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Behavioural Ontogeny of Male Northern Elephant Seals

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Behavioural Ontogeny of Male Northern Elephant Seals Animal Behaviour 166 (2020) 247e259 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/anbehav The genesis of giants: behavioural ontogeny of male northern elephant seals * C. Casey a, b, , I. Charrier c, N. Mathevon d, C. Nasr b, P. Forman b, C. Reichmuth b a Department of Ecology and Evolutionary Biology, University of California Santa Cruz, CA, U.S.A. b Institute of Marine Sciences, Long Marine Laboratory, University of California Santa Cruz, CA, U.S.A. c Equipe Communications Acoustiques, Neuro-PSI, CNRS UMR 9197, Universite, Paris Sud, Orsay, France d Equipe Neuro-Ethologie Sensorielle, ENES/CRNL, CNRS UMR 5292, INSERM UMR_S 1028, University of Lyon Saint-Etienne, France article info Dominance hierarchies structure the adult social networks of many mammals. To identify the conditions Article history: that support the establishment of stable hierarchical relationships within groups of familiar rivals, we Received 3 January 2020 explored the ontogeny of spatial, social and communicative behaviour among male northern elephant Initial acceptance 2 April 2020 seals, Mirounga angustirostris. We demonstrate that as male seals reach sexual maturity, they increase Final acceptance 14 May 2020 residency time ashore and restrict fine-scale movement patterns within the breeding colony. This spatiotemporal overlap creates a predictable social environment in which repeated interactions promote MS. number: A20-00005R greater social connectivity between older individuals. Moreover, as males become physically and behaviourally mature, their ritualized vocal displays transition from highly variable calls to stable and Keywords: unique individual acoustic signatures, supporting recognition between familiar competitors. The animal communication developmental onset of reliable signature calls e along with concurrent changes in space occupancy e behaviouralontogeny coincide with the formation of stable, structured dominance relationships among top-level competitors. dominance hierarchy fi individual acoustic signature These ndings advance our understanding of the ontogeny of social behaviour under conditions of individual recognition extreme competition. maleemale competition © 2020 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. northern elephant seal social network vocal production Dominance hierarchies are common among social animals from dominance hierarchies may be maintained through individual insects to mammals when individuals compete for access to limited recognition rather than direct assessment (Tibbetts & Dale, 2007). resources (Freeman, Freeman, & Romney, 1992; Kolmer & Heinze, In such cases, rivals rely on memory of prior experiences to limit 2000). As hierarchical status influences reproductive success, costly aggressive encounters with opponents with whom they have physiology and health (Mcdonald, 2007; Sapolsky, 2005), under- previously fought (Barnard & Burk, 1979). Recognition of compet- standing the development and structure of dominance relation- itors is enabled by cues that are reliable and unique that receivers ships has broad implications for the ecology and evolution of can perceive and decode (Sheehan & Tibbetts, 2009; Tibbetts & populations and species (Croft et al., 2009). While an individual's Dale, 2007). Consequently, individuals must have the opportunity position within a hierarchy is often linked to size, strength or to not only learn the characteristics of their familiar competitors, fighting ability (e.g. Sapolsky, 2005), factors related to social but also to have sufficient experience with these individuals for knowledge e including long-term memory of competitors, transi- their associated cues to become meaningful. ‘Familiarity’ can thus tive inference of fighting ability and winner/loser effects e may be be defined as the acquisition of social knowledge (e.g. relative rank equally important determinants of dominance (e.g. Mcdonald, and/or fighting ability) associated with competitors learned 2007). through previous experience with that individual. In systems where individuals occupy predictable breeding en- When familiarity is necessary to the formation of dominance vironments and frequently interact with familiar competitors, relationships among adults, the behaviour of individuals during maturation should provide ample experience to fine-tune recog- nition abilities. Juveniles may gain social knowledge by assessing * Correspondence: C. Casey, Long Marine Laboratory, 515 McAllister Rd, Santa one another during low-stakes interactions while at the same time Cruz, CA, 95076, U.S.A.. acquiring unique characteristics that others may learn and E-mail address: [email protected] (C. Casey). https://doi.org/10.1016/j.anbehav.2020.06.014 0003-3472/© 2020 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. 248 C. Casey et al. / Animal Behaviour 166 (2020) 247e259 remember. The developmental process by which individuals pro- maturation that these calls become individually distinct and vide and obtain information within their social environment recognizable to others. Finally, we assess how responsiveness to should become imperative to their long-term reproductive success acoustic displays of unfamiliar competitors changes as a function of (Turner, Bills, & Holekamp, 2018). Here, we explore behavioural age through the use of field playback experiments. Our integrated development among males in one of the most competitive approach captures the genesis of extreme intrasexual competition breeding systems known among mammals, the northern elephant in a social system based on individual recognition of familiar rivals. seal, Mirounga angustirostris. Northern elephant seals are an ideal model to evaluate the METHODS ontogeny of agonistic social behaviour owing to tremendous se- lection pressures for rival assessment (Le Boeuf, 1974). While General ashore, adult males compete fiercely to establish structured dominance hierarchies during the annual breeding season, which Research occurred at Ano~ Nuevo State Reserve in San Mateo may span more than 100 days without access to food or water County, California, U.S.A., which includes mainland and island (Deutsch, Haley, & Leboeuf, 1990; Le Boeuf, 1972). During this time coastal sandy beach haul-outs where northern elephant seals males are nearly continuously active, resting only during the congregate each winter. Approximately 2000 seals are distributed warmest periods of the day (Le Boeuf & Laws, 1994). Compared to over the 2.7 km span of mainland beaches at peak breeding season. females, males live shorter and more dangerous lives (Le Boeuf & Roughly 430 of these are males, and of these 12% (~52) can be Laws, 1994): only 5% of males survive to sexual maturity (Condit considered fully mature adults. The mainland site includes at least et al., 2014) with less than 1% ever gaining reproductive access to 20 harems annually, each with an average of 100 adult females and females (Le Boeuf & Laws, 1994). Given the tremendous competi- their dependent pups (range 50e150 females). As part of a long- tion that males exhibit during the breeding season, adult male term population monitoring effort, 300 weaned pups are tagged northern elephant seals exhibit extreme sexual dimorphism, annually each season with two serially numbered tags placed in the including a calloused chest shield and elongated nose, and they are interdigital webbing of their hindflippers (Jumbo Rototags, Dalton more than double the size of females (Le Boeuf & Laws, 1994). Supplies Ltd, Henley-on-Thames, U.K.). Consequently, approxi- Once established, dominance relationships among competing mately 35% of the males included in this study had known birth males remain stable throughout the breeding season, with most years. Additionally, some males are flipper-tagged as subadults or contests resolved through the exchange of ritualized multimodal adults without a known birth record. threat displays that include stereotyped posturing, seismic cues Between 2010 and 2018, we identified subadult and adult males and extremely loud pulsatile vocalizations (Bartholomew & Collias, upon their annual return to the site for the breeding season 1962; Southall, Casey, Holt, Insley, & Reichmuth, 2019). The vocal (DecembereMarch) by placing unique dye marks on their dorsal component of these threat displays is usually sufficient to elicit a flanks (as in Deutsch et al., 1990). These marks were referenced to directional response from familiar competitors: either attack if the flipper tags and associated metadata when available. Once marked, caller is subordinate or retreat if the caller is dominant (Insley, Holt, all males were photographed to document their size and physical & Southall, 2011). Each adult male in the breeding colony produces features. Between 81 and 350 males were identified in this manner a unique acoustic signature (Shipley, Hines, & Buchwald, 1981), and each season. vocal differences between males support individual recognition Once male elephant seals have survived adolescence (ages 1e3 through associative learning (Casey, Charrier, Mathevon, & years), they accelerate through rapid reproductive development Reichmuth, 2015). Both the timbre and rhythm of these calls are over a 4-year period (ages 4e8 years). During this time they more of particular importance, as male seals remember subtle differ- than triple in body size (Le Boeuf & Laws, 1994). Coincident with ences in call structure,
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