Transcript Past and modern invasive stories of Onychopoda (Cladocera):

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 study
with 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
• 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.
• 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.
• Currently we would like to apply molecular markers to
study the modern invasions of Onychopoda:
Bythotrephes sp., Cercopagis sp., Cornigerius sp.,
Podonevadne sp. and Evadne anonyx.
• 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 Evadne anonyx are going to
invade Baltic Sea. There is some chance that these
species could be settled in the Baltic Sea and may go
further .
We would like to put some questions that
should be answered using new tools,
results and implications.
Let’s start from taxonomy.
Onychopoda consists of Podonidae,
Polyphemidae and Cercopagidae
Family: Cercopagidae Mordukhai-Boltovskoi, 1968
Genera: Cercopagis
Subgenera: Cercopagis
1.
2.
3.
4.
5.
6.
7.
8.
9.
Cercopagis (Cercopagis) neonilae Sars, 1902
Black, Azov and Caspian Seas, Gulf of Finland, Asko
Only females
C. (C.) socialis (Grimm, 1877)
Middle and Southern Caspian Sea, Gulf of Finland
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
С. (C.) prolongata Sars 1897
Middle and Southern Caspian Sea, Gulf of Finland
Only females
С. (C.) spinicaudata Mordukhai-Boltovskoi 1968
Middle Caspian Sea
С. (C.) longiventris Mordukhai-Boltovskoi, 1964
Middle Caspian Sea
Only females
С. (C.) robusta Sars, 1897
Middle and Southern Caspian Sea
Only females
С. (C.) micronyx Sars, 1897
Middle and Southern Caspian Sea, Gulf of Finland
С. (C.) anonyx Sars, 1897
Middle and Southern Caspian Sea.
Subgenera: Apagis
1.
2.
3.
4.
Cercopagis (Apagis) ossiani Mordukhai-Boltovskoi, 1968
Middle Caspian Sea (only once in 1913), Estonia
Only females
C. (A.) cylindrata Sars, 1897
Middle and Southern Caspian Sea, Gulf of Finland, Asko
Only females
C. (A.) beklemishevi Mordukhai-Boltovskoi, 1964
Middle Caspian Sea
Only females
C. (A.) longicaudata Sars, 1902
Middle Caspian Sea
Only females
The following structure of
genus Cercopagis was
proposed by MordukhaiBoltovskoi in 1968.
Polyphemoidea = Onychopoda
Rivier, 1998
Marine
Ponto-Caspian
Freshwater
Total
Species number
Podonidae
7
9
1
17
Polyphemidae
0
1
1
2
Cercopagidae
0
13
1
14
Family
Polyphemoidea = Onychopoda
Aladin et al., 1999
Marine
Ponto-Caspian
Freshwater
Total
Species number
Podonidae
7
6
1
14
Polyphemidae
0
0
1
1
Cercopagidae
0
4
1
5
Family
Polyphemoidea = Onychopoda
Aladin et al., 2000
Marine
Ponto-Caspian
Freshwater
Total
Species number
Podonidae
7
5–6
1
13–14
Polyphemidae
0
0
2–3
2–3
Cercopagidae
0
4–5
2–3
6–8
Family
Polyphemoidea = Onychopoda
Aladin et al., 2005
Marine
Ponto-Caspian
Freshwater
Total
Species number
Podonidae
7
5
1
13
Polyphemidae
0
0
1-2
1-2
Cercopagidae
0
3
1
4
Family
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, Cornigerius and Podonevadne are
living now in Northern America and Eurasia.
2. We need to check again weather we have only
one species: Bythotrephes longimanus as recent
molecular-biology studies showed us.
3. We need special taxonomic revision of the whole
Onychopoda group for better understanding of
all three families.
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 or
horns, 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.
2.
3.
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?
Let’s continue with ecology.
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
Dynamics of Cercopagis pengoi aralensis
8
7
Abundance, ind/m 3
6
5
4
3
2
1
0
1969
1970
1971
1972
1973
1974
1975
1976
1977
Year
In this lake Cercopagis never reached high abundances.
The same is true for Cercopagis from the Caspian Sea.
1978
1980
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 Internet
http://www.caspianenvironment.org/biodb/eng/zooplankton/Cercopagis%20pengoi/main.htm
the following information about feeding is given:
Feeding type. Heterotrophic
Feeding 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.
2.
3.
4.
5.
6.
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?
Let’s continue with physiology.
Cercopagis is fairly eurytherm crustacean.
Differences are not high regardless the origin of studied population.
Optimum (darkned) and tolerant (stippled) temperature ranges for parthenogenetic females of Cercopagis pengoi
Black & Azov Seas
Caspian Sea
Aral Sea
0
2
4
6
8
10
12
14
16
18
20
22
tem perature °C
24
26
28
30
32
34
36
38
40
Cercopagis is fairly eurytherm crustacean.
Differences are not high regardless the origin of studied population.
Optimum (darkned) and tolerant (stippled) temperature ranges for parthenogenetic females of Cercopagis pengoi
Baltic Sea (Finnish Gulf)
Sudochye Lake
0
2
4
6
8
10
12
14
16
18
20
22
tem perature °C
24
26
28
30
32
34
36
38
40
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.
Cercopagis is fairly euryhaline crustacean.
Differences are not high regardless the origin of studied population.
Optimum (darkned) and tolerant (stippled) salinity ranges for parthenogenetic females of Cercopagis pengoi
Black & Azov Seas
Caspian Sea
Aral Sea
0
2
4
6
8
10
salinity g/l
12
14
16
18
Cercopagis is fairly euryhaline crustacean.
Differences are not high regardless the origin of studied population.
Optimum (darkned) and tolerant (stippled) salinity ranges for parthenogenetic females of Cercopagis pengoi
Baltic Sea (Finnish Gulf)
Sudochye Lake
0
2
4
6
8
10
salinity g/l
12
14
16
18
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.
1. According to our studies and those of our colleagues from
Lancaster University Cornigeriis, Podonevadne and Evadne
anonyx are capable only to amphyosmotic regulation.
2. These organisms could be hypoosmotics in the range from
5-8 g/l up to 22-35 g/l.
3. Cornigeriis, Podonevadne and Evadne anonyx hemolymph
are hyperosmotics to surrounding water only in the range
from fresh water up to 5-8 g/l.
4. These organisms could invade the whole Baltic Sea and
even straits connecting it with the World Ocean. All
Podonidae are better osmoregulators than Cercopagidae.
5. From the point of view of osmotic regulation Cornigeriis,
Podonevadne and Evadne anonyx are very close to marine
organisms and are very far from freshwater Cercopagidae.
What physiology questions we
should answer?
1. Is Cercopagis more freshwater organism
than brackishwater?
2. Is Cercopagis more psychrophilic
organism than thermophilic?
3. Are Cornigerius, Podonevadne more
marine organisms than brackishwater?
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.
Barentz Sea
Kara Sea
Taimyr
Western drainage route
Northward
drainage outlets
Putorana
Mountains
S
ck
Bla
Verkhoyansk
Mountains
West Seberian Lowlands
ea
Pur / Mensi Lakes
d
oo
l
F
Aral Sea
s
te
u
ro
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?
4. Are Cornigerius and Podonevadne originated
from marine forms or from those that lived in
brackish water environment?
Some years ago Cornigerius sp., Podonevadne
sp., Evadne anonyx started invading Baltic Sea.
If they settled, we need to study this invasion
without mistakes that we did while studying
Cercopagis invasion.
This new exotic onychopod to our opinion is a
true Caspian Sea endemic organism. It has
amphiosmotic type of osmoregulation. It could
concur whole Baltic Sea and may be Baltic Sea
straits because Cornigerius sp., Podonevadne
sp., Evadne anonyx upper salinity limits are
higher than those of Cercopagis .
Thank you for your attention.
You may reach me with you
answers to my questions by
my e-mail: [email protected]
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.