Detecting invisible growth rings of trees in seasonally dry forests in Thailand: isotopic and wood anatomical approaches

We measured radial variation of carbon isotope composition and vessel traits in tree species in seasonally dry forests of Northeast Thailand to explore a more reliable and amenable method of tropical dendrochronology for trees that lack visually detectable and consistent growth rings. Six Dipterocarpaceae species (3 Shorea, 2 Dipterocarpus, and 1 Hopea species) with indistinct or irregular growth rings and teak (Tectona grandis), a species which forms distinct growth rings, were examined. The δ¹³C value variations in all species showed annual cyclicity. Dipterocarpaceae species usually marked the lowest values of δ¹³C in the middle of the growing season, whereas teak had the lowest values at nearly the end of the growing season. Since the growing season of the species examined almost corresponds to the rainy season in the study area, the δ¹³C variation was likely caused by the change in moisture availability. The different variation pattern of teak was attributable to its stronger dependence on ¹³C-enriched reserved material early in the growing season. Changes in tree vessel traits for all species examined also showed annual cyclicity. Dipterocarpaceae species showed significant correlation between δ¹³C values and vessel measurements. Vessel lumen (mean area, tangential and radial diameter, and proportion of total area) had a negative correlation, whereas vessel frequency showed a positive correlation. The correlations indicated that changes in vessel traits were caused by the seasonal variation of moisture available to the trees. Thus, we concluded that methods using wood anatomy, as well as δ¹³C, have great potential for use as tools in tropical dendrochronology within the context of seasonal climate.     

A comparison of foliar nutrient concentration in trees from monsoon rainforest and savanna in northern Australia

Abstract Analysis of foliar nutrient concentrations revealed that two mesophyllic monsoon rainforest trees had higher concentrations of most nutrients in leaves than eight savanna species. One of the tested monsoon rainforest species with sclerophyllous leaves had similar nutrient concentrations to the savanna tree species. There were positive or no significant correlations between live foliar nutrient concentration and the percentage of nutrients withdrawn prior to litterfall. The nutrient concentration of litter was similar for most nutrients among tree species of monsoon rainforest or savanna. The results of this study suggest that the relative fertility of surface soils of monsoon rainforest compared with savanna is not determined by contrasting nutrient cycling strategies whereby monsoon rainforest tree species enrich their soils with relatively nutrient rich leaf litter relative to savanna tree species.     

Holocene boundary dynamics of a northern Australian monsoon rainforest patch inferred from isotopic analysis of carbon, (14C and δ13C) and nitrogen (δ15N) in soil organic matter

Abstract Soil organic matter (SOM) was sampled from lateritic soil profiles across an abrupt eucalypt savanna–monsoon rainforest boundary on the north coast of Croker Island, northern Australia. Accelerator mass spectrometry dating revealed that SOM that had accumulated at the base of these 1.5 m profiles had a radiocarbon age of about 5000 years. The mean carbon and nitrogen stable isotope composition of SOM from 10 cm deep layers from the surface, middle and base of three monsoon rainforest soil profiles was significantly different from the means for these layers in three adjacent savanna soil profiles, suggesting the isotopic ‘footprint’ of the vegetation boundary has been stable since the mid Holocene. Although there were no obvious environmental discontinuities associated with the boundary, the monsoon rainforest was found to occur on significantly more clay rich soils than the surrounding savanna. Tiny fragments of monsoon rainforest and abandoned ‘nests’ (large earthen mounds) of the orange‐footed scrubfowl, an obligate monsoon rainforest species, occurred in the savanna, signalling that the rainforest was once more extensive. Despite episodic disturbances, such as tropical storm damage and fires, the stability of the boundary is probably maintained because clay rich soils enable monsoon rainforest tree species to grow rapidly and achieve canopy closure, thereby excluding grass and reducing the risk of fire. Conversely, slower tree growth rates, grass competition and fire on the savanna soils would impede the expansion of the rainforest although high rainfall periods with shorter dry seasons may enable rainforest trees to grow sufficiently quickly to colonize the savanna successfully.     

Relative roles of termites and saprotrophic microbes as drivers of wood decay: A wood block test

Deadwood in tropical ecosystems represents an important but poorly studied carbon (C) pool. Biologically mediated decay of this pool occurs by both saprotrophic microbes and macro‐invertebrates, such as termites. The activity of these decay agents is influenced by abiotic conditions, especially water availability in tropical systems. While saprotrophic microbial activity is directly controlled by moisture, termites employ various morphological and behavioural modifications that should allow for continued activity in dry conditions. We therefore hypothesized that the relative role of termites would be enhanced in the dry season and a dry compared to a wet site. We deployed a novel wood bait (Pinus radiata) at two sites (rainforest and savanna), with or without access holes cut into termite‐excluding mesh. Mass loss from wood baits was measured after a dry season and after a full dry/wet annual cycle. Mass loss was higher at the rainforest site, demonstrating the overall role of moisture in driving wood decay. Counter to expectations, we found no evidence that the relative role of termites was higher at the dry site, nor during the dry season. However, the prevalence of termites was higher in the savanna compared to the rainforest. While termites clearly impact wood decay, these findings indicate that the relative importance of termites in the fate of deadwood may not reflect their mere presence within and across ecosystems. If moisture availability shifts under climate change, our results suggest similar functional responses between termites and saprotrophic microbes in driving C loss from deadwood.     

Wie wachsen Tropenbäume? Jahrringe als Ausdruck von Klimabedingungen und Lebensform

Growth of tropical trees is largely depending on the seasonality of the local climate. In many trees growing in areas with a distinct dry season, cambial activity ceases resulting in the formation of annual rings. In very humid mountain rainforests, trees stop to grow already after short rainless periods. By a combination of increment measurements and wood anatomical analyses, the climatic control of wood formation can be assessed. Intra‐annual wood density variations and content of various stable isotopes enable the climatological interpretation of the “wood signals”.     

Comparative Studies on Woods of Three Species of Normal and Dwarf Trees

Wood structure of three species i.e. Larix chinensis Beissn., Alnus sibirica Fisch. and Quercus mongolica Fisch. of normal and dwarf trees were comparatively studied. The age variation of width of annual rings and size of tracheary elements in these trees follows their own regularities respectively during the course of ontogenesis. In normal, as trees grow, the width of annual rings increases gradually, reaches maximum, then declines in subsequence; while the size of tracheary elements exhibits a crescendo increment, and remains constant after reaching maximum. These trends were not affected by the change of enviromental conditions in which the trees grow. However, the width of annual rings and size of tracheary elements of dwarf trees which grow in adverse circumstances are respectively narrower and smaller than those of normal trees. Further, in dwarf tree of L. chinensis (coniferous wood); the diameter of bordered pits on tracheids of early wood decreases, ray height is lower and ray frequence is higher. In dwarf tree of A. sibirica (diffuse porous wood), vessel frequence increases and the number of bars per perforation decreases. The quatitative features of wood structure of dwarf trees, as compared with those of normal trees, showed more variations; whereas, their own qualitative features of wood structure remain constant. These findings might indicate that modifications of wood structure responsing directly to change of enviromental conditions are usually only qualitative.     

三种正常与矮化植物的木材比较观察

本文比较观察了三种不同木材类型的正常与矮化树木的木材结构:针叶材的太白红杉(Larix chinensis Beissn.)、散孔材的辽东桤木(Alnus sibirica Fisch.)和环孔材的蒙古栎(Quercus mongolica Fisch.)。这些植物在个体发育过程中,各年的年轮宽度及管状分子长度、宽度等变化,存在各自的规律性。这些规律并不因生长环境的差异而变更。不过,逆境下生长的矮化植株的年轮宽度和管状分子的大小明显地比正常的要窄小,同时在木材结构的其它数量性状上,也有较大变化;然而,其各自的种属定性特征仍保持稳定。这些似乎可说明:生态环境的变化对木材结构的数量性状有较大影响,但是对木材种属的定性特征则无明显作用。     

The use of X-ray densitometry to evaluate the wood density profile of Tectona grandis trees growing in fast-growth plantations

Tectona grandis (teak) is an important commercial tree species that is widely used in tropical dendrochronology due to the formation of climate-sensitive annual growth rings. However, young trees growing in plantation conditions exhibit poor ring visibility during the first years of growth, limiting the dendrochronology application. In the present study, we use x-ray densitometry to determine the wood density profile between and within annual rings and at the sapwood-heartwood boundary in trees from fast-growth plantations. The resulting wood density profiles (WDP) can be categorized as uniform, stable growth, unstable growth, and false. The annual ring boundaries were indistinct in trees less than 8 years old. In mature trees, the annual ring boundaries are more defined. In relation to the sapwood-heartwood boundary, the WDP showed a decrease in the wood density; however, this decrease is influenced by the annual ring boundary when the two boundaries coincide. The identification of annual rings in trees growing in fast-growth plantations should be combined with X-ray densitometry and visual identification if wood density data are necessary for deriving other analysis, as climate change, from annual ring.     

Identification of anatomically non-distinct annual rings in tropical trees using stable isotopes

Annual rings are generally not anatomically distinct in trees growing in the humid tropics. The possibility to use radial variation in stable isotopes (δ¹⁸O and δ¹³C) for the identification of annual rings in these trees was investigated in two species growing in the tropical rainforest of Central Guyana, Carapa guianensis and Goupia glabra. The climate is characterised by an annual precipitation of 2,700 mm that is distributed over two rainy and two dry seasons. Cores were taken from trees of measured diameter increment rates. High-resolution tangential sections in radial direction were dissected from these cores and isotopic ratios were measured on whole wood. Variation in δ¹³C was about 1‰ at an annual scale, whereas δ¹⁸O showed two to four times larger annual excursions. The minima in δ¹⁸O were selected as primary indicators of annual boundaries at the main wet season when also δ¹⁸O of precipitation water has its minimum. The minima in δ¹³C coincided often with these. The simultaneous occurrence is consistent with increased discrimination against ¹³C at high water availability. They were used as secondary criteria. Annual rings could thus be identified with reasonable certainty in both species from radial variation in isotopic ratios as verified with measured diameter increment rates. The short sequence covered in the analysis did not show clear correlation with the available precipitation data for the area. The method supplemented with other dating methods may prove to be practically useful for identifying annual rings and applying classical dendrochronology when more cost effective automatic sampling devices become available.     

Evaluation of X-ray densitometry to identify tree-ring boundaries of two deciduous species from semi-arid forests in Brazil

The presence of visible annual rings in semi-arid tropical trees may allow the application of dendrochronological methods. However, variation in water availability may cause the formation of narrow, irregular ill- or non-defined annual rings hindering the correct dating of tree-ring series. We aimed to evaluate X-ray densitometry as a method to identify tree rings of two deciduous tree species from the Caatinga forest, a semi-arid region in the northeast of Brazil, and compare with two other methods commonly used in dendrochronology, the sliding-stage micrometer and image analysis. Xylem was observed macro- and microscopically and wood anatomical features were assessed in Aspidosperma pyrifolium and Poincianella pyramidalis trees. In both species, tree-ring boundaries were identified considering intra-annual density patterns and wood anatomical features. No significant differences in tree-ring widths were found among methods. X-ray densitometry measurements showed a positive correlation with the measurements obtained with image analysis and sliding-stage micrometer in A. pyrifolium and P. pyramidalis, revealing the high reliability of the methods used. However, inter-correlation of tree-ring width series showed differences in the accuracy of crossdating across measuring methods. The maximum, mean and minimum density values were species-dependent, with mean wood density of A. pyrifolium lower than P. pyramidalis. Our results highlight X-ray densitometry as an important and complementary tool to identify tree-rings boundaries in semi-arid tree species, especially in A. pyrifolium. Along with other measuring methods, it may provide higher accuracy in dendrochronological studies in semi-arid or subtropical environments.     

Wood density and its radial variation in six canopy tree species differing in shade-tolerance in western Thailand

Background and Aims

Wood density is a key variable for understanding life history strategies in tropical trees. Differences in wood density and its radial variation were related to the shade-tolerance of six canopy tree species in seasonally dry tropical forest in Thailand. In addition, using tree ring measurements, the influence of tree size, age and annual increment on radial density gradients was analysed.

Methods

Wood density was determined from tree cores using X-ray densitometry. X-ray films were digitized and images were measured, resulting in a continuous density profile for each sample. Mixed models were then developed to analyse differences in average wood density and in radial gradients in density among the six tree species, as well as the effects of tree age, size and annual increment on radial increases in Melia azedarach.

Key Results

Average wood density generally reflected differences in shade-tolerance, varying by nearly a factor of two. Radial gradients occurred in all species, ranging from an increase of (approx. 70%) in the shade-intolerant Melia azedarach to a decrease of approx. 13% in the shade-tolerant Neolitsea obtusifolia, but the slopes of radial gradients were generally unrelated to shade-tolerance. For Melia azedarach, radial increases were most-parsimoniously explained by log-transformed tree age and annual increment rather than by tree size.

Conclusions

The results indicate that average wood density generally reflects differences in shade-tolerance in seasonally dry tropical forests; however, inferences based on wood density alone are potentially misleading for species with complex life histories. In addition, the findings suggest that a ‘whole-tree’ view of life history and biomechanics is important for understanding patterns of radial variation in wood density. Finally, accounting for wood density gradients is likely to improve the accuracy of estimates of stem biomass and carbon in tropical trees.Key words: Radial gradients, shade-tolerance, tree biomass estimates, tree rings, tropical trees, wood density     

Age and Long-term Growth of Trees in an Old-growth Tropical Rain Forest, Based on Analyses of Tree Rings and 14C1

In an old‐growth tropical wet forest at La Selva, Costa Rica, we combined radiocarbon (¹⁴C) dating and tree‐ring analysis to estimate the ages of large trees of canopy and emergent species spanning a broad range of wood densities and growth rates. We collected samples from the trunks of 29 fallen, dead individuals. We found that all eight sampled species formed visible growth rings, which varied considerably in distinctiveness. For five of the six species for which we combined wood anatomical studies with ¹⁴C‐dates (ring ages), the analyses demonstrated that growth rings were of annual formation. The oldest tree we found by direct ring counting was a Hymenolobium mesoamericanum Lima (Papilionaceae) specimen, with an age of ca. 530 years at the time of death. All other sampled individuals, including very large trees of slow‐growing species, had died at ages between 200 and 300 years. These results show that, even in an everwet tropical rain forest, tree growth of many species can be rhythmic, with an annual periodicity. This study thus raises the possibility of extending tree‐ring analyses throughout the tropical forest types lacking a strong dry season or annual flooding. Our findings and similar measurements from other tropical forests indicate that the maximum ages of tropical emergent trees are unlikely to be much greater than 600 years, and that these trees often die earlier from various natural causes.     

论季雨林的水平地带性

季雨林是受制于湿度因子的经度地带性植被类型,它是随着湿度条件的下降由热带雨林向热带疏林过渡的居间类型,而不是受制于温度因子的纬度地带性植被类型,不是随着温度条件的下降由热带雨林向亚热带常绿阔叶林过渡的居间类型。我国南亚热带的榕树群系、黄桐群系,以及热带北缘的青皮群系均不应是季雨林,前二者是典型的南亚热带低地常绿阔叶林或南亚热带雨林,后者则是热带雨林的一分类群。     

Effect of wood density and water permeability on wood decomposition rates of 32 Bornean rainforest trees

Aims A better understanding of wood litter decomposition is essential for predicting responses of forest ecosystems to global climate change. Recent studies suggest that chemical properties of wood litters, rather than physical ones such as wood density, are more important for interspecific differences in wood decomposition rates. However, empirical data are still limited, especially for tropical trees. In addition, decomposition rate of wood litter often varies with time, which makes interspecific comparison difficult. We studied the wood decomposition of 32 rainforest trees to elucidate (i) the degree of interspecific variation in wood decomposition rate of a given size and configuration and (ii) if initial wood density and water permeability are consistent predictors of the overall decomposition rate and its pattern over time.Methods A common garden decomposition experiment was conducted in a tropical rainforest in Malaysian Borneo for 32 native tree species. Small wood sticks were set on the forest floor and the weight loss was monitored monthly for 2.7 years.Important findings We found large variation in the wood decomposition rate (a 49-fold range), suggesting that we need to consider this variation when calculating community-level carbon dynamics of tropical rain forests. The physical traits of wood, i.e. wood density and water permeability, were related to wood decomposition rate and its pattern over time. Decomposition half-time related positively and negatively to initial wood density and water permeability, respectively. The time-dependent-rate model fitted better for 18 species (56% of the study species) that had higher water permeabilities than the others, suggesting that micelle porosity in wood relates to temporal changes in decomposition rate.     

Evaluating the annual nature of juvenile rings in Bolivian tropical rainforest trees

Knowledge on juvenile tree growth is crucial to understand how trees reach the canopy in tropical forests. However, long-term data on juvenile tree growth are usually unavailable. Annual tree rings provide growth information for the entire life of trees and their analysis has become more popular in tropical forest regions over the past decades. Nonetheless, tree ring studies mainly deal with adult rings as the annual character of juvenile rings has been questioned. We evaluated whether juvenile tree rings can be used for three Bolivian rainforest species. First, we characterized the rings of juvenile and adult trees anatomically. We then evaluated the annual nature of tree rings by a combination of three indirect methods: evaluation of synchronous growth patterns in the tree- ring series, ¹⁴C bomb peak dating and correlations with rainfall. Our results indicate that rings of juvenile and adult trees are defined by similar ring-boundary elements. We built juvenile tree-ring chronologies and verified the ring age of several samples using ¹⁴C bomb peak dating. We found that ring width was correlated with rainfall in all species, but in different ways. In all, the chronology, rainfall correlations and ¹⁴C dating suggest that rings in our study species are formed annually.     

Can stable carbon isotopes (δ13C) in soil carbon be used to describe the dynamics of Eucalyptus savanna–rainforest boundaries in the Australian monsoon tropics?

The history of isolated patches of monsoon rainforest within large tracts of Eucalyptus savanna is poorly understood because of the scarcity of reliable palaeoecological records in the Australian monsoon tropics. Elsewhere in the world, the ratio of the stable isotopes ¹³C to ¹²C (δ¹³C) in soil organic matter has shed light on the dynamics of rainforest–savanna boundaries because tropical grasses with the C4 photosynthetic pathway have a distinct δ¹³C signature (–17 to –9‰) compared with that of woody plants with the C3 photosynthetic pathway (–32 to –22‰). In order to determine the magnitude of the variation in δ¹³C, unreplicated soil profiles were sampled beneath different vegetation types on three boundaries between Eucalyptus savanna and rainforest that were both growing on Tertiary age laterite parent material. Replicated (n = 3) soil profiles, which were also derived from Tertiary age laterite, were sampled from beneath: (i) dense stands of African grasses within a frequently burnt Eucalyptus savanna; and within the same long unburnt Eucalyptus savanna, (ii) patches of African and natives grasses and (iii) clumps of Acacia trees. The strongly negative δ¹³C values of soil organic matter derived from the frequently burnt and long unburnt grassy understoreys in the Eucalyptus savannas showed that a considerable amount of the soil carbon was derived from C3 (woody) species despite the presence of a ground layer dominated by C4 grasses. However, a feature of these data was the considerable variability among the three ‘replicate’ profiles. The surface soil samples from beneath three clumps of Acacia trees in the unburnt Eucalyptus savanna had much less variable δ¹³C values and were similar to two of the three monsoon rainforests sampled. The pattern of δ¹³C values from unreplicated soil profiles from different vegetation types across three rainforest boundaries was also very variable and not always obviously related the known disturbance history of the extant vegetation. Given the considerable variability within and between vegetation types with contrasting disturbance histories, it is concluded that the use of carbon stable isotopes to advance understanding of the dynamics of rainforest and Eucalyptus savanna boundaries will require further development, such as determination of the ¹⁴C age and δ¹³C values of different soil carbon fractions.     

Life-span growth dynamics and xylem anatomical patterns of diffuse-porous Afzelia africana Sm. (Fabaceae) in different ecological zones in Burkina Faso

Tropical West African savannas are exposed to high climatic variability with potential impacts on tree growth, forest dynamics and ecosystem productivity. In such context, understanding the long-term ecological responses of savanna trees to changing environmental conditions is of great relevance for taking appropriate conservation actions. We conducted the first study on tree-ring analysis and quantitative wood anatomy on Afzelia africana Sm. in Burkina Faso, to investigate the life-span growth trajectories and wood anatomical adjustment to site and to climate variations. A total of 24 stem discs was collected in four protected forests along the Sudano-sahelian and the Sudanian climatic zones. Wood samples were analyzed using standard dendrochronological methods and quantitative wood anatomy. The mean annual growth rates varied from 1.002 (± 0.249) mm. year⁻¹ in the Sudanian zone to 1.128 (± 0.436) mm. year⁻¹ in the Sudano-sahelian zone. Analysis of growth trajectories showed high variations within sites and between climatic zones. Wood anatomical traits significantly varied between sites. Principal Component Analysis revealed strong relationships between ring width, wood density and vessel traits, with 82.81 % of the total variance explained. Vessel size significantly increased from the pith to the bark, highlighting the ontogenetic effects on xylem anatomical variations. Inverse relationships were found between vessel size and vessel density across the driest site and the wettest site, suggesting that the higher the rainfall, the taller the tree, the larger vessel size, but the lower vessel density. By contrast, more arid conditions and high evapotranspiration lead to smaller vessel sizes and higher vessel density. Such anatomical adjustments highlight the trade-offs between water conductance efficiency and hydraulic safety, and emphasize physiological responses to climate variability. These variations on the long-term dynamics and xylem anatomical patterns underline complex interactions between ontogenetic effects and contrasting environmental factors that affect the eco-physiological functioning of A. africana throughout the Sudanian region.     

西双版纳森林植被研究

西双版纳是世界生物学多样性保护的关键和热点地区,倍受国际学术界的关注。笔者依据30多年来对西双版纳植被的调查,结合植物群落生态学与植物区系地理学研究,并参考世界类似热带植被的研究成果,对西双版纳植被的分类、物种组成、群落生态表现和植物区系特征等作了系统探讨,还进一步分析比较了其与世界类似热带森林植被的关系。结果显示,西双版纳的森林植被共包括32个较为典型的群系,且分属于7个主要的植被型,即热带雨林、热带季节性湿润林、热带季雨林、热带山地(低山)常绿阔叶林、热带棕榈林、暖热性针叶林和竹林。本文对西双版纳植被进行的全面记录和系统归纳,可为科学研究、生物多样性保护和自然保护区的管理提供参考。     

Drought impact on water use efficiency and intra‐annual density fluctuations in Erica arborea on Elba (Italy)

Erica arborea (L) is a widespread Mediterranean species, able to cope with water stress and colonize semiarid environments. The eco‐physiological plasticity of this species was evaluated by studying plants growing at two sites with different soil moistures on the island of Elba (Italy), through dendrochronological, wood‐anatomical analyses and stable isotopes measurements. Intra‐annual density fluctuations (IADFs) were abundant in tree rings, and were identified as the key parameter to understand site‐specific plant responses to water stress. Our findings showed that the formation of IADFs is mainly related to the high temperature, precipitation patterns and probably to soil water availability, which differs at the selected study sites. The recorded increase in the ¹³C‐derived intrinsic water use efficiency at the IADFs level was linked to reduced water loss rather than to increasing C assimilation. The variation in vessel size and the different absolute values of δ¹⁸O among trees growing at the two study sites underlined possible differences in stomatal control of water loss and possible differences in sources of water uptake. This approach not only helped monitor seasonal environmental differences through tree‐ring width, but also added valuable information on E. arborea responses to drought and their ecological implications for Mediterranean vegetation dynamics.     

Climate and land-use interactively shape butterfly diversity in tropical rainforest and savanna ecosystems of southwestern China

Human-induced habitat conversion and degradation, along with accelerating climatic change, have resulted in considerable global biodiversity loss. Nevertheless, how local ecological assemblages respond to the interplay between climate and land-use change remains poorly understood. Here, we examined the effects of climate and land-use interactions on butterfly diversity in different ecosystems of southwestern China. Specifically, we investigated variation in the alpha and beta diversities of butterflies in different landscapes along human-modified and climate gradients. We found that increasing land-use intensity not only caused a dramatic decrease in butterfly alpha diversity but also significantly simplified butterfly species composition in tropical rainforest and savanna ecosystems. These findings suggest that habitat modification by agricultural activities increases the importance of deterministic processes and leads to biotic homogenization. The land-use intensity model best explained species richness variation in the tropical rainforest, whereas the climate and land-use intensity interaction model best explained species richness variation in the savanna. These results indicate that climate modulates the effects of land-use intensity on butterfly alpha diversity in the savanna ecosystem. We also found that the response of species composition to climate varied between sites: specifically, species composition was strongly correlated with climatic distance in the tropical rainforest but not in the savanna. Taken together, our long-term butterfly monitoring data reveal that interactions between human-modified habitat change and climate change have shaped butterfly diversity in tropical rainforest and savanna. These findings also have important implications for biodiversity conservation under the current era of rapid human-induced habitat loss and climate change.