Experimental reintroductions of endangered plant species in their natural habitats in Spain

EXPERIMENTAL R E I N T R O D U C T I O N S OF E N D A N G E R E D PLANT SPECIES IN THEIR N A T U R A L HABITATS IN SPAIN

H. SAINZ-OLLEROt& J. E. HERNANDEZ-BERMFJO~ Departamento de Biologiay Fisiologia Vegetal, E.T.S. de lngenieros Agr6nomos, Universidad Polit~cnicade Madrid, Madrid 3, Spain

ABSTRACT The large number of Span&h endemic plants and the extent to which they may be endangered are analysed and compared with the equivalent situation in other European countries. The reasons for their threatened status are examined, and the application of different methods of protection is discussed. The protection method used is complementary to the establishment and management of" germ-plasm banks and is based on the reintroduction of living material into the areas where the species originally grew. The material for reintroductions is obtained by multiplication of germ-plasm preserved in a seed-bank. This method has been put into practice with several Iberian endangered endemics such as Vella pseudocytisus L., Silene hifacensis Rouy, Hutera rupestris Porta, Antirrhinum charidemi Lange and Artemisia granatensis Boiss. The initial problems faced in the reintroductions and the preliminary results obtained are discussed.

THE SPANISH FLORA: RICHNESSAND RISK There are many reasons for the high abundance of species in the Spanish flora: the geographical position of the Iberian Peninsula, in the Mediterranean area, as a bridge between Africa and Europe; the east-west direction of its predominant mountain ranges form powerful biogeographical barriers; the variety of its climates; its position in relation to the quaternary glaciations; the location and ecological peculiarities of the Spanish archipelagos (Balearic and Canary Islands). If we refer t Present address: Departamento de Botanica, Universidad Polit6cnica de Madrid, Madrid 3, Spain. :~Present address: Cfitedra de BotAnica Agricola, E.T.S. de Ingenieros Agr6nomos, Universidad de C6rdoba, Spain.

195 Biol. Conserv. 0006-3207/79/0016-0195/$02.25 © Applied Science Publishers Ltd, England, 1979 Printed in Great Britain

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exclusively to Peninsular Spain and the Balearic Islands, with the major exclusion of the Canary Islands, the above statements are still valid. If the number of vascular plant species in Europe is estimated at 12,000, approximately half of them grow (in many cases exclusively) in the Iberian Peninsula or the Balearic Islands. This valuable genetic heritage is seriously threatened by new developments, generating a continuous genetic erosion with the result that in recent decades the total extinction of several species from their natural habitats, such as Lysimachia minoricensis Rodr., has been observed; some others are nearly extinct (e.g. Silene hifacensis Rouy ex Willk., Origanumpaui Martinez, Diplotaxis siettiana Maire and A rtemisia granatensis Boiss), and a large list of species is more or less directly and severely threatened. The International Union for the Conservation of Nature and Natural Resources has recently (1976) compiled a list of rare and threatened species for the various European countries. We had the opportunity of collaborating in the preparation of the part relative to Spain. Figure 1 is based on the numerical data

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E n d e m i s m o f E u r o p e a n floras in relation to coefficient o f extinction risk, based o n data in I U C N (1976).

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given in this report; the logarithm of the threatening coefficient of 'extinction risk' has been calculated from the ordinates by the following expression: (3x Ex + 2 x E + V + R + T)/104km 2 where E x stands for the number of species recently extinct, E the imminently threatened species, V the number of the vulnerable species, R rare species, and T endangered species (according to Waiters, 1976). From Fig. 1, based on the above formula, it can be seen that the northern countries (Sweden, Norway, USSR) remain isolated as the less endemic and endangered area; in a middle position are the Central European countries, and in a high position of endemicism and risk, the countries of the Mediterranean peninsulas with the Iberian Peninsula in first place; and finally, the Mediterranean Islands and archipelagos. The Balearics head this final group, followed by Greece, which is included here mainly because of its strong maritime character. Belgium, Finland, Hungary, Luxemburg, Holland and Switzerland are not included, as the number of endemics or of threatened endemic species is nil. However, there are quantitative differences in the classification criteria for threatened or endangered species according to the opinion of the various groups of scientists who prepared the IUCN reports in each country. The Iberian Peninsula report appears to be amongst the least alarmist. It includes a total of 482 endemic species for peninsular Spain, 50 for the Balearic Islands and 62 for Portugal. However, a recent report (Sainz-Ollero & Hernandez-Bermejo, in preparation) on dicotyledonous species endemic to the Peninsula and the Balearic Islands shows a total of nearly 1100 endemic species and subspecies. There are various reasons for the more conservative estimate of the IUCN. First, endemic species growing on both sides of the Pyrenees have not been taken into consideration, secondly, endemic species found both in Portugal and Spain have not been included nor have species endemic to the Peninsula and the Balearic Islands. Endemics at the subspecies level have not been taken into account. For these reasons we could calculate the number of endemics for the Iberian Peninsula and the Balearic Islands together by multiplying by a coefficient of 2.5 the number of such endemics listed by the IUCN. This would provide a similar result to the estimation of extinction risks. CAUSES OF THREAT AND EXTINCTION

In general terms, the fundamental cause for the threatened state of the Iberian and Balearic flora is the long history of over-exploitation of natural resources both by forestry and agriculture, and also the enormous growth of industry, urbanisation and establishment of recreation areas. In particular, the vulnerable flora of narrow endemics has been threatened by: (a) Abuses in the exploitation of particular species, e.g. Hutera rupestris, once used as mustard (condiment), and Artemisia granatensis used as an infusion, always obtained from natural populations.

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(b) Excessive collecting of extremely rare species or of very localised populations, e.g. Silene hifacensis, which is now extinct on the Pefi6n de Calpe (but not elsewhere), and Lysimachia minoricensis, which has been exterminated on its only known statiOn. (c) Habitat'change, particularly through building operations, which can cause the extinction of a narrow endemic in a matter of a few days. For example, Vella pseudocytisusformerly grew in areas that are now devoted to agriculture in the basin of the Tajus river, and Senecio aiboranicus, Dipiotaxis siettiana and Anacyclus albonarensis: are threatened by the transformation of the Aiboran Islands into a military base. (d) Indirect effects of the growing pressures of tourism, urbanisation and agriculture; such as sheep-herding, which can lead to eventual extinction of rare species, or those growing in localised areas, e.g. Papaver suaveolens, Aquilegia cazorlensis, Naufraga balearica and Antirrhinum charidemi.

PROTECTION SYSTEMS

Possible ways of protecting threatened plant species are: (a) Conservation of their habitat, by creation of National or Local Parks, or even Ecological Reserves (see criteria and application for Spain in Hernandez-Bermejo and Sainz-Ollero, 1977). This course at first seems the most desirable, but has several difficulties: no country can dedicate more than a small part of its land to this purpose, and this is particularly true of those with a high population density. The percentage of surface area dedicated to Parks and Reserves in Spain is still very low in comparison with other developed countries, and it is even lower when one considers the value of the flora and the threats that exist. In addition, it is usually very difficult to restore sufficiently large populations of threatened species without any human influence. (b) To promote a social conscience regarding endangered species a n d the problems of conserving them. Some of the responsibility for protection could be given to associations of nature conservation, where these exist (Waiters, 1976). This, can, however, only be successful in mature and democratic countries, in which the level of popular participation in the management and conservation of the resources of the community is very high. Though Spanish society has much improved in this sense during recent years, we are still far from the point where this protection system could be trusted. (c) Botanic gardens orientated essentially towards the conservation of native species and those which are rare or threatened. This is a necessary course of action in direct relationship to (b), due to the cultural role that these gardens fulfil. In Spain, the Jardin Canario, in the Island of Gran Canaria, is a good example. (d) Cultivation of endangered species in private gardens and collections. There

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seems no doubt that this is a useful means of protection, particularly if there is coordination between those concerned and scientific bodies. (e) Gene banks are complementary to the methods mentioned above (GomezCampo, 1972; Thompson, 1974), as a great quantity of seeds, spores or pr0pagules of many species can be stored in a very small space, in a more or less artificial atmosphere (cold, anaerobic and dry conditions) and assuring the viability of these seeds during many years of storage. In Spain there is a bank of endemic species at the Departamento d e Biologia of the ETS de Ingenieros Agron6nomos de Madrid (Gomez-Campo & Hernandez-Bermejo, 1975-76).

MATERIALS AND METHODS

We have been working for three years on a more direct strategy towards the conservation of endangered species. This consists of the reintroduction of endangered species in their natural habitats, where they have become extinct. The small populations for these reintroductions were obtained by using seeds and propagules conserved at the ETS germ-plasm bank. Similar experiments have been made by de Bolos (1962) in Menorca, who unsuccessfully introduced a small population of Lysimachia rninoricensis and by Crompton (1975, and pers. comm.) in England, who has been working on several rare species including the British endemic Scleranthus perennis L. subsp, prostratus P.D. Sell. Once the danger situation has been detected and there is sufficient knowledge on the original habitat and the factors limiting the species, material is made available from a germ-plasm bank (Gomez-Campo & Hernandez-Bermejo, 1975-76), and the following process carried out.

Species used Greenhouse sowing. The germination problems of the seeds used must be previously known and resolved. Treatments with light, alternative temperatures, cold stratifications, break-down of layers, or those with gibberellics may be used. At most, 4 or 5 seeds are sown per pot (each about 10 cm diameter) and f~om 20-50 pots depending on species. Usually, the temperatures for germination and growth were between 20 o and 25 °C. Sowing on sterilised soil is recommended, and also the use of mist spraying at least during the initial stages. Transplanting. Transplanting is carried out by isolating seedlings as they grow and making sure that they do not become too large (for ease of transport) and that their root systems have fully utilised the volume of soil in the pot. Transport. Plants three months old (annuals), six months (biennials) or more than six months (old perennials) are carried on trays to the area of reintroduction, and afterwards on trays fitted to knapsacks on the backs of the reintroduction team

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members, due to the very wild and steep character of the sites. In some cases more sophisticated systems of climbing are necessary to reach the natural habitats. Planting. Much better results have been obtained from reintroduction in autumn and early winter. Plants used to frequent watering during their early stages in greenhouses have much greater difficulties if they are planted during the hotter periods: After excavating the holes, the neighbouring bushes are removed, in order to avoid competition during the first few months, and these uprooted bushes are used to camouflage the young introduced plants. Every plant is watered immediatelywith half to one litre of water, in order to facilitate survival and initial rooting. The number of plants in each reintroduction has been between 40 and 100. Though the size of these new populations might seem too small, it must be realised that the objective of these experiments was to plan a pilot scheme for the reintroduction of extinct species and making use of a very limited number of seeds. Recording. The sites are visited once or twice a year and compared with photographs and maps made at the time of the planting. Notes are taken of the conditions and size of the populations. Five Iberian Peninsula endemic species, which were in danger as a result of reduced area of distribution, were chosen (according to our own criteria and those of the IUCN, 1976). One of the five species appears to be extinct in the Peninsula but still survives in small populations on the Balearic Islands. Seed for all the species was available at the plant germ-plasm bank of the Universidad Polit6cnica in Madrid. The species used were: two Cruciferae (Vella pseudocytisus L. and Hutera rupestris P. Porta), one Cariophyllaceae (Silene hifacensis Rouy), one Compositae (Artemisia granatensis Boiss), and one Scrophulariaceae (Antirrhinum charidemi Lange).

PRELIMINARY RESULTS

The sites of reintroductions and other species being studied are shown in Fig. 2. Vellapseudocytisus L. belongs to the tribe Brassiceae (Cruciferae), which has a large number of endemic species in the west Mediterranean area. It is a shrub of between 50-70 cm, branched from its base, with many small leaves (2 cm) covered with many erect hairs on both sides, which does not, however, deter goats and even some rodents and rabbits from feeding on it. It is an old taxon, of'palaeoendemic' origin (according to Favarger & Contandriopulos, 1961), with a surviving relict distribution. The greater part of the population is located in the neighbourhood of Aranjuez, to the south of the province of Madrid, at Sotomayor farm, owned by the Patrimonio Nacional and closed to the public. Gomez-Campo, in IUCN (1977) estimated a

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population of 2000-3000 individuals. It is very plentiful on this farm, which is on an area of relatively deep soil, derived from gypsum, in valleys that run from the Meseta down the Tajus river in a S-N direction. It does not grow on very eroded slopes, in which the influence of gypsum is very strong, but on areas of accumulated deposit and on the small debris cones of torrents, where it can find a greater soil depth. It shares the same habitat with Retama sphaerocarpa and Asphodelus cerasiferus. It is interesting to note the vigour it has shown in areas abandoned 5 or 6 years ago, where cereals were once grown. Records and herbarium specimens exist from an area to the NE of the province of Granada (on a ecological scale similar to the Castellian-Manchega region-continental climate, xerophile, limey gypsum soil), but searches have met with no success and it can be considered extinct here. This is due to extensive agriculture and reafforestation (Gomez-Campo in IUCN, 1977). A population of about 100-150 individuals occurs in the province of Teruel (at Villalba Baja towards Alfambra). This is the glabrous var. badalii (Pau) Heywood, which only shows some marginal hairs on its leaves. Two different locations, upriver from Aranjuez (in the Tajus valley) were chosen for the reintroduction. One of them, near the hermitage of Castellar, in the Villanueva de Santiago district, was chosen for its natural habitat conditions (thin

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soil, derived from gypsum materials). The other one is situated at km 4 of the C-274 road, from Fuentidueha de Tajo to Extremera, on the left bank of the Tajus river, and was chosen to study how far the growth of this species is limited by soil conditions. Soil in this location is a rendzina, with no traces of gypsum, on pontiense limestones and with plenty of siliceous boulders on the surface. Small populations of 6-months-old Vella pseudocytisus were planted in both localities. Evidence of rabbit grazing was observed but localities without this disturbance could not be found. A second introduction was made at the first location, when material became available. Several individuals were planted in soil that showed a high proportion of gypsum. All plants are now (1978) in good condition, some branching and hardening of stems can be seen, though upward growth has been very limited. At the second location, almost all the plants disappeared, only one individual remaining after one year and a half in a degraded steppe grassland field. Results from the use of'jiffy' pots have proved to be very negative. They give rise to difficulties in rooting and seem in some way to attract rabbits, mice and moles, which sometimes uproot the pots, probably attracted by the smell of the peat or by the greater moisture that this soil maintains, due to a higher organic matter content. Hutera rupestris P. Porta belongs, as the latter species, to the tribe Brassiceae (Cruciferae). It is a biennial, erect species, 60-100cm high, with lyre-shaped pinnatifid and lobate leaves 10-20cm long, which are hairy when young. Its flowers are pale yellow and dark veined, on long racemes. The fruit is born on silicules, with two segments of 2-6 and 12-20mm respectively and, 4 to 7 seeds in each segment. It is a recent taxon, probably, formed when original populations invaded calcareous cliffs, on the Sierra de Alcaraz, to the extreme east of Sierra Morena and, where the soil is essentially siliceous (Gomez-Campo, in IUCN, 1977). It grows in fissures on limestone cliffs and rocks, in only one locality, at la Molata, on the Sierra de Alcaraz in the province of Albacete, at altitudes from 1040 to 1120 m. Occasionally, it can also be found on some nearby slopes, rather eroded and eutrophicated by cattle. It grows with Sanguisorba ancistroides, Sarcocapnos baetica and with some other species from the surrounding shrubs. The local climax is that of an evergreen oak forest. Many Hutera individuals are unable to produce fruit, cattle damage to'groups of leaves being frequently observed. The population, which in 1973 was estimated at between 1050-1100 mature plants, seems to have been reduced to 500-700 individuals in 1975 (Gomez-Campo, in IUCN, 1977). The reasons for this decline are uncertain, but it is clear that this species is in danger, both from collectors and by intensive grazing. In 1973 seed was scattered in a similar locality nearby (Vianos), without any success. Grazing in this area is extremely intensive and, consequently, it is very difficult to find favourable areas. For this reason this site was discarded as a possible reintroduction area. Three sites on the Sierra de Alcaraz were chosen for this:

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(1) Rocky cliffs near to la Mesta village (near la Molata), with an altitude and orientation similar to that of the original population. (2) South-east face of the Almenara mountain (1650 m high). This locality is much colder than the original one and 550 m higher. The vegetation is oromediterranean with: Draba hispanica, Globularia spinosa, Cerastium boissieri. (3) Los Chorros, at the source of the Mundo river, in a P. nigra forest. Fifteen mature plants were placed in each of these three localities. The greatest success was attained at the first, in which grazing does not seem to take place. The plants did not flower during the first year. At the second and third localities half of the population did not grow but some of the mature plants flowered and fruited, probably as a result of the especially hard conditions. The movement of scree in the third area may have been responsible for the failure of those individuals which had not been placed in rock fissures. Silene hifacensis Rouy ex Willk is a species similar to Silene italica (L.) Pers., which is widely distributed all over Europe. It grows 40-100cm high and is a stout plant, with a woody stock and lanceolate leaves; its loose inflorescences have red or purple flowers with an eglandular calyx. The capsule is 10 mm longer than the carpophore. Its systematic position is not clear, at least, in relation to Silene mollissima, S. cintrana Rothm. (Sierra de Cintra) and S. rothmaleri (Cabo de San Vicente), species which show many similarities to Silene hifacensis. It is probably a squizoendemic, derived from a slow and progressive differentiation. It is endemic to the Island of Ibiza (Cala Aubarca) and Espartar--both in the Balearic Islands--as well as to the Cabo de San Antonio and the Pefibn de Ifach, both in the province of Alicante on the Spanish mainland. It seems to have disappeared from these two last localities, and may be extinct. A meticulous search for it at the Pefibn de Ifach was unsuccessful, but it nevertheless would seem prudent not to make any definite statement on this, because of the especial characteristics of the area, which have several virtually inaccessible cliffs. It grows in fissures in limestone cliffs near the sea. During our visits to the Pefibn de Ifach, a very high rabbit density was observed; this may have had an adverse effect on the development of the species. On cliffs in the Pefibn de Ifach Scabiosa saxatilis, Antirrhinum barrelieri, Rhamnus lycioides (var. rupicola), Biscutella valentina and Hippocrepis valentina, also occur. The experimental reintroduction in the Pefi6n de Ifach was made with mature plants, grown from seeds collected in Cala Aubarca. Insular material was preferred, though some small differences can exist between the populations of the Balearic Islands and Pefi6n de Ifach. A total of 40 individuals was introduced, at two stages, with an interval of about 1 year between them. Data are only available regarding the first reintroduction. Many of the mature plants were damaged possibly both because of the effect of the high density of rabbits (plants grazed, a lot of excreta), and the use of jiffy pots. The jiffy system was

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therefore abandoned for the second introduction, and the plants used were older and more developed. These were located on two limestone cliffs, about 200 m above sea level, facing north and using rock fissures. A rtemisia granatensis Boiss. (Royal artemisia from Sierra Nevada), belongs to the tribe Heleniae Bentham, of the subfamily Asteroideae (Compositae). It is a small perennial bush with a very well developed root system which grows deeply in the rocky soil where it usually lives. Its leaves are deeply lobed and covered by dense hairs, which give them a silvery appearance. Florets occur in small flower-heads, at the tip of short peduncles, with an involucre formed by two or three rows of obtuse, hairy and dark rimmed bracts. The mature plant has a pleasant fragrance. It is endemic to Sierra Nevada and grows in screes and rock fissures or in stony places, near the summits of the central area of these mountains. It is beneath the snow nearly all the year, which protects it from severe temperatures and without which it could not survive. Infusions of the plant are drunk for its digestive properties, and it has therefore been very much collected for sale. Only flower-heads should b e collected, as with other artemisias, but collectors pull up the plant by the roots in order to get a bigger profit, since it is sold by weight. At present it is seriously endangered. Only a few very scattered individuals survive in virtually inaccessible places. The botanists who visited the Sierra Nevada in the middle of the last century wrote about this Artemisia as a frequent and plentiful species in the area. They do not record any precise localities but already refer to its medicinal properties and to intensive collecting. Rau, in as early as 1909, warned of its future extinction (in Font Quer, 1962), 'due to the war that artemisia collectors have declared on it', and proposed its controlled cultivation as the only measure to obtain effective conservation. This method would supply the trade demand and, at the same time, the pressure that artemisia collectors made upon the few plants remaining, would have been smaller. Two small, but not natural, populations occur, quite well preserved and guarded by Mr A. Zayas, manager of the University shelter. One of them is located in what now remains of an old Botanic Garden, which should be reorganised; and the other one is located at the meterorological station, in the surroundings of this shelter. Both populations are vigorous and, for the present, will provide sufficient seed for the preservation of this species. The first population includes about 80 individuals and there are 40 in the second one. Artemisia granatensis Boiss grows well in greenhouses, but does not flower and partially looses its flavour. Two localities at Sierra Nevada were chosen for the introduction of 43 individuals, one of them at the south face of the Mulhacen mountain (2.950m high), and the second one at Borreguiles (2.750 m high). The plants were placed on schists in both cases and the introductions were made at the end of spring.

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The first locality is away from the usual mountaineering and ski routes and even out of the way of collectors. This is not so for the second, which is near to a ski lift-the only thing protecting this population from collectors is the fact that they do not know there is any artemisia there. Data regarding the population at Borreguiles are available for one year after the introduction. The plants had survived the winter, some lignification has been observed, as well as a 30 ~ mortality, which cannot be considered excessive. Antirrhinum chariderni Lange (Scrophulariaceae) is a small, procumbent bush, woody, very branched, with shoots 30-40cm high. The shoots and leaves are eglandular-puberulent, and the calyx and corolla are glandular-pubescent. The leaves (10-25 x 4 - 8 m m ) are elliptical oblong. The rosette of 18-25mm is sometimes white, with red veins and a yellow throat. The capsule (8-9 mm) is subglobose. It is endemic to the 'Sierra del Cabo de Gata' (Almeria province), where it lives on volcanic rocks, between 100 and 350 m above sea level, in an area lashed by the wind throughout the year. It usually lives in fissures and does not show a clear preference for orientation. However, it is frequently found in the valleys that run down to the sea in the area of the lighthouse. Most of the bushes are apparently grazed. A few flocks of goats still live there, although the area has been abandoned by most of its inhabitants. A few damaged individuals have been observed surviving in this situation for some years. The population numbers between 500 and 1000 individuals in a 10 km 2 area. (A very wide search of the area was made in October 1977.) An acceptable level of regeneration was observed, in spite of the small size of the population; thus, it could be considered vulnerable more than endangered, provided its habitat survives. Some of the more important plants found with Antirrhinum were: Periploca

laevigata, Chamaerops humilis, Opuntia ficus-indica, Lobularia maritima, Ziziphus lotus, Lycium intrincatum. An introduction of 40 individuals has been made, in three localities nearby. These are concerned more with establishing a viable population than with extending the range. Two of them were located near the sea in the area where A. charidemi grows and the third a little further from the maritime influence, in a zone nearby.

Other species under consideration Work on other endangered species has also been undertaken, first by establishing some small populations in greenhouses. The endemic flora of the Balearic Islands is under a high degree of threat (there are 50 species endemic just to these Islands and at least ten of them are seriously endangered). This was the reason for special emergency work, in order to draw attention to the more endangered species in the archipelago. Naufraga balearica Constance & Cannon which is now being cultivated is a umbeliferous species, found in 1962, which grows in a small cliffy area, on the N E

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c o a s t o f Mallorca. A small p o p u l a t i o n o f L y s i m a c h i a m i n o r i c e n s i s Rodr. is an endemic k n o w n only f r o m one station in the island o f M e n o r c a . It is already extinct there a n d earlier f o r m e r reintroductions were not successful (A. de Bolos, 1962). Recently, the reintroduction o f this species in Sa Vall (Menorca) has been reattempted by L. Llorents and A. Llorents (L. Llorents, pcrs. comm.). Our individuals are derived f r o m the vegetative multiplication o f some plants m a d e available to us by M. L~souef (Brest), w h o grew them f r o m seeds in the Berlin D a h l e m Botanic G a r d e n , the only one that still has material available. W e have a small p o p u l a t i o n o f C y m b a l a r i a a e q u i t r i l o b a (viv.) A. Cheval subsp. f r a g i l i s (Rodr.) D. A. W e b b , also obtained f r o m individuals transferred to us by M. L~souef. It is endemic to the island o f M e n o r c a and, according to the opinion o f all the botanists w h o w o r k e d on these islands, is seriously threatened. Finally, we are trying to grow R a n u n c u l u s w e y l e r i Mar6s and Genista dorycniJblia F o n t Quer, b o t h having a very scattered distribution, respectively located in M a l l o r c a and Ibiza.

ACKNOWLEDGEMENTS W e would like to thank Prof. G 6 m e z - C a m p o for his suggestions during this w o r k and his c o m m e n t s on the draft o f this paper, and D r M. C o s t a T e n o r i o and D r M. Clemente Mufioz for their collaboration in field experiments.

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