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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]
I
Received November 14, 1996. Accepted May 7, 1997. equivalent of an from time - mortality curves, where
W.I. Lutterschmidt and V.H. Hutchison. Department of the "dosage" is the time during which animals are exposed
Zoology, University of Oklahoma, Norman, OK 73019, to a constant test temperature until death occurrs.
U.S.A. (e-mail: wilutters@aardvark.ucs.ou.edu; The dynamic method, the critical thermal minimum
vhutchison@ou .edu. (CTMin) and critical thermal maximum (CTMax), was
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
Table 1 (concluded).
n LRR
Hylidae
Hyla chrysoscelis 20 38.02 2.056 0.321 40.81 0.367 0.136 +
Reptilia
Squamata
Iguanidae
Cophosaurus texanus 35 47.65 1.753 0.224 49.42 0.808 0.152 +
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
introduced and defined by Cowles and Bogert (1944); CTMax obtained from animal suppliers. The lizard Cophosaurus texanus
was defined as "the thermal point at which locomotory was collected from central Kimble County, Texas.
activity becomes disorganized and the animal loses its ability Fishes were acclimatized in Living Streama aquaria for 2 weeks
to escape from conditions that will promptly lead to its at 10 f 1"C and a 12 h light : 12 h dark photoperiod; photophase
death." This definition was modified by Lowe and Vance was from 06:00 to 18:00, centered on noon CST. We use "acclima-
tion" to indicate adustment to one environmental factor and "accli-
(1955) to include statistical parameters. Standardized methods
matization" for changes to two or more factors, following Folk's
for determining heating rates and end point were added (1974) "rules" for uniform terminology. All measures of thermal
by Hutchison (1961, 1976). Thus, heating rates from about tolerance were made between the second and tenth hours of the
0.5 to 1.5OC - min-' are often used. As the temperature photophase to reduce possible effects of diel cycles on thermal
increases during a CTMax test, an animal usually displays a tolerance (Hutchison 1976). The same acclimation regimes were
For personal use only.
sequence of responses: loss of righting response (LRR), used for amphibians in an environmental chamber. However,
. sudden onset of muscular spasms (OS), and finally "heat measures of thermal tolerance of amphibians were made between
rigor," "coma," or "death." The latter three events are not 20:00 and 22:00 (second and fourth hours) of the scotophase,
definitive, are difficult to determine (Zweifel 1957), and are coinciding with the peaks of normal activity. Cophosaurus texanus
seldom described fully (Lutterschmidt and Hutchison 1997). (because of their high thermal requirements) were acclimated at
25°C and were also tested during peak diel activity (i.e., between
To assess whether OS is the better CTMax end point, we
10:00 and 16:00, or the fourth and tenth hours of their photophase).
collected data to (i) compare LRR and OS within different Although acclimation temperature influences thermal tolerance
ectothermic vertebrates and determine which CTMax end (Hutchison and Rowlan 1974), our use of 25°C in the acclimation
point has greater precision, and (ii) determine if the same end of C. texanus is valid because we evaluated the variability in end
point demonstrates this greater precision across taxa (i.e., points among individuals of the same species (i.e., pairwise com-
for fish, amphibians, and reptiles). To illustrate the impor- parisons) and not the differences in thermal tolerance among species
tance of standardizing methods for the determination of or treatments.
upper-temperature tolerance, we discuss the difficulties in
using data from studies in which widely divergent methods Measures of thermal tolerance
were used and the importance of obtaining thermal tolerance We used the dynamic method, CTMax, for determining thermal
data that can be used for comparisons with ecophysiological tolerance following the methods outlined by Hutchison (1961).
theory and the results of comparative physiology and com- We recorded both LRR and the onset of opercular spasms ( 0 s ) in
parative phylogeny investigations (Felsenstein 1985). A fishes or the onset of muscular spasms in amphibians and reptiles
phylogenetic analysis of these data will be published in a for indices of CTMax, with OS being regarded as the definitive end
separate paper. 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
Materials and methods
they lost equilibrium and demonstrated inverted swimming (e.g.,
Animal collection and acclimation Al-Johany and Yousuf 1993; Korhonen and Lagerspetz 1996;
We collected 439 fish representing 24 species and 9 families, Pyron and Beitinger 1993; Rutledge and Beitinger 1989). OS of fish
33 salamanders representing 4 species and 2 families, 103 frogs was exhibited as disorganized and high-frequency muscular move-
representing 5 species and 3 families, and 35 lizards represent- ments, rigidity of the pectoral fins, and, especially, high-frequency
ing 1 species in the Iguanidae. These animals represent 3 ver- quivering of the opercula. All individuals recovered from exposure
tebrate classes (Actinopterygii, Amphibia, and Reptilia) and to LRR and 0 s . These behaviors seem to fit best the definition of
8 orders (Siluriformes, Cypriniformes, Perciformes, Atherini- CTMax as "the arithmetic means of the collective thermal points
formes, Cyprinodontiformes, Caudata, Anura, Squamata) (Table 1). at which locomotor activity becomes disorganized and the animals
We collected all native fish by seining streams and reservoirs in lose their ability to escape from conditions that will promptly lead
central and south-central Oklahoma. Tilapia nilotica were obtained to their death" (Hutchison 1961).
from aquaculture ponds at the University of Oklahoma. Sala- We placed each fish in a heating chamber to increase T, .by
manders and frogs were collected from central and southeastern 1"C . min-' until LRR and OS were observed. The T, of fish
Oklahoma (Cleveland and LaFlore counties, respectively) and (or) >8.0 cm standard length and (or) 30 g body mass (M,) was
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
Tb = Te(0.941)+0.126
Animal care
(F = 1669.61; df = 1,15; P = 0.0001) 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
(BM = 164.7g; SVL = 13.3 cm) 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
Tb = Te(0.841)-0.362 accordance with the principles and guidelines of the Canadian
Council on Animal Care.
F = 803.43; df = 1,16; P = 0.0001)
For personal use only.
Results
(BM = 16.9g; SL = 7.8 cm)
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
Water Temperature (OC) 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
measured by inserting a 36 gauge thermocouple into their urogenital
99.1 % of the variance in Tb This suggests the appropriate-
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, ness of water as a heating medium for ease of controlling
was also measured with a thermocouple. The T, of smaller fishes heating rates for determining CTMax.
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 Discussion
were used. Measures and statistical comparisons of thermal-tolerance
end points
Statistical analyses Significantly more variance is associated with the end point
Mean LRR and OS were calculated for each species; their asso- LRR than OS for all taxa (Table 2). Additionally, tests for
ciated variances (s2) and standard errors (SE) are also shown the homogeneity of within-species variances of LRR and OS
(Table 1). These measures allowed for the evaluation of precision showed that these variances differed significantly only when
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 Group x SD SE
Mean OS
All taxa combined
(t = -13.80, df = 33, P < 0.0001) Mean LRR
Mean OS
ln(variances) of LRR and OS
Fishes
(t = 3.46, df = 20, P = 0.0025)
Fish
(t = 3.47, df = 20, P = 0.0024) ln(LRR SE)
ln(0S SE)
Amphibians and reptiles
(t = 3.75, df = 9, P = 0.0046) ln(LRR SE)
ln(0S SE)
All taxa combined
(t = 4.95, df = 30, P < 0.0001) ln(LRR SE)
ln(0S SE)
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). An underlying assumption of any comparative study, how-
Although OS variance was greater than LRR variance for ever, is that all individuals and species have received identical
some species (Table I), the homogeneity of these within- experimental treatments. Without this assumption, we may
species LRR and OS variances did not differ statistically. attribute physiological differences in high-temperature toler-
Specifically, 3 1 variances were compared from paired LRR ance to adaptation when aptation was a cause. Inferring
and OS end points for each species. Of these comparisons, evolutionary changes in physiological traits and function
24 showed LRR variance to be greater than OS variance; from invalid comparisons may lead to biased conclusions.
7 showed OS variance to be greater. However, for these We therefore emphasize the importance of adopting a definitive
seven observations of greater OS variance, there was no and standard end point for measuring CTMax.
significant difference in the homogeneity of variances between We have demonstrated that OS is a more meaningful end
LRR and 0 s . Of the 24 comparisons in which LRR variance point than LRR because of its precision and greater physio-
was greater, 11 differed significantly (P < 0.05). Thus, OS logical relevance. Although OS is more biologically mean-
is a more valuable and meaningful CTMax end point than ingful, we recommend that both LRR and OS be determined
LRR because of its greater precision. and reported (e.g., Berkhouse and Fries 1995) in future
comparisons with the results of past studies. We also encour-
A definitive and standard CTMax end point: its age the use of additional end points, if they are clearly
importance to comparative physiology defined and if the value of OS is determined. Most impor-
Studies in comparative animal physiology involve "the tantly, when comparing and contrasting data on thermal
comparing and contrasting of physiological mechanisms, tolerance among species from different studies, we recom-
processes, or responses of different species of animals, or of mend that investigators consider possible differences in
a single species under differing conditions" (Withers 1992). experimental methods (i .e., acclimation, heating rate, etc.),
Cyplinellalutrensis (20)
I -0-
I
Hybognathusplacitus (26)
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12
--
Menidia beryllina (20)
(OC)
l
35
. .
37
~ .
. . l . * . . l , d . . . n l n . L ~
39
I
~ ~
26 30 34 38 42 46 50
Temperature ("C)
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 lines for use of live amphibians and reptiles in field research.
drawn from studies in which different protocols were used Allen Press, Lawrence, Kans.
may be invalid. We advocate OS as the most biologically Bartlett, M.S., and Kendall, D.G. 1946. The statistical analysis of
relevant end point and hope that its adoption will facilitate variance heterogeneity and the logarithmic transformation. J. R.
the development of standard definitions and techniques for Stat. Soc. (Suppl.), 8: 128- 138.
Berkhouse, C.S., and Fries, J.N. 1995. Critical thermal maxima of
Can. J. Zool. Downloaded from www.nrcresearchpress.com by FORDHAM UNIVERSITY on 11/28/12
ously. The modification of thermal tolerance by many envi- Fry, F.E.J. 1957. The lethal temperature as a tool in taxonomy.
ronmental factors (e.g ., photoperiod, die1 and seasonal cycles, Colloq. Int. Biol. Mar. Stn. Biol. Roscoff Ann. Biol. 33:
respiratory gases, pH, salinity, diet, reproductive status) 205-219.
should be recognized and controlled as far as possible. Thus, Fry, F.E.J., Brett, J .R., and Clawson,. G.H. 1942. Lethal limits of
tolerance of high temperature must eventually be studied as temperature of young goldfish. Rev. Can. Biol. 1: 50-56.
Hutchison, V.H. 196 1. Critical thermal maximum in salamanders.
part of multiple-factor interactions. The adoption of more Physiol. Zool. 34: 92 - 125.
standardized methods and terminology will greatly improve Hutchison, V .H. 1976. Factors influencing thermal tolerances of
communication among investigators and allow for valid com- individual organisms. ERDA (Energy Res. Dev. Adm.) Symp.
parisons among their data (Hutchison 1976). This will ulti- Ser. CONF750425. pp. 10-26.
mately facilitate the necessary multiple-factor approach and Hutchison, V. H. 1979. Thermoregulation. In Turtles: perspectives
broader applications of these data to ecophysiological theory and research. Edited by M. Harless and H. Morlock. John Wiley
(Lutterschmidt and Hutchison 1997). and Sons, Inc., New York. pp. 207-228.
Hutchison, V.H., and Rowlan, S.D. 1974. Thermal acclimation
Acknowledgments and tolerance in the mudpuppy, Necturus maculosus. J . Herpetol .
9: 367 -368.
We thank R.D. Durtsche, P.W. Lienesch, G.A. Marvin, Jandel Scientific Software. Corp. 1994. Sigmastat@ 1.0. Jandel
J.F. Schaefer, and W .L. Shelton for help in animal collection. Scientific Software Corp., San Rafael, Calif.
We thank H.B. Haines, W.J. Matthews, J.N. Thompson, Korhonen, I.A., and Lagerspetz, K.Y .H. 1996. Heat shock
M.A. Smale, L.L. Wallace, and L.J. Vitt for reviews of the response and thermal acclimation in Asellus aquaticus. J. Therm.
Biol. 21: 49-56.
manuscript and M. Pyron for ideas and suggestions. Field- Lowe, C.H., and Vance, V.J. 1955. Acclimation of the critical
work was supported in part by a grant from The Nature thermal maximum of the reptile Urosaurus ornatus. Science
Conservancy (Oklahoma Chapter) to W .I.L. We also thank (Washington, D.C.), 122: 73 -74.
C .C. Vaughn (Oklahoma Natural Heritage Inventory) and Lutterschmidt, W.I., and Hutchison, V.H. 1997. The critical
J .N. Thompson (Department Chair of Zoology, University thermal maximum: history and critique. Can. J. Zool. 75:
of Oklahoma) for travel funds and equipment. 1561-1574.
Nelson, J.S. 1994. Fishes of the world. 3rd ed. John Wiley and
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