Lianas and trees in tropical forests in south China

Lianas (woody climbers) and trees are the most important life-forms in most tropical forests. In many of these forests lianas are abundant and diverse and their presence is often a key physiognomic feature. Lianas contribute substantially to the floristic, structural and functional diversity of tropical forests, and have both positive (providing valuable food resources, habitat, and connections among tree canopies that are used as pathways by arboreal animals) and negative (reducing tree growth, fecundity and survivorship) effects on forests.<o:p></o:p></span>Lianas are increasingly well studied in many areas around the world, but in southeast Asia they are relatively unknown. This PhD dissertation describes liana communities in selected but well distributed tropical forests in Xhishuangbanna, southwest China. In addition the question what makes lianas functionally different from trees is addressed. A number of structural-functional characteristics of lianas are analysed, comparative to trees. Special attention is put to growth performance and ecophysiological leaf and plant characters in a framework of adaptive ecology. The last part of the dissertation addresses adaptive behavior, both within one liana species as across a number of species differing in adult stature.<o:p></o:p></span><p class=MsoBodyText style='line-height:14.0pt;mso-line-height-rule:exactly; layout-grid-mode:char'><strong><span lang=EN-US style='font-size:10.0pt; color:windowtext'>Liana communities in different forests</span></strong><span lang=EN-US style='font-size:10.0pt;color:windowtext;mso-no-proof:no'><o:p></o:p></span>The liana communities of three common forest types are analysed: seasonally wet. montane forest and evergreen broad-leaved forest. In each forest five 0.1 ha (20 x 50 m) plots were established. The density of lianas varied significantly among the three forests, with on average 445, 276 and 301 individuals per plot in the seasonally wet, montane, and evergreen forests,respectively. All three forests combined consisted of a total of 147 liana species, representing 48 families and 75 genera. A plot had on average 40, 26, and 21 species in the seasonally wet, montane, and evergreen forest, respectively. The forests were rather different as similarity between their liana assemblages was low. In all three forests, most lianas were stem twiners and scramblers, with relatively few hook, tendril and root climbers. Liana species were mostly wind dispersed in the evergreen forest, but animal and gravity dispersed in the other two forests.<o:p></o:p></span>The higher liana abundance in the seasonal forest is consistent with the documented pattern that lianas peak in abundance with increasing seasonality. Compared to other tropical Asian tropical forests, the diversity and abundance of lianas is relatively high in Xishuangbanna, which may be due to the relatively warm climate, as well as its high seasonal rainfall and its high rates of disturbance and forest fragmentation.<o:p></o:p></span><p class=MsoNormal style='line-height:14.0pt;mso-line-height-rule:exactly; mso-layout-grid-align:none;text-autospace:none'><strong><span lang=EN-US style='font-size:10.0pt'>How different are lianas from trees?<o:p></o:p></span></strong>In two studies a large number of liana and tree species were compared for selected leaf structural and physiological characteritics. Chapter 3 focusses on differences in adaptation to climate seasonality. Most organisms decrease in abundance with decreasing annual precipitation and increasing seasonality. However, lianas are an exception to this general rule: they increase in abundance with increasing seasonality (Schnitzer 2005). In this chapter the hypothesis is tested that lianas are physiologically more robust than trees during the dry season, thus contributing to an explanation of their relatively high abundance in seasonal forests. We compared a range of leaf-level physiological attributes of 18 co-occurring liana and 16 tree species during the wet and dry seasons in a tropical seasonal rainforest in Xishuangbanna. During the wet season, lianas (liana leaves) had significantly higher nitrogen concentrations ( N_mass ), δ<st1:chmetcnv TCSC="0" NumberType="1" Negative="False" HasSpace="False" SourceValue="13" UnitName="C" w:st="on">¹³ C</st1:chmetcnv>values, and lower leaf mass per area (LMA) than trees, indicating that lianas have higher water-use efficiency (WUE) and lower structural investments. However, liana and tree species did not differ significantly in photosynthesis ( A_area ), dark respiration (R d_area ), chlorophyll content (Chl _mass ), carotenoid to chlorophyll ratio (Car/Chl), phosphorus concentration ( P_mass ), N:P ratios, and photosynthetic nitrogen- and phosphorus- use effeciency (PNUE, PPUE). During the dry season, the decrease in A_area and N_mass was far lower in lianas than in trees, suggesting that lianas fix more carbon and suffer less from water stress during this season. From the wet to the dry season, average A_area decreased by 30.1% in tree species, compared with only 12.8 % in liana species. N_mass , P_mass and PNUE changed little for lianas, while these factors decreased strongly for tree species. The δ<st1:chmetcnv TCSC="0" NumberType="1" Negative="False" HasSpace="False" SourceValue="13" UnitName="C" w:st="on">¹³ C</st1:chmetcnv>, LMA and Car/Chl values for both lianas and trees did not vary significantly with the season.<o:p></o:p></span>These results show that lianas are less negatively effected by a dry season than trees, providing eco-physiological evidences as to why lianas are abundant in the seasonally rainforest. The leaf-level physiological characteristics show that lianas tend to fix more carbon, have a higher resource capture efficiency (water and nitrogen) in the dry season, and have lower cost of resource capture, compared to trees, thus confirming the hypothesis that differences in photosynthetic attributes may contribute to the competitive advantage of lianas over trees in seasonal forests.<o:p></o:p></span>Chapter 4 addresses the question whether lianas are more efficient than trees in nutrient resorption during leaf senescence. This would give an additional advantage in nutrient poor environments as many tropical forests are. The chapter presents changes in leaf size, leaf mass and foliar nutrient concentrations during leaf senescence in 12 liana and 14 tree species in a tropical strongly phosporus-limited montane rain forest in Xishuangbanna. The relative leaf shrinkage and mass loss during senescence did not differ significantly between lianas and trees. Nutrient concentrations in mature leaves and nitrogen resorption efficiency of liana species were similar to those of tree species, but the phosphorus concentrations of liana litter were higher, and liana's phosphorus resorption efficiencies were lower. These results therefore provide clear evidence in favour of a novel mechanism whereby lianas may influence the ecosystems in which they occur. Through the production of nutrient-rich litter, they have the potential to greatly enhance the availability of nutrients in areas where they are abundant, and thus they may have significant effects on small-scale biodiversity.<o:p></o:p></span>Another important difference between lianas and trees is the larger growth rate of lianas, as has been often postulated. To examine this hypothesis more closely, a range of physiological, morphological, and biomass parameters at the leaf and whole plant level were compared in seedlingsof five Bauhinia species of different life form and light demand: two light-demanding lianas, one shade-tolerant liana, and two light-demanding trees. Seedlings of these five species were grown in a shadehouse with 25% of full sunlight. Compared to trees, the two light-demanding lianas had lower photosynthetic rates per unit area (A_area ) and similar photosynthetic rates per unit mass (A_mass ). High specific leaf area (SLA</st1:place>) and leaf mass fraction (leaf mass/plant mass, LMF) in the two light-demanding lianas were reflected in a higher leaf area ratio (LAR). The two light-demanding liana species had higher relative growth rate (RGR), allocated more biomass to leaf production (higher LMF and LAR) and stem mass fraction (SMF), and less biomass to the roots (root mass fraction, RMF) than the two tree species. The shade-tolerant liana had the lowest RGR of all five species, and had a higher RMF, lower SMF, and similar LMF than the two light-demanding liana species. Across species, RGR was positively related to<st1:place w:st="on">SLA</st1:place>, but not to LAR and Aarea. The faster growth of light-demanding lianas compared to light-demanding trees is based on morphological parameters (SLA, LMF, and LAR), and cannot be attributed to higher photosynthetic rates at the leaf level. The shade-tolerant liana exhibited a different growth strategy from the light-demanding species. Our study shows that, even within a genus (in this case Bauhinia), plant growth is rather variable, and that this variation is related to life form (lianas vs trees) and to light demand (light-demanding vs shade tolerant).<o:p></o:p></span><p class=MsoBodyText style='line-height:14.0pt;mso-line-height-rule:exactly'><strong><span lang=EN-US style='font-size:10.0pt;color:windowtext'>Seasonal acclimation of a liana<o:p></o:p></span></strong>Under natural conditions, photosynthesis is biochemically regulated to maintain a balance between the rates of its component processes and the concentrations of metabolites, and is affected by continuously changing environmental variables, such as light, water availability, and temperature. Xishuangbanna, biogeographically located in the transitional zone between tropical Southeast Asia and subtropical East Asia, has a rich tropical flora and typical tropical rain forests in the lowland area. It has been hypothesized that the vegetation there is likely to be affected by the seasonal drought and chilling because it is far from the Equator and at a relatively high altitude. To test this hypothesis, Chapter 6 addresses the photosynthetic adaptation and growth responses in seedlings of a local liana species (Zizyphus attopensis Pierre) in three contrasting natural microhabitats: understory, a small gap and a large gap. Photosynthetic capacity(light-saturated photosynthetic rate, A_max ), maximum rate of carboxylation (Vcmax</sub> ) and electron transport ( J_max ), and partitioning of leaf nitrogen into carboxylation ( P_c ) and electron light transport ( P_b ) differed significantly between seasons and microhabitats. Specific leaf area (SLA) did not change seasonally, but was different between plants grown in each of the three microhabitats and was negatively linear related to the daily integrated photon flux density (PPFD _i ). In contrast, nitrogen content per unit area (N_a ) changed seasonally but did not differ among microhabitats. Measurements of maximum photosystem II (PSII) photochemical efficiency showed that no chronic photoinhibition occurred for all microhabitats throughout the experimental period. Photosynthetic capacity was greatest in the wet season and lowest in the cool season. During the cool and dry seasons, the reduction in A_max was greater in seedlings grown in the large gap than in those grown in understory and small gap. Close logarithmic relationships were detected between PPFD, leaf N_a and photosynthetic capacity. Stem mass ratio decreased and root mass ratio increased in the dry season. These results show that seasonal acclimation in growth and photosynthesis of the seedlings was due to changes in biochemical features (particularly N_a and partitioning of total leaf nitrogen between the different photosynthetic pools) and biomass allocation, rather than to changes in leaf morphological features (such as<st1:place w:st="on">SLA</st1:place>). The local light level is the main factor driving seasonal variations in growth and photosynthesis in the study area due to the presence of heavy fog during the cool and dry seasons which reduces irradiance and supplies water to the soil surface layers.<o:p></o:p></span><p class=MsoNormal style='line-height:14.0pt;mso-line-height-rule:exactly; mso-layout-grid-align:none;text-autospace:none'><strong><span lang=EN-US style='font-size:10.0pt'>Light acclimation, adult stature and shade tolerance<o:p></o:p></span></strong>Finally, Chapter 7 addresses light acclimation of seedlings of six late-successional common woody species differing in adult stature and shade tolerance. Especially morphological and physiological leaf and whole-plant features are analysed. After 1 year of growth in low light (4.5% full sun), seedlings were transferred to high light (24.5% full sun) to investigate acclimation responses of existing leaves to forest gap opening and to determine whether seedling capacity for acclimation is a limiting factor in its natural regeneration. Leaves of the small shrub species are shade-adapted, as indicated by their low photosynthetic capacity, efficiency in using sunflecks, low stomatal density, low Chl a/b ratio and high spongy/palisade mesophyll ratio. The shrub species utilized sunflecks efficiently because of a short photosynthetic induction time and low induction loss. In all species, transfer of seedlings to high light resulted in a substantial initial reduction in the dark-adapted quantum yield of photosystem II ( F_v / F_m ) at<st1:time Hour="12" Minute="0" w:st="on">midday</st1:time>. Predawn F_v / F_m of the taller species did not change greatly, but predawn F_v / F_m of the short species (shrubs) decreased significantly without complete recovery within 25 days of transfer to high light, indicating chronic photoinhibition and damage to the previously shade-adapted leaves. Maximum net photosynthetic rate and dark respiration of the four taller species increased considerably after transfer to high light, but not in the shrub species. Similar trends were observed for the number of newly formed leaves and relative height growth rate. We conclude that the short species have limited potential for developmental and physiological acclimation to high light, which explains their absence from forest gaps. Compared with shrub species, the taller tree species, which are more likely to experience high light during their life span, showed a greater potential for light acclimation. Physiological differences among the four tree species were not consistent with differences in adult stature.<o:p></o:p></span><p class=MsoNormal style='line-height:14.0pt;mso-line-height-rule:exactly; mso-layout-grid-align:none;text-autospace:none'><strong><span lang=EN-US style='font-size:10.0pt;font-family:AGaramond-Regular;mso-bidi-font-family: AGaramond-Regular;mso-font-kerning:0pt'>Lianas versus trees: are differences adaptive?<o:p></o:p></span></strong>Phenotypic changes that we see over evolutionary time, across diverse environments and among taxa, often reflect adaptive evolution. In the broad sense adaptations are phenotypic traits that have been favored by natural selection, and can be identified by being variable, heritable and responsible for variation in fitness. The evolution of growth forms since the early terrestrial radiations is a complex history of innovation, complexification, simplification, conservatism, radiation and extinction (Rowe and Speck 2003, 2005). Trees and lianas have different ecological preferences and different attributes, but we are far from being able to link this directly to evolutionary differences. In more general terms we are confronted with questions like: are certain types of growth form highly constrained and immovable in evolutionary terms? Are some plant groups more 'flexible' in their capacity to evolve widely differing growth forms and is this capacity related to the evolutionary age or complexity of the group? What are the ecological factors that coerce to either canalise or facilitate growth form variation and evolution? Much more work is needed to be able to answer these questions. It is clear that lianas have growth strategies different from trees, as shown for some aspects in this thesis, but lianas do not always follow expected patterns. Additionally, for some characteristics lianas are far less different from trees than expected, as has been showed by a number of recent studies (Gilbert et al. 2006, Santiago and Wright 2007, Selaya 2007, this thesis). These new results shed new light on patterns of adaptive ecology of lianas versus trees in tropical forests. Together, these results force us to re-evaluate the broad generalizations that we sometimes use. This warrants further studies on the ecological differences between lianas and trees, including variations therein among forest types in different climates