The Need for a New Taxonomy for Lampreys

Abstract

Our results show that lampreys systematics are still very far from
perfect and requires teamwork of field biologists, ecologists,
morphologists and geneticists. The approach described in this paper,
allows explaining many aspects which could not be solved before such as
relations between migrating and non–migrating lampreys, parasitic and
non–parasitic lampreys; spatial–temporal communication or fragmentation
(and its degree) between different freshwater systems, a role of one or
another form for reproductive success maintenance of one or another
assemblage.

Full text

CHAPTER TEN
THE NEED FOR A NEW TAXONOMY
FOR LAMPREYS
ALEXANDR KUCHERYAVYY,
IVAN TSIMBALOV, ELIZAVETA KIRILLOVA,
DMITRY NAZAROV AND DMITRY PAVLOV
Introduction
We consider in this paper that some lamprey genera inhabiting Eurasia
are metapopulations (Levins 1969). Until recently this concept was seldom
used for fishes, particularly anadromous species such as, Salmonidae.
Recently it has received more attention, as reported by Braun et al. (2014);
Keefer & Caudill (2014); Moore et al. (2014); Pess et al. (2014). The
concept of metapopulations could apply to the Petromyzontidae that range
from typically anadromous species (Petromyzon, Caspiomyzon) to
freshwater (Ichthyomyzon), and to nonparasitic species (Docker 2009).
Of particular relevance is the lack of homing in lampreys which greatly
increases the connectivity within fresh water.
Modern taxonomy of lampreys includes the concept of satellite, or
paired species (Vladykov & Kott 1979; Docker 2009) which we have
proposed is problematic (Kucheryavyy & Tsimbalov 2015 b).
Anadromous species often inhabit shared watersheds and are sympatric
with satellite species. Some lamprey species have intermediate life history
strategies between nonparasitic brook lamprey and parasitic anadromous
lamprey stages (Kux 1965, 1967; AbouSeedo & Potter 1979; Tuunainen
et al. 1980; Iwata & Hamada 1986; Beamish 1987; Goodwin et al. 2006;
Kucheryavyi et al. 2007; Adams et al. 2008; Kucheryavyy 2008). Genetic
markers have also been unable to distinguish among satellite species
(Okada et al. 2010; Artamonova et al. 2011, 2015; Balakirev et al. 2014;
Li 2014; White 2014; Kucheryavyy & Tsimbalov 2015 a). There are also

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studies that report that different lamprey species can interbreed naturally
or artificially (Lauterborn 1926; Zanandrea 1959; Huggins & Thompson
1970; Piavis et al. 1970; Savvaitova & Maksimov 1978; Beamish &
Neville 1992; Cochran et al. 2008; Lasne et al. 2010; Hume et al. 2013;
Kucheryavyy et al. 2010; Kucheryavyy 2014b).
Understanding how populations or assemblages are isolated from each
other is important not only from the point of view of classical biology,
systematics, taxonomy, and evolution, but also for preservation of rare
species and the possibility of the resumption of fishery of some species.
Throughout this chapter, using principles of metapopulation theory, we
will show the importance of regional, temporal, biological interactions for
the understanding of lamprey species structure and for the maintenance of
their wellbeing. We propose to consider that some species of lampreys
are a taxon consisting of metapopulations associated by potential past or
present relationships.
Material and Methods
In this paper, we will use the classification of lampreys in accordance
with Lampreys of the World. An annotated and illustrated catalogue of
lamprey species known to date (Renaud 2011). The following names
differ from Renaud (2011): Arctic lamprey, Lethenteron camtschaticum
for following lampreys: Le. camtschaticum (Tilesius, 1811), Le. reissneri
(Dybowski, 1869), Le. kessleri (Anikin, 1905). Such usage is validated in
Kucheryavyy et al. (2007), Artamonova et al. (2011), Makhrov et al.
(2013), Balakiriev et al. (2014), Li (2014); European river lamprey,
Lampetra fluviatilis for following lamprey species: La. fluviatilis
(Linnaeus, 1758) and La. planeri (Bloch, 1784). This usage is validated in
Hume (2013); Korean lamprey, Lethenteron morii instead of
Eudontomyzon morii (Berg, 1931), that is validated in Pu et al. (2014);
Drin brook lamprey, Eudontomyzon stankokaramani (Karaman, 1974)
nonsynonym neither for Eu. mariae nor Eu. danfordi on the basis of the
data given in April et al. (2011) and the analysis given in this paper.
Genetics
Comparative analysis of mtDNA Cytochrome Oxidase subunit I was
based on sequences from genetic databases: GenBank (http://www.ncbi.
nlm.nih.gov/), EMBL (http://www.ebi.ac.uk/) and our own data.
Sequences analysis used alignment editor BioEdit (www.mbio.ncsu.edu/
bioedit/bioedit.html).

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253
Terminology
 Morph is a group of adult specimens that exhibit the same general
morphological and/or biochemical signs.
 The form is a final stage, for example, of an anadromous, resident
or lake type of life history. A non-matured specimen can be related
to a distinct form if it is reliably known that it cannot be related to
any other for, for example, juveniles migrating to sea may be
relegate to anadromous form.
 The territorial community is an aggregate of larvae and juvenile
specimens which populate a particular freshwater ecosystem.
 The primary group is an aggregate of adult specimens which spawn
within the limits of a particular freshwater ecosystem, during a
particular spawning season.
 The assemblage is an aggregate of all specimens which populate a
freshwater ecosystem and which consists of a primary group and
territorial community. A population is equivalent to an assemblage
only when a resident form populates a freshwater ecosystem for a
long time.
 A metapopulation is a group of assemblages.
Diversity of lampreys is represented by a composite complex of
species with a wide range of epigenetic forms (at least, in northern
latitudes of Eurasia). Development of a form in a freshwater system takes
place independently of other systems, and forms develop in response to
external factors (i.e. biotopes variety and their productivity, potentiality
for migrations to bigger watersheds).
Interpretation and Discussion
Morphs and forms
The anadromous feeding form, the lake form (as well as the forms
which have appeared in water storage reservoirs, can belong to the same
forms), the river feeding form, and the nonparasitic resident (freshwater)
form are accepted by overwhelming majority of researchers. It is
important to notice that, possibly, lake lampreys can be divided into
parasitic and nonparasitic forms, but at present we have no exact
information which allows us to determine the nonfeeding lake form. We
know that Lethenteron lamprey larvae live in river mouths that run into
Krasnoyarsk and Evenki water storage reservoirs (Yenisei River system),

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254
and also in Bratsk water storage reservoir (Angara River system). The
previously listed reservoirs are exposed in the center of the Eurasia
mainland and there are no reports of parasitic forms there. Furthermore,
Lampetra ammocoetes inhabit the Petrokrepost Cove of Ladoga Lake. We
know that, adults (Lethenteron) that differ both from nonfeeding resident,
and from parasitic lake specimens (and from anadromous specimens,
accordingly), spawn in the Raduga River upper reaches (Kamchatka River
system). One small nonparasitic matured male of Lampetra was found in
Ivankovskoye water storage below the Konakovskaya SDPP (Tver
Region).
We identify three typical anadromous morphs in the Okhotsk Sea
basin, and also, the so-called forma praecox, most likely, inhabits the
estuaries. We identified these forms using meristic, fecundity, feeding
migration, and sex ratio. According to the data from Orlov et al. (2008;
2014), besides horizontal distribution, there is also vertical distribution of
lampreys in the ocean. Data from Orlov et al. (2008) also are confirmed in
Lança et al. (2013), that show anadromous lampreys also differ in
biochemical parameters.
Our examinations for La. fluviatilis, which enters into the Neva River
from Gulf of Finland of Baltic Sea, show that, except for form diversities,
these interrelated forms also varied over years. Most likely, these have no
genetic basis and depend completely on external growth factors.
It is known that in Russia, parasitic lake forms of lampreys of genus
Lampetra inhabit Onega Lake, Ladoga Lake (Leningrad Region and
Republic of Karelia), Seliger Lake (Tver and Novgorod Regions);
lampreys of genus Lethenteron inhabit Azabachye Lake (Kamchatka
Peninsula) and Sopochnoe Lake (Iturup Island), and also Novosibirsk,
Vilyuy and Svetlinskoye water storage reservoirs (Nikanorov &
Nikanorova 1963; IvanovaBerg 1966; Sidorov & Pichugin 2005;
Golubtsov & Malkov 2007; Kucheryavyy 2014 a, b; Venediktov &
Kirillov 2014; Tsimbalov et al. 2015). They spawn in rivers and brooks
together with non-parasitic residents. In the latter cases (water storage
reservoirs) the origin of the parasitic lake forms is obviously traced from
the nonparasitic. For example, the Novosibirsk water storage reservoir
(1957-59), after building-up of the Novosibirsk HEPS dam. Lethenteron
lampreys also have appeared in basincooler waters of Belovskaya SDPS
(after 1964). They ascend from resident lampreys, but their biology still
needs to be studied (Yadrenkina 2005). As to the nonparasitic freshwater
(resident) form, its diversity is also large and associated with the
complexity of river systems (for example, brook and riverine morphs).

The Need for a New Taxonomy for Lampreys
255
The territorial community and primary group
We consider the territorial community (immature specimens populating
particular freshwater system) as aggregates of larvae (ammocoetes),
metamorphosing juveniles and postmetamorphic juvenile specimens.
Regional connection and communication between lamprey forms
The possibility of regular exchange by spawners straying into non-
natal rivers results in very close connection of freshwater habitats emptying
into a common marine basin. Here we give one more example thanks to the
Russian Academy of Sciences and Russian Geographical Society employees
who observed humpbacks whales Megaptera novaeangliae around
Commander Islands. As a result of these observations it has been ascertained
that the Pacific lamprey Entosphenus tridentatus actively uses whales. They
attach to its back, tail and fins, and do not unfasten even when parts of the
whale body appears out of the water (Fig. 101, centerfold, page xxiv-xxvi).
It is remarkable that dispersion of these species is the same in waters of the
northern Pacific Ocean including the Chukchi Sea and Gulf of Alaska, in
waters of Aleutian Islands, Eastern Kamchatka and British Columbia. It is
unlikely that lampreys can use such large mammals for feedings, but is
likely that they use whales for transportation.
Temporal communication between lamprey forms
Temporal communication exists because different generations of
spawners constantly occur in joint spawning areas and mix due to different
maturing rates of specimens of different form. This makes the separation
of forms within time, impossible as anadromous specimens bring new
combinations of attributes every spawning season.
Divergence and mechanisms of its overcoming
There are also relatively isolated systems such as short river systems in
which the resident form occurs, but anadromous adults might spawn there.
For example, the parasitic form of La. fluviatilis lamprey in the regulated
channel of the Volga watershed area has been noted (Vasilyeva & Sotnikov
2004). According to Naseka & Diripaska (2008), a specimen with characters
of anadromous Lampetra sp. has been captured in Taganrog Bay (Sea of
Azov). This marine basin is out of the area of the genus and the question on
origin of this lamprey remains open (see below).

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256
Fragmentation of species could appear in spawning areas used by
anadromous and resident specimens. However analysis of the data shows
that it does not take place frequently (Fig. 102). As it was mentioned
previously, the literature contains many examples of reciprocal crossing
between migrant and resident forms (in natural and managed conditions).
Here we will report some of our observations and experiments.
Figure 102. Position of the anadromous specimens in assemblages. A  Utkholok
River, grey color covers distribution of the territorial community,  places in
which anadromous form of Lethenteron camtschaticum found; B  Ottawa River,
spawning places of  Ichthyomyzon castaneus,  Ichthyomyzon unicupsis and

The Need for a New Taxonomy for Lampreys
257
 Ichthyomyzon fossor. The observed by Ren et al. (2014) level of similarity
between nucleotide sequences says that the two latter species are ecotypes of one
species.
Figure 103. Patterns of the non-classical spawning behavior (grey color shows
males). A  a female hiding its head under a stone; B  a male sticking its head
above a females head; C  group spawning of two anadromous (bigger) and
several resident specimens.

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258
Difference in body sizes between migrants and residents is one of the
essential principles providing sympatric speciation. But adults overcome it
by various behavior patterns (Fig. 103). In the spawning areas the
classical behavior occurs when one male is attached to the female head
and twists with the tail its body in urogenital area, during spawning. It is
often possible to observe specimens either hiding a head under a stone
(females), or attaching to it (males) above female head. Small males,
which fasten to female considerably below a head, can fertilize eggs
together with large male. The various types of behavior enhance the
probability of forms interbreeding.
Experiments on lamprey reproductive products ability to maintain the
fertility (Kucheryavyy 2014 b) have shown that unlike sperm, which loses
the vitality in less than ten minutes, eggs do not lose fertility for 60
minutes (3.2 % of fertilized eggs thus have developed to a stage of
breakout of embryos branchiate pouches). As far as we know, this aspect
of lamprey reproductive biology has not been investigated before.
Considering that lamprey spawners constantly dig up the ground in
spawning areas such egg survivability plays the extremely important role
in maintenance of gene exchange in a primary group.
Finally, it is important to recognize the selection of interfering
isolation of resident spawners in the cases of paired spawning. It is known
that paired spawning takes place on smaller stretches closer to riverbanks.
In intensive water-level recession during the spawning period, such
stretches often have seaweed and spawned eggs perish. This especially
works against the paired spawning of resident lampreys (Kucheryavyy
2014 b) and, probably, supports prevalence of descendants of the group
spawning. Data on the COI haplotype occurrences do not exhibit
correlation with the life history strategy of their carriers for Lethenteron
(Artamonova et al. 2015): in samples where the frequency of a haplotype
was high, there were always both anadromous and residential specimens
that carried it. Furthermore, if any haplotype was unique (found in only
one specimen), there were cases where the haplotype of an anadromous
specimen was derivate from that of a freshwater specimen.
Lamprey assemblages
In the most simplified form, it is possible to present all diversity of
lamprey assemblages as selfcontained type assemblages (true population),
assemblage of producing type (presented by migrant specimens), mixed
type and pseudoabsorbing type assemblage. Actually, in places not

The Need for a New Taxonomy for Lampreys
259
exposed to significant anthropogenic influence, Lampetra and Lethenteron
lampreys have in most cases mixed type assemblage (Fig. 104).
Figure 104. Theoretical schemas of the assemblage basic structures. Black color
of lines  resident specimens, dark grey  territorial community, light grey color 
migrant specimens. Each schema is in clockwise order. Mixed types of
assemblages: A  case of impossible influence of different origin migrants; B 
case of influence of migrants of different origin; F  anadromous species; I 
complex species. Donor type: C  in natural conditions, i.e. tributaries of upper
reaches of long rivers; D, H  cases of human-induced degradation. True
populations: E  population of residents; G  case of migrant species with
impossible influence of migrants of different origin.
True populations
River systems with true populations (Fig. 104 d, e, g) that are isolated
for quite some time from other lamprey assemblages, occur in the Moscow
Region rivers, such as the Chismena River. This river is a fourth order
tributary of the upper Volga River running into the Caspian Sea. We
consider that only the resident form of Lampetra is La. fluviatilis but its
taxonomy is uncertain. This species arrived here either in the end of the
last boulderperiod (68 KA), or, most likely, as a result of the

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Vyshnevolotskaya aqueous system constructed by Peter I in 1709. The
lamprey spawners and larvae (our collection has more than 200 specimens
of spawners and 150 specimens of larvae from the Chismena and the
Bolshaya Sestra rivers, collected in different years) have significant
differences compared to Caspiomyzon and Eudontomyzon that populate
this sea basin.
Renaud (2011) has shown that two species of lampreys  Eu. mariae
and Eu. danfordi  inhabit the Danube River system. He identified
occurrences of parasitism for Eu. mariae on pike Esox lucius. According
to his data, Eu. danfordi, is a parasitic freshwater species. There is a
question, whether the assemblages formed by these species are isolated?
At first sight, areas of these species overlap in the Danube River system.
Specified as parasitic, Eu. mariae inhabit Jelena and Prut Rivers. Both
these rivers belong to the Danube River system. According to Renaud
(2011), examples of Eu. mariae parasitism are not found in other river
systems.
Three lampreys from Tisza River, investigated by us (ZMMU p-8419,
Coll.: Anonym, 1948) TL 221240 mm, differed from Eu. mariae by their
sharp teeth and larger total body length. Three sequences (one haplotype)
COI (582-589 bp) IDs are presented in April et al. (2011): JN026603,
JN026604, JN026605, belong to the specimens caught in Turiec (runs to
Váh, Danube River system). This haplotype differs by 3.5 % from the
haplotype of Eu. mariae from the Teterev River (Dnepr River middle
course) ID: JN026606 (550 bp). Also, according to our data sequence of
the lamprey from the Leshcha River (Republic of Belarus, upper Dnepr
system) differs by 0.3 % from haplotype of lampreys from the Teterev
River COI haplotypes (611 bp, comparison by 348 bp).
Results of this investigation show that most likely, Eu. mariae has no
parasitic stage, and also, it is unlikely that it is widely dispersed in the
Danube River system where the parasitic Eu. danfordi occurs. Most likely,
these two rivers are examples of isolated types of assemblage.
River systems of European seas basins represent a very interesting
example (Fig. 105 a). In our opinion, this example is extremely
convincingly and shows an inconsistency about the idea of low genetic
polymorphism of lamprey resident species within genus (Docker 2009,
Mateus et al. 2014). We have performed relatively rough analysis of these
species based on short COI sequences. As the length of the analyzed
sequences was only 348 nucleotides, we report only minimum fixed
percentages of nucleotide polymorphism (Table 101). Nucleotide
sequences of Eu. helenicus and Eu. graecus were similar and we combined
them for comparison with sequences of other species. This pair of

The Need for a New Taxonomy for Lampreys
261
species strongly differs from all other representatives of Eudontomyzon,
even on such short sequence and even the genus status is questionable. If
we accept that the level of species distinction is 2%, the status of other
taxonomic units is not questionable, except for Eudontomyzon sp. This
taxonomic unit is described by Geiger et al. (2014) from the Greek part of
the Vardar River system, which originates from Bistra Mountain in
Macedonia however this lamprey is genetically very different from two
other Greek lampreys, i.e. Eu. hellenicus and Eu. graecus.
Table 101. Minimal known genetic polymorphism of the fragment
mtDNA COI gene between lampreys from the intracontinental seas of
Atlantic Ocean.
h+g lan dan sta sp.
lan 8.62 0
dan 12.64 4.31 0
sta 14.37 5.75 2.29 0
sp. 13.51 4.89 1.43 2.59 0
mar 15.51 6.89 3.45 4.59 3.16
Note: h+g  Eu. hellenicus + graecus; lan  La. lanceolata; dan  Eu. mariae
(danfordi); sta  Eu. stankokaramani; sp.  Eudontomyzon sp; mar  Eu. mariae.
See comments in the text.
Most likely, the Eudontomyzon sp. ancestor arrived in Southern Europe
by a different way from that for the other Greek lampreys. It was settled
by top  together with Eu. danfordi and Eu. stankokaramani ancestors,
before the Bosporus and Dardanelles breakout, and Eu. hellenucus
(+graecus) were settled well after that time (Fig. 105 b, c). This example
shows that in real species, unconnected by migrant forms, the genetic
divergence level is rather high and similar to that for another groups of
vertebrates (Kartavtsev 2011).
In connection with the report of Freyhof & Kottelat (2008) we suggest
that it is necessary to reconsider the finding of Lampetra sp. lamprey in
Taganrog Bay Naseka & Diripaska (2008). The described specimen could
be anadromous representative of Eudontomyzon.
Mateus et al. (2011) discuss Iberian refugia in the Pliocene and
Pleistocene. Agreeing that the Iberian Peninsula was a refugium, we reject
the assumption of the lampreys speciation towards nonparasitic taxa.
About 811 KA, in the end of the Pleistocene, the Baltic basin was opened

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for Atlantic waters after the total disappearance of the Scandinavian ice
shield (Monin & Shishkov 1979), possibly, providing access for lamprey.
Figure 105. Distribution and possible dispersal routs of the species from
intracontinental seas of Atlantic basin. A  modified median network of
haplotypes. Italics show number of replacements in COI fragment of mtDNA,
circles show sample sites: 1  Eudontomyzon hellenicus+graecus (GenBank ID:
KJ553189.1, KJ553102.1, KJ553090.1, KJ553041.1, KJ553040, KJ552986.1,
KJ552907, JN026601.1, JN026602.1, and KJ553013.1, KJ553159.1); 2 
Lampetra lanceolata (GenBank ID: KJ55404.1, KJ554056.1, HQ579127.1,
JN026951.1  JN026955.1); 3  Eudontomyzon mariae (danfordi) (GenBank ID:
JN026603, JN026604, JN026605); 4  Eu. stankokaramani (GenBank ID:
KJ553549.1, KJ553565.1, KJ553610.1, KJ553619.1, KJ553620.1, KJ553632.1,
KJ553650.1, JN026607.1]); 5  Eudontomyzon sp. (?danfordi) (GenBank:
KJ553314.1, KJ553433.1); 6  Eudontomyzon mariae (GenBank ID: JN026606
and unpubl. data). B  Bølling oscillation (1112 KA), in black adumbration are
modern borders of watersheds, dark grey on territory of Eurasia is Inland
Eurasian Ocean; light grey in Atlantics is a derelict; point on the map is Bistra

The Need for a New Taxonomy for Lampreys
263
Mountain. C  Holocene during the Bosphorus and Dardanelles perforation (7.55
KA).
Mateus et al. (2011) proposed that these lampreys lost the ability to
migrate into marine waters (see Fig. 105) but our data show very close
relations between representatives of resident lampreys from Mediterranean
and Baltics (Kucheryavyy & Tsimbalov 2015 a). Probably, La. lanceolata
and Le. morii, and also series of other restricted range species are self
contained assemblages (populations) for which the anadromous stage is
unknown.
Assemblages of the producing type
This type of assemblage pushes out numerous surpluses from the
system in the form of migrating specimens. Thus, this type performs one-
way communication with other assemblages. Currently, very little is
known about the producing type in un-regulated rivers (Fig. 104 b). Here
we can only address the information on Talnikovy tributary of Utkholok
River, where spawners of anadromous form of Le. camtschaticum have
not been documented, but silver specimens with sharp teeth, have been
caught migrating downstream. Similar data have been published for the
ObIrtysh basin (Loshakova & Knizhin 2015). Also there is a series of
Lethenteron specimens (ZISP 25632, Lampetra fluviatilis japonica, Coll.:
Blumberg, Det.: Berg, 1936; TL 156201 mm) caught in the upper
Yenisei River that had coloration, teeth and eye diameter characteristic of
juvenile anadromous lampreys (smolts).
Many river systems were influenced by anthropogenic factors, such as
dam construction. The Onega Lake system is bound from Baltic Sea by
series of dams insuperable to spawners going upstream. At the lake there
are parasitic lampreys that differ both from nonparasitic and parasitic
lampreys from Ladoga Lake located downstream. Occasionally, lampreys
with features, similar to lampreys from Onega Lake, were found in
spawning areas in the rivers running into Ladoga Lake (Tsimbalov et al.
2015). I.e. the assemblage of Onega Lake system is a producing type for
assemblage of Ladoga Lake system. It is quite probable that three cryptic
species of Lampetra lampreys described by Mateus et al. (2013) actually
are genitor type assemblages which have arisen in human pressure
conditions (Fig. 106).

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Figure 106. System of (A) Finn Bay  Neva River  (B) Ladoga Lake  Svir
River  (C) Onega Lake. Shown established types of assemblages and possible
ways of their connections (corridors) via migrant specimens.
Assemblages of the mixed type
Assemblages of the mixed type are the most widespread and
numerous. Examinations of P. marinus (Fig. 104 f) show that this species
does not home, in that form as occurs for other anadromous fishes
(Bergstedt & Seelye 1995; Waldman et al. 2008). This provides constant
data exchange between marine forms.
C. wagneri has been endemic to the Caspian Sea since Miocene (Meek
1916). It was found in many rivers over all sea basins in Kazakhstan,
Russia, Azerbaijan, Iran and Turkmenistan, and not just in South or
SouthWestern part of the sea (Kiabi et al. 1999; Turkmenistan 2002;
Nazari 2007; April et al. 2011; Ibragimov & Shakaralieva 2014).
In assemblages of non-broken systems of short rivers in the genus
Lethenteron there are mainly resident specimens and the anadromous form
of the genus Lampetra predominates. Such divergence in assemblage
constructions of these two genera is probably occurs because Lethenteron
inhabits the salmon rivers, which are more productive and provide more
habitat than the short European rivers (Kucheryavyy et al. 2010; Lepskaya
& Kucheryavyy 2011; Kuzishchin et al. 2012).

The Need for a New Taxonomy for Lampreys
265
Figure 107. System of mixed type assemblage in a giant river (Yenisei River).

Chapter Ten
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Large river systems require detailed consideration. On the one hand,
river size allows producing a larger quantity of residents because of the
more suitable habitats and decreased competition. On the other hand, the
large rivers of the world have been influenced by human development.
Hypothetically, the lamprey assemblage of the Yenisei middle course is an
example mixed type where there are anadromous representatives of
Lethenteron both from the upper river stretches and its tributaries, and
from the Yenisei Bay of Kara Sea (Fig. 107).
Mixed type assemblages in complex fluvial-lacustrine systems
Complex systems such as sea  river  lake (water storage reservoir) 
river may be of special interest for research. But unfortunately, they are
mostly not studied in Eurasia. We provide some examples of what
assemblage types can arise. The system of Finn Bay  Neva River 
Ladoga Lake  Svir River  Onega Lake is described previously (Fig.
106).
The Sopochnoe Lake (Iturup Island) is separated from the sea by a
200meter river (Fig. 108). Specimens caught in the lake in August,
2001, fed on the lake form of Oncorhynchus nerka, kokanee (Sidorov &
Pitchugin 2005). Only three small brooks run into the lake. Evidently, in
these brooks exists a local non-parasitic form, as the minimal length of
adult lampreys was 92mm. Availability of a freshwater habitat, which can
be used by parasitic form for feeding on fish, and nearness of marine
watersheds provide the presence of two different types of parasitic
lampreys in this system.
The following system is another example: Ilistaya River  Khanka
Lake  Sungacha River  Ussuri River  Amur River (Fig. 109). Length
of spawners does not exceed 170 mm (143 mm average) in the Ilistaya
River. Here lampreys spawn in the end of MayJune, mainly by group
spawning. Till now, resident spawners have not been recorded in the
Sungacha River. However, large (more than 200 mm, i.e. anadromous
ones) silver specimens spawn here, in small numbers, in early May.
According to the concept proposed, the Ilistaya River is a type that is
relatively isolated from other assemblages. It does not produce
anadromous specimens and exists at the expense of resident form, but has
not lost the potential connection with other assemblages.

The Need for a New Taxonomy for Lampreys
267
Figure 108. System of mixed type assemblage in a short marine  lake  brooks
system (Sopochnoe Lake).
Metapopulations
Currently, we can describe lamprey metapopulations only partially.
The most obvious to us is the metapopulation of the Sea of Okhotsk (Fig.
1010). Being based on the analysis of the data received during long-term
observations by TINRO-Center (Tikhookeanskaya 2003), on
morphological data (Kucheryavyi et al. 2007; Kucheryavyy 2008; 2014 a)
and on genetic data (Artamonova et al. 2011; 2015), we have come to the
conclusion that there is a common pot in which anadromous form
originating from different river systems of Sea of Okhotsk basin are
stirred. The determination of a certain Amur metapopulation would be
sufficiently validated as it genetically differs (due to absence of one of
type of the main haplotypes) from other mass of specimens in the sea of
Okhotsk (Aramonova et al. 2015), as well, it is geographically relatively

Chapter Ten
268
isolated by Sakhalin Island. Possibly, during further studies, it can be
referred to as a Sea of Japan metapopulation or, on the contrary, its
relative independence will be confirmed.
For P. marinus there are metapopulations in North America and
Europe (Genner et al. 2012). Most likely, C. wagneri represents a uniform
metapopulation in which connection is performed at the expense of the
specimens growing in the Caspian Sea. Possibly, a uniform
metapopulation of Lampetra lampreys is present in Europe.
Metapopulations represent assemblage of one river for most
Eudontomyzon species as it has been shown above.
Figure 109. System with an example of pseudoisolated assemblage (Illistaya
River)

The Need for a New Taxonomy for Lampreys
269
Figure 1010. Metapopulation in the Sea of Okhotsk (see comments in the text).
Only the documented assemblages are depicted.
Conclusion
Despite the constantly growing number of papers devoted to lamprey
biology and systematics we are still only beginning to understand the
depth of the processes that generate and maintain their diversity.
Particularly it comes from the complexity of the observed patterns and the
process that provide the basis for them. Evolutionally events,
contemporary interactions between specimens and environment, human
impact, biogeographic process  these all play an important role in the
equilibrium providing species and specimens success. We believe, in the
perspective contribution of models explaining how the lamprey diversity
varies across space, time, and environmental conditions.
We have tried to demonstrate the diversity of the mechanisms that
provide stability in lamprey species throughout a geological history, and
under anthropogenic influences. We understand that this paper can be
subjected to various criticism and we appreciate constructive and
reasonable questions and comments. It is likely that some conclusions will
need to be reconsidered together with an extension of our knowledge.

Chapter Ten
270
Our results show that lampreys systematics are still very far from
perfect and requires teamwork of field biologists, ecologists,
morphologists and geneticists. The approach described in this paper,
allows explaining many aspects which could not be solved before such as
relations between migrating and nonmigrating lampreys, parasitic and
nonparasitic lampreys; spatialtemporal communication or fragmentation
(and its degree) between different freshwater systems, a role of one or
another form for reproductive success maintenance of one or another
assemblage.
Several questions such as development, energetics of ontogenesis,
growth, plastic features and counts of specimen, behavior on various
stages etc. remain untouched upon the paper. All of them need the detailed
consideration. And each of them contributes to the debates and
explanation of any result of lamprey life history, as well as intraspecific
diversity and speciation in Petromyzontidae.
Acknowledgments
The ideas presented in the paper would never appear without grounds
given to us by Ksenia A. Savvaitova who dedicated her life to the
interspecific diversity in fishes. The longstanding observations would not
be possible without help of our numerous colleagues from the Moscow
State University, Russian Academy of Sciences, Institute of Fisheries and
Oceanology, different zoological Museums and Universities. We are sorry
not to identify the names but the list of personalities would take too much
space. We hope, all of you know how appreciated we are.
This work financial supported by the Russian Science Foundation,
projects no 14-14-01171 and the Program for Basic Research of the
Presidium of the Russian Academy of Sciences Basic Research in the
Interests for the Russian Arctic Zone.
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