HART, ROB C. Naupliar and copepodite growth and survival of two

Limnol. Oceanogr., 41(4), 1996, 648-658
0 1996, by the American Society of Limnology and Oceanography, Inc.
Naupliar and copepodite growth and survival of two freshwater calanoids at various
food levels: Demographic contrasts, similarities, and food needs
Rob C. Hart’
Department of Physiological Ecology, Max-Planck Institute of Limnology, POB 165, D-24302 Plan, Germany
Abstract
Various demographic responses of Tropodiaptomus spectabilis and Metadiaptomus meridianus (Copepoda:
Calanoida) were measured at 17°C at seven food levels of Cryptomonas (0.05-2.5 mg C liter-‘). In both
species, naupliar, copepodid, and total postembryonic durations declined monotonically, while survivorship,
fecundity, and adult size increased asymptotically with rising food supply. M. meridianus matured faster
than T. spectabilis up to -0.5 mg C liter- I, and its development responses were saturated at lower food
levels (- 0.3 5 mg C liter - I). High naupliar mortality led to lower overall survival in A4. meridianus (maximally
40%) than in T. spectabilis (90%). Survival asymptotes varied between -0.35 and 0.5 mg C liter-l. Clutch
sizes were 5-fold larger in A4. meridianus than in T. spectabilis. Although respective regression estimates of
food threshold levels for maturation (11 and 5), egg production (18 and 60), and population increase (46
and 79 pg C liter-l) in T. spectabilis and M. meridianus did not differ, the derived estimates of interspecific
equivalence for egg production and population increase (82 and 165 pg C liter- I) suggest that T. spectabilis
may be the better competitor below these food levels.
Acceptance of the well-founded premise of food limitation among freshwater zooplankton (Lampert 198 5)
leads to an ecologically obvious and inescapable conclusion: speciesable to utilize low food levels most effectively
to produce offspring will potentially enjoy a competitive
advantage. Experimental measurements of the food dependencies of various demographic responses accordingly
provide useful indices of competitive potential in relation
to food availability. In nature, this potential may be compromised by the complicating range of factors and interactions which collectively drive ecological succession,
commonly a seasonal phenomenon in freshwater plankton communities (Sommer et al. 1986; Sommer 1989).
Following the seminal ideas of size efficiency (HrbaEek
1962; Brooks and Dodson 1965; Hall et al. 1976), successional and related changes in zooplankton community
structure have largely been viewed, jointly or severally,
as manifestations of size-dependent or taxonomic differences in food threshold concentrations (e.g. Muck and
Lampert 1984; Gliwicz 1990), starvation tolerance
(Threlkeld 1976), and vulnerability to predation (e.g. Zaret 1980; Gliwicz and Pijanowska 1989). No consideration
’ Permanent address and correspondence: Department of Zoology & Entomology, University of Natal, Private Bag X01,
Scottsville, 3209 Pietermaritzburg, South Africa.
Acknowledgments
Travel and support costs for this study were provided by a
sabbatical grant from the South African Foundation for ResearchDevelopment, a fellowship award through the Max-Planck
Institute of Limnology in Germany, and a leave allowance from
the University of Natal.
Facilities of the Max-Planck Institute of Limnology (MPI)
were made available by Winfried Lampert. I thank Barbara
Santer for support and L. Schiiler for technical assistance during
my visit. I acknowledge the comments of two anonymous reviewers during preparation of this paper.
of food thresholds and their potential influence on ecological differentiation can summarily disregard exploitative resource competition as a factor.
In practice, however, understanding of the role of competition as a determinant of zooplankton succession derives largely from descriptive accounts and experimental
analyses of cladoceran zooplankters (DeMott 1989). Copepods have received scant attention. Their food thresholds have seldom been determined, and with few exceptions (reviewed by Green et al. 199 1) studies have focused on adult or copepodid stages, largely to the exclusion of naupliar instars. Direct measures of dietary overlap
and of tests for food limitation or competition are basically lacking (DeMott 1989). In part, these deficits are
attributable to two inherent features of copepod development: first, a complex life-history pattern comprising,
11 or 12 juvenile stages, of which the initial five or six
naupliar instars are particularly difficult to distinguish
interspecifically, especially in live animals; and second,
the relatively long development times which necessitate
greatly protracted experiments in order to study coexistence or competitive exclusion directly.
My study was undertaken to compare the food dependency of various demographic attributes and associated
indices of competitive potential in Tropodiaptomus spectabilis (Kiefer) and Metadiaptomus meridianus (Douwe).
These copepods are members of distinct subfamilies of
the Diaptomidae - the Paradiaptominae (hf. meridianus), an African (Ethiopian realm) endemic group, and
the Diaptominae (T. spectabilis), a widely distributed
group of the Ethiopian-Paleoarctic-Oriental
realm. Par-
adiaptomids are typically arid-adapted temporary water
inhabitants, some of which (like M. meridianus) colonize
man-made lakes, while the diaptomids are restricted to
more permanent waters (Rayner and Heeg 1994). Adult
females of M. meridianus and T. spectabilis, with respective mean metasome lengths of 1.09 and 1.14 mm,
are broadly comparable in size, although sexual dimor648
649
Copepod growth and food supply
phism is marked in the former. Corresponding male metasome lengths average 0.8 1 and 1.02 mm (Hart 199 1).
The species show a mixture of ecological contrasts and
similarities. Notably, T. spectabilis is more thermophilic
than M. merzdianus (Hart 1994a,b; Hart and Rayner
1994). Relative to M. meridianus, T. spectabilis development accelerates with rising temperature, and it matures faster above -24OC. T. spectabilis has larger eggs
(mean diameters of 140.8 vs. 97.6 pm) and smaller clutches (8.8 vs. 33.7 eggsper clutch, on average) than M. meridianus. The species accordingly show respective attributes of K and r selection (Hart 1994a).
This paper reports primarily on the influences of food
quantity on growth rates and various related attributes of
demographic performance in these species which, along
with various congeners, occur in many southern African
inland waters (Rayner and Heeg 1994). Development
times, survival, adult size, and fecundity were compared
at defined levels of Cryptomonas, a unialgal food source
known to be nutritionally adequate for these taxa (Hart
and Santer 1994). Experiments were made at 17°C in
order to limit l’ungal infection, although it was recognized
in advance that M. meridianus would be intrinsically favored at this cool temperature (seeabove). Food threshold
levels for maturation, breeding, and population increase
were derived from the ontogenetically inclusive numerical responses,, to compare the potential ecological performance of these species in relation to food supply.
Studies of functionally similar planktonic organisms
with distinct temporal or spatial separation have greatly
improved theoretical understanding of the mechanistic
nature of niche differentiation and competition (Tilman
1977; Rothhaupt 1988) under nonequilibrium conditions
which commonly prevail in pelagic environments (Sommer 1989). The present copepods are functionally similar
and show temporal separation, including a pattern of seasonal separation observed annually since 1990 in Albert
Falls, a reservoir on the Mgeni River in KwaZulu/Natal
(Hart 1992, 1#994a,b,1996), as well as two episodes of
complete species replacement in Midmar, a sister reservoir just upriver from Albert Falls (Ring et al. 1986; Hart
1994a). Secondarily, therefore, this study permits an indirect assessment of the potential role of competition as
a determinant of observed seasonal replacements of two
comparable representatives within the Calanoid copepods.
from - 100 detached egg sacsof each species air-freighted
to Germany, where the calanoids were reared and maintained at 17.2”C (SE = +0.3”C, n > 500). This relatively
cool temperature was used to pre-empt development of
fungal growth in the cultures.
Two to four replicate batches of -50 freshly hatched
nauplii (~24 h old) of both species were reared to maturity at defined food levels of Cryptomonas sp. This
elongate, pear-shaped, flagellated alga, averaging (+: SE,
n >> 500) 13.4kO.7 pm in maximum length, 8.8kO.3 pm
in maximum breadth, and 8.lkO.5 pm in ESD, was suspended at levels of 0.05, 0.1, 0.2, 0.35, 0.5, 1.0, and 2.5
mg C liter-’ in 100 ml of 0.45-pm-filtered lake water
from Schijhsee, a small lake adjacent to the limnological
institute. Food dilutions were based on measured light
extinctions (at 800 nm) of algal cultures, grown in modified WC medium (Guillard and Lorenzen 1972), in relation to calibration curves of carbon content vs. optical
density at 800 nm determined previously, as described
by Krambeck et al. (198 1).
Batches of copepods were transferred to 500-ml jars on
reaching the first copepodid instar (Cl). Animals were
examined and transferred to fresh medium daily until
maturity to yield median estimates (accurate to within
12 h) of naupliar (D,) and total postembryonic durations
(D,,,). Copepodid (DC) development times were determined by difference. Median values were used in preference to sample means to avoid biasing by tardy individuals (Carlotti and Nival 199 1). Experiments at the
lowest food level tested lasted nearly 3 months.
Clutch sizes were determined from stereoscopic counts
(at 40 x ) of attached, intact egg sacs in the case of T.
spectabilis; enumerations for M. meridianus generally required detachment and dissection of egg sacs containing
many small eggs.Corresponding metasome lengths of the
ovigerous females were measured with a calibrated ocular
micrometer. Nonovigerous females were included in
length determinations to increase sample size where necessary. Adult male metasome lengths were also measured.
Cumulative totals of individuals reaching first copepodid (Cl) and adult (C6) stages in the two to four replicate batches reared at given food levels were used to
calculate naupliar (S,), copepodid (S,), and overall (St,,)
survivorship as a percentage of the cumulative number
of stage one nauplii (Nl) initially isolated:
S, = lOOXl/~Nl;
SC= 1OOX6;X
Methods
1;
St,, = lOOX6/~Nl.
The influence of food resource level on development
times and other demographic responses was compared in
M. meridianus and T. spectabilis with experimental procedures comparable to those described by Hart and Santer
(1994) to test food suitability in these same copepods.
Stocks of ML meridianus and T. spectabilis were obtained from Lakes Midmar and Albert Falls, respectively.
These closely neighboring reservoirs have been described
elsewhere (Hart 1992). Cultures were established in the
Max-Planck Institute of Limnology laboratories in Plijn
Functional responses (Y, development times, clutch or
body sizes, etc.) were fitted as hyperbolic or reciprocal
hyperbolic functions of food supply (X), modified to incorporate a threshold food concentration (X,-J (e.g. Dam
and Petersen 199 1):
Y = Y,,,{ 1 - exp[E(X - X0)}
or
Y= Ymin{l - exp[E(X - X0)]}-‘.
650
Hart
75
explore selected functional responses and to estimate food
thresholds (described below) for growth, population increase, etc. These thresholds were estimated by iteratively
excluding data points to yield the highest regression coefficients. Resulting best-fit regressions mostly spanned
the food range 0.05-1.0 mg C liter-l. Note that these
thresholds are not equivalent to the X0 thresholds mentioned above.
The food threshold for growth was estimated as the
log,,-transformed food level (F, mg C liter-l) at which
adult female development rate (1/D,,, ,) was 0.00 1. Other
arbitrary values tested (0.05, 0.005, and 0.0001) did not
alter the resulting general pattern and ranking. Food
thresholds for breeding and for population increase were
based on rates of egg production and survival. Maximal
breeding rate per individual breeding female (Rif, eggs
female-’ d-l) was calculated directly as the quotient of
mean clutch size (CS, eggs breeding female-l) and days
to female maturity:
- -mm -
- A. Metadiaptomus
meridianus
Nauplll
-AMales
c-Females
-8
90
E75
B. Tropodiaptomus
r
- -n-m
spectabilis
Nauplll
g 60
-A-
Females
8
f3
H-------------E
1C. Tropodiaptomus
: Metadiaptomus
-O-
Dn
--A-
DC
+
cs
Rif = D tot0*
The above estimate was adjusted to a potential breeding
rate per female of the experimental population (R,, eggs
female- l d-l) by correcting individual mean clutch size
by the proportion (P& of females actually producing
clutches at a given food supply level:
Dtot
Finally, a more realistic per capita estimate of increase
rate per individual of population (Rpi, eggs ind.-’ d-l)
was calculated as
0.0
0.5
1.0
Food concentration
1.5
2.0
2.5
(mg C liter “1
Fig. 1. A, B. Naupliar, total male, and total female postembryonic durations of A4. meridianus and T. spectabilis. C.
Comparative durations of T. spectabilis relative to M. meridianus (Tropo : Meta) in relation to level of food supply (mg C
liter- I) of Cryptomonas sp.
where Pp is the proportion of isolated nauplii surviving
to maturity.
Breeding and population increase thresholds were respectively approximated by linear regression as the food
levels at which per diem female population breeding rates
(R,J and whole population increase rates (Rpi) were zero.
Species-specific equivalence levels (response breakpoints)
were calculated from the regression equations as the food
supply levels at which regression lines intersected.
Results
the maximal or minimal values of the
measured response (e.g. maximum clutch size or body
Lax and Kninare
size and minimum development times), and 6 is an exponent specifying the slope of the curve. Critical levels
(X,,,) for the responses fitted to these functions were
estimated as the food concentration at which the relevant
response was 90% saturated (Vidal 1980). Hyperbolic
functions were fitted with the iterative nonlinear regression capabilities of Statgraphics 5.0 (STSC, Inc.). This
procedure was used in analyses of durations, body size,
fecundity, and survival (see Table 3).
Standard statistical procedures (Zar 1984) were used
for other analyses. Linear regression analysis was used to
Comparative influences of food supply on development
times -Food-dependent
responses were qualitatively
similar in M. meridianus (Fig. 1A) and T. spectabilis (Fig.
1B) in respect to both naupliar and total postembryonic
development times. Development time ratios of T. spectabilis to M. meridianus were, however, mostly > 1 (Fig.
lC), reflecting faster maturation of M. meridianus at all
food concentrations tested despite its relatively slow naupliar development at and above 1 mg C liter-‘. Although
this quantitative difference is largely attributable to the
low experimental temperature chosen (see introduction),
relative changes also occurred with food supply (Fig. 1C)
651
Copepod growth and food supply
Table 1. Variability in development times (days) of Metadiaptomus meridianus and Tropodiaptomus spectabilis reared
on different food species at a standard resource level (1 mg C
liter-l).
M. meridianus
Food type
R
(SD)
Naupliar durations
Cryptomonas
Chlamydomonas
Rhodomonas
Cyclotella
6.4
6.7
6.0
13.5
(0.52)
(1.33)
(0.52)
(2.07)
,
---.--* :I00 3
s
:75z .I?
--C hfetadiaptomus
y50 5
3
u
b - Tfopodiaptomus
s
1.25
ii
-------
T. spectabilis
X
(SD)
9.0
9.8
;.g
.
(0.52)
(1.08)
g.;;;
.
-----__
------a
Total durations
Cryptomonas
$6
QQ
Chlamydomonas
$6
QQ
Rhodomonas
$8
QQ
Cyclotella
18.2
23.8
22.0
20.0
18.3
(3.51)
(2.06)
20.1
-
(1.13)
-
(2i6)
27.6
27.3
24.0
26.0
(2.19)
19.0
19.9
-
(0.76)
(0.35)
-
--c
Metadiaptomus
+-
Tropociiaptomus
-I-
MeWkwtomus
Tropodiaptomus
(1.57)
-
120
at 17°C. Maturation was relatively faster in M. meridianus
than in T. spectabilis up to 0.5 mg C liter-l, above which
food-level maturation times (and associated competitive
potential) approached interspecific equivalence (Fig. 1C).
Supplementary naupliar and total durations measured
with different unialgal foods at 1 mg C liter-l (Table 1)
revealed certain intraspecific differences in both species.
In particular, .M. meridianus nauplii took virtually twice
as long to develop on Cyclotella as on Cryptomonas (Table l), while maximum durations (Hart and Santer 1994)
were considerably longer with Chlamydomonas (10 d)
than with Cryptomonas (7 d). Cyclotella did not support
complete development. Such qualitative food influences
were not investigated further in this study. Even with
Cryptomonas as food, some batches of M. meridianus
reared at 1 mg C liter- l also showed very retarded naupliar (and subsequent total) development times (Fig. IA).
As paradiaptomids like M. meridianus naturally inhabit
small temporary water bodies (Rayner and Heeg 1994),
colloquially known as “pans,” I examined whether successive clutches showed chronologically consistent differences in development times, as reported for some crustacean inhabitants of temporary waters (Williams 1985).
However, naupliar durations at a standard level of CrypTable 2. Naupliar durations (days) of three successiveclutches
of two individual Metadiaptomus meridianus females determined at 17°C and a food level of 1 mg C liter - ’ of Cryptomonas.
Differences between successive clutches (paired t-test, matchedpairs rank sign lest, and Friedmann ANOVA) were not significant.
Female
1
1st clutches
2nd clutches
3rd clutches
6.08
6.17
6.21
2
6.33
6.25
6.38
100 $
8 18
g 15
0.0
80
0.5
1.0
Food concentration
1.5
2.0
60
fi
E
.kj
40
g
20
;
0
2
2.5
(mg C liter -‘)
Fig. 2. Comparative influences of food supply on mean clutch
size of breeding females (A), percentage of experimental females
breeding (B), and mean clutch size per female of population (i.e.
corrected for breeding proportions) (C) in M. meridianus and
T. spectabilis. Panel B also shows the comparative population
level fecundity (based on data in panel C) of M. meridianus
relative to T. spectabilis. Note different scales for T. spectabilis
and M. meridianus in panels A and C.
tomonas did not differ detectably between three successive clutches in either of two individual females of M.
meridianus tested (Table 2).
Food-duration responses of M. meridianus nauplii and
copepodites and of T. spectabilis nauplii were superficially
similar, reaching a lower asymptote at - 0.3 5 mg C liter - l
(Fig. 1). Copepodid durations of T. spectabilis, however,
continued declining with food supply to - 1 mg C liter-‘.
Fitted critical food supply levels (X,,,) were lower for M.
meridianus than for T. spectabilis, consistently so in respect to average durations (see Table 3). The X,,, values
indicate that the saturating food requirements for naupliar and copepodid development were roughly comparable in M. meridianus females, whereas roughly twice as
much food was required for naupliar as for copepodid
development in both sexes of T. spectabilis and in male
M. meridianus. Generalizing, these data indicate a greater
652
Hart
Table 3. Fitted parameter values for hyperbolic (or reciprocal hyperbolic) functions describing development times, body size and fecundity, and survivorship of Metadiaptomus
meridianus (Meta) and Tropodiaptomus spectabilis (Tropo) in relation to food supply. Regressions undertaken for average values at each food supply level rather than collectively for
all data points (see n values) are denoted as such (avg).
E
Nauplii
Male maturity
Female maturity
Nauplii (avg)
Male (avg)
Female (avg)
Male (avg)
Meta
Tropo
Meta
Tropo
Female (avg)
Clutch size (avg)
% breeding females
Nauplii (avg)
Copepodids (avg)
Overall (avg)
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
Meta
Tropo
x0
Durations
4.130
-0.041
2.013
-0.131
5.842
-0.009
4.076
-0.020
-0.066
3.284
-0.069
3.365
5.404
-0.037
-0.185
1.786
17.063
0.024
3.339
-0.062
9.296
-0.001
3.140
-0.084
Body size
1.946
-0.850
3.859
-0.481
2.152
-0.647
-0.502
3.308
Breeding
1.812
0.038
2.784
-0.050
0.046
7.902
-0.018
8.626
Survivorship
3.711
-0.052
4.112
-0.056
-0.023
10.381
24.675
0.030
4.713
0.011
7.075
0.023
yn-iin/
Y max
r2
n
x 90%
7.0
7.0
15.2
17.0
15.8
18.0
8.0
7.5
18.8
18.9
19.8
19.1
0.848
0.879
0.862
0.910
0.774
0.932
0.975
0.984
0.967
0.972
0.934
0.966
16
14
13
14
10
12
7
7
7
7
7
7
0.517*
1.013
0.385*
0.545
0.635
0.615
0.389*
1.104
0.159*
0.628
0.247*
0.649
1.01
1.11
1.40
1.30
0.847
0.925
0.878
0.965
7
7
7
7
0.333
0.215
0.423
0.194?
103.0
21.0
100.0
100.0
0.961
0.984
0.993
0.97 1
7
7
7
7
1.309
0.777-f
0.337
0.249t
44.0
97.0
83.0
100.0
34.0
89.0
0.473
0.841
0.892
0.919
0.666
0.909
7
7
7
7
7
7
0.568
0.504
0.199t
0.590
0.500
0.348-f
* Lower critical food requirement (X9,,) and corresponding potential competitive advantage
ofM. meridianus over T. spectabilis.
t Clear cases of converse advantage.
sensitivity to food limitation
pepodid life stages.
among naupliar
than co-
Breeding likelihood, fecundity, and body size in relation
to food supply- Clutch size understandably increased with
food availability,
but species-specific responses were
markedly different, both qualitatively
and quantitatively
(Fig. 2). Clutches of T. spectabilis were generally only
about a fifth as large as those of M. meridianus (Fig. 2A),
although egg production was less severely depressed at
low food levels in the former species. Comparative food
saturation levels for reproductive
output were roughly
twice as high in M. meridianus as they were in T. spectab&s, (Table 3).
Consideration of mean clutch size alone is somewhat
misleading in terms of overall population response. Figure 2B shows that the proportion of adult females actually
breeding was considerably depressed at low food levels
was more severe for M. merididifferences in
the clutch size-food supply relationship persist even when
mean clutch size is adjusted for this proportion of nonbreeding females (Fig. 2C). These are reflected most
prominently as changes in relative fecundity of M. meridianus compared to T. spectabilis (Fig. 2B; right ordinate). This ratio is based on the more realistic derived
population estimates plotted in Fig. 2C.
Food supply exerted a predictable positive influence on
body size for both sexes of both species (Fig. 3). Because
clutch size also increased with metasome length (Fig. 4),
the increases in mean clutch size with rising food supply
(Fig. 3) reflect both direct influences of food availability
on fecundity and indirect effects of food on adult size.
Relevant regression and partial correlation analysis statistics for these relationships are summarized in Table 4,
which reflects the controlling influence of body size. Surand that this reduction
anus than for T. spectabilis. Interspecific
653
Copepod growth and food supply
1.5
-z
Q3
]yetadiaptotnus
160 ,
120
meridianus
4
140 -
c,
-80
ZQ.1
I!
$j
.I
-60
;
3
c
-40
u
0
hfetadiaptomus
meridianus
4%
120 -
.fi 100 .
u)
q
=Y 606
q
0
n
‘818
-
60-
fe
BXA
d
nAu
3
mm
-20
0.0
1.5
0.5
1.0
Trop odiaptomus
1.5
2.0
20 .
2.5
0
-20
$
GJ
E 1.2
1
g 1.1
-15 ai
r
-10 B
,3
0
5: 1.0
3
g 0.9
-5
0.0
01.5
1.O
1.5
Food concentration
--A-
Males
-Females
2.0
prisingly, the influence of food supply on fecundity was
weak in T. spectabilis and insignificant for M. meridianus,
where food had to be forced into the multiple regression
(Table 4). In k’eeping with this, the partial effect of food
on fecundity ‘(i.e. controlled for, body size effects) was
considerably greater for T. spectabilis (partial correlation
coefficient of 0.189) than for M. meridianus (-0.00 1).
Survivorship - Naupliar, copepodid, and overall survival to maturity increased asymptotically with food supply in both species (Fig. 5) but was considerably lower in
all development categories of M. meridianus than in T.
spectabilis. Respective asymptotic survival values for
naupliar, copepodid, and overall development were - 50,
80, and 35% in M. meridianus and -90, 100, and 90%
in T. spectabilzs. In addition to their higher absolute levels, fitted asymptotic values were generally attained at a
lower food levlel in T. spectabilis than in M. meridianus,
with respective critical values for overall survival of 0.35
and 0.5 mg C liter-l (Table 3).
Although it is impossible to partition causality exactly,
routine culture inspections revealed that most mortality,
particularly in M. meridianus, arose through fungal parasitism. This is considered a somewhat artificial factor.
It was largely (and inexplicably) linked to the use of membrane-filtered lake water for preparation of culture media
and had been experienced independently by other work-
1
1
1.4
1.S
Q
Tropodlaptomus
spectabilis
.
n
aA
n
2.
A
-
*
.
3
‘5i 20 5
s 15 zs
IO5-
A
8
O1.1
1.0
Clutch size
SUPPlY.
1
1.3
25 -
2.5
Fig. 3. Mean male and female metasome lengths and clutch
sizes of M. meridianus and T. spectabilis in relation to food
I
1.2
.
30 -
(mg C liter ‘I)
--[I
I
1.1
-
YY
-3.4
f
1
1.0
25
spectabilis
l
40 -
1.2
1.3
1.4
Metasome length (mm)
l
2.5 mg C Ilter”
0
1.0 mg C liter-’
A
0.5 mg C liter”
v
0.2 mg C liter”
0
0.1 mg C liter”
A
0.05 mg C liter”
n
0.35 mg C liter”
Fig. 4. Clutch sizes of M. meridianus and T. spectabilis in
relation to parent metasome length at the food levels indicated
on the graphs.
ers in the MPI laboratories rearing Daphnia (D. C. Fiihlendorf pers. comm.) and various lotic invertebrates (J.
Adis pers. comm.). Handling losses were generally small,
although somewhat higher in M. meridianus than in T.
spectabilis in view of the former’s much smaller nauplii.
The survivorship values shown in Fig. 5 are accordingly
considered somewhat conservative, especially for M.
meridianus, but no objective basis exists for any upward
adjustment.
Food thresholdsfor eggproduction, population increase,
and development-Linear regression equations relating
potential female population breeding rate (R&, overall
population increase rate (Rpi), and individual growth rate
( l/Dtot) to food supply and the estimated food threshold
levels and interspecific equivalence points derived from
these relationships for each species are summarized in
Table 5. The predicted breeding thresholds and thresholds for population increase clearly overlap between M.
meridianus and T. spectabilis. Despite the interspecific
similarity in these thresholds, corresponding differences
in the response slopes were marked, leading to a 3-fold
faster progressive increase in reproductive advantage per
female (R,,) with rising food supply in M. meridianus
654
Hart
Table 4. Regression analyses of influences of food supply (mg C liter-‘)
(eggsper sac) and female body size measured as metasome length (mm).
on clutch size
Multiple linear regression of clutch size on body length and food supply. Significance levels
(P values) for the regression constant (a) and for regression coefficients for body size (b) and
food supply (c) are given below these respective values.
a
b
r2
n
c
Metadiaptomus meridianus
-242.8
231.6
187 -0.155”
0.564
P
0.0000
0.0000
0.9544
Tropodiaptomus spectabilis
-55.6
57.0
243
1.737
0.466
P
0.0000
0.0000
0.0027
Simple linear regression of clutch size on body length, disregarding food supply.
a
b
r2
P
n
M. meridianus
- 242.0
230.9
0.564
187
0.0000
T. spectabilis
-74.1
73.4
0.445
243
0.0000
Partial correlation coefficients for the respective effects of body size (controlled for food supply)
and of food supply (controlled for body size) on clutch size.
Clutch size on:
Length
Food
Controlling for:
Food
Length
hf. meridianus
T. spectabilis
0.655
0.443
-0.001
0.189
* Forced entry into the regression.
than in 7’. spectabilis (Fig. 6A). At the population level
(R,i, Fig. 6B), however, the interspecific difference was
broadly comparable up to 0.5 mg C liter-l. Average
threshold values for population increase were marginally
higher than those for breeding, but differences were not
significant either within or between species.
Food threshold level estimates for development were
considerably lower on average than those for breeding or
population increase, but no differences were significant.
As with the functional breeding responses, the interspecific growth thresholds also clearly overlap (Table 5). But
in view of the interspecific similarity in slope of the development time response, no progressive advantage accrues to either one of the species pair with rising food
supply (Fig. 7).
Discussion
General-Despite differences in magnitude, particularly in respect to reproductive output (clutch size), the
overall response patterns of both species were broadly
comparable functions of food quantity. Some influences
of food quality on development time were also evident
(Table l), and thus qualitative influences on other functional responses cannot be disregarded. However, with
the lack of further information on such qualitative effects,
the subsequent account focuses on the influences of food
quantity on potential competitive advantage. This appraisal is couched partly in terms of r and K selection,
notwithstanding the recognized deficiencies of this continuum (Begon et al. 1990). i&f. meridianus shows more
of the familiar demographic and life-history attributes
associated with an r-selected species, while T. spectabilis
appears more K selected (see Hart 1994a). Parameter
values of the hyperbolic functions describing durations,
body sizes, fecundity, and survivorship in relation to food
supply, along with the estimated critical saturating food
levels (XgoVO:
Table 3), provide a further numerical basis
for interspecific comparisons.
Development times--M. meridianus clearly develops
faster than T. spectabilis across the range of food levels
tested. This potential advantage is especially evident at
food levels below 0.5 mg C liter-l (Fig. 1C). However,
as development time is determined jointly by temperature and food supply (Hart 1990, 199 l), both factors must
be included in the consideration of demographic advantage.
As noted in the introduction, T. spectabilis is more
thermophilic than M. meridianus. Much of the apparent
advantage of faster development in M. meridianus reported here is accordingly attributable to the cool temperature (17°C) used to reduce fungal infection. But food
effects per se were also evident at this temperature: M.
meridianus developed relatively much faster than T. spectabilis at food levels below 0.5 mg C liter-l in particular
(Fig. 1C). While faster growth is a predictable r-selected
trait, the apparent enhancement of this advantage at low
resource levels is surprising in terms of classical r-K theory. Yet Table 3 indicates the saturation (X,,,) of development time responses of M. meridianus at much lower food levels than T. spectabilis, with one exception: a
slightly higher X,,, level in respect to female D,,, values.
Apart from this, the interspecific food requirements for
naupliar and copepodid development were qualitatively
quite uniform: more food (up to twice as much) was required to saturate naupliar than copepodid development.
655
Copepod growth and food supply
3100 - A.
5
I 80
.
A/
l’ A’
/cc
*-
- --
- - ___----
liA
. Al
0
+
Metadiapfomus
-A-
Tropodiaptomus
l
‘&
a 0.0
I”“I”“I”“,““‘,““I
g
. . 100
8
’ 80
E
-+-
?
P
h
.f
8
s
fg
hfetadiaptomus
1.2
1.0
0.8
0.8
0.4
0.2
0.0
0.0
-A-
yoo c.
..
8I 80
1 , /‘A---f
3
.I
60
;
ii
40
s
5
20
B
0
0.0
0.5
Tropodiaptomus
- --
A,d”----
--O-
Metadiaptomus
-A-
Tropodiaptomus
1.0
Food concentration
1.5
2.0
A
0.5
----O-
Metadiaptomus
-A--
Ttwodiaptomus
1.0
1.5
2.0
0.8 .k
0.6 -E
0.4 8
0.2 8
2.5
Food concentration (mg C liter -I)
Fig. 6. Comparative plots and fitted regression lines of daily
egg production rates in relation to food supply in hf. meridianus
and T. spectabilis. A. Per adult female (Rpb note different scales
for M. meridianus and T. spectabilis). B. Per individual of population (R,i). Fitted regressions exclude points shown as open
symbols.
natural populations (Hart 1994a) are consistent with the
designation of M. meridianus as an r-selected species,
while saturation of the fecundity-food supply response at
lower food levels in T. spectabilis (X90V0values in Table
3) is consistent with the higher resource utilization efficiency expected of a designated K-selected species.
Individual eggs differ markedly in size between these
species, with respective volumes of 0.486 x 1O-3 and
2.5
(mg C liter -I)
O-O7
I
Fig. 5. Influences of food supply on percentage survival of
naupliar stages (A), copepodid stages (B), and overall survival
to maturity (C) in M. meridianus and T. spectabilis.
A similar pattern obtained in parallel studies on Eudiaptomus gracilis (Santer 1994) suggests even wider interspecific consistency in this regard, which may be attributable to qualitative differences in optimal food types for
naupliar and copepodid life stages, ontogenetic changes
in feeding effic:iency, or both.
Metadiaptomus
-A-
Tropodiaptomus
-I
0.0
Fecundity and reproductive output -Significantly
greater clutch size in M. meridianus than T. spectabilis
in this study (Fyigs.3 and 4) and correspondingly greater
multiannual averages of 33.7 and 8.8 eggs clutch-l in
-O-
0.5
1 .O
Food concentration
1.5
2.0
2.5
(mg C liter ‘I)
Fig. 7. Influence of food supply on maturation rates of M.
meridianus and T. spectabilis females.
656
Hart
Table 5. Linear regression statistics relating breeding effort (Q, eggs female-’ d-l) and
potential rate of population incrase (Rpi, eggsind.-’ d-l) to food availability (F, mg C liter-l)
and the reciprocal of total female development time (1/D,,,, days) to log,,-transformed values
of food availability. Food thresholds for breeding, population increase, and individual development derived from these regressions are given, along with corresponding interspecific
equivalence levels (breakpoints). Superiority reflects the species with the potential advantage
below the breakpoint food level.
Regression parameters for the named responses
a+SE
b+SE
r2
n
F
Breeding effort (R,J
M. meridianus
-0.344kO.135
5.188kO.276
0.989
6
352.9
T. spectabilis
-0.054+0.039
1.634kO.136
0.980
5
145.2
Population increase (R,i)
M. meridianus
-0.156+0.052
1.812+0.107
0.986
6
284.9
T. spectabilis
-0.087+0.037
1.395kO.127
0.976
5
120.1
Development time ( 1/D,,,)
M. meridianus
0.05 1kO.003
0.022 kO.004
0.904
6
37.7
T. spectabilis
0.050+0.002
0.026 kO.003
0.960
6
96.3
Derived food thresholds (pg C liter- I)
Threshold for breeding or egg production (&, R & 95% C.L.)
M. meridianus
59.7-t 134.8
T. spectabilis
17.7+ 125.6
Threshold for population increase (Rpi, X + 95% C.L.)
M. meridianus
78.5k149.1
T. spectabilis
45.8f 135.1
Threshold for individual growth or development (l/D,,,, X and 95% C.I.)
95% C.I.
M. meridianus
4x.9
0.1-24.4
T. spectabilis
10.9
2.4-30.2
Interspecific equivalence levels (breakpoints) at 17°C
Food
level
Superiority
Egg production (breeding) (&)
82
Tropodiaptomus
Population increase (R,i)
165
Tropodiaptomus
Metadiaptomus (at all food levels)
Individual development (1/Q,J
-
0.06
0
l
A
a
:
*
0
Metadiaptomus
A
Tropodiaptomus
A
0.00
AO
A-a I I .,’
0.0
0.5
,‘,(,,,,,,,1,,,,,,,
1.0
Food concentration
I .5
2.0
2.5
(mg C liter -I)
Fig. 8. Total reproductive output of M. meridianus and T.
spectabilis in relation to food supply, Points lying above the
estimated response saturation level are open.
1.46 x 1O-3 mm3 in M. meridianus and T’.spectabilis (Hart
1994a)-also consistent with their r- and K-selected de+
ignations. However, on the simplifying assumption that.
egg volume is independent of food supply, application of
the above egg volumes to the fecundity-food supply response reported in Figs. 3 and 4 indicates that total re-,
productive output (egg volume x clutch size) is almost,
indistinguishable between these species (Fig. 8), certainly
at food levels below 0.5 mg C liter- l. Thus, greater pa-,
rental investment is not realized on a per brood basis,
despite its reality in terms of investment per individual
offspring.
Survival: A demographic leveler?- Despite greater fe-e
cundity in the r-selected M. meridianus, interspecific differences in developmental mortality (fungal parasitism in
particular) impose an overall demographic similarity. Al-.
though fungal parasitism may be construed as an artificiall
mortality factor of these experimental populations, its
primary manifestation in only one of the introduced spe-
Copepod growth and food supply
ties pair is notable. Does this reflect the weaker status of
M. meridianus than T. spectabilis or simply interspecific
differences in fungal specificity? As noted in the introduction, the host species are representatives of different
subfamilies of the Diaptomidae, differing in global distribution. On this biogeographical basis, the presumed
paleoarctic fungal parasite might be expected to show
lower specificity for the Ethiopian M. meridianus, although conversely the paradiaptomid is less likely than
the diaptomid to have evolved appropriate counterstrategies. The question is circular and unanswerable, but I
assume that higher fungal mortality simply reflects the
weaker status of M. meridianus, and this levels the demographic performance of the two taxa.
Implications to seasonal periodicity and succession of
natural populations- Competitive exclusion cannot be
disregarded as a causal factor underlying the fairly consistent pattern of seasonal alternation in dominance of
these calanoid;s observed in Albert Falls (Hart 19946) as
well as two episodes of complete replacement of T. spectabilis by M. rneridianus (for 5 yr or longer) in Midmar
(King et al. 1986; Hart 1994a) (see introduction). However, experimental results reported here strongly indicate
that any potential competitive advantage between the
species in terms of their respective resource utilization
responses is re.latively slight. The various food thresholds
and food level-response profiles considered here (Table
5) differ only slightly and insignificantly between species.
Viewed against an overall similarity in abundance levels
and temporal variability of chlorophyll, of algal density,
and of qualitative composition of phytoplankton in Midmar and Albe:rt Falls (Hart 1992, 1996), neither the recurrent seasonal replacements of M. meridianus and T.
spectabilis in Albert Falls nor their episodic switches in
Midmar are readily explicable simply in terms of gross
nutritional quantity or quality.
However, given the slight resource utilization superiority of T. spectabilis reported here, evidenced particularly in the saturation of its fecundity and developmental
survivorship responsesat lower food levels, declining food
supply during the spring-summer transition plausibly
contributes to the seasonal dominance switch between M.
meridianus and T. spectabilis in Albert Falls at this time
(Hart 1994a). .4lthough evidence is not unequivocal, rapid growth does)seem to compromise the ability to survive
and reproduce when food resources are scarce (DeMott
1989). However, this switch is more likely driven by rising temperatures acting in concert with declining food
supply, rather than in response to the latter effect alone.
The replacement of faster growing r-selected M. meridianus by the slightly more efficient K-selected competitor,
T. spectabilis, is generally in keeping with a seasonal alternation between density-independent (temperature-dependent) and density- (food-) dependent growth (Koch
1974; Huston 1979) combined with a temperature-associated shift in competitive ability (Sandercock 1967;
Hart 1994b). .Available evidence indicates that temperature-related shifts exert the greatest influence in the seasonal replacement of these species.
657
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Submitted: 5 January 1994
Accepted: 22 November 1995
Amended: 7 March 1994