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Flora of Jammu and Kashmir State (Family Asteraceae- Tribe

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Flora of Jammu and Kashmir State (Family Asteraceae- Tribe Journal of Plant Biology Research 2016 5(1): 12-19 eISSN:2233-0275 pISSN:2233-1980 http://www.inast.org/jpbr.html REGULARARTICLE Is the red coloration in the carnivorous plant Pinguicula moranensis related with protection against photodamage or against herbivory? Luz María Ayestarán, Raúl E. Alcalá* Departamento de Ecología Evolutiva, Centro de Investigación en Biodiversidad y Conservación. Universidad Autónoma del Estado de Morelos. Av. Universidad 1001, Cuernavaca, Morelos, México. C. P. 62209. ABSTRACT Understanding the relationship between phenotypic variation and environmental pressures has been useful to identify the factors that currently maintain functional traits in populations. The red coloration of leaves derived from anthocyanins is frequently related with a protective role against biotic and abiotic factors. Using a carnivorous plant species as a model system, we evaluated two alternative hypotheses: 1) that red color confers protection against photodamage or 2) it confers protection against herbivory. In summer of 2015, 1153 individuals of Pinguicula moranensis were marked in 58 1-m2 plots within a population located in central Mexico in which patches of plants exhibit contrasting light environments (sunny and shaded habitats) due to different orientation (northeast vs. southwest, respectively). The association between color of plants (red and green) with the spatial variation in light environment was tested through a contingency table. Regarding herbivory, in the sunny habitat 35 pairs of individuals were photographed to quantify the percent of damage through image analysis. The mean values of herbivory were compared through a t-test with dependent groups using the arcsin transformation. The proportion of red plants was 2 one order of magnitude higher in the sunny site (1 = 89.53, P < 0.0001). The mean values for the percentage of herbivory show no differences between both groups (t = -1.688, p = 0.10, n = 35). Overall, our study suggests that there is no a dual role explaining the presence of red coloration in Pinguicula. The absence of effects of the red coloration on the percentage of damage suggests that the interaction with herbivores is not involved in the maintenance of red coloration. In contrast, the strong bias in the density of red plants toward the sunny habitat supports the hypothesis about the protective role against photodamage. Consequently, exposition to direct sunlight seems to be the most likely ecological factor explaining the color polymorphism in Pinguicula. Keywords: Anthocyanins, Color polymorphism, Light environment, Sunscreen, Phenotypic variation. INTRODUCTION or multiple roles is particularly interesting for the The study of phenotypic variation has been a central balance between fitness gains and the costs of theme in evolutionary ecology mainly because the synthesis and maintenance or phenotypic traits [10- inter-individual differences in phenotypic traits are 12]. Secondary metabolites are universally present related with the ability to cope with environmental in plants and the evidence about their role and its pressures [1-7]. Understanding the relationship evolutionary significance is increasing [13-17]. A between phenotypic variations and environmental scenario for multipurpose functions could be pressures has been useful to characterize for expected for secondary metabolites given that these example, the mode and magnitude of natural compounds can confer protection against several selection [8] and to identify the ecological factors biotic and abiotic factors [18,19]. Multi- those involved with their origin [9]. functionality would be advantageous as several The presence of specific functional traits with dual direct and indirect costs for the synthesis and storing * Corresponding author E-mail: [email protected] J. Plant Bio. Res. 2016, 5(1): 12-19 of secondary metabolites have been demonstrated they are involved with energy acquisition [43]. [20-22]. Therefore, it can be predicted that leaf area lost by Secondary metabolites such as anthocyanins and the attack of herbivores could generate stronger other pigments are widely present in plants. For costs due to their dual role. If the polymorphism in example, these pigments are the responsible for the color could be somewhat involved with variation in color of several fruits and flowers [23] and are also the level of defense, as has been demonstrated for frequent in vegetative organs including petioles, other plant species, the red coloration in Pinguicula veins, stipules [24] and leaves [25]. Anthocyanins could be doubly advantageous. could be costly as they absorb visible light. The In this study standing levels of leaf herbivory were competition with chlorophylls could consequently compared between green and red colored reduce the photosynthetic efficiency. Thus, several individuals of Pinguicula moranensis Kunth to test hypotheses have been advanced to account for their the hypothesis that anthocyanic plants exhibit less presence in leaves [19,26]. Some studies showed herbivory. In addition, we tested the hypothesis that that the red coloration produced by the if anthocyanins act as sunscreen a higher proportion concentration of anthocyanins can be induced by or red plants is expected in sites exposed to higher biotic and abiotic factors [27-29]. For example, direct sunlight. there is evidence indicating that in foliage, anthocyanins increase the protection against MATERIALS & METHODS photoinhibition and damage caused by UV- Study system radiation [25,30,31]. In addition, other studies This study was conducted in a region composed by suggest that anthocyanins tend to confer protection a series of hillsides primarily covered by oak-pine against the attack of herbivores and pathogens [29, forests in the northern portion of Cuernavaca City 32-35]. However, evidence about the simultaneous (Morelos, Mexico). Along a rocky wall of some 500 role of anthocyanins acting as a protection against m there were about 2000 individuals of Pinguicula herbivores and as a sunscreen in the same plant moranensis growing in three main patches ranging species is limited (but see, 18,36]. from 20 to 50 m2. Two patches were selected as they Members of Pinguicula L. are small-size, rosetted showed contrasting light conditions due to different and dimorphic perennial herbs that obtain mineral orientation of the wall in which plants were nutrients through the capture and assimilation of growing. In the northeast oriented patch (hereafter, prey [37]. In the field, the summer rosette of most sunny habitat) plants are exposed to higher plants is pale-green colored. However, some irradiance as they received direct sunlight from individuals show red coloration ranging from a light 0900 h to 1400 h. In contrast, in the southwest- pigmentation on the leaves surface to individuals oriented patch plants are not exposed to direct bearing entire red colored leaves. Experimental sunlight. As a consequence this site shows shadier evidence showed that red coloration in Pinguicula and more humid conditions and the wall was is derived from the increase in anthocyanins covered by ferns (hereafter, shaded habitat). providing protection against UV radiation and photoinhibition [38]. However plants of Pinguicula Pinguicula moranensis presents seasonally colonize sites that can vary in orientation and dimorphic leaves. The resistance rosette is present consequently could be exposed to contrasting light during the drier and cooler months from November regimes [30,40]. If anthocyanins are involved with to May and it is composed by tiny non-glandular protective roles functioning as a sunscreen it can be leaves. The summer rosette (i.e., capture rosette) is predicted that patches of populations naturally present from June to October, and it is composed of exposed to direct light should show a higher larger leaves (6-12 cm) covered by stalked secreting concentration of these pigments in plants [41]. glands and sessile digestive glands. Nearly 80% of Conversely, the effect of red coloration against the prey capture corresponds to small flying insects. damaged induced by herbivores has not been Flower production occurs mostly the during evaluated in Pinguicula. This information would be summer months. The zygomorphic and useful, as independently from the color, leaves of hermaphroditic, spurred flowers are individually the summer rosette are the organs involved in prey inserted in stalks of up to 25 cm [44]. capture and assimilation [42], and at the same time, 13 J. Plant Bio. Res. 2016, 5(1): 12-19 Spatial pattern of anthocyanic plants RESULTS In summer of 2014 (middle of the growing season) In the sunny site 778 plants were found in the 34 two quadrants (17×2 m and 12×2 m; long and plots, overall density corresponded to 25.9 plants height) were traced respectively in the sunny and per square meter. In this site 188 plants (~32%) shaded habitats. Each quadrant was divided in 1-m2 corresponded to the red morph and 590 had green plots to facilitate the identification of all plants in rosettes. In the shaded site only 375 plants were current demographic studies. In summer of 2015, marked in 24 plots resulting in a density of 15.62 we utilized these quadrants to evaluate the spatial plants per square meter. Only 7 individuals (~2%) pattern of red individuals. A red plant was defined were red colored and 368 were green plants. Red as a plant with at least 50% of the total area being plants were present only in 25% of the 1-m2 plots in red. The association between color of
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