The critical thermal maximum: data to support

the onset of spasms as the definitive end point

William I. Lutterschmidt and Victor H. Hutchison

Abstract: We provide data to support the onset of spasms ( 0 s ) as the definitive end point for determining thermal
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12

tolerance with the critical thermal maximum (CTMax). We measured the CTMax of 610 animals in three vertebrate
classes, Actinopterygii, Amphibia, and Reptilia. All showed a significantly lower mean loss of righting response (LRR)
than 0 s . Statistical evaluation of the variability associated with the end points LRR and OS also showed that OS is a
more precise measure of thermal tolerance. OS is a more meaningful end point than LRR because it more closely fits
the original definition of the critical thermal maximum (R.B. Cowles and C.M. Bogert. 1944. Bull. Am. Mus. Nat.
Hist. 83: 261 -296) and occurs at temperatures required for physiological responses, such as heat-hardening and perhaps
the production of some heat-shock proteins. The adoption of OS as a standard end point would allow valid comparisons
of data from different studies and among taxa, an important consideration for comparative phylogenetic analyses. However,
we suggest that LRR should also be measured for comparisons with data from earlier studies.

RCsumC : On trouvera ici des donnkes qui supportent I'hypothkse selon laquelle le dkbut des spasmes ( 0 s ) marque
le point critique maximal de tempkrature (CTMax) dans l'kvaluation du seuil de tolkrance thermique. Nous avons mesurk
le CTMax de 610 animaux de trois classes de vertkbrks (actinoptkrygiens, amphibiens et reptiles). Chez tous les animaux,
le dkbut des spasmes s'est rkvklk un facteur plus constant que la perte moyenne de la capacitk de rkcupkration (LRR).
Une kvaluation statistique de la variabilitk associke aux seuils LRR et OS a kgalement dkmontre que la valeur de OS
For personal use only.

est une mesure plus prkcise de la tolkrance thermique. OS est un seuil plus fiable que LRR parce que c'est une variable
plus conforme a la dkfinition originale du point CTMax (R.B. Cowles et C.M. Bogert. 1944. Bull. Am. Mus. Nat.
Hist. 83 : 261 -296) et parce que le debut des spasmes se produit a des tempkratures qui dkclenchent des rkactions
physiologiques telles le durcissement dQ h la chaleur et peut-ttre aussi la production de protkines relike a un choc thermique.
L'adoption du seuil OS comme seuil standard aurait I'avantage de permettre des comparaisons valides entre les donnkes
de diffkrentes ktudes et entre diffkrents taxons, un atout important dans les analyses phylogknktiques comparatives.
Nous croyons cependant en la nkcessitk de continuer de mesurer la valeur LRR pour fins de comparaisons avec les
donnkes d'ktudes antkrieures.
[Traduit par la Rkdaction]

Introduction "phylogenetic provincialism," many authors being unaware

Measures of thermal tolerance have long been used to inves-
tigate the thermal capacities of organisms to tolerate their
complex holocoenotic environments. The increasing use of
data on organismal thermal tolerances indicates the con-
tinuing popularity and the usefulness of such physiological
parameters in modern biological investigations. To our
knowledge, at least 20 papers have been published within
the last year addressing the implications of thermal toler-
ance for physiological and ecological theory (reviewed in
Lutterschmidt and Hutchison 1997). However, a diversity of
experimental methods and terminology is still used by inves-
tigators despite pleas for standardization of test methods
(e.g., Hutchison 1976). Standardized methods were urged by
Hutchison (1979) and Paladino et al. (1980), who discussed
concerns about the validity of making comparisons of data
from different studies. The problem is further exacerbated by
of the techniques used with, and the results obtained from,
diverse taxonomic groups.
Our purpose is to provide general information for deter-
mining thermal tolerance and data that support the use of
the onset of spasms ( 0 s ) as the definitive end point for
determining thermal tolerance with the critical thermal maxi-
mum method. In a companion paper we provide a com-
prehensive review of thermal tolerance, and discuss its
applications to comparative physiology (see Lutterschmidt
and Hutchison 1997).
The two major methods for determining thermal tolerance
are discussed in Lutterschmidt and Hutchison (1997): (1) the
static or lethal temperature method, in which the time to
death at constant test temperatures is measured, and (2) the
dynumic method, which involves increasing test tempera-
tures until an appropriate end point is reached (Brett 1944;
Fry et al. 1942; Fry 1957). The static method uses statistical
techniques from pharmacology (Bliss 1937) to determine the

I
Received November 14, 1996. Accepted May 7, 1997.
W.I. Lutterschmidt and V.H. Hutchison. Department of
Zoology, University of Oklahoma, Norman, OK 73019,
U.S.A. (e-mail: wilutters@aardvark.ucs.ou.edu;
vhutchison@ou .edu.
equivalent of an from time - mortality curves, where
the "dosage" is the time during which animals are exposed
to a constant test temperature until death occurrs.
The dynamic method, the critical thermal minimum
(CTMin) and critical thermal maximum (CTMax), was

Can. J. Zool. 75: 1553- 1560 (1997) O 1997 NRC Canada

 Can. J. Zool. Vol. 75, 1997

Table 1. Sample sizes (n) and critical thermal maximum (CTMax) end points (loss of righting response (LRR) and the
onset of spasms (OS)), with their associated measures of dispersion (variance ( s 2 )and standard error (SE)), for 35
vertebrate species.

n LRR s2 SE 0s s2 SE P 5 0.05"

Actinopterygii
Siluriformes
Ictaluridae
Ictalurus punctatus
Cypriniformes
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Catostomidae
Ictiobus bubalus
Cyprinidae
Campostoma anomalum
Carassius auratus
Cyprinella lutrensis
Hybognathus placitus
Hybopsis amblops
Notemigonus crysoleucas
Notropis atherinoides
Phenacobius mirabilis
Pimephales notatus
Atheriniformes
Atherinidae
Menidia beryllina
For personal use only.

Cyprinodontiformes
Poecilidae
Gambusia afJinis
Perciformes
Percidae
Etheostoma spectaboli
Moronidae
Morone saxatilis
Centrarchidae
Lepomis cyanellus
Lepomis gulosus
Lepomis macrochirus
Lepomis megalotis
Lepomis microlophus
Micropterus dolomieui
Micropterus punctulatus
Micropterus salmoides
Cichlidae
Tilapia nilotica
Amphibia
Caudata
Salamandridae
Notophthalmus viridescens
Plethodontidae
Plethodon ouachitae
Plethodon richmondi
Desmognathus ochrophaeus
Anura
Ranidae
Rana berlandieri
Rana catesbeiana
Rana utricularia
Bufonidae
Bufo americanus

O 1997 NRC Canada

 Lutterschmidt and Hutchison
Table 1 (concluded).
n LRR
Hylidae
Hyla chrysoscelis 20 38.02
Reptilia
Squamata
Iguanidae
Cophosaurus texanus 35 47.65
Note: Taxonomic groupings for fishes (class, order, family, and species) follow Nelson (1994) and those for amphibians and
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12
reptiles follow Conant and Collins (1991).
"Homogeneity of variances for each end point of CTMax. We used an F test (Zar 1984) to compare differences between LRR
variance and OS variance. Significance to P I0.05 is indicated by "plus" if LRR variance > OS variance or "minus" if LRR
variance < OS variance; zero indicates nonsignificance.
introduced and defined by Cowles and Bogert (1944); CTMax
was defined as "the thermal point at which locomotory
activity becomes disorganized and the animal loses its ability
to escape from conditions that will promptly lead to its
death." This definition was modified by Lowe and Vance
(1955) to include statistical parameters. Standardized methods
for determining heating rates and end point were added
by Hutchison (1961, 1976). Thus, heating rates from about
0.5 to 1.5OC - min-' are often used. As the temperature
increases during a CTMax test, an animal usually displays a
For personal use only.
sequence of responses: loss of righting response (LRR),
. sudden onset of muscular spasms (OS), and finally "heat
rigor," "coma," or "death." The latter three events are not
definitive, are difficult to determine (Zweifel 1957), and are
seldom described fully (Lutterschmidt and Hutchison 1997).
To assess whether OS is the better CTMax end point, we
collected data to (i) compare LRR and OS within different
ectothermic vertebrates and determine which CTMax end
point has greater precision, and (ii) determine if the same end
point demonstrates this greater precision across taxa (i.e.,
for fish, amphibians, and reptiles). To illustrate the impor-
tance of standardizing methods for the determination of
upper-temperature tolerance, we discuss the difficulties in
using data from studies in which widely divergent methods
were used and the importance of obtaining thermal tolerance
data that can be used for comparisons with ecophysiological
theory and the results of comparative physiology and com-
parative phylogeny investigations (Felsenstein 1985). A
phylogenetic analysis of these data will be published in a
separate paper.
Materials and methods
Animal collection and acclimation
We collected 439 fish representing 24 species and 9 families,
33 salamanders representing 4 species and 2 families, 103 frogs
representing 5 species and 3 families, and 35 lizards represent-
ing 1 species in the Iguanidae. These animals represent 3 ver-
tebrate classes (Actinopterygii, Amphibia, and Reptilia) and
8 orders (Siluriformes, Cypriniformes, Perciformes, Atherini-
formes, Cyprinodontiformes, Caudata, Anura, Squamata) (Table 1).
We collected all native fish by seining streams and reservoirs in
central and south-central Oklahoma. Tilapia nilotica were obtained
from aquaculture ponds at the University of Oklahoma. Sala-
manders and frogs were collected from central and southeastern
Oklahoma (Cleveland and LaFlore counties, respectively) and (or)
2.056 0.321 40.81 0.367 0.136 +
1.753 0.224 49.42 0.808 0.152 +
obtained from animal suppliers. The lizard Cophosaurus texanus
was collected from central Kimble County, Texas.
Fishes were acclimatized in Living Streama aquaria for 2 weeks
at 10 f 1"C and a 12 h light : 12 h dark photoperiod; photophase
was from 06:00 to 18:00, centered on noon CST. We use "acclima-
tion" to indicate adustment to one environmental factor and "accli-
matization" for changes to two or more factors, following Folk's
(1974) "rules" for uniform terminology. All measures of thermal
tolerance were made between the second and tenth hours of the
photophase to reduce possible effects of diel cycles on thermal
tolerance (Hutchison 1976). The same acclimation regimes were
used for amphibians in an environmental chamber. However,
measures of thermal tolerance of amphibians were made between
20:00 and 22:00 (second and fourth hours) of the scotophase,
coinciding with the peaks of normal activity. Cophosaurus texanus
(because of their high thermal requirements) were acclimated at
25°C and were also tested during peak diel activity (i.e., between
10:00 and 16:00, or the fourth and tenth hours of their photophase).
Although acclimation temperature influences thermal tolerance
(Hutchison and Rowlan 1974), our use of 25°C in the acclimation
of C. texanus is valid because we evaluated the variability in end
points among individuals of the same species (i.e., pairwise com-
parisons) and not the differences in thermal tolerance among species
or treatments.
Measures of thermal tolerance
We used the dynamic method, CTMax, for determining thermal
tolerance following the methods outlined by Hutchison (1961).
We recorded both LRR and the onset of opercular spasms ( 0 s ) in
fishes or the onset of muscular spasms in amphibians and reptiles
for indices of CTMax, with OS being regarded as the definitive end
point (Paulson and Hutchison 1987). We recorded body tempera-
ture (T,) at both end points for completeness of data and for
statistical evaluation. T, for LRR in fishes was recorded when
they lost equilibrium and demonstrated inverted swimming (e.g.,
Al-Johany and Yousuf 1993; Korhonen and Lagerspetz 1996;
Pyron and Beitinger 1993; Rutledge and Beitinger 1989). OS of fish
was exhibited as disorganized and high-frequency muscular move-
ments, rigidity of the pectoral fins, and, especially, high-frequency
quivering of the opercula. All individuals recovered from exposure
to LRR and 0 s . These behaviors seem to fit best the definition of
CTMax as "the arithmetic means of the collective thermal points
at which locomotor activity becomes disorganized and the animals
lose their ability to escape from conditions that will promptly lead
to their death" (Hutchison 1961).
We placed each fish in a heating chamber to increase T, .by
1"C . min-' until LRR and OS were observed. The T, of fish
>8.0 cm standard length and (or) 30 g body mass (M,) was
O 1997 NRC Canada
 Can. J. Zool. Vol. 75, 1997

Fig. 1. Relationships between body temperature (T,) and associated with each CTMax end point (i.e., LRR and 0 s ) for each
chamber-waterlenvironmental temperature (T,) for Rana species. We then used paired t tests to determine significant differ-
catesbeiana and Lepomis macrochirus during heating at a rate of ences between the means, variances, and SEs associated with LRR
1°C min-I. and OS for all fishes, and amphibians, and reptiles. Paired t tests
were also used to determine if these measures of precision asso-
Time (min) ciated with LRR and OS were consistent for all taxa combined
(Table 2).
0 5 10 15 20 25 30 An a priori natural log transformation for normality was per-
formed on all measures of variance and SE (Bartlett and Kendall
Rana catesbeiana 1946) prior to statistical comparisons of LRR and 0 s . We deter-
(BM = 16.9g; SL = 7.8 cm) mined that all assumptions of normality were met prior to statistical
analyses and used Sigmastat l.OB (Jandel Scientific Software Corp.
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12

1994) for all pairwise comparisons and Statview 4.5@ (Abacus

Concepts 1992) for regression analyses.

Tb = Te(0.941)+0.126
(F = 1669.61; df = 1,15; P = 0.0001)
(BM = 164.7g; SVL = 13.3 cm)
Tb = Te(0.841)-0.362
F = 803.43; df = 1,16; P = 0.0001)
For personal use only.
Animal care
Animals were collected under authority of permits for scientific
collectors issued by the Oklahoma Department of Wildlife Conser-
vation. We followed guidelines for use of live animals in field
research (American Society of Icthyologists and Herpetologists
1987a, 19876). Laboratory study protocols were approved by the
University of Oklahoma Animal Care and Use Committee (Animal
Welfare Assurance No. 73-R-100 on file with the Office for the
Protection of Research Risks). The procedures followed were in
accordance with the principles and guidelines of the Canadian
Council on Animal Care.

(BM = 16.9g; SL = 7.8 cm)
Water Temperature (OC)
measured by inserting a 36 gauge thermocouple into their urogenital
opening (ca. 10- 15 mm into the lower intestine) prior to testing.
The T, of frogs with snout-vent length >9.0 cm and (or) 75 g M,
was also measured with a thermocouple. The T, of smaller fishes
and frogs closely followed the chamber-water temperature (Fig. 1) ,
so the use of thermocouples was unnecessary. All M, values for
salamanders and lizards were less than 75 g and no thermocouples
were used.
Statistical analyses
Mean LRR and OS were calculated for each species; their asso-
ciated variances (s2) and standard errors (SE) are also shown
(Table 1). These measures allowed for the evaluation of precision
Results
Measures and statistical comparisons of thermal-tolerance
end points
All 610 individuals of the 34 species demonstrated LRR at
lower temperatures than OS (Fig. 2). All paired t tests
showed that mean temperature was significantly lower for
LRR than for OS in fishes, amphibians and reptiles, and all
taxa combined (Table 2). We observed no size-dependent
effects on either LRR or OS within species.
Significantly greater variances were also associated with
the end point LRR for fishes, amphibians and reptiles, and
all taxa combined (Table 2, Fig. 2). These results show that
OS is a more precise measure of thermal tolerance. An F test
for comparing the homogeneity of within-species variances
of LRR and OS also showed that these variances differed
significantly only when LRR variance was greater than OS
variance (Table 1).
Regression analyses indicated that critical masses when
Tb and waterlenvironment temperature (T,) were equal were
greater than 164.7 and 43.7 g for a frog and a fish species,
respectively. The relationship between Te and Tb was highly
significant for all four analyses (Fig. I), with Te explaining
99.1 % of the variance in Tb This suggests the appropriate-
ness of water as a heating medium for ease of controlling
heating rates for determining CTMax.
Discussion
Measures and statistical comparisons of thermal-tolerance
end points
Significantly more variance is associated with the end point
LRR than OS for all taxa (Table 2). Additionally, tests for
the homogeneity of within-species variances of LRR and OS
showed that these variances differed significantly only when

O 1997 NRC Canada

 Lutterschmidt and Hutchison
Table 2. Critical thermal maximum (CTMax) end points; results of paired t tests
showing group means (a,
standard deviation (SD), and standard error (SE).
Comparison
Means of LRR and OS
Fishes
(t = -12.00, df = 23, P < 0.0001)
Amphibians and reptiles
(t = -9.65, df = 9, P < 0.0001)
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All taxa combined
(t = -13.80, df = 33, P < 0.0001)
ln(variances) of LRR and OS
Fishes
(t = 3.46, df = 20, P = 0.0025)
Amphibians and reptiles
(t = 3.73, df = 9, P = 0.0047)
All taxa combined
(t = 4.94, df = 30, P < 0.0001)
ln(standard errors) of LRR and OS
For personal use only.
Fish
(t = 3.47, df = 20, P = 0.0024)
Amphibians and reptiles
(t = 3.75, df = 9, P = 0.0046)
All taxa combined
(t = 4.95, df = 30, P < 0.0001)
Note: The parameters compared are means and measures of dispersion (i.e., variance and
SE) for loss of righting response (LRR) and the onset of spasms ( 0 s ) in fishes, amphibians and
reptiles, and all taxa combined.
LRR variance was greater than OS variance (Table I).
Although OS variance was greater than LRR variance for
some species (Table I), the homogeneity of these within-
species LRR and OS variances did not differ statistically.
Specifically, 3 1 variances were compared from paired LRR
and OS end points for each species. Of these comparisons,
24 showed LRR variance to be greater than OS variance;
7 showed OS variance to be greater. However, for these
seven observations of greater OS variance, there was no
significant difference in the homogeneity of variances between
LRR and 0 s . Of the 24 comparisons in which LRR variance
was greater, 11 differed significantly (P < 0.05). Thus, OS
is a more valuable and meaningful CTMax end point than
LRR because of its greater precision.
A definitive and standard CTMax end point: its
importance to comparative physiology
Studies in comparative animal physiology involve "the
comparing and contrasting of physiological mechanisms,
processes, or responses of different species of animals, or of
a single species under differing conditions" (Withers 1992).
-
Group x SD SE
Mean LRR
Mean OS
Mean LRR
Mean OS
Mean LRR
Mean OS
ln(LRR SE)
ln(0S SE)
ln(LRR SE)
ln(0S SE)
ln(LRR SE)
ln(0S SE)
An underlying assumption of any comparative study, how-
ever, is that all individuals and species have received identical
experimental treatments. Without this assumption, we may
attribute physiological differences in high-temperature toler-
ance to adaptation when aptation was a cause. Inferring
evolutionary changes in physiological traits and function
from invalid comparisons may lead to biased conclusions.
We therefore emphasize the importance of adopting a definitive
and standard end point for measuring CTMax.
We have demonstrated that OS is a more meaningful end
point than LRR because of its precision and greater physio-
logical relevance. Although OS is more biologically mean-
ingful, we recommend that both LRR and OS be determined
and reported (e.g., Berkhouse and Fries 1995) in future
comparisons with the results of past studies. We also encour-
age the use of additional end points, if they are clearly
defined and if the value of OS is determined. Most impor-
tantly, when comparing and contrasting data on thermal
tolerance among species from different studies, we recom-
mend that investigators consider possible differences in
experimental methods (i .e., acclimation, heating rate, etc.),
O 1997 NRC Canada
 Can. J. Zool. Vol. 75, 1997

(a> Temperature (OC)

lctalurus punctatus (20)

-
___
I I
Campstoma anomalum (I8)
I
Carassius auratus (11 )

Cyplinellalutrensis (20)
I -0-
I
Hybognathusplacitus (26)
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12

Hybopsis amblops (1)

lctiobus bubalus (1)

Notemigonus crysoleucas (28)

Notropis atherinoides (8)

Phenacobius mirabilis (2)

Pimephales notatus (29)

- o--IDo I

--
Menidia beryllina (20)

Gambusia affinis (20)

Etheostoma spectabile (19)

Morone saxatilis (3)

1
Ts.<-
5, I
Lepomis cyanellus (15)
I
For personal use only.

Lepmis gulosus (4) mD0 0 0 . I

Lepomis macrochirus (84)

Lepomis megalotis (59)

I -+ I
Lepomis microlophus (3)

Micropterus dolomieu (1) 0

0 I
Micropteruspunctulatus (5)

Micropterus salmoides (17)

Tilapia nilotica (25)
23
-
I
I
~
- l '
25
~
27
. ' I
29
' .
31
Temperature
.
33
.

(OC)
l
35
. .
37
~ .
. . l . * . . l , d . . . n l n . L ~
39
I
~ ~

Notophthalmus viridescens (10)

Plethodon ouachitae (9)

Plethodon richmondi (4)

Desmognathus ochrophaeus (10)

Rana berlandieri (20)

Rana catesbeiana (19)

Rana utricularia (20)

Bufo americanus (24)

Hyla chrysoscelis (20)

Cophosaunrs texanus (35)

26 30 34 38 42 46 50
Temperature ("C)

O 1997 NRC Canada

 Lutterschmidt and Hutchison
Fig. 2. Mean loss of righting response (LRR) and onset of spasms ( 0 s ) for fishes (a) and amphibians and reptiles (b). An open circle
indicates the range, a black rectangle indicates 2SE, and the white line at the midpoint of the black rectangle indicates mean CTMax T,.
Numbers in parentheses are sample sizes.
otherwise ecological and (or) evolutionary conclusions
drawn from studies in which different protocols were used
may be invalid. We advocate OS as the most biologically
relevant end point and hope that its adoption will facilitate
the development of standard definitions and techniques for
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12
making valid comparisons of the results of future studies.
Conclusion
A plea is once again made for a better appreciation of the
factors that influence the thermal tolerance of ectotherms and
consideration of the methods used for determining thermal
tolerance under experimental conditions (Hutchison 1976).
In nature, animals continually adjust to fluctuations in envi-
ronmental factors. Because it is not possible to control com-
pletely the entire holocoenotic environment and its variations
in the laboratory, we must recognize that many environmen-
tal factors may influence thermal tolerance and its measure-
ment. Animals' tolerance of a single environmental factor
y . ch as temperature is typically greater than their tolerance
of combinations of environmental factors studied simultane-
For personal use only.
ously. The modification of thermal tolerance by many envi-
ronmental factors (e.g ., photoperiod, die1 and seasonal cycles,
respiratory gases, pH, salinity, diet, reproductive status)
should be recognized and controlled as far as possible. Thus,
tolerance of high temperature must eventually be studied as
part of multiple-factor interactions. The adoption of more
standardized methods and terminology will greatly improve
communication among investigators and allow for valid com-
parisons among their data (Hutchison 1976). This will ulti-
mately facilitate the necessary multiple-factor approach and
broader applications of these data to ecophysiological theory
(Lutterschmidt and Hutchison 1997).
Acknowledgments
We thank R.D. Durtsche, P.W. Lienesch, G.A. Marvin,
J.F. Schaefer, and W .L. Shelton for help in animal collection.
We thank H.B. Haines, W.J. Matthews, J.N. Thompson,
M.A. Smale, L.L. Wallace, and L.J. Vitt for reviews of the
manuscript and M. Pyron for ideas and suggestions. Field-
work was supported in part by a grant from The Nature
Conservancy (Oklahoma Chapter) to W .I.L. We also thank
C .C. Vaughn (Oklahoma Natural Heritage Inventory) and
J .N. Thompson (Department Chair of Zoology, University
of Oklahoma) for travel funds and equipment.
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