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Reduced Food Availability Induces Behavioural Changes in Griffon Vulture Gyps Fulvus

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Reduced Food Availability Induces Behavioural Changes in Griffon Vulture Gyps Fulvus Ornis Fennica 87:00–00. 2010 Reduced food availability induces behavioural changes in Griffon Vulture Gyps fulvus Iñigo Zuberogoitia, José E. Martínez, Antoni Margalida, Imanol Gómez, Ainara Azkona & José Antonio Martínez I. Zuberogoitia, 1-Estudios Medioambientales Icarus S.L. Pintor Sorolla 6, 1° C., E- 26007 Logroño, Spain. E-mail [email protected] J.E. Martínez, Bonelli’s Eagle Study and Conservation Group. Plaza de Toledo, 10-5E, E-30009 Murcia, Spain A. Margalida, Bearded Vulture Study and Protection Group, Apdo. 43, E-25520 El Pont de Suert, Lleida, Spain I. Gómez & A. Azkona, Sociedad para el Estudio de las Aves Rapaces (SEAR). C/ Kart Marx, 15, 4° F., 48950 Erandio, Bizkaia, Spain J.A. Martínez, Juan de la Cierva 43, El Campello, E-03560 Alicante, Spain Received 12 august 2009, accepted 17 November 2009 In natural conditions, Griffon Vultures typically show shy behaviour and escape by flying if approached by humans. According to the state-dependent foraging theory, Griffon Vul- tures should modify their foraging behaviour depending on food availability and preda- tion risk, humans being the main potential predator. We tested the Reaction Time (RT) and Flight Initiation Distance (FID) in five different artificial feeding schemes over three years in which food availability in the field varied significantly. The first scenario was set in a so-called “vulture restaurant”, in which government employees feed vultures that may exhibit tame behaviour and stay within a few meters from a feeding person. Scenario 2 involved similar conditions, but here the researchers not employees placed the food in the vulture restaurant. The vultures did not land at the restaurant until one day had passed, and they flew away when people approached them within 250 m. The third scenario was established in a local zoo several months after the closure of the vulture restaurant. Here, employees fed captive vultures that were often accompanied by wild birds that landed to take food. The RT was 14.2 min and the FID was 50 m. The fourth scenario was estab- lished during the subsequent breeding season in a mountain where vultures were fed by the authors of the present study. The RT was 2.8 min and the FID was 15.2 m. The fifth scenario was established in another mountain after the breeding season. Now, the RT was 19.2 min and the FID was 52.2 m. These results demonstrate the ability of vultures to eval- uate the predation risk depending on food availability and their state of hunger, and their ability to modify their behaviour from “natural” caution (”shyness”) towards a more toler- ant (”fearless”) behaviour. 2 ORNIS FENNICA Vol. 87, 2010 1. Introduction ture Cathartes aura also live in cities, but this is not true for European vultures that have suffered Foraging occupies a substantial amount of the from human persecution for centuries (Donázar daily time budget of every animal species. In such 1993). In Spain, for example, Griffon Vultures cases, for a foraging animal, the optimal behaviour Gyps fulvus were killed as pests until 1966 after may vary both with the quality of the foraging which they have been protected by law (Donázar patch and with the internal state of an individual 1993). Nonetheless, farmers, shepherds and hunt- (McNamara & Houston 1986). This variation ers continued to poison and directly persecute vul- leads to a trade-off between energy gains and pre- tures until recently (Olea et al. 1999, Hernández & dation risk (Olsson et al. 2002). Individuals tend to Margalida 2008, Margalida et al. 2008, Hernández reduce the risk of predation by altering their be- & Margalida 2009). This activity has decreased haviour (Houston & McNamara 1989). However, since the banning of poison use in 1984, after food limitations may force animals to evaluate the which the Spanish population has been recovering trade-offs between predation risk and fitness, and increasing (Parra & Tellería 2004). From the which may depend on their future expectations 1980’s to the 1990’s, the Griffon Vulture popula- (i.e., breeding success and survival; Olsson et al. tion and distribution has rapidly increased, largely 2002). thanks to feeding them at feeding stations (artifi- Animals may start behaving tamely or show cial “vulture restaurants”) and to the active protec- habituation in the absence of predators (Blumstein tion of vulture breeding areas (Del Moral & Marti et al. 2004) when, for example, no aggressive in- 2001). ter-specific interactions occur for long periods of Food is a limited resource for birds, affecting time (Coleman et al. 2008). On remote islands, survival, breeding and behaviour (Lack 1954, wild animal species may not fear humans or terres- Newton 1998). The behavioural reaction to varia- trial predators because they have often not experi- tion in food supply has been documented for sev- enced negative impacts that would normally lead eral bird species (Poulin et al. 1992, Brown & them to become alert and escape from a threaten- Sherry 2006, Robb et al. 2008) and is related to ing situation (Rödl et al. 2007). Such behavioural predation risk (Olsson et al. 2002). However, until pattern is problematic for native animals that do now few studies have assessed vulture behaviour not recognize threats from introduced predators in relation to food availability. Due to sanitary re- (Massaro et al. 2008), and it also makes it difficult strictions, vulture conservation in Europe is pres- for individuals to adapt their behaviour to new ently conditioned by supplementary feeding activ- threats (Blumstein et al. 2004). In areas with in- ities (Donázar et al. 2009a, b). Little is known, creasing human use, some species have adapted however, if these activities lead to behavioural their behaviour to obtain the benefits of living changes in vultures, which could in turn be rele- close to humans, their behavioural flexibility hav- vant to vulture conservation. ing been conditioned by a favourable situation in The present study was done in an area where which humans do not show or show only little an- Griffon Vultures do not depend on feeding sta- tagonistic behaviour. Such adaptations are obvi- tions, and where extensively raised livestock pro- ous in urban areas, with pigeon Columba species, vide the biomass required to ensure the survival of gull Larus species, rats (e.g., Rattus norvegicus), the local population. The systematic removal of sparrow Passer species and crow Corvus species livestock from the mountains and the closing of serving as good examples. Some birds of prey vulture feeding stations in neighbouring provinces have adapted to living close to humans by using have caused the local population to decline, with a buildings to nest (Cade & Burnham 2003, Ellis et simultaneous decrease in breeding parameters al. 2009) and by hunting in gardens, orchards, (Zuberogoitia et al. 2009). Moreover, mortality parks and even streets (Van Nieuwenhuyse et al. due to starvation has become increasingly com- 2008). Some evasive raptors, such as the Goshawk mon in recently fledged birds of some vulture col- Accipiter gentilis, tolerate human activities in cit- onies. Another sign of food shortage is the recent ies (Kenward 2006). New World vulture species increase in formal complaints about vultures at- Black Vulture Coragyps atratus and Turkey Vul- tacking live livestock (Margalida & Campión Zuberogoitia et al.: Behavioural changes in Griffon Vulture 3 Fig. 1. Study area. Colonies of Griffon Vulture (black asterisks) around sites applied for the five scenarios (full circles; see text), and around sites applied for other scenarios during the breeding sea- son of 2008 (hollow circles). 2009). The only existing feeding station in the from the moment food is made available by hu- study area was closed in 2006. Simultaneously, a mans to the moment it is detected by vultures, i.e., policy involving greater control of dead livestock until the first vulture lands to feed; and (2) the in the field was initiated. Flight Initiation Distance (FID), measured as the These changes in food availability due to bo- distance at which feeding vultures allow humans vine spongiform encephalopathy (Donázar et al. to approach them without escaping by flight. We 2009a, b, Zuberogoitia et al. 2009) enabled us to suggest that vultures would adopt a “tame” or develop a behavioural experiment, in which the “fearless” behaviour related to the amount of main hypothesis was as follows: according to the available food. state-dependent foraging theory, the Griffon Vul- ture, a long-lived species that has long survived human persecution, will change its feeding behav- 2. Material and methods iour to maintain high physical fitness according to an artificial feeding programme, i.e., the establish- 2.1. Study area and design ment of feeding stations. Our main goal is to assess the relationship between food availability and for- The study was done west of Biscay, northern aging behaviour of Griffon Vultures by analyzing Spain, between 43°10’and 43°27’N and 3°27’and (1) the Reaction Time (RT), which is the time lag 2°31’W (Fig. 1). The study area is hilly and den- 4 ORNIS FENNICA Vol. 87, 2010 sely populated, with extensive industrial and other tion Time (RT), considered as being the time be- urban areas. More than 50% of the area is allocated tween one vulture flying above a carrion within a 5 to forestry at the expense of traditional small-scale km radius and the first vulture landing, and Flight farming, and the traditional patchwork of wood- Initiation Distance (FID), measured as the distance land, pasture and small holdings has been greatly at which feeding vultures allowed humans to ap- reduced. proach without taking off. In 1986 a “vulture restaurant”, a vulture feed- Scenario 1: Predictable food source in a food- ing station regulated by the local government, was rich environment and habituation to humans.
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