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 VIÑAS1, 2, *, GEORGINA D. CEPEDA1, 2 and MOIRA LUZ CLARA1, 2, 3

1Instituto Nacional de Investigación y Desarrollo Pesquero (INIDEP), Paseo Victoria Ocampo Nº 1, Escollera Norte, B7602HSA - Mar del

Plata, Argentina. 2Instituto 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. 3Instituto 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 ϕindicate

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 ϕrecorded during this season.

215

VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION

Table 1. Mean seasonal values ±SD of MT, MS and ϕat 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

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-aat 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 Chltotal and Chl<5showed a significant

increasing trend during the present series (Silva

2011; Ruiz et al. 2020; Negri et al. in prepara-

tion). Percentage of Chl<5displayed 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.

REFERENCES

ATIENZA D, CALBET A, SAIZ E, ALCARAZ M, TRE-

PAT I. 2006. Trophic impact, metabolism, and

biogeochemical role of the marine cladoceran

Penilia avirostris and the co-dominant cope-

pod Oithona nana in NW Mediterranean

coastal waters. Mar Biol. 50: 221-235.

BEAUGRAND G, KIRBY RR. 2018. How do marine

pelagic species respond to climate change?

Theories and observations. Ann Review Mar

Sci. 10: 169-197.

BEHRENFELD MJ, O’MALLEY RT, SIEGEL DA,

MCCLAIN CR, SARMIENTO JL, FELDMAN GC,

MILLIGAN AJ, FALKOWSKI PG, LETELIER RM,

Boss ES. 2006. Climate-driven trends in con-

temporary ocean productivity. Nature. 444:

752-755.

BÖTTJER D, MORALES CE, BATHMANN U. 2010.

Trophic role of small cyclopoid copepod nau-

plii in the microbial food web: a case study in

the coastal upwelling system off central Chile.

Mar Biol. 157: 689-705.

BREMEC CM, LASTA M. 1998. Mapeo sinóptico

del macrobentos asociado a la dieta en fondos

de alimentación de la corvina rubia (Micropo-

gonias furnieri) en el área de El Rincón.

Noviembre, 1994. INIDEP Inf Téc. 21: 117-

132.

CAPITANIO FL, CURELOVICH J, TRESGUERRES M,

NEGRI RM, VIÑAS MD, ESNAL G. 2008. Sea-

sonal cycle of appendicularians at a coastal

station (38°28′S, 57°41′W) of the SW Atlantic

Ocean. B Mar Sci. 82:171-184.

CARRETO JI, AKSELMAN R, MONTOYA NG, NEGRI

RM, BENAVÍDES HR, CARIGNAN MO, CUCCHI

COLLEONI AD. 1998. Alexandrium tamarense

Bloom dynamics and Mytilus edulis toxicity in

the coastal waters off Mar del Plata (Argenti-

na). In: REGUERA B, BLANCO J, FERNÁNDEZ

MI, WYATT T, editors. Harmful microalgae.

Santiago de Compostela: Xunta de Galicia and

230 MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)

IOC-UNESCO: 135-138.

CEPEDA G. 2013. Sistemática molecular, distribu-

ción y dinámica poblacional de las especies de

Oithona (Copepoda, Cyclopoida) en diversos

sectores costeros del Mar Argentino [PhD the-

sis]. Mar del Plata: Facultad de Ciencias Exac-

tas y Naturales, Universidad Nacional de Mar

del Plata. 193 p.

CEPEDA GD, DIMAURO RP, HOZBOR MC, CUCCHI

COLLEONI BD, HERNÁNDEZ D, VIÑAS MD.

2015. Spatial variation in life-history traits of

Oithona spp. in a shallow temperate estuarine

system (Río de la Plata, south-west Atlantic)

during spring. Mar Freshwater Res. 66: 795-

804.

CEPEDA G, TEMPERONI B, SABATINI M, VIÑAS

MD, DERISIO C, SANTOS B, ANTACLI J, PADO-

VANI L. 2018. Zooplankton communities of the

Argentine continental shelf (SW Atlantic, ca.

34°-55°S) an Overview. In: HOFFMEYER M,

SABATINI M, BRANDINI F, CALLIARI D, SANTI-

NELLI N, editors. Plankton ecology of the

Southwestern Atlantic from the subtropical to

the subantarctic realm. Springer. p. 171-200.

DAPONTE MC, CAPITANIO FL, NAHABEDIAN DE,

VIÑAS MD, NEGRI RM. 2004. Sagitta friderici

Ritter-Zahony (Chaetognatha) from South

Atlantic waters: abundance, population struc-

ture, and life cycle. ICES J Mar Sci. 61: 680-

686.

DIMAURO R, CAPITANIO F, VIÑAS MD. 2009.

Capture efficiency for small dominant meso-

zooplankters (Copepoda, Appendicularia) off

Buenos Aires Province (34°S-41°S), Argen-

tine Sea, using two plankton mesh sizes. Braz

J Oceanogr. 57: 205-214.

DIOSALVI N. 2006. Estudio del ciclo anual del

mesozooplancton en una estación permanente

ubicada en aguas costeras bonaerenses [tesis

de grado]. Mar del Plata: Facultad de Ciencias

Exactas y Naturales, Universidad Nacional de

Mar del Plata. 48 p.

EDWARDS M, RICHARDSON AJ. 2004. The impact

of climate change on the phenology of the

plankton community and trophic mismatch.

Nature. 430: 881-884.

EDWARDS M, BEAUGRAND G, HAYS GC, KOSLOW,

JA, RICHARDSON AJ. 2010. Multidecadal

oceanic ecological datasets and their applica-

tion in marine policy and management. Trends

Ecol Evol. 25: 602-610.

FLOOD PR, DEIBEL D, MORRIS CC. 1992. Filtra-

tion of colloidal melanin from sea-water by

planktonic tunicates. Nature. 355: 630-632.

HAYS GC, RICHARDSON AJ, ROBINSON C. 2005.

Climate change and plankton. Trends Ecol

Evol. 20: 337-344.

HENSON SA. 2014. Slow science: the value of

long ocean biogeochemistry records. Philos

Trans R Soc A. 372. doi:10.1098/rsta.2013.

0334

HOPCROFT RR, ROFF JC, CHAVEZ FP. 2001. Size

paradigms in copepod communities: a re-

examination. Hydrobiologia. 453: 133-141.

[IPCC] GRUPO INTERGUBERNAMENTAL DE EXPER-

TOS SOBRE EL CAMBIO CLIMÁTICO. 2019. El

océano y la criosfera en un clima cambiante.

Informe especial del Grupo Intergubernamen-

tal de Expertos sobre el Cambio Climático.

Resumen para responsables de políticas. In:

PÖRTNER HO, ROBERTS DC, MASSON-DELMOT-

TE V, Z HAI P, TIGNOR M, POLOCZANSKA E,

MINTENBECK K, NICOLAI M, OKEM A, PET-

ZOLD J, RAMA B, WEYER NM, editors. Geneva:

IPCC. 38 p.

JAMET JL, BOGÉ G, RICHARD S, GENEYS C, JAMET

D. 2001. The zooplankton community in bays

of Toulon area (northwest Mediterranean Sea,

France). Hydrobiologia. 457: 155-165.

KIØRBOE T, CEBALLOS S, HØGSBRO THYGESEN U.

2015. Interrelations between senescence, life-

history traits, and behavior in planktonic cope-

pods. Ecology. 96 (8): 2225-2235.

LENTINI CAD, CAMPOS EJD, PODESTÁ GG. 2000.

The annual cycle of satellite derived sea sur-

face temperature on the western South

Atlantic shelf. Rev Bras Oceanogr. 48 (2): 93-

105.

231

VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION

LEONARDUZZI E, BROWN DR, SÁNCHEZ R. 2010.

Seasonal variations in the growth of anchovy

larvae (Engraulis anchoita) on the Argentine

coastal shelf. Sci Mar. 74: 267-274.

LEONARDUZZI E, DOSOUTO M, DIAZ MV. 2021.

Early stages of anchovy: abundance, variabil-

ity and larval condition at the fixed coastal sta-

tion EPEA between 2000-2017. Mar Fish Sci.

34 (2): 123-142.

LIWKW, HARRISON WG. 2008. Propagation of

an atmospheric climate signal to phytoplank-

ton in a small marine basin. Limnol Oceanogr.

53: 1734-1745.

LUZ CLARA M, SIMIONATO CG, JAUREGUIZAR AJ.

2019. Annual variability of sea surface tem-

perature in the northern Argentinean continen-

tal shelf. Geoacta. 43.

MACKAS DL, GREVE W, EDWARDS M, CHIBA S,

TADOKORO K, ELOIRE D, MAZZOCCHI MG,

BATTEN S, RICHARDSON A, JOHNSON C, et al.

2012. Changing zooplankton seasonality in a

changing ocean: comparing time series of zoo-

plankton phenology. Progr Oceanogr. 97-100:

31-62.

MACKAS D, THOMSON RE, GALBRAITH M. 2001.

Covariation of zooplankton community

changes and oceanographic conditions on the

British Columbia continental margin, 1995-

1998. Can J Fish Aquat Sci. 58: 1-18.

MADIROLAS A, CABREIRA A, HANSEN JE. 2013.

Revisión y síntesis de las estimaciones acústi-

cas de abundancia de anchoíta (Engraulis

anchoita) efectuadas entre 1993 y 2008. Rev

Invest Desarr Pesq. 23: 35-48.

MADSEN SD, NIELSEN TG, HANSEN BW. 2008.

Annual population development and produc-

tion by small copepods in Disko Bay, western

Greenland. Mar Biol. 155: 63-77.

MARTÍNEZ-AVELLANEDA N. 2005. Ciclo anual y

variabilidad de baja frecuencia de la tempera-

tura superficial del mar en el Océano Atlántico

Sudoccidental [tesis de licenciatura]. Buenos

Aires: Facultad de Ciencias Exactas y Natura-

les, Universidad de Buenos Aires. 133 p.

MAUCHLINE J. 1998. The biology of calanoid

copepods. Adv Mar Biol. 33. 710 p.

MAZZOCCHI MG, RIBERA D’ALCALA M. 1995.

Recurrent patterns in zooplankton structure

and succession in a variable coastal environ-

ment. ICES J Mar Sci. 52: 679-691.

MORAN XAG, LÓPEZ-URRURIA A, CALVO-DIAZ A,

LIWKW. 2010. Increasing importance of

small phytoplankton in a warmer ocean. Glo-

bal Change Biol. 16: 1137-1144.

MULLER KARGER FE, PIOLA A, VERHEYE HM,

O’BRIEN TD, LORENZONI L. 2017. South

Atlantic Ocean. In: O’BRIEN TD, LORENZONI

L, ISENSEE K, VALDÉS L, editors. What are

Marine Ecological Time Series telling us

about the ocean? A status report. IOC-UNES-

CO, IOC Tech Ser. 129: 83-96.

NEGRI R, SILVA RI. 2003. Contribución de las dis-

tintas fracciones del fitoplancton a la biomasa

fototrófica durante un ciclo anual en la esta-

ción EPEA (38° 28′ S-57° 41′ W). V Jornadas

Nacionales de Ciencias del Mar. Mar del

Plata, Argentina. 147.

NEGRI R, SILVA RI. 2011. Estructura de la comu-

nidad del fitoplancton en la estación costera

EPEA durante el período 2000-2010 (provin-

cia de Buenos Aires, Argentina). Bol Soc

Argent Bot. 46 (Supl): 99-100.

O’BRIEN TD, LÓPEZ URRUTIA A, WIEBE PH, HAY

S. 2008. ICES Zooplankton Status Report

2006/2007. ICES Coop Res Rep. 292: 167 p.

O’BRIEN TD, LORENZONI L, ISENSEE K, VALDÉS L,

editors. 2017. What are Marine Ecological

Time Series telling us about the ocean? A sta-

tus report. IOC-UNESCO, IOC Tech Ser. 129

297 p.

O’BRIEN TD, WIEBE PH, FALKENHAUG T, editors.

2013. ICES Zooplankton Status Report

2010/2011. ICES Coop Res Rep. 318: 208 p.

PAFFENHÖFER GA. 1993. On the ecology of mari-

ne cyclopoid copepods (Crustacea, Copepoda,

Cyclopoida). J Plankton Res. 15: 37-55.

PENCHASZADEH P. 1980. Ecología larvaria y reclu-

tamiento del mejillón del Atlántico Surocci-

232 MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)

dental, Mytilus platensis D’Orbigny. Cah Biol

Mar. 21:169-179.

PITTOIS SG, SHAW M, FOX CJ, FRID CL. 2009. A

new fine-mesh zooplankton time series from

the Dove sampling station (North Sea). J

Plankton Res. 31: 337-343.

PODESTÁ GP, BROWN OB, EVANS RH. 1991. The

annual cycle of satellite-derived sea surface

temperature in the Southwestern Atlantic

Ocean. American Meteorological Society. J

Climate. 4: 157-467.

PURCELL JE, STURDEVANT MV, GALT CP. 2004. A

review of appendicularians as prey of inverte-

brate and fish predators. In: GORSKY G,

YOUNGBLUTH MJ, DEIBEL D, editors.

Response of marine ecosystems to global

change. Ecological impact of appendiculari-

ans. Paris: Editions des Archives Contempo-

raines. 359-435.

RAMÍREZ, FC. 1981. Zooplancton y producción

secundaria. Parte I. Variación y distribución

estacional de los copépodos. Contrib Inst Nac

Invest Desarr Pesq (Mar del Plata) Nº 383:

202-212.

REID PC, VALDÉS L. 2011. ICES status report on

climate change in the North Atlantic. ICES

Coop Res Rep. 310: 262 p.

RIBERA D’ALCALÁ MR, CONVERSANO F, CORATO

F, LICANDRO P, MANGONI O, MARINO D, MAZ-

ZOCCHI MG, MODIGH M, MOTRESOR M, NAR-

DELLA M, et al. 2004. Seasonal patterns in

plankton communities in a pluriannual time

series at a coastal Mediterranean site (Gulf of

Naples): an attempt to discern recurrences and

trends. Sci Mar. 68 (Suppl 1): 65-83.

RICE E, STEWART G. 2016. Decadal changes in

zooplankton abundance and phenology of

Long Island Sound reflect interacting changes

in temperature and community composition.

Mar Env Res. 120: 154-165.

RICHARDSON AJ. 2008. In hot water: zooplankton

and climate change. ICES J Mar Sci. 65: 279-

295.

RISARO D. 2020 Las tendencias de largo plazo de

la temperatura superficial del mar alrededor de

Sudamérica y su posible impacto ecológico

[PhD thesis]. Ciudad Autónoma de Buenos

Aires: Facultad de Ciencias Exactas y Natura-

les, Universidad de Buenos Aires. 185 p.

RODRÍGUEZ F, FERNÁNDEZ E, HEAD RN, HARBOUR

DS, BRATBAK G, HELDAL M, HARRIS RP. 2000.

Temporal variability of viruses, bacteria, phy-

toplankton and zooplankton in the western

English Channel off Plymouth. J Mar Biol

Assoc UK. 80: 575-586.

RUIZ MG, LUTZ VA, SEGURA V, B ERGHOFF CF,

NEGRI RM. 2020. The color of Epea: variabil-

ity in the in situ bio-optical properties in the

period 2000-2017. Mar Fish Sci. 33 (2): 205-

225.

SABATINI ME, MARTOS P. 2002. Mesozooplankton

features in a frontal area off northern Patago-

nia (Argentina) during spring 1995 and 1998.

Sci Mar. 66 (3): 215-232.

SÁNCHEZ RP, CIECHOMSKI JD. 1995. Spawning

and nursery grounds of pelagic fish species in

the sea-shelf off Argentina and adjacent areas.

Sci Mar. 59: 455-478.

SARMIENTO JL, SLATER R, BARBER R, BOPP L,

DONEY SC, HIRST AC, KLEYPAS J, MATEAR R,

MIKOLAJEWICZ U, MONFRAY P. et al. 2004.

Response of ocean ecosystems to climate

warming. Global Biogeochem. Cycles. 18:

GB3003. doi:10.1029/2003GB002134

SATAPOOMIN S, NIELSEN TG, HANSEN PJ. 2004.

Andaman-Sea copepods. Spatio-temporal

variations in biomass and production and role

in the pelagic food web. Mar Ecol Prog Ser.

274: 99-122.

SATO NE, HERNÁNDEZ D, VIÑAS MD. 2011a.

Hábitos alimentarios de Sagitta friderici Rit-

ter-Zahony, en las aguas costeras de la Provin-

cia de Buenos Aires, Argentina. Bol Investig

Mar Costeras. 40 (1): 59-74.

SATO NE, HERNÁNDEZ D, VIÑAS MD. 2011b.

Hábitos alimentarios de las larvas de Engrau-

lis anchoita (Hubbs & Marini, 1935) en las

aguas costeras de la Provincia de Buenos

233

VIÑAS ET AL.: ZOOPLANKTON VARIABILITY AT THE EPEA STATION

Aires, Argentina. Lat Am J Aquat Res. 39: 16-

24.

SILVA RI. 2011. Dinámica del ultrafitoplancton en

el Mar Argentino [PhD thesis]. Mar del Plata:

Facultad de Ciencias Exactas y Naturales,

Universidad Nacional de Mar del Plata. 187 p.

SILVA RI, NEGRI RM, LUTZ VA. 2009. Summer

succession of ultraphytoplankton at the EPEA

coastal station (Northern Argentina). J Plank-

ton Res. 31 (4): 447-458.

SIMPSON JH. 1981. The shelf-sea fronts: implica-

tions of their existence and behavior. Phil

Trans Roy Soc London A. 302: 531-546.

SIOKOU-FRANGOU I, SHIGANOVA T, CHRISTOU ED,

KAMBURSKA L, GUBANOVA A, KONSULOV A,

MUSAEVA EI, SKRYABIN VA, KHOROSHILOV V.

2004. Mesozooplankton communities in the

Aegean and Black seas: a comparative study.

Mar Biol. 114: 111-126.

STATSOFT, INC. 2007. STATISTICA (data analysis

software system), version 8.0. www.statsoft.

com.

TEMPERONI B, VIÑAS MD, DIOVISALVI NR, NEGRI

RM. 2011. Seasonal production of Oithona

nana Giesbrecht, 1893 (Copepoda: Cyclopoi-

da) in temperate coastal waters off Argentina.

J Plankton Res. 33: 729-740.

TÖNNESSON K, MAAR M, VARGAS C, MØLLER EF,

SATAPOOMIN S, ZERVOUDAKI S, CHRISTOU E,

GIANNAKOUROU A, SELL A, PETERSEN JK, et al.

2005. Grazing impact of Oikopleura dioica

and copepods on an autumn plankton commu-

nity. Mar Biol Res. 1: 365-373.

TURNER JT. 2004. The importance of small plank-

tonic copepods and their roles in pelagic

marine food webs. Zool Stud. 43: 255-266.

UYE S, SHIBUNO N. 1992. Reproductive biology

of the planktonic copepod Paracalanus sp. in

the Inland Sea of Japan. J Plankton Res. 14:

343-358.

VALDÉS L, LOMAS MW. 2017. New light for ship-

based time series. In: O’BRIEN TD, LORENZONI

L, ISENSEE K, VALDÉS L, editors. What are

Marine Ecological Time Series telling us

about the ocean? A status report. IOC-

UNESCO, IOC Tech Ser. 129: 11-17.

VIÑAS MD. 1990. Influence de la température sur

la durée du développement d’Euterpina acuti-

frons (Copepoda: Harpacticoida) elevé au

laboratoire. Mar Nat. 3: 29-35.

VIÑAS MD, NEGRI RM, CEPEDA GD, HERNÁNDEZ

D, SILVA R, DAPONTE MC, CAPITANIO FL.

2013. Seasonal succession of zooplankton in

coastal waters of the Argentine Sea (South-

west Atlantic Ocean): prevalence of classical

or microbial food webs. Mar Biol Res. 9 (4):

371-382.

VIÑAS MD, RAMÍREZ FC. 1996. Gut analysis of

first-feeding anchovy larvae from Patagonian

spawning area in relation to food availability.

Arch Fish Mar Res. 43: 231-256.

VIÑAS MD, RAMÍREZ FC, SANTOS B, MARRARI M.

2007. Spatial and temporal distribution pat-

terns of cladocerans in the Argentine Sea.

Hydrobiologia. 594: 59-68.

WILLIAMS JA, MUXAGATA E. 2006. The seasonal

abundance and production of Oithona nana

Copepoda: Cyclopoida) in Southampton

Water. J Plankton Res. 28: 1055-1065.

ZERVOUDAKI S, CHRISTOU ED, NIELSEN TG,

SIOKOU-FRANGOU I, ASSIMAKOPOULOU G,

GIANNAKOUROU A, MAAR M, PAGOU K,

KRASAKOPOULOU E, CHRISTAKI U, et al. 2007.

The importance of small-sized copepods in a

frontal area of the Aegean Sea. J Plankton Res.

29: 317-338.

234 MARINE AND FISHERY SCIENCES 34 (2): 211-234 (2021)