by Yclcna KRASNOVA, Cand Sc. (Biol.), research assistant, N. Pertsov White Sea Biological Station, Lomonosov Moscow State University
A small settlement of scientists-the Biological Station of Lomonosov Moscow State University-is situated at the intersection of the Arctic Circle with the Karelian coast of the White Sea. Thousands of Russian scientists carried out their first serious research there in their undergraduate years and fell in love with the nature of the North forever. In 70 years of the Station's existence, young students and teachers have detected numerous living organisms, from bacteria to higher animals and plants. There are few areas with so an ample description of the biota in the world, while in Russia it is the only one.
AN EXAMPLE OF SURPRISING BIODIVERSITY
The founder of the White Sea Biological Station (WSBS) Academician Lev Zenkevich (1889-1970), a prominent Soviet oceanologist, head of the Chair of Invertebrate Zoology at the Biological Faculty of Lomonosov Moscow State University, and his col-leagues were sure that education should be realized through research. Thus, the expedition, sent in 1938 to find a place for a future station, had to choose an area with reach fauna on the coast. This task was fulfilled suc-cessfully, which is confirmed by a catalog of biota pub-lished in 2008. It presents more than 6,008 species described by students, teachers, and scientists in differ-ent years. The preparation of this publication started in the middle of the 1990s on the initiative of Natalya Kalyakina, Cand. Sc. (Biol.), with active participation of
Yekaterina Bubnova, Cand. Sc. (Biol.), and Alexei Chesunov, Dr. Sc. (Biol.). Their list included 46 species of bacteria, 104 cyanobacteria, 462 non-photo-synthe-sizing protozoa, 816 fungi and fungus-like organisms (including several classes of organisms called Myxo-mycetes), 168 lichens, 1,413 algae, 650 higher plants, 2,349 multi-cellular animals (including 823 insect species and 230 vertebrates). A total of 0.34 percent of the entire species diversity is focused on a small area of about 40 km2 in Karelia-just 0.0000078 percent of the surface of our planet!
From the very first days of the work of the Station, the students have been involved in studies of all kinds and they have become true hosts there. Together with their teachers they travel along the coastline, scrape the sea bottom by trawls, select specimens. The collected organisms are then identified at laboratories. Divers lift sacs with soil and rare specimens from the bottom. Thousands of papers have been published, numerous scientific works have been fulfilled, including hundreds of theses. The accumulated information on the organ-isms inhabiting the sea, the coastline, fresh water bodies and dry land, allows to broaden our notions on the nature of the White Sea territory.
Comparison of the WSBS biota with the fauna and flora of other northern territories and water areas has shown that the local organisms are described rather amply, particularly the algae and fungi. Our area is a leading one by the number of their species in the territo-ry of the former USSR. Data on vascular plants have been collected here. Of the 34 types of multicellular animals known to world science, 22 types are registered in this region. About 61 percent of fauna representatives of the entire White Sea are concentrated here in a small water area.
A total of 104 species unknown to science before have been revealed and described here over the years of the station's work. The majority of them are microscopic multicellular animals, belonging to the little studied category of marine meiofauna (organisms 0.1-2 mm in size): free nematodes (25 species) and crustaceans (23 species, mainly the Copepoda subclass, Harpacti-coida order). In addition, 17 infusoria species, 6 sunfish species*, 5 fungi (including fungus-like organisms), 5 Gregarinidea order (including some unicellular para-sites of invertebrates) and 4 Foraminifera** species, 4 Poly-chaeta (Polychaeta class worms) and 4 bacteria, 3 spe-cies of sea mollusks, 2 entoprocts (sea attached palp-like organisms), 2 green algae and 2 higher plants, 1 Kino-rhyncha phylum*** and 1 Rotifera phylum species have been found here.
The above-mentioned creatures include not only rep-resentatives of new genera and families, but also unusu-al living forms. For example, the enigmatic plankton crustaceans-Hansenocaris facetotects: only their larvae have been found, while their stage 2 remains unknown. Or nematodes parasitizing in Foraminifera order-a unique case when a multicellular organism lives inside a unicellular one. And almost every year brings new dis-coveries.
CONVENIENT LIFE STRATEGIES OF NEW SPECIES
In 1985, Alexander Tsetlin (now Dr. Sc. (Biol.), head-ing the Station since 2005), a specialist in sea annelids, discovered heretofore unknown parasites attached to the
* Sunfishes are a group of Protozoa, including several taxa of carniv-orous and omnivorous amoeboid organisms with a spherical body up to 1 mm in diameter and thread-like radial processes.-Auth.
** Foraminifera order are Protozoa from the Rhizaria suprataxon (pre-viously referred to as Rhizopoda). Their body is 0.1 -1 mm in size, rarely reaching 20 cm, enveloped in a calcareous shell built up from sand par-ticles.-Auth.
*** Kinorhyncha phylum are a class of Scalidophora worms (previously referred to as nemathelminths), 0.2-1 mm long, inhabiting the sea bot-tom at a depth of up to 400 m..-Auth.
Laonice Polychaeta. Their detailed study has shown that they are also Polychaeta, but of the Spionidae family. However, the attempts at their detailed characterization have failed, as these enigmatic creatures could not be found for a long time, and only in 2001, some of their specimens were again detected in the samples. The stu-dent Yelena Vortsepneva attentively examined their structure and concluded that they belonged to the Scolelepis genus of the above-mentioned Spionidae fam-ily. Electron microscopic studies of ultrathin (0.2 µm) sections have shown that the outer integument of the par-asite and host fuse completely and the vessels under the skin interweave like the mammalian placenta, in which nutritious substances are transferred directly through the capillary walls from mother to fetus. Presumably, the "attached" organism is really fed this way. However, it was unclear why this category included only males, while females were always "victims", and they were never seen one at a time. What if we deal with dwarf par-asitic males and not a species? This situation is extreme-ly rare among Polychaeta class worms.
The most reliable method for verification is DNA comparison. Molecular analysis has shown that the nucleotide sequences in the studied host and parasite genes are virtually identical. Presumably, the latter one is not a separate organism, but a product of maternal budding? (This phenomenon is known for some Polychaeta.) Additional studies allowed to reveal some slight differences in the DNA and hence, the first hypothesis was correct.
The White Sea waters with their Arctic cold all the year round-even in summer the water is not warmer than 0°C-do not easily reveal their secrets. In 2002, Alexei Chesunov, Dr. Sc. (Biol.), in collaboration with Pavel Kornev, postgraduate student (Moscow State University) and Pavel Rybnikov, Cand. Sc. (Biol.), from the P. Shirshov Institute of Oceanology examined the meiobenthos* from deep areas and revealed two species of tantulocarides, microscopic parasitic crayfish. Previously they have never been found in the White or other Russian seas, which is not accidental-they are too small! They parasitize on other tiny (1-2 mm) Harpacti-coida and Tanaidaceae crayfishes, being smaller than the host's pedicle at the moment of attachment.
These animals have a special larva (tantulus) for dis-persal and searching a new victim. Of all stages of the life cycle it best of all corresponds to the crayfish "life style", except its size (about 100 µm). Attached to the host, the microscopic creature changes its appearance, transforming into a saccule, and grows, though even adult species are rarely bigger than 0.5 mm. Its further development can be different. One way is transforma-tion into a parthenogenetic** individual, which needs no fertilization and lays eggs into a sack-like body. The other is formation of a male, retaining for some time its relationship with the old membrane through the thread (umbilicus). Then it separates and comes out from the saccule into the habitat. And, finally, the development of a female capable of sexual propagation. Then it also
* Meiobenthos are organisms 0.1-2 mm in size, living in the soil at the bottom of reservoirs.-Ed.
** Parthenogenesis is a form of sexual propagation of organisms, when female sex cells develop without fertilization.-Ed.
gets out from the saccule. In any event, creatures devel-oping from eggs of parthenogenetic individuals or from eggs received as a result of ovicell fusion with spermato-zoa are tantuluses searching for a victim in order to prick its integument with a stiletto, thrust the proboscis into the wound, and attach to the host by means of a viscous substance.
Grigory Kolbasov, Dr. Sc. (Biol.), in collaboration with Alexandra Savchenko, postgraduate student, examined peculiarities of the tantulocaride structure by means of an electron microscope. All scientists engaged in the problem at the biostation concluded that they had discovered a new species. One crayfish was called Micro-dajus tchesunovi (by the name of one of the discoverers), the other Arcticotantulus pertzovi, in honor of Nikolai Pertsov, who had been head of the Biological Station for 36 years.
WINTER AND SUMMER SURPRISES
The White Sea received its name as it is covered with ice from November till May, hiding its inhabitants from frosty winter air. Some representatives of the local fauna and flora find their shelter inside this saving "shell", in particular, there can actively develop algae. In addition, according to the data obtained by Kirill Sokolov, work-ing at the biostation, the ice above the litoral and shal-low water is populated by numerous animals from the bottom soil, while above deeper areas Chesunov found free-living annular worms Theristus melnikovi and Cryo-nema crassum, previously found only in a drifting ice zone at high Arctic latitudes, separated from the White Sea by about 1,000 km of the ocean. Together with Darya Portnova, a postgraduate student, the scientist described one more new species (Hieminema obliquo-rum), rather numerous near the biostation.
Nematodes (annular worms) as a rule populate narrow passages in the thickness of the substrate-capillary fis-sures between sand particles, cavities in plant tissues. It has been found that the porous lower surface of the ice is also a place fit for living. There is enough food for them: sunlight penetrating through this "shield" is sufficient for the development of microscopic algae, the base for an entire ecosystem, where is enough space for herbivo-
Crayfish changes its appearance after attaching to the host. Drawing, G. Kolbasov
rous organisms and carnivorous animals-in this case nematodes. It is surprising that these creatures are found in the area near the biological station only in winter and only in the ice. It remains unknown where and how they spend summer. It would be interesting to find out whether there is any link between populations of the White Sea and Arctic Ocean or perhaps the former are geographi-cally isolated. Can animals approximately 1 mm in size, without limbs or other means for swimming, cover dis-tances of thousands of kilometers?
In summer the small inhabitants of the bottom layer can really travel with sea currents. We have found places in the water area adjacent to our station, where bottom nematodes were often seen in the thickness of the water during the period when it was not covered with ice. In order to understand how they get there and what is in store for them in future, we have identified their species. We have found out that it is in fact a tragedy for worms, living only in litoral waters, to get far from the coast. The probability to "get back" with the current is almost zero. I happened to observe a catastrophic carrying out of litoral meiobenthos into the sea after a storm. Numerous harpacticide crayfishes, nematodes, shell crayfishes were found in water far from their habitat; forming a suspension of approximately the same density as that of shallow water zooplankton. It was the time of sumptu-ous food for coastal fishes. By the way, nematodes from sublitoral zones (rather numerous in the plankton) also get into a water medium from the soil, made easily muddy by fast streams.
Some species turned to be good swimmers, for exam-ple, small worms Desmodora communis, Timmia acuti-cauda, Draconema sp. (about 1 mm long), and the larvae of rather large worms Enoplus communis. Foreign scien-tists have noted the susceptibility of these creatures to travels in other seas as well. In other words, not all nematodes "prefer" the bottom life style. Observations of their mobility in a dish with sea water have shown that some species are capable of active and rapid move-ments by sharply bending and unbending the body. It cannot be ruled out that long sea voyages make no prob-lem to them.
"COMPETENT APEXES"
More than 30 hydroid polyps live near the biostation. Their diversity is most evident in the rapids between the continental coast and two small islands-Bolshoi and Maly Yeremeyevsky islets. Studies of these colonial ani-mals of Cnidaria type (this is how the Coelenterata are now called) are carried out by a team headed by Nikolai Marfenin, Dr. Sc. (Biol.), Professor of the Department of Invertebrate Zoology of the Biological Faculty of Mos-cow State University.
The colony of Coelenterata is in fact a "superorgan-ism" functioning in a different way in comparison with an ordinary animal. It is an intricate system of polyps,
Dynamena pumila hydroid shoot. Photo under the scanning electronic microscope, I. Kosevich
which have lost their independence and transformed into organs for procuring food, a kind of "mouths". Fragments of the colony with three obligatory compo-nents: a polyp (or a branch with several polyps), stolon rhizome (a system of food distribution), and growth apex-serve as a self-sufficient functional unit in hydroids. In contrast to plants, propagation of cells takes place not at the tip of the shoot, but at some distance from it. The cells in this area are rather active, due to which this area enlarges or "shrinks" every several minutes. The period of pulsations depends on animal species and environ-ment temperature. The colony is a little bit lengthened as a result of each such cycle.
The mechanism of action of the growth apex remained unknown up to recent time, though zoologists have found out long before that these semispherical points, outwardly very much alike, are responsible for the size and shape of colonies, whose diversity, with the configuration of individual shoots and peculiar location of individual zooids, is really amazing. But what makes these "competent apexes" so different? Primarily-the genome. But, scientists are interested in details.
Of all White Sea hydroids, several were selected as model objects: Dynamena pumila and three obelias (Gonothyraea (Obelia) loveni, O. geniculata, and O. longissima). The first of them is particularly interesting. Its shoot resembles a spike with pairs of "grains"- zooids, located one opposite the other along a common axis. As the shoot grows, the apex now works for length-ening, now for budding off side zooids, for which it has to ramify: the central part continues the shoot growth and two lateral ones give birth to feeder zooids. This moment attracted the attention of scientists: how do apical cells behave when three form from one?
It was previously assumed that this division takes place on account of the modified curvature of soft tissues: there emerge three protrusions, and each starts indepen-dent pulsation. Igor Kosevich, Head of the Laborato-ry of Animal Development Biology, Biological Faculty of Moscow State University, Cand. Sc. (Biol.), and
Alexander Fedosov, a postgraduate student, have thor-oughly studied this process by examining under an elec-tron microscope longitudinal and transverse sections of the apex at different stages of division. They have found out that the outer chitinous skeleton (perisarc), envelop-ing the entire surface of the colony, including the growth point, plays a very important role in this process. This envelope has only one pliable zone: fresh chitin at the apical tip. The abundance of shoot shapes is due to dif-ferent rate of its hardening. Chitin "limits" lengthening out in tiny places, where the process is more rapid, while in other places there can form protrusions. In addition, chitinous crests at the base of the growth apex also pro-mote separation of lateral buds, which in time become anastomoses between the stem and zooids.
This discovery clarified the direction of further search for mechanisms of colony formation. The substance responsible for perisarc hardening is to be found and the regulation of its secretion studied.
Here I have told you about just a small part of numer-ous studies, which were possible due to the Biological Station functioning all the year round by the White Sea. Thus, mycology has been actively developing in recent time, specifically, studies of the biological diversity and vital cycles of microscopic sea fungi-important compo-nents of biological turnover, responsible for utilization of organic substances. Olga Konovalova, a postgraduate student, is engaged in studies of specific features of White Sea brown algae, which can be described as "lichen the other way round", with the alga for the host and the fungal mycelium inside it. The specialists are impatiently waiting for results of these studies.
A Laboratory of Molecular Zoology has been recent-ly created by joint efforts of our scientist Tatyana Nereti-na and Nikolai Myuge, Cand. Sc. (Biol.), from the N. Koltsov Institute of Development Biology, Russian Academy of Sciences. This laboratory is an object of our special pride. It will become a place for realization of an International Project for Barcoding-creation of collec-tion of DNA sequences of White Sea residents. Using this peculiar code, it will be possible to identify the species of the sample and rapidly evaluate the biological diversity of an ecological system without consulting spe-cialists in classification.
At the end of 2009, the White Sea Biological Station was granted a status of a Research and Education Center. Now it is available not only for special, but also for interdisciplinary practices-for cooperation of stu-dents of different faculties. The "Sea Ecology" under-graduate training program will be soon launched here. By the way, specialists of this profile have never been trained at Moscow State University or any other institu-tion of higher education up to the present time. That is why the number of applications from scientists willing to work at the White Sea Biostation is increasing with every year.
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