Nov 27, 1990 - High production estimates can be linkrd to ... diaptomus hessei life-history stages under controlled temperatures. ... representing each stage in any batch ranged from 500 for stages N2-N5, to 40-80 for C5 ..... 1972). Late copepodite and adult stages show strong vertical migration .... 1965; Miller et al., 1977).
Estuaritre,
Coastal
and Shelf
Science
(1991) 33,121-135
Population Production
Dynamics and Estimates of for the Calanoid Copepod Pseudodiaptomus hessei in a Warm Temperate Estuary
H. L. Jerling Department Elizabeth, Received
and T. H. Wooldridge
of Zoology and Institute for Coastal P.0. Box 1600, Port Elizabeth 6000, 4 June
Keywords: Africa
1990 and in revisedform
development;
growth;
Research, Republic
27 November
production;
University of Port of South Africa
1990
copepoda;
estuaries;
South
The copepod, Pseudodiaptomus hessei, was studied over 1 year in the Sundays River estuary. Maximum abundance occurred during summer in the upper half of the estuary. Nauplii and copepodid stages attained peak abundance higher up in the estuary compared with adults. Development time and body size were inversely related to temperature and varied between instars. Females took longer to reach maturity than males. Reproduction was continuous. Production esti-mates integrated over 1 year varied from 0.3 g dry mass mm 3 at the estuary mouth to 4.3 g dry mass m ’ in the upper estuary. Annual P/B ratios varied between 78.5 and 100.2 for the same regions. High production estimates can be linkrd to high summer temperatures.
Introduction Although zooplankton are often important in estuarine foodwebs, few quantitative data are available on the biology of individual species from many regions around the world. Pseudodiaptowzus hessei is the major contributor to copepod standing stock in southern African estuaries (Grindley, 1981), which flush periodically as a result of riverine flooding. After such events, P. he& is also the first copepod to recolonize the water column, attaining high population densities (Wooldridge & Melville-Smith, 1979; Wooldridge & Bailey, 1982). The prominence of P. hessei in local estuaries and its apparent ability to successfully exploit ’ new water ’ prompted a detailed investigation of the biology. The study forms part of a major study on trophic interactions in the warm temperate Sundays estuary. Temporal and spatial patterns of general zooplankton distribution have previously been described by Wooldridge and Bailey (1982). Wooldridge (1986) reported on the biology of the mysid, Rhopalophthalnzus terranatalis, while predatory feeding of R. terranatalis on a second mysid species, Mesopodopsis slabberi, has also been quantified (Wooldridge & Webb, 1988). 027’-771~,‘91:080121+
15 $03.00:0
@ 1991 Academic
Press Limited
122
H. L. Jerling & T. H. Wooldridge
Swortkops
I
Figure
1. Map
1 a 3 km
J
of the Sundays
Sundovs
River
estuary
River
estuorv
and location
of the sampling
stations
Methods Distrib~&o~t
and abundance
Monthly sampleswere collected at night around low spring tide during the darkest phaseof the lunar cycle. Ten stations (Figure 1) were sited along the 21-km estuary. Sampling was completed in 3 h, beginning at Station 10on eachoccasion. Temperature and salinity were recorded at 1-m depth intervals every 2 weeksat each station. Water depth in the estuary averaged 3-4 m with a maximum of 7 m at Station 2. Mean spring tidal range in the estuary was 0.75 m, while at neaps,the mean range was0.2 m (MacKay & Schumann, 1990). Two modified WP2 plankton nets (57 cm diameter and 90 urn meshfitted with Kahlsico 005 Wa 130 flowmeters) were each attached to a 1.0-m boom protruding laterally from the bow of a flat-bottomed
boat (4 m length).
This
ensured
that nets operated
in water
undisturbed by the boat. One net sampledsubsurfacewaters and the other the epibenthicmid-water layer. The latter washeld at the required depth using a graduated pole. Stations 1,8,9 and 10 were shallow ( < 2.0 m) and only subsurface sampleswere taken. Nets were towed for 1.5-2 min at l-2 knots. In the laboratory, sampleswere diluted to predetermined volumes. Two to five subsampleswere withdrawn with a wide-bore pipette and all developmental stagesof P. he& enumerated. Final abundance wasexpressedasnumbers m ’ of water. Determination
Growth of embryonic
and post-embryonic
development
times
was done in the
laboratory over 1 year. Experimental temperatures corresponded to average seasonal
Population
dynamics
and production
estimates
123
Thermostat heater
r Estuarine
water
Incubation
chamber
-
Figure 2. The apparatus used to determine development times for specific hessei life-history stages under controlled temperatures.
Pseudo-
diaptomus
ambient and were set at 16,20,23 and 26 ?C. The light/dark cycle in the laboratory also corresponded to prevailing ambient conditions. Fresh estuarine water was collected every 4 to 5 days and filtered through a 90-pm sieve. A salinity of 20 Ifr 1%0 was used in all experiments and this corresponded to the salinity in mid-estuarine regions where experimental animals were collected. Preliminary experiments indicated no difference in development time for the copepod over a range of cstuarine salinities (5-35). Incubation chambers (Figure 2) consisted of plastic vials (30 ml) floating in an inner tank filled with estuarine water. An outer tank, equipped with a Haake Dl thermostat heater, further reduced temperature fluctuations ( + 1 ‘C). Windows cut in experimental vials were covered with 200 pm mesh which allowed for exchange of water and food with the estuarine water in which the vials floated. Water in vials was partially drained and replaced automatically after each examination. An air-lift system ensured continuous mixing of estuarine water which was replaced every 4-5 days. Copepods were regularly collected from the estuary in order to establish development times through the five naupliar and five copepodid stages. Nl is retained in the egg (Jerling & Wooldridge, 1989). Two to three individuals, each at a different stage of development, were introduced into an incubation chamber. Thereafter, chambers were examined two to three times per day (between 06.00h and 22.00h). Individual copepods were monitored for two or three developmental stages only. This minimized potential adverse effects imposed
124
H. L.Jerling
& T. H. Wooldridge
by laboratory conditions. A moulting event was assumedto have taken place mid-way between observations, while the duration of any stagewastaken asthe time-span between the calculated mid-point of two successivedevelopmental stages. Average body length of eachstagefor different seasonswasdetermined from formalinpreserved animals. Measurements were taken from the anterior border to the tip of the caudal region in naupliar stages,while in copepodids, measurementsextended to the end of the caudal rami. Copepodswere removed from preserved winter (13.6 ‘C) and summer (25.7 “C) samplesto determine body massfor any specific stage.Animals were first rinsed in distilled water and transferred to aluminium foil weighing boats before being ovendried at 60 “C for 24 h and batch-weighed on a microbalance. The number of individuals representing each stage in any batch ranged from 500 for stagesN2-N5, to 40-80 for C5 and C6. Animals preserved in formaldehyde and used for dry massdeterminations may result in significantly lower values compared to fresh animals (Omori, 1978; Pace & Orcutt, 1981; Schram et al., 1981; Kimmerer & McKinnon, 1987). In contrast, Dumont et al. (1975) reported an insignificant lossin dry massafter formaldehyde preservation. To determine the possible influence of formaldehyde on the dry mass of P. hessei,three batches of freshly caught, unpreserved, non-ovigorous females were weighed. Animals from the samesample were also preserved for 6 months in approximately 5”,, estuarine water-formalin. Three replicates of 30 to 50 animals were batch-weighed using the method described above. There was no significant difference (t test, d.f. =4, P=O,145, a = 0.05) between the massof fresh and preserved animalsand no correction was madefor preserved animalsused in present determinations. Production
Reproduction in P. hessei is continuous. Cohort identification in successive series of sampleswas not possibleand consequently a method assumingapproximate steady state over discrete time intervals was employed. Production estimates were determined using the technique described by Rigler and Downing (1984) and Kimmerer (1987) which calculates production rate (PR) and integrated production (ZP). The production rate (ug dry massmm7day-i) was calculated from the equation PR = xg,B, (Kimmerer, 1987)
where PR is the production rate, g, the growth rate of stagei obtained by
where d, is the duration of stage i, mminthe masson entering stage i and VH,,, the masson entering stagei+ 1. Biomass(BJ was determined asfollows B;=
NWI
where wl
=
FFZ,;,
(3,
exp k,d,) ~ 1 (4)
‘54
and N is the abundance m-3 of stagei. W, is the mean weight of stagei. The development time D and body length L was related to temperature by D = a(T L=a(T
- v)~ - u)’
(Belehradek, 1935, 1957),
Population
dynamics and production estimutes
12s
following the procedure used by McLaren (1966), where a, b and a are constants and T is the temperature. Mean temperature values for each sampling station were calculated from data collected bimonthly at multiple depths at each site. Body length at that temperature was calculated with the corresponding equation in Table 3. Length was then used to calculate individual mass.The stageduration wascalculated by substitution of the desired temperature value in the relevant equation in Table 3, relating development time to temperature. These values were used in equations (l)-(4) to estimate PR. Using the equation IP =
i
PR,T(Kimmerer,
1987)
k=l
where T is the number of days between sampling times and N is the number of sampling sessions,integrated production (IP) over the year could be estimated. T was taken as28 days. Annual P/B ratio was derived from
where B refers to the mean annual biomass. Average egg-pack dry masswas determined by the difference between femaleswithout eggsand those with eggs.To calculate egg production, the equation
P = N(m,,,
- m&ID
was used (Rigler & Downing, 1984). N is the number of egg packs, mmax - mmln is taken as the meanweight of egg packs calculated and D (D = dE)is the duration of the development (seeTable 3).
Results Temperature
and salinity
Recorded water temperatures ranged from 13 ‘C in winter (July) to 26 ‘-C in summer (January). Stations nearer the mouth showed lessseasonalvariation compared with the upper estuary. In vertical profile, differences between surface and bottom waters seldom exceeded 1 C. A salinity gradient was evident along the axis of the estuary. In the mouth region salinity was constantly above 30%0,while at Station 10 it seldom exceeded 5%0.Stratification was evident at Stations 2-9, the difference between surface and bottom increasing up-estuary. On occasions, this difference exceeded 5%0.These patterns of salinity distribution are similar to those reported by Wooldridge and Bailey (1982). Distribution
and abundance
I’. hessei waspresent throughout the year at all stations, although numbers were relatively low during winter (Figure 3). Minimum numbers in the estuary were recorded in July, the average numbers being: nauplii 6908 mP3, copepodites 566 mP3 and adults 325 mm’. Abundance increased during spring, nauplii attaining a peak at the end of November at
126
H. L.Jerling
&3 T. H. Wooldridge
(a )
M
A
M
.I
.I
A
1986 Figure 3. Spatial and temporal copepodids (b) and adults (c). 2000 m ‘; adults 1000 m ‘.
s
0
N
D
J
F
M
1987 distribution of Pseudodiaptomus hessei nauplii (ai, Contour intervals: nauplii 1OOOOm ‘; copepodids
Population
dynamics and production estimates
127
Station 9 (113 038 me3). Copepodites peaked during January at Station 8 (30 784 mm‘), while adults attained peak abundance during the samemonth at Station 5 (11 129mm‘). Growth
Mean length and massfor all stages(Table 1) reflected exponential growth. Winter animals attained a larger body size and hence masscompared to their summer counterparts. These differences were not as marked during naupliar stages.Females were also substantially heavier than males. Length (pm) and dry mass (pg) were related by multiplicative equations nauplii
Log,,(mass) = 1.3891og,,(length) - 3.66 (r = 0.99)
Copepodites
Log,,(mass) = 2,3921og,,(length) ~ 6.54 (7. = 0.99).
Development times during the embryonic stage took longer at all experimental temperatures compared with other stages (Table 2). Development was variable between stages,the third naupliar stagereflecting the fastest development. Femalestook longer to reach maturity compared with males (Table 2). Table 3 lists the development time and body length for each naupliar and copepodid stage, related to temperature by Bttlehridek’s (1935, 1957) equation. Productio?z
Dry mass of an average egg pack was 5.25 pg for both summer and winter animals. Production was minimal during winter (1.1 mg dry massm ’ day-‘, averaged for all stations during July). A maximum production rate of 47.45 mg dry massmm’ day ’ was calculated for Station 8 in December (Table 4). Minimum and maximum daily P/B ratios occurred in July and January, respectively. Production was highest between Stations 4 and 10, with seasonalshifts between regions. In autumn and winter, lower stations had higher values compared to middle and upper estuarine stations. In spring, production increased substantially with maximum increasein the upper regions (Figure 4). Maximum integrated production over the year occurred in the upper estuary I3.34 g dry massmP3at Station 9) (Table 4), with an average value of 2.46 g dry massm ’ for all stations. The annual P/B ratio was also maximal (100.2) in the upper estuary at Station 8. A highly significant correlation wasapparent when daily P/B ratios were related to temperature (r = 0.95) and is described by P:B = - 0.0716 + 0.0149T where T is the temperature in C. Discussion Distributiorz
and abundance
The spatial distribution of P. hessei suggestsa wide salinity-tolerance range. This is supported by previous studies where the pioneer nature of P. hessei following fluvial flooding was demonstrated (Wooldridge & Melville-Smith, 1979; Wooldridge & Bailey, 1982). Grindley (1981) also noted a wide salinity-tolerance range for P. he&, recording the presenceof this speciesin water from < I%0to 74%0.
N2 N3 N‘i x5 N6 Cl C? C3 C4 male C-l female C5 male C5 female Male Female
Stage
were
(pm)
not divided
47 35 35 28 33 28 29 25 22 27 17 23 18 14
II
13.6 C SD
12 10 9 10 10 16 22 40 26 30 44 70 24 68
lengths
1. Body
,‘C4 animals
181 234 275 328 390 541 688 888 1064 1217 1283 1580 1497 2020
L
TABLE
into
175 229 272 322 388 534 660 842 1016 1144 1214 1480 1460 1899
L
and
mass
sexes
21 14 10 10 15 27 10 42 44 26 30 47 47 70
27 20 12 15 21 14 15 18 20 19 16 21 13 17
II
Body
(pg)
171 220 270 320 375 521 653 819 979 1100 1160 1470 1380 1810
L
(L)
determinations.
length
for all developmental
for weight
17.5 c SD
dry
13 11 8 6 10 20 13 36 34 28 34 50 32 48
20.8 C SD
stages
27 18 16 18 18 17 14 20 17 17 15 18 18 17
II
1131 1376 1340 1717
168 216 269 308 360 508 628 791 912
L
of Pseudodiapronzus
9 9 14 14 18 16 19 34 27 34 22 28 32 27
25.7 -C SD
hem-i
33 42 40 30 30 20 23 17 20 12 14 18 14 14
n
at different
47 56 50 50
300 300 160 100 80
0.89 1.20 1.98 3.12 5.70 6.50 12.20 13.10 29.60
300
n
0.51 -
C
500
13.6
Dry
mass
temperatures
0.26
m(W
water
25.7
5.49 8.96 10.65 21.60
0.52 0.61 0.79 1.08 1.43 2.63 3.67
0.30
m(m)
(m)
rr
80 75 50 50
500 500 300 300 250 200 100
500
~C
Population
TABLE
Stage
D(h)
Egg N2 N3 N4 N5 N6
