Download the leaf structure of some nepenthes danser

Analele ştiinţifice ale Universităţii “Al. I. Cuza” Iaşi
Tomul LIV, fasc. 1, s. II a. Biologie vegetală, 2008
THE LEAF STRUCTURE OF SOME NEPENTHES DANSER SPECIES
IRINA STĂNESCU∗, C. TOMA∗∗
Abstract: The authors analyze a few aspects referring to the modified leaf of four Nepenthes species, at
different levels, stress being laid on the structure of the vascular bundles, digestive and nectariferous
glands.
Key words: Nepenthes, digestive glands, nectariferous glands, hydathodes.
Introduction
The Nepenthes genus consists of more than 80 tropical species [8], spread around SE Africa, Sri-Lanka and Madagascar. Etienne de Flancourt described it in 1658 for the first
time [3] and in 1753 Linné called it Nepenthes. The plant is a climbing, weakly
branched liana. It presents a basal rosette of leaves with short internodes when
young; on sexual maturity, the internodes become elongated and the plant starts
being climbing or prostrate, according to the species.
The plant creates a special impression by its bizarre leaves, consisting of a basal
assimilatory part, a tendril which rolls up around different supports and a trap [2]. This trap
is like a pitcher with a lid, which covers the trap, avoiding the dilution of the liquid from
inside the trap by the rainwater. Some authors believe that the assimilatory part, the tendril
and the pitcher belong to the petiole of an archaic leaf, while the lid represents the limb.
Others consider that the pitcher and the lid form the limb, and the assimilatory part and the
tendril form the petiole.
Darwin stated that a carnivorous plant attracts, captures and digests the prey; the
supplementary nutritive elements brought by the prey are necessary in developing and
blooming. The capturing system in Nepenthes is passive; the plant does not need to move to
capture the prey, unlike those which have active traps, such as Dionaea muscipula.
The plants bear flowers with shiny colours and abundant nectar to attract the
pollinating insects; on the other hand, the plants use different traps with different attraction
elements: shiny colours or the reflection of the UV radiation, attracting odours or nectar
secreted by the nectariferous extrafloral glands; all these characteristics belong to the leaf.
Some authors [5, 7] evidenced the structure of the digestive glands; others [1, 6] considered
that the digestive glands are closely associated with the vascular bundles. Some histoanatomical aspects were evidenced in a previous work [9] devoted to Nepenthes maxima.
∗
Botanical Gardens of Iasi, Dumbrava Roşie Street, no. 7-9, Romania
“Al. I. Cuza” University, Faculty of Biology, Carol I. Bd., no. 20A, 700506, Iaşi, Romania
∗∗
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Materials and methods
The material under study, coming from the collection of the “Alexandru Borza”
Botanical Gardens of Cluj-Napoca, belongs to four taxa: N. x coccinea Mast, N.
distillatoria L., N. maxima Reinw. ex Nees and N. northiana Hook f.
The material subjected to analysis (the modified leaves of the plants) has been fixed
and preserved in 70% ethylic alcohol. The sections (from the assimilatory part, tendril and
pitcher) were cut with a microtome, then coloured with iodine green and alaun-carmine,
mounted in gel and analyzed on a Novex (Holland) light microscope. The light micrographs
were performed by means of Novex (Holland) microscope, using a Canon A95 camera.
Results and discussions
As already mentioned, the leaf of Nepenthes consists of three parts: a basal,
assimilatory one, a tendril and a pitcher which represents the trap of the plant.
In front side view, the upper epidermis of the assimilatory part appears as formed of
polygonal cells (Fig. 1); here and there, a few hydathodes are present. The lower epidermis
consists of small cells, bearing weakly waved walls (Fig. 2). Here and there, stomata of the
anomocytic type and hydathodes are present. A hydathode bears a short pedicel formed of a
few cells and a stellate part, formed of 4-10 cells. Another author [4] suggests that the
hydathodes do not only secrete water, but even absorb it from time to time.
In cross section, the upper epidermis evidences small cells covered by a thick
cuticle. Just beneath the epidermis, a few isodiametric-celled layers are present, forming an
acviferous tissue (Fig. 3); some authors [5] call it an acviferous hypodermis. Then, a 2-3
layered palisade tissue, with short cells, in which chloroplasts can be observed, is present.
The lacunary tissue is multi-layered, with small aeriferous spaces between the component
cells. A lot of isolated mechanical cells (idioblasts) with spiral thickenings can be observed
in the mesophyll; these were evidenced by other authors [5], too.
The lower epidermis consists of small, isodiametric cells, covered by a cuticle
thinner than the one covering the upper epidermis. Numerous stomata are present, as well
as numerous calcium oxalate crystals in the mesophyll.
The midvein is very prominent at the lower side of the assimilatory part (Fig. 4). A
large number of vascular bundles is present (8 big bundles, one of its being situated in the
centre or 6 bundles and a central one at N. northiana); most of them are implanted in a
thick sclerenchyma ring, formed of sclerenchymatic fibres with thickened and lignified
walls (or unlignified at N. coccinea). The vascular bundles have different orientation in the
sclerenchymatic ring. A vascular bundle (Fig. 5) consists of a phloem (sieved tubes and
companion cells) and a xylem (xylem vessels separated by celulosic parenchyma).
Sometimes, the sclerenchyma sheath bears very small vascular bundles, consisting of a few
phloem elements or of phloem and 1-2 xylem vessels.
In the fundamental, external parenchyma, idioblasts and small, isolated vascular
bundles are present, often consisting of a few phloem elements, surrounded by a thin
sclerenchymatic sheath.
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The tendril
In cross section, the tendril shows a circular shape, with 7-8 ribs at N. maxima (Fig.
6). Small cells, covered by a thick cuticle, form the epidermis. Here an there, hydathodes,
short, sometimes branched tector hairs and stomata prominig above the epidermis are
present. The cortical parenchyma is formed of 5-6 layers of large cells. Most of the vascular
bundles are implanted in a strong sclerenchyma ring. There is a high variability regarding
the number of bundles and on their position (N. coccinea and N. maxima present a lot of
vascular bundles of different size in the sclerenchyma ring and a central one in the
fundamental parenchyma; N. distillatoria presents 2 big vascular bundles in the center of
the parenchyma and a smaller one, close to them, while N. northiana shows the largest
number of vascular bundles, implanted in the sclerenchyma ring, and also two smaller ones
in the fundamental parenchyma, but close to the sclerenchyma. The tendril has an
homogenous parenchyma, formed of big, turgescent cells and a few idioblasts.
Near the pitcher, the cross section of the tendril is quite circular. The vascular
bundles form 2-3 rings (the internal bundles are bigger than the external ones, in the
fundamental parenchyma). A sclerenchymatic sheath surrounds each vascular bundle.
Numerous calcium oxalates are present in the fundamental parenchyma.
At the inferior level of the pitcher, a typical limb structure is present.
In front side view, the internal epidermis presents polygonal elongated cells, with
thick walls. Here and there, a lot of multicellular digestive glands are present (Fig. 7); a
small epidermal prolongation can be observed near each gland, yet without touching it. The
external epidermis (Fig. 8) consists of small polygonal cells with thin walls, anomocytic
stomata, hydathodes and nectariferous glands, which appear like multicellular, massive
structures, communicating with the exterior through a short channel.
In cross section, the wall of the pitcher is quite thick. The internal epidermis shows
elongated cells, covered by a thick cuticle. Numerous big digestive glands are present in
small epidermal cavities (Fig. 9); the epidermal cells form a small fold, without touching
the gland. A digestive gland shows 2-3 layers of oblate cells, 1-2 layers of isodiametrical
cells and an external layer of columnar-shaped cells. Each digestive gland is associated
with small vascular bundles (tracheids with ringed and spiral thickenings). In longitudinal
section, the small fold can be better observed (Fig. 10).
The external epidermis consists of small cells, covered by a thin cuticle. The
nectariferous glands are formed of three layers of cells delimiting a cavity which opens
towards the exterior through a short channel (Fig. 11). The nectariferous glands attract the
insects (the prey) to the trap and make them climb the wall of the pitcher to reach the
slippery peristome. The assimilatory parenchyma is thick, homogenous, formed of small
cells outside and bigger inside. A lot of calcium oxalates are present all over the
parenchyma.
The vascular bundles have different sizes, the biggest ones occupying the external
part of the parenchyma, while the smallest ones occupy the centre of it. Each vascular
bundle consists in phloem facing the exterior part of the pitcher and a xylem facing the
internal one, so that the internal epidermis represents the old upper epidermis of an archaic
leaf and the external epidermis represents the old lower epidermis. All the studied species
show mechanical sheaths surrounding the vascular bundles, consisting of fibres with
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moderately thickened and lignified walls. The assimilatory parenchyma also presents a few
idioblasts.
The middle level of the pitcher presents a quite similar structure to that of the
anterior level.
In front side view, the internal epidermis consists of polygonal cells with thick walls
and secretory glands, smaller than those occurring at the inferior level; the integumentary
fold do not touch the gland (Fig. 12). The external epidermis is formed of polygonal cells,
anomocytic stomata, multicellular tector hairs, nectariferous glands and hydathodes (Fig.
13).
In cross section, the pitcher shows a thinner wall. The internal epidermis presents
digestive glands which communicate with the tracheids (Fig. 14). In longitudinal section,
the fold can be better observed (Fig. 15). The external epidermis consists of small cells
covered by a thin cuticle. Anomocytic stomata, hydathodes, nectariferous glands (Fig. 16)
and multicellular tector hairs, often branched, are present. In the assimilatory parenchyma,
numerous calcium oxalates can be observed. Each vascular is bounded by a
sclerenchymatic sheath (Fig. 17). There are vascular bundles consisting only of a few
phloem elements. The assimilatory parenchyma presents idioblasts, too.
The superior level of the pitcher shows the same structure as the other levels. In
front side view, the internal epidermis presents large polygonal cells and digestive glands
(Fig. 18) smaller than those occurring at the other levels. The epidermal fold covers more
than half of the digestive glands. The external epidermis (Fig. 19) consists of small
polygonal cells, with waved lateral walls, tector hairs, hydathodes, nectariferous glands and
anomocytic stomata.
Cross section through the superior level of the pitcher shows the digestive glands in
their incipient stage of development (Fig. 20), consisting of a small number of cells. Almost
half of the gland is covered by the integumentary fold (Fig. 21); the developing stages of
the glands during ontogenesis were previously presented [9]. The external epidermis shows
similar structures to those of the anterior levels (Figs. 22 and 23). The assimilatory
parenchyma is thinner; the vascular bundles are bounded by a very thin mechanical sheath,
consisting of fibres with thickened walls, but weakly lignified; some of the bundles present
only a few phloem elements; calcium oxalates are not present.
The lid
In front side view, both the upper and the lower epidermis present polygonal cells,
with waved lateral walls, anomocytic stomata, secretory glands surrounded by an
integumentary fold (Fig. 24) and hydathodes (Fig. 25); tector hairs, sometimes branched,
are present only in the lower epidermis. The cross section of the lid is similar to that
occurring in the pitcher’s wall. Numerous digestive glands (Fig. 26) are present in both
epidermis. The fundamental parenchyma presents vascular bundles of different sizes (Fig.
27), the largest occupying the centre of the parenchyma. All vascular bundles are
surrounded by a thin sclerenchyma sheath formed of thin-walled and weakly lignified
fibres.
The peristome (Fig. 28) is a common characteristic of the pitcher plants. All four
investigated Nepenthes species have a ridged peristome. The epidermal cells are small,
covered by a very thick cuticle. Stomata and hydathodes are present in the lower epidermis.
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The peristome has an homogenous parenchyma, with large cells, a few idioblasts and small
vascular bundles, most of them consisting of phloem elements surrounded by sclerenchyma
fibres, with cellulosed unthickened walls.
Conclusions
In spite of the high variability of the pitcher size recorded from one species to
another, their histo-anatomy is quite similar.
There have been observed mostly quantitative differences (number of the vascular
bundles, size of the digestive glands at different levels, thickness of the sclerenchymatic
sheath, length of the integumentary fold which covers each digestive gland) and not
qualitative differences.
REFERENCES
1.
2.
3.
4.
5.
6.
7.
8.
9.
ANDERSON A. N., 1994 - Secretion and absorbtion in glands of the carnivorous plant Nepenthes alata. B.
A. honors thesis, Connecticut College, New London, C. T.
DALTON M. JOS., 1859 - Note sur l’ origin et le développement des urnes dans les plantes du genre
Nepenthes. Ann. des Sci. Nat.; sér.Bot., 12: 125-129
LLOYD F. E., 1942 - The Carnivorous Plants. Chronica Botanica, 9. Ronald Press, New York
MACFARLANE J. M., 1889 - Observations on pitchered insectivorous plants. Part I. Ann. of Bot., 3: 253265
METCALFE C. R., CHALK L., 1972 - Nepenthaceae in Anatomy of the Dicotyledons. 1: 1105-1111,
Clarendon Press, Oxford
STERN K., 1917 - Contribution to the knowledge of Nepenthes. Flora, 109: 213 – 283
PARKES D. M., 1980 - Adaptive mechanisms of surfaces and glands in some carnivorous plants. MSc
Thesis, Monash University, Clayton, Victoria, Australia
STAROSTA P., LABAT J.-J., 1993. - L’univers des plantes carnivores. Éd. Du May, Paris
TOMA I., TOMA C., STĂNESCU I., 2002 - Histo-anatomical aspects of the Nepenthes maxima Reinw. ex
Nees metamorphosed leaf. Rev. Roum. Biol., sér. Biol. végét., 47, 1-2: 3-7
Acknowledgments
The authors gratefully thank to Felician Micle PhD, Ex-Director of the Botanical
Garden of Cluj-Napoca and to Elena Rânba for supplying the material for the present
investigation.
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Explanation of plates:
Plate I
1. The upper epidermis of the assimilatory part of N. maxima, in front side view
2. The lower epidermis of the assimilatory part of N. distillatoria, in front side view
3. The mesophyll of the assimilatory part of N. distillatoria
4. Cross section through the midvein of the assimilatory part of N. maxima
5. The biggest vascular bundle of the midvein belonging to the assimilatory part of
N. maxima
6. Cross section through the tendril of N. maxima
Plate II
7. The internal epidermis of the inferior level of N. distillatoria pitcher, in front side view
8. The external epidermis of the inferior level of N. distillatoria pitcher, in front side view
9. Cross section through the inferior level of N. distillatoria pitcher
10. Longitudinal section of the inferior level of N. maxima pitcher
11. Cross section through the inferior level of N. distillatoria pitcher
12. The internal epidermis of the middle level of N. northiana pitcher, in front side view
Plate III
13. The internal epidermis of the middle level of N. maxima pitcher, in front side view
14. Cross section through the middle level of N. northiana pitcher
15. Longitudinal section through the middle level of N. maxima pitcher
16. Cross section through the middle level of N. distillatoria pitcher
17. Cross section through the middle level of N. maxima pitcher
18. The internal epidermis of the superior level of N. coccinea pitcher, in front side view
Plate IV
19. The internal epidermis of the superior level of N. distillatoria pitcher, in front side
view
20. Cross section through the superior level of N. distillatoria pitcher
21. Longitudinal section through the superior level of N. maxima pitcher
22. Cross section through the superior level of N. distillatoria pitcher
23. Cross section through the superior level of N. northiana pitcher
24. The upper epidermis of the lid belonging to N. northiana pitcher, in front side view
Plate V
25. The lower epidermis of the lid belonging to N. northiana pitcher, in front side view
26. Cross section through the lid of N. coccinea pitcher
27. Cross section through the lid of N. northiana pitcher
28. Cross section through the peristome of N. northiana pitcher
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IRINA STĂNESCU, C.TOMA
PLATE I
1
2
3
4
5
6
11
IRINA STĂNESCU, C.TOMA
PLATE II
7
8
9
10
11
12
12
IRINA STĂNESCU, C.TOMA
PLATE III
13
14
15
16
17
18
13
IRINA STĂNESCU, C.TOMA
PLATE IV
19
20
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IRINA STĂNESCU, C.TOMA
PLATE V
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28
15