Home range and habitat selection of captive-bred and rehabilitated cape vultures Gyps coprotheres in southern Africa
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Home range and habitat selection of captive-bred and
rehabilitated cape vultures Gyps coprotheres in
southern Africa
BEN JOBSON, KERRI WOLTER, LARA JORDAN
A R A M O N A D J E M and J . M A R C U S R O W C L I F F E
Abstract Following the continual decline of the Cape Introduction
vulture Gyps coprotheres since the s, captive breeding
and rehabilitation programmes have been established to
reinforce populations across southern Africa. This study ex- T he African vulture crisis has seen Gyps species follow-
ing global trends of declines caused by a combination
of threats, including persecution, reduced food availability,
amines the spatial ecology of captive-bred and rehabilitated
vultures following release. Our analysis used , GPS poisoning and electrocution on powerlines (Ogada et al.,
fixes from captive-bred and rehabilitated birds to , ). The Cape vulture Gyps coprotheres is categorized
calculate home range sizes using kernel density estimation. as Endangered on the IUCN Red List (BirdLife International,
We found that home range size did not differ significantly ) and its life history strategy, characterized by long gener-
between captive-bred and rehabilitated birds. The location ation times (Mundy et al., ), makes colonies susceptible
of home ranges differed: captive-bred birds showed greater to declines (Piper et al., ).
site fidelity, remaining close to their release site, whereas Vultures provide significant ecosystem services, including
rehabilitated birds dispersed more widely across the species’ the removal of carcasses, nutrient recycling and reducing the
native range. By remaining close to their release site within a transmission of diseases (Markandya et al., ; Ogada et al.,
protected area, captive-bred birds had a significantly high- ; López-López et al., ). Declines in vulture populations
er per cent of their GPS fixes within protected areas than can be self-reinforcing through the Allee effect, as popula-
did rehabilitated birds. Despite fidelity to their release site, tions rely on social information to enhance foraging efficiency
captive-bred birds demonstrated innate capabilities for nat- (Jackson et al., ). Reinforcement of populations at declin-
ural foraging behaviours and the same habitat selection ing colonies is preferable to full reintroduction projects and
strategy as rehabilitated individuals. These findings suggest this is particularly pertinent for vultures, as Allee effects are
that captive breeding and reinforcement of populations likely to limit the effectiveness of re-establishment efforts
at declining colonies could provide localized benefits. Fu- and the persistence of small colonies (Le Gouar et al., ;
ture long-term studies should seek to analyse survivorship Armstrong & Wittmer, ).
and identify the breeding behaviour of these captive-bred Rehabilitation is an often practiced but poorly moni-
birds once they reach sexual maturity. tored intervention for raptors (Monadjem et al., ),
which may enhance population growth during early stages
Keywords Cape vulture, dispersal, Endangered, Gyps of species recovery (Steven et al., ). For example, release
coprotheres, kernel density, protected areas, southern of rehabilitated Cape vultures can buffer the effects of col-
Africa, spatial ecology ony declines, as long as the proportion of rehabilitated
birds in the population does not exceed % (Monadjem
et al., ). Captive-bred Gyps vultures have been success-
fully reintroduced in Europe (Sarrazin et al., ).
Here we examine, for the first time, the movement ecol-
BEN JOBSON* (Corresponding author, orcid.org/0000-0001-6131-1476) ogy of captive-bred and rehabilitated Cape vultures, and
Imperial College London, Silwood Park, Berkshire, SL5 7PY, UK compare this with available data for wild birds (Bamford
E-mail ben.jobson@birdlife.org
et al., ; Phipps et al., ; Pfeiffer et al., ; Kane
KERRI WOLTER and LARA JORDAN VulPro, Rietfontein, Hartbeespoort Dam, North
West Province, South Africa
et al., ). Comparisons between captive-bred and reha-
bilitated groups are apt, as both groups could develop be-
ARA MONADJEM Department of Biological Sciences, University of Eswatini,
Kwaluseni, Eswatini, and Department of Zoology and Entomology, Mammal havioural aberrations during their time in anthropogenic
Research Institute, University of Pretoria, Pretoria, South Africa care that cause them to differ from their wild counterparts.
J. MARCUS ROWCLIFFE Zoological Society of London, Institute of Zoology, Juvenile dispersal presents a challenge for translocations
London, UK as dispersing vultures may leave colonies targeted for re-
*Present address: BirdLife International, The David Attenborough Building,
Pembroke Street, Cambridge, CB2 3QZ, UK inforcement. We aim to provide insight into the preliminary
Received December . Revision requested February . stages of the post-release spatial ecology of translocated
Accepted June . First published online September . Cape vultures, and to identify any similarities and
This is an Open Access article, distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives licence (http://creativecommons.org/licenses/by-nc-nd/4.0/),
which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is unaltered and is properly cited. The written permission of Cambridge
Downloaded from University Press must be obtained for commercial
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Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
https://doi.org/10.1017/S0030605319000814608 B. Jobson et al.
differences in home range size, patterns of habitat selection
and protected area usage between captive-bred and rehabi-
litated individuals. We predict that there are no differences
between the two groups, as they are expected to exhibit the
same innate patterns of spatial ecology.
Species and study area
Juvenile Cape vultures are known to disperse far from their
natal colony and forage in home ranges an order of magni-
tude greater than those of adults, which demonstrate colony
fidelity (Bamford et al., ). All individuals in this study
were released in the core of their distribution along the
Magaliesberg Mountain range at Nooitgedacht colony in
Gauteng and North West Provinces, South Africa (Fig. ). This
ridgeline, at , m altitude, is protected under UNESCO’s FIG. 1 The locations of Cape vulture Gyps coprotheres GPS fixes,
World Biosphere Reserve Programme and straddles the their release site, protected areas, and the IUCN Red List range
boundary between the Bushveld vegetation to the north and of the species (BirdLife, ).
Highveld grasslands to the south. This region holds two breed-
ing cliffs (Nooitgedacht and Skeerpoort) and previously
held the now extinct colony at Robert’s Farm (Wolter et al., ). Five individuals (two captive-bred and three rehabili-
). tated birds) did not produce asymptotic outputs from this
analysis and were excluded from the study. A two-tailed
Mann–Whitney test was used to compare the number of
Methods
GPS points for captive-bred and rehabilitated vultures be-
fore they achieved home range stabilization. We carried
Data collection
out home range estimation using R .. (R Core Team,
We analysed the movements of captive-bred and ) and the R package adehabitat (Calenge, ). We
rehabilitated Cape vultures, of all age classes. Rehabilitated used kernel density estimation to calculate the and %
vultures were wild birds that had sustained treatable contours for overall and core home ranges, respectively.
ailments, such as fractures or emaciation, and originated For smoothing of contours, we selected the default reference
from across northern South Africa (Naidoo et al., ). Age bandwidth as this is robust against potential outliers in
classes were fledgling (– months), juvenile ( months– large data sets (Hemson et al., ). We used generalized
years), immature (– years), subadult (– years) and linear models (GLMs) to examine whether overall and
adult (. years) (Piper et al., ). Vultures were fitted with core home range are a function of vulture group (rehabili-
GPS-Global System for Mobile Communications trackers, tated or captive-bred), age, injury, sex and time spent in
attached with a Teflon backpack-style harness within plastic rehabilitation. We log transformed home range size to
tubing, to reduce potential friction (Wolter et al., ). remove a pronounced skew. To identify any differences in
Before release, birds were subject to a variable period of the propensity of study birds to disperse long distances we
acclimation (, months) within a predator-proof enclosure compared correlates of dispersal distance. We examined
at the release site. We collated tracking data that were logged mean Euclidean dispersal distance between individuals by
during – from devices transmitting at a minimum comparing the distance from the release site to the centroid
rate of once every hours and a maximum of every minutes. of each bird’s home range with a two-tailed Mann–Whitney
Birds were tracked for a mean duration of ± SE days. test.
We standardized data by selecting three random points to
retain per tracking day, to account for varying transmission
rates and minimize spatial autocorrelation. Habitat selection
Habitat selection can be classified into three levels: first
Home range analysis order selection identifies a geographical range for a species,
second order selection ascertains its home range formation,
We initially calculated the asymptote of home range size and third order selection describes an individual’s use of
to determine whether home ranges of birds were still ex- habitat within the home range (Johnson et al., ). We
panding at the time of this study (Steiniger & Hunter, analysed second order habitat selection type by comparing
Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
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https://doi.org/10.1017/S0030605319000814Cape vultures in southern Africa 609
relative numbers of individual vulture GPS fixes in each equivalent number of GPS fixes to those recorded and ran-
habitat with the proportion of that habitat in the study area domly distributed them across its range (% local convex
(Manly et al., ). Locations were overlaid onto a m hull polygon). We then compared the per cent of actual
resolution land cover raster file that included the following GPS fixes falling within protected areas (observed visitation)
biome categories: aquatic vegetation/flooded land, bare with the percentage of randomly generated fixes within pro-
ground, cropland, grassland, vegetation dominated by lichen tected areas for each individual (expected visitation). We used
and mosses, open water, shrubland, trees and urban (ESA the χ test to determine whether there was any significant
CCI, ). Values pertaining to the nine categories were deviation between observed and expected points. Subsequent-
extracted from each location and compared to a layer of ly, we compared levels of protected area visitation between
randomly generated points. Only cropland, grassland, captive-bred and rehabilitated vulture groups, with a t test.
shrubland and trees were analysed with a generalized linear
mixed model (GLMM), as the other five habitats had
considerably lower levels of visitation by all vultures (Fig. ). Results
We used the GLMM to examine whether habitat selection
is a function of vulture group, sex, injury, age, time spent Home range
in rehabilitation (set as fixed variables), and each bird’s
We analysed , GPS fixes, revealing that vultures nav-
unique identifier (as a random variable), fitted to a Poisson
igated across eight southern African countries and estab-
distribution, with the lme package in R (Bates et al., ).
lished home ranges that spanned six orders of magnitude
We projected GPS location data into Universal Transverse
from , km to ,, km (mean , ± SE ,
Mercator Zone S using QGIS .. (QGIS Development
km). One rehabilitated bird traversed seven countries and
Team, ). We then overlaid all vulture GPS fixes on pro-
thereby substantially increased the known distance travelled
tected areas across southern Africa (IUCN & UNEP-WCMC,
by an individual Cape vulture. Mean home range size differed
). We used the intersection tool in QGIS to calculate
between captive-bred (mean , ± SE , km) and
protected areas available to the vultures as the intersection
rehabilitated birds (mean , ± SE , km; Table ).
between a % local convex hull polygon for each bird and
However, the GLM showed that the estimates of kernel
the protected area shapefile. For each bird, we generated an
density utilization for the overall (%) and core (%)
home ranges were not significantly different between
groups. The estimated home range size of rehabilitated and
captive-bred birds were similar to that of wild Cape vultures,
although estimates for captive-bred birds were closer to the
smaller home range estimates for wild adult birds (Table ).
Core home range was closer to the release site for captive-
bred than for rehabilitated vultures. The Mann–Whitney
test showed greater linear dispersal of rehabilitated
birds from their release site (mean . ± SE . km)
than by captive-bred birds (mean . ± SE . km;
Z = –., P = ..) Additionally, there were no signifi-
cant effects of age, sex, or time spent in rehabilitation on
home range size.
Habitat selection
Our analysis showed that captive-bred and rehabilitated
Cape vultures selected the same habitat types across the
landscape and the GLMM confirmed there were no statis-
tical differences between the groups. Both groups showed
positive selection, when compared with random points,
for cropland and shrubland, but visited grassland and
FIG. 2 Box plots of the per cent of GPS fixes in each habitat for
individual (a) captive-bred and (b) rehabilitated Cape vultures trees less than expected (Fig. ). Additionally, the GLMM
observed (O) and expected (E) habitat use for the four most used did not show any significant effects of sex, injury,
habitats (crop, grass, shrub and tree). Expected habitat use was age or time spent in rehabilitation on habitat selection.
calculated from the same number of locations randomly The χ test showed that observed visitation of protected
generated, to simulate non-selective foraging. areas was significantly higher than expected for all birds
Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
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https://doi.org/10.1017/S0030605319000814610 B. Jobson et al.
TABLE 1 Details of the captive-bred and rehabilitated Cape vultures Gyps coprotheres, with sex and type of injury, overall and core
home ranges ( and % kernel density estimates, respectively) and the total number of fixes and standardized fixes (after taking only
three points per bird, per day).
Home range (km2) Total no. Total no. of
ID Sex1 Injury 95% 50% of fixes standardized fixes
Captive-bred
CV1 F None 4.75 ,1 10,347 513
CV2 M None 4.02 ,1 4,623 87
CV3 F None ,1 ,1 14,922 1,134
CV4 F None 2.41 ,1 29,143 369
CV5 F None 6,635 897 11,629 516
CV6 F None 101,473 13,688 3,546 138
CV7 M None ,1 ,1 1,012 438
CV8 M None 273,569 77,502 9,291 459
CV9 M None 36,259 5,176 1,049 57
CV10 M None ,1 ,1 1,973 762
CV11 M None 5,386 817 6,465 177
CV12 F None 270,962 41,052 32,461 660
CV13 M None 4.84 ,1 13,977 270
CV14 F None 12,782 2,678 1,722 96
CV15 M None 507 82 2,033 459
CV16 M None 102,189 23,678 9,246 701
CV17 F None 3,858 637 1,174 135
CV18 M None 44,833 12,643 934 115
CV19 M None 230 37 708 81
CV20 F None 373,876 87,610 554 102
Mean ± SE 61,629 ± 24,942 13,323 ± 5,795
Rehabilitated
RH1 F Emaciated 2,022,465 455,844 8,372 3,109
RH2 M Bee stings 470 74 993 120
RH3 M Leg fracture 201,791 36,044 35,741 435
RH4 F Emaciated 3,155 515 6,287 141
RH5 M Emaciated 4,297 425 7,311 222
RH6 F Wing fracture 215,045 42,189 2,419 408
RH7 F Burn 812,755 219,342 2,895 303
RH8 F Emaciated 36,709 4,592 8,978 1,026
RH9 F Emaciated 282,229 66,849 2,052 206
RH10 F Emaciated 3 ,1 1,967 99
RH11 F Emaciated 95,238 15,675 7,688 684
RH12 F Wing fracture 248,647 54,390 10,932 714
RH13 F Unknown 217,820 49,096 1,227 123
Mean ± SE 318,510 ± 154,390 72,695 ± 35,841
F, female; M, male.
TABLE 2 Home range size of immature and adult Cape vultures Discussion
estimated in four previous studies.
Immatures (km2) Adults (km2) Source Our analysis of GPS tracking data for Cape vultures re-
leased from a captive breeding and rehabilitation centre sup-
482,276 21,320 Bamford et al. (2007)
492,300 121,655 Phipps et al. (2013) ported our prediction that the two groups had similar home
295,379 110,181 Kane et al. (2016) range sizes and habitat selection. However, comparison
287,199 Martens et al. (2018) with entirely wild birds is required, to examine whether
captive-bred and rehabilitated birds can integrate fully
(χ = ,., df = , P = , .). Captive-bred vultures had with the wild population. The main difference between
a higher per cent of GPS fixes within protected areas (mean captive-bred and rehabilitated vultures was the reduced
. ± SE .%) than rehabilitated vultures (mean . ± level of dispersal from the release site by captive-bred vul-
SE .%; t = ., P = .). tures, possibly the result of supplementary feeding near
Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
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https://doi.org/10.1017/S0030605319000814Cape vultures in southern Africa 611
the release site. In the wild, vultures have not been shown to The expectation that there would be equal usage of
alter their foraging behaviour as a result of the presence of protected areas between the two groups of vultures was
these so-called vulture restaurants but there may be an not met, with captive-bred birds visiting protected areas
effect on captive-bred birds that have experienced food more than rehabilitated birds. However, both groups visited
provisioning throughout their lives (Kane et al., ). protected areas significantly more than predicted based on
Predictability of food availability is an important factor random movement (Phipps et al., ). The apparent
in shaping the home ranges of other vulture species and preference for protected areas may be explained by our
could play a role in the behaviour of released Cape vultures release site being situated within a protected area and
(López-López et al., ). Food and water provisioning in the presence of consistent supplementary feeding. Addi-
protected areas, as well as the continual mitigation of threats tionally, by releasing captive-bred birds within protect-
across the species distribution, are likely to provide signifi- ed areas, it is likely they will form home ranges closer to
cant benefits to both rehabilitated and captive-bred birds. these locations and receive the protection conferred by
Because captive-bred birds have home ranges closer to the these sites.
release site, their scavenging ecosystem service will probably The inherent nomadism of vultures and the ranging
be reduced in other parts of their range. An important capabilities highlighted in this study provide support for the
question arising from our study is whether captive-bred ongoing prioritization of vulture conservation across southern
birds are likely to settle at distant colonies: this would Africa. That captive-bred vultures maintain innate capabilities
have implications for gene flow and heterozygosity. As to range in a way that is largely indistinguishable from that of
our study indicates that captive-bred Cape vultures may formerly wild rehabilitated birds supports continued captive
be less likely to disperse from their release site, it is breeding. Future long-term studies should seek to analyse sur-
important to continue analyses of these birds as they vivorship and identify the breeding behaviour of captive-bred
age and, ideally, to refit them with new GPS devices when birds once they reach sexual maturity.
the current ones stop transmitting, to obtain additional
longitudinal data. Acknowledgements We acknowledge the following VulPro
sponsors who contributed to rehabilitation, breeding, feeding, vet-
The size of Cape vulture home ranges in this study was erinary care, research and monitoring of the birds in this study,
more variable than reported in studies of wild birds (Phipps and provided financial support: Bayer SA, Banham Zoo, Birming-
et al., ; Pfeiffer et al., ; Kane et al., ). There ham Zoo (Alabama), Blair Drummond Safari Park, Boehringer-
were a few unusually small home ranges, which resulted Ingelheim, Boikarabelo Coal Mine, Cellular Tracking Technologies,
from some birds feeding regularly at the vulture restaurant, Chicago Board of Trade Endangered Species Fund, Cheyenne
Mountain Zoo, Cleveland Metroparks Zoo and Cleveland Zoological
remaining near the release site and roosting on the enclo-
Society, Columbus Zoo, Colchester Zoo, Dallas Zoo, DHL Supply
sures of the captive-breeding colony. An additional question Chain, Gauntlet Conservation Trust, GH Braak Trust, Hans
arising from our study is whether these captive-bred birds Hoheisen Charitable Trust, International Centre for Birds of Prey,
have the behavioural flexibility to learn from conspecifics, Jacksonville Zoo and Gardens, Lomas Wildlife Protection Trust,
and hence extend their home ranges over time. We did not LUSH Cosmetics, Martin Moore of the Moore Foundation, Max-
Planck-Gesellschaft, Monte Casino Bird Gardens, Natural Encounters
detect a difference between adult and juvenile home ranges,
Inc., Prince Bernhard Nature Fund, Rand Merchant Bank, Riverbanks
something other studies have identified (Bamford et al., ; Zoo and Garden, Rudi Wolter with Copper Sunset Sands Pty. Ltd,
Phipps et al., ; Krüger et al., ). However, the rela- Sacramento Zoo, The Hawking Centre UK, The Tusk Trust,
tively small sample sizes, especially within the rehabilitated SW Living Creatures Trust, ZKTeco and Zoo Atlanta–Reeder Con-
group, may have precluded determination of a clear effect servation Fund. We thank Ewan Flintham for his support.
of age.
Author contributions Study design and review: all authors; GPS
Rehabilitated birds may have individual differences in tracking and fieldwork: BJ, KW, LJ; data analysis and writing: BJ;
personality that originally caused them to sustain injuries revision: all authors.
and likewise influenced their spatial ecology. Individual vari-
ability in spatial ecology has been identified in raptors, and Conflicts of interest None.
although we controlled for individuality within the GLMM,
Ethical standards Research was approved by Imperial College
the rehabilitated study group may have comprised birds Research Ethics Committee and permits issued by Gauteng covered
prone to injury as a result of their personalities (Campioni the keeping (002619) and transportation (02889) of vultures, and
et al., ). Our habitat selection analyses suggest that for- otherwise abided by the Oryx guidelines on ethical standards. Risk of
aging is an innate capability retained by captive-bred birds, disease transmission is deemed naturally low for vulture species, as
as they demonstrated movement through the same suitable they have evolved to withstand otherwise contagious diseases and
are often highly resistant. Our population reinforcement project was
habitat types as rehabilitated birds. In light of significant de- categorized as a least-risk, least-regret translocation using IUCN/
clines in natural food sources, the ability to forage in the most Species Survival Commission terminology. All relevant risk categories
appropriate environments may increase the chances of sur- outlined by IUCN/Species Survival Commission were evaluated as
vival for translocated birds (Botha et al., ). having low/no risk.
Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
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Oryx, 2021, 55(4), 607–612 © The Author(s), 2020. Published by Cambridge University Press on behalf of Fauna & Flora International doi:10.1017/S0030605319000814
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