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Leaf Photosynthetic Characteristics in Eight Shaded Malaysian Filmy

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Leaf Photosynthetic Characteristics in Eight Shaded Malaysian Filmy Leaf photosynthetic characteristics in eight shaded Malaysian filmy ferns Características fotosintéticas foliares en ocho himenofiláceas de ambientes sombreados en Malasia Nurul Hafiza MR, KT Yong, N Osman, A Nasrulhaq-Boyce Abstract. The photosynthetic characteristics of eight Malaysian Resumen. Las características fotosintéticas de ocho Malasia Hy- Hymenophyllaceae filmy ferns from shady habitats were investigated menophyllaceae helechos membranosos de hábitats sombreados fue- in this study. Chlorophyll content was highest in Trichomanes me- ron investigados en este estudio. El contenido de clorofila fue mayor ifolium, followed by Cephalomanes obscurum, Hymenophyllum serrula- en Trichomanes meifolium, seguido por Cephalomanes obscurum, Hy- tum, H. denticulatum, H. javanicum, H. acanthoides, H. exsertum and menophyllum serrulatum, H. denticulatum, H. javanicum, H. acanthoi- H. blandum, with values ranging from 3.3 to 8.6 mg/g fresh weight. des, H. y H. exsertum blandum con valores que van desde 3,3 hasta 8,6 Soluble protein content was remarkably high in H. serrulatum, with mg/g peso fresco. El contenido de proteína soluble fue notablemente values of 53 ± 3.50 mg/g, followed by H. denticulatum, H. acanthoi- alta en H. serrulatum, con valores de 53 ± 3,50 mg/g, seguido por des, T. meifolium and the other species. Protein to chlorophyll ratios H. denticulatum, H. acanthoides, T. meifolium y las otras especies. La in the filmy ferns were low as expected, except for in H. serrulatum, relación proteína:clorofila en los helechos fue baja como se esperaba, H. acanthoides and H. denticulatum. Chloroplast number and size excepto en H. serrulatum, H. acanthoides y H. denticulatum. Número y ranged between 34 to 138 per cell profile, and between 4.8 to 6.5 μm tamaño de cloroplasto oscilaron entre las 34 y 138 por perfil de célula in diameter, in the Hymenophyllaceae. Quantum efficiency measure- y entre 4,8 a 6,5 μm de diámetro, en el Hymenophyllaceae. Mediciones ments in four Hymenophyllaceae spp. exhibited Fv/Fm values ranging de la eficiencia cuántica de cuatro Hymenophyllaceae spp. mostraron between 0.73 to 0.81. The Hymenophyllaceae spp. also showed low valores de Fv / Fm que oscilan entre 0,73 a 0,81. El Hymenophyllaceae in vivo CO2 assimilatory rates and light saturation points, ranging spp. también mostró baja en las tasas de asimilación de CO2 in vivo y 2 2 2 between 5 to 15 μmol CO2/m /s and below 150 μmol/m /s, respec- los puntos de saturación, que oscila entre 5 a 15 μmol CO2/m /s y por tively. The findings add further to our understanding on how the debajo de 150 μmol/m2/s, respectivamente. Los hallazgos se añaden a filmy ferns adapt and thrive in their humid and shady habitats. nuestra comprensión de cómo los helechos membranosos se adaptan y prosperan en sus hábitats húmedos y sombríos. Keywords: Plant science; Photosynthesis; Filmy ferns; Hymeno- phyllaceae; Shaded habitats. Palabras clave: Ciencia de las plantas; Fotosíntesis; Helechos va- porosos; Hymenophyllaceae; Hábitats sombreados. Institute of Biological Sciences, Faculty of Science, University of Malaya, 50603 Kuala Lumpur, Malaysia. Address Correspondence to: Prof. Amru Nasrulhaq Boyce, e-mail: [email protected] Recibido / Received 22.VIII.2013. Aceptado / Accepted 10.XII.2013. FYTON ISSN 0031 9457 (2014) 83: 353-361 354 Nurul Hafiza MR et al., FYTON 83 (2014) INTRODUCTION MATERIALS AND METHODS Filmy ferns from the Hymenophyllaceae family are aes- Plant material. The filmy ferns were collected from Gu- thetically attractive ferns that live abundantly in the hu- nung (Mount) Ulu Kali, Pahang which is 34 miles north- mid tropical rainforest. They show an amazing diversity in east of Kuala Lumpur. Gunung Ulu Kali (1772 m.a.s.l.) is terms of morphology and the habitats they occupy, making the southernmost tallest mountain in the Titiwangsa Range Hymenophyllaceae a great model for studying evolutionary in Peninsular Malaysia, not far from the summit area where ecology and related adaptive survival strategies in pteri- the renown hill resort, Genting Highlands is situated (Fig. dophytes (Dubuisson et al., 2003). They are small in size 1). Although there are heavy anthropogenic activities in the and some of them appear as very dark green or even black resort area, the surrounding region is made up of large tracts clumps and can be characterized by a single-cell thick lam- of montane forests that remain untouched and house rich bio- ina with lack of cuticle, giving them direct contact with logical diversity. The plants investigated in the present study air in their surroundings and are able to carry out rapid were obtained from these forests, with an elevation ranging gas exchange. Their physiology, however, has received little between 1300 - 1700 m.a.s.l. and annual rainfall ranging be- attention despite the large amount of literature on their morphology and taxonomy. Studies on sun and shade plants, particularly ferns, have been carried out for many years, since the early 1980s al- beit infrequently. It has been well documented that shaded plants are incapable of achieving high photosynthetic rates although they perform more efficiently at low light irradi- ances (Boardman, 1977; Givnish, 1988). Sun and shade plants have been shown to exhibit obvious differences in their morphology, ultrastructure, physiology and biochemis- try. Shade plants generally possess fewer, larger chloroplasts with larger grana, higher pigment content and lower pho- tosynthetic rates. On the other hand, most plants that grow in high light intensities in their natural habitats show the opposite characteristics of shaded plants, with higher rates of photosynthesis at saturating light intensity. Similar studies have been reported, particularly on ferns and bryophytes (Nasrulhaq-Boyce & Mohamed, 1987; Nasrulhaq-Boyce & Duckett, 1991; Proctor, 2003; Marschall & Proctor, 2004). More recently, Wong et al. (2012) studied the photosynthet- ic rates of woody and fern species from different light re- gimes. They reported that the shade adapted plants showed low gross photosynthetic rate when the dark-adapted leaves were exposed to 500 or 2000 μmol/m2/s photosynthetic photon flux (PPF). Proctor (2003) studied and compared the ecophysiological characteristics, such as light response, water relations and dessication tolerance between the filmy ferns, Hymenophyllum peltatum (Poir.) Desv. [syn. H. wilsonii] and H. tunbrigense (L.) Sm. They reported that the CO2 uptake in the filmy ferns studied were low at low light irradiances. Several authors have reported similar findings with other ferns species in terms of their structure and ecological adap- tation (Hebant & Lee, 1984; Nasrulhaq-Boyce & Duckett, 1991; Johnson et al., 2000; Proctor, 2005; Proctor, 2012). The aim of the present study was to investigate the chloro- phyll and protein content, and chloroplast anatomy in selected Fig. 1. Map of Gunung Ulu Kali, Genting Highlands, Pahang, Ma- Hymenophyllaceae species as well as their chlorophyll fluores- laysia, where the ferns were collected from. cence and photosynthetic activity in an attempt to understand Fig. 1. Mapa de Gunung Ulu Kali, Genting Highlands, Pahang, Mala- sia, donde se recogieron los helechos. further photosynthesis in the shaded filmy ferns. FYTON ISSN 0031 9457 (2014) 83: 353-361 Leaf photosynthetic characteristics in eight shaded Malaysian filmy ferns 355 tween 2480-3780 mm. Irradiance, surrounding temperature Microscopy. Fresh leaves were cut into small pieces and and relative humidity measured ranged between 33 - 93 μmol/ then mounted on a slide using distilled water as medium. m2/s, 14-25.3 °C and 51% - 100%, respectively. The mean The slides were examined and photographed using a Leica temperature was 17.9 °C, while the mean RH was 95.4%. DFC290 digital camera that attached to a compound micro- The plants were collected from the ground and tree trunks scope. Chloroplast size and number per cell were calculated in moist and shady areas, together with their underlying soil, from 20 different cells, with four cells each of five different placed in plastic bags, and brought back to the laboratory for leaves. work on the same day. Statistical analysis. The data obtained were pooled and Chlorophyll and protein analysis. Chlorophyll was ex- analysed using Minitab Pro v16.1.0.0 and SPSS statistical tracted in 80% acetone from freshly collected leaves and its software. A one-way ANOVA was applied to evaluate signifi- content was determined using the method of Arnon (1949) cant differences in the studied parameters. Least significant as outlined in Nasrulhaq-Boyce et al. (2011). Total protein difference was calculated following a significance at p=0.05. content was estimated using the Lowry et al. (1951) method. Measurement of light intensity, relative humidity and RESULTS temperature. Light intensity was taken using a Lux-meter The Hymenophyllaceae species collected in the present study (Field scout quantum meter, USA) at each site where the fern were generally from constantly moist, shaded highland habitats. species under study occur naturally. Readings were taken be- Table 1 shows that the irradiances of their habitats were consid- tween 11.00 am to 2.00 pm in the early afternoon when it was erably low for all the eight species of Hymenophyllaceae, where certain that no dark clouds were present in the sky. Readings the light intensities received by the plants were below 100 μmol/ were taken between ten to fifteen times. The same procedure m2/s. Light intensity increased in the morning as
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