- Email: [email protected]
Fear and below-ground food-webs
Soil Biology & Biochemistry xxx (2016) 1e3
Contents lists available at ScienceDirect
Soil Biology & Biochemistry journal homepage: www.elsevier.com/locate/soilbio
Fear and below-ground food-webs Dror Hawlena*, Moshe Zaguri Risk-Management Ecology Lab, Department of Ecology, Evolution & Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Israel
a r t i c l e i n f o
a b s t r a c t
Article history: Received 1 February 2016 Received in revised form 14 June 2016 Accepted 18 June 2016 Available online xxx
Predator induced trait mediated indirect interactions (TMIIs) are likely the dominant facet of trophic interactions in aboveground food-webs. New research is beginning to show that TMIIs are also important in revealing how soil food-webs (SFWs) regulate biogeochemical processes. We suggest that TMIIs can modify SFW functions by (a) regulating the quantity and nutritional quality of plants and animal production known to drive the SFW, (b) inducing defense phenotypes in soil-organisms, and (c) changing soil environmental conditions. Currently, very few studies have explored the role TMIIs play in shaping SFW functions, especially the cascading effects on SFW dynamics. Much theoretical and empirical research is needed before we can successfully incorporate the non-consumptive effects of predation into SFW models. © 2016 Published by Elsevier Ltd.
Keywords: Ecosystem function Food web interactions Inducible defenses Predator-prey interactions Trait-mediated interactions
1. Main text Food-webs are networks of consumer-resource interactions that shape ecological processes from the individual to the ecosystem levels. Conventionally, food-webs are viewed in terms of direct feeding interactions that trickle down and affect not only community composition but also important ecosystem functions, such as nutrient cycling (Vanni, 2002; Wardle and Bardgett, 2004). Growing evidence shows that natural enemies can additionally regulate ecosystem functions via trait-mediated indirect interactions (TMIIs) (Schmitz et al., 2010). Far from being helpless victims, prey can reduce their probability of being killed by predators by altering phenotypic expressions of behavioral, morphological, physiological and life-history traits (Lima and Dill, 1990; Tollrian and Harvell, 1999; Preisser et al., 2005). Implementation of such inducible defense strategies may interfere with non-emergency functions, and alter the prey’s role in conveying energy and elements up and down the food-web (Hawlena and Schmitz, 2010a). We posit that predator induced TMIIs can shape soil food-web (SFW) functions by 1) altering the nutritionalelemental composition of plant- and animal-derived organic inputs to soils, 2) inducing defense phenotypes in soil-organisms, and 3) changing soil conditions (Fig. 1 Pathways 1e3, respectively).
* Corresponding author. E-mail address: [email protected] (D. Hawlena).
Nutritional-elemental content of organic inputs to soils is an important determinant of SFW structure and function (Wardle et al., 2004; Hattenschwiler et al., 2005; De Deyn et al., 2008). The majority of these inputs are comprised of senesced, uneaten plant-litter, roots, and root exudates (Cebrian, 2004; Pollierer et al., 2007; Pangesti et al., 2013; Jackrel and Wootton, 2015). Thus, it is widely assumed that herbivores primarily affect the way SFWs regulate biogeochemical processes by altering the quantity and quality of plant-derived organics inputs to soils (Bardgett and Wardle, 2010). When threatened by predators, herbivores use defensive behaviors that constrain their dietary choices (reviewed in Brown and Kotler, 2007). Herbivores may also change their diet to consume a higher proportion of digestible carbohydrates needed to fulfill stress induced nutritional demands (Hawlena and Schmitz, 2010a, b). Consequently, predators can regulate the SFW function by causing differential herbivory on various plant species (Fig. 1 Pathway 1a-b). Predator induced dietary deviations may select for plant communities with different characteristics, altering the elemental composition of plant-derived organic inputs to soils (Fig. 1 Pathway 1a). For example, grasshoppers reared under chronic risk of spider predation alter their diet and consume more of the dominant forb Solidgo rugose, whose litter is recalcitrant to decomposition. This dietary change allows other plants to proliferate, increasing plant diversity and increases the detritus nutritional quality and rates of N-mineralization (Schmitz, 2006, 2008).
http://dx.doi.org/10.1016/j.soilbio.2016.06.019 0038-0717/© 2016 Published by Elsevier Ltd.
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019
2
D. Hawlena, M. Zaguri / Soil Biology & Biochemistry xxx (2016) 1e3
Fig. 2. Proposed mechanism by which predator induced changes in nutritional composition of animal carcasses and waste materials can alter subsequent decomposition of the large biomass of plantedetritus inputs to soils. The gray shade represents different nutritional composition (i.e., C:N ratio). Different triangle sizes represent different quantities of detrital inputs and inorganic compound outputs. Fig. 1. Proposed framework by which predator induced TMIIs can be incorporated into existing SFW models. The arrows represent three principle pathways by which predator induced TMIIs can alter SFW function. First, predators can alter the organic inputs to soils (1) by inducing herbivore dietary changes that (1a) select for a different plant community, (1b) induce plant physiological and defense responses, and/or by (1c) altering the quantity and nutritional composition of animal waste and carcasses. Second, aboveground and belowground (dashed frame) predators can induce defense phenotypes in soil-organisms (2). Third, predators can regulate soil conditions (3) by altering the activity and habitat domain of soil organisms (3a), by controlling plant traits via herbivore dietary changes (3b), and by altering animal and plant-derived organic inputs (3c).
Herbivores’ dietary changes in response to predation can additionally regulate the elemental quality of plant-derived organic inputs by altering plant physiology and by inducing chemical and mechanical defenses (Chen, 2008) (Fig. 1, pathways 1b). For instance, grasshoppers stressed by predation enhance plant carbon uptake and slow carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, fear of predation leads to increased carbon retention (Strickland et al., 2013). It is believed that animal waste materials and carcasses merely induce a localized ephemeral effect on SFWs, with little or no effect on ecosystem functioning (Bardgett and Wardle, 2010). This classical view requires revisions (Barton, 2015). Animal carcasses and waste material are rich in protein-N. Protein inputs to soils allow microbial communities to grow and produce extracellular enzymes that catalyze the decomposition of complex substrates into bioavailable products (Schimel et al., 2007). Therefore, animalderived organic inputs to soils may accelerate mineralization of subsequent inputs of much larger quantities of low-quality plantlitter biomass (Hawlena et al., 2012). By doing so, animal carcasses and waste material may generate a mosaic landscape of soil communities that differ in function. Predators can regulate SFW function by altering the nutritional composition of animal-derived organic inputs to soils (Fig. 1 Pathway 1c). Prey physiological stress responses to predation often involve allocation of resources from growth and reproduction to higher energy consuming emergency functions (Hawlena and Schmitz, 2010b). Prey can also allocate resources to develop and support new defense morphologies (e.g., larger tail muscles, and shell or exoskeleton fortifications; Tollrian and Harvell, 1999). Both physiological and morphological defenses can alter the nutritional composition of prey body and waste materials (e.g., Hawlena and Schmitz, 2010a; Dalton and Flecker, 2014; Guariento et al., 2015; Janssens et al., 2015). When decomposed, carcasses and waste materials of stressed animals may affect the SFW differently from those of non-stressed prey (Fig. 2). For instance, grasshoppers stressed by spiders have a higher body carbon-to-nitrogen ratio
than do non-stressed grasshoppers. This change in elemental content does not slow grasshopper decomposition but alters SFW function by decelerating the subsequent decomposition of the much bigger biomass (~140 times more) of plant-litter by 62% (Hawlena et al., 2012). Another way by which predators can affect SFW functions is by inducing defense responses in soil organisms (Fig. 1 pathway 2). Termites respond to ant predation risks by reducing detritus removal rates (Korb and Linsenmair, 2002). Similarly, under risk of spider predation, collembolans decrease their activity, resulting in lower soil N content, and lower soil CO2 flux (Sitvarin and Rypstra, 2014). These effects are, in-part, attributed to cascading effects on microbial respiration and the activities of N-fixers, possibly via mediation of nutrient release from detritus and by consumption of other soil organisms. Interestingly, the collembolans alter behavior in response mostly to pheromones of dead conspecifics (i.e. necromones; Sitvarin et al., 2015), a response that is presumably common to many soil detritivores (Yao et al., 2009). Experimental evidence implies that soil-predator induced TMIIs can substantially affect processes such as N2O emissions from soil (Thakur et al., 2014). For example, the risk of predation can induce bacterial defenses (for review see Jousset, 2012) that may subsequently alter important ecosystem functioning such as decomposition, pollutant degradation and plant productivity. Yet, to the best of our knowledge, the non-consumptive effects of soil-predators on decomposers, and their implications for SFW dynamics and function, have never been specifically explored. Soil food-web structure and function are also regulated by the soil chemical and physical conditions such as soil compaction, pH and water content (Breland and Hansen, 1996; Zak et al., 1999; Rousk et al., 2010). Soil organisms can modulate these conditions by engineering the environment (Anderson, 1995). Thus, attempts of soil organisms to escape predation by shifting their activity to a different habitat domain may alter soil conditions and affect SFW dynamics (Fig. 1 Pathway 3a). For instance, anecic earthworms (Pheretima aspergillum) evade predation by shifting their activity deeper into the soil. This behavioral shift leads to increased soil porosity, and soil-soluble N and total P (Zhao et al., 2013). Similarly, coprophagous beetles respond to elevated predation risk by increasing their tunneling depth, decreasing soil bulk density and increasing water content and soil soluble N, ultimately increasing plant biomass by 28% (Wu et al., 2014, 2015). Plant traits are known to be important determinants of soil conditions including moisture, light, and temperature. Thus, another indirect way by which predators can regulate soil conditions is by controlling plant community composition via herbivore risk-induced dietary deviations (Fig. 1 Pathway 3b). Control over the organic inputs to soils is the
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019
D. Hawlena, M. Zaguri / Soil Biology & Biochemistry xxx (2016) 1e3
third mechanism by which predation can regulate soil environmental conditions (Fig. 1 Pathway 3c). A decade ago, Preisser et al. (2005) demonstrated that intimidation costs, traditionally ignored in predatoreprey ecology, may actually be the dominant facet of trophic interactions in aboveground food-webs. Emerging research indicates that TMIIs are also important in explaining SFW functions. We provide a general framework by which TMIIs can be incorporated into existing SFW concepts. Testing this framework will pose great challenges, requiring scaling individual responses to ecosystem level processes. Moreover, in almost all studies linking TMIIs to ecosystem functioning, the SFW was treated as a black box. This opens the way for exciting new research that could explore how TMIIs trickle through the SFW. Such exploration may force us to adopt a detailed functional approach in an attempt to better understand SFW dynamics and functions. We hope that in ten years, enough data will be available to conclude whether and how TMIIs shape SFW functions. Acknowledgements We would like to acknowledge Yaya Tang and two anonymous reviewers for their invaluable comments, Netta Shamir for the drawings, the members of the risk management ecology lab for stimulating discussions, and the support of a European Research Council grant (ERC-2013-StG- 337023 (ECOSTRESS)) to DH. References Anderson, J.M., 1995. Soil prganisms as engineers: microsite modulation of macroscale processes. In: Jones, C.G., Lawton, J.H. (Eds.), Linking Species and Ecosystems. Chapman & Hall, London, pp. 94e106. Bardgett, R.D., Wardle, D.A., 2010. Aboveground-belowground Linkages. Oxford University Press, Oxford. Barton, P.S., 2015. The role of carrion in ecosystems. In: Benbow, M.E., Tomberlin, J.K., Tarone, A.M. (Eds.), Carrion Ecology, Evolution, and Their Applications. CRC Press, Boca Raton, FL, pp. 273e292. Breland, T.A., Hansen, S., 1996. Nitrogen mineralization and microbial biomass as affected by soil compaction. Soil Biol. Biochem. 28, 655e663. Brown, J.S., Kotler, B.P., 2007. Foraging and the ecology of fear. In: Stephen, D.W., Brown, J.S., Ydenberg, R.C. (Eds.), Foraging: Behavior and Ecology. The University of Chicago Press, Chicago, IL, pp. 437e480. Cebrian, J., 2004. Role of first-order consumers in ecosystem carbon flow. Ecol. Lett. 7, 232e240. Chen, M.-S., 2008. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15, 101e114. Dalton, C.M., Flecker, A.S., 2014. Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems. Oecologia 176, 691e701. De Deyn, G.B., Cornelissen, J.H.C., Bardgett, R.D., 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol. Lett. 11, 516e531. Guariento, R.D., Carneiro, L.S., Jorge, J.S., Borges, A.N., Esteves, F.A., Caliman, A., 2015. Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey. Ecol. Evol. 5, 4747e4756. Hattenschwiler, S., Tiunov, A.V., Scheu, S., 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 36, 191e218. Hawlena, D., Schmitz, O.J., 2010a. Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc. Natl. Acad. Sci. U. S. A. 107, 15503e15507. Hawlena, D., Schmitz, O.J., 2010b. Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am. Nat. 176, 537e556. Hawlena, D., Strickland, M.S., Bradford, M.A., Schmitz, O.J., 2012. Fear of predation
3
slows plant-litter decomposition. Science 336, 1434e1438. Jackrel, S.L., Wootton, J.T., 2015. Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function. Proc. R. Soc. B Biol. Sci. 282. Janssens, L., Van Dievel, M., Stoks, R., 2015. Warming reinforces nonconsumptive predator effects on prey growth, physiology, and body stoichiometry. Ecology 96, 3270e3280. Jousset, A., 2012. Ecological and evolutive implications of bacterial defences against predators. Environ. Microbiol. 14, 1830e1843. Korb, J., Linsenmair, K.E., 2002. Evaluation of predation risk in the collectively foraging termite Macrotermes bellicosus. Insectes Sociaux 49, 264e269. Lima, S.L., Dill, L.M., 1990. Behavioral decisions made under the risk of predation - a review and prospectus. Can. J. Zoology -Revue Can. De Zoologie 68, 619e640. Pangesti, N., Pineda, A., Pieterse, C.M.J., Dicke, M., van Loon, J.J.A., 2013. Two-way plant-mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front. Plant Sci. 4. Pollierer, M.M., Langel, R., Koerner, C., Maraun, M., Scheu, S., 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol. Lett. 10, 729e736. Preisser, E.L., Bolnick, D.I., Benard, M.F., 2005. Scared to death? the effects of intimidation and consumption in predator-prey interactions. Ecology 86, 501e509. Rousk, J., Baath, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. Isme J. 4, 1340e1351. Schimel, J., Balser, T.C., Wallenstein, M., 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386e1394. Schmitz, O.J., 2006. Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. Ecology 87, 1432e1437. Schmitz, O.J., 2008. Effects of predator hunting mode on grassland ecosystem function. Science 319, 952e954. Schmitz, O.J., Hawlena, D., Trussell, G.C., 2010. Predator control of ecosystem nutrient dynamics. Ecol. Lett. 13, 1199e1209. Sitvarin, M.I., Romanchek, C., Rypstra, A.L., 2015. Nonconsumptive predatoreprey interactions: sensitivity of the detritivore Sinella curviseta (Collembola: entomobryidae) to cues of predation risk from the spider Pardosa milvina (Araneae: lycosidae). Environ. Entomol. 44, 349e355. Sitvarin, M.I., Rypstra, A.L., 2014. Fear of predation alters soil carbon dioxide flux and nitrogen content. Biol. Lett. 10. Strickland, M.S., Hawlena, D., Reese, A., Bradford, M.A., Schmitz, O.J., 2013. Trophic cascade alters ecosystem carbon exchange. Proc. Natl. Acad. Sci. U. S. A. 110, 11035e11038. Thakur, M.P., van Groenigen, J.W., Kuiper, I., De Deyn, G.B., 2014. Interactions between microbial-feeding and predatory soil fauna trigger N2O emissions. Soil Biol. Biochem. 70, 256e262. Tollrian, R., Harvell, C.D., 1999. The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, New Jersey. Vanni, M.J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annu. Rev. Ecol. Syst. 33, 341e370. Wardle, D.A., Bardgett, R.D., 2004. Human-induced changes in large herbivorous mammal density: the consequences for decomposers. Front. Ecol. Environ. 2, 145e153. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629e1633. Wu, X., Griffin, J.N., Sun, S., 2014. Cascading effects of predator-detritivore interactions depend on environmental context in a Tibetan alpine meadow. J. Animal Ecol. 83, 546e556. Wu, X., Griffin, J.N., Xi, X., Sun, S., 2015. The sign of cascading predator effects varies with prey traits in a detrital system. J. Animal Ecol. 84, 1610e1617. Yao, M., Rosenfeld, J., Attridge, S., Sidhu, S., Aksenov, V., Rollo, C.D., 2009. The ancient chemistry of avoiding risks of predation and disease. Evol. Biol. 36, 267e281. Zak, D.R., Holmes, W.E., MacDonald, N.W., Pregitzer, K.S., 1999. Soil temperature, matric potential, and the kinetics of microbial respiration and nitrogen mineralization. Soil Sci. Soc. Am. J. 63, 575e584. Zhao, C., Griffin, J.N., Wu, X., Sun, S., 2013. Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. J. Animal Ecol. 82, 749e758.
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019
Contents lists available at ScienceDirect
Soil Biology & Biochemistry journal homepage: www.elsevier.com/locate/soilbio
Fear and below-ground food-webs Dror Hawlena*, Moshe Zaguri Risk-Management Ecology Lab, Department of Ecology, Evolution & Behavior, The Alexander Silberman Institute of Life Sciences, The Hebrew University of Jerusalem, Israel
a r t i c l e i n f o
a b s t r a c t
Article history: Received 1 February 2016 Received in revised form 14 June 2016 Accepted 18 June 2016 Available online xxx
Predator induced trait mediated indirect interactions (TMIIs) are likely the dominant facet of trophic interactions in aboveground food-webs. New research is beginning to show that TMIIs are also important in revealing how soil food-webs (SFWs) regulate biogeochemical processes. We suggest that TMIIs can modify SFW functions by (a) regulating the quantity and nutritional quality of plants and animal production known to drive the SFW, (b) inducing defense phenotypes in soil-organisms, and (c) changing soil environmental conditions. Currently, very few studies have explored the role TMIIs play in shaping SFW functions, especially the cascading effects on SFW dynamics. Much theoretical and empirical research is needed before we can successfully incorporate the non-consumptive effects of predation into SFW models. © 2016 Published by Elsevier Ltd.
Keywords: Ecosystem function Food web interactions Inducible defenses Predator-prey interactions Trait-mediated interactions
1. Main text Food-webs are networks of consumer-resource interactions that shape ecological processes from the individual to the ecosystem levels. Conventionally, food-webs are viewed in terms of direct feeding interactions that trickle down and affect not only community composition but also important ecosystem functions, such as nutrient cycling (Vanni, 2002; Wardle and Bardgett, 2004). Growing evidence shows that natural enemies can additionally regulate ecosystem functions via trait-mediated indirect interactions (TMIIs) (Schmitz et al., 2010). Far from being helpless victims, prey can reduce their probability of being killed by predators by altering phenotypic expressions of behavioral, morphological, physiological and life-history traits (Lima and Dill, 1990; Tollrian and Harvell, 1999; Preisser et al., 2005). Implementation of such inducible defense strategies may interfere with non-emergency functions, and alter the prey’s role in conveying energy and elements up and down the food-web (Hawlena and Schmitz, 2010a). We posit that predator induced TMIIs can shape soil food-web (SFW) functions by 1) altering the nutritionalelemental composition of plant- and animal-derived organic inputs to soils, 2) inducing defense phenotypes in soil-organisms, and 3) changing soil conditions (Fig. 1 Pathways 1e3, respectively).
* Corresponding author. E-mail address: [email protected] (D. Hawlena).
Nutritional-elemental content of organic inputs to soils is an important determinant of SFW structure and function (Wardle et al., 2004; Hattenschwiler et al., 2005; De Deyn et al., 2008). The majority of these inputs are comprised of senesced, uneaten plant-litter, roots, and root exudates (Cebrian, 2004; Pollierer et al., 2007; Pangesti et al., 2013; Jackrel and Wootton, 2015). Thus, it is widely assumed that herbivores primarily affect the way SFWs regulate biogeochemical processes by altering the quantity and quality of plant-derived organics inputs to soils (Bardgett and Wardle, 2010). When threatened by predators, herbivores use defensive behaviors that constrain their dietary choices (reviewed in Brown and Kotler, 2007). Herbivores may also change their diet to consume a higher proportion of digestible carbohydrates needed to fulfill stress induced nutritional demands (Hawlena and Schmitz, 2010a, b). Consequently, predators can regulate the SFW function by causing differential herbivory on various plant species (Fig. 1 Pathway 1a-b). Predator induced dietary deviations may select for plant communities with different characteristics, altering the elemental composition of plant-derived organic inputs to soils (Fig. 1 Pathway 1a). For example, grasshoppers reared under chronic risk of spider predation alter their diet and consume more of the dominant forb Solidgo rugose, whose litter is recalcitrant to decomposition. This dietary change allows other plants to proliferate, increasing plant diversity and increases the detritus nutritional quality and rates of N-mineralization (Schmitz, 2006, 2008).
http://dx.doi.org/10.1016/j.soilbio.2016.06.019 0038-0717/© 2016 Published by Elsevier Ltd.
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019
2
D. Hawlena, M. Zaguri / Soil Biology & Biochemistry xxx (2016) 1e3
Fig. 2. Proposed mechanism by which predator induced changes in nutritional composition of animal carcasses and waste materials can alter subsequent decomposition of the large biomass of plantedetritus inputs to soils. The gray shade represents different nutritional composition (i.e., C:N ratio). Different triangle sizes represent different quantities of detrital inputs and inorganic compound outputs. Fig. 1. Proposed framework by which predator induced TMIIs can be incorporated into existing SFW models. The arrows represent three principle pathways by which predator induced TMIIs can alter SFW function. First, predators can alter the organic inputs to soils (1) by inducing herbivore dietary changes that (1a) select for a different plant community, (1b) induce plant physiological and defense responses, and/or by (1c) altering the quantity and nutritional composition of animal waste and carcasses. Second, aboveground and belowground (dashed frame) predators can induce defense phenotypes in soil-organisms (2). Third, predators can regulate soil conditions (3) by altering the activity and habitat domain of soil organisms (3a), by controlling plant traits via herbivore dietary changes (3b), and by altering animal and plant-derived organic inputs (3c).
Herbivores’ dietary changes in response to predation can additionally regulate the elemental quality of plant-derived organic inputs by altering plant physiology and by inducing chemical and mechanical defenses (Chen, 2008) (Fig. 1, pathways 1b). For instance, grasshoppers stressed by predation enhance plant carbon uptake and slow carbon loss via ecosystem respiration and reallocation of carbon among plant aboveground and belowground tissues. Consequently, fear of predation leads to increased carbon retention (Strickland et al., 2013). It is believed that animal waste materials and carcasses merely induce a localized ephemeral effect on SFWs, with little or no effect on ecosystem functioning (Bardgett and Wardle, 2010). This classical view requires revisions (Barton, 2015). Animal carcasses and waste material are rich in protein-N. Protein inputs to soils allow microbial communities to grow and produce extracellular enzymes that catalyze the decomposition of complex substrates into bioavailable products (Schimel et al., 2007). Therefore, animalderived organic inputs to soils may accelerate mineralization of subsequent inputs of much larger quantities of low-quality plantlitter biomass (Hawlena et al., 2012). By doing so, animal carcasses and waste material may generate a mosaic landscape of soil communities that differ in function. Predators can regulate SFW function by altering the nutritional composition of animal-derived organic inputs to soils (Fig. 1 Pathway 1c). Prey physiological stress responses to predation often involve allocation of resources from growth and reproduction to higher energy consuming emergency functions (Hawlena and Schmitz, 2010b). Prey can also allocate resources to develop and support new defense morphologies (e.g., larger tail muscles, and shell or exoskeleton fortifications; Tollrian and Harvell, 1999). Both physiological and morphological defenses can alter the nutritional composition of prey body and waste materials (e.g., Hawlena and Schmitz, 2010a; Dalton and Flecker, 2014; Guariento et al., 2015; Janssens et al., 2015). When decomposed, carcasses and waste materials of stressed animals may affect the SFW differently from those of non-stressed prey (Fig. 2). For instance, grasshoppers stressed by spiders have a higher body carbon-to-nitrogen ratio
than do non-stressed grasshoppers. This change in elemental content does not slow grasshopper decomposition but alters SFW function by decelerating the subsequent decomposition of the much bigger biomass (~140 times more) of plant-litter by 62% (Hawlena et al., 2012). Another way by which predators can affect SFW functions is by inducing defense responses in soil organisms (Fig. 1 pathway 2). Termites respond to ant predation risks by reducing detritus removal rates (Korb and Linsenmair, 2002). Similarly, under risk of spider predation, collembolans decrease their activity, resulting in lower soil N content, and lower soil CO2 flux (Sitvarin and Rypstra, 2014). These effects are, in-part, attributed to cascading effects on microbial respiration and the activities of N-fixers, possibly via mediation of nutrient release from detritus and by consumption of other soil organisms. Interestingly, the collembolans alter behavior in response mostly to pheromones of dead conspecifics (i.e. necromones; Sitvarin et al., 2015), a response that is presumably common to many soil detritivores (Yao et al., 2009). Experimental evidence implies that soil-predator induced TMIIs can substantially affect processes such as N2O emissions from soil (Thakur et al., 2014). For example, the risk of predation can induce bacterial defenses (for review see Jousset, 2012) that may subsequently alter important ecosystem functioning such as decomposition, pollutant degradation and plant productivity. Yet, to the best of our knowledge, the non-consumptive effects of soil-predators on decomposers, and their implications for SFW dynamics and function, have never been specifically explored. Soil food-web structure and function are also regulated by the soil chemical and physical conditions such as soil compaction, pH and water content (Breland and Hansen, 1996; Zak et al., 1999; Rousk et al., 2010). Soil organisms can modulate these conditions by engineering the environment (Anderson, 1995). Thus, attempts of soil organisms to escape predation by shifting their activity to a different habitat domain may alter soil conditions and affect SFW dynamics (Fig. 1 Pathway 3a). For instance, anecic earthworms (Pheretima aspergillum) evade predation by shifting their activity deeper into the soil. This behavioral shift leads to increased soil porosity, and soil-soluble N and total P (Zhao et al., 2013). Similarly, coprophagous beetles respond to elevated predation risk by increasing their tunneling depth, decreasing soil bulk density and increasing water content and soil soluble N, ultimately increasing plant biomass by 28% (Wu et al., 2014, 2015). Plant traits are known to be important determinants of soil conditions including moisture, light, and temperature. Thus, another indirect way by which predators can regulate soil conditions is by controlling plant community composition via herbivore risk-induced dietary deviations (Fig. 1 Pathway 3b). Control over the organic inputs to soils is the
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019
D. Hawlena, M. Zaguri / Soil Biology & Biochemistry xxx (2016) 1e3
third mechanism by which predation can regulate soil environmental conditions (Fig. 1 Pathway 3c). A decade ago, Preisser et al. (2005) demonstrated that intimidation costs, traditionally ignored in predatoreprey ecology, may actually be the dominant facet of trophic interactions in aboveground food-webs. Emerging research indicates that TMIIs are also important in explaining SFW functions. We provide a general framework by which TMIIs can be incorporated into existing SFW concepts. Testing this framework will pose great challenges, requiring scaling individual responses to ecosystem level processes. Moreover, in almost all studies linking TMIIs to ecosystem functioning, the SFW was treated as a black box. This opens the way for exciting new research that could explore how TMIIs trickle through the SFW. Such exploration may force us to adopt a detailed functional approach in an attempt to better understand SFW dynamics and functions. We hope that in ten years, enough data will be available to conclude whether and how TMIIs shape SFW functions. Acknowledgements We would like to acknowledge Yaya Tang and two anonymous reviewers for their invaluable comments, Netta Shamir for the drawings, the members of the risk management ecology lab for stimulating discussions, and the support of a European Research Council grant (ERC-2013-StG- 337023 (ECOSTRESS)) to DH. References Anderson, J.M., 1995. Soil prganisms as engineers: microsite modulation of macroscale processes. In: Jones, C.G., Lawton, J.H. (Eds.), Linking Species and Ecosystems. Chapman & Hall, London, pp. 94e106. Bardgett, R.D., Wardle, D.A., 2010. Aboveground-belowground Linkages. Oxford University Press, Oxford. Barton, P.S., 2015. The role of carrion in ecosystems. In: Benbow, M.E., Tomberlin, J.K., Tarone, A.M. (Eds.), Carrion Ecology, Evolution, and Their Applications. CRC Press, Boca Raton, FL, pp. 273e292. Breland, T.A., Hansen, S., 1996. Nitrogen mineralization and microbial biomass as affected by soil compaction. Soil Biol. Biochem. 28, 655e663. Brown, J.S., Kotler, B.P., 2007. Foraging and the ecology of fear. In: Stephen, D.W., Brown, J.S., Ydenberg, R.C. (Eds.), Foraging: Behavior and Ecology. The University of Chicago Press, Chicago, IL, pp. 437e480. Cebrian, J., 2004. Role of first-order consumers in ecosystem carbon flow. Ecol. Lett. 7, 232e240. Chen, M.-S., 2008. Inducible direct plant defense against insect herbivores: a review. Insect Sci. 15, 101e114. Dalton, C.M., Flecker, A.S., 2014. Metabolic stoichiometry and the ecology of fear in Trinidadian guppies: consequences for life histories and stream ecosystems. Oecologia 176, 691e701. De Deyn, G.B., Cornelissen, J.H.C., Bardgett, R.D., 2008. Plant functional traits and soil carbon sequestration in contrasting biomes. Ecol. Lett. 11, 516e531. Guariento, R.D., Carneiro, L.S., Jorge, J.S., Borges, A.N., Esteves, F.A., Caliman, A., 2015. Interactive effects of predation risk and conspecific density on the nutrient stoichiometry of prey. Ecol. Evol. 5, 4747e4756. Hattenschwiler, S., Tiunov, A.V., Scheu, S., 2005. Biodiversity and litter decomposition in terrestrial ecosystems. Annu. Rev. Ecol. Evol. Syst. 36, 191e218. Hawlena, D., Schmitz, O.J., 2010a. Herbivore physiological response to predation risk and implications for ecosystem nutrient dynamics. Proc. Natl. Acad. Sci. U. S. A. 107, 15503e15507. Hawlena, D., Schmitz, O.J., 2010b. Physiological stress as a fundamental mechanism linking predation to ecosystem functioning. Am. Nat. 176, 537e556. Hawlena, D., Strickland, M.S., Bradford, M.A., Schmitz, O.J., 2012. Fear of predation
3
slows plant-litter decomposition. Science 336, 1434e1438. Jackrel, S.L., Wootton, J.T., 2015. Cascading effects of induced terrestrial plant defences on aquatic and terrestrial ecosystem function. Proc. R. Soc. B Biol. Sci. 282. Janssens, L., Van Dievel, M., Stoks, R., 2015. Warming reinforces nonconsumptive predator effects on prey growth, physiology, and body stoichiometry. Ecology 96, 3270e3280. Jousset, A., 2012. Ecological and evolutive implications of bacterial defences against predators. Environ. Microbiol. 14, 1830e1843. Korb, J., Linsenmair, K.E., 2002. Evaluation of predation risk in the collectively foraging termite Macrotermes bellicosus. Insectes Sociaux 49, 264e269. Lima, S.L., Dill, L.M., 1990. Behavioral decisions made under the risk of predation - a review and prospectus. Can. J. Zoology -Revue Can. De Zoologie 68, 619e640. Pangesti, N., Pineda, A., Pieterse, C.M.J., Dicke, M., van Loon, J.J.A., 2013. Two-way plant-mediated interactions between root-associated microbes and insects: from ecology to mechanisms. Front. Plant Sci. 4. Pollierer, M.M., Langel, R., Koerner, C., Maraun, M., Scheu, S., 2007. The underestimated importance of belowground carbon input for forest soil animal food webs. Ecol. Lett. 10, 729e736. Preisser, E.L., Bolnick, D.I., Benard, M.F., 2005. Scared to death? the effects of intimidation and consumption in predator-prey interactions. Ecology 86, 501e509. Rousk, J., Baath, E., Brookes, P.C., Lauber, C.L., Lozupone, C., Caporaso, J.G., Knight, R., Fierer, N., 2010. Soil bacterial and fungal communities across a pH gradient in an arable soil. Isme J. 4, 1340e1351. Schimel, J., Balser, T.C., Wallenstein, M., 2007. Microbial stress-response physiology and its implications for ecosystem function. Ecology 88, 1386e1394. Schmitz, O.J., 2006. Predators have large effects on ecosystem properties by changing plant diversity, not plant biomass. Ecology 87, 1432e1437. Schmitz, O.J., 2008. Effects of predator hunting mode on grassland ecosystem function. Science 319, 952e954. Schmitz, O.J., Hawlena, D., Trussell, G.C., 2010. Predator control of ecosystem nutrient dynamics. Ecol. Lett. 13, 1199e1209. Sitvarin, M.I., Romanchek, C., Rypstra, A.L., 2015. Nonconsumptive predatoreprey interactions: sensitivity of the detritivore Sinella curviseta (Collembola: entomobryidae) to cues of predation risk from the spider Pardosa milvina (Araneae: lycosidae). Environ. Entomol. 44, 349e355. Sitvarin, M.I., Rypstra, A.L., 2014. Fear of predation alters soil carbon dioxide flux and nitrogen content. Biol. Lett. 10. Strickland, M.S., Hawlena, D., Reese, A., Bradford, M.A., Schmitz, O.J., 2013. Trophic cascade alters ecosystem carbon exchange. Proc. Natl. Acad. Sci. U. S. A. 110, 11035e11038. Thakur, M.P., van Groenigen, J.W., Kuiper, I., De Deyn, G.B., 2014. Interactions between microbial-feeding and predatory soil fauna trigger N2O emissions. Soil Biol. Biochem. 70, 256e262. Tollrian, R., Harvell, C.D., 1999. The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, New Jersey. Vanni, M.J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annu. Rev. Ecol. Syst. 33, 341e370. Wardle, D.A., Bardgett, R.D., 2004. Human-induced changes in large herbivorous mammal density: the consequences for decomposers. Front. Ecol. Environ. 2, 145e153. Wardle, D.A., Bardgett, R.D., Klironomos, J.N., Setala, H., van der Putten, W.H., Wall, D.H., 2004. Ecological linkages between aboveground and belowground biota. Science 304, 1629e1633. Wu, X., Griffin, J.N., Sun, S., 2014. Cascading effects of predator-detritivore interactions depend on environmental context in a Tibetan alpine meadow. J. Animal Ecol. 83, 546e556. Wu, X., Griffin, J.N., Xi, X., Sun, S., 2015. The sign of cascading predator effects varies with prey traits in a detrital system. J. Animal Ecol. 84, 1610e1617. Yao, M., Rosenfeld, J., Attridge, S., Sidhu, S., Aksenov, V., Rollo, C.D., 2009. The ancient chemistry of avoiding risks of predation and disease. Evol. Biol. 36, 267e281. Zak, D.R., Holmes, W.E., MacDonald, N.W., Pregitzer, K.S., 1999. Soil temperature, matric potential, and the kinetics of microbial respiration and nitrogen mineralization. Soil Sci. Soc. Am. J. 63, 575e584. Zhao, C., Griffin, J.N., Wu, X., Sun, S., 2013. Predatory beetles facilitate plant growth by driving earthworms to lower soil layers. J. Animal Ecol. 82, 749e758.
Please cite this article in press as: Hawlena, D., Zaguri, M., Fear and below-ground food-webs, Soil Biology & Biochemistry (2016), http:// dx.doi.org/10.1016/j.soilbio.2016.06.019