Journal of Thermal Biology 28 (2003) 531–537

ARTICLE IN PRESS

*Correspond

ture, Marine B

92143-4844, US

E-mail addr

0306-4565/$ - se

doi:10.1016/S03

Thermoregulatory behavior and critical thermal limitsof the angelfish Pterophyllum scalare (Lichtenstein)

(Pisces: Cichlidae)

Estela P!ereza, Fernando D!ıazb,*, Sonia Espinac

aLaboratorio Acuario, Departamento de Biolog!ıa, Facultad de Ciencias, Universidad Nacional Aut !onoma de M!exico (UNAM), Mexico,

D.F. 04510, MexicobDepartamento de Acuicultura, Biotecnolog!ıa Marina, Centro de Investigaci !on Cient!ıfica y Educaci !on Superior de Ensenada (CICESE),

Km. 107, Carretera Tijuana-Ensenada, 22830, Ensenada, B.C., MexicocLaboratorio de Ecofisiolog!ıa, Facultad de Ciencias, Departamento de Biolog!ıa, Universidad Nacional Aut !onoma de M!exico (UNAM)

Mexico, D.F., 04510. Mexico

Received 14 March 2003; accepted 9 July 2003

Abstract

(1)

Final temperature preferendum of juvenile (0.9–1.9 g) and adult (5.2–12.5 g) angelfish Pterophyllum scalare were

determined with acute and gravitation methods. The final preferenda were similar, independent of the method and

development stage (29.0–31.1�C).

(2)

The critical thermal maxima (CTMax) for juveniles were 36.9�C, 37.6�C, 40.6�C, 40.8�C and for adults 38.4�C,

38.6�C, 41.0�C, 42.1�C. Adult angelfish CTMax was slightly higher than in juveniles (1�C; Po0:05); the endpoint

of CTMax was the onset of spasms.

(3)

The acclimation response ratio for both stages had an interval of 0.33–0.44; these values are in agreement with

results for subtropical and tropical fishes.

(4)

Therefore it is recommended that angelfish cultivation should be consistent with temperatures that do not change

abruptly throughout the year and temperature maximum does not exceed 30�C.

r 2003 Elsevier Ltd. All rights reserved.

Keywords: Preferred temperature; Acute and gravitation methods; Critical thermal maximum; Acclimation response ratio;

Pterophyllum scalare

1. Introduction

Among environmental factors, temperature is impor-

tant since it determines physiological responses of

aquatic organisms, limits the rates of the biochemical

reactions and affects distribution. Generally, fish are

ing author. CICESE, Department of Aquacul-

iotechnology, P.O. Box 434844, San Diego, CA

A. Fax: +1-52-6175-05-34.

ess: fdiaz@cicese.mx (F. D!ıaz).

e front matter r 2003 Elsevier Ltd. All rights reserve

06-4565(03)00055-X

well adapted to environmental temperatures, leading to

similarities in ecological responses to temperature

(Magnuson et al., 1979). To cope with environmental

temperature changes, ectotherms have the capacity of

behavioral thermoregulation, which includes the active

selection of a thermal optimal habitat and avoidance of

unfavorable ones (Reynolds, 1979). Kelsch (1996)

showed evidence that fish selected temperatures to

maximize the proportion of metabolism available for

growth, activity, reproduction and other biological

functions. Thus, the temperature that an organism

d.

ARTICLE IN PRESSE. P!erez et al. / Journal of Thermal Biology 28 (2003) 531–537532

prefers often agrees with the thermal optima for such

physiological processes as the metabolism, growth,

swimming speed and reproduction (Brett, 1971; Beitin-

ger and Fitzpatrick, 1979). Generally, this temperature

coincides with the final temperature preferendum.

Thermal preference is a species-specific response, mod-

ified by age, food availability, season, pathologic

conditions, water quality, light intensity and intra- an

inter-specific competition (McCauley and Casselman,

1981; Giattina and Garton, 1982)

Two measures of temperature preference were defined

by Fry (1947), as ‘‘acute’’ and ‘‘final temperature

preferenda’’. Acute temperature preference usually deter-

mined within 2 h after immersion, and in this case the

animals in the gradient are strongly influenced by their

acclimation temperatures. The final preferendum is only

determined after the animals have had a sufficient period

of time to gravitate towards a region of thermal

preference (Reynolds and Casterlin, 1979; Jobling, 1981).

According to Hutchison (1976) the knowledge of the

critical thermal maximum (CTMax) provides a relevant

ecological and physiological index. Angelfish in nature

may encounter such temperatures either temporally or

spatially. CTMax may occur at different temperatures in

different species, but the physiological responses are the

same across a diversity of taxa (Lutterschmidt and

Hutchison, 1997). The CTMax is modified by both

seasonal and acclimation temperatures. Such data are

useful for evaluating the thermal requirements of an

organism and its physiological status (Paladino et al.,

1980). For these reasons, CTMax is an excellent

standard index for evaluating the thermal requirements

and physiology of the organisms (Paladino et al., 1980;

Lutterschmidt and Hutchison, 1997).

The angelfish Pterophyllum scalare (Lichtenstein) is a

cichlid in great demand due to its beauty, reproductive

capacity and adaptability to captivity; in consequence,

the economic potential of the species is also high

(Chapman et al., 1997). Tropical fish like P. scalare is

a new species for aquaculture; it is used in hobbies and

marketed all over the world; however, little attention has

been paid to the optimum thermal conditions required

for growth, nutrition and reproduction (Degani, 1993;

Blom et al., 2000).

In this study, we present temperature preference and

the upper thermal tolerance of angelfish P. scalare

juvenile, and adults, and their acclimation response ratio

(ARR) for optimizing their culture.

Fig. 1. Linear regression of temperatures in the 15 segments of

the gradient.

2. Material and methods

2.1. Maintenance

Angelfish were obtained from the stock of fish

cultured in the Laboratory-Aquarium of the Facultad

de Ciencias, UNAM. Adult fish had remained for six

generations in 60-l glass aquaria at 2871�C (P!erez-Cruz

et al., 1998). In this study the adults (5.2–12.5 g) belong

to this sixth generation and the juveniles (0.9–1.9 g) to

the seventh. The fish of both stages were kept at culture

temperature, the adults in 60-l and the juveniles in 4-l

aquaria to a density of 1 fish l�1. Angelfish were fed

twice a day with commercial balanced food (Sera-Vipan)

and Artemia sp. given at 5% and 1% body weight to

juveniles and adults, respectively. The feeding period

was 2 h, and excess was siphoned later. Partial replace-

ments of the water were done twice a week. The

characteristics of the water were the following: 28–

29�C, 8.1–8.3�C pH, 6–7mg O2 l�1, alkalinity of

103–120 and hardness of 187mg CaCO3 l�1. The

photoperiod was of 12 hD/12 hL with a gradual dawn

to dusk transition of 30min.

2.2. Preferred temperature

The thermal preference for juvenile and adult angel-

fish was determined in a horizontal trough of 300 cm

length and 20 cm diameter, with 15 segments. A Neslab

(model HX 100) thermoregulator was connected at one

end of the trough for cooling, and a 1000W heater was

placed at the other end for maintaining the thermal

gradient which ranged from 11�C to 38�C. To eliminate

the stratification in the water column, 15 air stones were

placed along the gradient. A dissolved oxygen concen-

tration of 6.1–11.4mg l�1 was maintained. Fig. 1 shows

that this procedure allowed that a linear thermal

gradient be maintained. The organisms were not fed

for 24 h prior to the trials.

2.3. Acute method

The acute preference temperature was measured in

120 juvenile and 120 adult angelfish acclimated for 25

ARTICLE IN PRESS

Fig. 2. Relationship between preferred temperature of juvenile

(A) and adult (B) angelfish P. scalare and their acclimation

temperature. The arrow denotes the acute estimated final

thermal preferendum. Median795% confidence interval.

E. P!erez et al. / Journal of Thermal Biology 28 (2003) 531–537 533

days at 20�C, 24�C, 28�C and 32�C71�C. Ten

organisms of similar size, individually tagged (Ruiz

and Villalobos, 1991), were introduced into the gradient

in the segment having the same temperature as their

acclimation temperature. For each experimental condi-

tion three repetitions were done. For the determination

of the final preferendum we used the acute method

described by Reynolds and Casterlin (1979), which

consisted of 15 observations counting the number of fish

in each segment every 10min period. Simultaneously,

the temperature was measured with digital thermo-

meters that were distributed equidistantly along the

trough.

2.4. Gravitation method

Ten fish of similar weight tagged individually (Ruiz

and Villalobos, 1991) were introduced into the gradient

in the segment having the same temperature as their

acclimation temperature. Four repetitions were done for

adult and juvenile angelfish (N total=80). The observa-

tions of the fish were made from reflections in a mirror

oriented at a 45� angle, recorded hourly during 24 h;

simultaneously, the temperature was measured with

digital thermometers that were distributed equidistantly

along the gradient. Prior to these recordings, the

organisms were kept 2 h in the trough to reduce the

stress caused by handling. During the day the light

intensity was 0.4� 10�16 quanta seg�1 cm�2; during the

night a red light was used, with an intensity of

0.06� 10�17 quanta seg�1 cm�2.

2.5. Tolerance temperature

The CTMax of 120 juvenile and 120 adult angelfish

acclimated gradually at experimental temperatures, were

determined. The fish remained at 20�C, 24�C, 28�C and

3271�C for 30 days. Each fish was placed in a 1-l glass

flask provided with constant aeration, then they were

introduced into a 40-l aquarium provided with a 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 and heated at a rate of 1�Cmin�1.

The stress events registered were the loss of righting

response (LRR) and the onset of muscular spasms (OS)

according to the criteria of Lutterschmidt and Hutch-

ison (1997). When the fish reached this point they were

returned to their acclimation temperature. The organ-

isms were used once only and the data for the animals

that did not recover after returning them to their

acclimation temperature after OS were discarded.

In the angelfish, we determined the ARR defined by

Claussen (1977) as DCTM=DT or the change in the

CTM per degree change in acclimation temperature.

Preferred temperature data were processed with the

Exploratory Data Analysis (Tukey, 1977), and they were

plotted as parallel boxes; a Kruskall–Wallis test was

employed for determining if preferred temperature

differences (Po0:05) occurred in repetitions when we

used an acute and gravitation methods. After this was

confirmed, an analysis of variance of ranks (Kruskall–

Wallis test) was used to analyze pooled data (Zar, 1999).

3. Results

In juvenile P. scalare the thermal preference by the

acute method was 30.2�C and the influence of the

acclimation temperature was not significant in all groups

(P > 0:05), (Fig. 2A). The preferred temperatures of adult

angelfish were dependent on acclimation temperature

ARTICLE IN PRESSE. P!erez et al. / Journal of Thermal Biology 28 (2003) 531–537534

and were found to be 27.8�C, 28.8�C and 30.0�C, for

acclimation temperatures of 20�C, 24�C and 28�C,

respectively. In fish acclimated at 32�C the preferred

temperature was 29.4�C (Fig. 2B). In juveniles exposed

Fig. 3. Thermoregulatory behavior of juvenile (A) and adult

(B) angelfish P. scalare. Median795% confidence interval.

Table 1

Critical thermal maximum (CTMax) of juveniles (n ¼ 120) and adu

temperatures

Stress responses Acclimation temper

20

Juveniles LRR 34.0a

(32.9, 35.1)

OS 36.9b

(36.8, 37.0)

Adults LRR 36.2a

ð35:5; 36:9ÞOS 38.4b

ð37:8; 39:0Þ

The underline between groups indicates a similar effect of acclimatio

LRR: loss of righting response, OS: onset of muscular spasms. MediaSignificant difference of LRR between juvenile and adults (Po0:0bSignificant difference of OS between juvenile and adults (Po0:05

to light/dark cycle of 24 h the interval of preferred

temperatures was 26.7–29.2�C with a median value of

29.0�C (Fig. 3A) and in the adults was 28.4–31.2�C with

a median of 30.1�C (Fig. 3B). Differences in the final

preferendum in juvenile and adult angelfish between day

and night were not observed. Both stages had similar

thermoregulatory behavior (P > 0:05) (Figs. 3A and B).

During CTMax trials the LRR was observed first, and

later the OS, Table 1. Values of OS were considered the

end point of CTMax. As the acclimation temperatures

increased, CTMax also increased in both stages

(Po0:05). Adult angelfish had a thermal tolerance

1.0�C higher than the juveniles (Po0:05), but the

increase in tolerance as a function of rising acclimation

temperature, was similar in both development stages.

Values were 3.9�C and 3.7�C for juveniles and adults,

respectively (P > 0:05).The acclimation temperature ratio (ARR) was 0.40–

0.46 for juveniles and 0.33–0.44 for adults of angelfish,

respectively.

4. Discussion

The range of preferred temperatures for both stages of

P. scalare was independent of acclimation temperature

over the range of acclimation temperatures used in this

research; similar results were obtained by Badenhuizen

(1967) in Oreochromis mossambicus and Kelsch and

Neill (1990) in blue tilapia Oreochromis aureus. Both

species of cichlids had a narrow preferred temperature

range regardless of acclimation temperature. Fish have a

variety of temperature-preference relationships that can

be categorized into three classes on the basis of whether

they are positive, independent or negative functions of

lts (n ¼ 120) Pterophyllum scalare acclimated at four different

atures (�C)

24 28 32

35.9 38.6a 38.8

(35.5, 36.3) (38.2, 39.0) (37.8, 39.8)

37.6 40.6 40.8b

(37.3, 37.9) ð40:2; 41:0Þ ð40:4; 41:2Þ

36.5 38.1a 41.2

ð35:6; 37:4Þ (37.7, 38.5) (39.4, 43.0)

38.6 41.0 42.1b

ð38:1; 39:1Þ (40.6, 41.4) (42.0, 42.2)

n temperature (P > 0:05).an values and confidence interval (95%) in parenthesis.

5).

).

ARTICLE IN PRESSE. P!erez et al. / Journal of Thermal Biology 28 (2003) 531–537 535

the acclimation temperature (Johnson and Kelsch,

1998). Species such as cichlids that experience low

annual thermal amplitude, but may be exposed to

temperature fluctuations on a daily or sub-seasonal basis

(short cycle) exhibit temperature-preference relation-

ships that are independent of the acclimation tempera-

ture (Johnson and Kelsch, 1998). Therefore the final

preferenda can be used as a measure of the temperature

selected by angelfish as an index of the magnitude of

temperatures to which species are adapted (Johnson and

Kelsch, 1998).

When both stages of P. scalare are placed separately

in a thermal gradient during 24 h, the fish distribute in

accordance to the presumed effect of the temperature on

surplus power capacity (Bryan et al., 1990). According

to Fraenkel and Gunn (1961) angelfish used an

orthothermokinesis orientation mechanism; that is,

juveniles the interval of preferred temperatures was

26.7–29.2�C and in the adults 28.4–31.2�C. Then, the

angelfish will remain within a relatively narrow tem-

perature range decreasing speed in those temperatures

that maximize their available power (Kelsch and Neill,

1990; Bryan et al., 1990; Kelsch, 1996). Preferred

temperature of fishes are probably those that offer the

greatest scope for activity (according to Fry, 1947) and

therefore, the greatest amount of available power that

could be channeled into adaptative functions such

activity, growth reproduction and survival (Kelsch,

1996).

CTMax is considered as a measure of thermal

tolerance and is determined by raising the temperature

progressively from the acclimation temperature until

physical disorganization occurs in response to the

thermal stressor (Becker and Genoway, 1979; Paladino

et al., 1980; Beitinger et al., 2000). These authors also

emphasize that the rate of temperature rise employed is

an important factor. In this work, the rate of change

employed was 1�Cmin�1 (Lutterschmidt and Hutch-

ison, 1997). As the temperature increased during a

CTMax test, angelfish usually display a sequence of

responses the LRR followed by the sudden OS.

Lutterschmidt and Hutchison (1997) considered that

OS is a more meaningful end point than LRR due to its

precision and greater physiological relevance. We

considered the end point of CTMax as the pre-death

thermal point at which locomotory movements become

disorganized and a fish loses the ability to escape the

conditions which may ultimately lead to its death

Beitinger et al. (2000). In both stages of angelfish this

point was the onset of spasms; the fish exhibited high

frequency of muscular movements, rigidity of the

pectoral fins and a high frequency in quivering of the

opercula. These responses seem to fit best the definition

of CTMax as ‘‘the arithmetic mean of the collective

thermal points at which the endpoint was reached by

individuals of a random sample of fish’’ (Hutchison,

1961). In aquacultural practices it is of fundamental

importance to know the CTMax since it is a good

indicator of the thermal tolerance of the angelfish and it

allows the identification of the temperatures at which the

first signs of stress occur (Paladino et al., 1980).

In both stages of angelfish we determined the ARR,

according to Claussen (1977), which is a convenient

index of the extent of thermal acclimation achieved, the

value for P. scalare was 0.33–0.46. For Salmo trutta,

Salvelinus fontinalis, Oncorhynchus gairdneri, O. apache,

and O. gilae, organisms inhabiting cool streams, the

calculated ARR was of 0.09–0.13 (Lee and Rinne, 1980).

In the darters Etheastoma flabellare, E. blennioides and

E. caeruleum, inhabitants in cool to warm streams the

calculated ARR was of 0.18–0.24 (Holohowskyj and

Wissing, 1985). Rajaguru (2002) obtained ARR values

for estuarine fishes of about 0.20 in Therapon jarbua and

0.25 in Etroplus suratensis. In Poecillia sphenops,

Hernandez and Buckle (1998) reported a value of 0.36.

In the mosquitofish Gambusia affinis, inhabitant of

warm spring streams, the calculated ARR was 0.40

(Otto, 1973). Cox (1978) and Woiwode and Adelman

(1992) obtained ARR values of 0.43 and 0.46 in Morone

saxatilis and Morone chrysops hybrid. For the sub-

tropical fish Prochilodus scrofa for two-size class

organisms the calculated ARR was of 0.38–0.47

(Barrionuevo and Fernandes, 1995). In the catfish

Ictalurus punctatus, inhabitant of warm lakes and large

rivers, the ARR calculated has an interval of 0.39–0.63

(Cheetham et al., 1976; Bennett et al., 1998; Currie et al.,

1998; D!ıaz and Buckle, 1999).

The existent data for ARR in different fish species

suggest that subtropical and tropical species have higher

values. These results suggest that the ARR values are

dependent on the existing habitat temperatures. D!ıaz

et al. (2002) reported a similar trend in several

crustacean species from different habitats. This response

is typical of aquatic poikilotherms, Johnson and Kelsch

(1998), that temperate species experiencing gradual long-

term temperature changes would have the necessary time

to make metabolic changes that would result in

substantial shifts in their ranges of tolerance. On the

other hand, subtropical and tropical species that

experience their greatest thermal extremes over a short

term must have a broad range of tolerance to survive to

relatively rapid temperature changes without time for

acclimation to adjust their tolerance.

Knowledge of the preference and the thermal

tolerance of a species are important in defining appro-

priate culture conditions, since this allows us to know

the thermal requirements of the organisms in a short

time. Besides, the information concerning the lethal

temperature and that concerning the species physiologi-

cal optimum are important for inferring the level of

survival in a particular climate space. To cultivate

angelfish we recommend those geographical zones of

ARTICLE IN PRESSE. P!erez et al. / Journal of Thermal Biology 28 (2003) 531–537536

M!exico were the temperatures are close to 30�C. Several

investigations have noted the specific relationship

between preferred temperature and the optimum tem-

peratures for the performance of many physiological

functions (Jobling, 1981; McCauley and Casselman,

1981; Kellog and Gift, 1983; Giattina and Garton,

1982). The tolerance for living in high temperature

intervals is characteristic of P. scalare which shares with

African cichlids, that are also thermophilic, this

tolerance gives these species a good potential for

cultivation in tropical areas. In this sense it is

recommended that before selecting places based on the

regional temperatures, the behavioral responses of the

endemic species should be considered (Mart!ınez-Pala-

cios et al., 1996). Thus, the results obtained in this study

are important for improvement or for establishing

angelfish cultures. Based on this we recommend to

choose places with high temperatures that do not exceed

30�C and do not change abruptly through the year.

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