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The microcrustacean fauna (Cladocera, Copepoda and Ostracoda) of continental water bodies in the southern portion of Russian Far East is studied inadequately relative to the European Part of the country. The aim of the present study is to make inventory of the Cladocera and Copepoda fauna of the Lake Bolon basin and evaluate the biogeographic status of microcrustaceans found there. In toto, 45 taxa of Cladocera (of which four taxa could be identified only to genus) and 13 taxa of Copepoda are found. For some taxa we provide short morphological descriptions and comments on their distribution ranges in Northern Eurasia. We subdivided all taxa into five main faunistic complexes. In general, fauna of Cladocera and Copepoda of the Lake Bolon Basin is diverse and specific, it includes endemics of the Far East. In the investigated region cladocerans are more speciose and heterogeneous in their range types relative to the copepods. But most part of revealed cladoceran and copepod taxa belong to an artificial “complex” of species which are widely distributed in Eurasia (or even in Holarctic), or regarded as “cosmopolitan”. Each such taxon apparently needs an accurate taxonomic revision in the global scale keeping in mind Frey’s non-cosmopolitanism paradigm. Only newly obtained adequate data could provide a basis for biogeographical analysis of the Cladocera and Copepoda of the Far East fauna as a whole.
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© ARTHROPODA SELECTA, 2019
Arthropoda Selecta 28(1): 37–63
How to cite this article: Garibian P.G., Chertoprud
E.S., Sinev A.Yu., Korovchinsky N.M., Kotov A.A.
2019. Cladocera and Copepoda (Crustacea: Branchi-
opoda) of the Lake Bolon and its basin (Far East of
Russia) // Arthropoda Selecta. Vol.28. No.1. P.37–63.
doi: 10.15298/arthsel. 28.1.05
РЕЗЮМЕ. Фауна микроскопических ракообраз-
ных (Cladocera, Copepoda и Ostracoda) континен-
тальных водоемов юга Дальнего Востока Российс-
кой Федерации исследована несравнимо хуже, чем
фауна европейской части РФ. Цель данной работы
провести инвентаризацию фауны Cladocera и
Copepoda озера Болонь и его бассейна и оценить
биогеографический статус найденных видов. В об-
щей сложности нами было найдено 45 таксонов
Cladocera (среди них, определение четырех таксо-
нов было возможно только до уровня рода) и 13
таксонов Copepoda. Для некоторых таксонов при-
ведены морфологические описания и комментарии
по поводу их распространения в Северной Евра-
зии. Все найденные таконы отнесены к пяти основ-
ным фаунистическим комплексам. В общем, фауна
Cladocera и Copepoda Озера Болонь и его бассейна
разнообразна и специфична, она включает ряд эн-
демиков Дальнего Востока. Кладоцеры более раз-
нообразны в этом регионе, чем копеподы по видо-
вому составу и типу ареала. Однако большая часть
ABSTRACT. The microcrustacean fauna (Cla-
docera, Copepoda and Ostracoda) of continental water
bodies in the southern portion of Russian Far East is
studied inadequately relative to the European Part of
the country. The aim of the present study is to make
inventory of the Cladocera and Copepoda fauna of the
Lake Bolon basin and evaluate the biogeographic sta-
tus of microcrustaceans found there. In toto, 45 taxa of
Cladocera (of which four taxa could be identified only
to genus) and 13 taxa of Copepoda are found. For some
taxa we provide short morphological descriptions and
comments on their distribution ranges in Northern Eur-
asia. We subdivided all taxa into five main faunistic
complexes. In general, fauna of Cladocera and Copep-
oda of the Lake Bolon Basin is diverse and specific, it
includes endemics of the Far East. In the investigated
region cladocerans are more speciose and heteroge-
neous in their range types relative to the copepods. But
most part of revealed cladoceran and copepod taxa
belong to an artificial “complex” of species which are
widely distributed in Eurasia (or even in Holarctic), or
regarded as “cosmopolitan”. Each such taxon appar-
ently needs an accurate taxonomic revision in the glo-
bal scale keeping in mind Frey’s non-cosmopolitanism
paradigm. Only newly obtained adequate data could
provide a basis for biogeographical analysis of the
Cladocera and Copepoda of the Far East fauna as a
whole.
Cladocera and Copepoda (Crustacea: Branchiopoda) of the Lake
Bolon and its basin (Far East of Russia)
Cladocera è Copepoda (Crustacea) îçåðà Áîëîíü è åãî áàññåéíà
(Äàëüíèé Âîñòîê Ðîññèéñêîé Ôåäåðàöèè)
Petr G. Garibian1, Elena S. Chertoprud1,2, Artem Yu. Sinev1,3,
Nikolai M. Korovchinsky1, Alexey A. Kotov1*
Ï.Ã. Ãàðèáÿí1, Å.Ñ. ×åðòîïðóä1,2, À.Þ. Ñèíåâ1,3,
Í.Ì. Êîðîâ÷èíñêèé1, À.À. Êîòîâ1*
1 A.N. Severtsov Institute of Ecology and Evolution, Leninsky Prospect 33, Moscow 119071, Russia.
1 Институт проблем экологии и эволюции им. А.Н. Северцова РАН, Ленинский проспект, д. 33, Москва 119071, Россия.
2 Department of Hydrobiology, Biological Faculty, M.V. Lomonosov Moscow State University, Leninskie Gory, Moscow 119991, Russia.
2 Кафедра гидробиологии, Московский государственный университет им. М.В. Ломоносова, Ленинские горы, Москва 119991,
Россия.
3 Department of Invertebrate Zoology, Biological Faculty, M.V. Lomonosov Moscow State University, Leninskie Gory, Moscow 119991,
Russia.
3 Кафедра зоологии беспозвоночных, Московский государственный университет им. М.В. Ломоносова, Ленинские горы, Москва
119991, Россия.
*Corresponding author: alexey-a-kotov@yandex.ru
KEY WORDS: Crustacea, Cladocera, Copepoda, morphology, taxonomy, fauna, biodiversity.
КЛЮЧЕВЫЕ СЛОВА: Crustacea, Cladocera, Copepoda, морфология, систематика, фауна, биоразнооб-
разие.
38 P.G. Garibian et al.
ies of the Lower Amur River. It is located in Kha-
barovsk Territory of the Russian Federation on the
edge of the Amur River lowland [Grigoriev, 1964].
The water-surface area of the lake is 338 km² and the
average depth is 4 m. Its hydrological regime is regu-
lated by the run-off to the Amur River, connected with
the lake with two affluents [Nikonov, 1970]. The lake
has a floodplain valley origin and represents a remain-
der of a huge lake-river basin, located here in the
Lower Quaternary [Avarijaskin, 1970].
Until the last decade, data on the freshwater inver-
tebrates of the lake were scarce [Mikulich, 1948; Kh-
achina, 1948; Manuilova, 1964], although populations
of several taxa were studied in detail in special taxo-
nomic papers. Diaphanosoma dubium Manuilova, 1964
was described from Lake Bolon [Manuilova, 1964]
and then redescribed in detail [Korovchinsky, 2000].
Later, the material from the lake and its basin was used
for description of Leptodora richardi Korovchinsky,
2009 [Korovchinsky, 2009] and Diaphanosoma amu-
rensis Korovchinsky et Sheveleva, 2009 [Korovchin-
sky, Sheveleva, 2009]. A complex description of the
fauna of water invertebrates of the Bolonskiy State
Nature Reserve, partly covering the aquatiria of the
lake, has also been provided by Vshivkova & Nikitina
[2010]. Overall, to date only eight taxa of Cladocera
have been identified in the lake and its vicinities: Daph-
nia sp., Bosmina sp., Chydorus sp. [Mikulich, 1948],
Diaphanosoma dubium, D. amurensis, Leptodora ri-
chardi, Moina gouldeni Mirabdullaev, 1993 [Vshivko-
va, Nikitina, 2010], and Limnosida frontosa Sars, 1862
[Korovchinsky, 2014]. We do not find any identifica-
tions of the copepod species, except the subclass rank.
Thus, fauna of the planktonic crustaceans of the Lake
Bolon remains unknown despite its protected status
and the commercial fishing importance.
The aim of the present study is to make an invento-
ry of the Cladocera and Copepoda fauna of the Lake
Bolon basin and evaluate the biogeographic status of
the crustaceans found there.
Material and methods
Samples of zooplankton were collected in Septem-
ber 2007 in the vicinities of Djuen village, and in
August 2016 in the Bolonskiy State Natural Reserve.
The Djuen village is located on the north-western
shore of the Bolon Lake. Near it, a small river and
numerous drainage channels are located. Zooplankton
was collected from nine localities in Lake Bolon, its
oxbows and temporary water bodies in its basin (Fig. 1,
white squares).
Bolonskiy State Natural Reserve adjoins to Lake
Bolon from the south-west (Fig. 1, gray squares), it
occupies a territory between the Simmi and Harpi riv-
ers and includes wetlands with an area more than 100
thousand hectares. The floodplains of rivers are a bog-
gy plain covered with meadow vegetation or reed beds.
In rivers and river spills, the macrophytes are widely
кладоцер и копепод может быть отнесена к искус-
ственному «комплексу» видов, широко распрост-
раненных в Евразии (или даже в Голарктике), или
имеющих «космополитическое» распространение.
Каждый такой таксон должен быть подвергнут ак-
куратной таксономической ревизии в масштабе ми-
ровой фауны, принимая во внимание концепцию
«некосмополитизма» Дэвида Фрая. Именно такие
данные должны стать базисом для биогеографи-
ческого анализа Cladocera и Copepoda Дальнего
Востока и мировой фауны в целом.
Introduction
The microcrustacean fauna (Cladocera, Copepoda
and Ostracoda) of continental water bodies in the south-
ern part of the Russian Far East is studied inadequately
relative to the European part of the country [Kotov et
al., 2010], and even to more northern territories of the
Far East [Streletskaya, 1975a, b]. Efforts to study the
former were started from the largest water body, Lake
Khanka [Rylov, 1933]. Its fauna remains the most ex-
plored among all water bodies of this region; the num-
ber of publications on it keeps steadily growing [Uéno,
1939, 1940; Markovtsev, 1979; Barabanshchikov,
Kojevnikov, 1998; Barabanshchikov, 2000, 2004, etc.].
A series of large expeditions was organized to the
Amur basin in the 1930’s–1940’s [Rylov, 1933]. As a
result, the fishes of this region were intensively studied
[Berg, 1948; Nikolsky, 1956], but special studies of
the plankton began only in the second half of the 20th
century. They were focused mainly on large lakes and
basins of few large rivers [Borutsky, 1952a; Manujlo-
va, 1964; Borutsky et al., 1991], mainly the Amur (=
Hellong Jiang) River and its large affluent, the Ussuri
River [Mikulich, 1948; Barabanshchikov, 2014].
Many examples of the Far Eastern fauna specificity
were obtained to date, e.g. a series of specific East
Asian taxa of species and subspecies rank was found
there [Ueno, 1940; Borutsky, 1952a; Frey, 1973;
Borutsky et al., 1991; Korovchinsky, 2000, 2009; Ko-
tov et al., 2006; Korovchiunsky, 2009; Korovchinsky,
Sheveleva, 2009; Smirnov, Sheveleva, 2010]. This fact
stresses the relevance of faunistic and taxonomic in-
vestigations on the Far Eastern planktonic crustaceans.
However, at present, only few territories of this large
region are studied more or less satisfactorily, the exist-
ing literature is fragmentary and any publications on
some large territories are almost (or totally) absent.
The significance of such studies was demonstrated in a
series of publications on the Zeya River basin [Kotov
et al., 2011a, b; Kotov, Sinev, 2011]. The existence of
a specific Far Eastern endemic complex of cladocerans
was demonstrated in these papers, as well as the fact of
penetration of some thermophylous species from south-
ern regions to this basin.
One of the unexplored water bodies of the Far East,
with only scarce data on planktonic crustaceans, is
Lake Bolon. This lake is one of the largest water bod-
39
Cladocera and Copepoda of Lake Bolon
Fig. 1. Map of the region and photos of some localities. A — position of the region in Eastern Eurasia; B — map of region with
sampling stations in September 2007 (white squares) and August 2016 (gray squares); C — pelagic zone of Lake Bolon (Locality 2); D —
its littoral zone (Locality 4); E — Kipru channel, near Kordon Kipru (Locality 10). The base map for A is the Marble Virtual Globe 1.5.1
“plain map” (i.e., no attributable data layers) available at https://marble.kde.org/. Photo D by A.A. Kotov, C and E — courtesy by M.
Roshchin (published with his permission).
Рис. 1. Карта региона и фотографии некоторых водоемов. A — положение региона в Восточной Евразии; B — карта региона с
отмеченными точками пробоотбора в сентябре 2007 г. (белые квадраты) и августе 2016 г. (серые квадраты); C — пелагиаль озера
Болонь (точка 2); D — его литораль (местообитание 4); E — Канал Кипру около кордона Кипру (точка 10). Изначальная карта для
фрагмента A взята с портала Marble Virtual Globe 1.5.1 “plain map” и доступна по адресу https://marble.kde.org/. Фото D сделано
А.А. Котовым, C и E — М. Рощиным (публикуется с его разрешения).
represented; thickets sometimes occupy more than half
the area of the waterway. The most numerous macro-
phytes are the water nut (Trapa natans L.), the floating
heart (Nymphoides peltata (S.G. Gmel.) Kuntze), the
spatterdock (Nuphar sp.) and the pondgrass (Potamo-
geton natans L.). Zooplankton in this area was collect-
ed at 11 stations in the Simmi, Sel’gon, Harpi and
Kirpu rivers, and also in the Albite Lake. At each
station three replicate samples were collected by haul-
ing a plankton net (diameter 0.1 m, 50 µm mesh) verti-
cally through the water column, engaging the upper
layer of the bottom with the detached sediment filtered
through the net up to the surface. Sampling was per-
formed both from the shore and from the boat that
enabled reaching the pelagic zone of the water bodies.
The location of sampling stations is shown on Figure 1
and in Table 1.
All samples were preserved with 96% ethanol. All
samples were provisionally investigated under stereo-
scopic and compound microscopes using standard tech-
niques [Kotov, 2013]. General morphology of all found
individuals was studied in toto under an Olympus BX41
40 P.G. Garibian et al.
Table 1. Sampling localities in the Bolon Lake basin in 2007 and 2013.
Таблица 1. Список местообитаний в бассейне Озера Болонь, откуда были взяты пробы в 2007 и 2013 годах.
No. Water body N,° E,°
1. Littoral of Lake Bolon near Dzhuen 49.85061 136.2652
2. Lake Bolon' about 300 m from the shore (pelagic and vegetation) 49.8442 136.2761
3. A small puddle near Lake Bolon 49.85353 136.2678
4. Littoral of Lake Bolon with numerous hillocks 49.85242 136.2674
5. An affluent of River Sjumnjur (right bank), near railway station Bolon 49.89845 136.1425
6. A puddle, right bank of River Sjumnjur, near railway station Bolon 49.89836 136.1427
7. A puddle, leaf bank of River Sjumnjur, near railway station Bolon 49.8968 136.1452
8. A puddle near a stream, railway station Bolon 49.89786 136.1351
9. A ditch with vegetation, railway station Bolon 49.8981 136.1381
10. Kipru channel, near Kordon Kipru 49.50653 136.0273
11. River Simmy near Kordon Vakhtar 49.41304 135.8447
12. River Simmy near mouth of Normen River 49.43823 135.9643
13. River Simmy at Cheremshiniy Kordon 49.59206 136.1261
14. River Selgon near Kordon Shelkovoy Griady 49.59386 135.9275
15. River Selgon, Nymphaea patches 49.58988 135.9659
16. River Se'lgon, a backward 49.58374 136.0273
17. Ersun channel near Kordon Kiltasin 49.70731 136.283
18. River Kharpy, 15 km from its mouth 49.72874 136.1149
19. Lake Albite 49.67973 136.1936
20. River Kipru, 4 km from Kordon Kipru 49.50686 136.0455
compound microscope. Then some individuals were
dissected using tungsten needles electrolytically sharp-
ened in 10% NaOH [Frey, 1986]. Each dissected body
part was transferred individually by aforementioned
needles to a new drop of glycerol on a separate slide,
covered by a cover slip and investigated in detail under
an immersion lens at magnification x 100. Drawings
were prepared with a drawing tube attached to the light
microscope Olympus BX 41 or Olympus CX 41. Mor-
phological terminology is applied to Cladocera accord-
ing to Kotov [2013].
We used the computer package EstimateS [Col-
well, 2013] to estimate species richness of the Cla-
docerans in the region. Also a basic graph was made
with the portion of water bodies where each taxon is
recorded.
Results
A. General
Totally, 45 taxa of Cladocera are recorded, but four
taxa were identified only to the genus level. Exact
identification was not possible when the samples con-
tained juvenile specimens only. In the case of Diapha-
nosoma sp., few samples contained juvenile D. brachi-
urum-like females which, most probably, belong to D.
amurensis. These two taxa could not be discriminated
based on female morphology [Korovchinsky, 2018],
and we prefer to avoid exact species identification.
Thirteen taxa of Copepoda are identified, many sam-
ples contained only copepodites, the species identifica-
tion of which was impossible. Some remarkable taxa
are discussed below.
B. Taxonomic account on selected species
Superorder Cladocera Latreille, 1829
Order Ctenopoda Sars, 1865
Family Sididae Baird, 1850
Sida crystallina (O.F. Müller, 1776)
Fig. 2A–E.
Parthenogenetic female. Body ovoid, head small
with a large anterior and a pair of smaller anchoring
organs (Fig. 2A, B) dorsally, dorsal margin convex, its
postero-dorsal angle expressed, posterion margin
straight, postero-ventral margin expressed, bearing a
spine. Rostrum relatively long and either straight or
slightly curved, directed ventrally, compound eye large,
situated near ventral head margin, ocellus very small
(Fig. 2B, C). Postabdomen trapezium-shaped, its ven-
tral margin straight, proximal portion of dorsal side of
postabdomen weakly prominent (Fig. 2E). Row of 14-
16 anal teeth along each lateral side noticeably curved,
rows of minute spinules near these teeth. Postabdomi-
41
Cladocera and Copepoda of Lake Bolon
Fig. 2. Parthenogenetic females of Sida crystallina from Kipru channel, near Kordon Kipru, locality 10 (A–E) and S. ortiva from River
Simmy at Cheremshiniy Kordon, locality 13 (F–G). A — lateral view; B–C — head; D–E — postabdomen and postabdominal claw; F —
head; G — distal portion of postabdomen. Scale bars: 0.1 mm.
Рис. 2. Партеногенетическая самка Sida crystallina из протоки Кипру около кордона Кипру, точки 10 (A–E) и S. ortiva из Реки
Симми около Черемшиного кордона, точки 13 (F–G). A — вид сбоку; B–C — голова; D–E — постабдомен и постабдоминальный
коготок; F — голова; G — дистальная часть постабдомена. Масштабная линейка: 0,1 мм.
nal claw regularly bent, with four basal spines, proxi-
malmost spine small and situated closely to the neigh-
boring one (Fig. 2E). Postabdominal setae long, about
0.4 of body length, located on a strong projection. An-
tenna I long, with distal aesthetascs and distal sensory
seta longer than the former (Fig. 2B). Antenna II long,
its basal segment long, with some spines distally (Fig.
2A). Formula of antennal setae: 0-4-7/0-1-4. Six pairs of
thoracic limbs of typical structure for S. crystallina (see
Korovchinsky [2004]. Body size range 1.7–4.0 mm.
Comments. See comments on the following spe-
cies.
Sida ortiva Korovchinsky, 1979
Fig. 2F–G.
Parthenogenetic female. Body structure similar to
that of S. crystallina. Rostrum relatively short, directed
ventrally and curved, compound eye large, situated
near ventral head margin, ocellus very small (Fig. 2F).
Postabdomen trapezium-shaped, dorsum of postabdo-
men with weakly prominent proximal part. Row of 12–
14 anal teeth along each lateral side noticeably curved,
rows of minute spinules near these teeth. Postabdomi-
nal claw regularly bent, with four basal spines, proxi-
42 P.G. Garibian et al.
malmost spine is relatively large, almost of the same
size as the neighboring one (Fig. 2G). Postabdominal
setae long, about 0.4 of body length, located on a
strong projection. Antenna I long, with distal aesthetascs
and distal sensory seta longer than the former ones
(Fig. 2F). Other structures as in previous species. Body
size 1.5–3.0 mm.
Comments. Korovchinsky [1979] suggested that
two subspecies exist in northern Eurasia: S. cystallina
crystallina (O.F. Müller, 1776) and S. crystallina orti-
va Korovchinsky, 1979. Now they are regarded as
separate species due to high genetic differences and
wide range overlapping [Kotov et al., 2011a; Ko-
rovchinsky, 2018]. S. crystallina differs from S. ortiva
in (1) longer rostrum projected posteriorly and (2)
conspicuously smaller proximalmost basal spine on
postabdominal claws located closely to the neighbor-
ing one. In the Amur River basin both taxa are present
[Kotov et al., 2011a]. In few localities in Lake Bolon
basin, both species are found to co-occur.
Order Anomopoda Sars, 1865
Family Chydoridae Dybowski et Grochowski, 1894
emend. Frey 1967
Subfamily Aloninae Dybowski et Grochowski, 1894
emend. Frey, 1967
Acroperus harpae Baird, 1834
Fig. 3.
Parthenogenetic female. Body low oval, elongat-
ed in lateral view (Fig. 3A). Having a well-expressed
dorsal keel with variable shape with out separation on
carapace and head. Dorsal margin which moderately
convex, evenly arched from the tip of rostrum to the
postero-dorsal angle that rounded, posterior margin
weakly to moderately concave, postero-ventral angles
broadly rounded. Ventral margin relatively convex and
armed with 39 setae (Fig. 3C). Rostrum truncated,
pointed downward and oval (Fig. 3A, B). Head pores
as for Chydoridae, three connected head pores and two
minute lateral pores. Labrum relativity small, with sub-
triangular keel, without setules on apex (Fig. 3B). The
row of setae covers all margin, they are different size in
certain sections (Fig. 3A, C). Postabdomen long and
narrowing, with parallel margin or slightly narrowing
distally, its length about 4X height (Fig. 3H). Preanal
portion convex, preanal angle faintly defined, anal mar-
gin almost straight, postanal angle not defined, posta-
nal margin almost straight; postanal portion not much
longer than anal one. Postanal and anal margin with
groups of minute denticles (Fig. 3H, I). Laterally 13
series of fascicles of long setules. The base of postab-
dominal claw carries a cluster of long setules. Postab-
dominal claw long, straight, with slightly curved tip.
Basal spine long, straight and thin, about 0.18 length of
claw, bearing 5 setules. At the middle of the claw is a
prominent spine. (Fig. 3I).
Antenna I long and narrow (its length about 4X
width), with three groups of fine setules at anterior
face; among nine aesthetascs two longer than the rest,
longest aesthetascs longer than antenna I; antennular
seta thin and long, about 1/2 length of antenna I, pro-
truding somewhat 1/3 to distal (Fig. 3F). Antenna II
relativity long, antennal formula: setae 0-0-3/0-1-3,
spines 1-0-1/0-0-1. Apical setae differentiated in size,
apical spines about 1/3 length of apical segments, spine
on proximal exopod segment about 1/2 of length itself
(Fig. 3G). Limb I with ODL bearing a long seta, armed
with short setules distally; IDL with three setae, seta 2
and 3 large, 2-segmented, a little shorter than ODL
seta; (Fig. 3J). Size in our material 0.72 mm.
Comments. See comments on the following taxon.
6. Acroperus angustatus Sars, 1863
Fig. 4.
Parthenogenetic female. Body shape variable,
mostly suboval and elongated in lateral view (Fig. 4A).
Having a well-expressed dorsal keel as in previous
species with variable shape. Dorsal margin weakly con-
vex, in some specimens with discernible separation.
Postero-dorsal angle weakly identified, posterior mar-
gin relatively concave, postero-ventral angles broadly
rounded with 1–3 saw-like denticles Fig. 4D). Ventral
margin convex and armed with 44 different size setae
(Fig. 4C). Rostrum truncated, pointed downward and
oval (Fig. 4A, B). Head pores and labrum as in previ-
ous species (Fig. 4B). Postabdomen same as for previ-
ous species. Antenna I most as for previous species
except longest terminal aesthetasc which is relatively
longer (Fig. 4F). Antenna II shorter than previous,
antennal formula: setae 0-0-3/0-1-3, spines 1-0-1/0-0-
1. All apical setae relatively similar in size, apical
spines same as for previous (Fig. 4G). Limb I with
ODL bearing a long seta, armed with short setules
distally; IDL with three setae, seta 3 long as ODL and 2
shorter than 3; (Fig. 4J). Size in our material 0.65 mm.
Comments. Sinev [2009] demonstrated that two
aforementioned taxa are morphologically close, and
both are widely distributed in Northern Eurasia from
Europe to Far East. We confirm that both taxa are
common in the Lake Bolon basin.
3. Camptocercus uncinatus Smirnov, 1971
Fig. 5.
Parthenogenetic female. Body ovoid, elongated
in lateral view (Fig. 5A); strongly compressed laterally
and having a well-expressed dorsal keel both on cara-
pace and head. Dorsal margin without depression be-
tween valves and head shield, postero-dorsal angle
broadly rounded, posterior margin convex, postero-
ventral angles broadly rounded. Ventral margin slight-
ly undulated. Rostrum acute, pointed downward (Fig.
5A, B). Three connected main head pores, lateral pores
minute. Labrum with a sub-triangular keel; its posterior
margin without a denticle, with two groups of fine
setules (Fig. 5B). Row of ventral setae followed by a
row of fine setules, in dorsal portion of posterior mar-
43
Cladocera and Copepoda of Lake Bolon
Fig. 3. Parthenogenetic female of Acroperus harpae from an affluent of River Sjumnjur (right bank), near railway station of Bolon,
locality 5. A — general view; B — head; C — valve; D–E — armature of postero-ventral angle; F — postabdomen; G — its distal portion;
H — antenna I; I — antenna II; J — limb I. Scale bars: 0.1 mm.
Рис. 3. Партеногенетическая самка Acroperus harpae из заводи на правом берегу речки Сюмнюр у станции Болонь, точки 5. A —
общий вид; B — голова; C — створка; D–E — вооружение заднебрюшной части створки; F — постабдомен; G — его дистальная
часть; H — антенна I; I — антенна II; J — торакопод I. Масштабная линейка: 0,1 мм.
gin they are strong, denticle-like (Fig. 5C–D). Postab-
domen very long, narrowing distally, length about 5–
6X height (Fig. 5H). Preanal portion almost straight,
preanal angle well-developed, anal margin almost
straight, postanal angle not expressed, postanal margin
straight to slightly concave; postanal portion 3–4 times
longer than anal one. Postanal margin with about 19
clustered postanal denticles with fused bases (Fig. 5H).
44 P.G. Garibian et al.
Fig. 4. Parthenogenetic female of Acroperus angustatus from River Simmy near mouth of Normen River, locality 12. A — general
view; B — head; C — valve; D — armature of postero-ventral angle; E — postabdomen; F — its distal portion; G — antenna I; H —
antenna II; I — limb I; J — its inner-distal lobe. Scale bars: 0.1 mm.
Рис. 4. Партеногенетическая самка Acroperus angustatus из Реки Симми около устья реки Нормен, точки 12. A — общий вид;
B — голова; C — створка; D — вооружение заднебрюшного края створки; E — постабдомен; F — его дистальная часть; G —
антенна I; H — антенна II; I — торакопод I; J — его внутренняя дистальная доля. Масштабная линейка: 0,1 мм.
45
Cladocera and Copepoda of Lake Bolon
Fig. 5. Parthenogenetic female of Camptocercus uncinatus from Lake Albite, locality 19. A — general view; B — head; C — valve; D —
armature of ventral margin; E — armature of postero-ventral valve portion; F — postabdomen; G — its distal portion; H — antenna I; I —
antenna II; J — limb I; K — inner-distal lobe. Scale bars: 0.1 mm.
Рис. 5. Партеногенетическая самка Camptocercus uncinatus из Озера Альбите, точки 19. A — общий вид; B — голова; C —
створка; D — вооружение брюшного края; E — вооружение заднебрюшного края; F — постабдомен; G — его дистальная часть; H —
антенна I; I — антенна II; J — торакопод I; K — его внутренняя дистальная доля. Масштабная линейка: 0,1 мм.
46 P.G. Garibian et al.
Laterally series of fine setules. Postabdominal claw
long, straight, with slightly curved tip; basal spine short,
slightly bent, about 0.16 length of claw; few setules at
the end of proximal pecten as strong spines (Fig. 5H,
I). Antenna I with length about 3–4 width, with three
groups of fine setules at anterior face; among nine
aesthetascs two longer than the rest, longest aesthetascs
as long as antenna I; antennular seta thin, about 1/5
length of antenna I, protruding somewhat distally to
middle (Fig. 5F). Antenna II short, antennal formula:
setae 0-0-3/0-1-3, spines 1-0-1/0-0-1. Apical setae sub-
equal in size, apical spines very short, spine on proxi-
mal exopod segment also very short (Fig. 5G). Limb I
with ODL bearing a long seta, armed with long setules;
IDL with three setae, seta 1 large, well developed,
about 1/3 length of ODL seta; setae 2 and 3 thick,
curved, hook-like, with a short, setulated distal portion
(Fig. 5J-K). Size in our material 0.73–0.75 mm.
Comments. Earlier Kotov et al. [2012] concluded
that there are two close species in Korea: C. uncinatus
Smirnov, 1971 (widely distributed in East Asia) and C.
vietnamensis Than, 1980 (thermophylous taxon with a
predominantly tropical-subtropical distribution, pene-
trating North up to Korean Peninsula). We did not fond
the latter in the Bolon region, while C. uncinatus is a
usual taxon there, while the northernmost limit of C.
vietnamensis distribution is located in the Korean Pen-
insula.
4. Camptocercus lilljeborgi Smirnov, 1971
Fig. 6.
Parthenogenetic female. Body low oval, elongat-
ed in lateral view (Fig. 6A); strongly compressed later-
ally and having a well-expressed dorsal keel both on
carapace and head. Dorsal margin evenly arched from
the tip of rostrum to the postero-dorsal angle, which is
broadly rounded, posterior margin convex, postero-
ventral angles very broadly rounded. Ventral margin
slightly undulate and armed with 61 setae. Rostrum
truncated, pointed downward (Fig. 6A, B). Head pores
as for genus. Labrum relativity wide, with two or four
groups of fine setules (Fig. 6B). The row of setae reach
2/3 length of margin, in that portion of posterior mar-
gin they are strong, denticle-like (Fig. 6C–D). Postab-
domen very long, narrowing distally, length about 7X
height (Fig. 6H). Preanal portion almost straight, prea-
nal angle well-developed, anal margin almost straight,
postanal angle not expressed, postanal margin almost
straight ; postanal portion 4 times longer than anal one.
Postanal margin with about 20 clustered postanal den-
ticles with fused bases (Fig. 6H). Laterally a series of
fine setules. Postabdominal claw long, straight, with
slightly curved tip; basal spine short, slightly bent,
about 0.17X length of claw; few setules at the end of
proximal pecten as strong spines (Fig. 6I). Antenna I
with length about 3–4X width, with three groups of
fine setules at anterior face; among nine aesthetascs
two longer than the rest, longest aesthetascs as long as
antenna I; antennular seta thin, about 1/5 length of
antenna I, protruding somewhat distally to middle (Fig.
6F). Antenna II short, antennal formula: setae 0-0-3/0-
1-3, spines 1-0-1/0-0-1. Apical setae subequal in size,
apical spines very short, spine on proximal exopod
segment also very short (Fig. 6G). Limb I with ODL
bearing a long seta, armed with long setules; IDL with
three setae, seta 1 large, well developed, about 1/3
length of ODL seta; setae 2 and 3 thick, curved, hook-
like, with a short, setulated distal portion (Fig. 6J–K).
Size in our material 0.73–0.75 mm.
Comments. C. lilljeborgi is regarded to be a rare
Palearctic species [Smirnov, 1971]. To date it was
recorded from North and Central Europe (Germany,
Romania, Slovenia, Sweden and Northern part of Eu-
ropean Russia [Smirnov, 1998; Hudec, 2010]) and
North-East Asia (several localities in Yakutia and
Chukotka Peninsula [Streletskaya, 2010; Sinev, 2014;
Kotov, 2016]. In this paper, this taxon is reported from
the Amur basin for the first time. Our population is the
southernmost Asian one to date, separated by about
1000 km from the closest known Asian population (Cen-
tral Yakutia). Sinev [2014] suggested that although this
species is widely distributed throughout Northern Eur-
asia it was overlooked by researchers due to its rarity.
7. Kurzia latissima Kurz, 1875
Fig. 7.
Parthenogenetic female. Body ovoid, high in lat-
eral view, dorsal margin regularly curved from tip of
rostrum to slightly expressed postero-dorsal angle, pos-
terior margin convex, postero-ventral angle rounded,
ventral margin with a prominence anteriorly to middle
(Fig. 7A). Body compressed laterally, with a medial
keel on carapace, but not on head. Rostrum relatively
short, ocellus about half size of compound eye (Fig.
7B). Three major head pores connected, posterior pore
transversely elongated, lateral pores minute. Labrum
with large, triangular labral keel, anterior margin, its
apex with round tip (Fig. 7B). Setules on posterior
margin different in size (Fig. 7C–D). Postabdomen
distally elongated, with concave postanal margin; dor-
so-distal angle of postabdomen recognized; postanal
teeth about 11 (Fig. 7C). Postabdominal claw long,
slightly curved, with a single long basal spine (as long
as two claw widths), bearing a series of 5–6 thin spinules
(Fig. 7G–H). Antenna I elongated, sensory seta in prox-
imal part, nine aesthetascs of unequal size, three long-
est ones almost reach tip of rostrum (Fig. 7E). Antenna
II short, antennal formula: setae 0-0-3/1-1-3, spines 1-
0-1/0-0-1(Fig. 7F). Limb I with ODL bearing a single
bisegmented seta, setulated distally (Fig. 7I), IDL with
three setae, distal portion with a row of setules decreas-
ing to tip (Fig. 7D–E). Size in our material 0.57 mm.
Comments. K. latissima is described from the Lake
Bolon area for the first time. This taxon is common in
the Lake Khanka area (Kotov, unpublished) as well as
from China [Chiang, Du, 1979].
47
Cladocera and Copepoda of Lake Bolon
Fig. 6. Parthenogenetic female of Camptocercus lilljeborgi from Lake Albite, locality 13. A — general view; B — head; C — valve; D —
armature of ventral margin; E — armature of postero-ventral valve portion; F — postabdomen; G — its distal portion; H — antenna I; I —
antenna II; J — limb I; K — its distal portion. Scale bars: 0.1 mm.
Рис. 6. Партеногенетическая самка Camptocercus lilljeborgi из озера Альбите, точки 19. A — общий вид; B — голова; C —
створка; D — вооружение брюшного края; E — вооружение заднебрюшной части створки; F — постабдомен; G — его дистальная
часть; H — антенна I; I — антенна II; J — торакопод I; K — его дистальная часть. Масштабная линейка: 0,1 мм.
48 P.G. Garibian et al.
Fig. 7. Parthenogenetic female of Kurzia latissima from River Simmy near Kordon Vakhtar, locality 11. A — general view; B — head;
C–D — armature of postero-ventral valve portion; E — postabdomen; F — its distal portion; G — antenna I; H — antenna II; I — limb I.
Scale bars: 0.1 mm.
Рис. 7. Партеногенетическая самка Kurzia latissima из реки Симми рядом с кордоном Вахтар, точки 11. A — общий вид; B —
голова; C–D — вооружение заднебрюшной части створки; E — постабдомен; F — его дистальная часть; G — антенна I; H —
антенна II; I — торакопод I. Масштабная линейка: 0,1 мм.
49
Cladocera and Copepoda of Lake Bolon
Alona cf. affinis (Leydig, 1860)
Figs. 8–9.
Parthenogenetic female. In lateral view, body oval
(Fig. 8A), of moderate height, moderately compressed
laterally. Maximum height at the middle of the body. In
adults height/length ratio about 0.6. Dorsal margin of
valves convex; postero-dorsal and postero-ventral an-
gles broadly rounded. Posterior margin convex. Ante-
ro-ventral angle rounded. Ventral margin (Fig. 8B)
weakly convex to straight, with 70–85 setae. About 25
anteriormost setae very long, next 10 seta short, poste-
rior 40 setae of moderate length, decreasing in length
posteriorly. Postero-dorsal angle (Fig. 8C–E) with 1–4
denticles closely spaced denticles of variable shape, at
least one - with broad base, and one-two group of short
setules of similar length and thickness, with 3-5 setules
in each. A row of about 100 setules of variable length
along posterior margin on inner side of carapace, these
setules not organized into groups. Carapace ornamen-
tation as weakly developed longitudinal lines and dense
longitudinal striae between them. Head relatively small,
low triangle-rounded in lateral view. In lateral view
rostrum relatively narrow, protruding downwards. Ocel-
lus of moderate size, eye larger than ocellus. Distance
from tip of rostrum to ocellus 1.5–2 times greater than
that between ocellus and eye. Head shield (Fig. 8F)
with maximum width behind mandibular articulation,
covered by fine striae as on the valves. Rostrum short
and rounded. Posterior margin as prominent, acute dis-
tal angle. Two major head pores (Fig. 8G) of same
size, with a narrow connection between them. PP slightly
less than 2 IP in adults. Lateral head pores located in
small depressions more than 1 IP distance from mid-
line, at level before anterior major head pore. Striae
absent around head pores. A small pore like thickening
is located behind the posterior angle of head shield.
Labrum of moderate size. Labral keel moderately wide,
with a blunt apex. Anterior margin of keel in studied
specimens polygonal, posterior margin weakly convex
to straight, with two clusters of short setules. Thorax
two times longer than abdomen. Dorsal surface of ab-
dominal segments not saddle-shaped. Abdominal joint
not developed. Postabdomen (Fig. 8H) large, subrect-
angular, moderately high, with parallel margins, weak-
ly narrowing at the end. Length about 2.5 height. Ven-
tral margin straight. Basis of claws bordered from dis-
tal margin by clear incision. Distal margin almost
straight; distal angle rounded, sometimes weakly pro-
truding. Dorsal margin weakly convex to straight in
postanal portion and weakly concave in anal one, with
distal part about 2.5 times longer than preanal one,
with postanal portion 2.5–2.8 times longer than anal
one. Preanal angle well expressed, postanal angle not
defined. Preanal margin almost straight (Fig. 8I), with
11–13 well-developed, sharp composite denticles, each
with 2–4, rarely 5, spinules along anterior margin; size
of denticles increasing distally. Length of longest den-
ticles about 1.5X the width of base of postabdominal
claw, more than 3 times exceeding the width of the
denticle base. Postanal portion with 10–12 broad later-
al fascicles, posteriormost setule of each fascicle long-
est, thicker than others, 1.5 times shorter than neigh-
boring marginal denticles. Anal portion with several
smaller fascicles, spaced irregularly. Postabdominal
claw (Fig. 1J) of moderate length, slightly longer than
preanal portion of postabdomen. Basal spine long and
slender, about 0.35 length of the claw. A row of 7-10
long setules between basal spine and the base of post-
abdomen. Antenna I (Fig. 8K) of moderate size, length
about 3 widths, with a cluster of 3–4 long setules about
one third the length of antennule at anterior face. An-
tennular seta thin, more than 1/2 length of antennule,
arising terminally. Nine terminal aesthetascs, two of
them long and thick, longer than antenna I itself, all
others much shorter, about 1/2–1/3 the length of anten-
na I. Antenna II relatively short (Fig. 8L). Antennal
formula, setae 0-0-3/1-1-3, spines 1-0-1/0-0-1.Basal
segment robust, with very short seta between branches,
branches relatively short, all segments cylindrical, slen-
der. In each branch the basal segment is longest, mid-
dle segment slightly shorter than apical segment. Seta
arising from basal segment of endopodite thin, reach-
ing above the end of endopodite. Seta arising from
middle segment of endopodite, of similar size to apical
setae. Two shortest apical setae on exopodite and two
on endopodite with a very long spinule at the point of
articulation. Spine on basal segment of exopodite slight-
ly longer than middle segment. Spines on apical seg-
ments much shorter than apical segments.
Limb I of moderate size (Fig. 9A–C), with ovoid
epipodite. A long accessory seta only slightly shorter
than ODL seta, with long setules in distal part. ODL
with one seta. IDL with three setae and several clusters
of hard setules. IDL seta 1 large and broad, claw-like,
strongly curved, slightly longer than seta 2; IDL setae 2
and 3 with thin setules in distal part, seta 3 slightly
shorter than ODL seta, seta 2 about 2/3 the length of
seta 3. Endite 3 with four setae subequal in length.
Endite 2 (Fig. 3C) with two long distally setulated
setae (e–f), a shorter seta near their base (d) and a
naked inner seta (2) and small sensillum on anterior
face of limb; seta e long, two times longer than seta f.
Endite 1 with two 2-segmented setae (g–h), both setu-
lated in distal part, a flat plumose seta pointed the limb
base (i), and a naked inner seta (3). Inner seta 3 1.5
times longer than inner seta 2 Seven-eight rows of thin
long setules on ventral face of limb. Two ejector hooks,
one slightly shorter than other. Maxillar process elon-
gated, with a short setulated seta in distal part (not
represented in Fig. 9A).
Limb II subtriangular (Fig. 9D–E). Exopodite (Fig.
9, E: ext) elongated, with a slender seta as long as
exopodite body itself, and a cluster of very long setules
distally. Eight scraping spines, increasing in length
distally, scraper 4 being significantly shorter than scrap-
ers 3 and 5. Size of denticles on basal part of spines
decreasing from basal to distal spines. Distal armature
50 P.G. Garibian et al.
Fig. 8. Parthenogenetic female of Alona cf. affinis from River Kharpy, 15 km from its mouth, locality 19. A — general view; B —
valve; C–E — armature of postero-ventral valve portion; F — head shield; G — dorsal head pores; H — postabdomen; I — its dorso-distal
portion; J — postabdominal claw; K — antenna I; L — antenna II. Scale bars: 0.1 mm.
Рис. 8. Партеногенетическая самка Alona cf. affinis из реки Харпи 15 км вверх от устья, точки 19. A — общий вид; B —
створка; C–E — вооружение заднебрюшной части створки; F — головной щит; G — спинные головные поры; H — постабдомен;
I — его дорсодистальная часть; J — постабдоминальный коготок; K — антенна I; L — антенна II. Масштабная линейка: 0,1 мм.
of gnathobase with four elements. Filter plate II with
seven setae, the posteriormost member shorter than
others.
Limb III (Fig. 9F–G) with ovoid epipodite lacking
a projection. Exopodite of irregular shape, with seven
setae. Seta 3 being longest, setae 6 about 1/2 length of
seta 3, seta 7 1.5 times shorter than seta 6, other setae
very short. Setae 1–5 plumose, seta 6 with three rows
of hard setules in distal part, seta 7 with thin setules on
its distal part. Distal endite with 3 setae, two distalmost
members scraping, slender, sharp, with denticles in
distal part; short bottle-shaped sensillum located be-
tween their bases; basal most seta flattened, as long as
basal scraping setae, bilaterally armed with long set-
ules. Basal endite with 4 plumose setae increasing in
size basally. Four pointed soft setae increasing in size
basally, a small bottle-shaped sensillum near the distal-
most seta. Distal armature of gnathobase with four
51
Cladocera and Copepoda of Lake Bolon
Fig. 9. Thoracic limbs of parthenogenetic female of Alona cf. affinis from River Kharpy, 15 km from its mouth, locality 19. A — limb
I, inner view; B — its distal portion; C — a portion of limb corm; D — limb II; E — its exopodite; F — exopodite of limb III; G — inner-
distal portion of limb III; H — exopodite of limb IV; I — inner-distal portion of limb IV, inner view; J — its outer view; K — limb V; L —
limb VI. Scale bars: 0.1 mm.
Рис. 9. Торакоподы партеногенетической самки Alona cf. affinis из реки Харпи 15 км вверх от устья, точки 19. A — торакопод
I, вид изнутри; B — его дистальная часть; C — часть основания торакопода; D — торакопод II; E — его экхоподит; F — экзоподит
торакопода III; G — внутренняя дистальная часть торакопода III; H — экзоподит IV; I — внутренняя дистальная часть торакопода
IV, вид изнутри; J — вид снаружи; K — торакопод V; L — торакопод VI. Масштабная линейка: 0,1 мм.
elements; the first one elongated, narrowing distally
sensillum, second strongly geniculated seta, third and
fourth — spines. Filter plate III with seven setae.
Limb IV (Fig. 9H–J) with setulated pre-epipodite;
epipodite oval, with a finger-like projection shorter
than exopodite itself. Exopodite rounded, with six set-
ae. Seta 1 and 2 being longest, equal in length; seta 3
slightly shorter, bending toward inner portion of limb;
seta 4 about 2/3 length of seta 1, bending toward inner
portion of limb; setae 5–6 subequal in length, slightly
52 P.G. Garibian et al.
Fig. 10. General view of exuvium of parthenogenetic female of Coronatella trachystriata from Lake Bolon’ about 300 m from the
shore, locality 2. Scale bar: 0.1 mm.
Рис. 10. Общий вид экзувиума партеногенетической самки Coronatella trachystriata из озера Болонь, в примерно 300 м от
берега, точки 2. Масштабная линейка: 0,1 мм.
shorter than seta 4. Setae 1–4 plumose, setae 5–6 with
short setules. Inner portion of limb IV with four setae
and narrowing distally sensillum. Scraping seta slen-
der, three flaming-torch seta decreasing in size basally,
with 7–9 long setules each. Small sensillum between
the base of middle and basal flaming-torch setae. Three
soft setae slightly increasing in size basally. Gnatho-
base with one long 2-segmented setae, a small hillock
distally and a sensillum. Filter plate IV with five setae.
Limb V (Fig. 9K) with setulated preepipodite; epi-
podite oval, with a finger-like projection as long as
epipodite itself. Exopodite divided into two lobes, with
four plumose setae: setae 1–3 long, subequal in length;
seta 4 three times shorter. Inner lobe broad, rounded
with setulated inner margin. At inner face, two setae
densely setulated in distal part, one of them very long,
slightly longer than exopodite setae, the other two times
shorter. Filter plate V with three setae, two broad sen-
sillum-like structures between inner face setae and fil-
ter plate.
Limb VI (Fig. 9L) as elongated oval lobe with
setulated margin.
Length of adult female 0.73–0.92 mm.
Ephippial female and male. Not found.
Comments. The representatives of the studied pop-
ulation differ from Eurasian populations of A. affinis s.
str. [Sinev, 1997; Alonso, 1996; Hudec, 2010] in two
minor characters of their thoracic limbs: (1) scraper 4
of limb II is significantly shorter than scapers 3 and 5
and (2) the main sensillum of inner portion of limb IV
is elongated whereas it is bottle-shaped in typical A.
affinis. All studied specimens have some denticles on
postero-ventral corner of valves. According to Sinev
[1997], specimens of Alona affinis with denticles on
posteroventral angle represent a species variety. Thus,
the conspecificity of Lake Bolon’s population with
Alona affinis s.str. seems doubtful.
Coronatella trachystriata (Chen, Zhang et Liu, 1994)
Fig. 10.
Body low oval, strongly compressed laterally, with
maximum height at body middle. Dorsal margin of
carapace convex, posterior margin strongly convex,
postero-ventral angle broadly rounded, postero-dorsal
angle without denticles, with numerous thin setules not
organized into groups (Fig. 10). Valves with a promi-
nent linear longitudinal sculpture. Head small, rostrum
in lateral view truncated, much longer than antenna I.
Antenna I typical for genus, Antenna II with antennal
formula: setae 0-0-3/0-1-3; spines 1-0-1/0-0-1. Limb I
with IDL having two setae, seta 1 absent. Seta 3 large
and thick, with long, thick spinules; seta 2 two times
thinner and 1.5 times shorter than seta 3, also armed
with long, thick spinules.
Comments. Only a single exuvium (without post-
abdomen) was found, nevertheless this permits confi-
dent identification of this taxon. This is a rare Far
Eastern taxon found to date in China [Chen et al.,
1994], Far East of Russia [Kotov et al., 2011a] and on
Jeju Island (South Korea) [Kotov et al., 2018]. Our
record is only the second of C. trachystriata in Russia.
Subclass Copepoda Milne-Edwards, 1840
Order Calanoida Sars, 1903
Family Temoridae Giesbrecht, 1893
Heterocope soldatovi Rylov, 1922
Fig. 11A–D.
Female. Prosome narrow, the greatest width in ceph-
alosome, which is almost equal in length to thoracic
somites. Urosome long; genital double somite almost
the same width along the entire length (Fig. 11A).
53
Cladocera and Copepoda of Lake Bolon
Fig. 11. Heterocope soldatovi from Lake Bolon about 300 m from the shore, locality 2 (A–D) and Diacyclops crassicaudis from River
Simmy at Cheremshiniy Kordon, locality 13 (E–I). A — female, urosome; B — gonoporal plate; C — legs V; D — male, legs V; E —
female, caudal rami; F — antenna I; G — leg I; H — leg IV; I — leg V. Scale bar: 0.1 mm.
Рис. 11. Heterocope soldatovi из озера Болонь приблизительно в 300 м от берега, точки 2 (A–D) и Diacyclops crassicaudis из
Реки Симми у Черемшинного кордона, точки 13 (E–I). A — уросома самки; B — гонопорная пластинка; C — торакопод V; D —
самец, торакопод V; E — самка, каудальные ветви; F — антенна I; G — торакопод I; H — торакопод IV; I — торакопод V.
Масштабная линейка: 0,1 мм.
54 P.G. Garibian et al.
Gonoporal plate with two large, curved tooth-like pro-
cesses with short blunt lobes between them (Fig. 11B).
Surface of genital double somite covered with rows of
curved spinules. Caudal rami slightly shorter than anal
somite. Antenna I reaches anterior margin of caudal
rami. Legs V uniramous (Fig. 11C). Inner side of its
basis convex, with a row of fine setae on posterior
margin; first exopod segment with short outer spine
and inner row of fine setae; second exopod segment
with four inner spiniform processes equal in size, two
outer short spines, a single long, curved apical process
with a row of small spines in terminal half.
Male. Armature of all swimming legs symmetrical.
Legs V uniramous, asymmetrical. Exopod of right leg
V bi-segmented, without a specific armature (Fig. 11D).
Basal segment of left leg V with a long inner process;
first exopod segment long and slightly curved, with
spine on inner posterior margin; second exopod seg-
ment longer, with two outer spines, a row of fine setae
on inner margin, with one small and one long apical
spines, with inner posterior lateral row of 7-9 small
spines. Size in our material: female 2.3–2.4 mm, male
2.0–2.2 mm.
Comments. The species is an endemic of the Rus-
sian Far East. Earlier H. soldatovi was recorded from
the lower reaches of the Amur River [Borutsky, 1952b],
shallow water bodies of the Primorsky Krai [Smirnov,
1929], the Ussuri River, the channel from Lake Lebehe
to Lake Khanka [Rylov, 1933], and Gassi Lake [Ya-
vorskaya, 2018]. Probably this species will be found in
the north-east of China.
Order Cyclopoida Burmeister, 1834
Family Cyclopidae Rafinesque, 1815
Diacyclops crassicaudis (Sars, 1863)
Fig. 11E–I.
Female. Body relatively slender. Posterior margin
of the last prosome somite prominently protrudes. Gen-
ital double-somite wide, its length approximately equal
to width, seminal receptacle wide. Caudal rami about
4.0–4.2 times as long as wide, slightly divergent; later-
al setae attached at the beginning of posterior quarter
of caudal rami; outer terminal setae longer than inner
terminal setae (Fig. 11E). Antenna I 12-segmented,
reaching posterior margin of cephalothorax (Fig. 11F).
Exopodites and endopodites of legs I to 4 3-segmented
(Fig. 11G–H). Length of the third segment of legs IV
endopod approximately equal to its width. Of two
apical spines of this segment, inner one 1/3 longer than
the outer (Fig. 11H). Caudal side of coxopodite of legs
IV with four spine groups A-B-C-E [Alekseev, Defaye,
2011]. Apical spine of leg V exopodal segment slightly
longer than the segment (Fig. 11I). Size in our material
0.74–0.75 mm.
Comments. D. crassicaudis is recorded in water
bodies of Far East for the first time. This species is
regarded to be widely distributed from the Arctic to
subtropical latitudes [Rylov, 1948; Fefilova, 2015].
Two specimens were found in the River Simmy near
Cheremshiniy Kordon and are similar to those found in
more northern regions [Novichkova, Chertoprud, 2017;
Dimante-Deimantovica et al., 2018].
C. Biodiversity analysis
Our analysis of the Copepoda biodiversity (Fig. 12)
reveals that the group is comparatively better studied:
both sample-based rarefaction curve and the best spe-
cies richness estimator reach the same plateau at 13
taxa. In contrast, neither sample-based rarefaction curve
nor the best species richness estimator reaches a pla-
teau for the Cladocera. Therefore, the cladoceran biodi-
versity of the Lake Bolon basin is still incompletely
studied, but nevertheless some important conclusions
could be made. Finally, among the taxa revealed here,
either no obvious dominant species or dominant spe-
cies complexes were obtained.
Discussion
Cladocerans of the Far East of Russia are studied in
general better as compared with the copepods, and no
new records of the cladocerans from this region are
made here as compared to the list of Kotov [2016]. In
Table 2 we subdivided them into the main faunistic
complexes as it was made by Kotov [2016], but even
more roughly. Most our taxa belong to an artificial
“complex” of the species which are widely distributed
in Eurasia (or even in Holarctic), or regarded to be
“cosmopolitan”. Each such taxon apparently needs an
accurate global taxonomic revision keeping in mind
“Frey”s non-cosmopolitanism paradigm” of cladocer-
an biogeography [Frey, 1973, 1982]. We are sure that
many such “taxa” are in reality species complexes which
could not be discriminated at recent level of morpholo-
gy-based taxonomy. For instance, it was demonstrated
as a result of two pan-Palaearctic phylogeographic stud-
ies that “Chydorus sphaericus” is a group of several (at
least three) taxa with different distribution ranges, and
Chydorus sphaericus s.str. does not occur in the Rus-
sian Far East [Belyaeva, Taylor, 2009; Kotov et al.,
2016]. Also there is evidence of the existence of other
North Eurasian cryptic species groups: Diaphanosoma
brachyurum s.l. [Korovchinsky, 2004; Korovchinsky,
Sheveleva, 2009], Moina micrura [Bekker et al., 2016],
Polyphemus pediculus [Xu et al., 2009], and some
other taxa.
In some other cases, genetic data confirm the con-
specificity of populations from Europe and Far East as
it is the case of Eurycercus macracanthus, Daphnia
sinensis, Moina macrocopa [Bekker et al., 2012, 2016;
Popova et al., 2016] or some clades of P. pediculus
[Xu et al., 2009]. Therefore, both the «non-cosmopoli-
tanism” paradigm is not universal and taxonomic status
and geographical range of all poorly studied taxa need
a revision. This makes premature any global conclu-
sions on the cladoceran biogeography and status of the
55
Cladocera and Copepoda of Lake Bolon
Fig. 12. Empiric and estimated number of taxa of Copepoda (A), Cladocera (B) and portion of water bodies (among 20) where each
taxon was recorded (C). Triangles — sample-based rarefaction curve; quadrates — best species richness estimator (Chao 2 for Copepoda,
Chao 1 for Cladocera).
Рис. 12. Эмпирическое и ожидаемое число таксонов Copepoda (A), Cladocera (B) и доля водоемов (из 20), в которой найден
каждый таксон (C). Треугольникиэмпирическая кривая разряжения, квадратытаковая согласно лучшей модели оценки
биоразнообразия (Chao 2 для Copepoda, Chao 1 для Cladocera).
Far Eastern cladoceran fauna. Here we just confirm at
morphological level that Sida crystallina, Acroperus
harpae, A. angustatus, Camptocercus lilljeborgi, and
Kurzia latissima are present in the Far East, and their
females from the Far East and in Europe are morpho-
logically undistinguishable. However, for better confi-
dence we need to compare males because they are
more valuable for differentiation of close species (see
Popova et al., 2016; Smirnov, Kotov, 2018).
At the same time, other types of the cladoceran
distribution ranges are remarkable and could be pre-
liminarily analyzed. The taxa widely distributed in East-
ern Eurasia, but absent in Western Eurasia, have been
known long ago [Smirnov, 1971; Korovchinsky, 1979].
56 P.G. Garibian et al.
Taxon 1 2 3 4 5 6 7 8 9
Cladocera
Acroperus angustatus Sars, 1863 0 0 0 0 1 0 0 0 0
Acroperus harpae (Baird, 1834) 0 1 0 0 1 1 1 1 0
Alona cf. affinis (Leydig, 1860) 0 0 0 0 0 0 0 0 0
Alonella excisa (Fischer, 1854) 0 0 0 0 1 1 1 0 0
Alonella nana (Baird, 1843) 0 0 0 0 1 0 0 0 0
Bosmina longirostris (O.F. Müller,
1776) 0 1 0 0 0 0 0 0 0
Bosminopsis deitersi Richard,
1895 0 1 0 0 0 0 0 0 0
Camptocercus lilljeborgi Schödler,
1862 0 0 0 0 0 0 0 0 0
Camptocercus uncinatus Smirnov,
1971 0 0 0 0 0 0 0 0 0
Ceriodaphnia pulchella Sars, 1862 0 0 0 0 0 0 0 0 0
Ceriodaphnia reticulata (Jurine,
1820) 0 0 0 0 0 1 1 0 0
Chydorus cf. sphaericus (O.F.
Müller, 1776) 1 1 0 1 1 1 1 0 0
Coronatella rectangula (Sars,
1862) 0 1 0 1 0 0 0 0 0
Coronatella trachystriata (Chen,
Zhang et Liu, 1994) 0 1 0 0 0 0 0 0 0
Daphnia sp. 0 1 0 0 0 0 0 0 1
Diaphanosoma amurensis
Korovchinsky et Sheveleva, 2009 0 0 0 0 0 0 0 0 0
Diaphanosoma sp. 0 0 0 0 0 1 1 0 0
Diaphanosoma macrophtalma
Korovchinsky et Mirabdullaev,
1995 1 0 0 0 0 0 0 0 0
Disparalona chappuisi (Brehm,
1931) 0 0 0 0 0 0 0 0 0
Disparalona ikarus Kotov et
Sinev, 2011 0 0 0 0 0 0 0 0 0
Eurycercus macracanthus Frey,
1973 0 0 0 0 1 0 0 0 0
Flavalona costata (Sars, 1862) 1 1 0 1 1 1 0 0 0
Graptoleberis testudinaria
(Fischer, 1848) 0 0 0 0 0 0 0 0 0
Ilyocryptus spinifer Herrick, 1882 0 0 0 0 0 0 0 0 0
Kurzia latissima (Kurz, 1875) 0 0 0 0 0 0 0 0 0
Macrothrix rosea Jurine, 1820 0 0 0 0 0 0 0 0 0
Moina micrura Kurz, 1875 0 0 1 0 0 0 0 1 1
Table 2. Taxa recorded in twenty water bodies from the Lake Bolon basin.END — endemic of Far East; EUR — widely
distributed in Eurasia or even in Holarctic and needs a revision; EEUR — distributed in eastern portion of Eurasia;
COS — so-called “cosmopolitan” taxon needs a revision; THE — taxon of southern thermophylous complex for which the
Amur basin is its northernmost region of occurrence.
57
Cladocera and Copepoda of Lake Bolon
10 11 12 13 14 15 16 17 18 19 20
Total no. of
localities
Faunistic
complex
1 0 1 1 1 1 0 0 0 1 0 7 EUR
1 1 0 1 0 0 1 1 1 1 0 12 EUR
0 0 0 1 0 0 0 0 1 1 1 4 EUR
0 0 0 0 0 0 0 0 1 1 0 5 COS
0 0 0 0 0 0 0 0 0 0 0 1 COS
0 1 0 0 0 0 0 0 0 0 0 2 COS
0 1 0 0 0 0 0 0 0 0 0 2 THE
0 0 0 0 1 0 0 0 1 1 0 3 EUR
0 0 0 0 0 0 0 0 0 1 0 1 EEUR
0 1 0 1 0 0 0 1 0 0 0 3 COS
0 0 0 0 0 0 0 0 0 0 0 2 COS
1 1 1 1 1 1 1 1 0 1 0 15 COS
0 1 0 0 0 0 0 0 0 1 0 4 COS
0 0 0 0 0 0 0 0 0 0 0 2 END
0 0 0 0 0 0 0 0 0 0 0 2 ?
0 0 0 1 0 0 0 1 0 0 0 2 EEUR
0 1 0 0 0 0 0 0 0 0 0 3 ?
1 0 0 0 0 0 0 0 0 0 0 2 EUR
0 0 0 1 0 0 0 0 0 0 0 1 THE
0 0 1 0 0 0 0 0 0 0 0 1 END
0 1 0 0 0 1 1 0 1 1 1 7 EUR
0 1 1 1 1 0 0 1 1 1 0 12 COS
0 0 0 0 0 0 1 0 1 0 0 2 COS
0 0 0 0 1 0 0 0 0 0 0 1 THE
1 0 0 0 0 0 0 0 0 0 0 1 EUR
0 0 0 1 0 0 0 0 0 0 0 1 EUR
0 0 0 0 0 0 0 0 0 0 0 3 COS
Таблица 2. Таксоны, найденные в 20 водоемах в бассейне Озера Болонь. END — эндемик Дальнего Востока; EUR —
таксон, широко распространен а Евразии или даже в Голарктике, который должен быть подвергнут ревизии;
EEUR — распространен в восточной части Евразии; COS — так называемый «космополит», который должен быть
подвергнут ревизии; THE — таксон южного теплолюбивого комплекса, для которого бассейн Амуранаиболее
северный регион обитания.
58 P.G. Garibian et al.
Taxon 1 2 3 4 5 6 7 8 9
Monospilus daedalus Kotov et
Sinev, 2011 0 1 0 0 0 0 0 0 0
Nedorchynchotalona chiangi
Kotov et Sinev, 2011 0 1 0 0 0 0 0 0 0
Picripleuroxus laevis (Sars, 1862) 0 0 0 0 0 0 0 0 0
Picripleuroxus quasidenticulatus
(Smirnov, 1996) 0 0 0 0 0 1 0 0 0
Picripleuroxus striatus (Schödler,
1862) 0 1 0 0 1 1 1 0 0
Pleuroxus aduncus (Jurine, 1820) 0 0 0 0 0 0 0 1 0
Pleuroxus truncatus (O.F. Müller,
1785) 0 1 0 0 0 0 0 0 0
Polyphemus cf. pediculus
(Linnaeus, 1761) 1 1 0 1 1 1 1 0 0
Pseudochydorus globosus (Baird,
1843) 0 0 0 0 0 0 0 0 0
Scapholeberis kingii Sars, 1888 0 1 0 1 0 0 0 0 0
Scapholeberis mucronata (O.F.
Müller, 1776) 0 0 0 1 1 1 1 0 0
Scapholeberis sp. 1 1 0 0 0 0 0 0 0
Sida crystallina (O.F. Müller,
1776) 1 1 1 1 1 1 1 0 0
Sida ortiva Korovchinsky, 1979 0 1 0 0 0 0 0 0 0
Simocephalus exspinosus (De
Geer, 1778) 0 0 0 0 0 0 0 0 0
Simocephalus mixtus Sars, 1903 0 0 0 0 1 1 1 1 0
Simocephalus serrulatus (Koch,
1841) 0 0 0 0 1 1 0 0 0
Simocephalus sp. 0 0 0 1 1 0 0 0 0
Copepoda
Copepodites varia 0 1 0 1 1 1 1 0 0
Cryptocyclops bicolor (Sars, 1863) 0 0 0 0 0 0 0 0 0
Diacyclops crassicaudis (Sars,
1863) 0 0 0 0 0 0 0 0 0
Ectocyclops phaleratus (Koch,
1838) 0 0 0 0 0 0 0 0 0
Eucyclops macruroides
denticulatus (Graeter, 1903) 0 0 0 0 0 0 0 0 0
Eucyclops serrulatus (Fischer,
1851) 1 0 0 0 1 1 1 0 0
Eudiaptomus vulgaris (Schmeil,
1898) 0 0 0 0 0 0 0 0 0
Heterocope soldatovi Rylov, 1922 0 1 0 0 0 0 0 0 0
Macrocyclops albidus (Jurine,
1820) 0 0 0 0 0 0 0 0 0
Table 2 (continued)
59
Cladocera and Copepoda of Lake Bolon
10 11 12 13 14 15 16 17 18 19 20
Total no. of
localities
Faunistic
complex
0 0 0 0 0 0 0 0 0 0 0 1 END
0 0 0 0 0 0 0 0 0 0 0 1 END
0 0 0 0 0 0 0 0 1 0 0 1 EUR
0 0 0 0 0 0 0 0 0 0 0 1 THE
0 1 0 1 1 1 1 0 1 0 0 10 EUR
0 0 0 0 0 0 0 0 0 1 0 2 COS
0 1 1 1 1 1 1 1 1 1 0 10 EUR
1 0 1 1 1 1 0 1 0 1 1 14 EUR
0 0 0 0 0 0 0 0 1 0 0 1 EUR
0 0 0 0 0 0 0 0 0 0 0 2 THE
1 1 1 1 0 0 0 1 0 1 1 11 EUR
0 0 0 0 0 0 0 0 0 0 0 2 ?
1 1 0 1 1 1 1 1 1 1 0 16 EUR
0 0 1 1 0 0 0 0 0 0 0 3 EEUR
0 0 0 0 0 0 0 0 0 1 0 1 COS
0 1 1 0 1 1 1 1 1 0 1 12 COS
0 0 0 0 0 0 0 0 0 0 0 2 COS
0 0 0 0 0 0 0 0 0 0 0 2 ?
1 1 1 1 1 1 1 1 1 1 1 16
0 0 0 0 0 1 0 0 0 0 1 2 COS
0 0 0 1 0 0 0 0 0 0 0 1 COS
0 0 0 0 1 1 0 0 0 0 0 2 COS
1 1 0 1 0 0 1 0 1 1 1 7 EUR
1 1 1 1 1 1 1 1 0 1 0 13 COS
0 0 0 0 0 0 0 1 1 0 0 2 EUR
0 0 0 0 0 0 0 0 0 0 0 2 END
0 0 0 1 0 0 0 0 0 0 0 1 COS
Таблица 2 (продолжение)
60 P.G. Garibian et al.
Taxon 1 2 3 4 5 6 7 8 9
Megacyclops viridis(Jurine, 1820) 1 0 0 1 0 1 1 0 0
Mesocyclops leuckarti (Claus,
1857) 1 1 0 1 1 1 1 0 0
Microcyclops varians (Sars, 1863) 1 1 0 1 1 1 1 0 0
Paracyclops fimbriatus orientalis
(Alekseev, 1995) 1 1 0 0 0 1 1 0 0
Thermocyclops crassus (Fischer,
1853) 0 0 0 1 0 0 0 0 0
Total species richness of locality 11 22 2 13 18 19 16 4 2
Table 2 (continued)
Based on genetic data, it was concluded that there is a
main longitudinal biogeographic transitory zone be-
tween two faunistic super-complexes in the Yenisey
River basin (sometimes in the Ob River basin) [Bekker
et al., 2016, 2018; Kotov et al., 2016], as it was pre-
dicted earlier [Korovhinsky, 2004]. Only three cla-
docerans (Sida ortiva, Diaphanosoma amurensis,
Camptocercus uncinatus) from Lake Bolon basin be-
long to the Eastern Asian complex to date, but after
revisions of particular taxa such number should be
strongly increased.
At least five taxa (Scapholeberis kingi, Bosminop-
sis deitersi, Disparalona chappuisi, Picripleuroxus
quasidenticulatus, Ilyocryptus spinifer) of the Cladocera
found by us belong to a thermophylous (“tropical”)
complex, earlier revealed in the Zeya River basin [Ko-
tov et al., 2011a–b; Kotov, Sinev, 2011]. The number
of such taxa recorded from the Far East of Russia and
Korea is continuously increasing [Kotov et al., 2012;
Sinev, Samoamuang, 2013; Garibian, 2017; Neretina
et al., 2018]. For these taxa, the Amur River basin is an
“area of penetration” sensu Korovchinsky [2004, 2006],
while their “area of primary distribution” is situated in
tropics and subtropics. Their appearance in Russian
Far East could be a reflection of specific conditions
(monsoon climate) or historical factors which need to
be studied.
The most spectacular result of the last decade is a
conclusion on existing of a particularly remarkable
zone of the cladoceran endemism in the southern tem-
perate / northern subtropics of the Far East as it was
predicted by Korovchinsky [2004, 2006]. Such taxa
are absent in more northern regions, see publications
on Central Yakutia [Klimovsky et al., 2015a, b] and
Magadan Area [Streletskaya, 1975a, b]. Although they
are found in Korea [Kotov et al., 2012]. Some of them
are known from North China [Chiang, Du, 1979], but
we believe that the rest could be also found there. At
the same time, they are absent in tropical SE Asia
[Korovchinky, 2013; Kotov et al., 2013; Sinev, Ko-
rovchinsky, 2013]. Several taxa recorded in the Lake
Bolon area apparently belong to such East Asian en-
demics, and our study demonstrates that they are com-
mon in the Amur basin. We cannot conclude with
confidence whether they are strongly associated with
the Amur River basin in their northern distribution
limit, or not, which has to be studied later. Smirnov &
Kotov [2018] pointed out that the chydorids from such
an endemic complex demonstrate a specific Far East-
ern morphological style, e.g. having lateral projections
on valves.
The major part of the copepods noted in the Bolon’
s basin belong to cosmopolitan (9 species) and widely
distributed in Eurasia (3) species. Possible, many wide-
spread species of copepods are actually complexes of
cryptic species that are similar morphologically, in some
cases genetic methods could solve the problems of
cyclopoid taxonomy [Krajíèek et al., 2016; Mayor et
al., 2017]. A high level of polymorphism also was
recorded for some freshwater and brackishwater spe-
cies of the order Harpacticoida [Schizas et al., 1999;
Rocha-Olivares et al., 2001; Garlitska et al., 2012;
Kochanova et al., 2018]. Diacyclops crassicaudis,
which is recorded for the first time for this region, also
belongs to such “cosmopolitan” taxa. Being widely
distributed, it has been previously regarded as a “gla-
cial relict”, indeed, “areas of primary distribution” of
this species included the tundra and taiga zones, how-
ever, some populations are also found in more southern
regions (for example, North Africa and Creta) [Rylov,
1948]. In contrast, Heterocope soldatovi is an endemic
of the Russian Far East. No representatives of the south-
ern thermophylous species complex are found among
the copepods.
Thus, the fauna of the Cladocera and Copepoda of
the Bolon Lake Basin is diverse and specific, it in-
cludes endemics of the Far Eastern Region. The cla-
docerans are more speciose and heterogeneous in their
type ranges as compared to the copepods in this region.
Particularly, the southern thermophylous species com-
plex is detected there only for the former group, while
most copepods are cosmopolitan or widespread in Eur-
asia. In addition, if the fauna of copepods is adequately
evaluated in the Bolon lake basin, the cladoceran spe-
cies number is significantly underestimated. Further
investigations of the zooplankton of the Amur River
61
Cladocera and Copepoda of Lake Bolon
10 11 12 13 14 15 16 17 18 19 20
Total no. of
localities
Faunistic
complex
0 0 0 1 0 0 0 0 0 0 1 6 COS
1 1 1 1 0 1 1 1 0 1 0 14 COS
1 1 1 1 1 1 0 1 1 1 0 15 COS
0 1 1 1 0 1 1 1 1 1 1 13 EUR
1 0 1 1 0 0 1 1 1 0 1 8 COS
14 20 15 25 15 15 14 17 19 22 11
Таблица 2 (продолжение)
Basin water bodies are necessary. Just such data will
provide a basis for biogeographical analysis of the
Cladocera and Copepoda of Far East fauna as a whole.
Acknowledgments
The authors are very grateful to the staff of the
FSBI “Zapovednoe Priamurye” and Bolon’sky State
Nature Reserve for their help in organizing the expedi-
tionary works. Many thanks to R.J. Shiel for linguistic
corrections of earlier draft and M. Roshchin for pro-
viding photos of the Bolon Lake.
This study is supported by the Russian Science
Foundation (project No. 18-14-00325).
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Responsible editor V.A. Spiridonov
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FIGURE 4. Acroperus harpae (Baird, 1834) from Russia, Murmansk Area, Khibiny Mountains, Lake Malyi Vud'yavr. A – E—parthenogenetic female: A—antennule, B—antenna, C – D—outer and inner part of thoracic limb I, E—endites of limb II; F—juvenile male of instar I, inner part of thoracic limb I; G – H - juvenile male of instar II, G—antennule, H—inner part of thorachic limb I; I – K—adult male, I—antenna, J – K—outer and inner part of thoracic limb I. Scale bars: 0.05 mm.