Figures
Abstract
Despite the ubiquity and magnitude of food provision to wildlife, our understanding of its ecological effects and conservation implications is very limited. Supplementary feeding of ungulates, still one of the main paradigms of game management in Europe, occurs in natural areas on an enormous scale. We investigated the indirect effects of this practice on nest predation risk in the Polish Eastern Carpathians (Bieszczady Mountains). We hypothesized that the predators attracted to ungulate baiting sites would also forage for alternative prey nearby, increasing the nest predation risk for ground-nesting birds in the vicinity. We conducted a paired experiment by placing artificial nests (N = 120) in feeding and control sites (N = 12) at different distances from the ungulate feeding site. We also documented the use of three ungulate feeding sites by potential nest predators with automatic cameras. The proportion of depredated nests was 30% higher in the vicinity of feeding sites than at control sites (65%±31.5 vs 35%±32.1). The probability of a nest being depredated significantly increased with time and at shorter distances from the feeding site. We predicted that the area within 1-km distance from the feeding site would have a high risk (>0.5) of nest predation. We recorded 13 species of potential ground-nest predators at ungulate baiting sites. Most frequent were Eurasian jays Garrulus glandarius, mice and voles Muroidea, ravens Corvus corax, brown bears Ursus arctos, and wild boar Sus scrofa. Nest predators made most use of supplementary feeding sites (82% pictures with predators vs 8% with ungulates, the target group). Our study alerts of the impacts of ungulate feeding on alternative prey; this is of special concern when affecting protected species. We urge for a sensible management of ungulate feeding, which considers potential indirect effects on other species and the spatial and temporal components of food provision.
Citation: Selva N, Berezowska-Cnota T, Elguero-Claramunt I (2014) Unforeseen Effects of Supplementary Feeding: Ungulate Baiting Sites as Hotspots for Ground-Nest Predation. PLoS ONE 9(3): e90740. https://doi.org/10.1371/journal.pone.0090740
Editor: Marco Festa-Bianchet, Université de Sherbrooke, Canada
Received: October 30, 2013; Accepted: February 5, 2014; Published: March 5, 2014
Copyright: © 2014 Selva et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This study was supported by the Polish Ministry of Science and Higher Education (project NN304294037) and by the budget of the Institute of Nature Conservation PAS. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Supplementary feeding of wildlife is occurring on a colossal scale nowadays. Food supplementation has been widely used across the globe as a conservation and management tool, particularly for threatened species. Some examples include vulture restaurants, used for more than four decades in Africa, Europe, Asia and North America [1]; winter hay feeding of European bison Bison bonasus since the 18th century, and then during the restoration of the species into the wild in the 50s [2]; or feeding programmes of trophic specialists, like the Spanish imperial eagle Aquila adalberti [3] or the critically endangered Iberian lynx Lynx pardinus [4], after the collapse of their main prey. The provision of food to facilitate wildlife observations as a touristic attraction is also increasing together with a rapidly growing ecotourism industry [5]–[8]. Another recreational purpose is backyard bird feeding, whose popularity has increased over the last decades to the point that there is one feeder every nine birds estimated in the UK [9], and householders purchase half million tonnes of birdseed annually just in the USA and UK [10]. Supplementary feeding and baiting of game wildlife have even a longer tradition and since the last century have been common practices, mainly in Europe and North America [11]–[13]. Only in the Czech Republic, 83,367 ungulate feeding sites were reported in 2004 outside national parks [14].
Despite the ubiquity and magnitude of supplementary feeding practices in wildlife management, our understanding of the ecological effects and conservation implications of these food subsidies is still very limited [10]. As food availability is one of the main factors limiting animal populations [15], artificial feeding has been shown to bring direct benefits, like enhanced survival and reproductive performance [3], [16], [17]. However, these practices can be ineffective [18] or prove detrimental in the long-term [19]–[22]. Supplementary feeding also affects social and territorial behaviour, intra- and interspecific interactions, and animal movements and activity patterns [8], [23], [24]. The indirect effects of supplementary feeding have received comparatively less attention. Feeding sites seem to play a role in disease transmission [10], [25], [26] and the spread of exotics [27], and can initiate trophic cascades. The concentration of scavengers at carrion dumps and vulture restaurants diminishes the presence of alternative prey species of facultative scavengers and increases the probability of nest predation in their surroundings [28], [29]. Backyard bird feeding has also been shown to increase predation on arthropod prey in the area [30], [31]. Herbivore concentrations around feeding sites are associated with overgrazing of the palatable vegetation and changes in the plant composition in the area [11], [19], [27]. These cascading effects may get special relevance when food subsidies are provided in natural and semi-natural areas and when they affect species of conservation concern.
Supplementary feeding of ungulates is still one of the main paradigms of game management in Europe. With the exception of the Netherlands and some Swiss cantons, where it is forbidden, ungulate feeding is practiced in all European countries. It is even obligatory by law and, therefore, conducted intensively, in most central European countries [12]. In North America, this practice has been intensively debated [32], particularly in relation to disease transmission risk [25], [26], and has been widely restricted or prohibited [13]. The goals of this practice have been to maintain high densities of animals for hunting; to improve their nutritional status, survival and reproductive performance, especially in winter, as well as the quality of trophies; to prevent damages in forestry and agriculture; and to attract ungulates to shooting spots or for recreation [11]–[13]. As supplementary feeding, baiting also implies the provision of natural or non-natural food to wildlife. Although the management goals of ungulate supplementary feeding and baiting differ (see definitions in [13], [26]; baiting is rather oriented to hunt or capture the animal), from an ecological perspective, these practices are equal and have similar indirect effects. Therefore, we have treated them indistinctly in this paper.
Here we investigated the effects of ungulate supplementary feeding on the predation risk of ground-nesting birds in the Carpathian Mountains, where this practice is a deeply rooted tradition and obligatory by law [12]. In Poland, it has dramatically increased in the last decades: recent estimates yield about 143 million tonnes of food supplied annually to ungulates in the Polish forests [33]. Ungulate feeding commonly commences in the end of summer and continues till mid spring, though sometimes it extends beyond the period of food shortage. This practice involves simply the establishment of feeding sites or places where the food is regularly thrown on the ground. Selective feeders are not used. These food subsidies may attract target species, some of them trophic generalists, like the wild boar Sus scrofa, as well as non-target species, including predators [34], [35]. Therefore, by subsidizing predators and increasing their pressure in the area, ungulate feeding may have an impact on prey species [34], [36]. We hypothesized that the predators attracted to the ungulate bating sites would also forage for alternative prey nearby, increasing the nest predation risk for ground-nesting birds in the vicinity. We documented a significant negative effect of ungulate feeding sites on nest predation risk.
Materials and Methods
(a) Ethics statement
The field study did not involve endangered or protected species. No animals were harmed, captured or handled in this study; the methods employed were non-invasive. No samples were collected. The field study was done in strict accordance with legal requirements in Poland. It was conducted in the public forest lands, managed by the Polish State Forest Administration. Research and motorized access of scientists to the public lands managed by the State Forest is guaranteed by the Polish Law on Forest from 28 September 1991. Photo-monitoring of supplementary feeding sites and taking pictures of protected species in public lands with automatic cameras do not require any permit in Poland. In spite of this, agreement from the Forest Districts in the study area was additionally guaranteed previous to the installation of the automatic cameras in the feeding sites.
(b) Study area
The study was carried out in the Bieszczady Mountains (c.a. 2000 km2, SE Poland, Fig. 1), located in the North-Eastern part of the Carpathians. Bieszczady is characterized by mountains of middle and lower altitude (between 400 and 1400 m a.s.l) and gentle slopes [37], [38]. The typical vegetation is the mountain forest, dominated by beech Fagus sylvatica and fir Abies alba, with admixtures of Norway spruce Picea abies and intertwisted with valleys and meadows (between 500 and 1150 m a.s.l.). Higher locations are dominated by these two conifers. In the zone above the upper tree line (called “polonina”, >1150 m a.s.l.), alpine meadows and subalpine grass and shrub communities are typical. The climate is continental. Winters can be quite severe with temperatures dropping below −30°C. Snow cover persists for about three months. The average annual air temperature is 4.9°C [37], [38].
Map of the Bieszczady Mountains (SE Poland), located in the Northern Carpathians. The nest predation experiment was conducted in the beginning of May 2011 for 15 days in the areas indicated (A–F). In each area, an ungulate feeding site (red circles) and a control site (blue triangles) were selected. State Forest Districts: Komańcza (A, B), Baligród (C), Cisna (D), Lutowiska (E) and Stuposiany (F).
The vertebrate community of the Bieszczady Mountains, with 284 documented species [38], is very rich. It includes five ungulate species (red deer Cervus elaphus, roe deer Capreolus capreolus, wild boar, European bison, and moose Alces alces, this last quite rare), three species of large carnivores (brown bear Ursus arctos, Eurasian lynx Lynx lynx and wolf Canis lupus), and at least 19 species of birds of prey [38]. From the 165 bird species breeding in the study area, tetraonids are represented by the hazel grouse Tetrastes bonasia, which is quite common. The black grouse Tetrao tetrix and capercaillie Tetrao urogallus are present in other areas of the Polish Carpathians and are among the ground-nesting birds of major conservation concern [39], [40]. The Bieszczady Mountains have a significant value for biodiversity conservation. They are part of the Natura 2000 network and the East Carpathians UNESCO MAB Reserve. The Bieszczady Mountains include a protected part (the Bieszczady National Park c.a. 300 km2); the rest of the area, exploited by the State Forest Administration, undergoes timber harvest and game management.
The study was conducted in the exploited part of the forest, specifically in the Forest Districts of Baligród, Cisna, Komańcza, Lutowiska and Stuposiany (c.a. 900 km2, Fig. 1). In this commercial part, supplementary feeding of ungulates is a game management practice conducted almost year-round, though more intensively in winter. The feeding sites are located inside the forest and consist usually of a small glade or more open forest where supplementary food (maize, beetroots, fodder, grain) is more or less regularly thrown on the ground in the proximity of hunting towers. These sites are typically used for many years. The aim of this practice is to both feed and attract game to these shooting spots [41]. The magnitude of this practice is high, in both the amount of food provided and the density of feeding sites. A total of 170 feeding sites has been inventoried in the study area (Selva et al. unpublished data). The annual amount of supplementary food provided by the State Forest Administration in these five Forest Districts during the hunting seasons of 2010/2011 and 2011/2012 was 614 and 787 tonnes, respectively (data from the Regional Directorate of the State Forest Administration in Krosno).
(c) Nest predation experiment
We designed a paired experiment with artificial nests in which we distributed them in lines, one close to a feeding site and one at a control site in each area (Fig. 1). We selected six feeding sites located in different areas, where ungulate food was supplied throughout all the year and that were at least 2 km apart from neighboring feeding sites. Within the same area, a control site was chosen for each feeding site within a mean distance of 2.5 km (range: 1.7–3.7), on the basis of habitat similarity (forest type, age and openness, and altitude) and taking into account that no other feeding site was located closer. The proximity of public roads and human settlements were avoided in the selection of sites for the experiment. The lines were located inside the forest, and the nests within each line were distributed at increasing distances from the corresponding feeding site (see distances in Table S1). The distance from each nest in the line to the corresponding feeding site was measured from the central point where the supplementary food was supplied with a handheld GPS. Feeding sites were supplied with maize prior to the start of the experiment and during the first inspection in order to standardize food conditions.
The experiments were conducted during May 2011, coinciding with the bird nesting season. At each site, ten artificial nests, each consisting of two Japanese quail (Coturnix coturnix) eggs, were set out in a line, imitating the nests of hazel grouse, a ground-nesting bird species common in the study area [42]. Hazel grouse nests were simulated by scraping vegetation and litter from the soil surface and making a small depression in the ground where two eggs were placed (Fig. 2). The nests were placed at the base of standing large trees or large fallen logs or trees, and at about 50% of tree canopy cover. Eggs were kept refrigerated until the day they were deployed in the field. We used latex gloves and rubber boots during handling to reduce human scent. In any case, the amount of scent tracks that we could leave would be similar in both feeding and control sites. Nests at a given site were placed about 25–30 m away from each other by step counting. GPS coordinates were taken at each nest and the distance to the middle point of the feeding site measured. A spruce branch was placed at the tree or log near each nest to facilitate relocation. To control for potential effects of the features of the nest location, each nest was assigned to one of the two location categories: tree base or fallen log/tree. A total of 120 nests were deployed and checked (Table S1). The artificial nest experiment started on 2nd May in areas A–D and on 3rd May in areas E–F, dates when the eggs were exposed. To minimize disturbance, nests were checked twice: 6 and 15 days after their placement (on 8th and 17th May in areas A–D, and on 9th and18th May in areas E–F). A nest was considered depredated if at least one egg was damaged or missing (Fig. 2). The eggs were not replaced. Signs of potential nest predators were noted whenever observed.
Each nest consisted of two Japanese quail (Coturnix coturnix) eggs and imitated the nests of hazel grouse (Tetrastes bonasia, A). Nests (N = 120) were checked 6 and 15 days after deployment. A nest was considered depredated if at least one egg was damaged or missing (B). Photos: Nuria Selva, Anne Scharf.
(d) Identification Of Potential Predators
Half of the feeding sites where the nest experiments were conducted (areas B, C and F; Fig. 1) were continuously monitored with automatic cameras (Reconyx Rapid Fire Professional) to document the presence of potential predators of ground nests. The photo-monitoring of these sites started on 25th April, one week before the nest predation experiment was initiated, and it was conducted until the end of May, which corresponds to the hazel grouse's egg-laying and incubation period in Southern Poland [43]. The cameras were checked (batteries and memory card changed) in the days of nest placement or inspection. In order to obtain a statistically balanced data, the automatic cameras were programmed to take a single picture every 5 minutes. This design was preferred to the triggering program for several reasons: (1) to avoid biases related to species of larger size triggering the camera more often, and then being over-represented, and (2) because feeding sites cover a surface larger than the area of detection of camera motion sensors, therefore animals in the feeding site, but far away from the camera would also be registered. Each photograph taken by the automatic cameras was considered a record. The picture database included date, time, species presence/absence and number of individuals recorded. For each species of potential ground-nest predator, we reported the total number and mean proportion of pictures with the species present (calculated from the total number of positive pictures, i.e. those with species, genus or family identified, and then averaged for the three sites); the mean and maximum number of individuals observed; and, the percentage of camera-trap days when the species was recorded.
(e) Statistical Analysis
We used generalized linear mixed models (GLMMs) to relate nest predation (1/0, N = 120 nests) to the distance to the feeding site (meters, log-transformed), number of days elapsed since nest exposure (6 and 15 days) and type of simulated nest (at the base of standing tree N = 61, or by a log or fallen tree N = 59). The random term was the line at feeding and control sites (N = 12) nested in area (A–F, N = 6). Models were fitted in R (version 3.0.2) [44] with the lme4 package [45] (function glmer) using a logit link function and a binomial error distribution. Model terms that were not significant were eliminated in a backward stepwise procedure and the final model included only significant effects (p<0.05).
Results
The proportion of nests lost to predation was significantly higher (Wilcoxon matched pairs test, W = 35.5, p = 0.036) and almost double in the vicinity of ungulate feeding sites than at control sites (Fig. 3). After 6 days, 52% (SD±38.7) of the nests were depredated in the lines close to feeding sites, whereas in control sites only 20% (SD±16.7) of the nests were lost to predators. These proportions increased with time, and after 15 days, 65% (SD±31.5) and 35% (SD±32.1) of the nests were depredated in the feeding and control sites, respectively (Fig. 3). GLMM analysis showed that the distance to the feeding site and the number of days elapsed since nest exposure were the main factors affecting nest predation (Table 1). The probability of a nest being depredated significantly increased with time and at shorter distances from the feeding site. The type of nest and the interaction between the distance to the feeding site and the number of days elapsed since nest deployment did not have a significant effect on nest predation probability. Model predictions suggest that although the effect of feeding sites on the probability of a nest being depredated is a rather local effect (few hundred meters, Fig. 4) when the period of nest exposure is short, it significantly increases with time. Therefore, considering a typical incubation period of three weeks, all area within a 1-km radius from the feeding site would have a high risk of nest predation (>0.05, Fig. 4).
Boxplot of the probability of a nest being depredated in the vicinity of feeding sites (N = 6, between 9 and 108 m) and far away from ungulate feeding sites (N = 6, between 1.7 and 3.7 km). It shows field data as the proportion of depredated nests recorded at the end of the experiment, i.e. 15 days after nest deployment.
Estimates of the probability of nest predation with 95% confidence intervals (dashed lines) generated from the logistic model without random effects (Table 1, GLMM fitted to the field data using a logit link function and a binomial error distribution) as a function of the distance to the closest ungulate feeding site and the time elapsed since nest deployment. The effect of the time of nest exposure on nest predation probability is shown for two periods: A) 7 days and B) 21 days. Nest predation risk increased at shorter distances from ungulate feeding sites and with the number of days elapsed since nest deployment. Considering a typical incubation period of three weeks (B), model predictions indicate that the area within 1-km distance from ungulate supplementary feeding sites would have a high probability of nest predation (>0.05). Field data from the experiment is provided as a rug (small ticks inside the box) in the x-axis. Note the logarithmic scale in the x-axis.
We processed 26,249 pictures, obtained during 93 camera-trap days at three feeding sites during bird breeding period. We excluded 18 camera-trap days in which no pictures were obtained due to a technical error. We could identify wildlife to species, genus or family (including superfamily) in 5,122 pictures (19.5% of the total). For simplicity, we refer to them as species hereafter. Eighty-two per cent (4,178 pictures) of these positive pictures -where the species was identified- corresponded to potential egg predators. We recorded a total of 13 species of potential ground-nest predators at ungulate baiting sites, including nine mammalian and four avian species (Table 2). All these species are common in the study area [38]. We registered visits of woodpeckers Picidae, rodents Muroidea and a small mustelid Mustelidae; however the quality of images did not allow for proper species identification. The most frequent species of potential nest predator at the supplementary feeding sites was the Eurasian jay Garrulus glandarius, detected at 42% of the positive pictures and in 86% of the camera-trap days, followed by mice and voles, present in 68% of the camera-trap days (Table 2). The brown bear, the common raven Corvus corax, and the wild boar were also frequent at ungulate feeding sites, and were registered in 11, 8 and 6% of the positive pictures, respectively. Other visitors and potential egg predators included carnivores, such as the Eurasian badger Meles meles, the red fox Vulpes vulpes, the raccoon dog Nyctereutes procyonoides, and the wolf; red squirrels Sciurus vulgaris; and, the common buzzard Buteo buteo. In general, the most frequent species were also the most gregarious. Particularly the wild boar used to attend the feeding sites in large groups (Table 2). Ungulates, the target group of supplementary feeding practices, were recorded on 287 pictures, representing 7.9% (SD±7.68) of the positive pictures. When excluding the wild boar from the ungulate pictures, large herbivores were present just in 62 pictures (1.52% of the positive pictures, SD±1.834).
Discussion
We provided experimental evidence of an increase in the predation risk of artificial ground nests close to ungulate feeding sites. By attracting and concentrating nest predators in their vicinity, supplementary feeding sites can become predation hotspots. This is in agreement with other studies showing that the concentration of food subsidies redistributes local predators [28],[46],[47]. By aggregating predators, these subsidies increase the top-down effect of predation on alternative prey [28],[29],[31]. The magnitude and spatial extent of this effect may be stronger when the supplementary food is provided for long periods. This may be related to the fact that the probability of alternative prey being depredated increased with time ([31], this study). Experimental food additions for one month significantly increased predation risk in nests <50 m from feeders and also predator abundance in areas <100 m from feeders [47]. In the case of long-lasting ungulate carcasses, hares Lepus europaeus had a higher risk of encounter foxes within 1-km distance from those carcasses [28]. In our area, ungulate feeding sites have been used for decades and are supplied with food almost year-round. Our model indicated that the areas within 1-km distance from feeding sites had a probability of nest predation higher than 0.5 during the incubation period. Considering the large number of ungulate feeding sites in the study area, about one fifth of the area is estimated to have a high nest predation risk.
Our findings complement those of Cooper and Ginnett [34], who also found a lower survivorship of artificial nests close to deer feeders in North America. That study was conducted in a different habitat, mainly pastures for cattle grazing and in sites with open water, and simulated larger ground-nesting birds. Interestingly, the increase in nest predation rates obtained at feeding sites in relation to control sites was similar in both studies (27.5% vs 30% in our study). Hamilton et al. [36] also found that the survival of artificial turtle nests was 5.5 times higher at lakes without deer feeders. The consistency between these studies and our results indicates that the indirect negative effects of ungulate supplementary feeding practices on alternative prey, and particularly on ground-nesting species, may be more widespread than previously thought.
Artificial nests have been widely used in ecological studies, and in spite of their limitations in reflecting natural patterns [48], they often represent the only tractable way to get a sufficient sample to test hypothesis. They are particularly useful for comparisons among treatments or gradients of environmental conditions, and to investigate predation patterns of rare or endangered species [49]–[51]. In our study, the aim was to assess the effect of feeding practices on nest predation rates while controlling for field conditions as much as possible. Therefore, any potential bias would affect equally control and treatment sites. Moreover, a recent study using natural nests yielded the same results and confirmed the negative effect of food supplementation on nest predation rates [47].
Ungulate supplementary food attracted mostly non-target species. The species making most use of artificial food were potential nest predators (82% vs 8% of the pictures with ungulates). An intensive use of deer supplementary food by non-target species has also been documented in North America, mainly by raccoons Procyon lotor and passerine birds [34],[35]. Among the recorded visitors of ungulate feeding sites, squirrels, small mammals (shrews, voles and mice), corvids, mustelids, and canids have been often reported as predators of bird nests [52],[53]. By contrast, ungulates, the target group, were rare visitors, with the exception of the wild boar, which can become an important egg predator [54]. For instance, in some areas the proportion of capercaillie nests lost to wild boar can reach up to 30% [55]. In other areas of the Carpathian Mountains, both wild boar and brown bear have been recorded as frequent predators of hazel grouse and capercaillie nests [55]. Ungulate feeding practices are widely non-selective and may enhance population growth and range expansion of native species into new areas and sensitive habitats, such as the wild boar into alpine environments [56]. They also may promote invasive species which are potential nest predators, such as raccoons and raccoon dogs in Europe [57].
Wildlife management practices that increase nest mortality may come into conflict with the conservation of birds. Predation is one of the main causes of avian nest mortality [52],[58] and its increases can have important consequences for population dynamics [59]. The percentage of ground nests lost to predators has been estimated to average 30.6% in forest habitats and 48.8% in shrubs and grasslands [58]. In forest habitats, this practice may widely affect tetraonid birds, whose populations are seriously declining worldwide or are threatened at local, regional or national scales [40]. For instance, in some areas of the Carpathian Mountains about 65% of the capercaillie and hazel grouse clutches were lost to predators [55]. In open habitats, such as grasslands and wetlands, the impact of ungulate feeding sites may be even stronger, due to the generally higher predation rates in these habitats [58], and the higher probability of nest trampling [60]. Nest predation in European meadow birds has increased by more than 40% in the last decades, and is regarded as one of main reasons for the population decline of these birds [59]. These findings, together with the general increase of ungulate numbers and overabundance of them in many regions, including Poland [12],[41], stress the need to rethink ungulate supplementary feeding practices, particularly in central Europe.
We suggest that avoiding ungulate supplementary feeding sites in breeding areas of endangered species of ground-nesting birds may reduce the risk of nest predation, and should be seriously considered. In addition, removing the food from feeding sites before the start of the bird breeding season, when predation is higher [47],[55], seems also a sensitive and prudent strategy. Both recommendations are in line with those proposed by Cooper and Ginnett [34]. The location of ungulate feeding sites must be carefully selected, taking also into account the potential indirect effects on other species. We encourage further research on the effectiveness of these recommendations, and on the impacts of ungulate feeding sites on the reproductive success of specific bird species undergoing strong population declines. Not only game management, but also nature conservation projects should take into account the indirect effects of feeding practices. Supplementary feeding programs are also widely used in conservation (c.a. 50 European LIFE funded projects, LIFE project database http://ec.europa.eu/environment/life/project/Projects/). On the other side, conservation projects (e.g. for capercaillie conservation) aimed at improving the conservation status of ground-nesting birds often involve the direct reduction of nest predators, while ignoring indirect feeding of these predators through ungulate feeding practices.
Whenever strategies regarding supplementary feeding are to be adopted, the supply of food, and its temporal and spatial availability must be critically examined. The concentration of food supplies at feeding stations is an ecological perturbation, with important consequences for the plant and animal communities in the surrounding areas. This fact must be kept in mind when establishing and managing feeding sites, especially when protected and/or game species may be potentially affected [61]. Our findings remark that wildlife management should consider complex interactions, indirect effects, and community processes. Instead of management being focused on single species or group of species, an ecosystem approach should be favoured.
Supporting Information
Table S1. Data from the nest predation experiment conducted in May 2011. The area (A–F), nest line (a–l), type of site (feeding vs control), location of the nest (at the base of a large standing tree or under a fallen log or tree), air distance to the corresponding feeding site (m), number of days elapsed since the nest was deployed, and whether the nest was predated or not (1/0) in the field inspections. Field inspections were conducted 6 and 15 days after nest deployment.
https://doi.org/10.1371/journal.pone.0090740.s001
(XLSX)
Acknowledgments
We thank Piotr Kazimierczak, Zygmunt Sadura and Stanisław Sawiński from the Forest Districts of Stuposiany, Komańcza and Baligród for their cooperation during camera-trapping. The Regional Directorate of the State Forest Administration in Krosno provided data on the quantity of supplementary food. We are grateful to colleagues of the Carpathian Brown Bear Project for their support at different stages of the project, particularly to Anne Scharf and Ignacio Luque, who helped with the field work, and to Katarzyna Bojarska and Henryk Okarma. Dani and Albert Burgas helped with bird identification from the pictures, Przemek Chylarecki with bird literature, Jörg Albrecht with the code in R, and Anne Scharf and Adam Wajrak with pictures. Thomas Mueller provided helpful comments to a previous version of the manuscript. We thank Erica Nol and an anonymous reviewer for comments that greatly improved the manuscript. Phototrapping data will be provided by the authors upon request.
Author Contributions
Conceived and designed the experiments: NS. Performed the experiments: NS IEC. Analyzed the data: NS TBC. Contributed reagents/materials/analysis tools: NS TBC IEC. Wrote the paper: NS TBC IEC.
References
- 1.
Piper SE (2005) Supplementary feeding programs: how necessary are they for the maintenance of numerous and healthy vultures populations? In: Houston DC, Piper SE, editors. Proceedings of the international conference on conservation and management of vulture populations. Thessaloniki: Natural History Museum of Crete & WWF Greece. pp. 41–50.
- 2. Kowalczyk R, Taberlet P, Coissac E, Valentini A, Miquel C, et al. (2011) Influence of management practices on large herbivore diet- Case of European bison in Białowieża Primeval Forest (Poland). Forest Ecol Manag 261: 821–828.
- 3. González LM, Margalida A, Sánchez R, Oria J (2006) Supplementary feeding as an effective tool for improving breeding success in the Spanish imperial eagle (Aquila adalberti). Biol Conserv 129: 477–486.
- 4. López-Bao JV, Rodríguez A, Palomares F (2008) Behavioural response of a trophic specialist, the Iberian lynx, to supplementary food: Patterns of food use and implications for conservation. Biol Conserv 141: 1857–1867.
- 5. Walpole MJ (2001) Feeding dragons in Komodo National Park: a tourism tool with conservation complications. Anim Conserv 4: 67–73.
- 6. Orams MB (2002) Feeding wildlife as a tourism attraction: a review of issues and impacts. Tourism Manage 23: 281–293.
- 7. Brunnschweiler JM, Barnett A (2013) Opportunistic visitors: long-term behavioural response of bull sharks to food provisioning in Fiji. PLoS ONE 8: e58522.
- 8. Corcoran MJ, Wetherbee BM, Shivji MS, Potenski MD, Chapman DD, et al. (2013) Supplemental feeding for ecotourism reverses diel activity and alters movement patterns and spatial distribution of the southern stingray, Dasyatis americana. PLoS ONE 8: e59235.
- 9. Davies ZG, Fuller RA, Loram A, Irvine KN, Sims V, et al. (2009) A national scale inventory of resource provision for biodiversity within domestic gardens. Biol Conserv 142: 761–771.
- 10. Robb GN, McDonald RA, Chamberlain DE, Bearhop S (2008) Food for thought: supplementary feeding as a driver of ecological change in avian populations. Front Ecol Environ 6: 476–484.
- 11. Putman RJ, Staines BW (2004) Supplementary winter feeding of wild red deer Cervus elaphus in Europe and North America: justifications, feeding practice and effectiveness. Mammal Rev 34: 285–306.
- 12.
Apollonio M, Andersen R, Putman R (2010) European ungulates and their management in the 21st century. New York: Cambridge University Press. 618 p.
- 13.
Inslerman RA, Miller JE, Baker DL, Kennamer JE, Cumberland R, et al.. (2006) Baiting and supplemental feeding of game wildlife species. The Wildlife Society Technical Reviews 06-1.
- 14.
Bartoš L, Kotrba R, Pintíø J (2010) Ungulates and their management in the Czech Republic. In: Apollonio M, Andersen R, Putman R, editors. European ungulates and their management in the 21st century. New York: Cambridge University Press. pp. 243–261.
- 15.
Newton I (1998) Population limitation in birds. London: Academic Press. 597 p.
- 16. Schoech SJ, Bridge ES, Boughton RK, Reynolds SJ, Atwell JW, et al. (2008) Food supplementation: A tool to increase reproductive output? A case study in the threatened Florida scrub-jay. Biol Conserv 141: 162–173.
- 17. Newey S, Allison P, Thirgood S, Smith A, Graham IM (2010) Population and individual level effects of over-winter supplementary feeding mountain hares. J Zool 282: 214–220.
- 18. Margalida A (2010) Supplementary feeding during the chick-rearing period is ineffective in increasing the breeding success in the bearded vulture (Gypaetus barbatus). Eur J Wildl Res 56: 673–678.
- 19. Côté SD, Rooney TP, Tremblay JP, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Syst 35: 113–47.
- 20. Clout MN, Elliott GP, Robertson BC (2002) Effects of supplementary feeding on the offspring sex ratio of kakapo: a dilemma for the conservation of a polygynous parrot. Biol Conserv 107: 13–18.
- 21. Harrison T, Smith JA, Martin GR, Chamberlain DE, Bearhop S, et al. (2010) Does food supplementation really enhance productivity of breeding birds? Oecologia 164: 311–320.
- 22. Plummer KE, Bearhop S, Leech DI, Chamberlain DE, Blount JD (2013) Winter food provisioning reduces future breeding performance in a wild bird. Sci Rep 3: 2002.
- 23. Zanette L, Clinchy M (2010) Food supplementation leads to bottom-up and top-down food–host–parasite interactions. J Anim Ecol 79: 1172–1180.
- 24. Jerina K (2012) Roads and supplemental feeding affect home-range size of Slovenian red deer more than natural factors. J Mammal 93: 1139–1148.
- 25. Miller R, Kaneene JB, Fitzgerald SD, Schmitt SM (2003) Evaluation of the influence of supplemental feeding of white-tailed deer (Odocoileus virginianus) on the prevalence of bovine tuberculosis in the Michigan wild deer population. J Wildlife Dis 39: 84–95.
- 26.
Sorensen A, van Beest FM, Brook RK (2013) Impacts of wildlife baiting and supplemental feeding on infectious disease transmission risk: A synthesis of knowledge. Prev Vet Med: In press.
- 27.
Dunkley L, Cattet MRL (2003) A comprehensive review of the ecological and human social effects of artificial feeding and baiting of wildlife. Saskatchewan: Canadian Cooperative Wildlife Health Centre. 68 p.
- 28. Cortés-Avizanda A, Selva N, Carrete M, Donázar JA (2009a) Effects of carrion resources on herbivore spatial distribution are mediated by facultative scavengers. Basic Appl Ecol 10: 265–272.
- 29. Cortés-Avizanda A, Carrete M, Serrano D, Donázar JA (2009b) Carcasses increase the probability of predation of ground-nesting birds: a caveat regarding the conservation value of vulture restaurants. Anim Conserv 12: 85–88.
- 30. Martinson TJ, Flaspohler DJ (2003) Winter bird feeding and localized predation on simulated bark-dwelling arthropods. Wildlife Soc B 31: 510–516.
- 31. Orros ME, Fellowes MDE (2012) Supplementary feeding of wild birds indirectly affects the local abundance of arthropod prey. Basic Appl 13: 286–293.
- 32. Brown RD, Cooper SM (2006) The nutritional, ecological, and ethical arguments against baiting and feeding white-tailed deer. Wildlife Soc B 34: 519–524.
- 33. Marzec B (2012) Recepta na dokarmianie. (Recipe for supplementary feeding). Łowiec Polski 10: 14–22 (in Polish)..
- 34. Cooper SM, Ginnett TF (2000) Potential effects of supplemental feeding of deer on nest predation. Wildlife Soc B 28: 660–666.
- 35. Lambert BC, Demarais S (2001) Use of supplemental feed for ungulates by non-target species. Southwest Nat 46: 118–121.
- 36. Hamilton AM, Freedman AH, Franz R (2001) Effects of deer feeders, habitat and sensory cues on predation rates on artificial turtle nests. Am Midl Nat 147: 123–134.
- 37.
UNEP (2007). Carpathians Environmental Outlook. Geneva: United Nations Environment Programme. pp. 232.
- 38.
Winnicki T, Zemanek B (2009) Nature in the Bieszczady National Park. Ustrzyki Dolne: Bieszczady National Park. 176 p.
- 39.
Sikora A, Rohde Z, Gromadzki M, Neubauer G, Chylarecki P (2007) Atlas rozmieszczenia ptaków lęgowych Polski 1985–2004. (The atlas of breeding birds in Poland 1985–2004). Poznań: Bogucki Wydawnictwo Naukowe. 639 p. (in Polish).
- 40. Storch I (2007) Conservation status of grouse worldwide: an update. Wildlife Biol 13: 5–12.
- 41.
Wawrzyniak P, Jędrzejewski W, Jędrzejewska B, Borowik T (2010) Ungulates and their management in Poland. In: Apollonio M, Andersen R, Putman R, editors. European ungulates and their management in the 21st century. New York: Cambridge University Press. pp. 223–242.
- 42.
Bonczar Z (2007) Jarząbek Bonasa bonasia. In: Sikora A, Rohde Z, Gromadzki M, Neubauer G, Chylarecki P, editors. Atlas rozmieszczenia ptaków lęgowych Polski 1985–2004. (The atlas of breeding birds in Poland 1985–2004). Poznań: Bogucki Wydawnictwo Naukowe. pp. 88–89. (in Polish).
- 43. Swenson JE, Saari L, Bonczar Z (1994) Effects of weather on hazel grouse reproduction: an allometric perspective. J Avian Biol 25: 8–14.
- 44.
R Development Core Team (2013) R: A language and environment for statistical computing. www.R-project.org. (version 3.0.2). Vienna: R Foundation for Statistical Computing.
- 45.
Bates D, Maechler M, Bolker B, Walker S (2013) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.0-4. http://cran.R-project.org/package=lme4.
- 46. Wilmers CC, Stahler DR, Crabtree RL, Smith DW, Getz WM (2003) Resource dispersion and consumer dominance: scavenging at wolf- and hunter-killed carcassesin Greater Yellowstone, USA. Ecol Lett 6: 996–1003.
- 47. Borgmann KL, Conway CJ, Morrison ML (2013) Breeding phenology of birds: mechanisms underlying seasonal declines in the risk of nest predation. PLoS ONE 8: e65909.
- 48. Moore RP, Robinson WD (2004) Artificial bird nests, external validity, and bias in ecological field studies. Ecology 85: 1562–1567.
- 49. Summers RW, Green RE, Proctor R, Dugan D, Lambie D, et al. (2004) An experimental study of the effects of predation on the breeding productivity of capercaillie and black grouse. J Appl Ecol 41: 513–525.
- 50. McKinnon L, Smith PA, Nol E, Martin JL, Doyle FI, et al. (2010) Lower predation risk for migratory birds at high latitudes. Science 327: 326–327.
- 51. Seibold S, Hempel A, Piehl S, Bässler C, Brandl R, et al. Forest vegetation structure has more influence on predation risk of artificial ground nests than human activities. Basic Appl Ecol 14: 687–693.
- 52. Darveau M, Bélanger L, Huot J, Mélançon E, DeBellefeuille S (1997) Forestry practices and the risk of bird nest predation in a boreal coniferous forest. Ecol Appl 7: 572–580.
- 53. Pedersen Å, Yoccoz NG, Ims RA (2009) Spatial and temporal patterns of artificial nest predation in mountain birch forests fragmented by spruce plantations. Eur J Wildlife Res 55: 371–384.
- 54. Barrios-Garcia MN, Ballari SA (2012) Impact of wild boar (Sus scrofa) in its introduced and native range: a review. Biol Invasions 14: 2283–2300.
- 55. Saniga M (2002) Nest loss and chick mortality in capercaillie (Tetrao urogallus) and hazel grouse (Bonasa bonasia) in West Carpathians. Folia Zool 51: 205–214.
- 56. Geisser H, Reyer H-U (2005) The influence of food and temperature on population density of wild boar Sus scrofa in the Thurgau (Switzerland). J Zool 267: 89–96.
- 57.
Hulme PE (2007) Biological invasions in Europe: drivers, pressures, states, impacts and responses. In: Hester RE, Harrison RM, editors. Biodiversity under threat. Cambridge: RSC Publishing. pp. 56–80.
- 58. Martin TE (1993) Nest predation among vegetation layers and habitat types: revising the dogmas. Am Nat 141: 897–913.
- 59. Roodbergen M, van der Werf B, Hötker H (2012) Revealing the contributions of reproduction and survival to the Europe-wide decline in meadow birds: review and meta-analysis. J Ornithol 153: 53–74.
- 60. Mandema FS, Tinbergen JM, Ens BJ, Bakker JP (2013) Livestock grazing and trampling of birds' nests: an experiment using artificial nests. J Coast Conserv 17: 409–416.
- 61.
Selva N, Cortés-Avizanda A (2009) The effects of carcasses and carrion dump sites on communities and ecosystems. In: Donázar JA, Margalida A, Campión D, editors. Vultures, feeding stations and sanitary legislation: a conflict and its consequences from the perspective of conservation biology. Donostia: Sociedad de Ciencias Aranzadi. pp. 452–473.