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Revista de Biología Tropical, ISSN electrónico: 2215-2075 Vol. 69(S1): 452-463, March 2021 (Published Mar. 10, 2021)

Embryonic and larval development is conditioned by water temperature

and maternal origin of eggs in the sea urchin Arbacia dufresnii

(Echinodermata: Echinoidea)

Jimena Pía Fernández

1,2

Florencia Belén Chaar

1,2,3

Lucía Epherra

Jorge Marcelo González-Aravena

Tamara Rubilar

1,2

1. Laboratory of Chemistry of Marine Organisms, Instituto Patagónico del Mar, National University of Patagonia San

Juan Bosco, Bv. Almte. Brown 3051, Puerto Madryn, Argentina; rubilar@cenpat-conicet.gob.ar (*Correspondence).

2. Biological Oceanography Laboratory, Centro para el Estudio de Sistemas Marinos, Centro Nacional Patagónico,

Consejo Nacional de Investigaciones Científicas y Técnicas, Blvd. Almte. Brown 2915, Puerto Madryn, Argentina;

jpfernandez@cenpat-conicet.gob.ar; lepherra@cenpat-conicet.gob.ar

3. National University of Patagonia San Juan Bosco, Blvd. Almte. Brown 3051, Puerto Madryn, Argentina;

chaar@gmail.com

4. Scientific Department, Chilean Antarctic Institute, Plaza Muñoz Gamero 1055, Punta Arenas, Chile;

mgonzalez@inach.cl

Received 16-VII-2020. Corrected 30-X-2020. Accepted 02-XI-2020.

ABSTRACT

Introduction: Embryonic and larval development in sea urchins is highly dependent on maternal nutritional

status and on the environmental conditions of the seawater. Objective: To compare the development of Arbacia

dufresnii in two different water temperatures and in progeny with varying maternal origins. Methods: We

induced A. dufresnii females and males from Nuevo Gulf to spawn, collected the eggs of each female individu-

ally (progeny), separated them into two seawater temperatures (12 and 17 °C), and fertilized them. We recorded

the percentage of fertilized eggs and embryos per developmental stage according to time, temperature and

progeny. We measured larval growth by total length (TL) and midline body length (M) according to time post

fecundation (DPF), temperature, and progeny. Results: Temperature did not affect fertilization, but embryo

development was faster and more synchronized in the high temperature treatment. The generalized linear models

indicate that embryo development depends on a quadruple interaction between the embryonic stage, time (h),

seawater temperature and progeny. Larval growth was faster, producing larger larvae at the highest tempera-

ture. Larval growth depends on a triple interaction between time (DPF), seawater temperature and progeny.

Conclusions: We found a temperature and progeny impact during embryonic and larval development and, in

both cases, these factors generate a synergistic effect on developmental timing and larval size. This probably

provides a survival advantage as a more rapid speed of development implies a decrease in the time spent in the

water column, where the sea urchins are vulnerable to biotic and abiotic stressors.

Key words: Echinoderm; Echinoidea; parental provisioning; thermal effect; early life stages; larval growth.

Fernández, J.P., Chaar, F.B., Epherra, L., González-Aravena,

J.M., & Rubilar, T. (2021). Embryonic and larval

development is conditioned by water temperature

and maternal origin of eggs in the sea urchin Arbacia

dufresnii (Echinodermata: Echinoidea). Revista de

Biología Tropical, 69(S1), 452-463. DOI 10.15517/

rbt.v69iSuppl.1.46384

DOI 10.15517/rbt.v69iSuppl.1.46384

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Revista de Biología Tropical, ISSN electrónico: 2215-2075, Vol. 69(S1): 452-463, March 2021 (Published Mar. 10, 2021)

Embryonic and larval development in sea

urchins is highly dependent on maternal nutri-

tional status (George, Cellario & Fenaux, 1990;

Byrne, Sewell, & Prowse, 2008a; Byrne et

al., 2008b; Wong, Kozal, Leach, Hoshijima

& Hofmann, 2019) and on the environmental

seawater conditions in which they develop

(Sewell & Young, 1999; Gibson, Atkinson,

Gordon, Smith, & Hughes, 2011; Przeslawski,

Byrne & Mellin, 2015). Maternal nutritional

status depends on food availability, which var-

ies amongst regions and sea urchin populations

(George et al.,1990; Epherra et al., 2015; Wong

et al., 2019). During the gametogenesis, these

nutritional reserves transfer from the female to

the eggs (Walker, Lesser, Unuma, 2013). There-

fore, the nutritional reserves among popula-

tions may vary and, as a result, the quality and

quantity of eggs (George et al., 1990; Epherra

et al., 2015; Wong et al., 2019). As in other

sea urchins, in the Arbacia species, the quality

of eggs influences the development and sur-

vival of the offspring. In Arbacia lixula, better

maternal nutritional status has been related to

the high protein and lipid content of the eggs

and to larval survival (George et al., 1990).

However, in the Arbacia species, the available

data relating to these topics is very limited and

usually refers to A. lixula (Gianguzza, 2020).

Sea urchins embryos and larvae develop

under the influence of many environmental

factors. Seawater temperature is an important

factor, as it has a profound impact on many

physiological processes (Sewell & Young,

1999; Byrne, 2011; Przeslawski et al., 2015).

Temperature affects the kinetics of biochemi-

cal reaction and, therefore, the metabolic and

development rate but, on the other hand, it can

also alter seawater pH or cause oxidative stress

and other cellular stresses (Byrne, 2011; Irvine,

2020). In A. lixula, reproduction and larval

development is enhanced by high temperatures

(Privitera, Noli, Falugi & Chiantore, 2011;

Wangensteen, Turon, Casso & Palacín, 2013)

and some studies indicate that this is a ther-

mophilus species (Pérez-Portela et al. 2019;

Gianguzza et al., 2011). However, all organ-

isms have a limited body temperature range

in which they are functional (Pörtner, 2002).

Beyond the extremes of this range, organ-

isms experience functional constraints and can-

not survive (García, Clemente & Hernández,

2015). However, more studies are still needed

to determine how other Arbacia species react to

an increase in temperature during the different

life stages.

The sea urchin Arbacia dufresnii is an

abundant species in the South Atlantic and

Pacific Oceans (Bernasconi, 1947, 1966; Les-

sios et al., 2012; Brogger et al., 2013). It

presents a large distribution range from the

coast of Buenos Aires (35º S) to Puerto Montt

in Chile (42º S) and the close-lying islands of

the South Atlantic Ocean (Bernasconi, 1947,

1966; Brogger et al., 2013). This wide range

distribution also exposes the different popula-

tions to different seawater temperatures (rang-

ing from 23 ºC to 4 ºC). Food availability and

feeding varies according to the environment

the population inhabits, varying from mainly

herbivore to mainly carnivorous (Penchaszadeh

& Lawrence, 1999; Newcombe, Cárdenas &

Geange, 2012; Epherra, 2016). The population

of A. dufresnii at Nuevo Gulf experiences a

temperature range from 17.35 °C to 10.41 °C

throughout the year (monthly mean) (Rivas,

Pisoni & Dellatorre, 2016). In this population,

the gametogenic cycle starts in the fall and

spawning takes place in the spring and summer

(Brogger et al., 2013; Epherra et al., 2015).

During the spawning period, the seawater tem-

perature increased from 12 °C in early spring

to 17 °C by the end of summer (Rivas et al.,

2016). Some studies have been carried out on

the first stages of the life cycle of A. dufres-

nii (Bernasconi, 1942; Brogger, 2005; Fernán-

dez, Epherra, Sepúlveda & Rubilar, 2019).

Bernasconi (1942) first cultured A. dufresnii

embryos and early larvae at a temperature of

28 to 30 ºC, and later, Brogger (2005) cultured

early embryos and larvae at 26-28 ºC. In both

cases, the cultured organisms started to devel-

op, but after a few days they showed noticeable

signs of stress, stopped growing and died. The

temperatures used in these studies exceeded the

temperature of the natural habits and, possibly,

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the range geographic distribution of the spe-

cies. Fernández et al. (2019), cultured embryos

and larvae of this species up to the 8-armed

echinopluteus, but only at 17 ºC. It can, then,

be concluded that more information is needed

to understand how this species reacts to the dif-

ferent temperatures present in the environments

it inhabits. The aim of this work was to com-

pare the embryonic and larval development of

A. dufresnii at Nuevo Gulf exposed to the two

seawater temperatures normally found in the

sea during the spawning period (12 and 17 ºC),

and to analyze the responses in progeny with

different maternal origins.

MATERIALS AND METHODS

Collection of sea urchins: Arbacia dufres-

nii individuals (Mean = 33.64 ± 1.99 SD mm

diameter) were collected (N = 10) on Febru-

ary 3

2017 from Bahía Kayser, Nuevo Gulf

(42º46’44’’ S; 64º59’52’’ W) and transported

to the Experimental Aquarium at the CENPAT-

CONICET at Puerto Madryn.

Experimental design: Individuals were

acclimated for 24 h in the aquarium. Four

females and four males were used for the study.

The spawning was induced by the injection

in the peristomal membrane of 0.3 ml of a

0.55 M KCl solution (Ettensohn, 2017). The

eggs of each female were individually col-

lected on an aqueous medium (called progeny

one to four) and quantified in triplicate in a

Sedgewick-Rafter chamber using a Leica DM

2 500 microscope. The eggs of each progeny

were separated into two seawater temperatures

(12 °C and 17 °C) to obtain eight experimental

groups of 100 000 eggs each, and they were

placed in 100 ml of sea water filtered up to 1

µm and sterilized with UV light. Male gametes

were dry harvested in a single container and

kept on ice until used to preserve their viabil-

ity (Ettensohn, 2017). To fertilize the eggs of

each experimental group, sperm was used at a

1: 100,000 v/v dilution (around 300: 1 sperm-

egg ratio) and, then, gently mixed, according

to Fernández et al. (2019). After 30 min, two

seawater changes were performed in order to

remove the excess sperm. Fertilization success

was recorded based on the presence of the fer-

tilization envelope on the eggs, using an optical

microscope (Leica DM 2500) and a Bogorov

chamber. In samples of 100 µl from each

experimental group, the percentage of fertiliza-

tion was calculated as: (fertilized eggs / total

eggs) * 100. For the next 48 h, the developing

embryos of each experimental group were kept

with constant and gentle aeration, at a salinity

of 34-35 ppm, and a photoperiod 12 h of light

and 12 h of darkness. In samples of 100 µl from

each experimental group, the percentage of

embryos in the different developmental stages

was determined according to Gilbert (2005) at

different times (2, 3, 4, 6, 12, 24, 30, and 48 h).

Progeny four resulted in low viable embryos,

and they were, consequently, excluded from

the embryo stages determination. After 48 h,

200 swimming larvae of each experimental

group were transferred to a new container with

100 ml of sea water filtered up to 1 µm and

sterilized with UV light. In this case, as only

viable embryos reach the larva stage, the larvae

from progeny four were considered to ana-

lyze larval growth. The larvae were kept with

constant aeration, at a salinity of 34-35 ppm,

photoperiod 12 h of light and 12 h of darkness,

and after 3 days post fecundation (DPF), the

larvae were fed daily with a mix of microalgae

Tetraselmis suecica and Isochrysis galbana

(10 000 cells.ml

-1

). To maintain water qual-

ity, 50% of the seawater in each container was

replaced every 48 h. In order to assess larval

growth over time, between three to four larvae

of each experimental group were taken at 2, 3,

4, 7, 10, 13, 19 and 22 DPF. Each larva was

photographed using a Leica DM 2 500 optical

microscope, Leica ICC50W digital camera and

LAS EZ B4.5.0.418 Software. Images were

analyzed by using the software Image-J. Total

length (TL) and midline body length (M) were

used to monitor larval growth (Fig. 1).

Data analysis: Differences in the fer-

tilization between treatments were analyzed

by using one-way ANOVA. Normality was

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tested by using Kolmogorov-Smirnoff and

the homoscedasticity of variance was tested

using the Levene test (Zar, 1984). To ana-

lyze the effect of temperature, time (DPF)

and progeny (maternal origin of the eggs) in

the abundance of developmental embryonic

stages, a Generalized Linear Model (GLM)

was applied (McCullagh, 1984). We proposed

nineteen different models starting with a null

model (simpler model without any explanatory

variable). We increased complexity into the

models to end up with a complex quadrupole

interaction model. To analyze the effect of tem-

perature, time (DPF) and progeny (maternal

origin of the eggs) on the variables of larval

growth (TL and M), a GLM was also applied.

We proposed twelve different models starting

with a null model. We increased complex-

ity into the models to end up with a complex

triple interaction model. In both cases, the best

model was selected under the Akaike criterion

taking into account the residual analyzes, the

explained variances (deviations) and the prin-

ciple of parsimony or normality. All GLM

analyzes were performed with the free software

RStudio (version 3.5.1), and for the ANOVA,

Kolmogorov-Smirnoff and Levene tests, the

software InfoStat 2016 was also used.

RESULTS

Fertilization: The percentage of fertiliza-

tion was not significantly different between

temperature treatments (Mean 17 °C: 92.44 ±

3.71; Mean 12 °C: 88.24 ± 7.03) (ANOVA, F

1,5

= 0.28, P = 0.6252).

Embryonic development: At both tem-

perature treatments, a majority of normal

embryonic development was observed, with a

low occurrence of abnormal phenotypes. At the

highest temperature, a synchronized develop-

ment was observed (Fig. 2). This is particularly

noticeable at 6 and 12 h, where more than 97%

of the embryos were found to be at the same

stage of development. However, and in con-

trast, at the lowest temperature, there was a

major heterogeneity of embryonic development

at all times. This applied in particular between

3 and 48 hours, when the abundance of each

stage did not exceed 60% in any case. At the

same time, at 17 °C, the development of the

embryos was faster than at 12 °C (Fig. 2).

This difference in development time is evident

from the beginning of the embryonic devel-

opment and becomes more noticeable over

time. On the other hand, there was a progeny

effect which was more noticeable over time.

Progeny three showed a faster development at

both temperatures, and progeny two showed

the slower development. At 48 h in the 17 °C

treatment, most of the organisms in progeny 3

were in the larval stage, while in progeny 2 the

majority were at the blastula stage. In figure 2,

this effect can be observed as two predominant

columns and an increase in the standard error at

48 h in the 17 °C treatment. This heterogene-

ity is not observed within the same progeny;

however, it can be seen between the progeny of

different maternal origins. The GLM analysis

for embryonic development confirms these

observations. Table 1 presents the results of

Fig. 1. Measurements in the images of the larvae of A.

dufresnii. TL: Total length. M: Midline body length.

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the GLM analysis for embryonic development.

Even though there were three models with the

same AIC, the residuals analysis showed that

the most complex model, including the quadru-

pole interaction between the embryonic stage,

time (hours), seawater temperature and prog-

eny, was the best fit for the data. This indicates

that the embryonic stage is influenced by, all of

these factors.

Larval growth: A majority of normal

larval development was observed in both of

the temperature treatments showing a lower

occurrence of abnormal phenotypes with the 17

°C treatment. Larvae total length (TL) and the

midline body length (M) increased in both tem-

perature treatments over time but in a different

manner (Fig. 3). At 17 °C, larvae increased in

size more rapidly and the larvae were larger

than at 12 °C. After a rapid increase in length,

the larvae experienced a plateau and, then,

increased again at 17 °C. In contrast, at 12 °C

there was an initial increase but this increase

took place during a longer period of time, and

the plateau was also longer.

On the other hand, we also observed a

progeny effect in larval growth which became

more noticeable in TL over time. As seen in

figure 3, this effect can be observed especially

at 22 DPF as an increase in the standard error.

However, this heterogeneity occurs primarily

between progeny of different maternal origins.

The GLM analysis for larval growth confirms

these observations. Table 2 presents the results

of the GLM analysis for larval growth (TL and

M). The most complex model, which included

the triple interaction between the time (DPF),

seawater temperature and progeny, was the best

fit for the data, indicating that larval growth is

influenced by all of these factors.

DISCUSSION

There is a wide range of environmental

conditions inhabited by sea urchins and in

which their embryos and larvae must endure.

TABLE 1

Arbacia dufresnii. GLM analysis for embryonic development stages. In bold, the models with the best fit according to the

Akaike information criterion (AIC)

Model d.f. Akaike

1 Null 1 16 868.87

2 Stage 8 14 926.23

3 Time 9 16 884.86

4 Progeny 3 16 872.86

5 Temperature 3 16 872.86

6 Stage + Time 16 14 942.23

7 Stage + Progeny 10 14 930.23

8 Stage + Temperature 10 14 930.23

9 Stage x Time 72 4 064.65

10 Stage x Progeny 24 14 652.49

11 Stage x Temperature 24 14 652.49

12 Stage x Time + Stage x Progeny 88 3 790.91

13 Stage x Time + Stage x Temperature 88 3 790.91

14 Stage x Progeny + Stage x Temperature 24 14 652.49

15 Stage x Time x Progeny 216

3 557.67

16 Stage x Time x Temperature 216

3 557.67

17 Stage x Progeny x Temperature 24 14 652.49

18 Stage x Time+ Stage x Progeny + Stage x Temperature 88 3 790.91

19 Stage x Time x Progeny x Temperature 216

3 557.67

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Fig. 2. Arbacia dufresnii. Percentage of embryonic stages during the first 48 h at two different seawater temperatures. The

bars indicate mean ± standard error values (n = 3 progenies), at the two temperatures analyzed (12 and 17 °C).

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Early life stages are one of the most delicate

moments in the life cycle of any organism,

and temperature plays a fundamental role in

these stages (Byrne et al., 2009). Additionally,

there is strong evidence that the thermal accli-

matization of the parental females influences

the thermal tolerance of fertilization and the

development of their progeny (Fujisawa, 1995;

O’Connor & Mulley, 1977; Karelitz, Lamare,

Patel, Gemmel & Uthicke, 2020). However,

there is little knowledge regarding these exter-

nal factors in terms of the development of A.

dufresnii (Brogger, 2005; Catarino, De Ridder,

Gonzalez, Gallardo & Dubois, 2012).

The population of A. dufresnii inhabiting

the Nuevo Gulf starts to spawn in spring when

the seawater temperature is around 12 °C and

there is continuous spawning during the sum-

mer when the seawater temperature increases

to 17 °C (Epherra et al., 2015; Rivas et al.,

2016). In this way, spawned eggs experience

different seawater conditions in terms of the

timing of spawning. Our results show that at

both seawater temperatures the percentage of

fertilization registered was high and similar,

indicating that fertilization was not affected by

the analyzed temperatures. Other species of sea

urchins have been reported to exhibit a broad

tolerance to warming in egg fertilization (+6

°C above the ambient temperature) (Sewell &

Young, 1999; Byrne et al., 2009; Byrne, 2012).

The sperm:egg ratio is species-specific and can

Fig. 3. Larvae Growth. Larvae total length (TL) and Midline body length (M) (Mean ± SEM, n = 3 progenies) over time

(DPF) in 17 °C and 12 °C treatments.

TABLE 2

Arbacia dufresnii. GLM analysis for larval growth (Larvae total length TL, and Midline body length M) over time (DPF).

In bold, the models with the best fit according to the Akaike information criterion (AIC)

Model d.f. TL Akaike M Akaike

1 Null 1 6950.633 3035.320

2 Temperature 2 6750.147 2981.955

3 DPF 9 4519.118 2476.731

4 Progeny 4 6620.148 2887.862

5 Temperature + DPF 10 4096.245 2368.619

6 Progeny + DPF 12 3966.739 2279.837

7 Temperature + Progeny 5 6422.527 2834.999

8 Temperature * DPF 18 3743.943 2284.972

9 Progeny * DPF 35 3292.358 2123.422

10 Temperature * Progeny 8 6025.142 2776.841

11 DPF + Temperature + Progeny 13 3535.150 2166.551

12 DPF * Temperature * Progeny 66 2100.101 1885.455

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vary from 10: 1 to 1500: 1 for the same spe-

cies, depending on the experimental conditions

(Byrne et al., 2009; Ericson et al., 2012). The

sperm:egg ratio used (300:1) (Fernández et al.,

2019) did not affect the fertilization of eggs

even with a 5 °C thermal difference between

treatments. However, it is possible that with

a lower ratio, fertilization varies between the

temperatures analyzed.

An increase in seawater temperature is

usually related to an acceleration of develop-

ment and the growth rate in other sea urchin

larvae (O’Connor et al., 2007; Rahman, Rah-

man, & Uehara, 2007; Rahman, Tsuchiya, &

Uehara, 2009). Our results show that A. dufres-

nii developed more rapidly and synchronized

at 17 °C rather than at 12 °C. A rapid embry-

onic hatch allows for planktotrophic larvae

development and prompt feeding, increasing

the chance for survival. Due to the fact that

phytoplankton blooms are found in the spring

and summer at Nuevo Gulf (De Vido De Mat-

tio, 1980; Esteves, de Vido de Mattio, Cejas &

Frontali, 1981; Pastor & Bala, 1995), a rapid

development by the end of the summer may

ensure food supply for the larvae. However,

progeny is also important since produce a syn-

ergistic interaction. The fact that analyzing

these factors separately the AIC values were

the same, indicates that there is a strong mater-

nal influence on the progeny during embryonic

development. The females’ nutritional status

affects their gonadal development (Thompson,

1983; Lemire & Himmelman, 1996; Walker &

Lesser, 1998; Rubilar et al., 2016). Eggs from

females with a good nutritional status should

show a high quantity and quality of nutrients,

which will provide sufficient energy and other

nutrients until the organism can successfully

feed on their own (Byrne et al., 2008b). The

differences found during the embryonic devel-

opment according to progeny may be due to

differences in the nutritional status among

females in Nuevo Gulf where food is not abun-

dant (Epherra et al., 2015; Parra et al., 2015).

In this way, embryos of A. dufresnii are affect-

ed by endogenous (nutrients) and exogenous

(temperature) factors which interact simultane-

ously over time.

The sea urchin larvae growth rate is affect-

ed by several factors, such as salinity, pH,

solar radiation, seawater temperature and food

availability (Metaxas, 2013; Przeslawski et al.,

2015). The larvae of A. dufresnii grew faster

and larger at 17 °C than at 12 °C, suggesting

that development appears to be more efficient

at higher temperatures. The temperature may

increase survival as it implies a decrease in

the time spent at the water column where the

sea urchins are vulnerable to biotic and abiotic

stressors (Uthicke, Schaffelke & Byrne, 2009;

Hardy et al., 2014; Przesławski et al., 2015).

Because of this, some studies indicate that an

increase in seawater temperature can favor

the development of embryos and larvae in A.

lixula (Privitera et al., 2011; Wangensteen et

al., 2013; Gianguzza et al., 2014; Visconti et

al., 2017). Phytoplankton blooms in the Nuevo

Gulf during early spring are longer than in

late summer (Esteves et al., 1981; Esteves,

Santinelli, Sastre, Díaz & Rivas, 1992), gen-

erating longer periods of food availability for

A. dufresnii larvae in the spring than in the

late summer. However, at 12 °C larvae have

a longer period of development than at 17

°C. This may generate an increased survival

rate of larvae, due to food availability at low

temperatures and, due to the speed of develop-

ment at higher temperatures in Nuevo Gulf.

In A. lixula, discrepancies were found in the

optimal temperature for recruitment between

populations from different regions (Privitera et

al., 2011), probably indicating different strate-

gies to achieve metamorphosis, depending on

regional environmental factors, such as high

temperature or available food (Privitera et al.,

2011; Gianguzza, 2020). On the other hand, our

results show that in A. dufresnii there is a strong

progeny influence on larvae development. Both

temperature and progeny are important factors

and interact with each other, producing a syn-

ergistic effect. This indicates that other factors,

in addition to abiotic factors, are important to

larval survival and that endogenous factors also

play an important role.

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Unlike other sea urchins, Arbacia spe-

cies are found in tropical, temperate, and

subantarctic areas (Gianguzza, 2020). Some

studies indicate that A. lixula is a thermophilic

(heat-tolerant) species (Gianguzza et al., 2011;

Gianguzza et al., 2014; Pérez-Portela et al.

2019), and may develop normally in an ampli-

tude of 10 °C, with local differences depend-

ing on the thermal history prior to spawning

(Gianguzza, 2020). A. dufresnii also presents a

large distribution with different seawater tem-

peratures (ranging from 23 ºC to 4 ºC). Along

regions, the different populations show spatial

and temporal differences in their reproductive

cycle. This plasticity may be responsible for

its wide distribution and adaptation to different

environments. There is scarce data regarding

the thermal tolerance during the development

of A. dufresnii. However, numerous studies

have shown that for each species there is an

optimal temperature range for fertilization and

development, and that this thermal tolerance is

closely related to the thermal acclimatization

of the parental females (Karelitz et al., 2020).

This may explain the success in fertilizing eggs

but the failed larval development at 26-28 ºC as

regards A. dufresnii from Nuevo Gulf (Brogger,

2005). On the other hand, our results show

that within the optimal temperature range, the

higher temperature generates faster develop-

ment and larger larvae. However, there is still a

lack of data regarding other factors, impacting

the development of A. dufresnii and the pos-

sible interactions that can occur between such

factors. A clear example of one such interac-

tion is how changes in temperature, as well the

oceanic acidification expected to take place in

the next decades, will affect the distribution of

this species.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are fully

and clearly stated in the acknowledgements

section. A signed document has been filed in

the journal archives.

ACKNOWLEDGMENTS

We are grateful to the diver Ricardo Bebo

Vera for the collection of the sea urchins, to

Mariano Moris for helping with the experi-

ments and to Kathleen C. Anderson for the

revision of the English. This work was under-

taken with funds from PIP 0352/14, PICT

2018-1729. The sea urchins were collected by

the Provincial Permit N°586/18.

RESUMEN

El desarrollo embrionario y larvario está condicionado

por la temperatura del agua y el origen materno

de los huevos en el erizo de mar Arbacia dufresnii

(Echinodermata: Echinoidea)

Introducción: El desarrollo embrionario y larvario

de los erizos de mar depende en gran medida del estado

nutricional materno y de las condiciones ambientales del

agua de mar. Objetivo: Comparar el desarrollo de Arba-

cia dufresnii en dos temperaturas de agua diferentes y en

progenies con diferentes orígenes maternos. Métodos:

indujimos a las hembras y machos de A. dufresnii del

Golfo Nuevo a desovar, recolectamos los huevos de cada

hembra individualmente (progenie), los separamos en dos

temperaturas de agua de mar (12 y 17 ° C) y los fertiliza-

mos. Registramos el porcentaje de óvulos fecundados y

el porcentaje de embriones por etapa de desarrollo según

tiempo, temperatura y descendencia. Medimos el creci-

miento larvario según la longitud total (TL) y la longitud

corporal de la línea media (M) de acuerdo con el tiempo en

días post fecundación, la temperatura y la progenie. Resul-

tados: La temperatura no afectó la fertilización, pero el

desarrollo del embrión fue más rápido y más sincronizado

en el tratamiento de alta temperatura. Los modelos lineales

generalizados indican que el desarrollo del embrión depen-

de una interacción cuádruple entre el estadio embrionario,

el tiempo (h), la temperatura del agua de mar y la progenie.

El crecimiento larvario fue más rápido, produciendo larvas

más grandes a la temperatura más alta. El crecimiento de

las larvas depende de una triple interacción entre el tiem-

po (DPF), la temperatura del agua de mar y la progenie.

Conclusiones: Encontramos un impacto en la tempera-

tura y en la progenie durante el desarrollo embrionario y

larvario y, en ambos casos, estos factores generaron un

efecto sinérgico sobre el tiempo de desarrollo y el tamaño

de las larvas. Esto probablemente proporciona una ventaja

de supervivencia, ya que una velocidad de desarrollo más

rápida implica una disminución en el tiempo que pasan en

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la columna de agua, donde los erizos de mar son vulnera-

bles a los factores estresantes bióticos y abióticos.

Palabras clave: Equinodermos; reproducción; aprovisio-

namiento parental; efecto térmico; estadios tempranos del

desarrollo; crecimiento larval.

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