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Thermal preferences and effects of temperature on fitness parameters of an endemic Argentinean tarantula
(Grammostola vachoni)
Journal: Canadian Journal of Zoology
Manuscript ID cjz-2019-0180.R1
Manuscript Type: Article
Date Submitted by the Author: 09-Oct-2019
Complete List of Authors: Schwerdt, Leonela; CONICET Bahia Blanca, de Villalobos, Ana Elena; Centro de Recursos Naturales Renovables de la Zona Semiarida, CONICET-UNS; Pérez-Miles, Fernando; Facultad de Ciencias, Universidad de la República, EntomologíaFerretti, Nelson; INBIOSUR
Is your manuscript invited for consideration in a Special
Issue?:Not applicable (regular submission)
Keyword: Endemic, Tarantula, Grammostola vachoni<i></i>, Locomotor performance, Thermal sensitivity
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Thermal preferences and effects of temperature on fitness parameters of an endemic
Argentinean tarantula (Grammostola vachoni)
1. Schwerdt L.
2. de Villalobos A.E.
3. Pérez-Miles F.
4. Ferretti N.
1. Centro de Recursos Renovables de la Zona Semiárida-CONICET. Bahía Blanca,
Argentina; [email protected]
2. Centro de Recursos Renovables de la Zona Semiárida-CONICET, Departamento de
Biología, Bioquímica y Farmacia. Universidad Nacional del Sur, Bahía Blanca,
Argentina; [email protected]
3. Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay;
4. Instituto de Ciencias Biológicas y Biomédicas del Sur-CONICET, Bahía Blanca,
Argentina; [email protected]
Corresponding author: Leonela Schwerdt. San Andrés 850, CERZOS, 8000 Bahía
Blanca, Buenos Aires, Argentina. Phone: +54 291 4566129. Email: lschwerdt@cerzos-
conicet.gob.ar
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Thermal preferences and effects of temperature on fitness parameters of an endemic
Argentinean tarantula (Grammostola vachoni)
1. Schwerdt L.
2. de Villalobos A.E.
3. Pérez-Miles F.
4. Ferretti N.
Abstract
Mygalomorphs depend on thermal micro-habitats for successful behavior but their
thermal biology is still poorly known. Grammostola vachoni Schiapelli and Gerschman,
1961 is an endemic tarantula from Argentina and it is listed as vulnerable in the IUCN
Red List. However, little is known about its biology, therefore, we attempted to explore
the thermal biology of juveniles and adult females of G. vachoni under laboratory
conditions. We characterized the preferred temperatures, evaluated the relationship
between temperature and locomotor performance and calculated the thermal sensitivity.
Individuals showed a peak of temperature preference and spent 40% of the total time at
25-29 ºC; we did not find any significant differences in preference between juveniles
and females. We found that locomotor performance is strongly affected by high
temperatures. Different sprint speeds of juveniles and females were found at 5 °C, 35 °C
and 40 °C. The highest thermal sensitivity was recorded in the lowest temperature range
and thermal sensitivity was lowest in the highest ranges. Our results are relevant under a
context of climate change, because thermal parameters constitute a useful tool to
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explore some possible effects of this change on body temperature and thus the
physiological performance and vulnerability of ectotherms, such as G. vachoni.
Key words: endemic; tarantula; Grammostola vachoni; locomotor performance; thermal
sensitivity.
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Introduction
Biological processes in ectotherms are dependent on body temperature, either directly or
indirectly, which depends on the environmental temperature. In fact, temperature
influences the individual fitness, abundance and geographical distribution of many
species of ectotherms (Huey and Berrigan 2001; Martin and Huey 2008; Taucare Ríos
et al. 2018). Some ectothermic organisms, e.g. female tarantulas, show scarce activity
outside their burrows, and even select those burrows according to the thermal
characteristics of the environment where they live (Riechert and Tracy 1975;
Hammerstein and Riechert 1988; Veloso et al. 2012; Alfaro et al. 2013). Therefore, as
these thermal condition may affect their periods of activity so, consequently, they would
reflect any major impacts on their behavior and ecology (Shillington 2002). Thermal
preferences may vary with the habitat, nutritional state, developmental stage and
acclimation history (Sinclair et al. 2016). Also, individuals within a population may
differ significantly in respect to these preferences, due to both genetic and non-genetic
factors (Kingsolver et al. 2013; Logan et al. 2014). For example, juveniles and males
tend to be more susceptible to thermal/desiccation stress than females, and this could be
due to the differences in body mass, as large spiders are generally less prone to
desiccation than small spiders (Savory 1964; DeVito and Formanowicz 2003).
To accurately describe the thermal biology of an ectotherm organism, the following
features are frequently used: i) thermal preference, i.e. the temperature that an organism
chooses over a range of available temperatures (Light et al. 1966; Stork 2012); ii)
critical thermal limits, i.e. extreme temperatures above which, individuals are not
capable of functioning normally (Hutchison 1961); and iii) locomotor performance, i.e.
the measurement of mobility (e.g.: endurance, sprint speed, strike speed) over a range of
temperatures (Stork 2012).
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These measurements are acquired in different ways, e.g., the temperature value of
thermal preference arises from a gradient selected by organisms and kept over a period
of time. Also, the critical thermal limits are obtained from a thermal performance curve
(TPC) (Huey and Kingsolver 1989; Alfaro et al. 2013), allowing an evaluation of the
effects of body temperature on organismal-level performance or fitness (Huey and
Slatkin 1976). These critical thermal limits are the points at which physiological
performance falls to zero (Woodin et al. 2013). Finally, the locomotor performance can
be measured through the thermal sensitivity, as changes in the whole animal’s
performance that are reflected in changes in the reaction rates of the metabolic
processes involved (Arnold 1983; Stork 2012). Furthermore, locomotor performance is
dependent on the metabolic processes (Arnold 1983) and the factor by which metabolic
processes change over a given range of temperatures is known as the Q10 (Hegarty
1973; Watson 2008). Therefore, evaluation of the Q10 for locomotor performance allows
to estimates the thermal sensitivity of performance and metabolism (Stork 2011).
Understanding the physiological responses of organisms to temperature is of high
priority due to the global climate change events and their consequences (Mydlarz et al.
2010). Basically, air temperature increases and, hence, affects the thermal biology of
terrestrial animals (Huey et al. 2012). For these reasons, recent research on the effect of
temperature on biological processes has experienced a renaissance (Krenek et al. 2011),
particularly in ectotherms that are especially vulnerable to climate warming because
their basic physiological functions are directly influenced by the environmental
temperature (Deutsch et al. 2008).
Studies in this field are imperative for assessing the suitability of thermal habitats and
describing the thermal ecology of ectotherms, that depend on the thermal micro-habitats
for success in many behaviors, such as reproduction or prey capture (Hertz et al. 1993;
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Canals et al. 2007; Figueroa et al. 2010; Veloso et al. 2012; Neethling and Haddad
2019). Specifically, in the case of ectotherms, such as Mygalomorph spiders, that shows
certain biological characteristics (e.g. high mortality rate at the juvenile stage, later
sexual maturity, sedentary females and juveniles) which increase their vulnerability.
Despite its vulnerability, the thermal biology of these taxa is poorly known (Seymour
and Vinegar 1973; Shillington 2002; Alfaro et al. 2012; Veloso et al. 2012; Cubillos et
al. 2018; Montes de Oca et al. 2019).
Grammostola vachoni is an endemic Argentinean tarantula that inhabits mountainous
grasslands in central Argentina (Ferretti and Ferrero 2008). The geographic range which
this species inhabits is characterized by a humid and temperate climate with an average
annual rainfall of 850 mm and a mean annual temperature is 14.5 °C with an annual
amplitude of 14-15 °C. In the summer the average temperature is 20 °C and the records
that reach 40 °C are frequent, while the winter is characterized with a hardest frosts (-
10°C, with 5% of probability) (Michalijos and Uboldi 2013; Kristensen and Frangi
2015). This species strictly occupies shallow burrows constructed under stones (Ferretti
and Pérez-Miles 2011). Adult males of the species do not have fixed home ranges and
from October to December they frequently move in search of females (Ferretti and
Ferrero 2008). This species is characterized by a poor dispersal mechanism with an
aggregated distribution and with late sexual maturity. It is listed as vulnerable in the
IUCN Red List of Threatened Species (International Union for Conservation of Nature
and Natural Resources) (Ferretti and Pompozzi 2012). Although it is a threatened
species of high priority, its thermal biology is unknown. However, some studies have
been published on its reproductive behavior, intraspecific interactions and ecology
(Ferretti and Ferrero 2008; Ferretti and Pérez-Miles 2011; Schwerdt et al. 2018;
Schwerdt et al. 2019a, 2019b).
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To fill this gap, in the present study we attempted to explore the thermal biology of
juveniles and adult females of G. vachoni under laboratory conditions. We hypothesized
that: 1. Preferred temperature and critical thermal limits are different between juveniles
and females; 2. Locomotor performance is strongly affected by temperature, in both
juveniles and females; 3. Thermal sensitivity is higher at the lowest temperature ranges,
that represents temperatures that are less common in the habitats where G. vachoni is
found. To achieve these objectives, in the present study we: 1. Characterized the
preferred temperatures of juveniles and females of G. vachoni under laboratory
conditions; 2. Evaluated the relation between temperature and locomotor performance
through a thermal performance curve; 3. Calculated the thermal sensitivity for all
possible temperature ranges, discerning between juveniles and females.
Methods
Individuals
All the individuals of Grammostola vachoni used in the present study were bred in the
laboratory. Individuals were kept at 22 ± 2 °C under a 12:12 photoperiod and were
housed individually in a subdivided plastic terrarium. Spiders were fed once a week
with cockroaches [Blatella germanica (Linnaeus, 1767)] except during the experimental
period. The body mass (hereafter Mb) of each specimen was measured using a Denver
AA-160 balance with a precision of 0.001 g. We used juveniles of the same
development stage (age = 4 years) and adult females of similar sizes for both
experiments.
Experiments
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Thermal preference. A thermal gradient from 3ºC to 60ºC was generated in a glass cage
of 65 x 13 x 15 cm (length x width x height), with sand on the floor (0.5 cm). The hot
end had a constant heat source under the sand, while the cold end had a cold source (see
Veloso et al. 2012; Barahona‐Segovia et al. 2016). This gradient was calibrated and
checked before and during each experiment. The spiders (juveniles: n = 20, females: n =
13) were introduced individually at the center of the cage where the temperature was
about 30ºC. We avoided disturbing the individuals during the experiments. The spiders
were free to move during four hours in order to select their preferred temperature. The
body temperature of each individual was recorded every 30 min with an infrared
thermometer (EXTECH Instrument, Dual Laser; IR accuracy: ± 0.8 °C); the
measurements were obtained from the midpoint between the carapace and abdomen.
Critical thermal limits and locomotor performance. We considered the sprint speed as
the parameter for the relationship between performance and temperature. To evaluate
the thermal performance, each spider was placed in a sealed plastic tube and submerged
directly into a programmable thermostatic bath (Digital Thermostatic Bath v1.0) for 30
min under different random temperatures (5, 10, 15, 20, 25, 30, 35, 40 and 45 ºC) and
on different days. Each individual was evaluated for only one temperature per day. We
decided not to perform any experiments at the highest temperatures in order to avoid
extremely stressful conditions for the spiders. After removal from the bath, each spider
was immediately placed on an experimental setup to measure its sprint speed
performance [speed from the start in the set up to the first stop (cm sec-1)]. The
experimental setup consisted of a plexiglass cylinder (1 m long and 10 cm wide) with
graph paper in the background. The sprint speed was calculated by the distance
measured on the graph paper and a chronometer. The measurement was considered
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from the starting point of the carapace. All experiments were carried out by the same
operator.
The thermal performance curve (TPC) and their parameters were calculated with a
polynomial quadratic regression: critical thermal limits minimum and maximum (CTmin
and CTmax, respectively), maximal performance (Pmax), thermal optimum (Topt), thermal
performance breadth (Tbr) and tolerance range (TR). The ecophysiological
characteristics of CTmin and CTmax were derived numerically as the intersection points of
the resulting TPC on the temperature axis (µ=0) (Martin and Huey 2008; Gaitán-Espitia
et al. 2014). The Topt comprises the temperature at which an individual sprinted the
fastest; so Pmax is the sprint speed at Topt. The Tbr is an index that represents the
amplitude of performance and it was calculated using the following equation (Gilchrist
1996): ; where N equals the number of 𝑇𝑏𝑟 = √∑𝑁𝑖 = 1[𝑃𝑖(𝑇𝑖 ― 𝑇𝑜𝑝𝑡)/𝑃𝑚𝑎𝑥]2
temperatures and Pi is the sprint speed at temperature Ti. The tolerance range (TR) was
calculated as .𝑇𝑅 = 𝐶𝑇𝑚𝑎𝑥 ― 𝐶𝑇𝑚𝑖𝑛
In the thermal sensitivity (Q10), the subunit 10 only makes reference to a 10-degree
temperature range. However, in the present study we analyzed thermal sensitivity over a
5-degree temperature range, which, we will refer to as Q5 hereafter. The Q5 was
calculated using the sprint speed and comparing seven five-degree intervals (5-10, 10-
15, 15-20, 20-25, 25-30, 30-35 and 35-40°C) using the formula 𝑄5 = (𝑅2𝑅1)
(10
𝑇2 ― 𝑇1)
(Schmidt-Nielsen 1997). In this equation, R1 is the performance at temperature 1 of
range (T1), and R2 is the performance measured at temperature 2 of the same range
(T2).
Statistical analyses. The normality of data was evaluated by the Shapiro-Wilk test (Zar
1999). The locomotion performance (sprint speed) at the different temperatures was
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estimated using repeated measures ANOVA and the means were compared with the
Tukey test. Thermal parameters between juveniles and females and thermal sensitivity
of the sprint speed over a 5-degree range (Q5) were compared through ANOVA. We
used the Pearson correlation to explore the possible linear relationships between Mb
with thermal parameters and Q5. Data are presented as mean ± 1 standard deviation
(SD), except where otherwise indicated.
Results
The 13 adult G. vachoni used for the study weighed 14.13 ± 1.18 g (mean ± SD),
whereas the 20 juveniles weighed 6.55 ± 1.13 g (mean ± SD).
Thermal preference
Individuals of G. vachoni were able to move freely during the experiments until they
remained in a thermally preferred zone. We did not find any significant differences in
the preferred temperatures of juveniles and females (juveniles = 26.98 ± 0.9 °C and
females = 25.95 ± 0.7 °C; ANOVA, F = 0.69, p > 0.05) (Figure 1). All individuals
showed a preference peak and spent 40% of the total time in the 25-29 ºC range (Figure
2). We did not find any significant correlation between Mb and the preferred temperature
(Pearson, r = 0.21, p > 0.05; r = -0.26, p > 0.05; females and juveniles respectively).
Critical thermal limits and locomotor performance
We recorded an average Topt of 25.75 ± 2.0 °C (N = 33), and CTmin and CTmax showed
values of 5.39 ± 0.78 °C and 46.11 ± 4.26 °C, respectively. The Pmax was 4.87 ± 1.33
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cm sec-1, while values obtained for Tbr and TR were 14.74 ± 3.19 °C and 40.72 ± 4.63
°C, respectively. The significant differences in Topt, CTmax, Tbr and TR between the
juveniles and females are shown in Table 1.
The TPC showed that sprint speeds from spiders were significantly different between
the different temperatures (ANOVA repeated measure: F = 26.92; p < 0.0001 and F =
19.73; p < 0.0001; juveniles and females respectively) (Figure 3). Different speeds
between the juveniles and females were found at 5 °C, 35 °C and 40°C, but for the
remaining temperatures, the sprint speed values were almost equal (Figure 4).
Locomotor performance is strongly affected by high temperatures, especially in the
juveniles (N = 20) that showed the greatest sprint speed between 25 ºC and 30 ºC and
the slowest speeds at 5 ºC, 10 ºC and 40 ºC (Post Hoc Tukey, p < 0.05); while the
females (N = 13) showed the greatest sprint speeds at 35 °C and the slowest speeds at 45
°C and 5 °C. We did not find any significant correlations between Mb and the thermal
parameters.
The thermal sensitivity (Q5) evaluated for all spiders showed a mean value of 3.32 ±
6.80. Significant differences were found between the temperature ranges (ANOVA: F
= 5.95; p < 0.01) (Table 2). The highest thermal sensitivity was recorded in the lowest
temperature ranges, for 5-10 °C and 10-15 °C ranges, for both the juveniles and
females. However, the lowest Q5 values were obtained in the 25-30 °C, 30-35 °C and
35-40 °C ranges (Figure 5). In the latter temperature ranges reported, significant
differences were found between the juveniles and females (Table 2). The juveniles
showed the lowest values of Q5 in relation to females under those temperature ranges
(Figure 5). We did not find any significant correlation between Mb and Q5.
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Discussion
De Vito and Formanowicz (2003) reported that large spiders are generally less prone to
desiccation than small spiders and likewise, in previous studies, size-related differences
in the preferred temperature were reported (Sevacherian and Lowrie 1972; Humphreys
1975, 1978). However, we did not find any differences in the preferred temperature
between the different developmental stages studied in G. vachoni. The acclimation of
individuals under laboratory conditions could explain this similarity in the
developmental stages involved. The fact that body mass does not affect the preferred
temperature agrees with previous studies on other tarantula species (Alfaro et al. 2012;
Veloso et al. 2012). In addition, other studies showed that thermal preferences would
match the Topt for maximizing the fitness and in ectotherms, the thermal preferences
would be close to the body temperature (Huey and Bennett 1987; Angilletta et al. 2002;
Martin and Huey 2008). In fact, in this study we observed that the preferred temperature
is actually close to Topt for both the juveniles and females.
Martin and Huey (2008) suggested that ectotherms would avoid body temperatures that
approach CTmax, maintaining a broad “thermal-safety margin” (i.e., the distance
between Topt and CTmax) and our results agreed with this idea. Moreover, we observed
that the upper limit of preferred temperatures (about 32-34 °C) was much lower than the
CTmax (approximately 44 and 49 °C in juveniles and females, respectively). Similarly,
the lowest thermal limit chosen by G. vachoni (about 13 and 18 °C) was higher than
CTmin (approximately 5 ºC in juveniles and females). Our results showed that when the
breadth of thermal performance and the tolerance range showed a wide thermal
spectrum and the individuals are able to select temperatures from a gradient, they
preferred to remain under middle temperatures. Also, females a showed wider
temperature amplitude of performance than juveniles, with a higher CTmax. However,
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this result could not be explained by differences in the body mass of the spiders, since
no correlations between thermal parameters and body mass were found.
Extremely high temperatures negatively affect the individual performance or activity,
reaching zero performance at CTmax (Storks et al. 2017). The juveniles of G. vachoni
showed a reduced locomotion after being exposed to 40 ºC whereas the females showed
the same symptom at 45 °C. In these cases, some spasmodic movements were observed
in some cases. Krakauer (1972) reported muscular spasms prior to death during thermal
stress in Nephila clavipes (Linnaeus, 1767) (Araneidae). Lutterschmidt and Hutchison
(1997) suggested muscular spasms as a good CTmax limit point.
According to Nespolo et al. (2003), there is a lot of information on the Q10 regarding
metabolic rate in insects and the values reported usually ranged from 1.5 to 3 (Davis et
al. 1999; Rourke 2000; Rogowitz and Chappell 2000), that are in agreement with results
provided in other studies on tarantulas and other arachnids (Punzo 1991; Shillington
2005; Lardies et al. 2008). However, the thermal sensitivity is variable, depending on
the process being tested, e.g. a value of 5.3 was found for the excretion rate in a species
of grasshopper (Harrison and Fewell 1995). Animals tend to exhibit higher Q10 values at
the extremes of the metabolic tolerance and, species that exhibit a low metabolic
response at low temperatures tend to exhibit a high metabolic response at high
temperatures (Nespolo et al. 2003; Watson 2008). Therefore, a higher Q10 indicates
greater temperature sensitivity of processes over the range, whereas a lower Q10 would,
therefore, indicate stability and would be considered more favorable (Watson 2008). For
some thermodynamic considerations in many ectotherm processes, Q10 is predicted to
be higher at lower temperatures (Schmidt-Nielsen 1995). Our results have shown a
similar trend, by obtaining Q5 values higher at lower temperatures and decreasing as
temperatures increased, as reported in other studies (Punzo 1991; Nespolo et al. 2003;
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Stork 2012). Thermal sensitivity at both the 5-degree range and the 10-degree range is
the same, with the difference that Q5 provides more information than Q10, because it
shows the factor by which metabolic processes change over a given 5-degree range of
temperature and, hence, offers a larger number of more precise measurements. Our
results showed that the greater sensitivity was related to temperatures that are not
usually recorded inside the burrows of G. vachoni, for example, the temperature inside
the burrow is close to 13 °C during the coldest months it the field (Schwerdt 2018). It
was observed that the species fitness and some behavior were unsuccessfully displayed
over a temperature range and could be indicative of the temperature acting as an
ecological factor that limits the species distribution. According to Booster et al. (2015)
the thermal sensitivity of tarantula locomotion is directly relevant to their field ecology.
For example, in this study, the sprint speed can be a good measurement by which to
integrate the physiology and ecology of the species. This is because the sprint speed has
been shown to significantly affect vital life processes, such as predation, escape from
predators and intraspecific interaction in the mating season (Huey and Stevenson 1979).
However, in other spider species, such as Rabidosa rabida (Walckenaer, 1837), the
temperature does not seem to be a limiting factor for its geographical distribution (Stork
2012).
In this study, a significant variation was found in the thermal performance of speed
sprint in G. vachoni. Also, the CTmax recorded is probably greater than any temperature
experienced at night by the spiders, the time at which they are most active, even during
the warmest time of year (Schwerdt et al. 2018). Like other tarantulas, G. vachoni can
avoid unfavorable thermal conditions primarily through nocturnal activity patterns and
fossoriality (Punzo 1991; Schwerdt 2018). However, the air temperature has often been
higher as a direct effect of climate change (Huey et al. 2012). Hence, under a context of
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global warming, the thermal performance curve constitutes a useful tool for exploring
some possible effects of this change on body temperature and thus the physiological
performance and vulnerability (Huey et al. 2012; Sinclair et al. 2016). In addition,
tarantulas are especially susceptible since they have poor dispersal mechanisms,
aggregated distribution and long periods at the juvenile stage, implying that climate
change might actually constitute a relevant threat, affecting their thermal biology, as
found in other ectotherms (Punzo 1991; Huey et al. 2012; Nori et al. 2017; Ferretti et al.
2018; Montes de Oca et al. 2019).
Acknowledgements
The authors thank Viviana Echenique and Rodrigo Batista for making a Digital
Thermostatic Bath available. Also, we sincerely thank Pablo Rodriguez and Claudio
Veloso for assistance in the experimental design. We also thank Matias Gaviot for
making an infrared thermometer available. L.S was supported by a CONICET
scholarship.
References
Alfaro, C., Figueroa-Pérez, D., Torres-Contrera, H., Veloso, C., Venegas, F., Canals, L.,
and Canals, M. 2013. Effect of thermal acclimation on preferred temperatures in two
mygalomorph spiders inhabiting contrasting habitats. Physiol. Entomol. 38(1): 20-25.
Angilletta, M.J., Niewiarowski, P.H., and Navas, C.A. 2002. The evolution of thermal
physiology in ectotherms. J. Therm. Biol. 27(4): 249-268.
Arnold, S.J. 1983. Morphology, performance and fitness. Am. Zool. 23: 347-361.
Page 15 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
16
Barahona‐Segovia, R.M., Grez, A.A., and Bozinovic, F. 2016. Testing the hypothesis of
greater eurythermality in invasive than in native ladybird species: from physiological
performance to life‐history strategies. Ecol. Entomol. 41(2): 182-191.
Booster, N.A., Su, F., Adolph, S.C., and Ahn, A.N. 2015. Effect of temperature on leg
kinematics in sprinting tarantulas (Aphonopelma hentzi): high speed may limit hydraulic
joint actuation. J. Exp. Biol. 218(7): 977-982.
Canals, M., Salazar, M.J., Duran, C., Figueroa, D., and Veloso, C. 2007. Respiratory
refinements in the mygalomorph spider Grammostola rosea Walckenaer 1837 (Araneae,
Theraphosidae). J. Arachnol. 35(3): 481-486.
Cubillos, C., Cáceres, J.C., Villablanca, C., Villarreal, P., Baeza, M., Cabrera, R., and
Veloso, C. 2018. Cold tolerance mechanisms of two arthropods from the Andean Range
of Central Chile: Agathemera crassa (Insecta: Agathemeridae) and Euathlus condorito
(Arachnida: Theraphosidae). J. Therm. Biol. 74: 133-139.
Davis, A.L.V., Chown, S.L., and Scholtz, C.H. 1999. Discontinuous gas exchange cycles
in Scarabelus dung beetles (Coleoptera: Scarabaeidae): mass-scaling and temperature
dependence. Physiol. Biochem. Zool. 72: 555-565.
Deutsch, C.A., Tewksbury, J.J., Huey, R.B., Sheldon, K.S., Ghalambor, C.K., Haak,
D.C., and Martin, P.R. 2008. Impacts of climate warming on terrestrial ectotherms across
latitude. Proc. Natl. Acad. Sci. U.S.A. 105: 6668-6672.
DeVito, J., and Formanowicz, D.R. 2003. The effects of size, sex, and reproductive
condition on thermal and desiccation stress in a riparian spider (Pirata sedentarius,
Araneae, Lycosidae). J. Arachnol. 31(2): 278-285.
Page 16 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
17
Ferretti, N., and Ferrero, A. 2008. Courtship and mating behavior of Grammostola
schulzei (Schmidt 1994) a burrowing tarantula from Argentina. J. Arachnol. 36: 480-483.
Ferretti, N., and Pérez-Miles, F. 2011. Intraspecific non-sexual interactions of
Grammostola schulzei (Araneae, Theraphosidae) under laboratory conditions. Rev. Biol.
Trop. 59: 1173–1182.
Ferretti, N., and Pompozzi, G. 2012. Grammostola vachoni. In: IUCN 2012: IUCN Red
List of Threatened Species. Version 2012.3. Available from www.iucnredlist.org.
Ferretti, N., Arnedo, M., and González, A. 2018. Impact of climate change on spider
species distribution along the La Plata River basin, southern South America: projecting
future range shifts for the genus Stenoterommata (Araneae, Mygalomorphae,
Nemesiidae). Ann. Zool. Fenn. 55: 123-134.
Figueroa, D., Sabat, P., Torres-Contreras, H., Veloso, C., and Canals, M. 2010.
Participation of book lungs in evaporative water loss in Paraphysa parvula, a
mygalomorph spider from Chilean Andes. J. Insect Physiol. 56: 731-735.
Gaitán-Espitia, J.D., Bacigalupe, L.D., Opitz, T., Lagos, N.A., Timmermann, T., and
Lardies, M.A. 2014. Geographic variation in thermal physiological performance of the
intertidal crab Petrolisthes violaceus along a latitudinal gradient. J. Exp. Biol. 217: 4379-
4386.
Gilchrist, G.W. 1996. A quantitative genetic analysis of thermal sensitivity in the
locomotor performance curve of Aphidiu servi. Evolution, 50: 1560–1572.
Hammerstein, P., and Riechert, S.E. 1988. Payoffs and strategies in territorial contests:
ESS analyses of two ecotypes of the spider Agelenopsi saperta. Evol. Ecol. 2: 115-138.
Page 17 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
18
Harrison, J.F., and Fewell, J.H. 1995. Thermal effects on feeding behavior and net energy
intake in a grasshopper experiencing large diurnal fluctuations in body temperature.
Physiol. Zool. 68: 453-473.
Hegarty, T.W. 1973. Temperature coefficient (Q10), seed germination and other
biological processes. Nature, 243: 305-306.
Hertz, P.E., Huey, R.B., and Stevenson, R. 1993. Evaluating temperature regulation by
field active ectotherms: the fallacy of the inappropriate question. Am. Nat. 142: 796-818.
Huey, R.B., and Slatkin, M. 1976. Cost and benefits of lizard thermoregulation. Q. Rev.
Biol. 51(3): 363–384.
Huey, R.B., and Stevenson R.D. 1979. Integrating thermal physiology and ecology of
ectotherms: a discussion of approaches. Am. Zool. 19: 357-366.
Huey, R.B., and Bennett, A.F. 1987. Phylogenetic studies of coadaptation: preferred
temperatures versus optimal performance temperatures of lizards. Evolution, 41(5):
1098-1115.
Huey, R.B., and Kingsolver, J. 1989. Evolution of thermal sensitivity of ectotherm
performance. Trends Ecol. Evol. 4: 131-135.
Huey, R.B., and Berrigan, D. 2001. Temperature, demography, and ectotherm fitness.
Am. Nat. 158: 204–210.
Huey, R.B., Kearney, M.R., Krockenberger, A., Holtum, J.A.M., Jess, M., and Williams,
S.E. 2012. Predicting organismal vulnerability to climate warming: roles of behavior,
physiology and adaptation. Philos. Trans. R. Soc. Lond. B Biol. Sci. No. 367: 1665-1679.
Page 18 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
19
Humphreys, W.F. 1975. The influence of burrowing and thermoregulatory behaviour on
the water relations of Geolycosa godeffroyi (Araneae: Lycosidae), an Australian wolf
spider. Oecologia, 21: 291–311.
Humphreys, W.F. 1978. The thermal biology of Geolycosa godeffroyi and other burrow
inhabiting Lycosidae (Araneae) in Australia. Oecologia, 31: 319–347.
Hutchison, V.H. 1961. Critical thermal maxima in salamanders. Physiol. Zool. 34: 92-
125.
Neethling, J.A., and Haddad, C.R. 2019. Influence of some abiotic factors on the activity
patterns of trapdoor spiders, scorpions and camel spiders in a central South African
grassland. Trans. R. Soc. S. Afr. 74(2): 107-114. doi: 10.1080/0035919X.2019.1596177.
Kingsolver, J., Diamond, S.E., and Buckley, L.B. 2013. Heat stress and the fitness
consequences of climate change for terrestrial ectotherms. Funct. Ecol. 27: 1415–1423.
Krakauer, K.T. 1972. Tolerance responses of the orb-weaving spider, Nephila clavipes
(Araneae: Argiopidae). Am. Midl. Nat. 88: 245-250.
Krenek, S., Berendonk, T.U., and Petzoldt, T. 2011. Thermal performance curves of
Paramecium caudatum: a model selection approach. Eur. J. Protistol. 47(2): 124-137.
Kristensen, M.J., and Frangi, J.L. 2015. Chasmophytic vegetation and mesoclimates of
rock outcrops in Ventania (Buenos Aires, Argentina). Bol. Soc. Argent. Bot. 50(1): 35-
46.
Lardies, M.A., Naya, D.E., Berrios, P., and Bozinovic, F. 2008. The cost of living slowly:
metabolism, Q10 and repeatability in a South American harvestman. Physiol.
Entomol. 33(3): 193-199.
Page 19 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
20
Light, P., Dawson W.R., Shoemaker V.H., and Main A.R. 1966. Observations on the
thermal relations of western Australian lizards. Copeia, 1966(1): 97-110
Logan, M.L., Cox, R.M., and Calsbeek, R. 2014. Natural selection on thermal
performance in a novel thermal environment. Proc. Natl. Acad. Sci. U.S.A. 111: 14165–
14169.
Lutterschmidt, W., and Hutchison, V.H. 1997. The critical thermal maximum: history and
critique. Can. J. Zool. 75: 1561-1574.
Martin, L., and Huey, R. 2008. Why “Suboptimal” is optimal: Jensen`s inequality and
ectotherm thermal preferences. Am. Nat. 171: 102-118.
Michalijos, M.P., and Uboldi, J. 2013. Propuesta metodológica para la evaluación de
áreas afectadas por incendios mediante el uso de imágenes satelitales (Sierra de la
Ventana, Argentina). Rev. Geogr. Norte Gd. 56: 223-234.
Montes de Oca, L., Pérez-Miles, F., and Clavijo-Baquet, S. 2019. Thermal preferences in
seven species of Theraphosidae (Mygalomorphae): ecological implications. In 21st
International Congress of Arachnology, Canterbury, New Zealand, Feb 2019. p108.
Mydlarz, L.D., McGinty, E.S., and Harvell, C.D. 2010. What are the physiological and
immunological responses of coral to climate warming and disease? J.
Exp. Biol. 213: 934–945.
Nespolo, R.F., Lardies, M.A., and Bozinovic, F. 2003. Intrapopulational variation in the
standard metabolic rate of insects: repeatability, thermal dependence and sensitivity
(Q10) of oxygen consumption in a cricket. J. Exp. Biol. 206(23): 4309-4315.
Page 20 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
21
Nori, J., Leynaud, G.C., Volante, J., Abdala, C.S., Scrocchi, G.J., Rodriguez-Soto, C.,
and Loyola, R. 2017. Reptile species persistence under climate change and direct human
threats in north-western Argentina. Environ. Conserv. 45(1): 83-89.
Punzo, F. 1991. Intraspecific variation in responses to thermal stress in the tarantula,
Dugesiella echina Chamberlin (Orthognatha, Theraphosidae). Bull. Br. Arachnol. Soc.
8(9): 277-283.
Riechert, S.E., and Tracy, C.R. 1975. Thermal balance and prey availability: bases for a
model relating web-site characteristics to spider reproductive success. Ecology, 56: 265–
284.
Rogowitz, G.L., and Chappell, M.A. 2000. Energy metabolism of eucalyptus-boring
beetles at rest and during locomotion: gender makes a difference. J. Exp. Biol. 203: 1131-
1139.
Rourke, B. 2000. Geographic and altitudinal variation in water balance and metabolic rate
in a California grasshopper, Melanoplus sanguinipes. J. Exp. Biol. 203: 2699-2712.
Savory, T. 1964. Arachnida. Academic Press. London.
Schmidt-Nielsen, K. 1997. Animal physiology: adaptation and environment. Cambridge
University Press, Cambridge, United Kingdom.
Schwerdt, L. 2018. Ecología y biología de la conservación de una tarántula de Argentina
en peligro de extinción, Grammostola vachoni: énfasis en el Sistema de Ventania (Buenos
Aires). Ph.D. thesis, Universidad Nacional del Sur, Bahía Blanca, Buenos Aires,
Argentina. Available from http://repositoriodigital.uns.edu.ar/handle/123456789/4493
[accessed 19 July 2019].
Page 21 of 32
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Canadian Journal of Zoology
Draft
22
Schwerdt, L., Villalobos, A.E., and Pérez-Miles, F. 2018. Spiders as potential
bioindicators of mountain grasslands health: the Argentine tarantula Grammostola
vachoni (Araneae, Theraphosidae). Wildl. Res. 45(1): 64-71.
Schwerdt, L., Pompozzi, G., de Villalobos, A. E., and Pérez-Miles, F. 2019a. Trophic
traits of Grammostola vachoni, a tarantula (Araneae: Theraphosidae) from Argentina.
Aust. J. Zool. 66(3): 228-234.
Schwerdt, L., de Villalobos, A. E., and Pérez-Miles, F. 2019b. Factors that affect the
occupancy, activity and distribution patterns of Grammostola vachoni, an endemic
tarantula from the austral mountains of Argentina. J. Insect Conserv. 23(5-6): 967-975.
doi: 10.1007/s10841-019-00182-6.
Sevacherian, V., and Lowrie, D.C. 1972. Preferred temperature of two species of lycosid
spiders, Pardosa sierra and P. ramulosa. Ann. Entomol. Fenn. 65: 111–114.
Seymour, R.S., and Vinegar, A. 1973. Thermal relations, water loss and oxygen
consumption of a North American tarantula. Comp. Biochem. Physiol. 44: 83-96.
Shillington, C. 2002. Thermal ecology of male tarantulas (Aphonopelma anax) during the
mating season. Can. J. Zool. 80: 251-259.
Shillington, C. 2005. Inter-sexual differences in resting metabolic rates in the Texas
tarantula, Aphonopelma anax. Comp. Biochem. Physiol. A. 142(4): 439-445.
Sinclair, B.J., Marshall, K.E., Sewell, M.A., Levesque, D.L., Willett, C.S., Slotsbo, S.,
and Huey, R.B. 2016. Can we predict ectotherm responses to climate change using
thermal performance curves and body temperatures?. Ecol. Lett. 19(11): 1372-1385.
Page 22 of 32
https://mc06.manuscriptcentral.com/cjz-pubs
Canadian Journal of Zoology
Draft
23
Stork, R. 2012. Intraspecific Variation in the Thermal Biology of Rabidosa rabida
(Araneae: Lycosidae) (Walckenaer) from the Mountains of Arkansas. Environ. Entomol.
41(6): 1631-1637.
Stoks, R., Verheyen, J., Van Dievel, M., and Tüzün, N. 2017. Daily temperature variation
and extreme high temperatures drive performance and biotic interactions in a warming
world. Curr. Opin. Insect Sci. 23: 35-42.
Taucare-Rios, A., Veloso, C., and Bustamante, R.O. 2018. Thermal niche conservatism
in an environmental gradient in the spider Sicarius thomisoides (Araneae: Sicariidae):
Implications for microhabitat selection. J. Therm. Biol. 78: 298-303.
Veloso, C., Luhr, D., Marfull, R., Torres-Contrera, H., Figueroa-Pérez, D., Sabat, P., and
Canals, M. 2012. Characterization of the thermalmicro-environment of Paraphysa
parvula. J. Arachnol. 40: 34-38.
Watson, C.M. 2008. Comparative thermal biology and associated niche differentiation
among the five-lined skinks, PhD Dissertation, Biology. The University of Texas at
Arlington, Arlington, TX.
Woodin, S.A., Hilbish, T.J., Helmuth, B., Jones, S.J., and Wethey, D.S. 2013. Climate
change, species distribution models, and physiological performance metrics: predicting
when biogeographic models are likely to fail. Ecol. Evol. 3(10): 3334-3346.
Zar, J.H. 1999. Biostatistical analysis. Pearson Education India.
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Tables
Table 1. Thermal parameters of the thermal performance curve for juveniles and females
of Grammostola vachoni. Data are expressed as the mean ± SD. Significant results
(ANOVA) are in bold.
Parameter Juveniles Females F p
CTmin 5.59 ± 0.17 5.09 ± 0.21 3.5 0.07
CTmax 44.05 ± 0.77 49.33 ± 0.95 18.48 <0.001
Topt 24.82 ± 0.35 27.2 ± 0.46 16.35 <0.001
Pmax 4.64 ± 0.29 5.24 ± 0.32 1.64 0.21
Tbr 12.99 ± 0.52 17.45 ± 0.65 28.77 <0.001
TR 38.46 ±0.83 44.2 ± 1.03 18.95 <0.001
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Table 2. Thermal sensitivity over the temperature range analyzed for juveniles and
females of Grammostola vachoni. Different letters indicate the mean significant
differences between the temperature ranges (p < 0.05, Tukey test). Data are expressed
as the mean ± SD. Significant comparisons between juveniles and females (ANOVA)
are in bold.
Thermal sensitivity (Q5)Temperature range (°C)
Tukey test
All spiders Juveniles Females F p
5-10 C 7.65 ± 6.95 7.18 ± 1.17 3.96 ± 1.45 2.29 0.09
10-15 BC 5.91 ± 5.01 9.01 ± 3.26 7.89 ± 4.04 0.05 0.82
15-20 AB 3.02 ± 2.34 3.53 ± 0.51 2.23 ± 0.64 2.5 0.12
20-25 AB 2.97 ± 2.56 4.19 ± 1.25 2.48 ± 1.55 0.73 0.39
25-30 A 1.33 ± 1.09 1.47 ± 0.47 1.11 ± 0.58 0.28 0.62
30-35 A 1.04 ± 0.98 0.52 ± 0.30 1.83 ± 0.37 7.41 0.01
35-40 A 0.41 ± 0.37 0.19 ± 0.09 0.76 ± 0.11 16.03 0.0004
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Figure captions
Figure 1. Comparison of the temperature preferred (°C) by juveniles and females of
Grammostola vachoni. The temperature preferred was significantly different (ANOVA,
F = 0.69, p > 0.05; 25.95 ± 0.7 °C and 26.98 ± 0.9 °C (mean ± SD); for females and
juveniles respectively). The median line in each box represents the median temperature
and the cross indicates the mean for juveniles and females.
Figure 2. Time of permanence (% of all recordings) at different temperatures in
juveniles and females of Grammostola vachoni.
Figure 3. The thermal performance curve shown as the effect of temperature on the
locomotor performance, sprint speed, of juveniles (dark gray) and females (light gray)
of Grammostola vachoni.
Figure 4. Mean sprint speed ± standard error at different temperatures. * indicates
significant differences between juveniles and females (ANOVA: F = 17.88, p ≤ 0.001;
F = 15.08, p ≤ 0.001; F = 23.58, p ≤ 0.001; 5, 35 and 40 °C respectively).
Figure 5. Comparison of the thermal sensitivity (Q5) of Grammostola vachoni over
different temperature ranges. The median line in each box represents the median
thermal sensitivity. * indicates significant differences for Q5 between juveniles and
females (ANOVA, F = 7.41, p < 0.01; F = 16.03, p < 0.01; at 30-35 and 35-40 °C
respectively).
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Figure 1. Comparison of the temperature preferred (°C) by juveniles and females of Grammostola vachoni. The temperature preferred was significantly different (ANOVA, F = 0.69, p > 0.05; 25.95 ± 0.7 °C and
26.98 ± 0.9 °C (mean ± SD); for females and juveniles respectively). The median line in each box represents the median temperature and the cross indicates the mean for juveniles and females.
220x163mm (300 x 300 DPI)
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Figure 2. Time of permanence (% of all recordings) at different temperatures in juveniles and females of Grammostola vachoni.
310x175mm (300 x 300 DPI)
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Figure 3. The thermal performance curve shown as the effect of temperature on the locomotor performance, sprint speed, of juveniles (dark gray) and females (light gray) of Grammostola vachoni.
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Figure 4. Mean sprint speed ± standard error at different temperatures. * indicates significant differences between juveniles and females (ANOVA: F = 17.88, p ≤ 0.001; F = 15.08, p ≤ 0.001; F = 23.58, p ≤
0.001; 5, 35 and 40 °C respectively).
291x150mm (300 x 300 DPI)
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Figure 5. Comparison of the thermal sensitivity (Q5) of Grammostola vachoni over different temperature ranges. The median line in each box represents the median thermal sensitivity. * indicates significant
differences for Q5 between juveniles and females (ANOVA, F = 7.41, p < 0.01; F = 16.03, p < 0.01; at 30-35 and 35-40 °C respectively).
244x170mm (300 x 300 DPI)
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Graphical Abstract
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