anatomical considerations on spanish gypsophytes. where is their

Analele ştiinţifice ale Universităţii „Al. I. Cuza” Iaşi
Tomul LVII, fasc. 2, s. II a. Biologie vegetală, 2011
ANATOMICAL CONSIDERATIONS ON SPANISH GYPSOPHYTES.
WHERE IS THEIR PLACE WITHIN PLANT ECOLOGY?
M. – N. GRIGORE*, C. TOMA*, MARIA-MAGDALENA ZAMFIRACHE*,
MONICA BOŞCAIU**
Abstract: Several gypsophytes collected from gypsum soils (Tuejar, Spain) were histo-anatomically
investigated. Their anatomical features are discussed in relation to environmental conditions and possible
constraint factors occurring in these gypsic areas. The apparent xeromorphosis adaptations (intense lignification,
succulence, presence of protective hairs) could suggest that gypsophytes vegetate in habitats affected by physical
or physiological drought. However, the nature and position of these species in a distinct, well-defined ecological
class are largely commented.
Keywords: gypsophytes, physiological drought, gypsum, ecological class, conservation.
Introduction
Gypsophytes are plants growing exclusively on gypsum soils. The mechanism that
induces the restrictive occurrence of some species on gypsiferous soils is called gypsophily
[3]. The interrelationships between plants and gypsum substrate have been sporadically
mentioned during the time, starting yet from 18th century. Thus, Cavanilles [4], Boissier
[1], Willkomm [44], Contejan [10], Macchiati [22, 23, 24], Cockerell and Garcia [9]
referred to gypsophytes in their works. Most likely, Reyes Prósper [39] was the first author
using the term “yipsófilia” for delineate this ecological group of plants. However, Johnston
[21] has focused mainly on gypsophytes and explicitly introduced the words “gypsophily”
and “gypsophytes” as they are recognized until today. Later, Parsons [37] has reviewed the
concept in a deeper and pointed manner.
Nevertheless, despite a long history of gypsophytes concept (clearly or not
nominated), their status, and position within other “classic” ecological groups of plants are
still obscure. Intriguingly, gypsophytes are not included in any important monographs in
plant ecology – we use this term throughout present work as defined in a previous paper
[18]. Thus, in the plant ecology books such as those of Henslow [20], Warming [42, 43],
Schimper [41], and McDougall [26], there is no mention about gypsophytes. Surprisingly,
neither Clements [6, 7, 8] nor Warming [43] have not integrated gypsophytes in any
systems of ecological classification.
The occurrence of gypsophytes on gypsum soils is climate-dependent because it
only takes place in arid climates [3].
The nomenclature of gypsic areas may be a little bit confusing, but this seems to
be a common phenomenon in soil science, as in the case of saline soils [25; Mahjoory,
personal communication].
Nevertheless, gypsisols are soils with substantial secondary accumulation of
gypsum [46]. These soils are found in the driest part of the arid climate zone, which could
*
Alexandru Ioan Cuza University, Faculty of Biology, Bd. Carol I, no. 11, Iasi – 700506, Romania.
[email protected]
**
Instituto Agroforestal Mediterráneo, Universidad Politécnica de Valencia, Spain
31
explain why leading soil classification systems labeled many of them desert soils (in the
former Soviet Union). In The US Keys to Soil Taxonomy [45] gypsic soils are named
gypsids.
Gypsum soils spread over 100 million ha worldwide [46]. They are confined to
arid and semi-arid climates where low precipitation prevents gypsum from being removed
by leaching [37]. In addition to climatic conditions, gypsum soils have particularly stressful
physical and chemical properties for plant life [36]. Among the negative physical features
are the presence of a hard soil surface crust, which can affect seedling establishment [29;
12; 13]; the mechanical instability of the soil material caused by its lack of plasticity,
cohesion and aggregation [2]; and, in certain areas, its low porosity, which might limit the
penetration of plant roots [19]. Moreover, in semi-arid regions, the low water retention of
massive gypsum soils leads to a high infiltration of rainwater, which increases water deficit
during drought periods [19]. Chemically adverse features of gypsiferous soils are especially
related to the intense nutritional impoverishment of the soil caused by the exchange of
calcium for other ions retained in the soil complex [31; 19], and by the high concentration
of sulfate ions, which can be toxic for plants [11; 40].
Plant gypsophily has been explained in various ways. While some researchers
postulate physical constraints to account for gypsophily, others stress chemical or
nutritional requirements as causative factors [37; 28]. It is assumed that crusts either of
biogeneous (mostly lichens) or other origin (rocky edaphic horizons) and the hydric
performance of the superficial soil layer [30; 31] represent physical factors inducing
gypsophily. Some of the chemical hypotheses aiming at explaining gypsophily are
deficiency of macronutrients (N, K, and P), excess of others (Ca, Mg, and S), ionic
antagonism (Ca/Mg), and toxicity caused by micronutrients [33].
Materials and methods
The sample material subjected to our analysis is represented by leaves and stems
of two typical gypsophytes: Ononis tridentata L. ssp. tridentata (Fabaceae) and
Gypsophila struthium L. ssp. hispanica (Willk.) G. López (Caryophyllaceae). The
nomenclature of these species is according to Flora Iberica, adapted by Mota et al. [34, 35]
whose works are related especially to Spanish gypsophytes flora. These taxa are perennial
shrubs, and have been classified by Mota et al. [34] as “strictly (exclusively) gypsophytes”
(gipsófito estricto, in consulted paper). This means that species included in this category
grow exclusively on gypsum soils and only occasionally outside them. They were collected
in August of 2010 from Tuéjar (Valencia Province, Spain, Fig. 1), a region with important
gypsum areas. We have also collected Rosmarinus officinalis L., Thymus vulgaris L.
(Lamiaceae) and Helianthemum syriacum (Jacq.) Dum (Cistaceae), but anatomically
obtained data are not included in this present work.
For subsequent histo-anatomical investigations, the material was fixed and
preserved in ethanol (70°).
Sectioning of the leaf samples was made using a botanical razor and a microtome.
The cross sections thus obtained have been subsequently subjected to immersion in sodium
hypochlorite for 20-30 minutes, washing with acetic water and tap water, then staining: first
with iodine green (for 1 minute) and washing in ethylic alcohol (90°) bath then second with
red carmine (for 20 minutes), washing with water and finally fixation in glycerol-gelatine.
32
After obtaining permanent slides, micrographs have been taken using a NOVEX
(Holland) photonic microscope, with a Canon photo digital camera.
Results and discussions
Ononis tridentata L. ssp. tridentata
At the level of stem’ epidermis, there are located different types of hairs. Some of
them are protective, being very long, multicellular, and simple, with very thick, nonlignified walls. Others hairs are secretory, relatively long, with a multicellular stalk and
unicellular, spherical gland (Figs. 2 and 3).
The central cylinder of stem consists of 12-15 vascular bundles, separated by very
large medullary rays, and of a thick medulla (Fig. 4), whose cells are very big,
parenchymatic, with moderately thickened walls. All vascular bundles have secondary
growth, with many xylem vessels and few libriform fibers, sieve tubes, companion cells
and few cells of phloemic parenchyma. At the periphery of vascular bundles, is located a
thick strand of sclerenchymatic fibers, having walls extremely thickened (Fig. 5).
The leaf’ epidermis consists of isodiametric cells, having the external wall very
thick. The mesophyll is completely palisadic (6-7 layers of cells); the lamina has a bifacial
isofacial (isolateral) structure (Fig. 6)
Gypsophila struthium L. ssp. hispanica
The stem’ cortex is very thin, having only 2-3 layers of chlorenchymatic cells. The
stele is surrounding by a large belt consisting of 3-4 layers of sclerenchymatic fibers whose
walls are strongly thickened and lignified (Fig. 7). Underneath this sclerenchymatic
(mechanic) ring, it can be noticed a large area of cork, built up by 5-6 layers of suberized
(Fig. 7), with irregular contour, but slightly radially prolonged cells.
Conductive tissues are of cambial origin and have a ring disposition. The external
ring of secondary phloem is relatively thick, comprising sieve tubes, companion cells, and
parenchyma cells. The internal ring of secondary xylem is obviously thicker, having a huge
amount of libriform (Fig. 8), few vessels, and lignified parenchyma cells.
Medulla is relatively large, parenchymatic, with intercellular spaces and air-storing
lacunae between big cells; many of them contain crystals of calcium oxalate (Fig. 9).
The lamina of this species is cylindrical and succulent. The mesophyll is
homogeneous, almost entirely of palisadic type, with higher cells (Fig. 10). The conductive
tissues are arranged in 6-7 small vascular bundles, confined to an opened arch. In the all
mass of mesophyll and especially in the proximity of vascular bundles, it can be noticed
several huge cells containing a big crystal of calcium oxalate (Fig. 11). This foliar
architecture is more or less similar with that of Gypsophila muralis (Grigore and Toma,
unpublished data), a Romanian preferring halophyte [16] but is clearly similar with foliar
anatomy of Spergularia media [17], another species from Caryophyllaceae.
Of course, apart from basic anatomical features we are discussing in this paper, it
is of great interest to establish the ecological nature of gypsophily in plants. Moreover,
gypsophytes seems to have a special status in Spanish flora. This is because the Iberian
flora has about 30 endemic gypsophytes [28]. As far as gypsum outcrops are concerned, the
highest rates of endemicity are to be found in arid environments [21; 37; 38; 29; 30; 5; 32],
a fact that agrees the pattern of major singularity of the stressful environment observed in
the Mediterranean basin [14, 15; 27]. Most of gypsophytes are seriously threatened,
33
constituting a global biodiversity conservation priority [29]. Perhaps gypsum soils are
among the most threatened habitats in Europe and, especially, in the Mediterranean Basin
[15; 32], fact that would require further conservation strategies. In the case of gypsophytes,
two different models have been proposed to explain the occurrence of edaphic endemics
(for detailed comments, see Palacio et al. [36].
Since gypsum soils occur only in arid and semi-arid areas, where is a wateravailability limitation, perhaps this would imply that the ecological nature of gypsophytes’
adaptations is xerophytic. This suggests that soil could be physical or physiological drought
[43] and in this case, the place of gypsophytes would be among the xerophytes’ large
ecological communities.
Preliminary conclusions
The intense lignification in the central cylinder of stems, foliar succulence, and the
presence of protective hairs at the level of stems could suggest the xerophytic nature of
these adaptations in investigated gypsophytes. This would fit anyway with stressful
environmental conditions occurring in gypsum soils, especially with water scarcity and
nutrient imbalance. Further investigations will elucidate if gypsophytes should really be
included among xerophytes, as we propose in this preliminary work.
Acknowledgements
This paper was published with support provided by COST Action FA0901:
‘Putting Halophytes to work – From Genes to Ecosystems’ and by the
POSDRU/89/1.5/S/49944 project “Developing the innovation capacity and improving the
impact of research through post-doctoral programmes”.
REFERENCES
1. BOISSIER P. E., 1839-1845 – Voyage botanique dans le midi de l’Espagne pendant l’année 1837 (2 vol), Gide
et Cie, Paris.
2. BRIDGES E. M., BURNHAM C. P., 1980 – Soils of the state of Bahrain. J. Soil Sci., 31: 689 – 707.
3. CALVENTE MERLO MARIA ENCARNA, C. G. DE CARRASCO, ANA JOSE SOLA GÓMEZ, MARIA
LUISA JIMÉNEZ-SÁNCHEZ, MARIA LUISA RODRIGUEZ-TAMAYO, J. F. MOTA POVEDA,
2009 – Can gypsophytes distinguish different types of gypsum habitats? Acta Bot. Gallica, 156, 1: 63 –
78.
4. CAVANILLES A. J., 1795-1797 – Observaciones sobre la Historia Natural, Geografia, Agricultura, Población
y Frutos del Reyno de Valencia. Imprenta Real, Madrid.
5. CERRILLO M. I., DANA E. D., CASTRO H., RODRIGUEZ-TAMAYO M. L., MOTA J. F., 2002 – Selection
of priority areas for the conservation of gypsophilous flora in the southeast Iberian Peninsula. Revista
Chilena de Historia Natural, 75: 395 – 408.
6. CLEMENTS F. E., 1902a – A system of nomenclature for phytogeography. Bot. Jahrb., 31: 1 – 20.
7. CLEMENTS F. E., 1902b – Greek and Latin in biological nomenclature. University Studies, 3, University of
Nebraska, Lincoln, Nebraska.
8. CLEMENTS F. E., 1904 – The development and structure of vegetation. Botanical Seminar VII. Studies in the
vegetation of the State III. Botanical Survey of Nebraska, University of Nebraska.
9. COCKERELL T. D., GARCIA F., 1898 – Preliminary note on the growth of plants in gypsum. Science, 8
(187): 119 – 121.
10. CONTEJAN C., 1881 – Géographie botanique. Influence du terrain sur la végétation. Librairie J. B. Baillere
et fils, Paris.
11. DUVIGNEAUD P., 1968 – Essai de classification chimique (éléments minéraux) des plantes gypsicoles du
bassin de l’Ebre. Bull. Soc. Royale Bot. Belgique, 101: 279 – 291.
34
12. ESCUDERO A., SOMOLINOS R. C., OLANO J. M., RUBIO A., 1999 – Factors controlling the
establishment of Helianthemum squamatum, an endemic gypsophile of semi-arid Spain. J. Ecol., 87:
290 – 302.
13. ESCUDERO A., IRIONDO J. M., OLANO J. M., RUBIO A., SOMOLINOS R. C., 2000 – Factors affecting
establishment of a Gypsophyte: The case of Lepidium subulatum (Brassicaceae). Am. J. Bot., 87: 861 –
871.
14. GÓMEZ-CAMPO C. (Ed.), 1985 – Plant conservation in the Mediterranean area. Geobotany, 7. W. Junk,
Dordrecht, Boston, Lancaster.
15. GÓMEZ-CAMPO C. (Ed.), 1987 – Libro Rojo de las species vegetales amenazadas de España peninsular e
Islas Baleares, ICONA, Madrid.
16. GRIGORE M. – N., 2008 – Halofitotaxonomia. Lista plantelor de sărătură din România. Edit. Pim, Iaşi.
17. GRIGORE M. – N., TOMA C., 2010 – Halofitele. Aspecte de anatomie ecologică. Edit. Univ. „Al. I. Cuza”,
Iaşi.
18. GRIGORE M. – N., TOMA C., BOSCAIU M., 2011 – Ecological notes on halophytes species from
Mediterranean climate. Lucr. Şt. (Horticultură), USAMV „Ion Ionescu de la Brad”, Iaşi, 54, 1: 29 – 34.
19. GUERRERO CAMPO J., ALBERTO F., MAESTRO MARTINEZ M., HODGSON J., MONTSERRAT
MARTI G., 1999 – Plant community patterns in a gypsum area of NE Spain. II. Effects of ion washing
on topographic distribution of vegetation. J. Arid. Environ., 41: 411 – 419.
20. HENSLOW G., 1895 – The origin of Plant-Structures by Self-Adaptation to the environment. London, Kegan
Paul, Trench, Trübner, & Co, Ltd, Paternoster House, Charing Cross Road.
21. JOHNSTON I. M., 1941 – Gypsophily among Mexican desert plants. J. Arnold Arboretum, 22, 2: 145 – 170.
22. MACCHIATI L., 1888 – Contribuzione alla flora del gesso. Nuevo Giornale Botanico Italiano, 20: 418 – 422.
23. MACCHIATI L., 1891 – Seconda contribuzione alla flora del gesso. Nuevo Giornale Botanico Italiano, 23:
171 – 175.
24. MACCHIATI L., 1892 – Contribuzione alla flora del gesso. Nuevo Giornale Botanico Italiano, 24: 120 – 122.
25. MAHJOORY R. A., 2011 – The salt-land soil system placement (Taxonomy) in relation to global changes and
challenges. Proceedings of the Global Forum on Salinization and Climate Change (GFSCC2010),
Valencia, 25-29 October, Spain, World Soil Resources Reports No 105. FAO, Rome: 15.
26. MCDOUGALL W. B., 1941 – Plant Ecology (third ed.). Lea & Febiger, Philadelphia.
27. MÉDAIL F., VERLAQUE R., 1997 – Ecological characteristics and rarity of endemic plants from southeast
France and Corsica: implication for biodiversity conservation. Biol. Conserv., 80: 269 – 281.
28. MERLO M. E., MOTA J. F., CABELLO J., ALEMAN M. M., 1998 – La gipsofilia en plantas: un apasionante
edafismo. Investigación y Gestión, 3: 103 – 112.
29. MEYER S. E., 1986 – The ecology of gypsophile endemism in the Eastern Mojave desert. Ecology, 67: 1303 –
1313.
30. MEYER S. E., GARCIA-MOYA E., 1989 – Plant community patterns and soils moisture regime in gypsum
grassland of north central Mexico. J. Arid Environ., 16: 147 – 155.
31. MEYER S. E., GARCIA-MOYA E., LAGUNES-ESPINOZA L. C., 1992 – Topographic and soil surface
effects on gypsophile plant community patterns in central Mexico. J. Vegetation Sci., 3: 429-438
32. MOTA J. F., SOLA A. J., DANA E. D., 2003 – Plant succession in abandoned gypsum quarries in SE Spain.
Phytocoenologia, 33: 13-28
33. MOTA J. F., SOLA A. J., JIMÉNEZ-SÁNCHEZ M. L., PÉREZ-GARCIA F. J., MERLO M. E., 2004 –
Gypsicolous flora, conservation and restoration of quarries in the southeast of the Iberian Peninsula.
Biodiversity and Conservation, 13: 1797 – 1808.
34. MOTA J. F., et al., 2009 – Aproximación a la checklist de los gipsófitos ibéricos. Ann. Biol., 31: 71 – 80.
35. MOTA J. F., GARRIDO-BECERRA J. A., PÉREZ-GARCIA F. J., SOLA A. J., VALLE F., 2010 – Use of the
multi-response permutation procedure and indicator species value for the statistical classification of the
gypsicolous Iberian scrun communities. Candollea, 65, 1: 117 – 134.
36. PALACIO SARA, ESCUDERO A., MONTSERRAT-MARTI G., MAESTRO M., MILLA R., ALBERT
MARIA J., 2007 – Plants living on gypsum: Beyond the specialist model. Ann. Bot., 99: 333 – 343.
37. PARSONS R. F., 1976 – Gypsophily in plants – a review. Am. Midl. Nat., 96: 1 – 20.
38. POWELL A. M., TURNER B. L., 1977 – Aspects of the plant biology of gypsum putcrops of the Chihuahuan
desert. In: Transactions of a Symposium on Biological Resources of the Chihuahuan desert (ed. by
Riskinn D. H.), US Department of the Interior, National Park Service, Transactions Proceedings Series,
3: 315 – 325.
39. REYES PRÓSPER E., 1915 – Las estepas de España y su vegetación. Est. Tip. „Sucesores de Rivadeneyra”,
Madrid.
35
40. RUIZ J. M., LOPEZ-CANTARERO I., RIVERO R. M., ROMERO L., 2003 – Sulphur phytoaccumulation in
plant species characteristics of gypsipherous soils. Int. J. Phytoremediation, 5: 203 – 210.
41. SCHIMPER A. F. W., 1903 – Plant geography upon a physiological basis. Clarendon Press, Oxford.
42. WARMING E., 1895 – Plantesamfund. Grundträk af den okologiske Plantegeografi. Kjöbenhavn, Philipsens.
43. WARMING E., 1909 – Oecology of Plants. An introduction to the study of plant-communities.Clarendon
Press, Oxford.
44. WILLKOMM M., 1852 – Die strand-und steppengebeite der iberischen halbinsel und deren vegetation.
Leipzig.
45. * * *, United States Department of Agriculture, 2010 – Keys to Soil Taxonomy (eleventh ed.) Natural
Resources Conservation Service.
46. * * *, World reference base for soil resources. A framework for international classification, correlation and
communication, 2006 – FAO, Rome.
Explanation of plates
Plate I
Figure 1. Localization of gypsum areas from Tuéjar (Spain) (drawn from Google Maps)
Micrographs of cross section through:
Figures 2, 3 and 5. Stem of Ononis tridentata (X400)
Figure 4. Stem of Ononis tridentata (X200)
Figure 6. Lamina of Ononis tridentata (X200);
Plate II
Figures 7 and 8. Stem of Gypsophila struthium (X200)
Figure 9. Stem of Gypsophila struthium (X400)
Figures 10 and 11. Lamina of Gypsophila struthium (X400).
36
M. – N. Grigore, C. Toma, Maria-Magdalena Zamfirache, Monica Boşcaiu
Figure 1
PLATE I
Figure 2
Figure 3
Figure 4
Figure 5
Figure 6
37
M. – N. Grigore, C. Toma, Maria-Magdalena Zamfirache, Monica Boşcaiu
Figure 7
PLATE II
Figure 8
Figure 9
Figure 10
Figure 11
38