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 crayfishOrconectes 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: Thecompositionofthedietoftheinvasivespiny-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 mussels [10], or small and middle-sized mussels and aquatic gastropods to large ones [11-13]. The spiny-cheek crayfish, Orconectes limosus Being omnivorous throughout their life cycle, crayfish (Rafinesque, 1817), is the most common alien crayfish in may prefer different foods in different stages of their life, European freshwater ecosystems [1-3]. Characteristics with freshly hatched juveniles feeding mainly on animal determining its competitive advantage in comparison plankton and later on benthic invertebrates, while adults with native species include: an r-strategist life cycle with consuming mostly plants and detritus [14,15]. The faster reproduction and earlier maturation; a greater selection of plant foods often depends on mechanical tolerance to polluted waters; and the ability to spread structure, nutritional values, or plant chemical defenses the crayfish plague pathogen, together with its own [7,16-18]. According to Nyström and Strand [19] and resistance to that illness [4]. Cronin et al. [18], crayfish prefer newly budding or finely Crayfish forage on a wide range of foods, including branching plants to those that are well grown and rigid. water macrophytes, algae, detritus and macro- When foraging on submerged and emerged macrophytes, invertebrates [5-7]. Despite being generally omnivorous crayfish may cause changes to deep water environments. animals, different food components may be preferred Invasive species, in particular, may negatively affect in accordance with availability and energetic value [8]. aquatic plant density and diversity [19-21]. Söderbäck et al. [9] also showed that, in experimental Alien species compete with native species over conditions, crayfish feeding on animal-originated food many biological resource aspects, including food grow faster and show higher foraging activity than consumption. Despite a fairly wide literature on feeding those kept on a detrital diet. Feeding selectivity has also of different crayfish species, from which only a limited been experimentally documented for food of animal review is given above, little data has been reported origin, with crayfish foraging on thin-shelled rather than on the food and feeding impacts of the invasive spiny- thick-shelled mollusks [7], preferring fish eggs to zebra cheek crayfish. Staszak and Szaniawska [22], as well

* E-mail: [email protected] 58 R. Vojkovská et al.

as Anwand and Valentin [23], described O. limosus as 2. Experimental Procedures an omnivore. Staszak and Szaniawska [22] noted that, at higher densities, cannibalistic behavior of spiny- Qualitative and quantitative analyses of the main and cheek crayfish frequently occurs. Chiesa et al. [24] also particular food items were performed for the stomach characterized O. limosus as omnivorous. Based on contents of 368 spiny-cheek crayfish specimens of qualitative analyses of stomach contents, they divided different sizes and sexes, collected in the Labe (Elbe) these contents into four categories – animal, plant, detrital and Vltava River basins. Crayfish were collected in 26 and others (the latter containing abiotic components); localities of the Czech Republic, usually from April to the main food item found was of plant origin, followed October, 2003–2005 (Table 1; Figure 1). The material by detritus and animal food. Chybowski [25] studied was originally collected for distributional and biometric the foraging of O. limosus in Polish lakes in relation to purposes [27,28]. Specimens were caught by hand diurnal and annual activity. He identified plant material during the morning hours and preserved in 70% as the primary food item found in crayfish stomachs, ethanol within 2–4 hours. Some additional specimens and stated that annual consumption amounted to only were collected from the Prudník Brook, Odra river, NW 0.27% of the available aquatic vegetation. Similar results Moravian-Silesian region in 2008 [29]. Stomach contents are presented also by Anwand and Valentin [23] for the were analyzed in the laboratory for 368 O. limosus species in Kleiner Döllnsee Lake in Germany. Chucholl specimens (212 males and 156 females, including 17 [26] demonstrated the omnivorous feeding habits of the ovigerous females) (Table 2). calico crayfish, Orconectes immunis (Hagen, 1870), a Because of low numbers of specimens collected competitor of O. limosus in the Rhine River, Germany. from particular localities, all the crayfish used in this The aim of this study is elucidate the diet study were pooled into one sample, then sexed and composition of the non-indigenous spiny-cheek crayfish divided into three size classes (S, M, and L) according O. limosus in the Czech Republic using qualitative and to the post-orbital carapace length (POCL), measured quantitative analysis of stomach contents, contributing in the dorsal body midline from the level of the posterior to knowledge on the ecology of invasive animals and orbital margins to the posterior margin of the carapace to the conservation of native species and natural water (see [27]: S – up to 13 mm, M – 13–28 mm, L – over ecosystems. 28 mm).

Figure 1. Localities where samples of Orconectes limosus were taken for stomach content analyses.

59 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 Ostrá 50°10’ 14°54’ (confluence with Farský potok) 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 Třeboutice 50°31’ 14°12’ (confluence with Luční potok) 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’

Standing waters

Barbora (quarry) Oldřichov u Teplic 50°38’ 13°45’

Cítov (sand pit) Vliněves 50°22’ 14°27’

Kojetice (quarry) Kojetice u Neratovic 50°14’ 14°30’

Lhota (sand pit) Lhota 50°15’ 14°40’ sand pit Stará Boleslav 50°12’ 14°40’ near the airport Borek Orlík (reservoir) Temešvár 49°21’ 14°16’

Table 1. Geographical details of sampling localities.

Stomach contents were observed using an Arsenal particles and digested by crayfish immediately from the MBS-10-100 stereomicroscope and Arsenal LS 1001 substratum), together with more or less recognizable standard light microscope. The frequency of occurrence animal remains (e.g., sclerotized insect heads or legs, of a particular food item was calculated as a percentage mollusk shells), or plant parts (tree roots). of the number of analyzed stomachs containing an Stomach fullness was estimated visually in relation actual food item, i.e., excluding empty stomachs. Where to the potential total volume of a stomach and divided possible, animal remains in stomachs were determined into five classes: A – empty stomach; B – distinctly using identification keys. When not empty, stomachs less than half of the volume (e.g., one insect larva or a mostly contained any of three poorly identifiable low quantity of plant tissues); C and D – partially filled, food items – soft animal tissues (e.g., fresh muscles, around half or distinctly more than half, respectively, of fat bodies), plant tissues (fresh, with recognizable the stomach volume; E – full stomach. lignified vascular tissues), and detritus (particulate Based on the presence or absence of distinct food organic material consisting of minute fragments of items, the trophic index „D“ showing the wideness of the dead organisms exposed for a time among bottom food spectrum [30] was calculated:

60 R. Vojkovská et al.

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

Σ 368 112

Sex Males 212 62

Females 156 50

(included ovigerous females) (17) 0

Σ 368 112

spring 34 40 Seasons summer 237 33

autumn 54 39

Σ 368 112

Table 2. Number of specimens used for qualitative and quantitative analyses of stomach contents.

non-parametric method to test for the equality of

= log quantitative contents of main food items among crayfish groups (based on size classes and sexes).

where pi is a frequency of occurrence of a distinct food item, and s is a sum of all food items. According to 3. Results Herrera [30] the limit for this index is 0

61 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.

62 R. Vojkovská et al.

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 mussel Dreissena polymorpha (Pallas, 1771), were also (gastropod and bivalve shells – 8.3%) and bryozoans often present. Food particles of a size up to 4 mm were (statoblasts – 22.2%). Nymphs of Caenis macrura often swallowed whole, almost undamaged, by spiny- Stephens, 1835 (Ephemeroptera) (Figure 7), and some cheek crayfish. other insect species, were identified as almost intact Undamaged crayfish eggs were found in the specimens. Broken or undamaged shells of gastropods stomach of one ovigerous female. The size, stage of Ancylus fluviatilis O.F. Müller, 1774, Galba cf. truncatula development, and color of the eggs were all similar to (O.F. Müller, 1774), and the bivalve mollusk zebra the ova from the external egg mass carried by the same

63 Diet of Orconectes limosus

crayfish sex season crayfish size class Food components males females spring summer 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 4. Discussion analyses of stomach contents showed no important differences in food composition between the sexes, Most specimens of the spiny-cheek crayfishOrconectes but there were distinctions found for detritus, plant and limosus in this study had stomachs filled up to half their animal food components among seasons (Table 3). maximum volume, regardless of sex or size class. In For the quantitative analyses of stomach contents other studies on the noble crayfish Astacus astacus composition, the main food components (plants, (L., 1758) in Europe [32,33] or in Orconectes rusticus animals, and detritus) were evaluated by the Kruskal- (Girard, 1852) in America [34], a possible relation to Wallis test of non-parametric data in relation to crayfish seasons was detected. Chybowski [25] found that size classes, sexes, and seasons. The differences stomachs were frequently empty in Polish specimens of among food components were not significant for O. limosus during the January–March period. In Italy, medium and large-sized crayfish. The only significant about 20% of the same species were observed with relationship was found for detritus between sexes empty stomachs in July [24]. In our study, the seasonal (P<0.005486). effect of stomach fullness revealed a summer maximum The trophic index D reflects the relative width of and the lowest value occurring during the spring period, the food spectrum utilized. For all analyzed crayfish while the autumn period is indicated in the latter respect specimens, this index was 17.7, with a theoretical in Germany [23]. Stomach fullness, however, more maximum 42.7. The index for males was 16.7, and for likely depends also on the photoperiod. Lorman [34] females 16.0. For seasons, the D value was 12.9 in and Chybowski [25] reported higher frequencies of spring, for both summer and autumn was equally 14.9. full stomachs in O. rusticus and O. limosus during the The trophic index for standing waters was 17.3, and night. Our results are based on specimens collected 13.5 for running waters. mainly during the morning hours. The digestion of easily

64 R. Vojkovská et al.

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 water temperature, but stated that crayfish consumed capture, and after that, could partially affect the results. more food in higher temperature water. Food remains, however, are usually present quite long According to distinctly identifiable plant remains and time in the digestive tract. Chybowski [25], as well as particles, the most frequent plant food item in O. limosus Reynolds and O´Keefe [35], reported the presence were the filamentous algae Cladophora sp. Finely of food almost 16 and 72 hours after ingestion in branching or filamentous plants are known to be preferred O. limosus and Austropotamobius pallipes (Lereboullet, foods in other crayfish species [18,20,36]. Food of animal 1858), respectively. origin, mainly benthic invertebrates, is another important Qualitatively, the most frequent food component component for crayfish [37,38]. Lorman [34] found that of O. limosus stomachs in the present study (see males and small specimens of O. rusticus feed on animals Figure 5 – above) was plant matter (79.9%), but animal to a greater extent than females and larger specimens. matter and detritus were also present. Plant material Chiesa et al. [24] supposed that differences in frequency in O. limosus is regarded dominant also by Chybowski of the occurrence of animal components between sexes of [25], Chiesa et al. [24] and Anwand and Valentin [23]. O. limosus were due to increased demands on energy for Lorman [34], studying O. rusticus, noted an increasing oogenesis in females. In our study, O. limosus showed no ratio of the plant component as crayfish size increased. special preference for animal food. In some distinct cases, Staszak and Szaniawska [22] found no preference of small specimens were found with nothing but one or a few O. limosus for plant or animal food items in relation to chironomid larvae in their stomachs.

65 Diet of Orconectes limosus

Within the present study, the most frequent nutritional value compared with animals [39,44,45]. identifiable distinct animal components in food Chucholl [26], as well as Hollows et al. [46], identified extracted from crayfish stomachs were chironomid detritus as the most important food component in larvae [Insecta: Chironomidae] and ‘moss-animals’ stomachs of O. immunis and Paranephrops zealandicus statoblasts [Bryozoa], both occurring in about 22% (White, 1847), respectively. In the latter study, stable of stomachs, mainly in the summer and autumn isotope analyses of carbon and nitrogen showed aquatic periods. Mayfly nymphs [Insecta: Ephemeroptera] invertebrates in crayfish food as more important than were sometimes found; their bodies were often almost detritus. In the present study, food of clearly recognizable undamaged when dissected from crayfish stomachs animal origin was the least represented. The animal and well identifiable to species level (Caenis macrura food component, however, may be lower in crayfish in most cases). Mayfly nymphs were reported as being specimens collected in natural conditions, as noted by the most frequent animal food for O. rusticus and Saffran and Barton [47]. Nyström [7] concluded that O. luteus (Creaser, 1933) in their natural range [37]. In crayfish from natural conditions have more plants and general, soft bodied animals, including mayfly nymphs detritus in their stomachs, while in laboratory conditions and fish, are more easily digested by crayfish. There they prefer to feed on invertebrates. Söderbäck et al. were no food components in our specimens reliably [9] suggested that a higher percentage of detritus in identifiable as fish parts; however, Taylor and Soucek crayfish stomachs is associated with natural versus [39] point out that the presence of fish in crayfish artificial conditions. stomachs is often underestimated. On the other hand, The average trophic indexes evaluated during this hard-shelled remains and particles may be present study for O. limosus (D=17.7) are much lower than the for a longer time in the cardiac stomach. In our study, theoretical maximum value (42.7), though fluctuating minute intact gastropod shells, and crushed shells of some seasonally (D=12.9–14.9), between sexes the zebra mussel Dreissena polymorpha, were the (D=16.0 and 16.7) and between water bodies (13.5 and most frequent mollusk remains in crayfish stomachs. 17.3). For seasons, the lowest value was in the spring This bivalve species is currently widely distributed in period, in a comparison with summer and autumn, the Labe River and in quarries from which the present a higher index was for standing waters and lower for crayfish specimens were collected [40]. Feeding running waters. Similarity of these lowered indices, as relations of crayfish of the genus Orconectes to in all above cases, reflect moderate diversity of utilized zebra mussels has been a frequent subject of study food [see 30]. In contrast, the index for another invasive recently [10,41,42]. Crayfish are important predators crayfish in Europe, Procambarus clarkii (Girard, 1852), of mollusks [12,13,17,20,43]; they prefer to feed on has been found to be much higher, 24.6–35.1 [38,48,49], smaller mollusks, rather than on larger ones [11,12]. indicating a wider food niche and the ability of food- Another interesting finding was the presence of switching by extending to new areas in this species. about 10 undamaged eggs in the stomach of one of Summarizing our analysis of crayfish stomach the ovigerous O. limosus female examined. Based contents, we can conclude that: (1) the spiny-cheek on the shape, size, and coloration, these eggs likely crayfish, O. limosus, is a distinct omnivore with detrital, originated from the egg-mass of the same female. plant, and animal components well represented in Crayfish females do not eat their own eggs, according their consumed food; (2) the main quantitative food to Nyström [7], but males and non-berried females may component of O. limosus is detritus, and the second cannibalize ovigerous females. In the present case, most common is plant material; (3) the latter includes the egg-consuming behavior could have been a result also tree roots, which were more important during of post-capture stress of the female. None of the other spring months when animal food and detritus supply 17 ovigerous females were found with crayfish eggs were consumed at the lowest levels; (4) O. limosus may in their stomachs. Six of the berried females had their swallow food particles whole up to 4 mm in size, and stomachs empty, three had their stomachs half-filled, the bodies of small animals may sometimes be found mainly with plant fragments and detritus, and the others undamaged in stomachs. had a minimum stomach volume filled. According to previous reports on European crayfish Quantitative analyses of crayfish stomach contents (e.g., [7,13,14,19,33,35,50]), there is no evidence gave a more accurate picture of feeding relationships. of differences between indigenous and the invasive Plants were the most common food item present in crayfish species O. limosus studied here in feeding O. limosus stomachs, but the relative highest volume of ecology and diet. However, invasive crayfish are, thanks stomach contents was composed of detritus, with plants to their life strategies, able to switch food sources faster second, and animal matter third. Plants have a lower and are usually able to out-compete native crayfish

66 R. Vojkovská et al.

for food sources. As they also often occur in higher for reading an early version of the manuscript, and to densities and feed on the same food as local species, reviewers whose comments were gratefully accepted to they are important competitors for native crayfish and improve the quality of the final manuscript. This work may also negatively affect lower trophic levels in water was supported by the project of the Grant Agency of the ecosystems. 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), Acknowledgements funded jointly by the EU Operational Program ‘Research and Development for Innovations’, and by the project The authors are very grateful to Dr. Floyd Sandford, of the Student Grant Competition (sgs05/PřF/2012 and Prof. Emeritus (Coe College, Cedar Rapids, U.S.A.), sgs09/PřF/2013), University of Ostrava.

References

[1] Gherardi F., Holdich D.M. (Eds.), Crayfish in Europe [11] MacIsaac H.J., Size-selective predation on as Alien Species: How to Make the Best of a Bad zebra mussels (Dreissena polymorpha) by Situation? A.A. Balkema, Rotterdam, Brookfield, crayfish (Orconectes propinquus), J. N. Amer. 1999 Benthol. Soc., 1994, 13, 206-216 [2] Souty-Grosset C., Holdich D.M., Noël P.Y., [12] Warner G.F., Factors affecting the selection of pond Reynolds J.D., Haffner P. (Eds.), Atlas of Crayfish snail prey by signal crayfish, Freshw. Crayfish, in Europe, Muséum national d’Histoire naturelle, 1996, 11, 194-202 Paris, 2006 [13] Nyström P., Pérez J.R., Crayfish predation on the [3] Holdich D.M., Reynolds J.D., Souty-Grosset C., common pond snail (Lymnaea stagnalis): the effect Sibley P.J., A review of the ever increasing threat of habitat complexity and snail size on foraging to European crayfish from non-indigenous crayfish efficiency, Hydrobiologia, 1998, 368, 201-208 species, Knowl. Managt. Aquatic Ecosyst., 2009, [14] Goddard J.S., Food and feeding, In: Holdich 11, 394-395 D.M., Lowery R.S. (Eds.), Freshwater Crayfish, [4] Lindquist O., Huner J.V., Life history characteristics Management and Exploitation, Croom Helm, of crayfish: What makes some of them good London, Sydney, 1988 colonizers? In: Gherardi F., Holdich D.M. [15] Usio N., Effects of crayfish on leaf processing and (Eds.), Crayfish in Europe as Alien Species. invertebrate colonization of leaves in a headwater How to Make the Best of a Bad Situation? A.A. stream: decoupling of a trophic cascade, Oecologia, Balkema, Rotterdam, Brookfield, 1999 2000, 124, 608-614 [5] Holdich D.M., Reeve I.D., Functional Morphology [16] Chambers P.A., Hanson J.M., Burke J.M., Prepas and Anatomy, In: Holdich D.M., Lowery R.S. E.E., The impact of the crayfish Orconectes virilis (Eds.), Freshwater Crayfish, Management and on aquatic macrophytes, Freshw. Biol., 1990, 24, Exploitation, Croom Helm, London, Sydney, 1988 81-91 [6] Hamr P., Orconectes, In: Holdich D.M. (Ed.), [17] Lodge D.M., Kershner M.W., Aloi J.E., Covich A.P., Biology of Freshwater Crayfish, Blackwell Science, Effects of an omnivorous crayfish (Orconectes Oxford, 2002 rusticus) on a freshwater littoral food web, Ecology, [7] Nyström P., Ecology, In: Holdich D.M. (Ed.), Biology 1994, 75, 1265-1281 of Freshwater Crayfish, Blackwell Science, Oxford, [18] Cronin G., Lodge D.M, Hay M.E., Miller M., Hill A.M., 2002 Horvath T., et al., Crayfish feeding preferences for [8] Momot W., Redefining the role of crayfish in aquatic freshwater macrophytes: The influence of plant ecosystems, Rev. Fish. Sci., 1995, 3, 33-63 structure and chemistry, J. Crustac. Biol., 2002, 22, [9] Söderbäck B., Appelberg M., Odelström T., 708-718 Lindquist U., Food consumption and growth of [19] Nyström P., Strand J.A., Grazing by a native and the crayfish Astacus astacus L. in laboratory exotic crayfish on aquatic macrophytes, Freshw. experiments, Freshw. Crayfish, 1988, 7, 145-153 Biol., 1996, 36, 673-682 [10] Love J., Savino J.F., Crayfish (Orconectes [20] Olsen T.M., Lodge D.M., Capelli G.M., Houlihan virilis) predation on zebra mussels (Dreissena R.J., Mechanisms of impact of an introduced polymorpha), J. Freshw. Ecol., 1993, 8, 235-259 crayfish (Orconectes rusticus) on littoral congeners,

67 Diet of Orconectes limosus

snails and macrophytes, Can. J. Fish. Aquat. Sci., T., The food choice of the crayfish Astacus astacus 1991, 48, 1853-1861 L. in relation to environmental conditions, Acta [21] Smart A.C., Harper D.M., Malaisse F., Schmitz S., Univ. Uppsala, 1988, 165, 1-13 Coley S., Beauregard A.C.G., Feeding of the exotic [34] Lorman J.G., Feeding and activity of the crayfish Louisiana red swamp crayfish, Procambarus clarkii Orconectes rusticus in a northern Wisconsin lake, (Crustacea, Decapoda), in an African tropical lake: MS thesis, University of Wisconsin, Madison, USA, lake Naivasha, Kenya, Hydrobiologia, 2002, 488, 1975 129-142 [35] Reynolds J.D., O’Keeffe C., Dietary patterns [22] Staszak K., Szaniawska A., Feeding rates and in stream- and lake-dwelling populations food preferences of the spiny-cheek crayfish of Austropotamobius pallipes, Bull. Fr. Orconectes limosus at two different temperatures, Pêche Piscicult., 2005, 376/377, 715-730 Freshw. Crayfish, 2006, 15, 148-154 [36] Ilhéu M., Bernardo J.M., Trophic ecology of red [23] Anwand K., Valentin M., On the nutritional biology swamp crayfish Procambarus clarkii (Girard) - of Orconectes limosus (Raf.), (Crustacea), preferences and digestibility of plant foods, Freshw. Limnologica, 1996, 26, 83-91 Crayfish, 1995, 10, 132-139 [24] Chiesa S., Scalici M., Gibertini G., Occurrence [37] Rabeni C., Gossett M., McClendon D.D., of allochthonous freshwater crayfishes in Latium Contribution of crayfish to benthic invertebrate (central Italy), Bull. Fr. Pêche Piscicult., 2006, production and trophic ecology of an Ozark stream, 380/381, 883-902 Freshw. Crayfish, 1995, 10, 163-173 [25] Chybowski L., Morphometrics, fecundity, density [38] Alcorlo P., Geiger W., Otero M., Feeding and feeding intensity of spiny-cheek crayfish, preferences and food selection of the red swamp Orconectes limosus (Raf.) in natural conditions, crayfish, Procambarus clarkii, in habitats differing Arch. Polish Fish., 2007, 15, 175-241 in food item diversity, Crustaceana, 2004, 77, [26] Chucholl C., Understanding invasion success: life- 435-453 history traits and feeding habits of the alien crayfish [39] Taylor C.A., Soucek D.J., Re-examining the Orconectes immunis (Decapoda, Astacida, importance of fish in the diets of stream-dwelling Cambaridae), Knowl. Managt. Aquatic Ecosyst., crayfishes: implications for food web analyses 2012, 404, 1-22 and conservation, Amer. Midl. Natur., 2010, 163, [27] Ďuriš Z., Drozd P., Horká I., Kozák P., Policar T., 280-293 Biometry and demography of the invasive crayfish [40] Ďuriš Z., Horká I., Kristian J., Kozák P., Some Orconectes limosus in the Czech Republic, Bull. cases of macro-epibiosis on the invasive crayfish Fr. Pêche Piscicult., 2006, 380/381, 1215-1228 Orconectes limosus in the Czech Republic, Bull. [28] Petrusek A., Filipová L., Ďuriš Z., Horká I., Kozák Fr. Pêche Piscicult., 2006, 380/381, 1325-1337 P., Policar T., et al., Distribution of the invasive [41] Perry W.L., Lodge D.M., Lamberti G.A., Crayfish spiny-cheek crayfish (Orconectes limosus) in the (Orconectes rusticus) impacts on zebra mussel Czech Republic, Bull. Fr. Pêche Piscicult., 2006, (Dreissena polymorpha) recruitment other 380/381, 903-918 macroinvertebrates and algal biomass in a lake [29] Ďuriš Z., Horká I., First record of the invasive spiny- – outlet stream, Amer. Midl. Natur., 2000, 144, cheek crayfish Orconectes limosus (Rafinesque) 308-316 in Moravian and Silesian region, Czech Republic, [42] Martin G.W., Corkum L.D., Predation of zebra Čas. Sl. Muz. Opava (A), 2007, 56, 49-52 (in mussels by crayfish, Can. J. Zool., 1994, 72, Czech) 1867-1871 [30] Herrera C.M., A trophic index for presence-absence [43] Charlebois P.M., Lamberti G.A., Invading crayfish food data, Oecologia, 1976, 25, 187-191 in a Michigan stream: direct and indirect effects on [31] Zar J.H., Biostatistical Analysis, Prentice Hall, periphyton and macroinvertebrates, J. North Amer. Englewood Cliffs, New Jersey, 1984 Benthol. Soc., 1996, 15, 551-563 [32] Skurdal J., Fjeld E., Hessen D.O., Taugbol T., Dehli [44] Whitledge G.W., Rabeni C.F., Diel and seasonal E., Depth distribution, habitat segregation and variation in the food habits of crayfishes in a feeding of the crayfish Astacus astacus in Lake Missouri Ozrak stream, Freshw. Crayfish, 1996, 11, Steinsfjorden, S. E. Norway. Nord. J. Freshw. Res., 159-169 1988, 64, 113-119 [45] Parkyn S.M., Collier K.J., Hicks B.J., New Zealand [33] Odelström T., Appelberg M., Food choice of Astacus stream crayfish: functional omnivores but trophic astacus L. in some neutralised lakes, In: Odelström predators? Freshw. Biol., 2001, 46, 641-652

68 R. Vojkovská et al.

[46] Hollows J.W., Townsend C.R., Collier K.J., Diet of the Doňana National Park temporary fresh-water of the crayfish Paranephrops zealandicus in bush marsh (Spain), J. Crustac. Biol., 1998, 18, 120-127 and pasture streams: insights from stable isotopes [49] Correia A.M., Niche breadth and trophic diversity: and stomach analysis, New Zeal J. Mar. Fresh., feeding behaviour of the red swamp crayfish 2002, 36, 129-142 (Procambarus clarkii) towards environmental [47] Saffran K.A., Barton D.R., Trophic ecology of availability of aquatic macroinvertebrates in a rice Orconectes propinquus (Girard) in Gregorian Bay field (Portugal), Acta Oecol., 2002, 23, 421-429 (Ontario, Canada), Freshw. Crayfish, 1993, 9, [50] Gherardi F., Renai B., Corti C., Crayfish predation 350-358 on tadpoles: a comparison between a native [48] Gutiérez-Yurrita P.J., Sancho G., Bravo M.Á., (Austropotamobius pallipes) and an alien species Baltanás Á., Montes C., Diet of the red swamp (Procambarus clarkii), Bull. Fr. Pêche Piscicult., crayfish Procambarus clarkii in natural ecosystems 2001, 361, 659-668

69