.
Does size matter? Relating consumed prey sizes and diet
composition of otters in South Iberian coastal streams
Miguel CLAVERO, José PRENDA and Miguel DELIBES
Clavero M., Prenda J. and Delibes M. 2007. Does size matter? Relating
consumed prey sizes and diet composition of otters in South Iberian coastal
streams. Acta Theriologica 52: 37—44,
We analysed seasonal changes in the sizes of prey [grey mullets (Mugilidae), flatfish (Soleidae), eelAaguilla anguilla and crayfish Frocarnbarus clarku] consumed by otters Lutra lutra Linnaeus, 1758 in a Mediterranean-climate coastal area and relate them to the frequencies of occurrence of each
prey species in otter diet. The sizes of over 1500 otter prey were estimated
from measurements of key pieces found in 814 otter spraints, which were collected in lower stream stretches in a sandy coastal area. Clear relationships
between mean prey size and frequency of occurrence were observed for the
four prey types. These relationships were positive for grey mullets, flatfish
and crayfish (ie they occurred more in otter diet when more large individuals
were predated), but was negative in the case of eels. Results suggest that these patterns could be related to seasonal changes in habitat use. Previous
works in the study area showed that otter concentrate its predation efforts in
freshwater stream stretches during spring and summer, when more and larger crayfish are available. Freshwater stretches have neither grey mullets nor
flatfish, while eels are larger and scarcer there than near streams’ mouths,
where crayfish is absent.
Institut d’Ecclogia Aquttiea, Universitat de Girona, Facultat de Cincies, Campus MoatiLivi,
17071 Girona, Spain, e-mail: miguel.clavero@udg.es (MC); ]Jepartamento de BiuLogia Ambiental y
SaLad Ptlbliea, Universidad de Huelva. Campus Universitario de El Carmen, Avda, Andalucia s/n,
21071 Huelva, Spain (JP); Departamento de Biologia Aplicada. EstaciOn Biológica de Doriana.
CSIC. Pabellon del Peril, Avda. Maria Luisa s/n, 41013 Sevilla, Spain (MD)
Key words: Lutra lutra, predation, prey selection, estuaries, Mediterranean
streams, fish, human disturbance
centrate their foraging efforts on it (Stephens
and Krebs 1986). Fluctuations of prey availability across space and time are often reflected in
spatial changes in predators’ diet composition
and seasonal or inter-annual prey shifts, respectively. Moreover, if those fluctuations occur both
spatially and temporally, the predator’s responses could also involve changes in habitat
Introduction
Foraging theory predicts that opportunist
predators’ diet composition would change following changes in the availability of main prey
types, ie whenever an important prey type becomes abundant, predators are expected to con[37]
M. Clavero et at.
use. However, changes in habitat use can also be
forced by factors not related to trophic resources,
such as the level of human disturbance (Riffell et
at. 1996, Taylor and Knight 2003, Bdchet et at.
2004). The coastal line is probably one of the
most disturbed environments due to human activities, especially in the case of sand beaches,
which are heavily used by tourists (James 2000,
Lafferty 2001). For species that are facultative
users of the coastal line, these human disturbances could produce changes in habitat use
(eg avoidance of the coast when there are high
disturbance levels) that should imply dietary
changes.
The otter Lutra lutra Linnaeus, 1758 is a
semi-aquatic predator that obtains virtually all
its food in the water and can occupy a wide range
of aquatic environments, including coastal ones
(Kruuk 1995, Chanin 2003). In previous works
(Clavero et at. 2004, 2005a, 2006) we analysed
spatial and seasonal changes in otter diet composition and habitat use in a coastal area in the
southern Iberian Peninsula. In sandy coastal areas otter diet showed clear seasonal fluctuations, being based mostly on freshwater prey in
summer, while in autumn and winter estuarine
fishes were the dominant prey. Together with
this seasonal variation in diet composition, an
indirect measure of habitat use such as marking
intensity suggested that otters shifted from using mainly coastal areas in autumn winter to exploiting more intensely stream reaches during
spring and summer (Clavero et at. 2006).
The main objective of the present paper is to
analyse the relations of the seasonal changes in
otter diet with the size of consumed prey in a
sandy coastal area. We limited our analysis to
the four main otter prey types in the area: grey
mullets (Mugilidae), flatfish (Soleidae), eel Anguilla cinguitla and red swamp crayfish Procambarus clarkil, which constitute more than 70%
of the occurrences in otter faeces (spraints)
(Clavero et at. 2004). Since our data on prey
availability are hardly comparable, due to environmental heterogeneity in the area and differential detectability of each prey type (see Clavero
et at. 2005b), we limited quantitative prey surveys to eel populations in streams and coastal
areas within the study sector. Some reasons to
study specifically the eel are that it has been often cited as a favourite otter prey (eg Delibes et
at. 2000), it is effectively surveyed using &ke
nets (Jellyman and Graynoth 2005) and it is the
only important otter prey found both in estuarine
and stream stretches within the study area
(Clavero et at. 2005b).
The specific questions related to the general
aim of this paper are: (1) can seasonal changes
in the occurrence of the different prey types be
related to variations in the mean sizes of predated individuals? and (2) could these changes
be reflecting shifts in habitat use?
Study area
The study was carried out in Tarifa (Cddiz, Southern
Spain). The area comprises a coastal band that includes
three main water courses: El Valle, La Jara and La Vega
(Fig. 1). These rivers are very small (only La Jara is longer
than 10 km), thus suffering extreme seasonal changes following the typical Mediterranean climate cycle of autumn-winter floods and summer droughts. The coast is an almost
continnous sandy beach where rivers form small estuaries
with associated marshes. We collected otter spraints in four
600 m long transects located in the lower sections of the
three studied streams (Fig. 1). Two of these transects (numhers 1 and 3 in Fig. 1) were placed close to stream mouths,
while the other two were placed within the streams’ tidal-influenced sections. These tidal-influenced stretches are environmentally different from freshwater stream stretches, in
which flow ceases during summers, and have different fish
communities (Clavero et a?. 2005b). Among otter main prey,
grey mullets and flatfish are exclusive of estuarine and
lower stream stretches, crayfish is found only in freshwater
stream stretches and eel is found in all three aquatic environments. For more information on the study area’s characteristics see Clavero et al. (2004, 2005b).
Methods
Otter diet and eel survey
We studied otter diet through the analysis of spraints.
We collected otter spraints bimonthly from December 1999
to December 2001, although spraint collection could not be
performed in October 2001 due to heavy rains (see Clavero
et a?. 2006). Spraint analysis followed standard procedures,
as described in Clavero et of. (2004). Results regarding diet
composition were expressed as frequency of occurrence fF0,
number of occurrences of a certain prey type divided by
number of spraints analysed) (Mason and Macdonald 1986j.
In order to estimate the original sizes of consumed prey, we
Py
,39
i tt dit
Fig. 1. Map of the study area. Squares represent coastal transects where otter spraints were collected. Eel surveys were performed in coastal transects 1, 2 and 4, as well as in the two stream transects noted by circles.
measured key pieces (mouth hones and vertebrae for fishes
and uropods for crayfish) with a calliper to the nearest 0.1
mm. To estimate original prey length from the size of key
pieces we used the regression equations calculated by
Prenda et a!. (2002) for eels and for grey mullets and regression equations we calculated ourselves (unpublished
data) for crayfish and flatfish. Original length of fish was
estimated as total length, while that of crayfish was estimated as the distance from the tip of the rostrum to the tip
of the telson (Correia 2001).
Spatial patterns in eel density and size structure of eel
populations were studied through passive trapping using
fyke nets (Clavero et a!. 2005bi. Fyke nets were set at night
in five different transects (Fig. 1) and two different mesh
sizes (15 mm and 7 minI were always used in pairs in each
transect. Three of these transects were considered “coastal”
(transects 1, 2 and 4 in Fig. 1), whiLe the other two were
considered “stream” transects. Captured eels were counted,
measured and returned to the water. Eel surveys were performed in March, June and October 2001 and in May 2002.
Statistical
analyses
To analyse FO values, we selected only those transects
and surveys in which at least 10 spraints had been analysed (Table 1). We studied the temporaL variation in the
FOe of the main prey types through one-way ANOVAs, using “month” as factor. In order to homogenise variances, we
arcsine transformed F’O data prior to analyses. Arcsine transformation ensured normality of the data set (Kolmogorov-Smirnov test; p > 0.05 for all four prey types). We performed the same analysis to test for temporal variations in
the mean size of otter prey. The relationships between hi-
Table 1. Number of spraints analysed in the different transects (codes as in Fig. 1) and months and number of
individuals predated by otters whose original length could by estimated.
Number of spraints
February
April
June
August
October
December
Total
Individuals
1
2
3
4
Total
Mullets
Flatfish
Eel
Crayfish
41
89
17
25
18
50
54
42
42
41
29
70
22
7
6
7
32
45
39
41
29
2
22
94
156
129
94
75
101
259
96
32
21
9
59
98
78
19
9
1
43
170
147
79
41
8
80
173
88
76
70
57
21
78
190
278
119
227
814
315
320
528
390
monthly mean TO and mean size of the different prey types
were analysed through Pearson’s correlation analyses.
Eel density was expressed as catch-per-unit-of-effort
(CPUE), measured as individuals per pair of fyke nets (pooling captures for the two nets forming a pair). We analysed
temporal and spatial variations in eel density and eel size
through factorial ANOVAs, in which “month” and “location”
(coastal-stream) were used as factors, CPUE data were log
(x+1) transformed prior to analysis.
Results
Otter diet: frequencies and sizes
Along the study period we analysed 814 otter
spraints and estimated the original sizes of over
1500 individuals belonging to otter’s main prey
types (Table I). The mean FO of grey mullets
calculated averaging FO for each survey and
transect, was 28.6%, while flatfish occurred as a
mean in 27.2% of the spraints, eels in 37.9% and
crayfish in 48.5%. Mean size of predated grey
mullets was estimated to be 164 ± 97 (SD) mm,
mean size of predated flatfish was 138 ± 42 (SD)
mm, that of eels was 215 ± 77 (SD) mm and that
of crayfish 69 ± 21 (SD) mm (Fig. 2)
The frequency of occurrence of the four main
prey types showed significant intra annual variations (grey mullets F5 30 = 2.9, p = 0.03; flatfish
= 3.O,p = 0.02; eel F5,
= 3.4,p = 0.01; and
crayfish F5,30 = 4.3, p = 0.005). The consumption
of the three fish prey types peaked during autumn (October and December surveys), being
minimum in August surveys. Predation on crayfish followed an opposite pattern, penicing in
summer (June and August) and being minimum
along autumn and winter (Fig. 3). Mean sizes of
predated individuals also changed along the
year in the four analysed prey types (grey mullets F5309 = 4.5, p <0.001; flatfish F5,314 = 10.2,
p <0.001; eel F5, 522 = 2.7, p = 0.02: and crayfish
= 59.1, p < 0.001). In this case, the patF5,
terns of variation were similar in grey mullets
and flatfish, otter taking larger individuals in
autumn and winter, but variation in consumed
eel sizes was similar to that of crayfish’s, with
larger individuals being predated in summer
months (Fig. 3).
(a)
(b)
rna
151
1
5
C.)
0
300
>380
<50
100
200
>250
D
0
0
IL-
L
15
10]
0
<100
200
300
>400
Prey size (mm)
Fig. 2. Frequency distributions of the sizes of individuals predated by otters. (a) grey mullets, 30 mm intervals; (b) flatfish 20
mm intervals; (c) eel 25 miii intervals; and (d) crayfIsh 10 mm intervals.
41
Pr.y .ize. and ocounenaei in otter di.t
50 -I
(a)
&_
Oct
.
401
•
Dec
0
LI
1)
304
I
•Aug
150
170
Oct
(Jun
10
130
Feb
201
Apr
110
Dec•
I
I
I
Feb1
20j
Hi90
40 -I (b)
190
•.
Apr
Aug
0t
90 100
zri
120
140
160
0
0
I
Mean prey size (mm)
Fig. 3. Relationships between the mean FOs and the mean size of predated individuals in the months in which otter diet was
analysed (shown by abbreviations). (a) grey mullets r = 0.85, p = 0.03; (b) Ilatfish r = 0.93, p = 0.006; (ci eel r = —0.86, p = 0.03;
and (d) crayfish r = 0.88, p = 0.02.
The bimonthly values of mean FOs and mean
sizes of predated individuals were clearly associated in all four prey types (Fig. 3), though there
were two different and apparently contradictory
380
patterns. High frequencies of grey mullets, flatfish and crayfish consumption occurred in penods in which larger individuals of these three
prey types were consumed. However, larger eel
(a)
C? —
In
CO
340
Iiii
Mar Apr May Jun Jul Aug Sep Oct
Month
Month
Fig. 4. (a) Sizes of eels captured in fyke nets aa a function of transect location and month (location F12
= 170, p < 0001;
month P’3202 = 3.1, p = 0.03; location a month F20 = 0.5, p = 0.69). (b) Catch per unit of effort (CPUE, log (x+1) transformed)
in fyke nets as a function of transect location and month (location F1,133 = 11.2, p = 0.001; month F105 = 2.0, p = 0.12; location
a month F3133 = 2.1, p = 0.10). Open bars represent coastal transects and filled bars stream transects.
42
M. Clavero et
individuals were consumed in those months in
which importance of eel in otter diet was minimal.
Variation in eel densities and sizes
In the four different eel surveys a total of 113
IS’ke net pairs were used (42 in stream transects
and 71 in coastal ones), resulting in the capture
of 210 eels (39 in stream transects and 171 in
coastal ones). Eels captured in stream stretches
were larger than those captured in coastal
transects at any time (Fig. 4a). There was also a
significant effect of month on the size of captured eels, which were larger in March and
smaller in July. Eel density was very different
between stream and coastal transects (Fig. 4b),
with mean CPUE being more than three times
higher in coastal transects (2.3 i. x net pair
as mean) than in stream ones (0.7 i. x net
—1
pair as mean).
Discussion
Otters are often considered opportunistic
predators (Chanin 2003). Though some works
have found selective predation on certain fish
species (eg Beja 1997), the relative contribution
of different fish species or genera is usually
closely correlated with their relative proportions
in the field (Jçdrzejewska et al. 2001). Otters
have been also shown to use intensely some prey
items that are only seasonally available, such as
migrating salmonids (Carss et at. 1990) or reproducing amphibians (Lizana and Pérez-Mellado
1990, Weber 1990). However, it is often difficult
to accurately asses prey availability, and therefore its seasonal changes, since different capture
or censusing methodologies have diverse efficiencies regarding different prey types (eg Beja
1997). In our study area, fyke nets could be effective in surveying eel (Jellyman and Graynoth
2005) and crayfish (Gutiérrez-Yurrita and Montes 1999) populations (though the latter was not
present near the coast), but they were of little
utility for capturing grey mullets or flatfish (eg
Hayes 1989).
In the absence of data on prey availability, it
could be argued that otters would shift to a cert-
at.
am prey item whenever more large individuals
were available in the field, since the exploitation
of these large individuals would become eneTgetically rewarding. This pattern seems clear in the
case of crayfish. In the Iberian Peninsula crayfish is more abundant arid its populations feature relatively more large individuals during
spring and summer, coinciding with high crayfish consumption by otters (Beja 1996a, Correia
2001, Fidalgo et at. 2001). During winter, when
predation on crayfish remains relatively low,
crayfish are less conspicuous due to reduced activity (Correia 1998), and crayfish populations
are composed mainly by juveniles (Correia 1995).
In these conditions it would not be profitable for
otters to concentrate its foraging efforts on crayfish, resulting in the positive relationship between
frequency of occurrence and size of crayfish.
The explanation of the prey frequency-prey
size relationship is not so direct in the case of
flatfish and grey mullets, since the seasonal patterns of availability of these species in Mediterranean estuaries have not been identified as
clearly as that of crayfish in streams. It has been
reported that during autumn and winter populations of some flatfish species in Iberian estuaries
are dominated by large individuals, though
these patterns were not homogeneous across
species (Cabral 2000). Also, there are some grey
mullet species (eg Flathead mullet, Mugil cephalus) that spawn at sea during summer (Cardona
2000, Froese and Pauly 2003), which should result in lower abundances of large individuals in
estuarine areas in this season. Nevertheless,
other species, such as thinlip Liza ramada or
thicklip Cheton tabrosus grey mullets spawn at
sea during winter (Gómez-Caruana and Diaz-Luna 1991, Froese and Pauly 2003), so large,
mature individuals should be available in estuaries during summers.
An alternative explanation to the observed
patterns would be related to the differential
habitat use by otters. Clavero et at. (2006)
showed that otters used the coast less intensively during spring and summer, moving preferentially to stream reaches. In these seasons
otters would forage only occasionally in coastal
areas, therefore disposing of less time to select
certain prey items (eg large-sized individuals).
Prey cizee and occunencea b otter dIet
During winter otters would concentrate their
foraging efforts on coastal areas, being able to
effectively select more profitable prey Ge large
fish). It should be noted that this explanation
does not imply changes in otter diet due to differences in prey availability, but due to a temporal constraint related to changes in habitat use.
The longer the time the otter spent in a certain
habitat, the wider the spectrum of prey choice
there would be.
The negative relationship between eel size
and frequency of occurrence could also be explained by changes in habitat use. The reduction
in eel abundance and the increase of mean eel
size with increasing distance to the sea is a repeatedly reported pattern (eg Thbotson et al.
2002, Laffaielle et al. 2003), also observed in the
study area. Thus, if during spring and sumtner
otters forage more intensively in stream reaches
they would find less dense eel populations, but
larger individuals than foraging in the coast in
winter. These results would also imply that otters would not be especially selective towards
eels as had been previously suggested, neither
in terms of abundance (eg Kruuk 1995, Delibes
et al. 2000), nor in terms of sizes (eg Topping and
Kruuk 1996), since frequency of occurrence and
size of predated individuals changed in concordance with availability in the different exploited
habitats.
Thus, changes in habitat use could potentially largely account for the observed relationships between prey frequencies and prey sizes.
But what could lead otters to these seasonal
changes in habitat use? One possibility is that
otters showed a marked preference for crayfish
in spring and summer, leading to a more intense
use of stream reaches that would imply changes
in the frequencies and consumed sizes of fish
prey (as explained above). Crayfish has been
previously considered a less rewarding prey
than fish, due to reduced energy content and
longer handling times (Beja 1996a). But predators may concentrate foraging efforts on a low
quality prey type, such as crayfish, whenever it
becomes abundant enough to compensate for its
low profitability (eg Noyce et al. 1997). On the
other hand, otters could leave the coast during
spring and summer due to disturbances pro-
43
duced by tourism activities. However, previous
works suggested that otters are not especially
sensible to human disturbances (Mason and
Macdonald 1986, Beja 1996b). In fact, since
tourism is a seasonal phenomena that changes
in parallel with crayfish populations (peaking in
spring summer), our data do not allow us to discriminate if the diet patterns respond to human
disturbances or crayfish availability, or even to
both factors acting synergistically. To investigate this issue, more specific research should be
performed, ideally involving telemetry techniques and investigating the effects of variations in human disturbances, both seasonal and
punctual (ie weekends, holidays), on otter activity and habitat use.
References
Béchet A., Giroux J. F’. and Gauthier Li 2004. The effects of
disturbance on behaviour, habitat use and energy of
spring staging snow geese. Journal of Applied Ecology
41: 689—700.
Beja P. B. 1996a. An analysis on otter Lutra lutra predation
on introduced American crayfish Procambarus clarkii
in Iberian streams. Journal of Applied Ecology 33:
1156—1170.
Beja P. R. 1996b. Temporal and spatial patterns of rest-site
use by four female otters Lutra lutra along the
south-west coast of Portugal. Journal of Zoology, London 239: 741—753.
Baja P. R. 1997. Predation by marine-feeding otters (Lutra
lutra) in south-west Portugal in relation to fluctuating
food resources. Journal of Zoology, London 242: 503—518.
Cabral N. N. 2000. Distribution and abundance patterns of
flatfishes in the Sado estuary, Portugal. Estuaries 53:
351—358.
Cardona L. 2000. Effects of salinity on the habitat selection
and growth performance of Mediterranean flathead
grey mullet Mugil cephalus (Osteichthyes, Mugilidae).
Estuarine, Coastal and Shelf Science 50: 727—737.
Cares D. N., Kruuk H. snd Conroy J. W. H. 1990. Predation
on adult Atlantic salmon, Salmo salar L., by otters, Lutra
lutra (L.), within the River Dee system, Aberdeenshire,
Scotland. Journal of Fish Biology 37: 935—944.
Chanin P. 2003. Ecology of the European Otter. Conserving
Natura 2000 Rivers. Ecology Series No. 10. English Nature, Peterborough: 1—65.
Clavero N., Prenda I and Delibes M. 2004. Influence of
spatial heterogeneity on coastal otter (Lutra lutra) prey
consumption. Annales Zoologici Fennici 41: 551—561.
Clavero at., Prenda S. and Delibes M. 2005a. Amphibian
and reptile consumption by otters (Lutra lutra) in a coastal
44
M. Clavero et at.
area in southern Iberian Peninsula. The Herpetological
Journal 15: 125—131.
Clavero M., Blanco-Garrido F. and Prenda J. 2005b. Fish-habitat relationships and fish conservation in small
coastal streams in southern Spain. Aquatic Conservation: Marine and Freshwater Ecosystems 15: 415—426.
Clavero M., Prenda J. and Delibes hI. 2006. Seasonal use of
coastal resources by otters: comparing sandy and rocky
stretches. Estuarine, Coastal and Shelf Science 66:
387—394.
Correia A. M. 1995. Population dynamics of Procatabarus
clarkii (Crustacea: Decapoda) in Portugal. Freshwater
Crayfish 8: 276—290.
Correia A. hI. 1998. Seasonal and circadian foraging activity of Procambarus clarkii (Decapoda, Cambaridae) in
Portugal, Crustaceana 71: 158—166.
Correia A. M. 2001. Seasonal and interspecific evaluation of
predation by mammals and birds on the introduced
red swamp crayfish Procambarus clarkii (Crustacea,
Cambaridae) in a freshwater marsh (Portugal). Journal
of Zoology, London 255: 533—541.
Delibes M., Ferreras P. and Bldzquez M. C. 2000. Why the
Eurasian Otter (Lutra tiara) leaves a pond? An observational test of some predictions on prey depletion. Revue
d’Ecologie (Terre et Vie) 55: 57—65.
Fidalgo hI. L., Carvalho A. P. and Santos P. 2001. Population dynamics of the red swamp crayfish Procambarus
clarkii (Girard, 1852) from the Aveiro region, Portugal
(Decapodn, Cambaridae). Crustaceana 74: 369—375.
Froese K. and Pauly U. 2003. FishEase: www.flshbase.org
(accessed April 2006).
GOmez-Caruana F. and Diaz-Luna J. U. 1991. Guia de los
peces continentales de la Peninsula Ibdrica. Acción
Divulgativa, Madrid: 1—400.
Gutidrrez-Yurrita P. J. and Montes C. 1999. Bioenergetics
and phenology of reproduction of the introduced red
swamp crayfish, Procambarus clarkii, in Donana National Park, Spain, and implications for species management. Freshwater Biology 42: 561—574.
Hayes J. W. 1989. Comparison between a fine mesh trap
net and five other fishing gears for sampling shallow-lake fish communities in New Zealand. New Zealand Journal of Marine and Freshwater Research 23:
321—324.
Ibbotson A., Smith J., Scarlett P. and Aprahamian M. 2002.
Colonisation of freshwater habitats by the European eel
Anguitlo angu it/a. Freshwater Biology 47: 1696—1706.
James H. J. 2000. From beaches to bench environments:
linking the ecology, human-use and management of
beaches in Australia. Ocean & Coastal Management 43:
495— 514.
Jçdrzejewska B., Sidorovich V. E., Pikulik hI. hI. and
Jçdrzejewski W. 2001. Feeding hnbits of the otter and
the American mink in Bialowieza Primeval Forest (Poland) compared to other Eurasian populations. Ecography 24: 165—180.
Jellyman U. J. aad Ornynoth E. 2005. The use of fyke nets
as a quantitative capture technique for freshwater eels
(Anguilta spp.) in rivers. Fisheries Management and
Ecology 12: 237—247.
Kruuk H. 1995. Wild otters. Predation and populations. Oxford University Press, Oxford: 1—290.
Laffaille P., Feunteun E., Baisez A., Robinet T., Acou A.,
Legault A. and Lek S. 2003. Spatial organisntion of European eel (Anguilta anguilla L.) in a small catchment.
Ecology of Freshwater Fish 12: 254—264.
Lafferty K. D. 2001. Birds at a Southern California beach:
seasonality, habitat use and disturbance by human activity. Biodiversity and Conservation 10: 1949—1962.
Lizana M. and Perez Mellado V. 1990. Depredacion por la
nutria (Lutra lutra) del sapo de la Sierra de Gredos
(Rufo bufo gredosicota). Donana, Acta Vertebrata 17:
109—112.
Mason C. F. and Macdonald S. M. 1986. Otters, ecology and
conservation. Cambridge University Press, Cambridge:
1—236.
Noyce K. V., Kannowski P. B. and Riggs hI. R. 1997. Black
bears as ant-eaters: Seasonal associations between bear
myrmecophagy and ant ecology in north-central Minnesota. Canadian Journal of Zoology 75:1671—1686.
Prenda J., Arenas hI. P., Freitas 0., Santos-Reis M. and
Collares-Pereira lYE. J. 2002. Bone length of Iberian
freshwater fish, as predictor of length and biornass of
prey consumed by piscivores. Limnetica 21: 15—24.
Riffell S. K., Gutzwiller K. J. and Anderson S. H. 1996.
Does repeated human intrusion cause cumulative declines in avian richness and abundance? Ecological Applications 6: 492—505.
Stephens D. W. and Krebs J. H. 1986. Foraging theory.
Monographs in behaviour and ecology. Princeton Universitv Press, Princeton: 1—262.
Taylor A. K and Knight El. L. 2003. Wildlife responses to
recreation and associated visitor perceptions. Ecological
Applications 13: 951—963.
Topping hI. and Kruuk H. 1996. Size selection of prey by
otters, Lutra lutra L.: An experimental approach. Zeitschrift für Saugetierkuncle 61: 376—378.
Weber J. M. 1990. Seasonal exploitation of amphibians by
otters (Lutra tiara) in north-east Scotland. Journal of
Zoology, London 220: 641—651.
Received 12 may 2006, accepted 27 November 2006.
Associate editor was Andrzej Zalewski.