Reproduction of Potamothrix hammoniensis (Oligochaeta) in shallow eutrophic lakes

Potamothrix hammoniensis is one of the dominant species of Oligochaeta, abundantly inhabiting European waters up to Siberia (Grigelis 1990). The taxon is relatively rare in south-western France and in Spain (Martinez-Ansemil, Prat 1984). Although this typical pelophilous species prefers eutrophic waters, it is also found in oligotrophic lakes (Lang 1984). The high tolerance of this taxon in relation to habitat conditions is also evident in its frequent occurrence in lakes of various depths. According to Wiśniewski (1978), P. hammoniensis often dominates in all areas of the bottom in deep stratified lakes of central and northern Poland, being usually the only representative of this group of animals in the profundal zone, even at great depths. On the other hand, Żbikowski (2011) found overwhelming dominance of this species also in shallow eutrophic lakes.

The consequence of the mass occurrence of Potamothrix hammoniensis is the significant impact of the species on the functioning of aquatic ecosystems. It is an important element of the food base of predatory invertebrates and benthic fish (Jónasson, Thorhague 1976). In addition, through bioturbation (Svensson et al. 1998), modification of oxygen conditions at the lake bottom and change in the structure of soft-bottom sediments (Ciutat et al. 2006), the species significantly affects the direction and intensity of substance exchange in the sediment/water interface (Rîşnoveanu et al. 2004), which determines, among other things, the productivity of lakes. It is obvious that the role of P. hammoniensis in the environment largely depends on its abundance, which is strongly associated with the reproductive success. It seems, therefore, that the research aimed at identifying the factors that affect the reproductive activity of this important element of the biocoenosis of aquatic ecosystems is fully justified.

The results of previous studies indicate that the reproduction period of Potamothrix hammoniensis is definitely dependent on the temperature (Jónasson, Thorhauge 1972) and the oxygenation of the near-bottom water (Thorhauge 1975). According to Jónasson (1972) and Arkhipova (1980), the species breeds at low temperatures. On the other hand, the oxygen deficit, often occurring in early summer, ends the reproduction period irrespective of the thermal conditions (Thorhauge 1975). It can therefore be assumed that the reproductive activity of P. hammoniensis in deep lakes is more dependent on the oxygenation of the water above the bottom, because the water temperature in the deeper profundal of stratified lakes is usually within the limits of reproduction throughout the year.

Most studies on reproductive activity of Potamothrix hammoniensis were conducted in deep stratified lakes, where the dynamics of thermal and aerobic conditions during the year is completely different compared to shallow water bodies. According to Żbikowski (2011), the oxygenation of the near-bottom water in shallow lakes is generally good, except for the ice cover period, while in the growing season the water temperature often exceeds 20°C.

Considering the above information, the aim of this study was to indicate the abiotic parameters of water and bottom sediments, which significantly affect the reproduction of Potamothrix hammoniensis.

It was hypothesized that, unlike in deep lakes, the reproduction period of this species is more dependent on the temperature of water above the bottom than the water oxygenation.

Small oligochaetes classified into class II, III and IV were not considered in this paper, as no individuals with a developed reproductive system were found among them. Over 2700 individuals of Potamothrix hammoniensis were examined (Table 2). Most of the studied specimens were medium-sized individuals, included in classes from V to VII.

Table 2

Number of examined individuals of Potamothrix hammoniensis – the sum of all sampling sites and dates

The percentage of individuals with a developed reproductive system among the individuals capable of reproduction (starting from class V) varied in particular lakes and ranged from 14 to 72% (Fig. 2). It should be noted that the highest value was found in Lake Głuchowskie, where the number of examined individuals was the smallest one – only 43. On the other hand, in lakes with the highest number of studied individuals (Lake Stęgwica – 973 and Lake Zielone – 678), the proportion of sexually mature individuals was relatively small, 15 and 17%, respectively. There was no correlation between the lake type and the proportion of individuals with a developed reproductive system.

Figure 2

Single individuals with a developed reproductive system were observed already in class V (Table 3). Lake Jeziorak is distinguished by the fact that the reproductive organs were found in as many as 12% of individuals included in this class. Even though a higher value (20%) was determined in Lake Głuchowskie, only 5 individuals were in this class, thus only 1 specimen was capable of reproduction. It should be noted, however, that the highest percentage of sexually mature individuals in the distinguished classes was determined in the latter lake.

Table 3

Percentage of sexually mature individuals of Potamothrix hammoniensis in the distinguished size classes

Generally, the percentage of reproducing Potamothrix hammoniensis individuals increased with their size (Table 3). This pattern was very clear in the macrophyte-dominated lakes, while small exceptions to this rule were recorded in the phytoplankton-dominated lakes. Most individuals in the largest-size classes have a developed reproductive system.

The percentage of individuals with a developed reproductive system varied in particular months (Fig. 3). The results do not allow to indicate a period in which the percentage of sexually mature individuals would be only relatively high. There were also no regularities related to the distinguished types of lakes. Noteworthy is the lack of individuals reproducing in the summer months. On the other hand, only individuals with a developed reproductive system were recorded in the period from March to May and in November and December.

Figure 3

Physical and chemical parameters of water and bottom sediments (annual average values) of the studied lakes are presented in Table 4. Water transparency was higher in the macrophyte-dominated lakes (1.7–2.1 m) than in the phytoplankton-dominated ones (0.7–1.4 m). Water temperature ranged from 11.2 to 14.0°C, oxygen concentration was relatively good in all lakes (6.4–10.8 mg O₂ dm^-3), pH values ranged from 7.2 to 8.7 and conductivity from 199 to 577 μS cm^-1, except Lake Zielone, where it was clearly lower (100 μS cm^-1).

Table 4

Mean values of abiotic parameters of water and bottom sediments of the studied lakes

E × D values were higher in the deeper phytoplankton-dominated lakes (7.6 and 8.3) compared to the other lakes (2.2–5.5). Water content in the bottom sediments was relatively high, ranging from 93.3 to 97.4%. The percentage of organic matter content per unit of dry mass of the bottom sediments (OC-%) varied considerably among the studied lakes, ranging from 32.6 to 78.4%. Organic matter content (in mg) per 10 cm³ of the fresh bottom sediments ranged from 136 to 252 mg. SOD values varied considerably from 2.6 to 8.2 mg O₂ per 20 cm³ of fresh sediments per 1 h.

The highest values of the Pearson correlation coefficient between the percentage of individuals with a developed reproductive system and the measured parameters were found in the case of conductivity (r = 0.69; p < 0.001), pH (r = 0.51; p = 0.002) and OC-% (r = −0.42; p = 0.012) (Table 5). It is worth noting that there was no correlation between the proportion of sexually mature specimens and the water temperature (r = −0.22, p = 0.204). It was observed, however, that the individuals with the developed reproductive system were recorded at temperatures below 2°C, while the proportion of reproducing individuals was very low when the water temperature was higher than 23°C (Fig. 4). Also no correlation between the water oxygen concentration and the proportion of sexually mature individuals was found (r = −0.08; p = 0.648). Even when the oxygen concentration was very low (< 1 mg dm^-3), specimens with the developed reproductive system were found (Fig. 5). The total lack of reproductive activity was recorded mainly in summer and early autumn, when the oxygen concentration was high (from 6 to 13 mg dm^-3). On the other hand, in the same aerobic conditions, at other times of the year, the percentage of sexually mature individuals was high.

Table 5

Values of Pearson’s linear correlation coefficient (r) and the significance level (p) between the percentage of sexually mature individuals of Potamothrix hammoniensis and the environmental variables under study. Statistically significant values are boldfaced

Figure 4

Figure 5

Research on abiotic parameters that significantly affect the reproduction of Potamothrix hammoniensis was carried out mainly in the 20^th century. Discontinuation of such studies would suggest that the problem has already been solved. However, the results of this study do not fully confirm the previously observed (mainly in deep stratified lakes) regularities, which justifies the need to continue such studies also in shallow eutrophic lakes.

The percentage of sexually mature individuals of Potamothrix hammoniensis varied in particular lakes and ranged from 14 to 72%. Due to different methodology (described in the Materials and methods section) used in this study, our results are in line with the expectations usually higher compared to the results of other authors (Wiśniewski 1979; Arkhipova 1980; Rîşnoveanu & Vadineanu 2002), defining the percentage of sexually mature individuals in the entire population, and not only in the group of specimens with the size indicating the capability to reproduce. It may be surprising that there was no correlation between the type of lake and the percentage of individuals with a developed reproductive system, because Żbikowski (2011) proved that the abiotic environment of the three types of shallow lakes distinguished in this paper varies greatly. Perhaps the reproduction of P. hammoniensis is significantly influenced by factors not included in the above-mentioned paper.

The percentage of sexually mature individuals of Potamothrix hammoniensis varied in particular months. It is worth noting that these specimens are almost absent only in summer (July to September). This may be surprising because in a shallow eutrophic lake in the Danube Delta, Rîşnoveanu & Vadineanu (2002) have identified the constant presence of reproductive specimens of this species from May to September. Furthermore, Arkhipova (1980) found even a slight increase in the percentage of breeding individuals in the Rybinsk Reservoir in August. The lack of breeding individuals in summer is characteristic of the deep profundal zone of stratified lakes, where the oxygen deficit in early summer ends the breeding season (Thorhauge 1975). In the lakes under study, only specimens with the developed reproductive system were identified in the period from March to May and in November and December, suggesting the occurrence of conditions favorable for reproduction. On the other hand, Moroz (1976) (in the temperate zone) and Matčinskaja & Pligin (1988) (in an Ukrainian reservoir) report that Potamothrix hammoniensis breeds only once a year, from May to July. The above differences in the periods of reproductive activity of this species found between the studied lakes and literature data confirm the results of Thorhauge (1975) and Kravčenko & Šahmatova (1988), which show that P. hammoniensis can breed at different times of the year, depending on external conditions.

A very important aspect of this study was to identify the abiotic parameters of water and bottom sediments having an important impact on the sexual maturity of Potamothrix hammoniensis. The research has shown a significant correlation between the percentage of reproductive individuals and the conductivity, pH (positive correlations) and OC-% (negative correlation). Seasonal changes in the conductivity, pH and OC-% in the same lake were small, while these parameters varied in individual lakes. Data analysis shows that in some lakes, the worms generally reproduce more actively. Based on the research, it is difficult to explain the first two correlations. Whereas this study has confirmed the previous observations (Poddubnaja 1959; Arkhipova 1980; Reynoldson 1990) that the organic matter content in the sediments is one of the most important environmental factors affecting the life cycle of common Tubificidae.

In this study, no correlation between the water temperature and the percentage of individuals with a developed reproductive system was found. These results may be somewhat surprising, since the thermal conditions are considered as one of the most important environmental factors affecting the reproductive activity of aquatic worms. The researchers generally agree that the reproduction of Potamothrix hammoniensis begins when the water temperature reaches 5–7°C (Jónasson 1972; Arkhipova 1980). However, it is not easy to indicate the maximum temperature that limits the reproduction. Jónasson (1972) states that the species does not reproduce at a temperature above 13°C, while according to Rîşnoveanu & Vadineanu (2002) – above 20°C. The results obtained in this study may suggest that in shallow eutrophic lakes, P. hammoniensis could potentially breed already at temperatures of approx. 2–3°C, which is slightly lower than commonly believed. However, this hypothesis requires confirmation. The maximum temperature could be as high as 22–23°C, which is consistent with the results of Rîşnoveanu & Vadineanu (2002). It should be noted, however, that such a high temperature was recorded only in summer, when the reproductive activity was generally inhibited also at lower temperatures (17–20°C). On the other hand, the relative abundance of sexually mature individuals at the same temperature range in spring (17–20°C) was quite high, similar to that at lower temperatures. Thus, there is no clear evidence that a temperature slightly above 20°C is a key factor inhibiting the species reproduction.

Low oxygen concentration is another important environmental factor affecting the reproductive activity of Potamothrix hammoniensis (Poddubnaja 1959; Thorhauge 1975; 1976). The results obtained in our study do not support this theory. The individuals with the developed reproductive system were found even when the water oxygen concentration was as low as < 1 mg dm^-3. On the other hand, the lack of breeding individuals in summer and early autumn was unlikely due to the oxygen deficiency, because the oxygen concentration at that time was high enough and did not limit the reproduction in other seasons of the year. The results show that in shallow lakes, as opposed to deep lakes, oxygen conditions do not significantly affect the reproductive activity of P. hammoniensis.

Both in the shallow and deep lakes under study, we found no individuals of Potamothrix hammoniensis with a developed reproductive system in the second half of the summer. However, unlike the latter, the oxygen deficits were not a limiting factor for breeding in the shallow lakes. Furthermore, it cannot be concluded with certainty that the inhibition of species reproduction was mainly caused by too high water temperature near the bottom, because P. hammoniensis reproductive activity was high in spring when the temperature conditions were similar to those in summer. Perhaps the decisive factor is not only the absolute value, but also the time of exposure to the temperature considered to be close to the limit of reproduction. The spring temperature of approx. 20°C does not inhibit the reproductive activity of this species, but its maintenance in summer begins to limit the reproductive processes of P. hammoniensis. However, this hypothesis should be confirmed, which requires the continuation of this research.