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Thermal time - Concepts and utility

Article  in  Annals of Applied Biology · January 2005

DOI: 10.1111/j.1744-7348.2005.04088.x

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Annals of Applied Biology (2005), 146:1–14
1

Thermal time – concepts and utility

D L TRUDGILL1*, A HONEK2, D LI3 and N M VAN STRAALEN4

Scottish Crop Research Institute, Invergowrie, Dundee, Scotland DD2 5DA, UK

1
2
Research Institute of Crop Production, Drnoska 507, CZ-16106 Praha, 6-Ruzyne, Czech Republic
3
Biological Sciences, University of Singapore, 10 Kent Ridge Cresent, Singapore 1192600
4
Vrije Universiteit, Institute of Ecological Science, De Boelelaan 1087, 1081 HV Amsterdam, The
Netherlands

Summary
This paper (i) reviews temperature/development rate relationships in plants and poikilothermic
invertebrates, (ii) argues that the relationship is often linear over much of the range up to the thermal
optimum (To) and provides a possible mechanism, (iii) provides evidence of a trade-off between the
base temperature (Tb) and the thermal constant (DD) that enables each species to adapt to its thermal
environment, and (iv) indicates some of the practical and ecological implications. Where a linear
relationship has been characterised it is possible to estimate the base temperature for development (Tb,
expressed in °C) and the thermal constant for development (DD, the reciprocal of the temperature
coefficient (a), expressed in degree [°C] days accumulated above Tb). A possible basis for the linear
relationship between rate and temperature is proposed based on the Arrhenius and Sharpe-Schoolfield
equations involving activation enthalpy and progressive inactivation of the reactant molecules at both
low and high temperatures. Knowledge of Tb and DD enables rates of development of organisms/
processes to be calculated and compared at any given temperature between Tb and To. An analysis of
published results for differentiation processes (differentiation = a change of state) in species of insects,
Collembola, spiders, nematodes and plants showed that Tb tended to vary with the temperature of the
niche to which the organism is adapted, and that there was a trade-off between Tb and DD. Tropical
species had higher values of Tb than temperate and DD decreased as Tb increased (and vice versa). This
conferred a competitive advantage on each species in the thermal environment to which it was adapted.
The decrease in DD tended to be relatively greater than the increase in Tb, further favouring a high Tb
in tropical species. A mechanism for the trade-off is suggested whereby DD and Tb were shown to be
correlated (P < 0.01) with the activation enthalpy (HA) of an assumed, rate-limiting enzyme. Thermal
time can also be applied to processes involving growth (= an increase in dry weight) when the DD
requirement for development to maturity is the sum of the requirements for differentiation and growth.
Rates of both differentiation and growth can vary greatly between species, depending upon the niche
they inhabit, and the implications of such differences for resource requirements are considered. In
insects and nematodes, but not in annual plants, development is usually coupled to growth. Consequently,
when resources are inadequate, mature size in these animals varies less than in plants. Thermal time is
shown to provide insight into the life strategies of species within their communities and to have practical
implications.

Key words: Temperature, degree days, physiological time, threshold or base temperature, rates of
growth and development, resources, size, modelling, nematodes, insects, spiders, Collembola, plants

Introduction temperature (T e ) decreases, their rates of

Temperature is a basic factor that influences the
course of life, specifically the rate of its change –
physiological time. Thermal time provides a measure
of physiological time as it relates to many
poikilothermic species (those whose body
temperature is effectively identical to that of their
environment) of plants and invertebrate animals.
Most poikilothermic species are adapted to particular
temperature ranges and temperature is often a major
environmental factor influencing their distribution.
Within those ranges, as the environmental
development slow and, if the temperature falls low
enough, development will cease at their lower
developmental (base) temperature (T b ). As
temperature increases, their rates of development
increase up to a temperature optimum (To), above
which they again decrease and eventually cease at
their temperature maximum (Tm). When data on
durations of development at temperatures between
Tb and To are converted to their reciprocals, i.e. to
rates of development, the relationship between rate
and temperature is often close to linear (e.g. Fig. 1)
for plants and many invertebrate animals

*Corresponding Author E-mail: jeantrudgill@yahoo.co.uk

© 2005 Association of Applied Biologists

2 D L TRUDGILL ET AL.
(ectothermic vertebrates appear to have more
complicated responses to temperature). From this
relationship two vital constants can be determined:
1) the thermal constant (the number of degree-days
– DD – needed to complete the developmental
process at any temperature within the range Tb to
To) and 2) the base temperature Tb.
The thermal constant (DD) requirement for a
developmental process provides a measure of the
physiological time required for the completion of
that process. It is expressed as the number of degree
(in °C) days – hence DD and the term “thermal time”.
Together with Tb, it can be used to calculate the rate
of the process at any value of Te (up to To). A crucial
feature of thermal time is that the DD requirement
is based on a summation of the physiologically
effective temperature (i.e. Te minus Tb) over the
duration of the process, and expressing time in
thermal units removes the time-dependency of
biological processes where this is due to temperature
change (Van Straalen, 1983). A linear relation
between Te and the rate of the process under study is
essential for the estimation of both Tb (the intercept
on the Te axis; Allee et al., 1949) and DD (the
reciprocal of the temperature coefficient (a), i.e. the
reciprocal of the slope of the regression; Garcia-
Huidobro et al., 1982). Once the values of Tb and
DD have been determined, the rate and duration of
a process (e.g. moulting of arthropods, seed
germination, etc.) at any temperature (between Tb
and To) can be readily calculated (see Appendix 1,
Eqns 1 and 3).
Thermal time is not the only approach to
physiological time (e.g. Gillooly et al., 2001,
proposed a unifying theory linking size, temperature
and metabolic rate across the animal kingdom), but
it has proved a useful concept. A search of biological
abstracting services (CAB, Web of Science, BIOSIS)
using the terms ‘thermal time’, ‘degree days’ and
‘thermal constants’ produced several hundred
qualifying publications over the last 25 years.
However, the greater majority related to agriculture
and forestry. Thermal time has been used by applied
biologists to analyse the effects of temperature on
the germination of crop and weed seeds (Washitani
& Takenaka, 1984a,b; Steinmaus et al., 2000), rates
of leaf and inflorescence appearance and
development (Ellis et al., 1986, 1992; NeSmith,
1997; Granier & Tardieu, 1998; Yeh et al., 1999,
2000), potential productivity (Black & Ong, 2000;
Clifton-Brown et al., 2000), and determination of
optimum planting/harvesting/spraying dates (Wilson
et al., 1999; Fisher & Lieth, 2000; Steinmaus et al.,
2000). Thermal time has been used to model the
effects of climate change, both on plants (Pearson
et al., 1997) and their pathogens (Kaukoranta, 1996),
and the dynamics of the interaction between
pathogen and host (Mullens et al., 1995; Griffith et
al., 1996). Pathologists, especially entomologists
(Honek (1996b) lists 335 references to the thermal
time requirements of insects) have used thermal time
to determine and compare the requirements of the
different stages and species of various pests and
pathogens in relation to their biology (Dean, 1974;
Griffith et al., 1996; Honek, 1996a,b; Tzortzakakis
& Trudgill, 1996), epidemiology (Kaukoranta, 1996)
and control (Forcella & Banken, 1996; Soto et
al.,1999), and as a basis for risk assessment
(Lahtinen et al., 1988). The ability to apply thermal
time to the development of both pests and their plant
hosts makes it particularly useful when modelling
dynamic interactions (Ferris, 1976; Griffith et al.,
1996), including possible consequences of global
warming (Kaukoranta, 1996). Thermal time has also
been applied to other complex interactions, including
rates of soil organic matter decay and nitrogen
utilisation (Smith et al., 1998; Dejoux et al., 2000).
Despite its potential utility, thermal time has not
been widely used by ecologists and there have been
comparatively few thermal time studies applied to
natural systems. These include a model of the effect
of climate change on tree species distributions and
dynamics in northern Europe (Sykes & Prentice,
1996), and another describing the phenology of nine
wild plant species in relation to their use as climate
indicators (Spano et al., 1999). Others related to the
effects of thermal stratification in a marine
environment on copepod abundance and diversity
(Valdes & Moral, 1998), and to effects of incubation
temperature on rates of embryonic development in
aquatic insects (Gillooly & Dodson, 2000). A
particularly timely application was modelling the
effects of climate change on the distribution of
poikilothermic animals close to their climatic limits
(Thomas et al., 1999).
This review essay provides references to, and
examples of, a linear relationship for various
processes of development involving only
differentiation (= a change of state e.g. seed
germination, egg hatch, metamorphosis) but also
shows that a linear relationship may sometimes be
applied to processes involving growth (= increase
in dry mass), such as development to maturity. We
show that low T b values (< 8°C) are typically
associated with cool, and high values (> 12°C) with
warm environments, and that the DD value reflects
both the amount and rate of differentiation and/or
growth. Based on a re-analysis of several data sets,
we propose that the adaptation of poikilothermic
animals and plants to their thermal environment
involves a trade-off between the values of Tb and
DD whereby one increases as the other decreases. It
is evident that the DD requirement for development
to maturity has implications for resource
requirements and we show that plants and animals
have different strategies for responding to resource
 Thermal time – concepts and utility 3

limitations. The value of this information is that it
provides a means of describing and comparing the
rates and durations of processes in, and the thermal
adaptations of, poikilothermic animals and plants.
A linear relationship between the rate of a process
and temperatures between Tb and To is fundamental
to the thermal time method. However, until now there
has been no explanation for such a linear relationship
(the relationship would be expected to be curvi-linear
based on Van’t Hoff’s law, whereby rates of
development approximately double for every
increase of 10°C). Crucially, therefore, we offer a
physiological explanation for rates of development
being linearly related to temperature. Overall, we
propose that the thermal time approach has wide
utility because it applies to both plants and many
invertebrate animals, and because the values of Tb
and of DD for development to maturity provide a
basis for characterising developmental and
ecological strategies.
Thermal Time – Methods and Limitations
external stimuli (e.g. to overcome dormancy or
diapause), and the external resources required for
growth should be optimal or standardised. This essay
only relates to such active processes and stages, but
the study of the additional effects of factors such as
varying external resources are not precluded,
provided appropriate procedures and controls are
used.
The data on development duration and temperature
are the basis for calculating the thermal constants
for development (see Appendix 1). It is important
to note that the smaller the DD, the greater the slope
(a) of the linear part of the regression and that the
rate and duration of development at any given value
of Te (up to To) depends on the values of both Tb and
DD. Hence, in Fig. 2, a tropical species of root-knot
nematode (Meloidogyne javanica) has a smaller DD
requirement and a higher Tb than a comparable
temperate species (M. hapla).
Development Rate vs Temperature – Why is it
Linear?

Laboratory-based methods for assessing the Rates of development of poikilothermic species

thermal time requirements of poikilothermic are temperature-dependent because temperature
organisms have been described in numerous affects numerous physiological processes, including
publications (e.g. Covell et al., 1986; Leach et al., rates of diffusion and the degree of desaturation of
1986; Gillooly & Dodson, 2000; Fig. 1). All such membrane lipids. However, it seems probable that
studies are based on the Celsius rather than the
Kelvin (absolute) scale because the former is more
biologically relevant. For this reason, the Celsius
scale is also used here. In thermal time studies the
duration of the process being studied is accurately
measured at a series of precise constant temperatures,
preferably including at least one or two values close
to or beyond the extremes of the temperature range
the organism might naturally experience. Precise
start and end points are essential – in seed
germination studies the chosen end point is often
Rate (1/days)

50% of the seed producing a visible radical (1 mm)

(e.g. Ramin, 1997).
Development to maturity can be thought of as
having two components – differentiation and growth
(Van der Have & de Jong, 1996). Differentiation,
which does not require external resources, has been
most studied, but thermal time information can also
be applied to processes involving growth, which do
require external resources. To determine accurately
when the end point has been reached (i.e. the seed
has germinated, the egg has hatched, the insect has
matured etc.) the time interval between observations
should be small and, ideally, be varied in relation to
temperature and duration. The aim is to obtain
precise data on which to base a linear regression as
the estimates of Tb and DD are both derived from Temperature (°C)
the slope of that regression (a) and, therefore, are Fig. 1. Relationship between temperature and
inversely correlated. The process under study must development rate for one generation of the rhabditid
be continuous, it must be independent of any other nematode Goodeyus ulmi (Leach et al., 1986).
 4 D L TRUDGILL ET AL.
enzymes are of central importance. The activity
profiles of the enzymes of different species reflect
adaptations to different environments, including
temperature (Somero 1986; Milanovic et al., 1989).
For example, in Colias butterflies the occurrence of
alleles of phosphoglucose isomerases with different
kinetics was correlated with temperature-related
behavioural differences (Watt et al., 1983). However,
Van’t Hoff’s law assumes an exponential relationship
between enzyme reaction rate and temperature
whereby a 10°C increase in temperature produces a
standard increase in rate – usually designated Q10.
By this “law”, which has a solid foundation in
physical chemistry, the response to Te (in °C) is
exponential rather than linear. Consequently, the lack
of a theoretical basis in enzyme kinetics for a linear
relationship between temperature and development
rate is a major factor deterring many from using the
thermal time model.
Schoolfield et al. (1981) went some way to
overcoming this objection by developing a
biophysical model that described a linear response
at intermediate temperatures, but the response still
Rate of development (1/number of days)
Temperature (°C)
Fig. 2. Relationship between temperature and duration
of one generation of a temperate (Meloidogyne hapla,
Tb = 8.25°C and DD = 554 °C days) and tropical (M.
javanica, Tb = 12.9°C and DD = 350 °C days) root-
knot nematode. Their rates of development are
identical at 21°C (where the regression lines intersect).
Below this temperature the temperate species has the
greater rate of development, and above this temperature
the tropical species has the greater rate (data from
Trudgill & Perry, 1994).
became non-linear towards the temperature
extremes. Alternative models with a mechanistic
basis are those of Arrhenius and of Sharpe &
Schoolfield (see Gutierrez, 1996). Arrhenius’s model
extends Van’t Hoff’s law by incorporating the
concept of activation energy whereby a temperature
increase acts not only to increase the kinetic energy
of the reactants, but is also required to overcome
the energy threshold (HA, ‘activation enthalpy’)
needed to form the activated molecular complex that
precedes a chemical reaction. The Sharpe-
Schoolfield model further extends the Arrhenius by
assuming three states for molecules in a chemical
reaction: i) inactive due to low temperature, ii) active,
and iii) inactive due to high temperature (Sharpe &
De Michele, 1977; Schoolfield et al., 1981).
To reconcile the linear model with the Sharpe/
Schoolfield mechanisms, we propose that the linear
relation between Te and rate of development is the
result of progressive inactivation of enzymes (i and
iii above) as Te approaches To or Tb. This will have
the effect of turning down both ends of the reaction
curve, diminishing the increasing acceleration effect
implied by Van’t Hoff’s law and the Arrhenius
model. This process is clearly evident as T e
approaches and then exceeds To when a progressively
increasing proportion of enzyme molecules become
inactive, resulting in a progressive diminution in the
rate (Fig. 1), eventually decreasing to zero at Tm (the
value of Te when all the molecules are inactivated).
Relation to Thermal Environment and Trade-
off Between Tb and DD
Thermal constants provide practically and
ecologically useful information. Furthermore, as
they differ, even between related species (because
of adaptation of each to its environment), their study
reveals various aspects of temperature adaptation.
Differences in Tb
The temperature ranges where growth and
development of poikilothermic species may
potentially occur are reflected in their values of Tb,
To, and Tm (Scholander et al., 1953). Pritchard et al.
(1996) gave a range from –5 to > 15°C as the
estimated Tb values for egg development of 40
populations of aquatic insects. Tb values below 0°C
were assigned to the eggs and larvae of several
species of stonefly (Plecoptera) (Brittain & Mutch,
1984; Brittain et al., 1984; Mutch & Pritchard, 1986)
and the Antarctic beetle Hydromedion sparsutum
(Meyer-Arndt, 1984). Even though little
development could occur below 0°C, the occurrence
of such low estimated Tb values indicates the extent
of low-temperature adaptation. There is also
abundant evidence that tropical species have higher
 Thermal time – concepts and utility
Tb values than equivalent temperate species (e.g.
Angus et al., 1981; Honek, 1996b). The widespread
construction of glasshouses in temperate regions is
a practical demonstration of the higher temperature
requirements of plants from warmer latitudes; and
pests from similar latitudes also flourish in such
glasshouses. From published data (n = 335), Honek
(1996b) estimated that the mean Tb values for the
differentiation of insect eggs from temperate (40–
60 oN or S) and tropical (0–23 oN or S) regions were
8.7°C and 12.9°C respectively (significantly
different P < 0.01).
Trade-off between Tb and DD and the competitive
value it confers
T b defines the lower temperature limit for
development and the reason for temperate species
having low values is self-evident. However, the
reason for T b being higher in tropical than in
temperate species is less obvious and presents a
conundrum, as the effective temperature available
for development (Te minus Tb, Appendix 1, Eqns 2
and 3) decreases as Tb increases (except where Te >
To; Honek & Kocourek, 1990; Trudgill, 1995a). In
this section we provide further evidence to support
the suggestion of Honek & Kocourek (1990) and
Trudgill (1995a) that the answer to this conundrum
lies in a trade-off between Tb and DD. We further
suggest that the value of Tb and the relative rate of
the trade-off between Tb and DD modify fitness and
thus influence the outcome of competition between
related species and their distributions. We examine
several data sets, five of them in considerable detail,
to reveal examples of adaptive trade-offs between
Tb and DD and suggest that the rate of trade-off
between Tb and DD is such that, as Te increases, it
tends to favour tropical species. The evidence we
provide is based on data sets for processes only
involving differentiation. We have avoided analysing
data for processes involving growth because the DD
requirement may be further influenced by other
factors (e.g. differences in adult size, resource
availability etc.).
A complication when comparing the Tb and DD
requirements of species from different latitudes is
that the data for individual species often come from
Tb (°C)
different studies using different methods and over
different temperature ranges. However, there are
exceptions. Angus et al. (1981) compared the
germination rates of seed from tropical and
temperate crops in field trials at different sites in
Australia. They found that the seed of the temperate
crops germinated at lower temperatures, but had a
greater DD requirement for germination than those
of the tropical crops (e.g. Tb and DD for germination
of barley seed were c. 2.6°C and 80 °C days
compared with c.16°C and 20 °C days for sesame).
Similarly, in laboratory studies, Qi et al. (1999)
5
compared five temperate and six tropical legumes
and demonstrated that the Tb for germination was
consistently less for the temperate (mean 1°C) than
the tropical (mean 9°C). All the temperate legumes
had high DD requirements (mean 152 °C days) but,
whilst the DD requirements of the tropical legumes
were generally less (mean 87 °C days), they were
more variable. Craufurd et al. (1996) conducted two
experiments studying the germination of 12 cowpea
genotypes from West Africa and the estimated values
of Tb were highest, and those of DD generally lowest,
in the genotypes originating from close to the
equator. Based on a linear regression (Fig. 3; r2 =
0.63, P < 0.001), DD decreased from 50 to 23 °C
days as Tb correspondingly increased from 6.5°C to
10.3°C. However, this inverse relationship was not
observed in a third experiment with a wider
geographical range of genotypes.
The cowpea data of Craufurd et al. (1996; Fig. 3)
was almost as effectively described by a power
function as by a linear regression (r2 = 0.61 and 0.63
respectively). A linear regression indicated there was
> 2-fold range in the DD requirement (50 to 22 °C
days) compared with a 1.5-fold range for Tb (6.9°C
to 10.4°C). With these values, the most warm-
adapted genotype will germinate more rapidly than
the most cold-adapted at all values of Te > 13.1°C.
Based on data sets for many insect species Honek
& Kocourek (1988, 1990) and Honek (1996a)
suggested an inverse relationship between the values
of Tb and DD for the differentiation of eggs and of
pupae. Honek (1996b) recalculated the thermal
requirements of 335 species in relation to their origin
and demonstrated that, despite considerable
variation, Tb tended to decrease with increasing
latitude of origin whereas the value of DD tended to
increase. The data sets of Honek (1996a) are
relatively variable because of the large number of
different experiments and unrelated species
involved, but an analysis of the data for the
differentiation of insect pupae shows that the
DD (°C days)
Fig. 3. Relationship between Tb and DD for 12 cowpea
genotypes from West Africa. Data from Craufurd et
al. (1996), Expts 1 and 2. A linear regression was fitted
(y = –0.14x + 13.5; r2 = 0.63).
6 D L TRUDGILL ET AL.
relationship between Tb and DD is best described
by a linear regression (r2 = 0.24). Despite the
variability, the relationship is highly significant (P
< 0.001) and indicates a range in the DD requirement
from 400 to 20 °C days and for Tb of 3.1°C to 13.5°C.
From this it can be calculated that at Te = 14°C and
22°C the most cold-adapted species will require 34
and 21 days for egg hatch compared with 40 and 2.4
days respectively for the warm-adapted.
Li (1998) also reported a strong, inverse
relationship between T b and DD for egg
differentiation in published data for 17 species of
spiders from different environments. A curve fitted
to this data using a power function (Fig. 4; r2 = 0.74,
P < 0.001) showed that the value of DD ranged from
64 to 217 °C days (× 3.4 range) whereas the
corresponding values of Tb ranged from 15.7 to 5.6°C
(× 2.8 range). The competitive advantage as Te
increases of a greater rate of change of DD as
compared to Tb is demonstrated below by using the
extremes of the ranges as examples of a “temperate”
and a “tropical” species. With Te = 18°C, 21°C and
24°C, egg hatch will take 17.5, 14.1 and 11.8 days
respectively for the “temperate” species compared
with 27.8, 12.1 and 7.7 days for the “tropical”
species. The “tropical” species will have a more rapid
rate of development than the “temperate” at all
values of Te > 19.9°C, whereas the reverse will apply
below 19.9°C.
Variations in the Tb vs. latitude relationship were
observed by Honek (1996b) and by Li (1998) and
this is partly because geographic origin is only
loosely related to the microclimate of the habitat and
the season in which organisms develop. This is
demonstrated by Van Straalen (1994) who analysed
published data on the relationship between
temperature and the duration of egg differentiation
of 40 species of Collembola. A re-analysis of his
data showed that the 95% confidence limits for the
data points for each species typically overlapped
over only a small part of the total range, strongly
Tb (°C)
Tb (°C)
DD (°C days)
Fig. 4. Relationship between Tb and DD for 17 species
of spider (Arachnida). Data from Li (1998). Line fitted
using a ‘power’ function (y = 533.48x–0.847; r2 = 0.74).
suggesting that they are distinct and different. Van
Straalen (1994) concluded that differences in their
rates were associated more strongly with their habitat
than with latitude. In warm environments (> 15°C),
the eggs of above-ground species developed more
rapidly than those that lived below-ground, or in
caves. The data sets of Van Straalen (1994) are reused
here to estimate the values of Tb and DD for each
species (typically r2 > 0.9) and a strong negative
correlation was demonstrated between Tb and DD.
A logistic function gave a better fit to the data (r2 =
0.70; Fig. 5) than a power function (r2 = 0.56) and
variation in Tb (–3.8°C to 11.4°C) is large, as is the
corresponding range for DD (650 to 50 °C days).
Consequently, it can be calculated that the rate of
hatch of the eggs of warm-adapted Collembola
species will be greater than that of the most cold-
adapted for all values of Te > 12.7°C (e.g. at Te =
18°C the cold-adapted and the warm-adapted species
will require 29.8 and 7.6 days respectively). A
subsequent study (Birkemoe & Leinaas, 2000) of
the differentiation of the eggs of an arctic species of
Collembola (Hypogastrura tullbergi) suggested
values of Tb and DD (–1.32°C and 295 °C days
respectively) consistent with the regression in Fig.
5.
Differences in T b and DD may also reflect
differences in the time of year when species are most
active. Anderson & Coleman (1982) speculated that
four species of bacterial feeding nematodes were
able to cohabit because they had different
temperature ‘niche breadths’. Support for their
hypothesis came from Ferris et al. (1996) who
observed Tb and DD differences in six species of
bacterial feeding nematodes that all came from one
site. Their Tb values ranged from 0°C to 14.8°C and
the corresponding values of DD for egg
DD (°C days)
Fig. 5. Relationship between T b and DD for
embryogenesis in 38 species of Collembola. The data
is the same as that analysed by Van Straalen (1994).
The data were pooled where more than one study was
done on a species. A log regression line was fitted to
describe the relationship between T b and DD (y
= –5.922logx + 34.7; r2 = 0.7).
 Thermal time – concepts and utility
differentiation ranged from 36 to 10 °C days and for
development to maturity from 173 to 35 °C days
respectively. Fitting a ‘power’ function showed that
DD was inversely correlated with Tb (r2 = 0.91 and
0.63, and P < 0.001, < 0.05 for development of eggs
and development to maturity respectively).
Consequently, at Te = 16°C the most cold-adapted
species will hatch in less than half the time (2.25
days compared with 5 days) than the most warm-
adapted, whereas at Te = 22°C the warm-adapted
species will hatch in 1.25 days compared with 1.62
days for the cold-adapted. Such wide ranges in Tb
and DD will potentially reduce competition between
nematodes adapted to the different seasons and soil
horizons, but interpretation of the relationship for
development to maturity is complicated by
differences in adult size and behaviour.
A slightly unusual, independent confirmation of a
trade-off between Tb and DD in the development of
the eggs of aquatic insects comes from Pritchard et
al. (1996). Instead of calculating the Tb for each
species, they used 0°C as a universal Tb value when
calculating the DD requirements of 95 species over
a range of values of Te. They then regressed the DD
requirements against Te and used the slope of the
(linear) reaction norm as an index of adaptation to
low or high temperatures. Using this approach it can
be readily calculated that, if there is a trade-off, as
Te increases the DD requirement will gently increase
for species with a true Tb < 0°C whereas it will
decrease for those with a true Tb > 0°C. The results
confirmed a trade-off as the species adapted to cold
conditions had a positive (linear) regression, whereas
for the more warm-adapted species there was a
negative association that became more pronounced
in proportion to the degree of adaptation. Overall,
the cold-adapted species had greater DD
requirements and much lower temperature ranges
than the warm-adapted species.
These independent examples, derived from
different plant and invertebrate taxa indicate a
universal occurrence of a relationship between Tb
and DD. Explanations for differences in Tb and DD
have mostly focused on the phenological and
evolutionary consequences of the temperature
responses, e.g. the necessity to synchronise the
various life-stages with the seasons (Gilbert &
Raworth, 1996), and an understanding of the
underlying physiological mechanisms has been
lacking.
Mechanisms
The proximate reasons for the variations in Tb, and
for the trade-off between Tb and DD have been given
little attention. We attempt an explanation for the
trade-off and suggest that the answer must be sought
in the fact that temperature affects not only the rate
of chemical reactions, but also induces
7
conformational changes in biological systems.
Support for this hypothesis comes from Van Straalen
(1994), who used a modified Sharpe-Schoolfield
equation to estimate the kinetics of a hypothetical,
rate-controlling enzyme (see also Van der Have &
de Jong, 1996) and demonstrated a positive
correlation between HA (activation enthalpy – the
energy required to change the state of the reactants
from inactive to active) and rate of egg development
at 15°C of 38 species of Collembola. He concluded
that increasing HA was associated with more efficient
use of each unit of temperature increase (i.e. with
increasing a in Eqn 1 (Appendix 1), and therefore
decreasing DD). Regressing the estimated values of
Tb and DD (Fig. 5) against the comparable estimates
of HA showed that there was a significant negative
correlation between HA and DD (r2 = 0.47; P < 0.01)
and a positive correlation with Tb (r2 = 0.43; P <
0.01) (Fig. 6a and b). These results support the view
that the apparent trade-off between Tb and DD has a
basis in the thermal adaptation of enzymes.
Other Factors Influencing DD Requirement
We have shown how and why the DD requirements
may be inversely related to Tb. However, DD also
differs between species with a similar Tb. This
variation is due to innate differences in rates of
differentiation and development.
Differences in rates of differentiation and
development
The DD requirement for insect egg hatch range
from < 20 to > 500 °C days (Honek, 1996a, 1999).
For insect eggs with a Tb of c. 9°C to 10°C, Honek
(1996a) reported differences in DD requirements for
hatch ranging from < 10 °C days (e.g. Anaphes
flavipes) to > 200 °C days (e.g. Typhlocyba
froggatti). This variation was only weakly correlated
with egg mass. It was apparently due to species-
specific differences in rates of egg development
(Honek, 1996a). Similarly, the DD requirements for
embryogenesis in nematodes range from < 10 to >
260 °C days (Trudgill, 1995b). Eggs of the free-
living nematode Caenorhabditis elegans (T b =
5.0°C) require 8.2 °C days to hatch (Ferris et al.,
1996) whereas those of the plant parasite Xiphinema
diversicaudatum (Tb = 7.6°C, Trudgill, 1995b)
require 270 °C days to hatch. The much greater rate
of development of C. elegans compared with X.
diversicaudatum must reflect large differences in
their metabolic rates. The differences are so great
that C. elegans can pass through several generations
(DD requirement for one generation = 43 °C days;
Trudgill, 1995b) in the time required for the eggs of
X. diversicaudatum to hatch.
 8 D L TRUDGILL ET AL.

a) b)
HA (kJ mol–1)

HA (kJ mol–1)
DD (°C days) Tb (°C)
Fig. 6. Regression of the activation enthalpy (HA) of a hypothetical rate-controlling enzyme for the embryogenesis of
38 species of Collembola (data from Van Straalen, 1994) and a) the value of DD and b) Tb calculated from the same
data. A log regression line was used for DD (y = –21.5logx + 183.5; r2 = 0.47), and an exponential line was fitted to
the data for Tb (y = 60.05 e0.039x; r2 = 0.43).

Development to maturity
As is demonstrated in Figs 1 and 7, linear
Rate (1/days)

relationships between Te and rate can also apply for

multi-step processes that involve both differentiation
and periods of growth (e.g. development to
maturity). However, this depends on there being a
linear relationship for each of the component stages
and processes (Fig. 7), and the greater the number
of developmental steps and the amount of growth,
the greater the DD (Honek, 1999). For arthropods,
the summation of the DD requirement for
development to maturity is simplified by the
conclusion, derived from an analysis of data for
seven species of mites and 342 species of insects,
that T b is usually the same for each of the
developmental stages within each species population
(Jarosik et al., 2003).
Size at maturity
Size at maturity is a function of the rate and
duration of growth, and large size at maturity implies
a long generation time and a correspondingly large
DD requirement. However, various other factors
influence the DD requirement associated with
growth. It is influenced by the quality and availability
of the resources required for growth, and the
efficiency with which those resources are used for
growth. Honek (1996a) observed that differences in
DD requirements for insects to become adult were
associated more with differences in larval
requirements than with those for the eggs or pupae.
Honek (1999) showed that this variation in DD was
Temperature (°C)
Fig. 7. Relationship with temperature for the
development of eggs, nymphs and adults of Nysius
vinitor. Redrawn from Kehat & Wyndham (1972).
influenced by i) the total increase in mass (P <
0.001), ii) taxonomic group (P = 0.124 to < 0.001),
and iii) trophic specialisation (P < 0.001) – predators
had smaller DD requirements than herbivores (P <
0.005), presumably a reflection of the digestibility
and/or nutritional quality of the different foods
(Chapman, 1998). Life style also influences food
utilisation e.g. insects that fly have higher metabolic
rates, and expend more energy than less active
species, both when active and at rest (Reinhold,
1999). Consequently, DD requirements for
development to maturity ranged from < 100 °C days
in some Aphis spp. (Tb c. 7°C–10°C) to > 4000 °C
days in Periplaneta fuliginosa (Tb c. 12°C) (Honek,
1996a).
Large differences in mature mass do not signify
exactly equivalent differences in DD because growth
 Thermal time – concepts and utility
in plants and animals tends to be exponential rather
than linear, and is well approximated by power laws
(Gillooly et al., 2001; Charnov & Gillooly, 2003).
For example, Ferris et al. (1996) observed that, when
cultured on bacteria, the mature mass of the
nematode Cruznema tripartitum (Tb 10°C) was 12-
times greater than that of Caenorhabditis elegans
(Tb c. 5°C). However, the DD requirement for
development to maturity of C. tripartitum was 55
°C days compared with 31 °C days for C. elegans.
A comparative analysis of their growth showed that,
up to 31 °C days, the two species were of a similar
size and that most of the greater mass of C.
tripartitum was accumulated between 31 and 55 °C
days (Ferris, personal communication). The rapid
growth of C. tripartitum meant that it required only
20 °C days per µg increase in mass compared with
1300 °C days per µg for Cephalobus persignis, the
smallest species in the study (Ferris et al., 1996).
Effects of sub-optimal resources on DD
requirements and size
Sub-optimal availability of the resources required
for growth may also affect the DD requirement and
mass at maturity. However, the effects differ between
animals and plants. Plants, especially annuals, tend
to have a conserved DD requirement for
development to maturity that is largely unaffected
by the availability of resources and rates of growth.
Consequently, when resources are scarce, mature
plant size and crop yields are greatly decreased
(sometimes > 100-fold; Squire, 1990; Atkinson,
1994) but the DD requirement is unchanged. In
contrast, in insects, food scarcity increases the DD
requirement by reducing the rate of development,
thereby increasing the feeding duration of each larval
stage, and sometimes the number of larval stages
(Mukerji & Guppy, 1970; Honek, 1987; Chapman,
1998). Even so, adult size may be reduced by up to
two thirds because the increased duration of feeding
does not fully compensate for the decreased rates of
food intake and the increased maintenance
requirement. Growth and development of armyworm
(Pseudaetia unipuncta) and of the spider Linyphia
triangularis were linearly related to rates of food
intake with consequential effects on mature size,
survival rates and fecundity (Turnbull, 1962; Mukerji
& Guppy, 1970). The quality of the food will also
affect the DD requirement and mature size e.g. black
faced leaf hoppers (Graminella nigrifrons) grew
larger on maize than oats (Larsen et al., 1990).
Effects of temperature on mature size
Within the range Tb to To body size/mass typically
decreases as Te increases. This is because rates of
differentiation are determined by thermal time but
rates of resource acquisition and growth are also
influenced by calendar time. In annual plants the
9
DD requirement for development to flowering is
often fixed with the result that mature size decreases
as Te increases (Atkinson, 1994). Consequently, yield
in temperate cereals is decreased in years with warm
summers because the crop matures more rapidly,
with a corresponding decrease in the duration of light
interception (Atkinson & Porter, 1996).
Low temperatures have the opposite effect and
mature size is often increased. In a review of the
effect of temperature on the size of animals, plants,
protists and bacteria, mature size increased as
temperature decreased in 91 of 109 studies
(Atkinson, 1994). This phenomenon is particularly
apparent in insects, e.g. black faced leaf hoppers
(Graminella nigrifrons) became c. 25% heavier
when grown at 17°C compared with 27°C (Larsen
et al., 1990). Various explanations have been offered
for this effect, including the use of a biophysical
model (Van der Have & de Jong, 1996) to show that
differences in a (the temperature coefficient for
growth and differentiation) will lead to adult size
varying with T e. However, in this model size
decreased sharply at both temperature extremes.
Gilbert (1984) and Gilbert & Raworth (1996) went
one step further and, based on the effects of rearing
temperature on the size of Pieris rapae, proposed
that variations in adult size were due the values of
Tb for differentiation being higher, and of a being
lower than that for growth. They proposed a
functional explanation suggesting that, as fecundity
is related to adult size, it is advantageous for
multivoltine insect species to maximise fecundity
early in the year. But, as competition and predators
increase later in the year, reducing the generation
time becomes most advantageous.
Where vital functions (e.g. feeding) are impaired,
the relation between body size and temperature is
sometimes reversed at values of Te close to Tb. This
is evident in some insects where maximum adult
size is achieved at median temperatures (David et
al., 1994).
Decreasing the DD Requirement
As is demonstrated by C. elegans, and by many
other species with short generation times, rapid
development is a consequence of a small overall DD
requirement. Decreasing the number of
developmental steps can also reduce the DD
requirement. Tylenchid nematodes undergo their first
moult in the egg, in Meloidogyne spp. (root-knot
nematodes) the third and fourth juvenile stages are
also non-functional, and in the dorylaim nematode
Xiphinema americanum the number of juvenile
stages has been decreased from four to three
(Halbrendt & Brown, 1992). Many Meloidogyne
spp. are parthenogenetic, eliminating the time
required for mating. Similarly, aphids have a small
10 D L TRUDGILL ET AL.
DD requirement for development to maturity (mean
127 °C days; Honek, 1996a). This is achieved by
being parthenogenetic, by larval development
beginning within the body of the mother even before
her moult to adult, by producing live young (all of
which allows ‘telescoping’ of generations; Dixon,
1987), by small size, and by feeding almost
continuously.
Discussion and Conclusions
Thermal time provides a means of determining
and comparing rates of development of
poikilothermic organisms at temperatures within the
range Tb to To. It has wide utility because it applies
to many plants and invertebrate animals. Differences
in Tb indicate when organisms can become active in
a variable thermal environment and, together with
To and Tm, their temperature ranges. In particular,
the values of, and trade-off between Tb and DD,
provide insight into the adaptation and the ecological
strategies of organisms in relation to related species
and their thermal environment.
The approach to thermal time described here
differs from that of the unifying model of Gillooly
et al. (2001) in four ways. Firstly, our approach
differs in terms of scale. Gillooly et al. (2001)
assume a universal temperature relationship over the
whole of the animal kingdom. Consequently,
differences within taxa are averaged out, whereas
our approach focuses on such differences because
of their agricultural and ecological importance.
Secondly, our approach applies only to
poikilothermic invertebrates rather than to all
animals. Thirdly, it can also be applied to plants.
And fourthly, based on enzyme kinetics, Gillooly et
al. (2001) assume that the rate of a process will
increase exponentially rather than linearly with
temperature. Furthermore, having seen an early draft
of this paper, Charnov & Gillooly (2003)
subsequently proposed that those linear relations that
have been described are ‘linear approximations of
an exponential response’. However, a linear
relationship between temperature and rate of
development is fundamental to the thermal time
model. We believe that there are too many examples
of a linear relationship between rate of development
and Te for all of them to be ‘linear approximations’
as proposed by Charnov & Gillooly (2003).
Crucially, therefore, we provide an explanation for
the linear relationship by suggesting that the
proportion of enzyme molecules in an active state
progressively decreases as the temperature
approaches Tb and To. We also demonstrate a negative
relationship between the estimates of HA for a
hypothetical, rate limiting enzyme and DD, and a
positive relationship with Tb. Such a relationship can
be predicted on theoretical grounds and, if correct,
has important practical implications (e.g. it has
implications for the effectiveness of plant breeding
aimed at adapting genotypes to different thermal
environments). But, whilst these results help to
provide a theoretical basis for the thermal time
approach, in practice poikilothermic organisms must
function as a whole and their responses to
temperature are unlikely to be dependent on a single,
rate-limiting enzyme.
Before discussing the ecological consequences of
the linear relationship we need to consider the
confounding factors originating from experimental
error. Estimates of DD and Tb are both derived from
a (the slope of the regression) and, consequently,
are inversely correlated. Hence, an over-estimate of
a will result in an over-estimate of T b and a
corresponding under-estimate of DD (and vice versa
– see Appendix 1). We explored the effects of such
experimental errors in a series of simulations and
the results (not shown) indicate that the trade-off
between DD and Tb observed in Figs 3 to 5 is much
greater than expected from correlated measurement
errors. In particular, in the simulated results, the
estimates of Tb varied proportionately much more
than that of DD, whereas in the biological data the
reverse was observed. Additionally, we were able
to demonstrate that the ranges of some of the data
sets we examined (e.g. for Collembola) were distinct
and therefore the differences were unlikely to be due
to error.
Based on a linear relationship, we have shown that
there is an inverse relationship between Tb and DD
associated with latitude and/or habitat that adapts
each species to its thermal environment (Figs 3 to
5). A trade-off between Tb and DD, especially one
where the rate of change of DD is greater than that
of Tb, makes physiological and ecological sense
because it leads to each species and its ecological
strategy being adapted to its particular thermal
environment. This is demonstrated by species of
bacterial-feeding nematodes that co-existed at one
site (Ferris et al., 1996), whereby differences in
thermal requirements appear to help position the
development of each species in relation to that of
the other species within the community. Ferris et
al. (1995) linked physiology, thermal time and
ecology by relating rates of development to those of
CO2 evolution for eight species of bacterial-feeding
nematodes grown at five temperatures. They showed
that, at each temperature, unit metabolic rates varied
with the thermal adaptation of the species and
concluded that such differences may contribute to
the changes in predominance of species at different
times and soil depths.
Our analyses of the trade-off between Tb and DD
are based on comparisons between related species.
Within species, the DD requirement for development
to maturity may differ due to differences in size and/
 Thermal time – concepts and utility
or growth rates, but much of the available evidence
indicates Tb is less variable. Jarosik et al. (2003)
observed that Tb was usually the same for each
developmental step within a species of mite and
insect. Gomi (1996) examined the differentiation in
populations in Japan of the fall webworm
(Hyphantria cunea), an introduction from North
America. Populations in the south-west had shifted
from two (bivoltine) to three (trivoltine) generations
per year. Tb values were similar for both bi- and
trivoltine populations, but the results indicated that
in the trivoltine population the DD requirement for
development to maturity had decreased (particularly
for the larval stages). This change was also
accompanied by a change in the photoperiodic
response controlling pupal diapause (Gomi &
Takeda, 1996). Stacey & Fellows (2002) observed
no significant differences in T b within three
populations of Thrips major, three of T. tabaci or
two of Frankliniella occidentalis, but there were
significant differences in body size. Using published
data, they found a negative relationship between Tb
and DD for F. occidentalis and T. tabaci, and
suggested that a trade-off between Tb and DD may
constrain adaptation to local conditions. Even so,
Craufurd et al. (1996) reported differences in Tb in
cultivars of cowpea, and correlated differences in
DD in two of three experiments, and Mohamed et
al. (1988) observed differences in Tb, To and Tm in
four cultivars of groundnut and four of pearl millet.
Size at maturity is of practical and theoretical
interest because of its relationship to crop yields, to
generation time, to the fecundity of weeds and pests,
and to the relative performance of interacting
components of ecosystems. We have reported how
the availability of resources affects size at maturity
and why, because of their conserved DD
requirement, plant size may vary greatly. This is of
major importance to agriculture because of its
implications for crop yields. However, in most
invertebrate animals differentiation to the next larval/
juvenile stage depends, at least partly, on an increase
in mass and, when resources are limiting,
development is prolonged allowing more time for
feeding. Consequently, adult size varies within
narrower limits than for plants. Temperature has a
different influence on size. Increasing temperatures
tend to decrease mature size in many plants and
invertebrate animals (Atkinson, 1994), probably
because as Te increases the rate of differentiation and
development tends to increase proportionally faster
than the rate of growth, with the result that the time
available for resource capture is decreased.
The thermal time model applies only to organisms
during their active stages and our analysis is far from
comprehensive (e.g. the range T o –T m is not
considered). Tolerance of temperature extremes is
likely to be a major factor determining the ranges of
11
many species, water availability in relation to
transpiration demand is an important factor for
plants, pore space availability is important for soil-
dwelling nematodes, etc. Also, although the thermal
time model applies equally to aquatic organisms and
to those that live above- and below-ground, many
above-ground organisms are able to increase their
body temperature using radiant (solar) heat or by
activity. For above-ground species, Te frequently
varies greatly and, for periods, may be below Tb or
above To. Such seasonal or diurnal variations in Te
complicate the interaction between organisms and
their environment and, in some species, possibly
because of heterogeneity, there may be a lack of
linearity close to Tb that could be important early in
the growing season and when modelling dynamic
processes e.g. arthropod population dynamics
(Baker, 1972; Stinner et al., 1974; Diekkruger &
Roske, 1995). The ecological strategies of
poikilothermic species are further fine-tuned by
many other factors including photoperiodism,
dormancy and diapause that may be much more
important than temperature in determining onset of
activity, or development. Physiological condition
also has an influence on rates of processes (e.g. old
seed with reduced viability will germinate more
slowly than new seed), and heterogeneity,
particularly in DD requirements for certain
processes, is probably widespread (Trudgill et al.,
2000). Consequently, thermal time information is
most valuable when used in conjunction with
knowledge of the many other relevant environmental
and biological factors.
Information on thermal constants helps provide
insights into the position of species within
communities. Values of Tb and DD for each stage in
a life cycle define time to reproduction and longevity
at any given temperature. If size at maturity is
known, then relative rates of growth and their
resource requirements can be estimated. Pachepsky
et al. (2001) proposed that in natural communities
there is a trade-off between time to reproduction (i.e.
DD) and fecundity that sustains diversity and
governs the form of the relative abundance and
distribution. Hence, thermal time information has
value as a basis for characterising ecological
strategies, including modelling the relative growth
rates of interacting components of ecosystems – e.g.
Griffith et al. (1996) used it to model the interaction
between an endoparasitic nematode and its clover
host.
Throughout this paper we assume that the thermal
characteristics of species have been honed by
selection to maximise their physiological fitness in
relation to the thermal environment to which they
are adapted. We suggest that the linear thermal time
model has wide relevance amongst invertebrates and
plants and is conceptually and practically useful. The
12 D L TRUDGILL ET AL.
linear relation between temperature and rate
simplifies the mathematics associated with
calculating durations, and is the basis for estimating
the cardinal values (Tb, To, DD). It has numerous
applications e.g. agriculturalists have used thermal
time information to schedule sowing and harvesting
and to assess the risks posed by the accidental
introduction of pests (e.g. Lahtinen et al., 1988).
Such thermal time analyses demonstrate that the
population dynamics of many species are sensitive
to small differences in temperature, especially in
geographical regions close to the edge of their range.
Consequently, global warming perhaps provides the
greatest incentive for agriculturalists and ecologists
to utilise thermal time.
Acknowledgements
Drs H Ferris for supplying data on nematode sizes
and rates of development, G Squire for his
encouragement and support, D Mackerron and B
Marshall for help with mathematical modelling, and
C Scrimgeour for discussing enzyme kinetics.
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