MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
https://doi.org/10.47193/mafis.3422021010610
ABSTRACT. A significant sea surface temperature increase has been reported for the Southwest-
ern Atlantic Ocean between 20° S-50° S over the last decades. Zooplankton organisms are highly
sensitive to temperature rise. They play a very important role in marine ecosystems by providing the
main pathway of energy transfer from primary producers to consumers. Seasonal and interannual
(2000-2017) variability of metazooplankton in relation to environmental changes, particularly tem-
perature, were analyzed at the EPEA station (38° 28′ S-57° 41′ W). Copepods, appendicularians,
cladocerans, chaetognaths, and lamellibranch larvae were identified and quantified. Temperature
exhibited a positive interannual trend during the series, whereas the Simpson parameter showed a
decreasing tendency and salinity remained almost constant. Adults, copepodites, and nauplii of
small copepods belonging to Oithonidae (mostly Oithona nana) and Paracalanidae-Clausocalanidae
families dominated the metazooplankton community during the study period. Three groups of taxa
with different seasonal patterns of variability were clearly identified. Members of Oithonidae exhib-
ited positive interannual trends, whereas lamellibranch larvae and Calanidae showed negative inter-
annual trends. A direct influence of temperature anomaly on these changes is suggested as well as
possible indirect effects of this anomaly upon zooplankton through different phytoplankton frac-
tions. Under the current scenario of climate change, the maintenance of this time-series becomes
crucial in order to evaluate the eventual transfer of the environmental variability to the local food
webs through planktonic organisms.
Key words: Microzooplankton, mesozooplankton, time-series, EPEA station, Buenos Aires shelf,
Southwestern Atlantic.
Relación entre los cambios a largo plazo de la comunidad de zooplancton y la variabilidad
ambiental en la estación EPEA (Océano Atlántico Sudoccidental)
RESUMEN. En las últimas décadas se ha registrado un aumento significativo de la temperatura
superficial del mar en el Océano Atlántico Sudoccidental, entre 20° S-50° S. Los organismos del zoo-
plancton son muy sensibles al aumento de la temperatura. Ellos cumplen un rol muy importante en
los ecosistemas marinos dado que constituyen la principal vía de transferencia de energía desde los
productores primarios a los consumidores. En este trabajo se analizó la variabilidad estacional e inter-
anual (2000-2017) del metazooplancton en la estación EPEA (38° 28′ S-57° 41′ W), en relación con
los cambios ambientales, en particular de la temperatura. Copépodos, apendicularias, cladóceros,
quetognatos y larvas de lamelibranquios fueron identificados y cuantificados. La temperatura exhibió
una tendencia interanual positiva de las anomalías durante la serie mientras que el parámetro de
211
*Correspondence:
mdvinas@gmail.com
Received: 30 April 2021
Accepted: 16 June 2021
ISSN 2683-7595 (print)
ISSN 2683-7951 (online)
https://ojs.inidep.edu.ar
Journal of the Instituto Nacional de
Investigación y Desarrollo Pesquero
(INIDEP)
This work is licensed under a Creative
Commons Attribution-
NonCommercial-ShareAlike 4.0
International License
Marine and
Fishery Sciences
MAFIS
MARINE IMPACTS IN THE ANTHROPOCENE
Linking long-term changes of zooplankton community to environmental
variability at the EPEA station (Southwestern Atlantic Ocean)
MARÍA DELIA VIÑAS
1, 2, *
, GEORGINA D. CEPEDA
1, 2
and MOIRA LUZ CLARA
1, 2, 3
1
Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo Nº 1, Escollera Norte, B7602HSA - Mar del
Plata, Argentina.
2
Instituto de Investigaciones Marinas y Costeras (IIMyC-CONICET), Facultad de Ciencias Exactas y Naturales, Universidad
Nacional de Mar del Plata (UNMdP), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina.
3
Instituto Franco-
Argentino para el Estudio del Clima y sus Impactos (CNRS-IRD-CONICET-UBA; IRL 3351 IFAECI). Buenos Aires, Argentina.
ORCID María Delia Viñas https://orcid.org/0000-0003-2824-4405, Georgina D. Cepeda https://orcid.org/0000-0002-8234-6763,
Moira Luz Clara https://orcid.org/0000-0002-7539-5292
INTRODUCTION
Since the beginning of the twentieth century,
our planet has been experiencing a gradual
increase of the mean global temperature, with an
intensification of the warming rate over the last
decades (IPCC 2019).
An analysis of time series of satellite sea sur-
face temperatures (SST) carried out in the South
Atlantic Ocean during the last 30 years prior to
2012 indicated a SST increase in almost 86% on
this region (Muller-Karger et al. 2017). However,
whereas in the north Argentine continental shelf,
areas of significant increase of surface tempera-
ture were observed between 20° S-50° S, others
with a cooling trend were registered in latitudes
of 49° S-52° S in the south Patagonian shelf (Ri-
saro 2020).
Water temperature and salinity are excellent
indicators of the physical environment in which
plankton are living, affecting them both directly
(i.e., through physiology and growth rates) and
indirectly (i.e., through water column stratifica-
tion and related nutrient availability) (O’Brien et
al. 2013).
Marine zooplankton communities are highly
diverse and thus perform a variety of ecosystem
functions (Richardson 2008 and references with-
in). The most important role of these organisms is
to act as major grazers in food-webs by providing
the principal pathway for energy from primary
producers to consumers at higher trophic levels.
Zooplankton can be, moreover, recognized as
beacon of climate change for several reasons
(Richardson 2008). Because of their physiology
and short live cycles, zooplanktonic species are
highly sensitive to temperature rise (Mauchline
1998; Edwards and Richardson 2004; Beaugrand
and Kirby 2018). Therefore, present climate
changes may strongly affect their population
dynamics and phenology (Hays et al. 2005; Rice
and Stewart 2016). As these organisms are gener-
ally not commercially exploited, their long-term
trends of variability are mostly due to environ-
mental changes (Richardson 2008).
Sustained ocean time-series, particularly ship-
based repeated measurements, represent one of
the most valuable tools to characterize and quan-
tify ocean ecosystem cycles and fluxes, from the
plankton up to higher trophic levels, and their
association to changing climate (Edwards et al.
2010; Valdés and Lomas 2017). Time-series
observations over multiple decades are necessary
to differentiate between natural and anthro-
pogenic variability (O’Brien et al. 2017 and refer-
ences within).
In the northern coastal waters of Argentina
(38° 28′ S-57° 41′ W) (Figure 1), a biogeochemi-
cal time-series was established at the EPEA sta-
tion (Estación Permanente de Estudios Ambien-
tales/Permanent Station of Environmental Stud-
ies), as part of the DIPLAMCC (Dinámica del
Plancton Marino y Cambio Climático/Dynamics
of Marine Plankton and Climate Change) Project
of INIDEP (Instituto Nacional de Investigación y
Desarrollo Pesquero). Several chemical, physical,
212
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Simpson mostró una tendencia decreciente y la salinidad prácticamente se mantuvo invariable. Adultos, copepoditos, y nauplii de los
copépodos pequeños pertenecientes a las familias Oithonidae (en su mayoría Oithona nana) y Paracalanidae-Clausocalanidae dominaron
la comunidad del metazooplancton durante el período de estudio. Se identificaron claramente tres grupos de taxa con diferentes patrones
estacionales de variabilidad. Miembros de la Familia Oithonidae exhibieron tendencias interanuales positivas mientras que las larvas de
lamelibranquios y la Familia Calanidae mostraron tendencias interanuales decrecientes. Se sugiere un efecto directo de las anomalías de
la temperatura sobre estas variaciones así como posibles efectos indirectos de este parámetro sobre el zooplancton, a través de su influencia
sobre diferentes fracciones del fitoplancton. En el actual escenario de cambio climático, el mantenimiento de esta serie temporal es de gran
importancia para evaluar la transferencia eventual de la variabilidad ambiental a la trama trófica local a través del plancton.
Palabras clave: Microzooplancton, mesozooplancton, serie temporal, estación EPEA, plataforma bonaerense, Atlántico Sudoccidental.
photo-biological, and planktonic variables are
monitored there on a monthly basis since 2000. In
this coastal station, phytoplankton community
reaches its maximum biomass in winter, mainly
represented by 20-200 µm diatoms of the micro-
phytoplankton fraction (Negri and Silva 2011).
Ultraphytoplankton fraction < 5 μm makes its
major contribution to total biomass in summer,
thus configuring an oligotrophic-like ecosystem
(Silva et al. 2009; Negri and Silva 2011; Viñas et
al. 2013). The first approach to analyze phyto-
plankton dynamics at the EPEA station in an
interannual scale (2000-2009) indicated an
increasing trend in chlorophyll concentrations
during the last years of the study period, mainly
due to the contribution of the smallest phyto-
plankton size fraction, i.e. the picophytoeukariot-
ic organisms (Silva 2011). The proliferation of
these organisms due to climatic variations has
been reported on a large scale (Li and Harrison
2008; Moran et al. 2010) highlighting the increas-
ing importance of small phytoplankton in a future
global warming scenario (Sarmiento et al. 2004;
Behrenfeld et al. 2006).
Considering the zooplankton community, Dio-
visalvi (2006), Temperoni et al. (2011), Cepeda
(2013) and Viñas et al. (2013) analyzed the annu-
al cycle of abundance, size structure, and biomass
of its main components at the EPEA station,
whereas Daponte et al. (2004) and Capitanio et al.
(2008) focused particularly on chaetognaths and
appendicularians, respectively. Small-sized cope-
pods (< 1 mm total length) dominated by Oithona
nana and members of Paracalanidae constitute
the bulk of the metazooplankton (81%) through-
out the year in the EPEA station with maximum
values in summer in terms of abundance and bio-
mass (Viñas et al. 2013). It is known that the
reproductive cycle of small copepods in temper-
ate seas (Pittois et al. 2009) is positively con-
trolled by temperature (Viñas 1990; Uye and Shi-
buno 1992; Temperoni et al. 2011).
The present work shows an analysis of the
interannual patterns of variability of main compo-
nents of metazooplankton and their relationship
with physical cues carried out for the first time at
the EPEA station between March 2000 and
November 2017 (18 years). The concurrent analy-
213
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Figure 1. Location of the EPEA station (38° 28′ S -57° 41′ W).
40°
38°
36° S
60° W 58° 56°
N
EPEA
station
50 m 100 m 2000 m
Southwestern Atlantic
Mar del Plata
sis of seasonal patterns of zooplankton abundance
in relationship to the environmental factors will
contribute to the interpretation of changes
observed in the long-term scale. We hypothesized
that during the studied period, under a scenario of
Climate Change with increasing of both sea sur-
face temperature and smallest phytoplankton size
fraction concentration, a rise in the abundance of
small copepod species is to be expected.
MATERIALS AND METHODS
Hydrography
During each cruise to the EPEA station, con-
ductivity and temperature profiles were obtained
with a Seabird CTD (SBE19) 01 CTD. Data were
processed, quality checked, and stored in the
Regional Oceanographic Database (BaRDO) at
the Physical Oceanography Laboratory of
INIDEP.
Zooplankton sampling and laboratory analy-
sis
A total of 93 zooplankton samples were
obtained with a small Bongo net (67 and 220 µm
meshes) equipped with flowmeters in each mouth
for calculation of the filtered water volume. The
net was obliquely trawled through the water col-
umn from 5 m of the bottom (48 m depth) to the
surface. Tows were short (towing time: 2 min;
towing rate: 20 m min
-1
) with the ship moving at
2 knots speed. After obtained, samples were
immediately preserved in 4% formaldehyde solu-
tion. For the present study, only samples from the
finest mesh net were analyzed considering the
strong dominance of microzooplankton and
mesozooplankton smaller than 1 mm total length
previously reported at this station (Viñas et al.
2013) and the adequacy of this mesh size to retain
them (Di Mauro et al. 2009).
Zooplankton components were identified
under stereoscopic microscopy and grouped into
the following categories:
- Oithonidae (OIT): includes adult and cope-
podite stages of O. nana and O. aff. hel-
golandica.
- Oithonidae (OITN): includes nauplii of O.
nana and O. aff. helgolandica.
- Paracalanidae-Clausocalanidae (PACL): in-
cludes adult and copepodite stages of Para-
calanus parvus, Parvocalanus scotti and
Ctenocalanus spp.
- Paracalanidae-Clausocalanidae (PACLN): in-
cludes nauplii of Paracalanus parvus, Parvo-
calanus scotti and Ctenocalanus spp.
- Calanidae (CAL): includes only adult and
copepodite stages of Calanoides carinatus.
- Evdne nordmanni (ENO).
- Penilia avirostris (PAV).
- Appendicularians (APP).
- Chaetognaths (CHA).
- Lamellibranchs larvae (LLA).
The number of individuals per cubic meter
(ind. m-3) for each category was estimated from
the counts of individuals in different aliquots of
the original sample and the filtered volume by the
net. The aliquot size of each taxon was estab-
lished according to its original concentration in
the sample.
Data analysis
Considering that the zooplankton sampling was
performed obliquely through a portion of the water
column, mean temperature (MT) and mean salinity
(MS) were measured taking into account the max-
imum depth attained by the net. To determine the
location of the transition between stratified waters
and mixed waters, the stability Simpson parameter
(ϕ) was estimated (Simpson 1981). This is a meas-
ure of the mechanical work required to vertically
mix the water column. Small values of ϕ indicate
214
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
poorly stratified waters while high values are asso-
ciated with stratified ones. In this work, the value
of 40 J m
-3
was used as the limit between homoge-
neous (ϕ < 40) and stratified (ϕ>40) waters, as
established by Sabatini and Martos (2002).
Analyses of both seasonal and interannual
variability were performed on the zooplankton
data and then related with changes in physical
data (MT, MS, and ϕ).
As with other time-series worldwide, sampling
at the EPEA station exhibited irregularity in time-
frequency. This fact was recurrent in the time-
series and calculation of an annual average of
zooplankton abundance can be greatly influenced
by time of sampling. This problem is further com-
pounded by missing months within sampling
years. Mackas et al. (2001) proposed a solution to
this difficulty in which the annual anomaly is cal-
culated as an average of individual monthly
anomalies. This method, adopted by the Working
Group on Zooplankton Ecology (WGZE) of
ICES, reduces many of the issues of low frequen-
cy and/or irregular sampling and also removes
seasonal signal from the year-to-year analysis
(O’Brien et al. 2008). In order to estimate interan-
nual and seasonal anomalies of physical and bio-
logical variables in the EPEA time-series, the
method of Mackas et al. (2001) was used.
For seasonal analysis, the year was divided
into four periods of three months each, starting in
January for summer. Kruskal-Wallis non-para-
metric test was employed to compare abundances
by seasons in view of the non-normality of the
data. Before data analysis, the outliers of each
taxonomic category were estimated considering
the mean ± 1.96 SD of its abundance and elimi-
nating all minor or major values from the data-
base. This procedure was applied for each season
considered separately. After that, log (x + 1)
transformation was applied to the remaining data.
A Principal Component Analysis (PCA) was
employed to identify patterns in the data set corre-
sponding to the original variables (zooplankton
categories). Correlations among the biological
variables and between these and the physical ones
were used to interpret the grouping patterns pro-
duced by PCA. Analyses were performed employ-
ing Statistica v7 software (StatSoft Inc. 2007).
RESULTS
Hydrography
Temperature varied seasonally, with minima in
winter (10.93 ± 0.85 °C, July-September), and
maxima in summer (19.20 ± 0.88 °C, January-
March) (Table 1). Salinity did not exhibit a clear
seasonal variation and values fluctuated between
33.74 ± 0.14 in spring (October-December) and
33.94 ± 0.15 in autumn (April-June). Vertical
stratification, quantified by ϕ, was more accentu-
ated in summer (50.42 ± 44.23) and spring (23.50
± 23.52) than in autumn (4.26 ± 11.72) and winter
(2.63 ± 2.61). Mixing of water column, typical of
the winter months, was reflected in the lowest
value of ϕ recorded during this season.
215
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Table 1. Mean seasonal values ± SD of MT, MS and ϕ at the EPEA station during the period 2000-2017.
Season MT MS ϕ
Summer (J-F-M) 19.20 ± 0.88 33.76 ± 0.24 50.42 ± 44.23
Autumn (A-M-J) 15.71 ± 2.12 33.94 ± 0.15 4.26 ± 11.72
Winter (J-A-S) 10.93 ± 0.85 33.89 ± 0.13 2.63 ± 2.61
Spring (O-N-D) 13.71 ± 2.26 33.74 ± 0.14 23.50 ± 23.52
Interannual anomalies were analyzed in physi-
cal parameters during the study period. Whereas
temperature displayed an increasing trend, Simp-
son parameter showed a decreasing tendency, and
salinity did not show any important variation
(Figure 2).
Zooplankton
Composition and seasonal abundance
Microzooplankton was dominated by nauplii
of copepods and lamellibranch larvae (Table 2).
Within the mesozooplankton, adults and cope-
podites of small copepods (< 1 mm), represented
mostly by Oithonidae and members of Para-
calanidae-Clausocalanidae, dominated through-
out the year, alternating their preeminence among
seasons (Table 2; Figure 3). Thus, the dominance
of Oithonidae was higher in spring and winter. On
the contrary, Paracalanidae-Clausocalanidae pre-
dominated upon Oithonidae in summer and
autumn. Appendicularians were also abundant all
year round followed by cladocerans. Calanidae
and chaetognaths were the less abundant taxa.
Adult and copepodite stages of Oithonidae
attained their highest abundance in spring with a
mean of 11,293 ind. m
-3
, followed by a mean of
7,159 ind. m
-3
in summer (Table 2). Minimum
216
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Figure 2. Annual anomalies of mean temperature (A), mean salinity (B) and ϕ (C) at the EPEA station during the period 2000-
2017. Dashed line: ns. trend.
-15
-5
0
5
10
15
-0.08
0.00
0.08
0.16
0.24
-0.8
-0.4
0.0
0.4
0.8
A
-0.16
-10
Annual anomalies
2000 2002 2004 2006 2008 2010 2012 2014 2016
1.2
Annual anomalies
Annual anomalies
B
C
Year
217
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Table 2. Seasonal abundance of main components of micro and mesozooplankton (mean ± SD) at the EPEA station during the period 2000-2017. A: adults,
C: copepodites. Within parentheses: number of seasonal observations.
Summer Autumn Winter Spring
Microzooplankton
Nauplii of Oithonidae 3,546.09 ± 4,108.83 (18) 958.54 ± 921.65 (15) 6,498.75 ± 5,913.18 (16) 15,932.14 ± 13,939.34
(16)
(OITN)
Nauplii of Paracalanidae- 6,315.29 ± 5,967.95 (20) 2,640.30 ± 1,849.01 (15) 2,563.48 ± 1,921.88 (19) 2,895.74 ± 1,984.82 (18)
Clausocalanidae (PACLN)
Micro-mesozooplankton
Lamellibranch larvae 1,021.46 ± 1,096.61 (21) 261.26 ± 289.13 (18) 1,175.85 ± 1601.68 (21) 604.25 ± 734.60 (20)
(LLA)
Mesozooplankton
Oithonidae (A + C) (OIT) 7,159.12 ± 10,289.04 (21) 1,218.72 ± 967.50 (18) 5,039.15 ± 4,494.19 (21) 11,792.59 ± 9,200.15 (21)
Paracalanidae- 7,295.85 ± 5,730.31 (21) 2,540.22 ± 1,225.83 (17) 1,867.29 ± 1,311.71 (15) 2,956.31 ± 2,771.98 (21)
Clausocalanidae (A + C)
(PACL)
Calanidae (A+C) (CAL) 26.46 ± 81.86 (22) 36.57 ± 90.51 (19) 115.34 ± 123.02 (22) 69.84 ± 177.27 (22)
Evadne nordmanni (ENO) 108.32 ± 143.15 (21) 1.41 ± 5.98 (18) 10.90 ± 27.85 (21) 281.46 ± 430.75 (21)
Penilia avirostris (PAV) 735.33 ± 988.47 (20) 66.74 ± 125.93 (18) 0 ± 0 (21) 0 ± 0 (20)
Appendicularians (APP) 2,515.97 ± 2,279.54 (21) 526.89 ± 622.60 (18) 1,740.70 ± 1,846.93 (21) 2,485.34 ± 2,608.36 (21)
occurred in autumn (1,219 ind. m
-3
) which dif-
fered significantly from others seasons (Kruskal
Wallis test, H
(3, N = 81)
= 26.08; p = 0.000). Similar-
ly, nauplii of Oithonidae exhibited a clear increase
of abundances from winter onwards with the high-
est densities occurring in spring (15,932 ind. m
-3
),
a gradual decrease in summer (3,546 ind. m
-3
) and
minimum (958 ind. m
-3
) in autumn (Table 2).
Highly significant differences (H
(3, N = 65)
= 29.69;
p = .0000) among seasonal abundances were
recorded for these nauplii. Autumn was signifi-
cantly different from winter and spring, while the
latter differed from summer (p < 0.01).
The highest abundance (7,296 ind. m
-3
) of
adults and copepodites of Paracalanidae-Clauso-
calanidae was registered in summer (7,296 ind. m
-3
)
and the lowest in winter (1,867 ind. m
-3
), exhibit-
ing significant differences among seasons
(H
(3, N = 80)
= 18.68; p = .0003). Summer signifi-
cantly differed from winter and spring (p < 0.05)
(Table 2, Figure 5 A). Although nauplii of Para-
calanidae-Clausocalanidae showed also the high-
est values in summer (6,315 ind. m
-3
), non-signifi-
cant differences were observed among seasons
(H
(3, N = 72)
= 4.230; p = 0.24).
Among the Calanidae (> 2 mm), Calanoides
carinatus was the only identified species. It was
very scarce all around the year exhibiting the
highest abundance in winter (115 ind. m
-3
) and
the lowest one in summer (82 ind. m
-3
) (Table 2).
Significant dissimilarities among seasons were
documented for this species (H
(3, N = 85)
= 20.23;
p = .0002), with winter differing from summer
and spring (p < 0.05).
The abundance of lamellibranch larvae showed
the highest seasonal value in winter (1,176 ind. m
-3
),
another minor peak in summer (1,021 ind. m
-3
),
and the lowest value in autumn (261 ind. m
-3
)
(Table 2). This group showed significant seasonal
differences (H
(3, N = 80)
= 8.95; p = .0299) in gen-
eral, but no significant differences were detected
between pairs of seasons.
Among cladocerans, E. nordmanni presented
the peak of abundance in spring with 281 ind. m
-3
and the minimum in autumn (1.4 ind. m
-3
) with
significant seasonal differences (H
(3, N = 81)
= 27.89;
p = 0.0000). Autumn was dissimilar from summer
(p < 0.05) and spring (p < 0.001) and the latter dif-
fered from winter (p < 0.005) (Table 2; Figure 7
A). P. avirostris was absent in winter and spring
and was more abundant in summer (735 ind. m
-3
)
(Table 2). Significant differences among seasons
were detected (H
(3, N = 79)
= 47.77; p = .0000), with
summer differing from autumn (p < 0.05).
Appendicularians presented higher abundances
in summer and spring (2,516 and 2,485 ind. m
-3
,
218
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Figure 3. Mean seasonal percentages of contribution of OIT, PACL and CAL to copepods abundance at the EPEA station during
the period 2000-2017.
0
20
40
60
80
100
Summer Autumn Winter Spring
OIT PACL CAL
Percentage
respectively) and the lowest value in autumn
(527 ind. m
-3
) (Table 2). Significant differences
were recorded among seasons (H
(3, N = 81)
= 14.02;
p = .0029), with autumn differing from summer
and spring (p < 0.05).
Chaetognaths exhibited their highest abun-
dance in summer (75 ind. m
-3
) and the lowest
one in spring (19 ind. m
-3
) (Table 2). Significant
differences among seasons were observed
(H
(3, N = 80)
= 10.79; p = 0.0129) but only winter
and spring distinguished significantly (p < 0.05)
between them.
Grouping of taxa and their correlation with phys-
ical variables
Factors 1, 2, and 3 of the PCA explained
56.67% of the variance (Figure 4). In the space
configured by factors 1 and 2, a group of six taxa
(OIT, PACL, OITN, PACLN, ENO, and APP)
evidenced negative correlations with factor 1
(Table 3; Figure 4) and clearly separated from
CAL and PAV. These six taxa occurred all year
round with higher abundances during spring and
summer. In several cases, significant positive cor-
relations among them and physical variables,
especially MT and ϕ, were observed (Table 4).
On the contrary, CAL was strongly associated
with negative values of factor 2 (Table 3; Figure
4). CAL occurred throughout the year with the
highest abundance in winter, showing a negative
correlation with PAV and a positive one with
CHA. As regards physical variables, CAL was
negatively correlated with MT and φ (Table 4).
PAV was strongly and positively related to fac-
tor 2 (Table 3). This species was partially present
throughout the year, with maximum abundance in
summer and showing a positive correlation with
PACL and a negative one with OITN and CAL
(Table 4).
CHA was positively associated to factor 3
(Figure 4). This taxon presented the lowest abun-
dances in spring, a negative correlation with both
OIT and φ (p < 0.05), and a strong positive corre-
lation with CAL (p < 0.001) (Table 4).
219
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Figure 4. Principal Component Analysis (PCA) results. Projection of variables on the factor planes 1 x 2 (on the left) and 1 x 3
(on the right). Oithonidae (OIT), Paracalanidae-Clausocalanidae (PACL), Evdne nordmanni (ENO), Penilia avirostris
(PAV), nauplii of Oithonidae (OITN), nauplii of Paracalanidae-Clausocalanidae (PACLN), Appendicularians (APP),
Calanidae (CAL), Chaetognaths (CHA), Lamellibranch larvae (LLA). Blue dashed ellipses indicate grouping of taxa
(see text).
1.0
0.5
0.0
-0.5
-1.0
Factor 1 : 25.05%
Factor 2 : 16.58%
-1.0 -0.5 0.0 1.00.5
OITN
PACL
PACLN
ENO
APP
CHA
CAL
LLA
CHA
PACLN
OITN
OIT
APP
ENO
PACL
PAV
1.0
0.5
0.0
-0.5
-1.0
Factor 1 : 25.05%
Factor 3 : 15.05%
-1.0 -0.5 0.0 1.00.5
CAL
OIT
LLA
PAV
Long-term interannual variability
Among all the zooplankton categories ana-
lyzed, OIT and OITN showed increasing patterns
of variation, but trends were not statistically sig-
nificant (Figure 5 A and 5 B). By contrast, CAL,
LLA and CHA exhibited decreasing anomalies
(Figures 6 A, 6 B and 9 B).
Other taxa such as PACL, PACLN, ENO, PAV
and APP displayed neutral trends (Figures 7 A, 7
B, 8 A, 8 B and 9 A). No significant relationships
among anomalies of biological and physical vari-
ables were observed.
Long-term seasonal variability
Non-significant annual trends were observed
in the analyzed taxa of this time series. However,
at a seasonal scale, some significant tendencies
were registered. CAL and LLA exhibited
decreasing trends in winter (p = 0.05 and
p = 0.03, respectively). Also, a negative tendency
was observed for chaetognaths in summer
(p = 0.03) and a positive one for appendiculari-
ans in spring (p = 0.02). These anomalies had no
significant correlation with those of the physical
parameters.
DISCUSSION
Hydrography
In terms of the seasonal cycle, temperature at
the EPEA station behaves like a region influenced
by the deep water of Península Valdés (Luz Clara
et al. 2019). Minimum temperatures occurred in
July-September (with a peak in August) and max-
imum values corresponded to January-March
(peaking in February), in response to the annual
radiative cycle effect, as observed in other studies
in the South Atlantic Ocean (e.g. Podestá et al.
1991; Lentini et al. 2000; Martínez-Avellaneda
2005; Luz Clara et al. 2019).
Zooplankton
Composition and seasonal abundance
PCA analysis grouped zooplankton taxa with
similar environmental affinity. The resulting pat-
tern was comparable in composition with that
found by Viñas et al. (2013) in their annual 2000-
2001 study of zooplankton at the EPEA station.
One group, including species with more affinity
220
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Table 3. Principal Component Analysis (PCA) results. Factor coordinates of the variables. Variables that contributed the most to
each factor are indicated in bold.
Variable Factor 1 Factor 2 Factor 3
OIT -0.78 -0.05 -0.30
OITN -0.70 -0.35 -0.38
PACL -0.50 0.49 0.35
PACLN -0.51 -0.15 0.40
ENO -0.61 0.16 0.03
APP -0.71 0.12 0.23
PAV 0.05 0.80 0.21
CHA 0.13 -0.22 0.78
CAL -0.08 -0.71 0.47
LLA -0.04 0.19 0.25
for warm-temperate waters of spring and summer
such as the small copepods Oithonidae and Para-
calanidae-Clausocalanidae, the cladoceran E.
nordmanni and appendicularians, separated from
the large herbivore C. carinatus (Calanidae),
which showed more affinity to colder winter
waters (Cepeda et al. 2018 and references therein)
and from the cladoceran P. avirostris, with more
affinity for warmer waters of summer (Viñas et
al. 2007). Chaetognaths presented their highest
values in summer followed by lower and similar
values in autumn and winter. A comparable pat-
tern of seasonal abundance was found by
Daponte et al. (2004) in their study of an annual
cycle of Sagitta friderici, the main chaetognath
species of the EPEA station.
Copepod species smaller than 1 mm total
length numerically dominated the zooplankton
community throughout the year during the study
period. At the EPEA station, this fraction exceeds
other copepods not only in terms of abundance
but also in biomass (Viñas et al. 2013). Small
copepods are very abundant in temperate and
tropical coastal regions (Mazzocchi and Ribera
d’Alcalá 1995; Hopcroft et al. 2001; Satapoomin
et al. 2004; Turner 2004; Atienza et al. 2006; Zer-
221
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Table 4. Significant linear correlations among biological variables (log x + 1) and between these ones and physical variables.
Biological variable 1 Biological variable 2 r p N
OIT OITN 0.665 0.000 80
OIT PACL 0.362 0.001 80
OIT PACLN 0.232 0.038 80
OIT APP 0.321 0.004 80
OIT ENO 0.222 0.048 80
OIT CHA -0.265 0.017 80
PACL PACLN 0.297 0.007 80
PACL APP 0.346 0.002 80
PACL PAV 0.348 0.002 80
CAL PAV -0.328 0.003 80
CAL CHA 0.382 0.000 80
APP ENO 0.518 0.000 80
APP OITN 0.310 0.005 80
APP PACLN 0.251 0.025 80
ENO OITN 0.284 0.011 80
PAV OITN -0.221 0.048 80
Biological variable Physical variable r p N
PACL MT 0.317 0.002 93
CAL MT -0.270 0.009 93
OIT ϕ 0.238 0.021 93
PACL ϕ 0.213 0.040 93
CAL ϕ -0.294 0.004 93
CHA ϕ -0.222 0.033 93
222
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Figure 5. Interannual variation of abundance and annual anomalies of OIT (A) and OITN (B) during the period 2000-2017 at
the EPEA station. Red squares: outliers. Dashed line: ns. trend.
0
20
40
60
80
100
-0.6
-0.3
0.0
0.3
0.6
-0.6
-0.3
0.0
0.3
0.6
0.9
0
20
40
60
80
100
2000 2002 2004 2006 2008 2010 2012 2014 2016
Year
Annual anomalies
Abundance
(1 000 ind. m ),
-3
Annual anomalies
Abundance
(1 000 ind. m ),
-3
A
B
223
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Figure 6. Interannual variation of abundance and annual anomalies of CAL (A) and LLA (B) during the period 2000-2017 at the
EPEA station. Red squares: outliers. Dashed line: ns. trend.
2000 2002 2004 2006 2008 2010 2012 2014 2016
Year
-1.0
0.0
1.0
Annual anomalies
Abundance
(1 000 ind. m ),
-3
Annual anomalies
Abundance
(1 000 ind. m ),
-3
A
B
224
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Figure 7. Interannual variation of abundance and annual anomalies of (A) PACL and (B) PACLN during the period 2000-2017
at the EPEA station. Red squares: outliers. Dashed line: ns. trend.
2000 2002 2004 2006 2008 2010 2012 2014 2016
Year
Annual anomalies
Abundance
(1 000 ind. m ),
-3
Annual anomalies
Abundance
(1 000 ind. m ),
-3
A
B
225
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
Figure 8. Interannual variation of abundance and annual anomalies of ENO (A) and PAV (B) during the period 2000-2017 at the
EPEA station. Red squares: outliers. Dashed line: ns. trend.
-.10
-.05
00.
05.
10.
15.
0
1
2
3
4
5
-.06
-.03
00.
03.
06.
09.
0
1
2
3
4
5
2000 2002 2004 2006 2008 2010 2012 2014 2016
Year
Annual anomalies
Abundance
(1 000 ind. m ),
-3
Annual anomalies
Abundance
(1 000 ind. m ),
-3
A
B
226
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
Figure 9. Interannual variation of abundance and annual anomalies of APP (A) and CHA (B) during the period 2000-2017 at the
EPEA station. Red squares: outliers. Dashed line: ns. trend.
-.12
-.08
-.04
00.
04.
08.
00.
05.
10.
15.
20.
25.
-.16
-.08
0
08.
16.
0
5
10
15
20
25
2000 2002 2004 2006 2008 2010 2012 2014 2016
Year
Annual anomalies
Abundance
(1 000 ind. m ),
-3
Annual anomalies
Abundance
(1 000 ind. m ),
-3
A
B
voudaki et al. 2007) including the Argentine shelf
where they distribute in a large latitudinal range
(Ramírez, 1981; Cepeda et al. 2018). Moreover, it
was shown that small copepods and their early
developmental stages dominate all marine com-
munities (Hopcroft et al. 2001).
In the taxonomic analysis, a great percentage of
adults (ca. 80%) of Oithonidae were identified as
belonging to O. nana (not shown). Accordingly,
the present study assumes that most of the cope-
podite and nauplii stages of Oithonidae also cor-
responded to this species. In coincidence with the
present findings, a high abundance of O. nana in
all seasons has been typically observed at the
EPEA station (Temperoni et al. 2011; Viñas et al.
2013). The great tolerance of this species to sea-
sonal variation of temperature might explain its
ample distribution in temperate and tropical
coastal waters all around the world, i.e. the
Mediterranean Sea (Jamet et al. 2001), Southamp-
ton Water (Williams and Muxagata 2006), and the
Argentine shelf (Cepeda et al. 2015, 2018).
The notorious numerical dominance of
Oithonidae (mainly O. nana) all through the year
is probably related to its ability to consume a
wide size range of food particles including micro-
phytoplankton, microbial heterotrophic compo-
nents, and copepod nauplii (Paffenhöfer 1993;
Turner 2004; Atienza et al. 2006; Madsen et al.
2008; Böttjer et al. 2010). An additional advan-
tage could be the reproductive modality of this
species. The egg-carrier trait might be a good
strategy to prevent eggs predation, thus assuring
higher survival rates and consequently more
abundant populations (Kiørboe et al. 2015).
On a seasonal basis, the abundance of O. nana
started increasing in winter and attained its high-
est abundance in spring. In accordance, micro-
phytoplankton showed a similar pattern (Viñas et
al. 2013; Negri et al. in preparation). During this
period, adequate temperature range and food
availability have probably stimulated O. nana
females to reproduce intensively producing the
highest peak of nauplii of the year. O. nana as
well as Paracalanidae, very abundant in summer,
might have taken advantage of high densities of
microbial components associated to the abun-
dant picophytoplankton fraction recorded during
this season. In fact, this fraction had an outstand-
ing contribution from the end of spring up to
early autumn (Ruiz et al. 2020; Negri et al. in
preparation) during present period. Silva et al.
(2009) reported that this fraction can reach 50-
90% of the total Chl-a at the EPEA station dur-
ing summer.
It is worth mentioning that small copepods
(such as all stages of O. nana and Paracalanidae-
Clausocalanidae) are not able to graze efficiently
upon nano and picophytoplankton components.
In fact, these fractions are consumed by nano-
and micro-heterotrophs which are predated by
protozooplankton, especially ciliates, and the lat-
ter are the main prey for small copepods. In par-
ticular, they have a greater influence on the effi-
ciency of the trophic food webs than larger
species, coupling between the primary producers,
the protozooplankton, and the higher trophic lev-
els (Zervoudaki et al. 2007).
Microbial filter-feeders P. avirostris and
appendicularians displayed also their maximum
abundance in summer. As mentioned above, this
period is characterized by a strongly stratified
water column with phytoplankton biomass most-
ly represented by nano- and picophytoplankton
fractions (Silva et al. 2009; Viñas et al. 2013).
Penilia avirostris grazes mostly on small flagel-
lates, dinoflagellates and diatoms (Atienza et al.
2006), whereas appendicularians are major pico-
and nanoplankton feeders (Flood et al. 1992;
Tönnesson et al. 2005). The dominance of micro-
bial filter-feeding such as cladocerans and lar-
vaceans in warmer seasons is a common feature
in coastal waters of the Mediterranean (Ribera
d’Alcalá et al. 2004) and the Aegean and Black
Seas (Siokou-Frangou et al. 2004) as well as in
the Northeast Atlantic (Rodriguez et al. 2000).
In summer, chaetognaths, mostly represented
by S. friderici (Daponte et al. 2004) also exhibit-
227
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
ed their highest abundance. It is well known that
older chaetognaths prey upon appendicularians
(Purcell et al. 2004) and small copepodite stages
(Sato et al. 2011a), which are very abundant dur-
ing this season.
Present series recorded the highest abundance
of the herbivorous calanoid C. carinatus in cold
waters of winter and spring. The high nutrient
input typical of the mixing during the winter peri-
od and the starting of water column stratification
in spring favor the development of the main phy-
toplankton bloom of the year represented mainly
by the microphytoplankton fraction (Carreto et al.
1998; Negri and Silva 2003; Viñas et al. 2013).
Diatoms and dinoflagellates are the main food of
C. carinatus (Cepeda et al. 2018 and references
therein).
Long term annual and seasonal variability
During the study period, a positive trend of
interannual anomalies was observed in the mean
temperature of the water column, but it was non-
significant. However, bottom and surface temper-
ature analysis of a longer series (19 years) in the
EPEA showed a significant positive trend, as also
occurred in an extended satellite-sea surface-tem-
perature-series (Luz Clara et al. in preparation).
In support of our initial hypothesis, the abun-
dance of Family Oithonidae (more abundant
small copepods of the EPEA zooplankton com-
munity) increased during the 18 years of observa-
tion. This is clearly perceived when comparing
the abundance of this species at the beginning of
the series (period 2000-2001; Viñas et al. 2013)
with results of the entire series between 2000 and
2017. In summer 2000, OIT abundance (adults +
copepodites) was 4,428 ± 5,816 ind. m
-3
on aver-
age, whereas in the total series it was 7,159 ±
10,289 ind. m
-3
. In spring 2000 its abundance
attained only 2,293 ± 1,497 ind. m
-3
, five times
less than in the present study (mean 11,793 ±
9,200 ind. m
-3
). However, non-significant corre-
lation was found between interannual anomalies
of the abundance of these species and those of the
temperature during the sampling period. Duration
of time-series was probably no long enough to
detect such relationships in both Oithonidae and
other categories of metazooplankton.
It should be noted that in coincidence with the
positive trend observed in Oithonidae, concentra-
tions of Chl
total
and Chl
< 5
showed a significant
increasing trend during the present series (Silva
2011; Ruiz et al. 2020; Negri et al. in prepara-
tion). Percentage of Chl
< 5
displayed a significant
positive trend coincident with a significant posi-
tive tendency of pico and nanophytoplankton
fractions (Negri et al. in preparation). Increasing
food availability from a rich microbial food web
could have favored the development of
Oithonidae populations in the long-term, as it was
observed in summer, on a seasonal scale.
As previously mentioned, small copepod
species are the major contributor to the total
copepod community abundance at the EPEA sta-
tion, especially during the warmest period of the
year. This is probably related to the positive and
direct influence of the increasing temperature on
their reproductive cycle (Uye and Shibuno 1992;
Pittois et al. 2009) as well as the indirect and
favorable influence of this parameter increasing
the abundance of the smaller phytoplankton frac-
tion (Negri et al. in preparation).
But not all the zooplankton species of the
EPEA community seemed to be favored by the
temperature increase and its possible influence
upon the phytoplankton structure and phenology,
among other factors. For example, a significant
decreasing trend was observed in winter on the
abundance of herbivorous like lamellibranch lar-
vae and the calanoid C. carinatus during 2000-
2017 series. The highest peak of abundance of
lamellibranch larvae was recorded in August
(winter). Although no information on the species
composition of these larvae was available in the
present zooplankton series, they probably
belonged to Mytilus platensis, which beds are dis-
tributed in the study area (Bremec and Lasta
1998). A marked synchrony in the emission of
228
MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)
gametes with peaks of reproductive activity dur-
ing September and October has been reported for
M. platensis in the study area (Penchaszadeh
1980). In the present work, maximum emission of
gametes corresponded to August, one month ear-
lier than usual. One explanation for this observed
decreasing anomaly could be the temperature rise
on the sea surface throughout the time-series
studied. In such conditions, adults of M. platen-
sis, stimulated by higher temperature ranges,
could have had their spawning timing earlier,
which could produce a mismatch between the
recently hatched larvae and the adequate phyto-
plankton cells that bloom later in the season. Sim-
ilarly, the decreasing tendency observed in C.
carinatus was probably due to the same causes. In
both cases, fitness consequences tend to be nega-
tive when the organism is at the wrong seasonal
window. In other words, as the species completes
its life span within a single year, the fact of miss-
ing the best window to grow during that year pre-
vents them from getting another chance the fol-
lowing year (Mackas et al. 2012). Future results
of ongoing analysis of phytoplankton diversity
and long-term variability of the present series
(Negri et al. in preparation) would give some
insight to test this hypothesis.
Perturbations to average seasonal cycles of
environmental conditions, and the ability (or
inability) of biota to track these variations are
very important drivers of interannual variability
in growth, survival, and population size (Mackas
et al. 2012), as it was observed in the present
work.
Small copepods represent a main food source
for local fish, especially during larval stages
(Viñas and Ramírez 1996; Sato et al. 2011b). If
the observed increasing tendency of these
species (mainly O. nana and members of Para-
calanidae-Clausocalanidae) remains in the long
term, this would expand the availability of food
for fish larvae, thus favoring their growth and
survival. In the study area, Engraulis anchoita
larvae are dominant during a great part of the
year (Sánchez and Ciechomski 1995). With
acoustic biomass fluctuating between one and
five million tons in the period 1993-2008
(Madirolas et al 2013), this species has a superla-
tive ecological importance because of its central
role in pelagic food webs in the Argentine shelf
(Leonarduzzi et al. 2010 and references therein).
A recent study analyzing the same time-series
denoted that density and nutritional condition of
anchovy larval were higher in spring and
autumn, but lower in winter (Leonarduzzi et al.
2021). Interestingly, the present work shows that
higher concentrations of small copepods (all
stages together) were observed in spring and
summer whereas lower values corresponded to
autumn. Many factors must should be considered
to understand larval-zooplankton relationships:
real concentration of food in the larval habitat (a
mean concentration in the water column is not
the best approach), seasonal predators abundance
(non-considered in present work) and concentra-
tion of other zooplanktonic food items (i.e. pro-
tozooplankton), among others.
Time series provide the oceanographic com-
munity with the long, high-quality data necessary
to characterize the functioning of the ocean (Hen-
son 2014) and help to unravel natural and human-
induced changes in marine ecosystems (Reid and
Valdés 2011). Consequently, these time-series
sampling sites represent a phenomenal heritage
legacy, and intergovernmental bodies such as
ICES, the European Marine Board, or IOC-
UNESCO strongly recommend their continuity
and the establishment of new time-series based
on previous findings (Valdés and Lomas 2017).
CONCLUSIONS
This work covers a time-series of 18 years in
which the variability of main metazooplankton
taxa of the EPEA station was studied for the first
time. Results indicated that small copepods dom-
229
VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION
inate the metazooplankton at this station. The
most abundant family, Oithonidae, showed an
interannual increasing trend during the study
period, whereas lamellibranch larvae and other
cryophilic taxa exhibited a decreasing trend.
Physical parameters (MT, MS and ϕ) did not
show significant interannual trends. However,
temperature exhibited a strong increasing tenden-
cy. No clear relationships were found between
both long-term interannual and seasonal anom-
alies of taxa and those of the physical parameters,
probably because of the short period analyzed.
The increasing of Oithonidae abundance could be
due both to the direct effect of the temperature
rise on their reproductive rates and the positive
influence of this parameter on the concentration
of small phytoplankton fractions, an important
food item for these copepods. Opposite, for other
cryophilic taxa such as Calanidae and lamelli-
branch larvae with decreasing abundances, the
increase of temperature could have had a negative
effect, although the mechanisms involved are less
clear. More observations are necessary to confirm
these hypotheses.
ACKNOWLEDGMENTS
INIDEP provided financial support for samples
collection. We thank all the colleagues of the
DIPLAMCC project who collaborated in onboard
activities during the cruises. We are grateful to the
captains and crews of all the vessels who took
part in EPEA cruises for their shipboard assis-
tance. Part of the equipment used in this work
was acquired through grants from the Agencia
Nacional de Promoción Científica y Tecnológica
(PICT 15227/03), Universidad Nacional de Mar
del Plata EXA717/14 and EXA843/17 to MDV.
Our acknowledgment to anonymous reviewers
who provided very constructive comments on the
earlier version of the manuscript. This is INIDEP
contribution no 2246.
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