Limnol. Oceanogr., 39(7), 1994, 1594-1605
0 1994, by the American
Society of Limnology
and Oceanography,
Inc.
Processescontrolling recruitment of the marine Calanoid copepod
Temora Zortgicoks in Long Island Sound: Egg production,
egg mortality, and cohort survival rates
William T. Peterson
NOAA,
National
Marine
Fisheries Service, F/RE3,
1335 East West Highway,
Silver Spring, Maryland
20910
William J. Kimmerer
Biosystems Analysis Inc., 3 152 Paradise Dr., Tiburon,
State University,
3 150 Paradise Dr., Tiburon
California
94920, and Romberg Tiburon
Center, San Francisco
Abstract
Three phytoplankton
blooms were observed during our 6-month study period and each resulted in
increased rates of egg production (EPR) by female Temora longicornis. An EPR of 50 eggs female- I d-l
was observed during the first bloom (spring bloom, March). The maximum EPR observed during the
other blooms (May and July) was 20 and 30 eggs female- ’ d- ’ . At all other times the EPR was nearly
zero. Each pulse in egg production initiated a distinct cohort. Survivorship
from egg to adult was low:
3% for the first cohort and 0.8% for the second. The third cohort did not reach maturity. Mortality was
highest in the egg stage-only
10% of the eggs produced survived to first nauplius. Rates of egg mortality
were positively correlated with clearance rates of T. Zongicornis, suggesting cannibalism as a cause of high
mortality. However, the clearance rates required would be -34-fold too high, suggesting a different densitydependent factor, such as disease, viruses, ecto-parasitism or consumption by dinoflagellates. Advection
and resting egg production do not appear to explain high rates of egg loss.
It is well established that the egg production
rates of most copepods are dependent on food
concentration. Most field studies have shown
that food is usually present in quantities sufficient to support high rates of egg production
only during phytoplankton blooms. At all other times, rates of egg production are usually
far less than maximum and are limited by food
supply. As a result, recruitment is discontinuous, dependent upon ephemeral phytoplankton blooms. Therefore, temporal variation in
food supply is almost certainly a key factor in
controlling copepod population dynamics and
is thus a factor contributing
to variations in
recruitment rate.
Far less is known about copepod egg mortality as a factor controlling population dynamics. Landry (1978) and Uye (1982) showed
that only -20% and 7.5% of the eggsofAcartia
Acknowledgments
clausii reached the first nauplius stage. Kisrboe
The work reported in this paper was supported by Grant
et al. ( 1988) reported egg mortalities on the
NA86AADSG045
from the New York Sea Grant Institute
order of 99% and greater for copepod popuawarded to W. T. Peterson while at the State University
lations in Kosterfjorden, Sweden. Others have
of New York at Stony Brook.
reported mortality rates on the order of 50%:
For assistance at sea, the help of D. Bellantoni, H. Dam,
S. Horrigan, T. Johnson, and S. Leffert is appreciated.
Beckman and Peterson (1986) for Acartia tonComments on earlier drafts of this paper by S. Painting,
sa
in Long Island Sound, Daan ( 198 7) for T.
V. Stuart, H. Dam, and two anonymous reviewers imlongicornis eggs in the North Sea (due to Nocproved the final version. We thank D. Stoecker for thoughts
tiluca predation), and Ianora et al. (1992) for
and references on the possible role which dinoflagellates
might play in killing copepod eggs.
Centropages typicus from the Gulf of Naples.
1594
A basic ecological principle is that populations have the potential for exponential growth,
yet under natural conditions, maximum population growth rates are seldom achieved. A
key research issue is to determine the relative
importance of biotic and abiotic factors that
limit population growth. In this paper, the importance of two biotic factors is discussed in
light of the role of each in controlling population size of the marine copepod, Temora longicornis: seasonal variations in chlorophyll
concentration as a factor controlling birth rates,
and variations in egg mortality rate as a factor
controlling recruitment of nauplii to the population. Egg production and egg mortality constitute the initial steps in the recruitment process.
Temora egg mortality
Others have reported that mortality is highest either in the naupliar or copepodite stages.
However, neither egg production rate nor egg
concentration was measured in any of these
studies, so their conclusions are not necessarily
correct (Heinle 1966; Mullin and Brooks 1970
as examples).
We present evidence that recruitment of copepods in coastal waters can be controlled
largely by factors associated with eggs: food
limitation of egg production and high egg mortality rates. We use a population of T. longicornis in Long Island Sound as an example.
Methods
Study sites-Most
of the data reported here
were collected at a baseline station in central
Long Island Sound, near Port Jefferson, New
York (4 l”Ol’N,
72’57’W). This station, referred to as the “offshore station,” is located
5 km offshore at 40-m depth. Seventeen cruises were made from February through July 198 5,
a period that spans most of the growth season
of T. longicornis.
Limited sampling was carried out at two
nearshore sites. One site was at a pier at Stony
Brook (water depth, 3 m) and was sampled in
February and April when severe weather prevented cruises. During these visits, chlorophyll
concentration was measured and females were
collected for egg production measurements.
The other site was in the nearshore zone (water
depth, 10 m) and was sampled from May
through July during routine cruises from Port
Jefferson. We measured chlorophyll
concentrations and collected female T. longicornis for
measurement of egg production rates. This station was added to gain a rough idea of the
degree of spatial variability in egg production
rates.
Water-column sampling-Temperature
and
conductivity profiles were obtained at the offshore station with a Beckman RS-5 salinometer. Water samples for chlorophyll
analysis
were collected from standard depths (1, 3, 5,
10, 15,20,30, and 37 m) with a Jabsco pump
(flow rate, 10 liters min-l) and a 1.9-cm-i.d.
rubber hose. From each depth, a 50-ml water
sample was passed through a Millipore
AA
filter (pore size, 0.8 pm) for later analysis of
Chl a. The concentration of Chl a in several
size fractions was measured from a sample in
1595
which equal volumes of water from 1, 3, and
5 m were combined in a 20-liter plastic container. Subsamples were passed through a 20pm Nitex screen, a lo-pm Nitex screen, and a
5-pm membrane filter, and 50-ml subsamples
of each filtrate were passed through AA Millipore filters. Filters were kept in the dark on
ice in individual 15-ml plastic centrifuge tubes
until returned to the laboratory several hours
later.
Zooplankton
samples were collected by
hauling a WP-2 net (0.57-m mouth diameter,
200-pm mesh) vertically through the upper 37
m of the 40-m water column. The net was fitted
with a TSK flowmeter. Zooplankton was also
collected by pumping 4 liters of water from
each of three depths with the Jabsco pump and
combining them to produce a 12-liter integrated sample as follows: samples from 1, 3,
and 5 m were combined to represent the upper
mixed layer; 5, 10, and 15 m, the thermocline
region; and 15,22, and 30 m, the bottom mixed
layer. Each 12-liter sample was concentrated
with a 60-pm Nitex screen, rinsed into a sample bottle, and preserved with 5% buffered
formaldehyde.
Duplicate samples were collected from 1 + 3 + 5 m for zooplankton and
chlorophyll analysis - 3 h after the initial samples and processed as above.
Laboratory analyses- For chlorophyll analysis, 90% acetone was added to the centrifuge
tubes, and pigments were extracted for 24 h in
the dark at - 20°C. Fluorescence was measured
before and after acidification
with a Turner
Designs fluorometer and chlorophyll concentration calculated according to Strickland and
Parsons (1972). For each pump sample, the
entire sample was counted. For the plankton
net tows, two 1. l-ml subsamples were taken
with a piston pipette, and all developmental
stages of all copepod species were enumerated.
Counts were converted to numbers per cubic
meter of water filtered.
Egg production measurements-Copepods
were collected by lowering a 0.5-m-diameter,
240-pm-mesh net to a depth of 20 m and allowing it to sample while the ship drifted. After
5 min, the net was retrieved, and its contents
were diluted into a lo-liter insulated cooler
filled with surface seawater. Water used for
incubations was pumped from 5 m, filtered
through a 60-pm Nitex screen (to remove any
80-pm-diameter Temora or Acartia eggs from
Peterson and Kimmerer
1596
the water), and then added to l-liter plastic
(PMP) bottles.
In the laboratory, individual
adult T. Zongicornis females were sorted from the living
plankton collections into the seawater-filled
bottles-one
female per bottle. Sorting was always completed within 2 or 3 h of sample collection. Between six and nine bottles per station were set up. When sorting, care was taken
to reject females with broken antennules or
missing furcal rami. Anesthetics were not used
so that lethargic females could be rejected. The
bottles were incubated in a walk-in temperature- and light-controlled
room with environmental conditions adjusted to match those observed on the day of each cruise (i.e.
temperature at 20-m water depth and day
length). After 24 h, the water in each bottle
was filtered through a 60-pm Nitex screen, the
eggs and females were rinsed from the screen
into a counting dish, and the eggs were enumerated, yielding an estimate of eggs female- l
d-l (B in Eq. 1 and 5 below).
Estimates of egg production rate (EPR) in
situ were also made with the egg-ratio method
(Edmondson et al. 1962; Checkley 1980b):
B
E
ER=NfDBERis the EPR (ER is egg ratio), E is egg concentration estimated from the pump samples,
NY is female abundance, and D is embryonic
duration (or egg development
time) from
M&u-en (1978) and Peterson (unpubl.). D depends on water temperature and was estimated
by averaging the temperature of the upper 5
m of the water column between adjacent sampling dates. This is the region of maximum egg
concentration. The mean concentration of eggs
in the water column was calculated from
E = [5(N1+3+5,)
+ lW~+m+d
+ 15(N15+22+30m)1/30N is the number of eggs per
pump samples. Estimates
dance, NY, were obtained
abundances from the pump
(2)
liter in the pooled
of female abunby averaging the
and net samples.
Egg mortality rates-Egg mortality was calculated from measurements of EPR, female
abundance, egg abundance, and estimates of
egg development time (from McLaren 1978;
Peterson unpubl.). Egg development times (D)
were for the most part less than the interval
between sampling dates; therefore the calculation was made assuming that steady state
conditions existed around each sampling date.
At steady state, the rate at which eggs (or any
other developmental stage) pass through a stage
is a function of the rate at which they enter the
stage and of the mortality rate within the stage.
For eggs,
R, = R, exp(-ma)
(3)
(Kimmerer 1987). R, is the rate at which eggs
pass through age a per unit volume, R, the rate
of egg spawning per unit volume, and m the
daily mortality rate. Equation 3 was integrated
over a from 0 to D to obtain the number of
eggs per unit volume,
E = R, [ 1 - exp(- mD)/m].
Substituting
(4)
for R, (=BNJ and rearranging gives
E/BNI = [ 1 - exp(- mD)/m].
(5)
B is the EPR (eggs female-l
d-l) and Nr the
abundance of females (no. liter-l). The mortality rate m was determined iteratively from
Eq. 5.
The proportion of eggs surviving for 1 d (s)
was calculated from
S = exp(-m).
(6)
egg mortality
is
caused by cannibalism or consumption by other copepods, it should be correlated with clearance rate (filtration rate) of all copepods combined. We were able to test this hypothesis
because grazing measurements had been made
on female T. Zongicornis on each cruise during
the study period (data published by Dam and
Peterson 199 1). To test the cannibalism hypothesis, we made the following assumptions:
only T. Zongicornis C4, C5, and C6 (male and
female) were capable of ingesting the 80-pm
eggs. Abundance estimates from the pump
samples (see Fig. 6) were used; ingestion rate
of male T. Zongicornis = 0.67 x female, ingestion of C5 = 0.67 x male, ingestion of C4
= 0.67 x C5 (selection of the 0.67 multiplier
for stage-specific differences in ingestion is discussed by Peterson et al. 1990); filtration rates
(fl were calculated from the ingestion rate (r)
data using the formula
Sources of mortality-If
F = I/C.
Temora egg mortality
1597
MAR
FEE
.
:6
:
-
APR
MAY
:
6:;
3
‘I;!
:
j\b
. .
.
4 ‘I
2
12
.
.
.
I
.
.
6
.
“:I:
2
.
<2
.
.
.
I
‘.
I
&J
4
.‘..
.
I
412
JUL
JbIJ,,\
I
.4..““’
. .
16
1/i .
6
.
i.1
JUN
.
.
. . .
I
.
.
.
. .
.
.
2
.
. .
. .
. .
.
.
.
I
Fig. 2. Chlorophyll
isopleths bg Chl a liter- I) at the
offshore station. Dots indicate sampling depths.
MONTH
Fig. 1. Temperature at the offshore station averaged
over the upper 5 m and at 20 m, March-July
1985.
C is concentration of chlorophyll > 10 I.cm, assuming that Temora feeds selectively on chlorophyll-bearing particles > 10 pm (as suggested
by Peterson and Bellantoni 1987; O’Connors
et al. 1980). Population clearance rates are then
the sum of filtration rates for stages C4, C5,
male, and female.
Cohort survival-Stage-specific
developmental rates could be estimated because two
well-defined cohorts occurred during the study.
For each developmental
stage, we estimated
the date when the temporal mean (following
Rigler and Cooley 1974) of each stage occurred. Temporal mean was calculated from
Mean = (ZtiNi)lXti.
(7)
ti is time in days from 1 January and Ni the
abundance of a given stage on day tis Development time was estimated by regressing stage
vs. day of the temporal mean for each stage.
The slope of the regression is an estimate of
the average stage-specific development time
(D in Eq. 8 below).
Cohort survivorship can be calculated from
cohort data only if one has independently measured the development
time of each stage
(Hairston and Twombly 1985). We do not have
any independent measurements of stage duration, so we could only get an approximate
estimate of survivorship,
carried out by calculating recruitment (R) for each developmental stage (i) from
Ri = Ai/Di-
(8)
A is the area beneath the stage-frequency curves
for each stage i and D the stage-specific development time. This equation is correct only
if survival ‘of developmental
stages is high
(Hairston and Twombly 1985). We show later
(see Table 2) that this assumption is reasonable. Percent survival (s) was then calculated
from
Si = (Ri/R&
X 100.
(9)
R,, was estimated for each sampling date by
assuming that all eggs produced each day for
a period D days (equal to the egg development
time) prior to a cruise survived to hatch and
was estimated from
(10)
Raw = ZBNP
BNf is from Eq. 5, summed back in time to a
period corresponding to D. For each day, BNf
was estimated by linear interpolation between
adjacent cruise dates. The number of egg recruits (Eobs,see Table 3) was calculated from
Eq. 8.
Results
Water temperatures ranged from < 1°C in
February to > 21°C in late July (Fig. 1). The
water column at the offshore station was well
mixed through mid-April,
then stratified
thereafter, typical for Long Island Sound (Peterson 19863; Peterson and Bellantoni 1987).
The spring bloom began in mid-February.
Peaks of 2 1 and 17 pg Chl liter- l were observed on 6 and 11 March at the Stony Brook
dock and offshore stations, respectively. Chlorophyll was uniformly distributed with depth
from February through mid-April but was restricted to the upper 5-10 m after the water
column stratified (Fig. 2).
Peterson and Kimmerer
1598
Table 1. Concentration (no. liter- I) of eggs (E), females
(N,), embryonic duration (D), and EPR (eggs female-l d-l)
calculated from the egg-ratio method (BER) and measured
in 24-h incubations (B). D (from McLaren 1978; Peterson
unpubl.) is based on temperature in the upper 5 m of the
water column. R, is the number of eggs produced per liter
per day, and E, is the egg abundance (No. liter-l)
for
mortality = 0.0.
1985
E
N,
18
26
11
20
3
10
23
Feb
Feb
Mar
Mar
Apr
Apr
Apr
0.0
5.4
38.0
43.5
26.3
14.6
0.7
0.09
0.09
0.10
0.39
0.37
0.36
3.79
9
9
8
8
6
5
4
8,
Fz
20 t3 -+
w -ya
E-,
23
13
7
23
30
3
May
May
May
Jun
0.2
1.5
23.0
21.1
13.8
0.85
1.21
2.57
7.08
2.98
10 2
f:
“,:::
::;
0.6
0.0
i
c3s
F
M
A
MONTH
M
J
3
9 Jul
BE,
B
R”
E”
6.7
47.5
13.8
11.8
8.2
0.05
19.0
25.5
54.3
53.0
43.3
28.8
28.7
1.7
2.3
5.4
20.7
16.0
10.4
108.8
0.0
20.7
43.4
165.4
96.1
51.8
435.1
3
2.2
2
2
1.5
0.06
0.8
4.5
1.5
3.1
2.4
2.7
21.6
10.7
21.4
2.0
2.7
55.5
75.8
63.8
4.5
9.8
111.0
151.5
95.7
;::;
:::
;::
‘i:Z
::::
0.05
0.03
1.4
1.2
8.6
0.0
32.8
19.9
D
-
2:
1.6
0.6
2.3
0.7
J
Fig. 3. Upper panel-chlorophyll
concentration
averaged for the upper 5 m of the water column (O), in the
> 20-urn size fraction (Cl), and in the > 10-brn size fraction
(A). &wer panel-e&
production by female Temora longicornis estimated by the egg-ratio method (0) and bottle
incubation method (o-measurements
at the offshore station; A-measurements
at the shore station near Stony
Brook (February-April)
and at a station in the nearshore
zone (May-July).
Table l), although rates from the egg-ratio
method were a half to a fourth those from the
incubation method (Fig. 4; Table 1). We infer
that the difference between the results of the
two methods resulted from in situ mortality.
0
0
Phytoplankton
cells > 10 pm accounted for
80-90% of the phytoplankton
biomass before
stratification, but cells < 10 pm made up 8098% of the biomass afterward. There were three
notable exceptions to this rule: blooms occurred in late May, early July, and late July
during which the proportion of cells > 10 pm
made up 3wO% of the total chlorophyll.
There were several bursts in egg production
during the study period (Fig. 3). The first was
coincident with the spring bloom, lasting -45
d. Additional bursts occurred in late May and
early July, coincident with the blooms of largecelled phytoplankton.
Egg production ceased
by 23 July, possibly as a result of elevated
water temperatures stressful to this boreal speties.
Peaks in egg-ratio fecundity coincided with
peaks in bottle incubation fecundity (Fig. 3;
0
I
5
I
I
10
15
EGG RATIO
0
Feb -Apr
0
May - Jul
I
I
20
25
(eggs female-’ d-l)
Fig. 4. Comparison of EPR derived from the egg-ratio
method and from bottle incubations. Due to egg mortality,
the egg-ratio method seriously underestimates EPR.
Temora egg mortality
2.5
1
2
0.9 B
P
0.6
&
2
1.5
0.7 g
c
z
g
'
0.5
0.6 z
$
0.5 2
r
;
O
-0.5
o.4 5
0.2 z
0.3
-1
0.1 E
g
20 Feb
01 Apr
11 May
0
20Jun
DATE
-3.5
-3
-2.5
-2
-1.5
-1
-0.5
0
J
0.5
LOG POPULATION CLEARANCE RATE
c
3
a
&
0
5:
-1.5 I
0
100
200
300
400
500
600
i 0
COPEPOD BIOMASS
Fig. 5. A. Log mortality rate and proportion of eggs
surviving each day for Temora Iongicornis in Long Island
Sound in 1985. B. Scattergram of the relation between log
mortality rate (Y) and log of proportion of water column
swept clear (X, population clearance rate divided by 1,000)
for T. Zongicornis C4, C5, and adults. The equation describing the relationship
was Y = 0.92 X + 34, or in
exponential form, Y = 34 P.92; R2 = 0.62, n = 14; geometric mean regression after log transformation. The slope,
1599
Figure 5A shows that egg mortality rates were
relatively low from February through midApril, with a median of 0.46 d-l, but increased
dramatically in late April, with a median of
5.3 d-l until the end of the study period. In
terms of percentage of eggs dying per day, the
medians were 37% d-l for February through
mid-April and 99% d-l thereafter. The abundance of eggs that would exist in the absence
of egg mortality was far higher than actually
observed (Table 1).
The sudden increase in mortality on 23 April
coincided with a 5- 1O-fold increase in copepod
biomass (Table 2), suggesting that copepod
feeding was responsible for the high death rates.
Since T. longicornis makes up - 80-90% of the
copepod biomass in Long Island Sound (Peterson unpubl.), cannibalism was postulated.
The hypothesis was tested by regressing the
mortality coefficient vs. population clearance
rate after log-log transformation.
Figure 5B
shows that the two variables were significantly
related (Y = 34xO.92, r* = 0.62, n = 14; geometric mean regression after log transformation, P < 0.001). The slope, 0.92, was not
significantly
different from 1.0. Figure 5C
shows that mortality rates and copepod biomass are density-dependent
since the two are
significantly related.
-Cohorts were produced by each burst in egg
production (Fig. 6) in association with periods
of relatively low egg mortality (compare to Fig.
5A). The first cohort was generated during the
spring bloom following a period of high EPR
(50 eggs female-’ d-l) and low egg mortality
rate. The second cohort resulted from a lofold increase in fecundity (from 2 eggs female- l d- l in early May to 20 eggs d- l during
the bloom in late May), a 2-5-fold increase in
abundance of females during the same period,
and a reduction in egg mortality rate. The importance of a decline in egg mortality rate in
contributing to the initiation of the second cohort is shown in Table 2: from 13 May to 3
June, up to 28% of the eggs produced survived
to hatch, but before and after this period, survival averaged < 1%.
c
0.92, was not significantly different from 1 (P < 0.001).
C. Scattergram of the relation between log mortality rate
(Y) and log biomass of T. Iongicornis C4, C5, and adults:
Y = 0.0056 X - 0.23, R2 = 0.49, n = 14; geometric mean
regression after log transformation.
Peterson and Kimmerer
APR
MAI-
MAY
J UN
JUL
ADULTS
Table 2. Mortality rates (m, d-l, from Eq. 5), proportion of eggs dying each day (S is percentage surviving each
day, from Eq. 6), biomass &g dry liter- ‘) of Temora iongicornis C&C6 in pump samples, and Temora clearance
rates (ml liter - ’ d- I) calculated from gut fluorescence data
of Dam and Peterson (199 1). Note that population clearance rate divided by 1,000 is the proportion of the water
column swept clear per day.
Tenwra
1985
26
11
20
3
10
23
7
13
23
30
3
11
17
3
9
NI - N4
\
/’
(
ay.--..,*..-,
1, _ _
Feb
Mar
Mar
Apr
Apr
Apr
May
May
May
May
Jun
Jun
Jun
Jul
Jul
In
0.42
0.03
0.46
0.61
0.69
162.5
16.7
1.28
2.48
3.62
4.72
6.37
21.57
2.72
6.00
1-S
0.33
0.04
0.37
0.45
0.50
1.00
1.00
0.72
0.91
0.97
0.99
0.99
1.oo
0.93
0.99
Biomass
10.0
3.3
38.7
49.4
69.1
526.1
257.1
233.7
142.9
443.7
97.2
80.4
172.1
2.2
0.0
clearan~
rates
4.1
0.7
15.4
22.8
33.1
1,097.2
265.9
755.3
108.1
112.5
190.7
71.0
719.9
2.2
0.0
Figure 7 shows that the first cohort developed from egg to C3 at a rate of 3.7 d stage- l.
From C3 onward, the rate decreased to 9.3 d
stage-l, suggesting food limitation
of development. Egg-to-adult generation time for the
first cohort was 62 d. For the second cohort,
the slope for E to C5 was 0.41, equivalent to
a 2.4 d stage-l. Generation time was 1 month.
A third cohort was initiated in early July (as
indicated by an increase in EPR, Table 1 and
Fig. 3), but there was no evidence from watercolumn sampling that the cohort became established. The failure of this cohort could have
been due to high egg mortality or to the production of resting eggs.
Table 3 shows that over the period of one
generation, mortality was greatest in the egg
stage. For the first cohort, only 10% of the eggs
produced survived to Nl. After N6 was
reached, there was little mortality. Overall survivorship from egg to adult was 3% for the first
cohort, 0.8% for the second cohort, and 0.0%
for the third cohort. Had the egg-to-adult sur-
EGGS
FQ\
c
JUN
Fig. 6. Abundance
the offshore station.
of Temora longicornis life stages at
Temora egg mortality
1601
vivorship been calculated from the “observed
egg abundance” data (rather than from the estimates of “eggs produced”), we would have
concluded that survivorship
was 10 times
higher (31 and 6%, respectively) for the first
two cohorts.
Discussion
Our results show that recruitment of individuals to the population of 7’. Zongicornis in
Long Island Sound depends primarily on two
factors: food limitation of fecundity and high
rates of egg mortality. Eggs were produced only
during blooms of larger (> 10 pm) phytoplankton cells. These discrete egg-laying events of
several weeks’ duration initiated distinct cohorts that could be followed from egg to adult.
Mortality was concentrated in the egg stageonly a few percent of all eggs produced reached
the naupliar stages. Thus, recruitment variability in this copepod is probably controlled
by whatever physical factors control the initiation of blooms of large cells of phytoplankton and by whatever biological factors control
egg mortality.
Relationships between recruitment, phytoplankton blooms, and egg production in T.
Zongicornis have already been discussed (Peterson and Bellantoni 1987) for this same 1985
data set, so they need not be treated further
here. We do add a note of possible interestegg production rates of 50 eggs female-l d-l
observed during the spring bloom were two to
three times higher than any rates reported previously for this species (Harris and Paffenhiifer
1976: 15-20eggsd-l;Daan
1987: 18eggsd-l;
Van Rijswijk et al. 1989: 25 eggs d-l). We do
not know whether the high reproductive rate
DAYS SINCE 1 JAN
Fig. 7. Development times of the two cohorts of Temora Zongicornis calculated by the method of Rigler and
Cooley (1974) (see Eq. 7).
is due to phenotypic or genotypic differences
among populations, but it may be a factor that
partially
explains the extraordinary
dominance of T. Zongicornis in Long Island Sound
(Peterson 1985).
We presented evidence here that food limitation of population growth was not restricted
to egg production: cohort development was at
times food limited as well. For the first cohort,
stage duration averaged 3.7 d from egg to C3.
This is the rate expected for a population developing at maximum rates at a temperature
of 7.1”C. This rate was estimated from McLaren’s (1978) relationship between generation time (G) and water temperature (t) for T.
longicornis: G = 16,988 (t + 10.4°C)-2.05; since
there are 13 stages between egg and adult, average stage duration is G/ 13, or 3.7 d in this
example. Temperatures in the upper 20 m of
the water column (where all developmental
stages are found at this time of the year: Pe-
Table 3. Area (A) beneath the stage-abundance curves shown in Fig. 6, calculated by the trapezoid method, and
number of recruits (R) each day, calculated from Eq. 8. S is proportion of animals which reached each stage relative
to the number of eggs produced (from Eq. 10).
First cohort
Ew
tew)
Eggs (obs)
N5
N6
Cl
c2
c3
c4
c5
Second cohort
A,
R
S
A,
R
s
9,523,650
1,383,540
204,460
254,800
199,829
191,488
203,866
277,141
323,874
2,347,4 13
240,7 18
46,058
59,960
50,367
50,137
59,985
60,929
74,993
o_lO
0.02
0.026
0.022
0.02 1
0.026
0.026
0.032
3,149,250
418,570
15,830
20,655
33,537
28,744
39,825
37,46 1
40,4 12
2,000,750
259,437
8,488
10,503
18,492
14,911
23,426
15,609
16.838
0.13
0.004
0.005
0.009
0.008
0.012
0.008
0.008
1602
Peterson and Kimmerer
terson 1985) increased from 3 to 8°C between
20 March and 23 April as eggs developed to
C3. Therefore, our suggestion that development was progressing at a rate at or near the
maximum is reasonable.
However, during development from C4 to
adult (from early to mid-May), developmental
rate decreased greatly (to 9.3 d stage-l) while
water temperatures increased from 8 to 12°C.
Although most copepod species do show a decrease in stage duration during the late copepodite stages (cf. Landry 1983; Peterson and
Painting 1990), a decrease of this magnitude
at a time when the water column was warming
indicates food limitation
of growth. Support
for this hypothesis is that the concentration of
phytoplankton in the > 1O-pm size fraction declined to ~0.5 pg Chl a liter-l in early and
mid-May. If we assume a C : Chl ratio of 50
(Tandichodok
1990, data for Long Island
Sound), 0.5 pg Chl a liter-’ is equivalent to
25 pg C liter-’ - a concentration known to inhibit growth in T. Zongicornis in the laboratory
(Harris and Paffenhiifer 1976).
The second cohort also developed slowly.
Development from egg to C5 proceeded at a
rate of 2.4 d stage-l. This developmental rate
corresponds to a generation time of 29 d (2.4
d stage-l x 12 stages) and would be expected
at temperatures of 12°C. Temperatures observed in the upper mixed layer ranged from
14.5”C (on 1 June, when the cohort began) to
17°C (on 23 June, when the eggs reached C5),
and 11 and 14°C at 20 m (Fig. 1). At this time
of year, all developmental stages (except adults)
are distributed evenly in the upper 20 m (Peterson 198 5). Since individuals were probably
growing at temperatures > 12”C, the cohort
probably developed at less than maximum
rates. Chlorophyll
concentrations
were low
during most of June (Figs. 2 and 3), suggesting
food limitation.
The suggestion of food limitation of development must be viewed as an approximate and
average condition because eggs produced during the first few days of a bloom would experience unlimited food resources for the duration of the bloom (=many weeks), while those
produced near the end of a bloom would be
food limited almost immediately. For the first
cohort, the first eggs produced during the last
week of February would experience relatively
food-rich conditions (> 2 pg Chl a liter-l)
throughout March and much of April. During
this 50-d interval, much of the development
could be completed. Similarly, the bloom in
late May which initiated the second cohort had
a duration of 3 weeks-nearly
sufficient for the
first eggs produced to reach adulthood.
Few eggs reached adulthood, however. Mortality was concentrated in the egg stage. High
egg mortality has been noted by others: Uye
(1982) for A. clausii, Beckman and Peterson
(1986) for A. tonsa, and Kirarboe et al. (1988)
for Paracalanus parvus and Acartia spp. Uye
found for six cohorts that survival of eggs to
nauplii averaged 7.5% (range, 3.8-l 1.6%),
similar to values reported here. Beckman and
Peterson found an average of 50% mortality
for A. tonsa eggs in Long Island Sound in autumn. Kiorboe et al. reported mortalities on
the order of 99%. On the other hand, mortality
in Calanus marshallae seemed to be concentrated in the first two naupliar stages (Peterson
1986a, 1988). Ohman (1986) reported low egg
mortality for Pseudocalanus- a result expected for a copepod that carries its eggs in a sac.
Naupliar mortality was high, with only 10% of
Pseudocalanus nauplii reaching the Cl stage.
At variance with the above citations is the
work of Van Rijswijk et al. (1989): in a study
nearly identical to our Temora study, “expected” egg abundances were almost always
less than observed numbers (for measurements made in 1986 and 1987). One explanation for this is that advection consistently
brought water enriched in T. Zongicornis eggs
past their study site. Finally, Orians and Janzen (1974) noted that high rates of egg mortality are common in both terrestrial and
aquatic systems.
We initially thought that cannibalism might
explain the observed high rates of egg mortality. Since T. Zongicornis made up 85% of the
copepod biomass on average, it could be the
primary predator. Other copepods in the sound,
Acartia hudsonica and Pseudocalanus spp.,
made up only 14 and 1% of the biomass. We
found a strong relationship between population clearance rate and egg mortality rate, with
a slope not different from 1, which might be
considered evidence of cannibalism. However,
the intercept was 34, meaning that, on average,
the mortality rate was 34 times the population
clearance rate. Either the actual clearance rates
are 1.5 orders of magnitude higher than we
Temora egg mortality
have calculated, or some other factor is responsible for much of the mortality. A clearance rate that high would require individual
filtration rates on the order of 0.5-1.0 liter
copepod- l d- l, well beyond the range of published data. Thus, it is unlikely that cannibalism contributes substantially to this mortality.
The only other zooplanktivorous
predators
in the sound during spring are larval and juvenile sand lance (Ammodytes americanus).
They do eat T. Zongicornis eggs and nauplii,
but their density is not high enough to exert
heavy predation pressure (Monteleone and Peterson 1986). Other predators known to feed
on Temora eggs do not occur in Long Island
Sound: Noctiluca (Daan 1987), Phialidium
(Daan 1989), and Pleurobrachia (Miller and
Daan 1989).
Whatever the other factors(s) may be, they
must be density-dependent,
because mortality
rate increased with biomass of T. Zongicornis
(Table 2 and Fig. 5C). One density-dependent
factor that may be important is disease or viruses transmitted to the eggs from adult and
juvenile copepods. Nothing is known about
the communication
of diseases or viruses to
eggs, but since its importance would increase
with biomass, we offer it is as a tentative (and
testable) hypothesis. We do know that parasitism and adult mortality
can be related
through a density-dependent mechanisms (Ianora et al. 1987).
Microzooplankton
may contribute to copepod egg mortality. Parasitism on T. Zongicornis eggs and nauplii by the ectoparasitic dinoflagellate Dissodinium pseudolunula and
Syltodinium Zistii has been noted by Drebes
(1984, 1988). In addition, at least two species
of dinoflagellate are known to consume copepod eggs through pallium feeding (Schnepf
and Elbrachter 1992). Ciliates are also known
to attack copepod eggs in the laboratory (W.
Peterson and M. Roman pers. obs.), but the
frequency and importance of attacks in situ
are not known.
Eggs also may not hatch because of infertility. R. Harris and S. Poulet (pers. comm.) and
Ianora and Poulet (1993) included observations of hatching along with their routine egg
production measurements on Calanus spp.;
they noted that all or most eggs in a clutch will
at times not hatch and suggested infertility as
the cause. On the other hand, egg viability of
A. tonsa in most experiments
1603
was 70-l 00%
(Ambler 1986), as was that of C. marshallae
(W. Peterson unpubl.).
Losses due to advection are probably quite
low because Long Island Sound is a relatively
closed system. A numerical model of circulation demonstrated that the residence time of
water in the central sound, an area which encompasses our study site, is on the order of 60
d (R. Wilson pers. comm.). This result corroborates Riley’s (1952) estimate that no more
than a small percentage of the water in the
central sound is exchanged each day. The fact
that a cohort age structure is characteristic of
the T. Zongicornis population in Long Island
Sound year by year (Peterson 1985) is in itself
evidence that advection does not remove many
individuals from the sound. Furthermore, proportional advective losses would not vary with
population size. Also, T. Zongicornis is not a
dominant member of the copepod community
of the adjacent (to the east) Block Island Sound.
Deevey (1952) found that the dominant copepod there in spring was C. typicus; T. Zongicornis appeared in appreciable numbers only
in June and July. These differences in dominance are further evidence that the exchange
of water between Long Island and Block Island
Sounds is slight.
Sinking of eggs to the floor of the sound and
subsequent consumption by the benthos is a
possible source of mortality because the sound
is shallow (40 m at our study site). If we assume
that T. Zongicornis eggs sink at a rate of 15 m
d-i (the sinking rate of similarly sized eggs of
A. clausii and P. parvus: Valentin 1972; Checkley 1980a), they would reach the floor of the
sound within 2.5 d, where they would be subject to loss to benthic predators. Thus, from
February through early May when egg development times are ~3 d (see Tab& I), losses
to benthic predators could be an important
source of mortality. This mechanism might
explain the mean daily loss of 34% of the eggs
from February to early April, when copepod
clearance rates were low. However, it fails to
explain the relationship of mortality to population size.
The production of resting eggs could explain
high egg mortality rates in June and July, especially the failure of the third cohort in July.
Resting eggs would be expected at the end of
the seasonal cycle, but the frequency of oc-
1604
Peterson and Kimmerer
currence during other times of the seasonal
cycle is not known.
Because of high egg mortality rates, the eggratio method underestimates true egg production rates when applied to broadcast spawners.
Thus, EPR data presented by Checkley (1980b)
for P. parvus and Peterson (1985) for T. Zongicornis may be in error. Also, we note that
estimates of EPR are necessary to construct a
complete survivorship
curve. In the absence
of data on EPR (and female abundances), erroneous conclusions may be reached as to
which life cycle stages are most susceptible to
predation and other sources of mortality.
Future work of the type presented here could
be improved greatly if attention were given to
the following three conditions: experimental
work is needed on rates of egg consumption
by suspected predators (such as copepods and
dinoflagellates); routine measurements of egg
viability should be made of eggs produced by
females in incubations; eggs should be collected from the water column on a regular basis
and held in the laboratory for observations of
hatching success. These experiments would
give valuable information on some of the loss
terms associated with egg mortality.
In conclusion, two factors which Iimit population growth of T. Zongicornis in Long Island
Sound are food-limited fecundity and high rates
of egg mortality.
Food-limited
fecundity is
emerging as a general pattern for copepods in
coastal and estuarine systems, and most studies which have focused on egg mortality have
shown that staggering losses can occur at this
stage. We do not know what causes these high
rates of eggs loss; although cannibalism has
been suggested, the relationship between mortality and population clearance rate would appear to rule that out, at least for T. Zongicornis
in Long Island Sound.
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Submitted: 10 January 1992
Accepted: 8 February 1994
Amended: 1 June 1994