Cercopagis: taxonomy, morphology, distribution, ecology, physiology

and evolution. Some questions that should be answered.

Aladin N.V. (Zoological Institute RAS)in co-operation with:

Chuikov Yu.S. (Environment Protection Agency of Astrakhan Region),Plotnikov I.S. (Zoological Institute RAS)

HELCOM-BSRP Meeting on Ballast Waters

Klaipeda-Palanga, February 22-24, 2005

Let’s start from taxonomy.

Onychopoda consists of Podonidae, Polyphemidae and Cercopagidae

Family: Cercopagidae Mordukhai-Boltovskoi, 1968 Genera: Cercopagis Subgenera: Cercopagis

1. Cercopagis (Cercopagis) neonilae Sars, 1902 Black, Azov and Caspian Seas, Gulf of Finland, Asko Only females

2. C. (C.) socialis (Grimm, 1877) Middle and Southern Caspian Sea, Gulf of Finland

3. С. (С.) pengoi (Ostroumov, 1891) Black, Azov and Caspian Seas; Danube, Dnepr and Bug Deltas; Gebedjinsk Lake in Bulgaria; Tsimlanskoe water-reserve on river Don and Kakhovskoe water-reserve on river Dnepr; Gulf of Finland, Asko, Middle and Southern Caspian Sea, Gulf of Finland Only females

4. С. (C.) prolongata Sars 1897 Middle and Southern Caspian Sea, Gulf of Finland Only females

5. С. (C.) spinicaudata Mordukhai-Boltovskoi 1968 Middle Caspian Sea

6. С. (C.) longiventris Mordukhai-Boltovskoi, 1964 Middle Caspian Sea Only females

7. С. (C.) robusta Sars, 1897 Middle and Southern Caspian Sea Only females

8. С. (C.) micronyx Sars, 1897 Middle and Southern Caspian Sea, Gulf of Finland

9. С. (C.) anonyx Sars, 1897 Middle and Southern Caspian Sea.

Subgenera: Apagis

1. Cercopagis (Apagis) ossiani Mordukhai-Boltovskoi, 1968 Middle Caspian Sea (only once in 1913), Estonia Only females

2. C. (A.) cylindrata Sars, 1897 Middle and Southern Caspian Sea, Gulf of Finland, Asko Only females

3. C. (A.) beklemishevi Mordukhai-Boltovskoi, 1964 Middle Caspian Sea Only females

4. C. (A.) longicaudata Sars, 1902 Middle Caspian Sea Only females

The following structure of genus Cercopagis was

proposed by Mordukhai-Boltovskoi in 1968.

Species number

Family

Mar

ine

Pon

to-C

aspi

an

Fre

shw

ater

Tot

al

Podonidae 7 9 1 17

Polyphemidae 0 1 1 2

Cercopagidae 0 13 1 14

Polyphemoidea = OnychopodaRivier, 1998

Species number

Family

Mar

ine

Pon

to-C

aspi

an

Fre

shw

ater

Tot

al

Podonidae 7 6 1 14

Polyphemidae 0 0 1 1

Cercopagidae 0 4 1 5

Polyphemoidea = OnychopodaAladin et al., 1999

Species number

Family

Mar

ine

Pon

to-C

aspi

an

Fre

shw

ater

Tot

al

Podonidae 7 5–6 1 13–14

Polyphemidae 0 0 2–3 2–3

Cercopagidae 0 4–5 2–3 6–8

Polyphemoidea = OnychopodaAladin et al., 2000

Species number

Family

Mar

ine

Pon

to-C

aspi

an

Fre

shw

ater

Tot

al

Podonidae 7 5 1 13

Polyphemidae 0 0 1-2 1-2

Cercopagidae 0 3 1 4

Polyphemoidea = OnychopodaAladin et al., 2005

3. C. (C.) neonilae Sars, 1902 ♀

1. C. (C.) socialis (Grimm, 1877) ♀ + ♂

2. C. (C.) pengoi (Ostroumov, 1891) ♀ + ♂

4. C. (C.) spinicaudata Mordukhai-Boltovskoi, 1968 ♀ + ♂

5. C. (A.) ossiani Mordukhai-Boltovskoi, 1968 ♀

1. C. (C.) micronyx Sars, 1897 ♀ + ♂

2. C. (C.) anonyx Sars, 1897 ♀ + ♂

3. C. (A.) beklemishevi Mordukhai-Boltovskoi, 1964 ♀

1. C. (C.) prolongata Sars, 1897 ♀

5. C. (C.) longiventris Mordukhai-Boltovskoi, 1964 ♀

2. C. (C.) robusta Sars, 1897 ♀

3. C. (A.) cylindrata Sars, 1897 ♀

4. C. (A.) longicaudata Sars, 1902 ♀

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.

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).

What taxonomy questions we should answer?

1. Using classical and molecular biology studies we should answer how many species of Cercopagis are living now in Northern America and Eurasia.

2. We need special taxonomic revision of the whole Onychopoda group for better understanding of Cercopagidae family.

Let’s continue with morphology.

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

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

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

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

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

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.

What morphology questions we should answer?

1. 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)?

2. Could some morphological structures (hooks, sharp end of brood pouch) save from predators?

3. Is there any connection between reproduction mode and availability of hook?

4. Which morphologycal parameters are enough stable to serve taxonomy and are good to be used in species identification keys?

Let’s continue with distribution.

Cercopagis native areas and invaded areas in Eurasia.

Cercopagis invaded areas in Northern America.

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.

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

What distribution questions we should answer?

1. 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?

2. 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?

3. At what stage from the life cycle Cercopagis is traveling around the world? Are it living organisms in ballast waters or resting eggs attached to fouling organisms outside the boat? Or both?

Let’s continue with ecology.

Dynamics of Cercopagis pengoi aralensis

0

1

2

3

4

5

6

7

8

1969 1970 1971 1972 1973 1974 1975 1976 1977 1978 1980

Year

Ab

un

dan

ce, i

nd

/m3

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.

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.

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

In Internethttp://www.caspianenvironment.org/biodb/eng/zooplankton/Cercopagis%20pengoi/main.htm the 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.

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.

What ecology questions we should answer?

1. We need to find an answer why in invaded areas abundance of Cercopagis is so high if compare with native one.

2. Is this happened due to some changes in Cercopagis physiology or behavior in new localities?

3. Is Cercopagis true carnivorous?4. Is Cercopagis omnivorous?5. Is Cercopagis without hook available only in the

beginning of life cycle shortly after hatching from resting eggs?

6. How it is possible to explain from ecological point of view that true predator Cercopagis is reaching abundance of several thousands individuals in m3?

Let’s continue with physiology.

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40

Aral Sea

Caspian Sea

Black & Azov Seas

temperature °C

Optimum (darkned) and tolerant (stippled) temperature ranges for parthenogenetic females of Cercopagis pengoi

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

0 2 4 6 8 10 12 14 16 18 20 22 24 26 28 30 32 34 36 38 40

Sudochye Lake

Baltic Sea (Finnish Gulf)

temperature °C

Optimum (darkned) and tolerant (stippled) temperature ranges for parthenogenetic females of Cercopagis pengoi

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

Due to good tolerance to low temperatures Cercopagis

parthenogenetic females could survive in Baltic Sea waters with

high thermal pollution.

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.

0 2 4 6 8 10 12 14 16 18

Aral Sea

Caspian Sea

Black & Azov Seas

salinity g/l

Optimum (darkned) and tolerant (stippled) salinity ranges for parthenogenetic females of Cercopagis pengoi

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

0 2 4 6 8 10 12 14 16 18

Sudochye Lake

Baltic Sea (Finnish Gulf)

salinity g/l

Optimum (darkned) and tolerant (stippled) salinity ranges for parthenogenetic females of Cercopagis pengoi

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

1. According to our studies and those of our colleagues from Lancaster University Cercopagis is capable only to hyperosmotic regulation.

2. This organism could be osmoconformer in the very short range from 5-8 g/l up to 17 g/l.

3. Cercopagis hemolymph is hyperosmotic to surrounding water only in the range from fresh water up to 5-8 g/l.

4. Cercopagis will never invade even the Baltic Sea straits connecting it with the World Ocean. Salinity is too high.

5. 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.

6. From the point of view of osmotic regulation Cercopagis is very close to freshwater organisms and is very far from marine and Caspian Podonidae.

What physiology questions we should answer?

1. Is Cercopagis more freshwater organism than brackishwater one?

2. Is Cercopagis more psychrophilic organism than thermophilic one?

Let’s continue with evolution.

From molecular biology point of view Cercopagis

is also far away from Caspian Sea endemic

onychopods.

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

localities.

Black S

ea

Aral Sea

Flood routes

West Seberian Lowlands

Pur / Mensi Lakes

Northwarddrainage outle ts

PutoranaMountains

VerkhoyanskMountains

Kara Sea

Taimyr

Barentz Sea

W estern dra inage route

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

Our opinion slightly differs from Mordukhai-Boltovskoi. Freshwater genera are in the left, marine – in the middle, Caspian origin – in the right.

What evolution questions we should answer?

1. Is Cercopagis originated from fresh water forms or from those that lived in marine or brackish water environment?

2. Is Cercopagis is true Ponto-Caspian endemic form?

3. When Cercopagis separated from Bythotrephes?

Thank you for your attention.

You may reach me with you answers to my questions by my e-mail: aral@zin.ru

On the next slide you may find a list of papers on Cercopagis and Onychopoda published by our team.

You may order papers presented in the list for free.

1. Khlebovich V.V., Aladin N.V., 1976. Hypotonic regulation in marine Cladocerans Evadne nordmanni and Podon leuckarti // J. Comp. Biochem. Physiol. 12: 591-592 (in Russian)

2. Aladin N.V., 1978b. Osmoregulatory abilities of marine Cladocera // Morphology, systematics and evolution of animals. P. 42-43. (in Russian)

3. Aladin N.V., 1979. On the forming of a latent egg in the White Sea Evadne nordmanni and Podon leuckarti (Cladocera, Podonidae) // Zool. J., 58(2). (in Russian)

4. Aladin N.V., 1979. Morpho-physiological adaptations of marine cladocerans. Autoref. of cand. Sc. theses. (in Russian)

5. Aladin N.V., 1982a. Salinity adaptations and osmoregulation abilities of the Cladocera. 1. Forms from open seas and oceans // Zool. J., 61(3): 341-351 (in Russian)

6. Aladin N.V., 1982b. Salinity adaptations and osmoregulation abilities of the Cladocera. 2. Forms from Caspian and Aral Seas // Zool. J., 61(4): 507-514 (in Russian)

7. Aladin N.V., 1982c. Salinity adaptations and osmoregulation abilities of the Cladocera. 2. Forms from brackish and fresh waters // Zool. J., 61(6): 851-860 (in Russian)

8. Aladin N.V., Andreev N.I. 1984. Influence of salinity of the Aral Sea on changes in composition of fauna of Cladocera // Hydrobiol. J. 20(3): 23-28 (in Russian)

9. Aladin N.V. 1990. General characteristic of the Aral Sea hydrobionts from the viewpoint of osmoregulation physiology // Proc. Zool. Inst. Acad. Sc. USSR, 223: 5-18 (in Russian)

10. Aladin N.V., 1991e. Salinity tolerance and morphology of the osmoregulation organs to Cladocera from Aral sea // Hydrobiologia, 225: 2291-299

11. Aladin N.V., 1995b. The conservation ecology of the Podonidae from the Caspian and Aral Seas // Hydrobiologia. Vol. 307. P. 85-97.

12. N. V. Aladin, V. Ryabova, Yu. S. Chuykov, I. S. Plotnikov. 1999. Problems of macro- and microevolution in superfamily Polyphemoidea=Onychopoda (Cladocera) Proceed. of Zool. Inst., 281. Pp. 97-100.

13. Aladin N.V., Rivier I.K., Chuykov Yu.S., Richter S., Ryabova V.N., Avinsky V.A., Plotnikov I.S. 1999. On invasion of representatives of genus Cercopagis (Cercopagidae, Polyphemoidea, Cladocera) in the Baltic Sea and Lake Ontario. In: Proc. of Annual Sci. Conf. Of St.Petersburg Univ., Febr. 1999. Pp. 17-19. (in Russian)

14. Aladin N.V., Richter S., Chuykov Yu.S., Plotnikov I.S. 1999. Problems of macro- and microevolution in superfamily Polyphemoidea (Cladocera). In: Annual scientific session of Zoological Institute RAS. (in Russian)

15. Aladin N.V., Gorokhova E.V., Chuykov Yu.S., Richter S., Ryabova V.N., Avinskiy V.A., Plotnikov I.S. 1999. To the problem of genus Cercopagis (Cercopagidae, Polyphemoidea, Cladocera) representatives invasion into the Baltic Sea and Lake Ontario. 16th Baltic Marine Biologists Symposium. June 21-26, 1999. Klaipeda, Lithuania.

16. Grigorovich I.A., Macisaac H.J., River I.K., Aladin N.V., Panov V.E. 2000. Comparative biology of the predatory cladoceran Cercopagis pengoi from Lake Ontario, Baltic Sea and Caspian Sea // Arch. Hydrobiol. Stuttgart, 149. pp.23-50.

17. Gorokhova E., Aladin N., Dumont H. 2000. Further expansion of the genus Cercopagis (Crustacea, Branchiopoda, Onychopoda) in the Baltic Sea, with notes on taxa present and their ecology // Hydrobiologia. Hydrobiologia, 429. Pp. 207-218.

18. Richter S., A. Braband, N. Aladin, G. Scholtz. 2001. The Phylogenetic Relationship of “Predatory Water-Fleas” (Cladocera: Ohychopoda, Haplopoda) Inferred from 12S rDNA. Molecular Phylogenetic and Evolution, 19(1). Pp. 105-113.