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CommonBehavioralAdaptationsinLamprey
andSalmonids
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CHAPTER TWENTY THREE
COMMON BEHAVIORAL ADAPTATIONS
IN LAMPREY AND SALMONIDS
ELIZAVETA KIRILLOVA, PAVEL KIRILLOV,
ALEXANDR KUCHERYAVYY
AND DMITRY PAVLOV
Introduction
Quite often among representatives of different taxa which inhabit
similar environments, identical adaptations to external conditions in an
evolution process are formed. Berg (1935) noted ecological similarity
(ecological parallelism) of lamprey (Petromyzontidae) and salmon
fishes (Salmonidae) in a case study of European river lamprey Lampetra
fluviatilis, bull trout Salmo trutta and Atlantic salmon S. salar.
Subsequently, the ecological similarity was demonstrated in other
lampreys and Salmonid species which inhabit the same water bodies
including: Arctic lamprey Lethenteron camtschaticum, Pacific salmon of
the genus Oncorhynchus, chars of the genus Salvelinus, and Kamchatka
rainbow trout O. mykiss (Gritsenko 1968; Savvaitova et al. 2007). The
similar features between lamprey and salmonid ecology include: the
presence of various life forms within particular populations, realization of
particular life cycle stages in marine or fresh water and the usage of
identical spawning grounds.
Abakumov (1960) suggests that the ecological similarity between
lamprey and Salmonids arises because of parasitic lifestyle of the former
and the resulting adaptation to the host life cycle. He showed similar
dynamics of lamprey and salmonids abundance in particular water bodies
as basis of this statement. At the same time, lamprey inhabit some water
bodies where they express a resident form only and do not feed after
metamorphosis. Gritsenko (1968) further analyzed interrelations between
lamprey and salmonids at different life cycle stages: from egg development to
Common Behavioral Adaptations in Lamprey and Salmonids
197
feeding and spawning migrations. He concluded that lamprey and salmon
do not significantly influence each other. Gross et al. (1988) described
another compelling hypothesis of aquatic productivity and the evolution of
diadromous fish migration.
Frequently, researchers assign particular phases (spawning and
spawning migration) to the life cycle for comparison of ecological and
behavioral features of lamprey and salmon. However, it is necessary to
note that feeding migrations precede spawning migrations of anadromous
species (Schmidt 1946, Hitch et al. 2006). Feeding migrations occur in the
form of a downstream migration for anadromous species including
lamprey and salmon.
It is known that migrations which takes place in the early phases of
development, are a bottle-neck to survival. As abundance is determined
during this phase (Nikolsky 1974; Pavlov 1979; Pavlov et al. 2007, 2010,
2011). Change of habitat through migration requires increased energy
expenditure by the organism which renders it more vulnerable. Therefore,
it is assumed that similar adaptations will result for successful feeding
migrations of species which differ taxonomically, but inhabit similar
conditions.
Feeding migrations of lamprey and salmon begin in the form of a
downstream migration. The downstream migrations occur in juvenile fish
and lampreys moving downstream and represent the adaptation directed to
dispersion and optimization of usage of trophic resources (Nikolsky 1974;
Pavlov et al. 2004, 2007). This might result in dispersion within river
systems; moving from river to sea, i.e. to different ecological conditions;
or in both of these cases during different life cycle phases. Lamprey and
salmon which make downstream migrations exhibit various morphological
and biological characteristics, and can be at different developmental stages
or physiological states. Physiological changes (smoltification in salmon,
for example) can precede transferring to migratory state.
General patterns have been investigated and some mechanisms of
downstream migrations have been revealed in the study of Arctic lamprey
Lethenteron camtschaticum ammocoetes and salmonid juveniles of the
genera Oncorhynchus and Salvelinus in water bodies of the Kamchatka
Peninsula in the Russian Far East. We show that downstream migration
represents a common behavioral adaptation for distribution and optimum
usage of trophic resources even for such different groups of animals.
Chapter Twenty Three
198
Material and Methods
The data for this study were collected from 20042007 on the Utkholok
and Kalkaveyem Rivers on the Northwest of Kamchatka Peninsula.
Two methods were applied to study Arctic lamprey ammocoetes and
Salmonid juvenile downstream migration, and for determining seasonal
and diel patterns. A cone net was used for the capture of ammocoetes and
salmonid young-of-the-year (YOY). The net was made of 1.41 mm
diameter mesh, with inlet area of 0.43 m
2
and length of 2.38 m. The net
was set mid-stream in the river at the end of straight section of river
channel.
During the examination of diel patterns of downstream migration,
samples were collected round-the-clock every two hours, on even hours.
To further investigate the seasonality of downstream migrations, night-
time collections of ammocoetes were made periodically during collection
of icthyoplankton.The net was deployed in the mid-channel flow for 530
minutes, with exposure time depending on flow rate and water turbidity.
The intensity of ammocoete and YOY salmonids downstream migration
was estimated based on migrating individuals number by water volume
(ind. / 100 m
3
). For this calculation, flow rate was measured at the cone
net inlet and in-river at the deployment site. The formula for ammocoete
and YOY salmonids concentration (C) in water is as follows:
f
kV
n
C
100
,
where n is the number of individuals, which have been found in the
ichthyoplankton net per exposure time, ind.;
SvtV
out
; k
f
filtration
factor of ichthyoplankton net;
in
out
f
v
v
k
; t is ichthyoplankton net
exposition value, sec.; v
out
is flow rate in ichthyoplankton net setting place,
m/s; v
in
is flow rate in ichthyoplankton net opening, m/s; S is area of
ichthyoplankton net opening, m
2
.
Salmon juveniles of the second and subsequent years of life were
captured by a stationary trap, i.e. a fyke-net. The diameter of the fyke-net
capture hoop was 1 m, length was 4 m, inlet diameter in the hoop was 0.3
m, wings mesh was 10 × 10 mm and of bag 7 × 7 mm, wing-span was 22
m. Fyke-nets were set in the mouth of the Kalkaveyem River and in a side
channel of the Utkholok River, upstream of the confluence of Kalkaveyem
River.
Common Behavioral Adaptations in Lamprey and Salmonids
199
Both ammocoetes and salmonid juveniles may be divided into three
groups based on features of their feeding migrations:
1. Lamprey ammocoetes and YOY salmonids, i.e. individuals which
are dispersed from spawning areas to rearing places within the natal
river system or which migrate (in salmonid only) to sea soon after
emergence from redds;
2. Lamprey ammocoetes and salmon parr of various age groups (1+
and older) which make feeding migrations within the river;
3. Lamprey and salmon smolts 1+ and older which undergo
physiological transformations and migrate to sea to forage.
Seasonal patterns of downstream migration in older age classes of
juveniles were investigated by regularly sampling with night surveys from
22:00 to 05:00 (concurrent with YOY salmonids and ammocoete
sampling). The greatest mass downstream migration of almost all juvenile
Salmonid species was observed at this particular time. Round-the-clock
sampling data has confirmed that downstream migrations were less intense
during the daytime than at dusk-night time. Night surveys were made
every other day during the most intense downstream migration season
(MayJune). The gap between night surveys was been increased to
intervals of two, then four days, as downstream migration intensity
diminished. Additional night surveys were made when sudden changes of
environment abiotic parameters occurred (heavy rain, flood, moonlit or
cloudy dark night etc.).
Local surveys were made in various river systems with electrofishing
(voltage of 600700 V, frequency of 6070 Hz), a minnow seine, and dip
nets for the assessment of ammocoete and salmonid juvenile distribution
within the river basin. Species composition of fishes and lampreys, and
also their morphological characteristics were estimated in various habitats.
Results and Discussion
Migrations of Arctic lamprey (ammocoetes of different age groups)
and feeding migration of salmonid juveniles took place during the spring
autumn season (from May till October).
Migration of YOY ammocoetes and salmonids
Ammocoetes disperse within the river system soon after emergence
from ground. Among salmon, YOY coho salmon, Oncorhynchus kisutch,
and rainbow trout O. mykiss distribute within riverine habitats (Pavlov et
al. 2008; Kirillova et al. 2011); juvenile pink salmon, O. gorbuscha, and
Chapter Twenty Three
200
chum salmon O. keta, migrate to the sea. Despite different extension of
feeding migration for these species at specific life cycle stage, there are
several common patterns.
These feeding migrations have restricted time frames (Figure 231)
and involve a great amount of individuals. Concentrations of ammocoetes
reach thousands of individuals per 100 m
3
, while salmon juvenile
abundance reaches hundreds individuals per 100 m
3
(Pavlov et al. 2010;
Kirillova et al. 2011). Lamprey ammocoetes, coho salmon and rainbow
trout disperse within the river system in short time frames from several
days up to 24 weeks. Pink salmon migration to the sea occurs for longer
time up to 1.5 months. Chum salmon juveniles have two strategies of
migration pink salmon-like and coho salmon-like as described by
Gritsenko (1987) and Pavlov et al. (2008). The first ones migrate seaward
soon after emergence from redds. They do not feed in the river and most
of them have externally visible yolk sack. The second ones spend several
weeks in the river until they migrate to sea. They feed intensively and
grow significantly. Migrational behavior within the groups is different.
Representatives of pink salmon-like group avoid light and hide in
various shelters during the day time. They migrate downstream in the
darkest time of the day, drifting with river flow. Coho salmon-like chum
salmon are active both in the light and dark time of the day. They gather in
the schools and stay in the open water at shallow river curves feeding on
insects. Their downstream migration is predominantly active. Only the
first group of salmonid migrants demonstrate the special similarity of
feeding migration patterns to YOY ammocoetes.
Every year, downstream migrations both in ammocoetes and
salmonids begin at a time that varies slightly from year to year, depending
on phenological conditions. Migration intensity depends on in-river
hydrological conditions such as sudden flooding. Perhaps water
temperature does not directly influence the intensity of migration, but does
define migration initiation as it is a critical factor in development
(Gritsenko, 1987; Pavlov et al., 2008). Here, we illustrate seasonal
migration patterns for ammocoetes in the Utkholok and Kalkaveyem
Rivers in years with differing hydrological conditions (without separation
into age groups) (Figure 232).
Figure 231 (next page). Seasonal pattern of downstream migration for YOYs of
ammocoetes (1) and salmons: (2 pink salmon, 3 chum salmon, 4 coho
salmon, 5 rainbow trout) in Kalkaveyem River (I) and Utkholok River (II), 2006.
C_a ammocoetes concentration in water stream (ind./100 m
3
), C_s
concentration of salmon YOYs in water stream (ind./100 m
3
).
Common Behavioral Adaptations in Lamprey and Salmonids
201
Chapter Twenty Three
202
Figure 232. Seasonal pattern for ammocoetes downstream migration - c, ind./100
m
3
(1), for temperature - t, C (2), for water line - l, sm (3), in Kalkaveyem river (I)
and Utkholok River (II). a 2004, b 2005, 2006.
Migration of ammocoetes and salmon YOY primarily takes place
during the night-time at illuminance of less than 1 Lx: beginning at
twilight and ending at dawn (Figure 233). Diel downstream migration is
demonstrated only in chum salmon juveniles belonging to the coho salmon-
Common Behavioral Adaptations in Lamprey and Salmonids
203
Figure 233. Downstream migration diel pattern of ammocoetes (1) and salmon
YOYs pink salmon (2), chum salmon (3), rainbow trout (4) YOYs in connection
with illuminance (5) in Kalkaveyem River, June, 13 (a) and July, 23 (b) 2005. C_a
ammocoetes concentration in water stream, ind./100 m
3
, C_s concentration of
salmon YOYs in water stream, ind./100 m
3
, I illuminance, Lx.
Chapter Twenty Three
204
like group which stay in the river for a while before their seaward
migration. This mechanism of downstream migration is typical for early
ontogenetic stages of juvenile fish of various species (alevins and fry) for
which the vision is the leading mechanism for orientation in the river
(Hoar 1958; Ali & Hoar 1959; Pavlov, 1970a, 1979; Pavlov et al. 1999).
As soon as ambient illuminance drops below threshold values for
optomotor reaction, juvenile fishes lose visual reference points and are
carried instead by instream flow. This downstream migration mechanism
provides protection for juveniles against predatation (mainly by larger
salmon juveniles) (Hoar 1958; Pavlov, 1970a). Chum salmon have a more
complex mechanism of downstream migration initialization. Chum salmon
fry (pink salmon-like type) emerge into the instream flow under
conditions of visual orientation loss when illuminance drops below
threshold value (Hoar 1958; Ali & Hoar, 1959 etc.). Illuminance threshold
values for optomotor reaction increase concurrently with juvenile growth.
Additionally, the older juveniles orient themselves in the instream flow not
only by use of eyesight, but also at the by use of other sense organs
including touch, lateral line, and equilibrium (Dijgkraaf 1962; Pavlov
1970b; Harden & Jones 1968; Pavlov & Tyuryukov 1986, 1988, 1993).
Chum salmon orientation during night-time hours improves as juveniles
grow and results in an intensity decrease for nighttime downstream
migrations (Pavlov et al. 2010). The increased intensity of diel migrations
is associated with exhibition of other downstream migration mechanisms.
In fact, downstream migration of grown in the river chum salmon from
coho salmon-like group is initiated by mechanisms which are inherent
for older juveniles start to predominate (Pavlov et al. 2010). Reduction of
feeding areas at summer mean water and interspecific competition for food
make chum salmon migrating seaward.
YOY ammocoete eyes are underdeveloped relative to salmonid
species, though they are capable of discriminating changes in illuminance.
Therefore, their mechanism of downstream migration initiation differs
from that of salmonid juveniles. As it gets dark, ammocoetes make
bursting movements to the water surface. This movement gets them away
from the ground and involve in the current (Kirillova et al. 2011).
Clearly, migration of this group of ammocoetes and Salmonid YOY
(except for coho salmon-like chum salmon) is passive. This allows them
to preserve their small energy reserves that are critical for as-yet non
feeding young fishes (Kanidiev & Levanidov 1968).
Common Behavioral Adaptations in Lamprey and Salmonids
205
Migrations of older age groups within the river basin
Lamprey ammocoetes of various age groups and salmon parr of 1+ and
older age groups that make feeding migrations within the river, are very
diverse in biological characteristics and age composition. These organisms
make repeated migrations within the river system to disperse within water
body for optimal exploitation of food resources. These migrations take
place from early spring to late fall. These migrations are distinct from that
of younger juveniles in that they are observed in both upstream and
downstream directions.
This group of salmon juveniles includes parr (juveniles in the river
phase of life) of coho salmon, cherry salmon, rainbow trout, Dolly Varden
char and white-spotted char (Pavlov et al. 2008, Pavlov et al. 2011).
Ammocoetes are represented by various-aged individuals both pre- and
post- metamorphosis (Kirillova et al. 2011).
Comparison of downstream migration intensity is improper due to
variation in capture methods for ammocoetes and larger salmon juveniles.
Also it is impossible to estimate the scale of upstream migrations.
However, available data does allow us to present qualitative characteristics
of the upstream migration process.
In seasonal patterns of ammocoetes downstream migration, it is
possible to distinguish three phases of different migratory activity which
correspond to habitat redistribution (Kirillova et. al 2011): spring (May
June), summer (July) and autumn (AugustSeptember). In the spring
phase, migrants are predominantly one- and two-year olds; in the summer
phase, a massive migration of new-generation ammocoetes takes place;
subsequently in the autumn phase, four- and five-year old individuals
(including metamorphic ones) migrate most intensely.
The concentration of older ammocoetes migrating downstream is
generally insignificant in comparison with the concentration of young-of-
the-year ammocoetes at during the preliminary migration phase (Figure
232, 234); their concentration did not exceed 10 ind./100 m
3
.
As mentioned previously, salmon juveniles migrate within the river
system from early spring through late fall, i.e. the entire phase when water
temperature allows fish juveniles to feed (above 23 ) (Chebanova
2002). Water level fluctuations indirectly influence parr migration
intensity: feeding habitat decreases as secondary channels and creeks dry
up. Because of this, fish juveniles are forced to leave secondary habitats
(side channels, brooks, abandoned channels) and move to large tributaries
and main channel. It appears that these changes trigger parr migrations. In
addition, both ammocoetes and salmon juveniles leave those parts of rivers
Chapter Twenty Three
206
where spawning areas are located in season of mass spawning of Pacific
salmon Oncorhynchus (in JulySeptember) when there is intensive benthic
disturbance.
Figure 234. Downstream migration seasonal pattern of ammocoetes (1) and parrs
of salmon old ages groups (rainbow trout 2, coho salmon 3, cherry salmons
4, white-spotted char 5, Dolly Varden 6) age groups 1 + and older. S
downstream migration intensity of salmon juveniles, spec. / night, A downstream
migration intensity of ammocoetes, ind. / 100 m3.
It is necessary to note the importance of salmonid spawning season in
relation to the migration initiation in salmon parr and ammocoetes. During
this time, the salmon juveniles stay close to spawning areas since they feed
on eggs which have been washed out of redds (Pavlov et al. 2011).
Ammocoetes, by contrast, feed on the decaying tissue of salmon that die
Common Behavioral Adaptations in Lamprey and Salmonids
207
after spawning (Kucheryavy 2010). At this period salmon parrs migrate
both downstream and upstream from various rearing areas of the river to
spawning grounds to feed on eggs. It might be supposed that ammocoetes
also concentrate at salmon spawning grounds at this time. Salmonid eggs
and carcasses due to their high nutrition (Bogatov, 1994) support salmonid
juveniles and ammocoetes with energy that is important for further
survival in winter (Lund et al., 2003) and might play an important role in
choice of life strategy (Kucheryavy et al., 2010). Various aged
ammocoetes, as well as salmon parr can move both downstream and
upstream. It proves to be true that large ammocoetes (body length of 87
216 mm that corresponds to age 2 + and older, up to metamorphic
individuals) are found in Mysmont river middle course (second order
tributary of Utkholok River), considerably (510 km) upstream of
previously documented spawning areas (Kirillova et al. 2011). Results of
examinations on other species confirm the possibility of additional
lamprey upstream dispersion (Sugiyama & Goto 2002; Quintella et al.
2003, 2005)
Despite the similarity in seasonal downstream migration pattern in
ammocoetes and salmon parr, their diel migration patterns differ. Salmon
parr migrate both at night and during the day, while ammocoetes migrate
only at night. Depending on the species, salmon juvenile migration can be
most intense in the evening or morning twilight (rainbow trout, coho
salmon), or in the afternoon (cherry salmon). Migration intensity and
confinement to a certain time of day in salmonids is defined by feeding
and defensive behavior (Pavlov et al. 2011).
Seaward migration
Lamprey and salmon smolts of 1+ and older age groups is the special
group for which migration is directed to habitat change from freshwater to
marine, which includes significant morphological and physiological
transformations (i.e. smoltification). In outward appearance the smoltification
process manifests as a change to a silvery pelagic coloration both for
salmonid fish and for lampreys. External changes are accompanied by a
physiological transformation which allows the organism to survive in sea
water.
The migration patterns of salmonid smolts of various species has been
well studied, and numerous studies have been devoted to various aspects
of this phenomenon (Quinn 2005; Pavlov et al. 2008, Shuntov & Temnykh
2008; Pavlov et al. 2011). Downstream migration of smolt to the sea takes
place in the season when conditions for this are optimal, both in a river
Chapter Twenty Three
208
and in the sea (Saunders & Bailey 1980). It is well demonstrated that this
statement also is true of lamprey. Therefore, seaward migration is strictly
time-limited and is generally invariable from year to year. Some
insignificant variations are associated with discrete phenological features
of a specific year.
In a case study of salmon smolts in the Utkholok River, we elucidate
specific terms of seaward migration in a variety of species: firstly, Dolly
Varden migrate downstream to the sea, followed closely, if not
simultaneously by coho salmon. Unlike Dolly Varden, coho salmon
downstream migration is longer. Corresponding with the end of the coho
salmon downstream migration, the white-spotted char presence in the
migratory group increases. The white-spotted char abundance is then
replaced by rainbow trout and cherry salmon. In the Utkholok River, coho
salmon migration duration is approximately 2.5 months, rainbow trout
migration lasts 2 months, cherry salmon migration lasts 1 month; Dolly
Varden char and white-spotted char downstream migration usually does
not last longer than than 1.5 months (Figures 235 and 236).
Figure 235. Downstream migration intensity of salmon juveniles and
ammocoetes at various stages of life cycle.
Arctic lamprey metamorphosed juveniles preparing for or migrating to
the sea which we label as smolts (after Sidorov & Pichugin 2005), are
captured in samples beginning in the final third of June and persist until
the middle of October. However, it is impossible to discuss concrete
features of downstream migration of arctic lamprey since the available
data is based on a collection method that the juveniles can avoid due their
Common Behavioral Adaptations in Lamprey and Salmonids
209
Figure 236. Seasonal (spring to autumn) patterns of intensity of salmon juveniles
and ammocoetes downstream migration at different stages of life cycle.
Chapter Twenty Three
210
ability to swim upstream against strong currents. Therefore, the collected
data are rather qualitative. Quite often lamprey smolts were captured
during electrofishing samples at eroding riverbanks, among exposed roots
and other vegetation. It is possible to deduce that lamprey smolts select
these habitats during the day time where the soft substrate and
overhanging banks protect them from bright light.
Comparison of downstream migration patterns for foraging, has shown
that salmon juveniles and Arctic lamprey ammocoetes have a series of
analogous patterns. The preliminary migration of YOY fishes, dispersion
of older age individuals within the river system, and seaward run of smolts
all occur as downstream migrations (Savvaitova et al. 2007; Pavlov et al.
2008, 2010, 2011). All these movements previously described, represent
an adaptation to foraging resources and optimum usage of habitats. The
scale of feeding migration vary among species and years. From year to
year, the triggers for the beginning, duration and downstream migration
intensity are defined by ecological factors such as water temperature and
water level. Ammocoetes and salmonids that make downstream migration,
form the migratory part of the aquatic vertebrate community in the river
(Pavlov et. al. 2008). Numerous similarities in pattern and mechanism of
the initialization of downstream migrations are a clear example of
behavioral adaptations for phylogenetically distinct groups of organisms
which inhabit similar environments.
Acknowledgments
Material treatment and analysis are executed by financial support of
grant RNF 14-14-01171 and Wildlife Basic Researches Program of
Russian Academy of Sciences Presidium. Authors express sincere
appreciation to colleagues who were directly involved in the field
observations and samples collection: M.A. Gruzdeva, M.Yu. Pichugin,
O.P. Pustovit, A.M. Thompson, and also to volunteers, students and
technical staff of field camps.
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