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Effectiveness of population recovery projects based on captive breeding
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Effectiveness of population recovery projects based on captive breeding Paweł Adamskia,*, Zbigniew J. Witkowskib a
Institute of Nature Conservation, Polish Academy of Sciences, al Mickiewicza 33, 32-120 Krako´w, Poland Faculty of Ecology and Environmental Management, Academy of Physical Education, al. Jana Pawla II 78, 31-571 Krako´w, Poland
b
A R T I C L E I N F O
A B S T R A C T
Article history:
A recovery programme for a population of Apollo butterflies in the Pieniny National
Received 22 May 2006
Park was monitored over 12 years in order to assess its effectiveness. The programme
Received in revised form
was based on population ecology and metapopulation theory, and its object was to
14 May 2007
replenish wild populations with captive-reared individuals. Thanks to the adopted mea-
Accepted 22 June 2007
sures, the local population initially numbering only 30–50 individuals increased to ca.
Available online 14 September 2007
1000 imagines, forming a functional metapopulation. Nevertheless, analysis of population dynamics parameters indicated that only some of the subpopulations were stable;
Keywords:
a significant percentage of the subpopulation fractions represented sink populations
Apollo butterfly
whose survival depended either on an external supply of captive-reared individuals or
Population recovery
on individuals from other source subpopulations. In some cases, intensively supplying
Metapopulation
the subpopulation with captive-reared individuals resulted in a decrease of that deme’s
Captive breeding
abundance.
Reproduction rate
The results suggest that supplying captive-reared individuals to an endangered population may entail some risks and should be done with caution. Ó 2007 Elsevier Ltd. All rights reserved.
1.
Introduction
One of the most spectacular active measures employed to protect an endangered species or population is to aid its recovery with the use of captive breeding (Hutching, 1997; Saint-Jalme, 2002). Projects of this kind require major financial outlays for breeding centre upkeep (Kleiman et al., 1991) and long-term monitoring (Ramoto et al., 1993; Johnson, 1994). For these reasons, Caughley and Gunn (1996) suggest that recovery projects should be rather short-term, serving the immediate goal of taking a population out of extreme danger. To optimize the financial resources spent on recovery projects, it seems important to set clear-cut goals, which upon being reached trigger plans to discontinue or suspend extremely labour-intensive and costly measures (Machado,
1997). The plan should also indicate whether a given population will be self-sustaining or will continue to rely on a supply of captive-bred individuals. This paper evaluates the effectiveness of a 12-year project to restore the Apollo butterfly (Parnassius apollo) population in the Pieniny National Park.
2.
Study site
The Pieniny Mts. are a narrow limestone mountain range straddling the Polish-Slovakian border (Fig. 1). This area is inhabited by one of the best-known Apollo butterfly populations in the northern part of the Carpathians (Nowicki-Siła, _ 1865, 1870; Sitowski, 1922; Zukowski, 1959; Witkowski, 1986; Adamski and Witkowski, 1999a). The population is made up
* Corresponding author: Tel.: +48 126321101; fax: +48 1266322432. E-mail address: [email protected] (P. Adamski). 0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2007.06.027
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1. Restoration of subpopulations of the species at most of the critical sites that meet its habitat requirements (Witkowski et al., 1997). 2. Augmentation of the whole metapopulation to a level close to the carrying capacity of the Pieniny National Park, estimated in a pilot project to be 1000–1500 imagines (Witkowski et al., 1992). 3. Restoration of a functioning metapopulation in which exchange of individuals between subpopulations occurs (Witkowski et al., 1997). 4. Creation of at least one large major site exhibiting features of a metapopulation source within the Pieniny metapopulation (Pulliam, 1988).
Fig. 1 – Location and structure of the Pieniny Apollo butterfy metapopulation 1 – subpopulations, 2 – functional population centers: W –Western, C – Central, E – Eastern, G – ‘‘Miedzy Grabczychami’’, ? – possible, but unverified site; 3 – Border Pieniny National Park.
of the subspecies Parnassius apollo frankenbergeri (Slaby, 1955), which inhabits only Pieniny National Park and the Haligovske Hory mountain massif in Slovakia. Population decline and habitat shrinkage were observed as early as the beginning of the 20th century. These processes quickened significantly in the 1950s. Significant changes in land use exacerbated the Apollo’s decline. These changes included abandonment of grasslands previously used as meadows or pastures and, in the 1960s, afforestation of xerothermic grassland and stony debris, critical habitats for the Pieniny Apollo (Witkowski and Adamski, 1996; Witkowski et al., 1997). The Pieniny Apollo has also been under strong pressure from butterfly collectors (Adamski and Witkowski, 1999a).
3.
Study population
In the late 1980s and early 1990s, the Apollo butterfly population in the Pieniny National Park was near extinction. The total area of habitats optimal for the Apollo butterfly was estimated at about 10 ha. The majority of the sites were fragmented and transformed. The whole population inhabited only one site in the Trzy Korony massif (eastern part of metapopulation; Fig. 1), and its abundance was estimated to be between 20 and 30 imagines (Witkowski et al., 1997). Apart from the dramatic drop in population numbers, there were some other disquieting phenomena: a large proportion of individuals with pathologically developed wings in the population (Adamski and Witkowski, 1999b), and an increase in the average fluctuating asymmetry of individuals (Adamski and Witkowski, 2002). Those occurrences were probably linked with genetic erosion, but there was no direct analysis of that population. In order to prevent the extinction of the population, a recovery programme was launched in 1991. For the proper functioning of the restored Apollo butterfly metapopulation in the Pieniny National Park, four conditions would have to be met:
The degree to which these conditions have been met can serve as a measure of the effectiveness of the programme. Two principal measures were employed to achieve them (Witkowski and Adamski, 1996): Reconstruction of xerothermic grassland the crusial habitat for the apollo habitat of the Apollo butterfly. Two factors basic to the presence of the Apollo were analysed: the abundance of the Apollo’s host plant, Sedum maximum, and the extent of xerothermic grassland. Abundance and distribution analyses showed that the food plant is quite common but that much of it is unavailable to the Apollo because it grows in areas afforested by natural succession or by management activities (Witkowski et al., 1992). In such cases, conservation activity concentrated mainly on removing trees and shrubs from the historical localities of the Apollo butterfly (Witkowski et al., 1997). By 2003 the area of the Apollo’s habitat increased by ca. 19 ha. Moreover, it consisted of a more compact set of sites, and stepping-stones ßt between those sites had been established. Introducing captive-bred individuals into the habitat. The natural population was supplemented with captive-bred individuals from 1992 till 2001. The captive breeding programme was established in 1991 based on individuals taken from the last surviving Apollo deme from the ‘‘E’’ part of the population. Until 1995, replenishment was restricted to two areas – ‘‘E’’ and ‘‘G’’. In 1996 the first captive-reared individuals were introduced to restored habitats in the ‘‘W’’ and ‘‘C’’ parts of the metapopulation. Supplementation of the ‘‘W’’ and ‘‘G’’ parts of the metapopulation ceased in 1997 (Adamski and Witkowski, 1999a) (Fig. 2). In 1995, in order to obviate the potential effects of genetic erosion, it was decided to include in the breeding programme some
Fig. 2 – Intensity of captive- reared support of the wild population.
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individuals from the nearest population of the same subspecies, obtained from Haligowskich Skaly (Slovakia). After this measure, in 1996 three breeding lines were obtained: Polish, Slovak and mixed (Witkowski and Adamski, 1996; Adamski and Witkowski, 1999a). In the beginning of the project the idea of artificially increasing food plant abundance was considered. However, abundance studies of the stonecrop (Sedum maximum) (Witkowski et al., 1992) indicated that this perennial plant was still quite abundant at the sites, including highly altered ones. These activities were coupled with studies aimed at monitoring the effect of the activities and solving problems appearing during their implementation. After 12 years of intensive work, the data gathered to date warrant an assessment of whether the restored metapopulation is stable and can survive without permanent support from captive-reared individuals. The Pieniny metapopulation, restored as a result of preparatory activities and introduction, can be divided in three large functional population patches (Fig. 2). The eastern part of the metapopulation (E), inhabiting the Trzy Korony massif and Sobczanski gorge. The area has some nine screes of various sizes accompanied by xerothermic grassland. The central part (C), including the xerothermic grasslandcovered slopes of Gorczynski gorge and similar habitats of Nowa Go´ra, Macelowa Go´ra and the Cyrlowa Skałka hills. The western assemblage (W) of demes on fairly extensive and compact screes located on the Ubszar, Długa Grapa, Flaki and Cisowiec hills, and the slopes around Czorsztyn castle. The restored metapopulation occupies yet another single site on a large a large area of stonedebris called Miedzy Grabczychami (G); despite it’s proximity to the Trzy Korony massif (E) (Fig. 1), it is evidently isolated from it by the relief of the area. Currently the area suitable for the Apollo butterfly covers about 40 ha, under the management of National Park staff.
4.
Methods
The population numbers were determined by marking and recapturing imagines (Witkowski et al., 1997). During the period when the imagines were present, each of the potential sites of Apollo butterflies were visited twice a week for 1– 3 h, depending on site size. During these visits, all observed Apollo butterflies were captured and the following data were registered for each catch: (1) The date and time of capture. (2) The code of the individual. At capture each individual was marked with a unique code allowing its unambiguous identification. The individuals obtained from breeding in captivity were marked before their release to sites. (3) The sex of the individual, and in females the presence or absence of the sphragis, a structure formed by the male over the femaletßs abdomen to prevent her from remating and displacing his sperm.
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(4) The site of capture, and for larger sites also the approximate location within the site. The site where capture occurred, and in larger sites also the approximate location within the site. The collected data were used to estimate the population numbers of the Pieniny metapopulation through the Jolly method, using the Jolly software package (Pollock et al., 1990). This method, based on the ‘‘open population’’ was checked because of significant migration rate within the population and the emergence of newly hatched individuals during the sampling period; for this reason, method B was used. The total population abundance in the whole sampling period was extrapolated from the estimated population abundance in a given sampling (Seber, 1982; Pollock et al., 1990). The marking of individuals also revealed cases of migration between sites. To determine the stability of the restored population, a modified net reproduction rate coefficient (Krebs, 1994) was calculated, taking into account the presence of captive-bred individuals on the site Et ¼
Wtþ1 Wt þ Ct
ð1Þ
where Et represents the yearly effectiveness of restoration activity, Wt the number of wild individuals in the population in year t, Wt+1 the abundance of the wild population in the next year, and Ct the number of captive-reared individuals released to the site in year t. The coefficient was calculated for the whole population as well as for each of the four parts distinguished within it. In each year, a migration coefficient was determined for the metapopulation, indicating the fraction of marked individuals that undertook migration outside their original habitat patch. The coefficient was calculated separately for short-distance (within metapopulation centres) and long-distance migration (between these centres). To assess the impact of introducing captive-reared individuals into the population, regression analysis was performed to determine the effects of wild population size and introduction intensity on reproduction rate in a given part of the metapopulation, as well as on population number in the following year.
5.
Results
During the period in which the reintroduction measures were carried out, the range of the Pieniny metapopulation of the Apollo butterfly expanded from the single subpopulation in the Trzy Korony massif to more than a dozen subpopulations living at almost all the major sites potentially suitable for this species within the Pieniny National Park (Fig. 3). The estimated total number of the Pieniny metapopulation increased from a mere 30 individuals in 1991 to over 1200 in 2002 (Fig. 4a), with the greatest increase occurring in the Trzy Korony massif, where ca. 50% of the metapopulation live (Fig. 4b). The values for short-distance dispersion within metapopulation centres calculated since 1996 have fluctuated between 30% and 40% of the individuals found (Table 1). The
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Fig. 3 – Expansion of the metapopulation range during the recovery process.
long-distance migration coefficient increased initially, reaching a maximum 4.7% in 1999, and then declined to 2% in 2002, but the ratios of long-distance migrants between particular non-zero years did not differ significantly (v2 = 9.267, df = 8, p = 0.3206) (Table 1). In 1996, all individuals undertaking migration were those reared in captivity from either the Slovak or the mixed line. The sex ratio of the migrants did not differ from those of all marked specimens (v2 = 226, df = 1, p = 0.1448). The value of the reintroduction effectiveness index for the whole metapopulation exceeded 1 only in 1992 and 1997. The values of these indices for particular metapopulation centres are given in Table 2. Regression analysis indicates that the number of wild individuals emerging at a site in a given year was closely related to the number of a given subpopulation in the previous year (N = 48, betawild = 0.431, pwild < 0.0001 SEbetawild = 0.042), whereas the effect of captive-bred individuals introduced to the site in the previous year was not significant (N = 48, betacaptive = 0.084, pcaptive = 0.1366 SEbetacaptive = 0.055). Since population abundance at the sites often distinctly differed between years, the data were divided into two groups by the median of the number of individuals observed at the given site. When the number of observed individuals was lower than the median calculated for the site, population abundance in that year was positively related to the same value in the previous year (N = 29, betawild = 0.790, pwild < 0.0001, SEbetawild = 0.117, betacaptive = 0.115, pcaptive = 0.0228, SEbetacaptive = 0.047). When the population number at the site was more than the median, both mentioned parameters were also significantly correlated, but the relation between population abundance and the number of captive-reared individuals introduced into the field in the previous year was negative (N = 19, betawild = 0.434, pwild < 0.0001, SEbetawild = 0.047, betacaptive = 0.286, pcaptive = 0.0363, SEbetacaptive = 0.124).
6.
Fig. 4 – Changes in population abundance during the reintroduction process: a — whole metapopulation 1 – number of marked individuals, 2 – estimated population size, 3 – +/- standard error of the estimated population size, b — particular metapopulation centers.
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Discussion
As an important flagship species, the Apollo butterfly has been the object of successful population recovery projects. Some projects were aimed at expanding an existing population (Dolek and Geyer, 2002; Dankova´, 1997). One reintroduction project led to the restoration of an extinct population (Luka´sˇek, 2000). An increase in the spatial range of a metapopulation and increased abundance of wild populations have been routinely taken as proof of the effectiveness of a reintroduction programme (Dolek and Geyer, 2000; Geyer and Dolek, 1995; Witkowski et al., 1997; Adamski and Witkowski, 1999a). In the analysed case, close scrutiny of the effectiveness coefficients (Table 1) yields less optimistic conclusions. As mentioned earlier, the effectiveness coefficient calculated as given above is the net population reproduction rate determined for a given year and taking into account captive-reared individuals (Krebs, 1994) In these circumstances, in order to be deemed stable, the coefficient for a population should be at least equal to 1. Populations with a lower rate of reproduction over a period of many seasons are so-called sink populations, whose survival depends upon an uninterrupted inflow of individuals from
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Table 1 – Dispersive activity of butterflies as, percentages of individuals Year
Dispersion inside the metapopualtion centers E
1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
C
0.0 2.2 7.2 28.6 31.1 35.5 32.5 43.3 35.7 34.1 34.0 33.233
– – – – 32.4 34.5 32.4 40.6 37.2 32.6 31.7 35.2
W – – – – 32.1 33.7 31.6 40.5 37.0 36.6 31.5 31.4
Dispersion between the centers
G
Total
0.0 2.0 5.1 26.2 0.0 33.3 29.6 36.4 28.0 16.7 27.3 29.2
0.0 2.0 6.3 27.1 31.4 34.3 32.1 41.5 36.2 34.1 32.6 33.2
0 0 0 1.2 2.4 2.1 3.9 4.7 3.8 2.9 2.1 2.5
Table 2 – Effectiveness of the restoration programme, calculated by year
1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
E
C
W
G
Total
1.69 0.93 1.31 0.59 0.85 1.42 1.76 1.15 1.12 1.06 0.92 1.14
– – – – – 1.07 1.01 0.28 0.36 0.53 0.68 1.24
– – – – – 1.06 0.20 0.74 0.44 0.55 1.31 0.51
1.04 0.46 0.05 0.32 0.03 3.64 1.80 0.42 2.25 0.23 1.89 0.51
1.67 0.84 0.13 0.48 0.36 1.23 0.84 0.69 0.77 0.78 0.96 0.92
source populations (Pulliam, 1988; Pulliam and Daniellson, 1991), in this case the captive-bredpopulation. Analyses of the effectiveness coefficients for particular metapopulation centres give less pessimistic conclusions. In the Pieniny National Park the Apollo butterfly forms a metapopulation, so not all its parts need have the characteristics of source subpopulations (Pulliam and Daniellson, 1991). Moreover, the number of individuals in sink populations may even markedly exceed the number in the source population (Watkinson and Sutherland, 1995). In the Pieniny metapopulation of the Apollo butterfly, site E may definitely be recognized as a metapopulation source. It is inhabited by the strongest and most stable of the Pieniny Apollo butterfly subpopulations. Since 1996 the net reproductive rate at site E has either exceeded or been only slightly below 1 (Table 1). In other parts of the metapopulation where results were calculated, major year-to-year fluctuations were shown, particularly in the small subpopulation G. This low stability, possibly the result of low numbers of individuals in that population, coupled with its peripheral location and its isolation, means that the role of G in the functioning of the whole metapopulation is fairly minor. For the practice of conservation, the relation between population size and the extent of captive-bred supply in previous years is an important one. Our results show that for a relatively small population the effect of captive-bred supply
is positive, whereas in abundant subpopulations the opposite is true. Thus it can be suggested that introducing a large number of captive-reared individuals to a site may result in local overcrowding of the population. If, as a result, the combined numbers of wild and captive-reared populations at a given site approach the carrying capacity, one can expect a lower rate of increase due to higher migration (Bujalska and Gru¨m, 1994) or lower production of fertile offspring (Krebs, 1994). In the present case it may be assumed that the high number of imagines translates to a higher number of eggs laid, and thence a high number of caterpillars emerging at the site in the next year. Studies completed to date regarded the abundance of stonecrop (Sedum maximum) to be the limiting factor for the discussed metapopulation (Witkowski et al., 1992, 1997). The emergence of high numbers of caterpillars foraging on this plant early in the vegetation season may lead to temporary erosion of the food supply. Our oversupply hypothesis is supported by the finding that the most stable subpopulation, E, is the place where the relative level of captive-reared supply was lowest. Under such circumstances, supplementing small populations with small groups of captive-reared individuals should be regarded as the most effective strategy. Analysis of the movements of individuals between and within locations indicates that the suggested division of the Pieniny metapopulation into three distinct centres and one somewhat isolated site matches its actual dynamics. Within
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the main centres, the coefficient of exchange of individuals between restored habitat patches was very high; thus these areas should be treated, at least in part, as population patches in a greater metapopulation (Harrison, 1991; Harrison and Taylor, 1997). It might seem surprising that the individual exchange coefficients for all the metapopulation centres were similar, despite the much greater distances between the sites of the western centre. Straight-line distance, however, is only one of several factors affecting the probability of migration of individuals between sites (Hanski, 1997). In the case of the Apollo butterfly, the presence of open areas between sites enabling free dispersion of the species is at least equally important (Brommer and Fred, 1999). Studies of Parnassius smintheus describe the crucial role of habitat structure in the dispersion activity of the butterflies (Fownes and Roland, 2002; Matter et al., 2004). This structure involves not only the distribution of open areas but also the within-meadow structure (Ross et al., 2005). The lack of suitable migration corridors around site G is the factor behind the low level of migration among local individuals, as well as the low number of butterflies from other sites reaching subpopulation G. Interestingly, in the studied population the migration ratios of the males and females did not differ, in contrast to other results and theoretical predictions (Matter and Roland, 2002). Unfortunately the data available for the Pieniny population are insufficient to explain this phenomenon. The exchange of a few percent of the individuals between the main metapopulation centres seems enough to protect the metapopulation against genetic erosion (Gilpin, 1996), but it is not certain whether it is high enough to bring about spontaneous recovery of a subpopulation if one of the main centres becomes extinct. At the outset of the recovery programme, the Pieniny population of the Apollo butterfly had an extraordinarily low dispersion coefficient, and raising it was one of the priorities for the project (Witkowski and Adamski, 1996; Adamski and Witkowski, 1999a). It seems that the dispersion coefficient is boosted mainly by introducing into breeding some individuals from another less isolated population (Witkowski and Adamski l.c). The drop in longdistance migration noted in the last three years is most likely an artefact resulting from the fact that the probability of recapturing an individual decreases with increased population number (Seber, 1982; Turchin, 1998; Adamski, 2004). In most recovery projects for the Apollo butterfly, the key activity consists in maintaining or recovering suitable areas. In the Franconian Alps this activity also involved co-operation with mining enterprises located in this region (Dolek and Geyer, 2002). In the Pieniny Mts, introduction of pasture to habitats suitable for the Apollo butterfly is problematic because it may conflict with other conservation imperatives of Pieniny National Park. In such a case, the Apollo butterfly habitat is maintained through special activities of the National Park Service.
7.
Conclusions
It can be said that a functional metapopulation of the Apollo butterfly has been successfully restored in the Polish part of the Pieniny Mts. Since the supply of captive-reared individu-
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als is continuous, however, it is impossible to determine unambiguously whether the metapopulation would function without this kind of support. Undoubtedly the population patch of the Trzy Korony massif (metapopulation centre E) can be regarded as a stable part of the metapopulation. Its net reproduction rate throughout the last six years has exceeded 1 or fallen only slightly below it (Table 2). A coefficient for the exchange of individuals between metapopulation centres amounting to a few percent is too low to significantly affect the growth rate estimate for any particular metapopulation centre. The possibility that the stability of population patch E may be the result of an influx of migrants from other sites may thus be excluded. Under these circumstances, this local population patch may be regarded as a metapopulation source (Pulliam, 1988). Two other centres seem to have the characteristics of sink populations, but their actual status can only be determined after the supply of captive-reared individuals ceases. Also unclear is the status of the single site at G; significant fluctuations of population number occur there, but owing to its peripheral position, its impact on other subpopulations seems very limited. Nevertheless, due to its peripheral position, this population could function as a stepping stone between the population in the Pieniny National Park and the more numerous population at Haligovske Hory in Slovakia.
Acknowledgments The authors would like to thank Andrzej Kosior and Piotr Płonka for co-working on the project of Apollo butterfly recovery. Special thanks are due to the staff of the Pieniny National Park and PIENAP, particularly to Michał Sokołowski, Bogusław Kozik, Tadeusz Oles´, Sˇtefan Danko and Katarı´na Zˇlkovanova´. Authors are also grateful Polish and Slovak ministries of environment for enabling us exchange of individuals between captive breadings (Slovak CITES export permission No. 00045/95, Polish CITES import permission No. 4772/96/95).
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of the butterfly Parnassius smintheus. Ecol. Entomol. 27 (3), 308–316. Matter, S.F., Roland, J., Moilanen, A., Hanski, I., 2004. Migration and survival of Parnassius smintheus: detecting effects of habitat for individual butterflies. Ecol. Appl. 14 (5), 1526–1534. Nowicki-Siła, M., 1865. Motyle Galicyi. Drukarnia Instytutu Stauropigian´skiego, Lwo´w, p. 152. Nowicki-Siła, M., 1870. Wiadomostki z Pienin, Sprawozdania Komisji Fizjograficznej 4. Pollock, K.H., Nichols, J.D., Brownie, C., Hines, J.E., 1990. Statistical Inference for Capture-Recapture Experiments. Wildlife Monographs. Pulliam, H.R., 1988. Sources, sinks, and population regulation. Am. Naturalist 132, 652–661. Pulliam, H.R., Daniellson, B.J., 1991. Sources, sinks, and habitat selection; a landscape perspective on population dynamics. Am. Naturalist 137, 50–66. Ramoto, W.S., Santaprillai, C., Mackinnon, K., 1993. Conservation and managament of Javan rhino (Rhinoceros sondaicus) in Indonesia. In: Ryder O.A. (Ed.), Rhinoceros biology and conservation. Proceedings of an international conference, of Zoological Society, May 9–11, 1991, San Diego, California, San Diego, pp. 265–273. Ross, J.A., Matter, S.F., Roland, J., 2005. Edge avoidance and movement of the butterfly Parnassius smintheus in matrix and non-matrix habitat. Landscape Ecol. 20 (2), 127–135. Saint-Jalme, M., 2002. Endangered avian species captive propagation: an overview of functions and techniques. Avian Poult. Biol. Rev. 13 (3), 187–202. Seber, G.A.F., 1982. The estimation of Animal Abundance and Related Parameters. Charles Griffin, London. Sitowski, L., 1922. Charakter i osobliwos´ci przyrody Pienin´skiej. Ochrona Przyrody 3, 47–55. Slaby, J., 1955. Parnassius apollo L. im Pieninengebiet. Biolo´gia Bratislava 10, 179–188. Turchin, P., 1998. Quantitative Analysis of Movement: Measuring and Modeling Population Redistribution in Plants and Animals. Sinauer Associates, Sunderland, MA. Watkinson, A.R., Sutherland, W.J., 1995. Sources, sinks and pseudo-sinks. J. Animal Ecol. 64, 126–130. Witkowski, Z., 1986. Parnassius apollo (L.) in Poland its history and present status. In: Welthuis H.R.W. (Ed.), Proceedings of the 3th European Congress of Entomology, Amsterdam. Witkowski, Z., Adamski, P., 1996. Decline and rehabilitation of the apollo butterfly Parnassius apollo (Linnaeus, 1758) in the Pieniny National Park (Polish Carpathians). In: Settele, J., Margules, C., Poschol, P., Henle, K. (Eds.), Species Survival in Fragmented Landscapes. Kulwer Academic Publishers, Dordreht,/Boston/ London, pp. 7–14. Witkowski, Z., Klein, J., Kosior, A., 1992. Restytucja niepylaka apollo, Parnassius apollo frankenbergi Slaby w Pienin´skim Parku _ Narodowym I. Gdzie i jak licznie gatunek ten moze wyste˛powac´ w Pieninach? Chron´my Przyrode˛ Ojczysta˛ 48 (3), 69–83. Witkowski, Z., Adamski, P., Kosior, A., Płlonka, P., 1997. Extinction and reintroduction of Parnassius apollo in the Pieniny National Park (Polish Carpathians) Biologia. Bratislava (52/2), 199–208. _ Zukowski, R., 1959. Problemy zaniku i wymierania niepylaka apollo w Polsce. Sylwan 103 (6/7), 15–29.
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available at www.sciencedirect.com
journal homepage: www.elsevier.com/locate/biocon
Effectiveness of population recovery projects based on captive breeding Paweł Adamskia,*, Zbigniew J. Witkowskib a
Institute of Nature Conservation, Polish Academy of Sciences, al Mickiewicza 33, 32-120 Krako´w, Poland Faculty of Ecology and Environmental Management, Academy of Physical Education, al. Jana Pawla II 78, 31-571 Krako´w, Poland
b
A R T I C L E I N F O
A B S T R A C T
Article history:
A recovery programme for a population of Apollo butterflies in the Pieniny National
Received 22 May 2006
Park was monitored over 12 years in order to assess its effectiveness. The programme
Received in revised form
was based on population ecology and metapopulation theory, and its object was to
14 May 2007
replenish wild populations with captive-reared individuals. Thanks to the adopted mea-
Accepted 22 June 2007
sures, the local population initially numbering only 30–50 individuals increased to ca.
Available online 14 September 2007
1000 imagines, forming a functional metapopulation. Nevertheless, analysis of population dynamics parameters indicated that only some of the subpopulations were stable;
Keywords:
a significant percentage of the subpopulation fractions represented sink populations
Apollo butterfly
whose survival depended either on an external supply of captive-reared individuals or
Population recovery
on individuals from other source subpopulations. In some cases, intensively supplying
Metapopulation
the subpopulation with captive-reared individuals resulted in a decrease of that deme’s
Captive breeding
abundance.
Reproduction rate
The results suggest that supplying captive-reared individuals to an endangered population may entail some risks and should be done with caution. Ó 2007 Elsevier Ltd. All rights reserved.
1.
Introduction
One of the most spectacular active measures employed to protect an endangered species or population is to aid its recovery with the use of captive breeding (Hutching, 1997; Saint-Jalme, 2002). Projects of this kind require major financial outlays for breeding centre upkeep (Kleiman et al., 1991) and long-term monitoring (Ramoto et al., 1993; Johnson, 1994). For these reasons, Caughley and Gunn (1996) suggest that recovery projects should be rather short-term, serving the immediate goal of taking a population out of extreme danger. To optimize the financial resources spent on recovery projects, it seems important to set clear-cut goals, which upon being reached trigger plans to discontinue or suspend extremely labour-intensive and costly measures (Machado,
1997). The plan should also indicate whether a given population will be self-sustaining or will continue to rely on a supply of captive-bred individuals. This paper evaluates the effectiveness of a 12-year project to restore the Apollo butterfly (Parnassius apollo) population in the Pieniny National Park.
2.
Study site
The Pieniny Mts. are a narrow limestone mountain range straddling the Polish-Slovakian border (Fig. 1). This area is inhabited by one of the best-known Apollo butterfly populations in the northern part of the Carpathians (Nowicki-Siła, _ 1865, 1870; Sitowski, 1922; Zukowski, 1959; Witkowski, 1986; Adamski and Witkowski, 1999a). The population is made up
* Corresponding author: Tel.: +48 126321101; fax: +48 1266322432. E-mail address: [email protected] (P. Adamski). 0006-3207/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.biocon.2007.06.027
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1. Restoration of subpopulations of the species at most of the critical sites that meet its habitat requirements (Witkowski et al., 1997). 2. Augmentation of the whole metapopulation to a level close to the carrying capacity of the Pieniny National Park, estimated in a pilot project to be 1000–1500 imagines (Witkowski et al., 1992). 3. Restoration of a functioning metapopulation in which exchange of individuals between subpopulations occurs (Witkowski et al., 1997). 4. Creation of at least one large major site exhibiting features of a metapopulation source within the Pieniny metapopulation (Pulliam, 1988).
Fig. 1 – Location and structure of the Pieniny Apollo butterfy metapopulation 1 – subpopulations, 2 – functional population centers: W –Western, C – Central, E – Eastern, G – ‘‘Miedzy Grabczychami’’, ? – possible, but unverified site; 3 – Border Pieniny National Park.
of the subspecies Parnassius apollo frankenbergeri (Slaby, 1955), which inhabits only Pieniny National Park and the Haligovske Hory mountain massif in Slovakia. Population decline and habitat shrinkage were observed as early as the beginning of the 20th century. These processes quickened significantly in the 1950s. Significant changes in land use exacerbated the Apollo’s decline. These changes included abandonment of grasslands previously used as meadows or pastures and, in the 1960s, afforestation of xerothermic grassland and stony debris, critical habitats for the Pieniny Apollo (Witkowski and Adamski, 1996; Witkowski et al., 1997). The Pieniny Apollo has also been under strong pressure from butterfly collectors (Adamski and Witkowski, 1999a).
3.
Study population
In the late 1980s and early 1990s, the Apollo butterfly population in the Pieniny National Park was near extinction. The total area of habitats optimal for the Apollo butterfly was estimated at about 10 ha. The majority of the sites were fragmented and transformed. The whole population inhabited only one site in the Trzy Korony massif (eastern part of metapopulation; Fig. 1), and its abundance was estimated to be between 20 and 30 imagines (Witkowski et al., 1997). Apart from the dramatic drop in population numbers, there were some other disquieting phenomena: a large proportion of individuals with pathologically developed wings in the population (Adamski and Witkowski, 1999b), and an increase in the average fluctuating asymmetry of individuals (Adamski and Witkowski, 2002). Those occurrences were probably linked with genetic erosion, but there was no direct analysis of that population. In order to prevent the extinction of the population, a recovery programme was launched in 1991. For the proper functioning of the restored Apollo butterfly metapopulation in the Pieniny National Park, four conditions would have to be met:
The degree to which these conditions have been met can serve as a measure of the effectiveness of the programme. Two principal measures were employed to achieve them (Witkowski and Adamski, 1996): Reconstruction of xerothermic grassland the crusial habitat for the apollo habitat of the Apollo butterfly. Two factors basic to the presence of the Apollo were analysed: the abundance of the Apollo’s host plant, Sedum maximum, and the extent of xerothermic grassland. Abundance and distribution analyses showed that the food plant is quite common but that much of it is unavailable to the Apollo because it grows in areas afforested by natural succession or by management activities (Witkowski et al., 1992). In such cases, conservation activity concentrated mainly on removing trees and shrubs from the historical localities of the Apollo butterfly (Witkowski et al., 1997). By 2003 the area of the Apollo’s habitat increased by ca. 19 ha. Moreover, it consisted of a more compact set of sites, and stepping-stones ßt between those sites had been established. Introducing captive-bred individuals into the habitat. The natural population was supplemented with captive-bred individuals from 1992 till 2001. The captive breeding programme was established in 1991 based on individuals taken from the last surviving Apollo deme from the ‘‘E’’ part of the population. Until 1995, replenishment was restricted to two areas – ‘‘E’’ and ‘‘G’’. In 1996 the first captive-reared individuals were introduced to restored habitats in the ‘‘W’’ and ‘‘C’’ parts of the metapopulation. Supplementation of the ‘‘W’’ and ‘‘G’’ parts of the metapopulation ceased in 1997 (Adamski and Witkowski, 1999a) (Fig. 2). In 1995, in order to obviate the potential effects of genetic erosion, it was decided to include in the breeding programme some
Fig. 2 – Intensity of captive- reared support of the wild population.
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individuals from the nearest population of the same subspecies, obtained from Haligowskich Skaly (Slovakia). After this measure, in 1996 three breeding lines were obtained: Polish, Slovak and mixed (Witkowski and Adamski, 1996; Adamski and Witkowski, 1999a). In the beginning of the project the idea of artificially increasing food plant abundance was considered. However, abundance studies of the stonecrop (Sedum maximum) (Witkowski et al., 1992) indicated that this perennial plant was still quite abundant at the sites, including highly altered ones. These activities were coupled with studies aimed at monitoring the effect of the activities and solving problems appearing during their implementation. After 12 years of intensive work, the data gathered to date warrant an assessment of whether the restored metapopulation is stable and can survive without permanent support from captive-reared individuals. The Pieniny metapopulation, restored as a result of preparatory activities and introduction, can be divided in three large functional population patches (Fig. 2). The eastern part of the metapopulation (E), inhabiting the Trzy Korony massif and Sobczanski gorge. The area has some nine screes of various sizes accompanied by xerothermic grassland. The central part (C), including the xerothermic grasslandcovered slopes of Gorczynski gorge and similar habitats of Nowa Go´ra, Macelowa Go´ra and the Cyrlowa Skałka hills. The western assemblage (W) of demes on fairly extensive and compact screes located on the Ubszar, Długa Grapa, Flaki and Cisowiec hills, and the slopes around Czorsztyn castle. The restored metapopulation occupies yet another single site on a large a large area of stonedebris called Miedzy Grabczychami (G); despite it’s proximity to the Trzy Korony massif (E) (Fig. 1), it is evidently isolated from it by the relief of the area. Currently the area suitable for the Apollo butterfly covers about 40 ha, under the management of National Park staff.
4.
Methods
The population numbers were determined by marking and recapturing imagines (Witkowski et al., 1997). During the period when the imagines were present, each of the potential sites of Apollo butterflies were visited twice a week for 1– 3 h, depending on site size. During these visits, all observed Apollo butterflies were captured and the following data were registered for each catch: (1) The date and time of capture. (2) The code of the individual. At capture each individual was marked with a unique code allowing its unambiguous identification. The individuals obtained from breeding in captivity were marked before their release to sites. (3) The sex of the individual, and in females the presence or absence of the sphragis, a structure formed by the male over the femaletßs abdomen to prevent her from remating and displacing his sperm.
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3
(4) The site of capture, and for larger sites also the approximate location within the site. The site where capture occurred, and in larger sites also the approximate location within the site. The collected data were used to estimate the population numbers of the Pieniny metapopulation through the Jolly method, using the Jolly software package (Pollock et al., 1990). This method, based on the ‘‘open population’’ was checked because of significant migration rate within the population and the emergence of newly hatched individuals during the sampling period; for this reason, method B was used. The total population abundance in the whole sampling period was extrapolated from the estimated population abundance in a given sampling (Seber, 1982; Pollock et al., 1990). The marking of individuals also revealed cases of migration between sites. To determine the stability of the restored population, a modified net reproduction rate coefficient (Krebs, 1994) was calculated, taking into account the presence of captive-bred individuals on the site Et ¼
Wtþ1 Wt þ Ct
ð1Þ
where Et represents the yearly effectiveness of restoration activity, Wt the number of wild individuals in the population in year t, Wt+1 the abundance of the wild population in the next year, and Ct the number of captive-reared individuals released to the site in year t. The coefficient was calculated for the whole population as well as for each of the four parts distinguished within it. In each year, a migration coefficient was determined for the metapopulation, indicating the fraction of marked individuals that undertook migration outside their original habitat patch. The coefficient was calculated separately for short-distance (within metapopulation centres) and long-distance migration (between these centres). To assess the impact of introducing captive-reared individuals into the population, regression analysis was performed to determine the effects of wild population size and introduction intensity on reproduction rate in a given part of the metapopulation, as well as on population number in the following year.
5.
Results
During the period in which the reintroduction measures were carried out, the range of the Pieniny metapopulation of the Apollo butterfly expanded from the single subpopulation in the Trzy Korony massif to more than a dozen subpopulations living at almost all the major sites potentially suitable for this species within the Pieniny National Park (Fig. 3). The estimated total number of the Pieniny metapopulation increased from a mere 30 individuals in 1991 to over 1200 in 2002 (Fig. 4a), with the greatest increase occurring in the Trzy Korony massif, where ca. 50% of the metapopulation live (Fig. 4b). The values for short-distance dispersion within metapopulation centres calculated since 1996 have fluctuated between 30% and 40% of the individuals found (Table 1). The
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Fig. 3 – Expansion of the metapopulation range during the recovery process.
long-distance migration coefficient increased initially, reaching a maximum 4.7% in 1999, and then declined to 2% in 2002, but the ratios of long-distance migrants between particular non-zero years did not differ significantly (v2 = 9.267, df = 8, p = 0.3206) (Table 1). In 1996, all individuals undertaking migration were those reared in captivity from either the Slovak or the mixed line. The sex ratio of the migrants did not differ from those of all marked specimens (v2 = 226, df = 1, p = 0.1448). The value of the reintroduction effectiveness index for the whole metapopulation exceeded 1 only in 1992 and 1997. The values of these indices for particular metapopulation centres are given in Table 2. Regression analysis indicates that the number of wild individuals emerging at a site in a given year was closely related to the number of a given subpopulation in the previous year (N = 48, betawild = 0.431, pwild < 0.0001 SEbetawild = 0.042), whereas the effect of captive-bred individuals introduced to the site in the previous year was not significant (N = 48, betacaptive = 0.084, pcaptive = 0.1366 SEbetacaptive = 0.055). Since population abundance at the sites often distinctly differed between years, the data were divided into two groups by the median of the number of individuals observed at the given site. When the number of observed individuals was lower than the median calculated for the site, population abundance in that year was positively related to the same value in the previous year (N = 29, betawild = 0.790, pwild < 0.0001, SEbetawild = 0.117, betacaptive = 0.115, pcaptive = 0.0228, SEbetacaptive = 0.047). When the population number at the site was more than the median, both mentioned parameters were also significantly correlated, but the relation between population abundance and the number of captive-reared individuals introduced into the field in the previous year was negative (N = 19, betawild = 0.434, pwild < 0.0001, SEbetawild = 0.047, betacaptive = 0.286, pcaptive = 0.0363, SEbetacaptive = 0.124).
6.
Fig. 4 – Changes in population abundance during the reintroduction process: a — whole metapopulation 1 – number of marked individuals, 2 – estimated population size, 3 – +/- standard error of the estimated population size, b — particular metapopulation centers.
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Discussion
As an important flagship species, the Apollo butterfly has been the object of successful population recovery projects. Some projects were aimed at expanding an existing population (Dolek and Geyer, 2002; Dankova´, 1997). One reintroduction project led to the restoration of an extinct population (Luka´sˇek, 2000). An increase in the spatial range of a metapopulation and increased abundance of wild populations have been routinely taken as proof of the effectiveness of a reintroduction programme (Dolek and Geyer, 2000; Geyer and Dolek, 1995; Witkowski et al., 1997; Adamski and Witkowski, 1999a). In the analysed case, close scrutiny of the effectiveness coefficients (Table 1) yields less optimistic conclusions. As mentioned earlier, the effectiveness coefficient calculated as given above is the net population reproduction rate determined for a given year and taking into account captive-reared individuals (Krebs, 1994) In these circumstances, in order to be deemed stable, the coefficient for a population should be at least equal to 1. Populations with a lower rate of reproduction over a period of many seasons are so-called sink populations, whose survival depends upon an uninterrupted inflow of individuals from
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Table 1 – Dispersive activity of butterflies as, percentages of individuals Year
Dispersion inside the metapopualtion centers E
1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
C
0.0 2.2 7.2 28.6 31.1 35.5 32.5 43.3 35.7 34.1 34.0 33.233
– – – – 32.4 34.5 32.4 40.6 37.2 32.6 31.7 35.2
W – – – – 32.1 33.7 31.6 40.5 37.0 36.6 31.5 31.4
Dispersion between the centers
G
Total
0.0 2.0 5.1 26.2 0.0 33.3 29.6 36.4 28.0 16.7 27.3 29.2
0.0 2.0 6.3 27.1 31.4 34.3 32.1 41.5 36.2 34.1 32.6 33.2
0 0 0 1.2 2.4 2.1 3.9 4.7 3.8 2.9 2.1 2.5
Table 2 – Effectiveness of the restoration programme, calculated by year
1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003
E
C
W
G
Total
1.69 0.93 1.31 0.59 0.85 1.42 1.76 1.15 1.12 1.06 0.92 1.14
– – – – – 1.07 1.01 0.28 0.36 0.53 0.68 1.24
– – – – – 1.06 0.20 0.74 0.44 0.55 1.31 0.51
1.04 0.46 0.05 0.32 0.03 3.64 1.80 0.42 2.25 0.23 1.89 0.51
1.67 0.84 0.13 0.48 0.36 1.23 0.84 0.69 0.77 0.78 0.96 0.92
source populations (Pulliam, 1988; Pulliam and Daniellson, 1991), in this case the captive-bredpopulation. Analyses of the effectiveness coefficients for particular metapopulation centres give less pessimistic conclusions. In the Pieniny National Park the Apollo butterfly forms a metapopulation, so not all its parts need have the characteristics of source subpopulations (Pulliam and Daniellson, 1991). Moreover, the number of individuals in sink populations may even markedly exceed the number in the source population (Watkinson and Sutherland, 1995). In the Pieniny metapopulation of the Apollo butterfly, site E may definitely be recognized as a metapopulation source. It is inhabited by the strongest and most stable of the Pieniny Apollo butterfly subpopulations. Since 1996 the net reproductive rate at site E has either exceeded or been only slightly below 1 (Table 1). In other parts of the metapopulation where results were calculated, major year-to-year fluctuations were shown, particularly in the small subpopulation G. This low stability, possibly the result of low numbers of individuals in that population, coupled with its peripheral location and its isolation, means that the role of G in the functioning of the whole metapopulation is fairly minor. For the practice of conservation, the relation between population size and the extent of captive-bred supply in previous years is an important one. Our results show that for a relatively small population the effect of captive-bred supply
is positive, whereas in abundant subpopulations the opposite is true. Thus it can be suggested that introducing a large number of captive-reared individuals to a site may result in local overcrowding of the population. If, as a result, the combined numbers of wild and captive-reared populations at a given site approach the carrying capacity, one can expect a lower rate of increase due to higher migration (Bujalska and Gru¨m, 1994) or lower production of fertile offspring (Krebs, 1994). In the present case it may be assumed that the high number of imagines translates to a higher number of eggs laid, and thence a high number of caterpillars emerging at the site in the next year. Studies completed to date regarded the abundance of stonecrop (Sedum maximum) to be the limiting factor for the discussed metapopulation (Witkowski et al., 1992, 1997). The emergence of high numbers of caterpillars foraging on this plant early in the vegetation season may lead to temporary erosion of the food supply. Our oversupply hypothesis is supported by the finding that the most stable subpopulation, E, is the place where the relative level of captive-reared supply was lowest. Under such circumstances, supplementing small populations with small groups of captive-reared individuals should be regarded as the most effective strategy. Analysis of the movements of individuals between and within locations indicates that the suggested division of the Pieniny metapopulation into three distinct centres and one somewhat isolated site matches its actual dynamics. Within
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the main centres, the coefficient of exchange of individuals between restored habitat patches was very high; thus these areas should be treated, at least in part, as population patches in a greater metapopulation (Harrison, 1991; Harrison and Taylor, 1997). It might seem surprising that the individual exchange coefficients for all the metapopulation centres were similar, despite the much greater distances between the sites of the western centre. Straight-line distance, however, is only one of several factors affecting the probability of migration of individuals between sites (Hanski, 1997). In the case of the Apollo butterfly, the presence of open areas between sites enabling free dispersion of the species is at least equally important (Brommer and Fred, 1999). Studies of Parnassius smintheus describe the crucial role of habitat structure in the dispersion activity of the butterflies (Fownes and Roland, 2002; Matter et al., 2004). This structure involves not only the distribution of open areas but also the within-meadow structure (Ross et al., 2005). The lack of suitable migration corridors around site G is the factor behind the low level of migration among local individuals, as well as the low number of butterflies from other sites reaching subpopulation G. Interestingly, in the studied population the migration ratios of the males and females did not differ, in contrast to other results and theoretical predictions (Matter and Roland, 2002). Unfortunately the data available for the Pieniny population are insufficient to explain this phenomenon. The exchange of a few percent of the individuals between the main metapopulation centres seems enough to protect the metapopulation against genetic erosion (Gilpin, 1996), but it is not certain whether it is high enough to bring about spontaneous recovery of a subpopulation if one of the main centres becomes extinct. At the outset of the recovery programme, the Pieniny population of the Apollo butterfly had an extraordinarily low dispersion coefficient, and raising it was one of the priorities for the project (Witkowski and Adamski, 1996; Adamski and Witkowski, 1999a). It seems that the dispersion coefficient is boosted mainly by introducing into breeding some individuals from another less isolated population (Witkowski and Adamski l.c). The drop in longdistance migration noted in the last three years is most likely an artefact resulting from the fact that the probability of recapturing an individual decreases with increased population number (Seber, 1982; Turchin, 1998; Adamski, 2004). In most recovery projects for the Apollo butterfly, the key activity consists in maintaining or recovering suitable areas. In the Franconian Alps this activity also involved co-operation with mining enterprises located in this region (Dolek and Geyer, 2002). In the Pieniny Mts, introduction of pasture to habitats suitable for the Apollo butterfly is problematic because it may conflict with other conservation imperatives of Pieniny National Park. In such a case, the Apollo butterfly habitat is maintained through special activities of the National Park Service.
7.
Conclusions
It can be said that a functional metapopulation of the Apollo butterfly has been successfully restored in the Polish part of the Pieniny Mts. Since the supply of captive-reared individu-
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als is continuous, however, it is impossible to determine unambiguously whether the metapopulation would function without this kind of support. Undoubtedly the population patch of the Trzy Korony massif (metapopulation centre E) can be regarded as a stable part of the metapopulation. Its net reproduction rate throughout the last six years has exceeded 1 or fallen only slightly below it (Table 2). A coefficient for the exchange of individuals between metapopulation centres amounting to a few percent is too low to significantly affect the growth rate estimate for any particular metapopulation centre. The possibility that the stability of population patch E may be the result of an influx of migrants from other sites may thus be excluded. Under these circumstances, this local population patch may be regarded as a metapopulation source (Pulliam, 1988). Two other centres seem to have the characteristics of sink populations, but their actual status can only be determined after the supply of captive-reared individuals ceases. Also unclear is the status of the single site at G; significant fluctuations of population number occur there, but owing to its peripheral position, its impact on other subpopulations seems very limited. Nevertheless, due to its peripheral position, this population could function as a stepping stone between the population in the Pieniny National Park and the more numerous population at Haligovske Hory in Slovakia.
Acknowledgments The authors would like to thank Andrzej Kosior and Piotr Płonka for co-working on the project of Apollo butterfly recovery. Special thanks are due to the staff of the Pieniny National Park and PIENAP, particularly to Michał Sokołowski, Bogusław Kozik, Tadeusz Oles´, Sˇtefan Danko and Katarı´na Zˇlkovanova´. Authors are also grateful Polish and Slovak ministries of environment for enabling us exchange of individuals between captive breadings (Slovak CITES export permission No. 00045/95, Polish CITES import permission No. 4772/96/95).
R E F E R E N C E S
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