Asymptotic prey profitability drives star-nosed moles to the foraging speed limit

Foraging theory provides models for predicting predator diet choices assuming natural selection has favoured predators that maximize their rate of energy intake during foraging. Prey profitability (energy gained divided by prey handling time) is an essential variable for estimating the optimal diet. Time constraints of capturing and consuming prey generally result in handling times ranging from minutes to seconds, yet profitability increases dramatically as handling time approaches zero, providing the potential for strong directional selection for increasing predator speed at high encounter rates (tiny increments in speed increase profitability markedly, allowing expanded diets of smaller prey). We provide evidence that the unusual anatomical and behavioural specializations characterizing star-nosed moles resulted from progressively stronger selection for speed, allowing the progressive addition of small prey to their diet. Here we report handling times as short as 120 ms (mean 227 ms) for moles identifying and eating prey. ‘Double takes’ during prey identification suggest that star-nosed moles have reached the speed limit for processing tactile information. The exceptional speed of star-nosed moles, coupled with unusual specializations for finding and eating tiny prey, provide new support for optimal foraging theory.

[1]  N. F. Hadley Ventilatory Patterns and Respiratory Transpiration in Adult Terrestrial Insects , 1994, Physiological Zoology.

[2]  T. Bradley,et al.  Changes in the Rate of CO2 Release following Feeding in the Insect Rhodnius prolixus , 2003, Physiological and Biochemical Zoology.

[3]  Lighton,et al.  Ant breathing: testing regulation and mechanism hypotheses with hypoxia , 1995, The Journal of experimental biology.

[4]  Alan C. Kamil,et al.  Foraging behavior: ecological, ethological, and psychological approaches , 1980 .

[5]  S. Hermann,et al.  Direct oxygen measurements in the tracheal system of lepidopterous pupae using miniaturized amperometric sensors , 1994 .

[6]  R. S. Sohal,et al.  Mitochondrial adenine nucleotide translocase is modified oxidatively during aging. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[7]  N Suga,et al.  Disproportionate tonotopic representation for processing CF-FM sonar signals in the mustache bat auditory cortex. , 1976, Science.

[8]  K. Slăma A New Look at Insect Respiration , 1988 .

[9]  R. Levy,et al.  Discontinuous respiration in insects. II. The direct measurement and significance of changes in tracheal gas composition during the respiratory cycle of silkworm pupae. , 1966, Journal of insect physiology.

[10]  S. Chown,et al.  Discontinuous gas exchange cycles in aphodius fossor (Scarabaeidae): a test of hypotheses concerning origins and mechanisms. , 2000, The Journal of experimental biology.

[11]  J. Lighton,et al.  Discontinuous Gas Exchange in the Pseudoscorpion Garypus californicus Is Regulated by Hypoxia, Not Hypercapnia , 2002, Physiological and Biochemical Zoology.

[12]  James T. Anderson,et al.  INVERTEBRATE RESPONSE TO MOIST‐SOIL MANAGEMENT OF PLAYA WETLANDS , 2000 .

[13]  W. J. Hamilton Habits of the Star-Nosed Mole, Condylura Cristata , 1931 .

[14]  J. Tower,et al.  Induced overexpression of mitochondrial Mn-superoxide dismutase extends the life span of adult Drosophila melanogaster. , 2002, Genetics.

[15]  J. Avery Critical review. , 2006, The Journal of the Arkansas Medical Society.

[16]  G. Pyke Optimal Foraging Theory: A Critical Review , 1984 .

[17]  M. Finke Complete nutrient composition of commercially raised invertebrates used as food for insectivores , 2002 .

[18]  E. Charnov Optimal Foraging: Attack Strategy of a Mantid , 1976, The American Naturalist.

[19]  M. Wong-Riley,et al.  Quantitative light and electron microscopic analysis of cytochrome oxidase‐rich zones in the striate cortex of the squirrel monkey , 1984, The Journal of comparative neurology.

[20]  Larry L. Wolf Foraging Behavior: Ecological, Ethological, and Psychological Approaches, A.C. Kamil, D. Sargent (Eds.). Garland STMP Press, New York and London (1981), xvii , 1982 .

[21]  R. S. Sohal,et al.  Extension of life-span by overexpression of superoxide dismutase and catalase in Drosophila melanogaster. , 1994, Science.

[22]  J. Lighton Discontinuous gas exchange in insects. , 1996, Annual review of entomology.

[23]  Kamel Fezzaa,et al.  Tracheal Respiration in Insects Visualized with Synchrotron X-ray Imaging , 2003, Science.

[24]  J. Kaas,et al.  Somatosensory fovea in the star‐nosed mole: Behavioral use of the star in relation to innervation patterns and cortical representation , 1997, The Journal of comparative neurology.

[25]  T. Schoener Theory of Feeding Strategies , 1971 .

[26]  K. Cummins,et al.  Caloric equivalents for investigations in ecological energetics , 1971 .

[27]  S. Gould,et al.  Exaptation—a Missing Term in the Science of Form , 1982, Paleobiology.

[28]  J. Lighton Notes from Underground: Towards Ultimate Hypotheses of Cyclic, Discontinuous Gas-Exchange in Tracheate Arthropods' , 1998 .

[29]  D. Jamieson,et al.  Oxygen toxicity and reactive oxygen metabolites in mammals. , 1989, Free radical biology & medicine.

[30]  J. Lawrence,et al.  Nutrient absorption efficiencies of the lizard, Cnemidophorus sexlineatus (Sauria: Teiidae) , 1993 .

[31]  C. R. Taylor,et al.  Design of the oxygen and substrate pathways. VII. Different structural limits for oxygen and substrate supply to muscle mitochondria. , 1996, The Journal of experimental biology.

[32]  K. Slăma Active Regulation of Insect Respiration , 1999 .

[33]  Transformation of the afferent tactile signal into a motor command in the cat motor cortex , 2005, Neurophysiology.

[34]  K. Catania,et al.  Receptive fields and response properties of neurons in the star-nosed mole's somatosensory fovea. , 2002, Journal of neurophysiology.

[35]  K. Catania,et al.  Tactile Foveation in the Star-Nosed Mole , 2003, Brain, Behavior and Evolution.

[36]  Graham H. Pyke,et al.  Optimal Foraging: A Selective Review of Theory and Tests , 1977, The Quarterly Review of Biology.

[37]  C. Scholtz,et al.  Discontinuous Gas‐Exchange Cycles in Scarabaeus Dung Beetles (Coleoptera: Scarabaeidae): Mass‐Scaling and Temperature Dependence , 1999, Physiological and Biochemical Zoology.

[38]  J. Lighton,et al.  Gas exchange in wind spiders (Arachnida, Solphugidae): Independent evolution of convergent control strategies in solphugids and insects , 1996 .

[39]  A. Williams,et al.  The effect of respiratory pattern on water loss in desiccation-resistant Drosophila melanogaster. , 1998, The Journal of experimental biology.

[40]  J. Emlen The Role of Time and Energy in Food Preference , 1966, The American Naturalist.

[41]  R. Carpenter,et al.  Movements of the Eyes , 1978 .

[42]  R. S. Sohal,et al.  Simultaneous Overexpression of Copper- and Zinc-containing Superoxide Dismutase and Catalase Retards Age-related Oxidative Damage and Increases Metabolic Potential in Drosophila melanogaster(*) , 1995, The Journal of Biological Chemistry.