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 plantmaterial, 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,wewanted to knowwhatwould happen if drought and
over-fertilization occurred togethe

Eisenhauer, Nico

Siebert, Julia

Sünnemann, Marie

English

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BIODIVERSITYPublished: 08 October 2020doi: 10.3389/frym.2020.547630DOUBLEWHAMMY FOR LIFE IN SOIL? THE EFFECTSOF DROUGHT AND FERTILIZER USEMarie Sünnemann 1,2*, Julia Siebert 1,2 and Nico Eisenhauer 1,21Experimental Interaction Ecology, German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, Leipzig,Germany2Institute of Biology, Leipzig University, Leipzig, GermanyYOUNG REVIEWER:JEDIDIAHAGE: 14For the last two centuries, humans have been changing the Earththrough their way of life. Our actions are not only causing climatechange and leading to prolonged periods of drought, they arealso leading to an overaccumulation of nutrients in soil, due toburning of fossil fuels and fertilization of agricultural fields. Bothfactors are threatening the world beneath our feet: the soils. Theymay look rather boring and lifeless, but soils are actually hometo many organisms—from tiny bacteria to agile millipedes andslimy earthworms—all of which contribute to processes that areindispensable to life on Earth. For example, the activity of theseorganisms promotes decomposition of plant material, which ensuresthat the farmlands on which we grow our food remain fertile. Asalmost all soil organisms are very sensitive to changes in theirenvironments,wewanted to knowwhatwould happen if drought andover-fertilization occurred together.kids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 1Sünnemann et al. The E ects of Drought and FertilizationHUMAN ACTIVITIES CHANGE ECOSYSTEMSOver the last 200 years, human activities have changed the worldtremendously. Human-induced climate change is causing the planetto warm up, coupled with ever-longer periods of drought (prolongedperiods with little rainfall) in some regions. At the same time, thefarming of fields and meadows has changed dramatically in recentdecades. The world’s population is growing steadily, and all thesemany people need to eat. Therefore, large amounts of fertilizers areapplied on agricultural fields today, resulting in much higher cropyields [1]. While they may provide enough food for several billionpeople, these practices come with a significant drawback: similarto drought, excess fertilization a ects not only the plants visibleaboveground, but also the complex ecosystem belowground—theECOSYSTEMA community of plants,bacteria, animals, andfungi in a certainlocation, along with thenon-living componentsof that environment.soil and the organisms living in it.THE IMPORTANCE OF THE SOIL ECOSYSTEMSoils are an important part of terrestrial ecosystems. Although we areoften unaware of them, soils are teeming with living things. There aremicroorganisms, such as bacteria and fungi that are so tiny that theyare not visible to the naked eye. What they lack in size, however, theycompensate for in number: just one teaspoonful of soil can containseveral million soil microorganisms. Even many of the somewhatlarger creatures, such as mites and springtails, can only be seen witha magnifying glass. Among the biggest soil animals are woodlice,centipedes, and earthworms. All the somewhat larger soil creaturesare united by the fact that they do not have backbones, which is whythey are referred to as invertebrates. These creatures live together inINVERTEBRATESAnimals lacking spines,such as centipedes,woodlice,and earthworms.the soil and interact in various ways: some feed on each other, whileothers work together.The soil invertebrates perform numerous tasks that are necessaryfor our existence. One of the most important of these ecosystemfunctions is decomposition, which requires the cooperation ofECOSYSTEMFUNCTIONSNatural processes thatoccur in an ecosystem.DECOMPOSITIONAfter death, livingorganisms are brokendown into smaller andsmaller pieces. Thisreleases nutrients,which in turn areneeded forplant growths.a multitude of creatures. Soil organisms are responsible for thebreakdown of dead plant material. Withered leaves, dead roots,and seeds are their food resources. They break down these deadplant materials into smaller and smaller pieces. The resulting tinycompounds, in turn, provide an excellent food source for soilmicroorganisms like bacteria and fungi. Eventually, these resources areconverted back into a form that plants can use for their growth, namelyCO2 and nutrients.All these soil creatures, like almost all life on earth, are highlydependent on water for drinking, for breathing, or even as a means oftransportation. Increasingly long and frequent periods of drought aretherefore a problem for many small organisms. And even worse, whathappens if other harmful factors occur at the same time? Excessivekids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 2Sünnemann et al. The E ects of Drought and FertilizationFigure 1Figure 1In half of theexperimental plots inour study, we usedroofs to simulatedrought. The other halfof the plots received“fake” roofs with rainpanels putupside-down toaccount for thepotential side e ects ofthese roof structures(like changes in windspeed and light). ©JuliaSiebert.use of fertilizer, for example, can be harmful to soil organisms, as itchanges the pH value of the soil to make it more acidic. Many soilPH VALUEA scale indicatingwhether a solution hasan acidic or basiccharacter. The lowerthe value, the moreacidic the solution is.organisms cannot tolerate acidic soil conditions. Could fertilizationadd a further stress factor, making it even harder for soil organismsto withstand dry conditions? And how exactly can we learn whetherdrought and fertilization are harmful to soil organisms and interferewith their functions?HOWDIDWE STUDY SOIL MICROORGANISMS?To understand the e ects of drought and fertilization on soilorganisms, we started an experiment that simulated these twocommon factors that humans change [2]. We chose a meadow inCentral Germany where we selected small areas called experimentalplots and treated the plots in di erent ways. One-fourth of theexperimental plots were treated with drought using roofs (Figure 1),another fourth was treated with fertilizer, and yet another fourth wastreated with a combination of drought and fertilizer. The last fourthwas not treated at all, which was our control plot. Control plotsare important because they allow us to compare the treatments tonormal conditions.To understand how drought and fertilization a ect soil organisms, welooked at soil invertebrates and soil microorganisms separately. Weexamined the activity of soil invertebrates in each of our plots. To dothis, 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. Westuck some bait lamina test strips completely into the ground of ourplots (Figure 2). After 3 weeks, we observed the amount of the bait thathad been eaten by the soil animals. Soil ecologists use this method toassess how much soil invertebrates eat, which is a very good indicatorof their activity in general.kids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 3Sünnemann et al. The E ects of Drought and FertilizationFigure 2Figure 2To determine theactivity of soilinvertebrates in ourexperimental plots, weused bait lamina strips.The strips werecompletely insertedinto the ground for soilinvertebrates to feedon. After 3 weeks, wechecked how many ofthe little holescontaining the baitwere full, empty, orhalf-empty. The moreactive and hungrier thesoil invertebrates, themore of the bait waseaten.©Gottschall/Siebert.To examine the soil microorganisms more closely, we took a smallamount of soil from each of our plots back to the lab. We determinedthe microbial activity in these samples by measuring their respiration.Just like humans, soil organisms breathe in oxygen (O2) and exhalecarbon dioxide (CO2), so the more respiration that is happening ina sample, the more active are the microorganisms (think of yourselfexercising). To measure microbial respiration, we used a device witha special sensor that can measure the amount of oxygen used by themicroorganisms, and these data were then transferred to a computerfor storage. By knowing the activity of the soil microorganisms, wewere then able to calculate their biomass, which is a measure forBIOMASSMeasure for theamount of all microbesthat live in a definedamount of soil.the amount of all microbes that live in a defined amount of soil, forexample on a teaspoon.DROUGHT AND FERTILIZATION CAN AFFECT SOILINVERTEBRATESWe used statistical tests on our data to find out how the microbial andinvertebrate soil communities reacted to drought and fertilization. Wefound that both drought and fertilization severely disrupt the activityof soil invertebrates. Although the factors on their own had strongkids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 4Sünnemann et al. The E ects of Drought and FertilizationFigure 3Figure 3What did we find? (A)Drought, fertilization,and both togetherstrongly reduced thefeeding activity of soilinvertebrates. (B) Soilmicroorganisms werenot disturbed by thedrought treatment.Fertilization caused anincrease in the soilmicrobial biomass.negative e ects, their combination did not reduce invertebrate activityany further (Figure 3A). Soil microbes, however, reacted completelydi erently. Drought could not harm them, and additional fertilizationeven increased their biomass (Figure 3B).Why do drought and fertilization harm invertebrates much more thanmicroorganisms? Usually, both groups are highly dependent on soilmoisture and have trouble coping with droughts. Among other things,their food becomes so dry that they have diculty digesting it [3].Imagine eating old toast without jam all day, without drinking anythingwith it. To avoid drought conditions, invertebratesmay 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 thatfertilization leads to an acidification of soils, which means that the pHvalue falls below five. Earthworms and many other soil invertebratesdo not like to live in low-pH conditions, which can be damaging totheir delicate skin. A lemon, for example, has a pH value of 2. Haveyou 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 tookus by surprise, because our treatment reduced the annual rainfall byhalf, which naturally led to extremely dry soils. However, we think it ispossible that bacteria and fungi that normally live in the upper layer ofkids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 5Sünnemann et al. The E ects of Drought and Fertilizationthe soil are constantly exposed to the temperature and humidity cyclesof the seasons. For this reason, they must be able to survive even thedriest periods [4]. One way that they do this is by building themselvesa sugary protective shell that prevents their surfaces from drying out.Alternatively, they can create a very resistant form that allows themto survive, called a spore. Spores are in a dormant state and canoutlive extreme heat and drought for up to 1,000 years. This is whywe believe the drought conditions of our experiment hardly harmedthe soil microorganisms. But it is also possible that our experiment wastoo short to see any negative e ects of the drought.Fertilization, on the other hand, was even beneficial for themicroorganisms. This is because the additional nutrients from thefertilizer strongly promoted plant growth. Not only did the plantsrespond with longer shoots, larger flowers, and many more leaves,they also released more resources into the soil via their roots and themicroorganisms could feed on all these extra food sources.We were happy to find that drought and fertilizer did not reinforceeach other’s e ects, which means that both factors together do notseem to do more harm than either does on its own. This may meanthat ecosystems have some great coping mechanisms to use againstharmful environmental attacks. But in this study, we only measuredthe activity of soil organisms after 1 year. We should examine the soilafter many years of drought and fertilization, to see if the results arestill the same.WHATWILL THE FUTURE HOLD FOR OUR SOILS?To sum up, larger soil invertebrates seem to be much lesswell-equipped for future environmental changes thanmicroorganismsare. What does this mean for our soils in the future? The decline inthe activity of soil animals has several consequences for ecosystemsand therefore for humans. As we have already learned, all organismsin the soil are necessary to keep the process of decompositionrunning. The decomposition process is divided into several steps,which are indispensable for one another. While invertebrates aremostly responsible for breaking down larger pieces of dead animalsand plants, microorganisms digest the smaller pieces in the next stepand release a range of nutrients. Together, the soil organisms form alarge feeding community, in which each species has its own specialplace, fulfilling their specific tasks. However, if one link in this chain ismissing, the whole system is likely to lose its balance [5]. This couldmean that soils could lose their fertility in the long term. The resultwould be that not only grasses but also the wheat and maize in ourfields would no longer grow so luxuriantly, and we would eventuallyhave problems feeding all the people on Earth. We are thereforedependent on the well-being of all soil creatures and should keepkids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 6Sünnemann et al. The E ects of Drought and Fertilizationtheir importance inmind as wemake future decisions that could a ectour soils.ACKNOWLEDGMENTSWe thank the sta  of the Bad Lauchstädt Experimental ResearchStation for their help in maintaining the experimental site, and AllaKavtea, Tom Künne, and Ulrich Pruschitzki for their support withlab and field work. Furthermore, we thank the coordination of theInternational Drought-Net Experiment for providing protocols andsupport. We acknowledge editorial help by Susan Debad.ORIGINAL SOURCE ARTICLESiebert, J., Sünnemann, M., Auge, H., Berger, S., Cesarz, S., Ciobanu,M., et al. 2019. The e ects of drought and nutrient addition on soilorganisms vary across taxonomic groups, but are constant acrossseasons. Sci. Rep. 9:639. doi: 10.1038/s41598-018-36777-3REFERENCES1. 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.11366742. Siebert, J., Sünnemann, M., Auge, H., Berger, S., Cesarz, S., Ciobanu, M., et al.2019. The e ects of drought and nutrient addition on soil organisms vary acrosstaxonomic groups, but are constant across seasons. Sci. Rep. 9:639.doi: 10.1038/s41598-018-36777-33. 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 drierconditions. Nat. Clim. Change 8:75–8. doi: 10.1038/s41558-017-0032-64. Tonkin, J. D., Bogan, M. T., Bonada, N., Rios-Touma, B., and Lytle, D. A. 2017.Seasonality and predictability shape temporal species diversity. Ecology98:1201–16. doi: 10.1002/ecy.17615. Simpson, J. E., Slade, E., Riutta, T., and Taylor, M. E. 2012. Factors a ecting soilfauna feeding activity in a fragmented lowland temperate deciduous woodland.PLoS ONE 7:e29616. doi: 10.1371/journal.pone.0029616SUBMITTED: 31 March 2020; ACCEPTED: 27 August 2020;PUBLISHED ONLINE: 08 October 2020.EDITED BY: Helen Phillips, German Centre for Integrative Biodiversity Research(iDiv), GermanyCITATION: Sünnemann M, Siebert J and Eisenhauer N (2020) Double Whammy forLife in Soil? The E ects of Drought and Fertilizer Use. Front. Young Minds 8:547630.doi: 10.3389/frym.2020.547630kids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 7Sünnemann et al. The E ects of Drought and FertilizationCONFLICT OF INTEREST: The authors declare that the research was conducted inthe absence of any commercial or financial relationships that could be construedas a potential conflict of interest.COPYRIGHT © 2020 Sünnemann, Siebert and Eisenhauer. This is an open-accessarticle distributed under the terms of the Creative Commons Attribution License (CCBY). The use, distribution or reproduction in other forums is permitted, providedthe original author(s) and the copyright owner(s) are credited and that the originalpublication in this journal is cited, in accordance with accepted academic practice.No use, distribution or reproduction is permitted which does not comply with theseterms.YOUNG REVIEWERJEDIDIAH, AGE: 14Jedidiah is interested in science and math, particularly in how the environmentimpacts his daily life. He spends time working in the family garden, making moneyby selling eggs and vegetables he helps produce. In his spare time, Jed likes to playbaseball and play video games.AUTHORSMARIE SÜNNEMANNWhen she was 6 years old, her best friend challenged her to a dare: to eatan earthworm. Even though she would not do that today, her curiosity abouteverything that creeps and crawls belowground has never waned. Today, as adoctoral student, she studies the reactions of soil organisms to climate change inmeadows and agricultural fields. In her free time, she does combat sports and enjoysbeing outside. *marie.suennemann@idiv.deJULIA SIEBERTJulia has been fascinated by nature since she was a child. She spent as muchtime as possible outdoors, built moss houses in the forest, and searched for allkinds of animals. She followed this passion by studying biology and communicationscience and was always keen on finding ways to transfer knowledge to di erentaudiences. Her scientific studies focused on how changing climate conditionsa ect soil organisms and the ecosystem functions they drive. Furthermore, sheexplored ways to engage school students in biodiversity science. In her free time,she enjoys horse-riding, traveling, birdwatching, mountain biking, and all sorts ofoutdoor sports.NICO EISENHAUERNico 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 alwaysbeen fascinated by the beauty of nature and driven by the question of why a specificplant or animal species occurs in one place, but not in another. During his study ofkids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 8Sünnemann et al. The E ects of Drought and Fertilizationbiology, he discovered his interest in soil animals and their important activities thatare crucial for the functioning of ecosystems. When not at work, Nico likes playingsoccer and badminton, running, and spending timewith his family and friends.kids.frontiersin.org October 2020 | Volume 08 | Article 547630 | 9

Double Whammy for life in soil?: The effects of drought and fertilizer use

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Double Whammy for life in soil?: The effects of drought and fertilizer use

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