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First published online October 31, 2008
Journal of Experimental Biology 211, 3523-3528 (2008)
Published by The Company of Biologists 2008
doi: 10.1242/jeb.007187
Commentary |
Stereotypy, flexibility and coordination: key concepts in behavioral functional morphology
1 Department of Evolution and Ecology, University of California, One Shields
Avenue, Davis, CA 95616, USA
2 Department of Biological Sciences, Clemson University, 132 Long Hall, Clemson,
SC 29634, USA
* Author for correspondence (e-mail: pcwainwright{at}ucdavis.edu)
Accepted 15 September 2008
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Summary |
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Key words: behavioral integration, kinematics, motor pattern
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Introduction |
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TOPSummaryIntroductionStereotypy and flexibilityIntegration and coordinationReferences |
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; Mehta and Wainwright,
2007; Motta and Wilga,
2001; Reilly and Lauder,
1992; Wainwright,
1989; Wainwright et al.,
1989)? Is the pattern of muscle activity observed during feeding
more variable in one species than another
(Ralston and Wainwright, 1997;
Van Wassenbergh et al.,
2006b)? Does prey-capture behavior change during ontogeny
(Reilly, 1995;
Richard and Wainwright, 1995;
Van Wassenbergh et al.,
2006a)? How are locomotor and prey-capture kinematics coordinated
(Higham, 2007;
Rice et al., 2008;
Rice and Westneat, 2005)? How
are the movements of different body parts coordinated during locomotion
(Danos and Lauder, 2007;
Shemmell et al., 2007)? Each
of these questions is concerned with partitioning variation in behavioral
traits; within and among individuals, among species, among treatment groups
and among body parts.
While these studies have contributed to a deeper understanding of the
nature and diversity of animal functional morphology, this literature exhibits
inconsistencies in how these effects are interpreted and in the terminology
used to describe particular patterns of variation. For example, the term
`stereotyped' has been used in reference both to a behavior that shows low
variation (Deban et al., 2001;
Nishikawa, 2000), and to the
behavior of an organism that does not vary in response to a treatment effect,
such as changes in prey type (Matott et
al., 2005; Wainwright and
Lauder, 1986). In both of these cases, stereotyped refers to a
pattern of low variance, but in the first case it refers to repeatability of
the behavior within a specific set of treatment conditions, while the latter
usage describes the failure of the animal to alter the behavior in response to
a change in the treatment conditions. These different uses of the term
`stereotyped' can lead to significant confusion, because one can imagine that
these levels of variation relate to different abilities of the organism that
need not be related to one another. A highly repeatable kinematic pattern that
shows very little variation under a given set of conditions could be
considerably altered in response to some treatments. One such example was
illustrated in a study by Ferry-Graham and colleagues with the cheeklined
wrasse, Oxycheilinus digrammus
(Ferry-Graham et al., 2001).
This fish showed highly repeatable kinematics when feeding on a specific prey
type, but the kinematics of prey capture were altered when feeding on
different prey, with elusive prey eliciting faster movements and greater
excursions of cranial elements.
The coordination of movements and motor patterns among body parts used for
a specific behavioral output has long been recognized as a key aspect of
locomotion, feeding and respiration
(Weiss, 1950;
von Holst, 1973;
Hildebrand, 1980;
Dickinson et al., 2000;
Ferry-Graham and Lauder,
2001). Assessment of how repeatable, or stereotyped, the
coordination among body parts is during these behaviors can provide
significant insight into the relative abilities of animals to control complex
behaviors. The repeatability of a coordination pattern between two or more
body parts in successive trials, under a given set of conditions, represents
one facet of how tightly linked movements are during a particular behavior.
This can be distinguished from changes to the pattern of coordination in the
face of a treatment. Coordination and its relationship to performance are
understudied in the comparative literature, although this topic has been
explored in more depth in the human literature
(Anderson and Sideaway, 1994;
Egan et al., 2007;
Post et al., 2000).
In this paper we discuss these commonly studied sources of variation in the behaviors studied by functional morphologists. We use this discussion to highlight some of the ambiguities in functional morphology and propose terminology towards a standardized approach to quantifying these sources of variation. Our ideas are illustrated with examples from prey-capture kinematics in fishes, although we intend our comments to apply generally to movement and motor pattern data associated with animal behaviors.
The field of animal behavior has a long history of defining and quantifying
stereotypy and interpreting its significance
(Adams, 1931;
Altmann, 1965;
Barlow, 1968;
Barlow, 1977;
Brown, 1975;
Gerhardt, 1991). Some of the
issues addressed in the present paper recall discussions in animal behavior
that took place decades ago and in general functional morphologists have been
slow to incorporate the notions and lexicon common to animal behavior, even
though in many cases the issues are virtually identical. Where possible we
attempt to identify these connections and highlight relevant insights from
animal behavior that may prove valuable in functional morphology.
Functional morphologists usually quantify behaviors by measuring movements
or motor patterns. Displacements and the relative position of body parts, or
kinematics, are measured as a function of time, such as rotation of joints or
the position of the body with respect to some reference. Most kinematic
variables quantify either event timing or amplitude, or are a derivative of
displacement data, such as velocities or accelerations of movement. Behaviors
are also characterized at the level of motor patterns, by measuring activation
patterns of muscles or nerves. For example, timing and amplitude of muscle
activation are often measured from electromyograms. An individual cycle of the
behavior under study is typically characterized by a set of these variables
that define the relative timing and amplitude of major movements of the
behavior or the relative timing and amplitude of activity of muscles that
control the movements. It is standard practice to characterize the kinematics
or motor pattern of the behavior by measuring the panel of variables for
several cycles, thus producing an average value for each variable and a value
for variance under those observational conditions. Examples of this protocol
are abundant in both functional morphology
(Dial et al., 2008;
Irschick and Jayne, 1999;
Wainwright and Lauder, 1986)
and behavior (Gerhardt, 1991;
Stamps and Barlow, 1973;
Stankowich, 2008;
Wiley, 1973).
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Stereotypy and flexibility |
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TOPSummaryIntroductionStereotypy and flexibilityIntegration and coordinationReferences |
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) with the
extremes being termed `stereotyped' and `variable'. A stereotyped behavior
would be one that shows little variation from trial to trial, while a variable
behavior would show inconsistency and hence greater variation
(Table 1). Stereotypy can be
quantified as the variance in the variables that are measured to characterize
a behavior, but because variance is usually correlated with the mean value of
a trait, we follow the tradition of animal behaviorists who recommend the use
of the coefficient of variation (standard deviation as a percentage of the
mean) (Barlow, 1977;
Schleidt, 1974).
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To compare the variability of a trait between two species one could measure the coefficient of variation of the trait in several individuals per species and compare the average coefficient of variation between species with an analysis of variance. Fig. 1 illustrates the variation in a kinematic trait measured during prey capture by two species of sunfish feeding on live shrimp. Lepomis cyanellus shows a more stereotyped pattern than L. microlophus, as evidenced by a smaller coefficient of variation: 0.19 vs 0.46. Transforming raw values into logarithms is another method that usually disassociates mean and variance and would allow direct comparisons of variance.
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Another point we stress here is that assessment of whether a particular
behavior is stereotyped or not should be made in a comparative context. We do
not believe that it is useful to arbitrarily choose a particular cut-off for
the coefficient of variation to define `stereotyped'. One reason for this is
that insufficient data are currently available to gauge whether global
generalizations would be useful, and also we suspect that levels of stereotypy
will depend on the specific conditions under which behaviors are measured. We
note that in his classic work on frog mating calls, Gerhardt initially felt
that low and high variance components of calls could be readily categorized as
`static' or `dynamic' (Gerhardt,
1991). However, after reviewing a wider range of frog calls, he
subsequently concluded that variability in elements of frog calls was
continuous and did not always fall clearly into static and dynamic categories
(Gerhardt, 1991;
Gerhardt and Huber, 2002).
We propose to restrict the use of the term `stereotyped' to refer to
behaviors with low variance in traits measured across replicates of the
behavior under the same set of experimental conditions. This among-trial
variability reflects a basic capacity of the organism to repeat the behavior
consistently. Particularly in the case of repetitive and rhythmic behaviors,
such as steady locomotion, stereotypy among cycles may strongly influence the
overall effectiveness of the behavior
(Adams, 1931;
Alexander, 1980).
We further suggest that it will be helpful in future functional analyses to
distinguish between among-trial variation and variation due to the ability of
the animal to alter its behavior in response to different stimuli. We define
`flexibility' as the extent to which the behavior is altered in response to a
change in stimulus. A behavior that shows no statistically significant change
in response to a treatment would be described as `inflexible' with respect to
that stimulus, whilst a behavior that shows a relatively large change in
response to the treatment would be described as `flexible'
(Table 1). Flexibility can be
measured as the proportional change in the quantified elements of the
behavior, but comparisons of the behavior in two or more treatments should be
based on levels of variance within a treatment. For example, when comparing
two behavioral variables, we may observe that their means are quite different
in magnitude. However, if variance within each behavior is high these means
may not be statistically different from one another. Published examples of
tests for flexibility relate to a wide range of treatments, including the
effect of an incline on footfall patterns
(Garnier et al., 2008), the
effect of obstacles on limb kinematics during running
(Kohlsdorf and Biewener,
2006), the effect of temperature
(de Vries and Wainwright,
2006), the effect of flight speed on wing kinematics
(Tobalske et al., 2003), the
effect of food attributes on feeding motor patterns
(Ross et al., 2007;
Sanderson, 1988;
Wainwright, 1989), and the
effect of body size (Van Wassenbergh et
al., 2006a; Wainwright and
Richard, 1995). Tests of flexibility involve comparisons of mean
values under separate treatments and can be done with analysis of variance if
the factor of interest is categorical, such as different prey in a feeding
experiment, or substrate type in locomotion. Regression can be used when the
factor of interest varies continuously.
We argue for the importance of distinguishing stereotypy from flexibility
because the two need not have the same underlying cause and need not be
mutually exclusive or correlated. All combinations of stereotypy and
flexibility are realistic. An animal may show a highly variable behavior that
is not altered across treatments, or a stereotyped behavior that is flexible.
Researchers have even reported cases where choice of stimulus affects the
level of stereotypy in the behavior. In one example, it was noted that
pufferfish showed a more variable feeding behavior when feeding on pieces of
dead shrimp than when feeding on live prey
(Ralston and Wainwright, 1997)
(see also Fig. 2).
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In the functional morphology literature, `stereotyped' is often used to
refer to what we term `inflexible', or a lack of variation in a behavior with
respect to a wide range of controlled experimental treatments
(Matott et al., 2005;
Sanderson, 1991;
Van Wassenbergh et al., 2006b;
Wainwright and Lauder, 1986).
We feel it is advantageous to distinguish between among-trial variation and
variation across stimuli because stereotypy and inflexibility can have
different underlying causes.
It is interesting to note that, when determining levels of stereotypy,
behaviorists have shown the same inconsistency seen among functional
morphologists concerning whether to distinguish between among-trial variation
(the source of our stereotypy) and variation due to the response to changes in
stimuli (the source of our flexibility). Our proposal largely follows Barlow,
who calculated stereotypy as the inverse of the coefficient of variation of a
behavior, and who separately asked whether modal action patterns could be
altered (Barlow, 1977). In
contrast, when evaluating why some elements of frog mating calls showed high
coefficients of variation, Gerhardt and Huber noted that `Some of the high
within-male variation in these properties is almost certainly attributable to
purely environmental factors such as the calling behavior of neighbors and
variability in the availability of energetic resources needed to fuel
signaling' (Gerhardt and Huber,
2002). Altmann, who constructed his own metric of stereotypy for
analyzing the sequence of behaviors in rhesus monkeys, lumped many possible
environmental influences into the variation that was captured by his metric
(Altmann, 1965). Thus, both
Gerhardt and Altmann included variation due to alternative stimuli in their
measures of stereotypy.
Causes of stereotypy and flexibility
A stereotyped behavior is one that is repeated with little variation from
trial to trial. This control may be active, as when the individual has the
ability to alter the behavior in response to sensory information, or passive,
as when movements are limited mechanically
(Westneat, 1990), intrinsic
stabilizing mechanisms are involved
(Nishikawa et al., 2007), or
the neuromotor basis of the behavior is simple and not readily altered by
sensory input (Brown, 1975). A
high degree of control on the part of the individual is implied if a behavior
is stereotyped and flexible (Wöhl and
Schuster, 2007).
We note that the underlying cause of stereotypy and inflexibility may be
the same in some situations. If a stereotyped behavior cannot be altered by
sensory feedback and is therefore inflexible, it is likely that the root cause
of stereotypy and inflexibility is the same. We predict that such behaviors
will prove to be rare. There is a tendency to assume that stereotyped
behaviors will also be inflexible. On close inspection, however, many
candidate `modal action patterns' have been shown to be stereotyped, but also
flexible. Examples include the classic strut display of male sage grouse
(Wiley, 1973) that has
recently been shown to change in different contexts (G. Patricelli, personal
communication), the Mauthner cell-mediated C-start escape response of fishes
that is known to be altered in response to the nature of the stimulus
(Canfield, 2003;
Eaton, 1988;
Tytell and Lauder, 2002), and
prey-restraint behavior in early lineages of macrostomate snakes, which has
also been shown to be altered in response to changes in prey characteristics
(Mehta and Burghardt,
2008).
One should not assume that an absence of flexibility in an experiment is
caused by an inability of the animal to alter the behavior. There are at least
two other possible causes of inflexibility
(Bout, 1998). First, it could
be that the optimal or adaptive response is the same for all treatments being
considered (Wainwright, 2002).
In such a case the animal uses the same behavior with little modification
because that particular behavior is well suited to all situations examined. A
second possibility is that inflexibility is due to mechanical coupling between
the elements involved in the behavior, physically limiting variation in the
movements. In the case of mechanical coupling, it is still common to see
flexibility in the rate of movement. But in these cases, stereotypy and
inflexibility may be linked, both being caused by an inability of the animal
to create variation in the behavior.
We note that while the degree of stereotypy and flexibility is likely to be
significantly correlated (e.g. Horner and
Jayne, 2008), it is unlikely to be identical. The pattern of nerve
firing that is controlled by the central nervous system interacts with
environmental factors and musculoskeletal mechanical properties to produce a
kinematic pattern. Passive mechanical properties of the musculoskeletal system
can have a significant impact on the kinematic output produced by motor input
(Full et al., 2002;
Nishikawa et al., 2007).
Ultimately, we must directly measure levels of stereotypy and flexibility
prior to determining mechanisms of regulation.
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Integration and coordination |
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TOPSummaryIntroductionStereotypy and flexibilityIntegration and coordinationReferences |
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The underlying causes of a highly integrated movement range from neuromotor
control and regulation of structurally independent elements
(Card and Dickinson, 2008) to
mechanical coupling, as occurs in a structural linkage system
(Westneat, 1990). In a
four-bar linkage (Fig. 4), four
skeletal elements are connected together in a loop that allows planar motion
at each of the four joints connecting pairs of links
(Muller, 1996). A four-bar
linkage has only one degree of freedom: if one skeletal element moves there
must be exact compensatory motion in each of the other three links. In such a
system movements of the four links will be perfectly integrated. If the angle
at one joint is known, all of the other angles can be determined. A highly
integrated system has one degree of freedom and although the speed of movement
of the system may vary from trial to trial, the tight coupling means that the
relative timing of events is always the same
(Patek et al., 2007;
Westneat, 1990).
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Integration can also be assessed between physiological (e.g. muscle
function) and mechanical (e.g. joint angles) components of a system
(Higham and Nelson, 2008). For
example, distal limb muscles of many terrestrial vertebrates insert
via long elastic elements (tendons), allowing a muscle to operate at
a constant length (which may maximize force output) while the joint undergoes
an excursion (e.g. Roberts et al.,
1997). This enhanced performance can be viewed as being permitted
by reduced integration between muscle function and limb kinematics.
An important question in functional morphology is what pattern of
coordination results in the highest performance for the behavior under
consideration. In the field of human motor learning, coordination has been
defined as `the relative movement between interacting body parts and the
object to be intercepted during goal-directed behavior'
(Newell, 1985). `Coordination'
has been used for some time in this literature to relate performance of a
behavior to specific features of kinematics or the motor control of the task
(Dessing et al., 2007). Once a
specific metric of performance is defined, a group of trials can be evaluated
and one can ask what kinematic or motor pattern results in the highest
performance. For example, what pattern of muscle activity or limb and body
kinematics results in the longest jumps by a frog or lizard? What kinematic
pattern results in the strongest suction pressure in a suction-feeding fish
(Sanford and Wainwright, 2002;
Svanbäck et al., 2002)?
In addressing a somewhat different issue, one could also ask whether
high-performing individuals or species are characterized by a more tightly
integrated pattern of kinematics or muscle activity.
While coordination is routinely documented in vertebrate functional
morphology (Irschick and Jayne,
1999; Rice et al.,
2008; Ross et al.,
2007), the affect of coordination on performance has received much
less attention (Toro et al.,
2006; Astley and Jayne,
2007). Relatively little is known about what combinations of
kinematics or motor activity result in high performance or whether high
performance requires tight integration of kinematics, and yet this should be a
valuable avenue for investigation (Full et
al., 2002; Holzman et al.,
2007).
As in the case of stereotypy and flexibility, distinguishing strength of
integration from the question of which pattern of integration maximizes
performance will allow us to explore whether some highly integrated behaviors
may not result in high performance. It is likely that performance is more a
function of the pattern of integration, such as the relative timing of
movements, rather than of the variance of that timing
(Egan et al., 2007).
Understanding integration of movements may have important implications for
how they are controlled at the level of the CNS. Tightly integrated movement
across the three major leg joints in humans has been used to argue for a
simple kinematic regulatory mechanism that modulates the magnitude of torque
at only one joint (Shemmell et al.,
2007). But, just as morphological innovation during evolution
often proceeds by breaking trait correlations that constrain diversity in
ancestors, it may be useful to think of behavioral innovations in terms of the
mechanisms that allow coordination patterns to be altered during evolution
(Liem, 1979). Patterns of
coordination may vary among ecomorphs within diverse lineages
(Rice, 2008). The mechanisms
that underlie evolutionary shifts in integration may be structural, such as
the origin of novel joints (Konow et al.,
2008), or decoupling events
(Westneat, 1991). Whether
behavioral innovation is more often driven by breaking neural regulatory
linkages or by structural changes in the skeletal system promises to be an
important area of investigation. But, like answering other questions about the
nature of behavioral variation, it will be necessary to appropriately
attribute variation to its potential causes and, thus, a paradigm is needed
that promotes the ability to make key distinctions.
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Acknowledgments |
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