Life history and population dynamics of the marine cladoceran Penilia avirostris (Branchiopoda: Cladocera) in the Catalan Sea (NW Mediterranean)

Abstract

Penilia avirostris is a cosmopolitan marine cladoceran that inhabits coastal and shelf waters of most low and mid latitude ecosystems. In this study, we describe the life history and population dynamics of P. avirostris at a fixed coastal station in the NW Mediterranean Sea. This marine cladoceran was very seasonal, having population maxima in summer (2500-3000 ind m(-3)), and being practically absent from the water column for the rest of the year. The population typically collapsed in late summer-early autumn, and this decline was accompanied by a shift to gametogenetic reproduction, allowing the production of resting eggs to ensure the continuity of the species in the following season. Estimated birth rates of P. avirostris in the Catalan Sea ranged between 0.097 and 0.46 day(-1) and seemed to be decoupled from changes in P. avirostris standing stocks. Birth rates were mainly dependent on the changes in abundance of embryo-carrying females and their brood size, because during the period of population plateau the temperature-dependent embryonic developmental time was rather similar (2.3-2.7 days). Neonates are like miniature adults and need a very short period of growth and moulting to reach the reproductive stage. This life-history trait can explain the fast blooming and dominance of plankton communities by P. avirostris under suitable conditions. Finally, the causes for the seasonal decline of P. avirostris populations are also discussed.

Full text

Life history and population dynamics of
the marine cladoceran Penilia avirostris
(Branchiopoda: Cladocera) in the
Catalan Sea (NW Mediterranean)
D. ATIENZA1*, E. SAIZ1, A. SKOVGAARD2, I. TREPAT1AND A. CALBET1
1
INSTITUT DE CIE
`NCIES DEL MAR (CSIC), PASSEIG MARI
´TIM DE LA BARCELONETA 37-49,08003 BARCELONA,SPAIN AND
2
DEPARTMENT OF BIOLOGY,SECTION
OF PHYCOLOGY
,UNIVERSITY OF COPENHAGEN,ØSTER FARIMAGSGADE 2D,DK-1353 COPENHAGEN,DENMARK
*CORRESPONDING AUTHOR: datienza@icm.csic.es
Received December 13, 2007; accepted in principle December 13, 2007; accepted for publication December 18, 2007; published online
February 1, 2008
Corresponding editor: Roger Harris
Penilia avirostris is a cosmopolitan marine cladoceran that inhabits coastal and shelf waters of
most low and mid latitude ecosystems. In this study, we describe the life history and population
dynamics of P. avirostris at a fixed coastal station in the NW Mediterranean Sea. This marine
cladoceran was very seasonal, having population maxima in summer (2500 –3000 ind m
23
),
and being practically absent from the water column for the rest of the year. The population typi-
cally collapsed in late summer – early autumn, and this decline was accompanied by a shift to
gametogenetic reproduction, allowing the production of resting eggs to ensure the continuity of the
species in the following season. Estimated birth rates of P. avirostris in the Catalan Sea ranged
between 0.097 and 0.46 day
21
and seemed to be decoupled from changes in P. avirostris standing
stocks. Birth rates were mainly dependent on the changes in abundance of embryo-carrying females
and their brood size, because during the period of population plateau the temperature-dependent
embryonic developmental time was rather similar (2.3 – 2.7 days). Neonates are like miniature
adults and need a very short period of growth and moulting to reach the reproductive stage. This
life-history trait can explain the fast blooming and dominance of plankton communities by P. avir-
ostris under suitable conditions. Finally, the causes for the seasonal decline of P. avirostris popu-
lations are also discussed.
INTRODUCTION
Cladocerans play a major role in freshwater ecosystems
(Richman, 1958; Lampert, 1987), but have not been
very successful in colonizing the marine environment.
Such colonization requires the evolution of adaptation
mechanisms at the morphological, physiological and
behavioral level (Critescu and Hebert, 2002). The
acquisition of a closed brood pouch to keep the
embryos in a suitable nourishing environment, the pre-
sence of a resting egg provided with a thick wall instead
of an ephippium and the predatory grasping mode in
most species instead of filter-feeding seem to be essential
features linked to this colonization by cladocerans
(Lochhead, 1954; Aladin and Potts, 1995; Critescu and
Hebert, 2002). In this sense, P. avirostris is a rarity within
marine cladocerans for being the only filter-feeding
representative, in clear contrast to the broad presence of
this feeding strategy in freshwater cladocerans.
Penilia avirostris is a seasonally abundant and widely
distributed cladoceran in neritic tropical and subtropical
waters, expanding its distribution towards northern tem-
perate latitudes since the mid-20th century (Lochhead,
doi:10.1093/plankt/fbm109, available online at www.plankt.oxfordjournals.org
#The Author 2008. Published by Oxford University Press. All rights reserved. For permissions, please email: jour nals.permissions@oxfordjournals.org
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1954; Della Croce and Venugopal, 1973; Johns et al.,
2005). When abundant, P.avirostris may play an import-
ant role in marine food webs by concentrating organic
energy of small plankton and making it available to
consumers at higher trophic levels (Paffenho
¨fer and
Orcutt, 1986; Turner et al., 1988; Atienza et al., 2006a).
In this regard, previous field work showed that P.aviros-
tris feed on a wide range of prey, mostly nanoplankton
(2–20 mm), but also larger cells such as dinoflagellates
and diatoms (Atienza et al., 2006a). Moreover, P.avirostris
plays an important role in the recycling of nutrients in
the upper water column, actually contributing to the
limitation by P to phytoplankton growth by excreting
only N derivatives (Atienza et al., 2006b).
In spite of the relevance of this species in the biogeo-
chemical cycles, the information about its population
dynamics is mostly limited to their abundance and sea-
sonal distribution (Della Croce, 1964; Onbe
´and Ikeda,
1995; Tang et al., 1995; Marazzo and Valentin, 2003a;
Valentin and Marazzo, 2003; Wong et al., 2004). These
studies revealed that the temporal distribution of marine
cladocerans is discontinuous during the year, with peaks
of very high abundance followed by rapid decline and
eventual absence from the plankton. Until now, the
factors controlling this pattern remain unclear. Some
authors suggest that temperature may play an important
role in the population dynamics of P. avirostris (Onbe
´and
Ikeda, 1995); however, other factors such as food avail-
ability, chemical composition of seston and photoperiod
might be also relevant (Egloff et al., 1997).
Although the general pattern of its population seaso-
nal cycle is known, the difficulty of rearing these organ-
isms in the laboratory has complicated the estimation of
most of their reproductive parameters (Della Croce,
1964; Tang et al., 1995; Marazzo and Valentin, 2003b;
Wong et al., 2004). The life cycle of P. avirostris is charac-
terized by an alternation between gamogenesis and
parthenogenesis. Their populations are initiated by the
hatching of resting eggs, followed by peaks of high
abundance when parthenogenetic females reproduce
(Onbe
´, 1973, 1978). In marine cladoceran populations,
gamogenetic individuals usually appear immediately
after population maxima, coinciding with decreasing
parthenogenetic reproduction. Gametogenetic repro-
duction produces resting eggs, which sink and remain
on the sea bottom during the seasonal disappearance of
the parental population from the water column (Onbe
´,
1985; Egloff et al., 1997).
The general trend of population dynamics of P. aviros-
tris, briefly described here, resembles that of many fresh-
water cladocerans (Threlkeld, 1987). However, in
contrast to them, we lack deep knowledge about the
reproductive characteristics of P.avirostris at each of the
different phases of its seasonal cycle. Consequently, our
objective was to study the seasonal distribution of the
population of P.avirostris in the Catalan Sea (NW
Mediterranean), taking special care to describe in detail
the reproductive condition of the females during the
seasonal cycle. We believe that certain aspects of P.avir-
ostris life cycle should contribute to explain the explosive
growth and sudden disappearance of this species from
the water column. We also discuss here the influence
that some biological and physical factors could have on
the temporal variation of this species.
METHOD
Penilia avirostris population dynamics were studied from
June 2003 to December 2004 at a near shore station
located half a nautical mile off Port Olı
´mpic, Barcelona
(Spain, NW Mediterranean), characterized by shallow
open sea waters. Zooplankton samples were collected
biweekly, when it was possible, by hand pulling a micro-
plankton net (53 mm mesh, 25 cm mouth diameter;
without flowmeter) vertically from the bottom (38 m
deep). The content of the cod end was preserved in
borax-buffered formaldehyde at 4% final concentration.
In addition, water was collected at a depth of 1 m with a
transparent hydrographic bottle, temperature measured
and the water transported in dark plastic jars to the lab-
oratory for Chlorophyll a(Chl a) determination. Chl a
was measured by filtering 75 and 150 mL onto GF/F
Whatman and 5 mm pore-size polycarbonate nucleopore
filters, respectively. The filters were analyzed fluorometri-
cally after 24 h acetone extraction in darkness and cold.
Further details on sampling and description of the zoo-
plankton community can be found in Skovgaard and
Saiz (Skovgaard and Saiz, 2006).
The total abundance of P. a v i r o s t r i s was determined by
stereomicroscope counts of two 5 mL aliquots from each
sample (sample volume: 250 mL), resulting in at least 300
individuals counted per sample. In addition, for each
sample, 50 individuals of P.avirostris were randomly sorted,
sized and staged. Organisms were classified into the fol-
lowing stages: juveniles (,500 mm), non-reproducing
females, parthenogenetic female (with embryos), gameto-
genetic female (with resting eggs) and males. Body length
(BL, from the tip of the head to the base of the caudal
setae; Uye, 1982) was converted to dry weight (DW, mgC)
using the length– weight relationship log (DW) = 2.66
log BL27.369 (Atienza et al., 2006a) and assuming that
carbon content was 50% of DW (Uye, 1982).
For each of the 50 individual sorted groups, all repro-
ducing females (i.e. carrying embryos or resting eggs)
were dissected carefully with thin needles under the
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stereomicroscope, and the embryos or eggs in the brood
pouch were removed, counted, examined and sized (BL
for embryos; major axis for eggs). Resting eggs were
easily identified because they are ovoid, flattened, with
a thick chitinous membrane and are opaque (Fig. 1E),
occupying the entire brood pouch. Parthenogenetic
embryonic development was divided into four different
stages based on the external morphology of the embryo,
following the detailed description by Della Croce and
Bettanin (Della Croce and Bettanin, 1965) and the sim-
plified approach of Wong et al. (Wong et al., 2004). Stage
1 corresponds to the parthenogenetic egg, ellipsoidal
(although the posterior border of the head can be distin-
guished in the advanced phase), surrounded by an
elastic membrane and almost completely filled with yolk
granules (Fig. 1A). In stage 2, the cover membrane dis-
appears, the second antenna starts to develop and the
thorax region is differentiated (Fig. 1B). During stage 3,
the embryo elongates, the second antenna is fully
formed and the first antenna starts to elongate (Fig. 1C).
At this stage, all the thoracic segments are visible, and
sometimes rudiments of thoracic appendages are
evident. Stage 4 embryos are similar to adults, with all
the thoracic appendages completely formed, and the
carapace and the eye fully developed (Fig. 1D).
Recruitment from parthenogenetical eggs was esti-
mated from the population egg ratio (E/N, where Eis
the number of parthenogenetic eggs and embryos
recorded and Nthe total population size), using the
Paloheimo (Paloheimo, 1974) equation for the instan-
taneous per capita birth rate (b,day
21
),
b¼lnððE=NÞþ1Þ=Dð1Þ
where Dis the egg development time (in days). Dwas
estimated from surface temperature in the water column
using the equation of Bottrell (Bottrell, 1975) for fresh-
water cladocerans,
log D¼0:847ðlog TÞ23:609 log Tþ3:796 ð2Þ
where Tis the temperature in degrees Celsius. The use
of Bottrell’s equation for P. avirostris seems to be war-
ranted since Valentin and Marazzo (Valentin and
Marazzo, 2004) compared field estimates of develop-
mental time for P.avirostris at 24 –268C with Bottrell’s
equation predictions, and obtained similar values (2–3
days); other empirical estimations of embryo develop-
mental time in the literature for P.avirostris embryos in
natural conditions also fall in a similar range of values
(ca. 2 days; Mullin and Onbe
´, 1992; Atienza et al.,
2007).
Fig. 1. Developmental stages of P. avirostris defined for this study. (A) stage 1; (B) stage 2; (C) stage 3; (D) stage 4; (E) resting egg. a
1
, first
antenna; a
2
, second antenna; ca, carapace; ey, eye; h, head; m, membrane; ta, thoracic appendices; ts, thoracic segments; yg, yolk granules.
Scale bar denotes 100 mm.
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RESULTS
Figure 2 shows the temporal variation of surface temp-
erature and Chl aconcentration and P. avirostris densities
during the study period. Temperature ranged from ca.
128C in winter up to ca. 288C in summer, and Chl a
concentration showed peaks in winter, spring and early
summer, depicting the typical pattern for the northwes-
tern Mediterranean (Calbet et al., 2001; Ribera
D’Alcala et al., 2004). During most of the year, P.avirostris
was absent from the water column, the first individuals
starting to appear at the beginning of July and reaching
peak values by the end of the month (ca. 2500–
3000 ind m
23
, Fig. 2C). This population of P.avirostris
maintained until the end of August (2003) or
September (2004), when suddenly declining in the
water column to almost complete absence (followed in
2003 for sporadic low peaks, ,500 ind m
23
, until
December).
The temporal variation of P. avirostris population com-
position is shown in Fig. 3. During the phases of
increase and the peaks of high abundance, the popu-
lations were evenly dominated by juveniles, non-
reproducing females and parthenogenetic females (i.e.
with embryos). When the populations were in the
waning phase, males appeared followed by gametoge-
netic females (i.e. with resting eggs). This general
pattern was common for both years, although in 2003
P.avirostris presence in plankton extended under very
low levels until their complete disappearance (Fig. 3).
During this period, juveniles represented a much lower
fraction of the population compared with other periods,
and the relative contribution of non-reproducing
females was higher, indicating that recruitment during
those peaks failed. Regarding females with resting eggs,
they typically carried only one egg, except for two
females carrying two eggs in 2003 (accounting for 12%
of the gametogenetic females).
Table I and Fig. 4 show the BL of P. avirostris adults.
Gametogenetic females were significantly larger than
males and the other two female types. Mean sizes in
2003 were significantly larger (two-tailed t-test, Welch’s
correction, P,0.01), partly as a consequence of the
fact that the late autumn females in 2003 (absent in
2004) inhabited colder waters and were significantly
larger than the summer ones (Fig. 4, Table II).
Brood size ranged from one to eight embryos per
female and was positively correlated to female body size
(2003: r= 0.85, P,0.001; 2004: r= 0.86, P,0.005;
Fig. 5). Most females typically carried two to four
embryos (Fig. 6), and the two-tailed t-test, Welch’s cor-
rection confirms that there is no significant difference in
mean brood size between 2003 and 2004 (P,0.01). In
terms of population dynamics, there was no clear
change in the proportion of parthenogenetic females
with embryos (relative to the total parthenogenic
females) in the waning phases of P. avirostris populations
(Fig. 7A), nor in female brood size through the popu-
lation development (Fig. 7B). Interestingly, during the
decllining phases, and even during the late peaks in
2003, a significant number of parthenogenic females
were carrying embryos (Fig. 7C).
Embryo length increased with developmental stage
(Table III), ranging from 86 to 315 mm. The latter stage
set the smallest body size for the free living P.avirostris in
Fig. 2. Seasonal variation of surface water temperature (A),
chlorophyll aconcentrations (B) and P. avirostris abundance (C) in the
coastal Catalan Sea during the study.
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the water column. No significant differences were found
in embryo length between both years (two-tailed t-test,
Welch’s correction, P,0.05). There was a negative cor-
relation between embryo stage and brood size (2003: r
=20.95, P,0.001; 2004: r=20.90, P,0.001;
Fig. 8).
Finally, the estimated population egg ratios and the
birth rates were very variable with values ranging
between 0.54 and 3.64 embryos ind
21
and between
0.097 and 0.46 day
21
, respectively (Figs 9A and 9B).
This variability reflected mainly the changes in abun-
dance of embryo-carrying females and female brood
size, whereas the embryonic developmental time, which
depended on the changes in surface water temperature
during the seasonal occurence of P. avirostris, varied
between 2.3 and 2.7 days. Birth rates were highest
during the initial blooming period, thereafter showing
diverse peaks not associated with changes in P.avirostris
density (Fig. 9B). Actually, during the declining phases,
the population birth rates were rather high.
Finally, we found that P. avirostris abundance, egg pro-
duction, birth rates and mean brood size were positively
correlated (P,0.05) with temperature; also there was a
negative correlation between temperature and the size
of none-reproducing females and females with embryos.
Chl aconcentration was negatively correlated (P,0.05)
with P. avirostris abundance, size of none-reproducing
females, egg production, birth rates and mean brood
size (Table IV).
DISCUSSION
Penilia avirostris shows a pronounced seasonality in the
Catalan Sea, with a sudden appearance in the water
column in July due to rapid population growth until a
dense population is established and maintained until
the end of August–September, when standing stocks
diminish. Whereas P.avirostris can be continuously
present in the zooplankton community in tropical and
subtropical latitudes (Della Croce and Venugopal,
Fig. 3. Population composition (as %) of P. avirostris during summer 2003 (left panel) and 2004 (right panel). Abundance of P.avirostris from
Fig. 2 is in the upper panels (dashed line) for the sake of the comparison.
Ta b l e I :Penilia avirostris comparative size
(
m
m) of the different adult reproductive stages
between years
Reproductive
stage
2003 2004
Avg SE nn Avg S E nn
Non-reproducing
females
632.3 5.01 353 606.03 5.31 188 *
Females with
embryos
673.4 4.99 298 641.46 4.56 228 *
Males 651.1 8.93 31 629.05 16.71 23
Females with
resting eggs
799.8 16.66 8 721.92 11.41 19 *
Avg, average; SE, standard error; n, sample size.
*Significant at 0.01.
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1973), in temperate ecosystems and specifically in the
Mediterranean, the observed unimodal seasonal pattern
is the typical one (Alcaraz, 1970; Siokou-Frangou, 1996;
Calbet et al., 2001; Ribera D’Alcala
`et al., 2004).
The abrupt appearance and disppearance of the
populations is very characteristic for marine cladocerans
and reflects a typical opportunistic life history. In this
regard, the life cycle of P. avirostris is characterized by
two modes of reproduction, parthenogenesis and game-
togenesis, which follows the general pattern exhibited
by other marine and freshwater cladocerans (Egloff
et al., 1997). Related to both types of reproduction, two
kinds of eggs are also produced by this marine clado-
ceran, a parthenogenetic egg and a thick-walled resting
egg. Parthenogenetic eggs are thin-walled and relatively
small (86 mm), gametogenetic females lay resting eggs,
which are larger (279 mm), fewer in numbers, and
contain yolk (Egloff et al., 1997). In agreement with pre-
vious evidence, gametogenetic females in our study gen-
erally carried only one resting egg, except for the
observation of two individuals carrying two resting eggs
in the brood pouch. The outer membrane of the resting
egg is calcified, which may enhance survival through
the digestive system of potential predators (Onbe
´, 1985),
and facilitates its fast sinking after release, which might
act as an adaptation to prevent predation in the water
column and reduce dispersal by advection (Egloff et al.,
1997). Resting eggs are capable of undergoing diapause,
Fig. 4. Changes in BL of parthenogenetic females (non-reproducing and embryo-carrying) through the seasonal presence of P. avirostris in the
Catalan Sea. Filled circles: summer samples (July–August); open circles: autumn samples (September– October– November). Dotted line is
surface water temperature (from Fig. 2).
Ta b l e I I :Comparative size (
m
m) of P.
avirostris parthenogenetic females (females with
and without embryos) between different periods
in the same year
Reproductive
stage
Summer Autumn
Avg S E nn Avg S E nn
2003 Summer Autumn
Non-reproducing
females
583.4 5.68 142 666.1 6.56 211 *
Females with
embryos
624.7 5.16 161 730.6 6.08 137 *
2004 Summer Autumn
Non-reproducing
females
585.5 5.69 96 627.5 8.57 92 *
Females with
embryos
635.6 6.33 122 648.2 6.55 106
Avg, average; SE, standard error; n, sample size.
*Significant at 0.01.
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carrying the populations through overwintering periods
(Egloff et al., 1997), and their distribution and abun-
dance is a critical factor influencing the overall distri-
bution, seasonal population dynamics, and long-term
variations in the abundance of cladocerans (Viitasalo
and Katajisto, 1994). In some regions, such as the
Inland Sea of Japan, the seasonal fluctuations in the
abundance of resting eggs of this marine cladoceran
have been described in detail (Onbe
´, 1985), but data for
the Mediterranean are more scarce. Moscatello and
Belmonte (Moscatello and Belmonte, 2004) reported
the presence of cladoceran resting eggs in
Mediterranean sediments, and Sioko-Frangou et al.
(Sioko-Frangou et al., 2005) observed that P.avirostris
resting eggs were more abundant (63 –76 eggs m
22
)
in September and October, in agreement with the pre-
sence of gametogenetic females in the water column
found in our study.
The observed brood sizes for parthenogenetic P. avir-
ostris in the Catalan Sea are similar to previous reports
for this species (Della Croce and Venugopal, 1973;
Angelino and Della Croce, 1975; Tang et al., 1993;
Marazzo and Valentin, 2003a, b), although our highest
values did not reach the 13 embryos per female
recorded by Angelino and Della Croce (Angelino and
Della Croce, 1975) in the Agulhas Bank and Knysna
Lake (South Africa). Although brood size of marine cla-
docerans typically appears to be higher during the
initial phases of population growth and decreases
rapidly as population increases (Platt and Yamamura,
1986; Mullin and Onbe
´, 1992; Fofonoff, 1994), we did
not find any clear relation during our study between
either female brood size or population egg ratio and P.
avirostris standing stocks. An interesting result was
the negative correlation between the brood size and the
brood stage of development (Fig. 8), which suggests the
abortion and likely re-abortion of embryos, as described
for podonids by Egloff et al. (Egloff et al., 1997).
Fast recruitment of P. avirostris will depend on the
actual birth rates, which in our study were rather vari-
able and did not seem to be reflected in changes in
population abundance (Fig. 9). However, one must be
cautious with such interpretation, because much of the
variability in P.avirostris abundance may merely reflect
spatial variability (sampling was carried out at a single
fixed station, see below). Evidence that spatial varibility
exists was found in the data obtained by a parallel zoo-
plankton survey study conducted during summer 2003
and 2004 covering the whole Catalan Sea shelf ( four
CACO cruises; Atienza et al., in preparation). During
those cruises, we found a high variability in P.avirostris
abundance between station for the same sampling
period, and, for example, through CACO-1 (July 2003)
abundances ranged between 41 and 2491 ind m
23
between stations. The variability between stations was
the same for the other three cruises and clearly indi-
cated that spatial variability should be considered to
explain the variation in the abundance of P.avirostris.
For this reason, no attempt to estimate population
growth and mortality rates has been made. In this
regard, it is important to note that the observed varia-
bility in birth rates reflects essentially the variability in
the population egg ratio, since during the periods of
high standing stocks embryonic developmental times
were rather similar (2.3– 2.7 days).
Penilia avirostris must likely rely on the hatching of
resting eggs to establish the new population annually
because this marine cladoceran is practically absent
Fig. 5. Scatterplot of BL (mm) and brood size (number embryos
female
21
)ofP. avirostris.
Fig. 6. Frequency distribution of brood size (number embryos
female
21
) in the P. avirostris population in the Catalan Sea. Avg,
average; SE, standard error; n, sample size.
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from the water column in winter and spring. Once
certain threshold values in environmental variables are
reached, parthenogenetic growth can explain the rapid
development of the population. For instance, there is a
4-fold increase in volume between the egg (stage 1) and
the neonate (stage 4), neonates being one-half to
two-thirds to their eventual length as adults (Egloff et al.,
1997). This development allows the newly born P.aviros-
tris to reach adulthood (reproductive period) in about 1
day (Atienza et al., 2007). A simple calculation consider-
ing an average initial brood size of 4, an embryonic
developmental time of 2 days (Mullin and Onbe
´, 1992;
Fig. 7. (A) Proportion of parthenogenetic females carrying embryos in relation to total parthenogenetic females during the seasonal presence of
P. avirostris in the Catalan Sea. Abundance of P.avirostris from Fig. 2 is overlaid (dashed line) for the sake of the comparison. (B) Variation of
brood size (average+1SE). (C) Brood size class distribution (as %).
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Atienza et al., 2007) and a period of 1 day from the
neonate to the reproductive stage, suggests that every
female may produce near 100 young individuals in 8
days. Atienza et al (2007) suggested that it was this short
developmental time to the reproductive stage which
allowed P.avirostris to rapidly appear and bloom in
coastal environments in comparison with copepods,
which have similar embryonic development times but
much slower development to the reproductive adult
stage.
The possible causes for the sudden disappearance of
P. avirostris from the water column are not well under-
stood. The decline in the annual population of clado-
cerans is typically accompanied by the onset of
gamogenetic reproduction and the production of over-
wintering resting eggs. In natural populations, only a
fraction of parthenogenetic females turn into gametoge-
netic females (i.e. Evadne spp.: 8– 25%, Pseudoevadne terges-
tina: 5–10%, Onbe
´and Ikeda, 1995; Pleopis
polyphemoides: 10 –46%, Fofonoff, 1994; 20 –23% P. terges-
tina: Onbe
´, 1978; 50 – 80% Podon leuckarti: Egloff et al.,
1997; and 25–60% Evadne nordmanni: Fofonoff, 1994).
The fraction of gametogenetic P.avirostris females
observed in our study is in the low range of values
found for other marine cladocerans (4 –8% in 2003; 1 –
20% in 2004), as also observed by Marazzo and
Valentin (Marazzo and Valentin, 2003b) for P.avirostris
in Brazilian waters (11– 24%).
This shift from parthenogenetic to gametogenetic
reproduction is an interesting phenomenon. In fresh-
water cladocerans, it is known that the appearance of
males seems to be under hormonal regulation (Minelli
and Fusco, 2006) and that crowding, photoperiod,
temperature and food availability act as stimuli to
induce gamogenesis in parthenogenetic females (Stross
and Hill, 1968; Kleiven et al., 1992; Carvalho and
Hughes, 1983; Stross, 1987; Berg and Pa
´lsson, 2001).
Stross (Stross, 1965) suggested that at least two stimuli
are necessary to induce gametogenetic reproduction.
However, the causes that induce this shift from parthe-
nogenetic to gametogenetic reproduction in marine cla-
docera are not fully understood (Fofonoff, 1994). Recent
attempts to find evidence in freshwater cladocerans of
the presence of the endobacterium Wolbachia, which is
involved in the onset of parthenogenetic reproduction
in many invertebrates (Stouthamer et al., 1999) have
failed (Fitzsimmons and Innes, 2005).
Environmental conditions seem to play a key role in
the decline of populations at the end of the season (e.g.
decrease in temperature, photoperiod, food availability,
turbulence, crowding, predation; Frey, 1982; Fofonoff,
1994; Stross and Hill, 1968). Penilia avirostris populations
in the Mediterranean Sea typically vanish in late
summer–early autumn (Alcaraz, 1970; Lipej et al.,
1997; Calbet et al., 2001; Ribera D’Alcala
`et al., 2004).
The decline in P.avirostris population observed in 2003
(with some limited blooming in October and
November) was premature in comparison with the 2004
data. Although a priori this fact could suggest variability
in the timing of the onset of the factors triggering it,
however, a parallel zooplankton survey conducted during
summer 2003 and 2004 covering the whole Catalan
Sea shelf (CACO cruises; Atienza et al., in preparation)
shows that the observed decline was a local event at our
sampling station, associated with the intrusion of high
saline oceanic waters into the central (and compara-
tively narrower) shelf of the Catalan Sea. Very likely the
late peaks of P.avirostris in autumn 2003 reflect the
receding of these oceanic waters in this area. Similar
late peak events have been observed previously in the
NW Mediterranean (Castello
´n waters, Alcaraz, 1970;
Gulf of Trieste, Lipej et al., 1997), although it is not
known if the causes are similar.
Temperature has been proposed as the main physical
factor that controls P. avirostris populations (Gieskes,
Table III:Size (large axis,
m
m) of the
different embryo stages of P. avirostris
Embryos
stage
2003 2004
Avg SE nn Avg SE nn
Stage 1 86.5 4.61 88 85.5 4.22 68
Stage 2 179.8 3.68 57 179.4 3.31 50
Stage 3 221.4 2.75 103 219.9 3.69 87
Stage 4 315.4 6.88 51 305.0 8.63 23
Resting
eggs
282.3 14.97 8 277.2 2.99 1
Avg, average; SE, standard error; n, sample size. No significant
differences were found.
Fig. 8. Scatterplot of embryo stage and brood size of P. avirostris.
D. ATIENZA ET AL.
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LIFE HISTORY AND POPULATION DYNAMICS OF PENILIA AVIROSTRIS
353

1971; Onbe
´and Ikeda, 1995). In general, populations
of P.avirostris are often associated with warmer waters in
the northern (Lipej et al., 1997; Calbet et al., 2001) and
southern hemisphere (Resgalla and Montu´, 1993), and
we also found a positive correlation between the abun-
dance of this marine cladoceran and temperature.
However, this optimum range of warm temperatures
where P.avirostris can reproduce and grow successfully
appears to vary geographically. Some authors have
pointed out that the distribution of P.avirostris is mostly
restricted to waters above 188C but can range between
128C and 308C (Kim et al., 1994; Kim and Onbe
´,
1995), and it is known that this species has an optimum
temperature around 258C (China: Tang et al., 1995;
Japan: Onbe
´et al., 1996). Recently, Johns et al. (Johns
et al., 2005) showed that this species is increasing in
prevalence in the North Sea, where the sea surface
temperature has been increasing over the last decade
(more than 38C, and reaching temperatures higher than
198C).
Food availability has also been suggested to affect the
seasonal dynamics of P. avirostris. Lipej et al. (Lipej et al.,
1997) and Calbet et al. (Calbet et al., 2001) indicated
that during warm periods (summer), the water column
was stratified and the concentrations of nutrients and
chlorophyll above the pycnocline are rather low,
whereas pico- and nanoplanktonic autotrophs are abun-
dant. Penilia avirostris is a filter feeder that ingests nano-
flagellates preferentially (Atienza et al., 2006a), and the
higher abundance of these organisms results in a higher
availability of food that is rapidly exploited. It is also
important to notice that P.avirostris occurs mainly in
coastal and shelf waters, where chain-forming diatoms
Fig. 9. (A) Population egg ratio (average number of eggs/embryos ind
21
) and (B) estimated birth rates (day
21
)ofP.avirostris in the Catalan Sea.
Dotted line, abundance of P.avirostris.
Ta b l e I V:Spearman’s correlations between
different P. avirostris population parameters
and some environmental variables
TT Chl aa tot Chl aa >5mm
Abundance 0.78* 20.43* 20.46*
Size of non-reproducing females 20.79* 20.17 20.56*
Size of females with embryos 20.85* 20.15 20.43
Egg production 0.77* 20.44* 20.47*
Birth rates 0.72* 20.51* 20.51*
Mean brood size 0.44* 20.43* 20.47*
T, sea temperature; Chl atot, total chlorophyll aconcentration; Chl a.
5mm, chlorophyll a.5mm concentration.
*Significant at P,0.05.
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are typically an important component of autotrophic
biomass during the non-stratified periods. Penilia avirostris
is a typical filter feeder (Paffenho
¨fer and Orcutt, 1986),
and even though it shows some degree of prey selection
(Atienza et al., 2006a), it most likely experiences detri-
mental effects and clogging when exposed to long
chains of diatoms. It may well be that the preference for
warmer waters exhibited by P.avirostris is not only
related to temperature per se but also to the degree of
stratification of the water column as pointed out by
Alcaraz (Alcaraz, 1970); higher stratification in summer
would be accompanied by a relatively lower abundance
of long chain-forming diatoms and relatively higher
abundance of nanoflagellates. This hypothesis agrees
with the fact that in the Western Mediterranean the
decline of P.avirostris populations is typically associated
with a seasonal regime of thunderstorms and heavy
rainfall in late summer –early autumn (Duarte et al.,
1999) with associated wind stress and increased run-off
that must affect water column stability.
Finally, an additional cause for the disappearance of
P. avirostris populations in late summer –early autumn
could be predation pressure, which has shown to be
very important in freshwater systems affecting cladocer-
ans morphology, size, composition and abundance
(Grant and Bayly, 1981; Thys and Hoffmann, 2005).
The importance of predation in shaping marine zoo-
plankton communities has been traditionally neglected
(Verity and Smetacek, 1996). There is evidence that pre-
dators such as ctenophores, chaetognaths and fish
larvae have the potential to decimate marine cladoceran
populations (Canino and Grant, 1985; Duro
´and Saiz,
2000; Nip et al., 2003; Barz and Hirche, 2005).
However, in the NW Mediterranean, no studies have
addressed the effects of predation on the population
dynamics of P.avirostris.
ACKNOWLEDGEMENTS
The authors also wish to thank the help of Pepito and
Ramon for boat facilities and assistance at sea.
FUNDING
This work was supported by the Spanish projects
REN2001-1693 and CTM2004-02 575/MAR. D.A.
benefitted from fellowships from the Spanish Ministerio
de Educacio
´n y Ciencia, and from the Grup d’Ecologia del
Zoopla
`ncton Marı
´funded by the Generalitat de
Catalunya.
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