IN THE winter of 2006 beekeepers in America noticed something odd—lots of their hives were dying for no obvious reason. As the months passed, reports of similar phenomena began coming in from their European counterparts. Mystified scientists coined the label “colony collapse disorder” (CCD) to describe what was happening. Since then, much brow-sweat has been expended trying to work out just what CCD really is.

2006年冬，美国养蜂人注意到奇怪的现象，他们的蜜蜂成批死掉，原因不明。几个月后，类似的现象也出现在欧洲同行的报告上。困惑的科学家们给这个现象贴上了“蜂群衰竭失调”（CCD）的标签。自那时起，为揭开CCD的面纱，人们不知道多少次抹去额头的汗水。

Dying bees are a problem, and not just for apiarists. Bees pollinate many of the world’s crops—a service estimated to be worth $15 billion a year in America alone. And there is no shortage of theories to explain the insects’ decline. Climate change, habitat destruction, a paralysing virus, fungal infection and even a plague of parasitic mites have all been proposed. But one of the leading ideas is that the bees are suffering from the effects of neonicotinoids, a class of commonly used pesticides, introduced in the 1990s, which are toxic to insects but much less so to mammals.

蜜蜂之死不仅令养蜂家头痛。蜜蜂给世界上的很多庄稼授粉，仅在美国，这种服务每年价值150亿美元。尽管对蜜蜂数量下降的原因提出了形形色色的理论，如气候变化、栖息地遭破坏、麻痹病毒、霉菌感染，甚至还有寄生虫肆虐。但其中一个主导观点是蜜蜂正在遭受新烟碱的侵害，二十世纪九十年代人们引入这种杀虫剂，它对昆虫有毒，但对哺乳动物的毒性较小，使用范围广泛。

Two papers published this week in Science lend weight to this idea. The first, from a group led by Penelope Whitehorn and David Goulson of the University of Stirling, in Britain, examined the effects these insecticides have on bumblebees, which are closely related to honeybees. Bumblebees are less studied than their honeybee cousins, but they also pollinate many commonly eaten crops, including strawberries, raspberries and runner beans.

本期科学杂志刊登的两篇论文证实了这种观点。篇出自英国斯特林大学Penelope Whitehorn 和 David Goulson 指导的团队，他们检验了这些杀虫剂给大黄蜂带来的影响，大黄蜂和蜜蜂的关系密切。和同宗的蜜蜂比起来，对大黄蜂的研究要少一些。但它们给很多可食作物传粉，如草莓、树莓和红花菜豆。

The two researchers and their colleagues raised 75 bumblebee colonies in their laboratory. They exposed some, via contaminated pollen and sugar water, to high doses of imidacloprid, a type of neonicotinoid insecticide. Others were exposed to low doses (half as much as the high dose), or to no dose at all. Then, after two weeks of this treatment, the colonies were taken into the outside world and left there for six weeks, to see how the bees did.

两位研究人员和同事们在实验室饲养了七十五个大黄蜂蜂群。他们用受污染的花粉、糖水

将一些蜂群暴露在高剂量吡虫啉（一种新烟碱杀虫剂）的环境里，一些蜂群暴露在低剂量（高剂量的一半）杀虫剂的环境里，或者不加一点杀虫剂。接着经过两周的处理，把这些蜂群放在室外六周，观察蜂的行动。

All of the doses of imidacloprid, both high and low, that Dr Whitehorn gave her bees were “sublethal”—in other words, insufficient to kill the insects outright. Firms that produce pesticides, and the authorities that regulate them, are aware of the importance of bees to food production, and new products must be tested to make sure they are not fatal to helpful insects. But Dr Whitehorn found that even non-lethal doses of pesticide were bad for bees. Both the high-dose and the low-dose colonies grew more slowly than the undosed ones, gaining 8-12% less weight on average.

使用吡虫啉的蜂群，无论剂量大小，Whitehorn博士把“亚致死量”用在她的蜜蜂上，换句话说，不足以complete杀死昆虫。杀虫剂生产厂家和管理他们的机构意识到蜜蜂对食品生产的重要性，新产品要经过检测，保证它们不会对有益的昆虫造成致命伤害。但Whitehorn博士发现即使非致命性杀虫剂也会对蜜蜂有害。受到高剂量和低剂量杀虫剂影响的蜂群和没有受杀虫剂影响的同类比起来长得要慢。体重平均降低8-12%。

More importantly, the pesticides drastically inhibited the production of queens, which are needed to establish new nests each spring. (Unlike those of honeybees, bumblebee colonies do not survive the winter; they must be refounded by a hibernating queen.) The undosed colonies produced 13.7 queens, on average. Those given a small dose of insecticide produced two. Those given a high dose produced just 1.4. Worryingly, even colonies given the high dose may have got off lightly compared with their wild brethren. The researchers note that another British study found levels of imidacloprid in rape crops that were seven times higher than the food supplied by the researchers.

最重要的是，杀虫剂强烈地影响到春季筑造新巢所需的蚁后的生产。（和蜜蜂不同，大黄蜂蜂群在冬天不能存活，它们必须由冬眠的蚁后重建）。未受杀虫剂影响的蜂群产生13.7个蚁后。受低剂量影响的蜂群产生两个，受高剂量杀虫剂影响的蜂群产生1.4个。令人忧心的是，即便受高剂量杀虫剂影响的蜂群可能要比它们在野外的同伴受到的危害低一些。研究人员指出另一个英国研究项目发现油菜作物里的吡虫啉含量要比研究人员提供的食物里的吡虫啉含量高七倍。

Dr Whitehorn’s paper does not propose a mechanism by which pesticides do their damage. But the second study, by a group led by Mickaël Henry at the French National Institute for Agricultural Research, in Avignon, may shed some light on the matter. Inspired by previous laboratory-based work, which had suggested that sublethal doses of neonicotinoids damage honeybees’ memories, their ability to forage, and their ability to navigate back to their hive afterwards, Dr Henry decided to conduct some tests in the wild.

Whitehorn的论文没有说明杀虫剂实施破坏的方法。由法国国家农业研究院（位于阿维尼翁 ）的Mickaël Henry带队实施的第二项研究可能这个事情带来曙光。先前实验室工作表明亚致死剂量的新烟碱会损害蜜蜂的记忆、它们的觅食能力和它们返回蜂群的能力，受此启发，Henry博士决定在野外做一些测试。

To that end, he and his colleagues glued tiny radio transmitters to the thoraxes of worker bees. These triggered a detector on the hive whenever a worker bearing one returned from a foraging trip. Some hives were given realistic doses of thiamtethoxam, a variety of neonicotinoid, while others were left alone. Dr Henry found that around twice as many treated bees as untreated ones failed to return to the hive. That, mathematical models indicate, might easily cause a hive to collapse.

为此，他和同事们将微型无线电广播发射机系在工蜂的胸前。在工蜂觅食返回的途中，会在蜂群里触发探测器。给一些蜂群用一定剂量的阿克泰（一种新烟碱 ），其他的则不用，Henry博士发现用药的不能返巢的蜜蜂数量是没有用药的两倍。所以数学模型更容易的显示出一个蜂群的瓦解。

Colony club

蜂群俱乐部

Moreover, even if it did not do so alone, it could be a contributing factor. Many researchers believe the label “colony collapse disorder” covers a multitude of problems; that would account for the long list of possible causes. But neonicotinoids have the explanatory virtue of being a fairly recent development and also one which, as these two pieces of work suggest, could be a common factor in weakening a colony without actually pushing it over the edge. The killer blow would then be administered by something else: a mite infestation, perhaps, or a fungal infection, or whatever else happened to turn up that a healthy hive would have shrugged off. A paper published earlier this year in Naturwissenschaften, for example, showed that even small doses of neonicotinoids weakened bees’ resistance to Nosema, a common fungal parasite.

此外，如果没有单独做这些工作，这会是一个起作用的因素 。很多研究人员相信“蜂群衰竭失调”涵盖了很多问题，可以列出很多原因。但是新烟碱在最近的研究和这两项工作中做给出了解释，它是在没有外部因素的作用下削弱蜂群的一个原因。以下原因也可以被视为蜂群杀手如寄生虫肆虐、霉菌感染，或者导致蜂群健康降低的其他事情。今年早些时候自然科学杂志刊登的一篇论文说小剂量的新烟碱削弱蜜蜂对小孢子虫（一种普通的真菌寄生虫 ）的抵抗力。

A few countries, including France, Germany and Slovenia, have already restricted the use of neonicotinoids because of worries about their effects on bees. It would help other places that are thinking of following suit if more realistic trials were conducted in the future, in conditions that mimic nature as closely as possible in the way that these two experiments have done. That might be more expensive than the present way of doing things, in which tests are mostly confined to laboratories and are concerned with finding out how much insecticide is needed to kill bees outright. But the growing evidence that insecticides damage bees in subtle ways means it would be money well spent.

包括法国、德国和斯洛文尼亚在内的一些国家已经限制了新盐碱的使用，他们担心这种杀虫剂会给蜜蜂造成影响。这有助于其他地方考虑是否要在将来在模拟自然环境的条件和以上两个试验的条件尽可能接近的条件下更多的实际试验。试验受实验室的约束，并且为了能知道多大剂量才能杀死蜜蜂，花费可能要比当前昂贵。越来越多的证据表明杀虫剂对蜜蜂的损害是慢性的，所以这个钱值得花。