title: Understanding spatial distributions: negative density-dependence in prey causes predators to trade-off prey quantity with quality.
abstract: Negative density-dependence is generally studied within a single trophic level, thereby neglecting its effect on higher trophic levels. The 'functional response' couples a predator's intake rate to prey density. Most widespread is a type II functional response, where intake rate increases asymptotically with prey density; this predicts the highest predator densities at the highest prey densities. In one of the most stringent tests of this generality to date, we measured density and quality of bivalve prey (edible cockles Cerastoderma edule) across 50 km² of mudflat, and simultaneously, with a novel time-of-arrival methodology, tracked their avian predators (red knots Calidris canutus). Because of negative density-dependence in the individual quality of cockles, the predicted energy intake rates of red knots declined at high prey densities (a type IV, rather than a type II functional response). Resource-selection modelling revealed that red knots indeed selected areas of intermediate cockle densities where energy intake rates were maximized given their phenotype-specific digestive constraints (as indicated by gizzard mass). Because negative density-dependence is common, we question the current consensus and suggest that predators commonly maximize their energy intake rates at intermediate prey densities. Prey density alone may thus poorly predict intake rates, carrying capacity and spatial distributions of predators.
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands allert.bijleveld@nioz.nl.
authors.forename: Allert I
authors.identifier: http://orcid.org/0000-0002-3159-8944
authors.initials: AI
authors.lastname: Bijleveld
authors.affiliation: Department of Mechanical and Aerospace Engineering, Cornell University, Corson Hall, Ithaca, NY 14853, USA.
authors.forename: Robert B
authors.identifier: http://orcid.org/0000-0002-1726-151X
authors.initials: RB
authors.lastname: MacCurdy
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Ying-Chi
authors.initials: YC
authors.lastname: Chan
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Emma
authors.initials: E
authors.lastname: Penning
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853, USA Bioacoustics Research Program, Cornell Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA.
authors.forename: Rich M
authors.identifier: http://orcid.org/0000-0001-9794-1429
authors.initials: RM
authors.lastname: Gabrielson
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, National Marine Facilities, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: John
authors.initials: J
authors.lastname: Cluderay
authors.affiliation: Bioacoustics Research Program, Cornell Laboratory of Ornithology, Cornell University, 159 Sapsucker Woods Road, Ithaca, NY 14850, USA.
authors.forename: Eric L
authors.initials: EL
authors.lastname: Spaulding
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Anne
authors.initials: A
authors.lastname: Dekinga
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Sander
authors.identifier: http://orcid.org/0000-0002-7454-6933
authors.initials: S
authors.lastname: Holthuijsen
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Job
authors.initials: J
authors.lastname: ten Horn
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Maarten
authors.initials: M
authors.lastname: Brugge
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands.
authors.forename: Jan A
authors.identifier: http://orcid.org/0000-0002-4132-8243
authors.initials: JA
authors.lastname: van Gils
authors.affiliation: Department of Ecology and Evolutionary Biology, Cornell University, Corson Hall, Ithaca, NY 14853, USA.
authors.forename: David W
authors.initials: DW
authors.lastname: Winkler
authors.affiliation: NIOZ Royal Netherlands Institute for Sea Research, Department of Coastal Systems, and Utrecht University, PO Box 59, 1790 AB Den Burg, The Netherlands Chair in Global Flyway Ecology, Conservation Ecology Group, Groningen Institute for Evolutionary Life Sciences (GELIFES), University of Groningen, PO Box 11103, 9700 CC Groningen, The Netherlands.
authors.forename: Theunis
authors.identifier: http://orcid.org/0000-0001-9668-466X
authors.initials: T
authors.lastname: Piersma
mesh_terms: D063147:Animal Distribution; D000818:Animals; D049873:Cardiidae / Q000502:physiology*; D046091:Charadriiformes / Q000502:physiology*; D002149:Energy Intake; D005247:Feeding Behavior; D020387:Food Chain; D008954:Models, Biological; D009426:Netherlands; D011156:Population Density; D011235:Predatory Behavior
keywords: movement ecology; negative density-dependence; optimal foraging; phenotype-limited spatial distribution; resource-selection modelling; type IV functional response