Marine Ecology.

ISSN 0173-9565

ORIGINAL ARTICLE

Reproductive traits of Euterpina acutifrons in a coastal area

of Southeastern Brazil

nior, Leonardo K. Miyashita, Naira J. Silva, Salvador A. Gaeta & Rubens M. Lopes
Mauro de Melo Ju
Department of Biological Oceanography, Oceanographic Institute, University of S~
ao Paulo, S~
ao Paulo, Brazil

Keywords
Egg production; Harpacticoida; Southwest
Atlantic; weight-specific egg production;
zooplankton.
Correspondence

nior, Federal Rural
Mauro de Melo Ju
University of Pernambuco, UAST, PO Box:
063, Serra Talhada, Pernambuco 56900-000,
Brazil.
E-mail: mmelojunior@gmail.com
Accepted: 27 October 2012
doi: 10.1111/maec.12041

Abstract
We investigated the reproductive biology of the planktonic harpacticoid copepod
Euterpina acutifrons, including morphometric data, egg production rates (EPR)
and viability, and weight-specific egg production. Experiments were carried out
during 1 year in an inner-shelf area off Ubatuba (SE Brazil), a site seasonally
influenced by bottom intrusions of the relatively cold and nutrient-rich South
Atlantic Central Water (SACW). We hypothesized that E. acutifrons attain higher
reproductive rates when SACW penetrates in this region. Live females were incubated individually in cell culture plates during two periods of 24 h each, under
controlled temperature and light conditions. Euterpina acutifrons carried on average 16.9  6.9 eggs
sac 1, ranging between 10.8  5.7 and 30.8  7.4 eggs
sac 1.
Estimated EPRs ranged from 6.3  3.4 to 13.6  4.2 eggs
female 1
day 1, with mean
weight-specific egg production rates of 0.06  0.04 and 0.17  0.08 per day. Euterpina
acutifrons was not directly influenced by SACW intrusions, but body length and
clutch size were positively related to temperature and chlorophyll content. Egg
hatching time was clearly dependent on water temperature, as a 2 C increase
resulted in a decrease of 15 h in egg hatching time. This shows that even a small
variation in temperature may considerably affect E. acutifrons population
dynamics. Reproductive traits of this pelagic harpacticoid seem, therefore, to be
controlled by the trade-offs between increased food supply and the metabolic
demands at low temperatures associated with SACW bottom intrusions toward
this coastal area.

Introduction
The reproductive biology of marine pelagic copepods has
been largely studied in calanoids and cyclopoids (Sabatini &
Kirboe 1994; Gallienne & Robins 2001; Hirst & Bunker
2003) but our knowledge on most small-sized marine
copepods is still fragmentary. This is particularly evident for
harpacticoid copepods (Uye et al. 2002; B
ottger-Schnack
et al. 2008). Although most harpacticoid copepod species
are benthic, the few species that are planktonic may be quite
abundant (Ara 2001a; Uye et al. 2002).
Euterpina acutifrons (Dana, 1847) is a small pelagic
harpacticoid that often numerically dominates the mesoplanktonic community in coastal and estuarine ecosystems

Marine Ecology 34 (2013) 363372 2013 Blackwell Verlag GmbH

between 66N and 40S (Haq 1972; Sautour & Castel 1995;
Ara 2004; Eskinazi-SantAnna & Bj
ornberg 2006). This
species is eurythermic and euryhaline (DApolito & Stancyk 1979; Ara 2001a) but its thermohaline optimum varies
geographically (Moreira et al. 1982; Vi~
nas & Gaudy 1996).
The scarce investigations on the dietary composition of
E. acutifrons suggest a preference for herbivorous feeding
(Zurlini et al. 1978; Guisande et al. 1996), especially on
diatoms and chlorophytes (Guisande et al. 2002), but also
indicate utilization of small-sized particulate organic matter (Sautour & Castel 1993). Temperature, and food quantity and quality control E. acutifrons population dynamics,
as these parameters influence body length, generation
time, clutch size, and brood volume (Zurlini et al. 1978;

363


nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Reproductive traits of Euterpina acutifrons

Guisande et al. 1996, 2000; Vi~

nas & Gaudy 1996; D
az
et al. 2003).
In the Southwest Atlantic, E. acutifrons occurs throughout the year in wide temperature (1929 C) and salinity
(533) ranges, and attains high numbers mainly in coastal
and estuarine regions (Moreira et al. 1983; Ara 2001a,
2004; Eskinazi-SantAnna & Bj
ornberg 2006). Despite its
relatively high abundance in coastal zones, few studies
have emphasized the reproductive traits and growth of
E. acutifrons (Zurlini et al. 1978; Guisande et al. 1996;
D
az et al. 2003) or measured its egg production or
weight-specific egg production rates (Guisande et al.
2000), particularly in tropical and subtropical areas
(Hopcroft & Roff 1996, 1998). Moreover, the few egg
production estimates available in the tropics have not
accounted for the influence of incubation time and for
the estimation of individual weight-specific egg production rates (e.g. Runge & Roff 2000; Hirst & McKinnon
2001).
The present study focuses on the egg production rates,
hatching success, and weight-specific egg production of
E. acutifrons in relation to temperature and Chl a concentration in a coastal area of Southeastern Brazil, and
whether these rates are affected by the intrusion of the
South Atlantic Central Water (SACW), a relatively cold
and nutrient-rich water mass (Castro & Miranda 1998).
We hypothesized that this species has higher reproductive
rates when SACW penetrates in this subtropical coastal
area.

Material and Methods

Study area

The two oceanographic stations (inner station: 2331 S,

4504 W, 34 m depth; outer station: 2336 S, 4458 W,
40 m depth) studied were located on the inner shelf off Ubatuba, state of S~ao Paulo, on the southeastern coast of Brazil
(Fig. 1). Two water masses occur in this region. Coastal
Water (CW) is characterized by lower salinities (<35) and
temperatures ranging between 21 and 27 C throughout the
year, as a result of the mixture of land-drained water with
coastal shelf waters (Castro et al. 2006). CW occupies the
entire water column on the inner shelf when the South
Atlantic Central Water (SACW) retreats offshore. The
SACW is relatively cold and nutrient-rich with temperatures
and salinities below 20 C and 36.4 (parts per thousand),
respectively. The SACW may be transported southward by
the lower layer of the Brazil Current (200500 m) along the
shelf break (Castro & Miranda 1998). SACW bottom intrusions toward the coast occur mainly during the warm season
when northeast winds prevail (Castro & Miranda 1998).
When favorable winds last long enough during a meteorological cycle, SACW may reach near-surface waters. The
changing vertical position of SACW-driven pycnoclines is a
key factor influencing phyto- (Gaeta et al. 1999) and zooplankton production (Melo J

unior 2009; Miyashita et al.
2009; Miyashita & Lopes 2011), as well as fish recruitment
(Matsuura et al. 1992) in the study area.

Fig. 1. Sampling site off Ubatuba, Southeast

Brazil.

364

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nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Sampling and environmental parameters

Sampling at the inner station was carried out from 13

July to 31 October 2006, and at the outer station from 18
July 2006 to 4 June 2007. Stratified plankton tows were
performed with a closing plankton net (200-lm mesh
size) from near-bottom to mid-depth, and from middepth to surface for later zooplankton enumeration. During SACW intrusions the mid-depth was replaced by the
bottom of the pycnocline as reference for towing distance. Euterpina abundance (ind. m 3) was calculated
from microscopic counts and total sample volume estimated from flowmeter readings. Rapid on-board sample
inspection revealed that Euterpina females were restricted
to the upper layer, an observation later confirmed by
detailed microscopic analysis ashore. As a result, live zooplankton was collected for experimental work by shortterm (35 min) horizontal or oblique tows above the
thermocline (or mid-depth) with the same conical plankton net fitted with a non-filtering cod-end. Live samples
were carefully diluted in ambient seawater and kept in a
cooler to maintain a stable temperature and avoid direct
sunlight. Temperature was measured with a portable thermometer (inner station) or a CTD (outer station). For
total Chl a analysis, 296 ml of surface water was filtered
through Whatman-GF/F filters, extracted with 90%
acetone for 24 h, and determined by fluorometry
(Welschmeyer 1994).
Handling and incubation of females

Euterpina acutifrons females were rapidly (<20 min)

removed from zooplankton samples using wide-bore glass
pipettes, under dim light. Only individuals carrying an
egg sac were selected to ensure incubation of fertilized
females. For each experiment, 1035 females were individually placed in 12-ml cell well culture dishes, filled
with surface seawater collected from the same station,
previously sieved through a 40-lm nylon mesh to remove
large particles such as eggs and nauplii. Approximately
90% of this incubation media was exchanged every 24 h
to replenish the food; this was necessary because if typical
clearance rates of 0.120.45 ml
h 1 observed elsewhere
for E. acutifrons (Sautour & Castel 1993) were applied to
our experimental conditions, food limitation could have
occurred in cell wells after that time interval. Media
replacement was additionally important because food
composition and availability were not evaluated during
incubations. Experimental temperature (1 C) and light
conditions were similar to those recorded at the sampling
station during the same occasion.
Female health and activity were observed at 3-h intervals under a dissecting microscope, and egg hatching and
Marine Ecology 34 (2013) 363372 2013 Blackwell Verlag GmbH

Reproductive traits of Euterpina acutifrons

new clutch production were recorded. Upon detection of

a hatching event, the corresponding female was transferred to a clean cell well filled with new medium (the
same pre-filtered surface seawater), and an additional
24 h incubation round was set for egg production observations at the same inspection interval as before. Only
females producing nauplii in the first incubation round
were selected for the latter round. At the end of each
experiment, females, nauplii and unhatched eggs were
preserved in 4% buffered formalin solution. The remaining females and their eggs were kept under observation
until their nauplii hatched; in such cases the 24-h media
exchange schedule was maintained.
Thirteen egg viability and eight egg production experiments were carried out during the 1-year study. The
lower number of egg production experiments was a consequence of the excessively long hatching times in five of
the experiments, which precluded further incubations
within the available working schedule. In July and August
2006, up to four experiments were initiated on successive
days, each of them using freshly caught copepods from
one of the sampling stations.
Morphometry and weight estimates

Female prosome length, and egg diameter were measured

under a stereomicroscope coupled to a digitizing table
(precision of 0.04%; Roff & Hopcroft 1986). Prosome
length was obtained by measuring from anterior (including
the rostrum) to posterior margins of prosome, in lateral
view. We measured all females from each experiment, and
up to 10 eggs per clutch (all eggs within a clutch when clutch
size was <10). Female dry weight (DW, lg) was obtained
from the following regression equation (Ara 2001b): DW =
8.148 9 10 8 9 PL2.736 (r = 0.94; P < 0.0001), where PL
(lm) is the prosome length. Female carbon content was
estimated from a dry weight factor of 0.46 (Ara 2001b).
For estimating egg carbon content, we used the composite
relationship between egg diameter (ED, lm) and egg carbon content (CE, lg) proposed by Uye & Sano (1995) as
CE = 5.32 9 10 8 9 ED3.04.
Calculation of egg production and viability, and weightspecific egg production

Individual egg production rates (EPR; eggs female 1
day 1)

were calculated based on the equation P = E/F 9 D, where
E is the number of eggs produced (clutch size), F the
number of egg-producing females, and D the egg development time. The egg development time was obtained
for each temperature from the first 24 h experimental
round. Additionally, we calculated the egg hatching rate
according to Satapoomin et al. (2004) from the slope of
365


nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Reproductive traits of Euterpina acutifrons

a linear regression between the incubation time and the

cumulative hatching percentage, and egg hatching time
can be defined as the time required to reach 100% hatching (Satapoomin et al. 2004).
Egg viability rate was calculated based on the number
of hatched nauplii and the clutch size (nauplii + non-viable eggs), all derived from the experimental observations.
The weight-specific egg production was derived from the
egg mass relative to the individual female weight.
Statistical analysis

Differences in environmental parameters, female size, egg

diameter, clutch size, EPR and viability, and weight-specific egg production between seasonal periods were investigated using ANOVA by grouping data into two
categories, with and without SACW influence. Relationships between environmental (temperature and Chl a)
and morphometric and reproductive data were tested
with linear regression analysis.

Results
Hydrography, chlorophyll, and Euterpina abundance

Sea surface temperature varied from 22 C to 25 C

(Fig. 2), with CW being the dominant water mass at both
stations. From early spring (October 2006) to early
autumn (April 2007), the establishment of pycnoclines
associated with bottom temperatures in the range of
1620 C indicated SACW intrusions (Fig. 2). Chl a ranged from 0.35 to 7.32 mg
m 3, with peak concentrations
usually associated with SACW intrusions (Fig. 2).
Euterpina acutifrons abundance was higher during winter
(JulyAugust 2006, and June 2007) when the vertical
temperature gradient was minimal, and spring (October
November 2006). High abundances usually occurred
when bottom temperatures were close to, or above 20 C,
except in October 2006 (Fig. 2).
Morphometry and weight estimates

Smaller individuals were observed during the warmer

months (January and February 2007; Fig. 3), but no significant difference (ANOVA, P > 0.05) in body length was
observed between months with or without SACW influence. The estimated female dry weight varied between 1.25
and 2.96 lg, and averaged 1.98  0.33 lg, corresponding
to a mean carbon weight of 0.91  0.15 lg C.
Egg diameter did not vary between the two seasonal
periods, with or without SACW influence (ANOVA,
P > 0.05). Most eggs (91%) measured between 45 and
60 lm, with the largest percentage in the range of 50 to
366

Fig. 2. Temperature, DT (difference between surface and bottom

temperature), Chl a concentration and Euterpina acutifrons
abundance off Ubatuba, Brazil, July 2006 to June 2007. Horizontal
bars above sampling dates indicate when egg production experiments
were carried out.

55 lm (41%), and a mean of 53.1  2.9 lm. Egg carbon

content varied from 7 to 16 ng C (Table 1).
Reproductive traits

Clutch size averaged 16.9  6.9 eggs
sac 1 (Table 1),

ranging between 10.8  5.7 and 30.8  7.4 eggs
sac 1
(Fig. 3), with a maximum clutch size of 35 eggs
sac 1
observed in three individuals only. Clutch size did not
vary seasonally (ANOVA, P > 0.05). The ratio of egg
diameter to female prosome length varied from 0.091 to
0.122, with a mean of 0.107  0.007.
EPR averaged between 6.3  3.4 and 13.6  4.2 eggs
female 1
day 1 (Fig. 4), with a grand mean of 10.1  2.5
eggs female 1
day 1. Mean weight-specific egg production
rates ranged from 0.06  0.04 to 0.17  0.08 per day
(Fig. 4), with a grand mean of 0.11  0.04 per day. The
high variability in weight-specific egg production rates was
related to an extremely high value observed for a single
female (0.32 per day; outer station, on August 30, 2006).
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nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Reproductive traits of Euterpina acutifrons

(a)

(b)

(c)

(d)

Fig. 3. Euterpina acutifrons: temporal

variability of (a) female prosome length, (b)
egg diameter, (c) clutch size and (d) hatching
success, off Ubatuba, Brazil, July 2006 June
2007. Error bars represent the standard
deviation.

Table 1. Minimum, maximum and mean  standard deviation (SD)

values of some morphometric and reproductive parameters of Euterpina acutifrons females and eggs from Ubatuba, Brazil, June 2006 to
July 2007.

Female
Prosome (lm)
Dry weight (lg)
Carbon weight (lg C)
Eggs
Diameter (lm)
Volume (lm3 9 103)
Carbon weight (pg C)
Egg sacs
Egg number (eggs
sac 1)
Egg/femalea
a

Minimum

Maximum

Mean  SD

422.9
1.25
0.58

579.6
2.96
1.36

486.7  21.4
1.98  0.33
0.91  0.15

39.3
57.19
7

71.9
132.18
16

6
0.091

35
0.122

53.1  2.9
79.39  13.48
92
16.9  6.9
0.107  0.007

Ratio between egg diameter and female prosome length.

EPR and the weight-specific egg production did not vary

seasonally (ANOVA, P > 0.05). Egg viability ranged
between 80 and 99% (mean  SD = 90.2  5.4%; Fig. 3).
The time necessary to attain 100% egg hatching varied
from 26.5 h (24 C) to 41.3 h (22 C), with a typical egg
hatching time dependent on temperature (Fig. 5).
Relationships between morphometric, reproductive, and
environmental variables

There was a positive trend between E. acutifrons prosome

length and Chl a concentration (linear regression;
r2 = 0.25, P < 0.05) and a negative relationship between
Marine Ecology 34 (2013) 363372 2013 Blackwell Verlag GmbH

prosome length and temperature (linear regression;

r2 = 0.37, P < 0.05; Fig. 6). We did not find any correlation between prosome length and reproductive parameters (clutch size and egg diameter; P > 0.05). There was
no relationship between egg diameter and temperature or
Chl a (P > 0.05).
We observed a negative relationship between egg production rates and Chl a (Linear regression; r2 = 0.52,
P < 0.05), indicating that high EPR occurred in low Chl
a concentrations. Clutch size was positively correlated to
Chl a (Linear regression; r2 = 0.27; P < 0.05; Fig. 6), but
not to temperature (P > 0.05). However, weight-specific
egg production rates and egg viability did not correlate
with temperature or Chl a (P > 0.05).
Discussion
Sac spawners usually have lower egg production rates (up
to 7.5 times lower; Kirboe & Sabatini 1995) compared
with broadcast spawners (Bunker & Hirst 2004). However, E. acutifrons had higher or similar mean and maximum egg production rates to those reported for other
sac-spawning (Table 2) and broadcast spawning copepods
off Ubatuba, including Temora turbinata (mean = 2.6  2.4
eggs
female 1
day 1 and maximum = 8.0 eggs
female 1
day 1),
Paracalanus sp. (mean = 4.3  2.9 eggs
female 1
day 1
and maximum = 6.3 eggs
female 1
day 1), and Clausocalanus furcatus (mean = 10.7  4.5 eggs
female 1
day 1 and
unior 2009).
maximum = 16.4 eggs
female 1
day 1) (Melo J

Although E. acutifrons had high mean and maximum egg
production rates, its weight-specific egg production was
similar or lower than that of other sac-spawning species
367


nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Reproductive traits of Euterpina acutifrons

(a)

(b)

Fig. 4. Euterpina acutifrons (a) egg production and (b) weight-specific egg production rates off Ubatuba, Brazil. Error bars represent the
standard deviation.

Fig. 5. Cumulative hatching (CH) in relation to egg hatching time

(HT) of Euterpina acutifrons from Ubatuba, Brazil, July 2006 to June
2007. Error bars represent the standard deviation.

from Ubatuba and other subtropical and tropical areas

(Table 2).
In sac spawners, egg size is usually proportional to
female body length in addition to temperature or female
weight, whereas fecundity is positively correlated to temperature and body weight (Bunker & Hirst 2004). In our
study, female size did not influence egg diameter and
clutch size, but the latter was positively correlated to Chl
a concentration, indicating some influence of autotrophic
food availability on reproductive traits of E. acutifrons off
Ubatuba. However, the observed relationship of clutch
size with chlorophyll is not necessarily connected to an
exclusive herbivorous behavior by E. acutifrons, as this
368

species also preys on detrital material (Sautour & Castel

1993), which may provide a rich attached microbiota as
food source (Tang et al. 2010). Our results on clutch size
were comparable to those reported for E. acutifrons in
Anglesey, UK (Haq 1972), and in R
a de Vigo (Guisande
et al. 1996), but were about half the clutch size measured
in North Atlantic populations by DApolito & Stancyk
(1979) and D
az et al. (2003).
Temperature regulates metabolic demands and reproductive characteristics of marine pelagic copepods (Hirst
& Bunker 2003). We found a substantial reduction in egg
hatching time with temperature increase, as reported for
sac-spawning species (Uye & Sano 1995; Hirst & Bunker
2003), including E. acutifrons (DApolito & Stancyk
1979). The observed 15-h decrease in egg hatching time
off Ubatuba with a temperature rise of only 2 C, from
22 to 24 C (Fig. 5), was within the same range reported
by Haq (1972) in a temperate region, but resulting from
a much higher temperature gradient, from 10 to 20 C.
A further increase to 25 C had a comparatively minor
effect on hatching time in his experiments, and was
accompanied by a 15% failure in egg hatching (Haq
1972). Such latitudinal contrasts in egg development and
hatching time suggest that different E. acutifrons phenotypes have evolved in temperate and tropical/subtropical
populations, each showing a particular range of thermal
responses and tolerances (Moreira et al. 1982; Vi~
nas &
Gaudy 1996).
Studies performed in temperate environments have
shown that phytoplankton biomass and temperature
influence E. acutifrons body length (Zurlini et al. 1978;
Guisande et al. 1996; D
az et al. 2003). An increase in
body size was found for female adults (Zurlini et al.
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nior, Miyashita, Silva, Gaeta and Lopes

Melo Ju

Reproductive traits of Euterpina acutifrons

(a)

(b)

(c)

(d)

Fig. 6. Euterpina acutifrons: relationship between (a) prosome length (PL) and temperature (T), (b) prosome length and chlorophyll a (Chl a), (c)
clutch size (CS) and Chl a, and (d) egg production (EP) and Chl a, Ubatuba, Brazil, July 2006June 2007. Error bars represent the standard
deviation.

1978) and nauplii (Guisande et al. 1996) when high phytoplankton concentration was offered under laboratory
conditions, but D
az et al. (2003) argued that temperature, via female size, is the main factor controlling brood
volume. D
az et al. (2003) found evidence of lack of
influence of chlorophyll content on E. acutifrons reproductive parameters, while we observed a negative correlation between Chl a and egg production rates in this
species.
Our initial hypothesis has to be discharged. In fact, our
results show that E. acutifrons was not influenced by bottom intrusions of the cold- and nutrient-rich SACW off
Ubatuba, as neither abundance nor egg production
increased with the development of the seasonal pycnocline
and the consequent increase in chlorophyll concentration
in the study area. This seems to contradict previous
reports of positive responses of E. acutifrons body size and
abundance to the onset of eutrophic conditions in coastal
Brazilian waters (Yamashita & Moreira 1981) and
elsewhere (D
az et al. 2003). The explanation for our
Marine Ecology 34 (2013) 363372 2013 Blackwell Verlag GmbH

observations likely resides in the poor acclimation of tropical populations of E. acutifrons to low temperatures, as
opposed to populations from temperate coastal areas
(Vernberg & Moreira 1974). Therefore, the populational
dynamics of E. acutifrons in tropical shelf areas subjected
to the influence of cold and nutrient-rich oceanic waters
seem to be controlled by a balance between the benefits of
an increased food supply and the metabolic drawbacks of
low temperatures associated with SACW bottom intrusions.
Acknowledgements
We thank M. Pompeu, T. E. da Silva and M. da Cruz
Santos for their assistance in the field, and the anonymous reviewers and the associate editor for their thoughtful comments and suggestions. This study was partially
supported by the ANTARES project (www.antares.ws).
CAPES (#330020100025P2 to M.M.J.) and CNPq fellowships (#306266/2007-5 and #307928/2010-1 to R.M.L.;
369


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Melo Ju

Reproductive traits of Euterpina acutifrons

Table 2. Mean and maximum egg production rates (EPR; eggs female 1
day 1), and mean and maximum weight-specific egg production rates
(WSEPR; day 1) of some sac spawners copepod species from different subtropical and tropical areas.

Species

EPR (Mean)  SD
or ( SE)

EPR
(Max)

WSEPR
(Mean)

WSEPR
(Max)

T (C)

Chl a (mg
m 3)

Location

Source

Harpacticoida
Euterpina acutifrons
E. acutifrons
E. acutifrons

10.1  2.5
17.7 (7)
21.3 (5.3)

21.8

0.11
0.24
0.30

0.32

22.8
28
28

1.0  0.4
0.35
1.42.6

This study
Hopcroft & Roff (1998)
Hopcroft & Roff (1998)

0.46  0.75
0.21  0.61

9.1
2.8

0.09
0.01

0.10
0.16

20.6
20.6

0.44.1
0.44.1

Ubatuba, Brazil
Lime Cay, Jamaica
Kingston Harbour,
Jamaica
Ubatuba, Brazil
Ubatuba, Brazil

3.4

0.07

28

0.11

Hopcroft & Roff (1998)

Euchaeta marinella

3.2 (0.3)

11.1

0.13

0.48

2830

0.190.4

Discovery Bay,
Jamaica
Andaman Sea,
Thailand

Cyclopoida
Oithona plumifera
O. plumifera

1.8  1.9
2.4 (0.2)

6.6
11.2

0.05
0.05

0.17
0.23

20.6
2830

0.44.1
0.190.4

nior (2009)
Melo Ju
Satapoomin et al. (2004)

O. plumifera

6.5 (1.9)

0.26

28

0.11

Oithona nana

20 (3.9)

0.52

28

0.35

O. nana

17 (4.6)

0.46

28

1.42.6

Oithona simplex

6.7 (1.4)

0.32

28

1.42.6

Oncaea venusta
O. venusta

7.6  12.4
11.5 (0.9)

76.6
38.1

0.03
0.02

0.32
0.07

20.6
2830

0.44.1
0.190.4

Oncaea spp.

10.5

0.07

28

0.11

Onychocorycaeus
giesbrechti
Ditrichocorycaeus
amazonicus

19.8  8.6

28.8

0.30

0.42

20.6

0.44.1

Ubatuba, Brazil
Andaman Sea,
Thailand
Discovery Bay,
Jamaica
Lime Cay,
Jamaica
Kingston Harbour,
Jamaica
Kingston Harbour,
Jamaica
Ubatuba, Brazil
Andaman Sea,
Thailand
Discovery Bay,
Jamaica
Ubatuba, Brazil

49.5 (12.3)

0.43

28

1.42.6

Kingston Harbour,
Jamaica

Hopcroft & Roff (1998)

Macrosetella gracilis
Microsetella rosea
Calanoida
Euchaeta marina

nior (2009)
Melo Ju

nior (2009)
Melo Ju

Satapoomin et al. (2004)

Hopcroft & Roff (1998)

Hopcroft & Roff (1998)
Hopcroft & Roff (1998)
Hopcroft & Roff (1998)

nior (2009)
Melo Ju
Satapoomin et al. (2004)
Hopcroft & Roff (1998)

nior (2009)
Melo Ju

T, temperature; SD (standard deviation) or SE (standard error).

#142203/2010-6 and #142050/2012-1 to L.K.M.) were

awarded during the course of this study. M.M.J. was also
supported with funds from the CAPES/PROAP program.
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