Aquatic Botany 66 (2000) 273–280 Density-dependent morphological plasticity in Salvinia auriculata aublet Flávia F. Coelho a,∗ , Frederico S. Lopes a , Carlos F. Sperber b a Departamento de Biologia, Universidade Federal de Mato Grosso do Sul, C.P. 549, Campo Grande, MS 79070-900, Brazil b Setor de Ecologia, Departamento de Biologia Geral, Universidade Federal de Viçosa, Viçosa, MG 36570-000, Brazil Received 12 August 1998; received in revised form 9 March 1999; accepted 20 August 1999 Abstract This study examined the effect of crowding on the size of the floating and submerged leaves of Salvinia auriculata. In addition, we examined investment in reproductive structures (sporocarps) in response to the size of ramets. Ramets of S. auriculata growing on the surface of lagoons in the Southern Pantanal were sampled from populations of different densities. Ramets under densely crowded conditions were significantly larger than ramets under uncrowded conditions. There was a tendency for the number of sporocarps to increase with the size of submerged leaves, but not with length or specific area of floating leaves. These results indicate that S. auriculata exhibit density-dependent morphological plasticity, and may be a reflection of an evolved strategy that increases competitive ability of the ramets. It further suggests that the increase in production of sporocarps may not be a simple response to the size of ramets. ©2000 Elsevier Science B.V. All rights reserved. Keywords: Density-dependence; Morphological plasticity; Salvinia auriculata; Sporocarps 1. Introduction The response of individuals within a taxon to environmental variation (i.e., phenotypic plasticity) represents a central feature of evolutionary biology because of the potential adaptive nature of such variation (Petit et al., 1996). Phenotypic plasticity is the ability of an individual organism to alter its physiology or morphology in response to variation in environmental conditions (Schlichting, 1986). In ∗ Corresponding author. E-mail address: flaviafc@nin.ufms.br (F.F. Coelho) 0304-3770/00/$ – see front matter ©2000 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 9 9 ) 0 0 0 8 4 - 4 274 F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 conditions of low resource availability, physiological plasticity has been viewed as a profitable adjunct to morphological plasticity for the acquisition of resources. Hutchings and de Kroon (1994) proposed that morphological plasticity will be more restricted in plants which are characteristic of such conditions. The capacity of an individual to survive and reproduce in different environments may be enhanced if the phenotype can be changed or maintained as needed (Levin, 1988). However, the definition of phenotypic plasticity does not necessarily imply that such responses are adaptive; the plant fitness may not to be enhanced due to the physiological or morphological response (Schlichting, 1986). Spencer et al. (1973) and Duarte and Kalff (1987), showed the influence of environmental factors on the leaf shape, size and specific leaf area in submerged macrophytes. Factors such as density, incident light and self-shading may induce morphological response in such leaves. In many cases, changes in the production of reproductive structures in plants grown at different densities can be explained in terms of size-dependent reproduction of individuals (Thompson and Beattie, 1981; Weiner, 1988). Individual plants growing at a range of densities can alter the production of reproductive structures in response to their own size (Weiner, 1988). According to the model of Samson and Werk (1986), reproductive allocation is expected to increase with increasing plant size. Nevertheless, within-species reproductive allocation can either increase or decrease with size, presumably depending on morphological characteristics (Bazzaz et al., 1987). In this study, we examine the influence of densely crowded conditions on the size of the floating and submerged leaves in S. auriculata. In addition, we test whether the investment in sporocarps increases with the ramet size. 2. Materials and methods 2.1. Morphology of ramets S. auriculata (Salviniaceae) is a free-floating fern, which consists entirely of a plagiotropic shoot system. The basic morphological module is a ramet. Each ramet consists of a stem segment bearing three leaves, an apical bud and laterals bud which have the potential to grow into new ramets. Two of the leaves are green and float, their upper surfaces having special water-repellent hairs. True roots are absent; the third leaf is finely dissected and submerged, absorbing water and ions and functioning as a root (De la Sota, 1962; Sculthorpe, 1967). Spore-producing organs are borne on the submerged leaves and consist of sori surrounded by a globose indusium (‘sporocarp’) (De la Sota, 1962). 2.2. Study area The Pantanal of Mato Grosso is an area with temporary aquatic habitats such as lagoons and abandoned meanders of old rivers. These lagoons are regionally called ‘baı́as’, and can be thickly covered by vegetation. They are generally shallow and can completely dry up in F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 275 a few months by a decrease in water level (Carvalho, 1986). The fluctuation in the water level with an unpredictable magnitude makes these ‘baı́as’ in the Pantanal, a temporary environment for many plants. The climate of the Pantanal is tropical with a marked wet season (Brazil, 1979). Local precipitation is relatively low (a yearly average of about 972 mm). The overflowing of ‘baı́as’ which is common in the region is, however, not related to rainfall, but to the poor drainage of the soil (Amaral Filho, 1986). The study was conducted in the Miranda-Abobral sub-regions (sensu Adámoli, 1982) of the Pantanal of Corumbá municipal district, where the Universidade de Mato Grosso do Sul maintains a base for studies (19◦ 34′ 37′′ S; 57◦ 00′ 42′′ W). Plant material was collected in lagoons near this base, and in lagoons located along the road MS-184. 2.3. Study site Colonies of S. auriculata ramets were collected during the period from January to September 1997. Colonies were sampled in ‘baı́as’ with different densities of ramets (low densities: less than 50% of water surface covered by plants; high densities: more than 50% of water surface covered by plants). From each lagoon 50 ramets were randomly sampled. We measured the length and surface area of floating leaves, the length of submerged leaves and counted the number of sporocarps per ramet. 2.4. Data analyses To test the effect of the densely crowded conditions, we compared the size of the floating leaves, length of the floating leaves, and length of submerged leaves at high and low densities using a t-test. To test the effect of the size of ramets on the sporocarp production, we performed a simple linear regression of sporocarp number as a function of the length of submerged, and length and area of floating leaves. 3. Results The densely crowded conditions affected the length (Fig. 1) and size (Fig. 2) of the floating leaves as well as the length of the submerged leaves (Fig. 3). The ramets were significantly larger with vertically oriented, folded floating leaves in densely crowded mats. There was a significant difference in mean length of floating leaves between high density (4.41 cm ± 1.07 cm) and low density (3.92 cm ± 0.91 cm) (t = 5.90; p < 0.001). The mean size of floating leaves was also larger of high density (8.93 cm ± 3.81 cm) than of low density (7.26 cm ± 2.54 cm) (t = 6.66; p < 0.001). Mean length of submerged leaves followed the same pattern as floating leaves, being larger of high density (4.82 cm ± 2.57 cm) than of low density (2.41 cm ± 1.45 cm) (t = 15.95; p < 0.001). 276 F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 Fig. 1. Length of floating leaves under crowded conditions (maximum = 7.35; minimum = 1.14; mean = 4.41; median = 4.41) vs. uncrowded conditions (maximum = 5.66; minimum = 1.25; mean = 3.92; median = 4.06). There was a tendency for an increase in the number of sporocarps on the larger submerged leaves (F = 23.149; r2 = 0.030; p < 0.001) (Fig. 4), but sporocarp number did not increase with length of floating leaves (F = 3.646; r2 = 0.035; p = 0.057) (Fig. 5), nor the size of floating leaves (F = 0.810; r2 = 0.030; p = 0.368) (Fig. 6). Fig. 2. Size of floating leaves under crowded conditions (maximum = 22.66; minimum = 1.38; mean = 8.93; median = 8.42) vs. uncrowded conditions (maximum = 13.92; minimum = 0; mean = 7.26; median = 7.39). F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 277 Fig. 3. Size of submerged leaves under crowded conditions (maximum = 18.46; minimum = 0.62; mean = 4.82; median = 4.40) vs. uncrowded conditions (maximum = 7.51; minimum = 0.10; mean = 2.41; median = 1.96). 4. Discussion 4.1. Plasticity of floating leaves S. auriculata under uncrowded conditions exhibits smaller ramets with flat, circular leaves. Larger ramets with folded leaves are typical of densely crowded mats (Room, 1990; Fig. 4. Relationship between sporocarp number per ramet and submerged leaf length (Y = 0.364X + 2.04). 278 F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 Fig. 5. Relationship between sporocarp number per ramet and floating leaf length (Y = −0.394X + 3.30). Fig. 6. Relationship between sporocarp number per ramet and floating leaf area (Y = 0.047X + 3.81). F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 279 Gopal and Goel, 1993). According to Sculthorpe (1967), only in crowded conditions where competition is acute, will Salvinia species exhibit such a growth form. This plastic response allows to the plant maximize leaf the photosynthetic area, important at sites with high density of plants, where competition for light is intense and space is restricted for horizontal growth. Eichhornia crassipes Solms (Pontederiaceae), presents similar pattern. As plant density increases, the plants start vertical growth (elongation of petioles) together with an increase in leaf surface area (Center and Spencer, 1981). The aquatic macrophytes are particularly well known for their great phenotypic plasticity and, in these plants, the shape of leaves is a significant adaptive feature (Madsen, 1991; Gopal and Goel, 1993). Leaf construction is a trade-off between maximizing photosynthetic area and avoiding stress (light or nutrient limitation, due to increase in density) (Madsen, 1991). 4.2. Plasticity of submerged leaves We found submerged leaves larger under densely crowded mats. Room (1988) showed that in the absence of nitrogen in the water, an increase occurs in the size of the ‘roots’ (a process common at densely crowded sites). The relationship that we found between density and size of submerged leaves in S. auriculata, accords with results found in Salvinia molesta, and can be interpreted as a strategy that confers competitive advantage to ramets. Larger ‘roots’ can be better competitors and more efficient at the uptake of nutrients than smaller ‘roots’. 4.3. Plasticity in the production of sporocarps Our data showed that there was no relationship between floating leaf length and number of sporocarps. S. auriculata did not alter the production of sporocarps in response to floating leaf length. De la Sota (1962) related the presence of sporocarps in S. auriculata to variability in the leaf shape, and not only to the size. Fertile ramets, generally, have folded floating leaves, typical of densely crowded mats. Sterile ramets would have flat and circular floating leaves, typical of uncrowded conditions. Nevertheless, the presence of sporocarps is not always correlated with the morphology of floating leaves (De la Sota, 1962). The reproductive allocation within species can either increase or decrease with size, depending on morphological characteristics (Bazzaz et al., 1987). We found sporocarps in submerged leaves of all sizes, even on the smallest leaves. However, there was a tendency for an increase in the number of sporocarps on the larger submerged leaves. It is probable that the increase in the production of sporocarps is not a response to submerged leaf size. Rather, sporocarp production is probably affected indirectly by morphological variation of leaves and directly by environmental variation inducing morphological response in such leaves. Plant size may be the mechanism through which variation in environmental conditions (such increase in density) is detected and translated into variation in reproductive behavior (Weiner, 1988). 280 F.F. Coelho et al. / Aquatic Botany 66 (2000) 273–280 Acknowledgements This study was developed during the M.Sc. program of the first author, and was supported by CAPES. We would like to thank the Universidade Federal de Mato Grosso do Sul, for providing facilities for this study. Our special thanks to Kirt Wackford, Erich A. Fischer, Otávio Froehlich and to Drs. Flávio A.M. dos Santos and Rogério Parentoni Martins for helpful suggestions which improved the manuscript and Alexandre Salino for plant identification. References Adámoli, J., 1982. O Pantanal e suas relações fitogeográficas com os cerrados Congresso Nacional de Botânica, Anais, pp. 109–119. Amaral Filho, Z.P., 1986. Solos do pantanal matogrossense. I. Simpósio sobre recursos naturais e sócio-econômicos do pantanal, Corumbá, Anais, pp. 91–103. Bazzaz, F.A., Chiariello, N.R., Coley, P.D., Pitelka, L.F., 1987. Allocating resources to reproduction and defense BioScience 37, 58–67. Brazil, 1979. Relatório da primeira fase, descrição fı́sica e recursos naturais. Estudo de desenvolvimento integrado da bacia do alto Paraguai-Superintendência do desenvolvimento da região centro-oeste, Brası́lia. Carvalho, N.O., 1986. Hidrobiologia da bacia do alto Paraguai. I. Simpósio sobre recursos naturais e sócio-econômicos do pantanal, Corumbá, Anais, pp. 43–49. Center, T.D., Spencer, N.R., 1981. The phenology and growth of water hyacinth (Eichhornia crassipes [Mart.] Solms) in a eutrophic north-central Florida lake Aquat. Bot. 10, 1–32. De la Sota, E.R., 1962. Contributio al conocimento de Las Salviniaceae neotropicales. II. Salvinia auriculata Aublet Darwiniana 12, 499–513. Duarte, C.M., Kalff, J., 1987. Weight-density relationships in submerged macrophytes: the importance of light and plant geometry Oecologia 72, 612–617. Gopal, B., Goel, U., 1993. Competition and allelopathy to aquatic plant communities Bot. Rev. 59, 155–208. Hutchings, M.J., de Kroon, H., 1994. Foraging in plants: the role of morphological plasticity in resource acquisition Adv. Ecol. Res. 25, 159–238. Levin, D.A., 1988. In: A.J. Davy, M.J. Hutchings and A.R. Watkinson (Eds.), Plasticity, canalization and evolutionary stasis in plants. Plant Population Ecology. Blackwell Scientific Publications, pp. 35–46. Madsen, J.D., 1991. Resource allocation at the individual plant level Aquat. Bot. 41, 67–86. Petit, C., Thompson, J.D., Bretagnolle, F., 1996. Phenotypic plasticity in relation to ploidy level and corm production in perennial grass Arhenatherum elatius Can. J. Bot. 74, 1964–1973. Room, P.M., 1988. Effects of temperature, nutrients and a beetle on branch architecture of the floating weed Salvinia molesta and simulations of biological control J. Ecol. 76, 826–848. Room, P.M., 1990. Ecology of a simple plant-herbivore system: biological control of Salvinia Trends Ecol. E 5, 74–79. Samson, D.A., Werk, K.S., 1986. Size-dependent effects in the analysis of reproductive effort in plants Am. Nat. 127, 667–680. Schlichting, C.D., 1986. The evolution of phenotypic plasticity in plants Annu. Rev. Ecol. Sys. 17, 667–693. Sculthorpe, C.D., 1967. The Biology of Aquatic Vascular Plants. Edward Arnold, London, p. 610. Spencer, D.H.N., Campbell, R.M., Crystal, J., 1973. Specific leaf areas and zonation of fresh-water macrophytes J. Ecol. 61, 317–328. Thompson, D.A., Beattie, A.J., 1981. Density-mediated seed and stolon production in Viola (Violaceae) Am. J. Bot. 68, 383–388. Weiner, J., 1988. In: J. Lovett-Doust and L. Lovett-Doust (Eds.), The influence of competition on plant reproduction. Plant reproductive ecology: patterns and strategies. Oxford University Press, Oxford, pp. 228–245.