eurasian otters modify their trophic niche after the introduction of non-native prey in...
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INVASION NOTE
Eurasian otters modify their trophic nicheafter the introduction of non-native prey in Mediterraneanfresh waters
Rafael Barrientos • Raquel Merino-Aguirre •
David H. Fletcher • David Almeida
Received: 29 August 2013 / Accepted: 2 December 2013
� Springer Science+Business Media Dordrecht 2013
Abstract Biological invasions are a major driver
behind disturbances in freshwater community struc-
ture. We investigated how the foraging strategy of the
Eurasian otter Lutra lutra (L.) has responded to this
change in a Mediterranean catchment of the Iberian
Peninsula, over a 30-year time span (1980 vs. 2010).
We found that, despite continuing to feed on a
considerable amount of native fish, this carnivore has
adapted its trophic niche to accommodate non-native
species. Prior to the massive introductions of these new
food items (1980), otters diversified their diet during
the limiting season (i.e. summer drought). However,
otters had largely incorporated non-native prey into
their diet in 2010, with red-swamp crayfish being their
main food resource, especially in the summer. This
increased crayfish consumption reflects a narrowing of
trophic niche during the summer drought in 2010. We
discuss how this heavy specialisation may compromise
the conservation of otters and their endemic fish prey.
Keywords Diet � Iberian Peninsula � Invasive
species � Lutra lutra � Red-swamp crayfish �Spraint analysis
Introduction
Inland waters are particularly vulnerable to biological
invasions, with non-native species exerting one of the
main drivers of global environmental change in
freshwater ecosystems (Gherardi 2007). This is of
particular concern in the Mediterranean region of
Europe, where a high level of endemism exists
(Ribeiro and Leunda 2012). Several negative effects
have been described after the introduction of non-
native species in Mediterranean fresh waters, includ-
ing competition, predation, disease transmission and
habitat alteration, with these impacts resulting in
disturbances in community composition and structure
(reviewed in Geiger et al. 2005; Gherardi 2007;
Ribeiro and Leunda 2012). Nonetheless, some studies
have highlighted how non-native species may have
positive effects on native biota (Rodrıguez 2006), for
example by providing alternative prey items to native
species (Delibes and Adrian 1987; Beja 1996; but see
Balestrieri et al. 2013). Indeed, one of the most
significant effects of colonisation by non-native spe-
cies is that it can lead to the reduction or even
R. Barrientos � D. Almeida
Departamento de Ciencias Ambientales, Facultad de
Medio Ambiente, Universidad de Castilla-La Mancha,
45071 Toledo, Spain
R. Merino-Aguirre
Department of Ecology, Complutense University
of Madrid, 28040 Madrid, Spain
D. H. Fletcher � D. Almeida (&)
Centre for Conservation Ecology and Environmental
Change, Bournemouth University, Poole, Dorset BH12
5BB, UK
e-mail: [email protected]
123
Biol Invasions
DOI 10.1007/s10530-013-0622-9
disappearance of native communities (Clavero et al.
2013). Yet, few studies have focused on how native
predators respond to these changes in the pool of
available prey (but see Delibes and Adrian 1987; Beja
1996; Tablado et al. 2010).
The Eurasian otter Lutra lutra (L.) plays a role as
top-predator and consequently is considered a key-
stone species of conservation concern in European
fresh waters (Balestrieri et al. 2013). After the popu-
lation declines observed during the 1950s–1970s, diet
is an essential element for understanding how the otter
is re-colonising its former range in Europe (Copp and
Roche 2003). This carnivore is a generalist predator
and thus displays foraging strategies as adaptive
responses adjusted to the food availability (e.g.
Almeida et al. 2012a, b). In particular, the comparison
between past and current data would offer a crucial
opportunity to study trophic plasticity in otters, within
an historical framework. This could be especially
relevant in Mediterranean Europe, where historic and,
more importantly, high-quality information on otter
diet (e.g. ingested biomass, trophic diversity) is scarce.
One valuable exception is the ‘Montes de Toledo’
mountain range in central Spain, where data are
available after comprehensive seasonal surveys for
otter spraints in the River Bullaque during 1980
(Cuesta 1994).
Native fish species are currently abundant in this
water course (60 % of the total fish and crayfish
available biomass, Almeida et al. 2012a) and conse-
quently, we expect that they are still commonly
predated by otters. Further, Clavero et al. (2003)
suggested that otters may experience variations in
their trophic niche breadth according to the structure
of prey communities. In this sense, Balestrieri et al.
(2013) tested whether non-native fish can provide an
alternative prey to compensate for a decrease in native
fish abundances, thereby modifying the otter niche
breadth; however they found no such a relationship.
The aim of this study was to assess how otters have
responded to the introduction of non-native species in
this Mediterranean catchment of the Iberian Peninsula,
i.e. the River Bullaque. Specifically, we compared the
seasonal changes in the dietary traits of otters after a
30-year time span (i.e. 1980 vs. 2010) to test whether:
(1) native fishes are still important in otter diet, as non-
native prey form the bulk of otter diet only where they
have substituted native fish species (see Balestrieri
et al. 2013 for a review); (2) there is a foraging shift to
predate on crayfish, especially during the dry season
(Delibes and Adrian 1987; Beja 1996); and (3) there is
a relationship between trophic diversity and trophic
breadth with the predation of non-native prey.
Materials and methods
The surveys were carried out in the River Bullaque
(94 km length, 550–620 m.a.s.l.), a tributary to the
River Guadiana (central Spain), which comprises a
catchment area of 1019 km2 (latitudinal range
39�0202800–39�2705100N; longitudinal range 4�1204400–4�2503500W). Limnological features and biological
communities of the study area have previously been
described in Almeida et al. (2012a). Specifically
regarding non-native species present in the study area
(see ‘‘Appendix’’), red-swamp crayfish Procambarus
clarkii (Girard) was introduced into the Iberian Penin-
sula in the early 1970s for aquaculture purposes,
although it was not detected in the study area until
mid-1980s. Eastern mosquitofish Gambusia holbrooki
(Girard) was introduced in the 1920s to control the
malaria carrying mosquito and is currently widespread
throughout the Iberian Peninsula, including the present
study area. Northern pike Esox lucius L. and largemouth
bass Micropterus salmoides (Lacepede) were intro-
duced in the 1950s for recreational angling. These two
piscivorous species have been present in reaches of the
River Guadiana next to the study area since their first
introductions. Common carp Cyprinus carpio L. was
introduced more than 300 years ago for ornamental
purposes and pumpkinseed Lepomis gibbosus (L.) was
introduced at the beginning of the 20th century.
However, common carp and pumpkinseed were only
detected in the study area after 1980, following massive
introductions of these two species, as well as largemouth
bass, in nearby reservoirs (Clavero et al. 2013).
Field sampling and laboratory procedures were
carried out as per Cuesta (1994) and Almeida et al.
(2012a). Otter spraints were seasonally collected from
middle-lower reaches of the River Bullaque (&40 km
of the total river length) in 1980 (n = 532 spraints:
159 spring, 154 summer, 79 autumn, 140 winter) and
2010 (n = 467: 148, 113, 99, 107). Fish and crayfish
were identified to the species level by using diagnostic
structures (i.e. fish bones and crayfish appendages),
which were measured with a digital calliper
(±0.01 mm). Linear regressions between the size of
R. Barrientos et al.
123
diagnostic structures and the body weight were used to
estimate the ingested biomasses for crayfish and fish
species (see Almeida et al. 2012a). Specifically for
crayfish, the estimated body weight was corrected to
avoid including mass from structures rarely consumed
by otters, for example quelipeds of large crayfish
individuals (Almeida 2008; Blanco-Garrido et al.
2008). Mean weights were allocated to the remaining
prey categories (see ‘‘Appendix’’ for other prey taxa
different from fish and crayfish), according to speci-
mens from collections. To permit reliable compari-
sons, all methodological approaches in the field and
the laboratory were kept the same between the study
periods, including spraint collection from similar sites
and meso-habitats (i.e. runs, riffles, pools), identifica-
tion keys and body mass estimations.
We considered ‘main prey’ those constituting at
least 10 % of ingested biomass in any year or season, as
only these food items can be considered as ‘key-
resources’ (Barrientos and Virgos 2006). Ingested
biomasses of the main prey were used to calculate two
dietary indices, the Shannon (H’) and the Levins
(B) indices, and thus to measure the trophic diversity
and the trophic niche breadth, respectively. Chi square
(v2) tests were used to compare the proportions of the
main prey and to study the differences in the
consumption of native fishes (all the species combined)
vs. all non-native fishes plus red-swamp crayfish (with
Yates’ correction for these 2 9 2 matrices) between
years for every season. Statistical analyses were
performed with SPSS v.19 (SYSTAT Software Inc.,
Chicago, USA).
Results
Otters fed predominantly on fish and crayfish, whereas
other prey taxa (i.e. Anura, Colubridae and Birds) only
reached the category of key-resource in some seasons
or years, when fish and crayfish intakes were reduced
(see ‘‘Appendix’’). Otters fed on native prey more
frequently in 1980, except for birds, which were more
important in autumn and winter 2010 (Fig. 1). In 1980,
native fishes were the main prey throughout the year,
particularly in autumn and winter, comprising more
than 85 % of ingested biomass in these seasons (see
‘‘Appendix’’). Conversely, non-native prey were most
commonly utilised in 2010. Specifically, red-swamp
crayfish was the most important food item,
constituting a third of 2010 ingested biomass and
almost half of the ingested biomass during the 2010
spring-summer period (see ‘‘Appendix’’ and Fig. 1).
Largemouth bass was another non-native species
considered as main prey, particularly in autumn and
winter 2010 (see ‘‘Appendix’’ and Fig. 1). Native
fishes represented 18–45 % of ingested biomass in
2010, with the highest value in winter.
Dietary indices illustrated the changes in diet
composition after the introduction of non-native spe-
cies. Trophic diversity was in general slightly higher in
2010 (Table 1), probably due to the availability of
more prey items after the introduction of non-native
species, except for summer, when this index decreased
due to the otter specialisation on crayfish (Fig. 1). This
pattern also applied to niche breadth, which reached
the highest value in summer 1980, but the lowest one in
the same season in 2010 (Table 1). In summer 1980,
otters had to compensate for the decrease in fish
availability with alternative prey (e.g. 11 % of Anura
or 20 % of Colubridae), whereas half of the biomass
intake corresponded to red-swamp crayfish during this
season in 2010 (‘‘Appendix’’ ).
Discussion
Our results suggest that otters displayed clear pisciv-
orous foraging of native species before red-swamp
crayfish and (massive) largemouth bass introductions.
As occurs in other European regions (Balestrieri et al.
2013), native fish are still important after the intro-
duction of non-native species, with only red-swamp
crayfish being an important introduced prey year-
round. However, the lower water temperature pro-
motes a decrease in crayfish activity—and conse-
quently availability—during autumn and winter (Beja
1996), which leads otters to predate more intensively
on largemouth bass and birds as an alternative. Thus,
we found support for our first hypothesis, as ingested
biomass of native fish was important in the 2010 diet
of otters (&30 % year-round), mainly in autumn and
winter, although clearly below the levels from 1980
(&70 %).
Following the introduction of red-swamp crayfish,
this species became a key-resource for otters in our
study area, which mirrors the findings obtained in
other Mediterranean sites (Delibes and Adrian 1987;
Beja 1996). Otters generally prey on a small number of
Eurasian otters and non-native prey in Iberia
123
widespread non-native fish species (Balestrieri et al.
2013), although there is a prompt shift towards preying
on crayfish, especially in summer, as they become
more active and widespread. This is facilitated by the
red-swamp crayfish’s ability to colonise pools and to
survive in these habitats during the dry season
(Delibes and Adrian 1987; Beja 1996), where and
when fish mortality is stronger. Furthermore, despite
crayfish providing lower absolute energy intakes
compared to fish (Beja 1996; Ruiz-Olmo and Jimenez
2009), the cost-benefit ratio of foraging on this
crustacean can be favourable for otters (Almeida
et al. 2012a). Thus, according to the predictions of the
optimal foraging theory (Schoener 1971), otters cur-
rently prefer to feed on crayfish over other prey in
summer, narrowing their trophic diversity and niche
breadth (see also Beja 1996). However, when this prey
was not available (e.g. in 1980), otters broadened their
trophic spectrum and increased their foraging on frogs
and aquatic snakes, which are sub-optimal food items
compared to fish (Clavero et al. 2003; Ruiz-Olmo and
Jimenez 2009). Consequently, despite non-native prey
being virtually absent from the otter diet during 1980,
the use of these non-fish prey (i.e. amphibians and
reptiles) allowed otters to increase their trophic
diversity, as shown elsewhere in the Mediterranean
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% in
gest
ed b
iom
ass
More in 2010
More in 1980
spring summer
autumn winter
NNFC NNFC NF NF
χχχχ2 = 58.85 P < 0.001
χχχχ2 = 61.57 P < 0.001
χχχχ2 = 74.62 P < 0.001
χχχχ2 = 76.72 P < 0.001
χχχχ2 = 40.75 P < 0.001
χχχχ2 = 50.06 P < 0.001
χχχχ2 = 65.16 P < 0.001
χχχχ2 = 69.52 P < 0.001
BI CO AN MS SP SA PC PC SA SP MS AN CO BI
More in 2010
More in 1980
Fig. 1 Percentage of change in the ingested biomass of
Eurasian otter for the main prey categories between 1980 and
2010. Chi square tests and significance levels are shown for each
season. Columns in grey are non-native species. Codes for the
prey categories (from left to right): PC P. clarkii, SA S.
alburnoides, SP S. pyrenaicus, MS M. salmoides; AN Anura, CO
Colubridae, BI Birds, NF Native fishes, NNFC Non-native fishes
and crayfish
Table 1 Dietary indices for trophic diversity (Shannon index, H’) and trophic niche breadth (Levins index, B) of Eurasian otter
between 1980 and 2010
Season Spring Summer Autumn Winter
Dietary index year 1980 2010 1980 2010 1980 2010 1980 2010
H’ 2.83 3.02 3.23 2.59 2.35 3.28 2.28 3.22
B 5.75 4.79 7.82 3.44 3.71 7.23 3.62 7.72
Results are shown by season
R. Barrientos et al.
123
region (Ruiz-Olmo and Palazon 1997; Clavero et al.
2003; see also Schoener 1971), where strong spatial
and temporal water shortages render fish availability
highly unpredictable (Clavero et al. 2003).
Given that otter populations are seasonally food-
limited in Mediterranean habitats (Ruiz-Olmo et al.
2001; Ruiz-Olmo and Jimenez 2009), the high
abundance of red-swamp crayfish during the con-
straining season (i.e. summer drought) can enhance
the occupied area and hence the survival of otters
(Beja 1996). However, despite these apparent bene-
ficial effects of non-native species, future risks for
otters are also possible as a consequence of their new
feeding habits. Whereas otters coped with summer
drought by diversifying their diet in 1980, they
currently concentrate on crayfish predation. Such
heavy specialisation on a single prey species may
compromise the survival of a predator if that prey
suddenly becomes scarce, which is less likely to occur
if the predator has a broad trophic niche. Studies on a
variety of top-predators (e.g. Iberian lynx Lynx
pardinus Temminck or Spanish imperial eagle Aquila
adalberti Brehm) have demonstrated that populations
of predatory species highly specialised on a single
prey can crash if that once super-abundant prey
becomes scarcer due to, for instance, an epidemic
process (Ferrer and Negro 2004). Several examples
from highly specialised otter populations in north-
eastern Spain (reviewed in Ruiz-Olmo and Palazon
1997) demonstrated that this is a real rather than just
theoretical risk for this carnivore. In particular, a
sudden collapse in crayfish populations could be
potentially harmful for otters in typical constrained
habitats of Mediterranean fresh waters, such as
seasonal streams and ponds. These environments
show an overall decline of their native fish assem-
blages in the Iberian Peninsula since the 1980s,
mainly because of the effects of invasive species and
habitat alterations (e.g. Aparicio et al. 2000). More-
over, these habitats are not suitable for non-native
fishes, which are not well adapted to their harsh
environmental conditions (e.g. Almeida et al. 2012a).
Thus, otters may find it difficult to display previous
feeding habits, which included preying on harder to
catch and less ‘profitable’ taxa, such as frogs and
aquatic snakes. In this sense, the maintenance of
healthy native (fish) prey populations is currently
considered a major issue in otter conservation strat-
egies (Beja 1996). Also, the high levels of non-native
prey utilisation by otters may pose a risk of potential
cascade effects occurring in the freshwater food-webs
due to the likely increase in habitat carrying capacity
for this predator (see Beja 1996; Tablado et al. 2010
for some effects after crayfish introductions). For
example, despite the existing belief that the presence
of alternative prey alleviates the predation pressure
from otters on threatened fish species (e.g. the case of
the native crucian carp Carassius carassius (L.) in
England, see Almeida et al. 2012b, 2013), the red-
swamp crayfish may actually impact imperilled
Iberian cyprinid populations of the endemic genus
Pseudochondrostoma via ‘apparent competition’, i.e.
through an increase in the predator population (Holt
1977). In fact, otters currently catch this fish taxon in
the study area, despite its scarcity in the wild
(Almeida 2008).
In conclusion, this paper provides detailed infor-
mation on how otters have adapted their trophic niche
to the spread of non-native species in Mediterranean
fresh waters after a 30-year time span. We found that
otters still preyed upon a considerable amount of
native fishes, but they have also largely incorporated
the red-swamp crayfish into their diet. This species,
which was likely a substitutional prey of fish during
summer drought, has become the main food resource
during the dry period of the year. This information is
relevant to the conservation and management of
Iberian biodiversity and healthy populations of Eur-
asian otters, as heavy specialisation on a single prey
can compromise survival of a predator if that prey
suddenly becomes scarce in the constrained habitats
typical of Mediterranean fresh waters (e.g. Iberian
seasonal streams).
Acknowledgments R.B. received financial assistance from
JCCM-FSE 2007/2013 postdoctoral program and from Juan de
la Cierva program from the Spanish Ministry of
Competitiveness. D.A. held a postdoctoral fellowship from
JCCM-FSE 2009/2011 (PO 2007–13) through the University of
Castilla-La Mancha (Spain).
Appendix
See Table 2.
Eurasian otters and non-native prey in Iberia
123
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Invertebrates
Terrestrial invertebrates \1 \1 \1 \1 \1 \1 \1 \1
aquatic invertebrates \1 \1 2 1 \1 \1 \1 \1
Procambarus clarkii – 41 – 50 – 27 – 18
Fishes
Esox lucius 1 1 9 – – 2 – –
Cyprinus carpio – 2 – – – – – 2
Luciobarbus microcephalus 2 1 6 2 2 2 5 4
Anaecypris hispanica \1 – \1 – \1 – \1 –
Squalius alburnoides 16 9 18 13 36 14 38 21
Squalius pyrenaicus 16 4 14 3 35 7 34 9
Iberochondrostoma lemmingii 6 1 6 2 8 5 3 6
Pseudochondrostoma willkommii 5 \1 6 \1 6 2 8 2
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Salaria fluviatilis – – \1 – \1 – \1 –
Other vertebrates
Anura 24 12 11 12 6 2 6 \1
Geoemydidae \1 – – – – – – –
Lacertidae – 1 – \1 \1 – – –
Colubridae 24 7 20 4 4 5 \1 –
Birds 1 8 5 3 3 13 1 15
Mammalia – \1 \1 – – – – \1
Native fishes 48 18 52 22 86 36 92 45
Non-native fishes and crayfish 1 53 10 56 – 44 – 37
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