According to the European Union, Regulation No. 1143/2014, a species, subspecies or lower taxa introduced beyond their distribution range should be considered alien taxa. Furthermore, the aforementioned regulation (No. 1143/2014) distinguishes an invasive alien species as one whose introduction and/or spread threatens the biodiversity of native fauna and flora and can cause damage to the economy or adversely affect human health. Invasive alien species may include those that are currently in the process of expansion, as well as those whose populations and range are stable, and even those with declining populations, but still harming nature and/or the economy (Najberek & Solarz 2016). Species of unknown or speculative origin are referred to as cryptogenic. They belong to little-studied taxonomic groups and are often described taxonomically by different names in each new area (Carlton 2009). According to Jaroszewicz (2011), the tendency to spread and colonize new territories is inscribed in the life strategy of each organism, and biological invasion is a phenomenon consisting in the rapid spread of a species (colonization, breeding, further spread, duration and negative impact on fauna and flora) in an area outside its natural occurrence. Currently, species ranges are changing rapidly due to i.a. human activity, and invasive species are expanding their geographic range limits, as demonstrated by comparing current data (GDOS 2018) with e.g. “Atlas of Crayfish in Europe” (Souty-Grosset et al. 2006).
Crayfish belong to the largest and longest-living crustaceans inhabiting freshwater ecosystems (Kozák et al. 2015). In Poland, one can observe both native species of crayfish (noble crayfish and narrow-clawed crayfish) and invasive species (signal crayfish, spiny-cheek crayfish, red swamp crayfish, marbled crayfish). There are five native species of crayfish in Europe (Souty-Grosset et al. 2006):
Body parameters and life expectancy of crayfish
Species | Total length (mm) | Maximum mass (g) | Maximum age (years) | References |
---|---|---|---|---|
200–250 | > 200 | 25 | Collins et al. 1983; Strużyński 2007 | |
150–200 | 150 | 20–25 | Trouilhé 2006; Strużyński 2007 | |
200 | > 200 | 20 | Mastyński & Andrzejewski 2005; Strużyński 2007 | |
122 (female); 111 (male) | * | 5 | Kulmatycki 1936; Pieplow 1938 | |
150 | > 200 | * | Paglianti & Gherardi 2004; Loureiro et al. 2015 | |
103 | > 30.1 | * | Vogt et al. 2015 |
* – no data
First observation (black dots) and distribution (red dots) of invasive crayfish in Poland in January 2020; A –
The objective of the study was to show the role played by abiotic and biotic environmental factors in the interspecific competition between native and invasive crayfish occurring in Poland and to compare the rank of these factors. The knowledge presented in this study will provide a better insight into the issue and may prove beneficial to other countries where a similar set of species occurs.
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).
Optimum pH and tolerance range of crayfish
Species | pH | ||
---|---|---|---|
Optimum | Range | References | |
7.8–8.0 | 4–11 | Pârvulescu et al. 2011; Kozák et al. 2015 after Svobodová et al. 1987 | |
7–9 | 6.8–7.8 | Mazlum et al. 2010; Kozák et al. 2015 after Svobodová et al. 1987 | |
7.8–8.0 | 7.2–9.1 | Hesni et al. 2008; Dobrzycka-Krahel et al. 2017 | |
* | 6.7–9.1 | Kozák et al. 2005; Ďuriš et al. 2006 | |
* | 6.5–8.6 | Smart et al. 2002; Scalici et al. 2009 | |
7.5–8.0 | * | Velisek et al. 2014 |
* – no data
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.
Optimum water temperature and tolerance range of crayfish
Species | Temperature (°C) | ||
---|---|---|---|
Optimum | Range | References | |
20.0 | 1.0–28.0 | Strużyński 2007; Reynolds & Souty-Grosset 2011 | |
17.0–21.0 | 4–32.0 | Karimpour et al. 2011; Reynolds & Souty-Grosset 2011; Kozák et al. 2015 after Svobodová et al. 1987 | |
13.0–23.0 | 1.0–33.0 | Holdich 2002; Reynolds & Souty-Grosset 2011 | |
c. 20.0 | from 10.0 | Pieplow 1938; Dubé & Portelance 1992; Kozák et al. 2015 | |
21.0–29.0 | to 34.0–35.0 | Arrignion et al. 1990; Holdich 2002; Reynolds & Souty-Grosset 2011 | |
18.0–25.0 | * | Seitz et al. 2005; Pârvulescu et al. 2017 |
* – no data
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.
Optimum water oxygen content and tolerance range of crayfish
Species | Oxygen content (mg l−1) | ||
---|---|---|---|
Optimum | Range | References | |
8.0–9.0 | from 3.2 | Mastyński & Andrzejewski 2005; Reynolds & Souty-Grosset 2011 | |
8.0–9.0 | from 2.0 | Mastyński & Andrzejewski 2005; Kozák et al. 2015 after Sládeček 1988 | |
* | from 4.7 | Babović et al. 2011 | |
* | from 3.0 | Souty-Grosset et al. 2006 | |
* | from 2.9 | Lőkkös et al. 2016 |
* – no data
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).
Maximum water salinity tolerance in adult individuals
Species | Water salinity (PSU) | |
---|---|---|
Range | References | |
to 14.0 | Rasmussen & Bjerregaard 1995 | |
to 20.8 | Susanto & Charmantier 1999; Kozák et al. 2009 | |
to 21.0 | Rutledge & Pritchard 1981; Holdich et al. 1997 | |
to 7.0 | Jaszczołt & Szaniawska 2011 | |
to 35.0 | Bissattini et al. 2015; Dörr 2020 | |
to 0.0 | Veselý et al. 2017 |
* – no data
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)
The life cycle of
Crayfish plague has been decimating European crayfish populations for over 150 years, which is why
Symptoms of the plague on dead noble crayfish (after Jiří Svoboda)
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
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 (
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 (
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
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
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).
The red swamp crayfish is tolerant of environments with the lowest pH, which is why it can occur in acidified, unclassified waters and eutrophic reservoirs, as opposed to the noble crayfish, which is an indicator of clean waters (Strużyński 2007; Scalici et al. 2009). Therefore, in the case of deteriorating Polish surface water, the red swamp crayfish will have an advantage over the native species as it will be able to function successfully in conditions unfavorable to other species.
With regard to the content of calcium ions dissolved in water, no clear difference is observed between the species. Therefore, it should not be considered as a factor of greater importance in the interspecific competition of crayfish.
Water temperature and oxygenation are closely related. Thus, species with a wide temperature tolerance range are the same as those resistant to deficiencies of oxygen dissolved in water, which in the face of progressive global warming and warmer seasons gives them a clear advantage over native species that can die as a result of overheating and hypoxia. The highest tolerance to high temperature and low oxygenation is shown by red swamp crayfish (Holdich 2002; Reynolds & Souty-Grosset 2011), while it is worth noting that marbled crayfish is able to survive in reservoirs with an ice cover under which the temperature is 4°C, which enables them to survive winter in Poland (Lőkkös et al. 2016).
Both native and invasive crayfish species, with the exception of marbled crayfish (Veselý et al. 2017), show some tolerance to water salinity. The species with the highest tolerance to water salinity is the red swamp crayfish, which theoretically, similarly to spiny-cheek and signal crayfish, could successfully colonize the waters of the Baltic Sea if not for its thermal limitations.
Noble crayfish and signal crayfish show different preferences for the substrate compared to other species mentioned in this work, which means that their ecological niches do not overlap. Among invasive crayfish, the marbled crayfish is the most flexible in terms of substrate and current selection (Chucholl et al. 2012), hence it can be found in any types of water bodies.
Crayfish plague caused by
All the above-mentioned crayfish species are omnivorous – they can feed on macrophytes and algae, actively prey on zoobenthos or feed on carrion (Englund & Krupa 2000; Loureiro et al. 2015). The type of food consumed by crayfish species is not specific, but depends on its availability (Strużyński 2007). Therefore, it is not a factor significantly affecting competition between crayfish species in Poland.
The vegetation cover has the same ecological function for all the listed crayfish species. However, the invasive crayfish are more likely to destroy and reduce macrophytes present in the environment (Twardochleb et al. 2013), which can lead to a decline in biodiversity in surface waters.
When interacting with predators, the red swamp crayfish shows the most useful adaptations. This species demonstrates a faster and stronger defense response in the presence of a predator than other crayfish species (Hazlett et al. 2003). Red swamp crayfish remember kairomones, which in the event of a re-encounter with a predator will trigger a faster defensive response giving a better chance of survival (Gherardi 2006).
Resistance to the crayfish plague alone gives invasive species a huge advantage over susceptible species, because the former can easily occupy free ecological niches or actively displace weakened and dying native crayfish populations.
In their study, Schrimpf et al. (2013) investigated what contributes to the long-term coexistence of spiny-cheek and noble crayfish in several reservoirs of Central Europe. The authors showed that out of three scenarios, i.e. noble crayfish resistance, reduced pathogenicity of
However, resistance to the crayfish plague alone does not guarantee the invasive success. Only the combination with other factors gives an advantage over other invasive species. Due to its high flexibility and resistance to changing and adverse environmental conditions, the spiny-cheek crayfish effectively complements the niches previously occupied by native crayfish, which give way due to the resulting interspecific pressure and lethal crayfish plague (Holdich & Black 2007). All these factors mean that the spiny-cheek crayfish may in the future become the dominant decapod species in European waters, even though it has no economic significance (Strużyński 2007). Marbled crayfish are as resistant as spiny-cheek crayfish. They can reproduce by parthenogenesis, which gives them a huge advantage over all other species of crayfish, because it does not require the presence of a second individual of the opposite sex to reproduce (Martin et al. 2010). In addition, this species can reproduce several times a year, provided the water temperature does not fall below 15°C (Pârvulescu et al. 2017), which means that with the current climate warming, the range of this species extends to areas of normally lower water temperature.
Not one, but many parallel adaptations determine the invasion success of the species in question. It can therefore be concluded that the more characteristics a given species has, the greater its coverage for the functions of an ecological niche, whether through outnumbering other species or using an unoccupied niche. However, this does not have to be a prerequisite, as one adaptation is possible, which in itself gives a huge advantage over other species.