CC BY-NC-ND
0Cent. Eur J. Biol.
DOI: 10.2478/s11535-013-0189-y
VERSITA
Central European Journal of Biology
The diet of the spiny-cheek crayfish Orconectes Hmosus in the Czech Republic
Research Article
Renata Vojkovska, Ivona Horka*, Zdenek Duns
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: The composition of the diet of the invasive spiny-cheek crayfish Orconectes 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 from the Labe (Elbe) and Vltava River basins. Food components were compared for three size classes of crayfish and both sexes. The following conclusions were reached: (1) the spiny-cheek crayfish is an omnivorous species consuming plants, animals and detritus; (2) quantitatively, the main food component of O. limosus is detritus, while the plant component was second; (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 macro-invertebrates [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
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 Nystrom 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 spiny-cheek crayfish. Staszak and Szaniawska [22], as well
E-mail: ivona.horka@osu.cz
Springer
as Anwand and Valentin [23], described O. limosus as an omnivore. Staszak and Szaniawska [22] noted that, at higher densities, cannibalistic behavior of spiny-cheek 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 Dollnsee 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.
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 Prudnik 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).
Figure 1. Localities where samples of Orconectes limosus were taken for stomach content analyses.
Watercourse / body Nearest settlement Latitude (N) Longitude (E)
Running waters
Labe Hnévice 50°27' 14°22'
Labe Kolín 50°02' 15°13'
Labe (confluence with Farsky potok) Ostrá 50°10' 14°54'
Labe Litomérice 50°32' 50°32'
Labe Malé Brezno 50°40' 14°10'
Labe Nebocady 50°43' 14°11'
Labe Obríství 50°18' 14°29'
Labe Podébrady 50°09' 15°06'
Labe Stétí 50°27' 14°22'
Labe Téchlovice 50°42' 14°12'
Labe Ústí nad Labem 50°39' 14°03'
Labe (confluence with Lucní potok) Treboutice 50°31' 14°12'
Cidlina Libice nad Cidlinou 50°07' 15°11'
Doubrava Záborí nad Labem 50°01' 15°21'
Jickovicky potok Jickovice 49°27' 14°13'
Jizera Novy Vestec 50°11' 14°44'
Ohre Doksany 50°27' 14°09'
Ohre Bohusovice nad Ohr 50°30' 14°09'
Prudník Osoblaha 50°17' 17°44'
Vltava Vrbno u Mélníka Standing waters 50°19' 14°27'
Barbora (quarry) Oldrichov u Teplic 50°38' 13°45'
Cítov (sand pit) Vlinéves 50°22' 14°27'
Kojetice (quarry) Kojetice u Neratovic 50°14' 14°30'
Lhota (sand pit) Lhota 50°15' 14°40'
sand pit near the airport Borek Stará Boleslav 50°12' 14°40'
Orlík (reservoir) Temesvár 49°21' 14°16'
Table 1. 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:
Classes Parameters Qualitative analyzes Quantitative analyzes
Size Small (POCL < 13 mm) 38 2
Medium (POCL 13 - 28 mm) 271 83
Large (POCL > 28 mm) 59 27
I 368 112
Sex Males 212 62
Females 156 50
(included ovigerous females) (17) 0
I 368 112
Seasons spring 34 40
summer 237 33
autumn 54 39
I 368 112
Table 2. Number of specimens used for qualitative and quantitative analyses of stomach contents.
D = log ft
where 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 oneway 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 spiny-cheek 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
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.
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 spiny-cheek 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
Food components
crayfish males
sex females
spring
season summer
autumn
crayfish size class small medium
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 Kruskal-Wallis 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
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.
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 (Figure 6), mainly in the summer and autumn periods (Table 3). 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 Nystrom [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]. Nystrom [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. Soderback 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 food-switching 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
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.),
References
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