The role of abiotic and biotic factors in interspecific competition of Polish crayfish – comprehensive literature review

The pH of the environment affects the pH of the body, and thus the proper course of physiological reactions and processes, including resorption or deposition of alkaligenous calcium, which is necessary, among others, for proper molting, muscle and nervous system processes (Edwards et al. 2015). In general, pH above 7 is considered optimal for crayfish (Strużyński 2007; Table 2). Noble crayfish are most sensitive to adverse environmental conditions (Pârvulescu et al. 2011). The species with the widest range of tolerance is the marbled crayfish, which can occur in waters with both acidic and clearly alkaline reaction (Table 2).

Crustaceans are among the animals with the highest Ca requirements due to their calcified exoskeletons and regular molt cycles (Edwards et al. 2015). The content of calcium ions in water is not a constant value and changes throughout the day, mainly due to changing CO₂ concentration, which is a consequence of respiratory processes of aquatic vegetation (Strużyński 2007). The range of 20–60 mg l⁻¹ is considered optimal for native species of crayfish (Strużyński 2007). Narrow-clawed crayfish were bred with the greatest efficiency in water containing 68 mg l⁻¹ Ca²⁺ (Strużyński & Niemiec 2001). Stable populations of narrow-clawed crayfish, signal crayfish, and spiny-cheek crayfish were observed in tanks with Ca²⁺ content of 37 mg l⁻¹ (Krzywosz & Krzywosz 2002). The highest survival rate in laboratory studies on the growth of red swamp crayfish was observed at 45.5 mg l⁻¹ Ca²⁺, while the fastest weight gain and the most frequent molting were observed at 65.5 mg l⁻¹ Ca²⁺ (Yue et al. 2009). Stable populations of marbled crayfish, on the other hand, were recorded in waters with a concentration of 31.6 mg l⁻¹ Ca²⁺ (Veselý et al. 2017).

Oxygen deficiency can result in large-scale mortality. The most temperature-tolerant species is narrow-clawed crayfish (Table 3), which is physiologically well-adapted to life in stagnant waters, characterized by periodic increases in temperature.

To ensure adequate breeding conditions for commercially important crayfish, the oxygen concentration should be maintained at a minimum of 6 mg l⁻¹ (Broussard & Engineer 1984; Table 4). In the case of spiny-cheek crayfish, the physicochemical parameters mentioned above are of little importance, which means that this species can be found in unclassified waters. In the case of red swamp crayfish, a temperature of 33°C is lethal to adults, while a temperature below 13°C causes growth inhibition (Arrignion et al. 1990; Strużyński 2007 after Suprunovich 1988). When the water temperature drops below 10°C, the development of embryos in eggs is inhibited (Loureiro et al. 2015). Narrow-clawed crayfish is a species that tolerates the lowest water oxygenation of 2 mg l⁻¹, but only in a short period of time (Kozák et al. 2015 after Sládeček 1988; Table 4). Marbled crayfish is a thermophilic species whose reproduction is inhibited when temperature drops to 15°C (Seitz et al. 2005; Pârvulescu et al. 2017). No data are available on the optimal water oxygen content and the range of tolerance for signal crayfish.

Salinity is an important abiotic factor affecting key life processes of animals such as feeding, growth, and reproduction, which determines their long-term survival, distribution and success in ecosystems (Veselý et al. 2017). Few crustacean species have successfully adapted to life in higher water salinity, which makes them all the more interesting in studies involving patterns of ontogeny of osmoregulation in crustaceans (Susanto & Charmantier 1999). Species are generally divided into euryhaline and stenohaline organisms, which reflects their ability to adapt to a wide or narrow range of salinity (Veselý et al. 2017). The red swamp crayfish is the species with the highest tolerance to high salinity (Table 5); only four out of 96 individuals grown for 54 days died during the experiment (Bissattini et al. 2015). In the case of marbled crayfish, intolerance to salinity can significantly reduce its ability to occupy new habitats. For this species, 100% mortality was observed at a salinity of 7 PSU (no data on lower salinity), while no higher mortality was observed in the absence of salinity (Veselý et al. 2017; Table 5).

Noble crayfish is widely regarded as an indicator of clean waters. The species prefers well-oxygenated flowing waters, but is also found in retention and post-mining reservoirs near rivers and streams (Strużyński et al. 2001). Narrow-clawed crayfish are characteristic of lentic waters. Narrow-clawed crayfish and spiny-cheek crayfish are less demanding in terms of substrate. Due to their very light body structure, these two species are adapted to life on a loamy, muddy, slightly muddy or sandy bottom (Haertel-Borer et al. 2005; Strużyński 2007). The situation is quite different in the case of noble crayfish and signal crayfish, whose structure, body mass and biology are similar. These two species prefer sandy and gravel substrates, as well as those consisting of small stones in which they do not sink (Engdahl et al. 2013). Spiny-cheek crayfish is an eurybiotic species that can be found in various types of both lentic and lotic waters, but prefers warm, slow-flowing and still waters, with rich aquatic vegetation and a muddy bottom (Kozák et al. 2015). Populations of this species inhabiting different types of reservoirs do not show significant differences in their development or growth (Ďuriš et al. 2006; Holdich & Black 2007). Red swamp crayfish shows similar substrate preferences as narrow-clawed crayfish and spiny-cheek crayfish. The species occurs in large numbers on loamy and muddy bottoms, where it can successfully dig burrows and tunnels, while avoiding gravel and stony substrates (Hanshew & Garcia 2012). It prefers lentic waters, while in watercourses it occupies places with the slowest current, giving way to noble and signal crayfishes (Bernardo et al. 2011). Marbled crayfish is a very flexible species in terms of environmental conditions. It is found in both lotic and lentic waters with a muddy bottom (Lőkkös et al. 2016), mainly in lakes, canals, streams, shallow ditches, rivers, ponds and around ports (Chucholl et al. 2012).

The disease with the greatest impact on crayfish populations in Poland is the crayfish plague caused by oomycetes (Oomycota) Aphanomyces astaci (Schikora 1906). This disease was brought into Europe from North America in the 19th century (Grabowski 2011). American crayfishes (spiny-cheek crayfish, signal crayfish, red swamp crayfish) and marbled crayfish show high resistance to the crayfish plague (and at the same time are its vectors), in contrast to native species, in which the disease causes high mortality (Unestam 1969, Svärdson 1992). However, if alien species are exposed to stress or impaired immunity as a result of molting, infection with other pathogens or an adverse environment, they may also die (Schrimpf et al. 2013).

The life cycle of A. astaci includes three basic forms: mycelium in host tissues and infectious units found in water, i.e. zoospores and cysts (Svoboda 2015). Mycelium hyphae, growing above the host epithelium, form the so-called primary spores, which shortly after being released from hyphae tips encapsulate and form a clump of tightly adherent primary cysts (Strużyński 2007). After a period of dormancy, the primary cysts release biflagellate zoospores that are able to move actively and demonstrate host chemotaxis (Rantamäki et al. 1992). The chemotaxis response is slow but facilitates the spread of oomycetes (Cerenius & Söderhäll 1992). Zoospores can survive from several days to a week in water and bottom sediments (Unestam 1973). If they encounter a host during this time, they lose cilia and form a secondary cyst that can release further zoospores or germinate, forming a form capable of penetrating the outer lipid membrane of the crayfish epithelium owing to the released enzymes with high lipid degradation capacity (Rantamäki et al. 1991). When zoospore production is inhibited, the spread of the disease stops (Cerrenius & Söderhäll 1992).

A. astaci is represented by five genetic groups that occur in different crayfish species. Group A (genotype As) is present only in native species, group B (PsI) and group C (PsII) are associated with P. leniusculus, group D (Pc) – with P. clarki, and group E (Or) – with F. limosus (Kozubíková et al. 2011). Groups B and C were isolated from signal crayfish, however, group C has only been found in signal crayfish originating from Canada and has not yet been reported from Europe (Ungureanu et al. 2020). In addition, differences in virulence of strains were demonstrated. Group B caused rapid and total mortality of A. astacus in laboratory experiments, while group A was generally less pathogenic (Becking et al. 2015). Although European crayfish are generally very susceptible and usually die within a few days after infection, the evidenced-based evolutionary adaptation of the host and pathogen appears to be the cause of the survival of some A. astacus populations co-occurring with invasive species, e.g. F. limosus and P. leptodactylus, observed in some places (Panteleit et al. 2018). Furthermore, not all invasive species populations (and individuals in infected populations) must be infected with A. astaci (Pârvulescu et al. 2012; Schrimpf et al. 2013), which can prevent native species from being infected.

Crayfish plague has been decimating European crayfish populations for over 150 years, which is why A. astaci from Oomycota is considered as one of the 100 most invasive species in the world (DAISE 2019). Crayfish plague is transmitted by natural diffusion, along with the water current, through infected individuals: people (fishing and fishing gear), fish and other animals, including crustaceans, e.g. alien species of shrimps (Unestam 1973; Strużyński 2007; Mrugała et al. 2019). A. astaci attacks only the soft parts of the epithelial tissue of the crayfish body, as well as cerebral and abdominal ganglia that are part of the nervous system (Nybelin 1936; Kocyłowski & Miączyński 1960). Behavioral changes are also observed, involving increased daily activity, moving along the river banks, going ashore, as well as difficulties in moving and assuming the dorsal position (Kocyłowski & Miączyński 1960). Infection with A. astaci is fatal even at temperatures close to 0˚C (Unestam 1973). The “cotton” mycelium between all segments of the body (Fig. 2A), especially the legs (Fig. 2B), can be observed in individuals of the noble crayfish that died of A. astaci; it can also cover the eyeballs (Fig. 2C), forming a layer containing numerous balls with invasive forms (Fig. 2D; Svoboda 2015).

Figure 2

Thelohaniasis, or porcelain disease, is a serious disease that affects a number of decapod crustaceans, including freshwater crayfish. It is caused by the microsporidian parasite Thelohania contejeani (Sprague & Couch 1971) and was originally described in Europe by Henneguy and Thelohan in 1892 as a causative agent of a disease that caused large losses in crayfish populations. In Poland, T. contejeani infects mainly noble crayfish (Voronin 1971). The disease has also been reported in several crayfish species from different countries (McGriff & Modin 1983). T. contejeani reproduces inside crayfish muscle cells, using them to form spores (Imhoff et al. 2009). The host muscle tissue is continuously infected by successive spore stages, ultimately leading to muscle damage and subsequent death (Strużyński 2007). In the late stage of the disease, the inner side of the abdominal area becomes transparent and white due to the huge amount of white spores released into the muscle tissue (Unestam 1973). In addition to muscles, cysts can also be found in abdominal, limb and various gastric muscles, in the eyestalk, in supraoesophageal ganglion cells, around the gills, hepatopancreas, and haemolymph (Cossins 1973; Cossins & Bowler 1974). Signal crayfish can also be vectors of this disease without showing symptoms of the disease (Imhoff et al. 2009).

The food base is not specific for any crayfish species, but merely regulated by its availability (Smart et al. 2002; Strużyński 2007). Therefore, each population of crayfish of the same species can feed on a different diet, while being omnivorous at the same time (Gutiérrez-Yurrita et al. 1999; Englund & Krupa 2000). It is believed that the type of food consumed by crayfish is a seasonal feature (Pieplow 1938). Crayfish also show cannibalistic tendencies toward smaller individuals, even those closely related, especially when population density is too high and there is not enough food in the environment (Celada et al. 1993; Loureiro et al. 2015). In early spring and late autumn, a wide variety of food of animal origin is the most popular choice. These may include mollusks, aquatic insect larvae, annelids, nematodes, flatworms, tadpoles, fry, other crustaceans, as well as weakened or recently dead vertebrates, such as fish and amphibians (Loureiro et al. 2015), and thus they also fulfil an extremely important sanitary function. At the peak of the growing season, however, crayfish switch to plant food, mainly vascular vegetation, including American waterweed (Elodea canadensis Michaux 1803), hornwort (Ceratophyllum demersum Linnaeus 1753), water-lily (Nuphar sp.) (Strużyński 2007), as well as shining pondweed (Potamogeton lucens Linnaeus 1753), water violet (Hottonia palustris Linnaeus 1753), and plants of the watermilfoil genus (Myriophyllum sp. Linnaeus 1753) (Goszczyński & Jutrowska 1996). They also eat algae of the Chara genus and moss Fontinalis sp. (Tondryk 2001).

The plant cover has several important functions. In addition to its protective function for young individuals who successfully find shelter there during their growth or molting, the vegetation itself serves as a food base, and at the same time as home to invertebrates, which are also part of the crayfish diet (Strużyński 2007). While both native and invasive crayfish (in particular signal crayfish and red swamp crayfish) exert a negative impact on macrophytes, the invasive crayfish tend to have slightly smaller effects (Twardochleb et al. 2013). The negative impact on macrophytes results from the fact that they are consumed, cut and pulled out or unearthed by crayfish individuals. All species of crayfish are most likely to be found near or among dense fields of American waterweed (E. canadensis), hornwort (C. demersum) and Chara sp., whose presence indicates a high content of calcium in water necessary for the proper growth and development of crayfish (Strużyński 2007).

All species of crayfish are a very important element of the food web as a food base for other animals. Crayfish in headwater streams are exposed to predation from two sources: fish and terrestrial predators including wading birds and mammals (Englund & Krupa 2000). Wels catfish Silurus glanis (Linnaeus 1758), European eel Anguilla anguilla (Linnaeus 1758), common perch Perca fluviatilis (Linnaeus 1758), brown bullhead Ameiurus nebulosus (Lesueur 1819) and trout (Salmonidae) cause the most serious depletion in crayfish populations, and the dominance of these species often leads to the disappearance of crayfish populations (Strużyński 2007). Fish predation affects the distribution of different size classes of crayfish in stream pools along the depth gradient, which is an evolutionary response to predator pressure. Fish prey mainly on small crayfish in deep water, and a comparison of the crayfish distribution in pools with and without fish indicates that small crayfish respond to this threat by increasing their use of shallow areas (Englund & Krupa 2000). In order to protect themselves from predators and other crayfish, most crayfish species dig burrows and corridors deep into the banks of watercourses and the shores of reservoirs, which can cause the slopes to collapse and small trees to sink into the water (Gardere 1992). A particular intensification of common perch preying occurs during the period when native crayfish become independent, when common perch individuals wait for juvenile crayfish near burrows or other hideouts, where they stay with a female, and catch them immediately after leaving the shelter (Strużyński 2007). Terrestrial predators feeding on crayfish include: birds, for example: grey heron Ardea cinerea (Linnaeus 1758), great egret Ardea alba (Linnaeus 1758), purple heron Ardea purpurea (Linnaeus 1766) and Eurasian bittern Botaurus stellaris (Linnaeus 1758), as well as mammals, especially the American mink Neovison vison (Schreber 1777) and the Eurasian otter Lutra lutra (Linnaeus 1758) (Englund & Krupa 2000; Strużyński 2007; Loureiro et al. 2015).

Particularly noteworthy is the red swamp crayfish, which has shown high behavioral flexibility in response to the presence of a potential predator. This species proved to use a wider range of information about the increased predation risk than native species, responding more strongly to heterospecific alarm cues (Hazlett et al. 2003). Provided that the prompt detection of alarm substances alerts an animal to the presence of a predator and thus increases the likelihood of avoiding it, this ability can contribute to the success of the species in new environments where new predators may be present; for example, the red swamp crayfish showed that it is capable of learning and remembering associations between different predation risk cues (Gherardi 2006). When trained to associate a new cue [i.e. goldfish Carassius auratus auratus (Linnaeus 1758)] with predation risk following pairing with a conspecific alarm scent, individuals of the invasive species remembered that association longer than native species (Acquistapace et al. 2003). However, alarm substances were found to stimulate feeding-related activities in red swamp crayfish bred in aquaculture ponds (Daniels et al. 2004). This phenomenon suggests that these crayfish, when reared in an environment with reduced predation risks, can respond differently to cues that in more risky habitats inform about the danger and further emphasizes the extreme flexibility of the behavior of this species (Gherardi 2006).

All crayfish species exhibit cannibalistic tendencies toward their own species’ representatives (Loureiro et al. 2015).

There is evidence to suggest that highly invasive crayfish tend to exhibit stronger interspecific aggression toward natives species, thus limiting access to critical resources for competitors (Linzmaier et al. 2018 after others).

The competition between spiny-cheek and marbled crayfish deserves special attention. In agonistic encounters, marbled crayfish were on average more aggressive than spiny-cheek crayfish, even against larger opponents (Linzmaier et al. 2018), which shows that in direct clashes this species can actively displace spiny-cheek crayfish from their habitats.

Red swamp crayfish and signal crayfish can coexist in one river, but due to their different habitat preferences they generally occupy different habitats (Bernardo et al. 2011). In this case, the dominance of one of these species is determined by water temperature, which prevents red swamp crayfish from becoming dominant.

According to Söderbäck (1991), laboratory tests on noble crayfish and signal crayfish show that the latter wins direct clashes with native species, showing more frequent strikes, threats and chases. This applies to both juvenile and adult forms. This shows that the signal crayfish can be a more aggressive and dominant species compared to the noble crayfish. The same is true for signal crayfish and narrow-clawed crayfish. Signal crayfish are more aggressive, more often initiate skirmishes and other interactions, and much more often win fights with narrow-clawed crayfish, effectively repelling them in laboratory conditions (Hudina et al. 2016).