3种地被类观赏竹对大气臭氧浓度倍增的生理响应

运用开顶式同化箱(OTCs)模拟环境背景大气O3浓度(CK,40~45 nL.L-1)的倍增1倍(TR-1,92~106nL.L-1)和倍增2倍(TR-2,142~160 nL.L-1)情景,分析美丽箬竹、黄条金刚竹和白缟椎谷笹竹叶片脂质过氧化、抗氧化酶和渗透调节物质等生理指标的变化,以明确竹子对大气O3浓度倍增的生理响应规律及耐受O3胁迫能力的种间差异性,为园林观赏竹种选育和应用提供参考。结果表明:(1)大气O3浓度倍增45 d时,随着O3浓度的升高,3种地被类观赏竹叶片O2.-和MDA含量、相对电导率、SOD活性均表现出增大趋势。叶片POD活性、可溶性糖含量美丽箬竹呈下降趋势,而黄条金刚竹和白缟椎谷笹竹呈升高趋势。叶片可溶性蛋白含量美丽箬竹和白缟椎谷笹竹呈下降趋势,黄条金刚竹呈升高趋势。(2)大气O3浓度倍增1倍时,美丽箬竹和黄条金刚竹未表现出伤害症状,而白缟椎谷笹竹表现出明显的伤害症状;大气O3浓度倍增2倍时,3种地被类观赏竹叶片活性氧含量大量积累,抗氧化系统遭到破坏,膜脂过氧化加剧,影响正常的生理代谢和生长发育。(3)主成分分析表明,叶片MDA含量是反映地被类观赏竹耐受O3胁迫最重要的生理指标,耐受O3胁迫能力表现为美丽箬竹>黄条金刚竹>白缟椎谷笹竹。     

CO2浓度升高对三种地被类观赏竹生理特性的影响

运用开顶式气室(OTCs)模拟大气CO₂浓度升高(500、700 μmol·mol^-1)情景,以环境背景大气为对照,研究CO₂浓度升高对3种地被类观赏竹(美丽箬竹、黄条金刚竹和白缟椎谷笹竹)叶片的膜脂过氧化和抗氧化系统的影响及其种间差异.结果表明: 试验进行103 d后,500 μmol·mol^-1CO₂浓度下,3种地被类观赏竹的叶片超氧阴离子含量、丙二醛(MDA)含量、相对电导率和可溶性糖含量总体上没有发生明显的变化,但叶片超氧化物歧化酶(SOD)、过氧化物酶(POD)、过氧化氢酶(CAT)和抗坏血酸过氧化物酶(APX)活性有一定程度的改变;700 μmol·mol^-1 CO₂浓度下,3个竹种的叶片MDA含量和相对电导率没有发生明显变化,但对叶片超氧阴离子含量、可溶性糖含量和SOD、POD、CAT、APX活性的影响较为明显.不同竹种对CO₂浓度升高环境的适应能力为美丽箬竹＞黄条金刚竹＞白缟椎谷笹竹.     

CO2浓度升高对三种地被类观赏竹生理特性的影响

运用开顶式气室(OTCs)模拟大气CO₂浓度升高(500、700 μmol·mol^-1)情景,以环境背景大气为对照,研究CO₂浓度升高对3种地被类观赏竹(美丽箬竹、黄条金刚竹和白缟椎谷笹竹)叶片的膜脂过氧化和抗氧化系统的影响及其种间差异.结果表明: 试验进行103 d后,500 μmol·mol^-1CO₂浓度下,3种地被类观赏竹的叶片超氧阴离子含量、丙二醛(MDA)含量、相对电导率和可溶性糖含量总体上没有发生明显的变化,但叶片超氧化物歧化酶(SOD)、过氧化物酶(POD)、过氧化氢酶(CAT)和抗坏血酸过氧化物酶(APX)活性有一定程度的改变;700 μmol·mol^-1 CO₂浓度下,3个竹种的叶片MDA含量和相对电导率没有发生明显变化,但对叶片超氧阴离子含量、可溶性糖含量和SOD、POD、CAT、APX活性的影响较为明显.不同竹种对CO₂浓度升高环境的适应能力为美丽箬竹＞黄条金刚竹＞白缟椎谷笹竹.     

四季竹对大气臭氧浓度升高的生理响应

运用开顶式同化箱(OTCs)在5个O3浓度梯度(过滤大气CF、环境大气NF、50 nL·L-1、100 nL·L-1和150nL·L-1)下,研究了大气O3浓度对四季竹(Oligostachyum lubricum)叶片光合色素、脂质过氧化和抗氧化系统的影响.结果显示:在胁迫处理90 d时,随着O3浓度的升高,四季竹叶片叶绿素(Chl)、类胡萝卜素(Car)、可溶性糖和可溶性蛋白含量呈持续下降趋势,相对电导率和丙二醛(MDA)含量持续升高,超氧化物歧化酶(SOD)活性先升高后降低,过氧化物酶(POD)活性呈升高趋势.与CF相比,四季竹叶片Chl、Car和MDA含量在O3浓度为100 nL·L-1时均有显著差异,在150 nL·L-1时均有极显著差异;相对电导率、SOD和POD活性、可溶性糖和可溶性蛋白含量在O3浓度为100 nL·L-1及以上时均有极显著差异.研究表明,大气长时间高O3浓度(100 nL·L-1及以上)胁迫对四季竹会产生明显伤害效应,致使其叶片光合色素降解或合成受阻,叶片老化加快,膜脂过氧化程度加剧,膜结构和抗氧化系统遭到破坏.     

大气O3浓度升高对毛竹光合生理的影响

以毛竹(phyllostachys edulis)为试材,运用开顶式气室(OTCs)模拟了4个大气O3浓度情景,分别为CF(背景大气经活性炭过滤后的处理,22～25 nL·L-1)、NF(直接将背景大气输入气室内,40～45 nL·L-1)、T1(O3平均浓度100 nL·L-1,92～106 nL·L-1)、T2(O3平均浓度150 nL· L-1,142 ～160 nL· L-1),分析大气O3浓度对毛竹叶片光合色素、气体交换参数、光合参数的影响.结果表明:不同浓度O3处理的毛竹叶片Pn和Tr日变化均呈单峰型,随着O3浓度的升高,叶片Gs、Ci、Ls日变化规律趋于简单,WUE变化趋于平缓.与环境背景大气比较,高浓度O3(≥100 nL·L-1)条件下叶片Pn、Ls、WUE日均值和Chl、Chl-a、Chl-b和Car含量均显著降低,Gs、Tr日均值显著提高,但对Ci日均值及叶片光合色素组成影响并不明显.T1、T2处理下,毛竹的Pn、Tr与PPED、VpdL、Tair、Ca和RH环境因子间均呈显著或极显著相关,Gs与PPED无显著相关,而与VpdL、Tair、Ca和RH环境因子间均呈显著或极显著相关.研究表明:O3浓度100、150 nL·L-1时分别会造成毛竹叶片发生气孔、非气孔限制,气孔对环境条件的反应变得不敏感,影响了正常的调节反馈机制,增加了水分蒸散,光合色素降解或合成受阻,对毛竹光合作用产生严重的负面效应,不利于毛竹干物质积累.     

土壤铅胁迫对地被竹出笋成竹的影响研究

以6种地被竹(菲黄竹、菲白竹、铺地竹、美丽箬竹、白纹椎谷笹和狭叶倭竹)为材料,设计3个土壤铅浓度处理(0、300、1500mg·kg^-1),研究土壤铅胁迫对地被竹出笋成竹数量和新竹抗逆生理特性的影响,并采用隶属函数法对地被竹出笋成竹期的土壤铅耐受性进行综合评价。结果表明:(1)土壤铅胁迫对地被竹笋期节律的影响主要出现在出笋盛期(4~5月),发笋数的降低会导致多数竹种退笋率下降,以稳定新竹数量,只有菲白竹、白纹椎谷笹、狭叶倭竹的新竹数在高浓度土壤铅胁迫下显著低于CK,降幅分别为15.87%、23.64%和31.25%。(2)土壤铅胁迫会普遍引起地被竹新竹超氧阴离子和丙二醛含量的增加,在高浓度铅胁迫下铺地竹中二者含量最低(9.96μg·g^-1、0.016μmol·g^-1),狭叶倭竹的超氧阴离子含量最高(15.99μg·g^-1),菲黄竹的丙二醛含量最高(0.021μmol·g^-1)。(3)与其余4个竹种不同,在土壤铅胁迫下白纹椎谷笹和狭叶倭竹不能显著积累游离脯氨酸,细胞渗透调节作用弱。(4)6种地被竹在出笋成竹期对高浓度土壤铅的耐受性排序为:美丽箬竹(0.79)>铺地竹(0.75)>菲白竹(0.70)>狭叶倭竹(0.49)>白纹椎谷笹(0.39)>菲黄竹(0.38),其中美丽箬竹、铺地竹和菲白竹出笋成竹数量正常,且具有较强的抗逆生理特性,具有在高浓度土壤铅污染地区应用的潜力。     

毛竹和四季竹对臭氧胁迫的耐受力差异

为了解竹子对大气O3浓度升高的生理响应规律及耐受O3胁迫能力的种间差异性,为气候变化背景下的竹林培育应对策略提供理论依据,运用开顶式同化箱(OTCs)开展了5个O3浓度梯度(过滤大气CF、环境大气NF、50、100和150 nl·L-1)对毛竹(Phyllostachys edulis)和四季竹(Oligostachyum lubricum)叶片光合色素、可溶性蛋白、脂质过氧化和抗氧化系统的影响研究.结果表明:处理90d后,随着O3浓度的升高,毛竹和四季竹叶片叶绿素(Chl)、类胡萝卜素(Car)含量均呈下降趋势,但毛竹的降幅大于四季竹.MDA含量、POD活性呈升高趋势,毛竹的升幅大于四季竹.SOD活性毛竹呈下降趋势,而四季竹表现出先升高后降低的规律.可溶性蛋白含量毛竹和四季竹分别呈升高、降低趋势;与CF相比,低O3浓度处理(≤50 nl·L-l)并未对毛竹和四季竹造成明显伤害,而高O3浓度处理(≥100 nl·L-1)下毛竹和四季竹叶片光合色素含量和SOD活性极显著降低,MDA含量和POD活性极显著提高,导致毛竹和四季竹叶片光合色素合成受阻,叶片老化加快,膜脂过氧化程度加剧,膜结构和抗氧化系统功能遭到破坏;主成分分析表明,四季竹对O3胁迫的耐受能力明显强于毛竹.     

美丽箬竹对模拟大气O3浓度倍增胁迫的生理响应

运用开顶式气室(OTCs)模拟当前环境大气O3浓度(对照,40～45 nL·L-1)、O3浓度倍增4倍(TR-1,92～106 nL·L-1)和O3浓度倍增2倍(TR-2,142～160 nL·L-1)胁迫,以叶片光合色素、MDA、可溶性蛋白质和可溶性糖含量及SOD和POD活性和相对电导率为指标,分析了美丽箬竹(Indocalamus decorus Q.H.Dai)对O3胁迫的生理响应规律.结果显示:随O3浓度的提高,叶片叶绿素a(Chla)、叶绿素b(Chlb)、总叶绿素和类胡萝卜素含量,SOD和POD活性,可溶性蛋白质和可溶性糖含量及二者的比值(SPC/SSC)均呈下降趋势;叶绿素a口与b的比值(Chla/Chlb)、MDA含量和相对电导率均呈增加趋势.TR-1条件下叶片POD活性和可溶性糖含量分别比对照下降38.86％和10.37％,差异显著;Chla/Chlb比值显著高于对照,其余指标均与对照无显著差异.而在TR-2条件下叶片Chla、Chlb、总叶绿素和类胡萝卜素含量显著低于对照,降幅分别为26.89％、40.91％、30.47％和20.37％;SOD和POD活性、可溶性蛋白质和可溶性糖含量以及PC/SSC比值也均显著低于对照,降幅分别为42.03％、46.62％、45.09％、11.52％和40.15％;Chla/Chlb比值、MDA含量和相对电导率均显著高于对照.另外,TR-1与TR-2处理组间光合色素含量和POD活性差异不显著,TR-2处理组MDA含量和相对电导率显著高于TR-1处理组,SOD活性显著低于后者.研究结果表明:美丽箬竹对O3胁迫具有强耐受性,可种植于O3浓度较高的环境中.     

毛竹对大气臭氧浓度倍增的生理响应

为了给气候变化背景下的竹林培育应对策略提供理论依据,以毛竹 （Phyllostachys edulis） 为材料,运用开顶式气室 （OTCs） 模拟当前环境背景大气O3浓度（NF,40~45nL·L-1）的倍增1倍（TR1,92~106nL·L-1）和倍增2倍（TR2, 142~160nL·L-1）情景,分析叶片光合色素、脂质过氧化及抗氧化酶等生理指标的变化规律。结果表明：大气O3浓度倍增处理90d时,毛竹叶片Chl、Car含量和SOD活性显著降低,叶片相对电导率和可溶性蛋白、MDA、O2-含量及POD活性显著升高。叶片O2-含量与SOD活性、光合色素含量呈极显著负相关,而与叶片相对电导率、POD活性和MDA、可溶性蛋白含量呈显著正相关。研究表明大气O3浓度倍增会导致毛竹叶片老化加快,光合色素降解或合成受阻,膜脂过氧化,膜结构和氧化系统破坏,影响毛竹的正常生长。本文从抗性生理方面揭示了毛竹对大气臭氧胁迫的耐受性,为竹子应对气候变化研究提供了参考。     

毛竹对大气臭氧胁迫的生理响应变化

以毛竹1年生盆栽苗为材料,运用开顶式气室(OTCs)模拟环境背景大气O3浓度(AA,40～45 nL·L-1)和高O3浓度(EO,92～106 nL·L-1)情景,分析毛竹叶片光合生理、脂质过氧化及抗氧化酶等主要生理指标的变化,为气候变化背景下的竹林培育应对策略提供理论依据.结果显示:(1)EO较AA在同一处理时间的毛竹叶片O3通量均显著升高,且二处理的叶片O3通量均随着处理时间的延长呈升高趋势.(2) EO较AA的光合速率(Pn)、气孔导度(Gs)和可溶性糖含量均显著下降,且叶片叶绿素(ChD含量、胞间CO2浓度(Ci)显著下降的时间点分别出现在EO处理的60 d和92 d,可溶性蛋白在处理60 d后显著升高;随处理时间的延长,EO的叶片Pn、Ci、Chl含量均呈下降趋势,可溶性糖和可溶性蛋白含量呈先升高后降低的趋势;Pn下降由气孔限制因素引起.(3)超氧自由基(O2)含量、丙二醛(MDA)含量、相对电导率分别在处理29 d、60 d、60 d后均显著升高,且随着处理时间的延长呈升高趋势.(4)超氧化物歧化酶(SOD)活性在高浓度O3处理60 d时显著升高,后显著下降,而POD活性均显著升高,且SOD和POD活性均随着处理时间呈先升高后降低的趋势.研究表明,毛竹对大气高O3胁迫存在着短时间的主动生理生化适应,但长期高O3胁迫会对毛竹造成严重的过氧化伤害,从而影响毛竹的正常生长.     

Shade tolerance of temperate Asian bamboos: a harbinger of their naturalization in Pacific Northwest coniferous forests?

Bamboos native to temperate East Asian coniferous forests arrive with increasing frequency in the United States as horticultural imports, and some are becoming naturalized locally. Given the strong floristic and physiognomic similarities between East Asian and western North American coniferous forests, we asked whether these introduced bamboos could tolerate the varied light regimes within coniferous forests in their new range. Seven temperate Asian bamboos and one North American bamboo (Arundinaria gigantea) were grown within shade structures in an experimental garden; these structures reduced ambient light to three light levels (50, 70, 90 % shade) that occur routinely within coniferous forests in the Pacific Northwest. Species’ responses under these light levels were measured by their light response curves to photosynthesis, resource allocation to light or carbon harvesting centers inferred by CO₂ response curves, and shifts amongst forms of leaf Chlorophyll. Bashania fargesii has lower chlorophyll content and photosynthetic rates under high shade (90 %) relative to other Asian species and to B. fargesii grown in 50 and 70 % shade. Bashania fargesii, Sasa kurilensis and A. gigantea also displayed lower photosynthetic rates under 90 % shade compared to plants grown in 50 and 70 % shade and lower electron transport capacity under 70 and 90 % shade compared to plants grown in 50 % shade. In contrast, Pleioblastus chino, Pleioblastus distichus, Pseudosasa japonica, Sasa palmata and Sasaella ramosa display strong tolerance of low light. Our results indicate these five Asian bamboos (and others yet to be introduced) could skirt a major environmental barrier to new species establishment in these North American forests. Measuring a species’ light response curve offers a reliable, rapid means to assess an immigrant species’ potential to tolerate forests’ varied light regimes.     

Using leaf optical properties to detect ozone effects on foliar biochemistry

Efficient methods for accurate and meaningful high-throughput plant phenotyping are limiting the development and breeding of stress-tolerant crops. A number of emerging techniques, specifically remote sensing methods, have been identified as promising tools for plant phenotyping. These remote sensing methods can be used to accurately and rapidly relate variations in leaf optical properties with important plant characteristics, such as chemistry, morphology, and photosynthetic properties at the leaf and canopy scales. In this study, we explored the potential to utilize optical (λ = 500–2,400 nm) near-surface remote sensing reflectance spectroscopy to evaluate the effects of ozone pollution on photosynthetic capacity of soybean (Glycine max Merr.). The research was conducted at the Soybean Free Air Concentration Enrichment (SoyFACE) facility where we subjected plants to ambient (44 nL L^?1) and elevated ozone (79–82 nL L^?1 target) concentrations throughout the growing season. Exposure to elevated ozone resulted in a significant loss of productivity, with the ozone-treated plants displaying a ~30 % average decrease in seed yield. From leaf reflectance data, it was also clear that elevated ozone decreased leaf nitrogen and chlorophyll content as well as the photochemical reflectance index (PRI), an optical indicator of the epoxidation state of xanthophyll cycle pigments and thus physiological status. We assessed the potential to use leaf reflectance properties and partial least-squares regression (PLSR) modeling as an alternative, rapid approach to standard gas exchange for the estimation of the maximum rates of RuBP carboxylation (V _c,max), an important parameter describing plant photosynthetic capacity. While we did not find a significant impact of ozone fumigation on V _c,max, standardized to a reference temperature of 25 °C, the PLSR approach provided accurate and precise estimates of V _c,max across ambient plots and ozone treatments (r ² = 0.88 and RMSE = 13.4 μmol m^?2 s^?1) based only on the variation in leaf optical properties and despite significant variability in leaf nutritional status. The results of this study illustrate the potential for combining the phenotyping methods used here with high-throughput genotyping methods as a promising approach for elucidating the basis for ozone tolerance in sensitive crops.     

干旱胁迫下黄条金刚竹的光合和叶绿素荧光特性

通过盆栽试验,研究了自然干旱胁迫处理下,黄条金刚竹植株形态、土壤含水量(SWC)、叶片含水量(LWC)、叶片水势(LWP)、光合作用参数和叶绿素荧光参数的变化,及与环境因素的关系.结果表明:自然干旱胁迫后第17天,黄条金刚竹出现干旱伤害症状,叶片失水下垂、内卷,第43天地上部分失水死亡;复水后10 d,叶片叶绿素荧光参数与第43天无显著差异.在干旱胁迫0～21 d,SWC显著下降,而在17 d以后,LWP急剧下降,29 d以后LWC显著降低.随着干旱胁迫程度的加剧,叶片蒸腾速率(T_r)、气孔导度(g_s)持续下降,而光合速率(P_n)波动较大,瞬时水分利用效率（PWUE）则先升高后降低;17 d后,P_n由气孔限制为主转为非气孔限制为主,实际光合效率(Φ_PSⅡ)开始下降;25 d后,黄条金刚竹的光合机构被破坏,最大光化学效率(F_v/F_m)和PSⅡ潜在热耗散能力(q_N)分别由0.64、0.79下降到-0.11、0.33.T_r、g_s、PWUE与LWP密切相关,大气湿度对P_n、T_r、g_s的影响显著,气孔是光合参数变化的主导因素.本试验条件下,黄条金刚竹适宜在土壤相对含水率≥12%的土壤中生长,且干旱胁迫持续时间不超过25 d.     

Bambusicolous fungi in Japan (5): three species of Tetraploa

Three species of Tetraploa collected from Sasa, or bamboos, are described and illustrated. Among them, T. curviappendiculata on Sasa kurilensis and T. longissima on Pleioblastus chino are compared with hitherto known species and described as new species. In the nomenclature, T. javanica is substituted for T. biformis, formerly reported from the dead bark of a broad-leaved tree in Japan, as a correct name.     

Enhancing hypericin production of Hypericum perforatum cell suspension culture by ozone exposure

Accumulation of secondary metabolites is one of the common reactions of plants to ozone exposure in nature. To investigate the effect of ozone on the production of desired compounds of plant cell cultures, we assayed hypericin production of Hypericum perforatum suspension cell cultures treated with different doses of ozone at different culture phases. The results show that hypericin contents of the cells treated with 60 to 180 nL L^?1 ozone are significantly higher than those of the control, showing that ozone exposure may stimulate hypericin synthesis. Hypericin production of the cells treated with ozone at exponential phase is higher than that of lag and stationary phase, which suggests that exponential phase cell cultures are more responsive to ozone exposure than lag and stationary phase cells. The highest hypericin production is obtained by the cells exposed to 90 nL L^?1 ozone at late exponential phase for 3 h, being about fourfold of the control. © 2011 American Institute of Chemical Engineers Biotechnol. Prog., 2011     

Ameliorating effect of UV-B radiation on the response of Norway spruce and Scots pine to ambient ozone concentrations

Elevated levels of both ozone and UV-B radiation are typical for high-altitude sites. Few studies have investigated their possible interaction on plants. This study reports interactive effects of O₃ and UV-B radiation in four-year-old Norway spruce and Scots pine trees. The trees were cultivated in controlled environmental facilities under simulated climatic conditions recorded on Mt Wank, an Alpine mountain in Bavaria, and were exposed for one growing season to simulated ambient or twice-ambient ozone regimes at either near ambient or near zero UV-B radiation levels. Chlorotic mottling and yellowing of current year needles became obvious under twice-ambient O₃ in both species at the onset of a high ozone episode in July. Development of chlorotic mottling in relation to accumulated ozone concentrations over a threshold of 40 nL L^–1 was more pronounced with near zero rather than ambient UV-B radiation levels. In Norway spruce, photosynthetic parameters at ambient CO₂ concentration, measured at the end of the experiment, were reduced in trees cultivated under twice-ambient O₃, irrespective of the UV-B treatment. Effects on photosynthetic capacity and carboxylation efficiency were restricted to trees exposed to near zero levels of UV-B radiation, and twice-ambient O₃. The data indicate that UV-B radiation, applied together with O₃, ameliorates the detrimental effects of O₃. The data also demonstrate that foliar symptoms develop more rapidly in Scots pine than in Norway spruce at higher accumulated ozone concentrations. Symbols and abbreviations: LSD, least significant difference; PAS300, UV-B irradiance weighted according to the plant action spectrum of Green et al. (1974) normalized at 300 (nm); AOT40, (AOT = accumulated over threshold) reflects the sum of hourly ozone concentrations above 40 nL L^–1 during daylight hours (> 50 Wm^–2) ( Kärenlampi & Skärby 1996 ); A₃₅₀, net photosynthesis at ambient CO₂; G₃₅₀, stomatal conductance for water vapour at ambient CO₂; A₂₅₀₀, net photosynthesis at saturating CO₂ (maximal potential photosynthetic activity); CE, carboxylation efficiency; ROS, reactive oxygen species; RuBP, ribulose 1,5-bisphosphate; Rubisco, ribulose 1,5-bisphosphate carboxylase/oxygenase; GLM, general linear model.     

Several changes of Indocalamus leaf active ingredients contents

In this paper, the leaves of Indocalamus herklotsii, Indocalamus decorus, and Indocalamus latifolius were collected from Nanjing in different seasons to study the seasonal changes of the total flavonoids, tea polyphenols, and soluble sugar contents in the leaves. There existed significant differences in the test active ingredients contents among the leaves of the three Indocalamus species. The leaf total flavonoids content of the three Indocalamus species in different seasons ranged in 1.7%-2.7%, being the highest for I. herklotsii and I. decorus in spring and for I. latifolius in winter. The leaf tea polyphenols content varied from 5.5% to 7.6%; and the leaf soluble sugar content was 1.0%-8.5%, with the maximum in spring. Within the three months after leaf unfolding, the active ingredients contents in I. herklotsii and I. decorus leaves increased with leaf age. The optimal period for harvesting Indocalamus leaves was from December to next March. Among the three Indocalamus species, I. latifolius had the highest contents of the three active ingredients in leaves, suggesting that I. latifolius had greater potential value in the utilization of its leaf active ingredients than the other two species.