Does riparian habitat condition influence mammalian
carnivore abundance in Mediterranean ecosystems?
Hugo M. Matos Æ Maria J. Santos Æ Francisco Palomares Æ
Margarida Santos-Reis
Abstract The severe loss or degradation of riparian habitats has led to their impoverishment and impaired function, which may have severe consequences on both the riparian
habitats themselves and their associated biota, including mammalian carnivores. We
selected 70 riparian habitat reaches to evaluate the condition of the riparian habitats in
southern Portugal and their use by carnivores. These sites were assessed for riparian
condition using the stream visual assessment protocol (SVAP) and surveyed for carnivore
presence along the riparian zones and across the surrounding matrix landscape, both in the
wet (winter) and the dry (summer) season. Results show that carnivore surveys adjacent to
riparian habitats consistently had significantly higher species richness than the matrix
habitats, in both sampling seasons. Carnivore relative abundance and relative abundance of
stone marten, common genet and Egyptian mongoose also showed higher values in riparian
habitats, with significant differences in at least one season. The Eurasian badger, on the
other hand, showed higher relative abundance values in the landscape matrix, though
differences were not significant. The SVAP index ranked about 83% riparian reaches as
poor or fair condition, and species richness was significantly higher in fair condition
reaches during the wet season. These results reflect the importance of riparian habitats in
Mediterranean ecosystems for mammalian carnivores. However, the generalized poor
condition of these habitats suggests that direct measures for riparian restoration could be
appropriate. The preservation or improvement of riparian habitats would certainly benefit
the mammalian carnivore populations and consequently their conservation.
Keywords Mediterranean ecosystems Mesocarnivores Restoration
Riparian corridors Species richness Stream assessment protocol
H. M. Matos (&) M. J. Santos M. Santos-Reis
Centro de Biologia Ambiental/Departamento de Biologia Animal, Faculdade de Ciências,
Universidade de Lisboa, Campo Grande, Edifı́cio C2, 1749-016 Lisbon, Portugal
e-mail: hmmatos@fc.ul.pt
F. Palomares
Departamento de Biologı́a de la Conservación, Estación Biológica de Doñana, CSIC, Avenida de
Maria Luisa s/n, Pabellón del Perú, 41013 Sevilla, Spain
123
Introduction
Riparian habitats are linear landscapes adjacent to inland aquatic systems with recognized
ecological value (Malanson 1993; Naiman et al. 2005), especially when the surrounding
matrix is impoverished due to activities that lead to their fragmentation. In spite of their
recognized importance as ecosystem service providers, riparian habitats are frequently
considered to have small or no direct economic value (Edwards and Abivardi 1998). This
situation has led to severe loss and degradation of these habitats in many European
countries (Tockner and Stanford 2002) without a proper evaluation of its consequences for
the structure and functioning of the broader Mediterranean ecosystems, including carnivore
communities. Although mammalian carnivores can persist in several habitat types, their
characteristic large ranges and low abundances make them highly vulnerable to human
persecution and habitat changes (Noss et al. 1996; Schaller 1996). Though the importance
of pristine oak woodlands for biota is widely recognized (Dı́az et al. 1997; Plieninger and
Wilbrand 2001), agriculture dominates land use in Mediterranean regions causing their loss
and fragmentation and thus hampering their function. Hence, riparian habitats are frequently the only forest and/or scrub habitat for carnivores at a landscape scale (Virgós
2001).
Additionally, Mediterranean regions have a unique combination of hot, dry summers
and cool, humid winters (Blondel and Aronson 1999). These harsh conditions are a
challenge to the mammalian carnivore communities present in these areas, particularly
during the hottest months when many surface water sources dry out and food resources
become scarce. During summer, watercourses with riparian vegetation are frequently the
only places where water can be found, often limited to small pools, making these places
essential for carnivore persistence. They also provide shelter and food, and may function as
travelling corridors that allow biota to disperse, including mammalian carnivores (Beier
1995; Dickson and Beier 2002; Knopf and Samson 1994; Virgós 2001). Therefore, good
models to address the role of the riparian habitat for mammalian carnivores in fragmented
landscapes are needed (Virgós 2001; Hilty and Merenlender 2004).
Riparian habitats can be described in terms of structural, compositional and spatial
parameters. Using a combination of measurements of each of these components, we tested
the hypothesis that a well conserved riparian element should be vital for individual carnivore species fitness, their biodiversity (to higher carnivore species richness and
abundance), and their conservation in Mediterranean ecosystems. We predicted that factors
such as vegetation cover and water availability would have a major importance in determining carnivore use of riparian areas, whereas it was expected that more disturbed
environments (for example with higher manure cover) would be less used, except for
cosmopolitan and synantropic species such as the red fox. We also predicted that the
importance of a well conserved riparian habitat increases when the surrounding matrix is
degraded.
Materials and methods
Study area
The study area (about 6,400 km2) is located in Alentejo, southern Portugal (38°190 1100 N,
8°120 6000 W; Fig. 1). Elevation ranges from 200 m in the west to 400 m in the east, with
some hills reaching 650 m. It has the highest thermal amplitude in the country with a mean
123
Fig. 1 Study area in southern Portugal with the location of the sampling sites: creek sites (triangles,
n = 24), stream sites (circles, n = 24) and river sites (squares, n = 22)
minimum temperature of 5°C and a mean maximum temperature of 33°C. Annual precipitation varies from 800 mm in the northwest to \400 mm in the southeast. Several
watercourses cross the area (Fig. 1) and many of them do not have a permanent water
regime and dry partially or even completely during summer.
The study area is characterized by a mosaic Mediterranean landscape dominated by
extensive agricultural areas (hay, wheat, barley, forage, etc.; 43%) interspersed with different sized patches of cork oak (Quercus suber) and holm oak (Q. ilex) woodlands (38%).
Intensive agricultural areas are the minority (ca. 10%), with the remaining area covered by
urban and rural areas. The cork and holm oak woodlands, called montado, form a unique
agro-silvo-pastoral system that can be found in southern Europe (Dı́az et al. 1997; Scarascia-Mugnozza et al. 2000). The montado supports human activities like cork and wood
extraction, livestock rearing (cattle, sheep and goats), hunting (mainly wild rabbit, Oryctolagus cuniculus and partridge, Alectoris rufa), intensive and traditional agriculture
(including olive groves and vineyards). Human population density, however, is low, rarely
exceeding 25 inhabitants per km2.
Riparian habitats are mainly dominated by white poplar (Populus alba), raywood ash
(Fraxinus angustifolia), grey willow (Salix atrocinerea), African tamarisk (Tamarix africana), oleander (Nerium oleander), alder (Alnus glutinosa), rock-rose (Cistus spp.), and
blackberries (Rubus spp.) (Chı́charo et al. 2001).
123
Data acquisition
From December 2003 to September 2004, we surveyed 70 riparian habitat stretches and
their adjoining landscape matrixes to evaluate their influence on carnivore species richness
(number of different species) and relative abundance (number of signs of presence per
distance walked). The sampling sites were selected using Geographic Information Systems
(GIS) software (ArcGis 9.1, ESRI, California, USA) following a stratified random selection
of the entire landscape according to the watercourse type (creek, stream and river) and the
adjacent matrix (cork oak woodland, holm oak woodland and cereal fields).
Watercourse type was assessed using a layer of the river network in southern Portugal
digitized from 1:25,000 resolution digital topographical maps. The land-cover data was
obtained from available 2000 CORINE land-cover, derived from supervised classification
of Landsat TM 30 m resolution multispectral imagery. This land-cover layer was used to
estimate the study area land-cover proportions as well as within the sampled plots. The
matrix was then determined as the land-cover type that covered [50% of the 2 km sampling plot.
In each of the selected riparian stretches, one 2,000 m transect along the edge of the
riparian habitat (within 5–15 m from the river bank), and two transects of 1,000 m, starting
from the edge of the waterline and going into the landscape matrix, were walked and
searched for carnivore signs of presence. These transects were established along dirt roads,
to assure sign detectability, and to reduce potential detection bias across multiple environments. Transects were surveyed by two experienced observers twice, once in the wet
season (December 2003–March 2004) and once in the dry season (June–September 2004).
Focal carnivore species were the red fox (Vulpes vulpes), the least weasel (Mustela nivalis), the European polecat (Mustela putorius), the stone marten (Martes foina), the
Eurasian badger (Meles meles), the wildcat (Felis silvestris), the common genet (Genetta
genetta), and the Egyptian mongoose (Herpestes ichneumon). Eurasian otter (Lutra lutra)
was excluded from the analysis because of its aquatic-obligate species condition and
therefore having a recognized riparian habitat association (Dunstone and Gorman 1998)
that could lead to data bias. All scats, latrines and footprints observed during surveys were
recorded.
Though this approach is not free from error (Davison et al. 2002; Foran et al. 1997) it
allows a low-cost and easily replicable evaluation of the carnivore richness and relative
abundance, and thus is an adequate approach for studying carnivores at broader scales
(Barea-Azcó n et al. 2006; Kendall et al. 1992; Webbon et al. 2004). Scats were identified
according to their shape, size, odour and location (Beltrán et al. 1991; Lawrence and
Brown 1967). We also considered footprints because of their effectiveness in species
identification (Lawrence and Brown 1967) and the fairly homogenous soil across the study
area (Cardoso et al. 1973). To avoid inflation of results due to the number of footprints in a
track we registered tracks as one sign of presence. Signs of presence were excluded from
further analysis if any doubt persisted.
Spatially correlated data may bias habitat selection inferences (Betts et al. 2006), since
a species presence at one location may affect the probability of detecting presence in a
nearby new location. We used Moran’s I index (Moran 1950) to evaluate potential effects
of transect spatial autocorrelation on species presence data. The index value was then used
to calculate the Moran’s I statistic, which tests the null hypothesis that there is no spatial
autocorrelation through comparison of the I statistic to a normal distribution (Cheng and
Stephens 1989; Epperson and Li 1996). This cross-autocorrelation coefficient measures the
similarity in the spatial patterns of the variables (Fortin et al. 1989) and varies from -1
123
(perfect negative spatial autocorrelation) to 1 (perfect positive spatial autocorrelation),
with values close to 0 representing no spatial autocorrelation. To estimate the threshold
distance at which spatial autocorrelation can be considered negligible, we progressively
increased the neighbourhood distance from a radius of 1,000 to 5,000 m and measured
cumulative Moran’s I index for each radius distances. Spatial autocorrelation was calculated using ROOKCASE Microsoft Excel Add-in (Sawada 1999). Since no significant
spatial autocorrelation was found at distances above 1.5 km we concluded that our data
was not affected by spatial autocorrelation and therefore we could use it for further
analysis.
Assessment protocols that evaluate the condition of the riparian habitats are tools of
recognized importance for effective conservation and management actions, especially in
highly humanized landscapes (Naiman et al. 2005). The SVAP was the chosen method for
evaluating the condition of the surveyed riparian habitat stretches (Bjorkland et al. 2001).
It is a user-friendly and inexpensive approach that gives a quick turnaround of results, with
easily understandable assessment information, and minimal training needed for implementation (Bjorkland et al. 2001). Following this method, 15 traits were measured based
on visual inspection of the physical and biological characteristics of instream and riparian
environments (Table 1) of each riparian habitat stretch. A numerical score was then calculated as the mean value of the analysed traits. Each stretch was then assigned a class of
riparian habitat condition: ‘‘excellent’’ for scores [9.0; ‘‘good’’ when ranging between 7.5
Table 1 Applicability and description of the stream characteristics considered by the SVAP (Bjorkland
et al. 2001)
Applicability
Stream
characteristic
Description
All streams
Channel condition
Identification of structures that may affect the way a stream
naturally works (dikes, levees, canalization, etc.)
Flooding frequency and withdrawals identification
Hydrologic
condition
Riparian zone
Width of the natural vegetation
Bank stability
Streams only
where
applicable
Identification of soil detachment from stream banks and its
movement into the stream
Water appearance Water turbidity, colour and other visual characteristics
Nutrient enrichment Water nutrient enrichment reflected by the types and amounts of
aquatic vegetation present
Barriers to fish
Presence and distance to drop structures, culverts, dams, or
movement
diversions
Instream fish cover Number of cover types that provide physical habitat for fish
Pools
Number and depth of pools present
Invertebrate habitat Types of habitat and cover for insect/invertebrate colonization
Canopy cover
Percentage of water surface shading
Manure presence
Identification of livestock operations or human waste discharges
Salinity
Salinity levels due to anthropogenic sources
Degree to which gravel and cobble substrate are surrounded by
Riffle
fine sediment (macroinvertebrates, fish spawning and egg
embeddedness
incubation habitat)
Macroinvertebrates Identification of the number and macroinvertebrate species
observed
present
123
and 8.9; ‘‘fair’’ when between 6.1 and 7.4; and ‘‘poor’’ for scores \6.0 (Bjorkland et al.
2001).
Statistical analyses
To evaluate if whether differences in species richness, carnivore relative abundance and
species-specific relative abundance between seasons were significant in either the riparian
habitats or the adjacent landscape matrix surveys, the Wilcoxon paired-sample test was
used (Zar 1999).
To assess the effect of watercourse type (creek, stream and river), adjacent landscape
matrix type (cork oak woodland, holm oak woodland or cereal fields), and the SVAP scoring
on the response variables of carnivore richness, relative abundance and species-specific
relative abundance, a three-way ANOVA was performed for each season (Zar 1999). We
included the SVAP score as a predictor variable to understand the importance of a well
conserved riparian habitat. Watercourse type was used as a surrogate for water availability
since it is expected that rivers will maintain water throughout the dry period. Possible
interactions between the predictor variables thought to have higher biological relevance for
the focal species were also evaluated. Hence, the interaction between watercourse type and
the adjacent matrix allowed evaluating whether any particular combination of these two
variables influenced the species richness and/or abundance values. Higher species richness
and/or abundance values were expected to be found in areas with forested matrixes in
combination with rivers, whereas lower values were expected to be found in areas with
cereal matrixes in combination with creeks. The interaction between adjacent matrix and
SVAP was also tested to allow evaluation of whether carnivores respond to changes in
riparian habitat quality by shifting to the adjacent matrix when riparian habitat quality is
low. The interaction between the watercourse type and SVAP was evaluated to elucidate the
effect of quality associated with water availability.
Significance was set at P \ 0.05 for all analyses and the values for relative abundance
were log(y ? 1) transformed in order to meet the homogeneity assumption. All statistical
tests were carried out using SAS/STAT software version 9.1 (SAS Institute Inc., North
Carolina, USA).
Results
All focal species were detected in the study area in both seasons except the wildcat, which
were never recorded. Although detected, the number of weasel and polecat signs of
presence was too low (nweasel = 11, npolecat = 2) to be considered for further analysis.
Moran’s I index results showed no significant spatial autocorrelation at distances above
1.5 km and significance at P \ 0.05 (Ispecies richness = 0.4, Iabundance of all carnivores = 0.1,
Istone marten abundance = 0.3, IEurasian badger abundance = 0.23, IEgyptian mongoose abundance = 0.42,
Ired fox abundance = 0.028, Icommon genet abundance = -0.017) and therefore we concluded that
our data was not affected by spatial autocorrelation and proceeded with further analysis.
A total of 2,245 signs of presence were found. From these, 1,287 were found in the wet
season and 958 in the dry season. Significant differences between seasons were detected
for the values of total carnivore relative abundance in the matrix surveys (Wilcoxon pairedsample test: Z = 2.27, P = 0.01).
The majority of species showed consistently higher relative abundance in riparian
habitats in both seasons (Fig. 2), with the exception of the Eurasian badger. The red fox
123
Fig. 2 Number of signs of presence per km of each species in the riparian habitat and in the adjacent
landscape matrix for the wet (a) and dry (b) seasons; matrix was cork, holm or cereal; * denotes significant
differences at P \ 0.05 using Wilcoxon paired-sample test
also had lower relative abundance in riparian areas surrounded by cereal fields but differences were not significant (Fig. 2). The Egyptian mongoose was the most frequently
detected species and the one that showed the greatest association with riparian habitats
(nriparian = 652, nmatrix = 135), with significant differences between these habitats and all
the landscape matrixes (Fig. 2). The common genet showed significant differences
between the riparian habitat and the cork oak matrix in the wet season, and the holm oak
matrix in the dry season (Fig. 2). The stone marten showed significant differences only
between the riparian habitat and the holm oak matrix in both seasons (Fig. 2). Species
richness values were also significantly higher in riparian habitats in both seasons (Wilcoxon paired-sample test: Zwet = -1.96, P = 0.03; Zdry = 2.03, P = 0.02).
The presence of a forested adjacent matrix (cork or holm oak woodlands) to the riparian
area significantly influenced carnivore richness and relative abundance, especially during
the wet season. Furthermore, this effect was also observed for the Eurasian badger (cork
and holm oak) and the genet (cork oak) in both seasons, and for the stone marten (holm
oak) in the wet season (Table 2). In addition, the combined effect of the adjacent matrix
123
and watercourse type was also significant for relative carnivore abundance in the wet
season, particularly when cork oak woodlands surrounded any watercourse type, but also
when holm oak woodlands surrounded streams and cereal plantations surrounded streams
and creeks. Species also responded to the combined effect of adjacent matrix and watercourse type, such as the common genet and the Egyptian mongoose in the wet season
(Table 2). The common genet was significantly more abundant in cork oak woodlands
surrounding streams and the Egyptian mongoose in cork oak woodlands surrounding
rivers. However, the watercourse type seems to have had a very limited effect on species
richness and relative abundances. In fact, only the red fox showed significant differences
among the relative abundance values found in the different watercourse types in the wet
season (Table 2), with higher values recorded in the river transects.
According to the SVAP, no site was considered as being in ‘‘excellent’’ condition and
only 17% of the surveyed riparian stretches were classified as being in ‘‘good’’ condition.
The majority of the sites were classified as being in ‘‘fair’’ condition (53%) and 30% were
classified as ‘‘poor’’ (Table 3). Rivers seemed to be in better condition than any other
watercourse type with 36% of them classified as ‘‘good’’ (Table 3), whereas creeks showed
the worst condition with no site classified as ‘‘good’’ and 50% classified as ‘‘poor’’
(Table 3). SVAP values were significantly related with species richness in the wet season
(Table 2), with higher values of richness registered in the stretches classified as being in
good and fair condition (average species richnessGOOD = 2.63; average species richnessFAIR = 2.35; average species richnessPOOR = 1.76).
The interaction between the watercourse type and the adjacent matrix resulted in significant differences for total carnivore, common genet and Egyptian mongoose relative
abundances in the wet season (Table 2). In all cases, this was due to the higher values
recorded in transects surveyed along rivers with adjacent cork oak. In the dry season, this
interaction did not have a significant effect on species richness or carnivore relative
abundance.
Finally, the interaction among SVAP values and adjacent matrix and among SVAP
values and watercourse type also revealed modest influence, with the first
(SVAP 9 adjacent matrix) being significantly different for the stone marten and the second (SVAP 9 watercourse type) for the red fox in the dry season. The stone marten was
significantly more abundant in fair condition riparian habitats surrounded by holm oak
woodlands and cereal. The red fox was significantly more abundant in streams and rivers
with either good or poor condition riparian habitats. In the wet season only the interaction
between SVAP values and watercourse type resulted in significant differences for the
Eurasian badger abundance, with higher badger abundances in poor quality streams.
Discussion
Riparian habitats in the Mediterranean ecosystems of southern Portugal showed an
extensive state of degradation. In spite of this, they still seem to play an important role as
carnivore habitat and thus in these species conservation. Riparian habitats consistently
recorded higher species richness values and higher relative abundances of the majority of
species that their adjacent landscape matrix. This may have to be interpreted with some
caution, however, due to the fact that the persistence of footprints may be dependent on
environmental conditions (Wilson and Delahay 2001). But given the trade-off between
introducing some bias due to the inclusion of footprints and that of having false absences,
we preferred to increase the amount of available information and include the footprint data.
123
Season Variables
Wet
Dry
Species richness
All carnivores
Red fox
Stone marten
Eurasian badger
Common genet
Egyptian mongoose
F
P
F
P
F
P
F
P
F
P
F
P
F
P
0.39
0.00*
0.01*
0.14
0.53
0.21
0.58
0.29
0.83
0.15
0.19
0.07
0.92
4.94
4.08
6.10
0.48
0.30
0.42
0.39
0.13
1.27
2.64
2.79
0.34
0.03*
0.05
0.02*
0.49
0.58
0.52
0.54
0.72
0.26
0.11
0.10
5.25
0.41
2.79
2.94
0.08
1.14
0.51
2.08
1.69
1.14
9.00
1.80
0.02*
0.52
0.10
0.09
0.78
0.29
0.48
0.15
0.20
0.29
0.00*
0.18
0.75
4.68
2.52
0.00
1.37
0.20
0.98
1.19
2.80
0.43
0.20
5.27
0.39
0.03*
0.12
0.95
0.24
0.65
0.32
0.28
0.10
0.51
0.66
0.02*
0.02
7.29
1.14
2.62
5.04
1.58
0.36
8.51
1.49
0.31
0.30
3.84
0.88
0.01*
0.29
0.11
0.03*
0.21
0.55
0.00*
0.23
0.58
0.59
0.05
0.62
18.44
2.80
5.96
0.10
2.44
0.66
6.17
1.23
0.34
1.41
0.37
0.43
0.00*
0.10
0.02*
0.75
0.12
0.42
0.01*
0.27
0.56
0.24
0.54
0.16
0.98
1.34
5.99
0.29
0.15
0.01
2.99
0.32
0.65
1.16
0.27
0.69
0.32
0.25
0.02*
0.59
0.70
0.92
0.09
0.58
0.42
0.28
0.61
Watercourse type
0.75
Adjacent matrix
12.77
SVAP score
7.59
Watercourse type 9 adjacent matrix 2.22
Watercourse type 9 SVAP
0.39
Adjacent matrix 9 SVAP
1.60
Watercourse type
0.30
Adjacent matrix
1.12
SVAP score
0.05
Watercourse type 9 adjacent matrix 2.10
Watercourse type 9 SVAP
1.76
Adjacent matrix 9 SVAP
3.29
Biodivers Conserv (2009) 18:373–386
Table 2 Three-way ANOVA results for the wet and dry seasons showing the F-value (F) and the P-value (P) for species richness, total carnivore relative abundance (all
carnivores) and the relative abundance of each of the analysed species according to each of the analysed variables and interactions
* Denotes significant differences at P \ 0.05
381
123
382
Biodivers Conserv (2009) 18:373–386
Table 3 Classification of the surveyed riparian stretches, per watercourse type, according to the SVAP
procedure
SVAP classification
River
Stream
Creek
Total
Excellent
Good
Fair
Poor
0
36
41
23
0
17
67
17
0
0
50
50
0
17
53
30
Results in percentage; ‘‘Excellent’’ if score [9.0; ‘‘Good’’ when ranging between 7.5 and 8.9; ‘‘Fair’’ when
between 6.1 and 7.4; and ‘‘Poor’’ if \6.0
Nonetheless, the results seem to confirm the importance of riparian habitats as resource
providers and travelling corridors as been found in previous studies (Beier 1995; Dickson
and Beier 2002; Knopf and Samson 1994; Virgó s 2001). They are also regarded as being
responsible for maintaining high biodiversity (Naiman et al. 2005) which is supported by
our results. Our findings are also similar to other studies that found higher species richness
in riparian habitats than in the surrounding matrix when analysing these habitats in
comparable Mediterranean ecosystems (Hilty and Merenlender 2004; Virgó s 2001). The
importance of the riparian habitat condition is also reinforced by higher species richness
values being related with riparian habitats in good condition. When in poor condition the
role of the riparian habitat as a food provider is affected or potentially lost due to a
decrease in carnivore prey (Maisonneuve and Rioux 2001). Despite of the impoverished
condition of the riparian habitat found in our study area, they still function as resource
providers for carnivores once their productivity seems to exceed that of the surrounding
landscape matrix. An evaluation of the small mammal abundance in the study area showed
that riparian habitats had values eleven times higher than the adjacent cork oak woodland
in spring (P. Pinheiro, unpublished data). This higher productivity was already identified in
studies that analysed riparian areas crossing shrublands, desert scrubs, or savanna grasslands matrixes (Malanson 1993). The discrepancy between impoverished habitats and
those that provide resources is even more emphasized in the summer when fundamental
resources for carnivores can be extremely scarce, especially water. Many water sources dry
out in this period with riparian habitats being one of the rare places where water is retained.
Frequently the water is only preserved in pools but these, nevertheless, make riparian
habitats invaluable for carnivore survival in drought periods.
The Egyptian mongoose is the species that best illustrates the importance of riparian
habitats for the carnivore community. This species has shown a strong association with
riparian habitats in all landscape matrixes and for the full duration of this study. This result
can be attributed to its foraging behaviour, but also to its recognized reluctance to move in
open areas (Palomares and Delibes 1993), especially because this is the only species with
marked diurnal behaviour. It also showed a strong association with rivers embedded in
cork oak woodland in the wet season. In general, rivers showed a better condition than
other watercourse types and the wet season includes the initial spring period when small
mammals’ abundance in riparian habitats reached a peak (P. Pinheiro, unpublished data).
Given this, the higher abundance of this species in these circumstances may be explained
by the search for food in areas with great resource productivity. This result agrees with its
opportunistic feeding behaviour since the Egyptian mongoose prefers the prey that are
more abundant and readily available (Palomares 1993). The common genet has also shown
an important association with riparian habitats in both seasons and with forested areas. This
123
Biodivers Conserv (2009) 18:373–386
383
can be attributable to its preference for hollow trees as resting sites (Palomares and Delibes
1994; Santos-Reis et al. 2004) and where the genet can find the wood mouse (Apodemus
sylvaticus), its main prey (Palomares and Delibes 1994; Rosalino and Santos-Reis 2002;
Virgó s and Casanovas 1997) as well as cray-fish in the summer (Santos et al. 2007). It also
showed a strong association with streams embedded in cork oak woodland in the wet
season, which may be attributable to the small mammal abundance peak verified in this
period in riparian areas, with the forested area offering plenty of their favourite refuges
(Palomares and Delibes 1994; Santos-Reis et al. 2004). Other studies point out the thermophilic tendencies of this species (Virgó s 2001; Virgó s and Casanovas 1997), especially
in periods of high temperatures, which may explain its association with riparian habitats in
the dry period. Stone martens showed a strong association with riparian habitats, especially
when embedded in holm oak woodlands. During the wet season, the holm oak woodlands
were even the preferred areas for the stone marten, revealing the importance of forested
areas for this species. These results seem to confirm the findings in rural areas of this and
other Mediterranean ecosystems, where the stone marten home ranges contained a high
proportion of wood and scrub vegetation, and a high proportion of watercourses in relation
to its availability (Rondinini and Boitani 2002; Santos-Reis et al. 2004). The dry period
includes the reproductive season and this may explain the increase in its abundance in
cereal crops, since during the reproductive season the stone marten searches for partners to
mate and may change its home range shape and composition (Genovesi et al. 1997;
Posillico et al. 1995). In contrast, the red fox and the Eurasian badger did not show a
significantly higher association with riparian habitats compared to the landscape matrix.
These results are somewhat contrary to a study using radio-tracking that has shown that
Eurasian badgers were associated with riparian habitats, but still with the cork oak
woodland with understorey as its main habitat preference (Rosalino et al. 2004). On the
other hand, Eurasian badgers showed an association with streams of poor condition in the
wet season. Poor condition of streams can be related to high manure cover and in these
conditions high numbers of adult insects (mainly Coleoptera) can be found, especially in
early spring. As such, one possible explanation for the badger presence in these conditions
may be due to the opportunistic consumption of a readily available food source that is also
one of the major food items for badgers in Portugal (Rosalino et al. 2005) especially in the
spring (F. Loureiro, unpublished data). As for the red fox, results seem to confirm its
behavioural plasticity (Goldyn et al. 2003; Lloyd 1980), occurring in all habitats without
showing higher activity in any of them. The only exception to this is its association with
creeks in poor condition in the dry season, which may be attributable to juvenile dispersion
in this period, forced to use sub-optimal habitat until the establishment of their territories.
The overall results of this study support the initial prediction that riparian habitats are
critical landscape elements for carnivore conservation in fragmented landscapes, but the
importance of the adjacent landscape matrix was also demonstrated. Our results indicate
that, at least in the wet season, the cork oak matrix recorded significantly higher values of
species richness, total carnivore abundance, and also abundance of the majority of species.
This suggests that not only a riparian habitat in good condition is important for carnivores
but that an associated forested matrix may be important as well. The large importance of a
well conserved riparian habitat is not reduced by the importance of the adjacent forested
area; instead, it seems to point out that a well conserved riparian habitat may be complemented with the adjacent landscape, which is similar to findings in Italy (Rondinini and
Boitani 2002). One possible explanation may be the search for shelter in critical periods for
these species, such as during the breeding season. In these periods females search for
shelters that provide sufficient protection for their litters which are easier to find in forested
123
384
Biodivers Conserv (2009) 18:373–386
areas. On the other hand, the type of watercourse does not seem to be relevant as long as it
is able to provide the essential resources.
The assessment of the condition of riparian habitats and potential recovery from an
impoverished state is also a key issue and challenge in the conservation of Mediterranean
ecosystems. The significant relation between the SVAP scoring and species richness,
though only verified in the wet season, indicates that this visual assessment may represent a
valid tool to evaluate the condition of the riparian habitat for mammalian carnivores. Given
these results, the preservation or even restoration of riparian habitats in the Mediterranean
ecosystems would certainly benefit the mammalian carnivore community and consequently
their conservation.
Acknowledgements We thank Luı́s Miguel Rosalino and Ana Rita Alves for their help in the field work.
We also thank the financial support from the Fundação para a Ciência e a Tecnologia (FCT, SFRH/BD/
10599/2002, POCTI/MGS/47435/2002). We also thank Francis Bozzolo for the English revision.
References
Barea-Azcón JM, Virgós E, Ballesteros-Duperó n E, Moleón M, Chirosa M (2006) Surveying carnivores at
large spatial scales: a comparison of four broad-applied methods. Biodivers Conserv 16:1213–1230.
doi:10.1007/s10531-006-9114-x
Beier P (1995) Dispersal of juvenile cougars in fragmented habitat. J Wildl Manage 59:228–237. doi:
10.2307/3808935
Beltrán JF, Delibes M, Rau JR (1991) Methods of censusing red fox (Vulpes vulpes) populations. Hystrix
3:199–214
Betts MG, Diamond AW, Forbes GJ, Villard M-A, Gunn JS (2006) The importance of spatial autocorrelation, extent and resolution in predicting forest bird occurrence. Ecol Modell 191:197–224. doi:
10.1016/j.ecolmodel.2005.04.027
Bjorkland R, Pringle CM, Newton B (2001) A stream visual assessment protocol (SVAP) for riparian
landowners. Environ Monit Assess 68:99–125. doi:10.1023/A:1010743124570
Blondel J, Aronson J (1999) Biology and wildlife of the Mediterranean region. Oxford University Press,
Oxford
Cardoso JC, Bessa MT, Marado MB (1973) Carta de Solos de Portugal (1:1 000 000). Agronomia Lusitana
33:481
Cheng RCH, Stephens MA (1989) A goodness-of-fit test using Moran’s statistic with estimated parameters.
Biometrika 76:385–392. doi:10.1093/biomet/76.2.385
Chı́charo MA, Chı́charo LM, Galvão H, Barbosa A, Marques MH, Andrade JP et al (2001) Status of the
Guadiana estuary (south Portugal) during 1996–1998: an ecohydrological approach. Aquat Ecosyst
Health Manage 4:73–89. doi:10.1080/146349801753569298
Davison A, Birks JDS, Brookes RC, Braithwaite TC, Messenger JE (2002) On the origin of faeces: morphological versus molecular methods for surveying rare carnivores from their scats. J Zool 257:141–
143. doi:10.1017/S0952836902000730
Dı́az M, Campos P, Pulido FJ (1997) The Spanish dehesas: a diversity in land-use and wildlife. In: Pain DJ,
Pienkowski MW (eds) Farming and birds in Europe: the common agricultural policy and its implications for bird conservation. Academic Press, London, pp 178–209
Dickson BG, Beier P (2002) Home-range and habitat selection by adult cougars in southern California.
J Wildl Manage 66:1235–1245. doi:10.2307/3802956
Dunstone N, Gorman ML (eds) (1998) Behaviour and ecology of riparian mammals. Cambridge University
Press, Cambridge, 408 pp
Edwards PJ, Abivardi C (1998) The value of biodiversity: where ecology and economy blend. Biol Conserv
83:239–246. doi:10.1016/S0006-3207(97)00141-9
Epperson BK, Li T (1996) Measurement of genetic structure within populations using Moran’s spatial
autocorrelation statistics. Proc Natl Acad Sci USA 93:10528–10532. doi:10.1073/pnas.93.19.10528
Foran DR, Crooks KR, Minta SC (1997) Species identification from scat: an unambiguous genetic method.
Wildl Soc Bull 25:835–839
Fortin M-J, Drapeau P, Legendre P (1989) Spatial autocorrelation and sampling design in plant ecology.
Plant Ecol 83:209–222. doi:10.1007/BF00031693
123
Biodivers Conserv (2009) 18:373–386
385
Genovesi P, Sinibaldi I, Boitani L (1997) Spacing patterns and territoriality of the stone marten. Can J Zool
75:1966–1971. doi:10.1139/z97-828
Goldyn B, Hromada M, Surmacki A, Tryjanowski P (2003) Habitat use and diet of the red fox Vulpes vulpes
in an agricultural landscape in Poland. Zeitschrift für Jagdwissenschaft 49:191–200
Hilty JA, Merenlender AM (2004) Use of riparian corridors and vineyards by mammalian predators in
northern California. Conserv Biol 18:126–135. doi:10.1111/j.1523-1739.2004.00225.x
Kendall KC, Metzgar LH, Patterson DA, Steele BM (1992) Power of sign surveys to monitor population
trends. Ecol Appl 2:422–430. doi:10.2307/1941877
Knopf FL, Samson FB (1994) Scale perspectives on Avian diversity in western riparian ecosystems.
Conserv Biol 8:669–676. doi:10.1046/j.1523-1739.1994.08030669.x
Lawrence MJ, Brown RW (1967) Mammals of Britain, their tracks, trails and signs. Blandford, London
Lloyd HG (1980) The red fox. Batsford, London
Maisonneuve C, Rioux S (2001) Importance of riparian habitats for small mammal and herpetofaunal
communities in agricultural landscapes of southern Québec. Agric Ecosyst Environ 83:165–175. doi:
10.1016/S0167-8809(00)00259-0
Malanson GP (1993) Riparian landscapes. Cambridge University Press, Cambrige
Moran PAP (1950) Notes on continuous stochastic phenomena. Biometrika 37:17–23
Naiman RJ, Décamps H, McClain ME (2005) Riparia: ecology, conservation, and management of
streamside communities. Elsevier, Burlington
Noss RF, Quigley HB, Hornocker MG, Merril T, Paquet PC (1996) Conservation biology and carnivore
conservation in the rocky mountains. Conserv Biol 10:949–963. doi:10.1046/j.1523-1739.1996.10040
949.x
Palomares F (1993) Opportunistic feeding of the Egyptian mongoose, Herpestes ichneumon, in southwestern
Spain. Revue d’Ecologie (Terre & Vie) 48:295–304
Palomares F, Delibes M (1993) Key habitats for Egyptian mongooses in Donana National Park, southwestern Spain. J Appl Ecol 30:752–758. doi:10.2307/2404253
Palomares F, Delibes M (1994) Spatio-temporal ecology and behavior of European genets in southwestern
Spain. J Mammal 75:714–724. doi:10.2307/1382521
Plieninger T, Wilbrand C (2001) Land use, biodiversity conservation, and rural development in the dehesas
of Cuatro Lugares, Spain. Agrofor Syst 51:23–34. doi:10.1023/A:1006462104555
Posillico M, Serafini P, Lovari S (1995) Activity patterns of the stone marten Martes foina Erxleben, 1777,
in relation to some environmental factors. Hystrix 7:79–97
Rondinini C, Boitani L (2002) Habitat use by beech martens in a fragmented landscape. Ecography 25:257–
264. doi:10.1034/j.1600-0587.2002.250301.x
Rosalino LM, Santos-Reis M (2002) Feeding habits of the common genet Genetta genetta (Carnivora:
Viverridae) in a semi-natural landscape of central Portugal. Mammalia 66:195–205
Rosalino LM, Macdonald DW, Santos-Reis M (2004) Spatial structure and land cover use in a low density
Mediterranean population of Eurasian badgers. Can J Zool 83:1493–1502. doi:10.1139/z04-130
Rosalino LM, Loureiro F, Macdonald DW, Santos-Reis M (2005) Dietary shifts of the badger Meles meles
in Mediterranean woodlands: an opportunistic forager with seasonal specialisms. Mamm Biol 70:12–
23. doi:10.1078/1616-5047-00172
Santos MJ, Pinto BM, Santos-Reis M (2007) Trophic niche partitioning between two native and two exotic
carnivores in SW Portugal. Web Ecol 7:53–62
Santos-Reis M, Santos MJ, Lourenço S, Marques JT, Pereira I, Pinto B (2004) Relationships between stone
martens, genets and cork oak woodlands in Portugal. In: Harrison DJ, Fuller AK, Proulx G (eds)
Martens and fishers (Martes) in human-altered environments an international perspective. Springer,
New York, 279 pp
Sawada M (1999) ROOKCASE: an excel 97/2000 visual basic (VB) add-in for exploring global and local
spatial autocorrelation. Bull Ecol Soc Am 80:231–234. doi:10.1890/0012-9623(1999)080[0231:
TT]2.0.CO;2
Scarascia-Mugnozza G, Oswald H, Piussi P, Radoglou K (2000) Forests of the Mediterranean region: gaps
in knowledge and research needs. For Ecol Manage 132:97–109. doi:10.1016/S0378-1127(00)00383-2
Schaller GB (1996) Introduction: carnivores and conservation biology. In: Gittleman JL (ed) Carnivore
behaviour, ecology and evolution. Cornell University Press, Ithaca, pp 1–10
Tockner K, Stanford JA (2002) Riverine flood plains: present state and future trends. Environ Conserv
29:308–330. doi:10.1017/S037689290200022X
Virgós E (2001) Relative value of riparian woodlands in landscapes with different forest cover for mediumsized Iberian carnivores. Biodivers Conserv 10:1039–1049. doi:10.1023/A:1016684428664
Virgós E, Casanovas JG (1997) Habitat selection of genet Genetta genetta in the mountains of central Spain.
Acta Theriol (Warsz) 42:169–177
123
386
Biodivers Conserv (2009) 18:373–386
Webbon CC, Baker PJ, Harris S (2004) Faecal density counts for monitoring changes in red fox numbers in
rural Britain. J Appl Ecol 41:768–779. doi:10.1111/j.0021-8901.2004.00930.x
Wilson GJ, Delahay RJ (2001) A review of methods to estimate the abundance of terrestrial carnivores using
field signs and observation. Wildl Res 28:151–164. doi:10.1071/WR00033
Zar JH (1999) Biostatistical analysis. Prentice Hall, Upper Saddle River
123