INTRODUCTION

The spruce bark beetle Ips typographus (L.) is the most important insect pest on Norway spruce Picea abies (L.) Karst in Europe, killing large volumes of mature trees. Tree mortality caused by I. typographus exceeded 150 million m³ from 1950 to 2000 in Europe, and damages have increased substantially in recent years (Grégoire et al., 2015; Hlásny et al., 2021; Jönsson et al., 2012; Schelhaas et al., 2003; Seidl et al., 2011). Due to climate change, damage levels are predicted to increase even more in the future (Seidl et al., 2014). One factor that may contribute to increased damages is an increase in number of generations per year (voltinism) in a warmer climate. Models, based on different climate scenarios and on thermal sums required for I. typographus development, have been used for predicting the increase in voltinism in different parts of Europe in the future (Bentz et al., 2019; Jönsson et al., 2012). It is important that the thermal sums used in such models are based on data for the specific areas included in the models.

Lower developmental threshold (LDT) temperatures limiting I. typographus development have been determined by rearing beetles at different constant temperatures in the laboratory (Annila, 1969; Wermelinger & Seifert, 1998). Most commonly, LDTs of 5 and 8.3°C are assumed for modelling I. typographus generation development. Similarly, accumulated effective thermal sums (accumulated daily mean temperatures above LDT) required for complete development from egg to mature adult were determined either in laboratory (Annila, 1969; Wermelinger & Seifert, 1998) or in field studies (Baier et al., 2007; Berec et al., 2013; Harding & Ravn, 1985; Ogris et al., 2019; Öhrn et al., 2014). In the field studies, thermal sums were calculated from colonization of trap trees to start of emergence of new-generation beetles. Models predicting development rates and generation development, and thus when emergence of the new generation can be expected, are based on known thermal requirements and information about air temperature, topography and solar radiation for a given locality (Baier et al., 2007). A major drawback of studies using trap trees is that, unless beetles are dissected and examined for the presence of mature eggs, it is not known whether emerging new-generation beetles are in a reproductive state or in reproductive diapause (i.e. just emerging from breeding material for hibernation in the litter). No dissections were conducted in the field studies mentioned above. Another issue is the difficulty to apply the results from local studies including a few trap trees to landscape level. That is because it is generally not known to what extent breeding substrates are utilized (or available) at different altitudes and sun exposures which will influence developmental rates. In addition, there may also be local I. typographus adaptations to differences in regional climatic conditions.

An alternative approach to the trap tree studies mentioned above is to investigate weekly trap catches of I. typographus from monitoring programs for the first date of occurrence of new-generation beetles in the summer. Based on the information on start of flight in spring, and temperature data from climate stations, thermal sums required for completion of development and start of flight of new-generation beetles can then be determined. This approach has several advantages: (1) The fact that beetles were attracted by a pheromone bait is a strong indication that they were not in reproductive diapause. (2) The trapped beetles originate from many different localities and types of breeding substrates in the surrounding landscape and thus give a good estimate for when, and at which temperature sum, the flight of the landscape-wide population of new-generation beetles is initiated. (3) Weekly monitoring of I. typographus is conducted in many regions and thus offers easy access to trapping materials.

In northern Europe, bivoltine populations of I. typographus are not predominant. Thus, from a population dynamic perspective, it is important to determine to what extent new-generation beetles reproduce before the winter. Climate chamber experiments, including Swedish I. typographus populations, demonstrated that at shorter day lengths, an increasing proportion of the new-generation beetles entered reproductive diapause and that some of the beetles from northern regions showed an obligatory diapause (Schebeck et al., 2022; M. Schroeder & Dalin, 2017). However, it is very likely that laboratory results regarding induction of diapause do not correspond with field observations under fluctuating temperatures and natural light conditions. Thus, it is difficult to translate laboratory results to certain proportions of reproductive new-generation beetles under field conditions. Analyses of trapping materials may offer a possibility to determine the proportion of total I. typographus seasonal flight activity that is constituted by new-generation flight. This proportion can then be used as a proxy for the influence of new-generation beetles on the population dynamics.

Two morphological traits have been used to distinguish between parent and new-generation beetles of I. typographus: density of bristles on the pronotum and elytra (Harding & Ravn, 1985) and body colour (Öhrn et al., 2014). Harding and Ravn (1985) separated beetles emerging from trap logs into parent beetles and new-generation beetles by the lower density of bristles on the pronotum and elytra of the former. However, the practicality of this method for classifying beetles from trap catches is questionable. Friction between the beetles in the trap, and the possibility that some new-generation adults may already have bored into trees before being trapped, can damage the bristles. Thus, differentiation by colour appears to be a more useful method for classifying the age of beetles collected in pheromone traps.

When beetles develop from pupae to adults, the cuticle is first soft and pale. As the proteins in the cuticle become sclerotized and melanized, the exoskeleton hardens and darkens (Moret & Moreau, 2012; Noh et al., 2016; Thompson et al., 2002). Merker and Wild (1954) reported that yellow/light brown to black beetles were present both in early spring (before flight period) and later in summer in colonized trees. Knowledge of the long-term change in cuticle colour of I. typographus is limited. Thus, a detailed understanding of colour change over the season is required in order to use colours as indicator of new-generation flight activity in the summer. So far, no study on I. typographus or any other bark beetle species has recorded the transitions in colour from the newly-moulted adults until colonization of new trees for a particular cohort of beetles. In addition, no earlier study has used a standardized method to classify I. typographus based on colour.

The aims of this study were: (1) to develop a standardized method to classify I. typographus individuals based on their cuticular colour; (2) to describe the seasonal colour change of I. typographus in breeding material and from trap catches in Sweden, and based on this information to determine the date of flight initiation of the new generation; (3) to determine the thermal sum required from start of flight of parent beetles in spring until onset of new-generation flight in summer along a climatic gradient; and (4) to estimate the proportion of total seasonal trap catch constituted by new-generation beetles as a proxy for their potential influence on population dynamics.

中文翻译：

---

基于被困甲虫表皮颜色季节变化的新一代云杉树皮甲虫发育和飞行起始的热量总和要求

介绍

云杉树皮甲虫Ips Typographyus (L.) 是挪威云杉Picea abies (L.) 喀斯特地区最重要的害虫，会杀死大量成熟树木。从 1950 年到 2000 年，欧洲由I. typographus引起的树木死亡率超过^1.5亿立方米，并且近年来损失大幅增加（Grégoire 等人，  2015 年；Hlásny 等人，  2021 年；Jönsson 等人，  2012 年；Schelhaas等人，  2003 年；Seidl 等人，  2011 年）。由于气候变化，预计未来损害程度会进一步增加（Seidl et al.,  2014）。可能导致损害增加的一个因素是在温暖的气候中每年的世代数增加（伏丁主义）。基于不同气候情景和I. typographus开发所需的热量总和的模型已被用于预测未来欧洲不同地区的 voltinism 增加（Bentz 等人，  2019 年；Jönsson 等人，  2012 年） . 重要的是，此类模型中使用的热量总和基于模型中包含的特定区域的数据。

较低的发育阈值 (LDT) 温度限制了I. typographus的发育，这是通过在实验室中以不同的恒定温度饲养甲虫来确定的 (Annila,  1969 ; Wermelinger & Seifert,  1998 )。最常见的是，假设 LDT 为 5°C 和 8.3°C，用于建模I.typgraphus生成开发。同样，在实验室（Annila，  1969；Wermelinger & Seifert，  1998）或现场研究（Baier 等，  2007；Berec 等人，  2013 年；Harding & Ravn， 1985；食人魔等人，  2019；Öhrn 等人，  2014 年）。在田间研究中，热量总和是从陷阱树的定殖到新一代甲虫出现的开始计算的。预测发展速度和发电发展的模型，从而预测何时出现新一代，是基于已知的热需求和特定地区的气温、地形和太阳辐射信息（Baier 等人，  2007 年））。使用诱捕树进行研究的一个主要缺点是，除非对甲虫进行解剖并检查成熟卵的存在，否则不知道新兴的新一代甲虫是否处于生殖状态或生殖滞育（即刚刚从繁殖材料中出现）在垫料中冬眠）。在上述实地研究中没有进行解剖。另一个问题是难以将当地研究的结果（包括一些陷阱树）应用到景观层面。这是因为通常不知道在不同的海拔高度和阳光照射下，育种基质在多大程度上被利用（或可用），这将影响发育速度。此外，还可能存在对区域气候条件差异的局部I. typographus适应。

上面提到的陷阱树研究的另一种方法是调查每周捕捞的I. typographus来自夏季新一代甲虫首次出现日期的监测计划。根据春季开始飞行的信息和气候站的温度数据，可以确定新一代甲虫完成开发和开始飞行所需的热量总和。这种方法有几个优点：（1）甲虫被信息素诱饵吸引的事实强烈表明它们没有处于生殖滞育状态。(2) 被捕获的甲虫来自周围景观中许多不同的地点和类型的繁殖基质，因此可以很好地估计何时以及在什么温度总和下，开始了新一代甲虫全景观种群的飞行. (3) 每周监测I. typographus在许多地区进行，因此很容易获得诱捕材料。

在北欧，I. typographus的二化种群并不占主导地位。因此，从种群动态的角度来看，确定新一代甲虫在冬季之前繁殖的程度非常重要。气候室实验（包括瑞典I. typographus种群）表明，在较短的日长下，越来越多的新一代甲虫进入生殖滞育，并且来自北部地区的一些甲虫表现出强制性滞育（Schebeck 等，  2022 ; M. Schroeder & Dalin,  2017）。然而，关于诱导滞育的实验室结果很可能与在波动温度和自然光条件下的实地观察不相符。因此，在野外条件下，很难将实验室结果转化为一定比例的繁殖新一代甲虫。诱捕材料的分析可能为确定由新一代飞行构成的I. typographus季节性飞行活动总量的比例提供了可能性。然后，这个比例可以用作新一代甲虫对种群动态影响的代表。

两种形态特征已被用于区分I. typographus的亲代和新一代甲虫：前胸背板和鞘翅上的刚毛密度 (Harding & Ravn,  1985 ) 和体色 (Öhrn et al.,  2014 )。哈丁和拉文（1985) 通过前者的前胸背板和鞘翅上较低的刷毛密度，将从诱捕原木中出现的甲虫分为亲代甲虫和新一代甲虫。然而，这种从诱捕器中对甲虫进行分类的方法的实用性值得怀疑。陷阱中甲虫之间的摩擦，以及一些新一代成虫在被困之前可能已经钻入树中的可能性，可能会损坏刷毛。因此，按颜色区分似乎是对信息素陷阱中收集的甲虫年龄进行分类的更有用的方法。

当甲虫从蛹发育成成虫时，表皮首先是柔软而苍白的。随着角质层中的蛋白质硬化和黑化，外骨骼变硬和变暗（Moret & Moreau，  2012；Noh 等人，  2016；Thompson 等人，  2002）。Merker 和 Wild ( 1954 ) 报告说，黄色/浅棕色到黑色的甲虫在早春（飞行期之前）和夏季后期在定殖的树木中都存在。对I. typographus角质层颜色长期变化的了解是有限的。因此，需要详细了解季节的颜色变化，才能将颜色用作夏季新一代飞行活动的指标。到目前为止，还没有关于I. typographus的研究或任何其他树皮甲虫物种记录了从新蜕皮的成虫到特定甲虫群的新树定殖的颜色转变。此外，更早的研究没有使用标准化的方法来根据颜色对I. typographus进行分类。

本研究的目的是：（1）开发一种标准化的方法，根据表皮颜色对I. typographus个体进行分类；(2) 描述瑞典育种材料和捕捞鱼中印章鱼的季节性颜色变化，并根据该信息确定新一代飞行开始日期；(3) 确定从春季亲代甲虫开始飞行到夏季开始新一代飞行沿气候梯度所需的热量总和；(4) 估计由新一代甲虫构成的季节性陷阱捕获总量的比例，作为其对种群动态的潜在影响的代表。