Research Article |
Corresponding author: YuV Bespalaya ( jbespalaja@yandex.ru ) Academic editor: Aleksandr P. Novoselov
© 2019 YuV Bespalaya, OV Aksenova, AS Aksenov, SE Sokolova, AR Shevchenko, OV Travina, AV Kropotin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Bespalaya Y, Aksenova O, Aksenov A, Sokolova S, Shevchenko A, Travina O, Kropotin A (2019) Reproductive features of Pisidium casertanum (Poli, 1791) (Bivalvia: Sphaeriidae) in relict lakes of Bolshezemelskaya Tundra. Arctic Environmental Research 19(3): 113-122. https://doi.org/10.3897/issn2541-8416.2019.19.3.113
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The reproductive features of the pea clam Pisidium casertanum in relict lakes of Bolshezemelskaya Tundra were studied. The P. casertanum population in the Vashutkiny Lakes of Bolshezemelskaya Tundra has a single period of summer reproduction. We suppose that the release of embryos mainly occurs between July and August and the breeding season could probably begin in May-June. The positive relationship between brood size and parent shell length was detected. We did not find a specific brooding mechanism, accompanied by asynchronous development and release of embryos by the parent in the population of P. casertanum in the Vashutkiny Lakes. The reason for this is probably related with the environmentally more stable freshwater habitats of the relict Vashutkiny Lakes in comparison with the lakes of the High Arctic.
brooding, Bolshezemelskaya Tundra, embryonic growth, Pisidium species, reproduction, relict lakes
The Vashutkiny Lakes represent the largest water system in the East of the Bolshezemelskaya Tundra and they have attracted the attention of hydrobiologists for many years (
According to previous data, 24 species of mollusks have been identified and the Pisidium casertanum (Poli, 1791) was considered dominant in the lakes (
The aim of our study is to describe the reproduction of P. casertanum in the relict Vashutkiny Lakes System.
This study was conducted in the Bolshezemelskaya Tundra. This territory is bounded by the Pechora River from the West and the Usa River from the South, as well as the Polar Urals and Pai-Khoy Mounain from the East (
Map of the study area. A – general view of the map revealing the geographic position of the Vashutkiny Lakes, (red point); B – general view of the Vashutkiny Lakes System. Sampling locations marked in orange circles; C – view on the Seito Lake from a helicopter; D – field works on the Seito Lake
To characterize the sizes and reproductive features of P. casertanum, 197 benthic samples were collected at 47 stations in the 9 lakes of the system. For each station, 2–7 replicates were gathered with a rectangular hand net (dimensions 0.28 m × 0.5 m, mesh size 200 μm), covering a total sampling area of 0.14 m2, or with a Peterson dredge (0.024 m2) in deeper waters. Samples were washed using a hydrobiological sieve (mesh size 0.56 mm) and fixed in 96% ethanol. A total of 412 P. casertanum specimens of all size classes were collected, measured and dissected. The specimens of P. casertanum were examined in the laboratory using a Leica M165C stereomicroscope (Fig.
The external morphology of the shell, anatomy and hinge of the right and left valves of P. casertanum from the Vashutkiny Lakes. A – external morphology of the right valve; B – internal anatomy of the dissected P. casertanum, C – teeth of the right valve; D – teeth of the left valve; E – general view of the male and female gonad of P. casertanum: o – oocyte, n – nucleus, sp – spermatocytes and spermatids aggregations
The differences in the shell length, number and length of embryos of P. casertanum between lakes were estimated using Kruskal-Wallis (multiple comparisons) tests in the program package PAST (
Hydrochemical characteristics of water from lake’s surface (pH, conductivity, dissolved O2, Na+, K+, Ca2+, Mg2+, HCO3-, SO42-, Cl- concentrations) were taken according to the methodology (
For histological examination were taken 5 randomly selected specimens of P. casertanum. Tissues were dehydrated through a graded alcohol series and embedded in paraffin. Histological sections with a thickness of 6 μm were made using a rotary microtome (HM 325, Thermo Scientific). The sections were stained with Mayer’s hematoxylin-eosin double stain for examination under a light microscope (Axio Lab.A1, Carl Zeiss, Germany).
The materials are stored in the collection of the Russian Museum of the Biodiversity Hotspots of the N. Laverov Federal Center for Integrated Arctic Research of Russian Academy of Sciences, Arkhangelsk, Russia.
The hydrochemical characteristics of the Vashutkiny Lakes are presented in Table
Limnological features of the Vashutkiny Lake. Data are presented as means and standard deviations (in parentheses) and ranges (in figure parentheses)
Lake | Depth | pH | Cond | HCO3- | O2, | SO42- | Cl- | Na+ | Mg2+ | K+ | Ca2+ |
---|---|---|---|---|---|---|---|---|---|---|---|
(m)* | (μS/cm) | (mg/l) | % | (mg/l) | (mg/l) | (mg/l) | (mg/l) | (mg/l) | (mg/l) | ||
Yurto | 2.9 (2.6) {0.2–8.0} | 7.7 (0.93) {7.1–8.9} | 47.6 (1.5) {45.9–49.3} | 29.4(6.4) {28.1–32.3} | 98.7 (1.9) {90.4–105} | 1.8 (0.07) {1.8–1.9} | 2.2 (0.14) {2.1–2.3} | 1.9 (0.14) {1.8–2.0} | 1.55 (0.21) {1.4–1.7} | 0.5 (0.07) {0.4–0.5} | 4.9 (0.35) {4.6–5.1} |
Bolbanty | 1.67 (2.1) {0.5–14} | 7.5 (0.65) {7.6–8.4} | 55.7 (3.6) {50.3–59.0} | 30.9(7.8) {28.7–32.9} | 92.5 (1.6) {86.8–106} | 2.3 (0.15) {2.2–2.5} | 2.3 (0.17) {2.2–2.5} | 2.6 (1.03) {1.7–3.7} | 1.7 (0.1) {1.6–1.8} | 0.5 (0.06) {0.4–0.5} | 6.2 (0.66) {5.5–6.8} |
Seito | 2.4 (2.5) {0.3–7.0} | 7.0 (0.05) {7.0–7.1} | 65.0 (13.0) {57.9–84.6} | 33.9(2.7) {30.5–42.7} | 93.9 (5.9) {92–98} | 4.3 (2.90) {2.3–6.4} | 2.3 (0.28) {2.1–2.5} | 2.0 (0.28) {1.8–2.2} | 2.2 (0.7) {1.7–2.7} | 0.4 (0.14) {0.3–0.5} | 8.7 (2.76) {6.8–10.7} |
Pernaty | 3.2 (4.3) {0.4–10} | 8.9 (0.94) {7.0–9.5} | 57.6 (0.6) 57.0–58.3} | ND | ND | 2.5 (0) | 2.2 (0) | 1.7 (0) | 1.8 (0) | 0.4 (0) | 7.1 (0) |
B. Starik | 1.4 (1.3) {0.5–4} | 8.0 (0.63) {6.8–9.0} | 63.2 (8.3) {57.4–84.8} | ND | ND | 3.6 (0) | 2.7 (0) | 7.3 (0) | 1.6 (0) | 1.7 (0) | 5.6 (0) |
M. Starik | 2.35 (5.0) {0.1–30} | 7.4 (0.39) {6.8–8.1} | 65.4 (15.9) {58.3–121.6} | 34.4 (17) {32.9–35.4} | 91.6 (1.3) {90.2–93.6} | 2.6 (0) | 2.4 (0.28) {2.2–2.6} | 2.1 (0.49) {1.8–2.5} | 1.8 (0.42) {1.5–2.1} | 0.5 (0) | 6.9 (0.7) {6.4–7.4} |
Diyaty | 2.7 (4.5) {0.7–21} | 7.6 (0.68) {6.7–8.8} | 71.4 (17.2) {61.3–116.7} | 50.3 (0) | 95.6 (0.2) {9.4–95.7} | 5.4 (0) | 1.9 (0) | 1.9 (0) | 3.1 (0) | 0.2 (0) | 12.5 (0) |
Vanukty | 2.8 (6.2) {0.2–34} | 8.0(0.71) {6.8–9.3} | 68.6 (15.7) {60.0–120.9} | 34.9 (3.9) {33.6–37.8} | 98.4 (1.8) {94.3–102.6} | 2.5 (0.49) {1.9–2.8} | 2.5 (0.42) {2.0–2.8} | 2.1 (0.23) {1.8–2.2} | 1.9 (0.21) {1.7–2.1} | 0.5 (0.06) {0.4–0.5} | 7.0 (1.62) 5.1–8.0} |
Makty | 2.2 (2.1) {0.5–6.0} | 8.7(0.54) {8.1–9.1} | 57.4 (0.55) {56.8–57.8} | ND | ND | 1.77 (0) | 0.99 (0) | 1.64 (0) | 1.85 (0) | 1.21 (0) | 9.04 (0) |
The size frequency structure of the P. casertanum population is presented in Fig.
Frequency histogram showing the variation in the length distribution of shells in gravid and nongravid individuals of Pisidium casertanum in Vashutkiny Lakes
Abundance, size, and reproductive features of Pisidium casertanum from the Vashutkiny Lakes. Data are presented as means and standard deviations (in parentheses) and ranges (in figure parentheses)
Lake | Abundance (ind./m2) | N* | SL * (mm) {range} | N* embryo {range} | Embryo L* (mm) | Class 1 | Class 2 | Class 3 | Class 4 | ||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
N | L | N | L | N | L | N | L | ||||||
Bolbanty | 106.8(146.6) {7.1–458.3} | 24 | 2.50 (0.48) {1.65–3.55} | 2.0 (1.73){1–4} | 0.88 (0.29) {0.55–1.15} | 0 | – | 0 | – | 0 | – | 2.0 (1.73) | 0.88 (0.29) |
Seito | 120. 4 (91.2) {7.1–250.0} | 78 | 2.48 (0.55) {1.6–3.5} | 4.69 (2.01){1–8} | 0.64 (0.26) {0.2–1.2} | 5.0 (0) | 2.24 (0.02) | 4.2 (2.17) | 0.4 (0.07) | 3.0 (2.71) | 0.59 (0.07) | 3.83 (1.83) | 0.90 (0.14) |
Pernaty | 97.6 (135.2) {7.1–333.3) | 8 | 2.28 (0.42) {1.6–2.9} | 4.75 (2.22){1–7} | 0.51 (0.22) {0.22–0.75} | 0 | – | 5.3 (2.08) | 0.32 (0.06) | 1.5 (0.71) | 0.59 (0.08) | 0 | – |
B. Starik | 85.1 (98.2){7.1–307.1} | 32 | 2.71 (0.44) {1.93–3.05} | 2.4 (0.55) {2–3} | 0.62 (0.42) {0.22–1.2} | 2.0 (0) | 0.2 (0) | 2.00 (0) | 0.25 (0) | 1 (0) | 0.5 (0) | 2.5 (0.7) | 1.13 (0.06) |
M. Starik | 140.3 (220.6) {7.1–750.0} | 14 | 2.45 (0.57) {1.75–3.8} | 3.0 (2.83) {1–5} | 0.73 (0.14) {0.65–1.2} | 0 | – | 0 | – | 0 | – | 3.0 (2.83) | 0.73 (0.14) |
Diyaty | 81.4 (50.1) {21.0–135.7} | 108 | 2.37 (0.45) {1.6–3.7} | 4.33 (4.04) {2–9} | 0.76 (0.42) {0.09–1.13} | 8.0 (0) | 0.15 (0.03) | 0 | - | 1.5 (0.71) | 0.84 (0.16) | 2.0 (0) | 1.13 (0.22) |
Vanukty | 63.7.0 (55.3) {7.1–167.7} | 67 | 2.63 (0.31) {1.8–3.25} | 5.5 (3.02) {2–11} | 0.65 (0.34) {0.15–1.0} | 3.0 (0) | 0.15 (0.01) | 6.5 (2.12) | 0.32 (0.09) | 5.0 (0) | 0.67 (0.1) | 3.0 (1.83) | 0.91 (0.07) |
Makty | 61.1 (34.40 {21.4–83.3}) | 66 | 2.51 (0.45) {1.5–3.75} | 4.5 (2.26) {2–8} | 0.93 (0.42) {0.16–1.33} | 5 (0) | 0.17 (0.01) | 3.0 (0) | 0.27 (0.02) | 3.0 (0) | 0.65 (0.05) | 4.0 1.83) | 1.16 (0.10) |
Yurto | 123.5(106.9) {14.3–307.1} | 32 | 2.73 (0.25) {2.55–2.9} | 4 (1.41) {3–5} | 0.64(0.26) {0.2–1.2} | 0 | – | 0 | - | 5.0 (0) | 0.61 (0.07) | 3.0 (0) | 0.85 (0.05) |
The average shell length of juveniles at birth was 0.96 mm ± 0.2 (0.5–1.3 mm) (N = 73). The bivalve populations in all nine lakes were characterized by having a higher number of nongravid than gravid individuals. The percentage of gravid mollusks varied from 3 to 15%. According to our data, the brood sacs with embryos in the examined population are formed when the shell length of mollusks is at least 2.2 mm. The proportion of juvenile (pre-reproductive) to mature bivalves was from 31.6 to 68.4%, respectively, in our total sample.
The mean number and length of embryos by class are shown in Table
Proportion of embryos in each class in P. casertanum collected from the nine Vashutkiny Lakes. Embryos in classes 1–3 are present in brood pouches; those in class 4 are extramarsupial
The presence of mature eggs and sperm in the gonads, as well as developed oogenic and spermatogenic areas, may indicate that the mollusks are at the stage of active reproduction (Fig.
According to our results, the number of embryos is correlated with the parent shell length, i.e. the greater shell length of the parent individuals, the higher the number of embryos (Fig.
We studied the size distribution and some reproductive features of P. casertanum from the Vashutkiny Lakes. The gonads conditions indicate that the mollusks are at the stage of active reproduction (Fig.
The shell length of adult individuals, the size of juveniles at birth, the length of embryos and their general number, correspond to the size parameters of P. casertanum in other parts of its distribution range (
According to a number of studies the shell length of a Pisidium species being positively correlated to high calcium, сonductivity, pH, alkalinity values and adult shell length (Hornbach and Cox 1987; Kilgour and Mackie 1991). Despite the generally low mineralization of the Vashutkiny Lakes, some of their areas have increased levels of dissolved salts as a result of local influences of mineralized subterranean waters (
Our previous research shows that the freshwater mollusk P. casertanum in the Arctic lakes of Vaigach Island and Yamal Peninsula has a specific process of breeding, accompanied by asynchronous development and spawning of embryos (
The positive relationship between brood size and parent shell length was detected. This agrees with previous observations (
The P. casertanum population in the Vashutkiny Lakes probably has a single period of summer reproduction. We suggest that birth mainly occurs between July and August and the breeding season can probably begin in May – June. The positive relationship between brood size and parent shell length was detected. Hence, with respect to the freshwater mollusk P. casertanum in the Vashutkiny Lakes, there is no specific process of breeding, accompanied by asynchronous development and spawning of embryos.
The authors express their gratitude to O.N. Bespaliy for his valuable assistance with the collecting of material. The Ministry of Science and Higher Education of the Russian Federation supported the expeditionary research (project no. АААА-А17-117033010132-2), the study of reproductions of mollusks was supported by the grant from the program of Presidium Ural Branch of RAS (no. АААА-А17-117122890059-1), the study of histological research, and hydrochemical characteristic of lakes supported by the Russian Foundation for Basic Research (no. 17-44-290016).