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Cent. Eur. J. Biol. • 9(1) • 2014 • 58-69
DOI: 10.2478/s11535-013-0189-y
Central European Journal of Biology
The diet of the spiny-cheek crayfish Orconectes
limosus in the Czech Republic
Research Article
Renata Vojkovská, Ivona Horká*, Zdeněk Ďuriš
University of Ostrava, Faculty of Science,
Department of Biology and Ecology,
710 00 Ostrava, Czech Republic
Received 30 June 2012; Accepted 25 March 2013
Abstract: T hecompositionofthedietoftheinvasivespiny-cheekcrayfishOrconectes limosus was studied using qualitative and quantitative analyses
of stomach contents. A total of 368 specimens collected in 2003–2005 and 2008 in Czech localities were examined, predominantly
fromtheLabe(Elbe)andVltavaRiverbasins.Foodcomponentswerecomparedforthreesizeclassesofcrayfishandbothsexes.The
followingconclusionswerereached:(1)thespiny-cheekcrayfishisanomnivorousspeciesconsumingplants,animalsanddetritus;
(2) quantitatively, the main food component of O. limosusisdetritus,whiletheplantcomponentwassecond;(3)O. limosus may swallow
whole food particles up to 4 mm in size, and the bodies of small animals may sometimes be found undamaged in their stomachs.
Keywords: Crayfish diet • Food particles • Invasive crayfish • Stomach content • Trophic index
© Versita Sp. z o.o.
1. Introduction
The spiny-cheek crayfish, Orconectes limosus
(Rafinesque, 1817), is the most common alien crayfish in
European freshwater ecosystems [1-3]. Characteristics
determining its competitive advantage in comparison
with native species include: an r-strategist life cycle with
faster reproduction and earlier maturation; a greater
tolerance to polluted waters; and the ability to spread
the crayfish plague pathogen, together with its own
resistance to that illness [4].
Crayfish forage on a wide range of foods, including
water macrophytes, algae, detritus and macroinvertebrates [5-7]. Despite being generally omnivorous
animals, different food components may be preferred
in accordance with availability and energetic value [8].
Söderbäck et al. [9] also showed that, in experimental
conditions, crayfish feeding on animal-originated food
grow faster and show higher foraging activity than
those kept on a detrital diet. Feeding selectivity has also
been experimentally documented for food of animal
origin, with crayfish foraging on thin-shelled rather than
thick-shelled mollusks [7], preferring fish eggs to zebra
58
mussels [10], or small and middle-sized mussels and
aquatic gastropods to large ones [11-13].
Being omnivorous throughout their life cycle, crayfish
may prefer different foods in different stages of their life,
with freshly hatched juveniles feeding mainly on animal
plankton and later on benthic invertebrates, while adults
consuming mostly plants and detritus [14,15]. The
selection of plant foods often depends on mechanical
structure, nutritional values, or plant chemical defenses
[7,16-18]. According to Nyström and Strand [19] and
Cronin et al. [18], crayfish prefer newly budding or finely
branching plants to those that are well grown and rigid.
When foraging on submerged and emerged macrophytes,
crayfish may cause changes to deep water environments.
Invasive species, in particular, may negatively affect
aquatic plant density and diversity [19-21].
Alien species compete with native species over
many biological resource aspects, including food
consumption. Despite a fairly wide literature on feeding
of different crayfish species, from which only a limited
review is given above, little data has been reported
on the food and feeding impacts of the invasive spinycheek crayfish. Staszak and Szaniawska [22], as well
* E-mail: [email protected]
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as Anwand and Valentin [23], described O. limosus as
an omnivore. Staszak and Szaniawska [22] noted that,
at higher densities, cannibalistic behavior of spinycheek crayfish frequently occurs. Chiesa et al. [24] also
characterized O. limosus as omnivorous. Based on
qualitative analyses of stomach contents, they divided
these contents into four categories – animal, plant, detrital
and others (the latter containing abiotic components);
the main food item found was of plant origin, followed
by detritus and animal food. Chybowski [25] studied
the foraging of O. limosus in Polish lakes in relation to
diurnal and annual activity. He identified plant material
as the primary food item found in crayfish stomachs,
and stated that annual consumption amounted to only
0.27% of the available aquatic vegetation. Similar results
are presented also by Anwand and Valentin [23] for the
species in Kleiner Döllnsee Lake in Germany. Chucholl
[26] demonstrated the omnivorous feeding habits of the
calico crayfish, Orconectes immunis (Hagen, 1870), a
competitor of O. limosus in the Rhine River, Germany.
The aim of this study is elucidate the diet
composition of the non-indigenous spiny-cheek crayfish
O. limosus in the Czech Republic using qualitative and
quantitative analysis of stomach contents, contributing
to knowledge on the ecology of invasive animals and
to the conservation of native species and natural water
ecosystems.
Figure 1.
2. Experimental Procedures
Qualitative and quantitative analyses of the main and
particular food items were performed for the stomach
contents of 368 spiny-cheek crayfish specimens of
different sizes and sexes, collected in the Labe (Elbe)
and Vltava River basins. Crayfish were collected in 26
localities of the Czech Republic, usually from April to
October, 2003–2005 (Table 1; Figure 1). The material
was originally collected for distributional and biometric
purposes [27,28]. Specimens were caught by hand
during the morning hours and preserved in 70%
ethanol within 2–4 hours. Some additional specimens
were collected from the Prudník Brook, Odra river, NW
Moravian-Silesian region in 2008 [29]. Stomach contents
were analyzed in the laboratory for 368 O. limosus
specimens (212 males and 156 females, including 17
ovigerous females) (Table 2).
Because of low numbers of specimens collected
from particular localities, all the crayfish used in this
study were pooled into one sample, then sexed and
divided into three size classes (S, M, and L) according
to the post-orbital carapace length (POCL), measured
in the dorsal body midline from the level of the posterior
orbital margins to the posterior margin of the carapace
(see [27]: S – up to 13 mm, M – 13–28 mm, L – over
28 mm).
Localities where samples of Orconectes limosus were taken for stomach content analyses.
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Diet of Orconectes limosus
Watercourse / body
Nearest settlement
Latitude (N)
Longitude (E)
Running waters
Labe
Hněvice
50°27’
14°22’
Labe
Kolín
50°02’
15°13’
Labe
(confluence with Farský potok)
Ostrá
50°10’
14°54’
Labe
Litoměřice
50°32’
50°32’
Labe
Malé Březno
50°40’
14°10’
Labe
Nebočady
50°43’
14°11’
Labe
Obříství
50°18’
14°29’
Labe
Poděbrady
50°09’
15°06’
Labe
Štětí
50°27’
14°22’
Labe
Těchlovice
50°42’
14°12’
Labe
Ústí nad Labem
50°39’
14°03’
Labe
(confluence with Luční potok)
Třeboutice
50°31’
14°12’
Cidlina
Libice nad Cidlinou
50°07’
15°11’
Doubrava
Záboří nad Labem
50°01’
15°21’
Jickovický potok
Jickovice
49°27’
14°13’
Jizera
Nový Vestec
50°11’
14°44’
Ohře
Doksany
50°27’
14°09’
Ohře
Bohušovice nad Ohří
50°30’
14°09’
Prudník
Osoblaha
50°17’
17°44’
Vltava
Vrbno u Mělníka
50°19’
14°27’
Barbora (quarry)
Oldřichov u Teplic
50°38’
13°45’
Standing waters
Cítov (sand pit)
Vliněves
50°22’
14°27’
Kojetice (quarry)
Kojetice u Neratovic
50°14’
14°30’
Lhota (sand pit)
sand pit
near the airport Borek
Orlík (reservoir)
Lhota
50°15’
14°40’
Table 1.
Stará Boleslav
50°12’
14°40’
Temešvár
49°21’
14°16’
Geographical details of sampling localities.
Stomach contents were observed using an Arsenal
MBS-10-100 stereomicroscope and Arsenal LS 1001
standard light microscope. The frequency of occurrence
of a particular food item was calculated as a percentage
of the number of analyzed stomachs containing an
actual food item, i.e., excluding empty stomachs. Where
possible, animal remains in stomachs were determined
using identification keys. When not empty, stomachs
mostly contained any of three poorly identifiable
food items – soft animal tissues (e.g., fresh muscles,
fat bodies), plant tissues (fresh, with recognizable
lignified vascular tissues), and detritus (particulate
organic material consisting of minute fragments of
dead organisms exposed for a time among bottom
particles and digested by crayfish immediately from the
substratum), together with more or less recognizable
animal remains (e.g., sclerotized insect heads or legs,
mollusk shells), or plant parts (tree roots).
Stomach fullness was estimated visually in relation
to the potential total volume of a stomach and divided
into five classes: A – empty stomach; B – distinctly
less than half of the volume (e.g., one insect larva or a
low quantity of plant tissues); C and D – partially filled,
around half or distinctly more than half, respectively, of
the stomach volume; E – full stomach.
Based on the presence or absence of distinct food
items, the trophic index „D“ showing the wideness of the
food spectrum [30] was calculated:
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Classes
Size
Qualitative analyzes
Quantitative analyzes
(POCL < 13 mm)
38
2
Medium (POCL 13 – 28 mm)
271
83
Large
59
27
Σ
368
112
Males
212
62
Females
156
50
(included ovigerous females)
(17)
0
Σ
368
112
spring
34
40
summer
237
33
autumn
54
39
Σ
368
112
Small
Sex
Seasons
Table 2.
Parameters
(POCL > 28 mm)
Number of specimens used for qualitative and quantitative analyses of stomach contents.
=
log
where pi is a frequency of occurrence of a distinct
food item, and s is a sum of all food items. According to
Herrera [30] the limit for this index is 0<D<s log N where
N is the size of a sample (here, the number of crayfish
stomachs analysed). The trophic index D is high in
generalist species (the theoretical maximum value is
for species feeding on all food items), and decreases in
specialists which utilize a reduced number of food items
[30].
A representative series of 112 stomach contents
was analyzed for quantitative purposes. Each stomach
content was placed in a distinctly marked area of a dish
(one quarter of the Petri dish, diameter 85 mm) and
photographed with the same magnification (30x) using
the Olympus C-5060 digital camera mounted on the
Olympus SZX7 stereomicroscope.
The image analysis BaDra software (version
1.3, 2009; P. Lukacz, unpublished), was applied to
semiqualitatively evaluate the main food items identified
in the photographs. For quantitative analysis, three
categories were selected: food of animal origin, food of
plant origin, and detritus. The total surface area of all
recognizable particles of these categories, expressed
as a percentage of the whole photograph frame area,
was considered a semi-quantitative parameter of food
item volume.
The Shapiro-Wilk test was used to evaluate
non-parametric quantitative data. The Kruskal-Wallis
one-way analysis of variance [31] was applied as a
non-parametric method to test for the equality of
quantitative contents of main food items among crayfish
groups (based on size classes and sexes).
3. Results
According to the level of stomach fullness, specimens
with mostly empty stomachs (i.e., up to half of its volume)
dominated in most cases, as shown here for crayfish
sexes (Figure 2) and size classes (Figure 3). Almost
identical pattern was also observed by us in specimens
from different water types, and different seasons (for the
latter see Figure 4).
The frequency of occurrence of main qualitative
food items, i.e., plants (79.9%), animals (69.7%), and
detritus (72%), analyzed in 325 crayfish stomachs
(specimens with empty stomachs, i.e. 43 of 368
specimens, were excluded from the analysis), showed
no important differences (Figure 5 – above). However,
the semi-quantitative analysis of the above food items
revealed a different relationship: the detrital component
was found to be the main item (54%) followed by food
of plant origin (38.9%), while there was distinctly less
animal food by volume (6.5%) (Figure 5 – below).
From the distinct food particles in the spinycheek crayfish stomachs (Figure 6, Table 3), the most
frequently occurring that could be identified as having
plant or animal origin were plant remains (65.8%) and
animal tissues (53.2%). Inorganic particles, e.g., sand
(50.2%) were also well represented. Filamentous algae
Cladophora sp. were present in the food in 26.8% of
the studied crayfish. The animal groups occurring
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Diet of Orconectes limosus
Figure 2.
Stomach fullness in sexed specimens of the crayfish Orconectes limosus (x-axis – estimation of the stomach fullness level). Estimated
stomach fullness classes: A, empty stomach; B, low volume (around 10%); C, half volume (30–60%); D, most volume filled (around
75%); E, full stomach.
Figure 3.
Number of Orconectes limosus specimens with different stomach fullness analyzed for three body size classes. S – specimens up to
13 mm POCL; M – specimens of 13–28 mm POCL; L – specimens larger than 28 mm POCL. Stomach fullness classes – see Figure 2.
Figure 4.
Number of Orconectes limosus specimens with different stomach fullness analyzed for seasons. Stomach fullness classes – see
Figure 2.
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Figure 5.
Qualitative (above) and quantitative (below) composition, as percentages, of the main food items in stomachs of the spiny-cheek
crayfish, Orconectes limosus.
Figure 6.
Mean frequencies of the occurrence of main food items in all analyzed stomachs of Orconectes limosus.
most often were chironomid larvae (21.8%), mollusks
(gastropod and bivalve shells – 8.3%) and bryozoans
(statoblasts – 22.2%). Nymphs of Caenis macrura
Stephens, 1835 (Ephemeroptera) (Figure 7), and some
other insect species, were identified as almost intact
specimens. Broken or undamaged shells of gastropods
Ancylus fluviatilis O.F. Müller, 1774, Galba cf. truncatula
(O.F. Müller, 1774), and the bivalve mollusk zebra
mussel Dreissena polymorpha (Pallas, 1771), were also
often present. Food particles of a size up to 4 mm were
often swallowed whole, almost undamaged, by spinycheek crayfish.
Undamaged crayfish eggs were found in the
stomach of one ovigerous female. The size, stage of
development, and color of the eggs were all similar to
the ova from the external egg mass carried by the same
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Diet of Orconectes limosus
crayfish sex
Food components
males
season
females
spring
summer
crayfish size class
autumn
small
medium
large
N
%
N
%
N
%
N
%
N
%
N
%
N
%
N
%
detritus
141
73.1
93
70.5
35
59.3
127
76.0
72
72.7
25
73.5
173
73.0
36
66.7
not-ident.plant remains
140
72.5
74
56.1
43
72.9
111
66.5
60
60.6
18
52.9
160
67.5
36
66.7
not-ident.anim.remains
97
50.3
76
57.6
22
37.3
89
53.3
62
62.6
17
50.0
126
53.2
30
55.6
inorganic particles
96
49.7
67
50.8
27
45.8
85
50.9
51
51.5
14
41.2
122
51.5
27
50.0
filamentous algae
52
26.9
35
26.5
8
13.6
55
32.9
24
24.2
9
26.5
59
24.9
19
35.2
statoblasts Bryozoa
47
24.4
25
18.9
5
8.5
50
29.9
17
17.2
2
5.9
65
27.4
5
9.3
Chironomidae
42
21.8
29
22
7
11.9
40
24.0
24
24.2
8
23.5
53
22.2
10
18.5
plants roots
43
22.3
26
19.7
20
33.9
33
19.8
16
16.2
2
5.9
55
23.2
12
22.2
fatty matter
27
14.0
21
15.9
11
18.6
28
16.8
9
9.1
1
2.9
35
14.8
12
22.2
mollusks
14
7.3
13
9.8
6
10.2
18
10.8
3
3.0
1
2.9
14
5.9
12
22.2
plant seeds
11
5.7
8
6.1
2
3.4
11
6.6
6
6.1
0
0
14
5.9
5
9.3
Cladocera
6
3.1
6
4.5
1
1.7
4
2.4
7
7.1
2
5.9
9
3.8
1
1.9
Coleoptera
4
2.1
3
2.3
0
0
3
1.8
4
4.0
0
0
6
2.5
1
1.9
Ephemeroptera
2
1.0
3
2.3
1
1.7
3
1.8
1
1.0
0
0
1
0.4
4
7.4
Heteroptera
2
1.0
2
1.5
0
0
2
1.2
2
2.0
0
0
3
1.3
1
1.9
Acarina
1
0.5
2
1.5
0
0
3
1.8
0
0
0
0
3
1.3
0
0
Ostracoda
0
0
2
1.5
0
1.7
0
0
0
0
0
0
2
0.8
0
0
Table 3.
Frequency of occurrence of distinct food items in stomachs of Orconectes limosus, listed separately for sexes, seasons and crayfish size
classes.
N – number of stomachs with the presence of a food item; % – percentage of the total number of examined stomachs in the analysis. The
items are presented in predominant descending order. Highlighted grey fields show more important changes in seasonal food items, with the
dominant seasonal food components highlighted black.
female under its abdomen. The detailed qualitative
analyses of stomach contents showed no important
differences in food composition between the sexes,
but there were distinctions found for detritus, plant and
animal food components among seasons (Table 3).
For the quantitative analyses of stomach contents
composition, the main food components (plants,
animals, and detritus) were evaluated by the KruskalWallis test of non-parametric data in relation to crayfish
size classes, sexes, and seasons. The differences
among food components were not significant for
medium and large-sized crayfish. The only significant
relationship was found for detritus between sexes
(P<0.005486).
The trophic index D reflects the relative width of
the food spectrum utilized. For all analyzed crayfish
specimens, this index was 17.7, with a theoretical
maximum 42.7. The index for males was 16.7, and for
females 16.0. For seasons, the D value was 12.9 in
spring, for both summer and autumn was equally 14.9.
The trophic index for standing waters was 17.3, and
13.5 for running waters.
4. Discussion
Most specimens of the spiny-cheek crayfish Orconectes
limosus in this study had stomachs filled up to half their
maximum volume, regardless of sex or size class. In
other studies on the noble crayfish Astacus astacus
(L., 1758) in Europe [32,33] or in Orconectes rusticus
(Girard, 1852) in America [34], a possible relation to
seasons was detected. Chybowski [25] found that
stomachs were frequently empty in Polish specimens of
O. limosus during the January–March period. In Italy,
about 20% of the same species were observed with
empty stomachs in July [24]. In our study, the seasonal
effect of stomach fullness revealed a summer maximum
and the lowest value occurring during the spring period,
while the autumn period is indicated in the latter respect
in Germany [23]. Stomach fullness, however, more
likely depends also on the photoperiod. Lorman [34]
and Chybowski [25] reported higher frequencies of
full stomachs in O. rusticus and O. limosus during the
night. Our results are based on specimens collected
mainly during the morning hours. The digestion of easily
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Figure 7.
Examples of specimens extracted from cardiac stomachs of Orconectes limosus. A, B, well intact mayfly nymphs Caenis macrura.
C, chironomid larvae. D, crushed shell of Dreissena polymorpha. E, bryozoan (Cristatella mucedo) statoblasts. F, shells of Galba cf.
truncatula.
dissociable food components by crayfish up to their
capture, and after that, could partially affect the results.
Food remains, however, are usually present quite long
time in the digestive tract. Chybowski [25], as well as
Reynolds and O´Keefe [35], reported the presence
of food almost 16 and 72 hours after ingestion in
O. limosus and Austropotamobius pallipes (Lereboullet,
1858), respectively.
Qualitatively, the most frequent food component
of O. limosus stomachs in the present study (see
Figure 5 – above) was plant matter (79.9%), but animal
matter and detritus were also present. Plant material
in O. limosus is regarded dominant also by Chybowski
[25], Chiesa et al. [24] and Anwand and Valentin [23].
Lorman [34], studying O. rusticus, noted an increasing
ratio of the plant component as crayfish size increased.
Staszak and Szaniawska [22] found no preference of
O. limosus for plant or animal food items in relation to
water temperature, but stated that crayfish consumed
more food in higher temperature water.
According to distinctly identifiable plant remains and
particles, the most frequent plant food item in O. limosus
were the filamentous algae Cladophora sp. Finely
branching or filamentous plants are known to be preferred
foods in other crayfish species [18,20,36]. Food of animal
origin, mainly benthic invertebrates, is another important
component for crayfish [37,38]. Lorman [34] found that
males and small specimens of O. rusticus feed on animals
to a greater extent than females and larger specimens.
Chiesa et al. [24] supposed that differences in frequency
of the occurrence of animal components between sexes of
O. limosus were due to increased demands on energy for
oogenesis in females. In our study, O. limosus showed no
special preference for animal food. In some distinct cases,
small specimens were found with nothing but one or a few
chironomid larvae in their stomachs.
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Within the present study, the most frequent
identifiable distinct animal components in food
extracted from crayfish stomachs were chironomid
larvae [Insecta: Chironomidae] and ‘moss-animals’
statoblasts [Bryozoa], both occurring in about 22%
of stomachs, mainly in the summer and autumn
periods. Mayfly nymphs [Insecta: Ephemeroptera]
were sometimes found; their bodies were often almost
undamaged when dissected from crayfish stomachs
and well identifiable to species level (Caenis macrura
in most cases). Mayfly nymphs were reported as being
the most frequent animal food for O. rusticus and
O. luteus (Creaser, 1933) in their natural range [37]. In
general, soft bodied animals, including mayfly nymphs
and fish, are more easily digested by crayfish. There
were no food components in our specimens reliably
identifiable as fish parts; however, Taylor and Soucek
[39] point out that the presence of fish in crayfish
stomachs is often underestimated. On the other hand,
hard-shelled remains and particles may be present
for a longer time in the cardiac stomach. In our study,
minute intact gastropod shells, and crushed shells of
the zebra mussel Dreissena polymorpha, were the
most frequent mollusk remains in crayfish stomachs.
This bivalve species is currently widely distributed in
the Labe River and in quarries from which the present
crayfish specimens were collected [40]. Feeding
relations of crayfish of the genus Orconectes to
zebra mussels has been a frequent subject of study
recently [10,41,42]. Crayfish are important predators
of mollusks [12,13,17,20,43]; they prefer to feed on
smaller mollusks, rather than on larger ones [11,12].
Another interesting finding was the presence of
about 10 undamaged eggs in the stomach of one of
the ovigerous O. limosus female examined. Based
on the shape, size, and coloration, these eggs likely
originated from the egg-mass of the same female.
Crayfish females do not eat their own eggs, according
to Nyström [7], but males and non-berried females may
cannibalize ovigerous females. In the present case,
the egg-consuming behavior could have been a result
of post-capture stress of the female. None of the other
17 ovigerous females were found with crayfish eggs
in their stomachs. Six of the berried females had their
stomachs empty, three had their stomachs half-filled,
mainly with plant fragments and detritus, and the others
had a minimum stomach volume filled.
Quantitative analyses of crayfish stomach contents
gave a more accurate picture of feeding relationships.
Plants were the most common food item present in
O. limosus stomachs, but the relative highest volume of
stomach contents was composed of detritus, with plants
second, and animal matter third. Plants have a lower
nutritional value compared with animals [39,44,45].
Chucholl [26], as well as Hollows et al. [46], identified
detritus as the most important food component in
stomachs of O. immunis and Paranephrops zealandicus
(White, 1847), respectively. In the latter study, stable
isotope analyses of carbon and nitrogen showed aquatic
invertebrates in crayfish food as more important than
detritus. In the present study, food of clearly recognizable
animal origin was the least represented. The animal
food component, however, may be lower in crayfish
specimens collected in natural conditions, as noted by
Saffran and Barton [47]. Nyström [7] concluded that
crayfish from natural conditions have more plants and
detritus in their stomachs, while in laboratory conditions
they prefer to feed on invertebrates. Söderbäck et al.
[9] suggested that a higher percentage of detritus in
crayfish stomachs is associated with natural versus
artificial conditions.
The average trophic indexes evaluated during this
study for O. limosus (D=17.7) are much lower than the
theoretical maximum value (42.7), though fluctuating
some seasonally (D=12.9–14.9), between sexes
(D=16.0 and 16.7) and between water bodies (13.5 and
17.3). For seasons, the lowest value was in the spring
period, in a comparison with summer and autumn,
a higher index was for standing waters and lower for
running waters. Similarity of these lowered indices, as
in all above cases, reflect moderate diversity of utilized
food [see 30]. In contrast, the index for another invasive
crayfish in Europe, Procambarus clarkii (Girard, 1852),
has been found to be much higher, 24.6–35.1 [38,48,49],
indicating a wider food niche and the ability of foodswitching by extending to new areas in this species.
Summarizing our analysis of crayfish stomach
contents, we can conclude that: (1) the spiny-cheek
crayfish, O. limosus, is a distinct omnivore with detrital,
plant, and animal components well represented in
their consumed food; (2) the main quantitative food
component of O. limosus is detritus, and the second
most common is plant material; (3) the latter includes
also tree roots, which were more important during
spring months when animal food and detritus supply
were consumed at the lowest levels; (4) O. limosus may
swallow food particles whole up to 4 mm in size, and
the bodies of small animals may sometimes be found
undamaged in stomachs.
According to previous reports on European crayfish
(e.g., [7,13,14,19,33,35,50]), there is no evidence
of differences between indigenous and the invasive
crayfish species O. limosus studied here in feeding
ecology and diet. However, invasive crayfish are, thanks
to their life strategies, able to switch food sources faster
and are usually able to out-compete native crayfish
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R. Vojkovská et al.
for food sources. As they also often occur in higher
densities and feed on the same food as local species,
they are important competitors for native crayfish and
may also negatively affect lower trophic levels in water
ecosystems.
Acknowledgements
The authors are very grateful to Dr. Floyd Sandford,
Prof. Emeritus (Coe College, Cedar Rapids, U.S.A.),
for reading an early version of the manuscript, and to
reviewers whose comments were gratefully accepted to
improve the quality of the final manuscript. This work
was supported by the project of the Grant Agency of the
Czech Academy of Sciences (GP505/12/0545), by the
project ‘Institute of Environmental Technologies‘, Ostrava
(CZ.1.05/2.1.00/03.0100
and
ED2.1.00/03.0100),
funded jointly by the EU Operational Program ‘Research
and Development for Innovations’, and by the project
of the Student Grant Competition (sgs05/PřF/2012 and
sgs09/PřF/2013), University of Ostrava.
References
[1]
Gherardi F., Holdich D.M. (Eds.), Crayfish in Europe
as Alien Species: How to Make the Best of a Bad
Situation? A.A. Balkema, Rotterdam, Brookfield,
1999
[2] Souty-Grosset C., Holdich D.M., Noël P.Y.,
Reynolds J.D., Haffner P. (Eds.), Atlas of Crayfish
in Europe, Muséum national d’Histoire naturelle,
Paris, 2006
[3] Holdich D.M., Reynolds J.D., Souty-Grosset C.,
Sibley P.J., A review of the ever increasing threat
to European crayfish from non-indigenous crayfish
species, Knowl. Managt. Aquatic Ecosyst., 2009,
11, 394-395
[4] Lindquist O., Huner J.V., Life history characteristics
of crayfish: What makes some of them good
colonizers? In: Gherardi F., Holdich D.M.
(Eds.), Crayfish in Europe as Alien Species.
How to Make the Best of a Bad Situation? A.A.
Balkema, Rotterdam, Brookfield, 1999
[5] Holdich D.M., Reeve I.D., Functional Morphology
and Anatomy, In: Holdich D.M., Lowery R.S.
(Eds.), Freshwater Crayfish, Management and
Exploitation, Croom Helm, London, Sydney, 1988
[6] Hamr P., Orconectes, In: Holdich D.M. (Ed.),
Biology of Freshwater Crayfish, Blackwell Science,
Oxford, 2002
[7] Nyström P., Ecology, In: Holdich D.M. (Ed.), Biology
of Freshwater Crayfish, Blackwell Science, Oxford,
2002
[8] Momot W., Redefining the role of crayfish in aquatic
ecosystems, Rev. Fish. Sci., 1995, 3, 33-63
[9] Söderbäck B., Appelberg M., Odelström T.,
Lindquist U., Food consumption and growth of
the crayfish Astacus astacus L. in laboratory
experiments, Freshw. Crayfish, 1988, 7, 145-153
[10] Love J., Savino J.F., Crayfish (Orconectes
virilis) predation on zebra mussels (Dreissena
polymorpha), J. Freshw. Ecol., 1993, 8, 235-259
[11] MacIsaac H.J., Size-selective predation on
zebra mussels (Dreissena polymorpha) by
crayfish (Orconectes propinquus), J. N. Amer.
Benthol. Soc., 1994, 13, 206-216
[12] Warner G.F., Factors affecting the selection of pond
snail prey by signal crayfish, Freshw. Crayfish,
1996, 11, 194-202
[13] Nyström P., Pérez J.R., Crayfish predation on the
common pond snail (Lymnaea stagnalis): the effect
of habitat complexity and snail size on foraging
efficiency, Hydrobiologia, 1998, 368, 201-208
[14] Goddard J.S., Food and feeding, In: Holdich
D.M., Lowery R.S. (Eds.), Freshwater Crayfish,
Management and Exploitation, Croom Helm,
London, Sydney, 1988
[15] Usio N., Effects of crayfish on leaf processing and
invertebrate colonization of leaves in a headwater
stream: decoupling of a trophic cascade, Oecologia,
2000, 124, 608-614
[16] Chambers P.A., Hanson J.M., Burke J.M., Prepas
E.E., The impact of the crayfish Orconectes virilis
on aquatic macrophytes, Freshw. Biol., 1990, 24,
81-91
[17] Lodge D.M., Kershner M.W., Aloi J.E., Covich A.P.,
Effects of an omnivorous crayfish (Orconectes
rusticus) on a freshwater littoral food web, Ecology,
1994, 75, 1265-1281
[18] Cronin G., Lodge D.M, Hay M.E., Miller M., Hill A.M.,
Horvath T., et al., Crayfish feeding preferences for
freshwater macrophytes: The influence of plant
structure and chemistry, J. Crustac. Biol., 2002, 22,
708-718
[19] Nyström P., Strand J.A., Grazing by a native and
exotic crayfish on aquatic macrophytes, Freshw.
Biol., 1996, 36, 673-682
[20] Olsen T.M., Lodge D.M., Capelli G.M., Houlihan
R.J., Mechanisms of impact of an introduced
crayfish (Orconectes rusticus) on littoral congeners,
67
Unauthenticated
Download Date | 6/15/17 11:05 PM
Diet of Orconectes limosus
[21]
[22]
[23]
[24]
[25]
[26]
[27]
[28]
[29]
[30]
[31]
[32]
[33]
snails and macrophytes, Can. J. Fish. Aquat. Sci.,
1991, 48, 1853-1861
Smart A.C., Harper D.M., Malaisse F., Schmitz S.,
Coley S., Beauregard A.C.G., Feeding of the exotic
Louisiana red swamp crayfish, Procambarus clarkii
(Crustacea, Decapoda), in an African tropical lake:
lake Naivasha, Kenya, Hydrobiologia, 2002, 488,
129-142
Staszak K., Szaniawska A., Feeding rates and
food preferences of the spiny-cheek crayfish
Orconectes limosus at two different temperatures,
Freshw. Crayfish, 2006, 15, 148-154
Anwand K., Valentin M., On the nutritional biology
of Orconectes limosus (Raf.), (Crustacea),
Limnologica, 1996, 26, 83-91
Chiesa S., Scalici M., Gibertini G., Occurrence
of allochthonous freshwater crayfishes in Latium
(central Italy), Bull. Fr. Pêche Piscicult., 2006,
380/381, 883-902
Chybowski L., Morphometrics, fecundity, density
and feeding intensity of spiny-cheek crayfish,
Orconectes limosus (Raf.) in natural conditions,
Arch. Polish Fish., 2007, 15, 175-241
Chucholl C., Understanding invasion success: lifehistory traits and feeding habits of the alien crayfish
Orconectes immunis (Decapoda, Astacida,
Cambaridae), Knowl. Managt. Aquatic Ecosyst.,
2012, 404, 1-22
Ďuriš Z., Drozd P., Horká I., Kozák P., Policar T.,
Biometry and demography of the invasive crayfish
Orconectes limosus in the Czech Republic, Bull.
Fr. Pêche Piscicult., 2006, 380/381, 1215-1228
Petrusek A., Filipová L., Ďuriš Z., Horká I., Kozák
P., Policar T., et al., Distribution of the invasive
spiny-cheek crayfish (Orconectes limosus) in the
Czech Republic, Bull. Fr. Pêche Piscicult., 2006,
380/381, 903-918
Ďuriš Z., Horká I., First record of the invasive spinycheek crayfish Orconectes limosus (Rafinesque)
in Moravian and Silesian region, Czech Republic,
Čas. Sl. Muz. Opava (A), 2007, 56, 49-52 (in
Czech)
Herrera C.M., A trophic index for presence-absence
food data, Oecologia, 1976, 25, 187-191
Zar J.H., Biostatistical Analysis, Prentice Hall,
Englewood Cliffs, New Jersey, 1984
Skurdal J., Fjeld E., Hessen D.O., Taugbol T., Dehli
E., Depth distribution, habitat segregation and
feeding of the crayfish Astacus astacus in Lake
Steinsfjorden, S. E. Norway. Nord. J. Freshw. Res.,
1988, 64, 113-119
Odelström T., Appelberg M., Food choice of Astacus
astacus L. in some neutralised lakes, In: Odelström
[34]
[35]
[36]
[37]
[38]
[39]
[40]
[41]
[42]
[43]
[44]
[45]
T., The food choice of the crayfish Astacus astacus
L. in relation to environmental conditions, Acta
Univ. Uppsala, 1988, 165, 1-13
Lorman J.G., Feeding and activity of the crayfish
Orconectes rusticus in a northern Wisconsin lake,
MS thesis, University of Wisconsin, Madison, USA,
1975
Reynolds J.D., O’Keeffe C., Dietary patterns
in stream- and lake-dwelling populations
of
Austropotamobius
pallipes,
Bull.
Fr.
Pêche Piscicult., 2005, 376/377, 715-730
Ilhéu M., Bernardo J.M., Trophic ecology of red
swamp crayfish Procambarus clarkii (Girard) preferences and digestibility of plant foods, Freshw.
Crayfish, 1995, 10, 132-139
Rabeni C., Gossett M., McClendon D.D.,
Contribution of crayfish to benthic invertebrate
production and trophic ecology of an Ozark stream,
Freshw. Crayfish, 1995, 10, 163-173
Alcorlo P., Geiger W., Otero M., Feeding
preferences and food selection of the red swamp
crayfish, Procambarus clarkii, in habitats differing
in food item diversity, Crustaceana, 2004, 77,
435-453
Taylor C.A., Soucek D.J., Re-examining the
importance of fish in the diets of stream-dwelling
crayfishes: implications for food web analyses
and conservation, Amer. Midl. Natur., 2010, 163,
280-293
Ďuriš Z., Horká I., Kristian J., Kozák P., Some
cases of macro-epibiosis on the invasive crayfish
Orconectes limosus in the Czech Republic, Bull.
Fr. Pêche Piscicult., 2006, 380/381, 1325-1337
Perry W.L., Lodge D.M., Lamberti G.A., Crayfish
(Orconectes rusticus) impacts on zebra mussel
(Dreissena
polymorpha)
recruitment
other
macroinvertebrates and algal biomass in a lake
– outlet stream, Amer. Midl. Natur., 2000, 144,
308-316
Martin G.W., Corkum L.D., Predation of zebra
mussels by crayfish, Can. J. Zool., 1994, 72,
1867-1871
Charlebois P.M., Lamberti G.A., Invading crayfish
in a Michigan stream: direct and indirect effects on
periphyton and macroinvertebrates, J. North Amer.
Benthol. Soc., 1996, 15, 551-563
Whitledge G.W., Rabeni C.F., Diel and seasonal
variation in the food habits of crayfishes in a
Missouri Ozrak stream, Freshw. Crayfish, 1996, 11,
159-169
Parkyn S.M., Collier K.J., Hicks B.J., New Zealand
stream crayfish: functional omnivores but trophic
predators? Freshw. Biol., 2001, 46, 641-652
68
Unauthenticated
Download Date | 6/15/17 11:05 PM
R. Vojkovská et al.
[46] Hollows J.W., Townsend C.R., Collier K.J., Diet
of the crayfish Paranephrops zealandicus in bush
and pasture streams: insights from stable isotopes
and stomach analysis, New Zeal J. Mar. Fresh.,
2002, 36, 129-142
[47] Saffran K.A., Barton D.R., Trophic ecology of
Orconectes propinquus (Girard) in Gregorian Bay
(Ontario, Canada), Freshw. Crayfish, 1993, 9,
350-358
[48] Gutiérez-Yurrita P.J., Sancho G., Bravo M.Á.,
Baltanás Á., Montes C., Diet of the red swamp
crayfish Procambarus clarkii in natural ecosystems
of the Doňana National Park temporary fresh-water
marsh (Spain), J. Crustac. Biol., 1998, 18, 120-127
[49] Correia A.M., Niche breadth and trophic diversity:
feeding behaviour of the red swamp crayfish
(Procambarus clarkii) towards environmental
availability of aquatic macroinvertebrates in a rice
field (Portugal), Acta Oecol., 2002, 23, 421-429
[50] Gherardi F., Renai B., Corti C., Crayfish predation
on tadpoles: a comparison between a native
(Austropotamobius pallipes) and an alien species
(Procambarus clarkii), Bull. Fr. Pêche Piscicult.,
2001, 361, 659-668
69
Unauthenticated
Download Date | 6/15/17 11:05 PM