.05, Fig. 3). During
this period, three guilds were composed by only one species
and the last guild was composed by two species, they were:
(2.1) Guild I: composed by the Iberian lynx and the
badger. These species converged in the consumption of rabbit (Oryctolagus cuniculus),
which accounted for 84.7 and 67.6% of the total
consumed biomass, respectively (Table 3).
Therefore, we named this guild as the “lagomorphs” feeding guild.
(2.2) Guild II: composed by the red fox, a generalist
species that consumed mammalian prey, but the
proportion of insects and fruits were more important in its diet (Table 3). We named this guild as
the “arthropods and fruits” feeding guild.
(2.3) Guild III: composed by the common genet,
whose diet was based on rodents (71.8%
consumed biomass, Table 3), so we named this
guild as the “rodents” feeding guild.
Table 1 Overall diets of predators form Patagonia from July 1998 to August 2000, expressed as percent of dry mass of vertebrate classes,
arthropods, and plant materials found in feces
Prey item
Edentates
Chaetophractus sp
Zaedyus pichiy
Rodents
Akodon spp.
Eligmodontia sp
Phyllotis xanthophygus
Reithrodon auritus
Ctenomys magellanicus
Microcavia australis
Dolichotis patagonum
Unidentified rodent
Lagomorpha
Lepus europaeus
Lama guanicoe
Galictis cuja
Conepatus humboldtii
Carrion
Birds
Reptiles
Arthropods
Plant material
Number of feces
a
Taken as carrion
Puma
concolor
Oncifelis
colocolo
Galictis
cuja
Conepatus
humboldtii
Pseudalopex
culpaeus
Pseudalopex
griseus
2.1
39.6
0
0.2
0
1.0
0
2.4
0.3
7.3
0
14.9
0
0
0
0
0
0
14.6
0
4.1
0.6
0.9
34.3
26.9
18.5
0
5.5
9.2
3.2
9.9
12.0
8.4
21.8
0
10.7
20.5
1.9
0
15.0
6.0
10.4
0
11.4
2.6
0.3
0.2
12.1
1.2
19.2
0
3.4
14.7
5.0
0.5
0.8
11.9
23.4
0
9.5
22.9
18.4
1.5
0.9
0
5.7
–
–
–
39
8.6
0
0.6
0
0
7.9
4.7
–
–
126
23.7
0
0
0.2
0
5.2
–
1.3
–
171
6.8a
0
0
0
25.5
1.2
2.2
58.1
19.1
217
42.4
0
0.3
0.8
9.9
4.3
0.3
1.2
13.2
316
9.5
0
0.1
0.2
9.6
6.6
0.6
29.4
0.3
203
Table 2 Frequency of occurrence (%) of the different prey categories in the diets of the Patagonian hog-nosed skunk, culpeo fox and grey fox
during spring–summer and autumn–winter
Prey class
Edentates
Rodents
Large rodents
Small rodents
Lagomorphs
Other mammals
Birds/reptiles
Carrion
Arthropods
Plant materials
Conepatus humboldtii
Pseudalopex culpaeus
Pseudalopex griseus
Spring–summer
Autumn–winter
G test: G = 15.34; df =4; p < 0.01
Spring–summer
Autumn–winter
G test: G = 21.5; df =8; p< 0.01
Spring–summer
Autumn–winter
G test: G = 22.3; df =6; p < 0.01
–
12.6
12.6
4.5
86.5
22.5
6.5
9.0
22.1
18.1
32.1
1.5
13.5
4
12
36.7
24.5
10.7
35.2
2.4
9.8
7.3
2.6
10.6
10
12.3
27.1
44.7
3.6
30
27.5
12.3
7.2
5.4
100
10.9a
5.4
57.8
21.4
2.7
3.6
68.9
5.6
The occurrence numbers of prey from these categories were used in G tests to search for seasonal differences in their diets
a
Only birds
(2.4) Guild IV: composed by the Egyptian mongoose,
a generalist species with a diet that included
rabbits, rodents, but also included birds, reptiles
and carrion in high proportions (Table 3). Accordingly, we named this guild as the “birds,
reptiles, and carrion” feeding guild.
After the arrival of the RHD, when the rabbit population
was diminished in Doñana, the same guilds were present
with variation in species composition (Fig. 4, cut point at
65% similarity, p < 0.05). The Iberian lynx, the common
genet, and the Egyptian mongoose stayed in the same
guilds as in the previous period (Fig. 4). The Iberian lynx
and the common genet still preyed on rabbits and rodents,
Fig. 2 Trophic guild structure
of carnivore assemblage from
NE Santa Cruz, Argentine Patagonia during spring–summer.
Dotted line at 63% of similarity
indicates the existence of four
guilds (in brackets) with statistical significance (p < 0.05).
Cophenetic correlation = 0.89
respectively (Table 3). Nevertheless, the Egyptian mongoose changed its diet, although it stayed in the same guild,
due to the increase in the consumption of carrion (Table 3).
The red fox, which increased the consumption of carrion
and birds (Table 3), overlapped its diet with that of the
Egyptian mongoose and changed to the “birds, reptiles, and
carrion” feeding guild. On the other hand, the badger
changed to the “arthropods and fruits” feeding guild, which
was composed by the red fox before the arrival of the RHD.
During this period, the badger consumed a great amount of
arthropods, which accounted for 45% of the total consumed
biomass (Table 3).
Fig. 3 Trophic guild structure
of carnivore assemblage from
Doñana (SO Spain), before the
arrival of the HRD period. Dotted line at 70% of similarity
indicates the existence of four
guilds (in brackets) with statistical significance (p < 0.05).
Cophenetic correlation = 0.94
Discussion
Trophic guild structure of carnivore assemblages
from Patagonia and Doñana: seasonal and annual
variation in guilds composition
We identified four feeding guilds at SE Patagonia, which
were present in the two studied periods, but with changes in
some species composition. These changes, related with
changes in diet overlaps among predators, have been
associated with fluctuations in the availability of resources
and with the opportunistic capacity of some species to take
advantage of these fluctuating resources (Erlinge et al.
1982; Jiménez et al. 1992; Meserve et al. 1995). Like in
other desert areas with marked seasonality (Miles 1990;
Polis 1991; Wiens 1991), a change is produced in
Patagonian steppes during the warmer season offering
new resources for predator and prey, mainly arthropods
and fruits, resulting in a period of relative abundance of
resources (Wiens 1991). The gray fox, a generalist species
(Zapata et al. 2005b) took advantage of these ephemeral
and abundant resources, resulting in trophic segregation
among the culpeo fox and the grison, and changed to the
“arthropods“ feeding guild. The lesser grison, although did
not show statistical differences in its diet over the two
seasons (Zapata et al. 2005a), decreased the consumption of
lagomorphs and increased the consumption of rodents
overlapping its diet with the pampas cat and changing to
the rodents feeding guild. The culpeo fox also took
advantage of fluctuating resources because it consumed
Table 3 Percent of consumed biomass of vertebrate classes, arthropods, and plant materials in feces for five carnivore species from Doñana
National Park before (first column) and after (second column) the arrival of the rabbit hemorrhagic disease (RHD)
Prey item
Lynx
Lynx
pardinus
pardinus
Number of feces, 153
Vulpes
Vulpes
vulpes
vulpes
Number of feces, 172
Meles
Meles
meles
meles
Number of feces, 141
Herpestes
Herpestes
ichneumon ichneumon
Number of feces, 101
Genetta
Genetta
genetta
genetta
Number of feces, 170
Ungulates
Rodents
Lagomorphsa
Carrion
Birds
Reptiles
Amphibians
Insects
Crustaceans
Plant materials
5.4
0.8
84.7
–
9.1
–
–
–
–
–
–
1.3
20.2
2.1
2.2
–
–
52.6
–
21.6
–
1.0
67.6
–
0.8
3.0
7.6
18.6
–
1.4
–
18.4
14.3
17.8
16.7
19.4
6.2
3.7
1.7
–
–
71.8
6.6
–
11.6
2.8
1.9
1.4
0.1
3.4
a
7.8
1.4
74.7
–
16.1
–
–
–
–
–
–
3.5
12.4
38.1
24.8
0.7
–
4.7
–
15.9
–
13.7
20.8
–
4.0
0.5
–
44.8
4.5
11.7
–
23.5
12.3
37
8.8
1.8
5.7
10.3
0.8
–
–
62.4
9.5
–
11.5
–
–
7.0
2.2
7.1
only rabbit (Oryctolagus cuniculus)
Note: diet data before the arrival of RHD were taken from Delibes (1980), Rau (1987), Palomares and Delibes (1991a, b), Martín et al. (1995).
Fig. 4 Trophic guild structure
of carnivore assemblage from
Doñana (SO Spain), after the
arrival of the HRD period. Dotted line at 65% of similarity
indicates the existence of four
guilds (in brackets) with statistical significance (p < 0.05).
Cophenetic correlation = 0.96
fruits in a large proportion. Nevertheless, the consumption
of lagomorphs was high over the year, independently of the
availability of this prey which is scarce during the cold
season (Zapata et al. 2005b). The culpeo is selective in the
consumption of this prey in Patagonia (Johnson and
Franklin 1994; Novaro et al. 2000; Zapata et al. 2005b).
The rest of the species also remained in the same trophic
guild in the two considered seasons. Travaini et al. (1996)
reported the trophic guild structure of a similar carnivore
assemblage from Neuquén province, northwestern Argentinean Patagonia, identifying only three trophic guilds. As in
our study during spring–summer, the lesser grison and
Geoffroys cat (Oncifelis geofroggy) composed the rodent
feeding guild, and the skunk (Conepatus chinga) and the
gray fox composed the arthropod feeding guild. Nevertheless, the puma composed with the culpeo fox the
lagomorphs feeding guild. This difference in the guild
structure between the two assemblages could be due to gaps
in resource space (Pianka 1980; Holling 1992). Ungulates,
maras and pichis, which are important in the diet of puma
in Santa Cruz (Zapata 2005) are ecologically extinct as prey
for pumas in NW Neuquén province (Novaro et al. 2000).
In Doñana, we also identified four trophic guilds, and
like in Patagonia, the same guild structure was present over
the two studied periods with some changes in species
composition. These variations have been related to the
changes in the availability of rabbits, which are a key prey
for some predators of Doñana (Delibes and Hiraldo 1981;
Jaksic and Soriguer 1981). Iberian lynx, common genet,
and the Egyptian mongoose exhibited fidelity to their guild
assignation before and after the arrival of the RHD disease.
The Iberian lynx is so a specialist predator on rabbits
(Delibes 1980; Palomares et al. 2001) that could not survive
without this prey. Ferreras et al. (2004) observed that the
Iberian lynx population from DNP concentrated in areas
where rabbits were still abundant as a response to the
decline of this prey (Ferreras et al. unpublished data). On
the contrary, rabbit is not an important prey in the diet of
the common genet and the Egyptian mongoose in Doñana
(Palomares and Delibes 1991a, b; Palomares 1993) so they
did not show changes in diet composition. The species that
exhibited major changes in diet composition, the badger
and the red fox, changed to other feeding guild. These
findings were previously reported by Travaini (1995).
Before the RHD, the badger preyed mainly on rabbits
(Martín et al. 1995) behaving as an opportunistic feeder on
this abundant resource, besides, the badger is not morphologically specialized for the consumption of rabbits (Zapata
2005). The change to the birds, reptiles, and carrion feeding
guild of the red fox responded to the increase in the
consumption of carrion and birds, overlapping its diet with
that of the Egyptian mongoose. The red fox compensated
the reduction in the availability of rabbits with increasing
the consumption of these prey. Carrion and birds are
abundant in Doñana; in addition, carrion is an important
food item in other sites of DNP (Fedriani 1996).
Comparison of results obtained for both assemblages
as a function of the use of resource base
Mammal prey promoted the formation of three trophic
guilds, both in Patagonia and in Doñana. The guild
“edentates, ungulates”, constituted by the puma in Patagonia, do not have its homologous in Doñana. On one hand,
edentates originate from South America and are absent in
Europe (Redford and Eisenberg 1992), and on the other
xhand, only the Iberian lynx is capable to subdue ungulates,
which are represented in Doñana by three species: red deer
(Cervus elaphus), roe deer (Dama dama), and wild boar
(Sus scrofa), but the frequency of these prey in its diet is
very low (Delibes 1980). The rest of the species consumed
ungulates only as carrion (Fedriani et al. 1999, this study).
In Doñana, ungulates were frequently consumed by wolves
(Canis lupus) before their extinction (Valverde 1984). This
species was not resident in the Park, but wolves visited
Doñana sporadically up to the middle of the last century
until they were exterminated (Mountfort 1958). It is
interesting that the wolf had utilized an abundant resource,
which was underutilized by the rest of the assemblage, and
had constituted a temporary trophic guild based on
the consumption of ungulates. Lagomorphs promoted the
formation of guilds in both assemblages, although the
taxonomic composition of the species that constitute them is
very different in both areas. The lagomorphs feeding guild
based on the consumption of European hare in Patagonia is
constituted by opportunistic species that take advantage of this
introduced species, like the canids and also the lesser grison, a
small mustelid specialized in the consumption of mammals in
Patagonia (Delibes et al. 2003; Zapata et al. 2005a). The
European hare was introduced in the early 1900s (Grigera
and Rapoport 1983), and there is not a specialist predator, in
an evolutionary sense (Futuyma and Moreno 1988), on this
species. On the contrary, it is presumed that the rabbit
(Oryctolagus cuniculus) had a very important role in the
evolution of the Iberian lynx. Both species originated in the
Iberian Peninsula, and there is no doubt that the Iberian lynx
cannot survive without its preferred prey, the rabbit (Delibes
1980; Palomares et al. 2001).
The rodent feeding guild is also present in both
assemblages, but in Patagonia, it is constituted by two
species, the lesser grison and the pampas cat. These species
are morphologically adapted to capture and consume this
prey type (Delibes et al. 2003; Zapata 2005; Zapata et al.
2005a). In Doñana, the rodents feeding guild is constituted
by only one species, the common genet, which dental
pattern is not specialized for the consumption of rodents
(Popowics 2003; Zapata 2005). Besides, rodents are the
resource base for the majority of the carnivores in
Patagonia assemblage (Zapata 2005), whereas in Doñana,
the rabbit is the key species (Delibes and Hiraldo 1981;
Ferrer and Negro 2004). Furthermore, it is remarkable that
rabbits are very abundant and rodents are scarce in Doñana
(Jaksic and Soriguer 1981).
Arthropods and fruits are the base for the formation of a
feeding guild in both assemblages, composed by species of
the same taxonomic origin (canids and mustelids). Finally,
birds and reptiles promote the formation of one guild in
Doñana, which is absent in Patagonia. In Doñana, the
resources are much more diverse than in Patagonia (Jaksic
and Delibes 1987), so it is expected less resource overlap
among carnivore species.
As stated above, arid and semiarid environments like
Patagonia are notorious for the fluctuation of trophic
resources, which affect the ecology of the resident species
(Wiens 1977, 1981, 1993; Korpimäki 1984; Jiménez et al.
1992; Meserve et al. 1995). In these environments, longterm studies have revealed changes in guild structure. These
changes have been explained as the individual responses of
different species to alternate periods of scarcity and
abundance of resources (Wiens 1993). Numerous authors
reported changes in guild structure as a response to periods
of scarcity and abundance of resources, mainly in bird
communities (see Jaksic et al. 1993; López de Casenave
2001 and references therein), rodents (M’Closkey 1976),
lizards (Dunham 1980), and raptors (Jaksic et al. 1991).
Nevertheless, in our study, we did not find changes in
trophic guild structure; the same guilds were present in the
two considered periods, but with seasonal changes in
species composition.
In the same way, dramatic responses of vertebrate
predators to fluctuations in the density of their prey, like
the rabbit in Doñana (after the arrival of the RHD), are
very well known in different parts of the world
(Andersson and Erlinge 1977; O’Donoghue et al. 1977,
1998a, b; Redpath and Thirgood 1999; Fuller and Sievet
2001). In Doñana, despite the great fluctuations in the
abundance of rabbits, the same trophic guilds were present
in the two considered periods, changing their specific
composition.
Carnivore species in both assemblages were resident in
the considered periods. Opportunistic species converged in
the use of resources that were abundant seasonally or
annually, and this convergence promoted changes in guild
composition, whereas specialist species continued utilizing
the same type of resources, despite fluctuations in their
abundance. These results support the hypothesis that guilds
are in part originated by opportunistic convergence of
species on abundant and energetically rewarding resources
(Jaksic et al. 1996; Farías and Jaksic 2004).
Acknowledgement
We thank Carlos Zoratti, Pablo Collavino,
Ernesto Aguilar, and Rolando Martínez Peck for their help during
field work at MNBP. Claudio Chehebar and the Administración de
Parques Nacionales authorized us to work inside the protected area
(MNBP). Local ranchers authorized us to search for feces in their
properties. Funds were provided by the Universidad Nacional de la
Patagonia Austral (P.I. 29/B013, 29/B050), CONICET (PEI 6065), the
Secretaría de Agricultura, Ganadería y Pesca de la Nación (SAGPyA
Nos. 613/96, 716/97 and 925/97), the Secretaría de Medio Ambiente y
Desarrollo Humano, and the Consejo Agrario Provincial. Miguel
Pascual and Julio Lancelotti helped SCZ with randomization
algorithms.
We declare that the material collected for this study comply with the
current laws of Argentina and Spain.
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