土壤生态系统随时间的变化而变迁

Soil Ecosystems Change With Time

ABSTRACT 摘要

“所有生活在我们脚下的动物都不是静止不动的。它们可以移动（移动到很多地方，因为土壤是一个三维空间）以及发生改变（例如，从一个茧变化为一个活跃状态）。因此，在给定的一片田地里的同一片土壤，在冬季和夏季，甚至是在一个阳光明媚的白天与寒风刺骨的晚上，二者相比较，所包含的生物群落也可能有所不同。例如，对土壤里的甲虫幼虫的研究表明，由于幼虫要寻求更优良的生存环境，因此它们出现了季节性的垂直移动。此外，土壤在其形成的过程中也会发生许多变化，因此土壤里的栖息动物也会随之发生改变。以甲螨这种微不足道但种类繁多的土壤螨类而言，科学家们观察到了甲螨群落在十数年到几百年间所发生的变迁。许多研究表明了一个基本但强有力的原则：生态系统并不是静止不动的照片，而是一个不断发生变化的环境。”

All the animals living below our feet are not still. They can move (to a lot of places because the soil is a 3D space) and to change (for example, from a cocoon to an active state). Therefore, the same soil below a given piece of field may not contain the same living communities in winter as in summer, or even during a sunny day compared to a cold night. For example, research on soil beetle larvae showed seasonal vertical movements, as the larvae searched for better living conditions. Moreover, the soil varies a lot during its formation, and consequently its inhabitants also change. In the case of oribatids, a minuscule but diverse group of soil mites, scientists observed changes in the community over dozen to hundreds of years! Many studies showed a basic but powerful principle: ecosystems are not still photographs, but instead are constantly changing environments.

ECOSYSTEMS ARE NOT STATIC PHOTOGRAPHS

生态系统并不是静态的照片

当我们想象生态系统多样性时，我们经常联想到的生态系统大多数都是静止不动、亘古不变的，就像书本上的图片一样，所有的植物和动物都处于一种冻结的平衡状态。在我们的脑海中（以及在许多书本的图片里），植物很容易被食草动物吃掉，食草动物则等待着被食肉动物捕食，而所有的这一切都发生在令人惬意的白天下。但事实并不是我们所想象的那样！生态系统里的大多数动物是在白天活动的，有些动物则只会在晚上出现。植物会根据季节变化生长出不同的可食用部分。整个生态系统甚至会因为森林火灾等大灾难而发生变化。更何况，我们甚至鲜少想象发生在我们脚底下土壤里的多样性的变化。

When we imagine ecosystem diversity, we often picture ecosystems as mostly stable and unchanging, like photographs in a book, with all the plants and animals existing in a frozen state of balance. In our heads (and in many book pictures), plants are readily available for herbivores to eat, and herbivores are waiting to be eaten by carnivores, all under wonderful daylight. But reality is not like that! Most of the animals in an ecosystem move during the day and some of them only appear at night. Plants produce different edible parts depending on the season. The entire ecosystem can even change due to catastrophes like forest fires. Not to mention, we rarely even imagine the diversity that happens in the soil under our feet.

HOW CHANGE WORKS UNDER OUR FEET

    那么，我们脚下的变化是如何发生的呢？

诚然，尽管土壤生物多样性的变化和地表所发生的变化不一定相同，但也会随着时间的变化而变化。首先，在土壤里活动显然会更艰难。蚯蚓，昆虫幼虫、蝼蛄（还有鼹鼠，但我们要关注的是小型无脊椎动物），以及许多其他微小的生物都必须用它们的嘴、爪子或腿来挖掘土壤。较小的生物则利用微小的、充满空气的空间即土壤孔隙，在土壤中移动。

在土壤栖息的生物并不局限于地表动物的水平移动。土壤里的无脊椎动物也可以在同一片地表以下上下移动，我们把这种移动称为“垂直迁移”。垂直迁移可以在一天内进行，也可以跨季节发生。白色蚯蚓是一种非常微小的蠕虫，是被观察到在白天迁移的少数居住在土壤里的动物之一。白蚯蚓会向土壤更深处移动以躲避正午时候干燥的地表环境，待到傍晚时分，它们喜爱的潮湿环境恢复时又会从土壤深处爬出来。这种迁移，是研究土壤里的土壤中型动物最常用的方法之一的基础。这种方法是将土壤样品放在一个漏斗中，漏斗上方挂着一个灯泡，将其干燥，这样所有的小生物就会“逃跑”而落入到底部的收集容器里。（图1）

Of course, soil biodiversity also changes with time, although not necessarily the same way changes happen aboveground. First, movement is certainly more difficult in the soil. Earthworms, insect larvae, mole crickets (also moles, but we are going to focus on small invertebrates), and many other tiny creatures must dig with their mouths, claws, or legs. Smaller creatures move throughout the soil mainly using tiny air-filled spaces called soil pores.Soil inhabitants are not limited to the typical horizontal movements of surface animals. Soil invertebrates can also move up and down beneath the same surface area, which is called vertical migration. Vertical migrations can occur during a single day, or across seasons. Enchytraeids, very tiny worms, are one of the few types of soil-dwelling animals that have been observed to migrate during the day. Enchytraeids move deeper into the soil to escape from dry surface conditions at midday and return from the deep in the evening, when their favorite moist conditions are reestablished. This migration is the basis of one of the most-used methods to study soil mesofauna. This method consists of drying a soil sample in a funnel with a light bulb at the top, so the creatures “escape” by falling to a collection container in the bottom (Figure 1).

          图1-分离土壤无脊椎动物进行研究

一种典型的Tullgren或Berlese漏斗式捕虫器，是以其发明者而命名的。土壤被放置在漏斗的顶部，由一层网纱支撑着。顶部一个灯泡给土壤加热使土壤干燥，迫使土壤里的生物往下移动。当它们从样本土壤中掉下时，它们会落入一个收集容器，这个容器通常充满了一种能维持它们存活的物质。这些收集起来的生物便可以被拿去研究

Figure 1 - Isolating soil invertebrates for study.

A typical Tullgren or Berlese funnel trap, named after its inventors. The soil is placed in the top of a funnel, held up by a layer of mesh. A light bulb heats and dries the soil, forcing the soil organisms to go down. When they drop from the sample, they fall into a collection container, usually filled with a substance that keeps them alive. The organisms can then be studied.

许多土壤里的无脊椎动物可以以抗性形式（resistant forms）存在，从而使它们能够在恶劣的条件下长期生存。地珍珠是一种体型微小圆胖、非常有趣的昆虫，它就是一个很好的例子。它们能在自己周围分泌出一层珍珠似的覆盖物，形成一个球形包囊或处于“休眠”阶段，这种状态往往可以保持几十年！但是，当有了美味的树根时，“包囊”就会发育成贪婪的成虫。如果条件非常好，许多地珍珠物种会克隆自己，使其尽可能地利用有利条件获利。一位倒霉的葡萄园园主可能一整年都看不到微小的地珍珠，但第二年却发现他的庄稼受到了大批成虫的侵扰，

在土壤的表面，许多小动物可以通过风、水被携带，有些甚至可以被其他动物所携带。一些居住在表层的小生物也会以这种方式移动，但所谓的土壤动物的被动散布最近得到了许多研究的关注，因为它可以解释土壤生物的远距离移动。

Many soil invertebrates can exist in resistant forms that allow them to survive harsh conditions for a long time. Ground pearls, small, rounded, and very interesting insects, are a perfect example. They can secrete a pearly covering around themselves, forming a spherical cyst or “resting” stage, in which they can remain for decades! But when delicious roots are available, the cysts develop and become voracious adults. If conditions are really good, many ground pearl species can clone themselves to profit as much as possible from favorable conditions. An unlucky vineyard farmer may not see the tiny ground pearls 1 year, but find his crops infested with adults the next.

At the soil surface, many small animals can be carried by the wind, water, and even by other animals. Some surface-dwelling creatures travel this way as well, but the so-called passive dispersal of soil fauna has gained a lot of research attention lately, as it may explain movements of soil organisms across large distances.

SEASONAL CHANGES

季节性的变化

在我早期的研究工作中，土壤生物的移动并没有像今天那样有所了解，每一个新发现都是如此的激动人心，这些发现包括生活在土壤中的幼虫会发生季节性的垂直移动。

每个月在西班牙南部的沙漠型灌木丛地带的不同地方进行土壤取样，为期两年。土壤样本是从不同深度的土壤中采集的，从表层的枯枝败叶到50cm深处。对每个样本的所有大型无脊椎动物都进行了计数和鉴定。在分析了每个季节和每个深度的土壤里的所有样本后，科学家们发现，一个名叫拟步甲科（Tenebrionidae）的甲虫大家族里的幼虫，它们以有机碎屑为食，每年都做同样的移动。它们在冬季土壤表面的数量比夏季更多（图2）。

During my early years as a researcher, movements of soil organisms were not as understood as they are today and every discovery was very exciting, including the discovery that some soil-living insect larvae perform seasonal vertical migrations [3]!

Soil was sampled in multiple locations every month for 2 years, in a desert-type shrubland in Southern Spain. Soil samples were collected at different depths, from the surface litter down to 50 cm deep. For each sample, all themacroinvertebrates were counted and identified. After analyzing all the samples, from every season and soil depth, scientists found that the larvae of one abundant beetle family called Tenebrionidae, which eat organic debris, made the same movement each year. They were more abundant at the soil surface in winter than they were in summer (Figure 2).

  图2-甲虫幼虫的垂直移动，取决于所处土壤的深度以及所处的季节

在夏季，幼虫在土壤的表层和深层的丰富程度是相等的，但在冬季，它们在土壤表层但丰富程度会更高一些，因为在那里它们可以吃到碎叶，而不会受到夏季炎热干燥的环境的伤害。

  Figure 2 - Vertical migration of beetle larvae, depending on soil depth and season.

In summer, the larvae are equally abundant at the surface and in the deeper levels of the soil, but in the winter they are much more abundant at the surface, where they can feed on leaf litter and not be damaged by the hot, dry conditions present in summer.

在所研究的地带，夏季高温干燥。然而，拟步甲科昆虫最喜欢的食物——碎叶，存在于裸露的土壤表面的“餐厅”如灌木和蚂蚁堆中。因此，这些甲虫的幼虫更喜欢在温和的冬天吞食土壤表层的碎叶，夏季则享用更深层的“餐馆”里的食物，如腐烂的根。当幼虫进行垂直迁移时，它们也为整个生态系统提供了良好的服务。就像大多数生活在潮湿的生态系统的蚯蚓一样，这些坚韧不拔的幼虫在干燥的土壤环境中移动土壤，因此空气、水和有机物质被混合在土壤中，这对土壤的健康是非常有益的。

In the studied area, summers are very hot and dry. However, Tenebrionidae’s favorite dish, litter debris, is found in exposed soil-surface “restaurants,” like shrubs and ant mounds. Therefore, these beetle larvae prefer to devour surface litter debris during the winter’s gentle weather, but enjoy other, deeper “restaurants,” such as decaying roots, in summer. When the larvae perform this vertical migration, they are also doing a great service for the entire ecosystem. Like earthworms in more humid ecosystems, these tough larvae move the soil in arid environments, so air, water, and organic materials are mixed in the soil, which is highly beneficial for soil health.

ECOSYSTEMS CAN GROW… AND EVEN AGE!

生态系统可以发展，甚至可以变老

在不同天气条件和食物可得性下发生的变化并不是生态系统变化的仅有特点。事实上，整个生态系统都可以通过一个被称为“生态系统的演替”的过程而发生变化。科学家们把目光聚焦于一组被称为甲螨（oribatid）的土壤螨类，已经研究出了土壤生物多样性是如何随生态系统的演替而变化的。甲螨体型微小、数量众多、种类多样，这就意味着你可以在一小块土壤样本里找到它们的整个群落。同时也有很多资源可以帮助鉴定各种甲螨的种类，因此它们是用于观察和研究土壤生态系统多样性变化的理想生物体。另外，因为甲螨生活在土壤深处，受阻于只能通过土壤孔隙活动，偶尔通过被动分散才得以移动，因此它们的活动能力也相对有限。因此，甲螨群落是主要通过生态系统的演替来发展的。

Changes in weather conditions and food availability are not the only changing features of ecosystems. In fact, an entire ecosystem can change during a process called ecosystem succession. Scientists have studied how the diversity of soil animals changes during ecosystem succession, focusing on a group of soil mites called oribatids. Oribatids are tiny, abundant, and diverse, which means that you can find an entire community of them in a small sample of soil. There are also many resources available to help identify various oribatid species, so they are a perfect organism to observe to study changes in soil ecosystem diversity. Also, the mobility of oribatids is relatively limited, since they exist in the deep soil are restricted to moving through soil pores and can occasionally move by passive dispersal. Therefore, oribatid communities mainly develop through the process of ecosystem succession.

在最近的一项研究中，科学家们对一片森林的年代序列进行了深入研究，这片森林是农田被废弃后重新生长的。他们想知道同一类的森林在不同的年龄阶段下所含的土壤生物群落是否相同。科学家们假定农田上可能只有少数丰富度较低的甲螨，在古老的森林中会形成具有高度多样性的复杂群落。将当前的航拍照片与1950年的照片作比较，科学家们确定哪些地区在1950年代曾是森林（历史悠久的森林long-established forests），以及哪些曾经是农田（近期森林recent forests），在近期森林中，我们还将其区分为孤立的森林（主要被农田包围着，很可能显示出的甲螨群落与在农田中发现的相似）和与其他森林相连接的森林（ 可能与古老的森林发现的甲螨群落相似）。

In a recent study, scientists carried out in a chronosequence of forests that are re-growing after cropland abandonment. They wanted to know if similar forests of different ages have the same soil communities. Scientists hypothesized that croplands probably had only a few oribatid species in low abundances, but that complex communities with high diversity would develop in older forests. Comparing current aerial photographs with others from the 1950s, scientists determined which areas had been forests in the 1950s (long-established forests), and which had been croplands (recent forests). Among the recent forests, we also distinguished between isolated forests (surrounded mainly by croplands and most likely showing oribatid communities similar to those found in croplands) and those connected to other forests (probably with oribatid communities similar to those found in old forests).

科学家们观察到两个重要的结果。第一，在历史悠久的森林（long-established forests）和与其他森林相连接的近期森林（recent forests which connected to other forests）当中，显示出了相似的甲螨数量和甲螨物种数量，这比在孤立森林中所看到的数量要高。第二，在孤立森林和与其他森林相连接的森林里的甲螨群落共有的物种比在历史悠久的森林中多（图三，底部）。很有可能，在生态系统发展的早期，甲螨主要是通过被动分散到达的。这大概就是为什么与历史悠久的森林相连的近期森林会迅速形成与历史悠久森林相类似的甲螨群落。但随着近期森林生态系统的继续发展，庇护所的缺乏和食物可获得性降低可能会阻止一些甲螨物种在那永久定居。这就可以解释为什么在与其他森林相连接的近期森林里的甲螨群落会与孤立森林和田地里的甲螨群落更相像。

Scientists observed two important results. First, long-established and recent but connected forests showed similar numbers of oribatids and similar numbers of species, which were higher than what was seen in the isolated forests. Second, oribatid communities in isolated and connected recent forests shared more species than they did with long-established forests (Figure 3, bottom). Likely, oribatids arrive mainly by passive dispersal early in ecosystem development. That is probably why recent forests connected to long-established forests quickly establish oribatid communities similar to those in the long-established forests. But as the recent forest ecosystem continues to develop, lack of refuge availability and access to food may prevent some oribatid species from permanently settling there. This could explain why oribatid communities in recent and connected forests are more like those of isolated forests and thus to those of croplands (Figure 3).

        图3-生态系统随着时间发生变化和发展

在1950年代（顶部），森林中的甲螨群落比耕地里的甲螨群落更加丰富。弃耕后（中间），一些来自森林的物种个体主要通过被动分散（箭头）的方式到达相连的耕地。最后，可能更需要发达成熟的土壤的少数物种的消失（虚线箭头），便造成了目前三种森林间的差异。（底部）

    Figure 3 - Ecosystems change and grow over time.

In the 1950s (top), there were more abundant and rich communities of oribatids in the forest than in croplands. After crop abandonment (middle), individuals of some species from the forest arrived in the connected croplands mainly by passive dispersal (arrows). Finally, the disappearance (dashed arrow) of a few species, which probably needed a more developed soil, created the current differences among the three kinds of forests (bottom).

生态系统不仅会“生长发展”，如果没有发生重大的干扰（如火灾），也会“老化”。科学家们研究了加拿大北部森林中生态系统的老化。他们根据上次森林火灾以来的时间，按年代序列对甲螨进行了采样，这些年代是根据100年前的地图、200年的树木的年轮和对深层土壤的化学测年得估算的，这些土壤的年份高达700多年。尽管在最近一次大火后森林发展的前200年里，甲螨的丰富度大幅度下降，但不同物种的数量起初并未真正受影响，直到森林老化后期才真正受到影响。这意味着磷、氮等营养物质的逐渐减少不能维持种群的丰富度，后来甚至无法维持某些物种的整个种群。科学家们还研究了在枯木下的土壤样本和裸露的土壤样本，他们发现，尽管甲螨的数量保持稳定，但枯木下的甲螨丰富度要比生活在裸露土壤中的要低。这使科学家们得出一个结论，生活在暴露土壤上的甲螨受生态系统老化的影响更大，这可能是因为随着森林的老化，碎叶的供应减少了。

Ecosystems not only “grow,” but can also “age” if no major disturbance occur, such as fires. Scientists studied ecosystem aging in Canadian boreal forests [4]. They sampled oribatids in a chronosequence based on the time since the last forest fire, which was estimated from 100-year-old maps, tree rings from trees up to 200 years old, and chemical dating of deep soil, which was up to 700 years old! Although oribatid abundance was drastically reduced during the first 200 years of forest development after the last fire, the number of different species was not really affected until the later stages of forest aging. This means that the progressive diminution of nutrients as phosphor and nitrogen could not maintain abundant populations, and later on, not even entire populations of some species. Scientists also studied soil samples beneath tree logs and exposed soil and found that oribatids beneath logs were less abundant than those living in exposed soil, although maintained their populations stable. This led lead scientists to conclude that oribatids living on exposed soil were more affected by aging, probably because of a reduction in the availability of leaf litter as the forest aged.

ECOSYSTEMS ARE LIKE PRECIOUS MOVIES

生态系统就像珍贵的电影

我希望现在， 当你想象一个森林里的生态系统多样性时，你的脑海里不仅仅是一幅静止不动的画面，因为这些生物都在变化和移动，出现和消失…我希望你也想象能到栖息在我们脚下土壤里的生物！生态系统作为活跃的脚本，并不是静止不动的，而是随着时间的变化高度充满活力的。这些生活在土壤里的微小生物会采用许多与众不同和令人惊奇的策略来随着生态系统的变化而变化。生活在土壤里的生物对生态系统尤为重要，因为它们可以维持土壤的健康，还是枯叶和根部循环利用的很关键的一部分，更是一个可以帮助减轻全球变暖，有助于整个地球健康的过程。

I hope that now, when you imagine ecosystem diversity in a forest, you have more than just a still picture in your head, since all these living creatures change and move, appear and vanish…and I hope that you also imagine the creatures inhabiting the soil beneath our feet! Ecosystems, as living scenarios, are not static but are highly dynamic over time. The tiny, diverse creatures living in the soil change with the ecosystems, using many different and amazing strategies. Soil-living creatures are especially important for the ecosystem, as they maintain soil health and are a critical part of the recycling of dead leaves and roots, a process that actually helps to reduce global warming and contributes to the health of our entire planet.

Glossary 术语表

Soil Biodiversity: ↑ The total variety of living creatures inhabiting soils.

土壤生物多样性：栖息在土壤中的所有生物组合

Invertebrates: ↑ Animals with no bones. In the soil, that means mainly worms and arthropods (centipedes, woodlices, insects, spiders…).

无脊椎动物：没有骨头的动物。在土壤里主要指蠕虫和节肢动物（蜈蚣、木虱、昆虫和蜘蛛等）

Soil Pores: ↑ Extremely small (<0.075 mm) spaces in the solid structure of the soil, filled mainly with air and water [1].

土壤空隙：在土壤固态结构中极其微小(<0.075 mm)的空间，主要充满着空气和水。

Vertical Migration: ↑ Vertical migration is typical of soil and aquatic environments, where mobile organisms are not limited to move over a (horizontal) surface. Like any other migration, it is normally guided to find resources or better environmental conditions.

垂直迁移：垂直迁移是土壤和水上环境中运动的典型特征，在这些环境中，生物不限于在（水平）表面上移动。与任何其他迁移一样，它通常是为了寻找资源或更好的环境条件。

Soil Mesofauna: ↑ Soil inhabitants, smaller than 2 mm, such as springtails, mites, and tiny worms [2].

土壤中型动物： 小于2毫米的土壤居民，如跳虫、螨虫和小型蠕虫[2]。

Passive Dispersal: ↑ Mobile organism can move actively (using their legs or appendices to go through the territory) or let themselves “go with the flow” (of water, wind or even other animals), which is call passive movement or dispersal.

被动散布：流动的生物体可以主动移动（用它们的腿或附肢穿行于领地），也可以让自己 "随波逐流"（被水、风甚至其他动物带走），这就是所谓的被动移动或被动散布。

Ecosystem Succession: ↑ The process by which ecosystems are “born” and “grow” after the creation of new surfaces, like a new coral island or the soil revealed after glaciers melt, or how ecosystems “regrow” after disturbances like forest fires.

生态系统的演替：生态系统在形成新的地表后 "诞生 "和 "生长发展"的过程，如新的珊瑚岛或冰川融化后露出的土壤，或生态系统在森林火灾等干扰后是如何 "重新生长"的。

Chronosequence: ↑ A group of ecosystems studied at the same time, which are similar in origin, plant species, and geographical area, but have different ages. Studying ecosystems in chronosequence is necessary because we cannot wait decades to sample one ecosystem over the course of its development.

年代序列：同时研究一组生态系统，这组生态系统的起源、植物种类和地理区域相似，但年龄不相同。按时间顺序研究生态系统是必要的，因为我们不可能在一个生态系统的发展过程中等上几十年来取样。

—The End—

附上作者信息：

Enrique拥有生物学博士学位，他是CREAF的研究员，他还对国际合作感兴趣，是欧洲-地中海项目MENFRI的负责人。他还对国际合作感兴趣，是欧洲-地中海项目MENFRI的负责人，他从该项目中创立了一个组织，建立伙伴关系，以克服发展和环境方面的复杂挑战。恩里克对全球变化下的景观复原力和管理研究做出了贡献，他还继续他的主要研究方向，即生态系统生物多样性随时间的变化。恩里克利用几种土壤无脊椎动物群落，研究了西班牙、新西兰和加拿大的森林和耕地的动态。（作者介绍是用机器翻译的，我实在没精力来，望见谅）

翻译者小婧唠叨几句：

这篇文章中英文加起来7000多字，而且相比起之前的文章学术性会强一些（因为有实验分析、实验过程和实验结果），很多长句和从句让人难以琢磨，所以文章难免会有些瑕疵，还望海涵。

翻译一篇文章其实是很消耗精力的，我在大年初一花了大半天翻译才翻译了1/2，这几天又继续翻译，再加上校对文稿和排版所花费的时间可谓既在意料之外，又在情理之中。当我写到此时已经是北京时间凌晨1:42，还有4天就开学了，其实我还有一些预习任务没有做完。

不过，不管怎样，既然我坚持做翻译，收获也自然是属于我自己的，在这过程也是与作业权衡取舍的过程，开学后我也会继续坚持下去的。在此非常感谢您能阅读至此，谢谢您对我文章的认可与喜爱。我会继续努力的！

PS：作者介绍是用机器翻译的，我实在没精力来，望见谅／捂脸／

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