Sprint performance of a generalist lizard running on different

Transcription

Sprint performance of a generalist lizard running on different
Journal of Zoology
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Journal of Zoology. Print ISSN 0952-8369
Sprint performance of a generalist lizard running on
different substrates: grip matters
Renata Brandt, Fabricio Galvani & Tiana Kohlsdorf
Department of Biology, FFCLRP, University of São Paulo, Ribeirão Preto, Sao Paulo, Brazil
Keywords
Tropidurus torquatus; sprint speed; grip;
substrate type; locomotor performance;
friction; lizard; running speed.
Correspondence
Tiana Kohlsdorf, Department of Biology,
FFCLRP, University of Sao Paulo, Avenida
Bandeirantes, 3900, Bairro Monte Alegre,
Ribeirao Preto, Sao Paulo 14040-901, Brazil.
Email: [email protected]
Editor: Mark-Oliver Rödel
Received 1 October 2014; revised 27 March
2015; accepted 28 March 2015
doi:10.1111/jzo.12253
Abstract
The relationships between locomotor performance and major features of environmental structure, such as incline and diameter, have been consistently identified in
several vertebrate groups. The effects of variation in characteristics such as texture
and structural complexity, in contrast, remain neglected, and associations between
sprint speeds achieved during steady-level locomotion and the way an animal grips
the surface are particularly obscure. In the present study, we have used the habitat
generalist lizard Tropidurus torquatus to test the hypothesis that animals run faster
on the substrates where gripping performance is higher. We ran 18 individuals on
seven different substrates (wood, thin and coarse sand, coarse gravel, rock, leaf
litter and grass) and recorded their maximum speeds using high-speed cameras.
Surfaces were characterized for height variation and grip, the last given by average
grip performance achieved by lizards of different sizes. Maximum sprint speeds
were highest on rock and grass and lowest on thin and coarse sand, and variation
in performance among substrates was explained by grip: substrates in which
lizards gripped stronger are those that enhanced average maximum sprint speed.
This study is the first report providing evidence for variation in maximum sprint
speeds achieved by a generalist lizard running on different substrates, and demonstrates how friction resulting from the interaction of the lizard with the substrate may be critically important for sprint speed.
Introduction
The influence of environmental structure on the locomotor
performance of organisms is a classical assumption of
Arnold’s paradigm (Arnold, 1983). Evidence for Arnold’s
paradigm assumption is prevalent among squamates, a vertebrate lineage in which several species exhibit locomotor adaptations to habitat structure (Garland & Losos, 1994). A
remarkable example is the presence of toe fringes in the lizard
Uma scoparia (Carothers, 1986), a sand dune specialist that
became a classic model of locomotor adaptation to a specific
substrate. The relationships between locomotor performance
and the characteristics of habitats occupied by different
species have attracted considerable attention mostly because
locomotion is a key feature for a wide array of ecological
tasks, including finding mates and escaping from predators,
which directly affect fitness. The best described effects of
habitat structure on lizard locomotor performance are the
speed reductions observed in animals moving on inclined surfaces (Irschick & Jayne, 1998; Jayne & Irschick, 1999) and on
perches of distinct diameters (Losos & Sinervo, 1989; Losos &
Irschick, 1996). The effects of moving on different substrates on running speeds are less known (Van Damme &
Vanhooydonck, 2001; but see also Kohlsdorf et al., 2004;
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
Vanhooydonck et al., 2005; Kohlsdorf & Navas, 2012; Tulli,
Abdala & Cruz, 2012; Vanhooydonck et al., 2015), and the
focus of the existing studies has mostly been given to the
evolution of morphologies adapted to specific substrates
(Kohlsdorf et al., 2004; Tulli et al., 2012). The influence of
characteristics as grip or structural complexity of different
substrates on performance, on the contrary, still remains
neglected (with some exceptions as Vanhooydonck et al., 2005
and Li et al., 2011).
Characteristics as friction and structural complexity of different substrates are particularly relevant for sprint speeds
because of the physical interaction between animal’s feet and
the supporting surface during terrestrial locomotion. Specifically, a successful step depends on how efficiently a foot exerts
forces to the surface during animal locomotion (Lejeune,
Willems & Heglund, 1998; Kerdok et al., 2002; Korff &
McHenry, 2011). In turn, the forces applied by the feet on the
surface are determined by interactions between characteristics
of the organism (e.g. bone lengths, muscle force production)
and those of the substrate (e.g. incline, granulation and friction). For example, in the absence of other forces (e.g. wind,
rain and locomotion of other animals), steps on a granular
substrate cause irreversible deformation of the surface. The
surface deformation results in substantial energy loss to the
1
Lizard running speed and grip on different substrates
substrate, which in lizards is often compensated by mechanical
work of the upper hind limb muscles, potentially affecting
performance (Li, Hsieh & Goldman, 2012). Frictional properties of the substrates also potentially affect performance, as
the interaction between a lizard’s foot and substrates of different textures likely results on distinct friction coefficients
(Alexander, 2003). Accordingly, lower friction coefficients
probably restrict acceleration and limit maximum sprint
speeds (Vanhooydonck et al., 2015) likely determining if
animals slip during locomotion (van der Tol et al., 2005) and
how do lizards grip to specific substrates (Zani, 2000; Tulli,
Abdala & Cruz, 2011).
Despite the expected effect of friction on locomotor performance, the relationships between grip performance and
running sprint speeds have not been tested. This is particularly
surprising because both performance traits seem to be connected by the way animals apply forces to the substrate and
deal with physical differences among surfaces (Kerdok et al.,
2002; Alexander, 2003; Korff & McHenry, 2011). Identifying
associations between sprint speeds and gripping performances
achieved on physically different surfaces is likely of interest to
studies focusing on generalist species that use a wide array of
substrates. If sprint performance in different ecological settings reflects the effects of friction coefficients when the foot
moves in contact with substrate, it will likely influence the
microhabitat choices of a generalist species when performing
different ecological tasks.
In this study, we compare the effects of different substrates
on sprint speeds achieved by an iguanian lizard, testing if the
variation observed is related to the grip performance exhibited
on each specific substrate. We chose Tropidurus torquatus
(Tropiduridae) as our study system because it is a generalist
species known to use the entire set of substrates incorporated
here, also displaying some microhabitat preferences depending on the population analyzed (Rodrigues, 1987). We measured sprint speeds on seven structurally different substrates
(wood, thin and coarse sand, coarse gravel, rock, leaf litter
and grass) and related results to average grip force achieved on
each surface. Specific questions addressed are as follows: (1)
Do sprint speeds achieved by the generalist lizard T. torquatus
differ among natural substrates? (2) Are the expected differences in sprint speeds explained by variation in grip forces
observed among substrates? Our prediction is that lizards will
exhibit higher sprint speeds on the substrates in which grip
performance is higher.
Material and methods
Animals and husbandry
The lizard T. torquatus is a generalist species distributed along
a wide range of ecological settings that uses diverse
microhabitats (Rodrigues, 1987). We maximized ecological
diversity by sampling two populations differing in body size
and in the main substrate used in nature. In an urban area at
Piracicaba/SP, Brazil, 10 lizards were collected on concrete
walls, tree trunks, grass and rock pavement. Eight additional
individuals were collected at Praia dos Neves, in Presidente
2
R. Brandt, F. Galvani and T. Kohlsdorf
Kennedy/ES, Brazil. Lizards from this second population are
found on a sandbank area that is characterized by sparse
vegetation and a thin leaf litter covering the sand soil under
the vegetation. All animals were collected under IBAMA
permit no. 14109-1. Lizards were captured by nose, placed in
cloth bags and transported to the laboratory at University of
São Paulo in Ribeirão Preto (São Paulo, Brazil). In captivity,
animals were maintained in plastic terraria with an incandescent lamp (40 W, 12:12 dark–light cycle) that provided
basking areas for behavioral thermoregulation. Animals were
fed after experiments three times a week with live cockroaches
and mealworms and offered water ad libitum. At the end of the
experiments, animals were killed by intraperitoneal overdose
of anesthetics for removal of muscle samples used in other
related studies developed in the laboratory; specimens were
fixed with 10% formalin and preserved in 70% ethanol at the
Coleção Herpetológica de Ribeirão Preto (CHRP – University of São Paulo). All procedures were approved by the Ethics
Committee for Animal Experimentation from University of
São Paulo (CEUA/USP). After fixation, we measured the
snout–vent length of each specimen using a digital caliper
(Mitutoyo CD-15B, Suzano, SP, Brazil; ±0.01 mm).
Physical and structural characteristics of
the substrates: grip and height variation
We used seven different substrates in our performance tests:
wood, thin and coarse sand, coarse gravel, rock, leaf litter and
grass. This sampling comprised granular substrates (two types
of sand and leaf litter), which likely displace under pressure of
lizard’s feet, fixed surfaces (wood, rock and coarse gravel),
which remain steady when an animal moves along them,
and a substrate with intermediate properties (grass). These
substrates were physically characterized regarding grip and
structurally characterized regarding complexity (i.e. height
variation). Grip was quantified in each substrate by measuring
the average grip force necessary to detach a large (23 g) and a
small (13 g) T. torquatus lizard from the substrate. We
adapted the protocol of Zani (2000) and placed the lizards on
each substrate allowing them to grasp with both hands and
feet. Animals were connected to a dynamometer (accuracy:
0.1 g; Pesola scale) by a string attached to their pelvic and
scapular girdles. Each lizard was then dragged horizontally at
a constant speed until its complete detachment from the substrate; at this moment, we registered the maximum force
attained. Each measure was corrected by the mass of the
animal. We performed this procedure five times with each of
the two lizards and corrected values by body size dividing the
force measurements for body mass of each lizard; averaged
mass-corrected values for each different substrate corresponded to the grip force characteristic of each condition. In
addition, we estimated the reliability of our grip measurements. We calculated intraclass correlation for both the small
(0.89) and the large lizards (0.82), and the variance within
(0.700) and among substrates (1.86), and verified that our
measurements are repeatable.
We also structurally characterized each substrate by calculating the average variation in height of each substrate using
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
R. Brandt, F. Galvani and T. Kohlsdorf
lateral view photographs of the racetrack at the level of each
substrate with a scale bar. Each substrate was photographed
five times sequentially from the same distance, which covered
the entire length of the track, and the largest difference in
height variation was quantified on each photograph using the
software Corel Draw (version 10.0, Corel Corporation,
Ottawa, ON, Canada.). Specifically, we identified the highest
and the lowest points on each photograph, and the difference
between these two points corresponded to variation in substrate height in that photograph (Supporting Information Fig.
S1). We averaged these five measures to obtain the substrate’s
index of height variation.
Sprint speed
Sprint speed was measured by stimulating the lizards to run
over the seven different substrates (wood, thin and coarse
sand, coarse gravel, rock, leaf litter and grass). Trials were
performed on a 2-m racetrack covered every time by a different substrate. In the case of granular substrates (i.e. thin and
coarse sand and leaf litter), the substrate layer had a minimum
of 2-cm depth in order to avoid the lizard’s feet from touching
the racetrack floor during the race. Up to three substrates were
tested per day, allowing the animals to rest for at least 30 min
between trials. Each lizard was stimulated to run on the same
substrate for at least 2 different days, and the order of the
substrates was randomly chosen in each of the two sets of
races performed. Therefore, within each set of races, all lizards
were tested on the same substrate order, but the order of
substrates was not the same in the first and the second experimental sets. All tests were performed at 35 ± 1.5°C (for details
on preferred temperatures of T. torquatus, see Kohlsdorf &
Navas, 2006), and animals were placed inside an incubator for
30 min prior to each race and in between trials, to achieve the
experimental temperature. We filmed the trials from a top
view using two high-speed cameras (JVC TK-C1380) at 60
frames s−1 (see Rocha-Barbosa et al., 2008; Li et al., 2011;
Collins et al., 2013 for studies with lizards that used equivalent
filming speeds), covering the entire track. We digitized a point
at the tip of the snout using the MOTUS Peak Performance
software to register the maximum sprint speed attained by
each lizard at each substrate.
Analyses
All analyses were implemented in R (version 3.1.0) using
RStudio (0.98.953); all variables were log10 transformed prior
to analyses. We first tested if substrate had any effect on the
maximum sprint speed achieved using a repeated-measures
analysis of variance (ANOVA) design with assumption checks
(ez version 4.2-2, Lawrence, 2013). Individual maximum
sprint speed was entered as a dependent variable, substrate
was considered a within-subject factor and population was
incorporated as a between-subject factor. Subsequently, we
calculated a mean sprint speed for every substrate using the
individual maximum sprint speeds and tested if running performance could be explained by differences in grip or height
variation among substrates using linear regression models.
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
Lizard running speed and grip on different substrates
Results
The present study tested for the differences in sprint speeds
given by changes in substrate structure, subsequently relating
the variation identified to the average grip measured on each
substrate. We first tested for the differences in maximum sprint
speed achieved by individuals of T. torquatus from two different populations running on seven different substrates and
found that substrate type significantly affected maximum
sprint speeds (repeated-measures ANOVA, F6,96 = 3.39, P <
0.01) but population of origin did not (F1,16 = 1.02, P = 0.33).
Also, there was no interaction between population and
substrate type (F6,96 = 0.65, P = 0.68). The effect of substrate
type on sprint speeds was detected even when P-values
were adjusted due to marginally significant sphericity
test (Mauchly’s W = 0.099, P = 0.05; Greenhouse–Geisser
epsilon = 0.55, corrected P < 0.05; Huynh–Feldt epsilon =
0.71, corrected P < 0.01). Maximum sprint speeds were highest
on rock and grass, and lowest on thin sand (Table 1; Fig. 1).
Differences among substrates in the sprint speeds achieved by
T. torquatus being forced to run did not exceed 15%. The
subsequent step consisted of testing if the differences among
substrates identified on maximum sprint speeds were related to
the differences in substrate structure given by height variation
and the resultant grip. Average maximum sprint speed was not
explained by height variation of the substrates (slope = −0.02,
R2 = 0.08, F1,5 = 0.429, P = 0.54), but significant effects of
grip were detected (slope = 0.059, R2 = 0.744, F1,5 = 14.527,
P < 0.05). As predicted, substrates in which lizards had higher
grip enhanced average maximum sprint speed (Fig. 1).
Discussion
The present study provides evidence for the effects of variation
in substrate characteristics on the maximum sprint speeds
achieved by a generalist lizard. The observed differences
among substrates in the running performance of T. torquatus
were not explained by structural differences due to height
variation (for a discussion about structural heterogeneity in
natural habitats, see Höfling et al., 2012). Instead, differences
in sprint speeds among substrates are related to the average
Table 1 Data for running performance (means ± SE) and mean value of
height variation and mass-corrected grip associated with each
substrate tested
Substrate
Sprint speed
(mm s−1)
Height variation
(mm)
Grip (gF)
Wood
Thin sand
Coarse sand
Coarse gravel
Rock
Leaf litter
Grass
2265 ± 72.27
2151 ± 80.90
2212 ± 79.77
2291 ± 51.64
2421 ± 75.27
2226 ± 66.02
2415 ± 73.36
0
10.5
10.5
17.4
2.7
29.6
11.9
2.418
0.825
1.319
3.971
4.024
1.114
3.172
Sprint speed was quantified in 18 lizards and grip performance in 2
individuals. Height variation was measured sequentially five times
along the racetrack (for details see, the Material and methods section).
3
log10 (Mean maximum sprint speed) (mm s–1)
Lizard running speed and grip on different substrates
R. Brandt, F. Galvani and T. Kohlsdorf
3.39
Grass
Coarse gravel
3.36
Wood
Leaf litter
Coarse sand
Thin sand
3.33
0.0
0.2
0.4
log10 (Grip) (gF)
grip achieved on each surface. A novelty of our study was to
assemble the physical properties that can vary among the
natural set of substrates used by the species and translate them
into this one single measure with a biological meaning (grip),
which contrasts with the classical dichotomic approach of
polarizing substrates in either granular or solid (e.g. Claussen
et al., 2002; Kohlsdorf & Navas, 2012; Li et al., 2012). Under
such approach, we show that a secure grip is not only required
to climb up vertical surfaces, as traditionally discussed in the
literature (see Vanhooydonck, Van Damme & Aerts, 2002;
Alexander, 2003; Biewener, 2003), but it has also a major
effect on steady-level locomotion and represents a determining factor for speeds achieved when running horizontally.
The relationship between speeds of T. torquatus running on
different substrates and the average grip measured in each
surface is expected from a biomechanical basis. Ground reaction forces at the foot–floor interface have been extensively
studied and are probably the most critical biomechanical
factor in slipping (Redfern et al., 2001). The probability of an
animal slipping during locomotion is determined by the frictional properties of the substrate (van der Tol et al., 2005)
because interactions between the lizard’s feet and the substrate
determine the friction coefficients (Alexander, 2003). Specifically, slips will happen when friction or traction between the
feet and the running surface is too low. This is exceptionally
relevant for sprinting because the speed achieved depends on
the forces effectively applied to the substrate when the feet of
the animal interact with the surface (Lejeune et al., 1998;
Kerdok et al., 2002; Korff & McHenry, 2011). When the traction or friction between the foot and the surface is low, a slip
is inevitable (Redfern et al., 2002), and the animal may even
4
Rock
0.6
Figure 1 Log-log plot of mean values of
maximum sprint speed (y-axis) versus grip
(x-axis) of the lizard Tropidurus torquatus
running on different substrates. The regression line corresponds to linear least-squares
(R2 = 0.744, P < 0.05), and the gray shade
represents 95% of confidence intervals.
fail in pushing its body forward. It is relevant to mention that
some surfaces are more slippery than others, undoubtedly
affecting how lizards grip to them (Zani, 2000; Tulli et al.,
2011) and thus restricting acceleration and lowering maximum
sprint speeds during locomotion. These associations are supported by our results, as T. torquatus lizards ran faster on
substrates in which the measured grip was higher.
As a generalist lizard, T. torquatus is expected to exhibit a
low degree of performance sensitivity when running on different substrates (Irschick & Losos, 1999; Irschick, 2002).
Indeed, differences in speed between substrates were no larger
than 15%. It is important to point out that the speeds we
registered with animals being forced to run were much lower
than differences described in the literature for undisturbed
lizards (Urosaurus ornatus, see McElroy et al., 2007). Still,
even when forced to run, T. torquatus were slower on thin and
coarse sand, which were also the substrates in which we measured the lowest grip values. Although these results contradict
studies performed with the closely related Liolaemini lizards,
for which fastest sprint speeds were measured on sand (Tulli
et al., 2012), they are coherent with biomechanical predictions
for running on granular surfaces (see Lejeune et al., 1998;
Claussen et al., 2002). A large amount of energy is lost to the
substrate during lizard locomotion on sand because of the
irreversible deformation of the surface (Ding et al., 2012; Li
et al., 2012). The feet penetrate the granular surface during
locomotion, increasing drag and often reducing stride
length (Claussen et al., 2002; Ding et al., 2012). As a result,
performance is potentially affected and locomotion likely
becomes energetically more expensive (see Lejeune et al.,
1998; Li et al., 2012).
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
R. Brandt, F. Galvani and T. Kohlsdorf
The association between grip and sprint speeds identified
within a range of slightly different substrates is probably ecologically relevant for a generalist lizard such as T. torquatus.
For example, a slip potentially affects survival during predator escape, and variation in running performance imposed by
how the animal grips a given surface likely determines which
substrates will be more often used in nature. Therefore,
knowing how performance varies across an environmental
gradient, such as the grip gradient simulated here, is essential
for understanding the processes responsible for delimiting a
species niche (Irschick & Losos, 1999). Highly territorial
species, such as T. torquatus (Pinto, Wiederhecker & Colli,
2005), spend most of their time surveying their territory
against intruders and searching for food (Irschick & Losos,
1996). Such behavior intensifies exposure to predators, which
makes these animals strongly dependent on sprint speeds to
escape. At least within the lizard genus Anolis, species that rely
on rapid locomotion seem to be constrained to use habitats in
which they can achieve maximal performance (Irschick &
Losos, 1999). We noted something similar when comparing
the generalist T. torquatus (see table 2 of Grizante et al., 2010
for the estimated proportion of habitat use in tropidurines)
with other tropidurine species that are more specialized in
substrate use. Differences in sprint speeds of Tropidurus
running on rock and sand reported elsewhere (see Kohlsdorf
& Navas, 2012) did not exceed 5% in T. torquatus, while it
averages 25% among specialists and gets to about 52% in
T. insulanus, a species that is strictly found moving on rocks.
The generalist T. torquatus is not faster nor slower when
compared to the Tropidurus that are specialized in a given
substrate type (Kohlsdorf & Navas, 2012), supporting the
hypothesis of a weak specialization for maximal sprint
speeds associated with a broader habitat breadth in
T. torquatus.
Despite the large body of work dedicated for understanding
the relationships of locomotor performance with habitat use
and ecology, particularly within the genus Anolis, such functional relationships remained poorly understood for most
animal groups (Irschick, 2002). We provide a mechanistic
explanation for the variation in sprint performance among
different substrates. We show that the grip animals achieve on
different substrates is not only essential for locomotion on
inclined and vertical surfaces, as traditionally considered
(e.g. Alexander, 2003; Biewener, 2003), but also influences
maximum sprint speeds exhibited on level surfaces. This relationship was first identified here for a generalist species, which
is adapted for moving along different surfaces. The conceptual
elements underpinning such association likely encompass
animal locomotion in a wide range of terrestrial taxa and are
essential for understanding how differences in habitat and
microhabitat use evolved in different lineages.
Acknowledgments
The authors are grateful to Fabio Barros and Felipe Zampieri
for their assistance during the fieldwork. The authors also
thank André Vieira Rodrigues for the helpful discussions.
Anthony Herrel and an anonymous reviewer provided valuJournal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
Lizard running speed and grip on different substrates
able comments on previous versions of this paper. R.B. is
supported by a FAPESP postdoctoral fellowship 2013/
14125-0. This research was supported by a FAPESP 2006/
60140-4 grant awarded to T.K.
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Supporting information
Additional Supporting Information may be found in the
online version of this article at the publisher’s web-site:
Figure S1. Illustration of the method used for calculating
variation in substrate height. Five sequential photographs of
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
R. Brandt, F. Galvani and T. Kohlsdorf
the racetrack were taken for each substrate, as exemplified by
the three photographs shown in the right. In each photograph
the substrate top profile was indentified and the highest and
lowest points were marked (illustrated by red arrow). The
Journal of Zoology •• (2015) ••–•• © 2015 The Zoological Society of London
Lizard running speed and grip on different substrates
difference between these two points corresponded to variation
in substrate height in that photograph. The five measures
obtained for each substrate were then averaged to obtain the
substrate’s index of height variation.
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