Роль Beroe ovata Bruguiere 1789 в качестве биологического контроля вредоносного вселенца Mnemiopsis leidyi A. Agassiz 1865 в морях Понто-Каспия


Role of Beroe ovata Bruguière 1789 as a biological controller of harmful invader Mnemiopsis leidyi A. Agassiz 1865 in the Ponto-Caspian seas

Шиганова Т.А.

Tamara A. Shiganova
 

Институт океанологии имени П.П. Ширшова РАН (Москва, Россия) 
 

Shirshov Institute of Oceanology RAS (Moscow, Russia)

 

УДК 574.5

На примере Понто-Каспийского бассейна, включающего Черное, Азовское и Каспийское моря, мы проанализировали вселение вредоносного гребневика Mnemiopsis leidyi A. Agassiz, 1865, вызвавшее деградацию всех трех экосистем и рыбных запасов и незапланированное появление его хищника Beroe ovata Bruguière 1789, который выполняет функцию биологического контроля над этими морскими экосистемами, что приводит к их постепенному восстановлению.

Ключевые слова: экология; чужеродные виды; биоконтроль

 Using the Ponto-Caspian basin, which include The Black, Azov and Caspian Sea as a case study, we have analyzed invasion of harmful ctenophore Mnemiopsis leidyi A. Agassiz, 1865, which caused the degradation of all three ecosystems and fish stocks and unplanned appearance of its predator Beroe ovata Bruguière 1789, which functioning as biological control for all these marine ecosystems, which leads to their gradual recovery..

Keywords: ecology; invasive species; biocontrol

Introduction

The Black, Azov and Caspian Seas were united in a single basin several times in the past, most recently in the Pliocene. Since 1952 all three seas were reconnected artificially again via the Volga-Don Canal (fig. 1). The Black Sea is also connected with the Mediterranean Sea.

Fig. 1. Map of the modern Caspian, Black and Azov Seas, the Volga–Don Canal and Volga Baltic Canal

Рис. 1. Карта современных Каспийского, Черного и Азовского морей, Волго-Донского
и Волго-Балтийского каналов

Owing to accelerating of the human activities like shipping, deliberate stocking, unintentional releases, and canal construction, many non-native species of phytoplankton, zooplankton, benthos and fish have arrived and established in these seas, causing ecosystem-wide effects (Shiganova, 2010).

One of the most remarkable invasions was that of the comb jelly, Mnemiopsis leidyi, a ctenophore native to western Atlantic coastal waters (Ghabooli et al., 2011), which was introduced accidentally by merchant ships' ballast water in the Black Sea. It was first observed in the early 1980s and became highly abundant since 1988 (Vinogradov et al., 1992). The Black Sea became permanent habitat (source area) for M. leidyi. From here, after spring warming, it penetrates with the currents into the Sea of Azov (sink area), creating reproductive population, grazing zooplankton and disappear after temperature drop below 4℃ (Studenikina et al., 1991).

In 1999 Mnemiopsis leidyi was first recorded in the Caspian Sea (Ivanov et al., 2000). It permanently lives only in the Southern Caspian, where the temperature does not decrease below 10°C, and with spring warming begins to spread with current in the Middle and then in the Northern Caspian, where the salinity is higher 4‰.

 Result

The invasion of the ctenophore Mnemiopsis leidyi caused a major decline in fish resources in the Ponto-Caspian seas. Its massive predation on zooplankton produced cascading effects at higher trophic levels, from a decrease in zooplankton to collapsing planktivorous fish (fig. 2) and drastic declines among large pelagic fish and marine mammals (dolphins in the Black, Azov seas and seal in the Caspian) were documented. Decrease in zooplankton also caused an increase in phytoplankton and increases in bacterioplankton, which led to increases in their predators, zooflagellates, and ciliates (Shiganova et al., 2004 a, b). Losses from the impact of M. leidyi were estimated in billions of US dollars annually for the Black Sea and Caspian countries. Catches of pelagic fish, first of all small ones ceased in Russia as well as in other Black Sea countries (Dumon et al., 2004).

In the Caspian Sea with the development of Mnemiopsis leidyi, there was a devastating drop of the anchovy kilka Clupeonella engrauliformis (Borodin, 1904) and of big-eyed kilka C. grimmi Kessler, 1877 catches in the Middle and Southern Caspian Sea due to their spawning and development period matches that of M. leidyi development (fig. 3), which facilitates the high level of competition for food (i.e., zooplankton).The common kilka C. caspia Svetovidov, 1941 suffered less, because it can migrate to the brackish and even fresh waters of the Northern Caspian and feeds on brackish and fresh-water plankton (Paritsky and Razinkov, 2014).

Fig. 2. Change of the total catch (tons) of planktivorous fish (Sprattus sprattus Linnaeus, 1758, Clupeonella cultriventris (von Nordmann 1840), Engraulis maeoticus Pusanov & Zeeb, 1926, E. engrasicolus (Linnaeus, 1758) in the Black Sea and Sea of Azov before and after M. leidyi invasion (after Shiganova, Bulgakova, 2000)

Рис. 2. Изменение общего вылова (тонны) планктоядных рыб (Sprattus sprattus Linnaeus, 1758, Clupeonella cultriventris (von Nordmann 1840), Engraulis maeoticus Pusanov & Zeeb, 1926, E. engrasicolus (Linnaeus, 1758) в Черном и Азовском морях до и после инвазии M. leidyi (по Shiganova, Bulgakova, 2000)

Fig. 3. Total annual Russian catches of kilka in 2001–2016 in the Caspian Sea

Рис. 3. Общий годовой улов кильки в России в 2001–2016 гг. в Каспийском море

Even the most valuable fish i.e., sturgeons, suffered from Mnemiopsis leidyi impacts. Before the invasion of M. leidyi, mollusks were the main food of Russian sturgeons. Juvenile and adult sturgeon also fed on Caspian kilkas (anchovy, common and big-eyed). Kilka was an essential food of sturgeon populations in the Middle and Southern Caspian, where the share of kilka in sturgeon diet reached 40%. In the diet of both Russian sturgeon (Acipenser gueldenstaedtii Brandt & Ratzeburg, 1833) and stellate sturgeon (Acipenser stellatus Pallas, 1771), a high share of kilka was observed in winter and spring and reached up to 20–40% in sturgeons food. Since 2000, the total stocks of kilka decreased and so did their share in sturgeon diet. Only the common kilka was recorded in the diet of the Russian and stellate sturgeon and beluga Huso huso (Linnaeus, 1758) (Kamakin et al., 2018).

Ten years later, in 1997 after the first observation of Mnemiopsis leidyi in the Black Sea, another warm-water ctenophore, Beroe ovata Bruguière, 1789, a predator on M. leidyi, was introduced with ballast water from the same area of the Northern America as M. leidyi (Shiganova & Abyzova, 2021). 

Beroe ovata invasion reduced Mnemiopsis leidyi populations and the ecosystem began to recover at all trophic levels (fig. 4).

Fig. 4. Relationship of Mnemiopsis leidyi and Beroe ovata abundance (ind.m^-3) after B. ovata appearance in the Black Sea

Рис. 4. Соотношение численности Mnemiopsis leidyi и Beroe ovata (экз.м^-3) после появления B. ovata
в Черном море

At present, Beroe ovata, having reached its peak in the Black Sea every year, penetrates into the Sea of Azov and in recent years, with increasing salinity in the Sea of Azov, it is able to spread widely in it and control the population of Mnemiopsis leidyi.

Since 2000 small pelagic species stocks and catches began gradually recover in the Black Sea. The highest catches comprised Azov anchovy and sprat (fig. 5), Mediterranean horse mackerel and red mullet followed.

Using this positive example of the Black Sea in order to assess an ability of Beroe ovata to combat Mnemiopsis leidyi population in the Caspian Sea, an international research team performed extensive laboratory experiments in Iran, using Caspian individuals of M. leidyi as a food for individuals of B. ovata, which were collected in the Black Sea (Drs. Shiganova T., Kideys A., Finenko G. and Annensky B.). In addition, Dr. Shiganova and Bulgakova performed experiments in Gelendzhik, Russia, with the Black Sea B. ovata, and determined that the species is able to survive at a minimal salinity of 7‰ and reproduces at minimal salinity of 10‰. Other studies indicated that B. ovata starts to release eggs at minimal temperature 19°C, peaks at 25–26°C and ceases at 29°C (Shiganova, 2004).

According to these results and in response to challenges, associated with the Caspian Sea ecosystem deterioration, a team of international experts, supported by Commission of the Caspian Sea Environmental Program (CEP), proposed to introduce Beroe ovata into the Caspian Sea to biologically control the population of the invasive Mnemiopsis leidyi and prepared “Environmental impact assessment on B. ovata introduction” (Shiganova, 2004). Proposals for deliberate introductions of B. ovata in the Caspian Sea have been submitted; however, this suggestion was not supported con-currently by all Caspian countries for 3 years due to doubts on the effectiveness of its biological control. Thus, we had to wait for B. ovata spontaneous penetration with ballast waters from the Black Sea via the Volga–Don Canal as those happened with other pelagic invaders. In fact, recently in 2019, B. ovata was recorded in the Southern Caspian and in 2022 first data on decreasing of M. leidyi population were collected for the first time (Shiganova et al., 2023).

Fig. 5. Change of small pelagic fish catches after Beroe ovata arrival in the Black Sea

Рис. 5. Изменение уловов мелкой пелагической рыбы после появления Beroeovata в Черном море

Fig. 6. Observations of Beroe ovata and Mnemiopsis leidyi in the Caspian Sea: red dots – transects in the Iranian waters in 2019–2020 (after Roohi et al., 2022, and after Bagheri et al., 2021); in 2021–2022 (blue dots – transects in Azerbaijani waters (this study); green dots – stations in the Middle Caspian in 2020 (after; Sayapina et al., 2021); violet dot – station off Makhachkala in 2020 (Vostokov et al., 2020). Neighboring yellow dots indicate simultaneous presence of M. leidyi during the observations. Circles indicate the ratio of mean abundance of M. leidyi (1); B. ovata (2); blank circle (3) indicate an absence of both ctenophores; attached labels indicate months and years of observation

Рис. 6. Наблюдения за Beroe ovata и Mnemiopsis leidyi в Каспийском море: красные точки – transects in the Iranian waters in 2019–2020 (по Roohi et al., 2022 и Bagheri et al., 2021); in 2021–2022 (blue dots – transects in Azerbaijani waters (this study); green dots – stations in the Middle Caspian in 2020 (after; Sayapina et al., 2021); violet dot – station off Makhachkala in 2020 (Vostokov et al., 2020). Neighboring yellow dots indicate simultaneous presence of M. leidyi during the observations. Circles indicate the ratio of mean abundance of M. leidyi (1); B. ovata (2); blank circle (3) indicate an absence of both ctenophores; attached labels indicate months and years of observation

Summarizing above mentioned published information for 2019–2023 (fig. 6), we argue that Beroe ovata now establish in the Caspian Sea. The Southern Caspian is its main habitat, as well as that of Mnemiopsis leidyi and is their source area. Presumably, B. ovata will follow M. leidyi to areas with appropriate temperature and salinity conditions, which are the Southern and Middle Caspian in warm seasons. The northern boundary of the B. ovata occurrence locates in the Middle Caspian, where salinity is lower than 10‰. However, some individuals are able to penetrate in the southern part of Northern Caspian, but without reproduction ability. Individuals of M. leidyi penetrated further in the Northern Caspian, where salinity was higher than 4,5‰ (fig. 6).

So, there is an expectation that after a while, Mnemiopsis leidyi probably will not be able to reach the Northern Caspian, being completely consumed by Beroe ovata in the Southern and Middle Caspian. Supposedly, with the time the predation of B. ovata on M. leiidyi will contribute to a gradual recovery of the Caspian Sea ecosystem. Ctenophore B. ovata, like M. leidyi, is a hermaphrodite with high fecundity, capable to self-fertilization; up to 100% of normal development can repeatedly happen from self-fertilized eggs of single individuals. Therefore, several individuals in the favorable environmental conditions (temperature and salinity) with prey (M. leidyi) availability are sufficient to produce established population. Thus, B. ovata seems to be simple, effective and cheap bio-control agent to combat M. leidyi.

The material for the study was obtained in the process of fulfilling the State assignment of the Shirshov Institute of Oceanology RAS No. FMWE-2021-0009.

Материал для исследования был получен в процессе выполнения Государственного задания Института океанологии им. П.П. Ширшова РАН № FMWE-2021-0009.

The author declares no conflicts of interest.

Авторы заявляют об отсутствии конфликта интересов, требующего раскрытия в данной статье.

Список литературы

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16. Shiganova T.A., Kamakin A.M., Pautova L.A., Kazmin A.S.,Roohi A., Dumont H.J. An impact of non-native species invasions on the Caspian Sea biota // Advances in Marine biology. 2023. V.94. P. 69–157. DOI: https://doi.org/10.1016/bs.amb.2023.01.002

Статья поступила в редакцию 10.11.2023
После доработки 06.12.2023
Статья принята к публикации 10.12.2023

Об авторе

Шиганова Тамара Александровна −Tamara A. Shiganova

доктор биологических наук
главный  научный сотрудник, Институт океанологии им. П.П.Ширшова РАН, Москва, Россия (P.P. Shirshov Institute of Oceanology RAS, Moscow, Russia)

shiganov@ocean.ru

https://orcid.org/0000-0001-6395-5574

Корреспондентский адрес: Россия, 117997, г. Москва, Нахимовский проспект, 36, ИО РАН. 

ССЫЛКА:

Шиганова Т.А. Роль Beroe ovata Bruguière 1789 в качестве биологического контроля вредоносного вселенца Mnemiopsis leidyi A. Agassiz 1865 в морях Понто-Каспия // Экология гидросферы. 2023. №2 (10). С. 10–17. URL: http://hydrosphere-ecology.ru/391

DOI – https://doi.org/10.33624/2587-9367-2023-2(10)-10-17     EDN – KFLYVR 

При перепечатке ссылка на сайт обязательна

Role of Beroe ovata Bruguière 1789 as a biological controller of harmful invader Mnemiopsis leidyi A. Agassiz 1865 in the Ponto-Caspian seas

Tamara A. Shiganova

Shirshov Institute of Oceanology RAS (Moscow, Russia)

Using the Ponto-Caspian basin, which include The Black, Azov and Caspian Sea as a case study, we have analyzed invasion of harmful ctenophore Mnemiopsis leidyi A. Agassiz, 1865, which caused the degradation of all three ecosystems and fish stocks and unplanned appearance of its predator Beroe ovata Bruguière 1789, which functioning as biological control for all these marine ecosystems, which leads to their gradual recovery.

Keywords:  ecology; invasive species; biocontrol

References

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   2. Dumont H.J.D., Shiganova T.A., Niermann U. Conclusions from the meeting. In: Dumont, H., Shiganova, T.A., Niermann, U. (eds) Aquatic Invasions in the Black, Caspian, and Mediterranean Seas. Nato Science Series: IV: Earth and Environmental Sciences, Vol. 35. Springer, Dordrecht, 2004. P. 301– DOI: https://doi.org/10.1007/1-4020-2152-6_18
   3. Ghabooli S., Shiganova T.A., Zhan A., Cristescu M.E., Eghtesadi-Araghi P., MacIsaac H.J. Multiple introductions and invasion pathways for the invasive ctenophore Mnemiopsis leidyi in Eurasia. Invasions. 2011. V.13. P. 679–690. DOI: https://doi.org/10.1007/s10530-010-9859-8
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   16. Vostokov S.V., Gadgiev A.A., Vostokova A.S., Rabazanov N.I. The ctenophore Beroe cf. ovata in the Caspian Sea. The beginning of a new stage in the evolution of the Caspian ecosystem? South of Russia: ecology, development. V.15. No. 4. P. 21–35. DOI: https://doi.org/10.18470/1992-1098-2020-4-21-35 (in Russ.)

    

Author

Shiganova Tamara A. 

P.P. Shirshov Institute of Oceanology RAS, Moscow, Russia

shiganov@ocean.ru

https://orcid.org/0000-0001-6395-5574

ARTICLE LINK:

Shiganova T.A. Role of Beroe ovata Bruguière 1789 as a biological controller of harmful invader Mnemiopsis leidyi A. Agassiz 1865 in the Ponto-Caspian seas. Hydrosphere Ecology. 2023. №2 (10). P. 10–17. URL: http://hydrosphere-ecology.ru/391

DOI – https://doi.org/10.33624/2587-9367-2023-2(10)-10-17     EDN – KFLYVR 

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