Richness and endemism in Asclepiadoideae ... - Springer Link

Biodiversity and Conservation 11: 1733–1746, 2002.  2002 Kluwer Academic Publishers. Printed in the Netherlands.

Richness and endemism in Asclepiadoideae (Apocynaceae) from the Espinhaç o Range of Minas Gerais, Brazil – a conservationist view ALESSANDRO RAPINI 1, *, RENATO DE MELLO-SILVA1 and MARIA ´ LUCIA KAWASAKI 2 1

˜ Paulo, Caixa Postal 11461, ˆ ˆ , Instituto de Biociencias , Universidade de Sao Departamento de Botanica ˜ Paulo, SP CEP 05422 -970, Brazil; 2 Herbario ˜ Paulo, Caixa Postal ´ , Instituto de Botanica ˆ de Sao Sao ˜ Paulo, SP CEP 01061 -970, Brazil; * Author for correspondence (e-mail: arapini@ usp.br) 4005, Sao Received 19 April 2001; accepted in revised form 29 October 2001

Key words: Asclepiadoideae, Brazil, Campos rupestres, Collecting effort, Conservation areas, Endemism, Espinhaço Range, Minas Gerais, Species richness Abstract. The Espinhaço Range, located in the states of Minas Gerais and Bahia, has a type of vegetation with one of the highest degrees of endemism in Brazil: the campos rupestres. In this area, Asclepiadoideae is among the most diverse angiosperm groups, including species with broad distributions and others restricted to small areas. This study attempts to evaluate the species richness and the degree of endemism in this region, as well as the influence of collecting efforts on the perception of biodiversity. It is based especially on the Asclepiadoideae from the Espinhaço Range of Minas Gerais (ERMG), though a brief consideration of the situation in Bahia is also introduced. For comparative studies, the ERMG was ´ Diamantina Plateau, and North. The species were then divided into four regions: South, Serra do Cipo, characterized according to their distribution and occurrence in each of these regions. Ninety-seven species of Asclepiadoideae are native to the ERMG; about 30% of them are endemic to this area and almost 25% are restricted to only one of the four regions. The Serra do Cipo´ and the Diamantina Plateau present the highest degrees of endemism, and the highest richness in number of species is found in the South. Nevertheless, there is a progressive decrease in collecting efforts northwards, which may distort species distribution and occurrence, and lead to misinterpretations about centers of diversity and endemism. The Espinhaço Range should be considered vulnerable in its entirety because of the singular flora still incompletely known and the restricted distribution of many species. Programs that establish priority areas of conservation without considering the region as a whole will only offer temporary, partial protection for its biodiversity.

Introduction The degree of regional endemism is an important criterion used to select priority conservation areas (e.g. Gentry 1986; Roberts 1988); therefore, mountain ranges, traditionally recognized as high-endemism areas (Kruckeberger and Rabinowitz 1985), deserve special attention in preservation of biodiversity. Studies on Asclepiadoideae from small areas of the Espinhaço Range in the states of Minas Gerais (Fontella-Pereira et al. 1984; Giulietti et al. 1987; Fontella-Pereira et al. 1995) and Bahia (Goyder 1995), and the survey of Asclepiadoideae from the Espinhaço Range of Minas Gerais (ERMG) (Rapini et al. 2001) have confirmed the significant

1734 richness and endemism in the Espinhaço Range and, consequently, the importance of this mountain chain for conservation programs. This paper attempts to evaluate the knowledge of the Espinhaço Range flora and the influence of collecting efforts on this flora, as well as to discuss the conservation of biodiversity in the region, based especially on the Asclepiadoideae from the ERMG (Rapini et al. 2001). The Espinhaço Range is located in the states of Minas Gerais and Bahia, Brazil. It is about 1100 km long, oriented in the north–south direction (108–208359 S), 50–100 km wide, and with elevations above 800 m, reaching about 2000 m in some particular spots. This mountain chain has a substrate mainly composed of quartzite and sandstone formations, with acid and oligotrophic soils that are usually shallow and sandy. The region has 3–4 months of dry season in the winter and an annual temperature average between 17.4 and 19.8 8C. The vegetation is composed of cerrado (savanna) and gallery forests, but it is largely dominated by campos rupestres (rock fields), an open vegetation that usually appears at elevations above 900 m and is composed mainly of herbaceous and sclerophyllous evergreen shrubs or subshrubs (Giulietti et al. 1997; see also Harley (1995) for more details and photos of the region). Because of the isolation of its mountains and its special environmental conditions, the Espinhaço Range has a singular floristic composition, and its campos rupestres may represent the association with the largest ratio of endemic species in the Brazilian flora (Giulietti et al. 1987). Velloziaceae, Eriocaulaceae, and Xyridaceae are among the most typical taxa in the region, but many genera are also very representative in the Espinhaço Range (see Harley 1995; Giulietti et al. 1997; Giulietti and Pirani 1998 for references on patterns of geographical distribution), such as Camarea (Malpighiaceae, Mamede 1990), Chamaecrista (Leguminosae, Irwin and Barneby 1982), Declieuxia (Rubiaceae, Kirkbride 1976), Enchlolirium (Bromeliaceae, Forzza 2001), Eriope (Lamiaceae, Harley 1988), Lavosiera (Melastomataceae, Semir and Martins in Giulietti et al. 1987), Luxemburgia (Ochnaceae, Feres 2001), and Lychnophora (Asteraceae, Semir 1991). The Asclepiadoideae (Apocynaceae), traditionally recognized at the level of family (see Endress and Bruyns (2000) for a recent classification of Apocynaceae, and Rapini (2000a) for comments on the current taxonomic arrangement of the family), are among the most complex groups of dicotyledons. They are easily recognized by the pollinaria, which are composed of two pollinia of adjacent stamens united by a translator. The subfamily includes about 2500 species and is represented almost all over the world, mainly in the tropics and subtropics. South America is an Asclepiadoideae center of diversity (Good 1952) and, in Brazil, the group is very diversified. Represented by species either with broad distribution or restricted to small areas, Asclepiadoideae is one of the most diverse plant groups in the Espinhaço Range, at least in the state of Minas Gerais, as it has already been demonstrated in previous floristic inventories in the Serra do Cipo´ (Giulietti et al. 1987; Fontella-Pereira et al. 1995). The first important Asclepiadoideae collections from the Espinhaço Range were made by naturalists who visited Brazil in the 19th century: A.F.C.P. de Saint-Hilaire, ´ C.F.P. Martius, F. Sellow, J.B.E. Pohl, G. Gardner, and L. Riedel. Alvaro da Silveira

1735 made important collections in the Serra do Cipo´ in the early 1900s, and H.M. Barreto in the southern regions of the Espinhaço Range during the 1930s. Jose´ Badini and collaborators collected extensively in the region of Ouro Preto for about 50 years, while collections from Serra do Cipo´ have improved significantly since the 1970s, when A.B. Joly, followed by A.M. Giulietti, J.R. Pirani, and others, initiated a program of floristic studies in the locality. In the state of Bahia, R.M. Harley and collaborators explored mainly Mucugeˆ and Pico das Almas. Gert Hatschbach, H.S. Irwin, and many other researchers and students from several institutions have collected or are still developing floristic studies in regions of the Espinhaço Range, ˜ ´ such as Grao-Mogol and Catoles.

Material and methods This work is based on field studies and on material deposited in the most representative Brazilian herbaria for collections from the Espinhaço Range and / or of Asclepiadoideae: BHCB, BHMH, ESA, HB, HXBH, MBM, OUPR, R, RB, SP, SPF, UB, and UEC; and in three American herbaria: F, MO, and NY (herbaria acronyms according to Holmgren et al. 1990). For comparison purposes, the ERMG was ´ (2) Serra do Cipo, ´ divided into four regions: (1) South, from Ouro Preto to Caete; between Santa Luzia and Congonhas do Norte; (3) Diamantina Plateau, from Presidente Kubitschek to Itamarandiba, including Serra do Cabral; and (4) North, between Itacambira and Espinosa, near Bahia (Figure 1). The species of Asclepiadoideae from the ERMG were classified according to their distributions and regions of occurrence in the ERMG (Table 1; see the caption for acronyms used in the text). The numbers and percentages of collections, species in each type of distribution, and native species, as well as collecting effort (number of collections / number of species rate), were obtained for the ERMG and for each of its four regions (Table 2).1

Results In the survey of the Asclepiadoideae from the ERMG, 99 species were recognized (Table 1; see Rapini (2000b) for photos of many of these species and Rapini et al. (2001) for references, descriptions, material examined, comments, and illustrations of each species). Two of these, Gomphocarpus physocarpus and Calotropis procera, were introduced from the Old World [I]. Of the 97 native species, 63 also occur beyond the Espinhaço Range [A 1 O 1 R 1 )ER(1 )ERMG(], 25 of them 1

Despite the limitations of the procedures of systematics, taxonomy is still the main way to express biodiversity. Here, species were assumed as instruments for measuring biological richness and degrees of endemism in a region (but see e.g. Slobodchikoff 1976; Wilson 1999 for some general discussions about ¨ controversies on species concepts; and Peterson and Navarro-Siguenza 1999 for practical differences in the use of distinct species concepts to determine priority conservation areas).

1736

Figure 1. The ERMG (modified from the ‘International chart of the world on the millionth scale, Brazil’; ´ Diamantina Plateau, and North. The pies IBGE 1972) divided into four regions: South, Serra do Cipo, show the distribution of Asclepiadoideae species presumably associated to the campos rupestres of the Espinhaço Range. The white sector represents the amount of species with broad distribution. The sectors with gray and black represent the amount of species that occur predominantly or exclusively in the Espinhaço Range; the black sector representing species endemic to the respective region (see the text and Tables 1 and 2 for details). The diagram of regions at the top shows the number of native Asclepiadoideae species in each area; the number of endemic species is given between parentheses.

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Table 1. List of Asclepiadoideae species from ERMG, their distributions and regions of occurrence in the ERMG a . Species

Distribution

Region

1. Asclepias candida Vell. 2. A. curassavica L. 3. A. mellodora A. St.-Hil. 4. Araujia sericifera Brot. 5. Blepharodon ampliflorum E. Fourn. 6. B. bicuspidatum E. Fourn. 7. B. lineare (Decne.) Decne. 8. B. nitidum (Vell.) J.F. Macbr. 9. Barjonia chloraeifolia Decne. 10. B. erecta (Vell.) K. Schum. 11. Calotropis procera (Aiton) W.T. Aiton 12. Cynanchum montevidense Spreng. 13. C. roulinioides (E. Fourn.) Rapini 14. Ditassa acerosa Mart. 15. D. aequicymosa E. Fourn. 16. D. auriflora Rapini 17. D. bifurcata Rapini 18. D. capillaris E. Fourn. 19. D. cipoensis (Fontella) Rapini 20. D. conceptionis Fontella 21. D. cordeiroana Fontella 22. D. decussata Mart. 23. D. diamantinensis Fontella 24. D. ditassoides (Silveira) Fontella 25. D. eximia Decne. 26. D. fasciculata E. Fourn. 27. D. glazioui E. Fourn. 28. D. grazielae (Fontella) Rapini 29. D. hastata Decne. 30. D. hemipogonoides E. Fourn. 31. D. hispida (Vell.) Fontella 32. D. inconspicua Rapini 33. D. itambensis Rapini 34. D. laevis Mart. 35. D. lenheirensis Silveira 36. D. linearis Mart. 37. D. longicaulis (E. Fourn.) Rapini 38. D. longisepala (Hua) Fontella and E.A. Schwarz 39. D. lourteigiae Fontella 40. D. magisteriana Rapini 41. D. micromeria Decne. 42. D. monocoronata Rapini 43. D. mucronata Mart. 44. D. myrtilloides Fenzl ex E. Fourn. 45. D. obcordata Mart. 46. D. parva (Silveira) Fontella 47. D. pedunculata Malme 48. D. pohliana E. Fourn. 49. D. polygaloides Silveira 50. D. refractifolia K. Schum. 51. D. retusa Mart. 52. D. semirii (Fontella) Rapini 53. D. succedanea Rapini

A A A A A A O A (ER) A I O A A (ERMG) L Lb O L R L )ERMG( L )ERMG( (ERMG) (ERMG) O L O Lc O L L L )ERMG( )ERMG( )ER( L O Lb A L )ERMG( L A (ERMG) L O L L )ER( L )ERMG(

S/C/D S/C/D S/C/D S/C S / C / D/ N S/C S / D/ N S / C / D/ N C / D/ N S / C / D/ N D/ N N S / D/ N S / C / D/ N S/C/D N D N C S N S / C / D/ N D C / D/ N C/D C / D/ N N D N C D/ N D D S S/C/D S/C S/D S D C S / C / D/ N S S/C S S / D/ N S/C/D S N C D S / C / D/ N C C / D/ N

1738

Table 1. (continued) Species

Distribution

Region

54. D. tomentosa (Decne.) Fontella 55. Gomphocarpus physocarpus E. Mey. 56. Gonioanthela hilariana (E. Fourn.) Malme 57. Gonolobus selloanus (E. Fourn.) Bacigalupo 58. Gyrostelma oxypetaloides E. Fourn. 59. Hemipogon abietoides E. Fourn. 60. H. acerosus Decne. 61. H. carassensis (Malme) Rapini 62. H. furlanii (Fontella) Rapini 63. H. hatschbachii (Fontella) Rapini 64. H. hemipogonoides (Malme) Rapini 65. H. luteus E. Fourn. 66. H. piranii (Fontella) Rapini 67. Macroditassa adnata (E. Fourn.) Malme 68. M. melantha (Silveira) Rapini 69. Marsdenia altissima (Jacq.) Dugand 70. M. macrophylla (Humb. and Bonpl.) E. Fourn. 71. M. suberosa (E. Fourn.) Malme 72. Matelea denticulata (Vahl) Fontella and E.A. Schwarz 73. M. pedalis (E. Fourn.) Fontella and E.A. Schwarz 74. Metastelma burchellii (Hook. and Arn.) Rapini 75. M. scoparium (Nutt.) Vail 76. Nephradenia acerosa Decne. 77. Oxypetalum aequaliflorum E. Fourn. 78. O. appendiculatum Mart. 79. O. arachnoideum E. Fourn. 80. O. banksii Schult. 81. O. capitatum Mart. 82. O. erectum Mart. 83. O. erostre E. Fourn. 84. O. foliosum Mart. 85. O. glabrum (Decne.) Malme 86. O. insigne (Decne.) Malme 87. O. jacobinae Decne. 88. O. minarum E. Fourn. 89. O. montanum Mart. 90. O. pachyglossum Decne. 91. O. pachygynum Decne. 92. O. pilosum Gardner 93. O. polyanthum (Hoehne) Rapini 94. O. rusticum Rapini 95. O. strictum Mart. 96. O. warmingii (E. Fourn.) Fontella and Marquete 97. O. wightianum Hook. and Arn. 98. Peplonia asteria (Vell.) Fontella and E.A. Schwarz 99. Tassadia propinqua Decne.

A I )ERMG( O R Ld A )ER( L L (ERMG) (ERMG) L O (ER) O O O O A O A O R A O O O A (ER) A )ERMG( A A )ERMG( (ER) A A O (ERMG) L )ER( A A O O

S S/C S/C/D S C C S / C / D/ N S / C / D/ N N C S / C / D/ N C/D C S/N C / D/ N S/C/N S D/ N S S/C S S/C D D S/C/D N S S S / D/ N S/C/D S/C/D S/C/D S/C S/C/D S C/D S S/C/D S C/D D S / C / D/ N S / C / D/ N S/C S D

a

´ D – Diamantina Plateau; I – A – ample distribution and common in the ERMG; C – Serra do Cipo; introduced (exotic); L – local endemic, restricted to only one region of the ERMG; N – North; O – broad distribution, but occasional (up to five collections) in the ERMG; R – rare (up to five collections), but occurring beyond the Espinhaço Range; S – South; )ER(– distributed predominantly in the Espinhaço Range (i.e. rare outside), occurring either in Bahia or in Minas Gerais; (ER) – endemic to the Espinhaço Range, but not restricted to the ERMG (i.e. also occurring in Bahia); )ERMG(– distribution predominantly in the ERMG (i.e. rare outside), but not occurring in the ERBA; (ERMG) – endemic to the ERMG, but occurring in more than one region. b Represented only from type collection. c Not collected in the last 100 years. d Collected only once and more than 100 years ago.

1739 Table 2. Regions of the ERMG with numbers and percentages of collections, species in each kind of distribution, native species and collecting effort a . Region Collections A

O

R

)ER(

(ER)

)ERMG( (ERMG) L

NS

CE

S

11 (19.3) 1 (1.92) 6 (11.54) 11 (32.35) 22 (22.68)

1 (1.75) 1 (1.92) 1 (1.92) – – 3 (3.09)

4 (7.02) 3 (5.77) 4 (7.69) 4 (8.82) 4 (4.12)

1 (1.75) 4 (7.69) 4 (7.69) 2 (5.88) 4 (4.12)

7 (12.28) 8 (15.38) 6 (11.54) 3 (8.82) 9 (9.28)

57 (58.76) 52 (53.61) 52 (53.61) 34 (35.05) 97 (100)

14.84

846 (44.15) C 499 (26.04) D 418 (21.82) N 153 (7.98) ERMG 1916 (100)

25 (43.86) 20 (38.46) 17 (32.69) 10 (29.41) 25 (25.77)

3 (3.51) 7 (13.46) 7 (13.46) 2 (5.88) 7 (7.22)

5 (8.77) 8 (15.38) 7 (13.46) 3 (8.82) 23 (23.71)

9.6 8.04 4.5 19.75

a

´ D – Diamantina Plateau; CE – A – ample distribution and common in the ERMG; C – Serra do Cipo; collecting effort (collections / NS); L – local endemic, restricted to only one region of the ERMG; N – North; NS – native species; O – broad distribution, but occasional (up to five collections) in the ERMG; R – rare (up to five collections), but occurring beyond the Espinhaço Range; S – South; )ER(– distributed predominantly in the Espinhaço Range (i.e. rare outside), occurring either in Bahia or Minas Gerais; (ER) – endemic to the Espinhaço Range, but not restricted to the ERMG (i.e. also occurring in Bahia); )ERMG(– distribution predominantly in the ERMG (i.e. rare outside), but not occurring in the ERBA; (ERMG) – endemic to the ERMG, but occurring in more than one region.

have broad distribution and are common in the ERMG [A], 22 species occasionally occur in the area [O], and Ditassa conceptionis, D. lourteigiae, and Oxypetalum aequaliflorum are rare [R]. Among the species that occur in the ERMG, 47 species are endemic to or occur predominantly in the Espinhaço Range [ER 1 ERMG 1 L], 30 are endemic to the ERMG [(ERMG) 1 L], and 23 are endemic to only one region [L]. Ditassa bifurcata and D. magisteriana are known only from their type collection, whereas D. diamantinensis is known from two collections, both from the same small population. Ditassa hemipogonoides has not been represented by any collection in the last 100 years and Hemipogon abietoides was collected only once and more than 100 years ago (Tables 1 and 2). Collections from the ERMG have indicated a greater richness in Asclepiadoideae in the South, which gradually decreases northwards. Nevertheless, the number of Asclepiadoideae collections also decreases from the South to the North; among the 1916 collections of Asclepiadoideae from the ERMG, almost 45% were collected in the South and less than 8% in the North. Collecting efforts are greater in the South, decreasing progressively towards the North. In the South, 57 native species of Asclepiadoideae were recognized in the 846 collections of the subfamily, resulting in an average of almost 15 collections for each species. On the other hand, in the North, there are 34 native species in 153 collections, an average of between four and five collections per species; i.e., a ratio of number of collections / number of species more than three times lower than in the South (Table 2). In the South and in the North, more than 60% of the Asclepiadoideae species have broad distribution [A 1 R 1 O], less than 15% are endemic to the ERMG, and less than 10% are endemic to only one region. On the other hand, in the Serra do Cipo´ and in the Diamantina Plateau, less than 50% of the species have broad distribution,

1740 more than 25% are endemic to the ERMG, and about 15% are endemic to only one region (Table 2). Differently from the South and the North, in Asclepiadoideae, most species from the Serra do Cipo´ and Diamantina Plateau occur exclusively or predominantly in the Espinhaço Range and then might present a strong association with its campos rupestres (see pies in Figure 1). Almost 75% of the species endemic to the ERMG occur in the area including these two regions, and about 80% of them are restricted to this area. Furthermore, of the 70 native species from the area of Serra do Cipo´ and Diamantina, 18 (ca. 25%) are only found in this area, confirming its high degree of endemism (see diagram in Figure 1).

Discussion Endemism and endangered species The occurrence of Asclepiadoideae species with broad distribution is common in the Espinhaço Range, mainly in the South. Species from this region are also found in other areas of campos rupestres of southern Minas Gerais (e.g. O. minarum and D. linearis, which also occur in Ibitipoca) and in other states, mainly of southern and southeastern Brazil, and Bahia (e.g. O. banksii and P. asteria, characteristically restricted to coastlands). Nevertheless, the large number of Asclepiadoideae species endemic to the ERMG confirms the rate of 30% that was previously estimated for endemism in the campos rupestres flora (Giulietti et al. 1987), corroborating the singularity of the flora of these mountains and the strong association of many species to its campos rupestres. Among the 14 species of Asclepiadoideae on the Minas Gerais list of endangered species (Mendonça and Lins 2000), nine (i.e. about 64%) occur in the ERMG. The distribution of many Asclepiadoideae species from the Espinhaço Range, however, suggests that many other names should be added to this list. Most species that are endemic to the ERMG include plants that are restricted to small areas and probably adapted to a unique type of environment, which makes them vulnerable. This is even more explicit in species that are endemic to only one region or locality, i.e. almost 25% of the Asclepiadoideae species from the ERMG. In the Espinhaço Range, species are frequently represented by only one collection, and others have not been recollected in the last 100 years. The first collection of D. magisteriana was made in 1998, on an alternative road on the western slopes of ´ a presumably well-explored region. Possibly, D. hemipogonoides and Serra do Cipo, H. abietoides are not extinct, as suggested on Mendonça and Lins’s (2000) list, but ´ These rather they may represent taxa restricted to very small areas of Serra do Cipo. areas, however, might not be on the route used by collectors in the last 100 years, ˜ do Mato Dentro, basically the road MG-010, between Lagoa Santa and Conceiçao ´ Among the and which encloses only a small portion of the Serra do Cipo. Asclepiadoideae species from the ERMG, only D. monocoronata seems to be on the verge of extinction; this taxon has been recently described and is found exclusively

1741 on Serra do Itabirito and Serra do Rola-Moça, two localities that have been intensively exploited for mining. Collecting efforts and species richness Collecting effort should be emphasized in discussions on distribution, biodiversity, and endemism. Based on the Asclepiadoideae from the ERMG, a much greater collecting effort was made in the South, which has been intensively explored since the first botanical expeditions in Brazil, decreasing progressively towards the North. The species richness in a region is not directly proportional to the collecting effort but, in view of the substantial differences among the four regions of the ERMG, an increase in the number of species would be expected in some of these regions, mainly northwards. ´ which is the There are 499 collections of Asclepiadoideae from the Serra do Cipo, second most collected region in the ERMG. Nevertheless, Fontella-Pereira et al. (1995) added 14 species of Asclepiadoideae to Fontella-Pereira’s preliminary list in Giulietti et al. (1987) and, more recently, in the studies on ERMG Asclepiadoideae ´ Thus, almost (Rapini et al. 2001) 10 new records were added to the Serra do Cipo. 25% of the Asclepiadoideae species that were found in this region were unknown there less than a decade ago. In spite of continued expeditions, the uneven sampling in the total area of Serra do Cipo´ has probably generated misleading data on the real distribution of several species and underestimated its species richness, as it has also been demonstrated in other tropical regions (e.g. Prance et al. 2000). Almost 90% (51 species, or more if historical collections deposited in European herbaria were considered) of the native Asclepiadoideae species from the South were collected there since 1938. In the North, on the other hand, about 20% (seven species) were collected only in the last 2 years and almost 40% (13 species) were collected only once in that region. Whereas there is a large number of historical collections (before 1930) from the South, more than 99% of the Asclepiadoideae collections from the North were obtained after 1967. Itacambira (a region in the North), for instance, was first visited in 1984; until 1997, only four expeditions were made to that locality and seven species had been collected there. Less than 1 day of collecting by two of these authors, in March of 1999, was enough to add three new records, which means an increase of more than 40% in the formerly known species ˜ of Asclepiadoideae from these mountains. Grao-Mogol, the locality in the North more often visited because of floristic studies in development by the Universidade ˜ Paulo, had an increment of three Asclepiadoideae species in 2 days of work, de Sao which is an increase of more than 15% in the previous inventory. In the Espinhaço Range, groups typical of campos rupestres, such as Declieuxia (Kirkbride 1976; personal communication) and Velloziaceae, present an apparent decrease in their diversity northwards. Based on simple observations, the same seemed to hold for Asclepiadoideae, and, in general, for the Espinhaço Range flora as a whole. Many plant groups in the Espinhaço Range, however, have a limited period of flowering and fruiting, in most cases presumably regulated by the frequency of rains; this could be also observed in Asclepiadoideae. Despite

1742 variations, such as A. mellodora that reaches its peak of flowering period in October, most of the Asclepiadoideae flower and / or fruit in March, decreasing until July, when the amount of fertile collections is almost 12 times lower than in March (Figure 2). Therefore, in the absence of a systematic program of collecting, phenology may drastically influence the perception of the biodiversity of a particular region that is visited only a few times during the year. Espinhaç o Range of Bahia Although the phytomorphologies of campos rupestres in Bahia and Minas Gerais are similar, the floristic compositions in these states are distinct from each other. In the Asclepiadoideae from the ERMG, for instance, few species endemic to the Espinhaço Range are shared with Bahia. Of the 47 species of ERMG that show strong association with the campos rupestres, about 83% are not represented in Bahia. Despite the increment of studies in the Espinhaço Range of Bahia (ERBA), the floristics of the region is still poorly known. The amount of Asclepiadoideae collection from ERBA is about 10% of that from ERMG and only three small areas have received special attention. Florula of Mucugeˆ (Harley and Simmons 1986), with four Asclepiadoideae species, has only five collections representing the group. Sixteen species were recognized in the 25 Asclepiadoideae collections included in the Flora of Pico das Almas (Goyder 1995); i.e. an average of less than two collections per species. It is not hard to understand, therefore, why several Asclepiadoideae species that were not included in that survey, e.g. A. mellodora (Hind PDC 4396), D. acerosa (Hatschbach 56761), D. hastata (Harley et al. 5003), D. obcordata (Harley 27122a), and M. altissima (Sarr et al. PDC 5094), have been ´ (Goyder and Rapini found in the Pico das Almas. The Asclepiadoideae from Catoles in Zappi et al., in preparation), the third area considered in the ERBA, have until now about 70 collections representing 24 species. Although the area has nearly three

Figure 2. Distribution (%) of the Asclepiadoideae (black columns) and A. mellodora (white columns) collections from ERMG, showing the variation of flowering and / or fruiting intensity along the year.

1743 times more collections than Pico das Almas, the collection effort (average of about three collections per species) is still below the one obtained for the region North of Minas Gerais, which has the lowest collection effort in ERMG. The decrease in collections northward along the Espinhaço Range in the state of Minas Gerais noted above and the uneven collection effort along the range continue into the state of Bahia. Despite this, it is still clear that endemism is also significant in that part of the Espinhaço Range. Metastelma myrtifolium Decne. is endemic to the ERBA, and several Asclepiadoideae species recently described, such as M. harleyi Fontella and M. giuliettianum Fontella (Fontella-Pereira 1986), Barjonia harleyi Fontella (Fontella-Pereira 1987), Cynanchum morrenioides Goyder (Goyder 1993), and Melinia harleyi Fontella (Fontella-Pereira 1994), seem to be restricted to small areas in the ERBA.

Conclusions In the ERMG, the Serra do Cipo´ and the Diamantina Plateau have presented the highest levels of Asclepiadoideae endemism, and the South is the richest region in number of Asclepiadoideae species. The uneven collecting efforts, however, have probably resulted in an incomplete knowledge of species distribution, providing misleading data about the diversity and endemism in the regions of the ERMG. Since the uniqueness of some regions that are considered priority areas for conservation may be only an artifact of sampling (e.g. Nelson et al. 1990) and several regions in the Espinhaço Range remain incompletely known botanically, a comparative evaluation cannot be made throughout the area. Consequently, it would be premature to select any of its regions as a priority area for conservation based on floristic approaches. Studies concerned with conservation in Minas Gerais (Costa et al. 1998) indicated the Espinhaço Range as an area of special biological importance. It presents a high degree of plant and vertebrate endemism, anthropological relevance, and an important hydric potential. The campos rupestres have the largest number of endangered species among the biomes of Minas Gerais and about 40% of the endangered plant species of this state occur in the Espinhaço Range. Nevertheless, the large number of species endemic to small areas and the limited period of flowering and fruiting, as well as the restricted areas repeatedly explored by most collectors may explain the absence or scarceness of recent collections of some species. In the Espinhaço Range, probably few species are severely threatened, but many are vulnerable because of their small area of distribution. Therefore, as multidisciplinary evaluations (Costa et al. 1998) previously concluded, conservation strategies to protect the whole area of the Espinhaço Range are needed. Isolated parks, such as the Chapada Diamantina in Bahia, and the Serra do Cipo´ in Minas Gerais, because of the high degree of local endemics in the Espinhaço Range, only preserve a small amount of taxa and, therefore, not a representative sample of the biodiversity of these mountains. This is especially true when inter-population genetic variability is also considered (Jesus et al. 2001). The Espinhaço Range

1744 presents low human pressure (Costa et al. 1998); its soil is unsuitable for agriculture and the irregular terrain makes human occupation difficult. The main economic, but largely depredatory, activities in the region are mineral extraction, cattle raising, cultivation of Eucalyptus, and seasonal harvesting of ‘everlastings’ (mainly species of Eriocaulaceae, pipewort family, see Giulietti et al. 1996, 1998). Along its extension, however, there are many natural attractions and some of the most important Brazilian historical cities, which encourage tourism in the region. It would be especially relevant to establish social and economic strategies to protect the whole region, promoting tourism and restricting depredatory activities. Large protected areas will also ensure biological interactions, a significant aspect that should not be ignored in conservation programs (Mori 1989). In addition, this kind of program would also be economically more viable, since the maintenance of multiple small parks or reserves is usually more complex and expensive than the maintenance of a large one (Simberloff 1988). Strategies concerned with the reallocation of economic activities would contribute to the conservation of the Espinhaço Range in its entirety and then to preserve the unique biodiversity of the campos rupestres.

Acknowledgements We thank P.T. Sano for his critical reading, J.R. Pirani for discussions, J.H. Kirkbride Jr. for his careful revision of an initial version of the manuscript, and D. Goyder for helpful suggestions and English revision of a later version. This work is ˜ Paulo part of the first author’s Ph.D. Thesis undertaken at the Universidade de Sao ˜ de Amparo a` Pesquisa do Estado de Sao ˜ Paulo (USP) and funded by Fundaçao ˜ de Aperfeiçoamento de Pessoal de Ensino Superior (FAPESP) and Coordenaçao (CAPES) foundation. R.M.S. and M.L.K. have fellowships from Conselho Nacional de Pesquisa (CNPq).

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