Download Life cycles of two limnetic cyclopoid copepods

Journal of Plankton Research Vol.20 no.6 pp.1073-1086, 1998
Life cycles of two limnetic cyclopoid copepods, Cyclops vicinus
and Thermocyclops crassus, in two different habitats
Toru Kobari and Syuhei Ban
Biological Oceanography, Faculty of Fisheries, Hokkaido University, 3-1-1
Minato-machi, Hakodate, Hokkaido 041-08-1, Japan
Abstract. The life cycles of Cyclops vicinus and Thermocyclops crassus in two shallow eutrophic
habitats, Junsainuma and Naganuma Ponds, Hokkaido, Japan, were investigated. Both ponds
exhibited similar seasonal patterns of temperature, oxygen levels and pH during ice-free periods;
however, oxygen levels were extremely lower under the ice in Naganuma Pond. Cyclops vicinus
showed different life cycles in the two ponds; in Junsainuma Pond, it reproduced in winter and spring
(January-May) and entered diapause during summer and autumn (June-October) as copepodite IV
stage, while it reproduced in autumn (October-November) and spring (April-May), and entered
diapause in summer (June-September) and winter (January and February) as copepodite V stage in
Naganuma Pond. Thermocyclops crassus entered diapause during winter (December-April) as copepodite IV and V stages in both ponds, and egg-bearing females appeared only during the warm season,
from early May to late October, when water temperatures were >10°C. Summer diapause in C.vicinus
was suggested to be an adaptation against fish predation, whereas C.vicinus entered winter diapause
in Naganuma Pond probably to avoid low oxygen levels. Thermocyclops crassus entered diapause in
both ponds to avoid low water temperature. These results suggest that biotic and abiotic factors are
important for leading to specific life cycles of cyclopoid copepods in small water bodies. -
Introduction
Some cyclopoid copepods have a dormant phase in their life cycle that seems
fundamentally identical to diapause in insects (Elgmork, 1980). The life cycle of
many cyclopoid copepods includes a diapause stage when they sink to the bottom,
burrow into the sediment, and cease development and activity (Elgmork, 1980).
Diapause is considered to be a strategy to avoid unfavorable conditions and to
reproduce under optimal conditions (Elgmork, 1980). It has been shown that
diapause allows cyclopoid copepods to avoid unfavorable biotic factors such as
fish predation (George, 1976; Nilssen and Elgmork, 1977; Maier, 1989a) and
competition with highly efficient filter feeders (Santer and van den Bosch, 1994;
Santer and Lampert, 1995), as well as abiotic factors such as anoxia (Elgmork,
1959), low temperatures (Maier, 1989b) and desiccation (Wyngaard et al, 1991;
Maier, 1992). Elgmork (1980) pointed out that biotic factors are of major importance in large water bodies that are well buffered, but abiotic factors are often
major forces leading to specific life history strategies in some small water bodies.
Cyclops vicinus and Thermocyclops crassus are common planktonic species in
freshwater lakes and ponds. Marked variations in their life cycles have been
observed among different waters. Cyclops vicinus generally disappears from the
water column in summer (Einsle, 1967; Vijverberg, 1977; Kawabata, 1989; Maier,
1989a; Santer and Lampert, 1995) and T.crassus in winter (Maier, 1989b) when
they enter diapause. In some lakes, however, C.vicinus occurs in the water column
throughout the year (George, 1976; Maier, 1989a; Hansen and Jeppesen, 1992).
Variations in life cycles are considered to be a result of different biotic factors,
© Oxford University Press
1073
T.Kobari and S.Ban
such as predation by planktivorous fish and competition with cladocerans, like
Daphnia, or abiotic factors such as the water temperature regime. Recently, it has
been reported that biotic factors are of major importance in lakes (Santer and
Lampert, 1995), but there are few detailed studies of the relationship between
abiotic factors and the diapause of these animals in small water bodies (Elgmork,
1959; Maier, 1989b, 1992; Wyngaard et al, 1991).
In this study, we investigated the life cycles of two dominant cyclopoid copepods, Cvicinus and T.crassus, and several environmental factors in two small
eutrophic habitats to discuss the importance of abiotic and biotic factors for
leading to specific life cycles in small water bodies.
Study area
Both ponds (Junsainuma and Naganuma) are situated near Lake Ohnuma on the
Oshima Peninsula in southwestern Hokkaido, Japan (Figure 1). The surface areas
and maximum depths are 0.66 km2 and 4.6 m in Junsainuma Pond (Hokkaido
Research Institute for Environmental Pollution, 1990), and 0.07 km2 and 2.5 m in
Naganuma Pond (authors' unpublished data), respectively. During the ice-free
period from 31 May to 1 December 1994 and from 20 April to 27 June 1995, both
ponds were partly covered with floating-leaved macrophytes along the shore.
Both ponds are meso- to eutrophic. The maximum chlorophyll a concentrations
in Junsainuma and Naganuma Ponds were 20.8 and 51.9 jxg I"1, respectively (see
Figure 3). Oxygen levels near the bottom during the warm season can fall to 1.8
and 0.4 ml I"1 in Junsainuma and Naganuma Ponds, respectively (see Figure 2).
Annual mean concentrations of total phosphorus, nitrogen and chemical oxygen
demand (COD) were 0.033,0.41 and 3.9 mg I"1, respectively, in Junsainuma Pond
(Hokkaido Research Institute for Environmental Pollution, 1990), although no
data on nutrient concentrations are available for Naganuma Pond.
Method
Zooplankton and sediment samples were taken at weekly intervals from 31 May
1994 to 27 June 1995 and twice during the ice-covered period from early December 1994 to mid-April 1995. Zooplankton samples were collected with a 5 1 Van
Dorn bottle from three different depths (0, 2 and 4 m in Junsainuma Pond; 0, 1
and 2 m in Naganuma Pond) at stations J1-J3 (bottom depth -4.5 m) and N1-N3
(bottom depth -2.5 m) (Figure 1). All stations were free of macrophytes. Each
sample was concentrated with a 50 )tm mesh net and preserved with 4%
sucrose-formalin.
To collect diapausing cyclopoid copepods, sediment samples were taken with
an Ekman-Birge grab sampler (15 x 15 cm) or a Kajak-type core sampler (inner
diameter 4.4 cm) at J1-J3 and N1-N3. To collect diapausing instars in littoral
areas, sediment samples were also taken with the Ekman-Birge grab sampler
from 17 October 1994 to 27 June 1995 at stations J4-J6 (4,3 and 2 m deep, respectively) in Junsainuma Pond and N4-N6 (2, 1.5 and 1 m deep, respectively) in
Naganuma Pond where the pond surface was covered by macrophytes.
1074
Life cycles of C.vicinus and T.crassus
Naganuma Pond
Junsainuma Pond ,
J6
500 m
\
Fig. 1. Location of Junsainuma and Naganuma Ponds, and the sampling stations.
All zooplankton samples were pooled in each pond, i.e. the water volume
sampled was 451, and cyclopoid copepods were counted under a dissecting microscope until at least 100 individuals of each developmental stage for each species
were counted. The whole sample was analyzed if <100 individuals of each
developmental stage were counted. Naupliar stages of all cyclopoids and the
copepodite I and II stages except for C.vicinus were pooled since different species
could not be distinguished. Diapausing individuals of C.vicinus and T.crassus
1075
T.Kobari and S.Ban
were isolated from the pooled sediment samples in each pond by the sugar-flotation method (Onbe, 1978) and counted under a dissecting microscope. Rotifers
in the zooplankton samples were also counted with a Sedgewick-Rafter chamber
under an inverted microscope, since they are potential prey for older copepodite
and adult stages of cyclopoid copepods (Zdnkai, 1984; Papinska, 1985; Adrian
and Frost, 1993).
Water samples for measuring dissolved oxygen, pH and chlorophyll a concentrations were taken with a 51 Van Dorn bottle at the surface and near the bottom
at stations J2 and N2 (Figure 1) on each sampling date. Water temperature was
measured with a mercury thermometer immediately after water samples were
collected. pH was measured with a pH meter (Hitachi-Horiba H-7LD). Dissolved
oxygen was measured using the Winkler method. To measure the size-fractionated chlorophyll a concentrations, 250 ml of pond water were filtered in sequence
through a 20 \xm mesh net, a 2 um pore size Nuclepore filter and a Whatman GF/F
filter. Chlorophyll from phytoplankton on the net and the filters was extracted
with 90% acetone, and the chlorophyll a was measured using a Turner Designs
fluorometer (Wetzel and Likens, 1991). Mean chlorophyll a concentrations of
three size classes, <2 p.m, 2-20 u.m and >20 u,m, were calculated from the values
at the surface and near the bottom. Both nauplii and copepodites of cyclopoid
copepods effectively collected nano-size particles (Horn, 1981; Toth and Zankai,
1985; Adrian, 1987; T6th et ai, 1987). Therefore, chlorophyll a of the 2-20 jim
size fraction was regarded as an indicator of edible phytoplankton biomass,
although recently Santer and van den Bosch (1994) revealed that not only size,
but also the features of the algae, like motility, determine the food quality.
Results
The seasonal changes in water temperature in both ponds showed similar patterns
(Figure 2). Surface water temperatures were >18°C in June 1994 and reached
>25°C in August 1994. Bottom water temperatures were only slightly lower than
surface temperatures, and were often the same from June to August 1994 due to
the shallow depths of the ponds and wind-induced mixing. From August to
November 1994, temperatures were the same at both the surface and the bottom,
and no stratification occurred. In December 1994, surface and bottom temperatures decreased to 5°C. Both ponds were covered with ice and snow from early
December 1994 to mid-April 1995, and water temperatures near the bottom were
2 and 3°C on 26 January and 13 February 1995, respectively. After the ice break,
water temperatures gradually increased to 15°C in May 1995.
The percentage saturation of dissolved oxygen was >80% in early June 1994
and decreased from mid-June to September 1994 in both ponds; it occasionally
decreased to lower levels during summer months, particularly in Naganuma Pond
(Figure 2). The dissolved oxygen levels measured using the Winkler method can
be under- or overestimated by the presence of substances such as sulfide, organic
matter and suspended materials (Kitano, 1964; Wetzel and Likens, 1991). There
were many suspended materials in both ponds and a strong hydrogen sulfide
smell at both ponds during the summer months and even in winter (author's
1076
life cycles of C.vicinus and T.crassus
Junsainuma Pond
Naganuma Pond
5.5
J J A S O N D J F M A M J
1994
1995
J
J A S O N O J F M A M J
1994
1995
Fig. 2. Seasonal changes in water temperature, dissolved oxygen saturation and pH at the surface
(solid lines) and near the bottom (broken lines) in Junsainuma (left panels) and Naganuma (right
panels) Ponds between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered
period. Dotted lines represent discontinuous sampling period.
unpublished data). The low values of dissolved oxygen observed in Junsainuma
and Naganuma Ponds may have been influenced by these substances in the water
in summer. On 27 January and 13 February 1995, dissolved oxygen was at an
undetectable low level at both the surface and near the bottom in Naganuma
Pond, but relatively high (>40%) in Junsainuma Pond. After the ice break,
dissolved oxygen was >70% in April-June 1995 in both ponds.
The pH in Naganuma Pond was usually higher than in Junsainuma Pond; it
varied between 5.9 and 7.6 in Junsainuma Pond, and between 6.6 and 7.5 in
Naganuma Pond (Figure 2). The pH near the bottom was lower than at the
surface, particularly from June to September 1994 and from January to February
1995 in both ponds.
Chlorophyll a concentrations varied between 3.8 and 20.8 u.g I"1 in Junsainuma
Pond, and between 1.7 and 51.9 u.g I"1 in Naganuma Pond (Figure 3). The
maximum chlorophyll a concentration in Naganuma Pond was 2- to 3-fold higher
than in Junsainuma Pond. Chlorophyll a concentrations of edible-size phytoplankton were always high (Junsainuma Pond, >3 jig I"1; Naganuma Pond,
1077
T.Kobari and S.Ban
Junsainuma Pond
JZ
Naganuma Pond
r
a.—
2 »
2 a
u
3 -a
I
J J A S O N D J F M A M J
1994
1995
J J A S O N D J F M A M J
1994
1995
Fig. 3. Seasonal changes in mean chlorophyll a concentration of 2-20, <2 and >20 |im size classes at
the surface and near the bottom, and rotifer abundance, in Junsainuma (left panels) and Naganuma
(right panels) Ponds between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered
period. Dotted lines represent discontinuous sampling period.
>7 (Jig I"1) from July to September 1994 and from April to June 1995, but relatively low (Junsainuma Pond, 1.3-1.8 u.g H; Naganuma Pond, 3.5 u.g H) in midJune 1994 in both ponds. Under the ice, chlorophyll a concentrations in this size
class were very low (<2 p.g I"1) in both ponds.
Rotifers were always abundant (>106 ind. m~2) in both ponds during the icefree period (Figure 3). Abundances were extremely high from mid-May to late
June 1995, with maxima occurring on 31 May 1995 (24 X 106 ind. nr 2 ) in
Junsainuma Pond and on 17 May 1995 (74 X 106 ind. nr 2 ) in Naganuma Pond.
Five cyclopoid copepods, Cvicinus Uljanin, Eucyclops serrulatus Fischer,
Mesocyclops ruttneri Kiefer, T.crassus Fischer and Diacyclops bicuspidatus Claus,
occurred in both ponds. Cyclops vicinus and T.crassus were the dominant
cyclopoid species (Figure 4). Thermocyclops crassus occurred from June to
October 1994 and from April to June 1995 in both ponds, while Cvicinus was
present only for short periods: from November 1994 to June 1995 in Junsainuma
Pond, and from October to December 1994 and from April to June 1995 in
Naganuma Pond. Cyclops vicinus disappeared under the ice in Naganuma Pond
in January and February 1995 when the oxygen content was very low. The population densities of both copepods in Naganuma Pond were -10-fold higher than
in Junsainuma Pond. Although the remaining three species occurred in very low
abundance compared with Cvicinus and T.crassus, E.serrulatus and M.ruttneri
were present during the ice-free period in both ponds, and D.bicuspidatus was
found in February and May 1995 in Junsainuma Pond and from May to June 1995
in Naganuma Pond. Cyclopoid nauplii probably occurred throughout the study
period in Junsainuma Pond, but not in January and February 1995 in Naganuma
1078
Life cycles of C.vicinus and T.crassus
Naganuma Pond
Junsalnuma Pond
100
yf| Cyclops vlclnut
|
^
Thermocyclop* ermsua
Dtecyc/ops blcutpMttut, Eueyelops nmilatu* «nd Matocyclops rvttntl
Fig. 4. Seasonal changes in species composition (CIII to adult) (upper panels) and nauplii (lower
panels) of cyclopoid copepods in open water in Junsainuma (left panels) and Naganuma (right panels)
Ponds between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered period.
Dotted lines represent discontinuous sampling period. Note the different scale of left and right panels.
Pond (Figure 4). According to the seasonal succession of the cyclopoid species as
described above, the nauplii that occurred from June to October 1994 were
considered to be mainly T.crassus in both ponds. Nauplii of C.vicinus might have
occurred in April and May 1995 in both ponds, and in January-February 1995 in
Junsainuma Pond.
The life cycle of C.vicinus was different in the two ponds. Cyclops vicinus disappeared from the water column from mid-June to late October 1994 in Junsainuma
Pond and from mid-June to late September 1994 in Naganuma Pond (Figure 5).
It was found in the sediments as copepodite IV (CIV) and V (CV) stages during
these periods (Figure 6). It can be assumed that the copepods in the sediments
were diapausing, since they exhibited empty alimentary tracts and numerous
orange oil globules (Elgmork, 1959). The timing of the emergence from summer
diapause was a month later in Junsainuma Pond than in Naganuma Pond. In
Jansainuma Pond, no CVs or adults were found in the open water between
November and early December 1994 (Figure 5), but CVs were found in the sediments on the littoral area in early December 1994 (Figure 6). Although eggbearing females were not collected, the adults that developed from arousal CIVs
might have reproduced during winter, since nauplii (see Figure 4) and early copepodites occurred in this period (Figure 5). These early stages slowly developed
into the adults and might have reproduced in April 1995. No collection of eggbearing females may probably be attributed to extremely low density due to
selective predation by planktivorousfish,such as pond smelt, that live in the pond
1079
T.Kobari and S.Ban
Junsalnuma Pond
Naganuma Pond
12
CI
a
6
. /VS.
0
. ^T*.
CO
CD
5
\
0
1
cm
3
0
2
0
0
1
cv
cv
1
0
0.5
\
\
CIV
crv
0
Adult
Adult
0.5
0
0
J J A S O N D J F M A M J
1994
1995
/\ f
<T
o "
J J A S O N D J F M A M J
1994
1995
Fig. S. Seasonal changes in abundance of copepodite stages (solid lines) and egg stock (circles) of
Cvicinus in the water column in Junsainuma (left panels) and Naganuma (right panels) Ponds
between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered period. Dotted lines
represent discontinuous sampling period.
Junsainuma Pond
Naganuma Pond
20
10
Fig. 6. Seasonal changes in abundance of copepodite stages of Cvicinus in the sediments at deep area
(closed bars) and shallow littoral area (shaded bars) in Junsainuma (left panels) and Naganuma (right
panels) Ponds between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered
period. Note the different scale of left and right panels.
1080
Life cycles of C.vicinus and T.crassus
(Hokkaido Research Institute for Environmental Pollution, 1990). In Naganuma
Pond, adults that developed from arousal CVs started to reproduce until midOctober 1994, and early developmental stages occurred in the water column by
late October 1994 (Figure 5) when no diapause instars were collected from the
sediments (Figure 6). All developmental stages disappeared from the water
column on 27 January and 13 February 1995 under the anoxic conditions, but
CIVs and CVs (mainly CVs) were found in the sediments in the littoral areas of
Naganuma Pond (Figure 6). In late April 1995, all copepodite stages including
adults occurred again in the water column and the adults reproduced. In both
ponds, copepodites disappeared again from the water column by the end of June
1995.
The life cycle of T.crassus was similar between the two ponds, but the population densities in Naganuma Pond were higher than in Junsainuma Pond. All
copepodite stages were found in the water column from June to September 1994
and from late April to June 1995, when water temperatures were >10°C in both
ponds, and reproduction occurred during this period (Figure 7). Although copepodite I and II stages (CI and II) included four species, T.crassus, E.serrulatus,
M.ruttneri and D.bicuspidatus, these younger stages were mainly composed of
Junsainuma Pond
Naganuma Pond
200
CI
CI
100
0
j£
Cll
Cll
20
£ o
0
I 2
20
0
CIV
CIV
AA.
20
cv
0
>
20
cv
0.6
0
0.3
30
o"
o
Adult
3
J J A S O N D J F M A M J
1994
1995
^
E
60 S
Adult
30
^AJBS
o
6
J J A S O N D J F M A M J
1994
1995
Fig. 7. Seasonal changes in abundance of copepodite stages (solid lines) and egg stock (circles) of
T.crassus in the water column in Junsainuma (left panels) and Naganuma (right panels) Ponds
between 31 May 1994 and 27 June 1995. Copepodite I and II stage included Diacyclops bicuspidatus,
Eucyclops serrulatus and Mesocyclops ruttneri, but the proportion of these copepods may be small.
Horizontal bars indicate the ice-covered period. Dotted lines represent discontinuous sampling
period. Note the different scale of left and right panels.
1081
T.Kobari and S.Ban
T.crassus (see Figure 4). Three distinct population peaks in adults were found
from June to October 1994 in Junsainuma Pond. Since these peaks were followed
by peaks in the younger stages, at least three generations may have existed during
the warm season. In Naganuma Pond, the first peak was weak, the second peak
was distinct, and the third peak was found for stages younger than CIV. The third
peak in early copepodite stages in September 1994 developed to CIV and might
have entered diapause in October. All stages disappeared from the water column
between late November 1994 and April 1995 in both ponds. During this period,
CIVs and CVs with empty alimentary tracts and numerous transparent oil globules were found in the sediment, mainly in littoral areas, although the densities
of these copepods were low (Figure 8). After the ice break, these CIVs and CVs
may have developed into adults, and reproduced (Figure 7). In Junsainuma Pond,
diapausing instars were also found from the sediments in June and September
1994 when this species occurred in the water column, but in extremely low
numbers (Figure 8).
Discussion
In Junsainuma Pond, the abundance of adults and CVs of Cvicinus did not
increase in the water column in November when the number of diapausing individuals decreased in the sediments. Non-diapausing copepodites and adults were
sometimes present within 50 cm above the bottom surface (Elgmork, 1959),
where it is difficult to collect copepods with a Van Dorn bottle. Arousal CIVs and
CVs in Cvicinus may have remained on the sediments, which would have
prevented them from being collected from water samples in Junsainuma Pond.
Junsainuma Pond
Naganuma Pond
CIV
CIV
Ihn . n .
i . J hill . .
.a .
6.14
cv
cv
1
Fig. 8. Seasonal changes in abundance of each copepodite stage of T.crassus in the sediments at deep
area (closed bars) and shallow littoral area (shaded bars) in Junsainuma (left panels) and Naganuma
(right panels) Ponds between 31 May 1994 and 27 June 1995. Horizontal bars indicate the ice-covered
period.
1082
Life cycles of C.vicinus and T.crassus
The number of CVs (0.7 X 103 ind. m~2) found in the sediment samples in late
November was nearly identical to the density of the adults under the ice.
In this study, C.vicinus entered diapause in summer in both ponds as reported
in the literature (Einsle, 1967; Vijverberg, 1977; Kawabata, 1989; Santer and
Lampert, 1995). It is unlikely that abiotic factors are the ultimate reason for this
summer diapause. Reproduction of this species has been shown to occur above
20°C (Vijverberg, 1980; Maier, 1989c). Oxygen levels were sufficient for the copepods even near the bottom during this period in both ponds. Therefore, summer
diapause of this species is probably a strategy to avoid fish predation (George,
1976; Maier, 1989a) or competition with highly efficient filter feeders (Santer and
van den Bosch, 1994; Santer and Lampert, 1995). Santer and Lampert (1995)
suggested that C.vicinus enters diapause to avoid mortality during the naupliar
stages due to competition with Daphnia, which is an efficient filter feeder. In this
study, Bosmina longirostris was dominant, but Daphnia did not occur throughout
the study period in either pond (author's unpublished data). Bosmina longirostris
is a less efficient filter feeder than Daphnia (DeMott, 1982; DeMott and Kerfoot
1982). Santer and Lampert (1995) described that the disappearance of Cyclops
nauplii in late spring seemed to be related to the increment of Daphnia but not
other cladocerans including Bosmina. Chlorophyll a concentrations were relatively high during summer months in both ponds, although low levels of chlorophyll a of edible size (<1.5 u.g I"1) were found for a few weeks in mid-June in
Junsainuma Pond. Thus, competition with cladocerans may be a minor factor for
summer diapause of this species in the two ponds. On the other hand, planktivorous pond smelts (Shiraishi, 1960), Hypomesus transpacificus nipponensis,
occur in Junsainuma Pond (Hokkaido Research Institute for Environmental
Pollution, 1990) and were frequently observed at the shore of the pond (author's
unpublished data). Maier (1990) suggested that the diapause of C.vicinus in deep
areas could be a strategy to avoid fish predation. Diapausing individuals of
C.vicinus in Junsainuma Pond were very abundant at the deepest stations during
summer. Although no qualitative and quantitative data on fish and cladocerans
in Naganuma Pond are available, predation by pond smelts may be an important
factor for summer diapause of this species, at least in Junsainuma Pond.
In some small water bodies, abiotic factors, such as water temperature and
dissolved oxygen, are the major factors leading to specific life cycles (Elgmork,
1980). In Naganuma Pond, C.vicinus disappeared from the water column and
appeared from the sediments in littoral areas during the ice-covered period, while
the population in Junsainuma Pond occurred only in the water column. In this
period, the oxygen content in the water column was extremely low in Naganuma
Pond, but relatively high in Junsainuma Pond. This difference in oxygen
conditions may have led to the different features of occurrence in C.vicinus in the
two ponds. Wierzbicka and Kedzierski (1964) observed that anaerobic conditions
induced diapause of C.vicinus in the laboratory. Elgmork (1959) reported that
Cyclops strenuus entered diapause in winter to avoid lack of oxygen. Watson and
Smallman (1971) found that diapausing individuals of Diacyclops navus could
tolerate anoxic conditions for long periods, especially at low temperatures. CVs
of C.vicinus in the littoral sediments showed the features of diapausing
1083
T.Kobari and S.Ban
individuals described above (see Results). Thus, these individuals in the sediments are considered to be diapausing to avoid the extremely low oxygen
conditions in the water column.
The difference in timing of emergence from the summer diapause between the
two ponds may support this hypothesis. Cyclops vicinus emerged from its diapause
in October in Naganuma Pond, a month earlier than in Junsainuma Pond. According to the ambient water temperature from October to November 1994 in
Naganuma Pond and Vijverberg's (1980) equation for predicting the development
time of Cvicinus, the development times from egg to adult were estimated to be
28-79 days. This indicates that Cvicinus produced by the females who develop
from arousal CVs can develop to CV before the pond water is covered with ice,
and suggests that C. vicinus in Naganuma Pond may have emerged from diapause
a month earlier in order to develop one generation and enter the diapause before
the pond water becomes anoxic. Because of no sampling in the littoral area in
summer and limited sampling during winter, however, it is possible that not all
copepodites emerged from the summer diapause, with part of the population
staying in the sediments during winter and emerging in spring.
In this species, the diapausing stage was also different in the two ponds. The
diapausing stage of Cvicinus is mainly CIV in Junsainuma Pond, as reported in
the literature (Einsle, 1967; Vijverberg, 1977; Kawabata, 1989; Maier, 1989a;
Santer and Lampert, 1995), but CV in Naganuma Pond. Diapausing as CV may
be more advantageous than CIV for reproduction quickly in favorable conditions.
Naess and Nilssen (1991a,b) suggested that diapause in the adult stage of
Cstrenuus is advantageous for reproduction immediately after emerging from
diapause. Thus, the diapausing stage and the timing at emergence from the
diapause may play an important role in optimizing the reproduction of cyclopoid
copepods.
In Nagamuna Pond, the population density of T.crassus was -10-fold higher
than in Junsainuma Pond. The egg stock in Naganuma Pond was ~2 orders higher
than in Junsainuma Pond. Water temperatures were very similar in the two ponds,
but edible phytoplankton and rotifers were always more abundant in Naganuma
Pond during the ice-free period. Increasing food availability increases egg
production (Whitehouse and Lewis, 1973). The survival of offspring is also highly
dependent on food conditions (Santer and van den Bosch, 1994; Santer and
Lampert, 1995). The predation pressure on T.crassus byfishis probably negligible
due to the small size of T.crassus. Therefore, food availability may be the major
factor affecting the population density of T.crassus in the two ponds.
Thermocyclops crassus disappeared from the water column and entered
diapause in the sediments during winter in both ponds. Winter diapause in this
species is unlikely to be related to low oxygen content, as is assumed for Cvicinus;
it also disappeared in Junsainuma Pond, where the oxygen content was high
under the ice. Maier (1989b) reported that T.crassus entered diapause in winter
and that egg production could be observed only when the water temperature was
>10°C in Gronne. In laboratory experiments, this species did not produce eggs
below 10°C (Maier, 1989c). In the present study, reproduction of T.crassus also
occurred at water temperatures >10°C in both ponds. This suggests that T.crassus
1084
Life cydes of C.vicinus and T.crassus
is adapted to the warm season, and winter diapause of this species may be a strategy to avoid low temperature. Water temperature may be an important factor
influencing the life cycle pattern of T.crassus.
The abundance of diapausing individuals of T.crassus was very low in both
ponds. Mortality was probably low in autumn when the copepods entered
diapause because the density of CIVs and CVs in the next spring was not lower
than the density of CIVs and CVs in October (see Figure 7). In the warm season,
food availability was high, and this species has been shown to be less heavily
preyed upon than other copepods byfish(Maier, 1989b). One explanation for the
small number of diapausing individuals is our failure to collect specimens from
the bottom sediments. In shallow littoral areas of the two ponds, the roots of the
macrophytes stretch into the bottom sediment. Thermocyclops crassus prefers
shallower areas as a diapausing habitat (Maier, 1990). Probably, all diapausing
individuals were not collected due to obstruction by the roots of the macrophytes,
although sediment samples were collected from shallow littoral areas.
In summary, the summer diapause in Cvicinus may be an adaptation to avoid
adverse biotic environmental conditions, at least in Junsainuma Pond, and winter
diapause of C.vicinus and T.crassus may be an adaptation to avoid low oxygen
levels and low water temperatures, respectively. Abiotic factors still appear to
play an important role for leading to specific life cycles of cyclopoid copepods in
small water bodies like Junsainuma and Naganuma Ponds.
Acknowledgements
We are grateful to Dr T.Minoda for helpful comments on the manuscript. We also
thank S.Sakai, A.Nakano, K.Nishiuchi, A.Yamaguchi and H.Lee for their assistance with our plankton sampling, and Dr J.R.Bower for correction of our English.
References
Adrian.R. (1987) Variety of phytoplankton in fecal pellets of two cyclopoid copepods. Arch.
Hydrobioi, 110, 321-330.
Adrian.R. and Frost.T.M. (1993) Omnivory in cyclopoid copepods: comparisons of algae and invertebrates as food for three, differently sized species. / Plankton Res., 15, 643-658.
DeMott.W.R. (1982) Feeding selectivities and relative ingestion rates of Daphnia and Bosmina.
Limnol. Oceanogr., 27,518-527.
DeMott.W.R. and Kerfoot.W.C. (1982) Competition among cladocerans: nature of the interaction
between Bosmina and Daphnia. Ecology, 63, 1949-1966.
Einsle.U. (1967) Die auBeren Bedingungen der Diapause planktisch lebender Cyclops-Anen. Arch.
Hydrobioi., 63, 387-403.
Elgmork.K. (1959) Seasonal occurrence of Cyclops slrenuus strenuus in relation to environment in
small water bodies in southern Norway. Folia'Limnol. Scand., 11, 1-196.
Elgmork.K. (1980) Evolutionary aspects of diapause in freshwater copepods. In Kerfoot.W.C. (ed.),
Evolution and Ecology of Zooplankton Communities. University Press of New England, Hanover,
NH, pp. 411-417.
George J3.G. (1976) Life cycle and production of Cyclops vicinus in a eutrophic reservoir. Oikos, 27,
101-110.
Hansen,A.M. and Jeppesen,E. (1992) Life cycle of Cyclops vicinus in relation to food availability,
predation, diapause and temperature. / Plankton Res., 14,591-605.
Hokkaido Research Institute for Environmental Pollution (1990) Lakes and Marshes in Hokkaido.
Hokkaido Research Institute for Environmental Pollution, Sapporo, 445 pp. (in Japanese).
1085
T.Kobari and S.Ban
Horn.W. (1981) Phytoplankton losses due to zooplankton grazing in a drinking water reservoir. Int.
Rev. Ges. Hydrobiol., 66,787-810.
Kawabata.K. (1989) Seasonal changes in abundance and vertical distribution of Mesocyclops thermocyclopoides, Cyclops vicinus and Daphnia longispina in Lake Biwa. Jpn. J. LimnoL, 50,9-13.
Kitano.K. (1964) Analytical method of dissolved oxygen in freshwater and seawater. Jpn Anal, 13,
573-577 (in Japanese).
Maier.G. (1989a) Variable life cycles in the freshwater copepod Cyclops vicinus (Uljanin 1875):
Support for the predator avoidance hypothesis? Arch. Hydrobiol., 115,203-219.
Maier.G. (1989b) The seasonal cycle of Thermocyclops crassus (Fischer, 1853) (Copepoda:
Cyclopoida) in a shallow, eutrophic lake. Hydrobiologia, 178,43-58.
Maier.G. (1989c) The effect of temperature on the development times of eggs, naupliar and copepodite stages of five species of cyclopoid copepods. Hydrobiologia, 184,79-88.
Maier.G. (1990) Spatial distribution of resting stages, rate of emergence from diapause and times to
adulthood and to the appearance of the first clutch in 3 species of cyclopoid copepods. Hydrobiologia, 206, 11-18.
Maier.G. (1992) Metacyclops minutus (Claus, 1863)—Population dynamics and life history characteristics of a rapidly developing copepod. Int. Rev. Ges. Hydrobiol., 77,455-466.
NilssenJ.P. and Elgmork.K. (1977) Cyclops abyssorum—Life cycle dynamics and habitat selection.
Mem. 1st. ltal. Idrobioi, 34,197-238.
Nsess.T. and NilssenJ.P. (1991a) Diapausing fertilized adults. Oecologia (Berlin), 86,368-371.
Nsess.T. and NilssenJ.P. (1991b) Life cycle dynamics of a Cyclops strenuus (Crustacea, Copepoda)
population with unusual diapause and reproductive characteristics. Arch. Hydrobiol., 122,323-334.
Onbe\T. (1978) Sugar flotation method for sorting the resting eggs of marine cladocerans and
copepods from sea-bottom sediment. Bull. Jpn. Soc. Sci. Fish., 44,1411.
Papinska.K. (1985) Carnivorous and detritivorous feeding of Mesocyclops leuckarti Claus
(Cyclopoida, Copepoda). Hydrobiologia, 120, 249-257.
Santer.B. and Lampert.W. (1995) Summer diapause in cyclopoid copepods: adaptive response to a
food bottleneck? / Anim. Ecol, 64,600-613.
Santer.B. and van den Bosch,F. (1994) Herbivorous nutrition of Cyclops vicinus: the effect of a pure
algal diet on feeding, development, reproduction and life cycle. J. Plankton Res., 16,171-195.
Shiraishi.Y. (1960) The fisheries biology and population dynamics of pond-smelt, Hypomesus olidus
(Pallas). Bull. Freshwater Fish. Res. Lab., 10,1-263 (in Japanese with English synopsis).
T6th,L.G. and Zankai,N.P. (1985) Feeding of Cyclops vicinus (Uljanin) (Copepoda: Cyclopoida) in
Lake Balaton on the basis of gut content analyses. Hydrobiologia, 122,251-260.
T6th,L.G., Zankai.N.P. and Messner, O.M. (1987) Alga consumption of four dominant planktonic
crustaceans in Lake Balaton (Hungary). Hydrobiologia, 145, 323-332.
VijverbergJ. (1977) Population structure, life histories and abundance of copepods in Tjeukemeer,
the Netherlands. Freshwater Biol., 7,579-597.
VijverbergJ. (1980) Effect of temperature in laboratory studies on development and growth of
Cladocera and Copepoda from Tjeukemeer, the Netherlands. Freshwater Biol., 10,317-340.
Watson,N.H.F. and Smallman.B.N. (1971) The physiology of diapause in Diacyclops navus Herrick
(Crustacea, Copepoda). Can. J. ZooL, 49,1449-1454.
Wetzel,R.G. and Likens.G.E. (1991) Limnological Analyses, 2nd edn. Springer-Verlag, New York, 391
pp.
WhitehouseJ.W. and Lewis3.G. (1973) The effect of diet and density on development, size and egg
production in Cyclops abyssorum Sars, 1863 (Copepoda, Cyclopoida). Crustaceana, 25,225-236.
Wierzbicka.M. and Kedzierski,S. (1964) On the dormancy state of some species of Cyclopoida under
experimental and national conditions. Pol. Arch. Hydrobiol., 12,48-80.
Wyngaard.G.A., Tayor3-E. and MahoneyJJ.L. (1991) Emergence and dynamics of cyclopoid
copepods in an unpredictable environment. Freshwater Biol., 25,219-232.
Zankai.N.P. (1984) Predation of Cyclops vicinus (Copepoda: Cyclopoida) on small zooplankton
animals in Lake Balaton. Arch. Hydrobiol., 99, 360-378.
Received on August 2, 1997; accepted on January 13, 1998
1086