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Composicion en elementos minerales en Antirrhinum subseccion Streptosepalum (Plantaginaceae) en Europe Occidental (Peninsula Iberica).

Mineral element composition in antirrhinum subsection Streptosepalum (Plantaginaceae) in Western Europe (Iberian Peninsula)

INTRODUCTION

The serpentinization of ultramafic rock is a common process in which the original rock changes its mineralogical composition owing to hydration of the original phases (O'HANLEY, 1996). The chemical composition of serpentinites depends on the nature of the original rock and on the origin of the fluid phase (PEREIRA & al., 2003), and this origin will also be reflected in the newly formed serpentinite group minerals. The serpentinicolous soils originated from different types of ultramafic rocks occur throughout the world and quite often in the form of ecological and/or pedological islands (LEFEBVRE & VERNET, 1990). Due to different anomalies in their physical and chemical properties, these soils represent an environment that is very hostile for plant life (RAJAKARUNA & BOYD, 2009). The slow erosion of the rocks, the intense heating of such rocks under conditions of extreme insolation, the rapid loss of water and strong pedological stress all contribute the making serpentines a highly xeric and very hostile substrate for vegetation, such that these materials represent an important route for the evolution of certain plants; i.e., those known as "serpentinophytes" (RODRIGUEZ-OUBINA & ORTIZ, 1995; IZCO & FERNANDEZ, 2001; LAZARUS & al., 2011).

Our work has focused on two important ultramafic massifs in the northwestern Iberian Peninsula: the Vinhais-Braganga and Morais Massifs. These ultrabasic areas of the north of Portugal occupy approximately 80 [Km.sup.2] (33 [km.sup.2] in the municipalities of Vinhais and Braganga, and 47 [km.sup.2] in the municipalities of Macedo de Cavaleiros and Mogadouro), and are situated between N 41[grados]25' and 41[grados]54', with an altitude between 450 and 1950 m.a.s.l. (PINTO DA SILVA, 1970).

The genus Antirrhinum consists of 24 perennial species that are native to the western Mediterranean (SUTTON, 1988; GUEMES, 2009). Most occur as narrow endemics on the Iberian Peninsula (GUEMES, 2009), and several are subject to different forms of threat (TORRES & al., 2003; BERNARDOS & al., 2006; GARCIA-BARRIUSO & al., 2011).

Speciation within the genus probably occurred first on the Iberian Peninsula as a result of drought during the Cenozoic period and the climatic changes following the Last Glacial Maximum (LGM, [approximately equal to] 20.000 years BP), with a climate in the Mediterranean basin that was first cooler (between 15 and 5 kyr BP) and wetter during the Nabtian Pluvial (between 10 and 6 kyr BP, REEDER & al., 2002; DUCASSOU & al., 2009), thereafter becoming a warmer and drier climate at about 6000 years ago (REEDER & al., 2002; DUCASSOU & al., 2009). These climate changes created some fragmented distributional areas (ROTHMALER, 1956; VARGAS & al., 2004).

Antirrhinum section Antirrhinum subsection Streptosepalum (ROTHMALER, 1956) includes A. braun-blanquetii Rothm. A. meonanthum Hoffmanns. & Link, and A. rothmaleri (Pinto da Silva) Amich, Bernardos & Garcia-Barriuso (GARCIA-BARRIUSO & al., 2012). The three species are endemic to the north and northwest of the Iberian Peninsula (GUEMES, 2009; GARCIA-BARRIUSO & al., 2012). Antirrhinum rothmaleri is a strict serpentinophyte of the Morais and Vinhais-Braganga massifs in the N of Portugal. Antirrhinum braun-blanquetii lives on limestone substrates, while A. meonanthum preferentially grows on siliceous materials (slates, schists and granites).

In this study, the accumulation of major and trace element composition (Ni, Ca, Mg, Fe, K) and their distribution in several plant species of Antirrhinum sect. Streptosepalum in the Iberian Peninsula was analysed. It is proposed that plant metal accumulation will be predictable from the soil bioavailable metal fraction.

The aims of the present work were: (1) to characterize the populations of Antirrhinum rothmaleri growing in areas of serpentinized rocks in NE Portugal and to compare them with Iberian populations of Antirrhinum braun-blanquetii and A. meonanthum via analyses of dry leaf matter and major and trace element contents, and (2) to characterize the pH of the soils and the composition of the rocks where populations of Antirrhinum rothmaleri are found, since this species behaves as a rupicolous or subrupicolous species.

MATERIAL AND METHODS

SAMPLING FOR ROCK AND SOIL ANALYSES

Rock samples were taken from the sites of all the populations of A. rothmaleri encountered (in Alimonde, Chacim-Balsemao and Gralhos). Major and trace elements were determined using acid treatment (HN[O.sub.3] plus HF) under pressure in an Ethos Sel microwave digestor from Milestone. The diluted solution was buffered with boric acid. Determination was performed with an Ultima 2 jobin Yvon optical emission plasma spectrometer at the Chemical Analysis Laboratory of the University of Salamanca.

Loss-on-Ignition (LOI) is a test used to measure the amount of moisture that a sample loses when it is ignited at certain temperatures (PE-REIRA & al., 2008). For this work, the LOI was calculated by measuring a few grams of powdered rock in a crucible, heating it to 950[grados]C in a muffle furnace, and allowing the water and other volatile elements to escape. After cooling in a controlled atmosphere, mass was re-determined and the difference was considered to be the LOI value.

Soil pH was determined in a soil/water (1:2.5) suspension with a pH-meter.

TAXONOMIC SAMPLING FOR ANALYSES OF MAJOR AND TRACE ELEMENTS IN DRY LEAF MATTER

Depending on the size the populations, between twenty one and thirty four plant samples (young green leaves) of each species were collected from natural environments of ultramafic areas in northern Portugal (A. rothmaleri), the province of Leon (A. braun-blanquetii) and the province of Salamanca (A. meonanthum) for analyses of major and trace elements (see Table 1, Fig. 1). Samples were air-dried and ground. About 0.1g of homogenized material was wet-ashed with 2 ml of concentrated HN[O.sub.3] in a Teflon pressure vessel at 150[grados]C for 10 h. The digest was finally made up to 10 ml with ultra-pure water. The solutions of rock samples were analyzed for their element composition (Al, Ca, Fe, K, Mg, Mn, Na, P, Si and Ti) using flame atomic absorption spectrophotometry (PERKIN-ELMER 2380; ASLIN, 1976; FLETCHER, 1981; KABATA-PENDIAS, 2001) at the University of Coimbra. The same rocks were analyzed for trace elements (Ba, Co, Cr, Cu, Ni, Pb, Sr and Zn) by ICP-MS at the Chemical Analysis Laboratory of the university of Salamanca. The solutions of plant samples were also analyzed for Ca, Fe, K, Mg and Ni by ICP-MS at the Chemical Analysis Laboratory of the University of Salamanca.

[FIGURE 1 OMMITED]

We performed an ANOVA test to analyse the differences between the three species of Antirrhinum, taking the major and trace element concentrations in leaf dry matter as explanatory variables (Ca, Fe, K, Mg, Ni), by means of SPSS (ANON., 2009).

A Garmin e-map GPS was used to locate the populations geographically using 1 x 1 km UTM and geographical coordinates. A representative voucher specimen from each population was collected and deposited at SALA.

RESULTS

ROCK AND SOIL ANALYSES

The serpentinized rocks of NE Portugal are massive, dense, and have a homogeneous structure. They often contain chromite crystals (VASCONCELOS FERREIRA, 1965). Tables 2 and 3 show the chemical composition in terms of the major and trace element concentrations of the ultramafic rocks where A. rothmaleri was found, together with the results reported by MENEZES DE SEQUEIRA (1969) for comparative purposes.

The degree of serpentinization is marked by the loss-on-ignition (LOI) parameter, in view of the high [H.sub.2]O content in the serpentine structure ([approximately equal to] 13% [H.sub.2]O) (D'ANTONIO & KRISTENSEN, 2004) (Table 2). The samples consisted of one serpentinite (Alimonde), and two serpentinized peridotites (Chacim-Balsemao and Gralhos).

The general characteristics of the serpentinites, including those of Portugal, are: (1) a high level of heavy metals, especially nickel; (2) high levels of [Fe.sub.2][O.sub.3] and, in particular, of MgO; and (3) low levels of calcium, potassium, and phosphorous (Tables 2 and 3).

The pH value in water showed little variation, varying between 7.33 and 7.40 (Table 4).

ANALYSES OF MAJOR AND TRACE ELEMENTS IN DRY LEAF MATTER

The concentrations of Ni and Mg were much higher in A. rothmaleri than in A. braun-blanquetii and A. meonanthum (Table 5), while the Ca concentration was much lower in A. rothmaleri. The [Mg.sup.2+/][Ca.sup.2+] ratio was < 0.5 in A. braun-blanquetii and A. meonanthum but > 1 in A. rothmaleri. Two of the three A. rothmaleri populations studied had clearly lower Fe and K concentrations than those seen for A. braun-blanquetii and A. meonanthum, while the remaining population (ARO 2) showed concentrations similar to those of the other taxa. Although all three A. rothmaleri populations grew on soils very rich in Fe (see Table 5), the ARO1 and ARO3 populations showed low concentrations of this element (8.6 and 7.5 % respectively), as they did for K (0.985 and 0.441 % respectively).

In light of the results of the analysis of variance, it may be concluded that the two explanatory variables were significant: Ni (F = 11.78, p = 0.038) y Ca (F = 19.12, and p = 0.020), but not for the other variables analysed: Mg (F = 1.041, p = 0.454), Fe (F = 3.530, p = 0.163), K (F = 0.783, p = 0.533).

The analyses revealed that even though the chemical composition of the serpentinized ultramafic rocks was similar at all three A. rothmaleri locations (Tables 2 and 3).

Despite some small differences, the habitat and ecology of A. rothmaleri are clearly reflected in its trace metal accumulation (Table 5). These plants appear to be perfectly adapted to soils developed from different types of ophiolitic bedrock, whose chemical and physical properties have long been known to produce an environment hostile to most plant life (Selvi, 2007). Unlike other serpentinophytes (i.e. Alyssum lusitanicum subsp. lusitanicum), A. rothmaleri does not thrive in soils disturbed by ploughing, mining, etc. (Fuente & al., 2007).

DISCUSSION

The adaptation of plant species to different soil types has been recognized as a consequence of the strong natural selection imposed by ecological discontinuities (WALLACE, 1858). The ecology of the three plant species analyzed here differs considerably: A. braun-blanquetii grows in the northern part of the Iberian Peninsula, on alkaline substrates in communities of the alliance Saxifragion trifurcato-canaliculatae (RIVAS-MARTINEZ & al., 2002); A. meonanthum is distributed over the NW quadrant of the Iberian Peninsula (slates, gneisses, granites) in phytocenoses corresponding to the alliance Parietario-Galion muralis (RIVAS-MARTINEZ & al., 2002); and A. rothmaleri lives on serpentinized ultramafic rocks in the northern of Portugal, in communities of the alliance Armerion eriophyllae (GARCIA-BARRIUSO & al., 2012, see Table V).

Apart from their different ecologies, the clear morphological differences between A. rothmaleri and A. braun-blanquetii and A. meonanthum (GARCIA-BARRIUSO & al., 2011) probably reflect phenomena of genetic divergence and reproductive isolation rather than the nutritional imbalances and toxicity of the ultrabasic soil where A. rothmaleri grows. A number of plant species endemic to metalliferous soils, such as A. rothmaleri, have been found to accumulate metals at extraordinarily high levels (> 1%), in contrast to normal concentrations in plants. This can be seen clearly in the values shown in Table 5.

Although examples of serpentinophytes have not been reported either for the family Plantagi naceae, in general, or in Antirrhinum in particular, it could be speculated, as has been proposed for other taxa (such as Silene dioica, WESTERBERGH & SAURA, 1992), that A. braun-blanquetii could have colonized serpentinicolous terrains several times independently, and could probably have been the ancestor of A. rothmaleri, with which it is closely linked (GARCIA-BARRIUSO & al., 2011).

It has been reported that the evolutionary transition of the serpentinicolous endemism may sometimes be exclusively unidirectional (ANACKER & al., 2011). If such speciation requires a relevant array of physiological and ecological adaptations and strategies to become adapted to serpenticolous soils this could lead to exclusion from non-serpentine zones and that this adaptation would be irreversible. The results obtained here suggest that in A. rothmaleri such adaptations and strategies did indeed occur and that it is now a restricted serpentinocolous endemism.

As in the case of other serpentinophytes, such as Notholaena marantae, and Onosma sp. pl. (PINTO DA SILVA, 1970; PICHI SERMOLLI, 1948; CECCHI & al., 2011), Antirrhinum rothmaleri could represent a pre-glacial relict, with its origin towards the beginnig of the Pleistocene, about 2.7 million years ago. As mentioned above, serpentines for an extremely xeric substrate, and those located in the Vinhais-Braganga-Morais massifs could have served as a refuge for different species inhabiting the northern part of the Iberian Peninsula during cold periods of the Pleistocene. Similar examples have been indicated for some taxa in other areas of Europe (STEVANOVIC & al., 2003; SELVI, 2007). Under these conditions, the populations could have been isolated and a strong selective pressure exerted by serpenticolous soils could have led to adaptive speciation.

doi: 10.5209/rev_LAZA.2012.v33.40278

ACKNOWLEDGEMENTS

We thank Dr. C. Aguiar (Technical College of Braganca, Portugal) for kindly showing us the serpentine areas in the Tras-os-Montes region, and Dr. P. Alonso Rojo (University of Salamanca, Spain) for laboratory analyses of soil pH.

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Recibido: 3 septiembre 2012

Aceptado: 11 octubre 2012

Monica Gama-Barriuso (*), Antonio L. Crespi (**), Cristina Nabais (***), Sonia Bernardos (*) & Francisco Amich (*)

* Evolution, Taxonomy and Conservation Group (ECOMED). Department of Botany. University of Salamanca. E-37005 Salamanca. E-mail: amich@usal.es.

** Centre for the Research and Technology of Agro-Environmental and Biological Sciences (CITAB). Herbarium/Botanic Garden. University of Tras-os-Montes e Alto Douro. P-5011-911. Vila Real.

*** Centre for Functional Ecology. University of Coimbra. P-3001-455 Coimbra.
Table 1

List of populations and number of plants (N) of Antirrhinum
representatives used for analyses of major and trace elements
in leaves (EL, *), and voucher number in SALA. Abbreviations:
PO, Portugal; SPA, Spain. Collectors: FA, F. Amich; SB, S.
Bernardos; MGB, M. Garcfa-Barriuso.

Taxon/Number and code of populations            N     EL   Voucher
/Origin and collection data

Antirrhinum braun-blanquetii

ABB1. SPA, Leon, Barrios de Luna, 1125 m, N     23    *    SALA 135487
  42[degrees]54' 21.1", W 5[degrees]53'
  18.3", 29.06.2007, FA & SB
ABB2. SPA, Leon, Busdongo de Arbas, 1205 m,     21    *    --
30TTN8062 (N 42[degrees]59' 3.9", W
  5[degrees]41' 34.4"), 15.07.2008, FA & SB
Subtotal                                        44

Antirrhinum meonanthum

AME1. SPA, Salamanca, San Esteban de la         33    *    SALA 135491
  Sierra, 750 m, 30TTK5388 (N 40[degrees]30'
  13.03", W 5[degrees]54' 25.78"),
  01.07.2008, FA & SB
Subtotal                                        33

Antirrhinum rothmaleri

ARO1. PO, Tras-os-Montes, Macedo de             34    *    SALA 135485
  Cavaleiros, Gralhos, near Nuestra Senora
  de La Salette, 625 m, 29TPF8799 (N
  41[degrees]31' 28.0", W 6[degrees]44'
  52.0"), 16.07.2007, FA, SB & MGB
ARO2. PO, Tras-os-Montes, Macedo de             21    *    SALA 135484
  Cavaleiros, Chacim,
  Monastery de Balsemao, 525 m, 29TPF7993
  (N 41[degrees]28' 30.1", W 6[degrees]51'
  21."), 26.07.2008, FA & SB
ARO3. PO, Tras-os-Montes, Braganca,             31    *    SALA 135483
  Alimonde, 730 m, 29TPG7429
  (N 41[degrees]47' 37.8", W 6[degrees]53'
  3.58"), 16.07.2007, FA, SB & MGB
ARO4. PO, Tras-os-Montes, Braganca,             --         SALA 135486
  Alimonde, road to Vila Boa, 670 m,
  29TPG7429 (N 41[degrees]47' 54.7",
  W 6[degrees]54' 12.9"), 03.07.2008,
  FA & SB
Subtotal                                        86
TOTAL                                           163

Table 2

Major element composition (%) of three rock samples in the
studied area. (b.d.l. = below detection limit)

Samples             LOI     Si[O.sub.2]           Ti[O.sub.2]

Menezes de          --      27-50                 Traces-0.6
  Sequeira (1969)
Alimonde (ARO3)     12.9    39.22 [+ or -] 2.88   0.01 [+ or -] 0.01
Gralhos (ARO1)      11.98   35.96 [+ or -] 2.76   0.12 [+ or -] 0.21
Chacim-Balsemao     11.77   39.02 [+ or -] 2.77   0.05 [+ or -] 0.02
  (ARO2)

Samples             [A.sub.2][O.sub.3]   [Fe.sub.2][O.sub.3]

Menezes de          0.05-7.6             6-13
  Sequeira (1969)
Alimonde (ARO3)     0.85 [+ or -] 0.11   7.61 [+ or -] 0.53
Gralhos (ARO1)      1.90 [+ or -] 0.23   10.83 [+ or -] 0.63
Chacim-Balsemao     1.41 [+ or -] 0.18   8.96 [+ or -] 0.59
  (ARO2)

Samples             MgO                   MnO

Menezes de          14-39                 0.06-0.20
  Sequeira (1969)
Alimonde (ARO3)     38.84 [+ or -] 2.98   0.09 [+ or -] 0.02
Gralhos (ARO1)      38.06 [+ or -] 2.96   0.10 [+ or -] 0.03
Chacim-Balsemao     38.16 [+ or -] 2.95   0.11 [+ or -] 0.02
  (ARO2)

Samples             CaO                  [Na.sub.2]O

Menezes de          0.05-25              0.25-1.17
  Sequeira (1969)
Alimonde (ARO3)     0.23 [+ or -] 0.04   0.05 [+ or -] 0.02
Gralhos (ARO1)      0.28 [+ or -] 0.04   0.01 [+ or -] 0.00
Chacim-Balsemao     0.84 [+ or -] 0.09   0.04 [+ or -] 0.01
  (ARO2)

Samples             [K.sub.2]O           [P.sub.2][O.sub.5]

Menezes de          0.02-0.17            --
  Sequeira (1969)
Alimonde (ARO3)     0.01 [+ or -] 0.00   0.01 [+ or -] 0.01
Gralhos (ARO1)      b.d.l.               0.03 [+ or -] 0.01
Chacim-Balsemao     b.d.l.               0.01 [+ or -] 0.00
  (ARO2)

Table 3

Composition in terms of trace-element concentration (ppm)
of three rock samples in the study area.
(b.d.l. = below detection limit)

Samples                  Ba                Co

Alimonde (ARO3)          11 [+ or -] 1.1   66 [+ or -] 7.01
Gralhos (ARO1)           b.d.l.            63 [+ or -] 6.87
Chacim-Balsemao (ARO2)   b.d.l.            61 [+ or -] 6.99

Samples                  Cr                    Cu

Alimonde (ARO3)          778 [+ or -] 18.9     b.d.l.
Gralhos (ARO1)           2264 [+ or -] 141.1   b.d.l.
Chacim-Balsemao (ARO2)   2536 [+ or -] 143.2   b.d.l.

Samples                  Ni                    Pb

Alimonde (ARO3)          2215 [+ or -] 140.4   b.d.l.
Gralhos (ARO1)           1835 [+ or -] 135.6   b.d.l.
Chacim-Balsemao (ARO2)   1961 [+ or -] 136.8   b.d.l.

Samples                  Sr                 Zn

Alimonde (ARO3)          70 [+ or -] 7.05   21 [+ or -] 2.1
Gralhos (ARO1)           63 [+ or -] 7.01   22 [+ or -] 2.1
Chacim-Balsemao (ARO2)   64 [+ or -] 6.88   32 [+ or -] 2.7

Table 4

Soil pH values for four populations of
Antirrhinum rothmaleri

Population   pH

ARO1         7.33
ARO2         7.38
ARO3         7.40
ARO4         7.39

Table 5

Major and trace element composition (%) in leaf
dry matter of Antirrhinum subsection Streptosepalum

Populations            Ni                   Ca

A. braun-              0.656 [+ or -] 0.09   2.18 [+ or -] 0.30
  blanquetii (ABB1)
A. braun-              0.750 [+ or -] 0.08   1.85 [+ or -] 0.29
  blanquetii (ABB2)
A. meonanthum (AME1)   0.358 [+ or -] 0.05   1.93 [+ or -] 0.30
A. rothmaleri (ARO1)   2.860 [+ or -] 0.39   0.84 [+ or -] 0.11
A. rothmaleri (ARO2)   1.770 [+ or -] 0.27   1.08 [+ or -] 0.27
A. rothmaleri (ARO3)   2.500 [+ or -] 0.31   0.64 [+ or -] 0.06

Populations            Mg                  Fe

A. braun-              0.95 [+ or -] 0.11   0.44
  blanquetii (ABB1)
A. braun-              0.31 [+ or -] 0.06   0.17
  blanquetii (ABB2)
A. meonanthum (AME1)   0.76 [+ or -] 0.09   0.39
A. rothmaleri (ARO1)   1.01 [+ or -] 0.12   1.20
A. rothmaleri (ARO2)   0.92 [+ or -] 0.11   0.85
A. rothmaleri (ARO3)   1.93 [+ or -] 0.29   3.09

Populations            K                  [Mg.sup.2+]/
                                          [Ca.sup.2+]

A. braun-              42.8 [+ or -] 4.1   1.667 [+ or -] 0.28
  blanquetii (ABB1)
A. braun-              21.7 [+ or -] 2.1   1.542 [+ or -] 0.25
  blanquetii (ABB2)
A. meonanthum (AME1)   11.5 [+ or -] 1.2   1.814 [+ or -] 0.28
A. rothmaleri (ARO1)   8.6 [+ or -] 0.9    0.985 [+ or -] 0.26
A. rothmaleri (ARO2)   42.1 [+ or -] 3.9   1.855 [+ or -] 0.29
A. rothmaleri (ARO3)   7.5 [+ or -] 0.9    0.441 [+ or -] 0.06
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Author:Garcia-Barriuso, Monica; Crespi, Antonio L.; Nabais, Cristina; Bernardos, Sonia; Amich, Francisco
Publication:Lazaroa
Date:Jan 1, 2012
Words:4100
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