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Journal of Thermal Biology 30 (2005) 618–622

www.elsevier.com/locate/jtherbio

Effect of salinity and temperature on thermal toleranceof brown shrimp Farfantepenaeus aztecus (Ives)

(Crustacea, Penaeidae)

Ana Denisse Rea, Fernando Diaza,�, Elizabeth Sierraa,Juan Rodrıguezb, Estela Perezb

aLaboratorio de Ecofisiologıa de Organismos Acuaticos, Departamento de Biotecnologıa Marina, Centro de Investigacion Cientıfica y de

Educacion Superior de Ensenada. (CICESE), Km. 107 Carretera Tijuana-Ensenada, Ensenada BC, MexicobLaboratorio Acuario, Departamento de Biologıa, Facultad de Ciencias, Universidad Nacional Autonoma de Mexico. (UNAM),

Mexico DF 04510, Mexico

Received 5 May 2005; accepted 7 September 2005

Abstract

The critical thermal maxima (CTMax) of Farfantepenaeus aztecus was not affected significantly by salinity (P40:05).A direct relationship was obtained between the critical temperature and the acclimation temperature which increased at

intervals of 3–5 1C.

The end point of CTMax in F. aztecus was loss of righting response (LRR).

The acclimation response ratio (ARR) for the juveniles of the brown shrimp ranged between 0.20 and 0.80, which

agreed with others obtained for crustaceans from tropical and subtropical climates.

The brown shrimp should not be exposed to conditions that cause total disorientation; if this is avoided, it will permit

an increase in growth and reduce mortalities in culture populations.

r 2005 Elsevier Ltd. All rights reserved.

Keywords: Critical thermal maxima; Salinity; Temperature; Acclimation response ratio; Farfantepenaeus aztecus

1. Introduction

The aquatic environment is thermally heterogeneous

in space and time. Animals living in changing environ-

ments possess physiological and behavioral mechanisms

allowing them to live successfully, at least within certain

e front matter r 2005 Elsevier Ltd. All rights reserve

erbio.2005.09.004

ing author at: Laboratorio de Ecofisiologıa de

uaticos, Departamento de Biotecnologıa Mar-

nvestigacion Cientıfica y de Educacion Superior

CICESE), P.O. Box 434844, San Diego, CA

A. Fax: 52 (646) 175 05 69.

ess: fdiaz@cicese.mx (F. Diaz).

limits. They also have the capacity of resisting extreme

temperatures for limited periods, which constitute an

expansion of their environmental space (Hutchison and

Maness, 1979).

Many species of commercial importance live in

lagoon–estuarine habitats that sustain the main fisheries

of the continental platform. Among these, the penaeid

shrimps are a source of commercial importance (Ven-

kataramiah et al., 1974; Yanez-Arancibia, 1986).

The penaeid shrimps mature and reproduce in the

open sea, the postlarva stages penetrate to the lagoon–

estuarine systems where growth occurs until they

become juveniles and preadults (Williams, 1960). In

d.

ARTICLE IN PRESSA.D. Re et al. / Journal of Thermal Biology 30 (2005) 618–622 619

these environments the organisms are exposed to daily

and seasonal fluctuations of diverse environmental

factors, especially salinity and temperature. Shrimps

respond to these variations as a highly integrated unit,

tolerating those environmental changes (Vernberg and

Vernberg, 1972; Venkataramiah et al., 1974; Prosser,

1991).

Salinity and temperature modify the physiological

responses of aquatic organisms; these factors in the

lagoon–estuarine ecosystems determine distribution and

survival. Salinity is a masking factor that modifies

numerous physiological responses such as metabolism,

growth, life of cycle, nutrition and intra-and inter-

specific relationships (Kinne, 1971; Fry, 1971; Venka-

taramiah et al., 1974).

Temperature is a direct and controlling factor of the

aquatic organism’s activity and, therefore mobile species

including the crustaceans show different behavioral

responses which include the selection of a thermal

habitat and avoidance of lethal temperatures (Reynolds,

1979; Giattina and Garton, 1982).

All life cycle stages must be considered to respond to

thermal acclimation that results in physiological com-

pensatory temperature responses and adaptative resis-

tance changes allowing a thermal niche expansion.

Temperature can be a limiting factor in the distribution

of an aquatic organism if they are exposed to the

resistance zone represented by the critical thermal

minima and maxima (Dıaz Herrera et al., 1998).

The critical thermal maxima is a characteristic

modified by acclimation temperature and therefore,

useful in evaluating the thermal requirements of an

organism’s physiological status (Becker and Genoway,

1979; Paladino et al., 1980; Lutterschmidt and Hutch-

ison, 1997).

The critical thermal maxima (CTMax) was defined by

Cowles and Bogert (1944), modified by Lowe and Vance

(1955) and standardized by Hutchison (1961). Cox

(1974) defined CTMax as follows: ‘‘these tolerance

measurements as the arithmetic mean of the collective

thermal points at which locomotory activity becomes

disorganized’’. This is when the animal loses its ability to

escape from conditions that will promptly lead to its

death. When heated from a previous acclimation

temperature at a constant rate just fast enough to allow

deep body temperatures to follow environmental tem-

peratures without a significant time lag.

The knowledge of the CTMax provides a relevant

physiological and ecological index; the brown shrimp in

lagoon–estuarine systems may encounter such tempera-

tures either daily and seasonally. CTMax may occur at

different temperatures in different species, but the

physiological responses are same across a diversity of

taxa (Lutterschmidt and Hutchison, 1997). For these

reasons critical thermal maxima is an excellent index for

evaluating the thermal requirements and physiology of

aquatic organisms (Becker and Genoway, 1979; Paladi-

no et al., 1980).

According to Claussen (1977), ARR is defined as

DCTMax/DT or change in the CTMax per change in

acclimation temperatures. It can be considered as a

reliable measure to denote the physiological response of

aquatic organisms to a given change in temperature.

It is important to evaluate the interactions of two or

more variables on the functional responses of the

aquatic organisms if these variables interact, since these

studies provide information about the adaptative and

physiological potentialities of the organisms exposed to

different environmental factors. In the Gulf of Mexico

three endemic species of shrimps, Farfantepenaeus

aztecus, Litopenaeus setiferus and Farfantepenaeus duor-

arum, are distributed. These species have potential for

culture; however, basic physiological studies are neces-

sary to implement the culture of these species are few.

The goal of this study was to determine the critical

thermal limits and their Acclimation Response Ratio

(ARR) of juveniles of brown shrimp F. aztecus exposed

to different combinations of temperature and salinity to

assess the ability of organisms to adapt to different

thermal and salinity regimens in a tropical area of Gulf

of Mexico.

2. Materials and methods

Juveniles of F. aztecus (n ¼ 400) were recollected in

the Northern part of the Lagoon of Tamiahua,

Veracruz, the water temperature was 25 1C and salinity

was in the a range of 25–30%. The shrimps were

transported to the laboratory in plastic bags with water

from the lagoon and a saturated atmosphere of oxygen.

The organisms were placed in a 3000 l reservoir,

provided with a biological filter at 25 1C and salinity

of 30%, for 1 week to diminish the stress caused by

transport.

From the original stock 320 juveniles were selected

(4.5–8.5 g weight wet), and placed in 15 reservoirs of 120

liters provided with a biological filter and constant

aeration. The experimental salinities were 10, 15, 20, 25

and 3071%, which were made by diluting filtered sea

water with tap water, the rate of decreased of salinity

was 2% daily until we obtained experimental salinities.

The experimental temperatures were 20, 25 and

3071 1C, which were maintained by 500W heaters

connected to temperature regulator provided with a

thermocouple, the increased and decreased rate of

temperature was 2 1C per day. Once salinities and

experimental temperatures were reached, juveniles re-

mained in those conditions for 21 days. The photoperiod

was maintained in 12 h light/12 h dark.

The organisms were fed daily with two rations at 10%

of weight wet with commercial food (Camaronina

ARTICLE IN PRESSA.D. Re et al. / Journal of Thermal Biology 30 (2005) 618–622620

Purina) with 35% of protein. The food remainder, feces

and molts were extracted daily from the reservoirs by

siphoning.

The CTMax of 320 juveniles of brown shrimp from

different combinations of salinity and temperature as

determined. Each shrimp was placed in a 1-l glass flask

provided with constant aeration, the experimental

salinity at which the organisms were acclimated, and

then they were introduced into 40 l aquarium provided

with 1000W immersion heater and permanent aeration

to maintain a uniform temperature. The water was

maintained at the experimental temperature for 30min

to reduce the stress produced by handling Perez et al.

(2003), determinations of CTMax were done between

9:00 and 14:00 h. The heating rate used was 1 1Cmin�1

(Lutterschmidt and Hutchison, 1997). The end point for

CTMax was Loss of Righting Response (LRR) when the

shrimp was on its back and could not recover its upright

posture, or remains reclined at 901 (Nelson and Hooper,

1982). When the shrimps reached this point they were

returned to their acclimation salinity and temperature

conditions. The organisms were used only once and the

data for the animals which did not recover after

returning them to their acclimation salinity and tem-

perature after LRR were discarded.

In the brown shrimp, we determined ARR defined by

Claussen (1977) as DCTMax/DT or the change in the

CTMax per degree change in acclimation temperature.

A two-way analysis of variance was used as previous

determination of the normality and homoscedasticity of

the data (Sigma Stat Version 3.1) to determine the effect

of salinity and temperature on the thermal tolerance of

the brown shrimp.

3. Results and discussion

The critical thermal maxima of the shrimps were not

changed when salinity was increased from 10 to 30%,

but when acclimation temperature was increased from

Table 1

Critical thermal maxima (CTMax) of juveniles of brown shrimp

temperatures expressed to the nearest degree

Temperature (1C) Salinities (%)

10 15

20 38 37

(37.8–38.3) (36.5–37.5)

25 39 39

(38.5–39.5) (38.8–39.2)

30 41 42

(40.7–41.3) (41.8–42.2)

The underline between groups indicates a similar effect to the salinit

parenthesis.

20 to 30 1C the thermal tolerance of juveniles was

increased by 3–5 1C (Table 1). An analysis of variance

indicated that the temperature had a significant effect

(Po0:05) on the CTMax but the effect of salinity and

the interaction temperature-salinity was not significant

(P40:05). Becker and Genoway (1979), Paladino et al.

(1980), and Beitinger et al. (2000) mention that the

critical thermal maxima is considered as a measure of

thermal tolerance of the aquatic organisms and is

determined by raising the temperature progressively

from the acclimation temperature until LRR, occurs in

response to the thermal stressor. We considered the end

point of CTMax in brown shrimp as LRR, the pre-death

thermal point at which locomotory movements become

disorganized due to neuromuscular blockade and pre-

synaptic failure, and shrimps lose the ability to escape

the conditions which may ultimately lead to death

(White, 1983; Beitinger et al., 2000).

In other species of crustaceans as Palaemonetes

kadiakensis, Procambarus clarkii, Macrobrachium tenel-

lum, M. rosenbergii and M. acanthurus (Nelson and

Hooper, 1982; Dıaz et al., 1994; Hernandez et al., 1996;

Dıaz Herrera et al., 1998; Dıaz et al., 2002) reported a

direct relationship between the CTMax and acclimation

temperature as obtained in F. aztecus. Paladino et al.

(1980) emphasized the importance of determining the

CTMax in aquacultural practices with aquatic organ-

isms since it is an indicator of the thermal tolerance of

brown shrimp and it allows the identification of the

temperature at which the first sign of stress occurs.

Salinity did not cause a significant effect on thermal

tolerance of brown shrimp, similar results were obtained

for Criales and Chung (1980) in juveniles of pink shrimp

(Farfantepenaeus brasiliensis), and both shrimp species

are characterized by a wide tolerance to salinity.

Hernandez and Dıaz (1995) obtained an osmoregulation

pattern for F. aztecus from Tamiahua, Veracruz when

exposed to different combinations of salinity and

temperature, and had a hypo-osmoregulation capacity

higher salinities and hyper-osmoregulation in lower

Farfantepenaeus aztecus acclimated to different salinities and

20 25 30

38 38 39

(37.6–38.4) (37.1–38.9) (38.5–39.5)

40 40 38

(39.4–40.6) (39.3–40.7) (37.8–38.2)

42 42 42

(41.5–42.5) (41.6–42.4) (41.3–42.7)

y (P40:05). Median values and confidence intervals (95%) in

ARTICLE IN PRESSA.D. Re et al. / Journal of Thermal Biology 30 (2005) 618–622 621

salinity. Therefore, they can be characterized as strong

osmoregulators, because they adapt rapidly to the new

salinities by increasing and decreasing hemolymph

osmotic concentration.

We calculated the ARR, according to Claussen (1977)

as a convenient index of thermal acclimation, the values

of CTMax of F. aztecus exposed to different combina-

tions of salinity and temperature was 0.3, 0.5, 0.4, 0.45,

and 0.3 for the five salinity groups. In different

crustaceans from cold waters such as Orconectes

rusticus, Claussen (1980) obtained a value of 0.24 and

in O. virilis of 0.15, Layne et al. (1987) reported ARR in

O. rusticus values between 0.23 and 0.25. McLesse

(1956) in postlarvae of the lobster (Homarus americanus)

obtained an ARR of 0.24. In Procambarus clarkii, a

crayfish that is distributed in temperate-warm areas, the

calculated ARR was 0.33 (Dıaz et al., 1994). In

Macrobrachium tenellum a subtropical species the

ARR calculated was 0.54 (Hernandez et al., 1996).

ARR range for postlarvae of M. rosenbergii a tropical

species was 0.45–0.63 for juveniles 0.45–0.55 (Dıaz

Herrera et al., 1998). In M. acanthurus a subtropical

prawn, the values obtained by Dıaz et al. (2002) for

ARR was of 0.33–0.52.

For different species of crustaceans the presented data

for ARR suggest that subtropical and tropical species

have higher ARR. Perez et al. (2004) reported similar

tendency in different species of fish of different habitats.

This response is typical of aquatic poikilotherms. The

species that inhabit temperate and cold regions experi-

encing gradual long-term temperature fluctuations

would have the time necessary to make metabolic

adjustments that would result in nonsubstantial shifts

in tolerance ranges. On the contrary, subtropical and

tropical species that experience their greatest thermal

extremes over short periods should have broad ranges of

tolerance to survive the relatively rapid changes in water

temperature, without time for acclimation, to adjust

their tolerance (Johnson and Kelsch, 1998). However, it

should be considered that higher ARR values may be

found in species living in (or reproducing in) estuarine

conditions.

Knowledge about the thermal requirements in a

commercial species such as brown shrimp is useful in

allowing the determination of the selection of places for

intensive aquaculture, and permits growth and low

mortality.

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