American Society of Naturalists

A membership society whose goal is to advance and to diffuse knowledge of organic evolution and other broad biological principles so as to enhance the conceptual unification of the biological sciences.

“False exclusion: A case to embed predator performance in classical population models”

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David J. S. Montagnes, Xuexia Zhu, Lei Gu, Yunfei Sun, Jun Wang, Rosie Horner, and Zhou Yang (Nov 2019)

Read the Article (Just Accepted)

Predator-prey dynamics are driven by insufficiently-explored predator behaviors that are inherently prey-dependent

“A large <i>Paramecium</i> attacked by four <i>Didinia</i>. Under such conditions the <i>Paramecium</i> is usually torn in pieces and each <i>Didinium</i> gets a portion. Sometimes however one <i>Didinium</i> gets the entire <i>Paramecium</i>, forcing the others off during the process of swallowing.” (Figure 9 from S.&nbsp;O. Mast, “The Reactions of <i>Didinium nasutum</i> (Stein) with Special Reference to the Feeding Habits and the Function of Trichocysts,” <i>Biological Bulletin</i>, 1909, 16:91-118.) This was one of the model systems that was used by Montagnes et&nbsp;al. and is one that has clearly been a focus for studies in <i>Am.&nbsp;Nat.</i> for well over a century.
“A large Paramecium attacked by four Didinia. Under such conditions the Paramecium is usually torn in pieces and each Didinium gets a portion. Sometimes however one Didinium gets the entire Paramecium, forcing the others off during the process of swallowing.” (Figure 9 from S. O. Mast, “The Reactions of Didinium nasutum (Stein) with Special Reference to the Feeding Habits and the Function of Trichocysts,” Biological Bulletin, 1909, 16:91-118.) This was one of the model systems that was used by Montagnes et al. and is one that has clearly been a focus for studies in Am. Nat. for well over a century.

Ignorance is not bliss. Global health and, ultimately, our survival rely on strategic forward planning. Today, computer-driven simulations are the “crystal balls” by which we predict the future. But computers require valid instruction. If we “falsely exclude” – ignore – essential facts and concepts, then predictions will go disastrously wrong. Recently, through a UK-Chinese collaboration, researchers have re-evaluated and quantified three very basic, but essential, biological concepts: 1) when animals are fed less they are more likely to die; 2) an animal’s efficiency to use food changes with food availability (e.g., when food is abundant animals are wasteful); and 3) reproduction only occurs when there is sufficient quantities of food. Surprisingly, these “food-dependent” behaviors have been overlooked, or at least inadequately incorporated, in many models that predict population dynamics. The first step of this research produced a theoretical, mathematical framework that embraces these concepts. Then, essential experimental evidence, provided proof of concept. Only then could the experimental data and the computer model be used to reveal that including all three of these fundamental aspects of animal biology places into question our current evaluation of population dynamics. For instance, the revised approach predicts extinction when the old ones predicted survival. Now biologists can include these food-dependent behaviors, making more informed predictions of how predators respond in nature.


Abstract

We argue that predator-prey dynamics, a cornerstone of ecology, can be driven by insufficiently-explored aspects of predator performance that are inherently prey-dependent: i.e., these have been falsely excluded. Classical—Lotka-Volterra-based—models tend to only consider prey-dependent ingestion rate. We highlight three other prey-dependent responses and provide empirically-derived functions to describe them. These functions introduce neglected nonlinearities and threshold behaviors into dynamic models leading to unexpected outcomes: specifically, as prey abundance increases predators: 1) become less efficient at using prey; 2) initially allocate resources towards survival and then allocate resources towards reproduction; and 3) are less likely to die. Based on experiments using model-zooplankton, we explore consequences of including these functions in the classical structure and show they alter qualitative and quantitative dynamics of an empirically-informed, generic predator-prey model. Through bifurcation analysis, our revised structure predicts: 1) predator extinctions, where the classical structure allows persistence; 2) predator survival, where the classical structure drives predators towards extinction; and 3) greater stability through smaller amplitude of cycles, relative to the classical structure. Then, by exploring parameter space, we show how these responses alter predictions of predator-prey stability and competition between predators. Based on our results, we suggest that classical assumptions about predator responses to prey abundance should be re-evaluated.