Pseudorasbora parva (Temminck & Schlegel, 1846): A New Threat to Fish Biodiversity in Ordu Province (Middle Black Sea Region)

The invasive fish species pose a significant threat to both local fish species and aquatic habitats. During the field surveys, an invasive fish species Pseudorasbora parva was found for the first time in Ulugöl (Ordu). In the field studies, 41 P. parva individuals from different size groups were captured. Total length (TL), fork length (FL), standard length (SL) and weight (W) of this invasive species which continuously increase distribution in Turkish inland waters were recorded. The average TL, FL, SL and W values of the P. parva were 7.24±1.2 cm (3.8-9.4 cm), 6.52±1.1 cm (3.4-8.4 cm), 5.73±0.9 cm (3.0-7.1 cm) and 3.24±1.4 g (0.4415-6.8632 g), respectively. P. parva species was reported as the first record in Ordu (Middle Black Sea Region). The increase in the number of P. parva individuals in Ulugöl is a great threat to Ordu fish biodiversity.


Introduction
Turkey is one of the very rich countries in terms of freshwater ichthyofauna due to the geological position and topographic structure (Tarkan et al. 2015;Çiçek et al. 2018). 409 fish species were reported in the inland water of Turkey. Among these fish species, 194 are endemic and 28 are non-native species for Turkish inland waters (Çiçek et al. 2015; Çiçek et al. 2018).
Maintaining biodiversity in natural and artificial habitats is vital for a sustainable environment and future. The freshwater fish fauna is under threat due to many different reasons such as numbers of water canals and dams in the system, domestic waste, introduction of invasive species, uncontrolled pesticide use, and habitat degradation (Özuluğ et al. 2013;Tarkan et al. 2015). These activities increase the negative effect of feeding, breeding and sustaining the species of fish which are found naturally in the freshwater source, or cause a decrease in the population or the continuity of the generation .
Invasive species have many negative impacts on ecosystem, local and national economies as well as their negative effects on food and habitat competition, predation, hybridization, disease and parasites transport on native species (Kennard et al. 2005;Ekmekçi and Kırankaya 2006). Easy adaptation to environmental conditions, early sexual maturation, successful reproductive strategies and wide nutritional tolerance play an important role in the success of invasive species spreading into habitats (Carman et al. 2006).
Topmouth gudgeon, Pseudorasbora parva (Temminck & Schlegel, 1846) which is a member of the Cyprinidae family, are freshwater fish of Asian origin and they can find in many different freshwater habitats (Banarescu 1999). It is widely spread in lakes and ponds which are very rich in terms of water plants (Kottelat and Freyhof 2007). P. parva mouth is upward, small and has no barbels around it. Their caudal fin is homocerc. The most prominent feature is the black band that starts right behind the head and extends to the caudal. During the breeding period, small tubercles are found in the head region of the P. parva as in many carp. In addition, during this period, pigmentation on the outer part of the scales becomes darker in males and therefore male and female individuals are more easily discriminated (Froese and Pauly 2018). The species is usually 2 cm to 7.5 cm in length it can reach up to 12.5 cm in length. According to the IUCN criteria, P. parva is considered Least Concern (LC) (Huckstorf 2012).
P. parva which is an invasive fish species was reported in the Thrace region in 1982 for the first time in Turkey (Erk'akan 1984). This fish species, which has many invasive features, has spread rapidly to many Turkish freshwater basins (Çetinkaya 2006;Ekmekçi et al. 2013;Özuluğ et al. 2019). However, there is no record of P. parva in the freshwater habitats in the Ordu. Unfortunately, a new record has been added to the distribution areas of P. parva which is known as one of the most important invasive freshwater fish species of Turkey.

Materials and Methods
Ulugöl is a small lake located in Ulugöl Nature Park in Gölköy district of Ordu province. Ulugöl has an area of 39 decares with 5-20 m depth at an altitude of 1200 m. This lake is formed as a result of the accumulation of water in the space formed by the landslide mass, the formation form is very different from the landslide lakes in the Black Sea Region (Taş et al. 2010). Carp (Cyprinus carpio) and endemic Abant trout (Salmo abanticus) which were released in 2007 during the stocking activities trout live in the Ulugöl (Anonymous 2012a; Anonymous 2012b).
The fish samples were captured using the electrosocker at along the Ulugöl lakeshore from the (Ordu) at 40°37'48''N and 37°32'46'' E coordinates ( Figure 1). The captured fish samples were brought dead to the Hydrobiology laboratory at Ordu University with the fish transport containers. All fish samples were identified using different studies (Kuru 1980;Kottelat and Freyhof 2007) and identification keys. Then, the sex determinations of these samples were made both microscopically and macroscopically according to their size. Some meristic and metric characters such as fish weight (nearest ±0.1 g), total length, fork length and standard length (nearest ±0.1cm) were measured for each P. parva samples. The weight-frequency and lengthfrequency distributions were determined.

Results
In this study, 41 P. parva were caught from different parts of the Ulugöl (Ordu) during the fieldwork (Figure 2). Maximum and minimum values of total length, fork length, standard length and weight of the samples with mean and standard deviation 3.8 cm and 9.4 cm (7.24±1.2), 3.4 cm and 8.4 cm (6.52±1.1), 3.0 cm and 7.1 cm (5.73±0.9) and 0.4415-6.8632 g (3.24±1.4), respectively. The male and female P. parva samples from Ulugöl are shown in Figure 2.
It was determined that P. parva fish samples from Ulugöl were 60.97% female and 39.03% male. As a result of t-test, there was no statistical difference between weight and length values of male and female samples (P>0.05). P. parva fish fin rays formulas are determined as Anal: III 6, Dorsal: II-III 7-8, Pektoral: I 8-12, and Ventral: I 7-8. The line lateral scales of the samples are between 36-40 and the pharyngeal teeth are 5-5. In the current study, we also examined the length and weight frequency of this invasive fish species. The weight-frequency and length-frequency distributions were presented in Figure 3.

Discussion
The introduction of invasive fish species into new aquatic environments in different pathways such as natural introduction, human introduction and involuntary introduction has dramatically increased the damage to these habitats. The existence of P. parva invasive species was recorded for the first time in Ulugöl (Ordu). The determination of the presence of P. parva is a major problem for both Ulugöl natural life and Ordu fish biodiversity. Male and female individuals belonging to different size groups have been captured (Figure 2). It proves that this species adapts to the Ulugöl and has successfully bred in the Ulugöl. Although 41 samples were captured in the sampling period, they were visually observed in an excessive amount of this species. P. parva can easily settle when transported to a reservoir in any way and it can be destructive for the other fish species due to its parasites (Andreou and Gozlan 2016). P. parva have also negative impacts on the native fish fauna via competition foods, spawning areas, and other sources ). C. carpio and S. abanticus inhabited in the Ulugöl (Anonymous 2012a; Anonymous 2012b). Therefore, it is important to investigate the relationship of P. parva with C. carpio and S. abanticus in Ulugöl fish fauna and its effects on these economic fish species. In many studies, control activities were focused on the destruction of P. parva from natural waters in some European countries, especially in the UK (Britton and Brazier 2006;Britton et al. 2010). This is the new record for the distribution of P. parva in Ordu inland waters. Since 1984, P. parva has expanded the distribution areas within 35 years and has established successful populations in Turkish inland waters. In the studies it is clear that P. parva quickly spread to Turkey inland waters (Table 1). P. parva was accidentally introduced into the Ulugöl in the course of stocking with C. carpio. In addition, many amateur fishing activities are carried out in Ulugöl, and local and traditional fishing competitions with competitors from different regions are organized. It is thought that P. parva may be spread by hunting or fishing activities used in different watersheds. In order to prevent the spread of this fish species in the inland waters of Ordu, flyers and leaflets can be a useful way of promoting public awareness about the invasive fish. In addition, people and fishermen in that area should be informed about the fishing gear used in fishing in Ulugöl not to be used in other ecosystems.
Invasive freshwater fish species continue to increase steadily in many freshwater habitats (İnnal 2012). There are many reasons for the high success of P. parva species in the Turkish inland waters such as reproduction activity rate during the breeding season, sexual maturation at an early age, relatively large eggs, male guarding eggs and short life cycle of the species (Ekmekçi and Kırankaya 2006). Ekmekçi and Kırankaya (2006) reported that P. parva can lay eggs in branches, leaves, plastic waste from the habitats. Therefore, when the consider the problem of the Ulugöl with aquatic plants, it is observed that this contributes to increase in the number of P. parva compared to other fish species in the habitat.
The reduction of biodiversity or the disappearance of certain species makes biological resources unusable and useless. On the other hand, when it comes to genetics, biodiversity becomes even more important. Biotechnological developments that will benefit human beings and ecosystems in the future depend on the wealth of gene pools of biological resources (Polat et al. 2011). Considering studies related to Turkish ichthyofauna, information for these destructive effects on the aquatic ecosystems of invasive fish species which increases the distribution area in Turkish inland waters is quite limited (Özuluğ et al. 2013). In order to avoid irreparable losses in fish biodiversity of Turkey, the distribution areas of these invasive species should be identified. Necessary management actions should be given to the fisheries studies about identifying possible mechanisms of invasive fish action on native fish species in the habitats such as disease, hybridization, food and habitat competition. Because of that the necessary steps against the occurrence of the invasive species and the species should be monitored in the habitats.