Diel patterns in three-dimensional use of space by sea snakes Udyawer et al. Udyawer et al. Anim Biotelemetry (2015) 3:29 DOI 10.1186/s40317-015-0063-6 Udyawer et al. Anim Biotelemetry (2015) 3:29 DOI 10.1186/s40317-015-0063-6 TELEMETRY CASE REPORT Open Access Diel patterns in three‑dimensional use of space by sea snakes Vinay Udyawer1*, Colin A Simpfendorfer1 and Michelle R Heupel1,2 Abstract Background: The study of animal movement and use of space have traditionally focused on horizontal and vertical movements separately. However, this may limit the interpretation of results of such behaviours in a three-dimensional environment. Here we use passive acoustic telemetry to visualise and define the three-dimensional use of space by two species of sea snake [Hydrophis (Lapemis) curtus; and Hydrophis elegans] within a coastal embayment and identify changes in how they use space over a diel cycle. Results: Monitored snakes exhibited a clear diel pattern in their use of space, with individuals displaying restricted movements at greater depths during the day, and larger movements on the surface at night. Hydrophis curtus gener- ally occupied space in deep water within the bay, while H. elegans were restricted to mud flats in inundated inter-tidal habitats. The overlap in space used between day and night showed that individuals used different core areas; how- ever, the extent of areas used was similar. Conclusions: This study demonstrates that by incorporating the capacity to dive in analyses of space use by sea snakes, changes over a diel cycle can be identified. Three-dimensional use of space by sea snakes can identify spatial or temporal overlaps with anthropogenic threats (e.g. trawling, dredging) and help develop targeted management policies that mitigate any adverse effects to ensure healthy populations of sea snakes. Keywords: Hydrophis (Lapemis) curtus, Hydrophis elegans, Kernel utilisation distribution (KUD), 3D Background understanding of the spatial ecology of a range of terres- The identification of patterns in the movements of indi- trial, avian, and marine organisms [2–5]. viduals, and their relationship to ecological phenomena, Since aquatic animals live in a three-dimensional envi- have been a critical aspect in studies of terrestrial, avian, ronment and have the ability to move in all three dimen- and marine organisms [1]. Traditionally, studies on the sions, their use of space is most accurately represented in movement and use of space by animals have been rep- the same number of dimensions. Sea snakes are a group resented in two dimensions (e.g. Latitude–Longitude of marine elapid snakes that spend their entire lifecycle or Easting–Northing); this, however, may not fully rep- in the marine environment and are found in a range of resent the reality of the environment that most animals habitats, including coral reefs, open oceans, and coastal occupy. Recent advances in technology and analytical embayments [6]. Past studies have used mark-recapture techniques have allowed integration of the vertical axis and genetic studies to infer broad-scale movements and into studies examining the use of space to a high degree population connectivity between patchy reef environ- of spatial resolution. These advances have improved our ments over large temporal scales [7, 8]. A few attempts to understand movement and use of space by reef-associated olive sea snakes [Aipysurus lae- vis; 9, 10] and pelagic yellow-bellied sea snakes [Hydro- *Correspondence: [email protected] phis (Pelamis) platura; 11, 12] have contributed the 1 Centre for Sustainable Tropical Fisheries and Aquaculture, College of Marine and Environmental Sciences, James Cook University, Townsville, majority of what is currently known about these taxa. QLD, Australia Rubinoff and colleagues [11, 12] studied the short-term Full list of author information is available at the end of the article © 2015 Udyawer et al. 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. Udyawer et al. Anim Biotelemetry (2015) 3:29 Page 3 of 9 movements (3.8–31.2 h monitored) of fifteen H. platura on the movement patterns of sea snakes in a coastal tagged with depth-sensing ultrasonic tags and examined system, we tracked two species of sea snake in Cleve- vertical and horizontal patterns of movement separately, land Bay, Queensland Australia (Fig. 1, Additional file 1, publishing their results in two articles. The first, exam- https://dl.dropboxusercontent.com/u/31456301/3DSS/ ined the movements of tagged snakes in the vertical axis, SM1/index.html) to define three-dimensional movement looking at the depths and durations of dives [11] followed patterns. The aims of this study were to: (a) use passive by the second that focused on the horizontal move- telemetry to understand and visualise how sea snakes use ments of tagged individuals [12]. They found that despite space within the water column, and (b) examine any diel H. platura being considered a surface-dwelling pelagic patterns in the use of three-dimensional space by tagged sea snake, tagged individuals spent the majority of the sea snakes. Patterns in the three-dimensional use of space monitoring period (87%) underwater and dove as deep were also considered in the context of their potential to as 50 m. Burns and Heatwole [9] found that A. laevis inform on the susceptibility of sea snakes to anthropo- displayed restricted movements around their home reef genic threats (e.g. trawling, dredging). with small home ranges (1,500–1,800 m2) and that home Results ranges of all snakes (n = 11) overlapped with two or more individuals. Estimates of space used and overlap between Twenty-five individuals from two species of sea snake, monitored individuals, however, did not consider their spine-bellied sea snake (Hydrophis curtus previously use of depth. Studies of eel movements by Simpfendorfer Lapemis curtus: n = 19) and elegant sea snake (Hydro- et al. [2] revealed that failure to consider vertical move- phis elegans: n = 6), were tagged within the study site ment can result in an overestimation of home range over- and monitored between January and November 2013. lap if individuals are using the same two-dimensional The majority of monitored individuals were juvenile, location but different depths. which were difficult to sex using external morphologi- Currently, very little is known about how sea snake spe- cal feature. Only two adult female H. curtus and a sin- cies that occupy coastal and inshore waters use space, gle adult male H. elegans were monitored; therefore, to with the majority of past studies in these habitats often avoid inaccurate conclusions related to the small sample focusing on abundance and diversity based on incidental size of reproductively mature individuals in this study, capture in trawl fisheries [13, 14]. To provide information sex was excluded as a covariate in further analyses. Fig. 1 Study site in Cleveland Bay. Points represent locations of acoustic receivers deployed at the study site. Broken grey lines indicate bathymetry. An interactive, three-dimensional model of the study site is available in the additional files (Additional file 1) Udyawer et al. Anim Biotelemetry (2015) 3:29 Page 4 of 9 Fig. 2 Patterns in diel use of different depths by tagged a Hydrophis curtus (n 19) and b Hydrophis elegans (n 6) over the monitoring period. = = Mean depths recorded by day (red) and night (blue) are represented as ticks on the y-axis Data from depth sensors showed that individuals from The integration of depth data into analysis of space use both species displayed a strong diel pattern in use of the showed a difference in the three-dimensional kernel utili- water column (Fig. 2). Snakes were found at significantly sation distributions (3DKUD) for individuals of both spe- greater depths during the day (06:00–18:00 h) and were cies during day and night (Fig. 3b, d; Additional files 4, 5; active on the surface at night (t test, H. curtus: t = 26.37, https://dl.dropboxusercontent.com/u/31456301/3DSS/ p < 0.05, H. elegans: t = 9.51, p < 0.05). Hydrophis curtus SM3/index.html, https://dl.dropboxusercontent.com/ displayed a more varied dive profile, diving to an average u/31456301/3DSS/SM5/index.html). Sufficient data from depth of 3.2 m (SE: ±0.03 m; max depth = 7.5 m) dur- 12 of the 19 tagged H. curtus, and 5 of the 6 H. elegans ing the day and 2.1 m (SE: ±0.03 m; max depth = 7.4 m) were available to calculate reliable 3DKUDs to compare at night. While, H. elegans generally used comparatively diurnal and nocturnal use of space. Despite the differ- shallower water and dived to an average of 2.5 m (SE: ence in depths occupied by individuals, generalised lin- ±0.05 m; max depth = 5.7 m) during the day and 1.8 m ear mixed models (GLMM) showed that volumes of core (SE: ±0.04 m; max depth = 6.2 m) at night. Individuals (50%-3DKUD) and extent (95%-3DKUD) of space used of H. curtus were generally present in deep water on the by H. curtus were not significantly different between eastern side of Cleveland Bay (Fig. 3a, Additional file 2, day and night (50%-3DKUD: F1,11 = 0.44, p = 0.52; 95%- https://dl.dropboxusercontent.com/u/31456301/3DSS/ 3DKUD: F1,11 = 0.20, p = 0.66; Fig.