Folia Zool. – 56(1): 90–96 (2007)

Development structure of ovaries in female white bream, Abramis bjoerkna from Lake Kortowskie in North-Eastern Poland

Wiesława KOPIEJEWSKA1 and Jacek KOZŁOWSKI2

1 Department of Zoology, Faculty of Biology, University of Warmia and Mazury in Olsztyn, M. Oczapowski St. 5, 10-967 Olsztyn, Poland; e-mail: [email protected] 2 Department of Fish Biology and Culture, Faculty of Environmental Sciences and Fisheries , University of Warmia and Mazury in Olsztyn, M. Oczapowski St. 5, 10-967 Olsztyn, Poland; e-mail: [email protected]

Received 1 August 2005; Accepted 19 March 2007

A b s t r a c t . Among white bream, Abramis bjoerkna from Lake Kortowskie in North-Eastern Poland, some females showed characteristics of defined fertility while some females in the period of vitellogenesis of the first and second batch of oocytes showed characteristics of undefined fertility. Some females representing defined fertility showed characteristics of single spawning during the reproduction season. The other females with both defined and undefined fertility showed characteristics of batch spawning reproduction type. The results showed that female white bream were characterized by diversified vitellogenetic activity. They showed linkages to both the reproduction type with single spawning during the reproductive season and the type of reproduction with batch spawning related to undefined fertility.

Key words: cyprinid, Abramis bjoerkna, development structure of ovaries, spawning pattern

Introduction

White bream, Abramis bjoerkna (L.) syn. Blicca bjoerkna (L.) belongs to the : (N e l s o n 1994). It is widely spread in almost all bream type waters (Szczerbowski 1981) and phylogenetically is most closely related to bream, Abramis brama (L.) (B r i o l a y et al. 1998, H ä n f l i n g & B r a n d l 2000). H ä n f l i n g & B r a n d l (2000) think that the generally used genus Blicca with Blicca bjoerkna – white bream – the newer Abramis should be included in the genus Abramis. They state that white bream, Abramis bjoerkna (L.) and bream, Abramis brama (L.) are sister species, which is defined as similar in morphology but isolated concerning reproduction (J u r a & K r z a n o w s k a 1992: Biological Lexicon), or as a pair of species developed as a result of the split between the parental species (http://pl.wikipedia.org/wiki/), or as a result of one speciation (Multimedia general encyclopedia 2007). Generally, fish species are characterized by a specific type of ovary organization, fertility and spawning (M u r u a & Saborido-Rey 2003). White bream and bream are defined as species with a group-synchronous development of oocytes and batch and single spawning during the reproductive season respectively (M a r z a 1938, P a p a d o p o l & I a n c u 1970, S t a t o v a 1970, B r y l i ń s k a & D ł u g o s z 1970, W a l l a c e & S e l m a n 1981, A n d r e e v a 1983, S p i v a k 1987, R i n c h a r d & K e s t e m o n t 1996, B r y l i ń s k a & T a d a j e w s k a 2000). However, females with single spawning during the reproductive season have been recorded in populations of white bream (Tryapitsyna 1975, Kopiejewska 1996, 1997), while R i n c h a r d & K e s t e m o n t (1996) suggested that white bream could be linked to the spawning model with single spawning. Additionally, it was established that white bream forms hybrids with

90 species such as roach Rutilus rutilus, bleak Alburnus alburnus, bream Abramis brama, rudd Scardinius erythrophthalmus, blue bream Abramis ballerus (B r y l i ń s k a et al. 2006), and among those hybrids the hybrids of white bream and bleak, as well as those of white bream and bream, reach sexual maturity and are fertile (K u d e r s k i j 1956, N i k o l y u k i n 1972, K u t u z o v 1983). This study aimed to obtain knowledge on the development structure of ovaries in the white bream population in view of the abovementioned data.

Materials and Methods

The females of white bream for these studies were caught in Lake Kortowskie situated in a region of the East Baltic – Belarus Lowland (K o n d r a c k i 2002). During the years 2003–2004 a total of 126 white bream ovaries were examined. Middle segments of the right and left parts of female fish gonads were fixed in buffer formalin, dehydrated through a series of increasing concentrations of ethanol, defatted in chloroform and embedded in paraffin. Sections 7 μm in thickness were stained with Delafield’s hematoxylin and eosin (Zawistowski 1986). The developmental stages of germinal cells and gonads were identified according to S a k u n & B u t s k a y a (1968), W a l l a c e & S e l m a n (1981), T y l e r & S u m p t e r (1996), M u r u a & Saborido-Rey (2003). The percentages of oocytes at the cortical alveoli and vitellogenesis stage were determined using Abercrombie’s formula (M a r r a b l e 1962): N = n T / (T + D) where N – number of oocytes, T – section thickness, D – arithmetic mean of the diameters of 20 oocytes at a given maturity stage, n – number of cross-sections of oocytes at a given maturity stage in three serial sections of the right and left parts of gonads. Abercrombie’s formula can be successfully applied in this kind of research, as proved by Kopiejewska (2003). Photographs of the cross-sections of gonads were taken with an Olympus digital camera. The diameters of oocytes were measured under a MMI–2 microscope, with an accuracy of 0.005 mm.

Results

Vitellogenesis in the studied white bream population started during the spring period. During the period preceding the reproductive season two groups of oocytes emerged: those in the stage of final vitellogenesis or mature stage and those in the cortical alveoli (vacuolization) stage (Fig. 1A-D, Table 1). The oocytes in the cortical alveoli stage were diversified in their stages of development. In some females they were only in the final stage of development, in some females in the final and early stages and in a few in the early stage of development only. During the period when, in the oocytes of the oldest generation, vitellogenesis started and progressed, the oocytes in the stage of cortical alveoli in some females were at the final, medium and initial stage of development. The share of oocytes in the stage of cortical alveoli in the pool of trophoplasmatic growth oocytes in females was diversified. In one female the oocytes in the stage of cortical alveoli represented a minor percentage – 4.2, which corresponded to single cross sections of such oocytes among vitellogenetic oocytes in cross- sections of ovaries. In some females their maximum share was slightly over 50%. In two

91 ica

fca

v v ica

v ica fca 1A 1B 1C

pg

no ms

pof fca

v pof 1D 1E ica 1F

pg

a 1G Fig. 1. Cross-sections of ovaries of white bream females in the pre-spawning and post-spawning season of 2003 and 2004 in Lake Kortowskie; A – oocytes at the final (fca) and initial (ica) stage of cortical alveoli in the ovaries of a female collected on 20.05.2003, B – oocytes at the initial and middle stage of vitellogenesis (v) and oocytes at the initial stage of cortical alveoli (ica) in the ovaries of a female collected on 20.05.2003, C – oocytes at the final stage of vitellogenesis (v) and oocytes at the initial (ica) and final (fca) stage of cortical alveoli in the ovaries of a female collected on 20.05.2003, D – oocytes at the mature stage (ms) and oocytes at the final stage of cortical alveoli (fca) in the ovaries of a female collected on 25.06.2004, E – post-ovulatory follicles (pof) in the first spawning, oocytes at the stage of vitellogenesis (v) – second portion of spawn, and oocytes at the cortical alveoli (ca) in the ovaries a female collected on 09.06.2003, F – post-ovulatory follicles (pof) in the first spawning, non-ovulated oocytes (no) and oocytes at the stage of primary growth (pg); absence of oocytes in cortical alveoli stage in the ovaries of a female collected on 09.06.2003, G – Atrophy of non-ovulated oocytes (a) and oocytes at the stage of primary growth (pg) in the ovaries of a female collected on 14.07.2004. Scale = 200 µm.

92 % 5.2–12.1 1.0–10.9 10.1–21.1 16.2 53.9 µ Initial 320–375 + + – 225–385 – 250–395 250–305 245–435 Ø middle – + – – – – – – – % 87.9–94.8 11.6–56.1 17.1–53.9 4.2–26.3 8.5 µ Ø Cortical alveoli stage of oocytes Final 420–685 + + 285–740 320–690 440–670 – 390–570 Initial vitellogenesis 445–590 2.1

% 43.9–88.4 40.9–80.5 73.7–95.8 78.9–89.9 75.3 44.0

µ Stage of the oocytes of the oldest generation Cortical alveoli Initial and middle stage of vitellogenesis Initial and middle stage of vitellogenesis Final stage vitellogenesis 565–1285 Final stage vitellogenesis 620–1140 Final stage vitellogenesis, mature stage 800–1165 Final stage vitellogenesis, mature stage 750–995 Final stage vitellogenesis, mature stage 715–810 Final stage vitellogenesis, mature stage 745–955 Ø n 4 7 2 2 2 1 1 27 15 17.5–22.0 8.1–33.0 9.3–146.1 24.7 Body weight g 13.7–21.5 13.4–26.8 19.5–36.5 20.2 28.4 Development stages of white bream oocytes in the pre-spawning season in Lake Kortowskie. Body length cm SL 8.8–10.0 8.6–10.8 9.6–10.0 7.3–11.6 7.7–18.0 10.0–11.7 10.3–10.5 9.7 11.2 + presence of a given development stage of oocytes, – absence of a given development stage of oocytes Table 1. Table

93 females in which the oocytes in the stage of cortical alveoli in the initial stage occurred they only represented 10.1 and 21.1% of the total pool of trophoplasmatic growth oocytes. After spawning, vitellogenesis started in the oocytes of the final stage of cortical alveoli. In some females no oocytes in the stage of cortical alveoli were present and the oldest generation the oocytes were in the stage of primary growth with sporadically present oocytes in the initial stage of cortical alveoli (Fig. 1E-G, Table 2). During vitellogenesis of the second batch of oocytes, in some females oocytes in the final and early stage of vacuolization were present, in some the oocytes were in the early stage or in the middle stage of vacuolization only, while in some females continuous vacuolization took place. During the autumn, winter and spring, vacuolization occurred in the oldest oocytes. In November and December, the oocytes most advanced in their development had 75% vacuolized cytoplasm while in April vacuolization reached 75–100% of cytoplasm.

Table 2. Development stages of white bream oocytes in the post-spawning season in Lake Kortowskie.

Body length Body Stage of the oocytes Cortical alveoli stage of oocytes n SL cm weight g of the oldest generation final middle initial 9.6-10.5 17.1-22.9 9 Cortical alveoli + - - 9.3-12.1 17.2-32.2 4 Cortical alveoli + - + 9.5-21.5 18.3-236.5 6 Cortical alveoli - + + 10.3-12.9 20.4-47.5 5 Vitellogenesis + - + 10.5-11.1 23.4-28.6 2 Vitellogenesis - - + 9.4-9.8 16.5-18.3 2 Vitellogenesis - + - 8.3-11.0 12.3-26.3 9 Vitellogenesis + + + Final stage of vitellogenesis, 10.9-12.3 27.4-39.9 2 + + + mature stage Previtellogenesis, sporadically 9.4-15.0 18.7-77.5 7 - - + initial stage of vacuolization Previtellogenesis/atrophy of 9.4-10.6 15.4-26.2 3 - - - non-ovulated oocytes

+ presence of a given development stage of oocytes, - absence of given development stage of oocytes

Discussion

The studies showed that in the population of white bream in Lake Kortowskie, similar to the population of white bream in the Włocławek in Poland (Kopiejewska 1996), in Kuchurganskij Liman in (S t a t o v a 1970), in the delta of the river (Tryapitsyna 1975) and in the some of the females in the Meuse river in Belgium (R i n c h a r d & K e s t e m o n t 1996) vitellogenesis occurred during the spring. However, in a few female white bream from the Meuse river (R i n c h a r d & K e s t e m o n t 1996) and in the Kurshyu – Mares bay (K u b l i t s k a s 1968 in Tryapitsyna 1975) presence of vitellogenic oocytes was found during the period of autumn and winter. The presence of oocytes in that stage during the autumn and winter season can indicate a high adaptive flexibility of white bream to the environmental conditions as well as the similarity of those females to the bream in the case of the first accumulations of yolk in oocytes which occur during autumn (B r y l i ń s k a & D ł u g o s z 1970, A n d r e e v a 1983). R i n c h a r d & K e s t e m o n t (1996) did not find new trophoplasmatic growth oocytes in white bream from the Meuse river during the period preceding the reproductive

94 season. In their study, during the period preceding the reproductive season new trophoplasmatic growth oocytes were absent from the some of the females but were present in others. The presence of females possessing no new trophoplasmatic growth oocytes and females possessing new trophoplasmatic growth oocytes before the reproductive season suggests that some females could have defined, and some undefined, fertility (H u n t e r & G o l d b e r g 1980, H u n t e r et al. 1992). During vitellogenesis of the first and second batch of oocytes, in the case of some females, vacuolization of oocytes was group-synchronic, which indicates that those females could have defined fertility. On the other hand, in the other females, vitellogenesis of the second batch of oocytes progressed simultaneously with continuous vacuolization indicating asynchronic development of oocytes and undefined fertility (H u n t e r et al. 1992, G r e e r W a l k e r et al. 1994). The filling of almost all trophoplasmatic growth oocytes with yolk in one female before the reproductive season and absence of those oocytes in some females after spawning indicate that some females had single spawning during the reproductive season, which confirmed the earlier studies concerning the presence of females with single spawning during the reproductive season in populations of white bream (Tryapitsyna 1975, Kopiejewska 1996, 1997). The presence of females with single spawning during the reproductive season indicates links of white bream with the single spawning reproduction type characteristic of bream (B r y l i ń s k a & D ł u g o s z 1970, A n d r e e v a 1983). Sexually mature hybrids of white bream and bream from Kuybyshev Reservoir showed characteristics of batch spawning reproduction type (K u t u z o v 1983). Could the white bream females with single spawning reproduction type in this study be hybrids of white bream and bream ? That would require in-depth studies. N i k o l y u k i n (1972) and K u t u z o v (1983) report that the morphological similarity of some individuals of hybrids of white bream and bream to white bream is such that by mistake they can be taken for white bream. On the other hand, M a n n et al. (1984) suggest that the number of batches of spawn can be influenced by the productivity of the habitat and geographic latitude at which the population lives. The potential reproduction can also be influenced by feeding conditions (B r o o k s et al. 1997), age and body size during sexual maturing (M o r g a n & H o e n i n g 1997).

Acknowledgements The photographs were taken by A. K o r y z n o , University of Warmia and Mazury, Olsztyn. The study was supported by Project No 0208 University of Warmia and Mazury, Olsztyn.

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