The Baltic Sea, inhabited by a small number of species and subject to strong human pressure, is susceptible to colonization by new species. As each new species can affect the functioning of marine communities, the importance of each newcomer has to be analyzed individually (Arbačiauskas 2005). It is often the case that interactions between alien and native species are not different from relationships between native species in their natural communities (Reise et al. 2006). Species that colonized the Baltic in the past have become an integral part of this ecosystem.
The spiny-cheek crayfish
In the Baltic Sea, the spiny-cheek crayfish has been reported from the Curonian Lagoon (Burba 2008). The species was present in the Polish coastal waters already in the 1950s (Wiktor 1955).
The species occurs in other Baltic countries such as Latvia (Briede 2011), Germany (Groβ et al. 2008; Martin et al. 2008), the Kaliningrad Oblast, i.e. the part of Russia adjacent to Poland (Burba 2010).
Salinity is a crucial limiting factor for many organisms (Remane 1971; Bonsdorff & Person 1999; Cognetti & Maltagliati 2000). The low salinity of the Baltic waters supports the “natural minimum of species”. With such a small number of species, many ecological niches and habitats are open to newly arrived species (Nehring 2001). In the Baltic, about 70% of alien species occur in the 0-10 PSU salinity zone (Paavola et al. 2005). For many freshwater invertebrates, the salinity barrier separating fresh waters from sea waters is insurmountable. It is important to determine why the spiny-cheek crayfish is present in the Polish coastal zone and to examine whether and how this crayfish can adapt to waters of low salinity. Osmoregulation is a crucial mechanism for overcoming this barrier. At salinity of 8 PSU, the ion ratios characteristic of sea waters are constant, whereas the ion ratios in fresh waters are very variable. While the body fluids of most marine invertebrates have the same osmotic pressure as sea water, their composition and the concentrations of their constituents are different. The body fluids of freshwater invertebrates have a higher osmotic concentration than the surrounding water (hyperosmotic animals) (Lockwood 1977). Osmoregulation involves the movement of ions against the concentration gradient and therefore requires an energy input. Presumably, the energy cost incurred by freshwater organisms when adapting to brackish water conditions is lower than in fresh water. Hence, the osmotic concentration of the body fluids in
Despite its negative influence on the environment, the spiny-cheek crayfish is an attractive pray for many fish, aquatic invertebrates, birds and mammals. It is thus a significant link in the food web (Stańczykowska 1986). Being an omnivore, this crayfish also plays a crucial role in the structure of aquatic ecosystems (Śmietana 2013). Knowing the energy values of male and female spiny-cheek crayfish, one can assess its role in the food web of a given water body and its suitability for consumption on the one hand, and determine how it utilizes the energy contained in its food on the other (Normant et al. 2002), hence when assessing the importance of the spiny-cheek crayfish, one should not take into consideration only its adverse effect on the environment, e.g. on native crayfish species. The introduction of this North American crayfish to Polish waters and breeding it in open water bodies led to unforeseen ecological consequences.
As the species is able to overcome ecological barriers, it continuously extends its distribution range. It is important to define parameters enabling the species to colonize the brackish waters in the coastal zone of the Baltic Sea. Consequently, the objectives of this work were as follows: to confirm the occurrence of
Further research on adaptive capabilities of the species in new conditions, especially in waters of low salinity, are required in the context of the colonization of new water bodies by
The presence of freshwater species in the coastal zones of the seas and saline waters of different water reservoirs is described in the literature. This paper shows data about abilities of freshwater crayfish to survive and thrive in saline waters.
The first information on the occurrence of
Records of spiny-cheek crayfish in the Polish coastal zone of the Baltic Sea in 2002-2014 based on the literature data and personal communications (for details see text)Figure 1
Adult males and females, berried females and juveniles have been found in the Vistula Lagoon, which proves that the species has an established population there.
The Baltic Sea is inhabited by a small number of decapod crustaceans. At the same time, it is exposed to colonization by alien species due to strong human impact (Reise et al. 2006). When conquering new water areas, a distance from the shoreline is crucial (Gruszka 1999; Paavola et al. 2005; Zaiko et al. 2007; Leppäkoski et al. 2009; Preisler et al. 2009). Non-native species have mainly colonized coastal and estuarine zones in the Baltic (Olenin & Leppäkoski 1999; Zaiko et al. 2010), including the Curonian and Vistula Lagoons, the Neva and Oder estuaries, and the Bay of Mecklenburg. In addition to providing suitable ecological niches, these regions are channels along which non-native species can reach the open sea, thereby enabling them to expand their range to as yet uncolonized areas of the coastal zone (Leppäkoski & Olenin 2000). The ratio of alien to native species is 1:40 in oceanic waters, 1:20 in open-sea waters and 1:5 in estuaries and lagoons (Reise et al. 1999; Wolff 2000; Nehring 2006).
In 1890, the spiny-cheek crayfish was introduced for the first time in Europe, to ponds near Barnówko (Lehman & Quiel 1962) (then in Germany, now in Poland). Sometime later, the species escaped into the Oder River. Following the second introduction in the early 20th century, the crayfish was found in the Vistula (Kulmatycki 1935). Afterward, the species expanded its range at a rate of about 10 km per year (Gajewski & Terlecki 1956). In 1900, there were only four localities of this crayfish in Pomerania, while by 1939 the number increased to 23. The species spread rapidly in the second half of the 20th century: in the 1970s, there were 102 localities in Pomerania and by the beginning of the 21st century – more than 800 (Śmietana 2013).
The spiny-cheek crayfish inhabits almost all types of freshwater bodies in Central Europe, and its range covers more than 20 countries (Pöckl et al. 2006; Holdich et al. 2009; Kouba et al. 2014) and is constantly expanding (Pârvulescu et al. 2009; Burba 2010). By the 1960s, the species had already colonized fresh waters in three-quarters of the area of Poland (Leńkowa 1962). At the beginning of the 21st century, only a small area in the south-east of the country remained uncolonized (Krzywosz 2004). It occurs both in large rivers (the Vistula, the Oder) and in fire-fighting reservoirs in large cities (Strużyński & Smietana 1998). It has displaced native crayfish
The successful expansion of the spiny-cheek crayfish can be attributed to its considerable physiological plasticity and the fact that the species is eurytopic. The species shows many characteristics facilitating its fast dispersal and ability to establish new populations (Krzywosz 2004).
The overall length of the animals (TL) was measured over the maximally extended abdomen from the tip of the rostrum to the rear edge of the telson (Kossakowski 1962; Ďuriš et al. 2016; Buřič et al. 2010). The spiny-cheek crayfish occurring in brackish and fresh waters differ in size. The maximum size (121 mm in length) was recorded by Chybowski (2000). The crayfish characterized by large maximum total lengths (118 mm in length) was recorded in the Vistula Lagoon (Skrzecz & Szaniawska 2005) where the salinity is 2-3 PSU. Crayfish occurring in lakes of Warmia had maximum lengths of 110 mm (Kossakowski 1966), those from lakes in the East Suwałki Lake District had maximum lengths of 107 mm, and those from the Masurian lakes were 95 mm long at most (Krzywosz et al. 2014). The maximum total length of the crayfish caught in lakes of Western Pomerania was 105 mm (Śmietana 2013) (Table 1). However, the differences in the maximum size do not always imply the differences in the mean size. We do not have statistically confirmed differences between the maximum size of individuals from various water bodies. It is not possible to compare the impact of fresh and marine waters on the
Maximum total lengths of spiny-cheek crayfish in Polish and other waters
Locality
Maximum length (mm)
Author
Vistula Lagoon (Poland)
118.0
Author’s own study
Lakes in Pomerania (Poland)
109.5
Śmietana 2013
Lakes in Western Pomerania (Poland)
100.2
Śmietana 2008
Lakes in Warmia (Poland)
110.0
Kossakowski 1966
Lake Pobłędzie (northern Poland)
107.0
Krzywosz et al. 2006
Poland
121
Chybowski 2000
lentic waters (Czech Republic)
116.5
Ďuriš et al. 2006
Central lakes (Germany)
107.0
Lieder 1959, after Śmietana 2013
North-eastern lakes (Germany)
110.0
Pieplow 1938
Delaware River (USA)
110.0
Holdich & Black 2007
Lakes in New England (USA)
109.0
Momot 1984
The claws play a crucial role in the aggressive and defensive behavior of crayfish, in intra- and interspecific competitive mechanisms, in confrontations with individuals of the same or another species (Gherardi & Cioni 2004). The spiny-cheek crayfish has smaller claws than native crayfish or the signal crayfish. Individuals with larger claws may have greater chances of survival in confrontations with animals less generously endowed (Martin & Moore 2008).
In the experiments (Staszak & Szaniawska 2006), crayfish were acclimated for 7 days to laboratory conditions (T = 12°C, fresh water, S = 100% aeration, not fed). Each of the 21 animals was kept separately in a tank (21 × 20 × 20 cm). The water in all tanks was aerated. The crayfish were supplied with shelters made of PVC. Each crayfish was supplied with one of the following brackish waters’ food types: animal-based (cod or crayfish abdominal muscle), plant-based (green algae,
Food preferences of Figure 2
Food resources are an important factor determining whether new areas can be colonized and how widespread could be a species in a given water body. Like other crayfish species,
The fact that fodder was the preferred food in the laboratory indicates that artificial food products are most suitable for breeding these animals. Even though in natural conditions cannibalism is not frequent, the abdominal muscle of
Osmotic concentrations were determined microcryoscopically, based on the method used in many studies of osmoregulation (Dobrzycka & Szaniawska 1995; Dobrzycka-Krahel & Szaniawska 2005; 2007). A stereoscopic microscope (NIKON SMZ800) with a polarizing (C-POL) accessory was used to observe the melting of hemolymph crystals. In the experiments (Michałowska et al. 2002), the osmolality of hemolymph increased with salinity. There was a significant increase in the osmolality of hemolymph, from 333.5 ± 82.2 mOsm kg-1 at 0 PSU to 879.5 ± 32.6 mOsm kg-1 at 35 PSU.
Osmotic concentrations of Figure 3
Crayfish can adapt to a wide range of environmental factors (McMahon 1986). At the end of the Mesozoic era, they became independent of the marine environment (Hobbs 1988), becoming adapted to life in fresh waters, although some species preserved the ability to survive in brackish waters (Mantel & Farmer 1983). Andrews (1967) studied seasonal changes in the hemolymph composition of
In the experiments (Jaszczołt & Szaniawska 2011), the animals were kept in aquaria (0.34 m2, V = 117 dm3) with 10 cm long PCV tubes as shelters. The salinity was 3 ± 0.5 PSU and 7 ± 0.5 PSU (T = ca 16°C, Sat > 80%, measured with a WTW Ecoline LF 170 TetraCon 700 probe) and pH was 6.7-8.2 (measured with a WTW ph 197 Sen Tix 97 T probe). The water was filtered, aerated, and illuminated with a low intensity of light until the crayfish larvae hatched, after which a 12/12h photoperiod was applied. The animals were acclimated to the experimental salinity in steps of 1 PSU and 1.5 PSU every other day, starting from an initial salinity of 2 PSU. A recirculating system was used. Natural water with salinity of 7 PSU was pumped into aquaria directly from Puck Bay, while water with salinity of 3 PSU was prepared by diluting the 7 PSU water with tap water. Ten females with pleopodal eggs were kept at each salinity. The young crayfish were separated from their mothers after gaining independence and were individually weighed to the nearest mg one month after hatching. To assess the crayfish growth rate, 50 juveniles (10 groups of specimens from 5 females) from 3 PSU water and the same number from 7 PSU water were used. The growth rate was assessed as the mean increase in carapace length at molt. The young crayfish were weighed to the nearest 1 mg, and their total length (TL) and carapace length (CL) were measured to the nearest 0.5 mm on the basis of photographs, using the Corel Draw 11 program. The increase in carapace length of juvenile specimens was classified into four groups: < 1.0, < 1.5-2.0 >, < 2.5-3.0 > and < 3.5-4.0 > mm. The growth examination lasted 3 months. The young crayfish were fed twice a day with artificial fodder.
No loss or death of eggs were recorded in ovigerous females taken from the environment and kept at salinities of 3 and 7 PSU. Neither of the two salinities influenced the development of eggs or juvenile stages. Berried females survived the exposure to salinities of 3 and 7 PSU, while incubating their eggs and their mortality occurred only after molting. Eggs hatched into stage 1 juvenile, and all molted into stage 2 juvenile. The total number of crayfish hatchlings from 10 females was 1100 at 3 PSU and 827 at 7 PSU. The total mortality of stage 2 juvenile was 1.6% at 3 PSU and 2.5% at 7 PSU. The reduction in the number of juveniles was approximately 50% five weeks after hatching at both salinities.
One month after hatching, the young crayfish varied in length from 9.0 to 13.5 mm at 3 PSU and from 10.0 to 15.0 mm at 7 PSU. The carapace length ranged from 4.5 to 7.0 mm at 3 PSU and from 5.0 to 7.5 mm at 7 PSU. The wet weight was 18-59 mg at 3 PSU and 20-67 mg at 7 PSU. The growth (CL) was 0.5 mm greater in the crayfish at 7 PSU than at 3 PSU (Fig. 4).
Carapace length (CL), total body length (TL) and wet weight (w.w.) for five groups of juvenile (one-month old) crayfish from 3 PSU and 7 PSU (based on Jaszczołt & Szaniawska 2011)Figure 4
During the experiment, 77 molts (among 50 tested crayfish) occurred in 3 PSU and 44 molts (among other 50 tested crayfish) in 7 PSU. Differences in the growth between 7 and 3 PSU were statistically significant (
Increases in carapace length in the class of length < 1.0 mm represented the highest percentage, 58.4% at 3 PSU and 34.1% at 7 PSU, respectively. It was similar in the class < 1.5-2.0 > mm in the same salinities – ca 32%. At salinity of 7 PSU in the classes < 2.5-3.0 > and < 3.5-4.0 > mm, it was 25% and 6.8%, respectively, and was greater than at 3 PSU (9.1% and 1.3%, respectively) (Fig. 5).
Frequencies of increase in carapace length of juvenile crayfish at salinities of 3 PSU and 7 PSU in the different length classes (based on Jaszczołt & Szaniawska 2011)Figure 5
The results showed that the embryonic development, hatching and the development of juveniles were normal at both salinities (3 and 7 PSU), and the body size of individuals was greater at 7 than at 3 PSU.
The spiny-cheek crayfish is capable of reproducing at the age of 1 + and the body length of 5-6 cm (Crome 1955). Mating usually takes place in autumn (Van den Brink et al. 1988; Holdich et al. 2006). Sometimes it takes place in spring (Strużyński 2000). Females do not extrude their eggs after the autumn mating season, waiting for the spring season. After the mating season, crayfish are hidden during daytime and generally less active (Buřič et al. 2009). The female carries from 250 to 400 eggs, and about 100 of them produce hatchlings (Leńkowa 1962; Jaszczołt 2013). According to Holdich et al. (2006),
Water salinity is one of the more important factors affecting the occurrence of aquatic species in newly colonized waters. Adults of the crustaceans
The salinities of 3 and 7 PSU are often quoted as being critical for many aquatic species. Kinne (1971) states that eggs, embryos and reproducing adults are particularly sensitive to salinities of 5-8 PSU. The fact that 100% of the reproducing females survived and that no eggs were deformed or died at 3 and 7 PSU indicates that
This study has demonstrated that at salinities of 3 and 7 PSU, ovigerous females can survive, embryos develop normally, the species has better reproductive success than that described in the literature, and juveniles undergo successive molts in a regular way. These results provide a broad insight into considerable adaptive capabilities of
In adults, the change in salinity to 3 and 7 PSU increases the rate of waste matter excretion and significantly decreases the metabolic efficiency for food consumed at these salinities. On the other hand, there is no change in the rate at which food is consumed (Jaszczołt 2013). This study has shown that salinities of up to 7 PSU do not reduce the occurrence of this species.