Tape lures swell bycatch on a Mediterranean island harbouring illegal bird trapping

1. Background

Natural resources are globally threatened owing to progressive overharvesting, with animal diversity being particularly affected by its consequences [1]. Many migratory birds are sensitive to anthropogenic impact, which has been a major cause of their decline [2,3]. In addition to indirect impacts caused by habitat loss [4,5] and environmental toxification [6], birds have also been impacted directly, by being targeted for food, the pet trade and sport [2,7,8].

Every year, over two billion birds migrate along the Afro-Palaearctic route [9] and concentrate in large numbers around the Mediterranean Basin [2,7,10]. Mediterranean islands are important stopover sites that provide sustenance and shelter for migrating birds. Humans have long exploited this sudden, seasonal abundance of food resources through hunting [11,12]. The need to supplement what historically was a low-protein diet has made such habits widespread and important culturally in several Mediterranean countries [2,13,14].

The island of Cyprus is an important stopover site for millions of migrant birds each year comprising over 200 species [15], and where illegal bird trapping currently represents the main threat to both resident and migratory birds [2,16,17]. Relative to its size, no other country has greater hunting pressure in the Mediterranean basin [2]. Poaching in Cyprus involves killing mostly passerines, and is a common practice rooted in Cypriot culture [13] that has received widespread condemnation in mainstream media [11,12,18]. Birds are trapped for food [2,19] and because of high demand, it is a lucrative business [11,12]. Eurasian blackcaps (Sylvia atricapilla), known locally as ‘ambelopoulia’, are most sought-after by poachers in Cyprus [16]. Although blackcaps are the main target, the use of non-selective trapping methods involving mist nets and limesticks results in the demise of individuals of many other species. Indeed, of 155 species recorded captured in 2018 in Cyprus, 82 are listed as conservation priority species under the EU Bird Directive [16] or in BirdLife International's European birds of conservation concern [20].

Poachers expect to amplify capture rates by using ‘tape lures’, playback devices that broadcast songs of target species. Birdsong typically blares from loudspeakers to attract migrating birds, which may respond to song from great distances [21]. Song playback has been shown to attract other species that may eavesdrop on heterospecific vocalizations as cues of habitat quality [22]. The use of tape lures to increase capture rates may thus harm both migratory and resident bird communities. Despite international condemnation, the massacre of birds in Cyprus continues, and hostile confrontations between hunters and conservationists are commonplace, mirroring conflicts in Malta [14]. One issue raised in the fight against poaching is that local authorities doubt the accuracy of estimates of bird casualties [18].

Here, we aimed to help conservation practitioners to estimate numbers of target and nontarget species captured by quantifying the effectiveness of target species' song playback in luring birds into nets in Cyprus. We used songs of Eurasian blackcap (hereafter blackcap), and of a local breeding species, Sardinian warbler (Sylvia melanocephala), to determine effects on capture rates of target and nontarget species. Both species may use vocalizations for conspecific and heterospecific interactions, including in competition for environmental resources. Because of this, we expected a strong response from conspecific as well as heterospecific competitors. Our findings should inform policy makers on the impact on wildlife of tape lures in illicit trapping operations.

2. Material and methods

3. Results

We caught significantly more birds (Wilcoxon signed-rank test: V = 273.5, p < 0.001) in experimental nets (mean = 2.77, 95% CI = 2.32–3.22), catching 333 birds (31 species), than in controls (mean = 0.75, CI = 0.46–1.04), where we caught 90 birds (24 species) (electronic supplementary material, table S4, figure 1). Blackcaps were attracted to both conspecific and Sardinian warbler playback, with fewer caught per experiment in summer, and more in spring, compared with autumn (table 1a; see electronic supplementary material, table S5 for model selection table). We also caught more blackcaps in 2019 than in 2016, indicating differences in blackcap abundance, but speakers used in 2019 also broadcast stimuli at higher amplitudes than in 2016 (electronic supplementary material, table S6). Sardinian warblers, by contrast, were positively affected by conspecific playback, but not blackcap playback (table 1b), while neither blackcap nor Sardinian warbler capture rates differed between controls (electronic supplementary material, table S7). Bycatch numbers were also significantly higher in experimental (n = 106 individuals of 30 species) than in control nets (n = 61 individuals of 23 species) (Wilcoxon signed-rank test: V = 515.5, p < 0.001) (figure 1), with both playbacks attracting more birds to experimental than control nets (table 1c). Significantly more nontarget birds were caught in summer compared with autumn, and in 2019 than in 2016. We also caught more species in experimental nets than in controls (table 1d).

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4. Discussion

Our study shows that use of tape lures results in an 11-fold increase in capture rates of target species. Indeed, in autumn, when trapping is rampant, blackcap numbers were almost fourteen times higher in experimental nets than in controls. Tape lures also attract more individuals of nontarget species, as well as a greater number of species, revealing more bycatch is expected to meet its demise at trapping sites. Yet, our increased capture rate estimates are likely conservative. Loudspeakers used in 2019 broadcast song at higher amplitudes than in 2016. If higher amplitude stimuli are more effective in luring birds to their demise, then poachers may swell numbers even more with powerful tape lures that can attract migrating birds from greater distances [21]. Furthermore, our use of few stimulus exemplars might also bias capture rates [26], e.g. if resident birds become habituated to specific exemplars. The proximity of playbacks might also increase captures in control nets if birds are drawn into the general area. More blackcaps caught in control nets in 2019 than 2016 suggests this possibility (electronic supplementary material, table S7).

Birdsong functions in mate choice and territory defence [35,36], so theoretically should only attract conspecific birds, and their close competitors (e.g. [37]). The song may also have a function during migration, however, and birds may use vocal signals to assess environmental quality [21,38] and dietary resource availability [39]. Indeed, some passerines, including blackcaps, may recognize other species’ song [23,40], especially if they share dietary and habitat preferences with those species whose songs they recognize, such as other Sylvia warblers (e.g. Sylvia curruca and Sylvia melanothorax) [23]. Phylogenetic relatedness might also correlate with similarity in song features [41].

Heterospecific responses from more distantly related species such as willow warbler (Phylloscopus trochilus), spotted flycatcher (Muscicapa striata), European chaffinch (Fringilla coelebs) and common redstart (Phoenicurus phoenicurus), however, are more likely to be elicited by either a food expectancy or the advantages of safety in numbers and increased risk detection [42]. By eavesdropping heterospecific signals, such as warning signals, birds may respond more rapidly to threats and optimize their foraging during migration [43]. That lower numbers of target species are captured in summer is largely because of the absence of blackcap during the breeding season and lower prevalence of these species at higher elevations where summer experiments took place. By contrast, increases in bycatch in summer suggest heterospecific attraction to vocal activity as an indication of dietary resources when parents are actively feeding young [22]. Our findings of a strong luring effect of playback on heterospecifics are not unprecedented [21,22,44–46] though and using playback with constant mist-netting efforts may lead to estimation biases in population dynamics studies [47].

Our aim here was to draw attention to the appalling bird slaughter in Cyprus by focusing on methods used by poachers and their consequent impacts. In this paper, we reveal that tape lures likely boost capture rates of target species by an order of magnitude. The joint use of non-selective traps with tape lures increases both numbers of individuals and breadth of species caught. Here, species captured included 12 listed as conservation priority under the EU birds directive and/or BirdLife International's list of European birds of conservation concern (electronic supplementary material, table S4). These included the breeding endemic Cyprus warbler S. melanothorax, whose population is already declining because of land-use change and displacement by a recent colonizer [24].

The tradition of using limesticks to catch migrant birds for a meal is illegal, much because the non-selectivity and extensive use of both limesticks and mist nets have led to the mass killing of birds in the Mediterranean region [11,12,18]. The situation in Cyprus is another example of the conflict between communities over hunting [14], but we believe conservationists should focus on emphasizing how the illegal wildlife trade-driven approach differs from local tradition, and that tape lures magnify the slaughter. We urge conservationists to take our findings on board [48], bearing in mind the limitations in the number of stimuli used and proximity of playbacks to control nets, and revise their capture rate estimation protocol to account for the over 10-fold increase in bird casualties where lures are used. Also, by targeting the sound source of song broadcasts, authorities can most effectively locate and dismantle traps; the broadcasts are, after all, what attract the birds there in the first place. Minimizing tape lure use would be a significant step in the battle against poaching.

Ethics

The Cyprus Game and Fauna Service provided ringing permits to A.N.G.K. and M.M., which also provided permission for use of playback devices. There is no project number given on these permits.

Data accessibility

Raw data and R code are available in the Dryad Digital Repository (https://doi.org/10.5061/dryad.905qftth1) [49]. Peer review accessible link: https://datadryad.org/stash/share/M6cXbFXz9VZ2JSvuRiyydqQvJyUg8foC5lS7skhFlQw.

Competing interests

M.M. volunteers as bird ringing officer for BirdLife Cyprus.

Funding

M.M. and M.S. were supported by grants from the AG Leventis Foundation.