474 Acta hydrochim. hydrobiol.

2006, 34, 474 – 479

Research Paper
Ratio of neonate to adult size explains life history
characteristics in cladoceran zooplankton

S. Nandinia, S. S. S. Sarmab

a
Divisi
n de Investigaci
n y Posgrado, UIICSE, Universidad Nacional Aut
noma de Mxico, Tlalnepantla,
Edo. de Mxico, Mxico
b
Laboratorio de Zoologa Acutica, Divisi
n de Investigaci
n y Posgrado, Edificio UMF, Universidad Nacional
Aut
noma de Mxico, Tlalnepantla, Edo. de Mxico, Mxico

The size ratio of adults to neonates varies greatly in cladocerans across taxa. In this study we
tested the impact of this ratio (using length basis) on the selected life history parameters of nine
species of freshwater cladocerans (Alona rectangula, Pleuroxus aduncus, Scapholeberis mucronata,
Moina macrocopa, Moina wierzejskii, Ceriodaphnia dubia, Daphnia laevis, Diaphanosoma birgei and
Daphnia pulex). Experiments were conducted on a mixed diet of Chlorella vulgaris (1.0 N 106 cells
mL – 1) and Scenedesmus acutus (0.5 N 106 cells mL – 1) at (22 l 1)8C. Using a cohort life table experi-
mental design, we quantified age-specific reproductive output. Body sizes of neonates and adults
as well as dry weight were determined using standard procedures. We found that the ratio of
neonate to adult body length decreased with increasing body size of the adult. In terms of clutch
size, however, smaller taxa produced lower numbers of offspring than larger ones. The influence
of ratio neonate/adult size on average lifespan, age at first reproduction and at the maximum
clutch showed U-shaped curves. In smaller taxa (a 700 lm) and larger taxa (A 1500 lm) the ratio
between the neonate and adult body size was less than 0.4 or more than 0.6. In medium sized
taxa (1000…1500 lm), the ratio of neonate to adult size was between 0.4 and 0.6. The results
have been discussed in relation to the life history strategies of cladocerans.

Keywords: Dry weight / demography / Cladocera / fecundity / lifespan /

Received: March 3, 2006; accepted: July 7, 2006

DOI 10.1002/aheh.200600642

1 Introduction mother is not a limiting factor while in ovoviviparous

Body size is an important attribute in explaining the life
history characters in animals, particularly those related
to reproduction [1, 2]. Among various taxa, different rela-
tions between offspring size and litter size are evident.
However, the lack of standard offspring number per
female across a wide spectrum of aquatic animal groups
has been attributed to various factors such as size of the
neonates [3, 4]. Oviparous animals normally produce
more offspring since the size of the brood chamber in the
Correspondence: S. Nandini, Divisi
n de Investigaci
n y Posgrado,
UIICSE, Universidad Nacional Aut
noma de Mxico, Campus Iztacala,
AP 314, CP 54090, Tlalnepantla, Edo. de Mxico, Mxico
E-mail: nandini@servidor.unam.mx
Fax: +52 5 6231256
organisms, the offspring must be retained within the
mother for a much longer duration and hence there is a
space constraint [5]. Fish species that reproduce ovipar-
ously may release several millions of eggs per female; on
the other hand those that reproduce viviparously pro-
duce only a fraction of this number [6]. In these cases, the
size of the neonate at birth is important. There appears
to be a positive relation between the size of adults and
the maximum number of offspring released at a time [7].
In ovoviviparous species such as Daphnia offspring may
be as large as 10% of the adult size [8]. This wide disparity
is one the cornerstones of life history theories [9, 10].
Cladocerans reproduce both parthenogenetically and
sexually. When reproducing parthenogenetically, they
release the offspring as miniature, but reproductively
immature ones. The number of neonates per reproduc-

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Acta hydrochim. hydrobiol. 2006, 34, 474 – 479
tion (clutch size) ranges between 2 to 100 depending on
the cladoceran taxa [11]. Many factors (food concentra-
tion, temperature, predation etc.) are known to influence
this number, but the body size of adults, neonates or
their ratios is rarely utilized as an explanation [12 – 14].
Among different animal taxa, there exists a positive rela-
tion between the size of offspring at birth and their survi-
vorship [15]. The investment of each female into few,
large offspring or many small ones is also known to be
influenced by crowding and predation. Growth rate,
length and the size of the first clutch of small Daphnia
(a 1.8 mm) are known to decrease under overcrowded
situation with conspecifics [16]. It has been shown that
Daphnia magna produces more but less healthy offspring
(lower triglyceride content in the eggs) when grown in
water with fish kairomones [17]. Among Daphnia, experi-
ments with infochemicals show that in the face of inver-
tebrate predation pressure, females switch from produ-
cing many small offspring to a few large ones, while the
reverse is true in the presence of vertebrate predation
pressure [18]. Information on other cladoceran genera is
scarce.
Among the various families of Cladocera, species diver-
sity is known to be highest in littoral ones particularly
the Chydoridae [11]. While considerable information
exists on pelagic families, particularly the Daphniidae,
much less is known about the demographic characteris-
tics of the Chydoridae [19]. In order to reach generaliza-
tions on the life history strategies, it is important to
study various taxa under similar test conditions. In this
study, we cultured nine species of freshwater cladocerans
(Alona rectangula, Pleuroxus aduncus, Scapholeberis mucro-
nata, Moina macrocopa, Moina wierzejskii, Ceriodaphnia
dubia, Daphnia laevis, Diaphanosoma birgei and Daphnia
pulex) under standard test conditions [20, 21] and quanti-
fied their age-specific reproductive output in relation to
the body length and weight of the adults and neonates.
2 Materials and methods
The test species used in this study were isolated from
local water bodies. Cultures maintained in 2 L beakers
were established from a single female. All the cladocer-
ans were maintained using EPA medium, which was pre-
pared by adding 0.9 g of NaHCO3, 0.6 g of CaSO4, 0.6 g of
MgSO4 and 0.04 g of KCl in one liter of distilled water [22]
under standard test conditions of (22 l 1) 8C, pH 7.0…7.5,
and constant but diffuse fluorescent illumination. The
chlorophytes, Chlorella vulgaris and Scenedesmus acutus
were used as food in this study. These algae were main-
tained on Bold’s basal medium [23]. The algae were sepa-
i 2006 WILEY-VCH Verlag GmbH & Co. KGaA, Weinheim
Body size ratio and cladoceran life histories 475
rately centrifuged, concentrated, and quantified using a
Neubauer haemocytometer.
We conducted life table demographic experiments
separately for each species, starting with neonates of
a 24 h age. Experiments were carried out in 100 mL glass
jars with 50 mL of test medium in each (mixture of algae
in EPA medium). The medium was prepared using the
algae Chlorella vulgaris (0.5 N 106 cells mL – 1) and Scenedes-
mus acutus (0.25 N 106 cells mL – 1) in a 1 : 1 ratio in terms of
algal biomass (0.0142 ng and 0.025 ng per cell, respec-
tively), which in terms of carbon gave a final concentra-
tion of 3.8 lg mL – 1 C [21]. We set up four replicate
(cohorts) jars for each species into each of which was
introduced a cohort of five neonates. A total of 36 test ves-
sels (9 species64 replicates) was run. Living individuals
of the test population in each jar were counted daily and
subsequently transferred to new containers with fresh
medium and algal diet. Neonates and dead adults, when
present, were enumerated and discarded. Experiments
were continued until the last individual of each cohort
died. The demographic variables from the basic survivor-
ship and reproduction data were calculated using the fol-
lowing formulae [15]:
Gross reproductive rate (GRR, offspring female – 1)
X
v
GRR ¼ mx ð1Þ
0
Net reproductive rate (R0, survival weighted offspring
female – 1)
X
v
R0 ¼ lx N m x ð2Þ
0
Generation time (T, d)
X
lx N mx N x
T¼ ð3Þ
R0
Rate of population increase (r, d – 1), Euler equation
(solved iteratively)
X
n
e
rx N lx N mx ¼ 1 ð4Þ
x¼w
In these equations, lx is the probability of an individual
surviving to an age class, mx is the age specific fecundity,
Ro is the average number of female offspring each female
in the population produces, and r is the growth rate of
the population.
In order to estimate the length-weight relationship of
the adults and neonates of each species we separated the
30…40 neonates on a single day from the test jars during
the experiment. These were divided into three replicates
and were maintained in the same test medium and condi-
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476 S. Nandini et al. Acta hydrochim. hydrobiol. 2006, 34, 474 – 479

Table 1. Life history variables of tested cladocerans species. ALS: average lifespan, d; E0: life expectancy at birth, d; GRR: gross
reproductive rate, offspring female – 1; NRR: net reproductive rate, survival-weighted offspring female – 1; T: generation time, d; r: rate
of population increase, d – 1. Values represent mean l standard error based on four replicates (cohorts).

Species Life history variable

ALS E0 GRR NRR T r

A. rectangula 35.0 l 5.3 34.5 l 5.3 46.8 l 6.2 28.25 l 4.9 23.4 l 2.3 0.26 l 0.03
C. dubia 38.2 l 5.5 37.7 l 5.5 175.0 l 19.9 127.1 l 19.7 22.9 l 1.6 0.42 l 0.02
D. birgei 24.3 l 1.4 23.8 l 1.4 51.8 l 6.0 32.4 l 3.9 17.4 l 1.3 0.28 l 0.01
D. laevis 19.1 l 1.5 18.6 l 1.5 24.7 l 4.3 17.4 l 3.0 14.0 l 0.9 0.23 l 0.01
D. pulex 38.4 l 4.8 37.9 l 4.8 190.3 l 33.8 171.1 l 41.7 23.8 l 2.0 0.37 l 0.01
M. macrocopa 10.4 l 0.9 9.9 l 0.9 83.2 l 16.8 56.7 l 8.5 6.9 l 0.4 0.74 l 0.01
M. wierzejskii 6.0 l 0.3 5.5 l 0.2 37.5 l 4.4 24.1 l 3.5 4.8 l 0.1 0.71 l 0.04
P. aduncus 31.7 l 0.8 31.2 l 0.8 19.6 l 2.2 12.8 l 1.2 21.4 l 1.1 0.15 l 0.01
S. mucronata 18.0 l 1.5 17.5 l 1.5 63.2 l 8.8 30.6 l 4.0 14.2 l 1.5 0.38 l 0.04

tions as in the life table study. We analyzed the length-

weight relationship by separating 10…20 individuals, a
few from each replicate, in order to avoid pseudoreplica-
tion. Small aluminium foil cups were weighed previously
in a Cahn 33 Electrobalance with a precision of 1 lg. Each
individual was measured in a microscope using a micro-
meter and then placed on a marked and pre-weighed foil.
These were then placed in an oven set at 608C [24]. After
24 h the petri dish containing the foils was removed,
placed in a desiccator in order to prevent absorption of
moisture and weighed. Corrections were made for
changes in the foil weight. Neonates were measured
within 24 h of their birth, and adult females at the age of
first reproduction (neonates present in the brood cham-
ber were gently squashed and removed prior to weighing).
Data were analyzed using F-tests and regression ana-
lyses following standard literature [25].

Figure 1. Age-specific survivorship (lx) (proportion, d) and

3 Results
The survivorship and fecundity curves of the test species
are shown in Figure 1. The survivorship curves were gen-
erally of Type 1, with steep slopes in Alona rectangula and
Scapholeberis mucronata. Daphnia pulex on the other hand
had low mortality for around 30 days after which it
showed a sudden and precipitous decline. Data on the
selected life history variables of the test species are pre-
sented in Table 1. The average lifespan was highest in Cer-
iodaphnia dubia and lowest in Moina wierzejskii. The gross
and net reproductive rates were highest in the daphnids
(Ceriodaphnia dubia and Daphnia pulex) and lowest in
Pleuroxus aduncus. Generation time was lowest (4…6 d) in
Moina macrocopa and M. wierzejskii, while population
growth rate (r) was highest in Moina (about 0.7 d – 1) and
lowest in P. aduncus (a 0.2 d – 1) (Table 1).
fecundity (mx) (offspring female – 1) curves of different cladoceran
species. Shown are the values mean € standard error based on
four replicates (cohorts).
The length of the cladocerans, both concerning neo-
nates and adults was significantly correlated with weight
(Fig. 2). Between the smallest and largest taxa, there was a
three-fold difference in the length as neonates and five-
fold difference as adults; in terms of weight, however
there was an 8-fold difference across the taxa, as neonates
or as adults. The ratio of neonate to adult body length
decreased with increasing body size of the adult (Fig. 3).
There were no significant correlations between adult or
neonate length or weight alone with life history vari-
ables. However, we found significant U-shaped relations
between the ratio of neonate and adult length (which
was greater in smaller than in larger cladoceran taxa)

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Acta hydrochim. hydrobiol. 2006, 34, 474 – 479 Body size ratio and cladoceran life histories 477

Figure 3. Relation between cladoceran body length vs the ratio

of neonate/adult lengths (coefficient of correlation, r 2 = 0.86,
p a 0.01). Plotted were the mean data for each species.

Figure 2. Length-dry weight relation of tested cladoceran spe-

cies. A: neonates (coefficient of correlation, r 2 = 0.44, p a 0.01);
B: adults (coefficient of correlation, r 2 = 0.58, p a 0.01). For each
species replicated data were plotted. Note the differences on the
scaling of both x and y axis.

and variables such as average lifespan, age at first clutch

and maximum clutch size. The neonate to adult length
ratio was inversely related to maximum offspring pro-
duction and net reproductive rate. In terms of the clutch
size, however, smaller taxa produced lower number of
offspring than larger taxa (Fig. 4). There was also a signifi-
cant positive relation between generation time and
mean lifespan.

4 Discussion
Life table experiments on zooplankton typically start
with neonates of known age. Many cultured zooplankton
species show little mortality during the first few days
and subsequently begin to die rapidly due to aging.
When the survival is plotted as function of age, the survi- Figure 4. Relation between the ratio of neonate to adult size
and the selected life history variables (A – E) of some cladoceran
vorship curves roughly appear rectangular (also called species. F: Relation between mean lifespan and generation
Type 1) [15]. However, depending on the stress including time.

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478 S. Nandini et al.
suboptimal food conditions, the survivorship curves devi-
ate from the ideal Type 1. Thus zooplankton under stress
may experience a certain mortality throughout their life-
span (Type 2) or heavy mortality in younger age-groups
(Type 3) [20]. In the present work, most species had survi-
vorship close to Type 1 pattern.
The influence of ratio neonate/adult size on some life
history variables such as average lifespan, age at first
reproduction and at the maximum clutch showed U-
shaped curves. In smaller taxa (a 700 lm) and larger taxa
(A 1500 lm) the ratio between the neonate and adult
body size was less than 0.4 or more than 0.6. In such spe-
cies there is a longer time of maturation, longevity and
peak reproductive output [20]. On the other hand, me-
dium sized taxa (1000…1500 lm), where the neonate to
adult ratio was between 0.4 and 0.6, have a shorter life-
span and correspondingly shorter time is needed to
reach maximum reproductive output. Thus, in aquatic
ecosystems where cladocerans are subject to both inver-
tebrate and vertebrate predation pressure [18], the most
favored size group would be in the range of 1000…1500
lm.
There seems to be the minimum body size of the neo-
nate for carrying out functions of a multicellular organ-
ism. Due to this limit, smaller taxa do not have the same
peak clutch size as the larger taxa. The ratio of neonate to
adult size also explains this better than either of the two
separately. The number of offspring per clutch as well as
the net reproductive rate also increased with increasing
body size of the adult and was inversely related with the
ratio of neonate to adult body length. This suggests that
more neonates are produced by larger rather than smal-
ler taxa [11]. Zooplankton species, which are ovovivipar-
ous, are constrained by the size of the brood chamber.
Increase in the size of the brood chamber with increasing
body size has also been documented for many cladocer-
ans [8]. For instance, certain species of Daphnia can pro-
duce up to 1000 offspring per female in their life span
while chydorids, although having the same lifespan [26]
produce only 30 individuals [11]. This is because of the
greater investment by the mother in large sized offspring
in smaller taxa but in many offspring in larger ones [27].
King [28] detected the existence of a direct relation
between generation time and mean life span. He
hypothesized that for iteroparous organisms, the life
span is twice the generation time. In the present study,
though a direct relation between the lifespan and genera-
tion time indeed existed, their ratio was around 1.5. Such
deviations have been documented for various zooplank-
ton species [26, 29]. We also observed an inverse relation-
ship between the age at first reproduction and the gross
reproductive rate in all the taxa with the exception of
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Acta hydrochim. hydrobiol. 2006, 34, 474 – 479
Daphnia pulex and Ceriodaphnia dubia where the neonate
production was higher. Roff [30] has also stated that there
should be a negative relation between the development
time and neonate production in organisms, although lit-
tle information has been documented on this aspect.
Across the animal kingdom, it has been shown that
females that invest more for each one in the offspring
have fewer but healthy individuals per clutch, and thus
conferring greater probability of survival to the young
[31]. While higher offspring production is a factor influ-
encing r (rate of population increase d – 1) of a given spe-
cies, the impact of neonates' survival is rarely considered
[10]. In our study, we found that this relation was lowest
in large sized species and highest in the small sized ones
such as chydorids. Since species in the littoral region also
experience strong predation pressure, it needs to be stud-
ied if a larger sized neonate in relation to the adults
indeed ensures greater survivorship capabilities to the
littoral taxa.
Body size has been inversely correlated to diversity in
plants, birds and terrestrial mammals [32, 33]. Orme et al.
[34] however did not find such a relationship across sev-
eral taxa (Cladocera not included). Earlier age at maturity
appears to contribute to greater species diversity in cer-
tain groups [33]. Such a relation was not observed in our
study. For example, Chydoridae is amongst the most
diverse in Cladocera, but we found that Alona and Pleur-
oxus had much longer age at maturity (8…10 d), while
Moina had the shortest. It remains to be tested whether
diversity is higher in families where there is a larger neo-
nate:adult ratio (which may confer greater probability of
species survival).
Two anonymous reviewers and Dr. Wolf von T
mpling have
improved our presentation. We also thank the authorities of
UNAM Campus Iztacala for facilities and PAPIIT (IN210205&
IN219405) for financial support.
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