Diversity of leaf deciduousness in important trees of dry tropical forest, India

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1 177 Biodiversity in Tropical Ecosystems (2015) : Editor : Prof. S. K. Tripathi Today and Tomorrow s Printers and Publishers, New Delhi ISBN (India) ISBN (USA) Diversity of leaf deciduousness in important trees of dry tropical forest, India C.P. Kushwaha *, S.K. Tripathi 1, K.P. Singh Department of Botany, Banaras Hindu University, Varanasi, Present address: Department of Forestry, Mizoram University, Aizawl Abstract Introduction Tropical trees exhibit variations in leaf initiation, maturation and leaf fall patterns. This study has demonstrated the diversity of these leaf events in various tropical trees and their possible ecological adaptive mechanism of these species to survive in extreme events. The results of the study has strong implication for global climate change scenario on changing pattern of leafing of tropical trees in Vindhyan dry tropical region which is experiencing high degree of environmental change due to increased industrial intensification. Plant phenological patterns are amongst the most sensitive parameters assumed to be altered as a result of global climate change (Corlett and Lafrankie 1998). Plant phenological patterns are the outcome of plant responses to particular environmental conditions where they are growing. The phenological patterns are varying widely at various spatial and temporal scales among the vegetation around the world. Phenological patterns in tropical deciduous forest trees are difficult to study because of huge diversity in phenological events and even the available information with variable often confusing terminology that makes it more difficult to generalize the results of species data into broader geographical area i.e. biome (Singh and Kushwaha 2005a). Most studies available on community level phenology may not be appropriate for climatic change issues because certain *Corresponding author: kushwahacp@yahoo.com / kushwahacp@gmail.com

2 178 information are lost in recording and so represents less diversity in phenological events. Quantitative approach to phenological studies at species or functional type level would be of great importance, particularly in tropical deciduous forests. Species level quantitative phenological studies of tropical trees are available with respect to timing and duration of different phenological events at level of species or functional types along with their interrelations and possible causal links between environmental variables and phenology (Borchert et al. 2002, Kushwaha and Singh 2005). Widely distributed tropical forests play significant role in global carbon and regional water cycles, sustain large human populations, acts as sites of biological and cultural conservation, and have large economic values. Tropical deciduous forests are broadly defined as tree dominated communities growing in climates characterized by alternating wet and dry periods with extended drought ( ca. 4-8 months during each annual cycle) during which the ratio of potential evaporation to rainfall is greater than one (Olivares and Medina 1992). Because of the prolonged drought in these forests, the predominant tree species showing degree of deciduousness as early dry season leaf fall and growth resumption after the onset of rainy season. Tropical deciduous forests represent great diversity of tree forming a mosaic composed of several phenological functional types adapted to seasonal drought in different ways (Borchert et al. 2002). This results in maintenance of high leaf cover well beyond the rainy season and least synchronization between periodic growth period of trees and duration of dry season. In tropics, the degree of drought to which trees are exposed varies widely, depending on temperature and availability of soil water, and also tree characteristics such as rooting depth (van Schaik et al. 1993) all depend on site characteristics like elevation, soil conditions, and extent of seasonality. The extent and intensity of seasonal drought may differ with the geographical location in dry tropics; for instance, Costa Rican dry tropics (having low latitude of ~10 N; low annual temperature variability to <2 C and 5 months dry period) sharply contrasts with Indian Vindhyan dry tropics (having higher latitude of ~24 N; higher annual temperature variation to >20 C and 8 months dry period) (Singh and Kushwaha 2005a). Structural and ecophysiological properties of dry tropical forests are closely determined by the duration and seasonality of the dry period, which selects adaptations associated with avoidance, resistance, or tolerance to water stress.

3 179 Leaf flush and fall Marked annual periodicity in both leaf-exchanging and deciduous species has been observed due to episodic leaf flush and senescence in tropical deciduous forests. However, considerable diversity exists in timing of both events among species because of tree water status, which represents the interaction between the environmental water status and structural and functional state of tree (Borchert 2000). Recent quantitative and ecophysiological studies (e.g. timing, synchrony and inter-annual variation in vegetative bud break) showed that vegetative bud break (leaf flush initiation) in deciduous and semievergreen species mainly between be and triggered by factors; a) shedding of old leaves during mid dry season, b) increasing day length and/or temperature during late dry season, and c) first significant rain (>20-30 mm) of rainy season (Rivera et al. 2002, Singh and Kushwaha 2005a, Elliott et al. 2006). Leaf-exchanging (evergreen as well as semi-evergreen) species generally show vegetative bud break induced by shedding of old leaves and are mostly located on moist microhabitats within the tropical deciduous forests. In such species timing of bud break varies considerably among conspecific individuals depending on soil water availability and inter-annual variation in the last major rain of rainy season (Rivera et al. 2002, Singh and Kushwaha 2005b). In deciduous species bud break of vegetative buds is either induced by increasing photoperiod and/or temperature or by first significant rain of the rainy season. Bud break induced by the increasing day length and/or temperature occur around spring equinox a period with increasing day length (spring flushing, Rivera et al. 2002) or during late dry season when both day length and temperature are increasing (summer flushing, Kushwaha and Singh 2005). Such bud break occurs well before the first significant rain of rainy season and is highly synchronous in a landscape and show minimum inter-annual variation. In Indian tropical deciduous forest bulk of species show synchronous leaf initiation during hot-dry summer, suggesting the joint action of increasing day length and temperature in bud breaks. In dry tropics, both spring and summer flushing generally precede first rains by 1-2 month, suggesting their timing has been selected for by the rainfall patterns. Rain induced bud break occur after the first significant rain of rainy season. Rapid rehydration due to rains result in synchronous bud breaks in all individuals at a given site. Such bud break varies significantly between sites and years depending on the date of first rains. Apart from varying timing of leaf flush initiation, tropical trees also varies in term of leaf flush duration that decreases with increase in the annual leafless period (Kushwaha and Singh 2005).

4 180 Fraction of species showing leaf flushing (bud break) induced by various triggering factors differs considerably among tropical deciduous forests (Figure 1). This suggests that response of tree community to impending climatic change (i.e. precipitation, temperature) will vary greatly among these forests. Role of several triggering factors in bud break has also been indicated in Australian seasonal tropics (Bowman and Prior 2005). In West African savanna, leaf-exchanging (evergreen and semi-evergreen) species and deciduous woody species differ in the timing of vegetative bud break (De Bie et al. 1998) which was evident from the varying timing of leaf flush initiation. Out of total deciduous species, 20% least deciduous species initiate leaf flushing in mid dry season, 42% intermediate deciduous species initiates flushing in late dry season, and remaining 38% long deciduous species flush their leaves during early rainy season. This indicates the role various factors in triggering the vegetative bud breaks in deciduous species in this region. % Species Fig.1 Fraction of tree species showing bud break of vegetative buds induced by leaf fall of old leaves, increasing day length and/or temperature, and first significant rain among tropical deciduous forests. Data source; Elliott et al., (2006). Like leaf flush, leaf fall timing also varies among tropical trees. Species with longer deciduousness (>4-mo-deciduous and stem succulents, Figure 2) show leaf fall just after the cessation of rains in the early dry season of the annual cycle. However, leaf-exchanging and short deciduous species exhibit leaf falls in mid dry season. While in leaf-exchanging species old leaves are replaced with the new, deciduous species remain leafless till late dry or early rainy season. Given that leaf senescence is an evolutionarily acquired process (Lim et al. 2007), variation in timing and pattern of leaf fall among phenological functional types may be result of their adaptations

5 181 to microhabitats varying in soil moisture levels. India >4-mo-deciduous 2-4-mo-deciduous Leaf fall <2-mo-deciduous Leaf flushing Mature leaf Semi-evergreen A M J J A S O N D J F M A M J Functional type Leaf flushing Mature leaf Leaf-exchanging Leaf fall Brevideciduous Deciduous Costa Rica Stem succulent Fig. 2 Approximate duration of various vegetative phenological events in four major phenological functional types recognized in India and Costa Rica. Data source: Kushwaha and Singh (2005) for India; Rivera et al., (2002) for Costa Rica. Duration of deciduousness The tree deciduousness traits have been in existence for at least 100 million years and may have evolved at generally lower latitudes as an adaptation to seasonal drought under climatic conditions present during the early Cretaceous (or Jurassic) period (Axelrod 1966, Bowman and Prior 2005). Evolution of deciduousness trait in tropics is apparent from the contiguous vegetation zones distributed along climatic gradients in America, Africa, and southern Asia where such vegetation-climatic gradients from wet evergreen rain forest to tropical deciduous forest, deciduous woodland, thorn scrub, and tropical desert are seen (Axelrod 1959). In India, for instance, along progressively drier areas there is a rising degree and duration of deciduousness during the dry season and an accompanying decrease in tree height, leaf size, community complexity, and the number of families and genera represented (Table 1). These major plant formations appear to have evolved by gradual adaptation to decreased precipitation, increased seasonal drought, and greater range of temperature variability. This inference is consistent with the evidence provided by Cretaceous and Tertiary fossil floras preserved in regions which are now semiarid to desert in southern

6 182 California, northern Africa, India, south Australia, and central Chile (Axelrod 1966). In these areas the fossil floras suggest that with decreasing rainfall and longer drought period tropical and subtropical evergreen forests were replaced gradually in time by woodland and thorn forest and later by the present day tropical desert vegetation (Axelrod 1950). Stable isotopes study in permineralized wood of Permian polar forests has demonstrated the presence of deciduousness during the late Permian at polar latitudes (Gulbranson et al. 2012). Table 1. Climo-vegetational characteristics of tropical forest in India (Data Source: Singh and Singh 1988). Climate/ characteristics Wet Moist Dry Thorn forest evergreen deciduous deciduous Mean annual temp. ( C) Mean January temp. ( C) Annual rainfall (cm) Annual dry months Vegetation deciduousness Entirely or Predominan- Entirely Entirely nearly absent tly deciduous; deciduous deciduous sub canopy or nearly so evergreen Species richness Extremely Rich Poor Extremely rich poor Canopy height (m) <10 Basal area (m 2 ha -1 ) <5 No. ligneous layer In deciduous trees, leaf fall (indicating the end of growing season) and the subsequent leaf flush (growth resumption) are separated by a discrete but variable duration of leaflessness or deciduousness (indicating the rest period). In seasonally dry tropics plant species are believed to be characterized by tree functional traits like deciduousness (~leaflessness) and adaptation for drought tolerance. In dry tropics, the time lag between the completion of leaf fall and the initiation of leaf flushing (i.e. the duration of deciduousness) is an important attribute of deciduous tree species, showing adaptations related to the seasonal drought. The degree of water stress experienced by dry tropical forest trees differs widely due to their varying adaptations, resulting in marked differences in the duration of deciduousness (from leaf exchanging to >8 months deciduous). Tropical

7 183 deciduous forests are composed of mosaics of tree functional types showing considerable variations with respect to the time of bud break of vegetative bud and duration of deciduousness (Borchert et al. 2002, Singh and Kushwaha 2005a). The impending impact of global climate change (e.g. changes in temperature and precipitation) on the extent of deciduousness and vegetative growth period ranks high among critical questions in the ecology of dry tropics (Do et al. 2005). For instance, knowledge of the deciduousness period of various tree species in relation to the annual cycle is a prerequisite to estimate the annual carbon fluxes. Thus, vegetative (leaf) phenology in dry tropics may be viewed from the broader perspective of a gradient of duration of deciduousness across tree species. The coexistence of four tree functional types including one semi-evergreen and three deciduous ones showing progressive increase in deciduousness has been demonstrated in Indian Vindhyan dry tropical forests (Kushwaha and Singh 2005) (Fig. 2). The trend of increasing deciduousness is also clearly evident in the four major leaf functional types recognized in Costa Rica. Singh and Kushwaha (2005a) have verified the ubiquitousness of deciduousness based tree functional types with a large species data-set and found that majority of tree species are <2-mo-deciduous (47%), 2-4- mo-deciduous (18%), >4-mo-deciduous (13%) and remaining are leafexchanging (21%). In deciduous forests of Costa Rica and Thailand 41% and 5% species show 3-5 months deciduousness and 34% and 42% species represent 1-3 months deciduousness, respectively (Elliott et al. 2006). Tropical tree species represent a gradient of deciduousness ranging from leaf-exchanging to >6 month deciduous species. Categorization of Indian tropical forests as moist evergreen, semi-evergreen, moist deciduous, dry deciduous and thorn forests based on annual canopy fullness and deciduousness (Champion and Seth 1968) can be regarded as marker of the amount and distribution of annual rainfall and seasonal variation in soil moisture availability. Proportion of deciduous species and the extent of deciduousness - both increasing with greater severity of annual drought significantly affect structure and functioning in these forests. In majority of species marked intra-specific asynchrony occurs in terms of deciduousness. Calculation of the duration of deciduousness in West African savanna trees from the data of De Bie et al. (1998, Appendix 1), indicating the periods in leaf and without leaf for different species at five sites, all located within the annual rainfall range mm, show large variation in deciduousness duration of the same species growing at different sites (Table 2). Individuals of same species growing at different sites differed radically from being leaf exchanging to 8 months deciduous

8 184 (e.g. Acacia seyal and Combretum nigricans, Table 2), reflecting high sensitivity to small changes in growing habits. Under current tropical climatic conditions large inter-annual variations in the length of growing and deciduousness periods are noticed in the tropical trees (Yoshifuji et al. 2006). Even conspecific individuals of dominant species growing at the same site often differ with respect to growing and deciduousness periods in response to micro-site variations (Singh and Kushwaha 2005b). In dry environments, heterogeneity and periodicity of water availability have been demonstrated as being crucial factors in phenological rhythms of tree communities and populations (Seghieri and Galle 1999). Borchert (1994) showed that in dry forests intra-species variation in phenology is guided by differences in soil water availability. Thus, wide conspecific variation in the extent of deciduousness, resulting from varying leaf flush and leaf fall timings, seems to be an essential functional attribute that leads to broader ecological amplitude of tree species by adaptation to varying microconditions. Table 2. Deciduousness variation in tropical tree species growing at five different sites in West Africa having long term average rainfall mm; The representative data presented in this table has been deduced from the Appendix 1 of De Bie et al. 1998). Species Range of deciduousness (mo) at different sites* Y B S T BB Period Variation Piliostigma reticulatum Feb 1 Diospyros mespiliformis Mar-Apr 2 Maytenus senegalensis Apr-May 2 Adansonia digitata Oct- Apr 3 Prosopis Africana Nov-Apr 4 Combretum glutinosum Nov-Mar 4 Sterculia setigera Oct-May 4 Ziziphus mauritiana Jan-May 5 Piliostigma thonningii Dec-Apr 5 Daniellia oliveri Oct-Mar 6 Combretum micranthum Oct-May 6 Combretum nigricans Sep-May 7 Parkia biglobosa Sep-Apr 7 Acacia seyal Oct-May 8 Pterocarpus lucens Oct-Jun 8 *Y (Yabo), B (Bissiga), S (Sourou), T (Tisse) are located in Forest Reserves at Burkina Faso and BB (Boucle du Baoule) is located in Biosphere Reserve at Mali.

9 185 In tropical trees estimates related to leaf functions have been generally generated in fully expanded leaf condition, during the growth promoting period (period of maximal carbon assimilation) (Prior et al. 2004). Such approximations may not act as representative of the annual values. All deciduous species (leafless from <1 month to >7 months, inter-annual and conspecific variations) show an absolute decline in assimilation rate during the deciduousness period and rely on reserves to support their activities. Deciduousness as an indicator of climate change It is important to search and identify unambiguous indicators of the impact of global climate change at a regional or local level (Donnelly et al. 2004). Ecological indicators provide information about the phenomena that are regarded as typical for, and/or critical to, environmental quality and they are used to simplify a complex reality (Smeets and Weterings 1999). Currently, the phenological observations of tree developmental stages have proved to be most effective impact indicators of climate change (Donnelly et al. 2004). The criteria established by the OECD (1993) for indicator selection are listed in Table 3, which emphasize on relevance and utility for users, analytical soundness, and measurability of the ecological indicator. Identifying a set of indicators which fulfill all of these criteria is a challenging task. Due to the complex and uncertain nature of climate change effects it is difficult to establish appropriate indicators of climate change impact on the environment. Table 3. OECD (1993) criteria for indicator selection and suitability of tree deciduousness as an ecological indicator for climate change in dry tropics. S.N. OECD criteria for indicator selection Suitability of deciduousness 1. Policy, relevance and utility for users A climate change indicator should: Provide representative picture of Deciduousness in tropical trees is best climatic conditions indicator of drought experienced Be simple, show trends over time and be easily interpreted Be representative to change and relate to human activity Be comparable internationally Be national in scope or applicable to regional climatic issue Deciduousness can be depicted from naked eye, it is very sensitive to small variation in the climate Documentation of deciduousness in tree functional types over the period will represent the changes Quantitative documentation will serve the purpose Under different climatic conditions, its extent will indicate the prevailing climatic conditions

10 186 Have a reference value against which comparisons 2. Analytical soundness A climate change indicator should: Be theoretically well founded in technical and scientific terms Be based on international standards Lend itself to being linked to economic models, forecasting and information system Values can be compared from the current extent of can be made so that users are able to assess the deciduousness in different tree functional types significance of the values associated with it Term deciduousness well situated for this criteria Quantitative documentation will be expected by Global scientific community Its role in C sequestration, as a drought and soil moisture condition indicator make it important 3. Measurability The data required to support the indicator should: Be readily available at a reasonable cost/benefit ratio Documentation of deciduousness involves minimum cost but provides immense significance Be of high quality and well documented The best indicator of tree rest period and can be deduced from growth period Be updated regularly in accordance with reliable Once quantification made, it can be periodically updated procedures In tropical trees the trait of deciduousness may act as a reliable indicator of climate change because it reflects an integrated effect of seasonal drought, tree characteristics and soil moisture conditions. Deciduousness is linked with rainfall, temperature and solar radiation and may be serve as an indicator of the response of vegetation to climate change (Bohlman 2010). Quantitative estimates of deciduousness may provide a means for predicting species ranges as well as other forest characteristics. Several models have depicted the possible response of tropical forests to future climatic changes (Steffen et al. 1996). Such models may have to be adjusted by assessing how well they predict deciduous behavior under different climates (Condit et al. 2000). Since deciduousness can be easily recorded from a satellite, it may become a key parameter for the analysis of the effect of climate change on tropical forests. Accurate quantitative documentation of deciduousness in tropical forests is essential for calibrating remote sensing images which attempt to assess canopy properties such as carbon cycling, productivity, or chlorophyll content (Condit et al. 2000). Recent advances in remote sensing have showed the potential to generate valuable ecological information such as leaf level drought

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