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Vulture restaurants and their role in reducing diclofenac exposure in asian vulturesBird Conservation International (2007) 17:63–77. ß BirdLife International 2007doi: 10.1017/S0959270906000621 Printed in the United Kingdom Vulture restaurants and their role in reducingdiclofenac exposure in Asian vultures MARTIN GILBERT, RICHARD T. WATSON, SHAKEEL AHMED, MUHAMMADASIM and JEFF A. JOHNSON The provision of supplementary food at vulture restaurants is a well-established tool in theconservation of vulture species. Among their many applications, vulture restaurants are used toprovide a safe food source in areas where carcasses are commonly baited with poisons. Rapid andextensive declines of vultures in the Indian subcontinent have been attributed to the toxic effectsof diclofenac, a pharmaceutical used in the treatment of livestock, to which vultures are exposedwhile feeding on the carcasses of treated animals. A vulture restaurant was established at theOriental White-backed Vulture Gyps bengalensis colony at Toawala, in Punjab provincePakistan, to test the effectiveness of the technique in modifying ranging behaviour and mortalityat the colony. Six male vultures were fitted with satellite transmitters to describe variation inmovement and home-range during periods when safe food was alternately available andwithheld at the vulture restaurant. There was considerable variation in individual home-rangesize (minimum convex polygons, MCP, of 1,824 km2 to 68,930 km2), with birds occupyingsmaller home-ranges centred closer to the restaurant being more successful in locating thereliable source of food. Fixes showed that 3 of the tagged vultures fed at the vulture restaurantand the home-range of each bird declined following their initial visit, with a 23–59% reductionin MCP. Mean daily mortality during provisioning was 0.072 birds per day (8 birds in 111 days),compared with 0.387 birds per day (41 birds in 106 days) during non-provisioning controlperiods. Vultures tended to occupy greater home-ranges, cover greater distances each day andspend proportionately more time in the air during the late brooding and post-breeding seasons.
Attendance at the vulture restaurant also declined during this period with fewer birds visitingless often and no tagged vultures visiting the vulture restaurant at all. These findings indicatethat vulture restaurants can reduce, but not eliminate, vulture mortality through diclofenacexposure and represent a valuable interim measure in slowing vulture population decline locallyuntil diclofenac can be withdrawn from veterinary use.
The populations of three species of Gyps vulture in the Indian subcontinent have undergonerapid and extensive declines since the early 1990s (Prakash 1999, Gilbert et al. 2002, Prakash etal. 2003). As a result, the Oriental White-backed Vulture Gyps bengalensis, Long-billed VultureG. indicus and Slender-billed Vulture G. tenuirostris have been classified as CriticallyEndangered (IUCN 2004). Population declines have been associated with high rates of mortalityaffecting all age classes (Prakash 1999, Gilbert et al. 2002), with annual mortality estimatedbetween 22% and 50% (Green et al. 2004). Examinations of large numbers of dead vultures inPakistan found that acute renal failure, manifested as visceral gout, was the proximate cause ofdeath in 85% of adult and sub-adult birds and renal failure was due, ultimately, to the toxiceffects of diclofenac (Oaks et al. 2004). Diclofenac is a pharmaceutical used regionally to treat M. Gilbert et al.
inflammation and fever in livestock. Residues of diclofenac were found in all (n 5 25) field casesof visceral gout tested, whereas vultures dying from other causes were all negative for the drug(n 5 13). Subsequently, tissues collected from 14 vultures with visceral gout in India and Nepalbetween 2000 and 2004 were also shown to contain diclofenac residues (Shultz et al. 2004) and asimulation model has demonstrated that diclofenac is at least the primary, and possibly onlycause of the vulture decline across the region (Green et al. 2004). Removing diclofenac from theveterinary market in at least three countries will take time and, given the continued rapidpopulation decline, any measures that can reduce diclofenac exposure in the interim will be ofconsiderable benefit to Gyps vultures.
The provision of supplemental food at ‘vulture restaurants' is well established as a management tool in the conservation of vulture populations (Mundy et al. 1992). In its simplestform carcasses are provided in areas with insufficient food (Wilbur et al. 1974, Meretsky andMannan 1999) or where nutrient availability is considered inadequate (Richardson et al. 1986).
Supplementary feeding was shown to increase the survival of first year Cape Vultures Gypscoprotheres at Potberg in South Africa (Piper et al. 1999), has been employed during successfulreintroduction programmes (Sarrazin et al. 1994, Terrasse et al. 1994), and has facilitated therecolonization of abandoned breeding sites (Mundy et al. 1992). Vulture restaurants have beenused to provide alternative sources of uncontaminated food in areas where carcasses are baitedwith poison to control carnivore populations (Wilbur et al. 1974, Terrasse 1985, Johnson et al.
1998, Susic and Pavokovic 2003). However, the effectiveness of this approach remains largelyuntested, particularly in areas where food availability is high such as Pakistan's Punjab province.
This study aims to determine whether vulture restaurants are effective in reducing vulture exposure to diclofenac and subsequent mortality. The study measures mortality at a colonyduring breeding and non-breeding periods when supplementary food was alternately availableand withheld. Platform terminal transmitters (PTTs) were used to record the movement ofvultures with global positioning system (GPS) accuracy to determine whether food provisioningis able to modify home-range and foraging behaviour.
Methods and materials Punjab province is dominated by the Indus basin, a broad, flat alluvial floodplain formed by thefive major tributaries of the Indus River and ranges from 82 to 276 m in elevation (Figure 1).
Human and livestock densities are generally high with the fertile plains heavily cultivated withcotton, wheat, and mango orchards (Roberts 1991). The Thal Desert, bounded by the Indus,Chenab and Jhelum Rivers, is more sparsely populated and is dominated by tropical thorn forestand sand dunes (Roberts 1991). Mean winter temperatures can fall as low as 5.6uC in Januaryand rise to 42.3uC in June (Pakistan Meteorological Department, Lahore, unpubl.). Annualrainfall is mainly concentrated during the monsoon months (July–September).
The vulture colony studied at Toawala (30.50550u N, 71.68662u E) lies north-east of Multan and runs along the Shujabad Canal, roughly parallel to the Chenab River. Vultures nest in treesthat are unevenly distributed along a 42.5 km stretch of canal, with the majority of nestsconcentrated along 18.7 km at the eastern limit of the colony. The colony is occupied throughoutthe year, with highest numbers present during the breeding period from October to May. Themajority of eggs are laid in November, with hatching in late December and early January.
Juvenile vultures fledge between mid-March and May.
Vulture mortality From 1 to 26 November 2003 the vulture colony was surveyed for dead vultures along all or partof its length on 11 occasions. Daily surveys were conducted along the entire 42.5 km of colony
Vulture restaurants and diclofenac exposure in Asian vultures Figure 1. Map of the Punjab province, Pakistan and study area.
between 27 November 2003 and 30 June 2004. All vulture carcasses located were counted andthen removed or marked to prevent double-counting. Cause of death was determined bynecropsy examination on the majority of carcasses using the protocols outlined in Gilbert et al.
(2002). It was not possible to conduct necropsies on every dead bird, as some became tangled indead branches and could not be immediately recovered, and others were partially consumed byferal dogs soon after death.
Counts of vultures roosting in the colony were made at 24 to 86 day intervals from 28 August2003 to 22 June 2004 to measure colony size. All vultures observed along the 42.5 km colonywere counted (excluding nestlings). It was not practical to traverse the whole study area in asingle evening so vultures in the 18.7 km where nest density was greatest were counted within 2hours of sunset and remaining birds counted within 2 hours of sunrise the following day.
Food provisioning A supplementary feeding site (vulture restaurant) was established close to the densest area of theToawala colony (30.50802u N, 71.72487u E), 3.8 km from the harmonic mean centre (the pointwhere the inverse reciprocal mean distance to all active nests is a minimum) and 1.4 km from theclosest active nest. The site consisted of an open rectangular field (67 m 6 45 m) that was visible M. Gilbert et al.
from the nearest nesting trees and with no overhead wires or similar aerial obstacles for at least500 m. A 1 m high perimeter fence was erected around the field to exclude dogs and wasreinforced with Acacia spp. branches. There were few trees in the immediate vicinity of thevulture restaurant, so four perches were erected to discourage birds from perching on nearbyfarm houses. A concrete pool was built during early April to provide a reliable supply of waterduring the hot and dry summer months. All feed animals were locally purchased donkeys andthese were marked and held for a period of at least 1 week to ensure that any residues ofdiclofenac administered prior to purchase were eliminated from their tissues before slaughter.
Although no published studies have described the pharmacokinetics of diclofenac in equines,work in humans has shown that 90% of diclofenac administered at therapeutic doses iseliminated by 96 hours (Reiss et al. 1978 cited in Todd and Sorkin 1988).
The study was divided into four periods. Period A (27 November to 31 December 2003) and period C (9 February to 18 April 2004) were control periods when no food was offered. Carcasseswere provided to meet consumption during period B (1 January to 8 February 2004) and period D(19 April to 30 June 2004). Thus provisioning occurred during the first month of chick rearing,and during the fledging and post-fledging period. Carcasses were placed in the centre of thefeeding area within 1 hour of sunrise and the upper half of the carcass was skinned to facilitateaccess to soft tissues. Additional carcasses were provided throughout the day depending onconsumption to enable all birds to feed until satiated. Carcasses that remained untouched after 1day quickly became dry and unpalatable so remaining skin was removed to expose fresh tissues.
Fresh carcasses were provided at least every second day to ensure that there was a constantsupply of freshly exposed meat at all times. Carcasses were weighed prior to being placed in thefeeding area and the mass of all bones, hide and tissues removed at the end of each day weresubtracted to approximate the mass of tissue consumed. Long bones were crushed and scatteredaround the provisioning area.
Vulture movement from GPS-PTT tracking During November 2003, six Oriental White-backed Vultures were trapped while feeding atcarcasses , 1 km from the colony using an adapted version of the padded jaw trap (Day et al.
1980). Each vulture was fitted with a Microwave Telemetry, Inc. solar powered GPS-PTT unitweighing 73 g (1.2–1.9% body mass). Transmitters were mounted on the patagium using themethod described by Wallace et al. (1994) and incorporated a coloured vinyl patagial tag to aid inindividual identification in the field. Hereafter these birds are identified as Black, Blue, White,Orange, Green and Yellow. The GPS-PTT units were programmed to record 13 GPS fixes athourly intervals from 06h00 to 18h00 (local time), and download these data via satellite linkevery 24 hours.
All six vultures were in adult plumage when trapped and all birds were later determined to be male using molecular methods described by Ito et al. (2003). Their breeding status was assessedthrough observation of marked birds encountered opportunistically and by searching areaswhere vultures returned most frequently.
Vulture positions determined from GPS-PTT fixes were analysed using Ranges6 software v1.2to characterize the movement and space use of individual vultures during provisioning andcontrol periods (Kenward et al. 2003). A measure of daily movement distance was calculated forall days during which 10 or more fixes were obtained by summing the distances betweensuccessive fixes. Home-range area was calculated using minimum convex polygons (MCPs) thatcalculate the smallest polygon with external angles greater than 180u to include all fix locations(Kenward 2001). Tracking resolution was set at 20 m to take account of GPS tracking unitaccuracy. Estimates of home-range using MCP methods are very sensitive to outlier positions Vulture restaurants and diclofenac exposure in Asian vultures recorded during infrequent movements outside the ‘normal' area of activity (Kernohan et al.
2001). Such outlier positions have a disproportionate influence on MCP area; an effect thatincreases with time and complicates comparisons of MCP estimates made during periods ofunequal duration. To counter this, outlier positions were excluded using a peeled polygon coremethod excluding 0, 5% and 10% of positions furthest from the harmonic mean centre (thepoint where inverse reciprocal mean distance to all the other fixes is a minimum) to obtain100%, 95% and 90% peeled polygon cores. Autocorrelation or independence of fixes is animportant consideration when calculating home-range using conventional radio-telemetry(Kenward 2001). However, this is not considered to be a problem in the use of GPS-PTT units solong as positions are recorded at regular intervals during the animal's normal activity cycle, thusensuring unbiased temporal coverage of the animal's movements during the study period (Otisand White 1999).
Fixes and sensor readings obtained from the PTT units were used to determine the activity, location and, as far as possible, behaviour of tagged vultures. Positions recorded at 06h00 wherevultures were immobile (speed sensor reading of 0 km/h) were considered to indicate vulturesperched at roost sites. All recorded roost positions in Toawala colony were within 6 km of thevulture restaurant; thus this distance was used as an arbitrary cut-off differentiating fixes ‘closeto' (, 6 km) and ‘distant from' (. 6 km) the restaurant.
Speed fixes greater than 10 km/h were a reliable indication that a vulture was in flight (although soaring vultures were occasionally recorded at 0 km/h, presumably indicating a birdflying into a headwind or manoeuvring in a tight circle). Roost positions did not exceed 256 melevation above sea level for any vulture during the study period, and this was assumed to be themaximum altitude at which a vulture could be perched in the study area. Vultures wereconsidered to be flying for all fixes obtained at altitudes exceeding 256 m, or when speed wasgreater than 10 km/h at altitudes less than 256 m.
Food consumption and numbers of vultures at the vulture restaurant While no birds visited the vulture restaurant during periods A or C, vultures visited therestaurant on 28 (73.7%) of 38 days when clean food was provided during period B, a time whenvultures were feeding young nestlings. On the first day a single vulture landed within thefenced area but by the third day birds began arriving in significant numbers. It was not possibleto determine the number of birds feeding each day; however, daily maximum counts regularlyexceeded 100–200 birds with a highest count of 337 vultures on the ground on 15 January.
Substantial quantities of tissue were consumed during period B, requiring considerable effort to procure feed animals to keep pace with demand. A total of 111 carcasses (about 6,499 kg liveweight) were offered of which 86 were weighed both before and after vultures had fed.
Combined mass of these 86 carcasses was 5,035 kg from which 1,515 kg (30%) of hide, bones andunconsumed tissue were recovered, indicating that vultures consumed about 4,549 kg of the 111carcasses offered. However, an additional 18 naturally available livestock carcasses wereobserved in the vicinity of the vulture colony during the feeding period, at least seven ofwhich were attended by vultures. Therefore, the amount of provisioned food consumed at thevulture restaurant can not be assumed to have fed the entire colony exclusively throughout thisperiod.
The vulture restaurant was stocked for 73 days during period D in the post-fledging period.
Vultures fed on only 12 days (16.4% of days) and in smaller numbers than during period B withmore than 10 birds recorded on only seven occasions and more than 100 birds recorded only once(156 birds on 20 April). The number of carcasses and mass of food consumed was not recordedduring this period.
M. Gilbert et al.
Vulture mortality We collected 50 dead adult and sub-adult vultures during the study period. Visceral gout,indicative of renal failure possibly due to diclofenac poisoning (Oaks et al. 2004, Shultz et al.
2004), was found in 29 of 30 dead vultures that were available for necropsy. The single non-goutcase was an emaciated sub-adult that was excluded from further analyses. During provisioningperiod B (38 days) four dead adult vultures were collected of which three were necropsied andfound to have visceral gout. Three adults and a sub-adult vulture were located duringprovisioning period D (73 days) of which two were necropsied and both had gout.
Mean daily mortality during provisioning was 0.072 birds per day (8 birds in 111 days), compared with 0.387 birds per day (41 birds in 106 days) during non-provisioning controlperiods. Because the abundance of vultures in the colony varied dramatically between seasons,we compared mortality between provisioning and non-provisioning periods only within eachseason. Mortality in the non-provisioning control period A (25 birds in 35 days) wassignificantly higher than during provisioning period B (4 birds in 38 days, x21 5 17.1, P ,0.001). Likewise, mortality in the non-provisioning control period C (16 birds in 71 days) wassignificantly higher than during provisioning period D (4 birds in 73 days, x21 5 7.5, P 5 0.006).
Numbers of adult and sub-adult vultures roosting at the colony varied through the breedingseason, reaching a maximum count of 537 on 26 December 2003 when eggs were beginning tohatch, and declining thereafter to reach a low of 280 on 16 May 2004 after all the nestlings hadfledged (Figure 2).
Figure 2. Combined counts of roosting adult and sub-adult vultures at Toawala colony between28 August 2003 and 22 June 2004. Shaded areas indicate periods during which the vulturerestaurant was operational.
Vulture restaurants and diclofenac exposure in Asian vultures GPS-PTT performance Five of the six GPS-PTT units performed very well, with a mean number of daily fixes of 11.8for Blue (n 5 230 days, SD ¡ 1.65), 10.6 for White (n 5228 days, SD ¡ 3.08), 12.2 for Orange(n 5 229 days, SD ¡ 1.96), 11.6 for Green (n 5 215 days, SD ¡ 2.46) and 9.7 for Yellow (n 5215 days, SD ¡ 3.11). The units failed to obtain any GPS fixes on only 1 (Blue), 3 (Orange,Green), 8 (White) and 11 days (Yellow), corresponding to periods when cloud cover, rain or duststorms prevented the solar-powered units from charging sufficiently. Due to a hardwareproblem the unit attached to the Black bird did not charge effectively, and GPS locations werereceived for only 31 days following attachment. Because the location fixes for this bird areincomplete, its home-range and movement characteristics could not be reported.
Vulture movement and biology The home-ranges traversed by the Yellow and Orange vultures were considerably greater thanthose of Blue, White and Green, with MCPs calculated across the study period of 68,930 km2,40,324 km2, 4,625 km2, 1,824 km2 and 5,069 km2, respectively (Figure 3). The Yellow vulturemoved widely, circumnavigating the Thal Desert on nine occasions during the study period andranging up to 257 km from Toawala. This vulture utilized multiple roost-sites across the Punjabincluding several known extant or recently extinct Oriental White-backed Vulture colonies,roosting within 6 km of the restaurant on only 16.8% (n 5 196) nights where roost locationcould be established. In contrast, the Blue, White and Orange birds roosted within 6 km of the Figure 3. The home-range of satellite-tagged vultures during the study period, expressed usingthe minimum convex polygon (MCP) method.
M. Gilbert et al.
restaurant site on 79.3% (n 5 228), 88.0% (n 5 216) and 48.2% (n 5 224) nights respectively.
These birds ranged up to 102 km (Blue), 35 km (White) and 316 km (Orange) from the colony.
Only one of the tagged vultures showed breeding activity during the study period, with the Green vulture observed incubating in December in an atypically solitary nest 24 km north-westof Toawala. The movements of this bird suggest that the nest hatched in early January, but failedapproximately 2 weeks later. During the 53 days prior to the failure of this nest the Green birdoccupied a home-range of 3,014 km2 and moved up to 90 km from the nest-site.
Visits to the vulture restaurant, home-range, roost-site use, mean daily distance travelled and mean daily time in flight varied between individual vultures, during control and provisioningperiods, and as the breeding season progressed through the study period. The large number ofindependent variables potentially influencing vulture behaviour and the small number ofvultures tagged makes statistical analysis difficult. However, by comparing parameters betweensuccessive control and provisioning periods, A to B, and C to D, and looking for common patternsamong the individual vultures, we can describe the following behavioural effects of foodprovisioning on vulture ranging behaviour.
During provisioning period B, fixes placed four of the six GPS-PTT birds within 6 km of thevulture restaurant, three of which made visits before provisioning ceased on 8 February. Blueand White made their first visits to the vulture restaurant on the 3 January and had visited on 11and 20 days, respectively, by the end of the period 36 days later. Orange failed to locate therestaurant during the first 12 days of period B, roosting at a maximum distance of 74 km andpassing within 6 km of the vulture restaurant on two occasions. It made its first visit to thevulture restaurant on 13 January and was subsequently recorded there on 11 of the remaining 26days before provisioning was discontinued.
The PTT unit attached to Black ceased transmitting GPS fixes at 18h00 on 2 January, at which time this bird was roosting along a canal 16 km north of the vulture feeding site. However, theunit continued to transmit Argos positions for a further 20 days, providing a record of the bird'smovements until 22 January. Eight fixes (class 2 or 3) were received from the Black-tagged bird'stransmitter within 6 km of the vulture restaurant on 4 days from 19 January until it ceasedworking. This bird was not observed at the feeding site at any time, despite its proximity on atleast these 4 days.
The attendance of tagged vultures at the restaurant is given in Table 1. Vultures are estimated to feed every 2–4 days (Green et al. 2004). Tagged vultures were absent for more than 4 days ontwo (Blue), one (White) and two (Orange) occasions, suggesting that birds may occasionallyhave been feeding at carcasses outside the restaurant. No tagged vultures were recorded at therestaurant after 1 February, although vultures did feed at the restaurant on 2 of the remaining 6days during which food was available.
Food was available for 36 days following the first visit to the restaurant made by Blue and White, and 26 days for Orange. Home-range for each bird over an equivalent period prior to thelocation of the restaurant was used to compare MCPs when food was alternately withheld andavailable. The home-range of each bird declined following their discovery of the restaurant, witha 23–59% reduction in MCP of 291 to 119 km2 (White), 395 to 306 km2 (Blue) and 3,555 to1,996 km2 (Orange) (Table 2). Green and Yellow did not discover and visit the vulture restaurantat all during the 38 days of period B. Positions were available for Green and Yellow only after 29November, so home-ranges during the 32 day period prior to and following the start of feedingwere compared. Green's home-range decreased by 49% from 3,014 km2 in period A to 1,546 km2in period B, while Yellow's home-range increased by 6% from 22,075 to 23,396 km2 (Table 2).
Vultures were more likely to roost close to the vulture restaurant once they had located the predictable source of food. Prior to locating the restaurant Orange roosted within 6 km on 34 Vulture restaurants and diclofenac exposure in Asian vultures M. Gilbert et al.
Table 2. Vulture home-range (km2) expressed using the minimum convex polygon (MCP) method.
aMCP during a period equivalent to ‘‘b'' prior to the discovery of the vulture restaurant.
bMCP following initial discovery of the vulture restaurant to the end of 7 February when food waswithdrawn.
cMCP during the 32 days prior to and following the onset of feeding on 1 January.
(59%) of 58 nights where roost site was established, and Blue on 33 (66%) of 50 nights. Oncevultures were aware of the reliable source of food they roosted close to the vulture restaurantmore frequently, with Orange roosting within 6 km on 16 (70%) of 23 nights and Blue on 32(91%) of 35 nights. White remained highly faithful to the vulture restaurant throughout periodsA and B, roosting within 6 km on 44 (92%) of 48 nights before discovering the site and 27 (90%)of 30 nights afterwards.
Mean daily distance travelled by Blue, White and Orange declined significantly (t 5 4.19, P , 0.001, d.f. 5 154) once these birds located the vulture restaurant (Table 3). In contrast, meandaily distance moved by vultures not visiting the vulture restaurant (Yellow and Green) washigher during period B than A. Mean daily time in flight also decreased once birds discovered therestaurant (t 5 7.77, d.f. 5 2, P 5 0.016), whereas it increased for Yellow and Green from periodA to B (Table 3).
Vultures did not visit the vulture restaurant every day and continued to range and sometimes roost at distant locations. Orange roosted more than 6 km from the restaurant on at least sevenoccasions (n 5 20, roost-site could not be determined for six) during period B and ranged up to42.6 km. Blue and White roosted more than 6 km on three occasions (n 5 36), and ranged up to22.3 and 11.6 km, respectively. It was not possible to confirm whether vultures were feedingduring these forays; however, it was possible to differentiate perched fixes, when vultures mayhave been feeding using altitude (, 256 m) and speed sensors (, 10 km/h). If perched positionswithin 200 m of roost locations are excluded, then following the discovery of the vulturerestaurant perched fixes were obtained for Orange (14 fixes), Blue (19 fixes) and White (eightfixes) on 8, 11 and 6 days, respectively.
All five vultures with functional tags were recorded within 6 km of the vulture restaurant whilecarcasses were available during provisioning period D, with White, Orange, Blue and Yellowrecorded on 73, 61, 68 and 33 days, respectively, out of the 73 day period. Only a single fix wasobtained for Green within 6 km of the restaurant, when it passed within 3 km at an altitude of1,686 m on 15 June. Despite their proximity, none of the satellite-tagged vultures visited therestaurant during provisioning period D, suggesting a marked change in behaviour that wasunrelated to the availability of food at the vulture restaurant. Other independent variables thatobviously changed between periods B and D included the stage of the breeding season anddramatically increased ambient temperature.
The home-range of four of the tagged vultures was significantly greater during periods C and D than during A and B (Freidman test: S 5 9.24, d.f. 5 3 P 5 0.026; Table 2). The one exceptionto this trend was Green, the only tagged bird that attempted to breed, which ranged most widelyduring period A and showed little variation from period B onward.
Vulture restaurants and diclofenac exposure in Asian vultures Table 3. Mean daily distance moved, and mean daily number of airborne fixes received from satellite-taggedvultures for all calendar days during which 10 fixes or more were received (N), and all calendar days duringwhich at least 10 three-dimensional fixes were received (n).
Mean distance moved Mean airborne fixes ¡ ¡SD (min.–max.), n SD (min.–max.), n 19.3 ¡ 11.9 (2.4–61.1), 46 1.9 ¡ 1.5 (0–5), 46 12.8 ¡ 12.6 (1.5–58.9), 26 1.2 ¡ 1.2 (0–4), 27 30.8 ¡ 24.5 (2.7–86.8), 61 2.9 ¡ 2.0 (0–7), 59 41.4 ¡ 28.2 (6.9–161.6), 72 4.4 ¡ 1.5 (1–7), 73 13.1 ¡ 6.7 (2.4–29.7), 45 2.8 ¡ 1.5 (0–5), 45 11.9 ¡ 5.1 (5.1–26.7), 20 1.8 ¡ 1.1 (0–4), 20 25.5 ¡ 19.8 (0.2–75.4), 38 3.8 –¡ 1.9 (0–8), 38 23.0 ¡ 17.3 (0.8–78.3), 69 4.0 ¡ 1.6 (0–7), 66 23.9 ¡ 18.1 (2.1–81.3), 45 3.1 ¡ 1.5 (0–6), 45 23.5 ¡ 20.9 (1.6–79.8), 26 2.0 ¡ 1.6 (0–6), 26 45.3 ¡ 35.0 (0.3–175.0), 69 3.6 ¡ 2.1 (0–8), 69 45.9 ¡ 28.1 (0.7–156.8), 73 4.4 ¡ 2.0 (0–9), 73 12.0 ¡ 16.0 (0.1–48.0), 15 1.6 ¡ 1.8 (0–4), 14 22.5 ¡ 21.8 (0.1–68.6), 28 2.0 ¡ 1.7 (0–5), 26 41.9 ¡ 21.3 (3.7–88.2), 70 5.2 ¡ 1.8 (1–9), 70 48.3 ¡ 23.8 (4.8–128.3), 73 6.5 ¡ 1.8 (2–9), 73 29.1 ¡ 20.8 (1.7–95.6), 23 2.5 ¡ 1.3 (0–5), 23 52.5 ¡ 36.3 (1.3–11.8), 11 2.6 ¡ 1.9 (0–5), 12 71.3 ¡ 49.7 (0.4–178.9), 54 4.1 ¡ 2.1 (0–9), 52 72.7 ¡ 56.9 (0.1–226.3), 52 3.9 ¡ 2.1 (0–8), 50 Blue and White continued to roost in the vicinity of the vulture restaurant with 81% (n 5 69) and 76% (n 5 66) of identified roosts respectively within 6 km during period C and 78% (n 573) and 92% (n 5 73) during period D. Only 38% (n 5 71) of Orange's and 3% (n 5 69) ofYellow's roost positions were within 6 km of the vulture restaurant during period C and 33% (n5 73) and 35% (n 5 63), respectively, during period D. Green did not roost within 6 km of thevulture restaurant at any time.
The mean daily distance moved was greater for all birds during the latter half of the study (Table 3), and each bird spent proportionately more time in flight during periods C and D thanduring periods A and B (Table 3) with up to nine hourly fixes per day received from flyingvultures. This marked change in movement parameters again suggests that some otherindependent variable had a greater effect on movements in the latter half of the study periodthan food availability at the vulture restaurant.
This study has demonstrated that the provisioning of uncontaminated food at vulturerestaurants can reduce diclofenac-related mortality at a vulture colony. Mean daily mortalitywas shown to decline from 0.387 (41 vultures in 106 days) during control periods to 0.072 (8vultures in 111 days). These comparisons are complicated by fluctuating numbers of vulturespresent in the colony between and during provisioning and control periods. However, meandaily mortality of 0.105 during provisioning period B (4 vultures in 38 days) was less than halfthe 0.225 in period C (16 birds in 71 days) when vulture numbers remained approximatelystable. Furthermore, mean daily mortality was consistently lower during provisioning thancontrol periods, indicating that vulture restaurants are able to reduce vulture mortality rates, M. Gilbert et al.
irrespective of the number of birds in the colony.
The movements of tagged vultures indicated that the restaurant was also successful in modifying foraging behaviour, consistently reducing home-range, time in flight and mean dailydistance travelled once the predictable food source had been located. However, as all taggedvultures were male and only one attempted to breed, it is not possible to determine whetherthese birds were representative of the breeding population. To address this question it would benecessary to tag a much larger sample size, or collect data over a longer period – options that areboth cost-prohibitive. The possibilities exist, for example, that the presence of the GPS-PTT unitand patagial tag affected their breeding behaviour, or these birds may have been ‘floaters'(Newton 1979) that would not have bred anyway but were otherwise more susceptible to beingtrapped. Despite these limitations the PTT units were successful in describing a range of foragingpatterns and the modification of some of these by the vulture restaurant.
Even with the ready availability of uncontaminated carcasses during provisioning periods at least five dead vultures were found with visceral gout while the restaurant was operating.
Although visceral gout is a non-specific finding indicative of renal failure and may have manycauses, this remains significant in the context of vultures in South Asia. Analyses haveconfirmed that all 39 cases of visceral gout in Gyps vultures examined in Pakistan, India andNepal contained residues of diclofenac (Oaks et al. 2004, Shultz et al. 2004). Visceral gout wasfound in 39 (97%) of the vultures examined in this study, which strongly suggests thatdiclofenac was the most important cause of death, including at least five vultures that diedduring provisioning periods.
In Punjab province, high densities of livestock have led to a ready supply of carcasses for foraging vultures. Even when vulture attendance at the restaurant was highest, the predictablefood source was not sufficiently attractive to deter birds from utilizing carcasses encounteredelsewhere. During the provisioning periods vultures were observed at livestock carcasses close tothe restaurant site, indicating a continued, albeit lower risk of diclofenac exposure. Reasons forthis may include intra-specific competition at the restaurant encouraging vultures to feedelsewhere, or preference for a more varied diet than that available at the restaurant. This couldbe tested by providing food at multiple sites, increasing the numbers of individual carcasses ateach site and using a greater diversity of food species.
The restaurant was affected by seasonal variations in foraging behaviour, attracting few vultures and no tagged birds during the post-breeding period. At this time vultures spent anincreasing proportion of time in flight, covered greater distances and occupied larger home-ranges. Nutrient requirements will decrease following breeding (Houston 1976) andobservations of soaring vultures over the restaurant suggest that these movements were notentirely motivated by food. Diurnal temperatures regularly exceed 45uC during these months(Pakistan Meteorological Department, Lahore, unpubl.), and it is possible that thermoregulationmay supersede foraging as the primary motivation for soaring, contributing to the seasonaldisinterest in the restaurant.
The relative failure of the restaurant to attract vultures during the post-breeding period suggests that the provision of uncontaminated food was unrelated to the reduction in mean dailymortality at this time. There are several possible explanations that might explain this apparentparadox: 1. Seasonal variation in nutritional requirements may reduce feeding frequency and diclofenac encounter rates.
2. Seasonal variation in disease incidence or livestock management may lead to a reduction in 3. Seasonal variation in ranging patterns may lead to vultures dying far from the colony, masking true diclofenac exposure rates.
Each of these factors may contribute to some degree. The restaurant was most successful when energy demands were greatest, during the early nestling period (Houston 1976). Breedingsuccess at Toawala during 2004 was only 40% (Gilbert et al. unpubl. data), so by the Vulture restaurants and diclofenac exposure in Asian vultures post-breeding period a large proportion of birds were no longer provisioning offspring. Also,seasonal increases in home-range size may have reduced the proportion of dead birds that couldbe located during mortality surveys. Irrespective of the reasons, vulture restaurants contributelittle or nothing to reducing mortality during the hot months of the non-breeding period.
Individual variation in vulture ranging behaviour also greatly affected the restaurant's effectiveness in modifying foraging patterns. Although all vultures were trapped at Toawala, thehome-range of just three was centred in the colony and amenable to modification by the vulturerestaurant. The restaurant was unable to attract the only vulture that attempted to breed(Green), which nested at a distance of 27 km, or the bird that ranged widely utilizing multipleroost-sites across the province (Yellow). We can conclude that without the continualmaintenance of multiple, widely dispersed provisioning sites it will only ever be possible toreduce diclofenac contamination in a subset of the total population that normally ranges near therestaurant.
This study has demonstrated that during the cool winter breeding season it was possible to modify vulture foraging behaviour and reduce mortality by provisioning a vulture restaurantwith uncontaminated food. However, the restaurant was only able to modify the behaviour ofvultures with home-ranges centred close by. The restaurant did not attract vultures during thenon-breeding season when other factors, such as high ambient temperatures, may influencesoaring behaviour and movement over large areas in which food was abundant and exposure todiclofenac-contaminated carcasses could occur. Even under optimum conditions it is not possibleto eliminate diclofenac exposure entirely where alternative carcass sources are readily available.
Supplementary feeding may prove to be a useful management tool for slowing declines locally inthe short term. However, extinction is inevitable in all populations foraging in areas wherediclofenac is in veterinary use and treated carcasses become vulture food at sufficient frequencyto cause deaths and negative population growth. Elimination of diclofenac in veterinary use isthe most certain way to prevent vulture deaths from diclofenac exposure, although education ofveterinarians and livestock owners to avoid treatment of terminally ill livestock, or to bury orburn carcasses of recently treated livestock, may also be helpful.
The Peregrine Fund's Asian Vulture Crisis Project was supported by the Gordon and BettyMoore Foundation, The Peregrine Fund, Disney Wildlife Conservation Fund, Zoological Societyof San Diego, UN Foundation, Summit and Ivorybill Foundations, and other important donors.
We would like to thank the following individuals and organizations for their partnership, helpand co-operation: the Ornithological Society of Pakistan (OSP), Nature Conservation Pakistan,Faisal Farid, Brigadier Mukhtar Ahmed, Punjab Department of Wildlife and Parks, NationalCouncil for the Conservation of Wildlife (NCCW), Bahauddin Zakariya University Multan,WWF-Pakistan, Zoological Society of San Diego, Washington State University, and Universityof Michigan.
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MARTIN GILBERT*, RICHARD T. WATSON, SHAKEEL AHMED, MUHAMMAD ASIMThe Peregrine Fund, 5668 West Flying Hawk Lane Boise, ID 83709, USA.
The Peregrine Fund, 5668 West Flying Hawk Lane, Boise, ID 83709, USA, and University of Michigan Museum of Zoology, 1109 Geddes Avenue, Ann Arbor, MI 48109, USA.
*Author for correspondence. Current address: Wildlife Conservation Society, 2300 Southern Boulevard, Bronx, NY 10460, USA; e-mail: email@example.com Received 7 June 2005; revision accepted 2 April 2006
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