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Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off.

Berghänel A, Schülke O, Ostner J - Sci Adv (2015)

Bottom Line: The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences.Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits.Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Ecology, University of Göttingen, 37077 Göttingen, Germany.

ABSTRACT
The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences. Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits. Prominent theories propose that locomotor play is (i) low cost, using surplus energy remaining after growth and maintenance, and (ii) beneficial because it trains motor skills. However, both theories are largely untested. Studying wild Assamese macaques, we combined behavioral observations of locomotor play and motor skill acquisition with quantitative measures of natural food availability and individual growth rates measured noninvasively via photogrammetry. Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth. Even under moderate natural energy restriction, investment in locomotor play accounted for up to 50% of variance in growth, which strongly contradicts the current theory that locomotor play only uses surplus energy remaining after growth and maintenance. Male immatures played more, acquired motor skills faster, and grew less than female immatures, leading to persisting size differences until the age of female maturity. Hence, depending on skill requirements, investment in play can take ontogenetic priority over physical development unconstrained by costs of play with consequences for life history, which strongly highlights the ontogenetic and evolutionary importance of play.

No MeSH data available.


Energy trade-off between locomotor play and growth.Red, female; blue, male. Residual plots of the individual values for the whole study period (Pearson partial correlations controlled for average food availability and lactation category; n = 12). 1Residuals are translated into deviations from average in percentage. (A) Growth rate over locomotor play (r = −0.889, P < 0.001); additionally controlled for sex (no figure): r = −0.785, P = 0.002; additionally controlled for average play intensity (no figure): r = −0.895, P < 0.001. (B and C) Growth rate (r = 0.612, P = 0.060) and locomotor play (r = −0.759, P = 0.011) over resting time. (D and E) Growth rate (r = −0.037, P = 0.919) and locomotor play (r = 0.155, P = 0.668) over feeding time.
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Figure 1: Energy trade-off between locomotor play and growth.Red, female; blue, male. Residual plots of the individual values for the whole study period (Pearson partial correlations controlled for average food availability and lactation category; n = 12). 1Residuals are translated into deviations from average in percentage. (A) Growth rate over locomotor play (r = −0.889, P < 0.001); additionally controlled for sex (no figure): r = −0.785, P = 0.002; additionally controlled for average play intensity (no figure): r = −0.895, P < 0.001. (B and C) Growth rate (r = 0.612, P = 0.060) and locomotor play (r = −0.759, P = 0.011) over resting time. (D and E) Growth rate (r = −0.037, P = 0.919) and locomotor play (r = 0.155, P = 0.668) over feeding time.

Mentions: Controlling for temporal variation in food availability, we found a strong negative correlation between individual growth rates and time spent in locomotor play (Fig. 1A, see also fig. S7). The range in locomotor play time (4.6 to 12.2% activity time; mean ± SD, 7.7 ± 2.3%) accounted for a difference in growth rate of about 30% (Fig. 1A). This energy trade-off was not caused by time constraints on feeding behavior, because resting time, not feeding time, was traded in for locomotor play time (Fig. 1, B to E, and fig. S8). The trade-off between play and growth was also independent of infant sex, and both sexes fit the same regression line (Fig. 1A). All the infants spent time in locomotor play during periods of low food availability even though low food availability also slowed down growth (Fig. 2).


Locomotor play drives motor skill acquisition at the expense of growth: A life history trade-off.

Berghänel A, Schülke O, Ostner J - Sci Adv (2015)

Energy trade-off between locomotor play and growth.Red, female; blue, male. Residual plots of the individual values for the whole study period (Pearson partial correlations controlled for average food availability and lactation category; n = 12). 1Residuals are translated into deviations from average in percentage. (A) Growth rate over locomotor play (r = −0.889, P < 0.001); additionally controlled for sex (no figure): r = −0.785, P = 0.002; additionally controlled for average play intensity (no figure): r = −0.895, P < 0.001. (B and C) Growth rate (r = 0.612, P = 0.060) and locomotor play (r = −0.759, P = 0.011) over resting time. (D and E) Growth rate (r = −0.037, P = 0.919) and locomotor play (r = 0.155, P = 0.668) over feeding time.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4643810&req=5

Figure 1: Energy trade-off between locomotor play and growth.Red, female; blue, male. Residual plots of the individual values for the whole study period (Pearson partial correlations controlled for average food availability and lactation category; n = 12). 1Residuals are translated into deviations from average in percentage. (A) Growth rate over locomotor play (r = −0.889, P < 0.001); additionally controlled for sex (no figure): r = −0.785, P = 0.002; additionally controlled for average play intensity (no figure): r = −0.895, P < 0.001. (B and C) Growth rate (r = 0.612, P = 0.060) and locomotor play (r = −0.759, P = 0.011) over resting time. (D and E) Growth rate (r = −0.037, P = 0.919) and locomotor play (r = 0.155, P = 0.668) over feeding time.
Mentions: Controlling for temporal variation in food availability, we found a strong negative correlation between individual growth rates and time spent in locomotor play (Fig. 1A, see also fig. S7). The range in locomotor play time (4.6 to 12.2% activity time; mean ± SD, 7.7 ± 2.3%) accounted for a difference in growth rate of about 30% (Fig. 1A). This energy trade-off was not caused by time constraints on feeding behavior, because resting time, not feeding time, was traded in for locomotor play time (Fig. 1, B to E, and fig. S8). The trade-off between play and growth was also independent of infant sex, and both sexes fit the same regression line (Fig. 1A). All the infants spent time in locomotor play during periods of low food availability even though low food availability also slowed down growth (Fig. 2).

Bottom Line: The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences.Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits.Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth.

View Article: PubMed Central - PubMed

Affiliation: Department of Behavioral Ecology, University of Göttingen, 37077 Göttingen, Germany.

ABSTRACT
The developmental costs and benefits of early locomotor play are a puzzling topic in biology, psychology, and health sciences. Evolutionary theory predicts that energy-intensive behavior such as play can only evolve if there are considerable benefits. Prominent theories propose that locomotor play is (i) low cost, using surplus energy remaining after growth and maintenance, and (ii) beneficial because it trains motor skills. However, both theories are largely untested. Studying wild Assamese macaques, we combined behavioral observations of locomotor play and motor skill acquisition with quantitative measures of natural food availability and individual growth rates measured noninvasively via photogrammetry. Our results show that investments in locomotor play were indeed beneficial by accelerating motor skill acquisition but carried sizable costs in terms of reduced growth. Even under moderate natural energy restriction, investment in locomotor play accounted for up to 50% of variance in growth, which strongly contradicts the current theory that locomotor play only uses surplus energy remaining after growth and maintenance. Male immatures played more, acquired motor skills faster, and grew less than female immatures, leading to persisting size differences until the age of female maturity. Hence, depending on skill requirements, investment in play can take ontogenetic priority over physical development unconstrained by costs of play with consequences for life history, which strongly highlights the ontogenetic and evolutionary importance of play.

No MeSH data available.