Annotation of the results obtained in 2021
In 2021, we focused on the laboratory and statistical processing of our own and material obtained in the framework of research collaboration, and writing manuscripts. Also, a significant amount of fieldwork was performed in different seasons on both White and Baltic Seas.. During the winter period in the White Sea we surveyed not only the warm water layer at a depth of 40-60 m, where most of fishes, including herring, but not stickleback, wintering, but also at the depth of 10-20 m, where, according to literature data, stickleback winter in the Baltic. However, sticklebacks were not found there. Therefore, we conclude that threespine stickleback in the White Sea winters offshore and most likely in other places than herring. Probably, it is the open parts of the sea covered with drifting ice which are inaccessible for us now. In the spring, we conducted a comprehensive study of herring in the Chupa Inlet of the White Sea, which included a study of their spawning run, and, later, the distribution of eggs and larvae. In general, herring spawners, eggs and larvae were about an order of magnitude lower than usual. As for larvae, the analysis of long-term data (1982-2021, with gaps) provided by Zoological Institute of the Russian Academy of Sciences and SevPINRO (Arkhangelsk) allows us to speak about it. The lowest numbers of larvae were in 1995, 2014, 2019, 2021, the highest in 1991-93, 2013, 2015, 2018. We were able to show that during the current period of high stickleback abundance (2013-2021), larval abundance was lower than when stickleback was almost completely absent (1982-1995). However, due to high interannual variability in abundance, statistically significant differences were found only for the Chupa Inlet top. This new information is important for understanding the mechanisms of interaction between these two key for our project species. The possibility of direct interaction between them is evidenced by the finding of herring larvae in the stomachs of stickleback during the offshore migration of the former and the inshore spawning migration of the latter in the central part of Chupa Inlet. Although their share in their stomachs was relatively low (5%), calculations based on abundance estimates of stickleback and amount of herring eggs excreted in Chupa Inlet indicate that stickleback consumption of young herring may be comparable with its total abundance, given also that even higher share of herring eggs (20%) in stickleback stomachs was observed. This year, we first observed the spawning migration of stickleback in the central part of the Kandalaksha Bay on a windless white night on June 2, when small shoals of stickleback swam right near the water surface, forming small waves. They were moving from the entrance to Kandalaksha Bay to its inner part, spreading along the shores. The average speed of stickleback shoals was about 1 km/h, and during a few days stickleback occupied all spawning grounds in Chupa Inlet, about 40 km long, but stickleback abundance in the mouth part of the inlet was several times less than closer to its top. We also studied food competition between stickleback and herring in the Baltic Sea based on materials from trawl catches in September 2020. The food spectrum was more diverse for stickleback - 10 taxa vs. 6 for herring. As in the White Sea, food objects of herring were larger, which indicates its size selectivity in favor of larger taxa. High value of Pianka's index of food spectra similarity clearly shows food competition between stickleback and herring. A good information of plankton composition and spatial distribution is very important to assess competition between planktivorous species. In previous years we systematically observed a discrepancy between the content of fish stomachs in the White Sea and plankton composition - there were much more large forms of plankton, primarily copepods Calanus glacialis, but also crayfish Hyperiidae and Euphasiidae, in stomachs than in our samples. This year we used a larger plankton net in addition to the conventional Jedi net, which allowed us to estimate the abundance of these important forms. Parasites are also directly related to the understanding of biotic relations of herring and stickleback, which can influence the species dynamics and their competition. This year, we showed on samples from the Baltic Sea that herring infestation is noticeably lower than that of stickleback from the same trawls. Similar relationships are apparently observed in the White Sea. Here the parasite trematode Cryptocotyle, one of the most abundant in stickleback, has been studied in more detail. We have studied in detail spatial and temporal variability of infection by this parasite, its connection with age, noted higher infection of juveniles, but we are still unable to say with certainty if Cryptocotyle can affect population dynamics of the host species. Also, this year we gave the first description of the stickleback microbiome. Obviously, this is an important aspect of the biology of the species, but it will require much more extensive research to develop. The same applies to studies of lipid metabolism, which, as we have been able to show in experiments, is very sensitive to changes in feeding conditions. Important information has been obtained on the population characteristics of the key species of the project. For stickleback the age structure was described in detail and its different dynamics on different spawning grounds was shown, as well as dependence of mortality on age and sex in the White Sea. For individuals spending their first and second winter, the annual mortality rate is about 80%. At the age of 2 years - 40-50%, after three years - 90-100%. Males survive up to 4 years and females up to 5 years. At one-year-olds, the sex ratio is about equal, and then females predominate. At the same time, using genetic analysis, we found that the predominance of females is sometimes observed already at the fry stage. Studies of different spawning habitats of stickleback in the White Sea were continued, in particular, the small lagoon Koliushkovaya, which is rather favorable spawning ground of stickleback because of increased temperature, low number of predators and abundant food, but there was also a high number of Cryptocotyle parasites. A detailed description of stickleback spawning dynamics in the Baltic is made. Studies of stickleback phylogenetics on the entire species range have shown that the threespine stickleback appeared in the White Sea basin after the last glaciation came from Europe and from the east of North America. Our morphological studies revealed, that the White Sea stickleback has more pronounced sexual dimorphism, than the majority of other populations of the species, which may be connected with a very high competition of males on the spawning grounds due to high density of fish there. We have developed a reliable method for counting stickleback on video images using a method of artificial intelligence, namely neural networks, which greatly expands our ability to study its behavior and spatial distribution in natural environments. Overall, in the final year of the project we were able to meet our plans. Two articles were published in WoS/Scopus list journals, one of which is Q1.

 

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Annotation of the results obtained in 2019
In 2019, it was shown that the seasonal dynamics of threespine stickleback spawning differs in different habitats. It can be assumed that the distribution of stickleback on spawning grounds, which is a key factor in terms of population fecundity, quality and number of offspring and mortality of adults, depends, on the first stage, on the type of habitat, and fish density on the second stage. Relatively isolated habitats such as lagoons, are generally characterized by high density of spawners and juveniles. This is most likely due to relatively high temperatures and absence of predators. Therefore, such habitats may play a significant role in the reproduction of stickleback in the White Sea. Opposite to spawning grounds in the open shores, dynamics of spawning is different here, when females appear on spawning grounds first. Limited water exchange with the sea can create obstacles for the migration of adults and young stickleback. We have developed a technique of sampling stickleback in open waters, and first data were obtained. This data is of great interest to the project, as we have so far been limited to materials obtained from inshore waters, while most of the life cycle of the stickleback occurs in the open sea. This is also where the closest interaction between two central species of the project takes place. We found the high heterogeneity of juvenile stickleback in size. These data may help to better understand patterns of their survival in winter period. The study of trophic links of mass pelagic fish is of key importance for understanding the structure and functioning of the ecosystem. Feeding data of herring and stickleback in the White Sea have shown that their diet is very diverse and notably overlap. In herring, we found 14 taxons and in stickleback - 24 taxons. For stickleback, we observed both seasonal and sexual differences in feeding. In females, 13 food components were found, in males - 24. In contrast, during spawning, female feeding is more diverse than male one - 20 and 13 components respectively (Demchuk et al., 2018). Probably, this is because during spawning males are limited in their activity due to the protection of offspring. Outside the spawning period, if males do not have such limitations, their activity is higher than females. Feeding data indicate a close trophic interaction between herring and stickleback in the White Sea. In particular, the presence of herring larvae has been observed in the open sea in stickleback stomachs. In turn, stickleback juveniles represent a significant proportion of herring diet in August (30%). Thus, stickleback and herring, on the one hand, can compete indirectly, due to limited common feed resources, and on the other hand, preying on each other's juveniles, compete directly. Our results on herring feeding show surprisingly low proportion of plankton organisms, although herring is often considered to be a typical planktivorous fish. According to our data, herring in the White Sea mainly feeds on fairly large organisms, including juveniles and adult fish of other species. These data certainly require confirmation. In the Gulf of Finland, plankton copepod crustaceans Eurytemora sp. were the dominant taxa in the food spectrum of stickleback (Ii = 44%) along with stickleback eggs (34%) and Chironomidae pupae (13%). Together, they accounted for more than 90% of the diet. This is generally consistent with earlier data (Golubkov, 2018). Stickleback feeding is more diverse in the Baltic than in the White Sea, with 33 taxa found here. In terms of studying competition between stickleback and herring in the face of climate change and the associated increase in stickleback abundance, valuable information can be obtained from comparative studies of the distribution of herring and plankton larvae in different periods that have begun this year. However, it is still too early to draw conclusions from these studies, as a detailed comparison of data obtained by different methods in different historical periods is required. We also plan to involve materials obtained by SevPINRO (Arkhangelsk) for comparison. In general, the results obtained during the first year of the project, are consistent with the plans, although some areas have been developed in more detail than others. This was due both to the specific weather conditions in 2019 and to the fact that the planning of work depends on specific circumstances, which are not always possible to predict in advance. In 2020, we plan to continue the studies we have started, and use various methods of population analysis, and analysis of the trophic status of fish based on that. Studying the size-age structure, migration of fish in spawning grounds and their response to different stimulus in experiments will provide an understanding of the factors influencing their distribution and abundance. Studying the density, size of stickleback nests and stages of embryo development in them will allow us to assess the level of population fecundity and mortality at early stages of development, including in connection with stickleback cannibalism. The stable isotope method will provide an independent picture of the trophic connections of the studied species in comparison with the analysis of stomach contents - on the one hand, less detailed, but more integral on the other hand. The stoichiometric approach, as well as the study of the microbiomes will allow an independent assessment of their physiological status.

 

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Annotation of the results obtained in 2020
Last year a number of important results on our project was obtained. The analysis and publication of data on long-term population dynamics of threespine stickleback in the White Sea were completed. On the basis of generalization and analysis of heterogeneous historical data, such as scientific and personal observations, archival data on fisheries, the dynamics of stickleback abundance in the White Sea for the last century and a half has been described. This is the longest time series of abundance for this species. The stickleback abundance was the highest during the warm period of 1920-1940s, and decreased during the colder period of 1950-1990s. The modern rise of stickleback, making it the most abundant fish in the sea, began in the late 1990s and became the object of our studies. Combining of historical and modern data showed that stickleback abundance decreases due to cold winters. It is not related to zooplankton biomass, positively correlated with herring Clupea sp. catches and negatively correlated with navaga Eleginus navaga catches. Thus, it was possible to relate stickleback abundance dynamics to temperature conditions and abundance of other most important components of the White Sea ecosystem. These results facilitate identification of further directions of our studies. Using the methodology of quantitative survey of threespine stickleback in open water areas, developed last year, we managed to clarify a number of important aspects of the species biology in the White Sea. The dynamics of spatial distribution of stickleback within several kilometers from the shore was described. Only about a half of fish are on spawning grounds at a time. The rest, judging by the state of their gonads, will spawn later. This leads to a noticeable increase in our estimates of the number of stickleback in the White Sea, because previously we assumed that during the peak of spawning, all mature stickleback are in the coastal area and are accounted for by our beach seines. It turned out that in open water areas the proportion of males is lower (17%) than in the coastal areas (40%), indicating that the systematic significant predominance of females in our catches observed throughout the study period is a consequence of their predominance in the population as a whole, and not due to specific patterns of spatial distribution of different sexes during the spawning period. Eggs in stickleback nests appear 5-6 days after the fish appear at the spawning grounds. At the peak of spawning, the density of stickleback nests on spawning grounds with dense seagrass beds was 3 per m2, and about 0.4 per m2 in fucoids. At the beginning of incubation, there were an average of 766 eggs in the nests, and by the end, the number of eggs decreased several times. Since stickleback eggs are an important food source for stickleback during the spawning period, we suggest that a significant proportion of the nests are eaten by the stickleback. Predators, primarily cod, also contribute to embryo mortality. Juvenile stickleback appear in early July and their numbers increase until early August. When they reach about 25 mm in body length, which usually occurs in late July, the juveniles begin their offshore migration, although until mid-August most of the fry (80-90%) still remain near shore. In early August juveniles start leaving the open sea, and by early September all juveniles leave the inshore zone, and most of them (80%) already left the inlets migrate into the open sea. In mid-September, all juveniles occur at a distance of several kilometers from the shore. The average size of juveniles in the pelagic zone during the entire observation period is 6-7 mm larger than in the coastal zone. At the same time, it is impossible to describe the growth patterns of juveniles based on average length of samples, since the largest juveniles constantly leave the inshore area and then move further into the open sea. Therefore, the average size of juveniles in both coastal and pelagic waters is smaller than the average size of juveniles at a given time. Adult stickleback feeding on the spawning grounds is much more diverse than in the open sea. For example, in pelagic fish, in early June and August, the diet of fish consisted of 7 and 11 components, respectively, with a clear dominance (up to 90%) in the food spectrum of one taxon - copepods Calanus glacialis in June and cladocera Podon leuckarti in August. In coastal waters in June-July, the number of food items reached 33 components, decreasing to 17 in areas of temporary accumulation of fish in open water areas near spawning sites. On spawning grounds, stickleback prefers benthos to plankton, and quite easily switch to the most available objects at a given time. In early July, small forms dominated in zooplankton in the open parts of the sea, but they were almost absent in the stomachs of stickleback, indicating a selectivity towards the largest food objects inhabiting significant depths, such as C. glacialis and pteropod Limacina helicina. This means that stickleback approach the spawning grounds at fairly high depth. Males have a less diverse diet than females, apparently due to limited mobility due to care of offspring. Judging by the diet of females after spawning in nearby pelagic areas, they leave spawning grounds earlier than males whose stomachs at that time are still full of coastal organisms in the same areas. Feeding of males and females in the open sea is also different. Males and females may feed at different depths. For example, in open waters, the main component of the female diet was copepoda Pseudocalanus sp., whose share in the planktonic community is much higher in the lower layers (20-40 m), while in males - cladocera P. leuckarti, inhabiting massively in the upper layers (0-10 m). Herring feeding in the White Sea is characterized by high individual heterogeneity. Like the stickleback, herring prefer the larger food objects such as Pseudocalanus spp. and Calanus glacialis. Both of these species also tend to form dense aggregations. Copepoda Metridia longa, which is also a rather large organism found in zooplankton samples, does not form dense clusters. Probably, that is why it was not found in the herring diet. Herring, like the other planktivours fish - capelin, generally prefers larger and mobile zooplankton, represented, besides the copepods noted, also by crustaceans of the families Hyperiidae and Euphausiidae, which were not found in our zooplankton samples, as they actively avoid the plankton net. In the future, we plan to use special nets in order to adequately assess these large mobile forms. Threespine stickleback (adults, roe and juveniles), in turn are an important food source for mass species of predatory fish living in the coastal area (sculpins) or coming there for feeding (cod, navage, herring). In inlets with dense beds of Zostera marina (preferred spawning grounds), stickleback comprises a higher proportion of the diet of predators than in fish from open areas or from protected areas with thickets of fucoids or low density of seagrass thickets. Stickleback make up a higher proportion of the diet of the studied species in locations with their high abundance. In some species, such as European sculpin, stickleback may be the only food. The role of herring as well as other fish (sandeel, ninespine stickleback) in the diet of predators is much less significant. With growth in the diet of the studied predators there is a shift from small invertebrates and juveniles of threespine stickleback to larger invertebrates (polychaetas, crustaceans), and then to the adult stickleback and, to a lesser extent, sandeel. In the diet of large cod the eggs of threespine stickleback constitute a significant portion. Works carried out in the Gulf of Finland also allow us to give a rather detailed description of stickleback spawning. At the beginning of spawning in May, maximum densities (up to 0.48 specimens/m2) of adult stickleback were recorded. By July, the stickleback gradually moved away from the spawning grounds, and in August and later we found only solitary individuals. At some stations in May, a fairly high number of immature fish (up to 30%) were recorded coming to shore with adult fish. In July and later they were not recorded. Gonado-somatic index of females, as well as their standard length, increased from May to July. Apparently, larger females ready to spawn come to the spawning grounds later than smaller ones. No departures in the sex ratio in the coastal waters of the Gulf of Finland, in contrast to the White Sea, were noted. Juveniles appear at all the stations studied in July, their density ranged from 0.009 ind./m2 to 1.286 ind./m2, with higher densities of juveniles at the northern shore of the Gulf of Finland than at the southern shore. During the warm season, 20 taxa were found in the stomachs of adult Gulf of Finland stickleback, all of which were found in the diet of females, and only 14 taxa were found in males. The reasons for such differences, as in the White Sea coast, are most likely lie in higher activity of females after spawning. After spawning, they start to feed actively, while males are occupied with protecting their nests. Throughout most of the season, the diet of both sexes was based on Chironomidae var. (larvae and pupae). A significant part of the diet in May and July (the spawning period) was its own eggs, and in July also fry. In addition to threespine stickleback, 14 other fish species belonging to 7 families were caught in the coastal area in 2020. The most abundant of them were the ninespine stickleback, bleak, gudgeon and roach. A comparative analysis of the diets of all these species suggests that the threespine stickleback can be a food competitor of the ninespine stickleback; with other species the overlap of the food spectra is much less. Detailed morphological studies of the White Sea stickleback have been carried out, in particular, its sexual dimorphism has been studied. It has been shown that in comparison with other populations of this species, the White Sea stickleback has relatively well developed anterior part of the body and spines, i.e. its body shape is shifted towards the male type. This may be caused by very high densities of spawners on the White Sea spawning grounds, which leads to high competition between males and, accordingly, to the increased development of those morphological structures which allow to obtain an advantage in this competition. In general, the data obtained on sexual dimorphism allow us to relate features of the body shape of males and females to their behavior (higher propensity of females to various migrations, and higher maneuverability and aggressiveness of males), as well as a shift of the sex ratio towards females. Seven articles have been published this year, four of which are in Q1 journals.

 

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