Tidal drift removes the need for area-restricted search in foraging Atlantic puffins.

Marine biology royalsocietypublishing.org/journal/rsbl Tidal drift removes the need for arearestricted search in foraging Atlantic puffins Research Ashley Bennison1,2, John L. Quinn1, Alison Debney3 and Mark Jessopp1,2 1 Cite this article: Bennison A, Quinn JL, Debney A, Jessopp M. 2019 Tidal drift removes the need for area-restricted search in foraging Atlantic puffins. Biol. Lett. 15: 20190208. http://dx.doi.org/10.1098/rsbl.2019.0208 Received: 15 March 2019 Accepted: 10 June 2019 Subject Areas: behaviour, ecology Keywords: movement ecology, foraging, area-restricted search, energetics Author for correspondence: Ashley Bennison e-mail: Electronic supplementary material is available online at http://dx.doi.org/10.6084/m9. figshare.c.4551716. School of Biological, Earth and Environmental Sciences, and 2MaREI Centre, Environmental Research Institute, University College Cork, Cork, Ireland 3 Zoological Society of London, Regents Park, London, UK AB, 0000-0001-9713-8310 Understanding how animals forage is a central objective in ecology. Theory suggests that where food is uniformly distributed, Brownian movement ensures the maximum prey encounter rate, but when prey is patchy, the optimal strategy resembles a Lévy walk where area-restricted search (ARS) is interspersed with commuting between prey patches. Such movement appears ubiquitous in high trophic-level marine predators. Here, we report foraging and diving behaviour in a seabird with a high cost of flight, the Atlantic puffin (Fratercula arctica), and report a clear lack of Brownian or Levy flight and associated ARS. Instead, puffins foraged using tides to transport them through their feeding grounds. Energetic models suggest the cost of foraging trips using the drift strategy is 28–46% less than flying between patches. We suggest such alternative movement strategies are habitat-specific, but likely to be far more widespread than currently thought. 1. Introduction Optimal foraging theory assumes that animals move between patches of prey in order to maximize prey encounter rate and nutritional intake [1,2]. Brownian motion or random walks appear to be optimal when prey is uniformly distributed [3] and are characterized by movement where turning angles between relocations are effectively random [4]. By contrast, when resources are patchy, or animals have a preferred direction or orientation, movement is non-random, leading to correlated random walks (CRWs) [5] or Lévy flights [6]. CRWs incorporate an element of directional persistence [7], while Lévy walks allow random direction, but step lengths between successive locations reflect a power-law distribution [8]. First reported in albatross [6], Lévy flight has been identified across multiple taxa; however, its universality for explaining foraging ecology has stimulated debate [6,9–13] and is now considered one element of a number of strategies used in foraging for resources [14–16]. This foraging component of animal movement is universally characterized by area-restricted search (ARS): the tendency for animals to concentrate search within relatively small areas before continuing wider range exploration [17]. ARS is widely accepted as a core component within foraging theory across a wide array of taxa ranging from grazing herbivores [18] to higher trophic-level predators [19]. ARS is scale-dependent [20,21] and because it occurs within CRWs and Lévy flights [22], has provided a link between movement ecology, optimal foraging theory and energetics. Seabird research has led much of the development of animal movement theory for Lévy flight and ARS, where individuals travel large distances between prey patches with subsequent fine-scale search behaviour above water [23,24]. The generality of ARS in seabirds is well established and it therefore could be assumed that ARS is energetically optimal. Here we report a lack & 2019 The Author(s) Published by the Royal Society. All rights reserved. 2 royalsocietypublishing.org/journal/rsbl all puffins from Little Saltee June 2017 and July 2018 N 0 5 10 20 km N 0 5 10 20 km Figure 1. An example GPS track from puffin EX01307 tracked from Little Saltee, County Wexford, Ireland in June 2017. The non-typical movement patterns can be seen clearly with a commuting stage away from the colony before long straight section in broad easterly – westerly directions. Different colours represent different foraging trips. Inset: all puffin trips recorded between 2017 and 2018. The area of interest showing colony location. of ARS in a seabird with a high cost of flight, the Atlantic puffin, Fratercula arctica, (hereafter puffin). Auks, including puffins, have previously been shown to use ARS between prey patches [25–27]. Unusual track patterns led us to hypothesize that puffins were exploiting tidal movement to transport them over prey patches. We predicted that this strategy must be energetically lower than engaging in flight/ARS, suggesting a new energetically optimal foraging strategy in seabirds. 2. Material and methods Research was approved by University College Cork Animal Ethics Committee and under licences from the British Trust for Ornithology, National Parks and Wildlife Service and the Health Products Regulatory Authority of Ireland. Sixteen chickprovisioning puffins were tracked during the breeding season (2017 n ¼ 12, 2018 n ¼ 4) on Little Saltee, Co. Wexford (52.137 N, 26.590 W), Ireland. Birds were caught using purse nets at burrow entrances, and only individuals returning with fish were tagged to ensure they were provisioning chicks. In 2017, birds were equipped with either an Ecotone Uria solar-charging GPS logger (n ¼ 10), or a PathTrack NanoFix tag with time-depth recorder (CEFAS G5 TDR) (n ¼ 2). In 2018, only Ecotone Uria tags were deployed (n ¼ 4). Ecotone tags downloaded data remotely, while Pathtrack tags required bird recapture. Both tag types recorded a GPS position every 15 min. TDRs were used to log dives deeper than 1 m, and longer than 5 s duration [28]. Ecotone tags deployed in 2018 were programmed to record times of descent and ascent using manufacturer recommended settings. Devices were attached ventrally to the lower back using strips of Tesa tape to minimize hydrodynamic and aerodynamic drag following Harris et al. [27] and Elliott et al. [29]. Mean deployment weight was 2.73% of body weight. Further information on tag attachment is provided in the electronic supplementary material. Tracks were atypical to those previously observed in this species, with no obvious ARS, and characterized by three distinct components: (1) straight line commuting from the colony out to sea, (2) slow directed phases in easterly or westerly directions and (3) return to the colony in a straight line (figures 1 and 2; electronic supplementary material, figures S1 and V1). Tracks of multiple puffins were observed to be synchronized as they moved over the core use area, often starting and ending drifting peri (...truncated)