Spatial genetic structure and dispersal of giant pandas on a mountain-range scale

Understanding the spatial genetic structure of populations can provide insight into the ecological or evolutionary processes of the species, and enable wise conservation decisions. We examined the spatial genetic structure of a giant panda (Ailuropoda melanoleuca) population in a heterogeneous mountainous landscape using noninvasive genetic sampling and 12 microsatellite loci. Nonrandom genetic structure was detected through spatial autocorrelation analysis, demonstrating a significantly positive autocorrelation over closer distances. Additional spatial analyses showed significantly positive genetic correlation among spatially-proximate males, and no correlation among females and among male–female pairs. These findings suggest a female-biased dispersal pattern and cryptic family grouping among giant pandas on a large mountain-range scale. The spatial extent of genetic structure occurred within 12.5 km, measured by a least-cost path distance model integrating information of habitat quality and habitat preferences of this species. Using the bearing analysis of PASSAGE, we found that directional genetic autocorrelations were in agreement with habitat structure, and habitat heterogeneity may affect the direction of giant panda dispersal. The characterization of spatial genetic structure can provide potentially valuable information for the conservation and management of giant pandas and their habitat.     

Evidence for female-biased dispersal in the protandrous hermaphroditic Asian Seabass, Lates calcarifer

Movement of individuals influences individual reproductive success, fitness, genetic diversity and relationships among individuals within populations and gene exchange among populations. Competition between males or females for mating opportunities and/or local resources predicts a female bias in taxa with monogamous mating systems and a male-biased dispersal in polygynous species. In birds and mammals, the patterns of dispersal between sexes are well explored, while dispersal patterns in protandrous hermaphroditic fish species have not been studied. We collected 549 adult individuals of Asian seabass (Lates calcarifer) from four locations in the South China Sea. To assess the difference in patterns of dispersal between sexes, we genotyped all individuals with 18 microsatellites. Significant genetic differentiation was detected among and within sampling locations. The parameters of population structure (F(ST)), relatedness (r) and the mean assignment index (mAIC), in combination with data on tagging-recapture, supplied strong evidences for female-biased dispersal in the Asian seabass. This result contradicts our initial hypothesis of no sex difference in dispersal. We suggest that inbreeding avoidance of females, female mate choice under the condition of low mate competition among males, and male resource competition create a female-biased dispersal. The bigger body size of females may be a cause of the female-biased movement. Studies of dispersal using data from DNA markers and tagging-recapture in hermaphroditic fish species could enhance our understanding of patterns of dispersal in fish.     

Identifying core habitats and corridors for giant pandas by combining multiscale random forest and connectivity analysis

Habitat loss and fragmentation are widely acknowledged as the main driver of the decline of giant panda populations. The Chinese government has made great efforts to protect this charming species and has made remarkable achievements, such as population growth and habitat expansion. However, habitat fragmentation has not been reversed. Protecting giant pandas in a large spatial extent needs to identify core habitat patches and corridors connecting them. This study used an equal‐sampling multiscale random forest habitat model to predict a habitat suitability map for the giant panda. Then, we applied the resistant kernel method and factorial least‐cost path analysis to identify core habitats connected by panda dispersal and corridors among panda occurrences, respectively. Finally, we evaluated the effectiveness of current protected areas in representing core habitats and corridors. Our results showed high scale dependence of giant panda habitat selection. Giant pandas strongly respond to bamboo percentage and elevation at a relatively fine scale (1 km), whereas they respond to anthropogenic factors at a coarse scale (≥2 km). Dispersal ability has significant effects on core habitats extent and population fragmentation evaluation. Under medium and high dispersal ability scenarios (12,000 and 20,000 cost units), most giant panda habitats in the Qionglai mountain are predicted to be well connected by dispersal. The proportion of core habitats covered by protected areas varied between 38% and 43% under different dispersal ability scenarios, highlighting significant gaps in the protected area network. Similarly, only 43% of corridors that connect giant panda occurrences were protected. Our results can provide crucial information for conservation managers to develop wise strategies to safeguard the long‐term viability of the giant panda population.     

Important population viability analysis parameters for giant pandas (Aliuropoda melanoleuca)

Population viability analysis(PVA) is a tool to evaluate the risk of extinction for endangered species and aid conservation decision-making.The quality of PVA output is dependent on parameters related to population dynamics and life-history;however,it has been difficult to collect this information for the giant panda(Aliuropoda melanoleuca),a rare and endangered mammal native to China,confined to some 30 fragmented habitat patches.Since giant pandas are long-lived,mature late,have lower reproductive rates,and show little sexual dimorphism,obtaining data to perform adequate PVA has been difficult.Here,we develop a parameter sensitivity index by modeling the dynamics of six giant panda populations in the Minshan Mountains,in order to determine the parameters most influential to giant panda populations.Our data shows that the giant panda populations are most sensitive to changes in four female parameters:initial breeding age,reproductive rate,mortality rate between age 0 and 1,and mortality rate of adults.The parameter sensitivity index strongly correlated with initial population size,as smaller populations were more sensitive to changes in these four variables.This model suggests that demographic parameters of females have more influence on the results of PVA,indicating that females may play a more important role in giant panda population dynamics than males.Consequently,reintroduction of female individuals to a small giant panda population should be a high priority for conservation efforts.Our findings form a technical basis for the coming program of giant panda reintroduction,and inform which parameters are crucial to successfully and feasibly monitoring wild giant panda populations.     

Microsatellite marker data suggest sex-biased dispersal in the common frog Rana temporaria

Despite being important models in ecological, evolutionary and conservation biology research, very little is known about the dispersal in anuran amphibians, and juvenile dispersal in particular. Using microsatellite data, we assessed signatures of sex-biased migration in the common frog (Rana temporaria) in Scandinavia. Significant heterozygosity deficiency (FIS) and lower assignment value (mAIc) among females suggest that dispersal in R. temporaria is female biased. Also variance of assignment (vAIc), estimated separately for the two sexes, was consistent with this inference, although the difference was not statistically significant. Possible proximate and ultimate explanations for female-biased dispersal in amphibians are discussed.     

四川省大熊猫保护地生态安全及其时空演变

大熊猫是生态保护的旗舰物种,保护大熊猫及其栖息地具有重要的示范作用和科学价值。中国致力于建设以国家公园为主体的自然保护地体系,分析大熊猫保护地生态安全,为建立大熊猫国家公园提供理论依据,具有重要意义。以四川省为例,选取被划入或将来可能被划入大熊猫保护地的典型县域,构建大熊猫保护地生态安全评价指标体系,采用熵权法、层次分析法进行综合评价,并结合空间相关性分析,从时间和空间两个维度对大熊猫保护地生态安全状况进行时空动态分析。结果表明：（1）2003-2017年四川省大熊猫保护地生态安全综合指数呈波动性上升趋势,生态环境改善显著,但仍有部分县域出现不同程度的环境恶化现象。（2）各县域生态安全状况表现出较强的差异性,并且相邻县域生态安全指数存在显著的空间正相关性和空间集聚性。（3）大熊猫保护地生态安全与周边社会经济发展之间矛盾依然尖锐,相邻县域之间的经济发展和生态保护状况相互影响的作用明显,需联合治理,共同促进生态平衡,提高大熊猫及其栖息地保护效果。     

Inbreeding and inbreeding avoidance in wild giant pandas

Inbreeding can have negative consequences on population and individual fitness, which could be counteracted by inbreeding avoidance mechanisms. However, the inbreeding risk and inbreeding avoidance mechanisms in endangered species are less studied. The giant panda, a solitary and threatened species, lives in many small populations and suffers from habitat fragmentation, which may aggravate the risk of inbreeding. Here, we performed long‐term observations of reproductive behaviour, sampling of mother–cub pairs and large‐scale genetic analyses on wild giant pandas. Moderate levels of inbreeding were found in 21.1% of mating pairs, 9.1% of parent pairs and 7.7% of panda cubs, but no high‐level inbreeding occurred. More significant levels of inbreeding may be avoided passively by female‐biased natal dispersal rather than by breeding dispersal or active relatedness‐based mate choice mechanisms. The level of inbreeding in giant pandas is greater than expected for a solitary mammal and thus warrants concern for potential inbreeding depression, particularly in small populations isolated by continuing habitat fragmentation, which will reduce female dispersal and increase the risk of inbreeding.     

Vocal discrimination of potential mates by female giant pandas (Ailuropoda melanoleuca)

In the current study, we used male giant panda (Ailuropoda melanoleuca) bleats in a habituation–discrimination paradigm to determine whether females discriminate between the vocalizations of different males. We found that females habituated to the bleats of a specific male showed a significant dishabituation when they were presented with bleats from a novel male. Further playbacks, in which we standardized the mean fundamental frequency (pitch) and amplitude modulation of male bleats, indicated that amplitude modulation is the key feature that females attend to when discriminating between male callers. Our results show that female giant pandas can discriminate between the vocalizations of potential mates and provide a platform for further studies investigating the functional role of caller identity in giant panda sexual communication.     

Non-invasive giant panda paternity exclusion

Giant panda hair samples obtained by noninvasive methods served as a source of DNA for amplification of seven giant panda microsatellite loci utilizing the polymerase chain reaction. Thirteen giant pandas held in Chinese zoos were tested for identification of paternity. Some males listed as sires have been excluded as the biological father of captive-born giant pandas. Because of the death of some potential sires, paternity is still not assigned for some giant pandas, although there is a high likelihood that paternity assignment could be made if postmortem samples are available for genetic analysis. The DNA microsatellite variation assayed by the test we have developed provides a rapid, highly informative, and noninvasive method for paternity identification in giant pandas. © 1994 Wiley-Liss, Inc.     

繁殖-育幼期雌性大熊猫的空间利用与活动模式特征

繁殖期间的空间利用与活动模式特征是野生动物长期适应环境的具体表现,研究野生动物繁殖期间行为特征与策略是动物生态学研究中最重要的基础问题之一。2010年3月至2012年3月,我们利用内置记录活动水平传感器的GPS项圈记录了1只受孕、产仔并育幼的野生大熊猫（Ailuropoda melanoleuca）的活动位点和活动水平。研究了该大熊猫各繁殖阶段（交配后期、产仔期和育幼期）的空间利用与活动模式特征。结果表明：在交配后期（2010年春季,即4-6月）,雌性大熊猫活动空间范围较大为3.49 km²,其日平均活动距离较大,活动水平也相对较强;在产仔期前后（2010年夏秋季,即7-10月）,雌性大熊猫的活动范围明显缩小为0.42 km²,日平均活动距离和活动水平都明显减低;自2010年冬季（2010年11月至2011年3月）开始雌性大熊猫带仔生活,其家域面积逐渐增大,且趋向稳定 （0.84~1.19 km²）,日平均活动距离和活动水平都开始逐渐增大。雌性大熊猫在求偶交配、受孕、产仔和育幼过程中的空间利用与活动模式特征反映了大熊猫在繁殖期间的行为策略。本研究结果可为繁殖期间大熊猫及栖息地的保护管理政策制定提供科学依据。     

Factors Affecting the Outcome of Artificial Insemination Using Cryopreserved Spermatozoa in the Giant Panda (Ailuropoda melanoleuca)

Artificial insemination (AI) is an important component of captive breeding programs for endangered species, such as the giant panda. The panda has been the subject of increasingly successful captive breeding programs involving a compilation of assisted breeding techniques, including AI using cryopreserved spermatozoa. AI implementation is currently hampered by a lack of understanding of the factors that may cause failure. We investigated factors influencing the probability of success of AI for 14 giant panda females housed at the China Center for Research and Conservation of the Giant Panda (CCRCGP) inseminated in a total of 20 instances using cryopreserved spermatozoa from 11 males currently residing in 6 different captive breeding institutions. One of the pandas was the oldest giant panda female to ever successfully conceive from AI (20.5 years old). The success of AI was significantly affected by the timing of AI in relationship to both timing of peak urinary estrogen of the female and percent decline in urinary estrogen between the peak level and the first AI attempt. Our results suggest that the window for successful AI in giant pandas may be narrower than previously suspected, although individual differences in rates of decline in urinary estrogen may reflect some degree of variation in this crucial window across females. Our results are consistent with recent research on pandas and other species that demonstrates the efficacy of cryopreserved spermatozoa for AI and highlights the need for more in‐depth analysis of factors related to female physiology that may influence its success. Zoo Biol 31:561‐573, 2012. © 2011 Wiley Periodicals, Inc.     

No evidence for MHC‐based mate choice in wild giant pandas

Major histocompatibility complex genes (MHC), a gene cluster that controls the immune response to parasites, are regarded as an important determinant of mate choice. However, MHC‐based mate choice studies are especially rare for endangered animals. The giant panda (Ailuropoda melanoleuca), a flagship species, has suffered habitat loss and fragmentation. We investigated the genetic variation of three MHC class II loci, including DRB1, DQA1, and DQA2, for 19 mating‐pairs and 11 parent‐pairs of wild giant pandas based on long‐term field behavior observations and genetic samples. We tested four hypotheses of mate choice based on this MHC variation. We found no supporting evidence for the MHC‐based heterosis, genetic diversity, genetic compatibility and “good gene” hypotheses. These results suggest that giant pandas may not use MHC‐based signals to select mating partners, probably because limited mating opportunities or female‐biased natal dispersal restricts selection for MHC‐based mate choice, acknowledging the caveat of the small sample size often encountered in endangered animal studies. Our study provides insight into the mate choice mechanisms of wild giant pandas and highlights the need to increase the connectivity and facilitate dispersal among fragmented populations and habitats.     

Sex biases in kin shoaling and dispersal in a cichlid fish

Animal dispersal is associated with diverse costs and benefits that vary among individuals based on phenotype and ecological conditions. For example, females may disperse when males benefit more from defending territories in familiar environments. Similarly, size differences in dispersal propensity may occur when dispersal costs are size-dependent. When individuals do disperse, they may adopt behavioral strategies that minimize dispersal costs. Dispersing fish, for example, may travel within shoals to reduce predation risks. Further, kin shoaling may augment inclusive fitness by reducing predation of relatives. However, studies are lacking on the role of kin shoaling in dispersal. We explored how sex and size influence dispersal and kin shoaling in the cichlid Neolamprologus caudopunctatus. We microsatellite genotyped over 900 individuals from two populations separated by a potential dispersal barrier, and documented patterns of population structure, migration and within-shoal relatedness. Genetic differentiation across the barrier was greater for smaller than larger fish, suggesting larger fish had dispersed longer distances. Females exhibited weaker genetic differentiation and 11 times higher migration rates than males, indicating longer-distance female-biased dispersal. Small females frequently shoaled with siblings, possibly offsetting dispersal costs associated with higher predation risks. In contrast, small males appeared to avoid kin shoaling, possibly to avoid local resource competition. In summary, long-distance dispersal in N. caudopunctatus appears to be female-biased, and kin-based shoaling by small females may represent a behavioral adaptation that reduces dispersal costs. Our study appears to be the first to provide evidence that sex differences in dispersal influence sex differences in kin shoaling.     

Dispersal is not female biased in a resource-defence mating ungulate, the European roe deer

Dispersal is frequently more prevalent in one sex compared to the other. Greenwood proposed that patterns of sex-biased dispersal among birds and mammals are linked to their mating strategies. For species where males defend resources rather than females, he predicted female-biased dispersal, because males should remain at their birth site where they are familiar with the distribution of the resources that they must defend. Greenwood's hypothesis has been extensively supported among birds, where most species exhibit a resource-defence mating strategy. However, almost no equivalent information is available for mammals as males generally defend mates in this group. An exception is the European roe deer, a resource-defence mating ungulate. We thus tested Greenwood's hypothesis on this atypical mammalian model, looking for female-biased dispersal using sex-specific inter-individual genetic distances. We conclusively show that gene flow is not higher among females compared to males in the studied roe deer population, and hence that dispersal is not female-biased, suggesting that male mating strategy is not the primary selective force driving the evolution of dispersal in roe deer. We discuss the role of female mate choice and intra-sexual competition as possible alternative selective pressures involved.     

Female giant panda (Ailuropoda melanoleuca) chirps advertise the caller's fertile phase

Although female mammal vocal behaviour is known to advertise fertility, to date, no non-human mammal study has shown that the acoustic structure of female calls varies significantly around their fertile period. Here, we used a combination of hormone measurements and acoustic analyses to determine whether female giant panda chirps have the potential to signal the caller''s precise oestrous stage (fertile versus pre-fertile). We then used playback experiments to examine the response of male giant pandas to female chirps produced during fertile versus pre-fertile phases of the caller''s reproductive cycle. Our results show that the acoustic structure of female giant panda chirps differs between fertile and pre-fertile callers and that male giant pandas can perceive differences in female chirps that allow them to determine the exact timing of the female''s fertile phase. These findings indicate that male giant pandas could use vocal cues to preferentially associate and copulate with females at the optimum time for insemination and reveal the likely importance of female vocal signals for coordinating reproductive efforts in this critically endangered species.     

秦岭大熊猫种群扩散格局及研究方法

种群扩散格局是研究种群扩散规律和机制的关键信息,也是制定物种保护对策的重要基础。大型动物种群扩散格局研究方法为扩散生态学研究的薄弱领域,并制约扩散生态学的发展。以秦岭大熊猫为研究对象,根据2000年以来的种群调查数据,基于大熊猫领域的特性,利用GIS的扩展区分析功能和景观分析方法研究了大熊猫种群分布区及动态;基于聚集的特性,利用GIS的核密度分析功能对大熊猫种群多度和聚集状况及空间变化进行了分析。发现2012年的秦岭大熊猫种群分布区较2000年增加5.5%(即15307.8hm~2),高密度种群聚集区从2处变成1处,种群聚集程度进一步增加、聚集格局的完整性大大提升,尤以中密度聚集区增长最显著,种群格局呈明显的分布区扩张、聚集度增加的态势。表明基于物种的生物学特性,立足于种群分布和多度格局变化,通过长期调查和监测可以有效掌握物种的种群扩散格局;大型动物可根据其生物学特性探索可行的方法与量化种群扩散的参数来研究其扩散格局,从而促进大型动物种群扩散研究的开展。     

汶川地震对大熊猫栖息地的影响与恢复对策

 大熊猫是生物多样性保护的旗舰种, 保护大熊猫及其栖息地是保护生物多样性和生态系统功能完整性与稳定性的重要保障体现。汶川地震灾区位于大熊猫重点分布区岷山-邛崃山, 地震及其次生灾害导致该区27个大熊猫自然保护区不同程度受损, 8.3%的大熊猫栖息地因地震而被破坏。地震及其次生灾害对大熊猫栖息地的影响主要表现在: 1) 地震埋没和砸毁大熊猫赖以生存的主食竹, 地震可能诱发主食竹开花, 威胁到大熊猫的健康和食物安全; 2) 地震及其诱发的土壤和山石运动显著影响森林的动态特征, 森林大面积丧失或质量下降; 3) 地震改变大熊猫栖息地生境特征, 大熊猫个体交流的廊道阻断, 形成“生殖孤岛”, 遗传多样性降低, 栖息地破碎化进程加快。应对震后大熊猫栖息地恢复的主要对策有: 1) 重新评估震后大熊猫栖息地质量, 并重新规划现有大熊猫保护区群的布局; 2) 应用地理信息系统、遥感及数学模型等手段与野外实地实证研究相结合的方法, 全面查清震后大熊猫栖息地主食竹资源状况及分布规律并及时监测其动态, 复壮更新大熊猫主食竹; 3) 利用天然植被自然恢复和人工重建等措施恢复因地震而退化或丧失的大熊猫栖息地。     

从北美的研究看大熊猫的种群动态

尽管人们对大熊猫的种群动态了解很少 ,但是我们可以从对相似物种的研究和经历中了解一些基本原理。在不减少对后续的有关大熊猫种群特征、遗传学和行为研究的前提下 ,根据对北美食肉动物种群生物学的理解 ,我提出了下面一般性的结论。首先 ,弹性分析确认 ,大熊猫演变出了确保雌性个体高存活率的生活史。比较而言 ,繁殖率并不重要。成年雌性个体的存活率增加 ,比相应的繁殖输出要导致 5倍的保护效益。第二 ,在可能表现大熊猫种群特征的假设前提下 ,雄性 (甚至成年个体 )的存活率相对而言也是不重要的。第三 ,尽管都认为大熊猫繁殖很缓慢 ,但是从数学上来说 ,如果生境 (以及与其相关的存活率 )允许 ,大熊猫的种群能够比较快地增长。最后 ,北美西部对濒危物种再引入的经验提醒我们 ,保留大片尚未破碎化的生境非常重要。狼在 2 0世纪中叶就在美国西部灭绝了 ,但是目前由于有广阔的生存区域和丰富的食物 ,种群恢复很快。对比而言 ,最近从原野中消失的黑足鼬 ,在种群重建过程中遇到了很大的困难 ,尽管人们在科学上做出了巨大的努力。看来黑足鼬可能只是没有足够的野外栖息地 (猎物 )以维持生存。如果没有足够的栖息地 ,再好的科学也不能拯救大熊猫     

Characterizing the spatial distribution of giant pandas (Ailuropoda melanoleuca) in fragmented forest landscapes

Aim To examine the effects of forest fragmentation on the distribution of the entire wild giant panda (Ailuropoda melanoleuca) population, and to propose a modelling approach for monitoring the spatial distribution and habitat of pandas at the landscape scale using Moderate Resolution Imaging Spectro‐radiometer (MODIS) enhanced vegetation index (EVI) time‐series data. Location Five mountain ranges in south‐western China (Qinling, Minshan, Qionglai, Xiangling and Liangshan). Methods Giant panda pseudo‐absence data were generated from data on panda occurrences obtained from the third national giant panda survey. To quantify the fragmentation of forests, 26 fragmentation metrics were derived from 16‐day composite MODIS 250‐m EVI multi‐temporal data and eight of these metrics were selected following factor analysis. The differences between panda presence and panda absence were examined by applying significance testing. A forward stepwise logistic regression was then applied to explore the relationship between panda distribution and forest fragmentation. Results Forest patch size, edge density and patch aggregation were found to have significant roles in determining the distribution of pandas. Patches of dense forest occupied by giant pandas were significantly larger, closer together and more contiguous than patches where giant pandas were not recorded. Forest fragmentation is least in the Qinling Mountains, while the Xiangling and Liangshan regions have most fragmentation. Using the selected landscape metrics, the logistic regression model predicted the distribution of giant pandas with an overall accuracy of 72.5% (κ = 0.45). However, when a knowledge‐based control for elevation and slope was applied to the regression, the overall accuracy of the model improved to 77.6% (κ = 0.55). Main conclusions Giant pandas appear sensitive to patch size and isolation effects associated with fragmentation of dense forest, implying that the design of effective conservation areas for wild giant pandas must include large and dense forest patches that are adjacent to other similar patches. The approach developed here is applicable for analysing the spatial distribution of the giant panda from multi‐temporal MODIS 250‐m EVI data and landscape metrics at the landscape scale.     

野生大熊猫现状、面临的挑战及展望

截至2003年底,我国野生大熊猫种群数量达1596只,分布在陕西、四川和甘肃3省的45个县境内,总栖息地面积达2304991hm^2。与第2次大熊猫调查相比,野生大熊猫生存状况已得到改善,分布范围扩大、栖息地面积增加、种群数量进一步增长。本文在第3次大熊猫调查的基础上,就野生大熊猫种群及栖息地现状进行了分析,指出未来保护大熊猫所面临的3个方面的挑战,即来自物种自身生物学特性的挑战、栖息地破碎化及隔离小种群未来命运的挑战以及大熊猫保护与社区经济发展需求相冲突的挑战。作者还就我国大熊猫保护前景进行了展望,即自然保护区数量将进一步增加,栖息地状况将进一步改善;种群数量在总体保持稳定的基础上将逐步增长,但局部小种群灭绝风险将加剧;圈养种群将形成能自我维持的种群,圈养个体通过培训将逐步放归到隔离野生小种群中以改变其命运。