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A study in endimism: Silene diclinis
A STUDY IN ENDEMISM: S I L E N E D I C L I N I S
HONOR C. PRENTICE The Botany School, Cambridge, Great Britain A BS TRA C T
Silene diclinis (Lag.) M. Lainz is a dioecious endemic with a highly restricted distribution in south-eastern Spain. The sparse literature on the plant is summarised before referring to the results of a study of S. diclinis in the wild. A new description of the species is presented and its taxonomic affinities discussed. Details of the flowering time of S. diclinis, possible pollinators and its population age structure are set out and its wild habitat described. Before examining the possible origin of the distribution of S. diclinis, an attempt is made to clarify the various classifications of endemism that have been widely used in the literature. It is considered that since these classifications are generally based on the supposed origins of endemics they do not foem a sound basis for the examination of evidence in individual cases. Types o f evidence that can be used to throw light on the history of individual endemics are examined and include evidence gained from experimental taxonomy, pollen and macrofossil analysis and ecological studies. Unfortunately, in the case of S. diclinis there is no direct evidence referring to its past. One hypothesis, based on present distribution and on a consideration of Mediterranean Cenozoic palaeoenvironments, is put forward tQ explain the present restriction of S. diclinis. Finally, the genetic situation in a restricted endemic population, the future of S. diclinis and conservation measures are discussed.
INTRODUCTION
The remarkably restricted dioecious Spanish endemic Silene diclinis (Lag.) M. Lainz (see Figs. 1 and 2) is a member of the section Elisanthe of the genus (Chater & Waiters, 1964), a European section which also contains the widespread species, S. alba (Mill.) E. H. L. Krause, S. dioica (L.) Clairv. and S. noctiflora L., and the less-restricted Balkan endemic, S. heuffelii So6. Waiters (1971) summarised the literature referring to S. diclinis. The plant was first described by Lagasca (1816), as Lychnis diclinis, growing: 'In montibus 15 Biol. Conserv. (10) (1976)--O Applied Science Publishers Ltd, England, 1976 Printed in Great Britain
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Fig. 1. S. diclinis (male).
Fig. 2.
S. diclinis (female).
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Setabi vicinis locis depressionibus in Valentii Regni.' Since Lagasca's work there has been little information collected on the species. A specimen at CGE (Cambridge University Herbarium), collected by E. Bourgeau in 1852, is labelled: 'Sierra de San Felipe de Xativa, Prov. de Valencia.' Both localities have been assumed to refer to the Sierra del Castillo, J~tiva, Prov. de Valencia. Plants have also been found at the Pla de Corral, Simat de Valdigna, Valencia, which is 25 km north-east of J~itiva (not south-east as given by Morisset & Bozman, 1969) by Professor E. M. Galiano (there is a specimen collected by Galiano in 1964 in CGE). In June 1974 a study of S. diclinis was made in its locus classicus. (A search of the Pla de Corral area was also made but it was not refound there.) Information was collected on the morphological variation, the habitat and species associated with S. dielinis with a view to providing a reliable set of data on the species which would also allow suggestions to be made about the cause of its present distribution and future protection.
DESCRIPTION OF THE SPECIES
The following description has been prepared from 21 male plants and 20 females (including, unfortunately, due to the time of year, only one flowering female) systematically examined in the field with details of seed morphology observed later under a low-power microscope in the laboratory where 30 seeds were scored. The description augments that in Chater & Walters (1964). Dioecious; perennial with short, thick stock and procumbent to ascending stems clothed with long, patent, soft, strongly flexuous eglandular hairs. Leaves pale yellowish-green with eglandular hairs on both surfaces, densest on the veins; glandular hairs occasional on margin. Basal leaves 3-13 cm sessile and spathulate; cauline leaves and bracts 2-9 cm sessile, spathulate, oblanceolate or oblong. Inflorescence a regular dichasial cyme with alar flowers. Pedicels strongly-deflexed in fruit ;. male 5-19 mm, female 3-5 ram. Calyx clothed with soft, flexuous hairs, often with sparse, short, straight, glandular hairs beneath; cylindrical in both sexes, becoming globose in fruiting females; male 9-19 mm and female 5-15 mm; nerves (9)-10-(11) in males and 20 in females; red pigment always present in males and seldom in females; teeth acute and shortly hairy. Corolla deep magenta; diameter, male 10-22 mm, female (single measurement) 19 mm (in cultivation male flowers are generally larger than female); coronal scales white with frilled margins; petals (4)-5, male emarginate, female emarginate to bifid (to less than ¼ of their length); arrangement often asymmetrical and in overlapping clumps; claw long, male 5-11 ram, female (single measurement) 14 mm, with two white, acute auricles. Stamens 10; anthers yellow; filaments hairless; pollen of 'S. dioica type' (see Birks, 1973, p. 230). Styles (3)-5 with long papillae. Carpophore very short. Capsule
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5-11 mm, globose; teeth (5, 7, 9)-10 deflexed when ripe, often splitting irregularly. Seeds pale to dark brown, 1.4-1.9 mm long, 1.2-1.5 mm wide; face convex; back rounded and 1.0-1"2 mm across; tubercles 240--270/~m, broadly conical; surface plates with stellate sutures. S. diclinis has more obvious affinities with section Elisanthe than with any of the other European sections of Silene. Nevertheless, it is a distinctive plant and differs from the other species of the section in many respects. Notable differences are its prostrate or ascending habit, its emarginate or shallowly-dissected (rather than bifid) petals and its small, globose capsule with its deflexed pedicel. Like all other members of the section, except S. noctiflora, it is dioecious, a rare feature in a restricted endemic. A herbarium specimen from the Sierra del Castillo has been deposited at CGE.
GENERAL BIOLOGY
In the second week of June 1974, nearly all the female plants of S. diclinis had ripe seed. In cultivation S. diclinis seed takes 4-5 weeks to mature after fertilisation and it seems reasonable to assume that the main flowering of the plant in the wild takes place in early May. The male individuals, as in S. alba and S. dioica, continue flowering after the females. In cultivation occasional plants, particularly males, will produce one or two flowers in the aatumn. Cultivated material starts to flower in March and continues until June. Individuals on the northern slopes of the Sierra flowered after those on the southern slopes. The leaves die back from their tips as flowering continues, are shrivelled in the summer and new leaves sprout in the autumn. S. diclinis has magenta, day-opening flowers with a barely-perceptible fragrance. Pollen is produced in aggregated lumps. From these features and from comparison with other species o f Silene, especially S. dioica, it seems likely that it is insectpollinated (see Baker, 1947). In the greenhouses at Cambridge I have seen S. diclinis visited by bumble bees, other bees and one moth (Plusia gamma). All the individuals possessed thick stocks and many appeared to be of considerable age when compared with material in cultivation. Individuals grown from seed in Cambridge in 1958 are still healthy. Copious seed was being produced in the wild population but no seedlings were found beneath the plants, although seeds were seen on the ground on a few occasions. It has not been possible, as yet, to make counts of the annual rings in the stocks and, in any case, such counts would have to be interpreted with caution in view o f the occurrence of anomalous secondary thickening in the Centrospermae. Wells & Barling (1971) have shown a similar age structure in populations of Pulsatilla vulgaris in the south of England, seedlings of that species being intolerant o f disturbance during establishment. As with Pulsatilla vulgaris, S. diclinis seeds showed high viability when grown in Cambridge but seedlings were easily killed by
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19
moving before they were properly established. Seedlings were also more sensitive to over-watering or droughting than the adult plants. In order to maintain a population of long-lived perennials, it would clearly not be necessary for many seedlings to survive each year. It is probable also, although the seeds do not appear to have a significant after-ripening requirement, that their germination may be dependent on autumn rain. Vegetative propagation by separation of ramets from the stock is easy in cultivation, and the mule ploughs may now play the role of propagators in the present habitat. Because of the incurved pedicel and the large size of the seeds, it is unlikely that dispersal is particularly efficient, although the solitary female plant to the west of the bulk of the population shows that seeds can be dispersed for some distance. The areas of the three sub-populations found (see below) were elongated perpendicular to the contours, which could be explained by the propagules falling downhill under gravity.
DISTRIBUTIONAND HABITAT I first located S. diclinis on the northern slopes and later on the south-eastern slopes of the Sierra del Castillo (see Fig. 3), growing in old, but still cultivated, terraced olive and carob groves beneath the main ridge (302 m) of hard, karst-
Fig. 3. The Sierra del Castillo, J~itiva, from the east.
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weathered limestone. The ridge was searched as thoroughly as its steepness allowed, access being gained from the south; the grikes in the weathered limestone were checked carefully. The plant was not found on the ridge, although vegetation co~taining Brachypodium ramosum R. & S. (see below) occurred in some of the grikes. The north side of the ridge presents a sheer, smooth wall with little opportunity for colonisation by plants. Nor was the plant found on the limestone shoulder below the ridge but ~bove the groves. Nevertheless, the possibility that a few individuals are on the ridge itself cannot be ruled out. It is also possible that S. diclinis occurs further to the west along the hill beyond the Sierra del Castillo: time did not permit a thorough search to be made in that area. Grove habitats similar to those on the Sierra del Castillo were unsuccessfully searched at Pla de Corral (see Introduction), at Corral de Carrero near Salem to the south, -and also in the hilly areas to the east towards Ambastida. Without evidence on the plant's ecological tolerance it was difficult to formulate a good search stratagem. Limestone hills are frequent in this area, rising steeply from the cultivated lowland plains. If one examines more closely the habitat of S. diclinis on the Sierra del Castillo (see Fig. 4), it becomes evident that the carob groves there are unusual in several respects when compared with typical groves in the area.
Fig. 4.
Groves on the northern slopes of the Sierra del CastiUo. Note the thicket of Pinus halepensis in the centre of the photograph.
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The groves containing S. diclinis have terrace banks which are not faced with stone walls and which support grassy communities. The groves on the north-east and south-east of the hill which possess S. diclinis show evidence of only very sporadic, light goat-grazing. The little hill to the north-east (marked on the map in Fig. 5) is heavily-grazed by a large herd of goats. Finally, the carob groves are in a state of sporadic cultivation. S. diclinis is found in the areas which are kept free from encroaching scrub and Pinus halepensis Mill. by mule ploughs which do not take in the ground around the carob tree bases on the terrace fiats, and weed killers are not used to clear the terrace banks. Three 'sub-populations' were distinguished on the hill. Their locations are indicated in Fig. 5 (one as two small adjacent areas). Within these areas the individuals occur on the stony terrace fiats around the bases of trees and on the terrace banks. Morisset & Bozman (1969) record the plant growing, 'In woods on Mount J~itiva' but 'open groves' would be more precise. The sub-populations (see Fig. 5) consist of ca. 300 individuals, of ca. 130 and of ca. 120. The areas occupied by the sub-populations are respectively 0.6 ha 0.2 ha and less than 0.1 ha. Relev6s were taken from the field layer within the three sub-populations, where there were good groups of S. diclinis, cover-abundances being recorded on the
Fig. 5. Sketch map of the Sierra del Castillo, Jfitiva. The main sub-populations of S. diclinis are indicated by vertical hatching, isolated finds by single dots, and the occurrence of S. alba by the letter 'a'. Tree symbols denote areas dominated by Pinus halepensis. Contours are at 20 m intervals and their heights are given in metres.
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TABLE 1 RELEVES FROM VEGETATIONCONTAININGS. diclinis ON THE SIERRA DEL CASTILLO Relev6 number 1 Aspect N Total cover ( ~ ) 90 Osyris alba L. 1 Aegilops ovata L. Arena sterilis L. Brachypodium ramosum R. & S. 8 Bromus madritensis L. Cynodon dactylon (L.) Pers. Cynosurus echinatus L. 4 Dactylis glomerata L. subsp, hispanica (Roth) Nyman 4 Anagallis arvensis L. Andryala integrifolia L. 1 Antirrhinum barrelieri Boreau 1 Asparagus acutifolius L. 1 Campanula erinus L. 1 Convolvulus althaeoides L. 2 C. arvensis L. C. sp. Daucus carom L. Euphorbia exigua L. Ferula communis L. 1 Geranium rotundiJblium L. 2 Hedypnois cretica (L.) Dum.-Courset. Lactuca sp. Leontodon taraxacoides (Vill.) M6rat subsp, saxatilis 1 L. taraxacoides subsp. Iongirostris Finch & Sell 1 Linum sp. Lobularia maritima (L.) Desf. 1 Mercurialis annua L. 1 Nigella sp. Ononis natrix L. subsp, ramosissima (Desf.) Batt. Paronychia argentea Lain. Petrorhagia prolifera (L.) P. W. Ball and Heywood Phagnalon saxatile (L.) Cass. 1 Plantago albicans L. Polycarpon tetraphyllum (L.) L. Ranunculus sp. Rumex bucephalophorus L. 1 Sanguisorba minor Scop. subsp, minor Scrophularia sciophila Willk 3 Sedum sediforme (Jacq.) Pau Silene diclinis (Lag.) M. Lainz 2 S. secundiflora Otth 1 S. vulgaris (Moench) Garcke 3 Thapsia maxima Miller 1 Trifolium dubium Sibth. 1 7". stellatum L. 2 Urospermum picroides (L.) Desf. 1
Aloinia aloides (Schultz.) Kindb. Antitrichia californica Sull. Barbula reflexa (Brid.) Brid. B. unguiculata Hedw. Brachythecium albicans (Hedw.) B., S. & G, Bryum sp. Eurhynchium meridionale (Sehimp.) De Not.
2
2 2 2
2 N 90
3 ESE 30
4 E 95
1 4 8 1
2
8
3
4 4
2
2 1 1 1 1
2
1
2 2 1
I
2 2 1 1
1 1
1
1 I 2 2 2
2
1
2 4
3 3
1 1 3
1 2 2 2 2 2 2
5 NE 80
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23
TABLE 2 RESULTSOF SOIL ANALYSESFROMRELEVES4 AND 5 (Replicated 3 g samples of air-dried fine earth (particle size < 2 mm)were extracted with 100 ml normal ammonium acetate at pH 7.0. Cation concentrations in the extracts were determined as follows: Na + and K + by flame photometry, Ca 2+ and Mg 2+ by atomic absorption spectrophotometry. Loss on ignition was measured by loss in weight of ca. 10 g air-dry samples ovendried for 24 h at 105°C and subsequently ignited in a muffle furnace at 400°C for 8 h. Bulk density was estimated by the method described in Jeffrey (1970).)
Cation concentrations (mequiv (100 g ) - 1, and mequiv d m - 3 in parentheses) Na + K+ Mg2+ Ca 2+ Relev6 4 Relev6 5 Relev6 4 Relev6 5
0"28 0.40 (2"6) (3.7) 0'30 0.37 (3.3) (4-0) Losses on ignition (%) 6-6 3.88
1.01 (9"3) 0"83 (9.0)
48"8 (451) 55'9 (606)
Domin scale. The relev6s are presented in Table I. Relev6s 1, 2 and 3 were from places with a very open tree layer of scattered Ceratonia siliquosa U (carob) on the terrace fiats; the tree layer in relev6 3 also consisted of Olea europaea L. (olive) and in relev6 4 entirely of olives. Relev6 3 was from a terrace flat and the remaining relev6s from terrace banks. Professor S. Rivas-Martinez (pers. comm.) relates these to the Teucrio-Brachypodietum ramosi O. Bol6s (All. Brachypodion ramosi, Ord. Thero-Brachypodietalia). Soil samples were collected from the sites of relev6s 4 and 5. Both samples were pale and friable with small limestone pebbles and little humus. Mr Brian Huntley has kindly analysed these samples and the results of the analyses are presented in Table 2. The soils are extremely calcareous and there was abundant free CaCO3, as minute fragments of pure limestone. The losses on ignition confirm that the soils had a very low organic content.
CLASSIFICATION OF ENDEMICS
It is not possible here to review all the relevant literature on endemism but in order to suggest working hypotheses about the origins of the isolation, both spatial and taxonomic, of S. diclinis it is necessary to examine briefly the available theories of plant endemism which are, in many cases, obscured by conflicting terminologies. A. P. de Candolle appears to be the first author to use the term 'endemic' in a botanical sense(see A. de Candolle, 1855, p. 474) to describe taxa with a limited geographical distribution, and Engler (1882) was the first to classify endemics into types. The main incentive for the subsequent study of endemics has been their supposed potential to throw light on the 'origin of floras', i.e. the reconstruction
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of past distribution and evolution is attempted from modern taxonomy and biogeography. Such reconstructions often involve considerable assumptions. Most classifications of endemism are unsatisfactory in that the correct allocation of a particular endemic to a 'type' requires knowledge of its history. This can lead to the same kind of logical circularity as results from the failure to separate fact from inference in 'phyletic' conceptions of taxonomy (see Gilmour, 1961). Three classifications have been widely applied. The first is based upon the supposed ages of the endemics and the second upon their past distributions. The evidence used is often the same in both cases. Neither provides a base from which to examine objectively the actual case-history of an endemic. The third is based on cytology and is precisely analogous to a special-purpose cytotaxonomic classification. It should not be forgotten that different taxonomic treatments of endemics can affect their assignment to types--a point often neglected. (1) Braun-Blanquet (1929) discusses the endemic flora of the C6vennes, defining two age classes of endemic--'end6miques pal6ogenes' (pal~oend~miques) and 'end6miques n6ogenes' (n6oend6miques)--palaeoendemics being ofpre-Quaternary origin. The evidence used to assign endemics to these categories is based on their distributions and on geological considerations. For example, species related in the phyletic sense which are now separated by a sea barrier are assumed to be as 'old' as the last land connexion between their present areas; some species are considered 'new' because of their affinities with other species from which they might reasonably be thought to have been separated by Quaternary events. Braun-Blanquet also used ecological specialisation and lack of plasticity and expanding power as evidence of ancient origin and concluded that, in the flora of the C6vennes, the taxonomically well-defined species were, in general, palaeoendemics, the less well-defined being neoendemics. Braun-Blanquet's evidence depends, like many biogeographic arguments, first of all on equating phenetic similarity with phyletic relationship, so that it is worth noting that this need not be valid, as assumptions about evolutionary rates are involved. Jardine et aL (1969) suggest a criterion of phenetic isolation for a group of taxa to be regarded as monophyletic, depending on the assumption that: d(i, j) > d(i, k) .~. t(i,j) > t(i, k) for all i,j and k, where i,.j and k are taxa, d denotes the degree of phenetic difference between a pair of taxa, and t the time since their evolutionary divergence. The greater the degree of isolation, the greater the deviations from this assumption that are tolerable for the phyletic inference to hold. Secondly, the semi-geological evidence that Braun-Blanquet used is tenuous. The arguments about palaeoendemics lacking plasticity are unsatisfactory: restricted endemics are almost by definition restricted in habitat (it is seldom proved experimentally that they have strict requirements), lack of plasticity is generally inferred from supposed ecological specialisation, and lack of expanding power from spatial restriction.
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(2) Endemics are also classified according to their past distributions. Briquet (1901) called these 'end6miques par conservation' and 'end6miques par novation', Ridley (1925) 'epibiotics' and 'endemics' and Chevalier & Cu6not (1927) 'pal6oend6miques' and 'neo-end6miques'. Several other terminologies have been used in this context. Palaeoendemics sensu Chevalier & Cu6not are 'relict', surviving in one part of what was previously a larger area, and neoendemics have arisen in situ and not yet spread further. It is possible that the idea of relictual species being old has arisen from an idea of 'age and area' .(see Willis, 1922), an 'old' taxon being presumed to have occupied a large area. Therefore, finding 'old' taxa as endemics, they are thought of as relicts, as by Engler (1882) and Briquet (1901). Similarly 'relict' species, having once occupied a wide area, ate considered to be 'old'. This equation is probably fair, but only in a very approximate sense. (3) Favarger & Contandriopoulos (1961) and Contandriopoulos (1962) discuss a new system of categories. They attack previous approaches to endemism, pointing out that, generally, whatever the definitions and supposed evidence, well-defined taxa have been categorised as palaeoendemics and ill-defined taxa as neoendemics. Favarger & Contandriopoulos arrive at a cytological classification of endemics containing four categories. Their 'pal6oend6miques' are defined as being isolated systematically, old, and with little variation, not necessarily having arisen in their area of survival. 'Schizoend6miques' are produced as a result of'gradual speciation' (see Valentine, 1948 and 1949), having a common origin and identical chromosome numbers. 'Patroend6miques' are restricted diploid endemics which give rise to widely-distributed polyploids, and 'apoend6miques' are polyploid species of restricted area which have arisen from widely-distributed diploid ancestors. The term 'cryptoend6mique' is added as an extra to cover unrecognised cytological races. Favarger & Contandriopoulos make the assumption that a polyploid has arisen from a morphologically similar diploid, and not the reverse. However, a polyploid has not necessarily arisen from a related present-day diploid unless an absurdly strict cytological view of species is adopted. Their category 'pal6oend6mique' encompasses both possible earlier definitions and is in no sense new. Gaussen & Leredde (1949) have proposed a neutral terminology: 'megaend6miques' and 'microend6miques' are defined respectively as 'Linnaean' and 'non-Linnaean' or microspecies. This terminology has no connotations of age or evolutionary origin.
EVIDENCE CONCERNING THE HISTORY OF
S. diclinis
How, then, can one suggest hypotheses about the origin of an endemic and its present isolation, and can any evidence be found in the case of S. diclinis?
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One means o f obtaining convincing evidence about the origin o f a taxon is to carry out crossing experiments. In this manner it is sometimes possible to synthesise a species artificially. The development of new hybrids can be watched in the wild. The production of hybrids between two species has been taken to mean that they are closely 'related'. This assumption is unsatisfactory if one is to allow for sterility barriers being built up between sympatric species (see Stebbins, 1966, Chapter 5). S. alba also occurs on the Sierra del Castillo very near to S. diclinis, yet there are no hybrids present and I have, so far, been unsuccessful in producing such hybrids in cultivation. Morisset & Bozman (1969) produced fertile hybrids between S. heuffelii and S. diclinis. I have successfully repeated this cross and have also produced fertile hybrids between S. diclinis and S. dioica. Nevertheless, this interfertility should be taken as no more than vindication of the grouping already based on morphological similarity. One can only say that S. diclinis bears most resemblance to the other members of section Elisanthe and that crossing experiments confirm this relationship. One could imagine (see remarks above on phyletic inferences) S. diclinis becoming distinct within section Elisanthe more recently than the whole section became distinct from the rest of Silene. Pollen and macrofossil analysis can aid the study of endemics in two ways: direct evidence can be obtained on the past distribution of a taxon, and the vegetation and palaeoenvironment of large areas can be investigated and used as a better foundation for suggesting hypotheses about their history. A combination of these approaches led to Pigott & Walters' (1954) convincing explanation of the disjunctions of some rarer British plants, some of which have been shown to have been widespread in the open-vegetation of the Late-Devensian and persisting now only in 'refugia'--habitats such as gorges and inland cliffs where the forest cannot have been present during the Flandrian forest maximum. Unfortunately, pollen, widely-dispersed, is often not identifiable to species level and macrofossil finds are more dependent on chance. Since S. diclinis has never been found as a fossil, there remains only indirect evidence: detailed knowledge of a plant's present environment and knowledge of the palaeoenvironment of a wide surrounding area can be combined to suggest the origin of endemic distributions, as was done by Montserrat & Villar (1972) in their study of Spanish endemism. The Sierra del Castillo is of Cretaceous limestone, but the surrounding area carries Miocene deposits, so S. diclinis must have evolved or become restricted to its present area not before the Cretaceous and probably in, or after, the Miocene. It is difficult to be more precise about the emergence of the area, since Quaternary Mediterranean sea levels are very difficult to correlate (see Hey, 1971). Knowledge of Tertiary floras and associated environments is fragmentary, based mainly on leaf-beds, e.g. Menrndez Amor (1948). A more coherent picture o f Quaternary palaeoenvironments in the Mediterranean region has emerged f r o m p o l l e n analysis of long cores, especially from Macedonia (Wijmstra, 1969),
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Syria (Niklewski & van Zeist, 1970), northern Italy (Frank, 1969) and southern Spain (Florschiitz et al., 1971); see also Bonatti (1966). It appears that the periods of maximum glaciation in high latitudes have been consistently characterised by Steppe-like vegetation with abundant Artemisia, Ephedra, Chenopodiaceae and Caryophyllaceae; the Steppe affinities are reinforced by electron microscope identification of certain Chenopodiaceae (Smit & Wijmstra, 1970) now restricted to areas much further east. By implication the climate is taken to have been cool and semi-arid. This contrasts with earlier views and does not suggest that the biogeographic effects of Quaternary events should be underplayed (cf. Montserrat & Villar, 1972). The interglacials and interstadials of high latitudes were characterised by mixed forest. At about 10,000 BP forest cover dramatically increased. Evergreen oak forest was widespread during the Flandrian (Beug, 1966) and there is evidence of man having cleared these forests (see Brande, 1973). The present habitat of S. diclinis is man-made and does not suggest any reason for its localisation. Its association with the Sierra del Castillo is more striking. In the light of geological evidence, an attractive hypothesis is that S. diclinis has been restricted by the widespread forests of 'interglacial' and Flandrian times to a habitat that has remained open, possibly failing to colonise man-made open habitats at any distance from its refugium. This is only a hypothesis and there is no evidence to discount S. diclinis having evolved in situ.
THE GENETIC SITUATION IN A RESTRICTED ENDEMIC
Wright (1969) sets out mathematically the theory of genetic drift in non-adaptive characters within populations. Some of the implications of this theory are discussed by Dobzhansky (1951, p. 363). It is predicted that in 'small' gamodemes there should be increased homozygosity and decreased polymorphism, and that selective values should have little effect, i.e. random genetic drift should be a major influence on evolution. The theory does not predict what constitutes a 'small' population since this can only be defined in relation to unknowns such as the mutation rate. The theory does predict that, in a fluctuating population, the minimum size is critical. Little work has been carried out along these lines using plants, and Wright's theory remains untested in wild populations. It would therefore be very interesting to have information on gene frequencies in an outbreeding and highly localised and definable plant population such as that of S. diclinis. S. diclinis has evident variation in flower size, shape and colour in its natural habitat (e.g. from a sample of 13 flowers from as many male plants, petal claw length has mean 14.2 mm and standard deviation 2.31 mm; corolla diameter, mean 16.2 ram, standard deviation 4.41 mm). This degree of variation is maintained in cultivation and is, therefore, presumably genetically based. This contrasts
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with the situation found in another species of Silene, S. viscariopsis Bornm., a similarly restricted but hermaphrodite and self-fertile Jugoslavian endemic (S. M. Waiters, pers. comm.). The possible inference from this subjective comparison could be tested by allozyme studies (which have been surprisingly neglected in plants: see Lewontin, 1974, p. 120).
CONSERVATION
S. diclinis on the Sierra del Castillo consisted, in 1974, according to my estimates, of a population of about 600 individuals. One must treat its position as precarious. Of course there is no evidence for how long it has existed as such a small population. There are many impending threats to the survival of S. diclinis in the carob groves of the Sierra del Castillo. Like many of the Greek and Turkish endemics, for example, it is existing solely in a man-made habitat (see Melville, 1970-). I have speculated that it once inhabited the limestone ridge above the groves. Increasing cultivation o f the groves would probably lead to the walling-up of the terrace banks or the use of weed-killers as in surrounding well-worked groves. Both changes, particularly the latter, could jeopardize S. diclinis. The complete abandonment of the groves would almost certainly allow Pinus halepensis, already present nearby (see Figs. 3 and 4), to engulf the area, as in many derelict groves throughout the Mediterranean. Little can compete with the pine thickets. A slight change in the grazing area of the local herds of goats could reduce the substratum of the groves to a dry, bare hillside like that to the north-east. Seed banks provide a way in which stocks of rare plants can be maintained (see Thompson, 1974) and increased by hand-pollination of cultivated plants. It is necessary to grow a large number of individuals for such hand-crossing, to ensure that as much genetic variation as possible is kept in the seed stocks. The distribution of seed to as many seed banks as possible will also help to ensure the retention o f the genetic variation. Seed of S. diclinis was sent to the seed bank at Kew in 1974. Seventy plants were raised in the Botanic Garden at Cambridge and were hand-pollinated in 1975 to produce more seed. Half of this was sent to Professor C. Gomez-Campo at Madrid for his seed bank of Spanish endemic plants, and half has been retained at Cambridge for further bulking-up and subsequent distribution. Some endemic plants, by virtue o f their attractiveness to alpine gardeners in particular, have become widespread in cultivation (see Melville, 1970-). Although the species will suffer selection for its most handsome forms, this is nevertheless another way in which stocks of rare plants can be increased. Seed and plants of S. diclinis have been distributed to a number of alpine gardeners. Information on S. diclinis has been added to the Index of Rare Endemic Vascular Plants of Europe which Dr S. M. Walters is compiling (see Walters, 1971) and will also be included in a future addition to the Red Data Book.
A STUDY IN ENDEMISM: Silene diclinis
29
It is hoped that these steps will help to preserve S. diclinis, at least in cultivation, if one takes the most pessimistic view o f its future in the wild. The data I have collected could form a provisional basis for any possible future attempts to conserve the species in the wild.
ACKNOWLEDGEMENTS
My supervisor, Dr S. M. Waiters, has encouraged my interest in endemism and I would like to thank him for all the ideas that he has given me, for his excellent guidance and for critically reading this paper. Professor C. G 6 m e z - C a m p o has been most helpful and kindly provided me with maps. Professor S. Rivas Martinez kindly examined the Jfitiva relev6s and commented on their phytosociological affinities. Dr H. J. B. Birks determined the mosses collected from the J~itiva relev6s and Mr P. D. Sell determined the composites. I am most grateful to Mr B. Huntley who analysed the soil samples and to Mr Jack Symonds o f the University Botanic Garden, Cambridge, for looking after my cultivated stock o f S. diclinis. Dr H. L. K. Whitehouse and Dr D. Briggs gave advice on the genetic aspects of this paper and Dr R. W. Hey discussed aspects o f Mediterranean geological history. This work was supported by a Science Research Council research studentship which is gratefully acknowledged. Finally, I would like to thank my husband, Colin, for help with the fieldwork and for his constructive criticism during the writing of this paper.
REFERENCES
BAKER, H. G. (1947). Biological flora of Melandrium (Roehling em.) Fries. J. Ecol., 35, 271-92. BEUG, J.-J. (1966). On the forest history of the Dalmatian coast. Rev. Palaeobot. & Palynol., 2, 271-9. BIRKS, 1-1. J. B. (1973). Past and present vegetation of the Isle of Skye. London, Cambridge University Press. BONATTI, E. (1966). North Mediterranean climate during the last WOrm glaciation. Nature Lond., 209, 984-5. BRANDE, VON A. (1973). Untersuchungen zur postglazialen Vegetationsgeschichte im Gebiet der Neretva-Niederungen (Dalmatien, Herzegowina). Flora, Jena, 162, 1-44. BRAUN-BLANQUET,J. (1929). L'origine et d6veloppement des flores dans le Massif Central de France. Annls Soc. linn. Lyon, 76, 1-109. BRIQUET, J. (1901). Recherches sur la flore des montagnes de la Corse et ses origines. Annu. Conserv. Jard. bot. Gendve, 5, 12-119. CANDOLLE,A. DE (1855). Gdographie botanique raison~e. Paris. CHATER, A. O. ~. WALTERS,S. M. (1964). Silene. In Flora Europaea, vol. 1, ed. by T. G. Turin and others, 158-81. London, Cambridge University Press. CHEVALIER,A. ~. CUI~NOT,L. 0927). Biogeographie. In Traite de Gdographie Physique, vol. 3, ed. by E. de Martonne, t062-517. Paris. CONTANDRIOPOULOS, J. (1962). Essai de classification des end6miques corses. Revue Cytol. Biol. v~g., 25, 449-59. DOBZHANSKY,T. (1951). Genetics and the origin of species, Third edn. New York, Columbia University Press.
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ENGLER, A. (1882). Versuch einer Entwicklungsgeschichte der Extratropischen Florengebiete der Sadlichen Hemisphdre, vol. 2. Leipzig, W. Engelmann. FAVARGER, C. & CONTANDRIOPOULOS,J. (1961). Essai sur l'end6misme. Bet. schweiz, hot. Ges., 71, 384--408. FLORSCH~2TZ,F., MEN~NDEZAMOR, J. & WIJMSTRA,T. A. (1971). Palynology of a thick Quaternary succession in southern Spain. Palaeogeogr., Palaeoclimatol., PalaeoecoL, 10, 233-64. FRANK, A. H. E. (1969). Pollen stratigraphy of the Lake of Vico (Central Italy). Palaeogeogr., Palaeoclimatol., Palaeoecol., 6, 67-85. GAUSSEN,H. & LEREDDE,C. (1949). Les end6miques pyr6n6o-cantabriques dans la region centrale des Pyr6n6es. Bull. Soc. bot. Fr., 96, 57-83. GILMOUR, J. S. L. (1961). Taxonomy. In Contemporary botanical thought, ed. by A. R. MacLeod & L. S. Cobley, 27-45. Edinburgh, Oliver and Boyd. HEY, R. W. (1971). Quaternary shorelines of the Mediterranean and Black Seas. Quaternaria, 15, 273-84. JARDINE, N., VAN RIJSBERGEN,C. J. & JARD1NE,C. J. (1969). Evolutionary rates and the inference of evolutionary tree forms. Nature, Lond., 224, 185. JEFFREY,D. N. (1970). A note on the use of ignition loss as a means for the approximate estimation of soil bulk density. J. Ecol., 58, 297-99. LAGASCA, M. (1816). Genera et Species Plantarum. Madrid. LEWONTIN, R. C. (1974). The genetic basis of evolutionary change, New York & London, Columbia University Press. MELVmLE, R. (1970-). Red Data Book, Vol. 5, Angiospermae. Morges, Switzerland, International Union for Conservation of Nature and Natural Resources. MEN~NDEZ AMOR, J. (1948). Notas preliminares al estudio sobre la flora Terciaria de la Cerdafia Espafiola. Ciencias, 13, 782-7. MONTSERRAT, P. & VILLAS, L. (1972). El endemismo Ib6rico. Aspectos ecol6gicas y fitotopogrfificos. Bol. Soc. broteriana, 46, 503-27. MORISSET, P. & BOZMAN, G. V. (1969). Note on the cytology of an F1 hybrid between Silene diclinis (Lag.) M. Lainz and S. heuffelii So6. New Phytol., 68, 1235-41. NIKLEWSKI, J. & ZEIST, W. VAN (1970). A Late Quaternary pollen diagram from northwestern Syria. Acta bot. neerl., 19, 737-54. PIGOTT, C. D. & WALTERS,S. M. (1954). On the interpretation of the discontinuous distributions shown by certain British species of open habitats. J. EcoL, 42, 95-116. RIDLEV, H. N. (1925). Endemic plants, d. Bot., 43, 182-3. SMIT, A. & WIJMSTgA, T. A. (1970). Application of transmission electron microscope analysis to the reconstruction of former vegetation. Acta bot. neerl., 19, 867-76. STEBmNS, G. L. (1966). Processes of organic evolution. New Jersey, Prentice-Hall. THOMPSON, P. A. (1974). The use of seed-banks for conservation of populations of species and ecotypes. BioL Conserv., 6, 15-19. VALENTINE, D. H. (1948). Studies in British primulas. II Ecology and taxonomy of primrose and oxlip (Primula vulgaris Huds. and P. elatior Schreb.). New PhytoL, 47, 111-30. VALENTINE, D. H, (1949). The units of experimental taxonomy. Acta biotheor., 9, 75-88. WALTERS, S. M. (1971). Index to the rare endemic vascular plants of Europe. Boissiera, 19, 87-9. WELLS, T. C. E. & BARLING,D. M. (1971). Biological flora of Pulsatilla vulgaris Mill. (Anemone pulsatilla L.). J. EcoL, 59, 275-92. WlJMSTRA, T. A. (1969). Palynology of the first 30 m of a 120 m deep section in northern Greece. Acta bot. neerL, 18, 511-27. WlLHS, J. C. (1922). Age and area. Cambridge University Press. WRIGrIT, S. (1969). Evolution and the genetics of populations, vol. 3. Chicago and London, University of Chicago Press. WULFF, E. V. (1950). An introduction to historicalplant geography. Waltham, Mass., The Chronica Botanica Company.
HONOR C. PRENTICE The Botany School, Cambridge, Great Britain A BS TRA C T
Silene diclinis (Lag.) M. Lainz is a dioecious endemic with a highly restricted distribution in south-eastern Spain. The sparse literature on the plant is summarised before referring to the results of a study of S. diclinis in the wild. A new description of the species is presented and its taxonomic affinities discussed. Details of the flowering time of S. diclinis, possible pollinators and its population age structure are set out and its wild habitat described. Before examining the possible origin of the distribution of S. diclinis, an attempt is made to clarify the various classifications of endemism that have been widely used in the literature. It is considered that since these classifications are generally based on the supposed origins of endemics they do not foem a sound basis for the examination of evidence in individual cases. Types o f evidence that can be used to throw light on the history of individual endemics are examined and include evidence gained from experimental taxonomy, pollen and macrofossil analysis and ecological studies. Unfortunately, in the case of S. diclinis there is no direct evidence referring to its past. One hypothesis, based on present distribution and on a consideration of Mediterranean Cenozoic palaeoenvironments, is put forward tQ explain the present restriction of S. diclinis. Finally, the genetic situation in a restricted endemic population, the future of S. diclinis and conservation measures are discussed.
INTRODUCTION
The remarkably restricted dioecious Spanish endemic Silene diclinis (Lag.) M. Lainz (see Figs. 1 and 2) is a member of the section Elisanthe of the genus (Chater & Waiters, 1964), a European section which also contains the widespread species, S. alba (Mill.) E. H. L. Krause, S. dioica (L.) Clairv. and S. noctiflora L., and the less-restricted Balkan endemic, S. heuffelii So6. Waiters (1971) summarised the literature referring to S. diclinis. The plant was first described by Lagasca (1816), as Lychnis diclinis, growing: 'In montibus 15 Biol. Conserv. (10) (1976)--O Applied Science Publishers Ltd, England, 1976 Printed in Great Britain
16
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Fig. 1. S. diclinis (male).
Fig. 2.
S. diclinis (female).
A STUDY IN ENDEMISM :
Silene dicBnis
17
Setabi vicinis locis depressionibus in Valentii Regni.' Since Lagasca's work there has been little information collected on the species. A specimen at CGE (Cambridge University Herbarium), collected by E. Bourgeau in 1852, is labelled: 'Sierra de San Felipe de Xativa, Prov. de Valencia.' Both localities have been assumed to refer to the Sierra del Castillo, J~tiva, Prov. de Valencia. Plants have also been found at the Pla de Corral, Simat de Valdigna, Valencia, which is 25 km north-east of J~itiva (not south-east as given by Morisset & Bozman, 1969) by Professor E. M. Galiano (there is a specimen collected by Galiano in 1964 in CGE). In June 1974 a study of S. diclinis was made in its locus classicus. (A search of the Pla de Corral area was also made but it was not refound there.) Information was collected on the morphological variation, the habitat and species associated with S. dielinis with a view to providing a reliable set of data on the species which would also allow suggestions to be made about the cause of its present distribution and future protection.
DESCRIPTION OF THE SPECIES
The following description has been prepared from 21 male plants and 20 females (including, unfortunately, due to the time of year, only one flowering female) systematically examined in the field with details of seed morphology observed later under a low-power microscope in the laboratory where 30 seeds were scored. The description augments that in Chater & Walters (1964). Dioecious; perennial with short, thick stock and procumbent to ascending stems clothed with long, patent, soft, strongly flexuous eglandular hairs. Leaves pale yellowish-green with eglandular hairs on both surfaces, densest on the veins; glandular hairs occasional on margin. Basal leaves 3-13 cm sessile and spathulate; cauline leaves and bracts 2-9 cm sessile, spathulate, oblanceolate or oblong. Inflorescence a regular dichasial cyme with alar flowers. Pedicels strongly-deflexed in fruit ;. male 5-19 mm, female 3-5 ram. Calyx clothed with soft, flexuous hairs, often with sparse, short, straight, glandular hairs beneath; cylindrical in both sexes, becoming globose in fruiting females; male 9-19 mm and female 5-15 mm; nerves (9)-10-(11) in males and 20 in females; red pigment always present in males and seldom in females; teeth acute and shortly hairy. Corolla deep magenta; diameter, male 10-22 mm, female (single measurement) 19 mm (in cultivation male flowers are generally larger than female); coronal scales white with frilled margins; petals (4)-5, male emarginate, female emarginate to bifid (to less than ¼ of their length); arrangement often asymmetrical and in overlapping clumps; claw long, male 5-11 ram, female (single measurement) 14 mm, with two white, acute auricles. Stamens 10; anthers yellow; filaments hairless; pollen of 'S. dioica type' (see Birks, 1973, p. 230). Styles (3)-5 with long papillae. Carpophore very short. Capsule
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5-11 mm, globose; teeth (5, 7, 9)-10 deflexed when ripe, often splitting irregularly. Seeds pale to dark brown, 1.4-1.9 mm long, 1.2-1.5 mm wide; face convex; back rounded and 1.0-1"2 mm across; tubercles 240--270/~m, broadly conical; surface plates with stellate sutures. S. diclinis has more obvious affinities with section Elisanthe than with any of the other European sections of Silene. Nevertheless, it is a distinctive plant and differs from the other species of the section in many respects. Notable differences are its prostrate or ascending habit, its emarginate or shallowly-dissected (rather than bifid) petals and its small, globose capsule with its deflexed pedicel. Like all other members of the section, except S. noctiflora, it is dioecious, a rare feature in a restricted endemic. A herbarium specimen from the Sierra del Castillo has been deposited at CGE.
GENERAL BIOLOGY
In the second week of June 1974, nearly all the female plants of S. diclinis had ripe seed. In cultivation S. diclinis seed takes 4-5 weeks to mature after fertilisation and it seems reasonable to assume that the main flowering of the plant in the wild takes place in early May. The male individuals, as in S. alba and S. dioica, continue flowering after the females. In cultivation occasional plants, particularly males, will produce one or two flowers in the aatumn. Cultivated material starts to flower in March and continues until June. Individuals on the northern slopes of the Sierra flowered after those on the southern slopes. The leaves die back from their tips as flowering continues, are shrivelled in the summer and new leaves sprout in the autumn. S. diclinis has magenta, day-opening flowers with a barely-perceptible fragrance. Pollen is produced in aggregated lumps. From these features and from comparison with other species o f Silene, especially S. dioica, it seems likely that it is insectpollinated (see Baker, 1947). In the greenhouses at Cambridge I have seen S. diclinis visited by bumble bees, other bees and one moth (Plusia gamma). All the individuals possessed thick stocks and many appeared to be of considerable age when compared with material in cultivation. Individuals grown from seed in Cambridge in 1958 are still healthy. Copious seed was being produced in the wild population but no seedlings were found beneath the plants, although seeds were seen on the ground on a few occasions. It has not been possible, as yet, to make counts of the annual rings in the stocks and, in any case, such counts would have to be interpreted with caution in view o f the occurrence of anomalous secondary thickening in the Centrospermae. Wells & Barling (1971) have shown a similar age structure in populations of Pulsatilla vulgaris in the south of England, seedlings of that species being intolerant o f disturbance during establishment. As with Pulsatilla vulgaris, S. diclinis seeds showed high viability when grown in Cambridge but seedlings were easily killed by
A STUDY IN ENDEMISM" Silene diclinis
19
moving before they were properly established. Seedlings were also more sensitive to over-watering or droughting than the adult plants. In order to maintain a population of long-lived perennials, it would clearly not be necessary for many seedlings to survive each year. It is probable also, although the seeds do not appear to have a significant after-ripening requirement, that their germination may be dependent on autumn rain. Vegetative propagation by separation of ramets from the stock is easy in cultivation, and the mule ploughs may now play the role of propagators in the present habitat. Because of the incurved pedicel and the large size of the seeds, it is unlikely that dispersal is particularly efficient, although the solitary female plant to the west of the bulk of the population shows that seeds can be dispersed for some distance. The areas of the three sub-populations found (see below) were elongated perpendicular to the contours, which could be explained by the propagules falling downhill under gravity.
DISTRIBUTIONAND HABITAT I first located S. diclinis on the northern slopes and later on the south-eastern slopes of the Sierra del Castillo (see Fig. 3), growing in old, but still cultivated, terraced olive and carob groves beneath the main ridge (302 m) of hard, karst-
Fig. 3. The Sierra del Castillo, J~itiva, from the east.
20
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weathered limestone. The ridge was searched as thoroughly as its steepness allowed, access being gained from the south; the grikes in the weathered limestone were checked carefully. The plant was not found on the ridge, although vegetation co~taining Brachypodium ramosum R. & S. (see below) occurred in some of the grikes. The north side of the ridge presents a sheer, smooth wall with little opportunity for colonisation by plants. Nor was the plant found on the limestone shoulder below the ridge but ~bove the groves. Nevertheless, the possibility that a few individuals are on the ridge itself cannot be ruled out. It is also possible that S. diclinis occurs further to the west along the hill beyond the Sierra del Castillo: time did not permit a thorough search to be made in that area. Grove habitats similar to those on the Sierra del Castillo were unsuccessfully searched at Pla de Corral (see Introduction), at Corral de Carrero near Salem to the south, -and also in the hilly areas to the east towards Ambastida. Without evidence on the plant's ecological tolerance it was difficult to formulate a good search stratagem. Limestone hills are frequent in this area, rising steeply from the cultivated lowland plains. If one examines more closely the habitat of S. diclinis on the Sierra del Castillo (see Fig. 4), it becomes evident that the carob groves there are unusual in several respects when compared with typical groves in the area.
Fig. 4.
Groves on the northern slopes of the Sierra del CastiUo. Note the thicket of Pinus halepensis in the centre of the photograph.
A STUDY IN ENDEM1SM."Silene diclinis
21
The groves containing S. diclinis have terrace banks which are not faced with stone walls and which support grassy communities. The groves on the north-east and south-east of the hill which possess S. diclinis show evidence of only very sporadic, light goat-grazing. The little hill to the north-east (marked on the map in Fig. 5) is heavily-grazed by a large herd of goats. Finally, the carob groves are in a state of sporadic cultivation. S. diclinis is found in the areas which are kept free from encroaching scrub and Pinus halepensis Mill. by mule ploughs which do not take in the ground around the carob tree bases on the terrace fiats, and weed killers are not used to clear the terrace banks. Three 'sub-populations' were distinguished on the hill. Their locations are indicated in Fig. 5 (one as two small adjacent areas). Within these areas the individuals occur on the stony terrace fiats around the bases of trees and on the terrace banks. Morisset & Bozman (1969) record the plant growing, 'In woods on Mount J~itiva' but 'open groves' would be more precise. The sub-populations (see Fig. 5) consist of ca. 300 individuals, of ca. 130 and of ca. 120. The areas occupied by the sub-populations are respectively 0.6 ha 0.2 ha and less than 0.1 ha. Relev6s were taken from the field layer within the three sub-populations, where there were good groups of S. diclinis, cover-abundances being recorded on the
Fig. 5. Sketch map of the Sierra del Castillo, Jfitiva. The main sub-populations of S. diclinis are indicated by vertical hatching, isolated finds by single dots, and the occurrence of S. alba by the letter 'a'. Tree symbols denote areas dominated by Pinus halepensis. Contours are at 20 m intervals and their heights are given in metres.
22
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TABLE 1 RELEVES FROM VEGETATIONCONTAININGS. diclinis ON THE SIERRA DEL CASTILLO Relev6 number 1 Aspect N Total cover ( ~ ) 90 Osyris alba L. 1 Aegilops ovata L. Arena sterilis L. Brachypodium ramosum R. & S. 8 Bromus madritensis L. Cynodon dactylon (L.) Pers. Cynosurus echinatus L. 4 Dactylis glomerata L. subsp, hispanica (Roth) Nyman 4 Anagallis arvensis L. Andryala integrifolia L. 1 Antirrhinum barrelieri Boreau 1 Asparagus acutifolius L. 1 Campanula erinus L. 1 Convolvulus althaeoides L. 2 C. arvensis L. C. sp. Daucus carom L. Euphorbia exigua L. Ferula communis L. 1 Geranium rotundiJblium L. 2 Hedypnois cretica (L.) Dum.-Courset. Lactuca sp. Leontodon taraxacoides (Vill.) M6rat subsp, saxatilis 1 L. taraxacoides subsp. Iongirostris Finch & Sell 1 Linum sp. Lobularia maritima (L.) Desf. 1 Mercurialis annua L. 1 Nigella sp. Ononis natrix L. subsp, ramosissima (Desf.) Batt. Paronychia argentea Lain. Petrorhagia prolifera (L.) P. W. Ball and Heywood Phagnalon saxatile (L.) Cass. 1 Plantago albicans L. Polycarpon tetraphyllum (L.) L. Ranunculus sp. Rumex bucephalophorus L. 1 Sanguisorba minor Scop. subsp, minor Scrophularia sciophila Willk 3 Sedum sediforme (Jacq.) Pau Silene diclinis (Lag.) M. Lainz 2 S. secundiflora Otth 1 S. vulgaris (Moench) Garcke 3 Thapsia maxima Miller 1 Trifolium dubium Sibth. 1 7". stellatum L. 2 Urospermum picroides (L.) Desf. 1
Aloinia aloides (Schultz.) Kindb. Antitrichia californica Sull. Barbula reflexa (Brid.) Brid. B. unguiculata Hedw. Brachythecium albicans (Hedw.) B., S. & G, Bryum sp. Eurhynchium meridionale (Sehimp.) De Not.
2
2 2 2
2 N 90
3 ESE 30
4 E 95
1 4 8 1
2
8
3
4 4
2
2 1 1 1 1
2
1
2 2 1
I
2 2 1 1
1 1
1
1 I 2 2 2
2
1
2 4
3 3
1 1 3
1 2 2 2 2 2 2
5 NE 80
A STUDY IN ENDEMISM" S i l e n e diclinis
23
TABLE 2 RESULTSOF SOIL ANALYSESFROMRELEVES4 AND 5 (Replicated 3 g samples of air-dried fine earth (particle size < 2 mm)were extracted with 100 ml normal ammonium acetate at pH 7.0. Cation concentrations in the extracts were determined as follows: Na + and K + by flame photometry, Ca 2+ and Mg 2+ by atomic absorption spectrophotometry. Loss on ignition was measured by loss in weight of ca. 10 g air-dry samples ovendried for 24 h at 105°C and subsequently ignited in a muffle furnace at 400°C for 8 h. Bulk density was estimated by the method described in Jeffrey (1970).)
Cation concentrations (mequiv (100 g ) - 1, and mequiv d m - 3 in parentheses) Na + K+ Mg2+ Ca 2+ Relev6 4 Relev6 5 Relev6 4 Relev6 5
0"28 0.40 (2"6) (3.7) 0'30 0.37 (3.3) (4-0) Losses on ignition (%) 6-6 3.88
1.01 (9"3) 0"83 (9.0)
48"8 (451) 55'9 (606)
Domin scale. The relev6s are presented in Table I. Relev6s 1, 2 and 3 were from places with a very open tree layer of scattered Ceratonia siliquosa U (carob) on the terrace fiats; the tree layer in relev6 3 also consisted of Olea europaea L. (olive) and in relev6 4 entirely of olives. Relev6 3 was from a terrace flat and the remaining relev6s from terrace banks. Professor S. Rivas-Martinez (pers. comm.) relates these to the Teucrio-Brachypodietum ramosi O. Bol6s (All. Brachypodion ramosi, Ord. Thero-Brachypodietalia). Soil samples were collected from the sites of relev6s 4 and 5. Both samples were pale and friable with small limestone pebbles and little humus. Mr Brian Huntley has kindly analysed these samples and the results of the analyses are presented in Table 2. The soils are extremely calcareous and there was abundant free CaCO3, as minute fragments of pure limestone. The losses on ignition confirm that the soils had a very low organic content.
CLASSIFICATION OF ENDEMICS
It is not possible here to review all the relevant literature on endemism but in order to suggest working hypotheses about the origins of the isolation, both spatial and taxonomic, of S. diclinis it is necessary to examine briefly the available theories of plant endemism which are, in many cases, obscured by conflicting terminologies. A. P. de Candolle appears to be the first author to use the term 'endemic' in a botanical sense(see A. de Candolle, 1855, p. 474) to describe taxa with a limited geographical distribution, and Engler (1882) was the first to classify endemics into types. The main incentive for the subsequent study of endemics has been their supposed potential to throw light on the 'origin of floras', i.e. the reconstruction
24
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of past distribution and evolution is attempted from modern taxonomy and biogeography. Such reconstructions often involve considerable assumptions. Most classifications of endemism are unsatisfactory in that the correct allocation of a particular endemic to a 'type' requires knowledge of its history. This can lead to the same kind of logical circularity as results from the failure to separate fact from inference in 'phyletic' conceptions of taxonomy (see Gilmour, 1961). Three classifications have been widely applied. The first is based upon the supposed ages of the endemics and the second upon their past distributions. The evidence used is often the same in both cases. Neither provides a base from which to examine objectively the actual case-history of an endemic. The third is based on cytology and is precisely analogous to a special-purpose cytotaxonomic classification. It should not be forgotten that different taxonomic treatments of endemics can affect their assignment to types--a point often neglected. (1) Braun-Blanquet (1929) discusses the endemic flora of the C6vennes, defining two age classes of endemic--'end6miques pal6ogenes' (pal~oend~miques) and 'end6miques n6ogenes' (n6oend6miques)--palaeoendemics being ofpre-Quaternary origin. The evidence used to assign endemics to these categories is based on their distributions and on geological considerations. For example, species related in the phyletic sense which are now separated by a sea barrier are assumed to be as 'old' as the last land connexion between their present areas; some species are considered 'new' because of their affinities with other species from which they might reasonably be thought to have been separated by Quaternary events. Braun-Blanquet also used ecological specialisation and lack of plasticity and expanding power as evidence of ancient origin and concluded that, in the flora of the C6vennes, the taxonomically well-defined species were, in general, palaeoendemics, the less well-defined being neoendemics. Braun-Blanquet's evidence depends, like many biogeographic arguments, first of all on equating phenetic similarity with phyletic relationship, so that it is worth noting that this need not be valid, as assumptions about evolutionary rates are involved. Jardine et aL (1969) suggest a criterion of phenetic isolation for a group of taxa to be regarded as monophyletic, depending on the assumption that: d(i, j) > d(i, k) .~. t(i,j) > t(i, k) for all i,j and k, where i,.j and k are taxa, d denotes the degree of phenetic difference between a pair of taxa, and t the time since their evolutionary divergence. The greater the degree of isolation, the greater the deviations from this assumption that are tolerable for the phyletic inference to hold. Secondly, the semi-geological evidence that Braun-Blanquet used is tenuous. The arguments about palaeoendemics lacking plasticity are unsatisfactory: restricted endemics are almost by definition restricted in habitat (it is seldom proved experimentally that they have strict requirements), lack of plasticity is generally inferred from supposed ecological specialisation, and lack of expanding power from spatial restriction.
A STUDY IN ENDEMISM:
Silene diclinis
25
(2) Endemics are also classified according to their past distributions. Briquet (1901) called these 'end6miques par conservation' and 'end6miques par novation', Ridley (1925) 'epibiotics' and 'endemics' and Chevalier & Cu6not (1927) 'pal6oend6miques' and 'neo-end6miques'. Several other terminologies have been used in this context. Palaeoendemics sensu Chevalier & Cu6not are 'relict', surviving in one part of what was previously a larger area, and neoendemics have arisen in situ and not yet spread further. It is possible that the idea of relictual species being old has arisen from an idea of 'age and area' .(see Willis, 1922), an 'old' taxon being presumed to have occupied a large area. Therefore, finding 'old' taxa as endemics, they are thought of as relicts, as by Engler (1882) and Briquet (1901). Similarly 'relict' species, having once occupied a wide area, ate considered to be 'old'. This equation is probably fair, but only in a very approximate sense. (3) Favarger & Contandriopoulos (1961) and Contandriopoulos (1962) discuss a new system of categories. They attack previous approaches to endemism, pointing out that, generally, whatever the definitions and supposed evidence, well-defined taxa have been categorised as palaeoendemics and ill-defined taxa as neoendemics. Favarger & Contandriopoulos arrive at a cytological classification of endemics containing four categories. Their 'pal6oend6miques' are defined as being isolated systematically, old, and with little variation, not necessarily having arisen in their area of survival. 'Schizoend6miques' are produced as a result of'gradual speciation' (see Valentine, 1948 and 1949), having a common origin and identical chromosome numbers. 'Patroend6miques' are restricted diploid endemics which give rise to widely-distributed polyploids, and 'apoend6miques' are polyploid species of restricted area which have arisen from widely-distributed diploid ancestors. The term 'cryptoend6mique' is added as an extra to cover unrecognised cytological races. Favarger & Contandriopoulos make the assumption that a polyploid has arisen from a morphologically similar diploid, and not the reverse. However, a polyploid has not necessarily arisen from a related present-day diploid unless an absurdly strict cytological view of species is adopted. Their category 'pal6oend6mique' encompasses both possible earlier definitions and is in no sense new. Gaussen & Leredde (1949) have proposed a neutral terminology: 'megaend6miques' and 'microend6miques' are defined respectively as 'Linnaean' and 'non-Linnaean' or microspecies. This terminology has no connotations of age or evolutionary origin.
EVIDENCE CONCERNING THE HISTORY OF
S. diclinis
How, then, can one suggest hypotheses about the origin of an endemic and its present isolation, and can any evidence be found in the case of S. diclinis?
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One means o f obtaining convincing evidence about the origin o f a taxon is to carry out crossing experiments. In this manner it is sometimes possible to synthesise a species artificially. The development of new hybrids can be watched in the wild. The production of hybrids between two species has been taken to mean that they are closely 'related'. This assumption is unsatisfactory if one is to allow for sterility barriers being built up between sympatric species (see Stebbins, 1966, Chapter 5). S. alba also occurs on the Sierra del Castillo very near to S. diclinis, yet there are no hybrids present and I have, so far, been unsuccessful in producing such hybrids in cultivation. Morisset & Bozman (1969) produced fertile hybrids between S. heuffelii and S. diclinis. I have successfully repeated this cross and have also produced fertile hybrids between S. diclinis and S. dioica. Nevertheless, this interfertility should be taken as no more than vindication of the grouping already based on morphological similarity. One can only say that S. diclinis bears most resemblance to the other members of section Elisanthe and that crossing experiments confirm this relationship. One could imagine (see remarks above on phyletic inferences) S. diclinis becoming distinct within section Elisanthe more recently than the whole section became distinct from the rest of Silene. Pollen and macrofossil analysis can aid the study of endemics in two ways: direct evidence can be obtained on the past distribution of a taxon, and the vegetation and palaeoenvironment of large areas can be investigated and used as a better foundation for suggesting hypotheses about their history. A combination of these approaches led to Pigott & Walters' (1954) convincing explanation of the disjunctions of some rarer British plants, some of which have been shown to have been widespread in the open-vegetation of the Late-Devensian and persisting now only in 'refugia'--habitats such as gorges and inland cliffs where the forest cannot have been present during the Flandrian forest maximum. Unfortunately, pollen, widely-dispersed, is often not identifiable to species level and macrofossil finds are more dependent on chance. Since S. diclinis has never been found as a fossil, there remains only indirect evidence: detailed knowledge of a plant's present environment and knowledge of the palaeoenvironment of a wide surrounding area can be combined to suggest the origin of endemic distributions, as was done by Montserrat & Villar (1972) in their study of Spanish endemism. The Sierra del Castillo is of Cretaceous limestone, but the surrounding area carries Miocene deposits, so S. diclinis must have evolved or become restricted to its present area not before the Cretaceous and probably in, or after, the Miocene. It is difficult to be more precise about the emergence of the area, since Quaternary Mediterranean sea levels are very difficult to correlate (see Hey, 1971). Knowledge of Tertiary floras and associated environments is fragmentary, based mainly on leaf-beds, e.g. Menrndez Amor (1948). A more coherent picture o f Quaternary palaeoenvironments in the Mediterranean region has emerged f r o m p o l l e n analysis of long cores, especially from Macedonia (Wijmstra, 1969),
A STUDY 1N ENDEMISM"
Silene diclinis
27
Syria (Niklewski & van Zeist, 1970), northern Italy (Frank, 1969) and southern Spain (Florschiitz et al., 1971); see also Bonatti (1966). It appears that the periods of maximum glaciation in high latitudes have been consistently characterised by Steppe-like vegetation with abundant Artemisia, Ephedra, Chenopodiaceae and Caryophyllaceae; the Steppe affinities are reinforced by electron microscope identification of certain Chenopodiaceae (Smit & Wijmstra, 1970) now restricted to areas much further east. By implication the climate is taken to have been cool and semi-arid. This contrasts with earlier views and does not suggest that the biogeographic effects of Quaternary events should be underplayed (cf. Montserrat & Villar, 1972). The interglacials and interstadials of high latitudes were characterised by mixed forest. At about 10,000 BP forest cover dramatically increased. Evergreen oak forest was widespread during the Flandrian (Beug, 1966) and there is evidence of man having cleared these forests (see Brande, 1973). The present habitat of S. diclinis is man-made and does not suggest any reason for its localisation. Its association with the Sierra del Castillo is more striking. In the light of geological evidence, an attractive hypothesis is that S. diclinis has been restricted by the widespread forests of 'interglacial' and Flandrian times to a habitat that has remained open, possibly failing to colonise man-made open habitats at any distance from its refugium. This is only a hypothesis and there is no evidence to discount S. diclinis having evolved in situ.
THE GENETIC SITUATION IN A RESTRICTED ENDEMIC
Wright (1969) sets out mathematically the theory of genetic drift in non-adaptive characters within populations. Some of the implications of this theory are discussed by Dobzhansky (1951, p. 363). It is predicted that in 'small' gamodemes there should be increased homozygosity and decreased polymorphism, and that selective values should have little effect, i.e. random genetic drift should be a major influence on evolution. The theory does not predict what constitutes a 'small' population since this can only be defined in relation to unknowns such as the mutation rate. The theory does predict that, in a fluctuating population, the minimum size is critical. Little work has been carried out along these lines using plants, and Wright's theory remains untested in wild populations. It would therefore be very interesting to have information on gene frequencies in an outbreeding and highly localised and definable plant population such as that of S. diclinis. S. diclinis has evident variation in flower size, shape and colour in its natural habitat (e.g. from a sample of 13 flowers from as many male plants, petal claw length has mean 14.2 mm and standard deviation 2.31 mm; corolla diameter, mean 16.2 ram, standard deviation 4.41 mm). This degree of variation is maintained in cultivation and is, therefore, presumably genetically based. This contrasts
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with the situation found in another species of Silene, S. viscariopsis Bornm., a similarly restricted but hermaphrodite and self-fertile Jugoslavian endemic (S. M. Waiters, pers. comm.). The possible inference from this subjective comparison could be tested by allozyme studies (which have been surprisingly neglected in plants: see Lewontin, 1974, p. 120).
CONSERVATION
S. diclinis on the Sierra del Castillo consisted, in 1974, according to my estimates, of a population of about 600 individuals. One must treat its position as precarious. Of course there is no evidence for how long it has existed as such a small population. There are many impending threats to the survival of S. diclinis in the carob groves of the Sierra del Castillo. Like many of the Greek and Turkish endemics, for example, it is existing solely in a man-made habitat (see Melville, 1970-). I have speculated that it once inhabited the limestone ridge above the groves. Increasing cultivation o f the groves would probably lead to the walling-up of the terrace banks or the use of weed-killers as in surrounding well-worked groves. Both changes, particularly the latter, could jeopardize S. diclinis. The complete abandonment of the groves would almost certainly allow Pinus halepensis, already present nearby (see Figs. 3 and 4), to engulf the area, as in many derelict groves throughout the Mediterranean. Little can compete with the pine thickets. A slight change in the grazing area of the local herds of goats could reduce the substratum of the groves to a dry, bare hillside like that to the north-east. Seed banks provide a way in which stocks of rare plants can be maintained (see Thompson, 1974) and increased by hand-pollination of cultivated plants. It is necessary to grow a large number of individuals for such hand-crossing, to ensure that as much genetic variation as possible is kept in the seed stocks. The distribution of seed to as many seed banks as possible will also help to ensure the retention o f the genetic variation. Seed of S. diclinis was sent to the seed bank at Kew in 1974. Seventy plants were raised in the Botanic Garden at Cambridge and were hand-pollinated in 1975 to produce more seed. Half of this was sent to Professor C. Gomez-Campo at Madrid for his seed bank of Spanish endemic plants, and half has been retained at Cambridge for further bulking-up and subsequent distribution. Some endemic plants, by virtue o f their attractiveness to alpine gardeners in particular, have become widespread in cultivation (see Melville, 1970-). Although the species will suffer selection for its most handsome forms, this is nevertheless another way in which stocks of rare plants can be increased. Seed and plants of S. diclinis have been distributed to a number of alpine gardeners. Information on S. diclinis has been added to the Index of Rare Endemic Vascular Plants of Europe which Dr S. M. Walters is compiling (see Walters, 1971) and will also be included in a future addition to the Red Data Book.
A STUDY IN ENDEMISM: Silene diclinis
29
It is hoped that these steps will help to preserve S. diclinis, at least in cultivation, if one takes the most pessimistic view o f its future in the wild. The data I have collected could form a provisional basis for any possible future attempts to conserve the species in the wild.
ACKNOWLEDGEMENTS
My supervisor, Dr S. M. Waiters, has encouraged my interest in endemism and I would like to thank him for all the ideas that he has given me, for his excellent guidance and for critically reading this paper. Professor C. G 6 m e z - C a m p o has been most helpful and kindly provided me with maps. Professor S. Rivas Martinez kindly examined the Jfitiva relev6s and commented on their phytosociological affinities. Dr H. J. B. Birks determined the mosses collected from the J~itiva relev6s and Mr P. D. Sell determined the composites. I am most grateful to Mr B. Huntley who analysed the soil samples and to Mr Jack Symonds o f the University Botanic Garden, Cambridge, for looking after my cultivated stock o f S. diclinis. Dr H. L. K. Whitehouse and Dr D. Briggs gave advice on the genetic aspects of this paper and Dr R. W. Hey discussed aspects o f Mediterranean geological history. This work was supported by a Science Research Council research studentship which is gratefully acknowledged. Finally, I would like to thank my husband, Colin, for help with the fieldwork and for his constructive criticism during the writing of this paper.
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