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Visual Similarities of Marine Debris to Natural Prey Items of Sea Turtles

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Visual Similarities of Marine Debris to Natural Prey Items of Sea Turtles Schuyler et al. BMC Ecology 2014, 14:14 http://www.biomedcentral.com/1472-6785/14/14 RESEARCH ARTICLE Open Access Mistaken identity? Visual similarities of marine debris to natural prey items of sea turtles Qamar A Schuyler1*, Chris Wilcox2, Kathy Townsend3, B Denise Hardesty2 and N Justin Marshall4 Abstract Background: There are two predominant hypotheses as to why animals ingest plastic: 1) they are opportunistic feeders, eating plastic when they encounter it, and 2) they eat plastic because it resembles prey items. To assess which hypothesis is most likely, we created a model sea turtle visual system and used it to analyse debris samples from beach surveys and from necropsied turtles. We investigated colour, contrast, and luminance of the debris items as they would appear to the turtle. We also incorporated measures of texture and translucency to determine which of the two hypotheses is more plausible as a driver of selectivity in green sea turtles. Results: Turtles preferred more flexible and translucent items to what was available in the environment, lending support to the hypothesis that they prefer debris that resembles prey, particularly jellyfish. They also ate fewer blue items, suggesting that such items may be less conspicuous against the background of open water where they forage. Conclusions: Using visual modelling we determined the characteristics that drive ingestion of marine debris by sea turtles, from the point of view of the turtles themselves. This technique can be utilized to determine debris preferences of other visual predators, and help to more effectively focus management or remediation actions. Keywords: Chelonia mydas, Chromatic space, Eretmochelys imbricata, Marine debris, Vorobyev-Osorio model Background turtles responded exclusively to visual cues [10]. There- Sea turtles, like many other marine taxa, are increasingly fore, the visual similarity between plastic bags and jellyfish prone to marine debris ingestion and associated problems can cause confusion even in the absence of chemical [1].Despitemanystudiesrecording instances of debris stimuli associated with food sources. Loggerhead sea ingestion e.g. [2,3], little is known about the cues that turtles have been shown to approach plastic bags in a attract turtles to eat plasticdebris.Thepredominant similar manner to gelatinous prey, indicating that they hypotheses are that 1) turtles, as opportunistic feeders, use visual characteristics to select their food [11]. simply consume items in proportion to what they encounter The spectral sensitivity of an animal depends not only in the environment, including plastics; and 2) that turtles on its photopigments, but also on the transmissivity of the feed on plastic because of its similarity to prey; particularly ocular media and, in the case of turtles, of the oil droplets jellyfish [4,5]. Though the proportion of gelatinous prey associated with the cones. Turtles have a well-developed in a turtle’s diet varies depending on the life stage and visual system with at least three different photopigments, the species of the turtle, all species do target these prey indicating the ability to see colour [12]. The visual sys- at some stage of their lives [6,7]. tem of sea turtles is similar to that of fresh water turtles; Turtles are primarily visual predators. Research indicates however, the sea turtles’ visual pigments are slightly shifted that loggerhead turtles have limited ability to find food towards the shorter wavelengths, due to the differences based on chemical stimuli alone [8], which may explain in spectral characteristics of the waters in which the why they are primarily caught during the day on longline different animals live [13]. Sea turtles generally inhabit fishing lines, and rarely at night [9]. Similarly, when pre- clearer, oceanic waters, whereas fresh water contains sented with both chemical and visual cues, leatherback many dissolved organics and sediments, shifting the maximum light transmission to longer wavelengths * Correspondence: [email protected] 1 [13-15]. The bulk of sea turtle vision studies to date School of Biological Sciences, University of Queensland, St. Lucia, Australia Chelonia mydas Full list of author information is available at the end of the article have been conducted on green ( )and © 2014 Schuyler et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. 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. Schuyler et al. BMC Ecology 2014, 14:14 Page 2 of 7 http://www.biomedcentral.com/1472-6785/14/14 loggerhead (Caretta caretta) sea turtles e.g. [16,17]. ingested by turtles was significantly different from beach Liebman and Granda found 3 photopigments in the debris for all environmental variables investigated with green turtle retina absorbing maximally at 440 nm (SWS), the exception of background contrast and the contribu- 502 nm (MWS), and 562 nm (LWS) [18]. Recent evidence tion of the UV cone (Table 1). Turtles differentiated indicates that green turtles are also likely to have a fourth, items most strongly based on their luminance (p < 0.001, ultraviolet sensitive (UVS) photo-pigment, like their fresh- selectivity ratio = 0.640), flexibility (p < 0.001, selectivity water relatives [17]. Turtles possess at least four different ratio = 0.437), and translucency (p = 0.001, selectivity types of oil droplets, again indicatingtheyhavefourspectral ratio = 0.290). Items ingested by turtles tend to be less sensitivities, like birds [17]. Each type of oil droplet may be bright (i.e. lower luminance value), more flexible, and associated with a specific photopigment, or may combine more translucent than items found in the environment. with different photopigments to produce multiple cone With respect to wavelengths, items ingested by turtles receptor types [14,19]. had significantly lower short wavelength spectrum values Turtles, like many other vertebrates, also possess double (p < 0.001, selectivity ratio = 0.215). cones, a specialized structure consisting of two cones joined A simple inspection of the turtle visual space models together [20]. The function of the double cone is still un- (Figure 2) shows the difference in the wavelengths of known; however it has been hypothesized in both birds and ingested debris and beach debris. The average value of reptiles to play a role in discriminating between levels of lu- debris ingested by turtles is lower in the short wave- minosity or brightness [20-23]. Although the exact compos- length spectrum than that of beach debris, indicating ition of the double cone structure is unknown, in fresh that the items turtles eat are less blue than what is avail- water turtles both of the members that make up the double able to them in the environment. cone have LWS photoreceptors [19]. There were no significant differences observed between We created a chromatic space model of the green turtle plastics ingested by sea turtles of different life history visual system (sensu [24]) to investigate the following ques- stages (new recruits and juvenile turtles) with respect to the tions: Are green, hawksbill, and flatback turtles selectively factors tested (colour, texture, translucency, luminance, ingesting particular types of debris over others, and if so, and background contrast). However, hawksbill and flatback what characteristics of that debris (colour, texture, translu- turtles did exhibit some significant differences compared to cency, luminance, or background contrast) are most green turtles. Because we only had a small sample size for relevant to turtles’ foraging choices? hawksbills (n = 2) and flatbacks (n = 1), we omitted them from analyses. Results Our visual model resulted in peak sensitivities of 365, 440, Discussion 515, and 560–565 (Figure 1). The mixed effects modelling The spectral sensitivities we calculated (365, 440, 515 results indicate that sea turtles select the debris they ingest and 560–565) are well matched with previously published based on a variety of physical properties. In fact, debris electroretinography (ERG) data of C. mydas spectral 1 0.8 0.6 0.4 0.2 0 300 350 400 450 500 550 600 650 700 Wavelength Figure 1 Modelled spectral sensitivity of C. mydas. Each peak represents the photopigment multiplied by the transmissivity of its associated oil droplet and by the ocular media. Schuyler et al. BMC Ecology 2014, 14:14 Page 3 of 7 http://www.biomedcentral.com/1472-6785/14/14 Table 1 Model coefficients for physical factors influencing the selectivity of debris ingestion by sea turtles Intercept SE of intercept Turtle effect SD of turtle effect p-value Selectivity ratioa Flexibility 1.755 0.088 0.767 0.133 <0.001* 0.437 Translucency 1.295 0.069 0.375 0.104 0.001* 0.290 SWS 0.268 0.006 −0.058 0.010 <0.001* 0.215 MWS 0.291 0.005 0.028 0.008 0.002* 0.096 LWS 0.311 0.008 0.040 0.012 0.002* 0.127 UVS 0.130 0.007 −0.010 0.010 0.345 0.075 Contrast 25.981 1.551 −1.468 2.356 0.573 0.057 Luminance (sum of cones) 239.27 16.225 −153.144 24.569 <0.001* 0.640 Luminance (double cone) 74.978 4.930 −43.441 7.47 <0.001* 0.579 Note that the selectivity ratio indicates the relative strength of the turtles’ selectivity based on each factor. *indicate p values that are significant at the 0.05 level. aCalculated as the absolute value of the ratio of the size of the turtle effect to the size of the intercept. sensitivities. Levenson and colleagues [25] observed well- Colour is not the only visual factor employed in food defined peaks at 515 and 570, with a relatively constant selection.
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