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Seed germination and early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains
Aquatic Botany 70 (2001) 89–103
Seed germination and early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains Pia Parolin∗ Max-Planck-Institute for Limnology, Tropical Ecology, P.O. Box 165, 24302 Plön, Germany Received 28 January 2000; received in revised form 8 June 2000; accepted 18 January 2001
Abstract Plants are subjected to extended periods of waterlogging and submersion in the floodplains of Central Amazonia. Several adaptations and growth strategies allow them to survive. In this study, germination and seedling growth of seeds of six tree species from nutrient-rich várzea and six from nutrient-poor igapó were analysed in the Amazon Research Institute (INPA) in Manaus, Brazil. Germination rates and duration were lower in species from várzea than from igapó. The cotyledons opened later and had lower longevity in várzea, where the environment provides sufficient nutrients to the establishing seedling and there is less need for nutrient supply by the mother plant. Species from várzea produced smaller seeds and the seedlings tended to grow less than in igapó where large-seeded species predominated. Mortality of waterlogged and submerged seedlings was low in all species, except in submerged seedlings of Senna reticulata. Leaf production and shedding was continuous in the várzea species, but in the species from igapó leaves had higher longevity. An explanation for the dynamic leaf phenology in várzea might be that this is an adaptation against the high sediment load which covers the leaves and impedes photosynthetic activity. Morphological adaptations to flooding (adventitious roots, lenticels, stem hypertrophy) occurred only in waterlogged seedlings from várzea species, maybe as a consequence of the oxygen deficiencies in the rhizosphere caused by the high plant productivity and decomposition in this ecosystem. The production of morphological adaptations might be limited by the low nutrient availability in igapó. The differences in germination and growth in várzea and igapó may be responses to the different nutrient availabilities in the two ecosystems and thus represent different survival strategies. In várzea, morphological adaptations which require high nutrient supply allow the plants to maintain growth and photosynthetic activity at high levels, even during waterlogging. Igapó species have a fast initial growth and constant leaf production, investing in high seed mass, leaf sclerophylly and
∗ Present address: Institut fur Allgemeine Botanik, Universität Hamburg, AB Systematik, Ohnhorststr. 18, 22609 Hamburg, Germany. Tel.: +49-40-880-1007; fax: +49-40-881-29282. E-mail address: [email protected] (P. Parolin).
0304-3770/01/$ – see front matter © 2001 Elsevier Science B.V. All rights reserved. PII: S 0 3 0 4 - 3 7 7 0 ( 0 1 ) 0 0 1 5 0 - 4
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reduced leaf loss. They tend to remain in a state of rest during flooding. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Floodplain forest; Várzea; Igapó; Seed germination; Seedling establishment; Survival strategies; Submergence; Morphological adaptations
1. Introduction The floodplains of Central Amazonia can be divided into nutrient-rich whitewater (várzea) and nutrient-poor blackwater (igapó) ecosystems according to the water quality of the flooding rivers (Prance, 1979). Near Manaus, Brazil, the whitewater river Rio Amazonas (Rio Solimões) and the blackwater river Rio Negro meet. The regular, extended inundations caused by the average annual water level changes of 10 m are the same on the two rivers, as are most environmental factors which can influence tree growth, such as precipitation, light incidence, temperature, and soil pH (Furch, 1997). The main difference lies in the quality of the soils. Whitewater rivers originating in the Andes have a high sediment load and are rich in nutrients. Blackwater rivers have little sediment load and the flooded soils have low nutrient contents (Sombroek, 1979; Sioli, 1984; Furch, 1984, 1997). Flooding represents an important, dominating ecological factor (‘flood pulse concept’, Junk et al., 1989) which affects plants equally in várzea and igapó. The plants growing along the river margins are waterlogged or submerged for up to 210 days every year (Junk, 1989). The extended flooding induces physiological disturbances which become evident as the formation of growth rings (Worbes, 1997) and reductions of CO2 -uptake (Maia, 1997; Parolin, 2000). Changes of transpiration (Parolin, 1997), stomatal closure (Schlüter and Furch, 1992), water potential (Scholander and Perez, 1968), leaf chlorophyll (Furch, 1984) and nitrogen content are induced by waterlogging, as well as reductions of leaf size, growth and biomass production (Parolin, 1997). Root and shoot morphology, and the anatomy of the seedlings can be altered by waterlogging and submersion (Fernandes-Corrêa and Furch, 1992; Schlüter and Furch, 1992; Waldhoff et al., 1998). The differences in nutrient availability between the two ecosystems do, as expected, have consequences for tree growth. The floristic compositions (Prance, 1979; Ayres, 1993; Ferreira, 1997; Amaral et al., 1997), plant growth and productivity (Klinge et al., 1995) differ in várzea and igapó. Species from the várzea have higher net productivity than those from igapó, and the trees have higher increment rates and lower wood densities than in igapó (Worbes, 1997). Inter- and intra-specific differences in wood increment indicate that tree growth is faster in species from whitewater floodplains (Parolin et al., 1998). The exclusive occurrence of fast-growing, light-demanding pioneer species (sensu Swaine and Whitmore, 1988) in várzea suggests that nutrient availability plays a dominant role in tree growth and distribution. Phenological studies show that deciduous and evergreen species occur in both systems, but there is a tendency for evergreen trees with sclerophyllous leaves to predominate in igapó (Worbes, 1997). Big and heavy seeds are found only in nutrient-poor igapó, while in várzea the production of many small to middle sized seeds predominates (Parolin, 2000). In a study of germination and establishment (Parolin, unpublished), differences of cotyledon longevity, leaf length and seedling height were found
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in 31 species of várzea and igapó. Eighty percent of the species from igapó had hypogeal germination with big, fleshy cotyledons, whereas only 30% of the várzea species had these features. These results may reflect the role of nutrient availability in the two ecosystems, where different adaptations and different strategies are needed for survival and growth in relation to periodical flooding. Characteristics like time to germination and initial morphology of the seedlings are closely related to the strategies of establishment of a species at a specific site (Ng, 1978). The purpose of the present study was to compare germination and early growth in typical species from várzea and igapó, and to explore whether the differences point to different adaptive strategies of the plants in the two ecosystems.
2. Methods 2.1. Plant material 12 tree species common in the floodplains around Manaus/Central Amazonia were chosen for this study, six from várzea and six from igapó. The chosen range of species shared a wide array of ecological features including successional status, leaf phenology, level on the flooding gradient, and germination type (Table 1). Most species are restricted to either Table 1 Species from nutrient-rich whitewater (v´arzea) and nutrient-poor blackwater floodplain forests (igap´o) chosen for this studya Species
V´arzea Cecropia latiloba Miq. Crateva benthami Eichl. in Mart. Nectandra amazonum Nees Senna reticulata Willd. (Irwin and Barn) Tabebuia barbata E.Mey. Vitex cymosa Benth. Igap´o Aldina latifolia Spruce ex Benth. Campsiandra comosa Benth. Crudia amazonica Spruce ex Benth. Mora paraensis Ducke Swartzia polyphylla A.DC. Vatairea guianensis Aubl. a
Successional Leaf Level in Germination CO2 -assimilation stage phenology flooding type (mmol m−2 s−1 ) gradient P NP NP P
E D E E
L L L H
E E H E
10.6 ± 1.4 9.2 ± 1.9 6.7 ± 1.6 9.0 ± 0.6
NP NP
D D
L L
H E
6.3 ± 0.9 8.0 ± 1.1
NP
E
H
H
5.1 ± 1.1
NP NP NP NP NP
E D D E E
L L H H H
H H H H H
6.0 ± 0.3 5.9 ± 0.9 6.7 ± 0.5 4.4 ± 0.8 5.1 ± 0.5
Successional stage (P: pioneer; NP: non-pioneer; sensu Swaine and Whitmore, 1988), leaf phenology (E: evergreen; D: deciduous), level on the flooding gradient (L: low: 18–25 m a.s.l.; H; high: 25–28 m a.s.l.), germination type (E: epigeal; H: hypogeal), and mean CO2 -assimilation of the seedlings under normal (non-flooded) conditions.
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várzea or igapó, although Crudia amazonica, Tabebuia barbata, Nectandra amazonum, and Vatairea guianensis can occur in both (Amaral et al., 1997; Ayres, 1993; Ferreira, 1991; Kubitzki, 1989; Parolin et al., 1998; Rankin de Merona and De Merona, 1988; Revilla, 1981; Rosales et al., 1999; Worbes et al., 1992). Mature seeds of each species were collected in the floodplains of the Rio Amazonas (Solimões) and Rio Negro in the vicinity of Manaus, and transported to the Amazon Research Institute (INPA) in Manaus, where germination and growth experiments were performed. 2.2. Experiments Seed germination and seedling development were analysed in the Amazon Research Institute (INPA) in Manaus, Brazil between May 1995 and August 1995 at an open experiment site which was sunny in the morning and in the afternoon, but shady between 11.00 and 14.00 h. 2.2.1. Germination rate and duration Germination rate and duration to germination were determined in seeds placed in plastic cups (300 ml) in mixed soil, in equal proportions, from várzea and igapó. Fifty seeds per species, each in a separate cup, were tested and checked daily for germination. Germination was defined as shoot emergence because in the small-seeded species (Cecropia latiloba, S. reticulata), it was not possible to observe seed opening and radicule emergence of all the seeds without damaging them. Germination rate was calculated by the number of seeds germinated after 7 weeks in relation to total initial seed number (in %). The limitation to 7 weeks (49 days) was chosen because this was the time by which all species had a germination rate of at least 20%. 2.2.2. Seedling development The seedlings resulting from the procedure described in Section 2.2.1 were grown on and the duration to the expansion and longevity of the cotyledons, duration to true leaf expansion, leaf number, leaf length, seedling height and biomass were measured. The results 5 weeks after germination are presented. 2.2.3. Relations between seed weight and seedling biomass The increase (in %) from seed dry mass (=100%) to seedling dry biomass of 5 weeks after germination was calculated for each species. 2.2.4. Submerged germination Ten pairs of each species consisting of one cup with seed + well watered soil and one cup with seed +soil+water (seeds submerged) were tested for germination, here differentiating between seed opening (swelling after absorption of water), germination of the radicula, and germination of the shoot. 2.2.5. Mortality of submerged seedlings Some seedlings obtained from the procedure described in Section 2.2.2 were used to test survival following complete submergence. They were placed in containers filled with water
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in order to cover the whole plant. After 12 weeks, the seedlings were taken out of the water. Survival was defined by the resprout of leaves. 2.2.6. Leaf phenology with waterlogging and submersion The production of new leaves and leaf loss were measured in the waterlogged and submerged seedlings of the 12 species. The results after 12 weeks are presented. 2.2.7. Morphological adaptations to flooding The capacity to produce morphological adaptations against flooding (Gill, 1970; Crawford, 1989; Joly, 1990) was monitored qualitatively, i.e. whether the seedlings produced adventitious roots, lenticels and/or stem hypertrophy. 3. Results 3.1. Germination rate and duration Germination rates after 7 weeks under the given conditions were slightly lower in várzea than in igapó species (Tables 2 and 3), varying between 20% (Campsiandra comosa) and 100% (Mora paraensis, Vtairea guinanensis). Time to germination was also lower in várzea than in igapó species, varying between 5 (S. reticulata, V. guinanensis) and 24 days (C. comosa). Both germination rate and duration until germination were not significantly different in the two ecosystems (Table 3). 3.2. Seedling development The cotyledons opened between means of 2.2 (C. latiloba) and 35 days (C. comosa) after germination, defined as shoot emergence. Species from várzea opened their cotyledons significantly faster than species from igapó (Tables 2 and 3). Mean cotyledon longevity, i.e. the duration until their fall or deterioration, was between 25 (S. reticulata, C. latiloba) and 56 days (N. amazonum). Differences between várzea and igapó were not statistically significant (Table 3). The duration to the expansion of the first leaf after germination was almost five times lower in species from várzea than from igapó, which was highly statistically significant, with a minimum of 3 days in T. barbata and a maximum of 29 days in C. amazonica. At a seedling age of 5 weeks, the average number of expanded leaves was equal in várzea and igapó, with a minimum of 1.5 leaves in C. comosa and a maximum of 8.6 leaves in V. guianensis. The average length of the entire leaves was twice as high in species from igapó as in those from várzea, and mean seedling height at an age of 1 month was six times higher in igapó species. Both leaf length and seedling height were highly statistically significantly different in the two ecosystems (Table 3). The smallest seedlings were those of Vitex cymosa mean height (5.1 cm), the tallest those of V. guianensis (99.7 cm). Mean seed weight of the chosen species varied between 0.002 g in C. latiloba and 69.4 g in Aldina latifolia, and was significantly higher in all igapó species. Mean seedling biomass was 12 times higher in igapó species, varying between 0.58 g DW in C. latiloba and 55.9 g DW in A. latifolia.
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Table 3 Comparison of species from nutrient-rich v´arzea and nutrient-poor igap´o: overall means for the two habitats and statistical significance of the differencesa V´arzea
Germination rate (shoot emergence) (%) Duration until germination (shoot emergence) (days) Shoot germination rate in submerged seeds (%) Duration until cotyledon opening (days) Cotyledon longevity (days) Duration to first leaf after shoot emergence (days) Mean number of expanded leaves Mean leaf length (cm) Mean seedling height (cm) Seed weight (g), n = 10 % DW increment seed to seedling at age 5 weeks a
Igap´o
Average
S.D.
Average
S.D.
65.0 12.4 0.0 13.8 38.9 6.2 3.8 4.5 10.4 0.5 9330
22.8 6.0 0.0 10.3 12.7 2.3 1.5 2.2 7.7 0.8 1419
67.5 13.6 0.0 21.8 44.0 29.0 3.8 9.2 64.1 29.5 95
34.0 7.7 0.0 10.0 4.5 0.0 2.5 2.9 30.8 23.5 26
F-ratio
P
0.521 1.213 – 2.709 2.766 115.728 0.457 65.302 200.842 64.713 178.88
0.539 0.272 – 0.102 0.101 0.0001 0.501 0.0001 0.0001 0.0001 0.0001
F-ratio of the ANOVA and statistical probability P.
3.3. Relations between seed weight and seedling biomass The percentage increase from seed mass (=100%) to seedling biomass was extremely high in the pioneer species from the várzea (33892% in C. latiloba, 19300% in S. reticulata) compared to the non pioneers (901% in T. barbata to 313% in N. amazonum), and to species
Fig. 1. Biomass increase (%) from seed dry mass to seedling dry biomass at an age of 5 weeks, based on five seedlings per species. CL: Cecropia latiloba; SR: Senna reticulata; TB: Tabebuia barbata; CB: Crateva benthami; VC: Vitex cymosa; NA: Nectandra amazonum; CC: Campsiandra comosa; MP: Mora paraensis; CA: Crudia amazonica; SP: Swartzia polyphylla; VG: Vatairea guianensis; AL: Aldina latifolia.
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from igapó (125% in C. comosa to 56% in A. latifolia) (Fig. 1). The differences were highly statistically significant (Table 3). 3.4. Submerged germination Germination rate defined as shoot emergence was nil in all species when the seeds were submerged. In some species from both várzea and igapó, there was seed opening and germination of the radicula in the submerged seeds, but none grew to a seedling (Fig. 2). It is notable that seeds which were not needed for the experiment soon after collection in the field were put into water for conservation. They remained viable for at least 3 months if the
Fig. 2. Seed germination in six species from v´arzea (A) and six species from igap´o (B), with seed opening, germination of the radicula and of the shoot in seeds put on wet soil and in seeds put on wet soil and submerged by water.
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water was changed frequently, while seeds which were kept in the air dried or decomposed within a few days or weeks. 3.5. Mortality of submerged seedlings Seedling mortality after 12 weeks was 100% in S. reticulata, and 0–30% in the other species. 3.6. Leaf phenology with waterlogging and submersion After 12 weeks, the submerged seedlings of the várzea had lost 70–100% of the initial leaves by continuous shedding of the older ones and production of new ones, while igapó species kept all or most of their leaves (Fig. 3). 3.7. Morphological adaptations to flooding The six species from várzea produced adventitious roots, lenticels and stem hypertrophy 2–3 weeks after the start of waterlogging (Table 4). The six species from igapó did not produce any of these morphological adaptations, with the exception of V. guianensis, which produced adventitious roots.
Fig. 3. Reductions of leaf number after 12 weeks of waterlogging and submersion in six species from v´arzea and six species from igap´o.
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Table 4 Morphological adaptations (adventitious roots, lenticels, stem hypertrophy) produced by the species from nutrient-rich whitewater (v´arzea) and nutrient-poor blackwater floodplains (igap´o) subjected to waterlogginga Species
Adventitious roots
Lenticels
Stem hypertrophy
V´arzea Cecropia latiloba Crateva benthami Nectandra amazonum Senna reticulata Tabebuia barbata Vitex cymosa
++ − ++ +++ + ++
+++ +++ − +++ ++ −
+ + − − − −
Igap´o Aldina latifolia Campsiandra comosa Crudia amazonica Mora paraensis Swartzia polyphylla Vatairea guianensis
− − − − − +
− − − − − −
− − − − − −
Production of respective morphological adaptation from − (no production) to +++ (strong production), i.e. adventitious roots exceed 1 m length, or lenticels cover whole submerged stem. a
4. Discussion The differences between species from várzea and igapó in this study point to different adaptive strategies of the plants in the two ecosystems which might be linked to differences in nutrient availability. The timespan of the experiment and the timespans of the individual events monitored (e.g. seedling development) may be related to actual durations of inundation and exposure events in the natural habitats where the duration of inundation depends on the height in the inundation gradient where a plants get established (Ferreira, 1991; Junk, 1989). The timing of the experiments (May–August 1995) corresponded to the period of highest water level of the rivers and beginning of the dry period, i.e. to the period of germination and seedling establishment, and therefore to the seasonal cycles of events in the floodplains. 4.1. Germination The six species from igapó, all with hypogeal germination, had big, fleshy cotyledons which opened faster and had higher longevity than the chosen species from várzea, where the cotyledons were smaller and more foliaceous. The function of the cotyledons in igapó is mainly to supply the establishing plant with nutrients (Hladik and Miquel, 1990) which are not available in the soils. In várzea, the environment provides sufficient nutrients to the establishing seedling and there is less need for nutrient supply by the mother plant. 4.2. Seedling development The differences in seedling development measured in this study can be considered to be adaptations of the seedlings to the specific site conditions, but they are probably also a
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consequence of differences in seed size. In the chosen species from várzea, mean seed mass was 0.5 g, compared to 29.5 g in the six species from igapó. Seeds of different sizes are suited to different germination strategies and establishment conditions (Foster and Janson, 1985). Since small seeds germinate faster than large seeds, and seedling size, growth rate, seedling establishment and survivorship are closely linked to seed size (Murali, 1997), it is to be expected that differences appear in the species from the two ecosystems. Small seeds are advantageous because there are less limits to the amount of seed production, and the higher number of seeds allows occupation of more available microsites. Large seeds allow higher rates of seedling establishment since they have more endosperm and are richer in energy reserves for the developing embryo (Michaels et al., 1988). The importance of the seed reserves is shown by some surplus seeds of A. latifolia which were left on a concrete floor: they germinated and grew to a height of more than 1.20 m without soil and water. Thus, species from várzea produce many small seeds and seedlings from these grow less than those of the big seeds from igapó. Nevertheless, the pioneers in the várzea have the capacity to grow to considerable heights, as reflected in their high biomass increment from seed to seedling. Under natural conditions, C. latiloba and S. reticulata reach heights up to one and four metres, respectively, before the first period of flooding (Parolin, 1997, 1998). The size of seedlings of the other species found in the field did not show such dramatic differences to the seedlings of the experiment (personal observation). Among the chosen species from igapó, large seeded species predominate which produce large, resistant seedlings before the onset of flooding. The 12 species used here represent only a small percentage of the vegetation of each ecosystem, with more than 250 tree species in whitewater floodplain forests and even more species in igapó (Worbes, 1997). The differences of average seed size in várzea and igapó are smaller, but still very significant,
Fig. 4. Freshwater sponge growing on the leaf of a shrub in the blackwater river Tarumã, Manaus, documenting the high leaf longevity in species from igap´o.
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when more species are included. In 31 species from várzea, mean seed mass was 1.16 g, compared to a mean of 7.08 g in 27 species from igapó (Parolin, 2000). 4.3. Effects of waterlogging and submersion Seedlings and adults of the species growing in várzea and igapó are highly flood tolerant and can cope with long periods of flooding. Mortality of waterlogged and submerged seedlings was extremely low in all species, except in submerged seedlings of S. reticulata, a species in which the adult did not survive complete submersion (Parolin, 1998). Leaf phenology with waterlogging was different in species from várzea and igapó. Leaves were produced and shed continuously in the várzea species, whereas igapó species retained the original leaves. The same trend is apparent among adult trees, with more várzea species deciduous than in igapó (Worbes, 1997). Leaf longevity and sclerophylly are probably higher generally in species from igapó (Medina, 1984; Worbes, 1997, Fig. 4). The dynamics of leaf phenology in species from várzea may be related to the high sediment load (Irion et al., 1983). The mud layers which cover the surfaces and persist after emersion, impede photosynthetic activity. If leaves were kept after submersion, they would probably lose most of their function, whereas their loss and replacement is not a limiting factor for survival (Worbes, 1997). 4.4. Morphological adaptations to flooding Morphological adaptations to flooding occurred only in waterlogged seedlings from várzea species, with the exception of the igapó species V. guianensis, which produced adventitious roots. This latter species does, according to Amaral et al. (1997), also occur in whitewater floodplains. Adventitious roots are not restricted to várzea (Fig. 5), but there is a tendency to greater morphological adaptations in várzea. This may be linked to the higher lack of oxygen caused by the high plant productivity and subsequent decomposition, which cause high oxygen deficiencies in the rhizosphere (Furch, 1997). Adventitious roots, lenticels and stem hypertrophy represent important adaptations to supply the roots with oxygen (Crawford, 1989) and so are likely to be of greater importance at the lower oxygen levels which occur in the várzea than in the igapó (Saint-Paul, 1996; Waldhoff et al., 1998). Also, the production of these morphological adaptations may be limited by the low nutrient availability in igapó.
5. Conclusions The differences of germination and growth may be responses to the different nutrient availability in the two ecosystems and thus be related to different survival strategies of the species from várzea and igapó. In várzea, the stress induced by periodical flooding is compensated for by morphological adaptations which require high nutrient supply and allow the plants to maintain growth and photosynthetic activity at high levels also with waterlogging. The production of adventitious roots, lenticels and stem hypertrophy, and the high
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production and loss of leaves observed exclusively in whitewater species indicates highly dynamic activities during flooding. Igapó species, on the other hand, which grow in nutrientpoor environments, cannot ‘afford’ the costly production of morphological adaptations and frequent changes of leaves. Their strategy is to invest in high seed mass, which supports a fast initial growth producing long-lived sclerophyllous leaves and to remain in a state of rest during flooding, whereas the species from várzea adapt to the changing environmental conditions by production and loss of leaves and by longer-term morphological adaptations.
Acknowledgements This study was a collaboration between the Max-Planck-Institute for Limnology, Plön, Germany and the National Amazon Research Institute (INPA), Manaus, Brazil. I wish to thank Leandro V. Ferreira for discussions. References Amaral, I.L., Adis, J., Prance, G.T., 1997. On the vegetation of a seasonal mixedwater inundation forest near Manaus, Brazilian Amazonia. Amazoniana 14 (3/4), 335–347. Ayres, J.M.C., 1993. As matas de várzea do Mamirauá. In: Sociedade Civil Mamirauá (Ed.), Estudos de Mamirauá, Vol. I, pp. 1–123. Crawford, R.M.M., 1989. The anaerobic retreat. In: Crawford, R.M.M. (Ed.), Studies on Plant Survival. Ecological Case Histories of Plant Adaptation to Adversity. Blackwell Scientific, Oxford. Stud. Ecol. 11, 105–129. Fernandes-Corrêa, A.F., Furch, B., 1992. Investigations on the tolerance of several trees to submergence in blackwater (igapó) and whitewater (várzea) inundation forests near Manaus, Central Amazonia. Amazoniana 12 (1), 71–84. Ferreira, L.V., 1991. O efeito do periodo de inundação na zonaçao de comunidades, fenologia e regeneraçao em uma floresta de igapó na Amazonia Central. Masters thesis, 161 pp. Ferreira, L.V., 1997. Is there a difference between the white water floodplain forests (várzea) and black water floodplain forests (igapó) in relation to number of species and density? Rev. Brasileira Ecol. 2, 60–62. Foster, S.A., Janson, C.H., 1985. The relationship between seed size and establishment conditions in tropical woody plants. Ecology 66, 773–780. Furch, B., 1984. Untersuchungen zur überschwemmungstoleranz von bäumen der várzea und des igapó. Blattpigmente. Biogeographica 19, 77–83. Furch, K., 1997. Chemistry of várzea and igapó soils and nutrient inventory in their floodplain forests. In: Junk, W.J. (Ed.), The Central Amazon Floodplain: Ecology of a Pulsing System. Springer, Heidelberg, Ecol. Stud. 126, 47–68. Gill, C.J., 1970. The flooding tolerance of woody species — a review. For. Abstr. 31 (4), 671–688. Hladik, A., Miquel, S., 1990. Seedling types and plant establishment in an African rain forest. In: Bawa, K.S., Hadley, M. (Eds.), Reproductive Ecology of Tropical Forest Plants. Man Biosphere Ser. 7, 261–282. Irion, G., Adis, J., Junk, W.J., Wunderlich, F., 1983. Sedimentological studies of the, Ilha de Marchantaria‘ in the Solimões/Amazon River near Manaus. Amazoniana 8, 1–18. Joly, C.A., 1990. Adaptaçoes de plantas de savanas e florestas neotropicais a inundação. In: Sarmiento, G. (Ed.), Las Sabanas Americanas: Aspectos de su Biogeograf´ıa, Ecolog´ıa y Utilización. Fundación Fondo Editorial Acta Cient´ıfica Venezolana, Caracas, pp. S.243–257. Junk, W.J., 1989. Flood tolerance and tree distribution in Central Amazonian floodplains. In: Nielsen, L.B., Nielsen, I.C., Balslev. H. (Eds.), Tropical Forests: Botanical Dynamics, Speciation and Diversity. Academic Press, London, pp. 47–64. Junk, W.J., Bayley, P.B., Sparks, R.E., 1989. The flood pulse concept in river-floodplain systems. In: Dodge, D.P. (Ed.), Proceedings of the International Large River Symposium. Can. Publ. Fish. Aquat. Sci. 106, 110–127.
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Klinge, H., Adis, J., Worbes, M., 1995. The vegetation of a seasonal várzea forest in the lower Solimões River, Amazon region of Brazil. Acta Amazonica 25 (3/4), 201–220. Kubitzki, K., 1989. The ecogeographical differentiation of Amazonian inundation forests. Plant Syst. E 162, 285–304. Maia, L.M.A., 1997. Influência do pulso de inundação na fisiologia, fenologia e produçao de frutos de Hevea spruceana (Euphorbiaceae) e Eschweilera tenuifolia (Lecythidaceae), em área inundável de igapó da Amazônia central. Ph.D. Thesis, INPA/FUA Manaus, 186 pp. Medina, E., 1984. Nutrient balance and physiological processes at the leaf level. In: Medina, E., Mooney, H.A., Vazques-Yanes, C. (Eds.), Physiological Ecology of Plants of the Wet Tropics. Kluwer Academic Publishers, Boston, pp. 134–154. Michaels, H.J., Benner, B., Hartgerink, A.P., Lee, T.D., Rice, S., Willson, M.F., Bertin, R.I., 1988. Seed size variation: magnitude, distribution, and ecological correlates. Evol. Ecol. 2, 157–166. Murali, K.S., 1997. Patterns of seed size, germination and seed viability of tropical tree species in southern India. Biotropica 29 (3), 271–279. Ng, F.S.P., 1978. Strategies of establishment in Malayan forest trees. In: Tomlinson, P.B., Zimmermann, M.H. (Eds.), Tropical Trees as Living Systems. Cambridge University Press, Cambridge, MA, pp. 129–162. Parolin, P., 1997. Auswirkungen Periodischer Vernässung und Überflutung auf Phänologie, Photosynthese und Blattphysiologie von Baumarten unterschiedlicher Wachstumsstrategie in zentralamazonischen Überschwemmungsgebieten. Herbert Utz Verlag Wissenschaft, München, 166 pp. Parolin, P., 1998. Floristic composition and structure of two stands of Senna reticulata differing in age. Amazoniana 15 (1/2), 113–128. Parolin, P., 2000. Seed mass in Amazonian floodplain forests with contrasting nutrient supplies. J. Trop. Ecol. 16, 417–428. Parolin, P., Ferreira, L.V., Junk, W.J., 1998. Central Amazonian floodplains: effect of two water types on the wood density of trees. Verh. Int. Verein. Limnol. 26 (3), 1106–1112. Parolin, P. 2000. Phenology an CO2 -assimilation of trees in Central Amazonian floodplains, J. Trop. Ecol. 16 (3), 465–473. Prance, G.T., 1979. Notes on the vegetation of Amazonia. III. Terminology of Amazonian forest types subjected to inundation, Brittonia, New York. Bot. Garden 31 (1), 26–38. Rankin de Merona, J., De Merona, B., 1988. Les rélations poissons — forêt. In: Conditions Ecologiques et Economiques de la Production d’une ˆıle de Várzea: l’ˆıle du Careiro. Rapport Terminal ORSTOM, pp. 202–228. Revilla, J.D.C., 1981. Aspectos flor´ısticos e Fitossociológicos do Igapó De Praia Grande, Rio Negro, Amazonas. INPA, Manaus, 129 pp. Rosales, J.G., Petts, G., Salo, J., 1999. Riparian flooded forests of the Orinoco and Amazon basins: a comparative review. Biodivers. Conserv. 8, 551–586. Saint-Paul, U., 1996. Comparison of seasonal and diurnal vertical oxygen distributions in Central Amazonian white and black water lakes. Ecotropica 2 (1), 73–77. Schlüter, U.-B., Furch, B., 1992. Morphologische, anatomische und physiologische Untersuchungen zur Überflutungstoleranz des Baumes Macrolobium acaciaefolium, charakteristisch für die Weiß- und Schwarzwasserüberschwemmungswälder bei Manaus, Amazonas. Amazoniana XII (1), 51–69. Scholander, P.F., Perez, M.O., 1968. Sap tension in flooded trees and bushes of the Amazon. Plant Physiol. 43, 1870–1873. Sioli, H., 1984. The Amazon and its main affluents: hydrography, morphology of the river courses, and river types. In: Sioli, H. (Ed.), The Amazon. Dr. Junk Publishers, Dordrecht, Boston, Lancaster, pp. 127–165. Sombroek, W.G., 1979. Soils of the Amazon region and their ecological stability, ISM Annual Report, pp. 13–27. Swaine, M.D., Whitmore, T.C., 1988. On the definition of ecological species groups in tropical rain forests. Vegetatio 75, 81–86. Waldhoff, D., Junk, W.J., Furch, B., 1998. Responses of three Central Amazonian tree species to drought and flooding under controlled conditions. Int. J. Ecol. Environ. 24, 237–252. Worbes, M., 1997. The forest ecosystem of the floodplains. In: Junk, W.J. (Ed.), The Central Amazon Floodplain: Ecology of a Pulsing System. Springer, Heidelberg. Ecol. Stud. 126, 223–266. Worbes, M., Worbes, M., Klinge, H., Revilla, J.D., Martius, C., 1992. On the dynamics, floristic subdivision and geographical distribution of Várzea forests in Central Amazonia. J. Vegetation Sci. 3, 553–564.
Seed germination and early establishment of 12 tree species from nutrient-rich and nutrient-poor Central Amazonian floodplains Pia Parolin∗ Max-Planck-Institute for Limnology, Tropical Ecology, P.O. Box 165, 24302 Plön, Germany Received 28 January 2000; received in revised form 8 June 2000; accepted 18 January 2001
Abstract Plants are subjected to extended periods of waterlogging and submersion in the floodplains of Central Amazonia. Several adaptations and growth strategies allow them to survive. In this study, germination and seedling growth of seeds of six tree species from nutrient-rich várzea and six from nutrient-poor igapó were analysed in the Amazon Research Institute (INPA) in Manaus, Brazil. Germination rates and duration were lower in species from várzea than from igapó. The cotyledons opened later and had lower longevity in várzea, where the environment provides sufficient nutrients to the establishing seedling and there is less need for nutrient supply by the mother plant. Species from várzea produced smaller seeds and the seedlings tended to grow less than in igapó where large-seeded species predominated. Mortality of waterlogged and submerged seedlings was low in all species, except in submerged seedlings of Senna reticulata. Leaf production and shedding was continuous in the várzea species, but in the species from igapó leaves had higher longevity. An explanation for the dynamic leaf phenology in várzea might be that this is an adaptation against the high sediment load which covers the leaves and impedes photosynthetic activity. Morphological adaptations to flooding (adventitious roots, lenticels, stem hypertrophy) occurred only in waterlogged seedlings from várzea species, maybe as a consequence of the oxygen deficiencies in the rhizosphere caused by the high plant productivity and decomposition in this ecosystem. The production of morphological adaptations might be limited by the low nutrient availability in igapó. The differences in germination and growth in várzea and igapó may be responses to the different nutrient availabilities in the two ecosystems and thus represent different survival strategies. In várzea, morphological adaptations which require high nutrient supply allow the plants to maintain growth and photosynthetic activity at high levels, even during waterlogging. Igapó species have a fast initial growth and constant leaf production, investing in high seed mass, leaf sclerophylly and
∗ Present address: Institut fur Allgemeine Botanik, Universität Hamburg, AB Systematik, Ohnhorststr. 18, 22609 Hamburg, Germany. Tel.: +49-40-880-1007; fax: +49-40-881-29282. E-mail address: [email protected] (P. Parolin).
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reduced leaf loss. They tend to remain in a state of rest during flooding. © 2001 Elsevier Science B.V. All rights reserved. Keywords: Floodplain forest; Várzea; Igapó; Seed germination; Seedling establishment; Survival strategies; Submergence; Morphological adaptations
1. Introduction The floodplains of Central Amazonia can be divided into nutrient-rich whitewater (várzea) and nutrient-poor blackwater (igapó) ecosystems according to the water quality of the flooding rivers (Prance, 1979). Near Manaus, Brazil, the whitewater river Rio Amazonas (Rio Solimões) and the blackwater river Rio Negro meet. The regular, extended inundations caused by the average annual water level changes of 10 m are the same on the two rivers, as are most environmental factors which can influence tree growth, such as precipitation, light incidence, temperature, and soil pH (Furch, 1997). The main difference lies in the quality of the soils. Whitewater rivers originating in the Andes have a high sediment load and are rich in nutrients. Blackwater rivers have little sediment load and the flooded soils have low nutrient contents (Sombroek, 1979; Sioli, 1984; Furch, 1984, 1997). Flooding represents an important, dominating ecological factor (‘flood pulse concept’, Junk et al., 1989) which affects plants equally in várzea and igapó. The plants growing along the river margins are waterlogged or submerged for up to 210 days every year (Junk, 1989). The extended flooding induces physiological disturbances which become evident as the formation of growth rings (Worbes, 1997) and reductions of CO2 -uptake (Maia, 1997; Parolin, 2000). Changes of transpiration (Parolin, 1997), stomatal closure (Schlüter and Furch, 1992), water potential (Scholander and Perez, 1968), leaf chlorophyll (Furch, 1984) and nitrogen content are induced by waterlogging, as well as reductions of leaf size, growth and biomass production (Parolin, 1997). Root and shoot morphology, and the anatomy of the seedlings can be altered by waterlogging and submersion (Fernandes-Corrêa and Furch, 1992; Schlüter and Furch, 1992; Waldhoff et al., 1998). The differences in nutrient availability between the two ecosystems do, as expected, have consequences for tree growth. The floristic compositions (Prance, 1979; Ayres, 1993; Ferreira, 1997; Amaral et al., 1997), plant growth and productivity (Klinge et al., 1995) differ in várzea and igapó. Species from the várzea have higher net productivity than those from igapó, and the trees have higher increment rates and lower wood densities than in igapó (Worbes, 1997). Inter- and intra-specific differences in wood increment indicate that tree growth is faster in species from whitewater floodplains (Parolin et al., 1998). The exclusive occurrence of fast-growing, light-demanding pioneer species (sensu Swaine and Whitmore, 1988) in várzea suggests that nutrient availability plays a dominant role in tree growth and distribution. Phenological studies show that deciduous and evergreen species occur in both systems, but there is a tendency for evergreen trees with sclerophyllous leaves to predominate in igapó (Worbes, 1997). Big and heavy seeds are found only in nutrient-poor igapó, while in várzea the production of many small to middle sized seeds predominates (Parolin, 2000). In a study of germination and establishment (Parolin, unpublished), differences of cotyledon longevity, leaf length and seedling height were found
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in 31 species of várzea and igapó. Eighty percent of the species from igapó had hypogeal germination with big, fleshy cotyledons, whereas only 30% of the várzea species had these features. These results may reflect the role of nutrient availability in the two ecosystems, where different adaptations and different strategies are needed for survival and growth in relation to periodical flooding. Characteristics like time to germination and initial morphology of the seedlings are closely related to the strategies of establishment of a species at a specific site (Ng, 1978). The purpose of the present study was to compare germination and early growth in typical species from várzea and igapó, and to explore whether the differences point to different adaptive strategies of the plants in the two ecosystems.
2. Methods 2.1. Plant material 12 tree species common in the floodplains around Manaus/Central Amazonia were chosen for this study, six from várzea and six from igapó. The chosen range of species shared a wide array of ecological features including successional status, leaf phenology, level on the flooding gradient, and germination type (Table 1). Most species are restricted to either Table 1 Species from nutrient-rich whitewater (v´arzea) and nutrient-poor blackwater floodplain forests (igap´o) chosen for this studya Species
V´arzea Cecropia latiloba Miq. Crateva benthami Eichl. in Mart. Nectandra amazonum Nees Senna reticulata Willd. (Irwin and Barn) Tabebuia barbata E.Mey. Vitex cymosa Benth. Igap´o Aldina latifolia Spruce ex Benth. Campsiandra comosa Benth. Crudia amazonica Spruce ex Benth. Mora paraensis Ducke Swartzia polyphylla A.DC. Vatairea guianensis Aubl. a
Successional Leaf Level in Germination CO2 -assimilation stage phenology flooding type (mmol m−2 s−1 ) gradient P NP NP P
E D E E
L L L H
E E H E
10.6 ± 1.4 9.2 ± 1.9 6.7 ± 1.6 9.0 ± 0.6
NP NP
D D
L L
H E
6.3 ± 0.9 8.0 ± 1.1
NP
E
H
H
5.1 ± 1.1
NP NP NP NP NP
E D D E E
L L H H H
H H H H H
6.0 ± 0.3 5.9 ± 0.9 6.7 ± 0.5 4.4 ± 0.8 5.1 ± 0.5
Successional stage (P: pioneer; NP: non-pioneer; sensu Swaine and Whitmore, 1988), leaf phenology (E: evergreen; D: deciduous), level on the flooding gradient (L: low: 18–25 m a.s.l.; H; high: 25–28 m a.s.l.), germination type (E: epigeal; H: hypogeal), and mean CO2 -assimilation of the seedlings under normal (non-flooded) conditions.
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várzea or igapó, although Crudia amazonica, Tabebuia barbata, Nectandra amazonum, and Vatairea guianensis can occur in both (Amaral et al., 1997; Ayres, 1993; Ferreira, 1991; Kubitzki, 1989; Parolin et al., 1998; Rankin de Merona and De Merona, 1988; Revilla, 1981; Rosales et al., 1999; Worbes et al., 1992). Mature seeds of each species were collected in the floodplains of the Rio Amazonas (Solimões) and Rio Negro in the vicinity of Manaus, and transported to the Amazon Research Institute (INPA) in Manaus, where germination and growth experiments were performed. 2.2. Experiments Seed germination and seedling development were analysed in the Amazon Research Institute (INPA) in Manaus, Brazil between May 1995 and August 1995 at an open experiment site which was sunny in the morning and in the afternoon, but shady between 11.00 and 14.00 h. 2.2.1. Germination rate and duration Germination rate and duration to germination were determined in seeds placed in plastic cups (300 ml) in mixed soil, in equal proportions, from várzea and igapó. Fifty seeds per species, each in a separate cup, were tested and checked daily for germination. Germination was defined as shoot emergence because in the small-seeded species (Cecropia latiloba, S. reticulata), it was not possible to observe seed opening and radicule emergence of all the seeds without damaging them. Germination rate was calculated by the number of seeds germinated after 7 weeks in relation to total initial seed number (in %). The limitation to 7 weeks (49 days) was chosen because this was the time by which all species had a germination rate of at least 20%. 2.2.2. Seedling development The seedlings resulting from the procedure described in Section 2.2.1 were grown on and the duration to the expansion and longevity of the cotyledons, duration to true leaf expansion, leaf number, leaf length, seedling height and biomass were measured. The results 5 weeks after germination are presented. 2.2.3. Relations between seed weight and seedling biomass The increase (in %) from seed dry mass (=100%) to seedling dry biomass of 5 weeks after germination was calculated for each species. 2.2.4. Submerged germination Ten pairs of each species consisting of one cup with seed + well watered soil and one cup with seed +soil+water (seeds submerged) were tested for germination, here differentiating between seed opening (swelling after absorption of water), germination of the radicula, and germination of the shoot. 2.2.5. Mortality of submerged seedlings Some seedlings obtained from the procedure described in Section 2.2.2 were used to test survival following complete submergence. They were placed in containers filled with water
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in order to cover the whole plant. After 12 weeks, the seedlings were taken out of the water. Survival was defined by the resprout of leaves. 2.2.6. Leaf phenology with waterlogging and submersion The production of new leaves and leaf loss were measured in the waterlogged and submerged seedlings of the 12 species. The results after 12 weeks are presented. 2.2.7. Morphological adaptations to flooding The capacity to produce morphological adaptations against flooding (Gill, 1970; Crawford, 1989; Joly, 1990) was monitored qualitatively, i.e. whether the seedlings produced adventitious roots, lenticels and/or stem hypertrophy. 3. Results 3.1. Germination rate and duration Germination rates after 7 weeks under the given conditions were slightly lower in várzea than in igapó species (Tables 2 and 3), varying between 20% (Campsiandra comosa) and 100% (Mora paraensis, Vtairea guinanensis). Time to germination was also lower in várzea than in igapó species, varying between 5 (S. reticulata, V. guinanensis) and 24 days (C. comosa). Both germination rate and duration until germination were not significantly different in the two ecosystems (Table 3). 3.2. Seedling development The cotyledons opened between means of 2.2 (C. latiloba) and 35 days (C. comosa) after germination, defined as shoot emergence. Species from várzea opened their cotyledons significantly faster than species from igapó (Tables 2 and 3). Mean cotyledon longevity, i.e. the duration until their fall or deterioration, was between 25 (S. reticulata, C. latiloba) and 56 days (N. amazonum). Differences between várzea and igapó were not statistically significant (Table 3). The duration to the expansion of the first leaf after germination was almost five times lower in species from várzea than from igapó, which was highly statistically significant, with a minimum of 3 days in T. barbata and a maximum of 29 days in C. amazonica. At a seedling age of 5 weeks, the average number of expanded leaves was equal in várzea and igapó, with a minimum of 1.5 leaves in C. comosa and a maximum of 8.6 leaves in V. guianensis. The average length of the entire leaves was twice as high in species from igapó as in those from várzea, and mean seedling height at an age of 1 month was six times higher in igapó species. Both leaf length and seedling height were highly statistically significantly different in the two ecosystems (Table 3). The smallest seedlings were those of Vitex cymosa mean height (5.1 cm), the tallest those of V. guianensis (99.7 cm). Mean seed weight of the chosen species varied between 0.002 g in C. latiloba and 69.4 g in Aldina latifolia, and was significantly higher in all igapó species. Mean seedling biomass was 12 times higher in igapó species, varying between 0.58 g DW in C. latiloba and 55.9 g DW in A. latifolia.
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Table 3 Comparison of species from nutrient-rich v´arzea and nutrient-poor igap´o: overall means for the two habitats and statistical significance of the differencesa V´arzea
Germination rate (shoot emergence) (%) Duration until germination (shoot emergence) (days) Shoot germination rate in submerged seeds (%) Duration until cotyledon opening (days) Cotyledon longevity (days) Duration to first leaf after shoot emergence (days) Mean number of expanded leaves Mean leaf length (cm) Mean seedling height (cm) Seed weight (g), n = 10 % DW increment seed to seedling at age 5 weeks a
Igap´o
Average
S.D.
Average
S.D.
65.0 12.4 0.0 13.8 38.9 6.2 3.8 4.5 10.4 0.5 9330
22.8 6.0 0.0 10.3 12.7 2.3 1.5 2.2 7.7 0.8 1419
67.5 13.6 0.0 21.8 44.0 29.0 3.8 9.2 64.1 29.5 95
34.0 7.7 0.0 10.0 4.5 0.0 2.5 2.9 30.8 23.5 26
F-ratio
P
0.521 1.213 – 2.709 2.766 115.728 0.457 65.302 200.842 64.713 178.88
0.539 0.272 – 0.102 0.101 0.0001 0.501 0.0001 0.0001 0.0001 0.0001
F-ratio of the ANOVA and statistical probability P.
3.3. Relations between seed weight and seedling biomass The percentage increase from seed mass (=100%) to seedling biomass was extremely high in the pioneer species from the várzea (33892% in C. latiloba, 19300% in S. reticulata) compared to the non pioneers (901% in T. barbata to 313% in N. amazonum), and to species
Fig. 1. Biomass increase (%) from seed dry mass to seedling dry biomass at an age of 5 weeks, based on five seedlings per species. CL: Cecropia latiloba; SR: Senna reticulata; TB: Tabebuia barbata; CB: Crateva benthami; VC: Vitex cymosa; NA: Nectandra amazonum; CC: Campsiandra comosa; MP: Mora paraensis; CA: Crudia amazonica; SP: Swartzia polyphylla; VG: Vatairea guianensis; AL: Aldina latifolia.
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from igapó (125% in C. comosa to 56% in A. latifolia) (Fig. 1). The differences were highly statistically significant (Table 3). 3.4. Submerged germination Germination rate defined as shoot emergence was nil in all species when the seeds were submerged. In some species from both várzea and igapó, there was seed opening and germination of the radicula in the submerged seeds, but none grew to a seedling (Fig. 2). It is notable that seeds which were not needed for the experiment soon after collection in the field were put into water for conservation. They remained viable for at least 3 months if the
Fig. 2. Seed germination in six species from v´arzea (A) and six species from igap´o (B), with seed opening, germination of the radicula and of the shoot in seeds put on wet soil and in seeds put on wet soil and submerged by water.
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water was changed frequently, while seeds which were kept in the air dried or decomposed within a few days or weeks. 3.5. Mortality of submerged seedlings Seedling mortality after 12 weeks was 100% in S. reticulata, and 0–30% in the other species. 3.6. Leaf phenology with waterlogging and submersion After 12 weeks, the submerged seedlings of the várzea had lost 70–100% of the initial leaves by continuous shedding of the older ones and production of new ones, while igapó species kept all or most of their leaves (Fig. 3). 3.7. Morphological adaptations to flooding The six species from várzea produced adventitious roots, lenticels and stem hypertrophy 2–3 weeks after the start of waterlogging (Table 4). The six species from igapó did not produce any of these morphological adaptations, with the exception of V. guianensis, which produced adventitious roots.
Fig. 3. Reductions of leaf number after 12 weeks of waterlogging and submersion in six species from v´arzea and six species from igap´o.
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Table 4 Morphological adaptations (adventitious roots, lenticels, stem hypertrophy) produced by the species from nutrient-rich whitewater (v´arzea) and nutrient-poor blackwater floodplains (igap´o) subjected to waterlogginga Species
Adventitious roots
Lenticels
Stem hypertrophy
V´arzea Cecropia latiloba Crateva benthami Nectandra amazonum Senna reticulata Tabebuia barbata Vitex cymosa
++ − ++ +++ + ++
+++ +++ − +++ ++ −
+ + − − − −
Igap´o Aldina latifolia Campsiandra comosa Crudia amazonica Mora paraensis Swartzia polyphylla Vatairea guianensis
− − − − − +
− − − − − −
− − − − − −
Production of respective morphological adaptation from − (no production) to +++ (strong production), i.e. adventitious roots exceed 1 m length, or lenticels cover whole submerged stem. a
4. Discussion The differences between species from várzea and igapó in this study point to different adaptive strategies of the plants in the two ecosystems which might be linked to differences in nutrient availability. The timespan of the experiment and the timespans of the individual events monitored (e.g. seedling development) may be related to actual durations of inundation and exposure events in the natural habitats where the duration of inundation depends on the height in the inundation gradient where a plants get established (Ferreira, 1991; Junk, 1989). The timing of the experiments (May–August 1995) corresponded to the period of highest water level of the rivers and beginning of the dry period, i.e. to the period of germination and seedling establishment, and therefore to the seasonal cycles of events in the floodplains. 4.1. Germination The six species from igapó, all with hypogeal germination, had big, fleshy cotyledons which opened faster and had higher longevity than the chosen species from várzea, where the cotyledons were smaller and more foliaceous. The function of the cotyledons in igapó is mainly to supply the establishing plant with nutrients (Hladik and Miquel, 1990) which are not available in the soils. In várzea, the environment provides sufficient nutrients to the establishing seedling and there is less need for nutrient supply by the mother plant. 4.2. Seedling development The differences in seedling development measured in this study can be considered to be adaptations of the seedlings to the specific site conditions, but they are probably also a
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consequence of differences in seed size. In the chosen species from várzea, mean seed mass was 0.5 g, compared to 29.5 g in the six species from igapó. Seeds of different sizes are suited to different germination strategies and establishment conditions (Foster and Janson, 1985). Since small seeds germinate faster than large seeds, and seedling size, growth rate, seedling establishment and survivorship are closely linked to seed size (Murali, 1997), it is to be expected that differences appear in the species from the two ecosystems. Small seeds are advantageous because there are less limits to the amount of seed production, and the higher number of seeds allows occupation of more available microsites. Large seeds allow higher rates of seedling establishment since they have more endosperm and are richer in energy reserves for the developing embryo (Michaels et al., 1988). The importance of the seed reserves is shown by some surplus seeds of A. latifolia which were left on a concrete floor: they germinated and grew to a height of more than 1.20 m without soil and water. Thus, species from várzea produce many small seeds and seedlings from these grow less than those of the big seeds from igapó. Nevertheless, the pioneers in the várzea have the capacity to grow to considerable heights, as reflected in their high biomass increment from seed to seedling. Under natural conditions, C. latiloba and S. reticulata reach heights up to one and four metres, respectively, before the first period of flooding (Parolin, 1997, 1998). The size of seedlings of the other species found in the field did not show such dramatic differences to the seedlings of the experiment (personal observation). Among the chosen species from igapó, large seeded species predominate which produce large, resistant seedlings before the onset of flooding. The 12 species used here represent only a small percentage of the vegetation of each ecosystem, with more than 250 tree species in whitewater floodplain forests and even more species in igapó (Worbes, 1997). The differences of average seed size in várzea and igapó are smaller, but still very significant,
Fig. 4. Freshwater sponge growing on the leaf of a shrub in the blackwater river Tarumã, Manaus, documenting the high leaf longevity in species from igap´o.
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when more species are included. In 31 species from várzea, mean seed mass was 1.16 g, compared to a mean of 7.08 g in 27 species from igapó (Parolin, 2000). 4.3. Effects of waterlogging and submersion Seedlings and adults of the species growing in várzea and igapó are highly flood tolerant and can cope with long periods of flooding. Mortality of waterlogged and submerged seedlings was extremely low in all species, except in submerged seedlings of S. reticulata, a species in which the adult did not survive complete submersion (Parolin, 1998). Leaf phenology with waterlogging was different in species from várzea and igapó. Leaves were produced and shed continuously in the várzea species, whereas igapó species retained the original leaves. The same trend is apparent among adult trees, with more várzea species deciduous than in igapó (Worbes, 1997). Leaf longevity and sclerophylly are probably higher generally in species from igapó (Medina, 1984; Worbes, 1997, Fig. 4). The dynamics of leaf phenology in species from várzea may be related to the high sediment load (Irion et al., 1983). The mud layers which cover the surfaces and persist after emersion, impede photosynthetic activity. If leaves were kept after submersion, they would probably lose most of their function, whereas their loss and replacement is not a limiting factor for survival (Worbes, 1997). 4.4. Morphological adaptations to flooding Morphological adaptations to flooding occurred only in waterlogged seedlings from várzea species, with the exception of the igapó species V. guianensis, which produced adventitious roots. This latter species does, according to Amaral et al. (1997), also occur in whitewater floodplains. Adventitious roots are not restricted to várzea (Fig. 5), but there is a tendency to greater morphological adaptations in várzea. This may be linked to the higher lack of oxygen caused by the high plant productivity and subsequent decomposition, which cause high oxygen deficiencies in the rhizosphere (Furch, 1997). Adventitious roots, lenticels and stem hypertrophy represent important adaptations to supply the roots with oxygen (Crawford, 1989) and so are likely to be of greater importance at the lower oxygen levels which occur in the várzea than in the igapó (Saint-Paul, 1996; Waldhoff et al., 1998). Also, the production of these morphological adaptations may be limited by the low nutrient availability in igapó.
5. Conclusions The differences of germination and growth may be responses to the different nutrient availability in the two ecosystems and thus be related to different survival strategies of the species from várzea and igapó. In várzea, the stress induced by periodical flooding is compensated for by morphological adaptations which require high nutrient supply and allow the plants to maintain growth and photosynthetic activity at high levels also with waterlogging. The production of adventitious roots, lenticels and stem hypertrophy, and the high
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production and loss of leaves observed exclusively in whitewater species indicates highly dynamic activities during flooding. Igapó species, on the other hand, which grow in nutrientpoor environments, cannot ‘afford’ the costly production of morphological adaptations and frequent changes of leaves. Their strategy is to invest in high seed mass, which supports a fast initial growth producing long-lived sclerophyllous leaves and to remain in a state of rest during flooding, whereas the species from várzea adapt to the changing environmental conditions by production and loss of leaves and by longer-term morphological adaptations.
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