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Exploring Diversity of Baltic Sea Biota: New Tools, Results, and Implications

This study focuses on the past and modern invasive stories of Onychopoda (Cladocera) in the Baltic Sea. It examines molecular biology methods as a tool for studying the genus Cercopagis. The study aims to answer taxonomy, morphology, and distribution-related questions using new tools, results, and implications.

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Exploring Diversity of Baltic Sea Biota: New Tools, Results, and Implications

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  1. Exploring diversity of Baltic Sea biota:new tools, results and implications Past and modern invasive stories of Onychopoda (Cladocera): molecular-biology methods as a tool for the studywith special attention to genus Cercopagis Aladin N.V. (Zoological Institute RAS)in co-operation with: Plotnikov I.S. (Zoological Institute RAS), Chuikov Yu.S. (Environment Protection Agency of Astrakhan Region) Tvärminne Zoological Station, University of Helsinki, on April 22-24, 2005

  2. Within Cladocera, four major taxa can be distinguished: Anomopoda, Ctenopoda, Haplopoda and Onychopoda. • The last one shows remarkable geographical distribution. Most of the described species are restricted to the Caspian Sea, the Aral Sea, and peripheral areas of the Black Sea, including the Sea of Azov, i.e. in the remnants of Eastern Paratethys. • The remaining onychopods are either freshwater inhabitants or marine animals, widespread in the world ocean.

  3. Molecular phylogenetic analysis has demonstrated monophyly of three Onychopoda families, and sister group relationship between Onychopoda and Haplopoda (Richter, S., Braband, A., Aladin, N., Scholtz, G., 2001, Mol. Phyl. Evol.). • We suggested an independent invasion into the Ponto-Caspian basin at least three times, twice originating in Palearctic freshwater bodies and once starting from the world ocean.

  4. Currently we would like to apply molecular markers to study the modern invasions of Onychopoda: Bythotrephes sp., Cercopagis sp., Cornigerius sp., Podonevadne sp. and Evadneanonyx. • Bythotrephes sp. invaded and settled in freshwater reservoirs and lakes in Europe and later invaded and settled in Great American Lakes. • Cercopagis sp. invaded and settled in Baltic Sea and later invaded and settled in Great American Lakes. • Recently it was reported that Cornigerius sp., Podonevadne sp. and Evadneanonyx are going to invade Baltic Sea. There is some chance that these species could be settled in the Baltic Sea and may go further .

  5. We would like to put some questions that should be answered using new tools, results and implications.

  6. Let’s start from taxonomy.

  7. Onychopoda consists of Podonidae, Polyphemidae and Cercopagidae

  8. The following structure of genus Cercopagis was proposed by Mordukhai-Boltovskoi in 1968.

  9. Polyphemoidea = OnychopodaRivier, 1998

  10. Polyphemoidea = OnychopodaAladin et al., 1999

  11. Polyphemoidea = OnychopodaAladin et al., 2000

  12. Polyphemoidea = OnychopodaAladin et al., 2005

  13. Our present opinion is that only 3 Cercopagis species are available. Two species: C. socialis and C. micronyx are capable for sexual reproduction and one C. cylindrata is capable only for parthenogenitic reproduction.

  14. The following message I got from Hugh. Regardless morphological difference DNA studies showed that in North America only one species of Cercopagis that we prefer to call C. socialis (regulation of priority).

  15. What taxonomy questions we should answer? • Using classical and molecular biology studies we should answer how many species of Cercopagis, Cornigerius and Podonevadne are living now in Northern America and Eurasia. • We need to check again weather we have only one species: Bythotrephes longimanus as recent molecular-biology studies showed us. • We need special taxonomic revision of the whole Onychopoda group for better understanding of all three families.

  16. Let’s continue with morphology.

  17. Morphology of Cercopagis is diverse due to cyclomorphosis, cloning and predators impact

  18. Some scientists believe that hook is using to anchor during sexual reproduction. Others believe that hook serves against predation.

  19. Asexual (parthenogenetic) forms (clones) have no hook. Some scientists believe that hook also absent in spring forms that just hatched from resting eggs.

  20. A photograph of Cercopagis without hook, that I got from Henn in autumn 1998.

  21. Morphological differences between male, parthenogenetic and gamogenetic females is quite high. For some Cercopagis species males are still not known.

  22. Cercopagis is much smaller than Bythotrephes. Students from Asko Laboratory (Sweden) in the beginning determined Bythotrephes as Cercopagis. Originally scientists identified at least two Bythotrephes (B. cederstroemi and B. longimanus). Now after DNA studies left only B. longimanus.

  23. What morphology questions we should answer? • It will be nice to understand the reasons of morphological differences. Are they induced by different density of water that depends from salinity and temperature (cyclomorphosis)? • Could some morphological structures (hooks or horns, sharp end of brood pouch) save from predators? • Is there any connection between reproduction mode and availability of hook? • Which morphologycal parameters are enough stable to serve taxonomy and are good to be used in species identification keys?

  24. Let’s continue with distribution.

  25. Cercopagis native areas and invaded areas in Eurasia.

  26. Cercopagis invaded areas in Northern America.

  27. Worldwide distribution of Cercopagis (native and invaded areas) In Aral Lake Cercopagis was last observed in summer 1980. In Sudochie Lake Cercopagis was last observed in autumn 1982. In Sudochie Reservoir, that replaced the lake, Cercopagis was last observed in autumn 1999. In recent samples collected in this reservoir (2000-2004) Cercopagis was absent.

  28. The following message I got from Ragnar. It is important to note that even in rich country as Sweden not enough money for monitoring.

  29. What distribution questions we should answer? • We need very carefully to check samples from freshwater lakes around Baltic Sea. Is Cercopagis already invaded them but local researchers are continuing to label it as Bythotrephes? • Special monitoring program for control of possible invasions of Cercopagis to freshwater lakes in Northern Europe is needed. Why not to give special attention to Ladoga and other big lakes of Northern Europe? • At what stage from the life cycle Bythotrephes, Cercopagis, Cornigerius, Podonevadne are traveling around the world? Are they living organisms in ballast waters or resting eggs attached to fouling organisms outside the boat?Or both?

  30. Let’s continue with ecology.

  31. Cercopagis in the Aral Sea was observed for the last time in summer 1980.Before that it always was presented in zooplankton.It disappeared due to salinisation.More info about the fate of Cercopagis in Aral you may have from http://www.zin.ru/labs/brackish/files/Plankton-3E.zip In this lake Cercopagis never reached high abundances.The same is true for Cercopagis from the Caspian Sea.

  32. In opposite to native areas (Caspian, Aral, Black, Azov Seas) Cercopagis in newly invaded lakes and seas started to reach high levels of abundance (several thousands individuals in m3). Cercopagis formed a paste that led fishing nets to sink.

  33. Luckily more often abundance of Cercopagis in invaded areas is much lower (several hundreds individuals in m3).

  34. In Internethttp://www.caspianenvironment.org/biodb/eng/zooplankton/Cercopagis%20pengoi/main.htmthe following information about feeding is given: Feeding type. HeterotrophicFeeding behavior. Members of the family Cercopagidae are active predators. Cercopagids capture prey (mainly small plankton crustaceans) with the first pair of thoracic legs (thoracopods I), retain prey by other three pairs of thoracic legs (thoracopods II-IV), crush its cuticle by mandibles, and suck the prey body contents. Detailed information on feeding behavior of C.(C.) pengoi is not available. Food spectrum. Information is not available.Supply of food. Information is not available.Quantitative characteristics of feeding. Information is not available. From this situation it is clear that more studies are needed. Recent experiments made by Joseph Makarewicz team gave some more info on this matter. Unfortunately direct filming still is not available. Takashi Onbe tried to do this but didn’t succeed. Lot of scientists still believe that Cercopagis is omnivorous. If Cercopagis is strictly carnivorous at the bottom of aquaria should be lots of exeskeletons of sucked victims. Unfortunately we didn’t see them in our aquarias.

  35. In Internet on the same page (paragraph on Life history and development ) it is said: Parthenogenetic females of the first generation of C. (C.) pengoi, hatch from resting eggs, and are anatomically distinct from parthenogenetic females of following generations. They resemble С. (Apagis)ossiani M.-Bolt., which are characterized by 4 pairs of caudal spines, a significantly shortened caudal process without a loop and maximal fecundity (Simm and Ojaveer, 1999; Rivier 2000; Grigorovich et al., 2000; Rivier unpubl.). From this situation it is clear that more studies are needed. Cercopagis ossiani according to Mordukhai-Boltovskoi is very rare morphotype. If this hypothesis about spring forms is correct, at the beginning of spring should be a lot of these forms in all known localities. We have a lot of sympathy to this hypotheses, but unfortunately we don’t know data confirming this hypotheses. Special experiments are needed as well as direct observations during special spring monitoring.

  36. What ecology questions we should answer? • We need to find an answer why in invaded areas abundance of Cercopagis is so high if compare with native one. • Is this happened due to some changes in Cercopagis physiology or behavior in new localities? • Are Cercopagis, Cornigerius and Podonevadne true carnivorous? • Are Cercopagis, Cornigerius and Podonevadne omnivorous? • Is Cercopagis without hook available only in the beginning of life cycle shortly after hatching from resting eggs? • How it is possible to explain from ecological point of view that “true predator” Cercopagis is reaching abundance of several thousands individuals in m3?

  37. Let’s continue with physiology.

  38. Cercopagis is fairly eurytherm crustacean.Differences are not high regardless the origin of studied population.

  39. Cercopagis is fairly eurytherm crustacean.Differences are not high regardless the origin of studied population.

  40. Due to good tolerance to low temperatures Cercopagis parthenogenetic females could survive in Baltic Sea waters with high thermal pollution.

  41. Near atomic power plant in Sosnovy Bor even in winter water temperature always is positive and surface is never covered with ice. It is possible that parthenogenetic females of Cercopagis could survive here.

  42. Cercopagis is fairly euryhaline crustacean.Differences are not high regardless the origin of studied population.

  43. Cercopagis is fairly euryhaline crustacean.Differences are not high regardless the origin of studied population.

  44. According to our studies and those of our colleagues from Lancaster University Cercopagis is capable only to hyperosmotic regulation. • This organism could be osmoconformer in the very short range from 5-8 g/l up to 17 g/l. • Cercopagis hemolymph is hyperosmotic to surrounding water only in the range from fresh water up to 5-8 g/l. • Cercopagis will never invade even the Baltic Sea straits connecting it with the World Ocean. Salinity is too high. • Way of Cercopagis osmoregulation in identical to those of Bythotrephes and Polyphemus. It is the huge difference in osmoregulation capacities of marine and brackish water Podonidae. • From the point of view of osmotic regulation Cercopagis is very close to freshwater organisms and is very far from marine and Caspian Podonidae.

  45. According to our studies and those of our colleagues from Lancaster University Cornigeriis, Podonevadne and Evadne anonyx are capable only to amphyosmotic regulation. • These organisms could be hypoosmotics in the range from 5-8 g/l up to 22-35 g/l. • Cornigeriis, Podonevadne and Evadne anonyxhemolymph are hyperosmotics to surrounding water only in the range from fresh water up to 5-8 g/l. • These organisms could invade the whole Baltic Sea and even straits connecting it with the World Ocean. All Podonidae are better osmoregulators than Cercopagidae. • From the point of view of osmotic regulation Cornigeriis, Podonevadne and Evadne anonyxare very close to marine organisms and are very far from freshwater Cercopagidae.

  46. What physiology questions we should answer? • Is Cercopagis more freshwater organism than brackishwater? • Is Cercopagis more psychrophilic organism than thermophilic? • Are Cornigerius, Podonevadne more marine organisms than brackishwater?

  47. Let’s continue with evolution.

  48. From molecular biology point of view Cercopagis is also far away from Caspian Sea endemic onychopods.

  49. Arctic immigrants invasion route.May be via this route ancestors of Cercopagis came to the present native localities.

  50. The following evolution scenario was proposed by Mordukhai-Boltovskoi.Freshwater genera are in the left, marine – in the right, Caspian origin – in the middle.

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