Differentiating causality and correlation in allometric scaling: Ant colony size drives metabolic hypometry

James S. Waters, Alison Ochs, Jennifer Fewell, Jon Harrison

    Research output: Contribution to journalArticle

    1 Citation (Scopus)

    Abstract

    Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in sizereduced colonies could be due to increased anabolic processes associated with brood care and colony growth.

    Original languageEnglish (US)
    Article number20162582
    JournalProceedings of the Royal Society B: Biological Sciences
    Volume284
    Issue number1849
    DOIs
    StatePublished - Feb 22 2017

    Fingerprint

    Ants
    allometry
    Causality
    ant
    walking
    Harvesters
    Pogonomyrmex californicus
    Formicidae
    Ecology
    Nutrients
    Food
    insect colonies
    Animals
    Aptitude
    nutrient transport
    brood rearing
    metabolic studies
    Social Environment
    Social Behavior
    social insects

    Keywords

    • Allometry
    • Ants
    • Locomotion
    • Metabolism
    • Scaling
    • Social insect

    ASJC Scopus subject areas

    • Medicine(all)
    • Immunology and Microbiology(all)
    • Biochemistry, Genetics and Molecular Biology(all)
    • Environmental Science(all)
    • Agricultural and Biological Sciences(all)

    Cite this

    Differentiating causality and correlation in allometric scaling : Ant colony size drives metabolic hypometry. / Waters, James S.; Ochs, Alison; Fewell, Jennifer; Harrison, Jon.

    In: Proceedings of the Royal Society B: Biological Sciences, Vol. 284, No. 1849, 20162582, 22.02.2017.

    Research output: Contribution to journalArticle

    @article{f01f1b684de949088c89345198ef61a0,
    title = "Differentiating causality and correlation in allometric scaling: Ant colony size drives metabolic hypometry",
    abstract = "Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in sizereduced colonies could be due to increased anabolic processes associated with brood care and colony growth.",
    keywords = "Allometry, Ants, Locomotion, Metabolism, Scaling, Social insect",
    author = "Waters, {James S.} and Alison Ochs and Jennifer Fewell and Jon Harrison",
    year = "2017",
    month = "2",
    day = "22",
    doi = "10.1098/rspb.2016.2582",
    language = "English (US)",
    volume = "284",
    journal = "Philosophical Transactions of the Royal Society B: Biological Sciences",
    issn = "0800-4622",
    publisher = "Royal Society of London",
    number = "1849",

    }

    TY - JOUR

    T1 - Differentiating causality and correlation in allometric scaling

    T2 - Ant colony size drives metabolic hypometry

    AU - Waters, James S.

    AU - Ochs, Alison

    AU - Fewell, Jennifer

    AU - Harrison, Jon

    PY - 2017/2/22

    Y1 - 2017/2/22

    N2 - Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in sizereduced colonies could be due to increased anabolic processes associated with brood care and colony growth.

    AB - Metabolic rates of individual animals and social insect colonies generally scale hypometrically, with mass-specific metabolic rates decreasing with increasing size. Although this allometry has wide ranging effects on social behaviour, ecology and evolution, its causes remain controversial. Because it is difficult to experimentally manipulate body size of organisms, most studies of metabolic scaling depend on correlative data, limiting their ability to determine causation. To overcome this limitation, we experimentally reduced the size of harvester ant colonies (Pogonomyrmex californicus) and quantified the consequent increase in mass-specific metabolic rates. Our results clearly demonstrate a causal relationship between colony size and hypometric changes in metabolic rate that could not be explained by changes in physical density. These findings provide evidence against prominent models arguing that the hypometric scaling of metabolic rate is primarily driven by constraints on resource delivery or surface area/volume ratios, because colonies were provided with excess food and colony size does not affect individual oxygen or nutrient transport. We found that larger colonies had lower median walking speeds and relatively more stationary ants and including walking speed as a variable in the mass-scaling allometry greatly reduced the amount of residual variation in the model, reinforcing the role of behaviour in metabolic allometry. Following the experimental size reduction, however, the proportion of stationary ants increased, demonstrating that variation in locomotory activity cannot solely explain hypometric scaling of metabolic rates in these colonies. Based on prior studies of this species, the increase in metabolic rate in sizereduced colonies could be due to increased anabolic processes associated with brood care and colony growth.

    KW - Allometry

    KW - Ants

    KW - Locomotion

    KW - Metabolism

    KW - Scaling

    KW - Social insect

    UR - http://www.scopus.com/inward/record.url?scp=85013781656&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=85013781656&partnerID=8YFLogxK

    U2 - 10.1098/rspb.2016.2582

    DO - 10.1098/rspb.2016.2582

    M3 - Article

    VL - 284

    JO - Philosophical Transactions of the Royal Society B: Biological Sciences

    JF - Philosophical Transactions of the Royal Society B: Biological Sciences

    SN - 0800-4622

    IS - 1849

    M1 - 20162582

    ER -