PRIMARY RESEARCH PAPER

Hot and salty: the temperature and salinity preferencesof a temperate estuarine shrimp larva, Upogebia pusilla(Decapoda: Thalassinidea)

Filipa Faleiro • Jose Paula • Luıs Narciso

Received: 10 April 2011 / Revised: 19 January 2012 / Accepted: 26 February 2012 / Published online: 13 March 2012

� Springer Science+Business Media B.V. 2012

Abstract At a time when global climate changes are

forcing life to adapt to a warming and salinity-

changing environment, it is essential to understand

how future changes in ocean chemistry will affect

species. This study evaluates the combined effects of

temperature and salinity on survival and development

of Upogebia pusilla larvae. Combinations were made

from three temperatures (18, 23, and 28�C) and three

salinities (15, 25, and 35). Survival, larval duration

and megalopa size were compared between treat-

ments. U. pusilla larvae developed optimally in the

highest salinity (35) and higher temperatures

(23–28�C). Low salinities and temperatures did not

support larval survival and development, with salinity

being the main restricting factor for survival, while

temperature affected mainly the duration of the larval

stages. Larvae at higher temperatures (23–28�C)

presented a higher development rate but no differences

were found in megalopa size.

Keywords Upogebia pusilla � Thalassinid larvae �Salinity � Temperature � Survival � Growth

Introduction

Estuarine species have to face a wide range of

environmental conditions. Temperature and salinity

are among the most important environmental factors

that affect estuarine organisms, including their sur-

vival, growth, development, reproduction, feeding,

and activity. Their capacity to survive in such an

unstable environment relies on their tolerance toward

environmental fluctuations but also on life strategies to

avoid unsuitable conditions, particularly at early

ontogenic stages. Although some species may have a

wide tolerance range and present larval retention

inside the estuary (e.g. Antonopoulou & Emson, 1989;

Paula, 1993; Munro et al., 1994; Numaguchi, 1998;

Verween et al., 2007), many species have to avoid the

changing estuarine environment at an early stage by

exporting the newly hatched larvae to neritic areas,

undergoing most development in seawater and return-

ing to the estuary at the less vulnerable megalopal

stage (e.g., Nagaraj, 1992, 1993; Paula et al., 2001,

2003).

Besides the regular environmental fluctuations all

through the day and seasons, estuarine organisms will

also have to adapt to future changes in ocean

chemistry. Global climate changes are predicted to

occur in the future through increases in temperature,

water acidification, and changes in seawater salinity.

Mean global temperature has increased by about 0.7�C

in the last century, and further increases of about 1.8 to

4.0�C are expected by the end of this century

Handling editor: Darcy J. Lonsdale

F. Faleiro (&) � J. Paula � L. Narciso

Universidade de Lisboa, Faculdade de Ciencias, Centro de

Oceanografia, Laboratorio Marıtimo da Guia, Avenida

Nossa Senhora do Cabo 939, 2750-374 Cascais, Portugal

e-mail: filipafaleiro@gmail.com

123

Hydrobiologia (2012) 691:89–95

DOI 10.1007/s10750-012-1060-x

(Solomon et al., 2007). Global warming is affecting

the hydrological cycle (e.g., precipitation, evapora-

tion, river runoff, and ice melt) and leading to large-

scale changes in ocean salinity. From the 1960s to the

1990s, the subtropical waters have increased in

salinity, while the high-latitude regions have fresh-

ened. In addition to these meridional changes, the

Atlantic is becoming saltier over much of the water

column (Solomon et al., 2007). Climate change can

thus pose great risks for aquatic ecosystems, particu-

larly for estuarine and marine coastal areas. The

evaluation of the combined effects of temperature and

salinity changes on biological responses of marine and

estuarine organisms is therefore essential, as deviation

from the optimum values may result in deleterious

consequences for their physiological performance.

Upogebia pusilla is a burrowing thalassinid shrimp

that can be found in mudflats in marine and estuarine

environments, all through the eastern Atlantic region

from Bretagne to Mauritania, and also in the Medi-

terranean and Black Sea (Holthuis, 1991). Even

though their presence may go unnoticed, thalassinid

shrimps play an important role in benthic ecology,

namely in benthic communities structure (e.g., Berke-

nbusch et al., 2000), sediment bioturbation (e.g.,

Berkenbusch & Rowden, 1999), nutrient cycling (e.g.,

Kinoshita et al., 2003) and pollutants redistribution

(e.g., Whitehead et al., 1988). The decline of U. pusilla

populations due to eutrophication (e.g., Todorova &

Konsulova, 2000) and commercialization as live bait

is thus raising conservational and ecological concerns.

This study intends to identify the tolerance limits and

optimal conditions of temperature and salinity during

development of U. pusilla larvae. Results will help to

understand how temperature and salinity fluctuations

will affect larval development, a main concern at a

time when global climate changes are forcing life to

adapt to a warming and salinity-changing

environment.

Materials and methods

Experimental methodology

Wild ovigerous females were collected at Ria Formosa

lagoon, south Portugal, in September 2008. Data on

the temperature and salinity regimes of the Ria

Formosa indicate that temperature fluctuates between

16.4 and 19.0�C in the winter and between 18.8 and

28.4�C in the summer (when larvae hatching occurs),

while salinity generally oscillates around 35 (Newton

& Mudge, 2003).

Ovigerous females were transported to the labora-

tory and kept in a recirculating rearing system, in

separated incubation tanks with individual larval col-

lectors. Husbandry conditions reproduced the summer

conditions in nature: photoperiod 14 L:10 D, salinity

34–35, water temperature 23–24�C, and pH 8.2–8.3.

Newly hatched larvae (total length of 1.86 ±

0.06 mm) were reared in transparent plastic boxes with

10 compartments (3.0 9 3.0 9 2.0 cm and 15 ml each).

The experiment followed a factorial design and combi-

nations were made from three temperatures (18, 23, and

28�C) and three salinities (15, 25, and 35). For each

combination, ten larvae from the same brood were

chosen among the most active and placed individually in

the rearing compartments. Three replicate boxes with

larvae from three different females were obtained for

each combination (N = 30). Larvae were acclimatized to

the required experimental conditions through salinity and

temperature adjustments of 3 and 2�C per hour, respec-

tively. The experimental set up was covered to prevent

evaporation and, consequently, salinity increase. Water

baths were used to maintain temperatures constant.

Larvae were fed on Brachionus plicatilis

(32 prey ml-1), as rotifers proved to be adequate for

feeding U. pusilla zoeal stages (Faleiro & Narciso,

2009). Rotifers were replaced and larvae were trans-

ferred to new media every day to assure good water

quality.

Larvae survival and the development stage (see dos

Santos & Paula, 2003) were analyzed daily, until the

megalopal stage was reached. Megalopae were mea-

sured (to the nearest 0.02 mm) under a stereomicro-

scope with a calibrated micrometer eyepiece. Total

length (TL) and carapace length (CL) were measured

in dorsal view from the top of the eyes to the tip of the

telson and to the posterior margin of the carapace,

respectively.

Statistical analysis

A survival analysis was used to compare survival

curves between treatments. The multiple-sample test

used was an extension of Gehan’s generalized Wilco-

xon test, Peto and Peto’s generalized Wilcoxon test,

and the log-rank test.

90 Hydrobiologia (2012) 691:89–95

123

The combined effects of temperature and salinity

on the survival of each zoeal stage were examined

using multiple regression analysis. Larval survival

was arcsine transformed. The model included linear

and quadratic terms of both independent variables and

an interaction term (product of the variables). Partial

tests of significance were used for each component of

the regression model to verify if a particular compo-

nent significantly improved the fit when other vari-

ables were included in the model.

Megalopa survival, size, and larval duration were

compared between treatments using Anova and a pos-

teriori tests (Tukey HSD and Unequal N HSD). Larval

duration was analyzed based on the cumulative

number of days necessary to zoea I metamorphose to

zoea II, zoea III, zoea IV, and megalopa stages. The

combined effects of temperature and salinity on

megalopa survival and zoea I duration were analyzed

through factorial Anova. A one-way Anova was used

to evaluate the effect of temperature on megalopa size

and duration of zoea II, III, and IV stages only for

salinity 35, since almost no larvae survived at

salinities 15 and 25.

To evaluate the overall tolerance of each zoeal stage

to all experimental combinations, survival was deter-

mined for each stage and compared between stages

using a one-way Anova and the Tukey HSD test.

All statistical analyses were performed for a

significance level of 0.05, using Statistica 9.0 software

(StatSoft Inc.).

Results

Larvae reared at different temperature and salinity

combinations had different survival rates (v2 = 97.8,

P = 0.000) (Figs. 1, 2). No larvae reached the megal-

opa stage at salinities 15 and 25. At salinity 35, the

proportion of megalopae at 18, 23, and 28�C was 3.3,

16.7, and 20.0%, respectively. Temperature, salinity,

and the interaction factor had a significant effect on the

proportion of megalopae obtained (FT = 4.2, PT =

0.032; FS = 28.8, PS = 0.000; FTS = 4.2, PTS =

0.014), with higher proportions achieved for the

T23S35 and T28S35 combinations.

The regression analysis demonstrated that survival

was significantly influenced by temperature and

salinity (F \ 42.3, P \ 0.001), with regression mod-

els for each development stage explaining between

81.2 and 91.0% of the variance shown by the data

(Fig. 3; Table 1). The tolerance to culture conditions

varied between development stages (Fig. 4), with zoea

I presenting a higher survival rate than zoea II, III, and

IV (F = 10.4, P = 0.000).

Larval duration was not affected by salinity

(F = 0.4, P = 0.531). Temperature affected the dura-

tion of zoea I (F = 165.2, P = 0.000), zoea II

(F = 41.5, P = 0.000), and zoea III (F = 10.7, P =

0.001), but not of zoea IV (F = 1.6, P = 0.265), with

shorter development periods observed at higher tem-

peratures (Fig. 5).

In what concerns megalopa size, no differences

were found between treatments, neither in total length

(F = 1.4, P = 0.305), nor in carapace length (F =

0.5, P = 0.622). Megalopae presented an average TL

of 2.86 ± 0.17 mm (X ± SE) and an average CL of

1.17 ± 0.03 mm (X ± SE).

Discussion

In variable water environments such as estuaries, some

species are extremely resistant to environmental

fluctuations and able to survive in the estuarine

environment, even during early ontogeny. Other

species, however, are not so tolerant and need to

adopt life cycle strategies to avoid estuarine environ-

mental stress and high-predation pressure, particularly

in early stages. This seems to be the case of U. pusilla.

Low salinities and temperatures did not support larval

survival and development. Salinity was the limiting

factor for survival, while temperature affected mainly

0 5 10 15 20 25 30

Time (days)

0.0

0.2

0.4

0.6

0.8

1.0

Cum

ulat

ive

Pro

port

ion

Surv

ivin

g

T18

S15

T18

S25

T18S35

T23

S15

T23

S25

T23S35

T28

S15

T28

S25

T28S35

Fig. 1 Survival curves for larvae reared under different

temperature and salinity combinations

Hydrobiologia (2012) 691:89–95 91

123

the development time. Larvae had a higher tolerance

to temperature changes (optimal temperature ranging

from 23 to 28�C) than to salinity fluctuations (optimal

salinity around 35).

Estuarine species that have a narrow tolerance

range and reach optimal development near seawater

salinity generally present a larval exportation strategy,

with newly hatched larvae migrating rapidly to neritic

areas, thus avoiding the changing estuarine environ-

ment at an early stage (e.g., Nagaraj, 1992, 1993;

Paula et al., 2001, 2003). Maximum survival of U.

pusilla larvae at salinity 35 clearly suggests a larval

exportation strategy for this species, which is sup-

ported by the presence of zoea I in the terminal section

of the estuary (Paula, 1993). Indeed, an exportation

strategy toward the adjacent coastal waters seems to be

a common characteristic of the life cycle of thalassinid

shrimps. Although thalassinids are euryhalines when

adults and present a high tolerance to salinity fluctu-

ations (e.g., Day, 1951; Thompson & Pritchard, 1969;

Hornig et al., 1989), larval survival and development

are improved at higher salinities (e.g., Forbes, 1973;

Thessalou-Legaki, 1990; Paula et al., 2001).

In general, temperature is not as restrictive as

salinity. Within a tolerated range, temperature mostly

affects the duration of larval stages. Development is

faster at higher temperatures; the difference between

species is in their optimal thermal range. U. pusilla

proved to be physiologically well adapted to survive

wide fluctuations in water temperature. Larval devel-

opment was optimized at higher temperatures,

between 23 and 28�C. The reduced survival at 18�C

seems to suggest that this temperature is outside the

optimal range for this species. Optimal larval devel-

opment at higher temperatures may be an adaptation to

summer conditions, when larval development takes

place. A faster development may increase the chance

of survival during planktonic stage, since larvae are

exposed for a shorter period to potentially harmful

factors such as physical stress, food limitation, and

pelagic predation (Morgan, 1995). Moreover, shorter

molting periods may reduce molting asynchronism,

Fig. 2 Succession of developmental stages for the different temperature and salinity combinations (I zoea I; II zoea II; III zoea III; IVzoea IV; M megalopa)

92 Hydrobiologia (2012) 691:89–95

123

size variation and, consequently, cannibalism (Quini-

tio et al., 2001; Hamasaki, 2003).

Nevertheless, when temperature increases above

the tolerance range of the species, survival, and

development may be compromised. Several studies

with decapods have shown that higher development

rates at elevated temperatures may result in smaller

larvae (e.g., Shirley et al., 1987; Smith et al., 2002),

with lower survival and growth rates (e.g., Kunisch &

Anger, 1984; Lovrich & Vinuesa, 1995). Moreover,

high temperatures have shown to increase the inci-

dence of malformations during fish development (e.g.,

Ottesen & Bolla, 1998). These facts may be in part

related to the conservation of some essential nutrients.

Smith et al. (2002) demonstrated that for some

essential nutrients, such as ascorbic acid and polyun-

saturated fatty acids, a positive correlation exists

between nutrient conservation and low incubation

temperature. Moreover, supraoptimal temperatures

result in increased membrane fluidity and loss in

membrane function (Pruitt, 1990).

Besides the straight effects of temperature and

salinity on larval survival and development, there is

also an important interaction effect between these

two factors. At higher temperatures, U. pusilla

larvae were more tolerant to salinity fluctuations.

A salinity effect on temperature tolerance has also

been reported for several aquatic invertebrates living

in habitats with strongly fluctuating temperature and

salinity conditions. Some species can tolerate sub-

normal temperatures at the lower end of their

salinity range and supranormal temperatures at the

upper end of their salinity range (e.g., Kinne, 1970).

In contrast, other species of invertebrates (e.g.,

mussels) have shown greater tolerance of suboptimal

temperatures at the upper end of the salinity range

and vice versa (e.g., Wright et al., 1996; Verween

et al., 2007).

In conclusion, U. pusilla larvae evidenced low

tolerance to brackish waters and optimal development

at high temperatures. These preferences may be an

advantage under the actual global warming scenario,

given the rising temperature of oceans and the

increased salinity of the Atlantic (Solomon et al.,

2007). Nevertheless, further studies will be important

to evaluate the potential effects of global warming on

the physiological performance of U. pusilla. Given the

important role of thalassinid shrimps in benthic

ecology, temperature and salinity changes will directly

Zoe

a I

18 19 20 21 22 23 24 25 26 27 2815

17

19

21

23

25

27

29

31

33

35Sa

lini

ty

0.8

0.6

0.4

0.2

Zoe

a II

18 19 20 21 22 23 24 25 26 27 2815

17

19

21

23

25

27

29

31

33

35

Salin

ity

0.2

0.4

0.6

Zoe

a II

I

18 19 20 21 22 23 24 25 26 27 2815

17

19

21

23

25

27

29

31

33

35

Sali

nity

0.1

0.2

Zoe

a IV

18 19 20 21 22 23 24 25 26 27 28

Temperature (ºC)

15

17

19

21

23

25

27

29

31

33

35

Sali

nity

0.1

Fig. 3 Response surface plots for survival of each development

stage at different temperature and salinity conditions

Hydrobiologia (2012) 691:89–95 93

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influence species recruitment, but will have also an

indirect effect on the physic-chemical environment

and community structure.

Acknowledgments The authors would like to thank Fundacao

para a Ciencia e a Tecnologia for providing financial support.

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Table 1 Multiple regression models and associated statistics for survival of each development stage (%S survival; S salinity;

T temperature)

R2 F P Regression equation PT PS PT2 PS2 PTS

Zoea I 0.908 41.274 0.000 %SI = -2.605 - 0.395 T ? 3.589 S ? 0.471

T2-2.875 S2 ? 0.168 TS

0.718 0.000 0.661 0.000 0.700

Zoea II 0.910 42.329 0.000 %SII = 4.506 - 3.010 T - 3.260 S ? 2.503

T2 ? 2.394 S2 ? 1.893 TS

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T2 ? 3.711 S2 ? 1.481 TS

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Zoea IV 0.825 19.761 0.000 %SIV = 0.421 ? 1.098 T - 4.528 S - 1.788

T2 ? 3.532 S2 ? 1.982 TS

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IV)

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Temperature (ºC)

0

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atio

n (d

ays)

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Fig. 5 Duration of larval stages at different temperatures

(Mean; Mean ± SD; Mean ± 1.96 SD)

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