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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 weredetermined 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 withresults for subtropical and tropical fishes.
(4)
Therefore it is recommended that angelfish cultivation should be consistent with temperatures that do not changeabruptly 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: [email protected] (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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