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

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.

## REFERENCES

1. Nielsen, U. (Ed.). 2019. "Soil and its fauna," in *Soil Fauna Assemblages: Global to Local Scales* (Cambridge: Cambridge University Press). p. 1–41. doi: 10.1017/9781108123518.002

2. Orgiazzi, A., Bardgett, R. D., Barrios, E., Behan-Pelletier, V., Briones, M. J. I., Chotte, J. L. et al. (Eds.). 2016. *Global Soil Biodiversity Atlas*. Luxembourg: Publications Office of the European Union.

3. Doblas-Miranda, E., Sánchez-Piñero, F., and González-Megías, A. 2009. Vertical distribution of soil macrofauna in an arid ecosystem: are litter and belowground compartmentalized habitats? *Pedobiologia* 52:361–73. doi: 10.1016/j.pedobi.2008.11.006

4. Doblas-Miranda, E., and Work, T. T. 2015. Localized effects of coarse woody material on soil oribatid communities diminish over 700 years of stand development in black-spruce-feathermoss forests. *Forests* 6:914–28. doi: 10.3390/f6040914
**SUBMITTED:** 17 March 2020; **ACCEPTED:** 12 January 2021;

**PUBLISHED ONLINE:** 04 February 2021.

**EDITED BY:** Helen Phillips, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION:** Doblas-Miranda E (2021) Soil Ecosystems Change With Time. Front. Young Minds 9:543498. doi: 10.3389/frym.2021.543498

**CONFLICT OF INTEREST:** The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2021 Doblas-Miranda. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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## AUTHOR

### ENRIQUE DOBLAS-MIRANDA

Enrique has a Ph.D. in biology and is a researcher at CREAF. He is also interested in international cooperation and was the head of the Euro-Mediterranean project called MENFRI, from which he founded an organization that forges partnerships to overcome complex challenges to development and the environment. Enrique has contributed to research on landscape resilience and management in the face of global change, and he also continues his principal line of research about variations in the biodiversity of ecosystems over time. Using several soil invertebrate communities, Enrique has studied the dynamics of forests and croplands in Spain, New Zealand, and Canada. *e.doblas@creaf.uab.cat

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# MICROBIAL MATS: PRIMITIVE STRUCTURES THAT COULD HELP US FIND LIFE ON OTHER WORLDS

Santiago Cadena<fnref n="1" />,<fnref n="2" />, Paula Maza-Márquez<fnref n="3" />, Sandra I. Ramírez Jiménez<fnref n="2" />, Sharon L. Grim<fnref n="3" />, José Q. García-Maldonado<fnref n="1" />*, Leslie Prufert-Bebout<fnref n="3" /> and Brad M. Bebout<fnref n="3" />

## YOUNG REVIEWERS:

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AGE: 15

Some microscopic organisms grow together to build structures known as microbial mats. These mats are formed from several layers with different colors, and their structure depends on environmental conditions such as sunlight, humidity, and available food. Microbial mats are found in oceans, lakes, and coastal lagoons, as well as in extreme environments like deserts, polar regions, and hot springs. The study of fossils indicates that microbial mats were a common form of life on early Earth, and they have persisted on our planet ever since! Therefore, the study of modern mats helps us to understand microbial life in the past, and how they might help to regulate the Earth's climate. Scientists believe that microbial mats can prosper on rocky planets like Earth, so they are studying mats in different terrestrial environments to help them to recognize evidence indicating the presence of mats on other worlds.

<footnote n="1">¹Departamento de Recursos del Mar, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional, Mérida, Mexico</footnote>

<footnote n="2">²Centro de Investigaciones Químicas, Universidad Autónoma del Estado de Morelos, Cuernavaca, Mexico</footnote>

<footnote n="3">³Exobiology Branch, National Aeronautics and Space Administration (NASA) Ames Research Center, Mountain View, CA, United States</footnote>
## MICROORGANISMS CAN FORM LARGE STRUCTURES!

Microorganisms are tiny living things that cannot be seen with the naked eye, as most of them are made up of only one cell. We need to use a microscope to see them. They live in and on our bodies, and in our surroundings, including the soil, water, and air. Sometimes microorganisms work together to build big structures that are observable without microscopes. Lichens, for example, look like plants, but they result from an interesting relationship between algae and fungi, which form flakes or leafless branches on trees or rocks. Yogurt, vinegar, cheese, and bread are produced by fermentation processes, which are performed by groups of particular microorganisms. Some plants built small structures called root nodules, where microorganisms can live. Thanks to the microorganisms in these nodules, the plants can obtain more food from the environment and thanks to the plants, the microorganisms have a place to live and a lot of sugar to feed on. Commonly, when your food spoils in the refrigerator, you can observe a layer of microorganisms known as a **biofilm** growing on it.

In nature, many microorganisms live in the ground. Using soil, water, and minerals these microorganisms can form big, solid structures. When high-quality food is present, some microorganisms can reproduce by the millions, attached to grains of soil or sand, creating structures that look like normal rocks or mud, but that are actually living structures built by multitudes of microscopic organisms. There are different types of rocky microbe structures. They have names like microbialites, endoevaporites, oncolites, and stromatolites (Figure 1) [1]. These structures can have diverse shapes and colors, which are strongly influenced by the environmental conditions present during their formation. **Microbial mats** are a specific example of a structure built by microorganisms.

## WHAT ARE MICROBIAL MATS AND WHAT DO THEY DO?

Microorganisms need energy and water to build a microbial mat. Water can be provided by hot springs, lagoons, or a coastal shoreline, and many microorganisms use solar light as their main energy source. With enough energy and water, microorganisms can flourish on a surface, sticking together with food and grains of sand or soil, and building mats that can be up to a few centimeters thick (Figure 1C). In some cases, a new living mat grows on top of an older, dead mat, creating thick layers (Figures 1G,H). As the name suggests, mats resemble carpets or rugs, in the way that they cover surfaces of various sizes. When seen up close, mats also have interesting vertical layering (Figure 2). Microorganisms can be distributed in green, orange, red, and purple layers, with each layer representing a different community of microorganisms that needs different amounts of sunlight and oxygen (Figure 1I). All the

### BIOFILM

A layer of microorganisms that are stuck to one another and stuck to (or floating on) a surface.

### MICROBIAL MAT

A large structure built by microorganisms, that grow on the top of sediments. It is usually composed by grains of soil, minerals, nutrients, and microbes.
Figure 1

Examples of structures made by microorganisms using soil, water, rocks, and minerals. (A) Oncolites from Casey Falls locality, Canning Basin, Western Australia (photograph credit: Heidi Allen). (B) Endoevaporite. (C) Microbial mat. (D,E,G,H) Microbial mats in the Yucatán Peninsula in Mexico. (F) Microbial mats from the Middle Island Sinkhole, Lake Huron in North America (photo credit: John Bright, NOAA Thunder Bay National Marine Sanctuary). (I) A cross-section of a microbial mat from Guerrero Negro, Mexico.

<figure><img src="image_256.png" /><figcaption>Figure 1</figcaption></figure>

ECOSYSTEM

A community of organisms living in a certain area, and the non-living components of their environment (weather, landscapes).

¹ If you want to explore deeper into microbial mats, watch this video: https://youtu.be/VpCkgvb41Ag

FOSSIL RECORD

The history of life on Earth, documented by fossils, remains, or imprints of organisms that lived many years ago.

microorganisms in the mat work together to sustain themselves and to interact with their surrounding environment.

Studies have shown that microbial mats are important for the functioning of **ecosystems**. For example, when mats colonize the ground, they contribute to the health of soils and sediments, producing nutrients that enrich them. Mats participate in the recycling of some chemical elements, including carbon, nitrogen, and sulfur. They can also clean the water and they both take up and release gases from the atmosphere, such as oxygen, hydrogen, carbon dioxide, and methane. Mats are also a food source for animals. Some flies, snails, worms, crabs, and birds feed on small pieces of microbial mats, and larger organisms can then feed on those smaller ones [2]. Because they are continuously eaten, mats often do not grow much, except in extreme environments¹.

MICROBIAL MATS AROUND THE WORLD

Nowadays, microbial mats can be found in tropical coastal lagoons, estuaries, and bays, but they may be difficult to spot because they can only grow large when they have enough food and when they are protected from grazing organisms. However, mats are found extensively in the **fossil record**, indicating that, billions of years ago, these structures were abundant on the early Earth. Just think about it! Dinosaurs originated 0.245 billion years ago (BYA), fishes 0.530 BYA and aquatic plants 1.2 BYA, but microbial mats were present on Earth
<caption>**Figure 2**</caption>

Zoom to the top first centimeter of a microbial mat. (A) Structure of a classic microbial mat. Living microbes are found in the top layer, while older mat is below. (B) A close-up look at a cross-section of the first centimeter of a mat, showing the different layers formed. (C) Different types of microorganisms live in the different layers of a microbial mat. Important elements such as carbon, nitrogen, and oxygen are recycled by microorganisms.

<figure><img src="image_257.png" /><figcaption>Figure 2</figcaption></figure>

even 3.5 BYA, long, long before any other forms of life existed. On early Earth, these microbial structures proliferated on rocky or sandy surfaces worldwide. Imagine that! Today, microbial mats usually get eaten by other organisms, but billions of years ago, those higher lifeforms had not yet evolved, so the mats just kept growing! Microbial mats are one of the oldest forms of organized life and the study of today's mats helps scientists to understand their contribution to ecosystems on both modern and early Earth.

Geological data and laboratory studies have revealed the importance of microbial mats in the history of Earth. It is believed that, in the past, the abundance and high activity of mats created the atmosphere that we breathe today. Furthermore, as ancient mats released carbon dioxide and methane, they also contributed to the regulation of Earth's climate, helping to create the warm atmosphere that made the Earth a habitable planet [3].

## MATS AS MODELS FOR EXTRATERRESTRIAL LIFE

Microbial mats have been observed in extreme ecosystems, such as in extremely salty areas around coasts and in deserts soils. Also, they can form in the polar regions attached to permafrost, which is soil that never thaws. Mats have been discovered at high temperatures, close to volcanoes and hot springs. They have also been found in the deep ocean, under harsh conditions of light and pressure.

Since mats can grow under extreme variations of sunlight, water, temperature, and salinity, scientists believe that microbial mats might exist beyond Earth, growing on other rocky planets or moons. Most planets and moons in our solar system are not suitable places for life, due to the high amounts of ultraviolet light or cosmic radiation they receive, and their lack of a life-supporting atmosphere. But evidence suggests that some planets and moons in the solar system may have water, sometimes protected by ice layers. If there is life in those remote places, it is likely to be microbial life, not big animals, or plants. Therefore, by studying the characteristics of microbial mats, scientists can discover the microbial mats' **biosignature**. A biosignature is like an identification card that suggests the presence of life. For example, the

## BIOSIGNATURE

Any feature, molecule, substance, or characteristic that strongly suggest evidence of life.
gases produced by microorganisms or the structures they built in rocks and sand could be their biosignatures. Using cameras and instruments on spacecrafts, large structures produced by microorganisms would be far easier to detect than would microorganisms themselves. If we observe the biosignature of microbial mats on another planet using a spacecraft's cameras, it will indicate that microorganisms could be living on that planet.

Currently, scientists are looking for live or fossilized mats in our solar system. The planet Mars and two moons of the planet Saturn (Titan and Enceladus), have geological characteristics that are promising for the formation of microbial mats. Mars has a rocky, dry surface but recently, NASA's Mars Reconnaissance Orbiter provided strong evidence of liquid water on the planet [4]. The Cassini-Huygens and Voyager spacecraft missions studying Saturn and its moons found evidence of water and polar ice on Titan and Enceladus, probably similar to the ice and water found in the polar ice caps on Earth [5]. There is no evidence yet of any kind of life prospering beyond our planet, but the study of extreme ecosystems on Earth helps us to predict the conditions needed for microbial life elsewhere in the Universe, and to design strategies and devices that will help us to find it. For example, we must know which instruments to send on space missions to detect gases produced by microorganisms, and we must know how to identify microbial mats in photographs.

## HOW ARE MICROBIAL MATS STUDIED?

Microbial mats are everywhere on Earth, in both mild and extreme environments, and in both accessible and hard-to-reach places. Some of the most famous microbial mats are found at Yellowstone National Park, California (USA), where they grow near hot springs and geysers. However, you can find mats on some shallow coasts, where seawater rises and falls with the tides. For example, mats can grow in mangrove forests, salt marshes, wetlands, or at the edges of rivers and lakes. Sometimes, in other places where the water is not cleaned regularly, bits of biofilm or small mats can grow—for example, in birdbaths, fountains, or fish tanks (Figures 3A–H).

Current microbial mat research is conducted through field trips and expeditions that investigate the ability of mats and microorganisms to survive in various ecosystems, under diverse environmental conditions. This information helps scientists to understand the role of mats in ecosystems, and the limits of sunlight, water, temperature, and other conditions under which these microorganisms can function. In addition to studying mats in their natural locations, pieces of mats are transported to laboratories, where long-term experiments can be performed, and various laboratory tools can be used to learn about the lives of the microorganisms. For example, we can grow mats in the laboratory and use instruments to measure how much
<caption>**Figure 3**</caption>

Algae and mat-like biofilms growing in familiar places, such as (A) a bird bath, (B) a street gutter, (C) an exterior roof board, (D) the bottom of a fish tank, (E) a water collector from a roof drain, (F) the waters of an estuary, and (G) a board found under a shed. (H) Floating algae in an upstream area of Elkhorn Slough, California. (I) A view of the microbial mat collecting area. (J) Sampling microbial mats. (K) Transporting mats from the field site. (L) Mats incubating in a greenhouse at NASA's Ames Research Center.

<figure><img src="image_258.png" /><figcaption>Figure 3</figcaption></figure>

oxygen they produce and how much carbon dioxide they consume (Figures 3I–L).

CONCLUSION

In conclusion, microbial mats are complex systems that provide an excellent opportunity to study microbial diversity, ecology, and evolution. Mats are found all over Earth in many kinds of ecosystems, and they come in a wide variety of shapes and sizes. Just like the mats themselves, scientist interested in studying microbial mats can be found all around the world. Do you know, or have visited any place where mats would grow?

ACKNOWLEDGMENTS

This work was supported by Consejo Nacional de Ciencia y Tecnología (CONACYT) through grant CF-2019-848287. Sampling at Yucatán Peninsula was supported by Programa de Apoyo a Proyectos de Investigación e Innovación Tecnológica (PAPIIT-UNAM) IN216219. Santiago thanks CONACYT Ph.D., fellowship (grant 570049-2017-2020). SIRJ acknowledges CONACYT grant 377887. Many thanks to Mike Kubo and Sanjoy Som for the support during the Young Scientist Program from Blue Marble Space Institute of Science. Thank you so much to Drs. Claudia Teutli and Jorge Herrera for making possible the sampling at Yucatán. Thanks to Veronica and Bart for the
hospitality at Santa Clara. We are grateful to Anabel Suárez-Guevara for the elaboration of the figures. The insightful comments by editors Rémy Beugnon and Susan Debad are gratefully acknowledged.

## REFERENCES

1. Yanez-Montalvo A., Águila Salgado B., Gómez-Acata E., Beltrán Y., Valdespino-Castillo P., Centeno C., et al. 2019. Microbialites: what on earth? *Front. Young Minds*. 7:112. doi: 10.3389/frym.2019.00112

2. Seckbach J., and Oren A. 2010. *Microbial Mats: Modern and Ancient Microorganisms in Stratified Systems*. Amsterdam: Springer. doi: 10.1007/978-90-481-3799-2

3. Hoehler T. M., Bebout B. M., and Des Marais D. J. 2001. The role of microbial mats in the production of reduced gases on the early Earth. *Nature*. 412:324-7. doi: 10.1038/35085554

4. Nazari-Sharabian M., Aghababaei M., Karakouzian M., and Karami M. 2020. Water on Mars-A literature review. *Galaxies*. 8:40. doi: 10.3390/galaxies8020040

5. Mitri G., Postberg F., Soderblom J. M., Wurz P., Tortora P., Abel, B., et al. 2018. Explorer of enceladus and titan (E2T): investigating ocean worlds' evolution and habitability in the solar system. *Planet. Space Sci.* 155:73-90. doi: 10.1016/j.pss.2017.11.001

**SUBMITTED**: 15 January 2021; **ACCEPTED**: 08 February 2022;

**PUBLISHED ONLINE**: 18 March 2022.

**EDITOR**: Rémy Beugnon, German Centre for Integrative Biodiversity Research (iDiv), Germany

**SCIENCE MENTOR**: Ruchira Sharma

**CITATION**: Cadena S, Maza-Márquez P, Ramírez Jiménez SI, Grim SL, García-Maldonado JQ, Prufert-Bebout L and Bebout BM (2022) Microbial Mats: Primitive Structures That Could Help us Find Life on Other Worlds. *Front. Young Minds* 10:654148. doi: 10.3389/frym.2022.654148

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2022 Cadena, Maza-Márquez, Ramírez Jiménez, Grim, García-Maldonado, Prufert-Bebout and Bebout. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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## YOUNG REVIEWERS

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## AUTHORS

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### SANTIAGO CADENA

I am a marine biologist dedicated to the study of marine and hypersaline microorganisms. I am very interested in geomicrobiology, astrobiology, and biotechnology. I have experience in the study of the methane and sulfur cycles in microbial mats. Also, we are studying the microorganisms living in mangrove forests. In brief, I am interested in studying the role of microorganisms in nature and their potential use for biotechnological purposes.

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### PAULA MAZA-MÁRQUEZ

I am a postdoctoral researcher in the Exobiology Branch at NASA's Ames Research Center. I study the structure and function of microbial mats. I am particularly interested in genes that control nitrogen cycling, to explore the hypothesis that key features of the modern biological nitrogen cycle evolved in microbial mat systems.

<figure><img src="image_264.png" /></figure>

### SANDRA I. RAMÍREZ JIMÉNEZ

I am an astrobiologist at Centro de Investigaciones Químicas, Universidad Autónoma del Estado de Morelos, interested in microorganisms from extreme ecosystems, specifically, bacteria living in high salt concentrations. I study the adaptation strategies bacteria use in environments mimicking the salty water of the satellite Europa or the subsurface of the planet Mars, to understand the limits of terrestrial life and the potential for life on other bodies in the solar system.
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SHARON L. GRIM

I am a postdoctoral fellow at NASA's Ames Research Center. I study cyanobacteria, which are photosynthetic microorganisms that have shaped Earth's atmosphere for billions of years by producing oxygen. I use computational tools to understand the genes and biogeochemistry of cyanobacteria and other microorganisms in extreme microbial mats.

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JOSÉ Q. GARCÍA MALDONADO

I am a research scientist working at the Marine Resources Department in the Center for Research and Advanced Studies of the National Polytechnic Institute (CINVESTAV), in Mexico. My investigations are mainly related to the ecology and biotechnology of complex microbial communities in marine and extreme environments. *jose.garcia@cinvestav.mx

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LESLIE PRUFERT-BEBOUT

I am a microbial ecologist and geobiologist. I am interested in how the sedimentary mineral environment characteristics affect colonization by different populations of microorganisms. I focus on cyanobacterial species and how they distribute themselves in their environments. I am also very interested in how much and what colors of light exist inside of sands and rocks.

<figure><img src="image_268.png" /></figure>

BRAD M. BEBOUT

I am a scientist at NASA's Ames Research Center now, but I have been studying microbial mats since I was a graduate student; that was 30 years ago! I am mostly interested in how mats help recycle carbon and nitrogen in the environments where we find them, but also in the biosignatures that they produce so that we, at NASA, can see if they occur in places other than Earth.
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# HOW SOIL INVERTEBRATES DEAL WITH MICROPLASTIC CONTAMINATION

Carlos Barreto<fnref n="1" />*†, Matthias C. Rillig<fnref n="2" />,<fnref n="3" />†, Walter R. Waldman<fnref n="4" />† and Stefanie Maaß<fnref n="3" />,<fnref n="5" />†

## YOUNG REVIEWERS:

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AGE: 8

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Small animals living in soils, called soil invertebrates, represent a very diverse group of soil inhabitants. They include earthworms, woodlice, spiders, springtails, mites, and some insects. Soil invertebrates feed on dead plants, on fungi and bacteria, or on other soil invertebrates. The many ways soil invertebrates interact with each other, and the large number of different species, make life in soils complex and difficult to understand. Unfortunately, soil invertebrates have been dealing with soil pollution, including contamination with tiny particles of plastic called microplastics for decades now. But are microplastics harmful to these organisms? Can microplastics be passed between soil invertebrates when one feeds on another? Most questions about microplastics and soil invertebrates have been investigated using earthworms, but a few studies on others, like

<footnote n="1">¹Department of Biology, Biotron Experimental Climate Change Research Centre, Western University, London, ON, Canada</footnote>

<footnote n="2">²Plant Ecology, Institute of Biology, Freie Universität Berlin, Berlin, Germany</footnote>

<footnote n="3">³Berlin-Brandenburg Institute of Advanced Biodiversity Research (BBIB), Berlin, Germany</footnote>

<footnote n="4">⁴Center of Science and Technology for Sustainability, Federal University of São Carlos, Sorocaba, Brazil</footnote>

<footnote n="5">⁵Plant Ecology and Nature Conservation, Institute of Biochemistry and Biology, Universität Potsdam, Potsdam, Germany</footnote>
springtails, mites, and nematodes, also exist. In this article, we summarize the effects of microplastics on soil invertebrates.

## WHO ARE THE HIDDEN SUPERHEROES IN THE SOIL AND WHAT ARE THEIR JOBS?

Many animals live in soils, but... why can we not see them all? The tiny animals living in soils are called **soil invertebrates**, and they vary greatly in size. Some species are even smaller than the diameter of a human hair! We can classify soil invertebrates into three main groups based on their sizes [1] (Figure 1). Macroinvertebrates are big invertebrates like earthworms, woodlice, spiders, millipedes, centipedes, and some insects like beetles. They are bigger than 2 mm and can create their own living spaces in soils. Mesoinvertebrates have an intermediate size (0.1–2 mm) and live in air-filled pore spaces in soils. Examples include springtails [2], mites, and potworms. Microinvertebrates are <0.1 mm, so small that we cannot see them without the help of a microscope. They live in the water that is present around soil particles. Examples include nematodes, rotifers, and water bears.

Each soil invertebrate group likes different foods [3]. In general, some soil invertebrates, like spiders, feed on other soil invertebrates. Others, like springtails, feed on microbes like fungi and bacteria; and still others, like earthworms, feed on dead plants. These feeding relationships are part of a complex food web that is composed of many species (Figure 2) and many interactions.

### SOIL INVERTEBRATES

Small, soil-dwelling animals without backbones or bony skeletons.

<caption>**Figure 1**</caption>

Examples of soil invertebrates of different size. (A) water bear, (B) wheel animal, (C) nematode, (D) potworm, (E) springtail, (F) mite, (G) spider, (H) beetle, (I) woodlouse, (J) earthworm, (K) centipede, and (L) millipede. Illustrations do not represent the actual size of the soil invertebrates.

<figure><img src="image_272.png" /><figcaption>Figure 1</figcaption></figure>
**Figure 2**

Examples of soil invertebrates. Microinvertebrates (<0.1 mm) include (A) water bears and (B) nematodes; mesoinvertebrates (between 0.1 and 2 mm) include (C) potworms, (D-G) springtails, and (H,I) mites; macroinvertebrates (>2 mm) include (J) woodlice, (K) beetles, (L) earthworms, (M) millipedes, (N) centipedes, and (O) spiders (photo credits: A,C-O: Frank Ashwood; B: Devdutt Kamath).

<figure><img src="image_273.png" /><figcaption>Figure 2</figcaption></figure>

All soil invertebrates are important for the environment. For example, water bears can colonize new environments and serve as food for other organisms. Nematodes can help cycle nutrients through the soil, with the help of springtails, mites, woodlice, and earthworms. Woodlice, springtails, and some mites [4] help decompose leaves and other formerly living materials in the soil [5], and they also help trap carbon from the atmosphere in the soil. Earthworms help rainwater to infiltrate into the soil. Some soil invertebrates may feed on organisms that cause plant diseases, protecting plants from these pests. Each in their own way, these creatures help to keep the soil healthy, which is also necessary to ensure the quality of our food.

**MICROPLASTICS**

Small plastic particles (<5 mm) which can be harmful to soil and aquatic life.

**THE THREAT OF MICROPLASTICS**

Unfortunately, the homes of many soil invertebrates have been invaded by pollutants such as **microplastics**. Microplastics are small particles (<5 mm) that are created in many ways (Figure 3; Box 1). For example, when cars are driven on roads, their tires wear out and
**Figure 3**

Examples of microplastics. (A) Springtail and urea-formaldehyde particles. (B) Springtail and plastic scraped off a pop bottle. (C) Polypropylene microbeads. (D) Polypropylene microfibers. (E,F) Adult nematodes with fragments of polystyrene. (G) Particles formed by tire abrasion. (H) Close-up of a polyurethane sponge. (I) Powder-like polypropylene (photo credits: A,B: C. Reinhart and D. Daphi, C,I: Stefanie Maaß, D: Carlos Barreto, E,F: Shin Woong Kim, G: Eva Leifheit, H: Walter Waldman).

<figure><img src="image_274.png" /><figcaption>Figure 3</figcaption></figure>

**ADDITIVES**

Chemicals that make the plastic more colorful flexible, or less flammable.

**DEGRADATION**

The breakdown or separation of something into simpler/smaller parts.

**LEACHING**

When a liquid substance is released away from its solid source.

lose microplastics, which can be picked up by the wind and end up in soils. Also, when we do laundry, plastic fibers are released from the clothes into the water. One fleece coat alone can release up to one million fibers per wash cycle! Many of these plastic fibers end up in the sewage, which is a problem because treated sewage can be used to fertilize the soil that crops are grown in. Microplastics can also enter the soil through plastic trash and rainwater.

Microplastics have a huge range of chemical and physical properties. Plastic materials often contain **additives**. These additives can make microplastics even more harmful to the environment, especially once the microplastic particles start to undergo **degradation**. Plastic particles become increasingly brittle due to sunlight, water, and the surrounding soil particles that rub on them. Over time, microplastic particles fall apart into even smaller particles, called **nanoplastics**. During degradation, the additives slowly start to **leach** out of the microplastics, into the soil. The particles can also leach into the tissues of organisms if they are eaten. Unfortunately, we still do not know much about the effects that leaching of additives from plastics can have on the environment.

So, microplastic particles can clearly affect the soil, but how do they affect soil invertebrates? [6] If we look at earthworms, with their constant appetite for dead leaves and their intense digging activities, we can easily imagine that they regularly ingest microplastic particles and transport them deep into the soil. Not only by feeding, but also on their skin, they can transport these particles. The same has
Box 1 | Sources of microplastics in soils.

<table><thead><tr><td>Object</td><td>Plastic (formal names)</td><td>Comment</td></tr></thead><tbody><tr><td>Paints</td><td>Epoxy and alkyd resins</td><td>Microplastics are formed from sanding painted surfaces and when paint peels off walls or other structures.</td></tr><tr><td>Plastic bags</td><td>Low-density polyethylene (LDPE)</td><td>When plastic bags are discarded improperly, they might end up on the ground and get degraded by the sun, eventually forming microplastics.</td></tr><tr><td>Mulching films</td><td>Low-density polyethylene (LDPE)</td><td>Some farmers use plastic mulching films to protect plants from water loss. These plastics will break down from sun exposure and form microplastics.</td></tr><tr><td>Tires</td><td>Polyisoprene (natural rubber)</td><td>Although tires are made primarily of natural rubber, they also contain additives and their toxicity is currently being tested.</td></tr><tr><td>Foam</td><td>Polystyrene (PS)</td><td>Foams are widely used in house insulation and in packaging to protect products during transport and storage. Damage and breakdown of foams produce microplastics.</td></tr><tr><td>Glitter</td><td>Polyethylene terephthalate (PET)</td><td>Glitter spreads easily and can detach from makeup and toys and contaminate soil.</td></tr><tr><td>Water bottles</td><td>Polypropylene (PP)</td><td>Breakdown of improperly disposed water and soft drink bottles can contaminate the soil.</td></tr><tr><td>Soft drink bottles</td><td>Polyethylene terephthalate (PET)</td><td></td></tr><tr><td>Clothes</td><td>Polyesters and polyamides</td><td>Synthetic fibers release microfibers during washing, and they end up in the soil via fertilizers prepared from sewage.</td></tr></tbody></table>

been shown for springtails. What does this mean? On the one hand, the microplastic particles will become more degraded as they pass through the guts of soil organisms. But on the other hand, once particles are carried deeper into the soil, degradation slows down due to the absence of sunlight and reduced microbial activity. In other words, the deeper the particles move into the soil, the longer it takes for them to totally degrade.

MICROPLASTICS CAN AFFECT THE HEALTH OF SOIL ORGANISMS

Soil organisms feel sick when they eat microplastics, and this is has been reported for earthworms and springtails. After feeding on microplastic particles, earthworms suffered from several health problems, including inflammation and damage to the gut [7]. Additionally, ingestion of microplastics put the immune system of the earthworms on higher alert than usual. Springtails that ingested microplastics suffered changes in the helpful bacteria living in
their digestive systems [8]. Both earthworms and springtails grew
more slowly, had fewer offspring, and died more often after they
ingested microplastics.

This sounds like bad news for nematodes, but here is the good news: scientists have not seen a build-up of microplastic particles in organisms over time, which means that they might not suffer that much harm after all. However, it is likely that microplastic particles can be passed on along through the soil food web, from microbes like fungi, to springtails, to predatory mites; or from microbes to earthworms, and then to chickens [9]—and maybe also to humans! We still do not know much about how microplastics move through the soil food web, but research is progressing quickly on that topic. Despite these concerns, scientists have found a gleam of light! One research group reported that certain bacteria in the guts of earthworms can digest ingested microplastics, leading to high degradation rates [10]. This means that bacteria might be able to speed up the destruction of microplastics in soil. Can other soil invertebrates do the same? We simply do not know yet.

## WHAT CAN WE DO TO PROTECT SOIL INVERTEBRATES?

You might wonder why scientists have not made more progress answering important questions about the effects of microplastics on soils and the organisms that live there. Unfortunately, these studies face numerous difficulties. For example, we do not yet have a reliable method for measuring the amount of all types of microplastics in all types of soil. Also, many studies consist of short-term experiments that are done in the lab, instead of long-term studies done outdoors in the soil. The huge diversity of plastic types and additives makes it impossible to test everything under real-world conditions. Lab experiments are only informative to a certain degree. Lab experiments are also difficult because not all soil organisms will survive in the laboratory environment. But rest assured: scientists are doing their best to solve these problems. In the meantime, there are ways that you can help!

We should all try our best to minimize the future addition of plastics of any type and size into the environment. You may already know some of the most important ways! Avoid single-use plastic items like plastic cups or straws. Choose your favorite metal or reusable plastic cup, and a metal straw, and keep them handy in your lunch bag! It is also important to put plastic waste in the correct recycling container: This can help reduce the amount of plastic that ends up in the water and soil. Additionally, avoid beauty products that have microplastics in their ingredients, like some conditioners! There are alternative products that are free of microplastics, and some smartphone apps can help you choose the best ones for you. To reduce the number of plastic fibers released into the environment, try not to throw away old clothes
just because you do not want them anymore! Instead, try to sell, donate, or reuse them in a creative way. Let's join forces and save our tiny soil superheroes from further microplastic pollution. It is worth every effort!

## ACKNOWLEDGMENTS

We thank Frank Ashwood (Forestry Commission UK), Shin Woong Kim (Freie Universität Berlin), and Devdutt Kamath (University of Guelph) for kindly allowing us to use their soil invertebrate pictures. We thank C. Reinhart, D. Daphi, and Eva Leifheit (Freie Universität Berlin) for the pictures of plastics. We thank Anderson Abel de Souza Machado, Alice A. Horton, and Taylor Davis for their work on the book chapter on microplastics which was the starting point for this article. MR acknowledges funding from an ERC Advanced Grant (694368). This work was also partly funded by the German Federal Ministry of Education and Research BMBF within the Collaborative Project Bridging in Biodiversity Science-BIBS (phase 2, funding number 01LC1501B). We thank Helen Phillips, Rémy Beugnon, and Malte Jochum, the editors of the Soil Biodiversity collection, for such a great and important initiative. Last, but not least, we thank our young reviewers for their comments.

## REFERENCES

1. Coleman, D. C., Callaham, M. A., and Crossley, D. A. Jr. 2018. *Fundamentals of Soil Ecology, 3rd Edn.* London: Academic Press. p. 376.

2. Potapov, A. 2020. Springtails — worldwide jumpers. *Front. Young Minds* 8:545370. doi: 10.3389/frym.2020.545370

3. Erktan, A., Pollierer, M., and Scheu, S. 2020. Soil ecologists as detectives discovering who eats whom or what in the soil. *Front. Young Minds* 8:544803. doi: 10.3389/frym.2020.544803

4. Barreto, C., and Lindo, Z. 2020. Armored mites, beetle mites, or moss mites: the fantastic world of oribatida. *Front. Young Minds* 8:545263. doi: 10.3389/frym.2020.545263

5. Barreto, C., and Lindo, Z. 2020. Decomposition in peatlands: who are the players and what affects them? *Front. Young Minds* 8:107. doi: 10.3389/frym.2020.00107

6. de Souza Machado, A. A., Horton, A., Davis, T., and Maaß, S. 2020. Microplastics and their effects on soil function as a life-supporting system. In: *The Handbook of Environmental Chemistry*, eds D. He and Y. Luo. Cham: Springer. p. 1–24.

7. Rodriguez-Seijo, A., Lourenço, J., Rocha-Santos, T. A. P., da Costa, J., Duarte, A. C., Vala, H., et al. 2017. Histopathological and molecular effects of microplastics in *Eisenia andrei* Bouché. *Environ. Pollut.* 220:495–503. doi: 10.1016/j.envpol.2016.09.092

8. Zhu, D., Qing-Lin, C., Ana, X., Yanga, X., Christiec, P., Ked, X., et al. 2018. Exposure of soil collembolans to microplastics perturbs their gut microbiota
and alters their isotopic composition. *Soil Biol. Biochem.*
116:302–10. doi: 10.1016/j.soilbio.2017.10.027

9. Huerta Lwanga, E., Mendoza Vega, J., Quej, V.K., de los Angeles Chi, J., Sanchez del Cid, L., Chi, C., et al. 2017. Field evidence for transfer of plastic debris along a terrestrial food chain. *Sci. Rep.* 7:14071. doi: 10.1038/s41598-017-14588-2

10. Huerta Lwanga, E., Thapa, B., Yang, X., Gertsen, H., Salánki, T., Geissen, V., et al. 2018. Decay of low-density polyethylene by bacteria extracted from earthworm's guts: a potential for soil restoration. *Sci. Total Environ.* 624:753–7. doi: 10.1016/j.scitotenv.2017.12.144

**SUBMITTED**: 02 November 2020; **ACCEPTED**: 22 July 2021;

**PUBLISHED ONLINE**: 18 August 2021.

**EDITED BY**: Rémy Beugnon, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION**: Barreto C, Rillig MC, Waldman WR and Maaß S (2021) How Soil Invertebrates Deal With Microplastic Contamination. Front. Young Minds 9:625228. doi: 10.3389/frym.2021.625228

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2021 Barreto, Rillig, Waldman and Maaß. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWERS

### ASTÈRE, AGE: 8

My age is 8. I like reading, doing DIY, drawing, coloring, art, maths, writing, and history. My favorite books are Harry Potter and Percy Jackson.

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### JUNIE, AGE: 10

I have many hobbies but the ones that I do the most are cooking, reading, drawing, and sewing. I go to a primary school in a big city in the UK and my age is 10. My favorite books are Percy Jackson, books by Judy Blume, Scarlet and Ivy, and North child.

<figure><img src="image_276.png" /></figure>
## AUTHORS

### CARLOS BARRETO

At a very young age, Carlos realized that he liked animals, maybe too much. In school, science was always his favorite discipline, all the way through to high school. That is when he decided that he wanted to do something that involved science and animals. He tried to be a vet; it did not work out. No regrets. So, he became an ecologist a few years later, and since then, he has been working with little animals (mostly insects and mites) in tropical forests, iron ore and limestone caves, boreal forests, urban fields, and peatlands on three continents: South America, North America, and Europe. *cbarreto@uwo.ca; †orcid.org/0000-0003-2859-021X

<figure><img src="image_277.png" /></figure>

### MATTHIAS C. RILLIG

Matthias likes soil and all the critters in it, not just the animals. Actually, his favorite are the fungi. His favorite soil process is soil aggregation, the formation of the little crumbs of soil. Matthias is a professor at Freie Universität Berlin and gets to think about soil and what is going on in there all day. Currently he is very interested in how soils are being affected by a wide range of factors, including microplastics. †orcid.org/0000-0003-3541-7853

<figure><img src="image_278.png" /></figure>

### WALTER R. WALDMAN

Walter is a proud Brazilian chemist who loves music, chemistry, food, cinema, and polymers. His first experiment involved chewing gum and the hair of an ex-friend. The experiment did not end well for all the participants, but the adhesive power of polyisoprene was confirmed, and a polymer scientist was born that day. Now he tries to understand the role of polymer degradation on the impact of microplastics. When he has some free time, you can find him reading something about chemistry and polymers. And eating... †orcid.org/0000-0002-7280-2243

<figure><img src="image_279.png" /></figure>

### STEFANIE MAAß

Stefanie wanted to become a make-up artist or costume designer but due to lack of art skills, she moved on to something completely different: biology. When she was introduced to tropical insects and mites of tree bark during her studies, she became fascinated by their beauty and diversity. She then worked on soil insects and mites and has become a passionate and curious soil ecologist who wants to understand the feeding relationships, reactions to pollutants (like microplastics), and distribution patterns of her beloved soil creatures. †orcid.org/0000-0003-4154-1383

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# DIRT IS NOT DEAD: HOW LAND USE AFFECTS THE LIVING SOIL

Jes Hines<fnref n="1" />,<fnref n="2" />* and Franciska T. de Vries<fnref n="3" />

YOUNG REVIEWER:

<figure><img src="image_282.png" /></figure>

KONSTANTIN

AGE: 14

Humans use land to grow crops for food, and the farming methods we use can influence the organisms that live in the soil. Soil organisms do important work, like decomposing organic matter and releasing nutrients for plant growth. By adding more pesticides and fertilizers to farmland, we can produce more crops in a smaller space. But those methods can also harm soil organisms and the work that they do. In contrast, we can use gentler methods to grow crops, which are better for soil animals, but those methods require more land. People in all countries need food from crops to live healthy lives. Because we all share one land surface, when we decide how to use land, we need to remember how agriculture influences soil animals.

<footnote n="1">¹German Centre for Integrative Biodiversity Research (iDiv) Jena-Halle-Leipzig, Leipzig, Germany</footnote>

<footnote n="2">²Institute of Biology, Leipzig Universität, Leipzig, Germany</footnote>

<footnote n="3">³Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, Netherlands</footnote>
Figure 1

The soil food web is composed of many kinds of soil organisms: (1) bacteria, (2) fungi, (3) arbuscular mycorrhizal fungi, (4) protozoans, (5) bacteria-feeding nematodes, (6) fungal-feeding nematodes, (7) root-feeding nematodes, (8) collembolans, (9) predatory nematode, and (10) predatory mites. Arrows point from the organisms that are eaten to the organisms that eats them. Interaction pathways form three main energy channels: bacteria-based channel (orange arrows), fungal-based channel (yellow arrows), and root-based channel (green arrows). The magnifying glass shows that nutrients and energy flow through each soil organism when it eats and respires.

SOIL ORGANISMS

All of the types of life
forms that live below
ground. This includes
single celled organisms
like bacteria, and
multi-cellular
organisms like
earthworms, protozoa,
nematodes, and mites.

ECOSYSTEM
SERVICES

The important things
environments do for
people. In soils
ecosystems, examples
include recycling
nutrients, retaining and
draining water, and
mixing organic matter.

<figure><img src="image_283.png" /><figcaption>Figure 1</figcaption></figure>

7.8 BILLION PEOPLE, AND COUNTING, EAT FOOD THAT GROWS IN SOIL

There are 7.8 billion people and all of them need to eat healthy food. Vegetables and other crops are part of a healthy diet. But producing food for so many people comes with a cost to the environment. First, we need enough farmland and then we need farming practices that keep the environment healthy. The organisms that live in soil can tell us if our farming practices are good or bad for the environment.

In the soil, there are billions of organisms, such as bacteria, fungi, nematodes, and isopods that live in soil (Figure 1). They all eat, and grow, and use oxygen and release carbon dioxide, just like we do. When **soil organisms** carry out these life processes, they release nutrients from their food that are useful for plant growth (Figure 1, inset). They also mix organic matter (i.e., dead plants and organisms) throughout the soil. They improve the structure of the soil, which improves water availability for plants. Soil organisms supply the resources that help plants grow the food that humans like to eat. Soils provide important **ecosystem services**, such as water filtration and nutrient recycling, that help keep humans alive and healthy.

SOIL ORGANISMS FORM A FOOD WEB UNDER YOUR FEET

The organisms in the soil do not work alone; they are connected with each other in a network of interactions called the **soil food web**. Changes in the abundance of one species can affect the abundance of their predators and prey, in a chain of interactions called an **energy channel** (Figure 1). Soil food webs have three main energy channels: one fueled by bacteria, another fueled by fungi, and a third fueled by
Figure 2

Three common ways that natural environments are used. Extensive land use does not involve much plowing and harvesting or the addition of lots of fertilizers and pesticides, and it produces diverse ecosystem services. Medium-intensity land use needs some plowing and harvesting and yields intermediate harvests. High-intensity land use requires lots of work plowing and harvesting, as well as lots of chemical use, to produce a lot of crops from a smaller area. In high-intensity land use, some ecosystem services are reduced in favor of high-output of crop production.

SOIL FOOD WEB

The network of feeding interactions among soil organisms. The interactions start from three main resources (roots, fungi, bacteria) that form energy channels.

TILLING

Preparing soil for agriculture by plowing or digging. Tilling buries weeds and makes it easier for crop roots to enter the soil.

LAND USE

How the natural environment is managed and modified. Examples in text include Intensive land use, extensive land use, and natural areas.

<figure><img src="image_284.png" /><figcaption>Figure 2</figcaption></figure>

plant roots. Bacteria and fungi eat organic matter, such as dead roots and leaves, and later they are eaten by other organisms. There are also organisms that feed directly on living roots, such as root-eating nematodes (tiny worms), which are also eaten by other animals. When humans use the land in a way that disrupts these energy channels (such as by **tilling** the soil or adding fertilizers), they may alter the ability of soil food webs to provide their usual ecosystem services. But how many species are affected by humans and how strong is our effect on the processes soil organisms normally perform?

AN EXPERIMENT TESTING THE EFFECTS OF LAND USE ON
SOIL FOOD WEBS

Scientists hypothesized that different types of **land use** would affect the structure of the soil food webs (Figure 2) [1]. They thought that intensive land use, such as tilling the land, would reduce the number of soil organisms and limit the ecosystem services provided by soils [1]. Scientists also thought that soil organisms would be more abundant when farmers applied extensive land use practices (such as hay meadows and pasture). In extensive land use, there is less plowing and less fertilizer added, but more land area is needed to produce the same amount of food. They thought that soil organisms would do best in natural grasslands, where farmers do not use the land to grow crops [1].

With the goal of using sites exposed to a broad range of environmental conditions (temperature, precipitation, soil texture, etc.), a team of scientists went to four countries across Europe: Sweden, Czechia, United Kingdom, and Greece. In each country, they went to sites with three types of land use: high-intensity agriculture, medium-intensity agriculture, and natural grasslands [1] (Figure 2). At
each site, they measured a variety of soil organisms, including fungi, bacteria, protozoa, nematodes, earthworms, enchytraeids, mites, and collembolans. To find out how the ecosystem services differed between the land uses, they also measured some of the important processes performed by soil organisms.

## INTENSIVE FARMING REDUCES BIODIVERSITY IN THE SOIL

The scientists found that the type of land use was important for the numbers and types of organisms that they found in the soil. They found that more intensive land use reduced the biodiversity of the soil food web: there were fewer groups of organisms present, and within these groups, there were also fewer species [2]. They also found that the total weight of most groups of soil organisms was lower where there was high- and medium-intensity land use. The organisms that are fueled by plant roots were the most reduced, and organisms that eat bacteria and fungi were affected less. This is probably because tilling the soil has strong effects on plant roots in medium- and high-intensity land use, which has extended effects on the organisms that are fueled by plant roots. But how much of the change was due to the direct effects of the tilling on the soil, and how much was due to changes in the soil food webs?

## PROCESSES CARRIED OUT BY SOIL ORGANISMS

To evaluate the question above, the scientists looked at relationships between groups of soil organisms and the processes that these organisms carry out. The scientists focused on two processes: respiration and the cycling of nitrogen. When we are talking about tiny organisms, **respiration** is the name of the process that uses oxygen and releases carbon dioxide, to produce the energy that the organisms need to grow and perform their functions. Nitrogen is an essential element for all life, including plants. It cycles through the environment in several steps. **Mineralization** is the process by which nitrogen is released from organisms into the soil (Figure 3), usually when they decay. Nitrogen in the soil can be lost through **leaching**, which means being flushed out of the soil by water, or by **denitrification**, in which the nitrogen is turned into a gas called nitrous oxide (NO₂) produced by bacteria and escapes from the soil into the atmosphere.

## NATURAL GRASSLANDS ENHANCE SOIL RESPIRATION

First, scientists found that the respiration of soil organisms was higher in natural grasslands and where there were more earthworms in the soil. Earthworms mix the soil, and by doing this, they stimulate the activity of other soil organisms. Just like us, when soil organisms
<caption>Figure 3</caption>

Nitrogen is transformed by soil food webs so that it can move through plants, water, or air. Soil organic matter (dead plants and animals) is mineralized to inorganic nitrogen by the feeding activity of soil organisms. Inorganic nitrogen in soil can be taken up by plants and fungi, or it can be lost from the soil by either leaching into ground water or by conversion to N₂O gas by bacteria, in a process called denitrification.

<figure><img src="image_285.png" /><figcaption>Figure 3</figcaption></figure>

become more active, they need to eat more and respire more. When there is more organic matter available as food, there will be a greater number of active soil organisms. Because natural grasslands have higher organic matter than the fields used for medium- and high-intensity agriculture, respiration was higher in these sites.

## MORE NITROGEN FLOWS INTO AND OUT OF INTENSIVELY MANAGED FARMS

When scientists looked at the cycling of nitrogen, they found that nitrogen mineralization was higher in food webs with a stronger bacterial energy channel (see soil food web in glossary). Bacteria are often very abundant in areas with intensive land use, where they grow quickly and die quickly, releasing the nitrogen from their tissues into the soil.

After they measured the mineralized nitrogen that was released into the soil, the scientists wanted to know how land use affected where the nitrogen went next. They found that, in areas with less intensive land use where there were a lot of arbuscular mycorrhizal fungi, there was less leaching of nitrogen into the water, meaning that more nitrogen stayed in the soil where plants could use it. Farmers want to limit the amount of nitrogen leaching, so that most of the nitrogen can be used by crop plants instead of flowing out of the fields. Arbuscular mycorrhizal fungi are a special group of fungi that attach to plant roots
and help the plant take up nutrients, including nitrogen. These fungi might take up nitrogen from the soil and prevent it from being lost through leaching. So, the presence of arbuscular mycorrhizal fungi could be a good indicator of reduced leaching across different types of land use.

To evaluate the amount of denitrification, scientists measured the concentration of nitrous oxide gas (N₂O). They found lower N₂O concentrations where there was an increased number of flagellates—tiny creatures that use a tail to propel themselves forward in the water that is within the soil and that eat bacteria. Importantly, denitrification is not actually done by flagellates, but by a specific group of bacteria. Because flagellate increased in areas where denitrifying bacteria were not abundant, we may be able to use flagellate abundance as an important indicator of other processes (e.g., denitrification) and soil organisms (e.g., denitrifying bacteria). Understanding what is happening in soil food webs with low concentrations of denitrifying bacteria is important because, when nitrogen leaves the soil as N₂O, it can make climate change worse. N₂O is a greenhouse gas that is 314 times stronger than CO₂!

## INCREASE SOIL BIODIVERSITY TO MINIMIZE THE IMPACTS OF INTENSIVE FARMING

The question of the "right" way to use land to grow vegetables and other crops is an ongoing scientific and social debate. How can humans produce healthy and enough food for billions of people with the minimal impact to the planet? Scientists are learning that soil organisms are sensitive to changes humans make to the environment. Farming practices do not just influence individual organisms, they influence a complex network of species interactions. Changes in this interaction network affect how energy flows through an ecosystem, which nutrients are retained, which nutrients are lost, and how farmers will have to rely on fertilizers and pesticides. While intensive land use takes up less land area, which is positive, it also causes many negative impacts since it decreases soil biodiversity and increases losses of nutrients and carbon. In opposition, lower intensity land use produces fewer crops but is more environmentally-friendly. So, one solution is to restore soil biodiversity in intensive land use areas to make them less dependent on fertilizers and pesticides, which is good for the environment and therefore for humans. So, if you have the possibility to grow your own vegetables you will be protecting the environment because you will not be producing them through intensive agriculture practices. If you cannot plant your vegetables, you can still protect the environment if you can buy vegetables and other crops that are not produced in intensive farmland. Little by little we can make our planet healthier and healthier.
## ORIGINAL SOURCE ARTICLE

de Vries, F. T., Thébault, E., Liiri, M., Birkhofer, K., Tsiafouli, M. A., Bjørnlund, L., et al. 2013. Soil food web properties explain ecosystem services across European land use systems. *Proc. Natl. Acad. Sci. U.S.A.* 110:14296–301. doi: 10.1073/pnas.1305198110

## REFERENCES

1. de Vries, F. T., Thébault, E., Liiri, M., Birkhofer, K., Tsiafouli, M. A., Bjørnlund, L., et al. 2013. Soil food web properties explain ecosystem services across European land use systems. *Proc. Natl. Acad. Sci. U.S.A.* 110:14296–301. doi: 10.1073/pnas.1305198110

2. Tsiafouli, M. A., Thébault, E., Sgardelis, S. P., de Ruiter, P. C., van der Putten, W. H., Birkhofer, K., et al. 2015. Intensive agriculture reduces soil biodiversity across Europe. *Glob. Change Biol.* 21:973–85. doi: 10.1111/gcb.12752

**SUBMITTED**: 06 April 2020; **ACCEPTED**: 13 October 2020;

**PUBLISHED ONLINE**: 09 November 2020.

**EDITED BY**: Malte Jochum, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION**: Hines J and de Vries FT (2020) Dirt Is Not Dead: How Land Use Affects the Living Soil. Front. Young Minds 8:549486. doi: 10.3389/frym.2020.549486

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2020 Hines and de Vries. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWER

### KONSTANTIN, AGE: 14

Hi I am Konstantin, your nearby Young Mind! I am from Rousse, Bulgaria and since I was little I had questions like: what is the point in recycling etc. Now, as an adolescent, I really got into ecology and decided to help bring awareness of some of the problems in our world has like the air pollution, species extinction, and deforestation. If I, an ordinary student, can make a difference you can too-so what are you waiting for my young reader!

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## AUTHORS

### JES HINES

Jes is an ecologist working at the German Centre for Integrative Biodiversity Research (iDiv). Her research focuses on how biodiversity responds to changes in the environment. She is interested in how complex systems grow and how species influence the flux of nutrients, energy, and information through ecosystems.
>jessica.hines@idiv.de

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### FRANCISKA T. DE VRIES

Franciska de Vries is a professor at the University of Amsterdam. Her research focusses on understanding how interactions between plants and soil microbes respond to climate change, and how this affects the functioning of the ecosystem.

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# DOUBLE WHAMMY FOR LIFE IN SOIL? THE EFFECTS OF DROUGHT AND FERTILIZER USE

Marie Sünnemann<fnref n="1" />,<fnref n="2" />*, Julia Siebert<fnref n="1" />,<fnref n="2" /> and Nico Eisenhauer<fnref n="1" />,<fnref n="2" />

YOUNG REVIEWER:

<figure><img src="image_290.png" /></figure>

JEDIDIAH

AGE: 14

For the last two centuries, humans have been changing the Earth through their way of life. Our actions are not only causing climate change and leading to prolonged periods of drought, they are also leading to an overaccumulation of nutrients in soil, due to burning of fossil fuels and fertilization of agricultural fields. Both factors are threatening the world beneath our feet: the soils. They may look rather boring and lifeless, but soils are actually home to many organisms—from tiny bacteria to agile millipedes and slimy earthworms—all of which contribute to processes that are indispensable to life on Earth. For example, the activity of these organisms promotes decomposition of plant material, which ensures that the farmlands on which we grow our food remain fertile. As almost all soil organisms are very sensitive to changes in their environments, we wanted to know what would happen if drought and over-fertilization occurred together.

<footnote n="1">¹Experimental Interaction Ecology, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany</footnote>

<footnote n="2">²Institute of Biology, Leipzig University, Leipzig, Germany</footnote>
### ECOSYSTEM

A community of plants, bacteria, animals, and fungi in a certain location, along with the non-living components of that environment.

### INVERTEBRATES

Animals lacking spines, such as centipedes, woodlice, and earthworms.

### ECOSYSTEM FUNCTIONS

Natural processes that occur in an ecosystem.

### DECOMPOSITION

After death, living organisms are broken down into smaller and smaller pieces. This releases nutrients, which in turn are needed for plant growths.

## HUMAN ACTIVITIES CHANGE ECOSYSTEMS

Over the last 200 years, human activities have changed the world tremendously. Human-induced climate change is causing the planet to warm up, coupled with ever-longer periods of drought (prolonged periods with little rainfall) in some regions. At the same time, the farming of fields and meadows has changed dramatically in recent decades. The world's population is growing steadily, and all these many people need to eat. Therefore, large amounts of fertilizers are applied on agricultural fields today, resulting in much higher crop yields [1]. While they may provide enough food for several billion people, these practices come with a significant drawback: similar to drought, excess fertilization affects not only the plants visible aboveground, but also the complex **ecosystem** belowground—the soil and the organisms living in it.

## THE IMPORTANCE OF THE SOIL ECOSYSTEM

Soils are an important part of terrestrial ecosystems. Although we are often unaware of them, soils are teeming with living things. There are microorganisms, such as bacteria and fungi that are so tiny that they are not visible to the naked eye. What they lack in size, however, they compensate for in number: just one teaspoonful of soil can contain several million soil microorganisms. Even many of the somewhat larger creatures, such as mites and springtails, can only be seen with a magnifying glass. Among the biggest soil animals are woodlice, centipedes, and earthworms. All the somewhat larger soil creatures are united by the fact that they do not have backbones, which is why they are referred to as **invertebrates**. These creatures live together in the soil and interact in various ways: some feed on each other, while others work together.

The soil invertebrates perform numerous tasks that are necessary for our existence. One of the most important of these **ecosystem functions** is **decomposition**, which requires the cooperation of a multitude of creatures. Soil organisms are responsible for the breakdown of dead plant material. Withered leaves, dead roots, and seeds are their food resources. They break down these dead plant materials into smaller and smaller pieces. The resulting tiny compounds, in turn, provide an excellent food source for soil microorganisms like bacteria and fungi. Eventually, these resources are converted back into a form that plants can use for their growth, namely CO2 and nutrients.

All these soil creatures, like almost all life on earth, are highly dependent on water for drinking, for breathing, or even as a means of transportation. Increasingly long and frequent periods of drought are therefore a problem for many small organisms. And even worse, what happens if other harmful factors occur at the same time? Excessive
Figure 1

In half of the experimental plots in our study, we used roofs to simulate drought. The other half of the plots received “fake” roofs with rain panels put upside-down to account for the potential side effects of these roof structures (like changes in wind speed and light). ©Julia Siebert.

PH VALUE

A scale indicating whether a solution has an acidic or basic character. The lower the value, the more acidic the solution is.

<figure><img src="image_291.png" /><figcaption>Figure 1</figcaption></figure>

use of fertilizer, for example, can be harmful to soil organisms, as it changes the **pH value** of the soil to make it more acidic. Many soil organisms cannot tolerate acidic soil conditions. Could fertilization add a further stress factor, making it even harder for soil organisms to withstand dry conditions? And how exactly can we learn whether drought and fertilization are harmful to soil organisms and interfere with their functions?

HOW DID WE STUDY SOIL MICROORGANISMS?

To understand the effects of drought and fertilization on soil
organisms, we started an experiment that simulated these two
common factors that humans change [2]. We chose a meadow in
Central Germany where we selected small areas called experimental
plots and treated the plots in different ways. One-fourth of the
experimental plots were treated with drought using roofs (Figure 1),
another fourth was treated with fertilizer, and yet another fourth was
treated with a combination of drought and fertilizer. The last fourth
was not treated at all, which was our control plot. Control plots
are important because they allow us to compare the treatments to
normal conditions.

To understand how drought and fertilization affect soil organisms, we looked at soil invertebrates and soil microorganisms separately. We examined the activity of soil invertebrates in each of our plots. To do this, we used narrow plastic strips with several small holes in them, called bait lamina test strips. Every hole was filled with a bait mixture, which soil invertebrates like to eat—imagine invertebrate cereal. We stuck some bait lamina test strips completely into the ground of our plots (Figure 2). After 3 weeks, we observed the amount of the bait that had been eaten by the soil animals. Soil ecologists use this method to assess how much soil invertebrates eat, which is a very good indicator of their activity in general.
<caption>Figure 2</caption>

To determine the activity of soil invertebrates in our experimental plots, we used bait lamina strips. The strips were completely inserted into the ground for soil invertebrates to feed on. After 3 weeks, we checked how many of the little holes containing the bait were full, empty, or half-empty. The more active and hungrier the soil invertebrates, the more of the bait was eaten.
©Gottschall/Siebert.

<figure><img src="image_292.png" /><figcaption>Figure 2</figcaption></figure>

To examine the soil microorganisms more closely, we took a small amount of soil from each of our plots back to the lab. We determined the microbial activity in these samples by measuring their respiration. Just like humans, soil organisms breathe in oxygen (O₂) and exhale carbon dioxide (CO₂), so the more respiration that is happening in a sample, the more active are the microorganisms (think of yourself exercising). To measure microbial respiration, we used a device with a special sensor that can measure the amount of oxygen used by the microorganisms, and these data were then transferred to a computer for storage. By knowing the activity of the soil microorganisms, we were then able to calculate their **biomass**, which is a measure for the amount of all microbes that live in a defined amount of soil, for example on a teaspoon.

## DROUGHT AND FERTILIZATION CAN AFFECT SOIL INVERTEBRATES

We used statistical tests on our data to find out how the microbial and invertebrate soil communities reacted to drought and fertilization. We found that both drought and fertilization severely disrupt the activity of soil invertebrates. Although the factors on their own had strong

### BIOMASS

Measure for the amount of all microbes that live in a defined amount of soil.
<caption>**Figure 3**</caption>

What did we find? (A) Drought, fertilization, and both together strongly reduced the feeding activity of soil invertebrates. (B) Soil microorganisms were not disturbed by the drought treatment. Fertilization caused an increase in the soil microbial biomass.

<figure><img src="image_293.png" /><figcaption>Figure 3</figcaption></figure>

negative effects, their combination did not reduce invertebrate activity any further (Figure 3A). Soil microbes, however, reacted completely differently. Drought could not harm them, and additional fertilization even increased their biomass (Figure 3B).

Why do drought and fertilization harm invertebrates much more than microorganisms? Usually, both groups are highly dependent on soil moisture and have trouble coping with droughts. Among other things, their food becomes so dry that they have difficulty digesting it [3]. Imagine eating old toast without jam all day, without drinking anything with it. To avoid drought conditions, invertebrates may travel to deeper, moister soil layers that we did not reach with our tests. However, why did fertilization lower their activity as well? The reason is that fertilization leads to an acidification of soils, which means that the pH value falls below five. Earthworms and many other soil invertebrates do not like to live in low-pH conditions, which can be damaging to their delicate skin. A lemon, for example, has a pH value of 2. Have you ever had a cut on your finger and then gotten lemon juice on it? Not very pleasant.

The drought treatment did not harm soil microorganisms. This took us by surprise, because our treatment reduced the annual rainfall by half, which naturally led to extremely dry soils. However, we think it is possible that bacteria and fungi that normally live in the upper layer of
the soil are constantly exposed to the temperature and humidity cycles of the seasons. For this reason, they must be able to survive even the driest periods [4]. One way that they do this is by building themselves a sugary protective shell that prevents their surfaces from drying out. Alternatively, they can create a very resistant form that allows them to survive, called a spore. Spores are in a dormant state and can outlive extreme heat and drought for up to 1,000 years. This is why we believe the drought conditions of our experiment hardly harmed the soil microorganisms. But it is also possible that our experiment was too short to see any negative effects of the drought.

Fertilization, on the other hand, was even beneficial for the microorganisms. This is because the additional nutrients from the fertilizer strongly promoted plant growth. Not only did the plants respond with longer shoots, larger flowers, and many more leaves, they also released more resources into the soil via their roots and the microorganisms could feed on all these extra food sources.

We were happy to find that drought and fertilizer did not reinforce each other's effects, which means that both factors together do not seem to do more harm than either does on its own. This may mean that ecosystems have some great coping mechanisms to use against harmful environmental attacks. But in this study, we only measured the activity of soil organisms after 1 year. We should examine the soil after many years of drought and fertilization, to see if the results are still the same.

## WHAT WILL THE FUTURE HOLD FOR OUR SOILS?

To sum up, larger soil invertebrates seem to be much less well-equipped for future environmental changes than microorganisms are. What does this mean for our soils in the future? The decline in the activity of soil animals has several consequences for ecosystems and therefore for humans. As we have already learned, all organisms in the soil are necessary to keep the process of decomposition running. The decomposition process is divided into several steps, which are indispensable for one another. While invertebrates are mostly responsible for breaking down larger pieces of dead animals and plants, microorganisms digest the smaller pieces in the next step and release a range of nutrients. Together, the soil organisms form a large feeding community, in which each species has its own special place, fulfilling their specific tasks. However, if one link in this chain is missing, the whole system is likely to lose its balance [5]. This could mean that soils could lose their fertility in the long term. The result would be that not only grasses but also the wheat and maize in our fields would no longer grow so luxuriantly, and we would eventually have problems feeding all the people on Earth. We are therefore dependent on the well-being of all soil creatures and should keep
their importance in mind as we make future decisions that could affect
our soils.

ACKNOWLEDGMENTS

We thank the staff of the Bad Lauchstädt Experimental Research
Station for their help in maintaining the experimental site, and Alla
Kavtea, Tom Künne, and Ulrich Pruschitzki for their support with
lab and field work. Furthermore, we thank the coordination of the
International Drought-Net Experiment for providing protocols and
support. We acknowledge editorial help by Susan Debad.

ORIGINAL SOURCE ARTICLE

Siebert, J., Sünnemann, M., Auge, H., Berger, S., Cesarz, S., Ciobanu, M., et al. 2019. The effects of drought and nutrient addition on soil organisms vary across taxonomic groups, but are constant across seasons. *Sci. Rep.* 9:639. doi: 10.1038/s41598-018-36777-3

REFERENCES

1. Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., et al. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. *Science* 320:889–92. doi: 10.1126/science.1136674

2. Siebert, J., Sünnemann, M., Auge, H., Berger, S., Cesarz, S., Ciobanu, M., et al. 2019. The effects of drought and nutrient addition on soil organisms vary across taxonomic groups, but are constant across seasons. *Sci. Rep.* 9:639. doi: 10.1038/s41598-018-36777-3

3. Thakur, M. P., Reich, P. B., Hobbie, S. E., Stefanski, A., Rich, R., Rice, K. E., et al. 2018. Reduced feeding activity of soil detritivores under warmer and drier conditions. *Nat. Clim. Change* 8:75–8. doi: 10.1038/s41558-017-0032-6

4. Tonkin, J. D., Bogan, M. T., Bonada, N., Rios-Touma, B., and Lytle, D. A. 2017. Seasonality and predictability shape temporal species diversity. *Ecology* 98:1201–16. doi: 10.1002/ecy.1761

5. Simpson, J. E., Slade, E., Riutta, T., and Taylor, M. E. 2012. Factors affecting soil fauna feeding activity in a fragmented lowland temperate deciduous woodland. *PLoS ONE* 7:e29616. doi: 10.1371/journal.pone.0029616

SUBMITTED: 31 March 2020; ACCEPTED: 27 August 2020;

PUBLISHED ONLINE: 08 October 2020.

EDITED BY: Helen Phillips, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION:** Sünnemann M, Siebert J and Eisenhauer N (2020) Double Whammy for Life in Soil? The Effects of Drought and Fertilizer Use. Front. Young Minds 8:547630. doi: 10.3389/frym.2020.547630
**CONFLICT OF INTEREST:** The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2020 Sünnemann, Siebert and Eisenhauer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWER

### JEDIDIAH, AGE: 14

Jedidiah is interested in science and math, particularly in how the environment impacts his daily life. He spends time working in the family garden, making money by selling eggs and vegetables he helps produce. In his spare time, Jed likes to play baseball and play video games.

<figure><img src="image_294.png" /></figure>

## AUTHORS

### MARIE SÜNNEMANN

When she was 6 years old, her best friend challenged her to a dare: to eat an earthworm. Even though she would not do that today, her curiosity about everything that creeps and crawls belowground has never waned. Today, as a doctoral student, she studies the reactions of soil organisms to climate change in meadows and agricultural fields. In her free time, she does combat sports and enjoys being outside. *marie.suennemann@idiv.de

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### JULIA SIEBERT

Julia has been fascinated by nature since she was a child. She spent as much time as possible outdoors, built moss houses in the forest, and searched for all kinds of animals. She followed this passion by studying biology and communication science and was always keen on finding ways to transfer knowledge to different audiences. Her scientific studies focused on how changing climate conditions affect soil organisms and the ecosystem functions they drive. Furthermore, she explored ways to engage school students in biodiversity science. In her free time, she enjoys horse-riding, traveling, birdwatching, mountain biking, and all sorts of outdoor sports.

<figure><img src="image_296.png" /></figure>

### NICO EISENHAUER

Nico has been interested in nature since his early childhood. He dug for earthworms, caught frogs and fish, and helped lizards survive the winter months. He has always been fascinated by the beauty of nature and driven by the question of why a specific plant or animal species occurs in one place, but not in another. During his study of

<figure><img src="image_297.png" /></figure>
biology, he discovered his interest in soil animals and their important activities that are crucial for the functioning of ecosystems. When not at work, Nico likes playing soccer and badminton, running, and spending time with his family and friends.
<figure><img src="image_298.png" /></figure>

# SOIL ORGANISMS HAVE FAVORITE FORAGE PLANTS

Felicity V. Crotty*

School of Agriculture, Food and Environment, Royal Agricultural University, Cirencester, United Kingdom

## YOUNG REVIEWERS:

<figure><img src="image_299.png" /></figure>

JACK

AGE: 13

<figure><img src="image_300.png" /></figure>

SOPHIA

AGE: 15

Cows and sheep eat plants known as forages. Forage plants can include grass, chicory, and clover. Forage plants vary in nutrients and tastiness. These plants can also change the ecosystem belowground for soil animals. Soil animals may move to eat or live beneath different forages. Earthworms mix up the soil and food, improving the soil habitat. Fungi break down dead plants, and organisms that eat fungi speed up this breakdown process, which creates more food for other plants and soil animals. We tested which forage plants soil animals preferred. Large numbers of earthworms were found under white clover. Tiny fungal-feeding worms and springtails (insect-like creatures) were found in greater numbers under clover and chicory. Plant-eating soil animals compete with cows and sheep for food. These plant-eaters were found in larger numbers below ryegrass. Growing plants that increase the numbers of helpful soil animals can lead to healthier soils.
## Figure 1

Weight of soil animals per hectare (ha), measured in sheep. Adult sheep weigh around 60 kg [1]. The soil organisms in one hectare weigh around 53 sheep [2]. The standard for farming is around 16 sheep per hectare so, added up, the weight of soil organisms is more than the weight of sheep above ground, per hectare.

<figure><img src="image_301.png" /><figcaption>Figure 1</figcaption></figure>

## FORAGE/FORAGE PLANTS

Plant material eaten by grazing animals, like cows and sheep.

## ECOSYSTEM SERVICES

The important things environments do for people and animals. In soil ecosystems, examples include recycling nutrients, retaining and draining water, and mixing dead plant material into the soil.

### TAP ROOT

A large, wide, main root, tapering in shape and growing directly downwards (similar to a carrot).

### SOIL ORGANISMS

All the organisms that live below ground, including tiny microorganisms like bacteria, fungi, protozoa and nematodes, medium-sized organisms like springtails and mites, and large organisms like earthworms.

## SO MANY SOIL ANIMALS!

Cows and sheep eat a wide-ranging diet that depends on the types of plants growing within a field, which are called **forage plants** or simply **forages**. The most common forage plant is grass (ryegrass), but others include clover and chicory. These plants vary in their tastiness and nutrient content, which gives cows and sheep a choice of food and provides a healthy, varied diet. In addition, forage plants provide **ecosystem services**. For example, clover creates its own nitrogen fertilizer to help itself (and other plants) to grow. Chicory has a deep **tap root** that helps increase the airflow within the soil.

Taken together, the soil animals that live below ground weigh more than the sheep and cows above them (Figure 1)! These soil animals eat lots of different foods, and they choose to live in different places because of the plants growing there. Imagine living in a city: in some areas there are lots of people living close together, while in other areas there are fewer people. Some people like to be close to resources like schools, work, and shops. However, some may prefer to live in less crowded areas. The same is true for soil animals. When resources are limited or poor, soil animals may move to find more or better ones. Soil animals also provide important ecosystem services within the soil. For example, they break down dead plant material, recycle nutrients, and improve soil structure.

Forage plants provide a stable habitat for **soil organisms**. After they are planted, forages grow and are grazed for many years, without disturbing the soil. There is a large diversity of soil animals that all have different roles within the soil. Earthworms are the superheroes of the soil, or “ecosystem engineers.” They change the whole soil habitat, mixing soil, and moving air and food within it. Springtails and mites
## NUTRIENT CYCLING

Movement and exchange of various nutrients between the living and non-living parts of an ecosystem. Nutrient cycling helps plants grow.

## TULLGREN FUNNEL

Device in which the soil is warmed up and the small soil animals move away from the heat and light, falling into a collection pot under the funnel.

## ANECIC

Group of large earthworms that create deep vertical burrows that go up and down through the soil, moving dead plant material around to eat later.

help to break down dead plant material, making the soil stick together properly, and disperse fungi. Nematodes (tiny worms) eat fungi and bacteria, speeding up **nutrient cycling**. The number of organisms that live within the soil can be an indicator of soil health. Increasing the number of soil organism can lead to better soil health and can help plants grow.

## DO SOIL ORGANISMS HAVE FAVORITE FORAGE PLANTS?

Since there have not been many studies looking at the effects of forage plant species on soil organisms, we decided to do an experiment. We grew forages of ryegrass, chicory, red clover, and white clover in separate plots. These plots were next to each other in the same field. There were four plots for each forage. The plants grew for 3 years, during which the forages were cut regularly, to simulate grazing by sheep and cows. After 3 years, soil animals (earthworms, springtails, mites, insects, and nematodes) were measured within each plot, to see which forage plants they preferred.

Different sampling methods were used to count the soil animals. For earthworms, we dug up a square cube of soil and sorted through it, picking out all the earthworms we could find. Earthworms were then sorted into groups, based on their size and color. To collect springtails, mites, and other small insects, we took small soil samples and placed them on **Tullgren funnels**. You can make your own Tullgren funnel at home by following instructions in Barreto and Lindo [3]. We had to identify these soil animals with a microscope because they are so small. Nematodes were collected by placing soil within tissue paper and resting it in a tray of water. The nematodes swam out of the soil into the water, where we collected them and identified them under a microscope.

## WHITE CLOVER INCREASES THE NUMBER OF SOIL ANIMALS

Our results are summarized in Figure 2. The most earthworms were found in the white clover plots, and the fewest in the ryegrass plots. Earthworm numbers in the soil below the chicory and red clover forage plots were in-between. The deep-burrowing (**anecic**) earthworms showed the most plant preferences compared to other kinds of earthworms. Dividing the nematodes into feeding groups, showed some had favorite forages. Larger numbers of fungal-feeding nematodes were found below the clovers compared to the ryegrass. Plant-eating nematodes were found in larger numbers below the ryegrass compared to the clovers or chicory. Thousands of springtails and mites were found per square meter of soil. Two groups of springtails were found in different numbers in the soil below the
<caption>Figure 2</caption>

Differences in soil animal numbers below ryegrass, chicory, red clover, and white clover forage plants. Ryegrass had the most plant-eating soil animals (true bugs, thrips, and plant-feeding nematodes). White clover had the most earthworms, fungal-feeding nematodes, and Poduromorpha springtails. Red clover had in-between numbers of earthworms, fungal-feeding nematodes, and Poduromorpha springtails. Red clover had a larger number of predatory mites than the other forages. Chicory had in-between numbers of earthworms but fewer of the other organisms than the clovers (Plant pictures adapted from Cotswold Seeds).

<figure><img src="image_302.png" /><figcaption>Figure 2</figcaption></figure>

## PODUROMORPHA

Group of springtails that look fat and have a small springing tail, mostly eat fungi, bacteria, and dead plant material.

A group of springtails called **Poduromorpha**, which eat fungi, bacteria, and dead plant material, were found in larger numbers below the clovers. Plant-eating springtails (Symphypleona) were found in larger numbers below the ryegrass. Greater numbers of predatory mites were also found below the red clover plants. "Other" invertebrates were found to differ in numbers in the soil below the forages. The ryegrass plants had many more "other" invertebrates in the soil than either red clover or chicory. There were large numbers of bugs and thrips (tiny plant eating insects) below the ryegrass plots compared to the other forages.

We calculated the total soil animal biodiversity for each forage and found that the lowest animal diversity was found in the ryegrass soil and the highest was in the soils of the two clovers. The diversity of soil animals below chicory was in-between.

## HEALTHY SOIL ORGANISMS = HEALTHY AGRICULTURE

Large and diverse populations of soil organisms are thought to improve soil health, which could lead to increased crop growth. It is important to monitor soil animal numbers to see if they are affected by the types of forages grown by farmers. This will tell us whether changes in the types of plants farmers choose to grow might affect the health of the soil. Our findings show that soil animal numbers change depending on the type of forage plants grown. This means that changes in plant species can influence the biodiversity of the soil animals living under those plants.

All plants were located next to each other within the same field, so the soil animals could move to live below whichever forage plants they preferred. Three years of plant growth led to changes in the
soil habitats, because the four forages had different root structures and changed the nutrient availability in the soil. The moving speeds of soil animals vary. For example, earthworms can move more than 1m per day, but some species of mites only move 1-8m per year [4, 5]. The earthworms found below white clover had time to move there during the three-year experiment. However, some of the other animals may not have had enough time to reach their favorite forage crop to live below it. Earthworm numbers reflect how much food is available. The larger numbers found under white clover suggest there is more food there. Since earthworms can improve soil structure, larger numbers of earthworms could improve soil health [6]. Plants can use the deep burrows of anecic earthworms as ready-made channels for their roots to grow into. Forage plants that draw large numbers of anecic earthworms could therefore improve other plants growth.

Maintaining a high diversity of soil animals is important. If soils experience a loss in soil animal biodiversity due to poor soil management, this could reduce the ability of the soil to grow plants, store water and cycle nutrients. Our research showed that changing the type of forage plants being grown could help to maintain soil animal biodiversity and therefore help to keep soils healthy. Healthy soils are important because they support the growth of crop plants. This means that choosing the right forage plants could ultimately help farmers grow enough food to feed the growing human population!

## FUNDING

This research was undertaken as part of the PROSOIL project (Project Ref. A AAB 62 03 qA731606). This work was funded through the Rural Development Plan for Wales 2007-2013, funded by the Welsh Government and the European Agricultural Fund for Rural Development.

## ORIGINAL SOURCE ARTICLE

Crotty, F. V., Fychan, R., Scullion, J., Sanderson, R., and Marley, C. L. 2015. Assessing the impact of agricultural forage crops on soil biodiversity and abundance. *Soil Biol. Biochem.* 91:119-26. doi: 10.1016/j.soilbio.2015.08.036

## REFERENCES

1. Schon, N. L., Mackay, A. D., Minor, M. A. 2011. Soil fauna in sheep-grazed hill pastures under organic and conventional livestock management and in an adjacent ungrazed pasture. *Pedobiologia*. 54:161-8. doi: 10.1016/j.pedobi.2011.01.001
2. Crotty, F. V. 2021. "Assessing soil health by measuring fauna," in Otten, W. (Ed.), *Advances in Measuring Soil Health* (Cambridge: BDS Publishing).

3. Barreto, C., and Lindo, Z. 2020. Armored mites, beetle mites, or moss mites: the fantastic world of oribatida. *Front. Young Minds*. 8:545263. doi: 10.3389/frym.2020.545263

4. Caro, G., Decaens, T., Lecarpentier, C., and Mathieu, J. 2013. Are dispersal behaviours of earthworms related to their functional group? *Soil Biol. Biochem.* 58:181-7. doi: 10.1016/j.soilbio.2012.11.019

5. Lehmitz, R., Russell, D., Hohberg, K., Christian, A., and Xylander, W. E. R. 2012. Active dispersal of oribatid mites into young soils. *Appl. Soil Ecol.* 55:10-9. doi: 10.1016/j.apsoil.2011.12.003

6. Blouin, M., Hodson, M. E., Delgado, E. A., Baker, G., Brussaard, L., Butt, K. R., et al. 2013. A review of earthworm impact on soil function and ecosystem services. *Eur J Soil Sci.* 64:161-82. doi: 10.1111/ejss.12025

**SUBMITTED**: 29 January 2021; **ACCEPTED**: 14 February 2022;

**PUBLISHED ONLINE**: 18 March 2022.

**EDITOR**: Helen Phillips, Saint Mary's University, Canada

**SCIENCE MENTOR**: Patricia Welch Saleeby

**CITATION**: Crotty FV (2022) Soil Organisms Have Favorite Forage Plants. *Front. Young Minds* 10:660785. doi: 10.3389/frym.2022.660785

**CONFLICT OF INTEREST**: The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2022 Crotty. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWERS

### JACK, AGE: 13

My name is Jack. I am interested in coding, programming, and cybersecurity. I participate in science and math competitions like Science Olympiad and Math League. I am an avid basketball player. I love to travel and have visited 4 of the 7 continents so far.

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## SOPHIA, AGE: 15

My name is Sophia. I am on the pre-med pathway in high school. I compete in Science Olympiad, Quiz Bowl, and the Science Fair. I have a love for spelling. I won my school spelling bee multiple years and competed in the Scripps national spelling bee. For relaxation, I enjoy doing art projects and baking culinary treats for my friends and family. I also love to travel. One of my favorite places is Tokyo.

## AUTHOR

### FELICITY V. CROTTY

Dr. Felicity Crotty is a senior lecturer in soil science and ecology at the Royal Agricultural University. She has been researching soil biology and soil health for the last 14 years, focusing on understanding the linkage between sustainable agriculture and soil health, within both the animal and crop sectors. *felicity.crotty@rau.ac.uk

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# HOW INTRODUCED EARTHWORMS ALTER ECOSYSTEMS

Malte Jochum<fnref n="1" />,<fnref n="2" />* and Nico Eisenhauer<fnref n="1" />,<fnref n="2" />

## YOUNG REVIEWERS:

<figure><img src="image_307.png" /></figure>

LILU

AGE: 10

<figure><img src="image_308.png" /></figure>

MICHELLE

AGE: 16

We all know earthworms as important friends in our garden: they help plants to grow better by providing nutrients, water, and air in the soil. However, in some cases, earthworms have more negative effects. This is because other organisms need to be used to the activities of earthworms to benefit from their presence. Some regions of the world have developed without earthworms for over thousands of years. For example, in northern North America, earthworms have been absent for more than 10,000 years and have only been re-introduced over the past ~400 years. In many cases, introduced earthworms find a perfect environment, because no other organisms have been able to use the resources that these earthworms now consume. As so-called ecosystem engineers, earthworms dramatically alter many ecosystem characteristics. In this article, we summarize the known consequences of earthworm invasion, report on how scientists study these, and highlight remaining knowledge gaps that you might help solving should you decide to become an ecologist.

<footnote n="1">¹German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany</footnote>

<footnote n="2">²Institute of Biology, Leipzig University, Leipzig, Germany</footnote>
## ECOSYSTEM FUNCTION

A process that takes place in an ecosystem and either represents, or is driven by, the activity of organisms. Examples include the decomposition of organic material, nutrient cycling, or water retention.

## PERTURBATION

A disturbance, in ecology usually a disturbance to an equilibrium state, or any level of biological organization (individual, population, community, ecosystem).

## BIODIVERSITY

The variety of life on earth, usually measured as variability at the genetic, species, or ecosystem level.

## ECOSYSTEM ENGINEER

An organism that modifies its environment by redistributing material and energy via non-feeding interactions with living and dead components of its ecosystem.

## BURROWING

Tunnel-building activity of earthworms.

## CASTING

The activity of building small piles of earthworm droppings on the soil surface and in the soil.

## MIXING

The activity of redistributing different parts of the soil with each other and organic material from the soil surface.

## INTERACTING ORGANISMS HELP ECOSYSTEMS PROVIDE SERVICES TO HUMANS

Within an ecosystem, different species interact, for example by eating, helping, or providing habitat for each other. Every species consumes its resources and is eaten by other species. They all have their unique roles in nature. Some species have particularly important roles in ecosystems because they eat dead leaves or animals. These species recycle materials and provide them back to the ecosystem. Other organisms help plants to produce flowers and seeds. All organisms carry out **ecosystem functions**, such as decomposition, pollination, and many others. We humans rely on the functions and services that intact ecosystems provide to us. However, these services depend on the diversity and interactions of the species present. **Perturbations** to an ecosystem can alter its **biodiversity** and the interactions of species within it. Changing climate (e.g., higher temperature), altered land use (e.g., transforming forests into agricultural fields), or species invasions (the introduction of new species to an ecosystem) all have the potential to disrupt ecosystems in ways that can alter their functions and the services they provide.

## INVASIVE SPECIES CHANGE ECOSYSTEMS

An invasive species is a species that arrives in a new environment, establishes itself, substantially increases in abundance, and forms novel interactions there, significantly altering the invaded ecosystem. Species invasions are one of the most important causes of global biodiversity change. Invaded ecosystems are changed by things like the establishment of new feeding relationships, the replacement of natural plants by dominating invasive plants, the disappearance of previously-established species, or the facilitation of further invasions. The effects of species invasions are strongest if the invasive species differs a lot from the species already living in the ecosystem [1]. Differences could include resource use, robustness to stressors, growth speed, or the ability to eat food that the other species cannot digest. Some invasive species have particularly strong effects because they actively alter their environment by creating or modifying habitats. Such species are called **ecosystem engineers**. Examples are beavers, which build dams and temporarily turn terrestrial habitats into freshwater ones, and earthworms, which alter soils by **burrowing** (building tunnels), **casting** (building small piles of their droppings on and in the soil), and **mixing** dead plant material on the ground with the soil below [2].
EARTHWORMS ARE VERY IMPORTANT FOR SOIL
ECOSYSTEMS—IN A GOOD OR BAD WAY

Earthworms naturally occur in most terrestrial ecosystems around the globe. They constantly structure the soils that they live in. Their burrowing activities mix the soil and improve the flow of air and water through the underground world. By eating dead organic material from the soil surface, dragging it down into the soil, digesting it, and then leaving their droppings, they redistribute nutrients throughout the soil. These activities affect other life below and above the ground. The altered air, water, and nutrient availability changes how other organisms can use their resources, where they can live, and how well they can grow and reproduce. Through these activities, earthworms influence bacteria, fungi, springtails, mites, beetles, plants, and even animals that live above the soil surface, such as aphids. Consequently, earthworms are very important soil organisms<fnref n="1" /> with impacts beyond the belowground world. This is fine in areas where the other organisms are used to having earthworms around, but it can become problematic where they are not used to these squishy neighbors.

INVASIVE EARTHWORMS ARE A GLOBAL ISSUE

In many places, earthworms are considered "the gardener's best friend." They commonly improve soil quality in gardens, fields, meadows, and forests. Other organisms have shared these ecosystems with the earthworms for a very long time, and are used to their presence and activity. Hundreds of earthworms and up to a dozen earthworm species per square meter can be found in these ecosystems, but this is not the case everywhere in the world. Some places have a low number of earthworms, and in other areas earthworms are completely absent [3]. In areas where earthworms are naturally rare or absent, introduced earthworm species can become a big problem [4]. This is because, in these places, microbial, plant, and animal species are not used to having earthworms around. The native species may not be able to deal with the changes the earthworms make to the soil's water, air, and nutrient availability. It is important to study the effects of earthworm invasion on ecosystems and predict their future impact because it is impossible to remove earthworms from areas where they have established without killing other animals and plants.

NORTHERN NORTH AMERICA IS BEING INVADED BY
EARTHWORMS

Huge parts of the northern USA and Canada were covered by vast ice sheets during the last glaciation period (Figure 1). Under these ice sheets, earthworms could not survive. Thus, at least since the ice disappeared about 12,000 years ago, most of North America has been

<footnote n="1">1 Clay video by
Maxwell
Helmberger:
https://www.
youtube.com/watch?
v=3a7lFGOYL7s&
list=PLB9tSz89_6
_qBS8RRF0h5YZhy
C31KJHoc&
index=5</footnote>
<caption>**Figure 1**</caption>

Approximate extent of the northern North American ice shield during the last glacier period. The graph at the lower left shows the approximate maximum thickness of the ice sheet in comparison to the highest building in North America (546 m, One World Trade Center, New York City, USA). The thickness of the ice sheet varied across time and space during the glaciation. Original satellite image by NASA, from wikipedia.org.

<figure><img src="image_309.png" /><figcaption>Figure 1</figcaption></figure>

² MinuteEarth video: https://www.youtube.com/watch?v=icGV8bJRkkg

naturally earthworm-free. Natural reintroduction of earthworms takes a long time, because they spread slowly into new habitats (<10 m per year). However, when the European settlers arrived in North America, they accidentally and/or intentionally brought earthworms with them². Once introduced, the earthworms liked many of these areas a lot. The forests had thick layers of not-yet-decomposed organic matter (dead remains of formerly living stuff), which was a great feast for the earthworms (Figure 2). They made themselves at home and their numbers grew rapidly. By building roads, moving soil, moving plants, and similar activities, the settlers actively distributed earthworms throughout the northern part of the continent much faster than the earthworms could have traveled on their own. In some areas, earthworms were likely introduced by fishermen, who may have dropped their unused bait close to lakes, streams, or fishing cabins. As a result, the spread of earthworms was helped by humans who did not know or did not care what ecosystem-scale effects these newcomers would have.
**Figure 2**

Illustration of how invasive earthworms alter previously earthworm-free ecosystems. By burrowing, feeding on leaf litter, and mixing soil, earthworms affect the soil properties causing changes in soil layers, vegetation, and soil organisms. These changes affect ecosystem processes, such as greenhouse-gas emissions and loss of nitrogen (N leaching) from the soil. Increasing atmospheric levels of greenhouse-gases, e.g., carbon dioxide or nitrous oxide, are an environmental issue. Different functional groups of soil animals, shown in the black center box (size groups from large to small: macrofauna—e.g., spiders and woodlice; mesofauna—e.g., springtails and mites; microfauna—e.g., nematodes, and microorganisms—e.g., bacteria and some fungi), are affected by the three ecological groups of earthworms (epigeic—live in leaf litter and on the soil surface, endogeic—build mostly horizontal burrows in upper soil layers, and anecic—build deep, vertical burrows; see right panel). What changes can you spot? Originally published in Ferlian et al. [5], reproduced with the permission of the original publisher.

<figure><img src="image_310.png" /></figure>

## RESEARCHERS STUDY HOW EARTHWORMS CHANGE ECOSYSTEMS

Scientists have been studying earthworm invasions for many decades, using three different approaches: First, in field observation studies, researchers compare uninvaded to similar, already invaded ecosystems. Second, in field experiments, researchers compare small areas without earthworms to areas nearby where they experimentally release earthworms. Alternatively, they first measure ecosystem properties, then release earthworms there and then measure the same properties again. Another approach is to keep small patches of soil and plants in laboratories under controlled conditions, with light, water, and temperature controlled by researchers. Some patches then receive earthworms and others do not so that they can be directly compared. In all these approaches, researchers can assess the ways that earthworms change ecosystems, such as how earthworms alter the **physical**, **chemical**, and **biological properties** of soils, and various ecosystem functions. All these different approaches and measurements help us to better understand how invasive earthworms change their new homes.

## WHAT DO WE ALREADY KNOW?

We already know quite a lot about how earthworms change the chemical and physical properties of the soil. Earthworms create soils that are warmer, drier, and less acidic, and they alter the availability
Figure 3

Extreme example of the potential consequences of earthworm invasion in a maple forest in Minnesota, USA. The upper panel shows an uninvaded forest area, the lower panel shows a forest area invaded by European earthworms. Photo credit: Ulrich Pruschitzki (top) and Olga Ferlian (bottom), altered after [6].

Uninvaded

<figure><img src="image_311.png" /></figure>

Invaded

<figure><img src="image_312.png" /><figcaption>Figure 3</figcaption></figure>

PHYSICAL SOIL
PROPERTY

Soil properties related to matter, energy, or force. For example, the water or air content.

CHEMICAL SOIL
PROPERTY

Soil properties related to elements and compounds of atoms, molecules, and ions. For example, the availability of different nutrients and elements, or acidity.

BIOLOGICAL SOIL
PROPERTY

Soil properties related to living things. For example, the number of species present, their biomasses, or interactions.

of soil nitrogen and carbon, two very important chemical elements. In addition, earthworm invasion often reduces the number of other soil organisms and the number of different animal and plant species (Figures 2, 3). Not all organisms are negatively affected though. For example, oribatid mites and springtails are often reduced, but prostigmatid mites are increased where earthworms have invaded. Also, some species locally disappear, but other species, particularly those that are used to the presence of earthworms, might follow the earthworms' example and become invasive. Earthworm invasion can cause a cascade of ecosystem consequences that are also relevant to humans, such as altered water quality and the likelihood of forest fires [6]. We know that invasive earthworms reduce the number of plant species, but they increase the importance of grass-like plants and the number of non-native plants. Earthworms also influence large animals, such as salamanders and birds that nest on the soil surface. While some salamanders can use earthworm burrows to hide and feed on earthworms, the nests of ground-nesting birds can be destroyed by earthworms burying leaf litter, which is the primary nest-building material.
## EARTHWORM INVASION RESEARCH CONTINUES ...

It takes time to study ecosystem responses to perturbations—studies often need to run for many years. This is why, despite decades of research on the effects of invasive earthworms on their new homes, there is still a lot that we do not know [7]<fnref n="3" />. We know more about how earthworm invasion affects the physical structure, other organisms, and ecosystem functions below the ground than above. We also do not know a lot about how earthworm invasion changes the way above- and below-ground systems interact, or how energy flows through the networks of organisms eating each other. While we know how earthworm invasion alters the plant community as a whole, we do not know much about how it influences the characteristics of individual plants, such as the size of their leaves, which is very important for plant life and function (e.g., photosynthesis). Most of our knowledge is based on observational studies and laboratory experiments because field experiments are often difficult to run and require special care to make sure the worms cannot escape and invade previously uninvaded areas. Finally, you probably know that our planet's climate is rapidly changing. Higher temperatures and changing intensity of rain can interact with earthworm invasions. It is therefore important to study what happens when organisms in an ecosystem must simultaneously cope with a combination of higher temperature, changing precipitation patterns, and their new squishy neighbors. Curious young minds like you can help answering these questions and further unravel the secret details of life below the ground, especially in response to species invasions and their impacts on the ecosystems of our ever-changing planet.

## AUTHOR CONTRIBUTIONS

MJ drafted the text and figures and NE contributed to the writing and discussion of the content.

## ACKNOWLEDGMENTS

We were very grateful for the constructive comments of two Science Mentor-Young Reviewer pairs and Associate Editor Nathan M. Good which have substantially improved our manuscript. We acknowledge funding by the European Research Council under the European Union's Horizon 2020 research and innovation program (grant no 677232 to Nico Eisenhauer) and the German Centre for Integrative Biodiversity Research Halle-Jena-Leipzig, funded by the German Research Foundation (FZT 118).

<footnote n="3">³ EcoWorm project introduction video: https://www.youtube.com/watch?v=Au_-VYDUhAw&list=PLJFvA(Py3UkyUbNO48W7bY2KoVuSYIlec&index=10&t=0s</footnote>
## REFERENCES

1. Wardle, D. A., Bardgett, R. D., Callaway, R. M., and Van der Putten, W. H. 2011. Terrestrial ecosystem responses to species gains and losses. *Science* 332:1273-7. doi: 10.1126/science.1197479

2. Eisenhauer, N., and Eisenhauer, E. 2020. The "intestines of the soil": the taxonomic and functional diversity of earthworms-a review for young ecologists. *EcoEvoRxiv*. doi: 10.32942/osf.io/tfm5y

3. Phillips, H. R. P., Guerra, C. A., Bartz, M. L. C., Briones, M. J. I., Brown, G., Crowther, T. W., et al. 2019. Global distribution of earthworm diversity. *Science* 366:480-5. doi: 10.1101/587394

4. Hendrix, P. F., Callaham, M. A. Jr., Drake, J. M., Huang, C. Y., James, S. W., Snyder, B. A., et al. 2008. Pandora's box contained bait: the global problem of introduced earthworms. *Annu. Rev. Ecol. Evol. Syst.* 39:593-613. doi: 10.1146/annurev.ecolsys.39.110707.173426

5. Ferlian, O., Eisenhauer, N., Aguirre-bengoa, M., Camara, M., Ramirez-Rojas, I., Santos, F., et al. 2018. Invasive earthworms erode soil biodiversity: a meta-analysis. *J. Anim. Ecol.* 87:162-72. doi: 10.1111/1365-2656.12746

6. Frelich, L. E., Blossey, B., Cameron, E. K., Dávalos, A., Eisenhauer, N., Fahey, T., et al. 2019. Side-swiped: ecological cascades emanating from earthworm invasions. *Front. Ecol. Environ.* 17:502-10. doi: 10.1002/fee.2099

7. Eisenhauer, N., Ferlian, O., Craven, D., Hines, J., and Jochum, M. 2019. Ecosystem responses to exotic earthworm invasion in northern North American forests. *Res. Ideas Outcomes* 5:e34564. doi: 10.3897/rio.5.e34564

**SUBMITTED**: 12 February 2020; **ACCEPTED**: 13 October 2020;

**PUBLISHED ONLINE**: 09 December 2020.

**EDITED BY**: Nathan M. Good, University of California, Berkeley, United States

**CITATION**: Jochum M and Eisenhauer N (2020) How Introduced Earthworms Alter Ecosystems. Front. Young Minds 8:534345. doi: 10.3389/frym.2020.534345

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2020 Jochum and Eisenhauer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
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## YOUNG REVIEWERS

### LILU, AGE: 10

I love polar bears and I am fighting against Climate Change to save them! I love guinea pigs too.

<figure><img src="image_314.png" /></figure>

### MICHELLE, AGE: 16

I am a Spanish girl who wants to be a pilot. At school, my favorite subjects are Biology and Maths. My hobbies are aviation and playing tennis.

<figure><img src="image_315.png" /></figure>

## AUTHORS

### MALTE JOCHUM

Malte studied biology because, as a teenager, he built a small pond in his parents' garden and realized that this subject would never cease to amaze him. As a community ecologist, he is very interested in how human activities affect plant and animal communities and their functioning. His work has focused on aquatic and terrestrial ecosystems across temperate and tropical areas and mainly involves macroinvertebrates. When not at work, he likes to explore nature with his two daughters, do rock climbing, cycling, or canoeing, and more recently, has discovered an interest in beginner-level triathlon. *malte.jochum@idiv.de

<figure><img src="image_316.png" /></figure>

### NICO EISENHAUER

Nico has been interested in nature since early childhood. He dug for earthworms, caught frogs and fish, and helped lizards survive the winter months. He has always been fascinated by the beauty of nature and driven by the question of why a specific plant or animal species occurs at one place, but not at another place. During his study of biology, he discovered his interest in the distribution of biological diversity, particularly in the soil, and how it affects the functioning of ecosystems. When not at work, Nico likes soccer, badminton, running, and spending time with his family and friends.
<figure><img src="image_317.png" /></figure>

# CAN WE SAVE THE BEAST BY CONSERVING THE BEAUTY?

Felix Gottschall<fnref n="1" />,<fnref n="2" />*, Erin K. Cameron<fnref n="3" />, Inês S. Martins<fnref n="4" />, Julia Siebert<fnref n="1" />,<fnref n="2" /> and Nico Eisenhauer<fnref n="1" />,<fnref n="2" />

## YOUNG REVIEWERS:

<figure><img src="image_318.png" /></figure>

ANHAD

AGE: 11

<figure><img src="image_319.png" /></figure>

ASHIMA

AGE: 12

Because having a wide variety of species on earth is essential for human health and our economy, conservation areas have been established worldwide. These conservation efforts mostly focus on "beauties," such as pandas or tigers. Many other species are not as charismatic and thus merely considered "beasts." Many "beasts" live invisible lives in the soil but are extremely important for mankind. We asked whether current conservation efforts based on saving the "beauties" can help to automatically protect the "beasts." In other words, is there high biological diversity in the soil at locations with high aboveground biodiversity? We mapped aboveground and belowground biodiversity across the world and found that there are many areas where aboveground biodiversity is high and belowground biodiversity is low, or the other way around. Our results suggest that conserving the "beauties" may not be enough to protect the

<footnote n="1">¹Experimental Interaction Ecology, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig, Germany</footnote>

<footnote n="2">²Institute of Biology, Leipzig University, Leipzig, Germany</footnote>

<footnote n="3">³Department of Environmental Science, Saint Mary's University, Halifax, Canada</footnote>

<footnote n="4">⁴Department of Biology, Leverhulme Centre for Anthropocene Biodiversity, University of York, York, United Kingdom</footnote>
## ECOSYSTEM SERVICES

Functions and processes of an ecosystem that in some way benefit humans. For example, production of fruit, timber, and oxygen, or the purification of water.

## BIODIVERSITY

Biodiversity describes the variety and variability of life. Depending on the context it can refer to different measures. Most common is the number and variety of different species in a given location.

## EXTINCTION

The permanent disappearance of a species. Extinction can be caused by a natural incident (dinosaurs) or human actions (dodos).

## INTRINSIC VALUE

A value that is coming from within. Valued for what it is, rather than for what it is worth.

> **"beasts."** We need to consider life belowground when planning new conservation areas.

## WHAT NATURE PROVIDES AND WHY WE NEED IT

When going for a hike in nature or a walk in a park, there are many different animals and plants to discover. Singing birds, buzzing bees, and pretty flowers are beautiful by themselves and something we enjoy. Furthermore, they provide important functions to our ecosystem and services for us as humans (which are called **ecosystem services**). For instance, birds can control pests like aphids, and plants provide us with necessary oxygen while also producing food, with the help of bees that spread pollen. The amount and extent of these functions and ecosystem services strongly depends on the variety of different plant and animal species. This variety is referred to as **biodiversity** [1].

Many plant and animal species worldwide are threatened by human activities. Increasing agriculture, deforestation, and climate change due to excessive use of fossil fuels have pushed many species to **extinction** [2]. This loss of species is not only worrying in terms of the **intrinsic value** of nature, but also because we depend on nature's services. With ongoing loss of species, we will not only lose parts of the beauty of nature, but also many of its functions that are essential for human life on earth [3].

## THE PROTECTION OF NATURE'S BEAUTY AND SERVICES

By actively protecting certain areas of the world [4], we support threatened species, preserving them and their services for us and for future generations. When deciding which areas to protect, we often chose regions with especially charismatic and noticeable "beauties," like pandas, tigers, or golden eagles. These species often need a large, high-quality living area and live in regions that contain a high diversity of other species. By protecting these "beauties," it is assumed that a lot of other, smaller animals and plants are also automatically protected and cared for. People are more willing to invest money in "beauties" because everybody knows and loves them. Who does not like to watch a panda rolling around in the forest?

## THE BEASTS BELOW US AND WHY THEY ARE OFTEN OVERLOOKED

However, everybody who has done some gardening work or explored the soil below their feet knows that nature provides shelter to more species than we can see at first glance. Below our feet and the feet
of the panda lies a hidden community of earthworms, ants, spiders, springtails, centipedes, and beetles. If we look even closer (e.g., with a microscope) there are tiny bacteria and fungi in the soil as well. Like birds, flowers, and bees, all these belowground species fulfill important functions and services. For example, fungi and springtails digest wood and leaves, providing nutrients to the soil and plants. Earthworms loosen the soil and allow air to enter the ground, making it more productive. Centipedes and spiders control pests and thereby prevent pest species from taking over.

Although belowground species fulfill vital roles and provide important services, they are often overlooked. Scientists are just starting to understand how many species there are in the soil and how these species work together in different ways to shape belowground processes. There are several reasons for this lack of knowledge. Soil is not easy to access (or to see through), which makes experiments, monitoring, and observational studies hard to plan and conduct. Furthermore, many important players in belowground systems are tiny and do their work in secret. Some people even consider soil animals as "beasts." Worms, insects, spiders, bacteria, and fungi are rarely considered "beauties," although their alien appearances and ways of life hold their own kind of charm. During the establishment of new protected areas, however, these issues lead to belowground species being left out of consideration.

## CAN WE SAVE THE "BEAST" BY PROTECTING THE "BEAUTY"?

In our research, we asked whether we would automatically protect the important belowground "beasts" like earthworms by choosing protected areas based on aboveground "beauties" like the panda. Can we save the "beast" by protecting the "beauty"?

This question is very important because it helps us to understand whether the current way of choosing protected areas is good enough, or if it has to be adjusted to include ecosystem services that may have been overlooked so far, but are essential for human well-being.

## HOW DID WE APPROACH THIS QUESTION AND WHAT DID WE FIND?

To determine whether protecting aboveground species also automatically protects belowground species, we assembled big sets of data about the presence and diversity of aboveground species (mammals, birds, amphibians, and plants) and belowground species (bacteria, fungi, and soil animals). Most of the data was already collected and published by collaborating scientists and some information was extracted from **public databases** [5]. We then used

### PUBLIC DATABASE

An organized collection of data that can be accessed by scientists or the general public from all over the world.
<caption>**Figure 1**</caption>

Global map showing the distribution and overlap of aboveground (mammals, birds, amphibians, and plants) and belowground (fungi, bacteria, insects, and worms) biodiversity. Colors indicate different combinations of above- and belowground biodiversity. Orange: high aboveground biodiversity and low belowground biodiversity; beige: low aboveground biodiversity and low belowground biodiversity; green: high aboveground biodiversity and high belowground biodiversity; turquoise: low aboveground biodiversity and high belowground biodiversity; and gray: no data available. From this map, you can see that there are big areas of mismatch (orange), where it is not possible to protect the "beasts" by protecting the "beauties."

<figure><img src="image_320.png" /></figure>

special computer techniques (ArcGIS: a software used to create maps and analyze geographic information) to create maps to show patterns in the data around the globe. By analyzing and comparing these maps, we were able to answer our question.

What is the answer? With the help of our maps (Figure 1), we saw that there are many areas where both aboveground biodiversity and belowground biodiversity are high ("match"), such as in many tropical regions of the globe (Figure 1—green areas). However, we also saw that there are many areas where aboveground biodiversity is high and belowground biodiversity is low (Figure 1—orange areas), or the other way around (Figure 1—turquoise areas) ("mismatch"). One example of high belowground biodiversity but low aboveground biodiversity is the northern regions of the earth, like the vast tundra and boreal regions in the northern hemisphere. The overall area of mismatch, where it is not possible to protect the "beasts" (belowground diversity) simply by protecting the "beauties" (aboveground diversity) spans roughly one third of the land surface of the Earth.

## WHAT ABOUT THE FUTURE?

Given our results, we strongly suggest that we need to adapt the way experts decide which regions to declare as protected areas (Figure 2). While it is very important to protect the habitat of "beauties" like the panda or tiger, we have to be careful not to overlook the "beasts" in the soil that are so important for our well-being. If we only focus on the areas containing "beauties," we risk losing many soil species and their services (examples: soil carbon storage, water purification, nutrient cycling), because these soil species may be very diverse in regions of the world where "beauties" are less diverse.

The results of this study only mark the beginning of new approaches to nature conservation. Since soil is not easily accessible, we still
<caption>Figure 2</caption>

How do we decide
which areas to protect?
Left: A scientist checks
aboveground to see if
the area is worth
protecting. The
decision is based on
diversity of
aboveground species
and occurrence of
"beauties". A positive
outcome leads to the
protection of the
area and ecosystem.
Middle: A scientist
checks and finds low
aboveground diversity
and is unaware of
belowground diversity.
The area does not get
protected. Soil
organisms are
overlooked and
threatened by industry
and agriculture.
Important functions
and services of
soil life are lost.
Right: In addition to the
aboveground check,
scientists also consider
soil organisms. The
area will be protected
based on the positive
results for soil diversity.
The ecosystem and the
soil functions and
services are preserved.

<figure><img src="image_321.png" /><figcaption>Figure 2</figcaption></figure>

need much more information on threats to belowground processes
and soil organisms, as well as on the roles, needs, and behaviors
of these organisms. This will help to make recommendations for
areas to protect and a general adjustment of common industrial and
agricultural practices outside of conservation areas. Therefore, an
important next step is to increase the overall knowledge about soil
species worldwide, by conducting surveys and monitoring programs.
Basically, that means that we have to "dig deeper"! To enable scientists
to do this important work, it is essential to raise awareness among
both the general public and governments about the importance of the
curious "beasts" below our feet.

ORIGINAL SOURCE ARTICLE

Cameron, E. K., Martins, I. S., Lavelle, P., Mathieu, J., Tedersoo, L., Bahram, M., et al. 2019. Global mismatches in aboveground and belowground biodiversity. *Conserv. Biol.* 33:1187–92. doi: 10.1111/cobi.13311
## REFERENCES

1. Merritt, M., Maldaner, M. E., and de Almeida, A. M. R. 2019. What are biodiversity hotspots? *Front. Young Minds* 7:29. doi: 10.3389/frym.2019.00029

2. IPBES. 2019. *Summary for Policymakers of the Global Assessment Report on Biodiversity and Ecosystem Services of the Intergovernmental Science-Policy Platform on Biodiversity and Ecosystem Services*. Bonn: IPBES Secretariat.

3. Cardinale, B. J., Duffy, J. E., Gonzalez, A., Hooper, D. U., Perrings, C., Venail, P., et al. 2012. Biodiversity loss and its impact on humanity. *Nature* 486:59–67. doi: 10.1038/nature11148

4. UNEP-WCMC, IUCN. 2020. *Protected Planet: The World Database on Protected Areas (WDPA)*. Available online at: www.protectedplanet.net (accessed April 8, 2020).

5. Cameron, E. K., Martins, I. S., Lavelle, P., Mathieu, J., Tedersoo, L., Bahram, M., et al. 2019. Global mismatches in aboveground and belowground biodiversity. *Conserv. Biol.* 33:1187–92. doi: 10.1111/cobi.13311

**SUBMITTED**: 31 March 2020; **ACCEPTED**: 24 August 2020;

**PUBLISHED ONLINE**: 06 October 2020.

**EDITED BY**: Malte Jochum, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION**: Gottschall F, Cameron EK, Martins IS, Siebert J and Eisenhauer N (2020) Can We Save the Beast by Conserving the Beauty? *Front. Young Minds* 8:547740. doi: 10.3389/frym.2020.547740

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2020 Gottschall, Cameron, Martins, Siebert and Eisenhauer. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWERS

### ANHAD, AGE: 11

Hello my name is Anhad and I like writing about topics (sometimes). I also love watching TV and playing video games on my console and also love hanging out with my friends and family. I like watching netflix in my free time and cooking.

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ASHIMA, AGE: 12

Hi, I am Ashima. I like to read fiction books and swim. I love to study. My favorite subject is mathematics. Quadratic functions are my favorite topic in mathematics.

AUTHORS

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FELIX GOTTSCHALL

Already as a kid, Felix was fascinated by dinosaurs and all kinds of extinct animals. After memorizing all his children's books, he spent a lot of time in museums and imagined how it would be to search for long-lost animals himself. Over time, his interest switched to living animals, like birds (which basically are dinosaurs!), and he began to study biology. As a scientist, he has worked on many different topics, from glowing snails over thirsty treetops to life below ground. Instead of digging for dinosaurs, he is now digging for soil bacteria and still sees the adventure in it. *fgottschall@gmail.com

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ERIN K. CAMERON

Erin enjoyed playing outside as a child but did not consider becoming a biologist. Eventually, she started helping with research examining how human activities affect songbirds and she found it fascinating. Once she started to work on soil organisms and saw how much is still unknown about them, she was convinced that she wanted to study biology. Now she investigates how human activities affect soil biodiversity and the functioning of ecosystems. Erin also enjoys cross-country skiing, bicycling, and kayaking in her free time.

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INÊS S. MARTINS

Inês always loved learning how things are created, where they came from, and how they are changing. Nothing holds more questions like that than nature, so it is not surprising Inês choose to pursue biology in school. While studying, she became particularly interested in looking at how humans have been influencing organisms by changing their habitats. Now, she spends her days trying to model and understand how biodiversity responds to past and possible future environmental changes across vast areas of the world. Outside work, Inês likes to play sports, go to the cinema, and to simply enjoy time with friends and family.

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JULIA SIEBERT

Julia has been fascinated by nature since she was a child. She spent as much time as possible outdoors, built moss houses in the forest, and searched for all kinds of animals. She followed this passion by studying biology and communication science and was always keen on finding ways to transfer knowledge to different audiences. Her scientific studies focused on the effects of global change on soil organisms and their ecosystem functions in agroecosystems. Furthermore, she explored ways to engage school students in biodiversity science. In her free time, she enjoys horse-riding, traveling, birdwatching, mountain biking, and all sorts of outdoor sports.
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NICO EISENHAUER

Nico has been interested in nature since his early childhood. He dug for earthworms, caught frogs and fish, and helped lizards survive the winter months. He has always been fascinated by the beauty of nature and driven by the question of why a specific plant or animal species occurs at one place but not at another place. During his study of biology, he discovered his interest in soil animals and their important activities that are crucial for the functioning of ecosystems. When not at work, Nico likes to play soccer and badminton, to run, and to spend time with his family and friends.
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# PROTECTING SOIL BIODIVERSITY: A DIRTY JOB, BUT SOMEBODY'S GOTTA DO IT!

Alberto Orgiazzi*

European Commission, Joint Research Centre, Ispra, Italy

## YOUNG REVIEWERS

<figure><img src="image_330.png" /></figure>

KAYSVILLE
JUNIOR
HIGH

AGES: 12–13

Soil biodiversity means the range of creatures, of various shapes and sizes, living in the soils—from microorganisms to animals. Soil diversity is extremely important and, to protect it, we need to know where potentially endangered soil organisms live. Unfortunately, we do not have data on the distribution of most soil species. However, we do know the potential threats to soils and soil inhabitants. Therefore, we identify areas where risks are high and try to reduce those risks, which allows us to indirectly protect soil organisms. Following this path, we mapped the risk to soil microorganisms and animals in 27 countries of the (pre-Brexit) European Union. Our results highlight the urgent need to act, as organisms living within more than 40% of soils are at high risk in most countries.

## SOIL BIODIVERSITY MATTERS

An estimated one quarter of the life on our planet lives under our feet, in the soil. The vast range of organisms living in the soil is
## SOIL BIODIVERSITY

All the living creatures that inhabit the soil.

called the **soil biodiversity**. Organisms living in the soil provide many essential services to humankind. They support food production by helping plants to grow, and they play a key role in controlling nutrient cycles (especially carbon and nitrogen), and thus in regulating the Earth's climate. Other less obvious but still crucial services include water purification, which makes water drinkable, and the production of substances that have important medical uses. For example, most of the antibiotics that we currently use come from soil organisms.

Despite its importance, soil biodiversity is generally not considered when people think about how to protect the Earth's biodiversity. Most of the current plans for biodiversity protection only target organisms that live above ground. It is also not that easy to protect soil biodiversity—it is a dirty job, but one that needs to be done!

## SOIL

### MICROORGANISMS

Organisms living in the soil that can be seen only through a microscope. Soil microorganisms include archaea, bacteria, fungi, and protists.

## SOIL FAUNA

Organisms living in the soil that belong to the kingdom Animalia. These range from tiny worms called nematodes (<0.1 mm) to larger animals like moles.

## HOW TO PROTECT SOIL BIODIVERSITY

Imagine you are a superhero with a new, challenging mission: you must save a group of mammals, plants, reptiles, and insects that will disappear in a few days. If the target group lives above ground, you can easily identify where your endangered community lives. This allows you to create a protected area—maybe a kind of a fence surrounding the space where your endangered group lives. Mission accomplished: you are protecting biodiversity.

However, often the job is not that easy. If you need to safeguard organisms living below ground, you might not have much information about who they are or where they live. This is because most of the species living beneath our feet are yet to be discovered [1]. Furthermore, soil biodiversity is extremely complex and ranges from **soil microorganisms**, which are invisible to the naked eye, to **soil fauna**, including animals like earthworms and moles. Therefore, pinpointing exactly where soil organisms live is an extremely difficult, sometimes impossible task. Luckily, there is another, indirect way to protect soil biodiversity. Even if you do not know where a group of organisms lives, you can figure out the areas where soil organisms might be in danger from potential risks. Once you have mapped those high-risk areas, you can work to reduce the threats that potentially affect your target organisms. But it is not quite as easy as it sounds...

## IDENTIFYING RISKS TO SOIL BIODIVERSITY

Of course, every mission faces difficulties. Indirect protection of soil biodiversity needs to overcome three main obstacles. First, we must understand the main threats to soil biodiversity. Many things can affect soil organisms, but we need to identify current threats that can be measured and that are actually *known* to be dangerous to life in the
## Figure 1

Level of risk associated with 13 potential threats to soil microorganisms and fauna. Numbers indicate the position of each threat based on scientists' rankings, from least risky (smallest numbers) to most risky (largest numbers). Transparent bars indicate threats on which experts cannot agree, so they remain controversial and require more research. You can see that, for both microorganisms and soil fauna, the biggest risk to soil biodiversity is intensive human usage.

<figure><img src="image_331.png" /><figcaption>Figure 1</figcaption></figure>

## GENETICALLY
MODIFIED
ORGANISM (GMO)

An organism that has had its DNA modified to give it new abilities, such as pest resistance or the ability to grow in the presence of weed-killing chemicals.

## ARIDITY

A condition characterized by limited-to-no water availability in an environment, mainly due to scarce precipitation.

soil. Over the years, scientists have worked to find out what puts soil life at risk. Therefore, as a superhero, your first step should be to read all the available literature on this topic. Even though we are not superheroes, that is what we did in our study mapping at-risk soils in the European Union [2]. We identified 13 potential threats to soil organisms, from pollution and use of genetically modified organisms (GMOs) to increasing aridity (dryness) and soil loss due to extreme weather events (Figure 1).

Once we have a list of the threats to soil organisms that we want to map, our second obstacle becomes clear: soil biodiversity is immense. Are we sure that, for instance, increasing aridity has the same negative effect on all soil organisms? Increased aridity will likely be a big problem for earthworms (which love wet, moist soils), but may be less of an issue for microorganisms that can better tolerate harsh conditions. Furthermore, not all earthworm or bacterial species are affected in the same way by the same threat. In an ideal situation, we would try to create a risk map for each species of soil organism, but that would lead to millions of maps, which would be impossible even for superheroes to manage. We need a compromise. As a first step, we decided to create maps for two main groups: soil microorganisms (including bacteria and fungi) and soil fauna (including earthworms, insects, springtails, and mites [1]).

Now we have a list of threats to map and of target groups to be considered. A third obstacle emerges. To what extent does each threat affect the different groups of organisms? Aridity can cause earthworms to die, so this has a high level of risk for them. However, some
bacteria can recover quickly from a dry period, so aridity poses a low level of risk to them. To assess these differences, we called on the knowledge of soil scientists who have been working on risks to soil organisms for a long time. We knew that these experts could help us by providing accurate information about the risk levels our threats pose for various species. We contacted over 100 researchers and asked them to rank our 13 threats to soil biodiversity based on the level of risk (low, moderate, high) to the soil microorganisms and fauna they studied. This information helped us to pinpoint the most accurate level of risk associated with each of the proposed threats and groups of organisms.

## RISKS TO SOIL BIODIVERSITY IN THE EUROPE UNION

Now you are part of a team of superheroes; you have all you need to accomplish your mission. You have pooled all the information to identify your most dangerous enemies, combined expert opinions on groups of soil organisms, and ranked the threats to soil microorganisms and fauna (Figure 1). When we did these things, our findings suggested that, for both soil microorganisms and animals, the most dangerous threat is intensive human use of soil, which mainly means agriculture through intense physical (high cattle density, heavy machinery) and chemical (pesticides and fertilizers) inputs [3]. This is not surprising because no soil organism can do well when strange machines come to break up or destroy its home on a regular basis. At the opposite end of the scale, the use of GMOs in agriculture was ranked as being the least risky. GMOs are agricultural plants whose DNA has been modified by humans to make them grow better and produce more food [4]. The use of GMO plants in agriculture is controversial. Our findings suggested that, while the use of GMOs is not completely risk-free, other threats are more dangerous to soil biodiversity.

Scientists often disagree and, in our case, sometimes the level of disagreement was so high that it was impossible to classify the level of risk for some threats (Figure 1). For example, biodiversity experts could not agree on the effect of pollution on soil animals and the effect of climate change on soil microorganisms. These "controversial threats" were expected. An interesting side-product of our analysis has been the identification of those threats about which we still do not know enough to say how risky they are. These threats require further investigation in the future, so there is plenty of work to keep soil scientists busy!

## FINDING THE ENEMIES

The next step of your mission: find out where the enemies are, by combining threat rankings with some geographical data. For instance,
## Figure 2

Maps of risk to soil microorganisms and fauna in 27 countries of the European Union, based on data collected from 2016. In more than half of the countries studied, 40% of the soils posed high levels of risk to soil microorganisms and soil fauna.

<figure><img src="image_332.png" /></figure>

for the threat "use of GMOs in agriculture," we combined a map of the European countries in which GMO cultivation is allowed (Spain, Portugal, Romania, Czechia, and Slovakia) with a map of the agricultural areas in those countries. This allowed us to identify soils where GMOs might be grown. For the threat of "intensive human usage," we made a map showing fertilizer application (the more fertilizers used, the more intense the human usage) and number of cattle (the more cattle, the greater the impact on the soil).

Once all our geographical data were collected, thanks to supercomputers, we brought all the data together to produce maps showing the risk to soil biodiversity in the European Union (Figure 2). As we looked closely at the risk distribution in each of the 27 European countries, we found an alarming situation. In more than half of the countries studied (14 out of 27), 40% of the soils posed high levels of risk to soil microorganisms and animals. Only five countries showed that more than 40% of their soils posed low risks to soil life.

The maps we produced not only allowed us to identify the areas with higher levels of risk in each country, but they also gave us information about the activities affecting soils in those regions. All these data are fundamental to ensure the proper protection of soil biodiversity.

## WHAT NEXT?

We have mapped the risks to soil biodiversity and discovered areas where help is needed to preserve soil organisms. Does this mean we can say, "Mission accomplished! Life belowground is safe!"? Not really. But here is the best part: we must now identify real-life actions that will reduce the risks to soil organisms in the high-risk areas. For instance, maybe protected areas (like national parks) can be set up to avoid, or at least reduce, human interference. However, in many cases this may not be enough. For example, extreme weather events do not have
boundaries; they also occur in national parks. To reduce the impacts
of severe weather on soil organisms, we need wider measures that will
help to slow or reverse climate change. That is another story—a true
superhero mission!

ACKNOWLEDGMENTS

The author want the thank Gráinne Mulhern for carefully proofreading
the manuscrip, and to all the authors of the original publication [2]. The
original source article and research were supported by the European
Commission within the EcoFINDERS project (FP7-264465).

ORIGINAL SOURCE ARTICLE

Orgiazzi, A., Panagos, P., Yigini, Y., Dunbar, M. B., Gardi, C., Montanarella, L., et al. 2016. Knowledge-Based approach to estimating the magnitude and spatial patterns of potential threats to soil biodiversity. Sci. Total Environ. 545-546:11-20. doi: 10.1016/j.scitotenv.2015.12.092

REFERENCES

1. Orgiazzi, A., Bardgett, R. D., Barrios, E., Behan-Pelletier, V., Briones, M. J. I., Chotte, J. C., et al. 2016. *Global Soil Biodiversity Atlas*. European Commission, Publications Office of the European Union, Luxembourg.

2. Orgiazzi, A., Panagos, P., Yigini, Y., Dunbar, M. B., Gardi, C., Montanarella, L., et al. 2016. Knowledge-Based approach to estimating the magnitude and spatial patterns of potential threats to soil biodiversity. *Sci. Total Environ.* 545-546:11-20. doi: 10.1016/j.scitotenv.2015.12.092

3. Tsiafouli, M. A., Thébault, E., Sgardelis, S. P., De Ruiter, P. C., Van Der Putten, W. H., Birkhofer, K., et al. 2015. Intensive agriculture reduces soil biodiversity across Europe. *Glob. Change Biol.* 21:973-85. doi: 10.1111/gcb.12752

4. Carpenter J. 2011. Impact of GM crops in biodiversity. *GM Crops*. 2:7-23. doi: 10.4161/gmcr.2.1.15086

SUBMITTED: 08 March 2021; ACCEPTED: 08 February 2022;

PUBLISHED ONLINE: 16 March 2022.

EDITOR: Helen Phillips, Saint Mary's University, Canada

SCIENCE MENTOR: Christopher A. Emerling

**CITATION:** Orgiazzi A (2022) Protecting Soil Biodiversity: A Dirty Job, but Somebody's Gotta Do It! *Front. Young Minds* 10:677917. doi: 10.3389/frym.2022.677917
**CONFLICT OF INTEREST:** The author declares that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2022 Orgiazzi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWERS

### KAYSVILLE JUNIOR HIGH, AGES: 12–13

The students that reviewed this article were selected from Mr. Lanford's Science 7 classes at Kaysville Jr High. Students that live in the area come from strong communities that also know how to appreciate and enjoy nature in the Western US. A lot of the families make a habit to go hiking, fishing, camping, rock hounding, river rafting, biking, and too many other hobbies to mention.

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## AUTHOR

### ALBERTO ORGIAZZI

When he was a child, Alberto wanted to become a helicopter pilot. However, life is full of surprises, and instead he has gone the way of the ostrich, putting his head in the ground. Switching from the sky to the soil, he is now a soil researcher at the European Commission's Joint Research Center. His current mission focuses on the creation of detailed maps of life in European soils. *alberto.orgiazzi@gmail.com

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# TINY FUNGI IN THE SOIL ARE LIKE MEDICINE FOR NATURE

Lena Neuenkamp<fnref n="1" />* and Nadia I. Maaroufi<fnref n="1" />,<fnref n="2" />

## YOUNG REVIEWERS:

<figure><img src="image_336.png" /><figcaption>JOVENA</figcaption></figure>

AGE: 9

<figure><img src="image_337.png" /><figcaption>KAVIN</figcaption></figure>

AGE: 9

<figure><img src="image_338.png" /><figcaption>TANISHKAA</figcaption></figure>

AGE: 8

<figure><img src="image_339.png" /><figcaption>THUVISHA</figcaption></figure>

AGE: 13

<figure><img src="image_340.png" /><figcaption>VETRIVEL</figcaption></figure>

AGE: 12

<figure><img src="image_341.png" /><figcaption>YUTHIGA</figcaption></figure>

AGE: 8

Like humans, plant and animal species have a specific type of place, called an ecosystem, where they prefer to live. If the ecosystem changes too much, some species will disappear, much the same way people avoid living in the desert because it is too hot and dry. Humans modify many ecosystems, sometimes so severely that almost no plants or animals can live there anymore. To help damaged ecosystems recover, we often start by planting trees or other plants. Biologists found that mycorrhizal fungi, tiny fungi living in the soil and inside plant roots, could speed up ecosystem recovery by making plants grow back faster and stronger. In this article, we describe how the recovery of ecosystems can be enhanced by mycorrhizal fungi, and when mycorrhizal fungi are especially helpful.

<footnote n="1">¹Institute of Plant Sciences, University of Bern, Bern, Switzerland</footnote>

<footnote n="2">²Department of Forest Mycology and Plant Pathology, BioCenter, Swedish University of Agricultural Sciences (SLU), Uppsala, Sweden</footnote>
### ECOSYSTEM

An environment colonized by different organisms that are living together and interacting with each other.

### DEGRADED ECOSYSTEM

An ecosystem that has been damage or destructed, which also negatively affects the organisms living in the ecosystem and hampers the functioning of the ecosystem.

### ECOLOGIST

A scientist that studies how ecosystems function, and how the organisms in an ecosystem interact with each other and the environment.

## DEGRADED ECOSYSTEMS NEED OUR HELP

Natural **ecosystems**, such as forests, grasslands, or bogs—provide many functions and serve as homes for native plants, animals, and tiny microorganisms in the soil. Some ecosystems also filter and store water, keep excess carbon out of the atmosphere, and preserve a healthy soil layer where plants can grow and produce fruits and vegetables for us to eat. Ecosystems provide these functions if they are healthy and intact, but sometimes ecosystems become disturbed and stop functioning well. Such disturbances include fires, floods, or tree fall after storms. Fortunately, healthy ecosystems can usually recover easily from these disturbances. However, if disturbances occur frequently over a long period, or if they are very intense, ecosystems have more difficulty recovering and might change. For example, a forest might become a grassland after a very intense storm pulls all the trees over. As another example, after a long period of drought (when there is not enough water for plants to survive) plants may have a hard time growing back even when water is available again. If, after disturbances, ecosystems change to become less complex and have fewer species living in them, we call them **degraded ecosystems**.

Humans use ecosystems to create space for cities, to produce food in agricultural fields, or to mine for stones, sand, or metals for building or manufacturing. These human activities often disturb ecosystems so severely and for so long that the ecosystems are pushed over the edge from where they can no longer recover without help. **Ecologists**, which are scientists who study how ecosystems function and can be home to many species, can help restore degraded ecosystems, helping them to regain their health and their functions. When ecologists restore ecosystems, they might plant trees to help forest recovery after trees are cut down for timber production, or sow seeds to help grasslands recover after they have been used as agricultural fields. Even with this help, sometimes the new plants do not grow well, or the ecosystem looks different after restoration than it did before the disturbance. Why does restoration sometimes not work as well as other times? Recently, ecologists have begun to understand that successful ecosystem restoration needs to take care of both the plants and animals aboveground and the organisms that live belowground, in the soil.

## WHY ARE THE SMALL CREATURES LIVING IN THE SOIL SO IMPORTANT?

Because plants cannot move, they use their roots to look for nutrients and water in the soil. The soil is an important part of the ecosystem and is the habitat of many small creatures [1]. One teaspoon of soil is inhabited by more organisms than there are people on earth—around 7.5 billion [2] (Figure 1A)! All these small creatures interact with each other and contribute to the functioning of the ecosystem, so the health
## Figure 1

The small creatures inhabiting the soil. (A) Microscope pictures of bacteria, fungi, mites, nematodes, and springtails. Nematodes are small roundworms, mites look a bit like mini spiders, and springtails are tiny insects that sometimes can jump (Photo credits: Mehdi Maaroufi, Nadia I. Maaroufi and Arne Fjellberg). (B) Pictures of different types of mycorrhizal fungi and their host plants. (1) An orchid and the orchid mycorrhizal fungi inside the plant root. (2) Arbuscular mycorrhizal fungi inside a blueweed plant. (3) A heather plant and ericoid mycorrhizal fungi inside the plant root. (4) A pine tree and ectomycorrhizal fungi on the surface of the plant root (Photo credits: Lena Neuenkamp, Petr Kohout, Jane Oja, Javi Puy).

## DECOMPOSERS

Organisms that feed on dead plant and animal material, and by that break this material down into the different nutrients it is made off until it becomes soil again. Plants, in turn, take up the nutrients in the soil as food. Many decomposers are fungi.

## PATHOGENS/ PATHOGENIC FUNGI

Organisms that cause diseases for example a pathogenic fungus that makes plant leaves turn brown and incapable of doing photosynthesis.

<figure><img src="image_342.png" /><figcaption>Figure 1</figcaption></figure>

of these soil organisms is likely to be quite important for ecosystem restoration. The most abundant soil organisms are bacteria and fungi. Some of them, called **decomposers**, feed on dead plants and help to break down the plant material until it becomes soil again [3]. Some soil organisms, called **pathogens**, can attack plant roots and make plants sick. Other soil organisms, called **symbionts**, cooperate with plants by exchanging nutrients with them. **Mycorrhizal fungi** are one group of symbionts that researchers believe may help with ecosystem restoration [4, 5] (Figure 1B).
## SYMBIONTS/ SYMBIOTIC FUNGI

Organisms that live together and help each other. For example, symbiotic fungi, such as mycorrhizal fungi that live in plant roots and help plants with nutrient uptake from the soil in exchange for carbon produced by plants in their leaves.

## MYCORRHIZAL FUNGI (MI-CO-RYE-Z-ALL FUN-GUY)

A group of fungi that live in the soil and the roots of plants. Mycorrhizal fungi help the plants with nutrient uptake and resistance against drought or disease caused by other fungi, and in return fungi get food from the plants.

## SOIL INOCULATION

Adding soil organisms (for example, mycorrhizal fungi or bacteria) to the soil to make plants grow better.

# MYCORRHIZAL FUNGI ARE LIKE POWERFUL MEDICINE FOR PLANTS

Mycorrhizal fungi can help plant roots to collect more nutrients and water from the soil, therefore helping the plants to grow better. So, let us call them helper fungi from now on. In addition, these helper fungi can protect plants against pathogens that can cause plant diseases! In return for the benefits helper fungi provide, plants give helper fungi some of their carbon—a nutrient that plants produce with the help of sunlight during photosynthesis. So, the partnership between plants and fungi is a win-win situation for both partners, called **symbiosis**. Ecologists tested the effects of the helper fungi for assisting ecosystem restoration (Figure 2). The process of adding helper fungi to the soil is called **soil inoculation**. Studies testing the effects of soil inoculation on ecosystem restoration showed that replanted tree seedlings and grasses grew better when helper fungi were added to the soil [4]. In addition, the studies showed that grasslands restored by adding helper fungi were richer in plant species.

## THE POWER OF HELPER FUNGI VARIES

Different types partnerships exist between helper fungi and plants, depending on which species of fungi are most abundant in a specific ecosystem (Figure 1B). Plants and helper fungi differ in when and how much they need each other and how fairly they trade resources and benefits with each other. So, restoration of ecosystems with plants that depend strongly on helper fungi might need mycorrhizal fungi as a medicine more than other ecosystems in which the plants are more independent from helper fungi [5]. When scientists looked through all ecosystem restoration experiments that used helper fungi, they actually did find that the benefits of adding helper fungi varied between studies [4]. So, helper fungi are a good medicine for plants, but when they are most powerful depends on the plants and the ecosystem.

The scientists concluded that helper fungi were the most helpful in the following three conditions:

* for plants that give shelter to bacteria in their roots, making the plants hungry enough for two—theirselfs and the bacteria (like pea or bean plants);

* for plants that have trouble finding nutrients because their roots are too big to reach into the small soil pores where many nutrients are sitting (like some grasses); and

* for plants growing on soils that are both severely disturbed and nutrient-poor.
<caption>Figure 2</caption>

Examples of results of ecosystem restoration projects using mycorrhizal fungi. (A) Heathland restoration in the Netherlands, with the aim of re-establishing a heathland on an old agricultural field with the help of heather plants and ericoid mycorrhizal fungi. (B) Limestone quarry restoration in Estonia, with the aim of speeding up revegetation of an abandoned limestone quarry with the help of grassland seeds, hay, and arbuscular mycorrhizal fungi (Photo credits: Jasper Wubs, Tanel Vahter).

<figure><img src="image_343.png" /></figure>

## WANT TO HELP YOUR OWN HOUSE PLANTS?

About 80% of all plants—even your potted plants at home—have a symbiosis with one type of helper fungi, called arbuscular mycorrhizal fungi. You can keep your plants healthy by making your own arbuscular mycorrhizal fungal inoculum (Figure 3). Many gardeners already do this! You will need a shovel, a 10-liter bucket to mix the soil, 3–5 l of sand, seeds of grass and clover plants, and 4–6 flowerpots.

### The steps:

* **Plant selection:** Select one or two plants from your garden that form arbuscular mycorrhizal symbioses (maybe a grass and a clover plant) and dig them out together with a good portion of soil around the roots.
<caption>Figure 3</caption>

Do-it-yourself mycorrhizal inoculum. The most important steps for producing your own mycorrhizal inoculum (Based on the instructions given here: https://orgprints.org/35308/1/symanczik-etal-2018-Mycorrhizal-fungi-as-natural-biofertilizer_technical note.pdf).

<figure><img src="image_344.png" /><figcaption>Figure 3</figcaption></figure>

BAIT PLANTS

Plants used as a lure to attract mycorrhizal fungi in their roots, where mycorrhizal fungi reproduce and grow. The multiplied fungal material in the roots and the surrounding soil can then be used to produce a fungal inoculum.

* **Source inoculum:** Remove the leaves and stems of both plants, cut their roots into small pieces, and mix all roots and soil well. This is your source inoculum, which we will multiply so that we do not have to dig out too many garden plants to create the inoculum.

* **Inoculum multiplication:** Mix the source inoculum with sand (1 part of inoculum with 1 part of sand, or even 1 of part inoculum with 2 parts of sand) and put it into the flowerpots. Add the grass and clover seeds to the pots, water them, and let them grow for 2-4 months. The seeded species are called **bait plants** because they attract the arbuscular mycorrhizal fungi. When the bait plants start growing, the arbuscular mycorrhizal fungi will colonize their roots and the fungal population will grow. The longer the plants grow, the more fungi will be in the soil.

* **Inoculum harvest:** After 2-4 months, remove all leaves from the bait plants, cut their roots into small pieces, and mix them with the soil. The inoculum is now ready to be added in small amounts to your potted plants—either dry or mixed with water.

TAKE HOME MESSAGE

Human activities can degrade ecosystems so severely that they need help to recover. Mycorrhizal fungi are helper fungi for plants that could support ecosystem recovery, because they can increase
plants' nutrient uptake and protect plants against diseases or drought. Different types of helper fungi exist with different properties, thus when and which helper fungi are most powerful for ecosystem recovery depends on the plants and the ecosystem.

## AUTHOR CONTRIBUTIONS

LN and NM conceived the original idea and wrote the first draft of the manuscript. All authors gave final approval for submission.

## REFERENCES

1. Maaroufi, N. I., and De Long, J. R. 2020. Global change impacts on forest soils: linkage between soil biota and carbon-nitrogen-phosphorus stoichiometry. *Front. For. Glob. Change* 3:16. doi: 10.3389/ffgc.2020.00016

2. Available online at: http://www.soil-net.com/ (accessed November 06, 2020).

3. Maaroufi, N. I., Nordin, A., Palmqvist, K., Hasselquist, N. J., Forsmark, B., Rosentstock, N. P., et al. 2019. Anthropogenic nitrogen enrichment enhances soil carbon accumulation by impacting saprotrophs rather than ectomycorrhizal fungal activity. *Glob. Change Biol.* 25:2900–14. doi: 10.1111/gcb.14722

4. Neuenkamp, L., Prober, S. M., Price, J. N., Zobel, M., and Standish, R. J. 2019. Benefits of mycorrhizal inoculation to ecological restoration depend on plant functional type, restoration context and time. *Fungal Ecol.* 40:140–9. doi: 10.1016/j.funeco.2018.05.004

5. Neuenkamp, L., Moora, M., Öpik, M., Davison, J., Gerz, M., Männistö, M., et al. 2018. The role of mycorrhizal type and status in modulating the relationship between plant and arbuscular mycorrhizal fungal communities. *New Phytol.* 220:1236–47. doi: 10.1111/nph.14995

**SUBMITTED**: 30 April 2020; **ACCEPTED**: 30 October 2020;

**PUBLISHED ONLINE**: 30 November 2020.

**EDITED BY**: Helen Phillips, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION**: Neuenkamp L and Maaroufi NI (2020) Tiny Fungi in the Soil Are Like Medicine for Nature. *Front. Young Minds* 8:557383. doi: 10.3389/frym.2020.557383

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

**COPYRIGHT** © 2020 Neuenkamp and Maaroufi. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice.
No use, distribution or reproduction is permitted which does not comply with these
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AUTHORS

LENA NEUENKAMP

I am a plant ecologist, and I started to investigate the soil because it could help me to understand plants. Well, I then became fascinated by mycorrhizal fungi and how they interact with plant roots. I am working as a researcher at the University of Bern in Switzerland. I am interested in understanding how human disturbances and climate change influence plant and soil communities, as well as the interactions between plants and soil organisms. I would like to use that knowledge to predict how

<figure><img src="image_351.png" /></figure>
well ecosystems can function and provide services to humans, in the face of current human disturbances and climate change. *lena.neuenkamp@ips.unibe.ch

NADIA I. MAAROUFI

I am a soil ecologist interested in the small creatures inhabiting the soil. I am working both at the University of Bern in Switzerland and at the Swedish University of Agricultural Sciences, Uppsala in Sweden. I am particularly interested in understanding how soil organisms are impacted by human and natural disturbances, and how these disturbances affect forest and grassland ecosystem functioning.

<figure><img src="image_352.png" /></figure>
<figure><img src="image_353.png" /></figure>

# LEARNING MORE ABOUT EARTHWORMS WITH CITIZEN SCIENCE

Victoria J. Burton<fnref n="1" />* and Erin K. Cameron<fnref n="2" />

## YOUNG REVIEWER:

<figure><img src="image_354.png" /></figure>

AYA

AGE: 9

Have you ever wanted to conduct scientific research? Citizen, or community science involves non-scientists in assisting scientists with research. The term covers a huge variety of projects: from online-only where you can classify galaxies, to practical outdoor activities, and even helping with scientific expeditions. Ideally, citizen science benefits everyone—scientists collect more data, and over larger geographic areas than they could on their own. Non-scientists benefit by learning something new and experiencing how science works, and hopefully having fun! The small size of most soil organisms is challenging for citizen science. However, earthworms are easy to recognize and relatively large, so there have been several citizen science projects focused on them. In this article, we discuss earthworm citizen science from its origins with 18th and 19th century natural historians, to the modern day. Discover what non-scientists have contributed to earthworm science and how you can design your own earthworm investigations.

<footnote n="1">¹Life Sciences Department, Natural History Museum, London, United Kingdom</footnote>

<footnote n="2">²Department of Environmental Science, Saint Mary's University, Halifax, NS, Canada</footnote>
## CITIZEN SCIENCE

Scientific studies carried out in whole or part by volunteers rather than paid scientists, also known as community science.

¹ setiathome.berkeley.edu/

² foldingathome.org/

³ www.zooniverse.org/

⁴ www.birdcount.org

⁵ freshwaterwatch.thewaterhub.org/

## WHY CITIZEN SCIENCE?

Science is not only carried out by scientists. When other people, like students or families, collect scientific data and help with research, it is called **citizen science**. Citizen science, also known as community science, allows anyone to participate in research, and its popularity has been increasing. Scientists benefit because this helps them to gather data that would have been difficult, expensive, or impossible for them to collect on their own. On the other hand, citizen scientists gain the opportunity to be directly involved in research and learn about science.

## TYPES OF CITIZEN SCIENCE

There are many kinds of citizen science. Some projects borrow the power of personal computers to search for alien life¹ or to find cures for diseases². Some online citizen science projects ask people for help with identifying wildlife or galaxies, translating documents, and many more tasks³. Other citizen science projects need people to go outside to survey wildlife⁴ or to measure water pollution⁵. There are even expedition-style projects, in which volunteers help scientists with research on volcanoes and rainforests.

## WHY STUDY EARTHWORMS?

Healthy soils are important for all life on Earth, as they recycle nutrients, filter water, and help plants to grow. As earthworms feed and burrow, they mix the soil and provide the nutrients that most plants need. Depending on the location of a study, the scientific questions addressed by earthworm research differ. In some places, like the United Kingdom, earthworms are considered beneficial and scientists want to find out more about where they are, to improve soil health. But in other areas of the world, like most of Canada and the northern United States, the last ice age wiped out the earthworms. Now the only earthworms living there are those that were brought into the region by people, often accidentally, with soil or plants that were imported from Europe. Scientific research in these areas often tries to determine where earthworms are found and how they are spreading, to try to reduce their impacts in forests. Even where earthworms are invasive, they are still usually considered beneficial in gardens and for composting and are only a problem when they escape into wild areas.

## CITIZEN SCIENCE FOR EARTHWORMS

Earthworms were some of the first soil animals to be studied by early scientists and they continue to be studied by scientists today, with
**Figure 1**

There are three main types of earthworms, called ecotypes: endogeic, anecic, and epigeic. Some of their characteristics are described here (Credits: earthworm clipart from Vecteezy.com Earthworm photographs © Trustees of the Natural History Museum/Harry Taylor).

<figure><img src="image_355.png" /><figcaption>Figure 1</figcaption></figure>

**ECOTYPE**

Groups of earthworms based on their burrowing and feeding habits.

**ENDOGEIC**

An earthworm that creates horizontal burrows in soil, feeding on soil as it burrows. Usually pale in color.

**ANECIC**

A type of earthworm that builds deep vertical burrows and comes to the surface to feed on leaf litter. Often large and red in color.

**EPIGEIC**

Earthworms that feed and burrow on or near the soil surface, feeding on leaf litter. Usually small and red in color.

the help of farmers, gardeners, students, and many others. Most soil organisms are small and require special equipment and knowledge to study them, which makes it difficult to include them in citizen science. Earthworms are a happy exception, as they are relatively large and easy to find and observe without special equipment. The usual method for finding earthworms is to dig out a cube of soil from the ground and then search through it by hand, picking out any earthworms. Another method uses a mixture of hot mustard powder and water poured on the soil. If the mustard water touches any earthworms in the soil, they move to the surface where they can be captured, but the mustard does not do permanent harm.

Although the species of most earthworms cannot be identified without a microscope, they can be grouped into different categories according to their lifestyle. These categories are called **ecotypes**. The three ecotypes—**endogeic**, **anecic**, and **epigeic** (Figure 1)—can usually be distinguished by citizen scientists.

**EARLY EARTHWORM CITIZEN SCIENCE**

The earliest natural scientists, such as John Ray (1627–1705) and Carolus Linneaus (1707–1778), grouped all long, wiggly animals together as “worms” and many still have common names that reflect this. Some moth caterpillars are called inchworms, legless lizards are called slow worms, and glowing beetle larvae are known as glow worms. John Ray was the first to record the phrase “the early bird catches the worm” in his book “A Handbook of Proverbs,” published in 1670. Linneaus developed rules for naming organisms and named
the common earthworm *Lumbricus terrestris*—the same name it has today.

The English pastor Gilbert White (1720–1793) was the first to observe and write about how earthworms live. He described that earthworms seem to promote plant growth and are an important part of the food chain. Inspired by White's writing, Charles Darwin (1809–1882) was also fascinated by earthworms. Darwin's book *The Formation of Vegetable Mould Through the Action of Worms, with Observations on their Habits* [1] is the result of his 40-years study of earthworms and it was the final book he published, in October 1881. It was very popular, selling 6,000 copies in the first year.

## WHAT DID DARWIN DISCOVER ABOUT EARTHWORMS?

Darwin found that earthworms have no sense of hearing. He discovered this by shouting at earthworms and playing them various musical instruments including a piano, a bassoon, and a tin whistle. However, earthworms in pots placed on a piano hid in their burrows when notes were played, showing that they can sense vibrations through the soil. Darwin also investigated earthworms' sense of smell by blowing tobacco smoke and perfume at them, and they did not react. They can smell their favorite foods though—Darwin experimented with giving captive earthworms many different foods and noted which they preferred. He found that wild cherry leaves were preferred over lime and hazel leaves. Cabbages, horseradish, carrot, and celery were also liked, but herbs, such as sage, thyme, and mint were barely touched.

Darwin observed the way that large stones and ancient buildings are slowly buried, including making a journey to Stonehenge to examine buried stones there. Darwin placed a large stone on the soil surface of his garden and, over 29 years, recorded how long it took the stone to be buried by earthworms. Using this experiment, Darwin estimated that earthworms move 34,000 kg of soil (the weight of five and a half African elephants) per hectare (about one and quarter soccer pitches) to the surface each year—this process is called **bioturbation**.

## BIOTURBATION

The movement of soil by living animals or plants.

## EARTHWORM CITIZEN SCIENCE TODAY

Despite the long history of research involving earthworms, we still do not know enough about where they are most common and how they are affecting other species. Citizen science is helping scientists answer these questions. There are increasing numbers of programs in different parts of the world that involve earthworm sampling (Figure 2 and Table 1). The data citizen scientists collect is mailed to scientists or sent in through smartphone apps. Some of the programs are designed for use in schools and include suggestions for how they fit with
<caption>Figure 2</caption>

Examples of earthworm
citizen science projects
in various countries.
OPVT, L'Observatoire
Participatif des Vers de
Terre.

<figure><img src="image_356.png" /></figure>

course material, while other programs are designed so that anyone
can participate.

DISCOVERIES FROM EARTHWORM CITIZEN SCIENCE

A lot of the research from citizen science projects is still underway, but there have already been some exciting discoveries. And Citizen Scientists have been extremely important! For example, in the United States, citizen scientists have helped to detect the spread of new species, such as jumping worms (*Amynthas* species), which were introduced from Asia. In Finland, citizen scientist helped showing that the number of earthworm species decreases moving from the south to the north of the country. In the north, most of the places surveyed had no earthworms or only one species, likely because of the cold temperatures. In the United Kingdom, the OPAL Soil and Earthworm Survey discovered that citizen scientists find it quite difficult to identify earthworm species but can tell ecotypes apart correctly 70-90% of the time.

The project "What is Under Your Feet?" confirmed that earthworm numbers change with the seasons, with the most found in spring and autumn [3]. There were also more earthworms found after rain. The project #60minworms counted earthworms from farm fields and found that plowing the soil reduced the number of earthworms [4]. Some farms had no epigeic or anecic earthworms, which may mean the fields are plowed too often. The "Earthworm Watch" project found that gardens that use organic fertilizer, such as manure and compost, have 20% more earthworms than gardens that added no fertilizers.
<caption>Table 1</caption>

Past and present
earthworm citizen
science projects
around the world.

<table><caption>Table 1</caption><thead><tr><th>Country</th><th>Project name</th><th>Aimed at</th><th>More information</th><th>Year</th></tr></thead><tbody><tr><td rowspan="2">United States</td><td>Great Lakes Wormwatch</td><td>Anyone</td><td>https://www.k-state.edu/cecd/partnerships/EarthwormsAcrossKansas.htm</td><td>2006–today</td></tr><tr><td>Earthworms across Kansas</td><td>School students</td><td>https://www.k-state.edu/earthworm/</td><td>2010–2012</td></tr><tr><td rowspan="2">Canada</td><td>Alberta Worm Invasion<br/>Worm Tracker</td><td>Anyone</td><td>https://worms.educ.ualberta.ca/</td><td>2013–today</td></tr><tr><td>WormWatch</td><td>Anyone</td><td>https://www.naturewatch.ca/wormwatch/</td><td>2014–today</td></tr><tr><td rowspan="5">United Kingdom</td><td>Open Air Laboratory (OPAL)<br/>Soil and Earthworm Survey</td><td>Anyone</td><td>https://www.imperial.ac.uk/opal-soil</td><td>2009–2020</td></tr><tr><td>What is Under Your Feet?</td><td>School students</td><td>https://jointhepod.org/teachers/other/information-pack-whats-under-your-feet</td><td>2018–today</td></tr><tr><td>#60minworms</td><td>Farmers</td><td>https://www.rothamsted.ac.uk/news/earthworm-research-spurs-farmers-act</td><td>2018</td></tr><tr><td>Earthworm Watch</td><td>Anyone</td><td>https://earthwormwatch.org/</td><td>2016–2018</td></tr><tr><td>Earthworm Society of<br/>Britain</td><td>Anyone</td><td>https://www.earthwormsoc.org.uk/</td><td>2009–today</td></tr><tr><td>France</td><td>L'Observatoire Participatif<br/>des Vers de Terre (OPVT)</td><td>Anyone</td><td>https://ecobiosoil.univ-rennes1.fr/OPVT_ACCUEIL.php</td><td>2011–today</td></tr><tr><td>Australia</td><td>Earthworms Downunder</td><td>School students</td><td>[2]</td><td>1992</td></tr><tr><td>Finland</td><td>Matoseuranta</td><td>School students</td><td>http://matoseuranta.it.helsinki.fi/fi</td><td>2016–2018</td></tr><tr><td>Norway</td><td>Forskningskampanjen<br/>2010–Meitemark</td><td>School students</td><td>https://www.miljolare.no/aktiviteter/land/natur/ln6/</td><td>2010</td></tr></tbody></table>
## HABITATS

The home environment of animals, plants or other organisms, providing food, shelter, protection and mates.

# DOING YOUR OWN EARTHWORM RESEARCH

Whether earthworms are helpful for harmful for soil health depends where in the world you are, but they are always important. Using citizen science, scientists, students, families, farmers, and anyone else interested, can work together to find out more about earthworms. There are still many unanswered questions about earthworms that you can investigate. Here are a few suggestions if you want to start your own project on earthworms:

* Recreate one of Darwin's experiments—how long do earthworms take to bury a stone in your garden? Does this vary depending on where the stone is in your garden?

* How does season affect the number of earthworms found in your garden, or the number of different types of earthworms?

* How does the number and types of earthworms vary across different **habitats** (like your garden compared with a forest)?

* Start a compost bin in your yard—how long does it take for earthworms to arrive?

## REFERENCES

1. Darwin, C. 1882. *The Formation of Vegetable Mould Through the Action of Worms With Observations on Their Habits*. London: John Murray. Available online at: http://darwin-online.org.uk/EditorialIntroductions/Freeman_VegetableMouldandWorms.html

2. Baker, G. H., Thumlert, T. A., Meisel, L. S., Carter, P. J., and Kilpin, G. P. 1997. "Earthworms downunder": a survey of the earthworm fauna of urban and agricultural soils in Australia. *Soil Biol. Biochem.* 29:589-97. doi: 10.1016/S0038-0717(96)00184-8

3. Martay, B., and Pearce-Higgins, J. W. 2018. Using data from schools to model variation in soil invertebrates across the UK: the importance of weather, climate, season and habitat. *Pedobiologia* 67:1-9. doi: 10.1016/j.pedobi.2018.01.002

4. Stroud, J. L. 2019. Soil health pilot study in England: outcomes from an on-farm earthworm survey. *PLoS ONE* 14:e0203909. doi: 10.1371/journal.pone.0203909

**SUBMITTED**: 02 April 2020; **ACCEPTED**: 07 December 2020;

**PUBLISHED ONLINE**: 14 January 2021.

**EDITED BY**: Rémy Beugnon, German Centre for Integrative Biodiversity Research (iDiv), Germany

**CITATION**: Burton VJ and Cameron EK (2021) Learning More About Earthworms With Citizen Science. Front. Young Minds 8:548525. doi: 10.3389/frym.2020.548525

**CONFLICT OF INTEREST**: The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
**COPYRIGHT** © 2021 Burton and Cameron. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

## YOUNG REVIEWER

### AYA, AGE: 9

Aya wants to study marine biology. She wants to specialize in sharks and rays. Her favorite subjects in school are reading, writing, math, and music. In her free time she likes to read books, try out challenging puzzles, training for track and cross country, experimenting with different art techniques, and roller skating.

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## AUTHORS

### VICTORIA J. BURTON

I spent my childhood playing outside, making nature journals, and learning how to identify plants, birds, and insects in the woods. I did not like school but always wanted to be a scientist, so I studied for a degree with The Open University. I have just finished my Ph.D. with Imperial College London, where I researched how soil and leaf-litter invertebrate communities respond to human activities. In my free time I enjoy looking after my pets and plants and helping run the Bug Club for young people interested in insects. *v.burton@nhm.ac.uk

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### ERIN K. CAMERON

I enjoyed playing outside as a child and loved science but did not consider becoming a biologist until I was in university. Eventually, I started helping with research examining how human activities affect songbirds and found it fascinating. Once I started to work on soil organisms and saw how much is still unknown about them, I was convinced that I wanted to study ecology. Now I investigate how human activities affect soil biodiversity and the functioning of ecosystems. I enjoy cross-country skiing, bicycling, and kayaking in my free time.

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