Explaining Leaf Herbivory Rates on Tree Seedlings in a Malaysian Rain Forest

Seedlings of five species of dipterocarp trees were planted in experimental plots in rain forest gaps in Sabah, Malaysia, and the rates of herbivory on their mature leaves recorded over 6 mo. A novel method was used to estimate the feeding pressure exerted by the local insect herbivore community, derived from the relative abundances of the dominant generalist herbivores and their feeding preferences. Characteristics of the leaves related to their defense and nutritional value were measured—phenolic content, laminar fracture toughness, laminar thickness, and nitrogen content. Three main groups of herbivorous insects were present—coleopteran and lepidopteran herbivores, which were sampled by hand from the seedlings, and orthopteran herbivores, which were sampled by sweep netting. The feeding preferences of the main coleopteran and orthopteran herbivores were determined using laboratory feeding trials. Combining variables in a Principal Components Analysis, a clear separation was found between the five seedling species along the first extracted component. This correlated closely with herbivory rates between species. The first extracted component comprised a negative influence of phenolic content and positive effects of nitrogen content, laminar fracture toughness, abundances of coleopteran and lepidopteran herbivores, and estimated feeding pressure of the coleopteran community. Further studies are required to determine the potential applications of the latter measure of estimated herbivore community impact.     

Land management affects grass biomass in the Eucalyptus tetrodonta savannas of monsoonal Australia

Abstract We surveyed herbaceous biomass across the range of Eucalyptus tetrodonta savannas in north‐western Australia. Sample sites (n = 211) were stratified within four broad geographical regions characterized by different mixes of land management regimes. Grasses dominated (87% mean) the herbaceous biomass. After controlling for climatic and edaphic gradients, herbaceous biomass was highest in the Greater Darwin region (2.2 t ha⁻¹) which is managed predominantly by Europeans, and least under semi‐traditional Aboriginal management in Arnhem Land region (1.1 t ha⁻¹). In the drier Gulf of Carpentaria and Kimberley regions, where a mix of Aboriginal, conservation and pastoral land uses occurs, fuel loads were higher than in Arnhem Land region but still considerably lower than around Darwin. Sarga was recorded in all regions except the Gulf of Carpentaria and had the highest biomass in Darwin (0.88 t ha⁻¹) and lowest biomass in the Kimberley (0.54 t ha⁻¹). The proportion of herbaceous biomass made up of perennial grasses was least in Darwin (17%) and greatest in the Gulf (77%) regions. We suggest that climate, soils and land management account for differences between the drier pastoral regions of the Gulf of Carpentaria and the Kimberley and the wet Greater Darwin region relative to the Arnhem Land region. The high frequency, and larger spatial scale, of fires in the Greater Darwin region relative to the Arnhem Land region underpins the contrasting trends in total herbaceous biomass and abundance of flammable annual grasses.     

福建和溪亚热带雨林土壤酶活性的研究

福建和溪亚热带雨林土壤酶活性的研究郑文教,王良睦,林鹏（厦门大学环境科学研究中心,３６１００５）ＳｏｉｌＥｎｚｙｍａｔｉｃＡｃｔｉｖｉｔｙｉｎｔｈｅＳｕｂｔｒｏｐｉｃａｌＲａｉｎＦｏｒｅｓｔｉｎＨｅｘｉ,Ｆｕｊｉａｎ．￥ＺｈｅｎｇＷｅｎｊｉａｏ;Ｗａ...     

Ecology of Aglaia mackiana (Meliaceae) Seedlings in a New Guinea Rain Forest1

The large seeds of Aglaia mackiana (Meliaceae) germinate and produce vigorous seedlings under closed canopies or in large gaps. To assess seedling ecology after germination, we measured growth, herbivore damage, and survivorship of seedlings over one year. The sample included shaded seedlings from dispersed seeds, undispersed seeds under parent trees, and seedlings transplanted to gaps. We quantified the light environment using hemispherical canopy photographs taken above seedlings at the beginning and end of the one–year study. Seedlings transplanted to gaps grew faster and had more leaves, larger total leaf surface area, longer secondary roots, and greater root mass than shaded seedlings. Seedlings in gaps did not differ from shaded seedlings in survivorship or amount of herbivore– and pathogen–caused leaf damage. The canopy photographs taken one year apart suggest there is a rough equilibrium in closed canopies with slight changes occurring around an average light level. Sites with < 0.06 ISF (a unitless, relative measure of canopy openness or reflected sunlight) tended to remain the same with minor fluctuations toward brighter or darker. Sites with canopy openness > 0.06 ISF tended to close; few gaps grew larger. Seedlings under parenr trees and seedlings away from parent trees had similar amounts of leaf damage and virtually identical survivorship after 18 months, but seedlings under parent trees had slower growth rates and smaller total leaf surface areas. Dispersal did not strongly benefit seeds via escaping high levels of mortality or comperition around the parent.     

西双版纳地区热带雨林土壤酸杆菌(Acidobacteria)群体结构和多样性分析

酸杆菌(Acidobacteria)广泛存在于自然界,在许多生态系统中发挥重要作用。本文以西双版纳热带森林的土壤为研究对象,提取土壤的总基因组DNA为模板,采用特异引物扩增酸杆菌16SrRNA基因,构建酸杆菌门细菌16SrRNA基因克隆文库,利用限制性片段长度多态性(RFLP)对随机克隆进行筛选、测序,对该生态环境下酸杆菌菌群种类和组成进行了系统发育分析。结果表明该地区热带森林土壤的酸杆菌有5个类群:分别为Gp1、Gp2、Gp3、Gp5和1个未知分类的酸杆菌种。其中Gp1是该土壤环境下酸杆菌门的绝对优势菌群,约占整个酸杆菌群的50%-80%,其次是Gp2,占12%-25%,不同采样点酸杆菌类群的分布趋势是一致的。研究表明西双版纳热带森林土壤中的酸杆菌类群具有适应其土壤环境的广泛的多样性。     

Induced Natural Transformation of Acinetobacter calcoaceticus in Soil Microcosms

Factors affecting natural transformation of Acinetobacter calcoaceticus BD413 with homologous chromosomal DNA in a silt loam soil microcosm were investigated. Inducible transformation of declining populations of noncompetent A. calcoaceticus cells was detectable for up to 6 days when a simple carbon source, salts, and freshly added DNA were used. In two different experimental setups, the residence time in soil of induced cells could be increased to either 11 or 24 h before DNA addition without reduced transformation frequency; 200-to 1,000-fold fewer transformants were observed following the addition of water. These observations suggest that A. calcoaceticus remains transformable for several hours after its activation by nutrients in soil. Increasing the levels of phosphate salts significantly enhanced the numbers of transformants without increasing the recipient counts correspondingly. Variable levels of ammonium or divalent cations (Mg(sup2+) and Ca(sup2+)) did not have a similar major influence. Soil moisture content significantly affected the transformation frequency of A. calcoaceticus cells, with a general tendency of higher frequencies in drier soil. A minimal frequency was observed at around 35% soil moisture. The data indicate that A. calcoaceticus cells in soil which cannot be detectably transformed are easily induced by nutrients to undergo natural transformation with chromosomal DNA. Access to nutrients seems to be critical for the development and maintenance of competence in soil, which is also affected by abiotic factors like moisture level and phosphate salt concentration.     

The Influence of Soil Type on Rain Forest Insect Herbivore Communities

Insect herbivores were collected from five species of dipterocarp tree seedling within a large‐scale reciprocal transplant experiment in Sabah, Malaysia, on alluvial and sandstone soils in both gap and understory plots. The aim was to determine whether the location and ecological specialization of seedlings influenced the herbivore communities found on and around them. Three major groups of folivores were collected: Coleoptera, Orthoptera, and larval Lepidoptera. Herbivory of all species was confirmed through laboratory trials. Herbivore abundance in the understory plots was extremely low relative to the gaps. Rank‐abundance curves were similar on both soil types, differing only within the Lepidoptera. Coleoptera and Orthoptera communities were numerically dominated by a small suite of species capable of feeding on all dipterocarp species tested, whereas lepidopteran communities had both greater species richness and diversity. When corrected for leaf area surveyed, the abundance of Coleoptera was similar on both soil types, while larval Lepidoptera were more abundant in sandstone plots and Orthoptera were more abundant in alluvial plots. Estimated species richness of all three taxa was greater in alluvial forest, but there were contrasting patterns in Simpson diversity and evenness between groups. Species richness of Lepidoptera was greatest on seedlings when grown in their native soil type, providing partial evidence for possible escape effects, although this was not matched by differences in folivore abundance. The link between herbivore communities and herbivory rates on rain forest tree seedlings is complex and is unlikely to be detected through simplistic measures of abundance, species richness, or diversity.     

Soil Seedbank in a Dipterocarp Rain Forest in Xishuangbanna,Southwest China1

Dipterocarp rain forest reaches its northern latitudinal limit in Xishuangbanna, Southwest China. We studied the soil seedbank of dipterocarp rain forest in Xishuangbanna during the dry and wet seasons. Results showed that there were large seed accumulations in both the dry (mean ± SD; 3925 ± 2533 seeds/m²) and wet seasons (5415 ± 3232 seeds/m²). One hundred and sixteen species of seed plants were identified from germination, 66 percent of which were woody species. Weed or pioneer species dominated the seedbank. The soil seedbank in Xishuangbanna had similar species composition as compared to those in tropical Asia, but higher seed storage reflects the intense disturbance and forest fragmentation in this area.     

Seasonal changes in hydraulic conductance, xylem embolism and leaf area in Eucalyptus tetrodonta and Eucalyptus miniata saplings in a north Australian savanna

Eucalypt saplings in north Australian savannas commonly die back, sometimes to ground level, during the 5 months of the long dry season. Water potentials are lower in saplings than large trees during the dry season, and we hypothesized that low water potentials may lead to high levels of xylem embolism and consequent death of branches and whole shoots. As the dry season progressed, hydraulic conductance of terminal branches decreased by 50% in Eucalyptus tetrodonta but not in Eucalyptus miniata saplings. Hydraulic conductance per leaf area decreased seasonally by 34% in E. tetrodonta branches. These decreases may be associated with the loss of leaves recorded from E. tetrodonta but not E. miniata branches. We modelled the effect of sequential loss of parallel resistors, representing petioles on a branch. This showed there is a non-linear decrease in flow as basal resistors are lost, which can lead to a decrease in mean flow per resistor due to increased mean path-length. Thus the observed loss of basal leaves, together with xylem embolism, probably contributed to the seasonal loss of hydraulic conductance in E. tetrodonta saplings. Loss of hydraulic conductance due to xylem embolism was generally low ( < 15%) in both species, and the seasonal increase in embolism could not fully account for the decline in hydraulic conductance of E. tetrodonta branches. There was little evidence that branch and shoot death was caused by these levels of embolism. Developing an embolism vulnerability curve for species with long vessels is problematic and this issue is discussed.     

The Effects of Soil Bacterial Community Structure on Decomposition in a Tropical Rain Forest

Soil microorganisms are key drivers of terrestrial biogeochemical cycles, yet it is still unclear how variations in soil microbial community composition influence many ecosystem processes. We investigated how shifts in bacterial community composition and diversity resulting from differences in carbon (C) availability affect organic matter decomposition by conducting an in situ litter manipulation experiment in a tropical rain forest in Costa Rica. We used bar-coded pyrosequencing to characterize soil bacterial community composition in litter manipulation plots and performed a series of laboratory incubations to test the potential functional significance of community shifts on organic matter decomposition. Despite clear effects of the litter manipulation on soil bacterial community composition, the treatments had mixed effects on microbial community function. Distinct communities varied in their ability to decompose a wide range of C compounds, and functional differences were related to both the relative abundance of the two most abundant bacterial sub-phyla (Acidobacteria and Alphaproteobacteria) and to variations in bacterial alpha-diversity. However, distinct communities did not differ in their ability to decompose native dissolved organic matter (DOM) substrates that varied in quality and quantity. Our results show that although resource-driven shifts in soil bacterial community composition have the potential to influence decomposition of specific C substrates, those differences may not translate to differences in DOM decomposition rates in situ. Taken together, our results suggest that soil bacterial communities may be either functionally dissimilar or equivalent during decomposition depending on the nature of the organic matter being decomposed.     

夜间低温对2种热带雨林树种幼苗叶绿素荧光的影响

研究了夜间低温(5℃±1℃,12h,连续3个晚上)对生长于3种光照条件下(100%、25%和8%光照)的热带雨林冠层树种绒毛番龙眼(Pometiatomentosa)和中层树种滇南风吹楠(Horsfieldiatetratepala)幼苗叶绿素荧光的影响。结果表明:低温处理使生长于全光下的绒毛番龙眼幼苗的Fv/Fm(PSII最大光化学量子产量)急剧降低,中午发生了强烈的光抑制,但随着低温胁迫的解除Fv/Fm能很快恢复,表明没有发生不可逆的光氧化损伤。低温使生长于全光和25%光照条件下2个树种幼苗的NPQ(非光化学猝灭,热耗散)受到抑制,但没有引起2个树种幼苗Fo(初始荧光)的升高,不会导致幼苗PSII反应中心的失活。2种热带雨林植物对低温的抗性可能与这些植物的地理分布和历史渊源有关。     

西双版纳热带季节雨林土壤氮含量对乔木树种多样性的影响?

大气氮沉降或人类活动导致生态系统氮输入增加,可能会提高土壤氮含量水平,促进优势种的生长和减少环境异质性,从而使物种共存的生态位减少,群落物种多样性降低。为研究土壤氮含量的增加对森林群落乔木树种多样性的影响,本研究在西双版纳热带季节雨林随机设置了14个1 ha的样方,对各样方土壤总氮( TN)含量、乔木树种丰富度以及西双版纳热带季节雨林20 ha动态监测样地中各样方乔木树种及建群种望天树( Parashorea chinensis)生物量进行了调查。结果表明：土壤氮含量与乔木树种丰富度具有显著负相关而与群落及建群种望天树生物量具有显著正相关。我们推测其机制可能是：土壤氮含量增加促进了建群种望天树等的生长及群落生物量的积累,减少树种共存的生态位,由于竞争排斥等原因而导致群落树种丰富度降低。因此,减少生态系统人为氮输入,对于保护西双版纳热带季节雨林乔木树种多样性具有重要意义。     

High Noon in the Rain Forest

Guido Boggiani. Fotograf. Fotografo. Fotografo. Photographer. Pavel Fric and Yvonna Fricova. eds. Nakladatelsvi Titanic, Praha, 1997. 82 photographs. 137 pp. Text and captions are in Czech, Italian, Spanish, Portuguese, and English.     

Migratory Response of Soil Bacteria to Lyophyllum sp. Strain Karsten in Soil Microcosms

In this study, the selection of bacteria on the basis of their migration via fungal hyphae in soil was investigated in microcosm experiments containing Lyophyllum sp. strain Karsten (DSM2979). One week following inoculation with a bacterial community obtained from soil, selection of a few specific bacterial types was noticed at 30 mm in the growth direction of Lyophyllum sp. strain Karsten in sterile soil. Cultivation-based analyses showed that the migration-proficient types encompassed 10 bacterial groups, as evidenced by (GTG)₅ genomic fingerprinting as well as 16S rRNA gene sequencing. These were (>97% similarity) Burkholderia terrae BS001, Burkholderia sordidicola BS026, Burkholderia sediminicola BS010, and Burkholderia phenazinium BS028; Dyella japonica BS013, BS018, and BS021; “Sphingoterrabacterium pocheensis” BS024; Sphingobacterium daejeonense BS025; and Ralstonia basilensis BS017. Migration as single species was subsequently found for B. terrae BS001, D. japonica BS018 and BS021, and R. basilensis BS017. Typically, migration occurred only when these organisms were introduced at the fungal growth front and only in the direction of hyphal growth. Migration proficiency showed a one-sided correlation with the presence of the hrcR gene, used as a marker for the type III secretion system (TTSS), as all single-strain migrators were equipped with this system and most non-single-strain migrators were not. The presence of the TTSS stood in contrast to the low prevalence of TTSSs within the bacterial community used as an inoculum (<3%). Microscopic examination of B. terrae BS001 in contact with Lyophyllum sp. strain Karsten hyphae revealed the development of a biofilm surrounding the hyphae. Migration-proficient bacteria interacting with Lyophyllum sp. strain Karsten may show complex behavior (biofilm formation) at the fungal tip, leading to their translocation and growth in novel microhabitats in soil.Bacterial-fungal interactions are common in a wide variety of habitats like decaying wood, human bodies, and marine and soil environments (7, 12, 13, 15, 18). Especially in soil, interactions are likely to occur frequently, as members of both kingdoms abound in this system and depend on strategies that allow them to utilize the sparse carbonaceous nutrients that are available (6, 22, 26, 27). Interactions may be deleterious, neutral, or even beneficial for either or both of the partners. In particular, the putative beneficial effects exerted by soil fungi on associated bacteria may enhance bacterial fitness and thus provide a selective force on these (4, 5, 11, 14, 29). A range of different mechanisms is thought to play a role in the putative bacterial selection, in which particular fungus-released compounds may exert key effects in this selection (1, 10, 14, 28). In addition, changes in the structure of the local (soil) habitat effected by either of the partners (2) and/or production of antibacterial substances by the fungal partner (7, 9) may play roles.The capacity of soil bacteria to use fungal hyphae as a means to reach and colonize novel microhabitats in soil has been proposed as a mechanism for pollutant-degrading bacteria to become efficient in polluted soil (16). However, the study addressed only bacterial migration with fungi via so-called fungal highways in non-soil systems like agar plates and glass bead systems. Clearly, such fungal highways might be used by bacteria to cross air gaps (23) during growth and movement in soil, but evidence for this is lacking. Movement of the bacterial partner was probably driven by motility of the bacterial cells in the water film surrounding the fungal hyphae. The observation of bacteria moving along fungal highways was supported by an earlier study that addressed bacterial motility via dead hyphae of an oomycete in soil (32). Together, these studies suggest that bacteria can utilize the mycosphere (here defined as the fungal hyphal network) in soil to reach and colonize novel microhabitats. However, these studies do not allow an in-depth assessment of which bacteria get selected by growing fungi and how they mechanistically make use of fungal highways.In the current study, we assessed the putative selection of organisms from a soil bacterial community that was able to migrate in the mycosphere of Lyophyllum sp. strain Karsten, a close saprotrophic relative of the ectomycorrhizal fungus Laccaria proxima. We initially assessed the selection of particular bacterial species by L. proxima (29), which was an abundant ectomycorrhizal species with hazel trees. Thus, we developed a microcosm system composed of three compartments, which allowed the outgrowth of fungal hyphae from a nutrient source into sterile soil. Different aspects of bacterial migration along with the fungal front were studied. Based on these findings, a mechanism for bacterial migration in which biofilm formation plays a role is proposed.     

Influence of Environmental Factors on Plasmid Transfer in Soil Microcosms

A model system was established to determine whether plasmid transfer occurs in soil and how various environmental conditions and cellular energy states affect the rate of plasmid transfer. Different donor and recipient bacteria were inoculated into sterile sandy lutitic soil microcosms. Dispersion studies were performed with a multipoint inoculator sampler. Transconjugant cells were enumerated by direct plating on antibiotic-amended LB medium. The influences of soil moisture (6.7 to 60%), incubation temperature (4° to 44°C) and pH (5.3 to 9.2) on cell dispersal and on plasmid transfer were examined. Maximum transfer frequencies were observed at: 20% of moisture content, pH between 7 and 8, and 30°C. These results indicate that plasmid transfer may occur in soil and that environmental conditions may significantly affect the rate of transfer.     

Factors Limiting Tropical Rain Forest Regeneration in Abandoned Pasture: Seed Rain,Seed Germination,Microclimate, and Soil1

Vegetation, seed rain, seed germination, microclimate, and soil physical and chemical parameters were measured in a recently abandoned pasture and adjacent primary rain forest in southern Costa Rica. The goal of this study was to assess the importance of these factors in limiting forest regeneration in abandoned pastures. Seed rain of animal dispersed species decreased dramatically in the pasture >5 m from the forest/pasture edge; fewer wind dispersed seeds fell in the pasture than in the forest, but the difference was much less than for animal dispersed seeds. Percent seed germination of most species studied was similar in the forest and in pasture with grasses; seed germination was lower during the dry season in areas of pasture cleared of grasses. Air temperature, vapor pressure deficit (VPD), and photon flux density (PFD) were much higher in the pasture than in the forest at 1 m above the ground. VPD and PFD at ground level and soil temperature were similar in the pasture and the forest, indicating that pasture grasses strongly modify microclimatic conditions near the soil surface. The lowest gravimetric water content recorded in the pasture during the dry season was 0.5 and leaf relative water contents of the two species measured in the forest and pasture were identical, suggesting that plants in the pasture were not water stressed. Levels of most soil nutrients were lower in the pasture as compared to the forest; however, aboveground and root biomass for seedlings grown in pasture and forest soils did not differ significantly. Although a number of factors impede forest recovery in abandoned pastures, these results suggest that the most imporrant limitation is lack of seed dispersal.     

Differences in Survival and Growth Among Tropical Rain Forest Pioneer Tree Seedlings in Relation to Canopy Openness and Herbivory

Although differences in canopy openness, herbivory and their interaction may promote species coexistence, how these factors affect pioneer tree species and potentially limit growth, and survival has been poorly studied, particularly in tropical South Asia. We monitored the effect of canopy openness and herbivore damage on seedling survival and growth of 960 individuals of six pioneer tree species: Dillenia triquetra, Macaranga indica, Macaranga peltata, Schumacheria castaneifolia, Trema orientalis, and Wendlandia bicuspidata. Seedlings were placed in four gap‐understory positions—center, outer gap edge, inner forest edge, and understory—in four large, natural gaps within the Sinharaja World Heritage Reserve, Sri Lanka. Canopy openness positively affected survival probability beyond the 550‐d experiment, while herbivory decreased survival and was highest in understory conditions. The relative order of species survival stayed fairly consistent between gap‐understory positions and followed their known shade tolerance rankings. When averaged across all experimental conditions, T. orientalis had the lowest survival probability estimate beyond the 550‐d experiment (0.05), but the greatest capacity for growth where it successfully established, while the species with highest averaged survival probability (0.79), D. triquetra, showed the lowest growth. One species, W. bicuspidata, responded positively to herbivory by re‐sprouting. Coexistence of D. triquetra, T. orientalis, and W. bicuspidata can be explained by a trade‐off among species in survival, growth, and response to herbivory. In addition to variation in canopy light environment, herbivory may be important in determining pioneer species distribution through fine‐scale niche partitioning and should be carefully considered in reforestation efforts.     

福建闽清福建青冈天然林种子雨和种子库

对福建闽清黄楮林自然保护区的福建青冈(Cyclobalanopsis chungii)天然林的种子雨和土壤种子库进行了观测和分析.结果表明,福建青冈种子雨持续2个月,其高峰期在11月下旬～12月上旬,总量为12.44个m~(-2),在种子散布过程中完好种子、虫蛀种子、败育种子、霉烂种子和萌发种子的比例差异明显,其中虫蛀种子是萌发种子的19.44倍.土壤种子库中虫蛀种子占53.79%,与种子雨相比,完好种子和萌发种子数量分别减少2.15个m~(-2)和0.20个m~(-2).土壤种子库种子存活率仅13.51%,动物捕食率达45.90%,说明动物的捕食和搬运是福建青冈种子缺失的原因之一.福建青冈天然林土壤种子库有69种植物种子,但种子数量较少,且分布不均匀,种子库中78.42%种子分布在2～5 cm土层中.福建青冈天然林中实生幼苗少与福建青冈种子本身特性及其生长环境密切相关,福建青冈种子发育成熟后因动物侵扰、虫蛀、霉烂和败育等情况发生,难以在土壤中长期保存,以致福建青冈林分天然更新严重受阻.     

西双版纳不同海拔4种雨林幼苗的光合特性和生物量

在云南西双版纳勐仑(600 m,低海拔)、菜阳河(1 100 m,中海拔)和勐宋(1 600 m,高海拔),对热带季节雨林4种主要树种绒毛番龙眼(Pometio tomentosa)、云南玉蕊(Barringtonia macrostachya)、云南肉豆蔻(Myristica yunnanensis)和小叶红光树(Knema globularia)幼苗进行移栽试验,测定幼苗的光合作用和生物量.结果表明,高海拔七的低温使幼苗处于休眠或光系统受到不可恢复的破坏,光合作用几乎停止;4种幼苗的最大净光合速率及生物量均随海拔的增加而下降;低、中海拔上4种幼苗的净光合速率日变化曲线均表现为"双峰型",低海拔的第一个峰明显高于中海拔.除小叶红光树外,其它幼苗的根生物量分数均随海拔增高而增加.海拔升高,温度降低是限制幼苗光合特性、生物量积累的主要因子,也是某些幼苗在更高海拔雨林群落中消失的潜在原因.此外,幼苗的根生物量分数随海拔上升而增加是其对极限环境温度的一种重要适应特征.