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. 2021 Apr 26;16(4):e0249066. doi: 10.1371/journal.pone.0249066

From cockroaches to tanks: The same power-mass-speed relation describes both biological and artificial ground-mobile systems

Alexander Kott 1,*, Sean Gart 1, Jason Pusey 1
Editor: Hussain Md Abu Nyeem2
PMCID: PMC8075212  PMID: 33901211

Abstract

This paper explores whether artificial ground-mobile systems exhibit a consistent regularity of relation among mass, power, and speed, similar to that which exists for biological organisms. To this end, we investigate an empirical allometric formula proposed in the 1980s for estimating the mechanical power expended by an organism of a given mass to move at a given speed, applicable over several orders of magnitude of mass, for a broad range of species, to determine if a comparable regularity applies to a range of vehicles. We show empirically that not only does a similar regularity apply to a wide variety of mobile systems; moreover, the formula is essentially the same, describing organisms and systems ranging from a roach (1 g) to a battle tank (35,000 kg). We also show that for very heavy vehicles (35,000–100,000,000 kg), the formula takes a qualitatively different form. These findings point to a fundamental similarity between biological and artificial locomotion that transcends great differences in morphology, mechanisms, materials, and behaviors. To illustrate the utility of this allometric relation, we investigate the significant extent to which ground robotic systems exhibit a higher cost of transport than either organisms or conventional vehicles, and discuss ways to overcome inefficiencies.

Introduction

Remarkable regularities are observed with respect to relations among the speed, mass, and energy expenditures of biological organisms. Most of these relations are allometric, i.e., they describe how a function or attribute of organisms changes with their scale (e.g., with mass). Although the accuracy of the relations tends to be limited to an order of magnitude, these relations hold over very large ranges of values and over multiple orders of magnitude. For example, one of the earliest such observations was Kleiber’s Law [1], which states that for the vast majority of animals–from tiny mouse to huge elephant–the organism’s metabolic rate is approximately proportional to the organism’s mass to the 3/4 power; the data for all biological organisms fall on the same curve.

In a similar allometric fashion, it has been observed that for all biological organisms, the maximum speed V of animals increases proportionately to their mass M to the power of 1/6, i.e., V ~ M1/6, even when the mass of organisms varies by many orders of magnitude [2,3].

Another allometric law refers to the metabolic cost of transport (CoTm), which is the metabolic energy consumption that an organism requires to move a unit of mass of its body over a unit of distance. Equivalently, the amount of metabolic energy per unit time Pm required for the organism to move with speed V per unit of its mass M is CoTm = Pm/(M·V). For all biological organisms, CoTm diminishes approximately with mass to the power of -1/3, i.e., Pm/(M·V) ~ M(-1/3) [48]. Metabolic energy is the energy that an organism obtains through its food, though typically measured as the organism’s consumption of oxygen [9].

Unlike metabolic energy, the mechanical energy of an organism P is produced by the organism’s muscles in order to deliver forces by which it propels itself relative to the terrain and surrounding media, and moves its limbs with respect to the rest of its body. It has been observed that unlike the metabolic CoTm, the mechanical CoT = P/(M·V) remains approximately constant, or at least within the same order of magnitude, over a very wide range of M [4,6,7,1014].

Elaborating on the latter observation, Heglund proposed an empirical formula for estimating the mechanical power P expended by an organism of mass M in order to move itself at speed V [13]:

P=M·0.478·V1.53+0.685·V+0.072 (1)

Do similar regularities apply to artificial, human-made systems? If they do, how do they differ from those that apply to biological systems?.

We are aware of one observation reported in this regard: the speed of ships increases with mass to the power of 1/6 along the same curve as fishes, and planes similarly follow the curve for birds [15]. A potentially related observation was made by Marden and Allen [16] who found strong similarities in mass-force relations of animals and human-made motors. Isalgue’s [15] observation is intriguing and raises further questions to ask: Does such a relation apply to ground-mobile systems? Does the relation include energy expenditures? What is the extent of differences between biological and artificial relations of power, speed, and mass? Our paper is the first to explore these questions and provide initial answers.

Our motivation in asking these questions combines foundational and applied interests. First, we seek fundamental insights into underlying mechanisms and limits, as well as opportunities to optimize the energy envelope [8] of future artificial systems. Second, with growing interest in bio-inspired approaches to robotics, we seek to learn about the tradeoffs in speed, mass, and power of biological systems, including their behavioral and terrain navigation tradeoffs [8], as these tradeoffs may apply to robotic system design. For example, the CoT for even successful legged robots like BigDog and ASIMO is much higher than for animals [17]. Advanced and challenging design approaches are required to achieve a CoT comparable to that of animals, e.g., the case of MIT’s Cheetah robot [17,18].

If we were to know whether and to what extent the power-speed-mass relations of human-made systems exhibit a consistent relation to those of biological organisms, the designers of robotic systems would have additional guidance for specifying achievable performance targets. We illustrate this applied aspect later in the paper.

This study makes the following contributions. First, we find that artificial ground-mobile systems of multiple types and over a great range of scale comply with the same power-mass-speed relation–the Heglund formula (Eq 1)–proposed nearly 40 years ago for biological organisms [7]. To our knowledge, this has never before been reported. Second, we show that the Heglund formula does not capture well the power-mass-speed relation for artificial ground-mobile systems at the extreme end of the mass scale, starting at approximately 35,000 kg and beyond. Third, we develop a modified formula in the spirit of Heglund’s pioneering proposal but that captures the behavior of both biological and artificial systems over a greater range of mass–more than 11 orders of magnitude.

The paper is organized as follows. In the next section, we review the data we used in this study. The Results section describes our observations regarding the quantitative regularities we found in the data. After that, the Discussion section explores the meaning, implications, and limitations of our findings. The next section, An Application, offers an example of how our findings could apply to the development of future robotic vehicles. The paper ends with conclusions and recommendations for future work.

Data

In this paper, we focus on expenditures of mechanical energy and on corresponding data. Mechanical energy expenditures should not be confused with those of metabolic energy [9] which considers consumption of chemical energy of the fuel (in vehicles) or food (in animals). For example, metabolic energy expenditure by an animal is typically derived from the rate of oxygen consumption, recorded during exercise, applying an energetic equivalent of 20.1 J to 1 ml of O2 consumed, e.g., refs [1921]. Metabolic energy is outside the scope of this paper.

In the case of vehicles, we take the mechanical power output of a vehicle’s engine Pe as approximately equal (for the purposes of our allometric study) to the mechanical power expended for the vehicle’s locomotion. In doing so we neglect the energy that a vehicle may expend while stationary, e.g., for operating sensors or air conditioning, as well as the expenditures of mechanical energy for maintaining the operation of the engine itself, e.g., tanks’ cooling fans that may take 10–15% of the engine output [22, p.258]. In steady state locomotion, at constant altitude, the entire mechanical power output of the engine Pe is transformed eventually into heat and transferred to the environment of the vehicle (air and ground). This involves a complex chain of energy transformations ultimately ending in dissipative processes such as friction of sliding elements, gears, joints, and hysteresis in the rubber of tyres [22, p.228; 23].

Similarly, in the case of animals, we take the net mechanical power output of an animal’s muscles Pa as approximately equal the mechanical power expended for the animal’s locomotion. In doing so we neglect the mechanical energy that an animal may expend while stationary. In steady state locomotion, at constant altitude, the entire mechanical power output of the muscles Pa is transformed eventually into heat and transferred to the environment of the animal (air and ground). This involves a complex chain of energy transformations ultimately ending in dissipative, heat-generating processes such as inelastic deformations of tendons and muscles [2426].

However, the conceptual similarity of Pe and Pa breaks down when we turn to the ways in which the mechanical power output is experimentally measured, and the corresponding availability of experimental data. In vehicles, the mechanical power output of an engine Pe can be measured directly in several relatively simple ways, typically involving measuring the torque and angular velocity at the end of the engine’s shaft, and for vehicles the data are usually available at least for the maximum “rated” power output (see [27]) approximately corresponding to the vehicle travelling at maximum rated speed and maximum load weight. In animals, on the other hand, measuring the rate at which muscles produce and output mechanical energy Pa is extremely difficult [24] and the corresponding data are essentially unavailable.

Instead of Pa, experimental biologists measure so called external work of an animal, the rate of which we designate here as Pext. This quantity in locomotion of an animal is derived using a number of approaches [9]. Most of them assess the changes in the body’s potential and kinetic energy. The movement of the body’s center of mass can be determined either using a recording of the movement of a marker placed near the center of mass, or most commonly from the forces that the body exerts against the ground (or force plates), i.e., the ground reaction forces, often using the procedure popularized in [24]. Examples include refs [6,1113].

For the purposes of our research, the challenge is that Pext is not directly comparable to Pa. One major difference between Pext and Pa is that Pext includes the elastic energy stored in muscles and tendons of an animal [28] and as such can be significantly greater than Pa. We explore this matter in detail in the Discussion section, where we show that although Pext and Pa are fundamentally different quantities, Pext can serve as an order-of-magnitude approximation of Pa.

In the next section of the paper, we use Pext as a surrogate of Pa. We show that Pext exhibits the same regularity, i.e., complies with the same formula, as Pe. Then, in the Discussion section we return to deriving the relation between Pext and Pa, and show that Pext approximates Pa well within an order of magnitude, appropriately for our allometric study.

For biological organisms, we obtained the data on speed, mass, and power Pext via a rigorous review of experimental literature, which we believe to be exhaustive, to the best of our knowledge. These included (see Supporting information) cockroaches, spiders, crabs, humans, quails, chipmunks, dogs, kangaroos, horses, kangaroo rats, ground squirrels, spring hares, wild turkeys, penguins, stump-tailed monkeys, lemurs, greater rheas, Asian elephants, sheep, frogs, and lizards.

For artificial ground-mobile systems, our data on speed, mass, and power Pe represent diverse classes of defense-related systems (artillery systems, tanks, etc.) along with civilian transportation, construction, mining, and outdoor recreational vehicles (see Supporting information).

Results

Being interested in the relation among speed, power, and mass of systems, we focus on how artificial and biological systems compare in terms of the previously described the Heglund formula, Eq (1). Remarkably, the data suggest that the Heglund formula, originally developed for animals of up to 70 kg of mass, applies rather well to artificial systems, e.g., vehicles at least 2–3 orders of magnitude heavier.

Fig 1 compares the actual system/organism power versus power predicted by the Heglund formula. (Here the term “actual” refers to experimentally measured or estimated values in the case of biological organisms, and experimental or design specification values in the case of artificial systems.) Visual inspection suggests that both biological and artificial systems generally follow the Heglund formula over a very wide range of masses and powers of systems.

Fig 1. Comparison of mechanical power predicted by the Heglund formula vs. the actual measured or specified power.

Fig 1

The diagonal line illustrates the close agreement of predicted vs. actual values. For organisms and systems with a weight of <35,000 kg, R2 is 0.98 (on the log10 basis; throughout the paper log refers to log10).

There is, however, a visually notable deviation of actual power from the predicted power, approximately above 300–400 hp, where the data points refer mainly to tanks and heavy trucks.

Excluding, for the time being, all data points above the 35,000 kg limit, the R2 between predicted and actual power (on the log10 scale) for the entire set comprising both biological and artificial systems is 0.988. The R2 for biological organisms is 0.989, and R2 for artificial systems 0.945. To further assess whether the Heglund formula applies equally well to biological organisms and artificial systems below 35,000 kg, we performed an analysis of covariance (ANCOVA) to compare the slope and intercept of the regression line fitted to organism data to the slope and intercept of the regression line fitted to artificial system data (Fig 2). We found no statistically significant difference between the intercepts (0.0160; p-value = 0.985) and the slopes (0.0214; p-value = 0.357).

Fig 2. Log of actual power versus predicted power for organisms and artificial systems.

Fig 2

Below 35,000 kg, both organisms and artificial systems fit well the line with slope 0.946 ± 0.125 and intercept -0.0830 ± 1.20. There is no statistically significant difference in slopes (p-value = 0.357) and intercepts (p-value = 0.985). For systems over 35,000 kg, however, the curve fit is distinctly different.

To include systems with a mass greater than 35,000 kg, we developed a new formula, Eq (2). The formula takes inspiration from the Heglund formula, in the sense that it approximates the power expended by a system as a product of two functions–a function of the system’s mass and a function of the system’s speed. Unlike the Heglund formula, the proposed formula also takes into account the deviations at high mass values (Fig 3). Specifically, we assumed a piecewise-linear model and used multiple linear regression to identify the coefficients in the following:

P=A·Mb·Vc, (2)

or

logP=a+b·logM+c·logV (2a)

where a = 0.006, b = 0.986, c = 1.12 for M<35,000kg, and otherwise, a = 2.99, b = 0.489, c = 0.485; here P is power in watts, M is mass in kilograms, and V is speed in meters per second. The confidence intervals (at 0.95) for the intercepts and coefficients are listed in Table 1.

Fig 3. Comparison of actual measured or specified power vs. mechanical power predicted by Eq (2).

Fig 3

The diagonal line illustrates the close agreement of predicted vs. actual values. For the entire set of organisms and systems, R2 is 0.987.

Table 1. Confidence intervals (at the 0.95 level) for intercepts and coefficients using Eq (2a).

N a b c
Below 35,000 kg 260 [-0.0535, 0.0655] [0.965, 1.01] [1.05, 1.18]
Above 35,000 kg 50 [2.22, 3.75] [0.315, 0.663] [-0.239, 0.731]

With this formula (which for the sake of brevity, we refer to as the KGP formula, from the initials of the authors), the R2 for the entire set of data (comprising both biological organisms and artificial systems) is 0.987 and the mean absolute percentage error (MAPE) is 0.0269 both on the log10 basis. For M<35,000kg, a simplified formula P = 1.01·M·V provides a close approximation, with fit only marginally worse than by using Eq 2 and coefficients of Table 1.

As seen in Fig 3, the data for lower values of power (and, generally, lower mass) refer mainly to biological organisms, while the data for higher values of power (and mass) refer to artificial systems.

Discussion

Let’s begin the discussion by revisiting the question of relation between Pa and Pext which we introduced earlier in the Data section. In the following, we build on the approach and data of Cavagna and co-workers [28]. Per Eqs 5 and 6 of [28], neglecting the negative work of muscles (as [28] does), the efficiency γ with which muscles transform chemical energy into positive work is γ = Pa/Pmet = (Pext + Pint−Pelast)/Pmet, where Pa and Pext were introduced earlier, Pint is the rate of work associated with movements of an animal’s limbs with respect to its center of gravity, Pelast is the power recycled via elastic storage within an animal’s limbs, and Pmet is the chemical power input to muscles. Per [28], γ ranges from 0.2 to 0.3, and empirical values of α = Pext/Pmet range from 0.15 to 0.75, for a number of species (rhea, turkey, spring hare, kangaroo, dog and monkey).

Then, rearranging, the mechanical power output produced by muscles (comparable conceptually to the mechanical power output of an engine) Pa = γ·Pmet = Pext + Pint−Pelast = (γ/α)·Pext. Taking the range of values of γ and α mentioned above, we find that the values of Pa/Pext = γ/α are in the range 0.27–2.0.

Therefore, although Pext and Pa are not directly comparable, Pext can serve as an order-of-magnitude approximation of Pa. Although the range of values above suggest that Pext could be twice smaller or nearly 4 times larger than Pa, this is acceptable for our allometric, order-of-magnitude study. For example, to become an outlier in Fig 3 (see the discussion of outliers later in this section), a data point would have to disagree with the predicted value of power by a factor of approximately 5. And although the values of α provided in [28] cover only 6 species, Fig 3 illustrates that data for many other species fall into the same pattern, consistent with the premise that Pext can serve as an order-of-magnitude approximation of Pa.

With this, returning to the results of the preceding section, we see a strong similarity between biological and artificial systems in terms of the relation among speed, mass, and mechanical power of locomotion: both organisms and artificial systems agree closely with the Heglund formula (Fig 1) and its extension, the KGP formula (Fig 3 and Eq (2)).

This is remarkable for several reasons. First, the agreement covers an enormous range of mass and power values–over 11 orders of magnitude in mass, from a cockroach (less than 1 g) to a loaded freight train (nearly 100,000,000 kg) and 12 orders of magnitude in terms of mechanical power.

Second, the Heglund formula was originally based on data limited to only a few animals with masses not exceeding 70 kg. There is no obvious reason why it should continue to be as valid when extrapolated to systems of dramatically greater mass–up to 3 orders of magnitude greater, about 35,000 kg (Fig 1).

Third, the Heglund formula was developed originally for biological organisms only. It is notable that the formula is also valid for systems of entirely different morphology and functionality, such as trucks and tanks of up to 35,000 kg in mass.

Turning to the KGP formula, let us first mention outliers. Following [29], we determined data to be an outlier if the standardized residual was greater than three scaled median absolute deviation (MAD) from the median standardized residual. Out of 316 points in the data set, only 15 are outliers. Most of them are bicycles and elephants, not surprisingly as both of these have been discussed in prior literature as remarkably efficient in terms of energy cost of locomotion. Bicycles had been mentioned as outliers in [30] and elephants’ external mechanical CoT had been found in [31] to be far lower than any other animal.

Continuing to explore the KGP formula, and particularly its coefficients (Table 1), we note that for organisms and systems below 35,000 kg, the exponent for mass b is close to 1.0, similar to the Heglund formula (Eq 1). The exponent for speed c is higher than 1.0, i.e., the power grows nonlinearly with speed, also similar to the Heglund formula. To put it differently, the mechanical CoT, P/(M·V), increases with speed. This is a trend common for many mobile systems, as reflected in the Gabrielli–von Karman diagram [32].

Then, as systems become heavier, approximately above 35,000 kg, the relation among power, mass, and speed enters a very different regime. As seen in Table 1, power depends on mass with an exponent significantly less than 1.0. Furthermore, the dependence of power on speed diminishes. To put it differently, the CoT (or the specific resistance in the Gabrielli–von Karman terminology) becomes less dependent on speed and diminishes with mass proportionately to M(b-1), where b is between 0.315 and 0.663 (Table 1). What could explain this behavior?.

The literature offers numerous explanations for the diverse allometric relations among mass, body length, speed, and power expenditures of biological organisms. Typically, such explanations build on the organism’s need to minimize energy expenditures or the need to maintain acceptable level of stress in bones (see Supporting information). In a similar spirit, we too offer an explanation of why, as we have shown in this paper, heavy mobile systems’ CoT diminishes with mass, proportionately to M(b-1), where b is between 0.315 and 0.663.

For a system like a heavy tank, a key constraint on its speed is the sheer stress S it imposes on the ground, which cannot exceed a soil-dependent value of Smax [33]. Such a system expends power P ~ S·F·V, where F is the system’s footprint–the area of contact with the ground [34]. A heavy system attempting to reach its maximum speed is likely to be limited by Smax, a constant for a given soil type and its moisture content [35]. Therefore, its power P ~ Smax ·F·V. Then, P/(M·V) ~ (Smax·F)/M. Because the footprint is proportional to the square of a system’s linear dimension, which in turn is proportional to M1/3, we have P/(M·V) ~ (Smax·M 2/3)/M, and therefore P/(M·V) ~ Smax·M(-1/3). This is qualitatively consistent with our findings.

Having offered an explanation for one of our key findings, we cannot however recommend giving it too much credence. We are reluctant to rely on explanations that are mono-casual in nature, e.g., based on a stress within the system or optimization of energy consumption, etc. To explore this point, let’s consider the remarkable multiplicity of factors governing the maximum speed that a vehicle of a given gross weight can develop using a given source of power (e.g., an internal combustion engine).

For this purpose, we refer to the NATO Reference Mobility Model [35,36], extensively developed over several decades and experimentally validated on thousands of vehicle tests in multiple countries. For example, Vong et al. [37] explore how a given vehicle’s speed can be limited by dozens of different constraints involving soil properties, terrain characteristics, drivers tolerance for shocks, vehicles geometry and features (see Supporting information).

The constraints that govern the maximum speed and power requirements of an artificial, engineered ground-mobile system are complex and multi-faceted, involving multiple heterogeneous factors and interacting among themselves in diverse ways. This may be even more so in case of intricate biological systems. As such, future work must look beyond mono-causal explanations for the allometric relations discussed in this paper.

An application

The findings of this paper are particularly relevant to designing robotic, ground-mobile systems. For one thing, robotics tends to have a significant theoretical and practical affinity to bio-inspired approaches and analogies. The growing interest in legged robots is one example. As such, the common regularity of biological and artificial systems is of interest. Furthermore, like biological organisms, robotic systems used for defense applications are more likely to operate on offroad terrain than a typical transportation vehicle [38], and our data collection strategy includes a broad range of data relevant to offroad locomotion.

Determining the feasible yet ambitious targets for tradeoffs among the power, speed, and mass of future terrestrial robots, particularly for defense applications, is a difficult task. It is undesirable to base such targets on current experience, because military hardware is often developed and used for multiple years and even decades; therefore, the specifiers and designers of such hardware must base their targets–competitive yet achievable–on future technological opportunities not necessarily fully understood at the time of design.

To be sure, much research literature discusses detailed models for the analysis and design optimization of power-efficient robots, e.g., refs [17,18,34,39]. Here our intent is different: we explore how robotic applications can benefit from the KGP relation. Since the KGP formula allows the designer of a robotic system to estimate power requirements from the system’s desired mass and speed, it may help serve as a preliminary check of the design’s realism and potential performance bounds.

Here, we consider a preliminary design concept–a quadrupedal robotic “mule” that we call Exploratory Design for Mule-like Equipment Carrier (EDMEC). EDMEC weighs 600 kg and travels at a speed of 2 m/s. EDMEC is envisioned to carry a payload up to 90 kg [40] consisting of munitions, food, extra batteries, and communication equipment. This quadrupedal system will be able to travel in complex terrains (dense forests, rocky plains, and moderately difficult mountain trails) and over obstacles like building rubble. We estimated the total power required for EMDEC locomotion as 5 kW (see Supporting information).

However, the KGP formula predicts that a 600 kg vehicle moving at a speed of 2 m/s would need 1,200 W of power. This means that EMDEC consumes 4.1 times more power than predicted by the KGP formula. Is something wrong with EMDEC’s design or our power consumption model? Not necessarily.

Consider Fig 4, where we plotted a number of robotics systems in comparison with the data in Fig 3. These systems include a number of commercially available or fielded systems (green asterisks), research systems (green squares), and the EMDEC concept (the purple star). Most of these data points are positioned well above the diagonal curve, indicating that the corresponding systems consume more power than the KGP formula predicts based on animals and conventional (tracked or wheeled) vehicles.

Fig 4. Fielded and experimental robotic systems—Legged, tracked, and wheeled—Compared with the data in Fig 3.

Fig 4

Particularly notable are the legged systems that lie significantly above the curve: the University of Maryland Micro-robot [41], NASA Valkyrie [42], and Boston Dynamics Atlas [43]. These systems consume 64, 52, and 60 times more power, respectively, than the curve predicts (Fig 4). Agility Robotics Digit [44] is another outlier. Two of the most efficient walking robots, the Cornell Ranger [38] and the MIT Cheetah [17], use 3.0 and 3.6 times the power predicted by the KGP curve, respectively.

On the other hand, we should also note there are three data points that are close to, or even below, the curve and whose power is of the same order of magnitude as EMDEC. These are wheeled or tracked systems (Clearpath Robotics Jackal [45] and Warthog [46], and iWarrior 710 [47]), which tend to be more efficient than their legged counterparts [17,48].

The relative inefficiency of legged systems is a common topic of discussions in literature, e.g., [17,4951]. In fact, many ground vehicles lag behind their animal counterparts in movement efficiency when not moving on specially prepared surfaces like roads [1517,52]. Much of the legged robots’ inefficiency can be explained by the lack of passive elements like tendons in animals [4]. Passive elements allow for energy to be stored and recycled back into the system, thus increasing efficiency [17]. In fact, animal tendons can contribute up to 45% of the power required for locomotion in kangaroos and 40% in horses and camels [4]. Another reason for why artificial systems perform less efficiently than animals is due to difficulties and inefficiencies in sensing and path planning [53].

Although attractive for efficiency reasons, including passive elements in the design of a legged robotic system often comes at the cost of reducing the system’s versatility. Passive elements that recycle energy back into the system restrict the movement of appendages and often need to be empirically tuned to specific operating environments [17,54]. Without passive elements, a legged robot sacrifices some efficiency but gains adaptability to variable environments [55], which helps it move in difficult environments inaccessible to more efficient wheeled and tracked vehicles.

Conclusions

We found that artificial ground-mobile systems–as diverse as ground robots, small utility vehicles, trucks, and tanks–exhibit a consistent regularity of relation among mass, power, and speed. For the range of mass from 1 g to 35,000 kg, this regularity is similar to the Heglund formula, known since 1980s and applied to a range of ground-mobile animals. Therefore, a single formula describes organisms and systems, from a cockroach to a battle tank.

These findings point to a fundamental similarity between biological and artificial locomotion that transcends great differences in morphology, mechanisms, materials, and behaviors.

We also show that for very heavy vehicles, ranging approximately 35,000–100,000,000 kg, the relation among power, mass, and speed enters a different regime. The CoT (or the specific resistance in the Gabrielli–von Karman terminology) becomes less dependent on speed and also diminishes with mass, proportionately to M(b-1), where b is on the order of 0.5.

To cover the two different regimes–both below and above 35,000 kg–we propose a piecewise-linear regression formula that closely agrees with the available data. The agreement covers enormous ranges of mass and power values–over 11 orders of magnitude in mass, from a cockroach (less than 1 g) to a loaded freight train (nearly 100,000,000 kg), and over 12 orders of magnitude in terms of mechanical power.

When the proposed formula is considered in relation specifically to an important class of future ground vehicles–legged robots–we note a consistent inefficiency in current designs: the power consumption is from 3 to 60 times greater than predicted by the formula. In other words, today’s legged robots are significantly less efficient than animals or tracked and wheeled vehicles of comparable speed and mass. This, however, may be the inevitable price to pay to allow them to adapt to diverse and difficult terrains.

With regard to theoretical explanations of these empirical findings, we note that the constraints governing the maximum speed and power requirements of an artificial ground-mobile system are numerous, complex, and multi-faceted, involving multiple heterogeneous factors and interacting among themselves in diverse ways. This may be even more so in case of intricate biological systems. As such, we find it difficult to give too much credence to theories that are mono-casual in nature, e.g., based on a stress within the system or optimization of energy consumption. Future work must explore the theoretical space beyond mono-causal explanations for the allometric relations discussed in this paper.

Supporting information

S1 File

(DOCX)

Acknowledgments

The views presented in this paper are those of the authors and not of their employer. Phyllis Mcgovern of CCDC Army Research Laboratory (ARL) searched for multiple books and articles that supplied the raw data for this research. Jody Priddy of the U.S. Army Engineer Research and Development Center assisted with obtaining data related to numerous ground vehicles. Carol Johnson, the ARL editor, improved the style and the grammar of the manuscript.

Data Availability

All relevant data are within the paper and its Supporting information files.

Funding Statement

The authors received no specific funding for this work.

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Decision Letter 0

Hussain Md Abu Nyeem

28 Aug 2020

PONE-D-20-21456

From Cockroaches to Tanks: the Same Power-Mass-Speed Relation Describes both Biological and Artificial Ground-Mobile Systems

PLOS ONE

Dear Dr. Kott,

Thank you for submitting your manuscript to PLOS ONE. After careful consideration, we feel that it has merit but does not fully meet PLOS ONE’s publication criteria as it currently stands. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

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Hussain Md Abu Nyeem, Ph.D.

Academic Editor

PLOS ONE

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Reviewer #1: Partly

Reviewer #2: Yes

**********

2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: I Don't Know

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The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #2: Yes

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PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

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5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: The paper investigates allometric relationship of mechanical power expended per unit of momentum (cost of transportation, CoT) for a wide range of natural and artificial systems exhibiting terrestrial locomotion. Authors find that the previously known relationship proposed for the mass range of 10^-3-10^1 kg by Heglund [13] holds over a much wider range of masses, 10^-3-10^4 kg, in animals and engineered systems alike. They also analyze the data available for engineered systems in the range of 10^4-10^6 kg and find that a qualitatively different scaling law applies for that range. Two linear functions describing CoT in the sub-ranges are fitted to the data. The resulting piecewise-linear relation holds for the whole range of masses that was considered (10^-3-10^6 kg). The relationship is additionally verified by checking that it holds on the data on sauropods and elephants that was not used in fitting of the empirical law, and finding that the data agrees with the law. Some existing ground-based robotic systems are considered in the context of the considered allometric relations and, for the most part, are found to be outliers. Implications of this fact for design of such systems are discussed.

All the claimed findings are, to the best of my knowledge, novel. While allometric studies that include both animals and engineered systems are not unprecedented (e.g. ref [39, 17] of the manuscript), no systematic studies of that sort were done before for terrestrial locomotion. Pre-existing work is properly cited.

Data collection methods used in the study are mostly sound. the only issue I found was the method in which the elephants and sauropods data was obtained. Mechanical power expended by the animals is derived from literature estimates of metabolic power by multiplying it by a constant factor. The factor is taken from the study on horses ([27], masses around 5e2 kg) and used for animals with masses at least two order of magnitude larger. Meanwhile, in Introduction the authors mention that the metabolic and mechanical cost of transportation scales differently. That makes the proportionate estimate dubious at best.

I ask that authors do one of the following:

1) provide a justification for proportional estimation of mechanical cost of transport from the metabolic cost, for the relevant mass range, or

2) provide a more careful estimation of mechanical cost of transport for elephants and sauropods and redo the related analysis and Figure 4, or

3) drop the elephant and sauropod data analysis from the paper altogether.

Another issue with this part of the study is that the data, while available in raw form in the primary sources, is processed to obtain the mechanical CoT estimates. It would be beneficial to make the processed data available.

Also, Figure 4 is cluttered. Please only show the relevant range of masses and consider dropping the data for animals and artificial systems other than elephants and sauropods.

This issue, however, is minor, as it the data is only used to provide additional support to a claim established with other data. Even if that part of the study is removed its primary claims can be sufficiently well supported.

Data analysis methods are sound. There is a minor presentation issue with ANCOVA analysis at the bottom of page 4: a single value is given as "difference" between slopes, and the value (0.964) is too large to be the true absolute difference between slopes that are close to 1. Please provide both of the slopes with confidence intervals.

Another minor issue encountered throughout the paper: values are reported to the third digit of the error margin. It is customary, at least in physical sciences, to round error margins down to one significant digit (two if the first one is 1) and also round the point estimate to the same decimal. For example, 0.964 \\pm 0.0224 becomes 0.96 \\pm 0.02. Similarly, for p-values usually only one significant digit is reported. Such conventions vary by the discipline, so I won't ask an adherence to this one, but in my opinion it could improve readability of the paper.

There is also a similar minor issue with the power estimate for EDMEC given in the Supplementary. The estimate is valid, but crude and must be treated as such. In light of that, the power consumption estimate of 4920W should be truncated to a single significant digit and presented as 5kW.

Language-wise, the manuscript is well-organized and accessible. There are a few places with typos and unclear language (listed below), but that is easily fixable and did not affect my ability to understand the intent of authors.

I recommend that the paper is accepted for publication after these issues are addressed.

----------------

Abstract:

"We show empirically not only..." - possible forgotten "that"

Introduction:

"metabolic rate scales approximately to the 3/4 power of the organism's mass" - awkward wording

In the discussion of CoTm, a typo: "P/(M*V)" -> "Pm/(M*V)"

Results:

p.10 last paragraph: "the slopes and intercepts of organism and system regression lines" - unclear

Supplementary:

The explanation of power expenditure section: "...is on the order of a magnitude or nearly constant magnitude of 10 body lengths per second..." - awkward

Reviewer #2: The authors test how predictable the relationship between mass and mechanical power is for biological and artificial systems based on a previously proposed formula. The authors extend the formula to consider systems of larger mass, where the previously proposed formula failed. The authors then use this metric to analyze the efficiency of current artificial legged walkers and find that for the most part they are several times more inefficient than predicted by the formula. They discuss the reasons for this departure and argue for more biologically inspired technologies as a direction forward. The manuscript is straightforward, well written, and technically sound.

**********

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Reviewer #1: Yes: Anton Bernatskiy

Reviewer #2: No

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Decision Letter 1

Hussain Md Abu Nyeem

9 Nov 2020

PONE-D-20-21456R1

From Cockroaches to Tanks: the Same Power-Mass-Speed Relation Describes both Biological and Artificial Ground-Mobile Systems

PLOS ONE

Dear Dr. Kott,

Thank you for submitting your manuscript to PLOS ONE. All the comments of the editor and earlier reviewers have been addressed well. However, a few questions about the comparison measures and the implications of the given data need further clarification. Therefore, we invite you to submit a revised version of the manuscript that addresses the points raised during the review process.

Note PLOS ONE strives to facilitate timely review with our continued effort to improve the speed and quality of the review process. However, please understand that due to unavoidable circumstances of the academic editor, your manuscript experienced an unusual delay this time. 

Please submit your revised manuscript by Dec 24 2020 11:59PM. If you will need more time than this to complete your revisions, please reply to this message or contact the journal office at plosone@plos.org. When you're ready to submit your revision, log on to https://www.editorialmanager.com/pone/ and select the 'Submissions Needing Revision' folder to locate your manuscript file.

Please include the following items when submitting your revised manuscript:

  • A rebuttal letter that responds to each point raised by the academic editor and reviewer(s). You should upload this letter as a separate file labeled 'Response to Reviewers'.

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If you would like to make changes to your financial disclosure, please include your updated statement in your cover letter. Guidelines for resubmitting your figure files are available below the reviewer comments at the end of this letter.

If applicable, we recommend that you deposit your laboratory protocols in protocols.io to enhance the reproducibility of your results. Protocols.io assigns your protocol its own identifier (DOI) so that it can be cited independently in the future. For instructions, see: http://journals.plos.org/plosone/s/submission-guidelines#loc-laboratory-protocols

We look forward to receiving your revised manuscript.

Kind regards,

Hussain Md Abu Nyeem, Ph.D.

Academic Editor

PLOS ONE

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Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #3: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #3: Partly

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: Yes

Reviewer #3: No

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #3: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: All of the issues I pointed out in my review have been fully addressed. The paper now satisfies all the requirements of PLOS ONE: it reports a novel result and it is technically sound. The reviewer thanks the authors for a good read!

Reviewer #3: The biggest challenges to this paper is in understanding the different metrics being used for ‘system/organism power’, perceiving whether these different metrics are reasonably comparable, and in interpreting the implications of the presented relationships.

Comparing metrics…

It is reasonable to begin with the Heglund (Cavagna, Taylor, Fedak) studies of the 1980s for the broad-brush scaling data and exponent fits. Of the three I recall (metabolic, center of mass and center of mass + ‘internal’) the third is selected for the initial scaling equation (Heglund et al. 1982 IV). This is the energy put into the center of mass added to the energies of the limbs about the center of mass (with this metric, it is assumed there is no transfer between the two). However, it is the second that is used for the majority of the biological data survey. Why not use center of mass power for both (Heglund et al., 1982 III)? Power proportional to mass and velocity (so a constant mechanical cost of transport): this appears to provide a better fit to the data too ( Table 1: a=0; b=1; c=1?). A bigger issue is that neither form for mechanical power is (and is acknowledged to be) a very poor predictor for the metabolic or ‘biological engine’ power.

But what is the ‘system’ power being described for the vehicles? It is presumably not the direct equivalent to the mechanical power demand of the animals – on flat level ground at constant speed this would be zero. Presumably it is the power supplied by the engine…? Under what condition? Maximum power or maximum speed?

And then, what of the horse-drawn guns? Is the work calculated the ‘animal’ way or the ‘machine’ way?

And so it is not immediately clear to me that the chosen animal and machine powers are reasonably comparable.

Implications…

If we believe there is some valid equivalency between the two metrics for power, the striking finding is the lack of evidence that a wheel improves matters. If I were to start off with a one-human-power runner (measured the animal way), and then put the human mass on a bicycle, I would hope one human-power to drive either a much more massive load or to travel much more quickly. That this is not evident across the data presented (compare 1000kg bull v.s truck) leads me to wonder whether 1) the two metrics for power are not comparable, or 2) trucks and tanks are horribly un-wheel-like. Where does a motorbike on a road sit on this line? And a small train on a railway track? It would be nice to see where a couple of ‘good’ (fast or economical) wheeled vehicles sit on this plot.

Minor points

To offer ‘data on request’ or ‘see pdf’ is not very 2020. The data are indeed available online

https://apps.dtic.mil/sti/pdfs/AD1098609.pdf

(Which may bring into question the issue of novelty – that is a policy decision outside my remit) but why not provide them as a spreadsheet so that the reader can easily start trying out their own statistical approaches?

The scaling relationship for the maximal speed in running animals falls over a bit at the larger sizes (Garland etc.)

Please double check the values taken from Heglund – there may be an issue with conversion to SI units. See Blickhan, R. & Full, R. J. 1987 Locomotion energetics of the ghost crab II. Mechanics of the center of mass during walking and running. J. Exp. Biol. 130, 155-174.

It appears odd to resort to using metabolics to derive the elephant ‘animal-power’. Does not Genin, Willems, Cavagna, Lair and Heglund (J. Exp. Biol., 2010) provide a more appropriate starting point? It may be that the elephant data point would then fit rather poorly: note that Genin et al. report CoM energy fluctuations 1/3rd that of smaller mammals.

And including sauropods as empirical points does feel a bit of a stretch.

**********

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Reviewer #1: Yes: Anton Bernatskiy

Reviewer #3: No

[NOTE: If reviewer comments were submitted as an attachment file, they will be attached to this email and accessible via the submission site. Please log into your account, locate the manuscript record, and check for the action link "View Attachments". If this link does not appear, there are no attachment files.]

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PLoS One. 2021 Apr 26;16(4):e0249066. doi: 10.1371/journal.pone.0249066.r004

Author response to Decision Letter 1


22 Dec 2020

The comments of the first 2 reviewers have been already answered to their satisfaction in previous revisions of the paper. This revision addresses the comments of Reviewer #3, and a detailed Response to Reviewer 3 has been provided as a file included in this submission.

Attachment

Submitted filename: Authors Responses to Reviewer 3.docx

Decision Letter 2

Hussain Md Abu Nyeem

15 Jan 2021

PONE-D-20-21456R2

From Cockroaches to Tanks: the Same Power-Mass-Speed Relation Describes both Biological and Artificial Ground-Mobile Systems

PLOS ONE

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Hussain Md Abu Nyeem, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments (if provided):

The paper has been significantly improved and addressed all the major questions of the previous reviewers.

However, the academic editor is still interested in learning how the remaining questions of the current reviewer are addressed.

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

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Reviewer #3: (No Response)

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2. Is the manuscript technically sound, and do the data support the conclusions?

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Reviewer #3: Partly

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3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

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Reviewer #3: Yes

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Reviewer #3: Yes

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6. Review Comments to the Author

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Reviewer #3: The major issue with this paper is that it assumes comparability between two potentially quite different forms of power.

The vehicle values are for engine power, if possible, the ‘rated power’ (responses). This is the power (torque x angular velocity) at the end of the drive shaft. The rated power is useful in informing (once other losses are considered, and given suitable gearing) the capacity of a vehicle to accelerate, pull a load up an incline, or overcome drag.

The animal values are the rate of mechanical work of the center of mass during steady state locomotion.

Is it reasonable to assert an equivalency between ‘rated power’ and ‘center of mass power’? The difficulty is that the ‘center of mass power’ of a wheeled vehicle at any steady speed (even exceedingly high, and against drag) on level ground is zero. So ‘rated power’ cannot sensibly translate to ‘center of mass power’. But is the reverse likely? Does the center of mass power of an animal display something equivalent to its rated power? One can certainly imagine cases where this fails (consider cycling), but might it be reasonable for legged locomotion?

For the purposes of this paper, it would appear sufficient to state it as an assumption that it is reasonable, with whatever justification can be thought of and while acknowledging that others have also made this assumption.

At the moment, this is not sufficiently addressed. The term ‘rated power’ only appears in the responses – a description of the vehicle power close to the one I give above is required. Also in the responses is the justification:

“We do believe that for all systems (biological or artificial) in our study we are looking at fundamentally the same metrics: the amount of mechanical energy expended to propel the system.”

This is insufficient. Why is the center of mass power (that can be zero given wheels) ‘the amount of mechanical energy expended to propel the system’. Until an explicit work-around is given for this, any informed reader will view this study as a comparison of apples and oranges.

I wonder whether the biological literature is as exhaustive as claimed. I would suggest doing a citation search on Cavagna, 1975 ‘force platforms as ergometers’. Off the top of my head, are the reported values for cats, tortoise, penguins all unusable? Any lizards?

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Reviewer #3: No

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PLoS One. 2021 Apr 26;16(4):e0249066. doi: 10.1371/journal.pone.0249066.r006

Author response to Decision Letter 2


21 Feb 2021

We accepted the reviewer's comments and provided revision accordingly. See the Response to Reviewers document provided with this submission.

Attachment

Submitted filename: Authors Responses to Reviewer 3 for Rev5.docx

Decision Letter 3

Hussain Md Abu Nyeem

11 Mar 2021

From Cockroaches to Tanks: the Same Power-Mass-Speed Relation Describes both Biological and Artificial Ground-Mobile Systems

PONE-D-20-21456R3

Dear Dr. Kott,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

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Kind regards,

Hussain Md Abu Nyeem, Ph.D.

Academic Editor

PLOS ONE

Additional Editor Comments:

The paper has been significantly improved and reasonably addressed the previous comments of the reviewers. Upon the 'ACCEPT' recommendations of the all the three reviewers, and seeing the improvements in the revised versions, the academic editor is now also convinced for its publication. 

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #3: All comments have been addressed

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2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #3: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #3: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #3: Yes

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5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #3: Yes

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6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #3: I am grateful for the consideration given to my previous comments. I shall give a couple of additional thoughts, but certainly do not require further responses.

I would agree that the external mechanical power of a legged locomotor might be taken as a reasonable – at least order of magnitude – estimate of the minimum actuator work. Elastic mechanisms may play some role, and mean that it cannot be taken as an absolute minimum value, but the effect of these are likely – at the scales of interest here – to be negligible. However, the true actuator (muscle or engine) work may be much, much higher, and this may not necessarily be covered by an ‘order of magnitude’ argument. ‘Internal’ mechanical work demands may be significant; and external work could approximate zero. The Adaptive Suspension Vehicle (Waldron et al., 1984) carried its driver horizontally and steadily: external power approximately zero. However, the motor power is not.

So: cases can be imagined where the ‘apples with apples’ might not be true. How important this is (after all, horses really do not look at all like the ASV) to interpreting the current study can, in my view, now be left to the reader.

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Reviewer #3: No

Acceptance letter

Hussain Md Abu Nyeem

15 Apr 2021

PONE-D-20-21456R3

From cockroaches to tanks: the same power-mass-speed relation describes both biological and artificial ground-mobile systems

Dear Dr. Kott:

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on behalf of

Dr. Hussain Md Abu Nyeem

Academic Editor

PLOS ONE

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