Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming

Papastamatiou et al. Movement Ecology (2018) 6:9 https://doi.org/10.1186/s40462-018-0127-3 RESEARCH Open Access Activity seascapes highlight central place foraging strategies in marine predators that never stop swimming Yannis P. Papastamatiou1, Yuuki Y. Watanabe2,3, Urška Demšar4* , Vianey Leos-Barajas5, Darcy Bradley6, Roland Langrock7, Kevin Weng8, Christopher G. Lowe9, Alan M. Friedlander10,11 and Jennifer E. Caselle12 Abstract Background: Central place foragers (CPF) rest within a central place, and theory predicts that distance of patches from this central place sets the outer limits of the foraging arena. Many marine ectothermic predators behave like CPF animals, but never stop swimming, suggesting that predators will incur ‘travelling’ costs while resting. Currently, it is unknown how these CPF predators behave or how modulation of behavior contributes to daily energy budgets. We combine acoustic telemetry, multi-sensor loggers, and hidden Markov models (HMMs) to generate ‘activity seascapes’, which combine space use with patterns of activity, for reef sharks (blacktip reef and grey reef sharks) at an unfished Pacific atoll. Results: Sharks of both species occupied a central place during the day within deeper, cooler water where they were less active, and became more active over a larger area at night in shallower water. However, video cameras on two grey reef sharks revealed foraging attempts/success occurring throughout the day, and that multiple sharks were refuging in common areas. A simple bioenergetics model for grey reef sharks predicted that diel changes in energy expenditure are primarily driven by changes in swim speed and not body temperature. Conclusions: We provide a new method for simultaneously visualizing diel space use and behavior in marine predators, which does not require the simultaneous measure of both from each animal. We show that blacktip and grey reef sharks behave as CPFs, with diel changes in activity, horizontal and vertical space use. However, aspects of their foraging behavior may differ from other predictions of traditional CPF models. In particular, for species that never stop swimming, patch foraging times may be unrelated to patch travel distance. Keywords: Sharks, Acceleration, Hidden Markov models, Coral reefs, Foraging, Telemetry Background Central place foraging (CPF) is a ubiquitous behavior seen across animal groups ranging from insects, to birds, and humans [1]. Unlike random movements within a home range, CPF behavior consists of periodic and predictable movements to and from a central place, often with multiple individuals sharing the central place [1]. CPF animals tend to rest at the central place, with their energy costs increasing as they travel greater distances from this location [1, 2]. As such, the costs associated with travel distance to * Correspondence: 4 School of Geography and Sustainable Development, University of St Andrews, St Andrews, Scotland, UK Full list of author information is available at the end of the article the patch should define the limits of the animals foraging range from the central place [2, 3]. CPF behavior can lead to heterogeneity in habitat or prey distribution as the animal’s foraging rates will likely vary with distance from the central place [4, 5]. As patch distance to the central place increases, travel costs also increase, and the animal should spend more time foraging at the patch [1, 4]. A key assumption of CPF theory is that an animal rests at the central place, and foraging costs increase with travel distance to a feeding patch. Yet, there are many species of marine predators that exhibit CPF-like behavior, but never stop swimming, and never truly rest. For these animals, energy costs may be independent of travel distance to the patch, and simply a function of © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Papastamatiou et al. Movement Ecology (2018) 6:9 swim speeds. Such predators include large coral reef-associated fishes (sharks and teleosts), which swim within a relatively small core area during the day, and move over an expanded area at night, with periodicity of movements related to diel or tidal cycles [6–9]. Marine animals also move in a three-dimensional (3D) environment and CPF behavior can include a vertical component as well as a horizontal one, with individuals performing diel vertical migrations (DVM) relative to the central place [10–12]. While few studies have measured actual activity and swim speeds, some tropical reef sharks display patterns of activity that also vary with diel and tidal cycles [13–17]. However, why predators that do not use a shelter or ever stop swimming require a central place, is unclear. CPF animals that never stop swimming are almost exclusively ectotherms, so metabolic rates are sensitive to changes in ambient temperature. At any particular time, routine metabolic rates should be a function of body temperature, movement speed, and other aspects of the movement process (e.g. turning costs more than straight line swimming [18]). While the animal may not stop swimming, they can establish the central place in cooler waters where metabolic rates are reduced. If the animal simultaneously maintains low activity in the central place while cooler, then energy costs may be essentially similar to ‘resting’ [10]. In addition to changes in body temperature, routine metabolic rates can be modulated via changes in swim speed. Hence, the energetics of CPF in these animals must consider body temperature and movement rates. Accelerometers have become popular for measuring both the activity and energy requirements of free-ranging marine animals [14, 19–21]. Accelerometer data can be combined with information about the geographic location of the animal to generate a spatial representation of the animal’s energy costs [19–21]. However, it is difficult to separate areas of high-energy expenditure (e.g. traversing through an energetically expensive habitat) from areas of high animal activity related to specific behaviors (e.g. foraging) within the landscape, especially for animals whose behaviors cannot be easily defined from sensor measurements (e.g. continuously swimming fish). For our general case of CPF foragers, we are interested in how the predator’s foraging activity varies spatially in relation to the central place. This challenge is further complicated in fishes because space use an (...truncated)