1 1 ‘The thieving magpie’? No evidence for attraction to shiny objects 2 T.V. Shephard, S.E.G. Lea, N. Hempel de Ibarra 3 Centre for Research in Animal Behaviour, University of Exeter, Perry Road, Exeter, EX4 4QG, 4 UK 5 6 Corresponding Author: 7 Dr Toni Vernelli Shephard 8 T.Shephard@exeter.ac.uk 9 2 10 Abstract 11 It is widely accepted in European culture that magpies (Pica pica) are unconditionally attracted 12 to shiny objects and routinely steal small trinkets such as jewellery, almost as a compulsion. 13 Despite the long history of this folklore, published accounts of magpies collecting shiny objects 14 are rare and empirical evidence for the behaviour is lacking. The latter is surprising considering 15 that an attraction to bright objects is well documented in some bird species. The present study 16 aims to clarify whether magpies show greater attraction to shiny objects than non-shiny objects 17 when presented at the same time. We did not find evidence of an unconditional attraction to 18 shiny objects in either captive or free-living birds. Instead, all objects elicited responses 19 indicating neophobia in free-living birds. We suggest that humans notice when magpies 20 occasionally pick up shiny objects because they believe the birds find them attractive, while it 21 goes unnoticed when magpies interact with less eye-catching items. The folklore may therefore 22 result from observation bias and cultural inflation of orally-transmitted episodic events. 23 3 24 Introduction 25 It is widely believed across Europe that magpies (Pica pica) are unconditionally attracted to, and 26 collect, shiny objects. A Google search on the term 'magpie shiny object' produced 60,100 results 27 in 0.28 seconds (February, 2014). Most of these are descriptions of magpies that make reference 28 to their 'weakness for shiny things' (Winterman, 2008) or reputation for 'stealing jewellery' 29 (BBC, 2003). Although such assertions are usually stated as fact, no references or examples are 30 given. The belief is so ingrained in our culture that one definition given for ‘magpie’ in the 31 Collins English Dictionary is 'a person who hoards small objects' (Collins, 2013). Perhaps the 32 most famous example of this folklore penetrating popular culture is Rossini's opera 'The thieving 33 magpie', first performed in 1817, where a servant girl is executed for a series of silver thefts 34 which were actually committed by a magpie. Despite the folklore’s long history and widespread 35 acceptance, published accounts of magpies stealing or collecting shiny objects are rare and 36 empirical research on the subject is lacking. 37 An extensive internet search uncovered just two published accounts of magpies stealing shiny 38 things: a missing engagement ring that was discovered in a magpie nest (Telegraph, 2008) and a 39 magpie in Rochdale stealing keys, coins and a spanner (a shiny tool) from an automotive garage 40 (Manchester Evening News, 2007). Without empirical research, it is not known whether these 41 birds had an unconditional attraction to shiny objects, or if the folklore has caused observation 42 bias in the human population. In other words, we notice when magpies collect shiny objects 43 because we 'know' they are attracted to shiny objects but we do not notice when they interact 44 with less eye-catching items. A non-specific attraction to objects was demonstrated by Heinrich 45 (1995) with four hand-raised juvenile ravens, birds who are also reputedly attracted to shiny 46 objects. The young birds contacted novel items placed in their familiar aviary significantly more 47 than familiar items; however, their attraction depended solely on the novelty of the item "without 48 relevance to its palatability or shininess." 4 49 Research investigating cognitive abilities and object interaction in magpies is scarce. However, 50 attraction to shiny or bright objects has been documented in several other bird species, with 51 many using them as non-body ornaments, to attract mates or influence parental investment 52 (outlined in Schaedelin and Taborsky 2009). Black kites (Milvus migrans) place them in the nest 53 to act as threats to conspecifics, revealing the viability and conflict dominance of the signaller 54 (Sergio et al. 2011). Some corvid species are known to collect and cache non-food objects and 55 this may be an expression of exploration, although this behaviour does not appear to be colour 56 specific (Jacobs et al. 2014). We performed experiments with captive wild-born magpies and 57 free-living magpies (during breeding and non-breeding periods) to test for an unconditional 58 attraction to shiny objects or any sign of collection of non-food objects, and to investigate 59 possible explanations for such behaviour. In the absence of such an attraction, a neophobic 60 response to objects might be expected; accordingly we recorded behaviour that could indicate 61 either neophobia or ambivalence towards the objects. Neophobia was measured as a reduction in 62 the rate of feeding in the presence of the test objects. Five behaviours, approach/withdrawals 63 (see Greenberg and Mettke-Hoffman, 2001), walk-bys, fly-overs, jumping jacks (see Heinrich, 64 1988) and neck extensions, were classified as ambivalent behaviour, and ambivalence scores 65 were calculated as the sum of the numbers of all these behaviours exhibited in a session. Full 66 operational definitions of these behaviours are given in Table S1. 67 68 Methods 69 Captive Study 70 Eight magpies were obtained from three wildlife rescue centres in the UK. All birds were 71 deemed to be suitable for release back into the wild at the time of acquisition. They were housed 72 in an aviary on the roof of the laboratory. The accommodation provided a shed and a flight cage 5 73 (Fig. S1). There was a large, hinged hatch in the wall of the shed adjacent to the flight cage. A 74 large tray filled with soil was situated in the flight cage (outside of the test arena) so the birds 75 could cache food or other objects. A second large tray filled with water was provided for 76 bathing. The birds were colour banded for individual identification. All birds that arrived in a 77 group were housed as a group. They were locked in the shed overnight, and while test materials 78 were being set out; during experimental sessions, birds not being tested were also locked in. At 79 all other times, all birds had free access to both the shed and the flight cage. 80 On arrival at the laboratory, the birds were habituated to feeding from two plastic trays situated 81 at the opposite ends of the main aviary (test arena, Figure S1). The shiny-object tests formed part 82 of a random sequence of novel object tests that followed habituation; the other tests involved 83 presenting birds with familiar shaped trays in novel colours (black, silver and red or blue) and 84 novel shaped trays (8cm deeper) in the familiar colour. In all tests, the trays contained 85 mealworms. In the shiny objects test, two piles of six zinc-plated steel woodscrews were placed 86 in the aviary, each 20cm from a feeding tray. One pile contained silver screws and the other blue 87 screws. This test was only performed once with each bird. The screws were 7cm long. Before 88 the study began, half of the screws were painted blue with matt aerosol paint. The remaining 89 screws were left in their original shiny silver colour. 90 All sessions were videotaped with a tripod-mounted video camera situated inside an observation 91 hide located approximately 20m from the flight cage. The tests were performed between May 92 and August 2010. 93 94 Field Study 95 The field experiment was conducted at eight sites on the university campus, where magpies are 96 accustomed to regular human activity, allowing observations to be conducted from a close 6 97 proximity (<20m). To prevent pseudoreplication, the sites were separated by a minimum of 98 500m, about twice the maximum extent of territories defended by breeding magpies across 99 northern Europe (Birkhead 1991, p. 43). Each study site had a resident pair of magpies, 100 identified as the same pair in each session by their habituation to the observer and to the feeding 101 protocol, as well as their defence of the feeding area when other magpies approached. This 102 provided a total of 16 birds in the field study, but, as the two birds at each site could not be 103 reliably individually identified they are treated as one unit for analyses of mean feeding latency 104 and frequency and the mean ambivalence score. 105 The experiment took place in two phases. The first series of tests were performed at six sites 106 during the non-breeding season, from August to September 2011. The same tests were then 107 repeated at four of the same sites and two new sites throughout the breeding season, February to 108 April 2012. The new sites were required as the birds from two summer sites did not re-engage in 109 the breeding season. 110 The test objects were screws as used in the captive study, small foil rings (3cm diameter) and a 111 small rectangular piece of aluminium foil (7cm x 5cm). Half of the screws and rings were 112 painted blue with matt aerosol paint, and the rest left in their original shiny silver colour, as was 113 the piece of aluminium foil. 114 Before the beginning each phase, food was provided in two loose piles on the ground daily at 115 each study site for two weeks, and the observer recorded data as in the intended tests. The birds 116 were considered to be habituated when all of the food provided was taken in the presence of the 117 observer and within 20 minutes of provisioning. Food continued to be provided throughout the 118 study, with test objects placed next to the food during test sessions. Once the birds were 119 habituated, three control sessions were conducted to determine the birds' feeding motivation and 120 whether they had a side preference (right or left side of the feeding area). Two equal portions of 7 121 nuts were placed in loose piles on the ground approximately three metres apart, and at roughly 122 equal distance from the observer and from tree cover. Figure S2 illustrates these procedures. 123 Shiny object tests were conducted once three successful control sessions had been completed 124 (success was defined as the birds appearing within 15 minutes and feeding from the piles). Two 125 loose piles of nuts were placed on the ground in the same locations as in the control sessions but 126 with the addition of two piles of objects (screws or rings), each placed 30cm from a nut pile. One 127 object pile contained four silver objects and the other four blue objects. During the breeding 128 season, a further test was conducted with a rectangular piece of aluminium foil placed on the 129 ground next to one nut pile and secured with a small hair pin (Fig. S2). In the non-breeding 130 phase two object tests were performed at each site, one with screws and one with rings. In the 131 breeding phase a minimum of eight tests were performed at each site, with multiple exposures to 132 the rings and screws and one test with the foil rectangle. The tests were spaced out to incorporate 133 early nest-building, final nest-building and incubation and were performed in a random 134 sequence. In both phases, the sequence of tests varied across sites. Control sessions lasted for 30 135 minutes or until the food was depleted, whichever came first. All test sessions lasted for 30 136 minutes, even if the food was depleted sooner, to give the birds ample time to investigate the 137 objects. If no magpies arrived in the first 15 minutes of an experimental session it was 138 abandoned and its data were discarded. 139 140 Binoculars (10x magnification) were used to confirm the number of food items taken in each 141 visit. All sessions were videotaped with a tripod-mounted video camera situated 15 to 20m from 142 the food and positioned to give a panoramic view of the feeding area. The video footage was 143 viewed to measure feeding latency and feeding frequency, which were considered to be 144 measures of neophobia, and to record ambivalent behaviours. One person coded the sessions 145 from the non-breeding phase and another coded those from the breeding phase, and also recoded 8 146 three sessions from the non-breeding phase. Pearson's correlations and comparisons of means 147 confirmed consistent coding: the correlations between coders were 1.00, 0.99 and 0.99 for 148 feeding latency, feeding frequency and ambivalence scores respectively, P<.05 in all cases, and 149 the Means ±se for the two observers were 246s ±202 and 245s ±202 for feeding latency, 7.33 150 ±1.09 and 8.67 ±1.61 for feeding frequency, and 11 ±5.86 and 12 ±6.49 for ambivalence score. 151 152 Statistical procedures 153 Data from the captive test and the foil test were analysed using Wilcoxon Rank Sum tests. 154 General Estimating Equations (GEE) were used to analyse the remaining field data to 155 accommodate the non-normal distribution and the use of repeated measures (Garson, 2012). The 156 most appropriate model type, working correlation matrix structure and subset of predictors were 157 chosen based on the Goodness of Fit statistics QIC (quasi-likelihood under independence 158 criterion) and QICC (a corrected version that rewards parsimony). Feeding latency data were 159 analysed using identity-inverse Gaussian regression whereas feeding frequency and ambivalence 160 data were analysed using negative binomial regression. Least Significant Difference tests were 161 used to examine pairwise contrasts. Spearman Correlation Coefficients were used to explore 162 whether ambivalent behaviour changed with repeated exposure to the objects in the field study. 163 GEE analyses on feeding latency, feeding frequency and ambivalence scores were first run with 164 the control sessions split into multiple phases, each comprised of the three sessions preceding a 165 test. No qualitative differences between the control sessions across the different phases were 166 found so their data were combined and treated as one control condition. This resulted in a better 167 model fit for each of the analyses. All analyses were carried out using SPSS v20. 168 9 169 Results 170 Captive study 171 None of the eight birds made contact with any object, shiny or blue. The presence of the objects 172 did not deter them from feeding from the trays next to the objects. Feeding latencies in this test 173 were not significantly different to the preceding control session (means ±se: control = 42s ±13, 174 screw test = 23s ±19; W = 16, N = 8, P = 0.313). Additionally, there was no significant 175 difference in feeding latency between the trays next to silver and blue screws (means ±se: silver 176 = 325s ±161, blue = 370s ±223; W = 4, N = 8, P = 0.844). The birds exhibited little ambivalence 177 in the presence of the screws, with scores in this test lower than the other novel object tests 178 conducted during the study (mean score ±se: shiny object test = 3.13 ±1.34, other tests in captive 179 study ranged from 8.88 ±2.70 to 25.88 ±7.97). 180 Field study 181 Magpies only made contact with a shiny object twice in 64 tests. Both incidents occurred at the 182 same site, once in the non-breeding phase and once during early nest-building. One silver ring 183 was picked up and immediately discarded in both instances. No other object interactions 184 occurred at any site. 185 Figure 1 shows that birds in the field appeared to find the test objects aversive, with significant 186 differences in feeding latencies and frequencies for the food piles across three conditions 187 (control, ring test, screw test; feeding latency: χ2 = 23.52, df = 2, P <0.001; feeding frequency: χ2 188 = 12.68, df = 2, P = 0.002). Pairwise contrasts between conditions confirm that magpies fed from 189 the piles significantly faster and took significantly more nuts in the control condition than when 190 objects were present. In the foil test, magpies showed a preference for the control pile over the 191 pile next to the foil rectangle, feeding from the control pile sooner (W = 1, N = 6, P = 0.080; 192 Figure 1a) and taking significantly more nuts from it (W = 0, N = 6, P = 0.041; Figure 1b). The 10 193 aversion to feeding from food piles beside objects remains when the non-breeding and breeding 194 phases are examined separately (test*season interaction: feeding latency: χ2 = 5.87, df = 2, P = 195 0.053; feeding frequency: χ2 = 1.28, df = 2, P = 0.527). 196 Figure 1 also shows that screw colour (shiny or blue) did not affect magpies’ reactions to the 197 food piles during either phase (breeding and non-breeding). The birds took significantly longer 198 to feed from piles beside blue rings in the breeding season (test*colour*season interaction: 199 feeding latency: χ2 = 14.16, df = 4, P = 0.007; Figure 1a) but there was no difference in the non- 200 breeding phase. Ring colour did not affect feeding frequency in either phase (test*colour*season 201 interaction: feeding frequency: χ2 = 5.09, df = 4, P = 0.278, Figure 1b). Colour comparisons were 202 not confounded by a positional bias (mean feeding latency ±se: right pile = 350s ±49, left pile = 203 298s ±40, χ2 = 1.62, df = 1, P = 0.203; mean feeding frequency ±se: right pile = 4.65 ±0.31, left 204 pile = 4.90 ±0.41, χ2 = 2.62, df = 1, P = 0.106). 205 Figure 2 shows that the pattern of ambivalent behaviour also implies that the birds were wary of 206 the objects. There was a significant difference in ambivalence scores across the four conditions 207 (control, ring test, screw test, foil test; χ2 = 27.5, df = 3, P <0.001). Pairwise contrasts between 208 conditions reveal the magpies displayed significantly more ambivalence in the ring and screw 209 tests than in the control sessions. Ambivalence scores decreased with repeated exposure to the 210 objects (N = 6, n = 163, r = -0.187, P = 0.017). 211 212 Discussion 213 This study exonerates Rossini’s magpie, finding no evidence to suggest the species is 214 unconditionally attracted to shiny objects. The birds either ignored or avoided both shiny and 215 blue objects, with little difference observed between breeding and non-breeding seasons. There 216 were two interactions with shiny rings at one site, but these occurred after the food was depleted 11 217 rather than when the objects were first presented, suggesting investigations into a potential food 218 item rather than unconditional attraction. 219 Rather than being attractive to magpies, the objects appeared to induce neophobia in most of the 220 birds in the field - demonstrated by increased feeding latency, decreased feeding frequency and 221 more ambivalent behaviour when objects were present than during control sessions. The free- 222 living birds reacted this way to both shiny and blue objects, as well as to different shaped 223 objects. The decline in ambivalence scores with repeated exposure to the objects suggests the 224 birds did habituate to their presence over time. This agrees with descriptions of object neophobia 225 in other corvid species (Greenberg 2003; Greenberg and Mettke-Hofmann 2001) and we have 226 investigated it more fully in other studies (Vernelli, 2013). Birds in captivity did not show any 227 object-related avoidance. Similar differences between wild and captive populations have been 228 observed in kea (Huber & Gajdon 2006) and spotted hyenas (Benson-Amram, Weldele & 229 Holekamp 2013). They may reflect the artificial nature of captive settings where animals are 230 confined in close proximity to novel stimuli, whereas wild animals are free to avoid fear- 231 provoking objects. 232 We suggest the widely-held belief that magpies are unconditionally attracted to shiny objects 233 results from cultural generalisation of anecdotal evidence, demonstrating how biases in 234 observations of animals may determine the broad public perception of species and their impact 235 on the environment. 236 237 Acknowledgements: 238 We thank RSPCA, Secret World Wildlife Rescue and Crows are Us for providing rescued 239 magpies for the captive study. TVS was funded by the University of Exeter Research 240 Studentship. The authors declare that they have no conflict of interest. 12 241 242 References 243 244 BBC (2003, 4th July) Magpies. Retrieved March 26th, 2014, from 245 http://news.bbc.co.uk/dna/place-lancashire/plain/A1094230 246 Bensom-Amram S, Weldele ML & Holekamp KE (2013) A comparison of innovative problem- 247 solving abilities between wild and captive spotted hyaenas, Crocuta crocuta. Anim Behav 248 85:349-356. 249 250 Birkhead TR (1991) The Magpies: The ecology and behaviour of Black-billed and Yellow-billed Magpies (1 ed.). London: T & AD Poyser. 251 Collins (2014) English dictionary: Definition of magpie. Retrieved March 26th, 2014 from 252 http://www.collinsdictionary.com/dictionary/english/magpie?showCookiePolicy=true 253 Garson GD (2013) Generalized Linear Models / Generalized Estimating Equations, 2013 254 Edition. Asheboro, NC: Statistical Associates Publishers. 255 Greenberg R (2003) The role of neophobia and neophilia in the development of innovative 256 behaviour of birds. In SM Reader & KN Laland (Eds) Animal Innovation (pp 175-196). 257 Oxford: OUP. 258 259 Greenberg R & Mettke-Hofmann C (2001) Ecological aspects of neophobia and neophilia in birds. In V Nolan Jr & CF Thompson (Eds) Current Ornithology 16: 119-178. 260 Heinrich B (1988) Why do ravens fear their food? Condor 90: 950-952. 261 Heinrich B (1995) Neophilia and exploration in juvenile common ravens, Corvus corax. Anim 262 263 264 Behav 50: 695-704. Huber L & Gajdon GK (2006) Technical intelligence in animals: the kea model. Anim Cog 9:295-305. 13 265 266 267 Jacobs IF, Osvath M, Osvath H, Mioduszewska B, von Bayern AMP & Kacelnik A (2014) Object caching in corvids: Incidence and significane. Behav Proc 102:25-32. Manchester Evening News (2007, 15th February) Magpie swoops to steal keys and tools. 268 Retrieved March 26th, 2014, from http://www.manchestereveningnews.co.uk/news/greater- 269 manchester-news/magpie-swoops-to-steal-keys-and-tools-1045325 270 Schaedelin FC , Taborsky M (2009) Extended phenotypes as signals. Biol Rev 84:293-313. 271 Sergio F, Blas J, Blanco G, Tanferna A, Lopez L, Lemus JA, et al. (2011) Raptor nest 272 273 decorations are a reliable threat against conspecifics. Science 331:327-330. The Telegraph (2008, 28th August) Magpie steals woman's engagement ring and buries it in nest 274 for three years. Retrieved March 26th, 2014, from 275 http://www.telegraph.co.uk/news/newstopics/howaboutthat/2637365/Magpie-steals-womans- 276 engagement-ring-and-buries-it-in-nest-for-three-years.html 277 278 279 280 281 Vernelli T (2013) The complexity of neophobia in a generalist foraging corvid: the common magpie (Pica pica). Unpublished PhD thesis, University of Exeter. Winterman, D (2008, 28th March) Why are magpies so often hated? BBC News Mag. Retrieved March 26th, 2014, from http://news.bbc.co.uk/1/hi/magazine/7316384.stm 14 282 Figure captions 283 284 Figure 1. Feeding behaviour of free-living magpies (6 sites, 202 total trials). Birds (a) fed more 285 quickly and (b) took more food items when no objects were present. The two columns in control 286 condition represent the left and right food piles. Error bars show the standard error. *P <0.05, 287 **P <0.005. 288 289 Figure 2. Ambivalence scores (±se) for field-tested magpies (6 sites, 202 total trials). Birds 290 showed more ambivalence when test objects were present. *P = 0.050, **P ≤0.026. 291 15 292 Figure 1. Feeding behaviour of free-living magpies (6 sites, 202 total trials). Birds (a) fed more 293 quickly and (b) took more food items when no objects were present. The two columns in control 294 condition represent the left and right food piles. Error bars show the standard error. *P <0.05, 295 **P <0.005. 296 297 16 298 Figure 2. Ambivalence scores (±se) for field-tested magpies (6 sites, 202 total trials). Birds 299 showed more ambivalence when test objects were present. *P = 0.050, **P ≤0.026. 300