大山雀的婚外父权调查

婚配制度作为一种进化稳定对策是动物对某一环境包括种群内部环境适应的结果,在动物生殖过程中具有重要意义.大山雀(Parus major)是一种广域分布物种,研究显示广域分布物种的形态、生理、行为、生态特征及婚配制度在不同地区或种群间存在显著差异,因此,该文选择了分布于中国辽宁仙人洞国家级自然保护区的大山雀(P.m.minor)种群开展其婚配制度研究.野外共采集了22巢大山雀亲代和子代血液样本.结果如下:(1)从11个微卫星位点中筛选出了8个多态性较好的微卫星位点用于大山雀父权鉴定,在母本已知的情况下确定父权的准确率可达99.98％;(2)巢内父权鉴定结果显示,31.8％ (7/22)的巢包含婚外父权,8.12％ (16/197)的子代为婚外子代.与其他森林雀形目鸟类相比,大山雀婚外子代的比例明显偏低(＜10％),每个存在婚外父权巢的婚外子代比例各异(55.6％～9.1％),且无明显规律.     

社会性单配制鸟类婚外父权的发生和影响因素

一雌一雄单配制鸟类中,雌性个体与配偶外雄性发生交配的行为称为婚外交配,继而导致了婚外受精产生婚外子代的现象称为产生了婚外父权。婚外父权广泛存在于鸟类中,针对其发生和影响因素已经成为了鸟类行为生态学研究的热点。本文收集了近十年社会性单配制鸟类婚外父权方面的研究文献,从婚外父权的发生及其影响因素两个方面综述了单配制鸟类婚外父权的研究进展。婚外父权发生原因的探讨主要包括：1、从两性的角度探讨雌雄两性在婚外行为中不同的进化繁殖策略。雄性策略旨在增加自身的繁殖输出;有关雌性策略则提出了确保受精假说、食物供给假说、遗传利益假说等,但目前尚存争议;2、在遗传利益假说中较常见的又分为3个假说：“优秀基因”假说、“遗传相容性”假说和“遗传多样性”假说,该三种假说是针对雌性从遗传方面获得的利益而提出的,不断有报道指出雌性配偶选择会被潜在的雄性遗传特性所影响;3、非遗传利益——母系效应影响婚外父权的进化。一些研究指出遗传质量参数,如体重、身体大小、存活率和免疫应答等方面可能会存在母系效应。婚外父权发生的影响因素这里主要指环境因素,包括繁殖同步性、繁殖密度、栖息地环境、产卵及孵化时机等。由于物种不同,受到环境压力不同,导致婚外父权发生率千差万别。最后本文针对未来的研究方向做出了展望。尽管近十年的研究进一步解释了鸟类婚外父权现象,但是该领域仍然存在并且产生了许多新的未解决的问题,而相关实验操作和理论的完善是深入探讨这些问题的关键。     

人工巢箱繁殖鸟类主要巢捕食者及其影响因素

巢捕食是影响鸟类繁殖成功率的一个重要因素,也是鸟类繁殖生态研究中的一项重要内容。确定鸟类的主要巢捕食者及影响巢捕食的因素对于了解鸟类繁殖成功率、种群增长率及种群数量等具有重要意义。2009—2012年,对辽宁仙人洞国家级自然保护区人工巢箱中繁殖的杂色山雀(Parus varius)、沼泽山雀(P.palustris)、大山雀(P.major)和白眉姬鹟(Ficedula zanthopygia)四种鸟类的巢捕食率及影响巢捕食的因素进行了研究。研究共记录到238个繁殖巢(杂色山雀74巢、沼泽山雀21巢、大山雀118巢、白眉姬鹟25巢),其中35巢被捕食,捕食率为14.7%,雏鸟期被捕食占91.4%。巢捕食率在4种鸟类之间无差异(x~2=0.429,df=3,P=0.934)。以锦蛇(Elaphe spp.)为代表的蛇类是该地区小型森林洞巣鸟类繁殖期主要捕食者,占总捕食率的94.3%。对影响巢捕食的22个相关因子进行二元逻辑斯蒂回归分析发现,坡度、地面裸露率、草本盖度对巢捕食具有显著性影响;出雏时间、坡位、距碎石块距离对巢捕食的影响接近显著水平;而巢高、树粗、巢箱年龄、窝卵数、距路距离等对巢捕食无显著影响。因此,处于坡度较陡,坡位较高,草本覆盖率较高,地面裸露率较低,距碎石块距离较近,且出雏时间较晚的巢更容易被捕食。     

不同性别杂色山雀血浆活性氧和超 氧化物歧化酶与繁殖成效的关系

氧化应激是指活性氧等氧化剂的产生大于抗氧化防御系统清除能力时的不平衡状态,是个体应对内外环境刺激的适应性生理机制,是衡量个体身体状况的综合性生理指标。为探究氧化应激对鸟类繁殖的预测作用,本研究测量了育雏前期(雏鸟6～8日龄)杂色山雀(Sittiparus varius)亲鸟血浆氧化应激分子活性氧和超氧化物歧化酶含量,通过巢箱监测获得了杂色山雀的繁殖参数,采用偏最小二乘回归法分析杂色山雀氧化应激对其雏鸟出飞率和繁殖成功率的预测作用。结果显示,雌性杂色山雀亲鸟血浆活性氧浓度与雏鸟出飞率(n=13,P 0.05)、繁殖成功率(n=13,P 0.01)均呈显著负相关关系,即血浆活性氧水平越低的雌性杂色山雀,其繁殖巢雏鸟出飞率和繁殖成功率越高;雌性杂色山雀亲鸟血浆超氧化物歧化酶浓度与雏鸟出飞率(n=13,P0.05)、繁殖成功率(n=13,P 0.05)无显著相关关系。本研究中这两项血浆氧化应激标记物与杂色山雀雄性亲鸟繁殖成效间均无显著的相关关系。该结果表明,杂色山雀雌性亲鸟活性氧水平对其繁殖成效具有显著的预测作用。     

杂色山雀双亲差异性育雏策略

社会性单配制鸟类的配偶双方在抚育子代时常存在性别差异,不同鸟种的雌雄双亲往往采取不同的育雏策略。以杂色山雀(Sittiparus varius)为研究对象,2017年3—7月对繁殖巢箱进行录像监测,记录杂色山雀育雏期亲代投入情况。分析结果显示:1)双亲递食率在育雏前期(4—6日龄)无显著差异,而育雏后期(10—12日龄)雌性的递食率显著高于雄性。2)雌性亲鸟后期递食率较育雏前期显著增加;而雄性亲鸟育雏前期和后期递食率无显著差异。3)雌性递食率与自身喙宽呈极显著正相关,雄性递食率与双亲体征参数均无相关关系。总的来说,在育雏阶段,杂色山雀雌性亲鸟的递食率随着雏鸟的需求和自身身体质量发生调整,雌性在育雏后期递食率显著升高,而雄性亲鸟递食率无变化,这可能与育雏期双亲投入分工不同有关。     

揭秘鸟类合作繁殖的进化:以青藏高原特有物种地山雀作为模式系统的一项长期努力

鸟类合作繁殖系统的进化机制是行为生态学和进化生态学领域的热点,许多基本理论问题依然悬而未决.青藏高原草甸荒漠气候恶劣、植被贫乏,是地球上独特的生态地理区域.自2004年以来,我们以此极端环境的特有物种地山雀(Parus humilis)为模式系统,探讨合作繁殖系统的特征和适应方式.在掌握合作系统基本结构的基础上,将继续进行长期数据的积累.通过比较帮助者和独立繁殖者的终生适合度,检验亲属选择理论;建立时空尺度上合作繁殖与气候因子的关系,揭露生态压力的作用机制;理清不同种群合作繁殖与婚外父权的关系,阐明遗传单配制作为合作繁殖行为进化的驱动力;联系外源与内源因素,确定合作繁殖物种种群动态的调节机理.地山雀社会系统的神秘需要研究者用不懈的努力去探索.     

杂色山雀体型、子代性别比与鸣唱特征的相关性研究

鸣声在鸣鸟的生活史中具有重要作用,是其与外界进行信息交流最有效的方式之一。鸟类的鸣唱与其个体因素(如体型、子代性别比等)有着十分重要的联系。为了揭示个体体型、子代性别比与鸣唱特征之间的相关性,于2014—2015年3—6月在辽宁省仙人洞国家级自然保护区对杂色山雀指名亚种Parus varius varius的鸣声进行录制,测量了各体型参数,并对每巢雏鸟进行性别鉴定。结果显示:(1)杂色山雀体型与其鸣唱的最高频率具有显著相关性,但单一体型参数(体质量、跗蹠长度)与其鸣声参数相关性均不显著;(2)鸣唱语句长度与子代性别比具有显著相关性,子代性别比与其他鸣声参数均不存在显著相关性。本研究结果有助于进一步了解小型鸟类体型与鸣唱的关系,以及鸣唱与子代性别比之间的关系。     

人工巢箱条件下杂色山雀的巢位选择及其对繁殖成功率的影响

杂色山雀(Parus varius)是一种分布区域极其狭窄的小型森林洞巢鸟类,种群数量稀少,在中国大陆仅见繁殖于辽宁省的东南部山区和毗邻辽宁的吉林省西南部山区,为当地留鸟.为了探讨巢址选择对杂色山雀繁殖的影响,找出影响杂色山雀繁殖成功率的巢址选择方面的主要因子,于2009-2011年3-7月,在辽宁省仙人洞国家级自然保护区通过悬挂人工巢箱,进行杂色山雀对人工巢箱的巢址选择以及不同的巢址对杂色山雀繁殖成功率的影响研究.研究表明:杂色山雀多在针阔混交林中活动和繁殖,对位于赤松与蒙古栎混交林中的巢箱有一定偏好.野外共发现24巢杂色山雀在人工巢箱中繁殖,其中15巢繁殖成功,9巢繁殖失败.对杂色山雀利用的巢址样方主成分分析表明,巢位因子( 19.826％)、乔木因子(17.571％)、灌木因子(13.11％)、光照因子(11.587％)、隐蔽因子(10.562％)和边缘效应因子(7.572％)是影响杂色山雀对人工巢箱选择的重要因子.利用巢箱与对照巢箱相比,两者在距水源距离、距路距离、乔木平均高度、灌木平均高度和植被类型这5个环境变量上存在显著差异.繁殖成功巢与繁殖失败巢相比,繁殖成功的巢箱所在位置距路稍远,坡度较高,乔木最大高度较高,灌木盖度略低于繁殖失败巢箱.人为干扰和天敌捕食是造成杂色山雀繁殖失败的主要原因.以上研究结果表明,巢向偏南、距地面2 m以上、周围乔木高大、灌木平均高度大于1.5m、盖度在45％-55％之间、距水源20 m左右、距路20 m以外的位于针阔混交林边缘的巢箱是杂色山雀繁殖的最优巢址.目前杂色山雀的种群数量还很稀少,希望本研究能对这一珍稀鸟类的保护提供重要参考.     

动物的婚配制度

婚配制度是动物种群个体为获得配偶普遍采取的一种行为策略。一般分为单配制、一雄多雌制、一雌多雄制和混交制。作为动物的一种进化稳定对策,婚配制度又具有一定的可塑性,有时可以逆转,有时又是兼性的。配偶外交配主要存在于单配制物种中特别是单配制鸟类中。其发现表明通过观察个体间联系来确定的“社会性婚配制度”和通过个体实际上的交配对象来描述的“遗传性婚配制度”有可能存在差异。婚配制度影响有害动物的不育控制,在存在繁殖性竞争的情况下,对单配制和一雄多雌制而言,不育效果最佳。     

杂色山雀的反盗食贮食策略

盗食现象在贮食动物中非常普遍,种内竞争者或种间竞争者的盗食是贮藏食物丢失的主要原因之一,同时也是贮食动物贮食行为不断进化的重要选择压力,开展反盗食贮食策略的研究有助于阐释贮食行为进化的原因和对贮食鸟类的保护。杂色山雀(Parus varius)秋季有明显的贮食行为,贮食方式为分散贮食。通过人为投食的方法,以投食点为中心,根据贮食点距投食点距离远近设定了被盗高风险区、被盗中风险区和被盗低风险区,研究杂色山雀个体在无潜在盗食者和有潜在盗食者的情况下,在上述3个风险区贮食比例的变化,探讨杂色山雀个体基于自身以及周围环境条件,在权衡取食及贮藏过程中时间及能量的花费和收益后,其反盗食贮食策略的选择。40只杂色山雀个体贮食策略的统计结果表明,不论潜在盗食者出现与否,杂色山雀个体贮食的总体趋势大致相同,即主要将食物贮藏在中风险区,而高风险区和低风险区贮食比例较低;比较种间和种内潜在盗食者出现的情况下与无潜在盗食者时,杂色山雀个体在各贮食风险区的贮食策略:种间及种内潜在盗食者的出现,都会引起被盗高风险区贮食比例降低(种间潜在盗食者:F=3.174,P0.05;种内潜在盗食者:F=90.475,P0.05),低风险区贮食比例上升(种间潜在盗食者:F=220.440,P0.05;种内潜在盗食者:F=15.651,P0.05);但种间潜在盗食者出现时,杂色山雀个体在被盗中风险区的贮食比例降低(F=143.749,P0.05),而种内潜在盗食者出现时,杂色山雀个体在被盗中风险区贮食比例不变(F=0.776,P0.05),即杂色山雀个体对种间潜在盗食者的出现更加敏感,防范盗食的投入更大。此外,分别比较无潜在盗食者、有种间潜在盗食者和有种内潜在盗食者存在的情况下,雌雄杂色山雀个体在各贮食风险区的反盗食贮食策略,发现其结果也明显不同。无潜在盗食者和种内潜在盗食者出现时,雄性杂色山雀为预防灾难性盗食发生而付出的努力较雌性个体高(无潜在盗食者:高风险区t=4.962,df=16.546,P0.05;中风险区t=﹣0.890,df=29.255,P0.05;低风险区t=﹣2.166,df=30,P0.05。有种内潜在盗食者:高风险区t=﹣0.152,df=29,P0.05;中风险区t=2.352,df=19.568,P0.05;低风险区t=﹣2.287,df=19.563,P0.05);种间潜在盗食者出现时,雌雄杂色山雀反盗食贮食策略趋于一致(高风险区t=1.361,df=29,P0.05;中风险区t=﹣0.194,df=21.529,P0.05;低风险区t=﹣1.599,df=29,P0.05)。     

Lifespan, lifetime reproductive performance and paternity loss of within-pair and extra-pair offspring in the coal tit Periparus ater

The hypothesis that females of socially monogamous species obtain indirect benefits (good or compatible genes) from extra-pair mating behaviour has received enormous attention but much less generally accepted support. Here we ask whether selection for adult survival and fecundity or sexual selection contribute to indirect selection of the extra-pair mating behaviour in socially monogamous coal tits (Periparus ater). We tracked locally recruited individuals with known paternity status through their lives predicting that the extra-pair offspring (EPO) would outperform the within-pair offspring (WPO). No differences between the WPO and EPO recruits were detected in lifespan or age of first reproduction. However, the male WPO had a higher lifetime number of broods and higher lifetime number of social offspring compared with male EPO recruits, while no such differences were evident for female recruits. Male EPO recruits did not compensate for their lower social reproductive success by higher fertilization success within their social pair bonds. Thus, our results do not support the idea that enhanced adult survival, fecundity or within-pair fertilization success are manifestations of the genetic benefits of extra-pair matings. But we emphasize that a crucial fitness component, the extra-pair fertilization success of male recruits, has yet     

Long-term fitness consequences of female extra-pair matings in a socially monogamous passerine

Whether female birds choose extra-pair mating partners to obtain genetic fitness benefits is intensely debated. The most straightforward and crucial test of 'good genes' models of female extra-pair mating is the comparison of naturally 'cross-fostered' maternal half-siblings sharing the same rearing environment as any systematic differences in performance between the two categories of offspring phenotype can be attributed to differential paternal genetic contribution. We analysed local recruitment and first-year reproductive performance of maternal half-siblings in the coal tit (Parus ater), a passerine bird with high levels of extra-pair paternity. We provide a highly comprehensive measure of the long-term fitness consequences of female extra-pair matings based on a large sample of 736 within-pair offspring (WPO) and 368 extra-pair offspring (EPO) from 91 first and 55 second broods, from which 132 breeders recruited into the study population. In contrast to predictions derived from 'good genes' models, we found no differences in local recruitment and seven parameters of first-year reproductive performance when comparing WPO and EPO. These results question the universal validity of findings in other bird species supporting 'good genes' models, particularly as they are based on the best approximation to female fitness obtained so far.     

Cuckoldry and recapture probability of adult males are not related in the socially monogamous coal tit ( Parus ater)

Despite substantial research effort, the benefits of female extra-pair matings in socially monogamous bird species remain elusive. The good genes hypothesis assumes that females engage in extra-pair copulations with males of superior genetic quality compared to their respective social mate. Therefore, a negative association between the degree of cuckoldry and male survival is predicted, if genetic quality is phenotypically reflected by high viability. Furthermore, genetic sires of extra-pair offspring (EPO) should survive better than the social fathers they cuckolded. We tested these predictions in a nestbox population of the coal tit (Parus ater), a socially monogamous passerine with low breeding dispersal and high rates of extra-pair paternity (EPP). Based on 257 genotyped first broods of two consecutive years, we found no relationship between the incidence of EPP or the proportion of EPO within a given brood and male or female recapture probabilities. Furthermore, recapture rates did not differ between social and genetic fathers of EPO or males that did or did not appear as extra-pair sires in other broods. Our results were not affected by differential (short-range) breeding dispersal with respect to EPP or by other potentially confounding variables. Hence, they are not in accordance with the good genes as viability genes hypothesis.Communicated by F. Bairlein     

Extra-pair mate choice in the female great tit <Emphasis Type="Italic">Parus major</Emphasis>: good males or compatible males

The good genes hypothesis and the genetic compatibility hypothesis are the two main hypotheses that focus on the genetic benefit that a female can gain through her choice of a mate. We tested the two hypotheses on extra-pair mating in the great tit, Parus major. We found that female great tits choose males on the basis of breast stripe width, which is in accordance with the good genes hypothesis. Although females chose less related extra-pair males, the evidence for female choice for compatible males was overall weak. However, our data suggest a post-copulatory mechanism of inbreeding avoidance. The observed individual inbreeding coefficient, F, was similar for within-pair offspring (WPO) and extra-pair offspring (EPO). The observed individual F of WPO was lower than the expected individual F, whereas the observed F of EPO was similar to what was expected. These results highlight the importance of processes after copulation for the outcome of female mate choice. Our study shows that in a system with apparent pre-copulatory female choice for good genes, a post-copulatory mechanism may still promote the production of offspring that carry compatible genes.     

Indirect selection on female extra-pair reproduction? Comparing the additive genetic value of maternal half-sib extra-pair and within-pair offspring

One specific hypothesis explaining the evolution of extra-pair reproduction (EPR) by socially monogamous females is that EPR is under indirect selection because extra-pair offspring (EPO) sired by extra-pair males have higher additive genetic value for fitness than the within-pair offspring (WPO) a female would have produced had she solely mated with her socially paired male. This hypothesis has not been explicitly tested by comparing additive genetic value between EPO and the WPO they replaced. We show that the difference in additive genetic breeding value (BV) between EPO and the WPO they replaced is proportional to the genetic covariance between offspring fitness and male net paternity gain through EPR, and estimate this covariance with respect to offspring recruitment in free-living song sparrows (Melospiza melodia). Recruitment and net paternity gain showed non-zero additive genetic variance and heritability, and negative genetic covariance. Opposite to prediction, EPO therefore had lower BV for recruitment than the WPO they replaced. We thereby demonstrate an explicit quantitative genetic approach to testing the hypothesis that EPR allows polyandrous females to increase offspring additive genetic value, and suggest that there may be weak indirect selection against female EPR through reduced additive genetic value for recruitment of EPO versus WPO in song sparrows.     

Genetic evaluation of the mating system in the blue-and-yellow macaw (Ara ararauna, Aves, Psittacidae) by DNA fingerprinting

More than 90% of birds are socially monogamous, although genetic studies indicate that many are often not sexually monogamous. In the present study, DNA fingerprinting was used to estimate the genetic relationships between nestlings belonging to the same broods to evaluate the mating system in the socially monogamous macaw, Ara ararauna. We found that in 10 of 11 broods investigated, the nestlings showed genetic similarity levels congruent with values expected among full-sibs, suggesting that they shared the same parents. However, in one brood, the low genetic similarity observed between nestlings could be a result of intraspecific brood parasitism, intraspecific nest competition or extra-pair paternity. These results, along with available behavioral and life-history data, imply that the blue-and-yellow macaw is not only socially, but also genetically monogamous. However, the occurrence of eventual cases of extra-pair paternity cannot be excluded.     

Intensity of nest defence is not related to degree of paternity in the willow tit Parus montanus

We asked whether willow tit Parus montanus males adjust their parental care according to their paternity in current brood. The origin of the nestlings was determined by using molecular technique, and the studied broods were assigned into extra-pair paternity (EPP) broods, if at least one nestling was fathered by another male, and truly monogamous broods. Over 3  years, 14 of 40  broods (35%) included EP-offspring, and 29 of 273  nestlings (11%) were EP-young. Intensity of parental care was measured with risk-taking against a potential predator, mounted stoat Mustela erminea . The results showed that risk-taking by EPP males did not differ from that by monogamous males. Neither was the sexual difference in risk-taking different at EPP and monogamous broods. Our results are consistent with the hypothesis that males do not adjust their level of care to paternity, perhaps because they have no reliable cues for assessing their paternity. This may be related to the success of mate-guarding in their breeding environment, closed forests. Guarding is seemingly successful as the EPP levels are rather low, but it is not totally sure making the potential costs, rejection of own young, too high. We also discuss other population characteristics which may further prevent the evolution of paternity assessment in northern willow tits.     

Extra pair paternity in birds: a review of interspecific variation and adaptive function

The application of molecular genetic techniques has revolutionized our view of avian mating systems. Contrary to prior expectations, birds are only very rarely sexually monogamous, with 'extra-pair offspring' found in approximately 90% of species. Even among socially monogamous species, over 11% of offspring are, on average, the result of extra-pair paternity (EPP). Based on over 150 molecular genetic studies of EPP in birds, we review two topical areas: (i) ecological explanations for interspecific variation in the rate of EPP; and (ii) evidence bearing on the adaptive function of EPP. We highlight the remaining challenges of understanding the relative roles of genes and ecology in determining variation between taxa in the rate of extra paternity, and testing for differences between extra-pair offspring and those sired within-pair.     

Differences in perceived predation risk associated with variation in relative size of extra‐pair and within‐pair offspring

Extra‐pair paternity (EPP) is a widespread phenomenon in birds. Researchers have long hypothesized that EPP must confer a fitness advantage to extra‐pair offspring (EPO), but empirical support for this hypothesis is definitively mixed. This could be because genetic benefits of EPP only exist in a subset of environmental contexts to which a population is exposed. From 2013 to 2015, we manipulated perceived predator density in a population of tree swallows (Tachycineta bicolor) breeding in New York to see whether fitness outcomes of extra‐pair and within‐pair offspring (WPO) varied with predation risk. In nests that had been exposed to predators, EPO were larger, longer‐winged and heavier than WPO. In nonpredator nests, WPO tended to be larger, longer‐winged and heavier than EPO, though the effect was nonsignificant. We found no differences in age, morphology or stress physiology between extra‐pair and within‐pair sires from the same nest, suggesting that additive genetic benefits cannot fully explain the differences in nestling size that we observed. The lack of an effect of predator exposure on survival or glucocorticoid stress physiology of EPO and WPO further suggests that observed size differences do not reflect more general variation in intrinsic genetic quality. Instead, we suggest that size differences may have arisen through differential investment into EPO and WPO by females, perhaps because EPO and WPO represent different reproductive strategies, with each type of nestling conferring a fitness advantage in specific ecological contexts.     

Weather conditions affect levels of extra-pair paternity in the reed bunting Emberiza schoeniclus

Extra-pair paternity (EPP) is common in many socially monogamous birds, but large variations in frequency of EPP are found both between and within species. Local ecological factors can affect the costs and benefits of extra-pair mating behaviour, and may therefore influence the chance that individuals engage in extra-pair copulations (EPCs). We investigated the effect of weather conditions during the peak fertile period of the female on the levels of EPP in reed buntings Emberiza schoeniclus . The reed bunting is a socially monogamous passerine, with extremely high levels of EPP (50% of offspring in 80% of broods). We found that higher daily minimum temperatures and more rainfall during the peak fertile period were associated with lower proportions of EPP. As during adverse weather conditions individuals have to invest more in self maintenance, we suggest that during long periods of rain the extra-pair mating behaviour of all individuals will be restricted, leading to lower proportions of EPP. During cold mornings, time-consuming activities such as mate guarding are likely to be more strongly affected than less time-consuming activities such as EPCs, leading to higher proportions of EPP.