Human–Wildlife Interactions 11(3):339–350, Winter 2017
Large birds of prey, policies that alter food availability and air traffi c: a risky mix for human safety R˞ˋ˳˗ M˘˛ˎ˗˘-O˙˘, Evolution and Conservation Biology Research Group, University Complutense of Madrid, E-28049 Madrid, Spain A˗˝˘˗˒ Mˊ˛ːˊ˕˒ˍˊ, Life Sciences and Engineering, University of Lleida, E-25198 Lleida, Spain [email protected]
Abstract: Raptors are considered to pose one of the greatest aviation bird strike risks. We investigated raptor bird strikes reported at the largest Spanish airport (Adolfo Suárez Madrid Barajas; AS-MB) from 2009 to 2016 to determine the factors contributing to the increased incidences and develop recommendations to mitigate the risks. We hypothesized that increased raptor bird strikes resulted from changes in foraging and dispersal patterns of Iberian Peninsula vultures (Aegypius spp. and Gyps spp.) after 2004–2005. We used information on raptor bird strikes obtained from offi cial databases and published studies, reported incidences of raptor bird strikes and their characteristics (i.e., time, location, species involved), data collected about raptor fl ight heights, and estimates of relative abundance of large raptors and their prey species obtained through standardized surveys conducted in the high priority aviation area around the airport to assess bird strike risks. Our fi eld work was conducted from June 2014 to May 2016. We confi rmed a direct relationship between the relative abundance of the raptors studied and their prey species in the priority aviation areas. Raptor bird strike risks increased during spring and summer when food sources were abundant in locations where fl ight altitudes of aircraft were <1000 m above ground level. Our observations appear to be related to European Union sanitary policies that altered the availability and occurrence of livestock carcasses. These changes may have increased the overall movement of vultures in search of new, scarcer, and more distant food sources, enhancing the likelihood of overlap with air traffi c corridors. Although further studies on aviation risk are needed, our results suggest the need to implement immediate remedial management actions to alter vulture habitat quality by reducing food sources in sensitive areas, and providing alternative food resources at distances suffi ciently far from commercial airports.
Key words: Aegypius monachus, airport management, bird strike, cinereous vulture, food availability, griff on vulture, Gyps fulvus, raptors, risk assessment, sanitary policies, Spain
Flying birds are one of the most hazardous et al. 2013). However, in general, there is a elements to commercial, private, and military lack of specifi c protocols for large raptors, aviation when air traffi c routes are poorly especially outside of North America, in terms of designed with respect to bird population deterrence activities inside and around airports distribution and migration routes (Cleary and and in managing food sources. Although risks Dolbeer 2005, DeVault et al. 2013, Lambertucci for aircraft collisions associated with Old World et al. 2015). Aircraft collisions with birds (i.e., vultures have been reported in Asia and Africa, bird strikes) result in economic losses due to including the highest ever recorded bird strike damage to aircraft components and sometimes collision (>11,000 m above ground; Satheesan lead to fatal accidents. At least 286 deaths and Satheesan 2000), in a European context worldwide have been caused by bird strikes or bird strikes have mainly involved waterfowl att empts to avoid birds during fl ight (Thorpe and medium- and small-sized fl ocking birds 2012). The risk varies depending on the traits (Soldatini et al. 2010). and size of the bird involved and is more An emerging trend has recently been serious when caused by large birds, including detected as a result of human safety concerns soaring raptors (DeVault et al. 2011). Raptors in Spain (Margalida 2016). In 2016, 10 people were estimated to cause 47% of bird strikes died in 3 crashes of private aircraft caused with private aircraft (Thorpe 2012). by collisions with Eurasian griff on vultures The bird strike problem has been addressed (Gyps fulvus). This level of risk had not been by managers and governing bodies (DeVault previously recorded and represents a milestone 340 Human–Wildlife Interactions 11(3)
Figure 1. Survey transects for obtaining relative abundances of birds of prey (numbers 5 and 6), and wild rabbit (Oryctolagus cuniculus), wood pigeon (Columba palumbus), and red partridge (Alectoris rufa; numbers 1 to 4), in the high-priority area (HPA) around the Adolfo Suárez-Madrid Barajas Airport, Madrid, Spain, between 2014 and 2016. The names of the towns in the study area are also shown (scale 1:10000). in comparison to global historic bird strike (Soldatini et al. 2010). Despite being a priority data. For example, from 1912 to 2012 for aircraft issue for aviation safety and the fact that <5,700 kg, 69 casualties from 32 accidents were Spain is home to the most important western recorded worldwide (mean 0.69 deaths/year; European populations of raptors (Deinet et al. Thorpe 2012). In addition, there have been at 2013), global patt erns of the impact, times, and least 26 collisions with raptors between 2006 places where the risk may be highest have not and 2015 around the largest Spanish hub been properly studied. This analysis is urgent (Adolfo Suárez-Madrid Barajas, AS-MB), with given the growing concern for the aff ected no human injuries reported (Tragsatec 2016), stakeholders (Margalida 2016). and yet no incidents had been reported before Our study constitutes the fi rst detailed analysis 2006. As a result, a change in the likelihood of of the interaction between large raptors (LBPs) collisions with raptors has occurred in recent and commercial aviation in Europe, specifi cally years, which necessitates a scientifi c assessment in Spain. We were interested in determining the and the adoption of appropriate management relative abundance of LBPs, the species involved, measures. places, time, season, and correlations with prey The causes of raptor bird strike hazards species and their causes in areas of greatest risk are not well understood for either the AS- for aviation, using the largest airport in Spain as MB airport or for aviation across Spain, in a case study. We hypothesized that the incidents terms of seasons, height from the ground, reported by the airport management authority, regions, species, time, and circumstances. At a both in numbers and in relation to height from European level, the available information on the ground, were correlated with the relative aircraft collision hazards is similarly scarce abundance of LBPs, and that their presence was Policies to mitigate bird risks • Moreno-Opo and Margalida 341 associated with prey species numbers inhabiting 1,000 m from the ground, where >90% of all priority avian areas. We assessed the eff ects that bird strikes are registered (Dolbeer 2006). diff erent environmental management policies Aviation at the airport was mainly dedicated to have had on LBP bird strikes locally and across passenger transport (>50 million movements/ Spain. Finally, we reviewed and proposed year, the fi fth highest in Europe) with a mean mitigation measures that could be implemented daily frequency of 1,036 fl ight operations on at the national level to reduce the LBP bird strike their 4 runways (
Table 1. Percentage distribution of fl ight height locations, in meters from the ground, of diff erent species of large soaring birds of prey.
Height from Aegypius Gyps Coragyps Aquila Gyps Gypaetus the ground 1 2 atratus and 4 5 5 Mean ± SD (m) monachus fulvus Cathartes aura3 nipalensis coprotheres barbatus 0–400 16.2 49.9 96.0 48.8 87.5 90.3 64.7 ± 31.5 401–800 55.7 38.1 4.0 37.4 12.5* 9.7* 26.2 ± 20.4 801–1,200 26.2 11.6 0.0 8.1 0.0* 0.0* 7.6 ± 10.3 >1,200 1.9 0.4 0.0 5.7 0.0* 0.0* 1.3 ± 2.6
1Jiménez and González 2012 2Boscaje 2012 3DeVault et al. 2005 4Spaar and Bruderer 1996 5Rushworth and Krüger 2014 *estimated from the published article selection patt erns of high priority areas around Data analysis the AS-MB airport. The monitoring period Data were analyzed to determine the lasted from June 2014 to May 2016 (2 years). relationship between the number and patt erns of In addition, we completed prey species LBP bird strikes and sightings with the relative surveys to evaluate the food abundance abundances of foraging LBPs and prey by for LBPs in the HPA and to understand its season. The relationship between the presence relationship with the relative abundance of of LBPs in the HPA and the relative abundance LBPs. The surveys were conducted biweekly by of prey species was also analyzed. driving a car along 4 predetermined transects Parametric techniques were used when on non-paved roads (Figure 1). We recorded all the data met the principles of normality and live wild rabbits (Oryctolagus cuniculus), wood homoscedasticity, including their logarithmic pigeons (Columba palumbus), and red partridges transformation. We performed linear regressions (Alectoris rufa), which are the selected prey of when the dependent and independent variables large raptors in Spain (Fernández de Simón were quantitative. This was the case of the et al. 2011), including vultures and facultative analyses of the relationship between the number scavengers that consume them as carcasses of incidents, the relative abundance of LBPs, (Delibes-Mateos et al. 2007, Blanco-Aguiar et al. and the relative abundance of prey, as well as 2012, Moreno-Opo et al. 2012, Moreno-Opo et those checking the link between fl ight heights al. 2016, Margalida et al. 2017). of the LBPs and of the incidents. Simple linear Prey surveys were conducted during the fi rst regression was also used to compare the trend hour after dawn or the hour prior to dusk, at a of the number of incidents around the AS-MB continuous speed of no more than 20 km/hr. We airport and the trend of the number of aviation also considered the distance traveled by vehicle fl ights in Madrid and all of Spain. For comparing to calculate a kilometer abundance index (KAI), the distribution of percentages of the fl ight expressed as the number of individuals divided at which incidents occurred, we carried out a by the distance driven in km. For rabbits, we frequency analysis (Chi-square). We considered also applied stratifi ed counts in assigned bands statistical signifi cance at P < 0.05. The statistical (up to 25 m from the vehicle and more than 25 m analyses were conducted with Statistica 6.1 to the vehicle; Fernández de Simón et al. 2011) (StatSoft, Tulsa, Oklahoma, USA). to obtain a relative density index expressed as the number of rabbits per hectare. The distance Results of the 4 itineraries of census was 12.8, 4, 4.5, and We found a direct relationship between food 5.2 km (Figure 1). We discarded monitoring availability, LBPs, and the number of aircraft during rainy and windy (>20 km/hr). The work incidents (mean 197.00 ± 181.59 incidents/year). was conducted from June 2014 to May 2016 (2 Regarding the hypothesis of a direct signifi cant annual periods). relationship between the number of incidents Policies to mitigate bird risks • Moreno-Opo and Margalida 343
Figure 2. Relationship between Kilometer Abundance Index (KAI) expressed as individuals (n)/km of cinereous vulture (Aegypius monachus; r2 = 0.62; P = 0.002) and griff on vulture (Gyps fulvus; r2 = 0.39; P = 0.028), as well as the relative density (individuals (n)/ha) of wild rabbit (Oryctolagus cuniculus; r2 = 0.62; P = 0.002) in relation to the number of incidents (sightings from aircraft + collisions) with aircraft around Adolfo Suárez-Madrid Barajas Airport, Madrid, Spain, between June 2014 and May 2016. and the relative abundance of the studied birds, Higher than 800 m, only 10.4% of incidents we checked this relationship for the species with soaring birds were recorded (Table 2). As causing >90% of the registered incidents such as a consequence, there was a marginally positive the cinereous and griff on vultures (F1,10 = 16.41, relationship between the proportion of locations
P = 0.002 and F1,10 = 6.52, P = 0.028 respectively; of the LBPs and the proportion of incidents for
Figure 2). Thus, the number of sightings and height classes (F1,2 = 12.59; P = 0.071). LBP bird strikes were directly related to their Our hypothesis on the association between relative abundance (F1,2 = 18.22, P = 0.050; LBPs and prey numbers was confi rmed: Figure 3). cinereous vultures and prey abundances were
With respect to fl ight heights, information associated (F1,133 = 6.78, P = 0.010 for rabbit, and on the distribution of aerial locations of LBPs F3,150 = 4.24, P = 0.041 for all prey species jointly; showed an increased relative abundance Figure 4). Moreover, prey numbers were also between 0 to 400 m above ground, except for positively correlated to the number of incidents cinereous vultures (Table 1). Higher than 800 with aviation for all LBP species, both for rabbits m, the proportion of fl ight locations declined (F1,10 = 7.17, P = 0.023; Figure 2) and for all prey by 13.8%, while only 5.7% of the records species considered (F1,10 = 10.36, P = 0.009). corresponded to fl ights higher than 1,200 m. On Finally, we observed that fl ights decreased the other hand, the height at which incidents between 2004 and 2015 (8.7% from 401,503 to 2 occurred was heterogeneous (χ 3 = 62.24; P < 366,608 in Madrid, F1,10 = 6.41, P = 0.029; and 7.5%
0.001; Table 2), with these events observed to from 2,056,959 to 1,902,967 in Spain, F1,10 = 9.29, a greater extent between 0 and 400 m (69.4%). P = 0.012), unrelated to an increase in LSR bird 344 Human–Wildlife Interactions 11(3)
Figure 3. Linear regression of the number of incidents with aircraft (sightings from aircraft + collisions) in which a large bird of prey species was involved for the 2009–2016 period, in relation to their mean abun- dance (individuals (n)/km; r2 = 0.90; P = 0.050) around the Adolfo Suárez-Madrid Barajas Airport, Madrid, Spain, between June 2014 and May 2016.
strike hazards (F1,10 = 0.33; P = 0.58;
Table 2. Number and percentage distribution of commercial aviation incidents around Adolfo Suárez-Madrid Barajas Airport between January 2009 and May 2016 relative to the registered height from the ground (Tragsatec 2016). Height from the Bird sightings from ground (m) aircraft Bird strikes Total incidents n % n % n % 0–400 82 73.9 4 30.8 86 69.4 401–800 23 20.7 2 15.4 25 20.2 801–1,200 4 3.6 6 46.1 10 8.0 >1,200 2 1.8 1 7.7 3 2.4
Figure 4. Relationship between Kilometer Abundance Index (KAI) expressed as individuals (n)/km of cinereous vulture (Aegypius monachus) and wild rabbit (Oryctolagus cuniculus; r2 = 0.05; P = 0.010), around Adolfo Suárez-Madrid Barajas Airport, Madrid, Spain, between June 2014 and May 2016. in demographic parameter values (Margalida Changes in food occurrence and et al. 2014) as a result of the sanitary policy availability for the management of animal byproducts The enforcement of Regulation EC 1774/2002 implemented in the mid-2000s have been entailed the removal from the fi eld and described (Donázar et al. 2009). This policy destruction of >85% of livestock carcasses since (Council of Europe 2002) resulted in the closure 2004 in Spain (Moreno-Opo and Margalida of many widely distributed small feeding sites 2014). This changed the occurrence, abundance, for scavengers associated with slaughterhouses, and characteristics of food for scavenger species farms, or village dumping sites as well as the and in turn led to shifts in the demographic, compulsory removal of livestock carcasses ecological, and behavioral patt erns of vultures from the fi eld for their subsequent incineration. (Donázar et al. 2009, Margalida et al. 2014). 346 Human–Wildlife Interactions 11(3)
This regulation for carcass management did regulatory changes of the mid-2000s (Donázar not suffi ciently consider the negative eff ects at et al. 2010), moving toward more ingestion of an ecological level, applying the precautionary smaller carcasses (e.g., rabbit). For this reason, principle only for sanitary reasons (Margalida in the summer vultures perform larger foraging et al. 2010). Unfortunately, no accurate data on movements to areas with food, which increases variables related to LBP bird strike risk before the risk of collision with aircraft (DeVault and and after the application of the aforementioned Washburn 2013), as has been observed at the regulation are available for the AS-MB airport. AS-MB. However, there is evidence, at a national scale, The aforementioned changes have led of changes in space use by vultures that could griff on vultures to expand dispersal or be related to a higher probability of aircraft foraging movements to areas far from their incidents. nesting colonies (Margalida et al. 2010). An Vulture feeding sites were reconfi gured augmentation of travel distance, maximal in Spain after 2004–2005, with the general displacement, and fl ight elevation has been closure of indeterminate but abundant and shown to be a consequence of the reduction widely distributed sites (Margalida et al. 2010). in food availability (Spiegel et al. 2013), which This decline triggered previously infrequent would lead to an increase in collision risk with behaviors in vultures, especially for griff on aircraft because of a higher total number of vultures, such as predation on dying animals, prospective fl ights by vultures searching for the use of other types of prey, a greater tolerance food (DeVault and Washburn 2013). for human activity, and presence in areas far from the breeding range (Donázar et al. 2009, Hazard management Zuberogoitia et al. 2010). Reducing the LBP bird strike hazard is possible From the mid-2000s, food acquisition by if eff ective preventive measures are implemented vultures in landfi lls increased substantially (DeVault et al. 2013). These may include: 1) land (Donázar et al. 2010). Although this had use planning prior to the establishment of airport previously been observed in the griff on vulture, infrastructure, such that risk and environmental it was much less geographically and numerically assessments adequately consider the presence widespread. For the cinereous vulture, of soaring birds (Blackwell et al. 2009, Soldatini att endance at landfi lls had been very rare, but et al. 2010), and 2) risk detection in air traffi c now is common in practically all landfi lls in their corridors up to the maximum fl ight height of range. Furthermore, this att racts vultures to more birds (<1200 m; Table 1). urbanized zones, including airports, thus serving Avian radars have shown interesting as a lure toward areas sensitive for aviation. results at diff erent commercial and military Food availability for avian scavengers is not aerodromes (Beason et al. 2013). These radars uniform throughout the year. In general, the may allow large birds to be detected at a far highest mortality rate in livestock coincides enough distance from airports for eff ective with both adverse weather and calving. In mitigation, although available models do not wild ungulates, in addition to coinciding always track single soaring birds accurately with calving, the highest mortality occurs in (Gerringer et al. 2016). In the case that soaring autumn and winter, overlapping with the main raptors could be detected by the radars entering hunting season. These 2 food sources, with air traffi c corridors, it should be possible to which feeding sites are supplied, provide the modulate aircraft routes and fl ight frequencies highest biomass to the vulture diet (Costillo accordingly (Beason et al. 2013). et al. 2007, Donázar et al. 2010). During spring The fi rst proposed line of mitigation is the and summer, a higher energetic demand is management of food sources (Cook et al. 2008, needed due to chick-rearing, which is partially DeVault et al. 2013). The reduction in populations alleviated by the continuous presence of food in of prey species, especially rabbits, is essential landfi lls and by an increase in rabbit mortality given the key role played by this species as prey as a consequence of viral diseases (Delibes- (Delibes-Mateos et al. 2007). However, rabbit Mateos et al. 2007). In this sense, the diet of the control is not easy and requires suffi ciently most abundant griff on vulture shifted after the intense and frequent measures such as ferreting Policies to mitigate bird risks • Moreno-Opo and Margalida 347
(trapping rabbits with the help of domestic Management implications ferrets [Mustela furo]), the artifi cialization of the It is advisable to further explore changes in airport habitat (e.g., asphalting or enmeshing food availability for scavengers. The number soils and slopes to hinder warren construction), and distribution of feeding sites before 2003– gassing of burrows, or removal of surface- 2005 increased the carrying capacity and living individuals by shooting, which is the vulture numbers, and, along with other factors, most eff ective in reducing densities (Thompson shaped the spatial distribution of LBP breeding and Armour 1951). As for the management of nuclei. However, once the availability of sites with abundant and predictable carrion, livestock resources was modifi ed, LBP shifted their disposal and closure is the most widely spatio-temporal patt erns of foraging and food recommended measure in areas interfering selection, increasing their presence at new with commercial aviation (Cook et al. 2008, patchy and more predictable food resources. DeVault et al. 2013). It is essential to suspend These new patt erns may have led LBPs to move any biomass provision that could be exploited throughout the Iberian Peninsula in a diff erent by scavenging raptors in landfi lls or feeding way than before 2003–2005, which increased sites near airports. the potential for LSR bird strikes. In relation to the management of LBP The situation in Spain is novel and unique, populations, the main approach is to shift requiring urgent commitment from all sectors foraging movements from the most sensitive involved, with suffi cient economic investment areas to others with less potential risk. Changes to ensure human safety. The priority actions in habitat quality and diversion of birds to other to be further studied and developed are the areas with a greater ecological att ractiveness following: 1) test the usefulness of radar and free from aviation hazards have been systems aimed at detecting the bird strike risk in implemented for several species (Martin et al. sensitive air traffi c corridors to modify aircraft 2011, DeVault et al. 2013). The most effi cient routes or fl ight frequencies if appropriate, measure is to reduce food availability in higher and 2) implement active management of food risk areas along with a concurrent increase in resources for LBPs in 2 complementary ways: food availability in remote areas by means of the population reduction of prey species at the provision of carcasses (Margalida et al. 2010). HPA around the airports, and the promotion A wide range of bird deterrence measures and establishment of feeding sites for LBPs, have been used in airport management (Belant especially for vultures, outside sensitive areas and Martin 2011, DeVault et al. 2013). All for aviation with the purpose of modifying the the Spanish airports and several from other foraging movements toward more safety zones. parts of the world have control services that dissuade medium- and small-sized birds from Acknowledgments runways through falconry (Erickson et al. This work was carried out within the 1990). However, falconry has not been applied framework of the project “Guidelines for the to date for large soaring birds in airports due prevention of large soaring bird-strike hazard to the time investment in teaching falcons in relation to air safety,” commissioned by the to att ack non-prey species like raptors. This Spanish Ministry of Environment (MAPAMA) requires a signifi cant economic cost and live and developed by TRAGSATEC. It is part raptors used as decoys. Moreover, this has not of the collaboration between MAPAMA, the been previously tested to address this issue. State Air Traffi c Agency (AESA) and the However, pyrotechnics (Cleary and Dolbeer company managing air navigation and airport 2005), noise, light, and fi rearms have been operations of the Madrid airport (AENA). J. used to drive away raptors (Blackwell et al. Sánchez performed most of the fi eld work, 2002, Cook et al. 2008), even within the AS- and M. Abascal, D. Muñoz, R. Martínez, L. M. MB. 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Wildlife Research 56:623–632. R˞ˋ˳˗ M˘˛ˎ˗˘-O˙˘ is a wildlife biologist working at the General Directorate on Biodiversity Spaar, R., and B. Bruderer. 1996. Soaring mi- of the Spanish Ministry of gration of steppe eagles Aquila nipalensis in Environment and collabo- southern Israel: fl ight behaviour under various rates with the Evolution and Conservation Biology wind and thermal conditions. Journal of Avian Research Group of the Biology 27:289–301. University Complutense of Madrid. His main Spiegel, O., R. Harel, W. M. Getz, and R. Na- duties are related to the than. 2013. Mixed strategies of griff on vultures’ design of conservation (Gyps fulvus) response to food deprivation programs of endangered species, mainly birds, lead to a hump-shaped movement pattern. and the resolution of confl icts between wildlife and Movement Ecology 1:1. socioeconomic land uses. His Ph.D. degree was dedicated to the conservation and management of Thompson, H. V., and C. J. Armour. 1951. Control the populations and habitat of the cinereous vulture of the European rabbit (Oryctolagus cuniculus) (Aegypius monachus), and he has studied diff erent an experiment to compare the effi ciency of gin ecological aspects of avian scavengers in Spain. trapping, ferreting and cyanide gassing. Annals A˗˝˘˗˒ Mˊ˛ːˊ˕˒ˍˊ got his Ph.D. degree of Applied Biology 38:464–474. in ecology and evolution at the University of Bern. Thorpe, J. 2012. 100 Years of fatalities and de- Currently, he is a Ramón y Cajal researcher in the stroyed civil aircraft due to bird strikes. Pro- Department of Animal Sci- ceedings of the 30th International Bird Strike ence (Division of Wildlife) Committee, IBSC 30/WP, Stavanger, Norway. at the University of Lleida (Spain) and associate se- Tragsatec. 2016. Diagnosis of the potential haz- nior scientist in the Division ard of soaring raptors on commercial aviation of Conservation Biology (Institute of Ecology and around the Adolfo Suárez-Madrid Barajas. Evolution) at the University Technical report for the Ministry of Agriculture, of Bern. His research inter- Food and Environment, Madrid, Spain. ests include conservation biology, behavioral ecology Vergara, P., J. I. Aguirre, and M. Fernández-Cruz. and ecological modeling, 2007. Arrival date, age and breeding success especially using the bearded vulture (Gypaetus barbatus) and other large raptors as study species. in white stork Ciconia ciconia. Journal of Avian Biology 38:573–579. Zuberogoitia, I., J. E. Martinez, A. Margalida, I. Gómez, A. Azkona, and J. A. Martinez. 2010. Reduced food availability induces behavioural changes in griff on vulture. Ornis Fennica 87:52–60. Zuberogoitia, I., J. A. González-Oreja, J. E. Martínez, J. Zabala, I. Gómez, and P. López-López. 2013. Foraging movements of Eurasian griff on vultures (Gyps fulvus): implications for supplementary feeding management. European Journal of Wild- life Research 59:421–429.
Associate Editor: Travis DeVault