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Speed and Body Mass Colimit Prey Space of Mammalian Predators

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Speed and Body Mass Colimit Prey Space of Mammalian Predators PDF hosted at the Radboud Repository of the Radboud University Nijmegen The following full text is a publisher's version. For additional information about this publication click this link. https://hdl.handle.net/2066/222180 Please be advised that this information was generated on 2021-10-05 and may be subject to change. Received: 28 August 2019 | Revised: 1 May 2020 | Accepted: 5 May 2020 DOI: 10.1002/ece3.6411 ORIGINAL RESEARCH Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators Myriam R. Hirt1,2 | Marlee Tucker3,4,5 | Thomas Müller3,4 | Benjamin Rosenbaum1,2 | Ulrich Brose1,2 1EcoNetLab, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena- Abstract Leipzig, Leipzig, Germany 1. Realized trophic niches of predators are often characterized along a one-dimen- 2 Institute of Biodiversity, Friedrich Schiller sional range in predator–prey body mass ratios. This prey range is constrained by University Jena, Jena, Germany 3Senckenberg Biodiversity and Climate an “energy limit” and a “subdue limit” toward small and large prey, respectively. Research Centre (BiK-F), Frankfurt, Germany Besides these body mass ratios, maximum speed is an additional key component 4 Department of Biological Sciences, Goethe- in most predator–prey interactions. University, Frankfurt, Germany 2. Here, we extend the concept of a one-dimensional prey range to a two-dimen- 5Department of Environmental Science, Institute for Wetland and Water Research, sional prey space by incorporating a hump-shaped speed-body mass relation. This Radboud University, Nijmegen, the new “speed limit” additionally constrains trophic niches of predators toward fast Netherlands prey. Correspondence 3. To test this concept of two-dimensional prey spaces for different hunting strate- Myriam R. Hirt, German Centre for Integrative Biodiversity Research (iDiv) gies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial Halle-Jena-Leipzig, Deutscher Platz 5e, mammalian predator–prey interactions, their body masses, and maximum speeds. 04103, Leipzig, Germany. Email: [email protected] 4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flex- Funding information Deutsche Forschungsgemeinschaft, Grant/ ible. Group hunters and ambushers have evolved different strategies to occupy Award Number: FZT 118; Robert Bosch a similar trophic niche that avoids competition with pursuit predators. Moreover, Stiftung our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro-lions”) or mega-carnivores (referred to as “mega-cheetahs”). 5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic under- standing of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions. KEYWORDS ambushing, body mass ratio, food webs, group hunting, mega-carnivores, movement, predator–prey interactions, prey range, pursuit predation This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2020 The Authors. Ecology and Evolution published by John Wiley & Sons Ltd. 7094 | www.ecolevol.org Ecology and Evolution. 2020;10:7094–7105. HIRT ET AL. | 7095 1 | INTRODUCTION (Brose, 2010; Portalier et al., 2019). Maximum prey size is thereby determined by the “subdue limit”: The prey has to be small enough to Pursuing and capturing prey is as vital to the predator as it is to be successfully subdued by the predator (Radloff & Du Toit, 2004). the prey to avoid capture. Thus, animals have evolved a variety of These limits differ depending on the movement mode of the pred- morphological traits and behavioral strategies that either maximize ator and the dimensionality of the ecosystem (Brose et al., 2019; capture success or minimize predation risk (Cortez, 2011; Walker, Pawar, Dell, Lin, Wieczynski, & Savage, 2019; Portalier et al., 2019). Ghalambor, Griset, McKenney, & Reznick, 2005; Wilson et al., 2018). For typical terrestrial mammalian predators, these limits imply that Predator avoidance strategies of prey have been intensely stud- prey body masses are between one and four orders of magnitude ied (Lima, 1998), but less attention has been paid to the behavior lower (Figure 1a, typical predator–prey body mass structure, Brose of the predator (Lima, 2002). More recent studies have focused on et al., 2006, Tucker & Rogers, 2014). However, there are exceptions the interplay between predator and prey, and the determinants of to this pattern where predator–prey body mass ratios are inverted predatory success in specific predator–prey pursuits, such as those and predators are able to consume much larger prey (Figure 1a, in- between lion and zebra, or cheetah and impala (Wilson et al., 2015, verse predator–prey body mass structure), such as lions (~200 kg) hunt- 2018). Locomotor abilities such as speed and maneuverability are ing African buffaloes (~650 kg). Lions are able to effectively subdue critical components in these interactions as well as body mass and their larger prey because usually multiple group members are simul- hunting strategy (Bailey, Myatt, & Wilson, 2013; Bro-Jørgensen, taneously attacking it. 2013; Caro, 2005; Wilson et al., 2018). While the determinants and Besides body mass constraints, movement speed as well as ac- success of specific predator–prey pursuits have thereby been ana- celeration, deceleration, and maneuverability play an important role lyzed explicitly, general determinants of predator–prey interactions during the hunting process (Wilson et al., 2018). Primarily, the pred- and trophic niches are less explored. From the predator's perspec- ator needs to be fast enough to be able to catch its prey, which we tive, this addresses the question: “which prey could possibly be cap- refer to as the “speed limit.” Under the assumption that maximum tured and subdued?” speed follows a power–law relationship with body mass (Bejan & Traditionally, this question on trophic niches was answered Marden, 2006; Hedenström, 2003; Peters, 1986), predators would by placing predator and prey on a single body mass axis and set- generally not be able to catch prey that is much larger than they are, ting lower and upper limits to the prey range predators can exploit since it would always be faster. Therefore, the traditional concept of (Brose, 2010; Portalier, Fussmann, Loreau, & Cherif, 2019; Schneider, predator–prey body mass ranges cannot provide satisfying answers Scheu, & Brose, 2012). Minimum prey size is determined by the “en- for the questions of (1) how the smaller predators manage to success- ergetic limit”: The prey has to be large enough to meet the energy fully catch their prey if the body mass structure of the interaction is demands of the predator. This means that the energetic costs of inverse (Figure 1a) and (2) why there are no pursuit predators that hunting and attacking the prey should not exceed the energetic gain are larger than mega-herbivores (e.g., mega-cheetahs). Therefore, a Predator-prey body mass structure Maximum speed and body mass (a) (b) Prey smaller Prey larger TypicalInverse and faster and faster Predator d spee Log Prey smaller Prey larger and slower and slower Log bodymass FIGURE 1 Concept of the prey space Hypothecal prey spaces of different hunting strategies. (a) Typical and inverse body mass ratio of predators and their prey. (b) Scaling of maximum (c) Pursuit predaon (d) Grouphunng (e) Ambushing speed with body mass in terrestrial Energy limit mammals. (c–e) Hypothesized prey space of pursuit predation (c), group hunting (d), Subdue limit and ambushing (e) set by the energetic, subdue, and speed limit. Panels c, d, and e Speed limit have the same axes as panel b. Note that these limits are drawn as conceptual lines to illustrate our a priori expectations 7096 | HIRT ET AL. trophic niche concept that goes beyond simple predator–prey body studies (Brose, 2010; Petchey, Beckerman, Riede, & Warren, 2008; mass ranges is necessary for a mechanistic understanding of interac- Schneider, Brose, Rall, & Guill, 2016), our concept focuses on the tions for both typical and inverse body mass structures (Figure 1a). trophic dimension of the species’ niches. We illustrate our concept Recent food web studies have revealed that the movement type and test its hypotheses by compiling a database comprising data on (e.g., running, flying, swimming) of predator and prey is an import- body masses and maximum speeds of terrestrial mammalian preda- ant factor constraining their interactions (Brose et al., 2019; Jacob tors and their dominant prey. Our empirical data is mostly limited by et al., 2011). Interestingly, the maximum speed of animals follows the availability of maximum-speed data. Due to the further restric- a hump-shaped pattern with body mass (Garland, 1983; Hirt, Jetz, tion to species pairs that are engaged in trophic interactions, our Rall, & Brose, 2017; Figure 1b), enabling medium-sized predators database comprises only 63 predator–prey links. While information to catch larger and therefore slower prey. This pattern adds a new on additional predator–prey interactions as well as
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