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All issues No 425 (2024) Knowl. Manag. Aquat. Ecosyst., 425 (2024) 14 Full HTML
Conservation genetics
Open Access
Issue
Knowl. Manag. Aquat. Ecosyst.
Number 425, 2024
Conservation genetics
Article Number 14
Number of page(s) 11
DOI https://doi.org/10.1051/kmae/2024012
Published online 15 July 2024

© A. Karjalainen et al., Published by EDP Sciences 2024

Licence Creative CommonsThis is an Open Access article distributed under the terms of the Creative Commons Attribution License CC-BY-ND (https://creativecommons.org/licenses/by-nd/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. If you remix, transform, or build upon the material, you may not distribute the modified material.

1 Introduction

Noble crayfish (Astacus astacus) has a threatened conservation status throughout Europe (Jussila and Edsman, 2020). In Finland the conservation status was updated from vulnerable (Edsman et al., 2010) to endangered (IUCN Red List status; EN A2a,b,c,e) (Hyvärinen et al., 2019), but the species is still exploited. The original distribution area of noble crayfish, with the northern distribution limit being roughly at 62ᵒN latitude after the last glaciations (Nylander, 1859; Helle, 1904; Järvi, 1910), has spread northward (Ruokonen et al., 2023). This spread has been aided by anthropogenic establishments as several translocations have been made into many new water bodies up to the latitude 68ᵒN (Westman, 1973; Souty-Grosset et al., 2006; Pursiainen and Rajala, 2009). The translocations have been typical in all Nordic countries, where some exploitable stocks still exist, and the more recent stocking programs have been initiated to stop the declining of populations (Jussila and Mannonen, 2004; Paaver and Hurt, 2009; Dannewitz et al., 2021). As a result, a total of 2.4 million noble crayfish have been introduced or reintroduced into more than 1 000 water bodies between 1989–2021 in Finland (Ruokonen et al., 2023). In addition, numerous not recorded stockings have also occurred.

A National Crayfish Strategy, implemented by the Finnish Fisheries Authority first in 1989 (Kirjavainen, 1989) and renewed in 2000 (Mannonen A, Halonen T, TE-keskusten työryhmä, 2000), in 2013 (Ministry of Agriculture and Forestry, 2014), in 2019 (Erkamo et al., 2019) and in 2023 (Ruokonen et al., 2023), has guided the management and conservation of noble crayfish, and defined and re-defined the geographical limits for previously licensed introductions of alien signal crayfish (Pacifastacus leniusculus). Stockings and farming of signal crayfish were banned in 2014 in European Union legislation (EU Regulation on Invasive Alien Species 1143/2014), entered into force in 2015 together with the national regulation and implement to the national crayfish strategy in 2019 in Finland (Erkamo et al., 2019). However, these national strategies are without any legislative force, and the nature of these strategies has received criticism from stakeholders (Ruokonen et al., 2018; Jussila and Edsman, 2020; Jussila et al., 2021).

National Crayfish Strategy 2023–2032 (Ruokonen et al., 2023) defines the protection areas to preserve the noble crayfish populations (i.e., water basins without known signal crayfish), and the management area that includes the water basins currently with signal crayfish. Current distribution of alien signal crayfish is remarkably overlapping with the original distribution range of noble crayfish (Ruokonen et al., 2023). Numerous illegal stockings of signal crayfish, along with crayfish plague (Aphanomyces astaci) outbreaks, have caused ongoing threat for the noble crayfish populations (Westman, 1991; Jussila and Mannonen, 2004; Souty-Grosset et al., 2006; Pursiainen, 2012; Ruokonen et al., 2018; Jussila and Edsman, 2020; Jussila et al., 2021; Ruokonen et al., 2023). In addition, changes in the fragile aquatic habitat can cause increased mortality, emigration, reduction in growth rate and production, and problems in reproduction for noble crayfish (Mannonen and Westman, 1998).

Previous studies concerning the noble crayfish genetic diversity in Finland are based on the microsatellite-like repeat located in the internal transcribed spacer 1-region (ITS1) indicating some genetic heterogeneity and characteristic fragmentation (Alaranta et al., 2006, see also Edsman et al., 2002; Alaranta et al., 2011a), and on the novel microsatellites showing some genetic heterogeneity (Gross et al., 2013). However, these studies are focused more to the development of the genetic analyses and included only limited number of Finnish populations. In addition to these data, the mitochondrial cytochrome oxidase I (COI) gene was used to assess genetic diversity of a total of 55 Finnish populations; however, no genetic variation was observed (Makkonen et al., 2015), and the single haplotype detected from all analysed individuals was the most common found in whole Europe (Schrimpf et al., 2011; Schrimpf et al., 2014). The colonization history and human translocations show significant role in noble crayfish populations in Fennoscandia. It has been suggested that the postglacial recolonization of Fennoscandia involved two independent colonization events following separate routes from a common refugium in south-eastern Europe (Dannewitz et al., 2021; see also Schrimpf et al., 2014; Gross et al., 2021). In Europe, populations have experienced significant declines, caused by anthropogenic pressures on the habitats, together with climate change and the spread of invasive species (Lovrenčić et al., 2022). However, except study based on the COI haplotype variation (Makkonen et al., 2015), the previous studies have not comprehensively covered the distribution range of noble crayfish in Finland, and therefore implications to the conservation and management have mostly been lacking.

The aims of this study are 1) to assess the genetic diversity of noble crayfish in Finland based on ITS1 microsatellite-like repeat variation, and 2) to assess the possible existence of autochthonous populations with implications for the future conservation and management of the species in Finland.

2 Materials and methods

2.1 Samples

Noble crayfish samples were collected by trapping, in collaboration with local fishermen, during the crayfish trapping seasons (from late July to late October) in 2004. In addition, previously collected samples from Lake Iso-Lauas population (sampling year 1995) and Lake Mäntyjärvi population (1997) were also included to this study. The stocking histories of the populations were obtained from the local fishermen, government’s fisheries authority and from the literature. A total of 1140 individual samples (10–69 crayfish from each site), were collected and analysed from a total of 38 water systems (Fig. 1, Tab. 1). Nine populations were locating within original distribution area below latitude 62ᴼN (Järvi, 1910) while 29 populations were located in more northern areas (Tab. 1). A total of eight populations were from a drainage basin within a current protection range (Ruokonen et al., 2023) and one out of those was locating within original distribution area (Fig. 1, Tab. 1).

thumbnail Fig. 1

Geographical distribution of 38 sampled noble crayfish populations. Eight populations with p-values < 0.05 (PDT) in paired comparison (see Tab. 3) are marked with circle, and eight populations locating in the protection area (Ruokonen et al., 2023) are marked with asterisk (*). Map © Maanmittauslaitos.
Table 1

Noble crayfish populations, location, size of the water system (ha), drainage basins code with an asterisk (*) if within protection area (Ruokonen et al., 2023;), number of samples, historical information, and findings from previous genetic analyses.

2.2 DNA extraction

Individual DNA was extracted from the walking leg muscle removed by using sterile wooden toothpick by using protocol described in Alaranta et al. (2006). DNA concentration was measured using spectrophotometer (NanoDrop® ND 1000) and DNA extractions were stored at − 70 ᵒC.

2.3 PCR, ITS1 fragment analysis and Population Divergence Test (PDT)

PCR was performed using the primers Asa1F (5’-tca ctc cgt cag cag tga gtc gct- 3’; Cy-5 labelled) and Asa1R (5’- gag tca aga cgt gca gcc tag gcc c-3’) (Edsman et al., 2002), ranging fragment sizes from 162 bp to 216 bp. Laboratory protocol and PCR reaction are described in Alaranta et al. (2006). In ITS1 fragment length analyses the PCR products were loaded to the Hydrolink Long Read 6% gel and the fragment lengths were separated by using ALFexpress automated sequences. CY-5 labelled external size markers (50–250 bp in 50 bp intervals) and two internal size markers (50 bp and 250 bp) were used. Fragment sizes were determined by using ALFwin Fragment Analyser (Pharmacia Biotech).

The population Divergence Test (PDT) measures differences between populations based on the frequencies of the fragments, and it produces probabilities (p-values from 0 to 1) expressing the difference between two populations in paired comparison (p-values < 0.05), identical populations having p-value 1. PDT is described more detailed by Edsman et al., (2002). PDT was performed in the Laboratory of Molecular Systematics (Swedish Museum of Natural History, Sweden).

3 Results

3.1 Genetic analyses

The amplified ITS1 fragment lengths varied from 168 bp to 216 bp. The following local fragments were observed from only one population: fragment of 214 bp (frequency of 3%, Lake Viitajärvi), fragment of 172 bp (frequency of 7%, Lake Mäntyjärvi), fragment of 180 bp (frequency of 4%; Lake Saimaa) and fragment of 216 bp (frequency of 19, Lake Linkullasjön) (Tab. 2).

Numbers of different fragments in a fragment profile varied from five (Lake Ahvenlampi) to 13 (Lake Saimaa) within populations and relative frequency of samples with unique fragment profiles within population from 17% (Lake Ahvenlampi) to 88% (Lake Saimaa) (Tab. 2).

According to PDT, the following eight populations differed (p-values < 0.05) from the other assessed populations in paired comparison: River Perhonjoki, Lake Ahvenlampi and Lake Suuri-Heinäjärvi, all locating within the protection area (see Ruokonen et al., 2023) but outside of the original range, Lake Koivujärvi and River Kasijoki locating in the management area outside of the original range, Lake Suuri-Vahvanen and Lake Köyliönjärvi locating within the original distribution area, and finally Lake Linkullasjön locating within the original distribution area and in the current protection area (Fig. 1, Tabs. 2 and 3). The remaining 30 populations showed no statistically significant differences (p-values > 0.05) in paired comparison with one (e.g., River Pajakkajoki together with seven populations) or up to 12 populations (Pond Valkeinen) (Tabs. 2 and 3).

Table 2

Population Divergence Test (PDT) results based on ITS1 microsatellite-like repeat variation; populations with no statistical difference (PDT p > 0.05) in paired comparison (see p-values in Tab. 3.), and relative frequency (%) of different ITS1 fragment profiles within population, total number of fragments within population and local fragments (bp) if detected with the frequencies.

thumbnail Table 3

The results from the Population Divergence Test (PDT). Numbers present p-values for probability of difference between the tested population pairs. Differences (p-values < 0.05) are highlighted in grey.

4 Discussion

The determination of genetic structure, e.g., ITS-fingerprints, of natural and managed populations forms a basis for conservation genetics that generally aims to conserve and restore the biodiversity (Coates et al., 2018). Genetically different populations are suggested as candidates for special management efforts to prevent the loss of unique genetic variants (Dowling and Childs, 1992). Therefore, management strategies are, or should be, focused to preserve genetic diversity within populations while separate stocks are recommended to be managed as distinct conservation units (Souty-Grosset et al., 1997). Considering the conservation and management of noble crayfish, the local populations may be better adapted to their local environment and introduction of genetically different individuals could adversely alter the gene pool (Souty-Grosset et al., 1997).

The populations with naturally high levels of genetic variation are thought to be capable to adapt more successfully to environmental changes while lack of genetic variation makes populations more vulnerable (Grandjean and Souty-Grosset, 2000). In addition, introductions by using small number of individuals can cause a strong bottleneck effect, and small populations are most likely to be affected by the loss of genetic variation due to the excessive harvest because of their small effective population size (Ryman et al., 1995). Knowledge of genetic and geographical origin is a key for effective conservation and sustainable exploitation. The lack of knowledge on the genetic structure may lead to the genetic contamination or homogenization of local populations (Largiadèr et al., 2000; Gross et al., 2017) and for the noble crayfish this has been already seen in other Baltic Sea area countries (Gross et al., 2013; Dannewitz et al., 2021; Gross et al., 2021).

In our study, a total of 30 out of 38 analysed populations showed no genetic difference with one or up to 12 populations in paired comparison. These results support the previous findings, based on COI-gene haplotype variation (Makkonen et al., 2015) and microsatellites (Gross et al., 2013; Dannewitz et al., 2021), indicating, in general, that the genetic diversity of noble crayfish in its northern distribution range, including Finland, is remarkably narrow due to the homogenizing effect caused by past crayfish introduction policies.

Interestingly, we were able to detect a total of eight noble crayfish populations that had statistically significant difference with all other analysed populations indicating as least some level of remaining heterogeneity. This finding might be, depending on the location of the population, also an indication of an autochthonous origin or autochthonous donor. Nevertheless, due to the introduction policy in the past the determination of autochthonous origin is not always unambiguous. It should be noted that stocking histories in Finland are impossible to assess comprehensively, as noble crayfish are inhabiting thousands of waters, and millions of individuals have been introduced. Our results here, however, could be used as a base for future analyses.

Criteria for determination of an autochthonous origin suggested here, based on the background information and results of this study, are 1) population is locating within original distribution range e.g., below the 62ᵒN latitude (Järvi, 1910), 2) statistically significant genetic difference with other analysed populations and 3) history of the populations observed from fisheries authority and local fishermen reveals no anthropogenic disturbance, e.g., introductions. The present data supports our preliminary findings (Alaranta et al., 2006) indicating Lake Linkullasjön population being possible solely autochthonous or it was established from autochthonous donor population since its location within original distribution area. In addition, Lake Köyliönjärvi and Lake Suuri-Vahvanen populations are locating within original distribution area but with some known anthropogenic disturbance. In addition, River Perhonjoki, Lake Ahvenlampi, Lake Suuri-Heinäjärvi, Lake Koivujärvi, River Kasijoki populations are located outside of the original noble crayfish distribution range and therefore they are most likely established.

We were also able to detect variation within populations, as for example majority of Lake Saimaa individuals (88%) showed individual fragmentation and the population showed the highest number of detected fragments. This is possibly due to the effect of one or multiple stockings of the presence of subpopulations due to the size of the water area (Lake Saimaa, 4 400 km2, one sampling site). In addition, Lake Ahvenlampi individuals were most homogenous: 83% of samples showed the identical fragmentation and the lowest number of detected fragments within population indicating a bottleneck effect as a possible consequence of establishing population with a low number of individuals from a single donor population. Individuals displayed distinctly different fragment patterns also within Swedish populations in previous analyses (Edsman et al., 2002). Harris and Crandall (2000) found considerable intragenomic variation in the genera Procambarus and Orconectes (Faxonius), even to the extent that variation within individuals exceeded that between different species.

In this study local e.g., private fragments, as described in Alaranta et al. (2006), were found from five populations with frequencies varying from 3% to 7%, except in Lake Linkullasjön, where local fragment frequency was 19%. Fragment of 214 bp (Lake Viitajärvi) was neither observed in other populations in Sweden nor in Estonia (Edsman et al., 2002; Alaranta et al., 2006). The fragment of 180 bp present in Lake Saimaa has earlier been found in some Estonian samples (Alaranta et al., 2006) and in one population from Montenegro (Edsman et al., 2002), while 172 bp present in Lake Mäntyjärvi has been found in one Swedish and Estonian population, and 216 bp (Lake Linkullasjön) in one Estonian population (Alaranta et al., 2006). Shared fragments are one indication of shared origin and sign of human-made translocation. The presence of local fragments is interesting, however, as seen here the existence is highly dependent of the number of populations compared.

Historical information proved to be extremely valuable when assessing the genetic data, however, it is usually lacking from the official records. According to our data, Lake Linkullasjön shows divergence in paired comparison, presents a local fragment and approximately 50% of the samples share the same fragmentation. Lake Linkullasjön is a privately owned small lake (60 ha) in South Finland (noble crayfish natural range) with good availability of historical information provided by the owner of the property. Based on the location and known history of Lake Linkullasjön as well as on the base of our previous (Alaranta et al., 2006) and current results, we suggest that population in Lake Linkullasjön might be of an autochthonous origin. However, individuals from Lake Linkullasjön share a local fragment with Estonia samples (Alaranta et al., 2006), and according to microsatellite analysis made by Gross et al. (2013) Lake Linkullasjön population tended to be genetically similar to Swedish populations rather than other analysed Finnish populations, indicating Swedish origin. Transfers of crayfish are known to have occurred across the Baltic Sea in both directions (Alm, 1929; Edsman, 2004). As a second example, established Lake Iso-Lauas population (Oksman and Lindqvist, 1977) shows no difference with 10 populations in paired comparison with geographical distant populations (distances varying from 20 km to 200 km). Results from Lake Iso-Lauas population indicate anthropogenetic effects due to the absence of local fragments and prominent level of individual fragmentation (63% of samples). According to local fishermen, prior crayfish plague outbreaks in 1996 and 2000 (Mannonen et al., 2006), Lake Iso-Lauas had produced a massive number of crayfish not reaching the consumable size of >10 cm (total length). Best catchments, with no consumable value, were up to 1 000 crayfish/day/fishermen. Therefore tens of thousands of small sized crayfish were sold for stocking; however, this data (Lake Iso-Lauas population acting as a donor) is totally lacking from the official stocking records (Korhonen, 2010).

Most common method of managing crayfish population has been, and still is, stockings: introduction to new areas, reintroductions to the areas where they have become extinct and restocking to boost existing populations. As perspective in the species level conservation, the creation of large-scale conservation areas has been discussed in Scandinavian countries (Mannonen and Westman, 1998; Mannonen et al., 2000; Edsman and Schröder, 2009) and launched also in Finland (Ministry of Agriculture and Forestry, 2014; Erkamo et al., 2019; Ruokonen et al., 2023). However, the current protection area in Finland is mainly outside of the original distribution range (Ruokonen et al., 2023), and the conservation efforts are focused now more on species, not on genetically distinct populations. In Europe, among the established populations the idea of catchment-specific gene pool is supported (Weiss et al., 2002; Schrimpf et al., 2014). Therefore, each catchment could be managed as a distinct unit in the original area of distribution while known established populations, located outside of the natural range, could be managed as one unit. As suggested by Vrijenhoek et al. (1985), genetically similar populations should be concerned and treated as a single population in management purposes.

Ideally, especially for conservation purposes, suitable habitat for introduction or re-introduction is geographically isolated location from other surface waters and human activities within natural dispersal range of the species (Peay, 2009; Alaranta et al., 2011b; Reynolds and Souty-Grosset, 2012). In addition, smaller refugee areas e.g., ark-sites, locating in a natural range have been applied in Europe to preserve indigenous freshwater crayfish populations (Holdich et al., 2004; Peay, 2009; Souty-Grosset and Reynolds, 2009; Lovrenčić et al., 2022). Idea of ark-sites has been taken forward in United Kingdom (Sibley et al., 2007) and Ireland (Horton, 2009) to protect white clawed crayfish (Austropotamobius pallipes), and in Finland to protect noble crayfish in state-owned areas (Alaranta et al., 2010; Alaranta et al., 2011b). This approach is also promoted in the current national crayfish strategy in Finland (Ruokonen et al., 2023). However, this approach, which is claimed to be the most suitable for the population level conservation, demands for detailed knowledge of genetic structure of the donor populations (Holdich et al., 2004; Peay, 2009; Souty-Grosset and Reynolds, 2009) and, as shown in this study, sufficient background information of the donor population. Also, more information is needed about suitable refugee habitats in original distribution area including existing conservation areas e.g., national parks as suggested by Alaranta et al. (2010), with the existence of noble crayfish within those waters. In national parks, fishing and other human activities are controlled or prohibited, and therefore, the spreading of crayfish plague due to human activity is highly restricted. However, further conversations and involvement of all national stakeholders would be highly needed to reach the comprehensive understanding to support the coordinated actions to the future conservation and management of noble crayfish in Finland.

As a conclusion, autochthonous populations still seem to exist in Finland, at least in some special locations with limited human interactions. Due to the anthropogenic disturbance and associated signs of the narrowed genetic variation (Gross et al., 2013; Makkonen et al., 2015; Dannewitz et al., 2021), we suggest that in Finland noble crayfish population should ideally be divided into catchment specific units, or if not possible, at least into two main conservation and/or management units; 1) native populations (within the original range, no stocking) for conservation, and 2) established populations for management. In addition, suspected autochthonous populations should be treated each as separate conservation units. For more detailed grouping, the analyses by using novel microsatellites would be needed (Dannewitz et al., 2021; Gross et al., 2021). In addition, it would be essential to better identify autochthonous and native populations since the human made translocations have caused remarkable unnatural genetic mixing of the populations. As seen in the present data, autochthonous populations e.g., population in the original distribution area without any unnatural genetic disturbance, seems to be very rare in Finland, while historical information is crucial for interpreting genetic data accurately. Secondly, due to the lack of information of the occurrence of the species, especially in the small size water bodies and subpopulations in large water bodies, monitoring programs within original range, designated protection area, and natural parks is highly recommended. The new genetic tools, e.g., eDNA applications (see Beng and Corlett, 2020; King et al., 2022), have shown potential in monitoring of aquatic systems in providing precise information about distribution and population size (Bohmann et al., 2014; Takahara et al., 2013). These tools have been already tested in Finnish conditions with promising results (Mäkinen et al., 2021). In addition, combinations of methods e.g., fine scale phylogenetics, population genetics with novel microsatellites and species distribution modelling (Lovrenčić et al., 2022) might be possibly used to assist the conservation actions needed. As a perspective of species conservation, preserving genetic variation and biodiversity is crucial for the evolutionary potential and sustainable exploitation of noble crayfish. Despite advancements in genetic analysis and genotyping methods, caution is needed due to potential risks in data interpretation (Selkoe and Toonen, 2006). Utilizing modern crayfish-specific population models is also recommended (Koivu-Jolma et al., 2023). To secure the evolutionary potential of noble crayfish stocks in Fennoscandia, it is essential to preserve genetic variation and biodiversity, in collaboration and involvement with all the national stakeholders. This would provide a solid base for effective conservation and potentially sustainable exploitation for the future decades.

Acknowledgements

We would like to thank Arja Korhonen from A.I. Virtanen institute (University of Eastern Finland, Kuopio campus) for the ALFexpress runs and Steve Farris from Laboratory of Molecular Systematics (Swedish Museum of Natural History, Sweden) for the Population Divergence Test. We are grateful to Paula Henttonen, Jenny Makkonen, Joose Raivo and Jaakko Haverinen for the valuable comments on the manuscript. Also, we would like to thank Linda Korhonen and everybody who has helped us to collect samples and information on the history of noble crayfish populations. The laboratory analyses of this study were conducted 2004–2006 and supported by the Ministry of Agriculture and Forestry and the grants from The Finnish Cultural Foundation and The Kuopio Naturalists’ Society.

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Cite this article as: Karjalainen A, Halmekytö M, Mononen J, Kortet R, Kokko H. 2024. Genetic diversity of noble crayfish in Finland based on ITS1 microsatellite-like repeat variation: implications to the conservation and management. Knowl. Manag. Aquat. Ecosyst., 425, 14.

All Tables

Table 1

Noble crayfish populations, location, size of the water system (ha), drainage basins code with an asterisk (*) if within protection area (Ruokonen et al., 2023;), number of samples, historical information, and findings from previous genetic analyses.

In the text
Table 2

Population Divergence Test (PDT) results based on ITS1 microsatellite-like repeat variation; populations with no statistical difference (PDT p > 0.05) in paired comparison (see p-values in Tab. 3.), and relative frequency (%) of different ITS1 fragment profiles within population, total number of fragments within population and local fragments (bp) if detected with the frequencies.

In the text

All Figures

thumbnail Fig. 1

Geographical distribution of 38 sampled noble crayfish populations. Eight populations with p-values < 0.05 (PDT) in paired comparison (see Tab. 3) are marked with circle, and eight populations locating in the protection area (Ruokonen et al., 2023) are marked with asterisk (*). Map © Maanmittauslaitos.
In the text
thumbnail Table 3

The results from the Population Divergence Test (PDT). Numbers present p-values for probability of difference between the tested population pairs. Differences (p-values < 0.05) are highlighted in grey.
In the text

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