Population Viability Analysis of Captive and Released Bearded Vulture Populations

Population Viability Analysis of Captive and Released Bearded Vulture Populations JAVIER BUSTAMANTE* Nationalparkverwaltung, Doktorberg 6, D 83471 Berchtesgaden, Germany, email [email protected]

Abstract: With the c o m p u t e r p r o g r a m VORTEX I r an a series o f s i m u l a t i o n s o f the B e a r d e d Vul ture (Gypae- tus barbatus) p o p u l a t i o n he ld in cap t iv i t y in E u r o p e a n z o o s a n d o f the p o p u l a t i o n released in the Alps. The s i m u l a t i o n s s h o w e d tha t the r isk o f ex t inc t ion o f the capt ive p o p u l a t i o n w i th the ex t rac t ion rates curren t ly in use is low. I t seems poss ib le to m a i n t a i n the cur ren t release rate o f two f l edg l ings p e r y e a r a t each o f the f o u r release sites in the Alps, b u t i t does n o t s eem poss ib le to increase the release rate by e x p a n d i n g the p ro j ec t to o ther E u r o p e a n m o u n t a i n s w i t h o u t dangerous ly deple t ing the capt ive popu la t ion . The mode l s s h o w e d tha t the m o s t effective w a y to increase the release rate w i t h o u t increas ing the capt ive p o p u l a t i o n s ize is by improving ha t ch ing success in captivity. The i n f o r m a t i o n o n the d e m o g r a p h i c p a r a m e t e r s o f the B e a r d e d Vul ture p o p u l a t i o n released in the Alps w a s n o t g o o d e n o u g h to p red i c t the u l t i m a t e f a t e o f the p r e s e n t p o p u l a t i o n or to a l l ow f o r r e c o m m e n d a t i o n s o n h o w long the p o p u l a t i o n s h o u l d c o n t i n u e to be supplemented . A l t h o u g h i t wi l l be necessary to w a i t s o m e y e a r s to see i f B e a r d e d Vul tures are ab le to breed in the w i l d in the Alps a n d to e s t imate f e c u n d i t y rates, i t s h o u l d be poss ib le to i m p r o v e the m o n i t o r i n g o f the i nd i v idua l s re leased to o b t a i n more-precise su rv i va l estimates. The mode l s o f the capt ive a n d released p o p u l a t i o n also s h o w e d tha t i t s h o u l d a t least be poss ib le to h a v e a n art i f ic ial ly s u p p l e m e n t e d B e a r d e d Vul ture p o p u l a t i o n in the Alps, b u t because this is n o t the goa l o f the p r e s e n t r e in t roduc t ion project , the o rgan i za t i ons i nvo l ved s h o u l d decide w h e t h e r this is a pol i t ica l ly or economica l l y des irable goal.

Anklisis de viabilidad de poblaciones para las poblaciones cautiva y liberada de quebrantahuesos

Resumen: Realicd u n a serie de s i m u l a c t o n e s de la p o b l a c i 6 n de Q u e b r a n t a h u e s o s (Gypaetus barbatus) cau- t i va en zool6gicos europeos y de la p o b l a c t 6 n l lberada en los Alpes con el p r o g r a m a VORTEX. Las s imu la - c tones m u e s t r a n que el riesgo de ex t tnc i6n de la p o b l a c t 6 n caut iva , con las tasas de ex tracc i6n e m p l e a d a s ac- tua lmente , es bajo. Parece pos ib le m a n t e n e r la tasa de l tberaci6n ac tua l de dos pol los p o r a ~ o en cada u n o de los cua t ro p u n t o s de sue l ta en los Alpes, p e r o no parece pos ib le i nc remen tar la p a r a ex t ender el proyec to a otras m o n t a ~ a s europeas. Los mode los m u e s t r a n que la m a n e r a mdts e fect iva p a r a a u m e n t a r la tasa de ex- tracci6n s in a u m e n t a r el t a m a ~ o de la p o b l a c t 6 n cau t i va serla m e j o r a r el dxito de eclosi6n en cautiverio. La i n f o r m a c i 6 n a cerca de los p a r d m e t r o s demogrd f l cos de la p o b l a c i 6 n de Q u e b r a n t a h u e s o s l iberada en los Alpes no es lo su f l c i en t emen te b u e n a p a r a predec i r el des t ino f i n a l de esta p o b l a c i 6 n o p a r a p e r m i t t r hacer re- c o m e n d a c i o n e s a cerca del t i empo q u e mdm deber~a c o n t i n u a r s i endo sup lemen tada . A u n q u e serd necesario esperar a lgunos a~os md~s p a r a ver s i los Q u e b r a n t a h u e s o s son capaces de cr lar en l lber tad en los Alpes y es- t i m a r su f e c u n d i d a d , es pos ib le m e j o r a r el s e g u i m i e n t o de los e jemplares l iberados p a r a ob tener e s t imas mO.s prec lsas de su superv ivencia . Los mode los de la p o b l a c i 6 n cau t i va y l iberada mues t ran , a s i mi smo , q u e a l m e n o s serta pos tb le m a n t e n e r en los Alpes u n a p o b l a c i 6 n de Q u e b r a n t a h u e s o s en l lber tad s u p l e m e n t a d a arti-

f l c ia lmen te ; p e r o d a d o q u e este no es el obje t ivo f i n a l del p royec to de re in t roducc i6n ac tua l las organ iza- c iones imp l i cadas deben p l a n t e a r s e si dste p u e d e ser u n ob je t ivo deseable desde u n p u n t o de v is ta po l i t i co o econ6mico.

*Current address: Estaci6n Biol6gica de Dof~ana, Consejo Superior de Investlgactones Cienttficas Pabell6n del Per~, Avda. Maria Luisa s/n, 41013 SeviUa, Spain. Paper submitted May 8, 1995; revised manuscript accepted September 19, 1995.

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Bustamante Bearded Vulture Viability Analyses 823

Introduction

Captive breeding of endangered species to reintroduce them to areas where they have disappeared or to supple- ment existing populations is frequently employed as a management tool (Newton 1979; Barclay 1987). These management actions are expec ted to increase the number of populations, their size, or the genetic variability within populations of the species concerned in order to decrease the probability of extinction.

Decisions on which species should have priority in reintroduction programs are usually subjective and based on politics, convenience, or public opinion pressure, although more-objective criteria are available. Once a reintroduction project is started and goals have been de- freed, it is possible to evaluate whe ther the management plan can meet the goals in a defined time frame. Money for conservation is limited, and funds employed in one project are sometimes withdrawn from others. Accord- ingly, it is important that the necessary information to evaluate whe ther goals are or will be accomplished be collected and analyzed.

Population viability analyses can be used as an objective tool to evaluate the risk of various management scenarios, to identify the demographic parameters to which the populations are more sensitive, and to indicate where research is more urgently needed to provide the information necessary for management of the population.

The Bearded Vulture (Gypaetus barbatus) is a cliff- nesting, accipitrid vulture inhabiting mountain ranges in Europe, Asia, and Africa and feeding predominantly on bones (Cramp & Simmons 1980; Brown & Plug 1990). Its breeding range in Europe has suffered a progressive reduction during the nineteenth and twentieth centu- ries. It is restricted n o w to the Pyrenees, the Southem Balkans, and the Islands of Corsica and Creta (Hiraldo et al. 1979; Frey 1994b).

The Bearded Vulture disappeared from the Alps, the northern limit of its historical range in Europe, in the nineteenth century (Cramp & Simmons 1980). Although it has been suggested that the cooling of the climate after the Middle Ages could have been responsible for the decline (Hailer 1983), it is generally assumed that direct persecution--ki l l ing of adults and robbery of eggs and ch icks - -and indirect mortality caused by poison baiting of carnivores helped to eliminate the species (Hiraldo et al. 1979).

The idea to reintroduce the Bearded Vulture to the Alps was first suggested by Oskar Heinroth in 1924 (G~roudet 1979). In the early 1970s there was an initial a t tempt to introduce birds taken f rom the wild; three birds from Afghanistan were released in the French Alps. Because of difficulties in obtaining a regular supply of wild birds for release, the high mortality suffered by the

birds, and the success of captive breeding by the Alpen- zoo Innsbruck since 1973, the initial plan was changed to a captive breeding project (G6roudet 1979; Walter 1979). The Bearded Vulture Reintroduction Project started as an international project in 1978 and initially involved 17 zoological gardens and 10 nature conservation organizations from Austria, France, Germany, and Swit- zerland.

In 1978, with a captive population of 30 wild-caught individuals (Frey & Walter 1989), efforts were directed to increasing the captive population through breeding and by trying to incorporate into the project all the birds kept by different zoos. In 1986 the first four Bearded Vultures born in captivity were released in Hohen Tauern National Park, Austria. By 1993 the captive population within the project included approximately 100 individuals, 53 of which were wild-caught, and 50 captive- born birds had been released into the Alps.

According to Frey and Bijleveld (1993), the project objective is "the establishment of a [Bearded Vulture] breeding population [in the Alps] totally independent of human management intervention." Released birds have not reproduced yet, although individuals seem to have survived to breeding age (more than 6 years). It is assumed that releases will continue at least until birds start breeding successfully in the wild, if they ever do, but there are no clear statements on h o w it will be deter- mined that the wild population requires no further management and that releases can be stopped. Considering that money for conservation is limited, it seems reasonable to ask h o w long it will be necessary to release birds into the Alps; if the information being gathered on the released birds is adequate to answer this question; if it would be poss ib le - -were an independent wild population not self-sustainable and the project objective was changed accordingly-- to continue releases from the captive population at the present rate; and, because there is a continuing demand for Bearded Vultures for other reintroduction projects in areas where the species has recently disappeared, such as the Cantabric Moun- tains and the Cazorla and Segura Mountains in Spain (Heredia 1981) or the Balkans (Grubac 1994; Negus 1994), would the captive population be able to supply birds for these demands in a reasonable period of time.

I have used a population viability analysis (PVA) of the captive and released Bearded Vulture populations to try to answer these questions with the information available. The PVA did not indicate what the fate of the captive and released Bearded Vulture populations would be, but it gave an objective evaluation of the risk of present and future management actions, indicated which information is more urgently needed to improve the models and help in management decisions, and suggested points on which to focus research effort.

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824 Bearded Vulture Viability Analyses Bustamante

Methods

I u sed the c o m p u t e r p r o g r a m VORTEX 5.1 (Lacy 1993) to s imulate de te rmin i s t i c and s tochas t ic factors affect ing the dynamics o f Bearded Vultures. VORTEX, a Monte Carlo s imula t ion o f d e m o g r a p h i c events , mode l s popula- t ion p roces ses as d iscre te , sequent ia l events , w i th proba- bil ist ic o u t c o m e s d e t e r m i n e d by a p s e u d o - r a n d o m num- b e r genera tor . VORTEX simulates b i r th and dea th p roces ses and t ransmiss ion o f genes t h rough genera- t ions b y genera t ing p s e u d o - r a n d o m n u m b e r s to deter- mine w h e t h e r each animal lives o r dies, w h i c h adul t female pai rs w i th each adul t male, w h e t h e r a pa i r ed adul t female p r o d u c e s a b r o o d o f a g iven size each year, the sex o f the offspring, and w h i c h of t w o alleles at a genet ic locus are t r ansmi t t ed f rom each pa ren t to each chick.

I used a s imula t ion m o d e l ins tead o f a de te rmin is t i c one because b o t h the cap t ive and re leased Bearded Vulture popu la t i ons w e r e small and they cou ld face a signif icant r isk o f ex t i nc t i on due to demograph ic , envi- ronmenta l , o r gene t i c s tochas t ic i ty or due to cata- s t roph ic events even in s i tuat ions in w h i c h the popula- t ions had a posi t ive g r o w t h rate. I s e l ec ted VORTEX because it is a we l l - known and wel l - tes ted p r o g r a m that cou ld m o d e l r easonab ly .we l l the Bearded Vulture popula t ion dynamics . T w o p o p u l a t i o n s w e r e s imulated, the cap t ive p o p u l a t i o n ma in ta ined in zoos and the popula - t ion re leased in the Alps.

Simulations of the Captive Population

The d e m o g r a p h i c p a r a m e t e r s used for the s imula t ion m o d e l o f the cap t ive p o p u l a t i o n (Table 1) w e r e the average values o b s e r v e d in capt iv i ty b e t w e e n 1978 and 1993 and w e r e ca lcu la ted f rom the da ta pub l i shed in the re- p o r t s o f the Bearded Vulture Re in t roduc t ion Pro jec t (Gy- pae tus Barbatus bul le t in nos. 1 to 15; Bearded Vulture Annual Repor t 1993). The annual cyc le was in i t ia ted at the t ime of egg laying, so ha tch ing success (46.76%), nest l ing survival (78.93%) and first-year post - f ledging survival (92.43%) w e r e inc luded in the es t imate o f first- year mor ta l i ty (65.9%). I u sed an adul t l i fespan of 7 to 31 years in the mode l s because females in cap t iv i ty laid the i r first egg at the m e d i a n age o f 6.5 years (n = 10) and the i r last egg at a med ian age of 31 years (n = 7), exclud- ing those tha t d i ed in the same yea r they laid eggs for the last t ime. The re w e r e no reasons to suspec t differ- ences in age at matur i ty or l i fespan b e t w e e n males and females. Obse rved annual mor ta l i ty rate is th ree t imes h ighe r in adul t b i rds than in immatu re birds, p r o b a b l y because i nexpe r i ence , w h i c h causes h ighe r mor ta l i ty rates a m o n g immatu re bi rds in the wild, does no t affect mor ta l i ty in capt iv i ty and because the adul t age class p r o b a b l y inc ludes seni le individuals suffering h ighe r

mor ta l i ty rates. There w e r e no signif icant d i f ferences in mor ta l i ty rates b e t w e e n males and females, so I u sed an average mor ta l i ty rate for b o t h sexes. Al though females in the wi ld lay a m a x i m u m of t w o eggs, females in cap- t ivi ty have laid up to four eggs, even t hough efforts have b e e n taken no t to fo rce doub le c lu tch ing wi th in the cap- t ive b reed ing p rogram. Initial age s t ruc ture and popula- t ion size (50 males and 39 females) w e r e t hose of the cap t ive popu l a t i on in January 1993. Adul t males (n = 9) and females (n = 5) o f u n k n o w n age w e r e given an age at r a n d o m b e t w e e n 7 and 31 years. Three individuals o f u n k n o w n sex ( they had no t b r e d and w e r e 1, 8, and 12 years old) w e r e given at r a n d o m the sex of male, female, and male respect ive ly . The re is no in format ion on the r isk o f a ca tas t rophe . I t hough t it r easonab le to assume that the re cou ld be a 1% probab i l i t y of a fire o r an epi- d e m i c in The Vienna Breed ing Unit (Austria) that ho lds 30% of the cap t ive p o p u l a t i o n and a p p r o x i m a t e l y 50% of the successful b r eed ing pairs, and that this cou ld resul t in the mor ta l i ty o f half the bi rds (0.85 mul t ip l ica t ive effect on survival) and no b r e e d i n g at the Vienna Breeding Unit in that year (0.5 mul t ip l ica t ive effect on r ep roduc- t ion). There w e r e a no the r 27 zoos co l labora t ing in the p ro j ec t in 1993, each k e e p i n g b e t w e e n one and six Bearded Vultures. Matings in the p ro j ec t are no t at ran- d o m as assumed by VORTEX, w h i c h makes the p r o g r a m inadequa te to s imulate the gene t ics o f the cap t ive popu-

Table 1. Summary of initial values for V O ~ for the captive population of Bearded Vultures.

Type of mating system: monogamous Age of first reproduction: 7 years Age after which adults do not reproduce: 31 years Sex ratio at birth (proportion of males): 0.5 Fecundity Rates

Maximum clutch size: 4 eggs Females laying 0 egg: 28.14%, SD = 16.88% Females laying 1 egg: 21.82% Females laying 2 egg: 46.16% Females laying 3 egg: 3.48% Females laying 4 egg: 0.39%

No density dependency in fecundity rates Mortality Rates

Juveniles (0-1 year): 65.90%, a SD -- 25.06% Immatures (2-6 year): 1.11%, SD = 4.03% Adults (7-31 year): 3.33%, SD = 3.07%

No correlation between mortality and fecundity annual rates No inbreeding depression Probability of a catastrophe: 1% b

Multiplicative effect on fecundity: 0.5 Multiplicative effect on mortality: 0.85

Initial population: 50 males and 39 females more than 1 year old c

Carrying capacity: projected at 200 individuals

alncludes 46.76% hatching success, 78.93% nestling survival, a n d 92. 43% first-year, post-fledging surv iva l b See methods f o r justif ication. C Init ial age distribution was that o f the captive popula t ion in Janu- ary 1993.

Conservation Biology Volume 10, No. 3,June 1996


lation. Inbreeding has been avoided, and until now there has been no pairing between related individuals. There were initially 30 wild-caught founders in the captive population, and another 23 wild-caught individuals were incorporated between 1978 and 1993. Individuals born in captivity have been transferred amorig zoos to avoid inbreeding (Frey 1993). I thought it best not to include inbreeding depression in the models because the ways VORTEX could model it were too unrealistic. I considered that the captive population could be simulated as a whole panmictic unit because individuals have been reg- ularly transferred among zoos to form breeding pairs. Al- though VORTEX gives values of observed and expected level of heterozygosity remaining after the simulation, I did not use those estimates in the conclusions because the assumptions of random mating, equal probability of breeding of all adults, and reshuffling of the breeding pairs every year do not apply to the captive population. Because the cost of the captive breeding project increases with population size, and 43% of the costs of the project are for keeping the birds in captivity (Patchlatko 1991), I assumed there would be a limit to population size. The maximum captive population size was limited in the models to 200 individuals (double the present size).

Populations were projected for 200 years, and each projection was run 500 times. Extraction rates of fledglings to be released to the wild were simulated under two scenarios.

In scenario 1 there was a fixed extraction rate: a fixed number of fledglings (the same number of males and females) were released every year, provided that at least that number was born into the captive population. The aim of the captive breeding project is to release at least two fledglings every year at each of the four release sites in the Alps (eight fledglings per year). The number of birds released was varied from three males and three females to seven males and seven females per year. The actual mean extraction rate from 1986 to 1993 was 5.9 fledglings per year.

In scenario 2 there were proportional extraction rates: a certain proport ion of the birds born each year is released to the wild. This is a more realistic scenario than scenario 1. The project tends to keep at least some of the birds born to maintain the captive population, and it can be assumed that the number of birds released would be reduced if the captive population declined. Propor- tional extraction rates were simulated in VORTEX by increasing In-st-year mortality accordingly. The proportion of birds released was varied from 40% to 80% of the chicks fledged each year. The actual extraction rate from 1986 to 1993 from the captive population was 60%.

Finaliy, I tested the sensitivity of the model to some demographic parameters by analyzing the relative effect on the population growth rate and on the number of chicks that could be released by improving each param-

eter. I ran simulations in which each demographic parameter at a time was improved by 10% and 100% of its biologically possible maximum improvement. I studied the effect of improving hatching success, nestling survival, first-year survival, immature survival, adult survival, and proportion of females that reproduce each year.

Simulations of the Population Released in the Alps

Because captive birds are released at the time of fledging and because the fecundity rate available for wild populations is the number of young fledged per breeding female, I started the annual cycle of the simulation of the released population at the time juveniles fledge. Esti- mates of demographic parameters are nonexistent or not as good as those for the captive population. The parameters used in the models came from different sources and are given in Table 2. For age at first breeding and for lifespan I used the same values as in captivity, although these might be optimistic. For mortalities and fecundities I used an optimistic and a pessimistic estimate for each parameter. Bearded Vultures have not reproduced in the Alps yet, so for fecundity rates I used an optimistic estimate of 0.67 fledglings per female-- the mean recorded productivity in the southern slopes of the Pyrenees between 1987 and 1991, n = 168 reproductions (Heredia 1991)--and a pessimistic estimate of 0.35 fledging per female--the mean recorded productivity in the northern slopes of the Pyrenees between 1986 and 1990, n -- 65 reproductions (Terrasse 1991). I cal- culated first-year mortality based on the 6 fledglings out of 41 (the 9 juveniles released in 1993 were excluded) that were recaptured, died, or disappeared with cer- tainty before the end of the first year (14.6% mortality), and I considered this as an optimistic estimate. The 95% upper confidence limit for this estimate, assuming a bi- nomial distribution, is 29%, and I used this as the pessimistic estimate for first-year mortality in the models. To estimate mortality rate after the first year I assumed a constant hazard rate and I adjusted the recorded ages at death to an exponential distribution (Crawley 1993). In- dividuals that outlive the duration of a study and will die at an unknown time in the future are said to be "censored." They contribute to our knowledge of the survi- vor function but not to our knowledge of the age at death (Crawley 1993). Birds assumed by the project to be alive were right-censored in September 1993. I did not right-censor the birds at the last published observation because I knew these were incomplete. Mean hazard (mortality) rate was 3.1%, and the 95% upper confidence limit was 9.4%. These estimates were used in the simulations as optimistic and pessimistic mortality rates after the first year (2-31 years of age). If each bird had been right-censored at the last published observation, the mean mortality rate and the upper limit would have been 5.7% and 17.6%. VORTEX assumes that the initial

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826 Bearded Vulture V'~ ' l i~ Analyses Bustamante

Table 2. Summary of initial values for VORTEX for the population released in the Mps

Type of mating system: monogamous Age at first reproduction: 7 years a Age after which adults do not reproduce: 31 years a Sex ratio at birth (proportion of males): 0.5 a Fecundity Rates ~

Maximum brood size at fledging: 1 Females raising 0 fledgling: 65.0-33.0% c Females raising 1 fledgling: 35.0-67.0%

No density dependency in fecundity rates Mortality Rates d

Juveniles ( l s t year): 14.6-29.0% c Immatures and adults (2-31 year): 3.1-9.4%

Correlation between mortality and fecundity annual rates Inbreeding depression: Recessive lethal model Probability of a catastrophe: 1%

Multiplicative effect on fecundity: 0.5 Multiplicative effect on mortality: 0.75

Initial population: 16 males and 24 females more than 1 year old e

Carrying capacity: projected at 500 individuals

a From the captive population. ~ From the Pyreneean population (Heredta 1991; Terrasse 1991). CMaximum and min imum rates used in the simulations (see methods). aFrom the population released in the Alps. eMaxtmum number still alive in September 1993.

p o p u l a t i o n is f o r m e d by un re l a t ed individuals and tha t individuals that are s u p p l e m e n t e d are un re l a t ed a m o n g themse lves and to o t h e r individuals in the p o p u l a t i o n (Lacy 1993). Actually, individuals In t he re leased popula- t ion are no t unre la ted . Many are offspr ing o f the same b reed ing pairs, and offspr ing o f these same pairs wil l con t inue to s u p p l e m e n t the p o p u l a t i o n In the future. Be- cause I have no in format ion on the degree o f i nb reed ing dep re s s ion in the Bearded Vulture, I u sed a recess ive leo thai m o d e l in all s imulat ions, w h i c h is p r o b a b l y an opti- mis t ic s imula t ion o f the poss ib le effect of inbreed ing . Also, I have no informat ion on the types and probabi l i - t ies o f ca t a s t rophes for the Bearded Vulture p o p u l a t i o n

in the Alps, so I d e c i d e d to k e e p the defaul t values o f VORTEX in all s imulat ions (see Table 2).

I p r o j e c t e d the r e l eased p o p u l a t i o n for 200 years and r e p e a t e d each s imula t ion 500 t imes. I s imula ted the pop- u la t ion u n d e r four di f ferent scenarios: (1) l o w mor ta l i ty and h igh fecundi ty , (2) l o w mor ta l i ty and l o w fecundi ty , (3) h igh mor ta l i ty and h igh fecundi ty , and (4) h igh mortal i ty and l o w fecund i ty (Table 2). In each scenar io I sim- u la ted that the p o p u l a t i o n was s u p p l e m e n t e d for O, 2, 5, 10, and 15 years w i th four males and four females m o r e each year.

I also s tud ied the effect o f annual var iabi l i ty in the pa- r amete r s due to env i ronmen ta l variabili ty. Environmen- tal var iance (EV) in p roduc t i v i t y based on the annual es- t imates for the Pyrenees (Hered ia 1991; Terrasse 1991) and Corsica (Fasce et al. 1989) ranges f rom 0.9 to 1.4 t imes d e m o g r a p h i c var iance ( D V ) - - t h e effect o f bino- mial sampl ing a round the m e a n in a small popu la t ion . Unfor tuna te ly the re are n o da ta available to es t imate en- v i ronmen ta l var iance in mortal i ty . Because the Alps are the no r the rn l imit o f the his tor ical d i s t r ibu t ion o f the Bearded Vulture In Europe, I e x p e c t e d that env i ronmen- tal var iance cou ld be at least as h igh as that of o t h e r areas. At the t w o scenar ios w i th l o w mor ta l i ty (1 and 2) I s tud ied the effect o f a l o w (1 × DV), m e d i u m (1.5 × DV), h igh (3 × DV), and very h igh (5 × DV) environ- menta l var iance in the pa ramete rs . In the s imula t ions no n e w individuals w e r e s u p p l e m e n t e d to the popu la t ion . Initial popu l a t i on size and age s t ruc ture w e r e that o f the bi rds assumed to b e alive in 1993.

Results

Captive Population

The aim of the s imula t ion was to s tudy w h i c h ex t r ac t ion rates cou ld be safely e m p l o y e d on the cap t ive population, arbi t rar i ly cons ide r ing as such those that gave a

Table 3.

Scenario

Population viability amflysis of the captive Bearded Vulture population under different extraction rates.

Probab i l i t y o f Years to Observed Ex trac t ion ex t inc t ion (%) ex t inc t ion he terozygos i ty

rate a ( ~ +- SE) ( ~ +- SE) ( ~ +- SE) (%)

Observed g r o w t h rate (5)

( ~ +- SE)

Fixed extraction rate

Proportional extraction rate

3M3F b 1.6 -+ 0.6 88 - 4.5 93.5 + 0.1 4M4F 8.6 --+ 1.3 70 --+ 3.0 93.4 + 0.1 5M5F 22.8 ----- 1.9 71 --+ 2.5 93.8 --+ 0.1 6M6F 52.6 ----- 2.2 64 --+ 1.6 93.9 -+ 0.2 7M7F 74.4 + 2.0 62 --+ 1.5 94.0 --+ 0.2

40 0.0 -- 0.0 93.6 -- 0.1 50 0.4 ----- 0.3 108 + 30.0 92.9 --+ 0.1 60 20.2 --+ 1.8 135 - 4.0 87.6 -+ 0.6 70 71.2 - 2.0 116 - 2.2 84.5 -+ 1.2 80 99.2 --+ 0.4 72 --+ 1.6 69.5 -+ 16.4

5.0 ----- 0.03 4.2 -- 0.03 2.9 -- 0.04 0.9 --+ 0.05

--1.4 --+ 0.06

3.3 ----- 0.03 2.1 --+ 0.03 O. 1 + 0.04

--2.1 --+ 0.05 --4.4 --+ 0.09

am = males; F = females. bPercentage o f fledglings released each year is shown f o r the proportional extraction rate scenario.


Bustanumte Bearded Vulture Viability Analyses 827

Table 4. Response of the captive Bearded Vulture population to improvement in a demographic parameter.

10% improvement 100% improvement

Observed Extraction rate* Observed Extraction rate* growth rate (%) fledglings/year growth rate (%) fledglings/year

Parameter improved (-~ +- SE) (-~ +-- SE) (~ +-- SE) (~ +- SE)

Hatching success 2.8 --- 0.03 15.0 --- 0.34 7.5 --- 0.03 25.2 -+ 0.22 Ne~tling mortality 2.2 -+ 0.03 12.7 - 0.39 3.7 - 0.03 16.9 -+ 0.29 First-year, post-fledging mortality 2.1 --- 0.03 12.1 --- 0.41 2.6 --- 0.03 13.5 --- 0.30 Immature mortality 2.1 +- 0.03 12.3 +- 0.38 2.5 --- 0.03 13.8 + 0.33 Adult mortality 2.3 --- 0.03 12.5 --- 0.35 4.2 - 0.03 15.2 - 0.14 Females breeding (%) 2.3 - 0.03 12.9 - 0.39 4.2 - 0.04 18.3 --- 0.35

*Number of fledglings released with a 50% release rate and a stable population of 200 individuals in captivify.

p r o b a b i l i t y o f e x t i n c t i o n o f t h e c a p t i v e p o p u l a t i o n n o t

g r e a t e r t h a n 5% in t h e n e x t 200 years . If a f i x e d ex t rac -

t i o n ra te w a s used , n o m o r e t h a n t h r e e ma le s a n d t h r e e

f e m a l e s c o u l d b e safely r e l e a s e d e a c h year , w i t h a p roba -

b i l i ty o f e x t i n c t i o n l o w e r t h a n 5% (Tab le 3). Re l ea s ing

f o u r m a l e s a n d f o u r f e m a l e s g ives a p r o b a b i l i t y o f ex t inc -

t i o n o f 8.6%. T h e l o w e r l imi t o f t h e 95% c o n f i d e n c e in-

t e rva l a r o u n d t h e e s t ima te , u s ing a b i n o m i a l d i s t r ibu t ion ,

w a s 6%, w h i c h is o v e r t h e 5% limit . H i g h e r r e l ea se ra tes

also g a v e p robab i l i t i e s o f e x t i n c t i o n s ign i f ican t ly o v e r

5%. If a p r o p o r t i o n a l e x t r a c t i o n ra te w a s e m p l o y e d , a

p r o p o r t i o n o f u p to 50% o f t he f ledgl ings c o u l d b e re leased

e v e r y y e a r w i t h a r isk o f e x t i n c t i o n n o t g r e a t e r t h a n 5%.

If t h e c r i t e r i o n to s e l e c t an e x t r a c t i o n ra te f r o m t h e

c a p t i v e p o p u l a t i o n w a s t h e m a x i m u m e x t r a c t i o n ra te

m a i n t a i n i n g a s l ight ly p o s i t i v e g r o w t h ra te in cap t iv i t y it

w o u l d b e p o s s i b l e to r e l ea se u p t o 12 b i rds p e r year , o r

60% o f t h e b i rds f l edged .

Table 5. Population viability analysis of the Bearded Vulture population released in the Alps, with effect of different mortality and fecundity rates and number of years releases are continued.

High survival Low survival

High Low High Low No. o f fecundity fecundity fecundity fecundity years a (~ +- SE) (~ +- SE) (~ +- SE) (~ +- SE)

Probability of ext inct ion (%)

Years to ext inct ion

Observed heterozygosity (%)

Final populat ion size ~

Observed growth rate (%) Without releases With releases

0 0.0 --+ 0.0 0.4 +- 0.3 61.4 --+ 2.2 100 - 0.0 2 0.0 -- 0.0 0.2 - 0.2 48.6 + 2.2 100 + 0.0 5 0.8 +--- 0.4 0.0 -+ 0.0 33.4 ----- 2.1 100 ----- 0.0

10 0.2 -- 0.2 0.8 +-- 0.4 19.4 --+ 1.8 100 --+ 0.0 15 0.0 ---- 0.0 0.2 ----- 0.2 11.4 ----- 1.4 99.8 ----- 0.2

0 27 ----- 14 99 -- 3.0 52 ----- 1.0 2 69 -- 0.0 107 ---+ 3.0 59 +--- 1.0 5 134 ----- 15 123 --+ 3.0 67 ----- 1.0

10 63 +- 0.0 85 +--- 23 134 ----- 4.0 81 +-- 1.0 15 73 + 0.0 148 _+ 5.0 89 ---- 1.0

0 96.5 ----- 0.07 95.5 ----- 0.14 79.2 --+ 1.36 2 97.2 + 0.06 97.0 -- 0.08 83.4 ----- 1.11 5 97.7 ----- 0.05 97.7 ----- 0.05 85.5 ----- 0.97

10 98.0 -- 0.04 98.2 -- 0.04 89.8 - 0.60 15 98.1 + 0.04 98.4 + 0.04 92.7 +-- 0.37

0 484 ----- 1.6 456 +-- 2.8 156 + 11.1 2 483 --+ 1.5 455 ----- 3.0 200 ----- 10.6 5 487 ----- 1.4 458 +-- 3.0 209 -- 9.1

10 486 +__ 1.5 458 --+ 3.1 237 ----- 4.0 15 484 ----- 1.7 456 ----- 2.8 267 +-- 7.8

8.2 _+ 0.03 3.7 -+ 0.03 --1.0 + 0.05 12.3 + 0.10 10.2 + 0.10 7.3 ----- 0.11

100 _+ 0.0

5 + 0 . 0

--5.8 - 0.11 ~5.8 -+ 0.11

aFour males and four females released every year during that number of years. Carrying capacity fixed at 500 individuals.

Conservation Biology Volume 10, No. 3, June 1996

828 Bearded Vulture ViabilitF Analyses Bustamante

Table 6. Population viabiliff anal~is of the Bearded Vulture population released in the Mps, with effect of environmeatal vartabiliff.

High s u r v i v a l

High L o w E n v i r o n m e n t a l f e c u n d i t y f e c u n d i t y

var iance a ( ~ +- SE) ( ~ +-- SE)

Probability of extinction (%)

Years to extinction

Observed heterozygosity (%)

Final population size ~

Observed growth rate (%)

Low (1 × DV) 0.0 - 0.0 0.4 -+ 0.3 Moderate (1.5 × DV) 0.0 - 0.0 2.0 - 0.6 High (3 × DV) 0.8 --_ 0.4 5.0 + 0.9 Very high (5 × DV) 19.2 -+ 1.8 25.4 - 2.0

Low (1 × DV) 27 --- 14.0 Moderate (1.5 × DV) 105 - 21.0 High (3 × DV) 102 --_ 33 79 -+ 10.0 Very high (5 × DV) 100 _ 5.0 86 - 5.0

Low (1 × DV) 96.5 - 0.07 95.5 -+ 0.14 Moderate (1.5 × DV) 96.3 -+ 0.09 94.6 -+ 0.29 High (3 × DV) 95.8 -+ 0.16 93.2 -+ 0.44 Very high (5 × DV) 93.9 -+ 0.42 93.3 -+ 0.42

Low (1 X DV) 484 -+ 1.6 456 -+ 2.8 Moderate (1.5 × DV) 475 -+ 2.3 438 -+ 4.0 High (3 × DV) 445 -+ 2.3 379 -+ 6.1 Very high (5 × DV) 416 +- 6.1 345 + 8.4

Low (1 X DV) 8.2 _+ 0.03 3.7 - 0.03 Moderate (1.5 × DV) 8.1 - 0.04 3.7 -+ 0.04 High (3 × DV) 7.8 --_ 0.05 3.4 --- 0.06 Very high (5 × DV) 7.5 -+ 0.07 3.3 -+ 0.07

aDV = demographic variance. Carrying capacity f ixed at 500 individuals.

The effect of improving the demographic parameters of the captive popu la t ion is g iven in Table 4. Hatching success is clearly the paramete r that, if improved, w ou l d give bo th a greater mean growth rate for the popu la t ion and a higher n u m b e r of fledglings to release pe r year wi th a l imited popu la t ion size.

Released Population

If the mortali ty rates of the popu la t ion were as low as our m i n i m u m mortalities, the released popu la t ion wou ld have a probabi l i ty of ex t inc t ion u n d e r the 5% limit (Ta- ble 5), even if no fur ther releases were conduc t ed and the popula t ion had a relatively low fecundity. If mortality rates were as high as the m a x i m u m values used in the simulations, even if the popu la t ion had a relatively high fecundi ty and releases were con t i nued for 15 years, the probabi l i ty of ex t inc t ion of the popu la t ion wou l d be over the 5% limit. In the wors t of all scenarios simulated, the popu la t ion wou ld b e c o m e ext inc t almost wi th cer- tainty if releases were d i scon t inued after 15 years.

The released popu la t ion takes a relatively long t ime to b e c o m e extinct . In the wors t s c e n a r i o - - l o w survival and low fecundi ty r a t e s - - t h e popu la t ion wou ld take a

m e a n of 52 years to b e c o m e ext inc t if no more releases were c onduc t e d (Table 5).

According to the simulations, the heterozygosi ty that remains in the popu la t ion after 200 years, if it does no t b e c o m e extinct , is relatively high. Only wi th a low survival and a high fecundi ty w ou l d the popu la t ion lose more than 5% of the original genet ic variability.

The released popu la t ion wou ld show a positive g rowth rate u n d e r all scenarios if birds f rom the captive popu la t ion con t inue to be released every year at the p resen t rate (four males and four females on average). In the scenarios wi th low survival, the growth rates were negat ive (the popu la t ion decl ined) if the popu la t ion was no t s u p p l e m e n t e d (Table 5).

The effect of env i ronmen ta l variability on the probability of ex t inc t ion w ou l d be impor tan t only if it was high or very high (more than three t imes the variability a t t r ibuted to demography; Table 6).

Discussion

Although VORTEX was able to simulate realistically most of the si tuations and m a n a g e m e n t options of the



Bearded Vulture populations, there are some important aspects that need further comment. Unfortunately, VOR- TEX is not able to model the long-term monogamy typi- cal of large birds of prey or to consider that all breeding pairs in the population will not have equal probability of reproducing successfully every year. (Pairs that breed successfully one year have a higher probability of breeding successfully the next year, both in captivity and in the wild.) This means that VORTEX, in general, will overestimate the number of genes transmitted to the next generation and will underestimate the extent of inbreeding. On the other hand, VORTEX always considers random mating, which is not applicable if pairing within the captive population is performed in trying to avoid inbreeding, as was the case. VORTEX is also unable to take account of the fact that the individuals in the initial population are related or that individuals released to the wild will be related among themselves or to the initial population, as is the case with the Bearded Vultures released to the Alps. This underestimates the risk of inbreeding depression. Also, the little information on the effect of inbreeding depression in birds and the lack of any data on the effect of inbreeding depression in large, long-lived raptors makes any values for the effect of inbreeding depression in the models highly speculative. Better models and more information on the effects of inbreeding depression would allow a more realistic model- ing of this aspect.

The results of the simulation show that it is possible to extract fledglings from the captive population of Bearded Vultures to use them for reintroduction projects without a significant risk to the captive population, provided that extraction rates are kept relatively low, no higher than three males and three females per year or no more than 50% of the chicks fledged in a particular year. The Bearded Vulture Reintroduction Project aims to release a minimum of two birds per release site, and four release sites are currently used in the Alps. This release scheme may be slightly over the safe extraction rate, but considering that in reality releases would be stopped if the captive population declined, these numbers can be considered safe. It would be dangerous to increase the extraction rate to start new reintroduction projects in other areas in the near future.

If the only criterion for selecting an extraction rate was the maximum extraction rate that allowed for a slightly positive growth rate in the captive population, it would be possible to release up to six males and six females per year, or 60% of the chicks fledged. But this probably would not be wise before the Alpine population can be guaranteed to be sel f -sustainable.

Only if the size of the captive population were sub- stantially increased or its present demographic parameters improved would it be possible to start new reintroduction projects in the next few years. From an economic point of view, improving some demographic parameters

would be cheaper in the long term because most of the funds for the reintroduction project are spent on mainte- nance of the captive population (Patchlatko 1991).

It is obvious that the improvement of any demographic parameter in the captive population would allow higher rates of release to the wild. The mortality rates of all age classes are relatively low, and it would probably be difficult to reduce them further. Even with zero mortality in certain age classes, its relative effect on the rate of release would be small. Hatching success is the parameter with the highest possibilities of increasing the growth rate of the captive population or the rate of release to the wild because of the greater sensitivity of the population to this parameter and because it can be improved to a greater degree. The present hatching success in the captive population (46.8%) is very low compared to the hatching success of birds of prey in the wild or in captivity, which range from 60% to 95% (New- ton 1979). Hatching success has not significantly improved since the project started (there is not a significant positive correlation with time from 1978 to 1993, r s = -0.1697, p = 0.51). Research focusing on why hatching success in the captive population is so abnor- maUy low and testing ways to improve it would be the strategy with the greatest possible benefits in the Bearded Vulture Reintroduction Project. If hatching success was improved up to 70%--the hatching success of the California Condor ( G y m n o g y p s c a l i f o r n i a n u s ) captive breeding project (Hartt et al. 1994) is below average hatching rates of birds of prey (Burnham 1983; Carpen- ter et al. 1987)mit would be possible to start soon rein- troductions to areas outside the Alps (Bustamante et al. 1994).

The lack of adequate data on the demographic parameters of the population released in the Alps means that almost any result is possible in the range of scenarios in which the population was simulated. Our simulations suggest that it would at least be possible to maintain an artificially supported population in the Alps if the present rate of release of captive birds was maintained. But this is not the present aim of the reintroduction project and the organizations involved in the project would have to decide if this was an economically or po- litically desirable aim.

Because Bearded Vultures in the Alps have not reproduced yet it is not possible to know what their fecundity rates will be. There is some information about mortality, which could be improved if the fates of all the birds released were known exactly. The only marking proce- dure currently allowed by the reintroduction project, apart from metal rings, is bleaching of flight feathers. This allows recognition of individuals for up to 1.5-2.5 years after release, depending on the positions of the markings and the rate of molt of flight feathers (Coton 1994). The project considers that recapturing individuals for remarking or using other longer-lasting marking


830 Bearded Vulture Viability Analyses Bustamante

m e t h o d s is t o o d a n g e r o u s o r t o o cos t l y (Frey & N i e b u h r

1994) a n d tha t e n o u g h i n f o r m a t i o n is o b t a i n e d w i t h o u t

m o r e s o p h i s t i c a t e d p r o c e d u r e s ( rad io t r a c k i n g o r longer -

las t ing marks) . T h e p r o j e c t s ta tes tha t 38 B e a r d e d Vul-

t u re s m o r e t h a n 1 y e a r o ld o f t h e 50 r e l e a s e d c o u l d theo-

re t ica l ly h a v e b e e n l iv ing f ree in S e p t e m b e r 1994 (F rey

1994a) . T h e 12 v u l t u r e s mi s s ing h a v e b e e n r e c a p t u r e d

(2 b i rds ) o r f o u n d d e a d (5 b i rds ) o r a re c o n s i d e r e d defin-

i t ive ly los t by t h e r e l ea se t e a m (5 birds) . O b s e r v a t i o n s

d u r i n g 1994 iden t i f i ed a m i n i m u m o f 25 d i f f e r en t indi-

v idua ls m o r e t h a n 1 y e a r o ld a l i v e - - t h e i den t i t y o f all o f

t h e m n o t e x a c t l y k n o w n ( K u r z w e i l 1994). C o m p a r i n g

t h e f igure o f v u l t u r e s t h e o r e t i c a l l y f r ee w i t h t h e mini-

m u m n u m b e r o b s e r v e d al ive r evea l s t ha t fo r a m i n i m u m

o f 13 ind iv idua l s r e l e a s e d (26%) it is n o t p o s s i b l e to say

w h e t h e r t h e y are a l ive o r dead . C o n s i d e r i n g tha t t h e to-

tal n u m b e r o f b i rds mi s s ing in t h e w i l d c o u l d add u p to

25, t h e p r o j e c t w o u l d h a v e b e e n ab le to f ind o n l y 28% o f

t h e b i rds mi s s ing (5 d e a d a n d 2 r e c a p t u r e d ) , and t h e ap-

p r o x i m a t e t i m e o f d i s a p p e a r a n c e f r o m t h e p o p u l a t i o n

w o u l d b e k n o w n in 48% o f t h e ind iv idua ls mi s s ing

(5 dead , 2 r e c a p t u r e d , and 5 lost) . If t h e m a r k i n g

m e t h o d a l l o w e d iden t i f i c a t i on fo r a l o n g e r p e r i o d o f

t i m e o r i f r ad io t r ansmi t t e r s w e r e e m p l o y e d , t h e s e fig-

u r e s c o u l d b e i m p r o v e d a n d t h e p r e c i s i o n in t h e mor ta l -

i ty e s t i m a t e s w o u l d i m p r o v e acco rd ing ly . Di f fe ren t t rap-

p i n g me thods , longer- last ing marks , and radio t ransmit te rs

h a v e b e e n e m p l o y e d o n w i l d B e a r d e d Vu l tu re s in t h e

P y r e n e e s (Sunyer 1991; Gil Galhis & Diez S~.nchez 1993)

and in Sou th Afr ica ( B r o w n 1988, 1990a , 1990b) w i t h

g rea t s u c c e s s and w i t h o u t a s ign i f ican t r isk to t h e

m a r k e d individuals . T h e i m p o r t a n c e o f g o o d e s t i m a t e s is

tha t w i t h o u t t h e m it wi l l b e i m p o s s i b l e to te l l i f t h e p o p -

u la t ion c a n b e se l f -sus ta inable and fo r h o w l o n g t h e re-

leases in t h e Alps s h o u l d c o n t i n u e . T o c o n t i n u e releas-

i ng b i rds it is n e c e s s a r y to b r e e d t h e m in capt iv i ty ,

w h i c h cos t s t i m e and m o n e y (Pa t ch i a tko 1991). Bo th o f

t h e s e r e s o u r c e s w o u l d b e w i t h d r a w n f r o m o t h e r possi- b le c o n s e r v a t i o n p ro j ec t s .

Acknowledgments

R. B6ge l and W. D ' O l e i r e h e l p e d w i t h s o m e p r e v i o u s

m o d e l i n g e x e r c i s e s o n t h e B e a r d e d Vu l tu r e w i t h VOR-

TEX. H. Frey h e l p e d to c lar i fy t h e p u b l i s h e d i n f o r m a t i o n

o n t h e m o r t a l i t y and r e p r o d u c t i o n o f b i rds h e l d in cap-

tivity. J. A. Donf izar and M. F e r r e r m a d e he lp fu l c o m -

m e n t s o n a p r e v i o u s draf t o f t h e p a p e r . T h e r e s e a r c h

w a s s u p p o r t e d b y a p o s t d o c t o r a l f e U o w s h i p o f t h e Span-

i sh C o u n c i l o f Sc ien t i f ic R e s e a r c h (CSIC) and by p r o j e c t P B 9 3 - 0 0 4 0 f r o m DGICYT.

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Population Viability Analysis of Captive and Released Bearded Vulture Populations

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